Abstract
Four species of Trichoderma genius (T. harzianum, T. citrinoviride, T. viride and T. asperellum) and Metarhizium anisopliae were assessed for their effects on larval mortality and progeny production of Trogoderma granarium Everts (Coleoptera: Dermestidae). The fungal strains were tested at 2.0 × 106, 2.0 × 107, 2.0 × 108 and 2.0 × 109 spores/kg. The larval mortality of T. granarium was recorded after 7, 14 and 21 days of treatment. The emerged adults (F1) from treated larvae were counted after 30 days of treatment, while F2 and grain weight loss were examined after 80 days of treatment. In general, increasing of spore concentration of all fungal strains enhanced the larval mortality. After 21 of treatment, all fungal strains induced notable larval mortality particularly at the highest concentration (2.0 × 109 spores/kg) except T. viride (19.4%). The highest larval mortality was observed in treatments with M. anisopliae (82.1%) and T. citrinoviride (69.0%) at 2.0 × 109 spores/kg, respectively. Furthermore, all spore concentrations of tested fungi decreased the emerged adults (F1 and F2) with M. anisopliae, T. citrinoviride and T. harzianum being the most potent, particularly at 2.0 × 109 spores/kg. After 80 days, M. anisopliae and T. citrinoviride at 2.0 × 109 spores/kg induced the highest protection of wheat grains against larvae of T. granarium with weight loss of 0.7 and 1.3%, respectively. The outcomes of the present study indicate that the two fungi, M. anisopliae and T. citrinoviride are highly effective seed protectants against T. granarium and could be applied in the integrated pest management programs (IPM) of khapra beetle as effective biological control agents.
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Introduction
Cereal crops, such as wheat, barley and rice are important grain crops in Egypt as well as different regions of the world (Matouk et al. 2017). The khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae) is one of the most destructive primary insect pests of stored cereal and other grain crops in tropical and subtropical zones (Barzin et al. 2019; Kavallieratos et al. 2019). Larvae of khapra beetle feed on whole and broken grains causing a huge loss in weight, germination, and quality of infested cereal grains, particularly at heavy infestation (Rajput et al. 2015; Athanassiou et al. 2019). The control of khapra beetle is currently based mainly on the use of chemical insecticides (Kavallieratos et al. 2017; Kavallieratos and Boukouvala 2018). The continuous application of chemical insecticides for the control of stored products insects induced high risks on the environment, and human and animal health (Karanastasi et al. 2020). Hence, alternative control methods have been applied for management of khapra beetle, such as bioinsecticides, modified atmospheres, essential oils and entomopathogenic fungi (Vassilakos et al. 2019; Kavallieratos et al. 2020; Ali et al. 2022; Iqbal et al. 2022).
Entomopathogenic fungi are biological control agents and a useful tool in the integrated pest management systems of many insect pests (Skinner et al. 2014). This biological control method could be a promising alternative for the control of stored product pests owing to its several properties and advantages, such as compatibility with dry conditions in grain storage systems, broad spectrum of insect hosts, mass-production on industrial scale, simple application techniques, relative safety for humans, animals and the environment as well as no toxic residues on treated stored products (Rumbos and Athanassiou 2017; Batta and Kavallieratos 2018). Recently, the entomopathogenic fungi, such as Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metschnikoff) Sorokin have been applied in the integrated pest management strategies of stored product insects attacking wheat, maize and rice either alone or in combination with other methods (Riasat et al. 2011; Luz et al. 2012; Wakil et al. 2015; Rumbos and Athanassiou 2017; Ak 2019; Mehdi and Al-Fadili 2021). Zidan (2014) found that treatment of stored wheat with the combinations of diatomaceous earth or spinosad with B. bassiana or M. anisopliae increased the mortality of Sitophilus oryzae compared with their application alone. Ak (2019) showed that treatment of wheat grains with B. bassiana and M. anisopliae at 1 × 108 conidia/ml caused 93.7 and 90.4% adult mortality of S. oryzae, respectively, after 7 days of treatment. Rizwan et al. (2019) concluded that the application of B. bassiana (1 × 108 conidia/kg) combined with diatomaceous earth (400 mg/kg) on wheat grains was highly effective against Tribolium castaneum (Herbst) and caused 88.13% mortality after 21 day exposure.
