Skip to main content
SpringerLink
Log in

Temperature dependent effects of carbon dioxide on avoidance behaviors in bigheaded carps

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Effective behavioral deterrents are needed to prevent aquatic invasive species from entering novel ecosystems. One deterrent strategy that shows promise is elevated carbon dioxide (CO2) concentrations in water which can alter the behavior of freshwater fishes, including invasive bigheaded carps (Hypophthalmichthys spp.). However, few studies have evaluated behavioral responses to elevated CO2 concentrations at different water temperatures. The objective of this study was to quantify CO2 concentrations needed to achieve avoidance (voluntary response) and narcosis (involuntary response observed by loss of equilibrium) behaviors in silver carp (H. molitrix) and bighead carp (H. nobilis) at 5, 15, and 25 °C. Overall, silver carp and bighead carp displayed avoidance and narcosis behaviors to CO2 at each water temperature, however bighead carp responded at higher CO2 concentrations than silver carp. Behavioral avoidance and narcosis were observed at approximately 40% lower CO2 concentrations in 5 °C water relative to 25 °C suggesting considerable influence of water temperature on a CO2 stimulus for both species. Results indicate that fluctuating water temperature (e.g., spatial and temporal variation across management sites) can influence how fish respond to elevated CO2, and may usefully be considered when applying CO2 as a behavioral deterrent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • American Sportfishing Association (2008) Today’s angler: a statistical profile of anglers, their targeted species and expenditures. American Sportfishing Association, Alexandria

    Google Scholar 

  • Anscombe FJ, Tukey JW (1963) The examination and analysis of residuals. Technometrics 5:141–160

    Article  Google Scholar 

  • APHA (1998) Standard methods for the examination of water and wastewater. American Public Health Association, District of Columbia, Washington

    Google Scholar 

  • Brauhn JL, Schoettger RA (1975) Acquisition and culture of research fish: Rainbow Trout, Fathead Minnows, Channel Catfish, and Bluegills. National Environmental Research Center, Office of Research and Development, U.S. Environmental Protection Agency, Project EPA-660/3-75-011, Final Report, Corvallis

  • Cudmore B, Mandrak NE, Dettmers J, Chapman DC, Kolar CS (2012) Binational ecological risk assessment of bigheaded carps (Hypophthalmichthys spp.) for the Great Lakes basin. DFO Canadian Science Advisory Secretariat Research Document 2011/114

  • Cupp AR, Erickson R, Fredricks KT, Swyers N, Hatton T, Amberg J (2016) Responses of invasive silver and bighead carp to a carbon dioxide barrier in outdoor ponds. Can J Fish Aquat Sci 74:297–305. https://doi.org/10.1139/cjfas-2015-0472

    Article  CAS  Google Scholar 

  • Cupp AR, Schreier TM, Schleis SM (2017a) Live transport of yellow perch and nile perch in AQUI-S 20E (10% Eugenol) at high loading densities. N Am J Aquac 79:176–182. https://doi.org/10.1080/15222055.2017.1281853

    Article  Google Scholar 

  • Cupp AR, Woiak Z, Erickson RA, Amberg JJ, Gaikowski MP (2017b) Carbon dioxide as an under-ice lethal control for invasive fishes. Biol Invasions 19(9):2543–2552. https://doi.org/10.1007/s10530-017-1462-9

    Article  Google Scholar 

  • Cupp AR, Tix JA, Smerud JR, Erickson R, Fredricks KT, Amberg JJ, Suski CD, Wakeman R (2017c) Using dissolved carbon dioxide to alter the behavior of invasive round goby. Manag Biol Invasions 8(4):567–574. https://doi.org/10.3391/mbi.2017.8.4.12

    Article  Google Scholar 

  • Davison W (1984) Temperature acclimation in the rockfish Acanthoclinus quadridactylus. N Z J Zool 11(3):329–335. https://doi.org/10.1080/03014223.1984.10428245

    Article  Google Scholar 

  • Dennis CE, Adhikari S, Suski CD (2015) Molecular and behavioral responses of early-life stage fishes to elevated carbon dioxide. Biol Invasion 17:3133–3151. https://doi.org/10.1007/s10530-015-0941-0

