Souvik Mandal

Cooperative defence operates by social modulation of biogenic amine levels in the honey bee brain

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.

Emergence of cooperation and division of labor in the primitively eusocial wasp Ropalidia marginata

Significance Cooperation and division of labor are two important features of eusocial insects such as ants, bees, wasps, and termites. Using the primitively eusocial wasp Ropalidia 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. In most primitively eusocial wasps new nests are initiated by a single female or by small groups of females. To study the emergence of division of labor (DOL) among the nest foundresses and to determine its possible effect on nest productivity we maintained newly eclosed females of Ropalidia marginata in small boxes with one, two, or three nestmate wasps of the same age per box. Only one wasp developed her ovaries and laid eggs in each box, while the other wasp(s) built the nest, brought food, and fed larvae, demonstrating the spontaneous emergence of reproductive DOL in the presence of more than one wasp. In nests with three wasps there was also a strong negative correlation between intranidal and extranidal work performed by the two nonreproductive workers, suggesting the spontaneous emergence of nonreproductive DOL; such nonreproductive DOL was absent in nests with two wasps. Both reproductive and nonreproductive DOL were modulated by dominance behavior (DB). In nests with two wasps the egg layer showed significantly more DB than the non-egg layer before nest initiation; in nests with three wasps queens showed significantly more DB than intranidal workers, which in turn showed significantly more DB than extranidal workers. Productivities of nests (as measured by total brood on the day of eclosion of the first adult) initiated by one or two wasps were not different from each other but were significantly lower than that of three wasps. Thus, nonreproductive DOL, and not merely reproductive DOL, is necessary for increase in productivity.

Homing abilities of the tropical primitively eusocial paper wasp Ropalidia marginata

Compared to our extensive knowledge about the navigation and homing abilities of ants and bees, we know rather little about these phenomena in social wasps. Here, we report the homing abilities of the tropical primitively eusocial wasp Ropalidia marginata and the factors that affect their homing success. To determine from how far these wasps can return to their nests, we transported foragers blindfold and released them at gradually increasing distances from their nests in four cardinal directions. Their homing success was determined by checking their presence on their nests on three consecutive nights. All foragers (56 individuals, 115 releases) returned back from an area of 0.73xa0±xa00.25xa0km2 on the day of release (minimal homing area), whereas 83.8xa0% of the foragers (217 individuals, 420 releases) returned when we enlarged the area of release to 6.22xa0±xa00.66xa0km2 around their nests (maximal homing area). Of 66 releases, no wasps returned from beyond the maximal homing area. The minimal homing area might be familiar to the foragers because they probably routinely forage in this area and the maximal homing area represents the maximum distances from which the wasps are capable of returning to their nests, with or without familiarity.

Homing in a tropical social wasp: role of spatial familiarity, motivation and age

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.

Ontogeny of familiarity with foraging landscape and foraging abilities in the tropical social wasp Ropalidia marginata

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.

A Route to Direct Fitness: Natural and Experimentally Induced Queen Succession in the Tropical Primitively Eusocial Wasp Ropalidia marginata

Insect societies are hallmarks of cooperation because one or a few queens monopolize reproduction and several non-reproductive workers cooperatively raise brood. However, the loss of the queen exposes a colony to potential reproductive conflict, which is resolved only after a new queen takes over. We studied queen succession in natural and experimental colonies of the primitively eusocial wasp Ropalidia marginata to understand the proximate behavioral strategies involved in the resolution of this conflict. Previous work has shown that in this species, experimental queen removal always results in only one worker becoming hyper-aggressive and taking over the colony as its next queen, without ever being challenged. Here we show that even during natural queen turnover, one and only one worker becomes hyper-aggressive and takes over as the next queen, without being challenged. During natural queen turn-over, aggression of the successor may sometimes begin before the loss of the old queen and may sometimes decline more rapidly, unlike in the case of experimental queen removal. The successor begins to lay eggs sooner after a natural queen turn-over as compared to experimental queen removal. This is expected because workers might detect the gradual decline of the queen preceding her disappearance. Because queen succession is expected to be more prevalent in tropical perennial species, we expect natural selection to have favored such an orderly queen succession so that a route to direct fitness is available without significant reduction in cooperation.

How do animals find their way back home? A brief overview of homing behavior with special reference to social Hymenoptera

Performing efficient homing, i.e., returning to a previously known place, is crucial for the survival of any motile animal. Animals perform homing across different spatial scales and environments, employing various mechanisms with the aid of different sensorimotor systems molded by their varied evolutionary histories and ecological constraints. Despite these differences, most of the homing mechanisms across different taxa can be explained by some general basic mechanisms. Studies from social hymenopterans contribute substantially to the knowledge base of this study field and are, especially, interesting—they show excellent homing capabilities while possessing relatively simple neural architectures, and hence, their homing mechanisms are considered as economic solutions to a complex problem. Moreover, many of their homing mechanisms have also been observed in other taxa including vertebrates. With the advent of new technologies and increased research, our understanding of the hymenopteran homing is improving faster than ever—and therefore, a regular contemporary update might be of much help. In this review, I present a brief synthesis of previous and current understanding of homing mechanisms in social hymenopterans, with descriptions of the cues that they exploit for homing, and a comparative discussion on terminologies frequently used in social Hymenoptera with analogous terminologies used to describe similar phenomena in other taxa. I conclude with a note on the potential of applying the knowledge from homing studies in other fields of research like neurobiology and robotics, and possible future directions.

Current indirect fitness and future direct fitness are not incompatible

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.