The roles of acclimation and behaviour in buffering climate change impacts along elevational gradients.
Bogert effect
NicheMapR
acclimation
activity restrictions
behavioural thermoregulation
global warming
mechanistic niche modelling
thermal-safety margins
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
17
12
2019
accepted:
29
02
2020
pubmed:
30
3
2020
medline:
27
2
2021
entrez:
30
3
2020
Statut:
ppublish
Résumé
The vulnerability of species to climate change is jointly influenced by geographic phenotypic variation, acclimation and behavioural thermoregulation. The importance of interactions between these factors, however, remains poorly understood. We demonstrate how advances in mechanistic niche modelling can be used to integrate and assess the influence of these sources of uncertainty in forecasts of climate change impacts. We explored geographic variation in thermal tolerance (i.e. maximum and minimum thermal limits) and its potential for acclimation in juvenile European common frogs Rana temporaria along elevational gradients. Furthermore, we employed a mechanistic niche model (NicheMapR) to assess the relative contributions of phenotypic variation, acclimation and thermoregulation in determining the impacts of climate change on thermal safety margins and activity windows. Our analyses revealed that high-elevation populations had slightly wider tolerance ranges driven by increases in heat tolerance but lower potential for acclimation. Plausibly, wider thermal fluctuations at high elevations favour more tolerant but less plastic phenotypes, thus reducing the risk of encountering stressful temperatures during unpredictable extreme events. Biophysical models of thermal exposure indicated that observed phenotypic and plastic differences provide limited protection from changing climates. Indeed, the risk of reaching body temperatures beyond the species' thermal tolerance range was similar across elevations. In contrast, the ability to seek cooler retreat sites through behavioural adjustments played an essential role in buffering populations from thermal extremes predicted under climate change. Predicted climate change also altered current activity windows, but high-elevation populations were predicted to remain more temporally constrained than lowland populations. Our results demonstrate that elevational variation in thermal tolerances and acclimation capacity might be insufficient to buffer temperate amphibians from predicted climate change; instead, behavioural thermoregulation may be the only effective mechanism to avoid thermal stress under future climates.
Identifiants
pubmed: 32221971
doi: 10.1111/1365-2656.13222
doi:
Banques de données
Dryad
['10.5061/dryad.dz08kprtv']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1722-1734Informations de copyright
© 2020 British Ecological Society.
Références
Addo-Bediako, A., Chown, S. L., & Gaston, K. J. (2000). Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society B: Biological Sciences, 267, 739-745. https://doi.org/10.1098/rspb.2000.1065
Ahmadi, M., Hemami, M. R., Kaboli, M., Malekian, M., & Zimmermann, N. E. (2019). Extinction risks of a Mediterranean neo-endemism complex of mountain vipers triggered by climate change. Scientific Reports, 9, 6332. https://doi.org/10.1038/s41598-019-42792-9
Araújo, M. B., Ferri-Yáñez, F., Bozinovic, F., Marquet, P. A., Valladares, F., & Chown, S. L. (2013). Heat freezes niche evolution. Ecology Letters, 16, 1206-1219. https://doi.org/10.1111/ele.12155
Araújo, M. B., Thuiller, W., & Pearson, R. G. (2006). Climate warming and the decline of amphibians and reptiles in Europe. Journal of Biogeography, 33, 1712-1728. https://doi.org/10.1111/j.1365-2699.2006.01482.x
Baudier, K. M., & O'Donnell, S. (2020). Rain shadow effects predict population differences in thermal tolerance of leaf-cutting ant workers (Atta cephalotes). Biotropica, 52, 113-119. https://doi.org/10.1111/btp.12733
