LARVAE OF

NARINE BIVALVES
AND
ECHINODERNS

V.L. KASYANOV® G.A. KRYUCHKOVA
V.A. KULIKOVA® L.A. MEDVEDEVA

Scientific Editor
David L. Pawson

LARVAE OF MARINE BIVALVES
AND
ECHINODERMS

V.L. KASYANOV, G.A. KRYUCHKOVA,
V.A. KULIKOVA AND L. A. MEDVEDEVA

Scientific Editor

David L. Pawson

SMITHSONIAN INSTITUTION LIBRARIES
Washington, D.C.
1998

Smin B87-101

Lichinki morskikh dvustvorchatykh
mollyuskov : iglokozhikh

Akademiya Nauk SSSR
Dal’nevostochnyi Nauchnyi Tsentr
Institut Biologii Morya

Nauka Publishers,
Moscow, 1983 (Revised 1990)

Translated from the Russian

© 1998, Oxonian Press Pvt. Ltd., New Delhi

Library of Congress Cataloging-in-Publication Data

Lichinki morskikh dvustvorchatykh molliuskov i iglokozhikh. English Larvae
of marine bivalves and echinoderms/V.L. Kasyanov .. . [et al.]; scientific
editor David L. Pawson.

. “em.

Includes bibliographical references.

1. Bivalvia — Larvae — Classification. 2. Echinodermata — Larvae —
Classification. 3. Mollusks — Larvae — Classification. 4. Bivalvia — Lar-
vae. 5. Echinodermata — Larvae. 6. Mollusks — Larvae.

I. Kas’ianov, V.L. II. Pawson, David L. (David Leo), 1938-III. Title.
QL430.6.L5313 1997 96-49571
594’.4139°0916454 — dc21 CIP

Translated and published under an agreement, for the Smithsonian Institution
Libraries, Washington, D.C., by Amerind Publishing Co. Pvt. Ltd., 66 Janpath,
New Delhi 110001

Printed at Baba Barkha Nath Printers, 26/7, Najafgarh Road Industrial Area,
New Delhi — 110 015.

WDE 5913

This book describes larvae of bivalves and echinoderms, living in the Sea
of Japan, which are or may be economically important, and where adult forms
are dominant in benthic communities. Descriptions of 18 species of bivalves
and 10 species of echinoderms are given, and keys are provided for the iden-
tification of planktotrophic larvae of bivalves and echinoderms to the family
level. Information on identified species is preceded by a description of the
morphology, physiology, and behavior of larvae of the given classes.

The book is addressed to marine biologists, embryologists, zoologists, and
specialists engaged in fisheries.

DEAD as
eee

FOREWORD TO THE ENGLISH EDITION

The Smithsonian Institution Libraries, in cooperation with the National Science
Foundation, has sponsored the translation into English of this and hundreds
of other scientific and scholarly studies since 1960. The program, funded with
Special Foreign Currency under the provisions of Public Law 480, represents
an investment in the dissemination of knowledge to which the Smithsonian
Institution is dedicated.

In this volume, the authors review and summarize many aspects of the
early life history of the marine bivalve mollusks and echinoderms that are
common in the Sea of Japan. Several of the species covered are of commercial
value, and the scientific information given here will be very useful in planning
successful exploitation and management. Many of these species have a wide
distribution in the Northern Hemisphere, and thus the book is of broad regional
interest.

For many readers, this English-language translation presents for the first
time a review of Russian research on mollusks and echinoderms that would be
otherwise inaccessible. It updates a 1980 book (in Russian) by V.L. Kasyanov,
L.A. Medvedeva, Y.M. Yakovlev and S.N. Yakovlev, and it includes relevant
literature references up to, and including, the year 1990. The editors have taken
great care to ensure that this translation accurately reflects the original text.
However, some scientific names and parts of the classification, especially in
the Echinodermata section, have been changed to reflect current thinking, and
to make the data more readily accessible.

This work is a significant addition to the literature on embryology and
larval development of mollusks and echinoderms, and it should prove to be
important and useful to fishery biologists, embryologists and marine biologists.

DAVID L. PAWSON

National Museum of Natural History
Smithsonian Institution

Washington, D.C.

is hau hel
fe Peal

RN

CONTENTS

FOREWORD TO THE ENGLISH EDITION
INTRODUCTION

CHAPTER I. LARVAE OF MARINE BIVALVES (MORPHOLOGY,
PHYSIOLOGY AND BEHAVIOR)

Identification of Pelagic Larvae of Bivalves

Pacific Mussel, Mytilus trossulus Gould

Crenomytilus grayanus (Dinker)

Long-bristled Modiolus, Modiolus difficilis
(Kuroda and Habe)

Musculista senhousia (Benson)

Crescent-shaped Adula, Adula falcatoides Habe

Boucard’s Arca, Arca boucardi Jousseaume

Giant Oyster, Crassostrea gigas Thiinberg

Chlamys farreri nipponensis Kuroda

Swiftopecten swifti (Bernard)

Mizuhopecten yessoensis (Jay)

Hiatella arctica Linné

Kellia japonica Pilsbry

Keenocardium californiense (Deshayes)

Baltic Macoma, Macoma balthica (Linné)

Tall Siliqua, Siliqua alta (Broderip and Sowerby)

Razor Clam, Solen krusensterni Schrenck

Chinese Mactra, Mactra chinensis Philippi

Spisula sachalinensis (Schrenk)

Philippine Ruditapes, Ruditapes philippinarum (Adams
and Reeve)

Vill

Mya japonica Jay

Truncate Mya, Mya truncata (Linnaeus)
Shipworm, Teredo navalis Linné

Bankia setacea (Tyron)

Crispate Zirphaea, Zirfaea crispata (Linné)
Japanese Barnea, Barnea japonica (Yokoyama)

CHAPTER II. LARVAE OF SEA STARS (MORPHOLOGY,
PHYSIOLOGY, BEHAVIOR)

Identification of Pelagic Larvae of Sea Stars
Patiria pectinifera (Miller and Troschel)
Asterias amurensis Litken

CHAPTER III. LARVAE OF SEA URCHINS (MORPHOLOGY,
PHYSIOLOGY, AND BEHAVIOR)

Identification of Pelagic Larvae of Sea Urchins
Strongylocentrotus nudus Agassiz
Strongylocentrotus intermedius (Agassiz)
Echinarachinus parma (Lamarck)
Scaphechinus mirabilis (Agassiz)

Scaphechinus griseus (Mortensen)
Echinocardium cordatum (Pennant)

CHAPTER IV. LARVAE OF BRITTLE STARS (MORPHOLOGY,
PHYSIOLOGY, AND BEHAVIOR)
Identification of Pelagic Larvae of Brittle Stars
Ophiura sarsi Liitken
Amphipholis kochii Litken

CHAPTER V. LARVAE OF SEA CUCUMBERS (MORPHOLOGY,

PHYSIOLOGY, AND BEHAVIOR)
Identification of Pelagic Larvae of Sea Cucumbers
Far Eastern Trepang, Stichopus japonicus Selenka
Japanese Cucumaria, Cucumaria japonica Semper
Fraudulent Eupentacta, Eupentacta fraudatrix
(Djakonov and Baranova)

CONCLUSION
REFERENCES

OF
98
99
101
102
103

104

W227)
152
134

138

170
177
179
182
185
187
190

195

216
2A
225

225
244
246

251
PISS)

PES)
258

INTRODUCTION

The life cycles of commercially exploited and cultured mollusks and echino-
derms comprise, in most cases, a prolonged benthic period and a brief pelagic
period. In the benthic period the animal feeds, grows, attains sexual maturity,
produces gametes, and participates in reproduction. The prodyction of gametes
(gametogenesis) and their subsequent release and fertilization by mollusks and
echinoderms inhabiting temperate waters usually occurs every year. The an-
nual reproductive processes in bivalves and echinoderms inhabiting the Sea of
Japan were described earlier by researchers in the Laboratory of Embryology,
Institute of Marine Biology [Razmnozhenie iglokozhikh i dvustvorchatykh
mollyuskov (Reproduction of Echinoderms and Bivalves), Kasyanov et al.,
1980]. The present book is a continuation of the 1980 publication. Here we
describe the larvae of bivalves, sea stars, sea urchins, brittle stars, and sea
cucumbers of the Sea of Japan, which are economically important or abundant
forms in benthic communities. The larvae of these species are planktonic, feed
on phytoplankton, grow, and are carried out to sea by currents. Then they
migrate from the surface to the bottom, settle there, and metamorphose, thus
completing the pelagic period of their life cycle. This period is less known and
understood than the benthic, even though many papers and books deal with the
subject. Among such works, mention should be made of those by Thorson
(1936, 1946, 1950), Mortensen (1921, 1937, 1938), Mileikovskii (1977, 1981),
and Jagersten (1972). The structure of the larvae discussed here have been
examined by O.M. Ivanova-Kazas in her two-volume work on the embryology
of mollusks and echinoderms (Ivanova-Kazas, 1977, 1978).

Particular attention is paid in the present book to those characters which
make possible the determination of the species affinities of larvae. Thus 18
species of bivalves and 10 species of echinoderms are described in detail, and
keys are provided to enable identification to family level of planktotrophic
larvae of bivalves and echinoderms from Peter the Great Bay. The descriptions
of the larvae are preceded by descriptions of the morphology, physiology, and

2

behavior of the larvae of individual classes, based on published and original
material. Larvae are examined not so much from an embryological point of
view (as a developmental stage of a definitive animal), but from a zoological
viewpoint (as an organism endowed with all the systems required for a viable
existence in the plankton). The general description of the larvae studied begins
with a brief report on early development (up to the stage of trochophore or
dipleurula). Cytoembryological aspects of early development are not described
because extensive literature is available on this topic. The description con-
cludes with a summary of the process of metamorphosis and a brief charac-
terization of lecithotrophic larvae. Ecological aspects of the pelagic life of
larvae and their settling to the bottom are not described due to space con-
straints of this book.

Plankton samples were collected mainly in Vostok Bay, which is situated
in the eastern part of Peter the Great Bay of the Sea of Japan. To obtain the
required stage of larval development, artificial fertilization with subsequent
culturing of larvae was done, in addition to selection of larvae from plankton
samples and subsequent culturing. This work was carried out under the guid-
ance of V.L. Kasyanov, assisted by S.Sh. Dautov, who described the larvae of
the sea star Asterias amurensis and compiled Table 5 (Types of Development
of Sea Stars). ;

The authors are grateful to V.A. Sveshnikov, the editor-in-chief of this
volume, to V.V. Malakhov and V.G. Chavtur for excellent advice, and to O.M.
Korn, T.I. Ponurovskaya, T.N. Chernenko, and the staff in the photographic
laboratory of the Institute of Marine Biology who assisted in manuscript prepa-
ration. We thank the corresponding member of the Academy of Sciences,
USSR, A.V. Zhirmunskii, the entire staff of the Laboratory of Embryology,
Mrs. Irina Barsegova and Mrs. Tatiana Kotnova for their support during this
endeavor. Collection of material and its analysis was partially financed by
TINRO MRKhi* of the USSR. The authors are grateful to Mr. Gulab Primlani
and Oxonian Press for translating their book into English.

In the new edition we have introduced corrections and additions. The list
of species described in the book has been enlarged, new illustrations have been
added, and species sections have been rewritten. It is hoped that through this
English language edition the book will reach a new circle of readers.

V. Kasyanov

* Pacific Scientific Research Institute of Fisheries and Oceanography, Ministry of Fisheries—
General Editor.

CHAPTER 1

LARVAE OF MARINE BIVALVES
(MORPHOLOGY, PHYSIOLOGY,
AND BEHAVIOR)

EARLY DEVELOPMENT

The development of bivalves has been best studied in Dreissena polymorpha,
a species inhabiting fresh and brackish waters and exhibiting a development
typical for marine bivalves (Meisenheimer, 1901); in Unionidae—freshwater
mollusks endowed as larvae, at the glochidium stage, with an adaptation to
temporary parasitism (Lillie, 1895); and in Crassostrea gigas —a marine bi-
valve in which the larva is a typical veliger (Fujita, 1929).

Egg

The eggs of bivalves contain relatively little yolk, which is uniformly
distributed throughout the egg cell. The position of an animal pole is indicated
by the extrusion of polar bodies in the egg cell. Bivalve eggs have a diameter
of 40-360 tm. Like the eggs of other Bilateria with external fertilization, they
are surrounded by a vitelline and a jellylike membrane. The thickness of the
vitelline membrane is 1—2 tm; the thickness of the jellylike membrane may
be more than 10 um. The jellylike membrane is generally transparent, delicate,
and is poorly defined after fixation (Drozdov and Kasyanov, 1985b). The eggs
have a jellylike membrane in addition to the vitelline one (Allen, 1953, 1961).

Fertilization: Eggs and spermatozoa are released in water where fertiliza-
tion and subsequent development take place. In species that brood the embryo
and larva in the mantle cavity or gills, sperms in the water pass through the
incurrent siphon of the maternal organism into the mantle cavity or oviduct
where fertilization occurs. In Mysella tumida spermatozoa fall in the gill
chambers of the female and the transported sperms become attached to the gill

4

filaments by microvilli issuing from the sperm acrosome. The sperm may
' remain so attached for several months, until fertilization (O’Foighil, 1985). In
Crassostrea virginica (Longwell and Stiles, 1969), Ostrea_ rivularis (Hamada,
1927), and Mytilus edulis (Longo and Anderson, 1969), fertilization takes
place at the stage of metaphase I division of the maturing oocyte. Contrarily,
in Ostrea circumpicta and Spisula solidissima, the oocytes retain the germinal
vesicle until the time of fertilization (Hamada, 1927; Schechter, 1941; Sachs,
1971). According to observations by Vasetskii (1973) and Ginzburg (1974), in
Crassostrea gigas, Spisula sachalinensis and Mactra chinensis, fertilization
may take place at any stage of the process of maturation up to metaphase II.
According to Hylander and Summers (1977), upon activation of the sperm
during fertilization, the axial rod of the acrosome surrounded by the membrane
of the acrosomal vesicle is transformed into an acrosomal process making
contact with the plasmic membrane of the microvilli of the egg.

Cleavage : The eggs of bivalves are subject to spiral heteroquadrant cleav-
age. The cleavage plane of the first division divides the egg into two unequal
blastomeres: the smaller AB and the larger CD. After the second division, a
four-celled embryo is formed in which blastomere D is much larger than the
remaining blastomeres (Figures 1 and 2). In many species, during division by
cleavage, a polar lobe forms; this is a large cytoplasmic process at the vegetal
pole which, during division by cleavage, merges with blastomere CD and in
the second division, with blastomere D (Figure 3). Cleavage in bivalves loses
its synchrony early. Blastomere D and its daughter cells divide faster than the
other blastomeres of the embryo. Among the daughter cells of blastomere D
of the main quartet, blastomeres 2d and 4d are distinguishable, which are the
first and second somatoblasts. In species with a polar lobe, its material first
merges with blastomere 1D and then with blastomeres 2d and 4d.

Cleavage in bivalves is characterized by a strict order of sequence of
dexitropic and laeotropic divisions. However, in many cases (for example, in
Crassostrea), this order is disturbed (Fujita, 1929).

Blastomere 2d, after four small cells have separated from it, splits uni-
formly into the right cell Xd and the left Xs. Blastomere 4d divides into two
equal cells, Md and Ms (Figure 4, A).

As a result of cleavage, a ciliated sterro- or coeloblastula is formed; this
is the first larval stage of bivalve mollusks which is provided with cilia. A
sterroblastula is characteristic of marine bivalves and a coeloblastula of brack-
ish and freshwater mollusks (Malakhov and Medvedeva, 1986). The
sterroblastular cavity is occupied by a large cell, 2d or its daughter cells
(Figure 4, B). In the fresh- and brackish-water mollusk Dreissena polymorpha,
on the other hand, the blastocoel, which performs an osmoregulatory function,
is formed very early (Meisenheimer, 1901). The primordium of the shell gland

Figure 1: Cleavage in Dreissena polymorpha Pall. (from Meisenheimer, 1901).

A— stage with two blastomeres; B — with four blastomeres; pb— polar body.

is formed as a result of multiplications of Xd and Xs cells (Figure 5). In marine
bivalves the primordium of the shell gland is invaginated in the embryo from
the very beginning. In freshwater forms it initially lies in the blastula wall and
then invaginates in the embryo (Lillie, 1895; Meisenheimer, 1901).

Cells Md and Ms each produce one entodermal cell (enteroblast) and then
transform into mesodermal teloblasts from which the transitory mesodermal
band originates later. Some part of the mesenchyme probably originates from
the ectodermal cells (Meisenheimer, 1901). A notable contribution to the study
of the early development of bivalves is the paper by Gustafson and Reid
(1986). They have described the development of a primitive protobranch bi-
valve, Solemya reidi. Cleavage of the large (270 um in diameter) eggs of this
species is to date the only example, possibly, for bivalve mollusks of an initial
homoquadratic spiral cleavage with equal-sized blastomeres.

Incomplete division has not been observed in bivalves.

Gastrulation : Gastrulation occurs through the invagination of the ento-
derm near the vegetal pole of the embryo. After eversion of the shell gland,
the blastopore shifts far forward on the ventral side of the embryo.

Trochophore

In marine bivalves already in the blastula (sterroblastula) stage, one or
several circlets of cilia appear and at the animal pole—cilia of the aboral
organ. Thus, in marine bivalves the blastula stage is a transition to free living.
Free living is also possible for stages with an everted rudimentary shell gland
and a well-formed blastopore. After eversion of the rudimentary shell gland,
a trochophorelike larva forms (Figure 6). In the fresh- and brackish-water

D

Figure 2: Cleavage in Mactra chinensis (from Medvedeva and Malakhov, 1983).

A — Stage with 2 blastomeres, lateral view; B — stage with 8 blastomeres, view from
animal pole; C — stage with 8 blastomeres, view from animal pole; D — stage with 16
blastomeres, view from vegetal pole. Legend given in text.

bivalve D. polymorpha, only trochophore larvae are free living (Meisenheimer,
1901; see Figure 5).

The prototroch—a broad ciliary circlet—is the main organ of locomotion
of the trochophore larva. On the animal pole of the trochophore an apical tuft
of cilia appears, under which lies a thickening. of the ectoderm (aboral organ).
The mouth is situated under the prototroch and leads to blind gut. The terminal

part of the gut adjoins the ventral wall of the trochophore where, later, the hind
gut and anus form.

Veliger

The trochophore transforms into a veliger, which has a more complex
structure (Figures 7 and 8). The animal pole of the trochophore develops into

Figure 3: Cleavage in Pinctada maxima (Jameson) (from Wada, 1941).

A — zygote; B— with two blastomeres; C — with four blastomeres; pb — polar body;
pl— polar lobe.

a sail or velum—a disk fringed with cilia that serves as a swimming organ. An
apical tuft of sensory cilia is located in the center of the velum. The rest of
the larval body is covered with a translucent shell through which the internal
organs are visible. :

The description of the internal structure of the veliger is based largely on
Meisenheimer’s (1901) classical description of the development of Dreissena
polymorpha.

Feeding : The digestive system consists of the ectodermal foregut, ento-
dermal midgut, and ectodermal hind gut. Capture of food and its transfer to
the oral opening is accomplished by means of the ciliary band of the velum
(Figure 9). The velum is thus important in feeding as well as in locomotion.
According to Yonge (1926), the food particles from the long cilia of the
preoral outer band are passed to the adoral band. The distance between them
in the veliger of O. edulis is several microns. The length of the cilia of the
adoral band is about 8 1m and the width of the band about 20 um. Food
particles are encased in mucus as they move along the adoral band toward the

Figure 4: Blastula of Dreissena polymorpha Pall. (A) (from Meisenheimer, 1901) and
Mactra chinensis (B) (from Medvedeva and Malakhov, 1983). Legend given in the text.

Figure 5: Gastrula (A) and trochophore (B) of Dreissena polymorpha Pall. in sagittal section
(from Meisenheimer, 1901).

atc —apical tuft of cilia; b|—blastopore; fg—foregut; p—prototroch; phg—primordium of
hind gut; ptc — postanal tuft of cilia; rpp—renopericardiac primordium; s — shell;
sg—shell gland.

Figure 6: Early larval development in Mactra chinensis (from Medvedeva and
Malakhov, 1983).
A — larva with everted shell gland and blastopore, lateral view; B — trochophore;
C—commencement of shell formation.
abo — aboral organ; ar —archenteron; mt — mesodermal teloblasts; r — rudiment of shell;
sg—shell gland.

10

te

NS ies Sis
Pp Ss AG YS ee Lee
A is. R Etc iN

Figure 7: Early veliger of Cardium edule L. (from Creek, 1960).
m— mantle; rv —retractor of velum; sh —shell; st — stomach; v—velum.

oral opening. Below the adoral band, under the oral opening, there is a postoral
ciliary band comprising one row of complex 15—20 ym long cilia. The coor-
dination of the beating cilia of the pre- and postoral ciliary bands ensures,
according to Strathmann and his colleagues (1972), concentration of food
particles from the water by the ciliary band. The larger the cilia of the preoral
band, the greater the rate (and the lower the efficiency) of filtration of particles
(Strathmann and Leise, 1979).

The rate of filtration of food particles (flagellate algae at a concentration
of 1.5—5.5 x 10° cells/ml water) in M. edulis larvae is 11.4 1l/hr per larva
(Riisgard er al., 1980). At a concentration of food particles exceeding 200 il,
the rate of feeding decreases (Bayne, 1976). Walne (1965) showed that larvae
of O. edulis efficiently capture particles from 3.0 to 8.0-9.0 lum in size. The
larvae of M. edulis cannot efficiently capture particles less than 1.0 um or
more than 8.0-9.0 um in size (Riisgard et al., 1980). Colloidal substances in
suspension are not suitable for feeding; they form lumps which entangle the
larvae of M. edulis. At the same time, frozen or lyophilized algae and granu-
lated food from macrophytes and detritus are better assimilated (Mason, 1972).
The larvae of Crassostrea virginica and Mercenaria mercenaria do not use
organic debris and pure bacterial cells as food (Loosanoff, 1969).

Figure 8: Veliger of Ostrea edulis L. (from Erdmann, 1935).
a—anus; aa— anterior adductor; ap — apical plate; bg — byssus gland; bl — buccal lobe
(plate); csg —gland of crystalline style; dg —digestive gland; es esophagus; m — mouth;
mc — mesenchymal cells; pn — protonephridium; rv —retractor of velum; st — stomach;
v—velum; wmc— wall of mantle cavity.

A positive relationship has been established between rate of larval growth
and number of cells caught by the larva. Flagellate algae, such as Monochrysis
and Isochrysis, devoid of a cell wall and forming no toxic substances, consti-
tute a better food for larvae (Ukeles, 1969, 1975). At a low concentration of
food particles, the rate of filtration and its efficiency increase.

The postoral tuft of cilia lies in the buccal region and is formed by the
postoral ciliary band. According to Waller (1981), these cilia may have a
sensory function or facilitate expulsion of excess mucus and excess food from
the mouth.

The oral opening, situated at the edge of the lower part of the velum, leads
to the esophagus. Cells of the esophagus contain vacuoles and bear powerful
cilia that fill the lumen of the esophagus and project exteriorly through the oral
opening. The next section of the digestive tract is the stomach. The gastric
cells contain vacuoles; cilia are absent. The digestive gland or liver consists

12

Figure 9: Velum of the veliger of Ostrea edulis L. (from Waller, 1981).

of two pouches (lobes) arising from the stomach (see Figure 8). The cells of
the liver vacuolize later. The right lobe of the liver is larger than the left and
shifted backward. Cells of the digestive gland are marked by larger size and
sometimes by color—greenish or reddish-brown depending on food. Accumu-
lated granules of food matter are visible in them. Neutral lipids, and not
glycogen as in adult mollusks, are the principal energy reserve of larvae
(Holland and Spencer, 1973; Holland, 1978). A changeover to the new reserve
nutrients takes place in three- to five-month-old spat (Holland and Hannant,
1974). The large liver allows us to suggest a storage function for this organ;
a large part of the reserve nutrients is consumed during metamorphosis and in
the initial period after settling on the bottom, during which the larva does not
feed (Holland and Spencer, 1973). It may be that together with such large
cells, the larval liver contains small undifferentiated cells of the future defini-
tive liver.

The gland of the crystalline style forms on the right side of the posterior
part of the stomach. It is lined with cilia. At the end of larval life, or after the
larva settles to the bottom, the cells of this gland secrete the crystalline style
containing digestive enzymes. Behind the stomach lies the small intestine,
which forms a loop, and in the larvae of M. edulis the blind gut (Bayne,1971).
In the early veliger the gut may lack a lumen and resemble a cylinder of
closely packed cells (La Barbera, 1975). The gut epithelium is simple, flat-
tened, and bears cilia. The small intestine passes into the short hind gut—the
proctodeum—with vacuolated cells. The proctodeum opens exteriorly through
the anus; cilia are visible in its lumen.

13

The gut wall lacks muscles and the movement of food in the gut is
accomplished by cilia. In the larvae of some species, behind the anal opening,
which is surrounded by short cilia, there is a postanal tuft of dense 15 {1m long
cilia (Figure 10). The postanal tuft facilitates removal of fecal matter from the
mantle cavity.

pat

Figure 10: Veliger of Ostrea edulis L. (from Waller, 1981).

Posterior view: b — border between prodissoconch I and II; pat — postanal tuft of cilia;
rf—rudiment of foot; v — velum.

Respiration : A specialized respiratory apparatus is absent in the larvae of
bivalves. Oxygen is supplied and carbon dioxide eliminated through diffusion.
Since diffusion is facilitated by a flow of water, the various locomotory hy-
drokinetic structures of the larvae, in addition to other functions, also accom-
plish respiration. These are, the pre- and postoral ciliary tufts, and also the
ciliary tracts of the esophagus and gut. Respiration is further assisted by cilia
situated along the margin of the mantle cavity, including the region of future
gill formation.

Transport of substances : The larvae of bivalves lack a circulatory system.
Nor do they possess a branched gastrovascular system, which could replace a
circulatory system. The transport of substances from one organ to the other and

14

particularly that of nutrients from the digestive system to other parts of the
body, occurs through the extensive body cavity. Transport of various sub-
stances in the cavities is accomplished by means of flexion and extension of
muscles.

The body cavity of larvae of Crassostrea virginica and C. gigas contains
two main types of coelomocytes:

(1) phagocytes participating in the processes of excretion, and

(2) coelomocytes with smooth endoplasmic reticulum that do not participate
in the process of phagocytosis, but evidently process and transport the
soluble nutrients secreted by the cells of the digestive system (Elston, 1980).

Excretion : In the larvae of some bivalves, unlike other mollusks (except
pulmonate gastropods), the excretory system is represented by larval
protonephridia. These have been described in Dreissena polymorpha, Teredo
navalis, Ostrea edulis, and Codakia orbicularis (Hatschek, 1980; Meisencheimer,
1901; Waller, 1981; Alatalo et al., 1984). Protonephridia originate from the
ectoderm and are arranged on both sides of the body under the epithelium,
extending from the esophagus to the base of the foot (Figure 11). A
protonephridium is composed of two to three cells. Along the sides of the
esophagus in the body cavity lie ciliated cells—one for each protonephridium.
These cells are usually conical, often with a vacuole, and bear a tuft of very
long cilia lying in the protonephridial canal and extending to its excretory
pore. The canal is formed by a second cell. In transverse section, it is possible
to see the covering of this intracellular canal, isolated from the cytoplasm of
the canal-forming cell (Figure 12). The main mass of cytoplasm and the
nucleus are situated in the distal part of the cell; in the proximal part, firmly
attached to the ciliated cell, the wall of the canal becomes very thin. A third,
sometimes poorly discernible cell, delimits the excretory pore of the
protonephridium. The pores of the protonephridia are scarcely visible as they
lie deep in the mantle cavity (Figure 13).

In veligers of other mollusks—Pandora inequivalvis, Cardium edule (Creek,
1960; Allen, 1961), and others—neither protonephridia nor other excretory
organs are seen. Possibly this function is taken up by the coelomocytes scat-
tered in the body cavity. Elston (1980) has described the diapedesis—passage
of coelomocytes loaded with processed substartces from the body cavity through
the velum tissue into the mantle cavity.

Locomotion : In the veliger, swimming consists of a vertical rise followed
by a passive sinking. The veliger moves by beating the cilia of the ciliary band
along the margin of the velum. The velum in bivalve larvae is usually oval.
A remarkable large bilobate velum (Figure 14) is found in transoceanic and
deepwater species. Such is the velum of the transoceanic larva Planktomya

Figure 11: Frontal section through the veliger of Dreissena polymorpha Pall. at level of
protonephridia (from Meisenheimer, 1901).

cg — cerebral ganglion; es — esophagus; m — mantle; pg — pedal ganglion;
pn— protonephridium; v — velum.

henseni belonging to an unidentified species (Allen and Scheltema, 1972). A
larger velum facilitates larval migration to greater distances and efficient
collection of food particles (which are rare in open seas) since an increase in
velum size means an increase in number of ciliary bands. For example, in the
deepwater pholadid Xylophaga atlantica, the larva has no less than six ciliary
bands (Culliney and Turner, 1976).

Beating of the cilia produces the upward and somewhat forward move-
ment of the veliger, during which the velum is slightly inclined forward
relative to the axis of movement. While swimming, the veliger resembles a
flying helicopter. The principal locomotor organ is the outer preoral ciliary
band of the velum, consisting of a double row of ciliated cells. In the veliger
of O. edulis, 20-80 long cilia (50-70 um in length) originate from each cell.
The cilia are in contact almost throughout their length and together form a

16

Figure 12: Protonephridium of the veliger of Dreissena polymorpha Pall. in longitudinal
(A) and transverse (B) section (from Meisenheimer, 1901).

cicpn — canalicular cell of protonephridium; clpn —canaliculus of protonephridium;
cpn—cilia of protonephridium; tcpn— terminal cell of protonephridium.

“complex cilium”. The orientation of cilia in the complex cilium, parallel or
perpendicular to the plane of beating, ensures a thrust of maximum force,
moving the veliger upward. The efficient beating of straight cilia is directed
downward and coordinated by the wave of beating by the entire band (Figure
15). The reverse upward motion of cilia is accomplished in a bent condition.
If the wave passes at a right angle to the plane of beating of an individual
complex cilium, then the veliger, moving upward, will rotate in the direction
opposite to that of the wave. Inhibition of this rotation is ensured by beating
cilia that are inclined relative to the beating ciliary band and relative to the
velar margin.

The postoral ciliary band of the velum also plays some role in the loco-
motion of the veliger. It is a single row of complex cilia 15—20 um long. Each
complex cilium consists of four to five simple cilia. Their beating is effectively
directed upward and counteracts the beating of the cilia of the preoral ciliary
band (pcb) (Waller, 1981).

At an average speed, the veliger expends nearly 10% of its energy for
locomotion. Locomotion at higher speeds increases this expenditure up to 50%
(Zeuthen, 1947).

The veliger moves upward with a fully extended velum and intensive cilial
beating. As the intensity of cilial beating decreases, the veliger slowly sinks.

hy

Uy ss

b
a

Y

Figure 13: Disposition of organs at base of mantle cavity of the pediveliger of Ostrea edulis

L. (from Waller, 1981).

Posterior view: a— anus; b — border between prodissoconch | and II; e — eye;
obg— opening of byssus gland; osc — opening of statocyst canal; pat—postanal tuft of cilia;

ppn— pore of protonephridium; rf—rudiment of foot.

Mohaldet i
, 6

YR ay t
let wen i
. SSE Ze
se iz pat :
= Pee:

avy

i
eos

Ma,

17

Figure 14: Stretched velum of the deepwater woodboring pholadid Xvlophaga atlantica

Richards (from Culliney and Turner, 1976).

18

C- opcb
Figure 15: Schematic presentation of beating of the cilia of the velum of the veliger of Ostrea
edulis L. (from Waller, 1981).
ac — apical cilia; acb —aderal ciliary band; ipcb — internal preoral ciliary band;
opcb— outer preoral ciliary band; pocb— postoral ciliary band; sh—shell. Arrows show the
direction of beating of the waves of cilia.

The speed of sinking increases when the cilia of the velum stop beating. The
speed of sinking is greatest when the velum is rolled and the valves of the shell
closed. Rolling of the velum is affected by two or three pairs of larval muscles,
the velum retractors. They originate from the shell in the region of the pos-
terior part of the hinge line. In Dreissena polymorpha the dorsal retractor
passes along the dorsal side of the larva and supplies muscle fibers in the
dorsal region of the velum, which are attached to the velum integument. The
medial retractor proceeds forward from the place of its insertion to the ventral
and medial regions of the velum. One muscle is attached to the apical plate,
while the remaining fascicles are attached to various areas of the anterior part
of the velum (Meisenheimer, 1901). In Cardium edule there are individual
retractors for the medial and ventral regions of the velum (Creek, 1960).
During rolling of the velum first the apical plate withdraws into the shell, then
the lateral parts of the velum apparently roll up and the valves of the shell
close. During withdrawal of the velum under the shell, the stomach and esopha-
gus are shifted backward. Opening of the valves, slackening of the muscles,
and filling of the fluid in the extensive cavity of the velum, ensure its exten-
sion.

The ascent of the veliger usually follows a spiral pattern; this type of
veliger locomotion is seen in Ostrea edulis, Mercenaria mercenaria, Dreissena
polymorpha, and others. In other species the veliger ascends in a vertical line,

19

rotating in the process like a flying cannonball; the veliger of Argopecten
irradians exemplifies this type of locomotion. The nature and speed of veliger
locomotion depend on change in salinity, temperature, and pressure
(Mileikovsky, 1973; Cragg and Gruffydd, 1975; Hidu and Haskin, 1978;
Cragg,1980).

The veliger of Mercenaria mercenaria ascends at a speed of 7-80 cm/min
(Turner and George, 1955; Carriker, 1961), the late veliger of Crassostrea
virginica at a maximum speed of 60 cm/min (Wood and Hargin, 1971), and
the veliger of Lyrodus pedicellatus at a speed of 45 cm/min (Isham and
Tierney, 1953, cited by Mileikovsky, 1973).

Nervous System: Under the apical plate of the velum lies the cerebral
ganglion connected with the anterior part of the plate. Initially, the cerebral
ganglion is a single structure that later becomes bilobate. Numerous nuclei and
nerve cell fibers are visible in sections. In the middle part of the ventral side
there are two large pedal ganglia, which later join through connectives with
the cerebral ganglion (Figure 16). Development of the pedal ganglia precede
that of the foot (Meisenheimer, 1901; Cranfield, 1973).

Sense organs : Considerable development of the nervous system and diver-
sity and degree of development of the sense organs are associated with the high
locomotor activity of the veliger. The most noteworthy sense organ of the
veliger is the apical plate, which may be drawn in, forming an apical pit. The
diameter of the pit in O. edulis is 10-15 um. In its anterior part lie 20—100 cilia,
6-8 tum long, which perform a sensory function (Waller, 1981). In Teredo
navalis the apical plate bears only three complex cilia. As the apical plate grows,
the cilia shift to its posterior half (Culliney, 1975). A sensory function is also
performed, evidently, by the cilia of the internal preoral band. These are small
cilia, about 20 1m long, arranged irregularly. In the veliger ciliary bands and the
ciliated field generally function in locomotion and reception.

Integument : Protection of the veliger from unfavorable external influences
is done by the cells of the outer epithelium; a firm contact between them
ensures some protection of the larva. According to Waller (1981), the cells of
the outer epithelium are covered with mucus; apparently, the secretion pro-
duced by these epithelial cells also has a protective function. However, these
adaptations are accessory in character relative to the prime protective struc-
ture—the shell. Like other organs of the larva, the shell simultaneously per-
forms several functions: protective, supportive for muscle attachment, and jet-
directing; however, the primary, and often basic function is protection. The
shell, as already mentioned, is a product of the activity of secretory cells of
the shell gland. The peripheral cells of the shell gland located along its narrow
opening secrete the primary unpaired organic periostracum (Kniprath, 1979),

20

Figure 16: Cerebral, pleural (A) and pedal, visceral (B) ganglia of the pediveliger of Dreissena
polymorpha Pall. (from Meisenheimer, 1901).

ap — apical pit; bg — byssus gland; cg —cerebral ganglion; es — esophagus; gr — gill
rudiment; hg—hind gut; m— mantle; mc— mantle cavity; pg— pedal ganglion;
plg — pleural ganglion; sh — shell; v — velum; vg — visceral ganglion.

which initiates shell formation of a veliger, i.e., the prodissoconch I. The shell
gland evaginates and soon a mantle forms consisting of a single row of cells.
The growing margins of the mantle envelop the larval body from the sides. The
shell bends along the mediodorsal line and becomes bivalved.

The precise moment of initiation of calcification of the shell in bivalves
is not known. Evidently, this process begins after eversion of the shell gland,
as in gastropods. Due to the activity of the margins of the growing mantle, the

21

size of the shell increases rapidly and already in the early veliger stage it
entirely covers the larval body. When this happens, the formation of the
prodissoconch I is completed. The outer surface of each valve in ostreids has
a punctate-stellate appearance; a small punctate zone occurs in the center and
an extensive stellate-radial zone along the periphery (Figure 17). Possibly, the
punctate zone is formed as a result of the activity of the cells of the shell gland
and the stellate zone because of the activity of the mantle cells after eversion
of the shell gland (Waller, 1981). The valves of the prodissoconch I are usually
similar in size; they are calcified and transparent. However, there is no calci-
fication on the dorsal side of their place of attachment; this area of the shell
is replaced by the thickened periostracum. The hinge margin is straight and
usually (except in mytilids) nondentate. The valve is D-shaped.

The cells of the free margin of the external mantle fold and the thickened

Cae ae ht:
S5u2 chs" %

Figure 17: Early prodissoconch I of Ostrea edulis soon after eversion of the shell gland and
before bending along the hinge line (from Waller, 1981).

Dots —two centers of calcification.

margin of the mantle under the hinge continue to discharge a secretion from
which a new area of the larval shell is formed—the prodissoconch II. It differs
from the prodissoconch I in hinge development, appearance of lines on the
shell surface (repeating the outline of the mantle margin), and a change in shell
shape. The most significant change in shell shape is the appearance of a
prominence (umbo) on both valves.

The umbones are arranged dorsal to the hinge margin. Like the
prodissoconch I, the prodissoconch II is also calcified; one exception is the
prodissoconch II of Planktomya henseni (Allen and Scheltema, 1972).

In Perumytilus purpuratus, umbones do not develop and, at the time of
metamorphosis, the shell is mainly represented by the prodissoconch I and is
D-shaped (Ramorino and Campos, 1979).

Structural features of the larval hinge (Figure 18) and size and shape of
the shell valves make it possible to identify the species of different larvae.
These will be discussed in detail later. The central straight part of the larval
hinge — the provinculum — consists of different cardinal teeth along the hinge

D2

Figure 18: Scheme of the hinge system of bivalves.
c — crest, f — flange; | — ligament; It — lateral tooth; p — provinculum; st — special tooth.

margin of one valve and corresponding alveoli in the hinge margin of the
other. The shape, number, and arrangement of teeth differ in different species.
Lateral to the provinculum lies the lateral hinge system. It consists of thick
dorsolateral margins on one valve — flanges — and thin internal crests run-
ning parallel to these margins. The lateral teeth — flange projections edging
the provinculum — comprise the lateral hinge system. In some species there
are so-called special teeth that belong neither to the provinculum nor to the
lateral teeth (Rees, 1950; Chanley and Andrews, 1971; Le Pennec, 1980).

The anterior and posterior sides of the teeth usually bear ridges and
furrows that correspond to the ridges and furrows in the alveolar walls of the
other valve (Figure 19). The center of curvature of these ridges and furrows
lies roughly on the axis of rotation of the valves. It has been demonstrated in
adult bivalves that such a system of ridges and furrows decreases the gap
between partially open valves. Larvae of Rangia cuneata (Chanley, 1965),
Tiostrea (Ostrea) lutaria, T. chilensis (Chanley and Dinamani, 1980), Gemma
gemma, Lyonsia hyalina (Chanley and Andrews, 1971), and some other species
with lecithotrophic development lack teeth on the prodissoconch.

Closure of the shell valves is achieved, first of all, by the working of the
anterior adductor. Initially, it is situated behind the dorsal edge of the velum
and is the most prominent of all the veliger muscles. The anterior adductor is
formed and functions also in those larvae whose adults have only a posterior
adductor developing later. In Planktemya henseni, the two adductors are simi-
lar in size (Allen and Scheltema, 1972). Besides the adductor, the velum
retractors and three lateral muscles are attached to the valves; they extend from
the valves in the region of attachment of the anterior adductor and muscles and
terminate in the body wall (see Figure 8) (Cragg, 1985).

Rudiments of definitive organs : In addition to functional organs, the body
of the veliger contains rudiments of definitive organs that develop later and
begin to function after the larva has settled to the bottom; sometimes the
rudiments of certain larval organs are also present but not developed in the

23

Figure 19: Ridges and furrows on lateral surfaces of teeth and alveoli of veliger valve of
Mizuhopecten yessoensis.

veliger since they function only in the later larva — the pediveliger. The first
group comprises rudiments of gills, renopericardic complex, some elements of
the nervous system, rudiments of the foot, byssus gland, some sense organs,
and the reproductive system. In view of the secondary simplification of the
adult organism, in some mollusks the foot, byssus gland, and sense organs —
eyes and statocysts — exist only in the later periods of larval life. Such, in
particular, is the case in ostroids and pectinids.

The stages of the developed veliger with umbo and the last larval stage —
the pediveliger —are often combined in the term veliconcha or veliconch,
which was introduced by Werner (1939).

Pediveliger

In this stage the larva, having attained maximum size, bears a functional
foot with which it can creep, while simultaneously retaining the ability to swim
by means of its developed velum (Figures 20 and 21). The ultimate objective
of the pediveliger is to select and colonize a substrate and then to change over
to a definitive mode of feeding and locomotion. Hence the pediveliger char-
acteristically has functional sense organs — eyes and statocysts, and a func-
tional organ of locomotion and attachment, the foot. Concomitant with these
larval organs, definitive organs are present in the body of the pediveliger,

24

Figure 20: Pediveliger of Ostrea edulis L. (from Erdmann, 1935).

a — anus; aa — anterior adductor; acb — adoral ciliary band; ap — apical plate; bc — buccal
cavity; bg — byssus gland; cg — cerebral ganglion; cplvc — cerebropleurovisceral connective;
cs —crystalline style; csg—crystalline style gland; dbg—duct of byssus gland;
dg — digestive gland; e —eye; es— esophagus; g— gut; gc — gill cavity; gr— gill
rudiment; lab— “mouth lobe” or “labium”; m— mouth; mc—mantle cavity;
mp —metapodium of foot; pa— posterior adductor; patc —postanal tuft of cilia;
pg — pedal gaglion; plg — pleural ganglion; pn — protonephridium; pocb — postoral ciliary
band; pp —propdium of foot; precb —preoral ciliary band; rer — rudiment of cerebrorenal
organ complex; rf — retractor of foot; rv — retractor of velum; st — stomach; stat — statocyst;
u—umbo; v—velum; vg — visceral ganglion.

which have yet to undergo the last stage of development during metamorphosis
before they can become functional.

Feeding: The digestive system of the pediveliger differs very little from
that of the veliger. The digestive gland enlarges and the small intestine elon-
gates, forming a long loop in many species.

Respiration: A functional specialized respiratory system is absent in the
pediveliger. To the structures described earlier for the veliger, which facilitate
gas exchange, we may add the two to three gill filament processes which form

LS

Figure 21: Pediveliger of Mytilus edulis L.( from Bayne, 1971).

f— foot; o — osphradium; rpr—renopericardial rudiment
Remaining legend same as in Figure 20.

on each gill rudiment (Bayne, 1971, 1976). During creeping, gas exchange is
facilitated by the movement of cilia on the foot and of the foot itself. The
circulatory and excretory systems do not change substantially during develop-
ment from veliger to pediveliger.

Locomotion : In the pediveliger stage the velum, the initial organ of loco-
motion, attains maximum development, partly in connection with the increase
in shell mass and in larval body size. In addition, the new locomotor organ—
the foot—begins to function. Like most larval organs, the foot, too, is a
multifunctional organ. Its primary function is to probe the substrate for settling
and attachment of the larva by means of byssus threads or a cementing secre-
tion. The foot develops as an ectodermal outgrowth on the ventral side of the
body between the mouth and the anal pore (see Figures 10 and 13). The heel
of the foot (metapodium) begins to develop early and is covered with short
cilia. Ventral to it lies the toe (propodium), which later becomes larger than
the metapodium. Between the propodium and metapodium lies a depression in
which the duct of the byssus gland opens. A furrow, extending the entire length
of the foot, divides it into two equal halves (Figure 22).

26

Figu.e 22: Foot of the pediveliger of Ostrea edulis L. ventral view (from Cranfield, 1973).

According to Creek (1960), in the pediveliger of Cardium edule the larval
retractor of the foot is functional, and is replaced by a definitive structure once
the larva has settled on the bottom. The posterior pair of retractors is attached
to the shell in the region of the posterior adductor; these muscles then pass
between the visceral ganglion and one of the pedal glands and are inserted in
the ventral surface of the foot. The anterior pair of retractors originates on the
dorsal side of each valve before the hinge line. These retractors pass along the
sides of the digestive tract and bending around the pedal ganglion, are inserted
in the dorsal surface of the foot along both sides of the furrow. The longi-
tudinal muscles of the dorsal and lateral sides of the foot are attached along
the dorsal side of each valve near the anterior adductor of the shell. The
cruciate muscles participate in turning the foot, connecting its left and nght
sides to the opposite valve (Figure 23) (Cranfield, 1973).

