Intraspecific Olfactory Communication in Zebra Finches

Chapter 27

Intraspecific Olfactory Communication in Zebra Finches (Taeniopygia guttata): Potential Information Apart from Visual and Acoustic Cues Barbara A. Caspers and E. Tobias Krause

Abstract In this chapter we review evidence for olfactory communication in the zebra finch (Taeniopygia guttata). We discuss studies that indicate that zebra finches are capable of olfaction and use olfactory cues for social communication and kin recognition. This finding establishes a so far completely neglected mechanism of kin recognition in songbirds.

27.1

The Sense of Smell in Passerines

Passerines or songbirds, especially males, are primarily known for their acoustic abilities as they use song to attract females and/or to deter male competitors (e.g. Catchpole and Slater 2008; Schmidt et al. 2008; Sprau et al. 2010; Naguib and Mennill 2010). Intraspecific communication in many songbird species is also achieved through visual signals, such as colourful plumage traits (e.g. Hill and Montgomerie 1994; Ohlsson et al. 2002; Hill and McGraw 2006) or nest constructions that attract females with their exaggerated architecture and decoration (e.g. Collias 1964; Borgia 1985, 1995; Brouwer and Komdeur 2004). The idea that olfactory signals might also play an important role in intraspecific communication in songbirds thus seems to be unlikely at first sight, for several reasons. First, because songbirds were for a long time thought to be anosmic, due to their small olfactory bulb (Bang and Cobb 1968). For example, the mean relative olfactory bulb size of 29% for species within the Procellariiformes, a bird taxon known for good olfactory

B .A. Caspers (181) • E. T. Krause Department of Anima! Behaviour, University of Bielefeld, PO Box 100131,33501 Bielefeld, Germany e-mail:. barbara.caspers @uni-bielefeld.de; tobias.krause@ uni -bielefeld.de M.L. East and M. Dehnhard (eds.), Chemical Signals in Verfehrates 12, 341 DOI 10.1007/978-1-4614-5927-9_27, ©Springer Science+Business Media New York 2013

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Fig. 27.1 Visual plumage traits may represent a basis for species (a vs. b), sex (a-male left, female right) and probably also individual recognition (individual differences between individual in a, b), as examples from a dimorphic species (a) the zebra finch (Taeniopygia guttata) and (b) a monomorphic species the diamond firetail (Stagonopleura guttata)

capacities (e.g. N evitt et al. 1995; Bonadonna and Nevitt 2004; Nevitt and Bonadonna 2005; Bonadonna et al. 2007; Mardon et al. 2010), is about three times bigger than the average relative olfactory bulb size of 9.7% in the Passeriformes (Bang and Cobb 1968). Second, as visual and acoustic signals are known to play such significant roles in bird behaviours such as in the recognition of species (e.g. Emlen 1972; Price 1998; Uy et al. 2009; Fig. 27.1), sex (e.g. Saetre and Slagsvold 1992; Fig. 27.1) and individual identity (Brooks and Falls 1975; Levrero et al. 2009; Jacot et al. 2010), it could be questioned which additional information might be communicated by olfactory signals because passerines, such as other birds, do not show any clear olfactorydriven behavümr. In this chapter we review evidence that olfactory signals are nevertheless likely to play an additional and important role in social communication of songbirds (e.g. Roper 1999; Zelano and Edwards 2002; Hagelin and Jones 2007) and discuss experimental evidence of olfaction in the zebra finch (Taeniopygia guttata).

27.2

Olfaction in Passerines

Within the last decade, evidence that songbirds indeed have a sense of smell has grown. Birds are thought to make use of their sense of smell for predator avoidance (e.g. Amo et al. 2008, 2011), to locate food (e.g. Kelly and Marples 2004; Mennerat

