RESEARCH ARTICLE
Additive effects of developmental acclimation and physiological syndromes on lifetime metabolic and water loss rates of a dry-skinned ectotherm
Mathias Dezetter,
Andréaz Dupoué,
Jean-François Le Galliard,
Olivier Lourdais,
Corresponding Author
Mathias Dezetter
CNRS Sorbonne Université, UMR 7618, iEES Paris, Université Pierre et Marie Curie, Paris, France
Centre d’étude Biologique de Chizé CNRS, UMR 7372, Villiers en Bois, France
Correspondence
Mathias Dezetter
Email: [email protected]
Search for more papers by this authorAndréaz Dupoué
CNRS Sorbonne Université, UMR 7618, iEES Paris, Université Pierre et Marie Curie, Paris, France
Search for more papers by this authorJean-François Le Galliard
CNRS Sorbonne Université, UMR 7618, iEES Paris, Université Pierre et Marie Curie, Paris, France
Ecole Normale Supérieure, PSL Research University, CNRS, UMS 3194, Centre de Recherche en Écologie Expérimentale et Prédictive (CEREEP-Ecotron IleDeFrance), Saint-Pierre-lès-Nemours, France
Search for more papers by this authorOlivier Lourdais
Centre d’étude Biologique de Chizé CNRS, UMR 7372, Villiers en Bois, France
School of Life Sciences, Arizona State University, Tempe, AZ, USA
Search for more papers by this authorMathias Dezetter,
Andréaz Dupoué,
Jean-François Le Galliard,
Olivier Lourdais,
Corresponding Author
Mathias Dezetter
CNRS Sorbonne Université, UMR 7618, iEES Paris, Université Pierre et Marie Curie, Paris, France
Centre d’étude Biologique de Chizé CNRS, UMR 7372, Villiers en Bois, France
Correspondence
Mathias Dezetter
Email: [email protected]
Search for more papers by this authorAndréaz Dupoué
CNRS Sorbonne Université, UMR 7618, iEES Paris, Université Pierre et Marie Curie, Paris, France
Search for more papers by this authorJean-François Le Galliard
CNRS Sorbonne Université, UMR 7618, iEES Paris, Université Pierre et Marie Curie, Paris, France
Ecole Normale Supérieure, PSL Research University, CNRS, UMS 3194, Centre de Recherche en Écologie Expérimentale et Prédictive (CEREEP-Ecotron IleDeFrance), Saint-Pierre-lès-Nemours, France
Search for more papers by this authorOlivier Lourdais
Centre d’étude Biologique de Chizé CNRS, UMR 7372, Villiers en Bois, France
School of Life Sciences, Arizona State University, Tempe, AZ, USA
Search for more papers by this authorHandling Editor: Katie Marshall
Abstract
- Developmental plasticity and thermal acclimation can contribute to adaptive responses to climate change by altering functional traits related to energy and water balance regulation. How plasticity interacts with physiological syndromes through lifetime in long-lived species is currently unknown.
- Here, we examined the impacts of long-term thermal acclimation in a long-lived temperate ectotherm Vipera aspis and its potential flexibility at adulthood for two related functional traits: standard metabolic rate (SMR) and total evaporative water loss (TEWL).
- We used climatic chambers to simulate three contrasted daily thermal cycles (warm, medium and cold) differing in mean temperatures (28, 24 and 20℃ respectively) and amplitudes (5, 10 and 13℃ respectively) during immature life (0 to 4 years of age). Individuals were then maintained under common garden conditions (medium cycle) for an additional 3-year period (4–7 years of age). SMR and TEWL were repeatedly measured in the same individuals throughout life during and after the climate manipulation.
- Individuals reduced their SMR (negative compensation) when experiencing the warm cycle but flexibly adjusted their SMR to common garden conditions at adulthood. In addition, thermal conditions during the juvenile life stage led to changes in TEWL persisting until adulthood.
- We further found consistent intra-individual variation for SMR and TEWL and a positive intra-individual and inter-individual covariation between them throughout life. Thus, plastic responses were combined with a physiological syndrome linking SMR and TEWL.
- Our study demonstrates the capacity of long-lived organisms to flexibly shift their SMR to reduce daily maintenance costs in warmer and less variable thermal environments, which might be beneficial to low-energy specialist organisms such as vipers. It further suggests that thermal conditions provide cues for developmental changes in TEWL. Beside plasticity, contrasted individual physiological syndromes could be selected for and contribute to the response to climate change.
