Naturwissenschaften

, Volume 98, Issue 7, pp 615–624 | Cite as

An individual and a sex odor signature in kittiwakes? Study of the semiochemical composition of preen secretion and preen down feathers

  • Sarah Leclaire
  • Thomas Merkling
  • Christine Raynaud
  • Géraldine Giacinti
  • Jean-Marie Bessière
  • Scott A. Hatch
  • Étienne Danchin
Original Paper

Abstract

The importance of olfaction in birds’ social behavior has long been denied. Avian chemical signaling has thus been relatively unexplored. The black-legged kittiwake provides a particularly appropriate model for investigating this topic. Kittiwakes preferentially mate with genetically dissimilar individuals, but the cues used to assess genetic characteristics remain unknown. As in other vertebrates, their body odors may carry individual and sexual signatures thus potentially reliably signaling individual genetic makeup. Here, we test whether body odors in preen gland secretion and preen down feathers in kittiwakes may provide a sex and an individual signature. Using gas chromatography and mass spectrometry, we found that male and female odors differ quantitatively, suggesting that scent may be one of the multiple cues used by birds to discriminate between sexes. We further detected an individual signature in the volatile and nonvolatile fractions of preen secretion and preen down feathers. These results suggest that kittiwake body odor may function as a signal associated with mate recognition. It further suggests that preen odor might broadcast the genetic makeup of individuals, and could be used in mate choice to assess the genetic compatibility of potential mates.

