The impact of ocean acidification on reproduction, early development and settlement of marine organisms

Water (Switzerland)

Volumn 3, Issue 4, 2011, Pages 1005-1030

  Ross, Pauline M ^a   Parker, Laura ^a   O'Connor, Wayne A ^b   Bailey, Elizabeth A ^a  

^a UNIVERSITY OF WESTERN SYDNEY   (Australia)

^b Port Stephens Fisheries Centre   (Australia)

Author keywords

Corals; Crustaceans; Echinoderms; Fish; Larvae; Molluscs; Ocean acidification; Reproduction; Review; Settlement; Temperature

Indexed keywords

ACIDIFICATION; ANIMALS; FISH; MARINE BIOLOGY; MOLLUSCS; OCEANOGRAPHY; REVIEWS; TEMPERATURE;

CORALS; CRUSTACEANS; ECHINODERMS; LARVAE; OCEAN ACIDIFICATIONS; REPRODUCTION; SETTLEMENT;

CLIMATE CHANGE;

ANTHOZOA; CRUSTACEA; ECHINODERMATA; INVERTEBRATA; MOLLUSCA;

EID: 84893919162     PISSN: None     EISSN: 20734441     Source Type: Journal    
DOI: 10.3390/w3041005     Document Type: Article

References (129)

