Who cares? Effect of coping style and social context on brood care and defense in superb fairy-wrens

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1 Behavioral Ecology The official journal of the ISBE International Society for Behavioral Ecology Behavioral Ecology (2016), 27(6), doi: /beheco/arw096 Original Article Who cares? Effect of coping style and social context on brood care and defense in superb fairy-wrens Timon van Asten, Michelle L. Hall, and Raoul A. Mulder School of BioSciences, The University of Melbourne, Melbourne, VIC 3010, Australia Received 6 August 2015; revised 27 May 2016; accepted 1 June 2016; Advance Access publication 2 July In cooperatively breeding species, a breeding pair is often assisted in brood care by relatives. Group members can assist in both offspring provisioning and nest- and territory defense. It has been hypothesized that task specialization should occur in stable groups to make them more efficient and that individuals should perform tasks best suited to their behavioral phenotype or coping style. Alternatively, individuals may vary in how cooperative they are overall. We tested whether cooperatively breeding superb fairy-wrens (Malurus cyaneus) show task division or individual variation in cooperativeness during brood care and territory defense and whether contribution was related to coping style. We recorded offspring provisioning rates and presented groups with a conspecific intruder (taxidermic mount) and a novel object near the nest to score territory- and nest defense behavior, respectively. These behaviors were then compared with each other and with novel environment exploration, a good proxy of coping style in our population. Contrary to predictions, our data provided no evidence for task division or individual variation in cooperativeness. Response to the intruder was generally stronger when more than 1 group member was present. Within groups, relatively fast explorers responded more strongly to the novel object than relatively slow explorers when other group members were present, but not when alone. These results demonstrate that coping style can influence contribution to certain tasks, depending on the social context. They also emphasize the importance of social context in defense behavior in general. Key words: coping style, personality, brood care, cooperative breeding, social context, Malurus cyaneus, defense. INTRODUCTION In group-living animals, the structure and cohesion of a group has important fitness consequences for all of its members (Raihani et al. 2010; Webster and Ward 2011; Modlmeier et al. 2012). The cohesion and efficiency of groups are largely determined by behavioral interactions and coordination between individual group members. How well a group functions and how well each member fits into its structure has important consequences for individual life-history strategies (Bowler and Benton 2005; Webster and Ward 2011). Consistent temporal or contextual differences in behavior between individuals, better known as personalities, can affect the frequency and nature of an individual s social interactions. This in turn creates social dynamics that shape the social environment by varying group cohesion and cooperation (Webster and Ward 2011). To measure individual differences in behavior, individuals are typically released in an artificial, novel environment to test how they cope with novel situations (i.e., social isolation and unfamiliar Address correspondence to T. van Asten. t.van@unimelb.edu.au. environments). Several behaviors (e.g., exploration, activity, and boldness) often correlate with each other, forming a coping style that ranges among individuals from proactive/fast to reactive/slow (Koolhaas et al. 1999; Groothuis and Carere 2005). Individuals with a more proactive coping style enter and explore the novel environment more quickly and readily. Those with a more reactive coping style enter and explore more slowly. Coping style may be associated with individual differences in behaviors observed in natural (social) contexts, such as cooperation. Proactive individuals are often more aggressive than reactive individuals or pay less attention to conspecifics behavioral cues, linking coping style to level of sociality (Groothuis and Carere 2005; Aplin et al. 2014). This, in turn, can lead to variation in cooperativeness between individuals. Male banded mongooses (Mungos mungo), for example, show consistent individual variation in the amount of offspring care provided (Sanderson et al. 2015). Ultimately, individual variation in sociality and the resulting variation in strength of the ties to the social environment can lead to variation in life-history trajectories. For example, a growing number of studies show an increased dispersal tendency of more exploratory and asocial individuals (Trefilov et al. 2000; Fraser et al. 2001; Dingemanse et al. The Author Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please journals.permissions@oup.com

2 1746 Behavioral Ecology 2003; Duckworth and Badyaev 2007; Blumstein et al. 2009; Cote et al. 2011; Debeffe et al. 2014). In addition to general differences in cooperativeness or social integration, coping style variation can also be related to behavioral specializations within the social environment (e.g., social niche specialization: Bergmüller and Taborsky 2010; Montiglio et al. 2013). For example, more proactive individuals tend to be producers, whereas more reactive individuals follow these producers and become scroungers (Beauchamp 2000; Kurvers et al. 2010, but see Groothuis and Carere 2005). Where multiple individuals share a breeding territory, more aggressive individuals may prioritize territory defense, while more docile individuals care for offspring (Bergmüller and Taborsky 2007; Wright et al. 2014). Task division is mainly expected to occur where dispersal options are limited or where group living provides significant benefits over floating or pair living. In such cases, task division could reduce conflict and increase group performance and hence individual fitness. Task division has been described in a variety of species, mostly in cooperative breeders with tight and stable groups where the same individuals frequently interact with each other (Arnold et al. 2005; Bergmüller and Taborsky 2007; Carter et al. 2014; Wright et al. 2014). There is still scant empirical evidence relating individual personalities to behavior in a social context, especially in highly social species like communal and cooperative breeders (but see, e.g., Bergmüller and Taborsky 2007; Wright et al. 2014; McCowan et al. 2015). Most of the current studies