{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T10:06:52Z","timestamp":1791281212177,"version":"4.1.0"},"reference-count":60,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,2,22]],"date-time":"2016-02-22T00:00:00Z","timestamp":1456099200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,2,22]],"date-time":"2016-02-22T00:00:00Z","timestamp":1456099200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Ocean acidification (OA) is expected to indirectly impact biota living in contaminated coastal environments by altering the bioavailability and potentially toxicity of many pH-sensitive metals. Here, we show that OA (pH 7.71; <jats:italic>p<\/jats:italic>CO<jats:sub>2<\/jats:sub> 1480\u2009\u03bcatm) significantly increases the toxicity responses to a global coastal contaminant (copper ~0.1\u2009\u03bcM) in two keystone benthic species; mussels (<jats:italic>Mytilus edulis<\/jats:italic>) and purple sea urchins (<jats:italic>Paracentrotus lividus<\/jats:italic>). Mussels showed an extracellular acidosis in response to OA and copper individually which was enhanced during combined exposure. In contrast, urchins maintained extracellular fluid pH under OA by accumulating bicarbonate but exhibited a slight alkalosis in response to copper either alone or with OA. Importantly, copper-induced damage to DNA and lipids was significantly greater under OA compared to control conditions (pH 8.14; <jats:italic>p<\/jats:italic>CO<jats:sub>2<\/jats:sub> 470\u2009\u03bcatm) for both species. However, this increase in DNA-damage was four times lower in urchins than mussels, suggesting that internal acid-base regulation in urchins may substantially moderate the magnitude of this OA-induced copper toxicity effect. Thus, changes in metal toxicity under OA may not purely be driven by metal speciation in seawater and may be far more diverse than either single-stressor or single-species studies indicate. This has important implications for future environmental management strategies.<\/jats:p>","DOI":"10.1038\/srep21554","type":"journal-article","created":{"date-parts":[[2016,2,22]],"date-time":"2016-02-22T10:15:06Z","timestamp":1456136106000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":95,"title":["Ocean acidification increases copper toxicity differentially in two key marine invertebrates with distinct acid-base responses"],"prefix":"10.1038","volume":"6","author":[{"given":"Ceri","family":"Lewis","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert P.","family":"Ellis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily","family":"Vernon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katie","family":"Elliot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sam","family":"Newbatt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rod W.","family":"Wilson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,2,22]]},"reference":[{"key":"BFsrep21554_CR1","doi-asserted-by":"publisher","first-page":"948","DOI":"10.1126\/science.1149345","volume":"319","author":"BS Halpern","year":"2008","unstructured":"Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948\u2013952, 10.1126\/science.1149345 (2008).","journal-title":"Science"},{"key":"BFsrep21554_CR2","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1126\/science.aac4722","volume":"349","author":"JP Gattuso","year":"2015","unstructured":"Gattuso, J. P. et al. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349, 45\u201355 (2015).","journal-title":"Science"},{"key":"BFsrep21554_CR3","doi-asserted-by":"publisher","first-page":"6225","DOI":"10.5194\/bg-10-6225-2013","volume":"10","author":"L Bopp","year":"2013","unstructured":"Bopp, L. et al. Multiple stressors of ocean ecosytems in the 21st Century: projections with CMIP5 models. Biogeosci. 10, 6225\u20136245 (2013).","journal-title":"Biogeosci."