Compensatory recruitment allows amphibian population persistence in anthropogenic habitats.

Habitat anthropization is a major driver of global biodiversity decline. Although most species are negatively affected, some benefit from anthropogenic habitat modifications by showing intriguing life-history responses. For instance, increased recruitment through higher allocation to reproduction or improved performance during early-life stages could compensate for reduced adult survival, corresponding to "compensatory recruitment". To date, evidence of compensatory recruitment in response to habitat modification is restricted to plants, limiting understanding of its importance as a response to global change. We used the yellow-bellied toad (Bombina variegata), an amphibian occupying a broad range of natural and anthropogenic habitats, as a model species to test for and to quantify compensatory recruitment. Using an exceptional capture-recapture dataset composed of 21,714 individuals from 67 populations across Europe, we showed that adult survival was lower, lifespan was shorter, and actuarial senescence was higher in anthropogenic habitats, especially those affected by intense human activities. Increased recruitment in anthropogenic habitats fully offset reductions in adult survival, with the consequence that population growth rate in both habitat types was similar. Our findings indicate that compensatory recruitment allows toad populations to remain viable in human-dominated habitats and might facilitate the persistence of other animal populations in such environments.

Population position along the fast-slow life-history continuum predicts intraspecific variation in actuarial senescence.

Patterns of actuarial senescence can be highly variable among species. Previous comparative analyses revealed that both age at the onset of senescence and rates of senescence are linked to position of a species along the fast-slow life-history continuum. As there are few long-term datasets of wild populations with known-age individuals, intraspecific (i.e. between-population) variation in senescence is understudied and limited to comparisons of wild and captive populations of the same species, mostly birds and mammals. In this paper, we examined how population position along the fast-slow life-history continuum affects intraspecific variation in senescence in an amphibian, Bombina variegata. We used capture-recapture data collected in four populations with contrasting life-history strategies. Senescence trajectories were analysed using Bayesian capture-recapture models. We show that in populations with fast life histories the onset of actuarial senescence was earlier and individuals aged at a faster rate than individuals in populations with slow life histories. Our study provides one of the few empirical examples of among-population variation in actuarial senescence patterns in the wild and confirms that the fast-slow life-history gradient is associated with both macroevolutionary and microevolutionary patterns of actuarial senescence.

Transport infrastructure severely impacts amphibian dispersal regardless of life stage.

Transport infrastructure such as roads has been reported to negatively affect dispersal. Their effects on dispersal are thought to be complex, depending on the characteristics of the structure and the intensity of the traffic using it. In addition, individual factors, such as age, may strongly affect dispersal decisions and success when individuals are confronted with transport infrastructure. Despite the importance of this topic for wildlife conservation, few studies have investigated the effect of transport infrastructure on individuals' dispersal decisions before and after sexual maturity. We examined the effects on two kinds of infrastructure, gravel tracks and paved roads, on the dispersal of an endangered amphibian, the yellow-bellied toad (Bombina variegata). We used capture-recapture data collected during a five-year period on a large, spatially structured population of B. variegata. Our study revealed that emigration rates increased with an individual's age, while dispersal distance decreased. It also showed that both tracks and roads had negative effects on immigration. The negative effect of roads was stronger than that of tracks. We additionally found that the effect of tracks on dispersal slightly decreased with a toad's age. In contrast, the negative effect of roads was severe and relatively similar across age classes.

Survival cost to relocation does not reduce population self-sustainability in an amphibian.

