Metarhizium brunneum: a key tool to strengthen Integrated Pest Management (IPM)

1 - Crop Pest Management, a challenging scenery

Modern agriculture is facing two major challenges, a) the adoption of technologies
to adapt to steading climate change, and b) the fast-growing population of the world,
which is expected to reach 10 bn by the year 2050 (United Nations 2011).

To ensure a reliable food supply in the coming years, agronomists and scientists from all over the world effort towards developing new agricultural practices for higher yields and harvest quality (FAO 2021). Among these practices, according to FAO’s report in 2021, the insect-pest management is one of the priorities since their incidence and voracity are strongly influenced by global warming and causes annual losses of about 10 to 20% globally what represents some 70 bn USD.

Over the past several decades, pest management has been run basically by the intense use of synthetic pesticides, which although offer quick pest eradication their use also causes hazards to both human health and agroecosystems (FAO 2021). Furthermore, persistent exposure to pesticides has developed pest resistance to several active ingredients.

Consequently, to reduce the negative effect of synthetic pesticides, and offer reliable long lasting mode of actions for pest management, numerous efforts have been made to develop new solutions to strength the IPM programs.

2 - Entomopathogenic Fungi (EPF) biopesticides fit in IPM programs

Biopesticides play a key role in Integrated Pest Management (IPM). They offer numerous advantages such as the preservation of pollinators and non-targeted species, they do not leave toxic residues on harvests, are safe for workers, and reduce populations resistant to chemical pesticides (EPA 2017).

In contrast to synthetic pesticides, which mode of action is site-specific, biopesticides based on EPF are multi-site non-specific, what reduces considerably the possibility of insects developing resistance against them. Pest populations develop resistance to site-specific mode of action because of their capacity to develop biochemical defensive mechanisms and inherit them to the next generations, making necessary to implement effective resistant management programs as component of the IPM strategies to alleviate the selection pressure and preserve effectiveness and longevity of currently available chemical pesticides (Eddiedu et al., 2020).

3 - Metarhizium brunneum Petch strain Ma43 (F52)

Previously known as Metarhizium anisoplaiae Petch strain BIPESCO 5/F52, it is a naturally found, soil-borne beneficial fungus, originally isolated in Austria from the codling moth Cydia pomonella L. It is an entomopathogenic fungus characterized by its radial mycelial growth in growing media, with abundant production of oblong (7-9 x 2.6-3.1 μm) conidia which turn to olive-green when mature, the growth temperature goes from 15 to 32 °C, being 26 °C the optimum for growth and sporulation (Zimmerman 2007, Tulloch 1976).

Metarhizium brunneum strain Ma43 (F52) infects and kill many soilborne and foliar insect and mite species harmful to crops, shows a minimum impact on users during the spraying process, and is safe for beneficials and non-targeted organisms from the surrounding environment which makes it a promising active ingredient to control soilborne and foliar pests of economic importance in the agriculture (European Commission 2014).

4 - Multi-site and non-specific mode of action

In rough terms, Metarhizium brunneum strain Ma43 (F52) mode of action is by “contact”. As illustrate in the image bellow, once the spore is in contact with the targeted insect (1), it produces a germinative tube (2), penetrates the insect cuticle, and produces a massive quantity of single cells called blastospores that spread all along the interior of the insect body (3), producing abundant fungus mycelium (4), and ultimately killing the insect in three to seven days (5) (Zimmermann 2007, St. Leger et al. 1991, Tulloch 1976).

Sounds simple at first glance, but going into little more details we can see that the mode of action process involves a complex chain of events, including a series of physical and biochemical mechanisms that make almost impossible for the targeted insect or mite to develop resistance at the same time against all and each of the multiple mechanisms involved, as described:

• Adhesion
  Along millions of years of coevolution with the hosts, Metarhizium brunneum has developed mechanisms of recognition and adhesion to the host surface. Electrostatic forces make the spore recognize the host and adhere to it when it is reached by the spraying or when the conidia are collected from the plant after the spraying (Padilla-Guerrero et al. 2011).

