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Testing hypoxia: physiological effects of long-term exposure in two freshwater fishes

Oecologia volume 186, pages 37–47 (2018)Cite this article

Abstract

Hypoxic or oxygen-free zones are linked to large-scale mortalities of fauna in aquatic environments. Studies investigating the hypoxia tolerance of fish are limited and focused on marine species and short-term exposure. However, there has been minimal effort to understand the implications of long-term exposure on fish and their ability to acclimate. To test the effects of long-term exposure (months) of fish to hypoxia we devised a novel method to control the level of available oxygen. Juvenile golden perch (Macquaria ambigua ambigua), and silver perch (Bidyanus bidyanus), two key native species found within the Murray Darling Basin, Australia, were exposed to different temperatures (20, 24 and 28 °C) combined with normoxic (6–8 mgO2 L−1 or 12–14 kPa) and hypoxic (3–4 mgO2 L−1 or 7–9 kPa) conditions. After 10 months, fish were placed in individual respirometry chambers to measure standard and maximum metabolic rate (SMR and MMR), absolute aerobic scope (AAS) and hypoxia tolerance. Golden perch had a much higher tolerance to hypoxia exposure than silver perch, as most silver perch died after only 1 month exposure. Golden perch acclimated to hypoxia had reduced MMR at 20 and 28 °C, but there was no change to SMR. Long-term exposure to hypoxia improved the tolerance of golden perch to hypoxia, compared to individuals held under normoxic conditions suggesting that golden perch can acclimate to levels around 3 mgO2 L−1 (kPa ~ 7) and lower. The contrasting tolerance of two sympatric fish species to hypoxia highlights our lack of understanding of how hypoxia effects fish after long-term exposure.

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References

  • Breitburg DL, Hondorp DW, Davias LA, Diaz RJ (2009) Hypoxia, nitrogen, and fisheries: integrating effects across local and global landscapes. Ann Rev Mar Sci 1:329–349

    Article  PubMed  Google Scholar 

  • Chabot D, Steffensen JF, Farrell AP (2016) The determination of standard metabolic rate in fishes. J Fish Biol 88(1):81–121

    Article  CAS  PubMed  Google Scholar 

  • Claireaux G, Chabot D (2016) Responses by fishes to environmental hypoxia: integration through Fry’s concept of aerobic metabolic scope. J Fish Biol 88(1):232–251

    Article  CAS  PubMed  Google Scholar 

  • Collins GM, Clark TD, Rummer JL, Carton AG (2013) Hypoxia tolerance is conserved across genetically distinct sub-populations of an iconic, tropical Australian teleost (Lates calcarifer). Conserv Physiol 1(1):1–9

    Article  Google Scholar 

  • Conley D, Carstensen J, Vaquer-Sunyer R, Duarte C (2009) Ecosystem thresholds with hypoxia. In: Andersen JH, Conley DJ (eds) Eutrophication in coastal ecosystems, vol 207. Springer, Netherlands, pp 21–29

    Chapter  Google Scholar 

  • Cook DG, Iftikar FI, Baker DW, Hickey AJ, Herbert NA (2013) Low-O2 acclimation shifts the hypoxia avoidance behaviour of snapper (Pagrus auratus) with only subtle changes in aerobic and anaerobic function. J Exp Biol 216(3):369–378

    Article  CAS  PubMed  Google Scholar 

  • Dean TL, Richardson J (1999) Responses of seven species of native freshwater fish and a shrimp to low levels of dissolved oxygen. N Z J Mar Freshw Res 33(1):99–106

    Article  Google Scholar 

  • Deutsch C, Ferrel A, Seibel B, Pörtner H-O, Huey RB (2015) Climate change tightens a metabolic constraint on marine habitats. Science 348(6239):1132–1135

    Article  CAS  PubMed  Google Scholar 

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321(5891):926–929

    Article  CAS  PubMed  Google Scholar 

  • Díaz RJ, Rosenberg R (2011) Introduction to environmental and economic consequences of hypoxia. Int J Water Resour Dev 27(1):71–82

    Article  Google Scholar 

  • Eliason EJ, Farrell AP (2016) Oxygen uptake in Pacific salmon Oncorhynchus spp.: when ecology and physiology meet. J Fish Biol 88(1):359–388

    Article  CAS  PubMed  Google Scholar 

  • Eliason EJ, Clark TD, Hague MJ, Hanson LM, Gallagher ZS, Jeffries KM, Gale MK, Patterson DA, Hinch SG, Farrell AP (2011) Differences in thermal tolerance among sockeye salmon populations. Science 332(6025):109–112

