Oceanography The Official Magazine of
The Oceanography Society
Volume 28 Issue 02

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Volume 28, No. 2
Pages 48 - 61

And on Top of All That… Coping with Ocean Acidification in the Midst of Many Stressors

Denise L. Breitburg Joseph Salisbury Joan M. BernhardWei-Jun Cai Sam Dupont Scott C. DoneyKristy J. KroekerLisa A. Levin W. Christopher Long Lisa M. Milke Seth H. MillerBeth PhelanUta Passow Brad A. Seibel Anne E. TodghamAnn M. Tarrant
Article Abstract

Oceanic and coastal waters are acidifying due to processes dominated in the open ocean by increasing atmospheric CO2 and dominated in estuaries and some coastal waters by nutrient-fueled respiration. The patterns and severity of acidification, as well as its effects, are modified by the host of stressors related to human activities that also influence these habitats. Temperature, deoxygenation, and changes in food webs are particularly important co-stressors because they are pervasive, and both their causes and effects are often mechanistically linked to acidification. Development of a theoretical underpinning to multiple stressor research that considers physiological, ecological, and evolutionary perspectives is needed because testing all combinations of stressors and stressor intensities experimentally is impossible. Nevertheless, use of a wide variety of research approaches is a logical and promising strategy for improving understanding of acidification and its effects. Future research that focuses on spatial and temporal patterns of stressor interactions and on identifying mechanisms by which multiple stressors affect individuals, populations, and ecosystems is critical. It is also necessary to incorporate consideration of multiple stressors into management, mitigation, and adaptation to acidification and to increase public and policy recognition of the importance of addressing acidification in the context of the suite of other stressors with which it potentially interacts.


Breitburg, D.L., J. Salisbury, J.M. Bernhard, W.-J. Cai, S. Dupont, S.C. Doney, K.J. Kroeker, L.A. Levin, W.C. Long, L.M. Milke, S.H. Miller, B. Phelan, U. Passow, B.A. Seibel, A.E. Todgham, and A.M. Tarrant. 2015. And on top of all that… Coping with ocean acidification in the midst of many stressors. Oceanography 28(2):48–61, https://doi.org/10.5670/oceanog.2015.31.


Alsterberg, C., J.S. Eklöf, L. Gamfeldt, J.N. Havenhand, and K. Sundbäck. 2013. Consumers mediate the effects of experimental ocean acidification and warming on primary producers. Proceedings of the National Academy of Sciences of the United States of America 110:8,603–8,608, https://doi.org/10.1073/pnas.1303797110.

Baker, A.C., P.W. Glynn, and B. Riegl. 2008. Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine, Coastal and Shelf Science 80:435–471, https://doi.org/10.1016/j.ecss.2008.09.003.

Baumann, H., R.B. Wallace, T. Tagliaferri, and C.J. Gobler. 2015. Large natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales. Estuaries and Coasts 38:220–231, https://doi.org/10.1007/s12237-014-9800-y.

Bibby, R., P. Cleall-Harding, S. Rundle, S. Widdicombe, and J. Spicer. 2007. Ocean acidification disrupts induced defenses in the intertidal gastropod Littorina littorea. Biology Letters 3:699–701.

Bopp, L., L. Resplandy, J. Orr, S. Doney, J. Dunne, M. Gehlen, P. Halloran, C. Heinze, T. Ilyina, and R. Séférian. 2013. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10:6,225–6,245, https://doi.org/10.5194/bg-10-6225-2013.

Boyd, J.N., and L.E. Burnett. 1999. Reactive oxygen intermediate production by oyster hemocytes exposed to hypoxia. Journal of Experimental Biology 202:3,135–3,143.

Boyd, P.W., and D.A. Hutchins. 2012. Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Marine Ecology Progress Series 470:125–135, https://doi.org/10.3354/meps10121.

Breitburg, D.L., and G.F. Riedel. 2005. Multiple stressors in marine systems. Pp.167–182 in Marine Conservation Biology: The Science of Maintaining the Sea’s Biodiversity. E.A. Norse and L.B. Crowder, eds, Island Press, Washington.

