Oceanic uptake of CO2 can mitigate climate change, but also results in global ocean acidification. Ocean acidification-related changes to the marine carbonate system can disturb ecosystems and hinder calcification by some organisms. Here, we use the calcification response of planktonic foraminifera as a tool to reconstruct the progression of ocean acidification in the California Current Ecosystem through the twentieth century. Measurements of nearly 2,000 fossil foraminifera shell weights and areas preserved in a marine sediment core showed a 20% reduction in calcification by a surface-dwelling foraminifera species. Using modern calibrations, this response translates to an estimated 35% reduction in carbonate ion concentration, a biologically important chemical component of the carbonate system. Assuming other aspects of the carbonate system, this represents a 0.21 decline in pH, exceeding the estimated global average decline by more than a factor of two. Our proxy record also shows considerable variability that is significantly correlated with Pacific Decadal Oscillation and decadal-scale changes in upwelling strength, a relationship that until now has been obscured by the relatively short observational record. This modulation suggests that climatic variations will play an important role in amplifying or alleviating the anthropogenic signal and progression of ocean acidification in this region.
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The authors declare that the data supporting the findings of this study are available within the article. New data generated as a part of this study have been made publicly available via PANGAEA (PDI-21505; https://doi.pangaea.de/10.1594/PANGAEA.909101). Additional data related to this study are available from the corresponding author on request. Publicly available data used in this study are described below. Carbonate chemistry measurements made within the SBB were collected seasonally by the California Cooperative Oceanic Fisheries Investigations time-series (CalCOFI; http://calcofi.org/) and during several NOAA West Coast Ocean Acidification Cruises (WCOA; https://www.nodc.noaa.gov/ocads/oceans/Coastal/WCOA.html). Observational data from the Hawaii Ocean Time-series program (HOT; http://hahana.soest.hawaii.edu/hot/) were also used. Shore Station Data (salinity; https://shorestations.ucsd.edu/shore-stations-data/) were used for carbonate system calculations.
Lüthi, D. et al. High-resolution carbon dioxide concentration record 650,000–800,000 years before present. Nature 453, 379–382 (2008).
Feely, R. A. et al. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366 (2004).
Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).
Gruber, N. et al. The ocean sink for anthropogenic CO2 from 1994 to 2007. Science 363, 1193–1199 (2019).
Khatiwala, S. et al. Global ocean storage of anthropogenic carbon. Biogeosciences 10, 2169–2191 (2013).
Le Quéré, C. et al. Global carbon budget 2015. Earth Syst. Sci. Data 7, 349–396 (2015).
Bednaršek, N. et al. New ocean, new needs: application of pteropod shell dissolution as a biological indicator for marine resource management. Ecol. Indic. 76, 240–244 (2017).
de Moel, H. et al. Planktic foraminiferal shell thinning in the Arabian Sea due to anthropogenic ocean acidification? Biogeosciences 6, 1917–1925 (2009).
De’ath, G., Lough, J. M. & Fabricius, K. E. Declining coral calcification on the Great Barrier Reef. Science 342, 116–119 (2009).
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. 65, 414–432 (2008).
Meier, K. J. S., Beaufort, L., Heussner, S. & Ziveri, P. The role of ocean acidification in Emiliania huxleyi coccolith thinning in the Mediterranean Sea. Biogeosciences 11, 2857–2869 (2014).
Moy, A. D., Howard, W. R., Bray, S. G. & Trull, T. W. Reduced calcification in modern Southern Ocean planktonic foraminifera. Nat. Geosci. 2, 276–280 (2009).
Ries, J. B., Cohen, A. L. & McCorkle, D. C. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 1131–1134 (2009).
Rivero-Calle, S., Gnanadesikan, A., Del Castillo, C. E., Balch, W. M. & Guikema, S. D. Multidecadal increase in North Atlantic coccolithophores and the potential role of rising CO2. Science 350, 1533–1537 (2015).
Iglesias-Rodriguez, D. et al. Phytoplankton calcification in a high-CO2 world. Science 320, 336–340 (2008).
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 320, 1490–1492 (2008).
Feely, R. A. et al. Chemical and biological impacts of ocean acidification along the west coast of North America. Estuar. Coast. Shelf Sci. 183, 260–270 (2016).
