Upper environmental pCO2 drives sensitivity to ocean acidification in marine invertebrates
1.Gattuso, J.-P. et al. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349, aac4722 (2015).
Google Scholar
2.Caldeira, K. & Wickett, M. E. Anthropogenic carbon and ocean pH. Nature 425, 365 (2003).CAS
Google Scholar
3.Hönisch, B. et al. The geological record of ocean acidification. Science 335, 1058–1063 (2012).
Google Scholar
4.Turley, C. & Gattuso, J.-P. Future biological and ecosystem impacts of ocean acidification and their socioeconomic-policy implications. Curr. Opin. Environ. Sustain. 4, 278–286 (2012).
Google Scholar
5.San Martin, V. A. et al. Linking social preferences and ocean acidification impacts in mussel aquaculture. Sci. Rep. 9, 4719 (2019).
Google Scholar
6.Falkenberg, L. et al. Ocean acidification and human health. Int. J. Environ. Res. Public Health 17, 4563 (2020).CAS
Google Scholar
7.Loewe, M. & Rippin, N. The Sustainable Development Goals of the Post-2015 Agenda. Comments on the OWG and SDSN Proposals (German Development Institute 2015).8.Doney, S. C. et al. The impacts of ocean acidification on marine ecosystems and reliant human communities. Annu. Rev. Environ. Resour. 45, 83–112 (2020).
Google Scholar
9.Ekstrom, J. et al. Vulnerability and adaptation of US shellfisheries to ocean acidification. Nat. Clim. Change 5, 207–214 (2015).
Google Scholar
10.Ponce Oliva, R. D. et al. Ocean acidification, consumers’ preferences, and market adaptation strategies in the mussel aquaculture industry. Ecol. Econ. 158, 42–50 (2019).
Google Scholar
11.Quatrinni, A. M. et al. Palaeoclimate ocean conditions shaped the evolution of corals and their skeletons through deep time. Nat. Ecol. Evol. 4, 1531–1538 (2020).
Google Scholar
12.Thomsen, J. et al. Naturally acidified habitat selects for ocean acidification-tolerant mussels. Sci. Adv. 3, e1602411 (2017).
Google Scholar
13.Rastrick, S. S. P. et al. Using natural analogues to investigate the effects of climate change and ocean acidification on Northern ecosystems. ICES J. Mar. Sci. 75, 2299–2311 (2018).
Google Scholar
14.Hall-Spencer, J. M. et al. Volcanic carbon dioxide vents reveal ecosystem effects of ocean acidification. Nature 454, 96–99 (2008).CAS
Google Scholar
15.Agostini, S. et al. Ocean acidification drives community shifts towards simplified non-calcified habitats in a subtropical–temperate transition zone. Sci. Rep. 8, 11354 (2018).
Google Scholar
16.Riquelme-Bugueño, R. et al. Diel vertical migration into anoxic and high-pCO2 waters: acoustic and net-based krill observations in the Humboldt Current. Sci. Rep. 10, 17181 (2020).
Google Scholar
17.Pérez et al. Riverine discharges impact physiological traits and carbon sources for shell carbonate in the marine intertidal mussel Perumytilus purpuratus. Limnol. Oceanogr. 61, 969–983 (2016).
Google Scholar
18.Vargas, C. A. et al. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol. 1, 0084 (2017).
Google Scholar
19.Saavedra et al. Local habitat influences on feeding and respiration of the intertidal mussels Perumytilus purpuratus exposed to increased pCO2 levels. Estuaries Coast. 41, 1118–1129 (2018).CAS
Google Scholar
20.Riebesell, U. & Gattuso, J.-P. Lessons learned from ocean acidification research. Nat. Clim. Change 5, 12–14 (2015).CAS
Google Scholar
21.Tilbrook, B. et al. An enhanced ocean acidification observing network: from people to technology to data synthesis and information exchange. Front. Mar. Sci. 6, 337 (2019).
