Chemosymbiotic species from the Gulf of Cadiz (NE Atlantic): Distribution, life styles and nutritional patterns

Biogeosciences

Volumn 10, Issue 4, 2013, Pages 2569-2581

  Rodrigues, C F ^a   Hilario A ^a   Cunha, M R ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; BIVALVE; CARBON ISOTOPE; CONTINENTAL MARGIN; MUD VOLCANO; NICHE PARTITIONING; NITROGEN ISOTOPE; POLYCHAETE; SPATIAL DISTRIBUTION; STABLE ISOTOPE; SULFUR ISOTOPE; SYMBIONT; TROPHIC INTERACTION;

ATLANTIC OCEAN; GULF OF CADIZ; IBERIAN MARGIN;

EID: 84880733189     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-10-2569-2013     Document Type: Article

References (70)

1. Becker, E., Macko, S., Lee, R., and Fisher, C.: Stable isotopes provide new insights into vestimentiferan physiological ecology at Gulf of Mexico cold seeps, Naturwissenschaften, 98, 169-174, 2011.
2. Brooks, J. M., Kennicutt, M. C., Fisher, C. R., Macko, S. A., Cole, K., Childress, J. J., Bidigare, R. R., and Vetter, R. D.: Deep-sea hydrocarbon seep communities: evidence for energy and nutritional carbon sources, Science, 238, 1138-1142, 1987.
3. Canfield, D. E.: Biogeochemistry of Sulfur Isotopes, Rev. Mineral. Geochem., 43, 607-636, 2001.
4. Carlier, A., Ritt, B., Rodrigues, C. F., Sarrazin, J., Olu, K., Grall, J., and Clavier, J.: Heterogeneous energetic pathways and carbon sources on deep eastern Mediterranean cold seep communities, Mar. Biol., 157, 2545-2565, 2010.
5. Cary, C., Fry, B., Felbeck, H., and Vetter, R. D.: Multiple trophic resources for a chemoautotrophic community at a cold water brine seep at the base of the Florida Escarpment, Mar. Biol., 100, 411-418, 1989.
6. Cavanaugh, C. M.: Microbial Symbiosis: Patterns of Diversity in the Marine Environment, Am. Zool., 34, 79-89, 1994.
7. Cavanaugh, C. M., Wirsen, C. O., and Jannasch, H. W.: Evidence for Methylotrophic Symbionts in a Hydrothermal Vent Mussel (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge, Appl. Environ. Microb., 58, 3799-3803, 1992.
8. Conway, N. M., Kennicutt Ii, M. C., and Van Dover, C. L.: Stable isotopes in the study of marine chemosynthetic-based ecosystems, in: Methods in ecology: Stable isotopes in ecology and environmental science, edited by: Lajtha, K. and Michener, R., Blackwell scientific, Great Britain, 158-186, 1994.
9. Craig, H., The geochemistry of the stable carbon isotopes. Geochim. Cosmochim. Ac., 3, 53-92, 1953.
10. Cunha, M. R., Rodrigues, C. F., Génio, L., Hilário, A., Ravara, A., and Pfannkuche, O.: Macrofaunal assemblages from mud volcanoes in the Gulf of Cadiz: abundance, biodiversity and diversity partitioning across spatial scales, Biogeosciences, 10, 2553- 2568, doi:10.5194/bg-10-2553-2013, 2013.
11. Dando, P. R., Ridgway, S. A., and Spiro, B.: Sulphide mining by lucinid bivalve molluscs demonstrated by stable sulphur isotope measurements and experimental models, Mar. Ecol.-Prog. Ser., 107, 169-175, 1994.
12. Dando, P. R., Southward, A. J., and Southward, E. C.: Rates of sediment sulphide oxidation by the bivalve mollusc Thyasira sarsi, Mar. Ecol.-Prog. Ser., 280, 181-187, 2004.
13. Dando, P. R., Southward, A. J., Southward, E. C., Lamont, P., and Harvey, R.: Interactions between sediment chemistry and frenulate pogonophores (Annelida) in the north-east Atlantic, Deep- Sea Res. I, 55, 966-996, 2008.
