Heterotrophic Fauna Research Articles

Riddles of Lost City: Chemotrophic Prokaryotes Drives Carbon, Sulfur, and Nitrogen Cycling at an Extinct Cold Seep, South China Sea.

Deep-sea cold seeps are one of the most productive ecosystems that sustained by hydrocarbons carried by the fluid. Once the seep fluid ceases, the thriving autotrophic communities die out, terming as the extinct seep. But heterotrophic fauna can still survive even for thousands of years. The critical role of prokaryotes in active seeps are well defined, but their functions in extinct seeps are poorly understood to date. Here, we clarified the diversity, taxonomic specificity, interspecies correlation, and metabolic profiles of sediment prokaryotes at an extinct seep site of Haima cold seep, South China Sea. Alpha diversity of archaea significantly increased, while that of bacteria remained unchanged in extinct seep compared to active seep. However, archaea composition did not differ significantly at extinct seep from active or nonseep sites based on weighted-unifrac dissimilarity, while bacteria composition exhibited significant difference. Distribution of archaea and bacteria showed clear specificity to extinct seeps, indicating the unique life strategies here. Prokaryotes might live chemolithoautotrophically on cycling of inorganic carbon, sulfur, and nitrogen, or chemoorganotrophically on recycling of hydrocarbons. Notably, many of the extinct seep specific species and networked keystone lineages are classified as Proteobacteria. Regarding the functional diversity and metabolic flexibility of this clade, Proteobacteria is supposed to integrate the geochemical cycles and play a critical role in energy and resource supplement for microbiome in extinct seep. Collectively, our findings shed lights on the microbial ecology and functional diversity in extinct seeps, providing new understanding of biogeochemical cycling after fluid cessation. IMPORTANCE This research paper uncovered the potential mechanisms for microbiota mediated geochemical cycling in extinct cold seep, advancing our understanding in deep sea microbiology ecology.

Trophic structure and chemosynthesis contributions to heterotrophic fauna inhabiting an abyssal whale carcass

The trophic structure and role of chemosynthesis remain unexplored in deep-sea whale-fall communities in areas other than the California margin. This gap limits the understanding of these communities and their ecological relationships with other chemosynthetic ecosystems, such as vents and seeps. Here, we studied 3 different whale skeleton microhabitats with hypothesized high, intermediate and low reducing conditions as well as the sediments surrounding an abyssal whale fall (4204 m depth, SW Atlantic Ocean). We analyzed trophic structures (δ13C and δ15N) and the contribution of chemosynthetically derived carbon to heterotrophic species. The high and intermediate reducing microhabitats harbored food webs dominated by consumers of chemosynthetic production, similar to those of diffusive areas of hydrothermal vents and seeps. Both the low reducing microhabitat and the sediments harbored food webs with greater trophic complexity, dominated by higher consumers mainly relying on whale and/or photosynthesis-derived organic matter, a type of food web commonly reported in small whale, wood and kelp falls. The main whale-fall ecosystem engineer, the bone-eating worm Osedax, appeared to produce unique food web effects not observed in other chemosynthetic habitats. We conclude that whale falls provide the deep sea with a mosaic of microhabitats that supports assemblages with different chemosynthesis reliance levels and trophic structures, similar to those found at vents and seeps. Such a mosaic allows species-rich communities with numerous trophic levels to develop in a very small area of the food-limited deep sea.

Energy transfer in the Congo deep-sea fan: From terrestrially-derived organic matter to chemosynthetic food webs