1. Caldeira, K.; Wickett, M.E. Anthropogenic carbon and ocean pH. Nature 2003, 425, 365-365
2. Guinotte, J.M.; Fabry, V.J. Ocean acidification and its potential effects on marine ecosystems. Ann. N. Y. Acad. Sci. 2008, 1134, 320-342
3. Turley, C.; Blackford, J.C.; Widdicombe, S.; Lowe, D.; Nightingale, P.D.; Rees, A.P. Reviewing the impact of increased atmospheric CO2 on oceanic pH and the marine ecosystem. In Avoiding Dangerous Climate Change; Schellnhuber, H.J., Cramer, W., Nakicenovic, N., Wigley, T., Yohe, G., Eds.; Cambridge University Press: Cambridge, UK, 2006; pp. 65-70
4. Royal Society. Ocean Acidification due to Increasing Atmospheric Carbon Dioxide. Policy Document 12/05; The Royal Society: London, UK, 2005; pp. 1-58
5. Pörtner, H.O.; Farrell, A.P. Ecology: Physiology and climate change. Science 2008, 322, 690-692
6. Thorson, G. Reproduction and larval ecology of marine bottom invertebrates. Biol. Rev. 1950, 25, 1-45
7. Kurihara, H. Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar. Ecol. Prog. Ser. 2008, 373, 275-284
8. Dupont, S.; Thorndyke, M.C. Impact of CO2-driven ocean acidification on invertebrates early life-history-What we know, what we need to know and what we can do. Biogeosci. Discuss. 2009, 6, 3109-3131
9. Pörtner, H.O.; Langenbuch, M.; Reipschläger, A. Biological impact of elevated ocean CO2 concentrations: Lessons from animal physiology and earth history. J. Oceanogr. 2004, 60, 705-718
10. Przeslawski, R.; Ahyong, S.; Byrne, M.; Wörheide, G.; Hutchings, P. Beyond corals and fish: The effects of climate change on noncoral benthic invertebrates of tropical reefs. Glob. Change Biol. 2008, 14, 2773-2795
11. Kleypas, J.A.; Buddemeier, R.W.; Archer, D.; Gattuso, J.-P.; Langdon, C.; Opdyke, B.N. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 1999, 284, 118-120
12. Gooding, R.A.; Harley, C.D.G.; Tang, E. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proc. Natl. Acad. Sci. USA 2009, 106, 9316-9321
13. Hendriks, I.E.; Duarte, C.M.; álvarez, M. Vulnerability of marine biodiversity to ocean acidification: A meta-analysis. Estuar. Coast. Shelf Sci. 2010, 86, 157-164
14. Dupont, S.; Dorey, N.; Thorndyke, M. What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? Estuar. Coast. Shelf Sci. 2010, 89, 182-185
15. Hendriks, I.E.; Duarte, C.M. Ocean acidification: Separating evidence from judgment-A reply to Dupont et al. Estuar. Coast. Shelf Sci. 2010, 89, 186-190
16. Kroeker, K.J.; Kordas, R.L.; Crim, R.N.; Singh, G.G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 2010, 13, 1419-1434
17. Calabrese, A.; Davis, H.C. The pH tolerance of embryos and larvae of Mercenaria mercenaria and Crassostrea virginica. Biol. Bull. 1966, 131, 427-436
18. Wilson, S.P.; Hyne, R.V. Toxicity of acid-sulfate soil leachate and aluminum to embryos of the Sydney Rock oyster. Ecotoxicol. Environ. Saf. 1997, 37, 30-36
19. Pagano, G.; Cipollaro, M.; Corsale, G. pH-Induced changes in mitotic and developmental patterns in sea urchin embryogenesis. I. Exposure of embryos. Teratog. Carcinog. Mutag. 1985, 5, 101-112
20. Pagano, G.; Cipollaro, M.; Corsale, G. pH-Induced changes in mitotic and developmental patterns in sea urchin embryogenesis. II. Exposure of sperm. Teratog. Carcinog. Mutag. 1985, 5, 113-121
21. Cipollaro, M.; Corsale, G.; Esposito, A. Sublethal pH decrease may cause genetic damage to eukaryotic cell: A study on sea urchins and Salmonella typhimurium. Teratog. Carcinog. Mutag. 1986, 6, 275-287
22. Alvarado-Alvarez, R.; Gould, M.C.; Stephano, J.L. Spawning, in vitro maturation, and changes in oocyte electrophysiology induced by serotonin in Tivela stultorum. Biol. Bull. 1996, 190, 322-328
23. Desrosiers, R.R.; Désilets, J.; Dubé, F. Early developmental events following fertilization in the giant scallop Placopecten magellanicus. Can. J. Fish. Aquat. Sci. 1996, 53, 1382-1392
24. Ishimatsu, A.; Kikkawa, T.; Hayashi, M.; Lee, K.-S.; Kita, J. Effects of CO2 on marine fish: Larvae and adults. J. Oceanogr. 2004, 60, 731-741
