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Advances in the aquatic sciences
RESEARCH ARTICLE

Predation of freshwater fish in environments with elevated carbon dioxide

Stephen R. Midway A C D , Caleb T. Hasler A , Tyler Wagner B and Cory D. Suski A
+ Author Affiliations
- Author Affiliations

A Department of Natural Resources and Environmental Science, University of Illinois at Urbana–Champaign, Urbana, IL 61801, USA.

B U.S. Geological Survey, Pennsylvania Cooperative Fish & Wildlife Research Unit, Pennsylvania State University, University Park, PA 16802, USA.

C Present address: Department of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, LA 70820, USA.

D Corresponding author. Email: smidway@lsu.edu

Marine and Freshwater Research 68(9) 1585-1592 https://doi.org/10.1071/MF16156
Submitted: 28 April 2016  Accepted: 27 November 2016   Published: 15 February 2017

Abstract

Carbon dioxide (CO2) in fresh-water environments is poorly understood, yet in marine environments CO2 can affect fish behaviour, including predator–prey relationships. To examine changes in predator success in elevated CO2, we experimented with predatory Micropterus salmoides and Pimephales promelas prey. We used a two-factor fully crossed experimental design; one factor was 4-day (acclimation) CO2 concentration and the second factor CO2 concentration during 20-min predation experiments. Both factors had three treatment levels, including ambient partial pressure of CO2 (pCO2; 0–1000 μatm), low pCO2 (4000–5000 μatm) and high pCO2 (8000–10 000 μatm). Micropterus salmoides was exposed to both factors, whereas P. promelas was not exposed to the acclimation factor. In total, 83 of the 96 P. promelas were consumed (n = 96 trials) and we saw no discernible effect of CO2 on predator success or time to predation. Failed strikes and time between failed strikes were too infrequent to model. Compared with marine systems, our findings are unique in that we not only saw no changes in prey capture success with increasing CO2, but we also used CO2 treatments that were substantially higher than those in past experiments. Our work demonstrated a pronounced resiliency of freshwater predators to elevated CO2 exposure, and a starting point for future work in this area.

Additional keywords: climate change, predator–prey dynamics, Micropterus salmoides, Pimephales promelas.


References

Allan, B. J. M., Domenici, P., McCormick, M. I., Watson, S.-A., and Munday, P. L. (2013). Elevated CO2 affects predator–prey interactions through altered performance. PLoS One 8, e58520–e58527.
Elevated CO2 affects predator–prey interactions through altered performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlyjs7c%3D&md5=9c06460368498a79356473df64b21fcbCAS |

Baumann, H., Wallace, R. B., Tagliaferri, T., and Gobler, C. J. (2015). Large natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales. Estuaries and Coasts 38, 220–231.
Large natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXit1Gitbk%3D&md5=b34084c544192ce69178e57b03125877CAS |

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 |

Butman, D., and Raymond, P. A. (2011). Significant efflux of carbon dioxide from streams and rivers in the United States. Nature Geoscience 4, 1–4.

Caldeira, K., and Wickett, M. E. (2003). Oceanography: anthropogenic carbon and ocean pH. Nature 425, 365.
Oceanography: anthropogenic carbon and ocean pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2ktrs%3D&md5=a8b1637cd17d0e707c43d3c5cfcad0d3CAS |

Chivers, D. P., McCormick, M. I., Nilsson, G. E., Munday, P. L., Watson, S.-A., Meekan, M. G., Mitchell, M. D., Corkill, K. C., and Ferrari, M. C. O. (2014). Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference. Global Change Biology 20, 515–522.
Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference.Crossref | GoogleScholarGoogle Scholar |

Claireaux, G., and Lefrançois, C. (2007). Linking environmental variability and fish performance: integration through the concept of scope for activity. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 362, 2031–2041.
Linking environmental variability and fish performance: integration through the concept of scope for activity.Crossref | GoogleScholarGoogle Scholar |

Clements, J. C., and Hunt, H. L. (2015). Marine animal behaviour in a high CO2 ocean. Marine Ecology Progress Series 536, 259–279.
Marine animal behaviour in a high CO2 ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmvFGmt7Y%3D&md5=e1c42c72077e4eb7c0576f9c7d50efe6CAS |

Clements, K. D., and Raubenheimer, D. (2006). Feeding and nutrition. In ‘The Physiology of Fishes’. (Eds D. H. Evans, and J. B. Claiborne.) pp. 47–82. (CRC Press: Boca Raton, FL.)

