Using intra-flock association patterns to understand why birds participate in mixed-species foraging flocks in terrestrial habitats

Bird species are hypothesized to join mixed-species flocks (flocks hereon) either for direct foraging or anti-predation-related benefits. In this study, conducted in a tropical evergreen forest in the Western Ghats of India, we used intra-flock association patterns to generate a community-wide assessment of flocking benefits for different species. We assumed that individuals needed to be physically proximate to particular heterospecific individuals within flocks to obtain any direct foraging benefit (flushed prey, kleptoparasitism, copying foraging locations). Alternatively, for anti-predation benefits, physical proximity to particular heterospecifics is not required, i.e. just being in the flock vicinity can suffice. Therefore, we used choice of locations within flocks to infer whether individual species are obtaining direct foraging or anti-predation benefits. A small subset of the bird community (5/29 species), composed of all members of the sallying guild, showed non-random physical proximity to heterospecifics within flocks. All preferred associates were from non-sallying guilds, suggesting that the sallying species were likely obtaining direct foraging benefits either in the form of flushed or kleptoparasitized prey. The majority of the species (24/29) chose locations randomly with respect to heterospecifics within flocks and, thus, were likely obtaining antipredation benefits. In summary, our study indicates that direct foraging benefits are important for only a small proportion of species in flocks and that predation is likely to be the main driver of flocking for most participants. Our findings apart, our study provides methodological advances that might be useful in understanding asymmetric interactions in social groups of single and multiple species.     

The social network structure of a wild meerkat population: 2. Intragroup interactions

Knowledge of the structure of networks of social interactions is important for understanding the evolution of cooperation, transmission of disease, and patterns of social learning, yet little is known of how environmental, ecological, or behavioural factors relate to such structures within groups. We observed grooming, dominance, and foraging competition interactions in eight groups of wild meerkats (Suricata suricatta) and constructed interaction networks for each behaviour. We investigated relationships between networks for different social interactions and explored how group attributes (size and sex ratio), individual attributes (tenure of dominants), and ecological factors (ectoparasite load) are related to variation in network structure. Network structures varied within a group according to interaction type. Further, network structure varied predictably with group attributes, individual attributes, and ecological factors. Networks became less dense as group size increased suggesting that individuals were limited in their number of partners. Groups with more established dominant females were more egalitarian in their grooming and foraging competition interactions, but more despotic in their dominance interactions. The distribution of individuals receiving grooming became more skewed at higher parasite loads, but more equitable at low parasite loads. We conclude that the pattern of interactions between members of meerkat groups is not consistent between groups but instead depends on general attributes of the group, the influence of specific individuals within the group, and ecological factors acting on group members. We suggest that the variation observed in interaction patterns between members of meerkat groups may have fitness consequences both for individual group members and the group itself.     

On the possible contribution of mixed species flocks to species richness in neotropical avifaunas

Summary Mixed species foraging flocks are a dominant component of the infra-structure of avian communities in neotropical forests. In Amazonia, these flocks consist of pairs of 10–20 species, many of which are permanently associated with mixed flocks. At least half of these flocking species maintain territories that correspond exactly to the flock home range. Small individuals that participate as permanent members of the flocks must adopt the large home range of the larger nucleus species. Therefore, the densities of smaller species are dependent on the availability and density of flocks rather than the availability of food resources. Single pairs of 4 small flocking species with individual body masses of 8 g occupied exclusive territories of 8–12 ha. These were the same exact territories that were defended by at least 6 other flocking species with individual body masses of up to 37 g. Because of their attachment to flocks with large territories, small species are expected to under-utilize available food resources. The under-utilization of food resources is expected to allow smaller species to coexist with greater niche overlap resulting in increased species richness. This hypothesis was tested by quantifying foraging niche in terms of foraging height, foraging maneuver, and prey substrate; and using these values in addition to body mass and bill size (length, depth and width) to determine relative niche overlap between large versus small species pairs.Smaller species had greater foraging overlap than large flocking species and particularly the three smallest species of the genus Myrmotherula; longipennis, axillaris and menetriesii had very high overlap (average foraging niche overlap for the 3 species=0.83±0.12 compared with 0.12±0.19 for all flocking species), similar body sizes (body masses differing by no more then 8%) and similar bill morphologies (maximum ratio in length=1.08, width=1.07, and depth=1.06). These results are consistent with the hypothesis that small species participating in Amazonian mixed flocks can coexist with greater niche overlap because their density is flock dependent rather than resource dependent.     

