Vol. 596: 1–12, 2018 MARINE ECOLOGY PROGRESS SERIES Published May 28 https://doi.org/10.3354/meps12617 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Trophic structure and chemosynthesis contributions to heterotrophic fauna inhabiting an abyssal whale carcass Joan M. Alfaro-Lucas1,3,*, Maurício Shimabukuro1, Isabella V. Ogata1, Yoshihiro Fujiwara2, Paulo Y. G. Sumida1 1Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, CEP 05508-120, São Paulo-SP, Brazil 2Japan Agency for Marine-Earth Science and Technology - JAMSTEC, 2-15 Natsushimacho, Yokosuka 237-0061, Japan 3Present address: Institut Français de Recherche pour l’Exploitation de la Mer (IFREMER), Centre de Bretagne, REM/EEP, F-29280, Plouzané, France ABSTRACT: The trophic structure and role of chemo - synthesis remain unexplored in deep-sea whale-fall communities in areas other than the California margin. This gap limits the understanding of these communi- ties and their ecological relationships with other chemosynthetic ecosystems, such as vents and seeps. Here, we studied 3 different whale skeleton micro- habitats with hypothesized high, intermediate and low reducing conditions as well as the sediments sur- rounding an abyssal whale fall (4204 m depth, SW At- lantic Ocean). We analyzed trophic structures (δ13C and δ15N) and the contribution of chemosynthetically derived carbon to heterotrophic species. The high and intermediate reducing microhabitats harbored food webs dominated by consumers of chemosynthetic Whale carcasses provide the deep sea with a mosaic of microhabitats that support faunal assemblages with differ- production, similar to those of diffusive areas of hy- ent trophic structures and chemosynthesis reliance levels. drothermal vents and seeps. Both the low reducing microhabitat and the sediments harbored food webs Photo: Yoshihiro Fujiwara with greater trophic complexity, dominated by higher consumers mainly relying on whale and/or photosyn- KEY WORDS: Deep sea · Whale fall · Trophic thesis-derived organic matter, a type of food web structure · Chemosynthesis · Osedax commonly reported in small whale, wood and kelp falls. The main whale-fall ecosystem engineer, the bone- eating worm Osedax, appeared to produce unique food web effects not observed in other chemosynthetic habitats. We conclude that whale falls provide the deep sea with a mosaic of microhabitats that supports INTRODUCTION assemblages with different chemo synthesis reliance levels and trophic structures, similar to those found at In deep-sea environments such as hydrothermal vents and seeps. Such a mosaic allows species-rich vents and cold seeps, where reduced compounds communities with numerous trophic levels to develop are abundant, autochthonous microbial chemosyn- in a very small area of the food-limited deep sea. thetic production supports abundant endemic fau- © The authors 2018. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Mar Ecol Prog Ser 596: 1–12, 2018 nal communities (Van Dover et al. 2002). At vents very likely to face, anthropogenic impacts, such as and seeps, unlike most of the vast, food-limited fisheries and deep-sea mining (Roman et al. 2014, deep sea, photosynthetically derived food sources Levin et al. 2016). Therefore, understanding their only supplement faunal diets. These food sources ecological interactions is crucial for their effective have decreasing importance with increasing depth, protection (Roman et al. 2014, Levin et al. 2016). and the intensity of reducing compound fluxes The trophic ecology of whale falls has received little within habitats affects their use (Levin & Michener attention beyond the deep California margin (Baco 2002, Levesque et al. 2006, Decker & Olu 2012, & Smith 2003, Smith & Baco 2003). This gap may Bernardino et al. 2012). Among chemo synthetic bias our understanding of these habitats and their ecosystems, those derived from cetacean carcasses, ecological links with vents, seeps and other organic the largest organic parcels exported from surface falls from other basins. Previous studies report that waters, may create conditions that support chemo - large whale skeletons in the sulfophilic stage create synthesis for years and even decades (Smith & Baco communities that are similar to those of vents with 3 2003, Smith 2006, Smith et al. 2015). to 5 trophic levels (Baco & Smith 2003, Smith & Baco Although ‘whale falls’ are thought to be common 2003). In the Pacific, the low δ15N values in the along cetacean migratory routes, they were only dis- fauna indicate local origins for much of the organic covered ca. 30 yr ago and have been much less stud- nitrogen (Smith & Baco 2003). In the latter