Classical biological control: exploiting enemy escape to manage plant invasions

Practitioners of classical biological control of invasive weeds are confronted with a dual expectation: to achieve successful control of plant invaders and to avoid damage to nontarget plants and adverse indirect effects. In this paper we discuss key issues that we consider to be crucial for a safe, efficient, and successful classical biological control project, and that have also caused some recent controversy. These include selection of effective control agents, host specificity of the biological control agents, implications of the genetic population structure of the target populations, and potential impact on native food webs. With regard to improving the success rate of biological control of plant invaders, we first emphasize the importance of a clear a priori definition of success and a more ecosystem-based approach to better document both negative effects of the invasive plant as well as potential positive and negative effects of introducing biological control agents. Secondly, pre-release impact assessment could be improved by better focusing on how to reach high densities of the control agents and by including tolerance to and compensation of herbivory. Thirdly, we advocate a reinforced effort to integrate and combine biological control in combination with existing or potential management options. Finally, we propose various ecological and evolutionary hypotheses in the framework of our topic to document that biological control programmes against plant invaders also offer a great opportunity to gain new insights into basic processes in ecology and evolution

Classical biological control: exploiting enemy escape to manage plant invasions

Practitioners of classical biological control of invasive weeds are confronted with a dual expectation: to achieve successful control of plant invaders and to avoid damage to nontarget plants and adverse indirect effects. In this paper we discuss key issues that we consider to be crucial for a safe, efficient, and successful classical biological control project, and that have also caused some recent controversy. These include selection of effective control agents, host specificity of the biological control agents, implications of the genetic population structure of the target populations, and potential impact on native food webs. With regard to improving the success rate of biological control of plant invaders, we first emphasize the importance of a clear a priori definition of success and a more ecosystem-based approach to better document both negative effects of the invasive plant as well as potential positive and negative effects of introducing biological control agents. Secondly, pre-release impact assessment could be improved by better focusing on how to reach high densities of the control agents and by including tolerance to and compensation of herbivory. Thirdly, we advocate a reinforced effort to integrate and combine biological control in combination with existing or potential management options. Finally, we propose various ecological and evolutionary hypotheses in the framework of our topic to document that biological control programmes against plant invaders also offer a great opportunity to gain new insights into basic processes in ecology and evolutio

Plant neighbours rather than soil biota determine impact of an alien plant invader

1. Various factors have been shown contributing to the ecosystem impact of invasive alien plants, but their relative importance remains unclear. We focused on the effects of neighbouring plant community and soil biota as these biotic factors have been repeatedly put forward to explain invasion success (e.g. as components of the novel weapons and of the biotic release hypothesis).2. To assess their relative importance in explaining the high impact of Centaurea stoebe during the invasion of new sites in the introduced range, we conducted a greenhouse experiment with both European (EU) and North American (NA) tetraploid C. stoebe competing with/without EU vs. NA neighbouring community and with the two neighbouring communities growing without C. stoebe. Plants were grown in sterilized commercial soil inoculated with naïve soil (from rhizosphere of plants other than C. stoebe) originating either from the home EU or the introduced NA range and half of which was sterilized to remove soil biota.3. In the competition pots, relative competitive ability (difference between the relative growth rates of C. stoebe and neighbouring community) and impact level (biomass of the neighbouring community relative to that in non-competition pots) of C. stoebe was significantly higher when grown with the NA than with the EU neighbouring community, although growth rates of EU and NA neighbouring communities did not differ in the non-competition pots. Both soil origin and C. stoebe origin had no effect on these processes. Soil sterilization increased growth of both C. stoebe and neighbouring communities, but had only a moderate effect on impact level and type, and no effect on the relative competitive ability of C. stoebe.4. These results suggest that during the colonization of new sites in North American grasslands, the impact of C. stoebe is strongly driven by reduced competitive ability of NA neighbours compared with EU neighbours, while altered biotic soil conditions in the introduced range and post-introduction evolutionary changes in the invader are of less importance. This differential impact appears to be due to inherently different mechanisms underlying the competitive interactions between EU and NA neighbouring communities when grown with C. stoebe

