The Science of Nature

, 103:37 | Cite as

Reproductive endocrine patterns and volatile urinary compounds of Arctictis binturong: discovering why bearcats smell like popcorn

  • Lydia K. Greene
  • Timothy W. Wallen
  • Anneke Moresco
  • Thomas E. Goodwin
  • Christine M. Drea
Original Paper

Abstract

Members of the order Carnivora rely on urinary scent signaling, particularly for communicating about reproductive parameters. Here, we describe reproductive endocrine patterns in relation to urinary olfactory cues in a vulnerable and relatively unknown viverrid—the binturong (Arctictis binturong). Female binturongs are larger than and dominate males, and both sexes engage in glandular and urinary scent marking. Using a large (n = 33), captive population, we collected serum samples to measure circulating sex steroids via enzyme immunoassay and urine samples to assay volatile chemicals via gas chromatography–mass spectrometry. Male binturongs had expectedly greater androgen concentrations than did females but, more unusually, had equal estrogen concentrations, which may be linked to male deference. Males also expressed a significantly richer array of volatile chemical compounds than did females. A subset of these volatile chemicals resisted decay at ambient temperatures, potentially indicating their importance as long-lasting semiochemicals. Among these compounds was 2-acetyl-1-pyrroline (2-AP), which is typically produced at high temperatures by the Maillard reaction and is likely to be responsible for the binturong’s characteristic popcorn aroma. 2-AP, the only compound expressed by all of the subjects, was found in greater abundance in males than females and was significantly and positively related to circulating androstenedione concentrations in both sexes. This unusual compound may have a more significant role in mammalian semiochemistry than previously appreciated. Based on these novel data, we suggest that hormonal action and potentially complex chemical reactions mediate communication of the binturong’s signature scent and convey information about sex and reproductive state.

Keywords

Female dominance Olfactory communication Urinary signals Reproductive endocrinology 2-Acetyl-1-pyrroline Viverrid 

References

  1. Abra L (2010) Notes on the development and behaviour of two binturong Arctictus binturong litters born at Taronga Zoo, Sydney. Int Zool Yearb 44:238–245. doi:10.1111/j.1748-1090.2009.00102.x CrossRefGoogle Scholar
  2. Adams A, De Kimpe N (2006) Chemistry of 2-acetyl-1-pyrroline, 6-acetyl-1, 2, 3, 4-tetrahydropyridine, 2-acetyl-2-thiazoline, and 5-acetyl-2,3-dihydro-4 H-thiazine: extraordinary Maillard flavor compounds. Chem Rev 106:2299–2319. doi:10.1021/cr040097y CrossRefPubMedGoogle Scholar
  3. Adams A, De Kimpe N (2007) Formation of pyrazines and 2-acetyl-1-pyrroline by Bacillus cereus. Food Chem 101:1230–1238. doi:10.1016/j.foodchem.2006.03.027 CrossRefGoogle Scholar
  4. Alberts AC (1992) Constraints on the design of chemical communication systems in terrestrial vertebrates. Am Nat: S62-S89Google Scholar
  5. Albone ES (1984) Mammalian semiochemistry: the investigation of chemical signals between mammals. Wiley, New YorkGoogle Scholar
  6. Andersen K, Vulpius T (1999) Urinary volatile constituents of the lion, Panthera leo. Chem Senses 24:179–189. doi:10.1093/chemse/24.2.179 CrossRefPubMedGoogle Scholar
