Behavioral Ecology and Sociobiology

, Volume 68, Issue 11, pp 1819–1827 | Cite as

Differences in olfactory species recognition in the females of two Australian songbird species

  • E. Tobias Krause
  • Christoph Brummel
  • Sarah Kohlwey
  • Markus C. Baier
  • Caroline Müller
  • Francesco Bonadonna
  • Barbara A. Caspers
Original Paper


Although birds have recently been shown to possess olfactory abilities and to use chemical cues in communication, limited effort has been made to demonstrate the use of odorants in social contexts. Even less is known regarding the use of odorants in species recognition. The ability to recognize conspecifics should be more pronounced in social species. This study investigated the importance of olfactory cues in species recognition in females of two estrildid finch species with different levels of sociality. Combining odor preference tests with chemical analyses, we surveyed whether female zebra finches and diamond firetails are able to distinguish between the species based on volatile traits and whether individuals exhibit species-specific differences in body odorants. Zebra finches are more social than diamond firetails; nevertheless, both species have an overlapping distribution area. Applying an experimental Y-maze paradigm, we showed that zebra finches can use differences in their species odor fingerprints and displayed a significant preference for the odor of conspecifics over that of heterospecifics, whereas diamond firetails did not reveal a preference. Using gas chromatography and mass spectrometry, we demonstrated that body odorants of the two species were significantly different in relative composition. This finding demonstrates the potential importance of olfactory cues in species recognition, at least in social bird species. Even these two closely related species displayed remarkable differences in their responsiveness to similar chemical cues, which might be caused by species-specific differences in ecology, physiology, or evolution.


Songbird Zebra finch Taeniopygia guttata Diamond firetail Stagonopleura guttata Sociality Olfaction Smell Scent Olfactory fingerprint 



ETK was funded by the Volkswagen Foundation (85994). We thank Elke Hippauf for help with the sex determination of the diamond firetails and Ulla Kodytek, Gitta Otte, Michael Meierhoff, and Kristina Ruhe for taking care of the animals. We thank two anonymous reviewers for helpful comments.

Ethical standards

After the experiments, all the birds remained in our lab stocks. The experiments were performed in accordance with the current laws of the country. Housing of birds was conducted with the permission of the Gesundheits-, Veterinär- und Lebensmittelüberwachungsamt, Stadt Bielefeld, Germany (no. 530.421630-1, 18/04/2002).

Supplementary material

265_2014_1791_MOESM1_ESM.docx (94 kb)
ESM 1 (DOCX 94 kb)


