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AMER. ZOOL., 22:647-659 (1982)
The Role of Dissolved Organic Matter in the
Nutrition of Deep-Sea Benthos1
ALAN J. SOUTHWARD AND EVE C. SOUTHWARD
Marine Biological Association of the United Kingdom, Citadel Hill,
Plymouth, Devon, PL1 2PB, United Kingdom
SYNOPSIS. Deep-sea sediments contain less particulate organic matter and lower biomass
than shallow-water sediments, but the dissolved organic matter in pore water varies less
with depth and may provide a significant food source for deep-sea benthos. Pogonophora
are a phylum of predominantly deep-sea animals, all without an internal digestive system.
Experiments show that one or two species ought to be able to live by uptake of dissolved
organic matter from pore water in deep-sea deposits: some other species may need local
enrichment of the habitat for such uptake to be useful. Less is known about nutrition of
other deep-sea animals, but dissolved organic matter may supplement a conventional diet
in several groups. Chemoautotrophy, using endosymbiotic bacteria, may be important for
the large vestimentiferan Pogonophora in the high-sulfide conditions of the hydrothermal
vents.
INTRODUCTION
We define deep-sea benthos as those animals that live on or in the sea-bed deeper
than the shelf-slope faunistic boundary,
which normally lies between 200 and 300
m (Grassle et al, 1979). The animals are
separated into macrobenthos and meiobenthos by size, usually whether or not they
are retained by a sieve with holes 0.5 mm
across (Holme and Mclntyre, 1971); megabenthos is a term loosely applied to large
animals caught in trawls or traps or seen
in bottom photographs. All deep-sea animals apart from Pogonophora have an apparently functional alimentary canal, and
would be expected to eat organic particles
or living prey. However, there are few observations on live animals and the type of
food has to be deduced from stomach contents or comparative morphology. On the
basis of deduced feeding habits the proportion of deposit feeders changes with
depth and distance from the coast, and a
characteristic zonation of feeding type has
been described (Sokolova, 1972). This
trophic zonation is most obvious in the
Pacific, where abyssal regions with very
poor food supply are reported to have a
' From the Symposium on The Role of Uptake of Organic Solutes in Nutrition of Marine Organisms presented
at the Annual Meeting of the American Society of
Zoologists, 27-30 December 1980, at Seattle, Washington.
dominance of suspension feeders in an
otherwise sparse population of macrobenthos (Filatova, 1969; Sokolova, 1969; but
see Hessler, 1974). Both trophic relations
and depth are important in controlling the
distribution of deep-sea benthos and great
care is required in assigning a species to
its trophic niche.
The environment of the deep-sea is better known than the biology of the animals:
hydrostatic pressure is high, temperatures
are low, and average water currents slight
(Marshall, 1979). The deep-sea floor is
mainly fine sediments, and there is little
solid substratum other than manganese
nodules except near the continents and at
the mid-ocean ridges where rocks are exposed. Biologically the deep-sea bottom
differs from shallow water in having less
organic matter, fewer bacteria (Sorokin,
1970, 1972a; Morita, 1979) and a lower
biomass of macrofauna. The biomass of
meiofauna and Pogonophora changes less
with depth and these groups become relatively more important (A. J. Southward,
1975; Thiel, 1979). Metabolism and growth
rates are slower at all levels of organization
(Smith, 1978; Allen, 1979; Jannasch, 1979).
The high pressure should have little
general effect on the benthic invertebrates
since their body fluids will be at ambient
pressure and they are without flotation organs. However, pressure can alter molecular volume, and this may influence metabolism and behaviour (Brauer, 1972).
647
648
A. J. SOUTHWARD AND E. C. SOUTHWARD
Enzymes of shallow water species can be
inactivated, and shallow water microorganisms can show reduced uptake and use
of dissolved organic matter (DOM), when
compressed (Paul and Morita, 1971). On
the other hand, deep-sea animals that have
been studied possess enzymes whose structure allows them to function under pressure (Low and Somero, 1975). We can presume that intestinal absorption must be
efficient in deep-sea animals, hence epidermal uptake of DOM need not be more
difficult in the deep-sea than in shallow
water.
