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

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Volume 28, No. 2
Pages 62 - 73

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Geochemical Proxies for Estimating Faunal Exposure to Ocean Acidification

By Lisa A. Levin , Bärbel Hönisch , and Christina A. Frieder 
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Article Abstract

Growing concern over the impacts of modern ocean acidification (OA) and interest in historical pH excursions have intensified the development of geochemical proxies for organism exposure to acidification and other components of the carbonate system. The use of carbonate structures produced by foraminifers, coccolithophores, corals, mollusks, brachiopods, echinoderms, ostracods, and fish for paleoreconstructions is an active area of study, and the resulting proxy development offers new opportunities for studying modern faunal exposures. Here we review information from field studies and laboratory experiments on carbonate system geochemical proxies in protists and metazoa. Geochemical proxy development for foraminifers and corals is most advanced; studies of fish and echinoderms are in their infancy. The most promising geochemical proxies are those with a mechanistic link to changes in seawater carbonate chemistry, such as boron isotopes (δ11B), B/Ca, and U/Ca ratios recorded in skeletal hard parts. We also discuss indirect geochemical proxies (other trace elements and carbonate polymorphs) along with their potential uses and limitations due to modification by physiological processes, precipitation rate, and degree of calcification. Proxy measurements in modern skeletal structures, otoliths, statoliths, and other hard parts could reveal environmental exposures of organisms from larval through adult stages, and could advance inferences about effects of OA (and other stressors) on survival, growth, population connectivity, and other ecological attributes. Use of geochemical proxies in live, field-collected organisms is an underutilized and underdeveloped approach to studying OA consequences, but it may offer a powerful, complementary approach to laboratory observations.

Citation

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.

References

Adkins, J.F., E.A. Boyle, W.B. Curry, and A. Lutringer. 2003. Stable isotopes in deep-sea corals and a new mechanism for “vital effects.” Geochimica et Cosmochimica Acta 67:1,129–1,143, https://doi.org/10.1016/S0016-7037(02)01203-6.

Al-Horani, F.A., S.M. Al-Moghrabi, and D. De Beer. 2003. The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Marine Biology 142:419–426, https://doi.org/10.1007/s00227-002-0981-8.

Allen, K.A., and B. Hönisch. 2012. The planktic foraminiferal B/Ca proxy for seawater carbonate chemistry: A critical evaluation. Earth and Planetary Science Letters 345–348:203–211, https://doi.org/10.1016/j.epsl.2012.06.012.

Allen, K.A., B. Hönisch, S.M. Eggins, and Y. Rosenthal. 2012. Environmental controls on B/Ca in calcite tests of the tropical planktic foraminifer species Globigerinoides ruber and Globigerinoides sacculifer. Earth and Planetary Science Letters 351–352:270–280, https://doi.org/10.1016/j.epsl.2012.07.004.

Allen, K.A., B. Hönisch, S.M. Eggins, J.M. Yu, H.J. Spero, and H. Elderfield. 2011. Controls on boron incorporation in cultured tests of the planktic foraminifer Orbulina universa. Earth and Planetary Science Letters 309:291–301, https://doi.org/10.1016/j.epsl.2011.07.010.

Anagnostou, E., K.F. Huang, C.F. You, E.L. Sikes, and R.M. Sherrell. 2012. Evaluation of boron isotope ratio as a pH proxy in the deep sea coral Desmophyllum dianthus: Evidence of physiological pH adjustment. Earth and Planetary Science Letters 349–350:251–260, https://doi.org/10.1016/j.epsl.2012.07.006.

Andersson, A.J., F.T. Mackenzie, and N.R. Bates. 2008. Life on the margin: Implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Marine Ecology Progress Series 373:265–273, https://doi.org/10.3354/meps07639.

Arkhipkin, A.I. 2005. Statoliths as ‘black boxes’ (life recorders) in squid. Marine and Freshwater Research 56:573–583, https://doi.org/10.1071/MF04158.

Bentov, S., C. Brownlee, and J. Erez. 2009. The role of seawater endocytosis in the biomineralization process in calcareous foraminifera. Proceedings of the National Academy of Sciences of the United States of America 106:21,500–21,504, https://doi.org/10.1073/pnas.0906636106.

Blamart, D., C. Rollion-Bard, A. Meibom, J.P. Cuif, A. Juillet-Leclerc, and Y. Dauphin. 2007. Correlation of boron isotopic composition with ultrastructure in the deep-sea coral Lophelia pertusa: Implications for biomineralization and paleo-pH. Geochemistry, Geophysics, Geosystems 8, Q12001, https://doi.org/10.1029/2007GC001686.

Bockmon, E.E., C.A. Frieder, M.O. Navarro, L.A. White-Kershek, and A.G. Dickson. 2013. Technical note: Controlled experimental aquarium system for multi-stressor investigation of carbonate chemistry, oxygen saturation, and temperature. Biogeosciences 10:5,967–5,975, https://doi.org/10.5194/bg-10-5967-2013.

