FOOD INPUTS, UTILIZATION, CARBON FLOW AND ENERGETICS
357
as well as sediment particles, it also merges with
detritivory (Walker and Bambach, 1974). I shall
therefore only include macrophagous animals that do
not necessarily kill their food. As mentioned earlier,
there are a number of benthic and benthopelagic fauna
groups, other than highly motile lysianassid amphipods
and fish, that are known to consume carrion on the
deep-sea bed. These include onuphid polychaetes, such
as Hyalinoecia (Dayton and Hessler, 1972), large
neogastropods such as Neptunea (e.g., C.R. Smith,
1985), octopods (Isaacs and Schwartzlose, 1975), ophiuroids (e.g., C.R. Smith, 1985), elasipod holothurians
(Pawson, 1976; Massin, 1982) and perhaps asteroids
and echinoids. Among peracarid crustaceans other than
amphipods, isopods are known as scavengers (e.g.,
Sekiguchi et al., 1982; Briones-Fourz´ an and LozanoAlvarez, 1991; Tso and Mok, 1991), as are many decapod crustaceans, including large, swimming caridean
prawns such as Acanthephyra (e.g., Desbruy` eres et al.,
1985). The large stone crab Neolithodes grimaldi has
also been photographed attracted to bait set on the
bottom in the deep Northeast Atlantic (Gage and Tyler,
1991, fig. 4.27). It is entirely possible that there are
many deep-sea species belonging to the wide range
of invertebrate groups known as occasional scavengers
in shallow water and reviewed by Britton and Morton
(1994) that may also function as facultative scavengers
on the deep-sea bed.
Tamburri and Barry (1999) found that the large
neogastropod Neptunea amianta, and the hagfish
Eptatretus stouti, able to survive for at least nine
months without food. Perhaps surprisingly, N. amianta
showed no apparent response to the odour from carrion
when tested, and Tamburri and Barry (1999) speculated
that the sensitivity to such chemical cues is related to
degree of motility of the scavenger.
Scavenging by fish, and the idea of an independent
trophic pathway based on scavenging
The extent to which scavenging is important in deepsea demersal fish is still debatable. Merrett and
Haedrich (1997) doubted whether many demersal deepsea fish are important scavengers at all. They pointed
out that direct evidence supporting scavenging is rare,
only the grenadier Coryphaenoides (Nematonurus)
armatus (family Macrouridae) being known from
baited-camera studies actually to feed on the bait.
Study of stomach contents has provided evidence for
scavenging only in the eel Synaphobranchus kaupi) and
in C. armatus. However, the jawless hagfish are thought
to contribute significantly to the rapid removal of
carrion on the continental slope (Martini, 1998). Like
lysianassid amphipods, hagfish are highly sensitive
to the water-borne odour from carrion; the odour
triggering characteristic searching activity (Tamburri
and Barry, 1999). In addition, hagfish defend carrion
from some other competitors by releasing slime during
feeding (Isaacs and Schwartzlose, 1975).
The idea of an independent and specialized trophic
pathway based on scavenging was first put forward by
Isaacs (1969). He envisaged a trophic pathway quite
independent from that of carnivores and organisms
exploiting the rain of fine detrital particles (Haedrich
and Rowe, 1977). This idea of divergence in trophic
strategies has also been developed by Mahaut et al.
(1990). However, for deep-sea fishes, the very substantial body of data that has accumulated from studies on
diet, particularly in the large and widely spread family
Macrouridae, and in sharks and chimaeroids, does not
support the great importance of scavenging (Mauchline
and Gordon, 1986; Merrett and Haedrich, 1997). As
predators, opportunism seems to play an important
part in foraging strategies of many species, as much
as specialized trophic behaviour targeting preferred
prey. Hence the evidence that deep-sea benthopelagic
fish may play an important rˆ ole as scavengers is still
equivocal. Merrett and Haedrich (1997) have argued
that predation by fish on pelagic organisms impinging
on the bottom at slope depths, as discovered by
Mauchline and Gordon (1991) and, in deeper water,
on suprabenthic invertebrates in the benthic boundary
layer, is more important.
For invertebrates, the evidence from dietary studies
is much more fragmentary, and morphological and
behavioural data have as yet failed to provide the
definitive evidence that even species as highly adapated
as large lysianassid amphipods rely entirely on scavenging for their nutrition. This view is supported in
the important review of marine carrion and scavenging
by Britton and Morton (1994), on the basis that
as a food source it is too ephemeral, and in any
case there would be too little of it available to
encourage evolution of obligate scavengers. Although
lysiannasid amphipods, and perhaps hagfish, approach
this concept most closely, the unpredictability and very
low density of natural carrion favour the evolution
of facultative, rather than obligate, marine scavengers.
