Edible Sea Urchins: Biology and Ecology

412 Pages·2001·7.681 MB·1-419\412

by  John M. Lawrence (Eds.)

Preface
Sea urchins have been known to the scientific community since the days of Aristotle. Until
about fifty years ago studies on them were primarily anatomical, developmental, and
paleontological. Since then, research on their biology and ecology has increased greatly. This
was stimulated first by a recognition of their ecological importance and then by a realization of
their economic importance.
This book was designed to provide a broad understanding of the biology and ecology of sea
urchins. Synthetic chapters consider sea urchins as a whole to give a broad view. Chapters that
consider the ecology of individual species integrate the various life-history phases. The goal was
to provide both individual and general perspectives. Although the impetus of this book was the
interest in fisheries and aquaculture, not all the species considered are important in fisheries or
candidates for aquaculture. I believe that an understanding of the biology and ecology of these
species will aid in understanding the biology and ecology of those species that are. My only
regret is that a wider range of species could not be considered.
Although the authors of the ecology chapters exchanged outlines, they were not required to
adhere to a specific one. This recognized the difference in the information available and in the
interests of the authors. I found this resulted in a diversity of emphasis and approach that is
extremely interesting and enlightening. The treatment of species in both the synthetic and
ecology chapters is complementary.
I am grateful to my friends and colleagues, experts in their fields, who have contributed to this
book. I thank Wenger Manufacturing, Inc., Sabetha, KS, for funds for the publication of the
frontispiece.
John Lawrence
Tampa, Florida
Edible Sea Urchins: Biology and Ecology
Editor: John Miller Lawrence
(cid:14)9 2001 Elsevier Science B.V. All rights reserved.
The edible sea-urchins
John M. Lawrence
Department of Biology, University of South Florida
Tampa, Florida 33620, USA
The "roe" of sea urchins have been consumed by humans since pre-historic times as indicated
by middens from the Aleutian Islands to the Caribbean Sea and Chilean coast. Strictly speaking,
gonads are eaten and not the roe, as roe are defined as eggs or ovaries containing eggs. Obviously
this would not apply to the testes. Nor would it apply to the pre-gametogenic stage of the ovaries,
which is the usual stage at which the gonads are eaten.
In recent years, increased demand has led to overfishing so that stocks have diminished. This
was noted already in the first review of sea-urchin fisheries (Sloan 1985). A re-analysis has
documented the continuing demand for sea urchins that has resulted in continued expansion of
fishing grounds and harvest (Keesing and .)899111aH This has had major consequences.
Sea urchins are major consumers in the shallow waters of the world oceans and often
determine community structure (Lawrence 1975; Lawrence and Sammarco 1982). A major
change in community structure resulting from the removal of a major herbivore by overfishing
can be predicted. This has been little noted or considered. The increase in the economic value
of sea urchins resulting from overfishing has been widely noted. The response here has been
primarily in attempts at fisheries management (California Sea Grant 1992). In addition, interest
in aquaculture of sea urchins has increased considerably (Hagen 1996; Lesser and Walker 1998;
Keesing and Hall 1998).
The sea-urchins that are eaten are distributed among a number of orders of regular echinoids
(Table )1 (Matsui 1966; Mottet 1976; Sloan 1985; Saito 1992a; Keesing and Hall 1998;
Lawrence and Bazhin 1998). I know no a priori reason why any sea-urchin species should not
be edible, but the fact remains that relatively few species are eaten. Some major taxa, such as
cidaroids, seem not to be eaten at all. Three possibilities could explain why so few species are
eaten. First is accessibility. All species that are eaten are found in shallow water. A second
possibility is palatability. Although Tetrapygus niger is abundant along the Chilean coast and
the tradition of consumption of sea urchins exists, the species is not consumed as it is not
palatable (Lawrence and Bazhin 1998). Although the raw gonads of Hemicentrotuspulcherrimus
are not eaten as they have a bitter taste, they are eaten after preservation in brine or alcohol
(Agatsuma, this volume). A third possibility is historical (cultural). Sea-urchin consumption in
the Mediterranean countries varies (Le Direac'h et al. 1987). It is high in France but is limited
on the north-African coast and the Aegean countries. Extensive consumption in the Caribbean
has been limited to Barbados (Lewis 1962; Scheibling and Mladenov 1987) and, in South
America, to Chile (Bustos et al. 1991; V~quez and Guisado 1992). The Japanese tradition of
consumption (Saito 1992a) has been so extensive it has led to true mariculture (Saito 1992b).