Relocations are increasingly popular among wildlife managers despite often low rates of relocation success in vertebrates. In this context, understanding the influence of extrinsic (e.g., relocation design, habitat characteristics) and intrinsic factors (e.g., age and sex) on demographic parameters, such as survival, that regulate the dynamics of relocated populations is critical to improve relocation protocols and better predict relocation success. We investigated survival in naturally established and relocated populations of yellow-bellied toads (Bombina variegata), an amphibian that was nearly extinct in Belgium by the late 1980s. We quantified survival at three ontogenetic stages (juvenile, subadult, and adult) in the relocated population, the source population, and a control population. In the relocated population, we quantified survival in captive bred individuals and their locally born descendants. Then, using simulations, we examined how survival cost to relocation affects the self-sustainability of the relocated population. We showed that survival at juvenile and subadult stages was relatively similar in all populations. In contrast, relocated adult survival was lower than adult survival in the source and control populations. Despite this, offspring of relocated animals (the next generation, regardless of life stage) survived at similar rates to individuals in the source and control populations. Simulations revealed that the relocated population was self-sustaining under different scenarios and that the fate (e.g., stability or increase) of the simulated populations was highly dependent on the fecundity of relocated adults and their offspring. To summarize, our results indicate that survival in relocated individuals is lower than in non-relocated individuals but that this cost (i.e., reduced survival) disappears in the second generation. A finer understanding of how relocation affects demographic processes is an important step in improving relocation success of amphibians and other animals.

Estimating dispersal in spatiotemporally variable environments using multievent capture-recapture modeling.

Dispersal is a key process in ecological and evolutionary dynamics. Spatiotemporal variation in habitat availability and characteristics has been suggested to be one of the main cause involved in dispersal evolution and has a strong influence on metapopulation dynamics. In recent decades, the study of dispersal has led to the development of capture-recapture (CR) models that allow movement between sites to be quantified, while handling imperfect detection. For studies involving numerous recapture sites, Lagrange et al. () proposed a multievent CR model that allows dispersal to be estimated while omitting site identity by distinguishing between individuals that stay and individuals that move. More recently, Cayuela et al. () extended this model to allow survival and dispersal probabilities to differ for the different types of habitat represented by several sites within a study area. Yet in both of these modeling systems, the state of sites is assumed to be static over time, which is not a realistic assumption in dynamic landscapes. For that purpose, we generalized the multievent CR model proposed by Cayuela et al. () to allow the estimation of dispersal, survival and recapture probabilities when a site may appear or disappear over time (MODEL 1) or when the characteristics of a site fluctuate over space and time (MODEL 2). This paper first presents these two new modeling systems, and then provides an illustration of their efficacy and usefulness by applying them to simulated CR data and data collected on two metapopulations of amphibians. MODEL 1 was tested using CR data recorded on a metapopulation of yellow-bellied toads (Bombina variegata). In this first empirical case, we examined whether the drying-out dynamics of ponds and the past dispersal status of an individual might affect dispersal behavior. Our study revealed that the probability of facultative dispersal (i.e., from a pond group that remained available/flooded) fluctuated between years and was higher in individuals that had previously dispersed. MODEL 2 was tested using CR data collected on a metapopulation of great crested newts (Triturus cristatus). In this second empirical example, we investigated whether the density of alpine newts (Ichthyosaura alpestris), a potential competitor, might affect the dispersal and survival of the crested newt. Our study revealed that the departure rate was lower in ponds with a high density of heterospecifics than in ponds with a low density of heterospecifics at both inter-annual and intra-annual scales. Moreover, annual survival was slightly higher in ponds with a high density of heterospecifics. Overall, our findings indicate that these multievent CR models provide a highly flexible means of modeling dispersal in dynamic landscapes.

Life history tactics shape amphibians' demographic responses to the North Atlantic Oscillation.

Over the last three decades, climate abnormalities have been reported to be involved in biodiversity decline by affecting population dynamics. A growing number of studies have shown that the North Atlantic Oscillation (NAO) influences the demographic parameters of a wide range of plant and animal taxa in different ways. Life history theory could help to understand these different demographic responses to the NAO. Indeed, theory states that the impact of weather variation on a species' demographic traits should depend on its position along the fast-slow continuum. In particular, it is expected that NAO would have a higher impact on recruitment than on adult survival in slow species, while the opposite pattern is expected occur in fast species. To test these predictions, we used long-term capture-recapture datasets (more than 15,000 individuals marked from 1965 to 2015) on different surveyed populations of three amphibian species in Western Europe: Triturus cristatus, Bombina variegata, and Salamandra salamandra. Despite substantial intraspecific variation, our study revealed that these three species differ in their position on a slow-fast gradient of pace of life. Our results also suggest that the differences in life history tactics influence amphibian responses to NAO fluctuations: Adult survival was most affected by the NAO in the species with the fastest pace of life (T. cristatus), whereas recruitment was most impacted in species with a slower pace of life (B. variegata and S. salamandra). In the context of climate change, our findings suggest that the capacity of organisms to deal with future changes in NAO values could be closely linked to their position on the fast-slow continuum.

