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Nuchal glands: a novel defensive system in snakes

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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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References

  • 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 7:163–168

    Google Scholar 

  • Akizawa T (1986) Studies on the activities of chemicals in the nuchal glands of Rhabdophis tigrinus. Ochanomizu Med J 34:85–97 (in Japanese)

    CAS  Google Scholar 

  • Akizawa T, Yasuhara T, Kano R, Nakajima T (1985a) Novel polyhydroxylated cardiac steroids in the nuchal glands of the snake, Rhabdophis tigrinus. Biomed Res 6:437–441

    CAS  Google Scholar 

  • 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 

  • Alfaro ME, Arnold SJ (2001) Molecular systematics and evolution of Regina and the thamnophiine snakes. Mol Phylogenet Evol 21:408–423

    Article  PubMed  CAS  Google Scholar 

  • Ariga F (1953) A case of eye disturbance by Rhabdophis tigrinus. Jpn Rev Clinic Ophthalmol 47:258–259 (in Japanese)

    Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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 38:388–390

    Article  PubMed  CAS  Google Scholar 

  • Baker N, Lim K (2008) Wild animals of Singapore. Draco Publ Distr and Nature Soc, Singapore

    Google Scholar 

  • Bowers JH (1966) Food habits of the diamond-backed water snake, Natrix rhombifera rhombifera, in Bowie and Red River Counties, Texas. Herpetologica 22:225–229

    Google Scholar 

  • Broadley DG (1983) FitzSimons’ snakes of Southern Africa. Revised edn. Delta Books, Johannesburg

    Google Scholar 

  • Brodie ED III, Brodie ED Jr (1999) Costs of exploiting poisonous prey: evolutionary trade-offs in a predator-prey arms race. Evolution 53:626–631

    Article  Google Scholar 

  • Campden-Main SM (1970) A field guide to the snakes of South Vietnam. Division of reptiles and amphibians. US Nat Mus, Smithsonian Inst, Washington

    Google Scholar 

  • 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 Island

    Google Scholar 

  • Daniel JC (1983) The book of Indian reptiles. Bombay Nat Hist Soc, Bombay

    Google Scholar 

  • David P, Ineich I (1999) Les serpents venimeux du monde: systématique et répartition. Dumerilia, vol 3. Lab Reptilies Amphibiens Mus Natn Hist Nat Paris, Paris

    Google Scholar 

  • David P, Vogel G (1996) The snakes of Sumatra. An annotated checklist and key with natural history notes. Edition Chimaira, Frankfurt

    Google Scholar 

  • 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 22:315–329

    Article  PubMed  Google Scholar 

  • De Silva A (1990) Colour guide to the snakes of Sri Lanka. R & A Publishing, Avon

    Google Scholar 

  • Disi AM, Modry D, Necas P, Rifai L (2001) Amphibians and reptiles of the Hashemite Kingdom of Jordan. Edition Chimaira, Frankfurt

    Google Scholar 

  • Dobashi H (1935) Eye disturbance caused by a venomous snake. Central J Ophthalmol 27:1175–1176 (in Japanese)

    Google Scholar 

  • Ernst CH, Barbour RW (1989) Snakes of eastern North America. George Mason Univ Press, Fairfax

    Google Scholar 

  • 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 pls

  • 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 pls

  • Fukada H (1961) Peculiar habits of the Japanese snake, Natrix t. tigrina (Boie). Bull Kyoto Gakugei Univ Ser B No. 18:13–16, 2 pls

  • 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 1–152

    Google Scholar 

  • Gruber U (1989) Die Schlangen Europas und rund ums Mittelmeer. Kosmos, Stuttgart

    Google Scholar 

  • 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 31:108–113

    CAS  Google Scholar 

  • He QY, Yu XD, Liu JP (2007) Study on venom from nuchal glands of Rhabdophis tigrinus lateralis in China. Sichuan J Zool 26:255–257

    Google Scholar 

  • 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 

  • Hirai T (2004) Dietary shifts of frog eating snakes in response to seasonal changes in prey availability. J Herpetol 38:455–460

