Effects of neighbor familiarity on reproductive success in the great tit (Parus major)

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1 Behavioral Ecology doi: /eheco/arr189 Advance Access pulication 1 Decemer 2011 Original Article Effects of neighor familiarity on reproductive success in the great tit (Parus major) Ada M. Graowska-Zhang, Teddy A. Wilkin, and Ben C. Sheldon Department of Zoology, Edward Grey institute, University of Oxford, South Parks Road, Oxford OX1 3PS, UK Social interactions can often affect the fitness of individuals. Territorial animals frequently interact with their neighors, and long-term familiarity might lead to the development of cooperative relationships, which might influence the fitness of neighoring individuals. Here we test the hypothesis that familiarity with neighors positively affects reproductive success in the great tit (Parus major). We used data from a 41 year long-term study of the great tit to quantify neighor familiarity and its relationship with different stages in the great tit reproductive cycle. Breeding irds had from 0 to 11 neighors with whom they were familiar y sharing a territory oundary the year efore; although owing to low annual survival, the mean proportion of familiar neighors (0.1) was quite small. Despite the low average proportion of familiar neighors, we found evidence suggesting positive effects of increased familiarity: females with more familiar individuals in their neighorhood laid larger clutches. We also found that oth males and females with more familiar neighors had a greater chance of successfully fledging offspring. These results suggest that long-term familiarity can enefit territorial reeding irds. Future work is needed to address the underlying mechanisms of how neighor familiarity influences individual fitness. Key words: familiarity, Parus major, reproductive success, sociality, territorial neighors. [Behav Ecol 23: (2012)] Address correspondence to A.M. Graowska-Zhang. ada. graowska@zoo.ox.ac.uk. Received 30 Decemer 2010; revised 27 Septemer 2011; accepted 4 Octoer Ó The Author Pulished y Oxford University Press on ehalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please journals.permissions@oup.com INTRODUCTION I n many organisms, individuals retain a relatively stale home range or territory over the long term. Benefits of territory fidelity include the accumulation of information aout the local haitat, availale resources, and the presence of predators, for example, local familiarity improved territory acquisition in juvenile lizards (Stamps 1987), and territory relocation was shown to cause short-term costs in damselfish (McDougall and Kramer 2007). Birds have een shown, when displaced, to prefer to pay the costs of finding the way ack to their home territory rather than to settle in an unfamiliar area (Pärt 1995). The importance of the territory to territorial species may depend not only on the characteristics of their haitat ut also on the social context of the neighorhood. Territory defense is costly, and renegotiating the oundary with an unfamiliar newcomer tends to incur more cost than defending the territory against an estalished neighor (Eason and Hannon 1994). Storing information aout the competitive aility of territorial rivals and retaining stale social relationships may e an additional enefit of site fidelity oserved in many species. At a asic level of association, neighor stranger discrimination affects territorial interactions and underlies the dear enemy phenomenon (DEP). In the DEP, territorial individuals react less aggressively to neighoring than to distant territorial or vagrant individuals (Briefer et al. 2008; Brunton et al. 2008; Rosell et al. 2008;reviewedinTemeles 1994). In agreement with game-theoretic predictions, territorial individuals modulate their response to the relative threat posed y neighors versus strangers (Jaeger 1981; Getty 1987; Temeles 1990;reviewedinTemeles 1994). In situations when a neighor poses less threat to the defended resources (food, mates, and reeding sites), reacting less aggressively to those individuals is adaptive, as the resident will expend less energy on escalating territorial contests. Treating neighors as dear enemies is not an invariant relationship and is dependent on the social context. For example, it has een shown that territorial male skylarks are dear enemies in the middle of the reeding season (when males with estalished territories did not pose a threat of territory overtake) ut reverse their strategies early or late in the season, when territory oundaries are much more fluid (Briefer et al. 2008). Familiarity can ring fitness enefits other than those resulting from diminished aggressive interactions. Repeated encounters etween the same individuals aid the evolution of cooperative ehaviors, such as reciprocity. Reciprocity is est known from tight-knit groups where repeated interactions allow a degree of protection against defectors (cheats) through strategies like tit for tat. The tit for tat strategy involves cooperation on the first encounter and then repeating the partner s previous move (Axelrod and Hamilton 1981). Recently, reciprocity has een suggested to occur in temporary territorial aggregations of a reeding passerine ird wherey reeding pairs of pied flycatchers (Ficedula hypoleuca) reciprocated y joining in a predator mo at the nest of previously cooperating pair ut not in a mo at the nest of defectors (Krams et al. 2008). This widely discussed experiment (Wheatcroft and Price 2008; Russell and Wright 2009; Wheatcroft and Krams 2009) suggests that reciprocity can operate in structured populations previously thought not to have stale enough associations for reciprocity to occur. Previous studies of the consequences of familiarity etween individuals have analyzed the effects of familiarity on a numer of traits in a variety of species. Reported effects include higher social tolerance in male lizards (Aragon et al. 2007), faster growth rate in wild sea trout (Salmo trutta) (Hojesjo Downloaded from y guest on 01 Octoer 2018

