Abstract: Animal groups often represent nonrandom subsets of individuals, and increasing evidence indicates that individuals may sort among groups based on their personalities. The size of a group can predict its personality composition in some species due to differential suitability of a personality for groups of certain sizes, and the group itself may function more effectively if particular personality types are present. We quantified cliff swallow (Petrochelidon pyrrhonota) behavioral measures using linear and generalized linear mixed models to identify whether they: (1) varied among individuals within colonies and among colonies, (2) were related to reproductive success, and (3) predicted levels of parental care. Significant among-individual and among-colony site variation in a cliff swallow’s latency to enter its nest when presented with a novel stimulus was revealed. We also found significant among-individual variation in the number of attacks directed toward a novel stimulus at the nest and in the response to broadcast of a cliff swallow alarm call recording, but among site variation in these measures was not significant. We did not find evidence for behavioral syndromes linking the personalities measured. Differences among individuals in latency to enter the nest and the number of attacks were not significantly related to reproductive success or to the extent to which birds fed their nestlings. However, extent of nestling feeding was significantly predicted by the number of mist net captures. The limited evidence in general of systematic variation in the behavior we measured among cliff swallow colonies may reflect the different and sometimes opposing selection pressures on behavior in different social environments. Future work should perhaps examine variation in other behavioral traits, such as foraging, in cliff swallow colonies of different sizes.
Discussion
Our study revealed significant among-individual and among-colony site variation in a cliff swallow’s latency to enter its nest when presented with a novel stimulus. We also found significant among-individual variation in the number of attacks directed toward a novel stimulus at the nest and in the response to broadcast of cliff swallow alarm call recordings, but among site variation in these measures was not significant. The behavioral measures were not correlated with one another or with the number of times an individual was captured by mist net. Differences among individuals in latency to enter the nest and the number of attacks were not significantly related to reproductive success or to the extent to which birds fed their nestlings. However, extent of nestling feeding was significantly predicted by the number of mist net captures, with pairs that were captured more on average also making more frequent food deliveries to the nest.
Measures and correlates of personality
Despite evidence for relatively high repeatability in both behavioral measures that involved a reaction to a novel stimulus, we did not find support for a behavioral syndrome [5]. This suggests that Latency to enter nest and Number of attacks are independent facets of personality [55, 65, 66]. There is no consensus on which commonly identified personality axes are thought to be measured by behavioral tests involving novel objects or novel environments: some studies use novelty tests to measure personality along the avoidance-exploration axis [22, 67, 68], whereas others use novelty tests to measure personality along the shy-bold axis [65, 69–71]. In the case of novel item tests, the context in which the novel item is introduced may cause further inconsistencies in measured behaviors. For example, coyotes (Canis latrans) showed little avoidance toward a novel stimulus in unfamiliar surroundings but showed avoidance and neophobic reactions toward the same stimuli in familiar surroundings [35]. In our study, the novel stimulus was added to the focal bird’s own nest, a very familiar environment for the bird, and thus strong behavioral responses were expected. In this context, Latency to enter nest may be a measure of personality along the exploration-avoidance axis as the bird determines whether the novel stimulus is a threat, whereas Number of attacks may be a measure of personality along the shy-bold axis as the bird risks injury while responding to the novel stimulus. Number of attacks might alternatively reflect defensive aggression, which describes motor patterns exhibited by a socially aggressive animal but typically directed at a predator or threatening situation rather than a conspecific individual [72]. Regardless of which personality axes are represented, we can conclude that our measured behaviors are independent.
We were surprised that neither Latency to enter nest or Number of attacks were correlated with Number of captures, because the mist net, although perhaps less conspicuous, seemingly also acts as a novel stimulus or possibly a threat, at least after first capture (see [73]). After several successive days of netting at a colony site, cliff swallows learn to avoid mist nets, possibly because of the trauma associated with capture [73]. Active North American red squirrels (Tamiasciurus hudsonicus) were trapped significantly more frequently than less active squirrels [74]. Thus, Number of captures may be a measure of personality known as activity [22], which tends to generally describe an animal’s propensity to move.
