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Stable isotopes provide new insights into vestimentiferan physiological ecology at Gulf of Mexico cold seeps

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Abstract

On the otherwise low-biomass seafloor of the Gulf of Mexico (GoM) continental slope, natural oil and gas seeps are oases of local primary production that support lush animal communities. Hundreds of seep communities have been documented on the continental slope, and nutrition derived from seeps could be an important link in the overall GoM food web. Here, we present a uniquely large and cohesive data set of δ13C, δ15N, and δ34S compositions of the vestimentiferan tubeworms Escarpia laminata and Lamellibrachia sp. 1, which dominate biomass at GoM seeps and provide habitat for hundreds of other species. Our sampling design encompassed an entire region of the GoM lower slope, allowing us for the first time to assess spatial variability in isotope compositions and to robustly address long-standing hypotheses about how vestimentiferans acquire and cycle nutrients over their long lifespan (200+ years). Tissue δ13C values provided strong evidence that larger adult vestimentiferans use their buried roots to take up dissolved inorganic carbon from sediment pore water, while very small individuals use their plume to take up carbon dioxide from the seawater. δ34S values were extremely variable among individuals of the same species within one location (<1 m2 area), indicating high variability in the inorganic sulfur pools on a very small spatial scale. This finding supports the hypothesis that vestimentiferans use their roots to cycle sulfate and sulfide between their symbionts and free-living consortia of sulfate-reducing archaea in the sediment. Finally, consistent differences in δ15N between two cooccurring vestimentiferan species provided the first strong evidence for partitioning of inorganic resources, which has significant implications for the ecology and evolution of this taxonomic group.

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Acknowledgments

We thank the captains, crews, and scientists aboard the research vessel Atlantis and National Oceanographic and Atmospheric Association (NOAA) Ship Ronald H. Brown, as well as the pilots and engineers of the deep submergence vehicle Alvin and the remotely operated vehicle Jason II. We particularly thank Erik Cordes and Stéphane Hourdez for their help and advice on this project and Elizabeth Podowski for reading earlier versions of the manuscript. This work was funded by the Bureau of Ocean Energy Management, Regulation, and Enforcement contract #1435-01-05-CT-39187 and the NOAA Office of Ocean Exploration. The map of the Gulf of Mexico for Fig. 1 was produced by Mary Lee Eggart, Department of Geography and Anthropology, Louisiana State University.

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Correspondence to Erin Leigh Becker.

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Supplementary Table 1

Mean and standard deviation of tissue δ13C, δ15N, and δ34S for each collection. The column titled “N” is the number of individuals sampled. Where the number of individuals sampled for sulfur is different from that of carbon to nitrogen, the number of individuals sampled for sulfur is indicated in parentheses. The site names are based on Bureau of Ocean Energy Management, Regulation, and Enforcement (BOEMRE) lease block designations and consist of a two-letter abbreviation, which stands for the region (AC = Alaminos Canyon, for example) followed by a three-digit number. A “collection” consists of individuals obtained from within a 1-m2 area. The collection name consists of the abbreviation for the study site plus a sequential number where there was more than one collection at a site. (DOC 789 kb)

Supplementary Table 2

Summary of the variability in vestimentiferan tissue stable isotope data among collections. The top portion of the table lists the standard deviation of the mean isotope values among collections. The bottom half of the table lists p values resulting from F tests for equal variances that compare the standard deviation of each pair of isotopes for each species. Asterisks signify significant results given a Bonferroni corrected α of 0.05 (DOC 215 kb)

Supplementary Figure 1

Schematic drawing depicting some of the key processes, sources, and isotope values for carbon and sulfur in seep vestimentiferan habitats (JPEG 356 kb)

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Becker, E.L., Macko, S.A., Lee, R.W. et al. Stable isotopes provide new insights into vestimentiferan physiological ecology at Gulf of Mexico cold seeps. Naturwissenschaften 98, 169–174 (2011). https://doi.org/10.1007/s00114-010-0754-z

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