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Double allomimesis of advancing and retreating individuals maintains cohesion in exploring groups of nomadic caterpillars

Despland, Emma, Gervais, David, Morcos, Lisanne
Behavioral ecology and sociobiology 2017 v.71 no.3 pp. 56
Malacosoma disstria, animals, cohesion, group size, insect larvae, instars, locomotion, models, prices, social insects, trail pheromones
Group-living entails that animals maintain cohesion during collective locomotion: This cohesion often requires that each individual respond to cues from several neighbours. Social insects generally use pheromone trails to integrate information from multiple group members. We demonstrate mechanisms used by nomadic social caterpillars to maintain cohesion when exploring off-trail. Our results show that forest tent caterpillars (Malacosoma disstria) use double allomimesis, responding to cues from both advancing and retreating neighbours. A group-level experiment measured cohesion and persistence of locomotion according to caterpillar age and group size. An individual-level experiment quantified responses to cues from neighbours, and a model was used to predict the group-level patterns that emerge from these responses. We show that double allomimesis generates feedback that maintains group cohesion, but at the price of locomotion efficiency, particularly in small groups of young caterpillars. We also show that the importance of allomimesis decreases as caterpillars age and show lesser responses to social cues. Finally, we demonstrate that, especially in the early instars, efficient collective locomotion is only possible in the large group sizes typically of field colonies. SIGNIFICANCE STATEMENT: Simple do-what-your-neighbour-is-doing mechanisms underlie mass collective locomotion of gregarious animals. Social insects generally use pheromone trails to follow each other. How then to stay together when exploring away from these trails? Forest tent caterpillars provide an intriguing example: They follow trails faithfully, but on unexplored territory turn back frequently to rejoin the trail behind them. We show how direct physical contact with advancing and retreating neighbours provides an explanation. An off-trail caterpillar turns back less often if it is propelled by a forward-moving neighbour, but more often if that neighbour turns back. This dual imitation keeps the group together, but at the price of efficient movement, especially in small groups. Groups as large as natural colonies seldom turn back due to the steady supply of advancing neighbours to propel forward and eventually replace vanguard individuals.