Cai, W.-J., X. Hu, W.-J. Huang, M.C. Murrell, J.C. Lehrter, S.E. Lohrenz, W.-C. Chou, W. Zhai, J.T. Hollibaugh, and Y. Wang. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience 4:766–770, https://doi.org/10.1038/ngeo1297.

Cai, W.-J., and C.E. Reimers. 1993. The development of pH and pCO2 microelectrodes for studying the carbonate chemistry of pore waters near the sediment-water interface. Limnology and Oceanography 38:1,762–1,773, https://doi.org/10.4319/lo.1993.38.8.1762.

Chen, X., and J.H. Stillman. 2012. Multigenerational analysis of temperature and salinity variability affects on metabolic rate, generation time, and acute thermal and salinity tolerance in Daphnia pulex. Journal of Thermal Biology 37:185–194, https://doi.org/10.1016/j.jtherbio.2011.12.010.

Cloern, J.E., and A.D. Jassby. 2012. Drivers of change in estuarine-coastal ecosystems: Discoveries from four decades of study in San Francisco Bay. Reviews of Geophysics 50, RG4001, https://doi.org/10.1029/2012RG000397.

Cooley, S.R., H.L. Kite-Powell, and S.C. Doney. 2009. Ocean acidification’s potential to alter global marine ecosystem services. Oceanography 22(4):172–181, https://doi.org/10.5670/oceanog.2009.106.

Côté, I.M., and E.S. Darling. 2010. Rethinking ecosystem resilience in the face of climate change. PLOS Biology 8(7):e1000438, https://doi.org/10.1371/journal.pbio.1000438.

Crain, C.M., K. Kroeker, and B.S. Halpern. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters 11:1,304–1,315, https://doi.org/10.1111/j.1461-0248.2008.01253.x.

Crozier, L., A. Hendry, P. Lawson, T. Quinn, N. Mantua, J. Battin, R. Shaw, and R. Huey. 2008. Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific salmon. Evolutionary Applications 1:252–270, https://doi.org/10.1111/j.1752-4571.2008.00033.x.

Darling, E.S., T.R. McClanahan, and I.M. Côté. 2010. Combined effects of two stressors on Kenyan coral reefs are additive or antagonistic, not synergistic. Conservation Letters 3:122–130, https://doi.org/10.1111/j.1755-263X.2009.00089.x.

Doney, S.C., M. Ruckelshaus, J.E. Duffy, J.P. Barry, F. Chan, C.A. English, H.M. Galindo, J.M. Grebmeier, A.B. Hollowed, and N. Knowlton. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science 4:11–37, https://doi.org/10.1146/annurev-marine-041911-111611.

Duarte, C.M., I.E. Hendriks, T.S. Moore, Y.S. Olsen, A. Steckbauer, L. Ramajo, J. Carstensen, J.A. Trotter, and M. McCulloch. 2013. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 36:221–236, https://doi.org/10.1007/s12237-013-9594-3.

Dupont, S., N. Dorey, M. Stumpp, F. Melzner, and M. Thorndyke. 2013. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Marine Biology 160:1,835–1,843, https://doi.org/10.1007/s00227-012-1921-x.

Falter, J.L., R.J. Lowe, Z. Zhang, and M. McCulloch. 2013. Physical and biological controls on the carbonate chemistry of coral reef waters: Effects of metabolism, wave forcing, sea level, and geomorphology. PLoS ONE 8(1):e53303, https://doi.org/10.1371/journal.pone.0053303.

Falkenberg, L.J., B.D. Russell, and S.D. Connell. 2012. Stability of strong species interactions resist the synergistic effects of local and global pollution in kelp forests. PLoS ONE 7(3):e33841, https://doi.org/10.1371/journal.pone.0033841.

Feely, R.A., S.R. Alin, J. Newton, C.L. Sabine, M. Warner, A. Devol, C. Krembs, and C. Maloy. 2010. The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuarine, Coastal and Shelf Science 88:442–449, https://doi.org/10.1016/j.ecss.2010.05.004.

