Contrasting effects of temperature and precipitation change on amphibian phenology, abundance and performance

Abstract

Climate change is determining a generalized phenological advancement, and amphibians are among the taxa showing the strongest phenological responsiveness to warming temperatures. Amphibians are strongly influenced by climate change, but we do not have a clear picture of how climate influences important parameters of amphibian populations, such as abundance, survival, breeding success and morphology. Furthermore, the relative impact of temperature and precipitation change remains underappreciated. We used Bayesian meta-analysis and meta-regression to quantify the impact of temperature and precipitation change on amphibian phenology, abundance, individual features and performance. We obtained effect sizes from studies performed in five continents. Temperature increase was the major driver of phenological advancement, while the impact of precipitation on phenology was weak. Conversely, population dynamics was mostly determined by precipitation: negative trends were associated with drying regimes. The impact of precipitation on abundance was particularly strong in tropical areas, while the importance of temperature was feeble. Both temperature and precipitation influenced parameters representing breeding performance, morphology, developmental rate and survival, but the response was highly heterogeneous among species. For instance, warming temperature increased body size in some species, and decreased size in others. Similarly, rainy periods increased survival of some species and reduced the survival of others. Our study showed contrasting impacts of temperature and precipitation changes on amphibian populations. Both climatic parameters strongly influenced amphibian performance, but temperature was the major determinant of the phenological changes, while precipitation had the major role on population dynamics, with alarming declines associated with drying trends.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Altwegg R, Reyer H-U (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882

    Article  PubMed  Google Scholar 

  2. Alvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195

    Article  Google Scholar 

  3. Anderson TL et al (2015) Abundance and phenology patterns of two pond-breeding salamanders determine species interactions in natural populations. Oecologia 177:761–773

    Article  PubMed  Google Scholar 

  4. Araujo MB, Thuiller W, Pearson RG (2006) Climate warming and the decline of amphibians and reptiles in Europe. J Biogeogr 33:1712–1728

    Article  Google Scholar 

  5. Arnqvist G, Wooster D (1995) Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol Evol 10:236–240

    CAS  Article  PubMed  Google Scholar 

  6. Banks B, Beebee TJC, Cooke AS (1994) Conservation of the natterjack toad Bufo calamita in Britain over the period 1970–1990 in relation to site protection and other factors. Biol Conserv 67:111–118

    Article  Google Scholar 

  7. Beebee TJC (1995) Amphibian breeding and climate. Nature 374:219–220

    CAS  Article  Google Scholar 

  8. Beebee TJC (2002) Amphibian phenology and climate change. Conserv Biol 16:1454

    Article  Google Scholar 

  9. Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125:271–285

    Article  Google Scholar 

  10. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377

    Article  PubMed  PubMed Central  Google Scholar 

  11. 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

    Article  Google Scholar 

  12. Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5:597–608

    Article  Google Scholar 

  13. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83

    CAS  Article  PubMed  Google Scholar 

  14. Buckley LB, Hurlbert AH, Jetz W (2012) Broad-scale ecological implications of ectothermy and endothermy in changing environments. Glob Ecol Biogeogr 21:873–885

    Article  Google Scholar 

  15. 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

    Article  Google Scholar 

  16. Cooper H, Hedges LV, Valentine JC (2009) The handbook of research synthesis and meta-analysis. Russel Sage Foundation, New York

    Google Scholar 

  17. Corn PS (2005) Climate change and amphibians. Anim Biodivers Conserv 28:59–67

    Google Scholar 

  18. Courtois E et al. (2015) Taking the lead on climate change: modeling and monitoring the fate of an Amazonian frog. Oryx. doi: 10.1017/S0030605315000083

  19. Dunn PO, Moller AP (2014) Changes in breeding phenology and population size of birds. J Anim Ecol 83:729–739

    Article  PubMed  Google Scholar 

  20. Earl JE, Semlitsch RD (2013) Carryover effects in amphibians: are characteristics of the larval habitat needed to predict juvenile survival? Ecol Appl 23:1429–1442

    Article  PubMed  Google Scholar 

  21. Ficetola GF (2015) Habitat conservation research for amphibians: methodological improvements and thematic shifts. Biodivers Conserv 24:1293–1310

    Article  Google Scholar 

  22. Ficetola GF, Pennati R, Manenti R (2012) Do cave salamanders occur randomly in cavities? An analysis with Hydromantes strinatii. Amphib-Reptil 33:251–259

    Article  Google Scholar 

  23. Ge QS, Wang HJ, Rutishauser T, Dai JH (2015) Phenological response to climate change in China: a meta-analysis. Glob Change Biol 21:265–274

    Article  Google Scholar 

  24. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge

    Google Scholar 

  25. Gomez-Mestre I, Pyron RA, Wiens JJ (2012) Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66:3687–3700

    Article  PubMed  Google Scholar 

  26. Grafe TU, Kaminsky SK, Bitz JH, Lussow H, Linsenmair KE (2004) Demographic dynamics of the afro-tropical pig-nosed frog, Hemisus marmoratus: effects of climate and predation on survival and recruitment. Oecologia 141:40–46

