Application of Beauveria bassiana using different baits for the control of grasshopper pest Dichroplus maculipennis under field cage conditions

1 Introduction

The univoltine and polyphagous grasshopper Dichroplus maculipennis (Blanchard) (Orthoptera: Acrididae) is a widely distributed species, occurring in Brazil, Argentina, Chile and Uruguay (Carbonell et al., 2017). It is also one of the most damaging grasshoppers in Argentina, particularly in large areas of the Pampas and Patagonia regions (Mariottini et al., 2013; Cigliano et al., 2014). From late 2008 through early 2011 a major outbreak of D. maculipennis occurred in the southern Pampas. Densities reached up to 75 individuals per m², swarm-like aggregative dispersal flights were observed, and crops (corn, soybean, sorghum, wheat, barley, alfalfa, wheat-grass, ray-grass, clover) and natural grasslands in an area of approximately 2.5 million ha were affected (Mariottini et al., 2012). Currently, chemical insecticides are the only option for the control of D. maculipennis but the use of these chemicals pollutes the environment and brings great problems in the health of farmers (Álvarez et al., 2013). The requirement for nonchemical alternatives has become increasingly important in recent years (Foster et al., 2010). Beauveria bassiana (Balsamo-Crivelli) Vuillemin s.l. is commonly used for the biological control of insect pests of agricultural crops (Jaronski, 2010; Vega et al., 2012). Insecticidal baits have been used for the control of acridid pests worldwide for more than a century. Baits are used on a regular basis in North America to control rangeland grasshoppers and Mormon crickets (Anabrus simplex Haldeman, Orthoptera: Tettigoniidae) (Latchininsky et al., 2007). A typical bait of these formulations consists of wheat bran or other solid carrier impregnated with a chemical or biological insecticide. An advantage of using baits might be protection of the fungal pathogen from degradation due to UV light and/or other environmental factors. Adding attractants and phagostimulants could result in improved bait formulations, making bait treatment even more efficacious (Latchininsky and VanDyke, 2006). Vegetable oils have kairomonal attractant properties for grasshoppers primarily due to the presence of linoleic and linolenic fatty acids (Bomar and Lockwood, 1994a). These fatty acids are dietary essentials for grasshoppers and, once volatilized, can be detected by the insects’ olfactory chemical-receptors (Bomar and Lockwood, 1994b). Due to the presence of fatty acids, certain vegetable oils used as insecticide carriers, can function as liquid baits, and markedly enhance the efficacy of grasshopper control programs (Lockwood et al., 2001; Latchininsky et al., 2007). The aim of this study was to determine, under laboratory bioassay and field cage conditions, the most effective treatment option (spray or bait) with the entomopathogenic fungus B. bassiana, for the control of the grasshopper pest D. maculipennis. The objectives were: 1) evaluate three B. bassiana strains for potential use against D. maculipennis nymphs; 2) compare spray and bait formulations of each B. bassiana strains against D. maculipennis nymphs in laboratory bioassays; and 3) evaluate spray and bait formulations of the B. bassiana strain that performed best in laboratory bioassays under field cage conditions against D. maculipennis nymphs.

2 Materials and methods

3 Results

In the laboratory bioassays was observed significant differences (df = 11; f = 2.23; p < 0.01) in the percentages of mortality against third-instar nymphs of D. maculipennis caused by the strains of B. bassiana, as well as between the treatments assessed. Was observed that isolate LPSc 1227 caused the highest mortality at each treatments tested, ranging from 93.3% in the treatment 1 (conidia only) to 100% in the treatments 2 (Wheat bran with conidia) and 3 (Canola oil, wheat bran, and conidia) (Fig. 1). On the other hand, the strain LPSc 1226 caused lower mortality, at each treatment tested, ranging from 73.3% in treatment 3 (Canola oil with conidia) to 100% in treatment 4 (Canola oil, wheat bran, and conidia) (Fig. 1). In the laboratory bioassays the MST all three strains in the treatment 1 (conidia only), showed that LPSc 1227 was the most virulent with values of 6 d while the least virulent isolate was LPSc 1226 with 8 d (Table 1). Moreover, the lower value of MST was obtained with the combination LPSc 1227 conidia-wheat bran plus canola oil (3.2 d) and the highest MST was observed in the combination LPSc 1226 conidia plus wheat bran (7.9 d) (Table 3). Under field cage conditions, significant differences were observed (df = 3; f = 328.67; p < 0.0001) in percentages of mortality against third-instar nymphs of D. maculipennis caused by LPSc 1227 strain of B. bassiana between the different treatments. The highest mortality was 100% in treatment 3 (canola oil, wheat bran, and conidia) and the lowest was 73.3 ± 2.2% in treatment 1 (conidia only) (Fig. 2). In the field cage trial, the lowest value of MST was obtained with the combination LPSc 1227conidia plus wheat bran and canola oil (6.4 d), and the highest MST was in treatment 1 (conidia only) at 8.3 d. Intermediate values of MST were observed with the combination LPSc 1227-wheat bran at 7.4 d and with LPSc 1227-canola oil at 7 d. No mortality was observed in the control (treatments 5), either in laboratory bioassays as in the field cage trial.

