Olfaction in the Zebra Finch (Taeniopygia guttata): What Is Known and Further Perspectives

CHAPTER TWO

Olfaction in the Zebra Finch (Taeniopygia guttata): What Is Known and Further Perspectives E. Tobias Krause*,1,2, Hans-Joachim Bischof†,2, Kathrin Engel†,2, € u € Maraci†,2, Uwe Mayer‡,2, Jan Sauer†,2, € ke†,2, Onc Sarah Golu †,1,2 Barbara A. Caspers *Institute of Animal Welfare and Animal Husbandry, Friedrich-Loeffler-Institut, Celle, Germany † Bielefeld University, Bielefeld, Germany ‡ Center for Mind/Brain Sciences (CIMeC), University of Trento, Rovereto, Italy 1 Corresponding authors: e-mail address: [email protected]; [email protected]

Contents 1. Introduction 2. Usage of Olfaction in the Life of Zebra Finches 2.1 Social Contexts 2.2 Nonsocial Contexts 2.3 Summary 3. Mechanisms of the Olfactory Signal 3.1 Production of Scent 3.2 Perception and Processing of Scent 4. Methods to Examine Olfaction in Zebra Finches 4.1 Behavioral Methods 4.2 Impairing the Olfactory Sense 4.3 Analyzing the Chemical Signal 5. Conclusion Acknowledgments References

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1. INTRODUCTION Since centuries, birds fascinated us by their colorful plumages and elaborated songs (e.g., Catchpole & Slater, 2008). This fascination of bird fanciers also led to a growing interest in the scientific evaluation of 2

The authors contributed equally.

Advances in the Study of Behavior, Volume 50 ISSN 0065-3454 https://doi.org/10.1016/bs.asb.2017.11.001

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2018 Elsevier Inc. All rights reserved.

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the avian biology. Especially, the visual and acoustic capabilities of birds have drawn the attention of scientists, probably because these senses are also essential for humans. The first investigations on the avian sense of smell lead to the opinion that birds cannot smell, a view which was held true for almost 2 centuries. In the 18th century Georges-Louis Leclerc, Comte de Buffon, concluded in parts of his “Histoire naturelle” that the olfactory perception is absent in most birds. Even avian species that can perceive odors were believed not to use it for the control of behavior (cf. Albus, 2005). In the 19th century, the ornithologist James John Audubon supported this view, providing an experiment (which was not optimal due to modern standards) on turkey vultures, suggesting that these birds indeed were not able to smell (cf. Birkhead, 2012). The idea of birds being anosmic pertained until the second half of the 20th century. At this time, evidence accumulated that birds possess and use a sense of smell (e.g., Bang & Cobb, 1968; Tucker, 1965; Wenzel, 1968, 1971). The first studies on the avian sense of smell focused mostly on anatomical and physiological questions (e.g., Tucker, 1965) and on the use of olfactory cues in nonsocial contexts like navigation (in pigeons: Papi, Ioale`, Fiaschi, Benvenuti, & Baldaccini, 1974; in Procellariiformes: Grubb, 1979) or foraging (in kiwis: Wenzel, 1968; in Procellariiformes: Grubb, 1972). A comparative study on the relative size of the olfactory bulbs among different birds species showed that the size varies quite strongly among species (Bang & Cobb, 1968), ranging from only 3% in the Black-capped chickadee (Poecile atricapillus), up to 37% in the snow petrel (Pagodroma nivea). It was proposed that in avian species with large olfactory bulbs, such as tubenosed marine birds, kiwis, vultures, and water birds, olfaction may be important, while it is relatively unimportant in birds with small olfactory bulbs, like, for example, the songbirds (Bang & Cobb, 1968). As the Passeriformes have relatively small olfactory bulbs (Bang & Cobb, 1968), the olfactory capacities remained for some more decades relatively unattended in this taxon. However, as olfaction is a quite important sense for mammals (e.g., Moulton, 1967; Penn, 2002; Penn & Potts, 1998a), including humans (e.g., Penn et al., 2007), interest arises whether this sense might also play a role in other birds. By the end of the 1990s, Roper (1999) noted in his review on olfaction in birds accumulating evidence for a role of the olfactory sense in the control of behavior also in bird species with small olfactory bulbs. In line with this, several studies on olfaction in songbirds have been published after this inspiring review. For example, European starlings (Sturnus vulgaris) have been

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shown to select nest fragments based on olfactory cues (e.g., Clark & Russell Mason, 1988; Gwinner, 1997; Gwinner & Berger, 2008). Blue tits (Cyanistes caeruleus) select nest material also by its scent and can perceive changes in nest scents (Mennerat, 2008; Petit, Hossaert-McKey, Perret, Blondel, & Lambrechts, 2002). Furthermore, odor perception is related to food rewarding (Mennerat, Bonadonna, Perret, & Lambrechts, 2005) and predator avoidance (Amo, Galva´n, Toma´s, & Sanz, 2008) in blue tits. Catbirds (Dumetella carolinensis) can navigate by the help of odors (Holland et al., 2009). In the dark-eyed junco (Junco hyemalis) several studies have been conducted, e.g., to characterize the individual’s body odor (Whittaker et al., 2010); to investigate the use of alien odors as predictors of brood parasitism (Whittaker, Reichard, Dapper, & Ketterson, 2009); or to show a linkage between chemoprofiles and reproductive success (Whittaker, Gerlach, Soini, Novotny, & Ketterson, 2013). The Zebra Finch (Taeniopygia guttata) is one of the most popular avian model species, (Griffith & Buchanan, 2010), and one of the most-studied songbird species. Thus, it is not surprising that the functions and mechanisms of olfaction have also been investigated in this species. In this review, we mainly aim to summarize the existing knowledge of olfaction in Zebra Finches. However, several topics (e.g., olfaction in relation to MHC (major histocompatibility complex) and neurobiology) warrant further investigation for this key avian model species (Griffith & Buchanan, 2010). Thus, for these topics, we expanded our review from Zebra Finches also to other bird species in order to provide an outlook for future research possibilities in the Zebra Finch. Zebra Finches are passerine birds, native to Australia, where they can be found almost on the entire continent, including different climate zones (Immelmann, 1965; Zann, 1996). Although they are distributed over such an enormous area, they virtually show no genetic population structure (Balakrishnan & Edwards, 2009; but see Forstmeier, Segelbacher, Mueller, & Kempenaers, 2007 for captive laboratory populations). Zebra Finches are quite social (Mariette & Griffith, 2012; Zann, 1996), which requires them to communicate with their conspecifics. Although we will focus on the usage and mechanisms of the sense of smell, the production, and the perception of olfactory cues and signals, it is important to keep in mind that the sense of smell is one of several senses important in the life of Zebra Finches (see Fig. 1). Olfaction in Zebra Finches has been neglected for a long time, probably because the use of visual (e.g., Bennett & Cuthill, 1994; Burley, Krantzberg, & Radman, 1982; Immelmann, 1959) and

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Vision

Acoustics

Olfaction

Fig. 1 Schematic representation of the major sensory modalities involved in communication in the Zebra Finch. In the lives of Zebra Finches, single sensory modalities are probably the exception; usually, the sensory modalities are all available during communication in parallel. This should be kept in mind by the interpretation of results of studies on single sensory modalities. For vision, a picture of two Zebra Finch males is shown; for acoustics, a sonogram of a male song is displayed; and for olfaction, a chromatogram of a Zebra Finches’ whole body is presented.

acoustic (e.g., Elie et al., 2010; Riebel, 2009; Spencer, Buchanan, Goldsmith, & Catchpole, 2003) cues and signals for communication was more obvious to researchers. However, recent findings highlighting the olfactory abilities of Zebra Finches indicate that many key features of communication may not be understood without taking olfactory signals and their interaction with the other senses into account (see Fig. 1). While we do not want to downscale the importance of visual and acoustic cues for Zebra Finch communication, this review will show that olfaction is another very important sensory modality for communication and sensory perception in Zebra Finches. After the general and very comprehensive reviews on avian olfaction of Roper (1999), Caro and Balthazart (2010), and Caro, Balthazart, and Bonadonna (2015), many new insights into olfaction in Zebra Finches were raised. They will build the body of this review, at some occasions complemented by side glances to other avian species.

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2. USAGE OF OLFACTION IN THE LIFE OF ZEBRA FINCHES 2.1 Social Contexts Zebra Finches are social birds, in which social communication is an essential part of everyday life. Zebra Finches are mainly colony-breeding birds and are attracted by the presence of conspecifics for nest site selection (Mariette & Griffith, 2012). As opportunistic breeders, they start breeding whenever the situation seems good, i.e., usually after the onset of flushes of seed production (Zann, 1996). 2.1.1 The Role of Olfaction in Juveniles As all altricial birds, young are highly dependent of parental provisioning and siblings compete for food. A previous study has demonstrated that Zebra Finches recognize kin labels shortly after fledging (Krause, Kr€ uger, Kohlmeier, & Caspers, 2012). At that time all senses are well developed, whereas Zebra Finches keep their eyes closed until around day 6 to 8 and start to emit begging calls around day 3 (Ikebuchi, Okanoya, Hasegawa, & Bischof, 2017; Muller & Smith, 1978; Zann, 1996). Typical for all vertebrates the chemical sense develops earlier than the auditory and visual sense (Lickliter, 2005) and is already well developed at hatching. It has been shown that Zebra Finch chicks show a preference for the body odor of their parents, already a few hours after hatching (Caspers et al., 2017). They begged significantly longer as a response to their mother’s and father’s odor compared to the odor of a same sex unfamiliar adult bird (Caspers et al., 2017). The ability to recognize parents at such an early nestling phase has not been considered before in altricial birds. Based on studies investigating visual and acoustic cues for parent–offspring recognition, it has been suggested that parent–offspring recognition in altricial birds develops shortly before the young fledge (Beecher, 1991). Bischof and Lassek (1985) propose that Zebra Finch chicks recognize their parents by visual cues around day 10 after hatching, and Jacot, Reers, and Forstmeier (2010) demonstrated that the chicks recognize the calls of their parents shortly before fledging (Jacot et al., 2010) which occurs around day 19 of life (Rehling et al., 2012). The ability of olfactory parent recognition from the first day demonstrates illustratively the sensitivity of olfaction in this species, at least in a laboratory setting (Caspers et al., 2017). In addition to parental recognition under standardized laboratory breeding conditions, Zebra Finch chicks have also been demonstrated to be able to recognize their genetic mother without prior

