A cuckoo in wolves' clothing? Chemical mimicry in a specialized cuckoo wasp of the European beewolf (Hymenoptera, Chrysididae and Crabronidae)

Background: Host-parasite interactions are among the most important biotic relationships. Host species should evolve mechanisms to detect their enemies and employ appropriate counterstrategies. Parasites, in turn, should evolve mechanisms to evade detection and thus maximize their success. Females of the European beewolf (Philanthus triangulum, Hymenoptera, Crabronidae) hunt exclusively honeybee workers as food for their progeny. The brood cells containing the paralyzed bees are severely threatened by a highly specialized cuckoo wasp (Hedychrum rutilans, Hymenoptera, Chrysididae). Female cuckoo wasps enter beewolf nests to oviposit on paralyzed bees that are temporarily couched in the nest burrow. The cuckoo wasp larva kills the beewolf larva and feeds on it and the bees. Here, we investigated whether H. rutilans evades detection by its host. Since chemical senses are most important in the dark nest, we hypothesized that the cuckoo wasp might employ chemical camouflage. Results: Field observations suggest that cuckoo wasps are attacked by beewolves in front of their nest, most probably after being recognized visually. In contrast, beewolves seem not to detect signs of the presence of these parasitoids neither when these had visited the nest nor when directly encountered in the dark nest burrow. In a recognition bioassay in observation cages, beewolf females responded significantly less frequently to filter paper discs treated with a cuticular extract from H. rutilans females, than to filter paper discs treated with an extract from another cuckoo wasp species (Chrysis viridula). The behavior to paper discs treated with a cuticular extract from H. rutilans females did not differ significantly from the behavior towards filter paper discs treated with the solvent only. hypothesized that cuckoo wasps either mimic the chemistry of their beewolf host or their host's prey. We tested this hypothesis using GC-MS analyses of the cuticles of male and female beewolves, cuckoo wasps, and honeybee workers. Cuticle extracts of Hedychrum nobile (Hymenoptera: Chrysididae) and Cerceris arenaria (Hymenoptera: Crabronidae) were used as outgroups. There was little congruence with regard to cuticular compounds between H. rutilans females and honeybees as well as females of C. arenaria and H. nobile. However, there was a considerable similarity between beewolf females and H. rutilans females. Beewolf females show a striking dimorphism regarding their cuticular hydrocarbons with one morph having (Z)-9-C25:1 and the other morph having (Z)-9-C27:1 as the major component. H. rutilans females were more similar to the morph having (Z)-9-C27:1 as the main component. Conclusion: We conclude that H. rutilans females closely mimic the composition of cuticular compounds of their host species P. triangulum. The occurrence of isomeric forms of certain compounds on the cuticles of the cuckoo wasps but their absence on beewolf females suggests that cuckoo wasps synthesize the cuticular compounds rather than sequester them from their host. Thus, the behavioral data and the chemical analysis provide evidence that a specialized cuckoo wasp exhibits chemical mimicry of the odor of its host. This probably allows the cuckoo wasp to enter the nest with a reduced risk of being detected by olfaction and without leaving traitorous chemical traces.