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An Overview of Chemosynthetic Symbioses in Bivalves

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An Overview of Chemosynthetic Symbioses in Bivalves Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Biogeosciences Discuss., 9, 16815–16875, 2012 www.biogeosciences-discuss.net/9/16815/2012/ Biogeosciences doi:10.5194/bgd-9-16815-2012 Discussions BGD © Author(s) 2012. CC Attribution 3.0 License. 9, 16815–16875, 2012 This discussion paper is/has been under review for the journal Biogeosciences (BG). An overview of Please refer to the corresponding final paper in BG if available. chemosynthetic symbioses in An overview of chemosynthetic bivalves symbioses in bivalves from the North S. Duperron et al. Atlantic and Mediterranean Sea Title Page S. Duperron1, S. M. Gaudron1, C. F. Rodrigues1,2, M. R. Cunha2, C. Decker3, and Abstract Introduction K. Olu3 Conclusions References 1Universite´ Pierre et Marie Curie, UMR7138 (UPMC CNRS IRD MNHN), Systematique,´ Tables Figures Adaptation, Evolution, 7, quai St. Bernard, batimentˆ A, 75005 Paris, France 1Departamento de Biologia and CESAM, Universidade de Aveiro, Campus Universitario´ de Santiago, 3810-193 Aveiro, Portugal J I 3Laboratoire Environnement Profond, Departement´ Etudes des Ecosystemes` Profonds, Centre Ifremer de Brest, BP 71, 29280 Plouzane,´ France J I Received: 13 November 2012 – Accepted: 20 November 2012 Back Close – Published: 26 November 2012 Full Screen / Esc Correspondence to: S. Duperron ([email protected]) Published by Copernicus Publications on behalf of the European Geosciences Union. Printer-friendly Version Interactive Discussion 16815 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Abstract BGD Deep-sea bivalves found at hydrothermal vents, cold seeps and organic falls are sus- tained by chemosynthetic bacteria which ensure part or all of their carbon nutrition. 9, 16815–16875, 2012 These symbioses are of prime importance for the functioning of the ecosystems. Sim- 5 ilar symbioses occur in other bivalve species living in shallow and coastal reduced An overview of habitats worldwide. In recent years, several deep-sea species have been investigated chemosynthetic from continental margins around Europe, West Africa, East America, the Gulf of Mex- symbioses in ico, and from hydrothermal vents on the Mid-Atlantic Ridge. In parallel, numerous more bivalves easily accessible shallow marine species were studied. We here provide a summary 10 of the current knowledge available on chemosymbiotic bivalves in the area ranging S. Duperron et al. west-to-east from the Gulf of Mexico to Marmara Sea, and north-to-south from the Arctic to the Gulf of Guinea. Characteristics of symbioses in 51 species from the area are summarized for each of the five bivalve families documented to harbor chemosyn- Title Page thetic symbionts (Mytilidae, Vesicomyidae, Solemyidae, Thyasiridae and Lucinidae), Abstract Introduction 15 and compared among families with special emphasis on ecology, life cycle, and con- nectivity. Chemosynthetic symbioses are a major adaptation to ecosystems and habi- Conclusions References tats exposed to reducing conditions, yet relatively little is known regarding their diversity Tables Figures and functioning apart from a few “model species” on which effort has focused over the last 30 yr. In the context of increasing concern about biodiversity and ecosystems, and J I 20 increasing anthropogenic pressure on Oceans, we advocate for a better assessment of bivalve symbioses diversity in order to evaluate the capacities of these remarkable J I ecological and evolutionary units to withstand environmental change Back Close 1 Introduction Full Screen / Esc Bivalve mollusks occur in a variety of marine and freshwater ecosystems, at all depths Printer-friendly Version 25 and latitudes. Among other adaptations, they have evolved various strategies for nu- trition, including filter-feeding using their gills, particle uptake using elongated labial Interactive Discussion 16816 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | palps, and carnivory through reduction of gills to muscular pumping elements. In some remarkable species (e.g. families Tridacnidae and Cardiidae), nutrition involves symbi- BGD otic interactions with micro-organisms such as photosynthetic dinoflagellates. Symbi- 9, 16815–16875, 2012 otic nutrition through gill-associated bacteria is the most recently discovered nutrition 5 mode. It was demonstrated in large clams and mussels found around deep-sea hy- drothermal vents, which were discovered in 1977 (Lonsdale, 1977). Authors were puz- An overview of zled when they discovered large fauna around chimneys emitting high-temperature, chemosynthetic toxic fluids. In fact, bivalves as well as some giant tubeworms (Annelida: Siboglinidae) symbioses in were