Exploring the effects of individual traits and within-colony variation on task differentiation and collective behavior in a desert social spider

Social animals are extraordinarily diverse and ecologically abundant. In understanding the success of complex animal societies, task differentiation has been identified as a central mechanism underlying the emergence and performance of adaptive collective behaviors. In this study, we explore how individual differences in behavior and body size determine task allocation in the social spider Stegodyphus dumicola. We found that individuals with high body condition indices were less likely to participate in prey capture, and individuals’ tendency to engage in prey capture was not associated with either their behavioral traits or body size. No traits were associated with individuals’ propensity to participation in web repair, but small individuals were more likely to engage in standard web-building. We also discovered consistent, differences among colonies in their collective behavior (i.e., colony-level personality). At the colony level, within-colony variation in behavior (aggressiveness) and body size were positively associated with aggressive foraging behavior. Together, our findings reveal a subtly complex relationship between individual variation and collective behavior in this species. We close by comparing the relationship between individual variation and social organization in nine species of social spider. We conclude that intraspecific variation is a major force behind the social organization of multiple independently derived lineages of social spider.     

Division of labor in a dynamic environment: response by honeybees (Apis mellifera) to graded changes in colony pollen stores

 A fundamental requirement of task regulation in social groups is that it must allow colony flexibility. We tested assumptions of three task regulation models for how honeybee colonies respond to graded changes in need for a specific task, pollen foraging. We gradually changed colony pollen stores and measured behavioral and genotypic changes in the foraging population. Colonies did not respond in a graded manner, but in six of seven cases showed a stepwise change in foraging activity as pollen storage levels moved beyond a set point. Changes in colony performance resulted from changes in recruitment of new foragers to pollen collection, rather than from changes in individual foraging effort. Where we were able to track genotypic variation, increases in pollen foraging were accompanied by a corresponding increase in the genotypic diversity of pollen foragers. Our data support previous findings that genotypic variation plays an important role in task regulation. However, the stepwise change in colony behavior suggests that colony foraging flexibility is best explained by an integrated model incorporating genotypic variation in task choice, but in which colony response is amplified by social interactions. Received: 17 October 1998 / Received in revised form: 11 March 1999 / Accepted: 12 March 1999     

What drives flexibility in primate social organization?

The importance of behavioral flexibility for understanding primate ecology and evolutionary diversity is becoming increasingly apparent, and yet despite the abundance of long-term studies across diverse sampling localities, we still do not understand the myriad factors responsible for among-site variation in species’ social organization. The goals of our study were to address this question via three main objectives: to quantify social organization flexibility (i.e., across-site intraspecific variation) of well-studied primate species, test the idea that closely related species exhibit similar levels of flexibility, and test hypotheses explaining variation in social organization flexibility among primate species. We obtained data for a total of 175 study sites from 32 primate species representing all major primate clades. We employed phylogenetic principal components analysis to quantify social organization flexibility for each species. We quantified the phylogenetic signal in social organization flexibility and then evaluated the best predictors of flexibility. We found that mean group size was positively related to social organization flexibility. Large social groups may be more flexible because the foraging costs and predation risk associated with adding or subtracting individuals are lower compared to small social groups. There was some support that absolute brain size and the presence of fission–fusion dynamics were also related to high levels of social organization flexibility, suggesting that cognitive ability and/or within-site behavioral flexibility may also lead to increased variation across sites. Our results serve as an early step in understanding the patterns and processes related to social organization flexibility in primates and other social mammals.     

Individual variation in winter foraging of black-capped chickadees

Summary Wintering black-capped chickadees (Paridae: Parus atricapillus) in northwestern Massachusetts showed a high degree of individual variation in foraging behavior. After accounting for the effects of different habitats and weather conditions, individual differences comprised 6–17% of the total observed variation in four measures of foraging location and rate of feeding. Differences between age and sex groups were not significant and explained comparatively little variation (0.0–1.4%). The chickadees did not fall into a few distinct behavioral categories but instead showed continuous variation on all measures of foraging behavior. It appeared that some variation among individuals was a consequence of behavioral convergence within social groups, since birds that were observed together were more similar in their foraging than expected by chance, after taking habitat differences into account. Our results therefore do not support the interpretation that individual variation in feeding behavior serves to reduce exploitation competition within social groups.     