2 Graowska-Zhang et al. Neighor familiarity and reproductive success 323 Figure 1 Summary of the investigated relationships etween sexes of territorial neighors. Few studied the influence on focal females of their female or male neighors as well as neighors irrespective of sex. Males were investigated for influence of their male neighors. Numers on arrows represent the numer of focal individuals used in each data set. et al. 1998) and juvenile salamanders (Plethodon cinereus) (Liegold and Cae 2008), and etter survival and growth in the Arctic char (Salvelinus alpinus) (Seppa et al. 2001). Preference for familiar shoal-mates and its enefits have een widely studied in fish (Griffiths et al. 2004; Bhat and Magurran 2006; Lee-Jenkins and Godin 2010). However, most studies that have compared familiar and unfamiliar individuals focused on variales for which the fitness consequences have to e assumed: There has een rather little empirical work on direct fitness consequences of familiarity. The only reported effects were the positive influence of familiar neighors on reproductive performance in male red-winged lackirds (Beletsky and Orians 1989), ut no effect was found in the females of the same species (Weatherhead 1995). Familiarity had no effect on the reproductive success of translocated New Zealand roins (Petroica australis longipes) (Armstrong 1995) or North Island saddleacks (Philesturnus carunculatus rufusater) (Armstrong and Craig 1995); although, in these studies, small sample sizes might have limited the power to detect any effects. The great tit (Parus major) is a small passerine ird common in European road-leaved forests (Perrins 1979). It is a secondary cavity nester, choosing holes in old trees, and stumps as nesting sites ut preferentially accepts nest-oxes as reeding sites in our study population (Perrins 1965). Males defend multipurpose territories on which they feed, mate, and rear young. The amount of time spent defending the territory depends on how often the male is contested y other males (Slagsvold et al. Tale 1 Variale areviations used in gloal model formula 1994). Previous work on this species reveals that once they have settled in a reeding territory, adults show very limited reeding dispersal in susequent years (Harvey et al. 1979); hence, there is the potential for long-term familiarity to arise etween neighoring individuals. Familiarity with males from neighoring territories could enefit the defender, as familiar males are more likely to have prior information aout each other s condition and are therefore less likely to challenge each other or escalate in territorial display. Both parents participate in chick rearing, ut it remains untested whether social environment affects their success as reeders. The aim of this study was to explore hypotheses aout familiarity with neighors and its effect on reproductive performance in great tits. The 2 sexes are likely to e affected differently or to a different degree y the presence of familiar individuals in the neighorhood. Familiarity can e defined in a variety of ways. We use a measure of familiarity with individuals from surrounding territories to assess its effect on different measures of reproductive success, from the onset of reeding to the recruitment success of the reproductive event. Defining familiar neighors as individuals that shared a territory oundary in the previous year is a straightforward measure, and one for which there is a large quantity of data availale. We use the numer of familiar neighors and a simpler, one-dimensional inary variale, the familiarity status of the nearest neighor, with familiarity defined in the same way. MATERIALS AND METHODS Study population The analysiswasperformedondatafromagreattitpopulationin Wytham Woods, Oxfordshire. The site is descried in more detail y Wilkin (2006). This piece of continuous woodland has over 1000 nest-oxes that have een kept at fixed localities throughout the study period. Breeding events from 1965 to 2005 were used in this study. Life-history traits (date of laying the first egg [laying date, where 1 ¼ April 1], clutch size, fledging success, fledgling mass, and numer of offspring recruited to the local reeding population) were recorded for all reeding attempts using a field protocol standardized throughout the study. Details of the methods have een descried y Perrins (1965); the major sources of variation in these life-history traits are descried y McCleery et al. (2004) and Browne et al. (2007). The identities of reeding individuals were estalished from British Trust for Ornithology rings y trapping adult irds in the nest-ox. All fledglings orn in Wytham are ringed in the nest-ox, and the immigration status (resident or immigrant)ofthereedercaneestalishedfromthering.immigration status of the reeding female has a documented Downloaded from y guest on 01 Octoer 2018 Response variales Covariates Parameter symols LD laying date AC spatial autocorrelation covariate 0 intercept CS clutch size ALT altitude w within-individual component of variance FM mean fledgling mass DIS distance moved from previous year etween-individual component of variance NS nest success EDG distance from the woodland edge u 0 random intercept RS numer of recruits FAM numer of familiar neighors u 1 random slope FS female status, resident or immigrant e (Gaussian) error term (distriution) NN familiarity with the nearest neighor TER territory size WRM the sum of maximum daily temperatures from 1st to 25th April ID reeder identity YEAR year