Feely, R.A., C.L. Sabine, J.M. Hernandez-Ayon, D. Ianson, and B. Hales. 2008. Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320:1,490–1,492, https://doi.org/10.1126/science.1155676.

Ferrari, M.C., M.I. McCormick, P.L. Munday, M.G. Meekan, D.L. Dixson, O. Lonnstedt, and D.P. Chivers. 2011. Putting prey and predator into the CO2 equation–qualitative and quantitative effects of ocean acidification on predator–prey interactions. Ecology Letters 14:1,143–1,148, https://doi.org/10.1111/j.1461-0248.2011.01683.x.

Foster, L.C., D.N. Schmidt, E. Thomas, S. Arndt, and A. Ridgwell. 2013. Surviving rapid climate change in the deep sea during the Paleogene hyperthermals. Proceedings of the National Academy of Sciences of the United States of America 110:9,273–9,276, https://doi.org/10.1073/pnas.1300579110.

Frieder, C., S. Nam, T. Martz, and L. Levin. 2012. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9:3,917–3,930, https://doi.org/10.5194/bg-9-3917-2012.

Gaylord, B., K.J. Kroeker, J.M. Sunday, K.M. Anderson, J.P. Barry, N.E. Brown, S.D. Connell, S. Dupont, K.E. Fabricius, J.M. Hall-Spencer and others. 2014. Ocean acidification through the lens of ecological theory. Ecology 96:3–15, https://doi.org/10.1890/14-0802.1.

Gianguzza, P., G. Visconti, F. Gianguzza, S. Vizzini, G. Sarà, and S. Dupont. 2013. Temperature modulates the response of the thermophilous sea urchin Arbacia lixula early life stages to CO2-driven acidification. Marine Environmental Research. 93:70–77, https://doi.org/10.1016/j.marenvres.2013.07.008.

Glud, R.N. 2008. Oxygen dynamics of marine sediments. Marine Biology Research 4:243–289.

Gobler, C.J., E.L. DePasquale, A.W. Griffith, and H. Baumann. 2014. Hypoxia and acidification have additive and synergistic negative effects on the growth, survival, and metamorphosis of early life stage bivalves. PLoS ONE 9:e83648, https://doi.org/10.1371/journal.pone.0083648.

Green, M.A., G.G. Waldbusser, S.L. Reilly, K. Emerson, and S. O’Donnell. 2009. Death by dissolution: Sediment saturation state as a mortality factor for juvenile bivalves. Limnology and Oceanography 54:1,037–1,047, https://doi.org/10.4319/lo.2009.54.4.1037.

Griffith, G.P., E.A. Fulton, and A.J. Richardson. 2011. Effects of fishing and acidification-related benthic mortality on the southeast Australian marine ecosystem. Global Change Biology 17:3,058–3,074, https://doi.org/10.1111/j.1365-2486.2011.02453.x.

Hettinger, A., E. Sanford, T.M. Hill, A.D. Russell, K.N. Sato, J. Hoey, M. Forsch, H.N. Page, and B. Gaylord. 2012. Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology 93:2,758–2,768, https://doi.org/10.1890/12-0567.1.

Hofmann, M., and H.-J. Schellnhuber. 2009. Oceanic acidification affects marine carbon pump and triggers extended marine oxygen holes. Proceedings of the National Academy of Sciences of the United States of America 106:3,017–3,022, https://doi.org/10.1073/pnas.0813384106.

Hopkinson, C.S., and E.M. Smith. 2005. Estuarine respiration: An overview of benthic, pelagic, and whole system respiration. Pp. 122–146 in Respiration in Aquatic Ecosystems. P. del Giorgio and P. Williams, eds, https://doi.org/10.1093/acprof:oso/9780198527084.003.0008.

Hutchins, D.A., F.X. Fu, E.A. Webb, N. Walworth, and A. Tagliabue. 2013. Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nature Geoscience 6:790–795, https://doi.org/10.1038/ngeo1858.

Ingels, J., A. Vanreusel, A. Brandt, A.I. Catarino, B. David, C. De Ridder, P. Dubois, A.J. Gooday, P. Martin, and F. Pasotti. 2012. Possible effects of global environmental changes on Antarctic benthos: A synthesis across five major taxa. Ecology and Evolution 2:453–485, https://doi.org/10.1002/ece3.96.