The foot is covered with a ciliated epithelium. Each ciliated cell bears
numerous microvilli. The cilia are irregularly arranged on the surface of the
foot and are dense and very long at its tip and on its ventral and ventrolateral

27

Figure 23: Pedal glands of the pediveliger of Ostrea edulis L. in frontal (A) and sagittal (B)
sections (from Cranfield, 1973).

ar — anterior retractor; crm—cruciate muscle; dbg — duct of byssus gland; pg — pedal
ganglion; pr — posterior retractor; A, B, C,, C,, DD, —cells of nine glands of byssus
complex.

surfaces (Lane and Nott, 1970). The subepidermal glands participating in the
movement of the foot over the substrate and in the formation and attachment
of byssus filament occupy the maximum volume in the foot of the pediveliger.

Swimming pediveligers generally exhibit a negative phototaxis and a posi-
tive geotaxis. Their highest density is observed in near-bottom water layers.
While a larva is swimming, its foot may be extended, but on contacting the
substrate functions in larval locomotion, namely, creeping. The sequence of
locomotor acts during creeping are: (1) The slightly relaxed and extended foot
moves over the substrate by means of cilia. Glands opening on the sole exude
a secretion that contains weakly acidic mucopolysaccharides with a low vis-
cosity. Smeared on the substrate, this secretion facilitates ciliary movement.
(2) The anterior part of the foot is temporarily attached to the substrate
by means of a proteinaceous secretion, which is released by another gland

28

opening at the tip of the foot. Such a gland has been reported for the pediveliger
of O. edulis and M. edulis, but is absent in the pediveliger of the scallop
Placopecten magellanicus. Hence during creeping the latter larva is not at-
tached to the substrate (Gruffydd et al., 1975). Contraction of the posterior part
of the foot hauls the entire larva forward. (3) The foot relaxes and the loco-
motory cycle is repeated after a few seconds.

Creeping serves to attach the larva to the substrate. Once the foot is
retracted, i.e., loses contact with the substrate, swimming is resumed (Lane and
Nott, 1970).

Nervous System: In the pediveliger stage those elements of the nervous
system are most developed which are associated with the functioning of the
foot. The pedal ganglia, interconnected with commissures, constitute the ter-
minal point of the anterior pedal nerves passing along the tip of the foot, which
send sensory impulses from the ciliated sense organs. Besides the cerebral and
pedal ganglia, visceral ganglia are also developed, which are situated near the
posterior adductor. Rudiments of the pleural ganglia are located near the
cerebral ganglion and later merge with the latter in all bivalves except the
protobranchia (Figure 24) (Hickman and Gruffydd, 1971; Cranfield, 1973).

Sense organs : Ciliated sense organs of the pediveliger are represented by
the apical plate and sensory cilia situated on the foot, primarily the long
mobile cilia on its tip. Sensory cilia also occur in the furrow and byssus duct
of the foot.

In many pediveligers there are statocysts and eyes in the mantle cavity.
A highly developed nervous system and sense organs are characteristic of
planktotrophic larvae, which live for a long time in the plankton. In the
planktotrophic pediveliger of O. edulis there are two openings 7-9 Lm in
diameter along the sides of the base of the foot, which lead into the statocyst
cavity. These openings are surrounded by two rings of cilia: short cilia 24 um
long and long cilia about 15 um long (Waller, 1981; see Figure 13). A statolith
forms in the cavity of the statocyst. The duct is later blocked and the statocyst
becomes a closed vesicle (Figures 25 and 26). In O. edulis, the duct of the
statocyst is retained even in the adult. Here, not far from the base of the foot,
there are two eyes in the larvae of many species. Each eye is an almost round
cup of pigmented epithelium filled with a jellylike substance (Hickman and
Gruffydd, 1971). The opening of the cup is covered with a transparent
crystalline lens. The size of the eye spot in Mytilus edulis and Modiolus
modiolus is 5-10 um (Schweinitz and Lutz, 1976) and in Tiostrea (Ostrea)
lutaria, 26-34 um (Chanley and Dinamani, 1980). Nerves to the statocysts and
eyes arise from the cerebral ganglion. In the pediveliger of M. edulis, as
described by Bayne (1971), a band of ciliated cells passes from the roof of the

29

Figure 24: Frontal section through the pediveliger of Dreissena polymorpha Pall. at level of
ganglia (from Meisenheimer, 1901).
bg — byssus gland; cg — cerebral ganglion; es — esophagus, f — foot; gr — gill rudiment;
hg —hind gut; mc— mantle cavity; pg-— pedal ganglion; plg — pleural ganglion;
rr —rena! rudiment; sh — shell; v — velum; vg — visceral ganglion.

mantle cavity to the visceral ganglia. He considers this band an osphradium —
a chemosensory organ that assesses the quality of the water entering the mantle
cavity.

Bayne (1964) has also reported that each larval stage has its own reaction
threshold to external stimuli. The nature and intensity of the response are
greatly influenced by temperature. The various responses of the larval stages
of M. edulis to direct light, gravity, and pressure under laboratory conditions
are presented in Table | (from Bayne, 1976).

Integument : As in the veliger, the main protective system in the pediveliger
is the shell. At this stage the prodissoconch II markedly enlarges, the hinge
system develops, the provinculum lengthens, and the number of teeth increase.
In addition to the anterior adductor, a posterior adductor develops, which is
located behind the visceral ganglion above the hind gut. In O. edulis, the
posterior adductor is present even in the veliger (Fujita, 1933).

Attachment apparatus : In the pediveliger the byssus gland develops rap-
idly and begins to function; it forms as a depression in the actoderm along the

30

Figure 25: Nervous system of the pediveliger of Pecten maximus (1) in the statocyst region
(from Cragg and Nott, 1977).
pg — pedal ganglion; plec — pleurocerebral connective; plg —pleural ganglion;
plpc — pleuropedal connective; plvc — pleurovisceral connective; sc — statocyst canal;
sn — statocyst nerve.

Figure 26: Pedal ganglion and statocysts of the pediveliger of Dreissena polymorpha Pall.
in section (from Meisenheimer, !901).

pg — pedal ganglion; sc —statocyst; sl — statolith.

Table |: Relative intensity of response of different larval stages of M. edulis to external stimuli*
(from Bayne, 1976)

External stimull

Larval stage Light Gravity Pressure

Trochophore 0) 0) (0)
Veliger aa 0 (0)
Veliconcha** +4++ 0 +++
Pediveliger (Swimming) — + (0)
Pediveliger (crawling) ils atk 0

* 0 = no response; (—) = negative response, (+) = positive.
** According to Bayne, the veliconcha stage corresponds to that of developed veliger with umbo.

31

midline of the foot in the region of the pedal ganglia. The byssus gland or,
more precisely, the byssus complex, comprises a series of glands producing
different secretions that facilitate the formation and attachment of byssus threads
to the substrate. The byssus threads of the pediveliger of O. edulis comprise
two strands, 3—7 1m in diameter, joined together and enveloped in a common
cover (Figure 27). In addition to the glands of the byssus complex, the foot of
the pediveliger may contain other glands (see Figures 23 and 28). In the
pediveliger of M. edulis and O. edulis, nine different types of glands have been
recorded in the foot; in Pecten maximus, there are five types of glands (Gruffydd
et al., 1975). Gruffydd and his colleagues divide the pedal glands of the
pediveliger into three groups: (1) glands producing very thin primary and
secondary byssus threads; (2) glands producing mucus on the tip and sole of
the: foot, which facilitates creeping; and (3) glands present but functioning only
after metamorphosis; and producing a secretion for attachment of the shell or
secondary byssus threads to the substrate (Table 2). The blanks in Table 2 are
probably due not so much to the absence of some glands, as to inadequate
study of the structure of the larvae. The number of cells in the glands of the
foot of the pediveliger vary in O. edulis from 10 to 250 (Cranfield, 1973).
Cranfield (1973) has identified five phases in the behavior of the pediveliger
of O. edulis during settling. These, in his opinion, represent the sequence of

Figure 27: Byssus threads of the pediveliger of Ostrea edulis L. (from Cranfield. 1973).

32

hierarchic, fixed motor reactions leading to the final act of cementing. In the
absence of stimuli specific for a particular response, the latter is not produced
and the larva returns to an earlier phase of settling. In the opinion of Cranfield,
settling of bivalves and polychaetes is very similar. During settling the
pediveliger changes from a ciliary to a muscular mechanism of locomotion
over the substrate; in this case the viscosity of the mucopolysaccharide secre-
tion increases and the secretion of byssus threads begins. At the end of settling,
a secretion is produced which cements the larva to the substrate. The first
exploratory stages of behavior of the pediveliger during settling were described
above. In the pediveliger of O. edulis, later, in the course of settling, the
muscular movement of the foot becomes sharper and stronger and the speed
of locomotion decreases. The body turns occur more often in locomotion.
Initially, the larva creeps in a straight line, rarely turning. Subsequently,
movement becomes zigzag. With an increase in frequency of turning, the angle
of the path of movement decreases; the track of a pediveliger resembles a star
and then a circle. The last phase of settling — cementing of the pediveliger
of an oyster commences with a turn to the right (all previous turns have been
to the left), the shell rests on the foot, and the larva rotates on the foot, which
is attached to the substrate by its tip, and the left valve. Similar processes were
observed by Coon and Borne (1985) during settlement of the pediveliger of
Crassostrea gigas. The larva, ready to settle, after having swum with con-
tracted legs, now begins to extend its legs forward during swimming. It then
drops to the bottom and moves over the substrate, executing a series of sliding

Table 2: Pedal glands of pediveliger of various bivalves
(from Gruffydd ef al., 1975)

Species Mucous glands Glands of furrows Glands of primary
(tentatively producing byssus
and attaching secondary threads

byssus threads)

Nucula delphinodonta
Mytilus edulis

Pecten maximus
Crassostrea virginica -
Ostrea edulis +
Musculium securis - -
Sphaerium notatum - -
Dreissena polymorpha - -
Lasaea rubra + ate
Chione cancellata - -
Mercenaria mercenaria - -
Venerupis pullastra - =
Venus striatula - -
Xylotrya gouldi ats -

+ +
+++ 45

++ teteteeptrept+et est

38

movements. If the substrate is not congenial for settling, the larva abandons
it and begins to swim again. If the substrate is suitable for settling, the larva
cements itself to it and metamorphoses into a juvenile oyster.

efm

ifm

mc

Figure 28: Foot and byssus complex of the pediveliger of Myrilus edulis L. in transverse
section (from Bayne, 1971).

be -— byssus complex; efm — external fold of mantle; f — foot; ifm — internal fold of mantle;
mc — mantle cavity; scm-—secretory cells of mantle.

Rudiments of the definitive organs: The gill apparatus, renopericardiac
complex, and circulatory and reproductive systems are not fully developed and
are nonfunctional in the pediveliger.

METAMORPHOSIS

Metamorphosis, the most crucial period in the life cycle, is completed when
the pediveliger, while creeping, finds a substrate suitable for settling and,
discharging the byssus threads, attaches itself to the selected site. Larvae of
different species exhibit a well-defined substrate specificity. In the absence of
a desirable substrate the larva may postpone metamorphosis. According to
Bayne (1976), the larvae of M. edulis are capable of delaying metamorphosis
by 40 days at a temperature of 10°C and by two days at 20°C; larvae of O.
edulis can delay metamorphosis by several days (Cranfield, 1973) and larvae
of Pecten megellanicus by a month (Culliney, 1974). In some species, during
an overall delay of metamorphosis, the velum is discarded and the larva loses
its ability to swim; in other species the larva continues to swim by means of
the velum. In Brachiodontes glomerata, in the absence of a substrate not only
the velum may disappear, but a narrow band of the dissoconch may form
(Campos and Ramorini, 1980).

34

In many bivalves metamorphosis with total or partial resorption of many
larval organs is characteristic. The digestive system, except for the trapping
apparatus, is subject to comparatively less change (Bayne, 1971). The oral
opening is shifted and occupies an anterodorsal position near the hinge line.
The anal opening likewise shifts and occupies a posteroventral position. The
digestive gland acquires a definitive structure. Disappearance of the larval liver
has been reported in protobranchs (Drew, 1899).

The respiratory function changes over from nonspecialized external tis-
sues to a gill apparatus that, in most bivalves except protobranchs, performs
simultaneously the function of catching food. After the foot has shifted forward
during metamorphosis, the gill filaments from each side of the mantle cavity
fuse and divide the mantle cavity into an incurrent and excurrent chamber.
This ensures efficient filtration of the incurrent water by the gill filaments. The
number of gill filaments increases after metamorphosis (Bayne, 1976). In most
bivalves in the superorder Autobranchia, the preoral lobes assist in directing
the food particles caught by the gill filaments to the mouth. In many mollusks
the mantle edges fuse along the median line and muscular tubules form ante-
riorly and posteriorly — incurrent and excurrent siphons — which regulate the
flow of water through the mantle cavity (Figure 29). Soon after settling, the
transport of substances within the organism is accomplished as in the larva.
The (blood) circulatory system develops later.

The larval excretory system disintegrates and is replaced by definitive
kidneys originating from the pericardial cavity, which open through ducts into
the mantle cavity.

The velum, or /ocomotor apparatus, of the veliger and the pediveliger
disintegrates (Figure 30). It is invaded by phagocytes, which absorb the velar

Figure 29: Renopericardial rudiment in Dreissena polymorpha Pall.
(from Meisenheimer, 1901).

hg — hind gut; m — mantle; rhp — rudiment of heart and pericardium; rr — renal rudiment,
sh — shell.

Bo pee tec es

Figure 30: Metamorphosis of the pediveliger of Mytilus edulis L. (from Bayne, 1971).
A — degeneration of velum; B— formation of oral lobes; aa —anterior adductor;
ap — apical plate; cg — cerebral ganglion; es — esophagus; f — foot; lol — lower oral lobe;

pg — pedal ganglion; phc — phagocytized cells; uol— upper oral lobe; v — velum.

a5

36

cells. The muscular system which served the velum is also destroyed (Bayne,
1971). In Placopectan magellanicus, large parts of the velum are discarded
during metamorphosis; only the apical part is retained, which participates in
the formation of the upper preoral lobe (Culliney, 1974). As a result of these
processes, the larval mechanisms of swimming and catching food disappear.
The locomotor functions are usually passed to the foot and the function of
particle capture to the gills and preoral lobes; the lower lobe makes contact
with the first gill filaments. The change in mechanisms of food capture may
require several days, during which time the larva does not feed, and uses its
reserve nutrients. The foot in burrowing mollusks develops further, shifting
anteriorly in the mantle cavity. The larval muscles of the foot are replaced by
definitive ones. In attached (sessile) species, however, the foot is usually
totally or partly reduced, and its cells are phagocytized (Hickman and Gruffydd,
1971):

The central nervous system generally retains its structure. Ganglia occupy
definitive positions. The visceral ganglion is further developed, the relative
size of the cerebral ganglion decreases, and the pedal ganglia are reduced if
the foot is reduced. The cerebrovisceral connective develops. In many, espe-
cially immobile species, the eyes and statocysts disappear. Ultimately, in all
species the apical tuft of cilia disappears. In mobile forms definitive sense
organs, lacking in larvae, are formed.

Changes in the structure of the shell represent the concluding stage of
metamorphosis. The microstructure and mineralogy of the shell drastically
change; layers of the new definitive shell — the dissoconch — are formed
(Wilbur, 1964). The larval hinge is also replaced by a definitive one. Changes
in the hinge system may precede metamorphosis, or follow it, depending on
the family. The shell changes considerably in specialized forms such as wood-
and rock-boring species (Kiseleva, 1970; Turner and Johnson, 1971; Boyle and
Turner, 1976).

The definitive shell is in a partially open state due to the ligament that first
appears in the prodissoconch or dissoconch (Lutz and Hidu, 1979). This liga-
ment is an elastic cord connecting the valves of the shell. It begins to form in
the ligament fossa of the shell. The position of this fossa and hence of the
ligament proper, differs in different families. In the vast majority of bivalves
it is situated ventral to the hinge line. It should be pointed out that the ligament
may not always be present in larvae; if present, it does not always develop in
the adult.

In the family Teredinidae, new protective structures appear during meta-
morphosis: a calcified cone, made of detritus, over the inlet to the passage
made by the mollusk; a calcified bed in the passage; and plates or palettes near
the siphon (Figure 31) (Turner, 1966).

37

In the two species of bivalves of the family Pholadidae — Zirphaea crispate
(Warner, 1939) and Martesia striata (Boyle and Turner, 1976)—a ventral
tooth and alveolus form; these are situated on the ventral edge of the shell
facing the umbo (Figure 32). The ventral hinge is used only in the period of
metamorphosis and settling, after which it totally disappears. After termination
of metamorphosis, the clasping apparatus in mobile mollusks may become
reduced (Broom, 1985).

In monomyarian mollusks the anterior adductor of the shell is destroyed
during metamorphosis and its place occupied by the posterior adductor. Upon

Figure 31: Posterior end of Bankia rochi Mall. with siphons and palettes (from Turner, 1966).
p — palettes; s — siphon.

38

Figure 32: Valves of the pediveliger I of Martesia striata L. with tooth and alveolus on
ventral side (from Boyle and Turner, 1976).

completion of metamorphosis, the attachment system in mobile mollusks may
be reduced.

The development of the genital system lags behind the development of all
other systems and occurs only after the termination of metamorphosis. The
primary germ cells in the freshwater mollusks Sphaerium are already visible
in the early stages of development of the embryo, in the mesodermal bands;
in other species, these cells become visible only after metamorphosis in the
region of the ventral part of the pericardium (Okada, 1936; Coe and Turner,
1938; Lucas. 1975).

On the whole, metamorphosis is a distinct sequence of processes trans-
forming the larva into a juvenile. A disturbance of this sequence or blockage
of any stage leads to deformity or mortality (Turner, 1976).

Lecithotrophic Larvae and Direct Development

In evolution, primary development with planktotrophic larvae is typical of
bivalves (Jagersten, 1972), yet in many families a lecithotrophic development
phase is observed, which is usually linked with larviparity of ovoviviparity
(Thorson, 1936; Ockelmann, 1962). This phenomenon has been detailed for
bivalves by Sellmer (1967) and Blacknell and Ansell (1974). Duration of the
lecithotrophic phase can be determined from the size of the eggs and
prodissoconch I. In most bivalves the duration of this phase terminates in the
early differentiation of the digestive tract and formation of the straight-hinged
veliger with emergence from its envelopes. However, in more than 25 families,

39

the lecithotrophic phase extends beyond the limits of the trochophore stage
(Blacknell and Ansell, 1974). The development of lecithotrophic larvae and of
brood care are common for small (usually less than 1 cm long) bivalves. If the
lecithotrophic larva does not leave the egg capsule before metamorphosis, it
loses the adaptation for swimming. Thus, in the larvae of Lasaea rubra (Oldfield,
1964), Thyasira gouldi (Blacknell and Ansell, 1974), and Cardiamya pectinata
(Gustafson et al., 1986) developing in the egg capsule, the velum loses cilia
and becomes a vitalline receptacle.

Some mention should be made of the unique larvae of the primitive
bivalves of superorder Protobranchia (Drew, 1897, 1899a, b; 1901). From the
yolk-rich eggs of Nucula delphinodonta and Yoldia limatula, barrel-shaped.
lecithotrophic larvae develop, swim briefly in plankton. In contrast to most
Bivalvia, the prototroch and pretrochal ectoderm are not modified into the
velum in these larvae. Growing in size, they cover the entire larval body,
forming a temporary larval mantle which consists of five transverse rings of
large vacuolated cells. The long cilia of the cells of the middle rings form three
ciliary bands. The anal group of small cells produces a tuft of sensory cilia.
Under the integument of the larval mantle, the development of the definitive
mollusk precedes (Figure 33). During metamorphosis the larval mantle is
discarded.

Jagersten (1972) considers this bell-shaped larva a secondarily modified
one that was lost by the trochophore of mollusks even before the veliger
appeared in evolution. Other authors (for example, Fioroni, 1971; Salvini-
Plawen, 1972, 1973; Starobogatov, 1979) consider the lecithotrophic larva of
Protobranchia to be the starting point for bivalves. In our opinion, Jagersten’s
viewpoint, also supported by Ivanova-Kazas (1977), is more justifiable.

Development that includes lecithotrophic larvae is observed in all
Protobranchia irrespective of place of habitation — the Arctic, Antarctic, trop-
ics and littoral or benthic zones. Development may or may not include a brief
pelagic stage.

In addition to Protobranchia, development without a planktotrophic larva
is typical of the suborders Carditida and Lucinida and coincides with different
forms of brood care. Some young are attached with the egg envelopes to the
substrate (Astartidae), others are carried in the gills right up to the juvenile
stage (genus Cardita), and still others, after brooding in ctenidia, are carried
in a chamber that forms on the ventral side of the shell of the female (Milneria
kelseyi and Thecalia concamerata) (Dall, 1903; Yonge, 1969). Development
without a planktotrophic larva is also typical of the order Pholadomyida (su-
perfamilies Myochamoidea, Clavigelloidea, Pandoroidea, Thraciotdea). Thus,
in Pandoroidea a swimming larva emerges from the envelope after completing
metamorphosis within a few days (Pelseneer, 1911; Allen, 1961). A tendency

40

}

shg

Awaee
es

nA

\ Re

PAA TAY VARY

BAe
Ais

ARYAN

Racha
eipye S
MH U

» ee

oh

Figure 33: Lecithotrophic larva of Yoldia limatula Dall (from Drew, 1899).

A —external appearance; B — median section; atc —apical tuft of cilia; cg — cerebral
ganglion; fg — foregut; Im — larval mantle; m— mouth; mg — midgut; shg — shell gland.

to lengthen the lecithotrophic phase is observed in the superfamily Ostreoidea.
In Crassostrea gigas and C. virginica, fertilization takes place in the external
medium (water) and the larva takes to active feeding in the straight hinge
stage. In Ostrea edulis, fertilization occurs in the mantle cavity and brooding
in the gills continues until the larval shell has reached a iength of about 160
uum. In O. chinensis and O. lutaria, females bear larvae up to the pediveliger
stage which, soon after their emergence in the sea, settle and metamorphose
(Millar and Hollis, 1963); in the absence of a substrate for settling, metamor-
phosis may be delayed for several days (Chanley and Dinamani, 1980). In the
family Teredinidae, fertilization occurs in water in Bankia and the lecithotrophic
phase is confined to the trochophore stage. In Lyrodus and Teredo, the duration
of the planktotrophic phase may be considerably shortened. This tendency
appears, obviously, independent of geographic distribution of the species and

41

is associated with specific conditions of existence. In the superfamily Veneroidea,
predominance of the lecithotrophic phase is related to colonization of polar
waters (Ockelmann, 1958; Dell, 1972) in one line, and in another to reduction
in body size (Hansen, 1953; Oldfield, 1964). In the superfamilies Tellinoidea
and Mytiloidea, development with lecithotrophic larvae is observed in species
colonizing arctic waters. Lecithotrophic larvae and direct development are also
characteristic of the suborder Erycinina, in which brooding of young up to the
juvenile stage is observed, as well as male dwarfism an uncommon phenom-
enon in bivalves. In the family Galeommatidae, male dwarfism is observed in
Ephippodonta oedipus and Chlamydoconcha orcutti. Male dwarfism evolved
from secondary brooding of juveniles under the protective mantle of the adult
mollusk (Morton, 1976, 1981). According to Morton, male dwarfism is a
temporary phase in the development of these mollusks, which later grow into
animals of definitive size. In the family Montacutidae, dwarf males are found
in commensal forms — Montacuta floridiana, M. percompressa (Jenner and
McCrary, 1968), and M. phascolionis (Deroux, 1960). Recently, dwarf males
were reported for two species of teredinides— Zachsia zenkewitchi and Z.
serenei — inhabiting the roots of sea grass (Terner and Yakovlev, 1981, 1983;
Yakovlev, 1988).Yakovlev and Malakhov (1985, 1988) have shown that dwarf
males of Z. zenkewitchi combine features of neotany, regression and special-
ization.

Mollusks of the suborder Erycinina are the smallest bivalves (less than 1
cm), exhibiting a sharp fall in fecundity with extended periods of brooding.
Thus Arthritica bifurca, living in silt singly or with the polychaeta Pectinaria
australis (Wear, 1966), incubates numerous larvae only up to a length of
120 um, while Lasaea rubra cares for its progeny up to the juvenile stage
(Oldfield, 1955, 1964); in this species there is a maximum of 33 embryos,
which reach a length of 500 tm. Booth (1979) observed one sexually mature
L. rubra hinemoa, | mm in length, brooding two embryos, each 400 um long.

Table 3 presents data from tables compiled by Sellmer (1967), Blacknell
and Ansell (1974), Sastry (1979), as well as data from other researchers, on
species of marine and brackish-water mollusks with some form of brood care.
The list, of course, is not exhaustive. The classification of bivalves is that
given by Skarlato and Starobogatov (1979), except for the genus
Chlamydoconcha, which is included in the family Galeommatidae.

IDENTIFICATION OF PELAGIC LARVAE OF BIVALVES
(Terminology and Taxonomic Characters)

In larvae, a distinction is made between the anterior and posterior, and upper
and lower (dorsal and ventral) margins of the shell. The velum and adductor

42

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52

in the veliger and the velum and foot in the veliconcha, are situated in the
anterior margin. The opposite end, where siphons later develop, is called the
posterior. Morphologically, the valves join on the dorsal margin. Since in
larvae the hinge develops along the dorsal margin, this margin is also termed
the hinge margin. The margin opposite to the hinge is called the ventral
margin. The anterior part of the dorsal margin (up to the umbo) is called the
anterior shoulder, and the posterior part (from the umbo), the posterior shoul-
der (Figure 34).

Sculpturing, concentric (lines of growth) and radial lines appear on the
outer surface of the valves. In individual species the pallial line, the imprint
of the mantle muscle, is quite noticeable on the inner surface (Figure 34).

The hinge in larvae consists of a provinculum and a lateral system (see
Figure 18). The provinculum is a thickening of the hinge margin and bears
cardinal teeth. The lateral hinge system is represented by flanges and crests
(Rees, 1950; Zakhvatkina, 1959). In a closed shell the thicker dorsal margins
of the flanges of one valve are overlapped by the thinner dorsal margins and
inner crests of the other valve. Sometimes lateral teeth develop on the flanges
where their ends touch the provinculum. In some species there are special
teeth, which belong neither to the provinculum nor to the lateral hinge system.

C D

Figure 34: Schematic structure of the larval shell in different stages.
A — veliger; B — veliconcha; C — spat; D — veliconcha.
am — anterior margin; as — anterior shoulder; d—shell thickness; dis — dissoconch;
dm — dorsal margin; gl — growth line; h —shell height; hi— hinge; 1 — shell length;
lig — ligament; pd I — prodissoconch I; pd II — prodissoconch II; pm — posterior margin;
ps — posterior shoulder; u— umbo; vm — ventral margin.

39

The valves of larvae are connected by a ligament. This ligament may be
external or internal to the hinge line (see Figure 18). The ligament is termed
anterior, median, or posterior according to its position relative to the midline
of the hinge. In identification of larvae the following parameters and characters
are taken into consideration.

1. Size parameters of larva : Length, height and thickness of shell (Figure
34). Length of shell is the maximum distance between the anterior and pos-
terior margins parallel to the hinge line. Height of shell is the distance from
the apex of the umbo to the ventral margin perpendicular to the hinge line. The
thickness, which characterizes the degree of convexity of valves, is the dis-
tance between the most convex areas of the valves. The length of the anterior
and posterior ends of the shell may be used as an auxiliary parameter; it is the
distance from the anterior or posterior margins of the shell to the line of height.
Many researchers (Rees, 1950; Zakhvatkina, 1959; Loosanoff et al., 1966;
Gal’perina, 1969; Chanley, 1968; Schweinitz and Lutz, 1976; and others) use
relative size parameters (ratio of shell height to length and height to thickness)
as identification characters.

2. Shape of larva: The shape of a larva is determined by the following
characteristics : (a) length and mutual disposition of shoulders (these may be
equal or unequal in length and slope to the umbo at a definite angle or parallel
to each other); (b) length and shape of anterior, posterior, and ventral margins
of the shell (these may be straight or curved, sharp or blunt, and also slope to
one or the other end); and (c) shape and size of the umbones (these may be
knob-shaped, slanted, round, flat, or obtuse) (Figure 35).

C D E

Figure 35: Shape of umbones of larvae.
A — knob-shaped; B — slanted; C — irregularly rounded; D — obtuse; E — angular.

54

In accordance with variations in these morphological indices, the shell
may be round, ovate, trigonal-ellipsoid, and so forth. It may also be equi- or
inequilateral. In equilateral shells the anterior margin of the valve is symmetric
or nearly symmetric to the posterior margin; in inequilateral shells it is asym-
metric. In the larvae of some species the left and right valves of the shell may
be different in shape and size. Shells with equal-sized valves are called equivalve
and those with unequal valves, inequivalve.

3. Structure of hinge: Length of provinculum, number of teeth on each
valve, their shape and size, and also the number and shape of special teeth, and
the structure of the lateral hinge system — these are of taxonomic importance.

4. Presence, disposition, and structure of ligament : In position, the liga-
ment may be outer or inner. The inner ligament may be anterior, median or
posterior relative to the hinge line. In transverse section 1t may be rounded,
rectangular, square, or oval.

5. Sculpture of larval shell.
6. Thickness of valves and their transparency.

7. Presence of eyes : Visible as dark pigment spots, distinct on both sides
of the shell, in live as well as mounted larvae.

8. Color of larva and presence of characteristic pigmentation of internal
organs preserved in mounted material.

In identification of live larvae such features may be taken into consider-
ation: size and shape of velum; presence or absence of apical ciliary tuft and
length of its cilia; shape of intestinal spiral; position and structure of gill
filaments; shape of depression leading to duct of byssus gland; position and
number of retractors of the foot and velum, and so on (Lebour, 1938; Allen,
1961; D’Asaro, 1967; Chanley and Andrews, 1971; Chanley and Castagna,
1971; Dinamani, 1973; Culliney, 1974; Turner and Boyle, 1974; Culliney et
al., 1975). However, one must exercise caution in using these parameters
because the internal structure in developing larvae even at the same stage is
highly variable, making interspecific comparison difficult. The fairly useful
index for identification of larvae of different species is their behavior, since
each “tracks” differently while swimming, as does the pediveliger while creep-
ing (Turner, 1975).

In view of the fact that in general practice the identification of larvae is
based on mounted specimens, and that larval tissue becomes deformed during
mounting, the principal method of identification relies on features character-
izing the larval shell. However, the most apparent taxonomic character of shell
structure — structure of the hinge system of the larva —is difficult to ascer-
tain during examination of large plankton samples. Considerable time is re-

35

quired to examine the structure of the valve hinge in each larva. It is necessary
to separate the valves and mount them for microscopic examination at high
magnification. The method proposed by many researchers (Turner and Boyle,
1974; Schweinitz and Lutz, 1976; Lutz and Hidu, 1979; Le Pennec, 1980),
based on a detailed examination and comparison of shell structures and hinge
systems using a scanning electron microscope, ensures accuracy of identifica-
tion but is not practicable for working with a large number of larvae. Iden-
tification predominantly based on size parameters of larvae also does not
guarantee total accuracy since the larva of each species, even at the same
stage, may change shape during growth; this hardly ensures constancy of
relative size parameters. Hence, in preparing a key to the identification of
larvae to family, it is expedient to use shape of shell as well as some more
apparent individual characters, such as presence of dark pigmentation in mem-
bers of the family Myidae or ocular spots in Mytilidae as the main taxonomic
characters; these are retained in fixed specimens and are readily visible under
a binocular microscope. Size parameters of larvae and structure of hinge are
better used as second-order characters.

Key to Families for Larvae of Veliconcha Stage

The structure of the veliconcha shell according to families is presented in
Figure 36 (larvae arranged with anterior and left and posterior and right).
Orientation of larvae in photos random.

1 ( 4). Shell inequivalve.

2( 3). Valves differ considerably in shape and size. Left valve large, con-

vex, with high umbo raised above right valve. Right valve small,

flat, with low umbo. Anterior and slopes sharply. Pigmented eyes

TOG) AG Yosh PN Seem, CiGA Lemos, 1A te Ostreidae, Figure 37.

3( 2). Valves differ slightly in shape and size. Left valve slightly more
convex than right. Anterior and highly raised. Pigmented eyes present
FEA ie Serra CeO EL TERME eM Re ES a il Pectinidae, Figures 38, 55, 56.

4( 1). Shell equivalve.

5(10). Shell round or nearly round.

6( 7). Shell flat, slightly colored, large. Valves thin, brittle. Umbones in-
distinct or very small. Striation barely perceptible............
SmI ay sett! ober Ae Gh LINDA UR yes ANDAR Orc cud Kelliidae, Figure 39.

7 ( 6). Shell convex, intensely colored, moderate in size. Valves thick strong
Umbones high, round. Striation well defined.

8( 9). Height of shell slightly more than or equal to length. Hinge system
with three large rectangular teeth on right valve and two on left. .
Byes Mb ENA Mh ae ARAM ied ND Teredinidae, Figures 40, 63, 64.

pe)
io”
n
i)
=)
>

56

9( 8).

10( 5).
11 (18).
12 (13).

13(12).

14(15).

Height of shell slightly less than, or equal to length. Hinge system
with two equal teeth on left valve and two on right, one of which
is longer and central in position......... Pholadidae, Figure 41.
Shell different in shape, not round.

All margins of shell round and merge smoothly into one another.
Shell transversely oval. Anterior margin ventrally produced. Ante-
rior shoulder much longer than posterior. Anterior part of hinge line
with special large tooth. Ocular spots absent . .Tellinidae, Figure 42.
Shell longitudinally oval, ovate. Anterior margin not produced ven-
trally. Shoulders differ only slightly in length. Special teeth absent.
Ocular spots present.

Anterior margin blunt. Ventral margin broad, slightly rounded, par-
allel to hinge line. Relief of concentric lines quite distinct......
SEER SE es OORT ES ONT TOROS SUA Lithophagidae, Figure 43.

O
Srei©
4

3

4 8 12

Figure 36: Structure of veliconcha shells in different families.

| —Pectinidae; 2 —Mytilidae; 3 — Ostreidae, Cordiidae; 4 — Solenidae,; 5 — Veneridae;
6 — Tellinidae; 7 — Mactridae; 8 — Myidae; 9 —Clinocardiidae; 10— Kelliidae; 11 —
Hiatellidae; 12 — Teredinidae; 13 — Pholadidae; pl — pallial line.

15(14).
16 (17).
17(16).
18 (11).

19 (22).
20(21).

21 (20).

22(19).
23 (26).

24 (25).

25 (24).

Si

Figure 37 : Veliconcha of Crassostrea gigas.

A — external view; B — left valve.

Anterior margin acute. Ventral margin appreciably rounded not par-
allel to hinge line. Concentric line of lesser relief indistinct.
Provinculum consisting of a continuous row of denticles.......
SES RSS NAN RE SE EDMOND Mytilidae, Figures 44, 52, 53, 54.
Denticles absent in central part of provinculum........ Arcidae.
Margins of shell not rounded.

Posterior margin of shell straight; anterior margin acute and stretched.
Posterior margin appreciably slopes towards ventral margin. Um-
bones low and flat. Dark pigmentation present along mantle margin
ang Shoulders sete pet mete: cca Sac pend Myidae, Figures 45, 62.
Posterior margin slopes slightly and almost perpendicular to ventral
margin. Umbones are high conical. Pigmentation absent along the
shoulders and mantle margin....... Mactridae, Figures 46, 60, 61.
Posterior margin of shell rounded; anterior margin not tapering or
almost net, and not stretched more than posterior margin.

Shell triangular-oval with triangular apex in umbonal region. Shoul-
ders drop steeply toward ventral side.

Ventral and lateral sides form regular semicircle. Shoulders of al-
most equal or equal length, symmetrical. Pallial line absent. Height
of shell equal to its length or slightly less . . . Veneridae, Figure 47.
Ventral and lateral sides semioval. Anterior shoulder longer than
posterior and slightly bent. Pallial line present. Height of shell less
thanaitswlenothyee Sea eee sens. contr Hiatellidae, Figures 46, 58.

58

Figure 38: Veliconcha of Patinopecten vessoensis.

A — external view; B— right valve.

59)

Figure 39: Veliconcha of Kellia japonica.

Figure 40: Veliconcha of Teredo navalis.

A — external view; B — right valve.

60

Figure 41: Right (A) and left (B) valve of the veliconcha of Zirfnaea crispata; veliconcha
of Barnea japonica (C).

26 (23).
27 (30).
28 (29).

29 (28).
30(27).

Shell rectangular-oval. Shoulders almost parallel to ventral margin
of shell.

Anterior margin slightly, tapering. Ligament external. One tooth
present at each end of locking line on right valve and a correspond-
ing match on left valve.

Shoulders rounded weakly sloping......... Solenidae, Figure 49.
Shoulders straight, appreciably sloping ..... Cultellidae, Figure 50.
Anterior margin tapering no more than posterior margin. Ligament
internal. Lock consists of row of denticles on right valve and notches
Onl LEf o oes Se GES Ne) Seale teeta one Cardiidae, Figure 51.

CHARACTERS OF LARVAE ACCORDING TO FAMILIES

Mytilidae

Both ends of the shell are rounded, but the anterior end is narrower than the
posterior; the shape of the shell is therefore triangular-oval. The umbo 1s
highly developed. The larvae are fairly large. The hinge line is longer relative
to the total size of the shell and, unlike most members of other families, grows
in length parallel to the growth of the shell. The hinge has a series of taxodont
teeth along the entire hinge line; tooth size increases toward the ends of the
row. The ligament is internal and posterior, rarely median. Pigmented spots
(eyes) are visible in the veliconcha stage.

61

yoo] — q {MAA [e1gUes —
DIIYIIVG DUOIDJY JO BYOUOSIIA

Tp ounsi4

62

Figure 43: Veliconcha of Adula falcatoides.

A — external view; B — hinge of right valve.

Figure 44: Veliconcha of Mytilus trossulus.

A — general view; B—right valve.

63

64

“DIDIUNA]

DAW (q) pue vo1uodvl vdpw (Vv) JO eyouOdI]aA :Gp oindi4

Figure 46: Veliconcha of Mactra chinensis.

65

66

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* Seer a eeee®

B

Figure 47: (A) Veliconcha of the family Veneridae; (B) right valve of the veliconcha of
Ruditapes philippinarum.

Figure 48: Left valve of the veliconcha of Histella arctica.

Figure 49: Veliconcha of Solen krusensterni.

67

68

Figure 51: Right valve of the veliconcha of Keenocardium californiense.

69

Mytilus trossulus Gould (see below), Mytilus coruscus Gould (larvae not
described), Crenomytilus grayanus (Dunker) (see below), Modiolus difficilis
(Kuroda and Habe) (see below), and Muculista senhousia (Benson) (see below)
inhabit Peter the Great Bay.

Arcidae

In shape, presence of eye spots, and structure of the lock, the larvae of the
family Arcidae are very similar to the larvae of the family Mytilidae, more
particularly to the Pacific mussel, Mytilus trossulus, and Gray’s mussel,
Crenomytilus grayanus. They differ mainly in that the larvae of the family
Arcidae have a broader anterior margin and do not bear denticles in the center
of the hinge line. The larvae of mussels are also more elongated and their
umbones are less massive.

Boucard’s arca, Arca boucardi Jousseaume, lives in Peter the Great Bay;
larvae described below.

Lithophagidae

The shell is equivalve, longitudinally oval, and its ventral margin parallel to
the hinge line. The length of the shell is much more than its height. The
umbones are large, broad, and round. The hinge system is similar to that in
the family Mytilidae, but teeth in the central part of the provinculum are
lacking. The ligament is posterior. The shell is strong, with distinctively raised
growth striae. Large dark ocular spots are present.

Adula falcatoides Habe inhabits Peter the Great Bay (see below).

Ostreidae

The veliconcha is large. The shell is inequivalve. The left valve is much larger
than the right, more convex, and has a high umbo. The right valve is flat and
has a low umbo. The anterior margin is more drawn out compared to the
posterior.The hinge comprises two anterior and one to three posterior rectan-
gular teeth. The space between the anterior and posterior teeth is smooth. The
lateral hinge system is absent. The ligament is posterior. Eyes are present and
visible at a shell length of 250-290 um. In the mature veliconcha, dark
pigmentation is perceptible in the subumbonal region.

Crassostrea gigas (Thunberg) inhabits Peter the Great Bay (see below).

70
Pectinidae

The shell is inequivalve. The left valve is slightly more convex than the right.
The shell is triangular and its apex coincides with the anterior end, which is
more acute and longer than the posterior, and produced frontally and dorsally.
The ventral margin slopes sharply toward the anterior end. The dorsal margins
are unequal, with the anterior margin usually longer than the posterior. The
umbones are small, round, and slightly raised. The valves are brittle, thin, and
colorless. The sculpture of the prodissoconch is fine and poorly visible. In the
developing dissoconch in the pediveliger stage, the sculpture is alate, with
radial ridges (veins). The taxodont hinge (provinculum) is very similar to that
in Mytilidae and comprises several rectangular teeth on each margin of the
tooth row. The number of teeth may increase as the larva grows. The central
part of the provinculum is so thin that no teeth whatsoever are present (in most
species) or the teeth are almost indistinguishable. The lateral hinge system is
lacking. The ligament is median or posterior. Ocular spots appear in the
veliconcha before metamorphosis.

Chlamys farreri nipponensis Kuroda (see below), Swiftopecten swifti
(Bernardi) (see below), and Mizuhopecten yessoensis Jay (see below) inhabit
Peter the Great Bay.

Hiatellidae

The veliconcha shell is equivalve and rounded-triangular. The anterior end is
pointed and directed forward sharply. The umbones are round and distinct. The
posterior margin is obtuse and straight while the ventral margin is roundish.
There is a large tooth on the right valve, located in the anterior part. The left
valve likewise has just one provincular tooth. One flange is located on the nght
valve and the other on the left valve. The ligament is large and posterior. Eyes
are absent.
Hiatella arctica (Linné) inhabits Peter the Great Bay (see below).

Kelliidae

The shell is equivalve, large, flat, and roundish or slightly squared. The ante-
rior end is more obtuse than the posterior. The umbones are small. The
provincular teeth are absent. A rudimentary lateral tooth appears by the end
of planktonic phase. The ligament is median or anterior. The posterior muscle
— adductor — and growth striae become visible very late. The larva is lightly
colored. The liver and velum are light, yellowish-green.

Kellia japonica Pilsbry is found in Peter the Great Bay and its larva is
described below.

71
Cardiidae

The veliconcha shell is longitudinally oval and equivalve. The anterior end is
narrow and slightly elongate; the posterior end obtuse and broad. The ventral
margin is round. The anterior shoulder is equal to, or slightly longer than the
posterior. The umbones may be high and round or low and broad. The shell
is slightly inflated. The hinge comprises a row of small sharp teeth on the right
valve and corresponding sockets on the left valve. Flanges are situated on the
left valve and crests on the right. Both anterior and posterior lateral teeth are
present. The ligament is posterior. Eyes are absent. The pallial line is distinct.

Keenocardium californiense (Deshayes) is found in Peter the Great Bay
and the larva is described below.

Tellinidae

The shell is equivalve. The veliconcha shell is transversely oval. The shell is
inequilateral. Although both ends are roundish, the anterior end is ventrally
produced and often longer than the posterior. The shoulders are long and slope
steeply. The umbo is initially round but later becomes knob-shaped. The
provinculum consists of a row of small rectangular teeth. As the larva grows,
special teeth develop in the anterior part of the provinculum. The lateral hinge
system is present and consists of alternate crests and flanges — anterior crest
and posterior flange on the right valve and anterior flange and posterior crest
on the left valve. The ligament is median. Eyes are absent.

Macoma balthica_ (Linné) (see below), Peronidia venulosa (Schrenck)
(larva not described). Macoma incongrua (Martens) (larva not described) and
Macoma orientalis Scarlato (larva not described) inhabit Peter the Great Bay.

Veneridae

The shell is equivalve. The veliconcha shell is irregularly rounded and almost
equilateral. The anterior margin is slightly more pointed and longer while the
posterior margin is broader and shorter. The shoulders are long, straight, and
sloped. The umbones are high, broad and roundish. The hinge system is of two
types. In members of the genus Venerupis, starting from the end of the first
week of life, several small indentations (teeth) develop on the prodissoconch;
these do not develop in larvae of the genus Venus. In some species of the genus
Venus, weak lateral processes appear, while in others it is difficult to see any
hinge structures. The lateral hinge system consists of flanges and crests —
flanges on the left valve and crests on the right. In some cases the hinge shows
the presence of special teeth. The ligament is posterior. Eyes are absent.
These species are found in Peter the Great Bay: Callista brevisiphonata

VA

(Carpenter), Saxidomus purpuratus (Sowerby), Dosinia japonica (Reeve),
Mercenaria stimpsoni (Gould), Protothaca jedoensis (Lischke), Protothaca
euglypta (Sowerby), and Callithaca adamsi (Reeve); their larvae have not been
described.

The larva of Ruditapes philippinarum (Adams and Reeve) has been de-
scribed (see below).

Cultellidae

The morphology of the larvae of this family is identical to that of the family
Solenidae. The principal difference is that in the veliconcha of the family
Cultellidae, the shoulders are straight, sloped, or slightly concave.

Siliqua alta (Broderip and Sowerby) (see below) inhabits Peter the Great
Bay.

Solenidae

The shell of the veliconcha is equivalve, oval, and anteroposteriorly elongate.
The anterior end of the shell is equal in length or slightly longer than the
posterior. The umbo is broadly roundish. The hinge system consists of two
large teeth (one on each end of the hinge line) on the right valve and corre-
sponding sockets on the left valve. Between the sockets of the left valve, a thin
row of very small sharp or blunt teeth occurs which, during closure of the
shell, enter the alveoli on the right valve. The ligament is external. A pallial
line is present on the inner surface of the valves. Eyes are absent.
Solan krusensterni Schrenck (see below) inhabits Peter the Great Bay.

