Advertisement

Temperature and salinity survival limits of the fluffy sea anemone, Metridium senile (L.), in Japan

  • Heather GlonEmail author
  • Yamaguchi Haruka
  • Marymegan Daly
  • Masahiro Nakaoka
Primary Research Paper

Abstract

Metridium senile, the fluffy (or plumose) sea anemone, is a circumboreal species adapted to the cold northern oceans. We performed a 40-day experiment on 108 individuals of M. senile collected from the Akkeshi-ko estuary in Japan to test their survivability in higher temperatures and their upper and lower salinity survivability limits. In addition to using survivorship to determine if there is a smaller tolerance range than the extreme limits of temperature and salinity, we used asexual reproduction via pedal laceration as an indicator of the most favorable environmental conditions for M. senile. The resulting limitations are used to both broaden our understanding of the biology of M. senile and to assess potential effects of changing oceanic conditions, since M. senile is unable to survive in warm water temperatures or in extreme salinities. Our results support the use of pedal laceration by M. senile as a way to quickly colonize an area with favorable environmental conditions in order to preserve a well-adapted phenotype.

Keywords

Lethal limits Tolerance Actiniaria Pedal laceration Asexual reproduction 

Notes

Acknowledgements

This project was funded through the East Asia and Pacific Summer Institute program jointly funded by the National Science Foundation (NSF; Award Number 1713898) and the Japan Society for the Promotion of Science (JSPS). This research was also partially supported by the Environmental Research and Technology Development Fund (S-15 Predicting and Assessing Natural Capital and Ecosystem Services [PANCES]) of the Ministry of the Environment, Japan. The authors thank all the Akkeshi Marine Station staff and faculty for assisting them in setting up experiments and for their hospitality. The authors specially thank Mizuho, Ahn-san, Takaaki, and Franz for their continued support during the experiment duration. Finally, they thank Mael Glon for statistics discussions and support at home.

