Lethal Effects of Fungi Beauveria bassiana (Bals.) and Nanosilica on Cabbage Aphid Brevicoryne brassicae (L.) and Its Parasitoid Diaeretiella rapae (McIntosh) in Laboratory Conditions

Document Type : Research Article

Authors

• S. Emami ¹
• Sh. Aramideh ²
• S. pirsa ²
• J.P. Michavd ³

¹ Ph.D. Student, Department of Plant Protection, Faculty of Agriculture, Urmia University, Urmia, Iran

² Associate Professor, Faculty of Agriculture, Urmia University, Urmia, Iran

³ Department of Entomology, Kansas State University, Agricultural Research Center-Hays, Hays, KS, USA

10.22067/jpp.2021.70807.1030

Abstract

Introduction: Cabbage aphid, Brevicoryne brassicae (L.), is one of the most important and harmful pests of crucifers, which is active in many parts of Iran and causes quantitative and qualitative damage in the cultivation of these plants during the winter. Some natural enemies such as the parasitoid wasp Diaeretiella rapae (McIntosh) are active on this pest. The indiscriminate use of insecticides for controlling pests caused evolution of pest resistance, environmental pollution and negative effects on natural enemies and beneficial insects. In recent years, environmentally compatible factors have received more attention due to less side effects in pest control. This study was carried out to determine the effects of the entomopathogenic fungus Beauveria bassiana (Bals.), and nanosilica separately and in combination on survival of the cabbage aphid and its parasitoid treated by different concentrations of fungus (10³, 10⁴, 10⁵, 10⁶ and 10⁷spore/ml) and nanosilica (125, 250, 500, 1000 and 2000 ppm).
Material and Methods: Cabbages (Brassica olearaceae var. capitata) were grown from seed in plastic flower pots. Aphids were collected from Brassicaceae plants in fields of Nazlo Campus of Urmia University near Urmia city. This colony was used as a source for all aphids used in all laboratory experiments. Also, a colony of D. rapae was reared on B. brassicae under greenhouse conditions. Wasps were fed a 10% honey solution and used to parasitize aphids, or for use in experiments, 24 hours later.Fungi was cultured on Sabouraud Dextrose Agar (SDA) in petri dishes (6 cm in diameter) and incubated for two weeks to induce sporulation. Spores were harvested from the surface of 14-day old culture and transferred to a test tube containing sterilized distilled water with 0.05% Tween^®-80. The conidial concentration of final suspension was determined by direct count using a neubauer hemocytometer and serial dilutions were made to obtain different conidial concentrations. Sio₂ nanoparticles of pashgamannano^® company was used in bioassay tests. Bioassay test was carried out on aphid and its parasitoid. Aphids were treated by conidial concentrations using dipping method. Control adults were treated with distilled water containing 0.05% Tween^®-80. In order to evaluate the effect of nanosilica on aphids, leaf discs were dipped in to different concentrations of nanosilica and after drying, adult cabbage aphids were transferred on treated leaf discs in Petri dishes. The mortality was counted 24, 48 and 72 hours after treatment. Experiments were carried out at 25±2 C^o temperature, 65±5% RH and a photoperiod of 16: 8 h. (L: D) under laboratory conditions. LC₂₅, LC₅₀ and LT₅₀ values of fungi and nanosilica were estimated. Also, combination effects of fungi and nanosilica were evaluated in laboratory. A preliminary test was evaluated to determine side effects of different concentrations of nanosilica on viability and germination of fungi spore. Germination rate for fungi was calculated after 24 hours. The LC₂₅, LC₅₀ and LT₅₀ values (with 95% confidence limits) were calculated using the Probit analysis method. Bioassay data were subjected to one-way analysis of variance (ANOVA) after checking for normality and means were compared by Tukey’s test.
Results and Discussion: The LC₅₀ values obtained from the analysis of probit as a result of the effect of different concentrations of B. bassiana 7 days after treatment and nanosilica 24, 48 and 72 hours after treatment on cabbage aphid were 2.2×10⁵ spore/ml and 4356.14, 1164.42, 487.19 ppm, respectively. Furthermore the LC₅₀ values of B. bassiana 4 days after treatment and nanosilica 24, 48 and 72 hours after treatment on D. rapae were 1.2×10⁶ spore/ml and 3639.79, 619.51, 289.77 ppm, respectively. Results showed that the adults of the cabbage aphid were completely sensitive to the fungal isolate. The shortest time needed for the mortality of 50% of the population of cabbage aphid was 5.02 days at 10⁷ conidia/ml concentration. The mortality rate of nanosilica at highest concentration, 72 hours after treatment was 90 and 96.6% respectively for cabbage aphid and parasitoid wasp. Also, combination of these factors against adults of cabbage aphid had significant difference with control.
Conclusion: According to the results of this study, it can be concluded that B. bassiana and nanosilica are effective on cabbage aphid and can be used as effective factors in the integrated pest management program of this pest.

