The effects of environmental history and thermal stress on coral physiology and immunity
Rising ocean temperatures can induce the breakdown of the symbiosis between reef building corals and Symbiodinium in the phenomenon known as coral bleaching. Environmental history may, however, influence the response of corals to stress and affect bleaching outcomes. A suite of physiological and immunological traits was evaluated to test the effect of environmental history (low vs. high variable pCO2) on the response of the reef coral Montipora capitata to elevated temperature (24.5 °C vs. thermal ramping to 30.5 °C). Heating reduced maximum photochemical efficiency (Fv/Fm) and chlorophyll a but increased tissue melanin in corals relative to the ambient treatment, indicating a role of the melanin synthesis pathway in the early stages of thermal stress. However, interactions of environmental history and temperature treatment were not observed. Rather, parallel reaction norms were the primary response pattern documented across the two temperature treatments with respect to reef environmental history. Corals with a history of greater pCO2 variability had higher constitutive antioxidative and immune activity (i.e., catalase, superoxide dismutase, prophenoloxidase) and Fv/Fm, but lower melanin and chlorophyll a, relative to corals with a history of lower pCO2 variability. This suggests that reef environments with high magnitude pCO2 variability promote greater antioxidant and immune activity in resident corals. These results demonstrate coral physiology and immunity reflect environmental attributes that vary over short distances, and that these differences may buffer the magnitude of thermal stress effects on coral phenotypes.
We thank Dr. Eric H. De Carlo and colleagues with NOAA PMEL and CRIMP CO2 program for Kāne‘ohe Bay pCO2 data, and two reviewers for suggestions that improved the manuscript. Biological collections were performed in accordance with the state of Hawai‘i Department of Land and Natural Resources Division of Aquatic Resources permitting guidelines. CBW was supported by an Environmental Protection Agency (EPA) STAR Fellowship Assistance Agreement (FP-91779401-1). The views expressed in this publication have not been reviewed or endorsed by the EPA and are solely those of the authors. HMP was supported by NSF OCE-PRF 1323822. LDM was supported by NSF 1017458, and CAR was supported by LSAMP Bridge to Doctorate program. This is HIMB contribution number 1722, SOEST contribution number 10328.
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Conflict of interest
The authors declare they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc Ser B Methodol 26:211–252Google Scholar
- Brown B, Dunne R, Goodson M, Douglas A (2002a) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21:119–126Google Scholar
- Calosi P, Rastrick SPS, Lombardi C, de Guzman HJ, Davidson L, Jahnke M, Giangrande A, Hardege JD, Schulze A, Spicer JI, Gambi M-C (2013) Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system. Philos Trans R Soc Lond B Biol Sci 368:20120444PubMedPubMedCentralCrossRefGoogle Scholar
- Coles SL, Jokiel PL, Lewis CR (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac Sci 30:159–166Google Scholar
- Douglas B, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48Google Scholar
- Dunne RP, Brown BE (2001) The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998. Coral Reefs 20:201–210Google 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 373:102–110CrossRefGoogle Scholar
- Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connell SD, Dupont S, Fabricius KE, Hall-Spencer JH, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Schreiber SJ, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15PubMedCrossRefGoogle Scholar
- Grottoli-Everett A, Kuffner IB (1995) Uneven bleaching within colonies of the Hawaiian coral Montipora verrucosa. In: Gulko D, Jokiel PL (eds), Ultraviolet radiation and coral reefs. HIMB Technical Report #41, UNIHI-Sea Grant-CR-95-03, pp 115–120Google Scholar
- Hochachka PW, Somero GN (2002) Biochemical adaptation, mechanism and process in physiological evolution. Oxford University Press, New YorkGoogle Scholar
- Hume BCC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci USA 113:4416–4421PubMedPubMedCentralCrossRefGoogle Scholar
- IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, Pachauri RK, Meyer LA (eds)]. IPCC, Geneva, 151 ppGoogle Scholar
- Kenkel CD, Aglyamova G, Alamaru A, Bhagooli R, Capper R, Cunning R, deVillers A, Haslun JA, Hédouin L, Keshavmurthy S, Kuehl KA, Mahmoud H, McGinty ES, Montoya-Maya PH, Palmer CV, Pantile R, Sánchez JA, Schils T, Silverstein RN, Squiers LB, Tang P-C, Goulet TL, Matz MV (2011) Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites. PLoS One 6:e26914PubMedPubMedCentralCrossRefGoogle Scholar
- Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-32. https://CRAN.R-project.org/package=lmerTest. Accessed 01 Mar 2017
- NOAA (2017) Tides and Currents. Mokuoloe, Hawaii, Station ID: 1612480. National Oceanic and Atmospheric Administration, USA. https://tidesandcurrents.noaa.gov/stationhome.html?id=1612480. Accessed March 2017
- Osmond CB, Anderson JM, Ball MC, Egerton JJG (1999) Compromising efficiency: the molecular ecology of light resource utilisation in terrestrial plants. In: Scholes C, Baker M (eds) Advances in physiological plant ecology. Blackwell, New Jersey, pp 1–24Google Scholar
- R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 01 Mar 2017
- Sabine C, De Carlo E, Musielewicz S, Maenner S, Bott R, Sutton A (2012) Partial pressure (or fugacity) of carbon dioxide, salinity and other variables collected from time series observations using bubble type equilibrator for autonomous carbon dioxide (CO2) measurement, carbon dioxide (CO2) gas analyzer and other instruments from MOORING CRIMP1_158W_21N in the North Pacific Ocean from 2005-12-01 to 2008-05-30 (NODC Accession 0100069). Version 3.3. National Oceanographic Data Center, NOAA. Dataset. Accessed March 2017Google Scholar
- Stat M, Pochon X, Franklin EC, Bruno JF, Casey KS, Selig ER, Gates RD (2013) The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress. Ecol Evol 3:1317–1329PubMedPubMedCentralCrossRefGoogle Scholar
- Sutton A, Sabine C, De Carlo E, Musielewicz S, Maenner S, Dietrich C, Bott R, Osborne J (2016) Partial pressure (or fugacity) of carbon dioxide, salinity and other variables collected from time series observations using Bubble type equilibrator for autonomous carbon dioxide (CO2) measurement, Carbon dioxide (CO2) gas analyzer and other instruments from MOORING_CRIMP2_158W_21N in the Kaneohe Bay and North Pacific Ocean from 2008-06-11 to 2015-05-13 (NCEI Accession 0157415). Version 2.2. NOAA National Centers for Environmental Information. Dataset. Accessed March 2017Google Scholar
- Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L, Berumen ML, Bourne DG, Cantin N, Foret S, Matz M, Miller DJ, Moya A, Putnam HM, Ravasi T, van Oppen MJH, Thurber RV, Vidal-Dupiol J, Voolstra CR, Watson S-A, Whitelaw E, Willis BL, Munday PL (2017) Rapid adaptive responses to climate change in corals. Nat Clim Chang 7:627–636CrossRefGoogle Scholar