Google Scholar
22.Barry, J. P., Hall-Spencer, J. M. and Tyrrell, T. in Guide to Best Practices for Ocean Acidification Research and Data Reporting (eds Riebesell, U. et al.) Ch. 3 (Publications Office of the European Union, 2010).23.Vargas, C. A. et al. Influence of glacier melting and river discharges on the nutrient distribution and DIC recycling in the southern Chilean Patagonia. J. Geophys. Res. Biogeosci. 123, 256–270 (2018).
Google Scholar
24.Feely, R. A. et al. Evidence for upwelling of corrosive ‘acidified’ water onto the Continental Shelf. Science 320, 1490–1492 (2008).CAS
Google Scholar
25.Vargas, C. A. et al. Riverine and corrosive upwelling waters influences on the carbonate system in the coastal upwelling area off Central Chile: implications for coastal acidification events. J. Geophys. Res. Biogeosci. 121, 1468–1483 (2016).
Google Scholar
26.Cao, Z. et al. Dynamics of the carbonate system in a large continental shelf system under the influence of both a river plume and coastal upwelling. J. Geophys. Res. Oceans 116, G02010 (2010).
Google Scholar
27.Feely, R. A. et al. The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Est. Coast. Shelf Sci. 88, 442–449 (2010).CAS
Google Scholar
28.Cai, W.-J. et al. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4, 766–770 (2011).CAS
Google Scholar
29.Kwiatkowski, L. et al. Nighttime dissolution in a temperate coastal ocean ecosystem increases under acidification. Sci. Rep. 6, 22984 (2016).CAS
Google Scholar
30.Wolfe, K., Nguyen, H. D., Davey, M. & Byrne, M. Characterizing biogeochemical fluctuations in a world of extremes: a synthesis for temperate intertidal habitats in the face of global change. Glob. Change Biol. 26, 3858–3879 (2020).
Google Scholar
31.Shaw, E. C., Phinn, S. R., Tilbrook, B. & Steven, A. Natural in situ relationships suggest coral reef calcium carbonate production will decline with ocean acidification. Limnol. Oceanogr. 60, 777–788 (2015).
Google Scholar
32.Takeshita, Y. et al. Coral reef carbonate chemistry variability at different functional scales. Front. Mar. Sci. 5, 175 (2018).
Google Scholar
33.Brodeur, J. R. et al. Chesapeake Bay inorganic carbon: spatial distribution and seasonal variability. Front. Mar. Sci. 6, 99 (2019).
Google Scholar
34.Hoshijima, U. & Hofmann, G. E. Variability of seawater chemistry in a kelp forest environment is linked to in situ transgenerational effects in the purple sea urchin, Strongylocentrotus purpuratus. Front. Mar. Sci. 6, 62 (2019).
Google Scholar
35.Koweek, D. A. et al. A year in the life of a central California kelp forest: physical and biological insights into biogeochemical variability. Biogeosciences 14, 31–44 (2017).CAS
Google Scholar
36.Cornwall, C. E. & Hurd, C. L. Experimental design in ocean acidification research: problems and solutions. ICES J. Mar. Sci. 73, 572–581 (2016).
Google Scholar
37.Kapsenberg, L. & Hofmann, G. E. Ocean pH time-series and drivers of variability along the northern Channel Islands, California, USA. Limnol. Oceanogr. 61, 953–968 (2016).
Google Scholar
38.Hofmann, G. E. et al. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6, e28983 (2011).CAS
Google Scholar
39.Baumann, H. Experimental assessments of marine species sensitivities to ocean acidification and co-stressors: how far have we come? Can. J. Zool. 97, 399–408 (2019).
Google Scholar
40.Cornwall, C. E. et al. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc. R. Soc. B 280, 20132201 (2013).