A free Plain Language Summary can be found within the Supporting Information of this article.
CONFLICT OF INTEREST
The authors declare no competing or financial interests.
Open Research
DATA AVAILABILITY STATEMENT
Data are available at Zenodo with https://doi.org/10.5281/zenodo.5561142 (Dezetter et al., 2021).
Supporting Information
| Filename | Description |
|---|---|
| fec13951-sup-0001-Summary.pdfPDF document, 1 MB | Supplementary Material |
| fec13951-sup-0002-AppendixS1.docxWord 2007 document , 19.1 KB | Appendix S1 |
| fec13951-sup-0003-TableS1.docxWord 2007 document , 16.3 KB | Table S1 |
| fec13951-sup-0004-TableS2.docxWord 2007 document , 19.6 KB | Table S2 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Addo-Bediako, A., Chown, S. L., & Gaston, K. J. (2002). Metabolic cold adaptation in insects: A large-scale perspective. Functional Ecology. https://doi.org/10.1046/j.1365-2435.2002.00634.x
- Angilletta Jr., M. J. (2009). Thermal adaptation. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198570875.001.1
- Arnold, P. A., Delean, S., Cassey, P., & White, C. R. (2021). Meta-analysis reveals that resting metabolic rate is not consistently related to fitness and performance in animals. Journal of Comparative Physiology B, 1–14. https://doi.org/10.1007/s00360-021-01358-w
- Baškiera, S., & Gvoždík, L. (2020). Repeatability and heritability of resting metabolic rate in a long-lived amphibian. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 253, 110858. https://doi.org/10.1016/j.cbpa.2020.110858
- Beaman, J. E., White, C. R., & Seebacher, F. (2016). Evolution of plasticity: Mechanistic link between development and reversible acclimation. Trends in Ecology & Evolution, 31(3), 237–249. https://doi.org/10.1016/j.tree.2016.01.004
- Berg, W., Theisinger, O., & Dausmann, K. H. (2017). Acclimatization patterns in tropical reptiles: uncoupling temperature and energetics. The Science of Nature, 104(11-12). https://doi.org/10.1007/s00114-017-1506-0
- Biro, P. A., & Stamps, J. A. (2010). Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends in Ecology & Evolution, 25(11), 653–659. https://doi.org/10.1016/j.tree.2010.08.003
- Blouin-Demers, G., & Weatherhead, P. J. (2001). Thermal ecology of black rat snakes (Elaphe obsoleta) in a thermally challenging environment. Ecology, 82, 3025–3043. https://doi.org/10.1890/0012-9658(2001)082[3025:TEOBRS]2.0.CO;2
- Bonamour, S., Chevin, L. M., Charmantier, A., & Teplitsky, C. (2019). Phenotypic plasticity in response to climate change: the importance of cue variation. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1768), 20180178. https://doi.org/10.1098/rstb.2018.0178
- Bonnet, X., Naulleau, G., & Lourdais, O. (1999). Growth in the asp viper (Vipera aspis L.): Insights from long term field study. Current Studies in Herpetology, 63–69.