The fungal strains of Trichoderma spp. are broadly recognized as biological control agents applied against many plant diseases and pathogens (Fiorentino et al. 2018; Poveda 2021). Despite of many of Trichoderma spp. have been applied as safe method for the control of stored product insect pests (Rodríguez-Gonzalez et al. 2018; Gad et al. 2020a, b, 2021; Abdelgaleil et al. 2021) no information is available on effectiveness of Trichoderma spp. against T. granarium. Thus, the current study focuses on the evaluation of the potential of Trichoderma spp. and Metarhizium anisopliae as biocontrol agents against T. granarium on stored wheat grains under laboratory conditions. The effects of four strains of Trichoderma spp. (T. harzianum, T. citrinoviride, T. viride and T. asperellum) and M. anisopliae on mortality of larvae, adult emergence, and weight loss and damage caused by T. granarium on wheat grains were evaluated.
Materials and methods
Insect culture
Stock culture of Trogoderma granarium was obtained from Plant Protection Research Institute, Giza, Egypt. Insect colony has been maintained in our laboratory for several years without exposure to insecticides in glass jars (13 cm diameter × 17 cm height) covered by fine mesh cloth to allow proper ventilation. The insect was reared on whole wheat, var. Giza 168, with 10.9% moisture content under environmental conditions of 30 ± 2 °C, 65 ± 5% r.h. and continuous darkness. The larvae with 2–4 mm size were used in bioassays (Athanassiou et al. 2015; Kavallieratos et al. 2016).
Isolation and identification of Trichoderma spp
Four strains of Trichoderma spp. (T. harzianum, T. citrinoviride, T. viride and T. asperellum) have been isolated from Egyptian soil using serial dilution technique according to Naher et al. (2019). Mixture containing 10 g soil samples and 100 ml sterilized distilled water (SDW) was shaken at 100 rpm for 10 min. using a rotary shaker. Then, serial dilution of soil suspension was carried out to isolate Trichoderma spp colonies. Soil suspension (1 ml) was added to 10 ml of SDW to prepare a dilution of 10− 1. Subsequent dilutions (10− 2, 10− 3, 10− 4 and 10− 5) were prepared by mixing 1 ml of each solution with 9 ml SDW. Then, 1 ml from each dilution was transferred to sterilized petri plates containing Rose Bengal Agar (RBA) medium (Khang et al. 2013) and incubated for 5–7 days at 25 ± 2ºC. The plates were observed daily and the emerged colonies were taken and further purified on potato dextrose agar (PDA). The PDA slants were prepared from pure cultures and kept at 4 ºC. Morphological properties (conidiophore branching patterns, phialide arrangement, and conidia shape and size) (Gams and Bissett 1998; Kumar and Sharma 2011) were taken as criteria for the identification of the four strains of Trichoderma spp.
Isolation and propagation of M. Anisopliae
White grubs, Pentodon bispinosus Kuster, larvae have been collected from Golf playground, Katameya, Cairo, Egypt and used as a source for isolation M. anisopliae fungus. A solution of sodium hypochlorite (2%) was used for sterilization of the surface of dead larvae. After rinsing twice with SDW and drying water, larvae were placed on Petri plates containing PDA supplemented with streptomycin sulfate at concentration of 100 µg ml− 1. The plates were incubated at 25 ± 2 °C. The emerged fungal hyphae and sporulation were sub-cultured by moving to new PDA plates and kept for 15 days at 25 ± 2 °C (Ayala-Zermeño et al. 2015). The PDA slants of pure cultures were kept at 4 ºC until use.
