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Acclimation to a low oxygen environment alters the hematology of largemouth bass (Micropterus salmoides)

Abstract

One of the most severe impacts of urbanization on aquatic systems is the increasing presence of low oxygen environments caused by anthropogenic sources of pollution. As urbanization increases nationally and globally, it is becoming exceedingly important to understand how hypoxia affects aquatic fauna, especially fish species. In an effort to better understand the impacts of prolonged hypoxia on fishes, largemouth bass were held at 3.0 and 9.0 mg L−1 for 50 days, which has previously shown to be temporally sufficient to impart plastic phenotypic changes. Following the holding period, fish from each group were subjected to a low dissolved oxygen (DO) challenge of 2.0 mg L−1 for 6 h, and their physiological and hematological parameters were compared with control fish held for 6 h with no change in DO. There were no differences in the physiological stress responses between the two holding groups; however, the low oxygen holding group had increased hemoglobin and hematocrit levels following the 6-h low oxygen challenge compared with the high oxygen group. These results suggest largemouth bass exposed to chronic low oxygen conditions, either naturally or anthropogenically, may possess a beneficial advantage of increased oxygen uptake capacity during periods of low oxygen.

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Notes

  1. Sequences 5′ → 3′:

    18S: F-GCAAAGCTGAAACTTAAAGGAATTG; R-CCCGTGATTGAGTCAAATTAAGC

    HIF-1α: F-AACACAGAGCGCAGCTTCTTC; R-CGGCCCCTGCTTGTGA.

References

  • Alp EA (2006) A method to evaluate duration of the storm effects on in-stream water quality. Dissertation, Marquette University

  • Anderson RO, Neumann RM (1996) Length, weight, and associated structural indices. In: Murphy BR, Willis DW (eds) Fisheries techniques, 2nd edn. American Fisheries Society, Bethesda, pp 447–482

    Google Scholar 

  • Baker LA (2009) New concepts for managing urban pollution. In: Baker LA (ed) The water environment of cities. Springer, New York

    Chapter  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 

  • Bell GW, Eggelston DB, Wolcott TG (2003) Behavioral responses of free-ranging blue crabs to episodic hypoxia. I. Movement. Mar Ecol Prog Ser 259:215–225

    Article  Google Scholar 

  • Bernhardt ES, Band LE, Walsh CJ, Berke PE (2008) Understanding, managing, and minimizing urban impacts on surface water nitrogen loading. Ann NY Acad Sci 1132:61–96

    Article  Google Scholar 

  • Bracken CP, Whitelaw ML, Peet DJ (2003) The hypoxia-inducible factors: key transcriptional regulators of hypoxic responses. Cell Mol Life Sci 60:1376–1393

    Article  CAS  PubMed  Google Scholar 

  • Brandt SB, Gerken M, Hartman KJ, Demers E (2009) Effects of hypoxia on food consumption and growth of juvenile striped bass (Morone saxatilis). J Exp Mar Biol Ecol 381:S143–S149

    Article  Google Scholar 

  • Burton GA, Pitt BE (2002) Stormwater effects handbook: a toolbox for watershed managers, scientists, and engineers. Lewis Publishers, Washington

    Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Caraguel CGB, Stryhn H, Gagné N, Dohoo IR, Hammell KL (2011) Selection of a cutoff value for real-time polymerase chain reaction results to fit a diagnostic purpose: analytical and epidemiologic approaches. J Vet Diagn Invest 23:2–15

    Article  PubMed  Google Scholar 

  • Cech J, Mitchell S, Wragg T (1984) Comparative growth of juvenile white sturgeon and striped bass: effects of temperature and hypoxia. Estuaries Coasts 7:12–18

    Article  Google Scholar 

  • Chabot D, Dutil JD (1999) Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J Fish Biol 55:472–491

    Article  Google Scholar 

  • Chapman LJ, Chapman CA, Crisman TL, Nordlie FG (1998) Dissolved oxygen and thermal regimes of a Ugandan crater lake. Hydrobiologia 385:201–211

    Article  CAS  Google Scholar 

  • Deere JA, Chown SL (2006) Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. Am Nat 168:630–644

    Article  PubMed  Google Scholar 

  • Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971

    Article  Google Scholar 

  • Fu SJ, Brauner CJ, Cao ZD, Richards JG, Peng JL, Dhillon R, Wang YX (2011) The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (Carassius auratus). J Exp Biol 214:2080–2088

    Article  CAS  PubMed  Google Scholar 

  • Geister TL, Fischer K (2007) Testing the beneficial acclimation hypothesis: temperature effects on mating success in a butterfly. Behav Ecol 18:658–664

