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Chemoautotrophic production incorporated by heterotrophs in Gulf of Mexico hydrocarbon seeps: an examination of mobile benthic predators and seep residents.

ABSTRACT The continental slope of the Gulf of Mexico supports dense aggregations of tubeworms and mussels that have symbiotic chemoautotrophic bacteria. Associated with these communities are numerous heterotrophic fauna and free-living bacteria. Here we examine the stable C, N, and S isotope compositions of fauna from two chemoautotrophic communities to identify isotope ranges of chemoautotrophic primary production and determine the usage of that primary production by heterotrophic invertebrates. The range in isotope values of the chemoautotrophic production is different between sites. A brine seep (GC233) dominated by mussels symbiotic with methanotrophic bacteria has 13C and t SN depleted nutrient sources (-50 to -65[per thousand] and -9 to -12[per thousand], respectively), indicating methanotrophy using biogenic methane and suggesting ammonium as the dominant nitrogen source. However, those same sources were [sup.34]S-enriched (6[per thousand]-11[per thousand]), as indicated by resident heterotrophs (Munidopsis sp., Methanoaricia dendrobranchiata Blake 2000, Alvinocaris stactophila Williams 1988, Phascolosoma turnerae Rice 1985), indicating that thiotrophy was a minor chemosynthetic method at the site. A site dominated by tube worms and mussels (GC234) has two isotopically distinct sources of carbon, one between -24 and -30[per thousand] and another of approximately 40[per thousand], as indicated by the resident heterotrophs. Resident heterotrophs at GC :234 had [[delta].sup.15]N and [[delta].sup.34] S values from 1[per thousand] to 5[per thousand] and -10[per thousand] to 6[per thousand], respectively. These isotope values suggest a mix of thiotrophy and methanotrophy (largely from thiotrophic sources) at the site. We estimate that hagfish (Eptatretus sp.) captured approximately 2 km from the communities derived at least 10% of their carbon from chemoautotrophic sources because of low [[delta].sup.13]C values. In contrast, giant isopods (Bathynomus giganteus Milne Edwards, 1879), captured with the hagfish show negligible incorporation of chemosynthetic production.

KEY WORDS: hydrocarbon seeps, stable isotopes, chemosynthesis, Gulf of Mexico


In the mid-1980s, cold-seep chemosynthetic communities, which harbored heterotrophic and symbiont-containing invertebrates as well as free-living and mat bacteria were discovered in the Gulf of Mexico (Paull et al. 1983, Kennicutt et al. 1985, Brooks et al. 1987, MacDonald et al. 1990, Kennicutt et al. 1992). Twenty-five years after discovery of these seeps, fundamental questions still remain concerning the degree to which fauna within and around these relatively shallow communities use chemoautotrophic production as opposed to photosynthetic production (Kennicutt et al. 1992, Carney 1994, Fisher 1996, Levin 2005, MacAvoy et al. 2002, MacAvoy et al. 2005a). Carney (1994) took the first comprehensive attempt to classify organisms within the Gulf of Mexico (GOM) hydrocarbon seep communities as either vagrant (species present in the background but not present within the seeps in high density), colonist (species present in the background but in high density at the seep, indicating an established in-seep population), or resident (seep species not present in the background). By comparing the species captured within the communities to organisms captured in trawls of adjacent areas, Carney (1994) established initial categories of residency status for many species, although in some cases the data were limited and residency status could not be established from observations. Also, the trophic structure and level of incorporation of chemosynthetic production by nonsymbiont containing heterotrophs closely associated with the mussels and tubeworms at the seeps remain largely unknown (Levin 2005). Unlike the deepocean hydrothermal vents, where entire communities are supported by chemoautotrophic primary production, many GOM seeps are relatively shallow (500-800 m) and may receive significant pulses of photodetritus (Rowe & Staresinic 1979). Even so, hydrocarbon seep communities have been described as oases, a concept coined by Laubier (1993) and extensively reviewed by Carney (1994). This concept remains largely untested (see also MacAvoy et al. 2002), and must be answered before an understanding of the ecological relationship between seep communities and the surrounding benthos can be achieved. If seeps are likened to oases of food in the desert of the deep sea, then they may be subject to heavy predation by the background benthos (Carney 1994, Levin & Michener 2002, MacAvoy et al. 2002, Kicklighter et al. 2004, Sahling et al. 2003, Levin 2005). Indeed, Kelley et al. (1998) report that primary production by chemoautotrophic bacteria may be a significant source of nutrients to wide areas of the benthos of northern GOM continental slope. The existence of such a relationship between hydrocarbon seep communities and the surrounding background fauna could alter the understanding of the benthos as being almost entirely dependent on pulses of photodetritus (e.g., Gooday & Turley 1990, Jumars et al. 1990).

