Nuance in the Narrative of a Brown Poison Frog: Environmental Alkaloids and Specialized Foraging in a Presumed Toxin-Free and Diet-Generalized Species.

Abstract

In poison frogs (Dendrobatidae), conspicuous colors have evolved repeatedly in tandem with high numbers and quantities of skin toxins (alkaloids). Here, we focus on an inconspicuously-colored species-Silverstoneia flotator-which has long been deemed toxin-free and thought to forage opportunistically on mites and ants. Both assumptions have received some empirical support, but there is also evidence that predators avoid S. flotator. In a Panamanian S. flotator population, we sampled invertebrates in frog diets and the surrounding environment (using Berlese and pitfall traps) and screened for skin, dietary, and environmental alkaloids using untargeted metabolomics. We found that while the frogs are opportunistic consumers of mites and ants, they display preferences at finer taxonomic scales (for symphypleonan springtails and Pheidole ants). We also annotated 64 skin compounds as alkaloids, 38 of which were present in the environment. One alkaloid present in the skin and environment is likely the highly potent epibatidine. While the average biosynthetic (class and superclass) diversity of alkaloids in a dorsal skin sample is higher than that of a ventral skin and environmental-but not dietary-sample, environmental samples diverge more in their alkaloids' biosynthetic diversities than do dietary or skin samples. The frogs consume a consistent set of alkaloids, forage in a variable chemical space, and possess diverse dorsal skin alkaloids. They might use finer-scale diet specialization to modulate the types, quantities, and numbers of alkaloids they ingest. We encourage further examination of inconspicuously-colored taxa to better understand the ecological importance of diet-acquired toxins and specialized diets in these organisms.