Physiological determinants of biogeography: The importance of metabolic depression to heat tolerance.
climate change
inter-individual variability
metabolic depression
physiological adaptations
species distribution modeling
thermal performance curve
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
Jun 2021
Jun 2021
Historique:
revised:
25
01
2021
received:
09
11
2020
accepted:
26
02
2021
pubmed:
6
3
2021
medline:
28
5
2021
entrez:
5
3
2021
Statut:
ppublish
Résumé
A quantitative understanding of physiological thermal responses is vital for forecasting species distributional shifts in response to climate change. Many studies have focused on metabolic rate as a global metric for analyzing the sublethal effects of changing environments on physiology. Thermal performance curves (TPCs) have been suggested as a viable analytical framework, but standard TPCs may not fully capture physiological responses, due in part to failure to consider the process of metabolic depression. We derived a model based on the nonlinear regression of biological temperature-dependent rate processes and built a heart rate data set for 26 species of intertidal molluscs distributed from 33°S to ~40°N. We then calculated physiological thermal performance limits with continuous heating using
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2561-2579Subventions
Organisme : National Natural Science Foundation of China
ID : 41776135
Organisme : National Natural Science Foundation of China
ID : 41976142
Organisme : National Natural Science Foundation of China
ID : 42025604
Organisme : Chinese Postdoctoral Science Foundation
ID : 2020M672140
Organisme : Young Elite Scientists Sponsorship Program by CAST
ID : 2019QNRC001
Organisme : Fundamental Research Funds for the Central Universities of the Ocean University of China
Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Anestis, A., Lazou, A., Portner, H. O., & Michaelidis, B. (2007). Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. American Journal of Physiology Regulatory Integrative and Comparative Physiology, 293(2), R911-921. https://doi.org/10.1152/ajpregu.00124.2007
Angilletta, Jr., M. J. (2006). Estimating and comparing thermal performance curves. Journal of Thermal Biology, 31(7), 541-545. https://doi.org/10.1016/j.jtherbio.2006.06.002
Angilletta, Jr., M. J. (2009). Thermal adaptation: A theoretical and empirical synthesis. Oxford University Press.
Angilletta, Jr., M. J., Wilson, R. S., Navas, C. A., & James, R. S. (2003). Tradeoffs and the evolution of thermal reaction norms. Trends in Ecology & Evolution, 18(5), 234-240. https://doi.org/10.1016/S0169-5347(03)00087-9
Araújo, M. B., Anderson, R. P., Márcia Barbosa, A., Beale, C. M., Dormann, C. F., Early, R., Garcia, R. A., Guisan, A., Maiorano, L., Naimi, B., O'Hara, R. B., Zimmermann, N. E., & Rahbek, C. (2019). Standards for distribution models in biodiversity assessments. Science Advances, 5(1), eaat4858. https://doi.org/10.1126/sciadv.aat4858
Araújo, M. B., & Peterson, A. T. (2012). Uses and misuses of bioclimatic envelope modeling. Ecology, 93(7), 1527-1539. https://doi.org/10.1890/11-1930.1
Austin, M. P., & Van Niel, K. P. (2011). Improving species distribution models for climate change studies: Variable selection and scale. Journal of Biogeography, 38(1), 1-8. https://doi.org/10.1111/j.1365-2699.2010.02416.x
Bates, A. E., Helmuth, B., Burrows, M. T., Duncan, M. I., Garrabou, J., Guy-Haim, T., Lima, F., Queiros, A. M., Seabra, R., Marsh, R., Belmaker, J., Bensoussan, N., Dong, Y. W., Mazaris, A. D., Smale, D., Wahl, M., & Rilov, G. (2018). Biologists ignore ocean weather at their peril. Nature, 560(7718), 299-301. https://doi.org/10.1038/d41586-018-05869-5
Braby, C. E., & Somero, G. N. (2006). Following the heart: Temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). Journal of Experimental Biology, 209(13), 2554-2566. https://doi.org/10.1242/jeb.02259
Briscoe, N. J., Elith, J., Salguero-Gomez, R., Lahoz-Monfort, J. J., Camac, J. S., Giljohann, K. M., Holden, M. H., Hradsky, B. A., Kearney, M. R., McMahon, S. M., Phillips, B. L., Regan, T. J., Rhodes, J. R., Vesk, P. A., Wintle, B. A., Yen, J. D. L., & Guillera-Arroita, G. (2019). Forecasting species range dynamics with process-explicit models: Matching methods to applications. Ecology Letters, 22(11), 1940-1956. https://doi.org/10.1111/ele.13348