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Fig. 1

Cumulative mortality (%) ± SE of third-instar Dichroplus maculipennis nymphs within 10 days after infection with 1 × 10⁸ conidia/ml of Beauveria bassiana strains (LPSc 1225; LPSc 1226 and LPSc 1227) under laboratory conditions. Different letters denote significant differences between Beauveria bassiana strains in the same treatment, according to the Tukey test (p < 0.05).

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Fig. 2

Cumulative mortality (%) ± SE of third-instar Dichroplus maculipennis nymphs within 15 days after infection with 1 × 10⁸ conidia/ml of LPSc 1227 Beauveria bassiana strain, under cage field conditions. Different letters denote significant differences between treatments, according to the Tukey test (p < 0.05).

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4 Discussion

In this work, we found that in the laboratory bioassays and under field cage conditions the combination of conidia of all three B. bassiana strains with wheat bran and canola oil improved the performance of conidia, enhancing mortality of D. maculipennis nymphs. In addition, we observed a reduction in MST when conidia of the different B. bassiana strains were combined with wheat bran and canola oil. Both canola oil and wheat bran likely provided protection to conidia against UV rays from solar radiation, allowing propagules to remain viable longer and thus causing higher percentage of infection on D. maculipennis nymphs. Studies carried out by Latchininsky et al. (2007) reported that there are certain vegetable oils such as olive, canola, corn, and flax that have phagostimulant properties on nymphs and adults of the North American grasshopper pest Melanoplus sanguinipes (Fabricius). That D. maculipennis nymphs were attracted to wheat bran baits impregnated with canola oil in our tests both in the laboratory and under field cage conditions would agree with Latchininky’s reports for M. sanguinipes in light of the relatively close phylogenetic relationship between melanoplines of genera Melanoplus and Dichroplus (Song et al., 2018). The use of poisoned baits with different chemical insecticides for the control of species of grasshopper pests is not a novelty (Onsager et al., 1980; Erickson and Onsager, 1981; Cowan, 1990). In the USA they have been used extensively and frequently, including as the main control mechanism of the once most noxious and now possibly extinct grasshopper Melanoplus spretus. To control this grasshopper pest and others, the bait called “Criddle mixture” was widely used (3000 t over 500.000 ha in Kansas alone in 1917; Lockwood, 2004), which was manufactured with dry horse dung and then sprayed with chemical insecticides. Baits are already being used successfully since 1980 successfully for standard application of spores of the long-term biocontrol agent of grasshoppers Paranosema locustae (Microsporidia) (Solter et al., 2012; Bjornson and Oi, 2014; Lange and Sokolova, 2017) and have been also employed for small experimental applications of Malameba locustae (Rhizopoda) (Lange and Lord, 2012). On the contrary, a work of Foster et al. (2010) showed that the use of baits with conidia of B. bassiana and Metarhizium brunneum Petch used for the control of the Mormon cricket Anabrus simplex (Haldeman), did not yield satisfactory results. One possible explanation for this result could have been that these baits were sprayed with paraffin oil instead of a vegetable oil such as olive or canola, rendering them less palatable. In several studies carried out under field conditions, in which entomopathogenic fungi were used for the control of acridid species, the mortality percentages obtained ranged between 70 and 90% after 9–20 d (Lomer et al., 2001; Magalhães et al., 2000; Peng et al., 2008; Keyser et al., 2017). In this work, we observed the highest mortality and the lowest MST values, both in the laboratory tests and those performed under field cage conditions.

5 Conclusions

In this work it was demonstrated that the combination of canola oil with wheat bran makes the bait poisoned with conidia of B. bassiana more palatable for nymphs of D. maculipennis. This was reflected in the higher mortality and lower MST values for this species of grasshoppers pest, both in laboratory bioassays and those carried out under field cage conditions. Furthermore, the use of this kind of bait has an important advantage respecting to the conventional application (spray), as biological insecticides are commonly applied under field conditions. This advantage is due to wheat bran protects the conidia of the entomopathogenic fungus from the direct action of radiation UV, and also, the canola oil, allows the conidia to stay hydrated for a more time, allowing it to maintaining its pathogenicity for more time. Although it would be necessary to make a thorough evaluation of the economic costs involved in the production of this type of bait for the control of D. maculipennis, we think that it could be a viable alternative that may contribute to minimize as much as possible the current use of chemical insecticides.