Elevations in atmospheric carbon dioxide (CO 2) are anticipated to acidify oceans because of fundamental changes in ocean chemistry created by CO 2 absorption from the atmosphere. Over the next century, these elevated concentrations of atmospheric CO 2 are expected to result in a reduction of the surface ocean waters from 8.1 to 7.7 units as well as a reduction in carbonate ion (CO 3 2？) concentration. The potential impact that this change in ocean chemistry will have on marine and estuarine organisms and ecosystems is a growing concern for scientists worldwide. While species-specific responses to ocean acidification are widespread across a number of marine taxa, molluscs are one animal phylum with many species which are particularly vulnerable across a number of life-history stages. Molluscs make up the second largest animal phylum on earth with 30,000 species and are a major producer of CaCO 3. Molluscs also provide essential ecosystem services including habitat structure and food for benthic organisms ( i.e., mussel and oyster beds), purification of water through filtration and are economically valuable. Even sub lethal impacts on molluscs due to climate changed oceans will have serious consequences for global protein sources and marine ecosystems.
References
[1]
Climate Change 2001: 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.G., Noguer, M., van der Linden, P.J., Dai, X., Maskell, K., Johnson, C.A., Eds.; Cambridge University Press: Cambridge, UK, 2001; Volume 881.
[2]
Solomon, S. Climate Change 2007: The Physical Science Basis: Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge, UK, 2007.
[3]
Doney, S.C.; Fabry, V.J.; Feely, R.A.; Kleypas, J.A. Ocean acidification: The other CO2 problem. Mar. Sci. 2009, 1, 169–192.
[4]
Raven, J.; Caldeira, K.; Elderfield, H.; Hoegh-Guldberg, O.; Liss, P.; Riebesell, U.; Shepherd, J.; Turley, C.; Watson, A. Ocean Acidification due to Increasing Atmospheric Carbon Dioxide; The Royal Society: London, UK, 2005.
[5]
Orr, J.C.; Fabry, V.J.; Aumont, O.; Bopp, L.; Doney, S.C.; Feely, R.A.; Gnanadesikan, A.; Gruber, N.; Ishida, A.; Joos, F. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 2005, 437, 681–686, doi:10.1038/nature04095.
[6]
Feely, R.A.; Sabine, C.L.; Lee, K.; Berelson, W.; Kleypas, J.; Fabry, V.J.; Millero, F.J. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 2004, 305, 362–366, doi:10.1126/science.1097329.
[7]
Cooley, S.R.; Doney, S.C. Anticipating ocean acidification’s economic consequences for commercial fisheries. Environ. Res. Lett. 2009, 4, 024007, doi:10.1088/1748-9326/4/2/024007.
[8]
Guinotte, J.M.; Fabry, V.J. Ocean acidification and its potential effects on marine ecosystems. Ann. N. Y. Acad. Sci. 2008, 1134, 320–342, doi:10.1196/annals.1439.013.
[9]
Hendriks, I.; Duarte, C.; Alvarez, M. Vulnerability of marine biodiversity to ocean acidification: A meta-analysis. Estuar. Coast. Shelf Sci. 2010, 86, 157–164, doi:10.1016/j.ecss.2009.11.022.
[10]
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, doi:10.1016/j.ecss.2010.06.013.
[11]
Duarte, C.A.; Giarratano, E.; Amin, O.A.; Comoglio, L.I. Heavy metal concentrations and biomarkers of oxidative stress in native mussels (Mytilus edulis chilensis) from Beagle Channel coast (Tierra del Fuego, Argentina). Mar. Pollut. Bull. 2011, 62, 1895–1904, doi:10.1016/j.marpolbul.2011.05.031.
[12]
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. Roy. Soc. B 2011, 278, 2376–2383, doi:10.1098/rspb.2010.2404.
[13]
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, doi:10.1111/j.1461-0248.2010.01518.x.
[14]
Ross, P.M.; Parker, L.; O’Connor, W.A.; Bailey, E.A. The impact of ocean acidification on reproduction, early development and settlement of marine organisms. Water 2011, 3, 1005–1030, doi:10.3390/w3041005.
[15]
Gutiérrez, J.L.; Jones, C.G.; Strayer, D.L.; Iribarne, O.O. Mollusks as ecosystem engineers: The role of shell production in aquatic habitats. Oikos 2003, 101, 79–90, doi:10.1034/j.1600-0706.2003.12322.x.
[16]
Norling, P.; Kautsky, N. Patches of the mussel Mytilus sp. Are islands of high biodiversity in subtidal sediment habitats in the Baltic Sea. Aquat. Biol. 2008, 4, 75–87.