Briscoe, N. J., Kearney, M. R., Taylor, C. A., & Wintle, B. A. (2016). Unpacking the mechanisms captured by a correlative species distribution model to improve predictions of climate refugia. Global Change Biology, 22(7), 2425-2439. https://doi.org/10.1111/gcb.13280
Brose, U., Archambault, P., Barnes, A. D., Bersier, L.-F., Boy, T., Canning-Clode, J., Conti, E., Dias, M., Digel, C., Dissanayake, A., Flores, A. A. V., Fussmann, K., Gauzens, B., Gray, C., Häussler, J., Hirt, M. R., Jacob, U., Jochum, M., Kéfi, S., … Iles, A. C. (2019). Predator traits determine food-web architecture across ecosystems. Nature Ecology & Evolution, 3(6), 919-927. https://doi.org/10.1038/s41559-019-0899-x
Buckley, L. B., Waaser, S. A., MacLean, H. J., & Fox, R. (2011). Does including physiology improve species distribution model predictions of responses to recent climate change? Ecology, 92(12), 2214-2221. https://doi.org/10.1890/11-0066.1
Burnett, N. P., Seabra, R., de Pirro, M., Wethey, D. S., Woodin, S. A., Helmuth, B., Zippay, M. L., Sarà, G., Monaco, C., & Lima, F. P. (2013). An improved noninvasive method for measuring heartbeat of intertidal animals. Limnology and Oceanography: Methods, 11(2), 91-100. https://doi.org/10.4319/lom.2013.11.91
Bush, A., Mokany, K., Catullo, R., Hoffmann, A., Kellermann, V., Sgro, C., McEvey, S., & Ferrier, S. (2016). Incorporating evolutionary adaptation in species distribution modelling reduces projected vulnerability to climate change. Ecology Letters, 19(12), 1468-1478. https://doi.org/10.1111/ele.12696
Castañeda, L. E., Rezende, E. L., & Santos, M. (2015). Heat tolerance in Drosophila subobscura along a latitudinal gradient: Contrasting patterns between plastic and genetic responses. Evolution, 69(10), 2721-2734. https://doi.org/10.1111/evo.12757
Chelazzi, G., De Pirro, M., & Williams, G. A. (2001). Cardiac responses to abiotic factors in two tropical limpets, occurring at different levels of the shore. Marine Biology, 139(6), 1079-1085. https://doi.org/10.1007/s002270100603
Chelazzi, G., Williams, G. A., & Gray, D. R. (1999). Field and laboratory measurement of heart rate in a tropical limpet, Cellana grata. Journal of the Marine Biological Association of the United Kingdom, 79(4), 749-751. https://doi.org/10.1017/S0025315498000915
Chen, S. Y., Feng, Z., & Yi, X. (2017). A general introduction to adjustment for multiple comparisons. Journal of Thoracic Disease, 9(6), 1725-1729. https://doi.org/10.21037/jtd.2017.05.34
Chidawanyika, F., & Terblanche, J. S. (2011). Rapid thermal responses and thermal tolerance in adult codling moth Cydia pomonella (Lepidoptera: Tortricidae). Journal of Insect Physiology, 57(1), 108-117. https://doi.org/10.1016/j.jinsphys.2010.09.013
Childress, E. S., & Letcher, B. H. (2017). Estimating thermal performance curves from repeated field observations. Ecology, 98(5), 1377-1387. https://doi.org/10.1002/ecy.1801
Choi, F., Gouhier, T., Lima, F., Rilov, G., Seabra, R., & Helmuth, B. (2019). Mapping physiology: Biophysical mechanisms define scales of climate change impacts. Conservation. Physiology, 7(1), coz028. https://doi.org/10.1093/conphys/coz028
Chown, S. L. (2012). Trait-based approaches to conservation physiology: forecasting environmental change risks from the bottom up. Philosophical Transactions of the Royal Society B: Biological Sciences, 367(1596), 1615-1627. https://doi.org/10.1098/rstb.2011.0422
Chown, S. L., & Gaston, K. J. (2008). Macrophysiology for a changing world. Proceedings of the Royal Society B: Biological Sciences, 275(1642), 1469-1478. https://doi.org/10.1098/rspb.2008.0137
Clarke, A. (2003). Costs and consequences of evolutionary temperature adaptation. Trends in Ecology & Evolution, 18(11), 573-581. https://doi.org/10.1016/j.tree.2003.08.007
Connell, J. H. (1961). Effects of competition, predation by Thais lapillus, and other factors on natural populations of the barnacle Balanus balanoides. Ecological Monographs, 31(1), 61-104. https://doi.org/10.2307/1950746
Connor, K., & Gracey, A. Y. (2020). Cycles of heat and aerial-exposure induce changes in the transcriptome related to cell regulation and metabolism in Mytilus californianus. Marine Biology, 167, 132. https://doi.org/10.1007/s00227-020-03750-6
Denny, M. W., & Dowd, W. W. (2012). Biophysics, environmental stochasticity, and the evolution of thermal safety margins in intertidal limpets. Journal of Experimental Biology, 215(6), 934-947. https://doi.org/10.1242/jeb.058958