- Bozinovic, F., Bastías, D. A., Boher, F., Clavijo-Baquet, S., Estay, S. A., & Angilletta, M. J. (2011). The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiological and Biochemical Zoology, 84, 543–552. https://doi.org/10.1086/662551
- Bruton, M. J., Cramp, R. L., & Franklin, C. E. (2012). Benefits of thermal acclimation in a tropical aquatic ectotherm, the Arafura filesnake, Acrochordus arafurae. Journal of Comparative Physiology B: Biochemical, Systems, and Environmental Physiology, 182, 541–551. https://doi.org/10.1007/s00360-011-0643-6
- Careau, V., Beauchamp, P. P., Bouchard, S., & Morand-Ferron, J. (2019). Energy metabolism and personality in wild-caught fall field crickets. Physiology & Behavior, 199, 173–181. https://doi.org/10.1016/j.physbeh.2018.11.023
- Careau, V., Gifford, M. E., & Biro, P. A. (2014). Individual (co)variation in thermal reaction norms of standard and maximal metabolic rates in wild-caught slimy salamanders. Functional Ecology, 28(5), 1175–1186. https://doi.org/10.1111/1365-2435.12259
- Careau, V., Thomas, D., Humphries, M. M., & Réale, D. (2008). Energy metabolism and animal personality. Oikos, 117(5), 641–653. https://doi.org/10.1111/j.0030-1299.2008.16513.x
- 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
- Chung, D. J., Bryant, H. J., & Schulte, P. M. (2017). Thermal acclimation and subspecies-specific effects on heart and brain mitochondrial performance in a eurythermal teleost (Fundulus heteroclitus). Journal of Experimental Biology, 220, 1459–1471. https://doi.org/10.1242/jeb.151217
- Clarke, A. (2006). Temperature and the metabolic theory of ecology. Functional Ecology, 20, 405–412. https://doi.org/10.1111/j.1365-2435.2006.01109.x
- Colinet, H., Sinclair, B. J., Vernon, P., & Renault, D. (2015). Insects in fluctuating thermal environments. Annual Review of Entomology, 60, 123–140. https://doi.org/10.1146/annurev-ento-010814-021017
- Costantini, D. (2008). Oxidative stress in ecology and evolution: Lessons from avian studies. Ecology Letters, 11, 1238–1251. https://doi.org/10.1111/j.1461-0248.2008.01246.x
- da Silva, C. R. B., Riginos, C., & Wilson, R. S. (2019). An intertidal fish shows thermal acclimation despite living in a rapidly fluctuating environment. Journal of Comparative Physiology B, 189(3-4), 385–398. https://doi.org/10.1007/s00360-019-01212-0
- Dai, A. (2013). Increasing drought under global warming in observations and models. Nature Climate Change, 3, 52–58. https://doi.org/10.1038/nclimate1633
- Davy, R., Esau, I., Chernokulsky, A., Outten, S., & Zilitinkevich, S. (2017). Diurnal asymmetry to the observed global warming. International Journal of Climatology, 37, 79–93. https://doi.org/10.1002/joc.4688
- Dezetter, M., Dupoué, A., Le Galliard, J.-F., & Lourdais, O. (2021). Data from: Additive effects of developmental acclimation and physiological syndromes on lifetime metabolic and water loss rates of a dry-skinned ectotherm. Zenodo, https://doi.org/10.5281/ZENODO.5561142
- Dupoué, A., Brischoux, F., & Lourdais, O. (2017). Climate and foraging mode explain interspecific variation in snake metabolic rates. Proceedings of the Royal Society B-Biological Sciences, 284, 20172108. https://doi.org/10.1098/rspb.2017.2108
- Dupoué, A., Stahlschmidt, Z. R., Michaud, B., & Lourdais, O. (2015). Physiological state influences evaporative water loss and microclimate preference in the snake Vipera aspis. Physiology & Behavior, 144, 82–89. https://doi.org/10.1016/j.physbeh.2015.02.042
- Einum, S., Ratikainen, I., Wright, J., Pélabon, C., Bech, C., Jutfelt, F., Stawski, C., & Burton, T. (2019). How to quantify thermal acclimation capacity? Global Change Biology, 25, 1893–1894. https://doi.org/10.1111/gcb.14598
- Fuller, A., Dawson, T. J., Helmuth, B., Hetem, R. S., Mitchell, D., & Maloney, S. K. (2010). Physiological mechanisms in coping with climate change. Physiological and Biochemical Zoology, 83, 713–720. https://doi.org/10.1086/652242
- Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007). Early life events and their consequences for later disease: A life history and evolutionary perspective. American Journal of Human Biology, 19, 1–19. https://doi.org/10.1002/ajhb.20590
- Goulet, C. T., Thompson, M. B., & Chapple, D. G. (2017). Repeatability and correlation of physiological traits: Do ectotherms have a “thermal type”? Ecology and Evolution, 7, 710–719. https://doi.org/10.1002/ece3.2632
- Goulet, C. T., Thompson, M. B., Michelangeli, M., Wong, B. B. M., & Chapple, D. G. (2017). Thermal physiology: A new dimension of the pace-of-life syndrome. Journal of Animal Ecology, 86, 1269–1280. https://doi.org/10.1111/1365-2656.12718
- 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(8), 1529–1539. https://doi.org/10.1111/1365-2435.12874
- 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(1808), 20150401. https://doi.org/10.1098/rspb.2015.0401
- Hadfield, J. (2009). MCMC methods for multi-response generalized linear mixed models. The MCMCglmm R package.
