Coral Reefs

, Volume 32, Issue 4, pp 909–921 | Cite as

Physiological acclimation to elevated temperature in a reef-building coral from an upwelling environment



Recent work has found that pocilloporid corals from regions characterized by unstable temperatures, such as those exposed to periodic upwelling, display a remarkable degree of phenotypic plasticity. In order to understand whether important reef builders from these upwelling reefs remain physiologically uncompromised at temperatures they will experience in the coming decades as a result of global climate change, a long-term elevated temperature experiment was conducted with Pocillopora damicornis specimens collected from Houbihu, a small embayment within Nanwan Bay, southern Taiwan that is characterized by 8–9 °C temperature changes during upwelling events. Upon nine months of exposure to nearly 30 °C, all colony (mortality and surface area), polyp (Symbiodinium density and chlorophyll a content), tissue (total thickness), and molecular (gene expression and molecular composition)-level parameters were documented at similar levels between experimental corals and controls incubated at 26.5 °C, suggesting that this species can readily acclimate to elevated temperatures that cause significant degrees of stress, or even bleaching and mortality, in conspecifics of other regions of the Indo-Pacific. However, the gastrodermal tissue layer was relatively thicker in corals of the high temperature treatment sampled after nine months, possibly as an adaptive response to shade Symbiodinium from the higher photosynthetically active radiation levels that they were experiencing at that sampling time. Such shading may have prevented high light and high temperature-induced photoinhibition, and consequent bleaching, in these samples.


Acclimation Coral reefs Endosymbiosis Gene expression Thermal stress Upwelling 

Supplementary material

338_2013_1067_MOESM1_ESM.docx (13 kb)
Supplementary material (DOCX 14 kb)
338_2013_1067_MOESM2_ESM.docx (17 kb)
Supplementary material (DOCX 18 kb)
338_2013_1067_MOESM3_ESM.eps (449 kb)
Electronic supplemental material Fig. 1. Molecular composition parameters. RNA/DNA (a) and protein/DNA (b) ratios, as well as Symbiodinium (c) and host (d) genome copy proportions (GCPs) were calculated in triplicate biological replicates of both the control (26.5 °C; white diamonds) and high (29.7 °C black triangles) temperature treatments after 2, 4, 8, 24, and 36 weeks of exposure. Error bars represent standard error of the mean. In c-d, letters above icons represent Tukey’s honestly significant difference groups (p < 0.05) for the effect of time only. (EPS 449 kb)


