Behav Ecol Sociobiol (2013) 67:2029–2039 DOI 10.1007/s00265-013-1613-7
ORIGINAL PAPER
Dominance, not kinship, determines individual position within 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 the evolution and maintenance of cooperative breeding behaviour in many bird species. However, although relatedness has been shown to affect the investment decisions of helpers in such systems, less is known about the role that kin discrimination plays in other contexts, such as communal roosting. Individuals that roost communally benefit from reduced overnight heat loss, but the exact benefit derived depends on an individual's position in the roost which in turn is likely to be influenced by its position in its flock's dominance hierarchy. We studied the effects of kinship and other factors (sex, age, body size and flock sex ratio) on an individual's roosting position and dominance status in captive flocks of cooperatively breeding longtailed tits Aegithalos caudatus. We found that overall, kinship had little influence on either variable tested; kinship had no effect on a bird's position in its flock's dominance hierarchy and the effect of kinship on roosting position was dependent on the bird's size. Males were generally dominant over females and birds were more likely to occupy preferred roosting positions if they were male, old and of high status. In this context, the effect of kinship on social interactions appears to be less important
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. Hatchwell Department of Animal & Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK e-mail:
[email protected] S. P. Sharp Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK A. McGowan Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn, Cornwall TR10 9EZ, UK
than the effects of other factors, possibly due to the complex kin structure 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 and confers many benefits in terms of increased foraging efficiency and reduced predation. However, group members also incur various costs through competition with one another (Krause and Ruxton 2002). In some species, the process of kin selection (Hamilton 1964; Maynard Smith 1964) may allow individuals living in groups with their relatives to mitigate some of these costs and enhance the benefits of group-living (Ekman et al. 2004). One way in which this can occur is through nepotistic behaviours within a group that reduce the costs of competition between group members (Sherman 1977; Griesser and Ekman 2005). Indeed the benefits of associating with kin might give rise to philopatry and kin-based sociality, potentially playing a key role in the evolution of cooperative breeding systems (Stacey and Ligon 1991; Ekman et al. 2004; Covas and Griesser 2007). In such systems, there has been intensive study of the role of kinship in determining the investment decisions of helpers (e.g. Dickinson 2004; Covas et al. 2006; Nam et al. 2010; Wright et al. 2010), but much less is known about the effect of kinship on interactions during the non-breeding season. However, during this time, there are many potentially important contexts for kin discrimination to occur, including space use (Hatchwell et al. 2001), group defence against predators (Austad and Rabenold 1985), foraging (Kaib et al. 1996) and communal roosting (McGowan et al. 2007). Communal roosting behaviour has evolved independently in several bird lineages (Beauchamp 1999), some of which include cooperatively breeding species (Chaplin 1982; Ligon
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et al. 1988; du Plessis et al. 1994). The main function of communal roosting is probably the thermoregulatory benefit of reduced heat loss, with individuals that roost communally losing less mass overnight than solitary birds (McKechnie and Lovegrove 2001; du Plessis 2004). Birds that roost communally may also be less likely to suffer from predation than those that do not (Weatherhead 1983; Eiserer 1984). However, the benefits that an individual gains from communal roosting are likely to depend on the individual's position in the roost, which in turn may depend on factors such as age, sex, body size and dominance status (e.g. Swingland 1977; Feare et al. 1995; Adams et al. 2000; Calf et al. 2002). In species that live in groups consisting of individuals of varying relatedness to one another, an individual's position may also depend on its kinship to the rest of the group. Previous studies of cooperatively breeding birds have shown that the individuals occupying the peripheral positions at the ends of linear roosts are the two most dominant individuals in the group, e.g. jungle babblers Turdoides striatus (Gaston 1977), varied sittellas Daphoenositta chrysoptera (Noske 1985) and Arabian babblers Turdoides squamiceps (Zahavi 1990; Bishop and Groves 1991). Dominant individuals in these species will therefore be likely to accrue lower thermoregulatory benefits overnight and to be subject to a greater risk of predation than their subordinates (Weatherhead 1983). Such apparently cooperative behaviour might be expected in groups that are made up of close relatives as it allows the dominant individuals' offspring to occupy less costly positions on the inside of the roost, increasing their chances of survival and therefore the dominant birds' fitness. In this study, we tested the hypothesis that kinship determines an individual's position in the communal roosts of cooperatively breeding long-tailed tits Aegithalos caudatus. Long-tailed tits spend the non-breeding season in mixed-sex flocks usually comprising 5–20 individuals. Flocks typically contain both adults and juveniles from two or more nuclear families as well as a proportion of unrelated immigrants. These immigrants disperse between flocks during their first winter and account for approximately one third of every flock (Hatchwell et al. 2001; McGowan et al. 2007). Flocks break down during the breeding season (March–June), when all birds initially attempt to breed in monogamous pairs; cooperation occurs when failed breeders become helpers at the nest of another pair, assisting them in feeding nestlings and fledglings (Hatchwell et al. 2004). Long-tailed tits can recognise their kin using vocalisations that they learn in the nest (Sharp et al. 2005) and helping behaviour in this species is kin-biased with the majority of helping occurring between brothers (Russell and Hatchwell 2001; Nam et al. 2010). During the non-breeding season, long-tailed tit flocks roost in tight linear huddles. Previous studies have shown that individuals in the middle of the huddle lose less mass overnight than those on the outside (Hatchwell et al. 2009) and that there