    Article  Google Scholar 

  • Hutchinson DA, Savitzky AH (2004) Vasculature of the parotoid glands of four species of toads (Bufonidae: Bufo). J Morphol 260:247–254

    Article  PubMed  Google Scholar 

  • 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 104:2265–2270

    Article  PubMed  CAS  Google Scholar 

  • Hutchinson DA, Savitzky AH, Mori A, Meinwald J, Schroeder FC (2008) Maternal provisioning of sequestered defensive steroids by the Asian snake Rhabdophis tigrinus. Chemoecology 18:181–190

    Article  CAS  Google Scholar 

  • 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

  • Jiang YF (2002) Observation on behaviors of Rhabdophis tigrinus lateralis. Sichuan J Zool 21:29–31 (in Chinese)

    Google Scholar 

  • 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 

  • 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 

  • Karsen SJ, Lau MW, Bogadek A (1986) Hong Kong amphibians and reptiles. Urban Council, Hong Kong

    Google Scholar 

  • 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 

  • Kawashima J (1957) Disturbance of the eye by snake venom (Natrix tigrina). Ganka Rinsho Iho 50:837–839 (in Japanese)

    Google Scholar 

  • Kawashima J (1959) Disturbance of the eye by snake venom (Natrix tigrina), II. Ganka Rinsho Iho 53:834–837 (in Japanese)

    Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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 

  • Kraus F, Brown WM (1998) Phylogenetic relationships of colubroid snakes based on mitochondrial DNA sequences. Zool J Linn Soc 122:455–487

    Article  Google Scholar 

  • 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 227–234

    Google Scholar 

  • 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 

  • Licht LE, Low B (1968) Cardiac response of snakes after ingestion of toad parotoid venom. Copeia 1968:547–551

    Article  Google Scholar 

  • Loveridge A (1958) Revision of five African snake genera. Bull Mus Comp Zool 119:1–198

    Google Scholar 

  • Lue KY, Tu MC, Hsiang G (1999) Atlas of Taiwan amphibians and reptiles. Nature Press, Taipei

    Google Scholar 

  • 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 81:228–236

    Article  Google Scholar 

  • Manthey U, Grossmann W (1997) Amphibien & Reptilien Südostasiens. Natur und Tier, Berlin

    Google Scholar 

  • Mao JJ, Chang HW (1999) Notes on nuchal gland anatomic of Rhabdophis tigrinus formosanus and Rhabdophis swinhonis (Natricinae: Squamata). J Nat Taiwan Mus 52:87–92

    Google Scholar 

  • Mori A (1997) A comparison of predatory behavior of newly hatched Rhabdophis tigrinus (Serpentes: Colubridae) on frogs and fish. Jpn J Herpetol 17:39–45

    Google Scholar 

  • Mori A (2006) Is headfirst ingestion essential in gape-limited predators? Prey-handling behavior of the anurophagous snake Rhabdophis tigrinus (Colubridae). Can J Zool 84:954–963

    Article  Google Scholar 

  • 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 114:408–413

    Article  PubMed  CAS  Google Scholar 

  • Mori A, Burghardt GM (2001) Temperature effects on anti-predator behaviour in Rhabdophis tigrinus, a snake with toxic nuchal glands. Ethology 107:795–811

    Article  Google Scholar 

  • 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 26:61–68

    Article  Google Scholar 

  • Mori A, Moriguchi H (1988) Food habits of the snakes in Japan: a critical review. Snake 20:98–113

    Google Scholar 

  • 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 275:47–56

    Article  Google Scholar 

  • 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 16:94–107

    Google Scholar 

  • 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 

  • Moriguchi H (1985) Body size differences between two populations of Rhabdophis tigrinus. Snake 17:140–143

    Google Scholar 

  • 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 

  • Moriguchi H, Naito S (1983) Tracing of distance of movement of Rhabdophis tigrinus (Boie) in a paddy field by mark-recapture method. Snake 15:14–15

    Google Scholar 

  • Moriguchi H, Toriba M (1985) Note on the number of eggs in oviduct of Rhabdophis tigrinus (Boie). Snake 17:144–147

