Behav Ecol Sociobiol DOI 10.

1007/s00265-007-0394-2

ORIGINAL PAPER

A critical analysis of false-feeding behavior in a cooperatively breeding bird: disturbance effects, satiated nestlings or deception?
Paul G. McDonald & Anahita J. N. Kazem & Jonathan Wright

Received: 27 November 2006 / Revised: 28 February 2007 / Accepted: 3 March 2007 # Springer-Verlag 2007

Abstract False feeding, where helpers arrive at nests with food but fail to provision the young, has been reported in several cooperative species. This and other potentially deceptive behavior has been interpreted as indicating that helping may operate as a signal within such social groups. We critically examine these phenomena in the provisioning behavior of the bell miner Manorina melanophrys. Excessively close observation distances can artificially elevate the rate of false feeding in this (and other) species, but once this had been accounted for, there was little evidence for any deceptive behavior by helpers or breeders. Natural and experimentally induced variation in the presence of a potential conspecific audience at the nest did not have any consistent influence upon the rate of false feeds, which was low at 7.94% of 6,880 nest visits. Instead, encountering unexpectedly low levels of brood demand provided a more parsimonious explanation for those visits where helpers failed to feed nestlings or ate the food themselves. Failure to completely transfer a load to nestlings was more likely when
Communicated by R. Gibson P. G. McDonald School of Biological Sciences, University of Wales, Bangor, Gwynedd LL57 2UW, United Kingdom P. G. McDonald Department of Zoology, La Trobe University, Bundoora 3086, Australia A. J. N. Kazem : J. Wright Institute of Biology, NTNU, Trondheim 7491, Norway P. G. McDonald (*) Centre for the Integrative Study of Animal Behaviour, Macquarie University, Sydney 2109, Australia e-mail: paul@galliform.bhs.mq.edu.au

the load contained a high proportion of sticky lerp, indicating a simple prey-transfer problem. Finally, individuals that arrived at nests without prey were often members of neighboring breeding pairs, suggesting that these few nonfeeding visits may instead involve an information-gathering function. We, therefore, suggest that future studies explicitly exclude the possibility of observer disturbance and all aspects of normal provisioning behavior before applying the terms false feeding or deceptive and inferring anything more than straightforward helping at the nest. Keywords Bell miner . White-winged chough . Carrion crow . Helping at the nest . Signaling hypotheses

Introduction Investigation of avian helping at the nest has provided numerous insights into the evolution of cooperation within social groups (see Brown 1987, Emlen 1991, Koenig and Dickinson 2004, and Cockburn 2006 for reviews). The traditional view of helping as an apparently altruistic behavior has been challenged by an increasing number of studies in which helpers have been reported to false feed. That is, helpers appear to gain the benefits of being seen to attend and provision the young without incurring the costs of actually transferring food to others. Such atypical provisioning behavior has been documented in cooperative groups of brown jays (Psilorhinus morio; Lawton and Guindon 1981), bell miners (Manorina melanophrys; Clarke 1984; Poiani 1993), white-throated magpie-jays (Calocitta formosa; Langen 1996), Arabian babblers (Turdoides squamiceps; Wright 1997), laughing kookaburras (Dacelo novaeguineae; Legge 2000), and carrion crows (Corvus c. corone; Canestrari et al. 2004), as well as one

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mammalian species (meerkats, Suricata suricatta; CluttonBrock et al. 2005). However, the most frequently cited example is that of the white-winged chough (Corcorax melanorhamphos; Boland et al. 1997). In this species, young helpers carry food to the nest area, but instead of provisioning the nestlings, they sometimes dip the food into a nestlings bill without releasing it before consuming the prey item themselves. This suggests that these individuals are attempting to minimize the costs associated with providing aid, yet still be identified as a helpful individual within the group. False feeding is more common when individuals are alone at the nest, with only 3 of 89 incidents occurring when another individual was present (Boland et al. 1997). As such, this behavior has been interpreted as a form of deception, sensu Semple and McComb (1996), where a receiver registers a situation that is not in reality occurring, and the signaler benefits while the receiver incurs a cost of this misinformation. Boland et al. (1997) suggest that direct benefits could accrue to deceptive helpers in this system via one of two hypotheses proposed to account for cooperative breeding. The first, the pay-tostay hypothesis, predicts that helping is simply a means of securing group membership and its associated benefits (Gaston 1978; Kokko et al. 2002). Individuals that fail to help sufficiently face aggression from dominant breeders or expulsion from the group (Reyer 1990; Mulder and Langmore 1993). Alternatively, helping effort has been hypothesized to be a reliable signal of individual quality, with individuals of high quality obtaining greater access to matings or beneficial alliances (social prestige; Zahavi 1977, 1995; Wright 1999). Thus, false feeding may allow individuals to retain access to the group, or be perceived as a high-quality individual, without incurring the costs of handing over the food to the nestlings. An alternative explanation for false feeds is simply that helpers base their decision to feed a brood upon the difference between their own and the broods nutritional state (Wright 1997; Canestrari et al. 2004; Clutton-Brock et al. 2005). Individuals that are in relatively poor condition and/or exposed to unexpectedly low brood demand during a provisioning visit may benefit by consuming prey items themselves, rather than feeding them to the nestlings. This hypothesis receives circumstantial support from the fact that it is the younger white-winged chough and breeding female crows that exhibit the highest rates of false feeding in the studies cited above. Younger chough are typically in poorer condition than adults (Boland et al. 1997), and breeding female crows face the greatest burden of all individuals over a breeding season as sole brooders and incubators of several clutches per season (Canestrari et al. 2004). Younger brown jays (Lawton and Guindon 1981) and floater whitethroated magpie-jays (Langen 1996) were also the most likely to make provisioning mistakes, and again, these are