Google Scholar
41.Rivest, E. B., Comeau, S. & Cornwall, C. E. The role of natural variability in shaping the response of coral reef organisms to climate change. Curr. Clim. 3, 271–281 (2017).
Google Scholar
42.Sanford, E. & Kelly, M. W. Local adaptation in marine invertebrates. Annu. Rev. Mar. Sci. 3, 509–535 (2011).
Google Scholar
43.Lewis, C. N. et al. Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice. Proc. Natl Acad. Sci. USA 110, E4960–E4967 (2013).CAS
Google Scholar
44.Spalding, M. D. et al. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–583 (2007).
Google Scholar
45.Aguilera, V. M., Vargas, C. A. & Dewitte, B. Intraseasonal hydrographic variations and nearshore carbonates system off northern Chile during the 2015 El Niño event. J. Geophys. Res. Biogeosci. 125, e2020JG005704 (2020).CAS
Google Scholar
46.Fassbender, A. J. et al. Seasonal carbonate chemistry variability in marine surface waters of the US Pacific Northwest. Earth Syst. Sci. Data 10, 1367–1401 (2018).
Google Scholar
47.Reum, J. C. P. et al. Seasonal carbonate chemistry covariation with temperature, oxygen, and salinity in a fjord estuary: implications for the design of ocean acidification experiments. PLoS ONE 9, e89619 (2014).
Google Scholar
48.Wallace, R. B. et al. Coastal ocean acidification: the other eutrophication problem. Estuar. Coast. Shelf Sci. 148, 1–13 (2014).CAS
Google Scholar
49.Rutgersson, A. et al. The annual cycle of carbon dioxide and parameters influencing the air–sea carbon exchange in the Baltic Proper. J. Mar. Syst. 74, 381–394 (2008).
Google Scholar
50.Clargo, N. M., Salt, L. A., Thomas, H. & de Baar, H. J. W. Rapid increase of observed DIC and pCO2 in the surface waters of the North Sea in the 2001–2011 decade ascribed to climate change superimposed by biological processes. Mar. Chem. 177, 566–581 (2015).CAS
Google Scholar
51.Ericson, Y. et al. Temporal variability in surface water pCO2 in Adventfjorden (West Spitsbergen) with emphasis on physical and biogeochemical drivers. J. Geophys. Res. Oceans 123, 4888–4905 (2018).CAS
Google Scholar
52.Geilfus, N.-X. et al. Spatial and temporal variability of seawater pCO2 within the Canadian Arctic Archipelago and Baffin Bay during the summer and autumn 2011. Cont. Shelf Res. 156, 1–10 (2018).
Google Scholar
53.Islam, F. et al. Sea surface pCO2 and O2 dynamics in the partially ice-covered Arctic Ocean. J. Geophys. Res. Oceans 122, 1425–1438 (2016).
Google Scholar
54.Copin-Montégut, C., Bégovic, M. & Merlivat, L. Variability of the partial pressure of CO2 on diel to annual time scales in the Northwestern Mediterranean Sea. Mar. Chem. 85, 169–189 (2004).
Google Scholar
55.Pardo, P. C. et al. Surface ocean carbon dioxide variability in South Pacific boundary currents and Subantarctic waters. Sci. Rep. 9, 7592 (2019).
Google Scholar
56.Gagliano, M., McCormick, M. I., Moore, J. A. & Depczynski, M. The basics of acidification: baseline variability of pH on Australian coral reefs. Mar. Biol. 157, 1849–1856 (2010).CAS
Google Scholar
57.Takeshita, Y. et al. Including high-frequency variability in coastal acidification projections. Biogeosciences 12, 5853–5870 (2015).
