Chemosynthetic ecosystems are habitats whose food webs rely on chemosynthesis, a process by which bacteria fix carbon using energy from chemicals, rather than sunlight-driven photosynthesis for primary production, and they are found all over the world on the ocean floor. Although these deep-sea habitats are remote, they are increasingly being impacted by human activities such as oil and gas exploration and the imminent threat of deep-sea mining. My dissertation examines deep-sea chemosynthetic ecosystems at several ecological scales to answer basic biology questions and lay a foundation for future researchers studying these habitats. There are two major varieties of chemosynthetic ecosystems, hydrothermal vents and cold seeps, and my dissertation studies both. My first chapter begins at cold seeps and at the population level by modeling the population dynamics and lifespan of a single species of tubeworm, Escarpia laminata, found in the Gulf of Mexico. I found that this tubeworm, a foundation species that forms biogenic habitat for other seep animals, can reach ages over 300 years old, making it one of the longest-lived animals known to science. According to longevity theory, its extreme lifespan is made possible by the stable seep environment and lack of extrinsic mortality threats such as predation. My second chapter expands the scope of my research from this single species to the entire cold seep community and surrounding deep-sea animals common to the Gulf of Mexico. The chemicals released at cold seeps are necessary for chemosynthesis but toxic to non-adapted species such as cold-water corals. Community studies in this area have previously shown that seeps shape community assembly through niche processes. Using fine-scale water chemistry samples and photographic mapping of the seafloor, I found that depressed dissolved oxygen levels and the presence of hydrogen sulfide from seepage affect foundation taxa distributions, but the concentrations of hydrocarbons released from these seeps did not predict the distributions of corals or seep species. In my third chapter I examine seep community assembly drivers in the Costa Rica Margin and compare the macrofaunal composition at the family level to both hydrothermal vents and methane seeps around the world. The Costa Rica seep communities have not previously been described, and I found that depth was the primary driver behind community composition in this region. Although this margin is also home to a hybrid “hydrothermal seep” feature, this localized habitat did not have any discernible influence on the community samples analyzed. When vent and seep communities worldwide were compared at the family-level, geographic region was the greatest determinant of community similarity, accounting for more variation than depth and habitat type. Hydrothermal vent and methane seeps are two chemosynthetic ecosystems are created through completely different geological processes, leading to extremely different habitat conditions and distinct sets of related species. However, at the broadest spatial scale and family-level taxonomic resolution, neutral processes and dispersal limitation are the primary drivers behind community structure, moreso than whether the habitat is a seep or a vent. At more local spatial scales, the abiotic environment of seeps still has a significant influence on the ecology of deep-sea organisms. The millennial scale persistence of seeps in the Gulf of Mexico shapes the life history of vestimentiferan tubeworms, and the sulfide and oxygen concentrations at those seeps determine seep and non-seep species’ distributions across the deep seafloor. / Biology

Vestimentiferan tubeworms of the eastern Pacific Ocean are often keystone species in vent communities. These polychaetes are host to intracellular Gammaproteobacteria symbionts. In this association, the siboglinid worms supply their symbionts with the compounds necessary to chemosynthesis while the sulfide oxidizing bacteria provide their host with the organic molecules necessary for their metabolism. The adult worms lack a digestive system and are therefore completely dependent on their symbionts for their nutrition. Given the obligate nature of the association for the host, it is surprising that the symbionts are not transmitted from parents to offspring but are acquired de novo from the environment at each generation. In other known cases of horizontally acquired mutualism (e.g. Rhizobium-legumes, dinoflagellates- corals), obtaining symbionts from the environment benefit the hosts by allowing for a degree of partner choice. According to the partner choice hypothesis, tubeworms that associate with the best-adapted partner(s) to a specific range of habitat conditions are in turn better adapted to this environment. Of course, this hypothesis assumes that there is diversity within the symbiotic partners. Phylogenetic analyses on the other hand seemed to indicate that nearly all species of vent tubeworms of the eastern Pacific were associated with the same species of symbionts: Candidatus Endoriftia persephone. However, these studies focussed on a few molecular markers. In this thesis, I used in situ hybridization and next generation sequencing to characterize the symbiont diversity at the species and strain level, as well as within individual hosts and across host species. I found that the intra-host symbiont populations are likely composed of multiple strains or lineages of the same bacterial species, that the symbiont populations separated by mid-ocean ridge discontinuities are vicariant, and that other factors such as local environmental conditions or host specificity might participate in shaping the genetic make-up of these populations. / Graduate / 0410 / 0307 / 0715 / 0306 / 0416 / 0329

The hydrothermal vent environment, in its extreme spatial and temporal variability, offers the opportunity to study habitats that are naturally fragmented and unstable. The vestimentiferan tubeworm Ridgeia piscesae is a foundation species inhabiting hydrothermal vent habitat in the Northeast Pacific Ocean. R. piscesae is a phenotypically plastic species and is arranged in a metapopulation spatial structure, with each local population displaying one of a range of morphotypes. Ridgeia piscesae participates in an obligate symbiosis that is dependent on hydrogen sulphide in the hydrothermal vent fluid that supplies each local population. Hydrothermal fluid flow is highly variable in the hydrothermal vent environment and hydrogen sulphide flux is a limiting nutrient for R. piscesae; this variability may create differences in habitat quality. The objective of this study is to determine whether local populations of R. piscesae centered on high and low flux hydrothermal fluid outputs are similar in body condition, reproductive condition, and juvenile recruitment. Using the submersibles ROPOS and Alvin, I collected high flux and low flux sample pairs from within meters of each other at multiple sample sites on Axial Seamount and the Endeavour segment of the Juan de Fuca Ridge. I used morphological measurements, histology and lipid analysis to assess physiological and reproductive condition. I also determined the relative abundances of new and older recruits in high and low flux local populations. I found that low flux habitat was inferior in its ability to support Ridgeia piscesae at all stages in the tubeworm’s life cycle. In terms of body condition, local populations in low flux habitat had lower body weight, greater body length, smaller anterior tube diameter, lower trophosome volume, lower total lipid volume, and lower branchial plume condition. With respect to reproductive condition, local populations in low flux habitat had lower proportions of reproductive individuals, less sperm transfer, lower gonad volume, and fewer mature oocytes; there was no difference in sperm development stages between high and low flux habitat. From the perspective of the individual, low flux tubeworms live longer, and lifetime reproductive output may be comparable to high flux tubeworms. However, turnover is higher in the high flux habitat, so reproductive output of high flux populations is greater than that of low flux populations. Juvenile recruitment was biased toward high flux habitat, although this trend was not significant and recruitment to low flux habitat was still notable. The differences between reproductive output and juvenile recruitment between these habitats support a source-sink model of population dynamics. From the perspective of the metapopulation, low flux habitat is inferior in its ability to support Ridgeia piscesae at all stages in the tubeworm’s life cycle. This distribution of relative contributions to the overall population of a key species in a Marine Protected Area (MPA) should factor into management decisions affecting MPA boundaries and use. / Graduate