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Hydrobiologia

, Volume 772, Issue 1, pp 161–174 | Cite as

Effects of the increase of temperature and CO2 concentration on polychaetae Nereis diversicolor: simulating extreme scenarios of climate change in marine sediments

  • Karyna C. Pereira
  • Pedro M. Costa
  • Maria H. Costa
  • Ángel Luque
  • T. A. DelValls
  • Inmaculada Riba López
Primary Research Paper

Abstract

In order to evaluate the effects of elevated temperature and pCO2 on the polychaete Nereis diversicolor from the Río San Pedro estuary in Spain, multifactorial stressor experiments were performed in various combinations: at two temperatures (ambient temperature and temperature estimated for the year 2100) and at three pHNBS levels (estimated level in cases of CO2 leakage, at the level used in the high and moderate CO2 treatment, and present-day ambient pH levels). Experimental temperature treatments were designed within the context of a high-emission CO2, “business as usual” scenario, with an approximate median increase in temperature of 3.7–4.8°C by the year 2100. In this study, it was investigated whether oxidative stress occurs in cellular responses to elevated temperatures and CO2 levels in N. diversicolor. It was measured the levels of oxidative stress biomarkers, of hemoglobin, and of the carbonate system. The effects of ocean acidification on these organisms are almost unknown. This study has shown that when subject to pH and temperature stress, the Nereidid polychaete N. diversicolor exhibits reduced survival rates. Also the biomarker (Lipid Peroxidation—LPO) was also found to be sensitive to the pH versus temperature relationship.

Keywords

CCS Polychaetes Oxidative stress Biomarkers Ocean acidification 

Notes

Acknowledgments

The first author thanks the Erasmus Mundus Programme for the Master Grant. The work was partially funded by the Spanish Ministry of the Economy and Competitiveness (European funds FEDER) under project numbers CTM2011-28437-C02-02/TECNO and CTM2012-36476-C02-01. Prof. I. Riba thanks the Ministry of Education (PRX14/00134) in Spain for funding her placement at University Nova of Lisbon (Portugal) and University of Las Palmas de Gran Canaria (Spain).

