Skip to main content

Advertisement

SpringerLink
Log in

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

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution and Systematics 34:661–689

    Article  Google Scholar 

  • 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 110:1387–1392

    Article  PubMed  CAS  Google Scholar 

  • Bower NI, Moser RJ, Hill JR, Lehnert SA (2007) Universal reference method for real-time PCR gene expression analysis of preimplantation embryos. Biotechniques 42:199–206

    Article  PubMed  CAS  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16S:129–138

    Article  Google Scholar 

  • Castillo KD, Helmuth BST (2005) Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Mar Biol 148:261–270

    Article  Google Scholar 

  • Coles S (1975) A comparison of effects of elevated temperature versus temperature fluctuations on reef corals at Kahe Point, Oahu. Pac Sci 29:15–18

    Google Scholar 

  • 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 156:2403–2411

    Article  CAS  Google Scholar 

  • 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 16:851–863

    Article  Google Scholar 

  • Dai CF (1991) Reef environment and coral fauna of southern Taiwan. Atoll Res Bull 354:1–28

    Article  Google Scholar 

  • 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 430:63–67

    Article  Google Scholar 

  • 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 2:533–544

    Article  CAS  Google Scholar 

  • 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 79–102

    Chapter  Google Scholar 

  • 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 373:102–110

    Article  Google Scholar 

  • Gates RD (1990) Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8:193–197

    Article  Google Scholar 

  • Glynn PW (1983) Extensive “bleaching” and death of reef corals on the Pacific coast of Panama. Environ Conserv 10:149–154

    Article  Google Scholar 

  • Grottoli A, Rodrigues L, Palardy J (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  PubMed  CAS  Google Scholar 

  • Heath AG, Turner BJ, Davis WP (1993) Temperature preferences and tolerances of three fish species inhabiting hyperthermal ponds on mangrove islands. Hydrobiologia 259:47–55

    Article  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • 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 129:279–303

    Article  Google Scholar 

  • 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 318:1737–1742

    Article  PubMed  CAS  Google Scholar 

  • IPCC (2007) Impacts, adaptation and vulnerability. In: Fourth assessment report on the intergovernmental panel on climate change. Cambridge University Press, Cambridge

  • 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 114:1–14

    Google Scholar 

  • Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo Pacific reef corals to elevated temperatures. Coral Reefs 8:155–162

    Article  Google Scholar 

  • Kultz D (2005) Molecular basis of the cellular stress response. Annu Rev Physiol 67:225–257

    Article  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • 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 19:871–890

    Article  Google Scholar 

  • 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 54:1167–1175

    Article  CAS  Google Scholar 

  • Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131

    Article  Google Scholar 

  • Mayfield AB, Gates RD (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp Biochem Physiol 147A:1–10

    CAS  Google Scholar 

  • 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 9:462–470

    Article  Google Scholar 

  • 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 395:215–222

    Article  Google Scholar 

  • 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:e26529

    Article  PubMed  CAS  Google Scholar 

  • 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 215:4183–4195

    Article  PubMed  CAS  Google Scholar 

  • 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 16:29–52

    Google Scholar 

  • 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 86:1–11

    Article  PubMed  CAS  Google Scholar 

  • 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. Platax

  • Mayfield AB, Fan TY, Chen CS (accepted) The physiological impact of ex situ transplantation on the Taiwanese reef-building coral Seriatopora hystrix. J Mar Biol

  • 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 156:67–75

    Article  PubMed  CAS  Google Scholar 

  • Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440

    Article  Google Scholar 

  • 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:e29816

    Article  PubMed  CAS  Google Scholar 

  • 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 207:2237–2254

    Article  PubMed  CAS  Google Scholar 

  • Putnam HM, Edmunds PJ, Fan TY (2010) Effect of a fluctuating thermal regime on adult and larval reef corals. Invertebr Biol 129:199–209

    Article  Google Scholar 

  • 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 Biol

  • Salih A, Larkum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853

    Article  PubMed  CAS  Google Scholar 

  • 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 32:463–474

    Article  Google Scholar 

  • 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 153:63–74

    Article  Google Scholar 

  • Veron JEN (2000) Corals of the world, vols. 1-3. Australian Institute of Marine Science, Townsville

  • 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 9:14

    Article  PubMed  Google Scholar 

  • Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Pei-Hsun Chan for assistance producing the coral nubbins. Special thanks are also given to Chen-Yi Wu for his assistance in the processing of samples for histology. Mern-Zi Chen is acknowledged for his help with the SEM-based analyses. Drs. Glen Watson and Joseph Neigel at the University of Louisiana, Lafayette are also thanked for the sharing of laboratory space in which the gene expression analyses were conducted. ABM was funded by an international research fellowship from the National Science Foundation (NSF) of the United States of America (OISE-0852960). The laboratory analyses conducted herein were funded by PADI Project Aware, PADI Foundation, The Journal of Experimental Biology, and NSF East Asia and Pacific Summer Institutes (EAPSI) grants to ABM.

Author information

Authors and Affiliations

  1. National Museum of Marine Biology and Aquarium, 2 Houwan Rd., Checheng, Pingtung, 944, Taiwan

    A. B. Mayfield, T.-Y. Fan & C.-S. Chen

  2. Living Oceans Foundation, Landover, MD, USA

    A. B. Mayfield

  3. Graduate Institute of Marine Biodiversity and Evolution, National Dong-Hwa University, Checheng, Taiwan

    T.-Y. Fan

  4. Graduate Institute of Marine Biotechnology, National Dong-Hwa University, Checheng, Taiwan

    C.-S. Chen

  5. Department of Marine Biotechnology and Resources, National Sun Yat-Sen University, Kaohsiung, Taiwan

    C.-S. Chen

Authors
  1. A. B. Mayfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T.-Y. Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C.-S. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. B. Mayfield.

Additional information

Communicated by Biology Editor Dr. Anastazia Banaszak

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (DOCX 14 kb)

Supplementary material (DOCX 18 kb)

338_2013_1067_MOESM3_ESM.eps

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mayfield, A.B., Fan, TY. & Chen, CS. Physiological acclimation to elevated temperature in a reef-building coral from an upwelling environment. Coral Reefs 32, 909–921 (2013). https://doi.org/10.1007/s00338-013-1067-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-013-1067-4

Keywords

Search

Navigation