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Cold Seep and Oxygen Minimum Zone Associated Sources of Margin Progress in Oceanography 96 (2012) 77-92 PROGRESS IN Contents lists available at SciVerse ScienceDirect OCEANOGRAPHY Progress in Oceanography ELSEVIER journal homepage: www.elsevier.com/locate/pocean Cold seep and oxygen minimum zone associated sources of margin heterogeneity affect benthic assemblages, diversity and nutrition at the Cascadian margin (NE Pacific Ocean) Katja Guilinia *, Lisa A. Levin b, Ann Vanreusela aBiology Department, Marine Biology Section, Ghent University, Krijgslaan 281/Sterre S8, 9000 Gent, Belgium blntegrative Oceanography Division, Scripps Institution of Oceanography, 9500 Gilman Drive, La Jolla, CA 92093-0218, USA ARTICLE INFO ABSTRACT Article history: Hydrate Ridge (HR), located on the northeastern Pacific margin off Oregon, is characterized by the Received 3 June 2011 presence of outcropping hydrates and active methane seepage. Additionally, permanent low oxygen con­ Received in revised form 19 October 2011 ditions overlay the benthic realm. This study evaluated the relative influence of both seepage and oxygen Accepted 19 October 2011 minima as sources of habitat heterogeneity and potential stress-inducing features on the bathyal Available online 28 October 2011 metazoan benthos (primarily nematodes) at three different seep and non-seep HR locations, exposed to decreasing bottom-water oxygen concentrations with increasing water depth. The nematode seep communities at HR exhibited low diversity with dominance of only one or two genera (D aptonem aa n d Metadesmolaimus), elevated average individual biomass and 513C evidence for strong dependance on chemosynthesis-derived carbon, resembling deep-sea seeps worldwide. Although the HR seep habitats harbored a distinct nematode community like in other known seep communities, they differed from deep-sea seeps in well-oxygenated waters based on that they shared the dominant genera with the surrounding non-seep sediments overlain by oxygen-deficient bottom water. The homogenizing effect of the oxygen minimum zone on the seep nematode assemblages and surrounding sediments was constant with increasing water depth and concomitant greater oxygen-deficiency, resulting in a loss of habitat heterogeneity. © 2011 Elsevier Ltd. All rights reserved. 1. Introduction or to tolerate these physico-chemical conditions (Levin et al., 2003). Several megafaunal seep-specialists are adapted to survive Cold-seeps are geochemical features, found worldwide on in these reduced habitats by carrying endosymbionts and/or by tectonically active and passive continental margins (Sibuet and having sulfide-binding or -oxidizing capabilities (e.g. siboglinid Olu, 1998). They are formed where subsurface interstitial fluids, polychaetes, cladorhizid sponges, bathymodiolin mussels, and ves- rich in reduced chemicals from biogenic or thermogenic origin icomyid, lucinid, solemyid, and thyasirid clams). This successful (mostly methane and sulfide), are released at the sediment surface exploitation of chemosynthetic derived energy is often evidenced as a result of a variety of processes such as tectonic activity, differ­ by highly increased levels of density and biomass of these few ses­ ential compaction of organic-rich sediments, gas hydrate dissocia­ sile or sedentary taxa. Their presence also adds structural complex­ tion and subsurface salt migration (Cordes et al., 2010). Therefore ity to the seep sediments which increases habitat heterogeneity cold-seep ecosystems appear in a variety of geomorphic and bio­ and supports many smaller fauna living associated with them logical forms on the seafloor and create a diverse suite of habitats (Levin, 2005). Overall, the aggregations of symbiotic foundation for both endemic seep organisms and more opportunistic colonists species and associated taxa at cold seeps are considered as excep­ (Levin et al., 2003; Cordes et al., 2010). Together with water depth tions on the general trends of high local metazoan diversity and and age of the geologic features, habitat heterogeneity created by evenness, and low metazoan density and biomass that are found the intensity and volume of fluid flow, and methane and sulfide in most of the deep sea (Levin, 2005). concentrations and fluxes, determines species richness and density In addition to cold seeps, oxygen minimum layers present at of the inhabiting fauna (Cordes et al., 2010). While chemo- intermediate water depths (ca. 100-1000 m), contribute to habitat autotrophic bacteria that thrive on hydrogen sulfide form mats at heterogeneity along continental margins worldwide. This hydro- sites of active seepage, relatively few taxa have the ability to use graphic feature persists over geological time scales and occurs where upwelling leads to high surface productivity, oxygen- depleted source waters are present, and water stability is imposed * Corresponding author. Tel: +32 9 264 85 31; fax: +32 9 264 85 98. by a strong pycnocline that induces accumulation of settling E-mail address: [email protected] (K. Guilini). 