Biological Control of Wheat Pests: A Meta-Analysis

Quadrastichus erythrinae Kim is a serious gall inducing invasive pest in recent years. Female lays eggs in the tissue of young leaves and shoots of coral trees (Erythrina spp.). After larvae hatched from eggs, they develop in host tissue, causing swelling and curling of the infested parts. Severe infestations will influence host health and even cause the death of hosts. The invasion of Q. erythrinae devastated coral trees in many places of Taiwan, including some elder trees. Up to date, the main method to against Q. erythrinae relies on chemical control. However, insecticide resistance may be induced when applying chemical control for a long time. Therefore, developing biological control may provide a better strategy for a long term concern and applying native enemies will cause less environmental impact compare to introduced ones. According to previous investigation, there are several parasitoid wasps use Q. erythrinae as a host. One of them is Eupelmus sp. (Eupelmidae) which distributes widely in Taiwan. However, little knowledge of its biology has been established. The life cycle of Eupelmus sp. was studied in this research to help estimate its potential as a biological control agent. Besides, the occurrences of other parasitoids were acquired through the investigation of Q. erythrinae in Taiwan for adding other choices in biological control. Two other species of wasps on Q. erythrinae were found in Taiwan through dissecting wild galls and rearing the parasitoid wasps. One belongs to Megastigmus sp. (Torymidae), and the other is Aprostocetus sp. (Eulophidae). Lab experiments showed that Eupelmus sp. will lay eggs when provided Q. erythrinae galls at 17 to 20 developmental days. It takes about 21 days for a euplemid wasp to develop from egg to adult in 25℃. Male biased was found in both lab rearing and wild Eupelmus sp. When offering different foods, adult longevity of males is longest in both treatments of 10% honey and honeydew of coral trees. Morphological characteristic measurement showed that females collected from wild is bigger than females emerged from Q. erythrinae galls. It suggests that the female collected in wild may not developed on Q. erythrinae. For mass rearing and control application, it is crucial to find out original hosts of Eupelmus sp. in Taiwan as the information is useful for developing effective rearing techniques and increase the control potential. Analysis of monitoring data shows that the occurrence time between Aprostocetus sp. and Eupelmus sp. did not overlap to each other and, therefore, a biological control strategy using both parasitoids may provide a compensatory effect to increase the control efficiency. Although the parasitoid wasps of Q. erythrinae so far found in Taiwan are less host specific, they have stably occurred on the population of Q. erythrinae. It suggests that there is a potential for applying parasitoid wasps as agents of biological control against Q. erythrinae in Taiwan.

Opinions about the value of biological control are often extreme. Colloquially, biological control most often refers to classical biological control, in which one species is introduced from another region to control pests such as arthropod herbivores in agricultural systems, or weeds in managed and natural systems.1 As such, biological control has the potential to be a low-cost, chemical free, means to control pests. Numerous biological control programs have been unqualified successes (Bellows 2001), such as the control of cacti in Australia with the moth Cactoblastis cactorum (Raghu and Walton 2007), of cottony-cushion scale (Icerya purchasi) in California with the vedalia lady beetle, Rodolia cardinalis (Caltagirone and Doutt 1989), and of glassy-winged sharpshooters in French Polynesia with the egg parasitoid Gonatocerus ashmeadi (Grandgirard et al. 2009). Yet, classical biological control, as with any introduction of a species into a new area, necessarily involves the unknown and therefore carries some inherent risk (Simberloff and Stiling 1996) – what will these organisms actually do in a novel ecosystem? The most unpredictable element in biological control is the extent to which the realized niche is modified in the new environment. This effect has been responsible for some disastrous outcomes of classical biological control, many of which occurred during an era when vertebrates were being introduced around the world by Europeans for a variety of reasons (e.g., introducing the birds of Shakespeare to America, Mirsky 2008), including for biological control (Howarth 1991). The introductions as biological control agents of cane toad to Australia (Crossland et al. 2000) and mongoose to Hawaii (Hays and Conant 2007) are notorious. Introductions of generalist invertebrate agents also have had dire consequences, such as the introduction of predatory snails to French Polynesia (Murray et al. 1988; Coote 2007). In retrospect, some of the unintended consequences of biological control could have been avoided with more ecological knowledge (McEvoy and Coombs 2000) or more societal appreciation for native species (which has developed with time, Henneman and Memmott 2001), but with other introductions, it would have been impossible to know ahead of time what the risks would be (e.g., gall fly agents of knapweeds providing supplementary food to mice that harbor hantavirus, Pearson and Callaway 2006). Many of the unknown outcomes of biological control are purely ecological – what is the risk that a wasp, introduced to parasitize an agricultural pest, will also be able to feed on a native insect? Other unknowns involve evolution – will a herbivore adapt over time to be able to feed on a new nontarget host or hybridize with a closely related species? This volume explores the evolutionary aspects of biological control. Although often overlooked, evolutionary considerations are critical to all stages of classical biological control, from agent selection, to quarantine, release, establishment, and ultimately success in pest control (Ehler et al. 2004). Many questions are unresolved. For example, should agents be chosen that have a long history with the host or are ‘new associations’ more likely to succeed (Hokkanen and Pimentel 1989)? Can one improve effectiveness through artificial selection (Hopper et al. 1993)? Will postcolonization adaptation of the agent increase the likelihood of success, and/or are hosts equally likely to evolve resistance over time (Roderick 1992; Holt and Hochberg 1997; Hufbauer 2001)? Are generalist consumers more likely to survive in novel environments or are specialists more effective (Murdoch et al. 1985; Waage 1990; Brodeur 2012)? More recently, concern for the environment, as well as theory examining the reasons for success of generalist predators, prompted a shift to the release of specialized consumers typically preceded by extensive testing aimed at delimiting the host range of candidate biological control agents. While this approach has clearly made biological control more predictive ecologically, research focused on host range currently lacks measures of genetic variation in host use and responses of those hosts, and thus evolutionary uncertainties remain.

