Journal of Chemical Ecology

, Volume 34, Issue 3, pp 398–407 | Cite as

Potential Chemosignals in the Anogenital Gland Secretion of Giant Pandas, Ailuropoda melanoleuca, Associated with Sex and Individual Identity

  • Jian-Xu Zhang
  • Dingzhen Liu
  • Lixing Sun
  • Rongping Wei
  • Guiquan Zhang
  • Honglin Wu
  • Hemin Zhang
  • Chenghua Zhao


With a combination of dichloromethane extraction and analysis by gas chromatography–mass spectrometry (GC-MS), we found 39 compounds (corresponding to 38 GC peaks) in the anogenital gland secretion (AGS) of captive adult giant pandas, Ailuropoda melanoleuca, during the non-mating season. In addition to indole, squalene, and some of the straight-chain fatty acids that had been characterized previously from the AGS of giant pandas, we identified several new compounds such as decenal, two isomers of decadienal, phenylacetic acid, 5-methylhydantoin, hydroquinone, phenylpropanoic acid, and erucic acid. Quantitative comparison of the relative abundances of the 20 main GC peaks revealed that 5-methylhydantoin, indole, and erucic acid are putative female pheromones, whereas squalene and hydroquinone are putative male pheromones. In addition to the presence of a few individual-specific compounds, the relative abundances of most of the 21 constituents varied more among individuals than within individuals. This suggests that individual identity might be coded in both digital and analog form. The chemical composition of different AGS samples from the same pandas consistently displayed a minimum cluster distance, much smaller than that between samples from different individuals in a hierarchical linkage cluster (average linkage) dendrogram. Our results indicate that the AGS might contain an “odor fingerprint.” Although putative sex pheromones such as squalene and erucic acid should be assessed further by bioassay, our study suggests that synthetic chemosignals might be useful in modulating the behavior and physiology of giant pandas.


Ailuropoda melanoleuca Anogenital gland secretions (AGS) Giant panda Individuality Pheromone Sex Sex specificity 



We are grateful to Dr. Steven J Seybold and the anonymous reviewers who gave us many helpful suggestions and comments. This work was supported by grants from NSFC (Nos. 30470233 and 30670268); International Cooperative Giant Panda Projects of State Forestry Administration, China (nos. WH0306 and WH0309) and International Partnership Project of Innovative Research, Chinese Academy of Science (CXTDS2005-4).


