AMER. ZOOL., 35:102-111 (1995)
Physiological Ecology of Sulfide Metabolism in Hydrothermal Vent and
Cold Seep Vesicomyid Clams and Vestimentiferan Tube Worms1
KATHLEEN M. SCOTT AND CHARLES R. FISHER
Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802
SYNOPSIS. The primary ecosystem-structuring organisms at many hydrothermal vents and cold seeps are phylogenetically related and quite similar
physiologically and anatomically. Vestimentiferan tube worms and Vesicomyid clams in particular all rely on chemoautotrophic sulfur-oxidizing
symbionts and have blood which binds sulfide with high affinity and
capacity. However, there are significant differences between cold seep and
hydrothermal vent environments, including large differences in flow rate
of the emitted fluid and the chemistry of that fluid. Here we review extant
data on the hydrothermal vent species, present new data on the physiologically relevant chemical microhabitat of cold seep vestimentiferans
and vesicomyids, and compare the physiological ecology of the seep species to their hydrothermal vent relatives.
INTRODUCTION
Chemoautotrophic symbioses were first
recognized in hydrothermal vent vestimentiferan tube worms (Felbeck, 1981; Cavanaugh et al, 1981) and shortly thereafter in
vesicomyid clams (Felbeck et al, 1981;
Cavanaugh, 1983). Both harbor abundant
intracellular chemoautotrophic sulfur bacteria that can use sulfide as an electron donor
(Fisher et al, 1989; Wilmot and Vetter,
1990; Childress et al, I99la,b) and apparently provide the bulk of their hosts' organic
carbon requirements (see Fisher [1990] and
Childress and Fisher [1992] for review).
To power carbon fixation, the host organisms must provide the symbionts with a
steady supply of their redox substrates, sulfide and oxygen. Providing both substrates
can be complicated. Large pools of sulfide
and oxygen do not coexist for long, as the
two react with each other spontaneously and
sulfide in oxygenated sea water can have a
half-life of less than 20 min. (Millero, 1986).
The two substrates occur in nature in spatially or temporally segregated patches so
the hosts must somehow bridge the distance
between them. Once the host has acquired
1
From the Symposium Life with Sulfide presented
at the Annual Meeting of the American Society of Zoologists, 27-30 December 1993, at Los Angeles, California.
both substrates, it must hinder internal
spontaneous sulfide oxidation in order to
deliver a steady supply of both gases to its
symbionts (Childress and Fisher, 1992).
Described here are the microhabitats, and
the behavioral, morphological, and physiological strategies, that hydrothermal vent
and cold seep vesicomyid clams and vestimentiferan tube worms have developed to
reap the benefits of a chemoautotrophic life
style in segregated and occasionally patchy
redox environments.
HYDROTHERMAL VENT VESICOMYIDS
Calyptogena magnifica, the giant hydrothermal vent clam, nouses a dense community of chemoautotrophic endosymbiotic bacteria in its hypertrophied gills
(Fiala-Medioni and Metivier, 1986), which
average more than 17% of its wet weight
(Fisher et al., 1988a). The bacteriocytes
studding these gills are directly exposed at
their microvilli-covered apical ends to the
sea water the clam draws into its mantle
cavity and their basal ends are associated
with the blood lacuna (Fiala-Medioni and
Le Pennec, 1987). Thus the bacteriocytes
have access, at their apical ends, to dissolved gases in the sea water bathing their
mantle cavities, while their basal ends have
access to the gases present in the blood (Arp
et al., 1984). The blood is abundant (aver-
102
SULFIDE ECOLOGY OF VENT AND SEEP FAUNA
age of about Vi of the wet weight; Fisher et
ai, 1988a) and bright red from an erythrocytic hemoglobin (Terwilliger et ai, 1983).
At the East Pacific Rise hydrothermal
vents, hot, sulfide-rich, anoxic hydrothermal fluid flows from the crevasses of the
basalt substratum and mixes with sulfidefree, oxygenated bottom water (Johnson et
ai, 19886). C. magnified cluster in cracks
in the basalt to reach the dilute hydrothermal fluid seeping from these crevasses (Fig.