the classes of an individual likely to be the most nutritionally stressed. A critical test of this second hypothesis requires that the begging response of a brood during specific visits is negatively correlated with the propensity that an individual withholds food from the nestlings. Boland et al. (1997) conducted a food supplementation manipulation and inferred reduced nestling hunger as a consequence (based on the number of begging vocalisations between provisioning events); however, the supplementary food was equally likely to have reduced hunger in attendants as well as nestlings. Under this scenario, a helper using a simple provisioning rule of feed nestlings when they seem hungrier than me would show the observed reduction in the frequency of false feeds, thereby, precluding the need for any explanation based on deceptive behavior (Canestrari et al. 2004). Likewise, while Canestrari et al. (2004) found evidence suggestive of this second alternative, neither study quantified the nestling begging levels at the critical moment when provisioners are faced with the decision to provision the young or false feed. Furthermore, under any signaling explanation, the decision to false feed might be expected to depend on prey quality/ size (i.e., the cost to helpers of giving the prey item to the nestlings as opposed to consuming it themselves), or the presence/absence of other individuals in the vicinity. This is not the case if false feeds merely reflect a temporal mismatch between anticipated brood demand and current state of the provisioning individual. Another possibility is that many apparently atypical provisioning behaviors are in fact a by-product of observerinduced disturbance at the nest (Wright 1997, 1999). Despite many of these studies relying upon relatively close observation or filming of cooperative groups at nests, specific statistical tests to detect any effect of observer-generated disturbance upon individual provisioning behaviors are disappointingly rare. Behaviors such as alarm calling and mobbing of observers are obvious, but other more subtle behavioral effects may pass unnoticed. For example, in their observations of Florida scrub-jays (Aphelocoma coerulescens), Stallcup and Woolfenden (1978) describe helper arrival at the nest without food, as well as possessive and prolonged attention around the nest by a helper that even snatched food from the beaks of other visiting adults, and high levels of nest vigilance especially by the breeding pair. Such behaviors are very similar to the behavior exhibited by other species when disturbed by observers present close to nests (Wright 1999). For example, Wright (1997) found that dominant Arabian babblers devoted more time to remaining in the nest area at the expense of foraging and provisioning activities when observers sat too close to nests. Further, Lawton and Guindon (1981) report that observers were sometimes mobbed by younger nest attendants during observations the very class of helper that displayed the highest rate of false

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feeds in their study. Observer-associated disturbance, therefore, seems one of the most likely causes of many aberrant behaviors at the nest, especially given that both the Arabian babbler and the Florida scrub-jay populations were habituated to humans through hand feeding and the observations carried out by unconcealed observers sitting very close to nests (Wright 1999). In this paper, we present a critical analysis of false feeding and other potentially deceptive provisioning behaviors in the bell miner, a species in which false feeds have been described previously (Clarke 1984; Poiani 1993). Bell miners form large colonies that contain a number of coteries, each of which consists of a number of breeding pairs and an attending assemblage of non-breeding helpers that are mostly male, and provision at multiple nests within their coterie (Clarke 1989). While some helpers are related to the breeding pair they assist, many are not (Conrad et al. 1998; Painter et al. 2000; e.g., 52% of helpers in this study). Circumstantial evidence points to a signaling explanation for helping in bell miners. For example, Clarke (1989) has documented five instances in which breeding males died or disappeared, and on each occasion, the widowed female subsequently paired with the unrelated male helper that had provided the greatest assistance in raising her previous brood. A subsequent study entailing experimental removal of breeding males revealed similar patterns of mate choice by widowed females (Jones 1998). This suggests that one of the benefits for non-kin helpers may be in showing off to the female and enhancing their chances of gaining future breeding opportunities (cf. social prestige). Unusually, bell miners also produce individually identifiable mew vocalisations during provisioning and when they leave the nest area (McDonald et al. 2007), meaning that individuals visits (and, therefore, potentially helping effort) may be more easily monitored by conspecifics than in many species. Therefore, bell miners would appear one of the cooperative systems most likely to involve helping as a signal and, thus, also greater potential for deceptive provisioning behavior and false feeding at the nest. We tested for this by conducting detailed observation of individual provisioning behavior on a visitby-visit basis, in conjunction with recording levels of nestling begging, as well as both natural and experimentally induced variation in the presence of any potential audience (e.g., the breeding male or female) near the nest.

individuals at the La Trobe University Wildlife Reserve, 20 km northeast of Melbourne, Australia (3742S, 14502E). The second was near Saint Andrews, 50 km northeast of Melbourne (3743S, 14503E), and contained 120135 birds. Molecular analyses Individuals within colonies were color banded, and a 70-l blood sample was collected from the alar vein for analysis. This sample was stored in 70% ethanol and then transported to the Australian National University, Canberra, Australia, where birds were sexed and six-loci genotyped according to the protocols outlined in Fridolfsson and Ellegren (1999) and Painter et al. (1997), respectively. Birds were then classed as either a breeding female or breeding male (mean pairwise relatedness r between breeding pairs 0.1520.059 SE, n =23 pairs), with helpers being classified into one of six groups according to their sex and relatedness to the breeding female. Relatedness was assessed using Kinship v1.2 (Goodnight and Queller 1999), which calculated the likelihood of helpers being either related (primary hypothesis, r =0.5; null hypothesis, r =0), or unrelated (primary hypothesis r =0, null hypothesis of r =0.5). We calculated the ratios of likelihoods between primary and null hypotheses based on the ratio required to exclude 95% of 1,000 simulated pairwise comparisons (Goodnight and Queller 1999). Based on the tests above, helpers were determined to be either related (males, r =0.4240.031 SE, n =23; females, r =0.530 0.041 SE, n =13), unrelated (males, r = 0.0680.020 SE, n =103; females, r = 0.1720.052 SE, n =17) or, if neither significantly related nor unrelated, as unresolved (males, r =0.2160.024 SE, n =46; females, r =0.1640.059 SE, n =8). Values of r can range between 1 and +1 in Kinship, with negative values indicating individuals that share fewer alleles than average for the population (Queller and Goodnight 1989). Theoretically, in a randomly mating population, r should approximate 0.5 for full siblings and 0.25 for half-sibs and so on (Queller and Goodnight 1989). Therefore, the estimated r values for our different classes of helpers are reassuringly close to those expected. For simplicity, all results are presented using relatedness calculated relative to the breeding female; the results did not differ if relatedness groups were assigned relative to either (1) breeding males or (2) the mean of the breeding pair (results not presented). Monitoring of nesting attempts

Materials and methods Study sites The study was conducted between June 2004 and December 2005 on two bell miner colonies. The first consisted of 4045 Once found, nest contents were monitored every second day to determine the hatching date. Only one female participated in nest construction, incubation, and brooding, thereby, allowing the breeding female to be identified for each nest. To identify breeding males (genetic data were

