Abstract
Amphibian life history traits are affected by temperature and precipitation. Yet, connecting these relationships to population growth, especially for multiple populations within a species, is lacking and precludes our understanding of amphibian population dynamics and distributions. Therefore, we constructed integral projection models for five populations along an elevational gradient to determine how climate and season affect population growth of a terrestrial salamander Plethodon montanus and the importance of demographic vital rates to population growth under varying climate scenarios. We found that population growth was typically higher at the highest elevation compared to the lower elevations, whereas varying inactive season conditions, represented by the late fall, winter and early spring, produced a greater variation in population growth than varying active season conditions (late spring, summer, and early fall). Furthermore, survival and growth were consistently more important, as measured by elasticity, compared to fecundity, and large females had the greatest elasticity compared to all other body sizes. Our results suggest that changing inactive season conditions, especially those that would affect the survival of large individuals, may have the greatest impact on population growth. We recommend future experimental studies focus on the inactive season to better elucidate the mechanisms by which these conditions can affect survival.
Similar content being viewed by others
References
Amburgey SM, Miller DAW, Grant EHC, Rittenhouse AG, Benard MF, Richardson JL, Urban MC, Hughson W, Brand AB, Davis CJ, Hardin CR, Paton PWC, Raithel CJ, Relyea RA, Scott F, Skelly DK, Skidds DE, Smith CK, Werner EE (2018) Range position and climate sensitivity: The structure of among-population demographic responses to climatic variation. Glob Change Biol 24:439–454
Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994
Benard MF (2015) Warmer winters reduce frog fecundity and shift breeding phenology, which consequently alters larval development and metamorphic timing. Glob Change Biol 21:1058–1065
Bendik NF (2017) Demographics, reproduction, growth, and abundance of Jollyville Plateau salamanders (Eurycea tonkawae). Ecol Evol 7:5002–5015
Bendik NF, Gluesenkamp AG (2013) Body length shrinkage in an endangered amphibian is associated with drought. J Zool 290:35–41
Benton TG, Grant A (1999) Elasticity analysis as an important tool in evolutionary and population ecology. Trends Ecol Evol 14:467–471
Benton TG, Grant A, Clutton-Brock TH (1995) Does environmental stochasticity matter? Analysis of red deer life-histories on Rum. Evol Ecol 9:559–574
Berven KA, Gill DE (1983) Interpreting geographic variation in life-history traits. Am Zool 23:85–97
Brown PJ, DeGaetano AT (2011) A paradox of cooling winter soil surface temperatures in a warming northeastern United States. Agric For Meteorol 151:947–956
Buckley LB, Urban MC, Angilletta MJ, Crozier LG, Rissler LJ, Sears MW (2010) Can mechanism inform species’ distribution models? Ecol Lett 13:1041–1054
Caruso NM, Rissler LJ (2019a) Demographic consequences of climate variation along an elevational gradient for a montane terrestrial salamander. Popul Ecol 61:171–182
Caruso NM, Rissler LJ (2019b) Museum specimens reveal life history characteristics in Plethodon montanus. Copeia 107:622–631
Caruso NM, Jacobs JF, Rissler LJ (2019) An experimental approach to understanding elevation limits in the northern gray-cheeked salamander, Plethodon montanus. Herpetol Conserv Biol 14:297–307
Caruso NM, Sears MW, Adams DC, Lips KR (2014) Widespread rapid reductions in body size of adult salamanders in response to climate change. Glob Change Biol 20:1751–1759
Castanet J, Smirina EM (1990) Introduction to the skeletochronological method in amphibians and reptiles. Annales des Sciences Naturelles Zoologie et Biologie Animale 13:191–196