14. Dufour, S. C.: Gill Anatomy and the Evolution of Symbiosis in the Bivalve Family Thyasiridae, Biol. Bull., 208, 200-212, 2005.
15. Dufour, S. C. and Felbeck, H.: Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves, Nature, 426, 65-67, 2003.
16. Duperron, S.: The Diversity of Deep-Sea Mussels and Their Bacterial Symbioses, in: The Vent and Seep Biota, edited by: Kiel, S., Topics in Geobiology, Springer, the Netherlands, 137-167, 2010.
17. Duperron, S., Halary, S., Lorion, J., Sibuet, M., and Gaill, F.: Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae), Environ. Microb., 10, 433-445, 2008.
18. Duperron, S., Rodrigues, C. F., Léger, N., Szafranski, K., Decker, C., Olu, K., and Gaudron, S. M.: Diversity of symbioses between chemosynthetic bacteria and metazoans at the Guiness cold seep site (Gulf of Guinea, West Africa), MicrobiologyOpen, 1, 467- 480, 2012.
19. Fisher, C. R.: Chemoautotrophic and methanotrophic symbioses in marine invertebrates, Aquat. Sci., 2, 399-436, 1990.
20. Fisher, C. R.: Toward an appreciation of hydrothermnal-vent animals: Their environment, physiological ecology, and tissue stable isotope values, in: Seafloor Hydrothermal Systems: Physical, Chemical, Biological, and Geological Interactions, Geophys. Monogr. Ser., AGU, Washington, DC, 297-316, 1995.
21. Fisher, C. R., Brooks, J. M., Vodenichar, J. S., Zande, J. M., Childress, J. J., and Burke Jr., R. A.: The Co-occurrence of Methanotrophic and Chemoautotrophic Sulfur-Oxidizing Bacterial Symbionts in a Deep-sea Mussel, Mar. Ecol., 14, 277-289, 1993.
22. Génio, L., Johnson, S. B., Vrijenhoek, R. C., Cunha, M. R., Tyler, P. A., Kiel, S., and Little, C. T.: New record of "Bathymodiolus" mauritanicus Cosel 2002 from the Gulf of Cadiz (NE Atlantic) mud volcanoes, J. Shellfish Res., 27, 53-61, 2008.
23. Goffredi, S. K. and Barry, J. P.: Species-specific variation in sulfide physiology between closely related Vesicomyid clams, Mar. Ecol.-Prog. Ser., 225, 227-238, 2002.
24. Hensen, C., Nuzzo, M., Hornibrook, E., Pinheiro, L. M., Bock, B., Magalhaes, V. H., and Bruckmann, W.: Sources of mud volcano fluids in the Gulf of Cadiz - indicators for hydrothermal imprint, Geochim. Cosmochim. Ac., 2007.
25. Hilário, A. and Cunha, M. R.: On some frenulate species (Annelida: Polychaeta: Siboglinidae) from mud volcanoes in the Gulf of Cadiz (NE Atlantic), Sci. Mar., 72, 361-371, 2008.
26. Hilário, A., Johnson, S. B., Cunha, M. R., and Vrijenhoek, R. C.: High diversity of frenulates (Polychaeta: Siboglinidae) in the Gulf of Cadiz mud volcanoes: a DNA taxonomy analysis, Deep- Sea Res. I, 57, 143-150, 2010.
27. Hilário, A., Capa, M., Dahlgren, T. G., Halanych, K. M., Little, C. T. S., Thornhill, D. J., Verna, C., and Glover, A. G.: New Perspectives on the Ecology and Evolution of Siboglinid Tubeworms, Plos One, 6, e16309, doi:10.1371/journal.pone.0016309, 2011.
