The role of predator-prey naïveté for the invasion success of lady beetles – A comparison of species interactions across two continents

According to the predator-prey naïveté hypothesis, a lack of co-evolutionary history between native prey and non-native predators can result in missing predator recognition and an inefficient antipredator response of prey. These mechanisms can also shape non-native predator-predator interactions. Predator-prey and predator-predator naïveté can contribute to the invasion success of non-native predators. To gain a better understanding of the underlying mechanisms of naïveté in insects, we examined the interactions between native and non-native lady beetle species (Coleoptera: Coccinellidae) and pea aphids Acyrthosiphon pisum (Hemiptera: Aphididae) as native prey and ants (Hymenoptera: Formicidae) as native predators. Experiments were conducted in Europe and North America to provide an intercontinental comparison of species-interactions. To test for predator-prey naïveté in the pea aphid, we compared avoidance behavior of aphids towards chemical cues of native and non-native lady beetles. Moreover, we quantified aphid consumption of lady beetles to assess their voracity. Predator-predator naïveté of ants was tested in interaction experiments between ants and native and non-native lady beetle species by assessing and comparing ant aggression and lady beetle reaction. Furthermore, we tested if cuticular chemical cues (cuticular hydrocarbons, CHCs) of lady beetles play a role in ant aggression and analyzed their composition to see if CHCs profiles are species-specific. Overall, we expected a weaker response of native aphids and ants towards non-native lady beetles and their cues compared to native lady beetles. Our findings showed that pea aphids avoid chemical cues of native lady beetles. Moreover, we demonstrated missing cue avoidance behavior of pea aphids towards chemical cues of the non native Asian lady beetle Harmonia axyridis only in Europe, but not in North America. On both continents, H. axyrids and Coccinella septempunctata were the largest lady beetle species and consumed the most aphids. The ant aggression experiments revealed differences in ant aggression as well as lady beetle reaction of native and non-native lady beetles on both continents. In Europe, the CHCs of lady beetle species were species-specific in their composition. Furthermore, we found that cuticular chemical cues of lady beetles contribute to ant aggression. Missing cue avoidance behavior towards chemical cues of non-native H. axyridis indicates prey naïveté in Europe. As H. axyridis was introduced to North America a longer time ago, our findings suggest a rapid adaptation of avoidance behavior by pea aphids towards chemical cues of non-native lady beetles. Moreover, non-native lady beetles may benefit from reduced ant aggression or ant tolerance, which might facilitate the access to ant-tended aphids. Overall, predator-prey and predator-predator naïveté and, thus, associated predation and competition advantages of non-native predators might decrease over time. In contrast, a relatively large body size compared to native predators might benefit non-native predators and contribute to their establishment and invasion success on the long term.