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The importance of warm habitat to the growth regime of cold-water fishes

Nature Climate Change volume 11, pages 354–361 (2021)Cite this article

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Abstract

A common goal of biological adaptation planning is to identify and prioritize locations that remain suitably cool during the summer. This implicitly devalues areas that are ephemerally warm, even if they are suitable most of the year for mobile animals. Here we develop an alternative conceptual framework, the growth regime, which considers seasonal and landscape variation in physiological performance, focusing on riverine fish. Using temperature models for 14 river basins, we show that growth opportunities propagate up and down river networks on a seasonal basis, and that downstream habitats that are suboptimally warm in summer may actually provide the majority of growth potential expressed annually. We demonstrate with an agent-based simulation that the shoulder-season use of warmer downstream habitats can fuel annual fish production. Our work reveals a synergy between cold and warm habitats that could be fundamental to support cold-water fisheries, and highlights the risk in conservation strategies that underappreciate warm habitats.

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Fig. 1: Example of how freshwater climate change adaptation devalues ephemerally warm habitats.
Fig. 2: The growth regime of rivers and its implications for mobile fish.
Fig. 3: Seasonal variation in the landscape patterning of fish growth potential in the John Day River Basin, Oregon.
Fig. 4: Variation among riverscape growth regimes.
Fig. 5: Results from an individual-based growth simulation in which the fish ration increased with stream size.

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Data availability

The Oregon stream temperatures used in Fig. 1 were sourced from 58 sites monitored by the Oregon Department of Environmental Quality and 17 sites monitored by The United States Geological Survey. These data are publicly available at https://www.oregon.gov/deq/wq/Pages/WQdata.aspx and https://waterdata.usgs.gov/nwis/sw, respectively. The water temperature data used in Figs. 2–4 are posted on GitHub at https://github.com/chris3jordan/Growth-Potential.

Code availability

The code for processing water temperature and growth potential data for Figs. 2–4 is posted on GitHub at https://github.com/chris3jordan/Growth-Potential. The code for the numerical simulation is posted on GitHub at https://github.com/aimeefullerton/growth_regime_IBM.

References

  1. Isaak, D. J., Young, M. K., Nagel, D. E., Horan, D. L. & Groce, M. C. The cold-water climate shield: delineating refugia for preserving salmonid fishes through the 21st century. Glob. Change Biol. 21, 2540–2553 (2015).

    Article  Google Scholar 

  2. Tabor, K. & Williams, J. W. Globally downscaled climate projections for assessing the conservation impacts of climate change. Ecol. Appl. 20, 554–565 (2010).

    Article  Google Scholar 

  3. Small-Lorenz, S. L., Culp, L. A., Ryder, T. B., Will, T. C. & Marra, P. P. A blind spot in climate change vulnerability assessments. Nat. Clim. Change 3, 91–93 (2013).

    Article  Google Scholar 

  4. Runge, C. A., Martin, T. G., Possingham, H. P., Willis, S. G. & Fuller, R. A. Conserving mobile species. Front. Ecol. Environ. 12, 395–402 (2014).

    Article  Google Scholar 

  5. Sears, M. W., Raskin, E. & Angilletta, M. J. The world is not flat: defining relevant thermal landscapes in the context of climate change. Integr. Comp. Biol. 51, 666–675 (2011).

    Article  Google Scholar 

  6. Ebersole, J. L., Liss, W. J. & Frissell, C. A. Thermal heterogeneity, stream channel morphology, and salmonid abundance in northeastern Oregon streams. Can. J. Fish. Aquat. Sci. https://doi.org/10.1139/f03-107 (2011).

  7. Baldock, J. R., Armstrong, J. B., Schindler, D. E. & Carter, J. L. Juvenile coho salmon track a seasonally shifting thermal mosaic across a river floodplain. Freshw. Biol. 61, 1454–1465 (2016).

    Article  CAS  Google Scholar 

  8. Armstrong, J. B. & Schindler, D. E. Going with the flow: spatial distributions of juvenile coho salmon track an annually shifting mosaic of water temperature. Ecosystems 16, 1429–1441 (2013).

    Article  CAS  Google Scholar 

  9. Wurtsbaugh, W. A. & Neverman, D. Post-feeding thermotaxis and daily vertical migration in a larval fish. Nature 333, 846–848 (1988).