Mactridae

In the veliconcha stage the larva is ovate or rounded-oval. The shell is equivalve.
The anterior end is longer and more pointed than the posterior. As the posterior
end is ventrally more produced than the anterior, it is considerably broader
than the anterior. The shoulders are slightly rounded and slope slightly; the
anterior shoulder is longer than the posterior. The umbo is broad and roundish,
sometimes becoming triangular later. The hinge system has one rectangular
tooth on the right valve and two teeth of different size on the left valve. In
the anterior part of the hinge line a large lobate tooth occurs. There are also
lateral teeth in the form of tubercles on both sides of the hinge on each valve.
In some species of Mactridae, the hinge is similar on both sides, comprising
a row of small rectangular denticles and one posteriormost distinct tooth. The
lateral system comprises flanges and crests. The ligament is posterior. Eyes are
absent.

73

Mactra chinensis Philippi ( see below), Spirula sachaliensis (Schrenck)
(see below), and Spisula voyi (Gabb) (larva not described) inhibit Peter the
Great Bay.

Myidae

The veliconcha shell is equivalve. The posterior end is broader than the an-
terior. The dorsal margin is straight and slopes markedly, while the ventral
margin is round. The umbones are flat and low. There is one provincular tooth
on each valve. One flange occurs on the right valve (posterior) and another on
the left (anterior). The ligament is posterior. Eyes are absent. Soft body with
dark pigmentation.

Mya japonica Jay (see below) and Mya truncata (Linné) (see below)
inhabit Peter the Great Bay.

Pholadidae

The veliconcha is large. The shell is equivalve, convex, and inequilateral. The
anterior end is slightly longer than the posterior. The margins are smooth and
broadly roundish. The dorsal margins are short, round, and slope abruptly. In
the early veliconcha the umbones appear roundish but later become knob-
shaped and considerably raised. The hinge has two teeth of the same size on
the left valve and two on the right, one of which is longer and central in
position while the second, smaller tooth is situated in the anterior part of the
hinge line. The small teeth on the left valve are separated by a wide socket
for the central tooth of the right valve. Flanges occur on the left valve and
crests on the right. The ligament is posterior. The margins of the valves are
edged with a dark band. A pallial line is present. Eyes are absent. The umbo
is purplish-red. The anterior adductor is slightly larger than the posterior.

Barnea japonica (Yokoyama) (see below) and Zirfaea crispata (Linné)
(see below) inhabit Peter the Great Bay.

Teredinidae

The shell of the veliconcha is round and highly convex. As it grows, the shell
becomes somewhat oval and dorsoventrally produced. The anterior and poste-
rior ends are broadly rounded and symmetric. The height of the shell is slightly
greater than its length. The dorsal margins are short, round, and slope sharply.
The umbo is round, becoming knob-shaped in late veliconcha. The hinge has
large rectangular teeth — three on the right valve and two on the left. Flanges
occur on the left valve and crests on the night. The ligament is posterior. The
surface of the shell has concentric striation. The larva is dark colored (from

74

yellow to brown), especially in the umbonal region. Eyes are absent. A mar-
ginal band passes along the edge of the shell. The posterior adductor is larger
than the anterior. The latter undergoes considerable reduction during larval
development while the posterior adductor grows continuously.

Teredo navalis Linné (see below), Bankia setacea (Tryon) (see below),
and Zachsia zenkewitchi Bulatoff and Rjabtschikoff (larva described by Terner
and Yakovlev, 1981) inhabit Peter the Great Bay.

PACIFIC MUSSEL, MYTILUS TROSSULUS GOULD
(Mytilidae)*

Veliconcha

The shell is triangular-oval, its anterior end tapering and raised. The
anterior shoulder is longer than the posterior, but just slightly. The umbone is
conoid but not broad (see Fig. 44). Umbones appear at a small shell length of
125—135 um. The larva is weakly colored. Striation is concentric and barely
noticeable. Eyes appear in larvae with a shell length of 230—240 um. The
diameter of the eyes is S—7 tm. The hinge line is weakly bent and its length
more than the umbonal width, constituting 75—85 Um in the early veliconcha
and 140—150 um in the late veliconcha. The early veliconcha is 130—140 um
in size, with three-four large teeth in the anterior part, two-three teeth in the
posterior part, and 11—13 denticles in the middle. The number of teeth in-
creases as the larva grows, reaching 8—10 on each side of the hinge line in the
late veliconcha. There are 15—20 denticles in the center (Figure 52). The
ligament is large, oval, and posterior. Metamorphosis occurs at a shell length
of 250—350 bm.

Ecology

Spawning of the Pacific mussel extends from May to September in Peter
the Great Bay, Sea of Japan. Larvae appear in the plankton from June to mid-
September at a water temperature of 13—23°C. The maximum number of
larvae is found from the second half of June to mid-July (Kasyanov et al.,
1976, 1980; Shepel’, 1979). In Avachin Inlet (southern Kamchatka) late larvae
are found from mid-August to September at a water temperature of 8—15°C
(Buyanovskii, 1987). In the waters of southern Sakhalin larvae of the Pacific
mussel are found in the plankton (from early August to mid-October; with
maximum occurring mid-August) at a water temperature of 8 20°C, settling en

* Using the method of protein electrophoresis, it was demonstrated that this species lives in
the Far-Eastern seas of Russia, and not the closely related species, Mytilis edulis Linné (MacDonald
et al., 1990).

75

Figure 52: Hinge of right valve of the veliconcha of Mytilus trossulus.

masse at the end of August (Kulikova, 1975). Thus, during the reproduction
of M. trossulus in the study area, the water temperature varies from 8 to 23°C.

CRENOMYTILUS GRAYANUS (DUNKER)

(Mytilidae)

Veliconcha

The shell is equivalve and longitudinally oval. The anterior end is longer
than the posterior and only slightly drawn dorsally. The umbones are broad,
massive, and round (Figure 53 A, B). The larva is yellowish-brown; the umbo
is more intensely colored. Striation of the shell is concentric, barely percep-
tible. The length of the provinculum is greater than the length of the umbones.
The number of provincular teeth increases as the larva grows. In a developed
larvae the provinculum has up to 20-25 central denticles and 10 large lateral
teeth. The ligament is oval and located at the end of the row of denticles. The
larva attains the veliconcha stage at a shell length of 120-130 um and a hinge
line length of 90 um. As the larva grows, the length of the provinculum
increases to 150 tm. Eyes appear in the larva at a shell length of 220 1m. The
diameter of the eyes is 15 um. The foot is fully formed and becomes functional
in the larva at a shell length of 250 um.

Larvae of C. grayanus differ from those of the Pacific mussel Mytilus
trossulus and Modiolus difficilis primarily in shape of the shell. Compared to
M. trossulus, the shell is shallower dorsoventrally and the provinculum bears
a larger number of denticles. C. grayanus differs from the larvae of Modiolus
difficilis mainly in having a wider and rounder anterior margin, a more fragile
shell, less distinct concentric striation, and a lighter color.

76

Figure 53: General view (A) and hinge of right valve (B) of the veliconcha of Crenomytilus
grayanus, general view (C) of the veliconcha of Modiolus difficilis.

Ecology

C. grayanus breeds throughout the summer along the southern coast of
Sakhalin, with larvae occurring in the plankton from July to early October.
Breeding peaks earlier or later, depending on temperature conditions. More

77

often, it occurs from July to early August, when the water temperature is
16 —17°C. In Peter the Great Bay this species spawns twice, end of May to June
and mid-August to September inclusively (Dzyuba, 1972; Kasyanov ef al.,
1980). Larvae are found in the plankton of Vostok Bay (Peter the Great Bay)
throughout summer; there are two population peaks in July and in September,
and larvae develop in a temperature range of 13—22°C. Duration of the pelagic
stage of development of C. grayanus along the southern coast of Sakhalin (Sea
of Okhotsk) and in Peter the Great Bay is 5—6 weeks.

Drozdov and Kulikova (1979) have described the embryonal and postem-
bryonal development of C. grayanus.

LONG-BRISTLED MODIOLUS, MODIOLUS DIFFICILIS
(KURODA AND HABE)

(Mytilidae)

Veliconcha

The shell is oblong-ovate (see Figure 53,C). The anterior end is not raised
and is slightly longer than the posterior end. The umbones are large and broad.
The shell is compact. The prodissoconch II has noticeable concentric striation.
The valves are massive. The larva is dense yellowish-brown. The hinge con-
sists of eight-nine lateral teeth and 15—18 small central teeth. The length of
the hinge is greater than the width of the umbones. The ligament is rectangu-
lar. Large, dark-colored eye spots appear at a shell length of 270 um or more.
The iarva settles at a shell length of 280-300 um.

Ecology

Modiolus larvae are found in August-September in the plankton of Vostok
Bay (Peter the Great Bay).

Larvae of this species are not described in the literature.

MUSCULISTA SENHOUSIA (BENSON)
(Mytilidae)

Veliger and Veliconcha

M. senhousia forms a clutch in the shape of twisted cords which are
composed of large adhesive eggs. Larvae hatch with a straight hinge margin.
Their later development is pelagic (Matveeva, 1975). Morton (1974) stated that
in the South China Sea, this species releases gametes in the water. The first
and most minute larvae observed by us in the plankton had a shell length of

78

100 um and height of 90 um. The veliger valves have a straight hinge margin,
bearing several minute, equal-sized teeth (Figure 54). The larva attains the
veliconcha stage at a shell length of 120-130 um. The shell is equivalve,
ovate, and highly convex. The anterior margin is pointed and only slightly
raised. The umbones are high and well developed. The ratio of length to height
and thickness of the valves is 1.6:1.3:1.0. The larva is dark brown and due to
the great convexity of the valves is less transparent. Striation on the shell is
concentric and distinct. The eyes are small and almost imperceptible against
the dark background of the shell (Figure 54). The hinge line is arcuate due to
the development of large teeth, five-six, at each margin of the provinculum.
There are 10—12 central rectangular denticles in the hinge row. The length of
the hinge line does not exceed the width of the umbones, but is equal to it,
reaching 100-110 ttm in developed larvae. The ligament is posterior but,
unlike the ligament in other members of the family Mytilidae, shifted much
closer to the middle of the hinge line. The shell in the veliconcha stage ranges
from 120—280 bm in length.

Ecology

The pelagic stage in M. senhousia continues for two-three weeks. Along
the southern coast of Sakhalin (Aniva Bay, Sea of Okhotsk) and in Vostok
Bay, larvae are found in the plankton for a fairly long time — from the end
of July to September inclusive, with a maximum water temperature of 18—
23°C.

Some data on the developmental biology of Musculista are available in
works of Morton (1974) and Matveeva (1975). Kulikova (1978, 1979) has
described the morphology of the pelagic larvae and their population dynamics
in the plankton of Busse Lagoon (southern Sakhalin).

CRESCENT-SHAPED ADULA, ADULA FALCATOIDES HABE
(Lithophagidae)

Veliconcha

The shell of the veliconcha is longitudinally oval and its length consider-
ably greater than its height. The ventral margin is almost parallel to the
posterior, the anterior margin only slightly produced dorsally, and the posterior
margin slightly produced ventrally. The shell is massive and strong. Concentric
striation is distinct, uniformly arranged, and even visible in live larvae. The
umbones are distinct — broad, round, and moderately high. The hinge system
is similar to that in the family Mytilidae but the smaller teeth in the central
part of the provinculum are either not visible or very weakly developed. The

79

Figure 54: General view (A) and hinge of right valve (B) of the veliconcha of Musculista
senhousia; general view (C) of the veliconcha of Arca boucardi.

80

hinge line of these Adula bears 12—13 large lateral teeth (see Figure 43). The
larva is opaque, brownish. The large dark red eyes are very distinct. The shell
of the veliconcha is 320—350 tm long. The larva of A. falcatoides is very
similar in structure to the larva of A. simpsoni described by Rees (1950) from
the North Sea.

Ecology

Larvae of A. falcatoides are observed in the second half of summer in
Vostok Bay, mainly in August, at a water temperature of 18—20°C.

No data on the morphology and ecology of this species were found in the
literature.

BOUCARD’S ARCA, ARCA BOUCARDI JOUSSEAUME
(Arcidae)

Veliconcha

The shell is equivalve and round, with its anterior margin narrower than
the posterior (see Figure 54, C). The umbones form at a shell length of more
than 150 um; they are broad, not exceeding the hinge line in length, but equal
to it. In a developed veliconcha, there are six large lateral teeth along each
margin of the hinge line and ten central teeth, which are half the height of the
lateral; thus there are eight teeth on each side. The provinculum is devoid of
teeth. Large bright eye spots appear in larvae 210 um long. Larvae settle with
an average shell length of 224 bm.

Ecology

Arca larvae are found in the plankton of Vostok Bay (Peter the Great Bay)
in July-August.

The morphology of Boucard’s arca has been reported by Kulikova and
colleagues (1987).

GIANT OYSTER, CRASSOSTREA GIGAS THUNBERG
(Ostreidae)

Veliconcha

The shell is inequivalve. The left valve differs from the right in shape and
size, being larger, more convex, and having a very well-developed umbo that
is much higher than on the right valve. The right valve is smaller than the left,
flattened, and with a low, round umbo. The height of the shell is somewhat
greater than its length. The anterior margin is longer than the posterior. The

81

hinge comprises three anterior and two posterior rectangular teeth (see Figure
37). The height of each anterior tooth is twice that of the posterior teeth. The
space between the anterior and posterior teeth is smooth. The ligament is
posterior. Eyes are present; they develop and become distinct at a shell length
of 250-270 um. Concentric and radial striations are equally well-developed on
both valves. In the umbonal region, the larva has a large black spot that
corresponds to the digestive gland. The larva attains the veliconcha stage at a
shell length of 100-120 um and a hinge line length of 50 tum. As the veliconcha
grows, the length of the hinge line increases to 65 um.

The larva of C. gigas, like the larvae of C. virginica and of C. angulata,
but unlike those of C. glomerata and C. cucullata, has an asymmetrical shell.
The umbo is shifted back, the anterior margin more drawn out ventrally and
larger, the three anterior teeth are two to three times longer than the posterior,
and the entire provinculum is short.

Ecology

Along the southern Sakhalin coast (Aniva Bay, Sea of Okhotsk), spawning
and development of oyster larvae in the plankton occurs in the warmest period
of the year, i.e., July—September, at a water temperature of 16—22°C. In
Vostok Bay, gamete release is observed from the second half of June to the
first half of August (Kasyanov ef al., 1976, 1980). In Posjet Bay, larvae are
found from June to September (Rakov, 1975), becoming maximum in July—
August. In Vostok Bay, larvae are mainly found in the plankton in August. The
duration of the pelagic phase of C. gigas in Peter the Great Bay is, on average,
26—28 days. A similar duration of this stage in the giant oyster has been
reported by Thorson (1946) and His and Kriaris (1972) in the North Sea and
in experimental culture.

Many works (Hori, 1926; Funita, 1933; Cahn, 1950; Loosanoff and Davis,
1963; Loosanoff et al., 1966; Rakov, 1974) have described the structure of the
larval shell of C. gigas, size characteristics, and methods of obtaining and
culturing larvae. Le Pennec (1980) examined the ontogenetic development of
the hinge of oysters. Data on the ecology of larval development are available
in the works of Korringa (1957), Thorson (1946), His and Kriaris (1972), and
Kulikova (1975, 1979).

CHLAMYS FARRERI NIPONENSIS KURODA
(Pectinidae)
Veliconcha

The maximum size of the larval shell is 220-230 um with a provinculum
100-110 um long. The shape of the shell of the Japanese scallop is typical of

82

the family, triangular-ovate. The valves are convex. The anterodorsal margin
slopes downward and hence the anterior end of the larva is raised and some-
what pointed. The umbones are small and round. The shell is inequivalve, with
the right valve slightly more massive than the left and its umbo somewhat

Figure 55: Veliconcha of Chalmys farreri nipponensis.
A — external view; B — right (1) and left (2) valves; C — hinge of right (1) and left (2) valves.

83

Figure 55 (contd.)

larger. Both valves are compact. Sculpture on the shell is indistinct. The
provincular margin of C. f niponensis bears five rectangular denticles. The
central part of the provinculum lacks teeth; the length here is almost equal to
the marginal areas bearing teeth (Figure 55). The margin of the shell is edged
with a moderately wide, distinct band.

Ecology

In Peter the Great Bay, larvae of this scallop are found from the end of
June to early August at a water temperature of 15—20°C. Larvae settled in mid-
July.

Kulikov, Medvedeva and Guida (1981) describe the structure of the shell
and of live larvae of this scallop. They present the characters that differentiate
the larvae of this species from those of Mizuhopecten yessoensis and Swiftopecten
swifti.

84
SWIFTOPECTEN SWIFTI (BERNARD)
(Pectinidae)

Veliconcha

The maximum length of the larval shell is 240—250 um and the length of
the hinge line 120—130 um. The shell is triangular and the valves are convex.
The anterodorsal margin slopes sharply downward. The umbones are high and
acute. The larval shell is stout and richly colored. Radial striation is indistinct,
while concentric striation is distinct. A broad marginal band is visible along
the entire edge of the shell. The hinge line in a developed larva has up to seven
large marginal teeth. The ligament is median and slightly shifted toward the
anterior margin (Figure 56).

Ecology

Larvae of this scallop are found en masse in the plankton of Busse Lagoon
(southern Sakhalin) and Peter the Great Bay during August—September at a
surface water temperature of 15—20°C. Typically, these larvae are dominant
near-bottom at depths of 10—20 m.

The morphology of larvae of Swiftopecten swifti has been described by
Kulikov, Medvedeva and Guida (1981). No data on the ecological develop-
ment of this species were found in the literature.

MIZUHOPECTEN YESSOENSIS (JAY)
(Pectinidae)

Veliconcha

The larval shell is 260—270 tum long and the provinculum 100—110 um
long. The veliconcha shell of the Primorsk scallop is triangular-ovate. The
anterior margin is short, round, and sharply drawn dorsally. The anterodorsal
margin is longer than the posterior and almost straight due to the highly raised
anterior end. The posterodorsal margin slopes sharply downward and gradually
merges with the posterior margin of the shell. The umbo is small, round, and
slightly raised over the hinge line. The larva is almost colorless and transpar-
ent. The shell is brittle, with distinct concentric and radial striations. The hinge
is of the taxodont type, bearing rectangular teeth along the margins of the
provinculum. A well-developed larva has five teeth on each side of the hinge
row (see Figures 38 and 57).

Figure 56: Veliconcha of Swiftopecten swifti.
A — external view; B — left valve; C — hinge of right (1) and left (2) valves.

85

86

Figure

87

Fi es : 2
gure 57: Hinge of right (1) and left (2) valves of the veliconcha of Mizuhopecten yessoensis

88

Ecology

In Busse Lagoon (southern Sakhalin), spawning of M. yessoensis and
development of larvae in the plankton are observed from early July to early
August. In Peter the Great Bay, larvae are found in the plankton for two
months, from June to July, at a water temperature of 8—18°C. Their number
is maximal from mid-June to mid-July. Duration of the pelagic stage of devel-
opment of the scallop varies from 20—40 days.

The morphology of M. yessoensis larvae has been described by Yamamoto
(1964), Maru (1972), and Kulikova, Medvedeva and Guida (1981). Data on the
ecology of larval development of this species along the coast of Japan and in
Mutsu Bay are available in Yamamoto’s work (1951). The ecology of the
larvae of this scallop along the southern Sakhalin coast was described by
Kulikova and Tabunkov (1974) and for Peter the Great Bay by Belogrudov
(1973, 1974).

HIATELLA ARCTICA LINNE
(Hiatellidae)

Veliconcha

The shell of the veliconcha is triangular. The anterior, posterior, and
ventral margins are roundish, with the anterior margin more stretched than the
posterior. The shoulders are straight, long, and slope steeply toward the ventral
surface. The umbones are high and round. One tooth each is present on the
right and left valves. The ligament is posterior (see Figures 48 and 58). The
maximum shell length of the pelagic larva is 380—400 um.

Ecology

In Busse Lagoon (southern Sakhalin), pelagic larvae of this species are
found from early September to early October at a water temperature of 15—
18°C. In Vostok Bay, larvae of H. arctica occur in the plankton in September.
In the southern Adriatic (Poggiani, 1968), H. arctica reproduces from January
to June—July at temperatures ranging from 6.0—23.5°C. Reproduction is maxi-
mum in March — first half of May at temperatures of 11—16 °C. In the
northern Adriatic (Brenco, 1971), larvae of H. arctica are found in the plank-
ton year-round, but are maximum in May—June. In Plymouth (La Mancha
Strait), H. arctica larvae have been found in the plankton from early summer
to December (Lebour, 1938). In Danish waters, according to Jorgensen (1946),
pelagic larvae of this species are abundant from July to September—November.
Along the eastern coast of Greenland (Ockelmann, 1958), this species repro-
duces from May to June.

Figure 58: Hinge of right (1) and left (2) valves of the veliconcha of Hiatella arctica.

90

Data on the morphology of H. arctica larvae in the veliconcha stage are
available in works by Odhner (1914), Lebour (1938), Jorgensen (1946); and
Rees (1950). Reports on the ecology of reproduction of this species are quite
numerous (see above).

KELLIA JAPONICA PILSBRY
(Kelliidae)

Veliger and Veliconcha

The larvae of Kellia are lecithotrophic and the pelagic period is brief.
Veligers with a straight hinge at a shell length of over 150 um, emerge from
the mantle cavity of females into the plankton. The veliconcha shell is equivalve,
round, and flat. The anterior margin is ventrally drawn. Umbones are lacking.
The dorsal margin remains almost flat. The larval valves are brittle, transpar-
ent, and display weak concentric striation. The larva is yellowish-green.
Provincular teeth are absent. The ligament is centered in the dorsal margin (see
Figures 39 and 59). The shell of a swimming larva is 360—380 1m long.

Ecology

Along the southern Sakhalin coast (Aniva Bay, sea of Okhotsk) and in
Vostok Bay, larvae of Kellia have been found in the plankton in the second
half of summer at water temperatures of about 16—23°C.

No data on the morphology and ecology of larvae of this species were
found in the literature.

Figure 59: Hinge of left valve of the veliconcha of Kellia japonica.

KEENOCARDIUM CALIFORNIENSE (DESHAYES)
(Cardiidae)

Veliconcha

The description of this species corresponds to that of the entire family.
The shell of the swimming larva reaches 280—300 fm in length, on average
(see Figure 51).

91

Ecology

K. californiense larvae are found in the plankton of Peter the Great Bay
in August—September.

No data on the development of this species were found in the
literature.

BALTIC MACOMA, MACOMA BALTHICA (LINNE)
(Tellinidae)

Veliconcha

The length of the veliconcha shell is initially slightly more than its height.
The anterior shoulder is much longer than the posterior. The larva lengthens
as it grows due to the extension of its anterior end (see Figure 42). The
maximum size of the larval shell is 300—315 um.

Ecology

In Vostok Bay (Peter the Great Bay) and in Busse Lagoon (southern
Sakhalin), this species reproduces from July to September at 17—24°C. In
other parts of its area of distribution, reproduction of the species also occurs
in the warmer part of the year—in spring and summer. Along the Danish
coast, the veligers of M. balthica are found (J@rgensen, 1946) in the plankton
from April-May to mid-August. In the Great Salma Strait, macoma larvae are
found in July at 7—11°C (Mileikovskui, 1960).

The larva of M. balthica has been described by Werner (1939), Jorgensen
(1946), and Sullivan (1948).

TALL SILIQUA, SILIQUA ALTA
(BRODERIP AND SOWERBY)

(Cultellidae)

Veliconcha

The description of this species corresponds to that given for the family.
The shell is pale yellow, almost white, its surface smooth, and the anterior part
thinner than the posterior. The shell is slender, semitransparent, and not broad.
The shoulders are straight and slope somewhat ventrally. The maximum length
of the larval shell is 380 tum (see Figure 50).

Ecology
In Busse Lagoon (Sea of Okhotsk), S. alta larvae appear in the plankton
mid-July. Their number is maximum in August. Mass settling of larvae occurs

92

from the end of August to early September. Their size at this time varies from
300 to 380 um. The temperature at which S. alta larvae are found in the
plankton ranges from 11—22°C. Mass settling coincides with autumn cooling
of waters. In Vostok Bay, development of larvae occurs in the same period at
a similar temperature.

Hayashi and Terai (1964) have described the morphology of larvae of this
species.

RAZOR CLAM, SOLEN KRUSENSTERNI SCHRENCK
(Solenidae)

Veliconcha

The description of this species is similar to that given for the family. The
shoulders of the larva are roundish and merge smoothly with the line of the
anterior and posterior margins of the shell: The maximum shell length of a
swimming larva is 350 um (see Figure 49).

Ecology

Larvae of razor clams are found in Busse Lagoon and Vostok Bay (Peter
the Great Bay) at the beginning of summer (May—June).

No data on the morphology and ecology of larvae of this species were
found in the literature.

CHINESE MACTRA, MACTRA CHIENENSIS PHILIPPI
(Mactridae)

Veliconcha

The maximum length of the larval shell is 260-270 um. The shell is oval-
‘triangular and somewhat truncate from the posterior end. The umbones are
high and somewhat shifted to the posterior end. The shoulders are round and
high (see Figures 46 and 60). The hinge system comprises one rectangular
tooth on the right valve and two on the left. The ligament is situated at the
posterior end of the hinge line. The anterior part of the dorsal edge of the left
valve has one lobate tooth. The lateral teeth along the hinge resemble tubercles
on both valves.

Ecology

In Peter the Great Bay, larvae of Mactra chinensis appear in large num-
bers in July. Settled juveniles are found in shallow sandy open inlets well-
warmed by the sun.

93

The shell of juveniles of M. chinensis is lustrous yellow and trihedral. The
posterior part of the body has two transparent siphons and a well-developed
foot that enables the mollusk to move quickly over the seabed.

Miyasaki (1933) has described the development of Mactra chinensis;
however, data are quite fragmentary. Larvae and juveniles of this species are
described by Hayashi and Terai (1964), including the hinge of the planktonic
larva and its external appearance. The early development of Mactra chinensis
has been described by Medvedeva and Malakhov (1983).

SPISULA SACHALINENSIS (SCHRENK)
(Mactridae)

Veliconcha

The larva attains this stage at a shell length of 300 um. The shell is
equivalve, ovate, and obtuse at the posterior end; the anterior part is flattened.
The anterior end is larger than the posterior. The umbones are low, broad, and
shifted to the posterior end. The shoulders slope gently (Figure 61). The hinge
begins to form in the larva when the umbo appears. Initially, the hinge consists
of two primary plates with small denticles separated by a deep pit. Later, the
denticles on the primary plates disappear and the plates become massive. A
lobate tooth is present in the anterior part of the hinge of the left valve. The

Figure 60: Veliconcha of Mactra chinensis.
A —right valve; B — hinges of right (1) and left (2) valves.

tf

.

ih
Hi

La)
ri

i
Hal
i

Figure 60 contd.

Figure 61: Veliconcha of Spisula sachalinensis.
A — left valve; B — left hinge (1) and right valve (2).

95

96

Figure 61 (contd.).

lateral teeth resemble tubercles on both sides of the hinge. The right valve has
two indentations corresponding to the primary plates of the left valve. The
ligament is triangular and posterior.

Ecology

In Peter the Great Bay, larvae of Spisula sachalinensis appear at the end
of June and are most numerous in mid-July. Larvae settle in shallow water,
sandy inlets, well-warmed by the sun. Freshening of water adversely affects
the young of the year population (Tabunkov, 1971).

Hayashi and Terai (1964) have described external changes in the pediveliger
after settling. Medvedeva (1981) gives a brief description of changes in the
hinge during larval growth. Some information is also available on rearing
larvae of S. sachalinensis in the work of Imai and coworkers (1950).

oF,

PHILIPPINE RUDITAPES, RUDITAPES PHILIPPINARUM
(ADAMS AND REEVE)

(Veneridae)

Veliconcha

The anterior end of the shell is slightly longer than the posterior. The
shoulders are straight, slope steeply, and reach almost up to the middle of the
anterior and posterior margins. The umbones are broad and triangular-roundish
(see Figure 47). Concentric striation is distinct. The hinge system of the larva
at the veliconcha stage is represented by a row of denticles, generally num-
bering 12—14. The ligament is large and posterior. The length of the veliconcha
shell increases with the growth from 160 to 244 tm; its height is slightly less
than its length. The maximum length of the hinge line is 85 Um.

Ecology

In Vostok Bay (Peter the Great Bay), the larvae of this species are found
in July-August, and in Busse Lagoon (southern Sakhalin), in August—early
September, at a temperature of 15—23°C and 10—20°C respectively.

The larvae of Ruditapes have been described by Yoshida (1935).

MYA JAPONICA JAY
(Myidae)

Veliconcha

The shell is equivalve, with the posterior end somewhat shorter than the
anterior. The posterior margin is broad and slopes from the shoulders in a
straight line to the ventral margin. The anterior margin is narrow and round.
The shoulders are straight, broad, and slope downward. The shell length is
almost equal to its height. The umbo is initially indistinct and appears trian-
gular, its line margin with the line of the shoulders. Later, before the larva
setiles, the umbo becomes roundish and distinct. The hinge system is weakly
differentiated. One provincular tooth is present on each valve. The ligament is
posterior. Weak concentric striation is distinguishable on the hollow valves of
the shell of the veliconcha. One of the main distinguishing characters of the
veliconcha of M. japonica is the presence of dark pigmentation on the soft
parts of the body in the region of the anterior and posterior muscles (retractors)
and along the velar margin (see Figure 45). Along the coasts of Primor’e, the
shell of the swimming larvae of M. japonica is 85-270 um long. Individual
specimens reach 300-320 um. Larger larvae have been recorded along the

98

Figure 62: Right valve of the veliconcha of Mya japonica.

coast of Japan (Yoshida, 1938). Larvae attain the veliconcha stage at a shell
length of 150 um and a hinge line of 50-70 um.

Ecology

In Sakhalin (Aniva Bay, Sea of Okhotsk), the spawning period of M.
japonica is protracted, beginning in early July and ending at the terminating
end of August or early September. The major part of the M. japonica popu-
lation usually spawns in Busse Lagoon (Aniva Bay) in July—beginning of
August. Spawning commences at a temperature of 14—15°C and larvae are
present in the plankton at a water temperature of 15—22°C. In Vostok Bay,
larvae of M. japonica are found in the plankton during June—July at tempera-
tures of 14—22°C.

Data on the morphology and ecology of larvae of this species are available
in the works of Yoshida (1938, 1953).

TRUNCATE MYA, MYA TRUNCATA (LINNAEUS)
(Myidae)

Veliconcha

The larva of Mya truncata is identical to that of M. japonica, both in
structure of hinge system and presence of dark pigmented bands along the
shoulder as well as the mantle margin. The only noticeable difference between
these two species 1s the larger size of the M. truncata larvae (90—320 Um) and
significant elongation longitudinally (see Figure 45).

99

Ecology

Larvae of this species are found in Vostok Bay (Peter the Great Bay) in
July—August at a temperature of 15—23°C.

The larva of M. truncata has been described by Jorgensen (1945) and Rees
(1950).

SHIPWORM, TEREDO NAVALIS LINNE
(Teredinidae)

Veliconcha

Larvae enter the plankton at the stage of straight hinge. The veliconcha
shell is equivalve, equilateral, oval, and dorsoventrally produced. The valves
are so highly convex that the larva is almost spherical. The shoulders are short,
round, and slope steeply. The umbones are narrow, high, and round. Striation
is concentric and distinct. A dark band occurs along the entire margin of the
shell and encloses a light-colored band. The shell is heavy and thick. The larva
is dark, brown, and opaque. The soft body of a live larva has both red and
green pigmentation. The height of the veliconcha shell is much greater than
its length (/-/ ratio 1.00:1.13). The left valve of the veliconcha has two teeth
identical in shape and size. The right valve has three teeth, of which the
median tooth is broader than the lateral ones (see Figures 40 and 63). The
hinge line is 4—55 tm long and the larval shell 70—220 um (Sullivan, 1948);
Imai et al., 1950; Loosanoff et al., 1966; Chanley and Andrews, 1971). Velig-
ers released by the female vary in length from 70—90 um. The umbones appear
at a shell length of 100 tm. Metamorphosis usually begins at a shell length
of 200 tm but may begin at other shell sizes as well: 200 m x 231 m
(Loosanoff et al., 1966) and 220 um x 250 um (Sullivan, 1948).

Ecology

Duration of the pelagic stage of development of T. nevalis varies from
region to region. At a temperature of 20°C, metamorphosis begins 28 days
(Loosanoff et al., 1966) or 24—35 days (Grave, 1928; Imai et al., 1950) after
fertilization.

Larvae occur in the plankton along the coast of southern Sakhalin (Sea of
Okhotsk) and in Peter the Great Bay in the warmest months of the year — May
to September — at temperatures of 15—23°C.

Because of its universal distribution, the morphology and ecology of lar-
vae of T. navalis have been described in many works (see above).

100

Figure 63: Hinge of right (1) and left (2) valves of the veliconcha of Teredo navalis.

101
BANKIA SETACEA (TYRON)
(Teredinidae)

Veliconcha

The veliconcha shell is equivalve and symmetric. In the initial period of
this stage the larva is round; as the shell grows and the umbones become
isolated, the shell expands dorsoventrally but is never as highly drawn as in
T. navalis. Compared to the latter, the shell of Bankia setacea is thinner and
also transparent. The larva is entirely light-colored and devoid of bright pig-
mentation. Dark and light bands occur along the margin of the shell. The hinge
system is identical to that of 7. navalis (Figure 64). The prodissoconch I varies
in length from 100-130 wm. The larval shell before settling varies in length
from 240-280 um, with a hinge line of 100 um (Quayle, 1953).

Ecology

In Busse Lagoon, Aniva Bay (Sea of Okhotsk), and Vostok Bay, release
of gametes and development of larvae in the plankton occur in warmer months
of the year (July-September) — at 14—17°C in Busse Lagoon and 15—23°C in
Vostok Bay. During the autumn, as the water cools to 7—10°C, larvae settle and
metamorphose. Judging from published data, B. setacea exhibits similar eco-
logical characteristics in other parts of its range. Ryabchikov (1957) recorded

Figure 64: Veliconcha of Bankia setacea.

102

autumn settling of larvae along the eastern coast of Sakhalin at temperatures
of 7—12°C. In Preobrazheniya Inlet (southern Primor’e), according to Adrianov
and Vol’ter (1947), mass metamorphosis is observed twice a year: spring
(March) and autumn (October—November). In southern Californian waters,
Coe (1941) reported reproduction of B. setacea at temperatures of 10—15°C
with an additional spawning period in winter and summer. In San Francisco
Bay (Kofoid and Miller, 1927), the season for release of gametes begins in
February at a minimum temperature of 10°C and ends, for the most part, before
the beginning of summer, peaking in April—May. Northward, along the coast
of Washington (USA) and Canada, the optimum temperature for settling is that
in October-December, 1.e., 8.0—9.5°C (Johnson and Miller, 1975). In British
Columbia (western coast of Canada), this species reproduces at temperatures
from 12 to 15°C, with maximum larval numbers observed at depths of more
than 6.0 m, where the water is warmer (14—17°C) (Quayle, 1959). Thus, the
temperature range for reproduction of this species throughout its area of dis-
tribution is 8—17°C. The pelagic stage of development of B. setacea in the
coastal waters of British Columbia and in southern Californian waters (Quayle,
1953; Coe, 1941) continues for 20-30 days. Our observations in Busse Lagoon
(southern Sakhalin) established an identical period of development.

Quayle (1953, 1955, 1959) has described the structure of larvae of B.
setacea. The ecology of larvae of this species has been thoroughly studied (see
above).

CRISPATE ZIRPHAEA, ZIRFAEA CRISPATA (LINNE)
(Pholadidae)

Veliconcha

Initially roundish, the shell then stretches dorsoventrally, as a result of
which its height becomes slightly more than its length. The shoulders start to
slope steeply and the anterior shoulder is somewhat longer than the posterior.
Concentric striation is conspicuous. Before metamorphosis, a tooth on one
valve and a corresponding notch on the other appear on the ventral margin of
the shell, forming a firm lock (Figure 41 A, B). The hinge system is repre-
sented by two 5—10 um broad teeth on the left valve, with a broad (20—25
tm) tooth situated between them on the right valve; a second small tooth
forms at the anterior end of the right valve before metamorphosis. A fully
grown larva is 300 um long, 285 tm wide, and has a hinge line 68 um in
length.

103

Ecology

Larvae of Zirfaea are found in the plankton of Busse Lagoon (southern
Sakhalin) and Peter the Great Bay in small numbers and are seen in August—
October at a temperature of 10—20°C. In Sond Strait (Ersund) in Danish
waters, larvae of Z. crispata are found in the plankton throughout the year,
except in March, April, and May. The maximum number is observed at the end
of summer—early autumn.

The morphology of the larvae of Z. crispata has been reported in many
works (Werner, 1939; Jorgensen, 1945; Sullivan, 1948; Rees, 1950).

JAPANESE BARNEA, BARNEA JAPONICA (YOKOYAMA)
(Pholadidae)

Veliconcha

Larvae large and roundish. The shell margin is broadly oval. The shoul-
ders are short and roundish, with the anterior shoulder slightly longer than the
posterior. The umbones are narrow and high (see Figure 41 C). The hinge line
is short. Concentric striation is visible on the hollow valves. A marginal band
is present. The central tooth on the right valve is two to three times longer than
the short front tooth. Before metamorphosis, another smaller tooth becomes
distinct on the right valve behind the large tooth.

Ecology

Larvae of Barnea are found in the plankton of Vostok Bay (Peter the Great
Bay) in the warmest months of the year, 1.e.,. July—August, at a temperature
of 15—20 °C.

The larva of this species is not described in the literature.

CHAPTER II

LARVAE OF SEA STARS
(MORPHOLOGY, PHYSIOLOGY, BEHAVIOR)

EARLY DEVELOPMENT

Egg

Eggs of sea stars have a diameter ranging from 100 to 3,540 um (see
Table on p. 105). From an egg of minute diameter containing very little yolk,
a definitive sea star develops after passing through larval stages of dipleurula,
bipinnaria, and usually branchiolaria, with subsequent metamorphosis. Larger
eggs bypass the stages of dipleurula and bipinnaria and often, in such cases,
a lecithotrophic modified brachiolaria develops, followed by metamorphosis
into a definitive sea star. In many species, larval stages are eliminated alto-
gether and development is direct (Pteraster militaris) (Kaufman, 1968; and
others). Sea star eggs with little yolk are often colorless, almost transparent.
Eggs containing many nutritive substances may be yellow, pink, orange, or
brown. Ovulation and shedding of eggs usually occur immediately before
metaphase I maturation division. In sea water oocytes are capable of “matu-
ration” without fertilization, i.e. proceeding from prophase I maturation divi-
sion (with intact germinal vesicle) to metaphase I, and then separating polar
bodies I and II. With rare execptions, the eggs of sea stars are shed directly
in water.

Egg membrane : Each egg is enclosed in a thin hyaline membrane sur-
rounding a vitalline and an exterior jellylike membrane. The jellylike mem-
brane is 5—20 um thick. In most species it is apparently present only up to
the beginning of cleavage, of soft consistency, and destroyed when eggs are
passed through a capron net. In some species the jellylike membrane is
relatively thick and sticky, and hence a batch of eggs can adhere to the
substrate.

105

Diameter of eggs of sea stars

Species Diameter Source
of eggs, um
Pentaceraster mammillatus about 100 Mortensen, 1937
Asterias amurensis about 100 Dautov and Kasyanov, 1981
Asterias sp. 110 Costello et al., 1957
Ophidiaster guildingii 110-120 Mortensen, 192]
Pycnopodia helianthoides 120 Greer, 1962
Stichaster australis 120—140 Barker, 1978
Odontaster validus 130 Pearse, 1969
Asterias rubens 120—150 Kaufman, 1977
A. rubens 160-190 Gemmill, 1914
Concinasterias calamaria 140-160 Barker, 1978
Pisaster ochraceus 160 Strathmann and Vedder, 1977
Sclerasterias richardi 170 Falconetti et al., 1978
Patiria pectinifera 170 Dautov and Kasyanov, 1981
Astropecten scoparius 230 Oguro et al., 1976
Astropecten latespinosus 250-400 Komatsu, 1975
Patiriella exigua 400 Lawson-Kerr and Anderson, 1978
P. calcar 400 Lawson-Kerr and Anderson, 1978
Asterina coronata 420 Komatsu, 1975
A. batheri 430 Kano and Komatsu, 1978
A. minor 430—500 Komatsu, 1976
A. burtoni 450-500 James, 1972
A. gibbosa 500 McBride, 1896
Urasterias lincki 700 Kaufman, 1977
Crossaster papposus 700 Kaufman, 1977
Leptasterias hexactis 800 Chia, 1968
Solaster endeca 800—1 ,000 Gemmill, 1912
Echinaster echinophorus 800—1 300 Atwood, 1973
Fromia ghardaquana about 1,000 Mortensen, 1937
Echinaster sepositus 1,000 Nachtsheim, 1914
Henricia sanguinolenta 1,000 Kaufman, 1977
Pteraster militaris 1,000 Kaufman, 1977
Mediaster aequalis 1,000-1,200 Birkeland ef al., 1971
Notasterias armata 3,540 McClintock and Pearse, 1986

Fertilization : Insemination and subsequent fertilization usually occur
between the dissolution of the germinal vesicle and the separation of polar
body I. The spermatozoa of sea stars are acrosomal and during fertilization
an acrosomal reaction of the spermatozoon occurs, whereby the acrosomal
filament of the spermatozoon penetrates the jellylike membrane and comes
into contact with the egg (J.C. Dan, 1970). This is followed by a cortical
reaction in the egg; one morphological manifestation of this reaction is the
extrusion of the contents of cortical granules into the perivitelline space
between the egg and the vitelline membrane, and the latter being modified
into a fertilization membrane. The vitelline membrane detaches from the

106

surface of the egg in a few minutes and enlargement of the perivitelline space
continues up to commencement of cleavage (Kume and Dan, 1968).

Cleavage: About |—2 hr after fertilization, cleavage begins, which is
usually radial in echinoderms. The first two cleavage furrows are meridional
and the third equatorial (Figure 65). The somewhat unequal size of the first
blastomeres in some species of sea stars, indicates weakly expressed bilateral
cleavage (Field, 1892; Gemmill, 1914; Kasyanov, 1977). Although the first
cleavages in general are synchronous, strict synchronization of cleavage is not
observed. In sea stars the blastomeres are usually very loosely bound to each
other right up to the formation of the coeloblastula. The characteristic divi-
sion into macro-, meso-, and micromeres of the sea urchin embryo is absent
in sea stars.

As a result of cleavage, a morula or blastula with rather loosely bound
blastomeres forms (Figure 66) and then a coeloblastula with an extensive
blastocoel and firmly adhering blastomeres (Dan-Sokhawa, 1977). The ab-
sence of completely radial division is a distinguishing feature of Fromia

Figure 66: Blastula of Patiria pectinifera. A—blastomeric blastula; B—coeloblastula.

107

ghardaquana (Mortensen, 1938). In this sea star cytotomy (cell division) is
preceded by repeated division of the nuclei; the latter then migrate to the
periphery of the egg and initially form a single layer that becomes multilay-
ered. Separation of the cellular boundaries in the embryo of F. ghardaquana
continues for a long time. Delayed cytotomy, compared to nuclear division,
characterizes the large eggs of Henricia saguinolenta. In the deepwater
Aspidodiadema jacobyi, at the blastula stage the egg yolk lies under the
blastoderm (Young and Cameron, 1987). In many sea stars (especially in
astropectinids and many asterinids), there are surface folds on the morula or
blastula which are smoothed with the emergence of the blastula from the
vitelline membrane. Shedding of the membrane, i.e., changing over to a free
larval life, occurs very early in echinoderms and especially in sea stars. The
first larval stage is the late blastula in some species of sea stars or the early
gastrula in others.

Gastrulation : Gastrulation begins soon after hatching or not long before
it. It is preceded by some flattening of the blastular walls at the vegetal pole
(Figure 66). Invagination of the cell layer begins at the site of flattening
(Figure 67). A long narrow archenteron forms and from its base expulsion
of the mesenchymal cells begins, which have long filopodia touching the cells
in the wall of the blastocoel (Figure 68). Later, the archenteron becomes
mushroom-shaped. The cavity of the “stalk” is lined with cndodermal cells
and the cavity of the “cap” (the future coelomic cavity) is bordered by
mesodermal cells. The primordium of the mesoderm divides into two closed

20 um:
————

Figure 67: Gastrula of Patiria pectinifera. Figure 68: Archenteron of the gastrula of
Pisaster ochraceus (from Chia, 1977).

108

vesicles that lie along the sides of the intestine — the left and right coeloms.
Each coelom later divides into three parts — anterior (axocoel), middle
(hydrocoel), and posterior (somatocoel); the left coeloms are better devel-
oped. Such is the typical picture. But in some species, the formation of
coeloms may be accelerated by independent formation of the left somatocoel
(in Patiria miniata— Heath, 1917; Henricia sanguinolenta — Masterman,
1902; Solaster endeca and Crossaster papposus —Gemmill, 1920). The di-
gestive tract at this time has only one opening — the blastopore.

Dipleurula

Before the formation of the mouth, the ecto-
derm of the anterior part of the ventral side of
the larva flattens. A small depression forms here,
1.e., the stomodeum primordium, and the tip of
the gut bends in this direction. Cells of the ec-
toderm and endoderm merge and form the mouth

Figure 69: Early opening. The blastopore becomes the anal open-
bipinnaria of Astropecten ing and shifts position to the ventral side. The
auranciacus (from

mouth opening is situated in the perioral depres-
sion and is edged with a ciliated band (Figure
69). This stage is called the dipleurula. In front of the perioral depression
rises the preoral plate and behind it, the anal plate with the anal opening.
These raised plates are edged with a better developed ciliary cover compared
to the remaining surface of the larva. Ciliated cells lying along the edge of
the preoral plate later produce the preoral ciliated band, while ciliated cells
lying along the edge of the anal plate are the primordium of the postoral
ciliated band that extends from the bottom upward, along the dorsolateral
margins of the larva. The ciliated bands merge at the anterior end of the larva
but later separate here (Figure 70).

Ho6rstadius, 1939).