  1. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution and Systematics 34:661–689CrossRefGoogle Scholar
  2. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA 110:1387–1392PubMedCrossRefGoogle Scholar
  3. Bower NI, Moser RJ, Hill JR, Lehnert SA (2007) Universal reference method for real-time PCR gene expression analysis of preimplantation embryos. Biotechniques 42:199–206PubMedCrossRefGoogle Scholar
  4. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16S:129–138CrossRefGoogle Scholar
  5. 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
  6. Coles S (1975) A comparison of effects of elevated temperature versus temperature fluctuations on reef corals at Kahe Point, Oahu. Pac Sci 29:15–18Google Scholar
  7. Correa AMS, McDonald MD, Baker AC (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar Biol 156:2403–2411CrossRefGoogle Scholar
  8. Crawley A, Kline D, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biol 16:851–863CrossRefGoogle Scholar
  9. Dai CF (1991) Reef environment and coral fauna of southern Taiwan. Atoll Res Bull 354:1–28CrossRefGoogle Scholar
  10. Doo SS, Mayfield AB, Chen HK, Byrne M, Fan TY (2012) Reduced expression of the rate- limiting carbon fixation enzyme RuBisCO in the benthic foraminifer Baculogypsina sphaerulata in response to heat shock. J Exp Mar Biol Ecol 430:63–67CrossRefGoogle Scholar
  11. Downs CA, Mueller E, Phillips S, Fauth JE, Woodley CM (2000) A molecular biomarker system for assessing the health of coral (Montastrea faveolata) during heat stress. Mar Biotech 2:533–544CrossRefGoogle Scholar
  12. Feder M (1996) Ecological and evolutionary physiology of stress proteins and the stress response: the Drosophila melanogaster model. In: Johnston IA, Bennett AF (eds) Animals and temperature: phenotypic and evolutionary adaptation. Cambridge University Press, Cambridge, pp 79–102CrossRefGoogle Scholar
  13. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102–110CrossRefGoogle Scholar
  14. Gates RD (1990) Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8:193–197CrossRefGoogle Scholar
  15. Glynn PW (1983) Extensive “bleaching” and death of reef corals on the Pacific coast of Panama. Environ Conserv 10:149–154CrossRefGoogle Scholar
  16. Grottoli A, Rodrigues L, Palardy J (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189PubMedCrossRefGoogle Scholar
  17. Heath AG, Turner BJ, Davis WP (1993) Temperature preferences and tolerances of three fish species inhabiting hyperthermal ponds on mangrove islands. Hydrobiologia 259:47–55CrossRefGoogle Scholar
  18. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  19. Hoegh-Guldberg O, Smith GJ (1989) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Biol Ecol 129:279–303CrossRefGoogle Scholar
  20. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  21. IPCC (2007) Impacts, adaptation and vulnerability. In: Fourth assessment report on the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  22. Jan S, Chen CTA (2008) Potential biogeochemical effects from vigorous internal tides generated in Luzon Strait: a case study at the southernmost coast of Taiwan. J Geophys Res 114:1–14Google Scholar
  23. Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo Pacific reef corals to elevated temperatures. Coral Reefs 8:155–162CrossRefGoogle Scholar
  24. Kultz D (2005) Molecular basis of the cellular stress response. Annu Rev Physiol 67:225–257PubMedCrossRefGoogle Scholar
  25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  26. Lee HJ, Chao SY, Fan KY (1999) Flood-ebb disparity of tidally induced recirculation eddies in a semi-enclosed basin: Nan Wan Bay. Cont Shelf Res 19:871–890CrossRefGoogle Scholar
  27. Liu PJ, Lin SM, Fan TY, Meng PJ, Shao KT, Lin HJ (2009) Rates of overgrowth by macroalgae and attack by sea anemones are greater for live coral than dead coral under conditions of nutrient enrichment. Limnol Oceanogr 54:1167–1175CrossRefGoogle Scholar
  28. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  29. Mayfield AB, Gates RD (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp Biochem Physiol 147A:1–10Google Scholar
  30. Mayfield AB, Hirst MB, Gates RD (2009) Gene expression normalization in a dual-compartment system: a quantitative real-time PCR protocol for symbiotic anthozoans. Mol Ecol Res 9:462–470CrossRefGoogle Scholar
  31. Mayfield AB, Hsiao YY, Fan TY, Chen CS, Gates RD (2010) Evaluating the temporal stability of stress-activated protein kinase and cytoskeleton gene expression in the Pacific corals Pocillopora damicornis and Seriatopora hystrix. J Exp Mar Biol Ecol 395:215–222CrossRefGoogle Scholar
  32. Mayfield AB, Wang LH, Tang PC, Hsiao YY, Fan TY, Tsai CL, Chen CS (2011) Assessing the impacts of experimentally elevated temperature on the biological composition and molecular chaperone gene expression of a reef coral. PLoS ONE 6:e26529PubMedCrossRefGoogle Scholar
  33. Mayfield AB, Chan PH, Putnam HP, Chen CS, Fan TY (2012a) 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 215:4183–4195PubMedCrossRefGoogle Scholar
  34. Mayfield AB, Hsiao YY, Fan TY, Chen CS (2012b) Temporal variation in RNA/DNA and protein/DNA ratios in four anthozoan-dinoflagellate endosymbioses of the Indo-Pacific: implications for molecular diagnostics. Platax 16:29–52Google Scholar
  35. Mayfield AB, Chen M, Meng PJ, Lin HJ, Chen CS, Liu PJ (2013) The physiological response of the reef coral Pocillopora damicornis to elevated temperature: results from coral reef mesocosm experiments in Southern Taiwan. Mar Environ Res 86:1–11PubMedCrossRefGoogle Scholar
  36. Mayfield AB, Fan TY, Chen CS (in press) Real-time PCR-based gene expression analysis in the model reef-building coral Pocillopora damicornis: insight from a salinity stress case study. PlataxGoogle Scholar
  37. Mayfield AB, Fan TY, Chen CS (accepted) The physiological impact of ex situ transplantation on the Taiwanese reef-building coral Seriatopora hystrix. J Mar BiolGoogle Scholar
  38. Meng PJ, Lee HJ, Wang JT, Chen CC, Lin HJ, Tew KS, Hsieh WJ (2008) A long-term survey on anthropogenic impacts to the water quality of coral reefs, southern Taiwan. Environ Pollut 156:67–75PubMedCrossRefGoogle Scholar
  39. Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440CrossRefGoogle Scholar
  40. Pochon X, Putnam HM, Burki F, Gates RD (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS ONE 7:e29816PubMedCrossRefGoogle Scholar
  41. Podrabsky JE, Somero GN (2004) Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J Exp Biol 207:2237–2254PubMedCrossRefGoogle Scholar
  42. Putnam HM, Edmunds PJ, Fan TY (2010) Effect of a fluctuating thermal regime on adult and larval reef corals. Invertebr Biol 129:199–209CrossRefGoogle Scholar
  43. Putnam HP, Mayfield AB, Fan TY, Chen CS, Gates RD (in press) The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2. Mar BiolGoogle Scholar
  44. Salih A, Larkum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853PubMedCrossRefGoogle Scholar
  45. Smith EG, D’Angelo C, Salih A, Wiedenmann J (2013) Screening by coral green fluorescent protein (GFP)-like chromoproteins supports a role in photoprotection of zooxanthellae. Coral Reefs 32:463–474CrossRefGoogle Scholar
  46. Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74CrossRefGoogle Scholar
  47. Veron JEN (2000) Corals of the world, vols. 1-3. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  48. Vidal-Dupiol J, Adjeroud M, Roger E, Foure L, Duval D, Mone Y, Ferrier-Pages C, Tambutte E, Tambutte S, Zoccola D, Allemand D, Mitta G (2009) Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BMC Physiol 9:14PubMedCrossRefGoogle Scholar
  49. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.National Museum of Marine Biology and AquariumChechengTaiwan
  2. 2.Living Oceans FoundationLandoverUSA
  3. 3.Graduate Institute of Marine Biodiversity and EvolutionNational Dong-Hwa UniversityChechengTaiwan
  4. 4.Graduate Institute of Marine BiotechnologyNational Dong-Hwa UniversityChechengTaiwan
  5. 5.Department of Marine Biotechnology and ResourcesNational Sun Yat-Sen UniversityKaohsiungTaiwan

Personalised recommendations