Skip to main content

Molecular and behavioral responses of early-life stage fishes to elevated carbon dioxide

Biological Invasions volume 17, pages 3133–3151 (2015)Cite this article

Abstract

Bigheaded carps are non-native invasive fishes that have quickly become the most abundant fishes in many portions of the Midwestern United States. While the spread of bigheaded carps into the Great Lakes is currently impeded by three electrified barriers, these fish have the potential to negatively impact the Great Lakes ecosystem if this barrier is breached, and these barriers may be particularly vulnerable to the passage of small fishes. As such, novel barrier technologies would provide an additional mechanism to prevent bigheaded carps from invading the Great Lakes, and provide much needed redundancy to the current electric barrier. The current study used a combination of molecular and behavioral experiments to determine the effectiveness of carbon dioxide as a chemical deterrent for larval and juvenile fishes, with an emphasis on bigheaded carps. Juvenile silver carp (Hypophthalmichthys molitrix), bighead carp (H. nobilis), bluegill (Lepomis macrochirus) and largemouth bass (Micropterus salmoides) showed avoidance of elevated CO2 environments at approximately 200 mg/L. Additionally, exposure to 120 mg/L CO2 resulted in the induction of hsp70 mRNA in 8 days old silver carp fry, while gill c-fos transcripts increased following hypercarbia exposure in all juvenile species examined. Together, our results show that CO2 has potential to deter the movement of larval and juvenile fishes.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Alsop D, Vijayan MM (2009) Molecular programming of the corticosteroid stress axis during zebrafish development. Comp Biochem Physiol A Mol Integr Physiol 153:49–54

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Applebaum SL, Wilson CA, Holt GJ, Nunez BS (2010) The onset of cortisol synthesis and the stress response is independent of changes in CYP11B or CYP21 mRNA levels in larval red drum (Sciaenops ocellatus). Gen Comp Endocrinol 165:269–276

    Article  CAS  PubMed  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525

    Article  CAS  PubMed  Google Scholar 

  • Beggel S, Werner I, Connon RE, Geist JP (2012) Impacts of the phenylpyrazole insecticide fipronil on larval fish: time-series gene transcription responses in fathead minnow (Pimephales promelas) following short-term exposure. Sci Total Environ 426:160–165

    Article  CAS  PubMed  Google Scholar 

  • Bierbower SM, Cooper RL (2010) The effects of acute carbon dioxide on behavior and physiology in Procambarus clarkii. J Exp Zool A Ecol Genet Physiol 313A:484–497

    Article  Google Scholar 

  • Bustin SA, Benes V, Garson JA et al (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Clingerman J, Bebak J, Mazik PM, Summerfelt ST (2007) Use of avoidance response by rainbow trout to carbon dioxide for fish self-transfer between tanks. Aquac Eng 37:234–251

    Article  Google Scholar 

  • Conover G, Simmonds R, Whalen M (2007) Management and control plan for bighead, black, grass, and silver carps in the United States. Asian Carp Work. Group, Aquatic Nuisance Species Task Force, Washington, DC

    Google Scholar 

  • Cooke SL, Hill WR (2010) Can filter-feeding Asian carp invade the Laurentian Great Lakes? A bioenergetic modelling exercise. Freshw Biol 55:2138–2152

    Article  Google Scholar 

  • Cummins EP, Selfridge AC, Sporn PH et al (2014) Carbon dioxide-sensing in organisms and its implications for human disease. Cell Mol Life Sci 71:831–845

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Curran T, Franza BR Jr (1988) Fos and jun: the AP-1 connection. Cell 55:395–397

    Article  CAS  PubMed  Google Scholar 

  • Dennis CE III, Kates DF, Noatch MR, Suski CD (2014) Molecular responses of fishes to elevated carbon dioxide. Comp Biochem Physiol A Mol Integr Physiol. doi:10.1016/j.cbpa.2014.05.013

    PubMed  Google Scholar 

  • Dettmers JM, Boisvert BA, Barkley T, Sparks RE (2005) Potential impact of steel-hulled barges on movement of fish across an electric barrier to prevent the entry of invasive carp into Lake Michigan. Aquatic Ecology Report 2005 (14), Illinois State Natural History Survey, Urbana, IL