},{"key":"BFsrep21554_CR4","unstructured":"IPCC. Climate Change 2013: The Physical Science Basis. Working Group I Contribution to the IPCC 5th Assessment Report\u2013Changes to the Underlying Scientific\/Technical Assessment. (2013)."},{"key":"BFsrep21554_CR5","doi-asserted-by":"publisher","first-page":"414","DOI":"10.1093\/icesjms\/fsn048","volume":"65","author":"VJ Fabry","year":"2008","unstructured":"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\u2013432, 10.1093\/icesjms\/fsn048 (2008).","journal-title":"ICES J. Mar. Sci."},{"key":"BFsrep21554_CR6","doi-asserted-by":"publisher","first-page":"1884","DOI":"10.1111\/gcb.12179","volume":"19","author":"KJ Kroeker","year":"2013","unstructured":"Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Chan. Biol. 19, 1884\u20131896, 10.1111\/gcb.12179 (2013).","journal-title":"Glob. Chan. Biol."},{"key":"BFsrep21554_CR7","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1038\/nature04095","volume":"437","author":"JC Orr","year":"2005","unstructured":"Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681\u2013686, 10.1038\/nature04095 (2005).","journal-title":"Nature"},{"key":"BFsrep21554_CR8","doi-asserted-by":"crossref","unstructured":"Fabricius, K. E., De\u2019ath, G., Noonan, S. & Uthicke, S. Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc. R. Soc. B-Biol. Sci. 281, 10.1098\/rspb.2013.2479 (2014).","DOI":"10.1098\/rspb.2013.2479"},{"key":"BFsrep21554_CR9","doi-asserted-by":"publisher","first-page":"203","DOI":"10.3354\/meps07768","volume":"373","author":"H-O P\u00f6rtner","year":"2008","unstructured":"P\u00f6rtner, H.-O. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist\u2019s view. Mar. Ecol. Prog. Ser. 373, 203\u2013217, 10.3354\/meps07768 (2008).","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"BFsrep21554_CR10","doi-asserted-by":"publisher","first-page":"995","DOI":"10.1038\/nclimate1982","volume":"3","author":"AC Wittmann","year":"2013","unstructured":"Wittmann, A. C. & P\u00f6rtner, H.-O. Sensitivities of extant animal taxa to ocean acidification. Nat. Clim. Chan. 3, 995\u20131001, 10.1038\/nclimate1982 (2013).","journal-title":"Nat. Clim. Chan."},{"key":"BFsrep21554_CR11","doi-asserted-by":"publisher","first-page":"1304","DOI":"10.1111\/j.1461-0248.2008.01253.x","volume":"11","author":"CM Crain","year":"2008","unstructured":"Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Let 11, 1304\u20131315, 10.1111\/j.1461-0248.2008.01253.x (2008).","journal-title":"Ecol. Let"},{"key":"BFsrep21554_CR12","doi-asserted-by":"publisher","first-page":"582","DOI":"10.1093\/icb\/ict049","volume":"53","author":"M Byrne","year":"2013","unstructured":"Byrne, M. & Przeslawski, R. Multistressor impacts of warming and acidification of the ocean on marine invertebrates\u2019 life histories. Integr. Comp. Biol. 53, 582\u2013596, 10.1093\/icb\/ict049 (2013).","journal-title":"Integr. Comp. Biol."},{"key":"BFsrep21554_CR13","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.jembe.2014.04.005","volume":"457","author":"JB Schram","year":"2014","unstructured":"Schram, J. B., Schoenrock, K. M., McClintock, J. B., Amsler, C. D. & Angus, R. A. Multiple stressor effects of near-future elevated seawater temperature and decreased pH on righting and escape behaviors of two common Antarctic gastropods. Journal of Exp. Mar. Biol. Ecol. 457, 90\u201396, 10.1016\/j.jembe.2014.04.005 (2014).","journal-title":"Journal of Exp. Mar. Biol. Ecol."},{"key":"BFsrep21554_CR14","doi-asserted-by":"publisher","first-page":"2122","DOI":"10.1111\/gcb.12833","volume":"21","author":"R Przeslawski","year":"2015","unstructured":"Przeslawski, R., Byrne, M. & Mellin, C. A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob. Chan. Biol. 21, 2122\u20132140, 10.1111\/gcb.12833 (2015).","journal-title":"Glob. Chan. Biol."