Feely, R. A. et al. The combined effects of acidification and hypoxia on pH and aragonite saturation in the coastal waters of the Californian Current Ecosystem and the northern Gulf of Mexico. Cont. Shelf Res. 152, 50–60 (2018).
Hauri, C. et al. Ocean acidification in the California Current System. Oceanography 22, 60–71 (2009).
Turi, G., Lachkar, Z., Gruber, N. & Munnich, M. Climatic modulation of recent trends in ocean acidification in the California Current System. Environ. Res. Lett. 11, 014007 (2016).
Gruber, N. et al. Rapid progression of ocean acidification in the California Current System. Science 337, 220–223 (2012).
Hauri, C., Gruber, N., McDonnell, A. M. P. & Vogt, M. The intensity duration and severity of low aragonite saturation state events on the California continental shelf. Geophys. Res. Lett. 40, 3424–3429 (2013).
Bednaršek, N. et al. Limacina helicina shell dissolution as an indicator of declining habitat suitability due to ocean acidification in the California Current Ecosystem. Proc. R. Soc. Lond. B 281, 20140123 (2014).
Takahashi, T., Williams, R. T. & Bos, D. L. in GEOSECS Pacific Expedition Volume 3: Hydrographic Data 1973–1974 (eds Broecker, W. S. et al.) 77–83 (National Science Foundation, 1982).
Barker, S. & Elderfield, H. Foraminiferal calcification response to glacial-interglacial changes in atmospheric CO2. Science 297, 833–836 (2002).
Bijma, J., Spero, H. J. & Lea, D. W. in Use of Proxies in Paleoceanography: Examples from the South Atlantic (eds Fisher, G. & Wefer, G.) 489–512 (Springer, 1999).
Spero, H. J., Bijma, J., Lea, D. W. & Bemis, B. E. Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes. Nature 390, 497–500 (1997).
Marshall, B. J., Thunell, R., Hennehan, M., Astor, Y. & Wejnert, K. Planktonic foraminiferal area density as a proxy for carbonate ion concentration: a calibration study using the Cariaco Basin ocean time series. Paleoceanography 28, 363–376 (2013).
Osborne, E. B. et al. Calcification of the planktonic foraminifera Globigerina bulloides and carbonate ion concentration: results from the Santa Barbara Basin. Paleoceanography 31, 1083–1102 (2016).
Aldridge, D., Beer, C. J. & Purdie, D. A. Calcification in the planktonic foraminifera Globigerina bulloides linked to phosphate concentrations in surface waters of the North Atlantic Ocean. Biogeosciences 9, 1725–1739 (2012).
Beer, C. J., Schiebel, R. & Wilson, P. A. Testing planktic foraminiferal shell weight as a surface water [CO3 2-] proxy using plankton net samples. Geology 38, 103–106 (2010).
De Villiers, S. Optimum growth conditions as opposed to calcite saturation as a control on the calcification rate and shell-weight of marine foraminifera. Mar. Biol. 144, 45–49 (2004).
Dore, J. E., Lukas, R., Sadler, D. W., Church, M. J. & Karl, D. M. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proc. Natl Acad. Sci. USA 106, 12235–12240 (2009).
Fassbender, A. J. et al. Estimating total alkalinity in the Washington State Coastal Zone: complexities and surprising utility for ocean acidification research. Estuar. Coasts 40, 404–418 (2016).
Caldeira, K. & Wickett, M. E. Anthropogenic carbon and ocean pH. Nature 425, 365 (2003).
Byrne, R. H., Mecking, S., Feely, Ra. & Liu, X. Direct observations of basin-wide acidification of the North Pacific Ocean. Geophys. Res. Lett. 37, L02601 (2010).
Bates, N. et al. A time-series view of changing ocean chemistry due to ocean uptake of anthropogenic CO2 and ocean acidification. Oceanography 27, 126–141 (2014).
Gruber, N. et al. Spatiotemporal patterns of carbon-13 in the global surface oceans and the oceanic Suess effect. Glob. Biogeochem. Cycles 13, 307–335 (1999).
Keeling, C. D. The Suess effect: 13carbon-14carbon interrelations. Environ. Int. 2, 229–300 (1979).
