Journal of Experimental Marine Biology and Ecology 342 (2007) 191 201

www.elsevier.com/locate/jembe

Brooding in echinoderms: How can modern experimental techniques

add to our historical perspective?
Jean M. Gillespie, James B. McClintock
Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama, 35294-1170, United States
Received 25 August 2006; received in revised form 25 September 2006; accepted 30 October 2006

Abstract
Echinoderms are among the most abundant and ecologically successful groups of marine animals on earth. Their unique
adaptations have enabled them to inhabit diverse environments ranging from various substrates in shallow water habitats to the
benthos of the deepest seas. Although members of the Echinodermata generally share common characteristics including radial
symmetry, a unique water vascular system, and decentralized cephalization, they have evolved a variety of life history strategies
that enable them to reproduce successfully across a wide range of habitats. These reproductive strategies range from a complete
lack of parental care (broadcasting) to internal and external brooding of the eggs, embryos, and juvenile phases. Although brooding
is relatively rare in echinoderms, it is of interest as a deviant or derived form of reproduction that has been the subject of much
study and debate. The aim of the present review is to examine how and why brooding occurs from a historical perspective, and then
explore how modern experimental techniques are providing novel approaches to answering fundamental questions related to
brooding in this very successful group of benthic marine invertebrates.
2006 Published by Elsevier B.V.
Keywords: Brooding; Echinodermata; Life history evolution

Contents
1.
2.
3.

Trade-offs in reproductive strategies . . . . . .

Evolution of brooding in echinoderms . . . . .
Taxonomic survey of brooding in echinoderms
3.1. Asteroidea . . . . . . . . . . . . . . . .
3.2. Holothuroidea . . . . . . . . . . . . . .
3.3. Ophiuroidea . . . . . . . . . . . . . . .
3.4. Echinoidea . . . . . . . . . . . . . . .
3.5. Crinoidea . . . . . . . . . . . . . . . .

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Corresponding author. Tel.: +1 205 975 2525; fax: +1 205 975 6097.
E-mail address: mcclinto@uab.edu (J.B. McClintock).
0022-0981/$ - see front matter 2006 Published by Elsevier B.V.
doi:10.1016/j.jembe.2006.10.055

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J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201

4. Future research and the role of modern techniques in addressing important questions . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Trade-offs in reproductive strategies

Reproduction in echinoderms can be divided into
three discrete modes based on the nutritional and feeding
patterns of embryos or larvae and whether they are, or are
not, released in to the water column (Menge, 1975;
McEdward, 1995; Poulin et al., 2002). These three
reproductive modes, planktotrophic, pelagic lecithotrophic and non-pelagic lecithotrophic, involve tradeoffs in terms of parental investment, fecundity, and
offspring mortality and dispersal, and development time
all of which influence potential reproductive success.
Planktotrophic larvae are produced by the spawning of
eggs and sperm directly into the water column, where
external fertilization occurs. Zygotes develop into freeswimming ciliated larvae that generally feed on
phytoplankton (Menge, 1975; Giese et al., 1991),
although absorption of dissolved organic material
(DOM) may supplement nutrition (Manahan et al.,
1983; Manahan, 1990; Shilling and Manahan, 1990,
1994; Shilling and Bosch, 1994). Adults that produce
planktotrophic larvae are referred to as broadcast
spawners and typically release millions of eggs in a
single spawning event (Giese et al., 1991). While
planktotrophic larvae have the advantage of wide
dispersal capabilities, the larvae experience high mortality as a group due to a variety of biotic and abiotic
factors (Young and Chia, 1987; Lawrence and Herrera,
2000; Poulin et al., 2002).
Pelagic lecithotrophic larvae are also produced by
external fertilization. However, lecithotrophic larvae are
derived from comparatively large, yolky eggs and derive
their nutrition from lipids, proteins and carbohydrates
stored in the egg itself, rather than from exogenous
sources such as phytoplankton or DOM. This nutritional
provisioning of the young can be considered an indirect
form of parental care (Lawrence and Herrera, 2000) and is
more energetically costly on a per egg basis to the adult
than broadcast spawning (Jaeckle, 1995), with the result
that fewer eggs are produced per spawning. One
advantage is that larger egg size translates into larger
juvenile size and thus, presumably lowers juvenile
mortality (Lawrence et al., 1984; Hendler and Tran,
2001; Bingham et al., 2004). Another advantage is a
reduction in development time as shown by Levitan
(2000) who describes an inverse proportional relationship
between egg size and development time for 37 species of