Because of the difficulty of conducting traditional community surveys at the depth these communities occur (500-800+ m below sea surface), alternative tools have been widely used to address questions of residency and nutrition (Carney 1994, Fisher 1996, Levin 2005, MacAvoy et al. 2002, MacAvoy et al. 2005a). One such tool is stable isotope analysis, which has offered important insights into how these systems function and how they are interlinked to the background environment (Brooks et al. 1987, Kennicutt et al. 1992, Fisher et al. 1994, Fisher 1996, Levin 2005, MacAvoy et al. 2002, MacAvoy et al. 2005a). Recent work has reported a likely carbon, nitrogen and sulfur stable isotope range for chemoautotrophic primary production within one GOM chemoautotrophic community (Green Canyon (GC) 185, also known as Bush Hill) (MacAvoy et al. 2005a). Grazing gastropods and deposit-feeding sipunculids were used to establish that bacterial chemoautotrophic production at GC185 ranged in [[delta].sup.13]C from-32[per thousand] to -20[per thousand], [[delta].sup.15]N from 0[per thousand] to 7[per thousand] and [[delta].sup.34]S from -14[per thousand] to -1[per thousand]. These values are substantially enriched relative to the chemoautotrophic symbiont-harboring megafauna, which dominate the sites (MacAvoy et al. 2005b). The isotope values of chemosynthetic communities often indicate the type of chemosynthesis within the community. Low [[delta].sup.13]C (-45[per thousand] to -65[per thousand]) indicate methanotrophy or consumption of methanotrophically-derived carbon, and the sites tend to be dominated by mussels (MacDonald et al. 1990). Low [[delta].sup.34]S (-25[per thousand] to -35[per thousand]) indicate sulfide-oxidizing systems, usually accompanied by tubeworms. Both characteristic chemosynthetic isotope values are different from normal GOM photosynthetic production, which show relative [sup.13]C and [sup.34]S-enrichment (approximately 19[per thousand] and 20[per thousand], respectively). Heterotrophic fauna that had stable isotope values in that range were likely to be largely dependant on free-living chemoautotrophic bacteria, with minimal nutrition derived from photosynthetic sources. The most intensively studied chemoautotrophic communities in the GOM are on the continental slope and are relatively shallow (540-640 m depth). At these shallow depths, photosynthetic production is a significant source of nutrition for many organisms, including some seep predators/scavengers (MacAvoy et al. 2002).

Endemic or resident seep species are likely to reflect chemoautotrophic production. Therefore, by examining the stable isotope values of these species at several areas, isotope ranges for chemoautotrophic production can be delineated (Levin & Michener 2002, MacAvoy et al. 2005a). Determining the isotopic ranges of chemoautotrophic production in different areas would be useful to those researchers seeking to better understand how much chemoautotrophic material is used from different areas of the benthos (Kelley et al. 1998, MacAvoy et al. 2002). With that information researchers could determine the degree to which different heterotrophic species in or around specific seeps use chemoautotrophic production. Additionally, fauna whose residency has remained unresolved can be characterized by examining their stable isotopes.

This study builds on previous work investigating ecosystem structure in Gulf of Mexico hydrocarbon seep communities using stable isotopic analysis. The investigation has been expanded from locations of earlier work to new sites, GC234 and GC233 (sites not examined in MacAvoy et al. 2005), and to further analyze new data from a previously studied site (GC234, MacAvoy et al. 2002). Three main questions are addressed: (1) What, if any, isotope differences exist between chemoautotrophic-harboring megafauna from different sites and why are there differences? (2) What are likely bacterial isotope values within two different sites? and (3) Do resident or vagrant heterotrophs, captured within or around the chemoautotrophic communities, derive nutrition from seep primary production including tubeworms or mussels, or do they rely on photosynthetic sources?


Study Sites

Sampling was conducted during 1998 and 2002 in the Gulf of Mexico Green Canyon Lease Area on research cruises of the submersible Johnson Sea Link (JSL) and the RV Edwin Link. Green Canyon (GC) occupies 22,000 [km.sup.2] of the continental slope, with depths ranging between 200 and 2,400 m. Sampling sites in this paper are referenced by the 4.8 x 4.8 [km.sup.2] numbered lease block in which they lie. The GC234 site (27[degrees]44.7'N; 91[degrees]13.3'W) is at a depth of approximately 540 m. The fauna at this site are dominated by tubeworms, Seepiophila jonesi Gardiner, McMullin & Fisher, 2001 and Lamellibrachia luymesi van der Land & Norrevang, 1975 with abundant mussel (Bathymodiolus childressi, Gustafson, 1998) beds. Methane gas and oil has been observed leaking from sediments (Nix et al. 1995, Sassen et al. 1994, Sassen et al. 1999). The GC233 site (27[degrees]43.4'N; 91[degrees]16.8'W) is at a depth of approximately 640 m. It is dominated by an anoxic brine pool that arises from saline seepage along a fault (Reilly et al. 1996, Sassen et al. 1999). Methane utilizing mussels, B. childressi, are the dominant symbiontbearing fauna at the site; tubeworms are scarce (Dattagupta et al. 2004, MacDonald et al. 1990). The sites GC233 and GC234 are 5.5 km apart. Previously, tubeworm community structure at a different site (GC185, Bush Hill) was examined by several of the authors (MacAvoy et al. 2005), however mussel beds were not. This study examines two different sites and the organisms collected represent those from mussel beds as well as tubeworm collections.

Samples from within the sites were collected using the suction arm of the JSL or a hydraulically actuated net, designed to capture entire tube worm aggregations with their associated fauna (Urcuyo 2000, Bergquist 2001, Bergquist et al. 2003a). Samples were collected from GC234 during dive numbers 4029 (July 6, 1998), 4047 (July 14, 1998), 4434 (June 22, 2002), and dive number 4039 (July 10, 1998), for GC233 collections. Off-site mobile predators were caught with surface deployed Z-frame traps, 150 x 180 x 90 cm, set approximately 2 km off the location of the seep communities in areas known from prior surveys to lack active seep communities. Z-traps were constructed of 2.5 cm square trap mesh, equipped with two 20-cm entry mouths, and baited with menhaden in a wire bait cage to minimize consumption (MacAvoy et al. 2002). Traps were deployed for two or three days depending on cruise logistics. The traps were deployed near GC234 at the following locations: 27[degrees]43.14'N; 91[degrees]13.3'W, 27[degrees]43.31'N; 91[degrees]12.392'W.