Benito Garzón, M., Alía, R., Robson, T. M., & Zavala, M. A. (2011). Intra-specific variability and plasticity influence potential tree species distributions under climate change. Global Ecology and Biogeography, 20, 766-778. https://doi.org/10.1111/j.1466-8238.2010.00646.x
Bogert, C. M. (1949). Thermoregulation in reptiles, a factor in evolution. Evolution, 3, 195-211. https://doi.org/10.1111/j.1558-5646.1949.tb00021.x
Brattstrom, B. H. (1968). Thermal acclimation in anuran amphibians as a function of latitude and altitude. Comparative Biochemistry and Physiology, 24, 93-111. https://doi.org/10.1016/0010-406X(68)90961-4
Brinckmann, S., Krähenmann, S., & Bissolli, P. (2016). High-resolution daily gridded data sets of air temperature and wind speed for Europe. Earth System Science Data, 8, 491-516. https://doi.org/10.5194/essd-8-491-2016
Buckley, L. B., Ehrenberger, J. C., & Angilletta Jr., M. J. (2015). Thermoregulatory behaviour limits local adaptation of thermal niches and confers sensitivity to climate change. Functional Ecology, 29, 1038-1047. https://doi.org/10.1111/1365-2435.12406
Buckley, L. B., & Kingsolver, J. G. (2012). Functional and phylogenetic approaches to forecasting species' responses to climate change. Annual Review of Ecology, Evolution, and Systematics, 43, 205-226. https://doi.org/10.1146/annurev-ecolsys-110411-160516
Calosi, P., Bilton, D. T., & Spicer, J. I. (2008). Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biology Letters, 4, 99-102. https://doi.org/10.1098/rsbl.2007.0408
Chevin, L.-M., Lande, R., & Mace, G. M. (2010). Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biology, 8, e1000357. https://doi.org/10.1371/journal.pbio.1000357
Choda, M. (2014). Genetic variation and local adaptation of Rana temporaria in the Cantabrian mountains (PhD thesis). Universidad de Oviedo, Oviedo.
Conover, D. O., & Schultz, E. T. (1995). Phenotypic similarity and the evolutionary significance of countergradient variation. Trends in Ecology & Evolution, 10, 248-252. https://doi.org/10.1016/S0169-5347(00)89081-3
Cuddington, K., Fortin, M.-J., Gerber, L. R., Hastings, A., Liebhold, A., O'Connor, M., & Ray, C. (2013). Process-based models are required to manage ecological systems in a changing world. Ecosphere, 4, 1-12. https://doi.org/10.1890/ES12-00178.1
Cupp Jr., P. V. (1980). Thermal tolerance of five salientian amphibians during development and metamorphosis. Herpetologica, 36, 234-244.
Dahl, E., Orizaola, G., Nicieza, A. G., & Laurila, A. (2012). Time constraints and flexibility of growth strategies: Geographic variation in catch-up growth responses in amphibian larvae. Journal of Animal Ecology, 81, 1233-1243. https://doi.org/10.1111/j.1365-2656.2012.02009.x
Deutsch, C. A., Tewksbury, J. J., Huey, R. B., Sheldon, K. S., Ghalambor, C. K., Haak, D. C., & Martin, P. R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America, 105, 6668-6672. https://doi.org/10.1073/pnas.0709472105
Dewitt, T. J., Sih, A., & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13, 77-81. https://doi.org/10.1016/S0169-5347(97)01274-3
Duarte, H., Tejedo, M., Katzenberger, M., Marangoni, F., Baldo, D., Beltrán, J. F., … Gonzalez-Voyer, A. (2012). Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Global Change Biology, 18, 412-421. https://doi.org/10.1111/j.1365-2486.2011.02518.x
Dufresnes, C., Nicieza, A. G., Litvinchuk, S. N., Rodrigues, N., Jeffries, D. L., Vences, M., … Martínez-Solano, Í. (2020). Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs. Molecular Ecology, 29(5), 986-1000. https://doi.org/10.1111/mec.15368
Enriquez-Urzelai, U., Palacio, A. S., Merino, N. M., Sacco, M., & Nicieza, A. G. (2018). Hindered and constrained: Limited potential for thermal adaptation in post-metamorphic and adult Rana temporaria along elevational gradients. Journal of Evolutionary Biology, 31, 1852-1862. https://doi.org/10.1111/jeb.13380