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is competition for these preferred central positions within a roost (McGowan et al. 2006). The outcome of this competition is a function of an individual's dominance status within the flock, and contrary to studies on other cooperatively breeding species, the outer positions in long-tailed tit roosts, which are costly in thermoregulatory terms, are occupied by subordinates (McGowan et al. 2006). The factors affecting an individual's status are unknown in this species, but kinship plays a prominent role in their social organisation both during the breeding (e.g. Russell and Hatchwell 2001; MacColl and Hatchwell 2004; Nam et al. 2010) and non-breeding (Hatchwell et al. 2001) seasons so we hypothesised that status and therefore roosting position would be influenced by an individual's relatedness to other members of their flock. Several studies have shown that there are fitness benefits to associating with close kin rather than unrelated individuals and that this can be due to nepotistic behaviours within a group (e.g. Hoogland 1983; Griesser and Ekman 2005; Dickinson et al. 2009). McGowan et al. (2007) showed that non-kin are able to join family flocks and concluded that failed breeders do not help in order to gain access to a winter flock per se. However, nepotism may still occur at a more subtle level and birds with relatives in the flock may gain access to the preferred central positions within a roost, thereby increasing their chances of over-winter survival, while unrelated immigrants might be forced to occupy the more costly outer positions. This is particularly likely if high status is a direct benefit of helping behaviour since helpers in this species are usually related to the brood they raise and subsequent flock they join (Russell and Hatchwell 2001). The principal objectives of this study were to use captive flocks of long-tailed tits to investigate behavioural interactions among flock members to determine the effect of kinship and other factors (sex, body size, age and flock sex ratio) on (1) an individual's position within a roost and (2) an individual's status within the dominance hierarchy of a flock.
Methods We studied the roosting behaviour of 18 temporarily captive flocks of long-tailed tits between October and January 2000– 2002 (N=8 flocks) and 2004–2006 (N=10 flocks) entire flocks 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 in mist-nets from colour-ringed populations in Melton Wood, Doncaster, UK (53°31′N, 1°13′W; N=7 flocks) and the Rivelin Valley, Sheffield, UK (53°23′N, 1°34 W; N=4 flocks) or from unringed populations in the vicinity of Sheffield, UK (N=7 flocks). Flocks were transported to the Department of Animal and Plant Sciences, University of Sheffield, UK by car in cloth bags and were housed in outdoor aviaries (3×3×2 m in 2000–2002 and 3×1×2 in 2004–2006) that provided protection from rain and some wind (although birds were exposed
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to ambient temperatures). Aviaries were supplied with numerous perches, branches and a max/min thermometer. Birds were fed ad libitum with wax moth larvae Galleria mellonella, mealworms Tenebrio molitor and crickets Gryllus bimaculatus and water was provided for drinking and bathing at all times.
(i.e. outer or inner) on all nights of observation so each individual was assigned to the position that they occupied the most frequently for analyses.
Observations of communal roosts
The dominance hierarchy within each flock was determined from video recordings of aggressive interactions during roost formation (in the form of pecks) and by direct observation of interactions over food. During roost formation, pecks were usually aimed at the nape of the victim, allowing victims and aggressors to be identified unambiguously. Pecks occur regularly during interactions among flock members in the wild (CJN and BJH, personal observation) and did not lead to bleeding or loss of feathers in the captive birds. Interactions over food consisted of ‘tugs of war’ over a food item and the aggressor was the bird that was initially without food while the victim was the one initially with food. The winner was the bird that obtained the food item. No bird was deprived of food as a result of these contests. The number of aggressive interactions observed in the two contexts varied widely between flocks but there was a highly significant correlation between the dominance hierarchy generated from pecks and that generated from interactions over food (McGowan et al. 2006). Therefore, all pairwise interactions were combined and a linear dominance hierarchy was constructed for each flock, with the individual that won the greater proportion of aggressive interactions in the dyad being dominant. Each individual was then assigned a dominance score according to their position in the dominance hierarchy within their flock. The most subordinate individual within a flock received a score of 0 and the most dominant a score of 1 and all other birds between received a score according to their rank rising 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 the hierarchy could not be separated (for example if they had equal scores), and in these cases, both individuals received the mean score of the adjacent positions. In other instances, interactions were not observed between two flock members (16.4 % of possible dyads), in which case we assumed transitivity, i.e. if A was dominant over B and B over C, then A was also dominant over C. Comparison of generalised linear mixed models (GLMMs) with and without ‘dominance score’ fitted as a predictor and in which ‘flock identity’ was fitted as a random term showed that there was no effect of dominance status on the number of aggressive interactions an individual was involved in (GLMM: χ2 =0.12, df=1, P=0.735). Two individuals were marginally more likely to interact if they were unrelated (GLMM: χ2 =3.49, df=1, P=0.062), but the relationship between number of dyadic interactions and kinship was not significant after an extreme outlier where an unusually high number of pecks occurred between two unrelated individuals was removed (GLMM: χ2 =2.69, df=1, P=0.101).