197
199
199

echinoids. Although the pelagic life style has the

advantage of increased dispersal, there is a trade-off for
lecithotrophs in terms of a higher risk of mortality due to
large, conspicuous, nutrient-rich larvae. However, in
some echinoderms and other benthic marine invertebrates
large lecithotrophic eggs, embryos and larvae have
evolved chemical defenses (McClintock and Baker,
1997a,b; Lawrence and Herrera, 2000). Such chemical
defenses provide benefits in terms of increased protection
but may raise parental investment due to increased
metabolic costs associated with provisioning eggs with
defensive secondary metabolites (McClintock et al.,
2001). For example, echinochrome found in the eggs of
some sea urchins has been suggested to be related to
chemical defenses (J.M. Lawrence, pers. comm.).
The third mode of reproduction is the production of
non-pelagic lecithotrophs which, in most echinoderm
species, are brooded by the parent. In this case, the
trade-off is the production of far fewer eggs requiring a
very high parental investment per egg, but with high
survival rates due to the protection afforded directly by
the parent. It should be noted that in contrast to pelagic
lecithotrophs, not all eggs brooded by echinoderms are
necessarily large (Turner and Dearborn, 1979; Walker
and Lesser, 1989). In such instances there is a necessity
for supplemental nutrition likely via the absorption of
DOM (Fontaine and Chia, 1968), perhaps facilitated in
some instances by endosymbiotic bacteria present under
the cuticles of embryonic tissues (Walker and Lesser,
1989). During the brooding process, the parent may
provide mechanisms for cleaning of the embryos, a
uniform environment, assistance in hatching, and
protection from predators and inhospitable conditions
including desiccation and harmful UV radiation (Chia,
1966; Hamel and Mercier, 1995). Brooding also raises
the probability that juveniles will recruit to suitable
habitats (Engstrom, 1982). In some echinoderm species,
parental care is elevated to matrotrophy (direct feeding
of the young from the female's body) (McClary and
Mladenov, 1990; Frick, 1998; Hendler and Tran, 2001).
In other echinoderms, juveniles may acquire nutrients
by feeding on smaller individuals in the same brood, a
process known as adelphophagy (Byrne, 1996; also see
Bosch and Slattery, 1999), or by consuming unfertilized
nurse eggs (Turner and Dearborn, 1979; Sewell and
Chia, 1994). Ultimately, this nutrition is similarly
provisioned by the parent via gametogenesis. Additional

J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201

costs of parental care that may be incurred by some

species include an elevated risk of predation to a
sedentary adult (Engstrom, 1982; Bosch and Slattery,
1999), the inability of the parent to feed during the
period of brooding, which may lead to reduced
survivability of the adults or reduced fecundity due to
longer reproductive cycles (Chia, 1966; Bosch and
Slattery, 1999), and as mentioned above, the increased
cost of allocating chemical defenses to eggs (McClintock and Baker, 1997b; McClintock et al., 2001). In
summary, there is essentially a continuum in echinoderm reproductive strategies ranging from the production of many small eggs with low parental investment
and no parental care, to smaller numbers of generally
yolky eggs that represent a high level of parental
investment per offspring and which therefore, may be
protected by chemical defenses and/or by brooding
(Byrne, 1996; Bosch and Slattery, 1999; Lawrence and
Herrera, 2000).
2. Evolution of brooding in echinoderms
From an evolutionary perspective planktotrophic
larvae are believed to represent the primitive condition
in the Echinodermata (Strathmann, 1985; Havenhand,
1993). Much research and debate has focused on the
selection pressures that would result in the derived
condition of parental brooding. In general, parental care
would be expected to evolve when ecological conditions
are such that the benefits exceed the costs for the
individual parent (Alcock, 1979). E.O. Wilson (from
Trumbo, 1996) proposed four prime movers that
would lead to the evolution of parental care: 1) a stable,
structured environment, 2) a harsh environment, 3) a
scarce, specialized food resource, and 4) high predation
pressure. Due to the complexity of parental care, it is
often hard to identify a single driving agent for selection
(Trumbo, 1996). However, considerable emphasis has
been placed on the idea that a harsh environment has led
to the evolution of brooding in echinoderms, in part
because of Thorson's Rule (see Young, 1994; Pearse,
1994). Based on the hypothesis that the incidence of
non-pelagic reproductive modes increases with latitude,
Thorson's Rule has its roots in observations made over a
century ago during the Challenger oceanographic
expeditions (18721876). Brooding in echinoderms
was a topic of special interest to Wyville Thomson, the
director of the Challenger expeditions (Young, 1994).
The subsequent paper Thomson wrote on brooding
echinoderms (Thomson, 1878) was quoted extensively
in Volume 1 of The Challenger Reports, which was
widely read in the popular and scientific literature. Due

