Marine Biology

, Volume 161, Issue 8, pp 1745–1754 | Cite as

Vertical zonation of endosymbiotic zooxanthellae within a population of the intertidal sea anemone, Anthopleura uchidai

  • Osamu MiuraEmail author
  • Teeyaporn Keawtawee
  • Nobuko Sato
  • Ken-ichi Onodera
Original Paper


Intertidal organisms commonly form zonation bands along the shore. Environmental stressors often determine the vertical position of each zonation band. These stressors may similarly affect the distribution pattern of endogenous species in their intertidal hosts. To evaluate this possibility, we investigated the distribution pattern of endosymbiotic zooxanthellae in the genus Symbiodinium in a population of the intertidal sea anemone Anthopleura uchidai. We used molecular genetics to identify the Symbiodinium clades and found that A. uchidai has two clades of Symbiodinium, clades A and F. These Symbiodinium clades were disproportionally distributed along the vertical gradient of the intertidal shore. Anemones on the upper shore exclusively possessed clade F Symbiodinium while clade A Symbiodinium became dominant in the sea anemones on the lower shore. Photosynthesis activity assays showed that these Symbiodinium clades had similar net productivities at 23.3 and 31.8 °C at all irradiance levels. At 35 °C, however, clade A Symbiodinium exhibited substantially lower net productivities than clade F Symbiodinium, demonstrating that these Symbiodinium clades have distinct tolerances to thermal stress. These results suggest that the thermal gradient across tidal height is a major factor shaping the zonation pattern of Symbiodinium clades in A. uchidai.


Photosynthetically Active Radiation Zonation Pattern Depth Gradient Infected Snail RFLP Pattern 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank K. Fukami for his valuable comments on this study. We also thank Y. Kumekawa, K. Matsuyama, K. Ohga, N. Yokoyama for their field assistance, and C. Keogh for English editing. Two anonymous reviewers provided useful comments. This study was performed through the Program to Disseminate Tenure Tracking System of the Ministry of Education, Culture, Sports, Science and Technology, the Japanese Government.