Individual boldness affects interspecific interactions in sticklebacks

Within populations of many species, individuals that are otherwise similar to one another in age, size or sex can differ markedly in behaviours such as resource use, risk taking and competitive ability. There has been much research into the implications of such variation for intraspecific interactions, yet little investigation into its role in influencing interspecific interactions outside of a predator–prey context. In this study, we investigated the role of individual-level behavioural variation in determining the outcomes of interactions between two ecologically similar fishes, the threespine and ninespine sticklebacks (Gasterosteus aculeatus and Pungitius pungitius). Experiment 1 asked whether individuals of both species were consistent in their expression of two behaviours: activity in novel surroundings and latency to attack prey. For each behaviour, focal individuals were assayed twice, 10 days apart. Performances were positively correlated between exposures, suggesting behavioural consistency within individuals, at least over this timescale. Experiment 2 revealed not only differences in habitat use described both by species-level variation, with ninespines spending more time in vegetated areas, but also by individual differences, with more active individuals of both species spending more time in open water than in vegetation. Experiment 3 revealed that when heterospecific pairs competed for prey, bolder individuals consumed a greater share, irrespective of species. These findings suggest that individual-level variation can facilitate overlap in habitat use between heterospecifics and also determine the outcomes of resource contests when they meet. We discuss how this might vary between populations as a function of prevailing selection pressures and suggest approaches for testing our predictions.     

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.     

Colony state and regulation of pollen foraging in the honey bee,Apis mellifera L.

Summary To place social insect foraging behavior within an evolutionary context, it is necessary to establish relationships between individual foraging decisions and parameters influencing colony fitness. To address this problem, we examined interactions between individual foraging behavior and pollen storage levels in the honey bee, Apis mellifera L. Colonies responded to low pollen storage conditions by increasing pollen intake rates 54% relative to high pollen storage conditions, demonstrating a direct relationship between pollen storage levels and foraging effort. Approximately 80% of the difference in pollen intake rates was accounted for by variation in individual foraging effort, via changes in foraging activity and individual pollen load size. An additional 20% resulted from changes in the proportion of the foraging population collecting pollen. Under both high and low pollen storage treatments, colonies returned pollen storage levels to pre-experimental levels within 16 days, suggesting that honey bees regulate pollen storage levels around a homeostatic set point. We also found a direct relationship between pollen storage levels and colony brood production, demonstrating the potential for cumulative changes in individual foraging decisions to affect colony fitness. Offprint requests to: J.H. Fewell at the current address     

Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (<Emphasis Type="Italic">Lepomis cyanellus</Emphasis>)

Within aquatic communities, individuals may gain survival benefits by responding to the chemical alarm signals of heterospecific prey guild members. Piscivorous individuals, however, should be selected to use such chemical signals as foraging cues. A variety of centrarchid species, such as largemouth bass (Micropterus salmoides), undergo an ontogenetic change in their response to the chemical alarm cues of heterospecific guild members, switching from antipredator to foraging responses. This ontogenetic shift should occur when potential foraging benefits outweigh any survival advantage gained from an antipredator response. To test this model, we exposed juvenile green sunfish (Lepomis cyanellus) to the skin extracts of conspecifics, a heterospecific prey guild member (finescale dace, Phoxinus neogeaus) or an allopatric heterospecific (green swordtails, Xiphophorus helleri). Juvenile sunfish exhibited a significant positive relationship between standard length and time spent moving and a significant negative relationship between length and time in a spine-erect posture, when exposed to dace skin extract, but not to either swordtail or conspecific skin extracts. Smaller individuals of less than 90 mm standard length (SL) decreased time moving and increased time with spines erect (indicating an antipredator response) while larger individuals (>90 mm SL) increased time moving and decreased time with spines erect (indicating a foraging response), when exposed to dace skin extract. Conversely, juvenile sunfish, regardless of size tested, always exhibited an antipredator response to conspecific skin extract. Sunfish exhibited no change in behaviour in response to swordtail skin extracts. These data further support our model of a threat sensitive trade-off in the response to chemical alarm signals by juvenile centrarchids.     

Patterns of participation and free riding in territorial conflicts among ringtailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>)

Cooperation in animal social groups may be limited by the threat of free riding, the potential for individuals to reap the benefits of other individuals actions without paying their share of the costs. Here we investigate the factors that influence individual contributions to group-level benefits by studying individual participation in territorial defense among female ringtailed lemurs (Lemur catta). To control for potentially confounding factors, particularly group size, we studied two semi-free-ranging groups at the Duke University Primate Center. First, we used a combination of experimental and observational methods to investigate the costs and benefits of territorial defense for individual lemurs. We found three indications of costs: physical contact occurred during inter-group encounters, participation in territorial defense was negatively correlated with ambient temperature, and rates of self-directed behaviors increased during encounters. Benefits were more difficult to quantify, but observational and experimental tests suggested that individuals shared the gains of territorial defense by foraging in defended territories. Thus, during experiments in which one of the groups was prevented from defending its territory, the free-ranging group made more frequent incursions into the other groups territory. Second, we examined variation in participation in territorial defense. Individuals varied significantly in their rates of aggression and genital marking during inter-group encounters. The extensive variation documented among individuals was partially accounted for by dominance rank, kinship and patterns of parental care. However, we found no evidence to suggest that participation was enforced through punishment (policing) or exchange of benefits involving grooming. In conclusion, this study provides further insights into cooperative behavior in mammalian social groups by revealing how the costs and benefits of territoriality influence patterns of individual participation in the context of shared (collective) goods.Communicated by P. Kappeler     

