Avian olfaction has been neglected for a long time, although pioneering work has been conducted from the 1960th on (Bang, ; Bang and Cobb, ; Wenzel, , ,; see also Nevitt and Hagelin, ). However, much of this research focused on odor perception in general or on the use of olfactory cues in non-social contexts, e.g., for navigation (Grubb, ; Papi et al., ; Wallraff, ; Gagliardo, ) or foraging (e.g., Grubb, ; Hutchison and Wenzel, ). In addition, this research focused on few avian taxa, in which the olfactory sense was regarded to be important due to large relative olfactory bulbs (Bang and Cobb, ). These taxa included, for example, the kiwi (Apteryx australia), which has a relative olfactory bulb size of 34% (ratio of the bulb to the hemisphere), the Procellariiformes, i.e., tube-nosed marine birds, with a mean ratio of 29%, and few other species and taxa (Bang and Cobb, ).
Within the last decade the use of olfactory cues in the above mentioned topics and avian taxa has been further explored (Nevitt and Bonadonna, ; Gagliardo et al., ; Amo et al., ; Gagliardo, ) and, in addition, the social olfactory communication has attracted the interest of research (e.g., Hagelin and Jones, ; Caro and Balthazart, ; Caspers and Krause, ; Caro et al., ). Thus, the potential not only of olfactory cues (i.e., information that has not designed for the purpose of communication by natural selection; Danchin et al., ) but also of olfactory signals (i.e., information/trait with adaptive function that alter the behavior of receivers; Danchin et al., ) became apparent also in avian taxa with smaller relative olfactory bulbs. Olfactory cues have been shown to play roles in inter-specific interactions such as for species recognition (Zhang et al., ; Mardon et al., ; Krause et al., ) or as chemical defenses against predatory species (e.g., Parejo et al., ). Olfactory signals are important in intra-specific communication. Offspring related odors (DeLeon et al., ; Caspers and Krause, ; Amo et al., ; Golüke et al., ) and the reproductive partners' scent (Bonadonna and Nevitt, ) can be recognized. The sex of an individual (Whittaker et al., ; Amo et al., ) and kinship (Coffin et al., ; Bonadonna and Sanz-Aguilar, ; Krause et al., ) can be encoded in the scent. Olfactory signals are used for mate choice decisions (Amo et al., ; Whittaker et al., ; Caspers et al., ) and provide information about the MHC (Strandh et al., ; Leclaire et al., ).
Why the chicken is interesting
Here, we want to highlight the possible importance of the sense of smell in social communication in another avian species, i.e., the chicken (Gallus gallus). The chicken is one of the most commonly used avian species in science (e.g., Rose, ; Hillier et al., ) and is the most common avian species on the world with ~22-billion specimens kept in captivity for egg and meat production (Nicol, ). Thus, a deeper understanding of the use of olfactory communication in chickens would add necessary knowledge to fundamental and applied science which additionally may have consequences for the management and welfare of farmed chicken.
Chickens show a complex social organization (Zuk et al., ; Collias and Collias, ) including defined social relationships (Schjelderup-Ebbe, ). They are able to discriminate dozens of individuals from each other (D'Eath and Keeling, ) when faced with live conspecifics, whereby the sensory modes underlying this individual discrimination are still unknown. Vocal communication includes about 30 different vocal types (Collias and Joos, ; Huber and Fölsch, ) that are known to transfer information about e.g., social relationships, status, and level of aggressiveness. Visual components of communication are comb sizes and colourations which correlate with social status (Cloutier and Newberry, ) as well as the plumage ornaments of males (Nicol, ) that can attract females. Thus, social communication is an essential component in the life of chickens. Whereas, the use of vision (e.g., Zuk et al., 1990b; Cornwallis and Birkhead, ) and sound (e.g., Sherry, ; Collias, ) for social communication are widely recognized the use of olfaction has been largely neglected. This is surprising as the natural forest habitat of chickens is characterized by dimmed light (Wood-Gush, ) which limits the use of visual signaling. Furthermore, acoustic signals may increase predation risk and, thus, also their use may be constrained. These communicatory limitations under natural conditions might have been compensated by the use of olfaction in social communication. Understanding whether and how chickens make use of olfactory signals will not only increase our knowledge on the behavior biology of chickens, but additionally could help to improve housing conditions and aspects of animal welfare under commercial conditions.
