REPRODUCTION, DEVELOPMENT AND LIFE-HISTORY TRAITS
411
for fertilization to occur (reviewed by Levitan, 1995).
In shallow water, fertilization success is assured by
breeding behaviors that bring animals into close
proximity (e.g., Run et al., 1988), by environmental
cues that assure simultaneous release of gametes
(reviewed by Giese and Kanatani, 1987), and, at least in
some species, by chemical communication (e.g., Miller,
1989). Internal fertilization is the most secure method
of assuring that eggs and sperm come together. In some
species this follows copulation, and in others sperm
are collected and maintained by the female until the
eggs are ready to be fertilized. Internal fertilization
occurs in many gastropod molluscs, in peracarid,
cirripede and decapod crustaceans, in bryozoans, in
colonial ascidians, and in many polychaetes. Among
free spawners, the timing of gamete release is often
controlled by photoperiodic cues such as sunrise and
lunar period. Epidemic spawning, wherein the gametes
of one individual provide a signal that stimulates
spawning in another, is commonly thought to facilitate
spawning throughout the animal kingdom (Thorson,
1946). However, evidence for epidemic spawning
remains equivocal for most species (Young, 1999), and
only a few experimental studies (e.g., Starr et al., 1990)
have shown its importance in shallow-water animals.
Fertilization success may also be facilitated by
gamete modifications that reduce dilution by water currents, or that increase gamete longevity (Eckelbarger,
1994b).
Predictions
Because photoperiodic spawning cues are absent
in the deep sea and many animals occur at low
population densities, an increase in the incidence
of internal fertilization is expected. Among species
that fertilize externally, behavioral mechanisms such
as spawning aggregation and an increase in the
importance of pheromonal communication have been
predicted (Young, 1999). Gamete modifications are
also expected (Eckelbarger et al., 1989c; Eckelbarger,
1994b).
Evidence
Internal fertilization is the rule among deep-sea
peracarids, which are the most diverse animals in the
deep sea, and also predominates among the deep-sea
gastropods, which include many diminutive species
that lay egg masses with developing embryos. Many
of the polychaetes living at hydrothermal vents have
sperm that are clearly modified for internal fertilization.
For example, the alvinellid and polynoid polychaetes
have spermathecae for receiving exogenous sperm from
other individuals and storing the sperm until eggs are
ready to be fertilized (Zal et al., 1994; Jollivet et al.,
2000). Internal fertilization also appears likely in a vent
siboglinid tube worm, Ridgeia piscesae. In this species,
sticky masses of sperm are apparently captured on the
vestimentum of the female worm, then transferred into
the gonoducts (Southward and Coates, 1985). Although
other siboglinids release unusual helical sperm in
bundles (Cary et al., 1989), evidence suggests that they
all fertilize externally (Van Dover, 1994; Young et al.,
1996b).
Elongate and modified sperm are much more
common among deep-sea free-spawning echinoderms
than among their shallow-water relatives (reviewed by
Eckelbarger et al., 1989c), and elongate sperm have
also been described for a hydrothermal-vent bivalve
(Beninger and Le Pennec, 1997). Some modifications,
such as lipid reserves associated with the mitochondria of echinothuriid sea-urchin sperm (Eckelbarger
et al., 1989b) appear to increase sperm longevity,
whereas others, such as the bipolar tailed, dimorphic
sperm of Phrissocystis multispina (Eckelbarger et al.,
1989a), may reduce dilution. The release of sperm
in swimming bundles by hydrothermal-vent and coldseep siboglinids may also help to maintain high
sperm concentrations in environment where buoyant,
turbulent water could easily carry individual sperm
away from the spawning females.
Many deep-sea echinoderms apparently facilitate
fertilization by living in perennial herds (Young,
1994b), but others occur as scattered individuals,
often at very low population densities. Many of the
latter, including species of echinoids, holothuroids and
ophiuroids, form pairs (Fig. 12.6) and other small-scale
aggregations prior to spawning (Tyler et al., 1992b;
Young et al., 1992; Young, 1994b, 1999). Indeed,
breeding aggregations have been documented in many
more deep-sea species than shallow-water ones, a
pattern that is particularly striking when sampling
bias is taken into account. Wilson (1975) posed the
following hypothesis on the basis of his own work with
insects:
“It is plausible (but unproved) that swarming is most
advantageous to members of rare species and to those
living in environments where the optimal time for
mating is unpredictable.”
Pairing behavior in rare deep-sea echinoderms that
live in an environment with few spawning cues lends
credible support to Wilson’s hypothesis.