25. Brownell, C.L. Water quality requirements for first-feeding in marine fish larvae. II. pH, oxygen, and carbon dioxide. J. Exp. Mar. Biol. Ecol. 1980, 44, 285-298
26. Ross, P.M.; Parker, L.M.; O'Connor, W.A. The impact of ocean acidification on reproduction and early development of marine organisms. Aust. Zool., in press
27. Gattuso, J.P.; Gao, K.; Lee, K.; Rost, B.; Schulz, K.G. Approaches and tools to manipulate the carbonate chemistry. In Guide to Best Practices for Ocean Acidification Research and Data Reporting; Riebesell, U., Fabry, V.J., Hansson, L., Gattuso, J.-P., Eds.; Publications Office of the European Union: Luxembourg, Luxembourg, 2010; pp. 41-51
28. Intergovernmental Panel on Climate Change. The Scientific Basis: Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change; Houghton J.T., Ding, Y., Griggs, D.J., Noguer, M., van der Linden, P.J., Dai, X., Maskell, K., Johnson, C.A., Eds.; Cambridge University Press: Cambridge, UK and New York, NY, USA, 2001; p. 881
29. Intergovernmental Panel on Climate Change. Synthesis Report: Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change; Pachauri R.K., Reisinger, A., Eds.; Intergovernmental Panel on Climate Change: Geneva, Switzerland, 2007; p. 104
30. Caldeira, K.; Wickett, M. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J. Geophys. Res. C 2005, 110, 1-12
31. Orr, J.C.; Fabry, V.J.; Aumont, O.; Bopp, L.; Doney, S.C.; Feely, R.A.; Gnanadesikan, A.; Gruber, N.; Ishida, A.; Joos, F.; et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 2005, 437, 681-686
32. Dupont, S.; Lundve, B.; Thorndyke, M. Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. J. Exp. Zool. Part B 2010, 314 B, 382-389
33. Kurihara, H.; Kato, S.; Ishimatsu, A. Effects of increased seawater pCO2 on early development of the oyster Crassostrea gigas. Aquat. Biol. 2007, 1, 91-98
34. Byrne, M.; Ho, M.; Selvakumaraswamy, P.; Nguyen, H.D.; Dworjanyn, S.A.; Davis, A.R. Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc. R. Soc. B Biol. Sci. 2009, 276, 1883-1888
35. Parker, L.M.; Ross, P.M.; O'Connor, W.A. The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Glob. Change Biol. 2009, 15, 2123-2136
36. Dupont, S.; Ortega-Martínez, O.; Thorndyke, M. Impact of near-future ocean acidification on echinoderms. Ecotoxicology 2010, 19, 449-462
37. Beiras, R.; His, E. Effects of dissolved mercury on embryogenesis, survival, growth and metamorphosis of Crassostrea gigas oyster larvae. Mar. Ecol. Prog. Ser. 1994, 113, 95-104
38. Green, M.A.; Jones, M.E.; Boudreau, C.L.; Moore, R.L.; Westman, B.A. Dissolution mortality of juvenile bivalves in coastal marine deposits. Limnol. Oceanogr. 2004, 49, 727-734
39. Parker, L.M.; Ross, P.M.; O'Connor, W.A. Comparing the effect of elevated pCO2 and temperature on the fertilization and early development of two species of oysters. Mar. Biol. 2010, 157, 2435-2452
40. Gosselin, L.A.; Qian, P.-Y. Juvenile mortality in benthic marine invertebrates. Mar. Ecol. Prog. Ser. 1997, 146, 265-282
41. Impacts of Ocean Acidification. Science Policy Briefing 37; European Science Foundation: Strasbourg, France, 2009; pp. 1-12
42. Moulin, L.; Catarino, A.I.; Claessens, T.; Dubois, P. Effects of seawater acidification on early development of the intertidal sea urchin Paracentrotus lividus (Lamarck 1816). Mar. Pollut. Bull. 2011, 62, 48-54
43. Parker, L.M.; Ross, P.M.; O'Connor, W.A. Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification. Mar. Biol. 2011, 158, 689-697
44. Waldbusser, G.G.; Bergschneider, H.; Green, M.A. Size-dependent pH effect on calcification in post-larval hard clam Mercenaria spp. Mar. Ecol. Prog. Ser. 2010, 417, 171-182
45. Sheppard Brennand, H.; Soars, N.; Dworjanyn, S.A.; Davis, A.R.; Byrne, M. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS One 2010, 5, 1-7
46. Parker, L.M.; Ross, P.M.; Raftos, D.A.; Thompson, E.; O'Connor, W.A. The proteomic response of larvae of the Sydney rock oyster, Saccostrea glomerata to elevated pCO2. Aust. Zool., in press