Bøggild, O. 1930. The shell structure of the mollusk. Det Kongelige Danske Videnskabernes Selskabs Skrifter, Natruvidenskabelig og Mathematisk, Afdeling, Ser 9:231–326.

Boiteau, R., M. Greaves, and H. Elderfield. 2012. Authigenic uranium in foraminiferal coatings: A proxy for ocean redox chemistry. Paleoceanography 27, PA3227, https://doi.org/10.1029/2012PA002335.

Borszcz, T., P. Kuklinski, and P.D. Taylor. 2013. Patterns of magnesium content in Arctic bryozoan skeletons along a depth gradient. Polar Biology 36:193–200, https://doi.org/10.1007/s00300-012-1250-z.

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, and others. 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.

Broecker, W.S. 1963. A preliminary evaluation of uranium series inequilibrium as a tool for absolute age measurements of marine carbonates. Journal of Geophysical Research 68:2,817–2,834, https://doi.org/10.1029/JZ068i009p02817.

Brown, R.E., L.D. Anderson, E. Thomas, and J.C. Zachos. 2011. A core-top calibration of B/Ca in the benthic foraminifers Nuttallides umbonifera and Oridorsalis umbonatus: A proxy for Cenozoic bottom water carbonate saturation. Earth and Planetary Science Letters 310:360–368, https://doi.org/10.1016/j.epsl.2011.08.023.

Byrne, M. 2011. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: Vulnerabilities and potential for persistence in a changing ocean. Oceanography and Marine Biology: An Annual Review 49:1–42, https://doi.org/10.1201/b11009-2.

Caldeira, K., and M.E. Wickett. 2003. Oceanography: Anthropogenic carbon and ocean pH. Nature 425:365–365, https://doi.org/10.1038/425365a.

Campana, S.E. 1999. Chemistry and composition of fish otoliths: Pathways, mechanisms and applications. Marine Ecology Progress Series 188:263–297, https://doi.org/10.3354/meps188263.

Campana, S.E., and S.R. Thorrold. 2001. Otoliths, increments, and elements: Keys to a comprehensive understanding of fish populations? Canadian Journal of Fisheries and Aquatic Sciences 58:30–38, https://doi.org/10.1139/f00-177.

Carpenter, S.J., and K.C. Lohmann. 1992. Sr/Mg ratios of modern marine calcite: Empirical indicators of ocean chemistry and precipitation rate. Geochimica et Cosmochimica Acta 56:1,837–1,849, https://doi.org/10.1016/0016-7037(92)90314-9.

Checkley, D.M., A.G. Dickson, M. Takahashi, J.A. Radich, N. Eisenkolb, and R. Asch. 2009. Elevated CO2 enhances otolith growth in young fish. Science 324:1,683–1,683, https://doi.org/10.1126/science.1169806.

de Nooijer, L.J., H.J. Spero, J. Erez, J. Bijma, and G.J. Reichart. 2014. Biomineralization in perforate foraminifera. Earth-Science Reviews 135:48–58, https://doi.org/10.1016/j.earscirev.2014.03.013.

Dickson, A.G. 1990. Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep Sea Research Part A 37:755–766, https://doi.org/10.1016/0198-0149(90)90004-F.

Dickson, J.A.D. 2002. Fossil echinoderms as monitor of the Mg/Ca ratio of Phanerozoic oceans. Science 298:1,222–1,224, https://doi.org/10.1126/science.1075882.

Dickson, J.A.D. 2004. Echinoderm skeletal preservation: Calcite-aragonite seas and the Mg/Ca ratio of Phanerozoic oceans. Journal of Sedimentary Research 74:355–365, https://doi.org/10.1306/112203740355.

Dissard, D., G. Nehrke, G.J. Reichart, J. Bijma. 2010. Impact of seawater pCO2 on calcification and Mg/Ca and Sr/Ca ratios in benthic foraminifera calcite: Results from culturing experiments with Ammonia tepida. Biogeosciences 7:81–93, https://doi.org/10.5194/bg-7-81-2010.

Djogic, R., L. Sipos, and M. Branica. 1986. Characterization of uranium (VI) in seawater. Limnology and Oceanography 31:1,122–1,131, https://doi.org/10.4319/lo.1986.31.5.1122.

Doney, S.C., V.J. Fabry, R.A. Feely, and J.A. Kleypas. 2009. Ocean acidification: The other CO2 problem. Annual Review of Marine Science 1:169–192, https://doi.org/10.1146/annurev.marine.010908.163834.

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.

Druffel, E. 1997. Geochemistry of corals: Proxies of past ocean chemistry, ocean circulation and climate. Proceedings of the National Academy of Sciences of the United States of America 94:8,354–8,361.

Ebert, T.A. 2007. Growth and survival of postsettlement sea urchins. Pp. 96–134 in Edible Sea Urchins: Biology and Ecology. J.M. Lawrence, ed., Elsevier Sciences.