1; Hessler et al, 1985). Water temperature
indicates the extent to which the hydrothermal fluid has been diluted with ambient
sea water, and therefore, is a rough measure
of the sulfide content (Johnson et al., 19886).
A consistent pattern of temperature anomalies has been measured in these clam clusters (Fisher et al., 1988a). At the Rose Garden site, the water temperature near the
clams' siphons is basically ambient, indicating an absence of sulfide there (Fisher et
al., 1988a). Based on measurements made
in 1985, Fisher et al. (1988a) reported temperatures within and below the clam aggregations reflecting sulfide concentrations of
20 to 40 nM and Johnson et al. (19886)
reported direct measurements of sulfide
among and below the clams which ranged
from 6 to 95 IIM. Temperature anomalies
measured in cracks below the clams in 1988
were as high as 8.9°C, reflecting the large
pool of sulfide there.
At Clam Acres (21°N on the EPR), vent
flow in the clam bed is apparently slightly
higher than in the areas occupied by clams
at Rose Garden. Temperature anomalies
measured at the top of the clam beds there
are larger than those measured at Rose Garden, yet are still less than 1°C warmer than
ambient bottom water (Hessler et al., 1985).
Sulfide is likely present at low concentrations around the siphons of many clams at
this site. As at Rose Garden, the magnitude
of the anomalies increases with depth into
the clam bed, with an anomaly of as much
as 14°C measured 10 to 30 cm in cracks
below the clams (Hessler et al., 1985). A
consistent pattern emerges from the two
sites; sulfide is scarce if at all present around
the siphons, increasing in abundance
between the clams, while the largest pool
lies below them.
103
FIG. 1. The location and positioning of Calyptogena
magnified in the hydrothermal vent environment.
Artist's reconstruction of the habitat of the clam showing a cutaway into the fissure with temperature anomalies and theflowof sulfide, oxygen, and carbon dioxide
through the surrounding water. Temperature anomalies for Rose Garden are from Fisher et al., 19886;
those from Clam Acres are as described by Hessler et
al., 1985. Modified from Arp et al., 1984, with permission.
Clams retrieved from these two sites carry
high concentrations of sulfide in their blood.
Those from Rose Garden average 0.25 mM
sulfide (Childress et al., 19916), while those
from the more active Clam Areas site range
from 0.96 to 1.91 mM (Arp et al., 1984).
C. magnified serum reversibly concentrates
sulfide when dialyzed against a dilute solution of this gas (Arp et al., 1984). Given the
low concentrations of sulfide measured at
the siphons, the high concentrations of sulfide measured in the blood of freshly collected clams, and the sulfide concentrating
ability of the serum, Arp et al. (1984) proposed that clams accumulate sulfide from
their environment into their blood by
stretching their well-vascularized, muscular
foot down into the larger pool of sulfide
beneath their shells and delivering it to the
bacteriocytes in the gills through their open
vascular system.
Experiments with whole animals support
this model. C. magnifica can accumulate
blood pools of sulfide one to two orders of
magnitude greater than the external concentration (Fig. 2; Childress et al., 19916).
Blood thiosulfate levels are also high in
clams exposed to sulfide (Childress et al.,
19916), presumably due to host sulfide oxi-
104
K. M. SCOTT AND C. R. FISHER
i
i
symbionts may also be able to use thiosulfate as an electron donor (Childress et ah,
19916).
Using the relationship between the blood
total sulfide and environmental total sulfide
based on the whole animal data (see Fig. 2;
Childress et al, 19916), the in situ sulfide
concentrations experienced by the clams can
be extrapolated from the sulfide levels in
the blood of freshly collected clams (Childress et al, 1991ft). The concentration of
external sulfide estimated by these calculations (12 to 146 fiM) exceeds that measured in situ at the siphons, supporting the
role of the highly vascularized foot as an
auxiliary "gill" in reaching beneath the clams
deep into the basalt crevasses to tap into the
larger pool of sulfide beneath them (Childress et al., 19916).