Neighbour origin and ploidy level drive impact of an alien invasive plant species in a competitive environment

Our understanding of the potential mechanisms driving the spread and naturalization of alien plant species has increased over the past decades, but specific knowledge on the factors contributing to their increased impact in the introduced range is still urgently needed. The native European plant Centaurea stoebe occurs as two cytotypes with different life histories (monocarpic diploids, allo-polycarpic tetraploids). However, only tetraploids have been found in its introduced range in North America, where C. stoebe has become a most prominent plant invader. Here, we focus on the ploidy level of C. stoebe and origin of neighbouring community in explaining the high impact during the invasion of new sites in the introduced range. We conducted a mesocosm experiment under open-field conditions with the diploid (EU2x) and tetraploid (EU4x) cytotype of Centaurea stoebe from its native European (EU) range, and with the invasive tetraploid (NA4x) cytotype from the introduced North American (NA) range in competition with EU (old) or NA (new) neighbouring plant communities. In the presence of competition, the biomass of EU neighbouring community was reduced to a comparable level by all three geo-cytotypes of C. stoebe. In contrast, the biomass of the NA neighbouring community was reduced beyond when competing with tetraploid, but not with diploid C. stoebe. The fact that the biomass of all three geo-cytotypes of C. stoebe was correlated with the biomass of the EU neighbouring community, but not with that of the NA neighbouring community suggests that different mechanisms underlie the competitive interactions between C. stoebe and its old vs. new neighbouring communities, such as competition for the same limiting resources at home vs competition through novel allelo-chemicals or differential resource uptake strategies in the introduced range. We therefore caution to simply use the ecosystem impact assessed at home to predict impact in the introduced rang

Aboveground environment type, soil nutrient content and arbuscular mycorrhizal fungi explain establishment success of Centaurea jacea on ex-arable land and in late-successional grasslands

We studied the relative importance of the aboveground and belowground environment for survival and growth of emerged seedlings of Centaurea jacea to better understand the general difficulty of establishing late-successional species at restoration sites on ex-arable land. Potted seedlings growing on soil from six late-successional grasslands and from six ex-arable (restoration) sites were reciprocally exchanged, and survival and relative growth rate of the seedlings monitored. In addition, we assessed aboveground herbivory and colonization of roots by arbuscular myccorhizal fungi of all plants, as well as nutrient availability, and microbial biomass and community composition using PLFA techniques in all twelve soils. Seedling survival was higher in restoration habitat and soil than in grassland habitat and soil, but growth did not differ between the aboveground and belowground environment types. Shoot growth rate was initially correlated with soil nutrient content, and later in the experiment with mycorrhizal colonization levels. Our results indicate that arbuscular mycorhizal fungi may be important for the successful establishment of C. jacea and that abiotic soil factors, like K availability and N:P ratio, can promote mycorrhizal colonization. Hence, the belowground environment should be considered when selecting sites for restoring species-rich grassland

Can plant resistance to specialist herbivores be explained by plant chemistry or resource use strategy?

At both a macro- and micro-evolutionary level, selection of and performance on host plants by specialist herbivores are thought to be governed partially by host plant chemistry. Thus far, there is little evidence to suggest that specialists can detect small structural differences in secondary metabolites of their hosts, or that such differences affect host choice or performance of specialists. We tested whether phytochemical differences between closely related plant species are correlated with specialist host choice. We conducted no-choice feeding trials using 17 plant species of three genera of tribe Senecioneae (Jacobaea, Packera, and Senecio; Asteraceae) and a more distantly related species (Cynoglossum officinale; Boraginaceae) containing pyrrolizidine alkaloids (PAs), and four PA-sequestering specialist herbivores of the genus Longitarsus (Chrysomelidae). We also assessed whether variation in feeding by specialist herbivores is attributable to different resource use strategies of the tested plant species. Plant resource use strategy was quantified by measuring leaf dry matter content, which is related to both plant nutritive value and to plant investment in quantitative defences. We found no evidence that intra-generic differences in PA profiles affect feeding by specialist herbivores. Instead, our results indicate that decisions to begin feeding are related to plant resource use strategy, while decisions to continue feeding are not based on any plant characteristics measured in this study. These findings imply that PA composition does not significantly affect host choice by these specialist herbivores. Leaf dry matter content is somewhat phylogenetically conserved, indicating that plants may have difficulty altering resource use strategy in response to selection pressure by herbivores and other environmental factors on an evolutionary time scal

