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Do fluctuating temperature environments elevate coral thermal tolerance?

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Abstract

In reef corals, much research has focused on the capacity of corals to acclimatize and/or adapt to different thermal environments, but the majority of work has focused on distinctions in mean temperature. Across small spatial scales, distinctions in daily temperature variation are common, but the role of such environmental variation in setting coral thermal tolerances has received little attention. Here, we take advantage of back-reef pools in American Samoa that differ in thermal variation to investigate the effects of thermally fluctuating environments on coral thermal tolerance. We experimentally heat-stressed Acropora hyacinthus from a thermally moderate lagoon pool (temp range 26.5–33.3°C) and from a more thermally variable pool that naturally experiences 2–3 h high temperature events during summer low tides (temp range 25.0–35°C). We compared mortality and photosystem II photochemical efficiency of colony fragments exposed to ambient temperatures (median: 28.0°C) or elevated temperatures (median: 31.5°C). In the heated treatment, moderate pool corals showed nearly 50% mortality whether they hosted heat-sensitive (49.2 ± 6.5% SE; C2) or heat-resistant (47.0 ± 11.2% SE; D) symbionts. However, variable pool corals, all of which hosted heat-resistant symbionts, survived well, showing low mortalities (16.6 ± 8.8% SE) statistically indistinguishable from controls held at ambient temperatures (5.1–8.3 ± 3.3–8.3% SE). Similarly, moderate pool corals hosting heat-sensitive algae showed rapid rates of decline in algal photosystem II photochemical efficiency in the elevated temperature treatment (slope = −0.04 day−1 ± 0.007 SE); moderate pool corals hosting heat-resistant algae showed intermediate levels of decline (slope = −0.039 day−1 ± 0.007 SE); and variable pool corals hosting heat-resistant algae showed the least decline (slope = −0.028 day−1 ± 0.004 SE). High gene flow among pools suggests that these differences probably reflect coral acclimatization not local genetic adaptation. Our results suggest that previous exposure to an environmentally variable microhabitat adds substantially to coral–algal thermal tolerance, beyond that provided by heat-resistant symbionts alone.

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References

  • Abrego D, Ulstrup K, Willis B, van Oppen M (2008) Species–specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Biol Sci Ser B 275:2273–2282

    Article  CAS  Google Scholar 

  • Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20

    Article  PubMed  Google Scholar 

  • Baker AC (2001) Ecosystems - Reef corals bleach to survive change. Nature 411:765–766

    Article  PubMed  CAS  Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkelands C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Mol Ecol 19:1705–1720

    Article  PubMed  CAS  Google Scholar 

  • Berkelmans R, Oliver J (1999) Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18:55–60

    Article  Google Scholar 

  • 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 Biol Sci Ser B 273:2305–2312

    Article  Google Scholar 

  • Brown BE, Dunne RP, Goodson MS, Douglas AE (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21:119–126

    Google Scholar 

  • Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism - A testable hypothesis. Bioscience 43:320–326

    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 (Berl) 148:261–270

    Article  Google Scholar 

  • Clausen CD, Roth AA (1975) Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis. Mar Biol 33:93–100

    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 

  • Coles SL, Brown BE (2003) Coral bleaching - Capacity for acclimatization and adaptation. Adv Mar Biol 46:183–223

    Article  PubMed  CAS  Google Scholar 

  • Coles SL, Jokiel PL (1978) Synergistic effects of temperature salinity and light on the hermatypic coral Montipora verrucosa. Mar Biol (Berl) 49:187–196

    Article  Google Scholar 

  • Coles S, Jokiel P, Lewis C (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals Pac Sci 30:159–166

    Google Scholar 

  • Craig P, Birkeland C, Belliveau S (2001) High temperatures tolerated by a diverse assemblage of shallow-water corals in American Samoa. Coral Reefs 20:185–189

    Article  Google Scholar 

  • Crawley MJ (2007) The R Book. Wiley and Sons, West Sussex

    Book  Google Scholar 

  • Dickerson BR, Vinyard GL (1999) Effects of high chronic temperatures and diel temperature cycles on the survival and growth of Lahontan cutthroat trout. Trans Am Fish Soc 128:516–521

    Article  Google Scholar 

  • Edmunds P, Gates R (2008) Acclimatization in tropical reef corals. Mar Ecol Prog Ser 361:307–310

