Do predators prefer toxic animals? A case of chemical discrimination by an Asian snake that sequesters firefly toxins

Abstract

Several Asian natricine snakes of the genus Rhabdophis feed on toads and sequester steroidal cardiac toxins known as bufadienolides (BDs) from them. A recent study revealed that species of the R. nuchalis Group ingest lampyrine fireflies to sequester BDs. Although several species of fireflies are distributed in the habitat of the R. nuchalis Group, only lampyrine fireflies, which have BDs, included in the diet of these snakes. Thus, we hypothesized that the R. nuchalis Group chemically distinguishes fireflies that have BDs from those that do not have BDs. We also predicted that the R. nuchalis Group detects BDs as the chemical cue of toxin source. To test these predictions, we conducted three behavioral experiments using R. chiwen, which belongs to the R. nuchalis Group. In the first experiment, R. chiwen showed a moderate tongue flicking response to cinobufagin, a compound of BDs. On the other hand, the snake showed a higher response to the chemical stimuli of lampyrine fireflies (BD fireflies) than those of lucioline fireflies (non-BD fireflies). In the second experiment, in which we provided live BD and non-BD fireflies, the snake voluntarily consumed only the former. In the third, a Y-maze experiment, the snake tended to select the chemical trail of BD fireflies more frequently than that of non-BD fireflies. These results demonstrated that R. chiwen discriminates BD fireflies from non-BD fireflies, but the prediction that BDs are involved in this discrimination was not fully supported. To identify the proximate mechanisms of the recognition of novel toxic prey in the R. nuchalis Group, further investigation is necessary.

Conspicuous coloration of toxin‐resistant predators implicates additional trophic interactions in a predator–prey arms race

“…Interactions between toxic prey and resistant predators seem especially likely to generate effects that extend to other trophic levels. For example, snakes in the related Natricine genus Rhabodophis sequester defensive bufadienolide toxins from toad and firefly prey and also display red patches on interscalar tissue when threatened (Fukuda et al, 2021;Hutchinson et al, 2007Hutchinson et al, , 2012Mori et al, 2012;Yoshida et al, 2020). Similarly, toxin-resistant monarch butterflies sequester the defensive cardiac glycosides in milkweeds and, as a result, some of the butterflies' avian and mammalian predators seem to have also evolved toxin-resistant mutations (Groen & Whiteman, 2021;Karageorgi et al, 2019;Petschenka & Agrawal, 2015).…”

An Investigation of Chemical Prey Discrimination by Rhabdophis subminiatus Hints the Source of Nuchal Gland Toxins

“…In experimental studies of squamate reptiles, the frequency of tongue flicking has been used as a measure of prey chemical discrimination, detection of predator chemicals, and response to pheromones (Cooper, 1998). Many studies have shown that the presentation of chemical stimuli aids in investigating snake prey preference (Burghardt, 1967;Tanaka et al, 2001;Aubret et al, 2006;Fukuda et al, 2021). These experimental snakes responded by flicking their tongue and also biting a cotton swab applicator soaked in prey chemical stimuli, especially if it carried the chemical stimuli of their preferred prey (Cooper and Burghardt, 1990).…”