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Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors

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Abstract

The effects of seawater acidification caused by increasing concentrations of atmospheric carbon dioxide (CO2), combined with other climatic stressors, were studied on 3 coastal Mediterranean bivalve species: the mussel Mytilus galloprovincialis and the clams Chamelea gallina and Ruditapes decussatus. CO2 perturbation experiments produced contrasting responses on growth and calcification of juvenile shells, according to species and location. In the Northern Adriatic (Italy), long-term exposure to reduced pH severely damaged the shells of M. galloprovincialis and C. gallina and reduced growth for the latter species. Seawater in the Ria Formosa lagoon (Portugal) was consistently saturated in carbonates, which buffered the impacts on calcification and growth. After 80 days, no shell damage was observed in Portugal, but mussels in the acidified treatments were less calcified. Reduced clearance, ingestion and respiration rates and increased ammonia excretion were observed for R. decussatus under reduced pH. Clearance rates of juvenile mussels were significantly reduced by acidification in Italy, but not in Portugal. Both locations showed a consistent trend for increased ammonia excretion with decreasing pH, suggesting increased protein catabolism. Respiratory rates were generally not affected. Short-term factorial experiments done in Italy revealed that acidification caused alterations in immunological parameters of adult bivalves, particularly at temperature and salinity values far from the optimal for the species in the Mediterranean. Overall, our results showed large variations in the sensitivities of bivalves to climatic changes, among different species and between local populations of the same species. Expectations of impacts, mitigation and adaptation strategies have to consider such local variability.

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References

  • Almeida C, Silva M (1987) Incidence of agriculture on water quality at Campina de Faro (south Portugal). In: IV Simposio de Hidrogeología de la Asociación Española de Hidrología Subterránea, Palma de Mallorca

  • Amaral A (2008) Management of aquaculture of clam, R. decussatus (Linnaeus, 1758) in the Ria Formosa lagoon (south of Portugal), effects on the ecosystem and species physiology. Doctoral thesis, Universidade de Santiago de Compostela, p 168

  • Andersson AJ, Mackenzie FT, Gattuso J-P (2011) Effects of ocean acidification on benthic processes, organisms, and ecosystems. In: Gattuso J-P, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 122–153

    Google Scholar 

  • Beesley A, Lowe DM, Pascoe CK, Widdicombe S (2008) Effects of CO2-induced seawater acidification on the health of Mytilus edulis. Clim Res 37:215–225

    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

    Article  CAS  Google Scholar 

  • Berge JA, Bjerkeng B, Pettersen O, Schaanning MT, Øxnevad S (2006) Effects of increased sea water concentrations of CO2 on growth of the bivalve Mytilus edulis L. Chemosphere 62:681–687

    Article  CAS  Google Scholar 

  • Bibby R, Widdicombe S, Parry H, Spicer J, Pipe R (2008) Effects of ocean acidification on the immune response of the blue mussel Mytilus edulis. Aquat Biol 2:67–74

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

  • Borges A, Gypens N (2010) Carbonate chemistry in the coastal zone responds more strongly to eutrophication than to ocean acidification. Limnol Oceanogr 55:346–353

    Google Scholar 

  • Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:R602–R614

    Article  CAS  Google Scholar 

  • Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages. Oceanogr Mar Biol Ann Rev 49:1–42

    Google Scholar 

  • Caldarone E, Wagner M, St Onge-Burns J, Buckley LJ (2001) Protocol and guide for estimating nucleic acids in larval fish using a fluorescence microplate reader. Northeast Fisheries Science Center Reference Document 1

  • Caldeira K (2010) Adaptation to impacts of greenhouse gases on the ocean (invited). AGU Fall Meeting Abstracts 52:03

    Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    Article  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res Oceans 110:C09S04

    Google Scholar 

  • Casimiro T (2011) Efeitos da acidificação da água do mar na reprodução de Mytilus edulis. Master thesis, Universidade do Algarve, Faro

  • Chicharo MA, Amaral A, Morais P, Chicharo L (2007) Effect of sex on ratios and concentrations of DNA and RNA in three marine species. Mar Ecol Prog Ser 332:241–245

    Article  CAS  Google Scholar 

  • CIESM (2008) Impacts of acidification on biological, chemical and physical systems in the Mediterranean and Black Seas. Frédéric Briand, Monaco

    Google Scholar 

  • Cima F, Matozzo V, Marin MG, Ballarin L (2000) Haemocytes of the clam Tapes philippinarum (Adams & Reeve, 1850): morphofunctional characterisation. Fish Shellfish Immun 10:677–693

