Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5336 No. 1: 21 Aug. 2023
Type: Article
Published: 2023-08-21
DOI: 10.11646/zootaxa.5336.1.3
Page range: 82-94
Abstract views: 185
PDF downloaded: 20

Growth in two deep-sea associates: the octocoral Pseudogorgia bellona and the euryalid snake star Asteroschema ajax

Laboratoire Littoral Environnement et Sociétés (LIENSs); UMR 7266; CNRS-La Rochelle Université; 2 rue Olympe de Gouges; F- 17042 La Rochelle Cedex 01; France
Faculty of Human Environmental Studies; Hiroshima Shudo University; 1-1-1 Ozuka-Higashi; Asaminami-ku; Hiroshima 731-3195; Japan
Institut Systématique Evolution Biodiversité (ISYEB); Muséum national d’Histoire naturelle; CNRS; Sorbonne Université; EPHE; Université des Antilles; 43 rue Cuvier; CP 26; 75005 Paris; France; Laboratoire des Sciences de l’Environnement Marin (LEMAR); UMR 6539 CNRS-UBO-IRD-Ifremer; Institut Universitaire Européen de la Mer; 29280 Plouzané; France
Octocorallia biological association Commensalism Chrysogorgiidae ophiuroidea Asteroschema Ophiocreas bellona Plateau New Caledonia Chesterfield Islands DNA barcoding

Abstract

The deep-sea octocoral Pseudochrysogorgia bellona was recently described from specimens sampled on the Chesterfield Plateau, off New Caledonia. It is morphologically and genetically similar to the con-familial Metallogorgia melanotrichos, which is known to closely associate with a species of brittle star, Ophiocreas oedipus. These latter two species have never been observed separately and are thought to grow synchronously. The morphological similarity between M. melanotrichos and P. bellona makes the latter another possible host for ophiuroids. However, no brittle star was associated with P. bellona specimens from the type collection. In 2017, 130 P. bellona colonies were sampled near the type locality, and 98% were associated with Asteroschema ajax, a species closely related to O. oedipus. Mitochondrial DNA analysis confirmed the morphological identifications of both P. bellona and A. ajax. Uni- and multivariate statistical analyses were used to characterize the morphological space of both species to test if larger ophiuroids are associated with larger corals. Two variables were measured to estimate the size of the coral (total height and diameter of the skeletal axis at its base) and 9 variables were used to characterize the brittle star (disc and arm morphology). Morphological variables representing the size for both species were significantly correlated (Spearman rank correlation coefficient: 50%, p < 0.001), suggesting that larger ophiuroids indeed associate with larger corals. This is one of the rare studies that allowed comparison of growth in associated deep-sea invertebrates.

 

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215 (3), 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 DOI: https://doi.org/10.1016/S0022-2836(05)80360-2
  2. Alitto, R.A. dos S., Amaral, A.C.Z., de Oliveira, L.D., Serrano, H., Seger, K.R., Guilherme, P.D.B., Di Domenico, M. & Christensenet, A.B. (2019) Atlantic west Ophiothrix spp. in the scope of integrative taxonomy: confirming the existence of Ophiothrix trindadensis Tommasi, 1970. PLoS ONE, 14 (1), e0210331. https://doi.org/10.1371/journal.pone.0210331 DOI: https://doi.org/10.1371/journal.pone.0210331
  3. Bouchet, P., Héros, V., Lozouet, P. & Maestrati, P. (2008) A quarter-century of deep-sea malacological exploration in the South and West Pacific: Where do we stand? How far to go? In: Héros, V., Cowie, R.H. & Bouchet, P. (Eds.), Tropical Deep-Sea Benthos 25. Mémoires du Muséum national d’Histoire naturelle, Paris, 196, pp 9–40.
  4. Buhl-Mortensen, L. & Mortensen, P.B. (2004) Symbiosis in deep-water corals. Symbiosis, 37, 33–61.
  5. Brugler, M.R. & France, S.C. (2008) The Mitochondrial Genome of a Deep-Sea Bamboo Coral (Cnidaria, Anthozoa, Octocorallia, Isididae): Genome Structure and Putative Origins of Replication Are Not Conserved Among Octocorals. Journal of Molecular Evolution, 67, 125–136. https://doi.org/10.1007/s00239-008-9116-2 DOI: https://doi.org/10.1007/s00239-008-9116-2
  6. Cairns, S.D. (2002) A new species of Chrysogorgia (Anthozoa: Octocorallia) from the Atlantic. Proceedings of the Biological Society of Washington, 115 (1), 217–222.
