Behavioral Ecology Advance Access published online on February 7, 2008
Behavioral Ecology, doi:10.1093/beheco/arm163
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Helper contributions to antiparasite behavior in the cooperatively breeding bell miner
a Department of Zoology, La Trobe University, Melbourne, Victoria, 3083, Australia b School of Biological Sciences, University of Wales, Bangor, Gwynedd LL57 2DG, UK c Institute of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway
Address correspondence to P.G. McDonald. E-mail: paul{at}galliform.bhs.mq.edu.au.
Received 21 June 2007; revised 20 December 2007; accepted 27 December 2007.
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ABSTRACT |
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Cooperatively breeding bell miners (Manorina melanophrys) have numerous male helpers assisting at multiple nests. Helpers are often related to the brood they aid, consistent with kin selection. However, there are also unrelated helpers for which other direct fitness benefits are likely to accrue. Bell miner nestlings can become infested by the larvae of a parasitic fly (Passeromyia indecora), which reduce growth and can be fatal. We investigated the amount of time that breeding pairs and helpers closely inspected nests and preened nestlings, behaviors apparently directed at detecting and removing parasites, a form of helping previously unstudied in a cooperative bird. Female breeders provided the greatest antiparasite effort, with breeding males and helpers not differing in effort regardless of their relatedness to the breeding female or brood. We also experimentally infested nests with nonparasitic flies and larvae. All individuals removed the introduced "parasites" if and when they encountered them. Compared with control sessions, inspection effort increased for all birds immediately after the experimental infestations, but only for a short, 5-min period. Further, we detected no changes in helper antiparasite behaviors after the temporary experimental removal of either breeding females or males. Such consistent helping behavior, independent of relatedness and potential audience effects, suggests that antiparasite behavior in bell miners is not particularly kin directed or operating as a signal of helper quality. Our results instead suggest that helper antiparasite effort appears to represent adaptive investment in the welfare of the brood, consistent with direct fitness benefits from group augmentation.
Key words: dipteran infestation, helping at the nest, parental care, Passeromyia, signaling hypotheses.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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The apparent altruism involved in helping behavior by cooperatively breeding birds has long been of interest to biologists (Brown 1987
; Emlen and Wrege 1989; Emlen 1997). In these systems, nonparental individuals (helpers) are often thought to increase their fitness indirectly by assisting to raise kin (kin selection: Hamilton 1964; Maynard Smith 1964). However, alternative hypotheses have also been proposed to account for helping behavior, particularly when individuals assist broods to whom they are not related (e.g., Clarke 1995; Cockburn 1998, 2006; Russell et al. 2007). Helping in this context may provide direct fitness benefits by increasing group size and thus the probability of survival and/or future reproduction by helpers (group augmentation and/or pseudoreciprocity: Woolfenden and Fitzpatrick 1978; Ligon 1981; Brown 1987; Connor and Curry 1995; Kokko et al. 2001; Doerr ED and Doerr VAJ 2007). In addition, helpers might accrue direct benefits simply through being known to have provided help, irrespective of whether there are positive effects on nestling fitness. For example, helping may constitute a payment of rent in return for access to group membership ("pay to stay": Gaston 1978; Reyer 1984; Mulder and Langmore 1993; Kokko et al. 2002) or might improve an individual's standing within a group, thus facilitating greater access to resources, matings, or beneficial coalitions in the future ("social prestige": Zahavi 1977, 1995; Wright 1999).
These various hypotheses have generally been examined by monitoring the provisioning effort of helpers feeding young in the nest (Emlen 1997; Cockburn 1998). However, there are other useful activities associated with rearing offspring in which helpers might contribute. For example, helpers may assist in the mobbing of predators or carry out nest sanitation activities such as fecal sac and parasite removal. By focusing on only one potential avenue of helping, incomplete conclusions may be drawn about both helper contribution levels and thus the pathway by which helpers derive benefits. Moreover, different modalities of helping may accrue benefits via different pathways, as most hypotheses proposed to account for cooperation are not necessarily mutually exclusive. Although the patterns associated with helping behavior in mobbing have received some attention in the literature (e.g., Arnold et al. 2005; Griesser and Ekman 2005), we are not aware of any study to date that has examined helper contributions to antiparasite nestling care in a cooperative system.