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et al. 2005), during nest construction (e.g. Mennerat 2008; Gwinner and Berger 2008) and for orientation (Holland et al. 2009; Caspers and Krause 2011). Furthermore, although the olfactory bulb is relatively small, songbirds have a large number of olfactory receptor genes (Steigeret al. 2008, 2009; Warren et al. 2010), indicating that the sense of smell might be more sophisticated and important than traditionally assumed. Chemical analysis of preen oil secretion of a north American songbird species, the dark-eyed junco (Junco Hyemalis), revealed that these birds indeed possess body odours that might encode information about sex, species, individual identity and population affiliation (Whittaker et al. 2010), and perhaps also about condition (Whittaker et al. 2011). Thus the chemical structure of these signals could potentially be used in mate recognition. Nevertheless studies showing that olfactory cues are used for social communication in songbirds are still rare and absent in many passerine species. In contrast to this lack of knowledge in passerines, experimental evidence exists that some other bird species indeed make use of the available body odour differences for sex (e.g. Mardon et al. 2010; Zhang et al. 2010; but see Mardon et al. 2011) and even mate recognition/choice (e.g. Bonadonna and Nevitt 2004; Leclaire et al. 2012). Only recently it has been detected in blue petreis (Halobaena caerulea) that closely related individuals have a more similar odour profile than unrelated individuals (Celerier et al. 2011). Thus olfactory cues might, as it has been shown for mammals, fish, amphibians and insects (e.g. Hepper 1991), provide information about kinship. Humboldt penguins (Spheniscus humboldti) have been shown to distinguish between kin and non-kin based on olfactory cues alone (Coffin et al. 2011). ls it possible that songbirds might also use olfactory cues for kin recognition?

27.2.1

Mechanisms of Kin Recognition in Songbirds

lnbreeding, i.e. mating with a closely related conspecific, leads to a reduction in genetic variation. This reduction of genetic variation usually leads to a decrease in heterozygosity and consequently to the possibility that inbred offspring suffer from deleterious and/or recessive traits. To avoid inbreeding depression, individuals should therefore preferably mate with non-related individuals. Furthermore, recognition of kin might not only prevent inbreeding, but also is thought to have promoted the evolution of cooperation (Hamilton 1964). By helping closely related individuals to raise their offspring, individuals increase the own inclusive fitness. However, in both cases individuals have to be able to recognise kin. Indeed, there is certain evidence that birds are able to recognise kin. Fernale zebra finches, for example, adjust their reproductive effort in response to the genetic similarity of their unfamiliar mates (Arct et al. 2010). Peacock (Pavo cristatus) malesform leks with close-related males that they have not been associated with before (Petrie et al. 1999). These findings lead to the question which underlying mechanism allows individuals to distinguish between kin and non-kin?

B.A. Caspers and E.T. Krause

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One mechanism of kin recognition is associative leaming of acoustic and/or visual cues. Long-tailed tit nestlings learn the call of their family members and are able to · recognise kin based on these calls (Sharp et al. 2005). Since the recognition signal is not or only partially genetically based, the possibility of mismatch is higher because there is the possibility that not only the receiver but also the sender learned the signal . from non-kin (Fig. 27.2). Male songs, for example, are learned from the father or another tutor and it has been shown that male songs are very similar to the tutor, no matter if it is the father or an unrelated male (Eales 1985; Slater et al. 1988). Zebra finches are probably one of the best studied songbird species in terms of imprinting and early learning (e.g. Immelmann 1959, 1961, 1968, 1970; Immelmann et al. 1978), and in this species, associative learning of visual and acoustic cues does not explain how individuals recognise kin. Fernale zebra finches are sexually imprinted on acoustic and visual cues of their fathers during the nestling period or shortly after. In mate choice tests, females showed a strong preference for males that looked (Oetting and Bischof 1996; Witte and Caspers 2006) and sang (Clayton 1988; Riebel2000) like their fathers do (Fig. 27.3). This suggests that females are likely to preferentially mate with unfamiliar brothers from an earlier brood or cousins (i.e. males which learned their song from the samegrandparental pathway). 1t is Jikely that female zebra finches do meet unfamiliar relatives from earlier broods

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Fig. 27.4 The time frame of the sensitive phases, in which templates are Jearned, for olfactory, visual and acoustic cues. Olfactory cues are probably learned within the first hours after hatching visual cues between day I 0 and 35 (Oetting and Bischof 1996; Witte and Caspers 2006) and acoustic cues between day 30 and 60 (Clayton 1988; Riebel2000)

in their natal colony as there is no sex-biased dispersal in this species, and despite high annual mortality, about 25% of the breeding birds are natal to the colony (Zann 1996). The use of visual and acoustic cues for kin recognition also appears error-prone, because contact with non-kin is possible during the sensitive period when sexual imprinting occurs (Fig. 27.4). The sensitive phase, during which visual cues are learned, is between day 10 and 35 (Oetting and Bischof 1996; Fig. 27.4) whereas song learning continues after fledging between day 30 and 60 post-hatching (Clayton 1988; Riebel 2000; Brainard and Doupe 2002; Fig. 27 .4). As visual and especially acoustic cues are learned afterjuveniles have left the nest, this increases the possibility that they learn these cues from non-kin (Figs. 27.3 and 27.4 ). So if association with the father is necessary to fmd a potential mate that is similar to the father but not too similar (Bateson 1982) using solely visual and acoustic cues might lead to mistakes in kin recognition. Additionally, associative learning of patemal cues