Denny, M. W., Dowd, W. W., Bilir, L., & Mach, K. J. (2011). Spreading the risk: Small-scale body temperature variation among intertidal organisms and its implications for species persistence. Journal of Experimental Marine Biology and Ecology, 400(1-2), 175-190. https://doi.org/10.1016/j.jembe.2011.02.006
Denny, M. W., Miller, L. P., & Harley, C. D. (2006). Thermal stress on intertidal limpets: Long-term hindcasts and lethal limits. Journal of Experimental Biology, 209(13), 2420-2431. https://doi.org/10.1242/jeb.02258
Deutsch, C., Ferrel, A., Seibel, B., Pörtner, H. O., & Huey, R. B. (2015). Ecophysiology. Climate change tightens a metabolic constraint on marine habitats. Science, 348(6239), 1132-1135. https://doi.org/10.1126/science.aaa1605
Deutsch, C., Penn, J. L., & Seibel, B. (2020). Metabolic trait diversity shapes marine biogeography. Nature, 585(7826), 557-562. https://doi.org/10.1038/s41586-020-2721-y
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(18), 6668-6672. https://doi.org/10.1073/pnas.0709472105
Diamond, S. E., Nichols, L. M., McCoy, N., Hirsch, C., Pelini, S. L., Sanders, N. J., Ellison, A. M., Gotelli, N. J., & Dunn, R. R. (2012). A physiological trait-based approach to predicting the responses of species to experimental climate warming. Ecology, 93(11), 2305-2312. https://doi.org/10.1890/11-2296.1
Dixon, A. F., Honěk, A., Keil, P., Kotela, M. A. A., Šizling, A. L., & Jarošík, V. (2009). Relationship between the minimum and maximum temperature thresholds for development in insects. Functional Ecology, 23(2), 257-264. https://doi.org/10.1111/j.1365-2435.2008.01489.x
Dong, Y. W., Han, G. D., Ganmanee, M., & Wang, J. (2015). Latitudinal variability of physiological responses to heat stress of the intertidal limpet Cellana toreuma along the Asian coast. Marine Ecology Progress Series, 529, 107-119. https://doi.org/10.3354/meps11303
Dong, Y. W., Li, X. X., Choi, F. M. P., Williams, G. A., Somero, G. N., & Helmuth, B. (2017). Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress. Proceedings of the Royal Society B: Biological Sciences, 284(1854), 20162367. https://doi.org/10.1098/rspb.2016.2367
Dong, Y. W., Liao, M. L., Meng, X. L., & Somero, G. N. (2018). Structural flexibility and protein adaptation to temperature: Molecular dynamics analysis of malate dehydrogenases of marine molluscs. Proceedings of the National Academy of Sciences of the United States of America, 115(6), 1274-1279. https://doi.org/10.1073/pnas.1718910115
Dong, Y. W., & Williams, G. A. (2011). Variations in cardiac performance and heat shock protein expression to thermal stress in two differently zoned limpets on a tropical rocky shore. Marine Biology, 158(6), 1223-1231. https://doi.org/10.1007/s00227-011-1642-6
Drake, M. J., Miller, N. A., & Todgham, A. E. (2017). The role of stochastic thermal environments in modulating the thermal physiology of an intertidal limpet, Lottia digitalis. Journal of Experimental Biology, 220(17), 3072-3083. https://doi.org/10.1242/jeb.159020
Duan, Q. Y., Gupta, V. K., & Sorooshian, S. (1993). Shuffled complex evolution approach for effective and efficient global minimization. Journal of Optimization Theory and Applications, 76(3), 501-521. https://doi.org/10.1007/Bf00939380
Duan, Q. Y., Sorooshian, S., & Gupta, V. K. (1992). Effective and efficient global optimization for conceptual rainfall-runoff models. Water Resources Research, 28(4), 1015-1031. https://doi.org/10.1029/91wr02985
Dubois, N. S., Gomez, A., Carlson, S., & Russell, D. (2020). Bridging the research-implementation gap requires engagement from practitioners. Conservation Science and Practice, 2(1), e134. https://doi.org/10.1111/csp2.134
Fangue, N. A., Mandic, M., Richards, J. G., & Schulte, P. M. (2008). Swimming performance and energetics as a function of temperature in killifish Fundulus heteroclitus. Physiological and Biochemical Zoology, 81(4), 389-401. https://doi.org/10.1086/589109
Fangue, N. A., Podrabsky, J. E., Crawshaw, L. I., & Schulte, P. M. (2009). Countergradient variation in temperature preference in populations of killifish Fundulus heteroclitus. Physiological and Biochemical Zoology, 82(6), 776-786. https://doi.org/10.1086/606030
Fell, D., & Cornish-Bowden, A. (1997). Understanding the control of metabolism. Portland Press London.
