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Ocean acidification impacts growth and shell mineralization in juvenile abalone (Haliotis tuberculata)

Abstract

Ocean acidification (OA) is a major global driver that leads to substantial changes in seawater carbonate chemistry, with potentially serious consequences for calcifying organisms. Marine shelled molluscs are ecologically and economically important species, providing essential ecosystem services and food sources for other species. Due to their physiological characteristics and their use of calcium carbonate (CaCO3) to build their shells, molluscs are among the most vulnerable invertebrates with regard to OA, with early developmental stages being particularly sensitive to pH changes. This study investigated the effects of CO2-induced OA on juveniles of the European abalone Haliotis tuberculata, a commercially important gastropod species. Six-month-old juvenile abalones were cultured for 3 months at four pH levels (8.1, 7.8, 7.7, 7.6) representing current and predicted near-future conditions. Survival, growth, shell microstructure, thickness, and strength were compared across the four pH treatments. After 3 months of exposure, significant reductions in juvenile shell length, weight, and strength were revealed in the pH 7.6 treatment. Scanning electron microscopy observations also revealed modified texture and porosity of the shell mineral layers as well as alterations of the periostracum at pH 7.6 which was the only treatment with an aragonite saturation state below 1. It is concluded that low pH induces both general effects on growth mechanisms and corrosion of deposited shell in H. tuberculata. This will impact both the ecological role of this species and the costs of its aquaculture.

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References

  • Auzoux-Bordenave S, Badou A, Gaume B, Berland S, Helléouet M-N, Milet C, Huchette S (2010) Ultrastructure, chemistry and mineralogy of the growing shell of the European abalone Haliotis tuberculata. J Struct Biol 171:277–290. https://doi.org/10.1016/j.jsb.2010.05.012

    CAS  Article  PubMed  Google Scholar 

  • Auzoux-Bordenave S, Brahmi C, Badou A, De Rafélis M, Huchette S (2015) Shell growth, microstructure and composition over the development cycle of the European abalone Haliotis tuberculata. Mar Biol 162:687–697. https://doi.org/10.1007/s00227-015-2615-y

    Article  Google Scholar 

  • Beniash E, Ivanina A, Lieb NS, Kurochkin I, Sokolova IM (2010) Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Mar Ecol Prog Ser 419:95–108. https://doi.org/10.3354/meps08841

    CAS  Article  Google Scholar 

  • Byrne M, Ho M, Wong E, Soars NA, Selvakumaraswamy P, Shepard-Brennand H, Dworjanyn SA, Davis AR (2011) Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proc R Soc B Biol Sci 278:2376–2383. https://doi.org/10.1098/rspb.2010.2404

    Article  Google Scholar 

  • Cook PA (2014) The worldwide abalone industry. Mod Econ 05:1181–1186. https://doi.org/10.4236/me.2014.513110

    Article  Google Scholar 

  • Courtoisde Viçose G, Viera MP, Bilbao A, Izquierdo MS (2007) Embryonic and larval development of Haliotis tuberculata coccinea Reeve: an indexed micro-photographic sequence. J Shellfish Res 26:847–854. https://doi.org/10.2983/0730-8000(2007)26%5b847:EALDOH%5d2.0.CO;2

    Article  Google Scholar 

  • Crim RN, Sunday JM, Harley CDG (2011) Elevated seawater CO2 concentrations impair larval development and reduce larval survival in endangered northern abalone (Haliotis kamtschatkana). J Exp Mar Biol Ecol 400:272–277. https://doi.org/10.1016/j.jembe.2011.02.002

    CAS  Article  Google Scholar 

  • Cunningham SC, Smith AM, Lamare MD (2016) The effects of elevated pCO2 on growth, shell production and metabolism of cultured juvenile abalone, Haliotis iris. Aquac Res 47:2375–2392. https://doi.org/10.1111/are.12684

    CAS  Article  Google Scholar 

  • Cyronak T, Schulz KG, Jokiel PL (2016) The Omega myth: what really drives lower calcification rates in an acidifying ocean. ICES J Mar Sci 73:558–562. https://doi.org/10.1093/icesjms/fsv075

    Article  Google Scholar 

  • Day RW, Quinn GP (1989) Comparisons of treatments after an analysis of variance in ecology. Ecol Monogr 59:433–463. https://doi.org/10.2307/1943075