Biological control of exotic invasive plants using exotic insects is practiced under the assumption that biological control agents are safe if they do not directly attack non-target species. We tested this assumption by evaluating the potential for two host-specific biological control agents (Urophora spp.), widely established in North America for spotted knapweed (Centaurea maculosa) control, to indirectly elevate Sin Nombre hantavirus by providing food subsidies to populations of deer mice (Peromyscus maniculatus), the primary reservoir for the virus. We show that seropositive deer mice (mice testing positive for hantavirus) were over three times more abundant in the presence of the biocontrol food subsidy. Elevating densities of seropositive mice may increase risk of hantavirus infection in humans and significantly alter hantavirus ecology. Host specificity alone does not ensure safe biological control. To minimize indirect risks to non-target species, biological control agents must suppress pest populations enough to reduce their own numbers.

Laterally acquired chitinase genes in venom facilitate parasitism in egg parasitoid wasps.

The invasive eucalyptus tortoise beetle, Paropsis charybdis, defoliates plantations of Eucalyptus nitens in New Zealand. Recent efforts to identify host specific biological control agents (parasitoids) from Tasmania, Australia, have focused on the larval parasitoid wasp, Eadya paropsidis (Braconidae), first described in 1978. In Tasmania, Eadya has been reared from Paropsisterna agricola (genus abbreviated Pst.), a smaller paropsine that feeds as a larva on juvenile rather than adult foliage of Eucalyptus nitens. To determine which of the many paropsine beetle hosts native to Tasmania are utilized by E. paropsidis, and to rule out the presence of cryptic species, a molecular phylogenetic approach was combined with host data from rearing experiments from multiple locations across six years. Sampling included 188 wasps and 94 beetles for molecular data alone. Two mitochondrial genes (COI and Cytb) and one nuclear gene (28S) were analyzed to assess the species limits in the parasitoid wasps. The mitochondrial genes were congruent in delimiting four separate phylogenetic species, all supported by morphological examinations of Eadya specimens collected throughout Tasmania. Eadya paropsidis was true to the type description, and was almost exclusively associated with P. tasmanica. A new cryptic species similar to E. paropsidis, Eadya sp. 3, was readily reared from Pst. agricola and P. charybdis from all sites and all years. Eadya sp. 3 represents the best candidate for biological control of P. charybdis and was determined as the species undergoing host range testing in New Zealand for its potential as a biological control agent. Another new species, Eadya sp. 1, was morphologically distinctive and attacked multiple hosts. The most common host was Pst. variicollis, but was also reared from Pst. nobilitata and Pst. selmani. Eadya sp. 1 may have potential for control against Pst. variicollis, a new incursion in New Zealand, and possibly Pst. selmani in Ireland. Our molecular data suggests that Pst. variicollis is in need of taxonomic revision and the geographic source of the beetle in New Zealand may not be Tasmania. Eadya sp. 2 was rarely collected and attacked P. aegrota elliotti and P. charybdis. Most species of Eadya present in Tasmania are not host specific to one beetle species alone, but demonstrate some host plasticity across the genera Paropsisterna and Paropsis. This study is an excellent example of collaborative phylogenetic and biological control research prior to the release of prospective biological control agents, and has important implications for the Eucalyptus industry worldwide.