Table .1 Classification of echinoids with representative genera (modified from Smith 1984).
Class Echinoidea
Subclass Perischoechinoidea
Subclass Cidaroida
Subclass Euechinoidea
Infraclass Echinothurioidea
Order Echinothurioida
Infraclass Acroechinoidea
Cohort Diadematacea
Order Diadematoida
Family Diadematidae
Genus Centrostephanus
Genus Diadema
Cohort Echinacea
Superorder Stirodonta
Order Phymosomatoida
Family Arbaciidae
Genus Arbacia
Superorder Camarodonta
Order Echinoida
Family Echinidae
Genus Echinus
Genus Loxechinus
Genus Paracentrotus
Genus Psammechinus
Family Echinometridae
Genus Anthocidaris
Genus Colobocentrotus
Genus Echinometra
Genus Evechinus
Genus Heliocidaris
Family Strongylocentrotidae
Genus Hemicentrotus
Genus Strongylocentrotus
Family Toxopneustidae
Genus Lytechinus
Genus Pseudoboletia
Genus Pseudocentrotus
Genus Toxopneustes
Genus Tripneustes
Cohort Irregularia
It is apparent that the only thing common to all these sea-urchin species is that they are
edible. They differ greatly in their biology and ecology. These characteristics include not only
their anatomy and morphology, but their growth rate, reproduction, and longevity (Lawrence
1990; 1991; Lawrence and Bazhin 1998). Understanding the biology and ecology of the sea
urchins is not merely of basic scientific interest. It is necessary to know the effect of removal of
immense numbers of sea urchins from the sea bottom. Similarly it is impossible to adequately
manage the fishery without understanding the biology and ecology of the species involved.
Knowledge of the ecology and biology of the species is also important as they will set the
requirements for aquaculture.
ACKNOWLEDGMENT: Preparation of this article was supported in part by Florida Sea Grant
NA76RG09120 to JML.
REFERENCES
Bustos R E, Godoy A C, Olave M S, Troncoso T R (1991) Desarrollo de t6cnicas de produci6n
de semillas y repoblaci6n de recursos bent6nicos. Instituto de Fomento Pesquero, Santiago
California Sea Grant College. 1992. The management and enhancement of sea urchins and other
kelp bed resources: a Pacific rim perspective. California Sea Grant College, University of
California, La Jolla. Report No. T-CSGCP-028
Hagen NT (1996) Echinoculture: from fishery enhancement to closed cycle cultivation. World
Aquaculture. December. 6-19
Keesing JK, Hall KC (1998) Review of harvests and status of world sea urchin fisheries point
to opportunities for aquaculture. J Shellfish Res "71 1505-1506
Lawrence JM (1975) The relationships between echinoids and marine plants. Ocean Mar Biol
Ann Rev 13:213-286
Lawrence JM (1990) The effect of stress and disturbance on echinoderms. Zool Sci 7:17-28
Lawrence J (1991) Analysis of characteristics of echinoderms associated with stress and
disturbance. In: Yanagisawa T, Yasumasu I, Oguro C, Suzuki N, Motokawa T (eds) Biology
of Echinodermata. AA Balkema, Rotterdam, pp 11-26
Lawrence JM, Bazhin A (1998) Life-history strategies and the potential of sea urchins for
aquaculture. J Shellfish Res 17:1515-1522
Lawrence JM, Sammarco PW (1982) Effects of feeding: Echinoidea. In: Jangoux M, Lawrence
JM (eds) Echinoderm nutrition. AA Balkema, Rotterdam, pp 499-519
Le Direac'h J-P (1987) La p~che des oursins en M6diterran6e: historique, techniques, 16gislation,
production. In: Boudouresque CF (ed) Colloque international sur Paracentrotus lividus et
les oursins comestibles. GIS Posidonie, Marseille, pp 335-362
Lesser MP, Walker CW (1998) Introduction to the special section on sea urchin aquaculture. J
Shellfish Res 17:1505-1506
Lewis J (1962) Notes on the Barbados 'sea egg'. J Barbados Mus Hist Soc 29:79-81
Matsui I (1966) Uni no zoshoku. Nihon Suisan Shigen Hogo Kyokai. (The propagation of sea
urchins. Fish Res Bd Canada Trans Ser No. 1063
Mottet MG (1976) The fishery biology of sea urchins in the family Strongylocentrotidae.