3 324 Behavioral Ecology (A) Mean familiarity (B) Mean familiarity Adult survival from previous year Mean recruits per rood from previous year Figure 2 Effects of annual variation in demographic variales on mean proportion of familiar neighors in great tits using model averaging; (A) adult survival from previous year and (B) mean numer of recruits per rood from previous year. effect on life-history traits (McCleery et al. 2004; Bouwhuis et al. 2010). Recruitment success was measured as the numer of young recruited to the Wytham population (Perrins and McCleery 1985); local recruitment only reflects fitness if natal emigration is independent of the state of individuals, which, as far as we are aware, is the case in our population (Verhulst et al. 1997; Bouwhuis et al. 2009). Distance moved etween reeding attempts y adults (reeding dispersal), although usually shorter than the width of a territory (Harvey et al. 1979), was also recorded due to its potential to decrease the familiarity with surrounding individuals. Environmental variales We included a numer of environmental variales as covariates ased on previous work in this population. The effect of Numer of reeding events female female female male female oth sexes male male Proportionate familiarity Log e transformed Figure 3 The distriution of proportionate familiarity across data sets of 4 focal reeder-neighor cominations (log e transformed). territory size on reproduction was descried y Wilkin et al. (2006). The measure of spring temperature in each year was recorded as warmth sum (after McCleery and Perrins 1998), which is the sum of maximum day temperatures from 1 March to 25 April. This measure was included as it is known to influence the timing of reeding through changes in food aundance. Altitude, as well as distance to forest edge, was previously shown to affect reproductive traits (Wilkin, Perrins, et al. 2007), as it affects plant phenology and the timing of food supply. Territory oundaries Nest-oxes occupied y great tits each year were mapped using Map Info Professional 8.5, using methods descried in Wilkin et al. (2006). Breeding territory oundaries were estimated y Dirichlet tessellation, which constructs a polygon that contains all points that are closer to the focal reference point (nest-ox) than to any other reference point, with edges equidistant to closest neighoring points. This measure of territory size assumes the use of all availale space etween the nest-oxes. Although this may e true for small territories, larger ones may contain space that is not frequently used y reeders. Consequently, reeders may have fewer interactions with neighors on large territories, as there will e unused space etween areas most frequented y territory holders. We acknowledge that this method provides a very simple model of space use, ut it has the advantage that it is ojective and can e applied at a large scale and can thus e applied retrospectively over large sample sizes. Previous work using this measure on this population has shown that it generates estimates of local population density, which are related in the expected way to a range of life-history traits, and that the measure is comparale to territories mapped from oservation (Wilkin et al. 2006). Identities of the focal individuals reeding at a particular nestox and their first-order neighors were analyzed from year to year to estalish previous year territory holders. The resulting dataase contained reproductive attempts from 1965 to 2005, each row containing a focal and neighor territory pair of Downloaded from y guest on 01 Octoer 2018

4 Graowska-Zhang et al. Neighor familiarity and reproductive success 325 (A) Clutch size (B) Nest success proaility Numer of neighors (oth sexes) familiar with females Numer of neighors (oth sexes) familiar with females Figure 4 The effect of etween-individual variation in familiarity with neighors of either sex on (A) clutch size and (B) nest success proaility. x axis contains the entire range of values of familiar neighors; y axis contains 61 standard deviation variation in clutch size. The figure was derived from the averaged model. reeders. Familiar neighors were defined as individuals that shared a territory oundary with the focal ird in the previous year. Identities of reeders were matched to territories, and the dataase was queried to extract those neighors in year t that were also neighors to the focal individual in year t 2 1. Data selection The analysis was performed on irds reeding for the second or susequent time, as it is clearly impossile for first time reeders to have neighors familiar from the previous reeding season, in this context. Four classes of neighors were analyzed in this study. They are summarized in Figure 1. First, the female neighors of the focal female were