Origin matters: diversity affects the performance of alien invasive species but not of native species

At local scales, it has often been found that invasibility decreases with increasing resident plant diversity. However, whether resident community diversity similarly resists invasion by alien versus native species is seldom studied. We examined this issue by invading constructed native plant assemblages that varied in species and functional richness with invasive alien or native Asteraceae species. Assemblages were also invaded with spotted knapweed, Centaurea stoebe, a native European aster that has been previously used in diversity-invasibility experiments in North America. We also conducted a field survey to explore the generality of the patterns generated from our experimental study. Both experimental and observational work revealed that increasing diversity reduced the performance of alien but not native invaders. Centaurea stoebe invading its native community performed poorly regardless of resident diversity, whereas in a parallel, previously published study conducted in North America, C. stoebe easily invaded low-diversity but not high-diversity assemblages. Our results suggest that diversity is an attribute of resident communities that makes them more or less susceptible to invasion by novel invasive alien but not native plant species

Origin matters: diversity affects the performance of alien invasive species but not of native species

At local scales, it has often been found that invasibility decreases with increasing resident plant diversity. However, whether resident community diversity similarly resists invasion by alien versus native species is seldom studied. We examined this issue by invading constructed native plant assemblages that varied in species and functional richness with invasive alien or native Asteraceae species. Assemblages were also invaded with spotted knapweed, Centaurea stoebe, a native European aster that has been previously used in diversity-invasibility experiments in North America. We also conducted a field survey to explore the generality of the patterns generated from our experimental study. Both experimental and observational work revealed that increasing diversity reduced the performance of alien but not native invaders. Centaurea stoebe invading its native community performed poorly regardless of resident diversity, whereas in a parallel, previously published study conducted in North America, C. stoebe easily invaded low-diversity but not high-diversity assemblages. Our results suggest that diversity is an attribute of resident communities that makes them more or less susceptible to invasion by novel invasive alien but not native plant species

Biological invasion of oxeye daisy (Leucanthemum vulgare) in North America: Pre-adaptation, post-introduction evolution, or both?

Species may become invasive after introduction to a new range because phenotypic traits pre-adapt them to spread and become dominant. In addition, adaptation to novel selection pressures in the introduced range may further increase their potential to become invasive. The diploid Leucanthemum vulgare and the tetraploid L. ircutianum are native to Eurasia and have been introduced to North America, but only L. vulgare has become invasive. To investigate whether phenotypic differences between the two species in Eurasia could explain the higher abundance of L. vulgare in North America and whether rapid evolution in the introduced range may have contributed to its invasion success, we grew 20 L. vulgare and 21 L. ircutianum populations from Eurasia and 21 L. vulgare populations from North America under standardized conditions and recorded performance and functional traits. In addition, we recorded morphological traits to investigate whether the two closely related species can be clearly distinguished by morphological means and to what extent morphological traits have changed in L. vulgare post-introduction. We found pronounced phenotypic differences between L. vulgare and L. ircutianum from the native range as well as between L. vulgare from the native and introduced ranges. The two species differed significantly in morphology but only moderately in functional or performance traits that could have explained the higher invasion success of L. vulgare in North America. In contrast, leaf morphology was similar between L. vulgare from the native and introduced range, but plants from North America flowered later, were larger and had more and larger flower heads than those from Eurasia. In summary, we found litte evidence that specific traits of L. vulgare may have pre-adapted this species to become more invasive than L. ircutianum, but our results indicate that rapid evolution in the introduced range likely contributed to the invasion success of L. vulgare