Personality can affect both reproductive success and survival in some species [74–76, 60]. A meta-analysis found that exploration had a positive effect on survival and that boldness had a positive effect on reproductive success but a negative effect on survival [77]. The lack of an association in our study between Reproductive success and Latency to enter nest (possibly a measure of exploration) and Number of attacks (possibly a measure of boldness) may have been influenced by our sample size which was relatively small for a demographic study and may have reduced our ability to find a relationship between neophobia measures and reproductive success. For example, slight differences in fitness components (such as annual reproductive success), while evolutionarily significant over the long term, may often be indistinguishable empirically from null models due to a lack of power [78].
In some animals, more explorative individuals find food sources faster than less explorative individuals [79], and fast-exploration has been linked to increased nestling feeding rates and increased reproductive success [80]. However, Latency to enter nest was not a predictor of the number of food deliveries to a nest in cliff swallows. This lack of a relationship, as well as that for Number of attacks, may have resulted from pooling food deliveries by both parents to a nest and/or by using combined personality scores of both parents. This may have masked sex-differences in parental provisioning related to personality. For example, Mutzel et al. [80] found that fast-exploring female Eurasian blue tits (Cyanistes caeruleus) fed their offspring at higher rates, whereas exploratory personality of males was unrelated to nestling feeding rate. We found evidence in cliff swallows for a relationship between mean Number of captures and the number of parental food deliveries to a nest. Number of captures may be a measure of an individual’s activity personality such that individuals captured more often in mist nets are those that are most active near the nest. This may explain why these birds are also the ones that visit their nest more frequently with food if they are not traveling as far from the nest during foraging.
Personality and coloniality
We did not find significant repeatability at the colony-site level for Number of attacks, Number of captures, or Alarm call response, suggesting that cliff swallows may not sort among colonies based on these behavioral measures. Both the rank order of neophobia trials and the rank order of alarm call trials were significant covariates, suggesting habituation to the novel stimulus and the alarm call play back [81]. Such habituation could reduce our ability to detect repeatable behavior at the colony-site level should habituation lead to reduced variability in the measured behavior across colonies.
The significant repeatability at the colony-site level for Latency to enter nest suggests that cliff swallows may sort into colonies based on this measure of personality. Individuals at the much larger CR-1 and Junkyard colonies were generally quicker to enter their nests when presented with a novel stimulus than individuals at the smaller McDougals colonies (Table 1, Fig 3). Our result contrasts with that of Dardenne et al. [12], who found higher levels of neophobia among barn swallows in larger colonies. They suggested that neophobic barn swallows may benefit from occupying a large colony where they can rely on other, more explorative individuals to lead them to food (c.f. [82]). If this scenario applies to cliff swallows, we would expect neophobic individuals to make fewer food deliveries, as they must wait to be led to food; however, we observed more frequent feeding visits at the small McDougals colonies compared to the larger colonies at CR-1 and Junkyard.
Increased predation odds at small versus large colonies may explain why more neophobic cliff swallows were found at the McDougals site. It is widely believed that predation risk of an individual is decreased when it occupies a large group [23–27, 83]. Without the safety in numbers afforded by large groups, animals in small groups may need to be more cautious to minimize predation risk, possibly explaining the increased neophobia in smaller cliff swallow colonies.
In great tits (Parus major), slow-exploring (neophobic) individuals were less aggressive toward conspecifics whereas fast-exploring individuals were more aggressive [84]. This relationship may also explain why cliff swallow individuals tended to be more neophobic at the smaller colony site. Not only were the CR-1 and Junkyard colonies much larger in size than at McDougals, but the nests at the larger colonies were also more densely packed (Fig 1), making avoidance of social interactions among neighboring individuals more difficult. A socially non-aggressive individual would be at a disadvantage in such a crowded colony where it would frequently need to fend off intruding neighbors [37]. Thus, there may be an advantage for neophobic individuals to choose small colonies where there is less opportunity for frequent social interaction.
