Effects of high pCO2 on early life development of pelagic spawning marine fish
Ana M. Faria A E , Soraia Filipe B , Ana F. Lopes A , Ana P. Oliveira C , Emanuel J. Gonçalves A and Laura Ribeiro DA Marine and Environmental Sciences Centre (MARE), ISPA – Instituto Universitário, Rua Jardim do Tabaco, 34, PT-1149-041 Lisboa, Portugal.
B Superior School of Tourism and Sea Technology, Santuário de Nossa Senhora dos Remédios, PT-2520-641 Peniche, Portugal.
C Instituto Português do Mar e da Atmosfera (IPMA, IP), Division of Oceanography and Environmental Bioprospecting, Avenida Brasília, 6, PT-1200 Lisboa, Portugal.
D Instituto Português do Mar e da Atmosfera (IPMA, IP), Aquaculture Research Station, Avenida 5 de Outubro, PT-8700-305 Olhão, Portugal.
E Corresponding author. Email address: afaria@ispa.pt
Marine and Freshwater Research 68(11) 2106-2114 https://doi.org/10.1071/MF16385
Submitted: 17 August 2016 Accepted: 21 March 2017 Published: 2 June 2017
Abstract
The present study investigated the effect of elevated pCO2 on the development of early stages of the pelagic spawning marine fish Solea senegalensis, Diplodus sargus and Argyrosomus regius. Eggs and larvae were reared under control (pH 8.0, ~570 μatm) and two elevated pCO2 conditions (pH 7.8, ~1100 μatm; pH 7.6, ~1900 μatm) until mouth opening (3 days post-hatching). Egg size did not change with exposure to elevated pCO2, but hatching rate was significantly reduced under high pCO2 for all three species. Survival rate was not affected by exposure to increased pCO2, but growth rate was differently affected across species, with A. regius growing faster in the mid-level pCO2 treatment compared with control conditions. S. senegalensis and A. regius hatched with smaller yolk sacs under increased pCO2 but endogenous reserves of D. sargus were not affected. Otoliths were consistently larger under elevated pCO2 conditions for all the three species. Differences among egg batches and a significant interaction between batch and pCO2 suggest that other factors, such as egg quality, can influence the response to increased pCO2. Overall, the results support the occurrence of a species-specific response to pCO2, but highlight the need for cautious analysis of potential sensitivity of species from unreplicated observations.
Additional keywords: carbon dioxide, growth rate, hatching rate, larval development, otoliths, survival rate.
References
Barazi-Yeroulanos, L. (2010). Synthesis of Mediterranean marine finfish aquaculture – a marketing and promotion strategy. Studies and Reviews, General Fisheries Commission for the Mediterranean, number 88, FAO, Rome, Italy.Baumann, H., Talmage, S. C., and Gobler, C. J. (2012). Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nature Climate Change 2, 38–41.
| Reduced early life growth and survival in a fish in direct response to increased carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Gjs7vE&md5=3b86ce2a946a97744790d4e1ed0f86f4CAS |
Bignami, S., Susponaugle, S., and Cowen, R. K. (2013). Response to ocean acidification in larvae of large tropical marine fish, Rachycentron canadum. Global Change Biology 19, 996–1006.
| Response to ocean acidification in larvae of large tropical marine fish, Rachycentron canadum.Crossref | GoogleScholarGoogle Scholar |
Bignami, S., Sponaugle, S., and Cowen, R. K. (2014). Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus. Aquatic Biology 21, 249–260.
| Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus.Crossref | GoogleScholarGoogle Scholar |
Borges, A. V., and Gypens, N. (2010). Carbonate chemistry in the coastal zone responds more strongly to eutrophication than to ocean acidification. Limnology and Oceanography 55, 346–353.
| Carbonate chemistry in the coastal zone responds more strongly to eutrophication than to ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVSgurg%3D&md5=22fac8c9151861033b3100b0a76e12d7CAS |
Brauner, C. J., and Baker, D. W. (2009). Patterns of acid–base regulation during exposure to hypercarbia in fishes. In ‘Cardio-Respiratory Control in Vertebrates: Comparative and Evolutionary Aspects’. (Eds M. Glass and S. C. Wood.) pp. 43–63. (Springer: Berlin, Germany.)
