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RESEARCH ARTICLE

Behavioural responses to simulated bird attacks in marine three-spined sticklebacks after exposure to high CO2 levels

Joacim Näslund A D , Erik Lindström A , Floriana Lai B and Fredrik Jutfelt A C
+ Author Affiliations
- Author Affiliations

A Department of Biological and Environmental Sciences, University of Gothenburg, PO Box 463, SE-405 30 Gothenburg, Sweden.

B Department of Biosciences, University of Oslo, PO Box 1066 Blindern, N-0316 Oslo, Norway.

C The Lovén Centre Kristineberg, Kristineberg 566, SE-451 78 Fiskebäckskil, Sweden.

D Corresponding author. Email: joacim.naslund@bioenv.gu.se

Marine and Freshwater Research 66(10) 877-885 https://doi.org/10.1071/MF14144
Submitted: 30 May 2014  Accepted: 21 November 2014   Published: 19 March 2015

Abstract

The rising partial pressure of CO2 (pCO2) in oceanic water, termed ocean acidification, is an impending threat to marine life and has previously been reported to affect several aspects of fish behaviour. We evaluated the behavioural response to a simulated avian predator attack and lateralisation in three-spined sticklebacks (Gasterosteus aculeatus) after 10 and 20 days of exposure to present day pCO2 (400 μatm) or elevated pCO2 (1000 μatm). We show that elevated pCO2 lead to reduced behavioural lateralisation. However, no major differences in the sheltering response after an overhead avian attack were observed; fish from both treatments exhibited similar and strong responses. Compared with fish exposed to high pCO2, the control fish took longer time to freeze (i.e. stop moving) after attack at Day 20 but not Day 10. The freezing duration was significantly reduced between Day 10 and Day 20 in elevated pCO2, whereas no such reduction was observed in the control-group. However, no significant differences between treatment groups were detected at Day 20. These results demonstrate that behaviour is indeed altered by high CO2 levels, although the general responses to avian predation stimuli remain similar to those of unexposed fish, indicating that some predator avoidance behaviours of three-spined sticklebacks are robust to environmental disturbance.

Additional keywords: carbon dioxide, gasterosteidae, global change, lateralisation, ocean acidification, predator avoidance.


References

Barber, I., Walker, P., and Svensson, P. A. (2004). Behavioural responses to simulated avian predation in female three spined sticklebacks: the effect of experimental Schistocephalus solidus infections. Behaviour 141, 1425–1440.
Behavioural responses to simulated avian predation in female three spined sticklebacks: the effect of experimental Schistocephalus solidus infections.Crossref | GoogleScholarGoogle Scholar |

Bignami, S., Sponaugle, S., and Cowen, R. K. (2013). Response to ocean acidification in larvae of a large tropical marine fish, Rachycentron canadum. Global Change Biology 19, 996–1006.
Response to ocean acidification in larvae of a large tropical marine fish, Rachycentron canadum.Crossref | GoogleScholarGoogle Scholar | 23504878PubMed |

Bisazza, A., and Brown, C. (2011). Lateralization of cognitive functions in fish. In ‘Fish Cognition and Behavior’, 2nd edn. (Eds C. Brown, K. Laland and J. Krause.) pp. 298–324. (Blackwell Publishing Ltd.: Oxford, UK.)

Bisazza, A., Faccin, L., Pignatti, R., and Vallortigara, G. (1998). Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual maturation. Behavioural Brain Research 91, 157–164.
Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3jslGmuw%3D%3D&md5=fbf59fb622537027fad95266d88496d4CAS | 9578448PubMed |

Briffa, M., de la Haye, K., and Munday, P. L. (2012). High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Marine Pollution Bulletin 64, 1519–1528.
High CO2 and marine animal behaviour: potential mechanisms and ecological consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtV2ntbjF&md5=0e3957ef8a8f6412cab82bcc4c8cbedcCAS | 22749063PubMed |

