Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-03T00:24:27.873Z Has data issue: false hasContentIssue false

Role of physico-chemical environment on gastropod assemblages at hydrothermal vents on the East Pacific Rise (13°N/EPR)

Published online by Cambridge University Press:  24 June 2008

Marjolaine Matabos
Affiliation:
Muséum National d'Histoire Naturelle, Département Milieux et Peuplements Aquatiques, UMR 5178 BOME (MNHN, UPMC, CNRS), CP53, 61 rue Buffon, F-75231 Paris cedex 05, France
Nadine Le Bris
Affiliation:
Ifremer, Département Etudes des Ecosystèmes Profonds, BP70, F-29280 Plouzané, France
Sophie Pendlebury
Affiliation:
National Oceanography Centre, European Way, Southampton, SO14 3ZH, UK
Eric Thiébaut*
Affiliation:
Université Pierre et Marie Curie-Paris 6, Station Biologique de Roscoff, UMR 7144 (CNRS, UPMC), BP 74, F-29682 Roscoff cedex, France
*
Correspondence should be addressed to: Eric Thiébaut Station Biologique de Roscoff, UMR7144BP 74, F-29682 Roscoff cedex, France email: [email protected]

Abstract

Deep-sea hydrothermal vents display extreme and highly variable environmental conditions that are expected to be among the most important factors structuring associated benthic populations and communities. We tested this assumption, focusing on the distribution of gastropods, as well as on the demographic population structure and reproductive biology of one dominant gastropod species in zones characterized by alvinellid polychaetes and vestimentiferan tubeworms. A total of 14 biological samples from both types of habitats were collected at three sites on the East Pacific Rise 13°N vent field in May 2002. At all vents except one, the physico-chemical environment was described in two steps: (1) pH, total sulphide and reduced iron concentrations have been measured in situ in Alvinella habitats and correlations to temperature were assessed at the scale of each sampled vent; and (2) assuming the consistency of these relationships within a single edifice, ranges of physico-chemical factors were estimated for each biological sample from the corresponding fine scale temperature measurements. A total of 11 gastropod species were identified from all samples and 2 main faunal assemblages were distinguished: one dominated by Lepetodrilus elevatus in the alvinellid zone as well as in the vestimentiferan zone, and one dominated by the peltospirids Nodopelta heminoda, N. subnoda and Peltospira operculata confined to the alvinellid zone. Peltospirid gastropods were dominant over lepetodrilid gastropods in the more acidic, sulphide-richer, and hotter environments. Although this pattern could be related to specific physiological tolerances to temperature and sulphide toxicity, the weak correlation between community structure and physico-chemical variables suggests that additional factors are also involved. Particularly, the low species richness and the overwhelming dominance of L. elevatus in one faunal assemblage suggest that this species may outcompete peltospirids and greatly affect community structure. This hypothesis is supported by large differences in the demographic structure and reproductive biology of L. elevatus between the 2 faunal assemblages.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bates, A.E., Tunnicliffe, V. and Lee, R.W. (2005) Role of thermal conditions in habitat selection by hydrothermal vent gastropods. Marine Ecology Progress Series 305, 115.Google Scholar
Chevaldonné, P., Desbruyères, D. and Le Haître, M. (1991) Time-series of temperature from three deep-sea hydrothermal vent sites. Deep-Sea Research Part I 38, 14171430.Google Scholar
Childress, J.J. and Fisher, C.R. (1992) The biology of hydrothermal vent animals: physiology, biogeochemistry, and autotrophic symbioses. Oceanography and Marine Biology: an Annual Review 30, 31104.Google Scholar
Clarke, K.R. and Ainsworth, M. (1993) A method of linking multivariate community structure to environmental variables. Marine Ecology Progress Series 92, 205219.Google Scholar
Clarke, K.R. and Warwick, R.M. (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edition. Plymouth, UK: PRIMER-E Ltd.Google Scholar
Colwell, R.K. (2005) EstimateS v7.5. Statistical estimation of species richness and shared species from samples. User's guide. http://viceroy.eeb.uconn.edu/estimatesGoogle Scholar
Copley, J.T.P., Tyler, P.A., Van Dover, C.L. and Philip, S.J. (2003) Spatial variation in the reproductive biology of Paralvinella palmiformis (Polychaeta: Alvinellidae) from vent field on the Juan de Fuca Ridge. Marine Ecology Progress Series 255, 171181.Google Scholar
