An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea S. Duperron, S. M. Gaudron, C. Rodrigues, M. R. Cunha, C. Decker, K. Olu To cite this version: S. Duperron, S. M. Gaudron, C. Rodrigues, M. R. Cunha, C. Decker, et al.. An overview of chemosyn- thetic symbioses in bivalves from the North Atlantic and Mediterranean Sea. Biogeosciences, European Geosciences Union, 2013, 10 (5), pp.3241-3267. 10.5194/bg-10-3241-2013. hal-01542777 HAL Id: hal-01542777 https://hal.sorbonne-universite.fr/hal-01542777 Submitted on 20 Jun 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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CC Attribution 3.0 License. Open Access Open Access Climate Climate of the Past of the Past Discussions An overview of chemosynthetic symbioses in bivalves from the Open Access Open Access North Atlantic and Mediterranean Sea Earth System Earth System Dynamics 1 1 1,2 2 3 3Dynamics S. Duperron , S. M. Gaudron , C. F. Rodrigues , M. R. Cunha , C. Decker , and K. Olu Discussions 1Universite´ Pierre et Marie Curie, UMR7138 (UPMC CNRS IRD MNHN), Systematique,´ Adaptation, Evolution, 7, quai St. Bernard, batimentˆ A, 75005 Paris, France Open Access Open Access 2Departamento de Biologia and CESAM, Universidade de Aveiro, Campus Universitario´ de Santiago,Geoscientific 3810-193 Aveiro, Geoscientific Portugal Instrumentation Instrumentation 3Laboratoire Environnement Profond, Departement´ Etudes des Ecosystemes` Profonds, CentreMethods Ifremer de Brest,and BP 71, Methods and 29280 Plouzane,´ France Data Systems Data Systems Correspondence to: S. Duperron ([email protected]) Discussions Open Access Open Access Geoscientific Received: 13 November 2012 – Published in Biogeosciences Discuss.: 26 November 2012 Geoscientific Revised: 16 April 2013 – Accepted: 18 April 2013 – Published: 14 May 2013 Model Development Model Development Discussions Abstract. Deep-sea bivalves found at hydrothermal vents, of bivalve symbioses in order to evaluate the capacities of Open Access cold seeps and organic falls are sustained by chemosynthetic these remarkable ecological and evolutionary unitsOpen Access to with- bacteria that ensure part or all of their carbon nutrition. These stand environmental change.Hydrology and Hydrology and symbioses are of prime importance for the functioning of the Earth System Earth System ecosystems. Similar symbioses occur in other bivalve species living in shallow and coastal reduced habitats worldwide. In Sciences Sciences recent years, several deep-sea species have been investigated 1 Introduction Discussions Open Access from continental margins around Europe, West Africa, east- Open Access ern Americas, the Gulf of Mexico, and from hydrothermal Bivalve mollusks occur in a variety of marine and fresh- Ocean Science vents on the Mid-Atlantic Ridge. In parallel, numerous, more water ecosystems, at allOcean depths andScience latitudes. Among other easily accessible shallow marine species have been stud- adaptations, they have evolved various strategies for nutri- Discussions ied. Herein we provide a summary of the current knowledge tion, including filter-feeding using their gills, particle uptake available on chemosymbiotic bivalves in the area ranging using elongated labial palps, and carnivory through reduc- Open Access west-to-east from the Gulf of Mexico to the Sea of Marmara, tion of gills to muscular pumping elements. In someOpen Access remark- and north-to-south from the Arctic to the Gulf of Guinea. able species (e.g., families Tridacnidae and Cardiidae), nu- Solid Earth Characteristics of symbioses in 53 species from the area are trition involves symbiotic interactionsSolid Earth with micro-organisms Discussions summarized for each of the five bivalve families documented such as photosynthetic dinoflagellates. Symbiotic nutrition to harbor chemosynthetic symbionts (Mytilidae, Vesicomyi- through gill-associated bacteria is the most recently discov- dae, Solemyidae, Thyasiridae and Lucinidae). Comparisons ered nutrition mode. It was demonstrated in large clams and Open Access Open Access are made between the families, with special emphasis on mussels found around deep-sea hydrothermal