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Marine Biology

, Volume 161, Issue 10, pp 2423–2431 | Cite as

Health and population-dependent effects of ocean acidification on the marine isopod Idotea balthica

  • Hannah L. WoodEmail author
  • Helen N. Sköld
  • Susanne P. Eriksson
Original Paper

Abstract

Three populations of the grazing isopod Idotea balthica were exposed to high CO2 treatment for a period of 20 days to investigate the effect of ocean acidification (OA) on animal health and immunocompetence. The results of the populations from more saline habitats were comparable and showed a 60–80 % decrease in immune response as a result of the high CO2 treatment. Analysis of protein carbonyls showed no treatment effect, indicating that short-term OA does not increase oxidative protein damage. Meanwhile, the third tested population from the lower saline Baltic Sea had higher background protein carbonyl levels. Ocean acidification in addition to this resulted in 100 % mortality. The results of this study show that OA reduced immunocompetence of this marine isopod. In addition, populations and individuals in poor health are potentially at greater risk to succumb under OA.

Keywords

Hemocyte Ocean Acidification High pCO2 Oxidative Stress Level High Oxidative Stress 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors wish to thanks Kirsten Seal for her assistance in the laboratory and the two anonymous reviewers whose comments contributed to the improvement of this article. This work was funded though The Centre for Marine Evolutionary Biology (CeMEB), a Linnaeus Centre of Excellence, with additional project funding from the Wåhlström Foundation.

