Helicoverpa armigera is a key insect pest of tomatoes reducing drastically yields. The effect of the endophytic colonization of tomato plants by Beauveria bassiana using leaf spray as an inoculation method on damage and survival of H. armigera was assessed in a screen house. Two B. bassiana isolates (Bb 115 and Bb 11) and two tomato varieties (a local variety Tounvi and an improved variety Padma) were included in the study. The adaxial and abaxial leaf surfaces were sprayed at a concentration of 107 conidia/ml and 109 conidia/ml for each isolate and each of the two tomato varieties. Thirty days after inoculation, five discs of tomato leaf and tomato root were cut for each isolate, each concentration per isolate and for each variety. The samples were incubated at room temperature (28°C ± 2°C) and periodically checked for fungal growth. Larval survival was checked and a damage assessment was done on tomato flowers and the leaves. The results show that the lowest Mean Survival Times (MSTs) were recorded on larvae feeding on plants inoculated with Bb 11 (4.2 ± 0.8 days against 11.5 ± 0.2 days for control). Compared to the other treatments, low damage rates of the flowers of the improved variety inoculated with Bb 11 at 109 conidia/ml were recorded from the 6th Day After Inoculation (DAI). This rate remains low until the end of treatment. Overall flower damage was lower than leaf damage. The results showed large differences in pathogenicity, with most endophytic isolate belonging to Bb 11 when inoculated at 109 conidia/ml using the leaf spraying technique. Data were discussed with regard to the use of endophytism B. bassiana in an integrated tomato pest control approach.
References
[1]
FAOSTAT (2019) Agricultural Production, Crop Primary Database. Food and Agriculture Organization of United Nation, Rome. http://www.fao.org/statistic
[2]
Sawadogo, I., Koala, M., Dabire, C., et al. (2015) Etude de l’influence des modes de transformation sur les teneurs en lycopène de quatre variétés de tomates de la région du nord du Burkina Faso. International Journal of Biological and Chemical Sciences, 9, 362-370. https://doi.org/10.4314/ijbcs.v9i1.31
[3]
Assogba Komlan, F., Sikirou, R. and Azagba, J. (2013) Comment réussir la culture de la tomate en toute saison: Cas des régions urbaines et périurbaines du Sud-Bénin. 2ème Edition, Référentiel Technico Economique, INRAB, 58 p.
[4]
Douro Kpindou, O.K., Djegui, D.A., Glitho, I.A. and Tamo, M. (2013) Comparative Study of the Efficacy of Entomopathogenic Fungi, Chemicals and Botanical Pesticides in the Management of Cotton Pests and Their Natural Enemies in Benin. International Journal of Advanced Science and Technology, 3, 21-33.
[5]
Tariku Tesfaye, E. (2018) Review on Bio-Intensive Management of African Bollworm, Helicoverpa armigera (Hub.): Botanicals and Semiochemicals Perspectives. Journal of Agricultural, Food and Environmental Sciences, 14, 1-9. https://doi.org/10.5897/AJAR2017.12832
[6]
Sinzogan, A.A.C., Kossou, D.K., Atachi, P. and van Huis, A. (2006) Participatory Evaluation of 130 Synthetic and Botanical Pesticide Mixtures for Cotton Bollworm Control. International Journal of Tropical Insect Science, 26, 246-255. https://doi.org/10.1017/S1742758406415691
[7]
James, B., Godonou, and Atcha-Ahowe, C. (2009) Promoting Biopesticide Candidates from Experimental to Commercial Level for Sustainable Vegetable Production. Pesticides Management in West Africa, No. 7, 62 p.