    Article  Google Scholar 

  • Dickson AG (2010) Standards for ocean measurements. Oceanography 23:34–47. https://doi.org/10.5670/oceanog.2010.22

    Article  Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34:1733–1743

    CAS  Article  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3, IOCCP Report 8, North Pacific Marine Science Organization, Sidney, British Columbia, p 191

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192. https://doi.org/10.1146/annurev.marine.010908.163834

    Article  Google Scholar 

  • Duquette A, McClintock JB, Amsler CD, Pérez-Huerta A, Milazzo M, Hall-Spencer JM (2017) Effects of ocean acidification on the shells of four Mediterranean gastropod species near a CO2 seep. Mar Pollut Bull 124:917–928. https://doi.org/10.1016/j.marpolbul.2017.08.007

    CAS  Article  PubMed  Google Scholar 

  • Ekstrom JA, Suatoni L, Cooley SR, Pendleton LH, Waldbusser GG, Cinner JE, Ritter J, Langdon C, Van Hooidonk R, Gledhill D, Wellman K, Beck MW, Brander LM, Rittschof D, Doherty C, Edwards PET, Portela R (2015) Vulnerability and adaptation of US shellfisheries to ocean acidification. Nat Clim Change 5:207–214. https://doi.org/10.1038/nclimate2508

    Article  Google Scholar 

  • Ellis RP, Bersey J, Rundle SD, Hall-Spencer JM, Spicer JI (2009) Subtle but significant effects of CO2 acidified seawater on embryos of the intertidal snail, Littorina obtusata. Aquat Biol 5:41–48. https://doi.org/10.3354/ab00118

    Article  Google Scholar 

  • Fitzer SC, Cusack M, Phoenix VR, Kamenos NA (2014a) Ocean acidification reduces the crystallographic control in juvenile mussel shells. J Struct Biol 188:39–45. https://doi.org/10.1016/j.jsb.2014.08.007

    CAS  Article  PubMed  Google Scholar 

  • Fitzer SC, Phoenix VR, Cusack M, Kamenos NA (2014b) Ocean acidification impacts mussel control on biomineralisation. Sci Rep 4:6218. https://doi.org/10.1038/srep06218

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Gallardo WG, Bautista-Teruel MN, Fermin AC, Marte CL (2003) Shell marking by artificial feeding of the tropical abalone Haliotis asinina Linne juveniles for sea ranching and stock enhancement. Aquac Res 34:839–842

    Article  Google Scholar 

  • Gattuso JP, Magnan A, Bille R, Cheung WWL, Howes EL, Joos F, Allemand D, Bopp L, Cooley SR, Eakin CM, Hoegh-Guldberg O, Kelly RP, Portner HO, Rogers AD, Baxter JM, Laffoley D, Osborn D, Rankovic A, Rochette J, Sumaila UR, Treyer S, Turley C (2015) Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349:4722. https://doi.org/10.1126/science.aac4722

    CAS  Article  Google Scholar 

  • Gazeau F, Quiblier C, Jansen JM, Gattuso J-P, Middelburg JJ, Heip CHR (2007) Impact of elevated CO2 on shellfish calcification. Geophys Res Lett. https://doi.org/10.1029/2006gl028554

    Article  Google Scholar 

  • Gazeau F, Gattuso JP, Dawber C, Pronker AE, Peene F, Peene J, Heip CHR, Middelburg JJ (2010) Effect of ocean acidification on the early life stages of the blue mussel Mytilus edulis. Biogeosciences 7:2051–2060. https://doi.org/10.5194/bg-7-2051-2010

    CAS  Article  Google Scholar 

  • Gazeau F, Parker LM, Comeau S, Gattuso J-P, O’Connor WA, Martin S, Pörtner H-O, Ross PM (2013) Impacts of ocean acidification on marine shelled molluscs. Mar Biol 160:2207–2245. https://doi.org/10.1007/s00227-013-2219-3

    CAS  Article  Google Scholar 

  • Guo X, Huang M, Pu F, You W, Ke C (2015) Effects of ocean acidification caused by rising CO2 on the early development of three mollusks. Aquat Biol 23:147–157. https://doi.org/10.3354/ab00615

    CAS  Article  Google Scholar 

  • Hendriks IE, Duarte CM, Álvarez M (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuar Coast Shelf Sci 86:157–164. https://doi.org/10.1016/j.ecss.2009.11.022

