Research progress on olfactory communication in the social behaviours of birds

doi:10.17520/biods.2022219

Abstract

Abstract:

Background: Historically, it was believed that birds had a weak sense of smell or a lack thereof. Currently, the evidence of avian olfaction has been confirmed in several fields, such as anatomy, electrophysiology, molecular biology, and behavioural ecology. In this paper, we conducted a review of recent research progress on olfactory communication in social behaviours of birds.

Results:Our literature review found evidence of olfactory communication in birds from 14 orders and 33 families. Olfaction may play an important role in functions such as foraging, navigation, defence, crypsis, vigilance, and social interactions. Focusing on the role of olfactory communication in the social behaviors of birds, we presented key results from relevant studies in the last decade and reviewed the potential roles played by avian olfaction in species and individual recognition, breeding behaviors, kin recognition, mate choice, and competition.

Conclusions: Innovations in research methods and integrative approaches are urgently needed. Combining molecular biology, anatomy, physiology, ethology, and neurobiology may comprehensively reveal the complex mechanisms and social functions of avian olfactory communication.

Key words: olfaction, social behaviours, species recognition, kin recognition, mate choice

Chen Zeng, Yang Liu. Research progress on olfactory communication in the social behaviours of birds[J]. Biodiv Sci, 2022, 30(11): 22219.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2022219

https://www.biodiversity-science.net/EN/Y2022/V30/I11/22219

Figures/Tables 2

Fig. 1 The phylogenetic tree for all bird families. Species in 14 orders and 33 families with evidence of olfactory communication in current studies are marked in blue. The tree was built under the taxonomy of BirdLife International (11,009 species in 243 families), and the mapping was done in R 4.1.3 using the packages ggplot2 and ggtree.

Fig. 2 The research framework of olfactory communication in birds. The black text and arrows represent olfactory-related factors and their transmission directions (dashed lines represent potential associations for which there is no conclusive evidence); the five boxes represent the five levels of division proposed in this review.

