Noa Pinter-Wollman

Behavioural syndromes and social insects: personality at multiple levels.

Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across two or more situations within a population. Social insect biologists have measured consistent individual variation in behaviour within and across colonies for decades. The goal of this review is to illustrate the ways in which both the study of social insects and of behavioural syndromes has overlapped, and to highlight ways in which both fields can move forward through the synergy of knowledge from each. Here we, (i) review work to date on behavioural syndromes (though not always referred to as such) in social insects, and discuss mechanisms and fitness effects of maintaining individual behavioural variation within and between colonies; (ii) summarise approaches and principles from studies of behavioural syndromes, such as trade‐offs, feedback, and statistical methods developed specifically to study behavioural consistencies and correlations, and discuss how they might be applied specifically to the study of social insects; (iii) discuss how the study of social insects can enhance our understanding of behavioural syndromes—research in behavioural syndromes is beginning to explore the role of sociality in maintaining or developing behavioural types, and work on social insects can provide new insights in this area; and (iv) suggest future directions for study, with an emphasis on examining behavioural types at multiple levels of organisation (genes, individuals, colonies, or groups of individuals).

The effect of individual variation on the structure and function of interaction networks in harvester ants.

Social insects exhibit coordinated behaviour without central control. Local interactions among individuals determine their behaviour and regulate the activity of the colony. Harvester ants are recruited for outside work, using networks of brief antennal contacts, in the nest chamber closest to the nest exit: the entrance chamber. Here, we combine empirical observations, image analysis and computer simulations to investigate the structure and function of the interaction network in the entrance chamber. Ant interactions were distributed heterogeneously in the chamber, with an interaction hot-spot at the entrance leading further into the nest. The distribution of the total interactions per ant followed a right-skewed distribution, indicating the presence of highly connected individuals. Numbers of ant encounters observed positively correlated with the duration of observation. Individuals varied in interaction frequency, even after accounting for the duration of observation. An ants interaction frequency was explained by its path shape and location within the entrance chamber. Computer simulations demonstrate that variation among individuals in connectivity accelerates information flow to an extent equivalent to an increase in the total number of interactions. Individual variation in connectivity, arising from variation among ants in location and spatial behaviour, creates interaction centres, which may expedite information flow.

How is activity distributed among and within tasks in Temnothorax ants

How social insect colonies behave results from the actions of their workers. Individual variation among workers in their response to various tasks is necessary for the division of labor within colonies. A worker may be active in only a subset of tasks (specialist), perform all tasks (elite), or exhibit no particular pattern of task activity (idiosyncratic). Here we examine how worker activity is distributed among and within tasks in ants of the genus Temnothorax. We found that workers exhibited elitism within a situation, i.e., in particular sets of tasks, such as those associated with emigrations, nest building, or foraging. However, there was weak specialization for working in a particular situation. A few workers exhibited elitism across all situations, i.e., high performance in all tasks in all situations. Within any particular task, the distribution of activity among workers was skewed, with few ants performing most of the work and most ants performing very little of the work. We further found that workers persisted in their task preference over days, with the same individuals performing most of the work day after day. Interestingly, colonies were robust to the removal of these highly active workers; they were replaced by other individuals that were previously less active. This replacement was not short-lived; when the removed individuals were returned to the colony, not all of them resumed their prior high activity levels, and not all the workers that replaced them reduced their activity. Thus, even though some workers specialize in tasks within a particular situation and are persistent in performing them, task allocation in a colony is plastic and colonies can withstand removal of highly active individuals.

Harvester ants use interactions to regulate forager activation and availability

Social groups balance flexibility and robustness in their collective response to environmental changes using feedback between behavioural processes that operate at different timescales. Here we examine how behavioural processes operating at two timescales regulate the foraging activity of colonies of the harvester ant, Pogonomyrmex barbatus, allowing them to balance their response to food availability and predation. Previous work showed that the rate at which foragers return to the nest with food influences the rate at which foragers leave the nest. To investigate how interactions inside the nest link the rates of returning and outgoing foragers, we observed outgoing foragers inside the nest in field colonies using a novel observation method. We found that the interaction rate experienced by outgoing foragers inside the nest corresponded to forager return rate, and that the interactions of outgoing foragers were spatially clustered. Activation of a forager occurred on the timescale of seconds: a forager left the nest 3-8 s after a substantial increase in interactions with returning foragers. The availability of outgoing foragers to become activated was adjusted on the timescale of minutes: when forager return was interrupted for more than 4-5 min, available foragers waiting near the nest entrance went deeper into the nest. Thus, forager activation and forager availability both increased with the rate at which foragers returned to the nest. This process was checked by negative feedback between forager activation and forager availability. Regulation of foraging activation on the timescale of seconds provides flexibility in response to fluctuations in food abundance, whereas regulation of forager availability on the timescale of minutes provides robustness in response to sustained disturbance such as predation.