Large amounts of recent terrestrial organic matter (OM) from the African continent are delivered to the abyssal plain by turbidity currents and accumulate in the Congo deep-sea fan. In the recent lobe complex, large clusters of vesicomyid bivalves are found all along the active channel in areas of reduced sediment. These soft-sediment communities resemble those fuelled by chemoautotrophy in cold-seep settings. The aim of this study was to elucidate feeding strategies in these macrofaunal assemblages as part of a greater effort to understand the link between the inputs of terrestrially-derived OM and the chemosynthetic habitats. The biochemical composition of the sedimentary OM was first analysed in order to evaluate how nutritious the available particulate OM is for the benthic macrofauna. The terrestrial OM is already degraded when it reaches the final depositional area. However, high biopolymeric carbon contents (proteins, carbohydrates and lipids) are found in the channel of the recent lobe complex. In addition, about one to two thirds of the nitrogen can be assigned to peptide-like material. Even if this soil-derived OM is poorly digestible, turbiditic deposits contain such high amounts of organic carbon that there is enough biopolymeric carbon and proteacinous nitrogen to support dense benthic communities that contrast with the usual depauperate abyssal plains.Stable carbon and nitrogen isotopes and fatty acid biomarkers were then used to shed light on the feeding strategies allowing the energy transfer from the terrestrial OM brought by the turbidity currents to the abyssal food web. In the non-reduced sediment, surface detritivorous holothurians and suspension-feeding poriferans rely on detritic OM, thereby depending directly on the turbiditic deposits. The sulphur-oxidising symbiont bearing vesicomyids closely depend on the reprocessing of OM with methane and sulphide as final products. Their carbon and nitrogen isotopic signatures vary greatly among sites and could reflect the intensity of the anaerobic oxidation of methane (AOM) in the sediments. Within the vesicomyid habitats, the heterotrophic fauna exhibits a distinctively light carbon isotopic signature in comparison to the background sediments, clearly indicating the utilisation of chemosynthetically-derived OM. Fatty acid biomarkers further confirm that dorvilleid polychaetes consume aggregates that perform AOM. Terrestrial OM reprocessing by microbial consortium thus ensures its transfer to the benthic food web in the Congo deep-sea fan.

Food-Web Complexity in Guaymas Basin Hydrothermal Vents and Cold Seeps.

In the Guaymas Basin, the presence of cold seeps and hydrothermal vents in close proximity, similar sedimentary settings and comparable depths offers a unique opportunity to assess and compare the functioning of these deep-sea chemosynthetic ecosystems. The food webs of five seep and four vent assemblages were studied using stable carbon and nitrogen isotope analyses. Although the two ecosystems shared similar potential basal sources, their food webs differed: seeps relied predominantly on methanotrophy and thiotrophy via the Calvin-Benson-Bassham (CBB) cycle and vents on petroleum-derived organic matter and thiotrophy via the CBB and reductive tricarboxylic acid (rTCA) cycles. In contrast to symbiotic species, the heterotrophic fauna exhibited high trophic flexibility among assemblages, suggesting weak trophic links to the metabolic diversity of chemosynthetic primary producers. At both ecosystems, food webs did not appear to be organised through predator-prey links but rather through weak trophic relationships among co-occurring species. Examples of trophic or spatial niche differentiation highlighted the importance of species-sorting processes within chemosynthetic ecosystems. Variability in food web structure, addressed through Bayesian metrics, revealed consistent trends across ecosystems. Food-web complexity significantly decreased with increasing methane concentrations, a common proxy for the intensity of seep and vent fluid fluxes. Although high fluid-fluxes have the potential to enhance primary productivity, they generate environmental constraints that may limit microbial diversity, colonisation of consumers and the structuring role of competitive interactions, leading to an overall reduction of food-web complexity and an increase in trophic redundancy. Heterogeneity provided by foundation species was identified as an additional structuring factor. According to their biological activities, foundation species may have the potential to partly release the competitive pressure within communities of low fluid-flux habitats. Finally, ecosystem functioning in vents and seeps was highly similar despite environmental differences (e.g. physico-chemistry, dominant basal sources) suggesting that ecological niches are not specifically linked to the nature of fluids. This comparison of seep and vent functioning in the Guaymas basin thus provides further supports to the hypothesis of continuity among deep-sea chemosynthetic ecosystems.