[17]
Buschbaum, C.; Dittmann, S.; Hong, J.S.; Hwang, I.S.; Strasser, M.; Thiel, M.; Valdivia, N.; Yoon, S.P.; Reise, K. Mytilid mussels: Global habitat engineers in coastal sediments. Helgol. Mar. Res. 2009, 63, 47–58, doi:10.1007/s10152-008-0139-2.
[18]
Comeau, S.; Jeffree, R.; Teyssié, J.L.; Gattuso, J.P. Response of the arctic pteropod Limacina helicina to projected future environmental conditions. PLoS One 2010, 5, e11362.
[19]
Gosling, E. Bivalve Molluscs; Blackwell Publishing: Oxford, UK, 2003.
[20]
Cooley, S.R.; Lucey, N.; Kite‐Powell, H.; Doney, S.C. Nutrition and income from molluscs today imply vulnerability to ocean acidification tomorrow. Fish Fish. 2012, 13, 182–215, doi:10.1111/j.1467-2979.2011.00424.x.
[21]
Doney, S.C.; Ruckelshaus, M.; Duffy, J.E.; Barry, J.P.; Chan, F.; English, C.A.; Galindo, H.M.; Grebmeier, J.M.; Hollowed, A.B.; Knowlton, N. Climate change impacts on marine ecosystems. Mar. Sci. 2012, 4, 11–37.
[22]
Narita, D.; Rehdanz, K.; Tol, R.S.J. Economic costs of ocean acidification: A look into the impacts on global shellfish production. Clim. Change 2012, 113, 1049–1065, doi:10.1007/s10584-011-0383-3.
[23]
Fisheries Aquaculture Department. The State of World Fisheries and Aquaculture 2008; Food and Agriculture Organization of the United Nations: Rome, Italy, 2010.
[24]
Smith, M.D.; Roheim, C.A.; Crowder, L.B.; Halpern, B.S.; Turnipseed, M.; Anderson, J.L.; Asche, F.; Bourillón, L.; Guttormsen, A.G.; Khan, A. Sustainability and global seafood. Science 2010, 327, 784–786, doi:10.1126/science.1185345.
[25]
Swartz, W.; Rashid Sumaila, U.; Watson, R.; Pauly, D. Sourcing seafood for the three major markets: The EU, Japan and the USA. Mar. Policy 2010, 34, 1366–1373, doi:10.1016/j.marpol.2010.06.011.
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, doi:10.1016/j.jembe.2011.02.002.
[28]
Hankewich, S.; Lessard, J. Resurvey of Northern Abalone, Haliotis Kamtschatkana, Populations along the Central Coast of British Columbia, May 2006; Fisheries and Oceans Canada: Nanaimo, Canada, 2008.
[29]
Feely, R.A.; Alin, S.R.; Newton, J.; Sabine, C.L.; Warner, M.; Devol, A.; Krembs, C.; Maloy, C. The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar. Coast. Shelf Sci. 2010, 88, 442–449, doi:10.1016/j.ecss.2010.05.004.
[30]
Waldbusser, G.G.; Voigt, E.P.; Bergschneider, H.; Green, M.A.; Newell, R.I.E. Biocalcification in the Eastern oyster (Crassostrea virginica) in relation to long-term trends in Chesapeake Bay pH. Estuar. Coasts 2011, 34, 221–231, doi:10.1007/s12237-010-9307-0.
[31]
Feely, R.A.; Sabine, C.L.; Hernandez-Ayon, J.M.; Ianson, D.; Hales, B. Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 2008, 320, 1490–1492, doi:10.1126/science.1155676.
[32]
Jackson, A.; Chapman, M.; Underwood, A. Ecological interactions in the provision of habitat by urban development: Whelks and engineering by oysters on artificial seawalls. Austral Ecol. 2008, 33, 307–316, doi:10.1111/j.1442-9993.2007.01818.x.
[33]
Thorson, G. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev. 1950, 25, 1–45, doi:10.1111/j.1469-185X.1950.tb00585.x.
Kurihara, H.; Asai, T.; Kato, S.; Ishimatsu, A. Effects of elevated pCO2 on early development in the mussel Mytilus galloprovincialis. Aquat. Biol. 2009, 4, 225–233, doi:10.3354/ab00109.
[36]
Kurihara, H. Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar. Eco. Prog. Ser. 2008, 373, 275–284, doi:10.3354/meps07802.
[37]
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, doi:10.1111/j.1365-2486.2009.01895.x.
ESF. European Food Systems in a Changing World. Report of a ESF/cost Forward Look; European Science Foundation: Strasbourg, France, 2009.