Olfaction in the chicken
The Galliformes have small relative olfactory bulbs ranging from 13.5 to 15% with the chicken (Gallus gallus) ranging at the upper edge with 15% (Bang and Cobb, ). Wood-Gush () mentioned that the sense of smell is believed to be very poorly developed, although the role of olfaction in the chicken's behavior had barely been investigated. Since that time, however, it has been shown in both, neurobiological (e.g., Tucker, ) as well as behavioral studies, that chicken perceive and react to olfactory stimuli (reviewed by Jones and Roper, ). Recent studies highlight the enormous number of olfactory receptor genes suggesting an important role of olfaction in many birds including chickens (Steiger et al., ; Khan et al., ). Also another class of receptors exists for volatile amines, i.e., the trace amine-associated receptors (TAAR), which however seem to be less pronounced in birds (Hashiguchi and Nishida, ).
Chickens discriminate and learn about odors and form memories of their home nest odor and their homes' scent (Burne and Rogers, ). Familiar odors are preferred throughout life (Jones and Gentle, ; Turro et al., ) and may reduce fear (Jones and Gentle, ). Olfactory cues can also provide information about predators and alarm contexts (Jones and Black, ; Fluck et al., ). Olfaction also seems to play a certain role during foraging, although it seems to be secondary compared to visual cues (Jones and Roper, ; but see Roper and Marples, ). Chickens avoid unfamiliar smelling food (Jones, ) and adverse reactions gradually appear to graded concentrations of odors (Burne and Rogers, ; Marples and Roper, ).
Since the seminal review on olfaction in chicken by Jones and Roper () more studies have been published on this topic. However, most of these studies have focused on non-social or mechanistic aspects of odor perception rather than on the potential importance of olfactory social communication. Several studies examined, for example, early experiences or exposure to olfactory cues (Porter and Picard, ; Sneddon et al., ; Burne and Rogers, ; Porter et al., ; Bertin et al., , ; Hagelin et al., ), olfactory memory (Jones et al., ; Siddall and Marples, ), reactivity to olfactory and gaseous stimulation (Jones et al., ; McKeegan et al., , ), and to predator cues (Zidar and Løvlie, ).
Jones and Roper () already pointed out that research on the use of olfaction in chickens has been mainly conducted using natural or artificial olfactory cues in non-social contexts. Thus, the use of olfaction for social communication remained widely neglected not only in chickens (Jones and Roper, ) but in birds in general (Hagelin and Jones, ; Caro and Balthazart, ; Caro et al., ). In chickens only very few studies have addressed aspects of social olfactory communication. Hirao et al. () showed that chicken males prefer females with intact uropyginal glands over uropygial glandectomized females for sexual behaviors, suggesting that the uropyginal gland and its secretions may act as a source of sexual odorous information. Furthermore, the results of Karlsson et al. () suggest that red jungle fowls have individual body odor profiles.
Social olfactory communication in chickens
In the face of the complex social life of chickens (Collias and Collias, ; Nicol, ), their ability of odor perception (Jones and Roper, ), and first hints for the use of olfactory communication (Hirao et al., ; Karlsson et al., ) we suggest that it will be promising to further elucidate olfaction as a so far almost neglected mode of social communication in chickens. We hypothesize that the role of social olfactory signals is likely to be important in numerous contexts and we suggest to examine social communication in chicken by combining behavioral experiments and analyses of the chemical profiles to understand the underlying processes.
Due to the mating systems of chicken it seems worthwhile, for example, to investigate the role of the males' scent and the link between dominance and body odors. Dominant male chickens sire most offspring (Collias and Collias, ; Pizzari and Birkhead, ) and it could be tested whether male quality is part of the chemical signal females perceive apart from visual and acoustic signals. It is likely that male courtship displays such as preening, wing-flapping or feather-ruffling behaviors are also used for odor transmission (Wood-Gush, ). Such roles of scent in male quality assessment is well known from mammals (e.g., Rich and Hurst, ) and there are already hints for this in some other avian species (Amo et al., ; Whittaker et al., ; Caspers et al., ).
