The 2020 ROV survey of the Site F cold seep (Formosa Ridge, northeastern South China Sea) closed with a multi-part agenda for South China Sea (SCS) seep biology: explain how local environmental factors and geographic isolation have driven population differentiation between SCS seep and Okinawa Trough hydrothermal-vent populations of shared species such as the mussel Gigantidas platifrons and the squat lobster Shinkaia crosnieri; identify undetermined Site F taxa; survey the Haima and Four Way Closure seeps; describe biodiversity, community composition and energy flow at all three known active seeps; determine the contribution of SCS seeps to the biogeography of chemosynthesis-based ecosystems; and assemble conservation baselines. As of 2026, substantial parts of that agenda are resolved: the Haima seep has been systematically surveyed and its community characterized; the vent–seep differentiation of both flagship species is documented by repeated genome-wide studies with inferred drivers (geographic setting, habitat type, ocean currents, local selection); and Site F community ecology has deepened. The surviving open core is precise and nonempty: the epifauna of the Yam seep on Four Way Closure Ridge — the third active SCS seep — remains essentially unsurveyed; numerous SCS seep taxa remain unidentified to species level; and population connectivity has been examined for only three of roughly 81 known SCS seep macrofaunal species, leaving the SCS's role in Northwest Pacific chemosynthetic biogeography — and the conservation planning that depends on it — undefined.

Background

Submarine cold seeps are seafloor sites where methane-rich fluids escape from sediments, fueling chemosynthesis-based ecosystems that, unlike the rest of the deep sea, do not depend on photosynthetic food input. Chemosynthetic bacteria oxidize methane and sulfide in the seeping fluids, either free-living or as symbionts of animals such as bathymodioline mussels (deep-sea mytilid bivalves hosting methane- or sulfide-oxidizing bacteria in their gills), siboglinid tubeworms (tube-dwelling annelids without a digestive tract, nutritionally dependent on internal symbionts), galatheoid squat lobsters, and vesicomyid clams. In the South China Sea (SCS), three active seep areas are known: Site F on Formosa Ridge (northeastern SCS, ~1120–1150 m depth), the Haima cold seep off Hainan (northwestern SCS, the largest active seep region), and the Yam seep on Four Way Closure Ridge off southwestern Taiwan (~1500–1700 m). Hydrothermal vents of the Okinawa Trough, in the adjacent Northwest Pacific, host fauna that overlaps strikingly with the SCS seeps: several species, most prominently the mussel Gigantidas platifrons and the galatheoid squat lobster Shinkaia crosnieri, live in both SCS seeps and Okinawa Trough vents. How such shared species maintain connectivity across a marginal sea — and whether vent and seep populations of the same species are genetically differentiated — bears directly on how biogeographic provinces of deep-sea chemosynthetic ecosystems are delimited.

The tools of this literature are standard population genomics and community ecology. Genome-wide single-nucleotide polymorphisms (SNPs) are obtained by restriction-site associated DNA sequencing (RAD-seq, which samples DNA adjacent to restriction-enzyme cut sites), by 2b-RAD (a variant using IIB enzymes), or by capture of ultraconserved elements (UCEs, highly conserved loci shared across taxa that can be sequenced from degraded DNA). Population structure is quantified with statistics such as FST (a measure of allele-frequency differentiation between populations), clustering analyses, and migration models; stable carbon and nitrogen isotope ratios (δ13C, δ15N) trace chemosynthetic carbon through food webs.

Before the source paper, mitochondrial-DNA comparisons had shown differentiation between vent and seep populations of S. crosnieri but apparent homogeneity in G. platifrons (Shen et al. 2016), while the first 2b-RAD SNP study of G. platifrons revealed two cryptic semi-isolated lineages separating the SCS from the open Northwest Pacific (Xu et al. 2018). The source paper (Zhao et al. 2020) then produced the first quantitative epifaunal survey of Site F — mapping authigenic carbonate substrates (carbonate rock precipitated in place from the seeping fluids, which pavements the seafloor and provides hard attachment habitat) and quantifying dominant taxa such as G. platifrons, S. crosnieri, the siboglinid tubeworm Paraescarpia echinospica and Munidopsis squat lobsters — and closed by listing the unresolved issues addressed here. By 2023, the same research group's synthesis of SCS seep macrofauna counted at least 81 species from eight phyla across Site F and Haima, with nine new species described over the preceding decade, and identified exactly which parts of the 2020 agenda remained unmet. That 2023 assessment, together with 2024–2026 studies, defines the current frontier: Haima and Site F are comparatively well characterized, but the Yam seep's epifauna is essentially unknown beyond two mussel records; a series of taxa remain morphospecies awaiting formal identification; and connectivity has been resolved for only three species (G. platifrons, S. crosnieri and the limpet Bathyacmaea nipponica), each showing seep–vent or SCS–open-ocean genetic breaks with asymmetric, ocean-current-mediated gene flow — a pattern whose generality across the remaining shared fauna, and whose consequences for the biogeographic placement and conservation of SCS seeps, is undetermined.

