Marine Biology

, Volume 161, Issue 7, pp 1531–1542

Is acclimation beneficial to scleractinian corals, Porites spp.?

Original Paper

Abstract

With coral reefs impacted by climate change, attention is turning to the extent to which scleractinian corals can acclimatize to new physical conditions. The implicit assumption that acclimatization is beneficial has not been tested for scleractinians, although it has been investigated in other systems and has been referred to as the beneficial acclimation hypothesis (BAH). This study tests this hypothesis for scleractinians in experiments on massive Porites spp. from Moorea, French Polynesia (17° 28.564S, 149° 49.018 W). Corals were acclimated for 15–21 days to three temperatures within the range experienced in the collection habitat and then transferred to each of the same temperatures for a treatment period of 14–15 days. The response of the holobiont was measured as growth, the response of the Symbiodinium populations as maximum photochemical efficiency of open reaction centers II (Fv/Fm). An ANOVA with polynomial contrasts was used to distinguish among the BAH, three alternative hypotheses and a null hypothesis describing the consequences of acclimation. In the first experiment (2009), massive Porites spp. were unresponsive to temperature. In the second experiment (2013), the BAH was not supported, but growth of the holobiont conformed to the “hotter is better” (HIB) hypothesis; the response of Symbiodinium populations conformed to developmental buffering. These results suggest that acclimation by massive Porites spp. to temperatures experienced routinely in the natural environment does not have clear beneficial value for growth or photochemical efficiency (i.e., BAH was not supported), but they reveal that acclimation to increased temperature can have value in responding to a variety of subsequent temperatures (i.e., support for HIB).