Shark personalities? Repeatability of social network traits in a widely distributed predatory fish

Interest in animal personalities has generated a burgeoning literature on repeatability in individual traits such as boldness or exploration through time or across different contexts. Yet, repeatability can be influenced by the interactive social strategies of individuals, for example, consistent inter-individual variation in aggression is well documented. Previous work has largely focused on the social aspects of repeatability in animal behaviour by testing individuals in dyadic pairings. Under natural conditions, individuals interact in a heterogeneous polyadic network. However, the extent to which there is repeatability of social traits at this higher order network level remains unknown. Here, we provide the first empirical evidence of consistent and repeatable animal social networks. Using a model species of shark, a taxonomic group in which repeatability in behaviour has yet to be described, we repeatedly quantified the social networks of ten independent shark groups across different habitats, testing repeatability in individual network position under changing environments. To understand better the mechanisms behind repeatable social behaviour, we also explored the coupling between individual preferences for specific group sizes and social network position. We quantify repeatability in sharks by demonstrating that despite changes in aggregation measured at the group level, the social network position of individuals is consistent across treatments. Group size preferences were found to influence the social network position of individuals in small groups but less so for larger groups suggesting network structure, and thus, repeatability was driven by social preference over aggregation tendency.     

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.     

Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success

Studying the structure of social interactions is fundamental in behavioral ecology as social behavior often influences fitness and thus natural selection. However, social structure is often complex, and determining the most appropriate measures of variation in social behavior among individuals can be difficult. Social network analysis generates numerous, but often correlated, measures of individual connectedness derived from a network of interactions. We used measures of individual connectedness in networks of affiliative and agonistic interactions in yellow-bellied marmots, Marmota flaviventris, to first determine how variance was structured among network measures. Principal component analysis reduced our set of network measures to four “social attributes” (unweighted connectedness, affiliation strength, victimization, and bullying), which revealed differences between patterns of affiliative and agonistic interactions. We then used these extracted social attributes to examine the relationship between an individual’s social attributes and several performance measures: annual reproductive success, parasite infection, and basal stress. In male marmots, bullying was positively associated with annual reproductive success, while in females, affiliation strength was negatively associated with annual reproductive success. No other social attributes were significantly associated with any performance measures. Our study highlights the utility of considering multiple dimensions when measuring the structure and functional consequences of social behavior.     

Individual variation in foraging behavior reveals a trade-off between flexibility and performance of a top predator

There is increasing evidence that behavioral flexibility is associated with the ability to adaptively respond to environmental change. Flexibility can be advantageous in some contexts such as exploiting novel resources, but it may come at a cost of accuracy or performance in ecologically relevant tasks, such as foraging. Such trade-offs may, in part, explain why individuals within a species are not equally flexible. Here, we conducted a reversal learning task and predation experiment on a top fish predator, the Northern pike (Esox lucius), to examine individual variation in flexibility and test the hypothesis that an individual’s behavioral flexibility is negatively related with its foraging performance. Pikes were trained to receive a food reward from either a red or blue cup and then the color of the rewarded cup was reversed. We found that pike improved over time in how quickly they oriented to the rewarded cup, but there was a bias toward the color red. Moreover, there was substantial variation among individuals in their ability to overcome this red bias and switch from an unrewarded red cup to the rewarded blue cup, which we interpret as consistent variation among individuals in behavioral flexibility. Furthermore, individual differences in behavioral flexibility were negatively associated with foraging performance on ecologically relevant stickleback prey. Our data indicate that individuals cannot be both behaviorally flexible and efficient predators, suggesting a trade-off between these two traits.     

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     

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.     

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.     

