REPRODUCTION, DEVELOPMENT AND LIFE-HISTORY TRAITS
409
and bivalves, appear to reproduce over a wide range
of body sizes, suggesting that reproduction is either
continuous or iteroparous (reviewed by Tyler and
Young, 1999). To date, no semelparous species have
been documented at vents or seeps, but it seems likely
that some of the abundant small gastropods might be
opportunistic and semelparous.
Seasonal vs. continuous breeding
Background
At the individual level, gametogenesis may proceed
rapidly or slowly depending on the mechanisms of yolk
deposition, and with either single or multiple cohorts
of eggs developing at any given time (reviewed by
Eckelbarger, 1994a). The mechanism of vitellogenesis
may be absolutely conserved in some groups, but in
others, selection can modify the timing and speed
of gametogenesis to produce life cycles that reflect
the environmental cycles in which the animal lives.
Some tropical animals, which live in environments
with virtually constant temperature and daylength breed
semi-continuously (reviewed by Giese and Pearse,
1974; Young, 1999), but the vast majority of shallowwater animals in both temperate and tropical latitudes
are periodic, synchronous breeders with annual reproductive cycles being the most common (Giese and
Pearse, 1974).
Predictions
Moseley (1880) thought that there might be some
seasonality in the deep sea, but his tentative suggestion
was soon overshadowed by an influential paper by
Orton (1920) predicting that deep-sea animals living
at constant temperature should reproduce continuously.
Although Orton advanced this idea as a testable
hypothesis, it was not tested for many decades.
During the intervening period, it became practically
canonized in the deep-sea literature, in part because
seasonal samples were hard to obtain, but also because
the dynamic nature of the deep sea was not fully
appreciated by biologists.
Evidence
Tables 12.1 to 12.4 list by major group all bathyal
and abyssal species for which gametogenesis has
been studied sufficiently well to infer periodicity of
reproduction. Only a small amount of evidence comes
from populations sampled regularly for reproductive
parameters throughout the years. Constraints in shiptime, so that different seasons are sampled in different
years, often make it necessary to piece data together to
make a composite year. It is not uncommon to find data
sets with many months missing. As a poor alternative to
seasonal sampling, patterns of reproductive periodicity
have often been inferred from single gonad samples.
This may be done by examining the cohort structure
of gametes; the presence of multiple egg sizes and
few mature gametes is suggestive of semi-continuous
reproduction, particularly when numerous individuals
of the population show a similar pattern. On the
other hand, population-wide synchrony in which all
individuals have a single gamete cohort is indicative
of periodic, synchronized reproduction.
It is clear from the data that the majority of deep-sea
species have aseasonal reproduction, but that seasonal
reproduction also occurs at all latitudes and to depths
of several thousand meters. Seasonal reproduction
is known among sponges, cnidarians, peracarid and
decapod crustaceans, molluscs, and echinoderms. Vent
species are mostly continuous breeders. However,
preliminary evidence suggests that some bivalves living
at relatively shallow hydrothermal vents may breed
seasonally (Comtet and Desbruy` eres, 1998; Comtet
et al., 1999) as do many animals at cold seeps. The
factors that drive seasonality remain unknown, as these
animals may obtain all of the carbon and energy needed
for maintenance from chemosynthetic sources. It is
possible that they use phytodetritus as an energy source
for gonad development, while relying on methane for
maintenance and construction of somatic tissue.
Because the very existence of seasonal breeding
came as a great surprise when it was first documented
in the deep sea, it has perhaps received undue attention.
It must be kept in mind that the vast majority of deepsea animals, particularly at abyssal depths, reproduce
aperiodically or continuously and therefore require no
periodic cues for the entrainment of their gametogenic
cycles.