Preparation of fungal spore suspensions
To the growing cultures of fungal strains on PDA, 10 ml of SDW containing Tween-80 (0.01%) in was added to the surface of each Petri dish plate. The spore suspension was collected in a sterile glass vial (50 ml) after rubbing the surface of the medium with a glass rod. The resulting spore suspension was vortexed for 5 min and filtrated through a layer of sterilized cheese cloth. Spore concentrations of 2.0 × 106, 2.0 × 107, 2.0 × 108and 2.0 × 109 spores/ml were prepared with aid of a haemocytometer and used in the bioassay experiments.
Bioassays
Efficacy of four strains of Trichoderma spp. and M. anisopliae were evaluated against larvae of T. granarium by admixing with whole wheat grains (Gad et al. 2020b). The concentrations of Trichoderma spp. and M. anisopliae were prepared in distilled water. The fungal strains were assessed at 2.0 × 106, 2.0 × 107, 2.0 × 108 and 2.0 × 109 spores/kg (Abdelgaleil et al. 2021). Fifty grams of the sterilized wheat grains (var. Giza 168 with 10.9% moisture content) were placed in each glass jar (400 ml). Fungal spores (1 ml) were uniformly mixed with 50 g wheat grains inside each jar to give final concentrations of 2.0 × 106, 2.0 × 107, 2.0 × 108 and 2.0 × 109 spores/kg. After mixing with wheat grains, jars were shaken for 2 min for a complete distribution of the fungal spores throughout the grain mass. In the control jars, 1 ml of distilled water was homogeneously distributed on wheat grains in each jar. Afterward, forty T. granarium larvae were introduced in each jar. Three replicates of each concentration and control were used. All treatments were reserved under environmental conditions of 26 ± 2 °C and 65 ± 5% r.h. The percentages of larval mortality of T. granarium were calculated after 7, 14 and 21 days after treatment. On the other hand, the larvae exposed to wheat grains treated with different concentrations of tested fungal spores were examined daily until complete adult emergence and the numbers of emerged adults were calculated and termed as F1 progeny production. Then, the jars were kept under the same rearing conditions for another 50 days and the number of emerged adults were recorded and expressed as F2 progeny production after 80 days. The reduction (%) in the number of progeny was calculated using the following equation:
% = (1 ˗ x/y) × 100.
where x = the number of adults emerging in the treatment; y = the number of adults emerging in the control.
Then, the treated and untreated wheat grains were sieved and the powders were discarded. The weight of remaining wheat grains in treatments and control was recorded to obtain the weight loss percentages after 80 days. The weight loss percentage was calculated from the following formula:
% weight loss = ((Wu–Wi)/Wu) × 100.
where Wu = weight of uninfested wheat grains; Wi = weight of infested wheat grains of control and treatment (Gad et al. 2020b).
Data analysis
Arcsine transformation of larval mortality and weight loss of wheat grains data was carried out before statistical analysis. Analysis of variance (ANOVA) (Kleinbaum et al. 1998) was run for all data to obtain the differences between treatments using Tukey’s HSD test (Haynes 2013) at a significance level ˂ 0.05 (SPSS, Chicago, IL, USA).
Results
Effect of fungal spores on larval mortality of T. granarium
The effects of different concentrations of fungal spores of Trichoderma spp. and M. anisopliae on the mortality of T. granarium larvae are present in Tables 1, 2 and 3. The results show that the larval mortality of T. granarium was significantly increased with increasing the concentration of fungal spores and exposure period. The highest larval mortality of T. granarium was obtained at concentration 2.0 × 109 spores/kg of T. citrinoviride (34.6%), followed by M. anisopliae (33.8%), T. harzianum (23.2%), T. asperellum (20.4%) and T. viride (12.9%) after 7 days of exposure (Table 1). At the highest tested concentration (2.0 × 109 spores/kg), M. anisopliae (75.8 and 82.1%) induced the highest rate of larval mortality, followed by T. citrinoviride (62.6 and 69.0%), T. asperellum (46.3 and 57.1%), T. harzianum (38.6 and 46.3%) and T. viride (17.8 and 19.4%) after 14 days and 21 days of treatment, respectively (Tables 2 and 3).
