Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Responses of pink salmon to CO2-induced aquatic acidification


Ocean acidification negatively affects many marine species and is predicted to cause widespread changes to marine ecosystems. Similarly, freshwater ecosystems may potentially be affected by climate-change-related acidification; however, this has received far less attention. Freshwater fish represent 40% of all fishes, and salmon, which rear and spawn in freshwater, are of immense ecosystem, economical and cultural importance. In this study, we investigate the impacts of CO2-induced acidification during the development of pink salmon, in freshwater and following early seawater entry. At this critical and sensitive life stage, we show dose-dependent reductions in growth, yolk-to-tissue conversion and maximal O2 uptake capacity; as well as significant alterations in olfactory responses, anti-predator behaviour and anxiety under projected future increases in CO2 levels. These data indicate that future populations of pink salmon may be at risk without mitigation and highlight the need for further studies on the impact of CO2-induced acidification on freshwater systems.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Growth measurements in pink salmon (Oncorhynchus gorbuscha) at yolk sac absorption (following ten weeks of CO2 exposure in freshwater).
Figure 2: Predator avoidance behaviour and olfactory responses of pink salmon reared at different p CO 2 tensions to conspecific alarm cues in freshwater.
Figure 3: Electrophysiological responses at the olfactory epithelium of pink salmon (week 8 of CO2 exposure) in response to various amino acids (10−3 M) at different p CO 2 tensions in freshwater.
Figure 4: Time pink salmon spent in different zones (centre and thigmotaxis zone) in a novel approach test in fish reared and tested in different freshwater p CO 2 tensions.
Figure 5: Absolute growth rates in pink salmon in the first two weeks following seawater transfer at different p CO 2 tensions.
Figure 6: RMR and MMR during development in pink salmon in freshwater and following seawater transfer at different p CO 2 tensions.


  1. 1

    Dixson, D. L., Munday, P. L. & Jones, G. P. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol. Lett. 13, 68–75 (2010).

    Article  Google Scholar 

  2. 2

    Cripps, I. L., Munday, P. L. & McCormick, M. I. Ocean acidification affects prey detection by a predatory reef fish. PLoS ONE 6, e22736 (2011).

    CAS  Article  Google Scholar 

  3. 3

    Munday, P. L. et al. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc. Natl Acad. Sci. USA 106, 1848–1852 (2009).

    CAS  Article  Google Scholar 

  4. 4

    Nilsson, G. E. et al. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Clim. Change 2, 201–204 (2012).

    CAS  Article  Google Scholar 

  5. 5

    Hamilton, T. J., Holcombe, A. & Tresguerres, M. CO2-induced ocean acidification increases anxiety in rockfish via alteration of GABAA receptor functioning. Proc. R. Soc. B 281, 20132509 (2014).

    Article  Google Scholar 

  6. 6

    Jutfelt, F., de Souza, K. B., Vuylsteke, A. & Sturve, J. Behavioural disturbances in a temperate fish exposed to sustained high-CO2 levels. PLoS ONE 8, e65825 (2013).

    CAS  Article  Google Scholar 

  7. 7

    Van de Waal, D. B., Verschoor, A. M., Verspagen, J. M., van Donk, E. & Huisman, J. Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Front. Ecol. Environ. 8, 145–152 (2009).

    Article  Google Scholar 

  8. 8

    Dudgeon, D. et al. Freshwater biodiversity: Importance, threats, status and conservation challenges. Biol. Rev. 81, 163–182 (2006).

    Article  Google Scholar 

  9. 9

    Willson, M. F. & Halupka, K. C. Anadromous fish as keystone species in vertebrate communities. Conserv. Biol. 9, 489–497 (1995).

    Article  Google Scholar 

  10. 10

    Quinn, T. P. The Behavior and Ecology of Pacific Salmon and Trout (Univ. Washington Press, 2005).

    Google Scholar 

  11. 11

    Stefansson, S. O., Björnsson, B. T., Ebbesson, L. O. E. & McCormick, S. D. in Fish Larval Physiology (eds Finn, R. N. & Kapoor, B. G.) 639–681 (Science, 2008).

    Google Scholar 

  12. 12

    Neave, F., Ishida, T. & Murai, S. Salmon of the North Pacific Ocean. Part VI. Pink salmon in offshore waters. Int. North Pac. Fish. Comm. Bull. 22, 1–33 (1967).

