Do Urinary Chemosignals Code for Sex, Age, and Season in the Giant Panda, Ailuropoda melanoleuca?

  • Dingzhen Liu
  • Hong Yuan
  • Zhipeng Wang
  • Rongping Wei
  • Guiquan Zhang
  • Lixing Sun


The urinary volatile compounds of captive giant pandas, Ailuropoda melanoleuca, were analysed with GC-MS (gas chromatography and mass spectrometry). Samples were collected from adult males and females during the mating season, as well as from adult and sub-adult males during the non-mating season. We detected more than 96 compounds, 50 of which were common to all individuals. The major volatile constituents were ketones, phenols, alcohols, and fatty acids. No single compound was found to be specific for characterising sex, age, and season. MANOVA analysis on the relative abundance of compounds showed that adult males and females differ in four urinary compounds in the mating season and adult males differ in seven compounds between the mating and the non-mating seasons. We also found significant age effects on the relative abundance of urinary compounds in males in the non-mating season. This result suggests that those compounds might be the potential chemosignals signalling information about male pandas’ age, sex, and reproductive state.


Giant Panda Mating Season Deer Mouse Asian Elephant MANOVA Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to Professors Helin Luan and Wen Yao for their help in GC-MS analysis. We also thank the staff at the China Conservation and Research Centre for the Giant Panda at Wolong for their assistance in sample collection. This work was supported by grants from the National Natural Science Foundation of China (Grant #30470233, #30230080, #30070107), the Research Fund for the Doctoral Program of Higher Education (Grant #98002717), and the grant from the China Wildlife Conservation Association (Grant #96035) and the International Cooperation Projects of Giant Pandas from State Forestry Administration, P. R. China (Grant #WH0309, #WH0306, #SD0630).