Elderfield, H., C.J. Bertram, and J. Erez. 1996. Biomineralization model for the incorporation of trace elements into foraminiferal calcium carbonate. Earth and Planetary Science Letters 142:409–423, https://doi.org/10.1016/0012-821X(96)00105-7.

Elderfield, H., M. Greaves, S. Barker, I.R. Hall, A. Tripati, P. Ferretti, S. Crowhurst, L. Booth, and C. Daunt. 2010. A record of bottom water temperature and seawater δ18O for the Southern Ocean over the past 440 kyr based on Mg/Ca of benthic foraminiferal Uvigerina spp. Quaternary Science Reviews 29:160–169, https://doi.org/10.1016/j.quascirev.2009.07.013.

Emiliani, C. 1955. Pleistocene temperatures. Journal of Geology 63:538–578.

Felis, T., A. Suzuki, H. Kuhnert, M. Dima, G. Lohmann, and H. Kawahata. 2009. Subtropical coral reveals abrupt early-twentieth-century freshening in the western North Pacific Ocean. Geology 37:527–530, https://doi.org/10.1130/G25581A.1.

Fitzer, S.C., M. Cusack, V.R. Phoenix, and N.A. Kamenos. 2014. Ocean acidification reduces the crystallographic control in juvenile mussels shells. Journal of Structural Biology 188:39–45, https://doi.org/10.1016/j.jsb.2014.08.007.

Foster, G.L. 2008. Seawater pH, pCO2 and [CO32–] variations in the Caribbean Sea over the last 130 kyr: A boron isotope and B/Ca study of planktic foraminifera. Earth and Planetary Science Letters 271:254–266, https://doi.org/10.1016/j.epsl.2008.04.015.

Frieder, C.A., J.P. Gonzalez, and L.A. Levin. 2014. Uranium in larval shells as a barometer of molluscan ocean acidification exposure. Environmental Science and Technology 48(11):6,401-6,408, https://doi.org/10.1021/es500514j.

Frieder, C.A., S. Nam, T.R. Martz, and L.A. Levin. 2012. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9:1–14, https://doi.org/10.5194/bg-9-3917-2012.

Gaetani, G.A., A.L. Cohen, Z. Wang, and J. Crusius. 2011. Rayleigh-based, multi-element coral thermometry: A biomineralization approach to developing climate proxies. Geochimica et Cosmochimica Acta 75:1,920–1,932, https://doi.org/10.1016/j.gca.2011.01.010.

Gauldie, R.W. 1993. Polymorphic crystalline structure of fish otoliths. Journal of Morphology 218:1–28, https://doi.org/10.1002/jmor.1052180102.

Gorzalek, P., J. Stolarski, M. Mazur, and A. Meibom. 2013. Micro- to nanostructure and geochemistry of extant crinoidal echinoderm skeletons. Geobiology 11:29–43, https://doi.org/10.1111/gbi.12012.

Green, M.A., G.G. Waldbusser, S.L. Reilly, K. Emerson, and S. O’Donnella. 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.

Gussone, N., and H.L. Filipsson. 2010. Calcium isotope ratios in calcitic tests of benthic foraminifers. Earth and Planetary Science Letters 290:108–117, https://doi.org/10.1016/j.epsl.2009.12.010.

Gussone, N., A. Eisenhauer, A. Heuser, M. Dietzel, B. Bock, F. Böhm, H.J. Spero, D.W. Lea, J. Bijma, and T.F. Nägler. 2003. Model for kinetic effects on calcium isotope fractionation (δ44Ca) in inorganic aragonite and cultured planktonic foraminifera. Geochimica et Cosmochimica Acta 67:1,375–1,382, https://doi.org/10.1016/S0016-7037(02)01296-6.

Gussone, N., F. Böhm, A. Eisenhauer, M. Dietzel, A. Heuser, B. Teichert, J. Reitner, G. Wörheide, and W.-C. Dullo. 2005. Calcium isotope fractionation in calcite and aragonite. Geochimica et Cosmochimica Acta 69:4,485–4,494, https://doi.org/10.1016/j.gca.2005.06.003.

Gussone, N., G. Langer, S. Thoms, G. Nehrke, A. Eisenhauer, U. Riebesell, and G. Wefer. 2006. Cellular calcium pathways and isotope fractionation in Emiliana huxleyi. Geology 34:625–628, https://doi.org/10.1130/G22733.1.

Hahn, S., R. Rodolfo-Metalpa, E. Griesshaber, W.W. Schmahl, D. Buhl, J.M. Hall-Spencer, C. Baggini, K.T. Fehr, and A. Immenhauser. 2012. Marine bivalve shell geochemistry and ultrastructure from modern low pH environments: Environmental effect versus experimental bias. Biogeosciences 9:1,897–1,914, https://doi.org/10.5194/bg-9-1897-2012.

