2012, Oceanography 25(1):246–255, http://dx.doi.org/10.5670/oceanog.2012.23
Breea Govenar | Rhode Island College, Providence RI, USA
Tectonic and volcanic processes that drive hydrothermal fluid flow and influence its chemistry also regulate the transfer of energy to hydrothermal vent ecosystems. Chemoautotrophic bacteria use the chemical energy generated by mixing the reduced chemicals in hydrothermal fluids with deep-ocean ambient seawater to fix inorganic carbon and produce biomass. These and other microbes, or their products, are then consumed by other organisms, which are subsequently consumed by other organisms. The connections between nutritional sources and consumers form a complex food web that links the lithosphere to the biosphere at hydrothermal vents. This article traces the path of energy transfer from geochemical to biological processes in hydrothermal vent food webs and explores the implications of changes in hydrothermal fluid flux on food web structure. One of the goals of studying food webs at hydrothermal vents is to develop better predictions of community resilience to disturbance and the relationships between community structure and ecosystem function, including productivity and nutrient cycling. In addition, improved understanding of energy transfer through hydrothermal vent food webs is critical for constructing models of chemical fluxes from chemosynthetic-based ecosystems to the open ocean.
Govenar, B. 2012. Energy transfer through food webs at hydrothermal vents: Linking the lithosphere to the biosphere. Oceanography 25(1):246–255, http://dx.doi.org/10.5670/oceanog.2012.23.
Bates, A.E. 2007. Persistence, morphology, and nutritional state of a gastropod hosted bacterial symbiosis in different levels of hydrothermal vent flux. Marine Biology 152:557–568, http://dx.doi.org/10.1007/s00227-007-0709-x.
Banasek-Ritcher, C., L.-F. Bersier, M.-F. Cattin, R. Baltensperger, J.-P. Gabriel, Y. Merz, R.E. Ulanowicz, A.F. Tavares, D.D. Williams, P.C. de Ruiter, and others. 2009. Complexity in quantitative food webs. Ecology 90(6):1,470–1,477, http://dx.doi.org/10.1890/08-2207.1.
Bemis, K., R.P. Lowell, and A. Farough. 2012. Diffuse flow on and around hydrothermal vents at mid-ocean ridges. Oceanography 25(1):182–191, http://dx.doi.org/10.5670/oceanog.2012.16.
Bennett, S.A., P.J. Stratham, D.R.H. Green, N. Le Bris, J.M. McDermott, F. Prado, O.J. Rouxel, K. Von Damm, and C.R. German. 2011. Dissolved and particulate organic carbon in hydrothermal plumes from the East Pacific Rise, 9°50’N. Deep-Sea Research Part I 58:922–931, http://dx.doi.org/10.1016/j.dsr.2011.06.010.
Bergquist, D.C., J.T. Eckner, I.A. Urcuyo, E.E. Cordes, S. Hourdez, S.A. Macko, and C.R. Fisher. 2007. Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web. Marine Ecology Progress Series 330:49–65, http://dx.doi.org/10.3354/meps330049.
Britayev, T.A., D. Martin, E.M. Krylova, R. von Cosel, and T.S. Aksiuk. 2007. Life-history traits of the symbiotic scale-worm Branchipolynoe seepensis and its relationships with host mussels of the genus Bathymodiolus from hydrothermal vents. Marine Ecology 28:1–13, http://dx.doi.org/10.1111/j.1439-0485.2007.00152.x.
Bruno, J.F., and M.D. Bertness. 2001. Habitat modification and facilitation in benthic marine communities. Pp. 201–218 in Marine Community Ecology. M.D. Bertness, S.D. Gaines, and M.E. Hay, eds, Sinauer Associates Inc., Sunderland, MA.
Childress, J.J., and C.R. Fisher. 1992. The biology of hydrothermal vent animals: Physiology, biochemistry and autotrophic symbioses. Pp. 337–441 in Oceanography and Marine Biology: An Annual Review, vol. 30. M. Barnes, H. Barnes, A.D. Ansell, and R.N. Gibson, eds, Routledge.
Crowell, B.W., R.P. Lowell, and K.L. Von Damm. 2008. A model for the production of sulfur floc and “snowblower” events at mid-ocean ridges. Geochemistry Geophysics Geosystems 9, Q10T02, http://dx.doi.org/10.1029/2008GC002103.