  1. Alatalo RV, Gustafsson L, Lundberg A (1994) Male coloration and species recognition in sympatric flycatchers. Proc R Soc Lond B 256:113–118CrossRefGoogle Scholar
  2. Amo L, Avilés JM, Parejo D, Peña A, Rodríguez J, Tomás G (2012a) Sex recognition by odour and variation in the uropygial gland secretion in starlings. J Anim Ecol 81:605–613PubMedCrossRefGoogle Scholar
  3. Amo L, Lopez-Rull I, Pagan I, Garcia C (2012b) Male quality and conspecific scent preferences in the house finch, Carpodacus mexicanus. Anim Behav 84:1483–1489CrossRefGoogle Scholar
  4. Arnaiz-Villena A, Ruiz-Del-Valle V, Gomez-Prieto P, Reguera R, Parga-Lozano C, Serrano-Vela I (2009) Estrildinae finches (Aves, Passeriformes) from Africa, south Asia and Australia: a molecular phylogeographic study. Open Ornithol J 2:29–36CrossRefGoogle Scholar
  5. Balakrishnan CN, Edwards SV (2009) Nucleotide variation, linkage disequilibrium and founder-facilitated speciation in wild populations of the zebra finch (Taeniopygia guttata). Genetics 181:645–60PubMedCrossRefPubMedCentralGoogle Scholar
  6. Blakers M, Davies SJJF, Reilly PN (1984) The atlas of Australian birds. Melbourne University Press, MelbourneGoogle Scholar
  7. Bonadonna F, Mardon J (2010) One house two families: petrel squatters get a sniff of low-cost breeding opportunities. Ethology 116:176–182CrossRefGoogle Scholar
  8. Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science 306:835–835PubMedCrossRefGoogle Scholar
  9. Bonadonna F, Sanz-Aguilar A (2012) Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition. Anim Behav 84:509–513CrossRefGoogle Scholar
  10. Bonadonna F, Cunningham GB, Jouventin P, Hesters F, Nevitt GA (2003a) Evidence for nest-odour recognition in two species of diving petrel. J Exp Biol 206:3719–3722PubMedCrossRefGoogle Scholar
  11. Bonadonna F, Hesters F, Jouventin P (2003b) Scent of a nest: discrimination of own-nest odours in Antarctic prions, Pachyptila desolata. Behav Ecol Sociobiol 54:174–178Google Scholar
  12. 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
  13. Campagna S, Mardon J, Celerier A, Bonadonna F (2012) Potential semiochemical molecules from birds: a practical and comprehensive compilation of the last 20 years studies. Chem Senses 37:3–25PubMedCrossRefGoogle Scholar
  14. Campbell DLM, Shaw RC, Hauber ME (2009) The strength of species recognition in captive female zebra finches (Taeniopygia guttata): a comparison across estrildid heterospecifics. Ethology 115:23–32CrossRefGoogle Scholar
  15. Caspers BA, Krause ET (2011) Odour-based natal nest recognition in the zebra finch (Taeniopygia guttata), a colony-breeding songbird. Biol Lett 7:184–186PubMedCrossRefPubMedCentralGoogle Scholar
  16. Caspers BA, Krause ET (2013) Intraspecific olfactory communication in zebra finches (Taeniopygia guttata)—potential information apart from visual and acoustic cues. In: East ML, Dehnhard M (eds) Chemical signals in vertebrates 12. Springer Verlag, Berlin, pp 341–351CrossRefGoogle Scholar
  17. Caspers BA, Schroeder FC, Franke S, Streich JW, Voigt CC (2009) Odour based species recognition in two sympatric species of sac-winged bats (S. bilineata, S. leptura): combining chemical analysis and odour preference tests. Behav Ecol Sociobiol 63:741–749CrossRefGoogle Scholar
  18. Caspers BA, Hoffman JI, Kohlmeier P, Krüger O, Krause ET (2013) Olfactory imprinting as a mechanism for nest odour recognition in zebra finches. Anim Behav 86:85–90CrossRefGoogle Scholar
  19. Catchpole CK, Slater PJB (2008) Bird song—biological themes and variations, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  20. Celerier A, Bon C, Malapert A, Palmas P, Bonadonna F (2011) Chemical kin label in seabirds. Biol Lett 7:807–810PubMedCrossRefPubMedCentralGoogle Scholar
  21. Christidis L, Boles WE (2008) Systematics and taxonomy of australian birds. Csiro Publishing, CollingwoodGoogle Scholar
  22. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  23. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, PlymouthGoogle Scholar
  24. Clayton NS (1990) Subspecies recognition and song learning in zebra finches. Anim Behav 40:1009–1017CrossRefGoogle Scholar
  25. Clayton NC, Pröve E (1989) Song discrimination in female zebra finches and Bengalese finches. Anim Behav 38:352–354CrossRefGoogle Scholar
  26. Clayton NS, Hodson D, Zann R (1991) Geographic-variation in zebra finch subspecies. Emu 91:2–11CrossRefGoogle Scholar
  27. Coffin HR, Watters JV, Mateo JM (2011) Odor-based recognition of familiar and related conspecifics: a first test conducted on captive humboldt penguins (Spheniscus humboldti). PLoS One 6:e25002PubMedCrossRefPubMedCentralGoogle Scholar
