Section: Ecology
Topic: Ecology, Population biology, Environmental sciences
Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers
10.24072/pcjournal.240 - Peer Community Journal, Volume 3 (2023), article no. e15.
Get full text PDF Peer reviewed and recommended by PCI
Strong phenological shifts in response to changes in climatic conditions have been reported for many species, including amphibians, which are expected to breed earlier. Phenological shifts in breeding are observed in a wide number of amphibian populations, but less is known about populations living at high elevations, which are predicted to be more sensitive to climate change than lowland populations. The goal of this study is to assess the main factors determining the timing of breeding in an alpine population of the common toad (Bufo bufo) and to describe the observed shifts in its breeding phenology. We modelled the effect of environmental variables on the start and peak dates of the breeding season using 39 years of individual-based data. In addition, we investigated the effect of the lunar cycle, as well as the individual variation in breeding phenology. Finally, to assess the individual heterogeneity in the timing of breeding, we calculated the repeatability of the timing of arrival at the breeding site. Breeding advanced to earlier dates in the first years of the study but the trend continued only until the mid 1990s, and stabilised afterwards. Overall, toads are now breeding on average around 30 days earlier than at the start of the study period. High temperatures and low snow cover in winter and spring, as well as reduced spring precipitation were all associated with earlier breeding. Additionally, we found evidence of males arriving on average before females at the breeding site but no clear and strong effect of the lunar cycle. We only found weak evidence of among-individual variation in shifts in the breeding phenology, as well as a low repeatability of arrival timing. Our findings show that the observed changes in breeding phenology are strongly associated with the environmental conditions. These results contribute to filling a knowledge gap on the effects of climate change on alpine amphibian populations. Moreover, we show that changes in phenology, especially in the mountains, can be hard to predict as local microclimatic conditions do not necessarily reflect the observed global climatic trends.
Type: Research article
CC-BY 4.0
@article{10_24072_pcjournal_240,
author = {Lenzi, Omar and Grossenbacher, Kurt and Zumbach, Silvia and L\"uscher, Beatrice and Althaus, Sarah and Schmocker, Daniela and Recher, Helmut and Thoma, Marco and Ozgul, Arpat and Schmidt, Benedikt R.},
title = {Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers},
journal = {Peer Community Journal},
eid = {e15},
publisher = {Peer Community In},
volume = {3},
year = {2023},
doi = {10.24072/pcjournal.240},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.240/}
}
TY - JOUR AU - Lenzi, Omar AU - Grossenbacher, Kurt AU - Zumbach, Silvia AU - Lüscher, Beatrice AU - Althaus, Sarah AU - Schmocker, Daniela AU - Recher, Helmut AU - Thoma, Marco AU - Ozgul, Arpat AU - Schmidt, Benedikt R. TI - Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers JO - Peer Community Journal PY - 2023 VL - 3 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.240/ DO - 10.24072/pcjournal.240 ID - 10_24072_pcjournal_240 ER -
%0 Journal Article %A Lenzi, Omar %A Grossenbacher, Kurt %A Zumbach, Silvia %A Lüscher, Beatrice %A Althaus, Sarah %A Schmocker, Daniela %A Recher, Helmut %A Thoma, Marco %A Ozgul, Arpat %A Schmidt, Benedikt R. %T Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers %J Peer Community Journal %D 2023 %V 3 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.240/ %R 10.24072/pcjournal.240 %F 10_24072_pcjournal_240