Observations began once flocks had been allowed to acclimatise to captivity for 48–72 h. Roosting behaviour was recorded using a video camera with an infrared night vision function (Sony CCD-TR427E) positioned above a roosting perch. In 2000–2002, the perch was placed in an openfronted wooden roosting box (1.2×0.5×0.8 m) in the aviary. However, flocks did not always choose to roost on the roosting perch, so in 2004–2006, the birds were moved to a smaller cage (0.4×0.5×0.3 m) containing the roosting perch shortly before dusk and released back into the aviary at dawn. Video recordings showed that roosting behaviour did 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 rings could not be seen from overhead during roost formation, a 5×5-mm black label was stuck to the tips of the birds' crown feathers using non-toxic glue. Each label was uniquely marked with white enamel paint to allow birds to be individually identified and their position in the roost to be determined. Labels were removed before the birds' release at the end of the observations and, although the tips of some crown feathers were clipped, there was no visible effect on the birds' appearance. The behaviour of birds towards conspecifics was unaffected by the addition of the labels. In 2000–2002, flocks were filmed for a 4-h period around dusk (1 h before and 3 h after) and for a further 4 h around dawn (2 h before and 2 h after). This ensured that all movements during roost formation and breakup as well as final roost positions were recorded. After an initial period of birds jockeying for position and relocating, positions were stable throughout the night (McGowan et al. 2006); so in 2004– 2006, roosts were filmed for only 1.5 h around dusk since this was sufficient to allow interactions during roost formations and final roost positions to be recorded. Roosts were filmed for up to seven nights per flock, and roosting positions within linear huddles were known with certainty for all individuals for a mean of 3.61±1.75 SD nights per flock (N.B. on a few occasions, one or more individuals chose to roost separately from the main huddle, or marks on labels could not be clearly discerned; in either case, data from those nights were 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 at least one bird on either side during roosting). The majority of birds (80.3 %, N=137) occupied the same roosting position
Dominance hierarchies
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Genetic analysis Blood samples (approximately 10 μl per bird) were taken from all birds by brachial venipuncture under UK Home Office Licence. Genomic DNA was extracted from blood samples and amplified as previously described (Simeoni et al. 2007). Individuals were sexed using standard molecular genetic techniques (Griffiths et al. 1998) and genotyped at nine 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 identified by Simeoni et al. (2007). Queller and Goodnight's (1989) coefficient of relatedness of flock members, r, was calculated using SPAGeDi 1.3 (Hardy and Vekemans 2002). Nam et al. (2010) and Simeoni (2011) showed that estimated r closely matched pedigree relatedness in two of the populations from which our study flocks were captured, but the extent to which estimated r reflected true relatedness could not be directly tested for the sample of birds used here because in the large majority of cases pedigree information was not available. Nevertheless, estimated r should provide a close approximation of relatedness in our sampled birds. Statistical analyses We adopted two approaches to investigate the effect of kinship on interactions within a flock. Firstly, we investigated the effect of kinship, dominance status, sex, body size, age and flock sex ratio on an individual's position in the roost using GLMMs, and secondly, we examined the effect of kinship, sex, body size, age and flock sex ratio on an individual's status within its flock using general linear models (GLMs). We then conducted model selection and averaging based on AICc (Akaike's Information Criterion corrected for small sample size). Model fitting To investigate the effect of kinship on an individual's position within the roost, we fitted GLMMs with a binomial error distribution 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 to control for the presence of multiple individuals belonging to the same flock. An individual's ‘kinship’, ‘dominance’ score, ‘sex’, body ‘size’ and ‘age’ and the ‘sex ratio’ of the flock were fitted as predictor variables, as well as all biologically meaningful first-order interactions. ‘Position’ was defined as ‘outer’ (positions on the ends of the linear huddle) or ‘inner’ (the remaining positions in which all birds had at least one bird on either side during roosting) while ‘kinship’ was defined as an individual's average relatedness to the rest of the flock as determined by molecular
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genetic analysis. Similar results were obtained when an individual's kinship to the rest of the flock was defined as the proportion 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 score as described above. Many of the birds in our captive flocks were of unknown age at the time of capture, either because they were immigrants into our study populations or because they were captured from unringed populations. Measurements of known-age birds in a long-term study population in the Rivelin Valley, Sheffield, show that adult long-tailed tits have longer wings than juveniles (Welch's two sample t test: t107.5 =4.961, P