Haynert, K., J. Schönfeld, R., Schiebel, B. Wilson, and J. Thomsen. 2014. Response of benthic foraminifera to ocean acidification in their natural sediment environment: A long-term culturing experiment. Biogeosciences 11:1,581–1,597, https://doi.org/10.5194/bg-11-1581-2014.

Heinemann, A., J. Fietzke, F. Melzner, F. Bohm, and J. Thomsen. 2012. Conditions of Mytilus edulis extracellular body fluids and shell composition in a pH-treatment experiment: Acid-base status, trace elements and δ11B. Geochemistry, Geophysics, Geosystems 13, Q01005, https://doi.org/10.1029/2011GC003790.

Hemming, N.G., and G.N. Hanson. 1992. Boron isotopic composition and concentration in modern marine carbonates. Geochimica et Cosmochimica Acta 56:537–543, https://doi.org/10.1016/0016-7037(92)90151-8.

Hemming, N.G., R.J. Reeder, and G.N. Hanson. 1995. Mineral-fluid partitioning and isotopic fractionation of boron in synthetic calcium carbonate. Geochimica et Cosmochimica Acta 59:371–379, https://doi.org/10.1016/0016-7037(95)00288-B.

Henehan, M.J., J.W.B. Rae, G.L. Foster, J. Erez, K.C. Prentice, M. Kucera, H.C. Bostock, M.A. Martínez-Botí, J.A. Milton, P.A. Wilson, and others. 2013. Calibration of the boron isotope proxy in the planktonic foraminifera Globigerinoides ruber for use in palaeo-CO2 reconstruction. Earth and Planetary Science Letters 364:111–122, https://doi.org/10.1016/j.epsl.2012.12.029.

Hofmann, G.E., J.E. Smith, K.S. Johnson, U. Send, L.A. Levin, F. Micheli, A. Paytan, N.N. Price, B. Peterson, Y. Takeshita, and others. 2011. High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE 6(12):e28983, https://doi.org/10.1371/journal.pone.0028983.

Hönisch, B., K.A. Allen, A.D. Russell, S.M. Eggins, J. Bijma, H.J. Spero, D.W. Lea, and J. Yu. 2011. Planktic foraminifers as recorders of seawater Ba/Ca. Marine Micropaleontology 79:52–57, https://doi.org/10.1016/j.marmicro.2011.01.003.

Hönisch, B., T. Bickert, and N.G. Hemming. 2008. Modern and Pleistocene boron isotope composition of the benthic foraminifer Cibicidoides wuellerstorfi. Earth and Planetary Science Letters 272:309–318, https://doi.org/10.1016/j.epsl.2008.04.047.

Hönisch, B., J. Bijma, A.D. Russell, H.J. Spero, M.R. Palmer, R.E. Zeebe, and A. Eisenhauer. 2003. The influence of symbiont photosynthesis on the boron isotopic composition of foraminifera shells. Marine Micropaleontology 49:87–96, https://doi.org/10.1016/S0377-8398(03)00030-6.

Hönisch, B., and N.G. Hemming. 2004. Ground-truthing the boron isotope-paleo-pH proxy in planktonic foraminifera shells: Partial dissolution and shell size effects. Paleoceanography 19, https://doi.org/10.1029/2004PA001026.

Hönisch, B., N.G. Hemming, D. Archer, M. Siddall, and J.F. McManus. 2009. Atmospheric carbon dioxide concentration across the mid-Pleistocene transition. Science 324:1,551–1,554, https://doi.org/10.1126/science.1171477.

Hönisch, B., N. Hemming, A.G. Grottoli, A. Amat, G.N. Hanson, and J. Bijma. 2004. Assessing scleractinian corals as recorders for paleo-pH: Empirical calibration and vital effects. Geochimica et Cosmochimica Acta 68(18):3,675–3,685, https://doi.org/10.1016/j.gca.2004.03.002.

Houlbrèque, F., R. Rodolfo-Metalpa, R. Jeffree, F. Oberhänsli, J-L. Teyssié, F. Boisson, K. Al-Trabeen, and C. Ferrier-Pagès. 2012. Effects of increased pCO2 on zinc uptake and calcification in the tropical coral Stylophora pistillata. Coral Reefs 31:101–109, https://doi.org/10.1007/s00338-011-0819-2.

Inoue, M., R. Suwa, A. Suzuki, K. Sakai, and H. Kawahata. 2011. Effects of seawater pH on growth and skeletal U/Ca ratios of Acropora digitifera coral polyps. Geophysical Research Letters 38(12), https://doi.org/10.1029/2011GL047786.

Jørgensen, B.B., J. Erez, P. Revsbech, and Y. Cohen. 1985. Symbiotic photosynthesis in a planktonic foraminiferan, Globigerinoides sacculifer (Brady), studied with microelectrodes. Limnology and Oceanography 30:1,253–1,267, https://doi.org/10.4319/lo.1985.30.6.1253.