References

  1. Abele, D., 2002. Toxic oxygen: the radical life-giver. Nature 420: 27.CrossRefPubMedGoogle Scholar
  2. Abele, D., B. Burlando, A. Viarengo & H. O. Pörtner, 1998. Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comparative Biochemistry and Physiology Part B 120: 425–435.CrossRefGoogle Scholar
  3. Abele-Oeschger, D. & R. Oeschger, 1995. Hipoxia-induced autoxidation of haemoglobin in the benthic invertebrates Arenicola marina (Polychaeta) and Astarte borealis (Bivalvia) and the possible effects of sulphide. Journal of Experimental Marine Biology and Ecology 187: 63–80.CrossRefGoogle Scholar
  4. Abele-Oeschger, D., R. Oeschger & H. Theede, 1994. Biochemical adaptations of Nereis diversicolor (Polychaeta) to temporarily increased hydrogen peroxide levels in intertidal sandflats. Marine Ecology Progress Series 106: 101–110.CrossRefGoogle Scholar
  5. Bachu, S. & T. L. Watson, 2009. Review of failures for wells used for CO2 and acid gas injection in Alberta, Canada. Energy Procedia 1: 3531–3537.CrossRefGoogle Scholar
  6. Barry, J. P., J. M. Hall-Spencer & T. Tyrell, 2010. In situ perturbation experiments: natural venting sites, spatial/temporal gradients in ocean pH, manipulative in situ pCO2 perturbations. In Riebesell, U., V. J. Fabry, L. Hansson & J. P. Gattuso (eds), Guide to Best Practices for Ocean Acidification Research and Data Reporting. Publications Office of the European Union, Luxembourg.Google Scholar
  7. Basallote, M. D., A. Rodríguez–Romero, J. Blasco, A. DelValls & I. Riba, 2012. Lethal effects on different marine organisms, associated with sediment – seawater acidification deriving from CO2 leakage. Environmental Science Pollution Research International 19: 2550–2560.CrossRefGoogle Scholar
  8. Basallote, M. D., A. Rodríguez–Romero, M. R. de Orte, A. DelValls & I. Riba, 2015. Evaluation of the threat of marine CO2 leakage-associated acidification on the toxicity of sediment metals to juvenile bivalves. Aquatic Toxicology 166: 63–71.CrossRefPubMedGoogle Scholar
  9. Batten, S. D. & R. N. Bamber, 1996. The effects of acidified sweater on the polychaete Nereis virens Sars, 1835. Marine Pollution Bulletin 32: 283–287.CrossRefGoogle Scholar
  10. Bautista- Chamizo, E., M. R. De Orte, A. Del Valls & I. Riba, 2016. Simulating CO2 leakages from CCS to determine Zn toxicity using the marine microalgae Pleurochrysis roscoffensis. Chemosphere 144: 955–965.CrossRefPubMedGoogle Scholar
  11. Beaugrand, G., 2009. Decadal changes in climate and ecosystems in the North Atlantic Ocean and adjacent seas. Deep Sea Research II 56: 656–673.CrossRefGoogle Scholar
  12. Beutler, E., 1975. Red cell metabolism. A Manual of Biochemical Methods, 2nd ed. Academic Press, New York: 38–131.Google Scholar
  13. Bopp, L., L. Resplandy, J. C. Orr, S. C. Doney, J. P. Dunne, M. Gehlen, P. Halloran, C. Heinze, T. Ilyina, R. Séférian, J. Tjiputra & M. Vichi, 2013. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10: 6225–6245.CrossRefGoogle Scholar
  14. Boveris, A. & B. Chance, 1973. The mitochondrial generation of hydrogen peroxide. Biochemical Journal 134: 707–716.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein- dye binding. Analytical biochemistry 72: 248–254.CrossRefPubMedGoogle Scholar
  16. Chan, V. B. S., C. Li, A. C. Lane, Y. Wang & X. Lu, 2012. CO2-driven ocean acidification alters and weakens integrity of the calcareous tubes produced by the serpulid tubeworm, hydroides elegans. PLoS One 7(8): e42718.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chandel, N. S., E. Maltepe, E. Goldwasser, C. E. Mathieu, M. C. Simon & P. T. Schumacker, 1998. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proceedings of the national academy of sciences USA 95: 11715–11720.CrossRefGoogle Scholar
  18. Chandel, N. S. & P. T. Schumacker, 2000. Cellular oxygen sensing by mitochondria: old questions, new insight. Journal of Applied Physiology 88: 1880–1889.CrossRefPubMedGoogle Scholar
  19. Corliss, B. H. & S. Honjo, 1981. Dissolution of deep-sea benthonic foraminifera. Micropaleontology 27: 356–378.CrossRefGoogle Scholar