Keywords

Kittiwake Odor Preen gland Uropygial secretion Individual signature 

References

  1. Balthazart J, Schoffeniels E (1979) Pheromones are involved in the control of sexual-behavior in birds. Naturwissenschaften 66:55–56PubMedCrossRefGoogle Scholar
  2. Balthazart J, Taziaux M (2009) The underestimated role of olfaction in avian reproduction? Behav Brain Res 200:248–259PubMedCrossRefGoogle Scholar
  3. Bang BG, Wenzel BM (1985) Nasal cavity and olfactory system. In: King AS, McClelland J (eds) Form and function in birds. Academic Press, London, pp 195–225Google Scholar
  4. Bohnet S, Rogers L, Sasaki G, Kolattukudy PE (1991) Estradiol induces proliferation of peroxisome-like microbodies and the production of 3-hydroxy fatty-acid diesters, the female pheromones, in the uropygial glands of male and female mallards. J Biol Chem 266:9795–9804PubMedGoogle Scholar
  5. Bonadonna F (2009) Olfactory sex recognition investigated in Antarctic prions. PLoS One 4:e4148, 4141–4143PubMedCrossRefGoogle Scholar
  6. Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science 306:835PubMedCrossRefGoogle Scholar
  7. Bonadonna F, Miguel E, Grosbois V, Jouventin P, Bessiere JM (2007) Individual odor recognition in birds: an endogenous olfactory signature on petrels’ feathers? J Chem Ecol 33:1819–1829PubMedCrossRefGoogle Scholar
  8. Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444:308–315PubMedCrossRefGoogle Scholar
  9. Burger BV, Reiter B, Borzyk O, Du Plessis MA (2004) Avian exocrine secretions. I. Chemical characterization of the volatile fraction of the uropygial secretion of the green woodhoopoe, Phoeniculus purpureus. J Chem Ecol 30:1603–1611PubMedCrossRefGoogle Scholar
  10. Caro SP, Balthazart J (2010) Pheromones in birds: myth or reality ? J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:751–766PubMedCrossRefGoogle Scholar
  11. Charpentier MJE, Boulet M, Drea CM (2008) Smelling right: the scent of male lemurs advertises genetic quality and relatedness. Mol Ecol 17:3225–3233PubMedCrossRefGoogle Scholar
  12. Cloe AL, Woodley SK, Waters P, Zhou H, Baum MJ (2004) Contribution of anal scent gland and urinary odorants to mate recognition in the ferret. Physiol Behav 82:871–875PubMedGoogle Scholar
  13. Coulson JC (1966) The influence of the pair-bond and age on the breeding biology of the kittiwake gull Rissa tridactyla. J Anim Ecol 35:269–279CrossRefGoogle Scholar
  14. Dekker MHA, Piersma T, Damste JSS (2000) Molecular analysis of intact preen waxes of Calidri canutus (Aves: Scolopacidae) by gas chromatography/mass spectrometry. Lipids 35:533–541PubMedCrossRefGoogle Scholar
  15. Douglas HD (2006) Measurement of chemical emissions in crested auklets (Aethia cristatella). J Chem Ecol 32:2559–2567PubMedCrossRefGoogle Scholar
  16. Douglas HD (2008) In defense of chemical defense: quantification of volatile chemicals in feathers is challenging. Auk 125:496–497CrossRefGoogle Scholar
  17. Douglas HD, Kitaysky AS, Kitaiskaia EV (2008) Seasonal covariation in progesterone and odorant emissions among breeding crested auklets (Aethia cristatella). Horm Behav 54:325–329PubMedCrossRefGoogle Scholar
  18. Drea CM, Vignieri SN, Kim HS, Weldele ML, Glickman SE (2002) Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): II. Discrimination of conspecific scent. J Comp Psychol 116:342–349PubMedCrossRefGoogle Scholar
  19. Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Sollecito SV (2003) Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 12:3077–3083PubMedCrossRefGoogle Scholar
  20. Gill VA, Hatch SA (2002) Components of productivity in black-legged kittiwakes Rissa tridactyla: response to supplemental feeding. J Avian Biol 33:113–126CrossRefGoogle Scholar
  21. Giraudeau M, Duval C, Guillon N, Bretagnolle V, Gutierrez C, Heeb P (2010) Effects of access to preen gland secretions on mallard plumage. Naturwissenschaften 97:577–581PubMedCrossRefGoogle Scholar
  22. Hagelin JC, Jones IL (2007) Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 124:741–761CrossRefGoogle Scholar
  23. Halpern CT, Udry RJ, Suchindran C (1998) Monthly measures of salivary testosterone predict sexual activity in adolescent males. Arch Sex Behav 27:445–465PubMedCrossRefGoogle Scholar
  24. Haribal M, Dhondt AA, Rosane D, Rodriguez E (2005) Chemistry of preen gland secretions of passerines: different pathways to same goal? why? Chemoecology 15:251–260CrossRefGoogle Scholar
  25. Havlicek J, Lenochova P (2008) Environmental effects on human body odour. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates XI. Springer, New York, pp 199–212CrossRefGoogle Scholar
  26. Hirao A, Aoyama M, Sugita S (2009) The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus. Behav Processes 80:115–120PubMedCrossRefGoogle Scholar
  27. Jacob J, Zeman A (1972) The uropygial gland wax from the kittiwake (Rissa tridactyla). Z Naturforsch B 27:691–695PubMedGoogle Scholar