References 90

[1]	Abankwah V, Deeming DC, Pike TW (2020) Avian olfaction: A review of the recent literature. Comparative Cognition & Behavior Reviews, 15, 149-161.
[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. Journal of Animal Ecology, 81, 605-613.
[3]	Amo L, López-Rull I, Pagán I,Macías Garcia C (2012b) Male quality and conspecific scent preferences in the house finch, Carpodacus mexicanus. Animal Behaviour, 84, 1483-1489.
[4]	Amo L, Tomás G, Parejo D, Avilés JM (2014) Are female starlings able to recognize the scent of their offspring? PLoS ONE, 9, e109505.
[5]	Amundsen T (2000) Why are female birds ornamented? Trends in Ecology & Evolution, 15, 149-155.
[6]	Audubon JJ (1826) Account of the habits of the Turkey buzzard, Vultur aura, particularly with the view of exploding the opinion generally entertained of its extraordinary power of smelling Edinburgh New Philosophical Journal, 2, e184.
[7]	Balthazart J, Schoffeniels E (1979) Pheromones are involved in the control of sexual behaviour in birds. Die Naturwissenschaften, 66, 55-56.
[8]	Bang BG (1971) Functional anatomy of the olfactory system in 23 orders of birds. Acta Anatomica, 79, 1-76. PMID
[9]	Barrera-Guzmán AO, Aleixo A, Shawkey MD, Weir JT (2018) Hybrid speciation leads to novel male secondary sexual ornamentation of an Amazonian bird. Proceedings of the National Academy of Sciences, USA., 115, E218-E225.
[10]	Belliure B, Mínguez E,de León A (2003) Self-odour recognition in European storm-petrel chicks. Behaviour, 140, 925-933.
[11]	Bonadonna F, Caro SP, Brooke ML (2009) Olfactory sex recognition investigated in Antarctic prions. PLoS ONE, 4, e4148.
[12]	Bonadonna F, Cunningham GB, Jouventin P, Hesters F, Nevitt GA (2003) Evidence for nest-odour recognition in two species of diving petrel. Journal of Experimental Biology, 206, 3719-3722. PMID
[13]	Bonadonna F, Mardon J (2013) Besides colours and songs, odour is the new black of avian communication. In: Chemical Signals in Vertebrates 12 (eds East M, Dehnhard M), pp. 325-339, New York, NY.
[14]	Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science, 306, 835. PMID
[15]	Bonadonna F, Sanz-Aguilar A (2012) Kin recognition and inbreeding avoidance in wild birds: The first evidence for individual kin-related odour recognition. Animal Behaviour, 84, 509-513.
[16]	Breed MD (2014) Kin and nestmate recognition: The influence of W. D. Hamilton on 50 years of research. Animal Behaviour, 92, 271-279.
[17]	Campagna S, Mardon J, Celerier A, Bonadonna F (2011) Potential semiochemical molecules from birds: A practical and comprehensive compilation of the last 20 years studies. Chemical Senses, 37, 3-25.
[18]	Caro SP, Balthazart J, Bonadonna F (2015) The perfume of reproduction in birds: Chemosignaling in avian social life. Hormones and Behavior, 68, 25-42. DOI PMID
[19]	Caspers BA, Gagliardo A, Krause ET (2015) Impact of kin odour on reproduction in zebra finches. Behavioral Ecology and Sociobiology, 69, 1827-1833.
[20]	Caspers BA, Hagelin JC, Paul M, Bock S, Willeke S, Krause ET (2017) Zebra finch chicks recognise parental scent, and retain chemosensory knowledge of their genetic mother, even after egg cross-fostering. Scientific Reports, 7, 1-8.
[21]	Caspers BA, Hoffman JI, Kohlmeier P, Krüger O, Krause ET (2013) Olfactory imprinting as a mechanism for nest odour recognition in zebra finches. Animal Behaviour, 86, 85-90.
[22]	Caspers BA, Krause ET (2011) Odour-based natal nest recognition in the zebra finch (Taeniopygia guttata), a colony-breeding songbird. Biology Letters, 7, 184-186. DOI PMID
[23]	Caspers BA, Krause ET (2013) Intraspecific olfactory communication in zebra finches (Taeniopygia guttata):Potential information apart from visual and acoustic cues. In: Chemical Signals in Vertebrates 12 (eds East M, Dehnhard M), pp. 341-351 New York, NY.
