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Meio-Epifauna of Costa Rican Cold Seeps Meio-epifauna of Costa Rican Cold Seeps María Adriana Gracia Clavijo Universidad Nacional de Colombia Facultad de Ciencias, Departamento de Biología Instituto de Estudios en Ciencias del Mar – CECIMAR Santa Marta D.T.C.H., Colombia 2018 Meio-epifauna of Costa Rican Cold Seeps María Adriana Gracia Clavijo Tesis de investigación presentada como requisito parcial para optar al título de: Doctor en Ciencias - Biología Director: Sven Zea, Ph.D. Codirectora: Lisa A. Levin, Ph.D. Línea de Investigación: Biología Marina Universidad Nacional de Colombia Facultad de Ciencias, Departamento de Biología Instituto de Estudios en Ciencias del Mar – CECIMAR Santa Marta D.T.C.H., Colombia 2018 A mi madre……… A Nelson y la pequeña gran familia que formamos… Acknowledgements In a very special way, I want to thank my two thesis directors Professors, Dr. Sven Zea, and Dr. Lisa Levin. Thanks to both of them for their dedication and effort in this thesis. I appreciate receiving from two of the greatest marine researchers all their knowledge and guidance always to be better. Several people have contributed to this study through their participation. To Dr. Javier Sellanes (Universidad de Concepción), and the professors Dr. Arturo Acero and Dr. Nestor Campos (Instituto de Estudios en Ciencias del Mar – CECIMAR, Universidad Nacional de Colombia, Caribbean Campus) for their support in the first part of the elaboration of my thesis project. To Ana Milena Cardenas (Universidad Nacional de Colombia) for her excellent collaboration in all the administrative processes of the University. This doctoral dissertation was supported by Colciencias- Colfuturo National Scholarship Grant N° 528. Thanks to Dr. Lisa Levin for let me be a part of her research developed at Scripps Institution of Oceanography - UC San Diego. Also, to Dr. Ben Grupe, who was one of the leaders of the macro project in which this thesis was involved. To Jennifer Gonzales for all her support and collaboration in the laboratory and sample management. Also, to all personnel involved in the cruises conducted by Scripps Institution. The research was supported by the National Science Foundation (NSF grants OCE 0826254 and OCE 0939557). To Dr. Gustavo Fonseca and colleagues for their support during the internship in nematodes carried out in his laboratory (Instituto do Mar - UNIFESP, Santos, Brazil). To Emeritus Professor Dr. William Neal (Grand Valley State University) for his contributions and improvements to Chapter 3. To José Manuel Gonzales (Universidad Nacional de Colombia) for his friendship, and all his guidance and support in the management of information, specifically in Chapter 4. To Fernando Dorado (Invemar) for his support, comments, and improvements to Chapter 4. To Dr. Carlos Neira (Scripps Institution) for his comments and improvements to Chapter 5. To Nadia Santodomingo for her friendship and good advice. To my colleagues at Invemar for their support and good timeshare at the Museum. Especially to Andrea Polanco, Erika Montoya and Miguel Martelo. I would like to thank Nelson Guillermo and his infinite effort for understanding some of what I've done over the years. Everything has been words of encouragement and support. Abstract & Resumen IX Abstract Reducing marine environments include hydrothermal vents, cold seeps, whale carcasses, oxygen minimum zones, sunken wood, accumulated loose seagrasses and other organic remains. Cold seeps are ocean floor areas where pore waters rich in CH4 and H2S, wich reach the upper sediment layer; Temperatures are usually at ambient deep-sea values. Macrofaunal and megafaunal species exhibit symbiotic associations with methane-oxidizing and sulfur-oxidizing bacteria. In this environment, there also are meiofaunal communities (> 42 µm) which throphically link bacterial and macrofaunal food webs. Although ubiquitous and more abundant compared to larger-sized invertebrates, meiofaunal communities are among the least studied and understood components of the deep-sea benthos. The best known meiofaunal community dwells within sea-floor sediments, but an important community, called meio-epifauna, inhabits solid surfaces (i.e., rocks, wood, biogenic material) usually present in these reducing environments, is almost unknown. The presence of these substrates can influence diversity at the microscale through the provision of habitat, food, shelter, and various biotic interactions. In the eastern Pacific, the Costa Rican continental margin has heterogeneous areas with different combinations of reducing systems. This work at seep areas of Costa Rica's Pacific Ocean (between ~380 and 1800 m deep) employed natural substrate samples and in situ experiments (for 10.5 months) to investigate at several scales the relationships between