  1. Alberts AC (1992) Constraints on the design of chemical communication-systems in terrestrial vertebrates. Am Nat 139:S62–S89CrossRefGoogle Scholar
  2. Albone ES (1984) Mammalian semiochemistry: the investigation of chemical signals between mammals. Wiley-Interscience, Wiley & Sons, Chichester, UK, p 360Google Scholar
  3. Andersen KF, Vulpius T (1999) Urinary volatile constituents of the lion, Panthera leo. Chem Senses 24:179–189PubMedCrossRefGoogle Scholar
  4. Beynon RJ, Robertson DHL, Hubbard SJ, Gaskell SJ, Hurst JL (1999) The role of protein binding in chemical communication. In: Johnston RE, Müller-Schwarze D, Sorensen PW (eds) Advances in chemical signals in vertebrates. Kluwer Academic/Plenum Publishers, New York, pp 137–147CrossRefGoogle Scholar
  5. Brahmachary RL, Dutta J (1981) On the pheromones of tigers: experiments and theory. Am Nat 118:561–567CrossRefGoogle Scholar
  6. Brown RE (1979) Mammalian social odors: a critical review. Adv Stud Behav 10:103–162CrossRefGoogle Scholar
  7. Dehnhard M, Hildebrandt T, Knauf T, Ochs A, Ringleb J, Göritz F (2005) Chemical signals in giant panda urine (Ailuropoda melanoleuca). In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical signals in vertebrates 10. Springer US, New York, NY, pp 110–117CrossRefGoogle Scholar
  8. Hagey L, MacDonald E (2003) Chemical cues identify gender and individuality in giant pandas (Ailuropoda melanoleuca). J Chem Ecol 29:1479–1488PubMedCrossRefGoogle Scholar
  9. Halpin ZT (1986) Individual odors among mammals: origins and functions. In: Rosenblatt JS, Beer C, Busnel M, Slater PJB (eds) Advances in the study of behavior, vol 16. Academic, New York, pp 39–70Google Scholar
  10. Johnston RE (1983) Chemical signals and reproductive behavior. In: Vandenbergh JG (ed) Pheromones and reproduction in mammals. Academic, New York, pp 3–37CrossRefGoogle Scholar
  11. Kleiman DG (1983) Ethology and reproduction of captive giant pandas (Ailuropoda melanoleuca). Z Tierpsychol 62:1–46CrossRefGoogle Scholar
  12. Liu D (1996) Studies on the behavioral ecology of captive giant pandas (Ailuropoda melanoleuca). PhD Dissertation (in Chinese), Beijing Normal University, BeijingGoogle Scholar
  13. Liu D, Fang J, Sun R, Zhang G, Wei R, Zhang H (1998) Behavioral comparison in individuals of different sexual ability in giant panda (Ailuropoda melanoleuca). Acta Zool Sinica (in Chinese) 44:27–34Google Scholar
  14. Liu D, Wang LW, Zhang XT, Wei RP, Zhang GQ, Yun ZH, Sun RY (2003) Urinary volatile profiles of the giant pandas pertaining to gender, season and sexual ability. J Beijing Normal University (Natural Science) (in Chinese) 39:123–130Google Scholar
  15. Liu D, Zhang G, Wei R, Zhang H, Fang J, Sun R (2005) Behavioral responsiveness of captive giant pandas (Ailuropoda melanoleuca) to substrate odors from conspecifcs of the opposite sex. In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical signals in vertebrates 10. Springer, New York, pp 101–109CrossRefGoogle Scholar
  16. Ma W, Klemm WR (1997) Variations of equine urinary volatile compounds during the oestrous cycle. Vet Res Commun 21:437–446PubMedCrossRefGoogle Scholar
  17. Ma W, Wiesler D, Novotny MV (1999) Urinary volatile profiles of the deermouse (Peromyscus maniculatus) pertaining to gender and age. J Chem Ecol 25:417–431CrossRefGoogle Scholar
  18. Miller KV, Jemiolo B, Gassett JW, Jelinek I, Wiesler D, Novotny M (1998) Putative chemical signals from white-tailed deer (Odocoileus virginianus): social and seasonal effects on urinary volatile excretion in males. J Chem Ecol 24:673–683CrossRefGoogle Scholar
  19. Novotny M, Harvey S, Jemiolo B, Alberts J (1985) Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci USA 82:2059–2061PubMedCrossRefGoogle Scholar
  20. Novotny MV, Ma W, Zidek L, Daev E (1999) Recent biochemical insights into puberty acceleration, estrus induction, and puberty delay in the house mouse. In: Johnston RE, Müller-Schwarze D, Sorensen PW (eds) Advances in chemical signals in vertebrates. Kluwer Academic/Plenum Publishers, New York, pp 99–116CrossRefGoogle Scholar
  21. Poddar-Sarkar M, Brahmachary RL (1999) Can free fatty acids in the tiger pheromone act as an individual fingerprint? Curr Sci 76:141–142Google Scholar
  22. Rasmussen LEL, George W (2002) Chemosignalling of musth by individual wild African elephants (Loxodonta africana): implications for conservation and management. Proc R Soc B Biol Sci 269:853–860CrossRefGoogle Scholar