[40]
Beniash, E.; Ivanina, A.; Lieb, N.S.; Kurochkin, I.; Sokolova, I.M. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Mar. Ecol. Prog. Ser. 2010, 419, 95–108, doi:10.3354/meps08841.
[41]
Fabry, V.J.; Seibel, B.A.; Feely, R.A.; Orr, J.C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 2008, 65, 414–432, doi:10.1093/icesjms/fsn048.
[42]
Wicks, L.C.; Roberts, M. Benthic invertebrates in a high-CO2 world. Oceanog. Mar. Biol. Ann. Rev. 2012, 50, 127–188.
[43]
Michaelidis, B.; Ouzounis, C.; Paleras, A.; P？rtner, H.O. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar. Ecol. Prog. Ser. 2005, 293, 109–118, doi:10.3354/meps293109.
[44]
Shirayama, Y.; Thornton, H. Effect of increased atmospheric CO2 on shallow water marine benthos. J. Geophys. Res. 2005, 110, C09S08, doi:10.1029/2004JC002618.
[45]
Gazeau, F.; Quiblier, C.; Jansen, J.M.; Gattuso, J.P.; Middelburg, J.J.; Heip, C.H.R. Impact of elevated CO2 on shellfish calcification. Geophys. Res. Lett. 2007, 34, doi:10.1029/2006GL028554.
Lischka, S.; Buedenbender, 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. Biogeosciences 2010, 7, 8177–8214, doi:10.5194/bgd-7-8177-2010.
[50]
Nienhuis, S.; Palmer, A.R.; Harley, C.D.G. Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail. Proc. Roy. Soc. B 2010, 277, 2553–2558, doi:10.1098/rspb.2010.0206.
[51]
Thomsen, J.; Melzner, F. Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Mar. Biol. 2010, 157, 2667–2676, doi:10.1007/s00227-010-1527-0.
[52]
Welladsen, H.M.; Southgate, P.C.; Heimann, K. The effects of exposure to near-future levels of ocean acidification on shell characteristics of Pinctada fucata (Bivalvia: Pteriidae). Molluscan Res. 2010, 30, 125–130.
[53]
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, doi:10.1007/s00227-010-1592-4.
[54]
McClintock, J.B.; Angus, R.A.; Mcdonald, M.R.; Amsler, C.D.; Catledge, S.A.; Vohra, Y.K. Rapid dissolution of shells of weakly calcified antarctic benthic macroorganisms indicates high vulnerability to ocean acidification. Antarct. Sci. 2009, 21, 449–456, doi:10.1017/S0954102009990198.
[55]
Bamber, R. The effects of acidic seawater on three species of lamellibranch mollusc. J. Exp. Mar. Biol. Ecol. 1990, 143, 181–191, doi:10.1016/0022-0981(90)90069-O.
[56]
Bednar？ek, N.; Tarling, G.A.; Bakker, D.C.E.; Fielding, S.; Cohen, A.; Kuzirian, A.; McCorkle, D.; Lézé, B.; Montagna, R. Description and quantification of pteropod shell dissolution: A sensitive bioindicator of ocean acidification. Glob. Change Biol. 2012, 18, 2378–2388, doi:10.1111/j.1365-2486.2012.02668.x.
[57]
Manno, C.; Morata, N.; Primicerio, R. Limacina retroversa response to combined effects of ocean acidification and sea water freshening. Estuar. Coast. Shelf Sci. 2012, 113, 163–171, doi:10.1016/j.ecss.2012.07.019.
[58]
Bibby, R.; Cleall-Harding, P.; Rundle, S.; Widdicombe, S.; Spicer, J. Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biol. Lett. 2007, 3, 699–701, doi:10.1098/rsbl.2007.0457.
[59]
Hüning, A.K.; Melzner, F.; Thomsen, J.; Gutowska, M.A.; Kr？mer, L.; Frickenhaus, S.; Rosenstiel, P.; P？rtner, H.O.; Philipp, E.E.R.; Lucassen, M. Impacts of seawater acidification on mantle gene expression patterns of the Baltic Sea blue mussel: Implications for shell formation and energy metabolism. Mar. Biol. 2012, doi:10.1007/s00227-012-1930-9.
[60]
Berge, J.A.; Bjerkeng, B.; Pettersen, O.; Schaanning, M.T.; ？xnevad, S. Effects of increased sea water concentrations of CO2 on growth of the bivalve Mytilus edulis L. Chemosphere 2006, 62, 681–687, doi:10.1016/j.chemosphere.2005.04.111.
[61]
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, doi:10.3354/meps08809.
