Abstract
This study tested the interactive effects of increased seawater temperature and CO2 partial pressure (pCO2) on the photochemistry, bleaching, and early growth of the reef coral Pocillopora damicornis. New recruits were maintained at ambient or high temperature (29 or 30.8 °C) and pCO2 (~ 500 and ~ 1100 μatm) in a full-factorial experiment for 3 weeks. Neither a sharp decline in photochemical efficiency (Fv/Fm) nor evident bleaching was observed at high temperature and/or high pCO2. Furthermore, elevated temperature greatly promoted lateral growth and calcification, while polyp budding exhibited temperature-dependent responses to pCO2. High pCO2 depressed calcification by 28% at ambient temperature, but did not impact calcification at 30.8 °C. Interestingly, elevated temperature in concert with high pCO2 significantly retarded the budding process. These results suggest that increased temperature can mitigate the adverse effects of acidification on the calcification of juvenile P. damicornis, but at a substantial cost to asexual budding.
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References
Albright R, Mason B, Langdon C (2008) Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs 27:485–490
Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci U S A 107:20400–20404
Anlauf H, D’Croz L, O’Dea A (2011) A corrosive concoction: the combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative. J Exp Mar Bio Ecol 397:13–20
Anthony K, Connolly SR, Willis BL (2002) Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol Oceanogr 47:1417–1429
Anthony K, Kline D, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446
Baghdasarian G, Osberg A, Mihora D, Putnam H, Gates RD, Edmunds PJ (2017) Effects of temperature and pCO2 on population regulation of Symbiodinium spp. in a tropical reef coral. Biol Bull 232:123–139
Brading P, Warner ME, Smith DJ, Suggett DJ (2013) Contrasting modes of inorganic carbon acquisition amongst Symbiodinium (Dinophyceae) phylotypes. New Phytol 200:432–442
Brading P, Warner ME, Davey P, Smith DJ, Achterberg EP, Suggett DJ (2011) Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol Oceanogr 56:927–938
Brennand HS, Soars N, Dworjanyn SA, Davis AR, Byrne M (2010) Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS One 5:e11372
Byrne M, Foo S, Soars NA, Wolfe KDL, Nguyen HD, Hardy N, Dworjanyn SA (2013) Ocean warming will mitigate the effects of acidification on calcifying sea urchin larvae (Heliocidaris tuberculata) from the Australian global warming hot spot. J Exp Mar Bio Ecol 448:250–257
Byrne M, Ho M, Wong E, Soars NA, Selvakumaraswamy P, Shepard-Brennand H, Dworjanyn SA, Davis AR (2011) Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proc R Soc Lond B Biol Sci 278:2376–2383
Cohen AL, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127
Cohen AL, McCorkle DC, de Putron S, Gaetani GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification. Geochem Geophy Geosy 10:Q07005
Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2013) The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point. Limnol Oceanogr 58:388–398
Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014a) Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations. Limnol Oceanogr 59:1081–1091
Comeau S, Carpenter RC, Nojiri Y, Putnam HM, Sakai K, Edmunds PJ (2014b) Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proc R Soc Lond B Biol Sci 281:20141339
Cooper TF, Ulstrup KE (2009) Mesoscale variation in the photophysiology of the reef building coral Pocillopora damicornis along an environmental gradient. Estuar Coast Shelf Sci 83:186–196
Cumbo VR, Edmunds PJ, Wall CB, Fan T-Y (2013) Brooded coral larvae differ in their response to high temperature and elevated pCO2 depending on the day of release. Mar Biol 160:2903–2917
de Putron SJ, McCorkle DC, Cohen AL, Dillon AB (2010) The impact of seawater saturation state and bicarbonate ion concentration on calcification by new recruits of two Atlantic corals. Coral Reefs 30:321–328
Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 348:161–172
Dimond JL, Kerwin AH, Rotjan R, Sharp K, Stewart FJ, Thornhill DJ (2013) A simple temperature-based model predicts the upper latitudinal limit of the temperate coral Astrangia poculata. Coral Reefs 32:401–409
Donelson JM, Munday PL, McCormick MI, Pitcher CR (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30–32
