Coral Reefs

, Volume 37, Issue 1, pp 71–79 | Cite as

Increased temperature mitigates the effects of ocean acidification on the calcification of juvenile Pocillopora damicornis, but at a cost

  • Lei Jiang
  • Fang Zhang
  • Ming-Lan Guo
  • Ya-Juan Guo
  • Yu-Yang Zhang
  • Guo-Wei Zhou
  • Lin Cai
  • Jian-Sheng Lian
  • Pei-Yuan Qian
  • Hui Huang


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.


Acidification Temperature Calcification Budding Trade-off Pocillopora damicornis 



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.

Supplementary material

338_2017_1634_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 kb)


  1. Albright R, Mason B, Langdon C (2008) Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs 27:485–490CrossRefGoogle Scholar
  2. 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 107:20400–20404CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 397:13–20CrossRefGoogle Scholar
  4. Anthony K, Connolly SR, Willis BL (2002) Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol Oceanogr 47:1417–1429CrossRefGoogle Scholar
  5. 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 105:17442–17446CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 232:123–139CrossRefPubMedGoogle Scholar
  7. Brading P, Warner ME, Smith DJ, Suggett DJ (2013) Contrasting modes of inorganic carbon acquisition amongst Symbiodinium (Dinophyceae) phylotypes. New Phytol 200:432–442CrossRefPubMedGoogle Scholar
  8. 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 56:927–938CrossRefGoogle Scholar
  9. 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:e11372CrossRefGoogle Scholar
  10. 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 448:250–257CrossRefGoogle Scholar
  11. 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 278:2376–2383CrossRefGoogle Scholar
  12. Cohen AL, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127CrossRefGoogle Scholar
  13. 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:Q07005CrossRefGoogle Scholar
  14. 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 58:388–398CrossRefGoogle Scholar
  15. 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 59:1081–1091CrossRefGoogle Scholar
  16. 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 281:20141339CrossRefGoogle Scholar
  17. 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 83:186–196CrossRefGoogle Scholar
  18. 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 160:2903–2917CrossRefGoogle Scholar
  19. 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 30:321–328CrossRefGoogle Scholar
  20. Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 348:161–172CrossRefGoogle Scholar
  21. 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 32:401–409CrossRefGoogle Scholar
  22. Donelson JM, Munday PL, McCormick MI, Pitcher CR (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30–32CrossRefGoogle Scholar
  23. Dunne RP (2010) Synergy or antagonism-interactions between stressors on coral reefs. Coral Reefs 29:145–152CrossRefGoogle Scholar
  24. Edmunds PJ (2012) Effect of pCO2 on the growth, respiration, and photophysiology of massive Porites spp. in Moorea. French Polynesia. Mar Biol 159:2149–2160CrossRefGoogle Scholar
  25. 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 18:2173–2183CrossRefGoogle Scholar
  26. 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 151–176CrossRefGoogle Scholar
  27. Foster T, Falter JL, Mcculloch MT, Clode PL (2016) Ocean acidification causes structural deformities in juvenile coral skeletons. Sci Adv 2:e1501130CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 34:1217–1226CrossRefGoogle Scholar
  29. 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:aac742CrossRefGoogle Scholar
  30. Graham EM, Baird AH, Willis BL, Connolly SR (2013) Effects of delayed settlement on post-settlement growth and survival of scleractinian coral larvae. Oecologia 173:431–438CrossRefPubMedGoogle Scholar
  31. 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 60:2108–2120CrossRefGoogle Scholar
  32. 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 35:529–542CrossRefGoogle Scholar
  33. 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 5:18371CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 163:134CrossRefGoogle Scholar
  35. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  36. 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 318:1737–1742CrossRefPubMedGoogle Scholar
  37. 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 2:116–120CrossRefGoogle Scholar
  38. 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 502:145–156CrossRefGoogle Scholar
  39. Hughes TP, Ayre D, Connell JH (1992) The evolutionary ecology of corals. Trends Ecol Evol 7:292–295CrossRefPubMedGoogle Scholar
  40. 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:e0161616CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 92–93:1–7CrossRefGoogle Scholar
  42. 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 473:169–175CrossRefGoogle Scholar
  43. 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 21:1219–1230CrossRefGoogle Scholar
  44. 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:e34659CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 36:987–1000CrossRefGoogle Scholar
  46. Klein SG, Pitt KA, Rathjen KA, Seymour JE (2014) Irukandji jellyfish polyps exhibit tolerance to interacting climate change stressors. Glob Chang Biol 20:28–37CrossRefPubMedGoogle Scholar
  47. 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 23:3690–3703CrossRefPubMedGoogle Scholar
  48. 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, TennesseeCrossRefGoogle Scholar
  49. 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 15:227–233CrossRefGoogle Scholar
  50. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  51. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627CrossRefGoogle Scholar
  52. Nemzer BV, Dickson AG (2005) The stability and reproducibility of Tris buffers in synthetic seawater. Mar Chem 96:237–242CrossRefGoogle Scholar
  53. Nitschke MR, Davy SK, Cribb TH, Ward S (2015) The effect of elevated temperature and substrate on free-living Symbiodinium cultures. Coral Reefs 34:161–171CrossRefGoogle Scholar
  54. 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 10:6807–6814CrossRefGoogle Scholar
  55. 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:e0132276CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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 473:149–162CrossRefGoogle Scholar
  57. 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 218:2365–2372CrossRefPubMedGoogle Scholar
  58. 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 160:2157–2173CrossRefGoogle Scholar
  59. Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, Melbourne, AustraliaCrossRefGoogle Scholar
  60. 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 27:17–25CrossRefGoogle Scholar
  61. 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:e75049CrossRefPubMedPubMedCentralGoogle Scholar
  62. Siebeck U, Marshall N, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460CrossRefGoogle Scholar
  63. Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53:597–608CrossRefPubMedGoogle Scholar
  64. 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 208:370–381CrossRefPubMedGoogle Scholar
  65. Thor P, Dupont S (2015) Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Chang Biol 21:2261–2271CrossRefPubMedGoogle Scholar
  66. Wall CB, Fan T-Y, Edmunds PJ (2014) Ocean acidification has no effect on thermal bleaching in the coral Seriatopora caliendrum. Coral Reefs 33:119–130CrossRefGoogle Scholar
  67. Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc Lond B Biol Sci 275:1767–1773CrossRefGoogle Scholar
  68. 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 34:471–478CrossRefGoogle Scholar
  69. 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 121:998–1008CrossRefGoogle Scholar
  70. 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 96:65–74CrossRefGoogle Scholar
  71. 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 127Google Scholar

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© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine BiologySouth China Sea Institute of Oceanology, CASGuangzhouChina
  2. 2.Tropical Marine Biological Research Station in HainanCASSanyaChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.Shenzhen Research Institute and Division of Life ScienceHong Kong University of Science and TechnologyHong Kong SARChina

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