},{"key":"BFsrep21554_CR15","doi-asserted-by":"publisher","first-page":"72","DOI":"10.5670\/oceanog.2009.98","volume":"22","author":"FJ Millero","year":"2009","unstructured":"Millero, F. J., Woosley, R., Ditrolio, B. & Waters, J. Effect of ocean acidification on the speciation of metals in seawater. Oceanogr. 22, 72\u201385 (2009).","journal-title":"Oceanogr."},{"key":"BFsrep21554_CR16","doi-asserted-by":"publisher","first-page":"191","DOI":"10.3354\/meps10082","volume":"470","author":"LJ Hoffmann","year":"2012","unstructured":"Hoffmann, L. J., Breitbarth, E., Boyd, P. W. & Hunter, K. A. Influence of ocean warming and acidification on trace metal biogeochemistry. Mar. Ecol. Prog. Ser. 470, 191\u2013205, 10.3354\/meps10082 (2012).","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"BFsrep21554_CR17","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.aquatox.2013.05.019","volume":"140","author":"AV Ivanina","year":"2013","unstructured":"Ivanina, A. V. et al. Short-term acute hypercapnia affects cellular responses to trace metals in the hard clams Mercenaria mercenaria. Aquat. Tox. 140, 123\u2013133, 10.1016\/j.aquatox.2013.05.019 (2013).","journal-title":"Aquat. Tox."},{"key":"BFsrep21554_CR18","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/0269-7491(92)90099-v","volume":"76","author":"GW Bryan","year":"1992","unstructured":"Bryan, G. W. & Langston, W. J. Bioavailability, accumulation and effects of heavy-metals in sediments with special reference to United-Kingdom estuaries-A review. Environ. Poll. 76, 89\u2013131, 10.1016\/0269-7491(92)90099-v (1992).","journal-title":"Environ. Poll."},{"key":"BFsrep21554_CR19","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1016\/j.marlpolbul.2006.10.013","volume":"54","author":"K Schiff","year":"2007","unstructured":"Schiff, K., Brown, J., Diehl, D. & Greenstein, D. Extent and magnitude of copper contamination in marinas of the San Diego region, California, USA. Mar. Poll. Bull. 54, 322\u2013328, 10.1016\/j.marlpolbul.2006.10.013 (2007).","journal-title":"Mar. Poll. Bull."},{"key":"BFsrep21554_CR20","doi-asserted-by":"publisher","first-page":"1127","DOI":"10.1016\/j.marpolbul.2007.04.021","volume":"54","author":"B Jones","year":"2007","unstructured":"Jones, B. & Bolam, T. Copper speciation survey from UK marinas, harbours and estuaries. Mar. Poll. Bull. 54, 1127\u20131138, 10.1016\/j.marpolbul.2007.04.021 (2007).","journal-title":"Mar. Poll. Bull."},{"key":"BFsrep21554_CR21","first-page":"112","volume":"2","author":"GW Bryan","year":"1983","unstructured":"Bryan, G. W. & Gibbs, P. E. Heavy metals in the Fal estuary, Cornwall: A study of long term contamination by mining waste and its effects on estuarine organisms. Occ. Pub. Mar. Biol. Assoc. 2, 112 (1983).","journal-title":"Occ. Pub. Mar. Biol. Assoc."},{"key":"BFsrep21554_CR22","doi-asserted-by":"publisher","first-page":"2201","DOI":"10.1016\/j.marpolbul.2010.08.018","volume":"60","author":"P-Y Pascal","year":"2010","unstructured":"Pascal, P.-Y., Fleeger, J. W., Galvez, F. & Carman, K. R. The toxicological interaction between ocean acidity and metals in coastal meiobenthic copepods. Mar. Poll. Bull. 60, 2201\u20132208, 10.1016\/j.marpolbul.2010.08.018 (2010).","journal-title":"Mar. Poll. Bull."},{"key":"BFsrep21554_CR23","doi-asserted-by":"publisher","first-page":"3559","DOI":"10.1016\/j.ecolmodel.2011.08.017","volume":"222","author":"R Richards","year":"2011","unstructured":"Richards, R., Chaloupka, M., Sano, M. & Tomlinson, R. Modelling the effects of \u2018coastal\u2019 acidification on copper speciation. Ecol. Mod. 222, 3559\u20133567, 10.1016\/j.ecolmodel.2011.08.017 (2011).","journal-title":"Ecol. Mod."