Methane seep communities on the Koryak slope in the Bering Sea
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
References (144)
Composition and distribution of polychaete assemblages associated with hydrothermal vents and cold seeps in the Bering Sea
Deep Sea Res. 2 Top. Stud. Oceanogr.
(2022)- et al.
New species of Ophryotrocha (Annelida: Dorvilleidae) associated with deep-sea reducing habitats in the Bering Sea, Northwest Pacific
Deep Sea Res. 2 Top. Stud. Oceanogr.
(2022) - et al.
Hydrate Ridge: a natural laboratory for the study of microbial life fueled by methane from near-surface gas hydrates
Chem. Geol.
(2004) - et al.
Nematode abundance at the oxygen minimum zone in the Arabian Sea
Deep Sea Res. 2 Top. Stud. Oceanogr.
(2000) - et al.
Can the hemoglobin characteristics of vesicomyid clam species influence their distribution in deep-sea sulfide-rich sediments? A case study in the Angola Basin
Deep Sea Res. 2. Top. Stud. Oceanogr.
(2017) - et al.
Variations in deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau
Deep Sea Res. 1 Oceanogr. Res. Pap.
(2001) - et al.
Deep-sea acorn worms (Enteropneusta) from the Bering Sea with the description of a new genus and a new species of Torquaratoridae dominating soft-bottom communities
Deep Sea Res. 2 Top. Stud. Oceanogr.
(2022) - et al.
Ecology and biogeography of the hydrothermal vent fauna of the Mid-Atlantic Ridge
Adv. Mar. Biol.
(1997) - et al.
Cold seep and oxygen minimum zone associated sources of margin heterogeneity affect benthic assemblages, diversity and nutrition at the Cascadian margin (NE Pacific Ocean)
Prog. Oceanogr.
(2012) - et al.
The vesicomyid bivalve habitat at cold seeps supports heterogeneous and dynamic macrofaunal assemblages
Deep Sea Res. 1 Oceanogr. Res. Pap.
(2017)
Correlation of the siboglinid (Annelida: Siboglinidae) distribution to higher concentrations of hydrocarbons in the Sea of Okhotsk
Mar. Pollut. Bull.
Community composition and temporal change at deep Gulf of Mexico cold seeps
Deep Sea Res. 2. Top. Stud. Oceanogr.
Simulation of long-term feedbacks from authigenic carbonate crust formation at cold vent sites
Chem. Geol.
Shell-bearing Gastropoda from the methane seeps and hydrothermal vents of the Bering Sea: a preliminary description
Deep Sea Res. 2 Top. Stud. Oceanogr.
Emergence of burrowing urchins from California Continental Shelf sediments - a response to alongshore current reversals?
Estuar. Coast Shelf Sci.
Influence of seep emission on the non-symbiont-bearing fauna and vagrant species at an active giant pockmark in the Gulf of Guinea (Congo–Angola margin)
Deep Sea Res. 2. Top. Stud. Oceanogr.
Cold seep communities in the deep eastern Mediterranean Sea: composition, symbiosis and spatial distribution on mud volcanoes
Deep Sea Res. 1. Oceanogr. Res. Pap.
Oxygen minimum zones (OMZs) in the modern ocean
Prog. Oceanogr.
Reports on the dredging operations off the west coast of Central America to the Galápagos, to the west coast of México, and in the Gulf of California, in charge of Alexander Agassiz, carried on by the U.S. Fish Commission Streamer “Albatross”, during 1891, Lieut. Commander Z. L. Tanner, U.S.N., Commanding. XXIII. Preliminary report on the Echini
Bull. Mus. Comp. Zool.
A chemosynthetic ecotone – “chemotone” - in the sediments surrounding deep-sea methane seeps
Limnol. Oceanogr.
Methane cold seeps as biological oases in the high-Arctic deep sea
Limnol. Oceanogr.
Cold seeps in a warming Arctic: insights for benthic ecology
Front. Mar. Sci.
Molecular taxonomy reveals broad trans-oceanic distributions and high species diversity of deep-sea clams (Bivalvia: Vesicomyidae: Pliocardiinae) in chemosynthetic environments
Syst. Biodivers.
The influence of pore-water chemistry and physiology in the distribution of vesicomyid clam at cold seeps in Monterey Bay: implications for patterns of chemosynthetic community organization
Limnol. Oceanogr.
A marine microbial consortium apparently mediating anaerobic oxidation of methane
Nature
Cold seep epifaunal communities on the Hikurangi Margin, New Zealand: composition, succession, and vulnerability to human activities
PLoS One
Actiniaria from the Gulf of California. Eastern pacific expeditions of the New York Zoological Society. XIX
Zoologica
Consideration of the oasis analogy for chemosynthetic communities at Gulf of Mexico hydrocarbon vents
Geo Mar. Lett.
