382
Craig M. YOUNG
being the most speciose group. On hard substrata in the
deep sea, cnidarians and sponges are especially abundant (Gage and Tyler, 1991) except at hydrothermal
vents, where the hard-bottom fauna is dominated by
polychaetes and molluscs (Grassle, 1986). As might be
expected, the most speciose and abundant groups are
also the best studied. I will discuss each of these major
phyla in turn, then briefly consider a few others for
which more limited information is available.
Annelida
Polychaete annelids are among the most abundant
and diverse macrofaunal organisms in the deep sea
(Hartman, 1965; Hartman and Fauchald, 1971). Most
are deposit feeders depending directly on detrital
material falling from above, and most live in the upper
few centimeters of sediment. However, polychaetes are
also well represented at hydrothermal vents and cold
seeps, where they may take on bizarre life styles and
spectacular forms. The giant tube worms of vents and
seeps and the filamentous perviate pogonophorans are
now recognized as polychaetes (family Siboglinidae)
specialized for the use of chemosynthetic energy
sources. Alvinellid polychaetes, which are common
at hydrothermal vents, may be the most eurythermal
metazoans (Cary et al., 1998). General aspects of
polychaete life-history biology and development have
been reviewed by Schroeder and Hermans (1975),
Giangrande (1997) and Pernet et al. (2002).
Gonads, gametogenesis, and reproductive
periodicity
Although many polychaetes are hermaphroditic, the
majority of deep-sea forms that have been studied
appear to have separate sexes. In polychaetes, the
oocytes always originate within distinct ovaries, often
found associated with the peritonea (Eckelbarger,
1986), but vitellogenesis, the stage of oogenesis in
which oocytes are invested with yolk, may occur either
within the ovary or while oocytes are floating freely
within the coelom (Eckelbarger, 1986). In like manner,
early spermatocytes released from the gonads often
aggregate into plaques, then complete spermatogenesis
while adrift in the coelom. Gametogenesis in the
deep-sea polychaete Pholoe anoculata is coelomic
in both sexes, with gametes concentrating near the
acicula of the neuropodium (Blake, 1993). An unusual
modification of the typical patterns occurs in the deepsea cossurid Cossura longocirrata. In this species,
oogenesis takes place in a single segment, which
releases mature oocytes into more posterior segments
for storage, making the abdominal region appear
beaded (Fournier and Peterson, 1991; Blake, 1993). In
the large bathyal terebellid Biremis blandi, scattered
oocytes may be found throughout the coelom, but the
highest concentrations are in the ventral region, where
they pool between the peritonea (Young, unpublished
observations).
With a single exception, all deep-sea polychaetes
that have been examined appear capable of reproducing
throughout the year, though several species may
have “fluctuating” reproductive cycles (as defined by
A. Scheltema, 1987), in which there are high and low
periods of spawning. One non-vent species, Cossura
longocirrata, reproduces more in the summer than at
other times of the year (Blake, 1993). All of the other
fluctuating species are associated with vents (McHugh,
1989; McHugh and Tunnicliffe, 1994; Zal et al., 1995),
and in every case sampling is inadequate to determine
the period of the fluctuation. The only truly seasonal
species is the non-vent spionid Aurospio dibranchiata,
which occupies an impressively broad bathymetric
range (300–3600 m). Notably, evidence for a seasonal
gametogenic cycle came not only from the shallowest
animals, but also from collections at 2000 m depth. No
mature animals were found in spring collections, but
animals collected in the summer and fall were ripe
(Blake, 1993). However, these data must be regarded as
preliminary, since only 13 of 425 individuals examined
were found to bear any gametes at all.
Gamete structure and fertilization
Sperm of some deep-sea polychaetes are of the
primitive type associated with free spawning and external fertilization (e.g., Amphisamytha galapagensis:
McHugh and Tunnicliffe, 1994), but the variety of
modified sperm described in the literature is striking
(Table 12.1). A number of species have elongate
sperm, often with limited mobility, which are probably
indicative of either internal fertilization, fertilization in
tubes, or pseudocopulation in gelatinous egg masses
(Franzen, 1956; Jamieson and Rouse, 1989). The sperm
of Paralvinella pandorae have a convoluted structure
of unknown function near the mitochondrion, and the
flagellum emerges at an acute angle near this structure
(McHugh, 1989), suggesting that motility is limited. On
the basis of this sperm structure, McHugh (1989) has
speculated that sperm are transferred from the male to
the female in bundles rather than being freely spawned.
