Parasitism of arbuscular mycorrhizal fungi: reviewing the evidence.

In order to understand the functioning of mycorrhizal fungi in ecosystems it is necessary to consider the full suite of possible biotic interactions in the soil. While a number of such interactions have recently been shown to be crucially important, parasitism is a highly neglected feature in the ecology of arbuscular mycorrhizal fungi (AMF). A number of studies have classified some interactions between populations of bacteria and fungi with AMF as parasitism, generating discussion about its consequences at both 'parasite' and host population levels. This paper reviews these various publications, and based on a set of criteria that are necessary to demonstrate parasitism, it was concluded that parasitism has not been conclusively shown to exist in AMF, even though some data are highly suggestive of such a relationship. The difficulties in gathering data supportive of parasitism were discussed, and hypotheses for defense were offered. This paper concludes by presenting potential consequences of AMF parasitism at the population/community levels and by discussing applied aspects.     

The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease

Botrytis cinerea is a necrotrophic fungal pathogen causing disease in many plant species, leading to economically important crop losses. So far, fungicides have been widely used to control this pathogen. However, in addition to their detrimental effects on the environment and potential risks for human health, increasing fungicide resistance has been observed in the B. cinerea population. Biological control, that is the application of microbial organisms to reduce disease, has gained importance as an alternative or complementary approach to fungicides. In this respect, the genus Trichoderma constitutes a promising pool of organisms with potential for B. cinerea control. In the first part of this article, we review the specific mechanisms involved in the direct interaction between the two fungi, including mycoparasitism, the production of antimicrobial compounds and enzymes (collectively called antagonism), and competition for nutrients and space. In addition, biocontrol has also been observed when Trichoderma is physically separated from the pathogen, thus implying an indirect systemic plant defence response. Therefore, in the second part, we describe the consecutive steps leading to induced systemic resistance (ISR), starting with the initial Trichoderma–plant interaction and followed by the activation of downstream signal transduction pathways and, ultimately, the defence response resulting in ISR (ISR‐prime phase). Finally, we discuss the ISR‐boost phase, representing the effect of ISR priming by Trichoderma spp. on plant responses after additional challenge with B. cinerea.     

Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens

Many strains of Pseudomonas fluorescens show potential for biological control of phytopathogens especially root pathogens. In taxonomic terms, several of them are indeed P. fluorescens sensu stricto , while others belong in fact to neighbouring species of the ' P. fluorescens ' complex or to ill-defined related species within the fluorescent Pseudomonas spp. These bacteria have become prominent models for rhizosphere ecological studies and analysis of bacterial secondary metabolism, and in recent years knowledge on their plant-beneficial traits has been considerably enhanced by widening the focus beyond the case of phytopathogen-directed antagonism. Current genomic analyses of rhizosphere competence and biocontrol traits will likely lead to the development of novel tools for effective management of indigenous and inoculated P. fluorescens biocontrol agents and a better exploitation of their plant-beneficial properties for sustainable agriculture.     

Characterisation of endophytic Bacillus thuringiensis strains isolated from wheat plants as biocontrol agents against wheat flag smut

To explore effective and ecofriendly means of controlling wheat flag smut (WFS) using biocontrol agents, three endophytic strains (58-2-1, 37-1 and YC-1) of Bacillus sp. were isolated from winter wheat plants in China and identified as Bacillus thuringiensis based on their 16S rDNA sequences as well as phenotypic characteristics. Four morphological (leaf length, root length, dry weight and tiller numbers) and one physiological [root vigour (RV)] parameters of wheat plants treated by strains 58-2-1 and 37-1 were significantly enhanced compared to the control. The soluble sugar contents in the roots of wheat samples treated by the two strains were significantly lower than the control. The resistance of wheat varieties to WFS was investigated by inoculation tests. Of the 12 wheat varieties tested, 6 (Yunhan-618, Bainongaikang-58, Kaimai-20, Zhengmai-9023, 04-zhong-36 and Yanzhan-4110) were identified as WFS-highly resistant (HR), 3 (Pumai-9, Jinboshi-1 and Yunong-202) WFS-moderately resistant (MR), 1 (Yubao-1) WFS-susceptible (S) and 2 (Yumai-012 and Yunong-416) WFS-highly susceptible (HS) varieties. The Urocystis tritici-induced yield loss on the S/HS varieties was significantly higher than that on the HR/MR ones. The strains 58-2-1 and 37-1 had control efficacies of 6.7–100% (av.54.8%) and 33.3–100% (av. 66.5%) on 9 and 7 out of 12 varieties, respectively. The strains 58-2-1 and 37-1 had enhanced yields of 10.2–54.9% (av. 32.9%) and 2.8–43.4% (av. 24.8%) on 10 and 8 out of 12 varieties, respectively. This is the first report on endophytic B. thuringiensis strains isolated from wheat plants with the abilities to suppress WFS and to enhance yields on multiple wheat varieties.     

Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum and Aspergillus terreus

Disease resistance is a highly desirable crop trait in the sustainable agricultural industry. Endophytic fungi with gibberellins-secreting potential are now widely known for their ability to stimulate plant growth, but their role in promoting disease resistance in plants has rarely been reported. We have studied the role of Penicillium citrinum LWL4 and Aspergillus terreus LWL5 in time-dependent manner on sunflower (Helianthus annuus L.) growth, disease resistance and their capacity for the regulation of hormone signaling networks involved in plant defense against the stem rot caused by Sclerotium rolfsii for 3, 6 and 12 days after treatment (DAT). Our results show that plant growth characteristics (i.e. shoot length, shoot diameter, shoot fresh/dry weight, transpiration, stomatal conductance, photosynthesis and chlorophyll content) were promoted in fungi-treated plants with or without the disease caused by Sclerotium rolfsii as compared to their respective controls in 3, 6 and 12 DAT. The negative impacts of stem rot in endophyte-treated diseased plants were greatly reduced in comparison to control diseased plants shown by low disease severity in 3, 6 and 12 DAT. Similarly, fungal endophytes in diseased plants relieved the biotic stress in time-dependent manner (3, 6 and 12 DAT) as shown by low level of endogenous salicylic acid and jasmonic acid contents and were significantly higher in control diseased plants. Furthermore, we observed that the Penicillium citrinum LWL4 association had a greater positive effect on sunflower plants than Aspergillus terreus LWL5. It was concluded that inoculation with fungal endophytes reprogramed plant growth during disease incidence by regulating responses associated with host plant defense. Management strategies involving endophytic symbiosis can help achieve sustainability in agriculture in an eco-friendly manner by reducing excessive fungicide use.     

生防菌诱导植物系统抗性及其生化和细胞学机制

生防菌通常可利用竞争、抗生、寄生和交叉保护等直接的拮抗机制抑制植物病害;同时某些生防菌还能促进植物生长,诱导植物对真菌、细菌和病毒引起的病害乃至对线虫和昆虫为害的抗性,称为诱导系统抗性(ISR).ISR具有非特异性、广谱性和系统性,其在表型上与病原菌侵染激发的系统获得抗性(SAR)相似,具有同样的效率;但在寄主植物上不发生过敏性坏死反应(HR),无可见症状,为发展和改善更加安全而环境友好的植物保护策略开辟了新的思路.本文总结了生防真菌和细菌诱导系统抗性及其激发子和信号转导途径等方面的研究进展,重点阐述了寄主防御反应的生化和细胞学机制,并对ISR在植物病害生物防治中的应用前景进行了展望.     

Significance of ecology in the development of biocontrol agents against soil‐borne plant pathogens

Approaches to the development of inoculant biocontrol agents (BCAs) of soil‐borne pathogens are discussed. Based on an analysis of the success of Peniophora (Phlebia) gigantea and Agrobacterium radiobacter it is argued that most subsequent attempts to develop inoculant BCAs have failed because the organisms were selected for in vitro antagonism but were ecologically unsuited to the environments where pathogens grow. The reported modes of action of BCAs are reviewed and in some cases reinterpreted. It is argued that antibiosis and some types of mycoparasitism have not been shown to be direct mechanisms of biocontrol in vivo; they might, instead, facilitate competition for substrates or sites as the primary mechanism of control. The ecology of BCAs in general is reviewed, with emphasis on interactions in microsites and the design of appropriate screening strategies. Specific examples are used to illustrate these points.     