assessed for familiarity, that is, a shared territory oundary in the previous year. The same procedure was performed for male neighors of the focal female. Next, neighors of either sex of the focal female were analyzed. We also performed the same analysis of the effects of male male familiarity. We counted the numer of familiar individuals surrounding the territory and assessed the familiarity status of the nearest neighor for each of those categories of reeders. The data set comprised different numers of reeding events and individuals for different analyses, as oth identity of the focal individual and the neighor had to e known. Any reeding attempts in which the identity of the focal individual was not known were also excluded from the analysis. The reason for this was that in such cases, it is impossile to determine an individual s social environment, and data on phenotypic characteristics are unavailale. In cases where some of the focal or previous-year neighors remained unidentified, focal year neighors might have een wrongly assigned unfamiliar status, which renders our analysis conservative, that is, we might assign familiar neighor as unfamiliar ut not the other way round. Cases that include unidentified neighors when the focal identity was known amounted to up to 14% of all investigated neighor pairs. Some individuals appear in the data set more than once, and reeder identity was therefore used as a random factor in our analyses to account for multiple reeding attempts y the same individuals across years. Across data sets, etween 945 and 1297(59 63%) individuals appear once, (aout 25%) appear twice, and (23 26%) individuals appear in the data set more than twice. We used within-suject centering (van de Pol and Wright 2009) to separate the variation in familiarity into etween-individual and within-individual components, as they generate 2 different hypotheses; the former relates to inherent differences etween individuals (variation in the population) and the latter indicates differential responses in the same individual (phenotypic plasticity). Individuals appear in the data set as focal reeders and are also included in the count of neighors in data points where their neighors appear as focals. This reappearance of individuals in 2 contexts in the data set does not affect the analysis; removal of a random suset of repeating pairs does not change the result. Different classes of individuals may e familiar in different contexts; for example, first-year individuals cannot e familiar for as long as older individuals. Our measure provides a simple way of ensuring all measured individuals have the same scope for familiarity etween years. All investigated individuals needed to have red in the population at least 2 years in a row, which excludes first-year individuals and first-time immigrants to the population. The primary interest was to estalish whether individuals with long-term neighors differ in their reproductive performance from those without familiar neighors. We divided the reproductive attempt into measures derived at 5 sequential stages, so that measures of reproductive performance included in the analyses are 1) egglaying date, 2) clutch size, 3) mean fledgling mass, 4) fledging success, and 5) recruitment success. We analyzed fledging success as a inomial measure of whether the nest produced at least one fledgling or failed efore the young fledged. Males who have stale neighors are expected to positively influence offspring traits, such as fledgling mass and recruitment success, whereas female familiarity with neighors may also affect the sex-specific traits of laying date and clutch size. If the effect on laying date is negative, it suggests familiarity enefits the females, as selection strongly favors early laying in the majority of years in this population (Charmantier et al. 2008). A female s long-term familiarity with neighors might affect her reproductive decisions ased on her perception of local density or competitor quality, leading to effects on laying date or clutch size or oth. Statistical methods We used an information theoretic approach with corrected Akaike s information criterion (AIC C ) to first explore the Downloaded from y guest on 01 Octoer 2018

5 326 Behavioral Ecology Tale 2 Averaged models examining the correlates of reproductive success in focal females Response: LD Estimatey Variance SE Unconditional SE Lower CI Upper CI Relative importance (Intercept) FS ALT DIS FAM W Response: CS (Intercept) na na AC na na FAM B na na LD na na Response: FM (Intercept) ALT CS FAM B LD a NN B TER Response: NS (Intercept) AC ALT CS FAM B FAM W LD a NN B a NN W TER Response: RS (Intercept) CS FAM B FM LD TER a NN B a NN W Variale areviations in all tales: LD, laying date; CS, clutch size; FM, mean fledgling mass; RS, numer of recruits; FS, female status, resident or immigrant; AC, spatial autocorrelation covariate; ALT, altitude; DIS, distance moved from previous year; FAM B, etween-individual component of the numer of familiar neighors; FAM W, within-individual component of the numer of familiar neighors; NN B, etween-individual component of familiarity with the nearest neighor; NN W, within-individual component of familiarity with the nearest neighor; EDG, distance from the edge of the forest; TER, territory size; RS, numer of recruits; WRM, warmth sum, the sum of maximum daily temperatures from 1st to 25th April; y, estimates have een standardized to 2 standard