Response and recovery of the Comanche carbonate platform surrounding multiple Cretaceous oceanic anoxic events, northern Gulf of Mexico

The ubiquity of carbonate platforms throughout the Cretaceous Period is recognized as a product of high eustatic sea-level and a distinct climatic optimum induced by rapid sea-floor spreading and elevated levels of atmospheric carbon-dioxide. Notably, a series of global oceanic anoxic events (OAEs) punctuate this time-interval and mark periods of significantly reduced free oxygen in the world's oceans. The best records of these events are often from one-dimensional shelf or basin sections where only abrupt shifts between oxygenated carbonates and anoxic shales are recorded. The Comanche Platform of central Texas provides a unique opportunity to study these events within a well-constrained stratigraphic framework in which their up-dip and down-dip sedimentologic effects can be observed and the recovery of the platform to equilibrium states can be timed and understood. Stable isotope data from whole cores in middle Hauterivian through lower Campanian mixed carbonate-siliciclastic strata are used to construct a 52-myr carbon isotope reference profile for the northern Gulf of Mexico. Correlation of this composite curve to numerous global reference profiles permits identification of several anoxic events and allows their impact on platform architecture and facies distribution to be documented. Oceanic anoxic events 1a, 1b, 1d, and 2 occurred immediately before, after, or during shale deposition in the Pine Island Member, Bexar Member, Del Rio Formation, and Eagle Ford Group, respectively. Oceanic anoxic event 3 corresponds to deposition of the Austin Chalk Group. Platform drowning on three occasions more closely coincided with globally recognized anoxic sub-events such as the Fallot, Albian-Cenomanian, and Mid-Cenomanian events. This illustrates that the specific anoxic event most affecting a given carbonate platform varied globally as a function of regional oceanographic circumstances.Using chemo- and sequence-stratigraphic observations, a four-stage model is proposed to describe the changing facies patterns, fauna, sedimentation accumulation rates, platform architectures, and relative sea-level trends of transgressive-regressive composite sequences that developed in response to global carbon-cycle perturbations. The four phases of platform evolution include the equilibrium, crisis, anoxic, and recovery stages. The equilibrium stage is characterized by progradational shelf geometries and coral-rudist phototrophic faunal assemblages. Similar phototrophic fauna typify the crisis stage; however, incipient biocalcification crises of this phase led to retrogradational shelf morphologies, transgressive facies patterns, and increased clay mineral proportions. Anoxic stages of the Comanche Platform were coincident with back-ground deposition of organic-rich shale on drowned shelves and heterotrophic fauna dominated by oysters or coccolithophorids. Eustatic peaks of this stage were of moderate amplitude (∼30 m), yet relative sea-level rises were greatly enhanced by reduced sedimentation rates. In the recovery stage, heterotrophic carbonate factories re-established at the shoreline as progradational ramp systems and sediment accumulation rates slowly increased as dysoxia diminished. Full recovery to equilibrium conditions may or may not have followed. Geochemical and stratigraphic trends present in the four stages are consistent with increased volcanism along mid-ocean ridges and in large-igneous provinces as primary drivers of Cretaceous OAEs and the resulting transgressive-regressive composite sequences.

Epiphyte toxicity bioassay for ecotoxicological and coastal monitoring

Marine epibionts are organisms that grow on submerged surfaces. Those found on seagrass leaves are especially important because of their interactions with the plants, their contribution to primary production in these ecosystems, and their role as food source for heterotrophic fauna. Given the relative lack of ecotoxicological studies on epibionts, the aim of this study is to evaluate the effect of environmental pollution on epiphytes experimentally attached to artificial devices (mimes) consisting of thermally-sealed silicone tubes supported on bamboo sticks that mimic the morphology of seagrasses and serve as an anchor surface for marine epibionts. Mimes were installed on the sea floor in subtidal waters of the Rio San Pedro (Cádiz), collected after 28days, and incubated in the laboratory with environmental concentrations of atrazine (herbicide), Irgarol (anti-fouling substance), and copper. Tube-dwelling diatoms formed the major component of the epiphyte community. Average surface covering, chlorophyll, and biomass content did not show significant differences between controls and treatments. The glutathione peroxidase activity increased significantly with 4μgL(-1) of atrazine and 5μgL(-1) of copper. This enzymatic activity increase seems to be sufficient to prevent oxidative cellular damage by removing reactive oxygen substances produced by oxidative stress; in addition to this enzyme, there might be other antioxidant enzymes which have not been measured in this study, that have also protected the organism from oxidative damage. Thus, the measurement of antioxidant enzymatic activity in epiphytes may be a useful toxicity indicator for coastal biomonitoring.

