Caste-specific processing of construction pheromones in mound-building termites

Abstract

Mound-building termites construct massive structures from soil. These structures contain intricate, interconnected passageways linking multiple chambers and atria, which house the brood and fungus gardens that support wood digestion, while also enabling efficient movement of termites. Remarkably, the major and minor workers who build these structures in their dark, subterranean milieu lack image-forming eyes. Coordinated construction on such a scale requires close communication among thousands of individuals. How do termites communicate and coordinate their activity within the mound? Previous studies have shown that communication between termites is mediated by a range of pheromones. A prominent hypothesis, the stigmergy hypothesis, suggests that termites communicate with their nestmates indirectly, by embedding chemical signals in the soil. We developed a choice assay to measure termite attraction to soil containing termite-deposited cues, offering a choice between soil from a repair site and unprocessed control soil. Using physical and chemical extraction methods, we removed volatile and non-volatile components and then measured termite attraction to the treated soils. In these experiments, termites preferred soil from their own mounds repair site over surrounding soil, indicating the presence of embedded pheromones. Of these, the non-volatile components could elicit responses to soil preserved for long periods of time. When extracted and added exogenously, these pheromones made unprocessed soil attractive to termites. Major and minor workers responded to volatile and non-volatile cues differently, indicating caste-specific responses to pheromones. These data show that termites use soil as a medium for communication, consistent with the stigmergy hypothesis. SignificanceMound-building termites achieve the collective construction of elaborate structures through finely tuned coordination of their building behaviors. Lacking image-forming eyes, they rely heavily on a sophisticated chemical communication system by embedding pheromones in the soil that their nestmates sense and interpret, to coordinate behavior. To investigate this communication system, we conducted a series of experiments using a novel choice assay which measures the behavioural responses of termites to pheromone cues in the soil. These pheromones contain volatile and non-volatile components to which the termites respond in a caste-specific manner. The non-volatile components elicit responses over a very long period. Our findings provide new insights into the chemical communication that drives collective behavior in social termites, with implications for collective robotics.