ORIGINAL PAPER

Dominance, not kinship, determines individual positionwithin the communal roosts of a cooperatively breeding bird

Clare J. Napper & Stuart P. Sharp & Andrew McGowan &

Michelle Simeoni & Ben J. Hatchwell

Received: 17 May 2013 /Revised: 17 July 2013 /Accepted: 22 July 2013 /Published online: 9 August 2013# Springer-Verlag Berlin Heidelberg 2013

Abstract Kin selection has played an important role in theevolution and maintenance of cooperative breeding behaviourin many bird species. However, although relatedness has beenshown to affect the investment decisions of helpers in suchsystems, less is known about the role that kin discriminationplays in other contexts, such as communal roosting. Individualsthat roost communally benefit from reduced overnight heatloss, but the exact benefit derived depends on an individual'sposition in the roost which in turn is likely to be influenced byits position in its flock's dominance hierarchy. We studied theeffects of kinship and other factors (sex, age, body size andflock sex ratio) on an individual's roosting position and dom-inance status in captive flocks of cooperatively breeding long-tailed tits Aegithalos caudatus. We found that overall, kinshiphad little influence on either variable tested; kinship had noeffect on a bird's position in its flock's dominance hierarchy andthe effect of kinship on roosting position was dependent on thebird's size. Males were generally dominant over females andbirds were more likely to occupy preferred roosting positions ifthey were male, old and of high status. In this context, the effectof kinship on social interactions appears to be less important

than the effects of other factors, possibly due to the complex kinstructure of winter flocks compared to breeding groups.

Keywords Aegithalos caudatus . Cooperative breeding .

Long-tailed tit . Dominance . Roost . Kinship

Introduction

Group-living is common throughout the animal kingdom andconfers many benefits in terms of increased foraging efficiencyand reduced predation. However, group members also incurvarious costs through competition with one another (KrauseandRuxton 2002). In some species, the process of kin selection(Hamilton 1964; Maynard Smith 1964) may allow individualsliving in groups with their relatives to mitigate some of thesecosts and enhance the benefits of group-living (Ekman et al.2004). One way in which this can occur is through nepotisticbehaviours within a group that reduce the costs of competitionbetween group members (Sherman 1977; Griesser and Ekman2005). Indeed the benefits of associating with kin might giverise to philopatry and kin-based sociality, potentially playing akey role in the evolution of cooperative breeding systems(Stacey and Ligon 1991; Ekman et al. 2004; Covas andGriesser 2007). In such systems, there has been intensive studyof the role of kinship in determining the investment decisionsof helpers (e.g. Dickinson 2004; Covas et al. 2006; Nam et al.2010; Wright et al. 2010), but much less is known about theeffect of kinship on interactions during the non-breeding sea-son. However, during this time, there are many potentiallyimportant contexts for kin discrimination to occur, includingspace use (Hatchwell et al. 2001), group defence against pred-ators (Austad and Rabenold 1985), foraging (Kaib et al. 1996)and communal roosting (McGowan et al. 2007).

Communal roosting behaviour has evolved independentlyin several bird lineages (Beauchamp 1999), some of whichinclude cooperatively breeding species (Chaplin 1982; Ligon

Communicated by J. A. Graves

Electronic supplementary material The online version of this article(doi:10.1007/s00265-013-1613-7) contains supplementary material,which is available to authorized users.

C. J. Napper (*) :M. Simeoni :B. J. HatchwellDepartment of Animal & Plant Sciences, University of Sheffield,Western Bank, Sheffield S10 2TN, UKe-mail: c.j.napper@sheffield.ac.uk

S. P. SharpLancaster Environment Centre, Lancaster University, Lancaster LA14YQ, UK

A. McGowanCentre for Ecology and Conservation, University of Exeter, CornwallCampus, Penryn, Cornwall TR10 9EZ, UK

Behav Ecol Sociobiol (2013) 67:2029–2039DOI 10.1007/s00265-013-1613-7

et al. 1988; du Plessis et al. 1994). The main function ofcommunal roosting is probably the thermoregulatory benefitof reduced heat loss, with individuals that roost communallylosing less mass overnight than solitary birds (McKechnie andLovegrove 2001; du Plessis 2004). Birds that roost commu-nally may also be less likely to suffer from predation thanthose that do not (Weatherhead 1983; Eiserer 1984). However,the benefits that an individual gains from communal roostingare likely to depend on the individual's position in the roost,which in turn may depend on factors such as age, sex, bodysize and dominance status (e.g. Swingland 1977; Feare et al.1995; Adams et al. 2000; Calf et al. 2002). In species that livein groups consisting of individuals of varying relatedness toone another, an individual's position may also depend on itskinship to the rest of the group. Previous studies of coopera-tively breeding birds have shown that the individuals occupy-ing the peripheral positions at the ends of linear roosts are thetwo most dominant individuals in the group, e.g. jungle bab-blers Turdoides striatus (Gaston 1977), varied sittellasDaphoenositta chrysoptera (Noske 1985) and Arabian bab-blers Turdoides squamiceps (Zahavi 1990; Bishop and Groves1991). Dominant individuals in these species will therefore belikely to accrue lower thermoregulatory benefits overnightand to be subject to a greater risk of predation than theirsubordinates (Weatherhead 1983). Such apparently coopera-tive behaviour might be expected in groups that are made upof close relatives as it allows the dominant individuals' off-spring to occupy less costly positions on the inside of theroost, increasing their chances of survival and therefore thedominant birds' fitness.