    Article  PubMed  Google Scholar 

  27. Griffiths RA, Sewell D, McCrea RS (2010) Dynamics of a declining amphibian metapopulation: survival, dispersal and the impact of climate. Biol Conserv 143:485–491

    Article  Google Scholar 

  28. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22

    Article  Google Scholar 

  29. Hadfield JD, Nakagawa S (2010) General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J Evol Biol 23:494–508

    CAS  Article  PubMed  Google Scholar 

  30. Harris I, Jones PD, Osborn TJ, Lister DH (2014) Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 Dataset. Int J Climatol 34:623–642

    Article  Google Scholar 

  31. Hof C, Araujo MB, Jetz W, Rahbek C (2012) Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480:516–519

    Google Scholar 

  32. Hossack BR et al (2013) Roles of patch characteristics, drought frequency, and restoration in long-term trends of a widespread amphibian. Conserv Biol 27:1410–1420

    Article  PubMed  Google Scholar 

  33. Intergovernmental Panel on Climate Change (2013) Climate change 2013. The physical science basis. IPCC, Switzerland

    Google Scholar 

  34. Kearney M, Porter W (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species ranges. Ecol Lett 12:334–350

    Article  PubMed  Google Scholar 

  35. Kéry M (2010) Introduction to WinBUGS for ecologists. Academic, Burlington

    Google Scholar 

  36. Kwon TS, Lee CM, Kim SS (2014) Northward range shifts in Korean butterflies. Clim Change 126:163–174

    Article  Google Scholar 

  37. Laurance WF (2008) Global warming and amphibian extinctions in eastern Australia. Austral Ecol 33:1–9

    Article  Google Scholar 

  38. Lawler JJ, Shafer SL, Bancroft BA, Blaustein AR (2010) Projected climate impacts for the amphibians of the western hemisphere. Conserv Biol 24:38–50

    Article  PubMed  Google Scholar 

  39. Li YM, Cohen JM, Rohr JR (2013) Review and synthesis of the effects of climate change on amphibians. Integr Zool 8:145–161

    Article  PubMed  Google Scholar 

  40. Lips KR, Diffendorfer JE, Mendelson JR III, Sears MW (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol 6:441–454

    CAS  Article  Google Scholar 

  41. Mac Nally R, Nerenberg S, Thomson JR, Lada H, Clarke RH (2013) Do frogs bounce, and if so, by how much? Responses to the ‘big wet’ following the ‘big dry’ in south-eastern Australia. Glob Ecol Biogeogr 23:223–234

    Article  Google Scholar 

  42. Maiorano L et al (2013) Building the niche through time: using 13,000 years of data to predict the effects of climate change on three tree species in Europe. Glob Ecol Biogeogr 22:302–317

    Article  Google Scholar 

  43. Mazaris AD, Kallimanis AS, Pantis JD, Hays GC (2013) Phenological response of sea turtles to environmental variation across a species northern range. Proc R Soc Lond B 280:20122397

    Article  Google Scholar 

  44. McCaffery RM, Maxell BA (2010) Decreased winter severity increases viability of a montane frog population. Proc Natl Acad Sci USA 107:8644–8649

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Menéndez-Guerrero PA, Graham CH (2013) Evaluating multiple causes of amphibian declines of Ecuador using geographical quantitative analyses. Ecography 36:756–769

    Article  Google Scholar 

  46. Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14

    Article  PubMed  PubMed Central  Google Scholar 

  47. Moller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc Natl Acad Sci USA 105:16195–16200

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Nakagawa S, Ockendon N, Gillespie DOS, Hatchwell BJ, Burke T (2007) Assessing the function of house sparrows bib size using a flexible meta-analysis method. Behav Ecol 18:831–840

    Article  Google Scholar 

  49. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872

    Article  Google Scholar 

  50. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    CAS  Article  PubMed  Google Scholar 

  51. Parmesan C et al (2013) Beyond climate change attribution in conservation and ecological research. Ecol Lett 16:58–71

    Article  PubMed  Google Scholar 

  52. Phillimore AB, Hadfield JD, Jones OR, Smithers RJ (2010) Differences in spawning date between populations of common frog reveal local adaptation. Proc Natl Acad Sci USA 107:8292–8297

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Pounds JA, Fogden MPL, Savage JM, Gorman GC (1997) Tests of null models for amphibian declines on a tropical mountain. Conserv Biol 11:1307–1322

    Article  Google Scholar 

  54. Pounds JA, Fogden MPL, Campbell JA (1999) Biological response to climate change on a tropical mountain. Nature 398:611–615

    CAS  Article  Google Scholar 

  55. Pounds JA et al (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167

    CAS  Article  PubMed  Google Scholar 

  56. Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR (2013) Disease and thermal acclimation in a more variable and unpredictable climate. Nat Clim Change 3:146–151