Frölicher, T. L., Fischer, E. M., & Gruber, N. (2018). Marine heatwaves under global warming. Nature, 560(7718), 360-364. https://doi.org/10.1038/s41586-018-0383-9
Gamliel, I., Buba, Y., Guy-Haim, T., Garval, T., Willett, D., Rilov, G., & Belmaker, J. (2020). Incorporating physiology into species distribution models moderates the projected impact of warming on selected Mediterranean marine species. Ecography, 43(7), 1090-1106. https://doi.org/10.1111/ecog.04423
Gaston, K. J. (2009). Geographic range limits: achieving synthesis. Proceedings of the Royal Society B: Biological Sciences, 276(1661), 1395-1406. https://doi.org/10.1098/rspb.2008.1480
Gatten, Jr., R. E. (1974). Effects of temperature and activity on aerobic and anaerobic metabolism and heart rate in the turtles Pseudemys scripta and Terrapene ornata. Comparative Biochemistry and Physiology Part A: Physiology, 48(4), 619-648. https://doi.org/10.1016/0300-9629(74)90606-9
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M., & Charnov, E. L. (2001). Effects of size and temperature on metabolic rate. Science, 293(5538), 2248-2251. https://doi.org/10.1126/science.1061967
Gracey, A. Y., Chaney, M. L., Boomhower, J. P., Tyburczy, W. R., Connor, K., & Somero, G. N. (2008). Rhythms of gene expression in a fluctuating intertidal environment. Current Biology, 18(19), 1501-1507. https://doi.org/10.1016/j.cub.2008.08.049
Guillera-Arroita, G., Lahoz-Monfort, J. J., Elith, J., Gordon, A., Kujala, H., Lentini, P. E., McCarthy, M. A., Tingley, R., & Wintle, B. A. (2015). Is my species distribution model fit for purpose? Matching data and models to applications. Global Ecology and Biogeography, 24(3), 276-292. https://doi.org/10.1111/geb.12268
Guppy, M., & Withers, P. (1999). Metabolic depression in animals: Physiological perspectives and biochemical generalizations. Biological Reviews, 74(1), 1-40. https://doi.org/10.1111/j.1469-185X.1999.tb00180.x
Han, G. D., Zhang, S., & Dong, Y. W. (2017). Anaerobic metabolism and thermal tolerance: The importance of opine pathways on survival of a gastropod after cardiac dysfunction. Integrative Zoology, 12(5), 361-370. https://doi.org/10.1111/1749-4877.12229
Han, G. D., Zhang, S., Marshall, D. J., Ke, C. H., & Dong, Y. W. (2013). Metabolic energy sensors (AMPK and SIRT1), protein carbonylation and cardiac failure as biomarkers of thermal stress in an intertidal limpet: Linking energetic allocation with environmental temperature during aerial emersion. Journal of Experimental Biology, 216(17), 3273-3282. https://doi.org/10.1242/jeb.084269
Hand, S. C., & Hardewig, I. (1996). Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annual Review of Physiology, 58, 539-563. https://doi.org/10.1146/annurev.ph.58.030196.002543
Harley, C. D., Randall Hughes, A., Hultgren, K. M., Miner, B. G., Sorte, C. J., Thornber, C. S., Rodriguez, L. F., Tomanek, L., & Williams, S. L. (2006). The impacts of climate change in coastal marine systems. Ecology Letters, 9(2), 228-241. https://doi.org/10.1111/j.1461-0248.2005.00871.x
Helmuth, B., Broitman, B. R., Blanchette, C. A., Gilman, S., Halpin, P., Harley, C. D., O'Donnell, M. J., Hofmann, G. E., Menge, B., & Strickland, D. (2006). Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change. Ecological Monographs, 76(4), 461-479. https://doi.org/10.1890/0012-9615(2006)076[0461:mpotsi]2.0.co;2
Helmuth, B., Harley, C. D., Halpin, P. M., O'Donnell, M., Hofmann, G. E., & Blanchette, C. A. (2002). Climate change and latitudinal patterns of intertidal thermal stress. Science, 298(5595), 1015-1017. https://doi.org/10.1126/science.1076814.
Helmuth, B., Yamane, L., Lalwani, S., Matzelle, A., Tockstein, A., & Gao, N. (2011). Hidden signals of climate change in intertidal ecosystems: What (not) to expect when you are expecting. Journal of Experimental Marine Biology and Ecology, 400(1-2), 191-199. https://doi.org/10.1016/j.jembe.2011.02.004
Hill, J. K., Thomas, C. D., Fox, R., Telfer, M. G., Willis, S. G., Asher, J., & Huntley, B. (2002). Responses of butterflies to twentieth century climate warming: implications for future ranges. Proceedings of the Royal Society of London B: Biological Sciences, 269(1505), 2163-2171. https://doi.org/10.1098/rspb.2002.2134
Hofmann, G. E., & Todgham, A. E. (2010). Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annual Review of Physiology, 72, 127-145. https://doi.org/10.1146/annurev-physiol-021909-135900
Huang, R., Chen, J., & Huang, G. (2007). Characteristics and variations of the East Asian monsoon system and its impacts on climate disasters in China. Advances in Atmospheric Sciences, 24(6), 993-1023. https://doi.org/10.1007/s00376-007-0993-x
Huey, R. B., & Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology & Evolution, 4(5), 131-135. https://doi.org/10.1016/0169-5347(89)90211-5
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