In this study, we tested the hypothesis that kinship deter-mines an individual's position in the communal roosts ofcooperatively breeding long-tailed tits Aegithalos caudatus.Long-tailed tits spend the non-breeding season in mixed-sexflocks usually comprising 5–20 individuals. Flocks typicallycontain both adults and juveniles from two or more nuclearfamilies as well as a proportion of unrelated immigrants.These immigrants disperse between flocks during their firstwinter and account for approximately one third of every flock(Hatchwell et al. 2001; McGowan et al. 2007). Flocks breakdown during the breeding season (March–June), when allbirds initially attempt to breed in monogamous pairs; cooper-ation occurs when failed breeders become helpers at the nestof another pair, assisting them in feeding nestlings and fledg-lings (Hatchwell et al. 2004). Long-tailed tits can recognisetheir kin using vocalisations that they learn in the nest (Sharpet al. 2005) and helping behaviour in this species is kin-biasedwith the majority of helping occurring between brothers(Russell and Hatchwell 2001; Nam et al. 2010).

During the non-breeding season, long-tailed tit flocks roostin tight linear huddles. Previous studies have shown that indi-viduals in the middle of the huddle lose less mass overnightthan those on the outside (Hatchwell et al. 2009) and that there

is competition for these preferred central positions within aroost (McGowan et al. 2006). The outcome of this competitionis a function of an individual's dominance status within theflock, and contrary to studies on other cooperatively breedingspecies, the outer positions in long-tailed tit roosts, which arecostly in thermoregulatory terms, are occupied by subordinates(McGowan et al. 2006). The factors affecting an individual'sstatus are unknown in this species, but kinship plays a prom-inent role in their social organisation both during the breeding(e.g. Russell and Hatchwell 2001; MacColl and Hatchwell2004; Nam et al. 2010) and non-breeding (Hatchwell et al.2001) seasons so we hypothesised that status and thereforeroosting position would be influenced by an individual's relat-edness to other members of their flock. Several studies haveshown that there are fitness benefits to associating with closekin rather than unrelated individuals and that this can be due tonepotistic behaviours within a group (e.g. Hoogland 1983;Griesser and Ekman 2005; Dickinson et al. 2009). McGowanet al. (2007) showed that non-kin are able to join family flocksand concluded that failed breeders do not help in order to gainaccess to a winter flock per se. However, nepotism may stilloccur at a more subtle level and birds with relatives in the flockmay gain access to the preferred central positions within aroost, thereby increasing their chances of over-winter survival,while unrelated immigrants might be forced to occupy themore costly outer positions. This is particularly likely if highstatus is a direct benefit of helping behaviour since helpers inthis species are usually related to the brood they raise andsubsequent flock they join (Russell and Hatchwell 2001).The principal objectives of this study were to use captive flocksof long-tailed tits to investigate behavioural interactions amongflock members to determine the effect of kinship and otherfactors (sex, body size, age and flock sex ratio) on (1) anindividual's position within a roost and (2) an individual'sstatus within the dominance hierarchy of a flock.

Methods

We studied the roosting behaviour of 18 temporarily captiveflocks of long-tailed tits between October and January 2000–2002 (N=8 flocks) and 2004–2006 (N=10 flocks) entireflocks of variable size (1 of 5 birds, 2 of 6 birds, 6 of 7 birds,3 of 8 birds and 6 of 9 birds; total=137 birds) were captured inmist-nets from colour-ringed populations in Melton Wood,Doncaster, UK (53°31′N, 1°13′W; N=7 flocks) and theRivelin Valley, Sheffield, UK (53°23′N, 1°34W; N=4 flocks)or from unringed populations in the vicinity of Sheffield, UK(N=7 flocks). Flocks were transported to the Department ofAnimal and Plant Sciences, University of Sheffield, UK by carin cloth bags and were housed in outdoor aviaries (3×3×2 min 2000–2002 and 3×1×2 in 2004–2006) that provided pro-tection from rain and some wind (although birds were exposed

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to ambient temperatures). Aviaries were supplied with numer-ous perches, branches and a max/min thermometer. Birds werefed ad libitum with wax moth larvae Galleria mellonella,mealworms Tenebrio molitor and crickets Gryllus bimaculatusand water was provided for drinking and bathing at all times.

