Sains Malaysiana 52(2)(2023): 467-476

http://doi.org/10.17576/jsm-2023-5202-11

 

Effect of Temperature on Germination, Radial Growth, and Sporulation of the New Isolates of Metarhizium anisopliae and Their Virulence to Whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae)

(Kesan Suhu terhadap Percambahan, Pertumbuhan Jejari dan Pensporaan Pencilan Baharu Metarhizium anisopliae dan Kevirulen terhadap Lalat Putih, Bemisia tabaci (Hemiptera: Aleyrodidae))

 

IBRAHIM SANI1,2, SYARI JAMIAN1,3, SITI IZERA ISMAIL1,3, NORSAZILAWATI SAAD1, SUMAIYAH ABDULLAH1, ERNEEZA MOHD HATA4 & JOHARI JALINAS5,*

 

1Department of Plant Protection, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

2Department of Biology, Faculty of Natural and Applied Sciences, Umaru Musa Yar’adua University, P.M.B., Katsina 2218, Nigeria

3Laboratory of Climate-Smart Food Crop Production, Institute of Tropical Agriculture and Food Security (ITAFoS), Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

4Laboratory of Sustainable Agronomy & Crop Protection, Institute of Plantation Studies, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

5Laboratory of Applied Entomology, Centre for Insect Systematics, Department of Biological Sciences and Biotechnology, Faculty of Science & Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor Darul Ehsan, Malaysia

 

Diserahkan: 26 April 2022/Diterima: 22 Disember 2022

 

Abstract

Metarhizium anisopliae is a potential entomopathogenic fungi (EPF) to control insect pests in Malaysia, yet little is known about the temperature influence on its growth and efficacy. The average daily temperature in Malaysia is between 21 °C and 32 °C, with some parts of Cameron Highland in Peninsular Malaysia experiencing temperatures as low as 14 °C. Therefore, for effective field application, the most effective EPF isolates should be tolerant to the temperature of the country. Here we conducted a laboratory experiment to determine the effects of average daily temperatures in Malaysia (15, 20, 25, and 30 °C) on conidial germination, radial growth, and conidial density of seven new isolates of M. anisopliae. However, at 25 and 30°C, the three isolates (Ma-2, Ma-9, and Ma-15) produced the highest number of conidia and were therefore selected for virulence test against the second instar of whitefly, Bemisia tabaci. The percentage mortality of the three isolates ranged between 36.1% and 97.7% across different temperatures for 7 days post-treatment. The isolates Ma-15 caused the highest percentage mortality of 97.7% and the shortest LT50 and LT90 values (1.68 and 3.98 days, respectively), at 30 °C incubation temperature. This study confirms that the growth and virulence of Malaysian isolates of M. anisopliae are strongly influenced by temperature and could be used as promising candidates for biocontrol of B. tabaci on vegetables planted in a tropical climate such as that of low land and highland in Malaysia, although extensive field and semi-field bioassays, as well as the development of ideal formulation, are still required.

 

Keywords: Bemisia tabaci; entomopathogenic fungui; Metarhizium anisopliae; percentage mortality; temperature

 

