Abstract
Bull trout (Salvelinus confluentus) are a thermally sensitive cold-water species with a threatened conservation status across much of North America. To improve our understanding of bull trout thermal ecology, we tagged more than 150 adults with temperature-sensing acoustic biotelemetry transmitters and monitored the animals in a British Columbia reservoir for two years. Thermal resource selection was estimated in open water from the summer to autumn as the system transitioned to isothermal conditions. On average, bull trout thermal history tracked seasonal changes and remained close to the optimum temperatures for growth and metabolism. As summer progressed, bull trout increasingly selected temperatures of 11–15 °C as they became less available within the water column. Selection indicated the movement to shallower waters where 11–15 °C temperatures existed. The results show that bull trout mainly occupy a narrow range of temperatures which suggests the importance of cold-water refuge for the species.
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References
Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268
Arthur SM, Manly BFJ, McDonald LL, Garner GW (1996) Assessing habitat selection when availability changes. Ecology 77:215. doi:10.2307/2265671
Beauchamp DA, Van Tassell JJ (2001) Modeling seasonal trophic interactions of adfluvial bull trout in Lake Billy Chinook, Oregon. Trans Am Fish Soc 130:204–216
Benjamin JR, Heltzel JM, Dunham JB et al (2016) Thermal regimes, nonnative trout, and their influences on native bull trout in the upper Klamath River basin, Oregon. Trans Am Fish Soc 145:1318–1330. doi:10.1080/00028487.2016.1219677
Bray KE (2002) Fish derby summary: Shelter Bay, Nakusp, and Mica 1997–2001. British Columbia, Revelstoke
Bray K (2012) Kinbasket and Revelstoke reservoirs ecological productivity monitoring. Progress report year 2 (2010), CLBMON-3. BC Hydro: Burnaby
Brett JR (1971) Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am Zool 11:99–113
Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology. Academic Press, New York, pp 279–352
Burnham K, Anderson D (2004) Multimodel inference understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304
Cartamil DP, Lowe CG (2004) Diel movement patterns of ocean sunfish Mola mola off southern California. Mar Ecol Prog Ser 266:245–253
COSEWIC (2012) COSEWIC assessment and status report on the bull trout Salvelinus confluentus in Canada. Ottawa
Cuenco ML, Stickney RR, Grant WE (1985) Fish bioenergetics and growth in aquaculture ponds: II. Effects of interactions among, size, temperature, dissolved oxygen, unionized ammonia and food on growth of individual fish. Ecol Model 27:191–206. doi:10.1016/0304-3800(85)90002-X
Díaz JA, Cabezas-Díaz S (2004) Seasonal variation in the contribution of different behavioural mechanisms to lizard thermoregulation. Funct Ecol 18:867–875
Downes S (2001) Trading heat and food for safety: costs of predator avoidance in a lizard. Ecology 82:2870. doi:10.2307/2679967
Dunham AE, Grant BW, Overall KL (1989) Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectotherms. Physiol Zool 62:335–355
Dunham J, Rieman B, Chandler G (2003) Influences of temperature and environmental variables on the distribution of bull trout within streams at the southern margin of its range margin of its range. North Am J Fish Manag 23:894–904. doi:10.1577/M02-028
Eckmann M, Dunham J, Connor EJ & Welch CA (2016) Bioenergetic evaluation of diel vertical migration by bull trout (Salvelinus confluentus) in a thermally stratified reservoir. Ecol Freshw Fish. doi:10.1111/eff.12321
Elliot J, Allonby J (2013) An experimental study of ontonenetic and seasonal changes in the temperature preference of unfed and fed brown trout, Salmo trutta. Freshw Biol 58:1840–1848
Furey NB, Hinch SG, Mesa MG, Beauchamp DA (2016) Piscivorous fish exhibit temperature-influenced binge feeding during an annual prey pulse. J Anim Ecol 85:1307–1317. doi:10.1111/1365-2656.12565
Gillies CS, Hebblewhite M, Nielsen SE et al (2006) Application of random effects to the study of resource selection by animals: random effects in resource selection. J Anim Ecol 75:887–898. doi:10.1111/j.1365-2656.2006.01106.x
Godvik IMR, Loe LE, Vik JO et al (2009) Temporal scales, trade-offs, and functional responses in red deer habitat selection. Ecology 90:699–710
Gutowsky LFG, Harrison PM, Guimaraes Martins EE et al (2015) Interactive effects of sex and body size on Adfluvial bull trout (Salvelinus confluentus) movement ecology. Can J Zool. doi:10.1139/cjz-2015-0104
Gutowsky LFG, Harrison PM, Landsman SJ et al (2011) Injury and immediate mortality associated with recreational troll capture of bull trout (Salvelinus confluentus) in a reservoir in the Kootenay-Rocky Mountain region of British Columbia. Fish Res 109:379–383. doi:10.1016/j.fishres.2011.02.022
