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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
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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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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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).
196
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
J.M. Gillespie, J.B. McClintock / Journal of Experimental Marine Biology and Ecology 342 (2007) 191201
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