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.
A species' life history is a strong determinant of its risk of extinction; traits such as body size, growth rate, age at maturity and fecundity influence population viability and persistence, as well as capacity for dispersal and colonisation of new habitats. Yet, despite the potential for substantial geographic variation in life history, most conservation programmes rely upon the species average rather than information specific to individual populations. We use the Guthega Skink (Liopholis guthega), a threatened alpine endemic lizard restricted to two geographically isolated locations in southeastern Australia, as a case study to demonstrate how geographic variation in life history traits may better inform conservation management. Liopholis guthega has a relatively short life span, with only a few years of reproductive activity, inter-annual variation in reproductive output, and less-than-annual reproduction. We show that the Victorian population has a significantly slower growth rate, attains a smaller maximum size, reaches reproductive maturity later, and produces significantly smaller litters, despite no difference in longevity suggesting that it may be more vulnerable to extinction. We, therefore, suggest evaluating genetic rescue from the New South Wales population to improve recruitment and longevity of Victorian L. guthega, ongoing population monitoring in both locations, and a dedicated pest control programme to reduce pressure on this population. Our study has far reaching impacts; primarily demonstrating how knowledge of geographic variation in life history has the potential to improve conservation management of threatened species.
Amphibian populations world-wide are threatened by declines and extinctions mainly due to habitat loss and fragmentation. Habitat fragmentation threatens the yellow-bellied toad Bombina variegata in the northern and western regions of its distribution where it is strictly protected. We studied the genetic structure and diversity of populations at three geographical scales using microsatellite loci to detect potential threats for population persistence. At the local scale, we sampled four neighbouring localities at 1–2.6 km distance to detect effects of short-term (decades) fragmentation on connectivity. At the regional scale, five additional localities in the mountains of the Westerwald (Rhineland-Palatinate, Germany) were studied at up to 50.1 km distance to analyse genetic diversity and population structure. At the continental scale, we included data from regions in the northern distribution with fragmented populations (Hesse and Lower Saxony, Germany) and more continuous populations in the South (Alsace, France; Geneva, Switzerland; Trentino, Italy) to evaluate variation of genetic diversity. At the local scale, short-term fragmentation caused significant genetic differentiation between breeding assemblages only 1.4 km apart from each other. At the regional scale, we found notable genetic distance among localities. At the continental scale, we identified Alsace, Trentino and Geneva in the South as regions with low genetic structuring and high allelic richness, and the northern remaining regions in Germany as deeply structured with reduced allelic richness. We suggest that reduced genetic diversity and habitat fragmentation in northern regions makes these populations particularly vulnerable to decline. In conclusion, informed conservation management of B. variegata should focus on measures maintaining or improving connectivity among neighbouring populations.
Yellow-bellied toad populations (Bombina variegata) show a wide fast–slow continuum of the life-history trait longevity ranging from 5 to 23 years. We investigated populations in Germany (n = 8) and Austria (n = 1) to determine their position within the continuum of longevity and the potential drivers of adult survival at the local and the continental scale. Intrinsic and extrinsic factors considered were local weather, nutritional state, allocation of ingested energy to somatic growth, pathogen prevalence, and geographical clines (latitude, altitude, and longitude). Capture-mark-recapture (CMR) monitoring and direct age assessment by skeletochronology allowed for reliable estimates of longevity and adult survival. Raw and corrected recapture rates as well as a probabilistic estimate of the lifespan of the eldest 1% adults of a cohort (CMR data) were used as surrogates for adult survival and thus longevity in a population. Additionally, survival rates were calculated from static life tables based on the age structure (skeletochronological data) of eight populations. Populations in Germany were short-lived with a maximum lifespan of annual cohorts varying from 5 to 8 years, whereas the population in Austria was long-lived with a cohort longevity of 13 to 23 years. We provide evidence that annual survival rates and longevity differ among years and between short- and long-lived populations, but there was no decrease of survival in older toads (i.e. absence of senescence). Variation of weather among years accounted for 90.7% of variance in annual survival rates of short-lived populations, whereas the sources of variation in the long-lived population remained unidentified. At the continental scale, longevity variation among B. variegata populations studied so far did not correspond to geographical clines or climate variation. Therefore, we propose that a population’s position within the fast–slow continuum integrates the response to local environmental stochasticity (extrinsic source of variation) and the efficiency of chemical antipredator protection determining the magnitude of longevity (intrinsic source of variation).
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