Huey, R. B., & Stevenson, R. (1979). Integrating thermal physiology and ecology of ectotherms: A discussion of approaches. American Zoologist, 19(1), 357-366. https://doi.org/10.1093/icb/19.1.357
Hui, T. Y., Dong, Y. W., Han, G. D., Lau, S. L. Y., Cheng, M. C. F., Meepoka, C., Ganmanee, M., & Williams, G. A. (2020). Timing metabolic depression: Predicting thermal stress in extreme intertidal environments. The American Naturalist, 196(4), 501-511. https://doi.org/10.1086/710339
Hutchins, L. W. (1947). The bases for temperature zonation in geographical distribution. Ecological Monographs, 17(3), 325-335. https://doi.org/10.2307/1948663
IPCC. (2018). Global Warming of 1.5°C. An IPCC. Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. In V. Masson-Delmotte, P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P. R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J. B. R. Matthews, Y. Chen, X. Zhou, M. I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, & T. Waterfield (Eds.). https://www.IPCC.ch/sr15/
Jimenez, A. G., Jayawardene, S., Alves, S., Dallmer, J., & Dowd, W. W. (2015). Micro-scale environmental variation amplifies physiological variation among individual mussels. Proceedings of the Royal Society B: Biological Sciences, 282(1820), 20152273. https://doi.org/10.1098/rspb.2015.2273
Karsenti, E., Acinas, S. G., Bork, P., Bowler, C., De Vargas, C., Raes, J., Sullivan, M., Arendt, D., Benzoni, F., Claverie, J.-M., Follows, M., Gorsky, G., Hingamp, P., Iudicone, D., Jaillon, O., Kandels-Lewis, S., Krzic, U., Not, F., Ogata, H., … Wincker, P. (2011). A holistic approach to marine eco-systems biology. PLoS Biology, 9(10), e1001177. https://doi.org/10.1371/journal.pbio.1001177
Kearney, M., & Porter, W. (2009). Mechanistic niche modelling: Combining physiological and spatial data to predict species’ ranges. Ecology Letters, 12(4), 334-350. https://doi.org/10.1111/j.1461-0248.2008.01277.x
Kearney, M. R., Wintle, B. A., & Porter, W. P. (2010). Correlative and mechanistic models of species distribution provide congruent forecasts under climate change. Conservation Letters, 3(3), 203-213. https://doi.org/10.1111/j.1755-263X.2010.00097.x
Knight, A. T., Cowling, R. M., Rouget, M., Balmford, A., Lombard, A. T., & Campbell, B. M. (2008). Knowing but not doing: Selecting priority conservation areas and the research-implementation gap. Conservation Biology, 22(3), 610-617. https://doi.org/10.1111/j.1523-1739.2008.00914.x
Laeseke, P., Martínez, B., Mansilla, A., & Bischof, K. (2020). Future range dynamics of the red alga Capreolia implexa in native and invaded regions: Contrasting predictions from species distribution models versus physiological knowledge. Biological Invasions, 22(4), 1339-1352. https://doi.org/10.1007/s10530-019-02186-4
Li, L. I., Li, A. O., Song, K., Meng, J., Guo, X., Li, S., Li, C., De Wit, P., Que, H., Wu, F., Wang, W., Qi, H., Xu, F., Cong, R., Huang, B., Li, Y., Wang, T., Tang, X., Liu, S., … Zhang, G. (2018). Divergence and plasticity shape adaptive potential of the Pacific oyster. Nature Ecology & Evolution, 2(11), 1751-1760. https://doi.org/10.1038/s41559-018-0668-2
Liao, M. L., Somero, G. N., & Dong, Y. W. (2019). Comparing mutagenesis and simulations as tools for identifying functionally important sequence changes for protein thermal adaptation. Proceedings of the National Academy of Sciences of the United States of America, 116(2), 679-688. https://doi.org/10.1073/pnas.1817455116
Liao, M. L., Zhang, S., Zhang, G. Y., Chu, Y. M., Somero, G. N., & Dong, Y. W. (2017). Heat-resistant cytosolic malate dehydrogenases (cMDHs) of thermophilic intertidal snails (genus Echinolittorina): Protein underpinnings of tolerance to body temperatures reaching 55°C. Journal of Experimental Biology, 220(11), 2066-2075. https://doi.org/10.1242/jeb.156935
Lima, F. P., & Wethey, D. S. (2009). Robolimpets: Measuring intertidal body temperatures using biomimetic loggers. Limnology and Oceanography: Methods, 7(5), 347-353. https://doi.org/10.4319/lom.2009.7.347
López-Villalta, J. S. (2008). A metabolic view of the diversity-stability relationship. Journal of Theoretical Biology, 252(1), 39-42. https://doi.org/10.1016/j.jtbi.2008.01.015
MacLean, S. A., & Beissinger, S. R. (2017). Species’ traits as predictors of range shifts under contemporary climate change: A review and meta-analysis. Global Change Biology, 23(10), 4094-4105. https://doi.org/10.1111/gcb.13736
Marshall, D. J., Dong, Y. W., McQuaid, C. D., & Williams, G. A. (2011). Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism. Journal of Experimental Biology, 214(21), 3649-3657. https://doi.org/10.1242/jeb.059899
Marshall, D. J., & McQuaid, C. D. (1993). Effects of hypoxia and hyposalinity on the heart beat of the intertidal limpets Patella granvlaris (Prosobranchia) and Siphonaria capensis (Pulmonata). Comparative Biochemistry and Physiology Part A: Physiology, 106(1), 65-68. https://doi.org/10.1016/0300-9629(93)90040-b
