, Volume 22, Issue 3, pp 187–198 | Cite as

Nuchal glands: a novel defensive system in snakes

  • Akira MoriEmail author
  • Gordon M. Burghardt
  • Alan H. Savitzky
  • Kathleen A. Roberts
  • Deborah A. Hutchinson
  • Richard C. Goris


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.


Rhabdophis tigrinus Bufo Dietary sequestration Antipredator behavior Bufadienolide Natricine snakes 



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.


  1. Akani GC, Luiselli L (1999/2000) Aspects of the natural history of Natriciteres (Serpentes, Colubridae) in Nigeria, with special reference to N. variegata and N. fuliginoides. Herpetol Nat Hist 7:163–168Google Scholar
  2. Akizawa T (1986) Studies on the activities of chemicals in the nuchal glands of Rhabdophis tigrinus. Ochanomizu Med J 34:85–97 (in Japanese)Google Scholar
  3. Akizawa T, Yasuhara T, Kano R, Nakajima T (1985a) Novel polyhydroxylated cardiac steroids in the nuchal glands of the snake, Rhabdophis tigrinus. Biomed Res 6:437–441Google Scholar
  4. Akizawa T, Yasuhara T, Azuma H, Nakajima T (1985b) Chemical structures and biological activities of bufadienolides in the nucho-dorsal glands of Japanese snake, Rhabdophis tigrinus. J Pharmacobio Dyn 8:s–60 (abstract)Google Scholar
  5. Alfaro ME, Arnold SJ (2001) Molecular systematics and evolution of Regina and the thamnophiine snakes. Mol Phylogenet Evol 21:408–423PubMedCrossRefGoogle Scholar
  6. Ariga F (1953) A case of eye disturbance by Rhabdophis tigrinus. Jpn Rev Clinic Ophthalmol 47:258–259 (in Japanese)Google Scholar
  7. Asahi H, Kohtari Y, Chiba K, Mishima A (1985) Effect of the nuchodorsal gland venom of the Yamakagashi snake on the eye. Folia Ophthalmol Japonica 36:379–383 (in Japanese with English abstract)Google Scholar
  8. Azuma H, Sekizaki S, Akizawa T, Yasuhara T, Nakajima T (1986) Activities of novel polyhydroxylated cardiotonic steroids purified from nuchal glands of the snake, Rhabdophis tigrinus. J Pharm Pharmacol 38:388–390PubMedCrossRefGoogle Scholar
  9. Baker N, Lim K (2008) Wild animals of Singapore. Draco Publ Distr and Nature Soc, SingaporeGoogle Scholar
  10. Bowers JH (1966) Food habits of the diamond-backed water snake, Natrix rhombifera rhombifera, in Bowie and Red River Counties, Texas. Herpetologica 22:225–229Google Scholar
  11. Broadley DG (1983) FitzSimons’ snakes of Southern Africa. Revised edn. Delta Books, JohannesburgGoogle Scholar
  12. Brodie ED III, Brodie ED Jr (1999) Costs of exploiting poisonous prey: evolutionary trade-offs in a predator-prey arms race. Evolution 53:626–631CrossRefGoogle Scholar
  13. Campden-Main SM (1970) A field guide to the snakes of South Vietnam. Division of reptiles and amphibians. US Nat Mus, Smithsonian Inst, WashingtonGoogle Scholar
  14. Cox MJ, van Dijk PP, Nabhitabhata J, Thirakhupt K (1998) A photographic guide to snakes and other reptiles of Peninsular Malaysia, Singapore and Thailand. Ralph Curtis Books, Sanibel IslandGoogle Scholar
  15. Daniel JC (1983) The book of Indian reptiles. Bombay Nat Hist Soc, BombayGoogle Scholar
  16. David P, Ineich I (1999) Les serpents venimeux du monde: systématique et répartition. Dumerilia, vol 3. Lab Reptilies Amphibiens Mus Natn Hist Nat Paris, ParisGoogle Scholar
  17. David P, Vogel G (1996) The snakes of Sumatra. An annotated checklist and key with natural history notes. Edition Chimaira, FrankfurtGoogle Scholar
  18. de Queiroz A, Lawson R, Lemos-Espinal JA (2002) Phylogenetic relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: How much DNA sequence is enough? Mol Phylogenet Evol 22:315–329PubMedCrossRefGoogle Scholar
