Trait‐mediated interactions and lifetime fitness of the invasive plant Centaurea solstitialis

Abstract

Plants interact with numerous enemies and mutualists simultaneously and sequentially. Such multispecies interactions can give rise to trait-mediated indirect effects that are likely to be common in nature but which are also inherently difficult to predict. Understanding multispecies interactions is also important in the use of biological control agents to control invasive plants because modern approaches to biocontrol rely on releasing multiple agents for each target weed. Centaurea solstitialis is one of the most problematic invasive weeds in California, USA, and the weevil Eustenopus villosus is its dominant biological control agent. We conducted a field experiment to quantitatively assess the direct effect of the recently approved biocontrol pathogen Puccinia jaceae f.s. solstitialis on plant performance and any indirect effects that might arise by altering the plant's interactions with Eustenopus or its pollinators (principally the nonnative Apis mellifera). We documented both synergy and interference between the two biocontrol agents depending on the life stage of the weevil. Puccinia infection increased the impact of bud-feeding by the adult weevils but reduced the impact of seed-feeding by larval weevils. Neither infection nor Eustenopus attack had an effect on pollinator visitation. The net effect was that attack by both the pathogen and the weevil did not reduce plant fitness relative to plants attacked only by the weevil. Because the consequence to the plant of interacting with one species may depend on the presence or absence of other interacting species, a careful consideration of multispecies interactions may be necessary for the selection of biocontrol agents that act in a complementary manner to reduce plant fitness. Likewise, relatively tractable weed-biocontrol systems allow us to examine multispecies interactions that can be difficult to study experimentally in native systems that are composed of numerous species with well-established populations.

Strength in numbers? Effects of multiple natural enemy species on plant performance

“…Here, multiple agents are often introduced to reduce populations of a particular weed [12], and agents also must interact with native generalists. Two broad rationales exist for introducing multiple biological control agents [13]: (i) the lottery model predicts that the introduction of more agents will more probably involve a successful agent [12], while (ii) the cumulative stress hypothesis predicts increased plant suppression with more agents, as small amounts of damage by individual species accumulate [14]. If multiple biological control agents are introduced, it would be optimal to introduce agents that will interact synergistically and counterproductive to introduce antagonistic agents.…”

Soil type mediates indirect interactions between Centaurea solstitialis and its biocontrol agents

“…In either case, additive or synergistic interactions among agents is possible and desirable. However, it is also possible for agents to interfere with one another, even when they never interact directly (Denno et al 1995, Swope andParker 2010a). In previous work, we found that infection by the foliar pathogen Puccinia jaceae f.s.…”

“…In previous work, we found that infection by the foliar pathogen Puccinia jaceae f.s. solstitialis, a newly released biocontrol agent, had a direct, negative impact on its host, the invasive plant Centaurea solstitialis, but infection also significantly reduced seed predation by the seed predator Eustenopus villosus, a well-established biocontrol agent (Swope and Parker 2010a). We hypothesized two possible underlying mechanisms.…”

“…Alternatively, C. solstitialis plants may have responded to initial infection with a biochemical defense (systemic acquired resistance; SAR) that was also effective against the seed predator (Karban et al 1987). Ultimately the pathogen's direct negative effect on its invasive host was canceled out by its indirect, positive impact via reduced seed predation (Swope and Parker 2010a). Regardless of whether the net impact of the direct and indirect interactions was super-additive (as in James et al 1992) or sub-additive (as in Swope and Parker 2010a), it is clear that the impact of one species may be influenced, sometimes quite strongly, by the presence or absence of another species.…”

“…In this study, we expand on previous work (Swope and Parker 2010a) to explore how abiotic conditions affect direct and indirect interactions between the recently released biocontrol pathogen Puccinia jaceae f.s. solstitialis and a suite of well-established insect seed predators (also biocontrol agents) via their shared host, Centaurea solstitialis.…”