Bipinnaria

Further development of the trapping and locomotor apparatus — the cili-
ated bands —transforms the dipleurula into a bipinnaria. These bands of
complex configuration pass along the elongate transparent body of the bipinnaria
and over numerous body projections (arms/processes) (Figure 71).

Feeding : Strathmann (1974) has noted that the body of a planktotrophic
larva is primarily a temporary structure for feeding. The digestive system
comprises the mouth cavity, esophagus, stomach, a very short, thin intestine,
and a thick intestine that terminates in the anal opening. Like the larvae of
bivalves, the larvae of sea stars feed on food particles suspended in the
surrounding water. Feeding involves the creation of water currents, separation

109

of food particles from the water, transportation of the same to the mouth, and
ingestion (Werner, 1959).

Evidently, larvae of sea stars do not possess chemoreceptors, which would
discern the quality of the food ingested, since they ingest not only unicellular
algae but also coal particles (Dautov, 1979). The perioral depression or the
oral field participates in the capture of food but the main trapping apparatus
is the ciliated bands — the small preoral band, the postorai edging the entire
body (except the preoral plate), and the adoral band bordering the oral open-
ing. The preoral band passes into the medioventral and the two preoral pro-
jections (arms), while the postoral band passes into the mediodorsal and
paired postoral, posterolateral, posterodorsal, and anterodorsal projections
(arms) (see Figure 71). The degree of development of any projection is
considered when determining the species affinity of a larva. In some species
of sea stars the ciliated band is barely discernible on the projections (arms)
(Asterias, Pisaster, Pycnopodia); in others (Patiria, Luidia) it is quite distinct
(Strathmann, 1971). The ciliated band reaches the maximum length in the
bipinnaria of Luidia (Figure 72) (Meek, 1927; Strathmann, 1971; Wilson,
1978). The adoral band forms two strands passing along the ventral side of
the esophagus and forms a long stretched loop. In the larvae of sea stars the
entire outer surface of the body is armed with individual cilia.

Figure 70: Bipinnaria of Patiria miniata (from Strathmann, 1971).
pocb--postoral ciliated band; prcb—preoral ciliated band.

110

Ciliated bands range from 20-30 um
in length. The band is about ten cells wide
and each cell bears one cilium. Cells bor-
dering the ciliated band secrete a mucus
(Tattersall and Sheppard, 1934; Strathmann,
1971). Such cells occur on the aboral side
of the band and are absent in the oral field.
Cilia beating at right angles to the ciliated
band create a water current directed away
from the perioral field, which moves the
larva forward. A flow is thereby created in
front and from the sides, which is directed
toward the perioral field. Food particles
trapped on the ciliated band are transported
by it and the cilia of the perioral field to
the mouth. The mechanism of filtration of
particles by the ciliated band is presumably
as follows: Particles of sufficient size which
touch the cilia of the band during active

ans ae Bay beating (directed from the perioral field),
gute ieee Geena ea ee: mechanically or chemically induce a local
adp — anterodorsal proiecnon (arm); temporary reversal of beating of the cilia
mdp — mediodorsal projection (arm); touched. The particles captured in this
mvp — medioventral projection (arm); movement are transported to the perioral
pdp — posterodorsal projection (arm); field and then to the mouth. Once these
plp — posterolateral projection (arm); j
pop—postoral projection (arm), Particles have been transferred to the
prop — preoral projection (arm). perioral field, the initial direction of effec-
tive ciliary beating is resumed. Some par-
ticles may be trapped directly by cilia in the perioral field, bypassing the
ciliated band. These particles reach the oral cavity through the upper and —
lateral areas of the adoral band. The cilia of these areas, like those of the
esophageal loop of the band, beat in the direction of the intestine. Transpor-
tation of food particles toward the mouth is facilitated by the secretion of the
mucous cells located alongside the ciliated band. Food particles entering the
mouth cavity may remain there for over 20 min, congealing into a compact
mass; individual particles pass through the mouth cavity without stopping and
enter the esophagus (Strathmann, 1975). Coal particles added to the culture
of bipinnariae of Aphelasterias japonica were detected in the esophagus after
50—60 sec, and in the stomach after 2 min (Dautov, 1979).

All sections of the digestive tract are lined with ciliated cells that assist
in the passage of food particles. The passage of food particles through the
esophagus is also aided by large circular esophageal muscles; their wavelike

IU

contraction pushes the food into the stomach, which is separated from the
esophagus by the cardinal sphincter. Food lumps are broken down in the
stomach where digestion takes place. The food enters the small intestine
through the open pyloric sphincter. Particles are sorted into edible and
nondigestible in the stomach. Passage of food particles through the entire
digestive system takes 15—20 min. According to Strathmann (1971), the
echinoderm larva ingests particles less than 65 —85 [1m in diameter and less
than 100—200 pm long. The rate of filtration of particles from water is 0.5 —
.3 l/min. On average, filtration proceeds at a speed of 0.3 —0.6 j1l/min per
1.0 mm of ciliated band. With an increase in concentration of algae, the rate
of filtration decreases. If the concentration is very high — over 5,000 — 10,000
cells/ml — the particles cannot be handled by the ciliated band. At concen-
trations of algae in excess of 50,000 cells/ml, aberrations in development may
occur, leading to larval mortality; the intestines of such larvae are jammed
with food and many intact, undigested algal cells are present in the feces
(Strathmann, 1971; Barker, 1978). During active feeding larvae cannot be

Figure 72: Bipinnaria of Luidia ciliaris (from Tattersall and Sheppard, 1934).
mp — medial projections (arms); pl — preoral lobe.

112

selective, accepting some and rejecting other species of algae; however, the
rate of filtration differs for different species of algae. Moreover, one species
of algae may influence the rate of filtration of another species — increasing
or decreasing it (Strathmann, 1975). The nutritional value of different food
particles has not been thoroughly investigated. Adequate data are not available
for judging the role of bacteria and soluble organic substances in the nutrition
of larvae of sea stars. But their role can hardly be important since the ciliated
band poorly retains particles less than 2—3 um in size and observations have
shown that growth mainly occurs with active feeding on phytoplankton.

Like sea urchins (Chia and Burke, 1978), it has been suggested that
reserve food, primarily in the form of lipids, is stored by the larvae of sea
stars in cells of the digestive tract.

Respiration: As in larvae of bivalves, the intake of oxygen and removal
of carbon dioxide in the larvae of sea stars occurs by diffusion. The minute
size of the larvae enables them to dispense with any specialized system. Their
constant motion — beating of ciliated bands, movement of other areas of the
body surface, and activity of the ciliated surface of the digestive system —
is conducive to gaseous exchange.

Transport of substances: In echinoderm larvae (as in larvae of other
marine invertebrates), which are minute in size, there is no need for a special
system for blood circulation. This function is fulfilled by extensive — pri-
mary and secondary — body cavities. Transport of substances in the primary
body cavity is facilitated by contraction of the body wall and esophagus, and
transportation of substances in the secondary cavity (coelom) facilitated by
beating of cilia lining the coelomic cavity.

Excretion: Larvae of sea stars possess no specialized excretory system.
The function of excretion, as in many lower groups of animals, is performed
by the developed digestive system. Evidently, mesenchymal cells participate
in the removal of metabolic products; these cells are scattered in the primary
body cavity. Possibly Field (1892) is correct, as his demonstration of the
excretory function of the pore canal is partly confirmed by the organized
directional movement of cilia in the coelomic cavities (Gemmill, 1914),
which causes a current in the direction of the pore canal. Ruppert and Balser
(1986) are more specific in naming the canal-hydropore complex the
nephridium.

In the course of development of sea stars the coelomic structures undergo
considerable transformation. They form various organs and systems in the
definitive organism, primarily its ambulacral system. We do not propose to
describe the development and transformation of coeloms; rather, we shall
describe only the coelomic formations of bipinnaria, since these are multi-

3)

functional structures performing supportive, dis-
tributive, and excretory functions. Coeloms of
the bipinnaria are extensive hollow pouches situ-
ated on both sides of the digestive tract. In the
early bipinnaria they are separate but in the late
bipinnaria they fuse above the oral lobe and pass
into the dorsomedial projection (arm) (Figure 73).
The left coelom is better developed than the right.
Septa (commissures) in the posterior region of
the coelom partly separate the left and right
coeloms (somatocoels) from the common coe-
lom. This separation becomes complete later
(Figure 74). The remaining part of the coelom is
a single structure that later separates into left and
Bet the bipinnitle ‘of right anterior and posterior coeloms, Ieee aXO-
Grciisieriae culamarin (horn and hydrocoels. The single coelom is linked with
Barker, 1978). the external medium through a pore canal, which
hp —hydropore; lc —left opens as a hydropore on the dorsal side, left of
Catone We sans Coat. the median line, at the level of the lower part of
the esophagus. In some species, in addition to the
left pore canal, there may be a right pore canal as well, which also opens
through a hydropore exteriorly (Figure 75) (Field, 1892; Gemmill, 1914,
1915). During the development of the bipinnaria, coeloms of the right and left
side are connected not only in the anterior region, but also in the region of
the somatocoels. The left somatocoel temporarily forms a process, termed the
ventral horn, which communicates with the right axocoel ventral to the stom-
ach, encircling the intestine from both sides. A dorsal horn also forms in the
left somatocoel, which establishes contact with the left axo-hydrocoel. Thus
the coeloms of the left side remain connected despite a dividing septum
(Figure 76). According to Gemmill (1914), the flow of coelomic fluid is
directed by cilia from the left axo-hydrocoel to the right axo-hydrocoel, from
there through the ventral horn to the left somatocel, and again into the left
axo-hydrocoel. In the pore canal, lined with a cuboidal ciliated epithelium,
as mentioned above, a weak outward beating of the ciliated band is percep-
tible. Possibly, the movement of fluid in the coelomic cavities is facilitated
by the pulsation of the closed madreporic vesicle (formed, probably, from the
mesenchymal cells), situated alongside the left hydropore (Gemmill, 1914).
This vesicle is not found in all species. Nor do all authors mention circulation
of the coelomic fluid (see, for example, Barker, 1978).

Figure 73: Development of

Locomotion : Bipinnariae swim by means of ciliated bands, the preoral
and, more so, the postoral. The structure of the ciliated bands has been

114

Figure 74: Development of coeloms in the bipinnaria of Patiria pectinifera.
ac —axocoel; Is — left somatocoel; rs — right somatocoel.

described in the section on feeding of the larva. The water current created by
the cilia of these bands enables the capture of food particles and concomi-
tantly locomotion of the bipinnaria. In this case the preoral lobe is directed
forward. In the bipinnariae of sea stars of the family Astertidae, the size of
the processes increases with bipinnarial growth and they transform into long
movable arms. The posterolateral and posterodorsal arms (Figure 77) become
the longest (Gemmill, 1914; Kume and Dan, 1968). Since the ciliated band
extends over the elongate processes of the bipinnaria, the total length of the
band increases considerably. In many sea stars, however, the ciliated band
on the arms is not well developed and does not participate in the capture of
food; it functions only in larval locomotion. The beating of the cilia on the
arms is directed from the base to the tip of the arm. The speed of movement
of the bipinnaria of Asterias rubens is about 2.0 cm/sec (Konstdntinova,
1966). Movement of the bipinnaria in a reverse direction is not performed by
reversal of direction of ciliary beating (as done in the pluteus), but rather by
the larva turning around. The bipinnaria executes a turn during swimming

Figure 75: Left and right hydropores
in the early larva of Asterias vulgaris
(from Field, 1892).
lhc — left hydrocoel; thp — left
hydropore; rhc —right hydrocoel;
rhp —right hydropore.

115

through contraction of the dorsal mus. les,
which produces considerable flexion of .he
larva on the dorsal side (Strathmann, 1971,
Movement of the giant bipinnariae of Luidia
ciliaris and L. sarsi occurs through contrac-
tion of muscles in the elongate anterior part of
the larva; apparently, the ciliated bands of the
larvae of these species (unlike L. foliolata) do
not participate in locomotion (Tattersall and
Sheppard, 1934; Strathmann, 1971).

Nervous system and sense organs: Ear-
lier authors assumed that larvae of sea stars
possessed a diffused nerve plexus under the
epithelial cover (Gemmill, 1914; Tattersall and
Sheppard, 1934). Burke (1983), while investi-
gating the nervous system of the bipinnaria of
Pisaster ochraceus using the glyoxalic method
and electron microscopy, observed no such
plexus, but demonstrated the presence of ax-
onal tracts at the base of the ciliated band and

Figure 76: Development of coeloms in the bipinnaria of Asterias rubens (from Gemmill,

1914).

ac —axocoel; lhc —left hydrocoel; ls —left somatocoel; rs —right somatocoel;

vh — ventral horn.

116

Figure 77: Bipinnaria of Astropecten auranciacus (from Horstadius, 1939).
abd — aboral disk of definitive sea star; ac — axocoel; es — esophagus; g — gut; lhc — left
hydrocoel; pocb — postoral ciliated band; preb — preoral ciliated band; st — stomach.

in the esophagus, and two types of nerve cells situated in the ciliated band:
one linked to the axonal tracts and the other provided with cilia. On the lower
lip, in the corners of the larval mouth, clusters of nerve cells occur. In the
bipinnaria of Asterias amurensis the presence of numerous seratonergic nerve
cells has been demonstrated along the ciliated band (Nakajima, 1987).
Bipinnariae do not have developed sense organs; however, it is quite possible
that ciliated nerve cells of the ciliated bands perform sensory functions (Burke,
1983).

Integument : Echinoderm larvae lack a specialized protective organ, equiva-
lent to the larval shell of bivalves — an organ that performs several functions
simultaneously. Hence protection of the internal tissue of the larva against
adverse effects is solely delegated to the cells of the integumentary epithe-
lium, which bear cilia and microvilli and produce mucus.

Rudiments of definitive organs: The development of sea stars from
planktotrophic larvae may proceed in two ways. In most sea stars there 1s a
brachiolaria stage immediately following the bipinnaria stage, during which
development of the organs of attachment and anchoring of the definitive body
of the organism are characteristic. Metamorphosis concludes with the attach-
ment of the larva to the substrate. In sea stars of the families Luidiidae and
Astropectinidae, organs of attachment do not appear during development,

117

instead, the entire development of the definitive sea star and the conclusion
of metamorphosis take place in the purely planktonic bipinnaria stage. Such,
in particular, is the development of Luidia ciliaris and L. sarsi (Tattersall and
Sheppard, 1934; Wilson, 1978); and Astropecten auranciacus and A. scoparius
(Horstadius, 1939; Oguro et al., 1976). The brachiolaria stage in these sea
stars is lacking. Hence, on the left side in the late bipinnariae of Luidiidae
and Astropectinidae it is possible to see the rudiments of all the organs
usually present in the definitive sea star. The organizing center for the for-
mation of the definitive organism is located in the region of the middle
coelom. We shall discuss metamorphosis in detail below. In other families of
sea stars rudiments of definitive organs that serve no functional purpose in the
larva are but slightly developed in the bipinnaria stage. These are the five
lobate processes of the coelom that appear in the late bipinnaria in the region
corresponding to the left hydrocoel, i.e., rudiments of radial canals of the
ambulacral system (see Figure 76). At present, based on available data, it
cannot be said for certain whether the definitive organs of sea stars lacking
in the larva develop during metamorphosis from imaginal “silent” cells, or
whether these organs differentiate from larval cells after dedifferentiation.
The second course appears more probable (except for gametes, whose fate is
predetermined). In the developed bipinnaria of most sea stars, rudiments of
temporary organs of the brachiolaria, such as the brachiolar arms and attach-
ment disk, appear in the preoral lobe.

Brachiolaria

The Brachiolaria differs from the bipinnaria in the presence of attachment
organs, large body, and large processes, and pronounced formation of the
definitive body of the sea star.

Feeding, transport of substances, respiration, and excretion: These ac-
tivities take place in the brachiolaria in a manner similar to that in the
bipinnaria. Barker (1977, 1978) has described the ultrastructure of the
integumental epithelium and coelomic lining of the brachiolariae of Stichaster
australis and Coscinasterias calamaria. In the region of the brachiolar stalk
the cells of the external epithelium contain numerous vacuoles and are armed
with microvilli. Under the epithelium lies the plexus of axions underlain by
the basement membrane. Under the basement membrane is a connective layer
of collagen fibers, fine fibrillar material, and occasional vacuolated cells. The
inner basement membrane separates the coelom lining from the connective
tissue. The longitudinal muscle fibers adjoin internally the inner basement
membrane. The coelomic epithelium lies deepest and comprises mainly flat
epithelial cells. Sometimes these cells have pseudopodial processes and long
solitary cilia (Figure 78).

118

Figure 78: Structure of the brachiolar wall of the brachiolaria of Coscinasterias calamaria
(from Barker, 1978).

ax — axons of nerve cells; bl — basement membrane; cc — coelomic lobe; ce — coelomic

epithelium; cf—collagen fiber; cl—cilia; ct— connective tissue; cye — cytoplasmic

processes of muscle cells; db — dense body; m— mitochondria; mv — microvilli; va —
vacuolated cells.

Locomotion : This is performed by means of cilia in the ciliated band. As
the body and processes grow, the size of the band increases and the processes
usually become long flexible arms. The elongate ciliated band enables the
brachiolaria to continue swimming as the definitive star develops. The move-
ment of the brachiolaria becomes more rapid and more complex. The larva
may reverse directions not only by describing a loop through flexion of the
dorsal side of the body, but also by changing the position of its arms. On
coming into contact with an obstacle, the brachiolaria extends its posterolat-
eral, posterodorsol, and postoral arms forward, while directing the mediodorsal
process ventrally. The water current generated in this action by the ciliated
band, which is directed forward, moves the larva in the opposite direction.
Flexion of the processes and arms of the brachiolaria occurs through contrac-
tion of the muscle fibers connecting the processes with the larval body (Fig-
ure 79) (Strathmann, 1971).

Nervous system and sense organs: In addition to the above-described
nervous system of the bipinnaria, a neuropyle-axon plexus develops in the
brachiolaria, which is situated apically, at the base of the brachioles and

119

Figure 79: Flexion of processes of the brachiolaria of Pisaster ochraceus during reversal of
movement (from Strathmann, 1971).

A — locomotion; B —reverse movement.

under the epithelium of the adhesive papillae and the disk (Barker, 1978b;
Burke, 1983). Here one also finds an accumulation of serotonergic neurons
(Bisgrove and Burke, 1987). The nerve cells of papillae and brachioles are
connected with processes from the preoral nerve strands (Nazlin and Dautov,
1987). Among the cells of the papillae and disk, Barker identifies neurose-
cretory cells that presumably participate in the attachment and adhesion of the
brachiolaria to the substrate. The only specialized sensory cells (if we do not
consider the presumed sensory cells described in the section on the bipinnaria)
are the ciliated cells of the adhesive papillae of the brachiolar arms. The basal
part of such cells reaches the subepithelial axon plexus. The lone cilium
surrounded by microvilli has a developed kinetochore. Probably the brachiolaria
uses these cells to probe the substrate for a suitable place to settle.

Attachment system: The attachment system of a brachiolaria typically
comprises three brachiolar arms, an attachment disk, and lateral papillae
(Figure 80). Lateral brachiolar arms appear only in the brachiolaria stage; the
medial arm is a modified medioventral process. During transformation into a

120

brachiole, the medioventral process in sea stars of the order Spinulosida (for
example, Acanthaster planci — Henderson and Lucas, 1971; Patiria pectinifera
— Mortensen, 1921; Kasyanov, 1977) is subjected to less change than in sea
stars of the order Forcipulatida (for example, Asterias rubens — Gemmill,
1914; Asterias amurensis —Kume and Dan, 1968). The axocoel processes
enter the brachiolar arm. The preoral ciliated band extends laterally on each
brachiolar arm. The brachiolar arms are crowned by a ring of attachment
papillae which serve in probing the substrate and temporary attachment to it
(Figure 81). Neurosecretory and sensory cells are present in the papillary
epithelium; the secretory cells predominate and produce a mucopolysaccha-
ride-type secretion. Each such cell is armed with cilia and encircled by a ring
of microvilli. Another type of secretory cell is rarely found, namely, one
devoid of cilia but covered with numerous microvilli. The characteristic
feature of the so-called vacuolated cells (possibly, these are actually secretory
cells partially devoid of secretion) is intracellular fibrils, which extend from
the basal part of the cell into the microvilli. The function of these structures
is supportive. The lateral papillae, situated on each side of the attachment
disk, are identical in structure.

The attachment disk is a round, slightly concave structure comprising
secretory cells covered with numerous branched microvilli. The proteinic secre-
tion of these cells acts as a cement for attaching the disk to the substrate. As
in the papillary cells, supporting fibrils are located in the disk cells (Figure 82).

While probing the substrate, the brachiolaria aligns itself by its ventral
side, flexes its arms covered with a ciliated band, and attaches itself by means
of one or two brachiolar arms contacting the substrate with their papillary

Figure 80: Attachment system of the Figure 81: Brachiolar arm of the
brachiolaria of Coscinasterias calamaria. brachiolaria of Patiria pectinifera.
ad — attachment disk; b — brachiolar arm.

121

ay fi ce

sil)

Figure 82: Structure of the attachment disk of the brachiolaria of Coscinasterias calamaria
(from Barker, 1978).

ap — attachment papilla; c —coelom; ce—coelomic epithelium; ct — connective tissue;
if — inner fibrils; is — intercellular space. Arrows indicate secretory granules.

crown. The brachiolaria, so to speak, walks along the substrate, attaching and
detaching its brachiolar arms. Scouting may continue for a few seconds to one
hour. If the substrate is not suitable for settling, the larva straightens its arms
and swims away. If the substrate is satisfactory, the larva ceases “scouting”,
alternately presses its brachiolar arms to the substrate, spreads them maxi-
mally apart, then lowers the attachment disk to the substrate. A firm contact
is ensured by the working of the attachment papillae situated on each side of
the disk. Cementation then commences, during which the secretion of the
cells of the attachment disk is discharged and binds the disk to the substrate.
This process takes one to several hours. Metamorphosis, which had already
begun in the pelagic period of larval life, terminates in the attached state.
After six to seven days the juvenile sea star is dislodged from the larval body
by means of the primary ambulacral podia and, thus freed, begins an inde-
pendent life (Barker, 1978; Strathmann, 1978).

Light retards metamorphosis. Larvae of the family Asteriidae maintained
in a normal daily range of illumination completed metamorphosis within ten
hours at night, while larvae illuminated continuously for five days were not
able to metamorphose even though they had attached to the substrate (Dautov,
1979).

Substrate selectivity is well developed in some species and lacking in
others. High selectivity is typical of lecithotrophic larvae (Strathmann, 1978).
The Brachiolariae of Acanthaster planci and Coscinasterias calamaria, plank-
ton feeders, settle on almost any substrate, provided it is covered with a
primary bacterial-algae film (Lucas, 1975, Barker, 1977). The microrelief of
the substrate is evidently not of special importance; however, the brachiolaria
in anchoring prefers, whenever possible, the lower surface of the substrate.
Yet some planktotrophic brachiolariae do exhibit high substrate specificity.
One such is the New Zealand sea star (Stichaster australis), which settles only

122

on coralline algae of the genus Mesophyllum. \n the absence of a suitable
substrate, the sea star can delay completion of metamorphosis and continue
swimming; according to Barker (1977), its threshold of selectivity drops
gradually. If the larva is unable to find a suitable substrate, it dies. Larvae
of Acanthaster planci, Culcita novaeguineae, and Linckia laevigata, feeding
on corals, settle on the coral algae Porolithon (Yamaguchi, 1973, cited by
Chia et al., 1984); tubes of the polychaete Phyllochaetopterus prolifica attract
larvae of the sea star Mediaster aequalis, the young of which feed on these
polychaetes (Birkeland et al., 1971).

Larvae of the families Luidiidae and Astropectinidae possess no special-
ized “larval” attachment organs. For scouting the substrate and temporary
attachment, the larva uses the already functional ambulacral podia of the
juvenile sea star (Strathmann, 1979).

METAMORPHOSIS

The metamorphosis of sea stars from planktotrophic larvae is catastrophic in
character. Intensive morphogenetic processes occur in which dedifferentiation
or resorption of many larval tissues takes place. The definitive sea star forms
on the left side of the larva. The oral-aboral axis of the sea star is at an angle
to the principal axis of the larval body. In most sea stars the principal and
concluding processess of metamorphosis are completed after the brachiolaria
has settled in the attached state.

Digestive system : The ciliated band performs the function of a capturing
mechanism and organ of locomotion only in the larva and, in the course of
metamorphosis, is subjected, like the remaining areas of the larval epithelium,
to dedifferentiation and resorption. Cells of the preoral ciliated band are part
of the stalk whereby the developing sea star is bound to the attachment disk;
in some species the stalk is divested after metamorphosis, while in others it
is resorbed (Chia and Burke, 1978). The entire epithelium is not resorbed; the
definitive integument of the juvenile sea star is differentiated from its cells
(after the preceding dedifferentiation). The digestive system undergoes sig-
nificant changes. The larval tissues of the mouth, part of the gut, and the anal
region are resorbed. Cells of the larval esophagus constitute part of the outer
epidermis and wall of the stomach. A definitive esophagus is formed, the
larval stomach is reconstructed, and rudiments of the pyloric appendages
appear. According to Bury (1895), the larval esophagus is directly trans-
formed into a definitive organ. On the oral side of the juvenile sea star a
mouth opening appears and on the aboral side an anal opening. A definitive
gut with rectal glands forms from parts of the larval gut (Gemmill, 1914).

123

Respiration: The respiratory function is transferred from the larval to
the definitive epithelrum. In the juvenile sea star visceral coeloms formed
from the larval somatocoels and the hemal and perihemal systems formed
from the left somatocoel and axocoel, also participate in the transportation
of substances.

Elimination of metabolic products: This involves several structures—
spheroid bodies with phagocytes, the axial organ, and the rectal glands
(Bachmann and Glodschmid, 1978; Jangoux, 1978; Hobaus, 1979). Larval
coeloms are considerably transformed; with their participation, a new loco-
motor organ, hemal and perihemal systems, axial organ, and coelomic cavity
of the definitive sea star are formed.

Locomotion : With a changeover to a benthic mode of life, the sea star
loses its swimming organ — the ciliated band. The transient locomotor appa-
ratus of the brachiolaria— the brachioles—— remains for a very short time,
allowing the sea star to move on the substrate. At this stage there occurs, so
to speak, a testing of a new locomotor mechanism through the assistance of
the apically papillate body processes, into which coelomic processes pen-
etrate. The definitive locomotor organ — the ambulacral system, which arises
during metamorphosis — works on a similar principle. The region of the left
hydrocoel plays a leading role in its formation; bending, the two ends later
merge and form the rudiment of the oral ring of the ambulacral system. From
the arc issue hydrocoelic processes — rudiments of the radial canals of the
ambulacral system (Figure 83). The terminal areas of these canals, in conjuntion
with the ectoderm surrounding them, later give rise to the terminal tentacle
(podia), while along the sides of the canal secondary processes form—rudi-
ments of the ambulacral podia. The axocoel takes part in the formation of the
stone canal from the larval pore canal and the hydropore (Gemmill, 1914).

Nervous system and sense organs: The larval nervous system and sense
organs are replaced by definitive ones. In the opinion of Gemmill (1912), the
nerve plexus of the preoral lobe of the brachiolaria participates in the forma-
tion of the oral ring of the definitive nervous system. The most developed
ectoneural system in sea stars is formed from the thickened ectoderm above
the circumoral ring and radial canals of the ambulacral system. In addition
to sense organs scattered in the integument, numerous sensory elements are
located in the terminal tentacle and ocelli at the base of the tentacle.

Integument: A variety of skin glands, spines, pedicellaria, and other ele-
ments of the skeleton of the definitive sea star perform protective functions.

Skeleton: The definitive skeleton has already begun to form in the
bipinnaria. In sea stars, as in all echinoderms, the skeleton is internal and of

124

pla

Figure 83: Initiation of radial canals of the ambulacral system in the brachiolaria of Asterias
vulgaris attached to the substrate by brachiolar arms (Goto, 1896*).
abr —anterior brachiolar arm; ada — anterodorsal arm (projection); es — esophagus;
hc —hydrocoel; lbr — lateral brachiolar arm; mda— mediodorsal arm (projection);
pda — posterodorsal arm (projection); pla— posterolateral arm (projection); poa — postoral
arm (projection); proa —preoral arm (projection); st— stomach; | to 5—rudiments of
radial canals of ambulacral system.

mesodermal origin. The first skeletal plates —- central, five radial, terminal,
and five interradial basal— form in the region of separation of the aboral
disk of the definitive asteroid. One basal plate becomes the madreporite,
which closes the outer opening of the stone canal of the ambulacral system.
Other elements of the skeleton appear later (Figure 84).

Rudiments of definitive organs: In the juvenile sea star, all systems of
the definitive body are found in various stages of formation; these become
fully developed as the asteroid grows. Within a few days after metamorpho-
sis, all these systems become functional except the reproductive. Develop-
ment of the reproductive system has not been fully investigated. Some authors

125

Figure 84: Lecithotrophic larva of Astropecten latespinosus with aboral (A) and oral (B)
sides of disk of definitive asteroid (from Komatsu, 1975).

(McBride, 1896; Chia, 1968) have observed the precursors of gametes in the
cellular wall separating the left and right somatocoels. Lender and Delavault
(1968) were the first to identify the primary gametes in the wall of the coelom
of the madreporal interradius in an | 1-day-old brachiolaria of Asterina gibbosa;
later, these were observed in the circular genital cord encompassed the
aboral perihemal ring. Processes of the genital cord in the ray of the asteroid
are gonadal rudiments.

LECITHOTROPHIC LARVAE

Many species of sea stars produce large eggs — 200-3,450 um — with a
large yolk mass. The larval stages, or the bipinnaria stage, are generally
bypassed in the development of such asteroids; only a highly altered
brachiolaria is retained, which lacks a ciliated band and a functional diges-
tive system. The body of such a brachiolaria is oval and provided with an
attachment apparatus — brachiolar arms and disk (Figure 85), which have
been partially described for Solaster endeca (Gemmill, 1912), Henricia

126

Figure 85: Brachiolaria of Echinaster echinophorus (from Atwood, 1973).
ad — attachment disk; br — brachiole; hp — hydropore.

sanguinolenta (Masterman, 1902), Leptasterias hexactis (Chia, 1966) Patiriella
exigua (Lawson-Kerr and Anderson, 1978), and Asterina minor (Komatsu et
al., 1979). Brachiolar arms are absent in some species — Asterina gibbosa
(McBride, 1896); in other species, they are developed but the attachment
stage is absent — Echinaster sepositus (Nachtsheim, 1914) and Asterina
batheria (Kano and Komatsu, 1978). The lecithotrophic larva of Astropecten
latespinosus possesses neither brachiolar arms nor attachment disk (Komatsu,
1975), which is not at all strange since the brachiolaria stage is absent in
astropectinids with planktotrophic larvae. Due to lecithotrophy, the number
and degree of development of larval structures are minimal and the definitive
organogenesis of such larvae proceeds in a more direct manner.

On the whole, it may be said that the secondarily acquired direct devel-
opment or development lecithotrophic larva is often observed in evolutionally
primitive groups of sea stars. (A similar picture is observed in many taxa of
invertebrates, for example in bivalves.) In the primitive order of sea stars
Paxillosida, direct development with brooding of offspring in the cavities
between paxilli occurs in the genera Ctenodiscus and Trophodiscus. In T.
almus the largest embryos are located along the margin of rays and in the
interradii of the female. Embryos emerge through movement of the paxilli.
Similar brooding is observed in 7. uber (D’yakonov, 1950). Development
without free-swimming larvae is also typical of Solaster endeca, Crossaster
papposus, Asterina gibbosa, and other species of the latter genus. In Pteraster
obscurus and P. militaris, fertilization and brooding of embryos occurs on the
dorsal side within a special cover (Kaufman, 1977). In species of the genus
Henricia, embryos are borne in clutches near the mouth or in the mouth of
the mother. Development without planktotrophic larva occurs in the order

127,

Forcipulatida; however, such development generally occurs in species inhab-
iting polar and adjacent waters, for example, species of the genus Leptasterias
(D’yakonov, 1950) (also see Table 4 and Kasyanov, 1987).

IDENTIFICATION OF PELAGIC LARVAE OF SEA STARS
(Terminology and Diagnostic Characters)

In the bipinnaria of a sea star (Figure 86) the dorsal and ventral, right and
left sides, and anterior and posterior ends are well defined. On the ventral side
lie the mouth and anal openings; on the left dorsal side, the hydropore leading
into the coelomic cavity; usually, there is no hydropore on the right dorsal
side. In the anterior part of the larva, in front of the
mouth, lies the preoral lobe, which is delimited from
the rest of the body by an independent preoral cili-
ated band. The anterior part of the preoral lobe
forms the medioventral process (arm), below which
the right and left preoral processes are located lat-
erally. The lower part of the preoral band borders
the preoral depression, which is hemmed by the
peristomial ciliated ring girdling the mouth. The
preoral depression is posteriorly bordered by the
transverse area of the main postoral ciliated band,
which hems the rest of the body of the bipinnaria.
This ciliated band ventrally passes over the left and
right postoral processes and the posterolateral pro-
A a ‘aaa cesses situated in the: posterior part of the larva.

SHaiae 1971). Dorsally, the cilited band borders (extending

posteroanteriorly) the left and right posterodorsal

and anterodorsal processes and finally the unpaired mediodorsal process.

In the later larva — brachiolaria — of the sea star (Figure 87), additional
projections appear on the preoral lobe, namely, the left and right brachiolar
arms, which are equipped with a crown of attachment papillae. The
medioventral process is also transformed into a brachiolar arm, with papillae
located on its tip and/or in two rows along the ventral surface. The large
attachment disk lies between the brachiolar arms.

The following parameters and characters are important in the identifica-
tion of larvae of sea stars:

1. Length of larva from tip of mediodorsal process to posteriormost point
of body (between posterolateral processes), measured in a larva in an
extended condition.

128

Table 4: Types of development of sea stars.

Species

Astropecten auranciacus
. irregularis

. latespinosus

. polyacanthus

. scoparius

. velitaris
Ctenopleura fisheri
Psilaster andromeda
Ctenodiscus australis
Leptychaster almus
Luidia ciliaris

L. clathrata

L. foliolata

L. sarsi

Luidia savignyi
Lysasterias belgicae
Trophodiscus almus
T. uber

moe www

Mediaster aequalis
Pentaceraster mammillatus
Porania pulvillus
Acanthaster brevispinus
A. planci

Asterina batheri

A. calcar

. coronata japonica

. exigua

. gibbosa

. minor

Echinaster purpureus
E. sentus

E. sepositus

Fromia ghardaquana
Linckia multifora
Ophidiaster guildingii
Patiria miniata

P. pectinifera
Patiriella obscura

P. pseudoexigua

P. regularis

P. vivipara
Gymnasteria carinifera

mM RR Dw

Type of Development

ORDER PAXILLOSIDA

Planktotrophic larva
Same
Lecithotrophic larva
Planktotrophic larva

Same
Same

lecithotrophic larva

Same
Brooding
Brooding

Same

Same

Planktotrophic

Same

Same
Brooding
Brooding

Same

ORDER VALVATIDA

Lecithotrophic larva _ Birkeland ef al., 1971
Planktotrophic larva Mortensen, 1937
Same Gemmill, 1915
Planktotrophic larva Lucas amd Jones, 1978
Same Henderson and Lucas, 1971
Pecithotrophic larva Kano and Komatsu, 1978
Same Lawson-Kerr and Anderson, 1978
Same Komatsu 1975
Same Lawson-Kerr and Anderson, 1978
Lecithotrophic larva Ludwig, 1882
Same Komatsu ef al. 1978
Same Mortensen, 1938
Same Siddall, 1979
Same Nachtsheim, 1914
Same Mortensen, 1938
Planktotrophic larva Mortensen, 1938
Planktotrophic larva Mortensen, 1921
Planktotrophic larva Heath, 1917
Same Kasyanov, 1977
Lecithotrophic larva _ Dartnall, 1971
Same Lawson-Kerr and Anderson, 1978
Planktotrophic larva Lawson-Kerr and Anderson, 1978
Brooding Dartnall, 1971
Planktotrophic larva Mortensen, 1921

larva

Source

Horstadius, 1925
Newth, 1925
Komatsu, 1975
Mortensen, 1937
Oguro et al., 1976
Mortensen, 1937
Komatsu, 1982*
D’yakonov, 1950
Lieberkind, 1928
Fisher, 1917
Tattersall and Sheppard, 1934
Dehn, 1979
Strathmann, 1971
Tattersall and Sheppard, 1934
Mortensen, 1938
Ludwig, 1903
D’yakonov, 1950
D’yakonov, 1950

Crossaster papposus
Pteraster militaris

P. obscurus

P. tesselatus
Hymenaster cannasus
H. membranaceus
solaster endeca

Echinaster echinophorus
Henricia sanguinolenta
H. abissicola

H. oculata

H. hayashi

Othilia echinophora

O. senta

Anasterias antarctica
A. studeri
Aphelasterias japonica
Asterias amurensis

A. forbesi

A. lincki

A. pallida

A rubens

A. vulgaris
Coscinasterias calamaria
Distolasterias nipon
Cryptasterias turqueti
Diplasterias brandti
D. brucei

D. meridionalis

D. octoradiata
Evasterias troscheli

E. retifera
Leptasterias arctica

L. groenlandica

L. hexactis

L. mulleri

L. polaris
Marthasterias glacialis
Orthasterias leptolena
Pisaster ochraceus
Pycnopodia helianthoides
Stichaster australis

S. roseus

129

ORDER VELATIDA

Lecithotrophic larva Gemmill, 1920

Same Kaufmna, 1968
Same D’yakonov, 1950
Same Chia, 1966
Same Fisher, 1940*
Same Pain er al., 1952

Lecithotrophic larva Gemmill, 1912
ORDER SPINULOSIDA

Lecithotrophic larva Atwood, 1973

Same Gemmill, 1916

Same Lonning, 1916

Same Brun, 1978

Same Gaginskaya ef al., 1983
Same Hyman, 1955

Same Hyman, 1955

ORDER FORCIPULATIDA

Brooding Hyman, 1955
Same Hyman, 1955
Planktotrophic larva Dautav, 1979
Same Dautov and Kasyanov, 1981
Same Mead,1901
Lecithotrophic larva _—_‘ Falk-Peterson and Sargent, 1982
Same Goto, 1896
Same Gemmill, 1914
Same Field, 1892
Same Barker, 1944
Same Dautov (personal communication)
Brooding Hyman, 1955
Same Hyman, 1955
Same Hyman, 1955
Same Hyman, 1955
Same Hyman, 1955
Lecithotrophic larva Mortensen, 1921
Same D’yakonov, 1950
Brooding Fischer, 1930
Same D’yakonov, 1950
Lecithotrophic larva Osterud, 1918
Same Ludwig, 1900
Same Emerson, 1977
Planktotrophic larva Gemmill, 1916
Same Mortensen, 1921
Same Mortensen, 1921
Same Greer, 1962
Same Barker, 1977

Lecithotrophic larva Gemmill, 1916

130

2. Relative length of preoral part of larva.
This part is usually less or almost equal
in length to the postoral part. Exceptions
are the bipinnariae of the family Luidiidae
in which, as a result of growth of the
medioventral and mediodorsal processes,
the preoral part is longer than the postoral.

3. Relative length and movability of paired
processes of bipinnaria. In bipinnariae of
the families Astropectinidae,
Gymnasteriidae, and Asterinidae, the pro-
cesses are relatively short and less mov-
able. In bipinnariae of the family
Asteriidae and some species of the family
Luidiidae, they are longer and capable of
greater movement.

4. Relative length and movability of
brachiolar arms. In brachiolariae of the
families Gymnasteriidae, Asterinidae, and
Acanthasteridae, the brachiolar arms are Figure 87: Brachiolaria of Asterias
relatively short and less movable than in rubens (Gemmill, 1914)
brachiolariae of the family Asteriidae.

5. Degree of development of unpaired brachiolar arms. In brachiolariae of
the family Asteriidae, the middle brachiolar arm is similar in structure to
the lateral ones. Two short lateral rows of small papillae occur on the
ventral surface of the middle brachiolar arm near its base. In brachiolariae
of the families Poraniidae, Asterinidae, Acanthasteridae, and some oth-
ers, the middle brachiolar arm is a relatively less modified medioventral
process, with two long rows of papillae on the ventral surface.

6. Color of larva and of its processes.

Identification of larvae before the late bipinnaria stage is difficult.
Key to Larvae Based on Late Bipinnaria Stage

In Peter the Great Bay sea stars belonging to five families of three orders
have been found. In Henricia sp. (family Echinasteridae) and Solester sp.
(family Solasteridae), development proceeds with lecithotrophic larva, and
the bipinnaria stage is absent; only a modified nonfeeding brachiolaria stage
occurs.

1 (4).

23):

3) (@)).

4 (1).

131

Preoral part of larva shorter than, or almost equal in length to
postoral part.

Preoral part of larva shorter than postoral part. Processes short, less
movable. Pigment absent on tips of processes..............
GARR io Phe ec Ets BC Re eerie Asterinidae, Figures 70 and 74.
Preoral part of larva shorter than, or almost equal in length to,
postoral part. Processes long, movable, especially posterolateral and
posterodorsal. Tips of processes orange... Asteriidae, Figures 76.
Preoral part of larva longer than postoral part..............
Brae OAR, te MMe hi Sa AER Se Aue Luidiidae, Figures 71 and 72.

Key to Planktotrophic Larvae Based on Brachiolaria Stage

In addition to the characters listed in the key above, new diagnostic characters
are found in the brachiolaria stage.

1 (4).
2B).

3 (2).

4 (1).

Brachiolaria stage present.
Lateral brachiolar arms relatively short, less movable. Crown of
papillae absent on middle brachiolar arms; papillae arranged in two

LOWS On, ventral suntaceais tay hae. een ee Asterinidae, Figure 80.
Lateral brachiolar arms relatively longer, movable. Middle brachiolar
arm with crown of papillae............. Asteriidae, Figure 87.
Brachiolaria stage absent.............. Luidiidae, Figure 71.

CHARACTERS OF LARVAE ACCORDING TO FAMILIES

Luidiidae

In some species the bipinnaria is giant in size— 15—30 mm in length. The
preoral part of the larva is very long, and curved. Larval locomotion is
powered in some species by beating of the cilia bordering long arms, in other
species by contraction of the muscles in the preoral part. Branching of. the
paired arms may be observed. The bipinnaria stage with characteristic attach-
ment organs is absent. Metamorphosis occurs in the planktonic period of life.
The larval body is resorbed or discarded. In the latter case, it may exist
independently in the plankton for over a month.

Luidia quinaria bispinosa Djakonov is found in Peter the Great Bay. The
larva of Luidia quinaria von Martens has been described (Komatsu et al.,

1982).

132
Asterinidae

The bipinnaria is relatively small, up to 1,000 um in length, the arms (espe-
cially the preoral and postoral) are short, less movable, and devoid of pig-
ment. Locomotion is performed by beating of the ciliated band. The brachiolaria
stage is present. The brachiolar arms are relatively short; the middle brachiolar
arm has no papillary crown but has two lateral rows of papillae on the ventral
surface. Metamorphosis begins in the planktonic stage and terminates in the
attached stage. In species with lecithotrophic larvae the bipinnaria is absent
and the brachiolaria is modified.

Patiria pectinifera (Miller and Troschel) is found in Peter the Great Bay
and its larva has already been described (Mortensen, 1921; Kasyanov, 1977;
Dautov and Kasyanov, 1981).

Asteriidae

The processes of the late bipinnaria are long, movable, and orange at the tips.
Locomotion is mediated by the beating cilia of the ciliated band and flexion
of the processes. The brachiolaria stage is present and the brachiolaria are 3—
4 mm long. The brachiolar arms are relatively long and the middle brachiolar
arm is identical in structure to the lateral ones. The brachiolariae of different
species of the family Asteriidae can be distinguished by the disposition and
number of papillae at the base of the attachment disk. Metamorphosis begins
in the planktonic stage and ends in the attached stage. In species with
lecithotrophic larvae, the bipinnaria is absent and the brachiolaria is modified.

The following species are found in Peter the Great Bay; Lysastrosoma
anthostricta Fisher, larva not described; Distolasterias nipon (Déderlein),
larva not described; Lethasterias fusca Djakonov, larva not described;
Aphelasterias japonica Bell, larva not described; Asterias amurensis Lutkén,
larva described (Kume and Dan, 1968; Dautov and Kasyanov, 1981); Evasterias
retifera tabulata Dyakonov, larva not described; and Evasterias echinosoma
Fisher, larva not described.

PATIRIA PECTINIFERA (MULLER AND TROSCHEL)
(Asterinidae)

Egg

The eggs of the Patiria are yellow, 170 um in diameter, and surrounded
by vitelline and jellylike membranes. Cleavage is radial, with weakly ex-
pressed bilaterality, and somewhat asynchronous (see Figure 65). The stage
of 4—16 blastomeres is attained 2—3 hr after fertilization at 18 —22°C. A

Figure 88: Bipinnaria of Patiria
pectinifera.

133

typical coeloblastula forms with a unilayered
blastoderm and an extensive blastocoel:; rotating
by means of cilia in its envelope, the coeloblastula
then exists from it (see Figure 66). Gastrulation
begins 16-20 hr after fertilization; it occurs by
invagination accompanied by slight unipolar im-
migration of the mesenchymal cells. The gas-
trula is 250 um x 200 um in size. Coeloms grow
faster than in larvae of the family Asteriidae.
After a relatively short dipleurula stage, the larva
becomes a bipinnaria.

Bipinnaria

The bipinnaria of Patiria is characterized by
relatively undeveloped and less movable pro-
cesses (Figure 68). Pigment is absent in the di-
stal ends of the processes. The left and right
axocoel grow forward and merge and the single
axo-hydrocoel encompasses the oral cavity with

Figure 89: Patiria pectinifera.
Formation of definitive skeleton.