DeBevoise, A.E., J.J. Childress, and N.W. Withers. 1990. Carotenoids indicate differences in diet of the hydrothermal vent crab Bythograea therymdron (Brachyura). Marine Biology 105(1):109–115, http://dx.doi.org/10.1007/BF01344276.
de Buron, I., and S. Morand. 2002. Deep-sea hydrothermal vent parasites: Where do we stand? Cahiers Biologie Marine 43:245–246.
De Busserolles, F., J. Sarrazin, O. Gauthier, Y. Gélinas, M.C. Fabri, P.M. Sarradin, and D. Desbruyères. 2009. Are spatial variations in the diets of hydrothermal fauna linked to local environmental conditions? Deep-Sea Research Part II 56:1,649–1,664, http://dx.doi.org/10.1016/j.dsr2.2009.05.011.
Dubilier, N., C. Bergin, and C. Lott. 2008. Symbiotic diversity in marine animals: The art of harnessing chemosynthesis. Nature Reviews Microbiology 6(10):725–740, http://dx.doi.org/10.1038/nrmicro1992.
Erickson, K.L., S.A. Macko, and C.L. Van Dover. 2009. Evidence for a chemoautotrophically based food web at inactive hydrothermal vents (Manus Basin). Deep-Sea Research Part II 56:1,577–1,585, http://dx.doi.org/10.1016/j.dsr2.2009.05.002.
Fisher, C.R., J.J. Childress, S.A. Macko, and J.M. Brooks. 1994. Nutritional interactions in Galapagos Rift hydrothermal vent communities: Inferences from stable carbon and nitrogen isotope analyses. Marine Ecology Progress Series 103:44–55.
Gollner, S., B. Reimer, P.M. Arbizu, N. Le Bris, and M. Bright. 2010. Diversity of meiofauna from the 9°50’N East Pacific Rise across a gradient of hydrothermal fluid emissions. PLoS ONE 5(8):e12321, http://dx.doi.org/10.1371/journal.pone.0012321.
Govenar, B. 2010. Shaping vent and seep communities: Habitat provision and modification by foundation species. Pp. 403–432 in The Vent and Seep Biota: Aspects from Microbes to Ecosystems. S. Kiel, ed., Topics in Geobiology, vol. 33, Springer, http://dx.doi.org/10.1007/978-90-481-9572-5_13.
Govenar, B., and C.R. Fisher. 2007. Experimental evidence of habitat provision by aggregations of Riftia pachyptila at hydrothermal vents on the East Pacific Rise. Marine Ecology 28:3–14, http://dx.doi.org/10.1111/j.1439-0485.2007.00148.x.
Govenar, B., M. Freeman, D.C. Bergquist, G.A. Johnson, and C.R. Fisher. 2004. Composition of a one-year old Riftia pachyptila community following a clearance experiment: Insight to succession patterns at deep-sea hydrothermal vents. The Biological Bulletin 207:177–182. Available online at: http://www.biolbull.org/content/207/3/177.full (accessed January 10, 2012).
Govenar, B., N. Le Bris, S. Gollner, J. Glanville, A.B. Aperghis, S. Hourdez, and C.R. Fisher. 2005. Epifaunal community structure associated with Riftia pachyptila in chemically different hydrothermal vent habitats. Marine Ecology Progress Series 305:67–77, http://dx.doi.org/10.3354/meps305067.
Haymon, R.M., D.J. Fornari, K.L. Von Damm, M.D. Lilley, M.R. Perfit, J.M. Edmond, W.C. Shanks III, R.A. Lutz, J.M. Grebmeier, S. Carbotte, and others. 1993. Volcanic eruption of the mid-ocean ridge along the East Pacific Rise crest at 9°45’–52’N: Direct submersible observations of seafloor phenomena associated with an eruption event in April, 1991. Earth and Planetary Science Letters 119:85–101, http://dx.doi.org/10.1016/0012-821X(93)90008-W.
Huber, J.A., D.A. Butterfield, and J.A. Baross. 2003. Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiology Ecology 43:393–409, http://dx.doi.org/10.1111/j.1574-6941.2003.tb01080.x.
Hugler, M., and S.M. Sievert. 2011. Beyond the Calvin Cycle: Autotrophic carbon fixation in the ocean. Annual Review of Marine Science 3:261–289, http://dx.doi.org/10.1146/annurev-marine-120709-142712.