193

to Thomson's biased presentation of information, the

conclusion was drawn that a brooding habit dominated
modes of reproduction in Antarctic echinoderms. In
addition, Alexander Agassiz perpetuated this assumption because he wrongly concluded that among the
echinoids collected by the Challenger, the presence of
large gonopores meant the production of large eggs and
that this in turn necessarily equated to a brooding habit.
Based on this information coupled with his own
observations on marine invertebrate reproduction in
the cold northern seas surrounding Greenland, Gunnar
Thorson proposed an inverse correlation between
pelagic development and latitude (Thorson, 1950). He
then extended this rationale to the deep-sea, relating the
many similarities in adaptations of marine benthic
invertebrates found in polar waters and the deep-sea.
These trends became entrenched over time and
ultimately deemed an ecological rule (Young, 1994).
Attempting to interpret this trend, reproductive biologists and larval ecologists construed the harsh environmental conditions as a mechanism to explain the
preponderance of brooding (Pearse, 1994). Polar
regions are typified by low, but relatively stable, water
temperatures, a short period of primary and secondary
production, fluctuations in salinity, storms and the
effects of ice, all of which create harsh conditions for
larval dispersal and survival (Pearse et al., 1991; Pearse,
1994; Poulin et al., 2002). Moreover, the short period of
secondary production may have implications for
secondary production by the parent, in addition to
offspring. This could lead to low secondary production
in itself and could be a selective pressure for direct
development (JM Lawrence, pers. comm.). Thorson
himself proposed that pelagic larvae would be selected
against in deep sea echinoderms because of the
challenges of thousands of meters of vertical migration
within the water column during periods of postembryonic and larval development followed by an
equally challenging return to the benthos to settle and
metamorphose (Young, 1994; Pearse, 1994).
The applicability of Thorson's rule across all classes of
echinoderms has been called into question following
studies documenting reproductive modes through larval
culture and plankton sampling (Pearse et al., 1991; Pearse,
1994; Poulin and Fral, 1996). What Thorson had no way
of knowing is that there are, indeed, a preponderance of
high latitude echinoderm species that produce large
lecithotrophic eggs, but that in some higher taxa, including
the Asteroidea, pelagic lecithotrophy is not uncommon
(Pearse et al., 1991; Pearse, 1994). Thorson's Rule
may have more relevance for the Echinoidea, a group
that displays a high incidence of brooding in polar

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J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201

environments. Poulin et al. (2002) suggests that in

Antarctica this may be the result of selective extinction
of many planktotrophic species during past glacial
episodes. They conjecture that during past glacial periods
permanent sea-ice eliminated phytoplankton as a food
source for planktotrophic species while lecithotrophic
species that evolved when Antarctica had a more
temperate climate were able to survive. Speciation
among these remaining taxa may explain the disproportionate number of brooding echinoids in the Antarctic.
With the reduction in sea-ice cover in contemporary
Antarctica, species of echinoids with planktotrophic
larvae have become ecologically dominant, although
they remain numerically inferior (Poulin and Fral, 1996;
Poulin et al., 2002).
Lawrence and Herrera (2000) hypothesize that
stress plays a role in the evolution of brooding in
echinoderms. They emphasize the importance of the
transfer of energy from the parent to the offspring and
define stress as anything that limits the animal's ability
to invest energy into reproduction. The hypothesized
result of such stress is considered a deviant or
derived form of reproduction, such as brooding, that
has the effect of increasing reproductive success.
Lawrence and Herrera (2000) provide support for their
hypothesis by highlighting deviant reproductive strategies in unrelated taxa that experience stress (convergent
evolution). A second line of support is derived from
cases of divergent evolution whereby certain taxa
experiencing stress exhibit deviant reproduction unlike
related taxa lacking stress. Stress, as defined above, may
be caused by low temperature or restricted food
availability as seen in cold water and deep-sea habitats,
but may also be linked to predation and the constraints
of small body size on nutrient procurement. Small body
size in echinoderms has been shown to be correlated
with a brooding habit (Strathmann and Strathmann,
1982; Pearse et al., 1991). For example, in a study of
two sympatric sea stars in the rocky subtidal of the
Pacific Northwest, Menge (1975) proposed that competition for food played a role in the evolution of
brooding in the smaller, less competitive, species. He
speculated that juvenile mortality was sufficiently high
so as to prevent the smaller nutrient-limited sea star from
producing the numbers of offspring necessary to replace
itself through a broadcasting mode of reproduction.
3. Taxonomic survey of brooding in echinoderms
Brooding is known to occur in the five major classes
of the Echinodermata. A sixth class (but see Janies and
Mooi, 1999), the Concentricloides, with only three