A comparison of visual and olfactory learning performance in the bumblebee Bombus terrestris

Animals use cues from a range of sensory modalities to discriminate stimuli and as predictors of reward. Whilst there is appreciable variation in the cognitive performance of animals, we know surprisingly little about the extent to which learning varies among individuals across different sensory modalities. Do individuals that are good at learning in one sensory modality also perform well in another (performance is correlated between modalities), or do individuals demonstrate specialisation in learning performance in one modality (trading-off performance between modalities)? We tested these hypotheses by examining the performance of 76 Bombus terrestris workers, from four colonies, in both an odour-and visual learning task. Olfactory learning was assessed using proboscis extension reflex (PER) conditioning and visual (colour) learning was examined using a well-established free-flying paradigm. Our results showed neither a correlation, nor a trade-off, in individual performance for learning tasks using different sensory modalities. However, there was considerable variation among workers within each colony in their performance in both learning tasks. This extent of interindividual variation in learning ability across sensory modalities could be adaptive for colonies dealing with changeable foraging conditions. There was also significant intercolony variation in final task performance level in the olfactory learning task, and both the strength and persistence of blue preference in the colour learning task. This is the first study to demonstrate variation in olfactory learning performance across multiple bumblebee colonies using PER conditioning, suggesting this is an effective paradigm for assessing associative olfactory learning performance both within and among colonies.     

Group leadership depends on energetic state in a nomadic collective foraging caterpillar

Group living is a common strategy among animals and has arisen independently in over 300 species of Lepidoptera. Yet, activity synchrony between individuals is necessary to derive the benefits that ensue from an aggregated lifestyle. Which individuals decide which activities to perform and when to perform them is, therefore, a fundamental question. In some species of social caterpillars and sawflies, the role of a potential behavioral polyethism between individuals has been suggested, whereby certain individuals are consistently more likely to initiate and lead a foraging event. However, in these cases, evidence in support of division of labor is lacking. This study was undertaken to determine if certain individuals of Malacosoma disstria are more likely to be consistent group leaders or if transient leaders could be predicted by the differences in energetic states between individuals. The results of this study indicate that unfed caterpillars initiate foraging bouts and are more likely to lead locomotion. There was no size or sex-based bias in those individuals that acted as temporary leaders. Consistent behavioral differences between individuals, if they exist, are therefore not necessary to explain task allocation and synchronization during foraging in this species.     

Network analysis reveals contrasting effects of intraspecific competition on individual vs. population diets

Optimal foraging theory predicts that individuals should become more opportunistic when intraspecific competition is high and preferred resources are scarce. This density-dependent diet shift should result in increased diet breadth for individuals as they add previously unused prey to their repertoire. As a result, the niche breadth of the population as a whole should increase. In a recent study, R. Svanb?ck and D. I. Bolnick confirmed that intraspecific competition led to increased population diet breadth in threespine stickleback (Gasterosteus aculeatus). However, individual diet breadth did not expand as resource levels declined. Here, we present a new method based on complex network theory that moves beyond a simple measure of diet breadth, and we use the method to reexamine the stickleback experiment. This method reveals that the population as a whole added new types of prey as stickleback density was increased. However, whereas foraging theory predicts that niche expansion is achieved by individuals accepting new prey in addition to previously preferred prey, we found that a subset of individuals ceased to use their previously preferred prey, even though other members of their population continued to specialize on the original prey types. As a result, populations were subdivided into groups of ecologically similar individuals, with diet variation among groups reflecting phenotype-dependent changes in foraging behavior as prey density declined. These results are consistent with foraging theory if we assume that quantitative trait variation among consumers affects prey preferences, and if cognitive constraints prevent individuals from continuing to use their formerly preferred prey while adding new prey.     