},{"key":"BFsrep21554_CR24","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.jembe.2011.11.025","volume":"413","author":"T Lacoue-Labarthe","year":"2012","unstructured":"Lacoue-Labarthe, T. et al. Temperature and pCO2 effect on the bioaccumulation of radionuclides and trace elements in the eggs of the common cuttlefish, Sepia officinalis. J. Exp. Mar. Biol. Ecol. 413, 45\u201349, 10.1016\/j.jembe.2011.11.025 (2012).","journal-title":"Sepia officinalis. J. Exp. Mar. Biol. Ecol."},{"key":"BFsrep21554_CR25","doi-asserted-by":"publisher","first-page":"2561","DOI":"10.5194\/bg-6-2561-2009","volume":"6","author":"T Lacoue-Labarthe","year":"2009","unstructured":"Lacoue-Labarthe, T. et al. Effects of increased pCO2 and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosci. 6, 2561\u20132573 (2009).","journal-title":"Biogeosci."},{"key":"BFsrep21554_CR26","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1016\/j.aquatox.2011.05.021","volume":"105","author":"T Lacoue-Labarthe","year":"2011","unstructured":"Lacoue-Labarthe, T. et al. Effects of ocean acidification on trace element accumulation in the early-life stages of squid Loligo vulgaris. Aquat. Tox. 105, 166\u2013176, 10.1016\/j.aquatox.2011.05.021 (2011).","journal-title":"Aquat. Tox."},{"key":"BFsrep21554_CR27","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.aquatox.2014.01.027","volume":"149","author":"S Goetze","year":"2014","unstructured":"Goetze, S., Matoo, O. B., Beniash, E., Saborowski, R. & Sokolova, I. M. Interactive effects of CO2 and trace metals on the proteasome activity and cellular stress response of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Aquat. Tox. 149, 65\u201382, 10.1016\/j.aquatox.2014.01.027 (2014).","journal-title":"Aquat. Tox."},{"key":"BFsrep21554_CR28","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1016\/0891-5849(94)00159-h","volume":"18","author":"SJ Stohs","year":"1995","unstructured":"Stohs, S. J. & Bagchi, D. Oxidative mechanisms in the toxicity of metal-ions. Free Rad. Biol. Med. 18, 321\u2013336, 10.1016\/0891-5849(94)00159-h (1995).","journal-title":"Free Rad. Biol. Med."},{"key":"BFsrep21554_CR29","first-page":"950","volume":"12","author":"A Parveen","year":"2010","unstructured":"Parveen, A. & Javed, M. Effect of Water-borne copper on the growth performance of fish Catla catla. Int. J. Agricult. Biol. 12, 950\u2013952 (2010).","journal-title":"Int. J. Agricult. Biol."},{"key":"BFsrep21554_CR30","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1007\/s003600050181","volume":"168","author":"T Wang","year":"1998","unstructured":"Wang, T. et al. Copper exposure impairs intra- and extracellular acid-base regulation during hypercapnia in the fresh water rainbow trout (Oncorhynchus mykiss). J. Comp. Phys. B-Biochem. Syst. Environ. Physiol. 168, 591\u2013599, 10.1007\/s003600050181 (1998).","journal-title":"J. Comp. Phys. B-Biochem. Syst. Environ. Physiol."},{"key":"BFsrep21554_CR31","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/j.jembe.2008.07.024","volume":"366","author":"S Widdicombe","year":"2008","unstructured":"Widdicombe, S. & Spicer, J. I. Predicting the impact of ocean acidification on benthic biodiversity: What can animal physiology tell us? J. Exp. Mar. Biol. Ecol. 366, 187\u2013197, 10.1016\/j.jembe.2008.07.024 (2008).","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"BFsrep21554_CR32","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/j.cbpa.2013.06.002","volume":"166","author":"M Collard","year":"2013","unstructured":"Collard, M. et al. Buffer capacity of the coelomic fluid in echinoderms. Comp. Biochem. Physiol. Part A, Molec. Integ. Physiol. 166, 199\u2013206, 10.1016\/j.cbpa.2013.06.002 (2013).","journal-title":"Comp. Biochem. Physiol. Part A, Molec. Integ. Physiol."},{"key":"BFsrep21554_CR33","doi-asserted-by":"publisher","first-page":"2207","DOI":"10.1007\/s00227-013-2219\u20133","volume":"160","author":"F Gazeau","year":"2013","unstructured":"Gazeau, F. et al. Impacts of ocean acidification on marine shelled molluscs. Mar. Biol. 160, 2207\u20132245, 10.1007\/s00227-013-2219\u20133 (2013).","journal-title":"Mar. Biol."