Because most carrion comes from the surface, the
observed increasing importance of scavenging with
357
as well as sediment particles, it also merges with
detritivory (Walker and Bambach, 1974). I shall
therefore only include macrophagous animals that do
not necessarily kill their food. As mentioned earlier,
there are a number of benthic and benthopelagic fauna
groups, other than highly motile lysianassid amphipods
and fish, that are known to consume carrion on the
deep-sea bed. These include onuphid polychaetes, such
as Hyalinoecia (Dayton and Hessler, 1972), large
neogastropods such as Neptunea (e.g., C.R. Smith,
1985), octopods (Isaacs and Schwartzlose, 1975), ophiuroids (e.g., C.R. Smith, 1985), elasipod holothurians
(Pawson, 1976; Massin, 1982) and perhaps asteroids
and echinoids. Among peracarid crustaceans other than
amphipods, isopods are known as scavengers (e.g.,
Sekiguchi et al., 1982; Briones-Fourz´ an and LozanoAlvarez, 1991; Tso and Mok, 1991), as are many decapod crustaceans, including large, swimming caridean
prawns such as Acanthephyra (e.g., Desbruy` eres et al.,
1985). The large stone crab Neolithodes grimaldi has
also been photographed attracted to bait set on the
bottom in the deep Northeast Atlantic (Gage and Tyler,
1991, fig. 4.27). It is entirely possible that there are
many deep-sea species belonging to the wide range
of invertebrate groups known as occasional scavengers
in shallow water and reviewed by Britton and Morton
(1994) that may also function as facultative scavengers
on the deep-sea bed.
Tamburri and Barry (1999) found that the large
neogastropod Neptunea amianta, and the hagfish
Eptatretus stouti, able to survive for at least nine
months without food. Perhaps surprisingly, N. amianta
showed no apparent response to the odour from carrion
when tested, and Tamburri and Barry (1999) speculated
that the sensitivity to such chemical cues is related to
degree of motility of the scavenger.
Scavenging by fish, and the idea of an independent
trophic pathway based on scavenging
The extent to which scavenging is important in deepsea demersal fish is still debatable. Merrett and
Haedrich (1997) doubted whether many demersal deepsea fish are important scavengers at all. They pointed
out that direct evidence supporting scavenging is rare,
only the grenadier Coryphaenoides (Nematonurus)
armatus (family Macrouridae) being known from
baited-camera studies actually to feed on the bait.
Study of stomach contents has provided evidence for
scavenging only in the eel Synaphobranchus kaupi) and
in C. armatus. However, the jawless hagfish are thought
to contribute significantly to the rapid removal of
carrion on the continental slope (Martini, 1998). Like
lysianassid amphipods, hagfish are highly sensitive
to the water-borne odour from carrion; the odour
triggering characteristic searching activity (Tamburri
and Barry, 1999). In addition, hagfish defend carrion
from some other competitors by releasing slime during
feeding (Isaacs and Schwartzlose, 1975).
The idea of an independent and specialized trophic
pathway based on scavenging was first put forward by
Isaacs (1969). He envisaged a trophic pathway quite
independent from that of carnivores and organisms
exploiting the rain of fine detrital particles (Haedrich
and Rowe, 1977). This idea of divergence in trophic
strategies has also been developed by Mahaut et al.
(1990). However, for deep-sea fishes, the very substantial body of data that has accumulated from studies on
diet, particularly in the large and widely spread family
Macrouridae, and in sharks and chimaeroids, does not
support the great importance of scavenging (Mauchline
and Gordon, 1986; Merrett and Haedrich, 1997). As
predators, opportunism seems to play an important
part in foraging strategies of many species, as much
as specialized trophic behaviour targeting preferred
prey. Hence the evidence that deep-sea benthopelagic
fish may play an important rˆ ole as scavengers is still
equivocal. Merrett and Haedrich (1997) have argued
that predation by fish on pelagic organisms impinging
on the bottom at slope depths, as discovered by
Mauchline and Gordon (1991) and, in deeper water,
on suprabenthic invertebrates in the benthic boundary
layer, is more important.
For invertebrates, the evidence from dietary studies
is much more fragmentary, and morphological and
behavioural data have as yet failed to provide the
definitive evidence that even species as highly adapated
as large lysianassid amphipods rely entirely on scavenging for their nutrition. This view is supported in
the important review of marine carrion and scavenging
by Britton and Morton (1994), on the basis that
as a food source it is too ephemeral, and in any
case there would be too little of it available to
encourage evolution of obligate scavengers. Although
lysiannasid amphipods, and perhaps hagfish, approach
this concept most closely, the unpredictability and very
low density of natural carrion favour the evolution
of facultative, rather than obligate, marine scavengers.
Because most carrion comes from the surface, the
observed increasing importance of scavenging with