    Google Scholar 

  13. 13

    Grant, A. et al. Growth and ionoregulatory ontogeny of wild and hatchery-raised juvenile pink salmon (Oncorhynchus gorbuscha). Can. J. Zool. 87, 221–228 (2009).

    Article  Google Scholar 

  14. 14

    Heard, W. R. in Pacific Salmon Life Histories (eds Groot, C. & Margolis, L.) 319–377 (UBC Press, 1991).

    Google Scholar 

  15. 15

    Parker, R. R. Estimations of ocean mortality rates for Pacific salmon (Oncorhynchus). J. Fish. Res. Board Can. 19, 561–589 (1962).

    Article  Google Scholar 

  16. 16

    Durkin, J. T. in Estuarine Comparisons (ed. Kennedy, V. S.) 365–376 (Academic Press, 1982).

    Book  Google Scholar 

  17. 17

    Healey, M. C. Timing and relative intensity of size-selective mortality of juvenile chum salmon (Oncorhynchus keta) during early sea life. Can. J. Fish. Aquat. Sci. 39, 952–957 (1982).

    Article  Google Scholar 

  18. 18

    Cole, J. J., Caraco, N. F., Kling, G. W. & Kratz, T. K. Carbon dioxide supersaturation in the surface waters of lakes. Science 265, 1568–1570 (1994).

    CAS  Article  Google Scholar 

  19. 19

    Raymond, P. A., Caraco, N. F. & Cole, J. J. Carbon dioxide concentration and atmospheric flux in the Hudson River. Estuaries 20, 381–390 (1997).

    CAS  Article  Google Scholar 

  20. 20

    Reum, J. C. et al. Seasonal carbonate chemistry covariation with temperature, oxygen, and salinity in a fjord estuary: Implications for the design of ocean acidification experiments. PLoS ONE 9, e89619 (2014).

    Article  Google Scholar 

  21. 21

    Prut, L. & Belzung, C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review. Eur. J. Pharmacol. 463, 3–33 (2003).

    CAS  Article  Google Scholar 

  22. 22

    Tseng, Y. et al. CO2-driven seawater acidification differentially affects development and molecular plasticity along life history of fish (Oryzias latipes). Comp. Biochem. Physiol. A 165, 119–130 (2013).

    CAS  Article  Google Scholar 

  23. 23

    Baumann, H., Talmage, S. C. & Gobler, C. J. Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nature Clim. Change 2, 38–41 (2012).

    CAS  Article  Google Scholar 

  24. 24

    Munday, P. L., Donelson, J. M., Dixson, D. L. & Endo, G. G. K. Effects of ocean acidification on the early life history of a tropical marine fish. Proc. R. Soc. B 276, 3275–3283 (2009).

    CAS  Article  Google Scholar 

  25. 25

    Pepin, P. Effect of temperature and size on development, mortality and survival rates of the pelagic early life history stages of marine fish. Can. J. Fish. Aquat. Sci. 58, 503–518 (1991).

    Article  Google Scholar 

  26. 26

    Hendry, A. P., Day, T. & Cooper, A. B. Optimal size and number of propagules: Allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness. Am. Nature 157, 387–407 (2001).

    CAS  Article  Google Scholar 

  27. 27

    Munday, P. L. et al. Replenishment of fish populations is threatened by ocean acidification. Proc. Natl Acad. Sci. USA 107, 12930–12934 (2010).

    CAS  Article  Google Scholar 

  28. 28

    Ferrari, M. C. O. et al. Putting prey and predator into the CO2 equation: Qualitative and quantitative effects of ocean acidification on predator–prey interactions. Ecol. Lett. 14, 1143–1148 (2011).

    Article  Google Scholar 

  29. 29

    Leduc, A. O., Kelly, J. M. & Brown, G. E. Detection of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: Laboratory and field tests. Oecologia 139, 318–324 (2004).

    Article  Google Scholar 

  30. 30

    Brown, G. E., Adrian, J. C. Jr, Lewis, M. G. & Tower, J. M. The effects of reduced pH on chemical alarm signalling in ostariophysan fishes. Can. J. Fish. Aquat. Sci. 59, 1331–1338 (2002).

    CAS  Article  Google Scholar 

  31. 31

    Leduc, A. O., Roh, E. & Brown, G. E. Effects of acid rainfall on juvenile Atlantic salmon (Salmo salar) antipredator behaviour: Loss of chemical alarm function and potential survival consequences during predation. Mar. Freshwat. Res. 60, 1223–1230 (2009).