Observations of communal roosts

Observations began once flocks had been allowed to accli-matise to captivity for 48–72 h. Roosting behaviour wasrecorded using a video camera with an infrared night visionfunction (Sony CCD-TR427E) positioned above a roostingperch. In 2000–2002, the perch was placed in an open-fronted wooden roosting box (1.2×0.5×0.8 m) in the aviary.However, flocks did not always choose to roost on theroosting perch, so in 2004–2006, the birds were moved to asmaller cage (0.4×0.5×0.3 m) containing the roosting perchshortly before dusk and released back into the aviary atdawn. Video recordings showed that roosting behaviourdid not differ between the two techniques (McGowan et al.2006), so data were pooled for the analyses presented here.

All birds were uniquely colour-ringed but since the ringscould not be seen from overhead during roost formation, a5×5-mm black label was stuck to the tips of the birds' crownfeathers using non-toxic glue. Each label was uniquelymarked with white enamel paint to allow birds to be individ-ually identified and their position in the roost to be deter-mined. Labels were removed before the birds' release at theend of the observations and, although the tips of some crownfeathers were clipped, there was no visible effect on the birds'appearance. The behaviour of birds towards conspecifics wasunaffected by the addition of the labels.

In 2000–2002, flocks were filmed for a 4-h period arounddusk (1 h before and 3 h after) and for a further 4 h arounddawn (2 h before and 2 h after). This ensured that all move-ments during roost formation and breakup as well as finalroost positions were recorded. After an initial period of birdsjockeying for position and relocating, positions were stablethroughout the night (McGowan et al. 2006); so in 2004–2006, roosts were filmed for only 1.5 h around dusk since thiswas sufficient to allow interactions during roost formationsand final roost positions to be recorded. Roosts were filmedfor up to seven nights per flock, and roosting positions withinlinear huddles were known with certainty for all individualsfor a mean of 3.61±1.75 SD nights per flock (N.B. on a fewoccasions, one or more individuals chose to roost separatelyfrom the main huddle, or marks on labels could not beclearly discerned; in either case, data from those nightswere excluded from analyses). Positions were defined as‘outer’ (positions on the ends of the linear huddle) or‘inner’ (the remaining positions in which all birds had atleast one bird on either side during roosting). The majority ofbirds (80.3 %, N=137) occupied the same roosting position

(i.e. outer or inner) on all nights of observation so eachindividual was assigned to the position that they occupiedthe most frequently for analyses.

Dominance hierarchies

The dominance hierarchy within each flock was determinedfrom video recordings of aggressive interactions during roostformation (in the form of pecks) and by direct observation ofinteractions over food. During roost formation, pecks wereusually aimed at the nape of the victim, allowing victims andaggressors to be identified unambiguously. Pecks occur regular-ly during interactions among flock members in the wild (CJNand BJH, personal observation) and did not lead to bleeding orloss of feathers in the captive birds. Interactions over foodconsisted of ‘tugs of war’ over a food item and the aggressorwas the bird that was initially without food while the victim wasthe one initially with food. The winner was the bird that obtainedthe food item. No bird was deprived of food as a result of thesecontests. The number of aggressive interactions observed in thetwo contexts varied widely between flocks but there was ahighly significant correlation between the dominance hierarchygenerated from pecks and that generated from interactions overfood (McGowan et al. 2006). Therefore, all pairwise interactionswere combined and a linear dominance hierarchy wasconstructed for each flock, with the individual that won thegreater proportion of aggressive interactions in the dyad beingdominant. Each individual was then assigned a dominance scoreaccording to their position in the dominance hierarchy withintheir flock. The most subordinate individual within a flockreceived a score of 0 and the most dominant a score of 1 andall other birds between received a score according to their rankrising in increments of 1/(N−1) where N=flock size. Therefore,a flock of seven individuals had scores of 0, 0.17, 0.33, 0.5, 0.67,0.83 and 1. In some cases, the positions of two individuals in thehierarchy could not be separated (for example if they had equalscores), and in these cases, both individuals received the meanscore of the adjacent positions. In other instances, interactionswere not observed between two flock members (16.4 % ofpossible dyads), in which case we assumed transitivity, i.e. ifAwas dominant over B and B over C, then Awas also dominantover C. Comparison of generalised linear mixed models(GLMMs) with and without ‘dominance score’ fitted as a pre-dictor and in which ‘flock identity’ was fitted as a random termshowed that there was no effect of dominance status on thenumber of aggressive interactions an individual was involved in(GLMM: χ2=0.12, df=1, P=0.735). Two individuals weremarginally more likely to interact if they were unrelated(GLMM: χ2=3.49, df=1, P=0.062), but the relationship be-tween number of dyadic interactions and kinship was not sig-nificant after an extreme outlier where an unusually high numberof pecks occurred between two unrelated individuals was re-moved (GLMM: χ2=2.69, df=1, P=0.101).