Moderate drought influences the effect of arbuscular mycorrhizal fungi as biocontrol agents against Verticillium-induced wilt in pepper

Previous studies have shown that the arbuscular mycorrhizal fungus (AMF) Glomus deserticola (Trappe, Bloss and Menge) can diminish the negative effect of Verticillium dahliae Kleb. on pepper yield. On the other hand, it is known that AMF can be more beneficial for plant growth and physiology under dry conditions than when soil moisture is plentiful. Therefore, our objective was to assess if a moderate water deficit imposed on pepper plants before their inoculation with V. dahliae could improve the effectiveness of G. deserticola as biocontrol agent. In the present experiment, the delay in disease development in Verticillium-inoculated plants associated with AMF did not occur under well watered conditions. In addition, the establishment of mycorrhizal symbiosis and the development of structures by AMF were delayed when both symbiotic and pathogenic fungi infected the same root. Therefore, it is suggested that the equilibrium between pepper plant, G. deserticola and V. dahliae is so complex that small changes in competition between symbiotic and pathogenic fungi for host resources can modify the efficiency of AMF as a biocontrol agent. On the other hand, water deficit enhanced the deleterious effect of V. dahliae on fruit set and yield only when pepper plants were not associated with G. deserticola, which reinforces the idea that AMF may be more important for host plants subjected to stressful conditions. However, comparing well watered non-mycorrhizal and predroughted mycorrhizal plants, we found that moderate water deficit imposed before inoculation with V. dahliae did not improve the effectiveness of G. deserticola as a biocontrol agent.     

Compatibility of systemic acquired resistance and microbial biocontrol for suppression of plant disease in a laboratory assay

Systemic acquired resistance (SAR) and microbial biocontrol each hold promise as alternatives to pesticides for control of plant diseases. SAR and Bacillus cereus UW85, a microbial biocontrol agent, separately suppress seedling damping-off diseases caused by oomycete pathogens. The purposes of this study were to investigate how expression of SAR affected the efficacy of biocontrol by UW85 and if UW85 treatment of plants induced SAR. We devised a laboratory assay in which seedling damping-off disease, induction of SAR, and growth of UW85 could be quantified. Seedlings of Nicotiana tabacum Xanthi nc were germinated on moist filter paper and transferred after 7 days to water agar plates (40 seedlings per plate). Zoospores of oomycete pathogens (Pythium torulosum, Pythium aphanidermatum, or Phytophthora parasitica) were applied at concentrations that caused 80% seedling mortality within 10 days. Seedling mortality was dependent on zoospore inoculum concentration. The level of disease suppression caused by treatment with UW85 depended on the UW85 dose applied. SAR was induced with 0.5-mM salicylic acid or 0.1-mM 2,6-dichloroisonicotinic acid. Expression of an SAR-related gene was confirmed by northern analysis with a probe prepared from a tobacco PR-1a cDNA. Induction of SAR suppressed disease caused by each of the oomycete pathogens, but did not alter the growth of UW85 on roots. Treatment of seedlings with UW85 did not induce the expression of PR-1a. The combination of induction of SAR and treatment with UW85 resulted in additive suppression of disease as measured by seedling survival.     

Application of actinomycetes as biocontrol agents in the management of onion bacterial rot diseases

This study was conducted to achieve biological control for the post-harvest onion bacterial rot diseases with the aid of Egyptian isolates of actinomycetes. In this respect, 45 actinomycetes strains were isolated from Egyptian soils and screened for their antagonistic effect against onion bacterial rot pathogens; Erwinia carotovora subsp. carotovora and Burkholderia cepacia. The most two active strains were identified based on their cultural, morphological and molecular properties as Streptomyces lavendulae HHFA1 and Streptomyces coelicolor HHFA2, the latter was most potent and so was used in vivo (pots and field) for controlling onion bacterial rot. S. coelicolor HHFA2 application resulted in enhancement in the photosynthetic pigments and some foliar growth parameters of onion plants confirming its growth promoting effect. The results of the post-harvest estimation of the disease incidence (DI) of the onion bacterial rot throughout storage revealed that, the application of S. coelicolor HHFA2 reduced the DI pronouncedly comparing with the untreated control and confirm its successful role in the biological control of onion bacterial rot diseases.     

