Methane seep communities on the Koryak slope in the Bering Sea

https://doi.org/10.1016/j.dsr2.2022.105203Get rights and content

Highlights

  • Methane seeps were discovered on the Koryak slope (Bering Sea) at 400–700m depth.

  • Composition and structure of seep communities differed at depths 400–402m, 417–429m and 647–695m.

  • Background species, echinoids and actiniarians, dominated the shallower seeps.

  • Chemosymbiotrophic pliocardiine Calyptogena pacifica dominated the deepest seeps.

  • The deepest seeps have the highest species richness and vary in community structure.

Abstract

Methane seep communities on the Koryak slope in the Bering Sea were discovered in 2018 during the 82nd cruise of the RV Akademik M.A. Lavrentyev using ROV Comanche 18. Methane seeps found between 400 m and 695 m depth are the northernmost chemosynthesis-based habitats (∼61°N) known to date in the Pacific. Macrofauna species composition and community structure of methane seep and background benthic communities were investigated at three depth horizons: 400–402 m, 417–429 m and 647–695 m.

A total of 335 macrofaunal species were identified. At the depth 647–695 m the species richness in the methane seep communities was 265 species and 72 species in the background. The deepest seep communities were characterized by the highest species richness, relatively high evenness and strong variations in the composition and structure. At shallower depths the species richness was low: 33–34 species at methane seeps and 66–71 in the background. The methane seep communities at shallow depths showed relatively low evenness and low diversity of community structure. The highest species richness at the greatest depth can be related in part to increased habitat heterogeneity associated with carbonate crusts and vesicomyid clam beds occurring only at deeper methane seeps. The deepest methane seep communities were dominated by the chemosymbiotrophic pliocardiine Calyptogena pacifica; dominant in the background was the ophiuroid Ophiophthalmus normani. At shallower methane seeps only single specimens of C. pacifica were found. The shallower methane seeps were dominated by the background species despite numerous extensive bacterial mats and high potential toxicity of the environment. The seep community at 417–429 m was dominated by the echinoid Brisaster latifrons with population density on the bacterial mat four times higher than in the background. Four chemosymbiotrophic species were recorded at 647–695 m and only one was found at shallower depths. Potentially obligate to reducing habitats polychaetes of the genus Neosabellides and Ophryotrocha occurred in methane seep communities at all depths. Further geochemical, geological and microbiological studies are required to better characterize differences of methane seeps at different depths and reasons of these differences.

Introduction

Areas of the deep seafloor with sulphide-rich and hydrocarbon fluids seeping out at nearly ambient temperature were first described more than thirty years ago (Martens et al., 1991). Since then it became evident that the phenomenon of so named “cold methane seeps” has the global magnitude: this discovery has changed fundamental concepts of energy and matter fluxes in the World Ocean. At methane seeps, communities depend on chemosynthetic primary production synthesized locally by microbes. Microbes utilize methane or sulphide as energy sources to produce organic matter. Concentration of methane in seeping fluids can be high whereas sulphide in this system is mainly an outcome of anaerobic methane oxidation, the process mediated by microbial consortium of methanotrophic archaea and sulphate-reducing bacteria (Boetius et al., 2000; Boetius and Suess, 2004). Methane seeps occur on active and passive continental margins, and methane can be of biogenic and/or thermogenic origin (Sibuet and Olu, 1998). Seeps are often associated with seafloor features such as pockmarks, craters, carbonate mounds, mud volcanoes or underwater pingos (Åström et al., 2017). Methane seeps have been discovered worldwide from shallow to hadal depths (Foucher et al., 2009; Vanreusel et al., 2009; Suess, 2018). Seep communities are often dominated by specialized chemosymbiotrophic species such as siboglinids, vesicomyids and mytilids (Levin et al., 2016a; Sibuet and Olu, 1998).

