Abstract
Odours are broadly used for individual, sexual and species recognition in vertebrates and may be reliable signals of quality and compatibility. Yet, chemical signals in birds have rarely been investigated. In fact, birds exhibit a wide array of communication mechanisms (e.g. colours and calls) but rarely display obvious olfactory-driven behaviours. This is probably why, despite three decades of physiological and behavioural studies establishing the existence of avian olfactory functions, chemical communication has been essentially ignored.
In spite of the fact that pheromones have never been highlighted in birds, several species produce characteristic scents that may have a social function. For example, odours seem to contribute to the courtship behaviours of ducks and chickens. In crested auklets, a characteristic citrus odour may act as a sexual olfactory ornament broadcasting resistance to ectoparasites. Eventually, it was shown that zebra finches (a passerine bird with a very small olfactory apparatus) display olfactory-driven behaviours.
Petrel seabirds are probably the most striking case-study, since findings relating to many aspects of petrels’ ecology including homing, recognition, mate choice and even interspecific competition for nesting sites, provide a comprehensive evidence for avian chemical communication. Some burrowing petrels use the odour of their mate to recognise their own nest and, interestingly, prefer the odour of a conspecific to their own. Using chemical analytical methods, it has been demonstrated that the preen secretions of these birds contain social information including species, sex and identity (i.e. a chemical signature). Results further show that some of this information is still present on the plumage and in the airborne volatiles emitted by birds. Recent results also show that “detective mice” (i.e. biological olfactometers) can identify similarities in individual kin-related petrel odours. Also, one species of storm petrel has been shown to recognise and avoid kin-related conspecifics in choice experiments.
Together, these results, almost 50 years after the first works on avian olfaction, indicate that chemical signals can contribute, as well as colours, calls and songs, to avian social behaviours; a realisation that has important implications for behavioural processes such as individual recognition and/or mate choice.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ables EM, Kay LM, Mateo JM (2007) Rats assess degree of relatedness from human odors. Physiol Behav 90:726–732
Amo L, Galvan I, Tomas G, Sanz JJ (2008) Predator odour recognition and avoidance in a songbird. Funct Ecol 22:289–293
Balthazart J, Schoffeniels E (1979) Pheromones are involved in the control of sexual behavior in birds. Naturwissenschaften 66:55–56
Balthazart J, Taziaux M (2009) The underestimated role of olfaction in avian reproduction? Behav Brain Res 200:248–259
Benham WB (1906) The olfactory sense in Apteryx. Nature 74:222–223
Benvenuti S, Fiaschi V, Foà A (1977) Homing behaviour of pigeons disturbed by application of an olfactory stimulus. J Comp Physiol A 120:175–179
Bertmar G (1981) Evolution of vomeronasal organs in vertebrates. Evolution 35:359–366
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 266:9795–9804
Bonadonna F (2009) Olfaction in petrels: from homing to self-odor avoidance. Ann N Y Acad Sci 1170:428–433
Bonadonna F, Mardon J (2010) One house two families: petrel squatters get a sniff of low-cost breeding opportunities. Ethology 116:176–182
Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science 306:835
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 84:509–513
Bonadonna F, Spaggiari J, Weimerskirch H (2001) Could osmotaxis explain the ability of blue petrels to return to their burrows at night? J Exp Biol 204:1485–1489
Bonadonna F, Hesters F, Jouventin P (2003) Scent of a nest: discrimination of own-nest odours in Antarctic prions, Pachyptila desolata. Behav Ecol Sociobiol 54:174–178
Bonadonna F, Villafane M, Bajzak C, Jouventin P (2004) Recognition of burrow’s “olfactory signature” in blue petrels, Halobaena caerulea: an efficient discrimination mechanism in the dark. Anim Behav 67:893–898
Bonadonna F, Miguel E, Grosbois V, Jouventin P, Bessiere JM (2007) Individual-specific odour recognition in birds: an endogenous olfactory signature on petrels’ feathers? J Chem Ecol 33:1819–1829