shown to harbor chemoautotrophic bacteria in their tissues. These bacteria oxi- bivalves 10 dize reduced sulfur from the fluids, and use the energy acquired to fix inorganic car- bon, which is subsequently transferred to their animal host (Cavanaugh, 1983; Rau S. Duperron et al. and Hedges, 1979). Similar and often related organisms and symbioses were then identified at cold seeps and large organic falls occurring in the deep sea (Pailleret et Title Page al., 2007; Paull et al., 1984; Smith and Baco, 2003) and subsequently, illustrating the 15 occasionally strange paths which a developing scientific field can take, in much more Abstract Introduction readily accessible habitats such as seagrass beds, mangroves, fjords, deltas, coastal reduced sediments, and even sewage sludge (Dubilier et al., 2008; Fisher, 1990). As Conclusions References will become evident in the following text, the term “symbiosis” must be interpreted in Tables Figures the broadest sense here, because isolating and evaluating costs and benefits for each 20 partner is far from an easy task (Douglas, 1994). J I The occurrence of chemosynthetic symbioses is one of the characteristic features of cold seeps and hydrothermal vent faunas, because they are responsible for most J I in situ primary production and fuel the high-biomass communities. That said, sym- Back Close bioses have often been overlooked in other habitats, in which symbiotic species tend 25 not to be dominant and somewhat smaller. Nevertheless, the ability to associate with Full Screen / Esc chemosynthetic bacteria is a recurring feature in the evolution of bivalves, since it has appeared independently in at least five families, the Mytilidae, Vesicomyidae, Solemyi- Printer-friendly Version dae, Lucinidae and Thyasiridae, and possibly more (e.g. Nucinellidae). Tight evolution- ary relationships exist between metazoans and their associated symbionts in various Interactive Discussion 16817 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | habitats, as evidenced by several studies supporting that deep-sea vent and seep bi- valve species tend to derive from shallow-water ancestors (Craddock et al., 1995; Little BGD and Vrijenhoek, 2003; Lorion et al., 2010; Williams et al., 2004). Examining the intra- 9, 16815–16875, 2012 and interspecific diversity displayed by chemosynthetic symbioses in as many species 5 as possible, in parallel with the functional, ecological, biogeographical and evolution- ary trends that exist in symbiotic systems will provide greater insight into this critical An overview of adaptation to reducing habitats. chemosynthetic The Atlantic Ocean opened relatively recently (∼ 180 MY), after fragmentation of the symbioses in Pangaea. Today, the northern hemisphere the Atlantic is connected with the Mediter- bivalves 10 ranean Sea and the Gulf of Mexico. The Mediterranean only re-connected with the At- lantic following the Messinian Salinity Crisis (5.96–5.33 MYA) during which it essentially S. Duperron et al. evaporated (Duggen et al., 2003). The Gulf of Mexico became exclusively connected to the Atlantic after the rise of the Isthmus of Panama about 5 MYA, restricting exchanges between the Pacific and Atlantic (Woods Hole Oceanographic Institution website). In Title Page 15 this context, the North Atlantic makes for an interesting focus area for investigating colo- Abstract Introduction nization, evolution and biogeography of chemosynthetic symbioses. This is supported by the fact that shallow-water coastal areas of the northern Atlantic, Gulf of Mexico Conclusions References and Mediterranean have been investigated in detail since a long time, and information Tables Figures regarding the diversity of bivalves are some of the most accurate available, although 20 certainly not exhaustive. On the continental shelf and in the deep-sea, most of the sam- J I pling effort has focused on a relatively small number of areas subject to hot and cold venting, which have been studied using manned submersibles and Remotely Operated J I Vehicles (Fig. 1). Many cold seep sites have been explored at varying depths in the Gulf Back Close of Mexico (see Cordes et al., 2010 for review) and several hydrothermal vents sites 25 have been explored on the Mid-Atlantic Ridge (MAR) including Lucky Strike, Menez Full Screen / Esc Gwen, Rainbow, Broken Spur, Lost City, TAG, Snake Pit, Logatchev, 5◦ S and 9◦ S (Desbruyeres` et al., 2000; van der Heijden et al., 2012). Other areas have been less Printer-friendly Version intensively or more recently investigated. These include deep vents in the Caribbean Sea (Piccard vent field, Mid-Cayman Ridge), cold seeps on the Barbados prism, the Interactive Discussion 16818 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | east American margin (Blake ridge), in the Marmara sea,
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