Abstrak

Metarhizium anisopliae merupakan kulat entomopatogen (EPF) yang berpotensi untuk mengawal perosak serangga di Malaysia. Namun, pertumbuhan EPF bergantung pada suhu. Purata suhu harian di Malaysia adalah antara 21 °C dan 32 °C, dengan beberapa bahagian Tanah Tinggi Cameron di Semenanjung Malaysia mengalami suhu serendah 14 °C. Oleh itu, untuk aplikasi lapangan yang berkesan dan pencilan EPF yang paling berkesan ialah suhu setempat. Di sini, kami menjalankan uji kaji makmal untuk menentukan kesan purata suhu harian di Malaysia (15, 20, 25 dan 30 °C) terhadap percambahan konidium, pertumbuhan jejari dan ketumpatan konidium bagi tujuh pencilan baharu M. anisopliae. Walau bagaimanapun, pada suhu 25 dan 30 °C, ketiga-tiga pencilan (Ma-2, Ma-9, dan Ma-15) menghasilkan bilangan konidia tertinggi dan oleh itu dipilih untuk ujian virulen terhadap instar kedua bagi lalat putih, Bemisia tabaci. Peratusan kematian ketiga-tiga pencilan adalah antara 36.1% dan 97.7% merentasi suhu berbeza selama 7 hari selepas rawatan. Pencilan Ma-15 menyebabkan peratusan kematian tertinggi iaitu 97.7% dan nilai LT50 dan LT90 terendah (masing-masing 1.68 dan 3.98 hari) pada suhu inkubasi 30 °C. Kajian ini mengesahkan bahawa pertumbuhan dan virulen pencilan M. anisopliae Malaysia sangat dipengaruhi oleh suhu dan boleh digunakan sebagai kawalan biologi yang berpotensi terhadap B. tabaci pada sayur-sayuran yang ditanam di iklim tropika seperti tanah rendah dan tanah tinggi di Malaysia, namun begitu, ujian lapangan dan semi-bioasai, serta pembangunan formulasi yang ideal masih diperlukan.

 

Kata kunci: Bemisia tabaci; kulat entomopatogen; Metarhizium anisopliae; peratusan kematian; suhu

 

RUJUKAN

Ali, S., Jianhui, W., Zhen, H. & Shun, X.R. 2010. Production and regulation of extracellular chitinase from the entomopathogenic fungus Isaria fumosorosea. Biocontrol Science and Technology 20(7): 723-738. doi:10.1080/09583151003714091

Antonio, F.M., Pucheta, M.D., Rodriguez, N.S., Mayra, D.T.M. & Miguel, A.R.L. 2012. Mycoinsecticide effects of Beauveria bassiana, Metarhizium anisopliae, and Isaria fumosorosea on the whitefly Bemisia tabaci (Homoptera: Aleyrodidae) in different strata of bean. African Journal of Microbiology Research 6(45): 7246-7252. doi:10.5897/AJMR12.648

Brunner-Mendoza, C., María del Rocío, R., Soumya, M., Michael, J.B. & Conchita, T. 2019. A review on the genus Metarhizium as an entomopathogenic microbial biocontrol agent with emphasis on its use and utility in Mexico. Biocontrol Science and Technology 29(1): 83-102. doi:10.1080/09583157.2018.1531111

Bugeme, D.M., Nguya, K., Maniania, M.K. & Hamadi, I.B. 2008. Effect of temperature on virulence of Beauveria bassiana and Metarhizium anisopliae isolates to Tetranychus evansi. Experimental and Applied Acarology 46(1-4): 275-285. doi:10.1007/s10493-008-9179-1

Cabanillas, H.E. & Walker, A.J. 2009. Effects of temperature and culture media on vegetative growth of an entomopathogenic fungus Isaria sp. (Hypocreales: Clavicipitaceae) naturally affecting the whitefly, Bemisia tabaci in Texas. Mycopathologia 167: 263-271. doi:10.1007/s11046-008-9176-2

Davidson, G., Phelps, K., Sunderland, K.D., Pell, J.K., Ball, B.V., Shaw, K.E. & Chandler, D. 2003. Study of temperature-growth interactions of entomopathogenic fungi with potential for control of Varroa destructor (Acari: Mesostigmata) using a nonlinear model of poikilotherm development. Journal of Applied Microbiology 94(5): 816-825. doi:10.1046/j.1365-2672.2003.01871.x

Hodges, G.S. & Gregory, A.E. 2005. An identification guide to the whiteflies (Hemiptera: Aleyrodidae) of the Southeastern United States. Florida Entomologist 88(4): 518-534. doi:10.1653/0015-4040(2005)88[518:AIGTTW]2.0.CO;2

Inglis, G.D., Goettel, M.S., Butt, T.M. & Strasser, H. 2001. Use of hyphomycetous fungi for managing insect pests. In Fungi as Biocontrol Agents: Progress, Problems and Potential, edited by Butt, N., Jackson, T.M. & Magan, C. Wallingford: CAB International. pp. 23-69.