Individual variation in exploratory behaviour improves speed and accuracy of collective nest selection by Argentine ants

Collective behaviours are influenced by the behavioural composition of the group. For example, a collective behaviour may emerge from the average behaviour of the groups constituents, or be driven by a few key individuals that catalyse the behaviour of others in the group. When ant colonies collectively relocate to a new nest site, there is an inherent trade-off between the speed and accuracy of their decision of where to move due to the time it takes to gather information. Thus, variation among workers in exploratory behaviour, which allows gathering information about potential new nest sites, may impact the ability of a colony to move quickly into a suitable new nest. The invasive Argentine ant, Linepithema humile, expands its range locally through the dispersal and establishment of propagules: groups of ants and queens. We examine whether the success of these groups in rapidly finding a suitable nest site is affected by their behavioural composition. We compared nest choice speed and accuracy among groups of all-exploratory, all-nonexploratory and half-exploratory-half-nonexploratory individuals. We show that exploratory individuals improve both the speed and accuracy of collective nest choice, and that exploratory individuals have additive, not synergistic, effects on nest site selection. By integrating an examination of behaviour into the study of invasive species we shed light on the mechanisms that impact the progression of invasion.

Harvester Ant Colony Variation in Foraging Activity and Response to Humidity

Collective behavior is produced by interactions among individuals. Differences among groups in individual response to interactions can lead to ecologically important variation among groups in collective behavior. Here we examine variation among colonies in the foraging behavior of the harvester ant, Pogonomyrmex barbatus. Previous work shows how colonies regulate foraging in response to food availability and desiccation costs: the rate at which outgoing foragers leave the nest depends on the rate at which foragers return with food. To examine how colonies vary in response to humidity and in foraging rate, we performed field experiments that manipulated forager return rate in 94 trials with 17 colonies over 3 years. We found that the effect of returning foragers on the rate of outgoing foragers increases with humidity. There are consistent differences among colonies in foraging activity that persist from year to year.

Interactions with combined chemical cues inform harvester ant foragers' decisions to leave the nest in search of food.

Social insect colonies operate without central control or any global assessment of what needs to be done by workers. Colony organization arises from the responses of individuals to local cues. Red harvester ants (Pogonomyrmex barbatus) regulate foraging using interactions between returning and outgoing foragers. The rate at which foragers return with seeds, a measure of food availability, sets the rate at which outgoing foragers leave the nest on foraging trips. We used mimics to test whether outgoing foragers inside the nest respond to the odor of food, oleic acid, the odor of the forager itself, cuticular hydrocarbons, or a combination of both with increased foraging activity. We compared foraging activity, the rate at which foragers passed a line on a trail, before and after the addition of mimics. The combination of both odors, those of food and of foragers, is required to stimulate foraging. The addition of blank mimics, mimics coated with food odor alone, or mimics coated with forager odor alone did not increase foraging activity. We compared the rates at which foragers inside the nest interacted with other ants, blank mimics, and mimics coated with a combination of food and forager odor. Foragers inside the nest interacted more with mimics coated with combined forager/seed odors than with blank mimics, and these interactions had the same effect as those with other foragers. Outgoing foragers inside the nest entrance are stimulated to leave the nest in search of food by interacting with foragers returning with seeds. By using the combined odors of forager cuticular hydrocarbons and of seeds, the colony captures precise information, on the timescale of seconds, about the current availability of food.

Fast and Flexible: Argentine Ants Recruit from Nearby Trails

Argentine ants (Linepithema humile) live in groups of nests connected by trails to each other and to stable food sources. In a field study, we investigated whether some ants recruit directly from established, persistent trails to food sources, thus accelerating food collection. Our results indicate that Argentine ants recruit nestmates to food directly from persistent trails, and that the exponential increase in the arrival rate of ants at baits is faster than would be possible if recruited ants traveled from distant nests. Once ants find a new food source, they walk back and forth between the bait and sometimes share food by trophallaxis with nestmates on the trail. Recruiting ants from nearby persistent trails creates a dynamic circuit, like those found in other distributed systems, which facilitates a quick response to changes in available resources.

Nest architecture shapes the collective behaviour of harvester ants.

Structures influence how individuals interact and, therefore, shape the collective behaviours that emerge from these interactions. Here I show that the structure of a nest influences the collective behaviour of harvester ant colonies. Using network analysis, I quantify nest architecture and find that as chamber connectivity and redundancy of connections among chambers increase, so does a colonys speed of recruitment to food. Interestingly, the volume of the chambers did not influence speed of recruitment, suggesting that the spatial organization of a nest has a greater impact on collective behaviour than the number of workers it can hold. Thus, by changing spatial constraints on social interactions organisms can modify their behaviour and impact their fitness.

A search for principles of disability using experimental impairment of Drosophila melanogaster

The results of life table experiments to determine the effects of artificial impairment (leg amputation) in 7500 Drosophila melanogaster adults revealed that the extent to which life expectancy was reduced in impaired individuals was conditional on: (1) leg location and number amputated--front leg had greatest impact and the number of legs amputated directly correlated with mortality impact; (2) age of amputation--the greatest relative reduction in remaining life expectancy occurred when young flies were impaired; (3) vial orientation--mortality in impaired flies was the least when vials held upside-down (most friendly environment) and the greatest when they were right-side up (least friendly environment); and (4) sex--male mortality was increased more than female mortality in nearly all impairment treatments. These results were used to formulate a set of general principles of disability that would apply not only to humans but to all organisms.