Environmental control of gametogenesis
Background
Among marine animals, the timing of reproduction is
almost invariably controlled on two different temporal
scales: a long scale associated with initiation and
progression of gametogenesis, and a shorter scale
associated with spawning. Factors that entrain seasonal
cycles of gametogenesis in shallow water include
predictable changes in the natural light regime (e.g.,
sunrise, sunset, increasing daylength), and predictable
409
and bivalves, appear to reproduce over a wide range
of body sizes, suggesting that reproduction is either
continuous or iteroparous (reviewed by Tyler and
Young, 1999). To date, no semelparous species have
been documented at vents or seeps, but it seems likely
that some of the abundant small gastropods might be
opportunistic and semelparous.
Seasonal vs. continuous breeding
Background
At the individual level, gametogenesis may proceed
rapidly or slowly depending on the mechanisms of yolk
deposition, and with either single or multiple cohorts
of eggs developing at any given time (reviewed by
Eckelbarger, 1994a). The mechanism of vitellogenesis
may be absolutely conserved in some groups, but in
others, selection can modify the timing and speed
of gametogenesis to produce life cycles that reflect
the environmental cycles in which the animal lives.
Some tropical animals, which live in environments
with virtually constant temperature and daylength breed
semi-continuously (reviewed by Giese and Pearse,
1974; Young, 1999), but the vast majority of shallowwater animals in both temperate and tropical latitudes
are periodic, synchronous breeders with annual reproductive cycles being the most common (Giese and
Pearse, 1974).
Predictions
Moseley (1880) thought that there might be some
seasonality in the deep sea, but his tentative suggestion
was soon overshadowed by an influential paper by
Orton (1920) predicting that deep-sea animals living
at constant temperature should reproduce continuously.
Although Orton advanced this idea as a testable
hypothesis, it was not tested for many decades.
During the intervening period, it became practically
canonized in the deep-sea literature, in part because
seasonal samples were hard to obtain, but also because
the dynamic nature of the deep sea was not fully
appreciated by biologists.
Evidence
Tables 12.1 to 12.4 list by major group all bathyal
and abyssal species for which gametogenesis has
been studied sufficiently well to infer periodicity of
reproduction. Only a small amount of evidence comes
from populations sampled regularly for reproductive
parameters throughout the years. Constraints in shiptime, so that different seasons are sampled in different
years, often make it necessary to piece data together to
make a composite year. It is not uncommon to find data
sets with many months missing. As a poor alternative to
seasonal sampling, patterns of reproductive periodicity
have often been inferred from single gonad samples.
This may be done by examining the cohort structure
of gametes; the presence of multiple egg sizes and
few mature gametes is suggestive of semi-continuous
reproduction, particularly when numerous individuals
of the population show a similar pattern. On the
other hand, population-wide synchrony in which all
individuals have a single gamete cohort is indicative
of periodic, synchronized reproduction.
It is clear from the data that the majority of deep-sea
species have aseasonal reproduction, but that seasonal
reproduction also occurs at all latitudes and to depths
of several thousand meters. Seasonal reproduction
is known among sponges, cnidarians, peracarid and
decapod crustaceans, molluscs, and echinoderms. Vent
species are mostly continuous breeders. However,
preliminary evidence suggests that some bivalves living
at relatively shallow hydrothermal vents may breed
seasonally (Comtet and Desbruy` eres, 1998; Comtet
et al., 1999) as do many animals at cold seeps. The
factors that drive seasonality remain unknown, as these
animals may obtain all of the carbon and energy needed
for maintenance from chemosynthetic sources. It is
possible that they use phytodetritus as an energy source
for gonad development, while relying on methane for
maintenance and construction of somatic tissue.
Because the very existence of seasonal breeding
came as a great surprise when it was first documented
in the deep sea, it has perhaps received undue attention.
It must be kept in mind that the vast majority of deepsea animals, particularly at abyssal depths, reproduce
aperiodically or continuously and therefore require no
periodic cues for the entrainment of their gametogenic
cycles.
Environmental control of gametogenesis
Background
Among marine animals, the timing of reproduction is
almost invariably controlled on two different temporal
scales: a long scale associated with initiation and
progression of gametogenesis, and a shorter scale
associated with spawning. Factors that entrain seasonal
cycles of gametogenesis in shallow water include
predictable changes in the natural light regime (e.g.,
sunrise, sunset, increasing daylength), and predictable