Top-down effects of intraspeciflic predator behavioral variation.

Among-individual variation in predator traits is ubiquitous in nature. However, variation among populations in this trait variation has been seldom considered in trophic dynamics. This has left unexplored (a) to what degree does among-individual variation in predator traits regulate prey populations and (b) to what degree do these effects vary spatially. We address these questions by examining how predator among-individual variation in functional traits shapes communities across habitats of varying structural complexity, in field conditions. We manipulated Chinese mantis (Tenodera sinensis) density (six or twelve individuals) and behavioral trait variability (activity level by movement on an open field) in experimental patches of old fields with varying habitat complexity (density of plant material). Then, we quantified their impacts on lower trophic levels, specifically prey (arthropods > 4 mm) and plant biomass. Predator behavioral variability only altered prey biomass in structurally complex plots, and this effect depended on mantis density. In the plots with the highest habitat complexity and mantis density, behaviorally variable groups decreased prey biomass by 40.3%. In complex plots with low mantis densities, low levels of behavioral variability decreased prey biomass by 32.2%. Behavioral variability and low habitat complexity also changed prey community composition, namely by increasing ant biomass by 881%. Our results demonstrate that among-individual trait variation can shape species-rich prey communities. Moreover, these effects depend on both predator density and habitat complexity. Incorporating this important facet of ecological diversity revealed normally unnoticed effects of functional traits on the structure and function of food webs.

Incorporating neurological and behavioral mechanisms of sociality into predator-prey models.

Consumer-resource population models drive progress in predicting and understanding predation. However, they are often built by averaging the foraging outcomes of individuals to estimate per capita functional responses (functions that describe predation rate). Reliance on per-capita functional responses rests on the assumption that that individuals forage independently without affecting each other. Undermining this assumption, extensive behavioral neuroscience research has made clear that facilitative and antagonistic interactions among conspecifics frequently alter foraging through interference competition and persistent neurophysiological changes. For example, repeated social defeats dysregulates rodent hypothalamic signaling, modulating appetite. In behavioral ecology, similar mechanisms are studied under the concept of dominance hierarchies. Neurological and behavioral changes in response to conspecifics undoubtedly play some sort of role in the foraging of populations, but modern predator-prey theory does not explicitly include them. Here we describe how some modern approaches to population modeling might account for this. Further, we propose that spatial predator-prey models can be modified to describe plastic changes in foraging behavior driven by intraspecific interaction, namely individuals switching between patches or plastic strategies to avoid competition. Extensive neurological and behavioral ecology research suggests that interactions among conspecifics help shape populations' functional responses. Modeling interdependent functional responses woven together by behavioral and neurological mechanisms may thus be indispensable in predicting the outcome of consumer-resource interactions across systems.

Predictors of colony extinction vary by habitat type in social spiders.

Many animal societies are susceptible to mass mortality events and collapse. Elucidating how environmental pressures determine patterns of collapse is important for understanding how such societies function and evolve. Using the social spider Stegodyphus dumicola, we investigated the environmental drivers of colony extinction along two precipitation gradients across southern Africa, using the Namib and Kalahari deserts versus wetter savanna habitats to the north and east. We deployed experimental colonies (n = 242) along two ~ 800-km transects and returned to assess colony success in the field after 2 months. Specifically, we noted colony extinction events after the 2-month duration and collected environmental data on the correlates of those extinction events (e.g., evidence of ant attacks, no. of prey captured). We found that colony extinction events at desert sites were more frequently associated with attacks by predatory ants as compared with savanna sites, while colony extinctions in wetter savannas sites were more tightly associated with fungal outbreaks. Our findings support the hypothesis that environments vary in the selection pressures that they impose on social organisms, which may explain why different social phenotypes are often favored in each habitat.

Spatial proximity and prey vibratory cues influence collective hunting in social spiders.

Social spiders are thought to predominantly receive information about their environment through vibrational cues. Thus, group living introduces the challenge of distinguishing useful vibrational information from the background noise of nestmates. Here we investigate whether spatial proximity between colony-mates may allow social spiders (Stegodyphus dumicola) to reduce background noise that might obstruct vibrational information from prey. To do so, we constructed experimental colonies and measured whether the number of spiders in proximity to one another whilst resting could predict the number of spiders that participated in prey capture. Additionally, we exposed spider colonies to five different simulated vibrational cues mimicking prey to determine which cue types spiders were most responsive to. We found that the number of spiders huddled together prior to foraging trials was positively correlated with the number of spiders participating in collective foraging. Furthermore, colonies responded more quickly to pulsed vibrational cues over other types of vibrational patterns. Together these data reveal that both social interactions and prey cues shape how social sit-and-wait predators experience and respond to their environment.

Assessing the repeatability, robustness to disturbance, and parent-offspring colony resemblance of collective behavior.

Groups of animals possess phenotypes such as collective behaviour, which may determine the fitness of group members. However, the stability and robustness to perturbations of collective phenotypes in natural conditions is not established. Furthermore, whether group phenotypes are transmitted from parent to offspring groups with fidelity is required for understanding how selection on group phenotypes contributes to evolution, but parent-offspring resemblance at the group level is rarely estimated. We evaluated the repeatability, robustness to perturbation and parent-offspring resemblance of collective foraging aggressiveness in colonies of the social spider Anelosimus eximius. Among-colony differences in foraging aggressiveness were consistent over time but changed if the colony was perturbed through the removal of individuals or via individuals' removal and subsequent return. Offspring and parent colony behaviour were correlated at the phenotypic level, but only once the offspring colony had settled after being translocated, and the correlation overlapped with zero at the among-colony level. The parent-offspring resemblance was not driven by a shared elevation but could be due to other environmental factors. The behaviour of offspring colonies in a common garden laboratory setting was not correlated with the behaviour of the parent colony nor with the same colony's behaviour once it was returned to the field. The phenotypes of groups represent a potentially important tier of biological organization, and assessing the stability and heritability of such phenotypes helps us better understand their role in evolution.

