Active foraging for toxic prey during gestation in a snake with maternal provisioning of sequestered chemical defences

Abstract

Many animals sequester dietary defensive compounds and incorporate them into the offspring, which protects the young against predation. One possible but poorly investigated question is whether females of such species actively prey upon toxic diets. The snake Rhabdophis tigrinus sequesters defensive steroids from toads consumed as prey; it also feeds on other amphibians. Females produce chemically armed offspring in direct proportion to their own level of toad-derived toxins by provisioning the toxins to their eggs. Our field observations of movements and stomach contents of radio-tracked R. tigrinus showed that gravid snakes preyed upon toads by actively foraging in the habitat of toads, even though toads were a scarce resource and toad-searching may incur potential costs. Our Y-maze experiments demonstrated that gravid females were more likely to trail the chemical cues of toads than were males or non-gravid females. These results showed behavioural switching in females and active foraging for scarce, toxic prey during gestation. Because exploitation of toads by gravid females results in their offspring being more richly endowed with prey-derived toxins, active foraging for toxic prey is expected to be an adaptive antipredator trait, which may enhance chemical defence in offspring.

Dramatic dietary shift maintains sequestered toxins in chemically defended snakes

“…Certain insects employ plant-derived defensive toxins as feeding attractants, as in the case of pipevine swallowtail butterflies (Troidini and Zerythiini), for which aristolochic acids serve both functions (38). Indeed, the moderate response of R. pentasupralabialis to toad scent, and the consumption of one toad by a captive individual, suggest that members of the R. nuchalis Group retain at least some degree of the ancestral chemical preference for toads as prey (39). The relatively elongate shape and soft bodies of most firefly larvae may also enhance their general resemblance to earthworms.…”

Coevolution takes the sting out of it: Evolutionary biology and mechanisms of toxin resistance in animals

“…Moreover, this species also exhibits maternal provisioning of nuchal gland toxins to their offspring as mothers deposit bufodienolides on their eggs (Hutchinson et al, 2008). Gravid females are known to shift their foraging behaviour to actively search for (scarce) toads, a potentially adaptive behaviour arguably selected because it provides higher levels of bufodienolides to the offspring, thus enhancing their chemical defence and potential survival (Kojima and Mori, 2015).…”

Corticosteroid responses of snakes to toxins from toads (bufadienolides) and plants (cardenolides) reflect differences in dietary specializations

“…Although bufonids comprise a relatively small proportion of the species' diet (Kojima and Mori, 2015), R. tigrinus sequesters BDs from toads for use in its own defense, thereby exposing at least some of its tissues to BDs for an extended period (Hutchinson et al, 2007). Furthermore, females of this species are known to forage preferentially for toads during the season when vitellogenesis occurs (Kojima and Mori, 2015). The generalist and resistant group (GR) included the congeners Thamnophis sirtalis, T. elegans, and T. radix.…”