Getting lost: the fungal hijacking of ant foraging behaviour in space and time

Abstract

Many parasites have evolved strategies to exploit host behaviour for successful transmission. Ophiocordyceps manipulations of carpenter ant behaviour represent an evident example. Manipulated ants are coerced to ascend vegetation and clamp down their mandibles in a stereotypical ‘death-grip’ bite. The fungus then kills the ant, sprouts a stalk and releases infective spores. Research has focused on this final manipulation, leaving the subtler behavioural changes prebiting largely unexplored. Field and transcriptome studies found that the host circadian clock, olfaction and communication may be disrupted, which suggests that the fungus is affecting ant foraging activity and effectivity. To test this hypothesis, we investigated if the foraging behaviour of Camponotus floridanus ants is notably affected during early stage Ophiocordyceps infection. Specifically, we used a maze to quantify foraging patterns and trail optimization. Moreover, by comparing infected individuals to healthy ants and those infected with nonmanipulating Beauveria bassiana, we aimed to distinguish between nonmanipulator-specific and manipulator-specific changes. We found that Ophiocordyceps-infected ants became arrhythmic in their activity patterns, were less likely to participate in effective foraging efforts and seemed less able to communicate with their nestmates compared to healthy ants. We hypothesize that these changes in behaviours are adaptive to Ophiocordyceps transmission since they reduce the chance of aggressive interference by nestmates. Indeed, Beauveria-infected individuals remained rhythmic; however, they also seemed to lose their ability to forage optimally, suggesting that, in part, these changes in behaviour might be mere general behavioural side-effects of infection. Overall, this study informs future work on parasitic strategies underlying host manipulation, other parasite–host interactions and the behavioural ecology of infectious diseases in general.