Description of two new sponges
First columbellid species (Gastropoda: Buccinoidea) from deep-sea hydrothermal vents, discovered in Okinawa Trough, Japan
Zootaxa
North Pacific ophiurans in the collection of the United States National Museum
Smithson. Instit. U. S. Natl. Museum Bullet.
A Catalogue of the Recent Sea-Urchins (Echinoidea) in the Collection of the British Museum (Natural History)
PRIMER V6: User Manual/tutorial
The influence of geological, geochemical, and biogenic habitat heterogeneity on seep biodiversity
Mar. Ecol.
Unusual habitats and organisms associated with the cold seeps of the Gulf of Mexico
On some new or interesting west American shells obtained from the dredgings of the U.S. Fish Commission steamer Albatross in 1888, and from other sources
Proceed. US Natl. Museum
Some new species of mollusks from California
Nautilus
The first sea anemone (Cnidaria: Anthozoa: Actiniaria) from a whale fall
J. Nat. Hist.
Biological communities at marine shallow-water vent and seep sites
Interactive comment on “An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea” by S. Duperron et al
Biogeosci. Discuss.
Fra den norske Nordhavsexpedition
Nyt. magazin for naturvidenskaberne
Bivalve molluscs as potential indicators of areas of hydrothermal activity. Materials of the Conference devoted to the Day of Volcanologist "Volcanism and Related Processes
Trace metal biogeochemistry in the methane seeps on the Koryak slope of the Bering Sea
Deep Sea Res. 2 Top. Stud. Oceanogr.
Handbook of deep-sea hydrothermal vent fauna
Denisia
Marine benthic hypoxia: a review of its ecological effects and the behavioural response of benthic macrofauna
Oceanogr. Mar. Biol.
Do ampharetids take sedimented steps between vents and seeps? Phylogeny and habitat-use of Ampharetidae (Annelida, Terebelliformia) in chemosynthesis-based ecosystems
BMC Evol. Biol.
The hydrothermal vent community of a new deep-sea field, Ashadze-1, 12°58′N on the Mid-Atlantic Ridge
J. Mar. Biol. Assoc. U. K.
Maractis rimicarivora, a new genus and species of sea anemone (Cnidaria: Anthozoa: Actiniaria: Actinostolidae) from an Atlantic hydrothermal vent
Proc. Biol. Soc. Wash.
Observations on the natural history of Sertularia gelatinosa of Pallas
Edinburgh Philosoph. J.
Structure and drivers of cold seep ecosystems
Oceanography
Cited by (13)
Seeps and vents of the Bering Sea
2023, Deep-Sea Research Part II: Topical Studies in OceanographyMega- and macrofauna of the hydrothermally active submarine Piip Volcano (the southwestern Bering Sea)
2023, Deep-Sea Research Part II: Topical Studies in OceanographySagartiidae (Cnidaria: Actiniaria) from hydrothermal vents and methane seeps in the Bering Sea
2023, Deep-Sea Research Part II: Topical Studies in OceanographyDeep-sea hydrozoans in the western part of the Bering Sea: some hydroids associated with methane seep communities at upper bathyal depths and abyssal hydroids with a description of two new species
2023, Deep-Sea Research Part II: Topical Studies in OceanographyCitation Excerpt :Hydroids were collected from four areas located at depths from 400 m to 660 m and from the surrounding background communities. The list of all identified hydroids based on Naumov (1960) was presented in Rybakova et al. (2022). Additionally, the southern slope of the Volcanologists Massif (3362–3931 m) and small high in the Komandorsky Basin northwest of the Volcanologists Massif (3653 m) in the southwestern part of the Bering Sea were observed during this cruise and some hydroids were collected.
New species of Ophryotrocha (Annelida: Dorvilleidae) associated with deep-sea reducing habitats in the Bering Sea, Northwest Pacific
2022, Deep-Sea Research Part II: Topical Studies in OceanographyCitation Excerpt :More recently these reducing habitats were investigated during three expeditions onboard RV Akademik M.A. Lavrentyev in 2016, 2018, and 2021 using ROV Comanche 18 (Galkin et al., 2019; Rybakova et al., 2022a, this issue). The expeditions have shown the relative spatiotemporal stability of benthic communities associated with the hydrothermal vents of the Piip Volcano, and the existence of five methane seep fields located in a narrow vertical range (400–700 m) of the upper bathyal zone of the Koryak slope (Galkin and Ivin, 2019; Galkin et al., 2019; Rybakova et al., 2022a,b, this issue). Hydrothermal activity on both summits of the volcano (concentrated mainly above the 450-m isobath) and active methane seepage on the Koryak slope were clearly marked by the presence of bacterial mats, reduced sediment, carbonate crust protrusions and populations of chemosymbiotic bivalves Calyptogena pacifica Dall, 1891.