Lenzi, Omar; Grossenbacher, Kurt; Zumbach, Silvia; Lüscher, Beatrice; Althaus, Sarah; Schmocker, Daniela; Recher, Helmut; Thoma, Marco; Ozgul, Arpat; Schmidt, Benedikt R. Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers. Peer Community Journal, Volume 3 (2023), article no. e15. doi : 10.24072/pcjournal.240. https://peercommunityjournal.org/articles/10.24072/pcjournal.240/
Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100469
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] R package 'circular': Circular statistics, 2017 (https://r-forge.r-project.org/projects/circular/)
[2] Phenological delay despite warming in wood frog Rana sylvatica reproductive timing: a 20‐year study, Ecography, Volume 43 (2020) no. 12, pp. 1791-1800 | DOI
[3] Multi-Model Inference, 2019 (https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf)
[4] Amphibian breeding and climate, Nature, Volume 374 (1995) no. 6519, pp. 219-220 | DOI
[5] The amphibian decline crisis: A watershed for conservation biology?, Biological Conservation, Volume 125 (2005) no. 3, pp. 271-285 | DOI
[6] Long-term area-mean temperature series for Switzerland—Combining homogenized station data and high resolution grid data, International Journal of Climatology, Volume 38 (2018) no. 6, pp. 2792-2807 | DOI
[7] Best environmental predictors of breeding phenology differ with elevation in a common woodland bird species, Ecology and Evolution, Volume 10 (2020) no. 18, pp. 10219-10229 | DOI
[8] Earlier snowmelt advances breeding phenology of the common frog (Rana temporaria) but increases the risk of frost exposure and wetland drying, Frontiers in Ecology and Evolution, Volume 9 (2021), p. 645585 | DOI
[9] Linking effective population size dynamics to phenotypic traits in the common toad (Bufo bufo), Conservation Genetics, Volume 20 (2019), pp. 987-995
[10] Amphibian breeding and climate change: Importance of snow in the mountains, Conservation Biology, Volume 17 (2003) no. 2, pp. 622-625 | DOI
[11] Variable breeding phenology affects the exposure of amphibian embryos to ultraviolet radiation, Ecology, Volume 83 (2002) no. 11, pp. 2958-2963 | DOI
[12] Climate variability and change in high elevation regions: past, present and future, Climatic Change, Volume 59 (2003), pp. 1-4 | DOI
[13] A new parameterization for integrated population models to document amphibian reintroductions, Ecological Applications, Volume 27 (2017) no. 6, pp. 1761-1775 | DOI
[14] Biology of amphibians, JHU Press, 1994
[15] Introduction to quantitative genetics, Longman, London, 1981
[16] Shifting aspect or elevation? The climate change response of ectotherms in a complex mountain topography, Diversity and Distributions, Volume 26 (2020) no. 11, pp. 1483-1495 | DOI
[17] Contrasting effects of temperature and precipitation change on amphibian phenology, abundance and performance, Oecologia, Volume 181 (2016) no. 3, pp. 683-693 | DOI
[18] Bringing the analysis of animal orientation data full circle: Model-based approaches with maximum likelihood, Journal of Experimental Biology, Volume 220 (2017) no. 21, pp. 3878-3882 | DOI
[19] Individual repeatability of avian migration phenology: A systematic review and meta-analysis, Journal of Animal Ecology, Volume 91 (2022) no. 7, pp. 1416-1430 | DOI
[20] Climate change, chytridiomycosis or condition: An experimental test of amphibian survival, Global Change Biology, Volume 17 (2011) no. 2, pp. 667-675 | DOI
[21] Scaling regression inputs by dividing by two standard deviations, Statistics in Medicine, Volume 27 (2008) no. 15, pp. 2865-2873 | DOI
[22] Population dynamics of the common toad (Bufo bufo) at a lake in Mid-Wales, The Journal of Animal Ecology, Volume 52 (1983) no. 3, p. 981 | DOI
[23] Population characteristics of the common toad (Bufo bufo) visiting a breeding site in Mid-Wales, Journal of Animal Ecology, Volume 49 (1980) no. 1, pp. 161-173 | DOI
[24] Growth strategies of ectothermic animals in temperate environments, Environment and animal development: Genes, life histories and plasticity, BIOS Scientific, Oxford, 2001, pp. 287-304