The widespread use of insecticides in forest ecosystems has raised significant concerns about their nontarget effects on biological control agents (BCAs), such as predators and parasitoid wasps, which play a pivotal role in natural pest suppression. This review evaluates the lethal and sublethal impacts of various insecticide classes on BCAs. Systemic insecticides, while effective in controlling pests, have been shown to impair the reproduction, foraging behavior, and host-seeking abilities of BCAs, leading to disruptions in pest regulation and biodiversity loss. In Pinus koraiensis (Siebold & Zucc) forests, parasitoid wasps such as Baryscapus dioryctriae (Yang & Song) are critical for managing pests such as Dioryctria pryeri. However, insecticide exposure threatens their efficacy, exacerbating pest outbreaks and ecosystem instability. The deployment of B. dioryctriae as a BCA provides a sustainable alternative to chemical control, with demonstrated success in reducing pest populations and minimizing environmental impacts. Integrated pest management (IPM) frameworks that combine biological control with targeted insecticide use offer promising solutions to mitigate nontarget effects. Future research should focus on optimizing mass-rearing and release strategies for BCAs, exploring semiochemical-based pest disruption and assessing the long-term ecological consequences of low-dose insecticide exposure. By advancing IPM approaches, forest managers can achieve effective pest control while preserving the ecological integrity and biodiversity of forest ecosystems.

This paper reviews prospective biological control agents of the varroa mite, Varroa destructor n. sp. (Acari, Mesostigmata). This ectoparasite has caused severe damage to populations of the European honeybee, Apis mellifera , world-wide in recent years. To date, no promising natural enemies of varroa species have been identified on A. mellifera or its original host, Apis cerana . Therefore, biological control will probably require natural enemies from other hosts. The following groups of organisms were reviewed as potential biological control agents: predatory mites, parasitoids and entomopathogens (nematodes, protozoa, viruses, Bacillus thuringiensis , rickettsiae, and fungi). The candidate groups were ranked according to their lethality to Acari, likely ability to operate under the physical conditions of honeybee colonies, ease of targeting, and ease of mass-production. Preferential consideration was given to the natural enemies of Acari that occupy taxonomic groups close to varroa. Entomopathogenic fungi, which kill a wide range of acarine species, were identified as prime candidates for screening against varroa. Bacillus thuringiensi s also requires study, particularly strains producing novel toxins active against non-insect hosts. Entomopathogenic protozoa and nematodes show less potential for varroa control, but nonetheless warrant preliminary investigation. We consider predators, parasitoids, viruses and rickettsiae to have little potential to control varroa. Because the physical conditions within honeybee colonies are similar everywhere, it is very likely that a biological control agent of varroa could be used successfully throughout the world.

The soil is often considered the milieu providing support for plant roots, water and nutrients for plant growth. But it is also considered a hostile environment harbouring plant pathogenic nematodes, bacteria and fungi. The most common attitude is to try to eliminate the plant pathogenic organisms by biocidal treatments such as methyl bromide fumigation, which are dangerous for man and the environment. Beside this pathogen eradication strategy, another approach to control soil-borne plant diseases consists in studying the plant-pathogen interactions at the cellular and molecular level to create new resistant cultivars or to develop new plant protection products based on elicitation of plant defence reactions. This field of research only focuses on plant pathogen interactions, not taking into account the environment in which they take place. Although a plant disease results from the intimate interaction between a plant and a pathogen, the importance of these direct interactions should not hide the role of environmental factors which influence disease severity. These indirect interactions are particularly important in the case of diseases induced by soil borne pathogens. Indeed, the pathogens are not freely interacting with the plant; they are included in the soil matrix and thus can not escape to the soil environment. Both their inoculum density and infectious capacities are controlled by the soil. Evidence of these interactions is given by the existence of soils that suppress diseases. In suppressive soils disease incidence or severity remains low in spite of the presence of the pathogen, a susceptible host plant and climatic conditions favourable for disease development. These suppressive soils provide examples of biotic and abiotic factors affecting the pathogen, the plant or the interaction between plant and pathogen. In other words, suppressive soils provide examples where biological control, similar to conservation biological control, is active in nature. Therefore many studies have been devoted to the understanding of soil suppressiveness in order to use suppressive mechanisms in biological control strategies. Since in many cases, antagonistic micro-organisms play a role in soil suppressiveness, the soil has been seen as a reservoir of potential biological control agents. For the two or three last decades the main approach was to identify effective antagonists in soil and try developing them as biological control agents. Most of the biological control agents on the market, even when aerial diseases are targeted, have been isolated from soil. But in order to control soil-borne diseases, one must admit that this strategy has not been as successful as expected. Indeed, even if the soil harbours effective antagonists, soil suppressiveness is due to an association of mechanisms and micro-

