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Nutritional Relations of Deep-Sea Hydrothermal Fields at the Mid-Atlantic Ridge: a Stable Isotope Approach

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Nutritional Relations of Deep-Sea Hydrothermal Fields at the Mid-Atlantic Ridge: a Stable Isotope Approach DEEP-SEA RESEARCH Part I PERGAMON Deep-Sea Research I 49 (2002) 395-412 www. elsevier. com/locate/dsr Nutritional relations of deep-sea hydrothermal fields at the Mid-Atlantic Ridge: a stable isotope approach A. Colaçoa’*, F. Dehairsb, D. Desbruyèresc a IM A R, Guia Marine Laboratory, Estrada do Guincho, 2750 Cascais, Portugal b Department of Analytical Chemistry (ANCH), Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium cIFREMER Centre de Brest-DRO /EP-BP70, 29280 Plouzané, France Received 5 December 2000; received in revised form 6 April 2001; accepted 5 September 2001 Abstract Nutritional relations among invertebrates from the hydrothermal vent fields at the Mid Atlantic Ridge (MAR) were studied via the carbon and nitrogen stable isotope approach. A large number of specimens of different vent species from different MAR vent fields were analysed, providing a general picture of the community structure. The isotopic composition at each vent field presents the same general trend. There is an obvious dichotomy of the trophic structure, with the mussels being significantly depleted in 13C and shrimps being significantly enriched in 13C. MAR and Pacific vent fields present the same picture, despite a different species composition. Primary consumers are divided into main groups according to their c)13C signature: > — 1 5 (shrimps) and < — 2 0 % o (mussels). Vent predators are tightly linked to one or the other group, but a mixed diet cannot be excluded. Bathyal species are top predators, making incursions into the vent fields to profit from the large biomass. Taking into account the above associations, a descriptive trophic model was elaborated. At the base of the food chain the chemolithotrophic bacteria predominate. Four trophic levels were then distinguished: primary consumers, feeding only on bacteria; mixotrophs feeding on bacteria and small invertebrates; vent predators feeding only on small invertebrates; and finally top predators that are mainly constituted by deep-sea fauna. © 2 0 0 2 Elsevier Science Ltd. All rights reserved. Keywords: Hydrothermal vents; Food web; Stable isotope; Mid-Atlantic ridge 1. Introduction (Lonsdale, 1977) brought up questions regarding the food resources of those species. Rau and The discovery of dense invertebrate assembl­ Hedges (1979) and Rau (1981) were the first to ages clustered around hydrothermal vents along suggest that the carbon and nitrogen sources for Galapagos Rift at depths greater than 2500 m the hydrothermal vent fauna were of local origin, in contrast to deep-sea fauna deriving their food from sunken organic matter produced at the * Corresponding author. Present address: IMAR, Depart­ ocean’s surface. Later, Jannasch (1989) and Fisher ment of Oceanography and Fisheries, University of Azores, (1990) showed that the primary producers at the Cais de St. Cruz, 9900 Horta-Faial-Azores, Portugal. Tel.: + 351-292-292-988; fax: +351-292-292-659. base of the food chain in hydrothermal vent E-mail address: [email protected] (A. Colaço). environments are chemoautotrophic bacteria. 0967-0637/02/$ - see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S0967-0637(01)00060-7 396 A. Colaco et al. / Deep-Sea Research 1 49 (2002) 395-412 These bacteria might live symbiotically within host Several stable isotope studies have been per­ tissues or exist as free-living cells, attached to solid formed on MAR species in order to understand substrates or suspended in the water (Van Dover their feeding biology. These focused on the shrimp and Fry, 1994). Rimicaris exoculata (Gebruk et al., 2000; Polz Deep-sea hydrothermal communities are dis­ et al., 1998; Pond et al., 1997a, b, 2000; Rieley tributed in concentric rings around the vent et al., 1999; Van Dover et al., 1988) and mussels openings. Bacterial feeders (some alvinellids and (Robinson et al., 1999; Pond et al., 1998; Trask shrimps) dwell on chimney walls (Desbruyères and Van Dover, 1999). At Hanging Gardens, et al., 1983; Alayse-Danet et al., 1985; Casanova 21°N, East Pacific Rise (EPR) (Van Dover and et al., 1993), while organisms living in symbiotic Fry, 1989), and at the Galapagos (Rau, 1985; association with primary producers (provannid Fisher et al., 1994) nutritional relations among the gastropods, vestimentiferans, clams and mussels) different species has been studied. However, at the colonise the intermediate area of diffuse mild MAR vent fields no studies on nutritional venting (Belkin et al., 1986; Cavanaugh et al., relations among species from different groups 1981; Distel and Felbeck, 1987; Felbeck, 1981; have been carried out. This work presents the first Fisher et al., 1987; Stein et al., 1988), or, like comparative study of the trophic structures of the mussels at the Mid-Atlantic Ridge (MAR), different communities from the northern part of colonise chimney walls (Van Dover et al., 1996; the Mid-Atlantic Ridge using the stable isotope Desbruyères et al., 2001). Filter feeding organisms approach. These results