411
for fertilization to occur (reviewed by Levitan, 1995).
In shallow water, fertilization success is assured by
breeding behaviors that bring animals into close
proximity (e.g., Run et al., 1988), by environmental
cues that assure simultaneous release of gametes
(reviewed by Giese and Kanatani, 1987), and, at least in
some species, by chemical communication (e.g., Miller,
1989). Internal fertilization is the most secure method
of assuring that eggs and sperm come together. In some
species this follows copulation, and in others sperm
are collected and maintained by the female until the
eggs are ready to be fertilized. Internal fertilization
occurs in many gastropod molluscs, in peracarid,
cirripede and decapod crustaceans, in bryozoans, in
colonial ascidians, and in many polychaetes. Among
free spawners, the timing of gamete release is often
controlled by photoperiodic cues such as sunrise and
lunar period. Epidemic spawning, wherein the gametes
of one individual provide a signal that stimulates
spawning in another, is commonly thought to facilitate
spawning throughout the animal kingdom (Thorson,
1946). However, evidence for epidemic spawning
remains equivocal for most species (Young, 1999), and
only a few experimental studies (e.g., Starr et al., 1990)
have shown its importance in shallow-water animals.
Fertilization success may also be facilitated by
gamete modifications that reduce dilution by water currents, or that increase gamete longevity (Eckelbarger,
1994b).
Predictions
Because photoperiodic spawning cues are absent
in the deep sea and many animals occur at low
population densities, an increase in the incidence
of internal fertilization is expected. Among species
that fertilize externally, behavioral mechanisms such
as spawning aggregation and an increase in the
importance of pheromonal communication have been
predicted (Young, 1999). Gamete modifications are
also expected (Eckelbarger et al., 1989c; Eckelbarger,
1994b).
Evidence
Internal fertilization is the rule among deep-sea
peracarids, which are the most diverse animals in the
deep sea, and also predominates among the deep-sea
gastropods, which include many diminutive species
that lay egg masses with developing embryos. Many
of the polychaetes living at hydrothermal vents have
sperm that are clearly modified for internal fertilization.
For example, the alvinellid and polynoid polychaetes
have spermathecae for receiving exogenous sperm from
other individuals and storing the sperm until eggs are
ready to be fertilized (Zal et al., 1994; Jollivet et al.,
2000). Internal fertilization also appears likely in a vent
siboglinid tube worm, Ridgeia piscesae. In this species,
sticky masses of sperm are apparently captured on the
vestimentum of the female worm, then transferred into
the gonoducts (Southward and Coates, 1985). Although
other siboglinids release unusual helical sperm in
bundles (Cary et al., 1989), evidence suggests that they
all fertilize externally (Van Dover, 1994; Young et al.,
1996b).
Elongate and modified sperm are much more
common among deep-sea free-spawning echinoderms
than among their shallow-water relatives (reviewed by
Eckelbarger et al., 1989c), and elongate sperm have
also been described for a hydrothermal-vent bivalve
(Beninger and Le Pennec, 1997). Some modifications,
such as lipid reserves associated with the mitochondria of echinothuriid sea-urchin sperm (Eckelbarger
et al., 1989b) appear to increase sperm longevity,
whereas others, such as the bipolar tailed, dimorphic
sperm of Phrissocystis multispina (Eckelbarger et al.,
1989a), may reduce dilution. The release of sperm
in swimming bundles by hydrothermal-vent and coldseep siboglinids may also help to maintain high
sperm concentrations in environment where buoyant,
turbulent water could easily carry individual sperm
away from the spawning females.
Many deep-sea echinoderms apparently facilitate
fertilization by living in perennial herds (Young,
1994b), but others occur as scattered individuals,
often at very low population densities. Many of the
latter, including species of echinoids, holothuroids and
ophiuroids, form pairs (Fig. 12.6) and other small-scale
aggregations prior to spawning (Tyler et al., 1992b;
Young et al., 1992; Young, 1994b, 1999). Indeed,
breeding aggregations have been documented in many
more deep-sea species than shallow-water ones, a
pattern that is particularly striking when sampling
bias is taken into account. Wilson (1975) posed the
following hypothesis on the basis of his own work with
insects:
“It is plausible (but unproved) that swarming is most
advantageous to members of rare species and to those
living in environments where the optimal time for
mating is unpredictable.”
Pairing behavior in rare deep-sea echinoderms that
live in an environment with few spawning cues lends
credible support to Wilson’s hypothesis.