Hariet L. Hinz

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.

Comparing Invasive Plants from Their Native and Exotic Range: What Can We Learn for Biological Control?1

Abstract This article reviews and summarizes data sets that attempt to compare performance, population dynamics, and herbivory of invasive plant species. Specifically, we review results from studies comparing (1) individual and population parameters of plant invaders in their native and exotic range, (2) herbivore pressure and natural enemy guilds associated with plant invaders in their native and exotic range, and (3) performance and defense levels of native and exotic populations of the invasive under standardized conditions and the performance of selected herbivores. We found a total of 39 published and 2 unpublished studies, investigating 40 plant species. The majority of studies within the first category showed that invaders form larger populations, grow denser, have higher reproductive output, larger seed banks, and higher regeneration rates in the exotic compared with the native range. In contrast, plant vigor was not always greater, presumably because of increased intraspecific competition. Nearly all studies within the second category showed that herbivory (percentage of attack, species number and load) was reduced and, if investigated, that the herbivore community shifted from specialists to generalists and from endophagous to exophagous species in the exotic compared with the native range. Under standardized conditions (category 3), an equal number of studies found increased vigor or no significant differences between plants from the exotic and native range. In a few cases, plants from the exotic range grew less vigorous. Specialist herbivores generally preferred or developed better on plants from exotic compared with native populations, which were also better defended. Studies comparing plant invaders at field sites in their native and exotic range or under standardized conditions can help identify factors facilitating successful invasions, which in turn can improve the selection and efficiency of biological control agents and the development of integrated management strategies. We therefore suggest to include comparative studies more frequently in biological control programs and to extend them to include manipulative experiments and comparisons of control agents. Additional index words: Biological weed control, comparative studies, enemy release hypothesis, evolution of increased competitive ability hypothesis. Abbreviations: EICA, evolution of increased competitive ability; ERH, enemy release hypothesis.

Successes We May Not Have Had: A Retrospective Analysis of Selected Weed Biological Control Agents in the United States

Abstract In this paper, we describe five successful classical biological weed control agents released in the United States. For each of the five arthropod species, we compared data from prerelease studies that experimentally predicted the agents host range with data collected postrelease. In general, experimental host range data accurately predicted or overestimated risks to nontarget plants. We compare the five cases with insects recently denied for introduction in the United States and conclude that none of the discussed agents would likely be approved if they were petitioned today. Three agents would be rejected because they potentially could attack economic plants, and two because of potential attack on threatened or endangered plants. All five biocontrol agents have contributed significantly to the successful management of major weeds with no or minimal environmental risk. We believe that the United States may miss opportunities for sustainable and environmentally benign management of weeds using biological control if the regulatory framework only considers the risks of agents as potential plant pests and treats any host-range data regarding economic or threatened and endangered species as a binary decision (i.e., mandates rejection if there is any chance of feeding or development). As a way forward we propose the following: (1) the addition of risk and benefit analyses at the habitat level with a clear ranking of decision-making criteria as part of the U.S. Department of Agriculture Animal and Plant Health Inspection Service Technical Advisory Groups evaluation process of biocontrol agents; (2) recognition of the primacy of realized host range data for potential agents that considers the insects host selection behavior instead of emphasizing fundamental host range data during release evaluations, and (3) development of formalized postrelease monitoring of target and nontarget species as part of the release permit. These recommendations may initially be advanced through reassessment of current policies but may in the longer term require the implementation of dedicated biocontrol legislation.

Comparative survey of the phytophagous arthropod faunas associated with Lepidium draba in Europe and the western United States, and the potential for biological weed control.

Abstract Hoary cress (Lepidium draba L.) is an invasive perennial mustard (Brassicaceae) introduced to North America from Eurasia. In 2001 we initiated a program to investigate the potential for classical biological control of this weed in the US. Literature and field surveys for the arthropods associated with L. draba were conducted on both continents. Field surveys began in Europe in 2001, and in 2002–2003 standardized surveys were conducted in both Europe and the western US. These field surveys resulted in 80 new host records for L. draba in Europe, and 37 new host records in the US. Although total species richness was nearly four times greater in Europe, there were approximately equal proportions of oligophagous and polyphagous species in each range. Monophagous species were only encountered in the European surveys. The literature surveys revealed that the arthropod fauna associated with L. draba is fairly well known in Europe (175 species), but not in the US (eight species), where the literature was virtually derelict of host records. In both the literature and field surveys, the order Coleoptera contained the most species (>50%) in Europe, whereas the order Hemiptera contained the most species (>40%) in the US. Nearly one-half of the species found in literature and field surveys are flower or seed feeders and the other half are primarily foliage or stem feeders. Ten potential biological control agents were discovered from the surveys, of which four are currently being investigated at the CABI Bioscience Centre in Switzerland. The phenologies of these four species are briefly described.

Interaction of specialist root and shoot herbivores of Alliaria petiolata and their impact on plant performance and reproduction

Abstract 1. This study explored interactions of two spatially and temporally separated weevils and their impact on Alliaria petiolata (garlic mustard) survival, growth, and reproduction at different herbivore densities.

Avoiding conflicts between insect and weed biological control: selection of non-target species to assess host specificity of cabbage seedpod weevil parasitoids

Abstract:  Classical biological control of insect pests and weeds may lead to potential conflicts, where insect pests are closely related to weed biological control agents. Such a conflict may occur in the classical biological control of the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) in North America, which belongs to the same subfamily, Ceutorhynchinae, as a number of agents introduced or proposed for introduction against non‐indigenous invasive weed species. We propose a step‐by‐step procedure to select non‐target species and thereby to develop a non‐target species test list for screening candidate entomophagous biological control agents of a herbivore pest insect in a way that would simultaneously evaluate non‐target potential on weed biological control agents and other non‐target species. Using these recommendations, we developed a non‐target test list for host specificity evaluations in the area of origin (Europe) and the area of introduction (North America) for cabbage seedpod weevil parasitoids. Scientifically based predictions on expected host–parasitoid interactions and ecological information about the ecological host range in the area of origin can help avoid conflicts, while still allowing the introduction of safe and effective agents against both insect pests and weeds.

Colletotrichum sp: A potential candidate for biocontrol of scentless chamomile (Matricaria perforata) in western Canada

Abstract Based on an assessment of 706 fungal isolates obtained from Canada and Europe, a group of Colletotrichum sp. isolates, tentatively identified as C. truncatum, was moderately efficacious for biocontrol of scentless chamomile (Matricaria perforata). In this study, 19 C. truncatum isolates, 11 from Canada and eight from Europe, were compared for virulence, crop safety, and minimum dew requirement for infection to narrow the selection of candidates. Applied at 1×106 spores mL−1, these isolates expressed variable virulence under controlled environments, with slightly higher variations observed on the Canadian isolates. There was also a slight difference in host specificity among the isolates tested; most isolates caused disease only on chamomile species (M. perforata and M. recutita) but two Canadian isolates also infected lentil, flax, or both. At 20°C, most isolates required more than 20 h dew for maximum infection. This requirement can be an impediment for using this fungus as a biocontrol agent in western Canada where the climate is semi-arid. Treatment of scentless chamomile at the 10-leaf stage with the herbicide metribuzin 48 h prior to fungal inoculation increased weed control to 72%, compared to 40 and 47% by the herbicide and fungus applied alone. However, a similar treatment using the herbicide bentazon did not enhance the weed control significantly as compared to the herbicide alone.

Effects of pasture competition and specialist herbivory on the performance of Cirsium arvense

Abstract Combining specialist herbivory with interspecific plant competition can be an effective means of controlling pasture weeds. Cirsium arvense (Canada thistle, Californian thistle, creeping thistle) is one of the worst weeds of pastoral production systems in New Zealand (NZ). The oligophagous leaf-feeding beetle, Cassida rubiginosa, was recently released in NZ for control of C. arvense. To assess the impact of this biocontrol agent we conducted an outdoor potted-plant experiment with low and high densities of Cassida larvae combined with different levels of interspecific competition from typical NZ pasture species. Secondly, we carried out a field-release experiment to quantify the impact of high densities of Cassida under more natural conditions. Interspecific competition reduced all measured plant parameters of C. arvense except mean shoot height and base diameter. Herbivory by Cassida only reduced root biomass, and showed a weak additive response when combined with competition. All other measured parameters of C. arvense showed a substitutive response, with competition being the only factor having a significant impact on the weed. There were no significant synergistic interactions with competition and herbivory on C. arvense. Interestingly, the number of root buds per plant was significantly greater in the presence of herbivory by Cassida, suggesting that C. arvense may compensate for defoliation. Similar to the potted-plant experiment, Cassida had no significant effect on shoot growth and development in the field-release experiment. The results of this study indicate that competition from typical NZ pasture species is a more important factor than herbivory by Cassida, and unless Cassida reaches outbreak densities, it will likely have an insignificant impact on this weed.

The impacts of some classical biological control successes.

We differentiate between the success of a classical biological control programme and its impact; the former addressing the completed implementation of the steps of a biological control programme, and the anticipated reduction of the target pest, and the latter addressing the societal and environmental benefits of control of the target pest. We provide ten case studies in which CABI has played a role to illustrate aspects of success and impact for biological control programmes against insects pests and weeds: cassava mealybug (Phenacoccus manihoti), mango mealybug (Rastrococcus invadens), pink hibiscus mealybug (Maconellicoccus hirsutus), orthezia bug (Insignorthezia insignis), brown peach aphid (Pterochloroides persicae), banana skipper (Erionota torus), black sage (Varronia curassavica), rubber vine (Cryptostegia grandiflora), leafy spurge (Euphorbia esula) and water hyacinth (Eichhornia crassipes). In light of these we discuss the assessment of success and impact of biological control programmes, why these aspects are often not adequately addressed, how they might be retroactively addressed and the implications for donor-funding of biological control programmes for developing countries.

Effect of generalist insect herbivores on introduced Lepidium draba (Brassicaceae): implications for the enemy release hypothesis

The enemy release hypothesis (ERH) states that decreased regulation by natural enemies allows plants to increase in distribution, abundance and vigour following their introduction into an exotic range. Invasive plants rarely escape herbivory entirely, and for hoary cress [Lepidium draba L. (Brassicaceae)] it has been demonstrated that generalist insect abundance is greater in its introduced North American range than in the native European range. We assessed the role of increased generalist herbivory on hoary cress using representatives of four important herbivore niches commonly found in the introduced range. We experimentally examined the density dependent impact of these herbivores individually and in combination on hoary cress in a series of greenhouse experiments. We found that defoliation of the oligophagous diamondback moth Plutella xylostella (L.) (Lep., Plutellidae) had the strongest and most consistent impact, while damage by the stem‐mining weevil Ceutorhynchus americanus Buchanan (Col., Curculionidae) tended to have the highest per capita effect. Plant response to feeding by the oligophagous crucifer flea beetle Phyllotreta cruciferae (Goeze) (Col., Chrysomelidae) was minor despite obvious feeding damage, and the impact of the polyphagous tarnished plant bug Lygus hesperus Knight (Het., Miridae) was negligible. In multiple‐species experiments, herbivore impacts were usually additive. In general, we found that hoary cress can tolerate high densities of oligophagous insect herbivory and effectively resisted attack by the polyphagous L. hesperus, but also the oligophagous C. americanus. Our results indicate that a combination of plant resistance and tolerance allows hoary cress to withstand increased generalist herbivore load in its introduced range, consistent with the predictions of the ERH.