    Article  CAS  Google Scholar 

  • Coles JA, Farley SR, Pipe RK (1995) Alteration of the immune response of the common marine mussel Mytilus edulis resulting from exposure to cadmium. Dis Aquat Org 22:59–65

    Article  CAS  Google Scholar 

  • Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanogr 11:338–345

    Article  Google Scholar 

  • Cooley SR, Lucey N, Kite-Powell H, Doney SC (2011) Nutrition and income from molluscs today imply vulnerability to ocean acidification tomorrow. Fish Fish 13:182–215

    Google Scholar 

  • Cushman-Roisin B, Gacic M, Poulain P-M, Artegiani A (2001) Physical oceanography of the Adriatic Sea. Kluwer Academic Publisher, Dordrecht, p 304

    Book  Google Scholar 

  • Cyronak T, Santos IR, McMahon A, Eyre BD (2013) Carbon cycling hysteresis in permeable carbonate sands over a diel cycle: implications for ocean acidification. Limnol Oceanogr 58:131–143

    Article  CAS  Google Scholar 

  • Dickinson GH, Ivanina AV, Matoo OB, Pörtner HO, Lannig G, Bock C, Beniash E, Sokolova IM (2012) Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. J Exp Biol 215:29–43

    Article  CAS  Google Scholar 

  • Diffenbaugh NS, Pal JS, Giorgi F, Gao X (2007) Heat stress intensification in the Mediterranean climate change hotspot. Geophys Res Lett 34:6

    Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A, Ramajo L, Carstensen J, Trotter JA, McCulloch M (2013) Is ocean acidification an open-ocean syndrome? Understanding Anthropogenic Impacts on Seawater pH. Estuar Coasts 36:221–236

    Google Scholar 

  • Eurostat (2011) EU-27 aquaculture production—quantities (Tonnes live weight): 1984 onwards. http://eu22.eu/aquaculture-production/

  • Fernández Reiriz MJ, Range P, Álvarez-Salgado XA, Labarta U (2011) Physiological energetics of juvenile clams Ruditapes decussatus in a high CO2 coastal ocean. Mar Ecol Prog Ser 433:97–105

    Article  Google Scholar 

  • Fernández-Reiriz MJ, Perez-Camacho A, Ferreiro MJ, Blanco J, Planas M, Campos MJ, Labarta U (1989) Biomass production and variation in the biochemical profile (total protein, carbohydrates, RNA, lipids and fatty acids) of seven species of marine microalgae. Aquaculture 83:17–37

    Article  Google Scholar 

  • Fernández-Reiriz MJ, Range P, Alvarez-Salgado XA, Espinosa J, Labarta U (2012) Tolerance of juvenile Mytilus galloprovincialis to experimental seawater acidification. Mar Ecol Prog Ser 454:65–74

    Article  Google Scholar 

  • Filgueira R, Labarta U, Fernandez-Reiriz MJ (2006) Flow-through chamber method for clearance rate measurements in bivalves: design and validation of individual chambers and mesocosm. Limnol Oceangr Methods 4:284–292

    Article  Google Scholar 

  • Findlay HS, Wood HL, Kendall MA, Spicer JI, Twitchett RJ, Widdicombe S (2009) Calcification, a physiological process to be considered in the context of the whole organism. Biogeosci Discuss 6:2267–2284

    Article  Google Scholar 

  • Galloway TS, Depledge MH (2001) Immunotoxicity in Invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 10:5–23

    Article  CAS  Google Scholar 

  • Gattuso J-P, Hansson L (2011) Ocean Acidification. Oxford University Press

  • Gattuso J-P, Lavigne H (2009) Approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6:2121–2133

    Article  CAS  Google Scholar 

  • Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Natl Acad Sci 103:14288–14293

    Article  CAS  Google Scholar 

  • Harvey BP, Gwynn-Jones D, Moore PJ (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol Evol. doi:10.1002/ece3.516

    Google Scholar 

  • Haugan PM, Drange H (1996) Effects of CO2 on the ocean environment. Energy Convers Manag 37:1019–1022

    Article  CAS  Google Scholar 

  • Hauton C, Hawkins LE, Hutchinson S (1998) The use of the neutral red retention assay to examine the effects of temperature and salinity on haemocytes of the European flat oyster Ostrea edulis (L). Comp Biochem Physiol 119B:619–623

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Hildreth DI, Crisp DJ (1976) A corrected formula for calculation of filtration rate of bivalve molluscs in an experimental flowing system. J Mar Biol Assoc UK 56:111–120

    Article  Google Scholar 

  • Hine PM (1999) The inter-relationships of bivalve haemocytes. Fish Shellfish Immunol 9:367–385

