Amphibian population genetics in agricultural landscapes: does viniculture drive the population structuring of the European common frog (Rana temporaria)?

Patrick P. Lenhardt,Carsten A. Brühl,Christoph Leeb,Kathrin Theissinger

doi:10.7717/peerj.3520

Abstract

Amphibian populations have been declining globally over the past decades. The intensification of agriculture, habitat loss, fragmentation of populations and toxic substances in the environment are considered as driving factors for this decline. Today, about 50% of the area of Germany is used for agriculture and is inhabited by a diverse variety of 20 amphibian species. Of these, 19 are exhibiting declining populations. Due to the protection status of native amphibian species, it is important to evaluate the effect of land use and associated stressors (such as road mortality and pesticide toxicity) on the genetic population structure of amphibians in agricultural landscapes. We investigated the effects of viniculture on the genetic differentiation of European common frog (Rana temporaria) populations in Southern Palatinate (Germany). We analyzed microsatellite data of ten loci from ten breeding pond populations located within viniculture landscape and in the adjacent forest block and compared these results with a previously developed landscape permeability model. We tested for significant correlation of genetic population differentiation and landscape elements, including land use as well as roads and their associated traffic intensity, to explain the genetic structure in the study area. Genetic differentiation among forest populations was significantly lower (median pairwise FST = 0.0041 at 5.39 km to 0.0159 at 9.40 km distance) than between viniculture populations (median pairwise FST = 0.0215 at 2.34 km to 0.0987 at 2.39 km distance). Our analyses rejected isolation by distance based on roads and associated traffic intensity as the sole explanation of the genetic differentiation and suggest that the viniculture landscape has to be considered as a limiting barrier for R. temporaria migration, partially confirming the isolation of breeding ponds predicted by the landscape permeability model. Therefore, arable land may act as a sink habitat, inhibiting genetic exchange and causing genetic differentiation of pond populations in agricultural areas. In viniculture, pesticides could be a driving factor for the observed genetic impoverishment, since pesticides are more frequently applied than any other management measure and can be highly toxic for terrestrial life stages of amphibians.

Highlights

The survival of amphibian wildlife populations is threatened by habitat loss, fragmentation of populations, diseases, invasive species, climate change and toxic substances (Stuart et al, 2008)
We introduced a habitat correction factor into the model (Table 2), since each habitat type may impact the genetic differentiation with a different magnitude
The highest percentage of linkage disequilibrium was detected for the locus pair BFG66 & BFG90 (95%)

Summary

Introduction

The survival of amphibian wildlife populations is threatened by habitat loss, fragmentation of populations, diseases, invasive species, climate change and toxic substances (Stuart et al, 2008). Beside habitat loss and fragmentation of remaining suitable habitats or populations, agriculture often requires the development of irrigation, drainage and/or retention systems, which can impact the availability and quality of amphibian breeding sites. Despite their limited dispersal capacity compared with other vertebrates (Hillman et al, 2014), amphibians have been able to persist in agricultural landscapes by adapting to the altered availability of breeding sites (Mann et al, 2009). Amphibians regularly have to cross agricultural land during dispersal and seasonal migration (i.e., spring migration for reproduction) or for foraging and are likely exposed to field cultivation measures (Becker et al, 2007; Lenhardt, Brühl & Berger, 2014; Joseph, 2016)

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