Gutowsky LFG, Harrison PM, Martins EG et al (2013) Diel vertical migration hypotheses explain size-dependent behavior in a freshwater piscivore. Anim Behav 86:365–373. doi:10.1016/j.anbehav.2013.05.027
Harrison PM, Gutowsky LFG, Martins EG et al (2013) Diel vertical migration of adult burbot: a dynamic trade-off between feeding opportunity, predator avoidance, and bioenergetic gain. Can J Fish Aquat Sci 70:1765–1774
Hertz PE (1992) Evaluating thermal resource partitioning. Oecologia 90:127–136
Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. Am Nat 142:796–818
Heupel MR, Semmens JM, Hobday AJ (2006) Automated acoustic tracking of aquatic animals: scales, design and deployment of listening station arrays. Mar Freshw Res 57:1–13
Howell PJ, Dunham JB, Sankovich PM (2010) Relationships between water temperatures and upstream migration, cold water refuge use, and spawning of adult bull trout from the Lostine River, Oregon, USA. Ecol Freshw Fish 19:96–106. doi:10.1111/j.1600-0633.2009.00393.x
Huey RB (1991) Physiological consequences of habitat selection. Am Nat 137:S91–S115
Jensen OP, Hrabik TR, Martell SJ et al (2006) Diel vertical migration in the Lake superior pelagic community. II. Modeling trade-offs at an intermediate trophic level. Can J Fish Aquat Sci 63:2296–2307
Jones LA, Muhlfeld CC, Marshall LA et al (2014) Estimating thermal regimes of bull trout and assessing the potential effects of climate warming on critical habitats. River Res Appl 30:204–216. doi:10.1002/rra.2638
Kessel ST, Cooke SJ, Heupel MR et al (2013) A review of detection range testing in aquatic passive acoustic telemetry studies. Rev Fish Biol Fish 24:199–218. doi:10.1007/s11160-013-9328-4
Kovach RP, Muhlfeld CC, Wade AA et al (2015) Genetic diversity is related to climatic variation and vulnerability in threatened bull trout. Glob Chang Biol 21:2510–2524. doi:10.1111/gcb.12850
Kovach RP, Muhlfeld CC, Al-Chokhachy R, Dunham JB, Letcher BH, Kershner JL (2016) Impacts of climatic variation on trout: a global synthesis and path forward. Rev Fish Biol Fish 26(2):135–151
Magnuson JJ, Crowder LB, Medvick PA (1979) Temperature as an ecological resource. Am Zool 19:331–343
Maret TR, Schultz JE (2013) Bull trout (Salvelinus confluentus) movement in relation to water temperature, season, and habitat features in Arrowrock Reservoir, Idaho, 2012 (No. 2013-5158). US Geological Survey
Maret TE, Schultz JE (2014) Bull trout (Salvelinus confluentus) movement in relation to water temperature, season, and habitat features in Arrowrock reservoir, Idaho, 2012
Martins EG, Gutowsky LFG, Harrison PM et al (2014) Behavioral attributes of turbine entrainment risk for adult resident fish revealed by acoustic telemetry and state-space modeling. Anim Biotelemetry 2:13
McPhail JD, Baxter JS (1996) A review of bull trout (Salvelinus confluentus) life-history and habitat use in relation to compensation and improvement opportunities. Fisheries Management Report No. 104. Department of Zoology, University of British Columbia, Vancouver
Mehner T (2012) Diel vertical migration of freshwater fishes - proximate triggers, ultimate causes and research perspectives: diel vertical migration in freshwater fishes. Freshw Biol 57:1342–1359. doi:10.1111/j.1365-2427.2012.02811.x
Mesa MG, Weiland LK, Christiansen HE et al (2013) Development and evaluation of a bioenergetics model for bull trout. Trans Am Fish Soc 142:41–49. doi:10.1080/00028487.2012.720628
Morita K, Fukawaka M, Tanimata N Yamamura O (2010) Size-dependent thermal preference in a pelagic fish. Oikos 119(8):1265–1272
Mysterud A, Ims RA (1998) Functional responses in habitat use: availability influences relative use in trade-off situations. Ecology 79:1435–1441
Niezgoda G, Benfield MC, Sisak M, Anson P (2002) Tracking acoustic transmitters by code division multiple access (CDMA)-based telemetry. Hydrobiologia 483:275–286
Paragamian VL, Walters JP (2011) Bull trout (Salvelinus confluentus) movement in a transboundary river. J Freshw Ecol 26:65–76. doi:10.1080/02705060.2011.553854
Parker FL, Benedict BA, Tsai C (1975) Evaluation of mathematical models for temperature prediction in deep reservoirs. EPA 660/3-75-038. U.S. Environtal Protection Agency, Corvallis
Plumb JM, Blanchfield PJ (2009) Performance of temperature and dissolved oxygen criteria to predict habitat use by lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 66:2011–2023. doi:10.1139/F09-129
Poole G, Dunham J, Hicks M, et al (2001) Technical synthesis: scientific issues relating to temperature criteria for Salmon, Trout, and Char Native to the Pacific Northwest. EPA 910-R-01-007. U.S. Environtal Protection Agency, Seattle
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Rieman BE, Isaak D, Adams S et al (2007) Anticipated climate warming effects on bull trout habitats and populations across the interior Columbia River basin. Trans Am Fish Soc 136:1552–1565. doi:10.1577/T07-028.1