Does habitat unpredictability promote the evolution of a colonizer syndrome in amphibian metapopulations?

Dispersal is a central component of life history evolution. An increasing number of studies suggest that spatiotemporally variable environments may promote the evolution of "dispersal syndromes," consisting of covariation patterns between dispersal and morphological, physiological, behavioral, and life history traits. At the interspecific scale, the "colonizer syndrome" appears to be one of the most frequently recorded associations between dispersal and life history traits, linking a high dispersal rate, high fecundity, and a short lifespan as systematically combined adaptations in spatiotemporally varying environments. However, few studies have highlighted the existence of a "colonizer syndrome" at the intraspecific scale, and none have investigated how different degrees of habitat stochasticity might shape covariation patterns between dispersal and life history traits. In this study, we examined this issue in free-ranging metapopulations of the yellow-bellied toad (Bombina variegata) using capture-recapture data. Combining the results of this study with another recent study, we found that a high dispersal rate, high fecundity, and a short lifespan are associated in metapopulations experiencing unpredictable environments. In contrast, a very low dispersal rate (close to zero), low fecundity and a long lifespan are associated in metapopulations occupying predictable environments. We discuss these results as well as their demographic and evolutionary consequences.

Contrasting patterns of environmental fluctuation contribute to divergent life histories among amphibian populations.

Because it modulates the fitness returns of possible options of energy expenditure at each ontogenetic stage, environmental stochasticity is usually considered a selective force in driving or constraining possible life histories. Divergent regimes of environmental fluctuation experienced by populations are expected to generate differences in the resource allocation schedule between survival and reproductive effort and outputs. To our knowledge, no study has previously examined how different regimes of stochastic variation in environmental conditions could result in changes in both the temporal variation and mean of demographic parameters, which could then lead to intraspecific variation along the slow-fast continuum of life history tactics. To investigate these issues, we used capture-recapture data collected on five populations of a long-lived amphibian (Bombina variegata) experiencing two distinct levels of stochastic environmental variation: (1) constant availability of breeding sites in space and time (predictable environment), and (2) variable spatio-temporal availability of breeding sites (unpredictable environment). We found that female breeding propensity varied more from year to year in unpredictable than in predictable environments. Although females in unpredictable environments produced on average more viable offspring per year, offspring production was more variable between years. Survival at each ontogenetic stage was slightly lower and varied significantly more from year to year in unpredictable environments. Taken together, these results confirm that increased environmental stochasticity can modify the resource allocation schedule between survival and reproductive effort and outputs and may lead to intraspecific variation along the slow-fast continuum of life history tactics.

Demographic responses to weather fluctuations are context dependent in a long-lived amphibian.

Weather fluctuations have been demonstrated to affect demographic traits in many species. In long-lived organisms, their impact on adult survival might be buffered by the evolution of traits that reduce variation in interannual adult survival. For example, skipping breeding is an effective behavioral mechanism that may limit yearly variation in adult survival when harsh weather conditions occur; however, this in turn would likely lead to strong variation in recruitment. Yet, only a few studies to date have examined the impact of weather variation on survival, recruitment and breeding probability simultaneously in different populations of the same species. To fill this gap, we studied the impact of spring temperatures and spring rainfall on survival, on reproductive skipping behavior and on recruitment in five populations of a long-lived amphibian, the yellow-bellied toad (Bombina variegata). Based on capture-recapture data, our findings demonstrate that survival depends on interactions between age, population and weather variation. Varying weather conditions in the spring result in strong variation in the survival of immature toads, whereas they have little effect on adult toads. Breeding probability depends on both the individual's previous reproductive status and on the weather conditions during the current breeding season, leading to high interannual variation in recruitment. Crucially, we found that the impact of weather variation on demographic traits is largely context dependent and may thus differ sharply between populations. Our results suggest that studies predicting the impact of climate change on population dynamics should be taken with caution when the relationship between climate and demographic traits is established using only one population or few populations. We therefore highly recommend further research that includes surveys replicated in a substantial number of populations to account for context-dependent variation in demographic processes.

