The dynamic influence of methane seepage on macrofauna inhabiting authigenic carbonates

Abstract

Methane seeps are highly productive deep-sea ecosystems reliant on chemosynthetic primary production. They are increasingly affected by direct human activities that threaten key ecosystem services. Methane seepage often generates precipitation of authigenic carbonate rocks, which host diverse microbes, and a dynamic invertebrate community. By providing hard substrate, even after seepage ceases, these rocks may promote a long-lasting ecological interaction between seep and background communities. We analyzed community composition, density, and trophic structure of invertebrates on authigenic carbonates at Mound 12, a seep on the Pacific margin of Costa Rica, using one mensurative and two manipulative experiments. We asked whether carbonate macrofaunal communities are able to survive, adapt, and recover from changes in environmental factors (i.e., seepage activity, chemosynthetic production, and food availability), and we hypothesized a key role for seepage activity in defining these communities and responses. Communities on in situ carbonates under different seepage activities showed declining density with increasing distance from the seep and a shift in composition from gastropod dominance in areas of active seepage to more annelids and peracarid crustaceans that are less dependent on chemosynthetic production under lesser seepage. Response to changing environmental context was evident from altered community composition following (1) a natural decline in seepage over successive years, (2) transplanting of carbonates to different seepage conditions for 17 months, and (3) defaunated carbonate deployments under different seepage regimes over 7.4 yr. Seep faunas on transplants to lesser seepage emerge and recover faster than transition fauna (characterized by native seep and background faunas, respectively) and are able to persist by adapting their diets or by retaining their symbiotic bacteria. The macrofaunal community colonizing defaunated carbonates deployed for 7.4 yr developed communities with a similar successional stage as in situ rocks, although trophic structure was not fully recovered. Thus, macrofaunal successional dynamics are affected by habitat complexity and the availability of microbial chemosynthetic productivity. This multi-experiment study highlights the interaction between biotic and abiotic factors at methane seeps at different time scales along a spatial gradient connecting seep and surrounding deep-sea communities and offers insight on the resilience of deep-sea macrofaunal communities.

Does substrate matter in the deep sea? A comparison of bone, wood, and carbonate rock colonizers

“…When seepage activity ceases, these rocks persist and provide hard substrate for background species that colonize them, sustaining such communities for decades [ 10 ]. Moreover, seepage activity is dynamic, and declines in fluid flux over time and space (see [ 11 – 13 ]) can create a transition zone surrounding the active area, where bacterial biomass and seep species diminish [ 14 ] but the rocks formed during high seepage activity levels persist, providing hard substrate for background species [ 10 ]. Although transition zones visually appear inactive, chemosynthetic microbial activity may also still persist within the carbonates [ 12 , 15 , 16 ], and some seep species can still be found on these rocks (see [ 11 , 13 ]).…”

“…Moreover, seepage activity is dynamic, and declines in fluid flux over time and space (see [ 11 – 13 ]) can create a transition zone surrounding the active area, where bacterial biomass and seep species diminish [ 14 ] but the rocks formed during high seepage activity levels persist, providing hard substrate for background species [ 10 ]. Although transition zones visually appear inactive, chemosynthetic microbial activity may also still persist within the carbonates [ 12 , 15 , 16 ], and some seep species can still be found on these rocks (see [ 11 , 13 ]). Thus, transition zones can be highly diverse, with both seep and background species coexisting, enhancing habitat and trophic complexity [ 13 , 17 ].…”

“…Although transition zones visually appear inactive, chemosynthetic microbial activity may also still persist within the carbonates [ 12 , 15 , 16 ], and some seep species can still be found on these rocks (see [ 11 , 13 ]). Thus, transition zones can be highly diverse, with both seep and background species coexisting, enhancing habitat and trophic complexity [ 13 , 17 ]. See S1 Table for a summary of terminology and definitions.…”

“…Colonization experiments with carbonate rocks and organic parcels have shown that chemosynthesis-based communities are able to rapidly colonize hard substrates on continental margins. Carbonate rocks deployed at methane seeps for 10.5 months [ 21 ] and 7.4 years [ 13 ] are colonized by seep species even at transition sites (i.e., a site within the transition zone), these species coexist with the background fauna. At hydrothermal vents, increasing hydrothermal activity supports higher functional diversity of colonizers on rocks deployed for 2 years close to active sites, although there was faunal overlap between rocks at active site and inactive sites and export of chemosynthetic production to colonizers at inactive sites [ 22 ].…”

“…We hypothesized the trophic contribution (i.e., nutrition) to macrofauna from organic-rich bones and wood should dominate at transition sites with lower seepage, and the macrofaunal community should differ among bones, woods, and carbonate substrates, based on previous studies that showed that geochemical processes and species composition at species level differ among CBEs (see [ 2 ]), with organic-fall specialists colonizing the organic substrates. At active sites, seepage activity should be a strong determinant of the macrofaunal community composition and its trophic structure across different types of hard substrate [see 13 ]. Seepage and the abundant food it creates should override the relative importance of the substrate itself and its nutritional influence, with macrofaunal communities on carbonate rock (methane seeps), bone (animal falls) and wood (wood falls) being more similar under active seepage, and less similar at transition sites where substrate would matter.…”