References

  1. Aaron-Morrison, A. P., S. A. Ackerman, N. G. Adams, R. F. Adler, A. Albanil, E. J. Alfaro, R. Allan, L. M. Alves, J. A. Amador, et al., 2017. State of the climate in 2016. Bulletin of the American Meteorological Society 98: S280.Google Scholar
  2. Addison, J. A. & M. W. Hart, 2005. Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution 59: 532–543.PubMedGoogle Scholar
  3. Anthony, K. R. N. & I. Svane, 1995. Effects of substratum instability on locomotion and pedal laceration in Metridium senile (Anthozoa: Actiniaria). Marine Ecology Progress Series 124: 171–180.CrossRefGoogle Scholar
  4. Assis, J., N. C. Coelho, T. Lamy, M. Valero, F. Alberto & E. Á. Serrão, 2016. Deep reefs are climatic refugia for genetic diversity of marine forests. Journal of Biogeography 43: 833–844.CrossRefGoogle Scholar
  5. Ayre, D. J., 1985. Localized adaptation of clones of the sea anemone Actinia Tenebrosa. Evolution 39: 1250–1260.CrossRefGoogle Scholar
  6. Benson-Rodenbough, B. & W. R. Ellington, 1982. Responses of the euryhaline sea anemone Bunodosoma cavernata to osmotic stress. Comparative Biochemistry and Physiology 72: 731–735.CrossRefGoogle Scholar
  7. Bickham, J. W., C. C. Wood & J. C. Patton, 1995. Biogeographic implications of Cytochrome b sequences and allozymes in sockeye (Oncorhynchus nerka). Journal of Heredity 86: 140–144.CrossRefGoogle Scholar
  8. Bucklin, A., 1982. The annual cycle of sexual reproduction in the sea anemone Metridium senile. Canadian Journal of Zoology 60: 3241–3248.CrossRefGoogle Scholar
  9. Bucklin, A., 1987a. Adaptive advantages of patterns of growth and asexual reproduction of the sea anemone Metridium senile (L.) in intertidal and submerged populations. Journal of Experimental Marine Biology and Ecology 110: 225–243.CrossRefGoogle Scholar
  10. Bucklin, A., 1987b. Growth and asexual reproduction of the sea anemone Metridium: comparative laboratory studies of three species. Journal of Experimental Marine Biology and Ecology 110: 41–52.CrossRefGoogle Scholar
  11. Canino, M. F., I. B. Spies, K. M. Cunningham, L. Hauser & W. S. Grant, 2010. Multiple ice-age refugia in Pacific cod, Gadus macrocephalus. Molecular Ecology 19: 4339–4351.CrossRefGoogle Scholar
  12. Carlgren, O., 1933. Zoantharia and Actiniaria. The Godthaab Expedition 1928. Meddelelser om Gronland 79: 1–55.Google Scholar
  13. Carlgren, O., 1949. A survey of the Ptychodactiaria, Corallimorpharia and Actiniaria. Kungliga Svenska Vetenskapsakademiens Handlingar 3: 1–121.Google Scholar
  14. Clarke, A., 1983. Life in cold water: the physiological ecology of polar marine ectotherms. Oceanography Marine Biological Annual Review 21: 341–453.Google Scholar
  15. Crisp, D. J., 1964. The effects of the severe winter of 1962-63 on marine life in Britain. Journal of Animal Ecology 33: 165–210.CrossRefGoogle Scholar
  16. Deaton, L. E. & R. J. Hoffmann, 1988. Hypoosmotic volume regulation in the sea anemone Metridium senile. Comparative Biochemistry and Physiology 91: 187–191.Google Scholar
  17. Fautin, D. G., 2016. Catalog to families, genera, and species of orders Actiniaria and Corallimorpharia (Cnidaria: Anthozoa). Zootaxa 4145: 1–449.CrossRefGoogle Scholar
  18. Fox, D. L. & C. F. A. Pantin, 1941. The colours of the plumose anemone Metridium senile (L.). Philosophical Transactions of the Royal Society B: Biological Sciences 230: 415–450.CrossRefGoogle Scholar
  19. Gemmill, J. F., 1920. The development of the sea-anemones Metridium dianthus (Ellis) and Adamsia palliata. Philosophical Transactions of the Royal Society of London 209: 351–375.CrossRefGoogle Scholar
  20. Griffiths, C. L., L. M. Kruger & C. E. Smith, 1996. First record of the sea anemone Metridium senile from South Africa. South African Journal of Zoology 31: 157–158.CrossRefGoogle Scholar
  21. Hand, C., 1955. The sea anemones of central California Part III. The Acontiarian Anemones. The Wasmann Journal of Biology 13: 189–251.Google Scholar
  22. Hellberg, M. E., 2007. Footprints on water the genetic wake of dispersal among reefs. Coral Reefs 26(3): 463–473.CrossRefGoogle Scholar
  23. Hewitt, G. M., 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58: 247–276.CrossRefGoogle Scholar
