Sean O’Donnell

Worker connectivity: a review of the design of worker communication systems and their effects on task performance in insect societies

Abstract.Within-group communication is a fundamental feature of animal societies. In order for animal groups to function as adaptive units, the members must share information such that group mates respond appropriately to each others’ behavior. One important function of social communication is to affect the allocation of tasks among group members. Theoretical and empirical findings on a diverse array of social insect taxa show that interactions among workers often play important roles in structuring division of labor. We review worker interactions that regulate division of labor in insect societies, which we refer to as worker connectivity. We present a framework for synthesizing and analyzing the study of worker connectivity. The widespread reliance on worker connectivity among eusocial insect taxa and the diversity of communicative mechanisms used to recruit workers suggest that the nature of worker interactions has evolved by natural selection. We suggest that colony-level selection acting on variation in task allocation has been an important force in the evolution of mechanisms for worker connectivity. We also propose that there are important links between individual worker cognition and task allocation at the colony level. Evolutionary changes in the cognitive aspects of worker responses may affect task allocation as much as changes in the communicative signals themselves.

Mushroom Body Volume Is Related to Social Aggression and Ovary Development in the Paperwasp Polistes instabilis

The mushroom bodies (MB) are a complex neuropil in insect brains that have been implicated in higher-order information processing such as sensory integration and various types of learning and memory. Eusocial insects are excellent models to test functional neural plasticity in the MB because genetically related nest mates differ in task performance, environmental experience and social interactions. Previous research on eusocial insects shows that experience-dependent changes in brain anatomy (i.e., enlarged MB calyces) are positively correlated with task performance and social interactions. In this study, we quantified relationships of task performance and social and reproductive dominance with MB volume in Polistes instabilis, a primitively eusocial paper wasp. We used experimental removals of dominant workers to induce changes in aggressive behavior and foraging by workers. Ovary development and social dominance were positively associated with the volume of the MB calyces relative to the region containing the Kenyon cell bodies. In contrast to highly eusocial insect workers, foraging behavior was not positively correlated with MB calycal volume. We conclude that mushroom body volume is more strongly associated with dominance rank than with foraging behavior in Polistes instabilis.

Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae)

Adult workers of some social insect species show dramatic behavioral changes as they pass through a sequence of task specializations. In the paper wasp, Polybia aequatorialis, female workers begin adult life within the nest tending brood, progress to maintaining and defending the nest exterior, and ultimately leave the nest to forage. The mushroom body (MB) calyx neuropil increases in volume as workers progress from in-nest to foraging tasks. In other social Hymenoptera (bees and ants), MB Kenyon cell dendrites, axons and synapses change with the transition to foraging, but these neuronal effects had not been studied in wasps. Furthermore, the on-nest worker of Polybia wasps, an intermediate task specialization not identified in bees or ants, provides the opportunity to study pre-foraging worker class transitions. We asked whether Kenyon cell dendritic arborization varies with the task specialization of Polybia workers observed in the field near Monteverde, Costa Rica. Golgi-impregnated arbors in the lip and collar calyces, which receive a predominance of olfactory and visual input, respectively, were quantified using Sholls concentric circles and a novel application of virtual spherical probes. Arbors of the lip varied in a manner reminiscent of honeybees, with foragers having the largest and in-nest workers having the smallest arbors. In contrast, arbors of the collar were largest in foragers but smallest in on-nest workers. Thus, progression through task specializations in P. aequatorialis involves subregion specific dendritic growth and regression in the MB neuropil. These results may reflect the sensitivity of Kenyon cell dendritic structure to specialization dependent social and sensory experience.

Predation and patchiness in the tropical litter: do swarm-raiding army ants skim the cream or drain the bottle?

1. Swarm-raiding army ants have long been considered as episodic, catastrophic agents of disturbance in the tropical litter, but few quantitative data exist on their diets, preferences, and, critically, their ability to deplete prey. 2. Here, we provide such data for two common species of swarm raiders broadly sympatric throughout the Neotropics: the iconic Eciton burchellii and the more secretive, less studied Labidus praedator. In Ecuador, Costa Rica, Venezuela and Panama, patches of forest floor were sampled for litter invertebrates immediately before and after army ant raids. These invertebrates have been shown to regulate decomposition and vary 100-fold in local densities across the forest floor. 3. Contrary to Ecitons popular image, only Labidus consistently reduced the biomass of litter invertebrates and only then by an average of 25%. Ecitons impacts were concentrated on rich patches of invertebrates, while Labidus prey depletion showed no such density dependence. Labidus reduced the biomass of some invertebrates-isopods, larviforms and coleoptera-by up to 75%; Eciton showed no such prey preferences. 4. Our results suggest that Eciton specializes on high biomass patches, while Labidus feeds profitably from any litter patch. Combined, these swarm raiders sum to be chronic, but not catastrophic, predators of common litter invertebrates of the brown food web.

Worker reproductive competition affects division of labor in a primitively social paperwasp (Polistes instabilis)

Abstract.Social insects are premier models for studying the evolution of self-organization in animal societies. Primitively social species may be informative about the early stages of social evolution and transitions in self-organization. Previous worker removal studies in Polistes instabilis paper wasps suggested that dominant but non-egglaying workers play an important role in regulating rates of task performance by inducing foraging in subordinates. We extend previous worker removal studies by quantifying changes in individuals’ behavior following removals, and by measuring associations between behavioral change and individuals’ reproductive capacity (ovary development). Workers changed their rates of aggressive behaviors more than queens following the dominant worker removals. Increases in worker’s rates of aggressive behaviors were correlated with decreases in their foraging rates. Changes in individual rates of social aggression were associated with their reproductive capacity: worker females with well-developed ovaries increased their rates of aggression. Further changes in rates of aggression after the dominant workers were returned also depended on ovary development. These patterns suggest that task performance and potential fecundity are linked in workers, and that worker interactions play a strong role in regulating task performance. We conclude that worker reproductive competition may have influenced the evolution of colony organization in social insects.