    Article  Google Scholar 

  • Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47

  • 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 

  • Fine M, Steindler L, Loya Y (2004) Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar Freshw Res 55:115–121

    Article  CAS  Google Scholar 

  • Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65

    Article  Google Scholar 

  • Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43

    Google Scholar 

  • Goreau TJ, Hayes RL (1994) Coral bleaching and ocean hotspots. Ambio 23:176–180

    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, 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 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  PubMed  CAS  Google Scholar 

  • Hutchison VH, Ferrance MR (1970) Thermal tolerances of Rana pipiens acclimated to daily temperature cycles. Herpetologica 26:1–8

    Google Scholar 

  • Jokiel P, Coles S (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162

    Article  Google Scholar 

  • Ketola T, Laakso J, Kaitala V, Airaksinen S (2004) Evolution of Hsp90 expression in Tetrahymena thermophila (Protozoa, Ciliata) populations exposed to thermally variable environments. Evolution 58:741–748

    PubMed  CAS  Google Scholar 

  • Koehn R, Newell R, Immermann F (1980) Maintenance of an aminopeptidase allele frequency cline by natural selection. Proc Natl Acad Sci USA 77:5385–5389

    Article  PubMed  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol (Berl) 141:387–400

    Article  Google Scholar 

  • LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, Pérez AL, Reyes-Bonilla H, Warner ME (2010) Host–symbiont recombination versus natural selection in the response of coral–dinoflagellate symbioses to environmental disturbance. Proc R Soc Biol Sci Ser B 277:2925–2934

    Article  Google Scholar 

  • Liu G, Strong AE, Skirving WJ, Arzayus LF (2006) Overview of NOAA Coral Reef Watch Program’s Near-Real-Time Satellite Global Coral Bleaching Monitoring Activities. Proceedings 10th International Coral Reef Symp: 1783–1793

  • Mayer A (1914) The effects of temperature upon tropical marine animals. Pap Tortugas Lab Carnegie Inst Wash VI:1–24

    Google Scholar 

  • McClanahan TR, Muthiga NA, Mangi S (2001) Coral and algal changes after the 1998 coral bleaching: Interaction with reef management and herbivores on Kenyan reefs. Coral Reefs 19:380–391

    Google Scholar 

  • McClanahan TR, Ateweberhan M, Graham NAJ, Wilson SK, Sebastian CR, Guillaume MMM, Bruggemann JH (2007) Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Mar Ecol Prog Ser 337:1–13

    Article  Google Scholar 

  • 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 211:1050–1056

    Article  PubMed  Google Scholar 

  • Oliver T, Palumbi S (2009) Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar Ecol Prog Ser 378:93–103

    Article  CAS  Google Scholar 

  • Otto R (1974) The effects of acclimation to cyclic thermal regimes on heat tolerance of the western mosquitofish. Trans Am Fish Soc 103:331–335

    Article  Google Scholar 

  • Piniak G, Brown E (2009) Temporal variability in chlorophyll fluorescence of back-reef corals in Ofu, American Samoa. Biol Bull 216:55

    PubMed  Google Scholar 

  • Podrabsky J, Somero G (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 H, Edmunds P, Fan T (2010) Effect of a fluctuating thermal regime on adult and larval reef corals. Invertebr Biol 129:199–209

    Article  Google Scholar 

  • Riegl B (2003) Climate change and coral reefs: different effects in two high-latitude areas (Arabian Gulf, South Africa). Coral Reefs 22:433–446

    Article  Google Scholar 

  • Roberts DA, Hofman GE, Somero GN (1997) Heat-shock protein expression in Mytilus californianus: acclimatization (seasonal and tidal height comparisons) and acclimation effects. Biol Bull 192:309–320

    Article  CAS  Google Scholar 

  • Rowan R (2004) Coral bleaching - Thermal adaptation in reef coral symbionts. Nature 430:742–742

    Article  PubMed  CAS  Google Scholar 

  • Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature (Lond) 388:265–269

    Article  CAS  Google Scholar 

  • Sastry A (1979) Metabolic adaptation of Cancer irroratus developmental stages to cyclic temperatures. Mar Biol 51:243–250

