Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-15T08:44:07.982Z Has data issue: false hasContentIssue false

Pathogenicity and performance of two candidate isolates of Metarhizium anisopliae and Beauveria bassiana (Hypocreales: Clavicipitaceae) in four liquid culture media for the management of the legume pod borer Maruca vitrata (Lepidoptera: Crambidae)

Published online by Cambridge University Press:  12 February 2015

V. Tumuhaise
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772 – 00100, Nairobi, Kenya University of Nairobi, PO Box 30197 – 00100, Nairobi, Kenya
S. Ekesi*
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772 – 00100, Nairobi, Kenya
S.A. Mohamed
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772 – 00100, Nairobi, Kenya
P.N. Ndegwa
Affiliation:
University of Nairobi, PO Box 30197 – 00100, Nairobi, Kenya
L.W. Irungu
Affiliation:
University of Nairobi, PO Box 30197 – 00100, Nairobi, Kenya
R. Srinivasan
Affiliation:
AVRDC – The World Vegetable Center, Tainan74151, Taiwan
N.K. Maniania
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772 – 00100, Nairobi, Kenya
*
Get access

Abstract

The aim of this study was to identify and develop entomopathogenic fungi as biopesticides for management of Maruca vitrata (Fabricius). Fourteen isolates of Metarhizium anisopliae (Metchnikoff) Sorokin and six of Beauveria bassiana (Bals.-Criv.) Vuill. were screened against first instar larvae of M. vitrata. The two most virulent isolates were selected and further tested for production in four liquid media. Different formulations of one isolate were evaluated against different developmental stages. Metarhizium anisopliae ICIPE 18 and ICIPE 69 caused highest larval mortality of 91 and 81%, with lethal time to 50% mortality (LT50) values of 1.8 and 1.7 days and LC50 of 1.07 × 107 and 3.01 × 106conidia/ml, respectively. ICIPE 69 yielded more biomass and propagules in two liquid media than ICIPE 18. All developmental stages and adult moths were susceptible to fungal infection and horizontal transmission caused a significant reduction in fecundity. Isolate ICIPE 69 was identified as the most potent isolate for managing M. vitrata based on demonstrated efficacy against different developmental stages and amenability to production in liquid media and could be utilized as an alternative to pesticides in cowpea IPM.

Type
Research Papers
Copyright
Copyright © ICIPE 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, W. S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265267.Google Scholar
Adámek, L. (1963) Submerse cultivation of the fungus Metarhizium anisopliae (Metsch.). Folia Microbiologica (Praha) 10, 255257.Google Scholar
Adati, T., Tamò, M., Yusuf, S. R., Downham, M. C. A., Singh, B. B. and Hammond, W. (2008) Integrated pest management for cowpea–cereal cropping systems in the West African savannah. International Journal of Tropical Insect Science 27, 123137.CrossRefGoogle Scholar
Adesoye, A., Machuka, J. and Togun, A. (2008) CRY 1AB trangenic cowpea obtained by nodal electroporation. African Journal of Biotechnology 7, 32003210.Google Scholar
Angel-Sahagún, C. A., Lezama-Gutiérrez, R., Molina-Ochoa, J., Galindo-Velasco, E., López-Edwards, M., Rebolledo-Dominguez, O., Cruz-Vázquez, C., Reyes-Velázquez, W. P., Skoda, S. R. and Foster, J. E. (2005) Susceptibility of biological stages of the horn fly, Haematobia irritans, to entomopathogenic fungi (Hyphomycetes). Journal of Insect Science 5, 50.Google Scholar
Atachi, P. and Sourokou, B. (1989) Use of Decis® and Systoate® for the control of Maruca testulalis (Geyer) in cowpea. International Journal of Tropical Insect Science 10, 373381.CrossRefGoogle Scholar
Bae, J. -T., Sinha, J., Park, J. -P., Song, C. -H. and Yun, J. -W. (2000) Optimization of submerged culture conditions for exo-biopolymer production by Paecilomyces japonica. Journal of Microbiology and Biotechnology 10, 482487.Google Scholar