Body size shapes caste expression, and cleptoparasitism reduces body size in the facultatively eusocial bees Megalopta (Hymenoptera : Halictidae)

We used the facultatively social sweat bee Megalopta genalis (Halictidae) to test whether body size is associated with social caste. Behavioral observations showed that non-reproductive foragers were significantly smaller than reproductive nest mate queens, and foragers were also smaller than presumed pre-dispersal reproductives. Moreover, among females from field-collected nests without behavioral observations, relative body size correlated with relative ovary size. Reproductive status is not a direct result of body size, as body size was not significantly associated with either ovary size or fecundity among both solitary and social reproductives. Reproductive status is apparently an outcome of social competition for reproductive dominance, and status is influenced by size relative to nest mates. Our study is the first to demonstrate an association of body size with caste expression in a facultatively social species with relatively weak seasonal constraints on independent nesting. Larvae of a parasitic fly (Fiebrigella sp., Chloropidae) consume pollen provisions stored in nest cells of M. genalis and M. ecuadoria. We tested whether fly parasitism of M. genalis reduces body size. Parasitized females are significantly smaller as adults than their unparasitized nestmates. This reduction is of a similar magnitude to the size differences between castes, and has the potential to shape host reproductive options by influencing competition with nest mates. We present data on the prevalence of parasitism from four collections of M. genalis and two collections of M. ecuadoria from Barro Colorado Island, Panama, and La Selva, Costa Rica.

Species and site differences in Neotropical army ant emigration behaviour

Abstract 1. Along with large wingless queens and group foraging raids, periodic colony movements or emigrations are a defining feature of army ant behaviour. Emigrations are important because they regulate spacing among colonies, and provide access to new foraging sites.

Elevational and geographic variation in army ant swarm raid rates

Geographic and elevational variation in the local abundance of swarm-raiding army ants has implications for the population dynamics of their prey, as well as affecting the profitability of army-ant-following behavior for birds. Here, we analyze systematically collected data on E. burchellii and L. praedator raid rates from geographically and elevationally wide-ranging sites, from lowland to montane forests. We show that raids of each species, and of both species pooled, reach peak densities at intermediate (premontane) elevations. These patterns suggest that army ant swarm raids are relatively abundant in Neotropical montane forests. Therefore, a paucity of ant raids does not explain the absence of obligate ant-following bird species, particularly true antbirds (Thamnophilidae), from montane forests. As army ant raids are relatively common at middle elevations, opportunities exist for other montane bird taxa to exploit army ant raids as a food source.

Worker connectivity: a simulation model of variation in worker communication and its effects on task performance

Abstract.We develop a simulation model of worker connectivity to analyze how variation in worker communication can influence task performance. The model generates predictions about how colony demography, worker communicative behavior, and worker cognition will affect the rate of recruitment of workers to a new task. The model explores some mechanisms for modulating the recruitment of workers. Under the conditions of our model– probabilistic interactions that lower worker’s response thresholds to tasks– worker recruitment follows a logistic growth pattern. The rate of recruiting workers increases exponentially toward an inflection point when 50% of the available force has been activated, then decreases toward the upper asymptote (all workers recruited). Many relevant features of colony design and worker behavior, including group size, probability of interacting, and strength of interaction effects on receivers, show a positive but decelerating effect on the rate of worker recruitment. We also identify features of worker cognition that can influence task recruitment, focusing on the time course of worker’s memories about previous interactions. Both learning (e.g., sensitization) and forgetting about previous interactions can influence the rate of worker recruitment to a task. The model suggests that worker cognition may be shaped by natural selection on task performance at the colony level. Forgetting about interactions may be especially costly, because it leads to unpredictable patterns of worker recruitment. We also show that social inhibition, when coupled with excitatory interactions, can effectively modulate worker recruitment at the colony level.

Choice of nest site protects army ant colonies from environmental extremes in tropical montane forest

Unlike most social insects, Eciton burchellii army ants cannot thermoregulate through nest construction. Instead, army ants thermoregulate behaviorally by creating a living nest (bivouac), shifting its position and structure, and potentially through nest site selection. We hypothesized that bivouac site selection is critical to E. burchellii colony survival. We predicted elevation above sea level, with associated variation in local abiotic environments, would affect bivouac site selection by E. burchellii colonies. We also expected nest sites to buffer against ambient variation in abiotic conditions. We recorded bivouac site choice by E. burchellii colonies at sites ranging from lowland wet forests to montane forests and reviewed previously published data. We measured microclimatic variables associated with nest sites in high-elevation montane forests: temperature, relative humidity, and light levels. Bivouac site selection varied with elevation: as elevation increased, fewer bivouac sites were exposed, more were underground, and fewer were elevated (in trees). High-elevation bivouac sites moderated diurnal temperature variation and had higher relative humidity levels and lower light levels than ambient conditions. The buffering of ambient temperature and humidity decreased with elevation in montane forests, suggesting that abiotic extremes in bivouac sites at the highest elevations may contribute to the upper elevational range limits of E. burchellii.