Mutualistic interaction between a weevil and a rust fungus, two parasites of the weed Cirsium arvense

Abstract

We present a mutualism between a stem-boring weevil, Apion onopordi Kirby (Coleoptera: Apionidae), and a rust fungus, Puccinia punctiformis (Str.) Röhl. (Uredinales), both parasites of the creeping thistle, Cirsium arvense (L.) Scop. (Asteraceae). Females, but not males, of A. onopordi induced systemic rust infections of thistle shoots in the season after they were attacked by the weevil, indicating that insect oviposition is a crucial stage in pathogen transmission. Adult weevils emerged from systemically infected thistle shoots were heavier than weevils from healthy C. arvense shoots. Heavier females had a higher fecundity and laid larger eggs. The weevil preferred to deposit eggs in systemically rust-infected over healthy thistle shoots, which seemed to be a sub-optimal host. This is to our knowledge the first report of a mutualistic interaction between an herbivorous insect and a biotrophic plant pathogen. The mechanism responsible for the advantage of rust-infected shoots for A. onopordi causes a different outcome in other thistle herbivores, and therefore can not be explained by a general enhancement of nutritional quality in rust-infected tissue. This mutualism likely has evolved from a competitive relationship. Unlike other thistle herbivores A. onopordi seems to be better suited as mutualist for P. punctiformis because of its small impact on the host plant and its feeding niche on plant parts not directly associated with pathogen reproduction.