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Biodiversity and Trophic Ecology of Hydrothermal Vent Fauna Associated with Tubeworm Assemblages on the Juan De Fuca Ridge

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Biodiversity and Trophic Ecology of Hydrothermal Vent Fauna Associated with Tubeworm Assemblages on the Juan De Fuca Ridge Biogeosciences, 15, 2629–2647, 2018 https://doi.org/10.5194/bg-15-2629-2018 © Author(s) 2018. This work is distributed under the Creative Commons Attribution 4.0 License. Biodiversity and trophic ecology of hydrothermal vent fauna associated with tubeworm assemblages on the Juan de Fuca Ridge Yann Lelièvre1,2, Jozée Sarrazin1, Julien Marticorena1, Gauthier Schaal3, Thomas Day1, Pierre Legendre2, Stéphane Hourdez4,5, and Marjolaine Matabos1 1Ifremer, Centre de Bretagne, REM/EEP, Laboratoire Environnement Profond, 29280 Plouzané, France 2Département de sciences biologiques, Université de Montréal, C.P. 6128, succursale Centre-ville, Montréal, Québec, H3C 3J7, Canada 3Laboratoire des Sciences de l’Environnement Marin (LEMAR), UMR 6539 9 CNRS/UBO/IRD/Ifremer, BP 70, 29280, Plouzané, France 4Sorbonne Université, UMR7144, Station Biologique de Roscoff, 29680 Roscoff, France 5CNRS, UMR7144, Station Biologique de Roscoff, 29680 Roscoff, France Correspondence: Yann Lelièvre ([email protected]) Received: 3 October 2017 – Discussion started: 12 October 2017 Revised: 29 March 2018 – Accepted: 7 April 2018 – Published: 4 May 2018 Abstract. Hydrothermal vent sites along the Juan de Fuca community structuring. Vent food webs did not appear to be Ridge in the north-east Pacific host dense populations of organised through predator–prey relationships. For example, Ridgeia piscesae tubeworms that promote habitat hetero- although trophic structure complexity increased with ecolog- geneity and local diversity. A detailed description of the ical successional stages, showing a higher number of preda- biodiversity and community structure is needed to help un- tors in the last stages, the food web structure itself did not derstand the ecological processes that underlie the distribu- change across assemblages. We suggest that environmental tion and dynamics of deep-sea vent communities. Here, we gradients provided by the biogenic structure of tubeworm assessed the composition, abundance, diversity and trophic bushes generate a multitude of ecological niches and con- structure of six tubeworm samples, corresponding to differ- tribute to the partitioning of nutritional resources, releasing ent successional stages, collected on the Grotto hydrother- communities from competition pressure for resources and mal edifice (Main Endeavour Field, Juan de Fuca Ridge) at thus allowing species to coexist. 2196 m depth. Including R. piscesae, a total of 36 macro- faunal taxa were identified to the species level. Although polychaetes made up the most diverse taxon, faunal densi- ties were dominated by gastropods. Most tubeworm aggre- 1 Introduction gations were numerically dominated by the gastropods Lep- etodrilus fucensis and Depressigyra globulus and polychaete Deep-sea hydrothermal vents occur along mid-ocean ridges Amphisamytha carldarei. The highest diversities were found and back-arc spreading centres, which are characterised in tubeworm aggregations characterised by the longest tubes by strong volcanic and tectonic activity. The resulting hy- (18.5 ± 3.3 cm). The high biomass of grazers and high re- drothermal fluid fosters dense communities of highly spe- source partitioning at a small scale illustrates the importance cialised fauna that colonise the steep physical and chem- of the diversity of free-living microbial communities in the ical gradients created by the mixing of hot vent fluids maintenance of food webs. Although symbiont-bearing in- with cold seawater. These communities are distributed ac- vertebrates R. piscesae represented a large part of the total cording to species’ physiological tolerance (Childress and biomass, the low number of specialised predators on this Fisher, 1992; Luther et al., 2001), resource availability (De potential food source suggests that its primary role lies in Busserolles et al., 2009; Levesque et al., 2003) and bi- otic interactions (Lenihan et al., 2008; Micheli et al., 2002; Published by Copernicus Publications on behalf of the European Geosciences Union. 