Problem Statement

Under the source paper's umbrella objective — fully characterize the cold-seep fauna of the South China Sea and determine its relationship to the chemosynthetic biogeography of the Northwest Pacific — the following research directions remain open as of 2026, after the Haima and Site F surveys and the population-genetic resolution of Gigantidas platifrons and Shinkaia crosnieri vent–seep differentiation documented in the Background:

  1. Survey and characterize the epifauna and macrofauna of the Yam seep on Four Way Closure Ridge (the third known active South China Sea seep, ~1500–1700 m depth, off southwestern Taiwan): determine its species inventory, community composition, abundance and substrate associations, and trophic/energy-flow structure, thereby completing the three-seep comparison that the source paper called for.

  2. Resolve the species-level identities of the South China Sea seep taxa that remain undetermined (including, at Site F, the ampharetid polychaete Amphisamytha sp., the alcyonacean soft coral Anthomastus sp., the white sponge, and several echinoderms), using integrative taxonomic and molecular work to determine which represent new or endemic species.

  3. Determine population-genetic connectivity for shared vent–seep species beyond the three already studied (G. platifrons, Shinkaia crosnieri, Bathyacmaea nipponica), across South China Sea seeps, Okinawa Trough vents and adjacent Northwest Pacific chemosynthetic ecosystems — establishing whether the seep–vent genetic breaks with current-mediated asymmetric gene flow found so far are a general pattern or species-specific, and hence what the South China Sea seeps contribute to (and how they should be provincialized within) the biogeography of chemosynthesis-based ecosystems, so that conservation plans can be devised for these ecosystems under increasing threats from human activities, especially extraction of methane hydrate from cold seeps and mining for metal-rich sulfide deposits from vent fields.

The three directions are independent and none is a prerequisite for the others: they may be pursued separately, and work addressing any one of them is not conditioned on the others being resolved.

