James L. L. Lichtenstein

Similar patterns of frequency-dependent selection on animal personalities emerge in three species of social spiders.

Frequency‐dependent selection is thought to be a major contributor to the maintenance of phenotypic variation. We tested for frequency‐dependent selection on contrasting behavioural strategies, termed here ‘personalities’, in three species of social spiders, each thought to represent an independent evolutionary origin of sociality. The evolution of sociality in the spider genus Anelosimus is consistently met with the emergence of two temporally stable discrete personality types: an ‘aggressive’ or ‘docile’ form. We assessed how the foraging success of each phenotype changes as a function of its representation within a colony. We did this by creating experimental colonies of various compositions (six aggressives, three aggressives and three dociles, one aggressive and five dociles, six dociles), maintaining them in a common garden for 3 weeks, and tracking the mass gained by individuals of either phenotype. We found that both the docile and aggressive phenotypes experienced their greatest mass gain in mixed colonies of mostly docile individuals. However, the performance of both phenotypes decreased as the frequency of the aggressive phenotype increased. Nearly identical patterns of phenotype‐specific frequency dependence were recovered in all three species. Naturally occurring colonies of these spiders exhibit mixtures dominated by the docile phenotype, suggesting that these spiders may have evolved mechanisms to maintain the compositions that maximize the success of the colony without compromising the expected reproductive output of either phenotype.

Prolonged food restriction decreases body condition and reduces repeatability in personality traits in web-building spiders

Variation in state, which is any factor that alters the value of decision options, is likely one of the most common drivers of personality differences. However, the general relationship between individuals’ body state and various personality metrics/average behavioral type, repeatability of behavior, and behavioral syndrome structure is still poorly resolved. Here, we manipulate body condition in three spider species (Agelenopsis aperta, Latrodectus hesperus, and Anelosimus studiosus) using contrasting feeding schedules. We then assessed the effects of historic feeding regime on individuals’ body condition, boldness, and foraging aggressiveness. We further assessed the effects of feeding regimes on the repeatability of boldness and aggressiveness and the presence/absence of correlations between these two traits. We found that feeding treatment impacted individuals’ average boldness and aggressiveness in two species (A. aperta and A. studiosus). We also noted that among-individual variance in both boldness and aggressiveness was severely reduced when A. aperta and A. studiosus were subjected to prolonged food restriction, steeply reducing repeatability in these traits. Finally, we noted that correlations between boldness and foraging aggressiveness were detectable only in one case, revealing no compelling relationship between food restriction and the presence/absence of behavioral correlations. Taken together, our results suggest that food restriction has only weak, circumstantial effects on individuals’ average personality type and the correlations between behavioral traits. However, there appears to be a robust positive relationship between food availability and the signature of consistent individual differences in behavior.Significance statementUnder laboratory conditions, we found that lower feeding rates sharply decreased the repeatability of aggressiveness and boldness in two spider species. In doing so, we provide the second body of evidence suggesting that a highly prevalent and ecologically relevant state variable, higher body condition, can increase the repeatability of foraging-related behavioral traits. Additionally, under some feeding regimes, we found that hunger levels could alter the average individual aggressiveness and boldness but not correlations between these traits. This work highlights the importance of state variables such as hunger in eroding behavioral repeatability, the defining trait of personality.

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.

Behavioral Hypervolumes of Predator Groups and Predator-Predator Interactions Shape Prey Survival Rates and Selection on Prey Behavior

Predator-prey interactions often vary on the basis of the traits of the individual predators and prey involved. Here we examine whether the multidimensional behavioral diversity of predator groups shapes prey mortality rates and selection on prey behavior. We ran individual sea stars (Pisaster ochraceus) through three behavioral assays to characterize individuals’ behavioral phenotype along three axes. We then created groups that varied in the volume of behavioral space that they occupied. We further manipulated the ability of predators to interact with one another physically via the addition of barriers. Prey snails (Chlorostome funebralis) were also run through an assay to evaluate their predator avoidance behavior before their use in mesocosm experiments. We then subjected pools of prey to predator groups and recorded the number of prey consumed and their behavioral phenotypes. We found that predator-predator interactions changed survival selection on prey traits: when predators were prevented from interacting, more fearful snails had higher survival rates, whereas prey fearfulness had no effect on survival when predators were free to interact. We also found that groups of predators that occupied a larger volume in behavioral trait space consumed 35% more prey snails than homogeneous predator groups. Finally, we found that behavioral hypervolumes were better predictors of prey survival rates than single behavioral traits or other multivariate statistics (i.e., principal component analysis). Taken together, predator-predator interactions and multidimensional behavioral diversity determine prey survival rates and selection on prey traits in this system.