VESICOMYIDS FROM HYDROCARBON
SEEPS AND OTHER LOW-FLUX
ENVIRONMENTS
CO
0.01
0.001
Environmental
(mM)
FIG. 2. Dependence of blood total sulfide (2H2S) and
thiosulfate concentrations on environmental 2H2S
concentration in Calyptogena magnified individuals
kept for 24 hr at constant 2H2S and greater than 130
MM O2 in flowing-water pressure (12.16 MPa) aquaria
at 8°C (Childress et al., 1991 b). Because of the log plots,
four individuals kept at zero environmental 2H2S concentrations could not be plotted. These four individuals all had 2H2S concentrations of less than 0.002
mM and thiosulfate concentrations of less than 0.007
mM. A, Crosses show 2H2S concentrations in blood;
the thinner line is a linear regression of blood 2H2S
concentrations whose equation is y = 9.05xosl, r =
0.85. The thick line is a unity line. B, Blood thiosulfate
concentrations. Data replotted from Childress et al,
19916, with permission.
dase activity (Powell and Somero, 1986) and
gill hematin (Powell and Arp, 1989). Blood
thiosulfate levels decrease quickly when sulfide is removed, which, along with carbon
fixation studies, suggests that the clam's
Vesicomyids found in low-flux environments such as cold seeps have been found
to be quite similar in physiology to C. magnified. Like C. magnifica, their gills are
packed with endosymbiotic sulfur-oxidizing chemoautotrophs and their tissue stable
carbon isotope values indicate that chemoautotrophic carbon fixation is the primary source of carbon (Fisher, 1990; Childress and Fisher, 1992).
Calyptogena elongata is sporadically
retrieved by trawls from the slightly reduced
sediments of the Santa Barbara Basin. This
organism has never been observed by submersible in situ and its microhabitat has not
been characterized. However, there is no
periostracum on their anterior ends and the
shells are discolored in this region, likely
from immersion in reducing sediments
(Fisher, 1990). The retrieval of some C.
elongata shells embedded in authigenic carbonate (a by-product of hydrocarbon biodegradation and methane oxidation, Roberts et al. [1989]) suggests that these clams
may be found in areas associated with active
seepage (CRF, personal observation).
C. elongata shows other similarities to C.
magnifica. Like its vent congener, this
organism's serum carries a sulfide-binding
SULFIDE ECOLOGY OF VENT AND SEEP FAUNA
molecule that can concentrate sulfide from
dilute solution during dialysis (Childress et
al, 1993). This compound's sulfide-binding
ability is linked to the presence of bound
zinc ion, the removal of which leaves the
molecule unable to bind sulfide (Childress
et al, 1993). Intact C. elongata, by virtue
of this sulfide-binding serum, can accumulate sulfide in its blood one to two orders
of magnitude higher than the external concentration (Fig. 3; Childress et al, 1993).
Thiosulfate levels in their blood also increase
during exposure to external sulfide (Childress et al, 1993), and like C. magnifica,
their symbionts may be able to use thiosulfate as another electron source (Childress
et al, 1993). Extrapolation of in situ sulfide
levels from the average blood sulfide concentration of freshly collected clams (5.94
mM; Childress et al, 1993) using the relationship between environmental total sulfide and blood total sulfide (see figure 3;
Childress et al, 1993) gives an estimate of
environmental sulfide levels of 0.18 mM,
which is likely found in the sediments where
they live. This is considerably higher than
sulfide concentrations measured in interstitial water from box cores taken from the
same area of the Santa Barbara Basin (< 10
MM; Cary et al, 1989). The larger environmental sulfide level extrapolated from the
blood data indicates that these organisms
are found on patches of more reduced sediment, as would be found associated with
an active seep. These clams likely use their
well-vascularized foot similarly to C. magnifica, to probe the sediments beneath them
for sulfide (Childress et al, 1993).
I
105
I
m
0.01
0.001
External
,S (mM)
FIG. 3. Blood total H2S concentration in Calyptogena
elongata in vivo as a function of the external total H2S
concentration. All experiments were carried out in a
flowing-water system at 5°C for 24 hr (see Childress et
al, 1993 for details). The thinner line represents a
linear regression fitted to the data collected at pH 8.1
under normoxic conditions. The equation for the line
is y = 16.74xO6M, r = 0.87. The thick line is a unity
line representing equal concentrations in the clams and
in the environment. Data replotted from Childress et
al., 1993, with permission.
obic encrusting organisms to the posterior
end of the shells of freshly recovered clams
suggest that their anterior ends are immersed
in reducing sediments while the posterior
(siphon) ends are positioned above the sediment/water interface (Fisher, 1990).