[62]
Waldbusser, G.G.; Steenson, R.A.; Green, M.A. Oyster shell dissolution rates in estuarine waters: Effects of pH and shell legacy. J. Shellfish Res. 2011, 30, 659–669, doi:10.2983/035.030.0308.
[63]
Range, P.; Piló, D.; Ben-Hamadou, R.; Chícharo, M.A.; Matias, D.; Joaquim, S.; Oliveira, A.P.; Chícharo, L. Seawater acidification by CO2 in a coastal lagoon environment: Effects on life history traits of juvenile mussels Mytilus galloprovincialis. J. Exp. Mar. Biol. Ecol. 2012, 424–425, 89–98.
[64]
Melatunan, S.; Calosi, P.; Rundle, S.D.; Widdicombe, S.; Moody, A.J. Effects of ocean acidification and elevated temperature on shell plasticity and its energetic basis in an intertidal gastropod. MEPS 2013, 472, 155–168, doi:10.3354/meps10046.
[65]
Thomsen, J.; Casties, I.; Pansch, C.; K？rtzinger, A.; Melzner, F. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: Laboratory and field experiments. Glob. Change Biol. 2013, doi:10.1111/gcb.12109.
[66]
Tomanek, L.; Zuzow, M.J.; Ivanina, A.V.; Beniash, E.; Sokolova, I.M. Proteomic response to elevated PCO2 level in eastern oysters, Crassostrea virginica: Evidence for oxidative stress. J. Exp. Biol. 2011, 214, 1836–1844, doi:10.1242/jeb.055475.
[67]
Gutowska, M.A.; P？rtner, H.O.; Melzner, F. Growth and calcification in the cephalopod Sepia officinalis under elevated seawater pCO2. Mar. Ecol. Prog. Ser. 2008, 373, 303–309, doi:10.3354/meps07782.
[68]
Gutowska, M.A.; Melzner, F.; P？rtner, H.O.; Meier, S. Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis. Mar. Biol. 2010, 157, 1653–1663, doi:10.1007/s00227-010-1438-0.
[69]
Ries, J.B. A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim. Cosmochim. Acta 2011, 75, 4053–4064, doi:10.1016/j.gca.2011.04.025.
[70]
Morse, J.W.; Andersson, A.J.; Mackenzie, F.T. Initial responses of carbonate-rich shelf sediments to rising atmospheric pCO2 and “ocean acidification”: Role of high Mg-Calcites. Geochim. Cosmochim. Acta 2006, 70, 5814–5830, doi:10.1016/j.gca.2006.08.017.
[71]
Gutowska, M.A.; Melzner, F.; Langenbuch, M.; Bock, C.; Claireaux, G.; P？rtner, H.O. Acid-base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. J. Comp. Physiol. B 2010, 180, 323–335, doi:10.1007/s00360-009-0412-y.
[72]
Range, P.; Chícharo, M.; Ben-Hamadou, R.; Piló, D.; Matias, D.; Joaquim, S.; Oliveira, A.; 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, doi:10.1016/j.jembe.2010.10.020.
[73]
Ries, J.B. Skeletal mineralogy in a high CO2 world. J. Exp. Mar. Biol. Ecol. 2011, 403, 54–64, doi:10.1016/j.jembe.2011.04.006.
[74]
P？rtner, H.O.; Langenbuch, M.; Reipschl？ger, A. Biological impact of elevated ocean CO2 concentrations: Lessons from animal physiology and earth history. J. Oceanogr. 2004, 60, 705–718, doi:10.1007/s10872-004-5763-0.
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, doi:10.3354/ab00009.
[77]
Havenhand, J.; 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, doi:10.5194/bg-6-3009-2009.
[78]
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, doi:10.1007/s00227-010-1508-3.
[79]
Thomsen, J.; Gutowska, M.; Saph？rster, J.; Heinemann, A.; Trübenbach, K.; Fietzke, J.; Hiebenthal, C.; Eisenhauer, A.; K？rtzinger, A.; Wahl, M. Calcifying invertebrates succeed in a naturally CO2 enriched coastal habitat but are threatened by high levels of future acidification. Biogeosciences 2010, 7, 5119–5156, doi:10.5194/bgd-7-5119-2010.
[80]
Przeslawski, R. A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses. Molluscan Res. 2004, 24, 43–63, doi:10.1071/MR04001.
[81]
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. Roy. Soc. B 2009, 276, 1883–1888, doi:10.1098/rspb.2008.1935.
[82]
Gosselin, L.A.; Qian, P.Y. Juvenile mortality in benthic marine invertebrates. Mar. Ecol. Prog. Ser. 1997, 146, 265–282, doi:10.3354/meps146265.
