Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution

This commentary highlights multivariate tools that have been used by evolutionary biologists in the study of syndromes and their evolution and discusses the insights that these methods provide into evolutionary processes relative to the metric ‘syndrome deviation’ that has recently been proposed by Herczeg and Garamszegi (Behav Ecol Sociobiol 66:161–169, 2012). We clarify that non-zero phenotypic correlations arise from the joint influences of within- and between-individual correlations, whereas only non-zero between-individual correlations represent behavioural syndromes, and discuss how acknowledgement of this subtle difference between phenotypic and between-individual correlations affects the applicability of syndrome deviation for the study of behavioural syndromes.     

The behaviour of ant transporters at the old and new nests during successive colony emigrations

Colonies of the ant Temnothorax albipennis improve their collective performance over successive emigrations (Langridge et al. Behav Ecol Sociobiol 56:523–529, 2004, Behav Ecol Sociobiol 62:447–456, 2008). Here, by analysing the performance of individual transporters (workers that carry the brood, queen and a proportion of adults), we investigate whether they spend less time at the old and new nests during repeated emigrations. Transporters expedited choosing and picking up brood items at the old nest and depositing them in the new nest. Such improvements were not associated with adult transport. Generally, when carrying brood items, but not when carrying adults, transporters visited several locations in the new nest before depositing them. Transporters did not interact with other adults when depositing brood items. Consequently, reductions in depositing times are the sum of time savings made by individual transporters. By contrast, transporters spent most time interacting with other adults before picking up brood items at the old nest. As the frequency of these interactions did not decline, we suggest the behaviours of interacting adults were modified in a way that hastened their completion. Thus, reductions in picking-up times probably occur because of time saved during interactions.     

Individual deviation from behavioural correlations: a simple approach to study the evolution of behavioural syndromes

The study of correlations between different behaviours in a population—referred to as behavioural syndromes—has begun to flourish during recent years. However, the evolutionary mechanisms that cause behavioural traits to vary non-independently from each other are still poorly understood. Here, we bring behavioural syndromes into a new perspective, in which the phenomenon is regarded at the individual level and on a continuous scale instead of as a population-level presence/absence trait. As the correlation between behaviours is never perfect (i.e. r < 1), individuals are likely to vary in how consistently they behave. Therefore, we can predict that if behavioural syndromes at the population level are results of natural selection, the consistency in a suite of behaviours—and not the behavioural configuration per se—should be heritable and involve fitness advantages at the individual level. We define a variable that describes the individual deviation from the hypothetical perfect correlation predicted by the syndrome. The use of such a variable depicting the consistency of behaviours of individuals allows us to make solid evolutionary inferences about correlated behaviours from patterns of individual instead of population variation. We suggest that, by adopting the concept of syndrome deviation, understanding the evolution of behavioural syndromes and, in particular, testing competing evolutionary hypotheses about the origin of behavioural syndromes becomes possible in a more rigorous manner than before.     

Uniform predation risk in nature: common,inconspicuous, and a source of error to predation risk experiments

Previous studies indicate that when predation risk is uniform across habitats, foragers concentrate their exploitation in fewer patches. Although uniform predation risk may seem rare in nature, some scenarios might cause it. Testing all scenarios in a single experiment is unfeasible; therefore, we developed a model that points whether concentration of exploitation in specific habitats due to uniform risk requires parameter values similar to what is found in literature. This model was based on Brown’s (Behav Ecol Sociobiol 22:37–47, 1988) fitness function but rescaled to multiple habitats and predators, including uniform risk predators. Deriving function’s maximum allowed comparisons with giving-up density studies. Results showed that uniform predation risk had a u-shaped effect in habitat exploitation, causing a concentration of habitat exploitation at probabilities of survival from 0.2 to 0.8. However, the length of this interval and degree of concentration depended on the value of safety to forager fitness. Heterogeneous, nonuniform, predation risk decreases habitat exploitation where it was higher, therefore suppressing the effect of uniform risk on prey behavior. Time spent in the focal habitat and metabolic costs reduced the detectability of habitat concentration, while total time did not. We also found that uniform risk reduced accuracy of heterogeneous risk measurements. Future studies should aim to control all possible predators, as even the mild ones can induce complex behavior.     