134

collar, extending ventrally to the midline of the stomach. The left and right
somatocoels lie lateral to the stomach. The first plates of the definitive
skeleton (Figure 89) begin to form in the middle and late bipinnaria. The
early bipinnaria is formed by the 2nd—3rd day of development and the
completely formed late bipinnaria by 13th— 15th day at 14— 16°C.

Brachiolaria

As in other asterinids, the brachiolaria of Patiria bears two lateral brachiolar
arms with terminl papillae. The brachiolar arms are smaller in size than in
the asteriid brachiolaria. The medioventral process performing the function of
a third brachiolar arm is relatively larger than the lateral brachiolar arm,
bearing two rows of small papillae (3—7 in each row) and one large papilla
at the tip of the process. The other processes remain almost unaltered (Figure
90). The brachiolaria is about 700 um long.

Ecology

Larvae of Patiria pectinifera are found in the plankton of Vostok Bay
from the second half of July to September. Patiria spawns in Vostok Bay
from the second half of July to early September (Kasyanov ef al., 1976,
1980). According to Novikova (1978), a second spawning is possible in
November. In Sagami Bay (Pacific Coast of Japan), Patiria spawn from April
to May (Kume and Dan, 1968).

ASTERIAS AMURENSIS LUTKEN
(Asteriidae)

Asterias amurensis belongs to the order Forcipulaida. The development of
most species of this order proceeds from a pelagic planktotrophic larva stage
through subsequent metamorphosis. Most species of this order exhibit devel-
opment with the pelagic larva stage followed by metamorphosis.

Egg

The eggs of A. amurensis are about 100 tm in diameter and colorless.
Cleavage is radial, with some signs of bilaterality, and somewhat asynchro-
nous. Division by cleavage results in a smooth blastula stage 14 — 16 hr after
fertilization (at 19°C).

In the blastula stage, the embryo exists from the fertilization membrane
and begins active swimming by means of cilia that uniformly cover the body
surface.

Gastrulation occurs through invagination. During gastrulation the larva is
stretched slightly along the animal-vegetal axis. At the end of gastrulation,
rudiments of the left and right coelom form. The gastrula is 100 um x 150

135

uum in size. The gastrula is flattened somewhat on the 3rd day and in the
middle of the ventral surface of the larva an investigation appears that comes
into contact with the bottom of the archenteron. At the site of this contact,
a secondary mouth forms. In front of the mouth on the ventral side, an
elevation forms, the preoral plate. The intestinal tract initially looks like a
thin tubule, but later differentiates into sections. The blastopore, which be-
comes the anal opening, shifts to the ventral surface. At this stage the larva
is called a dipleurula (Figure 91). It begins to feed. The dipleurula stage is
very brief. P:

Figure 91: Asterias amurensis.
Dipleurula; coelom rudiments visible.

Figure 90 : Brachiolaria of Patiria
pectinifera.

Bipinnaria

The ciliated epithelium of the larva forms two ciliated bands. One of
them, the preoral, borders the preoral plate. The second or postoral band
proceeds posteriorly along both sides of the larva, passes onto the dorsal side,
and extends anteriorly to terminate at the tip of the larval body. The cilia on
the rest of the body surface either disappear or are very sparse. However, two
other ciliated bands form, which are intimately
associated with feeding. A preoral depression forms
in the mouth region. The peristomal ciliated ring
passes along the margin of the mouth, thereby
separating it from the preoral depression. The
adoral ciliated band originates from the peristomal
ring, which passes with two branches deep into the
esophagus and forms a loop there. The preoral
depression extends laterally along both sides of
Figure 92: Asterias amurensis, the larva, bordered by ciliated bands. Thus the

Early bipinnaria. larval digestive apparatus is formed (Figure 92).

136

By the 7th — 8th day of development the bipinnaria is about 350 Um long
(Figure 93). The brachiolaria stage of A. amurensis has not been satisfactorily
described. However, Kume and Dan (1968) present photographs of the late

Figure 93: Asterias amurensis.
Late bipinnaria.

bipinnaria and brachiolaria of this sea star. Judging from these photographs,
in A. amurensis the planktotrophic brachiolaria has three brachiolar arms,
typical for the genus Asterias, long pigmented larval processes, and skeletal
elements of the juvenile sea star in the posterior end of the body (Figure 94).
Information on the duration of larval development is lacking. The larval
stage of a closely related species, A. rubens, extends for 8—9 weeks (Gemmill,
1914). One may tentatively estimate the duration of the pelagic stage of A.
amurensis as 1.5—2.0 months; however, this requires verification.

Ecology

Larvae of A. amurensis are found in the plankton of Peter the Great Bay
from the end of April to November (spawning twice a year; April — June and
August — September at surface water temperatures of 12 — 16°C) Kasyanov et
al., 1976; Novikova, 1978).

Besides Peter the Great Bay, the spawning period of A. amurensis is
known for some regions in Honshu: Tonkin Bay — January to June at 6—

137

Figure 94: Asterias amurensis.
Brachiolaria; papillae and attachment disk visible.

14°C (Ino et al., 1955) but according to other data, February to April at 14—
15°C (Kume and Dan, 1968); Sendai Bay — January to May at 8—11°C
(Hatanaka and Kosaka, 1958); Mutsu Bay — March to June at 5—10 °C
(Kim, 1968); and the Pacific coast — June to October at 6—-14°C (Kume and
Dan, 1968).

It can be seen from these fragmentary data that A. amurensis spawns at
a relatively wide temperature range (4— 16°C); only seasons with very high
and low temperatures are excluded. If our assumption regarding the duration
of development of the larvae of this species is reliable, then the pelagic stage
in A. amurensis is completed at relatively moderate temperatures, i.e.
5 — 20°C.

CHAPTER III

LARVAE OF SEA URCHINS
(MORPHOLOGY, PHYSIOLOGY, AND
BEHAVIOR)

EARLY DEVELOPMENT

Egg

The eggs of sea urchins usually do not exceed 80—100 um in diameter.
However, there are deviations from this range with diameters decreasing to
54-68 tm, as in Stomopneustes variolaris (Mortensen, 1931) and increasing
up to 1,470 um. In the yolk-rich floating eggs of the bathyal sea urchins
Araeosoma fenestratum (Cameron et al., 1987) and for the eggs of the brood-
ing Antarctic sea urchin Abatus nimrodi (McClintock and Pearse, 1986). Two
species, e.g. Prionocidaris baculosa (Mortensen, 1938) and Echinostrephus
molaris (Onoda, 1936) may be mentioned in which the diameter of the egg
is 150 tm. Eggs are still larger in Peronella japonica — 300 tm (Mortensen,
1921; Okazaki and Dan, 1954) and Heliocidaris erythrogramma — 500 um
(Mortensen, 1921). Egg size is not a distinguishing species characteristic.
According to Hagstrém and Lonning (1961), egg size may differ among
individuals of the same population as also in the same individual.

Yolky large-sized eggs are less transparent than small eggs and are more
intensely colored. Situated mostly in the cortical layer, the pigment granules
containing echinochrome impart an orange color to the eggs of Hemicentrotus
pulcherrimus and Asthenosoma ijimai, yellowish-brown to the eggs of
Echinostrephus molaris, green to the eggs of Heliocidaris crassispina, choco-
late-brown to the eggs of Temnopleurus hardwicki, and red to the eggs of
Arbacia punctulata. In the eggs of Paracentrotus lividus from-some habitats,
the reddish pigment forms a ring below the equator (Selenka, 1883; Boveri,
1901).

Ovulation and shedding of eggs in water occur upon completion of the

139

maturation divisions. Among echinoderms, the shedding of eggs which have
completed meiosis is observed only in sea urchins and sea lilies.

Egg membrane : The unfertilized egg of sea urchins is surrounded by a
vitelline membrane adjoining the plasma membrane and a jellylike mem-
brane. The jellylike membrane consists of sulfomucopolysaccharides secreted
by the egg in the later stages of oogenesis. It usually has the same refractive
index as water and cannot be seen without staining. Staining reveals the
micropyle in the jellylike membrane, in which polar bodies can then be
identified (Boveri, 1901; Lindahl, 1932; Harvey, 1956; Piatigorsky, 1975;
Schmekel, 1975). In the sand dollars Echinarachnius brevis (Onada, 1938),
E. parma, and Scaphechinus mirabilis, the jellylike membrane contains pig-
ment cells (Chia and Atwood, 1982), has a fine fibrillar structure, and is
clearly visible under a microscope. The thickness of this membrane is 20-60

um.

Fertilization: As in most animals, contact of the spermatozoon with the
mature egg produces an acrosomal reaction in the spermatozoon and a cor-
tical reaction in the egg. It is generally believed that the spermatozoon can
penetrate the egg at any point. At the site of sperm penetration, a fertilization
cone is produced, which usually disappears in a few minutes. As a result of
the release of the cortical granules of the egg in the space between the plasma
membrane and the vitelline membrane, the latter separates from the egg and
is transformed into the fertilization membrane. The content of cortical gran-
ules takes part in the formation of the fertilization membrane and the hyaline
membrane, which is a thin transparent fibrillar structure, a few microns thick,
that directly borders the plasma membrane of the zygote.

Cleavage : A definitive typical radial cleavage is observed in sea urchins
(Figures 95-97). In Paracentrotus lividus (Boveri, 1901) the disposition of
individual blastomeres is distinctly visible in the early stages of development.
The first two divisions of the egg occur in a meridional direction, giving rise
to four equal blastomeres. The third division is equatorial. After this, in
Paracentrotus lividus four nonpigmented animal and four pigmented vegetal
blastomeres are formed. Eventually, the animal blastomeres divide
meridionally, giving rise to eight mesomeres, while the vegetal blastomeres
divide longitudinally, giving rise to four pigmented macromeres and four
nonpigmented vegetal micromeres. Mortensen (1938) observed that in
Prionocidaris baculosa the fourth division occurs in the meridional plane in
all the blastomeres, as a result of which two coronas of eight cells each are
formed. In a large majority of sea urchins, cleavage proceeds according to
that described by Boveri in Paracentrotus lividus and the 16-blastomere stage
leads to formation of micro-, meso-, and macromeres. The fourth division is

140

often asynchronous, 1.e., blastomeres of the vegetal quadrant divide a few
minutes earlier than the blastomeres of the animal quadrant and form a brief
12-cell stage.

Thereafter, during the fifth division the mesomeres divide in the latitu-
dinal plane and the macromeres in the meridional plane; the division of the
micromeres proceeds with some delay in the latitudinal plane and the stage
of 32 blastomeres is preceded by 20- and 28-blastomeres stages. After the
sixth division, the order of disposition of the blastomeres and the synchrony
of their division are disturbed; only the macromeres form two regular crowns.

0 100 pm
Ee
Figure 95: Beginning of cleavage in Scaphechinus griseus.
A—two blastomeres; B—four blastomeres.

Figure 96: Early cleavage in Strongylocentrotus intermedius.
A— stage of 8 blastomeres; B—stage of 16 blastomeres; ma—macromere; me—mesomere;
mi—micromere.

141

mi

Oo 100 ym 0 100 pm
a (a es ee a

Figure 97: Stage of 32 blastomeres: view from the animal pole.
A—Scaphechinus_ mirabilis; B—Strongylocentrotus intermedius Optical section.
Legend same as in Figure 96.

In subsequent divisions the differences in size of blastomeres gradually dis-
appear (Selenka, 1880; Fewkes, 1893). In sea urchins with direct develop-
ment, micromeres are not formed during division and the fourth division is
uniform (Raff, 1986).

Blastula

In many species of sea urchins the blastula is formed on the first day of
development. According to Onoda (1938), blastula of Astriclypeus manni
hatches 4.5 hrs after fertilization. According to our data, in Scaphechinus
mirabilis the blastula also leaves the membrane after 4.5 hrs. In urchins of
the genus Strongylocentrotus, the blastula appears after 10 hrs in S. nudus
and S. intermedius (Buznikov and Podmarev, 1975) and after 13 hrs in S.
pulcherrimus (Onoda, 1936). The slowest blastula development occurs in
Scaphechinus griseus (16 hrs) and Echinocardium cordatum (28 hrs), though
for the latter species McBride (1918) has given a duration of 10 hrs.

Possibly, this is because he investigated the development of E. cordatum
on the coast of Scotland, where the species spawns at much lower tempera-
tures than in the Sea of Japan, where we conducted our observations. On the
average, the development of sea urchins from fertilization to the blastula
stage takes 5—8 hrs (Onoda, 1931, 1938; Aiyar, 1936). The blastula is
spherical and possesses an extensive blastocoel (Figure 98). In most species,
in the early blastula stage the contact between the blastomeres is relatively
weak. Only in the apicolateral areas they are joined by desmosomes. Later,
the blastomere contact strengthens and the wall of the blastula consists of
densely arranged cells. The inner surface of these cells, facing the blastocoel.,
is lined with a thin 0.1 fm layer of protein and polysaccharide material,
which had the function of the basal membrane (Okazaki, 1975). The

142

blastocoel contains mucopolysaccharides secreted by the blastomeres (Monne
and Harde, 1951). Cilia form on the blastula before it leaves the membrane;
each blastomere bears a single cilium. Some time after formation of cilia, the
blastula is immobile; then the cilia begin to move and the blastula initially
starts to rotate slowly inside the membrane. The blastula is capable of rotating
both in a clockwise and an anticlockwise direction around the animal-vegetal
axis. The direction of movement changes at brief halts (Fewkes, 1893). During
rotation the blastula veers to the margin and begins to “rub” it. The blastula
hatches after the 10th division due to the action of a hatching enzymes
secreted by the blastomeres beginning from the 8th division. After hatching,
the vegetal wall slightly flattens, and the region of the animal pole thickens
and forms an apical organ with long immovable cilia (Selenka, 1880; Okazaki,
1975). The blastula swims with its animal pole forward while rotating around
the animal-vegetal axis (Maruyama, 1981).

Thus, in sea urchins the embryo leaves the membrane in the blastula
stage to commence its free-swimming mode of life.

Gastrula

Within a few hours after the blastula has hatched, the cells of the mes-
enchyme lose their cilia and begin to migrate from the region of the vegetal
pole into the blastocoel; these cells later produce the spiculogenous syncy-
tium. This is followed by gastrulation. Its mechanism in sea urchins has been
described in detail by Gustafson (1963, 1964, 1975). In the course of gastru-
lation, the cells of the vegetal pole invaginate inside the blastocoel, to form

0 100 pm 0 100 ym
———————— OO

Figure 98: Blastula before leaving the membrane.
A—Scaphechinus mirabilis; B—Strongylocentrotus nudus.

143

the primary gut (archenteron) which in sea urchins is located at an angle to
the animal-vegetal axis. At the place of the vegetal pole a blastopore forms
(Figures 99, 100). The process of formation of an early gastrula in sea urchins
proceeds at a variable rate. In the sand dollars Echinarachnius parma and
Scaphechinus mirabilis, it takes just 8 hrs from the moment of hatching of the
blastula, while a slow rate of development, 2 days, has been reported for
Echinus esculentus (McBride, 1903). The late gastrula appears in
Echinarachnius and Scaphechinus mirabilis 12 hrs after hatching of the blas-
tula; a similar time has been reported for Echinostrephus molaris (Onoda,
1936). In other species of sea urchins the process of gastrulation is completed
within 14—19 hrs (Onoda, 1931, 1936, 1938; Fenaux and Fenaux, 1974), in
still others only after 23—32 hrs (Aiyar, 1936; Onoda, 1936, 1938; Kryuchkova,
1977).

After the formation of the archenteron, the cells of the primary mesen-
chyme begin to accumulate at two sides of its base. Soon one can distinguish
a small calcareous granule in the center of each such cluster which gradually
acquires the shape of a triradiate spicule. From this moment, the formation
of the larval skeleton begins (Figure 100). The formation and growth of the
skeletal rays were thoroughly studied by Okazaki (1960, 1963). Simulta-
neously with the formation of the calcareous granules, the coelomic sac
separates from the upper end of the archenteron. This process is accompanied
by the expulsion of the cells of the secondary mesenchyme (Gustafson and
Wolpert, 1967). The coelomic sac soon divides into right and left parts. After
this, in the region of the future esophagus an invagination forms, which
gradually deepens and reaches up to the upper end of the archenteron, causing
the walls of the archenteron and ectoderm of the esophagus to rupture, which
leads to the formation of a through gut. From this moment the blastopore
assumes the function of an anus. Soon the region of the vegetal pole of the
gastrula flattens and the animal pole region inclines somewhat towards the
future dorsal side (Figure 101). The larva, still entirely covered with cilia,
acquires the shape of a prism. This process has been studied in detail by
Onoda (1931) in Heliocidaris crassispina.

Prism Stage

Duration of this stage, corresponding to the dipleurula in sea stars, has
seldom been observed.

Differentiation of the intestinal tube into the esophagus, stomach and
small intestine occurs in the prism stage. As a result of contraction of the
apical areas of the presumptive cells of the sphincters, two constrictions occur
in the digestive tract, which become the cardiac and pyloric sphincters of the
stomach (Burke and Chia, 1980). The regions forming the esophagus, stom-
ach and small intestine do not differ in intensity of cell proliferation; the total

144

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100 um

Figure 99: Early gastrula.
A—Strongylocentrotus nudus; B—Scaphechinus mirabilis

145

0 100 pm

Figure 100: Midgastrula.
A—Strongylocentrotus nudus; B—Scaphechinus mirabilis.

0 100 pm

Figure 101: Flattening of the vegetal pole and inclination of the animal-vegetal axis of the
larva in Strongylocentrotus intermedius.

146

number of cells of the digestive tract in the prism stage is about 100 (Burke,
1980).

On both sides of the larva, at the level of the esophagus, two tubercles
form — the rudiments of the first pair of arms. The entire ciliary cover
gradually reduces to a single ciliated band running along the margin of the
preoral depression and the rudiments of the arms. The ectoderm under the
ciliated band is thick and the cells of the ciliated epithelium are cylindrical.

The triradiate spicules formed in the gastrula stage now increase in size
and each ray transforms into a rod of the larval skeleton (Figure 102). The
coelomic sac enlarges somewhat but is still not differentiated. The rudiments
of the arms gradually enlarge, and the larva acquires the shape typical of the
early pluteus.

Pluteus I stage

In sand dollars, larval development up to the pluteus I stage proceeds
rapidly, during only 20 hrs in Astriclypeus manni (Onoda, 1938) and 34 to 36
hrs in Echinarachnius parma, Scaphechinus mirabilis and Scaphechinus griseus
(Kryuchkova, 1977). On an average, the pluteus I stage is attained by the
2nd—3rd day (McBride, 1914; Aiyar, 1936; Onoda, 1936, 1938). While inves-

, 2S 100 ym
Wl Meee ea Mis thts

Figure 102: Prism stage in Scaphechinus mirabilis.
ar—anterolateral rods; b—basal rods; po—postoral rods; sb—secondary basal rods.

147

tigating the development of 7ripneustes gratilla in Japan, Onoda (1936) es-
tablished that the pluteus I stage formed by the fourth day. For this very
species in the Mediterranean Sea, Fenaux and Fenaux (1974) found that at a
temperature of 21°C the pluteus I stage develops within 40 hrs. The longest
period of development required for attaining this stage, 8 days, was observed
in Heliocidaris crassispina (Onoda, 1931). All the structures of the larva are
formed in the pluteus I stage and simply grow in size in later stages.

Skeleton : The distinctive feature of the larvae of sea urchins is the larval
skeleton, which provides support for the larva. The pluteus I stage has two
pairs of arms — anterolateral and postoral. The anterolateral arms are almost
parallel to each other and support the apical part of the pluteus — the oral
lobe; the postoral arms diverge at an obtuse angle to each other. The
anterolateral rods of the larval skeleton are always simple while the postoral
ones in some species may be complex triradiate and perforated. The basal
rods are situated at the base of the larval body, they often join to form
complex structures. Sometimes, besides the principal basal rods, one or two
pairs of secondary basal rods also develop. Above the stomach, from the base
of the basal rod to the center of the larva, there may be an inner transverse
rod. In heart urchins another unpaired aboral rod is seen ( Figure 103). The
skeleton structure is of systematic importance and many researchers are en-
gaged in its study.

Feeding : Unlike larval sea stars, the body of sea urchin larvae is bor-
dered by a single ciliated band. The length of the outer cilia is 25—30 um.
The width of the band is 3—5 cells and each cell contains one cilium. Few
secretory cells are found only on the tips of the arms (Strathmann, 1971).

In the larvae of sea urchins the ciliated band between the anterolateral
arms makes a ventral loop to the side of the transverse section of the postoral
part of the general ciliated band (Figure 103). In the region of the peristome
water currents are created by beating of the cilia of the ventral loop and the
transverse part of the postoral band. Two currents are generated: an incurrent
into the peristome and an excurrent from it. As in the larvae of sea stars, the
region of the peristome in plutei bears cilia.

The mechanism of capture of food particles by cilia of the ciliated band
and transport of these particles to the oral opening in planktotrophic larvae
is common to all classes of sea urchins (see above). In echinoplutei the speed
of movement of the food particles along the ciliated band is 0.5 mm/sec at
13°C. As soon as the food particles are trapped by the cilia, they are moved
along the ciliated band to the peristomal field. In this region they move at a
speed of almost 0.5—1.4 mm/sec. Cilia of the peristomal field transfer the
food particles to the adoral band, which forms a loop that extends along the

148

Figure 103: General appearance of the pluteus | stage.
A — Strongylocentrotus pulcherrimus (Onoda, 1936); B— Spatangus purpureus
(Fenaux, 1972).
al — anterolateral rods; asp —aboral spicule; b — basal rods; int —inner transverse rods;
po — postoral rods; sb — secondary basal rods.

ventral side of the esophagus. Cilia of the aboral band transport food particles
into the oral opening, where they reach the esophagus.

To remove inedible food particles and, possibly, to ingest large particles,
the oral opening in the echinopluteus I stage can be broadened through the
action of a pair of special muscles — the posterior dilators. One end of these
muscles is attached to the upper ventral part of the esophagus and the other
end to the larval skeleton at the place of divergence of the anterolateral and
inner transverse rods.

Numerous cilia line the esophagus and pass the food particles to its
posterior part where they are stored until the circular esophageal muscles
begin to contract and the cardiac sphincter opens up. The food mass enters
the stomach where sorting takes place. Two types of cells have been observed
in the stomach: cells secreting digestive enzymes and absorbing and sorting
nutrients, and cells phagocytizing food particles as a whole (Burke, 1981).
Experiments conducted by Strathmann (1971) have shown that when carmine
and crystals of calc1um carbonate together with algal culture reach the stom-
ach, the algae remain in the stomach while the carmine and calcium carbon-
ate pass through it unobstructed to the small intestine and are egested. The
separation of particles is observed until they reach the lower part of the
stomach. Clumps of algae circulate in the stomach for a long time. The time
of passage for the food through the digestive tract is, on average, 30 min.

149

When the pyloric sphincter is opened, the food particles from the stom-
ach enter the small intestine. Defecation is accompanied by a contraction of
the intestine, which happens when the pyloric sphincter is closed and the anal
sphincter is open (Figure 104). The larvae of sea urchins feed on various
species of microalgae whose diameter does not exceed 85 um, namely, spe-
cies of Amphidinium, Phaeodactylum, Dunaliella, and others.

Figure 104: Division of the intestinal canal into sections in Echinarachnius parma
(Fewkes, 1893).
asph—anal sphincter; csph—cardiac sphincter; e—esophagus; hg—hind gut,
psph — pyloric sphincter; s — stomach.

Although phytoplankton is the main food of sea urchin larvae, the plutei
of the heart urchin Echinocardium cordatum can obtain a large part of their
daily ration from soluble organic matter even at its fairly low concentration
in water (Vyshkvartsev and Sorokin, 1978). The pluteus of Dendraster
excentricus stores nutrients in the cells of the stomach wall (Chia and Burke,
1978).

Respiration, transport of metabolites, and excretion: The larva has no
special organs of respiration. Respiration is performed by the entire body
surface. Hemal and excretory systems are also absent. Transport of nutrients
within the larval body occurs through the primary and secondary body cavi-
ties. Excretion of metabolic products, after formation of the madreporic pore,
apparently proceeds with the participation of coelomic sacs.

At this stage in the larvae of sea urchins, the coelomic sacs enlarge along
the esophagus and divide into two: the anterior —axohydrocoel and the
posterior — somatocoel. The left axohydrocoel broadens anteriorly, becomes
thin-walled, and forms an ampulla in which the stone canal opens. The
madreporic pore opens on the left side of the larva and connects the
axohydrocoel with the external medium (McBride, 1903)— Figure 105.

150

eigeri | e
J}

Figure 105: Scheme of development of coelomic sacs in Echinus esculentus (McBride, 1903).
A — prism stage; B — pluteus I stage; C — pluteus II stage.
hc — hydrocoel; mp — madreporic pore; sc-— stone canal.

Locomotion: The ciliated band performs a locomotor function. At this
stage, locomotion occurs along the anterolateral and postoral arms and the
peristomal depression. When the larva moves, the cilia in some sections of
the band remain erect while those in other areas bend to one side or the other.
Thus, a wave is created which traverses the entire ciliated band. The larva can
change the direction of its movement and turn; in this process a change in the
direction of beating of the cilia occurs, which is preceded by a brief pause.
The direction of water currents created by beating of the ciliated band is
opposite to the direction of movement of the larva. When moving forward
with the arms, the current is directed by the wave motion of sections of the
band on the outside of the arms to the base of the larva. When the larva is
motionless, beating of the right sections of the band is directed in the direc-
tion opposite to beating of the left sections of the band. When the larva turns,
beating of the cilia is noticeable only on the outer side of the direction of
turning. Movement of the pluteus in a reverse direction is accomplished by
beating of the cilia of the ciliated band in a forward direction.

The speed of horizontal movement of the larvae of Strongylocentrotus
dreebachiensis, S. purpuratus, and Dendraster excentricus is 0.3—0.5 mm/sec
at 10—15°C (Strathmann, 1971; Strathmann ef al., 1972).

Nervous system and sense organs : The first mention of the presence of
nervous elements in the larvae of sea urchins is found in the work of McBride
(1903), who speaks of nerve fibrils situated above the adoral band. However,
no information whatsoever on the structure of the larval nervous system was

“151

available until histochemical methods and electron microscopy made identi-
fication of the nervous elements possible. Some works devoted to this prob-
lem have recently been published. Ryberg (1973, 1977) and Ryberg and
Lundgren (1977) described the cells forming the ectodermal nerve network
and the network surrounding the digestive tract as nerve cells of the sea
urchin larvae. However, it later became clear that the ultrastructure of these
cells nerve is different. The true nervous system of the larva is associated
with the ciliated band and muscle elements. The nerve cells are situated along
the ciliated band under which pass the axonal tracts — Figure 106 (Burke,
1978, 1983a, b). The nervous system of a pluteus develops from the cells of
the animal place of the gastrula containing catecholamines (Burke, 1983a, b).

Figure 106: (a) axonlike projections of cells of the ciliated band of a 60-hr pluteus of
Dendraster excentricus, Bar = 0.5 um; (b) cells of the ciliated band of a 72-hr pluteus; arrow
indicates an axonlike projection from the base of one cell, Bar - = | um; (c) higher magnification
of the axonlike process in (b), Bar = 0.5 um.
bl — basal lamina; dev — dense core vesicles; m— mitochondria; mt— microtubules
(Burke, 1983).

Pluteus II Stage

The rate of development up to the pluteus II stage may differ signifi-
cantly in various species. Thus Astriclypeus manni (Onoda, 1938) requires
only 45 hrs to attain this stage from the moment of fertilization. The devel-
opment of stage II in the sand dollars Echinarachnius parma, Scaphechinus
mirabilis, and Scaphechinus griseus takes three to five days. Echinarachnius

i52

brevis takes 15 days for this process (Onoda, 1938). McBride (1903) noted
that sea urchins of the genus Echinus require 7—8 days to complete the
pluteus II stage. A similar period is necessary for Salmacius bicolor (Atyar,
1936). Fundamental changes in the skeleton of the larvae of sea urchins occur
at this stage.

Skeleton : In addition to the anterolateral and postoral arms, posterodorsal
arms, develop in the pluteus II stage on the dorsal side between the anterolateral
and postoral arms. In some sea urchins the rods in the pairs of arms are simple
but in others complex and fenestrated. The rudiment of the dorsal arch is
situated at the level of the upper third of the stomach. In the heart urchins
the ends of this arch elongate very quickly, providing the beginning for the
rods of the preoral arms. These rods are simple in all sea urchins (Figure 107).

Figure 107: General view of pluteus II stage.
A —Parasalenia gratiosa (Onoda, 1938); B — Echinocardium mediterraneum (Fenaux, 1972).
al — anterolateral rods; asp— aboral spicule; b — basal rods; int — inner transverse
rods; pd — posterodorsal rods; pl — posterolateral rods; po — postoral rods; pr — preoral
rods; sb —secondary basal rods .

Respiration, transport of metabolites, and excretion: At this stage a
further complication in the structure of the coelomics sacs occurs in the
larvae. In particular, the left axohydrocoel divides into the axocoel and
hydrocoel — rudiment of the ambulacral system of the definitive sea urchin
(McBride, 1903).

153

Locomotion : With increase in the number of arms, the ciliated band
elongates. After the complete development of the posterodorsal arms, the
larva can spread the postoral and posterodorsal arms and thereby come to a
stop. The arms are moved by muscles which appear at the site of joining of
the postoral and posterodorsal rods with the basal rods. These muscle fibers
were observed by McBride (1903) in larvae of the genus Echinus. Grave
(1902) found muscle fibers in larvae of Mellita testudinata at the posterior
end of the body, which were situated between the rods proceeding from here
(Figure 108). On contraction, the postoral and posterodorsal arms diverge to
the sides.

Figure 108: Arrangement of muscle fibers in the posterior end of the Mellita testudinata
pluteus (Grave, 1902).
bw — body wall; hg —hind gut; mf— muscle fibers; sr — skeletal rods.

Nervous system and sensory organs: The nervous system remains un-
changed. In some species, pigment granules which perform a photosensory
function begin to accumulate in the cells at the tips of arms. According to
Ryberg and Lundgren (1979), localization of the pigment cells can be ob-
served in the regions of active morphogenetic processes. Histochemical meth-
ods revealed a carotene-protein complex in the pigment cells. The most
common carotenoid in the sea urchins is echininon, which is similar in its
function to the provitamin A. The pigment cells work as photoreceptors and
play an important role in the vertical migration of larvae.

Pluteus III Stage

Complete development of the larvae of sea urchins, according to many
investigators, requires different time spans. Larvae of the sand dollars
Astriclypeus manni (Onoda, 1938), Echinarachnius parma, Scaphechinus
mirabilis, and Scaphechinus griseus require only 5—7 days while
Echinarachinus brevis needs 38 days (Onoda, 1938); completely developed
larvae appear in sea urchins of the genus Echinus in 18-20 days (McBride,

154

1903). The average time requirement for attaining the pluteus III stage is 12—
15 days from the commencement of development.

As in the previous stage, the maximum changes are observed in the larval
skeleton and coelom.

Skeleton : In most species the basal part of the larval body is broadened;
sometimes a transverse rod of very complex structure is situated here. A
fourth pair of arms, the preoral, develops in which the rods are a continuation
of the ends of the dorsal arch. These rods are always simple. In some heart
urchins, anterior to the preoral arms on the dorsal side, another pair of arms,
the anterodorsal, develops, whose rods initially arise as processes of the
dorsal arch. These, like the preoral rods, are simple in shape. In other species.
yet another pair of arms, the posterolateral, emerges, whose rods originate
from the upper ends of the arcuate rods serving as the base of the aboral rod
(Figure 109).

Feeding : After the appearance of the preoral arms, the system of ciliated
bands in the peristomial field becomes complicated. The ventral loop of the
anterodorsal band no longer participates in filtration of feed particles from the
water. It is replaced by a preoral transverse band. An adoral band likewise
develops. The water currents created by these bands become complex.

Enlargement of the oral opening, priorly effected by the posterior dilater
muscles, is now enhanced by a pair of anterior muscles, the dilaters, situated
between the body wall in the region of the anterolateral arms and the preoral
transverse band. The rods of the preoral arms pass through these muscles
(Strathmann, 1971).

According to Burke (1981), at this stage in the pluteus of Dendraster
excentricus the esophagus is surrounded by muscle fibers, which are circular
in the upper part and longitudinal in the lower. The stomach sphincters
consist of myoepithelial cells with transversely striated fibers. The stomach
wall is lined with secretory cells and cells absorbing and storing nutrients.
The intestinal wall is made of epithelial nonspecialized cells.

Respiration, transport of metabolites, and excretion: At this stage, the
coelom of the right side remains unchanged. The left coelom enlarges, par-
ticularly the hydrocoel, in which five primary protuberances appear.

Respiration : The ciliated band enlarges with the increase in the number
of arms. To support the larval body in water and to ensure locomotion at this
stage, in some species additional ciliary fields develop — the epaulettes, which
may comprise several pairs. Sometimes they are so closely disposed to one
another that an additional annular ciliated band is formed (Figure 110). The
length of the cilia on the epaulettes may vary in different species of sea

Figure 109: General view of the pluteus III stage.
A —Prionocidaris baculosa (Mortensen, 1938); B — Lovenia elongata (Mortensen, 1937).
ad —anterodorsal arm; al— anterolateral arm; asp —aboral spicule; pd — posterodorsal
arm; pl — posterolateral arm; po — postoral arm; pr— preoral arm.

156

Figure 110: Epaulettes and pedicellaria in the pluteus of Echinometra mathaei
(Onoda, 1936).
lep — lower epaulettes; p— pedicellaria; uep — upper epaulettes.

urchins; in Strongylocentrotids it is 35 um. On the epaulettes, as also at the
base of the ciliated band, beating of the cilia is undulatory (Strathmann,
1971). In other species, in place of the epaulettes between the postoral and
posterodorsal arms, the integument and corresponding areas of the ciliated
band become stretched and vibratile lobes are formed (Figure 111).

The beating wave of cilia on the epaulettes of strongylocentrotids and
lobes of Dendraster is directed toward the median line of the larva. Such an
unusual direction of beating possibly counteracts rotation of the larva, created
by the beating of the ciliated band (Strathmann, 1971). Neither the cilia of
the epaulettes and various lobes nor the cilia of the bands bordering the aboral
rod of the pluteus of heart urchins participate in the seizure of food particles;
they serve only for locomotion.

Nervous system and sense organs: The nervous system of the larvae
remains unchanged. Pigmentation intensifies on the arms and new pigment
centers appear. Especially intensive pigmentation is observed in the region of
the stomach, coelom and amniotic sac; the latter appears at this stage (Figure
12)

Attachment apparatus : Settling, searching the substrate, and temporary
attachment to it are ensured in the metamorphosing larvae of sea urchins by
the five primary plates formed during metamorphosis at the base of the

157

Figure 111: Vibratile lobe in the pluteus of Laganum depressum (Mortensen, 1938).
vl — vibratile lobe.

ambulacral system of the definitive urchin. Hence, the attachment apparatus
and the act of settling are described at the end of the section on metamor-
phosis.

METAMORPHOSIS

As soon as the larva attains complete development, invagination of the
ectoderm takes place from the left side between the postoral and posterodorsal
rods. This invagination advances and acquires the shape of a small sac, which
separates from the body wall. Its formation was reported earlier by Fewkes
(1893), who called it the “Vasoperitoneal sac”. McBride (1914) designated
this structure the “amniotic sac”. It grows and descends toward the stomach
up to its contact with the left hydrocoel. A single complex is formed, which
comprises the hydrocoel and two-layered wall of the amniotic sac. McBride
(1914) noted that in Echinocardium cordatum the amniotic sac does not
communicate with the external medium, whereas in larvae of the genus
Echinus it forms a narrow canal opening externally. Aiyar (1936), based on
McBride, indicated that in larvae of the genus Echinus the coelomic wall is
always separated from the stomach by a space, while in Salmacis bicolor,
whose development was investigated by Aiyar, the coelomic wall firmly
adjoins the stomach.

Formation of the definitive juvenile occurs in the amniotic sac. This
is accompanied by the disintegration of reorganization of larval structures.

158

7

Figure 112: Psammechinus miliaris (Ryberg and Lundgren, 1979).
Arrows show disposition of pigment cells in the pluteus.

Thickening of the floor of the amniotic sac constitutes the imaginal disk of
organs of the oral half of the definitive urchin. As in sea stars, the oral-aboral
axis of the definitive animal lies at an angle to the principal axis of the larva.
Metamorphosis in sea urchins is markedly catastrophic in nature. Cidaroid sea
urchins might be an exception to this rule (Emlet, 1988).

Skeleton: Development of the definitive test in the amniotic sac is ac-
companied by resorption of rods of the larval skeleton beginning, first of all,
with rods supporting the larval body. The resorption of rods supporting the
arms is observed only after the juvenile individual has settled on the substrate
and moves rapidly for a few hours (Fewkes, 1893; McBride, 1903, 1914,
1918; Ubisch, 1913; Onoda, 1931; Atyar, 1936).

During the development of the definitive test the coronal elements de-
velop first, i.e., the interambulacral and ambulacral plates and spines. Forma-
tion of the oral and aboral sides terminates only after the juvenile individuals
have settled on the substrate (Gordon, 1926a, b, 1928; Onoda, 1931;
Kryuchkova, 1979a, b, c).

159

Formation of test in regular sea urchins (subclass Regularia): In
Strongylocentrotus nudus and Strongylocentrotus intermedius the interambulacral
plates and their spines appear first. Following the development of the first
interambulacral plates, the twin rudiments of the first ambulacral plates appear
(Figure 113). Then the ocular plates develop: four of them independent of the
larval skeleton, with the first one around the fragment of the left posterodorsal
tod. Development of the genital plates is associated more closely with the larval
skeleton. As in Arbacia pustulosa (= A. lixula), Strongylocentrotus lividus
(Ubisch, 1913), and Heliocidaris crassispina (Onoda, 1931), in Strongylo-
centrotus nudus genital plates 1, 4 and 5 are also modified from the plate
constituting the base of the pedicellariae, which remain on the juvenile indi-
vidual for some time after it settles. In Strongylocentrotus intermedius the
plates that developed in the larvae III stage around the left posterodorsal and

Figure 113: Arrangement of the ambulacral and interambulacral plates in Strongylocentrotus
intermedius.

am — ambulacral plate; iam — interambulacral plate; op — ocular plate.

160

left postoral rods as well as the plate which appeared at the base of the larval
body, are transformed into genital plates. In all regular urchins the madraporic
or second genital plate forms around the appendage of the dorsal arch. Only one
genital plate, the third, is not associated in its development with the larval
skeleton (Figures 114 and 116).

As described above, in the larvae some species of regular urchins, at the
place of connection of the rods supporting the arms and at the base of the
larval body, growing pedicellariae are attached by their bases to the skeletal
plates. These are complex capitate formations attached to the plate by a short
stalk. The bulb is composed of three articulating blades with a dentate mar-
gin. The stalk is similar in structure to the rods of the juvenile individual and
has a tetrahedral base (Figure 116). These pedicellariae have a special system
of muscles for opening the blades. On the surface of each blade sensory cells
occur among the epithelial; each sensory cell bears one cilium surrounded by
a ring of microvilli. In structure and function these pedicellariae are quite
similar to those of the adult, although their development is completed in the
larva much before the rapidly developing processes of metamorphosis. The
larval pedicellariae, in all probability, perform a defensive function in the
settling individual (Burke, 1980). The mesenchymal cells of the rudiment of
the pedicellariae are differentiated into skeletogenic and myogenic cells. The
ectodermal cells of the rudiment produce the covering epithelium of the
pedicellariae, nerve, and sensory cells. The larval pedicellariae begin to func-
tion very early in the larva. During metamorphosis they are shifted to the
aboral surface of the definitive individual. The plates, or future bases, as
already mentioned, are transformed into genital plates. The juvenile spines
present on the settling urchins perform a defensive and partly locomotor
function, then later disappear (Ubisch, 1913).

The mouth apparatus and its skeleton form in regular urchins after the
juvenile has settled.

Formation of test in the sand dollars (subclass Irregularia, order
Clypeasteroida): In the development of Echinarachnius parma (Gordon, 1928;
Kryuchkova, 1979a), Scaphechinus mirabilis, and Scaphechinus griseus
(Kryuchkova, 1979a), the second and third interambulacral plates and their
spines are the first to appear (Figure 117). Subsequently, the ambulacral
plates develop. The ocular plates develop independent of the larval skeleton.

The genital plates, except for the second, that is, the madreporite, appear
after settling and are not associated with the larval skeleton. The madreporite
forms around the projection of the dorsal arch of the larva. Besides the five
genital plates, two additional ones develop on the aboral side. These plates,
like the genital ones, fuse to form the single complex madreporic plate of the
adult (Figure 118).

161

Figure 114: Aboral view of the young urchin Strongylocentrotus intermedius.
gp — genital plate; m— madreporic plate; op — ocular plate; pr — periproct.

The skeleton of the oral apparatus (Aristotle’s lantern) begins to form
very early. Dental cones appear after the emergence of the first ambulacral
plates. Rudiments of the alveoli and epiphyses appear before settling (Figure
119).

Formation of test in the heart urchins (subclass Irregularia, order
Spatangoida): According to Gordon (1926a) and Kryuchkova (1979a), in
Echinocardium cordatum during the development of the definitive test,
interambulacral plates and their spines are the first to appear (Fig. 120).

The ocular plates are not associated with the larval skeleton. The third,
first and fifth ocular plates appear before settling while the second and fourth
plates appear after the juvenile individual settles.

Development of the genital plates is associated with the remains of the
larval skeleton. The second plate, as in all urchins, develops around the
process of the dorsal arch. The third, fifth and fourth plates appear around
fragments of the left posterodorsal, left postoral, and aboral rods respectively.
Only the first genital plate develops independent of the larval skeleton (Figure
IZID

162

Figure 115: Aboral view of the young urchin Strongylocentrotus nudus.

gp — genital plate; p — pedicellaria; pr — periproct; tp — terminal podium; siam — spines
of the interambulacral plates.

No rudiments of the oral apparatus are formed in heart urchins. The oral
field is gradually furnished with plates. On the oral side there are five sphaeridia
and five buccal podia.

Feeding: After metamorphosis the nature of urchin feeding changes
sharply. Hence the trapping and digestive apparatuses are considerably re-
structured. The trapping apparatus of the larvae —the ciliated band —is
completely destroyed. Cells of the ciliated band, like the cells of other regions
of the larval epidermis, are dedifferentiated, disassociated from one another,
and subsequently phagocytized by the cells of the larval digestive system
(Chia and Burke, 1978). In the sea urchin Lytechinus pictus the larval arms
bend, rudiment of the definitive individual makes contact with the surface,
and the former lining of the amniotic sac surrounds the tissues adjoining the

Figure 116: Structure of
pedicellariae in the pluteus of
Strongylocentrotus nudus.

bp — base of pedicellaria.

163

oral surface and forms the definitive epithelium
(Cameron and Hinegardner, 1974, 1978). After
metamorphosis, in most sea urchins the special
oral apparatus functions to capture food; it is
called Aristotle’s lantern.

During the development of the definitive di-
gestive system the larval mouth and anus close
before settling, and the tissues of the larval di-
gestive system are completely reorganized. The
definitive esophagus consists of two parts; inves-
tigation of the floor of the amniotic sac (ectoder-
mal part) and investigation of the stomach wall
(endodermal part). The mouth initially opens in
the epineural sac bound by the primary floor of
the amnion below and the epineural fold above;
the mouth opens outside, in Salmacis bicolor for
example, 10-12 days after the juvenile urchin
settles (Aiyar, 1936). The intestinal canal, earlier

monolayered, now becomes multilayered. The stomach and a part of the
intestinal canal become folded. The larval stomach transforms in the anterior

Figure 117: Diagram of disposition of spicules — the forerunners of interambulacral plates

in the sand dollars.

al — anterolateral rod; da— dorsal arch; pd— posterodorsal rod; po— postoral rod;
spp — spicule-forming plate; sps— spicule-forming spine.

164

Figure 118: Aboral view of the sand dollar.
anp — anal plate; ap (1, 2) — additional plates; m — madreporite; op (1, 2, 3, 4, 5) ocular
plates.

section of the definitive intestine, describing a loop, and the larval intestine
produces a counterloop in the definitive intestine. The definitive anus opens
again (Figure 122).

As in sea stars, the function of respiration is passed on to the definitive
epithelium and transport of metabolites to the hemal/perihemal systems and
visceral coelom, while excretion of products is passed on to the coelomocytes.

Locomotion : One of the most important functions of the larval ciliated
band is locomotion. During metamorphosis the ciliated band is replaced by
a new — the embulacral— system, specialized for performing this function.

165

ee

iam

Figure 119: Arrangement of the first dental cones and sphaeridia in the sand dollar.
am —ambulacral plate; de — dental cone; iam — interambulacral plate; sph — sphaeridium.

As in all echinoderms, the main rudiment from which it develops is the
hydrocoel. Long before larval settling, the hydrocoel begins to form the first
five processes that will become the radial canals of the ambulacral system of
the adult urchin. After this, the hydrocoel bends and takes the shape of a ring,
forming the ring canal of the ambulacral system (Figure 123). Soon the
coelomic processes are seen to rest upon the bottom of the amniotic sac. In
the opinion of McBride (1914), these processes in Echinocardium cordatum
are rudiments of the radial canals of the future urchin. A similar picture was
observed by Fewkes (1893) during the development of Echinarachnius parma
by Aiyar (1936) for Salmacis -bicolor (Figure 124), and by other investigators
for various urchins. By the time of settling, or soon after it, the first ambu-
lacral plates have formed. Aiyar (1936), while describing the metamorphosis

166

Figure 120: Arrangement of ambulacral and interambulacral plates in Echinocardium
cordatum.
asp—aboral spicule; iam —jinterambulacral plate; pd—posterodorsal rod;
p! — posterolateral rod; siam — spicules of the interambulacral plates; spam — spicules
forming an ambulacral plates;.

of Salmacis bicolor, mentioned that epaulettes remained for some time after
resorption of all the rods and continued to function even though the young
urchin had already begun to move using the spines and podia.

