Variable effects of a generalist parasitoid on a biocontrol seed predator and its target weed

Authors: Swope, Sarah; SATTERTHWAITE, WILLIAM - University Of California

Submitted to: Ecological Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/5/2011
Publication Date: 1/15/2012
Citation: Swope, S.M., Satterthwaite, W.H. 2012. Variable effects of a generalist parasitoid on a biocontrol seed predator and its target weed. Ecological Applications. 22(1):20-34.

Interpretive Summary: The goal of any biological control program is to reduce the target weed’s population size and/or growth rate; to do this the agent must establish its own populations that persist over the long-term, thereby providing continuous control. Potentially complicating this relationship are native predators and parasitoids that may attack the agents. The important role of native enemies is largely unstudied so we set out to estimate the degree to which a biocontrol agent’s impact on the target weed is affected by enemy attack over many decades. To do this we relied on detailed data from a multi-year, multi-site field study of the invasive plant yellow starthistle (Centaurea solstitialis) and its principal biocontrol agent the hairy weevil (Eustenopus villosus) which is attacked by a native, generalist parasitoid (Pyemotes tritici). Our field data came from two different sites in California with very different climates: coastal Marin County and the hot, dry Central Valley, allowing us to evaluate how these interactions might change in response to the local climate. We constructed a simulation model with the field data to project the outcome of the interaction between these three species and found that: (1) in coastal areas, the agent was capable of modestly reducing the plant’s abundance and population growth rate but only when it was free of the parasitoid; (2) when the parasitoid was included in the model, the agent’s populations in coastal areas were small, in decline and had no impact on the plant; (3) in the Central Valley, the agent reduced plant abundance (and population growth rate) so much in the absence of the parasitoid that it was essentially eating itself out of its proverbial house and home and its own populations were quickly declining; and (4) when the parasitoid was included in the model, the agent’s populations in the Central Valley were actually larger and growing rapidly and although the plant population was also larger, it was still smaller than it would have been if it were unattacked by the agent. In summary, in coastal areas, attack by the parasitoid rendered a modestly effective agent ineffective; in the Central Valley, the agent was successful in dramatically reducing the weed’s population size (the first goal of biocontrol) while the parasitoid actually bolstered the agent’s populations (the second goal of biocontrol) by preventing the agent from over-exploiting the plant on which it depends.

Technical Abstract: Biological control – the importation of enemies from an invasive species’ native range – is often seen as our best hope of reducing the abundance of the most widespread invaders. Classic predator-prey models provide the theoretical underpinning for the practice of biological control. Ideally, the predator (agent) drives its prey (invasive species) to acceptably low levels and then the two coexist at low density over long-time spans, and in this way the agent provides continuous control. But this model is not likely to work well when the invader is a plant and the biocontrol agent an insect because, unlike the predator in predator-prey models, the insect may itself be subject to predation by native, generalist species. We used a discrete time coupled plant-seed predator-parasitoid model to project the fate of both the invasive weed Centaurea solstitialis and the biocontrol agent (seed predator) Eustenopus villosus over several decades in the presence and absence of the generalist parasitoid Pyemotes tritici. As in reality, our model allows feedback from the plant to the seed predator and vice versa. We used detailed demography data from two sites in a long-term field study to parameterize the model and to compare how spatial variation may influence the outcome. We found that at both of our sites, parasitism of the seed predator caused a trophic cascade, i.e., plant populations benefited when the agent was parasitized. But the degree to which the agent’s impact was alleviated varied among sites. At the coastal site where both plant and seed predator population performance were lower, the parasitoid entirely eliminated the impact of the agent on the plant by all measures and caused agent populations to become so unstable that 15% went extinct more than a decade after successful establishment. At the Central Valley site where plant and seed predator performance were higher, even the parasitized agent significantly reduced plant population size over several decades, but not population growth rate ('>1.0). Interestingly, at this site, the parasitoid also had the counter-intuitive effect of bolstering the seed predator’s populations (larger population size and '>1.0) because parasitism prevented the seed predator from overexploiting the plant on which it depends. Our model results suggest that predators play an important role in stabilizing (or destabilizing) agent populations with downstream effects on the target weed and that to some extent this is determined by how well-matched the agent is to the local climate in the absence of top-down regulation. We recommend that even an incomplete understanding of the local food web coupled with estimates of how agent performance will vary among climatic zones will improve our ability to selectively release agents only into areas where they are most likely to be successful.