Passive vectoring of entomopathogenic fungus Beauveria bassiana among the wax moth Galleria mellonella larvae by the ectoparasitoid Habrobracon hebetor females

Abstract

Females of the ectoparasitoid Habrobracon hebetor attack and envenomate numerous host individuals during oviposition. The vectoring of the entomopathogenic fungus Beauveria bassiana during the adhesion stage by ectoparasitoid females among the wax moth larvae Galleria mellonella was explored under laboratory conditions. Vectoring occurred both from infected parasitoids to wax moth larvae and from infected to healthy wax moth larvae by parasitoids. The efficacy of vectoring in both cases was dose dependent. Parasitoid females were unable to recognize infected larvae in a labyrinth test. In addition, the presence of H. hebetor females significantly (1.5-13 fold) increased the mycoses level in clusters of G. mellonella, with 40% of the larvae infected with fungal conidia. Envenomation by H. hebetor increased conidia germination on the cuticles of the wax moth larvae by 4.4 fold. An enhanced germination rate (2 fold) was registered in the n-hexane epicuticular extract of envenomated larvae compared to that of healthy larvae. Both envenomation and mycoses enhanced the phenoloxidase (PO) activity in the integument of G. mellonella and, in contrast, decreased the encapsulation rate in hemolymphs. We hypothesize that changes in the integument property and inhibition of cellular immunity provide the highest infection efficacy of entomopathogenic fungi with H. hebetor.

Parasitoid envenomation alters the Galleria mellonella midgut microbiota and immunity, thereby promoting fungal infection

“…The mechanism of the observed synergy is unclear. Previously, we showed that one of the main antifungal reactions – encapsulation – was decreased in wax moth hemolymph after envenomation by H. hebetor 32,35 . The decrease in this parameter can be caused by either the direct action of the venom on hemocytes 33 or through the influence of midgut bacteria.…”

“…Moreover, the additional load of cultivable bacteria in the gut promotes the development of fungal infection. Previously, many researchers considered mechanisms of synergy between entomopathogenic fungi and various intestinal or systemic toxicants (including parasitoid venoms) based on different changes in humoral and cellular immune reactions 35,65–70 . However, the impact of the toxicants on microbial communities was insufficiently understood.…”

“…Envenomated insects do not survive; they are eventually colonized with different microorganisms, primarily bacteria. However, if envenomated larvae were topically inoculated with the entomopathogenic ascomycetes Beauveria, Isaria , or Metarhizium (even at extremely low doses) they were successfully colonized by the fungi 34,35 . Interestingly, envenomated wax moth larvae were thousands of folds more susceptible to fungal infection compared to nonenvenomated larvae 34 , and the susceptibility was increased to pathogenic but not opportunistic fungi 36 .…”

Compatibility between the endoparasitoid Hyposoter didymator and the entomopathogenic fungus Metarhizium brunneum: a laboratory simulation for the simultaneous use to control Spodoptera littoralis

“…Interactions between entomopathogenic fungi and parasitoids have been reported in many papers with mixed results. Some indicate high compatibility between these two biological control agents with no negative effects of the fungus on the parasitoid, or even describe the potential to use parasitoids as vectors of entomopathogenic fungi . However, other studies indicated antagonistic interactions between the two agents .…”

Effects of fluorine‐containing usnic acid and fungus Beauveria bassiana on the survival and immune–physiological reactions of Colorado potato beetle larvae

“…Many infected larvae survive until the prepupal stage, therefore, the insects have enough time to inflict significant damage on plants. Furthermore, generalist ascomycetes, such as Beauveria and Metarhizium , have been adapted to kill the weakest insects, for example, those that have been stressed by different ecological factors . In this respect, it seems relevant to search biological or chemical agents that would serve as synergists for the fungal pathogens.…”