• Germination
  Environmental moisture and biochemical substances released by the host stimulate the spore germination, producing a germinative tube with a penetration structure call germ tube or appressorium (Dongdong et al. 2023, Zimmermann 2007, St. Leger et al. 1991).

• Penetration
  The appressorium forms a thin penetration peg that, via mechanical pressure and the production of cuticle-degrading enzymatic action (proteases, chitinases, lipases), breaches the insect cuticula facilitating the penetration and letting the fungus reach the nutrient-rich insect hemolymph. During this step of the process, each type of enzyme plays a specific role, as described below (Dongdong et al. 2023, Mustafa and Kaur 2009,. St. Leger et al. 1991):

• • Lipases: hydrolyze the cuticle lipoproteins, fats and waxes of the insect’s integuments, contributing significantly to the cuticle penetration.
  • Proteases: once the epicuticle breaks down, the fungus produces great quantities of protease (Pr1) which degrades the proteinaceous material in the procuticle.
  • Chitinases: act synergically with proteases to degrade the insect cuticle which is rich in chitins in many insects.

• Invasion
  Once the fungus overcomes the insect defenses and reaches the hemolymph in the interior of the insect body, the germ tube produces a massive number of single-cell reproductive structures called “blastospores” that spread withing the hemolymph and produces toxins which triggers an immediate disease to the insect, making it stop feeding and reproducing. In the specific case of Metarhizium brunneum other secondary metabolites are produced, including six types of destruxins, cytochalasins (C and D) and hydroxyfungerins A and B, all of them are toxic metabolites that accelerate the fungus parasitism and cause insect mortality (Wang et al. 2023, Dongdong et al. 2023, Uchida et al. 2005).

After this, the infected insect may exhibit deformities and mummification, and eventually external sporulation is observed if the relative humidity is higher than 80%. Under this condition, infections are easily recognized since the fungal growth appears soon with a white color, but as conidia mature, they take a characteristic olive-green color.

The complex and multiple mechanisms of action provided by Metarhizium brunneum strain Ma43 (F52) makes it an ideal tool to be included in the IPM programs for pest resistance management strategies, considering that in a rotational program this entomopathogenic fungus will control a considerable percentage of those individuals not controlled by synthetic pesticides.

5 - Metarhizium brunneum in the pest management rotational programs

In the last decades, the average number of insects and mites resistant cases to synthetic pesticides have increased, a phenomenon that has been closely associated with the availability of new chemical groups introduced to the market. In the last decade, many countries have banned a considerable number of pesticides due to their harmful effects to human health and the environment, this shortage of available products is limiting the rotational options for an effective pest-resistant management, driving to a dramatic increase of the annual reported resistance cases.

Pesticide rotation is the alternation of products with different modes of action. If the same mode of action is used repeatedly, it is expected to increase the selection pressure on the pest population with the consequence of speeding up the appearance of resistance (IRAC 2023, Showket 2017). The Insecticides Resistant Action Committee (IRAC) has grouped insecticides and miticides into 36 known site-specific modes of action, and 7 unknown or multi-site nonspecific modes of action, where Metarhizium brunneum strain F52 is included. This chart represents a useful tool to design rotational programs oriented to mitigate the appearance of populations resistant to pesticides.

In recent years, growers have turned their attention to the use of entomopathogenic fungi to reduce selective pressure on insect and mite populations. Products based on Metarizhium brunneum Ma43, have demonstrated a lower probability of developing resistance because of the multiple targeted receptors involved in its infection process, as it was described above in the mode of action section of this article. Integrating this product in the rotational pest management programs offers the advantage of eliminating resistant and susceptible individuals in the same proportion, contrary to synthetic pesticides that only eliminate susceptible individuals when resistance has been generated to a specific mode of action.

6 - Conclusion

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In conclusion, the current crop pest management scenery demands biological solutions that fit into the Integrated Pest Management programs (IPM) and ensure a sustainable approach that helps growers produce sufficient and healthier food while reducing the risk of pesticide resistance and protecting the environment.

By strengthening the pesticides rotational programs with efficient biological products, the growers can extend the effectiveness of authorized synthetic pesticides and maximize productivity.

7 - Bibliography

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