Beyond thermal limits: comprehensive metrics of performance identify key axes of thermal adaptation in ants
Abstract
Summary How species respond to temperature change depends in large part on their physiology. Physiological traits, such as critical thermal limits ( CT max and CT min ), provide estimates of thermal performance but may not capture the full impacts of temperature on fitness. Rather, thermal performance likely depends on a combination of traits—including thermal limits—that vary among species. Here, we examine how thermal limits correlate with the main components that influence fitness in ants. First, we compare how temperature affected colony survival and growth in two ant species that differ in their responses to warming in the field— Aphaenogaster rudis (heat‐intolerant) and Temnothorax curvispinosus (heat‐tolerant). We then extended our study to compare CT max , thermal requirements of brood and yearly activity season among a broader set of ant species. While thermal limits were higher for workers of T. curvispinosus than A. rudis , T. curvispinosus colonies also required higher temperatures for survival and colony growth. This pattern generalized across 17 ant species, such that species whose foragers had a high CT max also required higher temperatures for brood development. Finally, species whose foragers had a high CT max had relatively short activity seasons compared with less heat‐tolerant species. The relationships betweenmore »
- Authors:
-
- Department of Applied Ecology and Keck Center for Behavioral Biology North Carolina State University Raleigh NC 27695 USA, North Carolina Museum of Natural Sciences Raleigh NC 27601 USA
- Department of Biology Case Western Reserve University Cleveland OH 44106 USA
- Center for Macroecology, Evolution and Climate Natural History Museum of Denmark University of Copenhagen DK‐2100 Copenhagen Denmark, Rubenstein School of Environment and Natural Resources University of Vermont Burlington VT 05405 USA
- Department of Applied Ecology and Keck Center for Behavioral Biology North Carolina State University Raleigh NC 27695 USA, Center for Macroecology, Evolution and Climate Natural History Museum of Denmark University of Copenhagen DK‐2100 Copenhagen Denmark
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1401497
- Grant/Contract Number:
- DEFG02‐08ER64510
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Functional Ecology
- Additional Journal Information:
- Journal Name: Functional Ecology Journal Volume: 31 Journal Issue: 5; Journal ID: ISSN 0269-8463
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Penick, Clint A., Diamond, Sarah E., Sanders, Nathan J., Dunn, Robert R., and Rezende, ed., Enrico. Beyond thermal limits: comprehensive metrics of performance identify key axes of thermal adaptation in ants. United Kingdom: N. p., 2017.
Web. doi:10.1111/1365-2435.12818.
Penick, Clint A., Diamond, Sarah E., Sanders, Nathan J., Dunn, Robert R., & Rezende, ed., Enrico. Beyond thermal limits: comprehensive metrics of performance identify key axes of thermal adaptation in ants. United Kingdom. https://doi.org/10.1111/1365-2435.12818
Penick, Clint A., Diamond, Sarah E., Sanders, Nathan J., Dunn, Robert R., and Rezende, ed., Enrico. Tue .
"Beyond thermal limits: comprehensive metrics of performance identify key axes of thermal adaptation in ants". United Kingdom. https://doi.org/10.1111/1365-2435.12818.
@article{osti_1401497,
title = {Beyond thermal limits: comprehensive metrics of performance identify key axes of thermal adaptation in ants},
author = {Penick, Clint A. and Diamond, Sarah E. and Sanders, Nathan J. and Dunn, Robert R. and Rezende, ed., Enrico},
abstractNote = {Summary How species respond to temperature change depends in large part on their physiology. Physiological traits, such as critical thermal limits ( CT max and CT min ), provide estimates of thermal performance but may not capture the full impacts of temperature on fitness. Rather, thermal performance likely depends on a combination of traits—including thermal limits—that vary among species. Here, we examine how thermal limits correlate with the main components that influence fitness in ants. First, we compare how temperature affected colony survival and growth in two ant species that differ in their responses to warming in the field— Aphaenogaster rudis (heat‐intolerant) and Temnothorax curvispinosus (heat‐tolerant). We then extended our study to compare CT max , thermal requirements of brood and yearly activity season among a broader set of ant species. While thermal limits were higher for workers of T. curvispinosus than A. rudis , T. curvispinosus colonies also required higher temperatures for survival and colony growth. This pattern generalized across 17 ant species, such that species whose foragers had a high CT max also required higher temperatures for brood development. Finally, species whose foragers had a high CT max had relatively short activity seasons compared with less heat‐tolerant species. The relationships between CT max , thermal requirements of brood and seasonal activity suggest two main strategies for growth and development in changing thermal environments: one where ants forage at higher temperatures over a short activity season and another where ants forage at lower temperatures for an extended activity season. Where species fall on this spectrum may influence a broad range of life‐history characteristics and aid in explaining the current distributions of ants as well as their responses to future climate change. A lay summary is available for this article.},
doi = {10.1111/1365-2435.12818},
journal = {Functional Ecology},
number = 5,
volume = 31,
place = {United Kingdom},
year = {Tue Jan 17 00:00:00 EST 2017},
month = {Tue Jan 17 00:00:00 EST 2017}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1365-2435.12818
https://doi.org/10.1111/1365-2435.12818
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 52 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Upward ant distribution shift corresponds with minimum, not maximum, temperature tolerance
journal, March 2013
- Warren, Robert J.; Chick, Lacy
- Global Change Biology, Vol. 19, Issue 7
Abrupt Climate Change and Extinction Events in Earth History
journal, May 1988
- Crowley, T. J.; North, G. R.