  • Dolan CR, Miranda LE (2003) Immobilization thresholds of electrofishing relative to fish size. Trans Am Fish Soc 132:969–976

    Article  Google Scholar 

  • Douglas CE, Michael FA (1991) On distribution-free multiple comparisons in the one-way analysis of variance. Commun Stat Theory Methods 20:127–139

    Article  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

    Article  Google Scholar 

  • Gilmour KM (2001) The CO2/pH ventilatory drive in fish. Comp Biochem Physiol A Mol Integr Physiol 130:219–240

    Article  CAS  PubMed  Google Scholar 

  • Hamel MJ, Brown ML, Chipps SR (2008) Behavioral responses of rainbow smelt to in situ strobe lights. N Am J Fish Manag 28:394–401

    Article  Google Scholar 

  • Hartley HO (1950) The maximum F-ratio as a short-cut test for heterogeneity of variance. Biometrika 37:308–312

    CAS  PubMed  Google Scholar 

  • Hasler CT, Suski CD, Hanson KC, Cooke SJ, Tufts BL (2009) The influence of dissolved oxygen on winter habitat selection by largemouth bass: an integration of field biotelemetry studies and laboratory experiments. Physiol Biochem Zool 82:143–152

    Article  CAS  PubMed  Google Scholar 

  • Healy TM, Tymchuk WE, Osborne EJ, Schulte PM (2010) Heat shock response of killifish (Fundulus heteroclitus): candidate gene and heterologous microarray approaches. Physiol Genomics 41:171–184

    Article  CAS  PubMed  Google Scholar 

  • Ings JS, Servos MR, Vijayan MM (2011) Hepatic transcriptomics and protein expression in rainbow trout exposed to municipal wastewater effluent. Environ Sci Technol 45:2368–2376

    Article  CAS  PubMed  Google Scholar 

  • Irons KS, Sass GG, McClelland MA, Stafford JD (2007) Reduced condition factor of two native fish species coincident with invasion of non-native Asian carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? J Fish Biol 71:258–273

    Article  Google Scholar 

  • Ishimatsu A, Hayashi M, Kikkawa T (2008) Fishes in high-CO2, acidified oceans. Mar Ecol Prog Ser 373:295–302

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Iwama GK, Afonso LOB, Todgham A et al (2004) Are hsps suitable for indicating stressed states in fish? J Exp Biol 207:15–19

    Article  CAS  PubMed  Google Scholar 

  • Jones KA, Hara TJ, Scherer E (1985) Locomotor response by Arctic char (Salvelinus alpinus) to gradients of H+ and CO2. Physiol Zool 58:413–420

    Google Scholar 

  • Kassahn KS, Crozier RH, Pörtner HO, Caley MJ (2009) Animal performance and stress: responses and tolerance limits at different levels of biological organization. Biol Rev 84:277–292

    Article  PubMed  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

    Article  CAS  Google Scholar 

  • Kieffer J, Cooke S (2009) Physiology and organismal performance of centrarchids. In: Cooke SJ, Philipp DP (eds) Centrarchid fishes: diversity, biology, and conservation. Wiley-Blackwell, West Sussex, pp 207–263

    Chapter  Google Scholar 

  • Kolar CS, Chapman DC, Courtenay Jr. WR, et al. (2007) Bigheaded carps: a biological synopsis and environmental risk assessment. In: Special Publication, American Fisheries Society Symposium, Bethesda, MD, pp 1–204

  • Landsman SJ, Gingerich AJ, Philipp DP, Suski CD (2011) The effects of temperature change on the hatching success and larval survival of largemouth bass Micropterus salmoides and smallmouth bass Micropterus dolomieu. J Fish Biol 78:1200–1212

    Article  CAS  PubMed  Google Scholar 

  • Lewis JM, Hori TS, Rise ML et al (2010) Transcriptome responses to heat stress in the nucleated red blood cells of the rainbow trout (Oncorhynchus mykiss). Physiol Genomics 42:361–373

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Zhu K, Chen N, et al (2013) Identification of HIF-1α promoter and expression regulation of HIF-1α gene by LPS and hypoxia in zebrafish. Fish Physiol Biochem 39:1–11

