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A physiological approach to quantifying thermal habitat quality for Redband Rainbow Trout (Oncorhynchus mykiss gairdneri) in the south Fork John Day River, Oregon

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Abstract

We examined tissue-specific levels of heat shock protein 70 (hsp70) and whole body lipid levels in juvenile redband trout (Oncorhynchus mykiss gairdneri) from the South Fork of the John Day River (SFJD), Oregon, with the goal of determining if these measures could be used as physiological indicators of thermal habitat quality for juvenile redband trout. Our objectives were to determine the hsp70 induction temperature in liver, fin, and white muscle tissue and characterize the relation between whole body lipids and hsp70 for fish in the SFJD. We found significant increases in hsp70 levels between 19 and 22°C in fin, liver, and white muscle tissue. Maximum hsp70 levels in liver, fin, and white muscle tissue occurred when mean weekly maximum temperatures (MWMT) exceeded 20–22°C. In general, the estimated hsp70 induction temperature for fin and white muscle tissue was higher than liver tissue. Whole body lipid levels began to decrease when MWMT exceeded 20.4°C. There was a significant interaction between temperature and hsp70 in fin and white muscle tissue, but not liver tissue. Collectively, these results suggest that increased hsp70 levels in juvenile redband trout are symptomatic of thermal stress, and that energy storage capacity decreases with this stress. The possible decrease in growth potential and fitness for thermally stressed individuals emphasizes the physiological justification for thermal management criteria in salmon-bearing streams.

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References

  • Allen PJ, Hodge B, Werner I, Cech JJ Jr (2006) Effects of ontogeny, season, and temperature on the swimming performance of juvenile green surgeon (Acipenser medirostris). Can J Fish Aquat Sci 63:1360–1369

    Article  Google Scholar 

  • Anthony JA, Roby DD, Turco KR (2000) Lipid content and energy density of forage fishes from the northern Gulf of Alaska. J Exp Mar Biol Ecol 248:53–78

    Article  CAS  PubMed  Google Scholar 

  • Baltz DM, Vondracek B, Brown LR, Moyle PB (1987) Influence of temperature on microhabitat choice by fishes in a California stream. Trans Am Fish Soc 116:12–20

    Article  Google Scholar 

  • Behnke RJ, American Fisheries Society (1992) Native trout of western North America. American Fisheries Society, Bethesda

    Google Scholar 

  • Beitinger TL, Bennett WA, McCauley RW (2000) Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ Biol Fish 58:237–275

    Article  Google Scholar 

  • Ciechanover A, Schwartz AL (1998) The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc Natl Acad Sci USA 95:2727–2730

    Article  CAS  PubMed  Google Scholar 

  • Cunjak RA, Green JM (1986) Influence of water temperature on behavioural interactions between juvenile brook charr, Salvelinus fontinalus, and rainbow trout, Salmo gairdneri. Can J Zool 64:1288–1291

    Article  Google Scholar 

  • Department of Environmental Quality. Water Pollution, Division 41. Oregon's 2002 Integrated Report and 303(d) List. http://www.deq.state.or.us/WQ/assessment/rpt02.htm.Cited 17 December 2008

  • Department of Environmental Quality. Water Pollution, Division 41. OAR 340-041-0028. Water quality standards: beneficial uses, policies, and criteria for Oregon. http://www.deq.state.or.us/wq/standards/temperature.htm. Cited 17 December 2008

  • Fader SC, Yu Z, Spotila JR (1994) Seasonal variation in heat shock proteins (hsp70) in stream fish under natural condition. J Therm Biol 19:335–341

    Article  CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  PubMed  Google Scholar 

  • Feldhaus JF, Heppell SA, Mesa MA, Li H (2008) Hepatic hsp70 and Plasma Cortisol Levels in Rainbow Trout (Oncorhynchus mykiss) after tagging with a Passive Integrated Transponder. Trans Am Fish Soc 137:690–695

    Article  CAS  Google Scholar 

  • Forsyth RB, Candido EPM, Babich SL, Iwama GK (1997) Stress protein expression in coho salmon with bacterial kidney disease. J Aquat Anim Health 9:18–25

    Article  Google Scholar 

  • Fowler SL, Hamilton D, Currie S (2009) A comparison of the heat shock response in juvenile and adult rainbow trout (Oncorhynchus mykiss)—implications for increased thermal sensitivity with age. Can J Fish Aquat Sci 66:91–100