47. Byrne, M.; Soars, N.; Selvakumaraswamy, P.; Dworjanyn, S.A.; Davis, A.R. Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. Mar. Environ. Res. 2010, 69, 234-239
48. Byrne, M.; Soars, N.A.; Ho, M.A.; Wong, E.; McElroy, D.; Selvakumaraswamy, P.; Dworjanyn, S.A.; Davis, A.R. Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification. Mar. Biol. 2010, 157, 2061-2069
49. Havenhand, J.N.; Schlegel, P. Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences 2009, 6, 3009-3015
50. Kurihara, H.; Ishimatsu, A. Effects of high CO2 seawater on the copepod (Acartia tsuensis) through all life stages and subsequent generations. Mar. Pollut. Bull. 2008, 56, 1086-1090
51. Frommel, A.Y.; Stiebens, V.; Clemmesen, C.; Havenhand, J. Effect of ocean acidification on marine fish sperm (Baltic cod: Gadus morhua). Biogeosci. Discuss. 2010, 7, 5859-5872
52. Kurihara, H.; Shirayama, Y. Effects of increased atmospheric CO2 on sea urchin early development. Mar. Ecol. Prog. Ser. 2004, 274, 161-169
53. Kurihara, H.; Shimode, S.; Shirayama, Y. Sub-lethal effects of elevated concentration of CO2 on planktonic copepods and sea urchins. J. Oceanogr. 2004, 60, 743-750
54. Ericson, J.A.; Lamare, M.D.; Morley, S.A.; Barker, M.F. The response of two ecologically important Antarctic invertebrates (Sterechinus neumayeri and Parborlasia corrugatus) to reduced seawater pH: Effects on fertilisation and embryonic development. Mar. Biol. 2010, 157, 2689-2702
55. Reuter, K.E.; Lotterhos, K.E.; Crim, R.N.; Thompson, C.A.; Harley, C.D.G. Elevated pCO2 increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrotus franciscanus. Global Change Biol. 2011, 17, 163-171
56. Havenhand, J.N.; Buttler, F.-R.; Thorndyke, M.C.; Williamson, J.E. Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr. Biol. 2008, 18, 651-652
57. Kurihara, H.; Asai, T.; Kato, S.; Ishimatsu, A. Effects of elevated pCO2 on early development in the mussel Mytilus galloprovincialis. Aquat. Biol. 2008, 4, 225-233
58. Albright, R.; Mason, B.; Miller, M.; Langdon, C. Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc. Natl. Acad. Sci. USA 2010, 107, 20400-20404
59. Parker, L.M.; Ross, P.M.; O'Connor, W.A.; Borysko, L.; Raftos, D.A.; Portner, H.O. Adult exposure influences offspring response to ocean acidification in oysters. Glob. Change Biol., in press
60. Clark, D.; Lamare, M.; Barker, M. Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: A comparison among a tropical, temperate, and a polar species. Mar. Biol. 2009, 156, 1125-1137
61. Dupont, S.; Havenhand, J.; Thorndyke, W.; Peck, L.; Thorndyke, M. Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar. Ecol. Prog. Ser. 2008, 373, 285-294
62. Gutowska, M.A.; Melzner, F. Abiotic conditions in cephalopod (Sepia officinalis) eggs: Embryonic development at low pH and high pCO2. Mar. Biol. 2009, 156, 515-519
63. Ellis, R.P.; Bersey, J.; Rundle, S.D.; Hall-Spencer, J.M.; Spicer, J.I. Subtle but significant effects of CO2 acidified seawater on embryos of the intertidal snail, Littorina obtusata. Aquat. Biol. 2009, 5, 41-48
64. Watson, S.-A.; Southgate, P.C.; Tyler, P.A.; Peck, L.S. Early larval development of the Sydney rock oyster Saccostrea glomerata under near-future predictions of CO2-driven ocean acidification. J. Shellfish Res. 2009, 28, 431-437
65. Gazeau, F.; Gattuso, J.-P.; Dawber, C.; Pronker, A.E.; Peene, F.; Peene, J.; Heip, C.H.R.; Middelburg, J.J. Effect of ocean acidification on the early life stages of the blue mussel (Mytilus edulis). Biogeosci. Discuss. 2010, 7, 2927-2947
66. Lischka, S.; Büdenbender, J.; Boxhammer, T.; Riebesell, U. Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: Mortality, shell degradation, and shell growth. Biogeosci. Discuss. 2010, 7, 8177-8214
67. Talmage, S.C.; Gobler, C.J. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proc. Natl. Acad. Sci. USA 2010, 107, 17246-17251
68. Comeau, S.; Gorsky, G.; Alliouane, S.; Gattuso, J.-P. Larvae of the pteropod Cavolinia inflexa exposed to aragonite undersaturation are viable but shell-less. Mar. Biol. 2010, 157, 2341-2345