  7. Anisko JJ (1976) Communication by chemical signals in Canidae. In: Doty R (ed) Mammalian olfaction, reproductive processes, and behavior. Academic, New York, pp 283–293Google Scholar
  8. Apps P, Mmualefe L, McNutt JW (2012) Identification of volatiles from the secretions and excretions of African wild dogs (Lycaon pictus). J Chem Ecol 38:1450–1461. doi:10.1007/s10886-012-0206-7 CrossRefPubMedGoogle Scholar
  9. Archie EA, Theis KR (2011) Animal behaviour meets microbial ecology. Anim Behav 82:425–436. doi:10.1016/j.anbehav.2011.05.029 CrossRefGoogle Scholar
  10. Asa CS, Mech LD, Seal US, Plotka ED (1990) The influence of social and endocrine factors on urine-marking by captive wolves (Canis lupus). Horm Behav 24:497–509. doi:10.1016/0018-506X(90)90038-Y CrossRefPubMedGoogle Scholar
  11. Beach FA (1974) Effects of gonadal hormones on urinary behavior in dogs. Physiol Behav 12:1005–1013. doi:10.1016/0031-9384(74)90148-6 CrossRefPubMedGoogle Scholar
  12. Berg IA (1944) Development of behavior: the micturition pattern in the dog. J Exp Psychol 34:343–368. doi:10.1037/h0055459 CrossRefGoogle Scholar
  13. Bjerselius R, Lundstedt-Enkel K, Olsén H, Mayer I, Dimberg K (2001) Male goldfish reproductive behaviour and physiology are severely affected by exogenous exposure to 17β-estradiol. Aquat Toxicol 53:139–152. doi:10.1016/S0166-445X(00)00160-0 CrossRefPubMedGoogle Scholar
  14. Bono G, Minori D, Gaiani R, Mattioli M (1982) Concentrations of oestrone sulphate, androgens and LH in the peripheral plasma of mating stallions. J Reprod Fertil 66:17–22. doi:10.1530/jrf.0.0660017 CrossRefPubMedGoogle Scholar
  15. Boulet M, Charpentier MJE, Drea CM (2009) Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate. BMC Evol Biol 9:281. doi:10.1186/1471-2148-9-281 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bradbury LM, Gillies SA, Brushett DJ, Waters DL, Henry RJ (2008) Inactivation of an aminoaldehyde dehydrogenase is responsible for fragrance in rice. Plant Mol Biol 68:439–449. doi:10.1007/s11103-008-9381-x CrossRefPubMedGoogle Scholar
  17. Brahmachary R (1996) The expanding world of 2-acetyl-1-pyrroline. Curr Sci 71:257–258Google Scholar
  18. Brahmachary RL, Sarkar MP, Dutta J (1990) The aroma of rice … and tiger. Nature 344:26. doi:10.1038/344026b0 CrossRefPubMedGoogle Scholar
  19. Brahmachary RL, Sarkar MP, Dutta J (1992) Chemical signals in the tiger. Chem Signals in Vertebrates 6, Springer: 471–475. doi: 10.1007/978-1-4757-9655-1_72
  20. Bubenik GA, Schams D, White RJ, Rowell J, Blake J, Bartos L (1997) Seasonal levels of reproductive hormones and their relationship to the antler cycle of male and female reindeer (Rangifer tarandus). Comp Biochem Physiol Part B: Biochem Mol Biol 116:269–277. doi:10.1016/S0305-0491(97)00183-1 CrossRefGoogle Scholar
  21. Burger BV, Visser R, Moses A, Le Roux M (2006) Elemental sulfur identified in urine of cheetah, Acinonyx jubatus. J Chem Ecol 32:1347–1352. doi:10.1007/s10886-006-9056-5 CrossRefPubMedGoogle Scholar
  22. Buttery RG, Ling LC, Juliano BO (1982) 2-Acetyl-1-pyrroline: an important aroma component of cooked rice. Chem Indust: 958–959Google Scholar
  23. Buttery RG, Ling LC, Juliano BO, Turnbaugh JG (1983) Cooked rice aroma and 2-acetyl-1-pyrroline. J Agric Food Chem 31:823–826CrossRefGoogle Scholar
