Non-destructive environmental safety assessment of threatened and endangered plants in weed biological control.

Assessing the risk of nontarget attack (NTA) for federally listed threatened and endangered (T&E) plant species confamilial to invasive plants targeted for classical biological control, is one of the most important objectives of pre-release environmental safety assessments in the United States. However, evaluating potential NTA on T&E species is often complicated by restrictive agency requirements for obtaining propagules, or the ability to propagate plants and rear agents to the appropriate phenostages synchronously for testing, or both. Here, we assessed whether plant cues associated with a host recognition can be used for testing the attractiveness of four T&E and one rare single population plant species non-destructively for a candidate biocontrol agent. We used the seed-feeding weevil, Mogulones borraginis, a candidate for the biological control of the invasive plant, Cynoglossum officinale (Boraginaceae) as the study system. We collected olfactory and visual cues in the form of flowering sprigs from T&E plant species confamilial to the invasive plant in a non-destructive manner and used them to measure behavioral responses and searching time of weevils. Female weevils preferred C. officinale to all tested plant species in dual-choice bioassays using either olfactory or visual cues in a modified y-tube device. Furthermore, female weevils were repelled by the combined olfactory and visual cues from all tested T&E plant species in a dual-choice test against controls (e.g., purified air in an empty arm), indicating that it would be extremely unlikely for the weevil to attack any of these species upon release in the United States. Principal component analysis based on 61 volatile organic compounds effectively separated the five confamilial plant species and C. officinale, corroborating the results of behavioral bioassays. We conclude that studies on pre-alighting host selection behavior and the underlying physiological mechanisms of how organisms select host plants they exploit can aid in environmental safety testing of weed biological control agents.

Field Assessment of the Host Range of Aculus mosoniensis (Acari: Eriophyidae), a Biological Control Agent of the Tree of Heaven (Ailanthus altissima).

Tree of heaven (Ailanthus altissima) is a fast-growing deciduous tree native to China, considered a serious invasive species worldwide, with several socio-economic and ecological impacts attributed to it. Chemical and mechanical methods have limited efficacy in its management, and biological controls may offer a suitable and sustainable option. Aculus mosoniensis (Ripka) is an eriophyid mite that has been recorded to attack tree of heaven in 13 European countries. This study aims to explore the host range of this mite by exposing 13 plant species, selected either for their phylogenetic and ecological similarity to the target weed or their economic importance. Shortly after inoculation with the mite, we recorded a quick decrease in mite number on all nontarget species and no sign of mite reproduction. Whereas, after just one month, the population of mites on tree of heaven numbered in the thousands, irrespective of the starting population, and included both adults and juveniles. Significantly, we observed evidence of damage due to the mite only on target plants. Due to the specificity, strong impact on the target, and the ability to increase its population to high levels in a relatively short amount of time, we find A. mosoniensis to be a very promising candidate for the biological control of tree of heaven.

Host Range and Impact of Dichrorampha aeratana, the First Potential Biological Control Agent for Leucanthemum vulgare in North America and Australia.

We evaluated the potential of the European root-feeding moth Dichrorampha aeratana as a biological control agent for the invasive weed Leucanthemum vulgare (oxeye daisy) in North America and Australia. The taxonomic proximity of the ornamental Shasta daisy (Leucanthemum × superbum) to L. vulgare and its popularity in North America made finding sufficiently host-specific biological control agents a challenge. No-choice tests conducted with 74 non-target species revealed partial or complete larval development on 11 species. In multiple-choice oviposition and larval development tests that were conducted in field cages, larvae were found on five of these, however in multiple-choice tests conducted under open-field conditions, larvae were only found on the ornamentals Shasta daisy and creeping daisy (Mauranthemum paludosum). Larval feeding by D. aeratana had no measurable impact on Shasta daisy, but larval feeding and plant competition reduced the biomass and number of flower heads of L. vulgare. We conclude that D. aeratana is a suitable biological control agent because it will not affect the ornamental value of Shasta or creeping daisies and because it is unlikely to feed on any other economically important or native species. We also expect D. aeratana to contribute to the suppression of L. vulgare populations.

