Marine Biology

, Volume 160, Issue 8, pp 1825–1834 | Cite as

Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification

  • Andrea Y. FrommelEmail author
  • Alexander Schubert
  • Uwe Piatkowski
  • Catriona Clemmesen
Original Paper


The accumulation of carbon dioxide in the atmosphere will lower the pH in ocean waters, a process termed ocean acidification (OA). Despite its potentially detrimental effects on calcifying organisms, experimental studies on the possible impacts on fish remain scarce. While adults will most likely remain relatively unaffected by changes in seawater pH, early life-history stages are potentially more sensitive, due to the lack of gills with specialized ion-regulatory mechanisms. We tested the effects of OA on growth and development of embryos and larvae of eastern Baltic cod, the commercially most important fish stock in the Baltic Sea. Cod were reared from newly fertilized eggs to early non-feeding larvae in 5 different experiments looking at a range of response variables to OA, as well as the combined effect of CO2 and temperature. No effect on hatching, survival, development, and otolith size was found at any stage in the development of Baltic cod. Field data show that in the Bornholm Basin, the main spawning site of eastern Baltic cod, in situ levels of pCO2 are already at levels of 1,100 μatm with a pH of 7.2, mainly due to high eutrophication supporting microbial activity and permanent stratification with little water exchange. Our data show that the eggs and early larval stages of Baltic cod seem to be robust to even high levels of OA (3,200 μatm), indicating an adaptational response to CO2.


Ocean Acidification Biochemical Indicator pCO2 Level Bornholm Basin Kiel Fjord 
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.



Funding support was provided through the European Community’s Seventh Framework Programme (FP7/2007-2013) “European Project on Ocean Acidification” (EPOCA, grant agreement N211384) and the project “Biological Impacts of Ocean ACIDification” (BIOACID), funded by the German Ministry for Education and Research (BMBF). The authors are grateful to the RV Alkor crew and supporting scientific staff.