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unavailable at the start of the nestling period), the nests were observed for 2 h within 48 h of nestlings hatching, and the male that fed the most during this period was assigned as the putative breeding male, as helpers rarely feed during this early period (Poiani 1993). Furthermore, breeding male home ranges overlap considerably with those of breeding females in this species (Clarke and Fitz-Gerald 1994), a situation observed in all assigned putative pairs in this study. Recording of provisioning behaviors Nests were observed for a minimum of 2 h each day (mean, 1797.6 SE min; range, 24 h) from the time nestlings were 6 days old (with day 0 as the day of hatching) through to fledging (either day 10 or 11). The nests were watched from a hide using a Kowa TS662 spotting scope with a 2060 zoom eyepiece (Tokyo, Japan) and also videoed using either an analogue (CCD-TR1100E, Sony, Tokyo, Japan) or digital Hi8 camcorder (DCR-TRY265E) placed on a tripod. Timestamped videos were later burnt onto DVDs using a DVD recorder (Pioneer DVR-310, Tokyo, Japan) and reviewed using Power DVD v4.0 (LG Electronics) on a laptop computer (Higrade Notino C7000, Essex, United Kingdom). Acoustic begging levels were recorded with a small tieclip microphone (Sony ECM77B, Sony) placed 20 cm below each nest. This microphone was connected to a Marantz PMD670 solid state recorder (Tokyo, Japan), with calls recorded at 48 kHz in uncompressed PCM format as wav files with the record level set to 7. These files were subsequently loaded into Raven 1.2.1 (Cornell, USA), and spectrograms constructed with a 512-point fast Fourier transform length (3 dB bandwidth, 124 Hz, with the smoothing function enabled) with a Hanning window function and overlap set at 90% (grid resolution 1.16 mS, grid spacing 86.1 Hz). Calls were then high-pass filtered to remove the background noise at frequencies lower than the begging vocalizations. The amplitude of the first bout of begging produced by nestlings after the arrival of an individual at the nest was then measured using the rootmean-square algorithm within Raven (Charif et al. 2004). A visual score of begging intensity based on nestling posture was also noted according to the following scale, where head orientation is measured in degrees from 0 (horizontal) to 90 (vertical plane): 1=no discernible response; 2=head lift less than 45; 3=head lift greater than 45, but nestlings remain on tarsi; 4=head lift 90 and nestlings stand. Other data recorded during the provisioning events included the duration of nest visits, prey type (lerp or invertebrate) and size relative to the attendants bill volume, distance travelled when leaving the nest area, and the number of mew calls given while feeding nestlings and when leaving the nest area (P. G. McDonald, A. J. N.

Kazem, L. te Marvelde, and J. Wright, unpublished data). Results did not differ if the total number of mew calls given was used, or if calls given while at or leaving the nest area were analysed separately. For simplicity we, therefore, used the number of mew calls given as birds left the nest area, as this component seems more likely to be vulnerable to disturbance effects or involved in any signaling of helping effort (rather than stimulation of begging). Lerp is a white sugary secretion produced by sap-sucking psyllids (Hemiptera; Psyllidae), a staple of adult miners commonly also fed to nestlings. Finally, the identity of all other birds at the nest (within 2 m of the nest cup) while the focal individual was present was recorded. The dense vegetation around most nests meant that, although a larger radius was monitored, we could not be sure that we had recorded every conspecific present on every occasion; by the same token, though, birds present at these greater distances themselves would not necessarily be able to monitor each others behavior at the nest. Assessment of disturbance by observers Initially, for four nests, we compared the provisioning behavior of birds when the observation hide was placed at 3 versus 10 m from the nests, without audiovisual equipment, counterbalancing the order of presentation. Notably, when hides were placed 3 m from the nests, the birds displayed obvious and marked agitation and disturbance behavior; for example, large numbers of alarm calls were given by both breeders and helpers. Breeding females especially stayed within close proximity of nests, rarely foraging for food. Visit rates were comparatively lower at the closer distance, with an extra 2.75 visits/h4.50 SE detected when the observer distance was 10 m compared to 3 m from the nests. More importantly, in this short observation period, an average of 1.250.63 SE additional helpers were detected when the observers were positioned further from the nests, regardless of the order of observation distance treatment. It is worth noting that some of the behaviors we observed at the closest distance of 3 m were very similar to the sentinel-like behavior and nest vigilance reported in other studies, where nests had been monitored (often at distances closer than this) by unconcealed observers (see Wright 1997, 1999). Given this clear disturbance effect, further hide watches at 3 m were abandoned, and a series of 14 subsequent nests were monitored using consecutive 2-h observations from either a near (hide, 10.5 m0.6 SE; camera, 1 m from the nest) or far position (hide, 17.9 m0.6 SE; camera, 3 m from the nest). The order of the near and far observations was counterbalanced so that seven replicates of each order were collected with the observer and equipment in the near and far positions, respectively, at nestling ages of between 6 and 8 days (mean 6.210.15 SE).

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In all cases, observations did not commence until 10 min had elapsed after the observer entered the hide to allow any disturbance associated with observer presence outside the hide to dissipate. In most cases (i.e., with hides 10 m from the nest), the birds resumed apparently normal provisioning within 23 min of an observer entering the hide, well before data recording began. There was no subsequent systematic change in any provisioning behavior over the course of the observation period (results not shown for reasons of brevity). This indicates that there were no adverse disturbance effects upon the birds due to the way in which observation sessions were initiated. Temporary removal experiments As part of a separate experiment (McDonald et al., unpublished data), either the breeding male or breeding female was removed for a period of 4 h when nestlings were at least 6 days old (male removals mean nestling age, 7.7 days0.26 SE, n =10; female removals, 7.7 days 0.4 SE, n =10). Nests were initially monitored in the manner described above, with observers 15.9 m0.8 SE (n =20) from the nest and camera equipment at 3 m, for a 2-h period (pre-control observation). Mist nets were then erected around the nest area and the randomly predetermined focal bird (either breeding female or breeding male) captured. The removed birds were placed in a sheltered cage, out of visual and acoustic contact with the rest of the colony, with sugar water available ad libitum. Mist nets were then removed and the nest left for at least 40 min to minimize any effects of disturbance before resumption of observations. Nest visit data were then collected for all birds during the subsequent 2-h removal observation period. A further 1-h playback observation period was then conducted (with the removed bird still absent). As visiting individuals arrived in the nest area, one mew call from the removed bird was played at natural volume from a Sony D-EJ100 player through a speaker (Sony RS-A27) located 4 m from the nest. This playback was intended to simulate the removed bird being in the vicinity of the nest area but out of visual contact, i.e., an experimental period with this audience potentially presentin contrast to the complete removal period. Over the hour, responses to the playback (measured in terms of degree of head movement towards the speaker) did not diminish in the remaining individuals, indicating that habituation was not occurring over this period (data not presented). The order of playback and removal observations was counterbalanced, so equal numbers of nests received removal then playback treatments and vice versa. Testing explicitly for order effects did not yield significant differences in any of the variables measured (McDonald et al., unpublished data). The nestling hunger levels indexed by