    Article  Google Scholar 

  10. Thompson, L. M., Staudinger, M. D. & Carter, S. L. Summarizing Components of US Department of the Interior Vulnerability Assessments to Focus Climate Adaptation Planning Open-File Report 2015–1110 (US Geological Survey, 2015).

  11. Bottrill, M. C. et al. Is conservation triage just smart decision making? Trends Ecol. Evol. 23, 649–654 (2008).

    Article  Google Scholar 

  12. Pacifici, M. et al. Assessing species vulnerability to climate change. Nat. Clim. Change 5, 215–224 (2015).

    Article  Google Scholar 

  13. Brady, M. E., Chione, A. M. & Armstrong, J. B. Missing pieces in the full annual cycle of fish ecology: a systematic review of the phenology of freshwater fish research. Preprint at bioRxiv https://doi.org/10.1101/2020.11.24.395665 (2020).

  14. Marra, P. P., Cohen, E. B., Loss, S. R., Rutter, J. E. & Tonra, C. M. A call for full annual cycle research in animal ecology. Biol. Lett. 11, 20150552 (2015).

    Article  Google Scholar 

  15. Smeraldo, S. et al. Ignoring seasonal changes in the ecological niche of non-migratory species may lead to biases in potential distribution models: lessons from bats. Biodivers. Conserv. 27, 2425–2441 (2018).

    Article  Google Scholar 

  16. Magnuson, J. J., Crowder, L. B. & Medvick, P. A. Temperature as an ecological resource. Integr. Comp. Biol. 19, 331–343 (1979).

    Google Scholar 

  17. Isaak, D. J., Wenger, S. J. & Young, M. K. Big biology meets microclimatology: defining thermal niches of ectotherms at landscape scales for conservation planning. Ecol. Appl. 27, 977–990 (2017).

    Article  Google Scholar 

  18. Poole, G. C. et al. The case for regime-based water quality standards. BioScience 54, 155–161 (2004).

    Article  Google Scholar 

  19. Pauly, S., Soriano-Bartz, M., Moreau, J. & Jarre-Teichmann, A. A new model accounting for seasonal cessation of growth in fishes. Mar. Freshw. Res. 43, 1151–1156 (1992).

    Article  Google Scholar 

  20. Brett, J. R. Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerkd). Integr. Comp. Biol. 11, 99–113 (1971).

    Google Scholar 

  21. Armstrong, J. B. & Schindler, D. E. Excess digestive capacity in predators reflects a life of feast and famine. Nature 476, 84–87 (2011).

    Article  CAS  Google Scholar 

  22. Childress, E. S. & Letcher, B. H. Estimating thermal performance curves from repeated field observations. Ecology 98, 1377–1387 (2017).

    Article  Google Scholar 

  23. Neuheimer, A. B., Thresher, R. E., Lyle, J. M. & Semmens, J. M. Tolerance limit for fish growth exceeded by warming waters. Nat. Clim. Change 1, 110–113 (2011).

    Article  Google Scholar 

  24. Lusardi, R. A., Hammock, B. G., Jeffres, C. A., Dahlgren, R. A. & Kiernan, J. D. Oversummer growth and survival of juvenile coho salmon (Oncorhynchus kisutch) across a natural gradient of stream water temperature and prey availability: an in situ enclosure experiment. Can. J. Fish. Aquat. Sci. https://doi.org/10.1139/cjfas-2018-0484 (2019).

  25. Sunday, J. M. et al. Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc. Natl Acad. Sci. USA 111, 5610–5615 (2014).

    Article  CAS  Google Scholar 

  26. Tattam, I. A., Li, H. W., Giannico, G. R. & Ruzycki, J. R. Seasonal changes in spatial patterns of Oncorhynchus mykiss growth require year-round monitoring. Ecol. Freshw. Fish 26, 434–443 (2017).

    Article  Google Scholar 

  27. Munch, S. B. & Conover, D. O. Accounting for local physiological adaptation in bioenergetic models: testing hypotheses for growth rate evolution by virtual transplant experiments. Can. J. Fish. Aquat. Sci. https://doi.org/10.1139/f02-013 (2011).

  28. Eliason, E. J. et al. Differences in thermal tolerance among sockeye salmon populations. Science 332, 109–112 (2011).

