Intensive agriculture increases fluctuating asymmetry of dorsal head shape in Iberian asp viper populations

Abstract

Habitats resulting from agricultural intensification harbour a wide array of stressors for resident organisms. Environmental stress during development can leave imprints on the phenotype that are useful as indicators of its impairment. Among them, fluctuating asymmetry (FA), considered the morphological manifestation of developmental instability (DI), may reflect the increment of developmental noise and the inefficiency of buffering mechanisms. Here, we evaluated for the first time the impact of intensive agriculture on the development of a viviparous reptile, the asp viper, Vipera aspis (Linnaeus 1758), by means of FA. To this end, we first quantified unsigned asymmetry indexes (uAI) of dorsal head shape captured by geometric morphometrics (GM) and of seven pholidotic traits in 127 and 482 individuals, respectively. Using linear models, we then tested for variation in uAI according to habitat type. Furthermore, we tested the effect of climatic variables with a potential influence on development, and thus, on FA. We performed analyses at the V. aspis zinnikeri subspecies range and at the population level, including three well-sampled natural localities (NAT) and three sites of intensive agriculture (AGR). We found significantly higher FA levels in dorsal head shape in individuals from agricultural habitats than in those from natural habitats, which suggests that asp viper development is impaired by stressors resulting from agricultural intensification. Our results also point to a lower sensitivity of traditional morphological tools to capture the signal that intensive agriculture leaves on development and a lack of capacity of climatic factors in isolation to predict variation in the degree of asymmetry. In addition to encouraging the use of high-precision methods, we hypothesize on the overall effect of different stressors linked to intensive agriculture as the real constraint.