    Article  Google Scholar 

  • Donaldson MR, Amberg J, Adhikari S, Cupp A, Jensen N, Romine J, Wright A, Gaikowski M, Suski CD (2016) Carbon dioxide as a tool to deter the movement of invasive bigheaded carps. Trans Am Fish Soc 145:657–670. https://doi.org/10.1080/00028487.2016.1143397

    Article  CAS  Google Scholar 

  • Emerson K, Russo RC, Lund RE, Thurston RV (1975) Aqueous ammonia equilibrium calculations: effects of pH and temperature. J Fish Res Board Can 32:2379–2383. https://doi.org/10.1139/f75-274

    Article  CAS  Google Scholar 

  • Finnoff D, Shogren JF, Leung B, Lodge D (2007) Take a risk: preferring prevention over control of biological invaders. Ecol Econ 62:216–222. https://doi.org/10.1016/j.ecolecon.2006.03.025

    Article  Google Scholar 

  • Gilmour KM (2001) The CO2/pH ventilatory drive in fish. Comp Biochem Physiol A Mol Integr Physiol 130:219–240. https://doi.org/10.1016/S1095-6433(01)00391-9

    Article  CAS  PubMed  Google Scholar 

  • Gilmour KM, Perry SF (2007) Bronchial chemoreceptor regulation of cardiorespiratory function. In: Hara TJ, Zielinski B (eds) Fish physiology 25: sensory systems neuroscience. Academic Press, San Diego, pp 97–151

    Google Scholar 

  • Gilmour KM, DiBattista J, Thomas J (2005) Physiological causes and consequences of social status in salmonid fish. Integr Comp Biol 45:263–273. https://doi.org/10.1093/icb/45.2.263

    Article  CAS  PubMed  Google Scholar 

  • Hannan KD, Jeffrey JD, Hasler CT, Suski CD (2016) The response of two species of unionid mussels to extended exposure to elevated carbon dioxide. Comp Biochem Physiol A Mol Integr Physiol 201:173–181. https://doi.org/10.1016/j.cbpa.2016.07.009

    Article  CAS  PubMed  Google Scholar 

  • Hasler CT, Midway SR, Jeffrey JD, Tix JA, Sullivan C (2016) Exposure to elevated pCO2 alters post-treatment diel movement patterns of largemouth bass over short time scales. Freshw Biol 61:1590–1600. https://doi.org/10.1111/fwb.12805

    Article  CAS  Google Scholar 

  • Hasler CT, Bouyoucos IA, Suski CD (2017) Tolerance to hypercarbia is repeatable and related to a component of the metabolic phenotype in a freshwater fish. Physiol Biochem Zool 90:583–587. https://doi.org/10.1086/693376

    Article  PubMed  Google Scholar 

  • Heisler N (1989) Interactions between gas exchange, metabolism, and ion transport in animals: an overview. Can J Zool 67:2923–2935. https://doi.org/10.1139/z89-415

    Article  CAS  Google Scholar 

  • Heisler N, Neumann P, Holeton GF (1980) Mechanisms of acid–base adjustment in dogfish (Scyliorhinus stellaris) subjected to longterm temperature acclimation. J Exp Biol 85:89–98

    CAS  Google Scholar 

  • Helsel DR (2012) Statistics for censored environmental data using Minitab and R, 2nd edn. Wiley, Hoboken

    Google Scholar 

  • Heuer RM, Grosell M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am J Physiol Regul Integr Comp Physiol 307(9):R1061–R1084

    Article  CAS  Google Scholar 

  • Hiromasa Y, Fumio K, Masao K (1994) The relationship between the EEG and brain pH in carp, Cyprinus carpio, subjected to environmental hypercapnia at an anesthetic level. Comp Biochem Physiol A Physiol 107:307–312. https://doi.org/10.1016/0300-9629(94)90386-7

    Article  Google Scholar 

  • Irons K, Sass G, McClelland M, Stafford J (2007) Reduced condition factor of two native fish species coincident with invasion of non-native Asian carps in the Illinois River, USA Is this evidence for competition and reduced fitness? J Fish Biol 71:258–273. https://doi.org/10.1111/j.1095-8649.2007.01670.x

    Article  Google Scholar 

  • Iwama GK, McGeer JC, Pawluk MP (1989) The effects of five fish anaesthetics on acid-base balance, hematocrit, blood gases, cortisol, and adrenaline in rainbow trout. Can J Zool 67:2065–2073. https://doi.org/10.1139/z89-294