  19. De Silva A (1990) Colour guide to the snakes of Sri Lanka. R & A Publishing, AvonGoogle Scholar
  20. Disi AM, Modry D, Necas P, Rifai L (2001) Amphibians and reptiles of the Hashemite Kingdom of Jordan. Edition Chimaira, FrankfurtGoogle Scholar
  21. Dobashi H (1935) Eye disturbance caused by a venomous snake. Central J Ophthalmol 27:1175–1176 (in Japanese)Google Scholar
  22. Ernst CH, Barbour RW (1989) Snakes of eastern North America. George Mason Univ Press, FairfaxGoogle Scholar
  23. Fukada H (1958) Embryological study on the integumental poison gland in the nuchal region of Natrix tigrina tigrina. Bull Kyoto Gakugei Univ Ser B No. 12:3–8, 2 plsGoogle Scholar
  24. Fukada H (1959) Biological studies on the snakes. VI. Growth and maturity of Natrix tigrina tigrina (Boie). Bull Kyoto Gakugei Univ Ser B No. 15:25–41, 2 plsGoogle Scholar
  25. Fukada H (1961) Peculiar habits of the Japanese snake, Natrix t. tigrina (Boie). Bull Kyoto Gakugei Univ Ser B No. 18:13–16, 2 plsGoogle Scholar
  26. Greene HW (1988) Antipredator mechanisms in reptiles. In: Gans C, Huey RB (eds) Biology of the Reptilia, vol 16. Ecology B. Defense and life history. Alan R Liss Inc, New York, pp 1–152Google Scholar
  27. Gruber U (1989) Die Schlangen Europas und rund ums Mittelmeer. Kosmos, StuttgartGoogle Scholar
  28. He QY, Yu XD (2008) Isolation and identification of a metalloproteinase RT-2 from nuchal gland venom of Rhabdophis tigrinus lateralis. Shanxi Daxue Xuebao Ziran Kexue Ban 31:108–113Google Scholar
  29. He QY, Yu XD, Liu JP (2007) Study on venom from nuchal glands of Rhabdophis tigrinus lateralis in China. Sichuan J Zool 26:255–257Google Scholar
  30. Hikita A (1947) A case of eye disturbance caused by the secretions of Rhabdophis tigrinus. Jpn Rev Clinic Ophthalmol 41:207–208 (in Japanese)Google Scholar
  31. Hirai T (2004) Dietary shifts of frog eating snakes in response to seasonal changes in prey availability. J Herpetol 38:455–460CrossRefGoogle Scholar
  32. Hutchinson DA, Savitzky AH (2004) Vasculature of the parotoid glands of four species of toads (Bufonidae: Bufo). J Morphol 260:247–254PubMedCrossRefGoogle Scholar
  33. Hutchinson DA, Mori A, Savitzky AH, Burghardt GM, Wu X, Meinwald J, Schroeder FC (2007) Dietary sequestration of defensive steroids in nuchal glands of the Asian snake Rhabdophis tigrinus. Proc Natl Acad Sci 104:2265–2270PubMedCrossRefGoogle Scholar
  34. Hutchinson DA, Savitzky AH, Mori A, Meinwald J, Schroeder FC (2008) Maternal provisioning of sequestered defensive steroids by the Asian snake Rhabdophis tigrinus. Chemoecology 18:181–190CrossRefGoogle Scholar
  35. Hutchinson DA, Savitzky AH, Mori A, Burghardt GM, Meinwald J, Schroeder FC (2011) Chemical investigations of defensive steroid sequestration by the Asian snake Rhabdophis tigrinus. Chemoecology. doi: 10.1007/s00049-011-0078-2
  36. Jiang YF (2002) Observation on behaviors of Rhabdophis tigrinus lateralis. Sichuan J Zool 21:29–31 (in Chinese)Google Scholar
  37. Jiang Y, Zhao E (1983) Studies on amphibians and reptiles of Mt. Gongga region, Sichuan, China. 3. A study of species-group nuchalis, genus Rhabdophis. Acta Herpetol Sinica 2:59–62 (in Chinese with English abstract)Google Scholar
  38. Kadowaki S (1992) Food resource overlap between the two sympatric Japanese snakes (Elaphe quadrivirgata and Rhabdophis tigrinus) in the paddy fields. Jpn J Ecol 42:1–7 (in Japanese with English Synopsis)Google Scholar
  39. Karsen SJ, Lau MW, Bogadek A (1986) Hong Kong amphibians and reptiles. Urban Council, Hong KongGoogle Scholar
