Skip to main content
Log in

Comparative experimental tests of natricine antipredator displays, with special reference to the apparently unique displays in the Asian genus, Rhabdophis

  • Article
  • Published:
Journal of Ethology Aims and scope Submit manuscript

Abstract

Nuchal glands are unique organs known in only twelve Old World natricine species (three genera) including Rhabdophis tigrinus tigrinus. The glands of R. t. tigrinus contain a toxic secretion that may be derived from its toxic toad diet. A series of peculiar antipredator behaviors, for example neck arch, neck butt, and dorsal-facing posture, are exhibited by R. t. tigrinus, and a functional association between this behavior and the nuchal glands has been suggested. To investigate the ubiquitousness of these putatively unique displays among snakes, antipredator responses of 27 taxa of natricine snakes, both with and without nuchal glands, were studied using a common testing procedure. Three of four taxa with nuchal glands exhibited neck arch, neck butt, and dorsal-facing posture. None of the remaining 23 taxa, which do not possess the glands, showed neck arch and neck butt. Principal-components analysis indicated the association of the above three displays along with the behaviors termed neck flatten and head elevation, confirming the presence of a series of nuchal gland-related behaviors. These results support the assumption that the suite of peculiar displays is associated with the deterrent effects of the nuchal gland secretion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    CAS  Google Scholar 

  • Arnold SJ, Bennett AF (1984) Behavioural variation in natural populations III: antipredator displays in the garter snake Thamnophis radix. Anim Behav 32:1108–1118

    Article  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

    PubMed  CAS  Google Scholar 

  • Burghardt GM, Schwartz JM (1999) Geographic variations on methodological themes in comparative ethology: a natricine snake perspective. In: Foster SA, Endler JA (eds) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, Oxford, pp 69–94

    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 

  • Fukada H (1958) Embryological study on the integumental poison gland in the nuchal region of Natrix tigrina tigrina. Bull Kyoto Gakugei Univ Ser B 12:3–8 + 2 pls

    Google Scholar 

  • Fukada H (1961) Peculiar habits of the Japanese snake, Natrix t. tigrina (Boie). Bull Kyoto Gakugei Univ Ser B 18:13–16 + 2 pls

  • Greene HW (1988) Antipredator mechanisms in reptiles. In: Gans C, Huey RB (eds) Biology of the Reptilia, Ecology B. Defense and life history, vol 16. Alan Liss, New York, pp1–152

  • Herzog HA Jr, Bowers BB, Burghardt GM (1992) Development of antipredator responses in snakes: V. species differences in ontogenetic trajectories. Dev Psychobiol 25:199–211

    Article  PubMed  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)

  • 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 

  • Klauber LM (1972) Rattlesnakes. Their habits, life histories, and influence on mankind, 2nd edn. University of California Press, Berkeley

    Google Scholar 

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

    Google Scholar 

  • Maslin TP (1950) Snakes of the Kiukiang-Lushan area, Kiangsi, China. Proc Calif Acad Sci 4th Ser 26:419–466

    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) Thermal 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 (2004) Thermal effects on antipredator behaviour of snakes: a review and proposed terminology. Herpetol J 14:79–87

    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 

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

    Google Scholar 

  • Nakamura K (1935) On a new integumental poison gland found in the nuchal region of a snake, Natrix tigrina. Mem Coll Sci Kyoto Imp Univ Ser B 10:229–240 + 1 pl

  • Ota H, Chen SL, Lin JT, Toriba M (1999) Taxonomic status of the Taiwanese populations of Rhabdophis tigrinus (Squamata: Colubridae): morphological and karyological assessment. Jpn J Herpetol 18:1–6

    Google Scholar 

  • Paik NK, Yang SY (1986) Taxonomic study on two subspecies of European grass snake (Rhabdophis tigrina) in Korea. Korean J Syst Zool 2:79–92 (in Korean with English abstract)

    Google Scholar 

  • Passek KM, Gillingham JC (1997) Thermal influence on defensive behaviours of the eastern garter snake, Thamnophis sirtalis. Anim Behav 54:629–633

    Article  PubMed  Google Scholar 

  • Scudder RM, Burghardt GM (1983) A comparative study of defensive behavior in three sympatric species of water snakes (Nerodia). Z Tierpsychol 63:17–26

    Google Scholar 

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

    Google Scholar 

  • SPSS (2002) SPSS Professional StatisticsTM 11.0, SPSS, Chicago

  • 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 

  • Suzuki R (1960) Disturbance of the eye by snake venom (Natrix tigrina (Boie)). J Clin Ophthalmol 14:1384–1387 (in Japanese with English abstract)

    Google Scholar 

  • Tabachnick BG, Fidell LS (2001) Using multivariate statistics, 4th edn. Allyn and Bacon, Boston

    Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

We would like to thank P. Andreadis, S.-L. Chen, D. Cunningham, N. Ford, T. Hikida, T. Hirai, M. Honda, G. Martin, H. Ota, R. Patankar, S. Ryabov, T. Sugawara, M. Toda, and M. Waters for their kind help in obtaining snakes or providing facilities for testing. We also thank M. Toriba, J. Placyk, L. Almli, and R. Mehta for their comments on the manuscript and H. Ota for bibliographic assistance. Snakes were handled under Guidelines for Animal Experiments of Kyoto University and Protocol L202 of the University of Tennessee. The research was partially supported by a grant from the Japan–US Cooperative Science Program (1996–1998: Japan Society for the Promotion of Science (JSPS) awarded to AM and the National Science Foundation, INT-9513100 awarded to GMB). Data analysis and manuscript preparation were partially supported by a grant for the Joint Project for the Japan–US. Cooperative Science Program from JSPS (2004–2005) and by a grant for the Biodiversity Research of the 21st Century COE (A14).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akira Mori.

About this article

Cite this article

Mori, A., Burghardt, G.M. 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 (2008). https://doi.org/10.1007/s10164-006-0033-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10164-006-0033-9

Keywords

Navigation