Cole, J. J., Caraco, N. F., Kling, G. W., and Kratz, T. K. (1994). Carbon-dioxide supersaturation in the surface waters of lakes. Science 265, 1568–1570.
Carbon-dioxide supersaturation in the surface waters of lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmtFagsrc%3D&md5=8660fc7657877d6a387cdb1a9e86b46dCAS |

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–e22737.
Ocean acidification affects prey detection by a predatory reef fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVyks7nO&md5=257899c1b6984ef66f95608ada1ebbf2CAS |

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 |

Dixson, D. L., Jennings, A. R., Atema, J., and Munday, P. L. (2015). Odor tracking in sharks is reduced under future ocean acidification conditions. Global Change Biology 21, 1454–1462.
Odor tracking in sharks is reduced under future ocean acidification conditions.Crossref | GoogleScholarGoogle Scholar |

Fabry, V. J., Seibel, B. A., Feely, R. A., and Orr, J. C. (2008). Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65, 414–432.
Impacts of ocean acidification on marine fauna and ecosystem processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFegtL4%3D&md5=1ad04d423654ec22c7d38f88230ebe6cCAS |

Ferrari, S., and Cribari-Neto, F. (2004). Beta regression for modelling rates and proportions. Journal of Applied Statistics 31, 799–815.
Beta regression for modelling rates and proportions.Crossref | GoogleScholarGoogle Scholar |

Ferrari, M. C. O., McCormick, M. I., Munday, P. L., Meekan, M. G., Dixson, D. L., Lonnstedt, Ö., 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., Lonnstedt, Ö., 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 |

Ferrari, M. C. O., Munday, P. L., Rummer, J. L., McCormick, M. I., Corkill, K., Watson, S.-A., Allan, B. J. M., Meekan, M. G., and Chivers, D. P. (2015). Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities. Global Change Biology 21, 1848–1855.
Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities.Crossref | GoogleScholarGoogle Scholar |

Goldstein, R. M. (1993). Size selection of prey by young largemouth bass. Proceedings of the Southeastern Association of Fish and Wildlife Agencies 47, 596–604.

Green, L., and Jutfelt, F. (2014). Elevated carbon dioxide alters the plasma composition and behaviour of a shark. Biology Letters 10, 20140538.
Elevated carbon dioxide alters the plasma composition and behaviour of a shark.Crossref | GoogleScholarGoogle Scholar |

Hambright, K. D. (1991). Experimental-analysis of prey selection by largemouth bass: role of predator mouth width and prey body depth. Transactions of the American Fisheries Society 120, 500–508.
Experimental-analysis of prey selection by largemouth bass: role of predator mouth width and prey body depth.Crossref | GoogleScholarGoogle Scholar |

Hamilton, T. J., Holcombe, A., and Tresguerres, M. (2013). CO2-induced ocean acidification increases anxiety in rockfish via alteration of GABAA receptor functioning. Proceedings. Biological Sciences 281, 20132509.
CO2-induced ocean acidification increases anxiety in rockfish via alteration of GABAA receptor functioning.Crossref | GoogleScholarGoogle Scholar |

Hasler, C. T., Butman, D., Jeffrey, J. D., and Suski, C. D. (2016a). Freshwater biota and rising pCO2? Ecology Letters 19, 98–108.
Freshwater biota and rising pCO2?Crossref | GoogleScholarGoogle Scholar |

Hasler, C. T., Midway, S. R., Jeffrey, J. D., Tix, J., Sullivan, C., and Suski, C. D. (2016b). Exposure to elevated pCO2 alters diel movement patterns of largemouth bass over short time scales. Freshwater Biology 61, 1590–1600.
Exposure to elevated pCO2 alters diel movement patterns of largemouth bass over short time scales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1yhtbzP&md5=e4d3f2eb8864ef74ed0b4fec73d791b8CAS |

Heuer, R. M., and Grosell, M. (2014). Physiological impacts of elevated carbon dioxide and ocean acidification on fish. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 307, R1061–R1084.
Physiological impacts of elevated carbon dioxide and ocean acidification on fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVeitLfN&md5=b43f44a71fdab5b951e82f9a7e405694CAS |

