Coordinated social behaviour is fundamental for ant ecological success. However, even distantly-
related organisms, such as plants, have evolved the ability to manipulate ant collective
performances to their own advantage. In the parasitic system encompassing Maculinea
butterflies, Myrmica ants, and Origanum vulgare plants, the ant-plant interaction elicits the
release of a volatile terpenoid compound (carvacrol) which is used by the gravid butterfly to
locate the ideal oviposition site. Here we show that this ant-plant association is maintained
by the effect of O. vulgare terpenoids on ant behaviour and that food plants might gain protection
by Myrmica ants by chemically manipulating workers to forage in their surroundings.
The variation in the locomotor ability of three ant species (Formica cinerea, Tetramorium
caespitum, and Myrmica scabrinodis) was studied after treatment with the two major O. vulgare
terpenoid volatile compounds (i.e., carvacrol and thymol). The brain levels of three biogenic
amines (dopamine, tyramine and serotonin) were analysed in ants exposed to the O.
vulgare terpenoids by HPLC-ESI-MS/MS. Carvacrol and thymol increased the locomotor
activity of all ant species tested, but if blended reduced the movement propensity of Myrmica
scabrinodis. Dopamine and tyramine production was positively correlated with the worker
locomotor activity. In Myrmica ants, both brain biogenic ammines were negatively correlated
with the aggressive behaviour. Blends of O. vulgare volatiles affected the locomotor ability
while increased the aggressiveness of Myrmica workers by altering the aminergic regulation
in the ant brains. This behavioural manipulation, might enhance partner fidelity and plant
protection. Our findings provide new insights supporting a direct role of plant volatiles in driving
behavioural changes in social insects through biogenic amine modulation.