The temperature in the deep sea is no
lower than shallow arctic and boreal seas,
but is less variable. The few studies on the
temperature coefficient of uptake of DOM
give conflicting results. Uptake rates do increase with rising temperature, but acclimation may alter the rate in either direction (Schlichter, 1975; Shick, 1975; Tempel
and Westheide, 1980). Experiments on uptake of DOM by deep-sea species have been
carried out successfully at environmental
temperatures of 4-6°C, so we suppose that
the animals are adapted to their environment.
In deciding the nutritional role of DOM
in the deep-sea great importance attaches
to the Pogonophora (including Vestimentifera). This phylum is found mainly in the
deep-sea and none of the known representatives has an internal digestive system
(Ivanov, 1963; Webb, 1969; E. C. Southward, 1975; van der Land and N^rrevang,
1977). This offers a strong presumption
that nutrition takes place through the epidermis, in solution.
T H E SUPPLY OF ORGANIC MATTER
IN THE DEEP SEA
Input of paniculate and dissolved material
Deep-sea organisms are assumed to depend on production of organic matter near
the surface, in the euphotic zone. In the
open ocean, away from land, it is supposed
that organic matter reaches the bottom in
three ways: 1) as infrequent "large lumps,"
the rapidly sinking carcasses of large fish
and cetaceans which are unlikely to be totally consumed by scavengers on the way
TABLE 1. Examples of input of particulate organic matter
to deep-sea sediments compared with metabolic needs of the
benthic fauna."
Input of
particulate
carbon,
g/mVyr
In situ
Calculated
input
of carbon
respiration
as O ; uptake
in ml/m2/hr
for oxygen
uptake
Upper slope
1,050-1,350 m 4.4-10.9
1.31"
Lower slope
1,850-3,650 m 2.0-6.4 0.24-0.50
Abyssal plain
4,670-5,582 m 0.24-0.62 0.02-0.09
6.14
1.12-2.34
0.09-0.42
"Smith, 1974, 1978; Wiebe el ai, 1976; Hinga el
al, 1979; Knzuer etai, 1979; Miiller and Suess, 1979;
Rowe and Gardner, 1979; Deuser and Ross, 1980;
Honjo, 1980.
b
For nearshore sediment only (San Diego Trough).
down; 2) as a "rain" of small particles,
mostly faecal pellets; and 3) in solution, in
a form which may or may not be available
for nutrition (Krogh, 1934). The "large
lump" contribution has not yet been seen
from manned submersibles, though baited
cameras and traps show how the megafauna and some smaller epifauna can congregate on and eat such "lumps" when they
are supplied (Isaacs and Schwartslose,
1975; Rowe and Staresinic, 1979). The
"rain" of small particles has been measured in several places with moored traps.
Sinking rates are of the order of 100
m/day and the amount reaching the bottom is related to surface production and
inversely to depth (Shanks and Trent,
1980; Suess, 1980). Although 20% of daily
production (measured as carbon fixed)
sinks below the euphotic zone, only about
1% reaches 3,000 m and only about 0.4 g
carbon/mVyr reaches the abyssal plain (Table 1). We can also compare the input of
organic matter to the bottom at different
depths with the biomass of the fauna. The
biomass values quoted by Filatova (1969),
Rowe (1971) and Menzies et al. (1973) show
a clear relation to depth. Below the faunistic boundary between shelf and slope, the
biomass per unit area decreases exponentially with depth so that at 1,000 m there
is 1% and at 3,000 m onlv 0.1% of the bio-
DOM
AND NUTRITION OF DEEP-SEA BENTHOS
mass on the bottom of shallow seas. The
benthic biomass is thus related to surface
production of organic matter and the proportion of it that reaches the bottom (Filatova, 1969; Rowe, 1971; Vinogradova,
1979; Suess, 1980). There are two other
sources of organic matter. One is evident
where ocean depths come close to land, in
canyons that dissect the slope, in deep-sea
trenches or in basins close to continents.
