Predicted alteration of surface activity as a consequence of climate change.
Appalachian
activity
climate change
ectotherm
global circulation model
hierarchical model
multivariate adaptive constructed analogs
plethodontid salamander
Journal
Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
09
01
2020
revised:
29
05
2020
accepted:
18
06
2020
pubmed:
3
8
2020
medline:
16
3
2021
entrez:
3
8
2020
Statut:
ppublish
Résumé
Wildlife are faced with numerous threats to survival, none more pressing than that of climate change. Understanding how species will respond behaviorally, physiologically, and demographically to a changing climate is a cornerstone of many contemporary ecological studies, especially for organisms, such as amphibians, whose persistence is closely tied to abiotic conditions. Activity is a useful parameter for understanding the effects of climate change because activity is directly linked to fitness as it dictates foraging times, energy budgets, and mating opportunities. However, activity can be challenging to measure directly, especially for secretive organisms like plethodontid salamanders, which only become surface active when conditions are cool and moist because of their anatomical and physiological restrictions. We estimated abiotic predictors of surface activity for the seven species of the Plethodon jordani complex. Five independent data sets collected from 2004 to 2017 were used to determine the parameters driving salamander surface activity in the present day, which were then used to predict potential activity changes over the next 80 yrs. Average active seasonal temperature and vapor pressure deficit were the strongest predictors of salamander surface activity and, without physiological or behavioral modifications, salamanders were predicted to exhibit a higher probability of surface activity during peak active season under future climate conditions. Temperatures during the active season likely do not exceed salamander thermal maxima to cause activity suppression and, until physiological limits are reached, future conditions may continue to increase activity. Our model is the first comprehensive field-based study to assess current and future surface activity probability. Our study provides insights into how a key behavior driving fitness may be affected by climate change.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e03154Subventions
Organisme : Bruce Family Scholarship in Herpetology Grant-in-Aid from Highlands Biological Station
Organisme : Herpetologist's League EE Williams Research Grant
Organisme : University of Missouri Life Science Fellowship
Organisme : EPA STAR Fellowship
Organisme : Charles W. Ash Scholarship from Highlands Biological Station
Organisme : GAANN Fellowship from the U.S. Department of Education
Organisme : Bruce Family Scholarship in Herpetology from Highlands Biological Station
Organisme : National Geographic Society Waitt Grant Program
ID : W203-11
Organisme : National Science Foundation Long Term Ecological Research Program to the Coweeta LTER Program at the University of Georgia
ID : DEB-0823293
Organisme : National Science Foundation Long Term Ecological Research Program to the Coweeta LTER Program at the University of Georgia
ID : DEB-1637522
Informations de copyright
© 2020 by the Ecological Society of America.
Références
Abatzoglou, J. T., and T. J. Brown. 2012. A comparison of statistical downscaling methods suited for wildfire applications. International Journal of Climatology 32:772-780.
Adler, K. 1969. Extraoptic phase shifting of circadian locomotor rhythm in salamanders. Science 164:1290-1292.
Albrecht, U., and G. Eichele. 2003. The mammalian circadian clock. Current Opinion in Genetics and Development 13:271-277.
Alford, R. A., and S. J. Richards. 1999. Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30:133-165.
Bailey, L. L., T. R. Simons, and K. H. Pollock. 2004. Estimating detection probability parameters for plethodon salamanders using the robust capture-recapture design. Journal of Wildlife Management 68:1-13.
Best, M. L. M., and H. H. Welsh. 2014. The trophic role of a forest salamander: impacts on invertebrates, leaf litter retention, and the humification process. Ecosphere 5:1-19.
Blaustein, A. R., S. C. Walls, B. A. Bancroft, J. J. Lawler, C. L. Searle, and S. S. Gervasi. 2010. Direct and indirect effects of climate change on amphibian populations. Diversity 2:281-313.
Buckley, L. B. 2008. Linking traits to energetics and population dynamics to predict lizard ranges in changing environments. American Naturalist 171:E1-E19.
Buckley, L. B., A. H. Hurlbert, and W. Jetz. 2012. Broad-scale ecological implications of ectothermy and endothermy in changing environments. Global Ecology and Biogeography 21:873-885.
Buckley, L. B., C. R. Nufio, E. M. Kirk, and J. G. Kingsolver. 2015. Elevational differences in developmental plasticity determine phenological responses of grasshoppers to recent climate warming. Proceedings of the Royal Society B 282:20150441.
Bürkner, P. 2017. brms: An R package for Bayesian multilevel models using Stan. Journal of Statistical Software 80:1-28.