References

  1. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  2. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253CrossRefGoogle Scholar
  3. Anthony KRN, Hoegh-Guldberg O (2003) Kinetics of photoacclimation in corals. Oecologia 134:23–31CrossRefGoogle Scholar
  4. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2012) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA 110:1387–1392CrossRefGoogle Scholar
  5. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc B 273:2305–2312CrossRefGoogle Scholar
  6. Birkeland C (1976) An experimental method of studying corals during early stages of growth. Micronesica 12:319–322Google Scholar
  7. Brown BE, Cossins AR (2011) The potential for temperature acclimatisation of reef corals in the face of climate change. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 421–433Google Scholar
  8. Castillo KD, Ries JB, Weiss JM, Lima FP (2012) Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat Clim Chang 2:756–760Google Scholar
  9. Coles SL (1997) Reef corals occurring in a highly fluctuating temperature environment at Fahal Island, Gulf of Oman (Indian Ocean). Coral Reefs 16:269–272CrossRefGoogle Scholar
  10. Coles SL, Jokiel PL (1978) Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar Biol 49:187–195CrossRefGoogle Scholar
  11. Coles SL, Jokiel PL, Lewis CR (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac Sci 30:159–166Google Scholar
  12. Cosgrove J, Borowitzka MA (2010) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Borowitzka MA, Prasil O (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Netherlands, pp 1–17CrossRefGoogle Scholar
  13. Craig P, Birkeland C, Belliveau S (2001) High temperatures tolerated by a diverse assemblage of shallow-water corals in America Samoa. Coral Reefs 20:185–189CrossRefGoogle Scholar
  14. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N et al (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37CrossRefGoogle Scholar
  15. Dustan P (1979) Distribution of zooxanthellae and photosynthetic chloroplast pigments of the reef-building coral Montastrea annularis Ellis and Solander in relation to depth on a west Indian coral reef. Bull Mar Sci 29:79–95Google Scholar
  16. Edmunds PJ (2009) Effect of acclimatization to low temperature and reduced light on the response of reef corals to elevated temperature. Mar Biol 156:1797–1808CrossRefGoogle Scholar
  17. Edmunds PJ (2011) Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnol Oceanogr 56:2402–2410CrossRefGoogle Scholar
  18. Edmunds PJ, Gates RD (2008) Acclimatization in tropical reef corals. Mar Ecol Prog Ser 361:307–310Google Scholar
  19. Edmunds PJ, Leichter JJ, Adjeroud M (2010) Landscape-scale variation in coral recruitment in Moorea, French Polynesia. Mar Ecol Prog Ser 414:75–89CrossRefGoogle Scholar
  20. Edmunds PJ, Putnam HM, Gates RD (2012) Photophysiological consequences of vertical stratificiation of Symbiodinium in tissue of the coral Porites lutea. Biol Bull 223:226–235Google Scholar
  21. Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174CrossRefGoogle Scholar
  22. Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43Google Scholar
  23. Geister TL, Fischer K (2007) Testing the beneficial acclimation hypothesis: temperature effects on mating success in a butterfly. Behav Ecol 18:658–664CrossRefGoogle Scholar
  24. Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963CrossRefGoogle Scholar
  25. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201CrossRefGoogle Scholar
  26. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, OxfordGoogle Scholar
  27. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866CrossRefGoogle Scholar
  28. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefGoogle Scholar
  29. Howells EJ, Berkelmans R, van Oppen MJ, Willis BL, Bay LK (2013) Historical thermal regimes define limits to coral acclimatization. Ecology 94:1078–1088CrossRefGoogle Scholar
  30. Huey RB, Berrigan D (1996) Testing evolutionary hypotheses of acclimation. In: Johnston IA, Bennett RB (eds) Animals and temperature: phenotypic and evolutionary adaptation. Cambridge University Press, Cambridge, pp 205–237CrossRefGoogle Scholar
  31. Huey RB, Berrigan D, Gilchrist GW, Herron JC (1999) Testing the adaptive significance of acclimation: a strong inference approach. Am Zool 39:323–336Google Scholar
  32. Hughes TP, Connell JH (1987) Population dynamics based on size or age? A reef-coral analysis. Am Nat 129:818–829CrossRefGoogle Scholar
  33. Hughes TP, Jackson JBC (1985) Population dynamics and life histories of foliaceous corals. Ecol Monogr 55:141–166CrossRefGoogle Scholar
  34. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  35. Jones AM, Berkelmans R, van Oppen MJ, 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 275:1359–1365CrossRefGoogle Scholar
  36. Kaniewska P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, Dove S, Hoegh-Guldberg O (2012) Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS ONE 7:e34659CrossRefGoogle Scholar
  37. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434CrossRefGoogle Scholar
  38. Kroeker KJ, Kordas RL, Crim RN, Hendriks IE, Ranajo L, Singh GG, Duarte CM, Gattuso J-P (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interactions with warming. Glob Chang Biol 19:1884–1896CrossRefGoogle Scholar
  39. Leichter JJ, Helmuth B, Fischer 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
  40. Leroi AM, Bennett AF, Lenski RE (1994) Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc Natl Acad Sci USA 91:1917–1921CrossRefGoogle Scholar
  41. Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 405–419Google Scholar
  42. Levy O, Keniewska P, Eisenberg E, Kerako-Lampert S, Bat LK, Reef R, Rodriguez-Lanetty M, Miller DJ, Hoegh-Guldberg O (2011) Complex diel cycles of gene expression in coral-algal symbioisis. Science 331:175Google Scholar
  43. Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  44. Mayfield AB, Chan PH, Putnam HM, Chen CS, Fan TY (2012) The effects of a variable temperature regime on the physiology of the reef-building coral Seriatopora hystrix: results from a laboratory-based reciprocal transplant. J Exp Biol 215:4183–4195CrossRefGoogle Scholar
  45. Mcleod E, Anthony KRN, Andersson A, Beeden R, Golbuu Y, Kleypas J, Kroeker K, Manzello D, Salm RV, Schuttenberg H et al (2012) Preparing to manage coral reefs for ocean acidification: lessons from coral bleaching. Front Ecol Environ 11:20–27CrossRefGoogle Scholar
  46. 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 211:1050–1056CrossRefGoogle Scholar
  47. Muscatine LM (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky S (ed) Coral reefs: ecosystems of the world, vol 25. Elsevier Science, Amsterdam, pp 75–87Google Scholar
  48. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  49. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefGoogle Scholar
  50. Platt JR (1964) Strong inference. Science 146:347–353CrossRefGoogle Scholar
  51. Prosser CL (1991) Environmental and metabolic animal physiology: comparative animal physiology, 4th edn. Wiley-Liss, New YorkGoogle Scholar
  52. Putnam HM, Edmunds PJ (2011) The physiological response of reef corals to diel fluctuations in seawater temperature. J Exp Mar Biol Ecol 396:216–223CrossRefGoogle Scholar
  53. Rosenberg E, Sharon G, Atad I, Zilber-Rosenberg I (2010) The evolution of animals and plants via symbiosis with microorganisms. Environ Microbiol Rep 2:500–506CrossRefGoogle Scholar
  54. Sanders HL (1968) Marine benthic diversity: a comparative study. Am Nat 102:243–282CrossRefGoogle Scholar
  55. Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annu Rev Mar Sci 4:39–61CrossRefGoogle Scholar
  56. Soong K, Chen CA, Chang JC (1999) A very large poritid colony at Green Island, Taiwan. Coral Reefs 18:42CrossRefGoogle Scholar
  57. Spencer-Davies P (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  58. Veron JEN (2000) Corals of the world, vol 1–3. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  59. Willmer P, Stone G, Johnston I (2005) Environmental physiology of animals, 2nd edn. Blackwell Science, OxfordGoogle Scholar
  60. Wilson RS, Franklin CE (2002) Testing the beneficial acclimation hypothesis. Trends Ecol Evol 17:66–70CrossRefGoogle Scholar
  61. Winter A, Appeldoorn RS, Bruckner A, Williams EH Jr, Goenaga C (1998) Sea surface temperatures and coral reef bleaching off La Parguera, Puerto Rico (northeastern Caribbean Sea). Coral Reefs 17:377–382CrossRefGoogle Scholar
  62. Woods HA, Harrison JF (2002) Interpreting rejections of the beneficial acclimation hypothesis: when is physiological plasticity adaptive? Evolution 56:1863–1866CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of BiologyCalifornia State UniversityNorthridgeUSA

Personalised recommendations