Enriquez-Urzelai, U., Sacco, M., Palacio, A. S., Pintanel, P., Tejedo, M., & Nicieza, A. G. (2019). Ontogenetic reduction in thermal tolerance is not alleviated by earlier developmental acclimation in Rana temporaria. Oecologia, 189, 385-394. https://doi.org/10.1007/s00442-019-04342-y
Enriquez-Urzelai, U., Tingley, R., Kearney, M. R., Sacco, M., Palacio, A. S., Tejedo, M., & Nicieza, A. G. (2020). Data from: The roles of acclimation and behaviour in buffering climate change impacts along elevational gradients. Dryad Digital Repository, https://doi.org/10.5061/dryad.dz08kprtv
Farallo, V. R., Wier, R., & Miles, D. B. (2018). The Bogert effect revisited: Salamander regulatory behaviors are differently constrained by time and space. Ecology and Evolution, 8, 11522-11532. https://doi.org/10.1002/ece3.4590
Fitzpatrick, M. J., Zuckerberg, B., Pauli, J. N., Kearney, M. R., Thompson, K. L., Werner II, L. C., & Porter, W. P. (2019). Modeling the distribution of niche space and risk for a freeze-tolerant ectotherm, Lithobates sylvaticus. Ecosphere, 10, e02788. https://doi.org/10.1002/ecs2.2788
Freidenburg, L. K., & Skelly, D. K. (2004). Microgeographical variation in thermal preference by an amphibian. Ecology Letters, 7, 369-373. https://doi.org/10.1111/j.1461-0248.2004.00587.x
García-París, M., Montori, A., & Herrero, P. (2004). Amphibia: Lissamphibia. In M. A. Ramos (Ed.), Fauna Ibérica (p. 640). Madrid: Museo Nacional de Ciencias Naturales. CSIC.
García-Robledo, C., Kuprewicz, E. K., Staines, C. L., Erwin, T. L., & Kress, W. J. (2016). Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proceedings of the National Academy of Sciences of the United States of America, 113, 680-685. https://doi.org/10.1073/pnas.1507681113
Gaston, K. J., & Chown, S. L. (1999). Elevation and climatic tolerance: A test using dung beetles. Oikos, 86, 584-590. https://doi.org/10.2307/354666310.2307/3546663
Gerick, A. A., Munshaw, R. G., Palen, W. J., Combes, S. A., & O'Regan, S. M. (2014). Thermal physiology and species distribution models reveal climate vulnerability of temperate amphibians. Journal of Biogeography, 41, 713-723. https://doi.org/10.1111/jbi.12261
Gunderson, A. R., Dillon, M. E., & Stillman, J. H. (2017). Estimating the benefits of plasticity in ectotherm heat tolerance under natural thermal variability. Functional Ecology, 31, 1529-1539. https://doi.org/10.1111/1365-2435.12874
Gunderson, A. R., & Leal, M. (2015). Patterns of thermal constraint on ectotherm activity. The American Naturalist, 185, 653-664. https://doi.org/10.1086/680849
Gunderson, A. R., & Stillman, J. H. (2015). Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proceedings of the Royal Society B: Biological Sciences, 282, 2015.0401. https://doi.org/10.1098/rspb.2015.0401
Gutiérrez-Pesquera, L. M., Tejedo, M., Olalla-Tárraga, M. Á., Duarte, H., Nicieza, A., & Solé, M. (2016). Testing the climate variability hypothesis in thermal tolerance limits of tropical and temperate tadpoles. Journal of Biogeography, 43, 1166-1178. https://doi.org/10.1111/jbi.12700
Gvoždík, L., Castilla, A. M., & Gvozdik, L. (2001). A comparative study of preferred body temperatures and critical thermal tolerance limits among populations of Zootoca vivipara (Squamata: Lacertidae) along an altitudinal gradient. Journal of Herpetology, 35, 486-492. https://doi.org/10.2307/1565967
Haylock, M. R., Hofstra, N., Klein Tank, A. M. G., Klok, E. J., Jones, P. D., & New, M. (2008). A European daily high-resolution gridded data set of surface temperature and precipitation for 1950-2006. Journal of Geophysical Research, 113, D20119. https://doi.org/10.1029/2008JD010201
Heath, J. E. (1964). Reptilian thermoregulation: Evaluation of field studies. Science, 146, 784-785. https://doi.org/10.1126/science.146.3645.784
Hereford, J. (2009). A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist, 173, 579-588. https://doi.org/10.1086/597611
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978. https://doi.org/10.1002/joc.1276