Behav Ecol Sociobiol (2013) 67:2029–2039 2031

Genetic analysis

Blood samples (approximately 10 μl per bird) were takenfrom all birds by brachial venipuncture under UK HomeOffice Licence. Genomic DNA was extracted from bloodsamples and amplified as previously described (Simeoniet al. 2007). Individuals were sexed using standard moleculargenetic techniques (Griffiths et al. 1998) and genotyped atnine microsatellite loci (Ase18, Ase37, Ase64, Hru2, Hru6,LOX1, Pca3, Pma22 and Ppi2; mean number of alleles=17.8,range 7–42) selected from the 20 polymorphic loci identifiedby Simeoni et al. (2007). Queller and Goodnight's (1989)coefficient of relatedness of flock members, r, was calculatedusing SPAGeDi 1.3 (Hardy and Vekemans 2002). Nam et al.(2010) and Simeoni (2011) showed that estimated r closelymatched pedigree relatedness in two of the populations fromwhich our study flocks were captured, but the extent to whichestimated r reflected true relatedness could not be directlytested for the sample of birds used here because in the largemajority of cases pedigree information was not available.Nevertheless, estimated r should provide a close approxima-tion of relatedness in our sampled birds.

Statistical analyses

We adopted two approaches to investigate the effect of kinshipon interactions within a flock. Firstly, we investigated the effectof kinship, dominance status, sex, body size, age and flock sexratio on an individual's position in the roost using GLMMs,and secondly, we examined the effect of kinship, sex, bodysize, age and flock sex ratio on an individual's status within itsflock using general linear models (GLMs). We then conductedmodel selection and averaging based on AICc (Akaike'sInformation Criterion corrected for small sample size).

Model fitting

To investigate the effect of kinship on an individual's positionwithin the roost, we fitted GLMMs with a binomial errordistribution and logit link function using the function ‘lmer’in the R package ‘lme4’ (Bates and Maechler 2010).‘Position’ was used as the response term in this analysis and‘flock identity’ was fitted as a random term in all models tocontrol for the presence of multiple individuals belonging tothe same flock. An individual's ‘kinship’, ‘dominance’ score,‘sex’, body ‘size’ and ‘age’ and the ‘sex ratio’ of the flockwere fitted as predictor variables, as well as all biologicallymeaningful first-order interactions.

‘Position’ was defined as ‘outer’ (positions on the ends ofthe linear huddle) or ‘inner’ (the remaining positions in whichall birds had at least one bird on either side during roosting)while ‘kinship’ was defined as an individual's average relat-edness to the rest of the flock as determined by molecular

genetic analysis. Similar results were obtained when an indi-vidual's kinship to the rest of the flock was defined as theproportion of the rest of the flock that were close relatives(r≥0.2) or the presence or absence of a close relative (r≥0.2)in its flock (for statistics see Online Resources 1 to 4).‘Dominance’ status was defined as a bird's dominance scoreas described above. Many of the birds in our captive flockswere of unknown age at the time of capture, either becausethey were immigrants into our study populations or becausethey were captured from unringed populations. Measurementsof known-age birds in a long-term study population in theRivelin Valley, Sheffield, show that adult long-tailed tits havelonger wings than juveniles (Welch's two sample t test:t107.5=4.961, P<0.001) while tarsus length remains relativelyconstant throughout a bird's life (Welch's two sample t test:t91.4=−0.739, P=0.462). Therefore, because it was not possi-ble to determine a bird's age directly, we used wing length as aproxy for ‘age’ while tarsus measurements were used as ameasure of body ‘size’. We did not attempt to place birds ofunknown age into age classes based on their wing length forthis analysis because although adults generally have longerwings than juveniles, there is considerable overlap betweenthe wing lengths of the two classes. Since wing length andtarsus length are likely to be correlated, we assessed colinear-ity between all input variables using variance inflation factors(VIFs) modified for mixed models. No variable had a VIF ofgreater than 3, so all traits were considered sufficiently inde-pendent to be treated separately in the analysis. The ‘sex ratio’of a flock was calculated for each individual when that indi-vidual was not included in the flock. For example, a flockcontaining six males and seven females would have a sex ratioof 0.42 for a male (5/12) and 0.5 for a female (6/12). If a birdof unknown sex was present in a flock (N=3 birds), the sexratio for all individuals in that flock was calculated with thisindividual excluded from the flock.

To investigate the factors affecting an individual's status inits flock's dominance hierarchy, we fitted GLMs with aGaussian error distribution as there was no longer a need tocontrol for the presence of multiple individuals in the sameflock since a separate dominance hierarchy was calculated foreach flock and all flocks had an identical distribution ofdominance scores (identical results were obtained when theanalysis was performed using GLMMs with ‘flock identity’fitted as a random effect). ‘Dominance’ score was used as theresponse term in the analysis and kinship, sex, sex ratio, ageand body size were fitted as predictor variables, as well as allbiologically meaningful first-order interactions. As above,kinship was defined as an individual's average relatedness tothe rest of the flock as determined by molecular geneticanalysis, sex ratio was calculated for each individual whenthat individual was not included in the flock, wing length wasused as a proxy for age and tarsus length as a measure of bodysize. These models were fitted using the data set as a whole as

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well as separately for each sex with sex removed as a predictorsince flock sex ratio might affect the dominance status ofmales and females differently.

