Density, climate and varying return points: an analysis of long-term population fluctuations in the threatened European tree frog

Experimental research has identified many putative agents of amphibian decline, yet the population-level consequences of these agents remain unknown, owing to lack of information on compensatory density dependence in natural populations. Here, we investigate the relative importance of intrinsic (density-dependent) and extrinsic (climatic) factors impacting the dynamics of a tree frog (Hyla arborea) population over 22years. A combination of log-linear density dependence and rainfall (with a 2-year time lag corresponding to development time) explain 75% of the variance in the rate of increase. Such fluctuations around a variable return point might be responsible for the seemingly erratic demography and disequilibrium dynamics of many amphibian population

Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers

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

Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers

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

Thermal conditions predict intraspecific variation in senescence rate in frogs and toads

Variation in temperature is known to influence mortality patterns in ectotherms. Even though a few experimental studies on model organisms have reported a positive relationship between temperature and actuarial senescence (i.e., the increase in mortality risk with age), how variation in climate influences the senescence rate across the range of a species is still poorly understood in free-ranging animals. We filled this knowledge gap by investigating the relationships linking senescence rate, adult lifespan, and climatic conditions using long-term capture-recapture data from multiple amphibian populations. We considered two pairs of related anuran species from the Ranidae (Rana luteiventris and Rana temporaria) and Bufonidae (Anaxyrus boreas and Bufo bufo) families, which diverged more than 100 Mya and are broadly distributed in North America and Europe. Senescence rates were positively associated with mean annual temperature in all species. In addition, lifespan was negatively correlated with mean annual temperature in all species except A. boreas. In both R. luteiventris and A. boreas, mean annual precipitation and human environmental footprint both had negligible effects on senescence rates or lifespans. Overall, our findings demonstrate the critical influence of thermal conditions on mortality patterns across anuran species from temperate regions. In the current context of further global temperature increases predicted by Intergovernmental Panel on Climate Change scenarios, a widespread acceleration of aging in amphibians is expected to occur in the decades to come, which might threaten even more seriously the viability of populations and exacerbate global decline.Peer reviewe

Sex-related differences in aging rate are associated with sex chromosome system in amphibians

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the "unguarded X/Z effect") or repeat-rich Y/W chromosome (the "toxic Y/W effect") could accelerate aging in the heterogametic sex in some vertebrate clades.Peer reviewe

Shifts in amphibian population dynamics in response to a change in the predator community

Predation can affect prey behavior, demography, abundance, and distribution, particularly in lentic freshwater ecosystems. Fish are predators known to reduce the abundance of their prey and to restrict the distribution of species. Using time series which spanned 43 and 22 yr, respectively, we analyzed the effect of a change in the fish predator community on the dynamics of two pond‐breeding amphibian populations (Rana temporaria and Rana dalmatina). Specifically, we used a state‐space time series model which allows for density dependence and observation error, to ask whether the change in predation risk affects population growth rate and the return point around which the populations fluctuate. The results showed that the type of observation error assumed did not affect the biological parameters. We found evidence for density dependence in both populations. The effect of the change in fish predation on population growth rate and the return point was strong in the population where fish invaded a previously fish‐free pond. The effect was weaker in the population where the change was from cyprinid fish to pike. The results showed that fish predation can have strong effects on amphibian population dynamics. The observed population dynamical pattern is phenomenologically similar to alternative stable states

Shifts in amphibian population dynamics in response to a change in the predator community

Abstract Predation can affect prey behavior, demography, abundance, and distribution, particularly in lentic freshwater ecosystems. Fish are predators known to reduce the abundance of their prey and to restrict the distribution of species. Using time series which spanned 43 and 22 yr, respectively, we analyzed the effect of a change in the fish predator community on the dynamics of two pond‐breeding amphibian populations (Rana temporaria and Rana dalmatina). Specifically, we used a state‐space time series model which allows for density dependence and observation error, to ask whether the change in predation risk affects population growth rate and the return point around which the populations fluctuate. The results showed that the type of observation error assumed did not affect the biological parameters. We found evidence for density dependence in both populations. The effect of the change in fish predation on population growth rate and the return point was strong in the population where fish invaded a previously fish‐free pond. The effect was weaker in the population where the change was from cyprinid fish to pike. The results showed that fish predation can have strong effects on amphibian population dynamics. The observed population dynamical pattern is phenomenologically similar to alternative stable states

Analysis of three amphibian populations with quarter-century long time-series.

Amphibians are in decline in many parts of the world. Long time-series of amphibian populations are necessary to distinguish declines from the often strong fluctuations observed in natural populations. Time-series may also help to understand the causes of these declines. We analysed 23-28-year long time-series of the frog Rana temporaria. Only one of the three studied populations showed a negative trend which was probably caused by the introduction of fish. Two populations appeared to be density regulated. Rainfall had no obvious effect on the population fluctuations. Whereas long-term studies of amphibian populations are valuable to document population declines, most are too short to reveal those factors that govern population dynamics or cause amphibian populations to decline