Entomopathogenic fungi are now known to have an endophytic capacity that induces a wide range of changes in the composition of plant nutrients and/or defensive compounds. These changes could influence interactions between the plant and higher trophic levels. In this study, we evaluated the predation/parasitism efficacy of larvae of the lacewing, Chrysoperla carnea, and the braconid parasitoid, Aphidius colemani, when offered aphids that had been challenged by the entomopathogenic fungus Beauveria bassiana. Aphids were either inoculated directly with a fungal suspension (lacewing bioassay only) or had been feeding on melon plants endophytically colonized by B. bassiana. Our results indicate that B. bassiana application did not significantly influence the number of aphid prey consumed by lacewings, or the time took them to consume each aphid. In a choice bioassay, C. carnea larvae preferred to feed on aphids reared on B. bassiana-colonized plants compared with control plants. In another choice assay, the number of aphids parasitized by A. colemani and their sex ratio were not influenced by whether the aphids had been feeding on B. bassiana-colonized plants or not. Our findings support the hypothesis that endophytic entomopathogenic fungi can be used in combination with other natural enemies, such as predators and parasitoids, in Integrated Pest Management programmes.

Entomopathogenic fungi are sprayed commercially for aphid control in greenhouses. Recently, their ability to grow endophytically within plants was discovered, offering the opportunity for systemic biological control. Endophytic colonization of host plants could also influence life-table parameters and behavior of herbivores. We investigated lethal and pre-mortality effects of Beauveria bassiana and Metarhizium brunneum on Aphis gossypii; aphids either received inoculum while feeding on recently sprayed leaves (surface inoculum and endophytically-colonized) or while feeding on unsprayed but endophytically-colonized leaves. We used choice assays to identify any preferences for endophytically-colonized or control plants. Volatile emissions from endophytically-colonized plants and control plants were also compared. Aphid mortality rates ranged between 48.2 and 56.9% on sprayed leaves, and between 37.7 and 50.0 on endophytically-colonized leaves. There was a significant effect of endophytic colonization on the rate of nymph production, but this did not result in an overall increase in the aphid population. Endophytic colonization did not influence host-plant selection even though there were qualitative and quantitative differences in the blend of volatiles released by endophytically-colonized and control plants. Although endophytic colonization did not change herbivore behavior, plants still benefit via indirect defense, resistance to plant pathogens or abiotic stress tolerance.

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Entomopathogenic fungi are gaining acceptance in Integrated Pest Management (IPM) systems as effective and environmental safety biological control agents to protect a great variety of crops against pest insects. Many of these insect-pathogenic fungi can establish themselves as endophytes and thereby may induce the plant immune system. The activation of plant defenses by the fungal endophytic colonization can have a direct impact on herbivores and plant pathogens. An integral component of many plant defense responses is also the release of volatile organic compounds, which may serve as an indirect defense by attracting the natural enemies of herbivores. Here we investigated the effect of endophytic colonization by the entomopathogenic fungus Beauveria bassiana on the volatile emission by melon and cotton plants, either unharmed or after being damaged by sap-sucking aphids or leaf chewing caterpillars. We found that when the plants are colonized by B. bassiana they emit a different blend of volatile compounds compared to uncolonized control plants. Some of the emitted compounds have been reported previously to be released in response to herbivory and have been implicated in natural enemy attraction. Several of the compounds are also known to have antimicrobial properties. Therefore, endophytic colonization by B. bassiana might help to not only direct control insect pests but also increase the resistance of plants against agronomically important pests and phytopathogens.

One of the main negative effects of climate change on biological pest control is alteration of relationships between insect pests and their natural enemies (both entomophagous and entomopathogenic). Indeed, environmental conditions can have multiple effects on pest control success when using entomopathogenic fungi (EPF), where conidial depletion, inactivation, and loss in virulence and infectivity can all occur. Appropriate mass production and formulation strategies for EPF can partially solve these problems. However, the only strategy to guarantee high virulence and infectivity is selection of environmentally competent fungal strains that are able to persist in the host environment for the required infection period. This review examines the criteria for selection of environmentally competent EPF. While UV radiation, followed by humidity and temperature, is probably the most important propagule depletion and inactivation factors in epigeal habitats, temperature is most critical for reducing the infectivity and virulence of EPF in epigeal and hypogeal habitats. In addition, geographical origin and other biotic and abiotic factors have an important impact which may guarantee the environmental competence of selected entomopathogenic fungal strains and, therefore, farmer willingness to replace chemicals with mycoinsecticides. To achieve this, it is urgent to promote the development of microbial control solutions adapted to relatively uniform climatic zones through more simplified, targeted, and less costly EPF approval and authorization.

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Biocontrol with hypocrealean entomopathogenic fungi (EF) is a key tool to develop Integrated Pest Management (IPM) programs for the progressive replacement of synthetic chemical insecticides with more environmentally friendly pest control measures. These fungi stand out among entomopathogens not only for their contact mechanism of infection through the arthropod integument, but also for developing close associations with plants including the endophytic lifestyle and rhizosphere competence that can enable them to make broader contributions to IPM and crop production. Anyhow, the interaction of EF with the plants incorporates multitrophic complexity at different levels including insect pests, plants, and their natural enemies. The aim of the present review was to gather and summarize all available data on multitrophic interactions of EF. These fungi can influence both the chemical ecology of host-plant selection by insect pests and the host or prey selection by parasitoid or predators, respectively. Moreover, EF treatments are compatible with natural enemies in terms of safety and effectiveness, which could allow biocontrol strategies for their synergistic application in IPM programs. A comprehensive understanding of the impact of these multitrophic interactions in longer term, farm-level real-life biocontrol implementation studies will provide new opportunities in plant protection and production.

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