Antiparasite care may be particularly relevant in cooperative breeding systems, as one of the potential costs of group living is likely to be increased rates of parasitism (Chapman and George 1991; Poulin 1991; Poiani 1992, 1994). Both adult and nestling birds are susceptible to attack by a wide range of parasites, including flies of the families Calliphoridae, Neottiophilidae, and Muscidae. Birds use a number of strategies to repel, avoid, or eliminate parasitic flies, such as careful nest and roost site selection, use of plant compounds, and preening (Hart 1997). Preening and scratching are activities common to all birds and represent the most immediate individual defense against parasites (Cotgreave and Clayton 1994). However, little investigation has been carried out concerning the antiparasite behavior of parents aimed at protecting their broods from infection. Studies of 3 altricial bird species have shown that higher rates of dipteran parasitism in nests can lead to an increase in the amount of provisioning and/or examination of broods (Moss and Camin 1970; Christe et al. 1996; Hurtrez-Boussès et al. 1998, 2000), although 1 study has failed to confirm this finding (Thomas and Shutler 2001).
The bell miner (Manorina melanophrys Latham, Meliphagidae) is a cooperatively breeding honeyeater endemic to southeast Australia. They occur in colonies of as few as 5 to several hundred individuals, with males being the more philopatric sex (Clarke and Heathcote 1990). Nests are attended by a breeding pair plus a variable number of helpers, each of which may aid in the provisioning of nestlings at a number of different nests (Clarke and Fitz-Gerald 1994). The majority of helpers are male, some of whom are related to the breeding pair and the brood, therefore suggesting kin-selected benefits to helping (Clarke 1984; Conrad et al. 1998; Painter et al. 2000). However, more than 50% of helpers are unrelated to at least one member of the breeding pair (Painter et al. 2000), and even breeding males assist at nests other than their own, implying direct fitness benefits of helping are also potentially important in this species.
Bell miner nestlings (but not adults) can be parasitized by the fly larvae of Passeromyia indecora, reducing their growth rate (Poiani 1993a; Pont 1974) and occasionally causing death. Miners often spend long periods inspecting nests and nestlings, presumably searching for such parasites. Active inspection and preening of the brood may therefore be an important antiparasite task performed by helpers in this species. We assessed the extent to which helpers assist in nest inspection and brood preening activities and determined whether or not related and nonrelated helpers differed in their frequency of nestling care, thereby separating the importance of indirect and direct fitness benefits. This was done by challenging nest attendants of differing relatedness to the brood with experimental infestations of a nonparasitic species and observing unmanipulated nests to quantify helping effort in this context. Further, we also assessed whether helpers modified their antiparasite behavior according to the experimentally induced absence of potential "audiences" (members of the breeding pair). In this way, we provide the first critical empirical assessment of helper contributions to antiparasite behavior in a cooperatively breeding bird and its possible adaptive function.
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METHODS |
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Study sites and bell miner populations
The study was conducted between August 2004 and December 2005 in 2 bell miner colonies (N = 45 and 135 individuals) located at 1) La Trobe University Wildlife Reserve, Victoria, Australia (37°42'58''S, 145°03'20''E) and 2) a private property in St Andrews, Victoria (37°35'09''S, 145°15'41''E). All birds were captured using mist nets and fitted with unique combinations of color bands allowing individual identification. While captured, a 70-µl blood sample was collected from the alar vein, stored in 70% ethanol, and sent to the Australian National University (Canberra, Australia), where they were sexed according to the protocol of Fridolfsson and Ellegren (1999)
and genotyped using 6 polymorphic microsatellite markers according to the protocol of Painter et al. (1997). For each nest, the breeding female was identified as the only individual that builds nests, incubates eggs, and broods nestlings (Poiani 1993b). The breeding male is the male that fed nestlings most often when they were 0–2 days old, a period when helpers rarely feed at nests (Clarke 1988). Broods are sired by the male identified in this manner in the vast majority of cases, with exceptions consisting of partial broods only and thus presumably extrapair fertilizations (4% of nestlings; Conrad et al. 1998).