Trophic structure of the bathyal benthos at an area with evidence of methane seep activity off southern Chile (~45°S)

Through application of carbon (C) and nitrogen (N) stable isotope analyses, we investigated the benthic trophic structure of the upper-slope off southern Chile (~45°S) including a recent methane seep area discovered as part of this study. The observed fauna comprised 53 invertebrates and seven fish taxa, including remains of chemosymbiotic fauna (e.g.chemosymbiotic bivalves and siboglinid polychaetes), which are typical of methane seep environments. While in close-proximity to a seep, the heterotrophic fauna had a nutrition derived predominantly from photosynthetic sources (δ13C > –21‰). The absence of chemosynthesis-based nutrition in the consumers was likely a result of using an Agassiz trawl to sample the benthos, a method that is likely to collect a mix of fauna including individuals from adjacent non-seep bathyal environments. While four trophic levels were estimated for invertebrates, the fish assemblage was positioned within the third trophic level of the food web. Differences in corrected standard ellipse area (SEAC), which is a proxy of the isotopic niche width, yielded differences for the demersal fishNotophycis marginata(SEAC = 5.1‰) andCoelorinchus fasciatus(SEAC = 1.1‰), suggesting distinct trophic behaviours. No ontogenic changes were detected inC. fasciatusregarding food sources and trophic position. The present study contributes the first basic trophic data for the bathyal area off southern Chile, including the identification of a new methane seep area, among the furthest south ever discovered. Such information provides the basis for the proper sustainable management of the benthic environments present along the vast Chilean continental margin.

Habitat heterogeneity influences cold‐seep macrofaunal communities within and among seeps along the Norwegian margin – Part 2: contribution of chemosynthesis and nutritional patterns

AbstractThe relative contribution of chemosynthesis in heterotrophic fauna at seeps is known to be influenced by depth and by habitat. Using stable isotopes of carbon and nitrogen, we investigated macro‐ and megafaunal nutritional patterns in Norwegian margin cold seeps by comparing food webs both among habitats within a seep site and between different sites. The very active Håkon Mosby mud volcano (HMMV) is characterized by geochemical gradients, microbial activity and faunal zonation from the centre to the periphery. The Storegga Slide (600–900 m depth) has pockmarks with patchy less active seeps, and also shows concentric zonation of habitats but at much smaller spatial scale. The dominant carbon source for macrofaunal nutrition in both areas was chemosynthetically fixed and the bulk of organic carbon was derived from sulphur‐oxidizing bacteria. In HMMV, food chains were clearly separated according to habitats, with significantly lighter δ13C signatures on microbial mats and adjacent sediment (−33.06 to −50.62‰) than in siboglinid fields (−19.83 to −35.03‰). Mixing model outputs revealed that the contribution of methane‐derived carbon was small in siboglinid fields (0–17%) but significant (39–61%) in the microbial mats. Moreover, the variability of macrofauna signatures within this later habitat suggests the co‐occurrence of two food chains, one based on primary production via methanotrophy and the other via sulphide oxidation. The length of the food chains also varied among habitats, with at least one more trophic level in the siboglinid fields located at the periphery of the volcano. Conversely, in Storrega pockmarks, faunal δ13C signatures did not vary among habitats but among species, although separate food chains seem to co‐occur. The small size of the seepage areas and their lower fluxes compared to HMMV allow more background species to penetrate the seep area, increasing the range of δ15N and the trophic level number. Probably due to the higher flux of photosynthetic particulate organic carbon, the overall chemosynthesis‐based carbon contribution in invertebrate nutrition was lower than that in HMMV.