  28. Jacob J, Ziswiler V (1982) The uropygial gland. In: Farner DS, King JR, Parkes KC (eds) Avian biology. Academic Press, New York, pp 199–324Google Scholar
  29. Jacob J, Balthazart J, Schoffeniels E (1979) Sex-differences in the chemical composition of uropygial gland waxes in domestic ducks. Biochem Syst Ecol 7:149–153CrossRefGoogle Scholar
  30. Jacob J, Eigener U, Hoppe U (1997) The structure of preen gland waxes from pelecaniform birds containing 3,7-dimethyloctan-1-ol—an active ingredient against dermatophytes. Z Naturforsch C 52:114–123Google Scholar
  31. James AG, Casey J, Hyliands D, Mycock G (2004) Fatty acid metabolism by cutaneous bacteria and its role in axillary malodour. World J Microbiol Biotechnol 20:787–793CrossRefGoogle Scholar
  32. Jodice PGR, Lanctot RB, Gill VA, Roby DD, Hatch SA (2000) Sexing adult black-legged kittiwakes by DNA, behavior, and morphology. Waterbirds 23:405–415Google Scholar
  33. Johnston RE (1986) Effects of female odors on the sexual-behavior of male hamsters. Behav Neural Biol 46:168–188PubMedCrossRefGoogle Scholar
  34. Jordan NR, Mwanguhya F, Kyabulima S, Ruedi P, Cant MA (2010) Scent marking within and between groups of wild banded mongooses. J Zool 280:72–83CrossRefGoogle Scholar
  35. Kikuyama S, Nakada T, Toyoda F, Iwata T, Yamamoto K, Conlon JM (2005) Amphibian pheromones and endocrine control of their secretion. Trends Comp Endocr Neurobiol 1040:123–130Google Scholar
  36. Lawson RE, Putman RJ, Fielding AH (2000) Individual signatures in scent gland secretions of Eurasian deer. J Zool 251:399–410CrossRefGoogle Scholar
  37. Lawson RE, Putman RJ, Fielding AH (2001) Chemical communication in Eurasian deer (Cervidae): do individual odours also code for attributes? J Zool 253:91–99CrossRefGoogle Scholar
  38. Leclaire S, Mulard H, Wagner RH, Hatch SA, Danchin E (2009) Can Kittiwakes smell? Experimental evidence in a Larid species. Ibis 151:584–587CrossRefGoogle Scholar
  39. Macdonald EA, Fernandez-Duque E, Evans S, Hagey LR (2008) Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancvmaae) subcaudal scent secretions. Am J Primatol 70:12–18PubMedCrossRefGoogle Scholar
  40. Mardon J, Saunders SM, Anderson MJ, Couchoux C, Bonadonna F (2010) Species, gender, and identity: cracking petrels’ sociochemical code. Chem Senses 35:309–321PubMedCrossRefGoogle Scholar
  41. Mardon J, Saunders JR, Bonadonna F (2011a) From preen secretions to plumage: the chemical trajectory of blue petrels’ Halobaena caerulea social scent. J Avian Biol 42:29–38CrossRefGoogle Scholar
  42. Mardon J, Saunders SM, Bonadonna F (2011b) Comments on recent work by Zhang and colleagues: "Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars". Chem Senses 36:3–4PubMedCrossRefGoogle Scholar
  43. Martin-Platero AM, Valdivia E, Ruiz-Rodriguez M, Soler JJ, Martin-Vivaldi M, Maqueda M, Martinez-Bueno M (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10–3, isolated from the uropygial gland of the hoopoe (Upupa epops). Appl Environ Microbiol 72:4245–4249PubMedCrossRefGoogle Scholar
  44. Meredith M, O’Connell RJ (1988) HRP uptake by olfactory and vomeronasal receptor neurons: use as an indicator of incomplete lesions and relevance for non-volatile chemoreception. Chem Senses 13:487–515CrossRefGoogle Scholar
  45. Miller SL, Maner JK (2010) Scent of a woman: men’s testosterone responses to olfactory ovulation cues. Psychol Sci 21:276–283PubMedCrossRefGoogle Scholar
  46. Mulard H (2007) Behavioural implications of strict monogamy: individual recognition and genetic bases of mate choice in the black-legged kittiwake, Rissa tridactyla. Université Pierre et Marie Curie, ParisGoogle Scholar
  47. Mulard H, Danchin E, Talbot SL, Ramey AM, Hatch SA, White JF, Helfenstein F, Wagner RH (2009) Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird. BMC Evol Biol 9Google Scholar
  48. Naves LC, Monnat JY, Cam E (2006) Breeding performance, mate fidelity, and nest site fidelity in a long-lived seabird: behaving against the current? Oikos 115:263–276CrossRefGoogle Scholar
  49. Olsen KH, Grahn M, Lohm J, Langefors A (1998) MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim Behav 56:319–327PubMedCrossRefGoogle Scholar
  50. Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H (2003) Major histocompatibility complex and mate choice in sand lizards. Proc R Soc Lond B 270:S254–S256CrossRefGoogle Scholar
  51. Penn DJ, Oberzaucher E, Grammer K, Fischer G, Soini HA, Wiesler D, Novotny MV, Dixon SJ, Xu Y, Brereton RG (2007) Individual and gender fingerprints in human body odour. J R Soc Interface 4:331–340PubMedCrossRefGoogle Scholar
  52. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  53. Reneerkens J, Piersma T, Damste JSS (2002) Sandpipers (Scolopacidae) switch from monoester to diester preen waxes during courtship and incubation, but why? Proc R Soc Lond B 269:2135–2139CrossRefGoogle Scholar