are compared with similar (serpulids, actinarians and cirripeds) settle on work in the Pacific fields by Rau (1985), Fisher the external ring. At depths exceeding 2000 m, et al. (1994) and Van Dover and Fry (1989). the vent ecosystem is generally rather isolated Furthermore, our study of vent communities from from the typical deep-sea organisms, as they do depths ranging from 3500 to 800 m, aims to not penetrate the vent fields. At shallower depths, provide more information about relative contribu­ or where the vent medium is diluted through tion of chemosynthetically vs. photosynthetically subsurface plumbing, this general scheme varies. derived food substrate for heterotrophs. Finally, a Phase separation of the vent fluid then provides a descriptive trophic model for the MAR vent fields less toxic environment and allows non-endemic is proposed. deep-sea vent fauna such as mobile scavengers and carnivores to enter (Van Dover, 1995). Analysing for natural stable carbon and nitro­ 2. Material and methods gen isotopic composition is a useful approach to unravel trophic interactions in a well-known A total of 19 species were collected from seven and delimited ecosystem. The <513C isotopic sites of the northern part of the Mid-Atlantic signature is an indicator of the consumed food Ridge. Description of the biological and geologi­ substrate(s), since <513C remains relatively un­ cal characteristics of these vent fields is given in changed between successive trophic levels (<513C Table 1. becomes enriched by about l%o between each trophic level (Conway et al., 1994)). The <51SN 2.1. Sampling isotopic signature is a better indicator of the trophic level since successive trophic levels become Samples were collected in June 1994, August enriched in 15N by about 3.4%o per trophic level 1997 and July 1998 from the submersible “Nau­ (Minagawa and Wada, 1984). The symbiotic tile” (samples taken by grab; slurp gun), during the associations between vent fauna and chemoauto- DIVA 1 and 2, MARVEL, FLORES and PICO trophic bacteria lead to lower <51SN values, and cruises, and in July 1997 from the submersible lower or higher <513C values than other deep-sea “Alvin” during the MAR97 cruise. The domi­ fauna (see Kennicutt et al., 1992; Fisher, 1995 a nant taxa (mussels, shrimps, crabs, gastro­ review). pods, polychaetes) were selected for this study. Table 1 General community description of the Mid-Atlantic Ridge deep-sea hydrothermal vent fields with the main geological characteristics Site Depth Latitude T (max.) Type of field Chimney walls Diffuse venting External ring Scavengers and References (m) carmvourous Menez 800 37°51'N 281°C 4 sites. Two at Mirocaris Bathymodiolus Chaceon affinis Segonzacia mesa- Fouquet et al. Gwen the SW flank of a fortunata azoricus (host tlantica (1995) volcano, two at the endosymbionts) Chorocaris chacei Colaço et al. E flank of the (1998) volcano Lucky 1700 37°18'N 330°C The field consists Rimicaris exocula- Rimicaris exocula- Actinaria Segonzacia mesa­ Fouquet et al. Strike of several sites ta, Bathymodiolus ta, Bathymodiolus tlantica (1995) . Colaco Colaco et al. around a lava azoricus, Branchi- azoricus, Branchi- Chorocaris chacei Langmuir et al. lake. Concentra­ polinoe polinoe seepensis, Phymorhynchus sp. (1997) tion of sites at the seepensis, Miro­ Mirocaris fortuna­ Van Dover et al. NW, SE and NE caris fortunata, ta, Amathys lutzi (1996) Amathys lutzi / Deep-Sea Deep-Sea Research 1 49 (2002) 395-412 Rainbow 2300 36°14'N 360°C The hydrothermal Rimicaris Bathymodiolus n. Chaetopteridae Segonzacia mesa­ Fouquet et al. field is hosted by exoculata sp. (host endosym- polychaetes tlantica (1998) serpentinites and Mirocaris bionts) Chorocaris chacei Desbruyères et al. covers an area of fortunata Branchipolynoe Phymorhynchus (2001) 250 m by 60 m with Amathys lutzi seepensis sp. several chimneys with different de­ grees of activity Broken 3100 29°10'N 365°C The vent field lies Rimicaris Bathymodiolus n. Segonzacia M urtón et al. Spur at the intersection exoculata sp. (host endosym­ mesatlantica (1995) of two sets of cross bionts) cutting fissures. There are three large high tem­ perature venting mounds Chorocaris chacei Copley et al. (1997) TAG 3600 26°08'N 365°C Black smoker mas- Rimicaris Actinaria Segonzacia Rona et al. (1993) sive sulphides and exoculata Chaetopteridae mesatlantica Galkin and Mos- vent biota occur at polychaetes Phymorhynchus kalev (1990) the junction be­ sp. tween the floor and (continued on next page) io Table 1 ( continued) Site Depth Latitude T (max.) Type of field Chimney walls Diffuse venting External ring Scavengers and References (m) carnivourous east wall of the rift valley Snake 3400 23°22'N 350°C The vent field is Rimicaris Bathymodiolus pu- Actinaria Phymorhynchus sp. Karson and Brown Pit located on an exoculata teoserpentis (host Chorocaris chacei (1988) elongated dome, endosymbionts) Alvinocaris mar­ Fouquet et al. which is part of an Branchipolynoe kensis (1993) axial neovolcanic seepensis Segonzac (1992) ridge in the rift X valley hydrother­ O mal area, and o -CiS' consists of three O mounds aligned Cb Si east west «bb Logatchev 3000 14°45'N 353°C The vent area has a Rimicaris Bathymodiolus pu­ Segonzacia mesa- Gebruk et al.
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