  24. delBarco-Trilllo J, Sacha CR, Dubay GR, Drea CM (2012) Eulemur, me lemur: the evolution of scent-signal complexity in a primate clade. Phil Trans R Soc B: Biol Sci 367:1909–1922. doi:10.1098/rstb.2011.0225 CrossRefGoogle Scholar
  25. delBarco-Trillo J, Harelimana IH, Goodwin TE, Drea CM (2013) Chemical differences between voided and bladder urine in the aye‐aye (Daubentonia madagascariensis): implications for olfactory communication studies. Am J Primatol 75:695–702. doi:10.1002/ajp.22083 CrossRefPubMedGoogle Scholar
  26. delBarco‐Trillo J, Burkert BA, Goodwin TE, Drea CM (2011) Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals. J Evol Biol 24:82–98. doi:10.1111/j.1420-9101.2010.02145.x CrossRefPubMedGoogle Scholar
  27. Drea CM (2007) Sex and seasonal differences in aggression and steroid secretion in Lemur catta: are socially dominant females hormonally ‘masculinized’? Horm Behav 51:555–567. doi:10.1016/j.yhbeh.2007.02.006 CrossRefPubMedGoogle Scholar
  28. Drea CM (2009) Endocrine mediators of masculinization in female mammals. Curr Dir Psychol Sci 18:221–226. doi:10.1111/j.1467-8721.2009.01640.x CrossRefGoogle Scholar
  29. Drea CM (2015) D’scent of man: a comparative survey of primate chemosignaling in relation to sex. Horm Behav 68:117–133. doi:10.1016/j.yhbeh.2014.08.001 CrossRefPubMedGoogle Scholar
  30. Drea CM, Vignieri SN, Cunningham SB, Glickman SE (2002) Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): I. Investigation of environmental odors and the function of rolling. J Comp Psychol 116:331–341. doi:10.1037//0735-7036.116.4.331 CrossRefPubMedGoogle Scholar
  31. Drea CM, Boulet M, delBarco-Trillo J, Greene LK, Sacha CR, Goodwin TE, Dubay GR (2013) The “secret” in secretions: methodological considerations in deciphering primate olfactory communication. Am J Primatol 75:621–642. doi:10.1002/ajp.22143 CrossRefPubMedGoogle Scholar
  32. Eisenberg JF, Kleiman DG (1972) Olfactory communication in mammals. Ann Rev Ecol Syst 3:1–32. doi:10.1146/annurev.es.03.110172.000245 CrossRefGoogle Scholar
  33. Ewer RF (1973) The carnivores. Cornell University Press, IthacaGoogle Scholar
  34. Ezenwa VO, Williams AE (2014) Microbes and animal olfactory communication: where do we go from here? BioEssays 36:847–854. doi:10.1002/bies.201400016 CrossRefPubMedGoogle Scholar
  35. Feldman HN (1994) Methods of scent marking in the domestic cat. Can J Zool 72:1093–1099. doi:10.1139/z94-147 CrossRefGoogle Scholar
  36. Glickman S, Frank L, Pavgi S, Licht P (1992) Hormonal correlates of ‘masculinization’ in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity. J Reprod Fertil 95:451–462. doi:10.1530/jrf.0.0950451 CrossRefPubMedGoogle Scholar
  37. Goodwin TE, Broederdorf LJ, Burkert BA, Hirwa IH, Mark DB, Waldrip ZJ, Kopper RA, Sutherland MV, Freeman EW, Hollister-Smith JA (2012) Chemical signals of elephant musth: temporal aspects of microbially-mediated modifications. J Chem Ecol 38:81–87. doi:10.1007/s10886-011-0056-8 CrossRefPubMedGoogle Scholar
  38. Goodwin TE, Songsasen N, Broederdorf LJ, Burkert BA, Chen CJ, Jackson SR, Keplinger KB, Rountree ME, Waldrip ZJ, Weddell ME (2013) Hemiterpenoids and pyrazines in the odoriferous urine of the maned wolf (Chrysocyon brachyurus). In East ML & Dehnhard D (eds) Chemical Signals in Vertebrates 12, Springer, New York, pp 171–184. doi: 10.1007/978-1-4614-5927-9_13