In such places benthic samples contain
much terrestrial plant debris, including
leaves, root masses and tree trunks, and
the supply is regular enough to support a
specialised fauna (Wolff, 1979). A further
supply of organic matter to the deep-sea
may be through chemoautotrophy. This
possibility, based on the existence of microorganisms that can use energy derived
from the oxidation of sulfide and other reduced inorganic compounds to fix CO2 and
inorganic nitrogen into organic matter, was
first suggested by Ekman (1953), quoting
work by Benecke. More is now known
about bacterial chemoautotrophy (Schlegel, 1975), but organic matter produced in
this way is usually only a form of secondary
production, since the reduced inorganic
compounds are formed by anaerobic decomposition of organic matter originally
produced by photosynthesis (Fenchel and
Riedl, 1970; Sorokin, 19726). Cycling organic matter in this way may increase its
stay in the sediment, but does not add to
the total. However, in the deep sea there
are autochthonous sources of reduced
compounds at hydrothermal vents in rift
zones (Corliss et al., 1979; RISE Project
Group, 1980). This "crustal" input of hydrogen sulfide sustains a flourishing growth
of microorganisms and of animals which
feed on them or take up the DOM which
they produce (Karl et al., 1980). Chemoautotrophic bacteria also appear to exist as
endosymbionts in some of the higher animals around the vents (Cavanaugh et al.,
1981; Felbeck, 1981), with the possibility of
direct nutrient transfer to the host, analogous to that in shallow water animals that
contain zooxanthellae (Smith, 1979). The
hydrothermal vents may not be the only
source of "crustal" energy. Some parts of
the oceans have a circulation of sea water
649
within the sediments, down to basement
rock (Langseth, 1980); the slow return flow
might carry reduced compounds for chemosynthetic production on a smaller scale
than at the vents.
Amount of DOM in the deep-sea
There are few realistic measurements of
the DOM content of pore water from deepsea sediments. Many estimates are of total
DOM content of sediment samples, or else
the method of extraction of the pore water
is not described. Harsh chemical extractants, high temperatures and prolonged
slurrying have all been used, but even gentle
suction or pressure can cause contamination by tissue fluids or cytoplasmic solutes
from animals and microorganisms. With
these reservations, there is more DOM in
deep-sea sediments than in the water above,
but no consistent decrease with depth as
with paniculate fall-out or total biomass.
The total DOM in sea water varies from
0.5 to 3 mg carbon/liter according to the
method of analysis (Krogh, 1934; Plunkett
and Rakestraw, 1955; Degens, 1970; Starikova, 1970), but there is twice as much in
surface waters as in the deep-sea (Williams,
1975). The amounts quoted correspond to
concentration range of a few to 100 \xMI
liter. Nitrogenous compounds make up
most of this, but only 10% has been fully
identified (Degens, 1970; Mopper and Degens, 1972), and there is controversy over
how much of it is complexes of high molecular weight and whether it is available
to microorganisms (Hamilton et al., 1970;
Williams, 1970; Sorokin, 1972a). However,
there is no doubt that analyses for specific
compounds show low concentrations, often
in the nanomolar range (Degens et al.,
1964; Vaccaro et al., 1968; Degens, 1970;
Johnson and Sieburth, 1977), suggesting
that the deep-sea water is not a significant
source of DOM for uptake.
The pore water from deep-sea sediments contains at least ten times more
DOM than the overlying water (Starikova,
1970; Tanone and Handa, 1980), and a
greater proportion of it is identifiable. Individual compounds are present in micromolar concentrations, with totals in the
millimolar range. For example, total free
650
A. J. SOUTHWARD AND E. C. SOUTHWARD
amino acids can reach 5.6 mg/liter, and
single amino acids 20 /uM/liter; free sugars
can total 0.4 mg/g dry weight of sediment,
and pore water values of 0.74 to 1.2 fxMI
liter have been reported (Degens et al.,
1964; Mopper and Degens, 1972; Southward and Southward, 19726, 1980; Henrichs and Farrington, 1979; Mopper etal,
1980). Evidence from oxygen consumption and sediment build-up suggests that
2 0 ^ 0 % of the particulate fall-out becomes
buried in the sediments (Rowe and Staresinic, 1979; Suess, 1980). Metabolic activity
of deep-sea bacteria is low (Morita, 1979),
with a low rate of breakdown of organic
matter in the sediments. There should thus
be a pool of buried or "historic" POM
undergoing slow conversion to DOM,
which then leaches out of the upper layer
of sediment (Suess, 1976; Williams et al,
1980). Most bacterial activity is found in
the upper 20 cm of sediment; lack of activity deeper is attributed to anoxic conditions, and it is held that anaerobic breakdown of "stable" organic matter is
"energetically unprofitable at low temperatures" (Sorokin, 1970, 1972a). A more recent view takes into account bioturbation
of sediments (Rowe etal., 1974; Henrikson
et al., 1980) and its effect on DOM. Almost
all photographs of the deep-sea floor show
burrows, excavations and faeces in various
stages of erosion and decomposition (Heezen and Hollister, 1971), and in some places
the surface mud consists almost entirely of
faecal matter undergoing continuous turnover by the benthos (personal observations). Turnover of the upper layers of deposit may account for the depth of bacterial
activity and provide continual replenishment of DOM.