Jost, G., M.V. Zubkov, E. Yakushev, M. Labrenz, and K. Jürgens. 2008. High abundance and dark CO2 fixation of chemolithoautotrophic prokaryotes in anoxic water of the Baltic Sea. Limnology and Oceanography 53(1):14–22, http://dx.doi.org/10.4319/lo.2008.53.1.0014.
Kelley, D.S., J.A. Baross, and J.R. Delaney. 2002. Volcanoes, fluids and life at mid-ocean ridge spreading centers. Annual Review of Earth and Planetary Sciences 30:385–491, http://dx.doi.org/10.1146/annurev.earth.30.091201.141331.
Kouris, A., S.K. Juniper, G. Frébourg, and F. Gaill. 2007. Protozoan-bacterial symbiosis in a deep-sea hydrothermal vent folliculinid ciliate (Folliculinopsis sp.) from the Juan de Fuca Ridge. Marine Ecology 28:63–71, http://dx.doi.org/10.1111/j.1439-0485.2006.00118.x.
Kouris, A., H. Limén, C.J. Stephens, and S.K. Juniper. 2010. Blue mats: Faunal composition and food web structure in colonial ciliate (Folliculinopsis sp.) mats at Northeast Pacific hydrothermal vents. Marine Ecology Progress Series 412:93–101, http://dx.doi.org/10.3354/meps08675.
Levesque, C., S.K. Juniper, and J. Marcus. 2003. Food resource partitioning and competition among alvinellid polychaetes of Juan de Fuca Ridge hydrothermal vents. Marine Ecology Progress Series 246:173–182, http://dx.doi.org/10.3354/meps246173.
Levesque, C., H. Limén, and S.K. Juniper. 2005. Origin, composition and nutritional quality of particulate matter at deep-sea hydrothermal vents on Axial Volcano, NE Pacific. Marine Ecology Progress Series 289:43–52, http://dx.doi.org/10.3354/meps289043.
Levin, L.A., G.F. Mendoza, T. Konotchick, and R. Lee. 2009. Macrobenthos community structure and trophic relationships within active and inactive Pacific hydrothermal sediments. Deep-Sea Research Part II 56:1,632–1,648, http://dx.doi.org/10.1016/j.dsr2.2009.05.010.
Limén, H., C. Levesque, and S.K. Juniper. 2007. POM in macro-/meiofaunal food webs associated with three flow regimes at deep-sea hydrothermal vents on Axial Volcano, Juan de Fuca Ridge. Marine Biology 153:129–139, http://dx.doi.org/10.1007/s00227-007-0790-1.
Limén, H., S.J. Stevens, Z. Bourass, and S.K. Juniper. 2008. Trophic ecology of siphonostomatoid copepods at deep-sea hydrothermal vents in the northeast Pacific. Marine Ecology Progress Series 359:161–170, http://dx.doi.org/10.3354/meps07344.
Lonsdale, P. 1977. Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep-Sea Research 24:857–863, http://dx.doi.org/10.1016/0146-6291(77)90478-7.
Marcus, J., V. Tunnicliffe, and D.A. Butterfield. 2009. Post-eruption succession of macrofaunal communities at diffuse flow hydrothermal vents on Axial Volcano, Juan de Fuca Ridge, Northeast Pacific. Deep-Sea Research Part II 56:1,586–1,598, http://dx.doi.org/10.1016/j.dsr2.2009.05.004.
McCollom, T.M., and J.S. Seewald. 2007. Abiotic synthesis of organic compounds in deep-sea hydrothermal environments. Chemical Reviews 107(2):382–401, http://dx.doi.org/10.1002/chin.200720264.
McCollom, T.M., and E.L. Shock. 1997. Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochimica et Cosmochimica Acta 61:4,375–4,391, http://dx.doi.org/10.1016/S0016-7037(97)00241-X.
Menge, B.A., and J.P. Sutherland. 1987. Community regulation: Variation in disturbance, competition, and predation in relation to environmental stress and recruitment. American Naturalist 130:730–757, http://dx.doi.org/10.1086/284741.
Micheli, F., C.H. Peterson, L.S. Mullineaux, C.R. Fisher, S.W. Mills, G. Sancho, G.A. Johnson, and H.S. Lenihan. 2002. Predation structures communities at deep-sea hydrothermal vents. Ecological Monographs 72:365–382, http://dx.doi.org/10.1890/0012-9615(2002)072[0365:PSCADS]2.0.CO;2.