investigating this relationship were conducted in captivity (but see McCowan et al. 2015). There is a need to link individual coping style to social behavior (or social personality) in the wild to further our understanding of social dynamics and how individual characteristics can cause variations in life histories among social animals. Cooperative breeders are particularly interesting subjects for the study of coping style, as they show large variation in life-history strategies. Many offspring delay dispersal and independent reproduction for at least 1 breeding season to assist their parents in raising more siblings, and some may even stay on the natal territory for life (Rowley 1965; Walters et al. 1988). This variation in life-history strategies can be related to coping style and the corresponding position in the social network or to the task (a) Defense more (b) an individual performs within its group. For instance, a captive study on cichlids found that more cooperative helper males are less likely to disperse than less cooperative helper males; however, helping behavior was not related to coping style (Schürch and Heg 2010). Generally, the relationship between coping style and helping behavior has not yet received much empirical attention and, to our knowledge, has not yet been studied in wild cooperative breeders. Coping style could relate to helping behavior in the wild in two ways: 1) independent of the social environment or 2) dependent on group composition. Where coping style is related to helping independent of the social environment, a relationship between coping style and the type or amount of help provided is expected across groups (i.e., a population-wide relationship, Figure 1a). As a result, groups consisting of more proactive individuals should function differently than groups consisting of more reactive individuals or groups with a high variety in coping styles. An individual s role within its group can also be determined by its coping style relative to that of other group members. In this case, a proactive individual might fulfill a caring role in a group with relatively more proactive individuals, whereas it would take up a defensive role in a group in which it was the most proactive individual (Figure 1b). Under this scenario, all groups of similar size should function similarly, regardless of their compositions, because roles are divided by rank order of coping styles rather than depending on absolute values. Finally, a combination of these two scenarios could also occur; where groups differ in average coping style, differences in average behavior between groups can still be seen, whereas within groups, behavior is still related to coping styles of members relative to each other (Figure 1c). We investigated whether absolute or relative individual differences in coping styles predict task division or levels of cooperative behavior during breeding in a natural population of a cooperatively breeding Australian passerine, the superb fairy-wren (Malurus cyaneus). During the breeding season, these birds are highly territorial and group members can contribute to both territory defense and offspring care. We scored nestling feeding rates of individual group members and placed a taxidermically mounted conspecific and a novel object near natural nests to score participation of individual (c) less reactive proactive reactive proactive Coping style reactive proactive Figure 1 Three hypothetical scenarios for a correlation between coping style and defense across and/or within cooperative groups (gray lines: within-group correlations between traits and broken black lines: across group correlations between traits). A positive overall correlation can be found, even when withingroup correlations show a random pattern (a). In this case, variation in behavior within groups cannot be very large, or no overall correlation will be found. Alternatively, an overall positive correlation can be absent, whereas within-group correlations can all be positive (b). This would indicate that individuals make behavioral decisions based on the behavior of others in their direct social environment and are less driven by internal motivations. Finally, a strong overall positive correlation between traits will be found when both within- and between-group correlations are positive (c).

3 van Asten et al. Fairy-wren coping style, brood care, and defense 1747 group members in nestling provisioning, territory defense, and nest defense, respectively. The aim was to test 1) whether superb fairywrens show task division or general variation in levels of cooperativeness with regard to offspring care and defense and 2) whether individual variation in provisioning and defense behavior is related to coping style (i.e., whether proactive individuals are more involved in defense, whereas reactive individuals take on a larger share in offspring provisioning). MATERIAL AND METHODS Study site and species The study was carried out using a wild population of superb fairy-wrens in a small (28 ha) area of open woodland habitat surrounding an artificial lake in Serendip Sanctuary, ±70 km West of Melbourne, Australia (38.00 S, E). More than 95% of birds in the area have been banded with a unique combination of 3 colored leg rings for individual identification in the field, as well as 1 numbered metal ring, provided by the Australian Bird and Bat Banding Scheme. Since 2011, the population has been censused weekly during the breeding season and monthly outside the breeding season, and as a result, the compositions of all groups are known. Helpers in this species are typically retained male offspring from previous nests. In each group containing more than 1 male, the oldest male was always considered dominant. Where 2 males were of similar age, dominance was determined by the timing of molt (Mulder and Magrath 1994). Any additional males in a group were considered helpers. Female offspring typically disperse between reaching nutritional independence and the onset of the next breeding season, however occasionally a female will stay in the natal group throughout the next breeding season. Such subordinate females occur only very infrequently and rarely help at the nest (Rowley, 1965; personal observation). Individual behavioral tests Pre- and post-breeding season catching sessions have been carried out since 2011, and as a result, 84% of the birds in the population have been caught and assayed for their coping style at least once. The catching and assaying procedures are described in detail in Hall et al. (2015). In short, birds were caught in or near their home territory using mist