On the adaptive meaning of chemically insignificant cues in multitrophic caterpillar-ant-plant symbioses

Abstract

Ants use cuticular hydrocarbons (CHCs) as chemical cues for recognition, which are exploited by myrmecophiles to usufruct the benefits of the social habit. We aimed to identify the functional role of CHCs of two riodinid caterpillar species that obligately associate with different multitrophic ant-plant symbioses. Experiments of ant acceptance of caterpillars showed the concerted action of larval-ant-organs that produce liquid rewards (tentacle nectary organs, TNOs) and luring signals (anterior tentacle organs, ATOs) was key to ant appeasement and larval survival. Experiments changing the symbiosis were often lethal for the caterpillars, mainly after emptying the secretions of their TNOs and their ATOs were never activated. Chemical profiles of caterpillars were insignificant. Field bioassays with chemically insignificant palatable insect prey attracted fewer ants, indicating that insignificant cues may reduce the probability of ant attacks. Thus, caterpillars control the emission of signals of ant-organs during symbiosis, whereas the cues of CHCs are silenced. It is possible that a trade-off exists between signals under control and non-controlled cues. Chemical insignificance may allow for a crucial period for caterpillars to make tactical decisions to appease aggressive ants and could be extended to other communication channels according to the sensorial universe of the receiver.