Dunne RP (2010) Synergy or antagonism-interactions between stressors on coral reefs. Coral Reefs 29:145–152
Edmunds PJ (2012) Effect of pCO2 on the growth, respiration, and photophysiology of massive Porites spp. in Moorea. French Polynesia. Mar Biol 159:2149–2160
Edmunds PJ, Brown D, Moriarty V (2012) Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Glob Chang Biol 18:2173–2183
Erez J, Reynaud S, Silverman J, Schneider K, Allemand D (2011) Coral calcification under ocean acidification and global change. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer Netherlands, Dordrecht, pp 151–176
Foster T, Falter JL, Mcculloch MT, Clode PL (2016) Ocean acidification causes structural deformities in juvenile coral skeletons. Sci Adv 2:e1501130
Foster T, Gilmour JP, Chua CM, Falter JL, Mcculloch MT (2015) Effect of ocean warming and acidification on the early life stages of subtropical Acropora spicifera. Coral Reefs 34:1217–1226
Gattuso J-P, Magnan A, Billé R, Cheung WWL, Howes EL, Joos F, Allemand D, Bopp L, Cooley SR, Eakin CM, Hoegh-Guldberg O, Kelly RP, Pörtner H-O, Rogers AD, Baxter JM, Laffoley D, Osborn D, Rankovic A, Rochette J, Sumaila UR, Treyer S, Turley C (2015) Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349:aac742
Graham EM, Baird AH, Willis BL, Connolly SR (2013) Effects of delayed settlement on post-settlement growth and survival of scleractinian coral larvae. Oecologia 173:431–438
Hoadley KD, Rollison D, Pettay DT, Warner ME (2015a) Differential carbon utilization and asexual reproduction under elevated pCO2 conditions in the model anemone, Exaiptasia pallida, hosting different symbionts. Limnol Oceanogr 60:2108–2120
Hoadley KD, Pettay DT, Dodge D, Warner ME (2016a) Contrasting physiological plasticity in response to environmental stress within different cnidarians and their respective symbionts. Coral Reefs 35:529–542
Hoadley KD, Pettay DT, Grottoli AG, Cai W-J, Melman TF, Schoepf V, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann JH, Warner ME (2015b) Physiological response to elevated temperature and pCO2 varies across four Pacific coral species: understanding the unique host+symbiont response. Sci Rep 5:18371
Hoadley KD, Pettay DT, Grottoli AG, Cai W-J, Melman TF, Levas S, Schoepf V, Ding Q, Yuan X, Wang Y, Matsui Y, Baumann JH, Warner ME (2016b) High-temperature acclimation strategies within the thermally tolerant endosymbiont Symbiodinium trenchii and its coral host, Turbinaria reniformis, differ with changing pCO2 and nutrients. Mar Biol 163:134
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hoegh-Guldberg O, Mumby P, Hooten A, Steneck R, Greenfield P, Gomez E, Harvell C, Sale P, Edwards A, Caldeira K (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120
Huang H, Yuan XC, Cai WJ, Zhang CL, Li X, Liu S (2014) Positive and negative responses of coral calcification to elevated pCO2: case studies of two coral species and the implications of their responses. Mar Ecol Prog Ser 502:145–156
Hughes TP, Ayre D, Connell JH (1992) The evolutionary ecology of corals. Trends Ecol Evol 7:292–295
Humanes A, Noonan SH, Willis BL, Fabricius KE, Negri AP (2016) Cumulative effects of nutrient enrichment and elevated temperature compromise the early life history stages of the coral Acropora tenuis. PLoS One 11:e0161616
Inoue M, Shinmen K, Kawahata H, Nakamura T, Tanaka Y, Kato A, Shinzato C, Iguchi A, Kan H, Suzuki A (2012) Estimate of calcification responses to thermal and freshening stresses based on culture experiments with symbiotic and aposymbiotic primary polyps of a coral, Acropora digitifera. Glob Planet Change 92–93:1–7
Jiang L, Huang H, Yuan XC, Yuan T, Zhang YY, Wen KC, Li XB, Zhou GW (2015) Effects of elevated pCO2 on the post-settlement development of Pocillopora damicornis. J Exp Mar Bio Ecol 473:169–175
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
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
Klein SG, Pitt KA, Carroll AR (2017a) Pre-exposure to simultaneous, but not individual, climate change stressors limits acclimation capacity of Irukandji jellyfish polyps to predicted climate scenarios. Coral Reefs 36:987–1000
Klein SG, Pitt KA, Rathjen KA, Seymour JE (2014) Irukandji jellyfish polyps exhibit tolerance to interacting climate change stressors. Glob Chang Biol 20:28–37