Washington, Dept Fisheries. Tech Rept No. 20
Saito K (1992a) Sea urchin fishery of Japan. In: Anonymous. The management and enhancement
of sea urchins and other kelp bed resources: a Pacific rim perspective. Califomia Sea Grant
College, La Jolla. Rep. No. T-CSGCP-028
Saito, K (1992b) Japan' s sea urchin enhancement experience. In: Anonymous. The management
and enhancement of sea urchins and other kelp bed resources: a Pacific rim perspective.
California Sea Grant College, La Jolla. Rep. No. T-CSGCP-028.
Scheibling RE, Mladenov PV (1987) The decline of the sea urchin, Tripneustes ,susocirtnev
fishery of Barbados: a survey of fishermen and consumers. Mar Fish Rev 49:62-69
Sloan NA (1985) Echinoderm fisheries ofthe world: a review. In: Keegan BF, O'Connor B.D.S.
(eds) AA Balkema, Rotterdam, pp 109-124
Smith A (1984) Echinoid palaeobiology. George Allen and Unwin, London
V~quez JA, Guisado C (1992) Fishery of sea urchin (Loxechinus albus) in Chile. In:
Anonymous. The management and enhancement of sea urchins and other kelp bed resources:
a Pacific rim perspective. California Sea Grant College, La Jolla. Rep. No. T-CSGCP-028
Edible Sea Urchins: Biology and Ecology
Editor: John Miller Lawrence
(cid:14)9 2001 Elsevier Science B.V. All rights reserved.
Reproduction of sea urchins
C.W. Walker ,*~ .T Unuma ,b N.A. McGinn ,~ L.M. Harrington a and M.P. Lesser a
aDepartment of Zoology, Center for Marine Biology and Marine Biomedical Research
Group, University of New Hampshire
Durham, New Hampshire 03824, USA
lanoitaNb Research Institute of Aquaculture
Nansei, Mie 516-0193, napaJ
Corresponding author: Office phone (603) 862-2111; FAX (603) 862-3784; e-mail:
[email protected]
I. INTRODUCTION
Gametogenesis and intra-gonadal nutrient storage and utilization are linked processes in
sea urchin reproduction. These processes involve the two cellular populations that make up
the germinal epithelium of the sea urchin gonad. Uniquely, sea urchin gonads grow ni size
not only because gametogenesis increases the size and/or numbers of germinal cells present
but also because somatic cells within the germinal epithelium, the nutritive phagocytes, store
extensive nutrient reserves before gametogenesis begins. Knowledge of these phenomena has
lead to successful manipulation of sea urchin reproduction. A thorough understanding of sea
urchin reproduction will provide increased opportunities for aquaculture.
