A total of 65 macrofauna were found at the Haima seep, and 35 of them appear endemic to this area.
Sediment-rich vents are in intermediate habitats between seeps and hard-substrate vents.
Seep communities in the South China Sea and the North Indian Ocean are closely related.
The rich and endemic biodiversity at Haima calls for conservation measures.
[1] | Baker, M.C., Ramirez-Llodra, E.Z., et al. (2010). Biogeography, ecology, and vulnerability of chemosynthetic ecosystems in the deep sea. In life in the world's oceans, pp. 161–182. |
[2] | Dubilier, N., Bergin, C., and Lott, C. (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6, 725−740. |
[3] | Beaulieu, S.E., and Szafranski, K. (2020). InterRidge global database of active submarine hydrothermal vent fields, Version 3.4. World wide web electronic publication available from http://vents-data.interridge.org. |
[4] | Bachraty, C., Legendre, P., and Desbruyères, D. (2009). Biogeographic relationships among deep-sea hydrothermal vent faunas at global scale. Deep Sea Res. Pt. I 56, 1371−1378. |
[5] | Arellano, S.M., Van Gaest, A.L., et al. (2014). Larvae from deep-sea methane seeps disperse in surface waters. P. Roy. Soc. B-Biol. Sci. 281, 20133276. |
[6] | Van Dover, C.L., German, C.R., et al. (2002). Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295, 1253−1257. |
[7] | Tunnicliffe, V., and Mary R. Fowler, C. (1996). Influence of sea-floor spreading on the global hydrothermal vent fauna. Nature 379, 531−533. |
[8] | Moalic, Y., Desbruyères, D., Duarte, C.M., et al. (2011). Biogeography revisited with network theory: retracing the history of hydrothermal vent communities. Syst. Biol. 61, 127−127. |
[9] | Mitarai, S., Watanabe, H., Nakajima, Y., et al. (2016). Quantifying dispersal from hydrothermal vent fields in the western Pacific Ocean. Proc. Natl. Acad. Sci. 113, 2976−2981. |
[10] | Breusing, C., Biastoch, A., Drews, A., et al. (2016). Biophysical and population genetic models predict the presence of phantom stepping stones connecting mid-Atlantic Ridge vent ecosystems. Curr. Biol. 26, 2257−2267. |
[11] | Yang, J.-S., Lu, B., Chen, D.-F., et al. (2013). When did decapods invade hydrothermal vents. Clues from the Western Pacific and Indian Oceans. Mol. Biol. Evol. 30, 305−309. |
[12] | Nakajima, R., Yamakita, T., Watanabe, H., et al. (2014). Species richness and community structure of benthic macrofauna and megafauna in the deep-sea chemosynthetic ecosystems around the Japanese archipelago: an attempt to identify priority areas for conservation. Divers. Distrib. 20, 1160−1172. |
[13] | Watanabe, H., Fujikura, K., Kojima, S., et al. (2010). Japan: Vents and seeps in close proximity. In the vent and seep biota, pp. 379–401. |
[14] | Suess, E., Huang, Y., Wu, N., et al. (2005). South China Sea continental margin: geological methane budget and environmental effects of methane emissions and gas hydrates. Ifm-geomar, Kiel. R/V Sonne cruise report 177. |
[15] | Klaucke, I., Berndt, C., Crutchley, G., et al. (2016). Fluid venting and seepage at accretionary ridges: the Four Way Closure Ridge offshore SW Taiwan. Geo.-Mar. Lett. 36, 165−174. |
[16] | Tseng, Y., Römer, M., Lin, S., et al. (2023). Yam Seep at Four-Way Closure Ridge: a prominent active gas seep system at the accretionary wedge SW offshore Taiwan. Int. J. Earth. Sci. 112, 1043−1061. |
[17] | Liang, Q., Hu, Y., Feng, D., et al. (2017). Authigenic carbonates from newly discovered active cold seeps on the northwestern slope of the South China Sea: Constraints on fluid sources, formation environments, and seepage dynamics. Deep Sea Res. Pt. I 124, 31−41. |