Sample Preparation

Most samples were of muscle tissue (exception being Phymorhynchus sp. viscera, dissected from the hindgut) taken from captured organisms and kept frozen until shipment to the laboratory. Isotope determinations were made on samples dried at 60[degrees]C for three days, homogenized, and lipid extracted by refluxing the samples in dichloromethane for ~35 min (Knoff et al. 2002). Approximately 5 to 6 mg of tissue was used for [[delta].sup.34]S analyses and 0.6 to 1.0 mg was used for [[delta].sup.13]C and [[delta].sup.15]N analyses.

Isotope values reported here are in standard [delta] notation as an abundance ratio of heavy to light isotope, in per mil ([per thousand):

[[delta].sup.x]E = [[([sup.x]E/[sup.y]E).sub.sample]/[([sup.x]E/[sup.y]E).sub.standard] -- 1] X 1,000 (1)

E being the element analyzed (C, N, or S), x is the atomic weight of the heavier isotope, and y is the atomic weight of the lighter isotope (x = 13, 15, 34 and y = 12, 14, 32 for C, N, and S respectively). Primary standards were Pee Dee Belemnite (PDB) for carbon, atmospheric air ([N.sub.2]) for nitrogen, and Canyon Diablo Troilite (CDT) for sulfur. Analysis were carried out at three laboratories; U. C. Davis Isotope Laboratories (carbon and nitrogen) on a Europa 20/20 Isotope Ratio Mass Spectrometer; Iso-Analytical Limited, Sandbach, UK (sulfur); and University of Virginia (carbon, nitrogen, and sulfur) on a Carlo Erba elemental analyzer coupled to a VG Optima isotope ratio mass spectrometer (EA/IRMS) (Fry et al. 1992, Giesemann et al. 1994). Reproducibility of all measurements is typically 0.3[per thousand] or better. Between every 12 samples, two laboratory standards were analyzed. In a typical run of 60 samples (+10 standards, 70 measurements total) the standard deviations for [[delta].sup.15]N and [[delta].sup.13]C were 0.16[per thousand] and 0.01[per thousand], respectively.

Mixing Equations

Because vagrant species are expected to have a diet combining seep and photosynthetic production, analyses included assessment of food source mixing. Isotopic mixing equations can be used to quantify food source dependence in systems with isotopically distinct food sources. The simple mixing equation used is:

[delta].sup.13][C.sub.predator] - F = ([delta].sup.13][C.sub.seep] x [f.sub.seep]) + ([delta].sup.13][C.ocean] X (1 - [f.sub.seep])) (2)

where [f.sub.seep]) is the fraction of diet from chemoautotrophic sources and [[delta].sup.13][C.sub.seep] and [[delta].sup.13][C.sub.ocean] are the mean carbon isotopic values of the chemoautotrophic material and background ocean respectively. The parameter F corrects for trophic enrichment and is dependent on the isotope used (as well as tissue collected). When using carbon isotopes, F is usually 1[per thousand], the typical diet-tissue discrimination associated with carbon (but see Pearson et al. 2003, Ayliffe et al. 2004, Arneson & MacAvoy 2005). Mixing equations rely on three basic assumptions: (1) that diet-tissue discrimination can be characterized accurately a priori, (2) that the isotope endmembers can be identified with confidence, and (3) that compounds consumed are incorporated into tissue in proportion to the amount of mixing. The first assumption is generally justified by numerous studies that have shown an approximate 1[per thousand] diet-tissue discrimination for [[delta].sup.13]C in animal muscle tissue versus diet (reviewed in Lajtha & Michener 1994), although it is recognized that the isotopic value of protein is the most important factor in observed diet-tissue discrimination (Hobson & Stirling 1997, Hobson & Bairlein 2003, Arneson & MacAvoy 2005, MacAvoy et al. 2005b). As to the second assumption, whereas the [[delta].sup.13]C value of zooplankton in the Northern Gulf of Mexico has been well-characterized (Fry 1983, Macko et al. 1984), there is a large range of [[delta].sup.13]C values for seep organisms that may be consumed (MacAvoy et al. 2005a). To address this problem, the standard deviations as well as the mean for the chemoautotrophic endmembers were used to estimate the percentage of carbon incorporated from that source prey. Investigations into the third assumption are an active area of research (Phillips & Gregg 2003, Arneson et al. 2006, MacNeil et al. 2006, Phillips & Eldridge 2006) and remain unresolved. It is likely, however, that animal tissues consumed by predators would have a similar percent of carbohydrate and protein, and any preferential incorporation of a nutrient type (protein for example) would occur equally regardless of chemoautotrophic or photoautotrophic source. Only carbon was used in the mixing equation. This was because the F-value for [[delta].sup.15]N is often more variable than carbon and the sulfur isotope value of primary production at these sites has a large range, based on the data reported here. Nitrogen isotope signatures were collected to help assess nitrogen sources used by seep fauna, and to estimate the likely [[delta].sup.15]N range of free-living bacteria. Sulfur isotopes were also used to identify free-living bacterial production and to help assess the importance of chemosynthetic and photosynthetic production among seep fauna.