For both analyses, all input variables were standardisedusing the function available in the R package ‘arm’ (Gelmanet al. 2012) to allow the direct comparison of the effect sizeestimates of the fixed effects as well as the interpretation of themain effects involved in any interactions (Schielzeth 2010).

Model selection and averaging

For each analysis, we generated a set of candidate modelscontaining all possible combinations of the predictor variablesdefined above. Candidate models were then ranked usingAICc and models within two AICc of the top model weredeemed to have considerable support and selected for modelaveraging (Burnham and Anderson 2002). A final model wasthen obtained by averaging parameter estimates from thesemodels according to their Akaike weights using the R package‘MuMIn’ (Barton 2012). The relative importance of eachexplanatory variable in the final model was calculated as asum of all the model weights in which that variable appears sothat if a variable appeared in all models it would have arelative importance of one. All statistical analysis was carriedout in the R environment, v 2.12.0 (R Development CoreTeam 2010). Means are reported as ±SD.

Ethical note

All birds were weighed shortly after capture and again justbefore release at the site of capture. The majority of birds(86 %, N=137) gained mass during the period of captivity(7–10 days) and no bird lost more than 10 % of its body massduring this time (mean mass loss=0.317 g). This is well withinthe range of expected mass lost overnight by this species(Hatchwell et al. 2009). Birds that lost mass were released fromcaptivity early while their weight was still within the normalrange for this species. All birds were released with at least oneother member of their flock. All of the birds from our long-termstudy population in the Rivelin Valley, Sheffield, UK that werereleased early (N=4) were observed breeding in the study sitein the breeding season following release so any weight loss thatdid occur during captivity did not appear to have any long-termadverse effects. Only data collected when the whole flock waspresent were used in analyses. With the exception of the releaseof birds that lost weight, flock composition was not alteredfrom that at capture during the period of captivity.

Birds were released in the mid-morning at the site of capturefollowing BTO ringers' guidelines (Redfern and Clark 2001) forthe release of birds as specified by our project licence. Thecondition of all birds was inspected before release; BJH hasbeen approved by the University of Sheffield veterinary officerto release birds into the wild. After release, flocks were

monitored until they had begun to forage and had resumednormal behaviour. The majority of colour-ringed birds that werereleased back into our study population in the Rivelin Valley,Sheffield, UK (75 %, N=24) bred following release. Therefore,temporary captivity did not have any obvious impact on survivalsince adult long-tailed tits have an approximately 55 % chanceof surviving between years (McGowan et al. 2003) and roughly40 % of the birds in our captive flocks were juveniles thatusually disperse away from the study site before breeding.

Results

The average coefficient of relatedness estimate, r, of an individ-ual to the rest of their flock was 0.164±0.135 (range=−0.158 to0.527) across the 137 birds in the 18 flocks used in the analyses.The GLMM analysis showed that kinship to the rest of the flockis an important predictor of roosting position and appeared in allmodels within two AICc of the top model (Table 1). Birds ofhigher average relatedness to the rest of the flock were morelikely to occupy inner positions than those with low averagerelatedness. However since the 95 % confidence interval rangesfor the effect of kinship included zero and the effect size ofkinship was relatively small, there is little evidence that kinshipalone has a strong effect on roosting position. The effect ofkinship to the rest of the flock on an individual's position inthe roost was also strongly dependent on an interaction withbody size; larger birds were found in favoured inner positionswhen they had a high average relatedness to the rest of the flock,whereas smaller birds were more likely to occupy inner posi-tions when they had fewer relatives in the flock.

Roosting position was also influenced by sex and dominancestatus; females occupied outer positions much more frequentlythan males (Fig. 1a), and individuals of high status were morelikely to occupy inner positions. Furthermore, sex and domi-nance interacted to determine a bird's position in the roost; bothsexes were more likely to occupy inner positions if they were ofhigher status but this effect was stronger for males than forfemales, so that the only males observed in outer positions wereof very low status (Fig. 1b). Roosting position was alsoinfluenced by a bird's age (Table 1); older birds were more likelyto occupy inner positions than younger birds although the effectof age was partly determined by a weak interaction with the sexratio of the rest of the flock. Finally, there were further weakeffects (the 95 % confidence interval ranges included zero andeffect sizes were relatively small) of sex ratio and body size onroosting position as well as weak interactions between body sizeand sex, dominance score, sex ratio and age (Table 1). With theexception of body size, these effects were relatively unimportantand the explanatory variables did not appear in every modelwithin two AICc for the top model (Table 1). The mean (±SD)of each of the continuous variables tested for birds in inner andouter positions is displayed in Table 2.

