Impact of endophytic colonization by entomopathogenic fungi on the behavior and life history of the tobacco peach aphid Myzus persicae var. nicotianae

Abstract

Entomopathogenic fungi can adopt an endophytic lifestyle and provide protection against insect herbivores and plant pathogens. So far, most studies have focused on Beauveria bassiana to increase plant resistance against abiotic and biotic stresses, while only little is known for other entomopathogenic fungi. In this study, we investigated whether root inoculation of sweet pepper (Capsicum annuum L.) by the entomopathogenic fungi Akanthomyces muscarius ARSEF 5128 and B. bassiana ARSEF 3097 can improve resistance against the tobacco peach aphid Myzus persicae var. nicotianae. First, dual-choice experiments were performed to test the hypothesis that the fungi deter aphids via modifying plant volatile profiles. Next, we tested the hypothesis that endophytic colonization negatively affects aphid life history traits, such as fecundity, development and mortality rate. Aphids were significantly attracted to the odor of plants inoculated with A. muscarius over non-inoculated plants. Plants inoculated with A. muscarius emitted significantly higher amounts of β-pinene than non-inoculated plants, and significantly higher amounts of indole than B. bassiana-inoculated and non-inoculated plants. Inoculation with the fungal strains also caused significantly higher emission of terpinolene. Further, both aphid longevity and fecundity were significantly reduced by 18% and 10%, respectively, when feeding on plants inoculated with A. muscarius, although intrinsic rate of population increase did not differ between inoculated and non-inoculated plants. Sweet pepper plants inoculated with B. bassiana ARSEF 3097 did not elicit a significant behavioral response nor affected the investigated life history traits. We conclude that endophytic colonization by entomopathogenic fungi has the potential to alter olfactory behavior and performance of M. persicae var. nicotianae, but effects are small and depend on the fungal strain used.

Bacterial volatiles elicit differential olfactory responses in insect species from the same and different trophic levels

“…, 2013; Wilberts et al. , 2022). Individuals that had passed a set line in one of the olfactometer arms (1 cm from the Y‐junction) at the time of evaluation were considered to have chosen the odor source presented by that olfactometer arm (Goelen et al.…”

“…Olfactory response was evaluated 10 min after parasitoid or hyperparasitoid release (Goelen et al, 2020a), or 20 min after aphid release, which was found to be the optimal time point of evaluation in preliminary experiments. Although different set-ups can be used to assess the olfactory behavior of aphids, previous studies have identified glass Y-tubes to not only be suited to assess the olfactory response of primary and secondary parasitoids, but also aphids (Fernández-Grandon et al, 2013;Wilberts et al, 2022). Individuals that had passed a set line in one of the olfactometer arms (1 cm from the Y-junction) at the time of evaluation were considered to have chosen the odor source presented by that olfactometer arm (Goelen et al, 2020a).…”

Effects of root inoculation of entomopathogenic fungi on olfactory‐mediated behavior and life‐history traits of the parasitoid Aphidius ervi (Haliday) (Hymenoptera: Braconidae)

“…In addition, an increasing number of studies have reported the potential of endophytic entomopathogenic fungi to induce plant resistance against pathogens and insect herbivores 14,20,22–24 . These indirect effects on insect herbivores may result from the induction of toxic and deterrent plant metabolites, leading to impaired herbivore performance and reduced feeding damage, respectively 14,16,23,25–27 . Endophytic entomopathogenic fungi can also protect plants against insect herbivores directly, when they colonize plants systematically and fungal propagules are ingested by the herbivores, resulting in mycosis 25 .…”

“…Given that endophytic entomopathogenic fungi can alter emissions of plant VOCs, 26,33 parasitoids could also be impacted by the inoculation of endophytic entomopathogenic fungi by modulating their attraction towards host‐infested plants. However, there is limited information describing the impact of endophytic entomopathogenic fungi on higher trophic levels, such as parasitoids, and the few studies conducted so far have only investigated effects on parasitoid life history 34–36 .…”

“…In this study, we investigated whether root inoculation of sweet pepper ( Capsicum annuum L.; Solanaceae) with the entomopathogenic fungus Akanthomyces muscarius ARSEF 5128 is compatible with parasitoid wasps for enhanced biocontrol of aphids, which constitute a major threat to modern agriculture 38,39 . In previous research, A. muscarius ARSEF 5128 was found to endophytically colonize sweet pepper plants, leading to reduced aphid longevity and fecundity 26 . Furthermore, the fungus has been found to alter the VOC profile of sweet pepper on root inoculation 26 .…”