  39. Gorman ML, Trowbridge BJ (1989) The role of odor in the social lives of carnivores. In: Gittleman JL (ed) Carnivore Behavior, Ecology, and Evolution, Springer: 57–88. doi: 10.1007/978-1-4757-4716-4_3
  40. Grassman LI, Tewes ME, Silvy NJ (2005) Ranging, habitat use and activity patterns of binturong Arctictis binturong and yellow-throated marten Martes flavigula in north-central Thailand. Wildl Biol 11:49–57. doi:10.2981/0909-6396(2005)11[49:RHUAAP]2.0.CO;2 CrossRefGoogle Scholar
  41. Greene LK, Grogan KE, Smyth KN, Adams CA, Klager SA, Drea CM (2016) Mix it and fix it: functions of composite olfactory signals in ring-tailed lemurs. R Soc Open Sci 3:160076. doi:10.1098/rsos.160076
  42. Hart BL (1974) Gonadal androgen and sociosexual behavior of male mammals: a comparative analysis. Psychol Bull 81:383. doi:10.1037/h0036568 CrossRefPubMedGoogle Scholar
  43. Hayata Y, Sakamoto T, Maneerat C, Li X, Kozuka H, Sakamoto K (2003) Evaluation of aroma compounds contributing to muskmelon flavor in porapak Q extracts by armona extract dilution analysis. J Agric Food Chem 51:3415–3418. doi:10.1021/jf0209950 CrossRefPubMedGoogle Scholar
  44. Hoffmann F, Musolf K, Penn DJ (2009) Freezing urine reduces its efficacy for eliciting ultrasonic vocalizations from male mice. Physiol Behav 96:602–605. doi:10.1016/j.physbeh.2008.12.014 CrossRefPubMedGoogle Scholar
  45. Hurst JL, Robertson DHL, Tolladay U, Beynon RJ (1998) Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim Behav 55:1289–1297. doi:10.1006/anbe.1997.0650 CrossRefPubMedGoogle Scholar
  46. Jorgenson J, Novotny M, Carmack M, Copland G, Wilson S, Katona S, Whitten W (1978) Chemical scent constituents in the urine of the red fox (Vulpes vulpes L.) during the winter season. Science 199:796–798. doi:10.1126/science.199.4330.796 CrossRefPubMedGoogle Scholar
  47. Kleiman DG (1966) Scent marking in the Canidae. Symp Zool Soc Lond 18:167–177Google Scholar
  48. Kleiman DG (1974) Scent marking in the binturong, Arctictis binturong. J Mammal 55:224–227. doi:10.2307/1379278 CrossRefGoogle Scholar
  49. Koren L, Mokady O, Geffen E (2006) Elevated testosterone levels and social ranks in female rock hyrax. Horm Behav 49:470–477. doi:10.1016/j.yhbeh.2005.10.004 CrossRefPubMedGoogle Scholar
  50. Kwak J, Willse A, Matsumura K, Opiekun MC, Weiguang Y, Preti G, Yamazaki K, Beaucahmp GK (2008) Genetically-based olfactory signatures persist despite dietary variation. PLoS ONE 3, e3591. doi:10.1371/journal.pone.0003591 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kwak J, Grigsby CC, Preti G, Rizki MM, Yamazaki K, Beauchamp GK (2013) Changes in volatile compounds of mouse urine as it ages: their interactions with water and urinary proteins. Physiol Behav 120:211–219. doi:10.1016/j.physbeh.2013.08.011 CrossRefPubMedGoogle Scholar
  52. Liu D, Yuan H, Wang Z, Wei R, Zhang G, Sun L (2013) Do urinary chemosignals code for sex, age, and season in the giant panda, Ailuropoda melanoleuca? Chem Signals in Vertebrates 12, Springer: 207–222. doi: 10.1007/978-1-4614-5927-9_16
  53. Macdonald D (1979) Some observations and field experiments on the urine marking behaviour of the red fox, Vulpes vulpes L. Z Tierpsychol 51:1–22. doi:10.1111/j.1439-0310.1979.tb00667.x CrossRefGoogle Scholar