[18] | Wang, X., Guan, H., Qiu, J.-W., et al. (2022). Macro-ecology of cold seeps in the South China Sea. Geogeo. 1, 100081. |
[19] | Kuo, M.-Y., Kang, D.-R., Chang, C.-H., et al. (2019). New records of three deep-sea Bathymodiolus mussels (Bivalvia: Mytilida: Mytilidae) from hydrothermal vent and cold seeps in Taiwan. J. Mar. Sci. Technol. 27, 6. |
[20] | Zhao, Y., Xu, T., Law, Y.S., et al. (2020). Ecological characterization of cold-seep epifauna in the South China Sea. Deep Sea Res. Part I 163, 103361. |
[21] | Chen, C., Okutani, T., Liang, Q., and Qiu, J.-W. (2018). A noteworthy new species of the family Vesicomyidae from the South China Sea (Bivalvia: Glossoidea). Venus 76, 29−37. |
[22] | Xu, T., Feng, D., Tao, J., and Qiu, J.-W. (2019). A new species of deep-sea mussel (Bivalvia: Mytilidae: Gigantidas) from the South China Sea: Morphology, phylogenetic position, and gill-associated microbes. Deep Sea Res. Pt. I 146, 79−90. |
[23] | Bohrmann, G., and Participants, C. (2008). Report and preliminary results of R/V Meteor Cruise M74/3, Fujairah Male, 30 October - 28 November, 2007. Cold seeps of the Makran subduction zone (continental margin of Pakistan). |
[24] | Mazumdar, A., Dewangan, P., Peketi, A., et al. (2021). The first record of the genus Lamellibrachia (Siboglinidae) tubeworm along with associated organisms in a chemosynthetic ecosystem from the Indian Ocean: a report from the Cauvery–Mannar Basin. J. Earth Syst. Sci. 130, 94. |
[25] | Mazumdar, A., Dewangan, P., Peketi, A., et al. (2019). The first record of active methane (cold) seep ecosystem associated with shallow methane hydrate from the Indian EEZ. J. Earth Syst. Sci. 128, 18. |
[26] | Li, X. (2017). Taxonomic research on deep-sea macrofauna in the South China Sea using the Chinese deep-sea submersible Jiaolong. Integr. Zool. 12, 270−282. |
[27] | Feng, D., Qiu, J.-W., Hu, Y., et al. (2018). Cold seep systems in the South China Sea: an overview. J. Asian Earth Sci. 168, 3−16. |
[28] | Dong, D., Li, X., Yang, M., et al. (2021). Report of epibenthic macrofauna found from Haima cold seeps and adjacent deep-sea habitats, South China Sea. Mar. Life Sci. Tech. 3, 1−12. |
[29] | Xu, H., Du, M., Li, J., et al. (2020). Spatial distribution of seepages and associated biological communities within Haima cold seep field, South China Sea. J. Sea Res. 165, 101957. |
[30] | Ke, Z., Li, R., Chen, Y., et al. (2022). A preliminary study of macrofaunal communities and their carbon and nitrogen stable isotopes in the Haima cold seeps, South China Sea. Deep Sea Res. Pt. I 184, 103774. |
[31] | Thomas, E.A., Liu, R., Amon, D., et al. (2020). Chiridota heheva—the cosmopolitan holothurian. Mar. Biodivers. 50, 110. |
[32] | Thomas, E.A., Sigwart, J.D., and Helyar, S.J. (2022). New evidence for a cosmopolitan holothurian species at deep-sea reducing environments. Mar. Biodivers. 52, 63. |
[33] | Xu, T., Sun, J., Watanabe, H.K., et al. (2018). Population genetic structure of the deep-sea mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific. Evol. Appl. 11, 1915−1930. |
[34] | Xu, T., Sun, Y., Wang, Z., et al. (2022). The morphology, mitogenome, phylogenetic position, and symbiotic bacteria of a new species of Sclerolinum (Annelida: Siboglinidae) in the South China Sea. Front. Mar. Sci. 8, 793645. |
[35] | Lin, Y.-T., Kiel, S., Xu, T., and Qiu, J.-W. (2022). Phylogenetic placement, morphology and gill-associated bacteria of a new genus and species of deep-sea mussel (Mytilidae: Bathymodiolinae) from the South China Sea. Deep Sea Res. Pt. I 190, 103894. |
[36] | Wang, H., Liu, H., Wang, X., et al. (2022). Stirring the deep, disentangling the complexity: report on the third species of Thermochiton (Mollusca: Polyplacophora) from haima cold seeps. Front. Mar. Sci. 9, 889022. |