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might Iead to recognition errors in nests containing chicks sired by more than one male. The ratio of extra pair young varies tremendously in songbirds, with species such as the zebra finch having a relatively low rate of about 2% (Griffith et al. 2010), to species with more than 70% of extra pair young (Griffith et aL 2002). Arecent study found that zebra finches adjust their reproductive effort in response to the genetic similarity to their partner (Arct et al. 2010) suchthat pairs composed of unfamiliar kin had a lower probability to reproduce successfully compared to pairs composed of random partners. These results suggest that zebra finches have the ability to recognise kin, but the exact underlying mechanism was unknown. In many other vertebrate species (e.g. Waldmann 1991; Penn 2002; Levy et al. 2004; Holmes and Mateo 2007) and even in some non-passerine bird species (e.g. Bonadonna and Nevitt 2004; Bonadonna et al. 2007; Mardon et al. 2010), olfactory cues have been found tobe crucially involved in social communication, including kin recognition. Recently zebra finches were found to use olfactory cues for Orientation and discrimination between natal and non-natal nest odours (Caspers and Krause 201 1). It seems possible that olfactory cues might represent an additional information channel to zebra finches as for example in parent-offspring communication, or kin recognition.

27.3 First Evidence for Olfactory Social Communication Parent offspring communication is the earliest social communication in the Iife of a zebra finch. In altricial birds, chicks are reared in a nest, making it difficult to disentangle cues used for nest and/or offspring recognition. To identify the own nest, parents rely on visual cues (e.g. Peek et al. 1972; Trillmich 1976; Hughes et al. 1995), or on acoustic cues, Iike the begging calls of the own chicks (e.g. Levrero et al. 2009). In order to test whether olfactory cues might also bear an informative value' in nest and/or offspring recognition, we performed odour choice tests with breeding zebra finches. In these tests wegavemal es and females the choice between (1) unused coconut fibres and nestmaterial from their own nest, (2) unused coconut fibre and nestmaterial from a conspecific nest containing nestlings of the same age as their brood, and (3) nest material of their own nest and nest material of a conspecific nest, simultaneously (Krause and Caspers 2012). Males as weil as females were tested once during the nestling phase of their offspring and once after the offspring had fledged. Males did not show any preference in all choice situations whereas females preferred the odour of their own nest during the nestling period of their offspring, when given the choice between their own nest and unused coconut fibre. Fernales also avoided the nest odour of a conspecific nest, when given the choice between unused coconut fibre and nest material of a conspecific nest. But females did not show any preference when given both nest odours simultaneously. After the offspring have fiedged, females did not show any preferences. We assume that the behavioural differences are based on motivational differences (Krause and

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27.4

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Triiimich F (1976) Recognition of individual nesting box in budgerigars, Melopsittacus-Undulatus Shaw (Aves, Psittacidae). Z Tierpsychol 42:1-11 Uy JAC, Moyle RG, Filardi CE, Cheviron ZA (2009) Difference in plumage co1or.used in species recognition between incipient species is Iinked to a single amino acidsubstitutein the melanocortin-1 receptor. Am Nat 174:244--254 Waldmann B (1991) Kin recognition in amphibians. In: Hepper PG (ed) Kin recognition. Cambridge University Press, Cambridge Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Künstner A et al (2010) The genome of a songbird. Nature 464:757-762 Whittaker DJ, Soini HA, Atwell JW, Hollars C, Novotny MV, Ketterson ED (2010) Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav Ecol 21:608-614 Whittaker DJ, Richmond KM, Miller AK, Kiley R, Burns CB, Atwell JW, Ketterson ED (2011) Intraspecific preen oil odor preferences in dark-eyed juncos (Junco hyemalis). Behav Ecol 22: 1256--1263 Witte K, Caspers B (2006) Sexual imprinting on a novel blue ornament in zebra finches. Behaviour 143:969-991 Zann RA (1996) The Zebra Finch: a synthesis of field and laboratory studies. UK, Oxford University Press, Oxford Zelano B, Edwards SV (2002) An MHC component to kin recognition and mate choice in birds: predictions, progress, and prospects. Am Nat 160:S225-S237 Zhang JX, Wei W, Zhang JH, Yang WH (2010) Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chem Senses 35:375-382