Desbruyères, D., Chevaldonné, P., Alayse-Danet, A.-M., Jollivet, D., Lallier, F., Jouin-Toulmond, C., Zal, F., Sarradin, P.-M., Cosson, R., Caprais, J.-C., Arndt, C., O'Brien, J., Guezennec, J., Hourdez, S., Riso, R., Gaill, F., Laubier, L. and Toulmond, A. (1998). Biology and ecology of the ‘Pompeii worm’ (Alvinella Pompejana Desbruyeres and Laubier), a normal dweller of an extreme deep sea environment: a synthesis of current knowledge and recent developments. Deep Sea Research Part II, 45, 383422.Google Scholar
Di Meo-Savoie, C.A., Luther, G.W. and Cary, S.C. (2004) Physicochemical characterization of the microhabitat of the epibionts associated with Alvinella pompejana, a hydrothermal vent annelid. Geochimica et Cosmochimica Acta 68, 2055–2066.Google Scholar
Dreyer, J.C., Knick, K.E., Flickinger, W.B. and Van Dover, C.L. (2005) Development of macrofaunal community structure in mussel beds on the northern East Pacific Rise. Marine Ecology Progress Series 302, 121134.Google Scholar
Gabe, M. 1968. Techniques histologiques. Paris: MassonGoogle Scholar
Govenar, B.W., Freeman, M., Bergquist, D.C., Johnson, G.A. and Fisher, C.R. (2004) Composition of a one-year-old Riftia pachyptila community following a clearance experiment: insight to succession patterns at deep-sea hydrothermal vents. Biological Bulletin. Marine Biological Laboratory, Woods Hole 207, 177182.Google Scholar
Govenar, B.W., Le Bris, N., Gollner, S., Glanville, J., Aperghis, A.B., Hourdez, S. and Fisher, C.R. (2005) Epifaunal community structure associated with Riftia pachyptila aggregations in chemically different hydrothermal vent habitats. Marine Ecology Progress Series 305, 6777.CrossRefGoogle Scholar
Johnson, K.S., Childress, J.J., Beehler, C.L. and Sakamoto-Arnold, C.M. (1994) Biogeochemistry of hydrothermal vent mussel communities: the deep-sea analogue to the intertidal zone. Deep-Sea Research Part I 41, 9931011.CrossRefGoogle Scholar
Johnson, K.S., Childress, J.J., Hessler, R.R., Sakamoto-Arnold, C.M. and Beehler, C.L. (1988) Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep-Sea Research Part II 35, 17231744.CrossRefGoogle Scholar
Jollivet, D. (1996) Specific and genetic diversity at deep-sea hydrothermal vents: an overview. Biodiversity and Conservation 5, 16191653.Google Scholar
Jollivet, D., Empis, A., Baker, M.C., Hourdez, S., Comtet, T., Jouin-Toulmond, C., Desbruyères, D. and Tyler, P.A. (2000) Reproductive biology, sexual dimorphism, and population structure of the deep-sea hydrothermal vent scale-worm, Branchipolynoe seepensis (Polychaeta: Polynoidae). Journal of the Marine Biological Association of the United Kingdom 80, 5568.Google Scholar
Kelly, N.E. and Metaxas, A. (2007) Influence of habitat on the reproductive biology of the deep-sea hydrothermal vent limpet Lepetodrilus fucensis (Vetigastropoda: Mollusca) from the Northeast Pacific. Marine Biology 151, 649662.Google Scholar
Le Bris, N. and Gaill, F. (2007) How does the annelid Alvinella pompejana deal with an extreme hydrothermal environment? Reviews in Environmental Science and Biotechnology 6, 197221.CrossRefGoogle Scholar
Le Bris, N., Govenar, B., Le Gall, C. and Fisher, C.R. (2006a) Variability of physico-chemical conditions in 9°50′N EPR diffuse flow vent habitats. Marine Chemistry 98, 167182.Google Scholar
Le Bris, N., Rodier, P., Sarradin, P.-M. and Le Gall, C. (2006b) Is temperature a good proxy for sulfide in hydrothermal vent habitats? Cahiers de Biologie Marine 47, 465470.Google Scholar
Le Bris, N., Sarradin, P.-M., Birot, D. and Alayse-Danet, A.-M. (2000) A new chemical analyzer for in situ measurement of nitrate and total sulfide over hydrothermal vent biological communities. Marine Chemistry 72, 115.CrossRefGoogle Scholar
Le Bris, N., Sarradin, P.-M. and Caprais, J.-C. (2003) Contrasted sulphide chemistries in the environment of 13°N EPR vent fauna. Deep-Sea Research Part I 50, 737747.Google Scholar
Le Bris, N., Sarradin, P.-M. and Pennec, S. (2001) A new deep-sea probe for in situ pH measurement in the environment of hydrothermal vent biological communities. Deep-Sea Research Part I 48, 1941–1951.CrossRefGoogle Scholar
Le Bris, N., Zbinden, M. and Gaill, F. (2005) Processes controlling the physico-chemical micro-environments associated with Pompeii worms. Deep-Sea Research Part I 52, 10851092.Google Scholar
Lee, R.W. (2003) Thermal tolerance of deep-sea hydrothermal vent animals from the northeast Pacific. Biological Bulletin. Marine Biological Laboratory, Woods Hole 205, 98101.Google Scholar