Marshall, D. J., & McQuaid, C. D. (2011). Warming reduces metabolic rate in marine snails: Adaptation to fluctuating high temperatures challenges the metabolic theory of ecology. Proceedings of the Royal Society of London B: Biological Sciences, 278(1703), 281-288. https://doi.org/10.1098/rspb.2010.1414
Marshall, D. J., McQuaid, C. D., & Williams, G. A. (2010). Non-climatic thermal adaptation: Implications for species’ responses to climate warming. Biology Letters, 6(5), 669-673. https://doi.org/10.1098/rsbl.2010.0233
Marshall, D. J., Rezende, E. L., Baharuddin, N., Choi, F., & Helmuth, B. (2015). Thermal tolerance and climate warming sensitivity in tropical snails. Ecology and Evolution, 5(24), 5905-5919. https://doi.org/10.1002/ece3.1785
Martínez, B., Arenas, F., Trilla, A., Viejo, R. M., & Carreno, F. (2015). Combining physiological threshold knowledge to species distribution models is key to improving forecasts of the future niche for macroalgae. Global Change Biology, 21(4), 1422-1433. https://doi.org/10.1111/gcb.12655
Martínez, B., Radford, B., Thomsen, M. S., Connell, S. D., Carreño, F., Bradshaw, C. J. A., Fordham, D. A., Russell, B. D., Gurgel, C. F. D., Wernberg, T., & Lahoz-Monfort, J. (2018). Distribution models predict large contractions of habitat-forming seaweeds in response to ocean warming. Diversity and Distributions, 24(10), 1350-1366. https://doi.org/10.1111/ddi.12767
McMahon, R. F., & Russell-Hunter, W. (1977). Temperature relations of aerial and aquatic respiration in six littoral snails in relation to their vertical zonation. The Biological Bulletin, 152(2), 182-198. https://doi.org/10.2307/1540558
Metcalfe, N. B., Van Leeuwen, T. E., & Killen, S. S. (2016). Does individual variation in metabolic phenotype predict fish behaviour and performance? Journal of Fish Biology, 88(1), 298-321. https://doi.org/10.1111/jfb.12699
Miatta, M., Bates, A. E., & Snelgrove, P. V. R. (2021). Incorporating biological traits into conservation strategies. Annual Review of Marine Science, 13, 14.1-14.22. https://doi.org/10.1146/annurev-marine-032320-094121
Mislan, K. A. S., Helmuth, B., & Wethey, D. S. (2014). Geographical variation in climatic sensitivity of intertidal mussel zonation. Global Ecology and Biogeography, 23(7), 744-756. https://doi.org/10.1111/geb.12160
Mislan, K. A. S., & Wethey, D. S. (2015). A biophysical basis for patchy mortality during heat waves. Ecology, 96(4), 902-907. https://doi.org/10.5281/zenodo.13380
Monaco, C. J., McQuaid, C. D., & Marshall, D. J. (2017). Decoupling of behavioural and physiological thermal performance curves in ectothermic animals: A critical adaptive trait. Oecologia, 185(4), 583-593. https://doi.org/10.1007/s00442-017-3974-5
Montalto, V., Helmuth, B., Ruti, P. M., Dell’Aquila, A., Rinaldi, A., & Sarà, G. (2016). A mechanistic approach reveals non linear effects of climate warming on mussels throughout the Mediterranean sea. Climatic Change, 139(2), 293-306. https://doi.org/10.1007/s10584-016-1780-4
Moyen, N. E., Somero, G. N., & Denny, M. W. (2019). Impact of heating rate on cardiac thermal tolerance in the California mussel, Mytilus californianus. Journal of Experimental Biology, 222(17), jeb203166. https://doi.org/10.1242/jeb.203166
Newell, R. C. (1969). Effect of fluctuations in temperature on the metabolism of intertidal invertebrates. American Zoologist, 9(2), 293-307. https://doi.org/10.1093/icb/9.2.293
Orton, J. H. (1920). Sea-temperature, breeding and distribution in marine animals. Journal of the Marine Biological Association of the United Kingdom, 12(2), 339-366. https://doi.org/10.1017/s0025315400000102
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(6), 1738-1750. https://doi.org/10.1111/gcb.12521
Patil, Y. N., Marden, B., Brand, M. D., & Hand, S. C. (2013). Metabolic downregulation and inhibition of carbohydrate catabolism during diapause in embryos of Artemia franciscana. Physiological and Biochemical Zoology, 86(1), 106-118. https://doi.org/10.1086/667808
Percy, J., & Aldrich, F. (1971). Metabolic rate independent of temperature in mollusc tissue. Nature, 231(5302), 393-394. https://doi.org/10.1038/231393a0
Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L., & Sunday, J. M. (2019). Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature, 569(7754), 108-111. https://doi.org/10.1038/s41586-019-1132-4
Pörtner, H. O. (2010). Oxygen- and capacity-limitation of thermal tolerance: A matrix for integrating climate-related stressor effects in marine ecosystems. Journal of Experimental Biology, 213(6), 881-893. https://doi.org/10.1242/jeb.037523
Pörtner, H. O., & Farrell, A. P. (2008). Ecology. Physiology and climate change. Science, 322(5902), 690-692. https://doi.org/10.1126/science.1163156