Bateman, R. P., Carey, M., Moore, D. and Prior, C. (1993) The enhanced infectivity of Metarhizium flavoviride in oil formulations to desert locusts at low humidities. Annals of Applied Biology 122, 145152.Google Scholar
Benz, G. (1987) Environment, pp. 177214. In Epizootiology of Insect Diseases (edited by Fuxa, J. R. and Tanada, Y.). Wiley and Sons, New York.Google Scholar
Burgerjon, A. (1956) Pulvérisation et poudrage au laboratoire par des préparations pathogènes insecticides. Annales des Epiphyties 7, 675683.Google Scholar
Butt, T. M. and Goettel, M. S. (2000) Bioassays of entomogenous fungi, pp. 141195. In Bioassays of Entomopathogenic Microbes and Nematodes (edited by Navon, A. and Ascher, K. R. S.). CABI Publishing, London, UK.Google Scholar
Campagne, P., Kruger, M., Pasquet, R., Le Ru, B. and Van den Berg, J. (2013) Dominant inheritance of field-evolved resistance to Bt corn in Busseola fusca. PLoS ONE 8, e69675.Google Scholar
Castillo, M., Moya, P., Hernandez, E. and Primo-Yufera, E. (2000) Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biological Control 19, 274282.Google Scholar
Chaudhury, D., Madanpotra, S., Jaiwal, R., Saini, R., Ananda Kumar, P. and Jaiwal, P. K. (2007) Agrobacterium tumefaciens-mediated high frequency genetic transformation of an Indian cowpea (Vigna unguiculata L. Walp.) cultivar and transmission of transgenes into progeny. Plant Science 172, 692700.Google Scholar
Chopra, K., Leemans, R., Kumar, P. and Simons, H. (2005) Ecosystems and Human Well-Being: Policy Responses, Volume 3–Findings of the Responses Working Group (Millennium Ecosystem Assessment Series) 2nd edn.Island Press, Washington/Covelo/London. 621 pp.Google Scholar
Daoust, R. A., Ward, M. G. and Roberts, D. W. (1983) Effect of formulation on the viability of Metarhizium anisopliae conidia. Journal of Invertebrate Pathology 41, 151160.Google Scholar
Dimbi, S., Maniania, N. and Ekesi, S. (2013) Horizontal transmission of Metarhizium anisopliae in fruit flies and effect of fungal infection on egg laying and fertility. Insects 4, 206216.Google Scholar
Dimbi, S., Maniania, N. K., Lux, S. A., Ekesi, S. and Mueke, J. K. (2003) Pathogenicity of Metarhizium anisopliae (Metsch.) Sorokin and Beauveria bassiana (Balsamo) Vuillemin, to three adult fruit fly species: Ceratitis capitata (Weidemann), C. rosa var. fasciventris Karsch and C. cosyra (Walker) (Diptera: Tephritidae). Mycopathologia 156, 375382.Google Scholar
Downham, M. C. A., Tamo, M., Hall, D. R., Datinon, B., Adetonah, S. and Farman, D. I. (2004) Developing pheromone traps and lures for Maruca vitrata in Benin, West Africa. Entomologia Experimentalis et Applicata 110, 151158.Google Scholar
Dugje, I. Y., Omoigui, L. O., Ekeleme, F., Kamara, A. Y. and Ajeigbe, H. (2009) Farmers' Guide to Cowpea Production in West Africa. IITA, Ibadan, Nigeria. 20 pp.Google Scholar
Eilenberg, J. (1987) Abnormal egg-laying behaviour of female carrot flies (Psila rosae) induced by the fungus Entomophthora muscae. Entomologia Experimentalis et Applicata 43, 6165.Google Scholar
Ekesi, S. (1999) Insecticide resistance in field populations of the legume pod-borer, Maruca vitrata Fabricius (Lepidoptera: Pyralidae), on cowpea, Vigna unguiculata (L.) Walp, in Nigeria. International Journal of Pest Management 45, 5759.Google Scholar
Ekesi, S., Adamu, R. S. and Maniania, N. K. (2002 a) Ovicidal activity of entomopathogenic hyphomycetes to the legume pod borer, Maruca vitrata and the pod sucking bug, Clavigralla tomentosicollis. Crop Protection 21, 589595.Google Scholar
Ekesi, S., Maniania, N. K. and Lux, S. A. (2002 b) Mortality in three African tephritid fruit fly puparia and adults caused by the entomopathogenic fungi, Metarhizium anisopliae and Beauveria bassiana. Biocontrol Science and Technology 12, 717.Google Scholar
Ekesi, S., Maniania, S. K. and Lux, S. A. (2005) Effect of different formulations of Metarhizium anisopliae on three tephritid fruit flies and their associated endoparasitoids. Biological Control 35, 8391.Google Scholar