- Science, Vol. 240, Issue 4855
Modeling Insect Development Rates: a Literature Review and Application of a Biophysical Model
journal, March 1984
- Wagner, Terence L.; Wu, Hsin-I; Sharpe, Peter J. H.
- Annals of the Entomological Society of America, Vol. 77, Issue 2
Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming
journal, June 2015
- Gunderson, Alex R.; Stillman, Jonathon H.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1808
Invasive ants alter the phylogenetic structure of ant communities
journal, October 2009
- Lessard, Jean-Philippe; Fordyce, James A.; Gotelli, Nicholas J.
- Ecology, Vol. 90, Issue 10
Impact of worker longevity and other endogenous factors on colony size in the fire ant, Solenopsis invicta
journal, June 2011
- Asano, E.; Cassill, D. L.
- Insectes Sociaux, Vol. 58, Issue 4
Critical thermal limits in Mediterranean ant species: trade-off between mortality risk and foraging performance
journal, February 1998
- Cerda, X.; Retana, J.; Cros, S.
- Functional Ecology, Vol. 12, Issue 1
Acclimation effects on critical and lethal thermal limits of workers of the Argentine ant, Linepithema humile
journal, June 2008
- Jumbam, Keafon R.; Jackson, Susan; Terblanche, John S.
- Journal of Insect Physiology, Vol. 54, Issue 6
Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field
journal, August 2012
- Chevin, Luis-Miguel; Collins, Sinéad; Lefèvre, François
- Functional Ecology, Vol. 27, Issue 4
Comparative study of thermal reaction norms for development in ants: Thermal reaction norms in ants
journal, July 2014
- Kipyatkov, Vladilen E.; Lopatina, Elena B.
- Entomological Science, Vol. 18, Issue 2
At the edge of the thermal window: effects of elevated temperature on the resting metabolism, hypoxia tolerance and upper critical thermal limit of a widespread African cichlid
journal, January 2015
- McDonnell, Laura H.; Chapman, Lauren J.
- Conservation Physiology, Vol. 3, Issue 1
Common garden experiments reveal uncommon responses across temperatures, locations, and species of ants
journal, November 2012
- Pelini, Shannon L.; Diamond, Sarah E.; MacLean, Heidi
- Ecology and Evolution, Vol. 2, Issue 12
Effect of Temperature on Rearing of the First Brood by the Founder Females of the Ant Lasius niger (Hymenoptera, Formicidae) : Latitude-Dependent Variability of the Response Norm
journal, March 2004
- Kipyatkov, V. E.; Lopatina, E. B.; Imamgaliev, A. A.
- Journal of Evolutionary Biochemistry and Physiology, Vol. 40, Issue 2
Life Inside an Acorn: How Microclimate and Microbes Influence Nest Organization in Temnothorax Ants
journal, August 2016
- Karlik, Joseph; Epps, Mary Jane; Dunn, Robert R.
- Ethology, Vol. 122, Issue 10
Thermal tolerance and the global redistribution of animals
journal, May 2012
- Sunday, Jennifer M.; Bates, Amanda E.; Dulvy, Nicholas K.
- Nature Climate Change, Vol. 2, Issue 9
Worker longevity in the fire ant Solenopsis invicta: Ergonomic considerations of correlations between temperature, size and metabolic rates
journal, January 1989
- Calabi, Prassede; Porter, Sanford D.
- Journal of Insect Physiology, Vol. 35, Issue 8
Effect of temperature on the oviposition rate of Argentine ant queens (Linepithema humile Mayr) under monogynous and polygynous experimental conditions
journal, January 2008
- Abril, Sílvia; Oliveras, Jordi; Gómez, Crisanto
- Journal of Insect Physiology, Vol. 54, Issue 1
Complex Life Cycles and the Responses of Insects to Climate Change
journal, June 2011
- Kingsolver, Joel G.; Arthur Woods, H.; Buckley, Lauren B.
