J. Avian Biol. 40: 481Á490, 2009 doi: 10.1111/j.1600-048X.2008.04682.x # 2009 The Authors. J. Compilation # 2009 J. Avian Biol. Received 7 August 2008, accepted 7 November 2008 Individual distinctiveness in the mobbing call of a cooperative bird, the noisy miner Manorina melanocephala Robert A. W. Kennedy, Christopher S. Evans and Paul G. McDonald R. A. W. Kennedy, C. S. Evans and P. G. McDonald (correspondence), Centre for the Integr. Study of Anim. Behav., Macquarie Univ., Sydney, Australia 2109. Email: [email protected] Individual differentiation is usually advantageous in maximising the fitness benefits of interactions with conspecifics. In social species, where intraspecific interactions are frequent, this is likely to be particularly important. Indeed, some form of differentiation underpins most hypotheses proposed to account for cooperative behaviour in birds. The auditory modality is a likely candidate for this function, particularly for species where individuals are widely spaced and in dense vegetation. In this study, we examined the acoustic structure of a distinctive mobbing signal, the ‘chur’ call, of the cooperatively breeding noisy miner Manorina melanocephala. Using 250 calls from 25 individuals, a combination of spectrographic-based measurement of call parameters, cross-correlation and multi-dimensional scaling was used to test for systematic individual differences in call structure. Strong differences between individuals were observed in all measures, indicating that this call encodes sufficient information to facilitate individual differentiation. We then conducted a series of field playbacks to test the effect of the behaviour on conspecifics. Results demonstrated that the call, in isolation, has a clear attractant effect. Given that chur calls are synonymous with the characteristic cooperative mobbing behaviour of this species, these findings suggest they are likely to have an important function in coordinating complex social behaviour. Individual differences in the vocalisations of territorial, The benefits of signalling identity must outweigh any socially monogamous, birds have been examined for many costs associated with doing so for individuality to be years (Stoddard 1996 for review). These studies have lead to retained and/or developed in a population. The auditory the development of such rich areas of research as the ‘dear modality has the potential to be a relatively low cost method enemy effect’ (e.g. Falls 1982) and the development of of signalling individual identity, particularly in habitats communication network theory (McGregor 2004). How- where visibility may be interrupted (due to dense vegeta- ever, the vocalisations of social species have received tion, for example). Individually distinctive vocal ‘signatures’ comparatively little attention, despite similar putative have characterised many call types across a wide range of benefits of individual recognition. For example, individuals avian taxa (gannets: White et al. 1970, penguins: Jouventin may vary the level of resources and/or aggression expended et al. 1999, skuas: Charrier et al. 2001, gulls: Mathevon during interactions with different individuals. Fully 9% of et al. 2003, passerines: Mammen and Nowicki 1981, Sharp avian taxa breed cooperatively (Cockburn 2003, 2006), that and Hatchwell 2005, McDonald et al. 2007). Differences in is, in systems where individuals apart from the breeding pair acoustic properties have even been used in the field to assist in rearing offspring. Cooperation may also extend to census individuals from species that are difficult to observe other modalities, such as the mobbing of predators. directly (e.g. Puglisi and Adamo 2004). Individual differentiation in these groups is of particular Whether individuals of such species actually attend to interest, because evolutionary models have suggested a range and utilise the individual vocal differences measurable in the of pathways through which direct and indirect benefits may acoustic structure of their calls remains largely unknown. accrue to such helpers. These include kin selection For example, song sparrows Melospiza melodia appear not to (Hamilton 1964), ‘pay to stay’ (Gaston 1978), group use vocal individuality to identify a single singer as such, but augmentation (Woolfenden and Fitzpatrick 1978, Kokko rather to discriminate on the basis of song type (Beecher et al. 2001), and social ‘prestige’ (Zahavi 1977, Wright et al. 1994). Similarly, many studies point to the ability of 1999). In all of these cases, individualised signals, and the songbirds to distinguish among the songs and/or song discrimination of such signals by receivers, are typically repertoires of individuals according to categories, such as either assumed to be present, or at the very least would be mate versus non-mate (Lind et al. 1996), or neighbour/ highly advantageous. Nevertheless, there have been few group member versus stranger (Payne et al. 1988). Other experimental studies of this to date. species have been shown to use calls to distinguish between 481 flock members or social partners, or offspring versus