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associative learning. The chicks retain their chemosensory knowledge of their mothers after being transferred as an egg into another nest (Caspers et al., 2017). Although the underlying mechanisms and functions are unclear yet and the ability seems limited to mothers, whereas fathers are not recognized by chicks being cross-fostered as eggs, this highlights the possibility that odors may transmit into the eggs (e.g., Caspers, Hagelin, Bock, & Krause, 2015; Hagelin, Simonet, & Lyson, 2013) and thus maternal cues are learned during embryonic development. Embryonic learning of chemical cues has been demonstrated in other vertebrate taxa, such as humans (Schaal, Marlier, & Soussignan, 1998), amphibians (Ferrari, Manek, & Chivers, 2010; Hepper & Waldman, 1992), and also in precocial birds (Bertin, Calandreau, Arnould, & Levy, 2012; Bertin et al., 2010; Hagelin et al., 2013; Sneddon, Hadden, & Hepper, 1998) and might probably be more the rule than an exception. The functional aspect of this ability is also unclear yet. Chicks should try to maximize their food intake by begging as much as possible to any bird that brings food. Particularly since conspecific brood parasitism in Zebra Finches can occur (Birkhead, Burke, Zann, Hunter, & Krupa, 1990; Griffith, Holleley, Mariette, Pryke, & Svedin, 2010), one would expect chicks to be less successful when reducing their begging intensity toward the foster mother. However, the ability to recognize the mother even after being raised by a foster mother might be important to be able to recognize also other kin. Only recently, it has been shown that the odor of conspecifics can modulate begging behavior in another altricial songbird species, the blue tit (C. caeruleus). Blue tit chicks begged significantly longer as a response to the odor of unfamiliar chicks compared to the odor of familiar chicks (Rossi et al., 2017). Thus, it can be speculated that the ability for kin recognition during the nestling stage (Boncoraglio, Caprioli, & Saino, 2009) is based on chemical cues, allowing chicks a more selfish behavior in the presence of unrelated individuals (Boncoraglio et al., 2009; Boncoraglio & Saino, 2008; Briskie, Naugler, & Leech, 1994). 2.1.2 The Role of Olfaction in Adults 2.1.2.1 Kin Recognition of Offspring and Siblings

Whether Zebra Finch parents are also able to recognize their own offspring’s scent or whether they are able to discriminate between own offspring and foreign offspring is unclear yet, but evidence is accumulating that they probably can (in the case of offspring calls, see Reers, Jacot, & Forstmeier, 2011). Zebra Finch females, for example, can recognize the scent of their own eggs, not directly after laying but after 10 days of incubation (Gol€ uke, D€ orrenberg,

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Krause, & Caspers, 2016). However, the ability to recognize an own egg by smell does not prevent birds from being exploited by intraspecific brood parasitism (Griffith et al., 2010; Schielzeth & Bolund, 2010), but the experiments show that females either learn the scent of their clutches, or that they impregnate their eggs with their own body scents and recognize that. After hatching of the young, Zebra Finch females show a preference for their own nest odor and avoid the odor of a conspecific nest as long as their young have not fledged (Krause & Caspers, 2012). This demonstrates that females are able to discriminate between the odor of their own nest and the odor of a foreign nest. Such odor preference for the own nest odor could not be demonstrated in females after the young fledged (Krause & Caspers, 2012). In both situations, i.e., during the nestling phase of their chicks and after the chicks fledged, fathers do not show any preference or avoidance of their own nest odor or the nest from conspecifics (Krause & Caspers, 2012). This finding might lead to the conclusion that fathers might not use olfactory cues to recognize their own nest or their own offspring, which supports the idea that fathers do not discriminate between own and foreign offspring (Kempenaers & Sheldon, 1996). Whether fathers are able to discriminate among own and foreign offspring that has been raised in their own nest needs to be addressed in future studies. It seems unlikely that olfactory abilities are restricted to a single sex in Zebra Finches. The usage of olfaction, however, might be depending on context and investment, which may vary between sexes. Yet, parental responses to offspring were only tested with odors of nests (Krause & Caspers, 2012). It remains open whether Zebra Finch parents can recognize the offspring’s individual body odor. Although we would expect such an ability in case of true olfactory kin recognition (Krause et al., 2012), there is currently no evidence that parents are able to do so, as foster chicks are successfully raised by the foster parents. However, further studies addressing this particular question are needed to confirm or rule out this possibility. The ability to recognize kin might not only be important for offspring recognition, but also for mate choice and the formation of feeding flocks during the nonbreeding season (Grabowska-Zhang, Hinde, Garroway, & Sheldon, 2016; McGowan, Fowlie, Ross, & Hatchwell, 2007). While association and learning of family cues might be one mechanism how individuals recognize kin (Ihle & Forstmeier, 2013; Sharp, McGowan, Wood, & Hatchwell, 2005), evidence exists that Zebra Finches assess relatedness based on olfactory cues and do not necessarily need prior association

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for kin recognition (Arct, Rutkowska, Martyka, Drobniak, & Cicho n, 2010; Caspers, Gagliardo, & Krause, 2015; Caspers et al., 2017). This suggests that female Zebra Finches are able to recognize unfamiliar close relatives based on olfactory cues (Caspers, Gagliardo, et al., 2015; Krause et al., 2012), an ability that has also been demonstrated in other avian species (e.g., Bonadonna & Sanz-Aguilar, 2012). Currently, it is unknown whether same sex social bonds occur in Zebra Finches or whether individuals benefit from association with kin in feeding flocks, but the ability to recognize unfamiliar kin has a potential adaptive value, for example, in terms of inbreeding avoidance. 2.1.2.2 Inbreeding Avoidance

To be able to recognize kin is also a prerequisite to avoid inbreeding. Studies in captive Zebra Finches have shown that inbreeding comes at a cost (Arct et al., 2010; Bolund, Martin, Kempenaers, & Forstmeier, 2010; Hemmings, Slate, & Birkhead, 2012). Thus, individuals should avoid mating with close related individuals. Several studies have been conducted to investigate whether Zebra Finches avoid breeding with close related individuals, coming to ambiguous results (reviewed in Ihle & Forstmeier, 2013). In a recent study, it was found that the ability to perceive conspecific odors has an impact on mate choice and reproductive investment (Caspers, Gagliardo, et al., 2015). In this study, triplets of Zebra Finches were formed consisting of one female and two males, both being unfamiliar to the female. One male was unrelated whereas the other one was an unfamiliar brother. Females were randomly assigned to one of two treatment groups. Half of the females acted as a control, whereas the other half were temporarily impaired in their sense of smell. The procedure led to no obvious side effects, and the anosmic birds behaved quite normal and laid clutches (median of 5 eggs) typical for Zebra Finches (compare, on average 5.32 eggs in Griffith et al., 2017). Females being able to perceive odors, however, less often formed a pair and laid fewer eggs compared to females being temporarily not able to smell. Probably, the presence of kin-odor, i.e., from an unfamiliar full-brother, disturbed pair formation and thus reproductive investment. This is in line with another study on maternal investment in sibling breeding pairs (Arct et al., 2010). In addition, females, not being able to smell, formed pairs as often with unfamiliar brothers as with the unrelated males (Caspers, Gagliardo, et al., 2015), while in the control treatment only two females produced clutches (one sired by the unrelated and one by the full-brother). Thus, females can perceive the presence of close kin if they are able to smell,

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indicating the presence of olfactory kin labels. These findings might also explain the results of Arct et al. (2010), who also found reduced reproductive investment in females that were paired to unfamiliar kin. Such inbreeding avoidance on the basis of olfactory cues has been suggested to be important also in other avian species (Bonadonna & Sanz-Aguilar, 2012). Already 40 years ago, the immune genes of the MHC have been shown to be involved in body odor production in mammals, i.e., mice (Yamazaki et al., 1976). Thus, MHC-linked assortative mating, which has been shown to be existent in some bird species, might hint to the use of olfaction for mate choice. 2.1.2.3 Mate Choice and MHC

Currently, to the best of our knowledge, no study exists examining whether Zebra Finches show MHC-assortative mating. The fact that Zebra Finches form lifelong pairs (Zann, 1996), show low levels of extra pair paternities (Birkhead et al., 1990; Griffith et al., 2010; Griffith, Owens, & Thuman, 2002), show costs of inbreeding (Arct et al., 2010; Bolund et al., 2010; Hemmings et al., 2012), and use odors to detect kin (Caspers, Gagliardo, et al., 2015; Krause et al., 2012), favors the idea that Zebra Finches mate assortative with respect to the MHC and respective scent components. However, as mentioned earlier, we expanded here our review from Zebra Finches to other bird species in order to provide an outlook what could be examined in future studies in the Zebra Finch. The MHC is a set of cell surface proteins that have their main function in the recognition of self and nonself molecules (Janeway, Travers, Walport, & Shlomchik, 2004; Milinski, 2006). As the MHC complex is an essential part of the adaptive immune system, MHC-related signals can broadcast information about the quality of the prospective partner with respect to the health status or its immune system (Tregenza & Wedell, 2000). The MHC complex is an extremely polymorphic gene cluster showing enormous allelic variations among individuals. As every individual MHC allele recognizes only a subset of pathogens, MHC heterozygosity provides individuals the advantage of being resistant to a broader spectrum of diseases (Murphy, Janeway, Travers, Walport, & Ehrenstein, 2008). Therefore, based on the “heterozygote advantage” hypothesis, preferences for MHC-dissimilar partners maximize the likelihood of MHC-heterozygous progeny, which consequently results in fitness benefits (Penn & Potts, 1998a, 1998b; Potts & Wakeland, 1990). Because the main function of the MHC proteins is the recognition of self and nonself (Janeway et al., 2004; Milinski, 2006),