Luther, G.W., Rozan, T.F., Martial, T., Nuzzio, D.B., Di Meo, C., Shank, T.M., Lutz, R.A. and Cary, S.C. (2001) Chemical speciation drives hydrothermal vent ecology. Nature 410, 813816.Google Scholar
Metaxas, A. (2004) Spatial and temporal patterns in larval supply at hydrothermal vents in the northeast Pacific Ocean. Limnology and Oceanography 49, 1949–1956.Google Scholar
Micheli, F., Peterson, C.H., Mullineaux, L.S., Fisher, C.R., Mills, S.W., Sancho, G., Johnson, G.A. and Lenihan, H.S. (2002) Predation structures communities at deep-sea hydrothermal vents. Ecological Monographs 72, 365382.Google Scholar
Mills, S.W., Mullineaux, L.S. and Tyler, P.A. (2007) Habitat associations in gastropod species at East Pacific Rise hydrothermal vents (9°50′N). Biological Bulletin. Marine Biological Laboratory, Woods Hole 212, 185194.Google Scholar
Mullineaux, L.S., Fisher, C.R., Peterson, C.H. and Schaeffer, S.W. (2000) Tubeworm succession at hydrothermal vents: use of biogenic cues to reduce habitat selection error? Oecologia 123, 275284.CrossRefGoogle ScholarPubMed
Mullineaux, L.S., Mills, S.W. and Goldman, E. (1998) Recruitment variation during a pilot colonization study of hydrothermal vents (9°50′N, East Pacific Rise). Deep-Sea Research Part II 45, 441464.Google Scholar
Mullineaux, L.S., Peterson, C.H., Micheli, F. and Mills, S.W. (2003) Successional mechanism varies along a gradient in hydrothermal fluid flux at deep-sea vents. Ecological Monographs 73, 523542.Google Scholar
Pendlebury, S.J.D. (2004) Ecology of hydrothermal vent gastropods. PhD thesis, University of Southampton, School of Ocean and Earth Science, Southampton, UK.Google Scholar
Pradillon, F., Le Bris, N., Shillito, B., Young, C.M. and Gaill, F. (2005a) Influence of environmental conditions on early developement of the hydrothermal vent polychaete Alvinella pompejana. Journal of Experimental Biology 208, 15511561.CrossRefGoogle Scholar
Pradillon, F., Zbinden, M., Mullineaux, L.S. and Gaill, F. (2005b) Colonisation of newly-opened habitat by a pioneer species, Alvinella pompejana (Polychaeta: Alvinellidae), at East Pacific Rise vent sites. Marine Ecology Progress Series 302, 147157.Google Scholar
Sadosky, F., Thiébaut, E., Jollivet, D. and Shillito, B. (2002) Recruitment and population structure of the vetigastropod Lepetodrilus elevatus at 13°N hydrothermal vent sites on East Pacific Rise. Cahiers de Biologie Marine 43, 399402.Google Scholar
Sarradin, P.-M., Caprais, J.-C., Briand, P., Gaill, F., Shillito, B. and Desbruyères, D. (1998) Chemical and thermal description of the environment of the Genesis hydrothermal vent community (13°N, EPR). Cahiers de Biologie Marine 39, 159167.Google Scholar
Sarrazin, J. and Juniper, S.K. (1999) Biological characteristics of a hydrothermal edifice mosaic community. Marine Ecology Progress Series 185, 119.CrossRefGoogle Scholar
Sarrazin, J., Robigou, V., Juniper, S.K. and Delaney, J.R. (1997) Biological and geological dynamics over four years on a high-temperature sulfide structure at the Juan de Fuca Ridge hydrothermal observatory. Marine Ecology Progress Series 153, 524.Google Scholar
Shank, T.M., Fornari, D.J., Von Damm, K.L., Lilley, M.D., Haymon, R.M. and Lutz, R.A. (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, 465515.CrossRefGoogle Scholar
Taylor, C.D., Wirsen, C.O. and Gaill, F. (1999) Rapid microbial production in filamentous sulfur mats at hydrothermal vents. Applied and Environmental Microbiology 35, 22532255.Google Scholar
Tivey, M.K., Bradleyb, A.M., Joyce, T.M. and Kadkod, D. (2002) Insights into tide-related variability at seafloor hydrothermal vents from time-series temperature measurements. Earth and Planetary Science Letters 202, 693707.Google Scholar
Tsurimi, M. and Tunnicliffe, V. (2003) Tubeworm-associated communities at hydrothermal vents on the Juan de Fuca Ridge, northeast Pacific. Deep-Sea Research Part I 50, 611629.Google Scholar
Van Dover, C.L. (2003) Variation in community structure within hydrothermal vent mussel beds of the East Pacific Rise. Marine Ecology Progress Series 253, 5566.Google Scholar
Visman, B. (1991) Sulfide tolerance: physiological mechanisms and ecological implications. Ophelia 34, 127.Google Scholar
Von Damm, K. and Lilley, M.D. 2004. Diffuse flow hydrothermal fluids from 9°50′N East Pacific Rise: origin, evolution, and biogeochemical controls. In Wilcock, W.S.D., DeLong, E.F., Kelley, D.S., Baross, J.A. and Cary, S.C. (eds) The subseafloor biosphere at Mid-Ocean Ridges. Washington: American Geophysical Union, pp. 243266.Google Scholar
Zar, J.H. (1999) Biostatistical analysis, 4th edition. Upper Saddle River: Prentice-Hall.Google Scholar