Ekesi, S., Maniania, N. K., Onu, I. and Löhr, B. (1998) Pathogenicity of entomopathogenic fungi (Hyphomycetes) to the legume flower thrips, Megalurothrips sjostedti (Trybom) (Thysan., Thripidae). Journal of Applied Entomology 122, 629634.Google Scholar
Fargues, J., Maniania, N. K., Delmas, J. C. and Smits, N. (1992) Influence de la température sur la croissance in vitro d'hyphomycètes entomopathogènes. Agronomie 12, 557564.Google Scholar
Fargues, J., Smits, N., Vidal, C., Vey, A., Vega, F., Mercadier, G. and Quimby, P. (2002) Effect of liquid culture media on morphology, growth, propagule production, and pathogenic activity of the hyphomycete, Metarhizium flavoviride. Mycopathologia 154, 127138.Google Scholar
Feng, M.-G. and Johnson, J. B. (1990) Relative virulence of six isolates of Beauveria bassiana on Diuraphis noxia (Homoptera: Aphididae). Environmental Entomology 19, 785790.Google Scholar
Fuxa, J. R. (1987) Ecological considerations for the use of entomopathogens in IPM. Annual Review of Entomology 32, 225251.Google Scholar
Goettel, M. S. and Inglis, G. D. (1997) Fungi: hyphomycetes, pp. 213248. In Manual of Techniques in Insect Pathology (edited by Lacey, L. A.). Academic Press, San Diego.Google Scholar
Hassan, M. N. (2007) Re-investigation of the female sex pheromone of the legume podborer, Maruca vitrata (Lepidoptera: Crambidae). PhD thesis, University of Greenwich, UK.Google Scholar
Huang, C., Peng, W. and Talekar, N. S. (2003) Parasitoids and other natural enemies of Maruca vitrata feeding on Sesbania cannabina in Taiwan. BioControl 48, 407416.Google Scholar
Huesing, J. E., Romeis, J., Ellstrand, N. C., Raybould, A., Hellmich, R. L., Wolt, J. D., Ehlers, J. D., Dabiré-Binso, L. C., Fatokun, C. A., Hokanson, K. E., Ishiyaku, M. F., Margam, V. M., Obokoh, N., Mignouna, J. D., Nang'ayo, F., Ouedraogo, J. T., Pasquet, R. S., Pittendrigh, B. R., Schaal, B. A., Tamò, M. and Murdock, L. L. (2011) Regulatory considerations surrounding the deployment of Bt-expressing cowpea in Africa. Report of the deliberations of an expert panel. GM Crops & Food 2, 211224.Google Scholar
Humphreys, A. M., Matewele, P., Trinci, A. P. J. and Gillespie, A. T. (1989) Effects of water activity on morphology, growth and blastospore production of Metarhizium anisopliae, Beauveria bassiana and Paecilomyces farinosus in batch and fed-batch culture. Mycological Research 92, 257264.Google Scholar
Inglis, G. D., Enkerli, J. and Goettel, M. S. (2012) Laboratory techniques used for entomopathogenic fungi: Hypocreales, pp. 189253. In Manual of Techniques in Invertebrate Pathology, 2nd edn (edited by Lacey, L. A.). Academic Press, San Diego.CrossRefGoogle Scholar
Inglis, G. D., Johnson, D. L. and Goettel, M. S. (1996) An oil-bait bioassay method used to test the efficacy of Beauveria bassiana against grasshoppers. Journal of Invertebrate Pathology 67, 312315.Google Scholar
Jackai, L. E. N. (1981) Relationship between cowpea crop phenology and field infestation by the legume pod borer, Maruca testulalis. Annals of the Entomological Society of America 74, 402408.CrossRefGoogle Scholar
Jackai, L. E. N. and Daoust, R. A. (1986) Insect pests of cowpeas. Annual Review of Entomology 31, 95119.Google Scholar
Jackson, M. A., Dunlap, C. A. and Jaronski, S. T. (2009) Ecological considerations in producing and formulating fungal entomopathogens for use in insect biocontrol. BioControl 55, 129145.Google Scholar
Jackson, M. A., Mcguire, M. R., Lacey, L. A. and Wraight, S. P. (1997) Liquid culture production of desiccation tolerant blastospores of the bioinsecticidal fungus Paecilomyces fumosoroseus. Mycological Research 101, 3541.Google Scholar
Jenkins, N. E. and Prior, C. (1993) Growth and formation of true conidia by Metarhizium flavoviride in a simple liquid medium. Mycological Research 97, 14891494.Google Scholar
Karel, A. K. (1985) Yield losses from and control of bean pod borers, Maruca testulalis (Lepidoptera: Pyralidae) and Heliothis armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology 78, 13231326.Google Scholar