.2 STRUCTURE OF THE GONADS OF THE SEA URCHIN
Branches of the genital coelomic and hemal sinuses (Hamann 1887; Campbell 1966;
Strenger 1973; Walker 1982; Pearse and Cameron 1991) interconnect all five gonads of sea
urchins. These sinuses project from similar components of the axial complex underneath the
madreporite (Figure 1 .)a Five branches penetrate the aboral connective tissues and one enters
each of the five gonads. A single gonoduct emerges from all five of the gonads. Each of these
gonoducts extends for a substantial distance within the branches of the aboral coelomic sinus
before exiting the test through a pentagonal array of gonopores in genital plates surrounding
the anus.
erugiF la. Diagrammatic representation of the sea urchin reproductive system in aboral
side view. Abbreviations: A - anus; GL - gonadal lumen; M - madreporite; TF - tube feet;
Figure lb is shown in miniature in the gonad facing the viewer; after Strenger (1973).
In both sexes, the structure of the gonadal wall of sea urchins is similar to that seen in sea
stars and brittle stars (Walker 1979; 1982; Shirai and Walker 1988; Pearse and Cameron
1991). Two sacs of tissues (outer and inner) compose the gonadal wall. Each consists of
several characteristic layers (Figure l b). Throughout the gonad, the genital coelomic sinus
(GCS) separates the outer sac from the inner sac. The outer sac includes a visceral
peritoneum (VP) that may concentrate nutrients tfh~eo m pedvisceral coelomic fluid and that
is attached to a connective tissue layer (CTL). Epithelial cells which apparently are not
muscular are also attached to the connective tissue layer on its opposite surface toward the
GCS. The inner sac is a genital hemal sinus (GHS) which bears longitudinally arranged,
flagellated muscle cells on its outer face like the gonads of sea stars (Walker 1979; 1982).
These muscles contract rhythmically during gamete release (Okada et .la 1984; Okada and
Iwata 1985) in response to the carbohydrate portion of a glycoprotein produced in the
intestine and stored in the aboral hemal tissues (Takahashi et al. 1990; 1991). Interconnecting
nerves synchronize the activities of the gonads during spawning. On its luminal face, the
GHS supports the germinal epithelium. The principal functions of the inner sac are
gametogenesis and nutrient storage. Contents of GHS vary during the gametogenic cycle.
Prior to and during gametogenesis, the GHS fills with PAS-positive glycoproteins, although
not as extensively as does the GHS of sea stars at a similar time during gametogenesis
(Walker 1979; 1982; Beijnink et al. 1984; Byme et al. 1998).
Figure lb. Diagrammatic representation of the tissues in the sea urchin gonadal wall.
Abbreviations: CTL - connective tissue layer; NP - nutritive phagocytes; GCS - genital
coelomic sinus; GHS - genital hemal sinus; VP - visceral peritoneum.
Severing the radial connections between the gonad and the aboral coelomic and hemal
branches (Okada 1979) prevents gonadal development and gametogenesis. In very small
Lytechinus pictus, the aboral hemal sinus has five radial extensions (Houk and Hinegardner
1980). These expansions of the hemal sinus become the inner sac and force surrounding
connective tissue into the form of the outer sac of each gonad. Expansions of the hemal sinus
contain precursors for somatic and gonial cells of the developing germinal epithelia. Both of
these precursor cell types are filled with yolk-like contents within membrane-bound vesicles
and may be recognized in the echinopluteus before metamorphosis. Very small females may
have recognizable oogonia, but oogenesis does not occur. Very small males may contain a
few differentiated spermatozoa. The testes of .S purpuratus produce spermatozoa within the
first twelve months of life (Cameron et al. 1990).
3. SEA URCHIN GAMETOGENIC AND NUTRITIVE PHAGOCYTE CYCLES:
STAGES, PHYSIOLOGY AND MOLECULAR BIOLOGY
3.1. Stages in the reproductive cycle
During the annual reproductive cycle, gonads of both sexes of the sea urchin pass through
a characteristic series of structural changes (Walker 1982; Pearse and Cameron 1991; Walker
et al. 1998). These changes can be classified according to the activities of the two major
populations of cells that compose the germinal epithelium. These cellular populations are
either: a) germinal cells (oogonia -> fully mature ova in the ovary or spermatogonia -> fully
differentiated spermatozoa in the testis); or b) somatic cells called nutritive phagocytes (NP)
and present in both sexes (Caullery 1925; Holland and Giese 1965; Holland and
Holland, 1969; Kobayashi and Konaka, 1971).
