356
John D. GAGE
Adaptation to necrophagy: giant amphipod
scavengers
The response to animal carcasses by highly specialized, motile scavengers is best known in the ‘giant’
amphipods belonging to the family Lysianassidae
(Shulenberger and Hessler, 1974; Shulenberger and
Barnard, 1976; Thurston, 1979; Hargrave, 1985). The
largest of these amphipods, such as Alicella gigantea
(measuring up to ~34 cm in body length in females)
and Eurythenes gryllus (up to ~14 cm in body length),
probably have a worldwide distribution (Barnard and
Ingram, 1986; De Broyer and Thurston, 1987). The
foraging of scavenging lysianassids has been reviewed
by Sainte-Marie (1992). They represent a highly
specialized response to isolated, discrete food-falls in
the deep ocean.
Olfaction, possibly combined with rheotactic swimming behaviour, is almost certainly the principal
means of detecting and finding carrion food-falls. The
amphipods possess shearing mandibles and capacious
guts, well equipped for rapid and voracious feeding on
carrion (Dahl, 1979; Thurston, 1979). In situ experiments by Hargrave et al. (1994) on Eurythenes gryllus
show that they are able to process meals as batch
reactors (a term borrowed from industrial chemistry
where food is processed as discrete batches in a large
gut – see Penry and Jumars, 1987). This method
is suited to the need for surviving for long periods
without feeding. Furthermore, enhanced activity by
barophilic bacteria in the intestinal tract represents hotspots in microbial degradation of organic material in
the deep sea (Wirsen and Jannasch, 1983); while high
oil content from lipid energy storage in these animals
may aid buoyancy as well as providing for concentrated
energy storage. Hargrave et al. (1994) thought that
Eurythenes gryllus might survive a year without food
by utilizing its most recent meal and stored lipids. The
added buoyancy from lipids may allow energy-efficient
hovering, like a buzzard or mosquito, in the uppermost
part of the benthic boundary layer (Jumars and
Gallagher, 1982). Here, increasing flow velocity, and
increasingly horizontally orientated turbulent mixing,
widen the disemination of the odour plume from a
target. As a consequence most Eurythenes gryllus
are caught in baited traps set at about 15 metres
above the bottom, although adults occur to about
300 metres above the bottom (Ingram and Hessler,
1983; K.L. Smith and Baldwin, 1984a; Charmasson
and Calmet, 1987; Christiansen et al., 1990). Scent
from carrion may diffuse upwards from below as well
as laterally, but baited-camera observations show large
scavenging amphipods approach from the down-current
direction, with the response maximized during peaks
in tidal flow (Thurston, 1979; Lampitt et al., 1983;
Desbruy` eres et al., 1985; Jones et al., 1998), indicating
efficient location of carrion. An alternative “sit-andwait” strategy might involve amphipods lying burrowed
in the sediment until they sense a target, but no hard
evidence is available, and this now seems unlikely.
However, aggregations of lysianassids are reported to
persist, “roosting”, possibly in a torpid state, in the
sediment for days near bait after gorging themselves
(C.R. Smith, 1985, 1986; Sainte-Marie, 1986).
A second group includes smaller, less specialized,
amphipod species (including genera of the Orchomene
complex) having a less specialized morphology and
a lifestyle withstanding perhaps shorter periods of
starvation. Experiments in aquaria have shown that the
species Orchomene obtusus may not survive longer
than about six weeks without food, but it reacts within
seconds to odours emitted from carrion (Tamburri
and Barry, 1999). Tamburri and Barry found that the
smell also triggered a strong positive geo-, or possibly
thigmo-tactic response, resulting in a search restricted
to the bottom where food-falls will naturally occur.
Even though members of the first group of amphipods
are extremely well adapted, the prevailing view is
that it is unlikely that any deep-sea species is an
obligate necrophage; the extensive vertical range of
lysianassid species enabling them to compensate for
deficient bottom resources by foraging for living prey
in the water column (Jumars and Gallagher, 1982;
Sainte-Marie, 1992; Britton and Morton, 1994). Such
feeding may contribute towards active transport of
organic material from the bathypelagic zone to the sea
floor. However, against the idea that these animals may
feed on live prey is the experimental evidence that
Orchomene obtusus when tested showed no response
to the odour of live, rather than dead prey (Tamburri
and Barry, 1999).