Caswell H (1982) Life history theory and the equilibrium status of populations. Am Nat 120:317–339
Caswell H (2000) Prospective and retrospective perturbation analyses: their roles in conservation biology. Ecology 81:619–627
Caswell H (2001) Matrix population models: construction, analysis, and interpretation, 2nd edn. Sinauer Associates, Sunderland
Cayuela H, Griffiths RA, Zakaria N, Arntzen JW, Priol P, Léna J-P, Besnard A, Joly P (2020) Drivers of amphibian population dynamics and asynchrony at local and regional scales. J Anim Ecol 89:1350–1364
Conde DA, Staerk J, Colchero F, da Silva R, Schöley J, Baden HM, Jouvet L, Fa JE, Syed H, Jongejans E, Meiri S, Giallard J-M, Chamberlain S, Wilcken J, Jones OR, Dahlgren JP, Steiner UK, Bland LM, Gomez-Mestre I, Lebreton J-D, Vargas JG, Flesness N, Canudas-Romo V, Salguero-Gómez R, Byers O, Berg TB, Scheuerlein A, Devillard S, Schigel DS, Ryder OA, Possingham HP, Baudisch A, Vaupel JW (2019) Data gaps and opportunities for comparative and conservation biology. Proc Natl Acad Sci 116:9658–9664
Coulson T, Gaillard J-M, Festa-Bianchet M (2005) Decomposing the variation in population growth into contributions from multiple demographic rates. J Anim Ecol 74:789–801
Cunningham HR, Rissler LJ, Apodaca JJ (2009) Competition at the range boundary in the slimy salamander: using reciprocal transplants for studies on the role of biotic interactions in spatial distributions. J Anim Ecol 78:52–62
Cunningham HR, Rissler LJ, Buckley LB, Urban MC (2016) Abiotic and biotic constraints across reptile and amphibian ranges. Ecography 39:1–8
Decker KLM, Wang D, Waite C, Scherbatskoy T (2003) Snow removal and ambient air temperature effects on forest soil temperatures in Northern Vermont. Soil Sci Soc Am J 67:1234–1243
Earl JE (2019) Evaluating the assumptions of population projection models used for conservation. Biol Conserv 237:145–154
Easterling MR, Ellner SP, Dixon PM (2000) Size-specific sensitivity: applying a new structured population model. Ecology 81:694–708
Ellner SP, Rees M (2006) Integral projection models for species with complex demography. Am Nat 167:410–428
Fabens AJ (1965) Properties and fitting of von Bertalanffy growth curve. Growth 29:265–289
Farallo VR, Miles DB (2016) The importance of microhabitat: a comparison of two microendemic species of Plethodon to the widespread P. cinereus. Copeia 104:67–77
Ficetola GF, Maiorano L (2016) Contrasting effects of temperature and precipitation change on amphibian phenology, abundance and performance. Oecologia 181:683–693
Gaillard J-M, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63
Gifford ME, Kozak KH (2012) Islands in the sky or squeezed at the top? Ecological causes of elevational range limits in montane salamanders. Ecography 35:193–203
Grant EHC, Brand AB, De Wekker SFJ, Lee TR, Wofford JEB (2018) Evidence that climate sets the lower elevation range limit in a high-elevation endemic salamander. Ecol Evol 8:7553–7562
Grant EHC, Miller DAW, Schmidt BR, Adams MJ, Amburgey SM, Chambert T, Cruickshank SS, Fisher RN, Green DM, Hossack BR, Johnson PTJ, Joseph MB, Rittenhouse TAG, Ryan ME, Waddle JH, Walls SC, Bailey LL, Fellers GM, Gorman TA, Ray AM, Pilliod DS, Price SJ, Saenz D, Sadinski W, Muths E (2016) Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines. Sci Rep 6:25625
Heppel SS, Caswell H, Crowder LB (2000) Life histories and elasticity patterns: perturbation analysis for species with minimal demographic data. Ecology 81:654–665
Henry HAL (2008) Climate change and soil freezing dynamics: historical trends and projected changes. Clim Change 87:421–434
Hijmans RJ, Cameron S, Parra J (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Hoffman M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM, Butchart SH et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509
Homyack JA, Haas CA (2009) Long-term effects of experimental forest harvesting on abundance and reproductive demography of terrestrial salamanders. Biol Conserv 142:110–121