When it turns out that olfactory signals are involved in reproductive processes, a promising next step will be to test whether kinship is recognized based on olfactory signals in chickens. Kin recognition is important to either avoid inbreeding or to benefit from the vicinity of close relatives during chick raising. Olfactory kin recognition is already known from mammals (e.g., Todrank et al., ; Mateo, ) and some other bird species (Coffin et al., ; Bonadonna and Sanz-Aguilar, ; Krause et al., ).
Furthermore, body odors are mixtures of various substances, including uropyginal gland secretion and by-products of every day metabolic processes. Therefore, we expect certain information, such as health status to be more reliable signaled via olfactory cues compared to visual signals, where changes become apparent with a greater delay.
Applied perspectives of social olfactory communication in chickens
If olfactory signals play an important role for chickens' social interactions considering the diverse constraints of olfaction in intensive housing conditions may lead to new approaches for understanding and solving welfare problems. Laying hens are kept in sex-homogenous groups and, thus, any communication with males is excluded. Both laying hens and broilers (i.e., chickens for meat production) are artificially hatched and raised without parents and, moreover, are housed in age-homogenous groups. This again restricts aspects of social communication, especially parent-offspring communication. Furthermore, commercial chickens are kept at large group sizes of several thousand individuals which clearly restrict the opportunity of individual recognition (D'Eath and Keeling, ). These intensive housings additionally lead to increased ammonia concentrations which negatively affect the olfactory capacities of the birds (Jones et al., ). A better understanding of possible consequences of these limitations for social olfactory communication may provide novel insights into some of the most urgent questions in animal welfare research.
For example, olfactory signals might be involved in behavioral disorders often observed in laying hens such as feather pecking (Kjaer and Sørensen, ; Jensen et al., ). Feather pecking has been found to be related to dust bathing (Vestergaard and Lisborg, ), and this behavior is used by chickens to remove feather lipids from the plumage (Scholz et al., ). These feather lipids are secreted by the uropyginal gland which in turn is involved in the production of the individual's odor. To a certain degree the scent of feathers is linked to the probability that conspecifics peck and eat feathers (McKeegan and Savory, ; but see Karlsson et al., ). Thus, it seems promising to investigate potential links between dust bath material, individual body odors and the prevalence for feather pecking. Olfaction also might be involved in the problem of cloaca cannibalism as the scent producing uropyginal glands are located near the cloaca. Despite possible involvement of olfaction in welfare problems, odors possibly can be used as an olfactory enrichment (Nielsen et al., ) and thereby improving the housing of chickens.
Taken together, in our opinion addressing the potential of olfactory social signaling in wild, feral and domesticated chicken is an important new field of research and will lead to important new insights on social communication and on consequences if this mode of communication is constraint.
Authors contributions
EK initiated the paper. EK, LS, BC wrote the paper.
Funding
EK was funded by two grants of the Volkswagen Foundation (85994 and 85994-1). BC was funded by a Freigeist-Fellowship from the Volkswagen Foundation.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Statements
Acknowledgments
This article is based on a talk given by the first author at an informal symposium on avian olfaction at Friedrich-Loeffler-Institute, Institute of Animal Welfare and Husbandry in Celle, Germany in November 2015. The meeting was held based on a joint research grant of EK and Luisa Amo from the Volkswagen Foundation (85994-1).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Summary
Keywords
chicken, red junglefowl, broiler, laying hen, social communication, mate choice, inbreeding, kin recognition
Citation
Krause ET, Schrader L and Caspers BA (2016) Olfaction in Chicken (Gallus gallus): A Neglected Mode of Social Communication?. Front. Ecol. Evol. 4:94. doi: 10.3389/fevo.2016.00094
Received
26 April 2016
Accepted
20 July 2016
Published
09 August 2016
Volume
4 - 2016
Edited by
Deseada Parejo, University of Extremadura, Spain
Reviewed by
Benjamin James Pitcher, Macquarie University, Australia; Atsushi Hirao, Jichi Medical University, Japan
Updates
Copyright
© 2016 Krause, Schrader and Caspers.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: E. Tobias Krause tobias.krause@fli.de
This article was submitted to Behavioral and Evolutionary Ecology, a section of the journal Frontiers in Ecology and Evolution
Disclaimer
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