Rodríguez, L., García, J. J., Carreño, F., Martínez, B., & Beger, M. (2019). Integration of physiological knowledge into hybrid species distribution modelling to improve forecast of distributional shifts of tropical corals. Diversity and Distributions, 25(5), 715-728. https://doi.org/10.1111/ddi.12883
Sadoul, B., Geffroy, B., Lallement, S., & Kearney, M. (2020). Multiple working hypotheses for hyperallometric reproduction in fishes under metabolic theory. Ecological Modelling, 433, 109228. https://doi.org/10.1016/j.ecolmodel.2020.109228
Sanford, E., & Kelly, M. W. (2011). Local adaptation in marine invertebrates. Annual Review of Marine Science, 3(1), 509-535. https://doi.org/10.1146/annurev-marine-120709-142756
Santini, G., Williams, G., & Chelazzi, G. (2000). Assessment of factors affecting heart rate of the limpet Patella vulgata on the natural shore. Marine Biology, 137(2), 291-296. https://doi.org/10.1007/s002270000339
Schleuning, M., Fründ, J., Schweiger, O., Welk, E., Albrecht, J., Albrecht, M., Beil, M., Benadi, G., Blüthgen, N., Bruelheide, H., Böhning-Gaese, K., Dehling, D. M., Dormann, C. F., Exeler, N., Farwig, N., Harpke, A., Hickler, T., Kratochwil, A., Kuhlmann, M., … Hof, C. (2016). Ecological networks are more sensitive to plant than to animal extinction under climate change. Nature Communications, 7, 13965. https://doi.org/10.1038/ncomms13965
Schoolfield, R. M., Sharpe, P. J., & Magnuson, C. E. (1981). Non-linear regression of biological temperature-dependent rate models based on absolute reaction-rate theory. Journal of Theoretical Biology, 88(4), 719-731. https://doi.org/10.1016/0022-5193(81)90246-0
Schulte, P. M. (2015). The effects of temperature on aerobic metabolism: Towards a mechanistic understanding of the responses of ectotherms to a changing environment. Journal of Experimental Biology, 218(12), 1856-1866. https://doi.org/10.1242/jeb.118851
Schulte, P. M., Healy, T. M., & Fangue, N. A. (2011). Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integrative and Comparative Biology, 51(5), 691-702. https://doi.org/10.1093/icb/icr097
Seabra, R., Wethey, D. S., Santos, A. M., & Lima, F. P. (2011). Side matters: Microhabitat influence on intertidal heat stress over a large geographical scale. Journal of Experimental Marine Biology and Ecology, 400(1-2), 200-208. https://doi.org/10.1016/j.jembe.2011.02.010
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
Sharpe, P., & DeMichele, D. (1977). Reaction kinetics of poikilotherm development. Journal of Theoretical Biology, 64(4), 649-667. https://doi.org/10.1016/0022-5193(77)90265-x
Sheppard, C. S., Burns, B. R., & Stanley, M. C. (2014). Predicting plant invasions under climate change: are species distribution models validated by field trials? Global Change Biology, 20(9), 2800-2814. https://doi.org/10.1111/gcb.12531
Sinclair, B. J., Marshall, K. E., Sewell, M. A., Levesque, D. L., Willett, C. S., Slotsbo, S., Dong, Y., Harley, C. D., Marshall, D. J., Helmuth, B. S., & Huey, R. B. (2016). Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecology Letters, 19(11), 1372-1385. https://doi.org/10.1111/ele.12686
Sokolova, I. M., Frederich, M., Bagwe, R., Lannig, G., & Sukhotin, A. A. (2012). Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Marine Environmental Research, 79, 1-15. https://doi.org/10.1016/j.marenvres.2012.04.003
Sokolova, I., & Pörtner, H. (2001). Physiological adaptations to high intertidal life involve improved water conservation abilities and metabolic rate depression in Littorina saxatilis. Marine Ecology Progress Series, 224, 171-186. https://doi.org/10.3354/meps224171
Somero, G. N. (1995). Proteins and temperature. Annual Review of Physiology, 57(1), 43-68. https://doi.org/10.1146/annurev.ph.57.030195.000355
Somero, G. N. (2005). Linking biogeography to physiology: Evolutionary and acclimatory adjustments of thermal limits. Frontiers in Zoology, 2(1), 1. https://doi.org/10.1186/1742-9994-2-1
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(6), 912-920. https://doi.org/10.1242/jeb.037473
Somero, G. N., Lockwood, B. L., & Tomanek, L. (2017). Biochemical adaptation: Response to environmental challenges from life’s origins to the anthropocene. Sinauer Associates.
Stenseng, E., Braby, C. E., & Somero, G. N. (2005). Evolutionary and acclimation-induced variation in the thermal limits of heart function in congeneric marine snails (genus Tegula): Implications for vertical zonation. Biology Bulletin, 208(2), 138-144. https://doi.org/10.2307/3593122
Stillman, J., & Somero, G. N. (1996). Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus Petrolisthes): Correlation of physiology, biochemistry and morphology with vertical distribution. Journal of Experimental Biology, 199(8), 1845-1855. PMID: 9319758.