The values used for the mean isotopic compositions of the chemoautotrophic prey, [[delta].sup.13][C.sub.seep], were calculated by averaging the analyses for selected resident fauna exclusive of vagrant species. The phytodetritus-based food sources of the background were considered to be relatively homogenous and a single set of C isotope values determined from the literature was used in Eq. (2). The [[delta].sup.13][C.sub.ocean] value of -17[per thousand] (derived from fish muscle tissues) was used as typical of values between phytoplankton and background predators (Fry & Sherr 1984, Peterson & Howarth 1987, Michener & Schell 1994, Roelke & Cifuentes 1997).

Statistical Analysis

Wilcoxon Signed Ranks tests were used for two group comparisons (i.e., comparing the two species of tubeworm, S.jonesi, and L. luymesi) ([alpha] = 0.05). The statistical comparisons were only made when individual groups (treatments) had an n [greater than or equal to] 3. Microsoft Excel 5.0 (Microsoft, Inc.), Statview SE + Graphics (Abacus Concepts, Inc.) and JMP (SAS software) were used for individual statistical tests.


Chemoautolithotrophic Symbiont-containing Invertebrates

Tubeworm species at GC234 were statistically different in [[delta].sup.13]C, with S. jonesi being depleted in [sup.13]C relative to L. luymesi (Wilcoxon z = -2.28, P [less than or equal to]0.026, df = 10) (Tables 1 and 2). The [[delta].sup.15]N values of the two GC234 tubeworm species were not significantly different (Wilcoxon z = 0.45, P [less than or equal to] 0.65, df = 10). The [[delta].sup.34]S values of tubeworms (L. luymesi) from GC234 were between -21[per thousand] and -25[per thousand] (Jarnegren et al. 2005), [sup.34]S enriched relative to tubeworm plumes from GC185, which are between -25[per thousand] and -33[per thousand] (MacAvoy et al. 2005). Tubeworms are very scarce at GC233 (which is dominated by the mussel Bathymodiolus childressi), and none were collected in this study.

Both carbon and nitrogen stable isotope values of B. childressi mussels were significantly different between GC234 and GC233 (Wilcoxon z = 2.35, P [less than or equal to] 0.019, df = 10). Bathymodiolus childressi is symbiotic with methane-utilizing bacteria but is also capable of filter feeding (Page et al. 1990). At both sites, the mussels were the most [sup.13]C-depleted of any organism collected. There was an approximately 30[per thousand] separation in [[delta].sup.13]C between mussels from GC234 and those from GC233 [-36.7[per thousand] (n = 3) and -65.8[per thousand] (n = 8)], respectively. There was also a 20[per thousand] difference in [[delta].sup.15]N between the two sites (4.9[per thousand] (n = 3) and -17.1[per thousand] (n = 8), respectively) The [[delta].sup.13]C values of GC234 and GC233 B. childressi were -36.7[per thousand] (n = 3) (Table 1) and -65.8[per thousand] (n = 8) (Table 2), respectively.

Resident Heterotrophs

GC 234

Resident nonsymbiont-containing heterotrophs at GC 234 had [[delta].sup.13]C values between -24 and -41[per thousand] and [[delta].sup.15]N values between 4[per thousand] and 10[per thousand] (Fig. 1, Table 1). The [[delta].sup.34]S range among resident heterotrophs was similar. Using muscle tissue from squat lobsters (Munidopsis sp.), shrimp, (Alvinocaris stactophila), and sipuncluids (Phascolosoma turnerae Rice 1985), the [[delta].sup.34]S range was 1.5[per thousand] to 6[per thousand] (Fig. lb).


At GC233, known resident fauna such as the Methanoaricia dendrobranchiata (Blake 2000) (a deposit feeding polychaete worm), and the Bathynerita naticoidea (Clark 1989) (a grazing snail), had low [[delta].sup.13]C and [[delta].sup.15]N values and elevated [[delta].sup.34]S values relative to resident heterotrophs at GC234 (Table 2). As noted earlier, Bathymodiolus childressi at this site were highly [sup.13]C depleted, and ranged from -63[per thousand] to -7[per thousand]. Known heterotrophic residents mostly ranged from -62[per thousand] to -50[per thousand] (Table 2, Fig. 2), although two A. stactophila shrimp were greatly [sup.13]C-enriched (-27[per thousand]). None of the GC233 resident heterotrophs reported in this study, or earlier studies at GC233, revealed organisms as [sup.13]C enriched as these two individuals (Brooks et al. 1987, Kennicutt et al. 1992, MacAvoy et al. 2002). The [[delta].sup.15]N values of heterotrophs at GC 233 were low, with the grazing Bathynerita naticoidea ranging between -9[per thousand] and -5[per thousand] (Fig. 2). The mussel Bathymodiolus childressi [[delta].sup.15]N was on average 10[per thousand] lower than the Bathynerita naticoidea. Also, heterotrophs at GC233 were considerably [sup.34]S-enriched relative to those at GC234 (Tables 1 and 2). Grazing B. naticoidea were among the most [sup.34]S-depleted (between 6[per thousand] and 12[per thousand]; mean 9.3[per thousand]) and the shrimp A. stactophila (mean 17.2[per thousand]) were among the most [sup.34]S-enriched of the GC234 fauna.