[25] Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines, Scientific Reports, Volume 6 (2016) no. 1, p. 25625 | DOI
[26] Amphibian breeding phenology trends under climate change: predicting the past to forecast the future, Global Change Biology, Volume 23 (2017) no. 2, pp. 646-656 | DOI
[27] Body size varies with abundance, not climate, in an amphibian population, Ecography, Volume 36 (2013) no. 8, pp. 947-955 | DOI
[28] Springtime emergence of overwintering toads, Anaxyrus fowleri, in relation to environmental factors, Copeia, Volume 104 (2016) no. 2, pp. 393-401 | DOI
[29] First results of a 20-year-study on common toad Bufo bufo in the Swiss Alps, Biota, Volume 3 (2002) no. 1-2, pp. 43-48
[30] Metapopulation dynamics, Nature, Volume 396 (1998) no. 6706, pp. 41-49 | DOI
[31] The reproductive dynamics of temperate amphibians: A review, North-Western Journal of Zoology, Volume 3 (2007)
[32] Age, growth and other population characteristics of Bufo bufo from different latitudes and altitudes, Journal of Herpetology, Volume 22 (1988) no. 4, p. 369 | DOI
[33] Sollzeit der Laichwanderung bei der Erdkröte, Bufo bufo (L.), Revue Suisse de Zoologie, Volume 75 (1968), pp. 1005-1022
[34] Chorusing behaviour, a density-dependent alternative mating strategy in male common toads (Bufo bufo), Ethology, Volume 79 (1988) no. 4, pp. 324-332 | DOI
[35] Random mating by size in a population of common toads (Bufo bufo), Amphibia-Reptilia, Volume 8 (1987) no. 4, pp. 321-330 | DOI
[36] Demographic consequences of phenological shifts in response to climate change, Annual Review of Ecology Evolution and Systematics, Volume 52 (2021) no. 1, pp. 221-245 | DOI
[37] The ecology and evolution of reproductive synchrony, Trends in Ecology & Evolution, Volume 5 (1990) no. 5, pp. 135-140 | DOI
[38] Warming-induced shifts in amphibian phenology and behavior lead to altered predator–prey dynamics, Oecologia, Volume 189 (2019) no. 3, pp. 803-813 | DOI
[39] Lunar phase as a cue for migrations to two species of explosive breeding amphibians—implications for conservation, European Journal of Wildlife Research, Volume 67 (2021) no. 1, p. 11 | DOI
[40] Climate change and geomorphological hazards in the eastern European Alps, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Volume 368 (2010) no. 1919, pp. 2461-2479 | DOI
[41] Density dependence and adult survival drive dynamics in two high elevation amphibian populations, Diversity, Volume 12 (2020) no. 12, p. 478 | DOI
[42] Competition for early arrival in migratory birds, Journal of Animal Ecology, Volume 68 (1999) no. 5, pp. 940-950 | DOI
[43] Spring migration distances of some Central European amphibian species, Amphibia-Reptilia, Volume 30 (2009) no. 3, pp. 367-378 | DOI
[44] Why is the alpine flora comparatively robust against climatic warming?, Diversity, Volume 13 (2021) no. 8, p. 383 | DOI
[45] Spring migration distances of some Central European amphibian species, Amphibia-Reptilia, Volume 30 (2009) no. 3, pp. 367-378 | DOI
[46] High individual repeatability of the migratory behaviour of a long-distance migratory seabird, Movement Ecology, Volume 10 (2022) no. 1, p. 5 | DOI
[47] lmerTest Package: Tests in Linear Mixed Effects Models, Journal of Statistical Software, Volume 82 (2017) no. 13 | DOI
[48] Circular data in biology: advice for effectively implementing statistical procedures, Behavioral Ecology and Sociobiology, Volume 72 (2018) no. 8, p. 128 | DOI
[49] lunar: Lunar phase and distance, seasons and other environmental factors, 2014 (https://cran.r-project.org/web/packages/lunar/index.html)
[50] Beyond demographic buffering: Context dependence in demographic strategies across animals, bioRxiv (2021) | DOI
[51] Unrepeatable repeatabilities: A common mistake, The Auk, Volume 104 (1987) no. 1, pp. 116-121 | DOI
