THESE DE DOCTORAT DE L'UNIVERSITE DE BRETAGNE OCCIDENTALE COMUE UNIVERSITE BRETAGNE LOIRE ECOLE DOCTORALE N° 598 Sciences de la Mer et du littoral Spécialité : Ecologie Marine Par Joan M. ALFARO-LUCAS Influence of hydrothermal activity and substrata nature on faunal colonization processes in the deep sea. Thèse présentée et soutenue à Brest le 10 décembre 2019 Unité de recherche : Unité Etude des Ecosystèmes Profonds (EEP) au laboratoire LEP (Ifremer) Rapporteurs avant soutenance : Composition du Jury : Dr François LALLIER Dr Sabine GOLLNER Professeur, Sorbonne Université Tenure Scientist, Royal Netherlands Institute for Sea Research Dr Jeroen INGELS Dr Eric THIEBAUT Research Faculty, Florida State University Professeur, Sorbonne Université Dr Gérard THOUZEAU (Président du Jury) Research Director, CNRS Dr François LALLIER Professeur, Sorbonne Université Dr Jeroen INGELS Research Faculty, Florida State University Dr Jozée SARRAZIN (Directrice de thèse) Cadre de Recherche, Ifremer Brest Invités : Dr Daniela ZEPPILLI Cadre de Recherche, Ifremer Brest Dr Florence PRADILLON Cadre de Recherche, Ifremer Brest Dr Olivier GAUTHIER Maître de Conférence, Université Bretagne Occidentale iii “It is this contingency that makes it difficult, indeed virtually impossible, to find patterns that are universally true in ecology. This, plus an almost suicidal tendency for many ecologists to celebrate complexity and detail at the expense of bold, first-order phenomena. Of course the details matter. But we should concentrate on trying to see where the woods are, and why, before worrying about the individual tree.” John H. Lawton (1999) iv Acknowledgements I would like to thank so much my supervisors Jozée Sarrazin, Florence Pradillon and Daniela Zeppilli for their massive support, advices and patience during all the thesis. I would like also to thank Dr Loic Michel for the friendship, scientific discussions and help in so many aspects of this work. I would like to thank so much Ifremer for all the support during the thesis. This thesis would not have been possible without the amazing working environment of our lab (LEP+LMEE). To all lab mates and friends, merci beaucoup for these priceless three years. I would like to warmly thank Drs Amanda Bates, Olivier Gauthier and Céline Rommevaux for the advices, comments and suggestions during all committee thesis meetings. I would like to also warmly thank Dr Pedro Peres Neto, and all the people of his lab, for the amazing and intense time in Montreal, it definetly was a turning point for this thesis. Thanks so much to Dr Pedro Martinez Arbizu and his lab for the amazing time in Germany, for the help in the copepod identification and the inspiring discussions about deep-sea biodiversity. Last but not least, I would like to thank Drs François Lallier and Jeroen Ingels for reviewing this manuscript. Thanks so much to Drs Sabine Gollner and Jeroen Ingels for coming from so far, and to all members of the thesis jury for their time. vi vii Als meus pares Anna i Manel, per tot el que ens heu donat, a la meva germana Anna i a la meva companya de vida Romina, per tot el que hem fet i els reptes que encara ens queden. viii Index| ix Index List of figures xiii List of tables xvii Résumé étendu* xxii Introduction The deep sea 1 A striking discovery that broke the rule: deep-sea chemosynthetic- 5 based ecosystems Diversity in space and time: from basin to local scales 7 Are vents discrete patches? The vent sphere of influence 13 Cognate habitats, the stepping-stone hypothesis and the continuum 17 of reducing environments Problematic 20 Promising opportunities and new approaches: hydrothermal vents 22 as natural laboratories Nothing but gradients: productivity, environmental stress and 24 biological interactions Determinants and patterns of environmental stress 25 Productivity, primary producers and its distribution 26 Biological interactions 27 Community assembly 29 Biodiversity and community assembly 31 Energy, environmental stress and their interaction on biodiversity 33 Current community assembly approaches 36 Thesis objectives Chapter 1 42 Chapter 2 43 Chapter 3 44 Index| x Chapter 1 A multifacet database 46 Study area: the Lucky Strike hydrothermal vent and the Eiffel Tower 46 edifice The experiment 50 Sample processing and faunal sorting 54 The taxonomic facet: species and morphospecies 54 The functional facet: species functional traits 59 The isotopic facet: δ13C, δ15N and δ34S stable isotopes 62 Chapter 2 Low environmental stress and productivity regime reduces 70 functional richness along a deep-sea hydrothermal vent gradient Abstract 72 Résumé* 74 Introduction 76 Material and methods 79 Results 86 Discussion 96 Acknowledgements 101 References 102 Apendix S3.1 110 Apendix S3.2 111 Apendix S3.3 117 Apendix S3.4 120 Apendix S3.5 124 Chapter 3 Environment and diversity of ressources structure biodiversity and 127 assemblage composition at deep-sea hydrothermal vents and wood falls Abstract 129 Index| xi