  23. Rasmussen LEL, Anthony J, Martin H, Hess DL (1996a) Chemical profiles of male African elephants, Loxodonta africana: physiological and ecological implications. J Mammal 77:422–439CrossRefGoogle Scholar
  24. Rasmussen LEL, Lee TD, Roelofs WL, Zhang AJ, Daves GD (1996b) Insect pheromone in elephants. Nature 379:684PubMedCrossRefGoogle Scholar
  25. Rasmussen LEL, Lee TD, Zhang A, Roelofs WL, Daves GD Jr (1997) Purification, identification, concentration and bioactivity of (Z)-7-dodecen-1-yl acetate: sex pheromone of the female Asian elephant, Elephas maximus. Chem Senses 22:417–437PubMedCrossRefGoogle Scholar
  26. Raymer J, Wieler D, Novotny M, Asa C, Seal US, Mech LD (1984) Volatile constituents of wolf (Canis lupus) urine as related to gender and season. Experientia 40:707–709PubMedCrossRefGoogle Scholar
  27. Schaller GB, Hu J, Pan W, Zhu J (1985) The giant pandas of Wolong. University of Chicago Press, Chicago, p 298Google Scholar
  28. Sun L, Müller-Schwarze D (1998a) Anal gland secretion codes for family membership in the beaver. Behav Ecol Sociobiol 44:199–208CrossRefGoogle Scholar
  29. Sun L, Müller-Schwarze D (1998b) Anal gland secretion codes for relatedness in the beaver, Castor canadensis. Ethology 104:917–927CrossRefGoogle Scholar
  30. Swaisgood RR, Lindburg DG, Zhou X (1999) Giant pandas discriminate individual differences in conspecific scent. Anim Behav 57:1045–1053PubMedCrossRefGoogle Scholar
  31. Swaisgood RR, Lindburg DG, Owen MA (2000) The effects of sex, reproductive condition and context on discrimination of conspecific odours by giant pandas. Anim Behav 60:227–237PubMedCrossRefGoogle Scholar
  32. Swaisgood RR, Lindburg DG, Zhang H (2002) Discrimination of oestrous status in giant pandas (Ailuropoda melanoleuca) via chemical cues in urine. J Zool 257:381–386CrossRefGoogle Scholar
  33. Todrank J, Heth G (2003) Odor-genes covariance and genetic relatedness assessments: rethinking odor-based “recognition” mechanisms in rodents. Adv Stud Behav 32:77–130CrossRefGoogle Scholar
  34. White AM, Swaisgood RR, 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 51:519–529CrossRefGoogle Scholar
  35. White AM, Swaisgood RR, Zhang H (2003) Chemical communication in the giant panda (Ailuropoda melanoleuca): the role of age in the signaller and assessor. J Zool 259:171–178CrossRefGoogle Scholar
  36. White AM, Swaisgood RR, Zhang H (2004) Urinary chemosignals in giant pandas (Ailuropoda melanoleuca): seasonal and developmental effects on signal discrimination. J Zool 264:231–238CrossRefGoogle Scholar
  37. Wyatt TD (2003) Pheromones and animal behaviour—communication by smell and taste. Cambridge University Press, London, p 391CrossRefGoogle Scholar
  38. Xu M, Wang Z, Liu D, Wei R, Zhang G, Zhang H, Zhou X, Li D (2012) Cross-modal signaling in giant pandas. Chin Sci Bull 57:344–348CrossRefGoogle Scholar
  39. Yamazaki K, Yamaguchi M, Baranoski L, Bard J, Boyse EA, Thomas L (1979) Recognition among mice. Evidence from the use of a Y-maze differentially scented by congenic mice of different major histocompatibility types. J Exp Med 150:755–760PubMedCrossRefGoogle Scholar
  40. Yuan H, Liu D, Sun L, Wei RP, Zhang GQ, Sun RY (2004) Anogenital gland secretions code for sex and age in the giant panda, Ailuropoda melanoleuca. Can J Zool 82:1596–1604CrossRefGoogle Scholar
  41. Zhang GQ, Swaisgood RR, Zhang HM (2004) Evaluation of behavioral factors influencing reproductive success and failure in captive giant pandas. Zoo Biol 23:15–31CrossRefGoogle Scholar
  42. Zhang JX, Soini HA, Bruce KE, Wiesler D, Woodley SK, Baum MJ, Novotny MV (2005) Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem Senses 30:1–11CrossRefGoogle Scholar
  43. Zhang JX, Rao XP, Sun L, Zhao C, Qin X (2007) Putative chemical signals about sex, individuality and genetic background in the preputial gland and urine of the house mouse (Mus musculus). Chem Senses 32:293–303PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Dingzhen Liu
    • 1
  • Hong Yuan
    • 1
  • Zhipeng Wang
    • 1
  • Rongping Wei
    • 2
  • Guiquan Zhang
    • 2
  • Lixing Sun
    • 3
  1. 1.Ministry of Education, Key Laboratory of Biodiversity Science and Ecological Engineering & Institute of EcologyBeijing Normal UniversityBeijingChina
  2. 2.China Research and Conservation Center for the Giant PandaSichuanChina
  3. 3.Department of Biological SciencesCentral Washington UniversityEllensburgUSA

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