To breed or not to breed: past reproductive status and environmental cues drive current breeding decisions in a long-lived amphibian.

Iteroparity is an adaptive response to uncertainty in reproductive success. However, spreading reproductive success over multiple reproduction events during a lifetime is constrained by adult mortality and the stochasticity associated with interactions between external factors and physiological states. The acquisition of information about environmental conditions during the growth of progeny and sufficient resources during the non-reproductive period are key factors for breeding success. Consequently, we hypothesized that long-lived animals may skip a breeding opportunity when information about unfavourable environmental conditions is available. In addition, nutritional constraints could prevent an animal from replenishing its reserves sufficiently to invest in the current breeding period. We investigated these questions using capture-recapture data from a 5-year study on a large population of yellow-bellied toads in a forest in north-eastern France. We took advantage of various advances in multi-state capture-recapture models (e.g. unobservable states and mixture models) to test our hypotheses. Our results show that the combined effects of rainfall deficit and the breeding/non-breeding state of individuals during the past breeding season affect breeding probability during the following breeding opportunity. We also found that females breed less frequently than males, suggesting that the overall energy cost of reproduction differs between genders. Finally, the results indicate that toad survival appears to be negatively influenced by rainfall deficits. We discuss the yellow-bellied toad's reproductive behaviour in term of bet-hedging strategy and life history trait evolution.

Exposure assessment of a burning ground for chemical ammunition on the Great War battlefields of Verdun.

The destruction of arsenical shells from the 1914/18 war in the vicinity of Verdun (France) during the 1920s resulted in a locally limited but severe soil contamination by arsenic and heavy metals. At the study site, the main part of the contaminant inventory occurs in the upper 20 cm of the topsoil which is essentially composed of combustion residues. Besides, some Cu (cmax.=16,877 mg/kg) and Pb (cmax.=26,398 mg/kg) in this layer, As (cmax.=175,907 mg/kg) and Zn (cmax.=133,237 mg/kg) were detected in very high concentrations. The mobilities of Cu, Mn, Pb and Zn in the soil system were derived from ammonium nitrate eluates. They are strongly influenced by the soil pH and can be described by quadratic regression curves from which threshold pH values were calculated. Below these values more than 10% of the element content was available as mobile species. Within the examined pH range, this method could not be adopted for arsenic, because the mobility of As was only slightly controlled by the soil pH. In the heavily contaminated topsoil, Cu and Pb were fixed by the moderately acidic soil pH which varied from 4.8 to 5.8. No migration to the underlying horizons occurred. A different behavior was observed for As and Zn. The calculated threshold pH of Zn was 5.5, so certain amount of this element was transferred to the subsoil and the leachate (cmax.=350 microg/l). However, a major dispersion of Zn was prevented by a rise of the soil pH in the carbonate-containing subsoil. Elevated concentrations of As were found in all soil horizons up to a depth of 2 m and also in the leachate (cmax.=2377 microg/l). Contrary to Cu, Pb and Zn the mobility of As evidently was less affected by the subsoil. Regarding organic contaminants, nitroaromatic explosives were detected only in minor concentrations in the soil (cmax.=14.7 mg/kg) and the leachate (cmax.=13.5 microg/l). No aromatic organoarsenicals were detected in the soil and the leachate samples. The main hazard of the site is the severe arsenic contamination and the transfer of this carcinogen by leachate, surface runoff and probably by wind. Nevertheless, some studies on the effects of the contaminant inventory on the local vegetation revealed that ammonium nitrate elutable zinc is responsible for the spatial distribution of some tolerant plant species and not arsenic. Previously undetected buried munitions from the former delaboration facility can be an other source of environmental contaminants. This is supported by elevated concentrations of chlorate (cmax.=71 mg/l) and perchlorate (cmax.=0.8 mg/l) detected in the leachate samples. This is the second report about environmental contamination related to post-war ammunition destruction activities along the 1914/18 Western Front.