deviations (Gelman 2008), with the exception of AC variale, estimates of which cannot e directly compared with other parameters within the models. The variales of interest are the numer of familiar neighors of either sex and the familiarity status of the nearest neighor of either sex. SE, standard error; CI, confidence interval; na, not applicale. a Unfamiliar as the reference category. predictors of familiarity at the population level and then to generate hypotheses aout the effects of familiarity on measures of reproductive success. We used the MuMIn package (Bartoń 2010) in the R environment (R Development Core Team 2005) to perform all suset selection and model averaging ased on AIC C value. The input variales were standardized using the arm package (Gelman et al. 2010), so that parameter estimates can e easily and correctly interpreted (Gelman 2008). Models with DAIC C 2 (i.e., for which there is no strong indication that one model has the est fit) were averaged to otain parameter estimates. We used the natural average method, where parameters are averaged only across models they occur in. We used a single est model as our source of inference if the second est model had a value of DAIC C 2. In order to understand the ehavior of familiarity as a variale, we performed model selection analysis in order to determine predictors of mean yearly familiarity in the population for the years used in the study. We explored the effects of demographic variales such as adult survival, recruitment, and population size on the annual levels of familiarity present in the population. Population size was estimated from nest-ox occupancy rates, the proxy for recruitment rate was the numer of recruits per rood, and survival rate was estimated from a capture-mark-recapture analysis, which controls for variation in resighting proaility (Bouwhuis et al. forthcoming). Our gloal model was: y ¼ SRV 1 2 REC 1 3 POP 1 e; where y is average familiarity in a given year, SRV is adult survival, REC recruitment as the average numer of recruits per rood, and POP population size. Error term e was drawn from Downloaded from y guest on 01 Octoer 2018

6 Graowska-Zhang et al. Neighor familiarity and reproductive success 327 Tale 3 Averaged models examining the correlates of reproductive success in focal females Response: LD Estimatey Variance SE Unconditional SE Lower CI Upper CI Relative importance (Intercept) FS a AC ALT DIS FAM B FAMw NN B WRM Response: CS (Intercept) AC FAM B LD NNw Response: FM (Intercept) AC ALT CS FAM B NN B NNw TER Response: NS (Intercept) AC ALT CS FAM B FAMw LD NN B NNw TER Response: RS (Intercept) AC CS FAM B FAMw FM LD NNw TER Models inspect the familiarity with male neighors. The variales of interest are the numer of familiar male neighors and the familiarity status of the nearest male neighor; areviations of variales as for Tale 2. SE, standard error; CI, confidence interval; y, estimates have een standardized to 2 standard deviations (Gelman 2008), with the exception of AC variale, estimates of which cannot e directly compared with other parameters within the models. a Immigrant as the reference category. Unfamiliar as the reference category. Downloaded from y guest on 01 Octoer 2018 a normal distriution. We also explored predictors of familiarity at the level of individual reproductive attempt. We looked for predictors of familiarity measured as the numer of familiar neighors (successes) and the numer of unfamiliar neighors (failures) in a model with inomial error structure. We examined the following gloal model with inomial error structure: y in ¼ DIS 1 2 EDG 1 3 TER 1 4 AGE 1 5 ALT 1 6 AC 1 e; where DIS is the reeding dispersal distance, EDG is the distance etween the nest-ox and the woodland perimeter, TER is territory size, AGE is reeder age, ALT is altitude, and AC is a spatial autocovariate controlling for autocorrelation. Finally, we examined the effects of 2 measures of familiarity on different aspects of reproductive success. The measures adopted in all models are 1) the numer of neighors that also shared a territory oundary the year efore and 2) the familiarity status of the nearest neighor. Those 2 variales of interest measure the overall level of familiarity within a territory and the importance of eing familiar with the closest territorial neighor, respectively. All gloal models contain TER a measure of territory size, to control for density effects. In order not to overparameterize our gloal models, we only included variales (for details, see Tale 1) that have een documented to affect the dependent variale (as recommended y Burnham and Anderson

7 328 Behavioral Ecology Tale 4 Averaged models examining the correlates of reproductive success in focal females Response: LD Estimatey Variance SE Unconditional SE Lower CI Upper CI Relative importance (Intercept) AC FS a ALT FAM B NN B Response: CS (Intercept) AC LD TER Response: FM (Intercept) AC ALT CS LD NN B NNw TER Response: NS (Intercept) AC ALT CS FAM B FAM W LD NN B NNw TER Response: RS (Intercept) AC CS FAM B FAMw FM LD NN B NNw TER Models inspect the familiarity with female neighors. The variales of interest are the numer of familiar female neighors and the familiarity status of the nearest female neighor; areviations of variales as for Tale 2. SE, standard error; CI, confidence interval; y, estimates have een standardized to 2 standard deviations (Gelman 2008), with the exception of AC variale, estimates of which cannot e directly compared with other parameters within the models. a Immigrant as the reference category. Unfamiliar as the reference category. Downloaded from y guest on 01 Octoer ). Gloal models used across all 4 data sets were performed in lme4 package (Bates and Maechler 2009): y LD ¼ 0 1 B NN 1 W NN 1 B FAM 1 W FAM 1 2 ALT 1 3 TER 1 4 FS 1 5 DIS 1 6 AC 1 u 0 ID 1 u 0 YEAR 1 u 1 YEAR 1 e ðgaussianþ y CS ¼ 0 1 B NN 1 W NN 1 B FAM 1 W FAM 1 2 LD 1 3 TER 1 4 EDG 1 5 AC 1 u 0 ID 1 u 0 YEAR y FM ¼ 0 1 B NN 1 W NN 1 B FAM 1 W FAM 1 2 LD 1 3 CS 1 4 TER 1 5 ALT 1 6 AC 1 u 0 ID 1 u 0 YEAR 1 u 1 YEAR 1 e ðgaussianþ y NS ¼ 0 1 B NN 1 W NN 1 B FAM 1 W FAM 1 2 LD 1 3 CS 1 4 TER 1 5 ALT 1 6 AC 1 u 0 ID 1 u 0 YEAR 1 u 1 YEAR 1 e ðinomialþ 1 u 1 YEAR 1 e ðgaussianþ