their begging levels did not rise significantly during the removal period (McDonald et al., unpublished data). After the completion of these observation periods, the removed individual was released within 50 m of the nest in a soft manner: The cage door was opened remotely from a distance of 10 m, and the bird was allowed to venture from the cage in its own time. All removed individuals went back to regularly provisioning the nestlings within a few minutes. To allow for any possible disturbance after the release of the removed individual, a final 2-h post-control observation began at least 40 min after its release. Statistical analyses As visual and acoustic begging measures were correlated (Pearson coefficient, r = 0.448, p < 0.005), we used a principal components analysis (PCA) to generate a composite measure of both these indices of begging intensity. The first component (PC1), hereafter begging effort, explained 72.4% of the overall variation in both measures of begging and was the only component with a eigenvalue greater than 1 (eigenvalue=1.448). Larger values of PC1 begging effort represent louder and more intense begging by nestlings. Due to occasional equipment failure, in a small minority of visits, either the visual or the acoustic begging measure was not recorded (1.7 and 6.9% of visits, respectively). Estimates of these missing values were generated by fitting linear regressions to the known dataset and calculating the missing values from the formulae obtained (visual begging score=0.0017acoustic amplitude; acoustic amplitude=331.63visual begging score), an unbiased method that enabled these visits to be included in subsequent PCA analysis. Repeated measures analysis of variance (RM-ANOVAs), or a combination of KruskalWallis and Wilcoxon signed rank tests (where data were not normally distributed), were used to examine changes in provisioning behavior according to hide placement distance, as well as variables such as the level of begging associated with typical versus false feeds by the same provisioner at a given nest (withinsubjects effect). Relatedness status (breeding female, breeding male, or one of the helper categories) was included in all models as a between-subjects factor. Helmert contrasts were also used to determine the significance of differences between specific relatedness classes within RMANOVA models (with only significant contrasts being presented for reasons of brevity). These involved a series of orthogonal contrasts comparing values for breeding females against the mean for all remaining status classes, breeding males against the mean for all helpers, then unrelated male helpers against the mean for all other classes of helper, and so on (with remaining classes of helper being assessed in the following order: unresolved male helpers,

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related male helpers, unrelated female helpers, unresolved female helpers, and related female helpers). Given the low numbers of some classes of female helpers in some analyses, tests were repeated including only male helpers to confirm the generality of conclusions. Differential begging effort was calculated by subtracting the begging effort experienced during an individuals previous visit from the begging effort during the current visit; thus, negative values indicate a reduction in begging effort between successive visits. Variables describing visit rates and the proportion of lerp in loads were normalized, using log and arcsine square root transformations, respectively. All analyses were carried out using the Statistical Package for the Social Sciences (SPSS) v12.0.2. All tests were twotailed and a critical p value of 0.05 applied throughout, unless subject to Bonferroni correction where indicated.

Results Quantifying disturbance effects Given the clear disturbance effect initially observed at 3 m, a series of 14 subsequent nests were monitored with hides placed 10 m (near) and 20 m (far) from nest sites, with electronic monitoring equipment at 1 and 3 m, respectively. We can confirm that none of the measures of provisioning behavior differed significantly between observations at distances of 10 versus 20 m and, despite biologically meaningful differences in some behaviors according to relatedness status within the group (McDonald et al., unpublished data), there was no significant interaction between the observation distance and the relatedness status (Tables 1 and 2). Frequency and type of false feeds observed Using only observations conducted at distances of 10 m, a total of 6,880 visits to the nest by 118 known individuals were observed during 185.6 h of observation, including 62 observation periods spread over 23 different nesting attempts. All of these visits were by birds of breeding age (greater than 8 months; Clarke and Heathcote 1990), with the exception of six individuals aged between 3 and 5 months. Helping in this species can begin as soon as 3 months after hatching. Exclusion of these young birds from the dataset did not influence any of the results reported in this paper, indicating that age and/or previous provisioning experience had little influence upon false feeding rates in this species. Of these visits, 6,334 (92.06%) were full transfers of the load brought to the nest, representing normal provisioning behavior during the vast majority of nest visits. Of the

remaining atypical feeds (n =546, 7.94%), three distinct forms of false-feeding were evident. On 225 occasions (3.27%), the visiting birds arrived with prey but failed to give it to the nestlings; in 126 (1.83%), the visiting birds failed to transfer their complete load to the nestlings; and during 195 visits (2.83%), the birds arrived at the nest area without any discernible prey at all (Table 3). Birds failing to transfer the full amount of their load either ate the remaining prey themselves at the nest cup, or took it with them upon leaving the nest area. The birds failing to transfer prey fully usually gave several mew calls from the nest cup, vocalisations known to stimulate begging (McDonald et al. 2007), with some also placing the prey inside nestlings bills without releasing the item before leaving the nest area. Few obvious patterns emerged when comparing the rate of occurrence of these different types of false feed according to the individuals relatedness status within the group (Table 3). Below, we conduct a more detailed examination of factors that might explain why these different types of false feed occur. Visits where provisioners failed to transfer prey at all Individuals bringing prey to nests were significantly less likely to feed nestlings when they experienced a reduction
Table 1 Tests for variation in provisioning behaviors according to observer distance RM-ANOVA tests Nest visit rate per hour Load size Factor Obs distance Status Dist status Obs distance Status Dist status Obs distance Status Dist Status Obs distance Status Dist status Obs distance Status Dist status Obs distance Status Dist Status F ratio 3.140 8.869 0.234 2.580 4.438 0.698 0.920 0.705 1.440 0.284 2.132 0.641 0.357 10.631 1.228 1.213 1.337 1.943 df 1.120 7.120 7.120 1.83 7.83 7.83 1.83 7.83 7.83 1.86 7.86 7.86 1.86 7.86 7.86 1.77 7.77 7.77 p value 0.079 <0.001 0.976 0.112 <0.001 0.673 0.340 0.668 0.201 0.596 0.049 0.721 0.552 <0.001 0.296 0.274 0.245 0.074

Proportion of lerp in load Number of mew calls given as leave nest area Duration of nest visit Proportion of exit flights>10 m

Results are presented for a single RM-ANOVA model with significant effects after Bonferroni correction (critical, =0.006) shown in bold. Obs distance Distance from which the observation was undertaken from the nest: near (10 m) versus far (20 m); Status relatedness status of the bird within the group; see Materials and methods for details; Diststatus interaction term between observation distance and relatedness status in the models

Behav Ecol Sociobiol Table 2 Tests for variation in provisioning behaviors according to observer distance Non-parametric tests Proportion of visits with no prey Factor Obs distance Status Dist status Obs distance Status Dist status Obs distance Status Dist status Test statistic Z = 1.869 2 =12.708 2 =6.840 Z = 0.894 2 =12.908 2 =3.782 Z = 1.019 2 =2.807 2 =2.656 df 7 7 7 7 7 7 p value 0.062 0.080 0.446 0.372 0.074 0.804 0.308 0.902 0.915