Checkley, D. M., Dickson, A. G., Takahashi, M., Radich, J. A., Eisenkolb, N., and Asch, R. (2009). Elevated CO2 enhances otolith growth in young fish. Science 324, 1683.
Elevated CO2 enhances otolith growth in young fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsFOmsL0%3D&md5=3b811b9781d730cb4d2cc3a562e08582CAS | 19556502PubMed |

Chung, W.-S., Marshall, N. J., Watson, S.-A., Munday, P. L., and Nilsson, G. E. (2014). Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors. The Journal of Experimental Biology 217, 323–326.
Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntlWht7s%3D&md5=fd765920316f0f0c9947e34e8a14c21fCAS | 24477607PubMed |

Cripps, I. L., Munday, P. L., and McCormick, M. I. (2011). Ocean acidification affects prey detection by a predatory reef fish. PLoS ONE 6, e22736.
Ocean acidification affects prey detection by a predatory reef fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVyks7nO&md5=5a30d758e94faf1e424f8b5b39c795ccCAS | 21829497PubMed |

DeFaveri, J., and Merilä, J. (2013). Variation in age and size in Fennoscandian three-spined sticklebacks (Gasterosteus aculeatus). PLoS ONE 8, e80866.
Variation in age and size in Fennoscandian three-spined sticklebacks (Gasterosteus aculeatus).Crossref | GoogleScholarGoogle Scholar | 24260496PubMed |

Dixson, D. L., Munday, P. L., and Jones, G. P. (2010). Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecology Letters 13, 68–75.
Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues.Crossref | GoogleScholarGoogle Scholar | 19917053PubMed |

Domenici, P., Allan, B., McCormick, M. I., and Munday, P. L. (2012). Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biology Letters 8, 78–81.
Elevated carbon dioxide affects behavioural lateralization in a coral reef fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFygtbw%3D&md5=193e2fe5f147adc33de088ba18181818CAS | 21849307PubMed |

Domenici, P., Allan, B. J. M., Watson, S. A., McCormick, M. I., and Munday, P. L. (2014). Shifting from right to left: the combined effect of elevated CO2 and temperature on behavioural lateralization in a coral reef fish. PLoS ONE 9, e87969.
Shifting from right to left: the combined effect of elevated CO2 and temperature on behavioural lateralization in a coral reef fish.Crossref | GoogleScholarGoogle Scholar | 24498231PubMed |

Doney, S. C., Fabry, V. J., Feely, R. A., and Kleypas, J. A. (2009). Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1, 169–192.
Ocean acidification: the other CO2 problem.Crossref | GoogleScholarGoogle Scholar | 21141034PubMed |

Doney, S. C., Ruckelshaus, M., Duffy, J. E., Barry, J. P., Chan, F., English, C. A., Galindo, H. M., Grebmeier, J. M., Hollowed, A. B., Knowlton, N., Polovina, J., Rabalais, N. N., Sydeman, W. J., and Talley, L. D. (2012). Climate change impacts on marine ecosystems. Annual Review of Marine Science 4, 11–37.
Climate change impacts on marine ecosystems.Crossref | GoogleScholarGoogle Scholar | 22457967PubMed |

Facchin, L., Bisazza, A., and Vallortigara, G. (1999). What causes lateralization of detour behavior in fish? Evidence for assymmetries in eye use. Behavioural Brain Research 103, 229–234.
What causes lateralization of detour behavior in fish? Evidence for assymmetries in eye use.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MvktFOnuw%3D%3D&md5=4d83cbe25f63f82c5c4649fc723afefcCAS | 10513591PubMed |

Ferrari, M. C. O., McCormick, M. I., Munday, P. L., Meekan, M. G., Dixon, D. L., Lönnstedt, O., and Chivers, D. P. (2011). Putting prey and predator into the CO2 equation – qualitative and quantitative effects of ocean acidification on predator-prey interactions. Ecology Letters 14, 1143–1148.
Putting prey and predator into the CO2 equation – qualitative and quantitative effects of ocean acidification on predator-prey interactions.Crossref | GoogleScholarGoogle Scholar |