    Article  Google Scholar 

  • Gonzalez R, McDonald D (1994) The relationship between oxygen uptake and ion loss in fish from diverse habitats. J Exp Biol 190:95–108

    PubMed  Google Scholar 

  • Hasler CT, Suski CD, Hanson CD, 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 

  • Houston AH (1990) Blood and circulation. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 273–334

    Google Scholar 

  • Jensen FB, Nikinmaa M, Weber RE (1993) Environmental perturbations of oxygen transport in teleost fishes: causes, consequences and compensations. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 162–179

    Google Scholar 

  • Kieffer JD, Baker DW, Wood AM, Papadopoulos CN (2011) The effects of temperature on the physiological response to low oxygen in Atlantic sturgeon. Fish Physiol Biochem 37:809–819

    Article  CAS  PubMed  Google Scholar 

  • Kramer DL, Mehegan JP (1981) Aquatic surface respiration, an adaptive response to hypoxia in the guppy Poecilia reticulate (Pisces, Poeciliidae). Environ Biol Fishes 6:299–313

    Article  Google Scholar 

  • Lai JCC, Kakuta I, Mok HOL, Rummer JL, Randall D (2006) Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen. J Exp Biol 209:2734–2738

    Article  CAS  PubMed  Google Scholar 

  • Lays N, Iversen MMT, Frantzen M, Jorgensen EH (2009) Physiological stress responses in spotted wolfish (Anarhichas minor) subjected to acute disturbance and progressive hypoxia. Aquaculture 295:126–133

    Article  Google Scholar 

  • Leroi AM, Bennet AF, Lenski RE (1994) Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc Natl Acad Sci USA 91:1917–1921

    Article  CAS  PubMed  Google Scholar 

  • Lewis JM, Hori TS, Rise ML, Walsh PJ, Currie S (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 

  • Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic Press, New York

    Google Scholar 

  • Lurman GJ, Bock CH, Portner HO (2009) Thermal acclimation to 4 or 10°C imparts minimal benefit on swimming performance in Atlantic cod (Gadus morhua L.). J Comp Physiol B 179:623–633

    Article  PubMed  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 

  • O’Connor EA, Pottinger TG, Sneddon LU (2011) The effects of acute and chronic hypoxia on cortisol, glucose and lactate concentrations in different populations of three-spined stickleback. Fish Physiol Biochem 37:461–469

    Article  PubMed  Google Scholar 

  • Officer CB, Biggs RB, Taft JL, Cronin LE, Tyler MA, Boynton WR (1984) Chesapeake Bay anoxia: origin, development, and significance. Science 223:22–27

    Article  CAS  PubMed  Google Scholar 

  • Paul MJ, Meyer JL (2008) Streams in the urban landscape. Annu Rev Ecol Syst 32:333–365

    Article  Google Scholar 

  • Petersen LH, Gamperl AK (2010) Cod (Gadus morhua) cardiorespiratory physiology and hypoxia tolerance following acclimation to low-oxygen conditions. Physiol Biochem Zool 84:18–31

    Article  Google Scholar 

  • Petersen JK, Petersen GI (1990) Tolerance, behavior and oxygen consumption in the sand goby, Pomatoschistus minutus (Pallas), exposed to hypoxia. J Fish Biol 37:921–933

    Article  Google Scholar 

  • Pichavant KJ, Person-Le-Ruyet J, Le Bayon N, Severe A, Le Roux A, Boeuf G (2001) Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. J Fish Biol 59:875–883

    Article  Google Scholar 

  • Pollock MS, Clarke LMJ, Dubé MG (2007) The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ Rev 15:1–14

    Article  CAS  Google Scholar 

  • Richards JG (2009) Metabolic and molecular responses of fish to hypoxia. In: Richards JG, Farrell AP, Brauner CJ (eds) Fish physiology: hypoxia, 1st edn. Academic Press, New York, pp 443–485

    Chapter  Google Scholar 

  • Rimoldi S, Terova G, Ceccuzzi P, Merelli S, Antonini M, Saroglia M (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 

  • Saroglia M, Cecchini S, Terova G, Caputo A, De Stradis A (2000) Influence of environmental temperature and water oxygen concentration on gas diffusion distance in sea bass (Dicentrarchus labrax, L.). Fish Physiol Biochem 23:55–58

    Article  CAS  Google Scholar 

  • Saroglia M, Terova G, De Stradis A, Caputo A (2002) Morphometric adaptations of sea bass gills to different dissolved oxygen partial pressures. J Fish Biol 60:1423–1430