- Havird, J. C., Neuwald, J. L., Shah, A. A., Mauro, A., Marshall, C. A., & Ghalambor, C. K. (2020). Distinguishing between active plasticity due to thermal acclimation and passive plasticity due to Q10 effects: Why methodology matters. Functional Ecology, 34, 1015–1028. https://doi.org/10.1111/1365-2435.13534
- Healy, T. M., Bock, A. K., & Burton, R. S. (2019). Variation in developmental temperature alters adulthood plasticity of thermal tolerance in Tigriopus californicus. Journal of Experimental Biology, 222. https://doi.org/10.1242/JEB.213405
- 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
- Kern, P., Cramp, R. L., & Franklin, C. E. (2015). Physiological responses of ectotherms to daily temperature variation. Journal of Experimental Biology, 218, 3068–3076. https://doi.org/10.1242/jeb.123166
- Kingsolver, J. G., & Huey, R. B. (2008). Size, temperature, and fitness: Three rules. Evolutionary Ecology Research, 10(2), 251–268.
- Lenth, R., Singmann, H., Love, J., Buerkner, P., & Herve, M. (2020). emmeans: Estimated marginal means. R package version 1.4.4. American Statistician, 34, 216–221.
- Ligon, D. B., Peterson, C. C., & Lovern, M. B. (2012). Acute and persistent effects of pre- and posthatching thermal environments on growth and metabolism in the red-eared slider turtle, Trachemys scripta elegans. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 317, 227–235. https://doi.org/10.1002/jez.1716
- Little, A. G., & Seebacher, F. (2017). Acclimation, acclimatization, and seasonal variation in amphibians and reptiles. In Amphibian and reptile adaptations to the environment (pp. 41–62). CRC Press.
- Lorioux, S., Vaugoyeau, M., Denardo, D. F., Clobert, J., Guillon, M., & Lourdais, O. (2013). Stage dependence of phenotypical and phenological maternal effects: Insight into squamate reptile reproductive strategies. The American Naturalist, 182, 223–233. https://doi.org/10.1086/670809
- Mathot, K. J., & Dingemanse, N. J. (2015). Energetics and behavior: Unrequited needs and new directions. Trends in Ecology & Evolution, 30(4), 199–206. https://doi.org/10.1016/j.tree.2015.01.010
- Mell, H., Josserand, R., Decencière, B., Artacho, P., Meylan, S., & Le Galliard, J. F. (2016). Do personalities co-vary with metabolic expenditure and glucocorticoid stress response in adult lizards? Behavioral Ecology and Sociobiology, 70, 951–961. https://doi.org/10.1007/s00265-016-2117-z
- Morash, A. J., Neufeld, C., MacCormack, T. J., & Currie, S. (2018). The importance of incorporating natural thermal variation when evaluating physiological performance in wild species. Journal of Experimental Biology, 221(14). https://doi.org/10.1242/jeb.164673
- Morley, S. A., Peck, L. S., Sunday, J. M., Heiser, S., & Bates, A. E. (2019). Physiological acclimation and persistence of ectothermic species under extreme heat events. Global Ecology and Biogeography, 28, 1018–1037. https://doi.org/10.1111/geb.12911
- Naulleau, G. (1983). The effects of temperature on digestion in Vipera aspis. Journal of Herpetology, 17, 166. https://doi.org/10.2307/1563457
- Nespolo, R. F., & Franco, M. (2007). Whole-animal metabolic rate is a repeatable trait: A meta-analysis. Journal of Experimental Biology, 210, 2000–2005. https://doi.org/10.1242/jeb.02780
- Nespolo, R. F., Lardies, M. A., & Bozinovic, F. (2003). Intrapopulational variation in the standard metabolic rate of insects: Repeatability, thermal dependence and sensitivity (Q10) of oxygen consumption in a cricket. Journal of Experimental Biology, 206, 4309–4315. https://doi.org/10.1242/jeb.00687
- Nettle, D., & Bateson, M. (2015). Adaptive developmental plasticity: What is it, how can we recognize it and when can it evolve? Proceedings of the Royal Society B: Biological Sciences, 282, 20151005. https://doi.org/10.1098/rspb.2015.1005
- Niehaus, A. C., Wilson, R. S., Seebacher, F., & Franklin, C. E. (2011). Striped marsh frog (Limnodynastes peronii) tadpoles do not acclimate metabolic performance to thermal variability. Journal of Experimental Biology, 214, 1965–1970. https://doi.org/10.1242/jeb.054478