To sum up: deep-sea sediments have
much less POM and less DOM than shallow sediments, but there is still a considerable amount of DOM which could provide a significant source of food. However,
compared to shallow water, the deep-sea
habitat as a whole is oligotrophic, and thus
all sources of energy, including POM, DOM
and chemoautotrophy have to be regarded
as potential food for the benthos; they
might even all be used by one individual.
NUTRITION OF THE POGONOPHORA
The Pogonophora differ from most other free-living Metazoa in being without any
internal digestive system (Ivanov, 1963,
1975). A few other metazoans do exist
without a gut in the adult stage, or with a
reduced gut, notably a polychaete, some
oligochaetes, a bivalve mollusc and some
brachiopods (McCammon and Reynolds,
1976; Erseus, 1979; Jouin, 1979; Reid,
1980), but these are rare examples compared with the whole phylum Pogonophora. Thus, examination of the nutritional
status of the Pogonophora affords a critical test of the role of DOM in general, as
well as in the deep-sea.
Uptake of DOM by Pogonophora
Pogonophora are widespread geographically, but are found mainly in the deepsea. The large species that occur below
2,000 m are difficult to locate and virtually
impossible to recover alive (cf., Menzies et
al., 1974). Hence experiments on uptake
of DOM have been confined to the small
species from shallower than 2,000 m, including one form that penetrates into cold
shelf waters (Table 2). Uptake of DOM was
studied using 14C and 3H labelled compounds. Except in one instance total flux
was not measured, since the animals are
very small and it is difficult to show a significant experimental reduction in ambient DOM.
The species examined show individual
and specific variation in uptake of DOM,
but they can accumulate amino acids (including alanine, glutamic acid, glycine and
phenylalanine) and glucose from concentrations between 1 and 10 /LtM/liter (refs.
in Table 2). Lesser quantities of other compounds (galactose, mannose, acetic acid,
butyric acid, palmitic acid, lactic acid and
glycolic acid) are accumulated, but not apparently fructose or mannitol. The neutral
amino acids are absorbed against a concentration gradient, probably by a carrier-mediated mechanism, and similar mechanisms may exist for other amino acids and
for glucose.
DOM is taken up by all regions of the
651
DOM AND NUTRITION OF DEEP-SEA BENTHOS
TABLE 2. Species of Pogonophora investigated for ability to take-up DOM.
Typical
wet weight,
mg
Species
Siboglinum mergophorum Nielsen
(and Oligobrachia floridana Nielsen)
Siboglinum atlanticum
1.0
15
Southward & Southward
Siboglinum ekmani Jagersten
0.2
Siboglinumfiordicum Webb
1.0
Sclerolinum brattstromi Webb
0.1
Locality sampled
and depth, m
References
Florida Straits
185
Bay of Biscay
1,500-2,000
Raunefjorden and
Korsefjorden
300-750
Ypsesund and Fanafjorden
30-35
Korsefjorden
700-750
body, but the postannular part accumulates amino acids at Mi or less the rate for
the preannular region; the tentacle accounts for a larger proportion of the soluble fraction accumulated by the preannular region than would be expected on a
simple volume basis (Southward and
Southward, 1970). The uptake rates for
different species differ by one or two orders of magnitude, apparently unrelated
to depth (Table 3). Siboglinum ekmani from
700 m has the highest rate of uptake of
both amino acids and glucose. S. fiordicum
Little and Gupta, 1968
Southward and Southward,
1968, 1970, 1972*
Little and Gupta, 1969; Southward and Southward, 1970,
19726, 1980
Southward and Southward,
1970; Southward et al, 1979
Southward and Southward,
1980
from only 30 m has the lowest uptake of
amino acids, while S. atlanticum from 1,800
m and Sclerolinum brattstromi from 700 m
have similar, low, rates of uptake of glucose. These species also differ in content
of free amino acids and in kinetics of uptake, so they probably differ in metabolism
and way of life. A different way of life is
obvious for S. brattstromi; like some other
species of Sclerolinum (Southward, 1972), it
lives in organic substrates such as rotting
wood, rope and paper.