Sulfide is slowly generated within the sediments of the Louisiana Slope from petroleum and methane degradation and anaerThe vesicomyids Calyptogena ponderosa obic sulfate reduction (Anderson et al, 1983;
and Vesicomya cordata are found living on Kennicutt et al, 1989). No sulfide has been
the slightly reducing sediments near hydro- detected above the surface of the sediments
carbon seeps on the Louisiana Slope. They near these clams (Table 1). Sulfide distriboth harbor abundant intracellular symbi- bution in the sediments around live clams
onts (Brooks et al, 1987), have appreciable is extremely patchy and sparse, and serum
activities of RuBP C/O (E. C. # 4.1.1.39) from freshly collected clams often does not
and ATP sulfurylase (E. C. # 2.7.7.4) in their contain detectable sulfide (Table 1). One of
symbiont-bearing gills (Brooks et al, 1987; the freshly collected clams had a high blood
CRF, unpublished data), and have tissue sulfide concentration (0.322 mM, Table 1)
stable carbon isotope values indicative of which supports preliminary laboratory
carbon fixed by chemoautotrophic bacteria observations of a blood sulfide binding
(Kennicutt et al, 1985; Brooks et al, 1987). component in these species (A. Arp and J.
In situ observations, stains on the anterior Childress, personal communication) indihalf of the shells, and the relegation of aer- cating that they can concentrate sulfide from
106
K. M. SCOTT AND C. R. FISHER
obturacular
region
tentacles
vestimentum
gonad
trunk
trophosome
coelomic
cavity
opisthosome
tube
u
FIG. 4. Schematic drawings of Riftia pachyptila showing major body regions and gross vascularization. Insert
at right shows "bottle brush" arrangement of capillaries found in each lobule of the trophosome. The heart is
located on the dorsal vessel. From Fisher, 1990, with permission.
same suite of enzymes measured in C. magnifica gill, diagnostic of chemoautotrophic
sulfur bacteria (Felbeck et al, 1981). The
HYDROTHERMAL VENT VESTIMENTIFERANS
lack of a mouth, gut, and anus (Jones, 1981)
The hydrothermal vent tube worm Riftia and the similarity in carbon isotope compachyptila houses its bacterial symbionts in position between the trophosome tissue and
its trophosome (Cavanaugh et ai, 1981), an the rest of the organism (Rau, 1981; Fisher
organ that fills its body cavity, is suspended et al, 19886) indicate that this tube worm
in coelomic fluid and is endowed with a relies on its symbionts for organic carbon.
R. pachyptila is found in the areas of vigwell-developed vascular system (Fig. 4;
orous
dilute hydrothermal fluid flow within
Jones, 1981). The trophosome contains the
a vent site (Hessler et al., 19886; Johnson
et al., 19886). The turbulence of mixing of
the hydrothermal fluid with the bottom
TABLE 1. Sulfide levels in Louisiana Slope clam hab- water in this active flow does not create a
itats and freshly collected blood.
steady spatial gradient. Tube worms living
in this sort of flow experience broad flucn
Mean
Range
n (totuations in their sulfide and oxygen pools
(mM)
(mM)
Sample type
(UD*) tal)
(zero
to >300 nM and zero to >100 MM
Sediment surface
UD
2 2
respectively) over time periods ranging from
0.002 UD-0.015
6 7
5 cm interstitial
seconds to hours (Johnson et ai, 1988a).
0.036 0.014,0.058
0 2
10 cm interstitial
Instead
of bridging a spatial gradient, tube
Vesicomya cordata
worms living amidst more active fluid flow
blood
0.107
UD-0.322
2 3
bridge a temporal gradient as eddies of sulCalyptogena pon0.007 UD-0.059
8 9
derosablood
fide-rich or oxygen-richfluidflowpast them
* UD = undetected, detection limits for dissolved (Johnson et ai, 1988a). Tube worms living
in areas of less active venting are occasionsulfide analyzed by gas chromatography were 1-3 iM
depending on sample size. Interstitial samples are de- ally found recumbent on the basalt with their
the environment like the other vesicomyids
described above.
scribed by their depth below the sediment surface.