    CAS  Article  Google Scholar 

  • Hiebenthal C, Philipp EER, Eisenhauer A, Wahl M (2013) Effects of seawater pCO2 and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.). Mar Biol 160:2073–2087. https://doi.org/10.1007/s00227-012-2080-9

    CAS  Article  Google Scholar 

  • Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism to-ecosystem perspectiv. Annu Rev Ecol Evol Syst 41:127–147. https://doi.org/10.1146/annurev.ecolsys.ll0308.120227

    Article  Google Scholar 

  • Huchette S, Clavier J (2004) Status of the ormer (Haliotis tuberculata L.) industry in Europe. J Shellfish Res 23:951–955

    Google Scholar 

  • Hüning AK, Melzner F, Thomsen J, Gutowska MA, Krämer L, Frickenhaus S, Rosenstiel P, Pörtner H-O, Philipp EER, Lucassen M (2012) Impacts of seawater acidification on mantle gene expression patterns of the Baltic Sea blue mussel: implications for shell formation and energy metabolism. Mar Biol 160:1845–1861. https://doi.org/10.1007/s00227-012-1930-9

    CAS  Article  Google Scholar 

  • IPCC (2014) Summary for policymakers. In: Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 1–32

  • Jardillier E, Rousseau M, Gendron-Badou A, Fröhlich F, Smith DC, Martin M, Helléouet M-N, Huchette S, Doumenc D, Auzoux-Bordenave S (2008) A morphological and structural study of the larval shell from the abalone Haliotis tuberculata. Mar Biol 154(4):735–744

    Article  Google Scholar 

  • Kimura RYO, Takami H, Ono T, Onitsuka T, Nojiri Y (2011) Effects of elevated pCO2 on the early development of the commercially important gastropod, Ezo abalone Haliotis discus hannai. Fish Oceanogr 20:357–366. https://doi.org/10.1111/j.1365-2419.2011.00589.x

    Article  Google Scholar 

  • Klok C, Wijsman JWM, Kaag K, Foekema E (2014) Effects of CO2 enrichment on cockle shell growth interpreted with a dynamic energy budget model. J Sea Res 94:111–116

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434. https://doi.org/10.1111/j.1461-0248.2010.01518.x

    Article  Google Scholar 

  • Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284. https://doi.org/10.3354/meps07802

    CAS  Article  Google Scholar 

  • Legrand E, Riera P, Pouliquen L, Bohner O, Cariou T, Martin S (2018) Ecological characterization of intertidal rockpools: seasonal and diurnal monitoring of physico-chemical parameters. Reg Stud Mar Sci 17:1–10. https://doi.org/10.1016/j.rsma.2017.11.003

    Article  Google Scholar 

  • Li J, Mao Y, Jiang Z, Zhang J, Fang J, Bian D (2018) The detrimental effects of CO2-driven chronic acidification on juvenile Pacific abalone (Haliotis discus hannai). Hydrobiologia 809:297–308. https://doi.org/10.1007/s10750-017-3481-z

    CAS  Article  Google Scholar 

  • Marchais V, Jolivet A, Herve S, Roussel S, Schone BR, Grall J, Chauvaud L, Clavier J (2017) New tool to elucidate the diet of the ormer Haliotis tuberculata (L.): digital shell color analysis. Mar Biol 164(4):1–13

    Article  Google Scholar 

  • Martin S, Richier S, Pedrotti ML, Dupont S, Castejon C, Gerakis Y, Kerros ME, Oberhansli F, Teyssie JL, Jeffree R, Gattuso JP (2011) Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J Exp Biol 214:1357–1368. https://doi.org/10.1242/jeb.051169

    CAS  Article  Google Scholar 

  • McClintock JB, Angus RA, Mcdonald MR, Amsler CD, Catledge SA, Vohra YK (2009) Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification. Antarct Sci 21:449–456. https://doi.org/10.1017/S0954102009990198

    Article  Google Scholar 

  • McNeill AR (1968) Animal mechanics. Sidgwick and Jackson, London

    Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907. https://doi.org/10.4319/lo.1973.18.6.0897

    CAS  Article  Google Scholar 

  • Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Portner HO (2009) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6:2313–2331

