Skip to main content

Advertisement

Log in

The effects of environmental history and thermal stress on coral physiology and immunity

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

(Data: NOAA PMEL; Drupp et al. 2011, 2013; Sabine et al. 2012; Sutton et al. 2016)

Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aeby GS, Ross M, Williams GJ, Lewis TD, Works TM (2010) Disease dynamics of Montipora white syndrome within Kaneohe Bay, Oahu, Hawaii: distribution, seasonality, virulence, and transmissibility. Dis Aquat Organ 91:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W (2016) Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352:338–342

    Article  CAS  PubMed  Google Scholar 

  • Albright R, Benthuysen J, Cantin N, Caldeira K, Anthony K (2015) Coral reef metabolism and carbon chemistry dynamics of a coral reef flat. Geophys Res Lett 42:3980–3988

    Article  CAS  Google Scholar 

  • Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Annu Rev Mar Sci 5:321–348

    Article  Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland 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  CAS  PubMed  Google Scholar 

  • Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5:e10871

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc Ser B Methodol 26:211–252

    Google Scholar 

  • Brown BE, Dunne RP, Goodson MS, Douglas AE (2000) Bleaching patterns in reef corals. Nature 404:142–143

    Article  CAS  PubMed  Google Scholar 

  • Brown B, Dunne R, Goodson M, Douglas A (2002a) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21:119–126

    Google Scholar 

  • Brown BE, Downs CA, Dunne RP, Gibb SW (2002b) Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar Ecol Prog Ser 242:119–129

    Article  Google 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 368:20120444

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carilli J, Donner SD, Hartmann AC (2012) Historical temperature variability affects coral response to heat stress. PLoS One 7:e34418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coles SL, Jokiel PL (1978) Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar Biol 49:187–195

    Article  Google Scholar 

  • Coles SL, Jokiel PL, Lewis CR (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac Sci 30:159–166

    Google Scholar 

  • Couch CS, Mydlarz LD, Harvell CD, Douglas NL (2008) Variation in measures of immunocompetence of sea fan coral, Gorgonia ventalina, in the Florida Keys. Mar Biol 155:281

    Article  CAS  Google Scholar 

  • Cox EF, Ribes M, Kinzie RAI (2006) Temporal and spatial scaling of planktonic responses to nutrient inputs into a subtropical embayment. Mar Ecol Prog Ser 324:19–35

    Article  CAS  Google Scholar 

  • Cunning R, Baker AC (2014) Not just who, but how many: the importance of partner abundance in reef coral symbioses. Front Microbiol 5:400–410

    Article  PubMed  PubMed Central  Google Scholar 

  • Cunning R, Ritson-Williams R, Gates RD (2016) Patterns of bleaching and recovery of Montipora capitata in Kāne‘ohe Bay, Hawai‘i, USA. Mar Ecol Prog Ser 551:131–139

    Article  CAS  Google Scholar 

  • De Carlo EH, Hoover DJ, Young CW, Hoover RS, Mackenzie FT (2007) Impact of storm runoff from tropical watersheds on coastal water quality and productivity. Appl Geochem 22:1777–1797

    Article  CAS  Google Scholar 

  • Dennison WC, Barnes DJ (1988) Effect of water motion on coral photosynthesis and calcification. J Exp Mar Bio Ecol 115:67–77

    Article  Google Scholar 

  • Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV (2015) Genomic determinants of coral heat tolerance across latitudes. Science 348:1460–1462

    Article  CAS  PubMed  Google Scholar 

  • Douglas B, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Google Scholar 

  • Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543

    Article  CAS  PubMed  Google Scholar 

  • Drupp P, De Carlo EH, Mackenzie FT, Bienfang P, Sabine CL (2011) Nutrient inputs, phytoplankton response, and CO2 variations in a semi-enclosed subtropical embayment, Kaneohe Bay, Hawaii. Aquat Geochem 17:473–498

    Article  CAS  Google Scholar 

  • Drupp PS, De Carlo EH, Mackenzie FT, Sabine CL, Feely RA, Shamberger KE (2013) Comparison of CO2 dynamics and air-sea gas exchange in differing tropical reef environments. Aquat Geochem 19:371–397