study, ied than vents and seeps, especially in basins outside chemosymbiotic bi valves (Vesicomya gigas and Idas the Northeast Pacific Ocean (Smith et al. 1989, Smith washingtonia) dominated macrofaunal abundance et al. 2015). Carcasses greatly impact small areas and constituted 58% of the molluscan biomass. of the seafloor (~100 m2), attracting opportunistic and Species that depend on chemosynthetic production specialized fauna and creating unique island-like accounted for up to 42% of the community biomass, habitats considered to be hot spots of biodiversity and with just a few species relying on the whale organic sources of evolutionary novelty (Smith et al. 2015). material (Smith & Baco 2003). In contrast, small The organic matter in enriched sediments around juvenile whale skeletons harbored communities carcasses and within the lipid-rich skeletons is anaer- mainly dependent on whale organic matter (Smith obically degraded by sulfate-reducing bacteria and & Baco 2003). archaea, which generate fluxes of reduced com- Here, we present a detailed stable isotope analysis pounds as by-products of their metabolism (Deming (δ13C and δ15N) of an abyssal whale-fall community et al. 1997, Smith & Baco 2003, Goffredi et al. 2008, (4204 m depth, off Brazil, SW Atlantic Ocean) at the Treude et al. 2009). The free-living chemosynthetic sulfophilic degradation stage in order to shed light on sulfide-oxidizing bacteria and chemosymbiotic inver- the reliance of heterotrophic fauna from 3 skeleton tebrates that exploit these fluxes also occur in vents, microhabitats and sediments on microbial chemosyn- seeps and other organic falls (Smith et al. 1989, Feld- thetic production. The carcass in this study was a man et al. 1998, Fujiwara et al. 2007, Lundsten et al. juvenile whale, and previous studies suggested that 2010a,b, Smith et al. 2015). Heterotrophic fauna also chemosynthesis may be important, especially in colonize whale falls during the ‘sulfophilic stage’, some parts of the skeleton (Sumida et al. 2016, creating extremely species-rich communities struc- Alfaro-Lucas et al. 2017). Based on visual observa- tured in several trophic levels (from 3 to 5) (Baco & tions and colonizing fauna, we hypothesized that a Smith 2003, Smith & Baco 2003). Bone fauna assem- gradient in the sulfide concentration would define blages are considered one of the most species-rich availability of chemosynthetic production across the hard-substrate habitats in the deep sea (Baco & skeleton microhabitats, in addition to the fauna from Smith 2003). sediments. As reported for vents and seeps, we Whale falls have been hypothesized to act as step- expected a decrease in faunal reliance on microbial ping stones for faunal evolution and dispersal chemosynthetic production from the hypothesized among distant nascent seeps and vents (Smith et al. high to low reducing microhabitats. Specifically, in 1989, Smith et al. 2017, Kiel 2017). Some chemo- this study, we address the following questions: (1) is symbiotic seep/vent fauna likely originated in shal- free-living microbial chemosynthetic primary pro- low waters and potentially used organic falls to duction an important food source for heterotrophic colonize the deep sea (Distel et al. 2000, Jones et species at whale-fall microhabitats; and (2) how does al. 2006, Miyazaki et al. 2010, Lorion et al. 2013, trophic structure vary among different whale-fall Thubaut et al. 2013). Deep-sea chemosynthetic microhabitats and across the entire whale-fall habitats, including whale falls, already face, or are community? Alfaro-Lucas et al.: Trophic ecology of an abyssal whale fall 3 MATERIALS AND METHODS by decreasing sulfide concentrations by enhancing oxygen penetration to the inner-bone matrices (Al- Study site, sample processing and faro-Lucas et al. 2017) (Fig. 1C). Vertebrae colonized whale-fall microhabitats by Osedax sp. were associated with different infaunal assemblages from those of non-colonized vertebrae We studied a partial natural whale carcass discov- (Alfaro-Lucas et al. 2017). ered by the submersible HOV (human occupied We analyzed carbon and nitrogen stable isotopes of vehicle) ‘Shinkai 6500’ during the Brazilian-Japan- infaunal species accounting for 97.5, 51.1 and 98.3% ese Iatá-Piúna expedition, a part of the around-the- of the total faunal abundance of the inferior parts of world Quelle 2013 project (Japanese Agency for the vertebrae not colonized by Osedax sp., the supe- Marine-Earth Science and Technology). The carcass rior parts of the vertebra not colonized by Osedax sp. was discovered at 4204 m depth at the base of São and the vertebra colonized by Osedax sp., respectively