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

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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.

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References

  • 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 

  • Addison, J. A. & M. W. Hart, 2005. Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution 59: 532–543.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ayre, D. J., 1985. Localized adaptation of clones of the sea anemone Actinia Tenebrosa. Evolution 39: 1250–1260.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bucklin, A., 1982. The annual cycle of sexual reproduction in the sea anemone Metridium senile. Canadian Journal of Zoology 60: 3241–3248.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Carlgren, O., 1933. Zoantharia and Actiniaria. The Godthaab Expedition 1928. Meddelelser om Gronland 79: 1–55.

    Google Scholar 

  • Carlgren, O., 1949. A survey of the Ptychodactiaria, Corallimorpharia and Actiniaria. Kungliga Svenska Vetenskapsakademiens Handlingar 3: 1–121.

    Google Scholar 

  • Clarke, A., 1983. Life in cold water: the physiological ecology of polar marine ectotherms. Oceanography Marine Biological Annual Review 21: 341–453.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Fautin, D. G., 2016. Catalog to families, genera, and species of orders Actiniaria and Corallimorpharia (Cnidaria: Anthozoa). Zootaxa 4145: 1–449.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hand, C., 1955. The sea anemones of central California Part III. The Acontiarian Anemones. The Wasmann Journal of Biology 13: 189–251.

    Google Scholar 

  • Hellberg, M. E., 2007. Footprints on water the genetic wake of dispersal among reefs. Coral Reefs 26(3): 463–473.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hewitt, G. M., 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.

    Article  CAS  Google Scholar 

  • Hoffmann, R. J., 1976. genetics and asexual reproduction of the sea anemone Metridium senile. Biological Bulletin 151: 478–488.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hoffmann, R. J., 1987. Short-term stability of genetic structure in populations of sea anemone. Marine Biology 93: 499–507.

    Article  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • Ingolfsson, A., 1992. The Origin of the Rocky Shore Fauna of Iceland and the Canadian Maritimes. Journal of Biogeography 19: 705–712.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Khalaman, V. V., 2001. Fouling communities of mussel aquaculture installations in the White Sea. Russian Journal of Marine Biology 27: 227–237.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lasker, H. R. & M. A. Coffroth, 1999. Responses of clonal reef taxa to environmental change. American Zoologist 39: 92–103.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pierce, S. K. & L. L. Minasian, 1974. Water balance of a euryhaline sea anemone Diadumene leucolena. Comparative Biochemistry and Physiology 49: 159–167.

    Article  CAS  Google Scholar 

  • Provan, J. & K. D. Bennett, 2008. Phylogeographic insights into cryptic glacial refugia. Trends in Ecology and Evolution 23: 564–571.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Sassaman, C. & C. P. Mangum, 1970. Patterns of temperature adaptation in North American Atlantic coastal actinians. Marine Biology 7: 123–130.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Shick, J. M., 1991. A Functional Biology of Sea Anemones. Chapman & Hall, London.

    Book  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Shick, J. M., R. Hoffmann & A. Lamb, 1979. Asexual reproduction, population structure, and genotype-environment interactions in sea anemones. American Zoologist 713: 699–713.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Stephenson, T. A., 1935. The British Sea Anemones, Vol. 2. The Ray Society, London: 429.

    Google Scholar 

  • Tsukada, M., 1983. Vegetation and climate during the Last Glacial in Japan. Quaternary Research 19: 212–235.

    Article  Google Scholar 

  • 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 

  • Uchida, T., 1940. The Fauna of Akkeshi Bay. Journal of the Faculty of Science Hokkaido Imperial University 7: 265–275.

    Google Scholar 

  • Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S. Springer, New York.

    Book  Google Scholar 

  • Wahl, M., 1984. The fluffy sea anemone Metridium senile in periodically oxygen depleted surroundings. Marine Biology 86: 81–86.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Wares, J. P. & C. W. Cunningham, 2001. Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55: 2455–2469.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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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.

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Authors and Affiliations

  1. Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, OH, USA

    Heather Glon & Marymegan Daly

  2. Akkeshi Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Akkeshi, Japan

    Yamaguchi Haruka & Masahiro Nakaoka

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  1. Heather Glon
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  2. Yamaguchi Haruka
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  3. Marymegan Daly
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  4. Masahiro Nakaoka
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Correspondence to Heather Glon.

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Glon, H., Haruka, Y., Daly, M. et al. Temperature and salinity survival limits of the fluffy sea anemone, Metridium senile (L.), in Japan. Hydrobiologia 830, 303–315 (2019). https://doi.org/10.1007/s10750-018-3879-2

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