[37] | Li, Q., Li, Y., Na, J., et al. (2021). Description of a new species of Histampica (Ophiuroidea: Ophiothamnidae) from cold seeps in the South China Sea and analysis of its mitochondrial genome. Deep Sea Res. Pt. I 178, 103658. |
[38] | Wolff, T. (2005). Composition and endemism of the deep-sea hydrothermal vent fauna. Cah. Biol. Mar. 46, 97−104. |
[39] | Kiel, S. (2016). A biogeographic network reveals evolutionary links between deep-sea hydrothermal vent and methane seep faunas. P. Roy. Soc. B-Biol. Sci. 283, 2016233. |
[40] | van Audenhaege, L., Fariñas-Bermejo, A., Schultz, T., and Lee Van Dover, C. (2019). An environmental baseline for food webs at deep-sea hydrothermal vents in Manus Basin (Papua New Guinea). Deep Sea Res. Pt. I 148, 88−99. |
[41] | Xu, T., Wang, Y., Sun, J., et al. (2021). Hidden historical habitat-linked population divergence and contemporary gene flow of a deep-sea patellogastropod limpet. Mol. Biol. Evol. 38, 5640−5654. |
[42] | Zhang, S., Zhang, J., and Zhang, S. (2016). A new species of Bathyacmaea (Gastropoda: Pectinodontidae) from a methane seep area in the South China Sea. Nautilus 130, 1−4. |
[43] | Lin, Y.-T., Li, Y.-X., Sun, Y., et al. (2023). A new species of the genus Catillopecten (Bivalvia: Pectinoidea: Propeamussiidae): morphology, mitochondrial genome, and phylogenetic relationship. Front. Mar. Sci. 10, 1168991. |
[44] | Chen, C., Zhong, Z., Qiu, J.-W., and Sun, J. (2023). A new Paralepetopsis limpet from a South China Sea seep hints at a paraphyletic Neolepetopsidae. Zool. Stud. 62, 26. |
[45] | Krylova, E.M., Sahling, H., and Borowski, C. (2018). Resolving the status of the families Vesicomyidae and Kelliellidae (Bivalvia: Venerida), with notes on their ecology. J. Mollus. Stud. 84, 69−91. |
[46] | Johnson, S.B., Krylova, E.M., Audzijonyte, A., et al. (2017). Phylogeny and origins of chemosynthetic vesicomyid clams. System. Biodivers. 15, 346−360. |
[47] | Decker, C., Olu, K., Cunha, R.L., and Arnaud-Haond, S. (2012). Phylogeny and diversification patterns among vesicomyid bivalves. PLoS One 7, e33359. |
[48] | Sato, K., Kano, Y., Setiamarga, D.H.E., et al. (2020). Molecular phylogeny of protobranch bivalves and systematic implications of their shell microstructure. Zool. Scr. 49, 458−472. |
[49] | Li, Y., He, X., Lin, Y., et al. (2023). Reduced chemosymbiont genome in the methane seep thyasirid and the cooperated metabolisms in the holobiont under anaerobic sediment. Mol. Ecol. Resour. Doi:10.1111/1755-0998.13846. |
[50] | Van Dover, C.L., Humphris, S.E., Fornari, D., et al. (2001). Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294, 818−823. |
[51] | Sasaki, T., Ogura, T., Watanabe, H.K., and Fujikura, K. (2016). Four new species of Provanna (Gastropoda: Provannidae) from vents and a seep off Nansei-shoto Area, Southwestern Japan. Venus 74, 1−17. |
[52] | Poitrimol, C., Thiébaut, É., Daguin-Thiébaut, C., et al. (2022). Contrasted phylogeographic patterns of hydrothermal vent gastropods along South West Pacific: Woodlark Basin, a possible contact zone and/or stepping-stone. PLoS One 17, e0275638. |
[53] | Lorion, J., Kiel, S., Faure, B., et al. (2013). Adaptive radiation of chemosymbiotic deep-sea mussels. P. Roy. Soc. B-Biol. Sci. 280, 20131243. |
[54] | Nan, F., Xue, H., Chai, F., et al. (2011). Identification of different types of Kuroshio intrusion into the South China Sea. Ocean Dyn. 61, 1291−1304. |
[55] | Liu, Z., Li, X., Colin, C., and Ge, H. (2010). A high-resolution clay mineralogical record in the northern South China Sea since the Last Glacial Maximum, and its time series provenance analysis. Chinese Sci. Bull. 55, 4058−4068. |
