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

  1. Deborah A. Hutchinson*,,
  2. Akira Mori,
  3. Alan H. Savitzky*,
  4. Gordon M. Burghardt§,
  5. Xiaogang Wu,
  6. Jerrold Meinwald,, and
  7. Frank C. Schroeder
  1. *Department of Biological Sciences, Old Dominion University, Norfolk, VA 23529;
  2. Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan;
  3. §Departments of Psychology and Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996; and
  4. Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853
  1. Contributed by Jerrold Meinwald, December 5, 2006 (received for review December 1, 2006)

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.

Footnotes

  • To whom correspondence may be addressed. E-mail: dhutchin{at}odu.edu or circe{at}cornell.edu
  • Author contributions: A.M., A.H.S., G.M.B., and J.M. designed research; D.A.H., X.W., and F.C.S. performed research; D.A.H., X.W., and F.C.S. analyzed data; and D.A.H., A.H.S., and F.C.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0610785104/DC1.

  • Abbreviations:
    HPLC-MS,
    high-performance liquid chromatography and mass spectroscopy;
    1H-NMR,
    proton NMR.
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