    Article  Google Scholar 

  • Saroglia M, Caricato G, Frittella F, Brambilla F, Terova G (2010) Dissolved oxygen regimen (PO2) may affect osmo-respiratory compromise in European sea bass (Dicentrarchus labrax, L.). Ital J Anim Sci 9e15:73–78

    Google Scholar 

  • Scott AL, Rogers WA (1981) Haematological effects of prolonged sublethal hypoxia on channel catfish Ictalurus punctatus (Rafineque). J Fish Biol 18:591–601

    Article  CAS  Google Scholar 

  • Sink TD, Lochmann RT, Fecteau KA (2008) Validation, use, and disadvantages of enzyme-linked immunosorbent assay kits for detection of cortisol in channel catfish, largemouth bass, red pacu, and golden shiners. Fish Physiol Biochem 34:95–101

    Article  CAS  PubMed  Google Scholar 

  • Soitamo AJ, Rabergh CM, Gassmann M, Sistonen L, Nikinmaa M (2001) Characterization of hypoxia-inducible factor (HIF-1α) from rainbow trout. J Biol Chem 276:19699–19705

    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 

  • Terova G, Rimoldi S, Cora S, Bernardini G, Gornati R, Saroglia M (2008) Acute and chronic hypoxia affects HIF-1α mRNA levels in sea bass (Dicentrarchus labrax). Aquaculture 279:150–159

    Article  CAS  Google Scholar 

  • Timmerman CM, Chapman LJ (2004) Behavioral and physiological compensation for chronic hypoxia in the sailfin molly (Poecilia latipinna). Physiol Biochem Zool 77:601–610

    Article  PubMed  Google Scholar 

  • Tun N, Houston AH (1986) Temperature, oxygen, photoperiod, and the hemoglobin system of the rainbow trout, Salmo gairdneri. Can J Zool 64:1883–1888

    Article  CAS  Google Scholar 

  • 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 

  • Wells RMG (2009) Gas transport and hemoglobin function: adaptations for functional and environmental hypoxia. In: Richards JG, Farrell AP, Brauner CJ (eds) Fish physiology: hypoxia, 1st edn. Academic Press, New York, pp 255–299

    Chapter  Google Scholar 

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

  • Wetzel RG (1983) Limnology. Saunder, Philadelphia

    Google Scholar 

  • Wilson R, Condon CHL, Johnston IA (2007) Consequences of thermal acclimation for the mating behavior and swimming performance of female mosquito fish. Philos Trans R Soc B 362:2131–2139

    Article  Google Scholar 

  • Wright PA, Perry SF, Moon TW (1989) Regulation of hepatic gluconeogenesis and glycogenolysis by catecholamines in rainbow trout during environmental hypoxia. J Exp Biol 147:169–188

    CAS  PubMed  Google Scholar 

  • Zhao WW, Pang X, Peng JL, Cao ZD, Fu SJ (2012) The effects of hypoxia acclimation, exercise training and fasting on swimming performance in juvenile qingbo (Spinibarbus sinensis). Fish Physiol Biochem 38(5):1367–1377

    Google Scholar 

  • Zhou BS, Wu RSS, Randall DJ, Lam PKS, Ip YK, Chew SF (2000) Metabolic adjustments in the common carp during prolonged hypoxia. J Fish Biol 57:1160–1171

    Article  CAS  Google Scholar 

  • Zhu W, Graney J, Salvage K (2008) Land-use impact on water pollution: elevated pollutant input and reduced pollutant retention. J Contemp Water Res Educ 139:15–21

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank the Water Environment Research Foundation (project U3R09) for providing the funds for this study, as well as the Illinois-Indiana Sea Grant College Program Grant # NA06OAR4170079 for supplemental funds. D. Kates, Z. Zuckerman, S. Liss, and D. Sutter provided assistance with data collection. Dr. R. Schooley provided valuable insight into earlier drafts of this work.

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Correspondence to Cory D. Suski.

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Gaulke, G.L., Dennis, C.E., Wahl, D.H. et al. Acclimation to a low oxygen environment alters the hematology of largemouth bass (Micropterus salmoides). Fish Physiol Biochem 40, 129–140 (2014). https://doi.org/10.1007/s10695-013-9830-6

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  • DOI: https://doi.org/10.1007/s10695-013-9830-6

Keywords

  • Stress
  • Physiology
  • Hematology
  • Hypoxia
  • Acclimation