Effects of body mass,age, dominance and parasite load on foraging time of bighorn rams,<Emphasis Type="Italic"> Ovis canadensis</Emphasis>

In sexually dimorphic ungulates, males generally spend less time foraging than females, possibly because of difference in body mass or because of the energetic requirements of lactation. The relationship between body size and foraging time has received little attention at the intra-specific level, because few studies have documented activity budgets for individuals of known size. Bighorn rams are a good model to explore how body mass affects foraging time, because they range in mass from 55 to 140 kg. We examined how the foraging time of bighorn rams varied according to individual characteristics. We observed rams in a marked population and constructed time budgets during the 3 months preceding the rut. We determined ram social rank based on agonistic encounters and collected fecal samples to count lungworm larvae. Time spent foraging was negatively correlated with body mass. After accounting for age differences, larger rams spent less time foraging and more time lying than smaller rams. Among rams aged 6–12 years, dominants spent less time feeding than subordinates, while fecal output of lungworm larvae was negatively correlated with foraging time for rams of all ages. Body mass accounts for much of the individual variation in foraging time, suggesting that sexual dimorphism is important in explaining differences in feeding time between males and females.Communicated by P. Heeb     

Does risk of intraspecific interactions induce shifts in prey-size preference in aquatic predators?

Interactions between foragers may seriously affect individual foraging efficiency. In a laboratory study of handling time, prey value and prey-size preference in northern pike and signal crayfish, we show that risk of intraspecific interactions between predators does not affect handling time or value of prey. However, the presence of agonistic intraspecific interactors shifts prey-size preference in these predators. Neither northern pike nor signal crayfish foraging alone show a prey-size preference, while pike foraging among conspecifics prefer small prey, and crayfish foraging in groups prefer large prey. We ascribe the different outcomes in prey preference to differences in susceptibility to interactions: northern pike under risk avoid large prey to avoid long handling times and the associated risk of interactions, while signal crayfish foraging among conspecifics may defend themselves and their prey during handling, and thus select prey to maximise investment. In addition, the value of pike prey (roach) is low for very small prey, maximises for small prey, and then decreases monotonically for larger prey, while crayfish prey (pond snail) value is low for very small prey, has a maximum at small prey, but does not decrease as much for larger prey. Therefore, a large and easily detected snail prey provides a crayfish with as much value as a small prey. We conclude that interaction risk and predator density affect prey-size preference differently in these aquatic predators, and therefore has different potential effects on prey-size structure and population and community dynamics. Received: 4 October 1999 / Revised: 20 March 2000 / Accepted: 27 May 2000     

Can environmental heterogeneity explain individual foraging variation in wild bottlenose dolphins (<Emphasis Type="Italic">Tursiops</Emphasis> sp.)?

Because behavioral variation within and among populations may result from ecological, social, genetic and phenotypic differences, identifying the mechanism(s) responsible is challenging. Observational studies typically examine social learning by excluding ecological and genetic factors, but this approach is insufficient for many complex behaviors associated with substantial environmental variation. Indian Ocean bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia show individual differences in foraging tactics, including possible tool use with marine sponges and social learning may be responsible for this diversity. However, the contributions of ecological factors to the development of these foraging tactics were not previously investigated. Here, we determined the relationship between ecological variables and foraging tactics and assessed whether differences in habitat use could explain individual differences in foraging tactics. We monitored 14 survey zones to identify how foraging tactics were spatially distributed and matched behavioral data to the ecological variables within each zone. Three of four foraging tactics were significantly correlated with ecological characteristics such as seagrass biomass, water depth, presence of marine sponges and season. Further, individual differences in habitat use were associated with some tactics. However, several tactics overlapped spatially and previous findings suggest demographic and social factors also contribute to the individual variation in this population. This study illustrates the importance of environmental heterogeneity in shaping foraging diversity and shows that investigating social learning by ruling out alternative mechanisms may often be too simplistic, highlighting the need for methods incorporating the relative contributions of multiple factors.     

