Marine Biology

, Volume 156, Issue 9, pp 1797–1808

Effect of acclimatization to low temperature and reduced light on the response of reef corals to elevated temperature

Original Paper

Abstract

This study tested the effects of acclimatization on the response of corals to elevated temperature, using juvenile massive Porites spp. and branching P. irregularis from Moorea (W149°50′, S17°30′). During April and May 2006, corals were acclimatized for 15 days to cool (25.7°C) or ambient (27.7°C) temperature, under shaded (352 μmol photons m−2 s−1) or ambient (554 μmol photons m−2 s−1) natural light, and then incubated for 7 days at ambient or high temperature (31.1°C), under ambient light (659 μmol photons m−2 s−1). The response to acclimatization was assessed as biomass, maximum dark-adapted quantum yield of PSII (Fv/Fm), and growth, and the effect of the subsequent treatment was assessed as Fv/Fm and growth. Relative to the controls (i.e., ambient temperature/ambient light), massive Porites spp. responded to acclimatization through increases in biomass under ambient temperature/shade, and low temperature/ambient light, whereas P. irregularis responded through reduced growth under ambient temperature/shade, and low temperature/ambient light. Acclimatization affected the response to thermal stress for massive Porites spp. (but not P. irregularis), with an interaction between the acclimatization and subsequent treatments for growth. This interaction resulted from a lessening of the negative effects of high temperature after acclimatizing to ambient temperature/shade, but an accentuation of the effect after acclimatizing to low temperature/shade. It is possible that changes in biomass for massive Porites spp. are important in modulating the response to high temperature, with the taxonomic variation in this effect potentially resulting from differences in morphology. These results demonstrate that corals can acclimatize during short exposures to downward excursions in temperature and light, which subsequently affects their response to thermal stress. Moreover, even con-generic taxa differ in this capacity, which could affect coral community structure.

Supplementary material

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Supplementary figure (DOC 48 kb)
227_2009_1213_MOESM2_ESM.doc (97 kb)
Supplementary figure (DOC 97 kb)
227_2009_1213_MOESM3_ESM.doc (82 kb)
Supplementary figure (DOC 82 kb)