species identified to date, occur in exclusive association

with log falls in the deep sea (Baker et al., 1986; Voight,
2005). These are brooders with intraovarian embryonic
development, although one species, Xyloplax turnerae,
has been shown to have oviparous development with
embryos developing outside of the ovary (reviewed in
Mah, 2006).
3.1. Asteroidea
Brooding in sea stars was first documented in the mid1800's. Members of the orders Spinulosida and Forcipulata have similar methods of positioning their egg
masses during brooding. The female arches the central
disk until it forms a concavity orally and then bends her
arms ventrally to form a brooding chamber in which the
eggs are held (Hyman, 1955; Chia, 1966). In the brooding
sea star Leptasterias hexactis (Order Forcipulata),
development takes about 40 days, at which time brooded
juveniles employ their newly developed tube feet to attach
to the substratum (Chia, 1966). Females stay with the
juveniles for approximately another 10 days. During the
brooding period, females do not feed and display a latent
period of two days before initiating feeding if the brooded
egg mass is artificially removed. Brooded eggs fail to
hatch when removed from females suggesting that the
female produces a substance, possibly an enzyme, that
may weaken the fertilization membrane of the eggs. Chia
(1966) also found that female adults who were not
brooding would pick up and attempt to brood artificial
embryo masses, as long as the masses had sticky surfaces
similar to natural egg masses. Non-sticky artificial egg
masses of the correct size and color were rejected, even
after being treated with a homogenate of embryos,
suggesting that the physical structure of the eggs is the
most important cue for the adult female to accept an egg
mass. That egg masses failed to develop in the absence of
the brooding parent also suggests that maternal nutrient
transfer might be important to embryonic development.
There is histological evidence for nutrient translocation in
the brooded juveniles of the sea star Pteraster militaris
(McClary and Mladenov, 1988).
Leptasterias polaris is one of the largest species of
brooding sea star (a rare exception to the generally small
adult body sizes of brooding sea stars), attaining a radius
of up to 25 cm (Hamel and Mercier, 1995). Males and
females aggregate prior to spawning, an adaptation likely
to ensure higher rates of fertilization as females retain
eggs under the central disk at all times. Aggregation may
be initiated by decreasing environmental temperatures
and facilitated by chemoreception. Males initiate
spawning, by releasing sperm that sinks to form a sticky

J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201

layer on the surrounding benthos. The sperm remains in a

state of inactivity until reactivation via contact with the
female's oocytes. Females brood fertilized eggs under
the central disk with their arms curved in a pinwheel
fashion in a plane parallel to the substrate surface.
Juvenile sea stars require an extensive time period of up
to six months to fully develop. In contrast to L. hexactis
(Chia, 1966), manipulations revealed that developing
embryos of L. polaris could develop in the absence of a
parent female (Hamel and Mercier, 1995).
In other species of sea stars, brooding is even more
derived with juveniles being held and maintained within
the female's body. In Asterias groenlandica, the developing embryos are held in pouches of the cardiac
stomach (Lieberkind, 1920). Two Australian species of
Parvulastra (formerly Patiriella) incubate their eggs
within the gonads and then release juveniles via the
gonopore, a rare mode of brooding in sea stars (Byrne,
1996). Juveniles are initially about the same size, but
intraspecific predation among juveniles ultimately results
in a size differential within the brood. Juveniles positioned
on the aboral side of siblings are more successful
cannibals and ultimately have higher survival rates.
Byrne (1996) found evidence of stomach duels between
brooded juveniles while inside the parent gonad whereby
juveniles would position themselves with their oral
surfaces facing one another, each with cardiac stomach
extruded, in an attempt to keep the other off of its aboral
surface. Byrne et al. (2003) and Byrne (2005) also report
intragonadal development in the sea star Cryptasterina
hystera unique in its highly derived life history.
Individuals possess ovitestes and embryos develop into
fully functional brachiolaria that swim in the gonadal fluid
before ultimately being released as juveniles that emerge
from the aboral gonopore. Similarly, the diminutive sea
stars Parvulastra vivipara and P. parvivipara (the world's
smallest known sea star) have intragonadal development
that is thought to be atypical and is proposed to have
involved the evolutionary retention of a large egg by an
ancestor that had lecithotrophic brachiolaria followed by a
secondary reduction in size of the ovum and simplification of the larva (Byrne and Cerra, 1996).
Some sea stars brood their young on the aboral surface
of the body wall. For example, the spinulosid asteroids of
the family Pterasteridae brood their young in a
nidamental chamber located between the aboral body
wall and the supradorsal membrane (Hyman, 1955). The
brooding chamber is supported by crowns of paxillae.
Brooded embryos are aerated by ciliary pumping of water
through the chamber. Because the nidamental chamber is
also well-developed in males, Hyman (1955) suggests
that use of the chamber for brooding evolved secondarily