Klein SG, Pitt KA, Nitschke MR, Goyen S, Welsh DT, Suggett DJ, Carroll AR (2017b) Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian. Glob Chang Biol 23:3690–3703
Lewis E, Wallace D, Allison LJ (1998) Program developed for CO2 system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Tennessee
Li X, Liu S, Huang H, Huang L, Jing Z, Zhang C (2012) Coral bleaching caused by an abnormal water temperature rise at Luhuitou fringing reef, Sanya Bay, China. Aquat Ecosyst Health Manag 15:227–233
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
McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627
Nemzer BV, Dickson AG (2005) The stability and reproducibility of Tris buffers in synthetic seawater. Mar Chem 96:237–242
Nitschke MR, Davy SK, Cribb TH, Ward S (2015) The effect of elevated temperature and substrate on free-living Symbiodinium cultures. Coral Reefs 34:161–171
Ohki S, Irie T, Inoue M, Shinmen K, Kawahata H, Nakamura T, Kato A, Nojiri Y, Suzuki A, Sakai K (2013) Calcification responses of symbiotic and aposymbiotic corals to near-future levels of ocean acidification. Biogeosciences 10:6807–6814
Parker LM, O’Connor WA, Raftos DA, Pörtner H-O, Ross PM (2015) Persistence of positive carryover effects in the oyster, Saccostrea glomerata, following transgenerational exposure to ocean acidification. PLoS One 10:e0132276
Penin L, Adjeroud M (2013) Relative importance of recruitment and post-settlement processes in the maintenance of coral assemblages in an insular, fragmented reef system. Mar Ecol Prog Ser 473:149–162
Putnam HM, Gates RD (2015) Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol 218:2365–2372
Putnam HM, Mayfield AB, Fan TY, Chen CS, Gates RD (2013) 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 160:2157–2173
Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, Melbourne, Australia
Rodolfo-Metalpa R, Peirano A, Houlbrèque F, Abbate M, Ferrier-Pagès C (2008) Effects of temperature, light and heterotrophy on the growth rate and budding of the temperate coral Cladocora caespitosa. Coral Reefs 27:17–25
Schoepf V, Grottoli AG, Warner ME, Cai W-J, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann JH (2013) Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS One 8:e75049
Siebeck U, Marshall N, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460
Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53:597–608
Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT, Warner ME, Ralph PJ (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381
Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Chang Biol 21:2261–2271
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
Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc Lond B Biol Sci 275:1767–1773
Woolsey E, Keith S, Byrne M, Schmidt-Roach S, Baird A (2015) Latitudinal variation in thermal tolerance thresholds of early life stages of corals. Coral Reefs 34:471–478
Yan H, Yu K, Shi Q, Tan Y, Liu G, Zhao M, Li S, Chen T, Wang Y (2016) Seasonal variations of seawater pCO2 and sea–air CO2 fluxes in a fringing coral reef, northern South China Sea. J Geophys Res Oceans 121:998–1008
Zhang C, Huang H, Ye C, Huang L, Li X, Lian J, Liu S (2013) Diurnal and seasonal variations of carbonate system parameters on Luhuitou fringing reef, Sanya Bay, Hainan Island, South China Sea. Deep Sea Res Part II Top Stud Oceanogr 96:65–74
Zhou GW (2011) Study on diversity of Symbiodinium and flexibility in scleractinian coral-algal symbiosis. Ph.D. thesis, Graduate School of Chinese Academy of Sciences, p 127
Acknowledgements
This work was funded by the National Natural Science Foundation of China (U1301232 and 41206140), Science and Technology Service Network Initiative (KFJ-EW-STS-123) and Science and Technology Planning Project of Guangdong Province, China (2014B030301064). We are grateful to Dr. Paul Cooper and the reviewers for their valuable and constructive comments that vastly improved the manuscript.
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Jiang, L., Zhang, F., Guo, ML. et al. Increased temperature mitigates the effects of ocean acidification on the calcification of juvenile Pocillopora damicornis, but at a cost. Coral Reefs 37, 71–79 (2018). https://doi.org/10.1007/s00338-017-1634-1
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DOI: https://doi.org/10.1007/s00338-017-1634-1