Keerio, A.U., Nazir, T., Abdulle, Y.A., Jatoi, G.H., Gadhi, M.A., Anwar, T., Sokea, T. & Qiu, D. 2020. In vitro pathogenicity of the fungi Beauveria bassiana and Lecanicillium lecanii at different temperatures against the whitefly, Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae). Egyptian Journal of Biological Pest Control 30: 41. doi:10.1186/s41938-020-00247-8

Lee, W.W., Shin, T.Y., Bae, S.M. & Woo, S.D. 2015. Screening and evaluation of entomopathogenic fungi against the Green Peach Aphid, Myzus persicae, using multiple tools. Journal of Asia-Pacific Entomology 18(3): 607-615. doi:10.1016/j.aspen.2015.07.012

Lord, J.V.C. 2005. From Metchniko V to Monsanto and beyond: The path of microbial control. Journal of Invertebrate Pathology 89: 19-29. doi:10.1016/j.jip.2005.04.006

Mascarin, G.M., Kobori, N.N., Quintela, E.D. & Delalibera, I. 2013. The virulence of entomopathogenic fungi against Bemisia tabaci Biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation. Biological Control 66(3): 209-218. doi:10.1016/j.biocontrol.2013.05.001

Misaka, B.C., Everlyne, N., Wosula, P.W., Marchelo-d’Ragga, T. & James, P.L. 2020. Genetic diversity of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) colonizing sweet potato and cassava in South Sudan. Insects 11(1): 58. doi:10.3390/insects11010058

Nishi, O., Shimizu, S. & Sato, H. 2017. Metarhizium bibionidarum and M. purpureogenum: New species from Japan. Mycol Progress 16: 987-998. doi:10.1007/s11557-017-1333-x

Norhelina, L., Sajap, A.S., Mansour, S.A. & Idris, A.B. 2013. Infectivity of five Metarhizium anisopliae (Deuteromycota: Hyphomycetales) strains on Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) infesting brinjal, Solanum melongena (Solanaceae). Academic Journal of Entomology 6(3): 127-132. doi:10.5829/idosi.aje.2013.6.3.7686

Onsongo, S.K., Bernard, M.G., Akutse, K.S., Thomas, D. & Mohamed, S.A. 2019. Performance of three isolates of Metarhizium anisopliae and their virulence against Zeugodacus cucurbitae under different temperature regimes, with global extrapolation of their efficiency. Insects 10: 9. doi:10.3390/insects10090270

Ortiz-Urquiza, A. & Keyhani, N.O. 2013. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects 4(3): 357-374. doi:10.3390/insects4030357

Rodríguez, M., Gerding, M. & France, A. 2009. Selection of entomopathogenic fungi to control Varroa destructor (Acari: Varroidae). Chilean Journal of Agricultural Research 69(December): 534-540.

Sain, S.K., Monga, D., Kumar, R., Nagrale, D.T., Kranthi, S. & Kranthi, R.K. 2019. Comparative effectiveness of bioassay methods in identifying the most virulent entomopathogenic fungal strains to control Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Egyptian Journal of Biological Pest Control 29(31): 1-11. doi:10.1186/s41938-019-0130-z

Sandhu, S.S., Sharma, A.K., Beniwal, V., Goel, G., Batra, P., Kumar, A., Jaglan, S., Sharma, A.K. & Malhotra, S. 2012. Myco-biocontrol of insect pests: Factors involved, mechanism, and regulation. Journal of Pathogens 2012: Article ID. 126819. doi:10.1155/2012/126819

Sani, I., Jamian, S., Ismail, S.I., Saad, N., Abdullah, S., Hata, E.M., Kamarudin, M.A. & Jalinas, J. 2022. Identification of entomopathogenic fungi Metarhizium anisopliae and Purpureocillium lilacinum from oil palm plantation soils in Universiti Putra Malaysia. Malaysian Journal of Microbiology 18(1): 105-112.

