Toads phenotypically adjust their chemical defences to anthropogenic habitat change

Veronika Bókony,Nikolett Ujhegyi,Bálint Üveges,Viktória Verebélyi,Ágnes M Móricz

doi:10.1038/s41598-019-39587-3

Abstract

Despite the well-documented effects of human-induced environmental changes on the morphology, physiology, behaviour and life history of wild animals, next to nothing is known about how anthropogenic habitats influence anti-predatory chemical defence, a crucial fitness component of many species. We investigated the amount and composition of defensive toxins in adult common toads (Bufo bufo) captured in natural, agricultural and urban habitats, and in their offspring raised in a common-garden experiment. We found that, compared to toads captured from natural habitats, adults from both types of anthropogenic habitats had larger toxin glands (parotoids) and their toxin secretion contained higher concentrations of bufagenins, the more potent class of bufadienolide toxins. Furthermore, urban toads had lower concentrations of bufotoxins, the compounds with lower toxicity. None of these differences were present in the captive-raised juveniles; instead, toadlets originating from agricultural habitats had smaller parotoids and lower bufotoxin concentrations. These results suggest that toads’ chemical defences respond to the challenges of anthropogenic environments via phenotypic plasticity. These responses may constitute non-adaptive consequences of pollution by endocrine-disrupting chemicals as well as adaptive adjustments to the altered predator assemblages of urban and agricultural habitats.

Highlights

Natural habitats worldwide are increasingly modified by human-induced environmental change; for example, agricultural and urban areas have taken up about 40% and 5% of the Earth’s land surface, respectively[1,2]
To infer whether the differences we observed between toads from natural and anthropogenic habitats were due to microevolution or phenotypic plasticity, we used a common garden experiment to compare the chemical defences of juveniles raised from the eggs of the adults captured from different habitats
Our finding that adult toads had larger parotoids in urban and agricultural habitats than in natural habitats suggests that the total amount of stored toxins was higher in the animals captured from anthropogenic habitats

Summary

Introduction

Natural habitats worldwide are increasingly modified by human-induced environmental change; for example, agricultural and urban areas have taken up about 40% and 5% of the Earth’s land surface, respectively[1,2]. Over the past two decades, a surge of studies documented wide-ranging effects of these environmental changes on the morphology, physiology, behaviour and life history of wild organisms[3,4,5,6,7,8] Some of these phenotypic changes are maladaptive and contribute to population declines, while some are adaptive and help living in anthropogenic habitats[4]. Some predators can learn to avoid toxic prey and switch to other species which may alter trophic interactions and community structure[14,15]; whereas other predators adapt to consuming toxic prey by evolving toxin resistance, leading to co-evolutionary arms races between the defended organisms and their enemies[16] Despite this potential of defensive toxins to impact multiple populations across wildlife communities and thereby biodiversity conservation, we www.nature.com/scientificreports/. To infer whether the differences we observed between toads from natural and anthropogenic habitats were due to microevolution or phenotypic plasticity, we used a common garden experiment to compare the chemical defences of juveniles raised from the eggs of the adults captured from different habitats

Methods

Results

Conclusion