    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 perspective. Annu Rev Ecol Evol Syst 41:127–147

    Article  Google Scholar 

  • Joos F, Frölicher T, Steinacher M, Plattner GK (2011) Impact of climate change mitigation on ocean acidification projections. In: Gattuso J-P, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 272–290

    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

    Article  Google Scholar 

  • Labarta U, FernandezReiriz MJ, Babarro JMF (1997) Differences in physiological energetics between intertidal and raft cultivated mussels Mytilus galloprovincialis. Mar Ecol Prog Ser 152:167–173

    Article  Google Scholar 

  • Lannig G, Eilers S, Pörtner HO, Sokolova IM, Bock C (2010) Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas—changes in metabolic pathways and thermal response. Mar Drugs 8:2318–2339

    Article  CAS  Google Scholar 

  • Lejeusne C, Chevaldonné P, Pergent-Martini C, Boudouresque CF, Pérez T (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol Evol 25:250–260

    Article  Google Scholar 

  • Liu W, He M (2012) Effects of ocean acidification on the metabolic rates of three species of bivalve from southern coast of China. Chin J Oceanol Limnol 30:206–211

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Luchetta A, Cantoni C, Catalano G (2010) New observations of CO2-induced acidification in the northern Adriatic Sea over the last quarter century. Chem Ecol 26(suppl):1–17

    Article  CAS  Google Scholar 

  • Marin MG, Chinellato A, Munari M, Bressan M, Matozzo V (in preparation) Long-term effects of sea water acidification on physiological responses of juvenile bivalves Mytilus galloprovincialis and Chamelea gallina

  • Martin LB, Hopkins WA, Mydlarz LD, Rohr JR (2010) The effects of anthropogenic global changes on immune functions and disease resistance. Ann NY Acad Sci 1195:129–148

    Article  Google Scholar 

  • Matozzo V, Marin MG (2010) First evidence of gender-related differences in immune parameters of the clam Ruditapes philippinarum (Mollusca, Bivalvia). Mar Biol 157:1181–1189

    Article  CAS  Google Scholar 

  • Matozzo V, Marin MG (2011) Bivalve immune responses and climate changes: is there a relationship? Invertebr Surviv J 8:70–77

    Google Scholar 

  • Matozzo V, Chinellato A, Munari M, Finos L, Bressan M, Marin MG (2012) First evidence of immunomodulation in bivalves under seawater acidification and increased temperature. PLoS One 7:e33820

    Article  CAS  Google Scholar 

  • Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Kitoh A, Knutti R, Noda A, Watterson IG, Weaver AJ (2007) Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • Melatunan S, Calosi P, Rundle SD, Moody AJ, Widdicombe S (2011) Exposure to elevated temperature and pCO2 reduces respiration rate and energy status in the Periwinkle Littorina littorea. Physiol Biochem Zool 84:583–594

    Article  CAS  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 6:e24223

    Article  CAS  Google Scholar 

  • Metzger R, Sartoris FJ, Langenbuch M, Pörtner HO (2007) Influence of elevated CO2 concentrations on thermal tolerance of the edible crab Cancer pagurus. J Therm Biol 32:144–151

    Article  Google Scholar 

  • Michaelidis B, Ouzounis C, Paleras A, Portner HO (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

    Article  Google Scholar 

  • Montecinos LA, Cisterna JA, Cáceres CW, Saldías GS (2009) Equilibrio ácido-base durante la exposición aérea en el molusco bivalvo Perumytilus purpuratus (Lamarck, 1819) (Bivalvia: Mytilidae). Rev Biol Mar Oceanogr 44:181–187

    Google Scholar 

  • Morgan ER, Wall R (2009) Climate change and parasitic disease: farmer mitigation? Trends Parasitol 25:308–313

    Article  Google Scholar 

  • Moschino V, Chicharo LMZ, Marin MG (2008) Effects of hydraulic dredging on the physiological responses of the target species Chamelea gallina (Mollusca: Bivalvia): laboratory experiments and field surveys. Sci Mar 72:493–501

    Google Scholar 

  • Nicholls RJ, Wong PP, Burkett V, Codignotto J, Hay J, McLean R, Ragoonaden S, Woodroffe CD, Abuodha P, Arblaster J, et al. (2007) Coastal systems and low-lying areas. Climate Change 2007: Impacts, Adaptation and Vulnerability. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on climate change. Cambridge University Press, Cambridge, UK, pp 315–356