Kaufman, A., W.S. Broecker, T.L. Ku, and D.L. Thurber. 1971. The status of U-series methods of mollusk dating. Geochimica et Cosmochimica Acta 35:1,155–1,183, https://doi.org/10.1016/0016-7037(71)90031-7.

Keul, N., G. Langer, L.J. de Nooijer, G. Nehrke, G.-J. Reichart, and J. Bijma. 2013. Incorporation of uranium in benthic foraminiferal calcite reflects seawater carbonate ion concentration. Geochemistry, Geophysics, Geosystems 14:102–111, https://doi.org/10.1029/2012GC004330.

Klochko, K., A.J. Kaufman, W. Yao, R.H. Byrne, and J.A. Tossell. 2006. Experimental measurement of boron isotope fractionation in seawater. Earth and Planetary Science Letters 248:261–270, https://doi.org/10.1016/j.epsl.2006.05.034.

Köhler-Rink, S. and M. Kühl. 2000. Microsensor studies of photosynthesis and respiration in larger symbiotic foraminifera: Part I. The physico-chemical microenvironment of Marginopora vertebralis, Amphistegina lobifera and Amphisorus hemprichii. Marine Biology 137:473–486, https://doi.org/10.1007/s002270000335.

Krief, S., E.J. Hendy, M. Fine, R. Yam, A. Meibom, G.L. Foster, and A. Shemesh. 2010. Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochimica et Cosmochimica Acta 74:4,988–5,001, https://doi.org/10.1016/j.gca.2010.05.023.

Kroh, A., and J.H. Nebelsick. 2010. Echinoderms and Oligo-Miocene carbonate systems: Potential applications in sedimentology and environmental reconstruction. Pp. 201–228 in Carbonate Systems During the Oligocene-Miocene Climatic Transition. M. Mutti, W.E. Piller, and C. Betzier, eds, International Association of Sedimentologists, Special Publication 42, Wiley-Blackwell.

Lacoue-Labarthe, T., E. Reveaillac, F. Oberhänsli, J.L. Teyssié, R. Jeffree, and J.P. Gattuso. 2011. Effects of ocean acidification on trace element accumulation in the early-life stages of squid Loligo vulgaris. Aquatic Toxicology 105:166–176, https://doi.org/10.1016/j.aquatox.2011.05.021.

Lares, M.L., and K.J. Orians. 1997. Natural Cd and Pb variations in Mytilus californianus during the upwelling season. Science of the Total Environment 197:177–195, https://doi.org/10.1016/S0048-9697(96)05409-5.

LaVigne, M., T.M. Hill, E. Sanford, B. Gaylord, A.D. Russell, E.A. Lenz, J.D. Hosfelt, and M.K. Young. 2013. The elemental composition of purple sea urchin (Strongylocentrotus purpuratus) calcite and potential effects of pCO2 during early life stages. Biogeosciences 10:3,465–3,477, https://doi.org/10.5194/bg-10-3465-2013.

Lemarchand, D., G.J. Wasserburg, and D.A. Papanastassiou. 2004. Rate-controlled calcium isotope fractionation in synthetic calcite. Geochimica et Cosmochimica Acta 68:4,665–4,678, https://doi.org/10.1016/j.gca.2004.05.029.

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. 2015. 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.

Limburg, K.E., C. Olson, Y. Walther, D. Dale, C. Slomp, and H. Høie. 2011. Tracking Baltic hypoxia and cod migration over millennia with natural tags. Proceedings of the National Academy of Sciences of the United States of America 108:E177–E182, https://doi.org/10.1073/pnas.1100684108.

Limburg, K.E., B.D. Walther, Z. Lu, G. Jackman, J. Mohan, Y. Walther, A. Nissling, P.K. Weber, and A.K. Schmitt. 2015. In search of the dead zone: Use of otoliths for tracking fish exposure to hypoxia. Journal of Marine Systems 141:167–178, https://doi.org/10.1016/j.jmarsys.2014.02.014.

Lombardi, C., R. Rodolfo-Metalpa, S. Cocito, M.C. Gambi, and P.D. Taylor. 2010. Structural and geochemical alterations in the Mg calcite bryozoan Myriapora truncata under elevated seawater pCO2 simulating ocean acidification. Marine Ecology 32:211–221, https://doi.org/10.1111/j.1439-0485.2010.00426.x.

Lowenstein, T.K., B. Kendall, and A.D. Anbar. 2014. The geological history of seawater. Pp. 569–622 in Treatise on Geochemistry, 2nd ed. H. Holland and K. Turekian, eds, Elsevier, Amsterdam.

Ma, Y., B. Aichmayerb, O. Paris, P. Fratzl, A. Meibom, R.A. Metzler, Y. Politi, L. Addadi, P.U.P.A. Gilbert, and S. Weiner. 2009. The grinding tip of the sea urchin tooth exhibits exquisite control over calcite crystal orientation and Mg distribution. Proceedings of the National Academy of Sciences of the United States of America 106:6,048–6,053, https://doi.org/10.1073/pnas.0810300106.