Storey, K. B., & Storey, J. M. (1990). Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. The Quarterly Review of Biology, 65(2), 145-174. https://doi.org/10.1086/416717
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(1713), 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(15), 5610-5615. https://doi.org/10.1073/pnas.1316145111
Sunday, J., Bennett, J. M., Calosi, P., Clusella-Trullas, S., Gravel, S., Hargreaves, A. L., Leiva, F. P., Verberk, W. C., Olalla-Tárraga, M. Á., & Morales-Castilla, I. (2019). Thermal tolerance patterns across latitude and elevation. Philosophical Transactions of the Royal Society B, 374(1778), 20190036. https://doi.org/10.1098/rstb.2019.0036
Sunday, J. M., Pecl, G. T., Frusher, S., Hobday, A. J., Hill, N., Holbrook, N. J., Edgar, G. J., Stuart-Smith, R., Barrett, N., Wernberg, T., Watson, R. A., Smale, D. A., Fulton, E. A., Slawinski, D., Feng, M., Radford, B. T., Thompson, P. A., & Bates, A. E. (2015). Species traits and climate velocity explain geographic range shifts in an ocean-warming hotspot. Ecology Letters, 18(9), 944-953. https://doi.org/10.1111/ele.12474
Sutherland, W. J., Freckleton, R. P., Godfray, H. C. J., Beissinger, S. R., Benton, T., Cameron, D. D., Carmel, Y., Coomes, D. A., Coulson, T., Emmerson, M. C., Hails, R. S., Hays, G. C., Hodgson, D. J., Hutchings, M. J., Johnson, D., Jones, J. P. G., Keeling, M. J., Kokko, H., Kunin, W. E., … Wiegand, T. (2013). Identification of 100 fundamental ecological questions. Journal of Ecology, 101(1), 58-67. https://doi.org/10.1111/1365-2745.12025
Teal, L. R., Marras, S., Peck, M. A., & Domenici, P. (2018). Physiology-based modelling approaches to characterize fish habitat suitability: Their usefulness and limitations. Estuarine, Coastal and Shelf Science, 201, 56-63. https://doi.org/10.1016/j.ecss.2015.11.014
Thomas, M. K., Kremer, C. T., Klausmeier, C. A., & Litchman, E. (2012). A global pattern of thermal adaptation in marine phytoplankton. Science, 338(6110), 1085-1088. https://doi.org/10.1126/science.1224836
Tomlinson, S., Rummer, J. L., Hultine, K. R., & Cooke, S. J. (2018). Crossing boundaries in conservation physiology. Conservation Physiology, 6(1), coy015. https://doi.org/10.1093/conphys/coy015
van der Meer, J. (2006). Metabolic theories in ecology. Trends in Ecology & Evolution, 21(3), 136-140. https://doi.org/10.1016/j.tree.2005.11.004
Verberk, W. C., Bartolini, F., Marshall, D. J., Pörtner, H. O., Terblanche, J. S., White, C. R., & Giomi, F. (2016). Can respiratory physiology predict thermal niches? Annals of the New York Academy of Sciences, 1365(1), 73-88. https://doi.org/10.1111/nyas.12876.
Vrugt, J. A., Gupta, H. V., Bouten, W., & Sorooshian, S. (2003). A Shuffled Complex Evolution Metropolis algorithm for optimization and uncertainty assessment of hydrologic model parameters. Water Resources Research, 39(8), 1201. https://doi.org/10.1029/2002wr001642
Wethey, D. S., Woodin, S. A., Hilbish, T. J., Jones, S. J., Lima, F. P., & Brannock, P. M. (2011). Response of intertidal populations to climate: Effects of extreme events versus long term change. Journal of Experimental Marine Biology and Ecology, 400(1-2), 132-144. https://doi.org/10.1016/j.jembe.2011.02.008
Wiens, J. A., Stralberg, D., Jongsomjit, D., Howell, C. A., & Snyder, M. A. (2009). Niches, models, and climate change: assessing the assumptions and uncertainties. Proceedings of the National Academy of Sciences of the United States of America, 106(Suppl. 2), 19729-19736. https://doi.org/10.1073/pnas.0901639106
Wolcott, T. G. (1973). Physiological ecology and intertidal zonation in limpets (Acmaea): A critical look at “limiting factors”. Biology Bulletin, 145(2), 389-422. https://doi.org/10.2307/1540048
Woodin, S. A., Hilbish, T. J., Helmuth, B., Jones, S. J., & Wethey, D. S. (2013). Climate change, species distribution models, and physiological performance metrics: Predicting when biogeographic models are likely to fail. Ecology and Evolution, 3(10), 3334-3346. https://doi.org/10.1002/ece3.680
Woods, H. A., Kingsolver, J. G., Fey, S. B., & Vasseur, D. A. (2018). Uncertainty in geographical estimates of performance and fitness. Methods in Ecology and Evolution, 9(9), 1996-2008. https://doi.org/10.1111/2041-210X.13035