  7. Cairns, S.D. (2007) Studies on western Atlantic Octocorallia (Gorgonacea: Ellisellidae). Part 7: The genera Riisea Duchassaing & Michelotti, 1860 and Nicella Gray, 1870. Proceedings of the Biological Society of Washington, 120 (1), 1–38. https://doi.org/10.2988/0006-324X(2007)120[1:SOWAOG]2.0.CO;2 DOI: https://doi.org/10.2988/0006-324X(2007)120[1:SOWAOG]2.0.CO;2
  8. Cairns, S.D., Stone, R.P., Moon, H.-W. & Lee, J.H. (2018) Primnoidae (Octocorallia: Calcaxonia) from the Emperor Seamounts, with Notes on Callogorgia elegans (Gray, 1870). Pacific Science, 72 (1), 125–142. https://doi.org/10.2984/72.1.8 DOI: https://doi.org/10.2984/72.1.8
  9. Cho, W. & Shank, T.M. (2010) Incongruent patterns of genetic connectivity among four ophiuroid species with differing coral host specificity on North Atlantic seamounts. Marine Ecology, 31 (s1), 121–143. https://doi.org/10.1111/j.1439-0485.2010.00395.x DOI: https://doi.org/10.1111/j.1439-0485.2010.00395.x
  10. Clark, A.H. (1949) Ophiuroidea of the Hawaiian Islands. Bulletin of the Bernice P. Bishop Museum, 195, 3–133.
  11. Dahm, C. (1996) Ecology and Population Dynamics of Antarctic Ophiuroids (Echinodermata). Berichte zur Polarforschung, 194, 1–289. https://doi.org/10.2312/BzP_0194_1996
  12. Dahm, C. & Brey, T. (1998) Determination of Growth and Age of Slow Growing Brittle Stars (Echinodermata: Ophiuroidea) From Natural Growth Bands. Journal of the Marine Biological Association of the United Kingdom, 78 (3), 941–951. https://doi.org/10.1017/S0025315400044891 DOI: https://doi.org/10.1017/S0025315400044891
  13. Ebert, T.A. & Southon, J.R. (2003) Red sea urchins (Strongylocentrotus franciscanus) can live over 100 years: confirmation with A-bomb 14carbon. Fishery Bulletin, 101 (4), 915–922.
  14. Emson, R.H. & Woodley, J.D. (1987) Submersible and laboratory observations on Asteroschema tenue, a long-armed euryaline brittle star epizoic on gorgonians. Marine Biology, 96, 31–45. https://doi.org/10.1007/BF00394836 DOI: https://doi.org/10.1007/BF00394836
  15. Gage, J.D. & Tyler, P.A. (1981) Re-Appraisal of Age Composition, Growth and Survivorship of the Deep-Sea Brittle Star Ophiura ljungmani from Size Structure in a Sample Time Series from the Rockall Trough. Marine Biology, 64, 163–172. https://doi.org/10.1007/BF00397105 DOI: https://doi.org/10.1007/BF00397105
  16. Gage, J.D. & Tyler, P.A. (1982) Growth and reproduction of the deep-sea brittlestar Ophiomusium lymani Wyville Thompson. Oceanologica Acta, 5 (1), 73–84.
  17. Girard, F., Fu, B. & Fisher, C.R. (2016) Mutualistic symbiosis with ophiuroids limited the impact of the Deepwater Horizon oil spill on deep-sea octocorals. Marine Ecology Progress Series, 549, 89–98. https://doi.org/10.3354/meps11697 DOI: https://doi.org/10.3354/meps11697
  18. Grange, K.R. (1991) Mutualism between the Antipatharian Antipathes fiordensis and the Ophiuroid Astrobrachion constrictum in New Zealand Fjords. Hydrobiologia, 216, 297–303. https://doi.org/10.1007/BF00026478 DOI: https://doi.org/10.1007/978-94-011-3240-4_43
  19. Hendler, G. & Tran, L.U. (2001) Reproductive Biology of a Deep-Sea Brittle Star Amphiura carchara (Echinodermata: Ophiuroidea). Marine Biology, 138, 113–123. https://doi.org/10.1007/s002270000446 DOI: https://doi.org/10.1007/s002270000446
  20. Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35 (2), 518–522. https://doi.org/10.1093/molbev/msx281 DOI: https://doi.org/10.1093/molbev/msx281
  21. Kalyaanamoorthy S., Minh, B.Q., Wong, T.K.F., von Haeseler A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285 DOI: https://doi.org/10.1038/nmeth.4285
  22. Katoh, K. & Toh, H. (2008) Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics, 9, 212. https://doi.org/10.1186/1471-2105-9-212 DOI: https://doi.org/10.1186/1471-2105-9-212