Ferrari, M. C. O., McCormick, M. I., Munday, P. L., Meekan, M. G., Dixson, D. L., Lönnstedt, O., and Chivers, D. P. (2012). Effects of ocean acidification on visual risk assessment in coral reef fishes. Functional Ecology 26, 553–558.
Effects of ocean acidification on visual risk assessment in coral reef fishes.Crossref | GoogleScholarGoogle Scholar |

Forsgren, E., Dupont, S., Jutfelt, F., and Amundsen, T. (2013). Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish. Ecology and Evolution 3, 3637–3646.
Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish.Crossref | GoogleScholarGoogle Scholar | 24198929PubMed |

Giles, N. (1981). Predation effects upon the behaviour and ecology of Scottish Gasterosteus aculeatus L. Ph.D. Thesis, University of Glasgow, Department of Zoology.

Giles, N. (1984). Development of the overhead fright response in wild and predator-naïve three-spined sticklebacks, Gasterosteus aculeatus, L. Animal Behaviour 32, 276–279.
Development of the overhead fright response in wild and predator-naïve three-spined sticklebacks, Gasterosteus aculeatus, L.Crossref | GoogleScholarGoogle Scholar |

Hamilton, T. J., Holcombe, A., and Tresguerres, M. (2014). CO2-induced ocean acidification increases anxiety in rockfish via alteration of GABAA receptor functioning. Proceedings of the Royal Society of London – B. Biological Sciences 281, 20132509.
CO2-induced ocean acidification increases anxiety in rockfish via alteration of GABAA receptor functioning.Crossref | GoogleScholarGoogle Scholar |

Harmon, J. P., and Barton, B. T. (2013). On their best behavior: how animal behavior can help determine the combined effects of species interactions and climate change. Annals of the New York Academy of Sciences 1297, 139–147.
On their best behavior: how animal behavior can help determine the combined effects of species interactions and climate change.Crossref | GoogleScholarGoogle Scholar | 23819891PubMed |

Jutfelt, F., and Hedgärde, M. (2013). Atlantic cod actively avoid CO2 and predator odour, even after long-term CO2 exposure. Frontiers in Zoology 10, 81.
Atlantic cod actively avoid CO2 and predator odour, even after long-term CO2 exposure.Crossref | GoogleScholarGoogle Scholar | 24373523PubMed |

Jutfelt, F., Bresolin de Souza, K., Vuylsteke, A., and Sturve, J. (2013). Behavioural disturbances in a temperate fish exposed to sustained high-CO2 levels. PLoS ONE 8, e65825.
Behavioural disturbances in a temperate fish exposed to sustained high-CO2 levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFWnurw%3D&md5=1a07de6c4fb38966121ea011687ed081CAS | 23750274PubMed |

Leduc, A. O. H. C., Munday, P. L., Brown, G. E., and Ferrari, M. C. O. (2013). Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 368, 20120447.
Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis.Crossref | GoogleScholarGoogle Scholar |

Lemmetyinen, R. (1973). Feeding ecology of Sterna paradisea Pontopp. and S. hirundo L. in the archipelago of southwest Finland. Annales Zoologici Fennici 10, 507–525.

Lew, M. J. (2008). On contemporaneous controls, unlikely outcomes, boxes and replacing the ‘Student’: good statistical practice in pharmacology, problem 3. British Journal of Pharmacology 155, 797–803.
On contemporaneous controls, unlikely outcomes, boxes and replacing the ‘Student’: good statistical practice in pharmacology, problem 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGhsb7J&md5=1d23f6040f4dc80aa7b49b9237dfed51CAS | 18806810PubMed |

Lönnstedt, O. M., Munday, P. L., McCormick, M. I., Ferrari, M. C. O., and Chivers, D. P. (2013). Ocean acidification and responses to predators: can sensory redundancy reduce the apparent impacts of elevated CO2 on fish? Ecology and Evolution 3, 3565–3575.
Ocean acidification and responses to predators: can sensory redundancy reduce the apparent impacts of elevated CO2 on fish?Crossref | GoogleScholarGoogle Scholar | 24223291PubMed |

