The ‘cuckoo strategy’ in ant-lepidoptera association: a facultative parasitism for survival benefits

Many ants enjoy symbiotic relationships with lycaenid caterpillars, deriving food rewards through the myrmecophilous organs (MO) of the larva. However, whether ants associate with caterpillars lacking these beneficial organs is unclear. An example of such a relationship exists between the Asian weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae), and the myrmecoxenous caterpillar of Parotis marginata (Lepidoptera: Crambidae). A total of 340 silk woven Oecophylla leaf nests of various sizes were sampled from various locations across West Bengal, India; of these, 187 lepidopteran caterpillars and 211 pupae were detected in 80 leaf-nests (~ 24% occurrence) (with/without queen). In some instances, the caterpillars and pupae were encountered inside the ant nests, wrapped in fine silks, and coexisting with the workers. It instigates why ants allow the caterpillar/pupae inside their nest as foreigners. Therefore, the aim of the study was to investigate why such a symbiotic relationship occurs where one (caterpillar) offers no apparent food rewards, and the host (ant) allows the intruder to their nest and provides protection.The presence of MO in caterpillar was examined using SEM, while the composition and characteristics of the pupal silk were analysed using SEM-XRD. Additionally, the cuticular hydrocarbon (CHC) profiles of both species were analysed and compared using GC-MS at their different growth stages (ant: brood stage I, II, adult worker; and lepidoptera: larval stage I, II, pupa). There was no MO in the caterpillar, and its pupal silk showed notable contrasts to the ant. The CHC profiles also varied remarkably between them [ Oecophylla : adult (n = 36), brood stage I (n = 12), and brood stage II (n = 22); Parotis: larval stage I (n = 12), larval stage II (n = 15), pupa (n = 0)]. So, the lepidopteran larvae and ant broods exhibited significant similarities in CHCs at their juvenile stages.Although the Parotis caterpillar does not have any explicit incentive to benefit ants, it does exhibit mimicking of CHCs to deceive ant broods. The ‘cuckoo-like’ behaviour is intended to safeguard the caterpillars from the highly aggressive weaver ants, particularly during the early larval stage, by developing chemical mimicry. Our results corroborate the facultative parasitism of Parotis caterpillar within Oecophylla nest.