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Kinship had no effect on an individual's status in aflock's dominance hierarchy, either when all birds wereincluded in the analysis or when each sex was treatedseparately, and kinship did not appear in any of the modelswithin two AICc of the top model in all three analyses(Table 3). Although there were weak effects of sex ratio,body size and age on an individual's status when all birdswere included in the analysis, the variable that had thegreatest effect on status was sex (Table 3) with malesgenerally being dominant over females (mean dominancescore for males=0.579±0.310 and females=0.387±0.323).The effect of sex was also strongly influenced by an inter-action with body size (Table 3).

When data were analysed separately for each sex, thedominance score of males increased with both their body sizeand age (Table 3). Age and size also interacted to determinemale status (Table 3). However, none of the explanatoryvariables tested were likely to have a strong effect on anindividual's status since all 95 % confidence interval rangesincluded zero (Table 3). For females, unsurprisingly, the meandominance score tended to decrease as the sex ratio of flocksbecame more male-biased (Table 3). Female dominance alsotended to increase with age, but in contrast to the effect inmales, status was relatively independent of body size althoughthere was an interaction between these two factors (Table 3).However, as for males, the 95 % confidence intervals includezero for all of these effects, suggesting that their influence ondominance was marginal.

Discussion

We have identified several factors that influenced roostingposition in long-tailed tits. First, kinship to other members of

the flock had a weak effect on the roosting position occupiedby an individual long-tailed tit, although the nature of thiseffect depended on the bird's size, as measured by tarsuslength; birds of high average relatedness to their flock weremore likely to gain access to preferred inner positions in theroost if they were larger. Second, an individual's roostingposition was also determined by sex and dominance. Asreported by McGowan et al. (2006), females and birds oflow status were more likely to roost in outer positions.Again, there was an interaction between these two factors,and only very subordinate males were found in outer posi-tions. Third, using a proxy for age (wing length), our resultssuggest that outer positions were more likely to be occupiedby young birds. By contrast, we found no indication thataverage kinship to other flock members influenced an indi-vidual's position within a flock's dominance hierarchy, but, asfor roosting position, sex was a significant factor in determin-ing status, with females' mean dominance score also decreas-ing as flocks became more male-biased.

Overall, kinship appears to have rather little influence onthe structure of long-tailed tit roosts and dominance hierar-chies. Any effect of kinship on roosting position was weak,and there was no effect of an individual's kinship to the rest ofthe flock on its position within the dominance hierarchy.These findings were contrary to expectations because thereis abundant evidence that kin selection has played a major rolein the evolution of this species' cooperative breeding system(Russell and Hatchwell 2001; MacColl and Hatchwell 2004;Sharp et al. 2005; Nam et al. 2010). There are several reasonswhy kinship may be a less important factor in interactionsoccurring during the non-breeding season than during breed-ing. First, during the breeding season, cooperative interactionsoccur among a small number of individuals (typical coopera-tive group size is three to five individuals) that are closely

Table 1 Parameter estimates,unconditional standard errors andrelative importance of explanato-ry variables affecting roostingposition after averaging across 16models within two AICc of thetop model

Model parameter Relative importance Estimate Unconditional SE Lower CI Upper CI

(Intercept) 1.952 0.478 1.015 2.889

Sex 1.00 1.739 0.792 0.185 3.292

Dominance 1.00 2.166 0.825 0.549 3.782

Kinship 1.00 0.806 0.655 −0.477 2.090

Sex ratio 0.66 −1.068 0.654 −2.350 0.213

Size 1.00 0.404 0.815 −1.193 2.002

Age 1.00 1.930 0.793 0.376 3.485

Sex × dominance 1.00 3.093 1.561 0.034 6.152

Sex × size 0.17 −1.697 1.430 −4.499 1.106

Dominance × size 0.29 2.022 1.607 −1.128 5.172

Kinship × size 1.00 3.798 1.725 0.417 7.179

Sex ratio × size 0.30 −1.736 1.116 −3.923 0.451

Sex ratio × age 0.42 −2.421 1.340 −5.047 0.204

Size × age 0.38 −2.252 1.571 −5.331 0.827

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related (Nam et al. 2010), whereas interactions within winterflocks involve many more individuals, some of whom may beclose kin, but many of whom are likely to be non-kin(Hatchwell et al. 2001; McGowan et al. 2007). Competition islikely within winter flocks (e.g. Bijleveld et al. 2012) and suchcompetitive interactions may have long-term consequences; forexample, communal roosting is thought to play a role in mateselection and pair formation in harriers (Wiacek 2010). In long-

tailed tits, competition could be particularly intense amongrelated, philopatric males to pair with unrelated females whohave dispersed into their flock. Under these circumstances, it isnot surprising that competitive, rather than cooperative, inter-actions dominate, as reported in the winter flocks of westernbluebirds Sialia mexicana (Dickinson et al. 2009).