28. Kennicutt, M. C., Bueke, R. A., MacDonald, J. R., Brooks, J. M., Denoux, G. J., and Macko, S. A.: Stable isotope partioning in seep and vent organisms: chemical and ecological significance, in: Isotope Fractionations in Organic Matter: Biosynthetic and Diagenetic Processes., edited by: Macko, S. A. and Engel, M. H., Chem. Geol. (Isot. Geosci. Sect.), 293-310, 1992.
29. Krouse, R.: Sulphur isotopes in our environment, in: Handbook of Environmental Isotope Geochemistry, 1, The Terrestrial Environment A, edited by: Fritz, P. and Fontes, J. C., 2nd Edn., Elsevier, Amsterdam, 435-472, 1980.
30. Krylova, E. M. and Sahling, H.: Vesicomyidae (Bivalvia): Current Taxonomy and Distribution, Plos One, 5, e9957, doi:10.1371/journal.pone.0009957, 2010.
31. Lee, R.W. and Childress, J. J.: Inorganic N assimilation and ammonium pools in a deep-sea mussel containing methanotrophic endosymbionts, Biol. Bull., 190, 373-384, doi:10.2307/1543030, 1996.
32. Levesque, C., Juniper, S. K., and Marcus, J.: Food resource partioning and competition among alvinelled polychaetes of Juan de Fuca Ridge hydrothermal vents, Mar. Ecol.-Prog. Ser., 246, 173-182, 2003.
33. Levin, L.: Ecology of cold seep sediments interactions of fauna with flow chemistry and microbes, Oceanogr. Mar. Biol., 43, 1-46, 2005.
34. Levin, L. A. and Michener, R. H.: Isotopic evidence for chemosynthesis-based nutrition of macrobenthos: The lightness of being at Pacific methane seeps, Limnol.Oceanogr., 47, 1336-1345, 2002.
35. MacAvoy, S. E., Carney, R. S., Fisher, C. R., and Macko, S. A.: Use of chemosynthetic biomass by large, mobile, benthic predators in the Gulf of Mexico, Mar. Ecol.-Prog. Ser., 225, 65-78, 2002.
36. MacAvoy, S. E., Fisher, C. R., Carney, R. S., and Macko, S. A.: Nutritional associations among fauna at hydrocarbon seep communities in the Gulf of Mexico, Mar. Ecol- Prog. Ser., 292, 51-60, 2005.
37. MacAvoy, S. E., Carney, R. S., Morgan, E., and Macko, S. A.: Stable isotope variation among the mussel Bathymodiolus childressi and associated heterotrophic fauna at four cold-seep communities in the Gulf of Mexico, J. Shellfish Res., 27, 147-151, 2008.
38. Mariotti, A.: Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements, Nature, 303, 685-687, 1983.
39. Mazurenko, L. L., Soloviev, V. A., Belenkaya, I., Ivanov, M. K., and Pinheiro, L. M.: Mud volcano gas hydrate in the Gulf of Cadiz, Terra Nova, 14, 321-329, 2002.
40. Mazurenko, L. L., Soloviev, V. A., Gardner, J. M., and Ivanov, M. K.: Gas hydrates in the Ginsburg and Yuma mud volcano sediments (Moroccan Margin): results of chemical and isotopic studies of pore water, Mar. Geol., 195, 201-210, 2003.
41. Niemann, H., Duarte, J., Hensen, C., Omoregie, E., Magalhães, V. H., Elvert, M., L. M., P., Kopf, A., and Boetius, A.: Microbial methane turnover at mud volcanoes of the Gulf of Cadiz, Geochim. Cosmochim. Ac., 70, 5336-5355, 2006.
42. Nuzzo, M., Hornibrook, E. R. C., Hensen, C., Parkes, R. J., Cragg, B. A., Rinna, J., von Deimling, J. S., Sommer, S., Magalhaes, V. H., Reitz, A., Bruckmann, W., and Pinheiro, L. M.: Shallow Microbial Recycling of Deep-Sourced Carbon in Gulf of Cadiz Mud Volcanoes, Geomicrobiol. J., 25, 283-295, 2008.