nets. Standard measurements and blood samples were collected, after which birds were taken to an on-site facility. Here, they were individually housed in cages for at least an hour to acclimatize. After acclimatization, individual birds were released into a test room containing 4 wooden stands with horizontal perches. A grid of equal-sized squares divided the floor into 9 zones. We scored boldness (time taken to enter the assay room), exploration behavior (number of unique perches and zones visited in the 5 min after entering the room), activity (total number of movement between perches and zones in the 2 min commencing 6 min after entering the room), and social behavior (response to a mirror, revealed 8 min after a bird entered the room). The behavior of a bird in the room was scored from an adjacent room using live video from a GoPro Hero mounted on the test room ceiling. Any missed or misidentified behaviors were later added or corrected from the saved video recording. Exploration behavior was the most repeatable behavior within individuals over the long term and also correlated with boldness and activity (Hall et al. 2015). This means individual superb fairy-wrens can be placed on a proactive reactive coping style axis with bold, exploratory, and active birds at one end and shy, low activity birds at the other. In the current study, we used the exploration score of each individual s first assay as a proxy of its coping style. Not all birds had been assayed more than once, so using first exploration scores, when the novel environment was still truly novel to each individual, allowed for direct comparison between individuals. Behavioral observations in the field We carried out all observations of behavior in the wild at nests built over the 2013 and 2014 breeding seasons (September to January). Each observation session was conducted from a portable hide (Altan Safe Outdoors HO-BD038), set up m from a nest. Hides were set up at least 1 h before initiation of observations to allow the birds to habituate. We identified individual birds by their unique color band combinations. Feeding share Feeding rates of individual group members were scored during two 1-h observation periods, normally when nestlings were 7- and 9 days old, unless an observation session had to be postponed by a day due to adverse weather conditions. All feeding observations were carried out between 2 PM and 1 h before sunset (average ± standard deviation [SD]: 5:26 PM ± 1:10 h) for 48 and for 52 nests over the 2013 and 2014 breeding seasons, respectively. For an additional 20 nests in each season, only 1 of two feeding observations could be used, due to disturbance or premature termination of 1 of the 2 observations. Each visit by a bird to the nest was entered in real time into a central server, using a custom-made layout in the FileMaker Go app on an iphone 4s. Feeding rate can be affected by food availability in the territory, time of day, or weather conditions, which makes it difficult to distinguish this from search effort or efficiency and therefore to draw population-wide conclusions with regard to the relationship between coping style and parental care. Here we looked at feeding share, as this eliminates territorial differences in food abundance and effects of brood size and age and emphasizes within-group differences in contributions to brood care. We estimated each bird s feeding share its contribution relative to what would be expected if feeding was shared equally among all group members from the individual feeding rates for each feeding observation separately: FS i F = ( F G ) where FS i is the feeding share of individual i, F i is the observed number of feeds by the individual, F G is the total number of feeds by the group, and G is the total number of birds in the group. A feeding share of 1 therefore means an individual fed at the group average rate. Feeding shares >1 and <1 indicate individuals that invested more or less in feeding relative to other group members, respectively. Territory- and nest defense assays The experiment was carried out by a single observer (T.v.A.) at 24 and 15 nests during the 2013 and 2014 breeding seasons, respectively. Groups tested ranged in size from 2 individuls to 5 individuals (mean ± SD: 3.03 ± 0.85) and nestling age in the nests used ranged from 7 days to 13 days (mean ± SD: 9.62 ± 1.11). i G

4 1748 Behavioral Ecology Each assay consisted of 3 trials: 1) a territory defense trial, 2) a novel object trial, and 3) a control trial (see below). The order in which trials were presented was balanced between the 6 possible trial orders. Each assay (i.e., 3 trials) was conducted between 2 PM and 1 h before sunset within 1 day, with a gap of at least 45 min between trials. Within an assay, each trial lasted 10 min, extended if necessary to obtain a minimum of 3 min observation for each bird. If one or more group members did not appear within the initial 10 min trial period, the trial was extended by 5 min. The maximum trial time, therefore, was 18 min (i.e., when a bird only appeared in the last second of the 5 min extension). This research was approved by the University of Melbourne animal ethics committee ( ). Experimental trials Intruder. With this trial, we aimed to measure territory defense against a recognizable stimulus: a conspecific intruder. The observer placed a taxidermically mounted juvenile superb fairy-wren (hereafter referred to as simulated intruder or intruder ) approximately 2 m away from the nest and then returned to the hide to start scoring the birds response (see below). The intruder was placed on the ground in the same location as the novel object. Two intruders were available (both juvenile, 1 3 months old) and used alternatingly between assaying days. Novel object. This trial was carried out to measure inspection of an unfamiliar stimulus near the nest: a form of nest defense. The observer placed a small, 5 cm diameter mirror ball approximately 2 m from the nest, and then returned to the hide. The novel object was suspended 10 cm above the ground from a tent peg, placed where most birds would see it when coming in to feed the nestlings. Where possible, the exact same location was used for both intruder and novel object, however if there was no ground location in view from the direct nest area, the object was suspended from a small branch in view of the nest or feeding route. In assays where the novel object was suspended from a branch, the intruder was placed on the ground or on a thick branch 2 m from the nest in the most visible location available. Taxidermic mounts were affixed to a wooden base that was too heavy to