Marchitto, T.M., W.B. Curry, and D.W. Oppo. 2000. Zinc concentrations in benthic foraminifera reflect seawater carbonate chemistry. Paleoceanography 15:299–306, https://doi.org/10.1029/1999PA000420.

Marchitto, T.M., J. Lynch-Stieglitz, and S.R. Hemming. 2005. Deep Pacific CaCO3 compensation and glacial-interglacial atmospheric CO2. Earth and Planetary Science Letters 231:317–336, https://doi.org/10.1016/j.epsl.2004.12.024.

Marchitto, T.M., D.W. Oppo, and W.B. Curry. 2002. Paired benthic foraminiferal Cd/Ca and Zn/Ca evidence for a greatly increased presence of Southern Ocean Water in the glacial North Atlantic. Paleoceanography 17:10.1–10.18, https://doi.org/10.1029/2000PA000598.

Martin, G.B., S.R. Thorrold, and C.M. Jones. 2004. Temperature and salinity effects on strontium incorporation in otoliths of larval spot (Leiostomus xanthurus). Canadian Journal of Fisheries and Aquatic Sciences 61:34–42, https://doi.org/10.1139/f03-143.

McClintock, J.B., M.O. Amsler, R.A. Angus, R.C. Challener, J.B. Schram, C.D. Amsler, C.L. Mah, J. Cuce, and B.J. Baker. 2011. The Mg-calcite composition of Antarctic echinoderms: Important implications for predicting the impacts of ocean acidification. The Journal of Geology 119:457–466.

McCulloch, M., J. Falter, J. Trotter, and P. Montagna. 2012a. Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Climate Change 2(8):623–627, https://doi.org/10.1038/nclimate1473.

McCulloch, M., J. Trotter, P. Montagna, J. Falter, R. Dunbar, A. Freiwald, G. Försterra, and others. 2012b. Resilience of cold-water scleractinian corals to ocean acidification: Boron isotopic systematics of pH and saturation state up-regulation. Geochimica et Cosmochimica Acta 87:21–34, https://doi.org/10.1016/j.gca.2012.03.027.

Min, R.G., L.R. Edwards, F.W. Taylor, J. Recy, C.D. Gallup, and W.J. Beck. 1995. Annual cycles of U/Ca in coral skeletons and U/Ca thermometry. Geochimica et Cosmochimica Acta 59(10):2,025–2,042, https://doi.org/10.1016/0016-7037(95)00124-7.

Morris, C.C. 1991. Statocyst fluid composition and its effects on calcium carbonate precipitation in the squid Alloteuthis subulata: Towards a model for biomineralization. Bulletin of Marine Science 49:379–388.

Munday, P.L., M. Gagliano, J.M. Donelson, D.L. Dixson, and S.R. Thorrold. 2011a. Ocean acidification does not affect the early life history development of a tropical marine fish. Marine Ecology Progress Series 423:211–221, https://doi.org/10.3354/meps08990.

Munday, P.L., V. Hermann, D.L. Dixson, and S.R. Thorrold. 2011b. Effect of ocean acidification on otolith development in larvae of a tropical marine fish. Biogeosciences 8:1,631–1,641, https://doi.org/10.5194/bg-8-1631-2011.

Nägler, T.F., A. Eisenhauer, A. Müller, C. Hemleben, and J. Kramers. 2000. The δ44Ca-temperature calibration on fossil and cultured Globigerinoides sacculifer: New tool for reconstruction of past sea surface temperatures. Geochemisty, Geophysics, Geosystems 1, 1052, https://doi.org/10.1029/2000GC000091.

Navarro, M.O., E.E. Bockmon, C.A. Frieder, J.G. Gonzalez, and L.A. Levin. 2014. Environmental pH, O2 and capsular effects on the geochemical composition of statoliths of embryonic squid Doryteuthis opalescens. Water 6:2,233–2,254, https://doi.org/10.3390/w6082233.

Ni, Y., G.L. Foster, T. Bailey, T. Elliott, D.N. Schmidt, P.N. Pearson, B. Haley, and C. Coath. 2007. A core top assessment of proxies for the ocean carbonate system in surface-dwelling foraminifers. Paleoceanography 22, PA3212, https://doi.org/10.1029/2006PA001337.

Nolf, D. 2013. The Diversity of Fish Otoliths, Past and Present. E. Steurbaut, ed., Royal Belgian Institute of Natural Sciences, 359 pp.

Pelejero, C., E. Calvo, M.T. McCulloch, J.F. Marshall, M.K. Gagan, J.M. Lough, and B.N. Opdyke. 2005. Preindustrial to modern interdecadal variability in coral reef pH. Science 309:2,204–2,207, https://doi.org/10.1126/science.1113692.

Penman, D.E., B. Hönisch, E.T. Rasbury, N.G. Hemming, and H.J. Spero. 2013. Boron, carbon, and oxygen isotopic composition of brachiopod shells: Intra-shell variability, controls, and potential as a paleo-pH recorder. Chemical Geology 340:32–39, https://doi.org/10.1016/j.chemgeo.2012.11.016.