Huey, R. B., Hertz, P. E., & Sinervo, B. (2003). Behavioral drive versus behavioral inertia in evolution: A null model approach. The American Naturalist, 161, 357-366. https://doi.org/10.1086/346135
Huey, R. B., Kearney, M. R., Krockenberger, A., Holtum, J. A. M., Jess, M., & Williams, S. E. (2012). Predicting organismal vulnerability to climate warming: Roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 1665-1679. https://doi.org/10.1098/rstb.2012.0005
Huey, R. B., & Kingsolver, J. G. (1993). Evolution of resistance to high temperature in ectotherms. The American Naturalist, 142, S21-S46. https://doi.org/10.1086/285521
Jankowski, J. E., Londoño, G. A., Robinson, S. K., & Chappell, M. A. (2013). Exploring the role of physiology and biotic interactions in determining elevational ranges of tropical animals. Ecography, 36, 1-12. https://doi.org/10.1111/j.1600-0587.2012.07785.x
Jensen, A., Alemu, T., Alemneh, T., Pertoldi, C., & Bahrndorff, S. (2019). Thermal acclimation and adaptation across populations in a broadly distributed soil arthropod. Functional Ecology, 33, 833-845. https://doi.org/10.1111/1365-2435.13291
Kearney, M. R., Matzelle, A., & Helmuth, B. (2012). Biomechanics meets the ecological niche: The importance of temporal data resolution. The Journal of Experimental Biology, 215, 922-933. https://doi.org/10.1242/jeb.059634
Kearney, M. R., Munns, S. L., Moore, D., Malishev, M., & Bull, C. M. (2018). Field tests of a general ectotherm niche model show how water can limit lizard activity and distribution. Ecological Monographs, 142, 273-322. https://doi.org/10.1002/ecm.1326
Kearney, M. R., Phillips, B. L., Tracy, C. R., Christian, K. A., Betts, G., & Porter, W. P. (2008). Modelling species distributions without using species distributions: The cane toad in Australia under current and future climates. Ecography, 31, 423-434. https://doi.org/10.1111/j.0906-7590.2008.05457.x
Kearney, M. R., & Porter, W. P. (2009). Mechanistic niche modelling: Combining physiological and spatial data to predict species' ranges. Ecology Letters, 12, 334-350. https://doi.org/10.1111/j.1461-0248.2008.01277.x
Kearney, M. R., & Porter, W. P. (2017). NicheMapR - An R package for biophysical modelling: The microclimate model. Ecography, 40, 664-674. https://doi.org/10.1111/ecog.02360
Kearney, M. R., & Porter, W. P. (2020). NicheMapR - An R package for biophysical modelling: The ectotherm and Dynamic Energy Budget models. Ecography, 43, 85-96. https://doi.org/10.1111/ecog.04680
Kearney, M. R., Shine, R., & Porter, W. P. (2009). The potential for behavioral thermoregulation to buffer ‘cold-blooded’ animals against climate warming. Proceedings of the National Academy of Sciences of the United States of America, 106, 3835-3840. https://doi.org/10.1073/pnas.0808913106
Kolbe, J. J., Kearney, M. R., & Shine, R. (2010). Modeling the consequences of thermal trait variation for the cane toad invasion of Australia. Ecological Applications, 20, 2273-2285. https://doi.org/10.1890/09-1973.1
Lambrinos, J. G., & Kleier, C. C. (2003). Thermoregulation of juvenile Andean toads (Bufo spinulosus) at 4300 m. Journal of Thermal Biology, 28, 15-19. https://doi.org/10.1016/S0306-4565(02)00030-X
Lamoureux, V., & Madison, D. M. (1999). Overwintering habitats of radio-implanted Green frogs, Rana clamitans. Journal of Herpetology, 33, 430-435. https://doi.org/10.2307/1565639
Levy, O., Buckley, L. B., Keitt, T. H., & Angilletta, M. J. (2016). Ontogeny constrains phenology: Opportunities for activity and reproduction interact to dictate potential phenologies in a changing climate. Ecology Letters, 19, 620-628. https://doi.org/10.1111/ele.12595
Linhart, Y. B., & Grant, M. C. (1996). Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics, 27, 237-277. https://doi.org/10.1146/annurev.ecolsys.27.1.237