Keywords

• Cabbage aphid
• Entomopathogenic fungi
• None-chemical control
• Parasitoid

20.1001.1.20084749.1400.35.3.6.5

Main Subjects

• pests

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References

1. Akbari S., Safavi S.A., and Ghosta Y. 2014. Efficacy of Beauveria bassiana (Bals.) Vuill. Against Cabbage aphid Brevicoryne brassicae (Hem.: Aphididae) in laboratory condition. Archives of Phytopathology and Plant Protection 47(12): 1454-1458.
2. Akbari S., Mirfakhraie S., Aramideh S., and Safaralizadeh M.H. 2020. Effect of fungal isolates and imidacloprid on cabbage aphid Brevicoryne brassicae and its parasitoid Diaeretiella rapae. Zemdirbyste-Agriculture 107(3): 255-262.
3. Al Antary T.M., Ateyyat M.A., and Abussamin B.M. 2010. Toxicity of certain insecticides to the parasitoid Diaeretiella rapae (McIntosh) (Hymenoptera: Aphidiidae) andits host, the cabbage aphid Brevicoryne Brassicae (Homoptera: Aphididae). Australian Journal of Basic and Applied Sciences 4(6): 994-1000.
4. Jarrahi A., and Safavi S.A. 2016. Effects of pupal treatment with Proteus^® and Metarhizium anisopliae sensu lato on functional response of Habrobracon hebetor parasitising Helicoverpa armigera in an enclosed experiment system. Biocontrol Science and Technology 26(2): 206-216.
5. Jarrahi A., and Safavi S.A. 2016. Sublethal effects of Metarhizium anisopliae on life table parameters of Habrobracon hebetor parasitizing Helicoverpa armigera larvae at different time intervals. Biocontrol 61: 167-175.
6. Blackman R.A., and Eastop V.F. 1984. Aphis on the Worlds Crops. John Wiley and Sons, New York. 466 pp.
7. De A., Bose R., Kumar A., and Mozumdar S. 2014. Management of insect pests using nanotechnology: as modern approaches. In Targeted delivery of pesticides using biodegradable polymeric nanoparticles (pp. 29-33). Springer, New Delhi.
8. Debnath N., Das S., Seth D., Chandra R., Bhattacharya S.C., and Goswami A. 2011. Entomotoxic effect of silica nanoparticles against Sitophilus oryzae (L.). Journal of Pest Science 84(1): 99-105.
9. Desneux N., Rafalimanana H., and Kaiser L. 2004. Dose-response relationship in lethal and behavioral effects of different insecticides on the parasitic wasp Aphidiuservi. Chemosphere 54(5): 619-627.
10. Dhiman S.C. 2007. Population dynamics of Diaeretiella rapae (McIntosh): a parasitoid of mustard aphid, Lipaphis erysimi (Kalt). Journal of Applied Zoological Researches 18(2): 117-120.
11. Dorschner K.W., Feng M., and Baird C.R. 1991. Virulence of an aphid derived isolate of Beauveria bassiana (Fungi: Hyphomycetes) to the hop aphid, Phorodon humuli (Homoptera: Aphididae). Environmental Entomology 20(2): 690-693.
12. El-Bendary H.M., and El-Helaly A.A. 2013. First record nanotechnology in agricultural: Silica nano-particles a potential new insecticide for pest control. Applied Scientific Reports 4(3): 241-246.
13. Embaby E.E., and Lotfy D.E. 2016. Controlling cabbage aphid (Brevicoryne brassicae) using isolated mycoinsecticides. Journal of Plant Protection and Pathology 7(1): 73-77.
14. Enayati A., and Ebrahimnejad P. 2012. Nanopesticides: Production, application and biological considerations. Journal of Mazandaran University of Medical Sciences 21(86): 296-311. (In Persian with English abstract)
15. Ezz N. 2012. Entomopathogenic fungi associated with certain scale insects (Hemiptera: Coccoidea) in Egypt. Egyptian Academic Journal of Biological Sciences 5(3): 211-221.
16. Feng M., Johnson J.B., and Kish L.P. 1990. Virulence of Verticillium lecanii and an aphid derived isolate of Beauveria bassiana (Fungi: Hyphomycetes) for six species of cereal-infesting aphids (Homoptera: Aphididae). Environmental Entomology 19(3): 815-820.
17. Ghidan A.Y., Al-Antary T.M., and Awwad A.M. 2016. Green synthesis of copper oxide nanoparticles using Punica granatum peels extract: Effect on green peach aphid. Environmental Nanotechnology, Monitoring and Management 6: 95-98.
18. Gurulingappa P., McGee P.A., and Sword G. 2011. Endophytic Lecanicillium lecanii and Beauveria bassiana reduce the survival and fecundity of Aphis gossypii following contact with conidia and secondary metabolites. Crop Protection 30(3): 349-353.
19. Harper S. 2010. New approaches needed to gauge safety of nanotech-based pesticides, Researchers Urge. Physics and Chemistry 4(33): 2010-2012.
20. Helle W., and Overmeer W.P.J. 1985. Toxicological test methods. In: W. Helle & Sabelis, M.W. (eds.), Spider Mites: their Biology, Natural Enemies and Control. Elsevier. Amsterdam. Oxford. New York. Tokio. 1: 391-395.
21. Hersanti Susanto A., Virgiawan R., and Joni I.M. 2018. The effectiveness of Penicillium mixed with silica nanoparticles in controlling Myzus persicae. In: American Institute of Physics Conference Series. 1927(1).