Depth plays an important role in structuring of chemosynthesis-based communities. This role is related to decreasing with depth of availability of organic matter of photosynthetic origin and increasing of the ecological relevance of chemosynthetic organic matter (Carney, 1994). Respectively, the composition and structure of chemosynthesis-based communities change with water depth. The boundary between “deep” and “shallow-water” types of methane seep and hydrothermal vent communities lies approximately at 200 m based on the ratio of taxa obligate to reducing habitats and dominance of chemosymbiotrophic forms (Dando, 2010; Tarasov et al., 2005). Shallow seeps and vents usually are populated by a subset of local background benthic fauna, whereas typical specialized obligate macrofauna of a high rank (genus or family) commonly occurs deeper 200 m (Dando, 2010; Gebruk et al., 1997; Hashimoto et al., 1993; Sibuet and Olu, 1998; Mironov et al., 2002; Sahling et al., 2003; Levin et al., 2000, 2003; Tarasov et al., 2005; Galkin, 2002). Sen et al. (2018) analysed data on deep- and shallow methane seeps and noted that at the shallowest sites there are very few symbiont-containing species whereas at about 400–500 m depth the number of symbiont-containing species rapidly reaches a maximum and then again decreases. Sahling et al. (2003) noted a decrease in the number of symbiotrophic species from the depth of 1600 m–160 m and suggested that the predator pressure may impede the successful settlement of obligate chemosymbiotrophic macrofauna at depths shallower ∼400 m.

Seep and vent communities play an important role as food sources for the surrounding background fauna and the significance of this food source also increases with depth (Sahling et al., 2003). However there are exceptions to this trend. Thus at the recently discovered shallow-water methane seep in the oligotrophic environment of the Laptev Sea (60–70 m depth) noticeable influence of chemosynthetic production on the background benthic community was observed expressed in the increase of abundance and biomass of local biota (Vedenin et al., 2020). At the same time, depth-related trends in the biodiversity of methane seep communities, in particular in the transition zone between shallow and deep horizons (∼200–1000 m), have not been sufficiently investigated.

Along with depth, geological and geochemical conditions affect chemosynthesis-based communities (Levin, 2005; Sahling et al., 2003). The substrate type and fluid composition are important factors controlling the composition and structure of chemosynthesis-based communities. Sulphide concentration is crucial for specialized chemosymbiotrophic species whereas toxic reducing compounds, heavy metals alongside with oxygen deficiency in this environment negatively affect non-specialized species and may limit biodiversity at seeps in comparison to non-reducing environments (Sibuet and Olu, 1998; Ondréas et al., 2020). Seafloor methane emissions fuel anaerobic methane oxidation that generates precipitation of calcium carbonate in the form of crusts adding hard substrate to otherwise soft-bottom-dominated environment (Van Dover, 2000). The added habitat complexity leads to increased biological diversity and biomass in these seafloor habitats (Cordes et al., 2010a). On the other hand, chemosymbiotrophic foundation species create specific habitats and may attract epifaunal and mobile organisms from the background thereby increasing local biodiversity (Levin et al., 2016a).

Methane seep communities on the Koryak slope of the Bering Sea were discovered in 2018 during the 82nd cruise of the RV Akademik M.A. Lavrentyev using ROV Comanche 18 (Galkin et al., 2019; Krylova et al., 2019). Gas chromatographic analysis of sea water was performed on 35 CTD-stations on the Koryak slope (Polonik, 2019; Demina et al., 2022, this issue). Significant methane anomalies were revealed in the near bottom and intermediate layers on the slope in the depth range from 400 m to 700 m. On the most stations methane concentration in the water gradually increased from the surface to the bottom or sharply increased in the bottom layer. The maximum concentration of methane in the bottom layer was 557 nmoll/l (Polonik, 2019). Water samples collected by Comanche 18 just above bacterial mats or Calyptogena beds also revealed increased methane concentrations from 18 to 493 nmoll/l (Demina et al., 2022, this issue). Other gaseous hydrocarbons except methane were absent in the CTD and Comanche samples. Therefore, biogenic origin of methane from the sedimentary deposits of the continental slope was proposed (Polonik, 2019). Moreover seismic studies in this area demonstrated presence of gas hydrates (Gretskaya and Petrovskaya, 2010; Kropp et al., 2012), which may also be sources of methane in the seeps (Polonik, 2019).

