Biocontrol insect impacts population growth of its target plant species but not an incidentally used nontarget

Abstract

Abstract. Understanding the impact of herbivory on plant populations is a fundamental goal of ecology.Damage to individual plants can be visually striking and affect the fates of individuals, but these impacts do not necessarily translate into population-level differences in vital rates (survival, growth, or fecundity) or population growth rates. In biological control of weeds, quantitative assessments of population-level impacts of released agents on both target invasive plants and native, nontarget plants are needed to inform evaluations of the benefits and risks of releasing agents into new regions. Here we present a 3-yr experimental demographic field study using the European root-feeding biocontrol weevil, Mogulones crucifer, first released in Canada in 1997 to control the invasive weed Cynoglossum officinale (Boraginaceae). Mogulones crucifer is an effective "search and destroy" agent in Canada, but sporadically feeds, oviposits, and develops on native nontarget Boraginaceae. We investigated the population-level impacts of this biocontrol insect on its target weed and a native nontarget plant, Hackelia micrantha (Boraginaceae), by releasing large numbers of weevils into naturally occurring patches of H. micrantha growing isolated from or interspersed with C. officinale. We followed the fates of individual plants on release and nonrelease (control) sites for two transition years, developed matrix models to project population growth rates (λ) for each plant species, and examined the contributions from differences in vital rates to changes in λ using life table response experiments (LTRE). In contrast to studies of the insect-plant interaction in its native range, as a biocontrol agent, M. crucifer increased mortality of C. officinale rosettes in the year immediately following release, depressing the weed's λ to below the population replacement level. However, λ for H. micrantha was never depressed below the replacement level, and any differences between release and nonrelease sites in the nontarget could not be explained by significant contributions from vital rates in the LTRE. This study is the first to simultaneously and experimentally examine target and nontarget population-level impacts of a weed biocontrol insect in the field, and supports the theoretical prediction that plant life history characteristics and uneven herbivore host preferences can interact to produce differences in populationlevel impacts between target and nontarget plant species.

Life history variation in an invasive plant is associated with climate and recent colonization of a specialist herbivore

“…Knowing the length of time weevils have infested a site would provide vital insight into how quickly life histories can shift in response to weevil attack, as well as provide insight into factors that might influence the rate of population growth of weevils after establishment. While our evidence builds on previous studies about life history changes observed in the introduced range in response to enemy escape, climate, and biocontrol reintroduction (Williams, 2009;Williams et al, 2010;Catton et al, 2016), we cannot determine the underlying genetic contributions or adaptive functions from our field surveys. Previous work demonstrated both genetic and environmental contributions to observed threshold flowering size (Wesselingh et al, 1997).…”

“…Larvae feed on the roots during development and then emerge to pupate in the soil from mid-June through mid-October in the native range (Schwarzlaender, 1997). Larvae can decimate root tissue, inhibiting houndstongue's ability to conduct water and nutrients (Catton et al, 2016). Because weevils target large individuals that have already converted meristems from vegetative to flowering, they do not affect individual growth, but can significantly reduce seed production (Williams et al, 2010), and the decimation of root tissue likely eliminates the advantage of iteroparity should individuals retain a side rosette (Williams, 2009).…”

“…In Canada, M. crucifer was released in 1997 as biocontrol agent. Since its introduction, houndstongue populations in Canada have almost disappeared (Catton et al, 2016). While M. crucifer is an approved biocontrol in Canada, concerns for other native members of the Boraginaceae family have prevented approval in the United States.…”

Retrospective analysis of a classical biological control programme

“…Prospective approaches have been useful for identifying life stage vulnerabilities, suggesting potential agents to exploit these vulnerabilities, and predicting the impact on pest populations by planned or ongoing biological control programmes (Barker & Addison, 2006;Davis et al, 2006;Maines, Knochel, & Seastedt, 2013;Mills, 2005;Shea & Kelly, 1998). Retrospective analyses can identify the contribution of specific vital rates and enhance our understanding of factors contributing to the success or failure of a programme (Catton, Lalonde, Buckley, & de Clerck-Floate, 2016;Dauer, McEvoy, & van Sickle, 2012;McEvoy & Coombs, 1999). Life table response experiments (LTRE) are a retrospective approach whereby changes in population growth due to an environmental variable can be decomposed into the individual contributions of the underlying vital rates (Caswell, 1996).…”

“…Life table response experiments, and analyses of the associated underlying life tables and matrix models, represent a robust approach for quantifying how changes in factors affecting vital rates ultimately contribute to population growth or decline. The addition of an exotic natural enemy to an ecosystem represents a clear change, the impacts of which should be measurable in terms of altered vital rates and an associated decline in the target pest population(Catton et al, 2016;Dauer et al, 2012;McEvoy & Coombs, 1999). While observations showing correlation between increased apparent parasitism and decline of pest density may support a conclusion of potentially successful biological control (e.g Bellows et al, 1992;De Barro & Coombs, 2009;Pickett, Keaveny, & Rose, 2013;.…”