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.

Intraindividual Behavioral Variability Predicts Foraging Outcome in a Beach-dwelling Jumping Spider

Animal personality, defined as consistent differences between individuals in behavior, has been the subject of hundreds if not thousands of papers. However, little work explores the fitness consequences of variation in behavior within individuals, or intraindividual variability (IIV). We probe the effects of behavioral IIV on predator-prey interaction outcomes in beach-dwelling jumping spiders (Terralonus californicus). Prior studies have found that spiders with higher body condition (body mass relative to size) behave more variably. Thus, we hypothesized that jumping spider activity level IIV would relate positively to foraging performance. To address this, we tested for associations between activity IIV, average activity level, and two measures of foraging success in laboratory mesocosms: change in spider mass and the number of prey killed. Activity IIV positively correlated with the mass that spiders gained from prey, but not with the number of prey killed. This suggests that spiders with high IIV consumed a greater proportion of their prey or used less energy. Interestingly, average activity level (personality) predicted neither metric of foraging success, indicating that behavioral IIV can predict metrics of success that personality does not. Therefore, our findings suggest that IIV should be considered alongside personality in studies of predator-prey interactions.

Female-Biased Sex Ratios Increase Colony Survival and Reproductive Output in the Spider Anelosimus studiosus

Negative frequency-dependent selection acting on the sexes is hypothesized to drive populations toward a balanced sex ratio. However, numerous examples of female-biased sex ratios pepper the arthropods. Theoretical examinations have proposed that female-biased populations or groups can have higher chances of surviving and propagating that may be advantageous. We evaluated this hypothesis in the semisocial spider Anelosimus studiosus by creating artificial colonies of varying sex ratios and sizes and observing colony performance at sites with high versus low group extinction rates. We also tested whether colony extinction rates and sex ratios were correlated across 25 collection sites, spanning 10° latitude. We found that colonies with female-biased sex ratios produced more egg cases and were more likely to survive the duration of a field season, suggesting that female-biased sex ratios confer both survival and reproductive advantages on colonies. The effect of sex ratio on colony survival and reproductive output was strongest for small colonies in high extinction areas. Moreover, we found that female-biased sex ratios correlated with greater extinction rates across 25 sites, indicating that female-biased sex ratios may have evolved at some sites in response to high extinction rates. These findings suggest that selection favoring groups with female-biased sex ratios may operate in A. studiosus, shedding light on some of the factors that may drive the evolution of biased sex ratios.

Personality variation in two predator species does not impact prey species survival or plant damage in staged mesocosms

Mounting evidence suggests that consistent individual differences in behavior, better known as animal personality, can shape aspects of population and community ecology. Yet, the potential for animal personality to affect more complex and non-linear food webs, like those seen in nature, remains understudied. Here, we explore the degree to which the aggregate behaviors of two predator species simultaneously interact to alter prey survival rates and the presence and magnitude of trophic cascades. We set up mesocosms in an old-field habitat containing four different insect prey species and either two Phidippus clarus (Salticidae), two Platycryptus undatus (Salticidae), or one of each predator. Prior to initiating each mesocosm, we assayed the activity level and boldness of each individual predator and included these metrics in our models predicting prey survival and plant damage. We then compared the number of surviving prey and plant damage under each of these conditions and tested for associations between each of these response variables and predator behavior. We found no significant effect of predator community composition or predators’ behavior on prey survival or plant damage. These results suggest that the effects of predator personality on prey survival may be subtle or absent in complex species interaction modules.Significance statementAlthough much research suggests that animal personality can influence broader scale ecological phenomena, the ability of animal personality to alter complex species interaction modules remains unresolved. We tested whether pairs of predators of different personality types differentially impacted prey survival rates and plant damage in a tritrophic system, and whether these effects varied based on predator community composition. We recovered no evidence that predator personality types influenced prey survival or plant damage regardless of the predator composition considered. These results suggest that the effects of personality may be absent or undetectable in more complex, realistic ecological settings. The majority of laboratory-based personality studies published to date evaluate only dyadic species interactions in simplified environments. Our findings therefore raise concerns that such studies are prone to overestimate the effects of animal personality.