Although cliff swallows might sort into different colony sites based on where they fall within the exploration-avoidance personality axis (as measured by Latency to enter nest), we cannot rule out that the observed behavioral variation among sites was instead shaped by the social environment after birds had already settled within a colony [85]. Behavioral plasticity shaped by changes in the social environment has been described in several birds [86–92], and most show a decrease in individual neophobia when in a group setting. King, Williams, and Mettke-Hofmann [93] found that individual Gouldian finches (Erythrura gouldiae) adjusted their boldness behavior to be more similar to that of their partner. We did not make comparisons of neophobia at the partner level over time, but on several occasions, a neophobia trial at the McDougals colony site elicited an almost colony-wide response, with several colony members from nearby nests hovering in front of the focal nest to inspect the novel stimulus. This collective response often occurred when the nest resident alarm-called in response to the piece of marking tape, and was not observed at the larger CR-1 or Junkyard colony sites. Bystanders at the McDougals site were possibly influenced by the alarm-calling (neophobic) nest resident, making bystanders more aware of the stimulus and potentially less likely to respond later when their own nests were tested. However, if this were the case, we should have seen overall shorter latencies to enter nest at the McDougals site compared to other sites.
In the only other study relating personality to colony size in cliff swallows, Roche and Brown [14] found some evidence for among-colony variation in vigilance behavior, but there was no clear relationship between vigilance level and colony size per se. While higher levels of neophobia in smaller colonies (this study) might lead to greater vigilance at those sites, vigilance can also reflect awareness of neighbors and the need to be alert to defend one’s nest from conspecifics, of which there are more in larger colonies. Possibly for this reason no systematic relationship between vigilance and colony size was detected [14].
We acknowledge some limitations to the present study. For example, the removal of ectoparasites, while necessary to increase the number of completed behavioral observations because of high nest failure rates due to swallow bug parasitism [37], might have altered the natural behavior of individuals in unknown ways. Perhaps the time necessary for parents to forage to provision offspring was reduced when nests were freed from parasitism [94, 95]. The laborious nature of these observations precluded conducting them at more colony sites, and thus we could not rigorously test the effect of colony size on individual behavior. However, we selected colony sites that were quite different in size while at the same time similar in other ways (e.g., all were in box-shaped concrete culverts; Fig 1), increasing the likelihood that observed differences among sites were related to colony size. Finally, given the highly social nature of cliff swallows, neophobia tests could not be conducted in isolation. As such, individuals may have seen the novel stimulus being presented at another nest nearby, and this may have happened more often than the protocol assumed. We know this occurred repeatedly at the McDougals site. Such unintended exposure (and resulting habituation) would have made us less likely to detect an effect of the novel stimulus, but we found the opposite result at McDougals, where neophobia was greater among residents.
Conclusions
We were surprised to find only limited evidence in general of systematic variation in behavioral measures of neophobia and risk-taking among cliff swallows in different colonies. This may reflect the divergent and sometimes opposing selection pressures on behavior in different social environments. For example, bold (less neophobic) individuals could benefit in a larger colony by not fleeing at every alarm call and thus not frequently leaving their nest unattended and susceptible to theft of nesting material, egg loss, or brood parasitism from their many conspecific neighbors [37]. However, large colonies are also attacked by predators more often, to a degree that per capita predation risk is greatest in the very largest colonies [37]. Thus, bold individuals in a large colony, while minimizing interference from neighbors by not consistently reacting to alarm calls, might thus have a higher overall risk of predation. The result would be no net advantage for bold versus shy individuals in colonies of different sizes, and thus potentially no selection for bold or shy personalities in the first place. Future work should perhaps examine variation in other behavioral traits, such as foraging, in cliff swallow colonies of different sizes.
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