8 Graowska-Zhang et al. Neighor familiarity and reproductive success 329 Tale 5 Averaged models examining the correlates of reproductive success in focal males Response: LD Estimatey Variance SE Unconditional SE Lower CI Upper CI Relative importance (Intercept) FS a AC ALT FAM B FAM W NN W TER WRM Response: CS (Intercept) AC LD TER Responce: FM (Intercept) AC ALT TER Response: NS (Intercept) AC ALT CS FAM B FAM W LD NN B NN W Response: RS (Intercept) CS FAM B FAM W FM LD TER NN B NN W Models inspect the familiarity with male neighors. The variales of interest are the numer of familiar male neighors, and the familiarity status of the nearest male neighor. SE, standard error; CI, confidence interval. Areviations of variales as for Tale 2; y, estimates have een standardized to 2 standard deviations (Gelman 2008), with the exception of AC variale, estimates of which cannot e directly compared with other parameters within the models. a Immigrant as the reference category. Unfamiliar as the reference category. y NS ¼ 0 1 B NN 1 W NN 1 B FAM 1 W FAM 1 2 LD 1 3 CS 1 4 FM 1 5 TER 1 6 AC 1 u 0 ID 1 u 0 YEAR 1 u 1 YEAR 1 e ðpoissonþ: We fitted random intercepts in our models (as recommended y Grueer et al. 2011); a random slope was fitted to year. Summary of random effects for gloal models can e found in Supplementary Tale 1. In order to statistically eliminate any spatial autocorrelation that may e present in our models, we included an autocorrelation variale as a fixed covariate in all our gloal models, as recommended y Dormann et al. (2007). The covariate was calculated with autocov_dist function in spdep package (Bivand et al. 2010). RESULTS Characterizing familiarity Mean familiarity varied across years. The mean ratio of the numer of familiar to the total numer of neighors varied from 0.03 to 0.22 (median ¼ 0.12, interquartile range [IQR] ¼ ). Model selection with AIC C resulted in the following est model: y ¼ SRV 1 2 REC 1 e: The second est model had DAIC C ¼ 2.24 (for details of model selection, see Supplementary Material). Adult survival and recruitment had the expected effects on familiarity, positive, and negative, respectively (Supplementary Tale 3), such that familiarity was higher in years when a larger proportion of adults had survived from the previous year and lower following high rates of juvenile recruitment. The effects Downloaded from y guest on 01 Octoer 2018

9 330 Behavioral Ecology (A) Mean fledgling mass (g) (B) Nest success proaility (C) Numer of recruits Unfamiliar Familiar Familiarity status of the nearest female Unfamiliar Familiar Familiarity status of the nearest female Numer of female neighors familiar with females Figure 5 The etween-individual effect of nearest female neighor familiarity on female reproductive traits. (A) Mean fledgling mass. (B) Proaility of nest success. (C) The effects of the numer of familiar female neighors on the numer of recruits. Effects are predictions from averaged models. in the tale are standardized to 2 standard deviations and are therefore on a comparale scale. Untransformed slopes are visualized in Figure 2. We further aimed to identify the correlates of familiarity in the individual s environment to e aware of their effects in further analysis. Across data sets, territory size had a negative effect on familiarity (for details, see Supplementary Tales 4 7). Distance moved etween years was negatively correlated with familiarity level of focal females ut not focal males. Distance from the forest edge was positively correlated with familiarity of females ut was not an important predictor for focal males. Neighoring individuals For females, the total numer of female neighors ranged from 1 to 12, with median of 5 neighors (IQR ¼ 4 6). The numer of familiar female neighors was etween 0 and 5, with median of 0 (IQR ¼ 0 1). Females had from 1 to 12 male neighors (median ¼ 5, IQR ¼ 4 6) and from none to 5 familiar male neighors (median ¼ 0, IQR ¼ 0 1). Females neighors of oth sexes ranged from 2 to 24 (median ¼ 10, IQR ¼ 8 12) and from none to 8 were familiar (median ¼ 0, IQR ¼ 0 2). Males had from 1 to 11 male neighors (median ¼ 5, IQR ¼ 4 6) and none to 5 familiar male neighors, with median of 1 (IQR ¼ 0 1). Hence, although the majority of neighors in any single year were unfamiliar, there is considerale spread in the proportion of prior familiarity among reeding neighors (Figure 3). Distriutions of the numer of familiar neighors as well as the total numer of neighors in a territory were similar for all analyses. The total numer of neighors did not differ etween males and females (two-sample t-test: t ¼ 21.12; P ¼ 0.262), ut females had on average 0.18 familiar neighors fewer than males (t ¼ 7.25; P, 