  20. Costa, P. M., T. S. Neuparth, S. Caeiro, J. Lobo, M. Martins, A. M. Ferreira, M. Caetano, C. Vale, T. A. DelValls, & M. H. Costa, 2011. Assessment of the genotoxic potential of contaminated estuarine sediments in fish peripheral blood: laboratory versus in situ studies. Environmental Research 111: 25–36.CrossRefPubMedGoogle Scholar
  21. DelValls, A., 2007. Diseño y aplicación de modelos integrados de evaluación de la contaminación y sus efectos sobre los sistemas marinos y litorales y la salud humana. Centro para la prevención y lucha contra la contaminación marítima y del litoral (CEPRECO). Madrid, Ministerio de la Presidencia. 94 pp –Premios de Investigación e Innovación Tecnológica en la Lucha contra la Contaminación Marítima y del Litoral.Google Scholar
  22. Dickson, A. G., 1990. Standard potential of the reaction: AgCl (s) + ½ H2 (g) = Ag (s) + HCl (aq), and the standard acidity constant of the ion HSO4 – in synthetic sea water from 273.15 to 318.15 K. Journal of Chemical Thermodynamics 22: 113–127.CrossRefGoogle Scholar
  23. Dickson, A.G., C. L. Sabine & J. R. Christian, 2007. Determination of dissolved organic carbon and total dissolved nitrogen in sea water. Guide to best practices of ocean CO2 measurements, PICES Special Publication 3. 191 pp.Google Scholar
  24. Dickson, A. G. & F. J. Millero, 1987. A comparison of the equilibrium-constants for the dissociation of carbonic-acid in seawater media. Deep-Sea Research Part a-Oceanographic Research Papers 34: 1733–1743.CrossRefGoogle Scholar
  25. Duranteau, J., N. S. Chandel, A. Kulisz, Z. Shao & P. T. Schumacker, 1998. Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. Journal of Biological Chemistry 273: 11619–11624.CrossRefPubMedGoogle Scholar
  26. Feely, R. A., R. H. Byrne, J. G. Acker, P. R. Beltzer & C. T. A. Chen, 1998. Winter-summer variations of calcite and aragonite saturation in the northeast Pacific. Marine Chemistry 25: 227–241.CrossRefGoogle Scholar
  27. França, M. B., A. D. Panek & E. C. A. Eleutherio, 2007. Oxidative stress and its effects during dehydration. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 146: 621–631.CrossRefGoogle Scholar
  28. Gibbins, J. & H. Chalmers, 2008. Carbon capture and storage. Energy Policy 36: 4317–4322.CrossRefGoogle Scholar
  29. Gough, C., S. Mander & S. Haszeldine, 2010. A roadmap for carbon capture and storage in the UK. International Journal of Greenhouse Gas Control 4: 1–12.CrossRefGoogle Scholar
  30. Guppy, M. & P. Withers, 1999. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biological Reviews 74: 1–40.CrossRefPubMedGoogle Scholar
  31. Hand, S. C., 1991. Metabolic dormancy in aquatic invertebrates. Advances in Comparative and Environmental Physiology 8: 1–50.CrossRefGoogle Scholar
  32. Haye, K. L., J. I. Spicer, S. Widdicombe & M. Briffa, 2012. Reduced pH sea water disrupts chemo-responsive behaviour in an intertidal crustacean. Journal of Experimental Marine Biology and Ecology 412: 134–140.CrossRefGoogle Scholar
  33. Hofmann, G. E., J. P. Barry, P. J. Edmunds, R. D. Gates, D. A. Hutchins & T. Klinger, 2010. The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to ecosystem perspective. Annual Review of Ecology and Systematics 41: 127–147.CrossRefGoogle Scholar
  34. Intergovernmental Panel on Climate Change, 2001. Climate Change 2001: the scientific basis. In: Houghton, J. T., Y. Ding, D. J. Griggs, M. Noguer, P. J. Van Der Linden, X. Dai, K. Maskell, C. A. Johnson. Contribution of Working Group I to the third assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press. 881 pp.Google Scholar
  35. Intergovernmental Panel on Climate Change, 2005. IPCC special report on carbon dioxide capture and storage. In: Metz, B., O. Davidson, H. C. Coninck, M. Loos, L. A. Meyer. Prepared by Working Group III of the Intergovernmental Panelon Climate Change Cambridge: Cambridge University Press. 442 pp.Google Scholar
  36. Intergovernmental Panel on Climate Change, 2013. Climate Change 2013: the physical science basis. In: Stocker, T. F., D. Qin, G. K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, P. M. Midgley. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press. 1535 pp.Google Scholar
