Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T09:59:46.989Z Has data issue: false hasContentIssue false
  • English
  • Français

From wood to vent: first cocculinid limpet associated with hydrothermal activity discovered in the Weddell Sea

Published online by Cambridge University Press:  22 April 2020

Chong Chen Open the ORCID record for Chong Chen [Opens in a new window]  and
Katrin Linse Open the ORCID record for Katrin Linse [Opens in a new window]
Chong Chen*
Affiliation:
X-STAR, Japan Agency for Marine-Earth Science and Technology(JAMSTEC), 2–15 Natsushima-cho, Yokosuka, Kanagawa Prefecture237-0061, Japan
Katrin Linse
Affiliation:
British Antarctic Survey, High Cross, CambridgeCB3 0ET, UK
*
[email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Lush ‘oases’ of life seen in chemosynthetic ecosystems such as hot vents and cold seeps represent rare, localized exceptions to the generally oligotrophic deep ocean floor. Organic falls, best known from sunken wood and whale carcasses, are additional sources of such oases. Kemp Caldera (59°42'S, 28°20'W) in the Weddell Sea exhibits active hydrothermal vents and a natural whale fall in close proximity, where an undescribed cocculinid limpet was found living in both types of chemosynthetic habitats. This represents the first member of the gastropod order Cocculinida discovered from hot vents, and also the first record from the Southern Ocean. Here, we applied an integrative taxonomy framework incorporating traditional dissection, electron microscopy, genetic sequencing and 3D anatomical reconstruction through synchrotron computed tomography in order to characterize this species. Together, our data revealed an unusual member of the genus Cocculina with a highly modified radula for feeding on bacterial film, described herein as Cocculina enigmadonta n. sp. Its phylogenetically derived position within the largely wood-inhabiting Cocculina indicates that it probably evolved from an ancestor adapted to living on sunken wood, providing a compelling case of the ‘stepping stone’ evolutionary trajectory from organic falls to seeps and vents.

Keywords

CocculinaCocculinidaeCocculiniformiamolluscnew speciesSouth Sandwich Arc
Type
Biological Sciences
Information
Antarctic Science , Volume 32 , Issue 5 , October 2020 , pp. 354 - 366
Check for updates
Copyright
Copyright © Antarctic Science Ltd 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

This article is registered in ZooBank under: urn:lsid:zoobank.org:pub:296FAB17-E989-4921-9E2D-2F8518B2D05F

Cocculina enigmadonta n. sp. is registered in ZooBank under: urn:lsid:zoobank.org:act:0F15867C-6B73-40E3-B0C9-762F8CFE5730