  24. Hewitt, G. M., 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.CrossRefGoogle Scholar
  25. Hoffmann, R. J., 1976. genetics and asexual reproduction of the sea anemone Metridium senile. Biological Bulletin 151: 478–488.CrossRefGoogle Scholar
  26. Hoffmann, R. J., 1986. Variation in contributions of asexual reproduction to the genetic structure of populations of the sea anemone Metridium senile. Evolution 40: 357–365.CrossRefGoogle Scholar
  27. Hoffmann, R. J., 1987. Short-term stability of genetic structure in populations of sea anemone. Marine Biology 93: 499–507.CrossRefGoogle Scholar
  28. Holder, K., R. Montgomerie & V. L. Friesen, 1999. A test of the glacial refugium hypothesis using patterns of mitochondrial and nuclear DNA sequence variation in rock ptarmigan (Lagopus mutus). Evolution 53: 1936–1950.PubMedGoogle Scholar
  29. Hooper, S. N. & R. G. Ackman, 1971. Trans-6-hexadecenoic acid and the corresponding alcohol in lipids in the sea anemone Metridium dianthus. Lipids 6: 341–346.CrossRefGoogle Scholar
  30. Hughes, R. N. & J. M. Cancino, 1985. An Ecological Overview of Cloning in Metazoa. In Jackson, J. B. C., L. W. Buss & R. E. Cook (eds), Population Biology and Evolution of Clonal Organisms. Yale University Press, New Haven.Google Scholar
  31. Hutchins, M., D. A. Thoney & N. Schlager, 2003. Frilled Anemone. Grzimek’s Animal Life Encyclopedia. Lower Metazoans and Lesser Deuterostomes. Gale Group, Farming Hills: 112–113.Google Scholar
  32. Ingolfsson, A., 1992. The Origin of the Rocky Shore Fauna of Iceland and the Canadian Maritimes. Journal of Biogeography 19: 705–712.CrossRefGoogle Scholar
  33. Johnson, L. & J. M. Shick, 1977. Effects of fluctuating temperature and immersion on asexual reproduction in the intertidal sea anemone Haliplanella luciae (Verrill) in laboratory culture. Journal of Experimental Marine Biology and Ecology 28: 141–149.CrossRefGoogle Scholar
  34. Kasim, M. & H. Mukai, 2006. Contribution of benthic and epiphytic diatoms to clam and oyster production in the Akkeshi-ko estuary. Journal of Oceanography 62: 267–281.CrossRefGoogle Scholar
  35. Khalaman, V. V., 2001. Fouling communities of mussel aquaculture installations in the White Sea. Russian Journal of Marine Biology 27: 227–237.CrossRefGoogle Scholar
  36. Laird, M. C. & C. L. Griffiths, 2016. Additions to the South African sea anemone (Cnidaria, Actiniaria) fauna, with expanded distributional ranges for known species. African Invertebrates 57: 15–37.CrossRefGoogle Scholar
  37. Lasker, H. R. & M. A. Coffroth, 1999. Responses of clonal reef taxa to environmental change. American Zoologist 39: 92–103.CrossRefGoogle Scholar
  38. Lee, K. M., E. C. Yang, J. A. Coyer, G. C. Zuccarello, W. L. Wang, C. G. Choi & S. M. Boo, 2012. Phylogeography of the seaweed Ishige okamurae (Phaeophyceae): evidence for glacial refugia in the northwest Pacific region. Marine Biology 159: 1021–1028.CrossRefGoogle Scholar
  39. Lombardi, M. R. & M. P. Lesser, 2010. The annual gametogenic cycle of the sea anemone Metridium senile from the Gulf of Maine. Journal of Experimental Marine Biology and Ecology 390: 58–64.CrossRefGoogle Scholar
  40. Maggs, C. A. C., R. Castilho, D. Foltz, C. Henzler, M. T. Jolly, J. Kelly, J. Olsen, K. E. Perez, W. Stam, R. Väinölä, F. Viard & J. Wares, 2008. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89: S108–S122.CrossRefGoogle Scholar
  41. Martin, J. P., A. Garese, A. Sar & F. H. Acuña, 2015. Fouling community dominated by Metridium senile (Cnidaria: Anthozoa: Actiniaria) in Bahia San Julian (Southern Patagonia, Argentina). Scientia Marina 79: 211–221.CrossRefGoogle Scholar
  42. Nelson, M. L. & S. F. Craig, 2011. Role of the sea anemone Metridium senile in structuring a developing subtidal fouling community. Marine Ecology Progress Series 421: 139–149.CrossRefGoogle Scholar
  43. Peltier, W. R., 2004. Global glacial isostasy and the surface of the Ice-Age Earth: the ICE-5G (VM2) model and GRACE. Annual Review of Earth and Planetary Sciences 32: 111–149.CrossRefGoogle Scholar
  44. Pierce, S. K. & L. L. Minasian, 1974. Water balance of a euryhaline sea anemone Diadumene leucolena. Comparative Biochemistry and Physiology 49: 159–167.CrossRefGoogle Scholar