107
SULFIDE ECOLOGY OF VENT AND SEEP FAUNA
plumes (obturacular regions) over cracks
issuing dilute hydrothermal fluid (Hessler et
al., 1988*). Thus, the hydrothermal vent
vestimentiferans position their plumes such
that they have access to pools of water containing each of their redox substrates.
R. pachyptila is proposed to accumulate
high concentrations of sulfide from its erratic
but hi-flux environment through its gill-like
plume by virtue of its hemoglobins' sulfide
binding abilities (Arp and Childress, 1983).
Freshly collected R. pachyptila coelomic
fluid sulfide levels range from 0.01 to 1.03
mM, and vascular fluid ranges from 0.05 to
3.39 mM sulfide (Childress et al., 1984;
Childress et al., 1991a). Like vesicomyid
serum, R. pachyptila blood can concentrate
sulfide from a dilute solution during dialysis
(Arp and Childress, 1983). However, in the
case of the vestimentiferans, two forms of
extracellular hemoglobin (Terwilliger et al.,
1980) bind sulfide (Arp et al, 1987). These
hemoglobins bind sulfide with high affinity
(Fig. 5; Fisher et al, 1988). Unique to these
hemoglobins, their high affinity for oxygen
is not significantly affected by sulfide binding (Arp et al, 1990). Sulfide does not interact with these hemoglobins' porphyrin rings
to form sulfhemoglobin (Arp et al, 1987),
as it does with other hemoglobins (Somero
et al, 1989). Instead, sulfide has been suggested to bind to the hemoglobins by disrupting disulfide bridges not involved in
maintaining protein structure (Arp et al,
1987).
o to
S 60
(A
.1
1
10
100
Free Sulfide
FIG. 5. Sulfide bindings by Riftia pachyptila carbonyl
hemoglobin as a function of free sulfide concentration.
The Hill curve fitted to these data: in [% saturation -5(100 - % saturation)] = 0.737 (in free sulfide) - 1.778,
r2 = 0.89, 95% confidence interval on the coefficient
= ±0.129. The line shown is the relationship between
the % saturation and free sulfide described by this Hill
equation. From Fisher et al., 1988c, with permission.
nal sulfide concentrations (Arp et al, 1985;
Johnson et al, 1988*).
Like C. magnifica, intact R. pachyptila
can accumulate sulfide in their hemolymph
(vascular fluid) to concentrations one to two
orders of magnitude greater than external
concentrations (Fig. 6; Childress et al,
1991 a). Thiosulfate does not accumulate in
the blood of these organisms during exposure to sulfide (Childress et al, 1991a) and
their symbionts can use only sulfide as an
Once in the blood, sulfide must travel electron source (Fisher et al, 1989; Wilmot
through the host from the plume to the sym- and Vetter, 1990). High levels of autotrobionts without spontaneously oxidizing phic enzymes (Felbeck et al, 1981; Fisher
during its transport. Sulfide in oxygenated et al, 1988*), carbon fixation rates per gram
saline is stabilized by the presence of R. of tissue that can exceed those of C. magpachyptila hemoglobin (Arp and Childress, nifica by more than an order of magnitude
1983; Fisher and Childress, 1984). Spon- (Childress et al, 1991*; Fisher et al, 1991 a),
taneous oxidation of internal oxygen and and rapid rates of inorganic carbon accusulfide pools in vivo is likely prevented by mulation by intact Riftia (Childress et al,
sequestering them to separate binding sites 1991a) suggest that symbiont sulfide oxion the hemoglobins (Arp et al, 1985). R. dation is sufficiently rapid to keep free sulpachyptila coelomic fluid averages 20.2% of fide levels low enough to minimize host tisits wet weight (Fisher et al, 1988*), and its sue interactions with sulfide.
