Bioscience Journal | 2022 | vol. 38, e38015 | ISSN 1981-3163 1 Salih KARABÖRKLÜ1 1 Department of Plant Protection, Duzce University, Duzce, Turkey. Corresponding author: Salih Karabörklü Email: salihkaraborklu@duzce.edu.tr How to cite: KARABÖRKLÜ, S. Biocontrol potential of Beauveria bassiana and Metarhizium anisopliae isolates from Turkey against Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) larvae under laboratory and field conditions. Bioscience Journal. 2022, 38, e38015. https://doi.org/10.14393/BJ-v38n0a2022-60197 Abstract Hyphantria cunea is one of the most important pest insects causing significant damage in many plant species. The present study aimed to evaluate the insecticidal activity of Turkey isolates of Beauveria bassiana and Metarhizium anisopliae against H. cunea larvae under laboratory and field conditions. B. bassiana isolates YK16, YK23 and YK26, and M. anisopliae isolates YK41 and YK45 were sprayed onto the larvae of H. cunea at the respective doses of 1x105 and 1x106 conidia mL-1 and monitored for seven days. Fungal isolates, bio- insecticide Bacillus thuringiensis and chemical insecticide diflubenzuron were used in field studies. Trials were carried out in five replications. All B. bassiana isolates caused 100% mortality on first instar larvae in laboratory trials. Mortality ratios ranged from 100 to 96% on second instar larvae. M. anisopliae isolates YK45 and YK41 caused 88 and 84%, and 81.33 and 77.11% mortalities for the first and second instar larvae, respectively. The mortality rates fluctuated between 91.78-72.89% for B. bassiana on third instar larvae in laboratory conditions. However, M. anisopliae isolates YK45 and YK41 caused 77.11 and 60.22% mortality on third instar larvae, respectively. In the field trials, B. bassiana YK23 displayed promising insecticidal activity with 80.60% mortality on second instar larvae of H. cunea. Other isolates as well caused mortalities ranging from 60.77 to 49.55%. The results revealed that some isolates of B. bassiana and M. anisopliae have potential to control H. cunea larvae. However, additional detailed studies need to be carried out to increase their effectiveness in field conditions. Keywords: Entomopathogenic Fungi. Fall Webworm. Insecticidal Activity. Microbial Control. Pest Insect. 1. Introduction The fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae), is one of the important pest insects causing significant damages on the green parts of ornamental trees, shrubs plants, orchards and forests (Schowalter and Ring 2017; Wang et al. 2020). The fall webworm spread to Central Europe and East Asia from the North America in the early 1940s (Ge et al. 2019). Currently, H. cunea has been distributed to more than 30 countries in North America, Europe, and Asia and causes serious harms on more than 600 plant species (Lu et al. 2017; Ge et al. 2009). In Turkey, H. cunea bring along significant defoliator effect in hazelnut orchards as well as other orchards, parks, gardens and forests for about half a century. In recent years, H. cunea population showed a serious increase (Gencer et al. 2020). In Turkey, synthetic chemicals with active substances cypermethrin and diflubenzuron, and a microbial bio-insecticides including Bacillus thuringiensis kurstaki (an entomopathogen) are used to control H. cunea population. Entomopathogens are successfully used against many pest insects in biological control programs (Karabörklü et al. 2018). Among BIOCONTROL POTENTIAL OF Beauveria bassiana AND Metarhizium anisopliae ISOLATES FROM TURKEY AGAINST Hyphantria cunea (DRURY) (LEPIDOPTERA: ARCTIIDAE) LARVAE UNDER LABORATORY AND FIELD CONDITIONS https://orcid.org/0000-0003-4737-853X Bioscience Journal | 2022 | vol. 38, e38015 | https://doi.org/10.14393/BJ-v38n0a2022-60197 2 Biocontrol potential of Beauveria bassiana and Metarhizium anisopliae isolates from Turkey against Hyphantria cunea (Drury)… the insect pathogens, entomopathogenic fungi have been also produced commercially and successfully used in controlling pest insects for many years (Wakefield 2018). Their infective and killing abilities offer promising control opportunities in different geographic, climatic, and agro-ecological zones (Lacey et al. 2015). That’s why entomopathogenic fungi offer environmentally friendly alternatives to conventional synthetic chemicals for pest control. Entomopathogenic fungi can cling to the cuticle of insects through the producing infective spores and, penetrating into tissues and hemocoel and kill insects in a very short time by their toxins. Apart from the cuticle, entomopathogenic fungi can also penetrate host through tracheal openings, injured areas, digestive system and other openings (Batta and Kavallieratos 2018; Karabörklü et al. 2019). Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metschnikof) Sorokin are among the most important entomopathogenic fungi. About 80% of the commercial bio-insecticides produced using entomopathogenic fungi are based on the genera of Beauveria and Metarhizium (De Faria and Wraight 2007; Karabörklü et al. 2018; Meyling et al. 2018). Nevertheless, commercial adoption is still hindered by limited field efficacy, sourcing susceptibility to ultraviolet light, low moisture, and difficulties in reaching target pests. However, the endophytic abilities of some genera as Beauveria and Metarhizium against pest insects add a very important advantage to improve their efficacy (Russo et al. 2021). Although many laboratory studies conducted for evaluating the toxicity of B. bassiana and M. anisopliae against H. cunea (Iskender et al. 2012; Zibaee et al. 2013; Aker and Tuncer 2016; Armas et al. 2020), very few studies were known to be conducted in field conditions (Bi et al. 2018). The current study was carried out to determine the insecticidal activity of Turkey native isolates of B. bassiana and M. anisopliae against the fall webworm H. cunea larvae under laboratory and field conditions. 2. Material and Methods Collection of larvae The adult emergence of Hyphantria cunea was observed for first generation and the larval development was also followed in gardens of hazelnut (Corylus avellana L.) in Duzce-Turkey. Just before the experiments, the first, second and third instar larvae were collected together with the small branches of hazelnut trees in June 2020. Spore suspensions Previously described five fungal isolates of B. bassiana (YK16, YK23 and YK26) and M. anisopliae (YK41 and YK45) from soils of Duzce-Turkey were used for preparing spore suspensions (Karabörklü et al. 2019). All isolates were taken from stock cultures, planted in Potato Dextrose Agar (PDA) medium, and kept in a climate chamber at 25°C, 60 ± 5% relative humidity and 14:10 h photoperiod for 10-15 days. Following the developmental period, the conidia were collected from rearing medium and transferred into distilled water including 0.03% Tween 80. Spore concentrations (1x105 and 1x106 conidia mL-1) were adjusted using a hemocytometer (0.100 mm × 0.0025 mm2) under light microscope. Laboratory essays Ten larvae for each instar were transferred into pet jars (1 L) as five replications. Three fresh hazelnut leaves, approximately 3, 4 and 6 gr weights, were added into each jar for feeding the first, second and third instar larvae for seven days, respectively. Spore suspensions were added to 50 mL spraying bottle and the concentrations were adjusted to 1x105 conidia mL-1 for each fungal isolate. Spore suspensions were then applied to larvae using a bottle by spraying method. To the control group distilled water including 0.03% Tween 80 was sprayed. After the spraying process, the plastic jars were covered with thin tulle and transferred to climate chamber. The larvae were kept at 23 ± 2°C, 65 ± 5% humidity and 14: 10 hour (light/dark) photoperiod in the laboratory. At the end of the 7th day of application, the numbers of living and dead larvae were determined. Mortality rates (%) were corrected using Abbott’s formula (Abbott 1925) for the mortalities in the controls for each fungal isolate and larval instar. Bioscience Journal | 2022 | vol. 38, e38015 | https://doi.org/10.14393/BJ-v38n0a2022-60197 3 KARABÖRKLÜ, S. Field essays The insecticidal activity of B. bassiana YK16, YK23 and YK26, and M. anisopliae YK41 and YK45 was tested on the second instar larvae of H. cunea from second generation. In the field essay, B. bassiana, M. anisopliae, a commercial synthetic insecticide diflubenzuron (Dimilin) and commercial bio-insecticide Bacillus thuringiensis var. kurstaki strain PB-54 (Bio-T Plus) were used in August 2020. A hazelnut garden, infested with high number of larval populations of fall webworm, was chosen for the trials. The numbers of living larvae were recorded for all treatments before the spraying. Spore suspensions of each fungal isolate (1x106 conidia mL-1) were added to 1 L pet spraying bottles separately. For commercial insecticides, recommended doses by manufacturers were used. Only distilled water including 0.03% Tween 80 was applied for the control groups. Trials were set up in five replicates in accordance with the randomized blocks trial pattern. After the spray of treatments, the hazelnut branches including larval clusters were covered with thin white tulles. At the end of the 7th day, the tulles were opened, and the numbers of living larvae were counted again. The dead larvae were brought to the laboratory to confirm the mortality caused by the isolates. Lethal efficacy of each isolate and commercial product was determined using formula developed by Henderson and Tilton (1955). Statistical analysis In comparison of data, variance analysis (one-factor ANOVA) was applied using the SPSS (SPSS 17.0 commercial software, SPSS, Inc., Chicago, IL) program. The averages were compared using a Tukey-Kramer HSD post-test at a 5% significance level. 