Vagrant Predators (Phymorhynchus sp., Eptatretus sp. Bathynomus giganteus)

The snails Phymorhynchus sp. captured at GC234 were significantly depleted in [sup.13]C relative to other vagrants, such as isopods (Bathynornus giganteus Edwards 1879) and hagfish (Eptatretus sp.) (Table l, Fig. la). The L. luymesi tubeworms at GC234 had very low [[delta].sup.34]S values (-21[per thousand] to -25[per thousand], Jarnegren et al. 2005), and the Phymorhynchus sp. snails were between 3[per thousand] and -10[per thousand] (Table 1, Fig. 2). The same Phymorhynchus sp. that had their muscle tissue examined for [[delta].sup.34]S had their viscera characterized as well. There was over a 40[per thousand] range in [[delta].sup.34]S among the Phyrnorhynchus sp. viscera (Fig. lb). In only one individual did muscle and viscera [[delta].sup.34]S fall within 5[per thousand] of each other.


Eptatretus sp. collected approximately 2 km from GC234 were [sup.13]C-depleted as a group (mean -18.7 [+ or -] 1.0[per thousand]; Table 1) relative to typical pelagic Gulf of Mexico predators in the area (usually -16[per thousand] to -17[per thousand], MacAvoy et al. 2002, Northern Gulf of Mexico Wahoo (Acanthocybium solandri, Cuvier 1831) and Hake (Urophysis sp.), [[delta].sup.13]C -16.6[per thousand] and -17.5[per thousand], respectively). Fry (1983) reported a [[delta].sup.13]C of 16.1[per thousand] for offshore benthic crustaceans in the northern Gulf of Mexico. An average [[delta].sup.13]C from GC234 that has been used previously for mixing equations is -32%0 [+ or -] 6[per thousand], and the average zooplankton and background predators in the Gulf of Mexico have been estimated to be -17[per thousand] (MacAvoy et al. 2002). Using these values as endmembers and shifting the chemoautotrophic endmember by [+ or -]1 standard deviation, it is estimated that between 12% and 40% (mean of 18 [+ or -] 7%) of the tissue carbon was derived from chemoautotrophic production. Bathynomus giganteus [[delta].sup.13]C and [[delta].sup.15]N were elevated relative to the Eptatretus sp. (Table 1). [[delta].sup.34]S values of B. giganteus were among the highest of any animal in this study (mean 19.3[per thousand], Table 1).


Chemoautolithotrophic Symbiont-containing Invertebrates

The fact that the Seepiophila jonesi were [sup.13]C-depleted relative to Lamellibrachia luymesi at GC234 was consistent with the difference observed among GC185 tubeworm species by MacAvoy et al. (2005a). It may be because of the fact that S. jonesi tends to have its gas exchange organ (plume) orientated near the sediment-water interface, whereas L. luymesi keeps its plume well above the sediment. Dissolved inorganic carbon (DIC) near the sediment water interface may be [sup.13]C depleted because of high levels of methanotrophy in the sediments (Sassen et al. 2003). If the worms obtain their carbon from DIC taken up across their plumes (Julian et al. 1999, Freytag et al. 2001), then their [[delta].sup.13]C differences may reflect heterogeneous DIC isotope signals. However, both species were substantially [sup.13]C-depleted relative to tubeworms at a neighboring site (GC 185) (MacAvoy et al. 2005a). This [[delta].sup.13]C trend has also been observed in previous work, which reported tubeworm [[delta].sup.13]C values from GC185 and GC234 (MacAvoy et al. 2002). Sassen et al. (1999) found venting methane [[delta].sup.13]C to be between 2[per thousand] and 4[per thousand] lighter at GC234 relative to GC185, which may have resulted in relatively [sup.13]C enriched DIC in pore waters at GC185. The higher [[delta].sup.34]S values observed among GC234 L. luymesi relative to those from GC185 suggests different sulfide [[delta].sup.34]S values between the two sites, because there is not significant fractionation upon uptake by bacteria (Canfield 2001).

The [[delta].sup.13]C differences between the Bathymodiolus childressi from GC234 and GC233 was partially caused by the origins of the C[H.sub.4] their symbiotic bacteria use as a carbon source. Methane from GC234 is of mostly of thermogenic origin and has a [[delta].sup.13]C of approximately -48[per thousand], whereas methane from GC233 is biogenic in origin, having a [[delta].sup.13]C value of-65[per thousand] (Sassen et al. 1999). B. childressi from GC233 clearly reflect the biogenic methane, because there is little or no fractionation upon symbiont utilization of the gas (Brooks et al. 1987, Kennicutt et al. 1992). At GC234, the mussels were approximately 10[per thousand] enriched in [[delta].sup.13]C relative to methane at the site. The [[delta].sup.13]C value of free-living chemosynthetic bacteria at GC234 was estimated to be between -40 and -24[per thousand] (see subsection below) and photosynthetic primary production in the Gulf of Mexico has a value of approximately -19[per thousand] (Fry 1984). It is likely that GC234 B. childressi were not deriving their nutrition solely from their symbionts but were also filtering photosynthetic-derived organic material from the water column (Van Dover et al. 2003). Page et al. (1990) report that B. childressi obtain carbon from both filter feeding and symbionts.

Resident Heterotrophs

GC 234

Using known seep resident species (Methanoaricia dendrobranchiata, Munidopsis sp., Alvinocaris stactophila) as indicators for the chemoautotrophic production range, there seems to be two sources of carbon from primary production, one between -24[per thousand] and -30[per thousand] and the other of approximately -40[per thousand] (Fig. 1). The [[delta].sup.15]N of primary production at GC234 was approximated by subtracting 3.4 [per thousand], the average trophic enrichment found by Minagawa & Wada (1984) from the [[delta].sup.15]N of A. stactophila and M. dendrobranchiata, because these heterotrophs are likely primary consumers (Bergquist et al. 2003a). Thus the [[delta].sup.15]N range of primary production was probably from 1 [per thousand] to 5[per thousand].