vascular fluid ranges from 9 to 20% of its
total body volume (Sanders and Childress,
HYDROCARBON SEEP VESTIMENTIFERANS
1993). Large blood volumes ensure that sulSeep vestimentiferans Escarpia sp. and
fide is supplied steadily to the symbionts Lamellibrachia sp., like all described vesduring short-term fluctuations in the exter- timentiferans have the same basic body plan
108
K. M. SCOTT AND C. R. FISHER
I
I
I
O
•?0.01
0.001
0.01
External H 2 S (mil)
FIG. 6. 2H2S and thiosulfate concentrations in hemolymph in Riftia pachyptila kept for 24 h at different
external sulfide concentrations and >42 nM O2. (A)
The broad solid line represents equal concentrations
of 2H2S outside the worm and in its fluids. The crosses
are the measured sulfide content of the hemolymph.
The narrow solid line fitted to these data is y =
12.53x0448. (B) The crosses represent the concentrations of thiosulfate in the hemolymph in these same
worms. Data replotted from Childress el al., 19916,
with permission.
as R. pachyptila and similar physiologies
(Jones, 1985; Fisher, 1990; Childress and
Fisher, 1992; Gardiner and Jones 1993).
Their trophosome tissue is similarly packed
with endosymbionts with high activities of
enzymes diagnostic of chemoautotrophic
bacteria (Brooks et al, 1987), that use sulfide as an electron source (Fisher et al,
1988c). Unlike R. pachyptila, which may
inhabit only a portion of its tube, the tissues
of these vestimentiferans stretch the full
length of their tubes, which can be as much
as three meters long (CRF, personal observation). In addition, their plumes are much
smaller, proportionally, than R. pachyptila 's (CRF, personal observation).
The low sulfide-flux seep environment is
radically different from the hydrothermal
vent environment. Sulfide is rarely detectable among these vestimentiferans' plumes
(Table 2; MacDonald et al, 1989), and when
present, its concentration is low (15 /iM,
maximum). Blood sulfide concentration in
freshly collected seep tube worms is low
compared to R. pachyptila (Table 2; Childress et al., 1986). Low blood sulfide levels
have several possible explanations. It is possible, since these organisms have blood sulfide binding properties similar to R. pachyptila, (Childress and Arp, unpublished
observation) that they accumulate their
small pools of blood sulfide through their
plumes from a sulfide pool that is below the
threshold of detection (below 2-3 ^M). It is
also possible that they obtain their sulfide
from a larger pool in the sediments, into
which their tubes can penetrate by as much
as a meter (MacDonald et al, 1989). Sulfide
distribution in the sediments near tube worm
bushes is as patchy as found among the seep
vesicomyids. However, when sulfide is
detectable in the interstitial water 10 cm
below the surface of the sediment, the average measured concentration (0.0226 mM)
exceed those found in the interstitial water
beneath vesicomyids. Since the tube worms
penetrate so deeply into the sediments, they
can draw from sulfide pools deeper than the
one sampled 10 cm below the surface, and
sediment cores from these sites reveal that
sulfide becomes more abundant with depth
in the sediment (Kennicutt et al, 1989). The
bodies of the seep vestimentiferans taper to
less than a millimeter in diameter in the
posterior end of their tubes, the walls of
which are thin enough to be translucent at
their buried distal end (CRF, personal
observation). Seep vestimentiferans' coelomicfluidfilledtrunk and thin-walled tubes
could act as a gas exchange surface, which
would aid them in drawing from pools of
sulfide deep in the sediments. In this see-
109
SULFIDE ECOLOGY OF VENT AND SEEP FAUNA
TABLE 2. Sulfide levels in Louisiana Slope tube worm habitats and freshly collected blood.