Rudiments of the nervous and reproductive systems appear. Their further
development, like that of the ambulacral system, occurs after settling.

Settling : During development of the juvenile in that period when larvae
are still to be found in the plankton, five primary ambulacral podia develop
in some urchins, which are usually much larger than the normal ambulacra

167

Figure 121: Aboral side of the young heart urchin Echinocardium cordatum.

anp —anal plate; gp (1, 3, 4, 5)— genital plates; iam — interambulacral plates; m—
madreporite; op (1, 2, 3, 4, 5) — ocular plates.

(McBride, 1903; Ubisch, 1913; Onoda, 1931, 1936, 1938; Aiyar, 1936;
Kryuchova, 1979b). Primary podia do not form in the sand dollars (Kryuchova,
1979b). McBride (1903) noted many years ago that after the primary podia
had developed, the larvae of sea urchins of the genus Echinus begin to touch
the container well with them as though seeking an attachment site in order
to complete metamorphosis.

The larvae of the sea urchin Strongylocentrotus purpuratus settle mostly
on coralline algae (Rowley, 1987). Cameron and Hinegardner (1974) identi-
fied the factors responsible for settling and demonstrated that for Lytechinus
pictus and Arbacia punctulata one of the factors was the bacterial film formed
on the walls of the containers holding larvae during metamorphosis. The
larvae of sea urchins generally prefer the bacterial-algal film common in the
sea as a substrate for settling (Chia et al., 1984). Parechinus angulosus

168

St

f: %, 38: Le
ony

des

les

Figure 122: Development of the definitive digestive system in Echinus esculentus (McBride,

1903).

A — larva III stage; B — juvenile; a— anus, des — definitive esophagus; hg —hind gut;
les — larval esophagus; st — stomach.

Figure 123: Formation of processes
in the amniotic sac in
Echinocardium cordatum
(McBride, 1914).
as — amniotic sac; cp — coelomic
processes.

Figure 124: Formation of ambulacral
ring canals and radial canals upon
branching of hydrocoel in
Echinarachnius parma (Fewkes,
1893).
arc —ambulacral ring canal; cp —
coelomic processes; pd — posterodosal
rod; rac —ambulacral radial canal.

requires the presence of shell fragments previously attached to the adult
animals. Mortensen (1921) observed a delay in settling of the larvae of
Mellita sexiesperforata in the absence of a sandy substrate. A peptide respon-
sible for the metamorphosis of larvae has been isolated from the tissue ex-

169

tracts of the adult sea urchin Dendraster excentricus (Burke, 1984, 1986).
Probably, this protein serves as the active agent at induction of metamorpho-
sis in larvae using water from the aquarium in which the adult individuals are
held; in nature, or using sand from natural habitats (Highsmith, 1982). Even
before some of this corroborative data was available, Strathmann (1978) had
concluded that the primary podia ought to perform the function of attachment
and consequently possess secretory and sensory cells capable of receiving
mechanical and chemical stimuli. In 1980, Burke investigated the morphol-
ogy of the primary podia of urchins and demonstrated that sensory and secre-
tory cells actually are present on the surface of the suction disks of the podia.
Sensory cells occur over the entire surface of each disk and lie in groups of
3—5 cells along its margin. Apically, each cell bears a simple cilium. The
basal ends of the sensory cells taper to the axonal process, which constitutes
the subepithelial nerve plexus (Figure 125). Thus, the presence of sensory and
secretory cells in the attachment of primary podia disks plays an important
role in scouting the substrate, settling, and successful completion of metamor-
phosis of the urchin.

LECITHOTROPHIC LARVAE

Among the present-day “regular” sea urchins only a few species exhibit brood
care. They are representatives of the order Cidaroida, including Austrocidaris
canaliculata (Hyman, 1955), Ctenocidaris nutrix, and Stereocidaris nutrix
(Baranova, 1968) from the Antarctic waters. They have special brood cham-
bers — dermal outgrowths — situated in the buccal field or the periproct. The
developed young is later transferred to the aboral side of the test where it
remains for some time before undertaking independent existence. Besides
cidaris, Hyrsiechinus coronatus (Mortensen, 1903) seems to be the only known
regular urchin with brood care. The young in this species are transferred to
the apical system of plates around the raised periproct.

In “irregular” urchins, the brood chambers are situated in the female
petaloids. Such urchins, are Fibularia nutriens (Mortensen, 1948; Hyman,
1955) from the order Clypeasteroida (sand dollars), which have a small in-
flated test and are found in the Pacific. Among the heart urchins (order
Spatangoida), there are also species in which the young develop in brood
chambers. One such urchin, Abatus (Hemiaster) cavernosus (Meisenheimer,
1921; Kilias, 1969), occurs around Kerguelen Island in the Southern Indian
Ocean.

The presence of brood chambers is usually observed in species living
either in Antarctic waters or at great depths where the water temperature is
low. Yet, in some sea urchins inhabiting waters of low temperatures, brood
chambers are absent. This is observed in Pourtalesia jeffreysi (order

170

Snatangoida) living in the Atlantic Ocean and having an egg diameter of 3.2
mm (Thorson, 1936). On the other hand, sea urchins with large eggs and
lecithotrophic larvae occur in the tropical zone of the Pacific Ocean. They
belong to the following three orders: Echinothurioida — Asthenosoma ijimai;
Cidaroida — Heliocidaris erythrogramma, and Clypeasteroida— Peronella
japonica. The development of these three species has been fairly well studied.

In Peronella japonica (Mortensen, 1921; Okazaki and Dan, 1954) the egg
diameter is 300 tum. Already in the late gastrula stage, invagination appears
in its anterior end which enlarged to form the amniotic sac between the
archenteron and ectoerm. In the pluteus the arms are sometimes not at all
developed, but usually one pair of arms may be present. After 60 hrs, the
amniotic sac in which development of the definitive individual takes place is
everted and the young urchin begins to move on the substrate by means of
the ambulacral podia. Remains of the larval body are retained for some time
(Figure 126).

In Heliocidaris erythrogramma (Mortensen, 1921) the egg diameter is
500 um. About 42 hrs after fertilization, the amniotic mvagination appears,
which remains open. It lies in the posterior part of the larva, is covered with
cilia, and occupies three-fourths its circumference. On the fourth day of
development, the oral disk of the definitive individual appears on the outer
surface and the ends of the larval body bend to the aboral side. The devel-
oping young urchin feeds on the yolk present in the larval body. According
to the data of Mortensen, the development of this urchin takes two days
(Figure 127).

The largest eggs, 1.2 mm in diameter, have been described in Asthenosoma
ijimai (Amemiya and Tsuchiya, 1979). The blastula hatches after 27 hrs. The
gastrula is formed after 48 hrs. By the third day of development, the late
gastrula has become flattened in a dorsoventral plane. After 4—5 days, two
tubercles appear on the ventral side of the larva. At this stage, the larva
remotely resembles the early bipinnaria of the sea stars. Four strongly reduced
arms appear in the larva after five days, which are devoid of rods and differ
in position from the arms in planktotrophic larvae (Figure 128). At this time,
the rudiments of organs of the juvenile also appear but the amniotic sac does
not develop. By the end of the fourth week, metamorphosis has been com-
pleted and the juvenile settles on the substrate (Figure 128).

IDENTIFICATION OF PELAGIC LARVAE OF SEA URCHINS
(Terminology and Diagnostic Characters)

The larvae of sea urchins have an elongate body that may taper in the basal
part. At the level of the esophagus, several pairs of processes are seen, the
so-called arms. The characteristic feature of the larvae of sea urchins is the

171

Table 5: Type of development of sea urchins

Species Type of Source
development

Order Echinothurioida

Asthenosoma ijimai Lecithotrophic Amemiya and Tsuchiya,
larva 1979

Order Cidaroida

Aporocidaris milleri Brood care Mortensen, 1927; Hyman, 1955
Ctenocidaris nutrix Same Thomson, 1878; Hyman, 1955
Ctenocidaris spinosa Same Baranova, 1968; Koehler,
1926; Hyman, 1955

Ctenocidaris geliberti Same Mortensen, 1950; Hyman, 1955
Ctenocidaris perrieri Same Mortensen, 1950; Hyman, 1955
Austrocidaris canaliculata Same Thomson, 1878; Hyman, 1955
Goniocidaris umbraculum Same Mortensen, 1925; Hyman, 1955
Notocidaris gaussensis Same Mortensen, 1909; Hyman, 1955
Rhynchocidaris triplopora Brood care Mortensen, 1909; Hyman, 1955
Stereocidaris nutrix Brood care Baranova, 1968

Order Echinoida

Heliocidaris erythrogramma Lecithotrophic larva Hyman, 1955; Mortensen, 1921

Order Temnopleuroida

Hypsiechinus coronatus Brood care Mortensen, 1903; Hyman, 1955

Order Clypeasteroida

Fibularia nutriens Brood care Mortensen, 1948; Hyman,1955
Peronella japonica Lecithotrophic larva Mortensen, 1921; Okazaki
and Dan, 1954

Order Cassiduloida

Anochanus sinensis Brood care Grube, 1868; Hyman, 1955
Tropholampas loveni Same Clark, 1923; Hyman, 1955

Order Spatangoida

Abatus cordatus Brood care Thomson, 1878; Hyman, 1955
Abatus cavernosus — Brood care Meisenheimer, 1921; Kilias, 1969
Plexechinus nordenskjéldi Same Mortensen, 1950; Hyman, 1955

Order Holasteroida

Pourtalesia jeffreysi Same Thorson, 1936

he

Figure 125: Strongylocentrotus droebachiensis (Burke, 1980). Sagittal section through the
terminal podium of a juvenile.
bnp — basiepithelial nerve plexus; cd — calcified disk; ct — connective tissue; mu — muscle
layer of the podium; myc — myoepithelial cells; nr—nerve ring; sec — secretory
cells; sen — sensory cells.

Figure 126: Sagittal section of the primordium of Peronella japonica (Okazaki and Dan,
1954).
A — early larva; B — late larva.
am — amniotic sac; arch —archenteron; bl—remains of blastopore; c —coelom;
g—rudiment of gut; h — hydrocoel.

173

B

Figure 127: Development of primordium of Heliocidaris erythrogramma (Kaestner,* 1963).
A — early larva; B — late larva.
am _— amniotic sac; amp — ambulacral podia.

Figure 128: Development of Asthenosoma ijimai (Amemiya and Tsuchiya, 1979).
A — blastula; B— 4-day-old larva; C — 14-day-old larva; D—same, aboral view;
E — juvenile.
a— arms; amp —ambulacral podia; sp —spine of interambulacral plates; tp — terminal
podia.

presence of an endoskeleton consisting of rods, which differ in structure in
different groups of these animals. These rods may fuse or simply be contigu-
ous. Rods proceeding from the esophagus and descending to the edge of the
body of the larva are called basal and usually comprise one pair. In addition
to these rods, in some species of sea urchins there may be one or two more
pairs extending parallel to the basal rods and often joining them. These are
the secondary basal rods. From the basal as well as secondary basal rods,
transverse rods are directed inward. These may be in two pairs, anterior and
posterior, and both pairs may not be present simultaneously in every species.

174

The rods extend inside, and lend support to, the arms. Their number
varies from species to species. Thus, in the regular urchins and sand dollars
the fully formed larva has four pairs of arms, while the larva of heart urchins
has six pairs. Moreover, in heart urchins the presence of an unpaired posterior
rod is characteristic; equipped with complex perforations, it is termed the
aboral rod.

Rods passing in direct proximity to the mouth of the larva from the dorsal
side are termed the preoral rods. They are simple in all species of sea urchins.
The rods situated behind the esophagus on the ventral side are called postoral,
while those lying behind the preoral ones are known as the anterolateral. The
anterolateral rods are always simple but the postoral ones are often complex,
triradiate, and with numerous perforations. The structure of the postoral rods
is of taxonomic significance.

The next pair of rods, the posterodorsal, is also rather frequently complex
in structure; these rods are situated on the dorsal side and basally adjoin the
base of the postoral rods. The structure of this pair of rods is likewise of
taxanomic significance.

In heart urchins, in front of the preoral rods on the dorsal side, one more
pair of rods develops. These rods are the anterodorsal pair and, like the
preoral rods, they are simple in structure. Further, in some species of heart
urchins yet another pair of rods, the posterolateral, may form, which diverge
from the upper ends of the archlike rod.

The basal and secondary basal rods in the larvae of some groups of sea
urchins are fused, and form in the basal part of the larva the so-called “basket
structure”.

In many species of sea urchins the pluteus III stage has one or several
pedicellariae, also of taxonomic importance.

1. In sea urchins the number of arms in the larvae is a diagnostic character.
In larvae of the order Spatangoida there are six pairs of arms in the
pluteus III stage, while in those of the orders Camarodonta and
Clypeasteroida there are four pairs.

2. Structure of the rods forming the skeleton: In species of the Superorder
Camerodonta, found in the Sea of Japan, all the skeletal rods are simple.
In species of the orders Clypeasteroida and Spatangoida both simple and
complex perforated rods occur.

3. Presence of pedicellariaes in larvae: These are characteristic of the larvae
of some species of the Superorder Camarodonta.

4. Presence of ciliated epaulettes or vibratile lobes: Ciliated epaulettes are
found in larvae of the Superorder Camarodonta while vibratile lobes are
found in larvae of the order Clypeasteroida.

5. Distribution and color of the pigment.

175

. Formation of fenestrated plates in the larvae of later stages. Such plates

are characteristic of larvae of the Superorder Camarodonta.

. Length of larva: Measured from the body base to the arm tip in a

perpendicular plane.

1 (6).
DOM

342):
4 (5).

5 (4).

6 (1).
7(18).
8(11).
9(10).
10 (9).
11 (8).
12(15).
13(14).
14(13).
15(12).
16(17).
17(16).

18 (7).

19 (24).

. Angle of bending of the dorsal arch.

Key to Species Based on Larvae in the Pluteus Stage

Aboral rodoresent: 2 2°, Syke leet i eee. CUS Loveniidae
Tv O, Pains Ofwarins: vay wep oee BA at RIE ke a etka! noe eligi
be CN Echinocardium cordatum, pluteus | stage (Figure 144).
More than two pairs of arms.
Three—four pairs of arms. Transverse rod present between the basal
rodssiabovesthe aboraltrodigaks: 2hiierh Se I.
. .... Echinocardium cordatum, pluteus II stage (Figure 145).
Five—six pairs of arms. Transverse rod absent between the basal
rodswabove ttheyaboralbrod: ws Aeiveicts Geos Be eee.
ee Echinocardium cordatum, pluteus III stage (Figure 146).
Aboral rod absent.
All skeletal rods simple.............. Strongylocentrotidae
Two pairs of arms.
Basal rods which processes at the distal end..............
SE ReRR Ores Strongylocentrotus nudus, pluteus I stage (Figure 129).
Basal rods clavate, one with a spine, the other with a depression.
. Strongylocentrotus intermedius, pluteus I stage (Figure 132).
More than two pairs of arms.
Three pairs of arms.
Secondary basal rods fused above the basal rods............
Oy pc aie Strongylocentrotus nudus, pluteus II stage (Figure 130).
Secondary basal rods are absent. Inner transverse rods present. . .
. Strongylocentrotus intermedius, pluteus II stage (Figure 138).
Four pairs of arms.
Three pedicellariae on the inner part of the arm rods; no fenestrated

Set oa Strongylocentrotus nudus, pluteus III stage (Figure 131).
Pedicellariae absent. Perforated plates on the inner part of the arm

.Strongylocentrotus intermedius, pluteus III stage (Figure 134).
Skeletal rodsisimplesandgcomplexés tanec (Se Ra erste). (an. 2
SR ERG ok ty ned nae Came Echinarachniidae and Dendrasteridae.
Two pairs of arms.

176

20(21). Basal and secondary basal rods form a basket. Single fenestrated
platexpresent understheiibaskets. 2 Qe. 2 ee ea
ar a a Echinarachinus parma, pluteus I stage (Figure 135).

21(20). Basket different in shape.

22(23). Basal and secondary basal rods fused in pairs, forming two plates
with numerous spines on the lower side............ .....
» ened isk Scaphechinus mirabilis, pluteus I stage (Figure 138).

23 (22). Distal ends of the basal and secondary basal rods thickened, bearing
numerous) spines; but not fused)... . 2029.90) (2 ee
ci eae acc Scaphechinus griseus, pluteus I stage (Figure 141).

24(19). Three-four pairs of arms.

25(26). Basket height three-fourths basal width. Angle of bending of the
dorsalvarchal80Sah) Saka) oe 2 RG OT SOa Se
.Scaphechinus mirabilis, pluteus II and III stages (Figures 139, 140).

26(25). Basket height greater than basal width. Angle of bending of the
dorsal arch 120°.

2728). Red pigment at. ends of arms) (8 80 Ve eee
Echinarachnius parma, pluteus II or III stage (Figures 136, 137).

28(27)., Larva light, green. -.6 2.20... 00 sens . Oe ee
. . Scaphechinus griseus, pluteus II or III stage (Figures 142, 143).

CHARACTERS OF LARVAE ACCORDING TO FAMILIES
Strongylocentrotidae

The larva has four pairs of arms. All the skeletal rods are simple. The basal
rods are clavate. In S. nudus and S. franciscanus the basal rods bear numerous
spines at their ends, which interlock the rods. Secondary basal rods are also
present but only in S. nudus and S. franciscanus. In the pluteus III stage the
ends of the basal rods are reduced and the base of the larval body is broad-
ened. Upper and lower epaulettes appear. In S. nudus and S. franciscanus
pedicellariae are present.

Three species of the genus Strongylocentrotus are found in Peter the
Great Bay: S. nudus, S. intermedius, and S. pulchellus. Descriptions of the
larvae are available for S. nudus (Kawamura, 1970; Kryuchkova, 1976), S.
intermedius (Kawamura, 1970; Krychkova, 1976), and S. pulchellus
(Kryuchkova, 1976).

Scutellidae, Dendrasteridae and Echinarachniidae

The larva has four pairs of arms. The rods of the postoral and posterodorsal
arms are fenestrated. The basal and secondary basal rods are fused, forming

177

a single fenestrated plate at the base of the larva. In Scaphechinus mirabilis
the single plate is not formed but the basal and secondary rods are fused in
pairs. In Scaphechinus griseus these rods are not fused, only contiguous.
Three species are found in Peter the Great Bay: Echinarachnius parma,
(Echinarachniidae), Scaphechinus mirabilis, and S. griseus, (Dendrasteridae).
Descriptions of the larvae are available for Echinarachnius parma (Fewkes,
1893; Kryuchkova, 1976), Scaphechinus mirabilis (Kryuchkova, 1976), and
Scaphechinus griseus (Kryuchkova, 1976).

Loveniidae

The larva has six pairs of arms and an aboral rod. The rods of the postoral
and posterodorsal arms as well as the aboral rod are fenestrated. In the pluteus
II stage the base of the aboral rod enlarges and assumes the shape of an
inverted arch with a long process in the middle. Fenestration in the aboral rod
commences from its base.

One sea urchin of this family is found in Peter the Great Bay, namely,
Echinocardium cordatum.

The larvae have been described by Selenka (1880), McBride (1914, 1918),
and Kryuchkova (1976).

STRONGYLOCENTROTUS NUDUS AGASSIZ
(Strongylocentrotidae)

Eggs of the mature female before they are shed in water are perfectly spheri-
cal, nontransparent, and grayish. Their size varies from 90 to 100 fm in
diameter. The fertilization membrane begins to separate 2—3 min after pen-
etration of a spermatozoon. The first division occurs 40 min later at a tem-
perature of 20—21°C. The free-swimming blastula develops after 32 hrs and
the pluteus I stage develops two days after fertilization.

Pluteus I stage

The larva is transparent, with a slightly bluish tinge. The endoskeleton is
visible through the tissue and is composed of simple rods. At this stage, the
larva has two pairs of arms: anterolateral and postoral. The body is supported
by thickened basal rods which, at the basal end, are somewhat flattened and
bear large spines that interlock the rods. Short inner transverse rods arise from
the site of fusion of the postoral and basal rods. Secondary basal rods are
attached to the inner transverse ones, they are shorter and do not fuse with
each other. The length of the larva at this stage is 200—400 um (Figure 129).

178

Pluteus II stage

From the time of appearance of the third pair of arms, the posterodorsal,
the larva enters the pluteus II stage. A calcification center arises on each side
at the base of the postoral arms and forms a single triradiate rod that later
transforms into a short rod. As it grows, a projection develops alongside the
postoral arm on the dorsal side of the larva. This projection is the posterodorsal
arm. Simultaneous with the development of the new pair of arms, the inner
transverse rods begin to interconnect. The secondary basal rods also begin to
enlarge but do not attain the full length of the basal rods; approximately
midlength of the latter they bend inward and cross. A short dorsal arch
arises on the dorsal side above the stomach. The basal part of the body
gradually enlarges and the spines at the distal ends of the basal rods break
off. This process becomes perceptible when the third pair of arms reaches the
size of the two earlier pairs and the larva is as long as 500—700 um (Figure
130).

Figure 130: Strongylocentrotus nudus.

Figure 129: Strongylocentrotus nudus. Pluteus II stage.
Pluteus I stage. ie da — dorsal arch.
Legend same as in Figure 103. Remaining legend same as in Figure 107.
Pluteus III stage

The ends of the basal arch elongate into a pair of new rods, which support
the processes appearing above the oral opening. These rods are termed the
preoral. With their appearance, formation of the larval skeleton terminates
and the larva enters the pluteus III stage. In the dorsal and ventral views, at
the level of the esophagus, dense ciliated bands of the ectoderm gradually

179

become discernible. The upper epaulettes appear. Slightly later, the lower
epaulettes appear, which are situated in the lower part of the larval body. At
this stage, three larval pedicellariae form, one between the lower epaulettes
and the other two on the dorsal and ventral sides of the larval body. By the
end of the pluteus III stage, the larva has accumulated crimson pigment,
which is initially evenly distributed over the entire body. This pigment gradu-
ally concentrates at the tips of the arms and in the region of formation of the
definitive test, which develops in the amniotic sac on the left side of the
larval body. The stomach becomes bright green. The length of the larva
reaches 900 um before metamorphosis (Figure 131).

Isp

Figure 131: Strongylocentrotus nudus.
Pluteus III stage.
as — amniotic sac; lep — lower epaulettes; p — pedicellariae; uep — upper epaulettes.

Ecology

The larvae of S. nudus appear in the plankton of Peter the Great Bay in
the middle ten days of July when the water temperature in the surface layer
is 18.5°C. The pluteus I stage is found up to August 20th. At August end, the
pluteus III stage can be seen undergoing metamorphosis. By mid-September,
the larvae of S. nudus have disappeared from the plankton, although in some
favorable years they are seen up to the end of September. According to Fuji
(1960a, b), spawning of S. nudus in southern Hokkaido is observed from mid-
August to mid-December.

180
STRONGYLOCENTROTUS INTERMEDIUS (AGASSIZ)
(Strongylocentrotidae)

The mature eggs of this species are smaller than those of S. nudus;
their diameter does not exceed 90 ttm. The eggs are nontransparent and
grayish. The fertilization membrane appears 5 min after penetration by the
spermatozoa. The first division occurs 45—50 min after fertilization at a
temperature of 20—21°C. The pluteus I stage develops two days later.

Pluteus I stage

The larval body is transparent, slightly bluish, with evenly scattered
granules of crimson pigment. The basal part of the body is highly elongate
and contains the basal rods whose ends are clavate. One of the rods terminates
with a small depression while the other bears a spine that fits into this
depression. Secondary basal rods are absent. The inner transverse rods are
very short. The rods supporting the anterolateral and postoral arms are two-
thirds of the length of basal rods. The larva at this stage is 250—400 um long
(Figure 132).

al’
da
d
po ‘
b
Figure 132: Strongylocentrotus intermedius. Figure 133: Strongylocentrotus intermedius.
Pluteus I stage. Pluteus II stage.
A — general view of the larva; B — basal rods. da — dorsal arch.

Legend same as in Figure 103. Remaining legend same as in Figure 107.

181

Pluteus II stage

Similar to S. nudus, the third posterodorsal pair of arms develop during
stage II in this species also. The dorsal arch becomes discernible and is much
narrower than in S. nudus. By the end of stage II, the clavate tips of the basal
rods break off but the position of the rods remains the same; hence the hind
end of the larva appears almost unaltered (Figure 133). On the 8th—9th day
of development, the ends of the basal arch elongate, giving rise to the preoral
rods. The pluteus II stage then becomes the pluteus stage III.

Pluteus III stage

The base of the larval body gradually enlarges and parts of the basal rods
contained therein gradually reduce. Ciliated epaulettes appear, which are
denser than in S. nudus and lie closer. The larva looks as if it has two
powerful ciliated bands. Pedicellariae do not form in S. intermedius. The
larval body is high set, resembling a truncated cone from which four pairs of
arms arise. All the skeletal rods are simple and armed with numerous short
spines. The larva soon loses its transparency, becoming bright red. This
change of color is due to the disappearance of the earlier scattered crimson
pigment granules, which are replaced by more numerous red granules. Now
the tips of the arms and the larval body are so filled with red granules that
the skeletal rods are no longer discernible. However, at higher microscopic
magnification, the reticular structures can be seen underneath the layer of
pigment on both sides of the stomach and at the base of the larval body. On
removal of the soft tissue, these structures are found to consist of lattice
plates, which have formed around the dorsal arch and left and right posterodorsal
and postoral rods. Another small plate is situated at the base of the larval
body. The fate of these plates was discussed above in the section on meta-
morphosis and formation of the definitive test. At the time of plate formation,
the length of the larva is 750—900 um (Figure 134).

Ecology

In Peter the Great Bay, larvae of the pluteus I stage begin to appear in
mid-July, when the water temperature in the surface layer is 16.5°C, and
continue to be found until early September with some interruptions. The first
juvenile individuals are found in early August. Large-scale settling is ob-
served in mid-August. In southern Hokkaido, according to Fuji (1960b), spawn-
ing of S. intermedius is observed from mid-August to late December. Accord-
ing to Kawamura and Taki (1965), who investigated the population of these
urchins near Rebun Island, spawning in this region occurs from early August
to mid-September.

182

Figure 134: Strongylocentrotus intermedius. Pluteus III stage.

b — basal rods.
Remaining legend same as in Figure 109.

ECHINARACHNIUS PARMA (LAMARCKk)
(Echinarachniidae)

Mature eggs of this sand dollar species are encased in an envelope densely
speckled with crimson pigment granules. The eggs are 130—140 um in di-
ameter and the membrane 60 tm thick. Development proceeds fairly rapidly.
The early pluteus stage is formed within 36 hrs after fertilization at a water
temperature of 20—21°C.

Pluteus I Stage

The larval body is short with a slightly tapering base. The body is
transparent, bluish, and devoid of pigment granules. Two pairs of arms de-
velop — the anterolateral and the postoral; the former is represented by simple
rods with short spines, while the latter contain complex perforations. From
the bases of these rods arise the inner transverse rods, which are connected
above the stomach and bear numerous small spines distally. The larval body
is supported by a pair of basal rods and a pair of secondary basal rods. All
these rods join in the basal part of the larval body; their distal ends are greatly
enlarged and form fenestrated plates, which are so tightly fused that traces of
their fusion are not visible in later stages. The secondary basal rods extend
to this plate and are likewise slightly enlarged at the site of connection. Such

183

a formation is known as a “basket”. It is completely formed in larvae 300—
400 um long. The width of the “basket” base is three-fourths of its height
(Figure 135). The length of the larvae is 250—300 um.

Pluteus II Stage

New arms, the posterodorsal, which also have a complex fenestrated
structure, appear as two small triradiate rods lying at the base of the postoral
arms. From the time of their appearance, the pluteus enters stage II. In this
stage the rudiment of the dorsal arch of about 120°C develops above the
stomach. From the posterodorsal rods, small secondary transverse rods are
directed inward. At this time, the first granules of crimson pigment begin to
appear at the tips of the arms. The length of the larva increases up to 500—
600 tum (Figure 136).

Pluteus III Stage

The preoral arms appear in stage III; their supporting rods are
simple because they are extensions of the dorsal arch. E. parma have
neither pedicellariae nor ciliated spaulettes. The epidermal vibratile plates
form between the posterodorsal and postoral arms. By the 7th—8th day of

Figure 135: Echinarachnius parma. Pluteus | stage.

A — general view of the larval skeleton; B — basket structure.
Legend same as in Figure 109.

184

development, the first signs of resorption of the larval skeleton becomes
evident. The basal plate in “the basket” disintegrates. The quantity of pigment
increases but only slightly. A fairly outstanding feature of the larva of this
stage is its change in color when placed in 70° alcohol. The red in the
pigment granules disappears and is replaced by green, which evenly colors
the entire larval body (Figure 137). The length of the larva is 700—800 um.

Ecology

Pluteus I stage begins to appear in the plankton of Peter the Great Bay
in early July, when the water temperature in the surface layer is 16.5°C.
Under conditions favorable for spawning, they may be found even in the
second ten-day period of June. The maximum density of pluteus I stage larvae
is observed in mid-July. The first individuals of settling juveniles are seen
after July 10.

According to Costello and coworkers (1957), spawning of E. parma along
the Atlantic coast of America (Woods Hole, Massachusetts) is observed from
late February to mid-August.

SCAPHECHINUS MIRABILIS (AGASSIZ)
(Dendrasteridae)

Mature eggs have a secondary envelope with inclusions of red pigment. The
eggs are 90—100 um in diameter and the envelope 40 um thick. Free-
swimming blastulae were found 13 hrs after fertilization in cultures at a
temperature of 20—21°C. Four hours later gastrulation was observed, and in
the 20th hr the first triradiate calcite spicules appeared in the gastrulae. The
early plutei developed 34 hrs after fertilization.

Pluteus I Stage

The larval body is transparent, shortened with a broad and flat base, and
slightly tapering. Two pairs of arms are present; anterolateral and postoral.
The structure of the rods supporting these arms is the same as in Echinarachnius
parma. The inner transverse rods join medially but unlike in E. parma do not
bear spines. The basal and secondary basal rods fuse in pairs. Each rod
thereby enlarges somewhat to form a small plate or lobe and basal and
secondary basal rods merge at the place of contact of these plates. Two large
plates develop at the base of the larval body, bearing numerous spines on the
lower margin and several small fenestrations. Thus, the “basket” in S. mirabilis
comprises two containing parts. The height of the “basket” base is three-
fourths its width. At this stage, the length of the larva is 200—400 um (Figure
138).

185

Figure 136: Echinarachnius parma.
Pluteus II stage. Structure of the larval skeleton.
Legend same as in Figure 107.

Figure 137: Echinarachnius parma.
Pluteus III stage.
da — dorsal arch. Remaining legend same as in Figure 109.

186

Figure 138: Scaphechinus mirabilis. Pluteus | stage.

A — structure of the larval skeleton; B — connection of the basal and secondary basal rods.
Remaining legend same as in Figure 103.

Pluteus II Stage

The third pair of arms, the posterodorsal, appears in this stage. The rods
of these arms are complexly fenestrated. The rudiment of the dorsal arch
becomes discernible; it is considerably broader than in Echinarachnius parma,
about 180°. In a live larva the accumulation of red pigment at the tips of the
arms is visible under a microscope. When the larva reaches a length of 500—
600 {1m, the transverse rods differentiate and extend from the posterodorsal
rods medially within the larva (Figure 139).

Pluteus III Stage

The preoral arms develop early in this stage; their supporting rods are
simple. As in Echinarachnius parma larvae, there are no ciliated epaulettes
and pedicellariae, but epidermal vibratile lobes are present. A gradual reduc-
tion of the plates forming the “basket” bottom takes place in the pluteus III
stage. Soon after their disintegration, resorption of the inner transverse rods
occurs. The amniotic sac becomes visible, arising, usually, on the 6th—7th
day of development. The larva by this time has reached a length of 800—900
um (Figure 140).

Ecology

Larvae of S. mirabilis appear in the plankton of Vostok Bay in late July
when the water temperature in the surface layer is 18°C. Maximum density
is observed in mid-August.

187

Figure 139: Scaphechinus mirabilis.
Pluteus II stage. Structure of the larval skeleton.
sint — secondary inner transverse rod; da — dorsal arch.
Remaining legend same as in Figure 107.

SCAPHECHINUS GRISEUS (MORTENSEN)
(Dendrasteridae)

The development of this and the preceding species has not yet been described
by other authors. Sometimes the older individuals of S. griseus are easily
confused with the juveniles of Echinarachnius parma because their size and
color are almost identical. The only distinguishing feature in such cases is the
position of the anal opening, which in S. griseus lies on the aboral side of the
test.

Mature eggs in S. griseus are 90—100 um in diameter but unlike in S.
mirabilis and E. parma, the secondary egg membrane is not visible. At a
temperature of 20—21°C, development proceeds at the same rate as in E.
parma. Thus, the blastula appears 16 hrs and the gastrula 24 hrs after fertili-
zation. The early pluteus develops 36 hrs after penetration of the egg by the
spermatozoa.

188

Figure 140: Scaphechinus mirabilis. Pluteus III Stage.
as — amniotic sac; Remaining legend same as in Figure 109.

Pluteus I Stage

The structure is identical in S. griseus to that of the pluteus of E. parma.
The basic difference in the pattern of the connection of the basal and second-
ary basal rods. In S. griseus these are not fused and the true “basket,”
characteristic of the larvae of sand dollars, is not formed. The ends of basal
rods have a similar thickening from which fairly long spines arise. These
spines are somewhat smaller in secondary basal rods. The rods interlock
through spines which fit into depressions formed by them on the opposite
pair. True fusion does not occur. The structure resulting from such an ar-
rangement may, at best, be termed a “pseudobasket”. The width of the
“nseudobasket” base is three-fourths of its height. The length of pluteus I does
not exceed 400 um (Figure 141).

Pluteus II Stage

The third pair of arms, the posterodorsal, appears in this stage. Like the
postoral, they have complex fenestrated rods. Simultaneous with them, the
dorsal arch develops which, as in Echinarachnius parma, is about 120°. The
larval body remains transparent, devoid of pigment granules. By the end of
stage II, the larva has increased in length up to 400 um (Figure 142).

189

Figure 141: Scaphechinus griseus. Pluteus | stage.
A — general view of the larva; B—— connection between the basal and secondary basal rods.
Remaining legend same as in Figure 103.

Figure 142: Scaphechinus griseus.
Pluteus II stage. Structure of the larval skeleton.
Legend same as in Figures 107 and 139.

Pluteus III Stage ;

The formation of the skeleton is completed and the fourth pair of arms,
the preoral, develops in this stage. Supporting rods inside these arms form
from elongated processes of the dorsal arch. As in the preceding species, there

190

are no ciliated epaulettes and pedicellariae in S. griseus, but the epidermal
vibratile lobes are far less developed. With the appearance of the amniotic sac
by the Sth—6th day of development, the basal and secondary basal rods elon-
gate distally and intertwine. Both pairs of inner transverse rods begin to
reduce. Few granules of red pigment appear at the arm tips. The larva reaches
a length of 900—1000 pm. Like the larvae of E. parma, the pluteus III stage
acquires a light green color when placed in 70° alcohol (Figure 143).

Ecology

Larvae of S. griseus begin to appear in the plankton of Vostok Bay in
September when the water temperature in the surface layer is 17°C. The first
settling urchins were obtained in the laboratory by mid-September.

Figure 143: Scaphechinus griseus. Pluteus III stage.
Legend same as in Figures 109 and 139.

ECHINOCARDIUM CORDATUM (PENNANT)
(Loveniidae)

Mature eggs vary in diameter from 90 to 100 um. The eggs are not pig-
mented. The blastula develops 28 hrs after fertilization and the gastrula after
42 hrs at a temperature of 20—21°C. The early pluteus, formed on the 3rd
day of culturing, exhibited a large number of granules of red pigment. The
bright color of the larvae of this heart urchin distinctly distinguishes them
from the larvae of other urchins that may occur concurrently in the plankton.

191

Pluteus I stage

In the early pluteus the postoral arms, which are complexly perforated,
are twice as long as the anterolateral arms represented by simple rods. The
aboral rod is present as a transverse rod with a pair of processes. Short basal
rods cross at the lower part of the larva. In shape, the larva initially resembles
a triangle but later, after the upper transverse rods appear, does not. These
rods fuse with each other and with the distal ends of the postoral rods. The
secondary basal rods diverge below from the base of the anterolateral rods.
These are likewise connected with each other by a short transverse rod formed
through the fusion of the lower transverse rods. These processes arise in the
secondary basal rods slightly above their distal ends. The secondary basal
rods are almost half as long as the basal and hence the basal part of the larval
body tapers slightly. Between each pair of these rods lies a transverse septum,
which forms above the lower inner transverse rods. The aboral rod basally
reaches the place of connection of the basal and secondary basal rods. On -
the 3rd—4th day of development, the aboral rod is equal in size to the
anterolateral arms. The length of pluteus I is twice that of the larvae of other
sea urchins, reaching 500—600 um (Figure 144).

Figure 144: Echinocardium cordatum. Pluteus | stage.
asp — aboral spicule.
Remaining legend same as in Figure 103.

192

Pluteus II stage

Five days after fertilization the third pair of arms, the posterodorsal,
appears. The rods supporting this pair of arms are complexly perforated.
Before the rudiments of the posterodorsal rods emerge, the connection be-
tween the basal and secondary basal rods disintegrates and the secondary
basal rods are reduced; however, the lower transverse septum is retained. The
developing posterodorsal rods bear two basal processes, the larger of which
fuses with the secondary basal rod while the smaller, hook-shaped, attaches
itself to the aterolateral rod. After emergence of the lower inner transverse
rods, diverging from the base of the secondary basal rods, the connection
between the basal and secondary basal rods totally disappears. By the time
of resorption of this connection, the smaller process of the posterodorsal rod
has straightened somewhat and runs parallel to the anterolateral rod. On the
side opposite to it, a new process begins to grow, which is directed below.
The dorsal arch appears at this time.

As soon as the posterodorsal arms attain the size of the postoral arms, the
ends of the dorsal arch begin to rapidly extend upward, giving rise to rods
for a new pair of arms, the preoral. Simultaneous with their development, the
lateral processes at the base of the aboral rod enlarge. The length of the
pluteus II stage is 900—1,000 tm (Figure 145).

Pluteus III stage

On the 7th—8th day of development, when the basal ends of the aboral
rod reach the base of the posterodorsal rods, a fifth pair of arms, the postero-
lateral, appear. The calcification centers of this pair appear from the outer
side somewhat below the lower inner transverse rods. The simple rods grow-
ing from these centers fuse with the basal ends of the aboral rod. The pos-
terolateral arms situated perpendicular to the anterolateral arms, together with
the aboral rod constitute a single structural unit which serves as a support for
the entire larval body. On the right, the arced rod connects the basal end of
the aboral rod with the posterodorsal rod. Probably the aboral rod develops
as a result of the enlargement of the lower lateral process of the posterodorsal
rod. A small perforated plate develops on the outer side of the postoral rod.
On the left side, likewise, a perforated plate appears on the postoral rod but
there is no connection with the aboral and posterodorsal rods. At this time,
on the lower side of the dorsal arch, a pair of processes appears on each side
of the esophagus. The upper processes remain short while the lower ones
grow rapidly. By the 10th—11th day, this lower pair has modified into rods
of the anterodorsal arms. The short processes of the basal arch serve as an
additional support for them from below. With the appearance of the sixth pair
of arms, formation of the larval skeleton is complete. The larvae of E.

193

i=

WW
(|)

a0 ;

Figure 145: Echinocardium cordatum. Pluteus II stage.
A - structure of the larval skeleton; B— connection of the anterolateral, posterodorsal and
postoral rods.
da — dorsal arch; asp —aboral spicule
Remaining legend same as in Figure 107.

cordatum have neither epaulettes, nor vibratile lobes, nor pedicellariae. The
bright red color of the larva is retained in all the stages of development. The
arms of a fully formed larva are very long and slender and the body is short.
The length of the pluteus III stage is 2 mm (Figure 146).

Ecology

Early larvae of E. cordatum usually appear in Vostok Bay in the last 10
days of June when the water temperature in the surface layer is 16.5°C. They
are found in maximum numbers in the last ten days of July, completely
disappearing from the plankton by July end. In favorable years, larvae of E.
cordatum are seen again in the middle ten days of September when the water
temperature in the surface layer drops to 17°C and stays at this level for two-
three weeks. Such a situation was observed, for instance, in 1970—1971.

According to the literature, reproduction of E. cordatum is observed off
the coast of Scotland from the end of May to mid-September (McBride,
1914), on the Isle of Man in the Irish Sea from June to early November

194

Figure 146: Echinocardium cordatum. Pluteus III stage.
asp —aboral spicule ; pda— process of the dorsal arch.
Remaining legend same as in Figure 109.

(Moore, 1936), in La Manche from mid-April to mid-August (Moore, 1936),
in Oresund (The Sound) from mid-July to early November (Thorson, 1946),
off the Swedish coast from mid-July to the end of October (Moore, 1966),
and in the Mediterranean Sea from mid-September to the end of December
(Moore, 1966).

CHAPTER IV

LARVAE OF BRITTLE STARS
(MORPHOLOGY, PHYSIOLOGY, AND
BEHAVIOR)

EARLY DEVELOPMENT

Information is available in the literature on the development of about 4% of
the known species of brittle stars. Of the approximately 2,000 species, 55 are
described as viviparous and nearly 30 as species with larval development; 48
species of larvae have been reported whose taxonomic position remains un-
clear. In brittle stars, three types of development are known: direct (viviparity
including brood care); development with planktotrophic larva; and develop-
ment with lecithotrophic larva.

Egg

According to Hendler (1975), there is no strict relationship between egg
size and type of development. Thus, in species with direct development the
egg diameter may range from 0.1 to 1.0 mm; a lecithotrophic larva develops
from an egg of 0.13—0.35 mm in diameter, and a planktotrophic larva from
an egg of 0.07—-0.9 mm in diameter. There is, however, a relationship between
the disk diameter of brittle stars, type of development, and number of eggs
produced by a single family. species with planktotrophic larvae produce the
largest number of eggs. For example, Ophiocoma echinata, in which the disk
diameter is roughly 25 mm, spawn up to 1,000,000 eggs, while in Ophionotus
hexactis, with a large diameter of nearly 40 mm, only 100 eggs mature by
the spawning period. Ophiocoma echinata develops with planktotrophic lar-
vae while in Ophionotus hexactis development is direct (Hendler, 1975). The
eggs of brittle stars are often reddish, yellowish, or yellowish-brown (Mortensen,
1937; Olsen, 1942).

196

Egg membrane : Oocytes are surrounded by a thick jellylike membrane,
which becomes loose (or disintegrates) after the oocytes are released into the
water (Lonning, 1976). As early as 1916, Kirk described a larva grown from
an egg with a dense chitinoid capsule. Unfortunately, the species affinity of
this larva was not determined since he had removed the eggs from the plank-
ton. In 1937, Mortensen described the secondary capsule, provided with spines,
for three species of the genus Ophiocoma: O. echinata, O. erinaceus, and O.
scolopendrina; he also noticed that the capsule obstructs emergence of the
embryo during hatching. In structure these capsules resemble the gemmules
of sponges or the chorion of eggs of some chitons.

Fertilization: The eggs in species with planktotrophic or lecithotrophic
larvae are shed in water through a slitlike opening in the bursa, where fer-
tilization occurs. One of the consequences of fertilization is the completion
of maturation division of the egg. Olson (1942) found two polar bodies in
Ophiopholis aculeata, which he above the blastomeres after the first division.
Hendler (1977), investigating the development of Amphioplus abditus, de-
scribed the formation of polar bodies that remained quite distinct during the
first three-four divisions.

During fertilization, the contents of the cortical granules of the eggs are
released into the space between the plasma membrane of the egg and its yolk
membrane, which transforms into a fertilization membrane and separates
from the surface of the egg. At this time, a hyaline layer appears that lines
the plasmatic membrane of the egg (Holland, 1979). This has been reported
for Ophiocoma nigra (Narasimhamurti, 1933), Gorgonocephalus caryi (Patent,
1970a), and Amphioplus abditus (Hendler, 1977).

Cleavage : Completely radial cleavage is observed in brittle stars. The
first two divisions occur in the meridional plane and the third in the equatorial
(Figure 147). The blastomeres in the animal hemisphere in Ophiocoma nigra
are somewhat smaller than those in the vegetal hemisphere (Narasimhamurti,
1933). Sometimes the blastomeres do not differ in size; the next division
gives rise to the blastula.

Blastula

Early development from fertilization to the blastula takes 24 hrs in
Ophiothrix fragilis (McBride, 1907), 21 hrs in Ophiopholis aculeata (Olsen,
1942), 6 hrs in Ophimaza cacaotica (Mortensen, 1937) and Ophiura sarsi and
2.5 hrs in Ophiothrix oerstedi (Mladenov, 1979). Mortensen (1937) noted that
in Ophiocoma lineolata the embryo hatches from the envelopes at the morula
stage. Formation of the blastocoel begins early in brittle stars. Narasimhamurti
(1933) noted that indications of the blastocoel appear in Ophiocoma nigra at
the 16-cell stage. In Ophiura sarsi an extensive primary cavity was noticed

197

Figure 147: Ophiura sarsi. Cleavage.

A — two blastomeres; B — four blastomeres; C — eight blastomeres.
View from the vegetal pole and laterally.

at the 32-blastomere stage. On the other hand, in Ophiocoma echinata (Grave,
1898) and Gorgonocephalus caryi (Patent, 1970a) blastomeres of small size
have been reported. The blastula does not emerge from the envelope with the
appearance of cilia, sometimes it remains immobile inside it for two hours.
Then the cilia begin to beat, initially slowly, but soon more and more rapidly.
The blastula turns around on its axis, the speed of rotation increases, the
envelope is ruptured, and the blastula begins to swim (Figure 148). Some-
times hatching does not occur. Patent (1970a) noted that in Gorgonocephalus
caryi the blastula does not leave the envelope and that it is devoid of cilia.

Figure 148: Ophiothrix fragilis (McBride, 1907).
Blastula.
M | —primary mesenchyme; M 2 — secondary mesenchyme.