Risk aversion in hand-reared bananaquits

Summary To study risk aversion in hand-reared bananaquits (Coereba flaveola) we placed individuals in a cage with a 1 m² floral board having a random array of 85 yellow and 85 red artificial flowers. Flowers of one color were filled with the same quantity of nectar (constant flowers), whereas flowers of the other color were filled with variable quantities of nectar (variable flowers). The constant and variable flowers had identical mean contents, only their variances differed. After three presentations, the constant flowers were made variable and vice versa to control for color preferences. Naive foragers tended to avoid variable flowers. The degree of risk aversion was influenced by previous experience, the relative variability of the variable flowers, and flower color. Variable flowers having similar coefficients of variation, but different reward variables (volume or concentration) resulted in similar levels of risk aversion. Within single foraging episodes the following was observed: sequences of constant flowers increased while sequences of variable flowers remained similar to random foraging; the probability of revisiting a constant flower was higher than revisiting a variable flower; the average amount of nectar consumed from constant and variable flowers was similar within the assessment periods (prior to favoring constant flowers); the proportion of visits falling below the mean expected reward during the assessment period or its inverse (the proportion visited with at least the equivalent of the mean) may be a cue used for risk aversion; risk aversion persisted through long foraging bouts despite changed nectar distributions suggesting that the bananaquits did not track resource distributions well within foraging bouts.     

Boldness is influenced by sublethal interactions with predators and is associated with successful harem infiltration in Madagascar hissing cockroaches

One of the contemporary challenges of the behavioral syndromes literature is to identify how individual variation in behavior is determined, and whether this variation impacts ecological success. Although variation in experience is an obvious potential driver of intraspecific behavioral variation, predicting the impact of experience on suites of correlated behavioral traits is less intuitive. Specifically, if experience impacts traits that shape individuals' success in multiple contexts (e.g., foraging and anti-predator behavior), then experience could generate cross-contextual performance trade-offs associated with behavioral spillover. In the present study, we explore how sublethal experience with predators impacts various aspects of male behavioral tendencies in the Madagascar hissing cockroach, Gromphadorhina portentosa. First, we found that males' activity level and boldness were correlated together in the form of a behavioral syndrome. Second, we found that repeated sublethal interactions with predators shifted male boldness but not activity level, thus suggesting that the syndrome's constituent traits can respond to experience at least semi-independently. Third, we discovered that although predator exposure only influenced boldness, we found that boldness was highly correlated with males' ability to obtain rewarding positions in the harems of rival males. Taken together, our data suggest (but do not yet confirm) that although sublethal exposure to predators influences only a narrow subset of male's behavioral tendencies, these effects could still have nonintuitive consequences for males' success in functionally dissimilar ecological contexts (i.e., social and sexual encounters).     

Foraging patterns of yellow-bellied marmosts: role of kinship and individual variability

Summary Two colonies of yellow-bellied marmots (Marmota flaviventris) at an elevation of 2900 m in Colorado were studied to elucidate the role of various behavioral and ecological factors as determinants of spatial foraging patterns. The locations of known individuals were periodically recorded. These locality data were plotted as three-dimensional block diagrams, the peak heights representing the frequency of observation. Predation risk and vegetation distribution influenced the location of foraging areas; kinship was an important factor in the determination of the amount of foraging area shared between individual marmots. Spatial overlap tended to be greater among close kin, but this was modified by individual behavioral characteristics, reproductive state, the existence of separate burrow systems within a colony, and the age of the animal. Mothers and juveniles, and littermates as young and resident yearlings, had nearly identical foraging areas.     