  54. Reneerkens J, Almeida JB, Lank DB, Jukema J, Lanctot RB, Morrison RIG, Rijpstra WIC, Schamel D, Schekkerman H, Damste JSS, Tomkovich PS, Tracy DM, Tulp I, Piersma T (2007) Parental role division predicts avian preen wax cycles. Ibis 149:721–729CrossRefGoogle Scholar
  55. Rennie PJ, Gower DB, Holland KT, Mallet AI, Watkins WJ (1990) The skin microflora and the formation of human axillary odor. Int J Cosmet Sci 12:197–207PubMedCrossRefGoogle Scholar
  56. Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nat Genet 35:103–106PubMedCrossRefGoogle Scholar
  57. SAS Institute Inc. (1999) SAS User’s Guide, Version 8. SAS Institute Inc., CaryGoogle Scholar
  58. Scordato ES, Dubay G, Drea CM (2007) Chemical composition of scent marks in the ringtailed lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures. Chem Senses 32:493–504PubMedCrossRefGoogle Scholar
  59. Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349CrossRefGoogle Scholar
  60. Shi P, Zhang J (2007) Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land. Genome Res 17:166–174PubMedCrossRefGoogle Scholar
  61. Singer AG, Beauchamp GK, Yamazaki K (1997) Volatile signals of the major histocompatibility complex in male mouse urine. Proc Natl Acad Sci USA 94:2210–2214PubMedCrossRefGoogle Scholar
  62. Smith TE, Tomlinson AJ, Mlotkiewicz JA, Abbott DH (2001) Female marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks. Chem Senses 26:449–458PubMedCrossRefGoogle Scholar
  63. Sockman KW, Schwabl H (1999) Daily estradiol and progesterone levels relative to laying and onset of incubation in canaries. Gen Comp Endocrinol 114:257–268PubMedCrossRefGoogle Scholar
  64. Soini HA, Schrock SE, Bruce KE, Wiesler D, Ketterson ED, Novotny MV (2007) Seasonal variation in volatile compound profiles of preen gland secretions of the dark-eyed junco (Junco hyemalis). J Chem Ecol 33:183–198PubMedCrossRefGoogle Scholar
  65. Spehr M, Kelliher KR, Li XH, Boehm T, Leinders-Zufall T, Zufall F (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 26:1961–1970PubMedCrossRefGoogle Scholar
  66. Stettenheim P (1972) The integument of birds. In: Farner DS, King JR (eds) Avian biology, vol II. Academic, New York, pp 1–63Google Scholar
  67. Toivanen P, Vaahtovuo J, Eerola E (2001) Influence of major histocompatibility complex on bacterial composition of fecal flora. Infect Immun 69:2372–2377PubMedCrossRefGoogle Scholar
  68. Wedekind C, Penn D (2000) MHC genes, body odours, and odour preferences. Nephrol Dial Transplant 15:1269–1271PubMedCrossRefGoogle Scholar
  69. Wedekind C, Seebeck T, Bettens F, Paepke AJ (1995) Mhc-dependent mate preferences in humans. Proc R Soc Lond B 260:245–249CrossRefGoogle Scholar
  70. 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
  71. Whittaker DJ, Soini HA, Atwell JW, Hollars C, Novotny MV, Ketterson ED (2010) Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav Ecol 21:608–614CrossRefGoogle Scholar
  72. Williams TD, Kitaysky AS, Vézina F (2004) Individual variation in plasma estradiol-17β and androgen levels during egg formation in the European starling Sturnus vulgaris: implications for regulation of yolk steroids. Gen Comp Endocrinol 136:346–352PubMedCrossRefGoogle Scholar
  73. Yamamoto K, Toyoda F, Tanaka S, Hayashi H, Kikuyama S (1996) Radioimmunoassay of a newt sex pheromone, sodefrin, and the influence of hormones on its level in the abdominal gland. Gen Comp Endocrinol 104:356–363PubMedCrossRefGoogle Scholar
  74. Yamazaki K, Beauchamp G, Singer AG, Bard J, Boyse EA (1999) Odortypes: their origin and composition. Proc Natl Acad Sci USA 96:1522–1525PubMedCrossRefGoogle Scholar
  75. Zhang JX, Wei W, Zhang JH, Yang WH (2010) Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chem Senses 35:375–382PubMedCrossRefGoogle Scholar
  76. Zimmer RK, Zimmer CA (2008) Dynamic scaling in chemical ecology. J Chem Ecol 34:822–836PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Sarah Leclaire
    • 1
    • 2
    • 7
  • Thomas Merkling
    • 1
    • 2
  • Christine Raynaud
    • 3
    • 4
  • Géraldine Giacinti
    • 3
    • 4
  • Jean-Marie Bessière
    • 5
  • Scott A. Hatch
    • 6
  • Étienne Danchin
    • 1
    • 2
  1. 1.CNRS, Université Paul Sabatier, ENFA; UMR5174 EDB (Laboratoire Évolution et Diversité Biologique)ToulouseFrance
  2. 2.Université de Toulouse; UMR5174 EDBToulouseFrance
  3. 3.INRA, LCA (Laboratoire de Chimie Agro-industrielle)ToulouseFrance
  4. 4.Université de Toulouse, INPT, LCA, ENSIACETToulouseFrance
  5. 5.Ecole Nationale Supérieure de Chimie de MontpellierMontpellierFrance
  6. 6.U.S. Geological Survey, Alaska Science CenterAnchorageUSA
  7. 7.Department of ZoologyUniversity of CambridgeCambridgeUK

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