References

  1. Zhao Y, Xu T, Law YS, Feng D, Li N, Xin R, Wang H, Ji F, Zhou H, Qiu J-W (2020) Ecological characterization of cold-seep epifauna in the South China Sea. Deep-Sea Research Part I: Oceanographic Research Papers 163:103361. DOI: 10.1016/j.dsr.2020.103361. https://doi.org/10.1016/j.dsr.2020.103361
  2. Yang C-H, Tsuchida S, Fujikura K, Fujiwara Y, Kawato M, Chan T-Y (2016) Connectivity of the squat lobsters Shinkaia crosnieri (Crustacea: Decapoda: Galatheidae) between cold seep and hydrothermal vent habitats. Bulletin of Marine Science 92(1):17–31. DOI: 10.5343/bms.2015.1031. https://doi.org/10.5343/bms.2015.1031
  3. Shen Y, Kou Q, Chen W, He S, Yang M, Li X, Gan X (2016) Comparative population structure of two dominant species, Shinkaia crosnieri (Munidopsidae: Shinkaia) and Bathymodiolus platifrons (Mytilidae: Bathymodiolus), inhabiting both deep-sea vent and cold seep inferred from mitochondrial multi-genes. Ecology and Evolution 6(11):3571–3582. DOI: 10.1002/ece3.2132. https://doi.org/10.1002/ece3.2132
  4. Xu T, Sun J, Watanabe HK, Chen C, Nakamura M, Ji R, Feng D, Lv J, Wang S, Bao Z, Qian P-Y, Qiu J-W (2018) Population genetic structure of the deep-sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific. Evolutionary Applications 11(10):1915–1930. DOI: 10.1111/eva.12696. https://doi.org/10.1111/eva.12696
  5. Cheng J, Hui M, Li Y, Sha Z (2020) Genomic evidence of population genetic differentiation in deep-sea squat lobster Shinkaia crosnieri (Crustacea: Decapoda: Anomura) from Northwestern Pacific hydrothermal vent and cold seep. Deep-Sea Research Part I: Oceanographic Research Papers 156:103188. DOI: 10.1016/j.dsr.2019.103188. https://doi.org/10.1016/j.dsr.2019.103188
  6. Xiao Y, Xu T, Sun J, Wang Y, Wong WC, Kwan YH, Chen C, Qiu J-W, Qian P-Y (2020) Population genetic structure and gene expression plasticity of the deep-sea vent and seep squat lobster Shinkaia crosnieri. Frontiers in Marine Science 7:587686. DOI: 10.3389/fmars.2020.587686. https://doi.org/10.3389/fmars.2020.587686
  7. Xu T, Wang Y, Sun J, Chen C, Watanabe HK, Chen J, Qian P-Y, Qiu J-W (2021) Hidden historical habitat-linked population divergence and contemporary gene flow of a deep-sea patellogastropod limpet. Molecular Biology and Evolution 38(12):5640–5654. DOI: 10.1093/molbev/msab278. https://doi.org/10.1093/molbev/msab278
  8. Ke Z, Li R, Chen Y, Chen D, Chen Z, Lian X, Tan Y (2022) A preliminary study of macrofaunal communities and their carbon and nitrogen stable isotopes in the Haima cold seeps, South China Sea. Deep-Sea Research Part I: Oceanographic Research Papers 184:103774. DOI: 10.1016/j.dsr.2022.103774. https://doi.org/10.1016/j.dsr.2022.103774
  9. Wang X, Guan H, Qiu J-W, Xu T, Peckmann J, Chen D, Feng D (2022) Macro-ecology of cold seeps in the South China Sea. Geosystems and Geoenvironment 1(3):100081. DOI: 10.1016/j.geogeo.2022.100081. https://doi.org/10.1016/j.geogeo.2022.100081
  10. Li Y-X, Sun Y, Lin Y-T, Xu T, Ip JCH, Qiu J-W (2023) Cold Seep Macrofauna. In: Chen D, Feng D (eds) South China Sea Seeps. Springer, Singapore, pp 69–88. DOI: 10.1007/978-981-99-1494-4_5. https://doi.org/10.1007/978-981-99-1494-4_5
  11. He X, Xu T, Chen C, Liu X, Li Y-X, Zhong Z, Gu X, Lin Y-T, Lan Y, Yan G, Sun Y, Qiu J-W, Qian P-Y, Sun J (2023) Same (sea) bed different dreams: Biological community structure of the Haima seep reveals distinct biogeographic affinities. The Innovation Geoscience 1(2):100019. DOI: 10.59717/j.xinn-geo.2023.100019. https://doi.org/10.59717/j.xinn-geo.2023.100019
  12. Wang H, Wang X, Cao L, Zhong Z, Luan Z, Li C (2023) Macrofauna community of the cold seep area at Site F, South China Sea. Frontiers in Marine Science 10:1068916. DOI: 10.3389/fmars.2023.1068916. https://doi.org/10.3389/fmars.2023.1068916
  13. Diao C, Wang M, Zhong Z, Li Y, Xian W, Zhang H (2023) Biodiversity exploration of Formosa Ridge cold seep in the South China Sea using an eDNA metabarcoding approach. Marine Environmental Research 190:106109. DOI: 10.1016/j.marenvres.2023.106109. https://doi.org/10.1016/j.marenvres.2023.106109
  14. Xu T, Chai X, Chen C, Watanabe HK, Sun J, Xiao Y, Wang Y, Chen J, Qiu J-W, Qian P-Y (2023) Genetic divergence and migration patterns of a galatheoid squat lobster highlight the need for deep-sea conservation. Molecular Ecology 33:e17200. DOI: 10.1111/mec.17200. https://doi.org/10.1111/mec.17200
  15. Tseng Y, Römer M, Lin S, Pape T, Berndt C, Chen T-T, Paull CK, Caress DW, Bohrmann G (2023) Yam Seep at Four-Way Closure Ridge: a prominent active gas seep system at the accretionary wedge SW offshore Taiwan. International Journal of Earth Sciences 112:1043–1061. DOI: 10.1007/s00531-022-02280-4. https://doi.org/10.1007/s00531-022-02280-4
  16. Ke Z, Huang H, Chen D, Tan Y (2024) Trophic relationship between mussels and scale worms under various seepage intensities in the Haima cold seep: Insights from stable isotopes (δ13C and δ15N) and C:N:P stoichiometry. Deep-Sea Research Part I: Oceanographic Research Papers 206:104264. DOI: 10.1016/j.dsr.2024.104264. https://doi.org/10.1016/j.dsr.2024.104264
  17. Dai Q, Xu T, Li Y, Sun Y, Lin Y, Yahagi T, Perez M, Qian P-Y, Qiu J-W (2025) Comparative population genetics of two alvinocaridid shrimp species in chemosynthetic ecosystems of the Western Pacific. Integrative Zoology 21(2):291–303. DOI: 10.1111/1749-4877.12954. https://doi.org/10.1111/1749-4877.12954
  18. Li Y-X, Xu T, Perez M, Chen C, Watanabe HK, Ip JC-H, Qiu J-W (2026) Sequencing Ultraconserved Elements (UCEs) for Marine Population Genomics: A Proof-of-Concept Using a Deep-Sea Mussel Species. Evolutionary Applications 19:e70195. DOI: 10.1111/eva.70195. https://doi.org/10.1111/eva.70195