    Article  CAS  Google Scholar 

  • Kates D, Dennis C, Noatch MR, Suski CD (2012) Responses of native and invasive fishes to carbon dioxide: potential for a nonphysical barrier to fish dispersal. Can J Fish Aquat Sci 69:1748–1759. https://doi.org/10.1139/f2012-102

    Article  CAS  Google Scholar 

  • Kolar CS, Chapman DC, Courtenay WR Jr, Housel CM, Williams JD, Jennings DP (2007) Bigheaded carps—a biological synopsis and environmental risk assessment, vol 33. Special Publication. American Fisheries Society, Bethesda

    Google Scholar 

  • Millero FJ (1979) The thermodynamics of the carbonate system in seawater. Geochimica et Cosmochimica Acta 43 (10):1651–1661

    Article  CAS  Google Scholar 

  • Moy PB, Polls I, Dettmers JM (2011) The Chicago sanitary and ship canal aquatic nuisance species dispersal barrier. In: Chapman DC, Hoff MH (eds) Invasive Asian carps in North America. American Fisheries Society, Bethesda, pp 127–137

    Google Scholar 

  • Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sørensen C, Watson S-A, Munday PL (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Chang 2(3):201–204

    Article  CAS  Google Scholar 

  • Noatch MR, Suski CD (2012) Non-physical barriers to deter fish movements. Environ Rev 20:71–82. https://doi.org/10.1139/a2012-001

    Article  Google Scholar 

  • Parker AD, Glover DC, Finney ST, Rogers PB, Stewart JG, Simmonds RL (2015) Direct observations of fish incapacitation rates at a large electrical fish barrier in the Chicago Sanitary and Ship Canal. J Great Lakes Res 41:396–404. https://doi.org/10.1016/j.jglr.2015.03.004

    Article  Google Scholar 

  • Perry SF, Gilmour KM (2006) Acid–base balance and CO2 excretion in fish: unanswered questions and emerging models. Respir Physiol Neurobiol 154:199–215. https://doi.org/10.1016/j.resp.2006.04.010

    Article  CAS  PubMed  Google Scholar 

  • Perry SF, Reid SG (2002) Cardiorespiratory adjustments during hypercarbia in rainbow trout (Oncorhynchus mykiss) are initiated by external CO2 receptors on the first gill arch. J Exp Biol 205:3357–3365

    CAS  PubMed  Google Scholar 

  • R Core Team (2016) R—a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rasmussen JL, Regier HA, Sparks RE, Taylor WW (2011) Dividing the waters: the case for hydrologic separation of the North American Great Lakes and Mississippi River Basins. J Great Lakes Res 37(3):588–592

    Article  Google Scholar 

  • Reynolds JB (1996) Electrofishing. In: Murphy BR, Willis DW (eds) Fisheries techniques, 2nd edn. American Fisheries Society, Bethesda, pp 221–253

    Google Scholar 

  • Robbins L, Hansen M, Kleypas J, Meylan S (2010) CO2calc: a user-friendly seawater carbon calculator for Windows, Mac OS X, and iOS (iPhone). U.S. Geological Survey Open-File Report, 2010-1280, 17 p

  • Ross QE, Dunning DJ, Menezes JK, Kenna MJ Jr, Tiller G (1996) Reducing impingement of alewives with high-frequency sound at a power plant intake on Lake Ontario. North Am J Fish Manage 16:548–559. https://doi.org/10.1577/1548-8675(1996)0162.3.CO;2

    Article  Google Scholar 

  • Ross RM, Krise WF, Redell LA, Bennett RM (2001) Effects of dissolved carbon dioxide on the physiology and behavior of fish in artificial streams. Environ Toxicol 16:84–95. https://doi.org/10.1002/1522-7278(2001)16:1<84:AID-TOX100>3.0.CO;2-1

    Article  CAS  PubMed  Google Scholar 

  • Sampson SJ, Chick JH, Pegg MA (2009) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi rivers. Biol Invasions 11:483–496. https://doi.org/10.1007/s10530-008-9265-7

    Article  Google Scholar 

  • Sass GG, Cook TR, Irons KS, McClelland MA, Michaels NN, O’Hara ETM, Stroub MR (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biol Invasions 12:433–436. https://doi.org/10.1007/s10530-009-9462-z