Sample type
Mean (mM)
Range (mM)
Among plumes and tubes
5 cm interstitial
10 cm interstitial
Lamellibrachia sp. blood
Escarpia sp. blood
Mixed group, both spp.t
<0.001
0.012
0.226
UD-0.015
UD-0.024
UD-1.172
UD-0.032
UD-0.015
UD-0.113
0.003
0.003
0.026
n (total)
23
1
5
13
4
2
26
2
12
15
6
7
* UD = undetected, detection limits for dissolved sulfide analyzed by gas chromatography were 1-3
depending on sample size. Interstitial samples are described by their depth below the sediment surface,
t From Childress et al, 1986.
nario, low blood sulfide concentrations could
result from equilibrium with a substantial
pool of deep interstitial sulfide, limited by
slow lateral diffusion through the sediment,
tube and body wall. Measurement of these
organisms' growth rates indicates that they
grow extremely slowly (less than 0.5 cm/yr,
Simpkins, 1994), but are long lived which
may reflect the low but steady sulfide flux
of this habitat. Another potentially confounding factor should be considered in
interpretation of the very low blood sulfide
levels found in freshly collected seep vestimentiferans. These organisms are from
shallow (600-800 m) cold seep communities and are not subjected to as severe
changes in temperature (ambient is about
7°C) or pressure during recovery as are the
vent vestimentiferans, which are collected
from warm flow into 2°C bottom water from
depths greater than 2,000 m. The seep vestimentiferans likely continue to oxidize
blood sulfide after collection and during
recovery, depleting their blood sulfide pool
before it is sampled at the surface at least
an hour after collection. Whatever the factors involved in the low blood sulfide levels
are, the environmental sulfide measurements, low growth rates, and long life spans
of the seep vestimentiferans indicate a life
history significantly different from their
hydrothermal vent relatives.
SUMMARY
Life for a vesicomyid at a cold seep is
conceptually similar in many ways to C.
magnified's life at the vents (Childress et al,
1993). Sulfide is absent at the siphons, but
is present within a foot's stretch from the
surface. The physiological and anatomical
adaptations which enable an autotrophic life
style at the hydrothermal vents are also
adaptive for a life in environments where
sulfide is sparse and its distribution patchy.
In some seep communities the sediments
are criss-crossed by the furrow the clams
leave as they search the sediments for sulfide pools to tap (Rosman et al, 1987; Fisher,
1990). Their ability to accumulate sulfide
into their blood from sub surface pools
allows vesicomyids to flourish at hydrothermal vents as well as a variety of lower
flux reducing habitats. On the other hand,
vestimentiferans at seeps may obtain sulfide
from their environment in a manner more
analogous to the vesicomyids than the
hydrothermal vent vestimentiferans. It is
likely that the seep vestimentiferans obtain
at least a portion of their sulfide from the
substantial pools in the sediments they are
buried in.
Diversity at many chemosynthetic communities is extremely low, probably due to
sulfide and other noxious substances present in these habitats (Hessler, 1988a; Childress and Fisher, 1992). The dense assemblages of organisms consist of a few species
that can utilize and/or tolerate the sulfide
present in these habitats. Vesicomyids and
vestimentiferans have "turned the tables"
on sulfide toxicity by allying themselves with
sulfide-oxidizing chemoautotrophs. They
are dependent on these bacteria for their
survival and growth in environments uninhabitable to other organisms, who can only
regard their microbially dependent sulfide
tolerance and growth with envy.
110
K. M. SCOTT AND C. R. FISHER
ACKNOWLEDGMENTS
We are thankful for the thoughtful comments of the reviewers. Thanks are also due
to the authors and publishers for the permission to print the figures in this review.
Special thanks to Dr. James Childress for
the data for Figures 2, 3, and 6, and to Dr.
Randall Kochevar for the prints for Figure
4. Figure 1 appears by courtesy of The University of Chicago Press (©1984 by The
University of Chicago. All rights reserved);
Figure 4 by courtesy of CRC Press (©1990
by CRC Press, Inc.); Figure 5 by courtesy
of Balaban Publishers (©1988 Balaban
Publishers).
We thank the Captains and crew of the
R. V.'s "Seward Johnson" and "Edwin
Link" and the pilots and crew of the D. S.
R. V. "Johnson Sea Link," and the Harbor
Branch Oceanographic Institute engineering group for assistance in the design and
construction of the water samplers. These
studies were supported by subcontract
LI0094 to Minerals Management Service
contract 14-12-0001-30555, NSF-EAR9158113, NSF-OCE-9114386, a NSF
Graduate Research Fellowship to KMS, the
NOAA National Undersea Research Center
at UNCW, and the Harbor Branch Oceanographic Institute.
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