Ludwig, G., Sinsch, U., & Pelster, B. (2013). Migratory behaviour during autumn and hibernation site selection in common frogs (Rana temporaria) at high altitude. Herpetological Journal, 23, 121-124. https://doi.org/10.1111/j.1469-7998.1984.tb06046.x
Ludwig, G., Sinsch, U., & Pelster, B. (2015). Behavioural adaptations of Rana temporaria to cold climates. Journal of Thermal Biology, 49-50, 82-90. https://doi.org/10.1016/j.jtherbio.2015.02.006
Lutterschmidt, W. I., & Hutchison, V. H. (1997). The critical thermal maximum: History and critique. Canadian Journal of Zoology, 75, 1561-1574. https://doi.org/10.1139/z97-783
Matesanz, S., Gianoli, E., & Valladares, F. (2010). Global change and the evolution of phenotypic plasticity in plants. Annals of the New York Academy of Sciences, 1206, 35-55. https://doi.org/10.1111/j.1749-6632.2010.05704.x
McCain, C. M., & Colwell, R. K. (2011). Assessing the threat to montane biodiversity from discordant shifts in temperature and precipitation in a changing climate. Ecology Letters, 14, 1236-1245. https://doi.org/10.1111/j.1461-0248.2011.01695.x
Miller, K., & Packard, G. C. (1977). An altitudinal cline in critical thermal maxima of Chorus frogs (Pseudacris triseriata). The American Naturalist, 111, 267-277. https://doi.org/10.1086/283159
Moran, E. V., Hartig, F., & Bell, D. M. (2016). Intraspecific trait variation across scales: Implications for understanding global change responses. Global Change Biology, 22, 137-150. https://doi.org/10.1111/gcb.13000
Muir, A. P., Biek, R., & Mable, B. K. (2014). Behavioural and physiological adaptations to low-temperature environments in the common frog, Rana temporaria. BMC Evolutionary Biology, 14, 110. https://doi.org/10.1186/1471-2148-14-110
Muñoz, M. M., & Losos, J. B. (2018). Thermoregulatory behavior simultaneously promotes and forestalls evolution in a tropical lizard. The American Naturalist, 191, E15-E26. https://doi.org/10.1086/694779
Navas, C. A., Antoniazzi, M. M., Carvalho, J. E., Suzuki, H., & Jared, C. (2007). Physiological basis for diurnal activity in dispersing juvenile Bufo granulosus in the Caatinga, a Brazilian semi-arid environment. Comparative Biochemistry and Physiology Part A, 147, 647-657. https://doi.org/10.1016/j.cbpa.2006.04.035
Navas, C. A., Úbeda, C. A., Logares, R., & Jara, F. G. (2010). Thermal tolerances in tadpoles of three species of Patagonian anurans. South American Journal of Herpetology, 5, 89-96. https://doi.org/10.2994/057.005.0203
Nicieza, A. G., & Metcalfe, N. B. (1997). Growth compensation in juvenile Atlantic salmon: Responses to depressed temperature and food availability. Ecology, 78, 2385-2400. https://doi.org/10.1890/0012-9658(1997)078[2385:GCIJAS]2.0.CO;2
Orizaola, G., & Laurila, A. (2016). Developmental plasticity increases at the northern range margin in a warm-dependent amphibian. Evolutionary Applications, 9, 471-478. https://doi.org/10.1111/eva.12349
Overgaard, J., Kearney, M. R., & Hoffmann, A. A. (2014). Sensitivity to thermal extremes in Australian Drosophila implies similar impacts of climate change on the distribution of widespread and tropical species. Global Change Biology, 20, 1738-1750. https://doi.org/10.1111/gcb.12521
Overgaard, J., Kristensen, T. N., Mitchell, K. A., & Hoffmann, A. A. (2011). Thermal tolerance in widespread and tropical Drosophila species: Does phenotypic plasticity increase with latitude? The American Naturalist, 178, S80-S96. https://doi.org/10.1086/661780
Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics, 37, 637-669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Pearson, G. A., Lago-Leston, A., & Mota, C. (2009). Frayed at the edges: Selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populations. Journal of Ecology, 97, 450-462. https://doi.org/10.1111/j.1365-2745.2009.01481.x
Pintanel, P., Tejedo, M., Ron, S. R., Llorente, G. A., & Merino-Viteri, A. (2019). Elevational and microclimatic drivers of thermal tolerance in Andean Pristimantid frogs. Journal of Biogeography, 46, 1664-1675.