The [[delta].sup.34]S range of the heterotrophic invertebrates (Munidopsis sp., Phymorhynchus sp. Alvinocaris stactophila and Phascolosoma turnerae), reflects the isotopic range of inorganic sulfur at the site, because there is little fractionation of sulfur isotopes during transformation from inorganic to organic forms (reviewed in Canfield 2001), and because there is minimal diet-tissue discrimination between dietary organic sulfur and consumer (Arneson & MacAvoy 2005). The heterotroph [[delta].sup.34]S values resulted from consumption of organisms utilizing a mixture of seawater sulfate and sulfate produced by oxidation of [H.sub.2]S (Aharon & Fu 2003). The only other fauna collected have had not been classified as resident or colonist, include an undescribed species of platyhelmenthies, two Oligopus sp. conger eels, a viperfish (Chauliodus sloani, Bloch & Schneider, 1801 and a Synaphobranchus sp. eel. The eels and viperfish had their isotope values reported in MacAvoy et al. (2002), but their residency was not addressed. Of the unclassified fauna, the platyhelmenthies and eels clearly made heavy use of chemoautotrophic carbon and nitrogen, based on its very depleted isotope values (Fig. 1). Based on the isotope values, it is highly likely that they are residents of the seeps. The Chauliodus sloani has [sup.13]C and [sup.15]N-enriched isotope values (similar to the hagfish Eptatretus sp., see later), and is probably a vagrant predator.


Known resident fauna such as the polychaete worm, Methanoaricia dendrobranchiata (a deposit feeder), and the snail, Bathynerita naticoidea (a grazer), probably reflect bacterial sources of production and would reveal the likely range of chemoautotrophic production within communities where they are found (MacAvoy et al. 2002, 2005a). The two [sup.13]C-enriched Alvinocaris stactophila probably indicated that they were not long-time residents at GC233 but had migrated from another site (sites can be quite close together). Alternatively, some inorganic carbon with a [sup.13]C-enriched signal masked the true tissue [[delta].sup.13]C value, however these samples were processed in the same way as the other A. stactophila. The very low [[delta].sup.13]C values observed in most of the heterotrophs indicates that bacteria utilizing biogenie methane dominate primary production within the seep, as observed in earlier studies (Sassen et al. 1999). Low [[delta].sup.13]C values and relatively high (for chemosynthetic production) [[delta].sup.34]S values suggest that carbon production from sulfate reducers or hydrogen sulfide oxidizers was not an important source of nutrients to GC233 fauna relative to the methane-utilizing bacteria.

The [sup.15]N-depleted values of both Bathymodiolus childressi and Bathynerita naticoidea suggest that ammonia assimilation may be driving the nitrogen signal at this site (Lee & Childress 1996). Anoxic bacteria have been shown to fractionate N[H.sub.3] between -12.3[per thousand] and-10.2[per thousand] (Beaumont et al. 2000, Hoch et al. 1992), and although the bacteria responsible for that fractionation were photosynthetic, a similar major [sup.15]N-depleting effect of assimilation may have been occurring at GC233. In any case, the highly [sup.15]N-depleted signal from GC233 is effectively a value for organisms utilizing nitrogen from GC233; even the two shrimp with markedly [sup.13]C-enriched signals relative to other organisms showed an unusually low [[delta].sup.15]N value (-2[per thousand]; Fig. 2). The wide range (-4[per thousand] to -16[per thousand]) of [[delta].sup.15]N among nonsymbiont containing heterotrophs probably does not reflect the familiar trophic enrichment (3.4[per thousand] increase per trophic level) because the animals are mostly primary consumers and rasping grazers, not secondary or tertiary consumers (Bergquist et al. 2003b). It is more likely that the [[delta].sup.15]N range reflects a dilution of the very [sup.15]N-depleted ammonium values occurring at the sediment water interface (which the B. childressi and platyhelmenthies reflect). Although almost all heterotrophs at the site were less than -50[per thousand] in [[delta].sup.13]C, they approached the [[delta].sup.34]S value of sulfate in the GOM bottom waters (20.3[per thousand], Aharon & Fu 2003), indicating that primary production from thiotrophy was not an important nutrient source.

An examination of the three isotopes together reveals that the GC233 fauna are within isotopically distinct groups. The B. childressi and platyhelmenthies were depleted in [sup.13]C and [sup.15]N relative to other fauna, possibly because of very close proximity to the sediment water interface, where transformations of C[H.sub.4] and N[H.sub.3] were presumably rapid, resulting in discrimination against the heavy isotope in those species. Each of the other species separates into an isotopic cluster with B. naticoidea [sup.34]S-depleted relative to A. stactophila, yet sharing the same [[delta].sup.13]C values, and M. dendrobranchiata as [sup.13]C-depleted as B. childressi, yet substantially [sup.15]N-enriched (Table 2). The mixture of isotope values illustrates niche separation among the fauna, but clearly shows that B. childressi are not a major source of carbon, nitrogen or sulfur to the other fauna (except, perhaps, the platyhelmenthies). In any case, carbon and nitrogen isotope values are much too low for photosynthetic primary production to be an important nutrient source even at this relatively shallow site, where phytodetritus is probably drifting into the area (Tyler 1988). Carbon isotope mixing equations, using -57.3[per thousand] and -17[per thousand] as the seep and photosynthetic endmembers respectively (values used for GC233 mixing equations based on a collection of symbiont-containing and heterotrophic fauna in MacAvoy et al. 2002), show that among M. dendrobranchiata, A. stactophila, Bathynerita naticoidea, Munidopsis sp. and the platyhelmenthies, 100% of carbon was chemosynthetically derived. The platyhelmenthies, classified as unresolved to date, are clearly seep residents. The dominant nutrient source for these heterotrophs appears to free-living methanotrophic bacteria and isotope differences among them are probably a result of niche separation.