[24]	Cava JA, Perlut NG, Travis SE (2016) Why come back home? Investigating the proximate factors that influence natal philopatry in migratory passerines. Animal Behaviour, 118, 39-46.
[25]	Célérier A, Bon C, Malapert A, Palmas P, Bonadonna F (2011) Chemical kin label in seabirds. Biology Letters, 7, 807-810. DOI PMID
[26]	Chung H, Carroll SB (2015) Wax, sex and the origin of species: Dual roles of insect cuticular hydrocarbons in adaptation and mating. BioEssays, 37, 822-830. DOI PMID
[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, e25002.
[28]	Corfield JR, Price K, Iwaniuk AN, Gutierrez-Ibañez C, Birkhead T, Wylie DR (2015) Diversity in olfactory bulb size in birds reflects allometry, ecology, and phylogeny. Frontiers in Neuroanatomy, 9, 102. DOI PMID
[29]	Cruz-Yepez N, González C, Ornelas JF (2020) Vocal recognition suggests premating isolation between lineages of a lekking hummingbird. Behavioral Ecology, 31, 1046-1053.
[30]	Driver RJ, Balakrishnan CN (2021) Highly contiguous genomes improve the understanding of avian olfactory receptor repertoires. Integrative and Comparative Biology. 61, 1281-1290.
[31]	Fracasso G, Tuliozi B, Hoi H, Griggio M (2018) Can house sparrows recognize familiar or kin-related individuals by scent? Current Zoology, 65, 53-59.
[32]	Gagliardo A (2013) Forty years of olfactory navigation in birds. Journal of Experimental Biology, 216, 2165-2171.
[33]	Gagliardo A, Ioalè P, Filannino C, Wikelski M (2011) Homing pigeons only navigate in air with intact environmental odours: A test of the olfactory activation hypothesis with GPS data loggers. PLoS ONE, 6, e22385.
[34]	Gagliardo A, Pollonara E, Wikelski M (2018) Only natural local odours allow homeward orientation in homing pigeons released at unfamiliar sites. Journal of Comparative Physiology, 204, 761-771.
[35]	Golüke S, Bischof HJ, Caspers BA (2021) Nestling odour modulates behavioural response in male, but not in female zebra finches. Scientific Reports, 11, 712. DOI PMID
[36]	Golüke S, Bischof HJ, Engelmann J, Caspers BA, Mayer U (2019) Social odour activates the hippocampal formation in zebra finches (Taeniopygia guttata). Behavioural Brain Research, 364, 41-49. DOI PMID
[37]	Golüke S, Dörrenberg S, Krause ET, Caspers BA (2016) Female zebra finches smell their eggs. PLoS ONE, 11, e0155513.
[38]	Grieves LA, Bernards MA, MacDougall-Shackleton EA (2019a) Behavioural responses of songbirds to preen oil odour cues of sex and species. Animal Behaviour, 156, 57-65.
[39]	Grieves LA, Gilles M, Cuthill IC, Székely T, MacDougall-Shackleton EA, Caspers BA (2022) Olfactory camouflage and communication in birds. Biological Reviews, 97, 1193-1209.
[40]	Grieves LA, Gloor GB, Bernards MA, MacDougall-Shackleton EA (2019b) Songbirds show odour-based discrimination of similarity and diversity at the major histocompatibility complex. Animal Behaviour. 158, 131-138.
[41]	Griggio M, Fracasso G, Mahr K, Hoi H (2016) Olfactory assessment of competitors to the nest site: An experiment on a passerine species. PLoS ONE, 11, e0167905.
[42]	Hill A (1905) Can birds smell? Nature, 71, 318-319.
[43]	Hirao A, Aoyama M, Sugita S (2009) The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus. Behavioural Processes, 80, 115-120.
[44]	Jorge PE, Marques PA, Phillips JB (2010) Activational effects of odours on avian navigation. Proceedings of the Royal Society B: Biological Sciences, 277, 45-49.
[45]	Kenyon HL, Toews DPL, Irwin DE (2011) Can song discriminate between Macgillivray’s and Mourning warblers in a narrow hybrid zone? The Condor, 113, 655-663.
[46]	Krause ET, Brummel C, Kohlwey S, Baier MC, Müller C, Bonadonna F, Caspers BA (2014) Differences in olfactory species recognition in the females of two Australian songbird species. Behavioral Ecology and Sociobiology, 68, 1819-1827.