198

sarsi the cilia are well developed but the fertilization membrane is not shed
even though the cilia emerges from it.

Gastrula

Formation of the gastrula takes from 9—12 hrs in Amphioplus abditus
(Hendler, 1977) and Ophiothrix oerstedi (Mladenov, 1979) to 40-48 hrs in
Ophiocoma nigra (Narasimhamurti, 1933). In Ophiura sarsi the gastrula
develops in one day.

In Ophiopholis aculeata (Olsen, 1942) and Ophiura sarsi the blastula
elongates before gastrulation along the animal-vegetal axis.

As soon as the vegetal pole of the blastula flattens, emigration of the
primary mesenchymal cells begins here (Figure 148). Then an invagination
appears, which forms the archenteron. Simulataneously, tapering of the ani-
mal pole region occurs where the so-called crest is formed; the latter consists
of vacuolated cells. Meanwhile the vegetal pole remains flat. At the same
time, the secondary mesenchymal cells begin to accumulate at the base of
the archenteron. Soon a bilobate coelomic sac develops from the archenteron,
which later divides into the right and left coeloms. The archenteron bends in
a ventral direction and touches the ectoderm to form an invagination in this
site. A rudiment of the esophagus is formed. After the ectoderm and the
bottom of the archenteron rupture, a gut is formed. The blastopore has now
become the anal opening.

Until the formation of the oral opening, a dense ridge formed from the
ciliated ectodermal cells is situated slightly above the blastopore. This ridge
girdles the entire gastrula. It delineates the future preoral field of the larva
(Figures 149, 150). Soon after the formation of the ciliated ridge, the crest,
in species where it is present, reduces. Under the ridge, along the edges of
the archenteron, in the accumulation of mesenchymal cells, spicules become
differentiated, from which the basal rods of the larval skeleton will develop
later. The embryo gradually acquires a triangular shape and changes over to
the prism stage.

Prism Stage

This stage is reached by the embryo after 16 hrs of development in
Amphioplus abditus (Hendler, 1977), after 48 hrs in Ophiopholis aculeata
(Olsen, 1942), and after 2 days in Ophiothrix fragilis (McBride, 1907). The
prism forms on the 4th day of development in Ophiocoma nigra
(Narasimhamurti, 1933) and in Ophiura sarsi.

At this stage, the embryo gradually acquires the shape typical of the
ophiopluteus. By this time, the blastopore has already shifted to the ventral
side, although division of the gut into sections has yet to occur. The larva is

199

Figure 149: Ophiothrix fragilis (McBride, 1907).
Gastrula.

A—commencement of gastrulation; B—formation of coelomic sacs
c—coelom; cr — ciliated ridge; cs — crest.

flattened dorsoventrally. The lateral margins of the ridge are stretched and
slightly upcurved. The ridge itself transforms into a ciliated band. Spicules,
already formed in the gastrula, are now modified into skeletal rods. Both
McBride (1907) in Ophiothrix fragilis and Olsen (1942) in Ophiopholis aculeata
have demonstrated the initiation of triradiate spicules in the gastrula stage,
which now give rise to three pairs of rods diverging from a common center.
A study of the development in Ophiura sarsi established the presence of
tetraradiate spicules. At the prism stage, only the upper and lower rays extend
into rods (Figure 151).

Hendler’s (1978) studies on the development of Amphioplus abditus showed
that after 24 hrs of development triradiate spicules formed in the embryo,
which after 5 hrs became tetraradiate. Examination of the structure of these
spicules under polarized light revealed differences in the crystal lattice of
individual spicular ends. Based on these results, Hendler concluded that the
first spicules du not have a single center of crystallization but are a complex
compound of different rods originating from different centers of crystalliza-
tion. Such a state is possibly associated with the peculiarities of disposition
of the spiculogenic cells.

200

Figure 150: Ophiopholis aculeata.

(Fewkes, 1893). Gastrula. General view.

bl — blastopore; cr—ciliated ridge;
cs — crest.

Pluteus I stage

Figure 151: Ophiura sarsi.
Prism stage. Optical section.
g— gut; sp —tetraradiate spicule.

Skeleton : In view of the fact that already at the prism stage there are in
some species rudiments of two pairs of arms, as in Ophiothrix fragilis (McBride,
1907), or three pairs of arms in others, as in Ophiura sarsi, and Olsen (1942)
describes a triradiate spicule in the prism stage and a tetraradiate spicule in
the early pluteus in Ophiopholis aculeata, the division of the developing
larvae into stages based on morphological characters is somewhat difficult. A
comparison of the morphological features of plutei of various species of
brittle stars based on the data of many authors (Fewkes, 1893; McBride, 1907;
Mortensen, 1921, 1931, 1937, 1938; Narasimhamurti, 1933; Olsen, 1942)

Figure 152: Ophiopholis aculeata
(Fewkes, 1893).
Early pluteus. General view.
al — anterolateral arms; pl — posterolateral
arms.

revealed that the first to develop are the
basal and wideset, long posterolateral rods.
The remaining arms, that is, the anterolateral
and postoral, develop somewhat later, de-
spite the fact that their rudiments are al-
ready present (Figure 152). The time inter-
val between the growth of processes giving
rise to the anterolateral and postoral rods:
may be quite substantial, from a few days
to a few weeks. Thus, Ophiura sarsi needs
one week to develop from the prism stage
to the complete formation of the postoral
rods, Ophiothrix fragilis requires three days
(McBride, 1907), and Ophiopholis aculeata
10 days (Olsen, 1942). Since already in the
early pluteus there are rudiments of the three

201

principal pairs of arms — posterolateral, anterolateral, and postoral (Figure
153)—the time of development of the postoral rods may be taken as the
termination of the formation of pluteus I stage.

Feeding : At this stage, until the complete development of the anterolateral
and posterolateral arms, the ciliated band passes along the margin of the
preoral depression. The ciliated band is involved in obtaining food for the
developing larvae only in species with planktotrophic larvae. According to
Strathmann (1971), a part of the ciliated band between the anterolateral arms
makes a loop above the preoral field towards the transverse section of the
band of postoral arms after their development. Beating of the cilia produces-
a water current over the mouth opening and extends beyond the limits of the
preoral field. Beating of the cilia of the posterolateral arms intensifies this
current. As in the larvae of sea stars and sea urchins, the ciliated band in the
ophiopluteus functions as a sieve which filters the food particles from the
plankton (Figure 154). The lateral bands are made up of a single layer of
cells. Studies conducted by Strathmann (1971) showed that in brittle stars
each cell of the ciliated band bears one cilium. The ciliated bands on the arms
are three to five cells wide; at some places the number of cells increases and,
as a result, the band becomes broader. The preoral and aboral fields bear few
cilia. Secretory cells have been detected in the tips of the arms of ophioplutei
but, as in echinoplutei, these cells are few in number. Very likely, the

Figure 153: Pluteus bimaculeatus (Metchnikoff, 1869).
Pluteus I stage. General view.

al — anterolateral arms; b — basal rods; pl — posterolateral arms; po — postoral arms.

202

Figure 154: Ophiothrix fragilis (McBride, 1907).
General view of pluteus | stage.

al — anterolateral arms; pl— posterolateral arms; po— postoral arms; talb — transverse
anterolateral band; tpob — transverse postoral band.

secretion produced by them helps to trap and to move food particles along the
band. The food which reaches the oral opening is transported to the esophagus
by means of the cilia in the oral cavity. All sections of the gut are provided
with cilia. When the food enters the esophagus, it is transported up to the
cardiac sphincter. As the latter opens, which is accompanied by a contraction
of the esophageal muscles, the food clump passes into the stomach. Here the
food is sorted. Strathmann (1971) demonstrated that when ophioplutei were
fed a mixture of algae and carmine particles, the latter were soon discarded
by the larvae, while the algae remained in the stomach for a long time. The
rate of passage of food particles through the gut may be regulated by the
speed with which the particles circulate in the upper part of the stomach and
gather near the pyloric sphincter, from where they enter the small intestine
and, upon contraction of the gastric muscles, are egested.

Brittle star larvae filter from the plankton microalgae that do not exceed
65 {1m in diameter and 150 um in length. These algae comprise various
species of Amphidinium, Cricosphaera, Phaeodactylum, Dunaliella and
others. The rate of filtration of food particles from the plankton varies from
1.8 to 3.0 ml/min.

In addition to sorting food in the stomach, brittle star larvae, like other
echinoderms, can eject too large algae from the oral cavity or esophagus. For
expulsion of such objects from the esophagus, the oral opening is enlarged,
the direction of beating of the adoral band cilia changes, and the esophageal
muscles contract. Enlargement of the oral opening by raising the preoral band

203

takes place through contraction of the muscles — dilatators — of the mouth,
which extend from the ends of the preoral transverse band to the anterolateral
arms. These muscles are able to contract together or individually. Expulsion
of algae from the oral cavity is effected only by raising the preoral band
through contraction of these muscles as well as contraction of the muscles of
the dorsal wall of the oral cavity, without involvement of the esophageal
muscles (Strathmann, 1971).

Respiration, transport of metabolites, and excretion: In brittle star larvae
there are no special organs of respiration and excretion. The hemal system is
also absent. Transport of nutrients is, possibly, done by the fluid of the
primary and secondary body cavities.

At this stage, the coelomic sac is still not connected with the surrounding
medium. The primary coelom is elongated and the two parts connected by a
narrow canal are readily discernible. The left coelomic sac is divided into
two: the upper — axocoel and hydrocoel, and the lower — somatocoel (Fig-
ure 155). Such a division was observed by McBride (1907) in Ophiothrix
fragilis and by Grave (1898) in Ophiocoma echinata. Olsen (1942) found that
in Ophiopholis aculeata the axocoel is the first to separate from the primary
coelom.

eA pl
ancl
Figure 155: Ophiothrix fragilis (McBride, 1907).
Separation of the somatocoel from the anterior section of the coelom.
ancl — left anterior coelom; ancr — right anterior coelom; ls — left somatocoel; rs — right

somatocoel.
Remaining legend same as in Figure 154.

204

Locomotion : The locomotory function, as in the larvae of other echino-
derms, is performed by the ciliated band. The posterolateral arms attain
maximum development in all planktotrophic larvae. During larval movement,
the wave created by beating of the cilia passes along the band (Strathmann
et al., 1972).

Water currents along the outer edge of the arms are directed toward the
narrowed basal part of the larva, pushing it forward. The brittle star larva does
not have great maneuverability since the bands of the anterolateral and postoral
arms participate basically in feeding. Moreover, in many brittle stars these are
much shorter than the posterolateral ones. Nevertheless, by changing direction
of beating of the cilia, the brittle star larva is capable of halting and turning.
A change in the direction of beating of the cilia along the greater part of the
ciliated band can produce a reverse movement of the larva. Swimming on the
bottom of the dish in which they were reared, the larvae were capable of
performing jerky movements with their oral opening down; the arms of brittle
star larvae are rigidly fixed.

Nervous system and sensory organs: Mortensen (1937), describing the
various larval stages of Ophiocoma lineolata, mentioned that nervous ele-
ments are present in different parts of the larval body. Unfortunately, he
provided no description of these structures. Other information on the larval
nervous system in brittle stars is lacking in the literature.

Pluteus II stage

Skeleton : Fully developed larvae of brittle stars have four pairs of arms.
The last pair, the posterodorsal, appears after the anterolateral arms on the
ventral side. The rays supporting them are processes of the anterolateral rods.
The basal rods distally bear one or two pairs of transverse processes of
varying lengths. In larvae of the genus Ophiocoma, these transverse processes
are absent and the basal rods interlock (Figures 156, 157).

Feeding : McBride (1907) noted in the larva of this stage that the oral
opening is bordered by the adoral ciliated band (Figure 158), in addition to
the preoral band and lateral band, connecting the transverse areas of the
anterolateral and postoral bands.

Respiration, transport of metabolites, and excretion: At this stage, the
coelomic structures are more complex. The left anterior coelom is connected
through the pore canal with the external environment and possibly partici-
pates in the excretion of products of metabolism. Studies on the development
of Ophiothrix fragilis (McBride, 1907) and Ophiocoma nigra (Narasimhamutti,
1933) showed that soon after the formation of the pore canal, separation of

205

Figure 156: Ophiothrix savignyi (Mortensen, 1938).
General view of the larva.
b — basal rods; pd — posterodorsal arms; tpb — transverse processes of the basal rods.
Remaining legend same as in Figure 154.

Figure 157: Ophiocoma scolopendrina (Mortensen, 1937).
General view of the skeleton. Note the absence of processes on the basal rods.

the hydrocoels begins. The left as well as the right hydrocoel remain con-
nected with the axocoel through small canals (Figure 159). The canal on the
left side of the larva later transforms into the stone canal.

Locomotion : With the appearance of the fourth pair of arms, the ciliated
band enlarges but the pattern of larval movements does not change. Strathmann
(1971) determined that the speed of horizontal movement of the larvae
is roughly 0.5 mm/sec and the length of the cilia in the band 25-30 um. At
this stage, in some species vibratile lobes bordered with cilia develop between
the posterolateral, postoral, and posterodorsal arms (Figure 160). Their

206

ie

LWW

Figure 158: Ophiothrix fragilis (McBride, 1907).
Longitudinal section of the pluteus II stage.
adb — adoral band; alb — anterolateral band; asph — anal sphincter; csph — cardiac sphincter;
e — esophagus; hg—hind gut; oc —oral cavity; pob— postoral band; psph
pyloric sphincter; s — stomach.

appearan°e is associated with the commencement of metamorphosis, when
growth of the juvenile begins, and the larva becomes heavier.

Nervous system and sense organs: In larvae of many species of brittle
stars an accumulation of pigment granules is seen at the tips of the arms and
in the body alongside the stomach. The pigmentation may be reddish, yellow-
ish, or greenish. It may be suggested that the cells containing the pigment
granules perform the function of photoreceptors, analogous to what has been
described by Ryberg and Lundgren (1979) in sea urchins.

Among the rudiments of the definitive organs in the ophiopluteus II stage,

we can mention the processes of the hydrocoel and the first spicules of the
definitive skeleton.

METAMORPHOSIS

In brittle stars metamorphosis occurs in free-swimming plutei. The de-
finitive brittle star develops on the ventral side of the larva and the fully

207

4 \
rend
eafen k
a)

Figure 159: Ophiothrix fragilis (McBride, 1907).
Separation of hydro- and axocoel. Formation of primary evaginations of hydrocoel.
axc —axocoel; hc — hydrocoel.

Figure 160: Ophiocoma scolopendrina (Mortensen, 1937).
Formation of vibratile lobes.
vl — vibratile lobes.

208

formed individual settles on the bottom. As in the sea stars and sea urchins,
metamorphosis in the brittle stars is catastrophic. The larval organs and.
tissues degenerate and are reorganized. The posterolateral arms supporting the
juvenile in the plankton remain longer than the other arms. In some species,
after the brittle star settles on the bottom, these arms with their fringe of
ciliated band swim independently in water for some time, similar to the
preoral lobe of bipinnariae of astropectinids and luidiids after the conclusion
of metamorphosis.

Skeleton : No amniotic sac forms in brittle stars and the commencement
of metamorphosis can be considered coincident with the appearance of pro-
cesses in the hydrocoel. However, the first spicules, from which the elements
of the definitive skeleton will develop, appear somewhat earlier than the
hydrocoelic processes. They are situated on either side of the stomach, with
five spicules on each side (Figure 161). With further development, they give
rise to five radial and five terminal plates. The central plate of the aboral side
appears somewhat later. Next come the rudiments of the proximal oral plates

Figure 161: Ophiothrix fragilis (McBride, 1907).
Arrangement of different parts of the coelom at commencement of metamorphosis in brittle
stars.

A — before turning and reduction; B — after turning and reduction of larval arms;
axcl — left axocoel; axcr —right axocoel; hcl —left hydrocoel; her — right hydrocoel;
mp — madreporic pore; scl —left somatocoel; scr — right somatocoel.

209
or ambulacralia. After this the paired distal oral plates develop (Figures 162,
163, 164). Soon after settling, rudiments of the dental plates appear between
the proximal oral plates. Development of the definitive skeleton of brittle
stars was studied by Fewkes (1887), Mortensen (1921, 1937, 1938), and
Hendler (1978).

Simultaneous with the development of the juvenile organism, reduction
of the larval arms starts with disappearance of the anterolateral and postero-
dorsal arms. The posterolateral arms are retained the longest. None of the
fragments of the larval skeleton take part in the formation of the elements of
the definitive skeleton.

Digestive system: Like other areas of the larval epithelium, the ciliated
band is dedifferentiated and partially resorbed. The definitive epithelium is
formed from the larval epithelium (Chia and Burke, 1978).

Brittle star larvae do not feed during metamorphosis since the small
intestine of the larva is destroyed and resorbed: the esophagus and stomach

Figure 162: Ophiura sarsi.
General view of the larva during metamorphosis.

al — anterolateral arms; hcp—hydrocoel process; pd— posterodorsal arms;
p! — posterolateral arms; po— postoral arms; sp — spicules, forerunners of the definitive
skeleton.

210

Figure 163: Ophiura sarsi.
Arrangement of plates on the aboral side of the juvenile.

Figure 164: Ophiura sarsi.
Arrangement of plates on the oral side of the juvenile.

211

are reorganized, acquiring the shape of a homogeneous cellular mass in
which, at a later stage, lumens appear and the epithelial structure is restored.
At this time, formation of the oral disk proceeds on the ventral side concomi-
tant with ectodermal thickening. The oral opening lies in the center of this
disk and is covered by the peristomial membrane. The peristomial membrane
delimits the peristomial cavity in which the dental apparatus develops after
the larva has settled. Brittle stars lack an anal opening (McBride, 1907;
Narasimhamurti, 1933; Olsen, 1942).

Respiration: The respiratory functions are passed on from the larval
epithelium to the definitive epithelium, including the epithelium covering the
ambulacral podia. The transport functions are transferred to the hemal and
perihemal systems and the visceral coelom. Spheroid bodies with phagocytes
and, possibly the axial organ, take part in excretion processes. Considerable
modifications of the coeloms lead to the formation of an ambulacral system,
hemal and perihemal systems, and perivisceral coelom of the definitive indi-
vidual.

Locomotion : During metamorphosis, the locomotor functions are passed
on from the ciliated band to the first terminal and first ambulacral podia; in
lecithotrophic larvae of Ophiura brevispina and Ophiolepis elegans the two
locomotor systems function simulataneously (Strathmann, 1978). Later, the
ambulacral system loses its leading role in locomotion in brittle stars and the
mobile arms of the definitive brittle stars act as the principal locomotor
organs.

Nervous system: The epineural radial and ring canals form under the
lateral processes of the hydrocoel and ring canal of the ambulacral system.
The ectoneural system passes in the canals of the epineural system. The
hyponeural system develops in the walls of the perihemal canals (McBride,
1907; Olsen, 1942).

Reproductive system : The primary gonads appear in the walls of the left
somatocoel adjacent to the stone canal and begin to form the gonadial strand
after the juvenile individual settles (Figure 165).

Settling : Development of the juvenile individual proceeds during the
planktonic larval period. Completely formed individuals settle on the sub-
strate. No attachment organs are present in brittle stars. There is no reliable
information on ability to search the substrate before settling (Strathmann,
1978). The juvenile brittle stars, on settling, attach themselves to the substrate
by primary ambulacral podia. Usually, by this time, nearly all the larval arms
are fully resorbed. However, McBride (1907) noted that in Ophiothrix fragilis
the posterolateral arms are shed after the juveniles settle on the bottom. Thus,

212

Figure 165: Ophiothrix fragilis (McBride, 1907).
Transverse section. Appearance of primary gonads.

axcl — left axocoel; mp — madreporic pore; pg — primary gonads; phc — perihemal canal;
stc — stone canal.

young brittle stars are capable not only of creeping on the substrate, but also
swimming over the bottom as well, for which they use the remains of the
ciliated band.

LECITHOTROPHIC LARVAE

Some brittle star species have lecithotrophic larvae, which are similar to
planktotrophic larvae; these are, for example, Amphiura filiformis ( Mortensen,
1931), Amphiura chiajei (Fenaux, 1963), and Ophiothrix oerstedi (Mladenov,
1979). Other species have larvae of the doliolaria type; these are Ophioderma
brevispine (Grave, 1916), Ophiolepis cincta (Mortensen, 1938), Ophioderma
longicauda (Fenaux, 1969), and Ophiolepis elegans (Stancyk, 1973). Devel-
opment of the third group of species is close to direct; these include
Gorgonocephalus caryi (Patent, 1970a) and Amphioplus abditus (Hendler,
1977). The development of the latter group of species is interesting in that
the egg membrane persists until the young brittle star hatches, although until
the prism stage it does not differ in development from planktotrophic larvae,
and rudiments of the larval skeleton remain up to much later stages (Figure
166). Thus, this type of development resembles the development of gastro-
pods in clutches or capsules.

Generally, in any type of development with a lecithotrophic larva, cleav-
age and formation of the blastula proceed in the same manner as in the case
of a planktotrophic larva. If in the process of development the larval skeleton
is formed, then it, too, develops as in a planktotrophic larva (Figure 167).
Amphiura chiajei (Fenaux, 1963) and Ophiothrix oerstedi (Mladenov, 1979)
develop only the posterolateral arms.

21S

Figure 166: Amphioplus abditus (Hendler, 1977).
Three stages of development of brittle stars within the envelope.

A — prism stage; B —first separation of the rudiments of the juvenile; C — formation of
rudiments of the ambulacral podia and mouth.

In the case of a larva of the doliolaria type development up to the gastrula
does not differ from development of a planktotrophic larva. The blastopore
closes early in the gastrula. The preoral lobe develops at the anterior end and
the oral opening itself is shifted to the posterior end.

Separation of the left hydrocoel, forming five rudiments of the various
canals of the ambulacral system (Figure 168), begins before the formation of
ciliated bands. Then, in the place of a uniform ciliary cover, four transverse
ciliated bands are formed, as in doliolariae of sea cucumbers. One of the bands
passes at the level of the oral opening, near which it becomes discontinuous
(Figure 169). At this stage, in some brittle stars, rudiments of the larval skeleton
become visible (in Ophiolepis cincta— Mortensen, 1938). Then the posterior
part of the larva gradually acquires a pentagonal shape and the larva descends
to the bottom where metamorphosis is completed (Figure 170).

With reference to the settling of doliolaria-type larvae, Stancyk (1973)

214

Figure 167: Ophiothrix oerstedi (Mladenov, 1977**).
Formation of the larval skeleton in the lecithotrophic larva.

al — anterolateral arms; pl — posterolateral arms.

noted that larvae of Ophiolepis elegans were able to swim as well as creep
for some time before they actually settled down.

In addition to development with planktotrophic and lecithotrophic larvae,
viviparity has been confirmed for many species of brittle stars. A majority of
these species live in polar regions or at great depths. Among them, some
species occur only in specific regions, for example, Stegophiura vivipara
(Matsumoto, 1915) off the coast of Japan. On the other hand, there are
cosmopolitan species, such as Amphipholis squamata, found almost univer-
sally in temperate latitudes. Wide distribution has also been reported for some
deepwater species, such as Ophiomusium lymani (Tyler, 1980) reported for
the Atlantic as well as the Pacific Ocean.

Figure 168: Ophioderma longicauda Figure 169: Ophiolepis elegans (Stancyk, 1973).
(Fenaux, 1969). Formation of the transverse ciliated bands in the
Formation of hydrocoel processes. doliolaria-type larva.
arch —- archenteron; bl — blastopore; amp —rudiment of ambulacral podia; cb (1, 2,
hcp — hydrocoel processes. 3, 4) —transverse ciliated bands; oo— oral

opening; pol — preoral lobe.

215

Figure 170: Ophiolepis cincta (Mortensen, 1938).
Arrangement of primary plates of the definitive skeleton.

A — oral side of the juvenile; B —aboral side of the juvenile.

Ophiuroidea is the only class of echinoderms in which dwarf males are
found. It is not clear if all brittle stars with dwarf males (four species are
known to date) have brood care as in bivalves (see Chapter 1); however, in
Astrochlamys bruneus, in which dwarf males perch on the aboral surface of
the females, viviparity has been observed.

In viviparous brittle stars the development of the young occurs in the
female bursae. The number of embryos is small, usually one or two. How-
ever, the number of developing embryos is sometimes fairly large. Murakami
(1941) —cited after Hendler, 1975 found up to 70 individuals in
Stegophiura sculpta and Mortensen (1936) up to 200 individuals in
Astrochlamys bruneus in each bursa.

Does viviparity actually occur in brittle stars? Or do we observe only
brood care in brood chambers, as in sea urchins and sea cucumbers? For many
species, this problem has yet to be solved. Only one comprehensive work is
available on the development of Amphipholis squamata (Fell, 1946), in which
viviparity has been confirmed. Fell demonstrated that the developing embryos
were attached to the horn of the bursa and not to the ovary. After differen-
tiation of layers in the embryo, the latter was surrounded by the wall of the
horn. At the site of attachment of the embryo to the horn of the bursa, the
parental and embryonal tissues fused. Later, the stalk on which the develop-
ing embryos are suspended in the bursal cavity appeared at this site. In his
earlier works, Fell proposed that feeding of the embryos is accomplished
through this stalk. In a later work, (Fell, 1946), he suggested that this stalk
is used only for attachment.

216

Experiments on embryos reared in vitro showed that for their normal
development additional substances are required. Observing the morphological
changes in the bursal wall in the last stages of development of embryos, Fell
concluded that nutrients are produced by the wall itself and feeding of the
embryo occurs by absorption through the entire surface of the embryo.

Another case of true viviparity has been described by Mortensen (1921)
in the Antarctic brittle star Ophionotus hexactis. In this species only one egg
matures in the ovary; development of the juvenile is also introovarian, evi-
dently due to feeding nutritive and visceral fluid (Turner and Dearborn,
1979). After emergence of the young brittle star, a new ovary develops.

Hyman (1955), based on data on the reproduction of brittle stars, con-
cluded that in the viviparous species the spawning period is more protracted
than in the species with lecithotrophic and planktotrophic development. A list
of species and their mode of development is given in Table 6.

IDENTIFICATION OF PELAGIC LARVAE OF
BRITTLE STARS
(Terminology and Diagnostic Characters)

Brittle star larvae have an endoskeleton composed of rods that support the
arms and basal part of the body, which is flattened dorsoventrally. The arms
are listed in the order of their appearance. In the early stages of plutei the
posterolateral and anterolateral arms develop on the ventral side and later the
postoral arms develop on the dorsal side. Generally, the rods supporting the
arms are simple, but in some species the rods of the posterolateral arms may
be fenestrated. The basal rods passing in the body of the larva may be distally.
bifurcate and sometimes the ends are interlocked. In many species one or two
pairs of transverse processes develop in the lower third of the basal rods.
Another pair of arms, the posterodorsal, appears at a later stage; these arms
develop behind the anterolateral arms on the ventral side. Their supporting
rods appear as processes of the anterolateral rods. Between the basic arms,
except the anterolateral, vibratile lobes may develop. Pigment granules ap-
pear under the ciliated band at the tips of the arms and in the region of the
stomach. Pigmentation varies in different species.

The following diagnostic characters are useful for identification of brittle
star larvae.

1. Number of arms. Three pairs in the first stage and four pairs in the second
stage.

2. Structure of rods of the larval skeleton. In larvae of the family amphiuridae
all skeletal rods are simple.

Zl

Table 6: Types of development in brittle stars

Species Type of Author
development
Order Ophiurida

Ophiomyxa serpentaria Lecithotrophic Tyler, 1980
larva

Ophiomyxa_ brevirima Viviparity Hendler, 1975

Ophiomyxa vivipara Same Same

Ophioscolex nutrix Same Same

Ophiacantha normani Same Tyler, 1980

Ophiacantha anomala Same Same

Ophiacantha bidentata Same Same

Ophiacantha dansispina Same Hendler, 1975

Ophiacantha vivipara Same Same

Ophiomitrella clavigera Same Same

Ophiomitrella ingrata Same Same

Ophiolebella biscutifera Same Same

Amphiura chiajei Planktotrophic Fenaux, 1963
larva

Amphiura _filiformis Same Mortensen, 1920

Amphiura annulifera Viviparity Mortensen, 1931

Amphiura stepanovii Same Same

Amphiura belgicae Same Hendler, 1975

Amphiura monorima Same Same

Amphiura stimpsoni Same Same

Amphiura capensis Same Same

Amphiura magellanica Same Same

Amphiura microplax Same Same

Amphioplus abditus Lecithotrophic Hendler, 1977
larva

Amphipholis squamata Viviparity Russo, 1891; Fell,

1946; Hendler, 1975

Amphipholis torelli Same Hendler, 1975

Axiognathus japonica Same Same

Ophiopholis aculeata Planktotrophic Olsen, 1942
larva

Ophiactis balli Same Mortensen, 1913

Ophiactis savignyi Planktotrophic Mortensen, 1931
larva

Amphilepis ingolfiana Lecithotrophic Tyler, 1980
larva

Ophiothrix angulata Planktotrophic Mortensen, 1921
larva

Ophiothrix fragilis Same McBride, 1907

Ophiothrix quinquemaculata Same Hendler, 1975

Ophiothrix savignyi Same Mortensen, 1938

Ophiothrix triloba Same Mortensen, 1937

(Contd.)

218

(Table 6 contd.)

—————_ A

Species

Type of
development

Author

—_—_—_——_——.::?”.__X_X_”_X”™”™”™”_™_00™_0_ _—

Ophiomaza cacaotica
Ophionereis squamulosa

Ophionereis vivipara
Ophiocoma echinata

Ophiocoma erinaceus
Ophiocoma pica
Ophiocoma pumila

Ophiocoma scolopendrina
Ophiocomina nigra
Ophioderma brevispina

Ophioderma longicaudum
Ophioconis vivipara
Pectinura cylindrica
Pectinura gracilis
Ophiura ljungmani

Ophiura texturata
Ophiura sarsi
Ophiura albida
Ophiura robusta
Ophiura affinis

Ophiura meridionalis
Ophiura ronchi
Ophiura loveni
Homalophiura tesselata

Stegophiura vivipara
Stegophiura sculpta
Amphiophiura rowetti
Amphiophiura pachylax
Amphiophiura bullata
Ophiolepis cincta

Ophiolepis elegans
Ophiocten sericeum

Ophiomusium lymani

Ophyophycis gracilis
Ophiozonella falklandica

Same
Lecithotrophic
larva
Viviparity
Planktotrophic
larva
Same
Same
Planktotrophic
larva
Same
Same
Lecithotrophic
larva
Same
Viviparity
Same
Same
Planktotrophic
larva
Same
Same
Same
Same
Lecithotrophic
larva
Viviparity
Same
Same
Lecithotrophic
larva
Viviparity
Same
Same
Same
Same
Lecithotrophic
larva
Same
Planktotrophic
larva
Lecithotrophic
larva
Viviparity
Same

Mortensen, 1937
Mortensen, 1921

Hendler, 1975
Grave, 1898

Mortensen, 1937
Same
Hendler, 1975

Mortensen, 1937
Narasimhamurti, 1933
Hendler, 1975

Fenaux, 1969
Mortensen, 1931
Same

Same

Same

Same

Our data
Mortensen, 1931
Thorson, 1946
Hendler, 1975

Hendler, 1975
Same

Tyler, 1980
Same

Matsumoto, 1915
Hendler, 1975
Same

Tyler, 1980
Same
Mortensen, 1938

Stancyk, 1973
Tyler, 1980

Same

Hendler, 1975
Same

(Contd.)

(Table 6 contd.)

219

Species Type of Author
development
Ophionotus hexactis Viviparity Hendler, 1975
Ophiopyren striatum Lecithotrophic Tyler, 1980
larva
Ophiopleura borealis Planktotrophic Same
larva
Ophioceres incipiens Viviparity Hendler, 1975
Ophiophrixus spinosus Same Tyler, 1980
Ophioplocus esmarki Same Hyman, 1955
Ophiotjalfa vivipara Same Hendler, 1975
Ophiurolepis gelida Same Same
Ophiurolepis martensi Same Same
Cryptopelta granulifera Same Mortensen, 1933

Astrotoma waitei
Astrochlamys bruneus
Gorgonocephalus caryi

Gorgonocephalus arcticus
Gorgonocephalus euchemis

Order Phrynophiurida

Viviparity Hendler, 1975
Same Same
Lecithotrophic Patent, 1970a
larva
Same Mortensen, 1931
Same Same

3. Joining of the basal rods of the skeleton.
4. Presence and number of transverse rods issuing from the basal rods.
5. Presence of vibratile lobes in the second stage larvae.
6. Presence and color of the pigment.
7. Length of the larva from body base to tips of arms, perpendicular.
8. Distance between tips of the posterolateral arms in the second-stage
larva.
Key to Species Based on Larvae at the Pluteus Stage
1 (2). Larva with one pair of arms.
2 (5). Larva with two-three pairs of arms.
3 (4). Basal rays smooth............ Amphipholis kochii, Stage I
AWG) ab asalerays With SPINES: ai... fee. ue Ophiura sarsi, Stage I
5 (2). Larva with two pairs of arms.
6 (9). Larva with three pairs of arms.
7 (8). Basal rays with three short terminal processes.............
Boe Suite cd tar aa aero a SAIL ee OI Amphipholis kochii, Stage II
Sa @)s Basalsrays without terminalprocesseS72.. 542 4540 2 es

220

9 (6). Larva with four pairs of arms.

10(11). All terminal processes on basal rays with many short spines. . . .
= ol oats be ie a. eal lasts (2 Oe en Amphipholis kochii, Stage II

11(10). Only two terminal processes of basal rays with spines........
Feehan ces ct ARR Nek Aha eR Ophiura sarsi, Stage II

FAMILY CHARACTERS OF LARVAL BRITTLE STARS
Ophiuridae

It is not possible to identify only one type of development as typical for the
brittle stars of this family. Planktotrophic and lecithotrophic larvae as well as
brood care have been observed here. In the planktotrophic type, larval devel-
opment is marked by very slender, elongate posterolateral arms; the rays
supporting them may be fenestrated in some species. A fully developed larva
has four pairs of arms. At later stages a bright green stomach becomes very
distinct. The pigment in the arms and body of the larva varies in color in
different species. Unlike larval sea urchins, there are no vibratile plates,
pedicellariae and ciliated epaulettes.

Ophiura sarsi Liitken and Ophiura sarsi vadicola Djakonov are found in
the Sea of Japan. The larvae have been described by Kryuchkova (1988).

Amphiuridae

Viviparity is characteristic of most of the studied species of this family.
During planktotrophic development of the larva the typical pluteus with four
pairs of arms develops. The transition to a larva with one pair of arms
occurred in the course of evolution of viviparity. The skeletal rods are simple
in all larvae. In larvae with four pairs of arms the body is compact and opaque
in the early stages; at later stages the body becomes almost transparent. In
larvae with a reduced number of arms the body continues to remain opaque
at all stages of development. At later stages, in species with a fully developed
larva an orange or red pigment appears along the rods supporting the arms
and at the end of the arms.

One species, Amphipholis kochii Liitken, is found in Peter the Great Bay.
The larva of this species has been described by Yamashita (1985) and
Kryuchkova (1988).

DDN
OPHIURA SARSI LUTKEN
(Ophiuridae)

Mature eggs are reddish, nontransparent, 100 {um in diameter. Under labora-
tory conditions the 8-cell stage is formed 1 hr after fertilization at a tempera-
ture of 16°C. After 6 hrs, the blastula can be seen; 2 hrs later the blastula
begins to swim but hatching from the membrane does not occur. Cilia pass
through the membrane adjoining the outer wall of the blastula. At this stage,
the blastula is spherical. After 21 hrs, the blastula changes, elongating along
the animal-vegetal axis; the animal pole is slightly tapered and the vegetal
pole flattened. The gastrula with a well-developed archenteron is formed
after 45 hours. An accumulation of primary mesenchymal cells is observed
around the base of the archenteron. In shape the gastrula resembles an isos-
celes triangle whose base is situated at the vegetal pole. The next day,
tetraradiate calcite spicules — rudiments of the larval skeleton — are discern-
ible among the cells of the primary mesenchyme. The length of the embryo
at this stage is 150 um. Along the perioral depression a ciliated band is
formed; all other cilia, except in the basal part of the body, disappear. Pluteus
I stage is fully formed on the 6th day.

Pluteus I Stage

At the point of divergence of the basal rods, the larval body has a distinct
girdle. All the skeletal rods are simple and provided with fine spinules. The
posterolateral arms are the first to differentiate, followed by the anterolateral
arms. The preoral arms remain for some time in a rudimentary state. As the ©
pluteus grows, the structure of the basal rods becomes more and more com-
plex. Large spines, two on each rod, arise on their distal ends, they contact
to form a ring. The ends of the basal rods, initially pointed, now become
thickened and flattened. The yolk membrane, yolk granules, and cilia disap-
pear at the basal end of the pluteus. By the time rudiments of the fourth pair
of arms appear, the pluteus has reached 450 um in length; 550 [tm between
tips of the posterolateral arms (Figure 171).

Pluteus II Stage

Plutei of this stage are distinguished by the yellow color of the stomach.
The fourth pair of rods, the posterodorsal, forms as processes of the anterolateral
rods, which are found in their lower third (Figure 171). On full development,
these rods are slightly shorter than the postoral. As soon as the larva reaches
a length of 750 um and 1,250 um between the tips of the posterolateral arms,
the skeletal rods become yellowish-brown and the stomach becomes green.
The basal rods are distally form thick processes, by means of which the rods

222

po al pl al

po

pl
pd
b
D
A
E

Figure 171: Ophiura sarsi.

A — Pluteus | stage; general view of the larval skeleton; B — Pluteus II stage; beginning of
formation of the posterodorsal rods.
Legend same as in Figure 162.

are interconnected. At this stage, it is possible to distinguish spicules in the
larvae, which give rise to the first plates of the definitive skeleton (see Figure
182).

Ecology

Brittle stars of this species are ready for spawning in Vostok Bay in late
April when the water temperature is 4.9°C. Larvae of this species were found
in the plankton only one month later, in May, when the water temperature
was 11°C. Larvae completing metamorphosis were found in early July when
the water temperature was 15°C.

Mortensen (1898, 1931) described the larva of “Ophiopluteus compressus”
with characteristic perforated rods and purplish-black granules of the postero-
lateral and posterodorsal arms and proposed that it might belong to Ophiura
sarsi on the basis that the adult animals of this species are fairly numerous
in Danish waters and their reproduction period coincides with the appearance
of the larvae in the plankton. Thorson (1946), based on Mortensen’s data, also
proposed that Ophiopluteus compressus might possibly be the larva of O.
sarsi. These larvae are found in Oresund Strait (The Sound) in April at a
water temperature of 5.8°C. However, Thorson does not describe the larvae
obtained by him while rearing O. sarsi.

pupae)
AMPHIPHOLIS KOCHII LUTKEN

Spawned eggs of A. kochii are 100 tm in diameter, opaque and slightly
brownish. After 6.5 hrs of development, the early blastula appears, which is
spherical and covered with a transparent, hyaline membrane through which
cilia protrude. Soon the shape of the blastula changes; it becomes oval and
elongates along the animal-vegetal axis. The gastrula forms after 20 hrs of
development. It is somewhat flattened laterally, retains the hyaline mem-
brane, and its surface is uniformly covered with cilia. After 25 hrs of devel-
opment, the gastrula forms a crest and then acquires a triangular shape. After
some time, it is possible to distinguish four axial spicules, rudiments of the
larval skeleton.

Pluteus I Stage

After 42 hrs of development, the early pluteus is formed. All the skeletal
rods in it are simple. At this stage, cilia are still retained over the entire body
of the larva but their length varies; the longest occur in the ciliated band and
at the basal end of the body. The crest is also retained. The entire larva is
opaque and reddish-brown. The hyaline membrane persists but its thickness
reduces considerably. In live specimens the skeletal rods are poorly visible.
at the 49th hr of development, the posterolateral arms increase somewhat in
length and their ends become transparent. The basal rods of the larval skel-
eton distally bear three prominent, short processes forming an analogue of a
lock. Cilia in the basal part of the body and the hyaline membrane are still
retained. The entire larva, except for the ends of its posterolateral arms and
the loop of the ciliated band of the oral region, is reddish-brown (Figure 172).

When the pluteus dimensions reach 350 um x 165 um, the skeletal rods
begin to show minute spines. The lower process of the basal rod elongates,
its length reaching 25 um. At the tip it becomes bifurcate. The larval body
in the region of the processes is drawn towards the ventral side. The reddish-
brown color disappears but the hyaline membrane is still intact at places.
Cilia of the basal part of the larva disappear. When the larva dimensions
reach 400 um x 200 tm, the rudiments of the posterolateral arms become
visible. The rods of these arms, as also the entire skeleton, are simple. At
dimensions of 450 um x 250 um, the lateral processes of the basal rods of
the skeleton elongate and form a rhombic structure, but do not fuse into a
single complex. At this stage, the hyaline membrane still persists at some
places, although its thickness reduced very significantly.

At dimensions of 500 um x 300 um, the posterolateral arms in the
pluteus become especially elongate and orange pigment granules begin to
appear along their spines. The hyaline membrane disappears completely.

224

Later, the posterolateral arms form and the overall body size of the larva
increases (Figure 172).

al

Figure 172: Amphipholis kochii.

A — early pluteus | stage; B — joining of rods of the larval skeleton in pluteus I stage;
C —pluteus I stage; D— joining of rods of the left half of the skeleton; E — joining
of basal rods of the skeleton.

al — anterolateral arms; br — basal rod; pl — posterolateral arm; po — postoral arm.

CHAPTER V

LARVAE OF SEA CUCUMBERS
(MORPHOLOGY, PHYSIOLOGY,
AND BEHAVIOR)

EARLY DEVELOPMENT

Egg

Among holothurians, Mortensen (1937) identified two species — Synaptula
vittata and Synaptula reciprocans — in which the egg diameter is 50 um. For
most species, eggs with a diameter of 100-200 um are characteristic. These
are Ophiodesoma grisea, Holothuria papillifera, H. difficilis (Mortensen, 1938),
Leptosynapta inhaerens (Runnstrém, 1927), and Stichopus japonicus. Among
holothurians of the genus Cucumaria, the egg diameter varies from 300 tm
in C. echinata to 1.5 mm in C. laevigata (Ohshima, 1921). The maximum
egg diameter has been observed in deepwater holothurians. According to
Ohshima (1921), Benthodytes gotoi and Euphronides depressa have eggs with
a diameter of about 2.5 mm and Enypniastes eximia of 3.5 mm.

Mortensen (1938) noted that in Ophiodesoma grisea the eggs are trans-
parent. Generally, the eggs of holothurians are opaque because of their large
yolk content, which is often red or yellowish-brown. In holothurians of the
genus Cucumaria, the eggs are yellowish-red at the animal pole and green at
the vegetal.

Smaller eggs are spherical. Large eggs are oval and often flattened at the
animal pole. This peculiar feature was noticed in Cucumaria echinata
(Ohshima, 1921), Thyone briareus (Ohshima, 1925), Cucumaria elongata
(Chia and Buchanan, 1969), and Caudina chilensis (Inaba, 1930). In Psolua
phantapus (Runnstr6m and Runnstrém, 1919) the eggs are oval.

The eggs are covered with vitelline and jellylike envelopes. The jellylike
envelope in some species is considerably thick. For example, in Cucumaria
echinata_ it is 50-70 um (Ohshima, 1921) and in C. elongata 40-60 um

226

(Chia and Buchanan, 1969). The presence of a micropyle process has been
reported at the animal pole of the oocyte, which is connected with the fol-
licular cells.

Fertilization : In holothurians extrusion of gametes in water as well as
their release in the coelomic sac has been observed, for example in Chiridota
rotifera (Clark, 1910). The spermatozoa penetrate not the mature egg but the
oocyte. When a micropyle is present, the sperm reaches the oocyte through
it. Ohshima (1925) observed in Thyone briareus sperm penetration at the
‘equator from the side of the vegetal hemisphere. During fertilization an
acrosomal reaction of the sperm occurs and a distinct fertilization cone is
formed (the primary eminence) in the eggs of Holothuria atra and Thyone
briareus (Colwin and Colwin, 1957).

After sperm penetration, meiotic division of the oocyte is completed with
the formation of polar bodies. Inaba (1930) observed in Caudina chilensis, in
the second meiotic division, the formation of three polar bodies which were
retained at the animal pole at the beginning of cleavage.

Cleavage : In holothurians, except for Cucumaria glacialis, independent
of the quantity of yolk in the egg, a complete uniform cleavage of the radial
type is observed. The first two divisions are meridional and the third equa-
torial. Thereafter, meridional and equatorial divisions alternate (Figure 73).
As the number of blastomeres increases, they shift to the animal and vegetal
poles, but the blastocoel remains open for some time in the polar region (Chia
and Buchnan, 1969). After formation of the 32-cell stage, the time of division
for different blastomeres differs and their radial disposition is disturbed (Kume
and Dan, 1968). In Thyone briareus (Ohshima, 1925), Cucumaria echinata
(Ohshima, 1921), and Caudina chilensis (Inaba, 1930), features appear during
division which are characteristic of spiral division. A unique division is
observed in Cucumaria glacialis in which the eggs are large and rich in yolk.
As reported by Ohshima, (1931), citing Mortensen, in the holothurian initially
only the nucleus divides and the newly formed nuclei are situated along the
periphery of the egg; thereafter division of the cytoplasm occurs with the
formation of blastomeres.

Blastula

According to Mortensen (1938), in Ophiodesoma grisea the blastula is
formed 4 hrs after fertilization. It takes 12-14 hrs before the blastula is fully
formed. In most species the blastula is spherical and the large blastocoel has
a cover of cilia (Figure 174). For several species (Synaptula vittata,
Ophiodesoma grisea, Holothuria spinifera, and H. papillifera) Mortensen
(1937,1938) reported that despite the presence of cilia, the blastula remains
inside the envelope. Usually, hatching takes place at this stage.

227

C

Figure 173. Caudina chilensis (Inaba, 1930).
Early stages of division.
A —4 blastomeres; B — 8 blastomeres; C — 16 blastomeres; pb — polar bodies.

