Peanut red mite Tetranychus ogmophallos Ferreira & Flechtmann (Acari: Tetranychidae) is considered an important emergent pest in Brazil because it causes economic and environmental losses (Lourenção et al. 2001; Melville 2015). This mite is found only on Arachis spp. plants in Brazil; therefore, it has quarantine importance for many countries (Bonato et al. 2000; Migeon & Dokeld 2007).

Tetranychus ogmophallos causes reduction in the productivity of peanut, Arachis hypogaea L. (Fabaceae), and when infestation occurs in the early crop stages, it may cause plant death (Melville 2015). This mite also causes damage in forage peanut, Arachis pintoi Krapov. & W.C. Gregory (Fabaceae), used as an ornamental plant and for animal feed (Ferreira & Flechtmann 1997). Bonato et al. (2000) verified that T. ogmophallos survived in the laboratory on a diet of bean leaves and soybeans plants. In addition, T. ogmophallos fertility was higher on a diet of bean leaves compared to peanut leaves.

In recent years, several T. ogmophallos outbreaks have been observed in peanut producing areas in the state of São Paulo, Brazil, which produces approximately 90% of the national peanut production (IBGE 2016). Several factors are identified as responsible for outbreaks, such as the banning of some broad spectrum insecticides and acaricides, frequent dry spells, use of new varieties with characteristics that may favor the development of mite populations, and the hormesis effect caused by new pesticides (Guedes & Cutler 2014; Guedes et al. 2016).

Applications of acaricides to reduce peanut red mite populations in peanuts crops have been the only mite control measure used. However, this strategy has caused great negative impact on environment and human health (Guedes et al. 2016). As an alternative to synthetic pesticides, fungal entomopathogens are considered to be potential agents to control mite populations. For example, Chandler et al. (2000) collected records of 58 fungal species infecting at least 73 mite species. Among fungal entomopathogens, Beauveria bassiana (Balsamo) Vuillemin (Cordycipitaceae) and Metarhizium anisopliae (Metschnikof) Sorokin (Clavicipitaceae) species stand out (Oliveira et al. 2004; Lacey 2017; Moro et al. 2011). To date, few pathogens have been developed as commercial acaricides due to mass production issues or poor performance under field conditions (Arthurs & Bruck 2017).

Numerous mite species, including tetranychids, are infected by entomopathogenic fungi, predominantly Entomophthorales (e.g., Neozygites floridana) and Hypocreales (e.g., B. bassiana, Isaria spp. (formerly Paecilomyces), M. anisopliae, Hirsutella thompsonii (Fischer), Cladosporium cladosporioides (Fresen), Cephalosporium diversiphialidum Balazy, and Lecanicillium lecanii species (Zimmermann) [formerly Verticillium lecanii (Zimmermann)]) (Chandler et al. 2000; Barreto et al. 2004; Oliveira et al. 2004; Maketon et al. 2008; Bugeme et al. 2009; Moro et al. 2011; Sanjaya et al. 2013; Geroh et al. 2015; Lacey 2017; Nakai & Lacey 2017).

Beauveria bassiana and M. anisopliae caused between 22 and 82% mortality among adult Tetranychus evansi Baker and Pritchard (Prostigmata: Tetranychidae) females under laboratory conditions (Bugeme et al. 2008; Wekesa et al. 2005). Both entomopathogens cause > 65% mortality among Tetranychus urticae (Koch) (Acari: Tetranychidae), which is a very important agricultural pest in Brazil (Alves et al. 2002; Tamai et al. 2002; Bugeme et al. 2009; Shi & Feng 2009; Moro et al. 2011; Cerqueira et al. 2017). Six B. bassiana isolates and 7 M. anisopliae isolates were pathogenic to Tetranychus kanzawai (Kishida) (Acari: Tetranychidae), causing > 85% mortality under laboratory conditions, evidencing high potential as a biological control agent (Sanjaya et al. 2013).

The use of fungal entomopathogens for the control of phytophagous mites is restricted to a few species (Lacey 2017), and there are no known reports of fungal entomopathogens for control of T. ogmophallos. Thus, the purpose of this study was to evaluate the susceptibility of T. ogmophallos to B. bassiana and M. anisopliae under laboratory and greenhouse conditions.

