Chemosynthetic and photosynthetic trophic support from cold seeps in Arctic benthic communities

Abstract

Benthic communities below the photic zone are largely reliant on the export of surface-water primary production and the flux of partially degraded organic matter to the seabed, i.e. pelagic−benthic coupling. Over the past decades, however, the role of chemosynthetically produced carbon in food webs has been recognized in various habitats. Cold seeps are now known to be widespread across circumpolar Arctic shelves where natural release of hydrocarbons occurs at the seabed. Here, we investigated to what extent chemosynthesis-based carbon (CBC) enters the food web in a high latitude shelf-system. Specifically, we estimated the contributions of chemosynthesis-based carbon to primarily benthic invertebrate taxa from seeps at both shallow and deeper shelves and comparative non-seep areas in the Svalbard-Barents Sea region using bulk stable isotope-analysis of carbon and nitrogen. Our results show low δ13C values (-51.3 to -32.7 ‰) in chemosymbiotic siboglinids and several species of benthic, higher-trophic level, invertebrates (mainly polychaetes and echinoderms; -35.0 to -26.1‰) collected at cold seeps, consistent with assimilation of chemosynthesis-based carbon into the Arctic benthic food web. Using a two-component mixing equation, we demonstrate that certain species could derive more than 50% of their carbon from chemosynthesis-based carbon. These findings show that autochthonous chemosynthetic energy sources can contribute to supporting distinct groups of ‘background’ benthic taxa at these Arctic seep-habitats beyond microbial associations and chemosymbiotic species. Furthermore, we found a higher degree of chemosynthesis-based carbon in benthos at the deeper Barents Sea shelf seeps (>330 m) compared to seeps at the Western Svalbard shelf (<150 m water-depth), and we suggest this result reflects the differences in depth range, surface production and pelagic-benthic coupling. We detected large intra-species variations in carbon signatures within and across geographical locations and, combined with isotopic niche-analysis, our results show that certain taxa that inhabits seeps, have wider trophic niches in comparison to taxa inhabiting non-seeps. The increasing number of discovered natural seeps in the Arctic suggests that chemosynthetic production from seeps could play a more critical role in Arctic trophic structure than previously thought. Seep-derived carbon should, hence, be accounted for as an additional carbon source and included in food-web and energy-flow models in future work.

Diversity, habitat endemicity and trophic ecology of the fauna of Loki’s Castle vent field on the Arctic Mid-Ocean Ridge

“…sPOM from areas without chemosynthetic influence in the Arctic region between 2000 and 2800 m depth showed δ 13 C values from − 21.35 to − 23.5‰ and δ 15 N from 5 to 8.62‰ 45 – 47 . pPOM from the Barents Sea and Norwegian Sea showed δ 13 C values from − 22 to − 27.3‰ and δ 15 N from 4 to 5.4‰ 48 – 50 .…”

The phylogeography and ecology of Oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic

“…Note that vents and seeps do not exclusively host specialist fauna, however, with the exception of shallow water locations, at least some specialists tend to be present at seeps, particularly chemosymbiotic species [ 13 , 14 ]. Other than the few shallow water ones [ 42 , 72 , 73 ], and thereby for the majority of Arctic seep sites studied, the lack of specialist fauna represents a deviation from trends at seeps in other parts of the world. Even on geological timescales, a paucity of seep specialist fauna has been observed at Arctic seeps [ 71 , [74] , [75] , [76] , [77] ].…”

Opportunistic consumption of marine pelagic, terrestrial, and chemosynthetic organic matter by macrofauna on the Arctic shelf: a stable isotope approach

“…and carnivores nephtyid polychaetes were the only taxa in their respective feeding group. In the section “Seep-associated fauna” we used additional data on Oligobrachia and δ 13 C values of methane from North Atlantic and Arctic seeps for comparison on a larger scale ( Gebruk et al, 2003 ; Decker & Olu, 2012 ; Lee et al, 2019a ; Åström, Bluhm & Rasmussen, 2022 ; Kravchishina et al, 2021 ). Several taxa were not assigned to a particular feeding habit: the gastropod Frigidoalvania sp., the bivalve Montacuta spitzbergensis , and thyasirid bivalves.…”

“…The exact quality and quantity of organic matter reaching the seafloor might depend on many factors and processes, both biotic and abiotic, including depth, water mass properties and currents, overall primary production, terrestrial inputs, grazing by zooplankton, and microbial degradation of sinking organic matter ( Iken, Bluhm & Gradinger, 2005 ; Roy et al, 2015 ; Stasko et al, 2018 ). Locally, benthic primary production is important for benthic food webs, including microphytobenthos and macroalgae in the coastal habitats ( Woelfel et al, 2010 , Renaud et al, 2015 ) and chemosynthetic production in the areas with seabed emission of reduced compounds, such as methane and hydrogen sulfide, also known as “methane seeps” and “hydrothermal vents” ( Sweetman et al, 2013 ; Åström, Bluhm & Rasmussen, 2022 ). Consequently, regional and local ecosystem features might drive differences in organic matter availability and consumption by macrofauna.…”

“…In the areas of methane seepage, distinct microbial communities in the sediments are formed that include chemosynthetic microorganisms capable of utilizing either methane (methanotrophs) or hydrogen sulfide (thiotrophs) as an energy source ( Åström et al, 2020 ). Carbon in the biomass of sulfur-oxidizing bacteria and methanotrophic microorganisms is usually characterized by very low δ 13 C values (<−30‰) ( Levin & Michener, 2002 ; Decker & Olu, 2012 ; Åström, Bluhm & Rasmussen, 2022 ).…”