Ishimatsu, A., Kikkawa, T., Hayashi, M., Lee, K. S., and Kita, J. (2004). Effects of CO2 on marine fish: larvae and adults. Journal of Oceanography 60, 731–741.
Effects of CO2 on marine fish: larvae and adults.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntVSjsLk%3D&md5=9eacbc15aeee78861cc1b857d5e4314eCAS |

Iwama, G. K., McGeer, J. C., and Pawluk, M. P. (1989). The effects of five fish anaesthetics on acid–base balance, hematocrit, blood gases, cortisol, and adrenaline in rainbow trout. Canadian Journal of Zoology 67, 2065–2073.
The effects of five fish anaesthetics on acid–base balance, hematocrit, blood gases, cortisol, and adrenaline in rainbow trout.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlsFSrurc%3D&md5=e37b2850735cc5fb6248cd4cba7ef8b0CAS |

Johnson, M. S., Billett, M. F., Dinsmore, K. J., Wallin, M., Dyson, K. E., and Jassal, R. S. (2010). Direct and continuous measurement of dissolved carbon dioxide in freshwater aquatic systems: method and applications. Ecohydrology 3, 68–78.
| 1:CAS:528:DC%2BC3cXksl2msL4%3D&md5=5e772da1166ddaa2a54035b7a2fb4dabCAS |

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 |

Jutfelt, F., and Hedgärde, M. (2015). Juvenile Atlantic cod behavior appears robust to near-future CO2 levels. Frontiers in Zoology 12, 11.
Juvenile Atlantic cod behavior appears robust to near-future CO2 levels.Crossref | GoogleScholarGoogle Scholar |

Kates, D., Dennis, C., Noatch, M. R., Suski, C. D., and MacLatchy, D. L. (2012). Responses of native and invasive fishes to carbon dioxide: potential for a nonphysical barrier to fish dispersal. Canadian Journal of Fisheries and Aquatic Sciences 69, 1748–1759.
Responses of native and invasive fishes to carbon dioxide: potential for a nonphysical barrier to fish dispersal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFCnsr%2FO&md5=968934947f37acc426806c5ddad111feCAS |

Kitchell, J. F., Eby, L. A., He, X., Schindler, D. E., and Wright, R. A. (1994). Predator–prey dynamics in an ecosystem context. Journal of Fish Biology 45, 209–226.
Predator–prey dynamics in an ecosystem context.Crossref | GoogleScholarGoogle Scholar |

Leduc, A. O. H. C., Ferrari, M. C. O., Kelly, J. M., and Brown, G. E. (2004). Learning to recognize novel predators under weakly acidic conditions: the effects of reduced pH on acquired predator recognition by juvenile rainbow trout. Chemoecology 14, 107–112.
Learning to recognize novel predators under weakly acidic conditions: the effects of reduced pH on acquired predator recognition by juvenile rainbow trout.Crossref | GoogleScholarGoogle Scholar |

Lima, S. L. (1998). Nonlethal effects in the ecology of predator–prey interactions. Bioscience 48, 25–34.
Nonlethal effects in the ecology of predator–prey interactions.Crossref | GoogleScholarGoogle Scholar |

Maberly, S. C. (1996). Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshwater Biology 35, 579–598.
Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltF2lu78%3D&md5=272c846da44a9e58ebafe2b1c9f840cbCAS |

Marking, L. L., and Meyer, F. P. (1985). Are better anesthetics needed in fisheries? Fisheries 10, 2–5.
Are better anesthetics needed in fisheries?Crossref | GoogleScholarGoogle Scholar |

McNeil, B. I., and Sasse, T. P. (2016). Future ocean hypercapnia driven by anthropogenic amplification of the natural CO2 cycle. Nature 529, 383–386.
Future ocean hypercapnia driven by anthropogenic amplification of the natural CO2 cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1Oisr0%3D&md5=d5d4b6cfbe3104328dc3452bc053aa9eCAS |

Munday, P. L., Jones, G. P., Pratchett, M. S., and Williams, A. J. (2008). Climate change and the future for coral reef fishes. Fish and Fisheries 9, 261–285.
Climate change and the future for coral reef fishes.Crossref | GoogleScholarGoogle Scholar |

Munday, P. L., Dixson, D. L., McCormick, M. I., Meekan, M., Ferrari, M. C. O., and Chivers, D. P. (2010). Replenishment of fish populations is threatened by ocean acidification. Proceedings of the National Academy of Sciences of the United States of America 107, 12930–12934.
Replenishment of fish populations is threatened by ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsVagur4%3D&md5=2e04a309508e46ad1821b58006c52077CAS |