  23. Knowlton, N., Brainard, R.E., Fisher, R., Moews, M., Plaisance, L. & Caley, M.J. (2010) Coral Reef Biodiversity. In: McIntyre, A.D. (Ed.) Life in the World’s Oceans: Diversity, Distribution and Abundance. Blackwell Publishing Ltd, pp. 65–78. https://doi.org/10.1002/9781444325508.ch4 DOI: https://doi.org/10.1002/9781444325508.ch4
  24. Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Molecular Biology and Evolution, 37 (5), 1530–1534. https://doi.org/10.1093/molbev/msaa015 DOI: https://doi.org/10.1093/molbev/msaa015
  25. Mortensen, P.B. (2001) Aquarium observations on the deep-water coral Lophelia pertusa (L., 1758) (Scleractinia) and selected associated invertebrates. Ophelia, 54 (2), 83–104. https://doi.org/10.1080/00785236.2001.10409457 DOI: https://doi.org/10.1080/00785236.2001.10409457
  26. Mosher, C.V. & Watling, L. (2009) Partners for Life: A Brittle Star and Its Octocoral Host . Marine Ecology Progress Series, 397, 81–88. https://doi.org/10.3354/meps08113 DOI: https://doi.org/10.3354/meps08113
  27. Nethupul, H., Stöhr, S. & Zhang, H. (2022) Order Euryalida (Echinodermata, Ophiuroidea), new species and new records from the South China Sea and the Northwest Pacific seamounts. ZooKeys, 1090, 161–216. https://doi.org/10.3897/zookeys.1090.76292 DOI: https://doi.org/10.3897/zookeys.1090.76292.figure10
  28. Okanishi, M. & Fujita, T. (2009) A New Species of Asteroschema (Echinodermata: Ophiuroidea: Asteroschematidae) from Southwestern Japan. Species Diversity, 14 (2), 115–129. https://doi.org/10.12782/specdiv.14.115 DOI: https://doi.org/10.12782/specdiv.14.115
  29. Okanishi, M. & Fujita, T. (2013) Molecular Phylogeny Based on Increased Number of Species and Genes Revealed More Robust Family-Level Systematics of the Order Euryalida (Echinodermata: Ophiuroidea). Molecular Phylogenetics and Evolution, 69 (3), 566–580. https://doi.org/10.1016/j.ympev.2013.07.021 DOI: https://doi.org/10.1016/j.ympev.2013.07.021
  30. Okanishi, M. (2016) Euryalida. AccessScience, McGraw-Hill Education, USA. Available from: https://www.accessscience.com/content/euryalida/246500 (accessed 7 August 2023)
  31. Packer, D.B., Watling, L. & Langton, R.W. (1994) The population structure of the brittle star Ophiura sarsi Lutken in the Gulf of Maine and its trophic relationship to American plaice (Hippoglossoides platessoides Fabricius). Journal of Experimental Marine Biology and Ecology, 179 (2), 207–222. https://doi.org/10.1016/0022-0981(94)90115-5 DOI: https://doi.org/10.1016/0022-0981(94)90115-5
  32. Palumbi, S.R. (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis, D., Moritz, C. & Mable, B. (Eds.), Molecular Systematics. 2nd Edition. Sinauer Press, Sunderland, Massachusetts, pp. 205–247.
  33. Pante, E. & France, S.C. (2010) Pseudochrysogorgia bellona n. gen., n. sp.: A new genus and species of chrysogorgiid octocoral (Coelenterata, Anthozoa) from the Coral Sea. Zoosystema, 32 (4), 595–612. https://doi.org/10.5252/z2010n4a4 DOI: https://doi.org/10.5252/z2010n4a4
  34. Pante, E., France, S.C., Couloux, A., Cruaud, C., McFadden, C.S., Samadi, S. & Watling, L. (2012) Deep-sea origin and in-situ diversification of chrysogorgiid octocorals. PLoS One, 7 (6), e38357. https://doi.org/10.1371/journal.pone.0038357 DOI: https://doi.org/10.1371/journal.pone.0038357
  35. Pante, E. & Simon-Bouhet, B. (2013) marmap: a package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS ONE, 8 (9), e73051. https://doi.org/10.1371/journal.pone.0073051 DOI: https://doi.org/10.1371/journal.pone.0073051
  36. Piepenburg, D. & Schmid, M.K. (1996) Brittle star fauna (Echinodermata: Ophiuroidea) of the arctic northwestern Barents sea: composition, abundance, biomass and spatial distribution. Polar Biology, 16, 383–392. https://doi.org/10.1007/BF02390420 DOI: https://doi.org/10.1007/s003000050069