Risk assessment for engineered bacteria used in biocontrol of fungal disease in agricultural crops

A plant growth promoting rhizobacterium (PGPR)Pseudomonas fluorescens SBW25 (WT) protects a number of crop plant species from damping-off caused by Pythium ultimum. A genetically modified, phenazine-1-carboxylic acid (PCA) producing variant, 23.10, carries on its chromosome a single copy of phzABCDEFG, under the control of the P tac constitutive promoter. The genetically modified biological control agent (GM-BCA), 23.10, has improved biocontrol activity when compared to wild type SBW25, and can effectively suppress Pythium spp. present at up to 100 times normal field infestations. GM-BCA inocula establish high population densities which persist well in the phytosphere of several crop plants including pea, wheat and sugar beet, effectively suppressed infection and promoted increase in total plant biomass. It also has an improved spectrum of activity over other plant phytopathogens such as Fusarium spp. Gaeumannomyces graminis var. tritici, Phytophtora cinnamomi and Rhizoctonia solani. However in developing BCAs and in particular GMBCAs it is important to determine whether their use has any adverse effect in the environment. Any observed changes following inoculation with wild type BCA or GM BCA in microbial diversity (bacteria and fungi) were negligible when assessed by either quantitive selective plate count methods (CFU/g) or culture independent molecular assays (SSU rRNA based PCR-DGGE). Rhizosphere community diversity profiles (DGGE) in infected plants in the presence of inocula were highly similar to disease free systems. Histological assessment of the impact of inocula on established functional mycorrhizae associations were conducted on cores collected from an established field margin grassland pasture. No adverse impact on mycorrhizal colonization and root infection were recorded after addition of WT or GM-BCA bacterial inocula as a soil drench. This approach and the related culturable and culture independent methods have recorded only a minor, transient perturbation to microbial communities, but as far as we are aware this is the first direct demonstration that a functional, AFC producing GMM also has only a transient impact on mycorrhizal associations in established plant communities. In all instances studied the plant species, plant stage of development and disease, damping-off, had a greater impact on changes in rhizosphere diversity than the presence of an introduced GM bacterial inocula.     

Isolation and screening of fungi associated with eggs and females of root-knot nematodes and their biocontrol potential against Meloidogyne incognita in Bangladesh

A total of 297 fungal isolates belonging to 20 genera and 33 species were isolated and identified from eggs and females of Meloidogyne spp. in Bangladesh. The predominant genera were Fusarium, Aspergillus and Penicillium; and the significant ones were Purpureocillium, Trichoderma and Pochonia. The 24 well tissue culture plate screening technique was applied for pathogenicity tests against Meloidogyne incognita in vitro. The average percentages of egg parasitism, egg hatch inhibition and juvenile mortality varied significantly and were ranged from 8.2 to 64.9% (p = 0.05), 24.8 to 72.4% (p = 0.05), and 2.3 to 33.1% (p = 0.05), respectively. Two isolates of Purpureocillium lilacinum (PLSAU 1 and PLSAU 2) and one isolate of Pochonia chlamydosporia (PCSAU 1) reduced more than 60% average root galls of tomato, eggplant and cucumber in greenhouse experiments. This is the first investigation of fungi associated with nematodes in the country and their biological control potential against M. incognita.     

Effects of chemical control agents and microbial biocontrol agents on numbers of non-target microbial soil organisms: a meta-analysis

Our aim was to investigate the non-target effects on soil micro-organisms in agricultural environments caused by chemical control agents (CCAs) and microbial biocontrol agents (mBCAs), including the recovery from these effects. This was a desk study in which quantifiable endpoints, such as numbers of colony forming units (CFU), were derived from a series of studies and the combined data then analysed with a meta-regression analysis. Three analyses of the same dataset were performed. The first analysis, which was performed at the level of the CCAs and mBCAs in general, revealed that the effects of CCAs differed significantly from those of mBCAs. The second analysis, which included the type of non-target group (bacteria, fungi, actinomycetes, and protozoa) as additional input, revealed that mBCAs have greater effects than CCAs on fungi at study initiation, that CCAs had greater effects than mBCAs on bacteria and protozoa and that when effects were measured, recovery occurred within 100 days post-treatment initiation. The final analysis, which included the type of CCA (fungicide, insecticide, herbicide) or mBCA (antagonist) as additional input, revealed that (1) antagonists had a greater effect on fungi than insecticides and fungicides, (2) insecticides and to a lesser extent fungicides had a larger effect on bacteria than fungicides and antagonists, and (3) recovery of the CFU occurred within 100 days for all types of pesticides, mBCAs as well as CCAs, and for all non-target groups. The findings are discussed in view of the regulatory context of admittance of mBCAs to the market.     

