Ant and mite diversity drives toxin variation in the Little Devil poison frog

Abstract

Poison frogs sequester chemical defenses from arthropod prey, although the details of how arthropod diversity contributes to variation in poison frog toxins remains unclear. We characterized skin alkaloid profiles in the Little Devil frog, Oophaga sylvatica (Dendrobatidae), across three populations in northwestern Ecuador. Using gas chromatography mass spectrometry, we identified histrionicotoxins, 3,5- and 5,8-disubstituted indolizidines, decahydroquinolines, and lehmizidines as the primary alkaloid toxins in these O. sylvatica populations. Frog skin alkaloid composition varied along a latitudinal gradient across populations in a principal component analysis. We also characterized diversity in arthropods isolated from frog stomach contents and confirmed O. sylvatica specialize on ants and mites. To test the hypothesis that poison frog toxin diversity reflects species and chemical diversity in arthropod prey, we (1) used liquid chromatography mass spectrometry to chemically profile consumed ants and mites, and (2) used sequencing of cytochrome oxidase 1 to identify individual prey specimens. We show that chemical profiles of consumed ants and mites cluster by frog population, suggesting different frog populations have access to chemically distinct prey. We identified 45 ants and 9 mites isolated from frog stomachs, finding several undescribed species. Finally, by comparing chemical profiles of frog skin and isolated prey items, we were able to trace the arthropod source of four poison frog alkaloids, including 3,5- and 5,8-disubstituted indolizidines and a lehmizidine alkaloid. Together, our data shows the diversity of alkaloid toxins found in O. sylvatica can be traced to chemical diversity in arthropod prey.