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=adb051d9690fe90415cee68cc2eadb4eCAS |

Näslund, J., Lindström, E., Lai, F., and Jutfelt, F. (2015). Behavioural responses to simulated bird attacks in marine three-spined sticklebacks after exposure to high CO2 levels. Marine and Freshwater Research 66, 877–885.
Behavioural responses to simulated bird attacks in marine three-spined sticklebacks after exposure to high CO2 levels.Crossref | GoogleScholarGoogle Scholar |

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=df2492071998aeb5af7b7a4dd5a2e4dbCAS |

Noatch, M. R., and Suski, C. D. (2012). Non-physical barriers to deter fish movements. Environmental Reviews 20, 71–82.
Non-physical barriers to deter fish movements.Crossref | GoogleScholarGoogle Scholar |

Ou, M., Hamilton, T. J., Eom, J., Lyall, E. M., Gallup, J., Jiang, A., Lee, J., Close, D. A., Yun, S.-S., and Brauner, C. J. (2015). Responses of pink salmon to CO2-induced aquatic acidification. Nature Climate Change 5, 950–955.
Responses of pink salmon to CO2-induced aquatic acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFCjsrfM&md5=771857b046225cb2050eb617651dacfdCAS |

Perry, S. F., and Gilmour, K. M. (2002). Sensing and transfer of respiratory gases at the fish gill. The Journal of Experimental Zoology 293, 249–263.
Sensing and transfer of respiratory gases at the fish gill.Crossref | GoogleScholarGoogle Scholar |

Phillips, J. C., McKinley, G. A., Bennington, V., Bootsma, H. A., Pilcher, D. J., Sterner, R. W., and Urban, N. R. (2015). The potential for CO2-induced acidification in freshwater: a great lakes case study. Oceanography 28, 136–145.
The potential for CO2-induced acidification in freshwater: a great lakes case study.Crossref | GoogleScholarGoogle Scholar |

Pilcher, D. J., McKinley, G. A., Bootsma, H. A., and Bennington, V. (2015). Physical and biogeochemical mechanisms of internal carbon cycling in Lake Michigan. Journal of Geophysical Research: Oceans 120, 2112–2128.
| 1:CAS:528:DC%2BC2MXmsFygsL8%3D&md5=e7d606f81f46c92a657f60fc13664924CAS |

Pistevos, J. C., Nagelkerken, I., Rossi, T., Olmos, M., and Connell, S. D. (2015). Ocean acidification and global warming impair shark hunting behaviour and growth. Scientific Reports 5, 16293.
Ocean acidification and global warming impair shark hunting behaviour and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVequ7nN&md5=a6e6e07a9189af647bd9c325199f779aCAS |

Rahel, F. J., and Nutzman, J. W. (1994). Foraging in a lethal environment: fish predation in hypoxic waters of a stratified lake. Ecology 75, 1246.
Foraging in a lethal environment: fish predation in hypoxic waters of a stratified lake.Crossref | GoogleScholarGoogle Scholar |

Regan, M. D., Turko, A. J., Heras, J., Andersen, M. K., Lefevre, S., Wang, T., Bayley, M., Brauner, C. J., Huong, d.T.T., Phuong, N. T., and Nilsson, G. E. (2016). Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels. The Journal of Experimental Biology 219, 109–118.
Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels.Crossref | GoogleScholarGoogle Scholar |

Solomon, S., Qin, D., and Manning, M. (2007). ‘Climate Change 2007: the Physical Science Basis: Working Group I Contribution to the Fourth Assessment Report of the IPCC (Vol. 4).’ (Cambridge University Press: New York, NY, USA.)

Sundin, J., and Jutfelt, F. (2016). 9–28 d of exposure to elevated pCO2 reduces avoidance of predator odour but had no effect on behavioural lateralization or swimming activity in a temperate wrasse (Ctenolabrus Rupestris). ICES Journal of Marine Science 73, 620–632.
9–28 d of exposure to elevated pCO2 reduces avoidance of predator odour but had no effect on behavioural lateralization or swimming activity in a temperate wrasse (Ctenolabrus Rupestris).Crossref | GoogleScholarGoogle Scholar |