[8]
Torres-Vila, L.M., Rodriguez-Molina, M.C., Lacasa-Plasencia, A., et al. (2002) Pyrethroid Resistance of Helicoverpa armigera in Spain: Current Status and Agroecological Perspective. Agriculture, Ecosystems & Environment, 93, 55-66. https://doi.org/10.1016/S0167-8809(02)00003-8
[9]
Herrero, M.I., Fogliata, S.V., Vera, A., et al. (2018) Biological Characterization and Mating Compatibility of Helicoverpa gelotopoeon (D.) (Lepidoptera: Noctuidae) Populations from Different Regions in Argentina. Bulletin of Entomological Research, 108, 108-115. https://doi.org/10.1017/S000748531700058X
[10]
Martin, T., Chandre, F., Ocho, O.G., et al. (2002) Pyrethroid Resistance Mechanisms in the Cotton Bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) from West Africa. Pesticide Biochemistry and Physiology, 74, 17-26. https://doi.org/10.1016/S0048-3575(02)00117-7
[11]
Tossou, E., Tepa-Yotto, G., Douro Kpindou, O.K., et al. (2019) Susceptibility Profiles of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) to Deltamethrin Reveal a Contrast between the Northern and the Southern Benin. International Journal of Environmental Research and Public Health, 16, 1882-1896. https://doi.org/10.3390/ijerph16111882
[12]
Djihinto, A.C., Katary, A., Djaboutou, M.C., et al. (2012) Variation in Biological Parameters of Cypermethrin Resistant and Susceptible Strains of Helicoverpa armigera from Benin Republic, West Africa. International Journal of Biological and Chemical Sciences, 6, 931-940. https://doi.org/10.4314/ijbcs.v6i3.2
[13]
Koch, E. and Roberts, S.J. (2014) Non-Chemical Seed Treatment in the Control of Seed-Borne Pathogens. In: Gullino, M. and Munkvold, G., Eds., Global Perspectives on the Health of Seeds and Plant Propagation Material. Plant Pathology in the 21st Century (Contributions to the 9th International Congress), Vol. 6, Springer, Dordrecht, 105-123. https://doi.org/10.1007/978-94-017-9389-6_8
[14]
Mccoy, C.W., Shapiro, W.D. and Ducan, L.W. (2000) Application and Evaluation of Entomopathogens for Citrus Pest Control. In: Lacy, L.A. and Kaya, H.K., Eds., Field Manual of Techniques in Invertebrates: Application and Evaluation of Pathogens for Insects and Other Invertebrate Pests, Kluwer Academic Publishers, Dordrecht, 33. https://doi.org/10.1007/978-94-017-1547-8_25
[15]
Sabbour, M.M. and Sahab, A.F. (2005) Efficacy of Some Microbial Control Agents against Cabbage Pests in Egypt. Pakistan Journal of Biological Sciences, 8, 1351-1356. https://doi.org/10.3923/pjbs.2005.1351.1356
[16]
Daisy, B.H., Strobel, G.A., Castillo, U., et al. (2002) Naphthalene, an Insect Repellent, Is Produced by Muscodor vitigenus, a Novel Endophytic Fungus. Microbiology, 148, 3737-3741. https://doi.org/10.1099/00221287-148-11-3737
[17]
Mcguire, M.R., Ulloa, M, Park, Y.H. and Hudson, N. (2005) Biological and Molecular Characteristics of Beauveria bassiana Isolates from California Lygus hesperus (Hemiptera: Miridae) Populations. Biological Control, 33, 307-314. https://doi.org/10.1016/j.biocontrol.2005.03.009
[18]
Toffa, M.J., Loko, Y.L.E., Douro, K.O., et al. (2020) Management of the Legume Pod Borer Maruca vitrata Fabricius (Lepidoptera: Crambidae) with Field Applications of the Entomopathogenic fungus Beauveria bassiana and a Mixed Formulation of the Baculovirus MaviMNPV with Emulsifiable Neem Oil. African Journal of Agricultural Research, 15, 113-121. https://doi.org/10.5897/AJAR2019.14391
[19]
Toffa, J., Loko, Y.L.E., Douro Kpindou, O.K., et al. (2021) Endophytic Colonization of Tomato Plants by Beauveria bassiana Vuillemin (Ascomycota: Hypocreales) and Leaf Damage in Helicoverpa armigera Larvae (Hübner) (Lepidoptera: Noctuidae). Egyptian Journal of Biological Pest Control, 31, 1-9. https://doi.org/10.1186/s41938-021-00431-4
[20]
Dannon, H.F., Dannon, A.E., Douro-Kpindou, O.K., et al. (2020) Toward the Efficient Use of Beauveria bassiana in Integrated Cotton Insect Pest Management. Journal of Cotton Research, 3, 1-21. https://doi.org/10.1186/s42397-020-00061-5
Quesada-Moraga, E., Lopez-Diaz, C. and Beatriz landa, B. (2014) The Hidden Habit of the Entomopathogenic Fungus Beauveria bassiana: First Demonstration of Vertical Plant Transmission. PLOS ONE, 9, e89278. https://doi.org/10.1371/journal.pone.0089278
[23]
Van Bael, S.A., Maynard, Z., Robbins, N., et al. (2005) Emerging Perspectives on the Ecological Roles of Endophytic Fungi in Tropical Plants. In: Dighton, J., Oudemans, P. and White, J., Eds., The Fungal Community: Its Organization and Role in the Ecosystem, 3rd Edition, CRC, Taylor and Francis Group, Boca Raton, 181-193. https://doi.org/10.1201/9781420027891.ch9
[24]
Vega, F.E., Goettel, M.S., Blackwell, M., et al. (2009) Fungal Entomopathogens: New Insights on Their Ecology. Fungal Ecology, 2, 149-159. https://doi.org/10.1016/j.funeco.2009.05.001
[25]
Jalgaonwala, R.E., Mohite, B.V. and Mahajan, R. (2011) A Review: Natural Products from Plant Associated Endophytic Fungi. Journal of Microbiology and Biotechnology Research, 1, 21-32.
