Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate-Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)

Simple Summary Grooming is a common behavior in animals. It serves the function of removing foreign materials and excessive amounts of self-secreted materials from the body's surface. Social insects, such as honeybees or ants, use various types of pheromones, some of which propagate information about the environment to conspecific individuals, for chemical communication. The individuals that receive such information can respond with suitable behaviors to protect themselves and their society. Hence, grooming is important for the maintenance of the correct performance of their sensory organs on antennae for pheromone perception. Here, we experimentally limited self-grooming of the antennae in workers of the Japanese carpenter ant (Camponotus japonicus) by removing a pair of antennal cleaning apparatuses from the forelegs and investigated their behavioral change in response to exposure to the alarm pheromone or to encounters with nestmates or non-nestmates. Comparisons between self-grooming-nonlimited and self-grooming-limited ants showed that the self-grooming-limited ants gradually exhibited decreased locomotion activity in their fight-or-flight response to the alarm pheromone and experienced increased failure in nestmate and non-nestmate discrimination. Thus, the results of the present study suggest that antennal sensory system maintenance supports social communication, which is indispensable not only to the individual workers but also to the survival of their society. Self-grooming of the antennae is frequently observed in ants. This antennal maintenance behavior is presumed to be essential for effective chemical communication but, to our knowledge, this has not yet been well studied. When we removed the antenna-cleaning apparatuses of the Japanese carpenter ant (C. japonicus) to limit the self-grooming of the antennae, the worker ants demonstrated the self-grooming gesture as usual, but the antennal surface could not be sufficiently cleaned. By using scanning electron microscopy with NanoSuit, we observed the ants' antennae for up to 48 h and found that the antennal surfaces gradually became covered with self-secreted surface material. Concurrently, the self-grooming-limited workers gradually lost their behavioral responsiveness to undecane-the alarm pheromone. Indeed, their locomotive response to the alarm pheromone diminished for up to 24 h after the antenna cleaner removal operation. In addition, the self-grooming-limited workers exhibited less frequent aggressive behavior toward non-nestmate workers, and 36 h after the operation, approximately half of the encountered non-nestmate workers were accepted as nestmates. These results suggest that the antennal sensing system is affected by excess surface material; hence, their proper function is prevented until they are cleaned.

Automated summary

Grooming is a common behavior in animals that serves to remove foreign and self-secreted materials from the body surface. Social insects, like honeybees or ants, use pheromones for chemical communication. Limiting self-grooming of antennae in Japanese carpenter ants led to decreased locomotion activity in response to alarm pheromones and impaired discrimination between nestmates and non-nestmates, highlighting the importance of antennal sensory system maintenance for social communication.