Kirubakaran, S. A., Sathish-Narayanan, S., Revathi, K., Chandrasekaran, R. and Senthil-Nathan, S. (2014) Effect of oil-formulated Metarhizium anisopliae and Beauveria bassiana against the rice leaffolder Cnaphalocrocis medinalis Guenée (Lepidoptera: Pyralidae). Archives of Phytopathology and Plant Protection 47, 977992.CrossRefGoogle Scholar
Kleespies, R. G. and Zimmermann, G. (1992) Production of blastospores by three strains of Metarhizium anisopliae (Metch.) Sorokin in submerged culture. Biocontrol Science and Technology 2, 127135.Google Scholar
Langyintuo, A. S., Lowenberg-DeBoer, J., Faye, M., Lambert, D., Ibro, G., Moussa, B., Kergna, A., Kushwaha, S., Musa, S. and Ntoukam, G. (2003) Cowpea supply and demand in West and Central Africa. Field Crops Research 82, 215231.Google Scholar
Lomer, C. J., Bateman, R. P., Godonou, I., Kpindou, D., Shah, P. A., Paraiso, A. and Prior, C. (1993) Field infection of Zonocerus variegatus following application of an oil-based formulation of Metarhizium flavoviride conidia. Biocontrol Science and Technology 3, 337346.Google Scholar
Mangenot, F. and Reisinger, O. (1976) Form and function of conidia as related to their development, pp. 789846. In The Fungal Spore: Form and Function (edited by Weber, D. J. and Hess, W. M.). John Wiley & Sons Inc., New York.Google Scholar
Maniania, N. K. (1992) Pathogenicity of entomogenous fungi (hyphomycetes) to larvae of the stem borers, Chilo partellus Swinhoe and Busseola fusca Fuller. International Journal of Tropical Insect Science 13, 691696.Google Scholar
Maniania, S. K., Oketch, M. A., Adino, J. O., Opere, J. O. and Ekesi, S. (2013) Transfer of inoculum of Metarhizium anisopliae between adult Glossina morsitans morsitans and effects of fungal infection on blood feeding and mating behaviors. Journal of Pest Science 86, 285292.CrossRefGoogle ScholarPubMed
Meadow, R., Vandenberg, J. D. and Shelton, M. (2000) Exchange of inoculums of Beauveria bassiana (Bals.) Vuill. (Hyphomycetes) between adult flies of the cabbage maggot Delia radicum L. (Diptera: Anthomyiidae). Biocontrol Science and Technology 10, 479485.Google Scholar
Migiro, L. N., Maniania, N. K., Chabi-Olaye, A. and Vandenberg, J. (2010) Pathogenicity of entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana (Hypocreales: Clavicipitaceae) isolates to the adult pea leafminer (Diptera: Agromyzidae) and prospects of an autoinoculation device for infection in the field. Environmental Entomology 39, 468475.Google Scholar
Ngumbi, P. M., Irungu, L. W., Ndegwa, P. N. and Maniania, N. K. (2011) Pathogenicity of Metarhizium anisopliae (Metch) Sorok and Beauveria bassiana (Bals) Vuill. to adult Phlebotomus duboscqi (Neveu-Lemaire) in the laboratory. Journal of Vector Borne Diseases 48, 3740.Google Scholar
Odindo, M. O., Otieno, W. A., Oloo, G. W., Kilori, J. and Odhiambo, R. C. (1989) Prevalence of microorganisms in field-sampled borers on sorghum, maize, and cowpea in western Kenya. International Journal of Tropical Insect Science 10, 225228.Google Scholar
Okeyo-Owuor, J. B., Agwaro, P. O. and Simbi, C. O. J. (1983) Studies on the legume pod-borer Maruca testulalis (Geyer)–V. Larval population. International Journal of Tropical Insect Science 4, 7581.Google Scholar
Okeyo-Owuor, J. B., Oloo, G. W. and Agwaro, P. O. (1991) Natural enemies of the legume pod borer, Maruca testulalis Geyer (Lepidoptera: Pyralidae) in small scale farming systems of Western Kenya. International Journal of Tropical Insect Science 12, 3542.Google Scholar
Onyango, F. O. and Ochieng'-Odero, J. P. R. (1993) Laboratory rearing of the legume pod borer, Maruca testulalis Geyer (Lepidoptera: Pyralidae) on a semi-synthetic diet. International Journal of Tropical Insect Science 14, 719722.Google Scholar
Otieno, W. A., Odindo, M. O., Okeyo-Owuor, J. B. and Sabwa, D. M. (1983) Studies on the legume pod-borer, Maruca testulalis Geyer–VII. Field surveys on pathogenic microorganisms. International Journal of Tropical Insect Science 4, 211215.Google Scholar