be attached to a thin branch, but even in less conspicuous locations were more likely to elicit approach than the novel object (see Results). Control. The observer walked up to the nest area as if placing a novel object or taxidermic mount within 2 m of the nest (without actually doing so) and then returned to the hide. Behavior was then observed as in the two experimental trials, using the novel object location as the point of focus. The behavioral response to the novel object was always more subtle than to the intruder (see Results) and therefore more important to score against a control situation. Behavioral scoring Stimuli (i.e., intruder and novel object) were placed so they could be seen by a bird when it visited the nest (i.e., 2 m away). Because the stimuli might not always have been visible from >2 m away, we set the radius of the monitoring area to 2 m around the focal point. Behavior of birds was scored only while they were present within this monitored area. Observation started upon sitting down in the hide after placement of the novel object or intruder or the sham placement in case of the control trial. The observer watched the birds within the monitored area through binoculars and continuously vocally reported the birds identity, distance, and behavior into a digital voice recorder (Tascam DR-05). This method enabled uninterrupted observation of the birds behavior. During each trial, the distance and aggressive behaviors of each group member within 2 m of the focal point at any given time were monitored constantly. However, to obtain a standardized score for betweenindividual comparison, only the behavior of each individual scored over 3 min from first coming within 2 m was used in the analyses. Voice recordings were later transcribed in 15-s intervals. For each bird that could be identified by its color bands within 2 m of the focal point, the closest distance to the focal point was scored for each 15 s interval. In addition to closest approach, we calculated a response intensity score, combining proximity and duration of response. To obtain this score, we used the following calculation: I i 12 Bi d where I i is the number of intervals individual i was within 2 m, of the 12 total intervals (3 min scored since arrival 4 intervals/min), and d is the average approach distance of the individual for the intervals it was present. Therefore, the longer a bird was present and the closer it came on average to the focal point, the higher was its response intensity score. Birds that had seen the intruder would not necessarily attack but would never ignore it (e.g., circling it at a distance or scolding from a nearby perch were common responses). Additionally, higher attack rates were also associated with higher response intensity (see Results). We therefore feel that response intensity is a good representation of individual engagement with the intruder. Additionally, counts of songs and attacks (hopping onto, pecking at, or hitting novel object or intruder ) were scored within the same 15 s time intervals. These were uncommon (see Results) and were included in the descriptive results, but not in statistical models. Data analysis = ( ) Correlations between feeding share and defense To test whether superb fairy-wrens show task division or variation in general helpfulness, we conducted Pearson correlations for closest approach and response intensity measures (both absolute and relative to other group members) and feeding share between contexts (i.e., territory defense and novel object inspection). If fairywrens show task division (i.e., brood care vs. defense), we expected to see negative correlations between feeding share and response intensity and positive correlations between feeding share and closest approach distance (i.e., a larger closest approach distance indicates a weaker defensive response). If individuals differed in general helpfulness, we expected to find positive correlations between feeding share and response intensity and negative correlations between feeding share and closest approach distance (i.e., some individuals both feed and defend more than others). Because we could only correlate values for birds that came within 2 m in both the simulated intruder and novel object trials, the sample sizes were lower than for each of the trials separately (N = 57 [24 female breeders, 18 male breeders, and 15 male helpers]). Feeding share and exploration behavior To test whether exploration behavior predicted feeding share, we ran a generalized linear mixed-effects model (GLMM) with Gaussian error distribution ( lme4 package version 1.1.9, Bates et al. 2015) for all breeding attempts with feeding observations during the 2013 and 2014 breeding seasons (N = 140 nests on 92 territories and a total of 247 individuals) with feeding share (two scores per individual per breeding attempt) as the response variable. Individual and breeding attempt were included as random

5 van Asten et al. Fairy-wren coping style, brood care, and defense 1749 Table 1 Factors affecting share in offspring provisioning by individuals in their home group as determined by a model selection approach based on AIC C : global model and results of model averaging (relative AIC C weights of fixed effects, estimates of their effect sizes (±unconditional standard errors) with 95% CIs). The same model was run once with absolute values of exploration score and age, and once with values relative to the group average. Variance explained by random effects and their 95% CIs are given at the bottom of the table. Global model: Feeding share ~ SexRole a x Expl x Age + Group type x Expl x Age + (rand: Breeding attempt + Bird) Fixed effects Absolute values effects in the model (Table 1), based on selection using lowest Akaike information criterion (AIC) values from full models with breeding attempt, year, and individual and their different combinations as random effects (following Zuur et al. 2009). As fixed effects in the model, we included age, sex/role, and group type in addition to exploration behavior (see Table 1 for the global model). To test whether exploration behavior explained feeding share at a global or group level (see Introduction), the same model was run twice: once with raw exploration score and once with exploration score relative to other group members. Continuous variables were centered and standardized by subtracting the mean and dividing by the SD. To obtain estimates for fixed effects, we performed multi-model averaging using the dredge function from the MuMIn package version (Bartoń 2015) in R version (R Core Team 2015). Parameter estimates and relative weights were