[83]
Melzner, F.; Gutowska, M.; Langenbuch, M.; Dupont, S.; Lucassen, M.; Thorndyke, M.C.; Bleich, M.; P？rtner, H.O. Physiological basis for high CO2 tolerance in marine ectothermic animals: Pre-adaptation through lifestyle and ontogeny? Biogeosciences 2009, 6, 2313–2331.
[84]
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, doi:10.1002/jez.90004.
[85]
Dupont, S.; Thorndyke, M. Impact of CO2-driven ocean acidification on invertebrates early life-history—What we know, what we need to know and what we can do. Biogeosciences 2009, 6, 3109–3131.
[86]
Gibson, R.; Atkinson, R.; Gordon, J.; Smith, I.; Hughes, D. 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. 2011, 49, 1–42.
[87]
Calabrese, A.; Davis, H.C. The pH tolerance of embryos and larvae of Mercenaria mercenaria and Crassostrea virginica. Biol. Bull. 1966, 131, 427–436, doi:10.2307/1539982.
[88]
Desrosiers, R.R.; Desilets, J.; Dube, F. Early developmental events following fertilization in the giant scallop Placopecten magellanicus. Can. J. Fish. Aquat. Sci. 1996, 53, 1382–1392, doi:10.1139/f96-071.
[89]
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, doi:10.1006/eesa.1996.1514.
[90]
Pagano, G.; Cipollaro, M.; Corsale, G.; Esposito, A.; Ragucci, E.; Giordano, G.G. pH-induced changes in mitotic and developmental patterns in sea urchin embryogenesis. I. Exposure of embryos. Teratog. Carcinog. Mutagen. 1985, 5, 101–112, doi:10.1002/tcm.1770050204.
[91]
Pagano, G.; Cipollaro, M.; Corsale, G.; Esposito, A.; Ragucci, E.; Giordano, G.G. pH-induced changes in mitotic and developmental patterns in sea urchin embryogenesis. II. Exposure of sperm. Teratog. Carcinog. Mutagen. 1985, 5, 113–121, doi:10.1002/tcm.1770050205.
[92]
Cipollaro, M.; Corsale, G.; Esposito, A.; Ragucci, E.; Staiano, N.; Giordano, G.G.; Pagano, G. Sublethal pH decrease may cause genetic damage to eukaryotic cell: A study on sea urchins and Salmonella typhimurium. Teratog. Carcinog. Mutagen. 1986, 6, 275–287, doi:10.1002/tcm.1770060404.
Bechmann, R.K.; Taban, I.C.; Westerlund, S.; Godal, B.F.; Arnberg, M.; Vingen, S.; Ingvarsdottir, A.; Baussant, T. Effects of ocean acidification on early life stages of shrimp (Pandalus borealis) and mussel (Mytilus edulis). J. Toxicol. Environ. Health A 2011, 74, 424–438, doi:10.1080/15287394.2011.550460.
[95]
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, doi:10.1007/s00227-010-1474-9.
[96]
Van Colen, C.; Debusschere, E.; Braeckman, U.; van Gansbeke, D.; Vincx, M. The early life history of the clam Macoma balthica in a high CO2 world. PLoS One 2012, 7, doi:10.1371/journal.pone.0044655.
[97]
Kimura, R.Y.O.; Takami, H.; Ono, T.; Onitsuka, T.; Nojiri, Y. Effects of elevated pCO2 on the early development of the commercially important gastropod, Ezo abalone Haliotis discus hannai. Fish Oceanogr. 2011, 20, 357–366, doi:10.1111/j.1365-2419.2011.00589.x.
[98]
Byrne, M. Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar. Environ. Res. 2012, 76, 3–15, doi:10.1016/j.marenvres.2011.10.004.
[99]
Reuter, K.I.M.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. Glob. Change Biol. 2010, 17, 163–171.
[100]
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, e5661, doi:10.1371/journal.pone.0005661.
[101]
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.
[102]
Gazeau, F.; Gattuso, J.; Dawber, C.; Pronker, A.; Peene, F.; Peene, J.; Heip, C.; Middelburg, J. Effect of ocean acidification on the early life stages of the blue mussel Mytilus edulis. Biogeosciences 2010, 7, 2051–2060.
[103]
Talmage, S.C.; Gobler, C.J. The effects of elevated carbon dioxide concentrations on the metamorphosis, size, and survival of larval hard clams (Mercenaria mercenaria), bay scallops (Argopecten irradians), and eastern oysters (Crassostrea virginica). Limnol. Oceanog. 2009, 54, 2072–2080.
[104]
Talmage, S.C.; Gobler, C.J. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfis. Proc. Natl. Acad. Sci. USA 2010, 107, 17246–17251.
[105]
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.
[106]
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.