Individuals attending each nest were assigned to a "social class" according to their relationship to the breeding female: 1) the breeding female herself, 2) the breeding male, 3) "related" male helpers (r: mean ± standard deviation = 0.41 ± 0.15, N = 15), 4) "unresolved" male helpers (r = 0.22 ± 0.14, N = 47), and 5) "unrelated" male helpers (r = –0.04 ± 0.19, N = 81). Female helpers (N = 8) were present in this study, but not in sufficient numbers or helping frequency for their inclusion in statistical analysis. The coefficient of pairwise relatedness (r) was calculated by comparing the proportion of shared alleles between 2 individuals (breeding female and each helper) with the allele frequencies in the whole population (using the program KINSHIP v.1.2; Queller and Goodnight 1989). A low or negative r value means individuals were unlikely to be related, r values close to 0.5 indicate individuals were full siblings, and r values close to 0.25 indicate half-siblings (Queller and Goodnight 1989). Log-likelihood estimates were calculated in each case in order to confirm that relatedness values of 0 (unrelated) and 0.5 (related) could be assigned with confidence (with null relatedness values of 0.5 and 0, respectively) using KINSHIP. Hence, helpers termed unresolved were those whose relatedness was not clear either because they had coefficients of relatedness close to 0.25 (they were half-siblings of the breeding female) or because their particular allele combinations resulted in unreliable levels of relatedness to the breeding female being assigned. It is important to note that relatedness was also calculated relative to the breeding male alone and to an average of both members of the breeding pair. However, the use of either method did not change the results obtained, and, for simplicity, results are presented only in terms of relatedness to the breeding female, as these are the most important and interesting relationships for any "signaling" hypotheses—see the introduction.
Three distinct analyses were performed: 1) an analysis of unmanipulated nestling care at 21 nests by breeders and helpers, 2) an experimental infestation of 10 nests with "parasites," and finally 3) an assessment of changes in nestling care during periods of temporary removals of either the breeding male or the breeding female (N = 10 nests for each sex). All the nests exposed to an experimental treatment were included in the natural behavior database; however, only the first 2 h of observation from 1 day, prior to any experimental treatments, were included in the natural data analyses. This did not involve days of experimental infestation, as initial controls in that experiment were only 1 h long. Temporary removals and infestations were performed on the same nests on 6 occasions, however, on subsequent days. No apparent differences were observed in control data between nests in this study depending on whether or not they had been exposed to a previous temporary removal. This was true of proportion of visit spent inspecting (no removal 23.4 ± 3.84% standard error [SE], N = 25 individuals; previous removal 22.6 ± 1.6% SE, N = 65; F1,84 = 0.061, P = 0.806), inspection per hour (no removal 40.8 ± 9.5 s SE; previous removal 44.4 ± 11.8 s SE; F1,84 = 0.071, P = 0.790), proportion of visit spent preening (no removal 3.5 ± 1.5% SE; previous removal 2.3 ± 0.6% SE; Kruskal–Wallis test: 
12 = 0.133, P = 0.716), and finally preening effort per hour (no removal 56.1 ± 30.0 s SE; previous removal 18.6 ± 8.2 s SE; Kruskal–Wallis test: 12 = 0.129, P = 0.720). Indeed, control data on removal days did not differ between pre- and postremoval observations on the actual day of removal (for additional removal experiment behavioral analyses, see McDonald, Kazem et al. forthcoming), indicating experimental treatments had no detectable long-lasting influence on provisioning behavior in this species.
Behavioral data collection—all experiments
Nests and a radius of 5 m from the nest were observed using a telescope (Nikon 20-45x Field EDII Spotting telescope; Tokyo, Japan) throughout the 5-h experimental period from a hide situated 15–20 m from the nest. Observations did not begin until 10 min after the observer entered the hide to allow normal provisioning behavior to resume. Activities at the nest were also video recorded using a camera (Sony CCD-TR1100E Hi8 or Sony DCR-TRV265E digital Hi8; Tokyo, Japan) placed 1–4 m from the nest. These observer and equipment distances have previously been shown not to influence provisioning behavior (McDonald et al. 2007). Videos were later burned onto DVD using a DVD recorder (Pioneer DVR-310; Tokyo, Japan) and behavioral data scored using Intervideo WinDVD v.6.