    Article  Google Scholar 

  • Gamperl AK, Rodnick KJ, Faust HA, Venn EC, Bennett MT, Crawshaw LI, Keeley ER, Powell MS, Li HW (2002) Metabolism, swimming performance, and tissue biochemistry of high desert redband trout (Oncorhynchus mykiss ssp): evidence for phenotypic differences in physiological function. Physiol Biochem Zool 75:413–431

    Article  CAS  PubMed  Google Scholar 

  • Hassanein HMA, Banhawy MA, Soliman FM, Abdel-Rehim SA, Muller WEG, Schroder HC (1999) Induction of hsp70 by the herbicide oxyfluorfen (goal) in the Egyptian Nile fish, Oreochromis niloticus. Arch Environ Contam Toxicol 37:78–84

    Article  CAS  PubMed  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University, New York

    Google Scholar 

  • Hofmann GE, Somero GN (1995) Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal mussel Mytilus trossulus. J Exp Biol 198:1509–1518

    CAS  PubMed  Google Scholar 

  • Hofmann GE, Somero GN (1996) Protein ubiquitination and stress protein synthesis in Mytilus trossulus occurs during recovery from tidal emersion. Mol Mar Biol Biotechnol 5:175–184

    CAS  Google Scholar 

  • Hughes NF, Grand TC (2000) Physiological ecology meets the ideal-free distribution: predicting the distribution of size-structured fish populations across temperature gradients. Environ Biol Fish 59:285–298

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li HW, Lamberti GA, Pearsons TN, Tait CK, Li JL, Buckhouse JC (1994) Cumulative effects of riparian disturbances along high desert trout streams of the John Day basin, Oregon. Trans Am Fish Soc 123:627–640

    Article  Google Scholar 

  • Linton TK, Morgan I (1998) Chronic exposure of rainbow trout (Oncorhynchus mykiss) to simulated climate warming and sublethal ammonia: A year-long study of their appetite, growth and metabolism. Can J Fish Aquat Sci 55:576–589

    Article  CAS  Google Scholar 

  • Lund SG, Caissie D, Cunjak RA, Vijayan MM, Tufts BL (2002) The effects of environmental heat stress on heat-shock mRNA and protein expression in Miramichi Atlantic salmon (Salmo salar) parr. Can J Fish Aquat Sci 59:1553–1562

    Article  CAS  Google Scholar 

  • Lund SG, Lund MEA, Tufts BL (2003) Red blood cell hsp 70 mRNA and protein as bioindicators of temperature stress in the brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60:460–470

    Article  CAS  Google Scholar 

  • Myrick CA, Cech JJ (2000) Swimming performances of four California stream fishes: temperature effects. Environ Biol Fish 58:289–295

    Article  Google Scholar 

  • Parsell DA, Lindquist S (1994) Heat shock proteins and stress tolerance. In: Morimoto RI, Tissiáeres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory, Plainview

    Google Scholar 

  • Railsback SF, Rose KA (1999) Bioenergetics modeling of stream trout growth: temperature and food consumption effects. Trans Am Fish Soc 128:241–256

    Article  Google Scholar 

  • Rechsteiner M (1987) Ubiquitin-mediated pathways for intracellular proteolysis. Annu Rev Cell Biol 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Reynolds S, Kunz T (2001) Standard methods for destructive composition analysis. In: Speakman JR (ed) Body composition analysis of animals: a handbook of non-destructive methods. Cambridge University, Cambridge

    Google Scholar 

  • Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23:49–75

    Article  CAS  PubMed  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Tait CK, Li JL, Lamberti GA, Pearsons TN, Li HW (1994) Relationships between riparian cover and the community structure of high desert streams. J N Am Benthol Soc 13:45–56

    Article  Google Scholar 

  • Tattam I (2006) Seasonal life history of Oncorhynchus mykiss in the South Fork John Day River basin. Oregon State University, Oregon, MS Thesis

    Google Scholar 

  • Torgersen CE, Price DM, Li HW, McIntosh BA (1999) Multiscale thermal refugia and stream habitat associations of Chinook salmon in northeastern Oregon. Ecol Appl 9:301–319