[107]
Gaylord, B.; Hill, T.M.; Sanford, E.; Lenz, E.A.; Jacobs, L.A.; Sato, K.N.; Russell, A.D.; Hettinger, A. Functional impacts of ocean acidification in an ecologically critical foundation species. J. Exp. Biol. 2011, 214, 2586–2594.
[108]
Talmage, S.C.; Gobler, C.J. 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 2011, 6, e26941.
[109]
Talmage, S.C.; Gobler, C.J. Effects of CO2 and the harmful alga Aureococcus anophagefferens on growth and survival of oyster and scallop larvae. Mar. Ecol. Prog. Ser. 2012, 464, 121–147.
[110]
Thiyagarajan, V.; Ko, G.W.K. Larval growth response of the Portuguese oyster (Crassostrea angulata) to multiple climate change stressors. Aquaculture 2012, 370–371, 90–95.
[111]
Timmins-Schiffman, E.; O’Donnell, M.J.; Friedman, C.S.; Roberts, S.B. Elevated pCO2 causes developmental delay in early larval Pacific oysters, Crassostrea gigas. Mar. Biol. 2012, doi:10.1007/s00227-012-2055-x.
[112]
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.
[113]
López, I.R.; Kalman, J.; Vale, C.; Blasco, J. Influence of sediment acidification on the bioaccumulation of metals in Ruditapes philippinarum. Environ. Sci. Pollut. R. 2010, 17, 1519–1528.
[114]
Riba, I.; García-Luque, E.; Kalman, J.; Blasco, J.; Vale, C. Effects of Sediment Acidification on the Bioaccumulation of Zn in R. Philippinarum. In Oceans and the Atmospheric Carbon Content; Duarte, P., Santana-Casiano, J.M., Eds.; Springer: Berlin, Germany, 2010; pp. 115–132.
[115]
Lacoue-Labarthe, T.; Martin, S.; Oberh？nsli, F.; Teyssié, J.L.; Markich, S.; Jeffree, R.; 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.
[116]
Gazeau, F.; Gattuso, J.P.; Greaves, M.; Elderfield, H.; Peene, J.; Heip, C.H.R.; Middelburg, J.J. Effect of carbonate chemistry alteration on the early embryonic development of the Pacific oyster (Crassostrea gigas). PLoS One 2011, 6, e23010.
[117]
Goldberg, J.I.; Doran, S.A; Shartau, R.B.; Pon, J.R.; Ali, D.W.; Tam, R; Kuang, S. Integratingbiology of an embryonic respiratory behaviour in pond snails: The embryo stir-bar hypothesis. J. Exp. Biol. 2008, 211, 1729–1736.
[118]
Diefenbach, T.J.; Koehncke, N.K.; Goldberg, J.I. Characterization and development of rotational behavior in Helisoma embryos: Role of endogenous serotonin. J. Neurobiol. 1991, 22, 922–934.
[119]
Waller, T.R. Functional Morphology and Development of Veliger Larvae of the European Oyster, Ostrea Edulis Linne; Smithsonian Institution Press: Washington, DC, USA, 1981; pp. 1–70.
[120]
Hayakaze, E.; Tanabe, K. Early larval shell development in mytilid bivalve Mytilus galloprovincialis. Venus Jpn. J. Malacol. 1999, 58, 119–127.
[121]
O’Donnell, M.J.; Hammond, L.T.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.
[122]
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.
[123]
Zippay, M.K.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.
[124]
Dineshram, R.; Wong, K.K.W.; Xiao, S.; Yu, Z.; Qian, P.Y.; Thiyagarajan, V. Analysis of Pacific oyster larval proteome and its response to high-CO2. Mar. Pollut. Bull. 2012, 64, 2160–2167.
[125]
Rodriguez, S.R.; Ojeda, F.P.; Inestrosa, N.C. Settlement of benthic marine invertebrates. Mar. Ecol. Prog. Ser. 1993, 97, 193–207.
[126]
Cigliano, M.; Gambi, M.; Rodolfo-Metalpa, R.; Patti, F.; Hall-Spencer, J. Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar. Biol. 2010, 157, 2489–2502.
[127]
Byrne, M.; Selvakumaraswamy, P.; Ho, M.; Woolsey, E.; Nguyen, H. Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep Sea Res. Part II 2011, 58, 712–719.
Howarth, R.; Chan, F.; Conley, D.J.; Garnier, J.; Doney, S.C.; Marino, R.; Billen, G. Coupled biogeochemical cycles: Eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front. Ecol. Environ. 2011, 9, 18–26.
[130]
Reynaud, S.; Leclercq, N.; Romaine‐Lioud, S.; Ferrier‐Pagés, 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.