For every visit to the nest, the individual was identified and visit duration and nestling care activities recorded. Nestling care behaviors were classified into 3 categories: 1) preening (individual gently groomed nestlings with its bill), 2) inspecting (individual perched on nest rim and stared at nest and/or nestlings without touching either), and 3) examination of the "outside" of the nest, often probing the nest material with its bill. In the case of experimentally simulated parasite infestations, an additional activity was considered: removal of a maggot/fly. Both the amount of time per hour dedicated to the different types of behavior (i.e., examination effort per hour) and the proportion of each visit dedicated to each behavior (i.e., examination effort per visit) were calculated.
Experimental parasite infestation protocol
In order to expose the birds to an appropriate cue that might stimulate an increase in their levels of care in terms of antiparasitic nest/nestling examination, 10 nests were experimentally infested with either 1-cm-long maggots (N = 6 nests) or adult flies (N = 4 nests), with the aim of simulating a natural infestation by P. indecora. For ethical reasons, experimental maggots and flies were of the nonparasitic species Calliphora vicina (Diptera, Calliphoridae). Both maggots and flies (hereafter parasites) were attached to nest material obtained from old bell miner nests. Maggots were tied to nest material using human hairs, whereas flies were glued to nest material with Spray Bandage (Elastoplast, North Ryde, Australia). In maggot treatments, a total of 10 larvae were used per nest (8 placed around the nest rim and 2 inside the nest cup). In fly treatments, 4 flies were positioned around the nest rim. All maggots and flies were still alive and moving when placed in the nest.
The experiment involved a within-nest design, thereby avoiding potentially complicating factors such as group size per nest, and was carried out over a 5-h period on a single day. The protocol involved scoring nestling care during visits as described above over 1 h of control observations (control 1), followed by a 1-h manipulation consisting of either a simulated infestation or a sham control; another hour of control observations (control 2), a further 1-h manipulation of the remaining treatment; and a final hour of control observations (control 3). There was a pause of approximately 10 min between each hour of the experiment when relevant experimental treatments were carried out. Sham control manipulations involved placing unparasitized nest material around the nest rim to control for the effect of handling/disturbing nests and assess the sensitivity of birds to this procedure. The order of sham control and experimental parasite presentation was rotated to control for order effects, as was the type of parasite, either flies or maggots. Nestling age in this experiment ranged between 5 and 10 days (mean 7.1 ± 0.7 SE days old).
Temporary breeder removal experimental protocol
In order to simulate the absence of the breeding female or male, in an additional experiment, 1 of the 2 breeders were captured with mist nets and temporarily removed (N = 10 removals for each sex, thus total N = 20) for 2 h. Removed birds were placed, out of visual and acoustic contact of the rest of the colony, in a temporary cage with sugar water available ad libitum. The antiparasite behavior of the remaining breeder and helpers during the experimental absence of this audience was compared with that exhibited during 2-h control periods either before (precontrol) or after (postcontrol observations) the removals took place. After completion of observations during experimental removals, removed individuals were released within 50 m of the nest area by remote release of the cage door. All removed individuals resumed provisioning within a short period (usually within 20 min). Experiments were carried out when nestlings were 6–10 days old (mean ± SE = 7.7 ± 0.3 days for male removals and 7.7 ± 0.4 days for female removals).
Statistical analyses
Repeated measures analysis of variances (RM-ANOVAs) or Kruskal–Wallis tests, if data could not be adequately transformed, were used to assess changes in social class differences in nestling care variables in the unmanipulated observation data. In both experimental databases (simulated parasite infestations and temporary removals), all aspects of behavior scored during control periods within each experimental trial did not differ significantly across controls or in interactions between control period and social class (Table 1). There were 2 significant influences of social class alone as expected (Table 1), details of which are examined below. Given this, control data within each experiment were combined to generate mean control values for ease of interpretation. For both experimental manipulations, RM-ANOVAs were conducted to test for differences in behavior according to "observation type"—that is, mean control observation and experimental treatment periods. These tests for changes in behavior took into account the differing social class of individuals as a between-subjects effect. In the parasite experiment, potential differences between infestation treatment (maggots vs. flies) were also considered. Mauchly's test for sphericity was used and violations corrected by the Greenhouse–Geisser method. Tests showing significant main effects of social class were followed by Helmert contrasts. These involved 4 orthogonal contrasts: 1) breeding females versus the remaining social classes, 2) breeding males versus all helpers, 3) unrelated helpers versus unresolved and related helpers (combined), and 4) unresolved versus related helpers. Whenever assumptions of normality could not be met after transformations, a nonparametric Kruskal–Wallis test based on differences between observational periods (i.e., differences in behavior between control and sham periods for an individual and also control and experimental periods) or Mann–Whitney U tests were used as appropriate. P levels were adjusted to 0.0125 using Bonferroni corrections to account for multiple testing in these cases.