References

  1. Belkin IM (2009) Rapid warming of large marine ecosystems. Prog Oceanogr 81:207–213CrossRefGoogle Scholar
  2. Bibby R, Cleall-Harding P, Rundle S, Widdicombe S, Spicer JI (2007) Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biol Lett 3:699–701CrossRefGoogle Scholar
  3. Bibby R, Widdicombe S, Parry H, Spicer JI, Pipe R (2008) Effect of ocean acidification on the immune response of the blue mussel Mytilus edulis. Aquat Biol 2:67–74CrossRefGoogle Scholar
  4. Bradassi F, Cumani F, Bressan G et al (2013) Early reproductive stages in the crustose coralline alga Phymatolithon lenormandii are strongly affected by mild ocean acidification. Mar Biol 160:2261–2269CrossRefGoogle Scholar
  5. Bussell JA, Gidman EA, Causton DR et al (2008) Changes in the immune response and metabolic fingerprint of the mussel, Mytilus edulis (Linnaeus) in response to lowered salinity and physical stress. J. Exp Mar Biol Ecol 358:78–85CrossRefGoogle Scholar
  6. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  7. Dickinson GH, Matoo OB, Tourek RT, Sokolova IM, Beniash E (2013) Environmental salinity modulates the effects of elevated CO2 levels on juvenile hard-shell clams, Mercenaria mercenaria. J Exp Biol 216:2607–2618CrossRefGoogle Scholar
  8. Dickson AG (1990) Standard potential of the reaction—AgCl(S) ? 1/2H–2(g) = AG(S) + HCL(aq) and the standard acidity constant of the ion HSO4- in synthetic sea-water from 27315-K to 31815-K. J Chem Thermodyn 22:113–127CrossRefGoogle Scholar
  9. Dickson AG, Millero FJ (1987) Comparison of the equilibrium constants for the dissociation of carbonic-acid in seawater media. Deep Sea Res 34:1733–1743CrossRefGoogle Scholar
  10. Feely RA, Doney SC, Cooley SR (2009) Ocean acidification: present conditions and future changes in a high-CO2 world Oceanogr 22:36–47Google Scholar
  11. Feistel R, Weinreben S, Wolf H, Seitz S, Spitzer P, Adel B, Nausch G, Schneider B, Wright DG (2010) Density and absolute salinity of the Baltic Sea 2006–2009. Ocean Sci 6:3–24CrossRefGoogle Scholar
  12. Findlay HS, Kendall MA, Spicer JI, Turley C, Widdicombe S (2008) Novel microcosm system for investigating the effects of elevated carbon dioxide and temperature on intertidal organisms. Aquat Biol 3:51–62CrossRefGoogle Scholar
  13. Havenhand JN, Buttler F-R, Thorndyke MC, Williamson JE (2008) Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr Biol 18:R651–R652CrossRefGoogle Scholar
  14. Hernroth B, Baden S, Thorndyke M, Dupont S (2011) Immune suppression of the echinoderm Asterias rubens L. following long-term ocean acidification. Aquat Toxicol 103:222–224CrossRefGoogle Scholar
  15. Hernroth B, Sköld HN, Wiklander K, Jutfelt F, Baden S (2012) Simulated change causes immune suppression and protein damage in the crustacean Nephrops norvegicus. Fish Shellfish Immunol 33:1095–1101CrossRefGoogle Scholar
  16. IPCC (2007) Climate change 2007: synthesis report: summary for policymakersGoogle Scholar
  17. Jormalainen V, Honkanen T, Mäkinen A, Hemmi A, Vesakoski O (2001) Why does herbivore sex matter? Sexual differences in utilization of Fucus vesiculosus by the isopod Idotea baltica. Oikos 93:77–86CrossRefGoogle Scholar
  18. Kurtz J (2002) Phagocytosis by invertebrate hemocytes: causes of individual variation in Panorpa vulgaris scorpionflies. Microsc Res Tech 57:465–468CrossRefGoogle Scholar
  19. Leidenberger S (2013) Adaptation to the Baltic Sea—the case of isopod genus Idotea. Doctoral Thesis, University of Gothenburg, Faculty of Science, Department of Biological and Environmental SciencesGoogle Scholar
  20. Levine RL, Stadtman ER (2001) Oxidative modification of proteins during aging. Exp Gerontol 36:1495–1502CrossRefGoogle Scholar
  21. Lewis CN, Brown KA, Edwards LA et al (2013) Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice. Proc Natl Acad Sci USA:E4960–E4967Google Scholar
  22. Matozzo V, Chinellato A, Munari M et al (2012) First Evidence of Immunomodulation in Bivalves under Seawater Acidification and Increased Temperature. PLoS ONE 7:e33820CrossRefGoogle Scholar
  23. Matozzo V, Chinellato A, Munari M, Bressan M, Marin MG (2013) Can the combination of decreased pH and increased temperature values induce oxidative stress in the clam Chamelea gallina and the mussel Mytilus galloprovincialis? Mar Pollut Bull 72:34–40CrossRefGoogle Scholar
  24. Mayor DJ, Everett NR, Cook KB (2012) End of century ocean warming and acidification effects on reproductive success in a temperate marine copepod. J Plankton Res 34:258–262CrossRefGoogle Scholar
  25. McNeil BI, Matear RJ (2008) Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc Natl Acad Sci USA 105:18860–18864CrossRefGoogle Scholar