    CAS  Article  Google Scholar 

  • Melzner F, Stange P, Trübenbach K, Thomsen J, Casties I, Panknin U, Gorb SN, Gutowska MA (2011) Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS One. https://doi.org/10.1371/journal.pone.0024223

    Article  PubMed  PubMed Central  Google Scholar 

  • Mercer JP, Mai KS, Donlon J (1993) Comparative studies on the nutrition of 2 species of abalone, Haliotis tuberculata Linnaeus and Haliotis discus hannai Ino. 1. Effects of algal diets on growth and biochemical composition. Invertebr Reprod Dev 23:75–88

    CAS  Article  Google Scholar 

  • Michaelidis B, Ouzounis C, Paleras A, Pörtner H-O (2005) Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar Ecol Prog Ser 293:109–118

    Article  Google Scholar 

  • Morash AJ, Alter K (2015) Effects of environmental and farm stress on abalone physiology: perspectives for abalone aquaculture in the face of global climate change. Rev Aquac 7:1–27. https://doi.org/10.1111/raq.12097

    Article  Google Scholar 

  • Morse JW, Arvidson RS, Luttge A (2007) Calcium carbonate formation and dissolution. Chem Rev 107:342–381. https://doi.org/10.1021/cr050358j

    CAS  Article  PubMed  Google Scholar 

  • Nicolas JL, Basuyaux O, Mazurié J, Thébault A (2002) Vibrio carchariae, a pathogen of the abalone Haliotis tuberculata. Dis Aquat Organ 50:35–43

    CAS  Article  Google Scholar 

  • Noisette F, Comtet T, Legrand E, Bordeyne F, Davoult D, Martin S (2014) Does encapsulation protect embryos from the effects of ocean acidification? The example of Crepidula fornicata. PLoS One. https://doi.org/10.1371/journal.pone.0093021

    Article  PubMed  PubMed Central  Google Scholar 

  • Onitsuka T, Takami H, Muraoka D, Matsumoto Y, Nakatsubo A, Kimura R, Ono T, Nojiri Y (2018) Effects of ocean acidification with pCO2 diurnal fluctuations on survival and larval shell formation of Ezo abalone, Haliotis discus hannai. Mar Environ Res 134:28–36. https://doi.org/10.1016/j.marenvres.2017.12.0152

    CAS  Article  PubMed  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. https://doi.org/10.1038/nature04095

    CAS  Article  PubMed  Google Scholar 

  • Parker L, Ross P, O’Connor W, Pörtner H, Scanes E, Wright J (2013) Predicting the response of molluscs to the impact of ocean acidification. Biology 2:651–692. https://doi.org/10.3390/biology2020651

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Pierrot DE, Lewis E, Wallace DWR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center. Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee

  • Przeslawski R, Byrne M, Mellin C (2015) A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob Change Biol 21:2122–2140. https://doi.org/10.1111/gcb.12833

    Article  Google Scholar 

  • Qui-Minet ZN, Delaunay C, Grall J, Six C, Cariou T, Bohner O, Legrand E, Davoult D, Martin S (2018) The role of local environmental changes on maerl and its associated non-calcareous epiphytic flora in the Bay of Brest. Estuar Coast Shelf Sci 208:140–152. https://doi.org/10.1016/j.ecss.2018.04.032

    CAS  Article  Google Scholar 

  • Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union

  • Ross PM, Parker L, O’Connor WA, Bailey EA (2011) The impact of ocean acidification on reproduction, early development and settlement of marine organisms. Water 3:1005–1030. https://doi.org/10.3390/w3041005

    CAS  Article  Google Scholar 

  • Shepherd SA (1973) Studies on southern Australian abalone (genus Haliotis). I. Ecology of five sympatric species. Aust J Mar Freshw Res 24:217–257

    Article  Google Scholar 

  • Talmage SC, Gobler CJ (2010) Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. PNAS 107:17246–17251. https://doi.org/10.1073/pnas.0913804107

    Article  PubMed  Google Scholar 

  • R Core Team (2015) R Core Team: a language and environment for statistical computing. Vienna, Austria

  • Thomsen J, Melzner F (2010) Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Mar Biol 157:2667–2676. https://doi.org/10.1007/s00227-010-1527-0

    Article  Google Scholar 

  • Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K, Fietzke K, Hiebenthal C, Eisenhauer A, Körtzinger A, Wahl M, Melzner F (2010) Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7:3879–3891. https://doi.org/10.5194/bg-7-3879-2010

