Colin M. Wright

Animal personality aligns task specialization and task proficiency in a spider society

Significance Here we demonstrate strong links among task specialization, task proficiency, and animal personality in a nonpolymorphic spider, reminiscent of the associations observed among task specialization, task aptitude, and castes in the social insects. Such links previously have been demonstrated only for single tasks, and some studies failed to find any links whatsoever. In contrast, the present study demonstrates such links in four different tasks important for proper colony function. Unlike morphological castes, individual differences in personality have been detected in almost every animal system imaginable. Thus, we argue that the classic canon of theories and predictions developed in the context of castes could be adaptively retrofitted and redeployed in the personality literature to a much broader swath of animal diversity. Classic theory on division of labor implicitly assumes that task specialists are more proficient at their jobs than generalists and specialists in other tasks; however, recent data suggest that this might not hold for societies that lack discrete worker polymorphisms, which constitute the vast majority of animal societies. The facultatively social spider Anelosimus studiosus lacks castes, but females exhibit either a “docile” or “aggressive” phenotype. Here we observed the propensity of individual females of either phenotype to perform various tasks (i.e., prey capture, web building, parental care, and colony defense) in mixed-phenotype colonies. We then measured the performance outcomes of singleton individuals of either phenotype at each task to determine their proficiencies. Aggressive females participated more in prey capture, web building, and colony defense, whereas docile females engaged more in parental care. In staged trials, aggressive individuals were more effective at capturing prey, constructing webs, and defending the colony, whereas docile females were more effective at rearing large quantities of brood. Thus, individuals’ propensity to perform tasks and their task proficiencies appear to be adaptively aligned in this system. Moreover, because the docile/aggressive phenotypes are heritable, these data suggest that within-colony variation is maintained because of advantages gleaned by division of labor.

Participation in cooperative prey capture and the benefits gained from it are associated with individual personality

Abstract In animal societies, behavioral idiosyncrasies of the individuals often guide which tasks they should perform. Such personality-specific task participation can increase individual task efficiency, thereby improving group performance. While several recent studies have documented group-level benefits of within-group behavioral (i.e., personality) diversity, how these benefits are realized at the individual level is unclear. Here we probe the individual-level benefits of personality-driven task participation in the social spider Stegodyphus dumicola. In S. dumicola, the presence of at least one highly bold individual catalyzes foraging behavior in shy colony members, and all group constituents heavily compete for prey. We assessed boldness by examining how quickly spiders resumed normal movement after a simulated predator attack. We test here whether (1) participants in collective foraging gain more mass from prey items and (2) whether bold individuals are less resistant to starvation than shy spiders, which would motivate the bold individuals to forage more. Next, we assembled colonies of shy spiders with and without a bold individual, added one prey item, and then tracked the mass gain of each individual spider after this single feeding event. We found that spiders that participated in prey capture (whether bold or shy) gained more mass than nonparticipators, and colonies containing a single bold spider gained more total mass than purely shy colonies. We also found that bold spiders participated in more collective foraging events and were more susceptible to starvation than shy spiders, suggesting that the aggressive foraging of bold individuals may represent a strategy to offset starvation risk. These findings add to the body of evidence that animal personality can shape social organization, individual performance, and group success.

The Achilles' heel hypothesis: misinformed keystone individuals impair collective learning and reduce group success.

Many animal societies rely on highly influential keystone individuals for proper functioning. When information quality is important for group success, such keystone individuals have the potential to diminish group performance if they possess inaccurate information. Here, we test whether information quality (accurate or inaccurate) influences collective outcomes when keystone individuals are the first to acquire it. We trained keystone or generic individuals to attack or avoid novel stimuli and implanted these trained individuals within groups of naive colony-mates. We subsequently tracked how quickly groups learned about their environment in situations that matched (accurate information) or mismatched (inaccurate information) the training of the trained individual. We found that colonies with just one accurately informed individual were quicker to learn to attack a novel prey stimulus than colonies with no informed individuals. However, this effect was no more pronounced when the informed individual was a keystone individual. In contrast, keystones with inaccurate information had larger effects than generic individuals with identical information: groups containing keystones with inaccurate information took longer to learn to attack/avoid prey/predator stimuli and gained less weight than groups harbouring generic individuals with identical information. Our results convey that misinformed keystone individuals can become points of vulnerability for their societies.

Exposure to predators reduces collective foraging aggressiveness and eliminates its relationship with colony personality composition

Predation is a ubiquitous threat that often plays a central role in determining community dynamics. Predators can impact prey species by directly consuming them, or indirectly causing prey to modify their behavior. Direct consumption has classically been the focus of research on predator-prey interactions, but substantial evidence now demonstrates that the indirect effects of predators on prey populations are at least as strong as, if not stronger than, direct consumption. Social animals, particularly those that live in confined colonies, rely on coordinated actions that may be vulnerable to the presence of a predator, thus impacting the society’s productivity and survival. To examine the effect of predators on the behavior of social animal societies, we observed the collective foraging of social spider colonies (Stegodyphus dumicola) when they interact with dangerous predatory ants either directly, indirectly, or both. We found that when colonies were exposed directly and indirectly to ant cues, they attacked prey with approximately 40–50% fewer spiders, and 40–90% slower than colonies that were not exposed to any predator cues. Furthermore, exposure to predatory ants disassociated the well-documented positive relationship between colony behavioral composition (proportion of bold spiders) and foraging aggressiveness (number of attackers) in S. dumicola, which is vital for colony growth. Thus, the indirect effects of predator presence may limit colony success. These results suggest that enemy presence could compromise the organizational attributes of animal societies.Significance statementThis study demonstrates that predator presence can compromise the organizational structure of complex animal societies. Indirect cues of predators proved to be most effective at eliminating the relationship between colony personality composition and group foraging. These results suggest that colonies may only incur the foraging benefits associated with particular personality compositions in habitats where their main predator does not occur. It is true that most, if not all, animals must respond at some time to the threat of predation, and shifts in behavior are often used as a first line of defense. Therefore, given the fact that individual differences in behavior are important in determining collective outcomes in many species, we feel our findings could have implications for a broad range of social taxa.