Bonadonna F, Caro S, Brooke M (2009) Olfactory sex recognition investigated in Antarctic prions. PLoS One 4:e4148. doi:10.1371/journal.pone.0004148
Bonneaud C, Chastel O, Federici P, Westerdahl H, Sorci G (2006) Complex MHC-based mate choice in a wild passerine. Proc R Soc Lond B Biol Sci 273:1111–1116
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland, MA
Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B Biol Sci 361:2061–2078
Burgener N, East ML, Hofer H, Dehnhard M (2008) Do spotted hyena scent marks code for clan membership? In: Hurst JL, Beynon RJ, Roberts S, Wyatt TD (eds) Chemical signals in vertebrates, vol XI. Springer, New York, pp 169–177
Burgener N, Dehnhard M, Hofer H, East ML (2009) Does anal gland scent signal identity in the spotted hyaena? Anim Behav 77:707–715
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 30:1603–1611
Caspers BA, Krause ET (2011) Odour-based natal nest recognition in the zebra finch (Taeniopygia guttata), a colony-breeding songbird. Biol Lett 7:184–186
Celerier A, Alvergne A, Huchard E, Fejan D, Plard F, Cowlishaw G, Raymond M, Bonadonna F (2010) Detective mice assess relatedness in baboons inquiring into olfactory clues. J Exp Biol 213:1399–1405
Celerier A, Bon C, Malapert A, Palmas P, Bonadonna F (2011) Chemical kin label in seabirds. Biol Lett 7:807–810
Cherel Y, Bocher P, De Broyer C, Hobson KA (2002a) Food and feeding ecology of the sympatric thin-billed Pachyptila belcheri and Antarctic P. desolata prions at Iles Kerguelen, Southern Indian Ocean. Mar Ecol Prog Ser 228:263–281
Cherel Y, Bocher P, Trouve C, Weimerskirch H (2002b) Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, Southern Indian Ocean. Mar Ecol Prog Ser 228:283–299
Clark L, Mason JR (1985) Use the nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67:169–176
Culik B (2001) Finding food in the open ocean: foraging strategies in Humboldt penguins. Zoology 104:327–338
Cunningham GB, Strauss V, Ryan PG (2008) African penguins (Spheniscus demersus) can detect dimethyl sulphide, a prey-related odour. J Exp Biol 211:3123–3127
De Leon A, Minguez E, Belliure B (2003) Self-odour recognition in European storm-petrel chicks. Behaviour 140:925–933
Diamond JM (1992) Rubbish birds are poisonous. Nature 360:19–20
Douglas HD (2008) Prenuptial perfume: alloanointing in the social rituals of the crested auklet (Aethia cristatella) and the transfer of arthropod deterrents. Naturwissenschaften 95:45–53
Dumbacher JP (1999) Evolution of toxicity in pitohuis: I. Effects of homobatrachotoxin on chewing lice (order Phthiraptera). Auk 116:957–963
Dumbacher JP, Beehler BM, Spande TF, Garraffo HM, Daly JW (1992) Homobatrachotoxin in the genus Pitohui: chemical defense in birds? Science 258:799–800
Dumbacher J, Spande TF, Daly JW (2000) Batrachotoxin alkaloids from passerine birds: a second toxic bird genus (Ifrita kowaldi) from New Guinea. Proc Natl Acad Sci U S A 97:12970–12975
Ekblom R, Saether SA, Grahn M, Fiske P, Kalas JA, Hoglund J (2004) Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media). Mol Ecol 13:3821–3828
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 12:3077–3083
Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121
Gillingham MAF, Richardson DS, Lovlie H, Moynihan A, Worley K, Pizzari T (2009) Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. Proc R Soc Lond 276:1083–1092
Grubb TC (1972) Smell and foraging in shearwaters and petrels. Nature 237:404–405
Gwinner H (1997) The function of green plants in nests of European starlings (Sturnus vulgaris). Behaviour 134:337–351
Gwinner H, Berger S (2005) European starlings: nestling condition, parasites and green nest material during the breeding season. J Ornithol 146:365–371
Gwinner H, Berger S (2008) Starling males select green nest material by olfaction using experience-independent and experience-dependent cues. Anim Behav 75:971–976
Gwinner H, Oltrogge M, Trost L, Nienaber U (2000) Green plants in starling nests: effects on nestlings. Anim Behav 59:301–309
Hagelin JC (2004) Observations on the olfactory ability of the Kakapo Strigops habroptilus, the critically endangered parrot of New Zealand. Ibis 146:161–164
Hagelin JC (2007) The citrus-like scent of crested auklets: reviewing the evidence for an avian olfactory ornament. J Ornithol 148:S195–S201
Hagelin JC (2008) New data and new questions for Crested Auklet research. Auk 125:497–498