Proportion of visits prey not given

Proportion of visits with partial feed

Results are presented for three separate tests using KruskalWallis (2 ) and Wilcoxon signed rank tests (Z), with significant effects after Bonferroni correction (critical, =0.006) shown in bold. Obs distance Distance from which the observation was undertaken from the nest: near (10 m) versus far (20 m); Status relatedness status of the bird within the group; see Materials and methods for details; Dist status interaction term between observation distance and relatedness status in the models

in begging effort relative to levels during their previous visit (Table 4, Fig. 1a). There was no significant effect of relatedness status, nor any interaction between relatedness status and change in begging effort experienced (Table 4). Thus, birds consumed the food themselves when faced with an unexpectedly satiated brood. Load size and the proportion of lerp in the load did not differ significantly between visits in which an individual fed nestlings or withheld the entire load (Table 4). The probability of retaining the food also did not differ between provisioning visits when the individual was feeding as a breeder at their own nest versus acting as a helper at the nest of another coterie member (Table 4). Interestingly, when failing to transfer any of their prey load to nestlings, individuals produced significantly more mew calls than when they had fed nestlings (Table 4, Fig. 1b). Birds more often withheld the whole prey load when a larger number of individuals were present near the nest; however, this difference was not significant (p =0.051; Table 4). By increasing the probability that failing to

provision is witnessed by others, both of these results appear contrary to the predictions from any signaling hypothesis and, perhaps, reflect the effects of having to queue to provision the brood or subsequent involvement in alternative cooperative activities with other coterie members away from the nest, such as the mobbing of potential predators. Visits where loads were not fully transferred Visits where birds did not transfer the whole load to nestlings were characterised by a greater proportion of lerp in the prey load (p =0.015, Table 4, incomplete load transfer; Fig. 2), although this was not significant after Bonferroni correction (critical, =0.008). Lerp is a relatively sticky item that often became stuck on the mandibles of birds, leading to bill wiping and cleaning with the tongue (McDonald, personal observation). There was no significant influence of relatedness status or an interaction between this and the proportion of lerp in the load (Table 4).

Table 3 Frequencies of different types of false feed according to relatedness status Type of false feed Relatedness status B Number of nest visits Nest visits with no prey Nest visits where prey was not given Nest visits with only partial feed Total false feeds 1,677 27 (1.61) 11 (0.66) 16 (0.95) 54 (3.22) B 1,166 3 (0.26) 21 (1.80) 26 (2.23) 50 (4.29) Unrel 1,684 103 (6.12) 95 (5.64) 49 (2.91) 247 (14.67) ? 1,154 36 (3.12) 51 (4.42) 22 (1.91) 109 (9.45) Rel 483 6 (1.24) 17 (3.52) 6 (1.24) 29 (6.00) Unrel 179 6 (3.35) 7 (3.91) 3 (1.68) 16 (8.94) ? 189 0 (0) 2 (1.06) 1 (0.53) 3 (1.59) Rel 348 14 (4.02) 21 (6.03) 3 (0.86) 38 (10.92)

The values represent the frequency of occurrence, with percentages in parentheses. Relatedness status Either the breeding female (B), breeding male (B), or for either male or female helpers, individuals that were significantly unrelated (Unrel/), unresolved (?/), or related (Rel/) to the breeding female (see Materials and methods for details).

Behav Ecol Sociobiol Table 4 Results of RM-ANOVAs assessing within-individual changes in mean levels of different aspects of provisioning, for typical feeding visits versus atypical visits where birds failed to transfer any of their load to nestlings or only partially transferred the load Variable Factor Load withheld F ratio Change in begging experienced during current versus previous nest visit Load size Begging change Statusa Beg status Load Status Load status Lerp Status Lerp status Calls Status Calls status No. of others Status Others status Own nest Sex of breederb Nest sex 45.469 0.801 1.130 0.005 1.652 0.339 3.385 0.793 1.366 9.699 1.699 0.333 3.897 1.114 0.889 2.111 0.216 0.022 df 1.77 7.77 7.77 1.95 7.95 7.95 1.90 7.90 7.90 1.95 7.95 7.95 1.95 7.95 7.95 1.15 1.15 1.15 p value <0.001 0.589 0.353 0.944 0.130 0.934 0.069 0.595 0.230 0.002 0.118 0.937 0.051 0.361 0.519 0.167 0.648 0.884 Incomplete load transfer F ratio 0.114 0.953 1.546 0.168 1.894 1.066 6.326 2.213 1.310 0.000 5.487 2.407 0.234 0.488 0.649 0.423 4.811 0.423 df 1.53 7.53 7.53 1.60 7.60 7.60 1.60 7.60 7.60 1.60 7.60 7.60 1.60 7.60 7.60 1.15 1.15 1.15 p value 0.737 0.474 0.172 0.683 0.086 0.396 0.015 0.045 0.261 0.983 <0.001 0.031 0.630 0.840 0.714 0.525 0.044 0.525

Proportion of lerp in load

Number of mew calls given as leave nest area

Number of other individuals near the nest during feed Provisioning at own nest versus nest of another breeding individual

Significant results after Bonferroni correction (critical, =0.008) are shown in bold. See Table 1 for details. b Status was replaced with a comparison between the sexes (Sex) in this test.
a

Visits ending in an incomplete feed did not differ significantly in terms of the change in begging effort experienced (relative to the individuals preceding visit) in comparison with visits involving more typical prey transfer. The occurrence of incomplete transfers also did not differ among provisioners according to their relatedness status or an interaction between relatedness and begging level (Table 4, incomplete load transfer). Likewise, there were no significant differences or interactions between visits with normal versus partial prey transfers in load size, the number of mew calls produced, the number of other individuals present in the nest area, or whether a breeding individual was feeding at its own nest or the nest of another coterie member (Table 4). A relatedness status effect was also apparent on the number of mew calls given as the birds left the nest area; however, this between-subjects effect was independent of whether or not attendants had transferred prey completely (Table 4). Nest visits with no prey The level of begging an individual experienced in the visit before its arrival without prey was not significantly different from that in visits where prey items where brought to the nest (Table 5). The number of mew calls individuals gave as they left the nest area also did not differ according

to whether or not they had arrived at the nest with prey (Table 5). Breeders accounted for a lower amount (15.38%) of all arrivals without prey than helpers, which is not unexpected given the high number of helpers in this system relative to only two members of the breeding pair. However, whether breeding individuals were at their own or another nest significantly influenced the probability of arriving without prey (F1,14 =7.635, p =0.014; Table 5). Breeding individuals were much more likely to arrive without prey when visiting another pair s nest rather than their own nest (Fig. 3). The lack of any effect of sex or an interaction suggests that both sexes of breeder made these non-feeding visits to inspect the nests of other coterie members, although breeding females did so more often than males, accounting for 13.85% compared to 1.54% of all empty visits, respectively. Given that brood demand influenced other provisioning behavior (see above), it is likely that non-breeding attendants were also simply investigating the brood during such visits, perhaps, to adjust their provisioning effort at that specific nest. Effect of bystanders upon provisioning behavior The presence or absence of a potential audience in the form of the breeding female, male, or other helpers had no effect

