Chemosynthetic communities in the deep sea : ecological studies

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 1989Deep-sea benthic communities dependent on chemosynthetic primary production are associated with areas of active venting of chemically-modified seawater. Patterns in the distribution of species that occur at hydrothermal vents can be used to predict locations of the vent sites. Patterns in the distributions of species among vents along ridge segments are used to identify the spatial scales over which biological and physical processes operate to control community composition. Within a vent, a zonation in species distributions correlates with gradients of temperature and water chemistry. Along a given ridge segment, vent communities share the same species pool, but the relative abundance of each species varies from one site to another. On a basin-wide scale, the fauna of vent communities represent biological continua, where gradual morphological and genetic differentiation in species is correlated with increasing distance between vent sites. Differentiation of distinctive faunals assemblages at vents occursat a global scale. Populations of species at vents are established and maintained through recruitment of larval stages. To study recruitment processes at vent sites, slate panels were placed at and near vent sites on the seafloor for varying lengths of time. Size distributions of animals on retrieved panels suggest that recruitment is an intermittent or continuous process rather than a single episodic event. Recruitment of vent-associated species was greater on panels placed within vent communities compared to panels placed adjacent to these communities, a pattern consistent with the observed maintenance of communities in discrete regions of hydrothermal flux. The trophic structure of chemosynthetic communities can be complex. Primary production by chemoautotrophic bacteria can take place within host tissues of some invertebrates as well as on surfaces and in the water column and subsurface conduits. Carbon and nitrogen isotopic compositions of host tissues can be used to demonstrate the dependence of symbiont species on chemosynthetically-derived organic material. From the patterns in the isotopic compositions of vent and seep symbionts, potential sources of inorganic carbon are identified. Deep-water dissolved inorganic carbon serves as a large, isotopically buffered pool of inorganic carbon used by tubeworms and bivalves at hydrothermal communities of Juan de Fuca, Gorda, Guaymas Basin, East Pacific Rise, Galapagos, and Marianas vents. Variability in tubeworm carbon isotopic compositions at seeps may be attributed to significant contributions of isotopically variable DIC in seep effluents. Isotopic techniques are also used to explore trophic relationships among a variety of heterotrophic and symbiont-containing fauna at Hanging Gardens on the East Pacific Rise and at Marianas vents. Carbon isotopic measurements suggest that free-living bacteria are important sources of food at both sites. Nitrogen isotopic analyses show that the Marianas community may be simpler in trophic structure than the Hanging Gardens community. The biomass of most known vent sites is conspicuously dominated by large invertebrates with symbiotic bacteria. At vent sites on the Mid-Atlantic Ridge, large swarms of shrimp dominate the biomass. There is no evidence for endosymbionts in these shrimp, based on analyses of morphology, stable isotopes, lipopolysaccharides and ribulose- l, 5-bisphosphate carboxylase activity. Instead, the shrimp appear to be normal heterotrophs, grazing on free-living microorganisms associated with black smoker chimneys. High bacterial productivity within the sulfide matrix of the chimneys must be required to sustain the shrimp populations. Hydrothermal vent environments exhibit some of the most extreme gradients of temperature and chemistry found in the biosphere. Many of the animals that colonize vent sites exhibit adaptations that allow them to exist in such an unusual environment. A novel eye in shrimp from Mid-Atlantic Ridge vents is described. The eye, comprised of a pair of large organs within the cephalothorax, contains a visual pigment but lacks image-forming optics. The eye appears to be adapted for detection of low-level illumination and is suggested to have evolved in response to a source of radiation associated with the environment of hydrothermal vents. An electronic camera was used to detect light emitted from high-temperature (350°C) plumes that rise from the orifice of black smoker chimneys on the Endeavour Segment of the Juan de Fuca Ridge. Calculations suggest that thermal radiation from hot water may account for most of the light detected and that this light may be sufficient for geothermally-drive photosynthesis by bacteria.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