IPCC. 2014. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York, New York, USA.

Keeling, R.F., A. Körtzinger, and N. Gruber. 2010. Ocean deoxygenation in a warming world. Annual Review of Marine Science 2:199–229, https://doi.org/10.1146/annurev.marine.010908.163855.

Kelly, R.P., M. Foley, W. Fisher, R. Feely, B. Halpern, G. Waldbusser, and M. Caldwell. 2011. Mitigating local causes of ocean acidification with existing laws. Science 332:1,036–1,037, https://doi.org/10.1126/science.1203815.

Knutson, T.R., J.L. McBride, J. Chan, K. Emanuel, G. Holland, C. Landsea, I. Held, J.P. Kossin, A. Srivastava, and M. Sugi. 2010. Tropical cyclones and climate change. Nature Geoscience 3:157–163, https://doi.org/10.1038/ngeo779.

Kremp, A., A. Godhe, J. Egardt, S. Dupont, S. Suikkanen, S. Casabianca, and A. Penna. 2012. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecology and Evolution 2:1,195–1,207, https://doi.org/10.1002/ece3.245.

Kroeker, K.J., R.L. Kordas, R. Crim, I.E. Hendriks, L. Ramajo, G.S. Singh, C.M. Duarte, and J.P. Gattuso. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19:1,884–1,896, https://doi.org/10.1111/gcb.12179.

Kroeker, K.J., E. Sanford, B.M. Jellison, and B. Gaylord. 2014. Predicting the effects of ocean acidification on predator-prey interactions: A conceptual framework based on coastal molluscs. The Biological Bulletin 226:211–222.

Levin, L.A., B. Hönisch, and C.A. Frieder. 2015. Geochemical proxies for estimating faunal exposure to ocean acidification. Oceanography 28(2):62–73, https://doi.org/10.5670/oceanog.2015.32.

Levin, L.A., K.-K. Liu, K.-C. Emeis, D.L. Breitburg, J. Cloern, C. Deutsch, M. Giani, A. Goffart, E.E. Hofmann, Z. Lachkar, and others. 2014. Comparative biogeochemistry-ecosystem-human interactions on dynamic continental margins. Journal of Marine Systems 141:3–17, https://doi.org/10.1016/j.jmarsys.2014.04.016.

Long, C.W., K.M. Swiney, and R.J. Foy. 2013. Effects of ocean acidification on the embryos and larvae of red king crab, Paralithodes camtschaticus. Marine Pollution Bulletin 69:38–47, https://doi.org/10.1016/j.marpolbul.2013.01.011.

Maas, A.E., L.E. Elder, H.M. Dierssen, and B.A. Seibel. 2011. Metabolic response of Antarctic pteropods (Mollusca: Gastropoda) to food deprivation and regional productivity. Marine Ecology Progress Series 441:129–139, https://doi.org/10.3354/meps09358.

Manzello, D.P., J.A. Kleypas, D.A. Budd, C.M. Eakin, P.W. Glynn, and C. Langdon. 2008. Poorly cemented coral reefs of the eastern tropical Pacific: Possible insights into reef development in a high-CO2 world. Proceedings of the National Academy of Sciences of the United States of America 105:10,450–10,455, https://doi.org/10.1073/pnas.0712167105.

Martin, S., and J.P. Gattuso. 2009. Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biology 15:2,089–2,100, https://doi.org/10.1111/j.1365-2486.2009.01874.x.

Melzner, F., J. Thomsen, W. Koeve, A. Oschlies, M.A. Gutowska, H.W. Bange, H.P. Hansen, and A. Körtzinger. 2013. Future ocean acidification will be amplified by hypoxia in coastal habitats. Marine Biology 160:1,875–1,888, https://doi.org/10.1007/s00227-012-1954-1.

Metzger, R., F.J. Sartoris, M. Langenbuch, and H.O. Pörtner. 2007. Influence of elevated CO2 concentrations on thermal tolerance of the edible crab Cancer pagurus. Journal of Thermal Biology 32:144–151, https://doi.org/10.1016/j.jtherbio.2007.01.010.