    Article  CAS  PubMed  Google Scholar 

  • Farrell AP (2016) Pragmatic perspective on aerobic scope: peaking, plummeting, pejus and apportioning. J Fish Biol 88(1):322–343

    Article  CAS  PubMed  Google Scholar 

  • Feng J, Guo Y, Gao Y, Zhu L (2016) Effects of hypoxia on the physiology of zebrafish (Danio rerio): initial responses, acclimation and recovery. Bull Environ Contam Toxicol 96(1):43–48

    Article  CAS  PubMed  Google Scholar 

  • Fu S-J, Brauner CJ, Cao Z-D, Richards JG, Peng J-L, Dhillon R, Wang Y-X (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(12):2080–2088

    Article  CAS  PubMed  Google Scholar 

  • Hague MJ, Ferrari MR, Miller JR, Patterson DA, Russell GL, Farrell AP, Hinch SG (2011) Modelling the future hydroclimatology of the lower Fraser River and its impacts on the spawning migration survival of sockeye salmon. Glob Change Biol 17(1):87–98

    Article  Google Scholar 

  • Helz GR, Adelson JM (2013) Trace element profiles in sediments as proxies of dead zone history; rhenium compared to molybdenum. Environ Sci Technol 47(3):1257–1264

    Article  CAS  PubMed  Google Scholar 

  • King AJ, Tonkin Z, Lieshcke J (2012) Short-term effects of a prolonged blackwater event on aquatic fauna in the Murray River, Australia: considerations for future events. Mar Freshw Res 63(7):576–586

    Article  Google Scholar 

  • Koehn JD, Nicol SJ (2016) Comparative movements of four large fish species in a lowland river. J Fish Biol 88(4):1350–1368

    Article  CAS  PubMed  Google Scholar 

  • Lintermans M (2007) Fishes of the Murray-Darling basin: an introductory guide. Murray Darling Basin Comission Publication, Canberra, ACT, pp 1–131

  • McBryan TL, Anttila K, Healy TM, Schulte PM (2013) Responses to temperature and hypoxia as interacting stressors in fish: implications for adaptation to environmental change. Integr Comp Biol 53(4):648–659

    Article  CAS  PubMed  Google Scholar 

  • McCarthy B, Zukowski S, Whiterod N, Vilizzi L, Beesley L, King A (2014) Hypoxic blackwater event severely impacts Murray crayfish (Euastacus armatus) populations in the Murray River, Australia. Austral Ecol 39(5):491–500

    Article  Google Scholar 

  • McMaster D, Bond N (2008) A field and experimental study on the tolerances of fish to Eucalyptus camaldulensis leachate and low dissolved oxygen concentrations. Mar Freshw Res 59(2):177–185

    Article  CAS  Google Scholar 

  • McNeil DG, Closs GP (2007) Behavioural responses of a south-east Australian floodplain fish community to gradual hypoxia. Freshw Biol 52(3):412–420

    Article  CAS  Google Scholar 

  • Metcalfe NB, Van Leeuwen TE, Killen SS (2016) Does individual variation in metabolic phenotype predict fish behaviour and performance? J Fish Biol 88(1):298–321

    Article  CAS  PubMed  Google Scholar 

  • Nash RD, Valencia AH, Geffen AJ (2006) The origin of Fulton’s condition factor—setting the record straight. Fisheries 31(5):236–238

    Google Scholar 

  • Neuheimer AB, Thresher RE, Lyle JM, Semmens JM (2011) Tolerance limit for fish growth exceeded by warming waters. Nat Clim Change 1(2):110–113

    Article  Google Scholar 

  • Nilsson GE, Crawley N, Lunde IG, Munday PL (2009) Elevated temperature reduces the respiratory scope of coral reef fishes. Glob Change Biol 15(6):1405–1412

    Article  Google Scholar 

  • Norin T, Clark TD (2016) Measurement and relevance of maximum metabolic rate in fishes. J Fish Biol 88(1):122–151

    Article  CAS  PubMed  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 

  • Pörtner HO, Lannig G (2009) Oxygen and capacity limited thermal tolerance. In: Jeffrey APF, Richards G, Colin JB (eds) Fish physiology, vol 27. Academic Press, Cambridge, pp 143–191

    Google Scholar 

  • Rand PS, Hinch SG, Morrison J, Foreman MGG, MacNutt MJ, Macdonald JS, Healey MC, Farrell AP, Higgs DA (2006) Effects of river discharge, temperature, and future climates on energetics and mortality of adult migrating Fraser River sockeye salmon. Trans Am Fish Soc 135(3):655–667