195

to the primary function of respiration. Among the Phanerozonid asteroids, there are some species that brood, but
the stiffness of their body wall and arms precludes the
formation of brood chambers. Instead, the young are
brooded on the aboral body wall surface amongst the
paxillae (Hyman, 1955). As the embryos develop, the
paxillae are pushed to the side forming a depression in
which juveniles develop. Remarkably, McClary and
Mladenov (1988) report that P. militaris broadcasts a
portion of their eggs and retains the balance in an aboral
brood chamber bounded by a membrane supported above
the body wall by the aboral paxillae.
3.2. Holothuroidea
Sea cucumbers exhibit a wide range of brooding
habits, from those that simply cover their developing
offspring with their ventral body wall, to those that
brood their young within the gonads (Hyman, 1955).
Cucumaria lubrica, found in the Pacific Northwest,
broods its young externally (Engstrom, 1982). When
females release eggs, vertically oriented individuals
release their grip on the substrate with two of the three
rows of tube feet such that the body is displaced away
from the substrate. Spawned eggs released from the
genital papilla accumulate on the ventral body wall
surface. The female then reattaches to the substrate,
covering the eggs with her body and remaining stationary throughout the brooding period. Males typically
spawn at midday and females subsequently at dusk. This
allows eggs to be spawned at a time when predation by
visual predators is presumably lower, while sperm has
already had time to settle on females and to be in place
when the eggs are spawned (Engstrom, 1982). A more
complex brooding habit is seen among Cucumaria,
Psolus and Thyonepslus spp. As they are spawned, eggs
are actively collected with the oral tentacles or
specialized tube feet and transported to external body
wall pits or depressions. Progressively more elaborate
forms of brooding include the retention of developing
young in invaginations of the body wall, or within the
coelom or gonads (Hyman, 1955). How fertilization
occurs in dioecious incubating species is unclear but may
be explained by movement of sperm through the
gonopore (Sewell and Chia, 1994). Developing young
within the coelom have been shown to exhibit
matrotrophy as evidenced by (1) a hundred-fold increase
in juvenile size from the original egg size, (2) documentation of feeding behaviors (tentacle stuffing) by
juveniles within the coelom, and (3) the presence of
labeled nutrients in the juvenile gut following injection
into the parent's coelomic fluid (Frick, 1998).

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J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201

3.3. Ophiuroidea
While much remains to be learned about the larval
development in the Ophiuroidea, of the seventy known
brooding species, only thirteen are known to be
gonochoric (Hendler and Tran, 2001). This strong
correlation between hermaphrodism and brooding has
yet to be adequately explained (but see Strathmann and
Strathmann, 1984; Leonard, 2006). Hendler and Littman
(1986) noted that among 33 species of brittlestars they
examined for modes of reproduction from the Belize
Barrier Reef, most brooding species had relatively small
adult body sizes. Most brittle stars have sac-like
invaginations (bursae) that open on the oral side of the
central disc near the arm bases. In non-brooding species,
mature gametes simply pass from the gonads through
the bursae and out through the bursal slits. In brooding
ophiuroids, gametes remain within the bursae which
serve as a brooding pouch or the gametes develop in
sacs that extend from the bursae (Hyman, 1955).
Hendler (1991) has described two types of brooding in
ophiuroids: sequential brooding, in which brooded
juveniles develop with others in the same age cohort,
and simultaneous brooding, in which brooded juveniles
occur in several age cohorts within the parent at the
same time. Hendler and Tran (2001) suggest this initial
distinction may be overly simplistic. They found that the
deep sea ophiuroid Amphiura carchara tends to brood
only one developmental stage at a time, but can brood
different stages simultaneously, usually in different
bursae. Moreover, Hendler and Tran (2001) found
evidence for matrotrophy in A. carchara. Here, almost
all late-stage juveniles were positioned with their
mouths and arms pressed against the bursal wall,
suggesting that juveniles acquire some of their nutrients
from the mother's body. Turner and Dearborn (1979)
found a 100,000 fold increase in the organic content
from egg to the largest juvenile stage in the brooding
Ophionotus hexactis and suggest that maternal nutrient
transfer via nurse eggs and parental fluids must account
for this dramatic increase. Similarly, the remarkably
small brooded eggs (only 100 m diameter) of the
diminutive viviparous brittlestar Amphipholis squamata
depend on the absorption of DOM to supplement their
nutritional requirements (Fontaine and Chia, 1968).
3.4. Echinoidea
The echinoids are among the best studied of all
invertebrates with regard to their reproduction and
embryonic and larval development. According to Emlet
et al. (2002), brooding is thought to have evolved

