Formulations of Beauveria bassiana MABb1 and mesoporous materials for the biological control of Sphenarium purpurascens in maize crops from Puebla, Mexico

Highlights

• A native strain of Beauveria bassiana was evaluated against Sphenarium purpurascens.

• In vitro and in situ assessment produced a significant mortality rate in the grasshopper.

• The yields of experimental maize plots showed a significant improvement after B. bassiana treatment.

Abstract

This investigation reports on the biological control of Sphenarium purpurascens by using different concentrations of conidia from a native strain of Beauveria bassiana (MABb1) isolated in Puebla, Mexico under laboratory and in situ conditions. Formulations containing this native strain combined with two mesoporous materials (diatomaceous earth “D” and zeolite “Z”) were assayed in order to determine their effect on the mortality of the grasshopper. Concentrations of 3.67 × 10⁸ to 10.30 × 10⁸ conidia mL⁻¹ caused a substantial mortality rate in the fourth-instar nymphs and adults of S. purpurascens. The observed mortality was directly proportional to the concentration of conidia. Under controlled conditions, the highest specific death rate K(d⁻¹) was 0.78 for the formulation containing Z + D + MABb1 at 72 h post-infection. The formulations of D + MABb1 and Z + D + MABb1 caused a noticeable decrease in the population of grasshoppers in the experimental plots with statistical significant differences (α < 0.05). Interestingly, an increase in the mortality of S purpurascens occurred in July, August and September 2017 when the highest incidence of the grasshopper was recorded. Remarkably, the treatment based on Z + D + MABb1, produced an improvement in the yields of experimental maize plots (7847.4 ± 0.70 Kg ha⁻¹) in comparison to control plots (4453.9 ± 0.50 Kg ha⁻¹). These favorable consequences are reported for the first time in corn crops from Mexico.

Introduction

Grasshoppers (Orthoptera: Acrididae, Romaleidae) are organisms that colonize diverse habitats including tropical and desert areas but, in grasslands, grasshopper reach higher densities mainly because of the geographical conditions and specific vegetation (Bustillos-Rodríguez et al., 2015, Lightfoot, 2018). In Mexico, grasshoppers have become a severe pest in agriculture by negatively affecting the foliage of bean, alfalfa, squash and corn crops (Barrientos-Lozano et al., 2002, Tamayo-Mejía, 2009, Morales-Martínez et al., 2013). Regarding this point, the most relevant pests of maize crops in Mexico are Melanoplus spp., Sphenarium mexicanum and Sphenarium purpurascens (Orthoptera: Pyrgomorphidae). S. purpurascens is the most abundant grasshopper in Mexico and its geographical distribution comprises the central, south and west regions of Mexico, including the provinces of Oaxaca, Guerrero, Michoacán, Jalisco, Veracruz, Puebla, Tlaxcala, Hidalgo, Morelos, Distrito Federal, Estado de México, Chiapas and Tabasco (Cerritos and Cano-Santana, 2007). S. purpurascens is commonly known as the maize grasshopper because of its high incidence in maize crops (Serrano-Limón and Ramos-Elorduy, 1989).

Maize is the most important and emblematic cereal in Mexico. The averaged consumption of maize in Mexico is around 267 g per day which exhibits the relevance of this cereal as elemental food for this country. Currently, an alarming increase of S. purpurascens invasions on corn monocultures in Mexico has been reported (Ranum et al., 2014, Vázquez-Jorge et al., 2016). Specifically, the valley of Puebla-Tlaxcala has experienced the most harmful grasshopper infestation which caused severe damage to the native corn crops affecting grain production (García et al., 2006, Cerritos and Cano-Santana, 2007, Huerta et al., 2014).

The use of organochlorines is one of the most common method for controlling pests of the order Orthoptera. Unfortunately, these insecticides causes collateral damage to the environment while the insects develop a marked resistance (Mujherkee and Madhuban, 1996). Due to this fact, the biological control of this group of organisms has been contemplated as a more sustainable alternative (Vázquez-Jorge et al., 2016). One of the best proposals for pest control is the use of entomopathogenic fungi (Rizwan et al., 2019, Mantzoukas and Panagiotis, 2020). Infections caused by fungi are usually highly specific and dramatically reduce the population of a specific insect; this fact proves that biological insecticides can be a feasible solution for controlling insect pests in agriculture (Barajas et al., 2009). Beauveria bassiana and Metarhizium anisopliae are fungi used as efficient natural insecticides. These organisms infect more than 200 species of insects and mites belonging to several genera of the orders Hemiptera, Lepidoptera, Dermaptera, Hymenoptera, Coleoptera and Orthoptera (Polar et al., 2008). These fungi are also highly effective in controlling S. purpurascens because they are able to penetrate the cuticle of the insect (Huerta et al., 2014). Beauveria bassiana (Bals.) Vuill.is a filamentous entomopathogenic fungus of the division Ascomycota. The fungus shows a fast growing in basic culture media producing white-creamy and/or pale-yellow colonies. The microscopic features of B. bassiana includes septate hypha, small spherical conidia and sinuous conidiophores grouped in whorls (García et al., 2011). B. bassiana has been widely used in pest management and native strains represent a good alternative for the biological control of many grasshopper species (Lord, 2001).

As it is well known, zeolite is a mesoporous material (<2 mm pore diameter), which is constituted by Si and Al (known as T atoms) (De Smedt et al., 2015). Those elements are tetrahedrally linked to oxygen atoms. Due to this physicochemical property, zeolite can be channeled to diverse uses (Curtis and Deem, 2003). Haryadi et al. (1994) demonstrated that natural zeolite can prevent the growth of Sitophilus zeamais (Motsch) whereas Kljajic et al. (2011) suggested that natural zeolite from Serbia can regulate the growth of three beetle species.

On the other hand, diatomaceous earth is constituted by silicon dioxide derived from fossil diatom algae (Cook y Armitagge, 2000). Silicon comprises between 70 and 90% of the total diatom composition and just a little amount of calcium, phosphorous, sulfur, nickel, zinc, manganese, aluminum, iron, magnesium and sodium (Korunic, 1998) are found. Diatomaceous earth is considered as natural insecticide which has been included for the management of pest control in several crops (Korunic, 1997, Arthur, 2004). The use of inert sources such as zeolite and diatomaceous earth which are simultaneously inoffensive for humans and the natural environment has a tremendous impact for pest management (Rouhani et al., 2012, De Smedt et al., 2015).

Considering the utility of fungi in the alternative pest treatment, this work was focused in the evaluation of standardized formulations containing conidia from a native strain of B. bassiana collected in Puebla, México, which was combined with two mesoporous materials as a support (diatomaceous earth and zeolite). The evaluation was carried out under laboratory and in situ conditions in order to determine their effect in the control of S. purpurascens.