Black, D., Thunell, R. C., Wejnert, K. & Astor, Y. Carbon isotope composition of Caribbean sea surface waters: response to the uptake of anthropogenic CO2. Geophys. Res. Lett. https://doi.org/10.1029/2011GL048538 (2011).
Sydeman, W. J. et al. Climate change and wind intensification in coastal upwelling ecosystems. Science 345, 77–80 (2014).
Di Lorenzo, E., Miller, A. J. & SchneiderNand McWilliams, J. C. The warming of the California Current System: dynamics and ecosystem implications. J. Phys. Oceanogr. 35, 336–362 (2005).
McGowan, J., Bograd, S., Lynn, R. J. & Miller, A. J. The biological response to the 1977 regime shift in the California Current. Deep Sea Res. Pt II 50, 2567–2582 (2003).
Roemmich, D. & McGowan, J. Climatic warming and the decline of zooplankton in the California Current. Science 267, 1324–1326 (1995).
Pak, D. K. & Kennett, J. P. A foraminiferal isotopic proxy for upper water mass stratification. J. Foram. Res. 32, 319–327 (2002).
Bringue, M., Pospelova, V. & Field, D. B. High resolution sedimentary record of dinoflagellate cysts reflects decadal variability and 20th century warming in the Santa Barbara Basin. Quat. Sci. Rev. 105, 86–101 (2014).
Sonnerup, R. E. & Quay, P. D. 13C constraints on ocean carbon cycle models. Glob. Biogeochem. Cycles 26, GB2014 (2012).
Hare, S. R. Low Frequency Climate Variability and Salmon Production. PhD thesis, Univ. Washington (1996).
Mantua, N. J. & Hare, S. R. The Pacific Decadal Oscillation. J. Oceanogr. 58, 35–44 (2002).
Nam, S., Kim, H.-J. & Send, U. Amplification of hypoxic and acidic events by La Niña conditions on the continental shelf off California. Geophys. Res. Lett. 120, 5387–5399 (2015).
Bemis, B. E., Spero, H. J. & Thunell, R. C. Using species-specific paleotemperature equations with foraminifera: a case study in the Southern California Bight. Mar. Micropaleo. 46, 405–430 (2002).
Darling, K. F. et al. Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405, 43–47 (2000).
Sautter, L. R. & Thunell, R. C. Seasonal variability in the δ18O and δ13C of planktonic foraminifera from an upwelling environment: sediment trap results from the San Pedro Basin, Southern California Bight. Paleoceanography 6, 307–334 (1991).
Marshall, B. J. et al. Morphometric and stable isotopic differentiation of Orbulina universa morphotypes from the Cariaco Basin, Venezuela. Mar. Micropaleo 120, 46–64 (2015).
Moore, W. S. Radium isotope measurements using germanium detectors. Nucl. Instrum. Methods Phys. Res. 223, 407–411 (1984).
Bruland, K. W. Pb-210 Geochronology in the Coastal Marine Environment. PhD thesis, Univ. California (1974).
Koide, M., Soutar, A. & Goldberg, E. D. Marine geochronology with 210Pb. Earth Planet. Sci. Lett. 14, 422–446 (1972).
Krishnaswami, S., Lai, D., Amin, S. & Soutar, A. Geochronological studies in Santa Barbara Basin: 55Fe as a unique tracer for particulate settling. Limnol. Oceanogr. 18, 763–770 (1973).
Carter, M. W. & Moghissi, A. A. Three decades of nuclear testing. Health Phys. 33, 55–71 (1977).
Ritchie, J. C. & McHenry, J. R. Application of radioactive fallout Cesium-137 for measuring soil erosion and sediment accumulations rates and patterns: a review. J. Environ. Qual. 19, 215–233 (1989).
Shchepetkin, A. F. & McWilliams, J. C. The regional oceanic modeling system (ROMS): a split-explicit, free-surface, topography-following-coordinate oceanic model. Ocean Model. 9, 347–404 (2005).
Gruber, N. et al. Eddy-resolving simulation of plankton ecosystem dynamics in the California Current System. Deep Sea Res. Pt I 53, 1483–1516 (2006).
Gruber, N. et al. Rapid progression of ocean acidification in the California Current System. Science 337, 220–223 (2012).
Hauri, C. et al. Spatiotemporal variability and long-term trends of ocean acidification in the California Current System. Biogeosciences 10, 193–216 (2013).