0.001); this is expected given slightly higher rates of reeding dispersal in female great tits compared with males (Harvey et al. 1979). Familiarity and reproductive success Our results show positive etween-individual effect of the numer of familiar neighors on clutch size for focal females with familiar neighors of oth sexes and a positive within- and etween-individual effect for focal females with familiar male neighors (Figures 4A and 6A, respectively). In oth of those cases, the confidence interval did not contain zero, indicating that numer of familiar neighors is a useful predictor of clutch size (Tales 2 and 3, respectively). Our measures of familiarity did not appear in the set of top models for this variale for female neighors of females and male neighors of male (Tales 4 and 5, respectively). The etween-individual component of familiarity (with nearest neighor for female female data set and numer for other data sets) improved the nest success proaility (Figure 5B). The direction of the effect was consistently in the direction such that the enefit of familiarity for producing a successful rood, ut for female oth sexes (Tale 2) and male male (Tale 5) data sets the confidence intervals included zero. There was a positive etween-individual effect of nearest neighor familiarity for female oth sexes data set. Withinindividual effects contained 0 in their confidence intervals, except for female male neighors data set, where there was a within-individual positive effect on clutch size. Familiarity with the nearest female neighor was also associated with the focal female fledging heavier young (Figure 5A). Nearest neighor familiarity was more informative than the numer of familiar neighors for fledgling mass and nest success in this data set, whereas numer of familiar neighors had an effect on the numer of recruits. Confidence intervals of our estimates did not include 0. Familiarity was not a useful predictor of laying date in any of the data sets or average fledgling mass for female oth sexes and male male data sets (Tales 2 and 5, respectively), however, etween-individual variation in numer of familiar neighors had a positive effect on fledgling mass for female male data set (Figure 6C). Downloaded from y guest on 01 Octoer 2018

10 Graowska-Zhang et al. Neighor familiarity and reproductive success 331 (A) Clutch size (C) Fledgling mass Numer of male neighors familiar with females Numer of male neighors familiar with females (B) These analyses suggest that there are effects of neighor familiarity on reproductive success ut that these occur predominantly at the etween-individual level rather than the within-individual level. DISCUSSION We characterized long-term familiarity etween reeding great tits and used this to explore hypotheses aout the effects of familiarity etween territorial neighors on reproductive success. We found that females with a larger numer of familiar neighors laid larger clutches and that for oth sexes of reeders, the proaility of reeding successfully was higher when surrounded y more familiar individuals or if the nearest neighor was familiar. In our characterization of interannual variation in familiarity, we found the expected effect of annual variation in adult survival rate (positive) and recruitment success (negative), which suggests that our measure of individual familiarity captures real differences in the extent to which long-term associations could arise. Adult survival had a positive effect on mean familiarity independent of juvenile recruitment and population size, which is captured in a multiple regression analysis. There was a small ut significant difference in the mean numer of familiar neighors etween sexes, with females having fewer familiar neighors than males. This is likely to e due to the fact that males defend territories and are less likely to disperse if they are territory owners (Harvey et al. 1979). Few great tits disperse from year to year, and dispersal distance is short (mean ¼ 66.1 m, IQR ¼ m Nest success proaility (D) Nest success proaility Numer of male neighors familiar with females Numer of male neighors familiar with males Figure 6 The etween-individual effect of the numer of familiar neighors on (A) clutch size of females with familiar male neighors, (B) proaility of nest success (females with familiar male neighors), (C) mean fledgling mass (females with familiar male neighors), and (D) nest success proaility for males with familiar male neighors (note confidence interval includes 0 here). for females; median ¼ 51.4, IQR ¼ m for males); in many cases, these dispersal distances are insufficient to move to a different group of neighoring individuals. However, there was evidence that reeding dispersal distance, territory size, and distance from edge influenced the level of individual familiarity. Breeding dispersal etween years had the expected negative effect on familiarity, although territory size had a negative effect on familiarity. Larger territories may themselves result from sudominant first-year reeders settling in the vicinity and may result in oth the focal male eing ale to defend a larger area and a decreased familiarity level. Distance of the focal nest-ox from the edge of the wood had a positive effect on familiarity, which may e caused y immigrants from outside the population settling to reed closer to the edge (Wilkin, Garant, et al. 2007), therey decreasing the chance of an adult reeder having neighors familiar