},{"key":"BFsrep21554_CR34","doi-asserted-by":"publisher","first-page":"219","DOI":"10.3354\/meps07775","volume":"373","author":"GE Hofmann","year":"2008","unstructured":"Hofmann, G. E., O\u2019Donnell, M. J. & Todgham, A. E. Using functional genomics to explore the effects of ocean acidification on calcifying marine organisms. Mar. Ecol. Prog. Ser. 373, 219\u2013225 (2008).","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"BFsrep21554_CR35","doi-asserted-by":"publisher","first-page":"2313","DOI":"10.5194\/bg-6-2313-2009","volume":"6","author":"F Melzner","year":"2009","unstructured":"Melzner, F. et al. Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosci. 6, 2313\u20132331 (2009).","journal-title":"Biogeosci."},{"key":"BFsrep21554_CR36","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/0022-0981(90)90069-o","volume":"143","author":"RN Bamber","year":"1990","unstructured":"Bamber, R. N. The effects of acidic seawater on three species of lamellibranch mollusc. J. Exp. Mar. Biol. Ecol. 143, 181\u2013191, 10.1016\/0022-0981(90)90069-o (1990).","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"BFsrep21554_CR37","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1007\/s10646-006-0083-3","volume":"15","author":"MA Fdil","year":"2006","unstructured":"Fdil, M. A. et al. Valve movement response of the mussel Mytilus galloprovincialis to metals (Cu, Hg, Cd and Zn) and phosphate industry effluents from Moroccan Atlantic coast. Ecotox. 15, 477\u2013486, 10.1007\/s10646-006-0083-3 (2006).","journal-title":"Ecotox."},{"key":"BFsrep21554_CR38","unstructured":"Farmanfarmaian, A. In Physiology of Echinodermata (ed R. A. Boolootian ) (Interscience Publishers, 1966)."},{"key":"BFsrep21554_CR39","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.jembe.2011.07.003","volume":"407","author":"JI Spicer","year":"2011","unstructured":"Spicer, J. I., Widdicombe, S., Needham, H. R. & Berge, J. A. Impact of CO2-acidified seawater on the extracellular acid-base balance of the northern sea urchin Strongylocentrotus droebachiensis. J. Exp. Mar. Biol. Ecol. 407, 19\u201325, 10.1016\/j.jembe.2011.07.003 (2011).","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"BFsrep21554_CR40","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1007\/bf00349148","volume":"124","author":"JI Spicer","year":"1995","unstructured":"Spicer, J. I. Oxygen and acid-base status of the sea urchin Psammechinus miliaris during environmental hypoxia. Mar. Biol. 124, 71\u201376, 10.1007\/bf00349148 (1995).","journal-title":"Mar. Biol."},{"key":"BFsrep21554_CR41","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1007\/bf00428659","volume":"93","author":"LH Bookbinder","year":"1986","unstructured":"Bookbinder, L. H. & Shick, J. M. Anaerobic and aerobic energy-metabolism in ovaries of the sea-urchin Strongylocentrotus droebachiensis. Mar. Biol. 93, 103\u2013110, 10.1007\/bf00428659 (1986).","journal-title":"Mar. Biol."},{"key":"BFsrep21554_CR42","doi-asserted-by":"publisher","first-page":"2344","DOI":"10.1007\/s11356-012-0743-1","volume":"19","author":"AI Catarino","year":"2012","unstructured":"Catarino, A. I., Bauwens, M. & Dubois, P. Acid-base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures. Environ. Sci. Poll. Res. 19, 2344\u20132353, 10.1007\/s11356-012-0743-1 (2012).","journal-title":"Environ. Sci. Poll. Res."},{"key":"BFsrep21554_CR43","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1016\/j.aquatox.2005.05.016","volume":"74","author":"GK Bielmyer","year":"2005","unstructured":"Bielmyer, G. K., Brix, K. V., Capo, T. R. & Grosell, M. The effects of metals on embryo-larval and adult life stages of the sea urchin, Diadema antillarum. Aquat. Tox. 74, 254\u2013263, 10.1016\/j.aquatox.2005.05.016 (2005).","journal-title":"Aquat. Tox."