Résumé* 130 Introduction 132 Material and methods 136 Results 142 Discussion 152 Acknowledgements 159 References 160 Apendix S4.1 169 Apendix S4.2 170 Apendix S4.3 178 Apendix S4.4 181 Apendix S4.5 186 Apendix S4.6 188 General discussion, conclusions and perspectives Biodiversity at vent systems: active and peripheral habitats 192 Functional richness in hydrothermal vent habitats 196 The relationship between species and functional richness: a matter 196 of scale and a clue to the coexistence of dense faunal assemblages in vent habitats Functional richness in peripheral habitats 199 Biodiversity in wood falls and their relationships with vents 201 Perspectives 209 The productivity-stress-diversity relationship in vents 210 Ecology of vents 218 Biological interactions 220 Relationships between vents, wood falls and other cognate habitats 222 Concluding remarks 224 General References 225 *In French xii Figures&Tables| xiii List of figures Figure 1.1. Relationships of energy measured as particulate organic carbon 4 (POC flux) and ecosystem structure and function in the deep sea. 210Pb Db= Bioturbation intensity. SCOC= sediment community oxygen consumption. Figure from Smith et al. (2008). Figure 1.2. Diagram illustrating the formation and circulation of hydrothermal 7 vents and fluids at an ocean spreading center. Image from NOAA. Figure 1.3. Global distribution of vent hydrothermal vents (circles) along mid- 9 ocean ridges and back-arc basins, denoting different spreading rates. Image from Mullineaux et al. (2017). Figure 1.4. Zonation of species along a hydrothermal vent gradient at the East 11 Scotia Ridge (Southern Ocean). Patterns of zonation in both horizontal (A) and vertical (B). Image from Marsh et al. (2012). Figure 1.5. Conceptual model of faunal succession on the East Pacific Rise 13 hydrothermal vents after the volcanic eruption. Image from Qiu (2010). Figure 1.6. Interaction of hydrothermal vent and deep-sea background 15 habitats. Image from Levin et al. (2016). Figure 1.7. Pillow lava in hydrothermal vent peripheral areas in the Galapagos 17 Ridge. Image from NOAA. Figure 1.8. Conceptual model of faunal succession on deep-sea wood falls 20 showing the different energy-based assemblages and their faunal compositions. Image from Bienhold et al. (2013). Figure 1.9. Current impacts facing deep-sea ecosystems at different depths. 22 Image from Levin and Le Bris (2015). Figure 1.10. Conceptual model of the main gradients found along a deep-sea 25 hydrothermal vent gradient based on successional studies in the East Pacific Rise. Image from Mullineaux et al. (2003). Figure 1.11. Conceptual model of community assembly. Image from 31 HillRisLambers et al. (2010). Figure 1.12. The different components of the β-diversity. β-diversity may be 33 caused by nestedness only (A), turnover only (B), nestedness and turnover (C) or turnover and species loss (D). Image from Baselga (2010). Figure 1.13. Putative changes of the functional structure (2-dimensional 39 functional space) of an 8-species assemblage to a hypothetical disturbance. Image from Mouillot et al. (2013). Figure 2.1. The southeast region of the Lucky Strike vent field located at 1700 52 m depth on the Mid-Atlantic Ridge, south of the Azores. A. Locations of the four deployment sites (red stars) and surrounding main active edifices Figures&Tables| xiv (black squares). Note that the far site is located further west, in the fossil lava lake. Colonized substratum blocks at B. active, C. intermediate, D. periphery and E. far sites. Also visible in the photos are the other types of substratum used in parallel experiments. Figure 2.2. Pictures of the different sites. A. Active site. B. Intermediate site. C. 53 Periphery site. D. Far site. Note the in A and B the by dense assemblages of B. azoricus mussel. The periphery and the far sites located in an area with no visible hydrothermal activity and in a poorly sedimented and on a basaltic seabed, respectively. Figure 2.3. Box plots of temperatures registered during 9 months at the 53 different sites along (Active & Intermediate) and away (Periphery & Far) the Eiffel Tower edifice in the Lucky Strike. Figure 2.4. Histograms of size of Bathymodiolus azoricus colonizing the three 58 (a-c) slate substrata at (A) the active and (B) the intermediate site. Figure 3.1. Percentage of species (Sp), functional entities (FE) and richness 89 (FRic) per site for (A) meio- and (B) macrofauna. Functional richness (volume) represented as the area in a twodimensional PCoA space for (C) meio- and (D) macrofauna. Note that the functional spaces for meiofauna in the periphery and the far sites are fully contained in the functional spaces of the active and the intermediate sites; they are not between them. For macrofauna, although they overlap substantially, the functional volume of the periphery and far sites are not fully contained in the volumes of the hydrothermally active sites, nor are they situated between them. Figure 3.2.