Caruso, N., and L. J. Rissler. 2018. Demographic consequences of climate variation along an elevational gradient for a montane terrestrial salamander. Population Ecology 1-12.
Caruso, N. M., M. W. Sears, D. C. Adams, and K. R. Lips. 2014. Widespread rapid reductions in body size of adult salamanders in response to climate change. Global Change Biology 20:1751-1759.
Chandler, R. B., and D. I. King. 2011. Habitat quality and habitat selection of golden-winged warblers in Costa Rica: an application of hierarchical models for open populations. Journal of Applied Ecology 48:1038-1047.
Clarke, L., J. Edmonds, H. Jacoby, H. Pitcher, J. Reily, and R. Richels. 2007. Scenarios of greenhouse gas emissions and atmospheric concentrations. In Sub-report 2.1a of synthesis and assessment product 2.1. Climate Change Science Program and the Subcommittee on Global Change Research, Washington D.C., USA.
Clay, T. A., and M. E. Gifford. 2017. Population level differences in thermal sensitivity of energy assimilation in terrestrial salamanders. Journal of Thermal Biology 64:1-6.
Clay, T. A., and M. E. Gifford. 2018. Thermal constraints of energy assimilation on geographical ranges among lungless salamanders of North America. Journal of Biogeography 45:1664-1674.
Collins, J. P., and A. Storfer. 2003. Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89-98.
Connette, G. M., J. A. Crawford, and W. E. Peterman. 2015. Climate change and shrinking salamanders: alternative mechanisms for changes in plethodontid salamander body size. Global Change Biology 21:2834-2843.
Connette, G., and R. D. Semlitsch. 2013. Life history as a predictor of salamander recovery rate from timber harvest in southern Appalachian forests, U.S.A. Conservation Biology 27:1399-1409.
Davic, R. D., and H. H. Welsh. 2004. On the ecological roles of salamanders. Annual Review of Ecology, Evolution, and Systematics 35:405-434.
Dodd, C. K., and R. M. Dorazio. 2004. Using counts to simultaneously estimate abundance and detection probabilities in a salamander community. Herpetologica 60:468-478.
Farallo, V., M. M. Munoz, J. C. Uyeda, and D. B. Miles. 2020. Scaling between macro- to microscale climatic data reveals strong phylogenetic inertia in niche evolution in plethodontid salamanders. Evolution 74:979-991.
Feder, M. 1983. Integrating the ecology and physiology of plethodontid salamanders. Herpetologica 39:291-310.
Feder, M. E., and P. L. Londos. 1984. Hydric constraints upon foraging in a terrestrial salamander, Desmognathus ochrophaeus. Oecologia 64:413-418.
Ficke, A. D., C. A. Myrick, and L. J. Hansen. 2007. Potential impacts of global climate change on freshwater fisheries. Reviews in Fish Biology and Fisheries 17:581-613.
Fielding, C. A., J. B. Whittaker, J. E. L. Butterfield, and J. C. Coulson. 1999. Predicting responses to climate change: the effect of altitude and latitude on the phenology of the Spittlebug Neophilaenus lineatus. Functional Ecology 13:65-73.
Fontaine, S. S., A. J. Novarro, and K. D. Kohl. 2018. Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian. Journal of Experimental Biology 221.
Gade, M. R., and W. E. Peterman. 2019. Multiple environmental gradients influence the distribution and abundance of a key forest-health indicator species in the Southern Appalachian Mountains, USA. Landscape Ecology 34:569-582.
Gifford, M. E., and K. H. Kozak. 2012. Islands in the sky or squeezed at the top? Ecological causes of elevational range limits in montane salamanders. Ecography 35:193-203.
Grant, E. H. C., et al. 2016. Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines. Scientific Reports 6:25625.
Gwinner, E. 1996. Circadian and circannual programmes in avian migration. Journal of Experimental Biology 199:39-48.
Hervant, F., J. Mathieu, and J. P. Durand. 2000. Metabolism and circadian rhythms of the European blind cave salamander Proteus anguinus and a facultative cave dweller, the Pyrenean newt (Euproctus asper). Canadian Journal of Zoology 78:1427-1432.
Highton, R., and R. B. Peabody. 2000. Geographic protein variation and speciation in salamanders of the Plethodon jordani and Plethodon glutinosus complexes in the southern Appalachian mountains with the description of four new species. Pages 31-93 in The biology of plethodontid salamanders, New York, NY: . Springer US.