Mikulski, C.M., L.E. Burnett, and K.G. Burnett. 2000. The effects of hypercapnic hypoxia on the survival of shrimp challenged with Vibrio parahaemolyticus. Journal of Shellfish Research 19:301–311.

Miller, S.H., S. Zarate, E.H. Smith, B. Gaylord, J.D. Hosfelt, and T.M. Hill. 2014. Effect of elevated pCO2 on metabolic responses of porcelain crab (Petrolisthes cinctipes) larvae exposed to subsequent salinity stress. PLoS ONE 9:e109167, https://doi.org/10.1371/journal.pone.0109167.

Mukherjee, J., K.K. Wong, K.H. Chandramouli, P.Y. Qian, P.T. Leung, R.S. Wu, and V. Thiyagarajan. 2013. Proteomic response of marine invertebrate larvae to ocean acidification and hypoxia during metamorphosis and calcification. The Journal of Experimental Biology 216:4,580–4,589, https://doi.org/10.1242/jeb.094516.

Munday, P.L., R.R. Warner, K. Monro, J.M. Pandolfi, and D.J. Marshall. 2013. Predicting evolutionary responses to climate change in the sea. Ecology Letters 16:1,488–1,500, https://doi.org/10.1111/ele.12185.

Murray, C.S., A. Malvezzi, C.J. Gobler, and H. Baumann. 2014. Offspring sensitivity to ocean acidification changes seasonally in a coastal marine fish. Marine Ecology Progress Series 504:1–11, https://doi.org/10.3354/meps10791.

O’Donnell, M.J., L.M. Hammond, and G.E. Hofmann. 2009. Predicted impact of ocean acidification on a marine invertebrate: Elevated CO2 alters response to thermal stress in sea urchin larvae. Marine Biology 156:439–446, https://doi.org/10.1007/s00227-008-1097-6.

Paulmier, A., D. Ruiz-Pino, and V. Garçon. 2011. CO2 maximum in the oxygen minimum zone (OMZ). Biogeosciences 8:239–252, https://doi.org/10.5194/bg-8-239-2011.

Pedersen, S.A., O.J. Håkedal, I. Salaberria, A. Tagliati, L.M. Gustavson, B.M. Jenssen, A.J. Olsen, and D. Altin. 2014. Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates. Environmental Science & Technology 48:12,275–12,284, https://doi.org/10.1021/es501581j.

Podolsky, R.D., and A.L. Moran. 2006. Integrating function across marine life cycles. Integrative and Comparative Biology 46:577–586, https://doi.org/10.1093/icb/icl026.

Pörtner, H.O. 2012. A new challenge. Journal of Thermal Biology 37:547, https://doi.org/10.1016/j.jtherbio.2012.06.009.

Pörtner, H.O., M. Gutowska, A. Ishimatsu, M. Lucassen, F. Melzner, and B. Seibel. 2011. Effects of ocean acidification on nektonic organisms. Pp. 154–175 in Ocean Acidification. J.P. Gattuso and L. Hansson, eds, Oxford University Press, Oxford.

Rabalais, N.N., W.-J. Cai, J. Carstensen, D.J. Conley, B. Fry, X. Hu, Z. Quinones-Rivera, R. Rosenberg, C.P. Slomp, and R.E. Turner. 2014. Eutrophication-driven deoxygenation in the coastal ocean. Oceanography 27(1):172–183, https://doi.org/10.5670/oceanog.2014.21.

Riebesell, U., J. Czerny, K.V. Bröckel, T. Boxhammer, J. Büdenbender, M. Deckelnick, M. Fischer, D. Hoffmann, S. Krug, and U. Lentz. 2012. Technical note: A mobile sea-going mesocosm system–new opportunities for ocean change research. Biogeosciences Discussions 9:12,985–13,017, https://doi.org/10.5194/bg-10-1835-2013.

Riebesell, U., and P.D. Tortell. 2011. Effects of ocean acidification on pelagic organisms and ecosystems. Pp. 99–121 in Ocean Acidification. J.P. Gattuso and L. Hansson, eds, Oxford University Press, Oxford.