},{"key":"BFsrep21554_CR44","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/0742-8413(90)90123-q","volume":"95","author":"F Boitel","year":"1990","unstructured":"Boitel, F. & Truchot, J. P. Comparative-study of the effects of copper on hemolymph ion concentrations and acid-base-balance in shore crabs Carcinus maenas acclimated to full-strength or dilute seawater. Comp. Biochem. Phys. C-Pharmacol. Tox. Endocrin. 95, 307\u2013312, 10.1016\/0742-8413(90)90123-q (1990).","journal-title":"Comp. Biochem. Phys. C-Pharmacol. Tox. Endocrin."},{"key":"BFsrep21554_CR45","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1007\/bf00356288","volume":"112","author":"JI Spicer","year":"1992","unstructured":"Spicer, J. I. & Weber, R. E. Respiratory impairment by water-borne copper and zinc in the edible crab Cancer-pagurus (l) (Crustacea, Decapoda) during hypoxic exposure. Mar. Biol. 112, 429\u2013435, 10.1007\/bf00356288 (1992).","journal-title":"Mar. Biol."},{"key":"BFsrep21554_CR46","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1016\/j.marpolbul.2011.04.023","volume":"63","author":"J-S Rhee","year":"2011","unstructured":"Rhee, J.-S. et al. Expression of superoxide dismutase (SOD) genes from the copper-exposed polychaete, Neanthes succinea. Mar. Poll. Bull. 63, 277\u2013286, 10.1016\/j.marpolbul.2011.04.023 (2011).","journal-title":"Mar. Poll. Bull."},{"key":"BFsrep21554_CR47","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/s0022-0981(02)00306-4","volume":"277","author":"L Geracitano","year":"2002","unstructured":"Geracitano, L., Monserrat, J. M. & Bianchini, A. Physiological and antioxidant enzyme responses to acute and chronic exposure of Laeonereis acuta (Polychaeta, Nereididae) to copper. J. Exp. Mar. Biol. Ecol. 277, 145\u2013156, 10.1016\/s0022-0981(02)00306-4 (2002).","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"BFsrep21554_CR48","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1016\/j.cbpc.2006.08.005","volume":"144","author":"G Jing","year":"2006","unstructured":"Jing, G., Li, Y., Xie, L. P. & Zhang, R. Q. Metal accumulation and enzyme activities in gills and digestive gland of pearl oyster (Pinctada fucata) exposed to copper. Comp. Biochem. Phys. C-Tox. Pharmacol. 144, 184\u2013190, 10.1016\/j.cbpc.2006.08.005 (2006).","journal-title":"Comp. Biochem. Phys. C-Tox. Pharmacol."},{"key":"BFsrep21554_CR49","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.cbpc.2011.02.004","volume":"154","author":"VL Maria","year":"2011","unstructured":"Maria, V. L. & Bebianno, M. J. Antioxidant and lipid peroxidation responses in Mytilus galloprovincialis exposed to mixtures of benzo(a)pyrene and copper. Comp. Biochem. Phys. C-Tox. Pharmacol. 154, 56\u201363, 10.1016\/j.cbpc.2011.02.004 (2011).","journal-title":"Comp. Biochem. Phys. C-Tox. Pharmacol."},{"key":"BFsrep21554_CR50","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1007\/bf00228784","volume":"44","author":"CA Flemming","year":"1989","unstructured":"Flemming, C. A. & Trevors, J. T. Copper toxicity and chemistry in the environment-a review. Wat. Air Soil Poll. 44, 143\u2013158, 10.1007\/bf00228784 (1989).","journal-title":"Wat. Air Soil Poll."},{"key":"BFsrep21554_CR51","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1007\/s002270050099","volume":"128","author":"BK Larsen","year":"1997","unstructured":"Larsen, B. K., Portner, H. O. & Jensen, F. B. Extra- and intracellular acid-base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Mar. Biol. 128, 337\u2013346, 10.1007\/s002270050099 (1997).","journal-title":"Mar. Biol."