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MHC-disassortative mating has been proposed as a mechanism to avoid inbreeding (Tregenza & Wedell, 2000). However, too much diversity in MHC alleles increases the risk of autoimmune diseases. Thus, by choosing a partner with optimal MHC dissimilarities (Woelfing, Traulsen, Milinski, & Boehm, 2009), individuals can pass genetic benefits to their offspring, i.e., sufficient protection from diseases without increasing the risk of inbreeding and autoimmune diseases. Based on this “complementary genes” hypothesis, individual mating preferences depend upon own MHC diversity, favoring those partners that carry different levels of MHC allelic diversity. As olfactory signals play a central role in differentiating MHC genotypes (for more details see Section 3.1.1) of conspecifics in many species (Brown & Eklund, 1994; Olsson et al., 2003; Ruff, Nelson, Kubinak, & Potts, 2012; Wedekind, Seebeck, Bettens, & Paepke, 1995; Yamazaki et al., 1979), MHC-disassortative mating might indirectly indicate the use of olfaction for mate choice. Although MHC-based mate choice has been reported in some bird species (Bonneaud, Chastel, Federici, Westerdahl, & Sorci, 2006; Juola & Dearborn, 2012; Leclaire, van Dongen, et al., 2014; Strandh et al., 2012), there is no universal model explaining MHC-based mate selection across avian taxa. Some bird species such as blue petrels (Halobaena caerulea) (Strandh et al., 2012), Savannah sparrows (Passerculus sandwichensis) (Freeman-Gallant, Meguerdichian, Wheelwright, & Sollecito, 2003), great frigate birds (Fregata minor) (Juola & Dearborn, 2012), and gray partridge (Perdix perdix) (Rymesˇova´ et al., 2017) prefer to reproduce with MHCdissimilar partners. The female ring-necked pheasants (Phasianus colchicus) mate with partners with compatible MHC alleles, showing intermediate levels of similarity to their own alleles (Baratti et al., 2012) and thereby optimizing the MHC diversity of their progeny. Similarly, house sparrows (Passer domesticus) avoid males with low allelic diversity for MHC class I as well as the ones that do not have any common alleles (Bonneaud et al., 2006). Based on Griggio, Biard, Penn, and Hoi (2011), in house sparrows not all females but the ones carrying a low number of MHC alleles, prefer males with high number of MHC alleles. In many pair-bonding bird species, a female’s tendency to seek extra pair copulations increases when their social mate is not compatible. FreemanGallant et al. (2003) investigated MHC-based mate preferences and extrapair copulations in Savannah sparrows. Their findings show that females generally choose MHC-dissimilar males and in the case of pair bonding with an MHC-similar partner incidences of extrapair copulations increased.

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For Seychelles warblers, Richardson, Komdeur, Burke, and von Schantz (2005) reported that females tend to seek extrapair copulations with males that have a higher MHC allelic diversity, in case their social mate has a low diversity. All these examples demonstrate the existence of MHC-assortative mate choice in birds. Moreover, recent findings that characteristics of the MHC are encoded in body odors of birds and that birds can assess MHC similarity based on smell (Leclaire, Strandh, Mardon, Westerdahl, & Bonadonna, 2017, see Section 3.1.1) indicate that birds may also use their sense of smell to determine genetic compatibility of potential mates. The Zebra Finch MHC is reported to be dispersed across several chromosomes, contrary to other species like, e.g., chickens (Warren et al., 2010). Whether this has any functional consequences needs to be addressed in future studies investigating the influence of the Zebra Finch MHC on the individual’s body odor (Section 3) and mate choice decisions. 2.1.3 Interspecific Interactions Beside the role of olfactory signals in intraspecific contexts, they can also play a role in the interaction with other species. Zebra Finch females prefer the scent of a conspecific over the scent of a Diamond Firetail female (Krause et al., 2014). Diamond firetails (Stagonopleura guttata) appear sympatric with Zebra Finches in the wild and thus interactions between the species are likely to occur. Chemical analyses revealed that the chemical fingerprints differ between the two species (Krause et al., 2014), enabling female Zebra Finches to discriminate between a conspecific and a heterospecific. Thus, body odors do provide information important for interspecific communication (Krause et al., 2014), similar to visual (Galoch & Bischof, 2006; Immelmann, 1959; Zann, 1996) and acoustic signals (Clayton, 1990; Clayton & Pr€ ove, 1989; Riebel, 2009). These results show that Zebra Finches can distinguish their species’ odor from that of other species. However, in the wild visual and acoustic signals may be used as first indicators to identify conspecifics, as they can already be perceived from larger distances.

2.2 Nonsocial Contexts 2.2.1 Food-Related Odors In the previous paragraph, the use and potential importance of olfactory signals in social contexts have been presented. However, olfactory cues can also play a role in nonsocial contexts. One of the first studies on olfactory abilities in Zebra Finches was, to our knowledge, conducted in a foraging context (W€ urdinger, 1990). In this study, different odors, such as lavender or

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peppermint oil, were added to salad. It was measured whether birds prefer untreated salad over treated. The results were partly ambiguous as in some cases novel odors led to a preference and in some cases to an avoidance of the salad. However, for the first time it was shown that odors may matter to Zebra Finches in foraging-related contexts (W€ urdinger, 1990). This idea got further support from a subsequent study, where Kelly and Marples (2004) found that novel food was less well accepted when novel color and especially an interaction of novel color and novel odors were present. This suggested that odors may be involved in avoiding novel and unfamiliar food (Kelly & Marples, 2004). Both studies used novel odors (Kelly & Marples, 2004; W€ urdinger, 1990) and therefore lead to the conclusion that Zebra Finches might have neophobia toward novel-smelling food. In another experiment, using familiar food, Zebra Finches were trained to locate a food-rewarded arm only on the basis of the scent of the food (Krause, Kabbert, & Caspers, 2016). Here, performance was not different from chance level and thus training on positive reward with food scent does not seem to work in Zebra Finches (Krause et al., 2016). This is in contrast to other birds. For example, in Procellariiformes and penguins, odors are known to play important roles in foraging as these birds are quite sensitive to dimethyl sulfide, an indicator for krill (Procellariiformes: Bonadonna, Caro, Jouventin, & Nevitt, 2006; Nevitt & Bonadonna, 2005; Nevitt, Veit, & Kareiva, 1995; Penguins: Amo, Rodriguez-Girones, & Barbosa, 2013; Wright, Pichegru, & Ryan, 2011). Interestingly, those species have all relatively large olfactory bulbs (Bang & Cobb, 1968), in contrast to the relative small olfactory bulbs in Zebra Finches. 2.2.2 Scents for Orientation and Predator Avoidance Most of our knowledge on the use of olfaction in avian orientation and navigation comes from the Procellariiformes (e.g., Dell’Ariccia & Bonadonna, 2013; Gagliardo et al., 2013; Nevitt & Bonadonna, 2005) and pigeons (Gagliardo, 2013; Gagliardo et al., 2011; Papi et al., 1974) that use olfactory navigation for homing. Large-scale orientation and homing might not be such important in Zebra Finches as they are not migratory (Zann, 1996), whereas Zebra Finches might make use of olfaction in small-scale orientation. Zebra Finches often breed in colonies and thus finding the way back to the home nest might be challenging. Adults probably have a good visual representation of the nest location as they already constructed the nest at that place (Krause & Caspers, 2012), whereas fledglings that leave the nest for the first time cannot make use of this information. They have no such visual

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representation of the relative position of the nest. However, as they have learned the nest odor shortly after hatching (Caspers, Hagelin, et al., 2015; Caspers, Hoffman, Kohlmeier, Kr€ uger, & Krause, 2013) they can use the nest odor to find back to the natal nest. In an experimental laboratory study, it was shown that fledglings prefer their home nest scent over the scent of a conspecific nest (Caspers & Krause, 2011). When comparing several nests of different Zebra Finch breeding pairs, chemical analyses revealed that they possess different nest odor profiles (Kohlwey, Krause, Baier, M€ uller, & Caspers, 2016). Consequently, olfaction allows here a small-scale orientation to fledglings that visual cues are not able to solve (Caspers & Krause, 2011). In other contexts, small-scale navigation may also appear based on vision (Bischof, 1988; Eckmeier et al., 2008; Watanabe, Mayer, & Bischof, 2011) or geomagnetic cues (Voss, Keary, & Bischof, 2007). In their natural habitat, Zebra Finches are subject to high proportions of nest predation, resulting in up to 66% of broods lost due to predator encounters (Zann, 1996). These predators are often ground predators such as snakes, lizards, and mammals (Zann, 1996), which lead to elevated nesting of Zebra Finches (Immelmann, 1962) and a preference for elevated nests (Krause & Schrader, 2016). Beside these adaptations, it might be possible that Zebra Finches show an ability to detect predator-related odors. Yet, this has not been systematically investigated but would be an interesting future question, as in other Passerines such recognition of predator odor has been shown (Amo et al., 2008; Amo, Visser, & van Oers, 2011; Roth, Cox, & Lima, 2008).