Most of the compounds taken up by the
TABLE 3. Rates of uptake of four classes of dissolved organic compounds by four small pogonophores."
Compound
Amino acids
Glucose
Species
Sclerolinum brattstromi
Siboglinum ekmani
S. fiordicum
S. atlanticum
Sclerolinum brattstromi
Siboglinum ekmani
S. fiordicum
S. atlanticum
Fatty acids, long chain
Siboglinum ekmani
S. fiordicum
Fatty acids, short chain;
and hydroxy acids
Siboglinum ekmani
S. fiordicum
a
Mean uptake
rate" (nAf/g/hr)
from 5 /xjw/liler
16
110-240
4
38
2
130
9
6
20
1.3
7
7
Environmental
concentration
{/JLM /liter)
Nutritive
valued
(% O, cons.)
12.2
12.9
(5)
61
45
4
4.9
6.5
1.2
30
1
1
12
11
(5)
(5)
(5)
(5)
16
15
Based on Southward and Southward, 1981.
Uptake rate for a "standard environmental concentration" of 5 /xJW/liter.
Measured, or (estimated) from published data.
d
Calculated nutritive value, as % contribution to O2 consumption made by uptake from environmental
concentration.
b
c
652
A. J. SOUTHWARD AND E. C. SOUTHWARD
pogonophores enter into the metabolism,
and are converted to other soluble and insoluble compounds, or respired (Southward et al., 1979; Southward and Southward, 1980). Autoradiographs of sections
of animals exposed to labelled amino acids
and glucose show good localization of label
in storage and secretory cells (Southward
and Southward, 1968, 19726; unpublished
observations). There is thus little doubt that
the animals were "feeding" under the experimental conditions, but the experiments do not show if they can grow under
the same conditions. Growth of a pogonophore was observed by Bakke (1977), who
reared Siboglinum jiordicum from larva to
juvenile over a period of 398 days at 6°C.
Measurements from drawings of the preserved specimens show that growth was
slow, but that volume increased by a factor
of 8 and length by a factor of 15 in this
time. The only source of nourishment was
a small amount of mud from the habitat,
frozen and thawed before use, and a slow
flow of sub-thermocline water, cleared by
sedimentation. This study does not prove
that DOM alone is sufficient for growth,
since chemoautotrophy could also have occurred, but it does indicate that POM is
unlikely to be food for these small pogonophores.
Nutritional status of the Pogonophora
The small pogonophores are usually
damaged by loss of the hind end during
capture, and do not appear to show "feeding behaviour" in the laboratory (Southward and Southward, 1963, 1981). Their
nutritional status has to be deduced from
the experiments reviewed above and from
morphology and distribution. There are
four hypotheses to be considered: 1) that
particles filtered from the water by a crown
of tentacles, or collected by a single tentacle, are digested among the tentacles or in
the coiled-up tentacle, possibly after withdrawal into the tube, and that the dissolved
products are taken up by the epidermis of
the tentacle. This hypothesis is deduced
from the morphology of the multitentacular species, but is unsupported by evidence for food collection or digestive secretion; 2) that pinocytosis of large molecules
(proteins etc.) occurs at the surface of
epidermal cells. This process has been
demonstrated (Little and Gupta, 1968,
1969; personal observations), but the
species shown to have this ability seem to
spend most of their time inside the tube,
which is permeable only to small molecules
(Southward and Southward, 1963). Pinocytosis could be more useful to species that
extend their tentacles outside the tube, such
as the large Vestimentifera. The choice at
the moment lies between hypothesis 3) that
DOM is a significant source of food; and
hypothesis 4) that chemoautotrophy is significant; or else a combination of the two.
As we have more data on uptake of DOM
this will be considered first.
DOM in pore water, or at the sediment/
water interface will be able to pass through
the wall of the tube and be available for
uptake at the microvillar surface of the
epidermis. A wide capability for uptake of
DOM has been demonstrated experimentally in small pogonophores, and it can take
place with the animals in situ in the tube.