Effect of fungal spores on progeny production of T. granarium
Treatment of wheat grains with different fungal spore concentrations of Trichoderma spp. and M. anisopliae decreased emerged adults (F1) of T. granarium (Table 4). The number of emerged adults in control was 40.6 ± 4.1. The fungal strains (M. anisopliae and T. citrinoviride) induced the highest reduction in F1 progeny at all tested concentrations. The maximum reduction of T. granarium adult F1 progeny was recorded at concentration of 2.0 × 109 spores/kg of M. anisopliae (5.6 ± 1.4), followed by T. citrinoviride (10.0 ± 2.2), T. harzianum (16.6 ± 1.0), T. asperellum (18.3 ± 1.6) and T. viride (27.3 ± 0.6). After 80 days of exposure, all fungal strains at the spore concentrations of 2.0 × 107, 2.0 × 108 and 2.0 × 109 spores/kg significantly inhibited adult progeny (F2) compared with control treatment (867.0 ± 37.9) (Table 5). The highest suppression of T. granarium F2 was observed in the treatment with M. anisopliae (19.0 ± 0.4) at concentration 2.0 × 109 spores/kg, followed by T. citrinoviride (24.0 ± 2.8), T. harzianum (145.3 ± 8.8), T. asperellum (306.7 ± 18.0) and T. viride (374.6 ± 17.7) at the same concentration.
Effect of fungal spores on weight loss of wheat grains
The results indicated that the untreated wheat grains (control) infested with larvae of T. granarium were significantly more damaged than treated wheat grains with spores of different fungal strains. The percentage of weight loss in untreated wheat grains was 54.3% after 80 days of exposure (Table 6). Weight loss and damage of wheat grains caused by T. granarium were gradually declined with the increase of spore concentration. At the concentration of 2.0 × 109 spores/kg, M. anisopliae and T. citrinoviride were the most effective fungi for the protection of wheat grains against damage caused by T. granarium with the lowest weight loss of 0.7 and 1.3%, respectively, followed by T. harzianum (7.6%), T. asperellum (18.2%) and T. viride (32.2%).
Discussion
The insecticidal efficacy of different entomopathogenic fungi on some stored grain insects including T. granarium has been evaluated by several researchers (Khashaveh et al. 2011; Gad et al. 2020a, b; Abdelgaleil et al. 2021; Mehdi and Al-Fadili 2021; Iqbal et al. 2022; Shahbazi et al. 2022). Nevertheless, this is the first study describing insecticidal efficacy of three strains of Trichoderma (T. citrinoviride, T. viride and T. asperellum against larvae of T. granarium in stored wheat grains. Our results demonstrate that the larval mortality of T. granarium increased with the increase of spore concentration of all fungal strains. After 21 days of treatment, all fungal strains caused notable larval mortality particularly at the highest concentration (2.0 × 109 spores/kg) except T. viride. The highest level of larval mortality was achieved at the highest concentration (2.0 × 109 spores/kg) of M. anisopliae and T. citrinoviride. It was also clear that larvae of T. granarium were more susceptible to M. anisopliae and T. citrinoviride than other tested fungal strains. These findings are matched with previous studies demonstrating that the fungal strains had the ability to induce high rate of larval and adult mortality of several stored grain insects. For example, Gad et al. (2020a, b) indicated that the treatment with T. harzianum at concentration of 2.1 × 107 spores/kg induced 57.3% mortality of (A) obtectus adults after 7 days and 68.0% mortality of S. oryzae adults after 21 days. The same fungus has been tested against the C. maculatus and C. chinensis adults and the mortality percentages were 75.2 and 76.4%, respectively at concentration of 1.0 × 107 spores/kg, after 7 days of exposure (Abdelgaleil et al. 2021). Mehdi and Al-Fadili (2021) found that the larval mortalities of T. granarium were 86.67 and 50% when larvae treated with 1.0 × 109 conidia/ml of local and imported isolates of M. anisopliae respectively, and 86.67 and 66.67% when larvae treated with 1.0 × 109 of local and imported isolates of (B) bassiana respectively after 14 days. Iqbal et al. (2022) tested M. anisopliae against larvae of T. granarium and found that the fungal strain at concentration of 1.0 × 108 conidia/ml caused larval mortality of 98.3% after 14 days.