Hagelin JC, Jones IL (2007) Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 124:741–761
Hagelin JC, Jones IJ, Rasmussen LEL (2003) A tangerine-scented social odour in a monogamous seabird. Proc R Soc Lond B Biol Sci 270:1323–1329
Hagey L, MacDonald E (2003) Chemical cues identify gender and individuality in giant pandas (Ailuropoda melanoleuca). J Chem Ecol 29:1479–1488
Hauser MD (1996) The evolution of communication. MIT Press, Cambridge, MA
Hirao A, Aoyama M, Sugita S (2009) The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus. Behav Process 80:115–120
Jacob J (1976) Chemotaxonomical relationships between penguins and tubenoses. Biochem Syst Ecol 4:215–221
Jacob J, Ziswiler V (1982) The uropygial gland. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 6. Academic, New York, pp 199–324
Jacob J, Balthazart J, Schoffeniels E (1979) Sex differences in the chemical composition of uropygial gland waxes in domestic ducks. Biochem Syst Ecol 7:149–153
Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289
Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299
Jones IL, Hunter FM (1993) Mutual sexual selection in a monogamous seabird. Nature 362:238–239
Jones IL, Hagelin JC, Major HL, Rasmussen LEL (2004) An experimental field study of the function of Crested Auklet feather odor. Condor 106:71–78
Jouventin P, Mouret V, Bonadonna F (2007) Wilson’s storm petrels Oceanites oceanicus recognise the olfactory signature of their mate. Ethology 113:1228–1232
Karlson P, Lüscher M (1959) ‘Pheromones’: a new term for a class of biologically active substances. Nature 183:155–156
Law-Brown J (2001) Chemical defence in the Red-billed Woodhoopoe Phoneiculus purpureus. MSc Thesis, University of Cape Town, Rondebosch, South Africa
Mardon J, Bonadonna F (2009) Atypical homing or self-odour avoidance? Blue petrels (Halobaena caerulea) are attracted to their mate’s odour but avoid their own. Behav Ecol Sociobiol 63:537–542
Mardon J, Saunders SM, Anderson MJ, Couchoux C, Bonadonna F (2010a) Species, gender, and identity: cracking petrels’ sociochemical code. Chem Senses 35:309–321
Mardon J, Saunders SM, Bonadonna F (2010b) Comments on recent work by Zhang & colleagues: ‘Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars’. Chem Senses 36:3–4
Mardon J, Saunders SM, Bonadonna F (2011) From preen secretions to plumage: the chemical trajectory of petrels’ social scent. J Avian Biol 42:29–38
Mennerat A (2008) Blue tits (Cyanistes caeruleus) respond to an experimental change in the aromatic plant odour composition of their nest. Behav Process 79:189–191
Mennerat A, Bonadonna F, Perret P, Lambrechts MM (2005) Olfactory conditioning experiments in a food-searching passerine bird in semi-natural and natural conditions. Behav Process 70:264–270
Montalti D, Gutierrez AM, Reboredo G, Salibian A (2005) The chemical composition of the uropygial gland secretion of rock dove Columba livia. Comp Biochem Physiol A Mol Integrat Physiol 140:275–279
Moore PJ, Reagan-Wallin NL, Haynes KF, Moore AJ (1997) Odour conveys status on cockroaches. Nature 389:25–26
Nevitt GA (2000) Olfactory foraging by Antarctic procellariiform seabirds: life at high Reynolds numbers. Biol Bull (Woods Hole) 198:245–253
Nevitt GA (2008) Sensory ecology on the high seas: the odor world of the procellariiform seabirds. J Exp Biol 211:1706–1713
Nevitt GA, Bonadonna F (2005) Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol Lett 1:303–305
Nevitt GA, Bergstrom DM, Bonadonna F (2006) The potential roles of ammonium as signal molecule for procellariiform seabirds. Mar Ecol Prog Ser 315:271–277
Papi F, Ioalè P, Fiaschi V, Benvenuti S, Baldaccini NE (1974) Olfactory navigation of pigeons: the effect of treatment with odorous air currents. J Comp Physiol A 94:187–193
Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21
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 4:331–340
Petit C, Hossaert-McKey M, Perret P, Blondel J, Lambrechts MM (2002) Blue tits use selected plants and olfaction to maintain an aromatic environment for nestlings. Ecol Lett 5:585–589
Piersma T, Dekker M, Sinninghe Damsté JS (1999) An avian equivalent of make-up? Ecol Lett 2:201–203
Pycraft WP (1910) A history of birds. Methuen and Co., London
Reneerkens J, Piersma T, Damste JS (2002) Sandpipers (Scolopacidae) switch from monoester to diester preen waxes during courtship and incubation, but why? Proc R Soc Lond 269:2135–2139