Other benthic necrophages
Britton and Morton (1994) have provided a general
survey of marine scavengers, including those in the
deep sea. Scavenging is not a sharply defined category
of feeding and, like deposit feeding and carnivory
where large ‘vacuum cleaner’ deposit feeders, such as
elasipod holothurians, may take in small invertebrates
John D. GAGE
Adaptation to necrophagy: giant amphipod
scavengers
The response to animal carcasses by highly specialized, motile scavengers is best known in the ‘giant’
amphipods belonging to the family Lysianassidae
(Shulenberger and Hessler, 1974; Shulenberger and
Barnard, 1976; Thurston, 1979; Hargrave, 1985). The
largest of these amphipods, such as Alicella gigantea
(measuring up to ~34 cm in body length in females)
and Eurythenes gryllus (up to ~14 cm in body length),
probably have a worldwide distribution (Barnard and
Ingram, 1986; De Broyer and Thurston, 1987). The
foraging of scavenging lysianassids has been reviewed
by Sainte-Marie (1992). They represent a highly
specialized response to isolated, discrete food-falls in
the deep ocean.
Olfaction, possibly combined with rheotactic swimming behaviour, is almost certainly the principal
means of detecting and finding carrion food-falls. The
amphipods possess shearing mandibles and capacious
guts, well equipped for rapid and voracious feeding on
carrion (Dahl, 1979; Thurston, 1979). In situ experiments by Hargrave et al. (1994) on Eurythenes gryllus
show that they are able to process meals as batch
reactors (a term borrowed from industrial chemistry
where food is processed as discrete batches in a large
gut – see Penry and Jumars, 1987). This method
is suited to the need for surviving for long periods
without feeding. Furthermore, enhanced activity by
barophilic bacteria in the intestinal tract represents hotspots in microbial degradation of organic material in
the deep sea (Wirsen and Jannasch, 1983); while high
oil content from lipid energy storage in these animals
may aid buoyancy as well as providing for concentrated
energy storage. Hargrave et al. (1994) thought that
Eurythenes gryllus might survive a year without food
by utilizing its most recent meal and stored lipids. The
added buoyancy from lipids may allow energy-efficient
hovering, like a buzzard or mosquito, in the uppermost
part of the benthic boundary layer (Jumars and
Gallagher, 1982). Here, increasing flow velocity, and
increasingly horizontally orientated turbulent mixing,
widen the disemination of the odour plume from a
target. As a consequence most Eurythenes gryllus
are caught in baited traps set at about 15 metres
above the bottom, although adults occur to about
300 metres above the bottom (Ingram and Hessler,
1983; K.L. Smith and Baldwin, 1984a; Charmasson
and Calmet, 1987; Christiansen et al., 1990). Scent
from carrion may diffuse upwards from below as well
as laterally, but baited-camera observations show large
scavenging amphipods approach from the down-current
direction, with the response maximized during peaks
in tidal flow (Thurston, 1979; Lampitt et al., 1983;
Desbruy` eres et al., 1985; Jones et al., 1998), indicating
efficient location of carrion. An alternative “sit-andwait” strategy might involve amphipods lying burrowed
in the sediment until they sense a target, but no hard
evidence is available, and this now seems unlikely.
However, aggregations of lysianassids are reported to
persist, “roosting”, possibly in a torpid state, in the
sediment for days near bait after gorging themselves
(C.R. Smith, 1985, 1986; Sainte-Marie, 1986).
A second group includes smaller, less specialized,
amphipod species (including genera of the Orchomene
complex) having a less specialized morphology and
a lifestyle withstanding perhaps shorter periods of
starvation. Experiments in aquaria have shown that the
species Orchomene obtusus may not survive longer
than about six weeks without food, but it reacts within
seconds to odours emitted from carrion (Tamburri
and Barry, 1999). Tamburri and Barry found that the
smell also triggered a strong positive geo-, or possibly
thigmo-tactic response, resulting in a search restricted
to the bottom where food-falls will naturally occur.
Even though members of the first group of amphipods
are extremely well adapted, the prevailing view is
that it is unlikely that any deep-sea species is an
obligate necrophage; the extensive vertical range of
lysianassid species enabling them to compensate for
deficient bottom resources by foraging for living prey
in the water column (Jumars and Gallagher, 1982;
Sainte-Marie, 1992; Britton and Morton, 1994). Such
feeding may contribute towards active transport of
organic material from the bathypelagic zone to the sea
floor. However, against the idea that these animals may
feed on live prey is the experimental evidence that
Orchomene obtusus when tested showed no response
to the odour of live, rather than dead prey (Tamburri
and Barry, 1999).
Other benthic necrophages
Britton and Morton (1994) have provided a general
survey of marine scavengers, including those in the
deep sea. Scavenging is not a sharply defined category
of feeding and, like deposit feeding and carnivory
where large ‘vacuum cleaner’ deposit feeders, such as
elasipod holothurians, may take in small invertebrates