  1. Belchier M, Clemmesen C, Cortes L, Doan T, Folkvord A, Garcia A, Geffen A, Hoie H, Johannessen A, Moksness E, de Pontual H, Ramirez T, Schnack D, Sveinsbo B (2004) Recruitment studies: manual on precision and accuracy of tools. In: ICES techniques in marine environmental sciences, series no.33. Copenhagen, DenmarkGoogle Scholar
  2. Beldowski J, Loffler A, Schneider B, Joensuu L (2010) Distribution and biogeochemical control of total CO2 and total alkalinity in the Baltic Sea. J Mar Syst 81:252–259CrossRefGoogle Scholar
  3. Bradford M (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  4. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefGoogle Scholar
  5. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res-Oceans 110:12CrossRefGoogle Scholar
  6. Checkley DM, Dickson AG, Takahashi M, Radich JA, Eisenkolb N, Asch R (2009) Elevated CO2 enhances otolith growth in young fish. Science 324:1683CrossRefGoogle Scholar
  7. Clemmesen C (1993) Improvements in the fluorometric-determination of the RNA and DNA content of individual marine fish larvae. Mar Ecol Prog Ser 100:177–183CrossRefGoogle Scholar
  8. Clemmesen C, Doan T (1996) Does otolith structure reflect the nutritional condition of a fish larva? Comparison of otolith structure and biochemical index (RNA/DNA ratio) determined on cod larvae. Mar Ecol Prog Ser 138:33–39CrossRefGoogle Scholar
  9. Devine BM, Munday PL, Jones GP (2011) Homing ability of adult cardinalfish is affected by elevated carbon dioxide. Oecologia. doi: 10.1007/s00442-011-2081-2 Google Scholar
  10. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A 34:1733–1743CrossRefGoogle Scholar
  11. Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75CrossRefGoogle Scholar
  12. Ferrari MCO, McCormick MI, Munday PL, Meekan MG, Dixson DL, Lonnstedt Ö, Chivers DP (2011) Putting prey and predator into the CO2 equation—qualitative and quantitative effects of ocean acidification on predator–prey interactions. Ecol Lett 14:1143–1148CrossRefGoogle Scholar
  13. Franke A, Clemme.sen C (2011) Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.). Biogeosciences 8:3697–3707CrossRefGoogle Scholar
  14. Frommel AY, Stiebens V, Clemmesen C, Havenhand J (2010) Effect of ocean acidification on marine fish sperm (Baltic cod: Gadus morhua). Biogeosciences 7:3915–3919CrossRefGoogle Scholar
  15. Frommel AY, Maneja R, Lowe D, Malzahn AM, Geffen AJ, Folkvord A, Piatkowski U, Reusch TBH, Clemmesen C (2011) Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nature Clim Change. doi: 10.1038/NCLIMATE1324 Google Scholar
  16. Houde ED (2008) Emerging from Hjort’s shadow. J Northwest Atl Fish Sci 41:53–70CrossRefGoogle Scholar
  17. IPCC (2007) Climate Change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. CUP, CambridgeGoogle Scholar
  18. Ishimatsu A, Hayashi M, Kikkawa T (2008) Fishes in high CO2, acidified oceans. Mar Ecol Prog Ser 373:295–302CrossRefGoogle Scholar
  19. Koester FW, Hinrichsen HH, Schnack D, St. John MA, Mackenzie BR, Tomkiewicz J, Möllmann C, Kraus G, Plikshs M, Makarchouk A, Aro E (2003) Recruitment of Baltic cod and sprat stocks: identification of critical life stages and incorporation of environmental variability into stock-recruitment relationships. Sci Mar 67:129–154Google Scholar
  20. Le Pecq JB, Paoletti C (1966) A new fluorometric method for RNA and DNA determination. Anal Biochem 17:100–107CrossRefGoogle Scholar
  21. Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. US Department of Energy, Oak RidgeGoogle Scholar
  22. MacKenzie BR, Gislason H, Möllmann C, Köster FW (2007) Impact of twentyfirst century climate change on the Baltic Sea fish community and fisheries. Glob Change Biol 13:1348–1367CrossRefGoogle Scholar
  23. Mehrbach C, Culberso Ch, Hawley JE, Pytkowic RM (1973) Measurement of apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  24. 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
  25. Melzner F, Gobel S, Langenbuch M, Gutowska MA, Pörtner HO, Lucassen M (2009a) Swimming performance in Atlantic cod (Gadus morhua) following long-term (4–12 months) acclimation to elevated seawater pCO2. Aquat Toxicol 92:30–37CrossRefGoogle Scholar
  26. Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Pörtner HO (2009b) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6:2313–2331CrossRefGoogle Scholar
  27. Morris R (1989) Acid toxicity and aquatic animals. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  28. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Doving KB (2009a) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci USA 106:1848–1852CrossRefGoogle Scholar
  29. Munday PL, Donelson JM, Dixson DL, Endo GGK (2009b) Effects of ocean acidification on the early life history of a tropical marine fish. Proc R Soc B-Biol Sci 276:3275–3283CrossRefGoogle Scholar
  30. Munday PL, Dixson DL, McCormick MI, Meekan M, Ferrari MCO, Chivers DP (2010) Replenishment of fish populations is threatened by ocean acidification. Proc Natl Acad Sci USA 107:12930–12934CrossRefGoogle Scholar
  31. Munday P, Gagliano M, Donelson JM, Dixson DL, Thorrold SR (2011a) Ocean acidification does not affect the early life history development of a tropical marine fish. Mar Ecol Prog Ser 423:211–221CrossRefGoogle Scholar
  32. Munday PL, Hernaman V, Dixson DL, Thorrold SR (2011b) Effect of ocean acidification on otolith development in larvae of a tropical marine fish. Biogeosciences 8:1631–1641CrossRefGoogle Scholar
  33. Nissling A (2004) Effects of temperature on egg and larval survival of cod (Gadus morhua) and sprat (Sprattus sprattus) in the Baltic Sea—implications for stock development. Hydrobiologia 514:115–123CrossRefGoogle Scholar
  34. Nissling A, Westin L (1997) Salinity requirements for successful spawning of Baltic and Belt Sea cod and the potential for cod stock interactions in the Baltic Sea. Mar Ecol Prog Ser 152:261–271CrossRefGoogle Scholar
  35. Pörtner HO, Langenbuch M, Reipschlaeger A (2004) Biological impact of elevated ocean CO2 concentration: lessons from animal physiology and Earth history. J Oceanogr 60:705–718CrossRefGoogle Scholar
  36. Sayer MDJ, Reader JP, Dalziel TRK (1993) Freshwater acidification—effects on the early-life stages of fish. Rev Fish Biol Fish 3:298CrossRefGoogle Scholar
  37. Siegenthaler U, Stocker TF, Monnin E, Luthi D, Schwander J, Stauffer B, Raynaud D, Barnola JM, Fischer H, Masson-Delmotte V, Jouzel J (2005) Stable carbon cycle-climate relationship during the late Pleistocene. Science 310:1313–1317CrossRefGoogle Scholar
  38. Thomsen J, Gutowska MA, Saphorster J, Heinemann A, Trübenbach K, Fietzke J, Hiebenthal C, Eisenhauer A, Kortzinger 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 7:3879–3891CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Andrea Y. Frommel
    • 1
    Email author
  • Alexander Schubert
    • 1
  • Uwe Piatkowski
    • 1
  • Catriona Clemmesen
    • 1
  1. 1.Leibniz-Institute of Marine Sciences IFM-GEOMARKielGermany

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