  37. Intergovernmental Panel on Climate Change, 2014: Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R.K. Pachauri and L.A. Meyer (eds)]. IPCC, Geneva, Switzerland, 151 pp.Google Scholar
  38. Isaji, S., 1995. Defensive strategies against shell dissolution in bivalves inhabiting acidic environments: the case of Geloina (Corbiculidae) in mangrove swamps. The Veliger 38: 235–246.Google Scholar
  39. Kleypas, J., R. W. Buddemeier, D. Archer, J. P. Gattuso & C. Langdon, 1999. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284: 118–120.CrossRefPubMedGoogle Scholar
  40. Kroeker, K. J., R. L. Kordas, R. Crim, I. E. Hendriks & L. Ramajo, 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19: 1884–1896.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lee, H., B. L. Boese, J. Pelletier, M. Windsor, D. T. Specht & R. C. Randall, 1989. Guidance manual: bedded sediment bioaccumulation tests. EPA/600/X-89/302. Environmental Protection Agency. Newport, Oregon. 232 pp.Google Scholar
  42. Livingstone, D. R., 2001. Contaminated-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin 42: 656–666.CrossRefPubMedGoogle Scholar
  43. Matoo, O., B., V. Ivanina-Anna, C. Ullstad, B. Elia & S. Inna, 2013. Interactive effects of elevated temperature and CO2 levels on metabolism and oxidative stress in two common marine bivalves (Crassostrea virginica and Mercenaria mercenaria). Comparative Biochemistry and Physiology, Comparative Biochemistry and Physiology, Part A 164: 545–553.CrossRefGoogle Scholar
  44. Mehrbach, C., C. H. Culberson, J. E. Hawley & R. M. Pytkowicz, 1973. Measurement of the apparent dissociation constant of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18: 879–907.CrossRefGoogle Scholar
  45. Melzner, F., S. Göbel, M. Langenbuch, M. Gutowska, H. O. Pörtner & M. Lucassen, 2009. Swimming performance in Atlantic Cod (Gadus morhua) following long-term (4–12 months) acclimation to elevated seawater pCO2. Aquatic Toxicology 92: 30–37.CrossRefPubMedGoogle Scholar
  46. Melzner, F., J. Thomsen, W. Koeve, A. Oschlies, M. A. Gutowska, H. W. Bange, H. P. Hansen & A. Körtzinger, 2012. Future ocean acidification will be amplified by hypoxia in coastal habitats. Marine Biology 160: 1875–1888.CrossRefGoogle Scholar
  47. Monastersky, R., 2013. Seabed scars raise questions over carbon-storage plan. Nature 504: 339–340.CrossRefPubMedGoogle Scholar
  48. Mucci, A., 1983. The solubility of calcite and aragonite in seawater at various salinities, temperatures and 1 atmosphere total pressure. American Journal of Science 238: 780–799.CrossRefGoogle Scholar
  49. Nikinmaa, M., 2002. Oxygen-dependent cellular functions – why fishes and their aquatic environment are a prime choice of study. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 133: 1–16.CrossRefGoogle Scholar
  50. Orr, J. C., V. J. Fabry, O. Aumont, L. Bopp, S. C. Doney, R. A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joo, R. M. Key, K. Lindsay, E. Maier-Reimer, R. Matear, P. Monfray, A. Mouchet, R. G. Najjar, G. K. Plattner, K. B. Rodgers, C. L. Sabine, J. L. Sarmiento, R. Schlitzer, R. D. Slater, I. J. Totterdell, M. F. Weirig, Y. Yamanaka & A. Yool, 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.CrossRefPubMedGoogle Scholar
  51. Pierrot, D., E. Lewis & D. W. R. Wallace, 2006. MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee.Google Scholar
  52. Pörtner, H. O., 2002. Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 132: 739–761.CrossRefGoogle Scholar
  53. Pörtner, H. O. & A. Reipschläger, 1996. Ocean disposal of anthropogenic CO2: physiological effects on tolerant and intolerant animals. In Ocean Storage of Carbon Dioxide. Environmental Impact 57–81.Google Scholar
  54. Queirós, A. M., J. A. Fernandes, S. Faulwetter, J. Nunes, S. P. S. Rastrick & N. Mieszkowska, 2014. Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem. Global Change Biology 21: 130–143.CrossRefPubMedGoogle Scholar