Weighting waiting in collective decision-making

Animals searching for food, mates, or a home often need to decide when to stop looking and choose the best option found so far. By re-analyzing experimental data from experiments by Mallon et al. (Behav Ecol Sociobiol 50:352–359, 2001), we demonstrate that house-hunting ant colonies are gradually more committed to new nests during the emigration. Early in house-hunting, individual ants were flexibly committed to new nest sites. However, when carrying to a new nest had started, ants hardly ever switched preference. Using a theoretical model based on experimental data, we test at which stage flexible commitment influences speed and accuracy most. We demonstrate that ant colonies have found a good compromise between impatience and procrastination. Early flexibility combined with later rigidity is identically effective as other strategies that include flexible commitment, but it is particularly good when emigration conditions are harsh.     

Timing matters when assessing dominance and chemical signatures in the paper wasp Polistes dominulus

A recent study (Izzo et al., Behav Ecol Sociobiol 64: 857–864, 2010) reported that cuticular hydrocarbons (CHCs) correlate with fertility, not dominance, in the paper wasp Polistes dominulus thus contradicting the results of recent investigations which concluded that social dominance is the main determinant for CHC signatures in this species. We suggest here that different forms of dominance in the pre-nesting and post-nesting phases caused the apparently contradictory results. Thus the assumption that dominance behaviour in the pre-nesting stage is synonymous with dominance after colony foundation is incorrect. We provide standardised definitions for forms of “dominance” observed in the P. dominulus life cycle to avoid apparent discrepancies in the future among studies dealing with the same topics in different annual stages.     

Boldness by habituation and social interactions: a model

Most studies of animal personality attribute personality to genetic traits. But a recent study by Magnhagen and Staffan (Behav Ecol Sociobiol 57:295–303, 2005) on young perch in small groups showed that boldness, a central personality trait, is also shaped by social interactions and by previous experience. The authors measured boldness by recording the duration that an individual spent near a predator and the speed with which it fed there. They found that duration near the predator increased over time and was higher the higher the average boldness of other group members. In addition, the feeding rate of shy individuals was reduced if other members of the same group were bold. The authors supposed that these behavioral dynamics were caused by genetic differences, social interactions, and habituation to the predator. However, they did not quantify exactly how this could happen. In the present study, we therefore use an agent-based model to investigate whether these three factors may explain the empirical findings. We choose an agent-based model because this type of model is especially suited to study the relation between behavior at an individual level and behavioral dynamics at a group level. In our model, individuals were either hiding in vegetation or feeding near a predator, whereby their behavior was affected by habituation and by two social mechanisms: social facilitation to approach the predator and competition over food. We show that even if we start the model with identical individuals, these three mechanisms were sufficient to reproduce the behavioral dynamics of the empirical study, including the consistent differences among individuals. Moreover, if we start the model with individuals that already differ in boldness, the behavioral dynamics produced remained the same. Our results indicate the importance of previous experience and social interactions when studying animal personality empirically.     

Model selection criteria for overdispersed data and their application to the characterization of a host-parasite relationship

In the statistical modeling of a biological or ecological phenomenon, selecting an optimal model among a collection of candidates is a critical issue. To identify an optimal candidate model, a number of model selection criteria have been developed and investigated based on estimating Kullback’s (Information theory and statistics. Dover, Mineola, 1968) directed or symmetric divergence. Criteria that target the directed divergence include the Akaike (2nd international symposium on information theory. Akadémia Kiadó, Budapest, Hungary, pp 267–281, 1973, IEEE Trans Autom Control AC 19:716–723, 1974) information criterion, AIC, and the “corrected” Akaike information criterion (Hurvich and Tsai in Biometrika 76:297–307, 1989), AICc; criteria that target the symmetric divergence include the Kullback information criterion, KIC, and the “corrected” Kullback information criterion, KICc (Cavanaugh in Stat Probab Lett 42:333–343, 1999; Aust N Z J Stat 46:257–274, 2004). For overdispersed count data, simple modifications of AIC and AICc have been increasingly utilized: specifically, the quasi Akaike information criterion, QAIC, and its corrected version, QAICc (Lebreton et al. in Ecol Monogr 62(1):67–118 1992). In this paper, we propose analogues of QAIC and QAICc based on estimating the symmetric as opposed to the directed divergence: QKIC and QKICc. We evaluate the selection performance of AIC, AICc, QAIC, QAICc, KIC, KICc, QKIC, and QKICc in a simulation study, and illustrate their practical utility in an ecological application. In our application, we use the criteria to formulate statistical models of the tick (Dermacentor variabilis) load on a white-footed mouse (Peromyscus leucopus) in northern Missouri.     

