Abstract
Species that sequester toxins from prey for their own defense against predators may exhibit population-level variation in their chemical arsenal that reflects the availability of chemically defended prey in their habitat. Rhabdophis tigrinus is an Asian snake that possesses defensive glands in the skin of its neck (‘nuchal glands’), which typically contain toxic bufadienolide steroids that the snakes sequester from consumed toads. In this study, we compared the chemistry of the nuchal gland fluid of R. tigrinus from toad-rich and toad-free islands in Japan and determined the effect of diet on the nuchal gland constituents. Our findings demonstrate that captive-hatched juveniles from toad-rich Ishima Island that had not been fed toads possess defensive bufadienolides in their nuchal glands, presumably due to maternal provisioning of these sequestered compounds. Wild-caught juveniles from Ishima possess large quantities of bufadienolides, which could result from a combination of maternal provisioning and sequestration of these defensive compounds from consumed toads. Interestingly, juvenile females from Ishima possess larger quantities of bufadienolides than do juvenile males, whereas a small sample of field-collected snakes suggests that adult males contain larger quantities of bufadienolides than do adult females. Captive-born hatchlings from Kinkasan Island lack bufadienolides in their nuchal glands, reflecting the absence of toads on that island, but they can sequester bufadienolides by feeding on toads (Bufo japonicus) in captivity. The presence of large quantities of bufadienolides in the nuchal glands of R. tigrinus from Ishima may reduce the risk of predation by providing an effective chemical defense, whereas snakes on Kinkasan may experience increased predation due to the lack of defensive compounds in their nuchal glands.
Highlights
Toads are capable of synthesizing their defensive bufadienolides from cholesterol (Siperstein, Murray & Titus, 1957; Porto, Baralle & Gros, 1972), R. tigrinus is dependent on dietary toads from which it can sequester these compounds for storage in the nuchal glands (Hutchinson et al, 2007)
Whole-body extracts of metamorphic B. japonicus, which were fed to the hatchling R. tigrinus in the experimental group, contained small quantities of bufadienolides, as confirmed by nuclear magnetic resonance (NMR) spectroscopy and high-performance liquid chromatography (HPLC) (Fig. 3a)
Our results demonstrate clearly that the quantity of bufadienolides present in the nuchal glands of R. tigrinus reflects the availability of toads in the environment and, in captivity, is influenced by the diet of hatchlings
Summary
Animals that rely on chemicals for antipredator defense may synthesize those compounds from nontoxic precursors (Daly, 1995; Eisner, Eisner & Siegler, 2005) or sequester defensive toxins from other organisms (González, Hare & Eisner, 1999; Nishida, 2002; Dumbacher et al, 2004; Williams, Brodie Jr & Brodie III, 2004; Opitz & Müller, 2009; Saporito et al, 2012; Savitzky et al, 2012). Geographic variation in chemical defense would be more likely to exist among animals dependent on prey for sequestered chemical defenses if critical prey species are distributed unevenly or have geographically variable toxicity (Hanifin et al, 1999; Thompson, 2005). Bufadienolides are cardiotonic steroids, Variation in chemical defense of Rhabdophis tigrinus similar to cardiac glycosides in foxglove plants (Digitalis), that act by inhibiting the sodium–potassium pump, causing arrhythmia and cardiac failure in high doses (Melero, Medarde & San Feliciano, 2000). Toads are capable of synthesizing their defensive bufadienolides from cholesterol (Siperstein, Murray & Titus, 1957; Porto, Baralle & Gros, 1972), R. tigrinus is dependent on dietary toads from which it can sequester these compounds for storage in the nuchal glands (Hutchinson et al, 2007). Bufadienolides sequestered from toads can be provisioned by female R. tigrinus to offspring in utero by deposition of those compounds in yolk and by transfer to oviducal eggs during gestation (Hutchinson et al, 2008, 2012)
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