352
John D. GAGE
per day from the sediment surface (Graf, 1989).
Jumars et al. (1990) suggested that this behaviour
may be characteristic in the deep sea in order to
sequester or hoard scarce food resources away from
smaller, often specialized, meiofaunal organisms, such
as Foraminifera. Hoarded material may be in the form
of faecal pellets, or as labile food plastered to the
burrow lining so that it is available for re-assimilation
later when resources are scarce at the sediment surface.
Although this is an appealing idea, it may be more
important for animals to ingest seasonal bonanzas
immediately, for conversion to reproductive production
(see Tyler et al., 1992, 1994).
Pulsed variability in organic flux to the bottom, not
surprisingly, has been linked to seasonal variability in
responses at the population level, such as reproduction,
recruitment and growth (Gage and Tyler, 1991; Tyler
et al., 1994), and possibly macrofaunal–microbial
interactions (C.R. Smith, 1994). The larger elements
of the benthic community, with lifespans that may
encompass several pulsed detrital inputs, may also
respond in terms of accelerated somatic growth. In
shallow-water fauna this is frequently expressed as
banding patterns in the growth of skeletal elements
such as mollusc shells. Such seasonal variability in
growth provides a useful age marker, which has been
used in numerous studies of population dynamics based
on unbiased samples aged by this method, or on growth
trajectories back-calculated from the pattern of skeletal
zones. In the deep sea, similar growth-zone patterns
occur across a broad range of fauna (e.g., Gage,
1987, 1990, and unpublished data; Gage and Tyler,
1985). These growth marks reflect the fact that growth
is typically intermittent, responding to the increased
availability of food after detrital maxima.
Data on behavioural differences have also started
to emerge. Motile epibenthic megafauna, such as
echinoids and holothurians, monitored with time-lapse
photography were twice as active in the presence of
detrital aggregates on the sea floor in the abyssal Pacific
(K.L. Smith et al., 1994). De Wilde et al. (1998), on
the European continental rise off Ireland, noted that
large, motile ’vacuum cleaner’ holothurians, such as
Psychropotes, were plentiful on the bottom when heavy
deposition occurred, but were absent at the same time
the following year when no deposition occurred. It
is possible that the animals may migrate to areas of
deposition, which may have a patchy distribition in
the area, but whether long-distance olfaction may be
involved as suggested by De Wilde et al. (1998) needs
further evidence.
Response of larger, non-deposit-feeding size
classes
Predators constitute a higher link in the food chain,
less directly connected to variability in organic input
than the consumers of passive organic inputs such as
carrion or large plant remains; but there are few data
on predators in the deep ocean. The benthopelagic
fauna, which includes macrobenthic organisms such as
peracarid crustaceans, makes up an important part of
the diet of motile megabenthos such as larger decapod
crustaceans and fish such as macrourids. Population
increases in some of these prey groups have been linked
to variability in advected organic flux on the continental
slope in the western Mediterranean, and this results
in increased abundance of benthopelagic predators
(Cartes, 1998). That episodic flux may also affect even
larger size classes higher up the food chain may explain
seasonal changes in response times of scavenging
grenadiers to bait detected by using acoustic tracking
techniques (Priede et al., 1994b), although how such
effects are mediated remains unknown.
Response to interannual variability in organic
flux
As seasonal changes have become better understood
over the past 15 years, so opportunities have been
provided from the long-term time-series mentioned in
previous Sections to make between-year comparisons
in order to detect any interannual variability in the
deep-sea benthic system. Such data are very difficult
and costly to obtain, and resolution is usually poor.
But just sufficient is available, particularly from the
Northeast Atlantic and Northeast Pacific to provide
strong indications of long-term variability in the
benthic populations, which is most likely driven by
interannual variability of organic flux to the deep-sea
bed. For example, data from the long-term studies
at Station ‘M’ off California by K.L. Smith and his
associates provide evidence for significant changes
over a seven-year study period in sediment community
oxygen consumption, and in the abundance of benthic
macro- and megafauna (K.L. Smith and Druffel, 1998;
K.L. Smith and Kaufmann, 1999; Drazen et al., 1998;
Lauerman and Kaufmann, 1998). Dramatic changes
in relative abundance of invertebrate megafauna have
also been recorded on the Porcupine Abyssal Plain at
the BENGAL site (Billett et al., 2001). Abundance
John D. GAGE
per day from the sediment surface (Graf, 1989).