Ludbrook, J., and Dudley, H. (1998). Why permutation tests are superior to t and F tests in biomedical research. The American Statistician 52, 127–132.
Why permutation tests are superior to t and F tests in biomedical research.Crossref | GoogleScholarGoogle Scholar |

Lueker, T. J., Dickson, A. G., and Keeling, C. D. (2000). Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium. Marine Chemistry 70, 105–119.
Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs1Wjsbo%3D&md5=e978363c1a1a094518da2573f3989145CAS |

Maneja, R. H., Frommel, A. Y., Browman, H. I., Clemmesen, C., Geffen, A. J., Folkvord, A., Piatkowski, U., Durif, C. M. F., Bjelland, R., and Skiftesvik, A. B. (2013). The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2. Marine Biology 160, 1963–1972.
The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1GgtbzI&md5=5bb98e957d8088fd5166818c7f9892daCAS |

McLellan, N. R., and Shutler, D. (2009). Sources of food delivered to ring-billed, herring and great black-backed gull chicks in marine environments. Waterbirds 32, 507–513.
Sources of food delivered to ring-billed, herring and great black-backed gull chicks in marine environments.Crossref | GoogleScholarGoogle Scholar |

Munday, P. L., Pratchett, M. S., Dixon, D. L., Donelson, J. M., Endo, G. G. K., Reynolds, A. D., and Knuckley, R. (2013). Elevated CO2 affects the behavior of an ecologically and economically important coral reef fish. Marine Biology 160, 2137–2144.
Elevated CO2 affects the behavior of an ecologically and economically important coral reef fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Ggu7rL&md5=f7e5947024ae892059af854d86978b35CAS |

Munday, P. L., Cheal, A. J., Dixson, D. L., Rummer, J. L., and Fabricius, K. E. (2014). Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps. Nature Climate Change 4, 487–492.
Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtVCgtbg%3D&md5=1d6939f1c0c1456df9de03a994aa3542CAS |

Nilsson, G. E., Dixson, D. L., Domenici, P., McCormick, M. I., Sørensen, C., Watson, S.-A., and Munday, P. L. (2012). Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Climate Change 2, 201–204.
Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVentLc%3D&md5=e43788b3bf922ec25fb92e9826d5fbb7CAS |

Popper, A. N., Ramcharitar, J., and Campana, S. E. (2005). Why otoliths? Insights from inner ear physiology and fisheries biology. Marine and Freshwater Research 56, 497–504.
Why otoliths? Insights from inner ear physiology and fisheries biology.Crossref | GoogleScholarGoogle Scholar |

Sarazin, G., Michard, G., and Prevot, F. (1999). A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples. Water Research 33, 290–294.
A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVOqur0%3D&md5=b371c9fcb408f2016ff574643b20a225CAS |

Schade, F. M., Clemmesen, C., and Wegner, K. M. (2014). Within- and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (Gasterosteus aculeatus). Marine Biology 161, 1667–1676.
Within- and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (Gasterosteus aculeatus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnvF2ls78%3D&md5=2b83fb1a81114de6892431c96dd0b8f8CAS |

Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K., Tignor, M. M. B., and Miller, H. L. (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.’ (Cambridge University Press: Cambridge, UK, and New York.)

Thomsen, J., and Melzner, F. (2010). Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Marine Biology 157, 2667–2676.
Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis.Crossref | GoogleScholarGoogle Scholar |

Wendeln, H., and Becker, P. H. (1996). Body mass change in breeding common terns Sterna hirundo. Bird Study 43, 85–95.
Body mass change in breeding common terns Sterna hirundo.Crossref | GoogleScholarGoogle Scholar |

Whoriskey, F. G., and FitzGerald, G. J. (1985). The effects of bird predation on an estuarine stickleback (Pisces: Gasterosteidae) community. Canadian Journal of Zoology 63, 301–307.
The effects of bird predation on an estuarine stickleback (Pisces: Gasterosteidae) community.Crossref | GoogleScholarGoogle Scholar |

Wootton, R. J. (1984). ‘A Functional Biology of Sticklebacks’. (University of California Press: Berkeley, CA.)