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Link to original content: https://pubmed.ncbi.nlm.nih.gov/17284596/
Dietary sequestration of defensive steroids in nuchal glands of the Asian snake Rhabdophis tigrinus - PubMed Skip to main page content
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. 2007 Feb 13;104(7):2265-70.
doi: 10.1073/pnas.0610785104. Epub 2007 Feb 6.

Dietary sequestration of defensive steroids in nuchal glands of the Asian snake Rhabdophis tigrinus

Deborah A Hutchinson  1 , Akira Mori, Alan H Savitzky, Gordon M Burghardt, Xiaogang Wu, Jerrold Meinwald, Frank C Schroeder
Affiliations

Dietary sequestration of defensive steroids in nuchal glands of the Asian snake Rhabdophis tigrinus

Deborah A Hutchinson et al. Proc Natl Acad Sci U S A. .

Abstract

The Asian snake Rhabdophis tigrinus possesses specialized defensive glands on its neck that contain steroidal toxins known as bufadienolides. We hypothesized that R. tigrinus does not synthesize these defensive steroids but instead sequesters the toxins from toads it consumes as prey. To test this hypothesis, we conducted chemical analyses on the glandular fluid from snakes collected in toad-free and toad-present localities. We also performed feeding experiments in which hatchling R. tigrinus were reared on controlled diets that either included or lacked toads. We demonstrate that the cardiotonic steroids in the nuchal glands of R. tigrinus are obtained from dietary toads. We further show that mothers containing high levels of bufadienolides can provision their offspring with toxins. Hatchlings had bufadienolides in their nuchal glands only if they were fed toads or were born to a dam with high concentrations of these compounds. Because geographic patterns in the availability of toxic prey are reflected in the chemical composition of the glandular fluid, snakes in toad-free regions are left undefended by steroidal toxins. Our findings confirm that the sequestration of dietary toxins underlies geographic variation in antipredatory behavior in this species and provide a unique example of sequestered defensive compounds in a specialized vertebrate structure.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Nuchal glands of R. tigrinus. (A) Snake in typical defensive posture (“neck arch”), with head bent and dorsal skin of neck exposed to predator. Arrow indicates the ridge formed by the underlying nuchal glands. (B) Vascular cast of skin in ventral view, showing the dense capillary beds of the paired nuchal glands. Blood vessels have been filled with yellow latex, and the surrounding tissues have been cleared with methyl salicylate. Anterior is toward the left. (Scale bar: 5 mm.) (C) Transverse section through a pair of nuchal glands, showing the absence of a secretory epithelium, lumen, or duct. The blue tissue is dermal collagen, which forms a dense capsule around each gland. The glands empty by rupturing through the thin skin between adjacent scales. Trichrome stain was used. (Scale bar: 1 mm.)
Fig. 2.
Fig. 2.
Bufadienolides from the toads B. fowleri and B. terrestris. Major components from B. fowleri include compounds T1, T2 (hellebritoxin), T3, T4, T5, and T6, whereas those in B. terrestris include T3, T6, T7 (gamabufotalin), T8, and T9 (11α-hydroxyresibufagenin). Compounds T1, T4, and T6 are new natural products.
Fig. 3.
Fig. 3.
Aromatic region of 1H-NMR spectra of nuchal gland fluid from R. tigrinus. (A) Dam no. 3 and her hatchlings. The dam and her unfed and fish-fed hatchlings lacked bufadienolides (note the absence of peaks in the three regions diagnostic of bufadienolides, highlighted in green). The hatchlings only accumulated the toxins when fed toads. (B) A hatchling born to dam no. 3 that lacked bufadienolides at hatching (day 0) but accumulated increasing quantities as toads were consumed during the following 2 months. Arrows indicate the presence of small quantities of bufadienolides. (C) A chemically defended dam (no. 4) and her offspring, which were maternally provisioned with toxins.
Fig. 4.
Fig. 4.
HPLC chromatogram of pooled samples of nuchal gland fluid from R. tigrinus hatchlings born to dam no. 4 that were fed toads for 34–64 days. The 17 bufadienolides we identified are indicated by number (see Fig. 5). mAU, milli-absorbance units at 280 nm.
Fig. 5.
Fig. 5.
Seventeen bufadienolides from the nuchal gland fluid of R. tigrinus. Compound 8 is 11α-hydroxytelocinobufagin, compound 10 is gamabufotalin, compound 13 is hellebrigenin, and compound 17 is telocinobufagenin. Compounds 2–6 and 9 are new natural products.
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