22. Kassa A. 2003. Development and testing of mycoinsecticides based on submerged spores and aerial conidia of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) for control of locusts, grasshoppers and storage pests. Doctoral Dissertation. Georg-August-University Gottingen. (Germany)
23. Laing M.D., Gatarayiha M.C., and Adandonon A. 2006. Silicon use for pest control in agriculture: a review. In: Proceedings of the South African Sugar Technologists’ Association 80: 278-286.
24. Meyling N.V., and Eilenberg J. 2007. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biological Control 43(2): 145-155.
25. Modarres-Najafabadi S.S., Akbari-Moghaddam H., and Gholamian G. 2005. Population fluctuations of cabbage aphid (Brevicoryne brassicae) and identification of its natural enemies in Sistan region. Iranian Journal of Science and Technology of Agriculture and Natural Resources 8(4): 175-185. (In Persian with English abstract)
26. Mweke A., Ulrichs C., Nana P., Akutse K.S., Fiaboe K.K.M., Maniania N.K., and Ekesi S. 2018. Evaluation of the Entomopathogenic Fungi Metarhizium anisopliae, Beauveria bassiana and Isaria sp. for the Management of Aphis craccivora (Hemiptera: Aphididdae). Journal of Economic Entomology 111(4): 1587-1594.
27. Oerke E.C., and Dehne H.W. 2004. Safe guarding production-losses in major crops and the role of crop protection. Crop Protection 23(4): 275-285.
28. Pavitra G., Sushila N., Sreenivas A.G., Ashok J., and Sharanagouda H. 2018. Biosynthesis of Green Silica Nanoparticles and Its Effect on Cotton Aphid, Aphis gossypii Glover and Mealybug, Phenacoccus solenopsis International Journal of Current Microbiology and Applied Sciences 7(10): 1450-1460.
29. Qayyum A. 2021. Effects of host age on two closely related parasitoid species Diaeretiella rapae (McIntosh) and Aphidius colemani (Vireck) (Aphidiidae: Hymenoptera). Pakistan Journal of Zoology 33: 193-200.
30. Quesada-Moraga E.E.A.A., Maranhao E.A.A., Valverde-García P., and Santiago-Álvarez C. 2006. Selection of Beauveria bassiana isolates for control of the whiteflies Bemisia tabaci and Trialeurodes vaporariorum on the basis of their virulence, thermal requirements, and toxicogenic activity. Biological Control 36(3): 274-287.
31. Rannback L.M., Cotes B., Anderson P., Ramert B., and Meyling N.V. 2015. Mortality risk from entomopathogenic fungi affects oviposition behavior in the parasitoid wasp Trybliographa rapae. Journal of Invertebrate Pathology 124: 78-86.
32. Rehner S.A., and Buckley E. 2005. A Beauveria phylogeny inferred from nuclear ITS and EF1-a sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97(1): 84-98.
33. Rouhani M., Samih M.A., and Kalantari S. 2013. Insecticidal effect of silica and silver nanoparticles on the cowpea seed beetle, Callosobruchus maculatus (Col.: Bruchidae). Journal of Entomological Research 4: 297-305.
34. Satar S., Kersting U., and Ulvsoy M.R. 2005. Temperature dependent life history traits of Brevicoryne brassicae (Hom.: Aphididae) on white cabbage. Turkish Journal of Agriculture 29(5): 341-346.
35. Serebrov V.V., Gerber O.N., Malyarchuk A.A., Martemyanov V.V., Alekseev A.A., and Glupov V.V. 2006. Effect of Entomopathogenic Fungi on detoxification enzyme activity in reater wax moth Galleria mellonella (Lepidoptera: Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. Biological Bulletin 33(6): 581-586.
36. Singh R., and Singh G. 2015. Systematics, distribution and host range of Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae, Aphidiinae). International Journal of Research Studies in Biosciences 3(1): 1-36.
37. Taheri Sarhozaki M., Aramideh S., Akbarian J., and Pirsa S. 2020. The effect of zinc oxide nanoparticles, kaolin powder and Beauveria bassiana (Balsamo) Vuillemin in combination with neemarin against Bemisia tabaci and pupae of Eretmoceru smundus under field conditions. Plant Protection 43(3): 97-115. (In Persian with English abstract)
38. Wraight S.P., Carruthers R., Bradley C.A., Jaronski S.T., Lacey L.A., Wood P., and Galaini-Wraight S. 1998. Pathogenicity of the entomopathogenic fungi Paecilomyces spp. and Beauveria bassiana against the silver leaf whitefly, Bemisia argentifolii. Journal of Invertebrate Pathology 71(3): 217-226.
39. Zavareh M., and Emam Y. 2000. An identification guide for rapeseed (Brassica napus) developmental stages. Iranian Journal of Crop Sciences 2(1): 1-14. (In Persian with English abstract)
40. Ziaee M., and Hamzavi F. 2014. Application of nanoparticles in pest management programs. Nanotechnology 10: 18-23. (In Persian)