Behav Ecol Sociobiol

Fig. 1 Mean (SE) difference between nest visits where birds ate the load themselves versus fed it to the brood in a mean change in begging experienced during the previous versus the current visit and b number of mew calls given as birds left the nest area (see Table 3a)

on the probability that individuals would arrive at the nest without prey (Table 6). Indeed, the presence of another helper did not influence any of the three reported falsefeeding rates. However, breeding female presence led to significant differences in the likelihood the full prey load wasnt transferred, or was only partially transferred, during a visit (Table 6). Relative to the predictions of the deception hypothesis, these two results were in inconsistent directions and comparatively small, with fewer partial transfers of prey items, when females were present (1.73%0.70 SE, n =169; versus 3.01%0.65 SE, n =225 when absent), but more visits where the load was not transferred at all when females were present (9.67%1.58 SE, n =169) rather than absent (8.28%1.41 SE, n =225). Finally, breeding male presence resulted in significantly fewer visits where prey loads were not transferred to nestlings (5.61% 1.48 SE, n =148; versus 8.39%1.24 SE, n =231 when absent), in the direction predicted by the deception hypothesis. To clarify these results, we also analysed the influence of temporary experimental removal of either the breeding

female or breeding male upon false-feeding rates (Table 7). No differences in provisioning behavior were detected between pre- and post-control observations; thus, a mean value for the combined control period was obtained and compared with false-feeding behavior during the removal and playback periods. Neither visits where partial prey loads where transferred nor those where individuals arrived without prey were influenced by the experimental removal of either member of the breeding pair, during either breeder removal or experimental simulation of their presence (playback observations; Table 7). In contrast, both removal and playback periods had a significant influence on the probability that prey loads brought were withheld from nestlings during breeding female removals (Table 7). Contrary to the deception hypothesis, prey loads were withheld in more visits during control periods than in removal periods (8.40%2.05 SE, n =80; cf. 1.78%1.41 SE, n =71, respectively). However, the opposite was found during playback periods when breeder female presence was simulated, with the rate of false feeding being lower than in the control periods at 3.06%1.92 SE (n =60). During breeding male removals, there was no difference between the control and the removal, or playback periods on the proportion of visits where prey were withheld (Table 7). Neither relatedness status nor interaction effects between treatment and relatedness status were observed in any of the tests presented in Tables 6 and 7 (results not presented for brevity). Thus, while one result in the direction predicted by deception hypotheses was found, most results were either nonsignificant or in the opposite direction to that predicted a priori, suggesting that bell miners did not take account of whether they were potentially witnessed by another bird during false-feeding visits.

Fig. 2 Mean (SE) difference in percentage of lerp in load between nest visits where birds withheld the entire prey load versus fed the whole load to the brood (see Table 4b)

Behav Ecol Sociobiol Table 5 Results of RM-ANOVAs assessing within-individual changes in provisioning during normal feeding visits versus visits where birds arrived at the nest area without prey Variable Begging during previous nest visit Factor Begging Statusa Beg status Calls Status Call status Nest type Sex of breederb Nest Sex F ratio 0.345 2.434 1.011 0.182 1.504 0.531 7.635 2.039 1.940 df 1.34 6.34 6.34 1.48 6.48 6.48 1.15 1.15 1.15 p value 0.561 0.046 0.435 0.671 0.197 0.782 0.014 0.174 0.184

Number of mew calls given as leave nest area

Provisioning at own nest versus nest of another individual

Significant results after Bonferroni correction (critical, =0.017) are shown in bold. See Table 1 for details. b See Table 3 for details.
a

Discussion Bell miners produce small nest cups concealed in relatively dense understorey vegetation, and if helping effort were being used as a signal, they might be expected to display relatively higher rates of cheating by false feeding than those in species with more open nests, such as the whitewinged chough. However, we observed false feeding during only 7.94% of visits, a slightly lower rate than reported in other studies, of both this species (14%, Clarke 1984) and others (chough, 11%; Boland et al. 1997; crows, 16%; Canestrari et al. 2004). Three distinct forms of false feeding were observed: birds arriving at the nest area without food, birds arriving with food but failing to feed the brood, and finally, nest visits in which not all the load was completely transferred. We suggest that, in this and other studies, these behaviors may simply reflect normal provi-

sioning behavior, being the result of observer-induced disturbance, information gathering, or temporal mismatches in perceived brood demand. Observer-induced disturbance effects We observed obvious effects of disturbance when hides were placed within 3 m of bell miner nests, a distance used in previous studies of this species (Clarke 1984; Poiani 1993). The effects included an increase in false-feeding behavior, but also ranged from obvious and easily detectable alarm calls through to subtle behavioral changes that would have been impossible to detect without explicit study, such as the absence of certain helpers. These results highlight the importance of explicitly testing for disturbance effects whenever monitoring nest sites, especially in complex cooperative groups, where changes in nest attendance and behavior may be subtle. This is especially critical given that the behaviors typical of disturbance that we have observed in this and other species (e.g., Wright 1997) are very similar to those that have previously been interpreted as additional nest guarding behavior, parental training of young, or competition for being seen to feed at nests (Wright 1999). Correctly interpreting provisioning behavior requires specific tests for possible observerinduced disturbance in the species concerned, as the minimum distance observers and equipment need to be from nests to avoid disturbance effects that are likely to vary from species to species. This is particularly important if researchers are examining subtle changes in social behavior associated with hypotheses such as helping as a signal. However, while higher rates of false feeding were induced by observer disturbance, once disturbance was eliminated, the behavior persisted, indicating that disturbance was not the sole factor causing false feeding in bell miners.

Fig. 3 Percentage (SE) of visits where breeding individuals arrived without any prey at their own versus the nest of another individual (see Table 5)

Behav Ecol Sociobiol Table 6 Changes in the rate of different types of false-feeding event according to the presence/absence of other birds at the nest, using Wilcoxon signed rank tests Observational data Breeding female presence Z Proportion of visits with no prey Proportion of visits where prey was not given Proportion of visits with only partial transfer 1.185 2.509 2.436 p value 0.236 0.012 0.015 Breeding male presence Z 1.385 2.780 1.626 p 0.166 0.005 0.104 Helper presence Z 0.713 1.456 1.693 p value 0.476 0.145 0.090

Significant results after Bonferroni correction (critical, =0.017) are shown in bold.