In Caudina chilensis, as in some sea stars, several invaginations enter the
blastula_ cavity, depressions marking them on the surface (Inaba, 1930)
(Figure 175). Folos remain up to the beginning of gastrulation when they
begin to gradually smoothen. A wrinkled blastula has also been reported in
Cucumaria normani and C. saxicora (Kume and Dan, 1968).

Figure 174. Cucumaria_ frondosa Figure 175. Caudina chilensis (Inaba,
(=Psolinus brevis). 1930).
(Kowalewsky, 1867). Wrinkled blastula. General view.

Blastula. Blastocoel is well developed.

In species in which development occurs in the body of the adult indi-
vidual, the blastula remains immobile. Such a blastula is found in Holothuria
floridana (Edwards, 1909), Synapta vivipara (Clark, 1898, 1910), Chiridota
rotifera (Clark, 1910), and Thyone briareus (Ohshima, 1925).

Gastrula

In Ophiodesoma grisea and Holothuria difficilis the gastrula is formed
10 hrs after fertilization (Mortensen, 1938). Development of the gastrula
takes 18 —20 hrs in Synaptula reciprocans, Holothuria impatien, H. pardalis,

228

H. papillifera, and H. spinifera (Mortensen, 1937, 1938). In Caudina chilensis
the gastrula develops during 33 hrs (Inaba, 1930). According to Mortensen
(1937, 1938), in Ophiodesoma grisea, Synaptula vittata, Holothuria spinifera,
and H. papillifera, embryos hatch at this stage.

In holothurians, gastrulation proceeds through invagination. Before that,
the blastula slightly stretches along the animal-vegetal axis and its vegetal
pole flattens. Ohshima (1921) in Cucumaria echinata and Inaba (1930) in
Caudina chilensis have reported immigration of a large number of mesenchy-
mal cells before the initiation of gastrulation. In other species immigration of
the mesenchymal cells generally occurs from the tip of the archenteron, after
it reaches the middle of the gastrula (Figure 176). Later, the archenteron
bends to the future ventral side. Then the mouth opens, a through gut appears,
and the blastopore becomes the anus. Division of the gut into sections is not
yet discernible. In species in which development occurs through the
planktotrophic auricularia stage, a dipleurula is formed.

Dipleurula

Formation of the dipleurula begins when the gastrula changes shape. It
bends on the dorsal side and a large preoral depression forms on the ventral
side. The larva acquires a beanlike shape. The formed preoral lobe slightly
overhangs the oral depression.. Formation of the anal lobe involves displace-
ment of the anus and turning of the lower end of the intestine. The anus is
now situated on the ventral side in the middle of the anal lobe. Cilia covering
the gastrula disappear altogether, except on the edge of the preoral depres-
sion and lobes. A single ciliated band is formed.

Soon the gut divides into sections; esophagus, stomach and hind gut
(Figure 177). The epithelium of the gut is provided with cilia. At this stage,
no lateral body processes arise. Rudiments of the coelom are present in the
form of clusters of mesenchymal cells.

Auricularia

In most species the early auricularia develops in two days. Such are the
auriculariae of Ophiodesoma grisea, Holothuria scabra, H. spinifera, H.
impatiens, and H. pardalis (Mortensen, 1937, 1938). Lateral processes form.
at this stage. In the late auricularia the lateral processes, up to six pairs, are
well developed but not equal in length. Sometimes one or two pairs are
especially prominent in their size (Figure 178). In the larvae of holothurians
these processes are designated as follows: the anterodorsal and mediodorsal
lie above the mouth opening, while the preoral processes lie at the level of
the mouth opening. In the lower part of the larvae there are postoral,
posterodorsal and posterolateral processes.

229

Figure 176. Cucumaria frondosa Figure 177: Holothuria nobilis (Mortensen,
(=Psolinus brevis) (Kowalewsky, 1867). 1938).
Immigration of mesenchyma after Late dipleurula. Division of the tubular gut
gastrulation. into sections.
arch — archenteron; bl — blastopore; e — esophagus; hg—hind gut;
mc— mesenchymal cells. s — stomach.

Skeleton : a well-developed larval skeleton is not found in the larvae of
holothurians; the skeletal elements are represented by rods of different shapes
and small wheels, which are retained in the later stages. These structures are
especially characteristic of holothurian auriculariae of the genera Holothuria
and Stichopus (Mortensen, 1921, 1937, 1938).

Feeding : The mechanism of feeding in the holothurian larvae is similar
to that in the larvae of other echinoderms. In the early auricularia the preoral
lobe above the oral depression has a notch, while the tip of the anal lobe is
drawn out somewhat. Between these lobes lies the arched preoral depression
(Figure 178).

The perioral field in holothurian larvae lacks a ciliary cover. The food
particles are held in the perioral field by the water currents produced by
beating of the cilia in the lateral areas of the band. As in all echinoderms,
each cell of the ciliated band bears one cilium. Three to seven cells make up
the width of the ciliated band (Strathmann, 1971). On both sides of the
ciliated band, numerous secondary cells are present in the auricularia of
Parastichopus.

As the size of the ciliated band bordering the lateral processes increases,
the feeding mechanism in the larvae, exhibiting no change whatsoever, be-
comes more effective. Besides the single ciliated band, another, the adoral
ciliated band, appears around the oral cavity. Cilia are not present in the oral
cavity itself and, evidently, because of this, the auricularia has well-devel-
oped esophageal muscles and the muscles situated in the dorsal wall of the
oral cavity. From the perioral field the food is directed to the esophagus.

230

Here, upon contraction of the muscles surrounding the esophagus after open-
ing of the cardiac sphincter, the food particles are pushed into the stomach.
Here the food is sorted and food particles suitable for feeding are retained for
some time in the anterior part of the stomach, while unsuitable particles
accumulate near the pyloric sphincter separating the stomach from the hind
gut. When the pyloric sphincter opens, the stomach contents pass into the
hind gut and then, after the anal sphincter opens, are egested.

As was demonstrated by Strathmann (1971), the primary sorting may
occur in the oral cavity. Rejection of food from the oral cavity or esophagus,
or unsuitable food, is done by contracting the muscles of the esophagus and
oral cavity, accompanied by a change in direction of beating of the cilia of
the aboral band.

Holothurian larvae can feed on microalgae of no more than 70 Um in
diameter and no more than 150 um long. Different species of the genera
Phaeodactylum, Dunaliella, Amphidinium, and some others can also be food
objects of holothurians. The rate of filtration of algae from the water in
Parastichopus californicus is about 3 ml/m (Strathmann, 1971).

Respiration, transport of metabolites, and excretion: Holothurian larvae
lack organs for respiration and excretion. The provisional hemal system is
also not formed. Transport of food substances and excretion of metabolic
products is effected by the fluids of the primary and secondary body cavities.

In the early auricularia, the secondary body cavity or coelom is repre-
sented by the unpaired coelomic sac with the pore canal. The coelomic sac
soon divides into three sections; the hydrocoel and the left and right
somatocoels (Figure 179) (Kume and Dan, 1968).

prb

pob

Figure 178: Holothuria impatiens Figure 179: Arrangement of coelomic sacs

(Mortensen, 1938). in the auricularia (Kume and Dan, 1968).

Arrangement of ciliated bands in the he — hydrocoel; hp — hydropore; Is — left
perioral field. somatocoel; rs — right somatocoel.

pob — postoral band; prb — preoral band.

231

In the late auricularia, the hydrocoel has six diverticulae, lying initially
on the left side. These diverticulae later produce the primary tentacles and the
polian vesicle (Figure 180). The change in shape and size of diverticulae in
Stichopus japonicus is accompained by pulsation of the walls (Figures 181,
182).

Figure 180: Holothuria impatiens (Mortensen, 1938).
General view of the late auricularia.

Locomotion : The locomotor function, as in all echinoderms, is performed
by the ciliated band. The larva is capable of moving horizontally, turning in
various directions, and remaining stationary. All of these complex movements
are accompanied by a change in direction of beating of the ciliated band.
Strathmann’s (1971) observations have shown that beating of the cilia is not
synchronous throughout the entire length of the band; there is a strict alter-
nation of sections in which beating occurs in opposite directions. Due to such
alternation of direction of beating of the cilia, a running wave is created,
which involves the water layer surrounding the larva. The resultant water
currents produce a movement of the larva with its preoral lobe directed
forward and performance of other locomotory maneuverings.

Nervous system and sensory organs: Metschnikoff (1869) detected a
larval nervous system in the auricularia of Labidoplax digitata. In the ecto-
derm of the perioral field there are two bands of cilia situated in an arch.
These bands comprise two rows of cells, under which lie the bi- and tripolar
neurons. Mortensen (1937, 1938) also mentioned that nervous elements are
situated in the perioral field of auriculariae of various species of sea cucum-
bers. Unfortunately, no detailed information is available in the literature on
the structure of the larval nervous system.

232

Figure 181: Stichopus japonicus.
Formation of coelomic diverticula — rudiments of primary tentacles.

hc — hydrocoel; sc — somatocoel.

The bands of cells in the perioral field are sensory. According to Semon
(1888), these cells are provided with cilia. Sensory cilia are also situated on
the anterior end of the larval body, where the aboral organ is located.

The diverticula of the hydrocoel may be considered rudiments of the
definitive organs in the auricularia. The elastic spheres situated at the ends
of the lateral processes of the auricularia can be considered rudiments of the
provisional formation of the next larval state, the doliolaria.

238

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234
METAMORPHOSIS

Unlike the classes of echinoderms described above, metamorphosis in sea
cucumbers is evolutive; the processes of histolysis and resorption during
metamorphosis of sea cucumbers are expressed less markedly than in other
echinoderms. During this period several larval stages pass in which the ex-
ternal shape changes and internal readjustment of larval systems occurs and
definitive structures are formed. The planktotrophic, bilaterally symmetric
auricularia changes into a nonfeeding planktonic, radially symmetric doliolaria;
_ while living in the plankton, the doliolaria transforms into a pentactula, which
is morphologically the closest to the definitive juvenile sea cucumber. The
concluding stage of metamorphosis — transition from the pentactula to the
definitive individual — occurs after settling on the substrate. The axis of
symmetry of the larva and the definitive organism coincides in holothurians
(Smiley, 1986).

Transition of auricularia into doliolaria : In the developed auricularia of
Holothuria and Stichopus, before its change into a doliolaria, the so-called
elastic spheres are situated under the ciliated band at the ends of the lateral
processes (Mortensen, 1937, 1938). Their disposition and number are variable
in different species. The function of these structures is not altogether clear.
Possibly, their appearance is associated with the transformation of the ciliated
band since they are found in the places where the ciliated band formed in the
doliolaria. It may also be assumed that these spheres are particular depots
of reserve substances as they disappear earlier than the ciliated bands (Figure
h83):

Studies on the development of Stichopus japonicus have revealed that
soon after the appearance of elastic spheres, resorption of the lateral body
processes begins. In the posterior part of the larva the posterolateral processes
come closer while the posterodorsal ones completely disappear. The ciliated
band between them reduces and only small areas remain near the elastic
spheres. The anal lobe also reduces. The ciliated band disappears completely.
The anal opening closes and the intestine shortens. Simultaneous with the
changes occurring in the posterior half of the larva, its anterior end is also
transformed. The mediodorsal and anterolateral processes disappear. The body
becomes flat in the region of the anterodorsal processes. Remains of the
ciliated band, as in the posterior part of the larva, are retained only near the
elastic spheres. The preoral lobe disappears completely. The preoral processes
only shorten. The larva acquires the shape of a barrel with five transverse
ciliated bands. These run in the areas of the elastic spheres (Figure 184). In
other species of sea cucumbers fragments of the ciliated band of the auricularia
play a great part in the formation of the ciliated bands of the doliolaria. Thus,

DBS

Figure 183: Stichopus japonicus.
Arrangement of coelomic sacs and diverticulae in the auricularia before metamorphosis.

cd— coelomic diverticula; hc —hydrocoel; ls —left somatocoel; py — polian vesicle;
rs —right somatocoel.

the lowermost band is formed through the fusion of the remains of the band
of the posterolateral processes. The band lying above them is formed from the
two fragments of the band of the posterodorsal processes and the two frag-
ments of the band of the anal lobe. The medial band is formed from areas
of the band of the mediodorsal processes; the band lying above them is
formed from two parts of the band of the anterodorsal processes and one part
of the band right of the preoral lobe. The uppermost band is formed from the
parts of the band of the oral zone of the larva and the left side of the preoral
lobe (Kume and Dan, 1968).

Formation of the cilliated bands of the doliolaria proceeds fairly rapidly;
in Stichopus japonicus it takes 30-36 hrs. Formation of the doliolaria is the
turning point in the life of a sea cucumber larva since metamorphosis begins
from this stage.

236

Figure 184: Stichopus japonicus.
Stages of transition of the auricularia into
the doliolaria.

A, B — disappearance of preoral and anal

lobes and change of body shape; C —

young doliolaria. “Elastic” spheres situated
under the ciliated bands.

Doliolaria

The larval body is barrel-shaped with four—five transverse ciliated bands.
All of the skeletal elements present in the auricularia are retained here (Figure
185). The doliolaria is smaller than the auricularia; its length sometimes

237

constitutes one-half to three-fourths the length of the auricularia (Kume and
Dan, 1968). Retaining contact with the external environment, the oral cavity
transforms into a vestibule (vestibulum), homologous with the amniotic sac
of the late pluteus of sea urchins. In the vestibule the integument of the
former oral cavity surrounds the coelomic diverticulae that shifted here. In the
late doliolaria the vestibule is shifted to the anterior end of the larva and
formation of the primary tentacles commences in it.

The hydropore closes and the pore canal turns to the ventral side and
transforms into the stone canal, at the end of which the madreporite forms.
In Stichopus japonicus the madreporite has already developed in the auricularia
stage (Kume and Dan, 1968). In this sea cucumber, at the place of appearance
of the future medioventral radial ambulacral canal, a small protrusion appears
on the ring canal, which initiates the first unpaired ambulacral podium. This
podium remains inside the body for some time. In other sea cucumbers the
medioventral radial canal elongates and passes along the stomach to the
posterior end of the body. Here it bifurcates and a pair of coelomic rudiments
of the ambulacral podia forms on its ends (Kume and Dan, 1968).

In some sea cucumber species it is possible to identify one more stage,
the prepentactula, distinguished by a wide opening of the vestibule from
which primary tentacles may protrude. The ciliated bands are retained. In
Stichopus japonicus ° at this time, the ambulacral podium shifts to the outside
of the body and the larva uses it for attachment to the substrate. The elastic
spheres disappear completely. Radial and interradial spicules arise from the
perioral calcareous ring.

Pentactula

At this stage, the larva has five well-developed primary tentacles; it
retains the ciliated bands and skeletal elements formed earlier. Some species
have a pentactula stage and, in addition, one or several ambulacral podia
(Figure 186). It is in this stage that the definitive organ systems develop.

Skeleton : Besides the skeletal rods already formed in the auricularia and
the perioral calcareous ring, new spicules appear. These are situated along the
interradii and constitute the rudiments of intradermal plates and rods. The
newly formed spicules are diverse in shape. In some sea cucumber species the
skeleton of the pentactula is better developed than that of the definitive
individual.

Digestive system: The oral opening, surrounded by primary _ tentacles,
opens and leads into the esophagus. Primary, and then secondary, tentacles
serve as the trapping apparatus substituting for the trapping function of the
ciliated band of the auricularia, which is basically resorbed. A large part of

238

Figure 185: Holothuria impatiens Figure 186: Holothuria impatiens
(Mortensen, 1938). (Mortensen, 1938).
Arrangement of ciliated bands in the Pentactula before settling. Part of the

doliolaria. ciliated bands of the doliolaria is retained.

the larval integumental ephithelium transforms into the definitive. The ante-
rior section of the gut is modified into the larval esophagus and stomach
while the middle and posterior sections give rise to the small intestine. The
anal opening appears again (Ivanov-Kazas, 1978), as in Stichopus californicus
(Smiley, 1986), or the primary one is retained (Chia and Burke, 1978).

During metamorphosis the respiratory functions are passed on from the
larval epithelium to the definitive ephithelium and then to the special respi-
ratory organs, the respiratory tree. These organs together with the so-called
brown bodies take upon themselves the function of excretion. As is common
for echinoderms, the transport of metabolites after completion of metamor-
phosis, is done by the hemal and perihemal systems and coelomic body
cavities.

Locomotion: During metamorphosis of sea cucumbers, the locomotory
function is performed successively by the single ciliated band of the auricularia,
the ringed ciliated band of the doliolaria, the primary tentacles and sometimes
the first ambulacral podia of the pentactula, and finally, by the ambulacral
podia and (or) muscles of the body wall of the definitive animal.

In the pentactula, the ambulacral system consists of the perioral ambu-
lacral ring canal, from which issue the five primary tentacles and the polian
vesicle. Moreover, rudiments of all the radial canals are present which, start-
ing from the ring canal, descend along the stomach to the posterior end of the
larva. Ambulacral podia, except for those already present, do not form in
some species.

Nervous system: The pentactula has a definitive nervous system consist-
ing of the nerve ring surrounding the esophagus at the base of the primary

239

tentacles and five radial nerves extending along the radial ambulacral canals.
The ring canal develops from the thickening of the vestibular bottom (Kume
and Dan, 1968). According to Ivanova-Kazas (1978), the presence of a con-
nection between the larval and definitive nervous system is assumed. This
assumption is based on the data of Metchnikoff, who observed that before
metamorphosis the nerve elements present in the auricularia in the preoral
field shift to the oral opening and become a part of the vestibular bottom of
the doliolaria. Semon (1888) was also of this view.

Statocysts lie at the base of the radial nerves of the pentactula; possibly
they are involved in larval settling.

Settling : After the appearance of spicules, the pentactula loses its ciliated
bands and finally settles down. Now the formation of secondary tentacles and
ambulacral podia commences. In the literature there is no information about
the mechanism of settling of sea cucumber larvae. Nothing specific is known
about their ability to recognize a suitable substrate for settling. Chia and
Spaulding (1972) mentioned that the polychaete tubes of Phyllochaetopterus
induce settling in Cucumaris miniata and Psolus chitinoides. Slime stimulates
metamorphosis in Molpadia intermedia (McEuen and Chia, 1985).

The pentactulae of all sea cucumbers have primary tentacles. In addition
to them, the species with ambulacral podia, develop one or two podia by the
time of settling. Strathmann (1978a) reported that various synaptids which
lack ambulacral podia in the adult stage, use their primary tentacles for
digging into the ground or creeping.

In the pentactula stage, Stichopus japonicus is capable of attaching to the
substrate by means of a single ambulacral podium which, by this time, has
appeared at the posterior body end. The larva, on attachment with this po-
dium, remains sessile for some time, then retracts the podium within its body
and resumes swimming. It repeats such maneuvers until the primary tentacles
are finally formed and the vestibule is reduced. After this, the podium is no
longer retractable, but the larva continues for some time to alternate swim-
ming over the substrate with creeping on it. While swimming, it touches the
substrate from time to time.

Based on the information available on the structure of the terminal podia
of sea urchins (Burke, 1980) (see Figure 127), it may be assumed that the
ambulacral podia in sea cucumbers have an analogous structure. If the am-
bulacral podia of sea cucumbers have sensory cells, they ought to play an
important role in the selection of the substrate and settling. Judged from the
observations of various researchers, the primary tentacles are capable of
discharging the same role.

240
LECITHOTROPHIC LARVAE

Species of sea cucumbers with lecithotrophic larvae have large eggs rich in
yolk. Their early development differs little from various species with
planktotrophic larvae. Differences are observed only from the gastrula stage.
A larva entirely covered with cilia and having a coelom and gut divided into
sections develops later (Kowalewsky, 1867; Ohshima, 1921; Inaba, 1930).
The anal end becomes slightly flattened and the oral opening forms from the
ventral side. The ciliary cover changes. Cilia persist at the preoral end and
near the anus; between these fields two-five ciliated bands form (Figure 187).
Thus, the doliolaria is formed, avoiding the stages of dipleurula and auricularia.
Oil drops are present in the preoral part of the doliolaria, which enable the
larva to maintain a vertical position in water. The doliolaria swims by rotating
around the animal-vegetal axis. In lecithotrophic larvae the digestive system
is not fully formed and the principal formative processes are associated with
the development of the coelom (Figure 188).

Figure 187: Caudina chilensis (Inaba, Figure 188: Chiridota rotifera (Clark, 1910).
1930). Differentiation of coelom into sections.

Doliolaria of lecithotrophic type of arch —archenteron; bl — blastopore;

development. Ciliary cover is retained on cb—ciliated band; hc —hydrocoel;

the preoral lobe. oo — oral opening. hp —hydropore; Is — left somatocoel;

rs —right somatocoel.

The structure of the pentactula in sea cucumbers with planktotrophic
larvae shows no substantial difference. The ciliated bands are retained and the
larva can swim as well as creep. In apodous pentaculae the ambulacral podia
do not develop, while in cucumariids one or two podia appear at this stage
(Figure 189). Their development, as in the species with planktotrophic larvae,
is associated with the medioventral ambulacral canal.

It is necessary to note that in some species development with lecithotrophic

241

larvae is quite close to direct development. In
Cucumaria frondosa (Edwards, 1909), for ex-
ample, the pentactula hatches from the enve-
lope with five tentacles and one ambulacral
podium.

A review of the literature shows that
development with lecithotrophic larvae is of-
ten founds sins Species sot the s order
Dendrochirotido (see Table 7). Moreover, in
this order as well as in Apodida, either brood
care or direct development is characteristic of

many species. At present, nearly 30 such spe-
(Inaba, 1930). ; é

Pentactula before settling. Preoral lobe eles ale known, among which almost half ale
has disappeared. Primary tentacles inhabitants of polar and adjacent regions.
protrude from the oral cavity. Ciliated Such, for example, are the Dendrochirotida
bands are still retained: species Cucumaria laevigata and Psolus
koehleri and the Apoda species Taeniogyrus
controtus from the Antarctica, and the Dendrochirotida species Cucumaria
glacialis from the Arctic. Brood sacs also occur in one Sakhalin species,

namely, Thyone imbricata (order Dendrochirota).

Brood care of the young in cold-water sea cucumbers takes place in
various brood sacs or pockets, which are specific dermal processes. In several
species (Psolus antarcticus, Psolus granulosus, Psolus punctatus, Psolus figulus,
Psolidium incubans, Cucumaria parva, and Cucumaria curata) the young are
carried on the smooth part of the creeping side (Hyman, 1955).

It is interesting to note that in tropical sea cucumbers the young develop
inside the body coelom of the mother. Sometimes lecithotrophic larvae de-
velop in such sea cucumbers. In Apodida the larva of Chiridota rotifera
(Clark, 1910) retains the ciliary cover while Synapta vivipara (Clark, 1898,
1910) does not, even though the larva of this sea cucumber develops through
the same stages as does Chiridota rotifera. One more type of brood care has
also been identified, wherein development of the young takes place in the
ovaries of the female. This type of development has been described in par-
ticular for the Antarctic Apodid, Taeniogyrus contortus (Hyman, 1955).

Besides brood care, instances of direct development are known in sea
cucumbers. In this case the eggs are spawned in water and the juvenile
develops avoiding both the auricularia and doliolaria stages. Development in
Thyone briareus (Ohshima, 1925) and Holothuria floridana (Edwards, 1909)
proceeds in this manner.

The feature common to species with brood care and species with direct
development is the presence of large yolky eggs. A list of species of sea
cucumbers and their type of development is given in Table 7.

Figure 189: Caudina chilensis

Table 7: Types of development in sea cucumbers

Species

Type of
development

Source

Cucumaria laevigata
Cucumaria glacialis
Cucumaria parva
Cucumaria curata
Cucumaria lateralis
Cucumaria crocea
Cucumaria joubini
Cucumaria ijimai
Cucumaria lamperti
Cucumaria planci
Cucumaria coatsi
Cucumaria vaneyi
Cucumaria echinata
Cucumaria elongata
Cucumaria saxicola
Cucumaria normani
Cucumaria frondosa
Pseudocucumis africanus

Thyone rubra
Thyone briareus
Thyone imbricata

Psolus ephippifer
Psolus antarcticus
Psolus granulosus
Psolus koehleri
Psolus punctatus
Psolus figulus

Psolus phantapus
Thyonepsolus nutriens
Psolidium incubans

Phyllophorus urna

Order Dendrochirotida
Family Cucumariidae

Brood care
Same
Same
Same
Same
Same
Same
Same
Same
Lecithotrophic larva
Brood care
Same
Lecithotrophic larva
Lecithotrophic larva
Same
Same
Same
Brood care

Family Phyllophoridae

Brood care

Family Sclerodactylidae

Direct development

Family Phyllophoridae

Brood care

Family Psolidae

Same
Same
Same
Same
Same
Same
Lecithotrophic larva
Brood care
Same

Family Phyllophoridae

Brood care

Hyman, 1955
Mortensen, 1894
Hyman, 1955
Same

Same

Same

Same

Same

Same

Same

Same

Same

Ohshima, 1921
Chia and Buchanan, 1969
Thorson, 1946
Same

Same

Hyman, 1955

Same

Ohshima, 1925

Hyman, 1955

Same

Same

Same

Same

Same

Same

Thorson, 1946
Hyman, 1955
Same

Hyman, 1955

243

Species

Type of
development

Source

Holothuria arenucola
Holothuria spinifera
Holothuria scabra
Holothuria impatiens
Holothuria pardalis
Holothuria papillifera
Holothuria difficilis
Holothuria nobilis
Holothuria marmorata
Holothuria floridana
Actinopyga mauritiana
Actinopyga serratidens

Stichopus variegatus
Stichopus japonicus

Bathyplotes natans

Paracaudina chilensis

Synapta vivipara
Synaptula hydriformis
Synaptula vittata
Synaptula reciprocans
Ophiodesoma grisea
Leptosynapta minuta
Leptosynapta inharens
Labidoplax digitata

Chiridota rotifera
Taeniogyrus contortus

Trochodota dunedinensis

Order Aspidochirotida

Family Holothuriidae

Planktotrophic larva
Same
Same
Same
Same
Same
Same
Planktotrophic larva
Same
Direct development
Planktotrophic larva
Same

Family Stichopodidae

Planktotrophic larva
Same

Family Synallactidae

Brood care

Order Molpadiida

Lecithotrophic larva
Order Apodida

Family Synaptidae

Brood care
Same
Planktotrophic larva
Same
Same
Brood care
Lecithotrophic larva
Planktotrophic larva

Family Chiridotidae

Brood care
Same
Same

Mortensen, 1937
Same

Same
Mortensen, 1938
Same

Same

Same
Mortensen, 1938
Mortensen, 1937
Edwards, 1909
Mortensen, 1937
Same

Mortensen, 1937
Our data

Hyman, 1955

Inaba, 1930

Clark, 1910

Hyman, 1955
Mortensen, 1937, 1938
Mortensen, 1937
Mortensen, 1938
Hyman, 1955
Thorson, 1946
Metschnikoff, 1869

Clark, 1910; Engstrom, 1980
Hyman, 1955
Same

244

IDENTIFICATION OF PELAGIC LARVAE OF SEA CUCUMBERS
(Terminology and Diagnostic Characters)

The absence of a developed endoskeleton is characteristic of holothurian
larvae. The larvae develop through several stages differing in external mor-
phological features, which are important for their identification.

Species with planktotrophic larvae pass through the stages of dipleurula,
auricularia, doliolaria, and pentactula. Species with lecithotrophic larvae pass
through the stages of doliolaria and pentactula. The species characters at the
stage of dipleurula are very poorly developed and cannot be used for the
identification of larvae. The latter becomes practically possible only from the
stage of auricularia, when lateral processes appear. There are generally six
pairs of processes differing in size but sometimes some of them do not
develop at all. Their position in a fully formed larva is as follows: above the
preoral lobe lie the anterodorsal processes, followed by the mediodorsal, and
the preoral process behind them. Somewhat lower are the postoral processes,
below them the posterodorsal, and at the base of the anal lobe the postero-
lateral processes. The auricularia has a single ciliated band. The lower end
of its body may be triangular, as in the larvae of the genus Holothuria, or flat,
as in the genus Stichopus. At this stage, the larvae of some sea cucumbers
have various spicules in the form of simple calcite plates of different shapes
or in the form of wheels and hooks. These skeletal elements are retained in
the later stages of larval development. In some members of the genera
Holothuria and Stichopus elastic spheres appear in the auricularia stage at the
tips of the processes and sometimes at the base of the larval body (Holothuria).
Their number and arrangement vary in different species. These spheres also
persist in later stages of development.

The doliolaria is barrel-shaped with four—five transverse ciliated bands
that are isolated from each other.

The lecithotrophic doliolaria differs in that the preoral and anal fields do
not shed their ciliary cover. The larva has no skeletal elements and elastic
spheres and the ciliated bands range from two to five.

The pentactula has well-developed primary tentacles, which may be di-
stally bifurcate or bear numerous papillae of various shapes. Rods, the rudi- °
ments of definitive ossicles, appear at this stage. In larvae with a planktotrophic
type of development the ossicles formed in the auricularia stage and the
ciliated bands are retained.

For identification of planktotrophic larvae, of primary importance are the
structure of the skeletal elements, the presence and number of elastic spheres
and their arrangement, and the degree of development of the lateral processes
in the auricularia.

For

245

identification of lecithotrophic larvae, the significant characteristics

are the number and arrangement of ciliated bands in the doliolaria, and the

presence

or absence of ambulacral podia and the shape of the tentacles in

the pentactula.

The

diagnostic features for the larvae of sea cucumbers are given below:

-1. In the auricularia stage :

a.
b.
C,
d.

e.

presence or absence of lateral processes;

shape of the lower end of the larva;

presence, number, and shape of calcite ossicles;

presence, number and arrangement of elastic spheres in the late
auricularia;

color of larva.

2. In the doliolaria stage :

a.
b.
c.

presence, number, and shape of ciliated bands;
presence, number, and shape of calcite ossicles;
color of larva.

3. In the pentactula stage :

a.
b.
C.
d.

i OD,

Daly:

1).

lO):

presence, number, and shape of calcite ossicles;
presence or absence of first ambulacral podia;
number of ambulacral podia;

shape of primary tentacles.

Key to Families Based on Eggs

Eggs large, oval, buoyant, reddish-green........ Cucumariidae
Eggs small sphericalycrayish. see eee ee Stichopodidae

Key to Families Based on Larvae in the Doliolaria Stage

Larva large, opaque and completely covered with short cilia. No
calcite ossicles in the basal part....... Cucumariidae sensu lato

. Larva small, transparent, with incomplete cover of short cilia and

five transverse ciliated bands. Calcite ossicles present in the basal
part. Siegal tay apace MN a Ma ata Stichopodidae (Stichopus japonicus )

Key to Families Based on Larvae in the Pentactula Stage

Primary tentacles with five papillae. Ciliated bands absent... . .
Eb TT: ROP is OUSIDE SER UDCA Ok RE Cucumariidae

. Primary tentacles lack papillae. Ciliated bands present........

Ra tee SRN a ge Areca Stichopodidae (Stichopus japonicus)

246
CHARACTERS OF LARVAE ACCORDING TO FAMILIES

Cucumariidae sensu lato

Development with lecithotrophic larva: The eggs are large, float on the
surface layer, 300-450 um in diameter. The animal pole may be tinted
reddish-orange, but the rest of the larva is greenish. Either the larva is entirely
and uniformly covered with short cilia or a few transverse ciliated bands
occur in its lower half. The pentactula has five primary tentacles, which are
distally bifurcate and provided with numerous papillae, as well as one or two
ambulacral podia, located above the anal opening and connected with the
medioventral ambulacral canal.

Two species of this family — Cucumaria japonica Samper and Eupentacta
(= Cucumaria) frudatrix (Djakonov and Baranova) — are found in Peter the
Great Bay.

Stichopodidae

Development with planktotrophic larva: The eggs are about 100 um in di-
ameter and spherical. The larva is transparent. The postoral processes are best
developed in the auricularia (Stichopus japonicus). Calcite lumps of various
shapes and sizes lie at the base of the anal lobe on both sides. The posterior
end of the larva is flat. Five pairs of elastic spheres appear in the late
auricularia. Five transverse ciliated bands are present in the doliolaria and the
elastic spheres and calcite lumps persist. The pentactula has five primary
tentacles and one ambulacral podium; elastic spheres are absent while calcite
ossicles and ciliated bands persist.

The only member of this family found in Peter the Great Bay is Stichopus
japonicus Selenka. The auricularia of this species has been described by
Kume and Dan (1968). A more complete description of the development of
S. japonicus is given below.

FAR EASTERN TREPANG
STICHOPUS JAPONICUS SELENKA

Mature eggs in the trepang are nontransparent, about 150 um in diameter.
Artificial fertilization is not always successful. Thermostimulation is the re-
liable method for obtaining viable larvae, whereby the female releases mature
eggs. The blastula forms 6-8 hrs after fertilization at a water temperature of
20-21°C. The blastula is spherical but gradually elongates in the animal-

247

vegetal axis. The gastrula forms by the end of the first day of development.
It is highly transparent, slightly flattened at the vegetal pole, with short cilia
completely covering its surface. At the end of the second day the gastrula
transforms into a dipleurula. This stage may last as long as two days. There-
after the next stage, the auricularia, sets in, which is the longest stage in the
development of the trepang.

Auricularia

The larva is transparent. In each corner of the anal lobe an irregularly
shaped calcite ossicle forms, which is much larger in the left corner. Under
the ciliary band, at the ends of the lobes, there are five pairs of round cavities,
the elastic spheres. Mortensen (1937) mentioned similar structures while
describing the larvae of Holothuria arenicola and H. scabra. These cavities
are possibly the organizing centers from which-formation of the ciliated bands
of the doliolaria originates. After their appearance, the oral and anal lobes
reduce and the ciliated band on them disappears. In the late auricularia the
lateral lobes are smooth. Before transition to the doliolaria, the length of the
auricularia is about 400 um (Figures 190, 191).

Doliolaria :

This stage continues for two days. It is characterized by a barrel-shapec
larva in either a ventral or dorsal view. In a lateral view it is clearly apparent
that the depression in the region of the mouth persists. The fully developed
doliolaria has five ciliated bands: anterolateral, preoral, oral, preanal, and
postanal. The doliolaria is less transparent than the auricularia. The calcite
ossicles are large and lie under the postanal band along the corners of the
doliolaria. The anterior and under the anterolateral band thickens. The length
of the larva at this stage is 400 um (Figs. 192, 193).

Prepentactula I

The larva is elongate. The round cavities are almost indistinguishable but
the ciliated bands are completely retained. The calcite granules underlying
the postanal band gather at this stage in the middle of the posterior end of
the larva. The five primary tentacles are distinctly visible through the integu-
ment; they are sometimes extruded and again retracted into the vestibular
cavity. Further, the perioral calcite ring and the madreporite are distinguish-
able. Below the calcite ring the unpaired ambulacral podium lies along the
stomach. The length of the larva at this stage is about 400 lum (Figure 194).

248

Figure 191: Stichopus japonicus.
Auricularia in stage of disappearance of the oral and anal lobes. Large cavities visible under
the ciliated bands.

Figure 192: Stichopus japonicus.
Doliolaria. General view.

Figure 193: Stichopus japonicus.
Postdoliolaria. Large cavities persisting. Calcite ossicles visible at the bottom.

250

Prepentactula II

This stage is characterized by the anal ambulacral podium which can
extrude by means of it the larva is capable of attachment to the substrate. All
the five ciliary rings persist and continue to perform a locomotory function
(Figure 195).

Figure 194: Stichopus japonicus.
Prepentactula. Large cavities have

Figure 195: Stichopus japonicus.
Prepentactula. Anal ambulacral podium has

disappeared.
Primary tentacles are distinctly visible in
the vestibular cavity.

emerged outside the body. One of the
primary tentacles protrudes from the
vestibular cavity.

Pentactula
At this stage, the primary tentacles of the larva are not retracted into the
vestibular cavity, which now remains wide open. The larva is capable of
moving by means of its tentacles and podia. At this stage, it is possible to
- distinguish skeletal rods of different shapes scattered throughout the body
under the integument. The length of the larva is about 500 tm (Figure 196).
In the trepang as well as in Thyone briareus (Ohshima, 1925) and Cucumaria
elongata (Chia and Buchanan, 1969), the first tentacles begin to appear only
in the juvenile.

Ecology

Larvae of the trepang begin to appear in Vostok Bay in July when the
water temperature is 18°C. Spawning is observed until August. According to
Mokretsova (1975), in Posjet Bay the average duration of development from

US|

Figure 196: Stichopus japonicus.
Pentactula. General view of the larva.

fertilization to settling at a water temperature of 21°C is 16—20 days. Spawn-
ing, as in Vostok Bay, continues from June to August. Kinosita (1938) also
reported these periods for Hokkaido, Tanaka (1958) reported for southern
Hokkaido that spawning of the trepang begins at the end of June. In other
parts of Japan the trepang may begin spawning in mid-May (Mitsukuri, 1903)
and even in mid-March (Choe, 1962).

JAPANESE CUCUMARIA
CUCUMARIA JAPONICA SEMPER

Eggs large, dark green, rich in yolk, 450 tum in diameter. They are found in
the plankton at a water temperature of 11°C. The blastula forms at the end
of the first day of development and is oval in shape. The gastrula develops
two days after fertilization. It is slightly flattened dorsoventrally. Like the
blastula, the gastrula is also entirely covered with short cilia. Both the blas-
tula and the gastrula swim in the surface water layer, rotating around their
axis with the animal pole directed forward.

D2

Doliolaria

Formed on the third day of development, the doliolaria is 650 um long.
Its entire body is covered with cilia and is tinted green. No ciliated bands
were observed, which are typical of the larvae of other holothurians of this
family. The oral opening is situated in the anterior third of the larva. A yolk
accumulation at the animal pole in the preoral lobe tints this part of the larva
dark green (Figure 197A).

() So°o °

o\ Jo 09 O89, f,
©0000 09™~op Y 20g,, 909
0500 00 ‘3 oO 0 2

Figure 197. Cucumaria japonica.

A — doliolaria; B — early pentactula; C — pentactula; D— madreporite; E — plate of the
perioral calcite ring; F — plates of the ambulacral podia.

Pentactula

The early pentactula may not differ in size from the doliolaria but the
green tinge diappears except in the preoral lobe. In a dorsal view of the larva
the primary tentacles and two ambulacral podia of the medioventral canal are
visible. At this stage, these are still immobile. In the late pentactula stage the

253

podia begin to protrude from the vestibular cavity (oral opening) and small
papillae appear on their suckers (Figure 197B). The pentactula may reach a
length of 1 mm. The dermal plates and skeletal elements of the ambulacral
podia begin to form while the pentactula is still in the plankton. Skeletal
elements are absent in the primary tentacles. Plates are visible in a live larva
at low microscopic magnification when the larva is slightly pressed (Figure
197D, E, F). On settling, the preoral lobe is reduced and the juvenile moves
over the substrate using its primary tentacles and two ambulacral podia (Fig-
ure 197C). Sometimes juveniles are trapped in bottom catches of plankton.

FRAUDULENT EUPENTACTA EUPENTACTA FRAUDATRIX
(DJAKONOV AND BARANOVA)

Eggs large, ellipsoidal, dark green, yolky, 400-420 um in diameter. They are
enveloped in a thick jellylike envelope. The blastula forms after 13—15 hrs
of development at a water temperature of 20—21°C. It is greenish and slightly
flattened dorsoventrally.

The gastrula has formed within 24 hrs upon fertilization. Like the blas-
tula, it has a greenish tint too, is flattened and uniformly covered with short
cilia. Both the blastula and the gastrula swim in the surface water layer, they
rotate around their axis with the animal pole directed forward.

Doliolaria

This stage develops within two days. It is slightly flattened dorsoven-
trally. The oral opening is situated slightly above the equator. The entire
doliolaria is uniformly covered with short cilia and tinted green. The preoral
lobe forms now and contains the entire nutrient reserve, because of which it
is darker than the rest of the larval body. The length of the larva at this stage
is 400-450 um (Figure 198A).

Pentactula

This stage is attained after 57 hrs of development. The body is also
slightly flattened dorsoventrally and covered with short cilia. As in C. ja-
ponica, ciliated bands do not form in this species. In the broadened vestibular
cavity the suckers of the five primary tentacles are discernible. At the lower
end of the body above the anus lie the two ambulacral podia of the medioventral
canal. The length of the larva at this stage is 500 um (Figure 198B). In the
late pentactula the madreporite and plates of the perioral calcite ring are
clearly visible. In addition, spicules develop on the dermal plates and two
plates of ambulacral podia, which lie in the suckers (Figure 198D, E, F). The
skeletal elements can be seen in a live larva at low microscopic magnification
and with slight pressing of the larva. On settling, the preoral lobe reduces and

254

Figure 198: Eupentacta fraudatrix.

A — doliolaria; B —early pentactula; C — pentactula, D—— madreporite; E —plate of
the perioral calcite ring; F —plates of the ambulacral podia.

the juvenile individual moves over the substrate by means of the primary
tentacles and two ambulacral podia. Sometimes juvenile individuals are trapped
in bottom catches of plankton (Figure 198C).

CONCLUSION

The main purpose of this book has been to presént the bulk of factual material
which requires further observations and analysis. In concluding it, perhaps a
brief comparison of the larvae of bivalves and echinoderms is warranted. To
a significant extent independent of the phylogenetic affinity of the organisms
and the similarity of the ecological niches occupied by them, the planktotrophic
larvae of these animals are highly similar in morphology, physiology, and
behavior. Such a similarity is the result of adaptation to a pelagic mode of
life. In contrast to the diversity of ecological conditions in the benthic period
of their life cycle, these organisms experience in the water column a more
uniform habitat or environment. The most important adaptation of larvae to
swimming and feeding in water was the appearance of the ciliated band —
the principal multifunctional provisional organ, which is primarily a locomo-
tory and trapping apparatus. The function of the ciliated band also facilitates
the processes of respiration and excretion and its separate elements serve as
sensory organs. The location of the ciliated bands on various processes of the
larval body (arms, processes, velum) facilitates floatation of the larvae; these
processes often function as stabilizers and rudders. The characteristic defen-
sive feature of pelagic larvae, as also of other planktonic organisms, is their
relative colorlessness and transparency. There are also some other characters
ensuring for planktotrophic larvae life in the water column. Some of these
features can be traced directly from the larvae of primitive multicellular
creatures, while others arose secondarily during the evolution of various
groups.

Comparing larval periods in the life cycles of bivalves and echinoderms,
we note that the postembryonal larval period begins exceptionally early, from
the stage of the late blastula or the early gastrula. Such an early transition to
the postembryonal period is encountered in lower multicellular animals, for
example hydroid polyps, but in most other animals it is delayed as a result

256

of embryonization of development (Ivanova-Kazas, 1975), which is not the
case in the groups under discussion. Of course, the free-swimming blastula or
early gastrula of echinoderms differs in many features from the similar stage
of bivalves. The principal difference is the presence already at this stage in
mollusks of the rudiment of a shell gland, which is a clear example of the
tendency towards “adultation” of development in bivalves (Jagertsen, 1972).
In echinoderms this tendency appears much weaker. As a result of “adultation”
the transition of larvae to definitive organisms has the nature of “evolutive”
metamorphosis in bivalves. For echinoderms, catastrophic metamorphism is
characteristic, which has caused greater divergence in the structure of pelagic
larvae and definitive organisms due to the changeover in the ancestral type
to radial symmetry and a sessile mode of life in the adult animal.

Speaking of the parallel paths in the evolution of pelagic larvae of bivalves
and echinoderms, mention must be made of lecithotrophic larvae, in which
the ciliary cover serves mainly as a locomotory apparatus. The ciliary cover
in the doliolaria of sea cucumbers is quite identical with the cover of the
doliolaria of sea lilies and brittle stars; on the other hand, the ciliary cover
of these echinoderm larvae is analogous with that of the lecithotrophic larvae
of bivalves of the subclass Protobranchia.

In conclusion, we would like to say a few words on some, in our opinion,
promising trends in investigation of the life cycles of bivalves and echino-
derms. The results presented in the preceding chapters together with the
material presented in our book “Razmnozhenie iglokozhikh 1 dvustvorchatykh
mollyuskov” [Reproduction of Echinoderms and Bivalves] (1980) provide an
overall picture of the life cycles of the investigated groups of animals in a
morphological aspect. Some answers have been obtained to the first questions
arising during studies on the life cycles of marine invertebrates with pelagic
larvae: when do the animals spawn? what processes occur in their gonads
throughout the year? which type of larva do they have? and, how to identify
this larva? All of this information is necessary but still insufficient for under-
standing how the actual life cycles proceed and which mechanism ensures
them.

Morphological approaches to investigation of the life cycles, based on a
knowledge of the reproductive cycles occurring in the gonads on one hand,
and descriptions of larval morphology, on the other, may at the cytological
level explain the cytological peculiarities that ensure any variation of the life
cycle. However, the considerable data on gametogenesis and cytology of
larvae have not yet been examined from this viewpoint.

Our book does not consider the ecological aspects of larval life. Numer-
ous investigations on the ecology of larvae in nature, conducted in the Sea
of Japan and various regions of the World Ocean have been supplemented in
the last decade with laboratory studies on the influence of ecological factors

Uy ty

on larvae. These data on the larvae of bivalves and echinoderms, diverse in
methods, conditions, and accuracy of studies requires systematization. The
next step to understanding the ecology of life cycles as a whole would be to
present the entire descriptive and experimental material in the conceptual
framework of any model of the life cycle —1, K-strategy — or other more
adequate models of the strategy of the life cycle, providing a vivid picture of
its “economy” in conditions of variable biotic factors. This step has been
done. In 1989, we published a book entitled “Reproduktivnaya strategiya
morskikh dvustvorchatykh mollyuskov 1 iglookozhikh” [Reproductive Strat-
egy of Marine Bivalves and Echinoderms] (Kasyanov, 1989). We leave it to
the reader to judge whether our step was in the right direction and whether
it was successful.

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