Reneerkens J, Piersma T, Sinninghe Damsté JS (2005) Switch to diester preen waxes may reduce avian nest predation by mammalian predators using olfactory cues. J Exp Biol 208:4199–4202
Reusch TBH, Häberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300–302
Richardson DS, Komdeur J, Burke T, von Schantz T (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc R Soc Lond B Biol Sci 272:759–767
Roper TJ (1999) Olfaction in birds. Adv Study Behav 28:247–332
Roper TJ (2003) Olfactory discrimination in yellow-backed Chattering Lories Lorius garrulus flavopalliatus: first demonstration of olfaction in Psittaciformes. Ibis 145:689–691
Roth TC, Cox JG, Lima SL (2008) Can foraging birds assess predation risk by scent? Anim Behav 76:2021–2027
Safi K, Kerth G (2003) Secretions of the interaural gland contain information about individuality and colony membership in the Bechstein’s bat. Anim Behav 65:363–369
Shallenberger RJ (1975) Olfactory use in the wedge-tailed shearwater (Puffinus pacificus) on Manana is (Hawaii). In: Denton A, Coughlan JP (eds) Olfaction and taste, vol V. Academic, London, pp 355–359
Singer AG, Beauchamp GK, Yamazaki K (1997) Volatile signals of the major histocompatibility complex in male mouse urine. Proc Natl Acad Sci U S A 94:2210–2214
Smith SA, Paselk RA (1986) Olfactory sensitivity of the Turkey Vulture (Cathartes avra) to three carrion-associated. Auk 103:586–592
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 26:449–458
Soudek S (1929). The sense of smell in birds. In: Proceedings of Xe Congres International de Zoology, Budapest, pp 755–765
Stager KE (1967) Avian olfaction. Am Zool 7:415–419
Strandh M, Lannefors M, Bonadonna F, Westerdahl H (2011) Characterization of MHC class I and II genes in a subantarctic seabird, the Blue Petrel, Halobaena caerulea (Procellariiformes). Immunogenetics 63:653–666
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027
Wallraff HG (2004) Avian olfactory navigation: its empirical foundation and conceptual state. Anim Behav 67:189–204
Walter WE (1943) Some experiments on the sense of smell in birds. Arch Neerl Physiol Homme Anim 27:1–72
Wedekind C, Furi S (1997) Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc R Soc Lond B Biol Sci 264:1471–1479
Weldon PJ, Rappole JH (1997) A survey of birds odorous or unpalatable to humans: possible indications of chemical defense. J Chem Ecol 23:2609–2633
Wenzel BM (1968) The olfactory prowess of the kiwi. Nature 220:1133–1134
Wenzel B (1973) Chemoreception. In: Farner DS, King JR (eds) Avian biology, vol 3. Academic, New York, pp 389–415
Wenzel BM (2007) Avian olfaction: then and now. J Ornithol 148:S191–S194
Westerdahl H (2004) No evidence of an MHC-based female mating preference in great reed warblers. Mol Ecol 13:2465–2470
Whelan CJ, Dilger ML, Robson D, Hallyn N, Dilger S (1994) Effects of olfactory cues on artificial-nest experiments. Auk 111:945–952
Whittaker DJ, Reichard DG, Dapper AL, Ketterson ED (2009) Behavioral responses of nesting female dark-eyed juncos Junco hyemalis to hetero- and conspecific passerine preen oils. J Avian Biol 40:579–583
Wright KLB, Pichegru L, Ryan PG (2011) Penguins are attracted to dimethyl sulphide at sea. J Exp Biol 214:2509–2511
Zala SM, Penn DJ (2004) Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Anim Behav 68:649–664
Zelano B, Edwards SE (2002) An MHC component to kin recognition and mate choice in birds: predictions, progress, and prospects. Am Nat 160:225–238
Zhang JX, Wei W, Zhang JH, Yang WH (2010) Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chem Senses 35:375–382
Acknowledgements
Our own work presented here was supported by Institut Polaire Français Paul Emile Victor (IPEV, Program no. 354), and by Agence Nationale de la Recherche Française (AMBO ANR-08-BLAN-0117-01 to FB).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Bonadonna, F., Mardon, J. (2013). Besides Colours and Songs, Odour is the New Black of Avian Communication. In: East, M., Dehnhard, M. (eds) Chemical Signals in Vertebrates 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5927-9_26
Download citation
DOI: https://doi.org/10.1007/978-1-4614-5927-9_26
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-5926-2
Online ISBN: 978-1-4614-5927-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)