Can male-male competition stabilize speciation? A test in Lake Victoria haplochromine cichlid fish

It has been suggested that sympatric speciation can be driven by sexual selection on male mating traits alone. However, a fundamental problem for this process is the lack of ecological differentiation that would stabilize the coexistence of incipient species through frequency-dependent selection. Such selection can also occur if male aggression is primarily directed towards similar rather than towards dissimilar phenotypes, so that rare male phenotypes would enjoy a negatively frequency-dependent fitness advantage. We experimentally tested such an aggression bias in two recently diverged, ecologically and anatomically similar sympatric cichlid species pairs of the genus Pundamilia from Lake Victoria. Territorial males of a pair of partially reproductively isolated species with red and blue nuptial coloration, respectively, studied in the laboratory were confronted simultaneously with both colour types enclosed in transparent tubes. Red males were more aggressive to red stimuli under white light but not when colour differences were masked under green light. Blue males were equally aggressive to both stimuli in both light conditions. Males of two apparently fully reproductively isolated species, again one with red and one with blue nuptial coloration, studied in the field, both directed more aggressive behaviour towards conspecific than towards heterospecific stimulus males. The differential allocation of aggression would create an advantage for males of the less abundant phenotype or species, thereby potentially supporting stable coexistence of the phenotypes. The finding that this effect was less clear in the partially reproductively isolated species pair than in the fully isolated species pair is discussed.     

Multi-scale foraging variability in Northern gannet (Morus bassanus) fuels potential foraging plasticity

The survival of marine predators depends on behavioural plasticity to cope with changes in prey distribution. Variability in behaviour might predict plasticity and is easier to assess than plasticity. Using miniaturized GPS loggers over several breeding seasons in two Norwegian Northern gannet (Morus bassanus) colonies, we investigated if and how the variability within and between individuals, but also between colonies and years, affected foraging strategies. Results revealed strong individual variability (foraging trip durations, foraging effort and different foraging areas). Individuals from both colonies showed preferred commuting routes, flight bearings and feeding hotspots. Individuals from the largest colony used larger and more foraging areas than individuals from the small colony. Feeding hotspots and foraging ranges varied amongst years in the largest colony only. Our study demonstrated that gannets show flexibility by changing prey fields that are driven by shifting oceanographic conditions.     

The role of individual behavior type in mediating indirect interactions

Trait-mediated indirect interactions (TMII) play an important role in structuring natural communities, and numerous studies have experimentally demonstrated their presence in a variety of systems. However, these studies have largely examined the presence or absence of traits that are responsible for these interactions, without considering natural variation between individuals in the extent to which these traits are manifested. We used a well-documented TMII to investigate the importance of individual behavior type for determining the strength of the TMII. The toadfish Opsanus tau has an indirect positive influence on bivalve survival because the mud crab Panopeus herbstii, a consumer of bivalves, reduces foraging effort in the presence of toadfish. We quantified variation in the strength of persistent individual mud crab responses to toadfish and resulting variation in the strength of TMII. We demonstrate that the strength of this TMII is strongly influenced by mud crab size and behavior type, strengthening with the intensity of response of individual mud crabs to toadfish predator cues. Further, we demonstrate that the spatial distribution within intertidal oyster reefs of crabs with different behavior types is not random; mud crabs inhabiting subtidal areas, where predator cues are more persistent, are significantly less responsive to toadfish cues than mud crabs from intertidal areas. This spatial behavioral structure should lead to spatial variation in the strength of TMII. Given the widespread importance of TMII and the broad occurrence of individual personality or behavior types across numerous taxa, these results should be generally applicable. The distribution of behavior types within a population may therefore be a useful metric for improving our ability to predict the strength of TMII.     

Stable isotope ratios of a tropical marine predator: confounding effects of nutritional status during growth

Stable isotope analysis of carbon and nitrogen is frequently used to study the diets and foraging ecology of marine predators. However, isotopic values may also be affected by an individual’s nutritional status and associated physiological processes. Here, we use C and N stable isotopes in blood and feathers of blue-footed booby chicks at the Galápagos Islands to examine how isotopic values are related to body condition and growth rate, and to assess the consistency in the isotope ratios of individuals during growth. Size dimorphism in blue-footed boobies provided an additional opportunity to examine how isotope ratios differ between sexes in relation to body size and growth rate. There was no significant difference between sexes but both C and N stable isotopes were significantly negatively related to the body condition of chicks. These data were consistent with individual variation in physiological processes affecting fractionation, although we cannot rule out the possibility that they were also influenced to some extent by population-level variation in the stable isotope ratios of prey fed to chicks, for instance related to prey size, depth or lipid content. Our results highlight the need for methods that take proper account of confounding physiological factors in isotopic studies of foraging ecology and diet.     

