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.

Metarhizium anisopliae, a fungal pathogen of terrestrial arthropods, kills the aquatic larvae of Aedes aegypti, the vector of dengue and yellow fever. The fungus kills without adhering to the host cuticle. Ingested conidia also fail to germinate and are expelled in fecal pellets. This study investigates the mechanism by which this fungus adapted to terrestrial hosts kills aquatic mosquito larvae. Genes associated with the M. anisopliae early pathogenic response (proteinases Pr1 and Pr2, and adhesins, Mad1 and Mad2) are upregulated in the presence of larvae, but the established infection process observed in terrestrial hosts does not progress and insecticidal destruxins were not detected. Protease inhibitors reduce larval mortality indicating the importance of proteases in the host interaction. The Ae. aegypti immune response to M. anisopliae appears limited, whilst the oxidative stress response gene encoding for thiol peroxidase is upregulated. Cecropin and Hsp70 genes are downregulated as larval death occurs, and insect mortality appears to be linked to autolysis through caspase activity regulated by Hsp70 and inhibited, in infected larvae, by protease inhibitors. Evidence is presented that a traditional host-pathogen response does not occur as the species have not evolved to interact. M. anisopliae retains pre-formed pathogenic determinants which mediate host mortality, but unlike true aquatic fungal pathogens, does not recognise and colonise the larval host.

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.