We can calculate the nutritional value of
DOM by comparing the amount of a compound taken up from a concentration equal
to that measured in the environment with
the amount of the same compound that
would be needed to account for the measured oxygen consumption of the species
(cf., Stephens, 1968). It is assumed that the
compound is efficiently deaminated and
fully oxidised, and that the oxygen consumption in nature is the same as that
measured in vitro. The effect of one compound on uptake of another has to be allowed for, and uptake rates and environmental concentrations have to be estimated
for some compounds not fully quantified.
The figures for individual contributions by
the compounds are then summed to give
a total potential contribution of DOM to
nutrition (Table 4). This sum does not take
into account the extra DOM that would be
needed for growth and reproduction (Sepers, 1977).
Only one pogonophore, S. ekmani, has a
mean uptake of DOM high enough for the
sum of all contributions to exceed 100%,
and thus show that it could live entirely on
DOM at the concentration measured in the
DOM AND NUTRITION OF DEEP-SEA BENTHOS
TABLE 4. Potential contribution of DOM to metabolic needs
of Pogonophora.
Species
Siboglinum ekmani
Siboglinum fiordicum
Siboglinum atlanticum
Sclerolinum brattstromi
% of oxygen consumption
equivalent to DOM taken
up at environmental
concentration
119a
73"
30°
30 c
a
From Southward and Southward, 1980.
From Southward et al, 1979.
0
Approximate value, based on fewer experiments
than with S. ekmani and S. fiordicum.
b
pore water. S.fiordicumshows a deficiency
of 30% on the mean uptake rates, but this
can be changed to a positive value if the
calculations are confined to the "best" individual results. This species had a very
wide range of individual uptake rates, and
standard deviations up to 100% of the
mean were found; removal of the low values, by assuming these particular animals
were in poor condition, balances the budget. The apparent budget deficiency for
the other two species cannot be balanced
in this way. However, for Sclerolinum we
have used environmental concentration
data for pore water of mud samples,
whereas this species lives in rotting wood
etc., not free in the mud. Mopper and Degens (unpublished Wood's Hole Technical
Report No. 68, 1972) report that as much as
15% free sugars (25 /xM/g) can be extracted
from rotting wood from anoxic deposits.
If we assume a local concentration of DOM
greater than 100 /xM/liter in the habitat of
Sclerolinum, then the budget for this species
also balances. Local enrichment could also
occur if pogonophores lived in association
with other organisms in the community,
including bacteria (Jagersten, 1957; Southward et al., 1979; Southward and Southward, 1981). For example, the pogonophores could produce local oxygenation of
the deposit to benefit heterotrophic microorganisms capable of attacking refractory
organic particles (cf., Stephens, 1975). Sepers (1977) has suggested that microorganisms are inherently more efficient than
metazoans at uptake of DOM from low
concentrations, which would put the meta-
653
zoans at a disadvantage in competition.
However, there appears to be wide variation in adaptation to different levels of
DOM among microorganisms, possibly related to microscale variations in concentration (Taylor and Williams, 1975; Williams,
1981). Therefore in the real world species
with widely differing rates of uptake may
be able to coexist.
At present most of the evidence for chemoautotrophy is provided by experiments
with tissue samples from the very large
species of Vestimentifera which live close
to the hydrothermal vents in the Pacific.
These animals have three enzymes associated with the oxidation of sulfide and two
associated with CO2 fixation via the Calvin
cycle (Felbeck, 1981), and a ratio of carbon
13 to carbon 12 consistent with direct use
of "crustal" energy rather than digestion
of bacteria (Rau, 1981). Anatomical studies
show the presence of bacteria (Cavanaugh
et al., 1981) in the trophosome tissues
where the enzymes have been detected. Elemental sulfur particles have also been seen
in this tissue (Felbeck, 1981), and Arp and
Childress (1981) link the rather high oxygen consumption rate of the whole animals
to the possibility of chemoautotrophy. This
evidence, coupled with the restriction of
the giant Vestimentifera to sulfide-rich
vents suggests that the sulfide-oxidising and
carbon-fixing enzymes belong to endosymbiotic microorganisms, on which the animals depend for nutrition (Felbeck, 1981).
However, we must remember that the vestimentiferans have a crown of many thousand fine tentacles which could provide a
large surface area for uptake of DOM,
hence there could be a combination of two
types of "feeding."