Knapp SM, Haas CA, Harpole DN, Kirkpatrick RL (2004) Initial effects of clearcutting and alternative silvicultural practices on terrestrial salamander abundance. Conserv Biol 17:752–762
Leclair MH, Levsseur M, Leclair R Jr (2008) Acitivity and reproductive cycles in northern population of the red-backed salamander Plethodon cinereus. J Herpetol 42:31–38
Liebgold EB, Brodie ED III, Cabe PR (2011) Female philopatry and male-biased dispersal in a direct-developing salamander, Plethodon cinereus. Mol Ecol 20:249–257
Lindström J, Reeve R, Salvidio S (2010) Bayesian salamanders: analyzing the demography of an underground population of the European plethodontid Speleomantes strinatii with state-space modelling. BMC Ecol 10:4
Lyons MP, Shepard DB, Kozak KH (2016) Determinants of range limits in montane woodland salamanders (genus Plethodon). Copeia 104:101–110
Milanovich JR, Trauth SE, Saugey DA, Jordan RR (2006) Fecundity, reproductive ecology, and influence of precipitation on clutch size in the western slimy salamander (Plethodon Albagula). Herpetologica 62:292–301
Milanovich JR, Peterman WE, Nibbelink NP, Maerz JC (2010) Projected loss of a salamander diversity hotspot as a consequence of projected global climate change. PLoS ONE 5:e12189. https://doi.org/10.1371/journal.pone.0012189
Miller DAW, Grant EHC, Muths E, Amburgey SM, Adams MJ, Joseph MB, Waddle JH, Johnson PTJ, Ryan ME, Schmidt BR, Calhoun DL, Davis CL, Fisher RN, Green DM, Hossack BR, Rittenhouse TAG, Walls SC, Bailey LL, Cruickshank SS, Fellers GM, Gorman TA, Haas CA, Hughson W, Pilliod DS, Price SJ, Ray AM, Sadinski W, Saenz D, Barichivich WJ, Brand A, Brehme CS, Dagit R, Delaney KS, Glorioso BM, Kats LB, Kleeman PM, Pearl CA, Rochester CJ, Riley SPD, Roth M, Sigafus BH (2018) Quantifying climate sensitivity and climate driven change in North American amphibian communities. Nat Commun 9:3926
Mills LS, Doak DF, Wisdom MJ (1999) Reliability of conservation actions based on elasticity analysis of matrix models. Conserv Biol 13:815–829
Mitchell JC, Pague CA (2014) Filling gaps in life-history data: clutch sizes for 21 species of North American anurans. Herpetol Conserv Biol 9:495–501
Morrison C, Hero J-M (2003) Geographic variation in life-history characteristics of amphibians: a review. J Ecol 72:270–279
Muñoz DJ, Hesed KM, Grant EHC, Miller DAW (2016) Evaluating within-population variability in behavior and demography for the adaptive potential of a dispersal-limited species to climate change. Ecol Evol 6:8740–8755
Muths E, Chambert T, Schmidt BR, Miller DAW, Hossack BR, Joly P, Grolet O, Green DM, Pilliod DS, Cheylan M, Fisher RN, McCaffery RM, Adams MJ, Palen WJ, Arntzen JW, Garwood J, Fellers G, Thirion J-M, Besnard A, Grant EHC (2017) Heterogeneous responses of temperate-zone amphibian populations to climate change complicates conservation planning. Sci Rep 7:17102
Otto CRV, Roloff GJ, Thames RE (2014) Comparing population patterns to processes: abundance and survival of a forest salamander following habitat degredation. PLoS ONE 9:e93859
Peterman WE, Semlitsch RD (2013) Fine-scale habitat associations of a terrestrial salamander: the role of environmental gradients and implications for population dynamics. PLoS ONE 8:e62184. https://doi.org/10.1371/journal.pone.0062184
Peterman WE, Crawford JA, Hocking DJ (2016) Effects of elevation on plethodontid salamander body size. Copeia 104:202–208
Pfister CA (1998) Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. Proc Natl Acad Sci 95:213–218
Plard F, Turek D, Grübler MU, Schaub M (2019) IPM2: toward better understanding and forecasting of population dynamics. Ecol Monogr 89:e01364
Pough FH, Smith EM, Rhodes DH, Collazo A (1987) The abundance of salamanders in forest stands with different histories of disturbance. For Ecol Manag 20:1–9
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 4 Apr 2018