    Article  CAS  Google Scholar 

  29. Forseth, T. et al. Thermal growth performance of juvenile brown trout Salmo trutta: no support for thermal adaptation hypotheses. J. Fish Biol. 74, 133–149 (2009).

    Article  CAS  Google Scholar 

  30. Kaeding, L. R. & Kaya, C. M. Growth and diets of trout from contrasting environments in a geothermally heated stream: the Firehole River of Yellowstone National Park. Trans. Am. Fish. Soc. 107, 432–438 (1978).

    Article  Google Scholar 

  31. Armstrong, J. B., Ward, E. J., Schindler, D. E. & Lisi, P. J. Adaptive capacity at the northern front: sockeye salmon behaviourally thermoregulate during novel exposure to warm temperatures. Conserv. Physiol. 4, cow039 (2016).

    Article  Google Scholar 

  32. Petty, J. T., Thorne, D., Huntsman, B. M. & Mazik, P. M. The temperature–productivity squeeze: constraints on brook trout growth along an Appalachian river continuum. Hydrobiologia 727, 151–166 (2014).

    Article  CAS  Google Scholar 

  33. Sommer, T. R., Harrell, W. C. & Nobriga, M. L. Habitat use and stranding risk of juvenile chinook salmon on a seasonal floodplain. North Am. J. Fish. Manag. 25, 1493–1504 (2005).

    Article  Google Scholar 

  34. Hayes, S. A. et al. Steelhead growth in a small central California watershed: upstream and estuarine rearing patterns. Trans. Am. Fish. Soc. 137, 114–128 (2008).

    Article  Google Scholar 

  35. Patrick, C. J. et al. Precipitation and temperature drive continental-scale patterns in stream invertebrate production. Sci. Adv. 5, eaav2348 (2019).

    Article  CAS  Google Scholar 

  36. Mejia, F. H. et al. Stream metabolism increases with drainage area and peaks asynchronously across a stream network. Aquat. Sci. 81, 9 (2018).

    Article  Google Scholar 

  37. Kaylor, M. J., White, S. M., Saunders, W. C. & Warren, D. R. Relating spatial patterns of stream metabolism to distributions of juveniles salmonids at the river network scale. Ecosphere 10, e02781 (2019).

    Article  Google Scholar 

  38. McNyset, K. M., Volk, C. J. & Jordan, C. E. Developing an effective model for predicting spatially and temporally continuous stream temperatures from remotely sensed land surface temperatures. Water 7, 6827–6846 (2015).

    Article  Google Scholar 

  39. Selong, J. H., McMahon, T. E., Zale, A. V. & Barrows, F. T. 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 (2001).

    Article  Google Scholar 

  40. Mesa, M. G., Weiland, L. K., Christiansen, H. E., Sauter, S. T. & Beauchamp, D. A. Development and evaluation of a bioenergetics model for bull trout. Trans. Am. Fish. Soc. 142, 41–49 (2013).

    Article  CAS  Google Scholar 

  41. Muhlfeld, C. C. & Marotz, B. Seasonal movement and habitat use by subadult bull trout in the upper flathead river system, Montana. North Am. J. Fish. Manag. 25, 797–810 (2005).

    Article  Google Scholar 

  42. Guzzo, M. M., Blanchfield, P. J. & Rennie, M. D. Behavioral responses to annual temperature variation alter the dominant energy pathway, growth, and condition of a cold-water predator. Proc. Natl Acad. Sci. USA 114, 9912–9917 (2017).

    Article  CAS  Google Scholar 

  43. Downing, J. A. et al. Global abundance and size distribution of streams and rivers. Inland Waters 2, 229–236 (2012).

    Article  Google Scholar 

  44. Tockner, K., Malard, F. & Ward, J. V. An extension of the flood pulse concept. Hydrol. Process. 14, 2861–2883 (2000).

    Article  Google Scholar 

  45. Fullerton, A. H. et al. Hydrological connectivity for riverine fish: measurement challenges and research opportunities. Freshw. Biol. 55, 2215–2237 (2010).

    Article  Google Scholar 

  46. Fullerton, A. H. et al. Simulated juvenile salmon growth and phenology respond to altered thermal regimes and stream network shape. Ecosphere 8, e02052 (2017).

