Entomopathogens and Parasitoids Allied in Biocontrol: A Systematic Review

Abstract

Biological pest control is an environmentally friendly alternative to synthetic pesticides, using organisms such as viruses, bacteria, fungi, and parasitoids. However, efficacy is variable and combining different biocontrol agents could improve success rates. We conducted a systematic review of studies combining a parasitoid with an entomopathogenic microorganism, the first of its kind. We searched in Web of Science and extracted data from 49 publications matching the pre-defined inclusion criteria. Combinations of 36 hymenopteran parasitoids with 17 entomopathogenic microorganisms used to control 31 target pests were found. Trichogramma pretiosum and Encarsia formosa were the most frequently studied parasitoids, while Beauveria bassiana, Metarhizium anisopliae, Lecanicillium muscarium, Bacillus thuringiensis var. kurstaki, the Spodoptera exigua multiple nucleopolyhedrovirus, and the Spodoptera frugiperda multiple nucleopolyhedrovirus were the main microbial agents assessed. Out of 49 parasitoid-microorganism combinations assessed in the laboratory experiments, thirty-eight were reported as compatible and six as incompatible. Timing and dosage of biopesticides played a crucial role, with later application and appropriate dosage minimizing adverse effects on parasitoid development. More research is needed to assess compatibility and efficacy under real-world conditions. Our review provides valuable insights for researchers and practitioners to optimize the combined use of micro- and macroorganisms for effective pest control.

Keywords: antagonism; compatibility; microbial pesticide; parasitoid wasp; pest management; synergism.

Figure 1

Types of interactions and factors influencing the compatibility of entomopathogenic microorganisms and parasitoids. * Comparison made with the more effective of agents A or B.

Figure 2

Order and family of target pests where combined biocontrol agents were used (n = 100 combination experiments from 49 studies).

Figure 3

Family and species of hymenopteran parasitoids used in combination with an entomopathogenic microorganism (n = 100 combination experiments from 49 studies).

Figure 4

Type and species of entomopathogenic microorganisms used in combination with a parasitoid (n = 100 combination experiments from 49 studies). Bb = Beauveria bassiana; Ma = Metarhizium anisopliae; Lm = Lecanicillium muscarium; Mb = Metarhizium brunneum; Ll = Lecanicillium longisporum; Pn = Pandora neoaphidis; As = Acremonium sclerotigenum; Mr = Metarhizium robertsii; Pv = Paecilomyces variotii; Ssp. = Simplicillium sp.; Btk = Bacillus thuringiensis var. kurstaki; Bta = Bacillus thuringiensis var. aizawai; Bti = Bt var. israelensis; Bl = Brevibacillus laterosporus; SeMNPV = Spodoptera exigua multiple nucleopolyhedrovirus; SfMNPV = Spodoptera frugiperda multiple nucleopolyhedrovirus; HearNPV = Helicoverpa armigera nuclopolyhedrovirus.