The multidimensional behavioural hypervolumes of two interacting species predict their space use and survival

Individual animals differ consistently in their behaviour, thus impacting a wide variety of ecological outcomes. Recent advances in animal personality research have established the ecological importance of the multidimensional behavioural volume occupied by individuals and by multispecies communities. Here, we examine the degree to which the multidimensional behavioural volume of a group predicts the outcome of both intra- and interspecific interactions. In particular, we test the hypothesis that a population of conspecifics will experience low intraspecific competition when the population occupies a large volume in behavioural space. We further hypothesize that populations of interacting species will exhibit greater interspecific competition when one or both species occupy large volumes in behavioural space. We evaluate these hypotheses by studying groups of katydids (Scudderia nymphs) and froghoppers (Philaenus spumarius), which compete for food and space on their shared host plant, Solidago canadensis. We found that individuals in single-species groups of katydids positioned themselves closer to one another, suggesting reduced competition, when groups occupied a large behavioural volume. When both species were placed together, we found that the survival of froghoppers was greatest when both froghoppers and katydids occupied a small volume in behavioural space, particularly at high froghopper densities. These results suggest that groups that occupy large behavioural volumes can have low intraspecific competition but high interspecific competition. Thus, behavioural hypervolumes appear to have ecological consequences at both the level of the population and the community and may help to predict the intensity of competition both within and across species.

Polistes metricus queens exhibit personality variation and behavioral syndromes

Abstract Consistent differences in behavior between individuals, otherwise known as animal personalities, have become a staple in behavioral ecology due to their ability to explain a wide range of phenomena. Social organisms are especially serviceable to animal personality techniques because they can be used to explore behavioral variation at both the individual and group level. Despite the success of personality research in social organisms generally, and social Hymenoptera in particular, social wasps (Vespidae) have received little to no attention in the personality literature. In the present study, we test Polistes metricus (Vespidae; Polistinae) paper wasp queens for the presence of repeatable variation in, and correlations (“behavioral syndromes”) between, several commonly used personality metrics: boldness, aggressiveness, exploration, and activity. Our results indicate that P. metricus queens exhibit personalities for all measured traits and correlations between different behavioral measures. Given that paper wasps have served as a model organism for a wide range of phenomena such as kin selection, dominance hierarchies, mate choice, facial recognition, social parasitism, and chemical recognition, we hope that our results will motivate researchers to explore whether, or to what degree, queen personality is important in their research programs.

Evidence for contrasting size-frequency distributions of workers patrolling vegetation vs. the ground in the polymorphic African ant Anoplolepis custodiens

It is often hypothesized that ant species with substantial variation in worker body size should have schemes for allocating workers to different foraging tasks based on size. Here, we document in Anoplolepis custodiens ants preliminary evidence for a relationship between worker body size and the foraging surfaces on which workers walk. Workers of A. custodiens were collected in pitfall traps near their nest entrances and compared in size to workers exploring the branches of associated shrubs (Salsola sp.). Although ants of all sizes moved freely on the ground, the bushes were almost entirely populated by the smallest workers. These results suggest an effect of substrate on the foraging behavior of an understudied species and suggest that A. custodiens might be a good model to explore size-based behavioral differences in polymorphic ants.

WASPnest: a worldwide assessment of social Polistine nesting behavior

Cooperative breeding decreases the direct reproductive output of subordinate individuals, but cooperation can be evolutionarily favored when there are challenges or constraints to breeding independently. Environmental factors, including temperature, precipitation, latitude, high seasonality, and environmental harshness have been hypothesized to correlate with the presence of cooperative breeding. However, to test the relationship between cooperation and ecological constraints requires comparative data on the frequency and variation of cooperative breeding across differing environments, ideally replicated across multiple species. Paper wasps are primitively social species, forming colonies composed of reproductively active dominants and foraging subordinates. Adult female wasps, referred to as foundresses, initiate new colonies. Nests can be formed by a single solitary foundress (noncooperative) or by multiple foundress associations (cooperative). Cooperative behavior varies within and among species, making paper wasps species well suited to disentangling ecological correlates of variation in cooperative behavior. This data set reports the frequency and extent of cooperative nest founding for 87 paper wasp species. Data were assembled from more than 170 published sources, previously unpublished field observations, and photographs contributed by citizen scientists to online natural history repositories. The data set includes 25,872 nest observations and reports the cooperative behavioral decisions for 45,297 foundresses. Species names were updated to reflect modern taxonomic revisions. The type of substrate on which the nest was built is also included, when available. A smaller population-level version of this data set found that the presence or absence of cooperative nesting in paper wasps was correlated with temperature stability and environmental harshness, but these variables did not predict the extent of cooperation within species. This expanded data set contains details about individual nests and further increases the power to address the relationship between the environment and the presence and extent of cooperative breeding. Beyond the ecological drivers of cooperation, these high-resolution data will be useful for future studies examining the evolutionary consequences of variation in social behavior. This data set may be used for research or educational purposes provided that this data paper is cited.