    Article  CAS  Google 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 20:201–210

    Google Scholar 

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

    Article  Google Scholar 

  • Ellner SP, Jones LE, Mydlarz LD, Harvell CD (2007) Within-host disease ecology in the sea fan Gorgonia ventalina: modeling the spatial immunodynamics of a coral-pathogen interaction. Am Nat 170:E143–E161

    Article  PubMed  Google Scholar 

  • Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169

    Article  CAS  Google Scholar 

  • Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685

    Article  CAS  Google Scholar 

  • Fitt W, Brown B, Warner M, Dunne R (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65

    Article  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 

  • 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 96:3–15

    Article  PubMed  Google Scholar 

  • Gibbin EM, Putnam HM, Gates RD, Nitschke MR, Davy SK (2015) Species-specific differences in thermal tolerance may define susceptibility to intracellular acidosis in reef corals. Mar Biol 162:717–723

    Article  CAS  Google Scholar 

  • Gibbin EM, Chakravarti LJ, Jarrold MD, Christen F, Turpin V, N’Siala GM, Blier PU, Calosi P (2017) Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life history and physiology in a marine metazoan? J Exp Biol 220:551–563

    Article  PubMed  Google 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 115–120

  • Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7:e33353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heron SF, Maynard JA, van Hooidonk R, Mark Eakin C (2016) Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Sci Rep 6:srep38402

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation, mechanism and process in physiological evolution. Oxford University Press, New York

    Google Scholar 

  • Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86

    Article  Google Scholar 

  • Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S (2017) Coral reef ecosystems under climate change and ocean acidification. Front Mar Sci 4:158

    Article  Google Scholar 

  • Hubbard DK (2015) Reef biology and geology—not just a matter of scale. In: Birkeland C (ed) Coral reefs in the anthropocene. Springer, Dordrecht, pp 43–66

    Chapter  Google Scholar 

  • Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC, Kleypas J, van de Leemput IA, Lough JM, Morrison TH, Palumbi SR, van Nes EH, Scheffer M (2017) Coral reefs in the anthropocene. Nature 546:82–90

    Article  CAS  PubMed  Google 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 113:4416–4421

    Article  CAS  PubMed  PubMed Central  Google 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 pp

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    Article  CAS  Google Scholar 

  • Jokiel PL, Brown EK (2004) Global warming, regional trends and inshore environmental conditions influence coral bleaching in Hawaii. Glob Change Biol 10:1627–1641

    Article  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99

    Article  CAS  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230

    Article  CAS  Google Scholar 

  • 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:e34659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenkel CD, Matz MV (2016) Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat Ecol Evol 1:14

    Article  PubMed  Google 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:e26914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV (2013a) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22:4335–4348

    Article  CAS  PubMed  Google Scholar 

  • Kenkel CD, Meyer E, Matz MV (2013b) Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Mol Ecol 22:4322–4334

    Article  CAS  PubMed  Google Scholar 

  • Kenkel CD, Moya A, Strahl J, Humphrey C, Bay LK (2017) Functional genomic analysis of corals from natural CO2-seeps reveals core molecular responses involved in acclimatization to ocean acidification. Glob Change Biol. https://doi.org/10.1111/gcb.13833

    Google 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

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  • Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252

    Article  Google Scholar 

  • Levin RA, Beltran VH, Hill R, Kjelleberg S, McDougald D, Steinberg PD, van Oppen MJH (2016) Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Mol Biol Evol 33:2201–2215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long MH, Rheuban JE, Berg P, Zieman JC (2012) A comparison and correction of light intensity loggers to photosynthetically active radiation sensors. Limnol Oceanogr Methods 10:416–424

    Article  Google Scholar 

  • Louis YD, Bhagooli R, Kenkel CD, Baker AC, Dyall SD (2017) Gene expression biomarkers of heat stress in scleractinian corals: promises and limitations. Comp Biochem Physiol C Toxicol Pharmacol 191:63–77

    Article  CAS  PubMed  Google Scholar 

  • Lowe RJ, Falter JL, Monismith SG, Atkinson MJ (2009) A numerical study of circulation in a coastal reef-lagoon system. J Geophys Res 114:C06022