69. Range, P.; Chícharo, M.A.; Ben-Hamadou, R.; Piló, D.; Matias, D.; Joaquim, S.; Oliveira, A.P.; Chícharo, L. Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO2 and reduced pH: Variable responses to ocean acidification at local scales? J. Exp. Mar. Biol. Ecol. 2011, 396, 177-184
70. Gutowska, M.A.; Pörtner, H.O.; Melzner, F. Growth and calcification in the cephalopod Sepia officinalis under elevated seawater pCO2. Mar. Ecol. Prog. Ser. 2008, 373, 303-309
71. Lacoue-Labarthe, T.; Martin, S.; Oberhänsli, F.; Teyssié, J.-L.; Markich, S.; Ross, J.; Bustamante, P. Effects of increased pCO2 and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosciences 2009, 6, 2561-2573
72. Weiss, I.M.; Tuross, N.; Addadi, L.; Weiner, S. Mollusc larval shell formation: Amorphous calcium carbonate is a precursor phase for aragonite. J. Exp. Zool. 2002, 293, 478-491
73. Wilt, F.H. Developmental biology meets materials science: Morphogenesis of biomineralized structures. Dev. Biol. 2005, 280, 15-25
74. Zippay, M.L.; Hofmann, G.E. Effect of pH on gene expression and thermal tolerance of early life history stages of red abalone (Haliotis rufescens). J. Shellfish Res. 2010, 29, 429-439
75. Sunday, J.M.; Crim, R.N.; Harley, C.D.G.; Hart, M.W. Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 2011, 6, doi:10.1371/journal.pone.0022881
76. Orr, J.C.; Caldeira, K.; Fabry, V.; Gattuso, J.P.; Haugan, P.; Lehodey, P.; Pantoja, S.; Pörtner, H.O.; Riebesell, U.; Trull, T.; et al. Research priorities for ocean acidification. In Report from the Second Symposium on the Ocean in a High-CO2 World; SCOR, IOC-UNESCO, IAEA, and IGBP: Monaco, Monaco, 6-9 October 2008
77. Pörtner, H.-O. Ecosystem effects of ocean acidification in times of ocean warming: A physiologist's view. Mar. Ecol. Prog. Ser. 2008, 373, 203-217
78. Doney, S.C.; Fabry, V.J.; Feely, R.A.; Kleypas, J.A. Ocean acidification: The other CO2 problem. Annu. Rev. Mar. Sci. 2009, 1, 169-192
79. O'Donnell, M.J.; Hammond, L.M.; Hofmann, G.E. Predicted impact of ocean acidification on a marine invertebrate: Elevated CO2 alters response to thermal stress in sea urchin larvae. Mar. Biol. 2009, 156, 439-446
80. O'Donnell, M.J.; Todgham, A.E.; Sewell, M.A.; Hammond, L.M.; Ruggiero, K.; Fangue, N.A.; Zippay, M.L.; Hofmann, G.E. Ocean acidification alters skeletogenesis and gene expression in larval sea urchins. Mar. Ecol. Prog. Ser. 2009, 398, 157-171
81. Todgham, A.E.; Hofmann, G.E. Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification. J. Exp. Biol. 2009, 212, 2579-2594
82. Stumpp, M.; Dupont, S.; Thorndyke, M.C.; Melzner, F. CO2 induced seawater acidification impacts sea urchin larval development II: Gene expression patterns in pluteus larvae. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2011, 160, 320-330
83. Stumpp, M.; Wren, J.; Melzner, F.; Thorndyke, M.C.; Dupont, S.T. CO2 induced seawater acidification impacts sea urchin larval development I: Elevated metabolic rates decrease scope for growth and induce developmental delay. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2011, 160, 331-340
84. Deigweiher, K.; Hirse, T.; Bock, C.; Lucassen, M.; Pörtner, H.O. Hypercapnia induced shifts in gill energy budgets of Antarctic notothenioids. J. Comp. Physiol. B 2010, 180, 347-359
85. Melzner, F.; Gutowska, M.A.; Langenbuch, M.; Dupont, S.; Lucassen, M.; Thorndyke, M.C.; Bleich, M.; Pörtner, H.-O. Physiological basis for high CO2 tolerance in marine ectothermic animals: Pre-adaptation through lifestyle and ontogeny? Biogeosciences 2009, 6, 2313-2331
86. Kurihara, H.; Shimode, S.; Shirayama, Y. Effects of raised CO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Mar. Pollut. Bull. 2004, 49, 721-727
87. Kurihara, H.; Matsui, M.; Furukawa, H.; Hayashi, M.; Ishimatsu, A. Long-term effects of predicted future seawater CO2 conditions on the survival and growth of the marine shrimp Palaemon pacificus. J. Exp. Mar. Biol. Ecol. 2008, 367, 41-46