False-feeding as deception If false feeding was a form of cheating (reduction in care), or even deception (i.e., an attempt to disguise that reduction in care), we would perhaps expect individuals to perform the behavior most commonly when alone in the nest area. However, we found only small and inconsistent influences of the presence or absence of a potential audience, namely, the breeding female, breeding male, or other helper, upon the rates of any type of false feeding. Under signaling hypotheses, where individuals might be expected to benefit from cheating or deception, helpers of differing relatedness would also be expected to differ in their rate of false feeding. For example, unrelated helpers obtain no kinselected benefits from helping, but could well benefit from using effort as a signal to impress the breeding female (social prestige) or to placate the breeding male (pay-tostay). Thus, helpers unrelated to the brood may be expected to false feed in a greater proportion of visits than related helpers and certainly more often than either member of the breeding pair. However, in the present study, none of the three types of false-feeding behavior were influenced by the relatedness status of the provisioner, regardless of whether this was calculated relative to the breeding female (as presented), the breeding male, or using mean relatedness to both. These results cast serious doubt upon the

interpretation of false-feeding behavior as a form of deception, at least in this species. In addition, punishment might have been expected to prevent cheating (under pay-to-stay) or conveying of a false impression (under social prestige). However, overt aggression was very rare and observed only once from a breeding female toward a male helper who had arrived in the nest area without food. False feeds were just as common in the presence of a bystander as when individuals were alone. Indeed, individuals gave significantly more mew calls after visits where they failed to feed nestlings, the opposite response to that predicted if punishment follows other coterie members becoming aware of this behavior. In general, all forms of aggression between provisioning individuals in the nest area are extremely rare in bell miners (<1% of nest visits; McDonald et al., unpublished data; 1.1%, Poiani 1993) and carrion crows (1.8%, Canestrari et al. 2004) as is any punishment in systems where false feeding has been studied in detail (3.1% of false feeds, Canestrari et al. 2004; n =3 events, Boland et al. 1997). This might be because false feeding is only witnessed on a low proportion of occasions; for example, in white-winged chough, the culprit was later harassed on all three occasions that a false feed took place when a second individual had been present at the nest. In any case, given our results, such an explanation cannot apply in bell miners.

Table 7 Changes in the rate of different types of false feeding event according to the presence/absence of other birds at the nest, using Wilcoxon signed rank tests Experimental removal dataa Comparison Breeding female removals Z Proportion of visits with no prey Proportion of visits where prey was not given Proportion of visits with only partial transfer
a

Breeding male removals Z 1.647 0.445 2.062 0.650 1.947 1.651 p value 0.100 0.657 0.039 0.516 0.052 0.099

p 0.307 0.532 0.001 0.004 0.287 0.387

Control Control Control Control Control Control

versus versus versus versus versus versus

removal playback removal playback removal playback

1.023 0.625 3.442 2.869 1.066 0.865

Involves comparison of control periods against both simple removal periods and removal periods with mew call playback to simulate the presence of an unseen bystandersee Materials and methods for details. Female helpers were excluded from this set of analyses due to extremely low representation within the sample. Significant results after Bonferroni correction (critical, =0.008) are shown in bold.

Behav Ecol Sociobiol

The evidence for deceptive behavior driving false feeding in this and other avian systems is, therefore, weak (Legge 2000; Canestrari et al. 2004; Clutton-Brock et al. 2005). Indeed evidence of other forms of atypical provisioning, for example, individuals competing with each other to provision nestlings, have also proved difficult to replicate (e.g., Carlisle and Zahavi 1986; Wright 1997, 1998). As such, relatively rare snatching of prey items (e.g., n =6 in Piper 1994) may simply reflect normal interactions involved in maintaining dominance between helpers, as opposed to competition for any prestige associated with provisioning behavior. Some differences in false feeding according to individual status within the group have been found in previous studies, with breeding female carrion crows being more likely to arrive at nests without prey (Canestrari et al. 2004). However, these females often then perform nest-cleaning activities during such visits, an important aspect of nestling care for which they are solely responsible. It, therefore, seems that these visits have little to do with provisioning and are not, in fact, false feeds. A similar result was found in the present study where individuals arriving at the nest area without prey were more often breeding birds from other areas of the colony. Given that nests within a coterie share the same set of helpers in this social system (Clarke 1989; Clarke and Fitz-Gerald 1994; McDonald et al., unpublished data; L. te Marvelde, P. G. McDonald, A. J. N. Kazem, and J. Wright, unpublished data), these neighboring breeders may well have been assessing the workload of their helper contingent and timing their own breeding to maximize helper availability. Similarly, non-breeding individuals that arrive without prey are likely to have been assessing the relative state of different broods they provision, or indeed be part of the breeding population that did not engage in a reproductive event during this study. It is also possible that some visits classified as without food involved individuals carrying extremely small prey items or nectar. However, on many of these occasions individuals arrived with open bills (as they were panting due to high temperatures), vocalized or preened themselves or the nestlings, without being observed to drop or swallow prey beforehand. As such, we are confident that this possibility was not a significant influence in the analyses presented in this paper. We were able to observe birds at the nest in great detail, both via telescope in the field and later in a frame-by-frame video review. We, therefore, believe that birds that arrive at the nest without food in this and at least one other study (Canestrari et al. 2004) can more appropriately be termed non-feeding visits aimed at examining brood demand/age. False-feeding and the role of brood demand Two other forms of false feeding were identified in this study. In the first, birds sometimes only partially transferred

their load to nestlings. Incomplete transfer of prey was significantly associated with the type of prey that individuals attempted to donate. Relatively sticky, lerp-rich prey loads were more likely to be incompletely transferred. These rare (<2% of visits) false feeds are most parsimoniously explained as a prey transfer problem, rather than cheating or deception. Unlike previous studies, we were able to determine the impact of changes in brood demand upon the probability of these behaviors. This allowed us to demonstrate that individuals arriving with food but failing to give it to nestlings experienced a significantly lower begging response during that visit than their preceding one. Thus, nestlings were less hungry than the individual would have expected, so birds sometimes reversed their decision to allocate the prey items to the brood, eating the prey themselves or taking it elsewhere, perhaps to another brood. This provides a more convincing explanation for this behavior than any attempt at deception and inference that provisioning constitutes a signal. This result matches the suggestion that provisioning birds use a simple rule of thumb when offering food to broods: If the nestlings are more in need of the food than the attendant, the food is transferred; if not, the bird consumes the load. A similar conclusion has been suggested in recent studies of false feeding in both birds (Canestrari et al. 2004) and mammals (Clutton-Brock et al. 2005). This explanation based on dynamic changes in brood state relative to provisioner state makes the prediction that classes of individual in relatively low condition will false feed more frequently because they are more often going to be hungrier than the nestlings. This has been borne out in many studies, with false feeders either being more likely to be young individuals (Stallcup and Woolfenden 1978; Lawton and Guindon 1981; Poiani 1993; Boland et al. 1997; Legge 2000), floaters without a regular territory (Langen 1996), or female breeders facing significant reproductive investments (Canestrari et al. 2004). Future work examining the additional effects of changes in individual condition and the different thresholds in relative condition required to induce decisions to withhold prey would be informative. In conclusion, there is clear evidence emerging from several systems of more parsimonious explanations for false-feeding behaviors than cheating or deception (Canestrari et al. 2004; Clutton-Brock et al. 2005; this study). We would suggest that the label false-feeding is often a misnomer because it implies adaptive benefits from deception that cannot be substantiated convincingly in most field studies. We would recommend that future workers adopt more neutral terminology in studies that do not test explicitly for the phenomenon of deception, as well as ensure that different types of atypical provisioning behavior