[26]
Ownley, B.H., Pereira, R.M., Klingeman, W.E., et al. (2004) Beauveria bassiana, a Dual Purpose Biocontrol Organism, with Activity against Insect Pests and Plant Pathogens. In: Lartey, R.T. and Cesar, A.J., Eds., Emerging Concepts in Plant Health Management, Research Signpost, Trivandrum, 255-269.
Saour, G. and Causse, R. (1996) Comportement alimentaire des chenilles d’Helicoverpa armigera Hbn (Lep. Noctuidae) sur la tomate cultivée sous serre. Journal of Applied Entomology, 120, 87-92. https://doi.org/10.1111/j.1439-0418.1996.tb01571.x
[29]
Douro Kpindou, O.K.K., Djegui, D.A., Glitho, I.A. and Tamò, M (2012) Réponse des stades larvaires de Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) à l’application de champignons entomopathogènes Metarhizium anisopliae et Beauveria bassiana. Biotechnology, Agronomy and Society and Environment, 16, 283-293.
[30]
Toffa, M.J., Atachi, P., Douro Kpindou, O., et al. (2014) Mortality of Maruca vitrata (Lepidoptera: Crambidae) Larval Stages Induced by Different Doses of the Entomopathogenic Fungi Metarhizium anisopliae and Beauveria bassiana. International Journal of Advanced Research, 2, 273-285.
[31]
Agboyi, L.K., Ketoh, G.K., Douro Kpindou, O.K., et al. (2020) Improving the Efficiency of Beauveria bassiana Applications for Sustainable Management of Plutella xylostella (Lepidoptera: Plutellidae) in West Africa. Biological Control, 144, Article ID: 104233. https://doi.org/10.1016/j.biocontrol.2020.104233
[32]
Harekrushna, S., Totan, A. and Arup, K.M. (2018) Novel Trichoderma Strains Isolated from Tree Barks as Potential Biocontrol Agents and Bio Fertilizers for Direct Seeded Rice. Microbiological Research, 214, 83-90. https://doi.org/10.1016/j.micres.2018.05.015
[33]
Goettel, M. and Inglis, G. (1997) Fungi: Hyphomycetes. In: Lacey, L.A., Ed., Manual of Techniques in Insect Pathology, Academic Press, London, 213-249. https://doi.org/10.1016/B978-012432555-5/50013-0
[34]
Institut National des Recherches Agricoles du Bénin (INRAB) (2020) Effet des dates de repiquage sur l’incidence et la sévérité de la virose et sur la productivité de tomate améliorée en période de contre saison au Sud Bénin. Filière Produits maraichers. https://inrab.org/filièreproduitsmaraichers
[35]
Assogba Komlan, F., Sikirou, R., Tiemoko, Y., et al. (2016) La culture de la tomate au Bénin. Dépôt légal N° 8550 du 19 Février, 1er trimestre 2016, Bibliothèque Nationale (BN), 16 p.