Robbins, L.L., J.G. Wynn, J.T. Lisle, K.K. Yates, P.O. Knorr, R.H. Byrne, X. Liu, M.C. Patsavas, K. Azetsu-Scott, and T. Takahashi. 2013. Baseline monitoring of the western Arctic Ocean estimates 20% of Canadian Basin surface waters are undersaturated with respect to aragonite. PLoS ONE 8:e73796, https://doi.org/10.1371/journal.pone.0073796.

Ruckelshaus, M., S. Doney, H. Galindo, J. Barry, F. Chan, J. Duffy, C. English, S. Gaines, J. Grebmeier, and A. Hollowed. 2013. Securing ocean benefits for society in the face of climate change. Marine Policy 40:154–159, https://doi.org/10.1016/j.marpol.2013.01.009.

Rummer, J.L., J.A. Stecyk, C.S. Couturier, S.-A. Watson, G.E. Nilsson, and P.L. Munday. 2013. Elevated CO2 enhances aerobic scope of a coral reef fish. Conservation Physiology 1:cot023, https://doi.org/10.1093/conphys/cot023.

Salisbury, J.E., D. Vandemark, C.W. Hunt, J.W. Campbell, W.R. McGillis, and W.H. McDowell. 2008. Seasonal observations of surface waters in two Gulf of Maine estuary-plume systems: Relationships between watershed attributes, optical measurements and surface pCO2. Estuarine, Coastal and Shelf Science 77:245–252, https://doi.org/10.1016/j.ecss.2007.09.033.

Schade, F.M., C. Clemmesen, and K.M. Wegner. 2014. Within- and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (Gasterosteus aculeatus). Marine Biology 161:1,667–1,676, https://doi.org/10.1007/s00227-014-2450-6.

Scheffer, M., and S.R. Carpenter. 2003. Catastrophic regime shifts in ecosystems: Linking theory to observation. Trends in Ecology & Evolution 18:648–656, https://doi.org/10.1016/j.tree.2003.09.002.

Schoo, K.L., A.M. Malzahn, E. Krause, and M. Boersma. 2013. Increased carbon dioxide availability alters phytoplankton stoichiometry and affects carbon cycling and growth of a marine planktonic herbivore. Marine Biology 160:2,145–2,155, https://doi.org/10.1007/s00227-012-2121-4.

Seebah, S., C. Fairfield, M.S. Ullrich, and U. Passow. 2014. Aggregation and sedimentation of Thalassiosira weissflogii (diatom) in a warmer and more acidified future ocean. PLoS ONE 9:e112379, https://doi.org/10.1371/journal.pone.0112379.

Seibel, B.A. 2011. Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. The Journal of Experimental Biology 214:326–336, https://doi.org/10.1242/jeb.049171.

Seibel, B.A. 2015. Environmental physiology of the jumbo squid, Dosidicus gigas (d’Orbigny, 1835) (Cephalopoda: Ommastrephidae): Implications for changing climate. American Malacological Bulletin 33:1–13, https://doi.org/10.4003/006.033.0113.

Seibel, B.A., A.E. Maas, and H.M. Dierssen. 2012. Energetic plasticity underlies a variable response to ocean acidification in the pteropod, Limacina helicina antarctica. PLoS ONE 7:e30464, https://doi.org/10.1371/journal.pone.0030464.

Sett, S., L.T. Bach, K.G. Schulz, S. Koch-Klavsen, M. Lebrato, and U. Riebesell. 2014. Temperature modulates coccolithophorid sensitivity of growth, photosynthesis and calcification to increasing seawater pCO2. PLoS ONE 9:e88308, https://doi.org/10.1371/journal.pone.0088308.

Sinclair, B.J., L.V. Ferguson, G. Salehipour-Shirazi, and H.A. MacMillan. 2013. Cross-tolerance and cross-talk in the cold: Relating low temperatures to desiccation and immune stress in insects. Integrative and Comparative Biology 53:545–556, https://doi.org/10.1093/icb/ict004.