independently at least fifteen times, with about 7% of

the approximately 900 known extant species exhibiting
this reproductive mode. However, Poulin and Fral
(1996) put the number of brooding species at 20% of all
extant echinoids and as high as 72% for known coastal
Antarctic species. Brooding is common in the regular
echinoid order Cidaroidea and the irregular echinoid
order Spatangoida (Hyman, 1955). Cidaroids typically
brood their direct developing young on the peristomial
membrane surrounding the mouth or in the vicinity of
the periproct (anus). The region in which the young
develop may be depressed and spines of the parent may
criss-cross over the young to facilitate protection and
retention. In the spatangoids, or heart urchins, the young
are brooded in deepened petalloids located aborally
(Hyman, 1955).
Brooding in Antarctic echinoids has attracted interest
for a considerable period of time and recent advancements in research capabilities have facilitated increased
attention (Pearse et al., 1991; Young, 1994). The genera
Abatus and Amphipneustes are well-known for their
brooding habit. Pearse and McClintock (1990) studied
two species of Abatus in McMurdo Sound, Ross Sea,
Antarctica, and found some similar and some dissimilar
adaptations in these echinoids that occur in contrasting
habitats. They found that more than 60% of the females
of both species were brooding during the late austral
spring and early austral summer. They also found that
females of both species simultaneously brooded embryos at different stages of development. Histological
observations of gonads indicated the presence of oocytes
at varying stages of development. These observations
suggest that reproduction is continuous in both A.
shackletoni and A. nimrodi. The time required for
oogenesis is probably several years and the time period
to complete posts-spawn brooding at least 8 months,
which is in keeping with many other slow growing polar
marine invertebrates (Pearse et al., 1991). There were
some differences between A. nimrodi and A. shackletoni.
Adults and juveniles of A. nimrodi are larger than those
of A. shackletoni. The authors suggest that the larger
adults of A. nimrodi may facilitate maintenance of the
population even though juvenile mortality is high in the
oligotrophic predator-rich habitat because they reproduce over a longer lifespan. In contrast, the smaller A.
shackletoni may have adapted to a habitat that supports
high turnover due to higher levels of production and
more organic input.
The Antarctic irregular sea urchin Amphipneustes
lorioli brood their young in four aboral sunken brooding
pouches, or marsupia (Galley et al., 2005). After
spawning, spines and pedicellaria transport the eggs

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into the marsupial chambers. Galley et al. (2005)

determined that there are two embryonic and four
subsequent juvenile stages present at the same time
within a given marsupium, with progressively more
immature embryos and juveniles located in the deeper
recesses of the pouch, perhaps a mechanism to reduce
crowding within the pouch. It appears that A. lorioli,
like A. nimrodi and A. shackletoni, has a continuous
reproductive pattern that may be due to a deposit feeding
mode that optimizes use of a rich food bank available
in the sediments year-round (Galley et al., 2005).
3.5. Crinoidea
Crinoids are dioecious, however, in contrast to other
echinoderms the gonads are not discrete, but rather
occur in multiplicity generally in the pinnules located
most proximal to the base of the arms (Hyman, 1955).
Two modes of brooding occur in crinoids, external and
internal. In external brooding, the eggs are released from
the gonads and stick to the genital pinnules and are
subsequently fertilized. Here they develop into doliolaria larvae that hatch from the egg envelope and then
develop as a free-swimming lecithotrophic larva (Balser,
2002). Internal brooding may occur in brood chambers,
or marsupia, which are saclike invaginations in the arms
at the base of the pinnule or in the reproductive pinnules
themselves. Eggs apparently access the marsupium via
rupture of the wall between the ovary and the
marsupium. Sperm have been observed in the genital
tube of the ovary, suggesting that the eggs are fertilized
on the way into the brood pouch (Hyman, 1955). It is
unclear how the sperm get into the female. There are
usually only a few brooded eggs per marsupium. In
some species, the brooded juveniles develop within the
female to the point that portions of the stalked young
(pentacrinoid) are visible protruding from the marsupium (Hyman, 1955). In other internal brooders, the
young develop within the ovarian lumen (Balser, 2002).
4. Future research and the role of modern techniques
in addressing important questions
Despite the fact that descriptive investigations of
brooding in echinoderms have been ongoing for well
over a century, there are still many echinoderms whose
basic life histories have yet to be documented. The
relatively recent establishment of permanent research
facilities that have state of art aquarium facilities and
that support small boat operations and scuba diving will
improve the gathering of information from Antarctica,
where among select echinoderm taxa such as the