    Article  Google Scholar 

  • Mayfield AB, Chan P-H, Putnam HM, Chen C-S, Fan T-Y (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 215:4183–4195

    Article  CAS  PubMed  Google Scholar 

  • Maynard JA, Anthony KRN, Marshall PA, Masiri I (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar Biol 155:173–182

    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 

  • Middlebrook R, Anthony KRN, Hoegh-Guldberg O, Dove S (2010) Heating rate and symbiont productivity are key factors determining thermal stress in the reef-building coral Acropora formosa. J Exp Biol 213:1026–1034

    Article  CAS  PubMed  Google Scholar 

  • Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925

    Article  Google Scholar 

  • Morrow KM, Bourne DG, Humphrey C, Botté ES, Laffy P, Zaneveld J, Uthicke S, Fabricius KE, Webster NS (2015) Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J 9:894–908

    Article  CAS  PubMed  Google Scholar 

  • Mydlarz LD, Palmer CV (2011) The presence of multiple phenoloxidases in Caribbean reef-building corals. Comp Biochem Physiol A Mol Integr Physiol 159:372–378

    Article  PubMed  CAS  Google Scholar 

  • Mydlarz LD, Holthouse SF, Peters EC, Harvell CD (2008) Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. PLoS One 3:e1811

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mydlarz LD, Couch CS, Weil E, Smith G, Harvell CD (2009) Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis Aquat Organ 87:67–78

    Article  CAS  PubMed  Google Scholar 

  • Mydlarz LD, McGinty ES, Harvell CD (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945

    Article  PubMed  Google Scholar 

  • Nakamura T, van Woesik R (2001) Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar Ecol Prog Ser 212:301–304

    Article  Google Scholar 

  • Nappi AJ, Christensen BM (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol 35:443–459

    Article  CAS  PubMed  Google Scholar 

  • Nappi AJ, Vass E (1993) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res 6:117–126

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Noonan SHC, Fabricius KE (2016) Ocean acidification affects productivity but not the severity of thermal bleaching in some tropical corals. ICES J Mar Sci 73:715–726

    Article  Google Scholar 

  • Ortonne J-P (2002) Photoprotective properties of skin melanin. Br J Dermatol 61:7–10

    Article  Google Scholar 

  • 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 1–24

    Google Scholar 

  • Padilla-Gamiño JL, Gaitán-Espitia JD, Kelly MW, Hofmann GE (2016) Physiological plasticity and local adaptation to elevated pCO2 in calcareous algae: an ontogenetic and geographic approach. Evol Appl 9:1043–1053

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palmer CV, Traylor-Knowles N (2012) Towards an integrated network of coral immune mechanisms. Proc Biol Sci 279:4106–4114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer CV, Modi CK, Mydlarz LD (2009) Coral fluorescent proteins as antioxidants. PLoS One 4:e7298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palmer CV, Bythell JC, Willis BL (2010) Levels of immunity parameters underpin bleaching and disease susceptibility of reef corals. FASEB J 24:1935–1946

    Article  CAS  PubMed  Google Scholar 

  • Palmer CV, McGinty ES, Cummings DJ, Smith SM, Bartels E, Mydlarz LD (2011a) Patterns of coral ecological immunology: variation in the responses of Caribbean corals to elevated temperature and a pathogen elicitor. J Exp Biol 214:4240–4249

    Article  CAS  PubMed  Google Scholar 

  • Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC (2011b) Corals use similar immune cells and wound-healing processes as those of higher organisms. PLoS One 6:e23992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898

    Article  CAS  PubMed  Google Scholar 

  • Pandolfi JM, Kiessling W (2014) Gaining insights from past reefs to inform understanding of coral reef response to global climate change. Curr Opin Environ Sustain 7:52–58

    Article  Google Scholar 

  • Putnam HM, Davidson JM, Gates RD (2016) Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol Appl 9:1165–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Putnam HM, Barott KL, Ainsworth TD, Gates RD (2017) The vulnerability and resilience of reef-building corals. Curr Biol 27:R528–R540

    Article  CAS  PubMed  Google 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