Consistent crustaceans: the identification of stable behavioural syndromes in hermit crabs

Consistent individual variation in behaviour has been termed ‘animal personality’ and has been identified across a range of behavioural contexts including aggression, boldness in response to a threatening stimulus and exploration. When behaviours are correlated across multiple functional behavioural categories or ‘contexts’, ‘behavioural syndromes’ are said to be present. It is possible, however, that behavioural syndromes may also show consistencies. Here we investigated the presence of behavioural syndromes linking startle responses, exploration and aggression in hermit crabs and assessed their stability across two situations (low versus high predation risk). Correlation analyses detected behavioural syndromes between startle responses, a measure of ‘boldness’, and the latency to investigate a novel object, as well as the latency to attack an opponent in an aggressive context. The startle response–investigation and startle response–aggression syndromes were stable between situations, whilst there was a lack of relationship between investigation and aggression in each situation. Here we propose that these consistent individual differences in the expression of behavioural syndromes reveal the presence of animal personality, manifesting in not just one, but a suite of interacting traits.     

Do honey bees tune error in their dances in nectar-foraging and house-hunting?

The "tuned-error" hypothesis states that natural selection has tuned the divergence angle in the dances of the honey bee to produce an optimal scatter of recruits across a resource. Weidenmüller and Seeley (Behav Ecol Sociobiol 46:190–199, 1999) supported this hypothesis by finding smaller divergence angles in dances indicating potential home sites, which are always point sources, than in dances indicating food sources, which often occur in patches. This study tested for the same effect, but controlled for variables, e.g., substrate and context, that may have confounded those results. When performed on the same substrate, divergence angle does not differ between dances for the two resources. Furthermore, dances performed for food within an observation hive exhibit significantly greater divergence angle when performed on comb (as Weidenmüller and Seeley measured food dances) than on hardware cloth (as they measured home-site dances on a swarm). These findings suggest that the angular variance in direction indication in dances is more likely an artifact of physical constraints, rather than an adaptive modification of a behavior that a bee could perform more precisely.     

How experienced individuals contribute to an improvement in collective performance in ants

Certain groups of organisms are capable of improving their collective performance with experience. In a recent study, we demonstrated that, over successive emigrations, colonies of the ant Temnothorax albipennis are able to improve their collective performance by reducing the time taken to complete an emigration (Langridge et al., Behav Ecol Sociobiol 56:523–529, 2004). In this paper, by recording the performance of individually marked workers during repeated emigrations, we were able to analyse some of the ways in which time gains are achieved. We found that: (1) those transporters that also transported in the preceding emigration began to transport earlier in the current emigration and, in the majority of emigrations, transported more items than those transporters that had not transported in the preceding emigration; (2) the time that elapsed before the first item was transported into the new nest reduced over successive emigrations, and this first item was, in the majority of emigrations, carried by a transporter that had also transported in the preceding emigration; (3) the number of adults that were transported reduced over successive emigrations. Our results strongly suggest that the behaviour of transporters that also transported in a preceding emigration may be modified as a result of their experience and that, consequently, their efforts in the next emigration make a major contribution to the improved performance of the colony as a whole.     

When does bearing magnets affect the size of deflection in clock-shifted homing pigeons?

Pigeons whose internal clock is shifted by 6 h show deflections from the direction of untreated controls, yet these deflections are often smaller than predicted. Magnets temporarily disabling the magnetic compass increased these the deflections significantly (R. Wiltschko and Wiltschko 2001), indicating a compromise between sun compass and magnetic compass. – Recently, Ioalé et al. (2006) claim that they could not replicate our findings. The reason lies in a difference in the behavior of the clock-shifted pigeons without magnets: in the study of Ioalè et al. (2006), their deflections was already almost as large as that of our pigeons carrying magnets. This difference is probably caused by the limited experience of the pigeons of Ioalè et al. (2006): Their birds, in contrast to ours, had not used their sun’ compass during extended homing flights at various times of the year and, not having been faced with the necessity to compensate the saisonal changes of the sun’s arc, gave the sun compass more weight than our birds did.A comment to the paper by Ioalè, Odetti and Gagliardo (2006) Behav Ecol Sociobiol 60: 516–521.     

