The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2

Marine Biology

Volumn 160, Issue 8, 2013, Pages 2157-2173

  Putnam, H M ^a   Mayfield, A B ^b   Fan, T Y ^b,c   Chen, C S ^b,c,d   Gates, R D ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b NATIONAL MUSEUM OF MARINE BIOLOGY AND AQUARIUM   (Taiwan)

^c NATIONAL DONG HWA UNIVERSITY   (Taiwan)

^d NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACCLIMATION; ACIDIFICATION; BODY SIZE; CARBON DIOXIDE; CORAL REEF; ENVIRONMENTAL CHANGE; GREENHOUSE EFFECT; GREENHOUSE GAS; LARVA; LIFE HISTORY TRAIT; MOLECULAR ECOLOGY; PHYSIOLOGICAL RESPONSE; RESPIRATION; TEMPERATURE EFFECT;

NANWAN BAY; TAIWAN;

ANTHOZOA; POCILLOPORA DAMICORNIS; POCILLOPORIDAE;

EID: 84881249759     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-012-2129-9     Document Type: Article

References (98)

1. Ainsworth TD, Hoegh-Guldberg O, Heron SF, Skirving WJ, Leggat W (2008) Early cellular changes are indicators of pre-bleaching thermal stress in the coral host. J Exp Mar Biol Ecol 364: 63-71. doi: 10. 1016/j. jembe. 2008. 06. 032.
2. Albright R (2011) Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals. J Mar Biol Article ID 473615, pp 14. doi: 10. 1155/2011/473615.
3. Albright R, Langdon C (2011) Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides. Glob Change Biol 17: 2478-2487. doi: 10. 1111/j. 1365-2486. 2011. 02404. x.
4. 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 USA 107: 20400-20404. doi: 10. 1073/pnas. 1007273107.
5. 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 Biol Ecol 397: 13-20. doi: 10. 1016/j. jembe. 2010. 11. 009.
6. 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. doi: 10. 1073/pnas. 0804478105.
7. Aranda M, Banaszak AT, Bayer T, Luyten JR, Medina M, Voolstra CR (2011) Differential sensitivity of coral larvae to natural levels of ultraviolet radiation during the onset of larval competence. Mol Ecol 20: 2955-2972. doi: 10. 1111/j. 1365-294X. 2011. 05153. x.
8. Bassim KM, Sammarco PW (2003) Effects of temperature and ammonium on larval development and survivorship in a scleractinian coral (Diploria strigosa). Mar Biol 142: 241-252. doi: 10. 1007/s00227-002-0953-z.
9. Brown BE, Dunne RP, Goodson S, Douglas AE (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 12: 119-126.
10. Byrne M (2011a) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol Ann Rev 49: 1-42.
11. Byrne M (2011b) Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Environ Res 76: 3-15. doi: 10. 1016/j. marenvres. 2011. 10. 004.
12. Chauvin A, Denis V, Cuet P (2011) Is the response of coral calcification to seawater acidification related to nutrient loading? Coral Reefs 30: 911-923. doi: 10. 1007/s00338-011-0786-7.
13. Coles SL, Brown BE (2003) Coral bleaching-capacity for acclimatization and adaptation. Adv Mar Biol 46: 183-223.
14. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43: 209-216.
15. Crawley A, Kline D, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob Change Biol 16: 851-863. doi: 10. 1111/j. 1365-2486. 2009. 01943. x.
16. Dickson A, Millero F (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34: 1733-1743.
17. 2 measurement. In: Dickson A, Sabine C, Christian J (eds) PICES Special Publication 3.
18. Doney SC, Balch WM, Fabry VJ, Feely RA (2009a) Ocean acidification: a critical emerging problem for the ocean sciences. Oceanography 22: 16-25.
19. 2 problem. Ann Rev Mar Sci 1: 169-192.
20. Donner SD (2009) Coping with commitment: projected thermal stress on coral reefs under different future scenarios. PLoS One 4(6): e5712. doi: 10. 1371/journal. pone. 0005712.
21. Downs CA, Mueller E, Phillips S, Fauth JE, Woodley CM (2000) A molecular biomarker system for assessing the health of coral (Montastraea faveolata) during heat stress. Mar Biotechnol 2: 533-544. doi: 10. 1007/s101260000038.
22. 2? Annu Rev Plant Physiol Plant Mol Biol 48: 609-639. doi: 10. 1146/annurev. arplant. 48. 1. 609.
23. Dupont S, Dorey N, Thorndyke M (2010a) What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? Estuar Coast Shelf Sci 89: 182-185. doi: 10. 1016/j. ecss. 2010. 06. 013.