    Article  Google Scholar 

  • Schaefer J, Ryan A (2006) Developmental plasticity in the thermal tolerance of zebrafish Danio rerio J Fish Biol 722–734

  • Smith L, Barshis D, Birkeland C (2007) Phenotypic plasticity for skeletal growth, density and calcification of Porites lobata in response to habitat type. Coral Reefs 26:559–567

    Article  Google Scholar 

  • Smith L, Wirshing H, Baker A, Birkeland C (2008) Environmental versus genetic influences on growth rates of the corals Pocillopora eydouxi and Porites lobata (Anthozoa: Scleractinia) 1. Pac Sci 62:57–69

    Article  Google Scholar 

  • Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76:449–462

    Article  PubMed  CAS  Google Scholar 

  • Suggett DJ, Smith DJ (2010) Interpreting the sign of coral bleaching as friend vs. foe. Global Change Biol published online: Dec 16 2009. doi:10.1111/j.1365-2486.2009.02155.x

  • Szmant A, Gassman N (1990) The effects of prolonged bleaching on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224

    Article  Google Scholar 

  • Thornhill D, LaJeunesse T, Santos S (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340

    Article  PubMed  CAS  Google Scholar 

  • Thorp JH, Wineriter SA (1981) Stress and growth response of juvenile crayfish to rhythmic and arrhythmic temperature fluctuations. Arch Environ Contam Toxicol 10:69–77

    Article  PubMed  CAS  Google Scholar 

  • Threader R, Houston AH (1983) Heat tolerance and resistance in juvenile rainbow trout acclimated to diurnally cycling temperatures. Comp Biochem Physiol 75:153–155

    Article  Google Scholar 

  • Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull (Woods Hole) 201:360–373

    Article  CAS  Google Scholar 

  • van Oppen MJH, Lough JM (2009) Coral bleaching: Patterns, processes. causes and consequences. Ecological Studies Book Series. Springer, Berlin, Heidelberg

    Book  Google Scholar 

  • van Oppen MJH, Palstra FP, Piquet AMT, Miller DJ (2001) Patterns of coral-dinoflagellate associations in Acropora: Significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Biol Sci Ser B 268:1759–1767

    Article  Google Scholar 

  • Walton E, Pringle J (1980) Effect of growth temperature upon heat sensitivity in Saccharomyces cerevisiae. Arch Microbiol 124:285–287

    Article  PubMed  CAS  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: A novel approach. Plant Cell Environ 19:291–299

    Article  Google Scholar 

  • Warner ME, Lesser MP, Ralph PJ (2010) Chlorophyll fluorescence in reef building corals. In: Suggett DJ, Prasil O, Borowitzka M (eds) Chlorophyll fluorescence in aquatic sciences: Methods and applications. Springer, Berlin, pp 209–222

    Chapter  Google Scholar 

  • Weis V (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059

    Article  PubMed  CAS  Google Scholar 

  • Weis V (2010) The susceptibility and resilience of corals to thermal stress: adaptation, acclimatization or both? Mol Ecol 19:1515–1517

    Article  PubMed  Google Scholar 

  • Wellington G, Glynn P, Strong A, Navarrete S, Wieters E, Hubbard D (2001) Crisis on coral reefs linked to climate change. EOS Trans Am Geophys Union 82:1–3

    Article  Google Scholar 

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Acknowledgments

The authors would like to acknowledge the assistance of C. Birkeland, Dan Barshis, Lance Smith, and Cheryl Squair at University of Hawaii, Peter Craig and Fale Tuilagi (US National Park Service, American Samoa); Seabird McKeon at the University of Florida; and Kirsten Oleson and Jason Ladner of Stanford University for their support in American Samoa; the Hawaiian Undersea Research Lab; and the National Park of American Samoa. An NSF Predoctoral fellowship program, the Woods Institute for the Environment at Stanford University, NOAA and the National Science Foundation provided funding.

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  1. Department of Biological Sciences, Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, Pacific Grove, CA, 93950, USA

    T. A. Oliver & S. R. Palumbi

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  1. T. A. Oliver
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  2. S. R. Palumbi
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Correspondence to T. A. Oliver.

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Oliver, T.A., Palumbi, S.R. Do fluctuating temperature environments elevate coral thermal tolerance?. Coral Reefs 30, 429–440 (2011). https://doi.org/10.1007/s00338-011-0721-y

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