Second, the non-breeding season flocks of long-tailed titsare unstable, fluid entities that may result from the merger oftwo or more nuclear family flocks, as well as including asubstantial proportion of immigrants, many of whom arelikely to have dispersed with kin (Sharp et al. 2008). Whensuch mergers and immigrations occur, there is no reason whyone particular kin-group should be able to assert dominanceover another kin-group or over groups of immigrants. Thiscontrasts with situations where immigrants disperse intosmall, stable family groups where they become subordinateto resident members of a kin-group, as observed in Siberianjays Perisoreus infaustus (Griesser et al. 2008). It is morelikely that as long-tailed tit flocks merge, dominants in eachflock will tend to retain high status and subordinates retaintheir lowly status in merged flocks, rather than one flock allasserting dominance over the other.

Finally, the importance of kinship in social interactions islikely to vary throughout the year. In this species, the contri-butions to inclusive fitness from independent breeding arehigher than those from helping (MacColl and Hatchwell2004). Since helpers in this species are failed breeders, theydo not sacrifice their own chances of breeding in order to help;however, a bird that gives up its roosting position to its relativemay decrease its chances of surviving the winter and breedingindependently. At this time of the year, therefore, any effect ofkinship on interactions might be less important than or con-founded by the effect of other factors. Indeed we have iden-tified many factors that were associated with dominance androosting position, which we now discuss.

The strongest predictors of roosting position were sex anddominance rank, with males and dominants occupying innerpositions more frequently than females and subordinates. Sexinfluences the outcome of diverse forms of competition, in-cluding that for preferred positions within roosts of Europeanstarlings Sturnus vulgaris (Summers et al. 1987), bramblingsFringilla montifringilla (Jenni 1993) and Andean condorsVultur gryphus (Donázar and Feijóo 2002), so the fact thatsex influences roosting position in long-tailed tits is consistentwith several previous studies. Individuals of higher statushave also been found to occupy preferred roosting positionsin other species, e.g. red-winged blackbirds Agelaiusphoeniceus (Weatherhead and Hoysak 1984), starlings(Feare et al. 1995) and bronze mannikins Lonchura cucullata(Calf et al. 2002), and it makes sense that dominant individ-uals can displace subordinates from the preferred positions ifthey want to. The finding that the roosting position of a male ismore dependent on its status than that of a female is probably

Fig. 1 The a frequency and b dominance scores (mean+SE) of males(black bars) and females (white bars) occupying inner and outer positionsin communal roosts across all 18 flocks of long-tailed tits in 2000–2002and 2004–2006

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an artefact of the effect of sex itself on position; males aremore likely to occupy inner positions than females so onlymales of very low status were found in outer positions, where-as a female with a relatively high dominance score may stilloccupy an outer position in a flock with a male-biased sexratio. This explanation is further supported by the weak effectof sex ratio on position: as the proportion of males in the flockincreased, the likelihood of a male occupying an outer posi-tion increased. In this context, it is also interesting to note thatthe mean dominance score of females decreased as flock sexratios became more male-biased.

The results of this study contrast with the findings of otherstudies on cooperatively breeding birds (Gaston 1977; Noske

1985; Zahavi 1990; Bishop and Groves 1991) that have allfound that dominant individuals occupy the least desirablepositions in the roost in terms of the thermoregulatory benefitsaccrued. In these species, groups are made up of parents andretained offspring that have remained on their parents' territoryafter fledging, so dominant parents were effectively giving upthe best roosting positions to their offspring. In contrast, therelatively weak kin structure of long-tailed tit flocks (seeabove) would be expected to lead to more intense competitioncompared to groups of more typical cooperative breeders,making it less beneficial for dominant individuals to give uppreferred roosting positions to subordinates, many of whichare unlikely to be relatives.

Table 2 Mean±SD of all variables tested across all flocks

Variable All birds Males Females

Inner (n=101) Outer (n=36) Inner (n=70) Outer (n=9) Inner (n=29) Outer (n=26)

Kinship 0.173±0.130 0.137±0.146 0.172±0.129 0.107±0.131 0.175±0.137 0.147±0.152

Sex ratio 0.577±0.189 0.631±0.195 0.578±0.193 0.710±0.195 0.574±0.182 0.604±0.191

Tarsus length (mm) 18.960±0.778 18.629±0.869 19.080±0.822 18.933±0.529 18.687±0.574 18.490±0.979

Wing length (mm) 61.755±1.267 60.470±1.376 62.231±0.981 60.889±1.833 60.704±1.235 60.375±1.173

Dominance score 0.573±0.301 0.303±0.320 0.624±0.290 0.228±0.232 0.440±0.298 0.329±0.346

Table 3 Results of general linearmodel analyses investigating theeffects of kinship, sex ratio, bodysize and age on an individual'sstatus in its flock's dominance hi-erarchy when all birds were in-cluded in the analysis and wheneach sex was treated separately.Parameter estimates were calcu-lated by averaging five modelswithin two AICc of the top modelwhen all birds were included inthe data set, three models whenthe dataset was limited to malesand five models when the data setonly included females