[131]
Metzger, R.; Sartoris, F.J.; Langenbuch, M.; P？rtner, H.O. Influence of elevated CO2 concentrations on thermal tolerance of the edible crab Cancer pagurus. J. Therm. Biol. 2007, 32, 144–151.
[132]
Anthony, K.; Kline, D.; 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.
[133]
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.
[134]
Martin, S.; Gattuso, J.P. Response of mediterranean coralline algae to ocean acidification and elevated temperature. Glob. Change Biol. 2009, 15, 2089–2100.
[135]
Matozzo, V.; Chinellato, A.; Munari, M.; Finos, L.; Bressan, M.; Marin, M.G. First evidence of immunomodulation in bivalves under seawater acidification and increased temperature. PLoS One 2012, 7, e33820.
[136]
Rosa, R.; Seibel, B.A. Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proc. Natl. Acad. Sci. USA 2008, 105, 20776–20780.
[137]
Lannig, G.; Eilers, S.; P？rtner, H.O.; Sokolova, I.M.; Bock, C. Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas—Changes in metabolic pathways and thermal response. Mar. Drugs 2010, 8, 2318–2339.
[138]
Hale, R.; Calosi, P.; McNeill, L.; Mieszkowska, N.; Widdicombe, S. Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 2011, 120, 661–674.
[139]
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.
[140]
Dickinson, G.H.; Ivanina, A.V.; Matoo, O.B.; P？rtner, H.O.; Lannig, G.; Bock, C.; Beniash, E.; Sokolova, I.M. Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. J. Exp. Biol. 2012, 215, 29–43.
[141]
P？rtner, H.O. Oxygen-and capacity-limitation of thermal tolerance: A matrix for integrating climate-related stressor effects in marine ecosystems. J. Exp. Biol. 2010, 213, 881–893.
[142]
Przeslawski, R.; Davis, A.; Benkendorff, K. Synergistic effects associated with climate change and the development of rocky shore molluscs. Glob. Change Biol. 2005, 11, 515–522.
[143]
McLusky, D.S.; Bryant, V.; Campbell, R. The effects of temperature and salinity on the toxicity of heavy metals to marine and estuarine invertebrates. Oceanogr. Mar. Biol. Ann. Rev. 1986, 24, 481–520.
[144]
Bibby, R.; Widdicombe, S.; Parry, H.; Spicer, J.; Pipe, R. Effect of ocean acidification on the immune response of the blue mussel, Mytilus edulis. Aquat. Biol. 2008, 2, 67–74.
[145]
Beesley, A.; Lowe, D.; Pascoe, C.; Widdicombe, S. Effects of CO2-induced seawater acidification on the health of Mytilus edulis. Clim. Res. 2008, 37, 215–225.
[146]
Davis, H.C. Survival and growth of clam and oyster larvae at different salinities. Biol. Bull. 1958, 114, 296–307.
[147]
Podolsky, R.D.; Moran, A.L. Integrating function across marine life cycles. ICB 2006, 46, 577–586.
[148]
Allen, R.M.; Buckley, Y.M.; Marshall, D.J. Offspring size plasticity in response to intraspecific competition: An adaptive maternal effect across life-history stages. Am. Nat. 2008, 171, 225–237.
[149]
Moran, A.L.; McAlister, J.S. Egg size as a life history character of marine invertebrates: Is it all it's cracked up to be? Biol. Bull. 2009, 216, 226–242.
[150]
Dupont, S.; Dorey, N.; Stumpp, M.; Melzner, F.; Thorndyke, M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 2012, doi:10.1007/s00227-012-1921-x.
[151]
Reipschl？ger, A.; P？rtner, H. Metabolic depression during environmental stress: The role of extracellular versus intracellular pH in Sipunculus nudus. J. Exp. Biol. 1996, 199, 1801–1807.
[152]
Cummings, V.; Hewitt, J.; van Rooyen, A.; Currie, K.; Beard, S.; Thrush, S.; Norkko, J.; Barr, N.; Heath, P.; Halliday, N.J. Ocean acidification at high latitudes: Potential effects on functioning of the antarctic bivalve Laternula elliptica. PLoS One 2011, 6, e16069, doi:10.1371/journal.pone.0016069.
[153]
Green, M.A.; Waldbusser, G.G.; Reilly, S.L.; Emerson, K. Death by dissolution: Sediment saturation state as a mortality factor for juvenile bivalves. Limnol. Oceanogr. 2009, 54, 1037–1047, doi:10.4319/lo.2009.54.4.1037.
[154]
Seibel, B.A.; Walsh, P.J. Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J. Exp. Biol. 2003, 206, 641–650, doi:10.1242/jeb.00141.