3. Results At the end of 7th day, all entomopathogenic fungal isolates exhibited high insecticidal activities on first, second and third instars larvae of H. cunea at a concentration of 1x105 conidia ml-1 under laboratory condition. When compared with the control group, it was determined that B. bassiana and M. anisopliae isolates had a significant lethal effect on first instar larvae of H. cunea (F = 30.400; df = 4; p <0.0001). When the efficacies of fungal isolates were evaluated, it was seen that their mortality effects ranged from 100% to 84% (Figure 1). All isolates of B. bassiana caused 100% mortality on first instar larvae of H. cunea and were significantly different from the two M. anisopliae isolates. M. anisopliae YK45 isolate caused 88% mortality on the same larval instar (Figure 1). Figure 1. Lethal effect of Beauveria bassiana and Metarhizium anisopliae isolates on first instar larvae of H. cunea. *Among the means indicated by different letters there is a significant difference (p < 0.05). Bb: Beauveria bassiana, Ma: Metarhizium anisopliae. Bars indicate standard errors of mean. Mortality (%) corrected based on Abbott’s formula (Abbott 1925). Bioscience Journal | 2022 | vol. 38, e38015 | https://doi.org/10.14393/BJ-v38n0a2022-60197 4 Biocontrol potential of Beauveria bassiana and Metarhizium anisopliae isolates from Turkey against Hyphantria cunea (Drury)… Beauveria bassiana and M. anisopliae isolates also exhibited pronounced mortality rates on second instar larvae of H. cunea at the same dose and period (Figure 2). Their mortality effects ranged from 77.5 to 100% on the second instar larvae (F = 13.189; df = 4; p < 0.0001). Complete mortality was obtained with the application of B. bassiana YK23 isolate. Other B. bassiana isolates caused 96% mortality on the same instar larvae (Figure 2). Figure 2. Lethal effect of Beauveria bassiana and Metarhizium anisopliae isolates on second instar larvae of H. cunea. *Among the means indicated by different letters there is a significant difference (p < 0.05). Bb: Beauveria bassiana, Ma: Metarhizium anisopliae. Bars indicate standard errors of mean. Mortality (%) corrected based on Abbott’s formula (Abbott 1925). Mortality rates caused by fungal isolates ranged from 91.78 to 60.22% on third instar larvae (F = 7.901; df = 4; p < 0.001) (Figure 3). The most effective isolate was found to be B. bassiana YK23 with 91.78% mortality rate, followed by M. anisopliae YK45 isolate with 77.11% mortality rate (Figure 3). Figure 3. Lethal effect of Beauveria bassiana and Metarhizium anisopliae isolates on third instar larvae of H. cunea. *Among the means indicated by different letters there is a significant difference (p < 0.05). Bb: Beauveria bassiana, Ma: Metarhizium anisopliae. Bars indicate standard errors of mean. Mortality (%) corrected based on Abbott’s formula (Abbott 1925). Beauveria bassiana and M. anisopliae isolates also revealed significant insecticidal activity against second instar of H. cunea in field conditions (F = 40.585; df = 6; p < 0.0001) (Table 1). In the field essay, at the end of the 7th day B. bassiana YK23 displayed promising insecticidal activity (80.60%) on second instar larvae at 1x106 conidia ml-1 dose, and it did not differ from the efficacy of diflubenzuron and Bacillus Bioscience Journal | 2022 | vol. 38, e38015 | https://doi.org/10.14393/BJ-v38n0a2022-60197 5 KARABÖRKLÜ, S. thuringiensis var. kurstaki. Other fungal isolates caused mortality varying between 49.55% and 60.77% at the same dose and period. Table 1. Lethal effect of Beauveria bassiana and Metarhizium anisopliae isolates against second larvae instar of Hyphantria cunea in field condition. Treatment Number of alive larvae (Mean SD) Efficacy (%) Before application After application Control 311.428.15 309.0028.19 - Diflubenzuron 305.217.95 12.8004.97 95.8201.47a Btk 305.224.10 36.6013.28 87.8304.70ab BbYK16 304.629.03 118.2021.19 60.7706.87c BbYK23 312.623.39 60.2013.44 80.6004.21b BbYK26 300.415.06 121.8019.82 59.2405.27c MaYK41 302.212.87 150.4027.69 49.5511.08c MaYK45 299.409.63 120.0014.87 59.6304.70c aMeans within each column followed by the different letter are significantly different (p ≤ 0.05). Control: distilled water with 0.03% Tween 80, Btk: Bacillus thuringiensis var. kurstaki, Bb: Beauveria bassiana, Ma: Metarhizium anisopliae, SD: Standard deviation. Efficacy (%) calculated based on Henderson and Tilton’s formula (Henderson and Tilton 1955). 