0079-6611 /$ - see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.pocean.2011.10.003 78 K. Guilini et al./Progress in Oceanography 96 (2012) 77-92 organic detritus (Levin, 2003; Gooday et al„ 2010). Typically, 02 to the autochthonous chemosynthetic-derived carbon input. When concentrations drop below 0.5 ml I-1. As reduced bottom-water seep-associated fauna depend largely on methane-derived carbon, oxygen concentrations enhance preservation of organic matter either by carrying methane- or sulfide-oxidizing endosymbionts from the surface (Cowie and Hedges, 1992), increased concentra­ or by feeding direct- or indirectly on chemoautotrophic methane tions of labile organic matter and phytodetrital food are found in oxidizers (aerobic bacteria and anaerobic Achaea with associated sediments where the OMZ intersects with the seafloor (often sulfate-reducing bacteria), their tissues will reflect the thermo- or >3%, up to 20.5% organic carbon; Levin, 2003; Gooday et al., biogenic 513C methane signal (513C o f-5 0 %o to -1 1 0 %a, e.g. Whiti- 2010). Strong zonation of benthic communities occurs in conjunc­ car et al., 1986). However, as most seep-associated fauna probably tion with varying bottom- and pore-water oxygen concentrations use multiple food sources, the interpretation of isotopic signatures and associated gradient in organic-matter input that change with is complicated. To yield at least upper and lower estimates of meth­ water depth (e.g. Levin et al., 1991, 2000, 2003, 2009; Wishner ane-derived carbon in organisms, two-end member linear mixing et al., 1990,1995; Levin and Gage, 1998; Neira et al., 2001). Macro- models with single isotope measures can be used (e.g. Levin and and megafauna communities inhabiting OMZ sediments are Michener, 2002; MacAvoyet al., 2002; C arlieret al., 2010; Demopo- generally distinct from the well-oxygenated surrounding margins ulos et al., 2010; Thurber et al., 2010). in having severely reduced densities, biomass and diversity (Wish­ Our study evaluates the relative influence of both seepage and ner et al., 1990; Levin and Gage, 1998; Smith et al., 2000; Levin oxygen minima as sources of habitat heterogeneity and potential et al., 2001; reviewed in Levin, 2003; Sellanes et al., 2010). stress-inducing features on the bathyal benthic community. We Although total meiobenthic biomass and abundance often follow focus hereby on the nematode community composition, diversity, the same pattern as mega- and macrofauna, in general both proto­ morphometry, biomass, density and nutrition and compare the lat­ zoan and metazoan meiofauna are less affected by low oxygen con­ ter with macrofauna data. Therefore three habitat types (clam beds, ditions (Levin et al., 1991; Bernhard et al., 2000; Cook et al., 2000; microbial mats and nearby non-seep margin sediments) were stud­ Gooday et al., 2000, 2009; Neira et al., 2001; Veit-Köhler et al., ied at three HR locations categorized according to increasing depth 2009). Among the metazoan meiofauna, deep-sea nematodes seem and decreasing bottom-water oxygen concentrations (500-600 m, very tolerant to low oxygen concentrations (Levin et al., 1991; 0.7 02 m ir1; 700-800 m, 0.2-0.3 02m ir1; 800-900 m, ^0.2 Moodley et al., 1997; Cook et al., 2000) and typically occur at high­ 02 ml I-1; Levin et al., 2010). This study sought to answer the fol­ er densities where 02 concentrations are lowest in OMZs compared lowing questions: (1) do the seepage habitats at HR harbor a dis­ to other taxa that are unable to tolerate low oxygen concentrations tinct nematode community compared to the non-seep margin such as harpacticoid copepods and nauplii (Hicks and Coull, 1983; sites and other known seepage sites worldwide? (2) Does the in­ Murrell and Fleeger, 1989; Levin et al., 1991; Giere, 2009; Neira creased habitat complexity created by clam beds affect the nema­ et al., 2001; Levin et al., 2009). If their elongated body-length tode community distribution in the sediment, resulting in an and therefore higher surface area-to-volume ratio could be an increase in biodiversity compared to the microbial mats? (3) Does adaptation to low oxygen partial pressure as suggested before the OMZ homogenize the nem atode com position in such a way that (Jensen, 1986, 1987; Schiemer et al., 1990; Soetaert et al., 2002), seep-related heterogeneity is more pronounced at more oxygen­ morphometric changes might occur along an oxygen-deficiency ated water depths? (4) Do water depth and co-varying 02 bottom gradient. water concentrations create
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