Hocking, D., and K. Babbitt. 2014. Amphibian contributions to ecosystem services. Herpetological Conservation and Biology 9:1-17.
Holt, R. E., and C. Jørgensen. 2015. Climate change in fish: effects of respiratory constraints on optimal life history and behaviour. Biology Letters 11:20141032.
Homyack, J. A., C. A. Haas, and W. A. Hopkins. 2010. Influence of temperature and body mass on standard metabolic rate of eastern red-backed salamanders (Plethodon cinereus). Journal of Thermal Biology 35:143-146.
Houlahan, J. E., C. S. Fidlay, B. R. Schmidt, A. H. Meyer, and S. L. Kuzmin. 2000. Quantitative evidence for global amphibian population declines. Nature 404:752-755.
Huey, R. B., C. A. Deutsch, J. J. Tewksbury, L. J. Vitt, P. E. Hertz, H. J. Á. Pérez, and T. Garland. 2009. Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society B 276:1939-1948.
Huey, R. B., and J. G. Kingsolver. 2019. Climate warming, resource availability, and the metabolic meltdown of ectotherms. American Naturalist 194:E140-E150.
Hufkens, K., D. Basler, T. Milliman, E. K. Melaas, and A. D. Richardson. 2018. An integrated phenology modelling framework in R. Methods in Ecology and Evolution 9:1276-1285.
IPCC. 2014. Climate change 2014: synthesis report. In Contribution of Working Groups I,II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R.K. Pachauri and L.A. Meyer (eds.)]. IPCC, Geneva, Switzerland.
Jaeger, R. G. 1980. Microhabitats of a terrestrial forest salamander. Copeia 2:265-268.
Johnson, M. 2019. climateR. R package version 0.0.3. https://github.com/mikejohnson51/climateR
Kearney, M., R. Shine, and W. P. Porter. 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.
Kellner, K. 2017. jagsUI: a wrapper around ‘rjags’ to streamline ‘JAGS’. https://cran.r-project.org/web/packages/jagsUI/index.html
Kéry, M., J. A. Royle, and H. Schmid. 2005. Modeling avian abundance from replicated counts using binomial mixture models. Ecological Applications 15:1450-1461.
Kery, M., and M. Schaub. 2012. Bayesian population analysis using WinBUGS. Academic Press, Cambridge, Massachusetts, USA.
Knutti, R., et al. 2008. A review of uncertainties in global temperature projections over the twenty-first century. Journal of Climate 21:2651-2663.
Kozak, K. H., and J. J. Wiens. 2010. Niche conservatism drives elevational diversity patterns in Appalachian salamanders. American Naturalist 176:40-54.
Li, Y., J. M. Cohen, and J. R. Rohr. 2013. Review and synthesis of the effects of climate change on amphibians. Integrative Zoology 8:145-161.
Maerz, J. C., N. L. Panebianco, and D. M. Madison. 2001. Effects of predator chemical cues and behavioral biorhythms on foraging activity of terrestrial salamanders. Journal of Chemical Ecology 27:1333-1344.
McCormack, J., B. Bowen, and T. Smith. 2008. Sky Islands. Pages 839-843 in R. Gillespie and D. Clague, editors. Encyclopedia of islands. University of California Press, Berkeley, California, USA.
McEntire, K. D., and J. C. Maerz. 2019. Integrating ecophysiological and agent-based models to simulate how behavior moderates salamander sensitivity to climate. Frontiers in Ecology and Evolution 7:1-10.
Milanovich, J. R., W. E. Peterman, N. P. Nibbelink, and J. C. Maerz. 2010. Projected loss of a salamander diversity hotspot as a consequence of projected global climate change. PLoS ONE 5. https://doi.org/10.1371/journal.pone.0012189.
Muñoz, D. J., K. M. Hesed, E. H. C. Grant, and D. A. W. Miller. 2016. Evaluating within-population variability in behavior and fitness for the climate adaptive potential of a dispersal-limited species, Plethodon cinereus. Ecology and Evolution 1-16.
Northrop, P. J., and R. E. Chandler. 2014. Quantifying sources of uncertainty in projections of future climate. Journal of Climate 27:8793-8808.
Novarro, A. J., C. R. Gabor, C. B. Goff, T. D. Mezebish, L. M. Thompson, and K. L. Grayson. 2018. Physiological responses to elevated temperature across the geographic range of a terrestrial salamander. Journal of Experimental Biology 221.
O'Donnell, K. M., and R. D. Semlitsch. 2015. Advancing terrestrial salamander population ecology: the central role of imperfect detection. Journal of Herpetology 49:533-540.