  45. Provan, J. & K. D. Bennett, 2008. Phylogeographic insights into cryptic glacial refugia. Trends in Ecology and Evolution 23: 564–571.CrossRefGoogle Scholar
  46. Rawlinson, R., 1934. A comparativestudy of Metridium senile (L.) var. dianthus (Ellis) and a dwarf variety of this species occurring in the River Mersey, with a discussion on the systematic position of the genus Metridium. Journal of the Marine Biological Association of the United Kingdom 19: 901–920.CrossRefGoogle Scholar
  47. Sassaman, C. & C. P. Mangum, 1970. Patterns of temperature adaptation in North American Atlantic coastal actinians. Marine Biology 7: 123–130.CrossRefGoogle Scholar
  48. Seeb, L. W. & P. A. Crane, 1999. High genetic heterogeneity in chum salmon in western Alaska, the contact zone between northern and southern lineages. Transactions of the American Fisheries Society 128: 58–87.CrossRefGoogle Scholar
  49. Shafer, A. B. A., C. I. Cullingham, S. D. Côté & D. W. Coltman, 2010. Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Molecular Ecology 19: 4589–4621.CrossRefGoogle Scholar
  50. Shick, J. M., 1976. Ecological physiology and genetics of the colonizing actinian Haliplanella luciae. In Mackie, G. O. (ed.), Coelenterate Ecology and Behavior. Springer, Boston: 137–146.CrossRefGoogle Scholar
  51. Shick, J. M., 1991. A Functional Biology of Sea Anemones. Chapman & Hall, London.CrossRefGoogle Scholar
  52. Shick, J. M. & A. N. Lamb, 1977. Asexual reproduction and genetic population structure in the colonizing sea anemone Haliplanella luciae. Biological Bulletin 153: 604–617.CrossRefGoogle Scholar
  53. Shick, J. M., R. Hoffmann & A. Lamb, 1979. Asexual reproduction, population structure, and genotype-environment interactions in sea anemones. American Zoologist 713: 699–713.CrossRefGoogle Scholar
  54. Shumway, S. E., 1978. Activity and respiration in the anemone, Metridium senile (L.) exposed to salinity fluctuations. Journal of Experimental Marine Biology and Ecology 33: 85–92.CrossRefGoogle Scholar
  55. Stephenson, T. A., 1935. The British Sea Anemones, Vol. 2. The Ray Society, London: 429.Google Scholar
  56. Tsukada, M., 1983. Vegetation and climate during the Last Glacial in Japan. Quaternary Research 19: 212–235.CrossRefGoogle Scholar
  57. Uchida, T., 1932. Occurrence in Japan of Diadumene luciae, a remarkable actinian of rapid dispersal. Journal of the Faculty of Science Hokkaido Imperial University 2: 69–82.Google Scholar
  58. Uchida, T., 1940. The Fauna of Akkeshi Bay. Journal of the Faculty of Science Hokkaido Imperial University 7: 265–275.Google Scholar
  59. Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S. Springer, New York.CrossRefGoogle Scholar
  60. Wahl, M., 1984. The fluffy sea anemone Metridium senile in periodically oxygen depleted surroundings. Marine Biology 86: 81–86.CrossRefGoogle Scholar
  61. Wahl, M., 1985. Metridium senile: dispersion and small scale colonization by the combined strategy of locomotion and asexual reproduction (laceration). Marine Ecology Progress Series 26: 271–277.CrossRefGoogle Scholar
  62. Walsh, P. J. & G. N. Somero, 1981. Temperature adaptation in sea-anemones - physiological and biochemical variability in geographically separate populations of Metridium senile. Marine Biology 62: 25–34.CrossRefGoogle Scholar
  63. Wares, J. P. & C. W. Cunningham, 2001. Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55: 2455–2469.CrossRefGoogle Scholar
  64. Yamada, K., M. Hori, Y. Tanaka, N. Hasegawa & M. Nakaoka, 2007. Temporal and spatial macrofaunal community changes along a salinity gradient in seagrass meadows of Akkeshi-ko estuary and Akkeshi Bay, Northern Japan. Hydrobiologia 592: 345–358.CrossRefGoogle Scholar
  65. Young, A. M., C. Torres, J. E. Mack & C. W. Cunningham, 2002. Morphological and genetic evidence for vicariance and refugium in Atlantic and Gulf of Mexico populations of the hermit crab Pagurus longicarpus. Marine Biology 140: 1059–1066.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Evolution, Ecology, and Organismal BiologyThe Ohio State UniversityColumbusUSA
  2. 2.Akkeshi Marine Station, Field Science Center for Northern BiosphereHokkaido UniversityAkkeshiJapan

Personalised recommendations