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Nuchal glands: a novel defensive system in snakes

Abstract

Of the various chemical defensive adaptations of vertebrates, nuchal glands are among the most unusual. First described in a Japanese natricine snake, Rhabdophis tigrinus, in 1935, these organs are embedded under the skin of the neck region as a series of paired glands that have neither lumina nor ducts. The major chemical components of the glandular fluid are bufadienolides, which are cardiotonic steroids also found in the skin secretion of toads. Here we review early studies of nuchal glands and briefly introduce our recent findings on the sequestration of bufadienolides from consumed toads and the maternal provisioning of those sequestered compounds. We summarize behavioral studies associated with the antipredator function of the nuchal glands, which have been conducted during our more than decade-long collaboration. Results of preliminary analyses on the possible costs of toad-eating and on the ultrastructure of the nuchal glands are also presented. Finally, we discuss the evolutionary origin of the nuchal glands and suggest future directions designed to understand the biological importance of these novel vertebrate organs, which have evolved in a limited number of snake species.

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Acknowledgments

We thank J. Placyk and J. M. Ray for their assistance in conducting experiments, M. Toriba for his comments on taxonomy of snakes, K. Isogawa, M. Motokawa, and K. Nishikawa for obtaining literature, and many students and colleagues for their help in collecting and keeping animals. We greatly appreciate J. Meinwald and F. C. Schroeder for their invaluable help with the chemical analyses. The first author especially wishes to thank the late A. Mutoh for his invitation to the amazing world of Rhabdophis tigrinus. The original idea of dietary sequestration was inspired during a discussion with M. Hasegawa. This research was supported in part by Grants from the Japan–US Cooperative Science Program (Japan Society for the Promotion of Science: JSPS); a Grant from JSPS (Scientific Research C: 23570115); Grants for the twentyfirst Century COE Program (A14) and the Global COE Program (A06) to Kyoto University; and grants from the US National Science Foundation (IBN-0429223 and IOB-0519458 to AHS and J. Meinwald). This paper is based on a presentation in the symposium “Sequestered Defensive Compounds in Tetrapod Vertebrates: A Symposium in Memory of John W. Daly”, held at the Sixth World Congress of Herpetology in Manaus, Brazil, on 21 August 2008 and supported by NSF IOS-0813842.

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Mori, A., Burghardt, G.M., Savitzky, A.H. et al. Nuchal glands: a novel defensive system in snakes. Chemoecology 22, 187–198 (2012). https://doi.org/10.1007/s00049-011-0086-2

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Keywords

  • Rhabdophis tigrinus
  • Bufo
  • Dietary sequestration
  • Antipredator behavior
  • Bufadienolide
  • Natricine snakes