Souvik Mandal

The solution of complex problems by the collective action of simple agents in both biologically evolved and synthetically engineered systems involves cooperative action. Understanding the resulting emergent solutions requires integrating across the organismal behavior of many individuals. Here, we investigate an ecologically relevant collective task in black carpenter ants Camponotus pennsylvanicus: excavation of a soft, erodible confining corral. These ants show a transition from individual exploratory excavation at random locations to spatially localized collective exploitative excavation and escape from the corral. Agent-based simulations and a minimal continuum theory that coarse-grains over individual actions and considers their integrated influence on the environment leads to the emergence of an effective phase space of behaviors, characterized in terms of excavation strength and cooperation intensity. To test the theory over the range of both observed and predicted behaviors, we use custom-built robots (RAnts) that respond to stimuli to characterize the phase space of emergence (and failure) of cooperative excavation. Tuning the amount of cooperation between RAnts, allows us to vary the efficiency of excavation and synthetically generate the entire range of macroscopic phases predicted by our theory. Overall, our approach shows how the cooperative completion of tasks can arise from simple rules that involve the interaction of agents with a dynamically changing environment that serves as both an enabler and a modulator of behavior.

Desert ants and honey bees start foraging when they are few days old, and subsequently increase their foraging effort and the amount of foraged food. This could be an optimal strategy for scavenger/gatherer animals inhabiting less-featured landscapes. Animals inhabiting cluttered landscapes, especially predatory ones, however, may need substantial familiarity with foraging landscapes to forage efficiently. They may acquire such spatial familiarity with increasing age/experience, and eventually reduce their foraging effort without compromising on foraging success/efficiency. To check whether this holds for individually-foraging predatory tropical paper-wasp Ropalidia marginata, we recorded the number and duration of all foraging trips, the identity of foraged materials, and the directions of outbound and inbound flights (with respect to the nest) of known-age wasps for three consecutive days from three naturally-occurring colonies – thus, we measured behavioural profiles of wasps of various ages, and not from the same wasp throughout its lifespan. Wasps increased their foraging duration rapidly until about four weeks of age, during which they rarely brought food, although some wasps brought building material and water. Thereafter, their foraging duration started decreasing. Nevertheless, their foraging success/efficiency in bringing food kept on increasing. With age, wasps developed individual directional preferences for outbound and inbound flights, indicating the development of spatial memory for rewarding sites. Also, the angular difference between their outbound and subsequent inbound flights gradually increased, indicating older wasps may have followed tortuous foraging routes. High investment in early-life to acquire familiarity with foraging landscapes and using that later to perform efficient foraging could be an optimal strategy for individually-foraging animals inhabiting feature-rich landscapes.

Possessing spatial familiarity with their foraging landscape may enable animals to reduce foraging effort without compromising on foraging benefits. For animals inhabiting feature-rich landscapes, spatial familiarity can increase with increasing age/experience. To check whether this holds for individually foraging tropical social wasp Ropalidia marginata , we recorded the number and duration of all foraging trips, the identity of the materials brought to the nest (building material, water or food) and the directions of outbound and inbound flights (respective to their nests) of known-age foragers from three natural colonies, each for three consecutive days. The average trip duration and time spent daily in foraging increased rapidly until about first four weeks of their life, during which they rarely brought food to their nest, although many of them brought building material and water. Thereafter, their average as well as per day duration of foraging trip started decreasing gradually. Nevertheless, their foraging efficiency and success for food kept on increasing monotonically with age. These results suggest that older wasps were more efficient in foraging despite spending less time doing so. With increasing age, wasps developed individual preferences for the direction of their outbound flights, increased directionality of their inbound trips as well as the angular difference between their outbound and subsequent inbound flights, indicating development of spatial memory. We conclude that wasps acquire familiarity with their foraging landscape in their initial foraging phase and gradually develop robust memory for rewarding sites and routes to those sites, which enables them to increase their foraging capabilities. SUMMARY STATEMENT: Contrary to insects inhabiting less-featured landscapes, tropical social wasps invest weeks to get familiar with foraging landscapes during their early foraging lives. This eventually enables them to increase foraging gain with reduced effort.

In primitively eusocial insects, many individuals function as workers despite being capable of independent reproduction. Such altruistic behaviour is usually explained by the argument that workers gain indirect fitness by helping close genetic relatives. The focus on indirect fitness has left open the question of whether workers are also capable of getting direct fitness in the future in spite of working towards indirect fitness in the present. To investigate this question, we recorded behavioural profiles of all wasps on six naturally occurring nests of Ropalidia marginata , and then isolated all wasps in individual plastic boxes, giving them an opportunity to initiate nests and lay eggs. We found that 41% of the wasps successfully did so. Compared to those that failed to initiate nests, those that did were significantly younger, had significantly higher frequency of self-feeding behaviour on their parent nests but were not different in the levels of work performed in the parent nests. Thus ageing and poor feeding, rather than working for their colonies, constrain individuals for future independent reproduction. Hence, future direct fitness and present work towards gaining indirect fitness are not incompatible, making it easier for worker behaviour to be selected by kin selection or multilevel selection.

The defence of a society often requires that some specialized members coordinate to repel a threat at personal risk. This is especially true for honey bee guards, which defend the hive and may sacrifice their lives upon stinging. Central to this cooperative defensive response is the sting alarm pheromone, which has isoamyl acetate (IAA) as its main component. Although this defensive behaviour has been well described, the neural mechanisms triggered by IAA to coordinate stinging have long remained unknown. Here we show that IAA upregulates brain levels of serotonin and dopamine, thereby increasing the likelihood of an individual bee to attack and sting. Pharmacological enhancement of the levels of both amines induces higher defensive responsiveness, while decreasing them via antagonists decreases stinging. Our results thus uncover the neural mechanism by which an alarm pheromone recruits individuals to attack and repel a threat, and suggest that the alarm pheromone of honey bees acts on their response threshold rather than as a direct trigger.

Significance: Cooperation and division of labor are two important features of eusocial insects such as ants, bees, wasps, and termites. Using the primitively eusocial waspRopalidia marginata, we investigated the minimum requirements for the emergence of cooperation and division of labor, both reproductive and nonreproductive, and their effect on productivity (i.e., total brood of a colony). We show that (i) two wasps are adequate for the emergence of reproductive division of labor and cooperation and that three wasps are both necessary and sufficient for the additional emergence of nonreproductive division of labor and (ii) reproductive division of labor and cooperation are inadequate for increasing productivity, which comes about only with the addition of nonreproductive division of labor.

We captured foragers of the tropical social wasp Ropalidia marginata from their nests and displaced them at different distances and directions. Wasps displaced within their probable foraging grounds returned to their nests on the day of release although they oriented randomly upon release; however, wasps fed before release returned sooner, displaying nest-ward orientation. When displaced to places far from their nests, thus expected to be unfamiliar, only a third returned on the day of release showing nest-ward orientation; others oriented randomly and either returned on subsequent days or never. When confined within mosquito-net tents since eclosion and later released to places close to their nests (but unfamiliar), even fed wasps oriented randomly, and only older wasps returned, taking longer time. Thus, contrary to insects inhabiting less-featured landscapes, R. marginata foragers appear to have thorough familiarity with their foraging grounds that enables them to orient and home efficiently after passive displacement. Their initial orientation is, however, determined by an interaction of the information acquired from surrounding landscape and their physiological motivation. With age, they develop skills to home from unfamiliar places. Homing behaviour in insects appears to be influenced by evolutionarily conserved mechanisms and the landscape in which they have evolved.