A global review of target impact and direct nontarget effects of classical weed biological control.

Recent reviews show that classical weed biocontrol measures can be successful in reducing the negative impacts of invasive plant species, have impressive returns on investment, and contribute to slower rates of weed spread. Quantitative post-release monitoring is necessary to account for differences in biocontrol outcomes across spatial and temporal scales. Direct nontarget attack (NTA) incidence and severity are decreasing over time, and pre-release host-specificity tests can accurately predict NTA post-release, as long as the nontarget plant species are included in testing. Less than 1% of NTA was found where the impacted plant species had been tested pre-release and was deemed not at risk. Effectiveness and environmental safety will likely further improve with the incorporation of new technologies, such as experimental evolutionary studies.

Feeding intensity of insect herbivores is associated more closely with key metabolite profiles than phylogenetic relatedness of their potential hosts.

Determinants of the host ranges of insect herbivores are important from an evolutionary perspective and also have implications for applications such as biological control. Although insect herbivore host ranges typically are phylogenetically constrained, herbivore preference and performance ultimately are determined by plant traits, including plant secondary metabolites. Where such traits are phylogenetically labile, insect hervivore host ranges are expected to be phylogenetically disjunct, reflecting phenotypic similarities rather than genetic relatedness among potential hosts. We tested this hypothesis in the laboratory with a Brassicaceae-specialized weevil, Ceutorhynchus cardariae Korotyaev (Coleoptera: Curculionidae), on 13 test plant species differing in their suitability as hosts for the weevil. We compared the associations between feeding by C. cardariae and either phenotypic similarity (secondary chemistry-glucosinolate profile) or genetic similarity (sequence of the chloroplast gene ndhF) using two methods-simple correlations or strengths of association between feeding by each species, and dendrograms based on either glucosinolates or ndhF sequence (i.e., a phylogram). For comparison, we performed a similar test with the oligophagous Plutella xylostella (L.) (Lepidoptera: Plutellidae) using the same plant species. We found using either method that phenotypic similarity was more strongly associated with feeding intensity by C. cardariae than genetic similarity. In contrast, neither genetic nor phenotypic similarity was significantly associated with feeding intensity on the test species by P. xylostella. The result indicates that phenotypic traits can be more reliable indicators of the feeding preference of a specialist than phylogenetic relatedness of its potential hosts. This has implications for the evolution and maintenance of host ranges and host specialization in phytophagous insects. It also has implications for identifying plant species at risk of nontarget attack by potential weed biological control agents and hence the approach to prerelease testing.

Corrigendum: Geographic population structure in an outcrossing plant invasion after centuries of cultivation and recent founding events.

[This corrects the article DOI: 10.1093/aobpla/ply020.][This corrects the article DOI: 10.1093/aobpla/ply020.].

Geographic population structure in an outcrossing plant invasion after centuries of cultivation and recent founding events.

Population structure and genetic diversity of invasions are the result of evolutionary processes such as natural selection, drift and founding events. Some invasions are also molded by specific human activities such as selection for cultivars and intentional introduction of desired phenotypes, which can lead to low genetic diversity in the resulting invasion. We investigated the population structure, diversity and origins of a species with both accidental and intentional introduction histories, as well as long-term selection as a cultivar. Dyer's woad (Isatis tinctoria; Brassicaceae) has been used as a dye source for at least eight centuries in Eurasia, was introduced to eastern USA in the 1600s, and is now considered invasive in the western USA. Our analyses of amplified fragment length polymorphisms (AFLPs) from 645 plants from the USA and Eurasia did not find significantly lower gene diversity (Hj) in the invaded compared to the native range. This suggests that even though the species was under cultivation for many centuries, human selection of plants may not have had a strong influence on diversity in the invasion. We did find significantly lower genetic differentiation (Fst) in the invasive range but our results still suggested that there are two distinct invasions in the western USA. Our data suggest that these invasions most likely originated from Switzerland, Ukraine and Germany, which correlates with initial biological control agent survey findings. Genetic information on population structure, diversity and origins assists in efforts to control invasive species, and continued combination of ecological and molecular analyses will help bring us closer to sustainable management of plant invasions.

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.

Two shoot-miners, Ceutorhynchus alliariae and Ceutorhynchus roberti, sharing the same fundamental niche on garlic mustard.

A combination of observational and experimental methods, in both the laboratory and field, were used to assess niche partitioning between Ceutorhynchus alliariae Brisout and C. roberti Gyllenhal (Coleoptera: Curculionidae), two coexisting shoot-boring weevils on garlic mustard, Alliaria petiolata (M. Bieb.) Cavara and Grande (Brassicaceae). We compared their morphology, oviposition behavior, larval development, distribution, abundance, and attack rates in their sympatric range, and of C. alliariae when found alone and in sympatry with C. roberti. Results indicate only very small differences in the fundamental niches of the two species. Comparison of C. alliariae in the range it occurs alone with the range where it co-occurs with C. roberti revealed some evidence for competition between the two species, i.e., attack levels of C. alliariae were reduced in areas where it co-occurred with C. roberti. However, the study showed no character displacement in regard to adult size or shoot choice of C. alliariae and we found no indication for superiority of either of the two species. Clearly, manipulative experiments would be necessary to unambiguously test for competition between the two species. Our results, based on a subset of niche dimensions known to be important in other systems, suggest that C. alliariae and C. roberti may present one of the rare cases, in which niche differentiation is not the main mechanism underlying coexistence.

Demographic models inform selection of biocontrol agents for garlic mustard (Alliaria petiolata).

Nonindigenous invasive plants pose a major threat to natural communities worldwide. Biological control of weeds via selected introduction of their natural enemies can affect control over large spatial areas but also risk nontarget effects. To maximize effectiveness while minimizing risk, weed biocontrol programs should introduce the minimum number of host-specific natural enemies necessary to control an invasive nonindigenous plant. We used elasticity analysis of a matrix model to help inform biocontrol agent selection for garlic mustard (Alliaria petiolata (M. Bieb.) Cavara and Grande). The Eurasian biennial A. petiolata is considered one of the most problematic invaders of temperate forests in North America. Four weevil species in the genus Ceutorhynchus (Coleoptera: Curculionidae) are currently considered potential biocontrol agents. These species attack rosettes (C. scrobicollis), stems (C. roberti, C. alliariae), and seeds (C. constrictus) of A. petiolata. Elasticity analyses using A. petiolata demographic parameters from North America indicated that changes in the rosette-to-flowering-plant transition and changes in fecundity consistently had the greatest impact on population growth rate. These results suggest that attack by the rosette-feeder C. scrobicollis, which reduces overwintering survival, and seed or stem feeders that reduce seed output should be particularly effective. Model outcomes differed greatly as A. petiolata demographic parameters were varied within ranges observed in North America, indicating that successful control of A. petiolata populations may occur under some, but not all, conditions. Using these a priori analyses we predict: (1) rosette mortality and reduction of seed output will be the most important factors determining A. petiolata demography; (2) the root-crown feeder C. scrobicollis will have the most significant impact on A. petiolata demography; (3) releases of single control agents are unlikely to control A. petiolata across its full range of demographic variability; (4) combinations of agents that simultaneously reduce rosette survival and seed production will be required to suppress the most vigorous A. petiolata populations. These predictions can be tested using established long-term monitoring sites coupled with a designed release program. If demographic models can successfully predict biocontrol agent impact on invasive plant populations, a continued dialogue and collaboration between empirical and theoretical approaches may be the key to the development of successful biocontrol tactics for plant invaders in the future.