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.

Dynamics of a mutualism in a multi-species context

“…Apion onopordi larvae develop and pupate in the stem of thistles and adults emerge in late summer. The weevil and the fungus engage in a mutualistic relationship: while female A. onopordi spread the plant pathogen, leading to an increase of systemically rust-infected thistle shoots in the year following weevil infestation, weevils bene t from higher adult body weight, fecundity and survival during winter diapause when developing in rust-infected shoots (Friedli & Bacher 2001a;Bacher et al 2002). This interaction can be classi ed as a by-product-purloined mutualism (Connor 1995); the weevil purloins bene ts by feeding on rust-infected plant tissue and the rust receives by-product bene ts from the weevil promoting systemic infections in healthy thistles in the year following weevil attack.…”

“…While the weevil alone has a limited impact on thistle performance (Friedli & Bacher 2001b), the rust is detrimental to thistle shoots, killing them before owering and reducing the vegetative growth of the root system (Watson & Keogh 1980;Thomas et al 1994). Because the rust seems to depend to a large extent on insect vectors (Friedli & Bacher 2001a), the mutualistic interaction between the weevil and the rust may greatly affect the dynamics of the shared host plant, C. arvense. Vice versa, because both mutualists depend on thistles as hosts, the plant's dynamics will also affect the dynamics of the mutualists.…”

“…The weevil prefers to oviposit into systemically rust-infected over healthy thistle shoots, although both are accepted in the eld (Friedli & Bacher 2001a). During the oviposition period females lay approximately one egg per day, independent of the availability of superior and inferior host plants (Friedli & Bacher 2001b).…”

“…Because it should be easier to locate the preferred host in a population when it is abundant, we hypothesize that the proportion of weevil eggs laid in rustinfected thistle shoots depends on the number and/or relative frequency of rust-infected shoots in the thistle population. There is a trade-off in the bene ts of this mutualism for the weevil: ovipositing in systemically infected shoots has a direct advantage for the weevil's offspring (the F 1 generation), but does not spread the rust, thereby leaving the F 2 generation with suboptimal food (Friedli & Bacher 2001a;Bacher et al 2002). However, ovipositing in healthy C. arvense shoots increases the num-ber of systemically infected shoots in the following season, thereby improving food quality for their offspring's offspring (the F 2 generation), but the female's direct offspring (the F 1 generation) develops in a suboptimal host and suffers tness reductions.…”

“…With the aid of the model, we investigate if the mutualism is regulated by the interaction between the weevil and the rust alone, and how the dynamics of the plant as a resource for both mutualists modulate the system. The biology of the three species is detailed in Friedli & Bacher (2001a).…”