- Nilsson, J.-Å., Åkesson, M., & Nilsson, J. F. (2009). Heritability of resting metabolic rate in a wild population of blue tits. Journal of Evolutionary Biology, 22, 1867–1874. https://doi.org/10.1111/j.1420-9101.2009.01798.x
- Noble, D. W. A., Stenhouse, V., & Schwanz, L. E. (2018). Developmental temperatures and phenotypic plasticity in reptiles: A systematic review and meta-analysis. Biological Reviews, 93, 72–97. https://doi.org/10.1111/brv.12333
- Noer, N. K., Pagter, M., Bahrndorff, S., Malmendal, A., & Kristensen, T. N. (2020). Impacts of thermal fluctuations on heat tolerance and its metabolomic basis in Arabidopsis thaliana, Drosophila melanogaster, and Orchesella cincta. PLoS One, 15, e0237201. https://doi.org/10.1371/journal.pone.0237201
- Norin, T., Malte, H., & Clark, T. D. (2014). Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. Journal of Experimental Biology, 217, 244–251. https://doi.org/10.1242/jeb.089755
- Norin, T., & Metcalfe, N. B. (2019). Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1768), 20180180. https://doi.org/10.1098/rstb.2018.0180
- Pallarés, S., Colado, R., Botella-Cruz, M., Montes, A., Balart-García, P., Bilton, D. T., Millán, A., Ribera, I., & Sánchez-Fernández, D. (2020). Loss of heat acclimation capacity could leave subterranean specialists highly sensitive to climate change. Animal Conservation, 1–9. https://doi.org/10.1111/acv.12654
- Pettersen, A. K., Marshall, D. J., & White, C. R. (2018). Understanding variation in metabolic rate. Journal of Experimental Biology, 221(1). https://doi.org/10.1242/jeb.166876
- Piersma, T., & van Gils, J. A. (2011). The flexible phenotype: A body-centred integration of ecology, physiology, and behaviour. Oxford University Press.
- Pinheiro, J., & Bates, D. (2006). Mixed-effects models in S and S-PLUS.
- Pörtner, H. O., Bock, C., & Mark, F. C. (2017). Oxygen- & capacity-limited thermal tolerance: Bridging ecology & physiology. Journal of Experimental Biology. https://doi.org/10.1242/jeb.134585
- Potter, K. A., Woods, H. A., & Pincebourde, S. (2013). Microclimatic challenges in global change biology. Global Change Biology. 19, 2932–2939. https://doi.org/10.1111/GCB.12257
- R Core Team. (2020). R: A Language and environment for statistical computing. pdfs.semanticscholar.org.
- Refsnider, J. M., Clifton, I. T., & Vazquez, T. K. (2019). Developmental plasticity of thermal ecology traits in reptiles: Trends, potential benefits, and research needs. Journal of Thermal Biology, 84, 74–82. https://doi.org/10.1016/j.jtherbio.2019.06.005
- Réveillon, T., Rota, T., Chauvet, É., Lecerf, A., & Sentis, A. (2019). Repeatable inter-individual variation in the thermal sensitivity of metabolic rate. Oikos, 128, 1633–1640. https://doi.org/10.1111/oik.06392
- Riddell, E. A., McPhail, J., Damm, J. D., & Sears, M. W. (2018). Trade-offs between water loss and gas exchange influence habitat suitability of a woodland salamander. Functional Ecology, 32, 916–925. https://doi.org/10.1111/1365-2435.13030
- Riddell, E. A., Odom, J. P., Damm, J. D., & Sears, M. W. (2018). Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity. Science Advances, 4. https://doi.org/10.1126/sciadv.aar5471
- Riddell, E. A., Roback, E. Y., Wells, C. E., Zamudio, K. R., & Sears, M. W. (2019). Thermal cues drive plasticity of desiccation resistance in montane salamanders with implications for climate change. Nature Communications, 10, 4091. https://doi.org/10.1038/s41467-019-11990-4
- Riddell, E. A., & Sears, M. W. (2020). Terrestrial salamanders maintain habitat suitability under climate change despite trade-offs between water loss and gas exchange. Physiological and Biochemical Zoology, 93(4), 310–319. https://doi.org/10.1086/709558
- Rohr, J. R., Civitello, D. J., Cohen, J. M., Roznik, E. A., Sinervo, B., & Dell, A. I. (2018). The complex drivers of thermal acclimation and breadth in ectotherms. Ecology Letters, 21, 1425–1439. https://doi.org/10.1111/ele.13107