  54. MacDonald DW (1980) Patterns of scent marking with urine and faeces amongst carnivore communities. Symp Zool Soc Lond 45:107–139Google Scholar
  55. McCune B, Grace JB, Urban DL (2002) Analysis of Ecological Communities, MjM software design Gleneden Beach, ORGoogle Scholar
  56. Mertl‐Millhollen AS, Goodmann PA, Klinghammer E (1986) Wolf scent marking with raised‐leg urination. Zool Biol 5:7–20. doi:10.1002/zoo.1430050103 CrossRefGoogle Scholar
  57. Moresco A, Larsen RS (2003) Medetomidine-ketamine-butorphanol anesthetic combinations in binturongs (Arctictis binturong). J Zool Wildl Med 34:346–351. doi:10.1638/03-016 CrossRefGoogle Scholar
  58. Müller-Schwarze D (2006) Chemical ecology of vertebrates. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  59. Peters RP, Mech LD (1975) Scent-marking in wolves: Radio-tracking of wolf packs has provided definite evidence that olfactory sign is used for territory maintenance and may serve for other forms of communication within the pack as well. Am Sci: 628–637Google Scholar
  60. Petty, JMA (2015) Understanding female social dominance: comparative behavioral endocrinology in the genus Eulemur. Doctoral dissertation, Duke UniversityGoogle Scholar
  61. Petty JMA, Drea CM (2015) Female rule in lemurs is ancestral and hormonally mediated. Sci Rep 5:9631. doi:10.1038/srep09631 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Pocock RI (1915) On the feet and glands and other external characters of the viverrinae, with the description of a new genius. Proc Zool Soc Lond 85:131–149. doi:10.1111/j.1469-7998.1915.00131.x CrossRefGoogle Scholar
  63. Pocock RI (1939) The Fauna of British India, including Ceylon and Burma. Mammalia, 2nd edn, I. Taylor & Francis, London, U.KGoogle Scholar
  64. Porton I (1983) Bush dog urine-marking: its role in pair formation and maintenance. Anim Behav 31:1061–1069. doi:10.1016/S0003-3472(83)80013-X CrossRefGoogle Scholar
  65. Raeside J (1979) Seasonal changes in the concentration of estrogens and testosterone in the plasma of the stallion. Anim Reprod Sci 1:205–212. doi:10.1016/0378-4320(79)90002-2 CrossRefGoogle Scholar
  66. Ralls K (1971) Mammalian scent marking. Science 171:443–449. doi:10.1126/science.171.3970.443 CrossRefPubMedGoogle Scholar
  67. Raymer J, Wiesler D, Novotny M, Asa C, Seal US, Mech LD (1984) Volatile constituents of wolf (Canis lupus) urine as related to gender and season. Experientia 40:707–709. doi:10.1007/BF01949734 CrossRefPubMedGoogle Scholar
  68. Romanczyk LJ, McClelland CA, Post LA, Aitken WM (1995) Formation of 2-acetyl-1-pyrroline by several Bacillus cereus strains isolated from cocoa fermentation boxes. J Agric Food Chem 43:469–475. doi:10.1021/jf00050a040 CrossRefGoogle Scholar
  69. Rothman RJ, Mech LD (1979) Scent-marking in lone wolves and newly formed pairs. Anim Behav 27:750–760. doi:10.1016/0003-3472(79)90010-1 CrossRefGoogle Scholar
  70. Schieberle P (1991) Primary odorants in popcorn. J Agric Food Chem 39:1141–1144. doi:10.1021/jf00006a030 CrossRefGoogle Scholar
  71. Scordato ES, Dubay GR, Drea CM (2007) Chemical composition of scent marks in the ringtailed lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures. Chem Senses 32:493–504. doi:10.1093/chemse/bjm018 CrossRefPubMedGoogle Scholar