The sperm of Paralvinella grasslei lack acrosome,
Craig M. YOUNG
being the most speciose group. On hard substrata in the
deep sea, cnidarians and sponges are especially abundant (Gage and Tyler, 1991) except at hydrothermal
vents, where the hard-bottom fauna is dominated by
polychaetes and molluscs (Grassle, 1986). As might be
expected, the most speciose and abundant groups are
also the best studied. I will discuss each of these major
phyla in turn, then briefly consider a few others for
which more limited information is available.
Annelida
Polychaete annelids are among the most abundant
and diverse macrofaunal organisms in the deep sea
(Hartman, 1965; Hartman and Fauchald, 1971). Most
are deposit feeders depending directly on detrital
material falling from above, and most live in the upper
few centimeters of sediment. However, polychaetes are
also well represented at hydrothermal vents and cold
seeps, where they may take on bizarre life styles and
spectacular forms. The giant tube worms of vents and
seeps and the filamentous perviate pogonophorans are
now recognized as polychaetes (family Siboglinidae)
specialized for the use of chemosynthetic energy
sources. Alvinellid polychaetes, which are common
at hydrothermal vents, may be the most eurythermal
metazoans (Cary et al., 1998). General aspects of
polychaete life-history biology and development have
been reviewed by Schroeder and Hermans (1975),
Giangrande (1997) and Pernet et al. (2002).
Gonads, gametogenesis, and reproductive
periodicity
Although many polychaetes are hermaphroditic, the
majority of deep-sea forms that have been studied
appear to have separate sexes. In polychaetes, the
oocytes always originate within distinct ovaries, often
found associated with the peritonea (Eckelbarger,
1986), but vitellogenesis, the stage of oogenesis in
which oocytes are invested with yolk, may occur either
within the ovary or while oocytes are floating freely
within the coelom (Eckelbarger, 1986). In like manner,
early spermatocytes released from the gonads often
aggregate into plaques, then complete spermatogenesis
while adrift in the coelom. Gametogenesis in the
deep-sea polychaete Pholoe anoculata is coelomic
in both sexes, with gametes concentrating near the
acicula of the neuropodium (Blake, 1993). An unusual
modification of the typical patterns occurs in the deepsea cossurid Cossura longocirrata. In this species,
oogenesis takes place in a single segment, which
releases mature oocytes into more posterior segments
for storage, making the abdominal region appear
beaded (Fournier and Peterson, 1991; Blake, 1993). In
the large bathyal terebellid Biremis blandi, scattered
oocytes may be found throughout the coelom, but the
highest concentrations are in the ventral region, where
they pool between the peritonea (Young, unpublished
observations).
With a single exception, all deep-sea polychaetes
that have been examined appear capable of reproducing
throughout the year, though several species may
have “fluctuating” reproductive cycles (as defined by
A. Scheltema, 1987), in which there are high and low
periods of spawning. One non-vent species, Cossura
longocirrata, reproduces more in the summer than at
other times of the year (Blake, 1993). All of the other
fluctuating species are associated with vents (McHugh,
1989; McHugh and Tunnicliffe, 1994; Zal et al., 1995),
and in every case sampling is inadequate to determine
the period of the fluctuation. The only truly seasonal
species is the non-vent spionid Aurospio dibranchiata,
which occupies an impressively broad bathymetric
range (300–3600 m). Notably, evidence for a seasonal
gametogenic cycle came not only from the shallowest
animals, but also from collections at 2000 m depth. No
mature animals were found in spring collections, but
animals collected in the summer and fall were ripe
(Blake, 1993). However, these data must be regarded as
preliminary, since only 13 of 425 individuals examined
were found to bear any gametes at all.
Gamete structure and fertilization
Sperm of some deep-sea polychaetes are of the
primitive type associated with free spawning and external fertilization (e.g., Amphisamytha galapagensis:
McHugh and Tunnicliffe, 1994), but the variety of
modified sperm described in the literature is striking
(Table 12.1). A number of species have elongate
sperm, often with limited mobility, which are probably
indicative of either internal fertilization, fertilization in
tubes, or pseudocopulation in gelatinous egg masses
(Franzen, 1956; Jamieson and Rouse, 1989). The sperm
of Paralvinella pandorae have a convoluted structure
of unknown function near the mitochondrion, and the
flagellum emerges at an acute angle near this structure
(McHugh, 1989), suggesting that motility is limited. On
the basis of this sperm structure, McHugh (1989) has
speculated that sperm are transferred from the male to
the female in bundles rather than being freely spawned.
The sperm of Paralvinella grasslei lack acrosome,