2.3 Summary To get a comprehensive understanding, it is important to see the use of olfactory signals and cues in relation to the other sensory modalities (Caspers & Krause, 2013). In this interaction, it becomes clear that the Zebra Finches’ sense of smell could add important insights to the understanding of the birds’ behavior throughout their life. As hatchlings, when the eyes are still closed, they can already recognize the parental scents, and later after fledging, scent cues provide unique opportunities to find the natal nest without parental help. In adulthood, kin can be recognized using olfactory signals and thereby maladaptive inbreeding, with, e.g., unfamiliar siblings, can be avoided. Thus, throughout life, olfactory information provides a potentially important source of information to the birds (see summary in Fig. 2). The understanding of the usage of olfaction in Zebra Finches is yet mainly based on laboratory studies that showed how many potential functions olfaction

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Fig. 2 Pathways of olfactory communication and odor perception in the Zebra Finch. Zebra Finch pictures taken from https://doi.org/10.6084/m9.figshare.1619777.v1.

might have. Future research should also address similar question on wild population to understand comprehensively the functions and potential adaptive values of olfaction in Zebra Finches.

3. MECHANISMS OF THE OLFACTORY SIGNAL 3.1 Production of Scent Body odors are most likely mixtures of several substances, produced from the preen gland secretion, potentially influenced by many factors such as genes, the health status, food consumption, hormonal status, and microbes on the skin, and environmental conditions, such as temperature and humidity (Fig. 3). In the following we will focus on three of these factors in detail, those of which we think are the most interesting to the current developments in the field: (i) the impact of genetic components in scent production; (ii) the preen gland, which is the main source of odorous secretion in birds; and (iii) the microbial community on the skin. Although progress has been taken to understand the production of scents in some bird species, the avian key model Zebra Finch (Griffith & Buchanan, 2010) has been barely examined yet with respect to this topic. Thus, we here again broaden our view to other bird species, which might provide the basis for future research in Zebra Finches. 3.1.1 Genetic Components in Scent Production Unfortunately, we do not know much as yet about the genetic mechanism that might be involved in the production or the perception of scent in birds

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Fig. 3 Factors most likely involved in shaping an individual’s body odor.

(reviewed in, e.g., Hess & Edwards, 2002; Zelano & Edwards, 2002). Therefore, it is necessary to step back and take a look at what is known about scent production in other vertebrates. In many species, olfactory signals are used to assess MHC genotypes of conspecifics (Brown & Eklund, 1994; Olsson et al., 2003; Ruff et al., 2012; Wedekind et al., 1995; Yamazaki et al., 1979). Most of our knowledge about olfactory kin and mate recognition in vertebrates stems from research on humans and other mammalians (Brown, Roser, & Singh, 1989; Penn & Potts, 1998b, 1998c; Wedekind et al., 1995; Yamazaki et al., 1983, 1976). As early as 1976, Yamazaki et al. (1976) presented convincing evidence that the MHC, which is an essential part of the immune system and their peptide ligands, are present in the odor profile of an individual (Boehm & Zufall, 2006; LeindersZufall et al., 2004; Singh, Brown, & Roser, 1987) and these cues are part of the individual’s olfactory identity. MHC molecules possess specific ligand-binding pockets (Boehm & Zufall, 2006). These binding regions are diverse and specific for alleles. Hence, each allelic product binds to a particular subset of peptides. Different peptide ligands of one particular MHC molecule share common residues, whose side chains fit into the binding pockets. These could further suggest that anchor residues of peptide ligands are the defining feature on which olfactory assessment might focus on (reviewed in Boehm & Zufall, 2006). In addition, it could be shown that small peptides of nine amino acids, which are complementary to the ligand-binding pocket of MHC molecules, can be bound by olfactory receptors (Leinders-Zufall et al., 2004; Milinski et al., 2005). These MHC–peptide complexes are released from the cell surface and excreted from the body in saliva, sweat, and urine, providing olfactory cues about an individual’s MHC genotype (Milinski, 2006; Penn, 2002).

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Furthermore, the MHC genotype might also influence an individual’s scent profile by affecting the composition of microbial communities (Archie & Theis, 2011). Our knowledge about how the MHC genotype alters olfactory cues in avian species is quite limited. A correlation between MHC similarity and chemical composition of uropygial gland secretion was reported in blacklegged kittiwakes (Leclaire, van Dongen, et al., 2014) and wild song sparrows (Slade et al., 2016), indicating that uropygial gland secretion contains MHC-related scent cues that may broadcast information about relatedness and facilitate disassortative mating. Recently, Leclaire et al. (2017) showed that blue petrels can discriminate MHC similarity using olfactory signals alone and use this information in mate choice. Within nonavian species, the MHC-based odor profile can be used to directly assess the genetic relationship of a conspecific (kin) and to recognize potential mates (Boyse, Beauchamp, & Yamazaki, 1987). There is strong evidence that a mechanistic link between the immune system and the olfactory systems allows individuals to directly assess a partner’s genotype (Boehm & Zufall, 2006) and to estimate the genetic quality of a potential mate. Via the perception of the MHC fragments in the scent profile, individuals can directly sense the composition and the compatibility of conspecifics immune system molecules and respond accordingly with social behavior. In terms of genetic architecture, the best-studied MHC complex in birds is that of the chicken, which differs from the MHC of all other vertebrates and also from passerine birds. This is largely due to the so-called minimal essential structure (Kaufman et al., 1999), meaning that there are only 19 genes in the MHC cluster making this region approximately 20 times smaller than, e.g., the human MHC complex. In comparison, the MHC in passerine birds seems to be much more complex showing in general multiple MHC class IIb loci with extensive gene duplication and high levels of polymorphism (Balakrishnan et al., 2010; Balasubramaniam et al., 2016; Sato et al., 2011). In the Zebra Finch, the second bird species with a sequenced genome (Warren et al., 2010), the genetic architecture of the MHC complex is not fully understood. It shows a complex structure which includes multiple class I and class II genes (Balakrishnan et al., 2010). The definite location of one functional MHC class I and one functional MHC class IIb locus together with several core MHC genes could be pinpointed most probably to chromosome 16 by Ekblom et al. (2011). Chromosome 16 is one of the

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smallest avian chromosomes (Ekblom et al., 2011). Furthermore, there seems to be only one functional copy of the MHC class I in Zebra Finches but several copies of the MHC class IIb genes (Balakrishnan et al., 2010). For the life-long monogamous Zebra Finches, with low extrapair paternity levels, selecting the optimal partner is crucial in terms of fitness (Griffith et al., 2010; Mainwaring & Griffith, 2013; McCowan, Mariette, & Griffith, 2015; Zann, 1996). Individual-specific mate choice is evident in female Zebra Finches (Forstmeier & Birkhead, 2004; Forstmeier, Martin, Bolund, Schielzeth, & Kempenaers, 2011), suggesting that male attractiveness is related to compatibility between the individuals, rather than having “the good genes.” Considering that this species has a well-developed sense of olfaction and discriminates kinship based on olfactory signals (Caspers, Gagliardo, et al., 2015; Krause et al., 2012), odor-mediated MHC-based mate choice is highly plausible in Zebra Finches. Therefore, understanding the pathways of MHC in mate choice and its relation with the olfactory system in Zebra Finches will add new dimensions to current literature. 3.1.2 The Uropygial Gland and Its Secretions The uropygial gland, also called preen gland, is often considered to be the key source of avian body odors (Campagna, Mardon, Celerier, & Bonadonna, 2012; Caro et al., 2015; Hagelin & Jones, 2007), as it is the main secretory gland of a bird’s skin (Jacob & Ziswiler, 1982). The uropygial gland is a holocrine gland unique to birds, which is located on the dorsal side of the tail. While preening, birds squeeze the sebaceous secretion from the gland and transfer it across the entire body (Jacob & Ziswiler, 1982). Traditionally, functions for self-maintenance and protection are attributed to the gland: Uropygial secretions serve as a water repellent (Elder, 1954; Giraudeau et al., 2010; Jacob & Ziswiler, 1982; Montalti & Salibia´n, 2000), help to maintain the feather integrity by keeping feathers flexible (Jacob & Ziswiler, 1982), and reduce feather degrading bacteria (F€ ul€ op, Czirja´k, Pap, & Va´ga´si, 2016; Møller, Czirjak, & Heeb, 2009; Shawkey, Pillai, & Hill, 2003; but see Czirja´k et al., 2013; Giraudeau et al., 2013) and are therefore assumed to be essential for good plumage condition (Elder, 1954; Giraudeau et al., 2010; Moyer, Rock, & Clayton, 2003). In Zebra Finches, as in several other species, the preen gland is enlarged during breeding, indicating a specific need for preen gland secretion during this specific life history stage (Gol€ uke & Caspers, 2017). Whether the preen gland secretion is used for chemical communication (i.e., parent–offspring communication, see Sections 2.1.1 and 2.1.2) during this time, however, needs to be tested.