Ohlberger, J. 2013. Climate warming and ectotherm body size-from individual physiology to community ecology. Functional Ecology 27:991-1001.
Peterman, W. E., and M. Gade. 2017. The importance of assessing parameter sensitivity when using biophysical models: a case study using plethodontid salamanders. Population Ecology 59:275-286.
Peterman, W. E., and R. D. Semlitsch. 2013. Fine-scale habitat associations of a terrestrial salamander: the role of environmental gradients and implications for population dynamics. PLoS ONE 8. https://doi.org/10.1371/journal.pone.0062184
Petranka, J. 1998. Salamanders of the United States and Canada. Smithsonian Institution Press, Washington D.C., USA.
Plummer, M. 2003. JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. In 3rd International Workshop on Distributed Statistical Computing (DSC2003), 124 p. Vienna, Austria:
Pollock, K. 1982. A capture-recapture design robust to unequal probability of capture. Journal of Wildlife Management 46:752-757.
R Development Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.r-project.org.
Reading, C. J. 2007. Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151:125-131.
Reppert, S. M., and D. R. Weaver. 2002. Coordination of circadian timing in mammals. Nature 418:935-941.
Riahi, K., A. Grübler, and N. Nakicenovic. 2007. Scenarios of long-term socio-economic and environmental development under climate stabilization. Technological Forecasting and Social Change 74:887-935.
Riddell, E. A., J. P. Odom, J. D. Damm, and M. W. Sears. 2018. Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity. Science Advances 4:5471-5482.
Riddell, E., and M. W. Sears. 2015. Geographic variation of resistance to water loss within two species of lungless salamanders: implications for activity. Ecosphere 6:1-16.
Rome, L. C., E. Stevens, and H. John-Alder. 1992. The influence of temperature and thermal acclimation on physiological function. Page 205. In M. Feder, and W. Burggren, editors. Environmental physiology of the amphibians. University of Chicago Press, Chicago, Illinois, USA.
Royle, J. A. 2004. N-mixture models for estimating population size from spatially replicated counts. Biometrics 60:108-115.
Royle, J. A., M. Kéry, R. Gautier, and H. Schmid. 2007. Hierarchical spatial models of abundance and occurrence from imperfect survey data. Ecological Monographs 77:465-481.
Rupp, D. E., J. T. Abatzoglou, K. C. Hegewisch, and P. W. Mote. 2013. Evaluation of CMIP5 20th century climate simulations for the Pacific Northwest USA. Journal of Geophysical Research Atmospheres 118:10884-10906.
Schuster, C., N. Estrella, and A. Menzel. 2014. Shifting and extension of phenological periods with increasing temperature along elevational transects in southern Bavaria. Plant Biology 16:332-344.
Seebacher, F., C. R. White, and C. E. Franklin. 2015. Physiological plasticity increases resilience of ectothermic animals to climate change. Nature Climate Change 5:61-66.
Sheridan, J. A., and D. Bickford. 2011. Shrinking body size as an ecological response to climate change. Nature Climate Change 1:401-406.
Spotila, J. R. 1972. Role of temperature and water in the ecology of lungless salamanders. Ecological Monographs 42:95-125.
Staub, N. L. 2016. The age of plethodontid salamanders: a short review on longevity. Copeia 104:118-123.
Studds, C. E., et al. 2017. Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites. Nature Communications 8:1-7.
Sutton, W. B., K. Barrett, A. T. Moody, C. S. Loftin, P. G. deMaynadier, and P. Nanjappa. 2015. Predicted changes in climatic niche and climate refugia of conservation priority salamander species in the northeastern United States. Forests 6:1-26.
Tingley, M. W., M. S. Koo, C. Moritz, A. C. Rush, and S. R. Beissinger. 2012. The push and pull of climate change causes heterogeneous shifts in avian elevational ranges. Global Change Biology 18:3279-3290.
Weisrock, D. W., and A. Larson. 2006. Testing hypotheses of speciation in the Plethodon jordani species complex with allozymes and mitochondrial DNA sequences. Biological Journal of the Linnean Society 89:25-51.
Wiens, J. J., et al. 2010. Niche conservatism as an emerging principle in ecology and conservation biology. Ecology Letters 13:1310-1324.
Wiens, J. J., A. Camacho, A. Goldberg, T. Jezkova, M. E. Kaplan, S. M. Lambert, E. C. Miller, J. W. Streicher, and R. L. Walls. 2019. Climate change, extinction, and Sky Island biogeography in a montane lizard. Molecular Ecology 28:2610-2624.