  1. Agilent Technologies 2002. Mass Spectral Libraries, NIST. Palo Alto, CA, USA.Google Scholar
  2. Andersen, K. F., and Vulpius, T. 1999. Urinary volatile constituents of the lion, Panthera leo. Chem. Senses 24:179–189.PubMedCrossRefGoogle Scholar
  3. Brown, R. E., and MacDonald, D. W. 1985. Social Odours in Mammals. Oxford University Press, Oxford, UK.Google Scholar
  4. Clapperton, B. K., Minot, E. O., and Crump, D. R. 1988. An olfactory recognition system in the ferret Mustela furo L. (Carnivora: Mustelidae). Anim. Behav. 36:541–553.CrossRefGoogle Scholar
  5. El-Sayed, A. M. 2005. The Pherobase: Database of insect pheromones and semiochemicals. <>.
  6. Epple, G., Golob, N. F., and Smith, A. B. I. 1979. Odor communication in the tamarin Saguinus fuscicollis (Callitrichidae): Behavioral and chemical studies, pp. 117–130, in F. J. Ritter (ed.). Chemical Ecology: Odour Communication in Animals. Elsevier, Amsterdam.Google Scholar
  7. Ferkin, M. H., Sorokin, E. S., Johnston, R. E., and Lee, C. J. 1997. Attractiveness of scents varies with protein content of the diet in meadow voles. Anim. Behav. 53:133–141.CrossRefGoogle Scholar
  8. Gassett, J. W., Wiesler, D. P., Baker, A. G., Osborn, D. A., Miller, K. V., Marchinton, R. L., and Novotny, M. 1996. Volatile compounds from interdigital gland of male white-tailed deer (Odocoileus virginianus). J. Chem. Ecol. 22:1689–1696.CrossRefGoogle Scholar
  9. Gosden, P. E., and Ware, G. C. 1976. The aerobic flora of the anal sac of the red fox (Vulpes vulpes). J. Appl. Bacteriol. 41:271–275.PubMedGoogle Scholar
  10. Hagey, L., and Macdonald, E. 2003. Chemical cues identify gender and individuality in giant pandas (Ailuropoda melanoleuca). J. Chem. Ecol. 29:1479–1488.PubMedCrossRefGoogle Scholar
  11. Liu, D., Fang, J., Sun, R., Zhang, G., Wei, R., and Zhang, H. 1998. Behavioral comparison in individuals of different sexual ability in giant panda (Ailuropoda melanoleuca). Acta Zool. Sin. 44:27–34.Google Scholar
  12. Liu, D., Zhang, G., Wei, R., Zhang, H., Fang, J., and Sun, R. 2002. The effects of sex and age on the behavior of captive giant pandas (Ailuropoda melanoleuca). Acta Zool. Sin. 48:585–590.Google Scholar
  13. Liu, D., Wang, Z. P., Tian, H., Yu, C. Q., Zhang, G. Q., Wei, R. P., and Zhang, H. M. 2003. Behavior of giant pandas (Ailuropoda melanoleuca) in captive conditions: Gender differences and enclosure effects. Zoo Biol. 22:77–82.CrossRefGoogle Scholar
  14. Liu, D., Zhang, G., Wei, R., Zhang, H., Fang, J., and Sun, R. 2005. Behavioral responsiveness of captive giant pandas (Ailuropoda melanoleuca) to substrate odors from conspecifics of the opposite sex, pp. 101–109, in R. T. Mason, M. P. LeMaster, and D. Müller-Schwarze (eds.). Chemical Signals in Vertebrates 10Springer, New York.CrossRefGoogle Scholar
  15. Liu, D., Yuan, H., Tian, H., Wei, R. P., Zhang, G. Q., Sun, L., and Sun, R. Y. 2006. Do the anogenital gland secretions of giant panda code for their sexual ability? Chin. Sci. Bull. 51:1986–1995.CrossRefGoogle Scholar
  16. Mason, R. T., Fales, H. M., Jones, T. H., Pannell, L. K., Chinn, J. W., and Crews, D. 1989. Sex pheromones in snakes. Science 245:290–293.PubMedCrossRefGoogle Scholar
  17. Mason, R. T., and Gutzke, W. H. N. 1990. Sex recognition in the leopard gecko, Eublepharis macularius (Sauria: Gekkonidae): Possible mediation by skin-derived semiochemicals. J. Chem. Ecol. 16:27–36.CrossRefGoogle Scholar
  18. Novotny, M., Ma, W., Zidek, L., and Daev, E. 1999. Recent biochemical insights into puberty acceleration, estrus induction, and puberty delay in the house mouse, pp. 99–116, in R. E. Johnston, D. Müller-Schwarze, and P. W. Sorensen (eds.). Advances in Chemical Signals in Vertebrates. Kluwer, New York.Google Scholar
  19. Schaller, G. B., Hu, J., Pan, W., and Zhu, J. 1985. The Giant Pandas of Wolong. University of Chicago Press, Chicago, IL.Google Scholar
  20. Singer, A. G., Beauchamp, G. K., and Yamazaki, K. 1997. Volatile signals of the major histocompatibility complex in male mouse urine. Proc. Natl. Acad. Sci. U. S. A. 94:2210–2214.PubMedCrossRefGoogle Scholar
  21. SPSS Inc. 1999. SPSS for Windows. Release 10.0.1. Chicago, IL.Google Scholar