Porter, W. P., Mitchell, J. W., Beckman, W. A., & DeWitt, C. B. (1973). Behavioral implications of mechanistic ecology - Thermal and behavioral modeling of desert ectotherms and their microenvironment. Oecologia, 13, 1-54. https://doi.org/10.1007/BF00379617
Qi, Y., Felix, Z., Wang, Y., Gu, H., & Wang, Y. (2011). Postbreeding movement and habitat use of the Plateau brown frog, Rana kukunoris, in a high-elevation wetland. Journal of Herpetology, 45, 421-427. https://doi.org/10.1670/10-171.1
Quintero, I., & Wiens, J. J. (2013). Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species. Ecology Letters, 16, 1095-1103. https://doi.org/10.1111/ele.12144
Recuero, E., & García-París, M. (2011). Evolutionary history of Lissotriton helveticus: Multilocus assessment of ancestral vs. recent colonization of the Iberian Peninsula. Molecular Phylogenetics and Evolution, 60, 170-182. https://doi.org/10.1016/j.ympev.2011.04.006
Richter-Boix, A., Katzenberger, M., Duarte, H., Quintela, M., Tejedo, M., & Laurila, A. (2015). Local divergence of thermal reaction norms among amphibian populations is affected by pond temperature variation. Evolution, 69, 2210-2226. https://doi.org/10.1111/evo.12711
Roznik, E. A., & Johnson, S. A. (2009). Burrow use and survival of newly metamorphosed Gopher frogs (Rana capito). Journal of Herpetology, 43, 431-437. https://doi.org/10.1670/08-159R.1
Ruiz-Aravena, M., Gonzalez-Mendez, A., Estay, S. A., Gaitán-Espitia, J. D., Barria-Oyarzo, I., Bartheld, J. L., & Bacigalupe, L. D. (2014). Impact of global warming at the range margins: Phenotypic plasticity and behavioral thermoregulation will buffer an endemic amphibian. Ecology and Evolution, 4, 4467-4475. https://doi.org/10.1002/ece3.1315
Schwartz, M. V., Iverson, L. R., Prasad, A. M., Matthews, S. N., & O'Connor, R. J. (2006). Predicting extinctions as a result of climate change. Ecology, 87, 1611-1615. https://doi.org/10.1890/0012-9658(2006)87[1611:PEAARO]2.0.CO;2
Seebacher, F., White, C. R., & Franklin, C. E. (2015). Physiological plasticity increases resilience of ectothermic animals to climate change. Nature Climate Change, 5, 61-66. https://doi.org/10.1038/nclimate2457
Sinclair, B. J., Marshall, K. E., Sewell, M. A., Levesque, D. L., Willett, C. S., Slotsbo, S., … Huey, R. B. (2016). Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecology Letters, 19, 1372-1385. https://doi.org/10.1111/ele.12686
Sinclair, B. J., Williams, C. M., & Terblanche, J. S. (2012). Variation in thermal performance among insect populations. Physiological and Biochemical Zoology, 85, 594-606. https://doi.org/10.1086/665388
Slatyer, R. A., & Schoville, S. D. (2016). Physiological limits along an elevational gradient in a radiation of montane ground beetles. PLoS ONE, 11, e0151959. https://doi.org/10.1371/journal.pone.0151959
Sørensen, J. G., Dahlgaard, J., & Loeschcke, V. (2001). Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: Down regulation of Hsp70 expression and variation in heat stress resistance traits. Functional Ecology, 15, 289-296. https://doi.org/10.1046/j.1365-2435.2001.00525.x
Stillman, J. H. (2003). Acclimation capacity underlies susceptibility to climate change. Science, 301, 65-65. https://doi.org/10.1126/science.1083073
Sultan, S. E., & Spencer, H. G. (2002). Metapopulation structure favors plasticity over local adaptation. The American Naturalist, 160, 271-283. https://doi.org/10.1086/341015
Sunday, J. M., Bates, A. E., & Dulvy, N. K. (2011). Global analysis of thermal tolerance and latitude in ectotherms. Proceedings of the Royal Society B: Biological Sciences, 278, 1823-1830. https://doi.org/10.1098/rspb.2010.1295
Sunday, J. M., Bates, A. E., Kearney, M. R., Colwell, R. K., Dulvy, N. K., Longino, J. T., & Huey, R. B. (2014). Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proceedings of the National Academy of Sciences of the United States of America, 111, 5610-5615. https://doi.org/10.1073/pnas.1316145111
Tewksbury, J. J., Huey, R. B., & Deutsch, C. A. (2008). Putting the heat on tropical animals. Science, 320, 1296-1297.