References

Aktipis, S.W. & Giribet, G. 2012. Testing relationships among the vetigastropod taxa: a molecular approach. Journal of Molluscan Studies, 78, 10.1093/mollus/eyr023.10.1093/mollus/eyr023CrossRefGoogle Scholar
Amon, D.J., Glover, A.G., Wiklund, H., Marsh, L., Linse, K., Rogers, A.D., et al. 2013. The discovery of a natural whale fall in the Antarctic deep sea. Deep Sea Research II, 92, 10.1016/j.dsr2.2013.01.028.CrossRefGoogle Scholar
Ardila, N.E. & Harasewych, M.G. 2005. Cocculinid and pseudococculinid limpets (Gastropoda: Cocculiniformia) from off the Caribbean coast of Colombia. Proceedings of the Biological Society of Washington, 118, 344–366.10.2988/0006-324X(2005)118[344:CAPLGC]2.0.CO;2CrossRefGoogle Scholar
Bates, A.E., Tunnicliffe, V. & Lee, R.W. 2005. Role of thermal conditions in habitat selection by hydrothermal vent gastropods. Marine Ecology Progress Series, 305, 1–15.10.3354/meps305001CrossRefGoogle Scholar
Bouchet, P., Rocroi, J.-P., Hausdorf, B., Kaim, A., Kano, Y., Nützel, A., et al. 2017. Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia, 61, 1–526.10.4002/040.061.0201CrossRefGoogle Scholar
Chen, C., Marsh, L. & Copley, J.T. 2018a. Is it sex in chains? Potential mating stacks in deep-sea hydrothermal vent snails. Plankton & Benthos Research, 13, 25–27.CrossRefGoogle Scholar
Chen, C., Linse, K., Uematsu, K. & Sigwart, J.D. 2018b. Cryptic niche switching in a chemosymbiotic gastropod. Proceedings of the Royal Society B: Biological Sciences, 285, 10.1098/rspb.2018.1099.Google Scholar
Cledón, M., Nuñez, J.D., Ocampo, E.H. & Sigwart, J.D. 2016. Sexual traits plasticity of the potentially invasive limpet Bostrycapulus odites (Gastropoda: Calyptraeidae) within its natural distribution in South America. Marine Ecology, 37, 10.1111/maec.12329.CrossRefGoogle Scholar
Cunha, T.J. & Giribet, G. 2019. A congruent topology for deep gastropod relationships. Proceedings of the Royal Society B: Biological Sciences, 286, 10.1098/rspb.2018.2776.Google ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.Google ScholarPubMed
Fretter, V. 1989. The anatomy of some new archaeogastropod limpets (superfamily Peltospiracea) from hydrothermal vents. Journal of Zoology (London ), 218, 123–160.CrossRefGoogle Scholar
Haszprunar, G. 1987. Anatomy and affinities of cocculinid limpets (Mollusca, Archaeogastropoda). Zoologica Scripta, 16, 305–324.10.1111/j.1463-6409.1987.tb00077.xCrossRefGoogle Scholar
Haszprunar, G. 1988. Comparative anatomy of cocculiniform gastropods and its bearing on archaeogastropod systematics. Malacological Review Supplement, 4, 64–84.Google Scholar
Hickman, C.S. 1983. Radula patterns, systematics, diversity, and ecology of deep-sea limpets. The Veliger, 26, 73–92.Google Scholar
Lanfear, R., Senfeld, T., Frandsen, P.B., Wright, A.M. & Calcott, B. 2016. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 10.1093/molbev/msw260.Google Scholar
Leal, J.H. & Harasewych, M.G. 1999. Deepest Atlantic molluscs: hadal limpets (Mollusca, Gastropoda, Cocculiniformia) from the northern boundary of the Caribbean Plate. Invertebrate Biology, 118, 116–136.CrossRefGoogle Scholar
Leat, P.T., Fretwell, P.T., Tate, A.J., Larter, R.D., Martin, T.J., Smellie, J.L., et al. 2016. Bathymetry and geological setting of the South Sandwich Islands volcanic arc. Antarctic Science, 28, 10.1017/S0954102016000043.10.1017/S0954102016000043CrossRefGoogle Scholar
Linse, K., Roterman, C.N. & Chen, C. 2019. A new vent limpet in the genus Lepetodrilus (Gastropoda: Lepetodrilidae) from Southern Ocean hydrothermal vent fields showing high phenotypic plasticity. Frontiers in Marine Science, 6, 10.3389/fmars.2019.00381.CrossRefGoogle Scholar
Linse, K., Jackson, J.A., Malyutina, M.V. & Brandt, A. 2014. Shallow-water northern hemisphere Jaera (Crustacea, Isopoda, Janiridae) found on whale bones in the Southern Ocean deep sea: ecology and description of Jaera tyleri sp. nov. PLoS ONE, 9, 10.1371/journal.pone.0093018.Google ScholarPubMed
Little, C.T.S. & Vrijenhoek, R.C. 2003. Are hydrothermal vent animals living fossils? Trends in Ecology & Evolution, 18, 10.1016/j.tree.2003.08.009.10.1016/j.tree.2003.08.009CrossRefGoogle Scholar