Sine-skewed axial distributions with an application for fallen tree data

An axis is an undirected line where there is no reason to distinguish one end of the line from the other. Phenomena in nature that can be described as axial data are numerous. In this paper a method of trigonometric moments for the axial normal or axial von Mises distribution as an alternative to the method by Arnold and SenGupta (Environ Ecol Stat 13:271–285, 2006) is discussed. Sine-skewed axial Jones–Pewsey, von Mises and wrapped Cauchy distributions are introduced as special cases of a more general construction of skew axial distributions. As an example the methods are applied to a data set which consists of the orientations of logs on the floor of a primeval spruce forest.     

Behavioral correlations across activity, mating, exploration, aggression, and antipredator contexts in the European house cricket, Acheta domesticus

Recently, there has been increasing interest in behavioral syndrome research across a range of taxa. Behavioral syndromes are suites of correlated behaviors that are expressed either within a given behavioral context (e.g., mating) or between different contexts (e.g., foraging and mating). Syndrome research holds profound implications for animal behavior as it promotes a holistic view in which seemingly autonomous behaviors may not evolve independently, but as a “suite” or “package.” We tested whether laboratory-reared male and female European house crickets, Acheta domesticus, exhibited behavioral syndromes by quantifying individual differences in activity, exploration, mate attraction, aggressiveness, and antipredator behavior. To our knowledge, our study is the first to consider such a breadth of behavioral traits in one organism using the syndrome framework. We found positive correlations across mating, exploratory, and antipredatory contexts, but not aggression and general activity. These behavioral differences were not correlated with body size or condition, although age explained some of the variation in motivation to mate. We suggest that these across-context correlations represent a boldness syndrome as individual risk-taking and exploration was central to across-context mating and antipredation correlations in both sexes.     

Is bird song a reliable signal of aggressive intent? A reply

We advocate assessing the reliability of signals of aggressive intent by eliciting aggressive signaling from a subject, giving the subject an opportunity to attack a model, and testing whether the subject’s displays predict a subsequent attack. Using this design, we found that most singing behaviors are poor predictors of attack in song sparrows (Melospiza melodia). Laidre and Vehrencamp (Behav Ecol Sociobiol, DOI 10.1007/s00265-007-0539-3, 2008) suggested altering our experimental design to make the model more realistic; it remains to be seen whether such design changes would change the association between display and attack. Laidre and Vehrencamp (Behav Ecol Sociobiol, DOI 10.1007/s00265-007-0539-3, 2008) also suggested that the reliability of soft song, the one display that predicts attack in song sparrows, can be explained by a vulnerability cost. We question the rationale for a vulnerability cost for this display and suggest instead that soft song has a competing functions cost, in that, by using soft song to counter an intruder, a male sacrifices other possible functions of vocal signaling.     

Testing for between individual correlations of personality and physiological traits in a wild bird

Recently, integration of personality traits into a ‘pace-of-life syndrome’ (POLS) context has been advocated. To be able to understand how an individual’s behavioural, physiological and life history traits may coevolve, we need to jointly quantify these traits in order to study their covariance. Few studies have established links between personality and immunity properties of an individual. We here examined covariation of a measure of skeletal size (tarsus length), three behavioural traits (activity, handling aggression and breath rate) and two immunological traits (IgG level and haematocrit), in 592 wild caught blue tits. Many individuals (201) were tested more than once, allowing quantification of individual consistency of all traits and partition of the covariances between the traits, using a multivariate mixed model, into between individual and residual covariances. We find individual consistency of all behavioural traits, indicating that these capture aspects of blue tit adult personality and also the physiological measures are repeatable. Contrary to the POLS expectation, we find no overall significant individual level correlation structure between these traits and a factor analytical approach confirmed that between individual correlations across traits were not due to a common (POLS) factor or driven by size (tarsus length). Based on a published power study, we conclude that there is no common syndrome of individual level covariance between personality and physiological traits in wild blue tits or that the effect sizes, such a syndrome generates, are too low (r?<?0.3) to detect. Future field-based work should be designed to explore low effect sizes and strive to measure specific traits whose involvement is implicated to have large effect sizes as based on, e.g. laboratory findings.     