    Article  Google Scholar 

  • Richardson J, Williams EK, Hickey CW (2001) Avoidance behaviour of freshwater fish and shrimp exposed to ammonia and low dissolved oxygen separately and in combination. N Z J Mar Freshw Res 35(3):625–633

    Article  Google Scholar 

  • Roche DG, Binning SA, Bosiger Y, Johansen JL, Rummer JL (2013) Finding the best estimates of metabolic rates in a coral reef fish. J Exp Biol 216(11):2103–2110

    Article  PubMed  Google Scholar 

  • Rogers NJ, Urbina MA, Reardon EE, McKenzie DJ, Wilson RW (2016) A new analysis of hypoxia tolerance in fishes using a database of critical oxygen level (Pcrit). Conserv Physiol 4(1):1–19

    Article  Google Scholar 

  • Rowland SJ (2008) Domestication of silver perch, Bidyanus bidyanus, broodfish. J Appl Aquac 16(1–2):75–83

    Google Scholar 

  • Rowland SJ (2009) Review of aquaculture research and development of the Australian freshwater fish silver perch, Bidyanus bidyanus. J World Aquac Soc 40(3):291–324

    Article  Google Scholar 

  • Rowland SJ, Tully P (2004) Hatchery quality assurance program for Murray cod (Maccullochella peelii peelii), golden perch (Macquaria ambigua), and silver perch (Bidyanus bidyanus). NSW Department of Primary Industries, Sydney

    Google Scholar 

  • R Studio Team (2016) RStudio: integrated development for R. RStudio, Inc., Boston, MA. http://www.rstudio.com/

  • Sollid J, Weber RE, Nilsson GE (2005) Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208(6):1109–1116

    Article  PubMed  Google Scholar 

  • Timmerman CM, Chapman LJ (2004) Behavioural and physiological compensation for chronic hypoxia in the Sailfin molly (Poecilia latipinna). Physiol Biochem Zool 77(4):601–610

    Article  PubMed  Google Scholar 

  • Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci 105(40):15452–15457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitworth KL, Baldwin DS, Kerr JL (2012) Drought, floods and water quality: drivers of a severe hypoxic blackwater event in a major river system (the southern Murray-Darling Basin, Australia). J Hydrol 450:190–198

    Article  Google Scholar 

  • Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Poll Bull 45(1):35–45

    Article  CAS  Google Scholar 

  • Zhang W, Cao Z-D, Peng J-L, Chen B-J, Fu S-J (2010) The effects of dissolved oxygen level on the metabolic interaction between digestion and locomotion in juvenile southern catfish (Silurus meridionalis Chen). Comp Biochem Physiol Mol Integr Physiol 157(3):212–219

    Article  Google Scholar 

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Acknowledgements

We would like to thank the Goyder Institute for Water research for funding which contributed to the success of this research. Funding from an ARC Future Fellowship (FT100100767) is also acknowledged. We would also like to thank Owen Burnell for his assistance in developing the novel approach to degassing multiple tanks to create hypoxic conditions long term in aquaria, and Lincoln Gilmore for building the respirometry chambers. Fish were kept according to the Australian Code of Practice for the care and use of animals for scientific purposes (8th Edition), and approved by the University of Adelaide’s animal care and ethics committee (AEC project approval S-2013-183).

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Authors and Affiliations

  1. Southern Seas Ecology Laboratories, School of Biological Sciences and Environment Institute, University of Adelaide, Adelaide, SA, 5005, Australia

    Kayla L. Gilmore, Zoe A. Doubleday & Bronwyn M. Gillanders

Authors
  1. Kayla L. Gilmore
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  2. Zoe A. Doubleday
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  3. Bronwyn M. Gillanders
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Contributions

KLG, BMG and ZAD conceived the experiment, KLG was responsible for the design of the experiment, performing the experiment and analysing data. KLG wrote the manuscript; BMG and ZAD were crucial in reviewing work and provided editorial advice.

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Correspondence to Kayla L. Gilmore.

Additional information

Communicated by Donovan P. German.

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Gilmore, K.L., Doubleday, Z.A. & Gillanders, B.M. Testing hypoxia: physiological effects of long-term exposure in two freshwater fishes. Oecologia 186, 37–47 (2018). https://doi.org/10.1007/s00442-017-3992-3

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  • DOI: https://doi.org/10.1007/s00442-017-3992-3

Keywords

  • Metabolic scope
  • Sub-lethal
  • Threshold limit
  • Acclimation
  • Water management