Methane seeps on the Koryak slope of the Bering Sea are the northernmost reducing habitats known to date in the Pacific (∼61°N). Earlier, reducing habitats with associated communities in the Bering Sea were recorded only on the Piip Volcano in the southwestern part of the Bering Sea (Galkin and Ivin, 2019) located at a distance of ∼800 km away from the methane seeps of the Koryak slope. The existence of specific communities on the Koryak slope was suggested based on findings of obligate chemosymbiotrophic bivalve mollusсs of the family Vesicomyidae (Pliocardiinae) in bottom fishing trawl hauls (Danilin, 2013; Krylova et al., 2018; Kolpakov et al., 2019). Methane seeps on the Koryak slope occur in the narrow depth range from 400 m to 695 m. This depth range is of a particular interest as a transition zone between “shallow” and “deep” types of chemosynthesis-based communities. The study of communities from this depth zone may be especially useful for understanding problems such as assessment of the impacts of depth on faunal structure and the prevalence of chemosymbiotrophic animals at seeps. At the same time, there is evidence of a significant variations in methane concentrations and geological characteristics on the Koryak slope in the investigated depth range (Polonik, 2019; Galkin et al., 2019; Krylova et al., 2019), factors potentially also affecting methane seep communities. Five methane seep areas were found and examined at depths from 400 m to 695 m on the Koryak slope in the Bering Sea between 60.8N 174.4E and 61.2N 175.4E. The aim of this study was to describe the benthic fauna of a new methane seep region and to examine the impact of methane seeps on the composition and structure of benthic communities at three depth ranges based on imaging and sampling.

Section snippets

Study area

The Koryak slope is a part of the North-Eastern Asian continental margin in the Bering Sea extending alongside the coast of the Koryak Mountains from the Cape Olyutorsky to the Cape Navarin (Fig. 1a). The margin here is of the continental escarpment type with rather narrow shelf zone approximately 60 km wide. The study area was located on the upper Koryak slope, relatively smooth with the steepness 1–2° (Udintsev et al., 1964) which is less than the world-wide average for continental slopes

Results

In total 335 macrofauna and megafauna taxa were recorded, 80 of them determined to the species level. The number of phyla identified was 14. Preliminary results showed that 17 species are new to science, among them in Actiniaria six new species, in Polychaeta 4, in Isopoda and Sipunculidea two and one new species in Gastropoda, Platyhelminthes and Holothuroidea. The number of new species is expected to increase after more detailed taxonomic and genetic studies. Four species of

Response of the background megafauna to methane seeps

Despite of a narrow bathymetric range examined in our study (400–695 m), we found that different megafauna was dominant at different depths in the background and response of this megafauna to methane seeps also was different.

At 400–402 m, the shallowest depth horizon in our study, the actiniarian Sagartiogeton californicus was one of the dominant species both in the background and at seeps, though the population density was lower at seeps. The sea anemones often occur in different reducing

Conclusion

The northernmost (∼61°N) known to date methane seeps and associated chemosynthesis-based communities with populations of live pliocardiines were discovered and examined on the Koryak slope of the Bering Sea. Methane seeps were detected and studied using ROV at three depth levels: 400–402 m, 417–429 m and 647–695 m.

The background faunal assemblages were different at each depth level and were characterized by own set of dominant species. Species composition of methane seep communities reflected

Supporting grants

Grant of Ministry of Science and Higher Education, Russian Federation (grant 13.1902.21.0012 for ID, contract No 075-15-2020-796)

Funding

The study was funded by the Ministry of Science and Higher Education, Russian Federation (grant 13.1902.21.0012 for ID, contract No 075-15-2020-796).

Author statement

Rybakova E.I.: Conceptualization, Data curation, Formal analysis, Methodology, Investigation, Validation, Visualization, Writing - original draft, Writing - review & editing.

Krylova E.M.: Conceptualization, Data curation, Methodology, Investigation, Validation, Writing - review & editing.

Mordukhovich V.V.: Conceptualization, Data curation, Methodology, Investigation, Validation, Project administration, Funding acquisition, Writing - review & editing.

Galkin S.V.: Conceptualization, Methodology,

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We are indebted to the A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch of Russian Academy of Sciences, for organizing and conducting the Cruise 82 of the RV Akademik M.A. Lavrentyev. We thank the captain and the crew of Akademik M.A. Lavrentyev, the chief of the expedition Denisov V.A. and the team of ROV Comanch 18 for their support during the cruise. Underwater images and video are the courtesy of the A.V. Zhirmunsky National Scientific Center of Marine

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