Somero, G.N. 2012. The physiology of global change: linking patterns to mechanisms. Annual Review of Marine Science 4:39–61, https://doi.org/10.1146/annurev-marine-120710-100935.

Steinacher, M., F. Joos, T. Frolicher, G.-K. Plattner, and S.C. Doney. 2009. Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6:515–533, https://doi.org/10.5194/bg-6-515-2009.

Strong, A.L., K.J. Kroeker, L.T. Teneva, L.A. Mease, and R.P. Kelly. 2014. Ocean Acidification 2.0: managing our changing coastal ocean chemistry. BioScience, https://doi.org/10.1093/biosci/biu072.

Stumpp, M., M. Hu, I. Casties, R. Saborowski, M. Bleich, F. Melzner, and S. Dupont. 2013. Digestion in sea urchin larvae impaired under ocean acidification. Nature Climate Change 3:1,044–1,049, https://doi.org/10.1038/nclimate2028.

Stumpp, M., M.Y. Hu, F. Melzner, M.A. Gutowska, N. Dorey, N. Himmerkus, W.C. Holtmann, S.T. Dupont, M.C. Thorndyke, and M. Bleich. 2012. Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proceedings of the National Academy of Sciences of the United States of America 109:18,192–18,197, https://doi.org/10.1073/pnas.1209174109.

Sugie, K., H. Endo, K. Suzuki, J. Nishioka, H. Kiyosawa, and T. Yoshimura. 2013. Synergistic effects of pCO2 and iron availability on nutrient consumption ratio of the Bering Sea phytoplankton community. Biogeosciences 10:6,309–6,321, https://doi.org/10.5194/bg-10-6309-2013.

Sydeman, W., M. García-Reyes, D. Schoeman, R. Rykaczewski, S. Thompson, B. Black, and S. Bograd. 2014. Climate change and wind intensification in coastal upwelling ecosystems. Science 345:77–80, https://doi.org/10.1126/science.1251635.

Thomsen, J., I. Casties, C. Pansch, A. Körtzinger, and F. Melzner. 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: Laboratory and field experiments. Global Change Biology 19:1,017–1,027, https://doi.org/10.1111/gcb.12109.

Todgham, A.E., and J.H. Stillman. 2013. Physiological responses to shifts in multiple environmental stressors: Relevance in a changing world. Integrative and Comparative Biology 53:539–544, https://doi.org/10.1093/icb/ict086.

Vargas, C.A., M. de la Hoz, V. Aguilera, V. San Martín, P.H. Manríquez, J.M. Navarro, R. Torres, M.A. Lardies, and N.A. Lagos. 2013. CO2-driven ocean acidification reduces larval feeding efficiency and changes food selectivity in the mollusk Concholepas concholepas. Journal of Plankton Research, https://doi.org/10.1093/plankt/fbt045.

Vinebrooke, R.D., K. Cottingham, M.S. Norberg, S. Dodson, S. Maberly, and U. Sommer. 2004. Impacts of multiple stressors on biodiversity and ecosystem functioning: The role of species co-tolerance. Oikos 104:451–457, https://doi.org/10.1111/j.0030-1299.2004.13255.x.

Waldbusser, G.G., E.N. Powell, and R. Mann. 2013. Ecosystem effects of shell aggregations and cycling in coastal waters: An example of Chesapeake Bay oyster reefs. Ecology 94:895–903, https://doi.org/10.1890/12-1179.1.

Wallace, R.B., H. Baumann, J.S. Grear, R.C. Aller, and C.J. Gobler. 2014. Coastal ocean acidification: The other eutrophication problem. Estuarine, Coastal and Shelf Science 148:1–13, https://doi.org/10.1016/j.ecss.2014.05.027.

Washington State Blue Ribbon Panel on Ocean Acidification. 2012. Ocean Acidification: From Knowledge to Action, Washington State’s Strategic Response.

Yamamoto-Kawai, M., F.A. McLaughlin, and E.C. Carmack. 2011. Effects of ocean acidification, warming and melting of sea ice on aragonite saturation of the Canada Basin surface water. Geophysical Research Letters 38, L03601, https://doi.org/10.1029/2010GL045501.