Chemosynthetic trophic support for the benthic community at an intertidal cold seep site at Mocha Island off central Chile

We analyzed C and N stable isotope ratios of benthic fauna and their potential food sources at an intertidal methane seep site and a control site without emanation at Mocha Island (central Chile). The objective was to trace the origin of the main food sources used by the local heterotrophic fauna, based on the hypothesis that chemosynthetic production could be partially fueling the local food web at the seep site. Food sources sampled at both sites included macroalgae, particulate organic matter and bacteria-like filaments found growing over the red algae Gelidium lingulatum within the areas of active methane release. At the control site, located 11 km away from the gas emanation, fauna exhibited moderate δ 13C values ranging from −16.2‰ (in a nereid polychaete) to −14.8‰ (in a cirolanid isopod), which were consistent with those of the potential photosynthetic food sources sampled at this site (−20.2 to −16.5‰). δ 13C values of the photosynthetic food sources at the seep site similarly ranged between −25.4 and −17.9‰. However, a portion of the animals at this site were consistently more 13C-depleted, with δ 13C values close to that of the seeping methane (−43.8‰) and the bacteria-like filaments (−39.2 ± 2.5‰) also collected at this site. Specific examples were the Marphysa sp. polychaetes (δ 13C = −44.7 ± 0.6‰), the Schistomeringos sp. dorvilleid polychaetes (δ 13C = −42.9‰), and the tanaid crustacean Zeuxo marmoratus (δ 13C = −37.3 ± 0.2‰). The significantly higher δ 13C values of the herbivorous gastropod Tegula atra at the seep site (−29.3 ± 3.1‰) than at the control site (−12.6 ± 0.3‰) also indicated differences among sites of the preferred carbon sources of this species. Mixing model estimates indicate that at the seep site bacteria-like filaments could be contributing up to ∼60% of the assimilated diet of selected invertebrates. Furthermore, several indicators of trophic structure, based in isotopic niche metrics, indicate a considerably higher variety of basal resources used at the seep site and a consequent enhanced trophic diversity, compared with the non-seep site. The isotopic data gathered at the seep site clearly and unequivocally reflects the ingestion of a 13C-depleted primary food source, which could be the bacteria-like filaments observed at this site.

Stable isotope signatures and methane use by New Zealand cold seep benthos

The carbon isotopic composition of seep faunal tissue represents a time-integrated view of the interaction between biology and the biogeochemical gradients within the environment. Here we provide an initial description of carbon and nitrogen stable isotope signatures of dominant symbiont-bearing megafauna and heterotrophic mega- and macrofauna from 10 methane-seep sites on the continental margin of the North Island of New Zealand (662–1201 m water depth). Isotopic signatures suggest that sulfide oxidation supports symbiont-bearing taxa including solemyid and vesicomyid bivalves, and methanotrophic symbionts are present in the seep mussel Bathymodiolus sp. Multiple species of Frenulata (Siboglinidae) are present and have a range of isotopic values that are indicative of both thiotroph- and methanotroph-based nutrition. Isotopic composition of the tubeworm Lamellibrachia sp. varied by 23.3‰ among individuals although there was no consistent difference among sites. Variation in methane use by heterotrophic fauna appears to reflect the availability of hard vs. soft substrate; macrofauna on hard substrates had high δ 13C signatures, reflecting consumption of photosynthetic-derived organic matter. Two unique, biotic assemblages were discovered to be fueled largely by methane: a hard-substrate, multi-phyla sponge-associated community (inhabiting the sponge Pseudosuberites sp.) and a soft-sediment assemblage dominated by ampharetid polychaetes. Isotope signatures yield estimates of 38–100% and 6–100% methane-derived carbon in sponge associates and ampharetid-bed macrofauna, respectively. These estimates are comparable to those made for deeper methane seeps at the Florida Escarpment (3290 m) and Kodiak, Alaska seeps (4445 m). The overall high use of methane as a carbon source by both symbiont-bearing and heterotrophic fauna suggests that New Zealand methane seeps are an ideal model system to study the interaction among metazoans, bacteria, archaea, and their resulting effect on methane cycles.