197

Echinoidea, there exists a preponderance of brooding

species (Pearse et al., 1991; Poulin and Fral, 1996).
Furthermore, the increased sophistication of submersible and ROV technologies will facilitate studies of
brooding in deep-sea echinoderms. While brooding is
relatively rare among deep-sea species examined to
date, it has been documented in a deep sea holothurian
(Hansen, 1968) and in concentricycloids (Rowe et al.,
1988; Mah, 2006). Young (2003) speculates that future
studies are likely to reveal that brooding also occurs in
many deep-sea ophiuroids and in some deep-sea
asteroids. Only a single description of the embryos
and larvae of the exclusively deep-water stalked
crinoids, considered the most basal group of extant
echinoderms, exists (Nakano et al., 2003). Here, Metacrinus rotundus was found to possess a dipleurula-type
larva, the presumptive evolutionary progenitor for
subsequent larval forms within the phylum. Additional
studies may shed light on whether brooding occurs
among some deep-water stalked crinoids. Studies of
embryonic development in brooding deep-sea echinoderms may require unique and challenging culture
techniques. For example, employing customized stainless steel pressurized chambers, Young and Tyler (1993)
demonstrated that embryos of the planktotrophic deepsea echinoid Echinus affinis require pressures equivalent
to those that occur at 10002000 m depths for
successful development. Thus, brooding adults or
isolated brooded embryos from deep-sea echinoderms
may require innovative culture conditions that include
maintenance under high pressure.
While the field of molecular developmental biology
has greatly exploited the gametes, embryos and larvae of
planktotrophic sea urchins as model developmental
systems (Cameron et al., 2000; Vickery et al., 2001)
there is potential to build on this field of knowledge with
comparative molecular studies of direct development in
brooding echinoderms. Ferkowitz et al. (1998) used a
comparative approach to examine phylogenetic relationships and developmental expression of Wnt genes that
regulate cellcell signaling and cell pattern formation
during development in three species of sea urchins with
contrasting modes of reproduction. While none of the
sea urchins examined were brooders, Heliocidaris
erythrogrammica possesses a larva that develops
lecithotrophically from large, freely spawned eggs
(Williams and Anderson, 1975). As lecithotrophy and
brooding are generally hypothesized to be evolutionarily derived from species with a pelagic feeding larva
(Strathmann, 1985; Havenhand, 1993), future molecular
studies with echinoderms with contrasting developmental modes should shed light on this hypothesis and

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J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201

related issues such as the potential for the independent

evolution of developmental regulatory genes.
Investigation into the energetics and nutritional
requirements of development in brooded eggs, embryos,
and juveniles in echinoderms poses a number of
significant challenges. Foremost are the likely difficulties inherent in working with isolated embryos that may
possess intrinsic maternal associations during brooding.
The lack of complex chemical cues and signals of
maternal origin may offset normal metabolic developmental processes. This said, it is known that embryos
removed from at least some brooding echinoderms will
develop in the absence of the female parent (e.g., the sea
star Leptasteria polaris; Hamel and Mercier, 1995).
Assuming that brooded embryos can be removed and
worked with in isolation there are several recent novel
techniques available for measuring the metabolic rates
of individual marine invertebrate embryos and larvae.
These include the couloximetric method (Peck and
Uglow, 1990) used to measure metabolic rates in the
individual larvae of the Antarctic sea star Odontaster
validus (Peck and Prothero-Thomas, 2002). Moreover,
an optode microtiter plate technique has recently been
developed and ground truthed via measurements of
metabolic rates of individual nauplii larvae of Artemia
sp. (Szela and Marsh, 2005). This technique would have
the advantage of facilitating large numbers of individual-level measurements to accurately describe the
distribution of metabolic rate potentials within individuals comprising a brood. Such studies are likely to
contribute to understanding differences in developmental rates that are known to occur within broods of some
echinoderms. The use of defined genetic crosses has
been used recently as an elegant technique to alter
quantitative traits of interest, in this case the physiological basis of differential growth rates in a model marine
invertebrate larval system (Pace et al., 2006). In this
study crosses of adult oysters (Crossostrea gigas) were
used to generate families of larvae with different growth
rates under identical conditions, allowing an evaluation
of growth variation. Among the variables measured in
each larval family were size, biochemical composition,
rates of particulate and DOM acquisition, absorption
efficiencies, respiration rates and enzyme activities. In
the case of planktotrophic oyster larvae, half of the
energy required for faster growth was attributable to
size-associated increased feeding ability and the other
half came from a cost savings in metabolic processes
that the investigators propose to be attributable to
differences in protein depositional efficiencies. Similar
approaches could provide insights into endogenous
factors that regulate physiological processes in embryos