Robertson CB, Langford MT, Zhu DZ, Leake A (2011) Reservoir thermal structure and its effect on hydropower operation induced fish entrainment. In World Environmental and Water Resources Congress 2011: Bearing Knowledge for Sustainability, pp. 2449–2458
Rogers KB, White GC (2007) Analysis of movement and habitat use from telemetry data. In: Guy CS, Brown ML (eds) Analysis and interpretation of freshwater fisheries data. Bethesda, American Fisheries Society, pp 625–676
Roughgarden J, Porter W, Heckel D (1981) Resource partitioning of space and its relationship to body temperature in Anolis lizard populations. Oecologia 50:256–264
Selong JH, McMahon TE, Zale AV, Barrows FT (2001) Effect of temperature on growth and survival of bull trout, with application of an improved method for determining thermal tolerance in fishes. Trans Am Fish Soc 130:1026–1037
Shroyer SM, Logsdon DE (2009) Detection distances of selected radio and acoustic tags in Minnesota lakes and rivers. North Am J Fish Manag 29:876–884
Simpfendorfer CA, Heupel MR, Hueter RE (2002) Estimation of short-term centers of activity from an array of omnidirectional hydrophones and its use in studying animal movements. Can J Fish Aquat Sci 59:23–32. doi:10.1139/f01-191
Sims DW, Wearmouth VJ, Genner MJ et al (2004) Low-temperature driven early spawning migration of a temperate marine fish. J Anim Ecol 73:333–341
Sims DW, Wearmouth VJ, Southall EJ et al (2006) Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark. J Anim Ecol 75:176–190. doi:10.1111/j.1365-2656.2005.01033.x
Storebakken T, Austreng E (1987) Ration level for salmonids: II. Growth, feed intake, protein digestibility, body composition, and feed conversion in rainbow trout weighing 0.5–1.0 kg. Aquaculture 60:207–221. doi:10.1016/0044-8486(87)90288-2
Swanberg TR (1997) Movements of and habitat use by fluvial bull trout in the Blackfoot River, Montana. Trans Am Fish Soc 126:735–746. doi:10.1577/1548-8659(1997)126<0735
Tracy CR, Christian KA (1986) Ecological relations among space, time, and thermal niche axes. Ecology 67:609. doi:10.2307/1937684
USFWS (2015) Recovery plan for the coterminous United States population of bull trout (Salvelinus confluentus). US Fish and Wildlife Service. Portland, Oregon
Wagner GN, Cooke SJ, Brown RS, Deters KA (2011) Surgical implantation techniques for electronic tags in fish. Rev Fish Biol Fish 21:71–81
Wildhaber ML, Crowder LB (1990) Testing a bioenergetics-based habitat choice model: bluegill (Lepomis macrochirus) responses to food availability and temperature. Can J Fish Aquat Sci 47:1664–1671
Wilhelm FM, Parker BR, Schindler DW, Donald DB (1999) Seasonal food habits of bull trout from a small alpine lake in the Canadian Rocky Mountains. Trans Am Fish Soc 128:1176–1192. doi:10.1577/1548-8659(1999)128<1176:SFHOBT>2.0.CO;2
Wood SN (2000) Modelling and smoothing parameter estimation with multiple quadratic penalties. J R Stat Soc Ser B Stat Methodol 62:413–428
Wood S (2006) Generalized additive models: an introduction with R. CRC Press, Boca Raton
Zuur AF, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Zuur AF, Saveliev AA, Ieno EN (2014) A beginner’s guide to generalised additive mixed models with R. Highland Statistics Ltd, Newburgh
Acknowledgements
We would like to thank Sean Landsman, Jason Thiem, Jeff Nitychoruk, Mark Taylor, Juan Molina, Taylor Nettles and Karen Bray. Thanks to our boat driver and friend Jamie Tippe. We would also like to thank Rick Chartraw for his hospitality. We thank the BC Ministry of Environment for issuing the necessary permits to carry out this study. This work was supported by BC Hydro, the Natural Sciences and Engineering Research Council (through NSERC HydroNet, grant number CRDPJ 387271-09 and NSERC DGs to Cooke and Power) and Fisheries and Oceans Canada (through the Centre of Expertise on Hydropower Impacts of Fish). Cooke is further supported by the Canada Research Chairs Program. All tagging procedures were approved by the Carleton University Animal Care Committee. Fish were obtained under the scientific collection permits issues by the British Columbia Ministry of Environment (Permit No. CB-PG10-61414).
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LFGG and PMH conceived and designed the study. LFGG, PMH, EGM, DAP and SJC performed field work. LFGG and EGM performed the analyses. LFGG and SJC wrote the manuscript; all other authors contributed editorial advice.
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Gutowsky, L.F.G., Harrison, P.M., Martins, E.G. et al. Daily temperature experience and selection by adfluvial bull trout (Salvelinus confluentus). Environ Biol Fish 100, 1167–1180 (2017). https://doi.org/10.1007/s10641-017-0634-x
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Keywords
- Charr
- Resource selection function
- Habitat selection
- Thermal history