- Integrative and Comparative Biology, Vol. 51, Issue 5
Thermal adaptation generates a diversity of thermal limits in a rainforest ant community
journal, November 2014
- Kaspari, Michael; Clay, Natalie A.; Lucas, Jane
- Global Change Biology, Vol. 21, Issue 3
Effect of Temperature on the Development and Survival of the Argentine Ant, Linepithema humile
journal, July 2010
- Abril, Silvia; Oliveras, Jordi; Gómez, Crisanto
- Journal of Insect Science, Vol. 10, Issue 97
Heating up the forest: open-top chamber warming manipulation of arthropod communities at Harvard and Duke Forests: Forest arthropod warming experiment
journal, March 2011
- Pelini, Shannon L.; Bowles, Francis P.; Ellison, Aaron M.
- Methods in Ecology and Evolution, Vol. 2, Issue 5
Thermal Performance Curves, Phenotypic Plasticity, and the Time Scales of Temperature Exposure
journal, August 2011
- Schulte, P. M.; Healy, T. M.; Fangue, N. A.
- Integrative and Comparative Biology, Vol. 51, Issue 5
The effects of temperature and food on the growth of laboratory colonies ofAphaenogaster rudis Emery (Hymenoptera: Formicidae)
journal, September 1988
- Southerland, M. T.
- Insectes Sociaux, Vol. 35, Issue 3
Impacts of climate warming on terrestrial ectotherms across latitude
journal, May 2008
- Deutsch, C. A.; Tewksbury, J. J.; Huey, R. B.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 18
Living in the Now: Physiological Mechanisms to Tolerate a Rapidly Changing Environment
journal, March 2010
- Hofmann, Gretchen E.; Todgham, Anne E.
- Annual Review of Physiology, Vol. 72, Issue 1
Inferring the historical patterns of biological evolution
journal, October 1999
- Pagel, Mark
- Nature, Vol. 401, Issue 6756
Very high resolution interpolated climate surfaces for global land areas
journal, January 2005
- Hijmans, Robert J.; Cameron, Susan E.; Parra, Juan L.
- International Journal of Climatology, Vol. 25, Issue 15
Who likes it hot? A global analysis of the climatic, ecological, and evolutionary determinants of warming tolerance in ants
journal, October 2011
- Diamond, Sarah E.; Sorger, D. Magdalena; Hulcr, Jiri
- Global Change Biology, Vol. 18, Issue 2
The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine 'winners' and 'losers'
journal, February 2010
- Somero, G. N.
- Journal of Experimental Biology, Vol. 213, Issue 6
Variation in thermal tolerance of North American ants
journal, February 2015
- Verble-Pearson, Robin M.; Gifford, Matthew E.; Yanoviak, Stephen P.
- Journal of Thermal Biology, Vol. 48
The Well‐Temperatured Biologist: (American Society of Naturalists Presidential Address)
journal, December 2009
- Kingsolver, Joel G.
- The American Naturalist, Vol. 174, Issue 6
Climatic warming destabilizes forest ant communities
journal, October 2016
- Diamond, Sarah E.; Nichols, Lauren M.; Pelini, Shannon L.
- Science Advances, Vol. 2, Issue 10
Thermoregulatory brood transport in the fire ant, Solenopsis invicta
journal, February 2008
- Penick, C. A.; Tschinkel, W. R.
- Insectes Sociaux, Vol. 55, Issue 2
Testing the Museum Versus Cradle Tropical Biological Diversity Hypothesis: Phylogeny, Diversification, and Ancestral Biogeographic Range Evolution of the Ants: the Tropics as Museum and Cradle of ant Diversity
journal, April 2013
- Moreau, Corrie S.; Bell, Charles D.
- Evolution, Vol. 67, Issue 8
Modulation of the heat shock response is associated with acclimation to novel temperatures but not adaptation to climatic variation in the ants Aphaenogaster picea and A. rudis
journal, February 2017
- Helms Cahan, Sara; Nguyen, Andrew D.; Stanton-Geddes, John
- Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, Vol. 204
Integrating Thermal Physiology and Ecology of Ectotherms: A Discussion of Approaches
journal, February 1979
- Huey, Raymond B.; Stevenson, R. D.
- American Zoologist, Vol. 19, Issue 1
Using Physiology to Predict the Responses of Ants to Climatic Warming
journal, July 2013
- Diamond, S. E.; Penick, C. A.; Pelini, S. L.
- Integrative and Comparative Biology, Vol. 53, Issue 6
Impact of temperature on colony growth and developmental rates of the ant, Solenopsis invicta
journal, January 1988
- Porter, Sanford D.
- Journal of Insect Physiology, Vol. 34, Issue 12
Evolutionary Responses to Changing Climate
journal, July 2005
- Davis, Margaret B.; Shaw, Ruth G.; Etterson, Julie R.
- Ecology, Vol. 86, Issue 7
Artificial Diet for Rearing Various Species of Ants
journal, December 1970
- Bhatkar, A.; Whitcomb, W. H.