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The idea that maternal preen oils can impregnate the eggs and provide odor information to the embryo seems to be realistic (Gol€ uke et al., 2016). Nevertheless, the fact that the preen gland secretion is spread all over the body makes it a promising candidate for studies concerning avian chemical communication. Whether the preen gland developed for the purpose of olfactory signaling or whether the odorous compounds of the secretion are simply a by-product of physiological processes (Hagelin & Jones, 2007) and communication is acquired as a secondary function, is still unknown. However, accumulating evidence suggests that preen gland secretion plays a role in intraspecific communication (Campagna et al., 2012; Caro & Balthazart, 2010; Caro et al., 2015; Hagelin & Jones, 2007; Moreno-Rueda, 2017). In the Zebra Finch it has already been shown that the chemical fingerprint of an individual, which is likely influenced by the preen gland secretion, differs in its relative composition from that of the Diamond firetails, i.e., from another closely related Estrildid finch species (Krause et al., 2014). In this study, however, no single odorants could be analyzed due to the methodological approach (but see for an example Zhang, Sun, & Zuo, 2009). To qualify as a potential semiochemical, molecules have to display certain chemical characteristics: they must possess the ability to transport the biologically relevant cues through the air over a distance. Therefore, only volatile compounds of gland secretions (like small fatty acids or alcohols) are most likely suitable for olfactory communication. Chemical analyses reveal that the secretions mainly consist of large esters (Campagna et al., 2012; Leclaire et al., 2011; Mardon, Saunders, Anderson, Couchoux, & Bonadonna, 2010; Piersma, Dekker, & Sinninghe Damste, 1999). Whereas, the composition of these esters can vary according to the seasonal cycles in some birds, as for example in red knots, where a shift from mono- to more costly diester waxes, appears in the breeding season (Piersma et al., 1999; Reneerkens, Piersma, & Damste, 2002, 2005; Reneerkens, Piersma, & Sinninghe Damste, 2007). As wax esters are large molecules, they are under low vapor pressure and under ambient temperatures nonvolatile (Mardon et al., 2010) and might consequently be unsuitable for chemical communication. However, they might be chemical precursors of olfactory cues (Mardon et al., 2010). These chemical precursors might be converted by biological processes (e.g., fermentation, see Section 3.1.3) into smaller, more volatile molecules (Jacob & Ziswiler, 1982; Mardon et al., 2010). For example, the most prominent substances, linear alcohols, aldehydes, and hydrocarbons are mostly produced through oxidation or

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reduction of fatty acids (Bonadonna, Miguel, Grosbois, Jouventin, & Bessiere, 2007), and the findings are consistent with those made in other studies (Burger, Reiter, Borzyk, & Du Plessis, 2004; Tuttle et al., 2014). In passerines, linear fatty alcohols ranging from C9 to C18 are the major volatile compounds found in dark-eyed juncos (Junco hyemalis) (Soini et al., 2007; Whittaker et al., 2010) and white-throated sparrows (Zonotrichia albicollis) (Tuttle et al., 2014). In a review, Campagna et al. (2012) provided a detailed description of the main classes of volatile and semivolatile compounds of preen gland secretions across different species. This indicates a potential common function for all species, but there is no volatile compound common to the preen oil of all bird species or even all passerines (Whittaker et al., 2010). In the Bengalese finch (Lonchura striata), which is a close relative to the Zebra Finch (Goodwin, 1982), hexadecanol and octadecanol are identified to be the major compounds in terms of relative abundance (Zhang et al., 2009). Both of these substances have been suggested to be potential sex pheromone candidates, as hexadecanol has a higher abundance in males, whereas octadecanol was more expressed in females (Zhang et al., 2009). On an interspecific level, Zhang et al. (2009) suggest saturated straight chain C13–C18 1-alkanols to be phylogenetically informative and thus separating between species, as the Bengalese finch shares more compounds with the close related Zebra Finch (e.g., 13 out of the 18 identified volatile compounds) than with more distant species (Zhang et al., 2009). Moreover, preen gland secretions can differ between avian species (Mardon et al., 2010; Zhang et al., 2009), sexes (Amo, Aviles, et al., 2012; Jacob et al., 2014; Leclaire et al., 2011; Mardon et al., 2010; Whittaker et al., 2010; Zhang, Wei, Zhang, & Yang, 2010), individuals (Bonadonna et al., 2007; Mardon et al., 2010), and seasons (Reneerkens et al., 2002, 2007; Soini et al., 2007; Tuttle et al., 2014). Therefore, preen gland secretion has the potential to act as an inter- as well as intraspecific chemosignal, for example, by signaling the species (Krause et al., 2014), the individual identity and quality (Amo, Lo´pez-Rull, Paga´n, & Macı´as Garcia, 2012; Whittaker et al., 2010), and the genetic variability or genetic compatibility (Amo, Lo´pez-Rull, et al., 2012; Leclaire et al., 2017; Leclaire, van Dongen et al., 2014; Slade et al., 2016). Interestingly, none of these studies identified a single compound to be unique to a certain species or sex group, indicating that group differences are mainly expressed by differences in relative abundances rather than differences in absolute quantities.

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Despite the increasing amount of studies proposing that the preen gland secretion encodes information about species, sex, individual quality, or reproductive status, bioassays demonstrating the biological relevance of these molecules are scarce (Balthazart & Schoffeniels, 1979). Thus far, only a few studies exist that could link uropygial gland secretions, and subsequently odor, with a behavioral reaction. One of the first is Hirao, Aoyama, and Sugita (2009), who proofed in domestic chicken (Gallus gallus domesticus) that female preen oil influences the sexual behavior of males via smell (Hirao et al., 2009). Evidence for passerines is coming from female budgerigars (Melopsittacus undulatus) and dark-eyed juncos (Junco hyemalis), which distinguish in a two choice situation between the uropygial gland secretions of male and female conspecifics (Whittaker et al., 2011; Zhang et al., 2010). Moreover, female budgerigars also prefer a synthesized 3-alkanol blend that should mimic a male odor over a female odor (Zhang et al., 2010; but see Mardon, Saunders, & Bonadonna, 2011a). More bioassays like those mentioned earlier are needed to reveal the nature (see Section 4), the function, and the importance of preen gland secretions for avian chemical communication and to find out whether already identified compounds provide biologically relevant information. The Zebra Finch is an ideal study organism (Griffith & Buchanan, 2010; Zann, 1996) for those studies as principles of preen gland composition and its potential functions can be studied in the laboratory and in the field. 3.1.3 Microbes on the Skin A Zebra Finch’s body, as all animals’ bodies, is populated with microbes. Besides some obligate pathogens, most bacteria are commensals and some even live in a mutually beneficial relationship with their host (Gilbert, Sapp, & Tauber, 2012; McFall-Ngai et al., 2013). Although current research shows that birds are able to use body odors for social communication (see Section 2.1), we lack the understanding to which extent microbes contribute to a birds’ body odor and therefore play a role in social communication. According to the fermentation hypothesis (Albone, Eglinton, Walker, & Ware, 1974; Albone & Perry, 1976; Gorman, 1976), some volatile components of an animals’ chemical signal are products of the metabolism of its symbiotic bacterial community. Furthermore, the variation in these bacterial communities correlates with variation in the animal’s odor (Theis, Schmidt, & Holekamp, 2012; Theis et al., 2013). Four different aspects should be highlighted in this context: Bacteria in glands, on the feathers, on the skin surface, and in the digestive tract.

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The influence of bacteria on olfactory signaling was found in a variety of mammalian species such as mongooses, beavers, or deer (for a summary, see Ezenwa & Williams, 2014). Evidence for a link between microbes and body odor comes from hyenas, which were shown to harbor microbial communities consisting of mostly fermentative bacteria in their anal pouches (Theis et al., 2012). The bacterial profile and the profile of volatile compounds in the gland secretion covaried, suggesting that they are responsible for species-, sex-, and reproductive-state-specific odors (Theis et al., 2013). A similar link has been reported in meerkats (Suricata suricatta), whose bacterial communities in the anal scent pouches correlate to group membership (Leclaire, Nielsen, & Drea, 2014). Although the fermentation hypothesis was once introduced for mammals that mark with secretions from specific scent glands, it might as well be applicable to birds and other nonmammalian species that use chemical cues for communication (Archie & Theis, 2011). Whittaker and Theis (2016) suggest applying the fermentation hypothesis on birds as well. They found most of the identified bacteria from dark-eyed junco (J. hyemalis) preen gland secretions to belong to genera which contain species that are known odor producers. In the European hoopoe (Upupa epops) and the woodhoopoe (Phoeniculus purpureus), the preen gland harbors a secretion that contains high amounts of bacteria, especially enterococci (Martı´n-Platero et al., 2006; Soler et al., 2008) that are known to be gut-associated bacteria, producing an odor (Law-Brown & Meyers, 2003). When hoopoe nestlings’ preen glands were injected with antibiotics that killed the majority of bacteria present in the gland cavity, the composition of the secretion changed drastically. In contrast to the control animals, treated hoopoes lacked most of the volatile compounds. Martı´n-Vivaldi et al. (2009) suggest therefore a central role of bacteria in the presence of these volatile compounds. They hypothesize that some volatile chemical compounds in European hoopoe and wood hoopoe preen gland secretions could be a secondary product of symbiotic bacteria and that different bacterial communities could explain interspecific differences in volatile chemicals from preen gland secretions. On the other hand, Whittaker et al. (2016) found no significant covariation between individual bacterial and volatile profiles, when they investigated the preen gland secretions of dark-eyed juncos (Junco hyemalis). Another possible source of body odor could be the bacteria that are present on bird feathers. Well documented are especially the feather degrading bacteria, namely, Bacillus licheniformis (e.g., F€ ul€ op et al., 2016;

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Verea et al., 2014) but also B. cereus (Verea et al., 2014) and Streptomyces spp. (Boeckle, Galunsky, & Mueller, 1995). The existence of such featherdegrading bacteria has been documented in many bird species, for example, house sparrows (F€ ul€ op et al., 2016), hoopoes (Ruiz-Rodrı´guez et al., 2009), dark-eyed juncos (Dille, Rogers, & Schneegurt, 2016), thrushes (Verea et al., 2014), and house finches (Shawkey et al., 2003). Bacteria such as B. licheniformis break down feather structures via secretion of keratinases (Lin, Lee, Casale, & Shih, 1992). They could be involved in odor production via breaking down keratin and other components of the feathers in small, possibly volatile, fragments. Other, nonfeather-degrading bacteria (e.g., preen oil-consuming bacteria) could be involved in odor production as well. To our knowledge, such speculative assumptions remain unproven. Feather bacteria seem to be more abundant on the distal than on the proximal half of the feathers, i.e., there seem to be less bacteria closer to the skin (Muza, Burtt, & Ichida, 2000). Nonetheless, there is evidence from noncultural approaches, that there is plenty of bacterial genetic material extractable from the skin of Zebra Finches, Diamond firetails (Stagonopleura guttata), and Bengalese finches (Lonchura striata domestica) (Engel et al., under review). These bacteria might also be involved in shaping the Zebra Finches body odor. Not only bacteria on the “outside” of the Zebra Finch but also from the “inside” could be odor producing. In the crop and esophagus of hoatzins (Opisthocomus hoazin), a folivorous bird, volatile fatty acids are produced by microbial fermentation (Grajal, Strahl, Parra, Dominguez, & Neher, 1989), a process that probably produces the frequently reported foul odor of this bird (Weldon & Rappole, 1997). 3.1.4 Summary of the Production of Scents Much progress has been made within the last years to understand the mechanisms of odor production in birds. The main source of odors used in olfactory communication is most likely the preen gland and its secretion. These secretions are known to encode information about species, sex, reproductive status, individual identity, and age; factors all being important to find a potential mate. Although, apart from information about the species, we currently do not know whether this information is also present in the preen gland secretion of Zebra Finches. Behavioral tests, however, have convincingly demonstrated that body odors of Zebra Finches encode information about genetic similarity or relatedness. Furthermore, behavioral experiments have shown that Zebra Finches have a well-developed sense of smell and that the sense of smell is fundamental to recognize unfamiliar kin. However, the underlying molecular

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mechanisms and pathways, the impact of the MHC on odor production and its interactions with microbes, as well as the neurobiological processing of these odors are still not known and will be in focus of future research.