obtained from full averages from the top 95% confidence set of models, based on the AIC values for small sample size (AIC C ; zero method: Burnham and Anderson 2002; Grueber et al. 2011). Repeatability of feeding share The multiple feeding observations of the same groups allowed us to test how consistently individuals differed from each other in feeding share (i.e., how similar or repeatable individuals were between feeding observations). We calculated adjusted repeatability of individual feeding share from a model with feeding share as response variable, individual and breeding attempt as random effects and sex/role, the only explanatory variable of importance after model averaging (see Results), as a fixed effect. This accounts for variance explained by the most important factors, thus avoiding pseudo-repeatability issues (Dingemanse and Dochtermann 2013). Adjusted repeatability and 95% confidence intervals (CIs) were obtained by simulating 1000 iterations of the model, using the sim function in the arm package version (Gelman and Su 2014) in R. Repeatability was calculated by dividing the variance explained by bird by the total variance. Subset bias test for defense assays General nest attendance in the wild, as well as approach distance of birds to an intruder or novel object, can be related to coping Relative to group average Σω i Est. (±SE) 95% CI (low, up) Σω i Est. (±SE) 95% CI (low, up) (Intercept) 0.63 (±0.09) (0.44, 0.81) 0.65 (±0.10) (0.46, 0.85) Exploration score (±0.05) ( 0.10, 0.07) (±0.05) ( 0.13, 0.07) SexRole a Male breeder (±0.11) ( 0.97, 0.55) (±0.12) ( 0.97, 0.49) Male helper (±0.13) ( 1.10, 0.60) (±0.14) ( 1.19, 0.62) Age (±0.06) ( 0.15, 0.09) (±0.08) ( 0.21, 0.11) Group type (±0.13) ( 0.42, 0.08) (±0.14) ( 0.48, 0.07) Random effects σ 2 95% CI σ 2 95% CI Breeding attempt 0.00 (0.00, 0.00) 0.00 (0.00, 0.00) Bird 0.46 (0.43, 0.51) 0.47 (0.41, 0.50) CIs not crossing 0 shown in bold. a SexRole is a three-category term, containing female breeder, male breeder and male helper. style (e.g., Stuber et al. 2013). We therefore tested whether the individuals that approached to within 2 m in each of our trials differed in coping style from those that did not to make sure we did not score a biased subset of birds. We ran a binomial GLMM ( came within 2 m vs. did not come within 2 m as response variable) with the interaction between exploration score and trial as fixed effect and breeding attempt ID and individual ID as random effects. Birds that did not come within 2 m did not differ in exploration score from those that did come within 2 m in any of the trial types (estimate [and 95% CI] of the interaction between exploration score and the intruder trial: 0.27 [ 0.72, 1.42], and the interaction between exploration score and novel object trial: 0.07 [ 0.86, 1.05]). Therefore, we are confident our data set gives an unbiased assessment of the relationship between exploration and defense behavior. Defense behavior and exploration score Closest approach and response intensity correlated positively between novel object and control trials (closest approach: Pearson r = 0.41, P = 0.001, response intensity: r = 0.50, P < ), but not between intruder and control trials (closest approach: Pearson r = 0.24, P = 0.052, response intensity: r = 0.06, P = 0.65). This suggests some natural variation in the tendency of birds to be in the vicinity of the novel object location (e.g., if the selected location was closer to the main flight path to the nest) that did not affect responses to intruders. To control for this, we subtracted the control values from the novel object values. Due to this calculation, when comparing exploration to novel object response we could only use data from birds that came within 2 m in both the control and novel object trials (N = 59 birds in 31 groups). During the intruder trials 82 of the 105 individuals came within 2 m and could therefore be used in our analyses. Three territories were excluded because either none of the birds came within 2 m of the intruder or birds could not be reliably identified. To test how exploration affected closest approach and response intensity toward the intruder and novel object, we ran 4 GLMMs with Gaussian error distributions (2 per trial type ( intruder and novel object)): 1 with closest approach and 1 with response intensity

6 1750 Behavioral Ecology as response variable (Tables 2 and 3). The residuals of the model for response intensity toward the intruder showed overdispersion and as the alternative log-link function did not allow the model to converge, we log transformed the response intensity data toward the intruder to normalize the error distribution and correct the overdispersion. All models contained exploration score, time of day, height off the ground of the intruder /novel object, group type (groups vs. pairs), sex, role (breeder vs. helper), age of adults (in years), age of nestlings (in days), and presence/absence of other group members (see below) and relevant interactions as fixed effects and territory ID as a random effect (Tables 2 and 3). We included whether any other group members were present during the scoring of any particular bird as a fixed effect, as in the field this seemed to have an effect on how close a bird would approach the intruder (i.e., seemingly closer in the presence of others). During the control trials, the average length of any bird s visit was 1.25 min (i.e., five 15-s intervals). Therefore, we decided the presence of any other group member within 2 m from the intruder for 5 or more intervals was counted as the presence of another individual. This was to avoid cases where 2 group members happened to be 2 m or less away from the intruder for 1 or a few intervals but had little opportunity to interact with each other. Parameter estimates and their 95% CIs were obtained through model averaging following the method described above (see Feeding share and exploration behavior ). We considered parameters with CIs not crossing 0 to be significant predictors. Variance explained by the random effect territory ID was calculated for each GLMM by running 1000 iterations of each model with territory ID as random effect and only those fixed effects from the global model that were significant after model averaging. The sim function from the arm package was used to run the model iterations after which the variance explained by territory ID was divided by the total variance. Since an individual s behavioral differences from other group members may be as important as behavioral differences relative to the population as a whole, we reran the same four GLMMs described above, using