[52] Reproductive tactics of large and small male toads Bufo bufo, Oikos, Volume 46 (1986) no. 1, p. 57 | DOI
[53] Die Höhenverbreitung der Erdkröte (Bufo bufo) im Berner Oberland (Schweiz) unter sich verändernden Klimabedingungen, Zeitschrift für Feldherpetologie, Volume 23 (2016), pp. 47-58
[54] Quantifying climate sensitivity and climate-driven change in North American amphibian communities, Nature Communications, Volume 9 (2018) no. 1, p. 3926 | DOI
[55] Climate-associated decline of body condition in a fossorial salamander, Global Change Biology, Volume 28 (2022) no. 5, pp. 1725-1739 | DOI
[56] Ecology and breeding phenology of larval Hyla andersonii: The disadvantages of breeding late, Ecology, Volume 71 (1990) no. 4, pp. 1590-1598 | DOI
[57] Segmented: An R package to fit regression models with broken-line, R News, Volume 8 (2008) no. 1, pp. 20-25
[58] Local adaptation with high gene flow: Temperature parameters drive adaptation to altitude in the common frog (Rana temporaria), Molecular Ecology, Volume 23 (2014) no. 3, pp. 561-574 | DOI
[59] Attribution of extreme weather events in the context of climate change, National Academies Press, Washington, D.C., 2016
[60] Exposure of global mountain systems to climate warming during the 21st Century, Global Environmental Change, Volume 17 (2007) no. 3-4, pp. 420-428 | DOI
[61] Grasshopper community response to climatic change: Variation along an elevational gradient, PLoS ONE, Volume 5 (2010) no. 9, pp. 1-11 | DOI
[62] Transgenerational effects and impact of compensatory responses to changes in breeding phenology on antipredator defenses, Ecology, Volume 97 (2016) no. 9, pp. 2470-2478 | DOI
[63] Environmental factors influencing calling in sympatric anurans, Oecologia, Volume 133 (2002) no. 4, pp. 616-625 | DOI
[64] Influences of species, latitudes and methodologies on estimates of phenological response to global warming, Global Change Biology, Volume 13 (2007) no. 9, pp. 1860-1872 | DOI
[65] A globally coherent fingerprint of climate change impacts across natural systems, Nature, Volume 421 (2003) no. 6918, pp. 37-42 | DOI
[66] Differences in spawning date between populations of common frog reveal local adaptation, Proceedings of the National Academy of Sciences, Volume 107 (2010) no. 18, pp. 8292-8297 | DOI
[67] A capture-recapture design robust to unequal probability of capture, The Journal of Wildlife Management, Volume 46 (1982) no. 3, pp. 752-757 | DOI
[68] Amphibian and reptile phenology: the end of the warming hiatus and the influence of the NAO in the North Mediterranean, International Journal of Biometeorology, Volume 64 (2020) no. 3, pp. 423-432 | DOI
[69] Genetic variability and phenotypic plasticity in flowering phenology in populations of two grasses, The Journal of the Torrey Botanical Society, Volume 129 (2002) no. 2, pp. 96-106 | DOI
[70] R: A language and environment for statistical computing, R foundation for statistical computing, Vienna, Austria, 2020 (https://www.R-project.org/)
[71] RStudio: Integrated Development for R, 2022
[72] Increase of extreme events in a warming world, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 44, pp. 17905-17909 | DOI
[73] The effects of variation in climatic temperature (1980–2001) on breeding activity and tadpole stage duration in the common toad, Bufo bufo, Science of The Total Environment, Volume 310 (2003) no. 1-3, pp. 231-236 | DOI
[74] Linking global warming to amphibian declines through its effects on female body condition and survivorship, Oecologia, Volume 151 (2007) no. 1, pp. 125-131 | DOI
[75] The impact of environmental temperature on larval development and metamorph body condition in the common toad, Bufo bufo, Amphibia-Reptilia, Volume 31 (2010) no. 4, pp. 483-488 | DOI
[76] Male breeding behaviour and mate acquisition in the common toad, Bufo bufo, Journal of Zoology, Volume 201 (1983) no. 2, pp. 237-246 | DOI