  40. Kawamoto F, Kumada N (1989) A case report of eye-injury caused by cervical gland venom of a snake, Rhabdophis tigrinus (Boie). Jpn J Sanitary Zool 40:211–212 (in Japanese with English abstract)Google Scholar
  41. Kawashima J (1957) Disturbance of the eye by snake venom (Natrix tigrina). Ganka Rinsho Iho 50:837–839 (in Japanese)Google Scholar
  42. Kawashima J (1959) Disturbance of the eye by snake venom (Natrix tigrina), II. Ganka Rinsho Iho 53:834–837 (in Japanese)Google Scholar
  43. Kitazume Y (1953) On the increasing action of nuchal gland inclusions of the snake, Natrix tigrina, upon the blood pressure of the rabbit. Zool Mag 62:225–227 (in Japanese with English abstract)Google Scholar
  44. Kitazume Y (1958) Further studies on the effect of the nuchal gland substance of Natrix tigrina upon the blood pressure of some animals. Zool Mag 67:111–115 (in Japanese with English abstract)Google Scholar
  45. Kraus F, Brown WM (1998) Phylogenetic relationships of colubroid snakes based on mitochondrial DNA sequences. Zool J Linn Soc 122:455–487CrossRefGoogle Scholar
  46. Lawson R (1986) Molecular systematics of some Old World natricine snakes. In: Rocek Z (ed) Studies in herpetology, Proc Eur Herpetol Meeting Prague 1985. Charles Univ, Prague, pp 227–234Google Scholar
  47. Lee WJ, Lue KY (1996) The preliminary study on the food habits of snakes in Taiwan. Biol Bull Nat Taiwan Normal Univ 31:119–124 (in Chinese with English abstract)Google Scholar
  48. Licht LE, Low B (1968) Cardiac response of snakes after ingestion of toad parotoid venom. Copeia 1968:547–551CrossRefGoogle Scholar
  49. Loveridge A (1958) Revision of five African snake genera. Bull Mus Comp Zool 119:1–198Google Scholar
  50. Lue KY, Tu MC, Hsiang G (1999) Atlas of Taiwan amphibians and reptiles. Nature Press, TaipeiGoogle Scholar
  51. Luiselli L (2003) Do snakes exhibit shifts in feeding ecology associated with the presence or absence of potential competitors? A case study from tropical Africa. Can J Zool 81:228–236CrossRefGoogle Scholar
  52. Manthey U, Grossmann W (1997) Amphibien & Reptilien Südostasiens. Natur und Tier, BerlinGoogle Scholar
  53. Mao JJ, Chang HW (1999) Notes on nuchal gland anatomic of Rhabdophis tigrinus formosanus and Rhabdophis swinhonis (Natricinae: Squamata). J Nat Taiwan Mus 52:87–92Google Scholar
  54. Mori A (1997) A comparison of predatory behavior of newly hatched Rhabdophis tigrinus (Serpentes: Colubridae) on frogs and fish. Jpn J Herpetol 17:39–45Google Scholar
  55. Mori A (2006) Is headfirst ingestion essential in gape-limited predators? Prey-handling behavior of the anurophagous snake Rhabdophis tigrinus (Colubridae). Can J Zool 84:954–963CrossRefGoogle Scholar
  56. Mori A, Burghardt GM (2000) Does prey matter? Geographic variation in antipredator responses of hatchlings of a Japanese natricine snake, Rhabdophis tigrinus. J Comp Psychol 114:408–413PubMedCrossRefGoogle Scholar
  57. Mori A, Burghardt GM (2001) Temperature effects on anti-predator behaviour in Rhabdophis tigrinus, a snake with toxic nuchal glands. Ethology 107:795–811CrossRefGoogle Scholar
  58. Mori A, Burghardt GM (2008) Comparative experimental tests of natricine antipredator displays, with special reference to the apparently unique displays in the Asian genus, Rhabdophis. J Ethol 26:61–68CrossRefGoogle Scholar
  59. Mori A, Moriguchi H (1988) Food habits of the snakes in Japan: a critical review. Snake 20:98–113Google Scholar
  60. Mori A, Vincent SE (2008) An integrative approach to specialization: relationships among feeding morphology, mechanics, behaviour, performance and diet in two syntopic snakes. J Zool Lond 275:47–56CrossRefGoogle Scholar