Model parameter Relative importance Estimate Unconditional SE Lower CI Upper CI

All birds

(Intercept) 0.805 0.043 0.720 0.891

Sex 1.00 0.212 0.099 0.016 0.408

Sex ratio 0.68 −0.056 0.080 −0.241 0.074

Size 1.00 0.086 0.087 −0.088 0.259

Age 1.00 0.123 0.101 −0.078 0.324

Sex × sex ratio 0.16 0.241 0.158 −0.073 0.554

Sex × size 1.00 0.577 0.228 0.125 1.030

Sex ratio × size 0.12 −0.154 0.149 −0.449 0.141

Sex ratio × age 0.36 0.298 0.167 −0.034 0.629

Size × age 1.00 −0.595 0.232 −1.055 −0.136

Males

(Intercept) 0.909 0.058 0.794 1.024

Size 1.00 0.168 0.112 −0.056 0.393

Age 0.59 0.095 0.114 −0.133 0.323

Size × age 0.35 −0.441 0.258 −0.956 0.074

Females

(Intercept) 0.653 0.063 0.526 0.780

Sex ratio 0.70 −0.226 0.121 −0.470 0.018

Size 1.00 −0.035 0.135 −0.307 0.238

Age 0.53 0.159 0.133 −0.109 0.426

Size × age 0.38 −0.508 0.279 −1.073 0.058

2036 Behav Ecol Sociobiol (2013) 67:2029–2039

The other important factor implicated as a determinant ofroost position was age; older long-tailed tits were much morelikely to occupy inner positions in the roost than youngerbirds. Unfortunately, we did not know the age classes (i.e.adult or juvenile) of most birds in our sample but used winglength as a proxy for age. There is some sexual size dimor-phism in long-tailed tits, males being larger than females (Namet al. 2011), but this age effect was in addition to the effect ofsex, suggesting that young females in particular are likely toroost in peripheral positions. Age has been found to have asimilar effect on roosting position in starlings (Summers et al.1987) and condors (Donázar and Feijóo 2002).

The variable with the greatest effect on an individual'sstatus within its flock was sex, males generally being domi-nant over females. This pattern was reported for long-tailedtits using a subset of the current data by McGowan (2002),and it is widespread in other species (e.g. Richner 1989;Donázar and Feijóo 2002). The status of males tended toincrease if they were larger (Table 3), as found in other species(e.g. Tokarz 1985; Richner 1989; Schuett 1997). One of thebehavioural contexts in which dominance was assessed in ourstudy involved physical competition over food items, theoutcome of which is probably determined by an individual'sstrength or size. In both sexes, analyses also suggested thatstatus was a function of the interaction between size (tarsuslength) and age (wing length). However, we treat these inter-actions with some caution for two reasons. First, wing lengthprovides only an approximation of age, as described above.Secondly, the 95 % confidence intervals for these resultsincluded zero, suggesting that the effects are, at best, weak.

A notable difference between the findings of this study andof many previous studies of factors affecting dominance statusin birds is that status in long-tailed tits is influenced by acombination of interacting variables. This contrasts withRichner (1989), for example, who found that in winter flocksof carrion crows Corvus corone males were dominant overfemales, then within each sex adults were dominant overjuveniles and within each age-sex class the largest birds weredominant. Such well-defined hierarchies are clearly not thecase for long-tailed tits; some females are dominant over males,some juveniles are dominant over adults and some smallerbirds are dominant over larger ones. Again, this is likely to beattributable to the relatively large flock sizes of long-tailed titsand their variation in composition through time (Hatchwellet al. 2001).

Finally, another major factor that could affect roosting posi-tion and dominance status in long-tailed tits that we did notconsider here due to lack of available data is social familiarity.For example, it is possible that birds that have recently joinedthe flock or who were not present in the flock during theprevious non-breeding season are subordinate or occupy outerpositions in the roost. Previous breeding status and socialfamiliarity during the breeding season might also influence

non-breeding interactions, for example, helpers might bemore familiar to the family they helped than other relativesand given higher status because of this. Therefore, it wouldbe interesting to use a measure of social association betweenflock members as well as kinship to further investigate thefactors affecting roosting position and dominance status incommunally roosting species.

Acknowledgments We thank numerous landowners includingDoncas-ter and Sheffield City Councils, Yorkshire Water and Hallamshire GolfClub for allowing us to catch and watch birds on their land.We also thankthe NERC Biomolecular Analysis Facility in Sheffield for access to thelab and expertise, numerous undergraduates for their assistance withbehavioural observations and two anonymous reviewers who providedhelpful comments on an earlier version of this paper. Financial support forthis study was provided by the Natural Environment Research Council, towhich we are most grateful.

Ethical standards This study complied with the laws of the UK.Temporary housing of birds in captivity and all observations were conductedunder English Nature licence (Project licence numbers 20053050 and20021791) and facilities for housing birds complied with UK HomeOffice regulations.

Conflict of interest The authors declare that they have no conflict ofinterest.

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