Improving function of biocontrol agents incorporated in antifungal fruit coatings: a review

The in-field performance of microbial biocontrol agents (BCAs) against fungal pathogens in fruit is subject to considerable variability due to their sensitivity to both adverse environmental conditions and their fluctuations. Therefore, to achieve an adequate development and implementation of biological agent-based products, it is necessary to improve their resistance and ability to control fungal diseases under a wide range of conditions. In this review, an overview of the latest strategies for the enhancement of the action of BCAs is given. The combination of the antagonists with edible polymers able to form coatings is one of the approaches with the greatest potential and it is analysed in depth. This formulation approach of biocontrol products, including adequate microbial protectants, can yield stable products with high microbial viability, ready for field applications, with improved adherence and survival of the BCA once applied in plant. The most recent studies into this field are reviewed and summarised.     

Harmonization of regulations for invertebrate biocontrol agents in Europe: progress,problems and solutions

The use of non‐native invertebrate biological control agents (IBCAs) in Europe is not covered by a Directive equivalent to that which regulates biocontrol with microorganisms or the genetic modification of crop plants. Regulation is at the discretion of individual member states and largely derived from national legislation on pesticides, plant health or environmental protection. There is no EU country with regulation of IBCAs that requires information on the microbial symbiont content of candidate species, and in the absence of horizontal transfer under natural conditions, this policy is unlikely to change. Although there have been few reported negative effects linked to the import and release of IBCAs, a number of countries have introduced or revised their regulatory frameworks in recent years. This article reviews major developments in the regulation and environmental risk assessment (ERA) of IBCAs in Europe over the last 10 years including: the fragmented pattern of regulation between countries, variation in information requirements for release licences, format and methods of ERA for different taxonomic groups of IBCAs, use and updating of the European Plant Protection Organisation Positive List, sources of expert advice on ERA data, communication between IBCA regulators, and options for the provision of international leadership to coordinate regulatory and ERA‐related issues with IBCA‐based biocontrol in Europe.     

A field experiment on the effectiveness of spiders and carabid beetles as biocontrol agents in soybean

1 Spiders and carabid beetles are abundant generalist predators that prey upon insect pests of soybean. A field experiment was conducted to determine the impact of spiders and carabids on soybean yield. Prior to planting, three 7 × 7 m plots were fenced in order to reduce spider and carabid immigration. Carabids that emerged within the plots were not removed, but spiders that ballooned into these predator‐reduction plots or that entered by climbing the fence were removed by pitfall trapping and searching the vegetation. Three unmanipulated, unfenced plots served as the control treatment. 2 Densities of spiders on soybean vegetation, and activity‐densities of spiders and carabids determined by pitfall trapping, were c. 75% lower in the spider‐carabid reduction treatment than in control plots. Despite clear differences between treatments in numbers and activity of these major generalist predators, the weight of soybeans harvested did not differ between control and spider‐carabid reduction plots. 3 Paralleling the absence of an effect of predator reduction on soybean yield was the absence of any significant difference between treatments in densities of whiteflies (Aleyrodidae), leafhoppers (Cicadellidae), thrips (Thysanoptera), Lepidoptera larvae and herbivorous Coleoptera. 4 Our experiment provides no evidence that spiders and carabid beetles at ambient densities affect soybean yield. Low populations of pest species or low predation pressure on soybean pests by spiders and carabids at the ambient densities of this experiment could be responsible for this result.     