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The potentially confounding effects on nestling care behaviors of colony, weather (precipitation and temperature), nestling age, and order of manipulation (e.g., parasite presentation before or after sham manipulation) were examined, and all found to be nonsignificant (all P > 0.05); thus, these factors were not considered in subsequent analyses. One nest subjected to the artificial parasite infestation was excluded from the analyses because it rained heavily for 4 of the 5 h during the day of observation, and birds other than the breeding female visited very infrequently. All analyses were performed using SPSS v.12.0 for Windows. Values are given as mean ± 1 SE, and a critical P value of 0.05 was applied unless otherwise specified.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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Natural rates of nestling care
In the database collected by observing 21 nests for 2 h each, 4570 visits were observed by 185 individuals (mean 6.8 helpers per nest ± 0.9 SE). There was a significant difference in the mean number of visits to the nest per hour according to social class (F4,180 = 14.35, P < 0.0005; Figure 1A). Breeding females and breeding males were the most frequent visitors, with breeding females visiting more than all other birds (contrast: P < 0.0005) and breeding males more than all helpers (contrast: P = 0.001). In addition, both unresolved and related helpers visited nests more than unrelated helpers (contrast: P = 0.011; Figure 1A). The duration of nest visits was also significantly influenced by social class (F4,180 = 14.11, P < 0.0005; Figure 1B), with the main difference again being the behavior of breeding females, who had significantly longer visit means than all other social groups (contrast: P < 0.0005).
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Surprisingly, there were no effects of social class on the proportion of time within each visit spent inspecting (F4,180 = 0.88, P = 0.475; Figure 2A). However, there was a significant difference in the absolute mean time spent inspecting per hour according to social class (F4,180 = 8.16, P < 0.0005; Figure 2B), with breeding females inspecting more per hour than any other class of bird (contrast: P < 0.0005) and breeding males more than helpers (contrast: P = 0.005), though no significant differences between the different classes of helper (contrasts P > 0.430). This is perhaps to be expected, given that the members of the breeding pair are the most frequent visitors to nests (Figure 1A).
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When considering preening effort per visit, there was again a significant difference between birds of different social class (Kruskal–Wallis test:
42 = 43.58, P < 0.0005; Figure 3A), mostly due to breeding females preening significantly more per visit than any other social class (Mann–Whitney U test: Z = –6.44, N1 = 21, N2 = 164, P < 0.0005). A similar result was found for mean time spent preening per hour (Kruskal–Wallis test: 42 = 39.76, P <0.001; Figure 3B), with females again dedicating significantly more time per hour to preening (Mann–Whitney U test: Z = –5.67, N1 = 21, N2 = 164, P < 0.0005; Figure 3B). All males, regardless of their relatedness or breeding status, preened nestlings at similarly low levels (Figure 3). Inspection of the outside of the nest cup was observed very rarely and only by breeding females. As such, it was not possible to examine changes in this behavior in further analyses.
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Parasite removal after simulated parasite infestation of nests
All birds, irrespective of their social class, were equally likely to remove both maggots and flies when they encountered an experimentally introduced parasite at the nest (F4,25 = 1.97, P = 0.131). There was also no significant difference in this response between the fly and maggot treatments (F1,25 = 1.29, P = 0.266; maggots removed 29.2 ± 5.0% SE of visits when present, flies 11.0 ± 2.7% SE; both N = 17). Birds never attempted to eat the maggots at the nest, although 2 flies were eaten at the nest by breeding females. Neither experimental maggots nor flies were fed to the nestlings. In all other cases, parasites were removed and taken at least 10 m from the nest.
