Origanum vulgare terpenoids modulate Myrmica scabrinodis brain biogenic amines and ant behaviour

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.

Multimodal Signaling in Myrmecophilous Butterflies

“…Very recently, it has been shown that this antplant interaction could be maintained through manipulation signals. Mixtures of carvacrol and thymol decrease Myrmica ant movements and increase their aggressive behaviors acting on the brain levels of biogenic amines (Mannino et al, 2018). Therefore, similarly to the scenario described by Hojo et al (2015) (for further details see below), here oregano seems to manipulate Myrmica ants by volatile cues in order to increase partner fidelity and obtain protection against herbivores by patrolling workers.…”

“…Using a multidisciplinary approach, authors shed light on the indirect mechanism used by M. arion females to detect the presence of the Myrmica ants by means of a very tiny variation in the LHP volatilome (Patricelli et al, 2015) and on the way a certain degree of overlap between the two butterfly resources, LHPs and Myrmica ants, can be maintained (Mannino et al, 2018).…”

Formicidal Potential of Thymol Derivatives: Adverse Effects on the Survival and Behavior of Acromyrmex balzani

“…Increasing walking speed could not only increase foraging efficiency but also cause greater energy expenditure by the colony. Mannino et al [55] also found an increase in the walking activity of the ants Formica cinerea, Tetramorium caespitum, and Myrmica scabrinodis, when exposed to thymol and carvacrol, as well as an increase in the levels of dopamine and tyramine in the brain of these ants, which is associated with their locomotion.…”

“…These amines may be related to the different behavior of ants since they have high metabolic diversity and act as neuromodulators and neurotransmitters [52][53][54]. Recent studies already demonstrate, for example, that thymol and its isomer carvacrol interfere with the level of dopamine and tyramine in ant brains, which is associated with their locomotion, as well as their aggressive behavior [55].…”

The Role of Biogenic Amines in Social Insects: With a Special Focus on Ants

“…BAs are nitrogen compounds with one (or more) amine groups originating from the decarboxylation of amino acids. An amazing diversity of BAs has been described, with some compounds acting as toxins, while only a few playing a significant physiological role, which differs between vertebrates and invertebrates [20,23,24].…”