The small pogonophores are not associated with noticeably high levels of sulfide
(Southward et al., 1979), though they occur in deposits which are probably anoxic
below the upper few mm. We find (Southward et al., 1981) that some of them have
bacteria-like inclusions in the peritoneal
cells of the postannular region. Tissue extracts of S. atlanticum contain two Calvin
cycle enzymes (ribulose phosphate kinase
and ribulose biphosphate carboxylase). The
latter is also present in extracts of S.fiordi-
654
A. J. SOUTHWARD AND E. C. SOUTHWARD
T A B L E 5. Dei'.p-sea
Species
metazoan species, otherthan Pogonophora, tested for ability totake up DOM.*
Compound
Maldanid polychaete
Amino acids
(mixed)
Plutonaster sp.
Glucose
Tharyx sp.
Glycine
1
Locality and depth
N. Bay of Biscay
1,800 m
N. Bay of Biscay
1,800 m
Korsefjorden
700 m
Ratio of uptake of DOM
by this species to uptake
of DOM uy pogonophore
species from same place
1.16
2.09
0.27
Southward and Southward, 1972a, 1980.
cum, but not apparently in S. ekmani. A few
experiments with the intact animal suggest
that in S. fiordicum fixation of CO2 might
provide 20 times more carbon than is provided by the low rate of uptake of glucose
by this species. If all the fixation of CO2 was
made available to the host, in addition to uptake of DOM, then the nutritional budget
would be near balance. It is, of course, possible that the observed uptake of DOM is part
of a mechanism whereby the host induces
the symbiont to part with some of its manufactured organic compounds. The role of
photosynthetic algae present in invertebrate tissues is not fully understood yet
(Smith, 1979): a similar controversy seems
likely over the symbionts in pogonophores,
since it is quite easy to postulate a role for
bacteria in removal of harmful sulfides (cf.,
Theede et ai, 1969; Powell et ai, 1979),
which might diffuse inward from the anoxic surroundings of the posterior part of
the animal.
and the starfish from the Bay of Biscay have
uptake rates of the same order of magnitude as those of S. atlanticum. All three
species can be assumed to be capable of
obtaining some part of their nutritional
needs by uptake of DOM, though all have
apparently functional digestive systems. For
deep-sea species in general some deductions can be made from what is known
about the uptake abilities of their shallow
water relatives. Groups with an impervious
cuticle such as Arthropoda and Nematoda
can be excluded; soft-bodied animals with
large surface areas in proportion to body
volume may have significant uptake of
DOM. In this category in the deep sea we
could include most of the meiofauna, longbodied worms, animals with long tentacles,
bivalve molluscs and some echinoderms.
Shallow water
There is now a large body of literature
on uptake and incorporation of DOM by
shallow water invertebrates (Stephens,
COMPARISON OF UPTAKE OF DOM BY
1968,1981;J(zfrgensen, 1976; Sepers, 1977;
POGONOPHORA AND OTHER INVERTEBRATES
Stewart, 1979). We have compared uptake
Deep-sea
by intertidal polychaetes with uptake by
The few deep-sea animals tested for pogonophores (Southward and Southability to take up DOM were all collected ward, 1972a, 1980). In general, uptake
with pogonophores (Table 5). Since only rates by shallow water invertebrates vary
one species was tested from each habitat between species and between groups over
and there is specific as well as individual a range of at least two orders of magnivariation in uptake capacity, caution is tude. Calculations of potential contribuneeded in assessing these results. The tion of DOM to nutrition range from only
polychaete Tharyx takes up glycine at only a few % in the meiofauna of coarse sands
25% of the rate shown by S. ekmani, but its (Tempel and Westheide, 1980) to over
rate is still quite high compared with other 200% in polychaetes from fine deposits
species of Pogonophora. The polychaete with high organic content (Costopulos et
DOM
AND NUTRITION OF DEEP-SEA BENTHOS
655
ai, 1979). In effect, the ranges in uptake 1967, 1980; Shick, personal communicarates in Pogonophora and other inverte- tion). In contrast to this flexible policy, the
brates are quite similar (Southward and Pogonophora would appear to have beSouthward, 1980).