    Article  Google Scholar 

  • Lodge DM, Williams S, MacIsaac HJ et al (2006) Biological invasions: recommendations for US policy and management. Ecol Appl 16:2035–2054

    Article  PubMed  Google Scholar 

  • López-Patiño MA, Hernández-Pérez J, Gesto M et al (2014) Short-term time course of liver metabolic response to acute handling stress in rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol A Mol Integr Physiol 168:40–49

    Article  PubMed  Google Scholar 

  • Mancebo MJ, Ceballos FC, Pérez-Maceira J, Aldegunde M (2013) Hypothalamic neuropeptide Y (NPY) gene expression is not affected by central serotonin in the rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A Mol Integr Physiol 166:186–190

    Article  CAS  PubMed  Google Scholar 

  • Milligan CL (1996) Metabolic recovery from exhaustive exercise in rainbow trout. Comp Biochem Physiol A Physiol 113:51–60

    Article  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268

    Article  Google Scholar 

  • Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288:R1079–R1090

    Article  CAS  PubMed  Google Scholar 

  • Noatch MR, Suski CD (2012) Non-physical barriers to deter fish movements. Environ Rev 20:71–82

    Article  Google Scholar 

  • Patel A, Glassner-Shwayder K, Eder T, Looney P (2010) Halting the invasion: maintaining the health of the Great Lakes and Mississippi River basins by preventing further exchange of aquatic invasive species. Environ Pract 12:342–356

    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

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Prunet P, Cairns MT, Winberg S, Pottinger TG (2008) Functional genomics of stress responses in fish. Rev Fish Sci 16:157–166

    Article  CAS  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 Gt Lakes Res 37:588

    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 

  • Ricciardi A (2013) Invasive species. In: Leemans R (ed) Ecological systems. Springer, NY, pp 161–178

    Chapter  Google Scholar 

  • Ricciardi A, MacIsaac HJ (2011) Impacts of biological invasions on freshwater ecosystems. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley-Blackwell, Chichester, pp 211–224

    Google Scholar 

  • Gattuso JP, Gao K, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. European Commision, Brussels, pp 41–52

    Google Scholar 

  • Rimoldi S, Terova G, Brambilla F et al (2009) Molecular characterization and expression analysis of Na+/H+ exchanger (NHE)-1 and c-Fos genes in sea bass (Dicentrarchus labrax, L) exposed to acute and chronic hypercapnia. J Exp Mar Biol Ecol 375:32–40

    Article  CAS  Google Scholar 

  • Rimoldi S, Terova G, Ceccuzzi P et al (2012) HIF-1α mRNA levels in Eurasian perch (Perca fluviatilis) exposed to acute and chronic hypoxia. Mol Biol Rep 39:4009–4015

    Article  CAS  PubMed  Google Scholar 

  • Robbins L, Hansen M, Kleypas J, Meylan S (2010) CO2calc: a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone). US Geol Surv Open-File Rep 1280:2010

    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

    Article  CAS  PubMed  Google Scholar 

  • Sassi A, Darias M, Said K, et al (2012) Cadmium exposure affects the expression of genes involved in skeletogenesis and stress response in gilthead sea bream larvae. Fish Physiol Biochem 39:1–11

    Google Scholar 

  • Sato M, Severinghaus JW, Basbaum AI (1992) Medullary CO2 chemoreceptor neuron identification by c-fos immunocytochemistry. J Appl Physiol 73:96–100

    CAS  PubMed  Google Scholar 

  • Serrano X, Grosell M, Serafy JE (2010) Salinity selection and preference of the grey snapper Lutjanus griseus: field and laboratory observations. J Fish Biol 76:1592–1608

    Article  CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman and Company, NY

    Google Scholar 

  • Sorensen PW, Stacey NE (2004) Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes. N Zeal J Mar Freshw 38:399–417

    Article  CAS  Google Scholar 

  • Sparks RE, Barkley T, Creque S et al (2010) Evaluation of an electric fish dispersal barrier in the Chicago Sanitary and Ship Canal. Am Fish Soc Symp 74:121–137

