Are predatory mites efficient dispersal agents of entomopathogenic fungi? : understanding the process of disease transmission from predators to prey for biological control

In biological control programs, predatory mites and entomopathogenic fungi are commonly used against western flower thrips, one of the most challenging pests in food and ornamental crops. Predatory mites can locate thrips even when thrips hide in plant crevices, but they only consume first instar larval thrips. Entomopathogenic fungi can infect all other stages, but their dispersal is passive and host encounter is therefore random. This thesis examines the potential role of predatory mites as dispersal agents of entomopathogenic fungi to thrips colonies. The experimental work has been divided into three sections. In the first section, we evaluated the pathogenicity of the entomopathogenic fungus Beauveria bassiana strain ANT-03 to all stages of the western flower thrips and to three species of predatory mites: Amblyseius swirskii and Neoseiulus cucumeris that are active on plants and Stratiolaelaps scimitus that is active in soil. We established that B. bassiana ANT-03, predatory mites and thrips form appropriate pathogen-vector-host associations. We also developed a commercially applicable method for predatory mites to collect B. bassiana spores directly from the rearing substrates and transport them to the environment. We demonstrated that spores did accumulate on predatory mites over time in the substrates. In the second section, using video recordings, we described how predatory mites dislodged spores by linking the number of spores remaining on a mite to the time spent grooming and walking. We compared behaviors of the predatory mites with and without spores following their release from rearing substrates. Using low-temperature scanning electronic microscopy, we visualized the spore distribution on mites. We showed that walking primarily contributed to predatory mites dislodging spores in our experimental arena, whereas grooming was insufficient. When bearing conidia, all three species of predatory mites extended their walking periods. The duration of grooming behavior was not affected for A. swirskii and N. cucumeris, and was even reduced for S. scimitus. For the third section, we determined the capacity of predatory mites to deliver spores to thrips colonies. Amblyseius swirskii and N. cucumeris were loaded with spores and released on plants that had been previously infested with first instar thrips clustered on leaves. We carefully characterized the spatial distribution of each organism on plants, calculated the spatial co-occurrence index of spores and thrips, and estimated the proportion of thrips with spores. Both mites dispersed similar amounts of spores per plant, but A. swirskii delivered more spores to thrips infested leaves and thereby played a significant role in spreading the fungal disease to thrips populations. The observed differences between predatory mite species resulted from different foraging activity patterns. By understanding how the pathogens can be transferred from foraging predatory mites to prey, we provided a theoretical basis for identifying candidate predators as efficient fungal dispersal agents. These methods, if validated in commercially representative settings, could increase the capacity of predatory mites to suppress thrips populations by combining predation and dispersion of entomopathogens for biological control.

Keyphrases: fungal dispersal, grooming behavior, spatial co-occurrence, tritrophic interactions, Beauveria bassiana, Amblyseius swirskii, Neoseiulus cucumeris, Stratiolaelaps scimitus