4. Discussion Beauveria bassiana and M. anisopliae isolates displayed significant insecticidal activity against the fall webworm H. cunea larvae in laboratory conditions. Fungal isolates were very effective especially on first and second instar larvae. All isolates of B. bassiana caused complete mortality on first instar larvae at the dose of 1x105 conidia ml-1. Mortality ratios ranged from 100 to 96% on second instar larvae. Iskender et al. (2012) reported that B. bassiana isolates (PaF04, PaF09 and PaF76) caused mortalities varying between 90 and 96.66% on the larvae at the dose of 1x106 conidia ml-1. In another study, Zibae et al. (2013) indicated that B. bassiana caused the highest mortality (76%) on fourth instar larvae of H. cunea at the dose of 107 conidia ml-1 for insect dipping method. Metarhizium anisopliae isolates caused 88 and 84% mortality on first instar and 81.33 and 77.11% on second instar larvae. The results in present study revealed that B. bassiana is more effective than M. anisopliae on the larval stages of H. cunea. Similar results were reported when B. bassiana and M. anisopliae were applied to fourth instar larvae of H. cunea in laboratory conditions (Armas et al. 2020). Fite et al. (2020) also reported that B. bassiana was more virulent to the third instar larvae of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) than M. anisopliae under laboratory conditions. Efficacy of fungal isolates decreased gradually depending on larval development. Third instar larvae of H. cunea appeared to be more resistant to fungal isolates compared with first and second instars at the same dose and period. The mortality values fluctuated between 91.78 and 72.89% for B. bassiana and 77.11 and 60.22% for M. anisopliae on 3th instar of H. cunea. Similarly, Aker and Tuncer (2016) reported that M. anisopliae caused 85% mortality on second instar larvae of H. cunea but decreased to 68.33% in third instar larvae at 1x108 conidia ml-1 dose at the end of 16 days. The B. bassiana and M. anisopliae also exhibited significant insecticidal activity on H. cunea larvae in field conditions. B. bassiana YK23 isolate displayed promising insecticidal activity by reaching 80.60% mortality rate on second instar larvae of H. cunea, and it did not differ from the efficacy of the commercial insecticides, diflubenzuron (95.82%) and Bacillus thuringiensis var. kurstaki (87.83%). Other fungal isolates caused mortalities varying between 49.55 and 60.77% at 1x106 conidia ml-1 dose at the end of 7th day. To the best of our knowledge, only one study (Bi et al. 2018) was conducted on the efficacy of B. bassiana and M. anisopliae against H. cunea larvae in field conditions. A trap-strips system was designed for H. cunea larvae in field conditions and 10 days later spore suspension of B. bassiana sprayed under each trap (1x108 conidia ml-1 dose) by Bi et al. (2018). The trap-strips provided an appropriate microenvironment for H. cunea to pupate and an acceptable humidity for B. bassiana to infect and reproduce. It was reported that the average infection rates for trap-strips systems were more than 90% against H. cunea. However, there are some reports on their effectiveness on other lepidopteran insect pests. Godonou et al. (2009) reported that B. bassiana (Bba5653) and M. anisopliae (Ma182) caused 94% and 80% mortality Bioscience Journal | 2022 | vol. 38, e38015 | https://doi.org/10.14393/BJ-v38n0a2022-60197 6 Biocontrol potential of Beauveria bassiana and Metarhizium anisopliae isolates from Turkey against Hyphantria cunea (Drury)… on third instar larvae of diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), respectively, at 1x108 conidia ml-1 dose in laboratory conditions. In field conditions, both emulsion and water-based formulations (equivalent to 1012 spore ml-1) of B. bassiana (Bba5653) were compared with the commercial insecticide bifenthrin by being practically 100% more efficient (Godonou et al. 2009). In addition, Agboyi et al. (2020) indicated that B. bassiana (Bb11) was able to reduce the density of P. xylostella by 83 and 93% in farm, compared with unsprayed control and deltamethrin application, respectively at the dose of 53 g/ha twice a week. Moreover, Fite et al. (2020) also indicated that B. bassiana is also effective against H. armigera by reducing larval infestations, decreasing pod damage and increasing chickpea yield in field conditions. Despite these, additional detailed studies need to be carried out to assess the effectiveness of B. bassiana and M. anisopliae in field conditions. 5. Conclusions All Turkey isolates of B. bassiana and M. anisopliae tested were pathogenic to the three first instars of H. cunea under laboratory condition, where the isolate YK23 of B. bassiana caused highest percent of mortality to the first and second instar of H. cunea. In the field condition, this isolate was also the most effective to cause the mortality of the second instar of H. cunea among all isolates tested, and it had the same efficacy of the commercial insecticides. Authors' Contributions: KARABÖRKLÜ, S.: conception and design, acquisition of data, analysis and interpretation of data, drafting the article, and critical review of important intellectual content. The author has read and approved the final version of the manuscript. Conflicts of Interest: The authors declare no conflicts of interest. Ethics Approval: Not applicable. Acknowledgments: The author would like to thank Dr. Semih Yılmaz and Khawar Jabran for improving the language of the manuscript. 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