    Google Scholar 

  • Stolte EH, Chadzinska M, Przybylska D et al (2009) The immune response differentially regulates Hsp70 and glucocorticoid receptor expression in vitro and in vivo in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 27:9–16

    Article  CAS  PubMed  Google Scholar 

  • Stouthart AJ, Lucassen EC, vanStrien F et al (1998) Stress responsiveness of the pituitary-interrenal axis during early life stages of common carp (Cyprinus carpio). J Endocrinol 157:127–137

    Article  CAS  PubMed  Google Scholar 

  • Suski CD, Killen SS, Kieffer JD, Tufts BL (2006) The influence of environmental temperature and oxygen concentration on the recovery of largemouth bass from exercise: implications for live–release angling tournaments. J Fish Biol 68:120–136

    Article  CAS  Google Scholar 

  • Takle H, Baeverfjord G, Lunde M et al (2005) The effect of heat and cold exposure on HSP70 expression and development of deformities during embryogenesis of Atlantic salmon (Salmo salar). Aquaculture 249:515–524

    Article  CAS  Google Scholar 

  • Tankersley CG, Haxhiu MA, Gauda EB (2002) Differential CO2-induced c-fos gene expression in the nucleus tractus solitarii of inbred mouse strains. J Appl Physiol 92:1277–1284

    Article  CAS  PubMed  Google Scholar 

  • US Army Corps of Engineers (2014) The Great Lakes and Mississippi River Interbasin Study (GLMRIS) report [online]. US Army Corps of Engineers. http://glmris.anl.gov/documents/docs/glmrisreport/GLMRIS_Report.pdf

  • Vanlandeghem MM, Wahl DH, Suski CD (2010) Physiological responses of largemouth bass to acute temperature and oxygen stressors. Fish Manag Ecol 17:414–425

    Article  Google Scholar 

  • Wang J, Wei Y, Li X et al (2007) The identification of heat shock protein genes in goldfish (Carassius auratus) and their expression in a complex environment in Gaobeidian Lake, Beijing, China. Comp Biochem Physiol Part C Toxicol Pharmacol 145:350–362

    Article  Google Scholar 

  • Wiseman S, Osachoff H, Bassett E et al (2007) Gene expression pattern in the liver during recovery from an acute stressor in rainbow trout. Comp Biochem Physiol Part D Genomics Proteomics 2:234–244

    Article  PubMed  Google Scholar 

  • Ye J, Coulouris G, Zaretskaya I et al (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134

    Article  PubMed Central  CAS  PubMed  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

    Article  Google Scholar 

  • Yoshikawa H, Kawai F, Kanamori M (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

    Article  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, USA

    Google Scholar 

  • Zubair S, Peake S, Hare J, Anderson WG (2012) The effect of temperature and substrate on the development of the cortisol stress response in the lake sturgeon, Acipenser fulvescens, Rafinesque (1817). Environ Biol Fishes 93:577–587

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Illinois Department of Natural Resources, through funds provided by the USEPA’s Great Lakes Restoration Initiative. Partial funding was also provided by the United States Geological Survey and by the United States Fish and Wildlife Service (USFWS) Federal Aid in Sport Fish Restoration Project F-69-R. Steve Kahrs and Pete Kahrs provided valuable help supplying larval bigheaded carps. We would like to thank James Luoma, Mark Gaikowski, along with the other biologists at UMESC, for providing valuable help with fish collection and juvenile bigheaded carps husbandry. David Sutter, Dan Kates, Thomas Kates, Will Cejtin, and Adam Wright provided field and laboratory assistance. All work performed in this study conformed to guidelines established by the Institutional Animal Care and Use Committee (IACUC) of the University of Illinois (Protocol # 13123).

Author information

Authors and Affiliations

  1. Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 S. Goodwin Ave, Urbana, IL, 61801, USA

    Clark E. Dennis III, Shivani Adhikari & Cory D. Suski

Authors
  1. Clark E. Dennis III
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shivani Adhikari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cory D. Suski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Clark E. Dennis III.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-0941-0

Keywords

  • Bigheaded carps
  • Hypercarbia
  • Avoidance
  • Barriers
  • Stress
  • Genes
  • Juvenile
  • Larval