Suppressive soil against Sclerotinia sclerotiorum as a source of potential biocontrol agents: selection and evaluation of Clonostachys rosea BAFC1646

The fungal diversity structures of soils that are suppressive and non-suppressive to Sclerotinia sclerotiorum were characterised and screened for fungal strains antagonistic to the S. sclerotiorum pathogen. Soil suppressiveness was associated with a particular fungal diversity structure. Principal component analysis showed that antagonism by fungal species in suppressive soils was associated with the occurrence of Fusarium oxysporum, Fusarium solani, Talaromyces flavus var. flavus and Clonostachys rosea f. rosea. In particular, C. rosea f. rosea occurred exclusively in suppressive soil samples, suggesting that this morpho-species plays an important role in suppression of S. sclerotiorum diseases. One strain of C. rosea f. rosea (BAFC1646) was selected for further experiments. Dual-culture assays confirmed the antagonistic behaviour of C. rosea f. rosea BAFC1646 against three different S. sclerotiorum strains. Antifungal activity was corroborated by diffusion assays with metabolite extracts. Greenhouse assays with soybean plants showed that the selected C. rosea f. rosea strain reduced the percentage of dead plants when co-inoculated with S. sclerotiorum. In addition, inclusion of C. rosea f. rosea alone increased shoot lengths significantly. In this work, we established the involvement of fungal species in soil suppressiveness and in further assays confirmed that C. rosea f. rosea BAFC1646 exhibits a bioprotective effect against S. sclerotiorum in soybean plants.     

Silicon-augmented resistance of plants to herbivorous insects: a review

Silicon (Si) is one of the most abundant elements in the earth's crust, although its essentiality in plant growth is not clearly established. However, the importance of Si as an element that is particularly beneficial for plants under a range of abiotic and biotic stresses is now beyond doubt. This paper reviews progress in exploring the benefits at two‐ and three‐trophic levels and the underlying mechanism of Si in enhancing the resistance of host plants to herbivorous insects. Numerous studies have shown an enhanced resistance of plants to insect herbivores including folivores, borers, and phloem and xylem feeders. Silicon may act directly on insect herbivores leading to a reduction in insect performance and plant damage. Various indirect effects may also be caused, for example, by delaying herbivore establishment and thus an increased chance of exposure to natural enemies, adverse weather events or control measures that target exposed insects. A further indirect effect of Si may be to increase tolerance of plants to abiotic stresses, notably water stress, which can in turn lead to a reduction in insect numbers and plant damage. There are two mechanisms by which Si is likely to increase resistance to herbivore feeding. Increased physical resistance (constitutive), based on solid amorphous silica, has long been considered the major mechanism of Si‐mediated defences of plants, although there is recent evidence for induced physical defence. Physical resistance involves reduced digestibility and/or increased hardness and abrasiveness of plant tissues because of silica deposition, mainly as opaline phytoliths, in various tissues, including epidermal silica cells. Further, there is now evidence that soluble Si is involved in induced chemical defences to insect herbivore attack through the enhanced production of defensive enzymes or possibly the enhanced release of plant volatiles. However, only two studies have tested for the effect of Si on an insect herbivore and third trophic level effects on the herbivore's predators and parasitoids. One study showed no effect of Si on natural enemies, but the methods used were not favourable for the detection of semiochemical‐mediated effects. Work recently commenced in Australia is methodologically and conceptually more advanced and an effect of Si on the plants' ability to generate an induced response by acting at the third trophic level was observed. This paper provides the first overview of Si in insect herbivore resistance studies, and highlights novel, recent hypotheses and findings in this area of research. Finally, we make suggestions for future research efforts in the use of Si to enhance plant resistance to insect herbivores.     

Entomogenous fungi in tropical forest ecosystems: an appraisal

Abstract. 1. Species of the genus Cordyceps (Ascomycotina; Clavicipitales) are the commonest fungi encountered on arthropods in tropical forests.
2. The asexual states of Cordyceps may occur in conjunction with or separately from the perfect state and are classified in the genera Hirsutella, Hymenostilbe, Nomuraea, Paecilomyces and Verticillium of the imperfect fungi (Deuteromycotina; Moniliales).
3. Most Cordyceps species have a restricted host range and this rigid host specificity, at the generic or tribal level, is especially evident in ant-fungal associations.
4. Pathogenicity was not tested but circumstantial evidence is presented which supports the view that Cordyceps species are primary pathogens of arthropods.
5. Observations of living, infected ants suggest that behavioural patterns are radically altered, possibly altruistically orientated.
6. It is thought that entomogenous fungi are involved in the regulation of arthropod populations and may help to maintain stability in tropical forest ecosystems.
7. The value of these organisms to man may be in the metabolites they produce rather than in their direct usage as biological control agents of insect pests.