from the previous year. Our results show that familiarity with neighors is related to increases in some, although not all, aspects of the reproductive success of great tits. It also suggests that familiarity with neighors mostly enefits the female at that stage, as it has een shown previously that traits like clutch size are predominantly controlled y the female of the reeding pair (Browne et al. 2007). The female decision to lay a larger clutch is unlikely to e influenced y altered territorial ehavior etween her partner and neighoring males, as her mate s familiarity with neighoring males showed no effect on clutch size (Tale 5). The fact that the familiarity of the nearest neighor, rather that familiarity among all neighors, was more informative for the female neighor data set (Tale 4) may reflect differences Downloaded from y guest on 01 Octoer 2018

11 332 Behavioral Ecology in social relationships or haitat use etween the sexes. It is possile that females do not venture to the edges of their territory as much as males, as they do not routinely defend the territory, and therefore may have far fewer interactions with neighors occupying more distant nest-oxes compared with the nearest neighor. We separated the effect of familiarity in our analysis, into etween- and within-individual effects, and found that in general, there is more evidence for an effect of familiarity at the etween-individual level than within individuals. This suggests that the effect of familiarity is due to different individuals reacting differently to their social environment. The within-individual effect, while suggesting effects in the same direction, in most cases, overlapped 0 in its confidence interval(ut see clutch size analysis in Tale 3). However, due tothefactthatonlyasmallproportionofindividualsappear in the data more than once and hence that there are few individuals for which within-suject effects could e estimated, it is likely that our analysis lacks the power to identify different responses within individuals across years (Martin et al. 2011), and hence, most of the effect is attriuted to the etween-individual term. The etween-individual analysis might suggest that spatial effects on productivity drive an association, if individuals were to remain resident for longer in areas where they had een more successful. For example, Doligez et al. (2002) showed experimentally that irds use pulic information in reeding haitat selection and ase their decisions aout emigrating from a haitat patch on the perceived local reproductive success. However, ecause we fitted terms for spatial autocorrelation in the models and the familiarity effects is roust to their inclusion, we suspect that haitat-driven effect is not the case in our study. One alternative is that individuals differ in their propensity to form stale long-term relationships. Variation in ehavioral traits such as exploration ehavior or prolem solving aility (e.g., Quinn et al. 2009; Cole et al. 2011) is well documented for this species. It is possile that similar variaility exists for social ehaviors. We identified a positive effect of neighor familiarity on the proaility of nest success (Figures 5B and 6B,D). It has een shown that pied flycatchers engage in reciprocal predator moing with neighoring conspecifics (Krams et al. 2008). Long-term familiarity may increase the likelihood of such reciprocity as stale neighors are less likely to defect, perhaps ecause they join in the mo sooner, and are therefore more likely to successfully deter a predator. Further in-depth, ideally experimental, study is needed to verify whether such mechanisms operate in the great tit. Future investigation should focus on further aspects of familiarity in populations of territorial animals. Exploring the time scales on which individuals ecome familiar can ring insight into different social relationships. Juvenile irds do not have the scope for long-term familiarity and may form social onds that are very dissimilar to those they would form as adult irds. Ultimately, we seek to identify the social contexts and relationships that affect individuals in different life stages and seasons. CONCLUSIONS Social context seems to e important for reproductive success in our study. Our results are in agreement with previous evidence that reeders respond to their social environment. Social factors are widely known to affect reproduction in group-living animals (Creel and Macdonald 1995). However, some solitary species (rown ears) have also een shown to e affected y social factors (Støen et al. 2006; Ordiz et al. 2008). Effects on reeders have also een recorded for territorial ank voles (Ylönen et al. 1990). The presence and direction of effects of social environment across taxa are likely to e a product of multiple factors, such as the species ecology, mating system, levels of intraspecific competition, and ehavior. SUPPLEMENTARY MATERIAL Supplementary material can e found at eheco.oxfordjournals.org/. FUNDING Natural Environment Research Council provided financial support to A.M.G.-Z through a DPhil scholarship. We thank Marco Zhang for help with data processing and Simon Verhulst for useful suggestions aout the analysis. We also thank 4 anonymous reviewers for their extremely useful comments, which helped to improve this manuscript. Thank you to many generations of fieldworkers collecting reeding data for making this study possile. 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