We expected positive correlations of sociability with one or both fitness components only in red-grey sites, but no significant associations were found. The same was true for the trait avoidance in red-only sites. Hence, our results suggested that the observed differences in the expression of personality traits by red squirrels in red-only than in red-grey study sites were not due to selection on these traits sociability and avoidance.
It must be noted that differences in personality among animal can also affect their dispersal behaviour 7 , Since we were unable to follow juvenile cohorts throughout the dispersal and settlement process 31 , we could not rule out that selection for higher sociability occurred in red squirrels when co-existing with grey squirrels during this phase.
Studying the personality of juvenile and subadult red squirrels and its relationship with dispersal and settlement success can reveal possible selection mechanisms for certain traits that might differ between areas with and without grey squirrels. Moreover, our study may have been too short 2 years to measure any selective advantage of a given personality trait see also Despite these potential problems, we argue that it is unlikely that competition with grey squirrels asserts a selective pressure on co-occurring native red squirrels in our study system.
Grey squirrels colonized our study sites very recently, between 2 and 8 years before the arena test experiments. Hence, selection on personality traits should have occurred in only two-three generations, which seems unlikely but see Also, keeping grey squirrel densities low by removal could decrease the intensity of interspecific competition resulting in reduced selective pressure on local adaptations of personality.
The second explanation of having more red squirrels with high sociability in sites with grey squirrels is that sociability has a marked flexible component itself, or is related with other behaviours that have context-related plasticity and facilitate red squirrels to share the woodland with the invasive competitor. In woodlands occupied by both species, the interspecific overlap of the foraging-niche, daily activity pattern and home ranges core-areas are high 19 , 26 and more sociable red squirrels are likely to sustain such pressure, that increase with grey squirrel density, better than individuals with a tendency to avoid conspecifics.
Also, higher sociability could be related with a lower susceptibility to physiological stress induced by the invader Conversely, dispersal as a conditional strategy 36 , could result in red squirrels with a strong avoidance personality being the first to emigrate from woodlands invaded by grey squirrels, as supported also by low local recruitment rates of juvenile red squirrels in areas of co-occurrence Finally, Sih et al.
Our data supported this hypothesis, since we found higher between-individual variance in sociability among red squirrels co-occurring with grey squirrels than among red squirrels in red-only sites. As far as the relationship between interspecific competition and activity was concerned, we predicted more active squirrels in areas where the native species has to compete with the invader, since higher activity was thought to be related with greater food resource acquisition.
However, we did not find any differences in the activity trait comparing the two situations red-only vs red-grey. We believe this was due to our grey squirrel control to keep their densities low. At such low densities, interspecific competition for food is reduced and might be insufficient to create a marked advantage for more active red squirrels. The study was carried out in six study sites that were not identical in tree species composition or red squirrel density see also study design below.
This was addressed statistically by modelling study site nested within situation as a random effect in the MCMCglmm, thereby correcting for any potential between site variation in the test for the situation effect red-only vs red-grey situation. Since we did find a significant effect of situation on sociability expression, this effect was much larger than any potential between study site variation.
In other words, any variation in the expression of personality traits, potentially due to differences between study sites in the proportions of conifers and deciduous tree species, or other ecological variables, was much smaller than the effect of the presence of grey squirrels on the expression of sociability. Few studies investigated individual differences in personality in relation to outcomes of interspecific competition.
Experiments with two ecologically similar fish species, the threespine and ninespine sticklebacks Gasterosteus aculeatus and Pungitius pungitius showed that more active individuals of both species spend more time in open waters than in vegetation, and bolder fish had a higher prey-consumption rate than more shy individuals, irrespective of species Authors suggested that individual variation in personality traits can facilitate interspecific niche overlap, which might affect prevailing selection pressures in areas where interspecific competition is more important compared to single-species situations see also 3 , In birds, territorial aggression can be very important in the context of interspecific competition for limited high-quality nesting sites Eastern bluebirds Sialia sialis showed a strong tendency toward assortative mating in areas of both high and low interspecific competition with tree swallows Tachycineta bicolor , but pairs that behaved the most similarly and displayed either extremely aggressive or extremely non-aggressive phenotypes experienced higher reproductive success only in areas of high interspecific competition However, since the study was over a single breeding season, they could not measure ongoing selection of bluebird personality traits driven by interspecific competition.
These authors suggested that interspecific competition may select for certain personality traits and that animal personality may be an important factor influencing the outcome of interactions between native and invasive species In conclusion, our data showed that, of the different personality traits investigated, only the sociability of red squirrels changed in sites invaded by grey squirrels. Red squirrels competing with the invasive species had higher sociability scores and higher between-individual variance in sociability than in sites without grey squirrels.
Although it was recently shown that natural selection of personality traits and emergence of behavioural syndromes can be rapid 33 , we found no evidence that the observed differences in personality traits were the consequence of character displacement driven by interspecific competition.
However, differences in dispersal tendency of individual red squirrels that are either social or avoiders could explain the higher average scores of sociability in woods shared with grey squirrels than in woods without the invasive competitor.
Further studies over a longer time-period should investigate whether the flexible component of the activity, sociability and avoidance personality traits vary over time with the increasing experience of the individual squirrel. Moreover, allowing grey squirrel density to increase in some study sites might reveal whether interspecific competition can drive selection for personality phenotypes that allow red squirrels to cope with the alien invasive species.
