Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae)

Entomopathogenic fungi are typically applied as innundative sprays with the expectation of short-term pest control, but a growing number of studies demonstrate the potential of these fungi to endophytically colonize a wide variety of plants and confer longer-term protection. Endophytic colonization of plants by fungal entomopathogens can also enable these fungi to establish intricate interactions in a tritrophic context; thus affecting other groups of natural enemies such as parasitoids. Yet to date, effects of endophytic plant colonization on parasitoids have mostly been investigated using the grass-endophyte organism systems. The present study investigates the effects of the fungal entomopathogens Beauveria bassiana and Metarhizium brunneum, following their endophytic colonization of sweet pepper Capsicum annum, on the development and fecundity of two successive generations of the green peach aphid Myzus persicae in addition to parasitism by the aphid endoparasitoid Aphidius colemani in two replicate greenhouse experiments. Plant roots were drenched with the conidial suspension of each fungal strain or sterile water, and the endophytic colonization of different plant parts (root, stem, and leaf) was confirmed 7 (when 1st generation M. persicae started feeding on caged treatment plants) and 17 (when A. colemani started parasitizing 2nd generation M. persicae reared on caged treatment plants) days post-inoculation (dpi). Inoculation with the tested fungal entomopathogens enhanced several plant growth parameters that were sampled 7 dpi (before M. persicae infestation) and all plant growth parameters sampled 35 dpi (following infestation with two successive generations of M. persicae). Fewer numbers of aphids were found when sampling plants inoculated with both fungal strains in comparison to the control during the development and reproduction of 1st and 2nd generations of M. persicae. The negative effects of plant colonization with the inoculated fungal strains on aphid development and fecundity also included prolonged development time, delayed onset of reproduction, and reduced birth rate. On the other hand, the percentage mummification and adult emergence of A. colemani progenies parasitizing 2nd generation aphid reared on inoculated or control plants were not affected by plant colonization with B. bassiana and M. brunneum. In addition, no differences were observed in development time, percentage female, and adult longevity of A. colemani progenies among inoculated and control plants. This study presents one of very few reports of the compatible use of endophytic fungal entomopathogens with other biological control agents, particularly parasitoids, for aphid suppression under controlled greenhouse conditions as part of an Integrated Pest Management (IPM) approach.