References

  1. Anthony KRN, Hoegh-Guldberg O (2003) Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: an analogue to plants in forest gaps and understoreys? Funct Ecol 17:246–259CrossRefGoogle Scholar
  2. Anthony KRN, Connolly SR, Willis BL (2002) Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol Oceangr 47:1417–1429CrossRefGoogle Scholar
  3. Baker AC (2004) Symbiont diversity on coral reefs and relationship to bleaching resistance. In: Rosenberg E, Loya Y (eds) Coral health and diseases. Springer, Berlin, pp 177–194Google Scholar
  4. Berkelmans R, Willis BL (1999) Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore central Great Barrier Reef. Coral Reefs 18:219–228CrossRefGoogle Scholar
  5. Bowler K (2005) Acclimation, heat shock and hardening. J Therm Biol 30:125–130CrossRefGoogle Scholar
  6. Brown BE, Dunne RP, Ambarsari I, Le Tissier MDA, Satapoomin U (1999) Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar Ecol Prog Ser 191:53–69CrossRefGoogle Scholar
  7. Brown BE, Dunne RP, Goodson MS, Douglas AE (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21:119–126Google Scholar
  8. Buddemeier RW, Kinzie RA (1976) Coral growth. Ocean Mar Biol Ann Rev 14:183–225Google Scholar
  9. Buddemeier RW, Baker AC, Fautin DG, Jacobs JB (2004) The adaptive hypothesis of bleaching. In: Rosenberg E, Loya Y (eds) Coral health and diseases. Springer, Berlin, pp 1427–1444Google Scholar
  10. Castillo KD, Helmuth BST (2005) Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Mar Biol 148:261–270CrossRefGoogle Scholar
  11. Coles SL, Brown BE (2003) Coral bleaching—capacity for acclimatization and adaptation. Adv Mar Biol 46:183–223PubMedCrossRefGoogle Scholar
  12. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216CrossRefGoogle Scholar
  13. Coles SL, Jokiel PL (1978) Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar Biol 49:187–195CrossRefGoogle Scholar
  14. Dana JD (1846) Zoophytes. US Explor Exped 1838–1842 7:1–740Google Scholar
  15. Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  16. Day TL, Nagel L, van Oppen MJH, Caley MJ (2008) Factors affecting the evolution of bleaching resistance in corals. Am Nat 171:72–88CrossRefGoogle Scholar
  17. Dove SG, Hoegh-Guldberg O (2006) The cell physiology of coral bleaching. In: Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. American Geophysical Union, Washington, pp 55–71Google Scholar
  18. Edmunds PJ (2004) Juvenile coral populations track rising seawater temperature on a Caribbean reef. Mar Ecol Prog Ser 269:111–119CrossRefGoogle Scholar
  19. Edmunds PJ (2005) The effect of sub-lethal increases in temperature on the growth and population trajectories of three scleractinian corals on the southern Great Barrier Reef. Oecologia 146:350–364PubMedCrossRefGoogle Scholar
  20. Edmunds PJ (2006) Temperature- mediated transitions between isometry and allometry in a colonial, modular invertebrate. Proc R Soc B 273:2275–2281PubMedCrossRefGoogle Scholar
  21. Edmunds PJ (2008) The effects of temperature on the growth of juvenile scleractinian corals. Mar Biol 154:153–162CrossRefGoogle Scholar
  22. Edmunds PJ, Gates RD (2008) Acclimatization in tropical reef corals. Mar Ecol Prog Ser 361:307–310CrossRefGoogle Scholar
  23. Edmunds PJ, Spencer-Daves P (1986) An energy budget for Porites porites (Scleractinia). Mar Biol 92:339–347CrossRefGoogle Scholar
  24. Edwards H, Haime JM (1860) Histoire naturelle des Coralliaires. Librairie Encyclopédique de Roret, Paris, vol 1, 2, 3, pp 1–326, 1–632, 1–560Google Scholar
  25. Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174CrossRefGoogle Scholar
  26. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685Google Scholar
  27. Forskål P (1775) Descriptiones Animalium, Avium, Amphibiorium, Piscium, Insectorum, Vermium que in intinere orientali observavit Petrus Forskål. IV Corallia. Hauniae, pp 131–139Google Scholar
  28. Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43Google Scholar
  29. Gorbunov MY, Kolber SZ, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46:75–85Google Scholar
  30. Gould SJ, Lloyd EA (1997) Individuality and adaptation across levels of selection: how shall we name and generalize the unit of Darwinism? Proc Natl Acad Sci USA 96:11904–11909CrossRefGoogle Scholar
  31. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189PubMedCrossRefGoogle Scholar
  32. Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42PubMedGoogle Scholar
  33. Hoegh-Guldberg OM, Fine M, Skirving W, Johnson R, Dove S, Strong A (2005) Coral bleaching following wintry weather. Limnol Oceanogr 50:265–271Google Scholar
  34. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  35. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305PubMedCrossRefGoogle Scholar
  36. Jokiel PL (2004) Temperature stress and coral bleaching. In: Rosenberg E, Loya Y (eds) Coral health and diseases. Springer, Berlin, pp 401–425Google Scholar
  37. Jokiel PL, Coles SL (1977) Effects of temperature on the mortality and growth of Hawaiin reef corals. Mar Biol 43:201–208CrossRefGoogle Scholar
  38. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Scheiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  39. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc B 275:1359–1365PubMedCrossRefGoogle Scholar
  40. Leichter JJ, Helmuth BST, Fisher AM (2006) Variation beneath the surface: quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida. J Mar Res 64:563–588CrossRefGoogle Scholar
  41. Levy O, Mizrah L, Chadwick-Furman NE, Achituv Y (2001) Factors controlling the expansion behavior of Favia favus (Cnidaria: Scleractinia): effects of light, flow, and planktonic prey. Biol Bull 200:118–126PubMedCrossRefGoogle Scholar
  42. Link HT (1807) Beschreibung der Naturalien Sammlungen der Universitat zu Rostock 3:161–165Google Scholar
  43. Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  44. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  45. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056PubMedCrossRefGoogle Scholar
  46. Mumby PJ, Chisholm JRM, Edwards AJ, Andrefout S, Jaubert J (2001) Cloudy weather may have saved Society Island coral reefs during the 1998 ENSO event. Mar Ecol Prog Ser 222:209–216CrossRefGoogle Scholar
  47. Muscatine L, Grossman D, Doino J (1991) Release of symbiotic algae by tropical sea anemones and corals after cold shock. Mar Ecol Prog Ser 77:233–243CrossRefGoogle Scholar
  48. Nakamura T, van Woesik R (2001) Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar Ecol Prog Ser 212:301–304CrossRefGoogle Scholar
  49. Porter JW, Lewis SK, Porter KG (1999) The effects of multiple stressors on the Florida Keys coral reef ecosystem: a landscape hypothesis and a physiological test. Limnol Oceanogr 44:941–949Google Scholar
  50. Quelch JJ (1884) Preliminary notice of new genera and species of Challenger reef corals. Ann Mag Nat Hist 13:292–297Google Scholar
  51. Quinn GP, Keough MJ (2003) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  52. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  53. Suwa R, Hirosa M, Hidaka M (2008) Seasonal fluctuation in zooxanthellar genotype composition and photophysiology in the corals Pavona divaricata and P. decussata. Mar Ecol Prog Ser 361:129–137CrossRefGoogle Scholar
  54. Tchernov D, Gorbunov MY, Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535PubMedCrossRefGoogle Scholar
  55. Vaughan TW (1918) Some shoal-water corals from Murray Islands, Cocos-Keeling Islands and Fanning Island. Pap Dept Mar Biol Carnegie Inst Wash 9:51–243Google Scholar
  56. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012PubMedCrossRefGoogle Scholar
  57. Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Mar Biol 141:31–38CrossRefGoogle Scholar
  58. Wethey DS, Porter JW (1976) Sun and shade differences in productivity of reef corals. Nature 262:281–282CrossRefGoogle Scholar
  59. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of BiologyCalifornia State UniversityNorthridgeUSA

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