More research on naturally co-occurring species in a guild and how both intra- and interspecific interactions contribute to the selection of personality traits is mandatory to increase our insight in the role of interspecific competition in shaping individual variation in personality.
The six red squirrel populations study sites we monitored are independent replicates in the same geographic area North Italy : three with only red squirrels and three with both red and grey squirrels. Since we used a natural setting, the six study sites were not identical in forest composition or red squirrel density.
However, the range of densities was comparable between red-only and red-grey sites Table S1 and social organisation, mating behaviour, foraging behaviour and activity patterns are similar and consistent over a wide range of habitat types 23 , 25 , 26 , Moreover, site heterogeneity was addressed statistically by adding study site nested in area-type as random effect in the MCMCglmm model see statistical analyses.
The red-grey sites are mature mixed broadleaf-conifer woods dominated by oaks Quercus robur , Q. The red-only sites are mixed conifer forests and data on forest structure and composition are reported elsewhere 37 , Trapping was carried out in two to four periods per year between January and December Supporting Information, Table S1. Traps were more or less homogeneously distributed over the study area, with average trap densities varying among sites, in relation to expected squirrel density Supporting Information, Table S1.
Traps were checked two times per day. Capture probabilities in red squirrel populations are high, and both bold and shy animals are trapped at least once per year; moreover, radio-tracking data confirm survival estimates based on CMR In the experimental sites, captured grey squirrels were removed as part of a red squirrel conservation project: animals were euthanized by CO 2 inhalation, following the EC and AVMA guidelines Doing so, grey squirrel densities were kept low, making any result of the relationships between interspecific competition and red squirrel personality conservative.
Trapping and handling squirrels complied with current laws on animal research and welfare in Italy. Trapping, marking and handling of red squirrels and arena-test experiments were carried out in accordance with the Guidelines for the Use of Animals in Research Animal Behaviour, , , I-X.
Grey squirrel control was carried out in accordance to the indications in Leary S. Details of arena tests in Supplementary material 2 and see To quantify individual personality, we performed two different experiments inside the arena: Open Field Test OFT to estimate activity and exploration levels in a novel environment and Mirror Image Stimulation MIS to test aggressiveness, sociability or avoidance towards conspecifics 28 , 40 , 41 , The two tests were performed in the same testing session, with the OFT also serving as habituation time before the MIS.
We performed arena tests for each individual only once per capture-session to reduce stress and habituation in animals minimum time between tests for the same individual: 77 days. In addition, to check the assumptions of repeatability of personality traits we repeated both experiments OFT and MIS in different capture-sessions to have at least two arena tests for most individuals.
In total we performed arena tests in red-only sites, in red-grey sites on different red squirrels 95 in red-only sites, 89 in red-grey sites; Table S1. We first transformed the time calculated by CowLog 3. To reduce the number of behaviours observed into few personality-linked variables we used the expert-based method described previously With the expert-based approach the researcher defines groups of behaviours, with each group related to a specific personality trait, summing the values of the single behaviours to obtain scores for each personality trait The method was validated by comparing its performance of grouping behaviours into personality traits with the outcomes of statistical grouping based on PCA or Factor Analysis Aggressiveness was considered as the number of attacks towards the mirror during MIS.
All analyses and interpretations were based on a multivariate mixed model fitted in a Bayesian framework using the package MCMCglmm in R Personality-trait scores were squareroot transformed before analysis.
All expert-based personality traits, survival and reproduction were treated as dependent variables after standardisation. For all expert-based personality traits, a Gaussian residual error distribution was used, while survival and reproduction were treated as binomial. As repeated observations were present, individual was added as a random effect. Because 91 individuals 60 males, 31 females were caught in at least two trapping sessions a total sample of tests , we were able to estimate the repeatability of the expert-based personality traits as the between-individual variation divided by the sum of the between-individual and residual variation.
For both the residual and between-individual variation, an unstructured variance-covariance matrix was modelled, allowing the estimation of correlations among the response variables covariance divided by the square root of the product of the variances.
Area-type, red-only vs red-grey, was treated as fixed effect, and area nested within area-type was added as random effect as a heterogeneous identity matrix to avoid pseudoreplication problems during the parameter estimation process. In addition, sex, body mass, year and arena test order first to fourth test of the same animal were added as fixed effects.
We did not include body mass measures of pregnant females to avoid a bias due to extra weight of developing embryos. The effect of sex was set to zero for the dependent variable reproduction and the effect of arena test order was set to zero for both reproduction and survival. For all fixed effects, the prior distribution was Gaussian with zero mean and variance equal to 1.
For the random effects and residual variation and inverse Wishard prior was set with diagonal elements equal to 0. The believe parameter was set to 0. Full model outputs are provided in Supporting Information, Table S3. These models were constructed as the full model except for the fixed effect of area-type full outputs in Supporting Information, Table S5.
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The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation. All authors contributed to the writing and review of the manuscript.
AS conducted the data analysis. DG and RM conceived the study design. DG conducted the data collection. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We also thank J. Mulvey, C. Godwin, F. Hayes, B. Piper, W. Boone IV, and the many volunteers whose countless hours conducting surveys made this project successful and M.
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