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

Regional Environmental Change

Volumn 14, Issue SUPPL.1, 2014, Pages 19-30

  Range, P ^a   Chicharo M A ^a   Ben Hamadou, R ^a,b   Pilo D ^a   Fernandez Reiriz, M J ^c   Labarta, U ^c   Marin, M G ^d   Bressan, M ^d   Matozzo, V ^d   Chinellato, A ^d   Munari, M ^d   El Menif, N T ^e   Dellali, M ^e   Chicharo L ^a,f  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b Qatar University   (Qatar)

^c INSTITUTO DE INVESTIGACIONES MARINAS   (Spain)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITY OF CARTHAGE   (Tunisia)

^f UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Carbon dioxide; Coastal waters; Gulf of Cadiz; Lagoon of Venice; Mollusks; Ocean acidification

Indexed keywords

BIVALVIA; CHAMELEA GALLINA; MOLLUSCA; MYTILUS GALLOPROVINCIALIS; RUDITAPES; VENERUPIS (RUDITAPES) DECUSSATUS;

EID: 84893702528     PISSN: 14363798     EISSN: 1436378X     Source Type: Journal    
DOI: 10.1007/s10113-013-0478-7     Document Type: Article

References (89)

1. 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.
2. 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.
3. 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.
4. 2-induced seawater acidification on the health of Mytilus edulis. Clim Res 37: 215-225.
5. 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.
6. 2 on growth of the bivalve Mytilus edulis L. Chemosphere 62: 681-687.
7. 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.
8. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
9. 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.
10. Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19: R602-R614.
11. Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages. Oceanogr Mar Biol Ann Rev 49: 1-42.
12. 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.
13. Caldeira K (2010) Adaptation to impacts of greenhouse gases on the ocean (invited). AGU Fall Meeting Abstracts 52: 03.
14. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425: 365.
15. 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.
16. Casimiro T (2011) Efeitos da acidificação da água do mar na reprodução de Mytilus edulis. Master thesis, Universidade do Algarve, Faro.
17. 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.
18. CIESM (2008) Impacts of acidification on biological, chemical and physical systems in the Mediterranean and Black Seas. Frédéric Briand, Monaco.
19. 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.
20. 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.
21. Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanogr 11: 338-345.
22. 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.
23. Cushman-Roisin B, Gacic M, Poulain P-M, Artegiani A (2001) Physical oceanography of the Adriatic Sea. Kluwer Academic Publisher, Dordrecht, p 304.
24. 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.
25. 2 levels on juvenile eastern oysters, Crassostrea virginica. J Exp Biol 215: 29-43.
26. Diffenbaugh NS, Pal JS, Giorgi F, Gao X (2007) Heat stress intensification in the Mediterranean climate change hotspot. Geophys Res Lett 34: 6.
27. 2 problem. Annu Rev Mar Sci 1: 169-192.
28. 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.
29. Eurostat (2011) EU-27 aquaculture production-quantities (Tonnes live weight): 1984 onwards. http://eu22. eu/aquaculture-production/.
30. 2 coastal ocean. Mar Ecol Prog Ser 433: 97-105.
31. 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.
32. 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.
33. 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.
34. 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.
35. Galloway TS, Depledge MH (2001) Immunotoxicity in Invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 10: 5-23.
36. Gattuso J-P, Hansson L (2011) Ocean Acidification. Oxford University Press.
37. Gattuso J-P, Lavigne H (2009) Approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6: 2121-2133.
38. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Natl Acad Sci 103: 14288-14293.
39. 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.
40. 2 on the ocean environment. Energy Convers Manag 37: 1019-1022.
41. 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.
42. Hendriks IE, Duarte CM, Álvarez M (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuar Coast Shelf Sci 86: 157-164.
43. 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.
44. Hine PM (1999) The inter-relationships of bivalve haemocytes. Fish Shellfish Immunol 9: 367-385.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193: 265-275.
53. 2-induced acidification in the northern Adriatic Sea over the last quarter century. Chem Ecol 26(suppl): 1-17.
54. 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.
55. 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.
56. 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.
57. Matozzo V, Marin MG (2011) Bivalve immune responses and climate changes: is there a relationship? Invertebr Surviv J 8: 70-77.
58. 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.
59. 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.
60. 2 reduces respiration rate and energy status in the Periwinkle Littorina littorea. Physiol Biochem Zool 84: 583-594.
61. 2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS One 6: e24223.
62. 2 concentrations on thermal tolerance of the edible crab Cancer pagurus. J Therm Biol 32: 144-151.
63. 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.
64. 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.
65. Morgan ER, Wall R (2009) Climate change and parasitic disease: farmer mitigation? Trends Parasitol 25: 308-313.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. Pipe RK, Coles JA (1995) Environmental contaminants influencing immune function in marine bivalve molluscs. Fish Shellfish Immunol 5: 581-595.
72. Portner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Mar Ecol Prog Ser 373: 203-217.
73. Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132: 143-151.
74. 2 and reduced pH: variable responses to ocean acidification at local scales? J Exp Mar Biol Ecol 396: 177-184.
75. 2 on life history traits of juvenile mussels Mytilus galloprovincialis in a coastal lagoon environment. J Exp Mar Biol Ecol 424-425: 89-98.
76. 2-induced ocean acidification. Geology 37: 1131-1134.
77. 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.
78. Rosa R, Marques A, Nunes ML (2012) Impact of climate change in Mediterranean aquaculture. Rev Aquac 4: 163-177.
79. 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.
80. 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.
81. Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14: 799-801.
82. 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.
83. Strickland JDH, Parsons TR (1968) A practical handbook of sea water analysis. Queen's Printer, Ottawa.
84. 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.
85. 2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7: 3879-3891.
86. 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.
87. 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.
88. 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.
89. Wollast R (1998) Evaluation and comparison of the global carbon cycle in the coastal zone and in the open ocean. Sea 10: 213-225.