Cabeçadas, L., and Oliveira, A. P. (2005). Impact of a Coccolithus braarudii bloom on the carbonate system of Portuguese coastal waters. Journal of Nannoplankton Research 27, 141–147.
Cai, W. J., Hu, X., Huang, W. J., Murrell, M. C., Lehrter, J. C., Lohrenz, S. E., Chou, W. C., Zhai, W., Hollibaugh, J. T., Wang, Y., Zhao, P., Guo, X., Gundersen, K., Dai, M., and Gong, G. C. (2011). Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience 4, 766–770.
| Acidification of subsurface coastal waters enhanced by eutrophication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGks7bK&md5=8eb225de644d86f1a667c1a896e0017bCAS |
Caldeira, K., and Wickett, M. E. (2003). Oceanography: anthropogenic carbon and ocean pH. Nature 425, 365.
| Oceanography: anthropogenic carbon and ocean pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2ktrs%3D&md5=a8b1637cd17d0e707c43d3c5cfcad0d3CAS |
Chambers, R. C., Candelmo, A. C., Habeck, E. A., Poach, M. E., Wieczorek, D., Cooper, K. R., Greenfiel, C. E., and Phelan, B. A. (2014). Effects of elevated CO2 in the early life stages of summer flounder, Paralichthys dentatus, and potential consequences of ocean acidification. Biogeosciences 11, 1613–1626.
| Effects of elevated CO2 in the early life stages of summer flounder, Paralichthys dentatus, and potential consequences of ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtlWqu7o%3D&md5=46993d90f3976cf62ca80b6407b9bf44CAS |
Checkley, D. M., Dickson, A. G., Takahashi, M., Radich, J. A., Eisenkolb, N., and Asch, R. (2009). Elevated CO2 enhances otolith growth in young fish. Science 324, 1683.
| Elevated CO2 enhances otolith growth in young fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsFOmsL0%3D&md5=96c5b0dfd733a3844757fbdbf8d52d2dCAS |
Devine, B. M., Munday, P. L., and Jones, G. P. (2012). Rising CO2 concentrations affect settlement behaviour of larval damselfishes. Coral Reefs 31, 229–238.
| Rising CO2 concentrations affect settlement behaviour of larval damselfishes.Crossref | GoogleScholarGoogle Scholar |
Domenici, P., Allan, B., McCormick, M. I., and Munday, P. L. (2012). Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biology Letters 8, 78–81.
| Elevated carbon dioxide affects behavioural lateralization in a coral reef fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFygtbw%3D&md5=2e52f2e4e2c0e5b2746a7cd12a62cbddCAS |
Doney, S. C., Fabry, V. J., Feely, R. A., and Kleypas, J. A. (2009). Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1, 169–192.
| Ocean acidification: the other CO2 problem.Crossref | GoogleScholarGoogle Scholar |
Dupont, S., Ortega-Martinez, O., and Thorndyke, M. (2010). Impact of near-future ocean acidification on echinoderms. Ecotoxicology (London, England) 19, 449–462.
| Impact of near-future ocean acidification on echinoderms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtVGjsbk%3D&md5=4b6a6c08ac00d0295cd89d95e14d87d7CAS |
Dupont, S., Dorey, N., Stumpp, M., Melzner, F., and Thorndyke, M. (2013). Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Marine Biology 160, 1835–1843.
| Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Gnsr7J&md5=930cf56d094282a1ad2db39ee268cb47CAS |
Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D., and Hales, B. (2008). Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf. Science 320, 1490–1492.
| Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVWru7s%3D&md5=ea5584288225ed9b6fbe3a9b6c01fcfdCAS |
Franke, A., and Clemmesen, C. (2011). Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.). Biogeosciences Discussions 8, 7097–7126.
| Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.).Crossref | GoogleScholarGoogle Scholar |
Frommel, A. Y., Maneja, R., Lowe, D., Malzahn, A. M., Geffen, A. J., Folkvord, A., Piatkowski, U., Reusch, T. B. H., and Clemmesen, C. (2011). Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nature Climate Change 2, 42–46.
| Severe tissue damage in Atlantic cod larvae under increasing ocean acidification.Crossref | GoogleScholarGoogle Scholar |
Frommel, A. Y., Schubert, A., Piatkowski, U., and Clemesen, C. (2013). Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification. Marine Biology 160, 1825–1834.
| Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Ggs7jE&md5=e87422e65c21db7218d651130a142dd0CAS |
Frommel, A. Y., Maneja, R., Lowe, D., Pascoe, C. K., Geffen, A. J., Folkvord, A., Piatkowski, U., and Clemmesen, C. (2014). Organ damage in Atlantic herring larvae as a result of ocean acidification. Ecological Applications 24, 1131–1143.
| Organ damage in Atlantic herring larvae as a result of ocean acidification.Crossref | GoogleScholarGoogle Scholar |
Garrido, S., Bem-Hamadou, R., Santos, A. M., Ferreira, S., Teodósio, A., Cotano, U., Irigoien, X., Peck, M., Sainz, E., and Ré, P. (2015). Born small, die young: intrinsic, size-selective mortality in marine larval fish. Scientific Reports 5, 17065.
| Born small, die young: intrinsic, size-selective mortality in marine larval fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFentr3M&md5=0a633a21842b779c4dc041426cbc2863CAS |
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfied, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., Knowlton, N., Eakin, C. M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R. H., Dubi, A., and Hatziolos, M. E. (2007). Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742.
| Coral reefs under rapid climate change and ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWhu7fN&md5=e385201e8c5c8a978fc57ce26f0c6b33CAS |
Houde, E. D. (1987). Fish early life dynamics and recruitment variability. American Fisheries Society Symposium 2, 17–29.
Houde, E. D. (2002). Mortality. In ‘Fishery Science – The Unique Contributions of Early Life Stages’. (Eds L. A. Fuiman and R. G. Werner.) pp. 64–87. (Blackwell Science Ltd: Oxford, UK.)
Hurlbert, S. H. (1984). Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54, 187–211.
| Pseudoreplication and the design of ecological field experiments.Crossref | GoogleScholarGoogle Scholar |
Hurst, T. P., Fernandez, E. R., and Mathis, J. T. (2013). Effects of ocean acidification on hatch size and larval growth of walleye pollock (Theragra chalcogramma). ICES Journal of Marine Science 70, 812–822.
| Effects of ocean acidification on hatch size and larval growth of walleye pollock (Theragra chalcogramma).Crossref | GoogleScholarGoogle Scholar |
Hurst, T. P., Laurel, B. J., Mathis, J. T., and Tobosa, L. R. (2015). Effects of elevated CO2 levels on eggs and larvae of a North Pacific flatfish. ICES Journal of Marine Science 70, 1–6.
Ishimatsu, A., Kikkawa, T., Hayashi, M., Lee, K., and Kita, J. (2004). Effects of CO2 on marine fish: larvae and adults. Journal of Oceanography 60, 731–741.
| Effects of CO2 on marine fish: larvae and adults.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntVSjsLk%3D&md5=9eacbc15aeee78861cc1b857d5e4314eCAS |
Jutfelt, F., and Hedgärde, M. (2013). Atlantic cod actively avoid CO2 and predator odour, even after long-term CO2 exposure. Frontiers in Zoology 10, 81.
| Atlantic cod actively avoid CO2 and predator odour, even after long-term CO2 exposure.Crossref | GoogleScholarGoogle Scholar |
Jutfelt, F., and Hedgärde, M. (2015). Juvenile Atlantic cod behavior appears robust to near-future CO2 levels. Frontiers in Zoology 12, 11.
| Juvenile Atlantic cod behavior appears robust to near-future CO2 levels.Crossref | GoogleScholarGoogle Scholar |
Kikkawa, T., Ishimatsu, A., and Kita, J. (2003). Acute CO2 tolerance during the early development stages of four marine teleosts. Environmental Toxicology 18, 375–382.
| Acute CO2 tolerance during the early development stages of four marine teleosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCmtrk%3D&md5=6eb56a4a570ee79db6092321ad1ab868CAS |
Kroeker, K. J., Kordas, R. L., Crim, R. N., and Singh, G. G. (2010). Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13, 1419–1434.
| Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms.Crossref | GoogleScholarGoogle Scholar |
Lachkar, Z. (2014). Effects of upwelling increase on ocean acidification in the California and Canary current systems. Geophysical Research Letters 41, 90–95.
| Effects of upwelling increase on ocean acidification in the California and Canary current systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivFOnsrc%3D&md5=8cc0e47d9dbc2a096455e95e45dfd76fCAS |
Lahnsteiner, F., Soares, F., Ribeiro, L., and Dinis, M. T. (2008). Egg quality determination in teleost fish. In ‘Methods in Reproductive Aquaculture: Marine and Freshwater Species’. (Eds E. Cabrita, V. Robles, and P. Herraez.) pp. 149–181. (CRC Press: Boca Raton, FL, USA.)
