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Ecology and Taxonomy of Free-Living Marine Nematodes from Cienfuegos Bay, Caribbean Sea

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Ecology and Taxonomy of Free-Living Marine Nematodes from Cienfuegos Bay, Caribbean Sea ECOLOGY AND TAXONOMY OF FREE-LIVING MARINE NEMATODES FROM CIENFUEGOS BAY, CARIBBEAN SEA Maickel Armenteros Almanza Promoter: Prof. Dr. Wilfrida Decraemer Co-promoter: Prof. Dr. Magda Vincx Academic year 2009 – 2010 Thesis submitted in partial fulfillment of the requirements for the degree of Doctor in Science (Biology) 2 3 A mis padres, A María Elena Ibarra, Examination and Defense PROMOTER: Prof. Dr. Wilfrida Decraemer, Royal Belgium Institute of Natural Science; Ghent University; Belgium CO-PROMOTER: Prof. Dr. Magda Vincx; Ghent University; Belgium CHAIRMAN OF THE COMMITEE: Prof. Dr. Dominique Adriaens; Ghent University; Belgium READING AND EXAMINATION COMMITTEES: Prof. Dr. Wilfrida Decraemer, Royal Belgium Institute of Natural Science; Ghent University; Belgium Prof. Dr. Gerrit Karssen; Wageningen University; The Netherlands Prof. Dr. Tom Moens; Ghent University; Belgium Dr. Agnes Muthumbi; University of Nairobi, Kenya Dr. Jan Vanaverbeke; Ghent University; Belgium Prof. Dr. Ann Vanreusel; Ghent University; Belgium Prof. Dr. Magda Vincx; Ghent University; Belgium THESIS DEFENDED IN PUBLIC: 2nd, December, 2009 Marine Biology Section, Ghent University, Belgium 7 Summary SUMMARY Present thesis focuses on ecology of assemblages and taxonomy of free-living marine nematodes. Most of the data are from Cienfuegos, a semi-enclosed bay in the Caribbean Sea; but, we also provided data on biodiversity from other areas in Cuban marine waters. Four main topics are included: description of biodiversity patterns, a microcosm experiment about effects of organic enrichment on assemblages, a taxonomic revision of the genus Terschellingia de Man, 1888, and the description of four new genera for science. Spatial and temporal biodiversity patterns of free-living marine nematodes were studied in Cienfuegos Bay, a tropical semi-enclosed basin in the Caribbean Sea. Taxonomic (to species level) and functional (biological trait) approaches were applied for describing the assemblage structure and relating it to abiotic environment based on a sampling scheme in six subtidal stations and three months. Biological trait approach added relevant information to species pattern regarding relationships between diversity patterns and the abiotic environment. The most common trait combinations were deposit feeding nematodes, with intermediate colonising abilities of 2–3 (in a scale from 1 to 5), tail conical cylindrical or filiform and body slender; and their abundance were correlated with depth, organic matter and silt/clay fraction. The number of trait combinations and the number of species was highly correlated suggesting that the increase of biodiversity can lead to potential increase of functional diversity. Chemical pollution (organic enrichment and heavy metals) and hydrodynamic regime possibly drove the biodiversity patterns. The spatial distribution of assemblages is in agreement with the previously supposed existence of two well differentiated basins inside the bay, the northern basin more polluted than the southern one. The low hydrodynamic regime would determine a poor dispersion of nematodes resulting in high spatial variance in the assemblage structure; and also the associated hypoxic conditions and pollutants in sediments can explain the dominance of tolerant nematode species such as Daptonema oxycerca, Sabatieria pulchra, Terschellingia gourbaultae, and Terschellingia longicaudata. A comparison of spatial–temporal patterns of biodiversity between Cienfuegos Bay and other semi- enclosed bays in temperate regions suggests several similarities: nematode assemblages are strongly influenced by anthropogenic disturbance, temporal trends are weak or overridden by spatial ones, and few cosmopolitan genera/species tolerant to pollution and hypoxic conditions are dominant 8 Summary Marine nematodes from subtidal tropical sediments in Cienfuegos Bay were subjected to additions of phyto-detritus (microalgae Spirulina) in a microcosm experiment. The follow up of the experimental conditions was measured at days 0, 4, 15 and 30. Observed effects on the nematodes were a decrease in abundance and diversity, and changes in the taxonomic and trophic structure due to the organic enrichment. The results suggested that the nematodes were not food limited in the microcosms and probably neither in their natural environment. The main factor affecting the nematodes was probably the byproducts (hydrogen sulphide and ammonia) due to enhanced bacterial development in microcosms. Hypoxic conditions occurred in all experimental units, as well in the field suggesting a nematode assemblage adapted to naturally enriched sediments. However, tolerant (dominant) species showed a grade of sensitivity to reduced conditions, in increasing order: Spirinia parasitifera, Terschellingia longicaudata, Metalinhomoeus filiformis, and Sabatieria pulchra. We predict that further organic enrichment in sediments from Cienfuegos Bay may cause a phase shift into a strongly depleted benthic fauna and reduced conditions in water and sediments. The cosmopolitan and often ecologically dominant genus Terschellingia (Nematoda: Linhomoeidae), with 39 nominal species, is taxonomically a problematic taxon. Its species show high morphological plasticity, possess few diagnostic characters and identification keys are lacking. A revision of the genus was carried out based on morphological and morphometric data from the literature and from observations of specimens collected in Cienfuegos Bay, Caribbean Sea, Cuba. The diagnosis of the genus Terschellingia is amended. Of the current 39 nominal species, 16 are considered as valid species based on morphological characters related to size and position of amphidial fovea; presence and position of cephalic and cervical setae; presence, size, and shape of pharyngeal bulb; shape of spicular apparatus and shape of tail. Tabular and pictorial keys were provided based on these characters. Three sympatric species: T. communis, T. gourbaultae and T. longicaudata were redescribed based on recently collected Cuban specimens. Each of them showed relatively large differences in body size in comparison with the respective type specimens, suggesting possible variation due to local environmental differences. The highest intraspecific variation pertains for the most widely spread cosmopolitan species T. longicaudata, suggesting that morphological plasticity enhanced adaptation to different environmental conditions. The notable taxonomic inflation 9 Summary within the genus (14 species inquirenda, 9 junior synonyms), probably also present in other highly specious genera of marine nematodes, can lead to an overestimation of the alpha-diversity. Four new free-living marine nematode genera and species are described: Cienfuegia cachoi gen. nov., sp. nov. (Xyalidae, Chromadorida), Guitartia tridentata gen. nov., sp. nov. (Xyalidae, Chromadorida), Macrodontium gaspari gen. nov., sp. nov. (Microlaimidae, Chromadorida), and Pseudoterschellingia ibarrae gen. nov., sp. nov. (Linhomoeidae, Monhysterida). For each species, detailed morphological descriptions, drawings and photos are provided, tabular keys were built and relationships with other genera within each family are discussed. The following general discussion is focused on five topics: scientific novelties of the research, evaluation of techniques for environmental assessment, coupling between distribution patterns in the nature and microcosm experiments, ecological characterization of the four new species and biodiversity of free-living marine nematode in Cuban marine waters. Future research avenues are presented covering both experimental ecology and molecular taxonomy. Two appendixes are included regard to an ecological study of meio- and macrofaunal assemblages in Havana bay; and a taxonomic checklist of nematodes recorded by the author and colleagues from Cuban marine waters. 10 11 Acknowledgements Acknowledgements Thanks so much to my promoters, Frieda and Magda, who constitute an example of how to work and supporting me in each moment that I needed. To my colleagues and friends, José Andrés and Alexei, who put much effort in this thesis, and it could not be possible without them. The most important that I have, my family and friends, these persons are too many to mention here, they know how much I bring them with me always and elsewhere. I acknowledge to my colleagues at Centro de Investigaciones Marinas, Universidad de La Habana for their support and trust in me during these three years; thanks especially to Ana María, Gaspar, Coqui, Erik G., Raúl, Ariel, Manolo, Lalana, Yureidy, Niurka, Elaine, Carmen, Bárbara, Patricia, Julia, Erick P, Hanaina, Yuriem, Ivan, Coco, and Luis. Equally, I will never forget my colleagues and friends from Cienfuegos for their support, friendship and good moments that we have had in “la Perla del Sur”: the strongest acknowledgements to Lisbet, Cacho, Yusmila, Misael, Carlos, Migue, and Yoan; also, I had the pleasure to dive with Duarte. Special acknowledges to the members of the revision and examination committees of this thesis: Gerrit Karssen, Ann Vanreusel, Tom Moens, Jan Vanaverbeke, Agnes Muthumbi and Dominique Adriaens. Their comments and criticism contributed to improve the document, and constituted a good input to my scientific preparation. “Dankzegging”, to my colleagues at Ghent University by their “technical support”; importantly, they are so welcoming persons that I enjoyed my stay in Belgium and their people. Special thanks to Guy, Isolde, Inge, Annick VK, Tania, Ellen, Marleen,
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