    Article  Google Scholar 

  57. Reading CJ (2003) The effects of variation in climatic temperature (1980–2001) on breeding activity and tadpole stage duration in the common toad, Bufo bufo. Sci Total Environ 310:231–236

    CAS  Article  PubMed  Google Scholar 

  58. Reading CJ (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151:125–131

    CAS  Article  PubMed  Google Scholar 

  59. Reading CJ (2010) The impact of environmental temperature on larval development and metamorph body condition in the common toad, Bufo bufo. Amphib-Reptil 31:483–488

    Article  Google Scholar 

  60. Reading CJ, Clarke RT (1995) The effects of density, rainfall and environmental-temperature on body condition and fecundity in the common toad, Bufo bufo. Oecologia 102:453–459

    Article  Google Scholar 

  61. Reading CJ, Clarke RT (1999) Impacts of climate and density on the duration of the tadpole stage of the common toad Bufo bufo. Oecologia 121:310–315

    Article  Google Scholar 

  62. Reinhardt T, Steinfartz S, Weitere M (2015) Inter-annual weather variability can drive the outcome of predator prey match in ponds. Amphib-Reptil 36:97–109

    Article  Google Scholar 

  63. Rohlf FJ (2005) tpsDig2, digitize landmarks and outlines. Department of ecology and evolution, State University of New York. http://life.bio.sunysb.edu/morph/soft-dataacq.html (Stony Brook, NY)

  64. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008) Evaluating the links between climate, disease spread, and amphibian declines. Proc Natl Acad Sci USA 105:17436–17441

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60

    CAS  Article  PubMed  Google Scholar 

  66. Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59:464–468

    Article  PubMed  Google Scholar 

  67. Rosenthal R (1994) Parametric measures of effect size. In: Cooper H, Hedges LV (eds) The handbook of research synthesis. Russel Sage Foundation, New York, pp 231–244

    Google Scholar 

  68. Scherer RD, Muths E, Lambert BA (2008) Effects of weather on survival in populations of boreal toads in Colorado. J Herpetol 42:508–517

    Article  Google Scholar 

  69. Schmidt BR, Hoedl W, Schaub M (2012) From metamorphosis to maturity in complex life cycles: equal performance of different juvenile life history pathways. Ecology 93:657–667

    Article  PubMed  Google Scholar 

  70. Stewart MM (1995) Climate driven population fluctuations in rain-forest frogs. J Herpetol 29:437–446

    Article  Google Scholar 

  71. Stuart SN et al (eds) (2008) Threatened amphibians of the world. Lynx, Barcelona

    Google Scholar 

  72. Timm BC, McGarigal K, Compton BW (2007) Timing of large movement events of pond-breeding amphibians in Western Massachusetts, USA. Biol Conserv 136:442–454

    Article  Google Scholar 

  73. Todd BD, Scott DE, Pechmann JHK, Gibbons JW (2011) Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community. Proc R Soc Lond B 278:2191–2197

    Article  Google Scholar 

  74. Tryjanowski P, Sparks T, Rybacki M, Berger L (2006) Is body size of the water frog Rana esculenta complex responding to climate change? Naturwissenschaften 93:110–113

    CAS  Article  PubMed  Google Scholar 

  75. Urban MC, Richardson JL, Freidenfelds NA (2014) Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change. Evol Appl 7:88–103

    Article  PubMed  Google Scholar 

  76. Walther GR et al (2002) Ecological responses to recent climate change. Nature 416:389–395

    CAS  Article  PubMed  Google Scholar 

  77. While GM, Uller T (2014) Quo vadis amphibia? Global warming and breeding phenology in frogs, toads and salamanders. Ecography 37:921–929

    Article  Google Scholar 

  78. Wilson DB, Lipsey MW (2000) Practical meta-analysis. Sage, London

    Google Scholar 

  79. Zug GR, Vitt LJ, Caldwell JP (2001) Herpetology. Academic, San Diego

    Google Scholar 

Download references

Acknowledgments

We thank R. Gavazzi for help in data gathering; the comments of two reviewers improved an earlier version of this paper. GFF is member of LECA, which is part of OSUG@2020.

Author contribution statement

GFF and LM jointly participated to all the phases of the research (planning, data gathering, analyses). GFF wrote the first draft of the manuscript, with subsequent contribution of LM.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gentile Francesco Ficetola.

Additional information

Communicated by Raoul Van Damme.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 76 kb)

Supplementary material 2 (PPTX 149 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ficetola, G.F., Maiorano, L. Contrasting effects of temperature and precipitation change on amphibian phenology, abundance and performance. Oecologia 181, 683–693 (2016). https://doi.org/10.1007/s00442-016-3610-9

Download citation

Keywords

  • Amphibian decline
  • Breeding success
  • Climatic oscillation
  • Geographical bias
  • Population dynamics