88. Hauton, C.; Tyrrell, T.; Williams, J. The subtle effects of sea water acidification on the amphipod Gammarus locusta. Biogeosci. Discuss. 2009, 6, 919-946
89. Findlay, H.S.; Kendall, M.A.; Spicer, J.I.; Widdicombe, S. Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution. Estuar. Coast. Shelf Sci. 2010, 86, 675-682
90. Findlay, H.S.; Kendall, M.A.; Spicer, J.I.; Widdicombe, S. Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Mar. Biol. 2010, 157, 725-735
91. McDonald, M.R.; McClintock, J.B.; Amsler, C.D.; Rittschof, D.; Angus, R.A.; Orihuela, B.; Lutostanski, K. Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite. Mar. Ecol. Prog. Ser. 2009, 385, 179-187
92. Arnold, K.E.; Findlay, H.S.; Spicer, J.I.; Daniels, C.L.; Boothroyd, D. Effect of CO2-related acidification on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences 2009, 6, 1747-1754
93. Walther, K.; Anger, K.; Pörtner, H.O. Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79°N). Mar. Ecol. Prog. Ser. 2010, 417, 159-170
94. Egilsdottir, H.; Spicer, J.I.; Rundle, S.D. The effect of CO2 acidified sea water and reduced salinity on aspects of the embryonic development of the amphipod Echinogammarus marinus (Leach). Mar. Pollut. Bull. 2009, 58, 1187-1191
95. Mayor, D.J.; Matthews, C.; Cook, K.; Zuur, A.F.; Hay, S. CO2-induced acidification affects hatching success in Calanus finmarchicus. Mar. Ecol. Prog. Ser. 2007, 350, 91-97
96. Findlay, H.S.; Kendall, M.A.; Spicer, J.I.; Widdicombe, S. Future high CO2 in the intertidal may compromise adult barnacle Semibalanus balanoides survival and embryonic development rate. Mar. Ecol. Prog. Ser. 2009, 389, 193-202
97. Walther, K.; Sartoris, F.J.; Pörtner, H.O. Impacts of temperature and acidification on larval calcium incorporation of the spider crab Hyas araneus from different latitudes (54° vs. 79°N). Mar. Biol. 2011, 158, 2043-2053
98. Suwa, R.; Nakamura, M.; Morita, M.; Shimada, K.; Iguchi, A.; Sakai, K.; Suzuki, A. Effects of acidified seawater on early life stages of scleractinian corals (Genus Acropora). Fish. Sci. 2010, 76, 93-99
99. Anlauf, H.; D'Croz, L.; O'Dea, A. 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. 2011, 397, 13-20
100. Albright, R.; Langdon, C. Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides. Glob. Change Biol. 2011, 17, 2478-2487
101. Kikkawa, T.; Ishimatsu, A.; Kita, J. Acute CO2 tolerance during the early developmental stages of four marine teleosts. Environ. Toxicol. 2003, 18, 375-382
102. Munday, P.L.; Crawley, N.E.; Nilsson, G.E. Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Mar. Ecol. Prog. Ser. 2009, 388, 235-242
103. Munday, P.L.; Dixson, D.L.; Donelson, J.M.; Jones, G.P.; Pratchett, M.S.; Devitsina, G.V.; Døving, K.B. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc. Natl. Acad. Sci. USA 2009, 106, 1848-1852
104. Munday, P.L.; Donelson, J.M.; Dixson, D.L.; Endo, G.G.K. Effects of ocean acidification on the early life history of a tropical marine fish. Proc. R. Soc. B 2009, 276, 3275-3283
105. Munday, P.L.; Gagliano, M.; Donelson, J.M.; Dixson, D.L.; Thorrold, S.R. Ocean acidification does not affect the early life history development of a tropical marine fish. Mar. Ecol. Prog. Ser. 2011, 423, 211-221
106. Munday, P.L.; Hernaman, V.; Dixson, D.L.; Thorrold, S.R. Effect of ocean acidification on otolith development in larvae of a tropical marine fish. Biogeosciences 2011, 8, 1631-1641
107. Anger, K. The D0 threshold: A critical point in the larval development of decapod crustaceans. J. Exp. Mar. Biol. Ecol. 1987, 108, 15-30
108. Hart, M.W.; Strathmann, R.R. Mechanisms and rates of suspension feeding. In Ecology of Marine Invertebrate Larvae; McEdward, L., Ed.; CRC Press: Boca Raton, FL, USA, 1995; pp. 193-222
109. Strathmann, M.F. Opisthobranchia. In Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast; Strathmann, M.F., Ed.; University of Washington Press: Seattle, WA, USA, 1987; pp. 268-302