values of exploration score and age relative Table 2 Factors affecting closest approach distance to the intruder and the novel object as determined by a model selection approach based on AIC C : global model and results of model averaging (relative AIC C weights of fixed effects, estimates of their effect sizes [±unconditional standard errors] with 95% CIs). Variance explained by the random effect territory (and 95% CI) is also included Global model a : Closest appr. ~ ST + NAge + Height + GT x Age + GT x Expl + OP x SexRole + OP x Expl + SexRole x Expl + (rand: Territory) Intruder Absolute values Relative to group average Fixed effects b Σω i Est. (±SE) 95% CI (low, up) Σω i Est. (±SE) 95% CI (low, up) (Intercept) 0.66 (±0.42) ( 0.20, 1.51) 0.02 (±0.21) ( 0.43, 0.40) Others present (±0.21) ( 0.83, 0.01) (±0.06) ( 0.14, 0.10) Height (±0.12) ( 0.33, 0.15) (±0.03) ( 0.05, 0.06) Age (±0.08) ( 0.24, 0.10) (±0.06) ( 0.22, 0.04) Exploration score (±0.10) ( 0.29, 0.12) (±0.06) ( 0.15, 0.07) Group type (±0.14) ( 0.33, 0.24) (±0.08) ( 0.13, 0.20) SexRole Male breeder (±0.07) ( 0.14, 0.12) (±0.06) ( 0.14, 0.11) Male helper (±0.06) ( 0.13, 0.12) (±0.05) ( 0.12, 0.10) Nestling age (±0.04) ( 0.08, 0.09) (±0.02) ( 0.04, 0.04) Start time (±0.05) ( 0.09, 0.10) (±0.03) ( 0.05, 0.07) Random effect σ 2 95% CI σ 2 95% CI Territory 0.36 (0.26, 0.46) 0.00 (0.00, 0.00) Novel object Absolute values Relative to group average Fixed effects b Σω i Est. (±SE) 95% CI (low, up) Σω i Est. (±SE) 95% CI (low, up) (Intercept) 2.43 (±0.73) (0.94, 3.92) 0.11 (±0.29) ( 0.49, 0.69) Others present (±0.13) ( 0.22, 0.31) (±0.08) ( 0.18, 0.16) Height (±0.04) ( 0.09, 0.09) (±0.03) ( 0.07, 0.07) Age (±0.10) ( 0.12, 0.29) (±0.12) ( 0.16, 0.31) Exploration score (±0.05) ( 0.09, 0.11) (±0.08) ( 0.11, 0.21) Group type (±0.10) ( 0.19, 0.23) (±0.11) ( 0.22, 0.21) SexRole Male breeder (±0.01) ( 0.29, 0.21) (±0.23) ( 0.63, 0.28) Male helper (±0.01) ( 0.24, 0.19) (±0.17) ( 0.41, 0.26) Nestling age (±0.07) ( 0.44, 0.14) (±0.03) ( 0.05, 0.05) Start time (±0.06) ( 0.10, 0.14) (±0.04) ( 0.07, 0.09) Random effect σ 2 95% CI σ 2 95% CI Territory 0.00 (0.00, 0.00) 0.00 (0.00, 0.00) Σω i : Summed relative AIC C weight of fixed effect, Est: effect size estimate (±unconditional standard error) and the 95% CI (CIs not crossing 0 shown in bold) based on full model average, σ 2 : variance associated with the random effect Territory. a Model fixed effects: ST = start time, NAge = nestling age, Height = height above the ground of presented stimulus, GT = group type (with or without helpers), Age = age of focal individual, SexRole = sex and role of focal individual (i.e., female breeder, male breeder, or male helper), Expl = exploration score of focal individual, OP = others present (yes/no, see main text for details) b All single fixed effects included. All interactions had negligible effects and are not included in the table

7 van Asten et al. Fairy-wren coping style, brood care, and defense 1751 Table 3 Factors affecting response intensity toward the intruder and the novel object as determined by a model selection approach based on AIC C : global model and results of model averaging (relative AIC C weights of fixed effects, estimates of their effect sizes [±unconditional standard errors] with 95% CIs). Variance explained by the random effect territory (and 95% CI) is also included Global model a : Resp. intensity ~ ST + NAge + Height + GT x Age + GT x Expl + OP x SexRole + OP x Expl + SexRole x Expl + (rand: Territory) Intruder Absolute values Relative to group average Fixed effects b Σω i Est. (±SE) 95% CI (low, up) Σω i Est. (±SE) 95% CI (low, up) (Intercept) 0.22 (±0.31) ( 0.83, 0.40) 0.02 (±1.33) ( 2.65, 2.69) Others present (±0.12) (0.36, 0.86) (±0.44) ( 0.62, 1.03) Height (±0.06) ( 0.09, 0.14) (±0.18) ( 0.36, 0.35) Age (±0.07) ( 0.09, 0.17) (±0.32) ( 0.64, 0.64) Exploration score (±0.11) ( 0.07, 0.39) (±0.34) ( 0.68, 0.67) Group type (±0.15) ( 0.10, 0.49) (±0.59) ( 1.30, 1.10) SexRole Male breeder (±0.04) ( 0.08, 0.07) (±0.25) ( 0.53, 0.48) Male helper (±0.05) ( 0.09, 0.10) (±0.28) ( 0.59, 0.53) Nestling age (±0.03) ( 0.07, 0.05) (±0.13) ( 0.27, 0.26) Start time (±0.03) ( 0.07, 0.06) (±0.15) ( 0.31, 0.31) Random effect σ 2 95% CI σ 2 95% CI Territory 0.17 (0.13, 0.26) 0.00 (0.00, 0.00) Novel object Absolute values Relative to group average Fixed effects b Σω i Est. (±SE) 95% CI (low, up) Σω i Est. (±SE) 95% CI (low, up) (Intercept) 0.68 (±0.35) ( 1.39, 0.02) 0.08 (±0.14) ( 0.36, 0.20) Others present (±0.05) ( 0.09, 0.12) (±0.06) ( 0.13, 0.11) Height (±0.04) ( 0.05, 0.11) (±0.02) ( 0.04, 0.05) Age (±0.05) ( 0.16, 0.03) (±0.03) ( 0.09, 0.03) Exploration score (±0.02) ( 0.04, 0.04) (±0.03) ( 0.07, 0.06) Group type (±0.04) ( 0.08, 0.09) (±0.04) ( 0.06, 0.10) SexRole Male breeder (±0.02) ( 0.05, 0.05) (±0.02) ( 0.04, 0.04) Male helper (±0.03) ( 0.05, 0.05) (±0.03) ( 0.05, 0.06) Nestling age (±0.04) (0.01, 0.16) (±0.01) ( 0.02, 0.03) Start time (±0.02) ( 0.05, 0.04) (±0.02) ( 0.04, 0.03) OP Expl (±0.10) (0.12, 0.51) Random effect σ 2 95% CI σ 2 95% CI Territory 0.00 (0.00, 0.00) 0.00 (0.00, 0.00) Σω i : Summed relative AIC C weight of fixed effect, Est: effect size estimate (±unconditional standard error) and the 95% CI (CIs not crossing 0 shown in bold) based on full model average, σ 2 : variance associated with the random effect Territory. a Model fixed effects: ST = start time, NAge = nestling age, Height = height above the ground of presented stimulus, GT = group type (with or without helpers), Age = age of focal individual, SexRole = sex and role of focal individual (i.e., female breeder, male breeder, or male helper), Expl = exploration score of focal individual, OP = others present (yes/no, see main text for details) b All single fixed effects included, but only those interactions that showed a substantial effect are included in the table. to the group mean, instead of absolute values. We also used the relative values for the response variables (closest approach and response intensity; Tables 2 and 3). We did this to test whether relative responses within groups differed, as individuals may respond more strongly to their direct social environment than at a population-level scale (Figure 1, see also van de Pol and Wright 2009). RESULTS Feeding share and response to intruder and novel object Feeding share was highly repeatable within individuals and explained 46% of overall variance in feeding share (Table 1). Female breeders provisioned more than male breeders or helpers, and feeding share was similar for both male categories (Table 1). Female breeders, male breeders, and helpers did not differ in their response (closest approach distance, response intensity, singing, or attacking) to the simulated intruder or novel object (Tables 2 and 3, Chi-squared tests for song and attack frequency: all P > 0.1). Singing and attacking only occurred during the intruder trials, with the exception of 1 song during a novel object trial. Thus, the overall response to the novel object was much more subtle than to the simulated intruder. Of all birds that came within 2 m of the intruder (N = 82), 15 (18.3%) sang, 6 (7.3%) attacked, and 9 (11.0%) both sang and attacked. Birds that sang were more likely to attack the intruder than those that did not sing (Yates χ 2 = 6.66, P = 0.01). Attackers also showed higher response intensity toward the intruder than non-attackers (Wilcoxon rank sum test: across groups: W = 165, P < , within groups: W = 294, P = 0.01).