Thomas, C. D., Cameron, A., Green, R. E., Bakkenes, M., Beaumont, L. J., Collingham, Y. C., … Williams, S. E. (2004). Extinction risk from climate change. Nature, 427, 145-148. https://doi.org/10.1038/nature02121
Tracy, C. R. (1976). A model of the dynamic exchanges of water and energy between a terrestrial amphibian and its environment. Ecological Monographs, 46, 293-326. https://doi.org/10.2307/1942256
Valladares, F., Matesanz, S., Guilhaumon, F., Araújo, M. B., Balaguer, L., Benito-Garzón, M., … Zavala, M. A. (2014). The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecology Letters, 17, 1351-1364. https://doi.org/10.1111/ele.12348
Veith, M., Baumgart, A., Dubois, A., Ohler, A., Galan, P., Vieites, D. R., … Vences, M. (2012). Discordant patterns of nuclear and mitochondrial introgression in Iberian populations of the European common frog (Rana temporaria). The Journal of Heredity, 103, 240-249. https://doi.org/10.1093/jhered/esr136
Vences, M., Galan, P., Palanca, A., Vieites, D. R., Nieto, S., & Rey, J. (2000). Summer microhabitat use and diel activity cycles in a high altitude Pyrenean population of Rana temporaria. Herpetological Journal, 10, 49-56.
Vences, M., Hauswaldt, J. S., Steinfartz, S., Rupp, O., Goesmann, A., Künzel, S., … Smirnov, N. A. (2013). Radically different phylogeographies and patterns of genetic variation in two European brown frogs, genus Rana. Molecular Phylogenetics and Evolution, 68, 657-670. https://doi.org/10.1016/j.ympev.2013.04.014
von May, R., Catenazzi, A., Corl, A., Santa-Cruz, R., Carnaval, A. C., & Moritz, C. (2017). Divergence of thermal physiological traits in terrestrial breeding frogs along a tropical elevational gradient. Ecology and Evolution, 7, 3257-3267. https://doi.org/10.1002/ece3.2929
Wake, D. B., & Lynch, J. F. (1976). The distribution, ecology, and evolutionary history of plethodontid salamanders in Tropical America. Los Angeles, CA: Natural History Museum of Los Angeles County. Retrieved from https://www.researchgate.net/publication/285484623_The_distribution_ecology_and_evolutionary_history_of_plethodontid_salamanders_in_tropical_America
Williams, J. W., Jackson, S. T., & Kutzbacht, J. E. (2007). Projected distributions of novel and disappearing climates by 2100 AD. Proceedings of the National Academy of Sciences of the United States of America, 104(14), 5738-5742. https://doi.org/10.1073/pnas.0606292104
Williams, S. E., Shoo, L. P., Isaac, J. L., Hoffmann, A. A., & Langham, G. (2008). Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biology, 6, e325. https://doi.org/10.1371/journal.pbio.0060325