3.2 Perception and Processing of Scent There is only a limited number of studies on the neurobiological basis of avian scent perception, and so far, nothing has been published concerning this issue in Zebra Finches. In this paragraph, we will therefore rely on what is known from other birds to discuss possible mechanisms of odor processing in the Zebra Finch brain. 3.2.1 The Olfactory Receptors In birds in general, like in other vertebrates, the odorants enter the nasal cavity, composed by a series of nasal chambers, through the paired nostrils (Bang, 1971; Jones & Roper, 1997). The olfactory receptor neurons within the most caudal chamber are embedded in the mucus-covered nasal epithelium. The dendrites of these neurons contain the so-called seven-transmembrane domain G protein-coupled receptors, to which the odorant molecules bind after passing the mucus (Reed, 1992). Binding leads to the formation of second messenger molecules that cause, by direct gating of cation channels, the olfactory receptor neurons to depolarize and generate action potentials (Schild & Restrepo, 1998). It is thought that each of the receptors is specialized for just one odor, and each receptor neuron projects to a special glomerulus, the functional units of the olfactory bulb (see Fig. 4), which is the next station of the olfactory system (Buck, 2004; Mombaerts et al., 1996).

Fig. 4 (A) Zebra Finch brain and (B) a coronal section through the olfactory bulb (OB) showing a high number of c-Fos expressing neuronal nuclei (neuronal activity marker) which are stained black after the immunohistochemical procedure. The nonactivated cells are blue due to the counter staining (Giemsa). Scale bar 200 μm.

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A second parallel olfactory system with an extrasensory epithelium, the vomeronasal organ, is lacking in birds as well as in crocodiles and turtles (Bruce, 2007; Reiner & Karten, 1985). This system has been thought to exclusively process pheromones (Eisthen, 1992; Halpern & Martı´nezMarcos, 2003). However, it is known that the main olfactory system also processes a big number of pheromones (Brennan & Zufall, 2006). Thus, the lack of this system in birds does not indicate that pheromones are not detected in birds (Caro & Balthazart, 2010). 3.2.2 Olfactory Receptor Genes in Birds The number of genes coding for olfactory receptors have recently been evaluated in several bird species, proposing that the number of olfactory receptor genes correlates with the scent detection abilities of a given species (Steiger, Fidler, Valcu, & Kempenaers, 2008). According to these experiments, birds comprise between 100 and 650 genes for olfactory receptors (Steiger, Fidler, & Kempenaers, 2009; Steiger et al., 2008; Steiger, Kuryshev, Stensmyr, Kempenaers, & Mueller, 2009). This is a higher number of genes compared with species like the zebrafish (Danio rerio, approximately 150), but lower than in mice (1000 receptors; Buck & Axel, 1991), making the birds an intermediate case on this regard. Humans are, with 339 genes (Malnic, Godfrey, & Buck, 2004), medial between the lowest and highest counts of birds. However, within the birds, Zebra Finches as well as chickens (Gallus gallus) have a significant larger amount of olfactory receptor genes than other birds (Khan et al., 2015). The variation in the number of olfactory receptor genes may be a result of functional specialization (see also Healy & Guilford, 1990). Nocturnal species, for example, tend to possess more olfactory receptor genes than diurnal ones, probably due to the increased need of scent discrimination abilities as an alternative sensory processing strategy when vision is not efficient (Steiger, Fidler, et al., 2009; Steiger et al., 2008; Steiger, Kuryshev, et al., 2009). Furthermore do they tend to have larger olfactory bulbs (Healy & Guilford, 1990). However, both Zebra Finches and chickens are rather diurnal than nocturnal and thus their high number of olfactory receptor genes (Khan et al., 2015) seems to have evolved on other selective pressures. In Zebra Finches, data mining of the complete genome revealed the presence of 479 olfactory receptor genes including 111 pseudogenes (genes that have lost some functionality; Steiger, Kuryshev, et al., 2009). Olfactory receptor gene studies therefore suggest that birds possess a quite well developed and adaptive sense of smell, in contrast to what has been believed previously based on neuroanatomy (Bang & Cobb, 1968).

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3.2.3 Processing of Olfactory Stimuli in the Avian Brain Calcium imaging on isolated olfactory epithelium in chicks of the domestic fowl revealed that these birds probably have better odor resolution than that predicted by the number of receptor types. The olfactory neurons of these birds respond to odorants with either increases or decreases in calcium ion (Ca2+) concentration (Restrepo, Zviman, & Rawson, 1995). Such odorantinduced calcium fluxes in the olfactory sensory neurons are common to most species (Gomez & Celii, 2008; Hildebrand & Shepherd, 1997; Jung, Wirkus, Amendola, & Gomez, 2005), but surprisingly some individual receptor cells of chicks respond to one odorant with an increase in calcium ions and to another odorant with a decrease in calcium ion concentration. This is different from a commonly accepted hypothesis of olfactory coding as mentioned earlier (Buck, 2004; Mombaerts et al., 1996) and may be seen as an adaptation to compensate for the relatively narrow olfactory receptor gene complement of chicks (only about 15 different odor receptors with about 100 functional variants; Leibovici, Lapointe, Aletta, & Ayer-Le Lievre, 1996; Lievre, Lapointe, & Leibovici, 1995; Nef, Lush, Shipman, & Parada, 2001; Nef & Nef, 1997) that may allow the system to detect and encode more distinct types of odorants with a limited number of neurons dedicated to odor processing (Gomez & Celii, 2008). Whether this mechanism is a speciality of chicks or could be generalized to other birds, including the Zebra Finch, or even nonavian species has to be investigated in future studies. Another set of studies was focusing on the electrophysiological properties of olfaction in birds, with data being collected beginning already in the 1960s (Wenzel, 2007). Recording of “response spindles” from the olfactory bulbs of several bird species showed the first direct evidence of odor processing’s in birds (Sieck & Wenzel, 1969; Wenzel, 1967; Wenzel & Sieck, 1972). Also, action potentials from fiber bundles in the olfactory nerves of 14 bird species representing a wide range of olfactory bulb size were recorded at about the same time (Tucker, 1965). This was followed by recordings of singleunit responses to odors from olfactory receptor cells in the turkey (Cathartes aura), the black vulture (Coragyps atratus), and also from the olfactory bulb of pigeons (Hutchison & Wenzel, 1980; Shibuya & Tonosaki, 1972; Shibuya & Tucker, 1967). More recently, by using electroolfactography, a standard technique to measure odorant-induced large-scale electrical activity across the surface of the olfactory epithelium (Scott & Scott-Johnson, 2002), it was possible to demonstrate that the olfactory system is functional already during their embryogenesis in chicks (Lalloue, Ayer-Le Lie`vre, & Sicard, 2003).

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From the olfactory receptor neurons, information is transferred to the olfactory bulb, a multilayered structure in the frontal part of the vertebrate brain. In birds, this structure is visibly smaller in proportion to the rest of the brain than, for example, in rodents (Bang & Cobb, 1968). It is organized into numerous uniform subunits, the so-called glomeruli, which are innervated directly by the axons of the receptor neurons on the ipsilateral side (Bang & Wenzel, 1985; Morrison & Costanzo, 1992; St John, Clarris, & Key, 2002). Typical for the glomerular organization of olfactory system is the convergence of axons from olfactory sensory neurons that express the same receptor onto the same glomeruli in a precise and stereotypic fashion (Mombaerts et al., 1996). This means that the more types of receptors are present in a species, the more glomeruli are required, and this in turn enhances the size of the olfactory bulb. Indeed, the number of the potentially functional olfactory receptor genes in birds correlates roughly with the size of their olfactory bulbs (Steiger et al., 2008). 3.2.4 The Olfactory Bulb and Olfactory Sensory Pathways In vertebrates, the relative size of the olfactory bulb correlates with olfactory capability and is often used to estimate the importance of olfaction to a species’ ecology (Corfield et al., 2015; Finlay & Darlington, 1995; Finlay, Darlington, & Nicastro, 2001; Gonzalez-Voyer, Winberg, & Kolm, 2009; Reep, Finlay, & Darlington, 2007; Yopak, Lisney, & Collin, 2015; Yopak et al., 2010). Birds also exhibit strong variation in olfactory bulb size (Bang & Cobb, 1968; Corfield et al., 2015), and this variation may again be due to adaptation to different ecological needs, as suggested by studies showing for a number of avian species correlations of the olfactory bulb size and olfactory-mediated behaviors such as foraging strategies, habitat, nesting behaviors, diet, and activity patterns (Bang, 1971; Bang & Wenzel, 1985; Buschh€ uter et al., 2008; Corfield, Eisthen, Iwaniuk, & Parsons, 2014; Hagelin, 2004; Healy & Guilford, 1990; Mackay-Sim & Royet, 2006). The response properties of olfactory bulb neurons in birds resemble those described in mammals. Avian olfactory bulb neurons are spontaneously active, either increase or decrease their firing rate after odor stimulation, and adapt to repeated presentation of the same stimulus (McKeegan, Demmers, Wathes, Jones, & Gentle, 2002; McKeegan & Lippens, 2003; Sieck & Wenzel, 1969; Wenzel & Sieck, 1972). Thus, the avian olfactory bulb (see Fig. 4) exhibits a high degree of structural and functional similarity with that of other vertebrates. But, as stated earlier, there are also differences: birds (together with crocodiles and turtles) lack the vomeronasal organ