Google Scholar
58.Carter, H. A., Ceballos-Osuna, L., Miller, N. A. & Stillman, J. H. Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes. J. Exp. Biol. 216, 1412–1422 (2013).CAS
Google Scholar
59.Ceballos-Osuna, L., Carter, H. A., Miller, N. A. & Stillman, J. H. Effects of ocean acidification on early life-history stages of the intertidal porcelain crab Petrolisthes cinctipes. J. Exp. Biol. 216, 1405–1411 (2013).CAS
Google Scholar
60.Miller, S. H. et al. Effect of elevated pCO2 on metabolic responses of porcelain crab (Petrolisthes cinctipes) larvae exposed to subsequent salinity stress. PLoS ONE 9, e109167 (2014).
Google Scholar
61.Bayne, B. L. Metabolic expenditure. Dev. Aquacult. Fish. Sci. 41, 331–415 (2017).
Google Scholar
62.Waldbusser, G. G. et al. Slow shell building, a possible trait for resistance to the effects of acute ocean acidification. Limnol. Oceanogr. 61, 1969–1983 (2016).
Google Scholar
63.Dorey, N., Lancon, P., Thorndyke, M. & Dupont, S. Assessing physiological tipping point for sea urchin larvae exposed to a broad range of pH. Glob. Change Biol. 19, 3355–3367 (2013).
Google Scholar
64.Kelly, M. W., Padilla-Gamiño, J. L. & Hofmann, G. E. Natural variation and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus. Glob. Change Biol. 19, 2536–2546 (2015).
Google Scholar
65.Gaitán-Espitia, J. D. et al. Spatio–temporal environmental variation mediates geographical differences in phenotypic responses to ocean acidification. Biol. Lett. 13, 20160865 (2017).
Google Scholar
66.Calosi, P. et al. Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid–base and ion-regulatory abilities. Mar. Pollut. Bull. 73, 470–484 (2013).CAS
Google Scholar
67.Foo, S. A., Dworjanyn, S. A., Poore, A. G. B. & Byrne, M. Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS ONE 7, e42497 (2012).CAS
Google Scholar
68.Chan, K. Y. K., Grünbaum, D., Arnberg, M. & Dupont, S. Impacts of ocean acidification on survival, growth, and swimming behaviours differ between larval urchins and brittlestars. ICES J. Mar. Sci. 73, 951–996 (2016).
Google Scholar
69.Stumpp, M. et al. Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc. Natl Acad. Sci. USA 109, 18192–18197 (2012).CAS
Google Scholar
70.Stumpp, M. et al. Digestion in sea urchin larvae impaired under ocean acidification. Nat. Clim. Change 3, 1044–1049 (2013).CAS
Google Scholar
71.Thor, P. & Dupont, S. Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob. Change Biol. 21, 2261–2271 (2015).
Google Scholar
72.Gibbin, E. M. et al. The evolution of phenotypic plasticity under global change. Sci. Rep. 7, 17253 (2017).
Google Scholar
73.Gibbin, E. M. et al. Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life history and physiology in a marine metazoan? J. Exp. Biol. 220, 551–563 (2017).
Google Scholar
74.Dam, H. G. et al. Rapid, but limited, zooplankton adaptation to simultaneous warming and acidification. Nat. Clim. Change 11, 780–786 (2021).
Google Scholar
75.Byrne, M. 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. 49, 1–42 (2011).
Google Scholar
76.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. 13, 1419–1434 (2010).
Google Scholar
77.Kroeker et al. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19, 1884–1896 (2013).
Google Scholar
78.Takahashi, T., Sutherland, S. C. & Kozyr, A. LDEO Database (Version 2019): Global Ocean Surface Water Partial Pressure of CO2 Database: Measurements Performed During 1957–2019 (NCEI Accession 0160492) Version 9.9 (National Oceanic and Atmospheric Administration National Centers for Environmental Information); https://doi.org/10.3334/CDIAC/OTG.NDP088(V2015)79.Manly, B. F. J. Randomization, Bootstrap and Monte Carlo Methods in Biology (CRC Press, 1997).80.Martinez, W. L. & Martinez, A. R. Computational Statistics Handbook with MATLAB (CRC Press, 2002). More