[56] | Feng, D., Cheng, M., Kiel, S., et al. (2015). Using Bathymodiolus tissue stable carbon, nitrogen and sulfur isotopes to infer biogeochemical process at a cold seep in the south China Sea. Deep Sea Res. Pt. I 104, 52−59. |
[57] | Feng, D., Peckmann, J., Li, N., et al. (2018). The stable isotope fingerprint of chemosymbiosis in the shell organic matrix of seep-dwelling bivalves. Chem. Geol. 479, 241−250. |
[58] | Sun, J., Zhang, Y., Xu, T., et al. (2017). Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes. Nat. Ecol. Evol. 1, 0121. |
[59] | Ip, J.C.-H., Xu, T., Sun, J., et al. (2021). Host-endosymbiont genome integration in a deep-sea chemosymbiotic clam. Mol. Biol. Evol. 38, 502−518. |
[60] | Sun, Y., Sun, J., Yang, Y., et al. (2021). Genomic signatures supporting the symbiosis and formation of chitinous tube in the deep-sea tubeworm Paraescarpia echinospica. Mol. Biol. Evol. 38, 4116−4134. |
[61] | Yang, Y., Sun, J., Sun, Y., et al. (2020). Genomic, transcriptomic, and proteomic insights into the symbiosis of deep-sea tubeworm holobionts. ISME J. 14, 135−150. |
[62] | Becker, E.L., Cordes, E.E., Macko, S.A., et al. (2013). Using stable isotope compositions of animal tissues to infer trophic interactions in Gulf of Mexico lower slope seep communities. PLoS One 8, e74459. |
[63] | Wang, X., Fan, D., Kiel, S., et al. (2022). Archives of short-term fluid flow dynamics and possible influence of human activities at methane seeps: evidence from high-resolution element geochemistry of chemosynthetic bivalve shells. Front. Mar. Sci. 9, 960338. |
[64] | von Rad, U., Berner, U., Delisle, G., et al. (2000). Gas and fluid venting at the Makran accretionary wedge off Pakistan. Geo.-Mar. Lett. 20, 10−19. |
[65] | Krylova, E.M., and Sahling, H. (2006). Recent bivalve molluscs of the genus Calyptogena (Vesicomyidae). J. Mollus. Stud. 72, 359−395. |
[66] | marumTV (2013). Cold Seeps in the deep sea https://www.youtube.com/watch?v=QnLA1HyGahU. YouTube. |
[67] | Assié, A., Borowski, C., van der Heijden, K., et al. (2016). A specific and widespread association between deep-sea Bathymodiolus mussels and a novel family of Epsilonproteobacteria. Env. Microbiol. Rep. 8, 805−813. |
[68] | Neulinger, S., Sahling, H., Süling, J., and Imhoff, J. (2006). Presence of two phylogenetically distinct groups in the deep-sea mussel Acharax (Mollusca: Bivalvia: Solemyidae). Mar. Ecol. Prog. Ser. 312, 161−168. |
[69] | Saraswat, R., Singh, D.P., Lea, D.W., et al. (2019). Indonesian throughflow controlled the westward extent of the Indo-Pacific Warm Pool during glacial-interglacial intervals. Glob. Planet. Change 183, 103031. |
[70] | Lohman, D.J., Bruyn, M.d., Page, T., et al. (2011). Biogeography of the Indo-Australian Archipelago. Annu. Rev. Ecol. Evol. Syst. 42, 205−226. |
[71] | Kiel, S., Aguilar, Y., and Kase, T. (2020). Mollusks from Pliocene and Pleistocene seep deposits in Leyte, Philippines. Acta Palaeontol. Pol. 65, 589−627. |
[72] | Wiedicke, M., Sahling, H., Delisle, G., et al. (2002). Characteristics of an active vent in the fore-arc basin of the Sunda Arc, Indonesia. Mar. Geol. 184, 121−141. |
[73] | Chen, L., Feng, Y., Okajima, J., et al. (2018). Production behavior and numerical analysis for 2017 methane hydrate extraction test of Shenhu, South China Sea. J. Nat. Gas Sci. Eng. 53, 55−66. |
[74] | Zhang, W., Liang, J., Liang, Q., et al. (2021). Gas hydrate accumulation and occurrence associated with cold seep systems in the Northern South China Sea: an overview. Geofluids 2021, 5571150. |