  22. Sun, L., and Müller-Schwarze, D. 1998a. Anal gland secretion codes for family membership in the beaver. Behav. Ecol. Sociobiol. 44:199–208.CrossRefGoogle Scholar
  23. Sun, L., and Müller-Schwarze, D. 1998b. Anal gland secretion codes for relatedness in the beaver, Castor canadensis. Ethology 104:917–927.CrossRefGoogle Scholar
  24. Swaisgood, R. R., Lindburg, D. G., and Zhou, X. 1999. Giant pandas discriminate individual differences in conspecific scent. Anim. Behav. 57:1045–1053.PubMedCrossRefGoogle Scholar
  25. Swaisgood, R. R., Lindburg, D. G., and Owen, M. A. 2000. The effects of sex, reproductive condition and context on discrimination of conspecific odours by giant pandas. Anim. Behav. 60:227–237.PubMedCrossRefGoogle Scholar
  26. Tian, H., Wei, R. P., Zhang, G. Q., Sun, R. Y., and Liu, D. Z. 2007. Age differences in behavioral responses of male giant pandas to chemosensory stimulation. Zoological Research 28:134–140.Google Scholar
  27. White, A. M., Swaisgood, R. R., and Zhang, H. 2002. The highs and lows of chemical communication in giant pandas (Ailuropoda melanoleuca): Effect of scent deposition height on signal discrimination. Behav. Ecol. Sociobiol. 51:519–529.CrossRefGoogle Scholar
  28. White, A. M., Swaisgood, R. R., and Zhang, H. 2003. Chemical communication in the giant panda (Ailuropoda melanoleuca): The role of age in the signaller and assessor. J. Zool. Lond. 259:171–178.CrossRefGoogle Scholar
  29. White, A. M., Swaisgood, R. R., and Zhang, H. 2004. Urinary chemosignals in giant pandas (Ailuropoda melanoleuca): Seasonal and developmental effects on signal discrimination. J. Zool. Lond. 264:231–238.CrossRefGoogle Scholar
  30. Xie, Z., and Gipps, J. 2005. The International Studbook for Giant Panda (Ailuropoda melanoleuca). Chinese Association of Zoological Gardens, Beijing.Google Scholar
  31. Yuan, H., Liu, D., Sun, L., Wei, R. P., Zhang, G. Q., and Sun, R. Y. 2004. Anogenital gland secretions code for sex and age in the giant panda, Ailuropoda melanoleuca. Can. J. Zool. 82:1596–1604.CrossRefGoogle Scholar
  32. Zhan, X. J., Li, M., Zhang, Z. J., Goossens, B., Chen, Y. P., Wang, H. J., Bruford, M. W., and Wei, F. W. 2006. Molecular censusing doubles giant panda population estimate in a key nature reserve. Curr. Biol. 16:R451–R452.PubMedCrossRefGoogle Scholar
  33. Zhang, J. X., Ni, J., Ren, X. J., Sun, L. X., Zhang, Z. B., and Wang, Z. W. 2003. Possible coding for recognition of sexes, individuals and species in anal gland volatiles of Mustela eversmanni and M. sibirica. Chem. Senses 28:381–388.PubMedCrossRefGoogle Scholar
  34. Zhang, J. X., Soini, H. A., Bruce, K. E., Wiesler, D., Woodley, S. K., Baum, M. J., and Novotny, M. V. 2005. Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem. Senses 30:727–737.PubMedCrossRefGoogle Scholar
  35. Zhang, J. X., Rao, X. P., Sun, L., Zhao, C., and Qin, X. 2007a. Putative chemical signals about sex, individuality and genetic background in the preputial gland and urine of the house mouse (Mus musculus). Chem. Senses 32:293–303.PubMedCrossRefGoogle Scholar
  36. Zhang, J. X., Rao, X. P., Zhao, C., Liu, X., and Qin, X. 2007b. Possible information about gender and individual recognition coded by insect pheromone analogs in the preputial glands in male Brandt’s voles, Lasiopodomys brandtii. Acta Zool. Sin. 53:616–624.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Jian-Xu Zhang
    • 1
  • Dingzhen Liu
    • 2
  • Lixing Sun
    • 3
  • Rongping Wei
    • 4
  • Guiquan Zhang
    • 4
  • Honglin Wu
    • 4
  • Hemin Zhang
    • 4
  • Chenghua Zhao
    • 1
  1. 1.State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Institute of ZoologyChinese Academy of SciencesBeijingChina
  2. 2.MOE, Key Laboratory of Biodiversity Science and Ecological Engineering, Institute of EcologyBeijing Normal UniversityBeijingChina
  3. 3.Department of Biological SciencesCentral Washington UniversityEllensburgUSA
  4. 4.Key Laboratory for Reproduction and Conservation Genetics of Endangered Wildlife of Sichuan ProvinceChina Conservation and Research Center for the Giant PandaWolongChina

Personalised recommendations