24. Dupont S, Lundve B, Thorndyke M (2010b) Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. J Exp Zool (Mol Dev Evol) 314B: 382-389.
25. 2-induced acidification in the acoel worm Symsagittiferaroscoffensis. PLoS One 7(1): e29568. doi: 10. 1371/journal. pone. 0029568.
26. Edmunds PJ (2011) Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnol Oceanogr 56: 2402-2410. doi: 10. 4319/lo. 2011. 56. 6. 2402.
27. Edmunds PJ, Gates RD, Gleason DF (2001) The biology of larvae from the reef coral Porites astreoides, and their response to temperature disturbances. Mar Biol 139: 981-989. doi: 10. 1007/s002270100634.
28. Edmunds PJ, Cumbo V, Fan TY (2011) Effects of temperature on the respiration of brooded larvae from tropical reef corals. J Exp Biol 214: 2783-2790. doi: 10. 1242/jeb. 055343.
29. Edmunds PJ, Brown D, Moriarty V (2012) Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Glob Change Biol 18: 2173-2183. doi: 10. 1111/j. 1365-2486. 2012. 02695. x.
30. 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, Berlin, pp 151-176.
31. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De'ath G, Okazaki R, Muehllehner N, Glas M, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1: 165-169. doi: 10. 1038/nclimate1122.
32. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65: 414-432. doi: 10. 1093/icesjms/fsn048.
33. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton pp 484.
34. Fan TY, Li JJ, Ie SX, Fang LS (2002) Lunar periodicity of larval release by pocilloporid corals in southern Taiwan. Zool Stud 41(3): 288-294.
35. Fangue NA, O'Donnell MJ, Sewell MA, Matson PG, MacPherson AC, Hofmann GE (2010) A laboratory-based, experimental system for the study of ocean acidification effects on marine invertebrate larvae. Limnol Oceanogr Methods 8: 441-452. doi: 10: 4319/lom. 2010. 8. 441.
36. Feder ME, Hofmann GE (1999) Heat shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61: 243-282.
37. 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. doi: 10. 1007/s003380100146.
38. Ganot P, Moya A, Magnone V, Allemand D, Furla P, Sabourault C (2011) Adaptations to endosymbiosis in a cnidarian-dinoflagellate association: differential gene expression and specific gene duplications. PLoS Genet 7(7): e1002187. doi: 10. 1371/journal. pgen. 1002187.
39. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440: 1186-1189. doi: 10. 1038/nature04565.
40. Hashimoto K, Shibuno T, Murayama-Kayano E, Tanaka H, Kayano T (2004) Isolation and characterization of stress-responsive genes from the scleractinian coral Pocillopora damicornis. Coral Reefs 23: 485-491. doi: 10. 1007/s00338-004-0410-1.
41. Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, Oxford pp 466.
42. 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. doi: 10. 1126/science. 1152509.
43. Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72: 127-145. doi: 10. 1146/annurev-physiol-021909-135900.
44. Hofmann GE, Buckley BA, Place SP, Zippay ML (2002) Molecular chaperones in ecothermic marine animals: biochemical function and gene expression. Integr Comp Biol 42: 808-814.
45. Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying marine organisms in marine ecosystems: an organism to ecosystem perspective. Annu Rev Ecol Evol Syst 41: 127-147. doi: 10. 1146/annurev. ecolsys. 110308. 120227.
46. Isomura N, Nishihira M (2001) Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals. Coral Reefs 20: 309-315. doi: 10. 1007/s003380100180.
47. Jones RJ, Ward S, Amri AY, Hoegh-Guldberg O (2000) Changes in quantum efficiency of photosystem II of symbiotic dinoflagellates of corals after heat stress and of bleached corals sampled after the 1998 Great Barrier Reef bleaching event. Mar Fresh Res 51: 63-71. doi: 10. 1071/MF99100.
48. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13: 1419-1434. doi: 10. 1111/j. 1461-0248. 2010. 01518. x.
49. 2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373: 275-284. doi: 10. 3354/meps07802.
50. 2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110: C09S07. doi: 10. 1029/2004JC002576.
51. Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon-concentrating mechanism n the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121: 1247-1255.
52. Leggat W, Whitney S, Yellowlees D (2004) Is coral bleaching due to the instability of the zooxanthellae dark reactions? Symbiosis 37: 137-153.
53. Leggat W, Seneca F, Wasmund K, Ukani L, Yellowlees D, Ainsworth TD (2011) Differential responses of the coral host and their algal symbiont to thermal stress. PLoS One 6(10): e26687. doi: 10. 1371/journal. pone. 0026687.
54. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16: 187-192.
55. Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Berlin, pp 405-420.
56. Levy O, Kaniewska P, Alon S, Karako-Lampert S, Bay LK, Reef R, Rodriguez-Lanetty M, Miller DJ, Hoegh-Guldberg O (2011) Complex diel cycles of gene expression in coral-algal symbiosis. Science 331: 175. doi: 10. 1126/science. 1196419.
57. Mayfield AB, Hirst MB, Gates RD (2009) Gene expression normalization in a dual-compartment system: a real-time quantitative polymerase chain reaction protocol for symbiotic anthozoans. Mol Ecol Res 9: 462-470. doi: 10. 1111/j. 1755-0998. 2008. 02349. x.
58. Mayfield AB, Hsiao YY, Fan TY, Chen CS, Gates RD (2010) Evaluating the temporal stability of stress-activated protein kinase and cytoskeleton gene expression in the Pacific corals Pocillopora damicornis and Seriatopora hystrix. J Exp Mar Biol Ecol 395: 215-222. doi: 10. 1016/j. jembe. 2010. 09. 007.
59. Mayfield AB, Wang LH, Tang PC, Fan TY, Hsiao YY, Tsai CL, Chen CS (2011) Assessing the impacts of experimentally elevated temperature on the biological composition and molecular chaperone gene expression of a reef coral. PLoS One 6(10): e26529. doi: 10. 1371/journal. pone. 0026529.
60. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18: 897-907.
61. Meinshausen M, Smith SJ, Calvin K, Daniel JS, Kainuma MLT, Lamarque J-F, Matsumoto K, Montzka SA, Raper SCB, Riahi K, Thomson A, Velders GJM, van Vuuren DPP (2011) The RPC greenhouse gas concentrations and their extensions from 1765 to 2300. Clim Change 109: 213-241. doi: 10. 1007/s10584-011-0156-z.
62. 2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6: 2313-2331.
63. Meyer E, Aglyamova GV, Matz MV (2011) Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol Ecol 20: 3599-3616. doi: 10. 1111/j. 1365-294X. 2011. 05205. x.
64. 2. Plant Cell Environ 21: 905-915.
65. Moss RH, Edmonds JA, Hibbard KA, Manning MR, Rose SK, van Vuuren DP, Carter TR, Emori S, Kainuma M, Kram T, Meehl GA, Mitchell JFB, Nakicenovic N, Riahi K, Smith SJ, Stouffer RJ, Thomson AM, Weyant JP, Wilbanks TJ (2010) The next generation of scenarios for climate change research and assessment. Nature 463: 747-756. doi: 10. 1038/nature08823.
66. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Døving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci USA 106: 1848-1852. doi: 10. 1073/pnas. 0809996106.
67. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26: 601-611.
68. Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B 222: 181-202.
69. Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition. Mar Biol 100: 185-193.
70. Nakamura M, Morita M, Kurihara H, Mitarai S (2011a) Expression of hsp70, hsp90 and hsf1 in the reef coral Acropora digitifera under prospective acidified conditions over the next several decades. Biol Open BIO2011036. doi: 10. 1242/bio. 2011036.
71. Nakamura M, Ohki A, Suzuki A, Sakai K (2011b) Coral larvae under ocean acidification: survival, metabolism, and metamorphosis. PLoS One 6: e14521. doi: 10. 1371/journal. pone. 0014521.
72. Negri AP, Marshall PA, Heyward AJ (2007) Differing effects of thermal stress on coral fertilization and early embryogenesis in four Indo Pacific species. Coral Reefs 26: 759-763. doi: 10. 1007/s00338-007-0258-2.
73. Pandolfi JM, Jackson JBC, Baron N, Bradbury RH, Guzman HM, Hughes TP, Kappel CV, Micheli F, Possingham HP, Sala E (2005) Are US reefs on the slippery slope to slime? Science 307: 1725-1726. doi: 10. 1126/science. 1104258.
74. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333: 418-422. doi: 10. 1126/science. 1204794.