- Rozen-Rechels, D., Dupoué, A., Lourdais, O., Chamaillé-Jammes, S., Meylan, S., Clobert, J., & Le Galliard, J. (2019). When water interacts with temperature: Ecological and evolutionary implications of thermo-hydroregulation in terrestrial ectotherms. Ecology and Evolution, 9, 10029–10043. https://doi.org/10.1002/ece3.5440
- Seebacher, F. (2005). A review of thermoregulation and physiological performance in reptiles: What is the role of phenotypic flexibility? Journal of Comparative Physiology B: Biochemical, Systems, and Environmental Physiology, 175(7), 453–461. https://doi.org/10.1007/s00360-005-0010-6
- Seebacher, F., Brand, M. D., Else, P. L., Guderley, H., Hulbert, A. J., & Moyes, C. D. (2010). Plasticity of oxidative metabolism in variable climates: Molecular mechanisms. Physiological and Biochemical Zoology, 83, 721–732. https://doi.org/10.1086/649964
- Seebacher, F., White, C. R., & Franklin, C. E. (2015). Physiological plasticity increases resilience of ectothermic animals to climate change. Nature Climate Change, 5(1), 61–66. https://doi.org/10.1038/nclimate2457
- Somero, G. N. (2010). The physiology of climate change: How potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. Journal of Experimental Biology, 213, 912–920. https://doi.org/10.1242/jeb.037473
- Sultan, S. E. (2017). Developmental plasticity: Re-conceiving the genotype. Interface Focus, 7(5), 20170009. https://doi.org/10.1098/rsfs.2017.0009
- Urban, M. C., Richardson, J. L., & Freidenfelds, N. A. (2014). Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change. Evolutionary Applications, 7(1), 88–103. https://doi.org/10.1111/eva.12114
- Verheyen, J., & Stoks, R. (2019). Temperature variation makes an ectotherm more sensitive to global warming unless thermal evolution occurs. Journal of Animal Ecology, 88, 624–636. https://doi.org/10.1111/1365-2656.12946
- Vincent, S. E., & Mori, A. (2007). Determinants of feeding performance in free-ranging pit-vipers (Viperidae: Ovophis okinavensis): Key roles for head size and body temperature. Biological Journal of the Linnean Society, 93, 53–62. https://doi.org/10.1111/j.1095-8312.2007.00928.x
- While, G. M., Noble, D. W. A., Uller, T., Warner, D. A., Riley, J. L., Du, W.-G., & Schwanz, L. E. (2018). Patterns of developmental plasticity in response to incubation temperature in reptiles. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 329, 162–176. https://doi.org/10.1002/jez.2181
- White, C. R., Marshall, D. J., Alton, L. A., Arnold, P. A., Beaman, J. E., Bywater, C. L., Condon, C., Crispin, T. S., Janetzki, A., Pirtle, E., Winwood-Smith, H. S., Angilletta, M. J., Chenoweth, S. F., Franklin, C. E., Halsey, L. G., Kearney, M. R., Portugal, S. J., & Ortiz-Barrientos, D. (2019). The origin and maintenance of metabolic allometry in animals. Nature Ecology & Evolution, 3, 598–603. https://doi.org/10.1038/s41559-019-0839-9
- Woods, H. A., & Smith, J. N. (2010). Universal model for water costs of gas exchange by animals and plants. Proceedings of the National Academy of Sciences of the United States of America, 107, 8469–8474. https://doi.org/10.1073/pnas.0905185107
- Xie, H., Lü, X., Zhou, J., Shi, C., Li, Y., Duan, T., Li, G., & Luo, Y. (2017). Effects of acute temperature change and temperature acclimation on the respiratory metabolism of the snakehead. Turkish Journal of Fisheries and Aquatic Sciences, 17, 535–542. https://doi.org/10.4194/1303-2712-v17_3_10
- Žagar, A., Carretero, M. A., Marguč, D., Simčič, T., & Vrezec, A. (2018). A metabolic syndrome in terrestrial ectotherms with different elevational and distribution patterns. Ecography (Cop.), 41, 1728–1739. https://doi.org/10.1111/ecog.03411
- Zari, A. T. (1996). Seasonal metabolic compensation in the fringe-toed lizard, Acanthodactylus boskianus (Reptilia. Lacertidae). Journal of Thermal Biology, 145–150. https://doi.org/10.1016/0306-4565(95)00040-2
