Chemosynthetic communities in the deep sea : ecological studies

Portions of this dissertation were supported by grants from NSF, ONR, Sea Grant, and the WHOI Ocean Ventures Fund, by the WHOI Education Office, the WHOI Biology Department, and an NSF graduate fellowship.

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution May 1989

Deep-sea benthic communities dependent on chemosynthetic primaryproduction are associated with areas of active venting of chemically-modifiedseawater. Patterns in the distribution of species that occurat hydrothermal vents can be used to predict locations of the ventsites. Patterns in the distributions of species among vents along ridgesegments are used to identify the spatial scales over which biologicaland physical processes operate to control community composition. Withina vent, a zonation in species distributions correlates with gradients oftemperature and water chemistry. Along a given ridge segment, ventcommunities share the same species pool, but the relative abundance ofeach species varies from one site to another. On a basin-wide scale,the fauna of vent communities represent biological continua, wheregradual morphological and genetic differentiation in species iscorrelated with increasing distance between vent sites. Differentiationof distinctive faunals assemblages at vents occursat a global scale.Populations of species at vents are established and maintained throughrecruitment of larval stages. To study recruitment processes at ventsites, slate panels were placed at and near vent sites on the seafloorfor varying lengths of time. Size distributions of animals on retrievedpanels suggest that recruitment is an intermittent or continuous processrather than a single episodic event. Recruitment of vent-associatedspecies was greater on panels placed within vent communities compared topanels placed adjacent to these communities, a pattern consistent withthe observed maintenance of communities in discrete regions ofhydrothermal flux.The trophic structure of chemosynthetic communities can be complex.Primary production by chemoautotrophic bacteria can take place withinhost tissues of some invertebrates as well as on surfaces and in thewater column and subsurface conduits. Carbon and nitrogen isotopiccompositions of host tissues can be used to demonstrate the dependenceof symbiont species on chemosynthetically-derived organic material.From the patterns in the isotopic compositions of vent and seepsymbionts, potential sources of inorganic carbon are identified. Deep-waterdissolved inorganic carbon serves as a large, isotopicallybuffered pool of inorganic carbon used by tubeworms and bivalves athydrothermal communities of Juan de Fuca, Gorda, Guaymas Basin, EastPacific Rise, Galapagos, and Marianas vents. Variability in tubewormcarbon isotopic compositions at seeps may be attributed to significantcontributions of isotopically variable DIC in seep effluents. Isotopictechniques are also used to explore trophic relationships among avariety of heterotrophic and symbiont-containing fauna at HangingGardens on the East Pacific Rise and at Marianas vents. Carbon isotopicmeasurements suggest that free-living bacteria are important sources offood at both sites. Nitrogen isotopic analyses show that the Marianascommunity may be simpler in trophic structure than the Hanging Gardenscommunity. The biomass of most known vent sites is conspicuouslydominated by large invertebrates with symbiotic bacteria. At vent siteson the Mid-Atlantic Ridge, large swarms of shrimp dominate the biomass.There is no evidence for endosymbionts in these shrimp, based onanalyses of morphology, stable isotopes, lipopolysaccharides andribulose- l, 5-bisphosphate carboxylase activity. Instead, the shrimpappear to be normal heterotrophs, grazing on free-living microorganismsassociated with black smoker chimneys. High bacterial productivitywithin the sulfide matrix of the chimneys must be required to sustainthe shrimp populations.Hydrothermal vent environments exhibit some of the most extremegradients of temperature and chemistry found in the biosphere. Many ofthe animals that colonize vent sites exhibit adaptations that allow themto exist in such an unusual environment. A novel eye in shrimp fromMid-Atlantic Ridge vents is described. The eye, comprised of a pair oflarge organs within the cephalothorax, contains a visual pigment butlacks image-forming optics. The eye appears to be adapted for detectionof low-level illumination and is suggested to have evolved in responseto a source of radiation associated with the environment of hydrothermalvents. An electronic camera was used to detect light emitted from high-temperature(350°C) plumes that rise from the orifice of black smokerchimneys on the Endeavour Segment of the Juan de Fuca Ridge.Calculations suggest that thermal radiation from hot water may accountfor most of the light detected and that this light may be sufficient forgeothermally-drive photosynthesis by bacteria.