  72. Sillero‐Zubiri C, Macdonald DW (1998) Scent‐marking and territorial behaviour of Ethiopian wolves Canis simensis. J Zool 245:351–361. doi:10.1111/j.1469-7998.1998.tb00110.x CrossRefGoogle Scholar
  73. Staples EJ, Viswanathan S (2005) Odor detection and analysis using GC/SAW zNose®. Electronic Sensor Technology, School of Engineering and Technology, National UniversityGoogle Scholar
  74. Story HE (1945) The external genitalia and perfume gland in Arctictis binturong. J Mammal 26:64–66CrossRefGoogle Scholar
  75. Swiecicka I (2008) Natural occurrence of Bacillus thuringiensis and Bacillus cereus in eukaryotic organisms: a case for symbiosis. Biocontrol Sci Technol 18:221–239. doi:10.1080/09583150801942334 CrossRefGoogle Scholar
  76. Toppari J, Larsen JC, Christiansen P, Giwercman A, Grandjean P, Guillette LJ, Jégou B, Jensen TK, Jouannet P, Keiding N (1996) Male reproductive health and environmental xenoestrogens. Environ Health Perspect 104(Suppl 4):741CrossRefPubMedPubMedCentralGoogle Scholar
  77. Weldon PJ, Gorra MF, Wood WF (2000) Short-chain carboxylic acids from the anal glands of the binturong, Arctictis binturong (Viverridae, Mammalia). Biochem Syst Ecol 28:903–904. doi:10.1016/S0305-1978(99)00128-3 CrossRefPubMedGoogle Scholar
  78. Wemmer C, Murtaugh J (1981) Copulatory behavior and reproduction in the binturong, Arctictis binturong. J Mammal: 342–352. doi: 10.2307/1380710
  79. Wong KC, Lim CL, Wong LL (1992) Volatile flavour constitudents of Chempadek (Artocarpus polyphema Pers.) fruit and jackfruit (Artocarpus heterphyllus Lam.) from Malaysia. Flavour Fragr J 7:307–311. doi:10.1002/ffj.2730070604 CrossRefGoogle Scholar
  80. Wood WF, Copeland JP, Yates RE, Horsey IK, McGreevy LR (2009) Potential semiochemicals in urine from free ranging wolverines (Gulo gulo Pallas, 1780). Biochem Syst Ecol 37:574–578. doi:10.1016/j.bse.2009.09.007 CrossRefGoogle Scholar
  81. Wynne-Edwards KE (2001) Hormonal changes in mammalian fathers. Horm Behav 40:139–145. doi:10.1006/hbeh.2001.1699 CrossRefPubMedGoogle Scholar
  82. Yoshihashi T (2002) Quantitative analysis on 2‐acetyl‐1‐pyrroline of an aromatic rice by stable isotope dilution method and model studies on its formation during cooking. J Food Sci 67:619–622. doi:10.1111/j.1365-2621.2002.tb10648.x CrossRefGoogle Scholar
  83. Zhang J, Soini H, Bruce K, Wiesler D, Woodley S, Baum M, Novotny M (2005) Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem Senses 30:727–737. doi:10.1093/chemse/bji065 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Lydia K. Greene
    • 1
    • 2
  • Timothy W. Wallen
    • 3
    • 6
  • Anneke Moresco
    • 4
    • 7
  • Thomas E. Goodwin
    • 3
  • Christine M. Drea
    • 1
    • 2
    • 5
  1. 1.University Program in EcologyDuke UniversityDurhamUSA
  2. 2.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA
  3. 3.Department of ChemistryHendrix CollegeConwayUSA
  4. 4.Carnivore Preservation Trust (now Carolina Tiger Rescue)PittsboroUSA
  5. 5.Department of BiologyDuke UniversityDurhamUSA
  6. 6.National Center for Environmental Health, Division of Laboratory Sciences, Clinical Chemistry BranchCenters for Disease Control and PreventionAtlantaUSA
  7. 7.Denver ZooDenverUSA

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