    Article  Google Scholar 

  • U.S. National Marine Fisheries Service (2007) Species lists. http://www.nwr.noaa.gov/ESA-Salmon-Listings/Salmon-Populations/upload/1pgr06-06.pdf. Cited May 2007

  • Viant MR, Werner I, Rosenblum ES, Gantner AS, Tjeerdema RS, Johnson ML (2003) Correlation between heat-shock protein induction and reduced metabolic condition in juvenile steelhead trout (Oncorhynchus mykiss) chronically exposed to elevated temperature. Fish Physiol Biochem 29:159–171

    Article  CAS  Google Scholar 

  • Vijayan MM, Pereira C, Forsyth RB, Kennedy CJ, Iwama GK (1997) Handling stress does not affect the expression of hepatic heat shock protein 70 and conjugation enzymes in rainbow trout treated with beta-naphthoflavone. Life Sci 61:117–127

    Article  CAS  PubMed  Google Scholar 

  • Vijayan MM, Pereira C, Kruzynski G, Iwama GK (1998) Sublethal concentrations of contaminant induce the expression of hepatic heat shock protein 70 in two salmonids. Aquat Toxicol 40:101–108

    Article  CAS  Google Scholar 

  • Werner I, Smith TB, Feliciano J, Johnson ML (2005) Heat shock proteins in juvenile steelhead reflect thermal conditions in the Navarro River watershed, California, USA. Trans Am Fish Soc 134:399–410

    Article  CAS  Google Scholar 

  • Werner I, Viant MR, Rosenblum ES, Gantner AS, Tjeerdema RS, Johnson ML (2006) Cellular responses to temperature stress in steelhead trout (Oncorhynchus mykiss) parr with different rearing histories. Fish Physiol Biochem 32:261–273

    Article  CAS  Google Scholar 

  • Zarate J, Bradley TM (2003) Heat shock proteins are not sensitive indicators of hatchery stress in salmon. Aquaculture 223:175–187

    Article  CAS  Google Scholar 

  • Zoellick BW (1999) Stream temperatures and the elevational distribution of redband trout in southwestern Idaho. Gt Basin Nat 59:136–143

    Google Scholar 

  • Zoellick BW (2004) Density and biomass of redband trout relative to stream shading and temperature in southwestern Idaho. West N Am Nat 64:18–26

    Google Scholar 

Download references

Acknowledgments

Funding for this research was obtained through grants from the US Department of the Interior and the National Oceanic and Atmospheric Administration (NOAA). We thank Chris Jordan (NOAA fisheries) and Michael Newsom (US Bureau of Reclamation) for their efforts to help secure funding. We thank C. Anthony, R. Chitwood, J.L. Feldhaus, F. Madriñan, L. Madsen, T. Momoda, M. Packard, I. Tattam, J. Osborne-Gowey, and many others for laboratory assistance, and scientific discussion. We thank G. Feist, K. Rodnick, and three anonymous reviewers for reviewing early manuscript drafts. This study followed the Institutional Animal Care and Use Committee guidelines at Oregon State University under permit #3080. The use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the US Government.

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  1. Joseph W. Feldhaus

    Present address: Oregon Department of Fish and Wildlife, Eastern Oregon University, 203 Badgley Hall, La Grande, OR, 97850, USA

Authors and Affiliations

  1. Oregon Cooperative Fish and Wildlife Research Unit, U.S. Geological Survey and Department of Fisheries and Wildlife, Oregon State University, 104 Nash Hall, Corvallis, OR, 97331-3803, USA

    Joseph W. Feldhaus & Hiram Li

  2. Department of Fisheries and Wildlife, Oregon State University, 104 Nash Hall, Corvallis, OR, 97331-3803, USA

    Scott A. Heppell

  3. U.S. Geological Survey, Western Fisheries Research Center, Columbia River Research Laboratory, 5501-A Cook-Underwood Road, Cook, WA, 98605, USA

    Matthew G. Mesa

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  1. Joseph W. Feldhaus
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Correspondence to Joseph W. Feldhaus.

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Feldhaus, J.W., Heppell, S.A., Li, H. et al. A physiological approach to quantifying thermal habitat quality for Redband Rainbow Trout (Oncorhynchus mykiss gairdneri) in the south Fork John Day River, Oregon. Environ Biol Fish 87, 277–290 (2010). https://doi.org/10.1007/s10641-010-9580-6

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