  61. Mori A, Layne D, Burghardt GM (1996) Description and preliminary analysis of antipredator behavior of Rhabdophis tigrinus tigrinus, a colubrid snake with nuchal glands. Jpn J Herpetol 16:94–107Google Scholar
  62. Mori A, Konishi E, Izumi T (2009) A putative predatory attempt by Meles meles on Rhabdophis tigrinus and a possible aversive function of the nuchal glands. Bull Herpetol Soc Japan 2009:18–20 (in Japanese)Google Scholar
  63. Moriguchi H (1985) Body size differences between two populations of Rhabdophis tigrinus. Snake 17:140–143Google Scholar
  64. Moriguchi H, Naito S (1982) Activities and food habits of Amphiesma vibakari (Boie) and Rhabdophis tigrinus (Boie). Snake 14:136–142 (in Japanese with English abstract)Google Scholar
  65. Moriguchi H, Naito S (1983) Tracing of distance of movement of Rhabdophis tigrinus (Boie) in a paddy field by mark-recapture method. Snake 15:14–15Google Scholar
  66. Moriguchi H, Toriba M (1985) Note on the number of eggs in oviduct of Rhabdophis tigrinus (Boie). Snake 17:144–147Google Scholar
  67. Mutoh A (1983) Death-feigning behavior of the Japanese colubrid snake Rhabdophis tigrinus. Herpetologica 39:78–80Google Scholar
  68. Nakai T (1953) Some actions of the secretion of the integumental poison glands of Natrix tigrina on the white mouse. Zool Mag 62:27–30 (in Japanese with English abstract)Google Scholar
  69. Nakamura K (1935) On a new integumental poison gland found in the nuchal region of a snake, Natrix tigrina. Mem College Sci Kyoto Imperial Univ Ser B 10:229–240, 1 plGoogle Scholar
  70. Nikol’skii AM (1964) Fauna of Russia and adjacent countries. Reptiles, vol II. Ophidia. Israel Prog Sci Trans, JerusalemGoogle Scholar
  71. Ogawa H, Ohasi D, Iritani I, Kisimoto H, Nakamura Y, Oda M, Tuduki H, Suzuki M (1992) Eye disturbance caused by nuchodorsal gland venom from a Yamakagashi (Rhabdophis tigrinus): 16th case report in Japan. Jpn J Toxicol 5:169–172 (in Japanese with English abstract)Google Scholar
  72. Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17:1738–1747CrossRefGoogle Scholar
  73. Pope CH (1935) The reptiles of China. Turtles, crocodilians, snakes, lizards. Am Mus Nat Hist, New YorkGoogle Scholar
  74. Roberts KA (2000) An ultrastructural survey of the nuchal glands of Rhabdophis tigrinus (Serpentes: Colubridae). Unpublished master thesis, Old Dominion UniversityGoogle Scholar
  75. Rossman DA, Ford NB, Seigel RA (1996) The garter snakes. Evolution and ecology. Univ Oklahoma Press, NormanGoogle Scholar
  76. Saitoh T (1949) Right eye disturbance caused by the secretions of Rhabdophis tigrinus and left eye disturbance by undiluted nitric acid. Jpn Rev Clinic Ophthalmol 43:336 (in Japanese)Google Scholar
  77. Schleich HH, Kästle W (eds) (2002) Amphibians and reptiles of Nepal. A R G Gantner, RuggellGoogle Scholar
  78. Shibuya H (1923) A case of corneitis caused by the skin secretions of a snake. Jpn Rev Clinic Ophthalmol 18:368–369 (in Japanese)Google Scholar
  79. Shimada K, Fujii Y, Yamashita E, Niizaki Y, Sato Y, Nambara T (1977) Studies on cardiotonic steroids from the skin of Japanese toad. Chem Pharm Bull (Tokyo) 25:714–730CrossRefGoogle Scholar
  80. Smith MA (1938) The nucho-dorsal glands of snakes. Proc Zool Soc Lond Ser B 100:575–583Google Scholar
  81. Smith MA (1943) The fauna of British India. Ceylon and Burma, including the whole of the Indo-Chinese sub-region. Reptilia and amphibia, vol III. Serpentes. Taylor and Francis, LondonGoogle Scholar