43. Nuzzo, M., Hornibrook, E. R. C., Gill, F., Hensen, C., Pancost, R. D., Haeckel, M., Reitz, A., Scholz, F., Magalhaes, V. H., Bruckmann, W., and Pinheiro, L. M.: Origin of light volatile hydrocarbon gases in mud volcano fluids, Gulf of Cadiz - evidence for multiple sources and transport mechanisms in active sedimentary wedges, Chem. Geol., 266, 350-363, 2009.
44. Oliver, P. G., Rodrigues, C. F., and Cunha, M. R.: Chemosymbiotic bivalves from the mud volcanoes of the Gulf of Cadiz, NE Atlantic, with descriptions of new species of Solemyidae, Lucinidae and Vesicomyidae, Zookeys, 113, 1-38, 2011.
45. Petersen, J. M., Zielinski, F. U., Pape, T., Seifert, R., Moraru, C., Amann, R., Hourdez, S., Girguis, P. R.,Wankel, S. D., Barbe, V., Pelletier, E., Fink, D., Borowski, C., Bach, W., and Dubilier, N.: Hydrogen is an energy source for hydrothermal vent symbioses, Nature, 476, 176-180, 2011.
46. Pinheiro, L. M., Ivanov, M. K., Sautkin, A., Akmanov, G., Magalhães, V. H., Volkonskya, A., Monteiro, J. H., Somoza, L., Gardnaer, J., Hamouni, N., and Cunha, M. R.: Mud volcanism in the Gulf of Cadiz: results from the TTR-10 cruise, Mar. Geol., 195, 131-151, 2003.
47. Rau, G. H. and Hedges, J. I.: C-13 deplettion in a hydrothermal vent mussel - suggestion of a chemo-synthetic food source, Science, 203, 648-649, 1979.
48. Robinson, J. J. and Cavanaugh, C. M.: Expression of form I and form II Rubisco in chemoautotrophic symbioses: Implications for the interpretation of stable carbon isotope values., Limnol. Oceanogr., 46, 1496-1502, 1995.
49. Rodrigues, C. and Duperron, S.: Distinct symbiont lineages in three thyasirid species (Bivalvia: Thyasiridae) from the eastern Atlantic and Mediterranean Sea, Naturwissenschaften, 98, 281- 287, 2011.
50. Rodrigues, C. F., Oliver, P. G., and Cunha, M. R.: Thyasiroidea (Mollusca: Bivalvia) from the mud volcanoes of the Gulf of Cadiz (NE Atlantic), Zootaxa, 1752, 41-56, 2008.
51. Rodrigues, C. F., Webster, G., Cunha, M. R., Duperron, S., and Weightman, A. J.: Chemosynthetic bacteria found in bivalve speci-es from mud volcanoes of the Gulf of Cadiz, FEMS Microbiol. Ecol., 73, 486-499, 2010.
52. Rodrigues, C. F., Paterson, G. L. J., Cabrinovic, A., and Cunha, M. R.: Deep-sea ophiuroids (Echinodermata: Ophiuroidea: Ophiurida) from the Gulf of Cadiz (NE Atlantic), Zootaxa, 2754, 1-26, 2011a.
53. Rodrigues, C., Hilário, A., Cunha, M.,Weightman, A., andWebster, G.: Microbial diversity in Frenulata (Siboglinidae, Polychaeta) species from mud volcanoes in the Gulf of Cadiz (NE Atlantic), edited by: van Leeuw, A., J. Microbiol., 100, 83-98, 2011b.
54. Rodrigues, C. F., Cunha, M. R., Olu, K., and Duperron, S.: The smaller vesicomyid bivalves in the genus Isorropodon (Bivalvia, Vesicomyidae, Pliocardiinae) also harbour chemoautotrophic symbionts, Symbiosis, 56, 129-137, 2012.
55. Rodrigues, C. F., Cunha, M. R., Génio, L., and Duperron, S.: A complex picture of associations between two host mussels and symbiotic bacteria in the northeast Atlantic, Naturwissenchaften, 100, 21-31, 2013.