Leggett, W. C., and DeBlois, E. (1994). Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages? Netherlands Journal of Sea Research 32, 119–134.
| Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages?Crossref | GoogleScholarGoogle Scholar |
Lüthi, D., Le Floch, M., Bereiter, B., Blunier, T., Barnola, J. M., Siegenthaler, U., Raynaud, D., Jouzel, J., Fischer, H., Kawamura, K., and Stocker, T. F. (2008). High-resolution carbon dioxide concentration record 650,000–800,000 years before present. Nature 453, 379–382.
| High-resolution carbon dioxide concentration record 650,000–800,000 years before present.Crossref | GoogleScholarGoogle Scholar |
Maneja, R. H., Frommel, A. Y., Browman, H. I., Clemmesen, C., Geffen, A. J., Folkvord, A., Piatkowski, U., Durif, C. M. F., Bjelland, R., and Skifesvik, A. B. (2013). The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2. Marine Biology 160, 1963–1972.
| The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1GgtbzI&md5=399e1f3abe9b2ca1e8668d6d17cdad7fCAS |
Maneja, R. H., Frommel, A. Y., Browman, H. I., Geffen, A. J., Folkvord, A., Piatkowski, U., Durif, C. M. F., Bjelland, R., Skifesvik, A. B., and Clemmesen, C. (2015). The swimming kinematics and foraging behavior of larval Atlantic herring (Clupea harengus L.) are unaffected by elevated pCO2. Journal of Experimental Marine Biology and Ecology 466, 42–48.
| The swimming kinematics and foraging behavior of larval Atlantic herring (Clupea harengus L.) are unaffected by elevated pCO2.Crossref | GoogleScholarGoogle Scholar |
Melzner, F., Gutowska, M. A., Langenbuch, M., Dupont, S., Lucassen, M., Thorndyke, M. C., Bleich, M., and Pörtner, H. O. (2009). Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6, 2313–2331.
| Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltVCqsA%3D%3D&md5=bfee150f388366da8cc8fa7d901306a0CAS |
Millar, R. B., and Anderson, M. J. (2004). Remedies for pseudoreplication. Fisheries Research 70, 397–407.
| Remedies for pseudoreplication.Crossref | GoogleScholarGoogle Scholar |
Millero, F. J., Graham, T. B., Huang, F., Bustos-Serrano, H., and Pierrot, D. (2006). Dissociation constants of carbonic acid in seawater as a function of salinity and temperature. Marine Chemistry 100, 80–94.
| Dissociation constants of carbonic acid in seawater as a function of salinity and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsFegsLk%3D&md5=dda3a27b25d4448e74f0d75b1133242fCAS |
Munday, P. L., Jones, G. P., Pratchett, M. S., and Williams, A. J. (2008). Climate change and the future for coral reef fishes. Fish and Fisheries 9, 261–285.
| Climate change and the future for coral reef fishes.Crossref | GoogleScholarGoogle Scholar |
Munday, P. L., Donelson, J. M., Dixson, D. L., and Endo, G. G. K. (2009). Effects of ocean acidification on the early life history of a tropical marine fish. Proceedings of the Royal Society of London – B. Biological Sciences 276, 3275–3283.
| Effects of ocean acidification on the early life history of a tropical marine fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFCgsLrJ&md5=ada4b0cde89dbbb59cc0af0231f7c633CAS |
Munday, P. L., Gagliano, M., Donelson, J. M., Dixson, D. L., and Thorrold, S. R. (2011a). Ocean acidification does not affect the early life history development of a tropical marine fish. Marine Ecology Progress Series 423, 211–221.
| Ocean acidification does not affect the early life history development of a tropical marine fish.Crossref | GoogleScholarGoogle Scholar |
Munday, P. L., Hernaman, V., Dixson, D. L., and Thorrold, S. R. (2011b). Effect of ocean acidification on otolith development in larvae of a tropical marine fish. Biogeosciences 8, 1631–1641.