[155]
Marchant, H.K.; Calosi, P.; Spicer, J.I. Short-term exposure to hypercapnia does not compromise feeding, acid-base balance or respiration of Patella vulgata but surprisingly is accompanied by radula damage. J. Mar. Biol. Assoc. UK 2010, 90, 1379–1384, doi:10.1017/S0025315410000457.
[156]
P？rtner, H.O. Ecosystem effects of ocean acidification in times of ocean warming: A physiologist’s view. Mar. Ecol. Prog. Ser. 2008, 373, 203–217, doi:10.3354/meps07768.
[157]
Fernández-Reiriz, J.; Range, P.; álvarez-Salgado, X.A.; Labarta, U. Physiological energetics of juvenile clams (Ruditapes decussatus) in a high CO2 coastal ocean. Mar. Ecol. Prog. Ser. 2011, 433, 97–105.
[158]
Liu, W.; He, M. Effects of ocean acidification on the metabolic rates of three species of bivalve from southern coast of China. Chin. J. Oceanol. Limn. 2012, 30, 206–211, doi:10.1007/s00343-012-1067-1.
[159]
Fernández-Reiriz, M.J.; Range, P.; Alvarez-Salgado, X.A.; Espinosa, J.; Labarta, U. Tolerance of juvenile Mytilus galloprovincialis to experimental seawater acidification. Mar. Ecol. Prog. Ser. 2012, 454, 65–74, doi:10.3354/meps09660.
[160]
Navarro, J.M.; Torres, R.; Acu？a, K.; Duarte, C.; Manriquez, P.H.; Lardies, M.; Lagos, N.A.; Vargas, C.; Aguilera, V. Impact of medium-term exposure to elevated pCO2 levels on the physiological energetics of the mussel Mytilus chilensis. Chemosphere 2013, doi:10.1016/j.chemosphere.2012.09.063.
[161]
Hammer, K.M.; Kristiansen, E.; Zachariassen, K.E. Physiological effects of hypercapnia in the deep-sea bivalve Acesta excavata (Fabricius, 1779) (Bivalvia; Limidae). Mar. Environ. Res. 2011, 72, 135–142, doi:10.1016/j.marenvres.2011.07.002.
[162]
Melatunan, S.; Calosi, P.; Rundle, S.D.; Moody, A.J.; Widdicombe, S. Exposure to elevated temperature and PCO2 reduces respiration rate and energy status in the periwinkle Littorina littorea. Physiol. Biochem. Zool. 2011, 84, 583–594, doi:10.1086/662680.
[163]
Sokolova, I.; P？rtner, H. Temperature effects on key metabolic enzymes in Littorina saxatilis and L. obtusata from different latitudes and shore levels. Mar. Biol. 2001, 139, 113–126, doi:10.1007/s002270100557.
[164]
Lindinger, M.; Lauren, D.; McDonald, D. Acid-base balance in the sea mussel, Mytilus edulis. III: Effects of environmental hypercapnia on intra-and extracellular acid-base balance. Mar. Biol. Lett. 1984, 5, 371–381.
[165]
Schalkhausser, B.; Bock, C.; Stemmer, K.; Brey, T.; P？rtner, H.-O.; Lannig, G. Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway. Mar. Biol. 2012, doi:10.1007/s00227-012-2057-8.
[166]
Melzner, F.; Stange, P.; Trübenbach, K.; Thomsen, J.; Casties, I.; Panknin, U.; Gorb, S.N.; Gutowska, M.A. Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS One 2011, 6, e24223.
[167]
Chassot, E.; Bonhommeau, S.; Dulvy, N.K.; Mélin, F.; Watson, R.; Gascuel, D.; Le Pape, O. Global marine primary production constrains fisheries catches. Ecol. Lett. 2010, 13, 495–505, doi:10.1111/j.1461-0248.2010.01443.x.
[168]
Anger, K. The D0 threshold: A critical point in the larval development of decapod crustaceans. J. Exp. Mar. Biol. Ecol. 1987, 108, 15–30, doi:10.1016/0022-0981(87)90128-6.
[169]
Strathmann, R. Larval Feeding. In Reproduction of Marine Invertebrates. General Aspects, Seeking Unity in Diversity; Giese, A.C., Pearse, A.C., Pearse, J.S., Eds.; Blackwell Scientific Publishing: San Francisco, CA, USA, 1987; Volume 9, pp. 465–550.
[170]
Hart, M.W.; Strathmann, R.R. Functional consequences of phenotypic plasticity in echinoid larvae. Biol. Bull. 1994, 186, 291–299, doi:10.2307/1542275.