Reading CJ (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151:125–131
Ribeiro do Valle D, Staudhammer CL, Cropper WP Jr (2007) Simulating nontimber forest product management in tropical mixed forests. J For 105:301–306
Riddell EA, Odom JP, Damm JD, Sears MW (2018) Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity. Sci Adv 4:eaar5471
Rittenhouse TAG, Harper EB, Rehard LR, Semlitsch RD (2008) The role of microhabitats in the desiccation and survival of anurans in recently harvested oak-hickory forest. Copeia 2008:807–814
Sæther B-E, Bakke O (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81:642–653
Schaub M, Abadi F (2011) Integrated population models: a novel analysis framework for deeper insights into population dynamics. J Ornithol 152:227–237
Schaub M, Royle JA (2014) Estimating true instead of apparent survival using spatial Cormack–Jolly–Seber models. Methods Ecol Evol 4:1316–1326
Schmidt BR, Feldmann R, Schaub M (2005) Demographic processes underlying population growth and decline in Salamandra salamandra. Conserv Biol 19:1149–1156
Stearns SC (1977) The evolution of life history traits. Annu Rev Ecol Evol Syst 8:145–172
Sutton WB, Barrett K, Moody AT, Loftin CS, deMaynadier PG, Nanjappa P (2015) Predicted changes in climatic niche and climate refugia of conservation priority salamander species in the northeastern United States. Forests 6:1–26
Tavecchia G, Tenan S, Pradel R, Igual J-M, Genovart M, Oro D (2016) Climate-driven vital rates do not always mean climate-driven population. Glob Change Biol 22:3960–3966
Thornton PE, Running SW, White MA (1997) Generating surfaces of daily meteorological variables over large regions of complex terrain. J Hydrol 190:214–251
Tilley SG (1980) Life histories and comparative demography of two salamander populations. Copeia 1980:806–821
Urban MC, Bocedi G, Hendry AP, Mihoub J-B, Pe’er G, Singer A, Bridle JR, Crozier LG, De Meester L, Godsoe W, Gonzalez A, Hellmann JJ, Holt RD, Huth A, Johst K, Krug CB, Leadley PW, Palmer SCF, Pantel JH, Schmitz A, Zollner PA, Travis JMJ (2016) Improving the forecast for biodiversity under climate change. Science 353:8466
Van Allen BG, Dunham AE, Asquith CM, Rudolf VHW (2012) Life history predicts risk of species decline in a stochastic world. Proc R Soc B Biol Sci 279:2691–2697
Von Bertalanffy L (1938) A quantitative theory of organic growth (inquires on growth laws. II). Hum Biol 10:181–213
Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago
Werner P, Lötters SBR, Engler JO, Rödder D (2013) The role of climate for the range limits of parapatric European land salamanders. Ecography 36:1127–1137
Wilkins RN, Peterson NP (2000) Factors related to amphibian occurrence and abundance in headwater streams draining second-growth Douglas-fir forests in southwestern Washington. For Ecol Manag 139:79–91
Xia J, Chen J, Piao S, Ciais P, Luo Y, Wan S (2014) Terrestrial carbon cycle affected by non-uniform climate warming. Nat Geosci 7:173–180
Acknowledgements
The authors would like to thank two anonymous reviewers who improved this manuscript.
Funding
NMC received grants through the Graduate Research Fellowship at the University of Alabama, E.O. Wilson Biodiversity Fellowship, the Smithsonian Institution Graduate Research Fellowship, and the Herpetologists’ League E.E. Williams Research Grant. Funding was provided by National Museum of Natural History.
Author information
Authors and Affiliations
Contributions
NMC, CLS, and LJR conceived the idea, NMC developed the models and analyzed the data, and NMC, CLS, and LJR wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by John Loehr.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Caruso, N.M., Staudhammer, C.L. & Rissler, L.J. A demographic approach to understanding the effects of climate on population growth. Oecologia 193, 889–901 (2020). https://doi.org/10.1007/s00442-020-04731-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04731-8