  55. Ries, J. B., A. L. Cohen & D. C. McCorkle, 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37: 1131–1134.CrossRefGoogle Scholar
  56. Rodríguez-Romero, A., M. D. Basallote, M. R. De Orte, A. DelValls, I. Riba & J. Blasco, 2014a. Simulation of CO2 leakages during injection and storage in sub-seabed geological formations: metal mobilization and biota effects. Environment International 68: 105–117.CrossRefPubMedGoogle Scholar
  57. Rodríguez-Romero, A., N. Jiménez-Tenorio, M. D. Basallote, M. R. De Orte, J. Blasco & I. Riba, 2014b. Predicting the impacts of CO2 leakage from sub-seabed storage: effects of metal accumulation and toxicity on the model benthic organism Ruditapes philippinarum. Environmental Science & Technology 48: 12292–12301.CrossRefGoogle Scholar
  58. Sarmiento, J. L. & N. Gruber, 2006. Ocean Biogeochemical Dynamics. Princeton: Princeton University Press, 503 pp.Google Scholar
  59. Sies, H., 1993. Strategies of antioxidant defence. European Journal of Biochemestry 215: 213–219.CrossRefGoogle Scholar
  60. Simpson, S.L., G.E, Batley, A. A., Chariton, J. L., Stauber, C. K., King, J. C., Chapman, R. V., Hyne, S. A., Gale, A. C., Roach & W. A., Maher, 2005. Handbook for Sediment Quality Assessment (CSIRO: Bangor, NSW). ISBN 0-643-09197-1.Google Scholar
  61. Solé, M., J. Kopecka- Pilarczyk & J. Blasco, 2008. Pollution biomarkers in two estuarine invertebrates, Nereis diversicolor and Scrobicularia plana, from a Marsh ecosystem in S.W Spain. Environment International. 35: 523–531.CrossRefPubMedGoogle Scholar
  62. Tschischka, K., D. Abele & H. O. Pörtner, 2000. Mitochondrial oxyconformity and cold adaptation in the polychaete Nereis pelagica and the bivalve Arctica islandica from the Baltic and White Seas. Journal of Experimental Biology 203: 3355–3368.PubMedGoogle Scholar
  63. Uchiyama, M. & M. Mihara, 1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analytical Biochemistry 86: 271–278.CrossRefPubMedGoogle Scholar
  64. U.S. Environmental Protection Agency, 1994. Methods for measuring the toxicity of sediment- associated contaminants with estuarine and marine amphipods. EPA-600/R-94/025, Narragansett, RI.Google Scholar
  65. Van Noorden, R., 2010. Carbon sequestration: buried trouble. Nature 463: 871–873.CrossRefPubMedGoogle Scholar
  66. Viarengo, A., D. Lowe, C. Bolognesi, E. Fabbri & A. Koehler, 2007. The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comparative biochemistry and physiology Part C toxicology & pharmacology 146: 281–300.CrossRefGoogle Scholar
  67. Waldbusser, G. G., E. L. Brunner, B. A. Haley, B. Hales & C. J. Langdon, 2013. A developmental and energetic basis linking larval oyster shell formation to acidification sensitivity. Geophysical Research Letters 40: 2171–2176.CrossRefGoogle Scholar
  68. Wittmann, A. C., H. O. Portner, 2013. Sensitivities of extant animal taxa to ocean acidification. Nature Climate Change 3: 995–1001.CrossRefGoogle Scholar
  69. Widdicombe, S., S. L. Dashfield, C. L. McNeill, H. R. Needham, A. Beesley & A. McEvoy, 2009. Effects of CO2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Marine ecology progress series 379: 59–75.CrossRefGoogle Scholar
  70. Widdicombe, S. & H. R. Needham, 2007. Impact of CO2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Marine ecology progress series 341: 111–122.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Karyna C. Pereira
    • 1
  • Pedro M. Costa
    • 2
    • 3
  • Maria H. Costa
    • 2
  • Ángel Luque
    • 4
  • T. A. DelValls
    • 1
  • Inmaculada Riba López
    • 1
  1. 1.Cátedra UNESCO/UNITWIN/WiCop, Facultad de Ciencias del Mar y AmbientalesUniversidad de CádizPuerto Real, CádizSpain
  2. 2.MARE – Marine and Environmental Sciences Centre, Departamento de Ciências e Engenharia do AmbienteFaculdade de Ciências e Tecnologia da Universidade Nova de LisboaCaparicaPortugal
  3. 3.Unit of Molecular Toxicology, Institute of Environmental Medicine (IMM)Karolinska InstitutetStockholmSweden
  4. 4.Departamento de BiologíaUniversidad de Las Palmas de Gran CanariaLas PalmasSpain

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