8 1752 Behavioral Ecology Task division versus individual variation in cooperative tendency Females that responded more intensely to the simulated intruder also responded more intensely to the novel object (r = 0.46, P = 0.02). However, we did not find a cross-contextual correlation of response intensity for male breeders or helpers or for all birds pooled together (all P > 0.1). Closest approach did not correlate between contexts (territory defense vs. novel object inspection, all P > 0.1), that is, birds with a close approach distance to the intruder did not also approach the novel object closely and vice versa. An individual s feeding share also did not predict its closest approach and response intensity toward either intruder or novel object (all Ps > 0.1). The same was true for relative values of closest approach and response intensity and for female breeders, male breeders, and male helpers separately (all Ps > 0.1). Feeding share and exploration score Individuals with a higher feeding share did not have a higher or lower exploration score (both overall and within groups) than those with a lower feeding share. There was also no relationship between feeding share and exploration score for male breeders, female breeders, or male helpers separately or in pairs with or without helpers (Table 1). Defense behavior and exploration score Exploration score did not predict response to the intruder (Tables 2 and 3) or which birds sang or attacked during the simulated intruder trial (Wilcoxon rank sum test: sang: W = 634, P = 0.53; attacked: W = 385, P = 0.16). There was a relationship between exploration score and response to the novel object: within groups, relatively more exploratory birds responded more intensely to the novel object than relatively shyer group members but only when scored while others were present. For individuals scored alone, no such relationship was found (Pearson correlation: others present: r = 0.67, P = , no others present: r = 0.04, P = 0.82, Table 3, Figure 2). There was no relationship between exploration score and novel object response across groups. Other factors affecting defense behavior Apart from exploration score, several other factors played an important role in the response to both the intruder and novel object. Social context had a strong effect on approach distance and response intensity toward the simulated intruder: individuals scored in the presence of others approached the intruder more closely and also showed higher response intensity (Tables 2 and 3, Figure 3). This is also reflected in the fact that territory ID explained a significant amount of variation across groups (i.e., individuals responded more similarly compared with other group members than compared with individuals in other groups). Additionally, individuals scored in the presence of others were more likely to sing (often duets between breeders [personal observation], χ 2 = 13.59, P = ). However, the likelihood of an individual physically attacking the intruder did not depend on the presence of other group members (χ 2 = 1.14, P = 0.29). Nestling age had a strong effect on response toward the novel object. Adults with older nestlings approached the novel object more closely and showed higher response intensity toward it (Tables 2 and 3). Age of adult group members did not predict their response to the intruder or the novel object. (a) 2.0 Minimum distance (m) Relative response intensity Relative exploration score Figure 2 Relationship between relative exploration score and relative response intensity toward the novel object in cases where other birds were present (filled circles) and where no others were present (open circles). No Yes log (Response intensity) DISCUSSION Individual differences in coping style are thought to be associated with individual differences in life-history strategies (Stamps 2007; Wolf et al. 2007; Réale et al. 2010). However, to date, there are few empirical tests relating coping style (typically scored in isolation) to behavioral specialization in the wild (typically in a social context). Here, we tested for the presence of individual task specialization or individual variation in cooperativeness within superb fairy-wren social groups. Additionally, we tested whether defense and brood care behaviors are related to social context and individual coping styles displayed in captivity. Contrary to our expectations, we did not find evidence for task specialization or individual differences in cooperativeness. However, (b) Others present Figure 3 (a) Minimum approach distance (in meters) and (b) response intensity (logtransformed) toward the simulated intruder for birds scored without and with other group members present (including only birds that came within 2 m of the intruder ). Boxes show median and 25th to 75th percentiles. Whiskers extend to 1.5 times the interquartile range and circles represent outliers. No Yes