Rae, J.W.B., G.L. Foster, D.N. Schmidt, and T. Elliott. 2011. Boron isotopes and B/Ca in benthic foraminifera: Proxies for the deep ocean carbonate system. Earth and Planetary Science Letters 302:403–413, https://doi.org/10.1016/j.epsl.2010.12.034.

Raitzsch, M., A. Duenas-Bohorquez, G.J. Reichart, L.J. de Nooijer, and T. Bickert. 2010. Incorporation of Mg and Sr in calcite of cultured benthic foraminifera: Impact of calcium concentration and associated calcite saturation state. Biogeosciences 7:869–881.

Raitzsch, M., E.C. Hathorne, H. Kuhnert, J. Groeneveld, and T. Bickert. 2011a. Modern and late Pleistocene B/Ca ratios of the benthic foraminifer Planulina wuellerstorfi determined with laser ablation ICP-MS. Geology 39:1,039–1,042, https://doi.org/10.1130/G32009.1.

Raitzsch, M., H. Kuhnert, E.C. Hathorne, J. Groeneveld, and T. Bickert. 2011b. U/Ca in benthic foraminifers: A proxy for the deep-sea carbonate saturation. Geochemistry, Geophysics, Geosystems 12, Q06019, https://doi.org/10.1029/2010GC003344.

Reynaud, S., N.G. Hemming, A. Juillet-Leclerc, and J.-P. Gattuso. 2004. Effect of pCO2 and temperature on the boron isotopic composition of a zooxanthellate coral: Acropora sp. Coral Reefs 23:539–546, https://doi.org/10.1007/s00338-004-0399-5.

Ries, J.B. 2004. The effect of ambient Mg/Ca on Mg fractionation in calcareous marine invertebrates: A record of Phanerozoic Mg/Ca in seawater. Geology 32:981–984, https://doi.org/10.1130/G20851.1.

Ries, J.B. 2006. Mg fractionation in crustose coralline algae: Geochemical, biological, and sedimentological implications of secular variation in the Mg/Ca ratio of seawater. Geochimica et Cosmochimica Acta 70:891–900, https://doi.org/10.1016/j.gca.2005.10.025.

Ries, J.B. 2011. Skeletal mineralogy in a high-CO2 world. Journal of Experimental Marine Biology and Ecology 403:54–64, https://doi.org/10.1016/j.jembe.2011.04.006.

Rink, S., M. Kühl, J. Bijma, and H.J. Spero. 1998. Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa. Marine Biology 131:583–595, https://doi.org/10.1007/s002270050350.

Rollion-Bard, C., and J. Erez. 2010. Intra-shell boron isotope ratios in the symbiont-bearing benthic foraminiferan Amphistegina lobifera: Implications for δ11B vital effects and paleo-pH reconstructions. Geochimica et Cosmochimica Acta 74:1,530–1,536, https://doi.org/10.1016/j.gca.2009.11.017.

Rosenthal, Y., C.H. Lear, D.W. Oppo, and B.K. Linsley. 2006. Temperature and carbonate ion effects on Mg/Ca and Sr/Ca ratios in benthic foraminifera: Aragonitic species Hoeglundina elegans. Paleoceanography 21, PA1007, https://doi.org/10.1029/2005PA001158.

Russell, A.D., S. Emerson, A.C. Mix, and L.C. Peterson. 1996. The use of foraminiferal uranium/calcium ratios as an indicator of changes in seawater uranium content. Paleoceanography 11:649–663, https://doi.org/10.1029/96PA02058.

Russell, A.D., S. Emerson, B.K. Nelson, J. Erez, and D.W. Lea. 1994. Uranium in foraminiferal calcite as a recorder of seawater uranium concentrations. Geochimica et Cosmochimica Acta 58:671–681, https://doi.org/10.1016/0016-7037(94)90497-9.

Russell, A.D., B. Hönisch, H.J. Spero, and D.W. Lea. 2004. Effects of changes in seawater carbonate ion concentration and temperature on shell U/Ca, Mg/Ca, and Sr/Ca of planktonic foraminifera. Geochimica et Cosmochimica Acta 68:4,347–4,361, https://doi.org/10.1016/j.gca.2004.03.013.

Sanyal, A., J. Bijma, H.J. Spero, and D.W. Lea. 2001. Empirical relationship between pH and the boron isotopic composition of G. sacculifer: Implications for the boron isotope paleo-pH proxy. Paleoceanography 16:515–519, https://doi.org/10.1029/2000PA000547.

Sanyal, A., N.G. Hemming, W.S. Broecker, D.W. Lea, H.J. Spero, and G.N. Hanson. 1996. Oceanic pH control on the boron isotopic composition of foraminifera: Evidence from culture experiments. Paleoceanography 11:513–517, https://doi.org/10.1029/96PA01858.