Behavioral responses to experimental infestations
To investigate the timescale of any responses to simulated parasitism events, behaviors were quantified during successive 5-min periods within the 1-h manipulation. Behavioral increases in nestling care were apparent during only the first 5 min after treatment in both preening and inspection effort (Figure 4). We next compared the proportion of a given visit an individual spent inspecting the brood with social class for these first 5 min of the experimental observation versus means for both the control and the sham observations. A significant effect of observation type was observed (F1.337,24.063 = 15.107, P < 0.0005), with an increase in inspection effort during experimental periods compared with both control and sham observations (contrast: P < 0.0005; experimental period: 35.4 ± 2.5% SE; control: 30.3 ± 1.8% SE; sham: 29.0 ± 2.3% SE; N = 23). As expected, there was no difference between the control and the sham observation periods (contrast: P = 0.404), more surprisingly no effect of social class (F4,18 = 1.346, P = 0.291) and no interaction between social class and observation type (F5.347,24.063 = 0.870, P = 0.521). A similar result was obtained for the number of seconds individuals spent inspecting the brood, with a significant observation effect (F2,36 = 13.544, P < 0.0005), due to a significantly increased nest inspection effort during experimental (17.3 ± 2.9 s SE) compared with control periods (13.5 ± 1.5 s SE; contrast: P = 0.001; Figure 4), with again no difference between sham and control observations (sham: 13.6 ± 1.7 s SE; contrast: P = 0.387). Again there was no interaction between social class and observation type (F8,36 = 1.046, P = 0.422) and only a trend for social class (F4,18 = 2.685, P = 0.065). This trend was principally driven by related helpers (2.8 ± 2.1 s SE; N = 4) spending less time inspecting than unresolved helpers (15.5 ± 6.1 s SE; N = 2; contrast: P = 0.022), with none of the other contrasts reaching significance.
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In contrast to inspection rates, the total time devoted to preening did not differ between control and experimental or control and sham observations (Kruskal–Wallis test:
12 = 3.626, P = 0.057). This trend arose through preening not being observed during experimental treatments, though on average 25.3 ± 10.4 s SE and 32.9 ± 11.9 s SE were spent preening in the sham and control observations, respectively. Only breeding females could be included in this analysis, as they performed the vast majority of preening (see above). The fact that preening was never observed during the first 5 min of an experimental observation leads to a significant difference in the proportion of visits in which preening occurred between control and experimental observations as opposed to the difference between sham and control observations (Kruskal–Wallis test: 12 = 10.371, P = 0.001). However, as these differences were driven by a "lack" of preening effort after parasite exposure, preening clearly is unlikely to be associated with removing parasites. During the control and experimental periods of simulated infestation trials, there were no significant effects of the presence of the breeding female at the nest during another individual's visits on proportion of visit spent inspecting (F2,24 = 1.62, P = 0.220) or time spent inspecting (F1.34,16.128 = 0.03, P = 0.970). This also appeared true for preening effort; however, this behavior was performed so rarely by individuals other than the breeding female that statistical analyses could not be performed. Breeding males only rarely encountered another individual at the nest, and as such, we also could not repeat these analyses assessing the influence of the breeding male's proximity to the nest.
Behavioral responses to temporary removal of male and female breeders
During the 2 h of observation when breeding females were temporarily removed from their territories, the remaining nest attendants (obviously excluding breeding females) did not change their antiparasite behavior when compared with control periods when females were present on their territory (and therefore within 
28 m of the nest; Clarke and Fitz-Gerald 1994). This was true for the proportion of time per visit spent inspecting (control mean: 29.8 ± 2.3% of visit SE; removal mean: 33.4 ± 2.7 SE; both N = 76), social class effects, and interactions between the 2 (Table 2). Likewise, when the time spent inspecting was assessed, a similar lack of significant differences between experimental and control periods was observed (Table 2; control mean: 52.8 ± 8.8 s SE; removal mean: 63.9 ± 13.5 SE; N = 76). The exception was a social class effect with inspection effort (Table 2), with breeding males inspecting on average 6.7 ± 1.4 s SE (N = 10) more per hour than other classes (contrast: P = 0.002).