[75] | Thomas, E.A., Molloy, A., Hanson, N.B., et al. (2021). A global red list for hydrothermal vent molluscs. Front. Mar. Sci. 8, 713022. |
[76] | Folmer, O., Black, M., Hoeh, W., et al. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294−299. |
[77] | Turbeville, J.M., Schulz, J.R., and Raff, R.A. (1994). Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology. Mol. Biol. Evol. 11, 648−655. |
[78] | Elwood, H.J., Olsen, G.J., and Sogin, M.L. (1985). The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol. Biol. Evol. 2, 399−410. |
[79] | Lenaers, G., Maroteaux, L., Michot, B., and Herzog, M. (1989). Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA. J. Mol. Evol. 29, 40−51. |
[80] | Colgan, D., McLauchlan, A., Wilson, G., et al. (1998). Histone H3 and U2 snRNA DNA sequences and arthropod evolution. Aust. J. Zool. 46, 419−437. |
[81] | Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114−2120. |
[82] | Prjibelski, A., Antipov, D., Meleshko, D., et al. (2020). Using SPAdes de novo assembler. Curr. Protoc. Bioinformatics 70, e102. |
[83] | Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792−1797. |
[84] | Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldón, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972−1973. |
[85] | Minh, B.Q., Schmidt, H.A., Chernomor, O., et al. (2020). IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530−1534. |
[86] | Team, R.C. (2022). R: A Language and Environment for Statistical Computing. |
[87] | Brunner, O., Chen, C., Giguère, T., et al. (2022). Species assemblage networks identify regional connectivity pathways among hydrothermal vents in the Northwest Pacific. Ecol. Evol. 12, e9612. |
[88] | Sangodkar, N., Gonsalves, M.J., and Nazareth, D.R. (2023). Macrofaunal distribution, diversity, and its ecological interaction at the cold seep site of Krishna-Godavari basin, east coast of India. Microb. Ecol. 85, 61−75. |
[89] | Dewangan, P., Sriram, G., Kumar, A., et al. (2020). Widespread occurrence of methane seeps in deep-water regions of Krishna-Godavari basin, Bay of Bengal. Mar. Pet. Geol. 124, 104783. |
[90] | Grabherr, M.G., Haas, B.J., Yassour, M., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644−652. |
[91] | Li, W., and Godzik, A. (2006). Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658−1659. |
[92] | Seppey, M., Manni, M., and Zdobnov, E.M. (2019). BUSCO: Assessing genome assembly and annotation completeness. In Gene Prediction: Methods and Protocols, pp. 227–245. |
[93] | Sun, J., Li, R., Chen, C., et al. (2021). Benchmarking Oxford Nanopore read assemblers for high-quality molluscan genomes. P. Roy. Soc. B-Biol. Sci. 376, 20200160. |
[94] | Liu, X., Sigwart, J.D., and Sun, J. (2022). Phylogenomic analyses shed light on the relationships of chiton superfamilies and shell-eye evolution. bioRxiv 2022.2012.2012.520088. |
[95] | dos Reis, M., and Yang, Z. (2011). Approximate likelihood calculation on a phylogeny for bayesian estimation of divergence times. Mol. Biol. Evol. 28, 2161−2172. |
He X., Xu T., Chen C., et al., (2023). Same (sea) bed different dreams: Biological community structure of the Haima seep reveals distinct biogeographic affinities. The Innovation Geoscience 1(2), 100019. https://doi.org/10.59717/j.xinn-geo.2023.100019 |
The distributions of vents and seeps in Indo-West Pacific and their biological community structures
A photo plate showing the dominant macrofauna at the Haima seep
A maximum likelihood phylogeny of Vesicomyidae based on partial COI gene
A time-calibrated phylogeny showing the estimated divergent time among bathymodioline species
Stable isotope compositions (δ13C, δ15N, and δ34S) of 23 macrofauna taxa collected from the Haima seep