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.

The use of entomopathogenic fungi represents one of the most important non-chemical alternatives for pest control in crop production. In addition to their pathogenicity to arthropods, they have many other important effects that favor their use in biological control. They live in plants as endophytes and have an inhibitory effect on plant pathogens. They inhabit the rhizosphere of many plants in natural and agricultural ecosystems and have a stimulatory effect on their growth and development. These recently acquired ecological functions are not yet fully understood, but point to the broader potential of using entomopathogenic endophytic fungi in crop production, not only as biopesticides but also as mycofungicides and growth stimulants (biostimulants). To achieve the full potential of entomopathogenic endophytic fungi in daily agricultural practice, practical application should be considered in the development of commercial products and the application techniques of entomopathogenic endophytic fungi that allow successful colonization of plants should be considered.

The use of microorganisms for biological pest control as biological control agents (BCAs) and biopesticides was developed worldwide in the 1960s. Despite the abundance of reviews published on this topic, no meta-analysis using bibliometric tools has been published. The objective of this study was to determine patterns of research on microorganisms for the biological control of pests, based on publications available in the SCOPUS® database. The data were obtained from the Elsevier® Scopus meta-database using the search terms “biological pest control” and “microorganism” (title, abstract, and keywords). The main publications were identified, along with the journals, countries, and institutions that have published on the subject. The data were analyzed with VOSviewer to determine the co-occurrence of terms, and four maps were generated. The results show two phases in the scientific research on the subject: The first is the characterization of biological control agents, and the second is focused on the commercial development of biopesticides and biological control agents. The most recent research emphasizes the discovery of new species and strains that have commercial potential, with an emphasis on genetic engineering and biotechnology.

The biological control of wireworm (Agriotes spp.) in potato crops has not yet caught up to conventional controls at a time in which deregistration of pesticides is increasing, leaving a paucity of options for growers. Some measure of control has been achieved with use of entomopathogenic fungi (EPF), and to a lesser extent, entomopathogenic nematodes (EPN), with varying success. Factors affecting efficacy range from instability of pathogens within a soil matrix to difficulty in accurately targeting a subterranean pest in a heterogeneous population. The overall aim of this project was to identify areas for improvement for biological control strategies for wireworm, through identification of bioactive compounds and exploring synergies between these and existing entomopathogens. Using historical research to identify botanical extracts for bioactivity against invertebrate pests, tea tree (Melaleuca alternifolia) and rosemary (Salvia rosemarinus) oils were found to elicit repellent properties in wireworm, positively associated with mortality. Cedarwood (Cedrus atlantica) oil produced the opposite effect, an attractant response with no adverse effects on larval health. The second aspect of the project posited a novel behavioural assay methodology, demonstrating wireworm plant preferences and complex behavioural responses to introduced botanical semiochemicals beyond that of a simple attraction or repulsion. Identified botanicals were then evaluated for compatibility with strains of Metarhizium brunneum, with each of the three exhibiting fungicidal and fungistatic effects on the EPF, but at lower concentrations improving mortality and rate of pathogenicity. Finally, wireworm behavioural responses to EPF inoculations were exploited with two fungal volatile organic compounds (VOC), 1-octen-3-ol and 3-Octanone, found to have direct bioactivity towards wireworm and marginal synergistic effects with a known biological control in the entomopathogenic nematode, Heterorhabiditis bacteriophora. The project has clearly demonstrated methods for improvement for existing biological controls and given strong evidence for use of botanicals as crop protectant compounds in an integration pest management system for potato crops.