Pimm, S.L. 2002. Food Webs. The University of Chicago Press, Chicago, IL, 258 pp.
Phleger, C.F., M.M. Nelson, A.K. Groce, S.C. Cary, K.J. Coyne, J.A.E. Gibson, and P.D. Nichols. 2005a. Lipid biomarkers of deep-sea hydrothermal vent polychaetes: Alvinella pompejana, A. caudata, Paralvinella grasslei and Hesiolyra bergii. Deep-Sea Research Part I 52:2,333–2,352, http://dx.doi.org/10.1016/j.dsr.2005.08.001.
Phleger, C.F., M.M. Nelson, A.K. Groce, S.C. Cary, K.J. Coyne, and P.D. Nichols. 2005b. Lipid composition of deep-sea hydrothermal vent tubeworm Riftia pachyptila, crabs Munidopsis subsquamosa and Bythograea thermydron, mussels Bathymodiolus sp., and limpets Lepetodrilus spp. Comparative Biochemistry and Physiology Part B 141:196–210.
Pomeroy, L.R., P.J.B. Williams, F. Azam, and J.E. Hobbie. 2007. The microbial loop. Oceanography 20(2):28–33, http://dx.doi.org/10.5670/oceanog.2007.45.
Polz, M.F., J.T. Robinson, C.M. Cavanaugh, and C.L. Van Dover. 1998. Trophic ecology of massive shrimp aggregations at a Mid-Atlantic Ridge hydrothermal vent site. Limnology and Oceanography 43(7):1,631–1,638, http://dx.doi.org/10.4319/lo.1922.214.171.1241.
Sancho, G., C.R. Fisher, S. Mills, F. Micheli, G.A. Johnson, H.S. Lenihan, C.H. Peterson, and L.S. Mullineaux. 2005. Selective predation by the zoarcid fish Thermarces cerebus at hydrothermal vents. Deep-Sea Research Part I 52:837–844, http://dx.doi.org/10.1016/j.dsr.2004.12.002.
Sauvadet, A.-L., A. Gobet, and L. Guillou. 2010. Comparative analysis between protist communities from the deep-sea pelagic ecosystem and specific hydrothermal habitats. Environmental Microbiology 12(11):2,946–2,964, http://dx.doi.org/10.1111/j.1462-2920.2010.02272.x.
Shank, T.M., D.J. Fornari, K.L. Von Damm, M.D. Lilley, R.M. Haymon, and R.A. Lutz. 1998. Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9°50’N, East Pacific Rise). Deep-Sea Research Part II 45:465–515, http://dx.doi.org/10.1016/S0967-0645(97)00089-1.
Shock, E., and P. Canovas. 2010. The potential for abiotic organic synthesis and biosynthesis at seafloor hydrothermal systems. Geofluids 10:161–192, http://dx.doi.org/10.1111/j.1468-8123.2010.00277.x.
Skebo, K., V. Tunnicliffe, I.G. Berdeal, and H.P. Johnson. 2006. Spatial patterns of zooplankton and nekton in a hydrothermally active axial valley on Juan de Fuca Ridge. Deep-Sea Research Part I 53:1,044–1,060, http://dx.doi.org/10.1016/j.dsr.2006.03.001.
Takai, K., S. Nakagawa, A.-L. Reysenbach, and J. Hoek. 2006. Microbial ecology of mid-ocean ridges and back-arc basins. Pp. 185–213 in Back-Arc Spreading Systems: Geological, Biological, Chemical, and Physical Interactions. D.M. Christie, C.R. Fisher, S.-M. Lee, and S. Givens, eds, Geophysical Monograph Series, vol. 166, American Geophysical Union, Washington, DC.
Taylor, G.T., M. Iabichella, T.-Y. Ho, M.I. Scranton, R.C. Thunell, F. Muller-Karger, and R. Varela. 2001. Chemoautotrophy in the redox transition zone of the Cariaco Basin: A significant midwater source of organic carbon production. Limnology and Oceanography 46(1):148–163, http://dx.doi.org/10.4319/lo.2001.46.1.0148.
Taylor, C.D., and C.O. Wirsen. 1997. Microbiology and ecology of filamentous sulfur formation. Science 277:1,483–1,485, http://dx.doi.org/10.1126/science.277.5331.1483.