Sani, I., Ismail, S.I., Abdullah, S., Jalinas, J., Jamian, S. & Saad, N. 2020. A review of the biology and control of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), with special reference to biological control using entomopathogenic fungi. Insects 11(9): 1-18. doi:10.3390/insects11090619

Santiago-Alvarez, C., Maranhaõ, E.A., Maranhaõ, E. & Quesada-Moraga, E. 2006. Host plant influences pathogenicity of Beauveria bassiana to Bemisia tabaci and its sporulation on cadavers. BioControl 51: 519-532. doi:10.1007/s10526-005-5737-1

Shadmany, M., Boykin, L.M., Muhamad, R. & Omar, D. 2019. Genetic diversity of Bemisia tabaci (Hemiptera: Aleyrodidae) species complex across Malaysia. Journal of Economic Entomology 112(1): 75-84. doi:10.1093/jee/toy273

Shan, L.T. & Ming, G.F. 2010. Evaluation of the biocontrol potential of various Metarhizium isolates against Green Peach Aphid Myzus persicae (Homoptera: Aphididae). Pest Management Science 66(6): 669-675. doi:10.1002/ps.1928

Sumikarsih, E., Herlinda, S. & Pujiastuti, Y. 2019. Conidial density and viability of Beauveria bassiana isolates from Java and Sumatra and their virulence against Nilaparvata lugens at different temperatures. Agrivita 41(2): 335-350. doi:10.17503/agrivita.v41i2.2105

Susan, D., Nguya, K.M., Slawomir, A.L. & Jones, M.M. 2004. Effect of constant temperatures on germination, radial growth and virulence of Metarhizium anisopliae to three species of African Tephritid fruit flies. BioControl 49: 83-94. doi: 10.1023/B:BICO.0000009397.84153.79

Syed, A.R., Sivapragasam, A., Loke, W.H. & Roff, M.N. 2000. Whiteflies infesting vegetables in Malaysia. Plant Resource Management Conference. Safety in Food and Environment at Hilton Kuching, Sarawak, edited by Mohamad Roff Mohd Noor, Cheah, U.B., Ron, A.G., Ho, N.K., Zakaria, S., Jeremy, N., Sepiah, M., Isa, I. & Teo, G.K. Malaysian Plant Protection Society. pp. 38-43.

Taylor, B.M. & Khan, A. 2010. Germination, radial growth and virulence of Metarhizium anisopliae & Paecilomyces fumosoroseus on Bemisia tabaci Gennadius (Homoptera: Aleyrodidae). Pakistan Entomologist 32(2): 148-154. https://www.cabdirect.org/cabdirect/abstract/20113215365

Tefera, T. & Pringle, K. 2003. Germination, radial growth, and sporulation of Beauveria bassiana and Metarhizium anisopliae isolates and their virulence to Chilo partellus (Lepidoptera: Pyralidae) at different temperatures. Biocontrol Science and Technology 13(7): 699-704. doi:10.1080/0958315031000151756

Thomas, M.B. & Nina, E.J. 1997. Effects of temperature on growth of Metarhizium flavoviride and virulence to the variegated grasshopper, Zonocerus variegatus. Mycological Research 101(12): 1469-1474. doi:10.1017/S0953756297004401

Tumuhaise, V., Ekesi, S., Maniania, N.K., Tonnang, H.E.Z., Tanga, C.M., Ndegwa, P.N., Irungu, L.W., Srinivasan, R. & Mohamed, S.A. 2018. Temperature-dependent growth and virulence, and mass production potential of two candidate isolates of Metarhizium anisopliae (Metschnikoff) sorokin for managing Maruca vitrata fabricius (Lepidoptera: Crambidae) on cowpea. African Entomology 26(1): 73-83. doi:10.4001/003.026.0073

Wu, S., Toews, M.D., Oliveira-Hofman, C., Behle, R.W., Simmons, A.M. & Shapiro-Ilan, D.I. 2020. Environmental tolerance of entomopathogenic fungi: A new strain of Cordyceps javanica isolated from a whitefly epizootic versus commercial fungal strains. Insects 11(10): 1-15. doi:10.3390/insects11100711

 

*Pengarang untuk surat-menyurat: email: johari_j@ukm.edu.my

   

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