    CAS  Article  Google Scholar 

  • Thomsen J, Haynert K, Wegner KM, Melzner F (2015) Impact of seawater carbonate chemistry on the calcification of marine bivalves. Biogeosciences 12:4209–4220. https://doi.org/10.5194/bg-12-4209-2015

    Article  Google Scholar 

  • Travers M-A, Basuyaux O, Le Goic N, Huchette S, Nicolas J-L, Koken M, Paillard C (2009) Influence of temperature and spawning effort on Haliotis tuberculata mortalities caused by Vibrio harveyi: an example of emerging vibriosis linked to global warming. Glob Change Biol 15:1365–1376. https://doi.org/10.1111/j.1365-2486.2008.01764.x

    Article  Google Scholar 

  • Vogel S (2003) Comparative biomechanics. Princeton University Press, Princeton

    Google Scholar 

  • Waldbusser GG, Steenson RA, Green MA (2011) Oyster shell dissolution rates in estuarine waters: effects of pH and shell legacy. J Shellfish Res 30:659–670

    Article  Google Scholar 

  • Weiss IM, Lüke F, Eichner N, Guth C, Clausen-Schaumann H (2013) On the function of chitin synthase extracellular domains in biomineralization. J Struct Biol 183:216–225. https://doi.org/10.1016/j.jsb.2013.04.011

    CAS  Article  PubMed  Google Scholar 

  • Welladsen HM, Southgate PC, Heimann K (2010) The effects of exposure to near-future levels of ocean acidification on shell characteristics of Pinctada fucata (Bivalvia: Pteriidae). Molluscan Res 30:125–130

    Google Scholar 

  • Wessel N, Martin S, Badou A, Dubois P, Huchette S, Julia V, Nunes F, Harney E, Paillard C, Auzoux-Bordenave S (2018) Effect of CO2-induced ocean acidification on the early development and shell mineralization of the European abalone Haliotis tuberculata. J Exp Mar Biol Ecol 508:52–63

    CAS  Article  Google Scholar 

  • Widdicombe S, Spicer JI (2008) Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? J Exp Mar Biol Ecol 366:187–197. https://doi.org/10.1016/j.jembe.2008.07.024

    Article  Google Scholar 

  • Wittmann AC, Pörtner H-O (2013) Sensitivities of extant animal taxa to ocean acidification. Nat Clim Change 3:995–1001. https://doi.org/10.1038/NCLIMATE1982

    CAS  Article  Google Scholar 

  • Zippay ML, Hofmann GE (2010) Effect of pH on gene expression and thermal tolerance of early life history stages of red abalone (Haliotis rufescens). J Shellfish Res 29:429–439

    Article  Google Scholar 

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Acknowledgements

N. Wessel was supported by a postdoctoral fellowship from the MNHN (Ministère de l’Enseignement Supérieur et de la Recherche, Paris, France). This work was supported in part by the ATM program “Biomineralization” of the MNHN funded by the Ministère délégué à l’Enseignement Supérieur et à la Recherche (Paris, France) and by the ICOBio project under the program “Acidification des Océans” funded by the Fondation pour la Recherche sur la Biodiversité (FRB) and the Ministère de la Transition Ecologique et Solidaire (MTES). We thank Dr. Chakib Djejat and Stéphane Formosa for their assistance in scanning electron microscopy (SEM, Plateau technique de Microscopie Electronique, MNHN, Paris and Concarneau, France). The Regional Council of Brittany, the General Council of Finistère, the urban community of Concarneau Cornouaille Agglomération and the European Regional Development Fund (ERDF) are acknowledged for the funding of the Sigma 300 FE-SEM of the Concarneau Marine Station. We thank Dr. Cedric Hubas for his valuable support for the statistical analyses and the Translation Bureau of the University of Western Brittany for improving the English of this manuscript. We also thank the three anonymous reviewers for their comments which have helped to improve this manuscript. Ph. Dubois is a Research Director of the National Fund for Scientific Research (Belgium).

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Auzoux-Bordenave, S., Wessel, N., Badou, A. et al. Ocean acidification impacts growth and shell mineralization in juvenile abalone (Haliotis tuberculata). Mar Biol 167, 11 (2020). https://doi.org/10.1007/s00227-019-3623-0

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