  82. Smith HM, White FN (1955) Adrenal enlargement and its significance in the hognose snakes (Heterodon). Herpetologica 11:137–144Google Scholar
  83. Spaur RC, Smith HM (1971) Adrenal enlargement in the hognosed snake, Heterodon platyrhinos. J Herpetol 5:197–199CrossRefGoogle Scholar
  84. Spawls S, Howell K, Drewes R, Ashe J (2002) A field guide to the reptiles of east Africa. Academic Press, San DiegoGoogle Scholar
  85. Steward JW (1971) The snakes of Europe. Fairleigh Dickinson Univ Press, RutherfordGoogle Scholar
  86. Stuebing RB, Inger RF (1999) A field guide to the snakes of Borneo. Nat Hist Publ (Borneo), Kota KinabaluGoogle Scholar
  87. Stuebing RB, Lian TF (2002) Notes on the fire-lipped keelback Rhabdophis murudensis (Smith 1925) (Ophidia: Colubridae: Natricinae) from northern Borneo. Raffles Bull Zool 50:227–230Google Scholar
  88. Sura P (1981) Captive breeding of Elaphe rufodorsata and Rhabdophis tigrinus from the Korean People’s Democratic Republic. Br Herpetol Soc Bull No. 3:20–24Google Scholar
  89. Suzuki R (1960) Disturbance of the eye by snake venom (Natrix tigrina (Boie)). J Clinic Ophthalmol 14:1384–1387 (in Japanese with English abstract)Google Scholar
  90. Tamura K (1940a) Eye disturbance caused by the secretions of a snake. Jpn Rev Clinic Ophthalmol 35:860–861 (in Japanese)Google Scholar
  91. Tamura K (1940b) Eye disturbance caused by the secretions of a snake II. Jpn Rev Clinic Ophthalmol 35:1191 (in Japanese)Google Scholar
  92. Tanaka K, Mori A (2000) Literature survey on predators of snakes in Japan. Curr Herpetol 19:97–111CrossRefGoogle Scholar
  93. Taylor EH (1965) The serpents of Thailand and adjacent waters. Univ Kansas Sci Bull 45:609–1096Google Scholar
  94. Tweedie MWF (1983) The snakes of Malaya, 3rd edn. Singapore Natn Printer, SingaporeGoogle Scholar
  95. Vidal N, Hedges SB (2002) Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. C R Biol 325:987–995PubMedCrossRefGoogle Scholar
  96. Watanabe S, Tsuneto S, Matsumoto Y (1988) Colubridae snake: Japanese Yamakagashi (Rhabdophis tigrinus tigrinus). Jpn J Acute Med 12:441–450 (in Japanese)Google Scholar
  97. Whitaker R, Captain A (2004) Snakes of India, the field guide. Draco Books, ChennaiGoogle Scholar
  98. Williams BL, Brodie ED Jr, Brodie ED III (2003) Coevolution of deadly toxins and predator resistance: self-assessment of resistance by garter snakes leads to behavioral rejection of toxic newt prey. Herpetologica 59:155–163CrossRefGoogle Scholar
  99. Zhao EM (1995) Taxonomic status of some snake species and subspecies. J Shuzhou Railw Teach Coll 12:36–39 (in Chinese with English summary)Google Scholar
  100. Zhao EM (1997) A new species of Rhabdophis (Serpentes: Colubridae) from Hainan Island, China. Asiatic Herpetol Res 7:166–169Google Scholar
  101. Zhao E, Meihua H, Yu Z (1998) Fauna Sinica, Reptilia, vol 3. Squamata, Serpentes. Science Press, Beijing (in Chinese)Google Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Akira Mori
    • 1
    Email author
  • Gordon M. Burghardt
    • 2
  • Alan H. Savitzky
    • 3
  • Kathleen A. Roberts
    • 3
    • 5
  • Deborah A. Hutchinson
    • 3
    • 6
  • Richard C. Goris
    • 4
  1. 1.Department of Zoology, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.Departments of Psychology and Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA
  3. 3.Department of Biological SciencesOld Dominion UniversityNorfolkUSA
  4. 4.KawasakiJapan
  5. 5.Department of Natural Resources and Environmental SciencesAlabama A & M UniversityNormalUSA
  6. 6.Department of BiologyCoastal Carolina UniversityConwayUSA

Personalised recommendations