[47]	Krause ET, Caspers BA (2012) Are olfactory cues involved in nest recognition in two social species of estrildid finches? PLoS ONE, 7, e36615.
[48]	Krause ET, Krüger O, Kohlmeier P, Caspers BA (2012) Olfactory kin recognition in a songbird. Biology Letters, 8, 327-329. DOI PMID
[49]	Leclaire S, Bourret V, Bonadonna F (2017a) Blue petrels recognize the odor of their egg. Journal of Experimental Biology, 220, 3022-3025.
[50]	Leclaire S, Strandh M, Mardon J, Westerdahl H, Bonadonna F (2017b) Odour-based discrimination of similarity at the major histocompatibility complex in birds. Proceedings of the Royal Society B: Biological Sciences, 284, 20162466.
[51]	Leclaire S, Voccia S, Merkling T, Ducamp C, Hatch SA, Blanchard P, Danchin É, Wagner RH (2014) Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird. Scientific Reports, 4, 6920. DOI PMID
[52]	Li ZQ, Courchamp F, Blumstein DT (2016) Pigeons home faster through polluted air. Scientific Reports, 6, 18989. DOI PMID
[53]	Mäntylä E, Kipper S, Hilker M (2020) Insectivorous birds can see and smell systemically herbivore-induced pines. Ecology and Evolution, 10, 9358-9370. DOI PMID
[54]	Maraci Ö, Engel K, Caspers BA (2018) Olfactory communication via microbiota: What is known in birds? Genes, 9, 387.
[55]	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. Behavioral Ecology and Sociobiology, 63, 537-542.
[56]	Mariette MM, Griffith SC (2012) Conspecific attraction and nest site selection in a nomadic species, the zebra finch. Oikos, 121, 823-834.
[57]	Mennerat A (2008) Blue tits (Cyanistes caeruleus) respond to an experimental change in the aromatic plant odour composition of their nest. Behavioural Processes, 79, 189-191. DOI PMID
[58]	Mihailova M, Berg ML, Buchanan KL, Bennett ATD (2014) Odour-based discrimination of subspecies, species and sexes in an avian species complex, the crimson rosella. Animal Behaviour, 95, 155-164.
[59]	Miller SE, Legan AW, Flores ZA, Ng HY, Sheehan MJ (2018) Strong, but incomplete, mate choice discrimination between two closely related species of paper wasp. Biological Journal of the Linnean Society, 126, 614-622.
[60]	Mora CV, Davison M, Martin WJ, Walker MM (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature, 432, 508-511.
[61]	Moreno-Rueda G (2017) Preen oil and bird fitness: A critical review of the evidence. Biological Reviews, 92, 2131-2143.
[62]	Nevitt GA, Prada PA (2015) The Chemistry of Avian Odors: An Introduction to Best Practices. In: Handbook of Olfaction and Gustation (ed. Doty RL), pp. 565-578. Wiley Blackwell, New Jersey.
[63]	Nie YG, Swaisgood RR, Zhang ZJ, Hu YB, Ma YS, Wei FW (2012) Giant panda scent-marking strategies in the wild: Role of season, sex and marking surface. Animal Behaviour, 84, 39-44.
[64]	Overath P, Sturm T, Rammensee HG (2014) Of volatiles and peptides: In search for MHC-dependent olfactory signals in social communication. Cellular and Molecular Life Sciences, 71, 2429-2442. DOI PMID
[65]	Papi F, Fiore L, Fiaschi V, Benvenuti S (1972) Olfaction and homing in pigeons. Italian Journal of Zoology, 6, 85-95.
[66]	Patel RM, Pinto JM (2014) Olfaction: Anatomy, physiology, and disease. Clinical Anatomy, 27, 54-60. DOI PMID
[67]	Price-Waldman RM, Shultz AJ, Burns KJ (2020) Speciation rates are correlated with changes in plumage color complexity in the largest family of songbirds. Evolution, 74, 1155-1169. DOI PMID
[68]	Rekdal SL, Anmarkrud JA, Lifjeld JT, Johnsen A (2019) Extra-pair mating in a passerine bird with highly duplicated major histocompatibility complex class II: Preference for the golden mean. Molecular Ecology, 28, 5133-5144. DOI PMID
[69]	Rosenthal GG, Rosenthal G (2017) Mate Choice:The Evolution of Sexual Decision Making from Microbes to Humans. Princeton University Press, Princeton, NJ.
[70]	Rossi M, Marfull R, Golüke S, Komdeur J, Korsten P, Caspers BA (2017) Begging blue tit nestlings discriminate between the odour of familiar and unfamiliar conspecifics. Functional Ecology, 31, 1761-1769.
