One of the most studied and best-known mutualistic relationships between insects is that between ants and phloem-feeding insects. Ants feed on honeydew excreted by phloem-feeding insects and, in exchange, attack the phloem feeders' natural enemies, including parasitic wasps. However, parasitic wasps are under selection to exploit information on hazards and avoid them. Here, we tested whether parasitic wasps detect the previous presence of ants attending colonies of phloem feeders. Behavioural assays demonstrate that wasps left colonies previously attended by ants more frequently than control colonies. This behaviour has a potential cost for the parasitic wasp as females inserted their ovipositor in fewer hosts per colony. In a further bioassay, wasps spent less time on papers impregnated with extracts of the ant cues than on control papers. Gas chromatography coupled with mass spectrometry analyses demonstrated that ants left a blend of cuticular hydrocarbons when they attended colonies of phloem feeders. These cuticular hydrocarbons are deposited passively when ants search for food. Overall, these results suggest, for the first time, that parasitic wasps of honeydew producers detect the previous presence of mutualistic ants through contact infochemicals. We anticipate such interactions to be widespread and to have implications in numerous ecosystems, as phloem feeders are usually tended by ants.
Generalist predators are increasingly used in biological pest control for greenhouse crops, as they control multiple pests and persist in crops even when prey is scarce. However, some of these predators may cause plant damage due to their omnivorous feeding behaviour. In many European regions, the omnivorous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is considered to be a serious tomato pest, regardless of the biological control services it offers, and integrated pest management (IPM) strategies are based instead on Macrolophus pygmaeus (Rambur). However, as N. tenuis may competitively displace M. pygmaeus and cause severe damage, growers often resort to pesticide use, disrupting their biological control practice. In this study, we evaluated the competitive interactions of three mirid predators, Dicyphus errans Wolff, Dicyphus bolivari Lindberg, and Dicyphus cerastii Wagner, with N. tenuis. The results showed that pre-establishment of heterospecific mirid species can successfully suppress N. tenuis in the greenhouse; population growth was reduced by more than 90% compared to plants without competing predators. Further laboratory trials revealed reciprocal intraguild predation between these species in the absence of extraguild prey. Dicyphus adults predated on N. tenuis nymphs, while this was not found for M. pygmaeus. In olfactometer bioassays, N. tenuis females preferred plants previously exposed to heterospecifics but not conspecifics, suggesting that this mirid does not avoid competition. These results suggest that the three Dicyphus species could be interesting candidates for preventive releases in tomato crops due to their ability to effectively suppress N. tenuis population growth.
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