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(Bruce, 2007). Consequently, the projection area of this structure, the accessory olfactory bulb, is also missing in birds (Reiner & Karten, 1985). The absence of the vomeronasal organ and the accessory olfactory bulb accounts of course for part of the reduced relative size of olfactory bulb in birds, with respect to other vertebrates. A unique feature of the olfactory sensory pathway is the fact that its primary sensory area (the olfactory bulb) is already located within the telencephalon, and its connections proceed further to telencephalic areas without passing the thalamus, like it is the case for the other sensory modalities. This feature is shared by all vertebrates, including the avian species. Probably, the first study to describe the telencephalic projections of the olfactory bulb in a bird was based on electrophysiological methods and the Fink–Heimer staining (Rieke & Wenzel, 1978). These authors reported projections from the pigeon olfactory bulb to the ipsilateral prepiriform cortex, the mesopallium, the medial striatum, the nucleus accumbens, and the contralateral globus pallidus (crossing via the anterior commissure). Partly deviating results were obtained from the same species in a subsequent study using autoradiographic techniques (Reiner & Karten, 1985). These authors reported contralateral projections (via the habenular commissure) to the septum, the prepiriform cortex and the piriform cortex, the olfactory tubercle, and the nucleus taeniae of the arcopallium. Only the prepiriform cortex was consistently indicated as a target region by both studies. Interestingly, Reiner and Karten (1985) directly compared the olfactory projection of pigeons with those of turtles, finding remarkable similarities, despite the larger relative size of the olfactory bulb in turtles. This suggests that the pattern of olfactory projections could be similar in birds and reptiles, except for the target regions inside the amygdala, which might be reduced in birds. Patzke, Manns, and G€ unt€ urk€ un (2011) mainly confirmed the results of Reiner and Karten (1985), and in addition showed that most likely the olfactory system of birds is not lateralized, a feature, which was suggested by results from behavioral studies (but see later). The most recent study by Atoji and Wild (2014) even extended the results mentioned earlier. In addition to the projections to the piriform and prepiriform cortex, they identified target areas like the anterior olfactory nucleus, the tenia tecta, the densocellular part of the hyperpallium, the hippocampal continuation, and the dorsolateral corticoid area. Each olfactory bulb was also projecting commissural fibers to its contralateral counterpart and receiving ipsilateral afferents from the ipsilateral (but not contralateral) pallium, including the prepiriform cortex. Projections from the prepiriform cortex reach the caudolateral nidopallium

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and parts of the limbic system, including the hippocampal formation, septum, lateral hypothalamic nucleus, and lateral mammillary nucleus. Moreover, the prepiriform cortex provides a centrifugal projection to the olfactory bulb and, overall, based on these results seems to act as a relay station to the limbic system (Atoji & Wild, 2014). 3.2.5 Brain Regions Involved in Behavior Affected by Olfaction Not much is known about the function of the areas that receive direct or indirect olfactory input. The role of olfaction in pigeon navigation has been tested behaviorally by manipulating the access to olfactory information and by releasing anosmic or piriform cortex lesioned birds (Wallraff, 2005 for references). Gagliardo, Odetti, Ioale`, Pecchia, and Vallortigara (2005) and Gagliardo et al. (2007) tested the role of olfactory cues for navigation in a familiar environment in pigeons by unilateral closure of the nostrils or unilateral piriform cortex lesions. According to their experiments, both hemispheres seem to be necessary for olfactory orientation, but there was a stronger effect with right hemisphere treatments. In a recent immediate early gene (IEG) expression study, increased IEG expression (indication of higher neural activity) was observed in both the olfactory bulb and the piriform cortex after navigation. This activation was significantly reduced after unilateral occlusion of the right, but not of the left, nostril, revealing again functional lateralization for this function (Patzke, Manns, G€ unt€ urk€ un, Ioale`, & Gagliardo, 2010). Lateralization of the piriform cortex in relation to olfactory-mediated navigation was also confirmed by Jorge, Marques, Pinto, and Phillips (2016). The hippocampal formation receives indirect olfactory input mediated by the prepiriform cortex (Atoji & Wild, 2014). Indeed, Jorge, Phillips, Gonc¸alves, Marques, and Ne˘mec (2014) showed in pigeons that odor exposure stimulates neuronal activity in the dorsolateral area of the hippocampal formation during navigation. The hippocampal formation is notoriously important for various forms of spatial navigation both in mammalian and avian species, including the Zebra Finch (Bingman et al., 2005; Bingman & Sharp, 2006; Mayer & Bischof, 2012; Mayer, Pecchia, Bingman, Flore, & Vallortigara, 2016; Mayer, Watanabe, & Bischof, 2013; Watanabe & Bischof, 2004; Watanabe, Mayer, Maier, & Bischof, 2008). It is presumed to combine different sensory cues and also memory content to a cognitive map of space (O’Keefe & Nadel, 1978). The results of Jorge et al. (2014) indicate that odor cues could also add to the cues used for forming such map as a basis for orientation within the hippocampus. The hippocampus is also

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strongly interconnected with the septum (Atoji & Wild, 2004), which is also recipient of projections from the olfactory bulb (Reiner & Karten, 1985). Another direct target region of the olfactory bulb is the nucleus taeniae, located within the arcopallium (Reiner & Karten, 1985), which is considered to be homologous to the mammalian subpallial, medial amygdala (Cheng, Chaiken, Zuo, & Miller, 1999; Jarvis et al., 2005; Reiner et al., 2004; Yamamoto & Reiner, 2005; Yamamoto, Sun, Wang, & Reiner, 2005) and thus named nucleus taeniae of the amygdala (TnA), that projects also to the hippocampus (Casini, Bingman, & Bagnoli, 1986; Cheng et al., 1999). The nucleus taeniae abundantly expresses androgen and estrogen receptors (Balthazart, Absil, Gerard, Appeltants, & Ball, 1998; Balthazart, Foidart, Wilson, & Ball, 1992; Bernard, Bentley, Balthazart, Turek, & Ball, 1999; Martinez-Vargas, Stumpf, & Sar, 1976) and is involved in a wide range of sociosexual behaviors (Absil, Braquenier, Balthazart, & Ball, 2002; Cheng et al., 1999; Ikebuchi, Hasegawa, & Bischof, 2009; Thompson, Goodson, Ruscio, & Adkins-Regan, 1998). Interestingly, in the Zebra Finch, an altricial species, the nucleus taeniae can be already delineated from the first day after hatching and is for several days the most prominent structure of the caudal forebrain (Ikebuchi, Nanbu, Okanoya, Suzuki, & Bischof, 2013). This suggests, together with the above-mentioned finding of the very early functionality of the olfactory system in birds (Lalloue et al., 2003), including Zebra Finch hatchlings (Caspers et al., 2017), an early involvement of this area in social functions, possibly in relation to responses of young nestlings to olfactory social cues, as it has been shown in a series of behavioral experiments (see Section 2.1; Caspers, Hagelin, et al., 2015; Caspers et al., 2013; Krause et al., 2012). The nucleus taeniae is, based on its homology to the medial amygdala, its connectivity, and its involvement in social behavior control, considered as to be part of the so-called social behavior network (and of the wider “social decision-making network,” encompassing the first one together with the “mesolimbic reward system”), a group of strongly interconnected areas that control sociosexual behaviors and contain sex steroids receptors (Goodson, 2005; Newman, 1999; O’Connell & Hofmann, 2011). It is thus conceivable that nucleus taeniae is one of the stations where olfactory information is fed into this network. Another node of the social behavior network, the septum, also receives direct olfactory input. In a third one, the preoptic area, although it does not receive direct olfactory input, a modulation of its neural activity has been shown in quails by olfactory input from the sexual partner (Taziaux, Kahn, Moore, Balthazart, & Holloway, 2008).

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3.2.6 Summary of the Perception of Scents Taken together, our present knowledge about the olfactory system in birds, presumably including the Zebra Finch, does not indicate that this system is in any aspect inferior to that of other vertebrates. Its principal organization is (with the exception of the vomeronasal system which is not existent in the Zebra Finch and birds in general) very similar in all vertebrates. The importance of the olfactory system for behavioral control and its size and organization appears to correlate with the environmental needs of a given species, independent of being a reptile, a bird, or a mammal. Especially, the gene studies on the richness of odor receptors clearly show that the resolution of the avian olfactory system is somewhat intermediate between “microsmatic” and “macrosmatic” species. Among birds, there is also a big variation between species in the number of olfactory receptor genes, ranging from 100 to 600 genes. Thus, some of the birds comprise gene counts more than humans—if the number of receptor genes indeed code the resolution of the system, Zebra Finches are, depending on how one reads the data, comparable with or even better than humans in smelling. However, although compelling, such comparisons should not be taken too serious. The main point of further research should be to extend our knowledge about the involvement of odor perception in the guidance of reproductive and social behavior (Caro et al., 2015) and navigation in space (Mayer et al., 2013). This is, on the physiological side, based on the findings described earlier concerning the connections of the olfactory system with the social behavior network and with the hippocampal formation, and also on a few experiments already indicating that odor plays a role in activating some of these areas. Thus, as already mentioned for other aspects of neurophysiological processing like song learning and production or learning (Brainard & Doupe, 2002; Scharff & Nottebohm, 1991) and orientation based on visual cues, the Zebra Finch might also be an ideal subject for the study of the neurophysiology of behavior guided by olfactory cues.

