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Research Article

Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation

Jennifer M. Sunday, Amanda E. Bates, Michael R. Kearney, Robert K. Colwell, Nicholas K. Dulvy, John T. Longino, and Raymond B. Huey
  1. aBiodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
  2. bEarth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6;
  3. cOcean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO14 3ZH, United Kingdom;
  4. dSchool of Life and Environmental Sciences, Deakin University, Warrnambool, VIC 3280, Australia;
  5. eDepartment of Zoology, University of Melbourne, Parkville, VIC 3010, Australia;
  6. fDepartment of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269;
  7. gUniversity of Colorado Museum of Natural History, Boulder, CO 80309;
  8. hDepartment of Biology, University of Utah, Salt Lake City, UT 84112; and
  9. iDepartment of Biology, University of Washington, Seattle, WA 98195

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PNAS first published March 10, 2014; https://doi.org/10.1073/pnas.1316145111
Jennifer M. Sunday
aBiodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
bEarth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6;
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  • For correspondence: sunday@zoology.ubc.ca
Amanda E. Bates
cOcean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO14 3ZH, United Kingdom;
dSchool of Life and Environmental Sciences, Deakin University, Warrnambool, VIC 3280, Australia;
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Michael R. Kearney
eDepartment of Zoology, University of Melbourne, Parkville, VIC 3010, Australia;
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Robert K. Colwell
fDepartment of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269;
gUniversity of Colorado Museum of Natural History, Boulder, CO 80309;
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Nicholas K. Dulvy
bEarth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6;
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John T. Longino
hDepartment of Biology, University of Utah, Salt Lake City, UT 84112; and
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Raymond B. Huey
iDepartment of Biology, University of Washington, Seattle, WA 98195
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  1. Edited by James H. Brown, University of New Mexico, Albuquerque, NM, and approved February 3, 2014 (received for review August 31, 2013)

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Significance

We find that most terrestrial ectotherms are insufficiently tolerant of high temperatures to survive the warmest potential body temperatures in exposed habitats and must therefore thermoregulate by using shade, burrows, or evaporative cooling. Our results reveal that exposure to extreme heat can occur even at high elevations and latitudes and show why heat-tolerance limits are relatively invariant in comparison with cold limits. To survive climate warming, ectotherms in most areas may need to rely on behaviors—and have access to habitats—that provide a reprieve from extreme operative temperatures.

Abstract

Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species’ vulnerability to climate warming and extreme events.

  • macrophysiology
  • operative temperature
  • climate sensitivity

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: sunday{at}zoology.ubc.ca.
  • Author contributions: J.M.S., A.E.B., R.K.C., N.K.D., J.T.L., and R.B.H. designed research; J.M.S. and A.E.B. performed research; A.E.B. and M.R.K. contributed new reagents/analytic tools; J.M.S., A.E.B., and R.B.H. analyzed data; and J.M.S., A.E.B., M.R.K., R.K.C., N.K.D., J.T.L., and R.B.H. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1316145111/-/DCSupplemental.

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Behavior thwarts thermal danger
Jennifer M. Sunday, Amanda E. Bates, Michael R. Kearney, Robert K. Colwell, Nicholas K. Dulvy, John T. Longino, Raymond B. Huey
Proceedings of the National Academy of Sciences Mar 2014, 201316145; DOI: 10.1073/pnas.1316145111

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Behavior thwarts thermal danger
Jennifer M. Sunday, Amanda E. Bates, Michael R. Kearney, Robert K. Colwell, Nicholas K. Dulvy, John T. Longino, Raymond B. Huey
Proceedings of the National Academy of Sciences Mar 2014, 201316145; DOI: 10.1073/pnas.1316145111
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