110. Cigliano, M.; Gambi, M.C.; Rodolfo-Metalpa, R.; Patti, F.P.; Hall-Spencer, J.M. Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar. Biol. 2010, 157, 2489-2502
111. Hall-Spencer, J.M.; Rodolfo-Metalpa, R.; Martin, S.; Ransome, E.; Fine, M.; Turner, S.M.; Rowley, S.J.; Tedesco, D.; Buia, M.-C. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 2008, 454, 96-99
112. Fabricius, K.E.; Langdon, C.; Uthicke, S.; Humphrey, C.; Noonan, S.; De'ath, G.; Okazaki, R.; Muehllehner, N.; Glas, M.S.; Lough, J.M. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Change 2011, 1, 165-169
113. Reynaud, S.; Leclercq, N.; Romaine-Lioud, S.; Ferrier-Pagès, C.; Jaubert, J.; Gattuso, J.-P. Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob. Change Biol. 2003, 9, 1660-1668
114. Metzger, R.; Sartoris, F.J.; Langenbuch, M.; Pörtner, H.O. Influence of elevated CO2 concentrations on thermal tolerance of the edible crab Cancer pagurus. J. Therm. Biol. 2007, 32, 144-151
115. Anthony, K.R.N.; Kline, D.I.; Diaz-Pulido, G.; Dove, S.; Hoegh-Guldberg, O. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl. Acad. Sci. USA 2008, 105, 17442-17446
116. Martin, S.; Gattuso, J.-P. Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob. Change Biol. 2009, 15, 2089-2100
117. Bibby, R.; Widdicombe, S.; Parry, H.; Spicer, J.; Pipe, R. Effects of ocean acidification on the immune response of the blue mussel Mytilus edulis. Aquat. Biol. 2008, 2, 67-74
118. Connell, J.H. Some mechanisms producing structure in natural communities: A model and evidence from field experiments. In Ecology and Evolution of Communities; Cody, M., Diamond, J., Eds.; Harvard University Press: Cambridge, MA, USA, 1975; pp. 460-490
119. Underwood, A.J. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance; Cambridge University Press: Cambridge, UK, 1997; p. 504
120. Byrne, M.; Ho, M.; Wong, E.; Soars, N.A.; Selvakumaraswamy, P.; Shepard Brennand, H.; Dworjanyn, S.A.; Davis, A.R. Unshelled abalone and corrupted urchins: Development of marine calcifiers in a changing ocean. Proc. R. Soc. B 2011, 278, 2376-2383
121. Martin, S.; Richier, S.; Pedrotti, M.-L.; Dupont, S.; Castejon, C.; Gerakis, Y.; Kerros, M.-E.; Oberhänsli, F.; Teyssié, J.-L.; Jeffree, R.; et al. Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J. Exp. Biol. 2011, 214, 1357-1368
122. Yu, P.C.; Matson, P.G.; Martz, T.R.; Hofmann, G.E. The ocean acidification seascape and its relationship to the performance of calcifying marine invertebrates: Laboratory experiments on the development of urchin larvae framed by environmentally-relevant pCO2/pH. J. Exp. Mar. Biol. Ecol. 2011, 400, 288-295
123. Crim, R.N.; Sunday, J.M.; Harley, C.D.G. Elevated seawater CO2 concentrations impair larval development and reduce larval survival in endangered northern abalone (Haliotis kamtschatkana). J. Exp. Mar. Biol. Ecol. 2011, 400, 272-277
124. Miller, A.W.; Reynolds, A.C.; Sobrino, C.; Riedel, G.F. Shellfish face uncertain future in high CO2 world: Influence of acidification on oyster larvae calcification and growth in estuaries. PLoS One 2009, 4, doi:10.1371/journal.pone.0005661
125. Jokiel, P.L.; Rodgers, K.S.; Kuffner, I.B.; Andersson, A.J.; Cox, E.F.; Mackenzie, F.T. Ocean acidification and calcifying reef organisms: A mesocosm investigation. Coral Reefs 2008, 27, 473-483
126. Morita, M.; Suwa, R.; Iguchi, A.; Nakamura, M.; Shimada, K.; Sakai, K.; Suzuki, A. Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 2010, 18, 103-107
127. Holcomb, M.; McCorkle, D.C.; Cohen, A.L. Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). 2010, 386, 27-33
128. Krief, S.; Hendy, E.J.; Fine, M.; Yam, R.; Meibom, A.; Foster, G.L.; Shemesh, A. Physiological and isotopic responses of scleractinian corals to ocean acidification. 2010, 74, 4988-5001
129. Rodolfo-Metalpa, R.; Martin, S.; Ferrier-Pagès, C.; Gattuso, J.P. Response of the temperate coral Cladocora caespitosa to mid-and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences 2010, 7, 289-300