Are spatial variations in the diets of hydrothermal fauna linked to local environmental conditions?

Abstract Trophic relationships in Bathymodiolus azoricus mussel bed communities on the Tour Eiffel hydrothermal edifice (Lucky Strike) were assessed using δ13C and δ15N signatures from 14 hydrothermal species. The nutritional basis of B. azoricus was also investigated with δ34S. Faunal samples and environmental data (temperature, pH, total dissolved sulfide, iron and copper concentrations) were collected from 12 different locations on the edifice. Chemical conditions varied between microhabitats, and were all correlated to temperature. Carbon and nitrogen isotopic results revealed the presence of two, apparently independent, trophic groups. The first was composed of symbiont-bearing fauna (B. azoricus and their associated polychaetes Branchipolynoe seepensis), while the second enclosed heterotrophic fauna (bacterivores, detritivores, scavengers, predators). A majority of mussels displayed δ13C values ranging from −27‰ to −34‰, supporting thiotrophy as the dominant nutritional pathway at Tour Eiffel, with methanotrophy and filter feeding emerging as secondary strategies. This result was corroborated by δ34S signatures. However, higher δ13C values in larger mussels suggested that, as they grow, B. azoricus mussels rely more heavily on their methanotrophic endosymbionts. Significant spatial variability in isotopic signatures for single faunal species was observed at the scale of the edifice for three species (B. azoricus, B. seepensis, Amathys lutzi), and environmental conditions explained variation in isotopic signatures for one-third of the species. This confirms the hypothesis raised by several authors on the role of hydrothermal fluids on the trophic network at small spatial scales. We suggest that vent fluid characteristics, by influencing microbial production, are key factors in the variation of local carbon sources at vents.

Chemoautotrophic Production Incorporated by Heterotrophs in Gulf of Mexico Hydrocarbon Seeps: An Examination of Mobile Benthic Predators and Seep Residents

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 15N depleted nutrient sources (−50 to −65‰ and −9 to −12‰, respectively), indicating methanotrophy using biogenic methane and suggesting ammonium as the dominant nitrogen source. However, those same sources were 34S-enriched (6‰–11‰), 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‰ and another of approximately −40‰, as indicated by the resident heterotrophs. Resident heterotrophs at GC 234 had δ15N and δ34S values from 1‰ to 5‰ and −10‰ to 6‰, 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 δ13C values. In contrast, giant isopods (Bathynomus giganteus Milne Edwards, 1879), captured with the hagfish show negligible incorporation of chemosynthetic production.

Stable Isotope Variation Among the Mussel Bathymodiolus childressi and Associated Heterotrophic Fauna at Four Cold-Seep Communities in the Gulf of Mexico

Efforts to determine the utilization of Gulf of Mexico (GOM) chemosynthetic production by benthic predators have relied on stable isotope differences between photosynthetic and chemosynthetic production. Whereas the photosynthetic δ13C value in GOM surface waters is relatively uniform, chemosynthetic production may differ in different areas depending on prevalence of thiotrophy versus methanotrophy and inorganic carbon source. In this paper we compare the δ13C and δ15N signatures of the symbiont-containing mussel, Bathymodiolus childressi Gustafson, 1998, from four different chemosynthetic sites to test the hypothesis that methanotrophic production results in significant differences among them. Bathymodiolus childressi from two areas characterized by brine seepage and biogenic methane (GC425 and GC233) had very low δ15N (−3.7‰ and −16.6‰) and δ13C (−57.5‰ and −63.5‰) relative to areas with substantial thiotrophic production (GC234 and GC185). Bathymodiolus childressi from each chemosynthetic community had significantly different δ13C, and three of the sites also had distinct δ15N values. The δ13C and δ15N signatures of hagfish (Eptatretus sp.) and giant isopods (Bathynomus giganteus) captured from two sites showed little or no chemosyntheic usage. Squat lobsters (Munidopsis sp.) showed heavy incorporation of chemosyntheic production, but did not directly consume B. childressi.