Material and Methods

Results

For both fungal entomopathogens, a gradual reduction in the percentage of adult T. ogmophallos females was observed throughout the study period at laboratory conditions. On the first d after application, a significant reduction in the number of surviving mites in treatments with fungal entomopathogens was observed, when compared to the control (F = 76.05; df = 2,27; P < 0.05), represented by 28.3 and 15.9% of individuals surviving in treatments with M. anisopliae and B. bassiana, respectively (Fig. 1).

At 3 d after applications, the percentage of surviving adult T. ogmophallos females was 13.1 and 3.4% for treatments with application of M. anisopliae and B. bassiana, respectively, significantly differing from control (F = 170.08; df = 2,27; P < 0.05) (Fig. 1). The same situation was observed at 5 d after applications (F = 562.27; df = 2,27; P < 0.05), where survival of tetranychids was 5.1% (M. anisopliae) and 2.7% (B. bassiana) (F = 404.18, df = 2.27, P < 0.05), with survival of 3.9% of adult females for treatment with M. anisopliae and total mortality for B. bassiana (Fig. 1).

Regarding the efficacy of fungal entomopathogens in the greenhouse on T. ogmophallos, control efficacy of 68.41 and 68.68% was observed at 5 d after applications for B. bassiana and M. anisopliae, respectively (Fig. 2A). At 10 d after applications, control efficacy increased to 83.86% (B. bassiana) and 92.18% (M. anisopliae) (Fig. 2B); however, control efficacy decreased to 71.82% (B. bassiana) and 59.34% (M. anisopliae) at 15 d after applications (Fig. 2C).

The population density of T. ogmophallos on peanut plants, under greenhouse conditions, at 5 d after application was not significantly different when fenpyroximate (synthetic acaricide) and fungal entomopathogen treatments were compared (Fig. 2A). There was a significant difference between the treatments with chemical acaricide and the negative control with water + adjuvant (Fig. 2A) (F = 10.48; df = 3,36; P < 0.05).

Fig. 1.

Survival (%) (± SE) of adult Tetranychus ogmophallos females 1, 3, 5, and 7 d after application for treatments with Beauveria bassiana and Metarhizium anisopliae at laboratory conditions. Values within a time interval topped by the same letter did not differ significantly from each other by the Tukey test (P < 0.05). Error bar corresponds to the standard error (± SE).

Fig. 2.

Mean number (± SE) of Tetranychus ogmophallos on peanut leaves 5 (A), 10 (B), and 15 (C) d after application. Values within a time interval topped by the same letter did not differ significantly from each other by the Tukey test (P < 0.05). Error bar corresponds to the standard error (± SE).

At 10 d after applications, a reduction in the number of T. ogmophallos was observed in treatments with entomopathogens, significantly differing from the other treatments (F = 30.61; df = 3,36; P < 0.05). In this evaluation, the number of mites per plant in treatments with B. bassiana and M. anisopliae was 68.3 ± 26.1 mites per plant and 33.1 ± 12.3 mites per plant, respectively. There were increases in mite densities at 15 d after applications in treatments with microorganisms; however, the mite densities were significantly lower compared to the negative control (F = 50.6; df = 3,36; P < 0.05) (Fig. 2C). In this evaluation, there were 201.2 ± 29.6 mites per plant in the treatment with B. bassiana and 290.3 ± 42.2 mites per plant in the treatment with M. anisopliae. In the treatment with fenpyroximate, no mites were found on plants at evaluations performed at 10 and 15 d after applications (Figs. 2B, C).

At 5 d after application, the miticide treatments were affected by plant stratum, with fewer mites present in the upper region of the plant. However, at this time there were no significant differences among the miticide treatments. At 10 d after application, possibly due to the drastic population reduction in all treatments, no difference in the number of mites per plant stratum was observed (Table 1). At 15 d after applications, B. bassiana displayed better control in the lower stratum, but M. anisopliae did not differ from the negative control in the lower stratum. In the upper region of the plant, the result was opposite to that observed in the lower stratum, as evidenced by the low population density of T. ogmophallos in the M. anisopliae treatment (Table 1).