56. Sassen, R., Joye, S., Sweet, S. T., DeFreitas, D. A., Milkov, A. V., and MacDonald, I. R.: Thermogenic gas hydrates and hydrocarbon gases in complex chemosynthetic communities, Gulf of Mexico continental slope, Org. Geochem., 30, 485-497, 1999.
57. Schmaljohann, R. and Flügel, H. J.: Methane-oxidizing bacteria in Pogonophora, Sarsia, 72, 91-98, 1987.
58. Schoell, M.: The hydrogen and carbon isotopic composition of methane from natural gases of various origins, Geochim. Cosmochim. Ac., 44, 649-661, 1980.
59. Scott, K. M., Schwedock, J., Schrag, D. P., and Cavanaugh, C. M.: Influence of form IA RubisCI and environmental dissolved inorganic carbin on the 13C of the clam-chemoautotroph symbiosis Solemya velum, Environ. Microbiol., 6, 1210-1219, 2004.
60. Southward, A. J. and Southward, E. C.: Dissolved organic matter and the nutrition of the Pogonophora: a reassessment based on recent studies of their morphology and biology, Kieler Meeresf., 5, 445-453, 1981.
61. Southward, A. J., Southward, E. C., Spiro, B., Rau, G. H., and Tunnicliffe, V.: C-13 C-12 of organisms from Juan de Fuca Ridge Hydrothermal vents - a guide to carbon and food sources, J. Mar. Biol. Assoc. UK, 74, 265-278, 1994.
62. Stadnitskaia, A., Ivanov, M. K., Blinova, V., Kreulen, R., and van Weering, T. C. E.: Molecular and carbon isotopic variability of hydrocarbon gases from mud volcanoes in the Gulf of Cadiz, NE Atlantic, Mar. Petrol. Geol., 23, 281-296, 2006.
63. Stewart, F. J. and Cavanaugh, C. M.: Bacterial endosymbioses in Solemya (Mollusca: Bivalvia) - Model systems for studies of symbiont - host adaptation, edite by: van Leeuw, A., J. Microbiol., 90, 343-360, 2006.
64. Taylor, J. D. and Glover, E. A.: Functional anatomy, chemosymbiosos and evolution of the Lucinidae, in: The Evolutionary biology of Bivalvia, edited by: Harper, E. M., Taylor, J. D., and Crame, J. A., Geological Society, London, 207-225, 2000.
65. Taylor, J. D. and Glover, E. A.: Chemosymbiotic Bivalves, in: The Vent and Seep Biota, edited by: Kiel, S., Topics in Geobiology, Springer Netherlands, 107-135, 2010.
66. Van Dover, C. L. and Fry, B.: Stable isotopic compositions of hydrothermal vent organisms, Mar. Biol., 102, 257-263, 1989.
67. Van Dover, C. L. and Fry, B.: Microorganims as food resources at deep-sea hydrothermal vents, Limnol. Oceanogr., 39, 51-57, 1994.
68. Van Rensbergen, P., Depreiter, D., Pannemans, B., Moerkerke, G., Van Rooij, D., Marsset, B., Akhmanov, G., Blinova, V., Ivanov, M., Rachidi, M., Magalhaes, V., L., P., Cunha, M., and Henriet, J. P.: The El Arraiche mud volcano field at the Moroccan Atlantic slope, Gulf of Cadiz, Mar. Geol., 219, 1-17, 2005.
69. Vanreusel, A., Andersen, A. C., Boetius, A., Connelly, D., Cunha, M. R., Decker, C., Hilário, A., Kormas, K. A., Maignien, L., Olu, K., Pachiadaki, M., Ritt, B., Rodrigues, C. F., Sarrazin, J., Tyler, P. A., Van Gaever, S., and Vanneste, H.: Biodiversity of cold seep ecosystems along the european margins, Oceanography, 110-127, 2009
70. Vetter, R. D. and Fry, B.: Sulfur contents and sulfur-isotope compositions of thiotrophic symbioses in bivalve molluscs and vestimentiferan worms, Mar. Biol., 132, 453-460, 1998.