  28. Cooney SJN, Watson DM (2005) Diamond firetails (Stagonopleura guttata) preferentially nest in mistletoe. Emu 105:317–322CrossRefGoogle Scholar
  29. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria,
  30. Dawley EM (1984) Recognition of individual, sex and species odors by salamanders of the Plethodon glutinosus and Plethodon jordani complex. Anim Behav 32:353–361CrossRefGoogle Scholar
  31. Emlen ST (1972) Experimental analysis of parameters of bird song eliciting species recognition. Behaviour 41:130–171CrossRefGoogle Scholar
  32. Forstmeier W, Segelbacher G, Mueller J, Kempenaers B (2007) Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Mol Ecol 16:4039–4050PubMedCrossRefGoogle Scholar
  33. Gilby A, Mainwaring M, Rollins L, Griffith S (2011) Parental care in wild and captive zebra finches: measuring food delivery to quantify parental effort. Anim Behav 81:289–295CrossRefGoogle Scholar
  34. Grant PR, Grant BR (1992) Hybridization of bird species. Science 256:193–197PubMedCrossRefGoogle Scholar
  35. Griffith SC, Holleley CE, Mariette MM, Pryke SR, Svedin N (2010) Low level of extrapair parentage in wild zebra finches. Anim Behav 79:261–264CrossRefGoogle Scholar
  36. Hagelin JC (2007) The citrus-like scent of crested auklets: reviewing the evidence for an avian olfactory ornament. J Ornithol 148:S195–S201CrossRefGoogle Scholar
  37. Hagelin JC, Jones IL, Rasmussen LEL (2003) A tangerine-scented social odour in a monogamous seabird. Proc R Soc Lond B 270:1323–1329CrossRefGoogle Scholar
  38. Hauber ME, Russo SA, Sherman PW (2001) A password for species recognition in a brood-parasitic bird. Proc R Soc Lond B 268:1041–1048CrossRefGoogle Scholar
  39. Hauber ME, Campbell DLM, Woolley SMN (2010) The functional role and female perception of male song in zebra finches. Emu 110:209–218CrossRefGoogle Scholar
  40. Hoffman JI, Krause ET, Lehmann K, Krüger O (2014) MC1R genotype and plumage colouration in the zebra finch: population structure generates artefactual associations. PLoS One 9:e86519PubMedCrossRefPubMedCentralGoogle Scholar
  41. Immelmann K (1959) Experimentelle Untersuchungen über die biologische Bedeutung artspezifischer Merkmale beim Zebrafinken (Taeniopygia castanotis Gould). Zool Jb Syst 86:437–592Google Scholar
  42. Immelmann K (1965) Australian finches in bush and aviary. Angus and Robertson Ltd., SydneyGoogle Scholar
  43. Irwin DE, Price T (1999) Sexual imprinting, learning and speciation. Heredity 82:347–354PubMedCrossRefGoogle Scholar
  44. Johnson NK, Johnson CB (1985) Speciation in sapsuckers (Sphyrapicus): II. sympatry, hybridization, and mate preference in S. ruber daggetti and S. nuchalis. Auk 102:1–15CrossRefGoogle Scholar
  45. Kelly DJ, Marples NM (2004) The effects of novel odour and colour cues on food acceptance by the zebra finch, Taeniopygia guttata. Anim Behav 68:1049–1054CrossRefGoogle Scholar
  46. Krause ET, Caspers BA (2012) Are olfactory cues involved in nest recognition in two social species of estrildid finches? PLoS One 7:e36615PubMedCrossRefPubMedCentralGoogle Scholar
  47. Krause ET, Naguib M (2011) Compensatory growth affects exploratory behaviour in zebra finches, Taeniopygia guttata. Anim Behav 81:1295–1300CrossRefGoogle Scholar
  48. Krause ET, Honarmand M, Wetzel J, Naguib M (2009) Early fasting is long lasting: differences in early nutritional conditions reappear under stressful conditions in adult female zebra finches. PLoS One 4:e5015PubMedCrossRefPubMedCentralGoogle Scholar
  49. Krause ET, Krüger O, Kohlmeier P, Caspers BA (2012) Olfactory kin recognition in a songbird. Biol Lett 8:327–329PubMedCrossRefPubMedCentralGoogle Scholar
  50. Lorbeer E, Mayr M, Hausmann B, Kratzl K (1984) Zur identifizierung flüchtiger substanzen aus biologischem material mit hilfe der CLSA (closed looped stripping apparatus). Monatsh Chem 115:1107–1112CrossRefGoogle Scholar
  51. Macedonia JM, Stamps JA (1994) Species recognition in anolis grahami (Sauria, Iguanidae)—evidence from responses to video playbacks of conspecific and heterospecific display. Ethology 98:246–264CrossRefGoogle Scholar
  52. Mainwaring MC, Hartley IR, Gilby AJ, Griffith SC (2010) Hatching asynchrony and growth trade-offs within domesticated and wild zebra finch, Taeniopygia guttata, broods. Biol J Linn Soc 100:763–773CrossRefGoogle Scholar
  53. Mardon J, Saunders SM, Anderson MJ, Couchoux C, Bonadonna F (2010) Species, gender, and identity: cracking petrels’ sociochemical code. Chem Sens 35:309–321CrossRefGoogle Scholar
  54. Matyjasiak P (2005) Birds associate species-specific acoustic and visual cues: recognition of heterospecific rivals by male blackcaps. Behav Ecol 16:467–471CrossRefGoogle Scholar