Social information use is a process across time, space, and ecology, reaching heterospecifics

Decision making can be facilitated by observing other individuals faced with the same or similar problem, and recent research suggests that this social information use is a widespread phenomenon. Implications of this are diverse and profound: for example, social information use may trigger cultural evolution, affect distribution and dispersal of populations, and involve intriguing cognitive traits. We emphasize here that social information use is a process consisting of the scenes of (1) event, (2) observation, (3) decision, and (4) consequence, where the initial event is a scene in such a process of another individual. This helps to construct a sound conceptual framework for measuring and studying social information use. Importantly, the potential value of social information is affected by the distance in time, space, and ecology between the initial observation and eventual consequence of a decision. Because negative interactions between individuals (such as direct and apparent competition) also depend on the distance between individuals along these dimensions, the potential value of information and the negative interactions may form a trade-off situation. Optimal solutions to this trade-off can result in adaptively extended social information use, where using information gathered some time ago, some distance away, and from ecologically different individuals is preferred. Conceivably, using information gathered from a heterospecific individual might often be optimal. Many recent studies demonstrate that social information use does occur between species, and the first review of published cases is provided here. Such interaction between species, especially in habitat selection, has important consequences for community ecology and conservation. Adaptively extended social information use may also be an important evolutionary force in guild formation. Complex coevolutionary patterns may result depending on the effect of information use on the provider of information.     

High social density increases foraging and scouting rates and induces polydomy in Temnothorax ants

Many organisms live in crowded groups where social density affects behavior and fitness. Social insects inhabit nests that contain many individuals where physical interactions facilitate information flow and organize collective behaviors such as foraging, colony defense, and nest emigration. Changes in nest space and intranidal crowding can alter social interactions and affect worker behavior. Here, I examined the effects of social density on foraging, scouting, and polydomy behavior in ant colonies—using the species Temnothorax rugatulus. First, I analyzed field colonies and determined that nest area scaled isometrically with colony mass—this indicates that nest area changes proportionally with colony size and suggests that ants actively control intranidal density. Second, laboratory experiments showed that colonies maintained under crowded conditions had greater foraging and scouting activities compared to the same colonies maintained at a lower density. Moreover, crowded colonies were significantly more likely to become polydomous. Polydomous colonies divided evenly based on mass between two nests but distributed fewer, heavier workers and brood to the new nests. Polydomous colonies also showed different foraging and scouting rates compared to the same colonies under monodomous conditions. Combined, the results indicate that social density is an important colony phenotype that affects individual and collective behavior in ants. I discuss the function of social density in affecting communication and the organization of labor in social insects and hypothesize that the collective management of social density is a group level adaptation in social insects.     

Influence of residency and social odors in interactions between competing native and alien rodents

Residency status of individuals in populations may be an important determinant of the outcomes of interspecific competition between native and introduced species. We examined direct behavioral interactions between two similarly sized rodents, the alien Rattus rattus and native Rattus fuscipes when they were respective residents and intruders in a small enclosure. Resident individuals were dominant in their behaviors toward intruders irrespective of the species that was resident. In contrast, interactive behaviors between conspecifics were often neutral or amicable, supporting suggestions that R. rattus and R. fuscipes are social animals. We then tested whether rodent species use heterospecific odors to avoid aggressive competitive interactions and partition space in the field. Neither R. fuscipes nor R. rattus responded to traps scented with the odors of male or female heterospecifics. If R. fuscipes does not recognize the odor of introduced R. rattus, then odors will not be cues to the presence or territorial space of competing heterospecifics. Rather, findings from both enclosure and field trials suggest that direct aggressive interactions between individual R. rattus and R. fuscipes probably facilitate segregation of space between these two species in wild populations, where resident animals may typically be the winners and exclude heterospecific intruders. These findings have implications for the invasion success of introduced rodents such as R. rattus into intact forests, where native populations may have competitive advantage because of their residency status.     

Individual specialization in the hunting wasp <Emphasis Type="Italic">Trypoxylon</Emphasis> (<Emphasis Type="Italic">Trypargilum</Emphasis>) <Emphasis Type="Italic">albonigrum</Emphasis> (Hymenoptera,Crabronidae)

Individual-level variation in resource use occurs in a broad array of vertebrate and invertebrate taxa and may have important ecological and evolutionary implications. In this study, we measured the degree of individual-level variation in prey preference of the hunting wasp Trypoxylon albonigrum, which inhabits the Atlantic Forest in southeastern Brazil. This wasp captures several orb-weaving spider genera to provision nests. Individuals consistently specialized on a narrow subset of the prey taxa consumed by the population, indicating the existence of significant individual-level variation in prey preferences. The population niche was broader in the wet season in terms of both prey size and taxa. In the case of prey size, the population niche expansion was achieved via increased individual niche breadths, whereas in the case of prey taxa, individual niches remained relatively constrained, and the population niche expanded via increased interindividual variation. The observed pattern suggests the possibility of functional trade-offs associated with the taxon of the consumed prey. The nature of the trade-offs remains unknown, but they are likely related to learning in searching and/or handling prey. We hypothesize that by specializing on specific prey taxa, individuals increase foraging efficiency, reducing foraging time and ultimately increasing reproductive success.