},{"key":"BFsrep21554_CR52","doi-asserted-by":"crossref","unstructured":"Stiff, M. J. Copper\/bicarbonate equilibria in solutions of bicarbonate ion at concentrations similar to those found in natural water. Water Res. 5, 171-&, 10.1016\/0043-1354(71)90049-2 (1971).","DOI":"10.1016\/0043-1354(71)90049-2"},{"key":"BFsrep21554_CR53","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1111\/gcb.12048","volume":"19","author":"DA Roberts","year":"2013","unstructured":"Roberts, D. A. et al. Ocean acidification increases the toxicity of contaminated sediments. Glob. Chan. Biol. 19, 340\u2013351, 10.1111\/gcb.12048 (2013).","journal-title":"Glob. Chan. Biol."},{"key":"BFsrep21554_CR54","doi-asserted-by":"crossref","unstructured":"Campbell, A. L., Mangan, S., Ellis, R. P. & Lewis, C. Ocean acidification increases copper toxicity to the early life history stages of the polychaete Arenicola marina in artificial seawater. Environ. Sci. Technol. (2014).","DOI":"10.1021\/es502739m"},{"key":"BFsrep21554_CR55","doi-asserted-by":"publisher","first-page":"2089","DOI":"10.1007\/s00227-012-2081-8","volume":"160","author":"C Lewis","year":"2013","unstructured":"Lewis, C., Clemow, K. & Holt, W. V. Metal contamination increases the sensitivity of larvae but not gametes to ocean acidification in the polychaete Pomatoceros lamarckii (Quatrefages). Mar. Biol. 160, 2089\u20132101 (2013).","journal-title":"Mar. Biol."},{"key":"BFsrep21554_CR56","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1007\/s10584-011-0156-z","volume":"109","author":"M Meinshausen","year":"2011","unstructured":"Meinshausen, M. et al. The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Clim. Change 109, 213\u2013241, 10.1007\/s10584-011-0156-z (2011).","journal-title":"Clim. Change"},{"key":"BFsrep21554_CR57","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1242\/jeb.64.1.45","volume":"64","author":"JP Truchot","year":"1976","unstructured":"Truchot, J. P. Carbon dioxide combining properties of blood of shore crab Carcinus maenas-l-carbon dioxide solubility coefficient and carbonic acid dissociation constants. J. Exp. Biol. 64, 45\u201357 (1976).","journal-title":"J. Exp. Biol."},{"key":"BFsrep21554_CR58","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/j.aquatox.2004.06.003","volume":"69","author":"HE Parry","year":"2004","unstructured":"Parry, H. E. & Pipe, R. K. Interactive effects of temperature and copper on immunocompetence and disease susceptibility in mussels (Mytilus edulis). Aquat. Tox. 69, 311\u2013325, 10.1016\/j.aquatox.2004.06.003 (2004).","journal-title":"Aquat. Tox."},{"key":"BFsrep21554_CR59","unstructured":"Camejo, G., Wallin, B. & Enoj\u00e4rvi, M. InFree radical and antioxidant protocols. Methods in molecular biology Vol. 108 (ed Amstrong D. ) 377\u2013387 (Humana, 1999)."},{"key":"BFsrep21554_CR60","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.mrgentox.2008.05.008","volume":"654","author":"C Lewis","year":"2008","unstructured":"Lewis, C. & Galloway, T. Genotoxic damage in polychaetes: A study of species and cell-type sensitivities. Mutat. Res.-Gen. Tox. Environ. Mutagen. 654, 69\u201375, 10.1016\/j.mrgentox.2008.05.008 (2008).","journal-title":"Mutat. Res.-Gen. Tox. Environ. Mutagen."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep21554","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep21554.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep21554.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,4]],"date-time":"2023-01-04T13:59:29Z","timestamp":1672840769000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep21554"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,2,22]]},"references-count":60,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,8,26]]}},"alternative-id":["BFsrep21554"],"URL":"https:\/\/doi.org\/10.1038\/srep21554","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,2,22]]},"assertion":[{"value":"15 September 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 January 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 February 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"21554"}}