    Google Scholar 

  • Mutoh A (1983) Death-feigning behavior of the Japanese colubrid snake Rhabdophis tigrinus. Herpetologica 39:78–80

    Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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 pl

    Google Scholar 

  • Nikol’skii AM (1964) Fauna of Russia and adjacent countries. Reptiles, vol II. Ophidia. Israel Prog Sci Trans, Jerusalem

  • 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 

  • Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17:1738–1747

    Article  Google Scholar 

  • Pope CH (1935) The reptiles of China. Turtles, crocodilians, snakes, lizards. Am Mus Nat Hist, New York

    Google Scholar 

  • Roberts KA (2000) An ultrastructural survey of the nuchal glands of Rhabdophis tigrinus (Serpentes: Colubridae). Unpublished master thesis, Old Dominion University

  • Rossman DA, Ford NB, Seigel RA (1996) The garter snakes. Evolution and ecology. Univ Oklahoma Press, Norman

    Google Scholar 

  • 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 

  • Schleich HH, Kästle W (eds) (2002) Amphibians and reptiles of Nepal. A R G Gantner, Ruggell

    Google Scholar 

  • 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 

  • 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) 25:714–730

    Article  CAS  Google Scholar 

  • Smith MA (1938) The nucho-dorsal glands of snakes. Proc Zool Soc Lond Ser B 100:575–583

    Google Scholar 

  • 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, London

    Google Scholar 

  • Smith HM, White FN (1955) Adrenal enlargement and its significance in the hognose snakes (Heterodon). Herpetologica 11:137–144

    Google Scholar 

  • Spaur RC, Smith HM (1971) Adrenal enlargement in the hognosed snake, Heterodon platyrhinos. J Herpetol 5:197–199

    Article  Google Scholar 

  • Spawls S, Howell K, Drewes R, Ashe J (2002) A field guide to the reptiles of east Africa. Academic Press, San Diego

    Google Scholar 

  • Steward JW (1971) The snakes of Europe. Fairleigh Dickinson Univ Press, Rutherford

    Google Scholar 

  • Stuebing RB, Inger RF (1999) A field guide to the snakes of Borneo. Nat Hist Publ (Borneo), Kota Kinabalu

  • Stuebing RB, Lian TF (2002) Notes on the fire-lipped keelback Rhabdophis murudensis (Smith 1925) (Ophidia: Colubridae: Natricinae) from northern Borneo. Raffles Bull Zool 50:227–230

    Google Scholar 

  • Sura P (1981) Captive breeding of Elaphe rufodorsata and Rhabdophis tigrinus from the Korean People’s Democratic Republic. Br Herpetol Soc Bull No. 3:20–24

    Google Scholar 

  • 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 

  • Tamura K (1940a) Eye disturbance caused by the secretions of a snake. Jpn Rev Clinic Ophthalmol 35:860–861 (in Japanese)

    Google Scholar 

  • Tamura K (1940b) Eye disturbance caused by the secretions of a snake II. Jpn Rev Clinic Ophthalmol 35:1191 (in Japanese)

    Google Scholar 

  • Tanaka K, Mori A (2000) Literature survey on predators of snakes in Japan. Curr Herpetol 19:97–111

    Article  Google Scholar 

  • Taylor EH (1965) The serpents of Thailand and adjacent waters. Univ Kansas Sci Bull 45:609–1096

    Google Scholar 

  • Tweedie MWF (1983) The snakes of Malaya, 3rd edn. Singapore Natn Printer, Singapore

    Google Scholar 

  • Vidal N, Hedges SB (2002) Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. C R Biol 325:987–995

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Whitaker R, Captain A (2004) Snakes of India, the field guide. Draco Books, Chennai

    Google Scholar 

  • 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 59:155–163

    Article  Google Scholar 

  • 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 

  • Zhao EM (1997) A new species of Rhabdophis (Serpentes: Colubridae) from Hainan Island, China. Asiatic Herpetol Res 7:166–169

    Google Scholar 

  • Zhao E, Meihua H, Yu Z (1998) Fauna Sinica, Reptilia, vol 3. Squamata, Serpentes. Science Press, Beijing (in Chinese)

    Google Scholar 

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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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