Vagrant Predators

Although the Phymorhynchus sp. was not as [sup.13]C-depleted as most resident heterotrophs (who presumably derive most, if not all, nutrients from chemoautotrophic production), they clearly derived some significant nutrition from chemoautotrophic sources. The snails showed carbon and nitrogen isotope values that suggest tubeworms were a nutrient source, however their muscle [[delta].sup.34]S values were substantially higher than would be expected if that were the case. In fact, the Phymorhynchus sp. were almost 20[per thousand] greater in [[delta].sup.34]S than GC234 tubeworms, indicating that tubeworm protein was not as substantial a nutrient source as the [[delta].sup.13]C and [[delta].sup.15]N data suggest. This result is consistent with that reported by MacAvoy et al. (2005a) where it was shown that tubeworms at a similar hydrocarbon seep (GC185) were unlikely to provide nutrition to heterotrophic fauna. Additionally, Kicklighter et al. (2004) found that the worms were unpalatable to some invertebrate heterotrophs and Bergquist et al. (2003a) reported that there was no visible evidence of grazing by heterotrophs on tubeworms. Therefore it seems likely that tubeworms are not consumed by heterotrophs.

The very large difference between the Phymorhynchus sp. muscle tissue and viscera (gut dissected from muscle) [[delta].sup.34]S, illustrates large and significant differences between what is consumed in a "last meal" (gut contents) and what is incorporated into tissues over a longer period of time. One individual had viscera with a [[delta].sup.34]S of 19.1[per thousand], which points to [sup.34]S enriched ocean sulfate associated with photosynthetic production, although the [[delta].sup.13]C value was -27.3[per thousand]. Three other individuals, however, had viscera [[delta].sup.34]S between -12.3[per thousand] and -21.9[per thousand], substantially [sup.34]S-depleted relative to muscle tissues. This would seem to indicate that they had been consuming chemoautotrophic material almost exclusively in the recent past. The combination of muscle and viscera sulfur isotopes illustrates that this vagrant snail forays into and out of the seep, deriving significant nutrients from seep production, but very much capable of leaving the seep to successfully forage on photosynthetically fixed material.

Even the conservative estimate of 12% is significant and adds to evidence linking chemoautotrophy at seeps to mobile benthic fauna (Levin 2005, Levin & Michener 2002, MacAvoy et al. 2002). Bathynomus giganteus captured with the Eptatretus sp. showed no appreciable chemoautotrophic carbon incorporation. Even as a benthic predator 550+ m below the ocean's surface, they still gained all of their nutrition from photosynthetic production, although they were captured relatively close to a chemoautotrophic community. Other benthic crustaceans, such as Rochina crassa, have shown limited chemosynthetic use in the Gulf of Mexico. It has been previously reported that between 8% and 17% of R. crassa biomass sulfur was derived from chemosynthetic sources in animals collected 2 km way from known chemosynthetic communities (GC185, MacAvoy et al. 2002).

Stable isotopes have proven useful for constraining possible nutrient sources available to deep ocean communities. Although they cannot be used to show precisely what the heterotrophs are consuming, isotope compositions can be used to verify what organisms are not consuming. In the two relatively shallow Gulf of Mexico seep communities examined in this study, most resident fauna derived almost all of their dietary carbon and sulfur from seep production. At one community (GC234) there was strong evidence that two sources of chemosynthetic production exist, which produced distinct [[delta].sup.13]C values. Tubeworms were not a significant source of nutrients to heterotrophs and, although the mussel B. childressi may have supported some heterotrophs, it is apparent that gazers had a nutrient source distinct from mussels. Possible reasons for the limited consumption of tubeworm or mussel carbon include: (1) "toxic exclusion" where hydrogen sulfides inhibit visits from predators, (2) abundance of food from photosynthetic sources at these relatively shallow sites, and (3) the presence of defensive chemicals in sessile chemosynthetic-harboring fauna. Chemosynthetic production was exploited by some vagrant benthic heterotrophs, although not to the extent that would be expected if the chemosynthetic communities were functional oases in the desert of the deep sea. However, chemoautolithotrophic production can be a significant nutrient source, even on the relatively shallow continental slope.


This work was supported in part by subcontract L100094, S700033, and S70027 to the Mineral Management Service project RF-6899 and the Mineral Management Service, Gulf of Mexico Regional OCS office through contract #1435-01-96-CT 30813 and NSF grant OCE 0118946 to SAM. Partial support was also provided by Mellon funds from American University to SEM. EM was supported by a Deans Undergraduate Research Award from American University. We would like to thank Dr. Ian MacDonald of the Geochemical and Environmental Research Group, Texas A&M University and Dr. Robert Avent of the Mineral Management Service for their interest and support. This research could not have been accomplished without the crews of the R.V. Edwin Link and Johnson Sea Link (Harbor Branch Oceanographic, Fort Pierce, FL). The authors extend special thanks to Drs. Charles Fisher, Derk C. Bergquist, John K. Freytag, and Erin McMullen (Penn State University) for their help on an off the ship. Dr. Mary Rice (Smith Marine Station), Dr. Timothy Shank (Woods Hole Oceanographic), Dr. Julie Amber (Millersville University), Brett Begley (Pennsylvania State University), Dr. Stephane Hourdez (Equipe Ecophysiologie Station Biologique de Roseoff), and Rachel Kosoff (Pennsylvania State University) all assisted with species identifications.