other playback trials aimed at determining the function of this young (Beecher 1981, Beecher et al. 1981, Nowicki 1982, vocalisation. Wanker et al. 1998). Experimental evidence of individual discrimination has been documented in great tits Parus major (Weary and Krebs 1992), however the results obtained Methods varied according to the playback equipment used and were based on a low number of exemplars, leading some Focal populations to question its broad applicability (e.g. Beecher et al. 1994). Better evidence for individual differentiation has been Calls were recorded from 2 different cohorts of noisy miners. The first cohort of birds (n11) were housed obtained through the use of operant conditioning, however individually in a compound of 33 m cages at Macquarie this has been carried out for only a few species (e.g. Brown Univ., New South Wales, 338 46?S, 1518 06?E. Birds were et al. 1988, Sturdy et al. 1999, Phillmore et al. 2002). local residents trapped within 25 m of the cages between 13 Noisy miners Manorina melanocephala are honeyeaters May and 21 June 2007. They were recorded from 20 June (Meliphagidae) endemic to wooded country in southern through 15 August, and released between 14 July and 21 and eastern Australia. Multi-brooded, obligate cooperative Aug. The second cohort were free-living birds located breeders, they form large colonies with complex internal opportunistically at 14 different sites in the surrounding social structures that occupy areas up to 200 ha (Dow 1977, region, visited during the breeding season between 20 July Higgins et al. 2001). Extra-pair fertilizations are typically through 8 Aug 2007. Recording sites were separated by rare (3.5% of nestlings: Po˜ldmaa et al. 1995), with broods 320Á2800 m from the next (mean: 1132 m9572 SD), attended by up to 22 helpers in addition to the breeding maximising the probability that each recording sampled a pair (Dow 1979a). These helpers are invariably from within different individual. Noisy miners are usually found within the colony, usually male, and of variable degrees of individual activity spaces within their colony, for which relatedness to the brood (Po˜ldmaa et al. 1995). mean diameters of 114 m for males and 74 m for females In addition to provisioning nestlings, noisy miners show have been reported (Dow 1979b), that is a third of the another kind of ‘helping’ behaviour. Adult members of a distance between recording sites used herein. As calls were colony work in groups to expel potential food competitors only recorded from birds present from the beginning of a and predators from their territory (Arnold et al. 2005). stimulus presentation, or which arrived within 1 min, it is While doing this they often give a repeated, loud, highly unlikely that birds were recorded at multiple sites. monosyllabic vocalization, henceforth referred to as the Vocalizations were recorded using a Sennheiser MKH ‘chur’ call (Date 1982, Higgins et al. 2001). This call is 816T microphone and a Sony TCD-D10 Pro II DAT generally given by an individual as soon as it perceives a recorder. A second microphone (Yoga FXÁ108) was used to terrestrial or avian predator of little imminent threat to record dictation by the observer (RK) onto the second adults (e.g. an egg thief). Other noisy miners may then join recording channel. Chur calls were elicited by presentation the initial caller in a vociferous ‘chorus’ of chur-calling. of taxidermic models (European fox Vulpes vulpes and While the chur call is predominately used in these mobbing domestic cat Felis cattus), typical contemporary ground contexts, it is also sometimes given in the apparent absence predators in the Sydney region. No apparent differences in of any threat, perhaps as a form of a contact call. Indeed, it behaviours elicited were detected according to model has been suggested that this vocalization leads to the species, nor were the calls of birds exposed to both models gathering of colony members, thus facilitating communal specific to each model type (n4, multivariate test: Wilks’ mobbing (Dow 1977). Such gatherings may also subse- Lambda0.882, F2,31 2.073, P0.143). Until record- quently become intense social interactions, involving a ing began, the models were kept covered in a dark blue range of vocalizations, displays and chases, which are cloth, with no alarm calls given to the model in this state. thought to reflect local dominance hierarchies (Dow The model was placed on the ground 3Á6 m in front of the 1975, Arnold 2000). focal bird (caged or free-living) and vocalizations recorded The apparent function of the chur vocalisation, and the from a distance of 3Á7.5 m. The focal bird was kept group behaviour associated with it, suggests that it may be constantly in view and dictation into one channel used to pivotal in the noisy miner’s complex sociality, and therefore denote calls of the focal bird for later isolation. After a prime candidate for individual distinctiveness. However, a 10 min, if no calls were elicited or the focal bird moved out system of individual recognition based on vocal character- of sight, sessions were terminated.