2630 Y. Lelièvre et al.: Biodiversity and trophic ecology of hydrothermal vent fauna Mullineaux et al., 2000, 2003). Although the fauna are highly fusion of food. Stable isotopes analysis is an important and dissimilar between oceanic basins (Bachraty et al., 2009; efficient tool in studying trophic ecology and offers many ad- Moalic et al., 2011), hydrothermal communities throughout vantages over traditional methods (behavioural observations, the world share some ecological similarities including a food stomach content analyses), providing the time-integrated web based on chemosynthesis (Childress and Fisher, 1992), overview of an animal’s diet over a long timescale. Nev- low species diversity compared with adjacent deep-sea and ertheless, the physiology of marine invertebrates is poorly coastal benthic communities (Van Dover and Trask, 2000; documented, resulting in a lack of precision on the turnover Tunnicliffe, 1991), high levels of endemism (Ramirez-Llodra rate of an organism’s tissue and therefore, the rate at which a et al., 2007), and elevated biomass associated with the pres- consumer integrates the isotopic signal, leading to an uncer- ence of large invertebrate species. tainty about trophic-step fractionation (isotopic enrichment The high spatial heterogeneity of environmental condi- between preys and predators). Moreover, although trophic tions in vent ecosystems is amplified by stochastic and pe- inferences using stable isotopes require the characterisation riodic temporal variation in hydrothermal activity, influenc- of basal sources, this remains difficult in the hydrothermal ing the composition (Sarrazin et al., 1999), structure (Mar- environment due to technological sampling constraints. De- cus et al., 2009; Sarrazin et al., 1997; Tsurumi and Tunni- spite this, the emergence of isotopic methods has opened new cliffe, 2001) and dynamics (Lelièvre et al., 2017; Nedoncelle perspectives in the understanding of food web functioning et al., 2013, 2015; Sarrazin et al., 2014) of faunal communi- and the organisation of species diversity within these ecosys- ties. In addition, the complexity of vent habitats is increased tems around the globe (Bergquist et al., 2007; De Busserolles by engineer species, whose presence strongly contributes to et al., 2009; Van Dover, 2002; Erickson et al., 2009; Gau- the modification of the physical (temperature, hydrodynam- dron et al., 2012; Levesque et al., 2006; Levin et al., 2009; ics processes) and chemical (hydrogen sulfide, methane, oxy- Limén et al., 2007; Portail et al., 2016; Soto, 2009; Sweet- gen, metals and other reduced chemicals) properties of the man et al., 2013). The carbon isotope composition (δ13C) is environment either by creating three-dimensional biogenic an indicator of the food assimilated and remains relatively structures (autogenic species) or through their biological ac- constant during trophic transfers (±1 ‰). The kinetics of en- tivity (allogeneic species) (Jones et al., 1994, 1997). Habitat zymes involved in the biosynthetic pathways of autotrophic provisioning and modification by engineer species increases organisms influence the carbon isotope ratio (13C = 12C), al- the number of potential ecological niches and, consequently, lowing the discrimination between the sources fuelling the influences species distribution and contributes to an increase community (Conway et al., 1994; Van Dover and Fry, 1989). in local diversity (Dreyer et al., 2005; Govenar and Fisher, Nitrogen isotope composition (δ15N) provides information 2007; Urcuyo et al., 2003). Engineer species promote local on trophic levels and becomes enriched in heavy isotopes diversity through various ecological mechanisms (Bergquist at an average rate of ±3.4 ‰ at each trophic level (Mich- et al., 2003), providing a secondary substratum for colonisa- ener and Lajtha, 2008). At the community scale, δ13C and tion, a refuge from predation and unfavourable abiotic con- δ15N signatures of all species in the ecosystem are used to re- ditions, and important food sources that enhance the devel- trace carbon and nitrogen fluxes along the trophic chain and, opment of macro- and meiofaunal communities (Dreyer et therefore, to reconstitute the food web (Levin and Michener, al., 2005; Galkin and Goroslavskaya, 2010; Gollner et al., 2002). Despite the relatively low diversity of vent commu- 2006; Govenar et al., 2005, 2002; Govenar and Fisher, 2007; nities, ample evidence suggests that hydrothermal food web Turnipseed et al., 2003; Zekely et al., 2006). structure is complex (Bergquist et al., 2007; Portail et al., Hydrothermal vent food webs are mainly based on lo- 2016), including many trophic guilds (Bergquist et al., 2007; cal microbial chemosynthesis (Childress and Fisher, 1992), De Busserolles et al., 2009) and multiple sources of primary performed by free-living or/and symbiotic chemoautotrophic production (Van Dover and Fry, 1994). The carbon signa- microorganisms that utilise the chemical energy released by ture (δ13C) of primary producers differs according to their the oxidation of reduced chemicals species (H2,H2S, CH4) carbon fixation pathways that differentially fractionate inor- present in the hydrothermal fluids (Childress and Fisher, ganic carbon sources. Despite the fact that the nitrogen sig- C 15 1992). Several electron donors (e.g. H2,H2S, CH4, NH4 ) nature (δ N) does not discriminate between primary produc- − 2− ers, the variability of δ15N signatures can be associated with and electron acceptors (e.g. O2, NO3 , SO4 ) can be used
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