  1. Bates A (2000) The intertidal distribution of two algal symbionts hosted by Anthopleura xanthogrammica (Brandt 1835). J Exp Mar Biol Ecol 249:249–262CrossRefGoogle Scholar
  2. Chavanich S, Wilson KA (2000) Rocky intertidal zonation of gammaridean amphipods in Long Island Sound, Connecticut. Crustaceana 73:835–846CrossRefGoogle Scholar
  3. Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Syst 3:169–192CrossRefGoogle Scholar
  4. Curtis LA (1987) Vertical distribution of an estuarine snail altered by a parasite. Science 235:1508–1511CrossRefGoogle Scholar
  5. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  6. Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263CrossRefGoogle Scholar
  7. Geller JB, Walton ED (2001) Breaking up and getting together: evolution of symbiosis and cloning by fission in sea anemones (genus Anthopleura). Evolution 55:1781–1794CrossRefGoogle Scholar
  8. Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallidal Symbiodinium symbiosis. Limnol Oceanogr 50:1490–1498CrossRefGoogle Scholar
  9. Haylor GS, Thorpe JP, Carter MA (1984) Genetic and ecological differentiation between sympatric colour morphs of the common intertidal sea anemone Actinia equina. Mar Ecol Prog Ser 16:281–289CrossRefGoogle Scholar
  10. Jones A, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE 5:e10437CrossRefGoogle Scholar
  11. Kemp D, Fitt W, Schmidt G (2008) A microsampling method for genotyping coral symbionts. Coral Reefs 27:289–293CrossRefGoogle Scholar
  12. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  13. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800CrossRefGoogle Scholar
  14. LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol 48:1380–1391CrossRefGoogle Scholar
  15. Lewis JR (1978) The ecology of rocky shores. Hodder and Stoughton, LondonGoogle Scholar
  16. Little AF, Van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494CrossRefGoogle Scholar
  17. Luckens PA (1975) Competition and intertidal zonation of barnacles at Leigh, New Zealand. N Z J Mar Freshwat Res 9:379–394CrossRefGoogle Scholar
  18. Miura O, Chiba S (2007) Effects of trematode double infection on the shell size and distribution of snail hosts. Parasitol Int 56:19–22CrossRefGoogle Scholar
  19. Miura O, Kuris AM, Torchin ME, Hechinger RF, Chiba S (2006) Parasites alter host phenotype and may create a new ecological niche for snail hosts. Proc R Soc Lond B 273:1323–1328CrossRefGoogle Scholar
  20. Monteiro FA, Solé-Cava AM, Thorpe JP (1997) Extensive genetic divergence between populations of the common intertidal sea anemone Actinia equina from Britain, the Mediterranean and the Cape Verde Islands. Mar Biol 129:425–433CrossRefGoogle Scholar
  21. Mortain-Bertrand A, Descolas-Gros C, Jupin H (1988) Growth, photosynthesis and carbon metabolism in the temperate marine diatom Skeletonema costatum adapted to low temperature and low photon-flux density. Mar Biol 100:135–141CrossRefGoogle Scholar
  22. Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:101–117Google Scholar
  23. Ottaway JR (1973) Some effects of temperature, desiccation, and light on the intertidal anemone, Actinia tenebrosa Farquhar (Cnidaria: Anthozoa). Aust J Mar Freshw Res 24:103–126CrossRefGoogle Scholar
  24. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701Google Scholar
  25. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogen Evol 56:492–497CrossRefGoogle Scholar
  26. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078CrossRefGoogle Scholar
  27. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (pyrrhophyta). J Phycol 42:568–579CrossRefGoogle Scholar
  28. Rodriguez-Lanetty M, Chang SJ, Song JI (2003) Specificity of two temperate dinoflagellate–anthozoan associations from the north-western Pacific Ocean. Mar Biol 143:1193–1199CrossRefGoogle Scholar
  29. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853CrossRefGoogle Scholar
  30. Sall J, Creighton L, Lehman A (2007) JMP start statistics: a guide to statistics and data analysis using JMP. SAS Institute Inc., CaryGoogle Scholar
  31. Schama R, Solé-Cava AM, Thorpe JP (2005) Genetic divergence between east and west Atlantic populations of Actinia spp. sea anemones (Cnidaria: Actiniidae). Mar Biol 146:435–443CrossRefGoogle Scholar
  32. Secord D, Augustine L (2000) Biogeography and microhabitat variation in temperate algal-invertebrate symbioses: zooxanthellae and zoochlorellae in two Pacific intertidal sea anemones, Anthopleura elegantissima and A. xanthogrammica. Invertebr Biol 119:139–146CrossRefGoogle Scholar
  33. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789CrossRefGoogle Scholar
  34. Sotka EE, Thacker RW (2005) Do some corals like it hot? Trends Ecol Evol 20:59–62CrossRefGoogle Scholar
  35. Stephenson TA, Stephenson A (1949) The universal features of zonation between tide-marks on rocky coasts. J Ecol 37:289–305CrossRefGoogle Scholar
  36. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956CrossRefGoogle Scholar
  37. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  38. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  39. Uchida H, Soyama I (2001) Sea anemones in Japanese waters. TBS Britannica, TokyoGoogle Scholar
  40. Underwood AJ (1973) Studies on zonation of intertidal prosobranch molluscs in the Plymouth region. J Anim Ecol 42:353–372CrossRefGoogle Scholar
  41. Underwood AJ (1975) Intertidal zonation of prosobranch gastropods: analysis of densities of four co-existing species. J Exp Mar Biol Ecol 19:197–216CrossRefGoogle Scholar
  42. Venn AA, Loram JE, Trapido-Rosenthal HG, Joyce DA, Douglas AE (2008) Importance of time and place: patterns in abundance of Symbiodinium clades A and B in the tropical sea anemone Condylactis gigantea. Biol Bull 215:243–252CrossRefGoogle Scholar
  43. Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol Oceanogr 51:1887–1897CrossRefGoogle Scholar
  44. Yamada SB, Boulding EG (1996) The role of highly mobile crab predators in the intertidal zonation of their gastropod prey. J Exp Mar Biol Ecol 204:59–83CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Osamu Miura
    • 1
    Email author
  • Teeyaporn Keawtawee
    • 2
  • Nobuko Sato
    • 1
  • Ken-ichi Onodera
    • 3
  1. 1.Oceanography Section, Science Research CenterKochi UniversityKochiJapan
  2. 2.Department of Aquatic Science, Faculty of Natural ResourcesPrince of Songkla UniversityHat YaiThailand
  3. 3.Oceanography Section, Science Research CenterKochi UniversityKochiJapan

Personalised recommendations