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S. E. MACAVOY, (1) * E. MORGAN, (1) R. S. CARNEY (2) AND S. A. MACKO (3)

(1) Department of Biology, American University, Washington, DC, 20016; (2) Coastal Studies Institute, Louisiana State University, Baton Rouge, Louisiana 70803; (3) Department of Environmental Sciences, University of Virginia, Charlottesville, Virginia 22903

* Corresponding author. E-mail:
Table 1.
Stable isotopes of GC234 fauna. "Resident" classification is from
Berquest et al., 2003b or MacAvoy et al., 2005a. Vagrant classification
is from Carney 1994 or MacAvoy et al., 2005a.

Resident symbiont-
 Mussels Bathymodiolus -36.7 ([+ or -] 0.3) (3)
 Tuberworms Seepiophila jonesi -32.0 ([+ or -] 4.0) (5)
 Lamellibrachia luymesi -25.8 ([+ or -] 2.1) (6)
 Tuberworm mean -28.6 ([+ or -] 4.4)
 Squat lobster Munidopis sp. -27.1 ([+ or -] 0.5) (2)
 Sipuncluid Phascolosoma turnerae -29.4 ([+ or -] 1.8) (2)
 Orbiniid Methanoaricia -41.0
 polychaete dendrobranchiata
 Shrimp Alvinocaris stactophila -24.1
 Resident mean -29.7 ([+ or -] 5.9)
 Giant isopod Bathynomus giganteus -16.4 ([+ or -] 0.5) (21)
 Hagfish Eptatretus sp. -18.7 ([+ or -] 1.0) (8)
 Predatory snail Phymorhynchus sp. -24.1 ([+ or -] 1.2) (3)
Unresolved species
 Flatworm -40.0 ([+ or -] 0.1) (2)

 [[delta].sup.15]N [[delta].sup.34]S
Resident symbiont-
 Mussels 4.9 ([+ or -] 0.6) (3)
 Tuberworms 4.4 ([+ or -] 1.6) (5)
 4.1 ([+ or -] 1.2) (6)
 4.2 ([+ or -] 1.4)
 Squat lobster 8.2 ([+ or -] 2.1) (2) 6.1
 Sipuncluid 7.4 (t0.1) (2) 1.5
 Orbiniid 4.2
 Shrimp 7.6
 7.1 ([+ or -] 1.8) 3.8 ([+ or -] 3.2)
 Giant isopod 14.0 ([+ or -] 0.6) (21) 19.3 ([+ or -] 0.4) (8)
 Hagfish 11.8 ([+ or -] 1.1) (8)
 Predatory snail 5.1 ([+ or -] 0.3) (3) -5.1 ([+ or -] 3.2) (3)
Unresolved species
 Flatworm 5.4 ([+ or -] 0.5) (2)

Table 2.
Stable isotopes of GC233 (Brine Pool NR1) fauna. "Resident"
classification is from Berquest et al. (2003b), MacAvoy et al. (2005a).
Vagrant classification is from Carney (1994) or MacAvoy et al. (2005a).

 ([per thousand])

 Mussels Bathymodiolus -65.8 ([+ or -] 3.0) (8)
 Squat lobsters Munidopsis sp. -55.6
 Grazing snail Bathynertia -55.8 ([+ or -] 4.8) (6)
 Orbiniid Methanoaricia -59.9 ([+ or -] 1.3) (9)
 polychaete dendrobranchiata
 Shrimp Alvinocaris -44.1 ([+ or -] 12.2) (6) *
 mean -50.4 ([+ or -] 10.3)
 Hagfish Eptatretus sp. 28.6
Unresolved species
 Flatworm -59.0 ([+ or -] 2.7) (4)

 [[delta].sup.15]N [[delta].sup.34]S
 ([per thousand]) ([per thousand])

 Mussels -17.1 ([+ or -] 0.9) (8) 12.1 ([+ or -] 2.4) (6)
 Squat lobsters -9.9 17.3
 Grazing snail -7.1 ([+ or -] 1.4) (6) 9.3 ([+ or -] 2.0) (6)
 Orbiniid -9.8 ([+ or -] 0.9) (9) 16.5 ([+ or -] 2.7) (9)
 Shrimp -7.3 ([+ or -] 3.0) (6) 17.2 ([+ or -] 2.2) (8)
 -7.4 ([+ or -] 2.2) 14.0 ([+ or -] 4.4)
 Hagfish 8.2
Unresolved species
 Flatworm -14.7 ([+ or -] 1.2) (4) 16.6 ([+ or -] 0.9) (2)

* There were 2 Alvinocaris stactophila with highly enriched
[[delta].sup.13]C values relative to the other four (-27[per thousand]
vs. roughly 50[per thousand]). This causes the large
standard deviation and high mean [[delta].sup.13]C for an endemic
group at this site.
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Article Details
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Author:Macavoy, S.E.; Morgan, E.; Carney, R.S.; Macko, S.A.
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2008
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