Nutritional associations among fauna at hydrocarbon seep communities in the Gulf of Mexico

The Gulf of Mexico supports dense aggregations of megafauna associated with hydro- carbon seeps on the Louisiana Slope. The visually dominant megafauna at the seeps — mussels and tube worms — derive their nutrition from symbiotic relationships with sulfide or methane-oxidizing bacteria. The structure of the tube worm aggregations provide biogenic habitat for numerous species of heterotrophic animals. Carbon, nitrogen and sulfur stable isotope analyses of heterotrophic fauna collected with tube worm aggregations in the Green Canyon Lease area (GC 185) indicate that most of these species derive the bulk of their nutrition from chemoautolithotrophic sources. The isotope analyses also indicate that although 2 species may be deriving significant nutritional input from the bivalves, none of the species analyzed were feeding directly on the tube worms. Grazing gastropods and deposit-feeding sipunculids were used to estimate the isotopic value of the free-living chemoau- tolithotrophic bacteria associated with the tube worms (δ 13 C -32 to -20‰; δ 15 N 0 to 7‰; δ 34 S -14 to -1‰). The use of tissue δ 34 S analyses in conjunction with tissue δ 13 C and δ 15 N led to several insights into the trophic biology of the communities that would not have been evident from tissue stable C and N analyses alone.

Use of chemosynthetic biomass by large, mobile, benthic predators in the Gulf of Mexico

The Gulf of Mexico supports communities of chemoautotrophic and heterotrophic fauna associated with hydrocarbon seeps. The chemoautotrophic invertebrates, mostly dense epifaunal assemblages of mussels and tubeworms, derive their nutrition from symbiotic relationships with sulfide- or methane-oxidizing bacteria. The extent to which benthic predatory fauna feed on the chemoautotrophic assemblages has been an open question. Owing to differences in stable isotope values between chemosynthetic- and photosynthetic-derived biomass, isotopic characterization of predatory fauna would be useful in determining their dependence upon chemoautotrophs for food. Carbon and sulfur stable isotope analyses reveal that fishes with similar feeding strategies (rat tail [Nezumia sp.] and eels [Synaphobranchus sp., Ophicthus cruentifer and Dysomma rugosa]) have similar δ 13 C values (-32.7 and -42.5%o, respectively), reflecting chemoautotrophic carbon. Large vagrant predators/scavengers such as isopods Bathynomus giganteus, hagfish Eptatretus sp. and spider crabs Rochina crassa, have isotope values closer to oceanic ranges (δ 13 C: -20 to -18‰; δ 34 S: 18 to 20%o), although some individual Eptatretus sp. and R. crassa show a chemosynthetic component. Colonist invertebrates, such as the sea star (Sclerasterias cf. tanneri) and a predatory snail Buccinum canetae, have greatly depleted δ 13 C and δ 34 S values, indicating an almost 100% reliance on seep production. Nitrogen isotope ratios are depleted (-19%o) in some seep areas, and B. canetae and Synaphobranchus sp. reflect the 15 N depletion (-10 and -3%o respectively). On a species-specific basis, some mobile benthic predators from the background fauna obtain close to 100% of their nutrition from seep production, indicating that they are residents of the seeps. There is a high degree of movement in and out of the seep habitat by vagrant benthic predators, and although the majority derive most of their nutritional needs from photosynthetic production, the incorporation of chemosynthetic production is substantial.

Why did ancient chemosynthetic seep and vent assemblages occur in shallower water than they do today?