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (eds) (1995) Assumptions of analysis of variance. In: Biometry. The principles and practice of statistics in biological research, 3rd edn. Freeman WH and Company, New York, pp 396–406

    Google Scholar 

  • Sparks RE, Barkley TL, Creque SM, Dettmers JM, Stainbrook KM (2010) Evaluation of an electric fish dispersal barrier in the Chicago Sanitary and Ship Canal. Am Fish Soc Symp 74:121–137

    Google Scholar 

  • Tix JA, Hasler CT, Sullivan C, Jeffrey JD, Suski CD (2016) Elevated carbon dioxide has the potential to impact alarm cue responses in some freshwater fishes. Aquat Ecol 51:59–71. https://doi.org/10.1007/s10452-016-9608-x

    Article  CAS  Google Scholar 

  • Tsehaye I, Catalano M, Sass G, Glover D, Roth B (2013) Prospects for fishery-induced collapse of invasive Asian carp in the Illinois River. Fisheries 38:445–454. https://doi.org/10.1080/03632415.2013.836501

    Article  Google Scholar 

  • Vörös L, Oldal L, Prèsing M, Balogh V (1997) Size-selective filtration and taxon-specific digestion of plankton algae by silver carp (Hypophthalmichthys molitrix Val.). Hydrobiologia 342:223–228

    Article  Google Scholar 

  • Waller D, Bartsch M, Fredricks KT, Schleis S, Bartsch L, Sheldon L (2016) Effects of carbon dioxide on juveniles of the freshwater mussel (Lampsillis siliquoidea). Environ Toxicol Chem 36:671–681. https://doi.org/10.1002/etc.3567

    Article  CAS  PubMed  Google Scholar 

  • Wanninkhof R (1992) Relationship between wind speed and gas exchange over the ocean. J Geophys Res 97(C5):7373–7382

    Article  Google Scholar 

  • Wetzel RG (2001) Limnology: lake and river ecosystems, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Wickham H (2009) Ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Williamson CJ, Garvey JE (2005) Growth, fecundity, and diets of newly established silver carp in the middle Mississippi River. Trans Am Fish Soc 134:1423–1430. https://doi.org/10.1577/T04-106.1

    Article  Google Scholar 

  • Yoshikawa HY, Ishida Y, Ueno S, Mitsuda H (1988) Changes in depth of anesthesia of the carp anesthetized with a constant level of CO2. Nippon Suisan Gakkaishi 54:457–462. https://doi.org/10.2331/suisan.54.457

    Article  Google Scholar 

  • Yoshikawa H, Yokoyama Y, Ueno S, Mitsuda H (1991) Changes of blood gas in carp, Cyprinus carpio, anesthetized with carbon dioxide. Comp Biochem Physiol A Physiol 98:431–436. https://doi.org/10.1016/0300-9629(91)90427-E

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice-Hall/Pearson, Upper Saddle River

    Google Scholar 

Download references

Acknowledgements

Financial resources for this study were provided by the U.S. Geological Survey (USGS) Ecosystems Mission Area Invasive Species Program and the Great Lakes Restoration Initiative. All procedures performed in this study involving animals were in accordance with the ethical standards of the USGS (protocol # AEH–16–CO2–02). We thank Dr. Caleb Hasler for guidance with shuttle-box setup. Any use of trade, firm, or product name is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Authors and Affiliations

  1. U.S. Geological Survey, Upper Midwest Environmental Sciences Center, 2630 Fanta Reed Rd., La Crosse, WI, 54603, USA

    John A. Tix, Aaron R. Cupp, Justin R. Smerud, Richard A. Erickson, Kim T. Fredricks & Jon J. Amberg

  2. Department of Natural Resources and Environmental Sciences, University of Illinois Urbana-Champaign, W-503 Turner Hall, 1102 South Goodwin Ave, Urbana, IL, 61801, USA

    Cory D. Suski

Authors
  1. John A. Tix
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aaron R. Cupp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Justin R. Smerud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Richard A. Erickson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kim T. Fredricks
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jon J. Amberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cory D. Suski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John A. Tix.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tix, J.A., Cupp, A.R., Smerud, J.R. et al. Temperature dependent effects of carbon dioxide on avoidance behaviors in bigheaded carps. Biol Invasions 20, 3095–3105 (2018). https://doi.org/10.1007/s10530-018-1761-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-018-1761-9

Keywords

Search

Navigation