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There were no significant differences between periods of temporary female removal and control observations in the proportion of each visit different birds spent preening (Kruskal–Wallis test:
32 = 0.47, P = 0.925; breeding male change relative to controls: –1.2 ± 1.5% SE, N = 10; unrelated helpers: 0.3 ± 7.5% SE, N = 35; unresolved helpers: –0.7 ± 6.3 SE, N = 23; related helpers: –0.4 ± 1.3% SE, N = 8) or the mean time spent preening per hour (Kruskal–Wallis test: 32 = 0.03, P = 0.998; breeding male change relative to controls: –16.7 ± 14.8 s SE; unrelated helpers: 1.1 ± 4.2 s SE; unresolved helpers: 6.9 ± 6.0 SE; related helpers: –0.4 ± 1.2 s SE).
When removals of breeding males were considered, similar results were obtained, with the only significant difference being a social class effect (Table 2). Breeding females (N = 10) spent on average 9.7 ± 0.3 s SE more time per hour inspecting than male breeders and helpers (contrast: P < 0.0005). Experimental removal of breeding males failed to influence the proportion of visits other attendant classes preened the nestlings (Kruskal–Wallis test: 32 = 1.60, P = 0.659; breeding female change relative to controls: 1.4 ± 1.5% SE, N = 10; unrelated helpers: –1.0 ± 1.4% SE, N = 50; unresolved helpers: –0.5 ± 0.7% SE, N = 26; related helpers: –0.01 ± 0.1% SE, N = 5) or the mean time preening per hour (Kruskal–Wallis test: 32 = 0.48, P = 0.924; breeding female change relative to controls: –8.9 ± 18.9 s SE; unrelated helpers: –1.9 ± 3.1 s SE; unresolved helpers: –1.4 ± 3.7 s SE; related helpers: –0.3 ± 0.6 s SE).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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Natural rates of nestling care
Both breeding females and breeding males visited the nest more frequently than helpers. However, it was the duration of visits to the nest by breeding females that was unusually long. This was not due to females brooding the nestlings, a task conducted only by breeding females in this species (Poiani 1993b
), as nestlings were generally beyond the brooding stage during the periods of data collection. Thus, the extended nest visit times reflect greater effort by breeding females in terms of preening and nestling inspection.
It is not clear why breeding males did not contribute more to nest examination activities, especially preening effort. Bell miners have low levels of extrapair paternity (4% of offspring sired by extrapair males; Conrad et al. 1998), and as such, breeding males might have been expected to invest substantially in their brood. The activities of birds when they were not near the nest were not recorded, and thus, it is possible that breeding males were devoting more time to other activities important to successful fledging, such as antipredator vigilance or interspecific aggression to reduce competition for food. Similarly, helpers could also be investing comparatively more than females in activities away from the nest area such as the mobbing of predators. Clarke and Fitz-Gerald (1994) noted that both males and females repel other avian species without any major sex differences in this behavior. In other species of honeyeaters, males are more likely to be involved in both intra- and interspecific aggressive acts (e.g., yellow-faced honeyeater, Lichenostomus chrysops; Clarke et al. 2003). Even if breeding males and male helpers do not invest more than breeding females in group activities away from the nest area, their behavior may be sufficient to reduce the load placed on breeding females and thus extend her breeding tenure (Russell et al. 2007).
Antiparasite activities at nests
The antiparasite behaviors considered here may possess different functions. Self-preening has been shown to be effective as an antiparasite behavior (Hart 1997). There is little in the literature regarding the potential antiparasite function of preening of nestlings, although the benefits are likely to be similar. After our experimental infestations with parasites, the preening activity of both breeders and helpers did not change substantially; indeed, less preening was observed after simulated parasite infestation, perhaps suggesting that preening nestlings is not exclusively related to parasite avoidance. Another possibility is that the artificial parasites were not perceived as true parasites by the birds. However, this appears unlikely given they were removed from the nest by all birds and not simply fed to the nestlings as would be expected if they were perceived as nonparasitic flies. It should also be noted that only the larvae of these parasitic species are a direct potential threat. Therefore, the 2 instances of a breeding female eating an adult fly placed on the nest do not argue against the interpretation that the experimental treatment elicited behaviors consistent with typical defense against real dipteran parasites. A more parsimonious explanation for nestling preening (and lack of any change after the experimental introduction of flies) is that it has not specifically evolved for the purpose of parasite removal but is more likely to be associated with the enhancement of feather condition in nestlings, as it is in adults (Cotgreave and Clayton 1994).