Behav Ecol Sociobiol

are assessed separately. For example, visits where no prey items are brought to the nest can more correctly be described as non-feeding visits. Individuals failing to transfer prey to nestlings are clearly doing so based upon recently updated provisioning decisions, or because of difficulty in transferring sticky or large loads to nestlings. Both these behaviors could be more correctly termed atypical provisioning events, or self-feeding and incomplete transfers, respectively.
Acknowledgment Nick and Joan Hoogenraad and the La Trobe University Wildlife Reserve kindly allowed field work to be undertaken on their land. We thank Maria Pacheco, Luc te Marvelde, James OConnor, Dean Ingerson, and Amanda Dare for their assistance with the fieldwork. Anna Lashko, Mike Double, and Andrew Cockburn provided facilities for and carried out the molecular analyses. Robert Gibson, Robert Heinsohn, and an anonymous reviewer commented on an earlier version of this manuscript. Leg bands were provided by the Australian Bird and Bat Banding Service. This research was carried out under a BBSRC grant (5/S19268) to J.W. and the University of Wales, Bangor, and was approved by the La Trobe University Animal Ethics Committee (license AEC01/19(L)/V2) and the Department of Sustainability and Environment (license 10002082).

References
Boland CRJ, Heinsohn R, Cockburn A (1997) Deception by helpers in cooperatively breeding white-winged choughs and its experimental manipulation. Behav Ecol Sociobiol 41:251256 Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, Princeton, New Jersey Canestrari D, Marcos JM, Baglione V (2004) False feedings at the nests of carrion crows Corvus corone corone. Behav Ecol Sociobiol 55:477483 Carlisle TR, Zahavi A (1986) Helping at the nest, allofeeding and social status in immature Arabian babblers. Behav Ecol Sociobiol 18:339351 Charif RA, Clark CW, Fristrup KM (2004) Raven 1.2 users manual. Cornell Laboratory of Ornithology, Ithaca, New York Clarke MF (1984) Cooperative breeding by the Australian bell miner Manorina melanophrys Latham: a test of kin selection theory. Behav Ecol Sociobiol 14:137146 Clarke MF (1989) The pattern of helping in the bell miner (Manorina melanophrys). Ethology 80:292306 Clarke MF, Fitz-Gerald GF (1994) Spatial organisation of the cooperatively breeding bell miner Manorina melanophrys. Emu 94:96105 Clarke MF, Heathcote CF (1990) Dispersal, survivorship and demography in the cooperatively breeding bell miner Manorina melanophrys. Emu 90:1523 Clutton-Brock TH, Russell AF, Sharpe LL, Jordan NR (2005) False feeding and aggression in meerkat societies. Anim Behav 69:12731284 Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc R Soc Lond B 273:13751383 Conrad KF, Clarke MF, Robertson RJ, Boag PT (1998) Paternity and the relatedness of helpers in the cooperatively breeding bell miner (Manorina melanophrys). Condor 100:343349 Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology, an evolutionary approach. Blackwell, Oxford, pp 301337

Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116121 Gaston AJ (1978) Ecology of the common babbler Turdoides caudatus. Ibis 120:415432 Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:12311234 Jones DA (1998) Parentage, mate removal experiments and sex allocation in the cooperatively breeding bell miner, Manorina melanophrys. MSc thesis, Queens University, Canada Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge Kokko H, Johnstone RA, Wright J (2002) The evolution of parental and alloparental effort in cooperatively breeding groups: when should helpers pay to stay? Behav Ecol 13:291300 Langen TA (1996) The mating system of the white-throated magpiejay Calocitta formosa and Greenwoods hypothesis for sexbiased dispersal. Ibis 138:506513 Lawton MF, Guindon CF (1981) Flock composition, breeding success, and learning in the brown jay. Condor 83:2733 Legge S (2000) Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter. Anim Behav 59:10091018 McDonald PG, Heathcote CF, Clarke MF, Wright J, Kazem AJN (2007) Provisioning calls of the cooperatively breeding bell miner Manorina melanophrys encode sufficient information for individual discrimination. J Avian Biol 38:113121 Mulder RA, Langmore NE (1993) Dominant males punish helpers for temporary defection in superb fairy-wrens. Anim Behav 45:830833 Painter JN, Crozier RH, Crozier YC, Clarke MF (1997) Characterization of microsatellite loci for a cooperatively breeding honeyeater. Mol Ecol 6:11031105 Painter JN, Crozier RH, Poiani A, Robertson RJ, Clarke MF (2000) Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys. Mol Ecol 9:13391347 Piper WH (1994) Courtship, copulation, nesting behavior and brood parasitism in the Venezuelan stripe-backed wren. Condor 96:654671 Poiani A (1993) Social structure and the development of helping behaviour in the bell miner (Manorina melanophrys, Meliphagidae). Ethology 93:6280 Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258275 Reyer H-U (1990) Pied kingfishers: ecological causes and reproductive consequences of cooperative breeding. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds: long term studies of ecology and behaviour. Cambridge University Press, Cambridge, pp 527557 Semple S, McComb K (1996) Behavioural deception. Trends Ecol Evol 11:434437 Stallcup JA, Woolfenden GE (1978) Family status and contributions to breeding by Florida scrub-jays. Anim Behav 26:11441156 Wright J (1997) Helping-at-the-nest in Arabian babblers: signalling social status or sensible investment in chicks? Anim Behav 54:14391448 Wright J (1998) Helpers-at-the-nest have the same provisioning rule as parents: experimental evidence from play-backs of chick begging. Behav Ecol Sociobiol 42:423429 Wright J (1999) Altruism as a signalZahavis alternative to kin selection and reciprocity. J Avian Biol 30:108115 Zahavi A (1977) Reliability in communication systems and the evolution of altruism. In: Stonehouse B, Perrins C (eds) Evolutionary ecology. University Park Press, Baltimore, pp 253259 Zahavi A (1995) Altruism as a handicap: limitations of kin selection and reciprocity. J Avian Biol 26:13