Abstract
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.
Highlights
The social organization of ants is based on communication signals which coordinate large numbers of individuals in collective-decision processes, without a centralised control [1]
Research on ants is still in its infancy, yet some supporting evidence was provided for colonies of the Red Imported Fire Ant, Solenopsis invicta, with a change in the nest-mate recognition determined by a decrease in the brain level of octopamine [23], and in Pheidole ants, where the depletion in the serotonin content modulates the trail-following behaviour of workers [24]
Our results show that dopamine levels, which are known to be directly correlated to the complexity of behavioral repertoire [53,54], and the tyramine content rise as the locomotor ability increases
Summary
The social organization of ants is based on communication signals which coordinate large numbers of individuals in collective-decision processes, without a centralised control [1]. Plant modulates ant behaviour through aminergic regulation most suitable place where to build a new nest [5,6] as well as decisions to attack either enemies or competitors [7,8]. This peculiar trait of eusocial organisms, together with the ability to regulate the number of individuals performing specific tasks (division of labour), enhances the colony plasticity to react promptly against biotic and abiotic variations [9,10]. Plant chemical signalling can manipulate and influence the decision-making of ants [11,12,13]. Research on ants is still in its infancy, yet some supporting evidence was provided for colonies of the Red Imported Fire Ant, Solenopsis invicta, with a change in the nest-mate recognition determined by a decrease in the brain level of octopamine [23], and in Pheidole ants, where the depletion in the serotonin content modulates the trail-following behaviour of workers [24]
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