In contrast, inspecting broods is an activity more likely to be aimed predominantly at detecting parasites, but it is also unlikely to be exclusively confined to this function. Both Hurtrez-Boussès et al. (2000) and Archard et al. (2006) described inspecting behavior as an antiparasite strategy, although they did not provide any empirical confirmation of this. In the present study, all birds showed an increase in inspection effort for a short period after artificial infestations, thereby firmly suggesting an antiparasite function of this behavior.
In all cases, there was no difference between the responses of bell miners to either maggots or adult flies placed on the nest. Both might constitute a threat to nestling bell miners, but for different reasons. Maggots are the direct parasites, and thus, their presence in the nest would be highly unwelcome; whereas adult female flies are the agents that lay eggs on nestlings, and consequently, their presence only potentially leads to later parasitism. Whether miners are able to make the association between adult flies and the risk of parasitism is unknown. However, it is clear from the experimental results that bell miners will specifically remove flies similar to Passeromyia if they settle on the nest, suggesting this link has been made.
Adaptive explanations for helping during nestling care and sanitation
Kin-selected benefits from helping have been suggested for bell miners based on putative relatedness to the brood (Clarke 1984, 1989), and this was later confirmed with molecular techniques (Conrad et al. 1998; Painter et al. 2000). In contrast, when assessing antiparasitic care, the results of the current study suggest that unrelated helpers provide as much aid as do related ones, regardless of whether relatedness was calculated relative to the breeding female, breeding male, or a combination of the 2. When nests were experimentally infested, unrelated helpers removed parasites as frequently as related individuals. Indeed, nest attendants of any class removed experimental parasites if and when they had an opportunity to do so. Moreover, during the experimentally induced absence of a breeder, both related and unrelated helpers displayed nest examination activities at similar rates and showed no change in behavior depending on the presence/absence of breeders, suggesting no obvious signaling function of antiparasite helping by nonrelatives versus relatives. Thus, any kin-selected benefits of antiparasite behavior in this system must be operating alongside other direct fitness benefits of helping nonrelatives, for example, via group augmentation and/or pseudoreciprocity (Woolfenden and Fitzpatrick 1978; Ligon 1981; Brown 1987; Connor and Curry 1995; Kokko et al. 2001).
If direct benefits from helping in bell miners were operating via signaling to breeders, for example, under the pay to stay hypothesis (Gaston 1978; Reyer 1984; Mulder and Langmore 1993; Kokko et al. 2002), then the presence or absence of the breeding male may be expected to have an effect on male helper behavior (assuming that such signaling is facultative)—yet no such change was detected. The experimental introduction of parasites into the nest could also have been interpreted by the breeding pair as a lack of nest examination effort by helpers. However, we saw no evidence after the experimental manipulations that helpers were harassed or punished for such "laziness." Indeed, overt aggression between males in bell miner colonies is very uncommon (Clarke and Fitz-Gerald 1994) and rarely seen in association with breeding activity (McDonald, te Marvelde et al. 2008). The presence of the breeding female or experimental absence of either member of the breeding pair (for a period of time long enough that their absence should have been detected by helpers) also did not affect the antiparasite activity of helpers, suggesting little evidence of nestling care by helpers acting as a signal as might be predicted if social prestige was important in this species (Zahavi 1977, 1995; Wright 1999). Together, neither the unmanipulated data nor the 2 different experimental treatments generated evidence that antiparasite helping behavior of related versus unrelated helpers differs, thereby failing to find support for signaling strategies driving these behaviors.
Instead, bell miners appear to have a rapid and effective parasite-removal strategy for dipteran parasites at the nest. Inspection behaviors returned to control levels within only 5 min of the experimental infestations, perhaps reflecting the birds’ confidence in their own efficiency at parasite removal. The potentially high benefit (i.e., preventing the nestlings from being infested) of inspecting and subsequent fly/maggot removal would suggest that it is always advantageous for any bird at the nest to carry out these behaviors. As with other helping behaviors in this system (McDonald, Kazem, et al. forthcoming; McDonald, te Marvelde, et al. 2008), such antiparasite care appears to represent genuine fitness investment in the brood for indirect (kin selected) and/or direct (e.g., group augmentation) fitness benefits, as opposed to having any signaling function.
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Biotechnology and Biological Sciences Research Council United Kingdom Grant (5/S19268) to J.W.; The University of Wales, Bangor.
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