[71]	Sardell RJ, Kempenaers B, DuVal EH (2014) Female mating preferences and offspring survival: Testing hypotheses on the genetic basis of mate choice in a wild lekking bird. Molecular Ecology, 23, 933-946. DOI PMID
[72]	Schausberger P (2007) Kin recognition by juvenile predatory mites: Prior association or phenotype matching? Behavioral Ecology and Sociobiology, 62, 119-125.
[73]	Shaw CL, Rutter JE, Austin AL, Garvin MC, Whelan RJ (2011) Volatile and semivolatile compounds in gray catbird uropygial secretions vary with age and between breeding and wintering grounds. Journal of Chemical Ecology, 37, 329-339. DOI PMID
[74]	Slade JWG, Watson MJ, Kelly TR, Gloor GB, Bernards MA, MacDougall-Shackleton EA (2016) Chemical composition of preen wax reflects major histocompatibility complex similarity in songbirds. Proceedings of the Royal Society B: Biological Sciences, 283, 20161966.
[75]	Stager KE (1967) Avian olfaction. American Zoologist, 7, 415-420.
[76]	Steiger SS, Fidler AE, Valcu M, Kempenaers B (2008) Avian olfactory receptor gene repertoires:Evidence for a well-developed sense of smell in birds? Proceedings of the Royal Society B: Biological Sciences, 275, 2309-2317.
[77]	Tuttle EM, Sebastian PJ, Posto AL, Soini HA, Novotny MV, Gonser RA (2014) Variation in preen oil composition pertaining to season, sex, and genotype in the polymorphic white-throated sparrow. Journal of Chemical Ecology, 40, 1025-1038. DOI PMID
[78]	Van Huynh A, Rice AM (2019) Conspecific olfactory preferences and interspecific divergence in odor cues in a chickadee hybrid zone. Ecology and Evolution, 9, 9671-9683. DOI
[79]	Wallraff HG (1970) Further aviary experiments with homing pigeons: Probable influence of dynamic factors of the atmosphere on their orientation. Journal of Comparative Physiology, 68, 182-201.
[80]	Walter WG (1942) Some Experiments on the Sense of Smell in Birds: Studied by the Method of Conditioned Reflexes. PhD dissertation, University of Amsterdam, Amsterdam.
[81]	Whittaker DJ, Gerlach NM, Soini HA, Novotny MV, Ketterson ED (2013) Bird odour predicts reproductive success. Animal Behaviour, 86, 697-703.
[82]	Whittaker DJ, Hagelin JC (2021) Female-based patterns and social function in avian chemical communication. Journal of Chemical Ecology, 47, 43-62. DOI PMID
[83]	Whittaker DJ, Kuzel M, Burrell MJ, Soini HA, Novotny MV, DuVal EH (2019) Chemical profiles reflect heterozygosity and seasonality in a tropical lekking passerine bird. Animal Behaviour, 151, 67-75.
[84]	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. Journal of Avian Biology, 40, 579-583.
[85]	Whittaker DJ, Richmond KM, Miller AK, Kiley R, Bergeon BC, Atwell JW, Ketterson ED (2011) Intraspecific preen oil odor preferences in dark-eyed juncos (Junco hyemalis). Behavioral Ecology, 22, 1256-1263.
[86]	Winternitz J, Abbate JL, Huchard E, Havlíček J, Garamszegi LZ (2017) Patterns of MHC-dependent mate selection in humans and nonhuman primates: A meta-analysis. Molecular Ecology, 26, 668-688. DOI PMID
[87]	Yu C, You ZQ, Wan Y, Li ZQ (2021) Effects of air pollution on individual performance in homing pigeon. Chinese Journal of Zoology, 56, 8-15. (in Chinese with English abstract)
	[于丛, 游章强, 万月, 李忠秋 (2021) 空气污染对信鸽比赛个体归巢速度的影响. 动物学杂志, 56, 8-15.]
[88]	Zhang JX, Sun LX, Zuo MX (2009) Uropygial gland volatiles may code for olfactory information about sex, individual, and species in Bengalese finches Lonchura striata. Current Zoology, 55, 357-365.
[89]	Zhang JX, Wei W, Zhang JH, Yang WH (2010) Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chemical Senses, 35, 375-382.
[90]	Zhang YH, Du YF, Zhang JX (2013) Uropygial gland volatiles facilitate species recognition between two sympatric sibling bird species. Behavioral Ecology, 24, 1271-1278.