Abstract

Summary Plant–pathogen–insect interactions may have various outcomes that are of great interest when considering the combined use of insects and pathogens in the biological control of weeds. Here effects of rust infection on herbivore attack and of herbivory on rust infection were analysed to ensure that these possible control agents do not impede each other. The system studied was the weed creeping thistle Cirsium arvense, the specialized rust fungus Puccinia punctiformis, and ectophagous and endophagous insect herbivores. On 20 sites around Göttingen, Germany, the abundance of ectophagous and endophagous insects on systemically rust‐infected and uninfected plants was quantified by suction samples and the dissection of shoots. Abundance of ectophagous insects was not reduced by rust infection, and aphids as well as several beetle species were more abundant on systemically infected plants. Preference of endophagous insects differed between species: larvae of Apion weevils were more abundant in infected shoots, whereas Melanagromyza aeneoventris, Urophora cardui, all of them oligophagous, and some leaf miners preferred uninfected plants. In dual‐choice feeding tests, larvae of the oligophagous chrysomelid beetle Cassida rubiginosa were more likely to feed on leaf segments of uninfected thistles. Enhancement of rust infection rate by simulated herbivory was analysed. Thistle leaves were perforated and infection rate was recorded after 2 weeks under natural Puccinia punctiformis spore concentrations. Numbers of uredosori were significantly higher in perforated leaves. Artificial inoculation resulted in an even greater increase in uredosori, both in perforated and unperforated thistles. As the majority of ectophagous and endophagous insects did not discriminate between systemically infected and uninfected thistles, herbivore damage together with infection with Puccinia punctiformis can be expected to increase stress on creeping thistle when used in biological control of the weed. Insects may not only affect plant growth by herbivory but may also increase the susceptibility of healthy thistles to local rust infection by wounding of leaves.

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