  • Rautio M, Korhola A (2002) UV-induced pigmentation in subarctic Daphnia. Limnol Oceanogr 47:295–299

    Article  CAS  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882

    Article  Google Scholar 

  • 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 2017

  • Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105:10444–10449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shamberger KEF, Feely RA, Sabine CL, Atkinson MJ, DeCarlo EH, Mackenzie FT, Drupp PS, Butterfield DA (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75

    Article  CAS  Google Scholar 

  • Söderhäll K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28

    Article  PubMed  Google Scholar 

  • Stat M, Bird CE, Pochon X, Chasqui L, Chauka LJ, Concepcion GT, Logan D, Takabayashi M, Toonen RJ, Gates RD (2011) Variation in Symbiodinium ITS2 sequence assemblages among coral colonies. PLoS One 6:e15854

    Article  CAS  PubMed  PubMed Central  Google 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 3:1317–1329

    Article  PubMed  PubMed Central  Google Scholar 

  • Stat M, Yost DM, Gates RD (2015) Geographic structure and host specificity shape the community composition of symbiotic dinoflagellates in corals from the Northwestern Hawaiian Islands. Coral Reefs 34:1075–1086

    Article  Google Scholar 

  • Stimson J, Kinzie RA III (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 

  • Sugumaran M (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res 15:2–9

    Article  CAS  PubMed  Google 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 2017

  • Tanner CA, Burnett LE, Burnett KG (2006) The effects of hypoxia and pH on phenoloxidase activity in the Atlantic blue crab, Callinectes sapidus. Comp Biochem Physiol A Mol Integr Physiol 144:218–223

    Article  PubMed  CAS  Google 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 7:627–636

    Article  Google Scholar 

  • van Vuuren DP, Edmonds J, Kainuma M, Riahi K, Thomson A, Hibbard K, Hurtt GC, Kram T, Krey V, Lamarque J-F, Masui T, Meinshausen M, Nakicenovic N, Smith SJ, Rose SK (2011) The representative concentration pathways: an overview. Clim Change 109:5–31

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S-PLUS, 4th edn. Springer, New York

    Book  Google Scholar 

  • Vijayan V, Jasmin C, Anas A, Kuttan PS, Vinothkumar S, Subrayan PP, Nair S (2017) Sponge-associated bacteria produce non-cytotoxic melanin which protects animal cells from photo-toxicity. Appl Biochem Biotechnol 183:396–411

    Article  CAS  PubMed  Google Scholar 

  • Wall CB, Fan T-Y, Edmunds PJ (2014) Ocean acidification has no effect on thermal bleaching in the coral Seriatopora caliendrum. Coral Reefs 33:119–130

    Article  Google Scholar 

  • Wall CB, Mason RAB, Ellis WR, Cunning R, Gates RD (2017) Elevated pCO2 affects tissue biomass composition, but not calcification, in a reef coral under two light regimes. R Soc Open Sci 4:170683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wangpraseurt D, Larkum AWD, Ralph PJ, Kühl M (2012) Light gradients and optical microniches in coral tissues. Front Microbiol 3:316

    Article  PubMed  PubMed Central  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warner ME, Lesser MP, Ralph PJ (2010) Chlorophyll fluorescence in reef building corals. In: Suggett DJ, Borowitzka MA, Prášil O (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 209–222

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wham DC, Ning G, LaJeunesse TC (2017) Symbiodinium glynnii sp. nov., a species of stress-tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the Pacific Ocean. Phycologia 56:396–409

    Article  Google Scholar 

  • Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, Achterberg EP (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:160–164

    Article  CAS  Google Scholar 

  • Zeebe RE (2012) History of seawater carbonate chemistry, atmospheric CO2, and ocean acidification. Annu Rev Earth Planet Sci 40:141–165

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher B. Wall.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: R. Hill.

Reviewed by C. Palmer and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wall, C.B., Ricci, C.A., Foulds, G.E. et al. The effects of environmental history and thermal stress on coral physiology and immunity. Mar Biol 165, 56 (2018). https://doi.org/10.1007/s00227-018-3317-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3317-z

Navigation