    CAS  Article  Google Scholar 

  32. 32

    Lemly, D. A. & Smith, R. J. F. Effects of acute exposure to acidified water on the behavioral response of fathead minnows, Pimephales promelas, to chemical feeding stimuli. Aquat. Toxicol. 6, 25–36 (1985).

    CAS  Article  Google Scholar 

  33. 33

    Miller, G. M., Watson, S. A., Donelson, J. M., McCormick, M. I. & Munday, P. L. Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nature Clim. Change 2, 858–861 (2012).

    CAS  Article  Google Scholar 

  34. 34

    Welch, M. J., Watson, S. A., Welsh, J. Q., McCormick, M. I. & Munday, P. L. Effects of elevated CO2 on fish behaviour undiminished by transgenerational acclimation. Nature Clim. Change 4, 1086–1089 (2014).

    CAS  Article  Google Scholar 

  35. 35

    Moore, A. An electrophysiological study on the effects of pH on olfaction in mature male Atlantic salmon (Salmo salar) parr. J. Fish Biol. 45, 493–502 (1994).

    Article  Google Scholar 

  36. 36

    Shoji, T. et al. Amino acids dissolved in stream water as possible home stream odorants for masu salmon. Chem. Senses 25, 533–540 (2000).

    CAS  Article  Google Scholar 

  37. 37

    Shoji, T., Yamamoto, Y., Nishikawa, D., Kurihara, K. & Ueda, H. Amino acids in stream water are essential for salmon homing migration. Fish Physiol. Biochem. 28, 249–251 (2003).

    CAS  Article  Google Scholar 

  38. 38

    Kitamura, S. & Ikuta, K. Acidification severely suppresses spawning of hime salmon (land-locked sockeye salmon, Oncorhynchus nerka). Aquat. Toxicol. 51, 107–113 (2000).

    CAS  Article  Google Scholar 

  39. 39

    Kitamura, S. & Ikuta, K. Effects of acidification on salmonid spawning behavior. Wat. Air Soil Pollut. 130, 875–880 (2001).

    Article  Google Scholar 

  40. 40

    Ikuta, K., Munakata, A., Aida, K., Amano, M. & Kitamura, S. Effects of low pH on upstream migratory behavior in land-locked sockeye salmon Oncorhynchus nerka. Wat. Air Soil Pollut. 130, 99–106 (2001).

    CAS  Article  Google Scholar 

  41. 41

    Leduc, A. O., Munday, P. L., Brown, G. E. & Ferrari, M. C. Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: A synthesis. Phil. Trans. R. Soc. B 368, 20120447 (2013).

    Article  Google Scholar 

  42. 42

    López-Patiño, M. A., Yu, L., Cabral, H. & Zhdanova, I. V. Anxiogenic effects of cocaine withdrawal in zebrafish. Physiol. Behav. 93, 160–171 (2008).

    Article  Google Scholar 

  43. 43

    Wong, K. et al. Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behav. Brain Res. 208, 450–457 (2010).

    CAS  Article  Google Scholar 

  44. 44

    López Patiño, M. A., Yu, L., Yamamoto, B. K. & Zhdanova, I. V. Gender differences in zebrafish responses to cocaine withdrawal. Physiol. Behav. 95, 36–47 (2008).

    Article  Google Scholar 

  45. 45

    Raymond, P. A. et al. Global carbon dioxide emissions from inland waters. Nature 503, 355–359 (2013).

    CAS  Article  Google Scholar 

  46. 46

    Park, P. K., Gordon, L. I., Hager, S. W. & Cissell, M. C. Carbon dioxide partial pressure in the Columbia River. Science 166, 867–868 (1969).

    CAS  Article  Google Scholar 

  47. 47

    Evans, W., Hales, B. & Strutton, P. G. Seasonal cycle of surface ocean pCO2 on the Oregon shelf. J. Geophys. Res. 116, C05012 (2011).

    Google Scholar 

  48. 48

    Hales, B., Takahashi, T. & Bandstra, L. Atmospheric CO2 uptake by a coastal upwelling system. Glob. Biogeochem. Cycles 19, GB1009 (2005).

    Article  Google Scholar 

  49. 49

    Frieder, C. A., Nam, S. H., Martz, T. R. & Levin, L. A. High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9, 3917–3930 (2012).