[77] Impacts of climate and density on the duration of the tadpole stage of the common toad Bufo bufo, Oecologia, Volume 121 (1999) no. 3, pp. 310-315 | DOI
[78] Monthly air temperature trends in Switzerland 1901–2000 and 1975–2004, Theoretical and Applied Climatology, Volume 91 (2008) no. 1, pp. 27-34 | DOI
[79] Inter-annual weather variability can drive the outcome of predator prey match in ponds, Amphibia-Reptilia, Volume 36 (2015) no. 2, pp. 97-109 | DOI
[80] Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming, Journal of Biogeography, Volume 38 (2011) no. 2, pp. 406-416 | DOI
[81] Analysis of climatic factors influencing migrations of the salamander Ambystoma talpoideum, Copeia, Volume 1985 (1985) no. 2, pp. 477-489 | DOI
[82] Phenotypic variation in the arrival time of breeding salamanders: Individual repeatability and environmental influences, The Journal of Animal Ecology, Volume 62 (1993) no. 2, p. 334 | DOI
[83] Seasonal changes in the migratory behaviour of the toad Bufo bufo: direction and magnitude of movements, Oecologia, Volume 76 (1988), pp. 390-398 | DOI
[84] Density regulation in toad populations (Epidalea calamita, Bufotes viridis) by differential winter survival of juveniles, Journal of Thermal Biology, Volume 55 (2016), pp. 20-29 | DOI
[85] rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models, Methods in Ecology and Evolution, Volume 8 (2017), pp. 1639-1644 | DOI
[86] Into thin air: vertical migration, body condition, and quality of terrestrial habitats of alpine common toads, Bufo bufo, Canadian Journal of Zoology, Volume 83 (2005), pp. 788-796 | DOI
[87] Emerging opportunities and challenges in phenology: A review, Ecosphere, Volume 7 (2016) no. 8, p. e01436 | DOI
[88] Ice core evidence for climate change in the Tropics: Implications for our future, Quaternary Science Reviews, Volume 19 (2000), pp. 19-35 | DOI
[89] Generating surfaces of daily meteorological variables over large regions of complex terrain, Journal of Hydrology (Aggregate Description of Land-Atmosphere Interactions), Volume 190 (1997) no. 3, pp. 214-251 | DOI
[90] Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community, Proceedings of the Royal Society Biological sciences, Volume 278 (2011), p. 2191-7 | DOI
[91] Changes in the first spawning dates of common frogs and common toads in western Poland in 1978–2002, Annales Zoologici Fennici, Volume 40 (2003), pp. 459-464
[92] Microclimate-driven trends in spring-emergence phenology in a temperate reptile (Vipera berus): Evidence for a potential “climate trap”?, Ecology and Evolution, Volume 12 (2022) no. 2, p. e8623 | DOI
[93] Escalator to extinction, Proceedings of the National Academy of Sciences, Volume 115 (2018) no. 47, pp. 11871-11873 | DOI
[94] Low repeatability of breeding events reflects flexibility in reproductive timing in the pied flycatcher Ficedula hypoleuca in Spain, Ardeola, Volume 69 (2021) no. 1, pp. 21-39 | DOI
[95] Evolutionary and demographic consequences of phenological mismatches, Nature Ecology & Evolution, Volume 3 (2019) no. 6, pp. 879-885 | DOI
[96] Phenological and elevational shifts of plants, animals and fungi under climate change in the European Alps, Biological Reviews, Volume 96 (2021) no. 5, pp. 1816-1835 | DOI
[97] The social behaviour of anuran amphibians, Animal Behaviour, Volume 25 (1977), pp. 666-693 | DOI
[98] Quo vadis amphibia? Global warming and breeding phenology in frogs, toads and salamanders, Ecography, Volume 37 (2014) no. 10, pp. 921-929 | DOI
[99] Climate change trade‐offs in the side‐blotched lizard (Uta stansburiana): Effects of growing‐season length and mild temperatures on winter survival, Physiological and Biochemical Zoology, Volume 81 (2008) no. 6, pp. 797-809 | DOI
[100] zoo: S3 infrastructure for regular and irregular time series, Journal of Statistical Software, Volume 14 (2005), pp. 1-27 | DOI
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