    Article  Google Scholar 

  47. Rand, P. S., Stewart, D. J., Seelbach, P. W., Jones, M. L. & Wedge, L. R. Modeling steelhead population energetics in Lakes Michigan and Ontario. Trans. Am. Fish. Soc. 122, 977–1001 (1993).

    Article  Google Scholar 

  48. Steel, E. A., Sowder, C. & Peterson, E. E. Spatial and temporal variation of water temperature regimes on the Snoqualmie River network. J. Am. Water Resour. Assoc. 52, 769–787 (2016).

    Article  Google Scholar 

  49. Armstrong, J. B. et al. Diel horizontal migration in streams: juvenile fish exploit spatial heterogeneity in thermal and trophic resources. Ecology 94, 2066–2075 (2013).

    Article  Google Scholar 

  50. Brewitt, K. S., Danner, E. M. & Moore, J. W. Hot eats and cool creeks: juvenile Pacific salmonids use mainstem prey while in thermal refuges. Can. J. Fish. Aquat. Sci. https://doi.org/10.1139/cjfas-2016-0395 (2017).

  51. Pépino, M., Goyer, K. & Magnan, P. Heat transfer in fish: are short excursions between habitats a thermoregulatory behaviour to exploit resources in an unfavourable thermal environment? J. Exp. Biol. 218, 3461–3467 (2015).

    Google Scholar 

  52. Warren, D. R., Robinson, J. M., Josephson, D. C., Sheldon, D. R. & Kraft, C. E. Elevated summer temperatures delay spawning and reduce redd construction for resident brook trout (Salvelinus fontinalis). Glob. Change Biol. 18, 1804–1811 (2012).

    Article  Google Scholar 

  53. Schlosser, I. J. Stream fish ecology: a landscape perspective. BioScience 41, 704–712 (1991).

    Article  Google Scholar 

  54. Lucero, Y., Steel, E. A., Burnett, K. M. & Christiansen, K. Untangling human development and natural gradients: implications of underlying correlation structure for linking landscapes and riverine ecosystems. River Syst. 19, 207–224 (2011).

    Article  Google Scholar 

  55. Muhlfeld, C. C. et al. Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout. Glob. Change Biol. 23, 4663–4674 (2017).

    Article  Google Scholar 

  56. Hitt, N. P., Snook, E. L. & Massie, D. L. Brook trout use of thermal refugia and foraging habitat influenced by brown trout. Can. J. Fish. Aquat. Sci. https://doi.org/10.1139/cjfas-2016-0255 (2016).

  57. Eaton, J. G. & Scheller, R. M. Effects of climate warming on fish thermal habitat in streams of the United States. Limnol. Oceanogr. 41, 1109–1115 (1996).

    Article  Google Scholar 

  58. Rieman, B. E. et al. Anticipated climate warming effects on bull trout habitats and populations across the interior Columbia River basin. Trans. Am. Fish. Soc. 136, 1552–1565 (2007).

    Article  Google Scholar 

  59. Starcevich, S. J., Howell, P. J., Jacobs, S. E. & Sankovich, P. M. Seasonal movement and distribution of fluvial adult bull trout in selected watersheds in the mid-Columbia River and Snake River basins. PLoS ONE 7, e37257 (2012).

    Article  CAS  Google Scholar 

  60. Hanson, P. C., Johnson, T. B., Schindler, D. E., & Kitchell, J. F. Fish Bioenergetics 3.0 for Windows (ASC, 1997).

  61. Hawkins, B. L., Fullerton, A. H., Sanderson, B. L. & Steel, E. A. Individual-based simulations suggest mixed impacts of warmer temperatures and a nonnative predator on Chinook salmon. Ecosphere 11, e03218 (2020).

    Article  Google Scholar 

  62. Crawford, S. S. & Muir, A. M. Global introductions of salmon and trout in the genus Oncorhynchus: 1870-2007. Rev. Fish Biol. Fisher 18, 313–344 (2008).

    Article  Google Scholar 

  63. Beauchamp, D. A. et al. Bioenergetic responses by Pacific salmon to climate and ecosystem variation. N. Pac. Anadr. Fish Comm. Bull. 4, 257–269 (2007).