Current versus future reproduction: an experimental test of parental investment decisions using nest desertion by mallards (<Emphasis Type="Italic">Anas platyrhynchos</Emphasis>)

Past investment in offspring may be important in determining a parent's ability to reproduce in the future and, hence, should affect the relative value of current offspring. However, there have been surprisingly few clear tests of whether animals actually adjust parental care in response to diminished opportunities for future reproduction. We modified the experimental protocol of Sargent and Gross [Behav Ecol Sociobiol (1985) 17:43–45] to examine offspring desertion by mallards ( Anas platyrhynchos), and decoupled the influence of past investment from expected current benefits by controlling for the effect of offspring age on clutch value. Using 9 years of nest mortality data, we accounted for the increasing prospects of egg survival with clutch age by calculating clutch sizes throughout incubation with equivalent expected benefits. Applying this approach, we experimentally reduced 203 clutches at two different incubation stages such that they had equivalent expected benefits but differed in the amount of past investment. Nest desertion rates did not differ between early- and late-incubated clutches that had equivalent expected benefits. Rather, the probability of desertion increased with the severity of the clutch reduction treatment. These results suggest that female mallards adjust parental care according to the expected benefits of current offspring, rather than to diminished prospects for future reproduction due to past investment. We further examined whether females assessed expected benefits on the basis of clutch size alone or clutch size adjusted for the age of the clutch. Using Akaike's Information Criterion, the most parsimonious model to explain the probability of deserting an experimentally reduced clutch included both the proportion of the clutch remaining and clutch age. Thus, female mallards appear to fine-tune their level of parental care not only according to the relative number of offspring in the clutch, but also to the increased prospects for offspring survival as they age.     

Patterns of body mass senescence and selective disappearance differ among three species of free-living ungulates

Declines in survival and reproduction with age are prevalent in wild vertebrates, but we know little about longitudinal changes in behavioral, morphological, or physiological variables that may explain these demographic declines. We compared age-related variation in body mass of adult females in three free-living ungulate populations that have been the focus of long-term, individual-based research: bighorn sheep (Ovis canadensis) at Ram Mountain, Canada; roe deer (Capreolus capreolus) at Trois Fontaines, France; and Soay sheep (Ovis aries) on St. Kilda, Scotland. We use two recently proposed approaches to separate contributions to age-dependent variation at the population level from within-individual changes and between-individual selective disappearance. Selective disappearance of light individuals in all three populations was most evident at the youngest and oldest ages. In later adulthood, bighorn sheep and roe deer showed a continuous decline in body mass that accelerated with age while Soay sheep showed a precipitous decrease in mass in the two years preceding death. Our results highlight the importance of mass loss in explaining within-individual demographic declines in later adulthood in natural populations. They also reveal that the pattern of senescence, and potentially also the processes underlying demographic declines in late life, can differ markedly across related species with similar life histories.     

How stable are personalities? A multivariate view of behavioural variation over long and short timescales in the sheepshead swordtail,Xiphophorus birchmanni

Many studies have revealed repeatable (among-individual) variance in behavioural traits consistent with variation in animal personality; however, these studies are often conducted using data collected over single sampling periods, most commonly with short time intervals between observations. Consequently, it is not clear whether population-level patterns of behavioural variation are stable across longer timescales and/or multiple sampling periods or whether individuals maintain consistent ranking of behaviours (and/or personality) over their lifetimes. Here, we address these questions in a captive-bred population of a tropical freshwater poeciliid fish, Xiphophorus birchmanni. Using a multivariate approach, we estimate the among-individual variance-covariance matrix (I), for a set of behavioural traits repeatedly assayed in two different experimental contexts (open-field trials, emergence and exploration trials) over long-term (56 days between observations) and short-term (4-day observation interval) time periods. In both long- and short-term data sets, we find that traits are repeatable and the correlation structure of I is consistent with a latent axis of variation in boldness. While there are some qualitative differences in the way individual traits contribute to boldness and a tendency towards higher repeatabilities in the short-term study, overall, we find that population-level patterns of among-individual behavioural (co)variance to be broadly similar over both time frames. At the individual level, we find evidence that short-term studies can be informative for an individual’s behavioural phenotype over longer (e.g. lifetime) periods. However, statistical support is somewhat mixed and, at least for some observed behaviours, relative rankings of individual performance change significantly between data sets.