  • 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(2):651–692

    Article  CAS  Google Scholar 

  • Pauly D, Christensen V, Guenette S, Pitcher TJ, Sumaila UR, Walters CJ, Watson R, Zeller D (2002) Towards sustainability in world fisheries. Nature 418:689–695

    Article  CAS  Google Scholar 

  • Philippart CJM, Anadón R, Danovaro R, Dippner JW, Drinkwater KF, Hawkins SJ, O’Sullivan G, Oguz T, Reid PC (2007) Impacts of climate change on the European marine and coastal environment ecosystems approach/European Science Foundation Marine Board. European Science Foundation Marine Board, Strasbourg

    Google Scholar 

  • Pipe RK, Coles JA (1995) Environmental contaminants influencing immune function in marine bivalve molluscs. Fish Shellfish Immunol 5:581–595

    Article  Google Scholar 

  • Portner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217

    Article  Google Scholar 

  • Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151

    Article  CAS  Google Scholar 

  • Range P, Chicharo MA, Ben-Hamadou R, Piló D, Matias D, Joaquim S, Oliveira AP, Chicharo L (2011) Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO2 and reduced pH: variable responses to ocean acidification at local scales? J Exp Mar Biol Ecol 396:177–184

    Article  Google Scholar 

  • Range P, Chicharo MA, Ben-Hamadou R, Piló D, Matias D, Joaquim S, Oliveira AP, Chicharo L (2012) Effects of seawater acidification by CO2 on life history traits of juvenile mussels Mytilus galloprovincialis in a coastal lagoon environment. J Exp Mar Biol Ecol 424–425:89–98

    Article  Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    Article  CAS  Google Scholar 

  • Rodolfo-Metalpa R, Houlbreque F, Tambutte E, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso J-P, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Chang 1:308–312

    Article  CAS  Google Scholar 

  • Rosa R, Marques A, Nunes ML (2012) Impact of climate change in Mediterranean aquaculture. Rev Aquac 4:163–177

    Article  Google Scholar 

  • Rufino MM, Gaspar MB, Pereira AM, Vasconcelos P (2006) Use of shape to distinguish Chamelea gallina and Chamelea striatula (Bivalvia: Veneridae): linear and geometric morphometric methods. J Morphol 267:1433–1440

    Article  Google Scholar 

  • Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15

    Article  CAS  Google Scholar 

  • Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    Article  CAS  Google Scholar 

  • Stigter TY, Carvalho Dill AMM, Ribeiro L, Reis E (2006) Impact of the shift from groundwater to surface water irrigation on aquifer dynamics and hydrochemistry in a semi-arid region in the south of Portugal. Agric Water Manage 85:121–132

    Article  Google Scholar 

  • Strickland JDH, Parsons TR (1968) A practical handbook of sea water analysis. Queen’s Printer, Ottawa

    Google Scholar 

  • 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

    Google Scholar 

  • Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K, Fietzke J, 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

    Article  CAS  Google Scholar 

  • Walther K, Sartoris FJ, Bock C, Pörtner HO (2009) Impact of anthropogenic ocean acidification on thermal tolerance of the spider crab Hyas araneus. Biogeosciences 6:2207–2215

    Article  CAS  Google Scholar 

  • Widdicombe S, Spicer JI, Kitidis V (2011) Effects of ocean acidification on sediment fauna. In: Gattuso J-P, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 176–191

    Google Scholar 

  • Widdows J (1985) Physiological measurements. In: Bayne BL, Brown D, Burns K, Dixon D (eds) The effects of stress and pollution on marine animals. Praeger, New York, pp 3–45

    Google Scholar 

  • Wollast R (1998) Evaluation and comparison of the global carbon cycle in the coastal zone and in the open ocean. Sea 10:213–225

    Google Scholar 

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Acknowledgments

This is a contribution of the ACIDBIV project, which is part of the CIRCLE Med network. Funding was provided by the Foundation for Science and Technology (FCT) of Portugal (ERA-CIRCLE/0004/2007), the Regional Ministry of Innovation and Industry of the Galician Government, and the Italian Ministry for Environment, Land and Sea, in the framework of Circle ERA Net project (which is funded by the European Commission 6th Framework Programme). PR was also supported by a post-doctoral grant from FCT (SFRH/BPD/69959/2010). The authors would like to acknowledge the staff of the Bivalve Production Group at IPMA-Tavira for their continuous support. Comments by the editors of this special issue and two anonymous referees substantially improved the original manuscript.

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Range, P., Chícharo, M.A., Ben-Hamadou, R. et al. Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Reg Environ Change 14 (Suppl 1), 19–30 (2014). https://doi.org/10.1007/s10113-013-0478-7

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