of brooding echinoderms. Similar to free swimming

echinoderm larvae (Manahan et al., 1983), brooded
embryos are also likely to have metabolic costs that are
met to varying extents by the uptake of DOM.
Particularly useful in evaluating the contribution of
DOM to metabolic costs in brooded embryos may be a
novel technique currently under development that will
employ antibodies to block specific amino acid transporters to facilitate measurement rates of DOM uptake from
specific membrane proteins (D.T. Manahan, pers.
comm.). It will be intriguing to compare the relative
endogenous versus maternal contribution of DOM to
metabolic demands of brooded embryos by comparing
DOM taken up directly from seawater bathing the brood
chamber to that derived from maternal sources. Ultimately, measurements of respiration and DOM uptake in
brooded echinoderm embryos will allow a determination
of developmental energy costs and budgets, although the
latter will be complicated by uncertainties in quantifying
all the potential DOM inputs.
Recent progress in molecular genetics has yielded
novel experimental approaches to explore questions
related to paternity in brooding echinoderms. Chenuil
et al. (2004) used RAPD (Random Amplified Polymorphic DNA) to evaluate paternity patterns associated
with embryos removed from a single brood of juveniles in
the common soft bottom Antarctic sea urchin Abatus
nimrodi. RAPD are dominant molecular markers that
provide a multiband pattern via polymerase chain reaction
using short random primers. Data are interpreted in terms
of the presence or absence for each fragment. Thus for a
given target fragment, heterozygotes (individuals that
inherited a copy of the fragment from only one of their
parents) are indistinguishable from homozygotes that
inherited two copies of the fragment (Chenuil et al.,
2004). Interestingly, the results of this study indicated that
there was more than one paternal genotype among the
cohort of brooded embryos examined. This raises
questions about sequential mating or even the possibility
of sneaker males, the latter behavior having been
observed in the brooding Antarctic sea star Neosmilaster
georgianus (Slattery and Bosch, 1993).
Molecular genetics has been increasingly exploited to
examine long standing questions about whether direct
development and brooding in benthic marine invertebrates including echinoderms is necessarily associated
with a narrow geographic range, low rates of colonization, low levels of gene flow, and high speciation and
extinction rates (Todd and Doyle, 1981; Jablonski, 1986;
Sheltema, 1989; Emlet, 1995; Hrincevich et al., 2004;
reviewed in Havenhand, 1995). Recently Sponer and
Roy (2002) conducted a molecular phylogenetic analysis

J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201

(sequence and restriction-fragment-length-polymorphisms (RFLP) analyses of nuclear and mitochondrial

DNA) of individuals of the internal brooding brittle star
A. squamata collected from 16 geographically separated
locations along the coast of New Zealand. They found
highly cryptic genetic variation and cryptic dispersal
potential, as well as evidence of genetically divergent
and reproductively isolated lineages (see also Le Gac
et al., 2004). Furthermore, their molecular analyses
suggested that while dispersal ability is regionally
restricted there is sporadic long-distance dispersal,
most likely via adults rafting on macroalgae. Additional
studies with brooding echinoderms are needed to
evaluate the hypothesis that poor dispersal ability is a
corollary of direct development. Antarctic echinoderms
will prove valuable models in this regard as many
brooding species are considered to have circumpolar
distributions (Pawson, 1969; Fell and Dawsey, 1969).
Importantly, information relating dispersal capacity to
reproductive mode may prove valuable in policy
decisions regarding the establishment of marine protected reserves.
Molecular phylogenetic approaches are facilitating
evaluations of the hypothesis that brooding in echinoderms is associated with increased rates of cladogenesis
compared to taxa that retain the presumptive ancestral
planktotrophic larva. For example, Hrincevich et al.
(2004) conducted a phyletic analysis of 1542 base pairs of
mitochondrial DNA sequences for 23 molecular lineages
in the brooding sea star genus Leptasterias. They used a
variety of techniques including maximum parsimony,
minimum evolution, and maximum likelihood to identify
five major clades (corresponding to species or species
complexes) in the subgenus Hexasterias. Interestingly,
two of the clades with geographic distributions above 48
north had shallow phyletic nodes that were suggestive of
recent radiations. Hrincevich et al. (2004) argue that this
pattern is consistent with the hypothesis that high latitude
taxa have high rates of extinction due to repeated
climactic crises as proposed by Poulin and Fral (1996)
for brooding Antarctic echinoids.
There are a host of additional intriguing questions yet
to be addressed upon which modern experimental
techniques may shed light. How do parentally produced
enzymes in some species of brooding echinoderms
facilitate the breakdown of fertilization membranes?
What are the mechanisms of chemoreception that mediate
malefemale bonding or mating aggregations in brooding
echinoderms? Why are most brooding ophiuroids
hermaphroditic? Do simultaneous hermaphroditic species
self-fertilize or outcross when mates are available? Do
outcrossed offspring outperform selfed offspring and

199

what can this tell us about the adaptive significance of

sex? Will genetic evidence support the hypothesis that
some brooding sea stars employ sneaky male mating
strategies? If so, does this reflect malemale competition,
a focus of models of sexual selection in dioecious species?
Are there compensatory metabolic mechanisms that offset
restricted energy intake in brooding adults over prolonged
periods of feeding cessation? These questions and many
others that are certain to follow suit promise that future
studies of brooding in echinoderms will continue to
advance from their somewhat tangled beginnings
(Young, 1994).
Acknowledgements
We thank John Lawrence, Adam Marsh, Donal
Manahan and Margaret Amsler for their valuable
comments and insights. An initial segment of this
review was completed by J.M.G. as a requirement for an
Advanced Invertebrate Zoology graduate course taught
by J.B.M. in spring 2006 at UAB. The preparation of
this review was supported by an Endowed University
Professorship in Polar and Marine Biology to J.B.M. We
dedicate this review paper to the fond memory of
Martha Rearick, Professor of Music at the University of
South Florida, who appreciated the lure of echinoderms
more than most any professional musician. [SS]
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