It is important to recognize that the size of sea urchin gonads does not necessarily relate
to the progress of gametogenesis alone. One must very carefully consider the stage of
gametogenesis that characterizes a particular individual in order to determine what cellular
population (germinal or somatic) actually predominates ni size and/or numbers within its
germinal epithelium (Walker et al. 1998).
Changes in the germinal epithelium of the sea urchin gonad have been described using
the staging systems of Fuji (1960 a, b) based on germinal cells and of Nicotra and Serafmo
(1988) based on nutritive phagocytes (NP) (Unuma et .la 1998, 1999; Byrne 1990; Meidel
and Scheibling 1998; Walker and Lesser 1998; Walker et .la 1998; Han'ington 1999). A valid
staging system must simultaneously consider both populations of cells and provide the basis
for a cellular understanding of gametogenesis. We employ the following stages: a) Inter-
Gametogenesis and NP Phagocytosis, b) Pre-Gametogenesis and NP Renewal, c)
Gametogenesis and NP Utilization and d) End of Gametogenesis, NP Exhaustion and
Spawning (Figure 2 for ovaries and 3 for testes). For color images and additional
information see the Web page: Normal and Manipulated Green Sea Urchin Gametogenesis -
~ttp ://zoology,unh.edu/f~u. lty/walker/urchin/gametogenesis.html)
3.2. later-gametogenesis and NP phagoeytosis
As the inter-gametogenesis and NP phagocytosis stage begins, NP are at their smallest
size for the year, following the mobilization and release of most of the nutrients that they
originally contained (Figures 2a, 3a). NP may still may have membrane-bound vesicles that
are empty or are filled with uniform or varying granular contents (Takashima 1968; Masuda
and Dan 1977; Nicotra and Serafmo 1988). Basally near the luminal face of the inner sac of
the gonad, these cells cover amitotic oogonial cells that will participate in the next
gametogenic event. Ovaries also contain: Residual primary oocytes between the NP and fully
mature ova within the ovarian lumen (Figure 2a). In the testes, residual spermatozoa remain
in the testicular lumen, and amitotic spermatogonia occur as individual or small clusters of
cells at the bases of the NP (Figure 3a, arrow; Nicotra and Serafino 1988). In gonads of both
sexes, luminal extensions of the depleted NP phagocytize residual gametes (Fuji 1960a, b;
Cruz-Landim and Beig 1976; Masuda and Dan 1977). Based on the high level of acid
phosphatase activity in residual oocytes, Masuda and Dan (1977) suggested that residual
fully mature ova are autolytic, digesting their own contents and thus reducing their size prior
to being phagocytised by NP. It is unclear why residual oocytes begin autodigestion. In both
sexes, variable numbers of residual gametes may still be present within the germinal
epithelium in the early months of the following pre-gametogenesis and NP renewal stage.
The inter-gametogenesis and NT phagocytosis stage begins late during or after the
spawning of most fully mature ova and spermatozoa and seems to be under the control of the
NP. These versatile cells organize the microenvironment for germinal cells throughout
gametogenesis (Walker 1979; Walker 1982). NP have multiple functions. Basally, they
protect amitotic oogonia and spermatogonia (Anderson 1968; Walker et al. 1998); laterally,
Figure 2: Stages in the annual reproductive cycle of female sea urchins, a) Inter-Gametogenesis
and NP Phagocytosis; b) Pre-Gametogenesis and NP Renewal; e) Gametogenesis and NP Utilization;
:d End of Gametogenesis, NP Exhaustion and Spawning. Abbreviations: C - coelom; RFMO - residual
fully mature ovum; NP- nutritive phagocyte; RPO- residual primary oocyte; circles indicate ovarian
wall; arrows show amitotic oogonia; inset shows oogonia mitosis (arrow). Scalebar = 50~tm