    Google Scholar 

  64. Independent Scientific Advisory Board Density Dependence and its Implications for Fish Management and Restoration Programs in the Columbia River Basin ISAB 2015-1 (Northwest Power and Conservation Council, 2015).

  65. Railsback, S. F. & Rose, K. A. Bioenergetics modeling of stream trout growth: temperature and food consumption effects. Trans. Am. Fish. Soc. 128, 241–256 (1999).

    Article  Google Scholar 

  66. Van Winkle, W. et al. Individual-based model of sympatric populations of brown and rainbow trout for instream flow assessment: model description and calibration. Ecol. Model. 110, 175–207 (1998).

    Article  Google Scholar 

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Acknowledgements

We thank the many people (particularly D. Isaak) who have developed thermal mapping techniques and associated frameworks to identify climate refugia. Although we raise concerns about certain extensions of these techniques, we recognize them as the foundation on which further refinements can be applied. G. Pess, J.M. Kershner and others provided helpful feedback.

Author information

Authors and Affiliations

  1. Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR, USA

    Jonathan B. Armstrong & Ivan Arismendi

  2. NOAA Northwest Fisheries Science Center, Seattle, WA, USA

    Aimee H. Fullerton & Chris E. Jordan

  3. US Environmental Protection Agency, Corvallis, OR, USA

    Joseph L. Ebersole

  4. Pacific Northwest Research Station, US Forest Service, Juneau, AK, USA

    J. Ryan Bellmore

  5. Pacific Northwest Research Station, US Forest Service, Corvallis, OR, USA

    Brooke E. Penaluna & Gordon H. Reeves

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  1. Jonathan B. Armstrong
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Contributions

J.L.E. and J.B.A. conceived project; J.B.A., J.L.E., J.R.B. and A.H.F. outlined paper, A.H.F. developed the simulations, C.E.J. and J.B.A. analysed the growth potential from weekly landscape temperature data, J.L.E. and I.A. compiled and analysed temperature data for Fig. 1, J.R.B. and A.H.F. developed the two-patch growth model for Fig. 2, B.E.P. and G.H.R. helped research the current state of freshwater climate adaptation planning and refined the paper outline. J.B.A. led the writing of the manuscript. All the authors helped revise the manuscript and analyses.

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Correspondence to Jonathan B. Armstrong.

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The authors declare no competing interests.

Additional information

Peer review information Nature Climate Change thanks Nann Fangue, Clint Muhlfeld and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Bi-weekly changes in the landscape patterning of fish growth potential for the John Day River Basin, Oregon, USA.

Maps show growth potential (grams fish•wk1) for a cold-water fish (bull trout) based on mean weekly temperature.

Extended Data Fig. 2 River network used in simulation of fish movement and foraging.

(a) Maximum water temperature during summer throughout the hypothetical stream network; (b) reaches that were accessible to fish during simulations, classified as seasonally warm (>20 °C) or perennially cold (<20 °C); and (c) ration of food available to fish in each reach before density effects occurred.

Extended Data Fig. 3 Parameters used in individual-based model.

Parameters used in individual-based model.

Extended Data Fig. 4 Sensitivity analysis for simulation model.

Sensitivity of fish production in all habitats (open bars) and in seasonally warm habitats (SWH; hatched bars) to perturbations of parameter values. Bars reflect the difference in total growth between the baseline scenario with nominal parameter values and a scenario with a particular parameter perturbation.

Extended Data Fig. 5 Simulation results from the individual based fish model for each of 4 scenarios.

a, Proportion of time during each season that fish occupied stream reaches classified by their maximum summer temperature; (b) trajectories of individual fish growth throughout the year, colored by the water temperature they experienced at each time step; (c) trajectories of individual fish mass throughout the year, colored by their presence in either a seasonally warm (>20 °C during summer) or perennially cold (< 20 °C) habitat; and (d) mass accrued overall and in different thermal habitats, where boxes represent variance across 500 simultaneously simulated fish (horizontal lines are medians, box edges are interquartile ranges, whiskers are 95% percentiles, and points are outliers).

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Armstrong, J.B., Fullerton, A.H., Jordan, C.E. et al. The importance of warm habitat to the growth regime of cold-water fishes. Nat. Clim. Chang. 11, 354–361 (2021). https://doi.org/10.1038/s41558-021-00994-y

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