locations, seepage activity, habitats, and substrates with taxon richness, abundance, and community structure of meio-epifaunal metazoans, and the controls over their presence and functions. This dissertation covers a broad range of colonization topics. The first chapter provides an introduction to the study area including some meiofaunal biological aspects. The second chapter looks for understanding on a large scale (six locations) meio-epifauna colonization processes associated with inorganic substrates (authigenic rocks) deployed at actively seeping and inactive sites. The analysis was carried out on both natural and experimental rocks. A rich community was found consisting of 27 meio- epifaunal taxa in natural rocks. Nematodes (58.1 %) followed by copepods (24.9 %) were the most abundant. Inactive areas supported for the highest mean number of individuals (19.2±17.6 (1 SD) ind.10cm-2, n=17). Significant differences in higher taxa composition and abundance were found between locations (Jaco scar, Jaco wall, Mound 11, Mound 12, Mound Quepos, Quepos landslide) and between habitats (Bacterial mats, carbonates, hard coral, mussel beds, near clam beds, Oxygen Minimum Zone, sediments, tubeworms), but not between seepage activities. Different locations exhibit different hydrographic characteristics, with depth and temperature being the variables that best explain the biological scheme found. After 10.5 months of colonization of authigenic rocks, the community was comprised of 14 meio-epifaunal taxa. Copepods accounted for the highest abundances (69 %), followed by nematodes (18 %). Also, the highest mean density was found in inactive areas (26.3±11.3 ind. 10cm-2, n=5) compared to active areas (16.4±16.4 ind. 10cm-2, n=6). As in natural rocks, in Mound 12 carbonate colonizers, significant differences were found between habitats but not between seepage activities. Nematodes were thus confirmed to be the dominant meio-epifaunal group inhabitants of deep-sea environments, but our colonization experiments suggest that copepods are better represented in the early stages of colonization. Chapter 3 discussed colonization on a smaller scale (Mound 12) using organic substrates (wood blocks). In this case, a less diverse community was found with nine meio-epifaunal higher taxa and a total of 9,951 individuals. Copepods accounted for the highest abundances (75 %), followed by nauplii larvae (12 %), and nematodes (10 %). The maximum number of individuals (26.3 ind.10cm-2) was found in wood blocks placed in inactive areas (near active mussel beds). Analysis grouped blocks according to seepage activity and not to habitat, but tests of similarity showed no significant differences in higher taxon composition and abundances, probably owing either to substrate homogeneity or low sample size. Contrary to previous studies, where nematodes appeared as the dominant colonizers in deep-sea environments, in the wood blocks used, copepods were the most abundant representatives, suggesting that this group is one of the most successful colonizing hard-wood substrates that are not yet decomposed. Chapter 4 dealt with copepods in experimental substrates (i.e., wood blocks, carbonates rocks, polychaetes tubes, and clam shells). A total of 24,467 individuals belonging to five orders and 15 families were identified. The order Harpacticoida was the best-represented with respect to families (7) and density (87.5 %). Miraciidae (38.6 %), Ectinosomatidae (34.2 %), Tegastidae (9.4 %) and Ameiridae (4.9 %), accounted for approximately 87.1 % of all copepods density. The highest densities of copepods occur in inactive areas, regardless of the type of experimental substrate, had the highest densities of copepods (16.4±9.9 (1 SD) ind.10cm-2, n=9) compared to active areas (8.8±9.9 ind.10cm-2, n=11). The cluster analysis revealed the presence of a typical configuration (stepped) of assemblages, related to environmental gradients. At the family level analyzed, the assemblage responds to characteristics given by the seepage activity. Also, a turnover in family dominance between Miraciidae and Ectinosomatidae according to seepage activity was observed. Lastly, Chapter 5 used nematodes to examine trophic structure and habitat relationships on natural rocks at Mounds 11 and 12. Nematode faunas were represented by two classes, six orders, 17 families, and 27 genera. The family Xyalidae was most abundant (30.1 %) followed by Comesomatidae (21.2 %) and Linhomoeidae (20.9 %). Daptonema and Metalinhomoeus were the genera reaching the highest density (29.3 % and 18.2 % respectively) in all surveys. The results demonstrate the existence of slight differences between habitats regarding nematode assemblage structure. On the substrates, the assemblages were composed of nematode taxa with different
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