  37. Prouty, N.G., Fisher C.R., Demopoulos, A.W.J. & Druffel, E.R.M. (2016) Growth rates and ages of deep-sea corals impacted by the Deepwater Horizon oil spill. Deep-Sea Research II: Topical Studies in Oceanography, 129, 196–212. https://doi.org/10.1016/j.dsr2.2014.10.021 DOI: https://doi.org/10.1016/j.dsr2.2014.10.021
  38. Quiroga, E. & Sellanes, J. (2009) Growth and size-structure of Stegophiura sp. (Echinodermata: Ophiuroidea) on the continental slope off central Chile: A comparison between cold seep and non-seep sites. Journal of the Marine Biological Association of the United Kingdom, 89 (2), 421–428. https://doi.org/10.1017/S0025315408002786 DOI: https://doi.org/10.1017/S0025315408002786
  39. Ravelo, A.M., Konar, B., Bluhm, B. & Iken, K. (2017) Growth and production of the brittle stars Ophiura sarsii and Ophiocten sericeum (Echinodermata: Ophiuroidea). Continental Shelf Research, 139, 9–20. https://doi.org/10.1016/j.csr.2017.03.011 DOI: https://doi.org/10.1016/j.csr.2017.03.011
  40. R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org/ (accessed 7 August 2023)
  41. Roberts, J.M., Wheeler, A., Freiwald, A. & Cairns, S. (2009) Cold-Water Corals: The Biology and Geology of Deep-Sea Coral Habitats. Cambridge University Press, Cambridge, 334 pp. DOI: https://doi.org/10.1017/CBO9780511581588
  42. Sánchez, J.A., McFadden, C.S., France, S.C. & Lasker, H.R. (2003) Molecular Phylogenetic Analyses of Shallow-Water Caribbean Octocorals. Marine Biology, 142, 975–987. https://doi.org/10.1007/s00227-003-1018-7 DOI: https://doi.org/10.1007/s00227-003-1018-7
  43. Sanvicente-Añorve, L., Solís-Marín, F.A. & Rosales-Contreras, I. (2021) Morphometry and relative growth of Ophiolepis crassa (Echinodermata: Ophiuroidea), a brittle star from the eastern Pacific. Zoological Studies, 60, 26. https://doi.org/10.6620/ZS.2021.60-26
  44. Schindelin, J., Rueden, C.T., Hiner, M.C. & Eliceiri, K.W. (2015) The ImageJ ecosystem: An open platform for biomedical image analysis. Molecular Reproduction and Development, 82 (7–8), 518–529. https://doi.org/10.1002/mrd.22489 DOI: https://doi.org/10.1002/mrd.22489
  45. Stewart, B.G. & Mladenov, P.V. (1997) Population structure, growth and recruitment of the euryalinid brittle-star Astrobrachion constrictum (Echinodermata: Ophiuroidea) in Doubtful Sound, Fiordland, New Zealand. Marine Biology, 127, 687–97. https://doi.org/10.1007/s002270050059 DOI: https://doi.org/10.1007/s002270050059
  46. Stewart, B. (1996) Growth Dynamics of the Radial Shields of the Euryalid Snake Star Astrobrachion constrictum (Echinodermata: Ophiuroidea). Invertebrate Biology, 115 (4), 321–330. https://doi.org/10.2307/3227021 DOI: https://doi.org/10.2307/3227021
  47. Stewart, B. (1998) Can a Snake Star Earn Its Keep? Feeding and Cleaning Behaviour in Astrobrachion constrictum (Farquhar) (Echinodermata: Ophiuroidea), a Euryalid Brittle-Star Living in Association with the Black Coral, Antipathes fiordensis. Journal of Experimental Marine Biology and Ecology, 221 (2), 173–189. https://doi.org/10.1016/S0022-0981(97)00126-3 DOI: https://doi.org/10.1016/S0022-0981(97)00126-3
  48. Vinogradov, G.M. (2000) Growth rate of the colony of a deep-water gorgonarian Chrysogorgia agassizi: In situ observations. Ophelia, 53 (2), 101–103. https://doi.org/10.1080/00785236.2000.10409439 DOI: https://doi.org/10.1080/00785236.2000.10409439
  49. Warner, G.F. (1982) Food and feeding mechanisms: Ophiuroidea. In: Jangoux, M., Lawrence, J. M. (Eds.), Echinoderm nutrition. CRC Press, London, 21 pp. https://doi.org/10.1201/9781003078920-7 DOI: https://doi.org/10.1201/9781003078920-7
  50. Watling, L., France, S.C., Pante, E. & Simpson, A. (2011) Biology of Deep-Water Octocorals. Advances in Marine Biology, 60, 41–122. https://doi.org/10.1016/B978-0-12-385529-9.00002-0 DOI: https://doi.org/10.1016/B978-0-12-385529-9.00002-0