| Effect of ocean acidification on otolith development in larvae of a tropical marine fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12rt7fM&md5=b896c29e28c469e90ad7d6cae8cb7c5aCAS |
Munday, P. L., Watson, S. A., Parsons, D. M., King, A., Barr, N. G., Mcleod, I. M., Allan, B. J. M., and Pether, S. M. J. (2016). Effects of elevated CO2 on early life history development of the yellowtail kingfish, Seriola lalandi, a large pelagic fish. ICES Journal of Marine Science 73, 641–649.
| Effects of elevated CO2 on early life history development of the yellowtail kingfish, Seriola lalandi, a large pelagic fish.Crossref | GoogleScholarGoogle Scholar |
Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R. M., Lindsay, K., Maier.Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R. G., Plattner, G. K., Rodgers, K. B., Sabine, C. L., Sarmiento, J. L., Schlitzer, R., Slater, R. D., Totterdell, I. J., Weirig, M. F., Yamanaka, Y., and Yool, A. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686.
| Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCjsL%2FE&md5=acebf1d12ada8d856d419b3578ed8f7dCAS |
Pimentel, M. S., Faleiro, F., Dionísio, G., Repolho, T., Pousão-Ferreira, P., Machado, J., and Rosa, R. (2014). Defective skeletogenesis and oversized otoliths on fish early stages in a changing ocean. The Journal of Experimental Biology 217, 2062–2070.
| Defective skeletogenesis and oversized otoliths on fish early stages in a changing ocean.Crossref | GoogleScholarGoogle Scholar |
Pimentel, M. S., Faleiro, F., Diniz, M., Machado, J., Pousão-Ferreira, P., Peck, M. A., Pörtner, H. O., and Rosa, R. (2015). Oxidative stress and digestive enzyme activity of flatfish larvae in a changing ocean. PLoS One 10, e0134082.
| Oxidative stress and digestive enzyme activity of flatfish larvae in a changing ocean.Crossref | GoogleScholarGoogle Scholar |
Pörtner, H. O., Langenbuch, M., and Reipschläger, A. (2004). Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. Journal of Oceanography 60, 705–718.
| Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history.Crossref | GoogleScholarGoogle Scholar |
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, S. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012). Fiji: an open-source platform for biological-image analysis Nature Methods 9, 676–682.
| Fiji: an open-source platform for biological-image analysisCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKnurbJ&md5=0433cc6d81a3f7e9e05a6d394cd4c0b2CAS |
Stiasny, M. H., Mittermayer, F. H., Sswat, M., Voss, R., Jutfelt, F., Chierici, M., Puvanendran, V., Mortensen, A., Reusch, T. B. H., and Clemmesen, C. (2016). Ocean acidification effects on Atlantic cod larval survival and recruitment to the fished population. PLoS One 11, e0155448.
| Ocean acidification effects on Atlantic cod larval survival and recruitment to the fished population.Crossref | GoogleScholarGoogle Scholar |
Stocker, T. F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S. K., Boschung, J., Nauels, A., Xia, Y., Bex, V., and Midgley, P. M. (Eds) (2013). ‘Climate Change (2013): the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.’ (Cambridge University Press: Cambridge, UK, and New York, NY, USA.)
Takagi, Y. (2002). Otolith formation and endolymph chemistry: a strong correlation between the aragonite saturation state and pH in the endolymph of the trout otolith organ. Marine Ecology Progress Series 231, 237–245.
| Otolith formation and endolymph chemistry: a strong correlation between the aragonite saturation state and pH in the endolymph of the trout otolith organ.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeiurs%3D&md5=fb242b9f80c1b0264f6357fb5c91c35fCAS |
Underwood, A. J. (1981). Techniques of analysis of variance in experimental marine biology and ecology. Oceanography and Marine Biology – an Annual Review 19, 513–605.
Weiss, R. F. (1974). Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Marine Chemistry 2, 203–215.
| Carbon dioxide in water and seawater: the solubility of a non-ideal gas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXmsV2rsA%3D%3D&md5=d553cb538b8f44c39103588d2aa5411dCAS |
Wittmann, A. C., and Pörtner, H. O. (2013). Sensitivities of extant animal taxa to ocean acidification. Nature Climate Change 3, 995–1001.
| Sensitivities of extant animal taxa to ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVShtr%2FL&md5=f3ed986fb943a8252427177e954fe7caCAS |