9 van Asten et al. Fairy-wren coping style, brood care, and defense 1753 we did find evidence for stronger nest defense behavior by relatively more exploratory individuals in a social context. Finally, the presence of other group members stimulated defense behavior against a conspecific intruder, whereas birds attending nests with older nestlings responded more intensely toward a novel object near the nest. Do fairy-wrens show task division or individual differences in cooperativeness? Defense and nestling provisioning were uncorrelated in superb fairy-wrens, suggesting that individuals do not specialize in certain tasks or differ in cooperativeness when it comes to brood care. This contradicts the idea that group living gives rise to task division or social niche specialization (Bergmüller and Taborsky 2010; Montiglio et al. 2013). Links between brood care and defense may be disrupted if high rates of extra-group paternity in superb fairywrens (Mulder et al. 1994; Dunn and Cockburn 1996) cause individual differences among males in brood care (Dunn and Cockburn 1996), but not defense. Indeed, an earlier study showed that a high proportion (49%) of offspring in our population are sired by extragroup males (Bain et al. 2014). Female breeders are the group members most related to the offspring they care for, and they indeed had a higher feeding share than males and were also more consistent in the intensity with which they responded toward intruder and novel objects near the nest. Nevertheless, we found some evidence of personality-dependent task division when multiple individuals were present in the same place at the same time: response intensity toward the novel object was related to exploration score only in the presence of others. When alone, individuals may behave more flexibly and set priorities based on external factors such as nestling age in the case of inspecting a novel object. In the current study, we had no control over the number of birds present near the nest at any time, and as a consequence, birds could be scored alone during the intruder trial and with others in the novel object trial or vice versa. If task division indeed only occurs where more than 1 individual is present, the difference in social context (alone vs. others present) between intruder and novel object trials could have prevented us from finding cross-contextual behavioral correlations. In other studies that have found individual task specialization, focal individuals were always accompanied by other group members (e.g., Arnold et al. 2005; Grinsted et al. 2013). Interestingly, in a study on cichlids, Bergmüller and Taborsky (2007) only found task specialization in helpers when breeders were present, but not when helpers were tested alone. This study, like ours (see below), therefore shows that social context plays an important role in task division; individuals likely make different behavioral decisions depending on whether other group members are present or not. Are brood care and defense related to coping style? Response to the intruding, taxidermically mounted fairy-wren was generally much stronger than to the novel object and was often accompanied by singing and attacking, likely because the intruder was a much more threatening stimulus than the novel object. If territory defense is indeed a high-priority task, this may explain why we did not find a relationship with exploration behavior, as any group member that appears will contribute. However, in other species, more proactive individuals are often also more aggressive toward conspecifics (e.g., Koolhaas et al. 1999; Bergmüller and Taborsky 2007; Amy et al. 2010). One possibility is that the proximity to the nest or the time of year evoked a strong response toward the intruder by all group members and that coping stylerelated differences in territory defense only become apparent near the territory boundary. Alternatively, because we only had access to juvenile models, the simulated intruder could have constituted different levels of threat to different group members. Female breeders may be less tolerant of immigrant juveniles (usually early dispersing female offspring; Cockburn et al. 2003) than males, leading to sex-related motivation to respond to the intruder, obscuring an underlying relationship between coping style and territory defense. In our study, however, this was likely not the case, as response to the intruder was not sex- or role dependent. Nest defense was related to relative exploration score (withingroup effect, scenario in Figure 1b), with relatively more exploratory individuals investigating the novel object in the presence of others. However, exploration scores did not predict response intensity when birds were alone, highlighting the importance of social context (discussed further below). Responses to the novel object were more investigative (perhaps reflecting neophilia or vigilance) than responses to the intruder : the songs and attacks elicited by the intruder were virtually absent during novel object presentation. The within-group effect is in line with the idea that task division by coping style may only occur when more than 1 individual is present and the potential threat is not severe (see above). Our results have to be interpreted with some care, however, as we were unable to measure individual repeatability in defense behaviors due to relatively low rates of nest success and changing nest locations and group compositions between breeding attempts. A long-term study with large sample size is needed to tease apart effects of group composition, social context, nest location, and other environmental factors that can affect individuals defense behaviors. Theory predicts a link between coping style and parental investment (Réale et al. 2010), but we did not find a relationship between exploration score and feeding share, although provisioning behavior was repeatable. Since provisioning rates depend on both motivation to feed nestlings and foraging efficiency (Westneat et al. 2011), a relationship between coping style and feeding share could be obscured if these components are differently affected by coping style. For example, foraging efficiency can depend on individual differences in risk taking or thoroughness in searching for food (Sih et al. 2004; Cole and Quinn 2011). Results from other studies on the relationship between parental provisioning and exploration have yielded mixed results (Patrick and Browning 2011; Mutzel et al. 2013; Burtka and Grindstaff 2015). In blue tits (Cyanistes caeruleus), for example, sex-specific relationships between personality traits and nestling provisioning were found (Mutzel et al. 2013). We did not find any sex- or role-dependent relationship between exploration and feeding rate. Conflicts of interest between group members can vary strongly with the high rates of extra-group paternity observed in superb fairy-wrens (Dunn and Cockburn 1996), but those intricate relationships were beyond the scope of this study. Overall, a direct relationship between coping style and feeding share does not seem to exist in our population. Social context and defense behavior Social context played an important role in how individuals responded to both intruder and novel object. Individuals scored in the presence of other group members especially responded much more strongly toward the intruder (closer approach, higher intensity, and more frequent singing). This confirms the results of earlier studies showing the impact of the presence of conspecifics