75. Parker LM, Ross PM, O'Connor WA, Borysko L, Raftos DA, Pörtner H-O (2012) Adult exposure influences offspring response to ocean acidification in oysters. Glob Change Biol 18: 82-92. doi: 10. 1111/j. 1365-2486. 2011. 02520. x.
76. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37: 637-669. doi: 10. 1146/annurev. ecolsys. 37. 091305. 110100.
77. Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ (2008) Rubisco regulation: a role for inhibitors. J Exp Bot 59: 1569-1580. doi: 10. 1093/jxb/ern084.
78. 2 system calculations. ORNL/CDIAC-105a.
79. Pörtner H-O (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Mar Ecol Prog Ser 373: 203-217. doi: 10. 3354/meps07768.
80. Pörtner H-O, Farrell AP (2008) Physiology and climate change. Science 332: 690-691. doi: 10. 1126/science. 1163156.
81. Pörtner H-O, Bennett AF, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman JH (2006) Trade-offs in thermal adaptation: the need for molecular to ecological integration. Phys Biochem Zool 79: 295-313. doi: 10. 1086/499986.
82. Putnam HM, Edmunds PJ, Fan TY (2008) Effect of temperature on the settlement choice and photophysiology of larvae from the reef coral Stylophora pistillata. Biol Bull 215: 135-142.
83. Putnam HM, Edmunds PJ, Fan TY (2010) Effect of a fluctuating thermal regime on adult and larval reef corals. Invertebr Biol 129: 199-209. doi: 10. 1111/j. 17447410. 2010. 00199. x.
84. Randall CJ, Szmant AM (2009) Elevated temperature reduces survivorship and settlement of the larvae of the Caribbean scleractinian coral, Favia fragum (Esper). Coral Reefs 28: 537-545. doi: 10. 1007/s00338-009-0482-z.
85. Riahi K, Rao S, Krey V, Cho C, Chirkov V, Fischer G, Kindermann G, Nakicenovic N, Rafaj P (2011) RCP 8. 5 A scenario of comparatively high greenhouse gas emissions. Clim Change 109: 33-57. doi: 10. 1007/s10584-011-0149-y.
86. Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) (2010) Guide to best practices for ocean acidification research and data reporting. European Commission, Brussels. doi: 10. 2777/58454.
87. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18: 5101-5114. doi: 10. 1111/j. 1365-294X. 2009. 04419. x.
88. 2 induced seawater acidification impacts sea urchin larval development II: gene expression patterns in pluteus larvae. Comp Biochem Physiol A 160: 320-330. doi: 10. 1016/j. cbpa. 2011. 06. 023.
89. 2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comp Biochem Physiol A 160: 331-340. doi: 10. 1016/j. cbpa. 2011. 06. 022.
90. Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6(8): e22881. doi: 10. 1371/journal. pone. 0022881.
91. Szmant AM, Gassman NJ (1990) The effects of prolonged "bleaching" on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8: 217-224.
92. Talmage SC, Gobler CJ (2010) Effects of past, present and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proc Natl Acad Sci USA 107: 17246-17251. doi: 10. 1073/pnas. 0913804107.
93. Talmage SC, Gobler CJ (2011) Effects of elevated temperature and carbon dioxide on the growth and survival of larvae and juveniles of three species of Northwest Atlantic bivalves. PLoS One 6(10): e26941. doi: 10. 1371/journal. pone. 0026941.
94. van Vuuren DP, Meinshausen M, Plattner GK, Joos F, Strassmann KM, Smith SJ, Wigley TML, Raper SCB, Riahi K, de la Chesnaye F, den Elzen MGJ, Fujino J, Jiang K, Nakicenovic N, Paltsev S, Reilly JM (2008) Temperature increase of 21st century mitigation scenarios. Proc Natl Acad Sci USA 105: 15258-15262. doi: 10. 1073/pnas. 0711129105.
95. van Vuuren DP, Edmonds J, Kainuma M, Riahi K, Thomson A, Hibbard K, Hurtt GC, Kram T, Krey V, Lamarque J-F, Masiu T, Meinshausen M, Nakicenovi N, Smith SJ, Rose SK (2011) The representative concentration pathways: an overview. Clim Change 109: 5-31. doi: 10. 1007/s10584-011-0148-z.
96. Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59: 1069-1080. doi: 10. 1093/jxb/erm328.
97. Veron JEN (2011) Ocean acidification and coral reefs: an emerging big picture. Diversity 3: 262-274. doi: 10. 3390/d3020262.
98. Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378: 105-112. doi: 10. 3354/meps07857.