vents, first dis- ecology, life cycle, and connectivity. Chemosynthetic sym- covered in 1977 (Lonsdale, 1977). Scientists were puzzled The Cryosphere when they discoveredThe large fauna,Cryosphere including bivalves and gi- bioses are a major adaptation to ecosystems and habitats Discussions exposed to reducing conditions. However, relatively little is ant tube worms around chimneys emitting high-temperature, known regarding their diversity and functioning, apart from a toxic fluids. In fact, both bivalves and tube worms (Annel- few “model species” on which effort has focused over the last ida: Siboglinidae) were shown to harbor chemoautotrophic 30 yr. In the context of increasing concern about biodiver- bacteria in their tissues. These bacteria oxidize reduced sul- sity and ecosystems, and increasing anthropogenic pressure fur from the fluids, and use the energy acquired to fix inor- on oceans, we advocate a better assessment of the diversity ganic carbon, which is subsequently transferred to their ani- mal host (Cavanaugh, 1983; Rau and Hedges, 1979). Similar, Published by Copernicus Publications on behalf of the European Geosciences Union. 3242 S. Duperron et al.: An overview of chemosynthetic symbioses in bivalves often related, organisms and symbioses were then identified focused on a relatively small number of areas subject to hot at cold seeps and large organic falls occurring in the deep and cold venting, employing manned submersibles and re- sea (Pailleret et al., 2007; Paull et al., 1984; Smith and Baco, motely operated vehicles (Fig. 1). Many cold seep sites have 2003). Subsequent examples of symbioses have been found been explored at varying depths in the Gulf of Mexico (see in much more readily accessible, reduced sediment habitats Cordes et al., 2010, for review), and several hydrothermal such as seagrass beds, mangroves, fjords, and deltas, and vents sites have been explored on the Mid-Atlantic Ridge even in sewage sludge they have been since recorded (Du- (MAR) (Desbruyeres` et al., 2000; van der Heijden et al., bilier et al., 2008; Fisher, 1990), illustrating the unexpected 2012). Other areas have been less intensively investigated, paths emerging scientific fields can follow. As will become such as deep hydrothermal vents in the Caribbean Sea evident in the following text, the term “symbiosis” must be (Piccard vent field, Mid-Cayman Ridge). Cold seeps are interpreted in the broadest sense here, because isolating and beginning to be explored in the Barbados prism, the east evaluating costs and benefits for each partner is not an easy American margin (Blake Ridge), the Sea of Marmara, the task (Douglas, 1994). eastern Mediterranean (Olimpi mud field, Anaximander The occurrence of chemosynthetic symbioses is one of the mounds, Nile deep-sea fan), the Gulf of Cadiz (various mud characteristic features of cold seeps and hydrothermal vent volcanoes), the Norwegian margin (Haakon Mosby mud faunas, because they are responsible for most in situ bio- volcano and Storegga Slide), the Gulf of Guinea (Guiness, logical productivity and fuel the often high-biomass com- Regab, Kouilou), the Arctic margin (Loki’s castle), the munities. That said, symbioses have often been overlooked Caribbean Sea off Colombia, and the Laurentian deep-sea in other habitats, in which symbiotic species tend not to be fan (Connelly et al., 2012; Cosel and Olu, 2009; Van Dover dominant and somewhat smaller. Nevertheless, the ability to et al., 2003; Gebruk et al., 2003; Gracia et al., 2012; Olu associate with chemosynthetic bacteria is a recurring feature et al., 1996; Olu-LeRoy et al., 2007a; Sahling et al., 2008, in the evolution of bivalves, since it has appeared indepen- Cunha et al., 2013). dently in at least five families: the Mytilidae, Vesicomyi- A survey of the literature indicates that approximately 200 dae, Solemyidae, Lucinidae and Thyasiridae. Recent discov- bivalve species, in these areas, belong to families or subfam- eries of associated bacteria in two families (Nucinellidae and ilies specifically reported to be associated with chemosyn- Montacutidae) suggest further species and habitats should be thetic bacteria. This