Colony-level selection effects on individual and colony foraging task performance in honeybees, Apis mellifera L.

In honeybees, as in other highly eusocial species, tasks are performed by individual workers, but selection for worker task phenotypes occurs at the colony level. We investigated the effect of colony-level selection for pollen storage levels on the foraging behavior of individual honeybee foragers to determine (1) the relationship between genotype and phenotypic expression of foraging traits at the individual level and (2) how genetically based variation in worker task phenotype is integrated into colony task organization. We placed workers from lines selected at the colony level for high or low pollen stores together with hybrid workers into a common hive environment with controlled access to resources. Workers from the selected lines showed reciprocal variation in pollen and nectar collection. High-pollen-line foragers collected pollen preferentially, and low- pollen-line workers collected nectar, indicating that the two tasks covary genetically. Hybrid workers were not intermediate in phenotype, but instead showed directional dominance for nectar collection. We monitored the responses of workers from the selected strains to changes in internal (colony) and external (resource) stimulus levels for pollen foraging to measure the interaction between genotypic variation in foraging behavior and stimulus environment. Under low-stimulus conditions, the foraging group was over-represented by high-pollen-line workers. However, the evenness in distribution of the focal genetic groups increased as foraging stimuli increased. These data are consistent with a model where task choice is a consequence of genetically based response thresholds, and where genotypic diversity allows colony flexibility by providing a range of stimulus thresholds. Received: 3 May 1999 / Received in revised form: 22 December 1999 / Accepted: 23 January 2000     

Limited flexibility in the temporal caste system of the honey bee

Caste theory predicts that social insect colonies are organized into stable groups of workers specialized on particular task sets. Alternative concepts of organization of work suggest that colonies are composed of extremely flexible workers able to perform any task as demand necessitates. I explored the flexibility of workers in temporal castes of the honey bee Apis mellifera by determining the ability of colonies to reorganize labor after a major demographic disturbance. I evaluated the flexibility of temporal castes by comparing the foraging rates of colonies having just lost their foragers with colonies having also lost their foragers but having been given a week to reorganize. The population sizes and contents of the colonies in each group were equalized and foraging rates were recorded for one week. Colonies given a weeks initial recovery time after the loss of their foragers were found to forage at significantly higher rates than those colonies given no initial recovery time. This result was consistent for nectar and pollen foraging. These results suggest that honeybee workers lack sufficient flexibility to reorganize labor without compromising foraging. This finding is consistent with the caste concept model of organization of work in insect societies.     

Predators use environmental cues to discriminate between prey

The cognitive processes of predators play a central role in the evolution of prey characters. Numerous studies have shown that vertebrate predators may learn to associate the characteristics of prey (e.g. color) with the cost or benefit of ingesting them, thus forming preferences and aversions for different kinds of prey. Although the distribution and quality of prey types can differ between environmental contexts, which may make it profitable to attack a prey type in some contexts but not in others, the influence of environmental cues in decisions to attack has rarely been addressed. Recent theory suggests that modification of prey preferences by environmental cues such as microhabitat or temperature may influence the evolution of prey characteristics. Here, we show that the environmental foraging context may determine prey choice in great tits (Parus major) through learned association between the prey phenotype (appearance and palatability) and a contextual background cue. The same individuals were able to learn and maintain two different sets of food preferences and aversions for use in two different environmental contexts (aviaries with red or blue wooden boards), indicating a role for contextual learning in vertebrate foraging behavior.