Popelka, J. C., Gollasch, S., Moore, A., Molvig, L. and Higgins, T. J. V. (2006) Genetic transformation of cowpea (Vigna unguiculata L.) and stable transmission of the transgenes to progeny. Plant Cell Reports 25, 304312.Google Scholar
Poprawski, T. J., Marchal, M. and Robert, P.-H. (1985) Comparative susceptibility of Otiorhynchus sulcatus and Sitona lineatus (Coleoptera: Curculionidae) early stages to five entomopathogenic hyphomycetes. Environmental Entomology 14, 247253.Google Scholar
Prior, C., Jollands, P. and le Patourel, G. (1988) Infectivity of oil and water formulations of Beauveria bassiana (Deuteromycotina: Hyphomycetes) to the cocoa weevil pest Pantorhytes plutus (Coleoptera: Curculionidae). Journal of Invertebrate Pathology 52, 6672.Google Scholar
R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org.Google Scholar
Ranga Rao, G. V. and Shanower, T. G. (1999) Identification and Management of Pigeonpea and Chickpea Insect Pests in Asia. Information Bulletin No. 57. (In En., Summaries in En, Fr.). International Crops Research Institute for the Semi-Arid Tropics, Patancheru, India. 99 pp.Google Scholar
Rombach, M. C. (1989) Production of Beauveria bassiana [Deuteromycotina, Hyphomycetes] sympoduloconidia in submerged culture. Entomophaga 34, 4552.Google Scholar
Schläger, S., Ulrichs, C., Srinivasan, R., Beran, F., Bhanu, K. R. M., Mewis, I. and Schreiner, M. (2012) Developing pheromone traps and lures for Maruca vitrata in Taiwan. Gesunde Pflanzen 64, 183186.Google Scholar
Sharma, H. C. (1998) Bionomics, host plant resistance, and management of the legume pod borer, Maruca vitrata – a review. Crop Protection 17, 373386.Google Scholar
Sharma, H. C., Saxena, K. B. and Bhagwat, V. R. (1999) The Legume Pod Borer, Maruca vitrata: Bionomics and Management. Information Bulletin No. 55. (In En., Summaries in En, Fr.). International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, India. 42 pp.Google Scholar
Singh, S. R. and Allen, D. J. (1979) Cowpea Pests and Diseases. Manual Series No. 2. IITA, Ibadan, Nigeria. 113 pp.Google Scholar
Singh, S. R. and Emden, H. F. V. (1979) Insect pests of grain legumes. Annual Review of Entomology 24, 255278.Google Scholar
Srinivasan, R. (2012) Integrating biopesticides in pest management strategies for tropical vegetable production. Journal of Biopesticides 5, 3645.Google Scholar
Tamò, M., Maniania, N. K. and Cherry, A. (2003) Biological control, a non-obvious component of IPM for cowpea, pp. 295309. In Biological Control in Integrated Pest Management Systems in Africa (edited by Neuenschwander, P., Borgemeister, C. and Langewald, J.). CABI Publishing, Oxford and Cambridge.Google Scholar
Taylor, T. A. (1967) The bionomics of Maruca testulalis Gey. (Lepidoptera: Pyralidae), a major pest of cowpeas in Nigeria. Journal of West Africa Science Association 12, 111129.Google Scholar
Ton, P. (2000) Endosulfan deaths and poisonings in Benin. Pesticides News 47, 1214.Google Scholar
Ulrichs, Ch., Mewis, I. and Schnitzler, W. H. (2001) Efficacy of neem and diatomaceous earth against cowpea aphids and their deleterious effect on predating Coccinelidae. Journal of Applied Entomology 125, 571575.Google Scholar
Usua, E. J. and Singh, S. R. (1979) Behaviour of cowpea pod borer, Maruca testulalis Geyer. Nigerian Journal of Entomology 3, 231239.Google Scholar
Vega, F. E., Meyling, N. V., Luangsa-ard, J. J. and Blackwell, M. (2012) Fungal entomopathogens, pp. 171–220. In Insect Pathology 2nd edn.Academic Press, London.Google Scholar
Vidal, C., Fargues, J., Lacey, L. A. and Jackson, M. A. (1998) Effect of various liquid culture media on morphology, growth, propagule production, and pathogenic activity to Bemisia argentifolii of the entomopathogenic Hyphomycete, Paecilomyces fumosoroseus. Mycopathologia 143, 3346.Google Scholar
Watson, D. W. and Petersen, J. J. (1993) Sexual activity of male Musca domestica (Diptera: Muscidae) infected with Entomophthora muscae (Entomophthoraceae: Entomophthorales). Biological Control 3, 2226.Google Scholar