  26. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  27. Meier HEM (2006) Baltic Sea climate in the late twenty-first century: a dynamical downscaling approach using two global models and two emission scenarios. Clim Dyn 27:39–68CrossRefGoogle Scholar
  28. Melatunan S, Calosi P, Rundle SD et al (2013) Effects of ocean acidification and elevated temperature on shell plasticity and its energetic basis in an intertidal gastropod. Mar Ecol Prog Ser 472:155–168CrossRefGoogle Scholar
  29. Melzner F, Thomsen J, Koeve W et al (2013) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 160:1875–1888CrossRefGoogle Scholar
  30. Niiranen S, Yletyinen J, Tomczak MT, Blenckner T, Hjerne O, MacKenzie BR et al (2013) Combined effects of global climate change and regional ecosystem drivers on an exploited marine food web. Glob Chang Biol 19:3327–3342Google Scholar
  31. Nylund GM, Pereyra RT, Wood HL, Johannesson K, Pavia H (2012) Increased resistance towards generalist herbivory in the new range of a habitat-forming seaweed. Ecosphere 3(12):(Article 125)Google Scholar
  32. Pansch C, Nasrolahi A, Appelhans YS et al (2013) Tolerance of juvenile barnacles (Amphibalanus improvisus) to warming and elevated pCO2. J Exp Mar Biol Ecol 160:2023–2035CrossRefGoogle Scholar
  33. Pierrot D, Lewis E, Wallace DWR (2006) Co2sys Dos Program Developed for CO2 System Calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, TennesseeGoogle Scholar
  34. Range P, Chicharo MA, Ben-Hamadou R, Pilo D, Matias D et al (2011) Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO(2) and reduced pH: variable responses to ocean acidification at local scales? J Exp Mar Biol Ecol 396:177–184CrossRefGoogle Scholar
  35. Raven J, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society policy document 12/05. The Clyvedon Press Ltd., Cardiff, UKGoogle Scholar
  36. Reznick AZ, Packer L (1994) Oxidative damage to proteins. Spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363CrossRefGoogle Scholar
  37. Roth O, Kurtz J (2009) Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Dev Comp Immunol 33:11151–11155CrossRefGoogle Scholar
  38. Roth O, Kurtz J, Reusch TBH (2010) A summer heat wave decreases the immunocompetence of the mesograzer, Idotea baltica. Mar Biol 157:1605–1611CrossRefGoogle Scholar
  39. Schiffer M, Harms L, Poertner HO et al (2014) Pre-hatching seawater pCO2 affects development and survival of zoea stages of Arctic spider crab Hyas araneus. Mar Ecol Prog Ser 501:127–139CrossRefGoogle Scholar
  40. Schlegel P, Havenhand JN Gillings MR, et al (2012) Individual variability in reproductive success determines winners and losers under ocean acidification: a case study with sea urchins. PLoS One:e53118Google Scholar
  41. Steenbergen JF, Steenbergen SM, Schapiro HC (1978) Effects of temperature on phagocytosis in Homarus americanus. Aquaculture 14:23–30CrossRefGoogle Scholar
  42. Styf HK, Skold HN, Eriksson SP (2013) Embryonic response to long-term exposure of the marine crustacean Nephrops norvegicus to ocean acidification and elevated temperature. Ecol Evol 3:5055–5065CrossRefGoogle Scholar
  43. Tomanek L, Zuzow MJ, Ivanina AV, Beniash E, Sokolova IM (2011) Proteomic response to elevated PCO2 level in eastern oysters, Crassostrea virginica: evidence for oxidative stress. J Exp Biol 214:1836–1844CrossRefGoogle Scholar
  44. Tuomi J, Ilvessalo H, Niemela P, Siren S, Jormalainen V (1989) Within plant variation in phenolic content and toughness of the brown alga Fucus vesiculosus L. Bot Mar 32:505–509CrossRefGoogle Scholar
  45. Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271CrossRefGoogle Scholar
  46. Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc Lond B 275:1767–1773CrossRefGoogle Scholar
  47. Wood HL, Nylund G, Eriksson SP (2014) Physiological plasticity is key to the presence of the isopod Idotea baltica (Pallas) in the Baltic Sea. J Sea Res 85:255–262CrossRefGoogle Scholar
  48. Wood HL, Sundell K, Sköld HN, Carney Almroth B, Eriksson. Evidence of countergradient variation and adaptive slow intrinsic growth rate in a marine Isopod (Idotea balthica) locally adapted to low salinity (in review)Google Scholar
  49. Wootton EC, Pipe RK (2003) Structural and functional characterisation of the blood cells of the bivalve mollusc, Scrobicularia plana. Fish Shellfish Immunol 15:249–262CrossRefGoogle Scholar
  50. Yan B, Dai Q, Liu X, Huang S, Wang Z (1996) Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant Soil 179:261–268CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Hannah L. Wood
    • 1
    Email author
  • Helen N. Sköld
    • 1
  • Susanne P. Eriksson
    • 1
  1. 1.Department of Biological and Environmental Sciences – KristinebergUniversity of GothenburgFiskebäckskilSweden

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