Marshall, B.A. 1985. Recent and Tertiary Cocculinidae and Pseudococculinidae (Mollusca: Gastropoda) from New Zealand and New South Wales. New Zealand Journal of Zoology, 12, 505–546.CrossRefGoogle Scholar
McLean, J.H. 1992. Cocculiniform limpets (Cocculinidae and Pyropeltidae) living on whale bone in the deep sea off California. Journal of Molluscan Studies, 58, 401–414.CrossRefGoogle Scholar
McLean, J.H. & Harasewych, M.G. 1995. Review of western Atlantic species of cocculinid and pseudococculinid limpets with descriptions of new species (Gastropoda: Cocculiniformia). Contributions in Science (Los Angeles), 453, 1–33.Google Scholar
Padilla, D.K. 1998. Inducible phenotypic plasticity of the radula in Lacuna (Gastropoda: Littorinidae). The Veliger, 41, 201–204.Google Scholar
Picken, G.B. & Allan, D. 1983. Unique spawning behaviour by the Antarctic limpet Nacella (Patinigera) concinna (Strebel, 1908). Journal of Experimental Marine Biology and Ecology, 71, 10.1016/0022-0981(83)90121-1.10.1016/0022-0981(83)90121-1CrossRefGoogle Scholar
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 10.1093/sysbio/syy032.CrossRefGoogle ScholarPubMed
Rogers, A.D., Tyler, P.A., Connelly, D.P., Copley, J.T., James, R., Larter, R.D., et al. 2012. The discovery of new deep-sea hydrothermal vent communities in the Southern Ocean and implications for biogeography. PLoS Biology, 10, 10.1371/journal.pbio.1001234.10.1371/journal.pbio.1001234CrossRefGoogle ScholarPubMed
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 10.1093/sysbio/sys029.CrossRefGoogle ScholarPubMed
Roterman, C.N., Copley, J.T., Linse, K.T., Tyler, P.A. & Rogers, A.D. 2016. Connectivity in the cold: the comparative population genetics of vent-endemic fauna in the Scotia Sea, Southern Ocean. Molecular Ecology, 25, 10.1111/mec.13541.10.1111/mec.13541CrossRefGoogle ScholarPubMed
Ruthensteiner, B. 2008. Soft part 3D visualization by serial sectioning and computer reconstruction. Zoosymposia, 1, 63–100.CrossRefGoogle Scholar
Sasaki, T. 1998. Comparative anatomy and phylogeny of the recent Archaeogastropoda (Mollusca: Gastropoda). The University Museum, the University of Tokyo, Bulletin, 38, 1–224.Google Scholar
Sasaki, T., Maekawa, Y., Takeda, Y., Atsushiba, M., Chen, C., Noshita, K., et al. 2018. 3D visualization of calcified and non-calcified molluscan tissues using computed tomography. In Endo, K., Kogure, T. & Nagasawa, H., eds. Biomineralization. Singapore: Springer Singapore, 83–93.CrossRefGoogle Scholar
Smith, C.R. & Baco, A.R. 2003. Ecology of whale falls at the deep-sea floor. Oceanography and Marine biology, 41, 311–354.Google Scholar
Smith, C.R., Glover, A.G., Treude, T., Higgs, N.D. & Amon, D.J. 2015. Whale-fall ecosystems: recent insights into ecology, paleoecology, and evolution. Annual Review of Marine Science, 7, 10.1146/annurev-marine-010213-135144.CrossRefGoogle ScholarPubMed
Thubaut, J., Puillandre, N., Faure, B., Cruaud, C. & Samadi, S. 2013. The contrasted evolutionary fates of deep-sea chemosynthetic mussels (Bivalvia, Bathymodiolinae). Ecology and Evolution, 3, 10.1002/ece3.749.CrossRefGoogle Scholar
Van Dover, C.L. 2000. The ecology of deep-sea hydrothermal vents. Princeton, NJ: Princeton University Press, 448 pp.Google Scholar
Vrijenhoek, R.C. 2013. On the instability and evolutionary age of deep-sea chemosynthetic communities. Deep Sea Research II, 92, 10.1016/j.dsr2.2012.12.004.CrossRefGoogle Scholar
Warén, A. & Bouchet, P. 1993. New records, species, genera, and a new family of gastropods from hydrothermal vents and hydrocarbon seeps. Zoologica Scripta, 22, 10.1111/j.1463-6409.1993.tb00342.x.CrossRefGoogle Scholar
Warén, A. & Bouchet, P. 2001. Gastropoda and Monoplacophora from hydrothermal vents and seeps: new taxa and records. The Veliger, 44, 116–231.Google Scholar
Zhang, S. & Zhang, S. 2018. Cocculina delphinicula sp. nov., a new cocculinid species from whale bone in the East China Sea (Gastropoda: Cocculiniformia). Zootaxa, 4455, 189–195.CrossRefGoogle Scholar