Sanyal, A., M. Nugent, R.J. Reeder, and J. Bijma. 2000. Seawater pH control on the boron isotopic composition of calcite: Evidence from inorganic calcite precipitation experiments. Geochimica et Cosmochimica Acta 64:1,551–1,555, https://doi.org/10.1016/S0016-7037(99)00437-8.

Segovia-Zavala, J.A., F. Delgadillo-Hinojosa, and S. Alvarez-Borrego. 1998. Cadmium in the coastal upwelling area adjacent to the California–Mexico border. Estuarine and Coastal and Shelf Science 46:475–481, https://doi.org/10.1006/ecss.1997.0296.

Shen, G.T., and R.B. Dunbar. 1995. Environmental controls on uranium in reef corals. Geochimica et Cosmochimica Acta 59:2,009–2,024, https://doi.org/10.1016/0016-7037(95)00123-9.

Spero, H., S.M. Eggins, A.D. Russell, L. Vetter, M.R. Kilburn, and B. Hönisch. 2015. Timing and mechanism for intratest Mg/Ca variability in a living planktic foraminifer. Earth and Planetary Science Letters 409:32–42, https://doi.org/10.1016/j.epsl.2014.10.030.

Stanley, S.M. 2006. Influence of seawater chemistry on biomineralization throughout Phanerozoic time: Paleontological and experimental evidence. Palaeogeography, Palaeoclimatology, Palaeoecology 232(2):214–236, https://doi.org/10.1016/j.palaeo.2005.12.010.

Takahashi, T., S.C. Sutherland, D.W. Chipman, J.G. Goddard, C. Ho, T. Newberger, C. Sweeney, and D.R. Munro. 2014. Climatological distributions of pH, pCO2, total CO2, alkalinity, and CaCO3 saturation in the global surface ocean, and temporal changes at selected locations. Marine Chemistry 164:95–125, https://doi.org/10.1016/j.marchem.2014.06.004.

Thorrold, S., D. Zacherl, and L.A. Levin. 2007. Population connectivity and larval dispersal: Using geochemical signatures in calcified structures. Oceanography 20(3):80–89, https://doi.org/10.5670/oceanog.2007.31.

Trotter, J., P. Montagna, M. McCulloch, S. Silenzi, S. Reynaud, G. Mortimer, S. Martin, C. Ferrier-Pagès, J.-P. Gattuso, and R. Rodolfo-Metalpa. 2011. Quantifying the pH ‘vital effect’ in the temperate zooxanthellate coral Cladocora caespitosa: Validation of the boron seawater pH proxy. Earth and Planetary Science Letters 303:163–173, https://doi.org/10.1016/j.epsl.2011.01.030.

Venn, A.A., E. Tambutté, M. Holcomb, D. Allemand, and S. Tambutté. 2011. Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6(5):e20013, https://doi.org/10.1371/journal.pone.0020013.

Venn, A.A., E. Tambutté, M. Holcomb, J. Laurent, D. Allemand, and S. Tambutté. 2013. Impact of seawater acidification on pH at the tissue–skeleton interface and calcification in reef corals. Proceedings of the National Academy of Sciences of the United States of America 110:1,634–1,639, https://doi.org/10.1073/pnas.1216153110.

Waldbusser, G.G., E.L. Brunner, B.A. Haley, B. Hales, C.J. Langdon, and F.G. Prahl. 2013. A developmental and energetic basis linking larval oyster shell formation to acidification sensitivity. Geophysical Research Letters 40:2,171–2,176, https://doi.org/10.1002/grl.50449.

Wei, G., M. Sun, X. Li, and B. Nie. 2000. Mg/Ca, Sr/Ca and U/Ca ratios of a Porites coral from Sanya Bay, Hainan Island, South China Sea and their relationships to sea surface temperature. Palaeogeography, Palaeoclimatology, Palaeoecology 162:59–74, https://doi.org/10.1016/S0031-0182(00)00105-X.

Weiner, S., and P.M. Dove. 2003. An overview of biomineralization processes and the problem of the vital effect. Reviews in Mineralogy and Geochemistry 54:1–29, https://doi.org/10.2113/0540001.

Yu, J., and H. Elderfield. 2007. Benthic foraminiferal B/Ca ratios reflect deep water carbonate saturation state. Earth and Planetary Science Letters 258:73–86, https://doi.org/10.1016/j.epsl.2007.03.025.

Yu, J., H. Elderfield, and B. Hönisch. 2007. B/Ca in planktonic foraminifera as a proxy for surface seawater pH. Paleoceanography 22, PA2202, https://doi.org/10.1029/2006PA001347.

Yu, J.M., H. Elderfield, Z.D. Jin, and L. Booth. 2008. A strong temperature effect on U/Ca in planktonic foraminiferal carbonates. Geochimica et Cosmochimica Acta 72:4,988–5,000, https://doi.org/10.1016/j.gca.2008.07.011.

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