  55. Moore WS, Koenig WD (1986) Comparative reproductive success of yellow-shafted, red-shafted, and hybrid flickers across a hybrid zone. Auk 103:42–51Google Scholar
  56. Nevitt GA, Bonadonna F (2005) Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol Lett 1:303–305PubMedCrossRefPubMedCentralGoogle Scholar
  57. Nicolai J, Steinbacher J (2001) Prachtfinken - Australien, Ozeanien, Südostasien. Verlag Eugen Ulmer, StuttgartGoogle Scholar
  58. Price T (2007) Speciation in birds. Roberts & Company Publishers, Greenwood VillageGoogle Scholar
  59. Ratciliffe LM, Grant PR (1983) Species recognition in Darwin’s finches (Geospiza, Gould) I. Discrimination by morphological cues. Anim Behav 31:1139–1153CrossRefGoogle Scholar
  60. Ratcliffe LM, Grant PR (1985) Species recognition in Darwin finches (Geospiza, Gould). 3. male-responses to playback of different song types, dialects and heterospecific songs. Anim Behav 33:290–307CrossRefGoogle Scholar
  61. Riebel K (2009) Song and female mate choice in zebra finches: a review. Adv Stud Behav 40:197–238CrossRefGoogle Scholar
  62. Robiller F (1978) Prachtfinken - Vögel von drei Kontinenten. Deutscher Landwirtschaftsverlag, BerlinGoogle Scholar
  63. Ryan M, Rand A (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647–657CrossRefGoogle Scholar
  64. Searcy WA (1990) Species recognition of song by female red-winged blackbirds. Anim Behav 40:1119–1127CrossRefGoogle Scholar
  65. Seddon N (2005) Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution 59:200–215PubMedCrossRefGoogle Scholar
  66. Soini HA, Whittaker DJ, Wiesler D, Ketterson ED, Novotny MV (2013) Chemosignaling diversity in songbirds: chromatographic profiling of preen oil volatiles in different species. J Chromatogr A 1317:186–192PubMedCrossRefGoogle Scholar
  67. Sossinka R (1970) Domestikationserscheinungen beim Zebrafinken Taeniopygia guttata castanotis (Gould). Zool Jb Syst 97:455–521Google Scholar
  68. Sossinka R (1982) Domestication in birds. In: Farner DS, King JR, Parkes KC (eds) Avian Biology VI. Academic, London, pp 373–403CrossRefGoogle Scholar
  69. Suzuki K, Ikebuchi M, Okanoya K (2013) The impact of domestication on fearfulness: a comparison of tonic immobility reactions in wild and domesticated finches. Behav Process 100:58–63CrossRefGoogle Scholar
  70. ten Cate C (1984) The influence of social relations on the development of species recognition in zebra finch males. Behaviour 91:263–285CrossRefGoogle Scholar
  71. ten Cate C, Los L, Schilperoord L (1984) The influence of differences in social experience on the development of species recognition in zebra finch males. Anim Behav 32:852–860CrossRefGoogle Scholar
  72. Tschirren B, Rutstein AN, Postma E, Mariette M, Griffith SC (2009) Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches. J Evol Biol 22:387–395PubMedCrossRefGoogle Scholar
  73. Wang N, Zhang ZW (2009) The novel primers for sex identification in the brown eared-pheasant and their application to other species. Mol Ecol Res 9:186–188CrossRefGoogle Scholar
  74. 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 21:608–614PubMedCrossRefPubMedCentralGoogle Scholar
  75. Whittaker DJ, Richmond KM, Miller AK, Kiley R, Burns CB, Atwell JW, Ketterson ED (2011) Intraspecific preen oil odor preferences in dark-eyed juncos (Junco hyemalis). Behav Ecol 22:1256–1263CrossRefGoogle Scholar
  76. Wiernasz DC, Kingsolver JG (1992) Wing melanin pattern mediates species recognition in Pieris Occidentalis. Anim Behav 43:89–94CrossRefGoogle Scholar
  77. Witte K, Caspers B (2006) Sexual imprinting on a novel blue ornament in zebra finches. Behaviour 143:969–991CrossRefGoogle Scholar
  78. Würdinger I (1990) Die Reaktionen von Zebrafinken (Taeniopygia guttata) auf Düfte - eine Pilotstudie. Vogelwarte 35:359–367Google Scholar
  79. Zann RA (1996) The zebra finch—a synthesis of field and laboratory studies. Oxford University Press, OxfordGoogle Scholar
  80. Zhang YH, Du YF, Zhang JX (2013) Uropygial gland volatiles facilitate species recognition between two sympatric sibling bird species. Behav Ecol 24:1271–1278CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • E. Tobias Krause
    • 1
    • 2
  • Christoph Brummel
    • 1
  • Sarah Kohlwey
    • 1
  • Markus C. Baier
    • 3
  • Caroline Müller
    • 3
  • Francesco Bonadonna
    • 4
  • Barbara A. Caspers
    • 1
  1. 1.Department of Animal BehaviourBielefeld UniversityBielefeldGermany
  2. 2.Behavioural Ecology Group, Department of Animal SciencesWageningen UniversityWageningenThe Netherlands
  3. 3.Department of Chemical EcologyBielefeld UniversityBielefeldGermany
  4. 4.Centre d’Ecologie Fonctionnelle et EvolutiveCNRS, UMR 5175MontpellierFrance

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