Coping with an antagonist: the impact of a phytopathogenic fungus on the development and behaviour of two species of alpine leaf beetle

Herbivorous insects and phytopathogenic fungi often share their host plants. This creates a network of direct and indirect interactions, with far-reaching consequences for the ecology and evolution of all three parties. In the Alps, the leaf beetles <i>Oreina elongata</i> and <i>Oreina cacaliae</i> (Coleoptera: Chrysomelidae), and the rust fungus <i>Uromyces cacaliae</i> (Uredinales: Pucciniaceae) are found on the same host plant, <i>Adenostyles alliariae</i> (Asterales: Asteraceae). We compare the impact of rust infection on these two closely-related beetle species, one of which, <i>O. cacaliae</i>, is a specialist on <i>A. alliariae</i>, while the other, <i>O. elongata</i>, moves repeatedly between Adenostyles and an alternative host, <i>Cirsium spinosissimum</i>. Larval performance, feeding preference, oviposition choice and dispersal behaviour were studied in field and laboratory experiments. When reared on rust-infected leaves, larvae of both beetle species had lower growth rates, lower maximum weights and longer development times. Larvae and adults discriminated among diets in feeding trials, showing a preference for discs cut from healthy leaves over those bearing a patch of sporulating rust, those from elsewhere on an infected leaf, and those from an upper leaf on an infected plant. Females of the two species differed in behaviour: in <i>O. cacaliae</i> they favoured healthy leaves for larviposition, while in <i>O. elongata</i> they showed no significant preference during oviposition. In the field, larvae and adults of both species dispersed more rapidly when placed on infected host plants. The results demonstrate that rust infection reduces the quality of the plant as a host for both <i>Oreina</i> species, and they combine the ability to detect systemic infection with the evolution of evasive behaviours. For these beetles, competition with a rust clearly increases the difficulty of survival in the harsh conditions of alpine environments, and may have a profound impact on the evolution of their life history traits and host plant use.