come specialized for a trophic niche that is
not fully exploited by other metazoans: but
DISCUSSION AND CONCLUSIONS
if reliance is placed on DOM alone, then
In comparison with other invertebrates there must be a lower limit of environfrom deep-sea and shallow-water habitats mental DOM below which survival is not
there seems to be nothing exceptional about possible. From experiments on total flux
the ability of Pogonophora to take up of primary amines in shallow water aniDOM. Contrary to previous statements (A. mals (Stephens, 1980) this lower limit of
J. Southward, 1975), it seems that loss of DOM can be placed in the range from 1
an internal digestive system has not been to 5 juM/liter, which is close to the K, conaccompanied by any great improvement of centrations found for the best investigated
the mechanism for epidermal uptake of pogonophore. The distribution of pogonDOM. Animals from the rich conditions at ophores suggests they are limited by orhydrothermal vents or from the special- ganic content of the habitat, since they are
ized wood-eating community show faster most abundant on steep slopes and in
growth (Turner, 1973; Turekian et al, trenches close to land masses where there
1979) than their relatives from the low or- is increased fall-out of organic matter from
ganic environment of the abyssal plain. The coastal regions and the land, and where
latter, with their slow metabolism and disturbance of the deposits by slumping
growth rate, can be assumed to be adapted and currents may help maintain the supply
to oligotrophic conditions, or to be show- of DOM. Pogonophora are notably absent
ing a phenotypic response (Marshall, 1979). from the abyssal plains where the panicWe may suppose that the Pogonophora are ulate input and biomass are low (p. 649).
also adapted to or are responding to oli- Other invertebrates can live in such exgotrophic conditions in their normal hab- tremely oligotrophic conditions, though
itat {i.e., other than at the vents or in or- Pogonophora cannot, hence there may be
ganic substrates). Their mechanism for some advantage in being able to use more
uptake of DOM must function at low tem- than one source of food.
peratures as well as at low concentrations.
This leads to consideration of the hyIn Siboglinum ekmani the rates of uptake of pothesis that the Pogonophora are also
DOM are quite high at its normal ambient polytrophic, but combine uptake of DOM
temperature (6°C), and the concentration with some reliance on endosymbionts caat which uptake is half-maximal (Kt) is gen- pable of producing organic matter by cheerally lower than is found in shallow water moautotrophy. At one extreme we have the
benthic animals, varying from 0.64 to 6.25 high-sulfide conditions at the hydrother/xM/liter for all compounds other than ace- mal vents, where growth is more rapid than
tic acid (Southward and Southward, 1980). elsewhere in the deep-sea, and where the
Adjustment of the metabolism and the up- giant Vestimentifera may rely mainly on
take process to low temperatures may have their endosymbionts. At the other extreme
enabled the Pogonophora to dispense with we have the conditions of the Atlantic conan internal digestive system, and thus avoid tinental slope, where only small pogonoenergy wasted in its maintenance.
phores live, and where reduced sulfur
compounds
must be derived mostly by anIn contrast, the other deep-sea animals
have kept the capacity for internal diges- aerobic breakdown of organic matter which
tion, though some of them may also nour- has come from the sea surface or the land.
ish their epidermis by direct uptake of In such places it might be more efficient
DOM, while at the same time filling the to use DOM directly as the main energy
stomach with mud or other food, as in some source rather than the indirect products of
shallow-water echinoderms (Ferguson, the sulfur cycle.
656
A. J. SOUTHWARD AND E. C. SOUTHWARD
starfish on epidermal uptake of dissolved organic
matter. Comp. Biochem. Physiol. 66A:461 —465.
We thank Dr. P. R. Dando for infor- Filatova,
Z. A. 1969. Quantitative distribution of
mation and discussions on metabolism and
deep sea benthic fauna. In L. Z. Zenkevich (ed.),
Drs. A. Arp.J. J. Childress, H. Felbeckand
The Pacific Ocean, Vol. 7, part 2, pp. 234-252.
Engl. transl. U.S. Naval Oceanographic Office,
G. Rau for pre-publication data on experWashington, D.C. 1970.
iments with the large Vestimentifera from
J. F., H. L. Sanders, and W. K. Smith. 1979.
the Galapagos Rise; The Royal Society Grassle,
Faunal changes with depth in the deep-sea benprovided part of the travel expenses for
thos. Ambio, Spec. Rept. 6:47-50.
one of us (E.C.S.).
Hamilton, R. D., O. Holm-Hansen, and J. D. H.
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