Nursery production is significantly affected by diseases and pest infestations, which diminish plant health, marketability, and overall yield. This study examines common nursery diseases, such as powdery mildew, botrytis blight, leaf spot, rust, and root rot, as well as prominent pests like aphids, whiteflies, thrips, and mealybugs. These biological threats lead to severe economic losses, making effective management strategies essential. The analysis emphasizes the role of Integrated Pest Management (IPM) as a sustainable and comprehensive approach. By combining cultural, biological, and chemical control methods, IPM effectively reduces pest populations while minimizing environmental impact. The use of biological control agents, such as predatory insects and beneficial microbes, is presented as an eco-friendly alternative to synthetic pesticides. Nursery crops are particularly vulnerable to leaf spot, damping-off, and anthracnose, which significantly compromise plant quality. Additionally, pests like the red palm weevil, rhinoceros beetle, and tea mosquito bug cause substantial damage to coconut, areca nut, and other plantation crops, all of which are vital to the region's economy. Managing these pests effectively requires region-specific strategies, including the use of botanical extracts, pheromone traps, and soil solarization. Emerging technologies, such as drone-based pesticide application, AI-powered pest detection, and genetic engineering for disease-resistant plants, have been identified as potential solutions for enhancing nursery productivity. These innovations offer precision and efficiency, reducing chemical usage while improving plant health. Effective disease and pest management in nurseries necessitates a multifaceted approach that integrates traditional techniques with modern innovations. The adoption of IPM strategies and cutting-edge technologies can significantly enhance plant protection, leading to increased productivity and sustainability in the nursery industry.

The zoophytophagous predator Dicyphus hesperus Knight (Hemiptera: Miridae) is effective in the biological control of whiteflies in greenhouses, but it can also cause damage to fruits and plants. Artificial selection on foraging behavior allows the development of more zoophagous lines that have the potential to be both more effective and less likely to cause damage. Moreover, highly zoophagous lines could affect other biological control agents through increased intraguild predation or competition. This study tests the biological control efficacy against tobacco whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and damage by highly and lowly zoophagous lines of D. hesperus in tomato greenhouses. The effect of these lines on Encarsia formosa Gahan (Hymenoptera: Aphelinidae) parasitoid wasp populations was also tested. In cage tests, we introduced D. hesperus from lowly or highly zoophagous and non‐selected lines. In half of the cage, E. formosa was introduced. The ability of predators and parasitoids to reduce B. tabaci populations was monitored for 12 weeks. Tomatoes produced were harvested and graded according to damage by D. hesperus. Highly zoophagous lines had a rapid and lasting impact on pest populations. Lowly zoophagous lines take longer to achieve the same level of pest control as highly zoophagous lines. Introductions of E. formosa also reduce populations, but without interacting with D. hesperus. Dicyphus hesperus did not affect E. formosa abundance. Lowly zoophagous lines generated higher proportions of damage. The results show that artificial selection based on zoophagy produces more efficient and less damaging lines in the greenhouse tomato crop. Over time, lines with low zoophagy compensated for low individual efficiency by increasing their numbers. Highly zoophagous lines are compatible with parasitoid wasps, which were little affected by D. hesperus.

We explored the relationships between synthetic fertilizer use, yield, and ecosystem services in a coffee agroecosystem in the Tarrazú region in the central highlands of Costa Rica. Working in nine farms ranging from 0.3 to 2.7 ha in the CoopeTarrazú farmers' cooperative, we focused on two important indicators of ecosystem services: biological control agents and mycorrhizal fungi. Biological control agents (especially parasitoid wasps) are essential for population regulation of herbivorous arthropods that reside in coffee agroecosystems. Mycorrhizal fungi contribute to plant nutrition and disease resistance and produce a highly stable protein, glomalin, which is critical for soil aggregation. Soil aggregates hedge against erosion, particularly in sloping soils, by improving porosity. Slopes in this study ranged from 4% to 66%. We manipulated synthetic fertilizer levels in experimental plots ranging from 6.9% increase to 53.3% decrease in total N relative to control plots that received a standard amount of fertilizer. The effects on coffee yields, soil glomalin production by mycorrhizal fungi, and wasp diversity were examined. Yield and glomalin decreased, but parasitoid diversity increased with greater reductions in fertilizer application six months after application. Reducing fertilizer use may bolster biological control assemblages, while glomalin is more directly dependent on plant production.