Sources of intraspecific variation in the collective tempo and synchrony of ant societies.

Populations of independently oscillating agents can sometimes synchronize. In the context of animal societies, conspicuous synchronization of activity is known in some social insects. However, the causes of variation in synchrony within and between species have received little attention. We repeatedly assessed the short-term activity cycle of ant colonies (Temnothorax rugatulus) and monitored the movements of individual workers and queens within nests. We detected persistent differences between colonies in the waveform properties of their collective activity oscillations, with some colonies consistently oscillating much more erratically than others. We further demonstrate that colony crowding reduces the rhythmicity (i.e., the consistent timing) of oscillations. Workers in both erratic and rhythmic colonies spend less time active than completely isolated workers, but workers in erratic colonies oscillate out of phase with one another. We further show that the queen's absence can impair the ability of colonies to synchronize worker activity and that behavioral differences between queens are linked with the waveform properties of their societies.

Collective aggressiveness limits colony persistence in high- but not low-elevation sites at Amazonian social spiders.

Identifying the traits that foster group survival in contrasting environments is important for understanding local adaptation in social systems. Here, we evaluate the relationship between the aggressiveness of social spider colonies and their persistence along an elevation gradient using the Amazonian spider, Anelosimus eximius. We found that colonies of A. eximius exhibit repeatable differences in their collective aggressiveness (latency to attack prey stimuli) and that colony aggressiveness is linked with persistence in a site-specific manner. Less aggressive colonies are better able to persist at high-elevation sites, which lack colony-sustaining large-bodied prey, whereas colony aggression was not related to chance of persistence at low-elevation sites. This suggests that low aggressiveness promotes colony survival in high-elevation, prey-poor habitats, perhaps via increased tolerance to resource limitation. These data reveal that the collective phenotypes that relate to colony persistence vary by site, and thus, the path of social evolution in these environments is likely to be affected.

Habitat structure changes the relationships between predator behavior, prey behavior, and prey survival rates.

The individual behavioral traits of predators and prey sometimes determine the outcome of their interactions. Here, we examine whether changes to habitat complexity alter the effects of predator and prey behavior on their survival rates. Specifically, we test whether behavioral traits (activity level, boldness, and perch height) measured in predators and prey or multivariate behavioral volumes best predict the survival rates of both trophic levels in staged mesocosms with contrasting structural complexity. Behavioral volumes and hypervolumes are a composite group-level behavioral diversity metric built from the individual-level behavioral traits we measured in predators and prey. We stocked mesocosms with a host plant and groups of cannibalistic predators (n = 5 mantises/mesocosm) and their prey (n = 15 katydids/mesocosm), and mesocosms varied in the presence/absence of additional non-living climbing structures. We found that mantis survival rates were unrelated to any behavioral metric considered here, but were higher in structurally complex mesocosms. Unexpectedly, katydids were more likely to survive when mantis groups occupied larger behavioral volumes, indicating that more behaviorally diverse predator groups are less lethal. Katydid mortality was also increased when both predators and prey exhibited higher average perch heights, but this effect was increased by the addition of supplemental structure. This is consistent with the expectation that structural complexity increases the effect of intraspecific behavioral variation on prey survival rates. Collectively, these results convey that the effects of predator and prey behavior on prey survival could depend highly on the environment in which they are evaluated.

Predator-induced selection on urchin activity level depends on urchin body size.

Temporally consistent individual differences in behavior impact many ecological processes. We simultaneously examined the effects of individual variation in prey activity level, covering behavior, and body size on prey survival with predators using an urchin-lobster system. Specifically, we tested the hypothesis that slow-moving purple sea urchins (Strongylocentrotus purpuratus) and urchins who deploy extensive substrate (pebbles and stones) covering behavior will out-survive active urchins that deploy little to no covering behavior when pitted against a predator, the California spiny lobster (Panulirus interruptus). We evaluated this hypothesis by first confirming whether individual urchins exhibit temporally consistent differences in activity level and covering behavior, which they did. Next, we placed groups of four urchins in mesocosms with single lobster and monitored urchin survival for 108 hours. High activity level was negatively associated with survival, whereas urchin size and covering behavior independently did not influence survival. The negative effect of urchin activity level on urchin survival was strong for smaller urchins and weaker for large urchins. Taken together, these results suggest that purple urchin activity level and size jointly determine their susceptibility to predation by lobsters. This is potentially of great interest, because predation by recovering lobster populations could alter the stability of kelp forests by culling specific phenotypes, like foraging phenotypes, from urchin populations.

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.

Selection for Collective Aggressiveness Favors Social Susceptibility in Social Spiders.

Particularly socially influential individuals are present in many groups [1-8], but it is unclear whether their emergence is determined by their social influence versus the social susceptibility of others [9]. The social spider Stegodyphus dumicola shows regional variation in apparent leader-follower dynamics. We use this variation to evaluate the relative contributions of leader social influence versus follower social susceptibility in driving this social order. Using chimeric colonies that combine potential leaders and followers, we discover that leader-follower dynamics emerge from the site-specific social susceptibility of followers. We further show that the presence of leaders increases colony survival in environments where leader-follower dynamics occur. Thus, leadership is driven by the "social susceptibility" of the population majority, rather than the social influence of key group members.

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.

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

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.

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.