4. METHODS TO EXAMINE OLFACTION IN ZEBRA FINCHES 4.1 Behavioral Methods Zebra Finches, as most songbird species, are dominated by their acoustic and visual capacities and do not show any obvious odor-guided behavior. The majority of studies testing the olfactory ability of birds, including Zebra Finches, used either tests, in which odors are given sequentially

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(Caspers, Hagelin, et al., 2015; Cunningham, Van Buskirk, Bonadonna, Weimerskirch, & Nevitt, 2003; Hagelin et al., 2013; Porter, Hepper, Bouchot, & Picard, 1999; Rossi et al., 2017) or simultaneously (e.g., Bertin et al., 2010; Bonadonna et al., 2006; De Leo´n, Mı´nguez, & Belliure, 2003; Hagelin, Jones, & Rasmussen, 2003; Krause et al., 2014; Leclaire et al., 2017; Sneddon et al., 1998; Whittaker et al., 2011). While the sequential presentation of odors has mainly been used for juvenile birds, binary choice tests have been used for all age classes to test whether birds discriminate between two odors belonging to two different groups (e.g., similar or dissimilar MHC type (Leclaire et al., 2017), partner vs conspecific (Bonadonna & Nevitt, 2004), conspecific vs heterospecific (Krause et al., 2014; Zhang, Du, & Zhang, 2013). Age-specific methods to measure olfactory sensitivity and olfactory discrimination abilities have also been used in Zebra Finches. Altricial hatchlings, for example, are quite immobile and show a limited repertoire of behaviors, of which begging is the most frequent (Muller & Smith, 1978). This behavior has been used to develop an odor discrimination begging test (Caspers, Hagelin, et al., 2015), based on the idea of Porter et al. (1999), which has been successfully used also in seabird chicks (Bonadonna et al., 2006; Cunningham et al., 2003). In the Zebra Finch test paradigm (Caspers, Hagelin, et al., 2015), the time of begging was measured as a response to sequentially presented olfactory stimuli (Caspers, Hagelin, et al., 2015). Therefore, a plastic wash bottle containing an odor stimulus was pressed 10 times (once per second) within one centimeter distance of the nares (Caspers, Hagelin, et al., 2015). Zebra Finch chicks usually start begging as a response to the odor stimuli, probably partly also induced by the tactile stimulus of the airflow (Bischof & Lassek, 1985). By comparing the begging durations as a response to the different sequential presented odor stimuli, it can be determined whether chicks are able to differentiate in their reactivity between two odors. This method has successfully been used not only in Zebra Finches (Caspers, Hagelin, et al., 2015; Caspers et al., 2017) but also recently in free-living blue tits (Rossi et al., 2017) and may probably be used in other altricial birds. Once the birds have their eyes open, and especially after fledging, young are mobile and heavily distracted by visual stimuli. Here, test setups are used where individuals are given the choice between simultaneously presented odors (Caspers et al., 2013; Caspers & Krause, 2011; Krause et al., 2014, 2016, 2012; Krause & Caspers, 2012) or sequentially presented odors (Kelly & Marples, 2004; W€ urdinger, 1990). Independent of the test situation used, the behavior of the test individual is analyzed, for example, the time a

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test individual spent in the vicinity of a certain odor, the latency until it reached the specific stimulus or the first choice of the test individual. These procedures are widely used, but have the disadvantage as those individuals that are inactive during the test procedures are usually not informative and thus not involved in the statistical analysis (Bonadonna & Nevitt, 2004; Caspers & Krause, 2011; Krause et al., 2014, 2012; Krause & Caspers, 2012). Thus, patterns of discrimination abilities are based on a subset of active birds only. Therefore, measuring physiological changes instead or ideally in combination with measuring the behavioral changes of test birds would probably reveal a more comprehensive understanding and is one of the major issues for future research.

4.2 Impairing the Olfactory Sense Another possibility to test the function of olfaction in birds is to impair the birds ability to perceive odors, either by sectioning the olfactory nerve (Balthazart & Schoffeniels, 1979) or by temporarily impairment, e.g., using zinc sulfate solutions (Gagliardo et al., 2013; Holland et al., 2009). Zebra Finch females that have been zinc sulfate treated, i.e., made temporarily anosmic, paired, and reproduced successfully, indicating that olfaction is not mandatory for reproduction in Zebra Finches (Caspers, Gagliardo, et al., 2015). However, females being treated with zinc sulfate behaved differently in the presence of close kin, compared to control females (Caspers, Gagliardo, et al., 2015; see also Section 2.1.3). Thus comparing control and olfactory impaired birds can reveal new insights on the function of olfaction, in situations where choice tests cannot be used. Where choice tests provide insights to the reactions to selected scents, these “knock-out” like experiments provide insights from the opposite perspective, i.e., what happens when all scent perceptions are absent.

4.3 Analyzing the Chemical Signal When conducting tests related to the role of olfaction in social communication, usually body odors of individuals belonging to different categories (e.g., conspecifics vs heterospecifics; kin vs nonkin) are used (e.g., Caspers et al., 2017; Krause et al., 2014; Rossi et al., 2017). To avoid any possible impact of visual or acoustic cues carriers of odor stimuli, e.g., odor impregnated transport bags (Caspers et al., 2017; Krause et al., 2014), cotton pads (Caspers, Hagelin, et al., 2015), or nest material (Caspers & Krause, 2011; Krause & Caspers, 2012; Krause et al., 2012) are used.

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As described earlier (see Section 3.1) much effort has been done to characterize the chemicals involved in olfactory communication in birds (reviewed in Campagna et al., 2012). Thereby, most studies focused on the preen gland secretion (Jacob, Balthazart, & Schoffeniels, 1979; Mardon et al., 2010; Soini et al., 2007; Whittaker et al., 2010) and only a few on feathers and overall body odors (Mardon, Saunders, & Bonadonna, 2011b). Chemical analyses, using gas chromatography (GC), revealed that the chemical fingerprints of Zebra Finches are significantly different from those of Diamond firetails (Krause et al., 2014). In this study Krause et al. (2014) analyzed the volatiles emitted from nylon socks containing the odor of a bird. Therefore, a bird impregnated a transport bag (a dark nylon sock) with its body odor. Afterward the sock was put into a glass container and the headspace was collected in a closed loop apparatus. This method allowed to sample all volatiles present on the bird’s body and not only those present in the preen gland secretion. However, identification of specific substances in the Zebra Finch body odor is still missing and is subject to current research. A similar technique has been used to characterize chemical fingerprints from different Zebra Finch nests (Kohlwey et al., 2016). Here, nest material of different families has been placed into the glass containers and the headspace of the nest material of different nests has been collected. For the alignment of GC-data, a new software tool implemented in R is available (Ottensmann, Stoffel, & Hoffman, 2017). Bioassays testing particular substances in birds are still rare (Balthazart & Schoffeniels, 1979), especially as Zebra Finches like many other birds show no specific olfactory-guided behaviors, as for example, a sniffing movement. However, odors can change frequencies and durations of behaviors in Zebra Finches (Caspers, Hagelin, et al., 2015; Caspers & Krause, 2011). To measure the olfactory signals as well as the behavioral response a couple of analytical tools and behavioral tests are available, which should be combined more often in future studies.

5. CONCLUSION As the Zebra Finch (Taeniopygia guttata) is an important avian key model (Griffith & Buchanan, 2010; Griffith et al., 2017), the knowledge on olfaction in this species and future studies are of key importance as they can be integrated in an unprecedented way in a large body of knowledge of behavioral development, mechanisms, and functions, providing a more integrated understanding of animal behavior (e.g., Buchanan, Griffith, & Pryke, 2010;

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Riebel, 2009; Warren et al., 2010; Zann, 1996) in both the laboratory (e.g., Forstmeier et al., 2007) and the field (e.g., McCowan, Mainwaring, Prior, & Griffith, 2015). We here reviewed the use of olfaction and its potential underlying mechanisms. We have shown that Zebra Finches have a well-developed sense of smell, which is particularly sensitive to odors used in social communication throughout life. Although progress was made in understanding of the functions of olfactory communication, much more future research is needed to fully understand the role of olfaction and its interaction with other senses throughout life. Furthermore, potential future research should direct to the understanding of the molecular pathways and the genes that are involved in odor production, as well as to what extend the MHC and microbes interfere with the body scent. We assume that the olfactory communication, thus far only tested in Zebra Finches in captivity, is also important in the free-living birds. Therefore, it will also be important to investigate the impact of odors under natural conditions. Investigating the use of olfactory communication in the wild will therefore enhance our understanding of the Zebra Finches world. Although Zebra Finches have small olfactory bulbs, this review illustrates that the relative size of this brain region is not necessarily associated with its function. It probably reflects the ecological needs of the species, where olfaction is probably more important in social communication than for nonsocial contexts such as, for example, foraging. We hope that our review inspires other researchers to have this sense in mind. The Zebra Finch is far more than just only a songbird; it is a scented songbird.

ACKNOWLEDGMENTS We thank Marc Naguib for encouraging us to write the chapter. We further thank Marc Naguib and an anonymous reviewer for constructive and helpful comments on an earlier version of the manuscript. B.A.C. was supported by a Freigeist Fellowship of the VolkswagenStiftung (88137). E.T.K. has been supported earlier, for the studies on olfaction in Zebra Finches, by a grant from the VolkswagenStiftung (85994).

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