Our results demonstrate that the tested entomopathogenic fungi might be valuable for the biological control of khapra beetle particularly M. anisopliae and T. citrinoviride, because of their capability to penetrate the insect cuticle and use the insect bodies as source of nutrients for growth and propagation (Gonzalez et al. 2020; Iqbal et al. 2022). The insect mortality may also due to secondary metabolites produced by fungal strains, such as peptaibols which have been reported to be produced by T. harzianum and showed pronounced insect toxicity (Charnley and Collins 2007; Shakeri and Foster 2007; Rahim and Iqbal 2019). Similarly, antifeeding properties of natural compounds isolated from fungal strains of T. citrinoviride have been described against Corcyra cephalonica and Schizaphis graminum (Evidente et al. 2008; Vijayakumar et al. 2016; Vijayakumar and Alagar 2017).
Our results also indicate that all treatments with spore concentrations of tested fungi reduced the adult F1 and F2 production of T. granarium after 80 days of exposure. Moreover, adult F1 and F2 production of T. granarium was highly suppressed at the highest tested concentration (2.0 × 109 spores/kg) of M. anisopliae, T. citrinoviride and T. harzianum. Several reports explained the effect of different spore concentrations of tested fungal strains on the reduction of the progeny of stored product insects. For instance, Wakil et al. (2015) found that concentration of 2.78 × 106 conidia/kg of M. anisopliae reduced progeny of S. oryzae 3-fold in comparison with untreated rice grains after 62 days. Gad et al. (2020a, b) showed that concentration of 2.1 × 107 spores/kg of T. harzianum induced strong suppression of A. obtectus progeny (94.5%) after 60 days of exposure and reduced progeny of S. oryzae (101.3 ± 4.9 beetles), compared with untreated wheat grains (516.0 ± 2.8 beetles) after 90 days. Abdelgaleil et al. (2021) stated that concentration of 1.0 × 107 spores/kg of T. harzianum reduced progeny of C. chinensis (69.1%) after 45 days. The high suppression of progeny of T. granarium for two generations observed in this study may be due to the quick death of larvae after treatments or to the adverse effect of these tested fungal strains on eggs and newly hatched neonate larvae (Athanassiou et al. 2005). Also, the highest concentration of tested fungi was highly effective to protect wheat grains against damage caused by T. granarium. The two fungi, M. anisopliae and T. citrinoviride, displayed the highest potential to protect weight loss of 0.7 and 1.3% after 80 days, respectively. Similarly, the tested fungi have been proved to be effective to protect stored commodities against the damage induced by other insect species (Padin et al. 2002; Rodríguez-Gonzalez et al. 2020; Gad et al. 2020a, b, 2021; Abdelgaleil et al. 2021).
Although the biological control agents may not be as efficient as chemical insecticides the use of entomopathogenic fungi for the management of stored product insects is very important approach to reduce environmental pollution, food contamination and delay the development of insect resistance. The results of the present study encourage the use of entomopathogenic fungi in integrated pest management programs for the control of khapra beetle. In this regard, a combination of virulent fungal isolates with low concentrations of insecticides may also be advantageous for practical use against stored grain insect pests. Taking into account most of insecticides used for the management of stored product insects showed week effectiveness against T. granarium at the recommend rates. The results of current study show that Trichoderma spp. and M. anisopliae are highly effective as grain protectants against damage caused by of T. granarium and may offer a solution for the feasible management of T. granarium in stored wheat.
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Hassuba, M.M., Gad, H.A., Atta, A.A. et al. Efficacy of entomopathogenic fungi for the management of Trogoderma granarium Everts on wheat grains. Int J Trop Insect Sci (2024). https://doi.org/10.1007/s42690-024-01253-1
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DOI: https://doi.org/10.1007/s42690-024-01253-1