Jumars et al. (1990) suggested that this behaviour
may be characteristic in the deep sea in order to
sequester or hoard scarce food resources away from
smaller, often specialized, meiofaunal organisms, such
as Foraminifera. Hoarded material may be in the form
of faecal pellets, or as labile food plastered to the
burrow lining so that it is available for re-assimilation
later when resources are scarce at the sediment surface.
Although this is an appealing idea, it may be more
important for animals to ingest seasonal bonanzas
immediately, for conversion to reproductive production
(see Tyler et al., 1992, 1994).
Pulsed variability in organic flux to the bottom, not
surprisingly, has been linked to seasonal variability in
responses at the population level, such as reproduction,
recruitment and growth (Gage and Tyler, 1991; Tyler
et al., 1994), and possibly macrofaunal–microbial
interactions (C.R. Smith, 1994). The larger elements
of the benthic community, with lifespans that may
encompass several pulsed detrital inputs, may also
respond in terms of accelerated somatic growth. In
shallow-water fauna this is frequently expressed as
banding patterns in the growth of skeletal elements
such as mollusc shells. Such seasonal variability in
growth provides a useful age marker, which has been
used in numerous studies of population dynamics based
on unbiased samples aged by this method, or on growth
trajectories back-calculated from the pattern of skeletal
zones. In the deep sea, similar growth-zone patterns
occur across a broad range of fauna (e.g., Gage,
1987, 1990, and unpublished data; Gage and Tyler,
1985). These growth marks reflect the fact that growth
is typically intermittent, responding to the increased
availability of food after detrital maxima.
Data on behavioural differences have also started
to emerge. Motile epibenthic megafauna, such as
echinoids and holothurians, monitored with time-lapse
photography were twice as active in the presence of
detrital aggregates on the sea floor in the abyssal Pacific
(K.L. Smith et al., 1994). De Wilde et al. (1998), on
the European continental rise off Ireland, noted that
large, motile ’vacuum cleaner’ holothurians, such as
Psychropotes, were plentiful on the bottom when heavy
deposition occurred, but were absent at the same time
the following year when no deposition occurred. It
is possible that the animals may migrate to areas of
deposition, which may have a patchy distribition in
the area, but whether long-distance olfaction may be
involved as suggested by De Wilde et al. (1998) needs
further evidence.
Response of larger, non-deposit-feeding size
classes
Predators constitute a higher link in the food chain,
less directly connected to variability in organic input
than the consumers of passive organic inputs such as
carrion or large plant remains; but there are few data
on predators in the deep ocean. The benthopelagic
fauna, which includes macrobenthic organisms such as
peracarid crustaceans, makes up an important part of
the diet of motile megabenthos such as larger decapod
crustaceans and fish such as macrourids. Population
increases in some of these prey groups have been linked
to variability in advected organic flux on the continental
slope in the western Mediterranean, and this results
in increased abundance of benthopelagic predators
(Cartes, 1998). That episodic flux may also affect even
larger size classes higher up the food chain may explain
seasonal changes in response times of scavenging
grenadiers to bait detected by using acoustic tracking
techniques (Priede et al., 1994b), although how such
effects are mediated remains unknown.
Response to interannual variability in organic
flux
As seasonal changes have become better understood
over the past 15 years, so opportunities have been
provided from the long-term time-series mentioned in
previous Sections to make between-year comparisons
in order to detect any interannual variability in the
deep-sea benthic system. Such data are very difficult
and costly to obtain, and resolution is usually poor.
But just sufficient is available, particularly from the
Northeast Atlantic and Northeast Pacific to provide
strong indications of long-term variability in the
benthic populations, which is most likely driven by
interannual variability of organic flux to the deep-sea
bed. For example, data from the long-term studies
at Station ‘M’ off California by K.L. Smith and his
associates provide evidence for significant changes
over a seven-year study period in sediment community
oxygen consumption, and in the abundance of benthic
macro- and megafauna (K.L. Smith and Druffel, 1998;
K.L. Smith and Kaufmann, 1999; Drazen et al., 1998;
Lauerman and Kaufmann, 1998). Dramatic changes
in relative abundance of invertebrate megafauna have
also been recorded on the Porcupine Abyssal Plain at
the BENGAL site (Billett et al., 2001). Abundance