- The Florida Entomologist, Vol. 53, Issue 4
Social Insects Dominate Eastern US Temperate Hardwood Forest Macroinvertebrate Communities in Warmer Regions
journal, October 2013
- King, Joshua R.; Warren, Robert J.; Bradford, Mark A.
- PLoS ONE, Vol. 8, Issue 10
Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica
journal, June 1999
- Petit, J. R.; Jouzel, J.; Raynaud, D.
- Nature, Vol. 399, Issue 6735
A physiological trait-based approach to predicting the responses of species to experimental climate warming
journal, November 2012
- Diamond, Sarah E.; Nichols, Lauren M.; McCoy, Neil
- Ecology, Vol. 93, Issue 11
Macrophysiology: large-scale patterns in physiological traits and their ecological implications
journal, April 2004
- Chown, S. L.; Gaston, K. J.; Robinson, D.
- Functional Ecology, Vol. 18, Issue 2
Thermal tolerance, acclimatory capacity and vulnerability to global climate change
journal, November 2007
- Calosi, Piero; Bilton, David T.; Spicer, John I.
- Biology Letters, Vol. 4, Issue 1
Tolerance landscapes in thermal ecology
journal, March 2014
- Rezende, Enrico L.; Castañeda, Luis E.; Santos, Mauro
- Functional Ecology, Vol. 28, Issue 4
Tradeoffs, competition, and coexistence in eastern deciduous forest ant communities
journal, December 2012
- Stuble, Katharine L.; Rodriguez-Cabal, Mariano A.; McCormick, Gail L.
- Oecologia, Vol. 171, Issue 4
The critical thermal maximum: data to support the onset of spasms as the definitive end point
journal, October 1997
- Lutterschmidt, William I.; Hutchison, Victor H.
- Canadian Journal of Zoology, Vol. 75, Issue 10
Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming
journal, August 2014
- Magozzi, Sarah; Calosi, Piero
- Global Change Biology, Vol. 21, Issue 1
Thermal Disruption of Transitive Hierarchies in Mediterranean Ant Communities
journal, May 1997
- Cerda, Xim; Retana, Javier; Cros, Sebastia
- The Journal of Animal Ecology, Vol. 66, Issue 3
Morphometric discrimination among sibling species in the fulva – rudis – texana complex of the ant genus Aphaenogaster (Hymenoptera: Formicidae)
journal, March 1996
- Umphrey, Gary J.
- Canadian Journal of Zoology, Vol. 74, Issue 3
Predicting future coexistence in a North American ant community
journal, April 2014
- Bewick, Sharon; Stuble, Katharine L.; Lessard, Jean-Phillipe
- Ecology and Evolution, Vol. 4, Issue 10
Cost to the cavity-nest ant Temnothorax crassispinus (Hymenoptera: Formicidae) of overwintering aboveground
journal, January 2013
- Mitrus, Slawomir
- European Journal of Entomology, Vol. 110, Issue 1
Ant biodiversity and its relationship to ecosystem functioning: a review
journal, September 1998
- Folgarait, Patricia J.
- Biodiversity and Conservation, Vol. 7, Issue 9
Reorganization of taxonomic, functional, and phylogenetic ant biodiversity after conversion to rubber plantation
journal, May 2016
- Liu, Cong; Guénard, Benoit; Blanchard, Benjamin
- Ecological Monographs, Vol. 86, Issue 2
Foraging by forest ants under experimental climatic warming: a test at two sites
journal, January 2013
- Stuble, Katharine L.; Pelini, Shannon L.; Diamond, Sarah E.
- Ecology and Evolution, Vol. 3, Issue 3
Global diversity in light of climate change: the case of ants: Global diversity of ants in light of climate change
journal, May 2011
- Jenkins, Clinton N.; Sanders, Nathan J.; Andersen, Alan N.
- Diversity and Distributions, Vol. 17, Issue 4
Observations on the Microfauna of the Duke Forest
journal, February 1946
- Pearse, A. S.
- Ecological Monographs, Vol. 16, Issue 2
Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits are more Labile
journal, April 2003
- Blomberg, Simon P.; Garland, Theodore; Ives, Anthony R.
- Evolution, Vol. 57, Issue 4
Functional and Phylogenetic Approaches to Forecasting Species' Responses to Climate Change
journal, December 2012
- Buckley, Lauren B.; Kingsolver, Joel G.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 43, Issue 1
Species interactions and thermal constraints on ant community structure
journal, March 2010
- Wittman, Sarah E.; Sanders, Nathan J.; Ellison, Aaron M.
- Oikos, Vol. 119, Issue 3
Modeling temperature-mediated fluctuation in colony size in the fire ant, Solenopsis invicta
journal, July 2012
- Asano, Erika; Cassill, Deby L.
- Journal of Theoretical Biology, Vol. 305