Cold-seep communities have relatively low diversity, are dominated by one or two taxa present in high density and high biomass in comparison with the surrounding fauna, and are restricted to aphotic habitats. Their associated heterotrophic fauna are usually distinctive from the fauna of their surroundings. In contrast, a more commonplace chemoautotrophically based community occurs in shallow photic habitats. The associated heterotrophic fauna includes many of the species typical of the surrounding communities and typically dominates abundance, whereas the species with chemoautotrophic symbionts dominate biomass. All modern seep assemblages are deeper than 550 m. Many fossil seep assemblages occurred in water as shallow as the mid-shelf (<200 m). In contrast, communities where species with chemoautotrophic symbionts are biomass dominants, but not numerical dominants, are common in shallow waters at present but rarely reported in the geological record. We suggest that the absence of cold-seep communities on the continental shelf presently is due to a combination of predation and competitive exclusion by primary consumers limiting the presence of species dependent on chemoautotrophic symbionts. We suggest that cold-seep assemblages are more common at shelf depths in the fossil record for two reasons: (a) The biases of preservation have accentuated their distribution by transforming communities where species with chemoautotrophic symbionts dominate by biomass, but not numerically, into cold-seep-appearing assemblages. (b) The importance of predation pressure and oligotrophy has varied, with decreased predation pressure accompanying increased oligotrophy favoring cold-seep communities. We suggest that the paucity of shallow-water assemblages with species harboring chemoautotrophic symbionts as biomass dominants in the fossil record is based on the reliance of paleoecological analysis on numerical abundance data when energy flow analyses are required to identify these assemblages. The distinctiveness of the fossil seep assemblage is intensified by taphonomic processes that bias the assemblage against small individuals and epifaunal species, so that diversity declines, the small heterotrophic component of the assemblage is significantly reduced, and the epifaunal component is minimized. The final assemblage is usually dominated by the better-preserved large infaunal clams which perchance are also the species with chemoautotrophic symbionts. In contrast, preservation does not enhance the distinctiveness of these chemoautotroph-harboring species in shallow water.

Can shallow- and deep-water chemoautotrophic and heterotrophic communities be discriminated in the fossil record?

The recognition of marine chemoautotrophic paleocommunities has added a new dimension to the interpretation of the fossil record. We compared the death assemblages formed by chemoautotrophic and heterotrophic molluscan faunas of the continental slope with their counterparts in shallow water and with a fossil chemoautotrophic analogue from the Tepee Buttes of the Pierre Shale (Cretaceous) to determine whether differences between them could be ascribed to differences in community structure or taphonomy. Evaluation of guild and tier structure and size-frequency distribution using abundance and energy flow (paleoproduction and paleoingestion) suggests that differences between inshore and offshore Recent heterotrophic assemblages reflect autecologic differences in the living communities forming them rather than differences in preservation. In contrast, the degree of similarity between chemoautotrophic assemblages is a function of their taphonomic and autecologic history. The differences observed amongst Recent chemoautotrophic assemblages issue from changes in the abundance and preservability of the small heterotrophic fauna, relatively poorly preserved offshore, and the presence of a large heterotrophic fauna, essentially restricted to shallow water. Taphonomic removal of the small heterotrophs (and juveniles of larger species) and the autecologic absence of large heterotrophs could produce an assemblage equivalent to that of the Cretaceous Tepee Buttes from any one of the Recent inshore or continental slope chemoautotrophic assemblages. Our analysis indicates that shelf communities represent the shallowest communities likely to be identified as fossil cold-seep faunas. Farther inshore, community attributes normally used to distinguish chemoautotrophic and heterotrophic faunas are no longer discriminative. Nearshore communities may have included a dominant chemoautotrophic guild, but recognition would rely solely on the identification of known chemoautotrophic taxa. Community trophic structure has classically been evaluated on the basis of numerical abundance and species composition. Comparing these chemoautotrophic and heterotrophic assemblages demonstrates the importance of evaluating community structure on criteria that more clearly document the way energy flowed through the community, namely paleoproduction and paleoingestion. Many of the unique structural attributes of these assemblages only became obvious using these measures.