Table 1.

Mean number (± SE) of Tetranychus ogmophallos in the lower and upper regions of peanut plants 5, 10, and 15 d after application (DAA).

Discussion

Beauveria bassiana and M. anisopliae were pathogenic to T. ogmophallos, which is the first report on the pathogenicity of these fungi to this mite species. Other studies also have reported the pathogenicity of B. bassiana and M. anisopliae to tetranychid species, such as T. urticae (Alves et al. 2002; Tamai et al. 2002; Shi & Feng 2009; Moro et al. 2011), T. evansi (Wekesa et al. 2005), T. kanzawai (Sanjaya et al. 2013), Mononychellus tanajoa (Bondar) (Acari: Tetranychidae) (Barreto et al. 2004), and Oligonychus yothersi (McGregor) (Acari: Tetranychidae) (Oliveira et al. 2002, 2004).

The high mortality of T. ogmophallos females observed for all treatments (Fig. 1) may be related to the concentration of the conidial suspensions used (Alves et al. 2002). At concentrations of 105, 106, and 107 conidia per mL of B. bassiana, aiming to control adult T. urticae females under laboratory conditions, Alves et al. (2002) observed mortality below 45.0%, while at concentration of 108 conidia per mL, the mortality rate of these tetranychids was 74.4%. Geroh et al. (2015) also observed a lower number of individuals surviving the use of more concentrated B. bassiana conidia suspensions, with mortality of T. urticae adults ranging from 45.6 to 91.0% using concentrations between 105 and 1012 conidia per mL.

The methodology used also should be considered an important point in relation to values found for the survival rate of T. ogmophallos. According to Geroh et al. (2015), the application of an entomopathogen directly on mites was more reliable in assessing potential mortality of T. urticae when compared to treatment of food.

Relative to plant strata, there were not many differences in the effectiveness of the entomopathognes for the first 10 d after treatment. After 15 d, B. bassiana was more effective in the lower stratum (as compared to M. anisopliae) (Table 1). In tomato cultivation under greenhouse conditions, Wekesa et al. (2005) observed that B. bassiana was efficient in controlling T. evansi in the upper and lower strata of plants, when compared to treatments with M. anisopliae at 7 and 14 d after applications. Stratum-specific responses may be due to the variation in moisture and temperature throughout the canopy of plants. For example, Shi & Feng (2009) evaluated 2 B. bassiana and 2 M. anisopliae isolates for spider mites in cotton in China and obtained desirable control over a period of 30 to 35 d with efficacy > 80%. High humidity in the canopy and moderate daily mean temperatures were advantageous to control.

This mite has caused many problems for forage peanut, which is used for animal feed (Ferreira & Flechtmann 1997; Santos 2016). Biological control with fungal entomopathogens may prove to be a useful tool to control T. ogmophallos in forages because the use of fungal entomopathogens presents minimal risks to human and animal health when compared to the use of synthetic pesticides (Zimmerman 2007; Hu et al. 2016).

The results of our research indicate that both entomopathogenic fungi have potential for managing T. ogmophallos in peanut crop. However, bioassays in the field are required to prove the real potential of these entomopathogens. In the field, the entomopathogenic fungi may be influenced by abiotic factors, principally temperature, relative humidity, and solar radiation, which may affect the development and reproductive parameters of these microorganisms (Bugeme et al. 2008; Oliveira et al. 2016).

The time of spraying entomopathogenic fungi also is a limiting factor for use of these microorganisms in the field to control the genus Tetranychus. High temperature and low relative humidity may be responsible for the failure of microbial control with entomopathogenic fungi. In the state of São Paulo, Brazil, the peanut crop is cultivated in the summer season, with medium temperature and high relative humidity, which makes it possible to use the formulated products based on M. anisopliae and B. bassiana, with the recommendation to spray in the evening, at temperatures between 25 to 35 °C and relative humidity of 60% (Koppert 2018a, b).