Terlizzi, C.M., M.E. Ward, and C.L. Van Dover. 2004. Observations on parasitism in deep-sea hydrothermal vent and seep limpets. Diseases of Aquatic Organisms 62:17–26.
Tunnicliffe, V. 1991. The biology of hydrothermal vents: Ecology and evolution. Oceanography and Marine Biology: An Annual Review 29:319–407.
Tunnicliffe, V., J.A. Baross, A. Gebruk, A.O. Giere, A. Koschinsky, A.L. Reysenbach, T.M. Shank, and M. Summit. 2003. Group Report: What are the interactions between biotic processes at vents and physical, chemical and geological conditions? Pp. 251–270 in Energy and Mass Transfer in Marine Hydrothermal Systems. P.E. Halbach, V. Tunnicliffe, and J.R. Hein, eds, Dahlem Press, Berlin.
Tunnicliffe, V., R.W. Embley, J.F. Holden, D.A. Butterfield, G.J. Massoth, and S.K. Juniper. 1997. Biological colonization of new hydrothermal vents following an eruption on Juan de Fuca Ridge. Deep-Sea Research Part I 44:1,627–1,644, http://dx.doi.org/10.1016/S0967-0637(97)00041-1.
Tunnicliffe, V., J.M. Rose, A.E. Bates, and N.E. Kelley. 2008. Parasitization of a hydrothermal vent limpet (Lepetodrilidae, Vetigastropoda) by a highly modified copepod (Chitonophilidae, Cyclopoida). Parasitology 135:1,281–1,293, http://dx.doi.org/10.1017/S0031182008004721.
Van Dover, C.L. 2011. Mining seafloor massive sulphides and biodiversity: What is at risk? ICES Journal of Marine Science 68:341–348, http://dx.doi.org/10.1093/icesjms/fsq086.
Van Dover, C.L., and B. Fry. 1989. Stable isotopic compositions of hydrothermal vent organisms. Marine Biology 102:257–263, http://dx.doi.org/10.1007/BF00428287.
Van Dover, C.L., M.E. Ward, J.L. Scott, J. Underdown, B. Anderson, C. Gustafson, M. Whalen, and R.B. Carnegie. 2007. A fungal epizootic in mussels at a deep-sea hydrothermal vent. Marine Ecology 28:54–62, http://dx.doi.org/10.1111/j.1439-0485.2006.00121.x.
Vanreuesel, A., A. De Groote, S. Gollner, and M. Bright. 2010. Ecology and biogeography of free-living nematodes associated with chemosynthetic environments in the deep sea: A review. PLoS ONE 5(8):e12449, http://dx.doi.org/10.1371/journal.pone.0012449.
Voight, J. 2005. Hydrothermal vent octopuses of Vulcanoctopus hydrothermalis, feed on bathypelagic amphipods of Halice hesmonectes. Journal of the Marine Biological Association of the United Kingdom 85:985–988, http://dx.doi.org/10.1017/S0025315405011999.
Voight, J.R., and J.D. Sigwart. 2007. Scarred limpets at hydrothermal vents: Evidence of predation by deep-sea whelks. Marine Biology 152:129–133, http://dx.doi.org/10.1007/s00227-007-0669-1.
Von Damm, K.L., and M.D. Lilley. 2004. Diffuse flow hydrothermal fluids from 9°50’N East Pacific Rise: Origin, evolution and biogeochemical controls. Pp. 245–268 in The Subseafloor Biosphere at Mid-Ocean Ridges. W.S. Wilcock, E.F. DeLong, D.S. Kelley, J.A. Baross, and S.C. Cary, eds., Geophysical Monograph Series, vol. 144, American Geophysical Union, Washington, DC.
Ward, M.E., C.D. Jenkins, and C.L. Van Dover. 2003. Functional morphology and feeding strategy of the hydrothermal-vent polychaete Archinome rosacea (family Archinomidae). Canadian Journal of Zoology 81:582–590, http://dx.doi.org/10.1139/z03-034.
Yilmaz, A., Y. Çoban-Yiliz, F. Telli-Karakoç, and A. Bologa. 2006. Surface and mid-water sources of organic carbon by photoautotrophic and chemoautotrophic production in the Black Sea. Deep-Sea Research Part II 53:1,988–2,004, http://dx.doi.org/10.1016/j.dsr2.2006.03.015.