Dee, D. P. et al. The ERA-Interim reanalysis: configuration and performance of the data assimilation system.Q. J. R. Meteorol. Soc. 137, 553–597 (2011).
Graven, H. D., Gruber, N., Key, R., Khatiwala, S. & Giraud, X. Changing controls on oceanic radiocarbon: new insights on shallow-to-deep ocean exchange and anthropogenic CO2 uptake. J. Geophys. Res. https://doi.org/10.1029/2012JC008074 (2012).
Leinweber, A. & Gruber, N. Variability and trends of ocean acidification in the Southern California current system: a timeseries from Santa Monica Bay. J. Geophys. Res. 118, 3622–3633 (2013).
Lee, K., Kim, T.-W., Byrne, R. H. & Liu, Y.-M. The universal ratio of boron to chlorinity for the North Pacific and North Atlantic Oceans. Geochim. Cosmochim. Acta 74, 1801–1811 (2010).
Zeebe, R. E. & Wolf-Gladrow, D. A. (eds) in CO 2 in Seawater: Equilibrium, Kinetics, Isotopes Vol. 65, 346 (Elsevier, 2001).
We dedicate this manuscript to co-author Robert C. Thunell, a wonderful colleague, friend and mentor, who lost his battle to cancer on 30 July 2018. This research was supported in part by a National Science Foundation grant to R.C.T. (1631977) and the Johanna M. Resig Fellowship granted to E.B.O. by the Cushman Foundation. R.A.F. was supported by the NOAA Ocean Acidification Program (PMEL contribution number 4546). N.G. acknowledges the support of ETH Zürich and of the Swiss National Foundation through the XEBUS project. We thank D. Burdige from Old Dominion University for collecting the box core used in this study; E. Tappa for his assistance with IRMS analyses and sediment trap recovery and deployments in the SBB; and N. Umling, whose review and scientific discourse greatly improved this manuscript.
The authors declare no competing interests.
Peer review information Primary Handling Editor: James Super.
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B. G. bulloides shell with its final chamber broken showing a cross-sectional view of the shell wall, the key morphometric used in this study to estimate [CO32−]. Shell wall thickness is indirectly estimated by measuring area normalized shell weight (ANSW: shell weight (μg) / 2-D surface area (μm2).
The location of the box-core (red circle) used for the down-core reconstruction as well as the sediment trap (yellow triangle) and hydrographic sampling location (Plumes and Blooms Project Station 4; orange square) used in the calibration portion of the study29.
The increasing shell weight over the down core record coincides with a decline in δ18O (note inverted axis), which represents an increase in temperature. This comparison provides a visualization of the importance of using size-normalized shell weights to estimate changes in calcification and shell thickness. Results from this study show that while overall shell weight and shell size are increasing as a result of warming temperatures, shell thickness is declining as a result of reduced [CO32-].
Extended Data Fig. 4 The long-term shift in G. bulloides shell diameter increases in concert with warming sea surface temperatures.
B. We compare the relative changes that are recorded G. bulloides δ18O to a Northern Hemisphere Temperature anomaly for the 1900–2000 period and see a good agreement between temperature trends recorded in these records (Jones et al., 2013). C. We also compared G. bulloides δ18O to in situ sea surface temperature (SST) measurements made in the Santa Barbara Basin (SBB; 1955-Present; Shore Stations Program) and see an excellent agreements between sea surface temperature and the δ18O recorded in our G. bulloides shells.
Extended Data Fig. 5 Time-series correlations between Pacific Decadal Oscillation Index and the detrended proxy-[CO3=] and ANSW sample standard error.
Corresponding values were compared at 5-year time steps due to difference in time resolution across records. An independent t-test was conducted to compare both detrended proxy-[CO3=] and area-normalized shell weight standard area (a measure of sample variability) to the Pacific Decadal Oscillation Index. Highly significant correlation coefficients exist between PDO and the respective variables p<0.005) and the results of a paired t-tests for both records are highly significant (p<0.005), further confirming significance of the relationships.
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Osborne, E.B., Thunell, R.C., Gruber, N. et al. Decadal variability in twentieth-century ocean acidification in the California Current Ecosystem. Nat. Geosci. 13, 43–49 (2020). https://doi.org/10.1038/s41561-019-0499-z
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