    CAS  Article  Google Scholar 

  50. 50

    Marliave, J. B., Gibbs, C. J., Gibbs, D. M., Lamb, A. O. & Young, S. J. in Biodiversity Loss in a Changing Planet (eds Grillo, O. & Venora, G.) 49–74 (In Tech, 2011).

    Google Scholar 

  51. 51

    Healy, T. M. & Schulte, P. M. Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Physiol. Biochem. Zool. 85, 107–119 (2012).

    CAS  Article  Google Scholar 

  52. 52

    Reidy, S. P., Nelson, J. A., Tang, Y. & Kerr, S. R. Post-exercise metabolic rate in Atlantic cod and its dependence upon the method of exhaustion. J. Fish Biol. 47, 377–386 (1995).

    Article  Google Scholar 

  53. 53

    Sylvestre, E. L., Lapointe, D., Dutil, J. D. & Guderley, H. Thermal sensitivity of metabolic rates and swimming performance in two latitudinally separated populations of cod, Gadus morhuaa L. J. Comp. Physiol. B 177, 447–460 (2007).

    Article  Google Scholar 

  54. 54

    Killen, S. S., Costa, I., Brown, J. A. & Gamperl, A. K. Little left in the tank: Metabolic scaling in marine teleosts and its implications for aerobic scope. Proc. R. Soc. B 274, 431–438 (2007).

    Article  Google Scholar 

  55. 55

    Wieser, W. Developmental and metabolic constraints of the scope for activity in young rainbow trout (Salmo gairdneri). J. Exp. Biol. 118, 133–142 (1985).

    Google Scholar 

  56. 56

    Peake, S. J. & Farrell, A. P. Locomotory behaviour and post-exercise physiology in relation to swimming speed, gait transition and metabolism in free-swimming smallmouth bass (Micropterus dolomieu). J. Exp. Biol. 207, 1563–1575 (2004).

    Article  Google Scholar 

  57. 57

    Clark, T. D., Sandblom, E. & Jutfelt, F. Aerobic scope measurements of fishes in an era of climate change: Respirometry, relevance and recommendations. J. Exp. Biol. 216, 2771–2782 (2013).

    Article  Google Scholar 

  58. 58

    Nendick, L. et al. Swimming performance and associated ionic disturbance of juvenile pink salmon Oncorhynchus gorbuscha determined using different acceleration profiles. J. Fish Biol. 75, 1626–1638 (2009).

    CAS  Article  Google Scholar 

  59. 59

    McDonald, D. G., McFarlane, W. J. & Milligan, C. L. Anaerobic capacity and swim performance of juvenile salmonids. Can. J. Fish. Aquat. Sci. 55, 1198–1207 (1998).

    Article  Google Scholar 

  60. 60

    McFarlane, W. J. & McDonald, D. G. Relating intramuscular fuel use to endurance in juvenile rainbow trout. Physiol. Biochem. Zool. 75, 250–259 (2002).

    CAS  Article  Google Scholar 

  61. 61

    Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl Acad. Sci. USA 104, 858–863 (2007).

    CAS  Article  Google Scholar 

Download references


We thank D. Ewart and the staff at Quinsam River Hatchery for providing us with pink salmon embryos and S. Balshine for her comments on the manuscript. Special thanks to G. Fullerton, P. Tamkee, B. Gillespie and the UBC Comphy group for their help and support throughout this project. The project was financially supported by Natural Sciences and Engineering Research Council (NSERC) Discovery grants to C.J.B. and T.J.H. and a NSERC Accelerator Supplement to C.J.B.

Author information




M.O. and C.J.B. devised the study. M.O., C.J.B., J.E., T.J.H. and S.-S.Y. designed the experiments. M.O., T.J.H., J.E., E.M.L., J.G., A.J. and J.L. conducted the experiments. M.O., E.M.L., J.E. and T.J.H. developed equipment. M.O. and E.M.L. collected water samples and conducted water analyses. M.O. and C.J.B. wrote the manuscript. M.O., C.J.B., T.J.H., J.E., S.-S.Y. and D.A.C. contributed to intellectual input and edited this manuscript. All authors approved this manuscript.

Corresponding authors

Correspondence to Michelle Ou or Colin J. Brauner.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ou, M., Hamilton, T., Eom, J. et al. Responses of pink salmon to CO2-induced aquatic acidification. Nature Clim Change 5, 950–955 (2015).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing