Phylogenomics-driven host test list selection for weed biological control

Improving success rates of classical weed biocontrol programs is an ongoing effort that requires a variety of different approaches. Previous assessments indicated biocontrol agent taxonomy and feeding characteristics and weed life history traits are associated with better control outcomes. We examined weed biocontrol releases for correlations between biocontrol agent and target weed traits associated with different levels of reported establishment and control. Data collated in the 5th edition of ‘Biological Control of Weeds: A World Catalogue of Agents and Their Target Weeds’ were used as the basis for this global analysis. Published literature was used to augment the catalog with data for eight biocontrol agent traits and four target weed traits. Biocontrol agent establishment and impact data were analyzed against these traits using generalized linear mixed models and categorical models, respectively. Analyses for biocontrol agent establishment reveal the following agent traits were correlated with a greater probability of establishment: being an internal feeder, feeding on above-ground plant tissues, multivoltine agents and agents that feed during both their adult and immature life stages. Insect taxon did not affect establishment except for the order Lepidoptera, which had the lowest establishment probability. For weed traits, those occurring in aquatic or riparian habitats were associated with a higher probability of biocontrol agent establishment. Regarding agent impact, using the definition categories in the catalog, agents feeding externally and on vegetative plant tissues, multivoltine agents and those with both adult and immature plant-feeding life stages were strongly correlated with greater impact. Perennials, reproducing only vegetatively and invading aquatic or riparian habitats were associated with greater biocontrol impact. Our findings could facilitate both the prioritization of invasive plants targeted for biocontrol and the selection of suitable biocontrol agent candidates, which should further improve biocontrol project outcomes.

Eriophyoids are tiny plant-feeding mites belonging to the families of Eriophyidae, Phytoptidae and Diptilomiopidae. Eriophyoid mites are obligatory phytohages that infest all plant parts, except the roots. Most of them are quite host specific. About 80% of currently known recorded species of eriophyoid mites are associated with a single species of host plant. Classical biological control involves the introduction of control agents into a region, that does not form part of their natural area of distribution, to provide control of invasive weed species. In order to avoid direct damage to non target species, biological control agents must be highly host specific. Classical biological control of weeds depends on finding agents that are highly host-specific. Eriophyoid mites (EM) have long been thought to have high potential as biological control agents of classical biological control of weeds, and many review papers have emphasized their prospects. The use of phylogenies based on the statistical analysis of large numbers of characters, whether molecular genetic or morphological, can help traditional taxonomy and subsequently biological control. Correct systematic identification is a first step to finding prospective agents on the appropriate genotypes of the weed that are targeted for biological control.

ABSTRACTThe invasive weed, parthenium (Parthenium hysterophorus L.) (Asteraceae: tribe Heliantheae), damages agriculture, adversely impacts biodiversity and is hazardous to human and animal health in Ethiopia. The host range of two natural enemies, a leaf-feeding beetle, Zygogramma bicolorata (Coleoptera: Chrysomelidae) and a stem-boring weevil, Listronotus setosipennis (Coleoptera: Curculionidae) was evaluated for biological control of the weed in Ethiopia. The specificity of Z. bicolorata and L. setosipennis was assessed against 29 and 31 non-target plant species, respectively. The host range of Z. bicolorata and L. setosipennis was first assessed using no-choice tests to examine their oviposition and feeding response on non-target plants. Although oviposition by Z. bicolorata occurred on six non-target species in four Asteraceae species in no-choice tests, it was significantly lower than on parthenium and no larvae developed. Zygogramma bicolorata nibbled the leaves of one of the five niger seed (Guizotia abyssinica L. – an oil seed crop closely related to parthenium) cultivars tested, but feeding and oviposition were significantly less than on parthenium. Furthermore, choice tests indicated that Z. bicolorata did not oviposit nor feed on G. abyssinica when parthenium was present. In no-choice tests, L. setosipennis did not oviposit on any of the non-target species assessed. Mean oviposition on parthenium was 39.0 ± 3.4 eggs per plant whereas no eggs were laid on any of the 31 species tested. Based on these and other host range tests, permission was obtained to field release Z. bicolorata and L. setosipennis in Ethiopia.

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.

After a difficult start, classical biological control of weeds is becoming recognized as an option for management of invasive plants in European Union (EU) Member States with intentional releases in three countries over the past 5 years. Many European countries are benefitting from the presence of Stenopelmus rufinasus, the azolla weevil, which has been accidentally introduced to the region. However, the UK experience with the official release of the psyllid Aphalara itadori against Japanese knotweed (Fallopia japonica) and the subsequent release of the rust Puccinia komarovii var glanduliferae against Impatiens glandulifera showed the regulatory framework that could be followed by EU Member States. This process was followed in advance of the subsequent release of Trichilogaster acaciaelongifoliae, a specific Australian bud‐galling wasp, against the invasive Acacia longifolia in Portugal. Soon the case of Ophraella communa, another accidental introduction that is severely limiting Ambrosia artemisiifolia populations, will influence affected countries, some of which have been uninterested in this technique until now, to consider the advantages and disadvantages of classical biocontrol. The future looks bright for classical weed biocontrol and the EU Regulation on Invasive Species should further aid this situation.

It has been only recently that the biological control of weeds by insects was practiced in Korea. Since the diverse crop farming practices in relatively small farms, it has been underestimated by the chemical control practice. The need to find alternative methods from the presence of herbicide‐resistant weeds and growing ecological concern requires immediate action to be followed. The Integrated Weed Management Laboratory at the National Institute of Agricultural Science and Technology at the Rural Development Administration was set up to initiate weed biological control research. Since then, four research projects on weed biological control by insects were carried out. The target weed species were as follows: Rumex obtusifolius, Ambrosia trifida, Acalypha australis, and Monochoria vaginalis. In this review, some of the findings both published and unpublished were presented to show the status of the weed biological control by insects in Korea.

Laboratory tests to estimate the non-target impacts of four Aphidius spp. parasitoids in the field

Eriophyid mites have been considered to have a high potential for use as classical biological control agents of weeds. We reviewed known examples of the use of eriophyid mites to control weedy plants to learn how effective they have been. In the past 13 years, since Rosenthal's 1996 review, 13 species have undergone some degree of pre-release evaluation (Aceria genistae, A. lantanae, Aceria sp. [boneseed leaf buckle mite (BLBM)], A. salsolae, A. sobhiani, A. solstitialis, A. tamaricis, A. thalgi, A. thessalonicae, Cecidophyes rouhollahi, Floracarus perrepae, Leipothrix dipsacivagus and L. knautiae), but only four (A. genistae, Aceria sp. [BLBM], C. rouhollahi and F. perrepae) have been authorized for introduction. Prior to this, three species (Aceria chondrillae, A. malherbae and Aculus hyperici) were introduced and have become established. Although these three species impact the fitness of their host plant, it is not clear how much they have contributed to reduction of the population of the target weed. In some cases, natural enemies, resistant plant genotypes, and adverse abiotic conditions have reduced the ability of eriophyid mites to control target weed populations. Some eriophyid mites that are highly coevolved with their host plant may be poor prospects for biological control because of host plant resistance or tolerance of the plant to the mite. Susceptibility of eriophyids to predators and pathogens may also prevent them from achieving population densities necessary to reduce host plant populations. Short generation time, high intrinsic rate of increase and high mobility by aerial dispersal imply that eriophyids should have rapid rates of evolution. This raises concerns that eriophyids may be more likely to lose efficacy over time due to coevolution with the target weed or that they may be more likely to adapt to nontarget host plants compared to insects, which have a longer generation time and slower population growth rate. Critical areas for future research include life history, foraging and dispersal behavior, mechanisms controlling host plant specificity, and evolutionary stability of eriophyid mites. This knowledge is critical for designing and interpreting laboratory and field experiments to measure host plant specificity and potential impact on target and nontarget plants, which must be known before they can be approved for release. One of the more successful examples of an eriophyid mite controlling an invasive alien weed is Phyllocoptes fructiphilus, whose impact is primarily due to transmission of a virus pathogenic to the target, Rosa multiflora. Neither the mite nor the virus originated from the target weed, which suggests that using "novel enemies" may sometimes be an effective strategy for using eriophyid mites.

Summary1. Biological control agents that impact on non‐target native species have limited desirability.Aculus hypericiwas introduced into Australia to help control the weed St John's wortHypericum perforatum, despite indications from pre‐release trials that this eriophyid mite could survive and reproduce on a non‐target native species,Hypericum gramineum. We used field experiments to explore the probability ofA. hypericicolonizing eitherH. gramineumorH. perforatumin sympatric populations of the alternative hosts, and to determine the impact ofA. hypericion the growth of field‐grownH. gramineum.2. We used a glasshouse experiment to compare the impact ofA. hypericion the ability of each host to recover from water stress and to investigate how such recovery affects herbivore populations on the alternative hosts. As Australia is frequently affected by drought, this issue is critical to both the efficacy and safety of biological weed control.3. The probability ofA. hypericicolonizingH. gramineumwas significantly lower than the probability of it colonizing the target weed. Despite the ability ofA. hypericito infestH. gramineum, the mite had negligible impacts on all measured indices of growth and reproduction.4. During the water limitation experiment, the non‐target host supported populations ofA. hypericithroughout the experimental period, but population size was consistently low. In comparison, mite populations increased considerably on the target weed and were associated with significant decreases in growth. Water limitation compounded the adverse impacts of mites on the weed, but did not affect impacts on the non‐target native.5. Despite the detrimental effects of mites on the growth ofH. perforatum, we found little evidence that they impaired the ability of eitherH. perforatumorH. gramineumto recover from water stress.6. Synthesis and applications.Rigorous host‐specificity testing is necessary to ensure that biological weed control agents do not impact on non‐target species. Potentially, however, these tests may reject beneficial agents unnecessarily, because of low level feeding or reproduction on non‐target species. Although host‐specificity testing might indicate that non‐target native species may host biocontrol agents, our results demonstrate that such non‐target species are not, necessarily, damaged.

Invasive alien species are among the most important threats to biodiversity, with invasive plants ranking among the highest. Classical weed biological control—or biocontrol—reunites exotic plants with host-specific natural enemies from their native range with the aim of controlling the invasive plant. We reviewed the attention classical weed biocontrol has received from scientific publications for the last 30 years, classified according to the area of academia and applied sciences, as well as the region of the world. Biological control journals were excluded from the analyses to avoid bias. This process allowed us to evaluate the support classical weed biocontrol has among the scientific community. We also recorded the number of weed biocontrol agents released from 1900 to date, where they were collected, and where they were released as a way to analyze the evolution of classical weed biocontrol policies in different parts of the world. Classical weed biocontrol releases peaked between 1990 and 1999, but have declined since, probably due to funding issues, increases in regulations, and bad publicity. Researchers in theoretical ecology appear to be more skeptical toward weed biocontrol than scientists in applied and experimental biology. Our synthesis also suggests that despite resistance to classical weed biocontrol in some quarters of the scientific community, the general scientific perception of the discipline has been consistently favorable. This means that the general scientific perception of classical weed biocontrol contradicts its level of current application. The five main objections against classical weed biocontrol—direct nontarget effects, indirect and hidden nontarget effects, evolution of host shifts in biocontrol agents, dispersion to unwanted areas, and disagreements on its level of success in the field—are summarized and analyzed in terms of their relevance and probability of occurrence. We also describe the way classical weed biocontrol practitioners deal with them at present to ensure safety and sustainability. Our analysis suggests the potential of classical weed biocontrol is undervalued in some areas of science and management due to objections that are plausible in theory, although their likelihood is very low and on-ground evidence scant.

ABSTRACTThe biology and host range of the defoliating beetle Physonota maculiventris Boheman (Chrysomelidae: Cassidinae) were studied in quarantine to determine its suitability for release as a biological control agent against Mexican sunflower, Tithonia diversifolia (Hemsl.) A. Gray (Asteraceae), in South Africa. Females laid 5.25 ± 0.25 (mean ± SE) egg batches during their lifetimes, with each batch consisting of approximately 33 eggs. Larvae were highly gregarious as early instars and both larvae and adults fed voraciously, often defoliating the plants completely. The life cycle of the beetle was completed in 67.5 ± 7.5 days under quarantine conditions. Among the 58 test plant species subjected to no-choice tests, P. maculiventris developed successfully on T. diversifolia and some sunflower (Helianthus annuus L.) cultivars. However, only minor damage was recorded on non-target species, notably the exotic weed Xanthium strumarium L. and some H. annuus cultivars. Also, survival to adulthood was considerably lower on sunflower cultivars than on the target weed during these tests. During choice tests, P. maculiventris oviposited and developed successfully on T. diversifolia only, with only minor feeding damage on some H. annuus cultivars, suggesting that the beetle’s field host range will be confined to the target weed. Risk analysis also showed that P. maculiventris presents an extremely low risk to non-target plant species (e.g. within the tribe Heliantheae and other close relatives). The study concluded that P. maculiventris is safe for release in South Africa and an application for its release is being considered by the relevant South African regulatory authorities.

On the face of growing pesticide contamination in the environment, non-target species of insects face serious threats in the ecosystem, ranging from species decline to behavioural changes. Social insects living in colonies are vulnerable to the multimodal effects of pesticide contamination, especially when they are relocating their nests. Nest relocation is a goal-oriented task in eusocial species, which exposes the whole colony to environmental stressors like pesticide contamination. In this context, we investigated the effect of a pyrethroid pesticide, alpha-cypermethrin, on the colony relocation of a non-target ponerine ant, Diacamma indicum. Using field-relevant cypermethrin contamination and simulating natural conditions of nest relocations, we asked if ant colonies would be able to relocate through a contaminated terrain. Furthermore, we tested the effect of prior exposure to pesticide contamination on nest choice during colony relocation using a T-maze set-up. Testing seventy naturally collected D. indicum colonies across five different relocation scenarios, we found cypermethrin impacted behaviour, relocation dynamics and nest choice. Five pesticide-induced behaviours (paralysis, trembling, appendage shaking, staggering and twitching) were identified and quantified. Although the majority of the colonies successfully relocated to the new nest, relocating through a contaminated terrain significantly delayed the process by 2.6 times compared to control colonies. Individual task performance was impaired as only half of the tandem leaders were working in treatment colonies. Interestingly, none of these leaders died, even though an average of 20% of the colony showed either paralysis or mortality a day after exposure. Colonies without prior exposure to pesticides preferred non-contaminated nests over contaminated ones, while colonies living in pesticide-contaminated environment randomly chose either the contaminated or control nest. Our results highlight the disruptive role of pesticide contamination on colony relocation and nest choice in a non-target ant species, and highlight the need to understand the effects of pesticides on aspects of life history other than foraging in both target and non-target species for a comprehensive understanding.

Host Specificity of Microsporidia (Protista: Microspora) from European Populations ofLymantria dispar(Lepidoptera: Lymantriidae) to Indigenous North American Lepidoptera

Host-Range Extension by Native Parasitoids to Weed Biocontrol Agents Introduced to South Africa

The status of weed biological control in the six Greater Mekong Subregion (GMS) countries was assessed, and opportunities to develop biological control in the region are proposed. Twenty biological control agents targeting nine weed species have been introduced into GMS countries, with 13 agents establishing on seven weed species. Another nine biological control agents have spread unintentionally into the region. These agents are having a slight to high impact on their target weeds. However, the number of weeds in the region that have been targeted for biological control is only a fraction of the number of weeds (45) in the region that have been targeted for biological control elsewhere. This presents a tremendous opportunity to expand weed biological control in the region and reduce the dependency on herbicides while increasing productivity. There are numerous highly effective biological control agents present elsewhere that could be introduced to assist with the management of the region's most important weeds, such as Pistia stratiotes , Salvinia molesta , Chromolaena odorata and Mikania micrantha . Along with the introduction of biological control agents, there is also a scope to increase the capacity and training in biological control within GMS countries to develop effective weed control and management.