Dose, temperature and formulation shape Metarhizium anisopliae virulence against the oriental fruit fly: lessons for improving on-target control strategies

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Abstract

Entomopathogenic fungi are a promising tool for the biological control of crop pests provided low or no impact on non-target organisms. Selection for host specificity as well as on-target applications open new avenues for more sustainable strategies for pest management. Isolates of Metarhizium anisopliae (Metschn.) Sorokin have been identified as promising for developing innovative entomovectoring-based strategies for the control of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in Africa. To be effective, this technology requires high strain virulence at a low number of spores, but sufficient incubation time to allow transmission to wild conspecifics. This depends on trophic interactions between the host and the pathogen, which are mediated by abiotic factors.

In the present study, we investigated the virulence of the Met69 strain against adult flies, depending on the inoculation dose, air temperature and formulation. High pathogenicity was observed at very low inoculation doses (LT50 of 4.85 days with 6100 spores per fly) independently of fly sex. Virulence increased with spore load in a tight range (5600 and 6100 spores per fly) and with air temperature observed in the field (20-28°C). Unexpectedly, corn starch used as an adjuvant to increase the carrying capacity of insects decreased the virulence of the pathogen.

The results will help improve area-wide control strategies based on the contamination of wild flies through auto-inoculation devices or interactions with released mass-reared sterile males coated with fungal spores. Furthermore, the study proposes an approach for calibrating area-wide control strategies, taking into account both the insect and pathogen bioecology and the environment in which they evolve.

Author roles

Anaïs Chailleux: Conceptualization, Funding acquisition, Methodology, Data curation, Writing – original draft. Oumou Noumou Coulibaly: Investigation, Writing – original draft. Babacar Diouf: Investigation, Visualization. Samba Diop: Investigation. Ahmad Sohel: Resources, Writing – review & editing. Thierry Brévault: Conceptualization, Funding acquisition, Project administration, Writing – review & editing.

Article activity feed

  1. Using entomopathogenic fungi for biological control is an effective method for controlling certain crop pests, with the perspective of reducing the use of chemical pesticides. Yet, the efficiency of pathogenic fungi is dependent upon many factors that need to be evaluated to improve biological control potential in the fields (Lacey, 2001). The article by Chailleux et al. (2024) presents an exciting contribution to the field of biological pest control, specifically focusing on using entomopathogenic fungi to manage the oriental fruit fly, Bactrocera dorsalis. This fly, a member of the Tephritidae family, is a major threat to orchards in Asia, the Pacific and Africa, as it attacks fruit and causes considerable damage, in addition to having a relatively rapid biological invasion dynamic (Clarke et al. 2005). 

    The objective of the Chailleux et al. (2024) study was to evaluate the virulence of Metarhizium anisopliae spores (strain Met69) on B. dorsalis adult flies according to various conditions: the inoculation dose and spore load, the formulation (adjuvant) and temperature conditions. The focus on host specificity and on-target applications was conducted to ensure minimal impact on non-target organisms, which is crucial for sustainable agriculture. The main challenge in this system was to achieve high strain virulence to kill wild individuals with a low number of spores—therefore limiting impact on non-target species such as natural enemies—but with a sufficient incubation period to allow transmission from mass-reared insects to wild conspecifics (Leite et al. 2022). A comparison of different inoculation methods is also provided and is interesting from a methodological point of view for future studies or even large-scale applications.

    Using a well-designed experimental setup, the authors show that high pathogenicity (measured by LD50) is achievable even at low spore doses and independently of the fly's sex. Lethal action speed was, however, dependent on the dose. Regarding temperature, the authors demonstrated that mycelium growth was affected by the mean temperature but, most importantly, by daily fluctuation regimes; night and day temperature alternation allowed faster growth than constant temperature. These notions of thermal fluctuations are still under-researched in terms of their modulating role in biological control yet seem central to understanding them, as the authors demonstrate here. The correlation between increased virulence and specific abiotic factors, such as temperature, offers valuable additional insights into the bioecology of the insect host and the fungal pathogen. Chailleux et al. finally point out the need for careful selection of adjuvants in formulations and pay attention to interactions with the abiotic environment to avoid compromising the effectiveness of biological control agents. Indeed, the survival rate of inoculated flies increased in the presence of the corn starch adjuvant, but this effect decreased with temperature. As corn starch unexpectedly delayed mortality, the authors suggest a potential for enhancing conspecific transmission

    From a broader perspective, the study emphasizes the importance of standardizing virulence evaluation to optimize biological control strategies like auto-dissemination or vectoring with sterile males, particularly in field conditions. The study contributions are timely and essential for advancing sustainable pest management strategies and improving inoculation methods. The findings underscore the need for field trials to refine these strategies, particularly in Africa, where climatic factors may affect pathogen efficacy and fly behavior. I recommend publishing this article in a referenced journal like the Peer Community Journal. 

    References

    Chailleux, A. Coulibaly, ON, Diouf B, Diop S, Sohel A, Brevault T (2023) Dose, temperature and formulation shape Metarhizium anisopliae virulence against the oriental fruit fly: lessons for improving on-target control strategies. bioRxiv, ver.2 peer-reviewed and recommended by PCI Zoology https://doi.org/10.1101/2023.12.14.571642

    Clarke, A. R. et al. (2005). Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annu. Rev. Entomol., 50, 293-319. https://doi.org/10.1146/annurev.ento.50.071803.130428

    Lacey, L. A. (2001). Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. J Invertebr Pathol, 77, 147. https://doi.org/10.1006/jipa.2000.5005

    Leite, M. O. et al. (2022). Laboratory risk assessment of three entomopathogenic fungi used for pest control toward social bee pollinators. Microorganisms, 10, 1800. https://doi.org/10.3390/microorganisms10091800