[36]
Brownbridge, M., Reay, S.D., Nelson, T.L. and Glare, T.R. (2012) Persistence of Beauveria bassiana (Ascomycota: Hypocreales) as an Endophyte Following Inoculation of Radiata Pine Seed and Seedlings. Biological Control, 61, 194-200. https://doi.org/10.1016/j.biocontrol.2012.01.002
[37]
Resquin-Romero, G., Garrido-Jurado, I. and Quesada-Moraga, E. (2016) Combined Use of Entomopathogenic Fungi and Their Extracts for the Control of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Biological Control, 92, 101-110. https://doi.org/10.1016/j.biocontrol.2015.10.007
[38]
Qayyum, M.A., Wakil, W., Arif, M.J. and Dunlap, C.A. (2015) Infection of Helicoverpa armigera by Endophytic Beauveria bassiana Colonizing Tomato Plants. Biological Control, 10, 1-30. https://doi.org/10.1016/j.biocontrol.2015.04.005
[39]
Kasambala, D., Vega, F. and Klingen, I. (2018) Establishment of the Fungal Entomopathogen Beauveria bassiana as an Endophyte in Sugarcane, Saccharum officinarum. Fungal Ecology, 35, 70-77. https://doi.org/10.1016/j.funeco.2018.06.008
[40]
Arnold, A.E., Maynard, Z., Gilbert, G.S., et al. (2000) Are Tropical Fungal Endophytes Hyper Diverse. Ecology Letters, 3, 267-274. https://doi.org/10.1046/j.1461-0248.2000.00159.x
[41]
Petrini, O. and Fisher, P.J. (1986) Fungal Endophytes in salicornia perennis. Transactions of the British Mycological Society, 87, 647-828. https://doi.org/10.1016/S0007-1536(86)80109-7
[42]
Allegrucci, N., Velazquez, M., Russo, M.L., et al. (2017) Endophytic Colonisation of Tomato by the Entomopathogenic Fungus Beauveria bassiana: The Use of Different Inoculation Techniques and Their Effects on the Tomato Leafminer Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Plant Protection Research, 57, 331-337. https://doi.org/10.1515/jppr-2017-0045
[43]
Ma, X., Liu, X., Ning, X., et al. (2008) Effects of Bacillus thuringiensis Toxin Cry1Ac and Beauveria bassiana on Asiatic Corn Borer (Lepidoptera: Crambidae). Journal of Invertebrate Pathology, 99, 123-128. https://doi.org/10.1016/j.jip.2008.06.014
[44]
Posada, F.J., Aime, M.C., Peterson, S.W., et al. (2007) Inoculation of Coffee Plants with the Fungal Entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycological Research, 111, 748-757. https://doi.org/10.1016/j.mycres.2007.03.006
[45]
Tefera, T. and Vidal, S. (2009) Effect of Inoculation Method and Plant Growth Medium on Endophytic Colonization of Sorghum by the Entomopathogenic Fungus Beauveria bassiana. Biocontrol, 54, 663-669. https://doi.org/10.1007/s10526-009-9216-y
[46]
Ownley, B.H., Griffin, M.R., Klingeman, W.E., et al. (2008) Beauveria bassiana: Endophytic Colonization and Plant Disease Control. Journal of Invertebrate Pathology, 98, 267-270. https://doi.org/10.1016/j.jip.2008.01.010
[47]
Vidal, S. and Jaber, L.R. (2015) Entomopathogenic Fungi as Endophytes: Plant-Endophyte-Herbivore Interactions and Prospects for Use in Biological Control. Current Science, 109, 46-54.
[48]
Shikano, I. (2017) Evaluationary Ecology of Multitrophic Interactions between Plants, Insect Herbivorees and Entomopathogens. Journal of Chemical Ecology, 43, 586-598. https://doi.org/10.1007/s10886-017-0850-z
[49]
Lopez, D. and Sword, G.A. (2015) The Endophytic Fungal Entomopathogens Beauveria bassiana and Purpureocillium lilacinum Enhance the Growth of Cultivated Cotton (Gossypium hirsutum) and Negatively Affect Survival of the Cotton Bollworm (Helicoverpa zea). Biological Control, 89, 53-60. https://doi.org/10.1016/j.biocontrol.2015.03.010
[50]
Hu, G. and Leger, R.J. (2002) Field Studies Using a Recombinant Mycoinsecticide (Metarhizium anisopliae) Reveal That It Is Rhizosphere Competent. Applied and Environmental Microbiology, 68, 6383-6387. https://doi.org/10.1128/AEM.68.12.6383-6387.2002
[51]
Quesada-Moraga, E., Munoz-Ledesma, F. and Santiago-Alvarez, C. (2009) Systemic Protection of Papaver somniferum L. against Iraellaluteipes (Hymenoptera: Cynipidae) by an Endophytic Strain of Beauveria bassiana (Ascomycota: Hypocreales). Environmental Entomology, 38, 723-730. https://doi.org/10.1603/022.038.0324
[52]
Bacon, C.W. and Hinton, D.M. (2007) Potential for Control of Seedling Blight of Wheat Caused by Fusarium graminearum and Related Species Using the Bacterial Endophyte Bacillus mojavensis. Biocontrol Science and Technology, 17, 81-94. https://doi.org/10.1080/09583150600937006
[53]
Gurulingappa, P., Sword, G.A., Murdoch, G. and Mcgee, P.A. (2010) Colonization of Crop Plants by Fungal Entomopathogens and Their Effects on Two Insect Pests When in Planta. Biological Control, 55, 34-41. https://doi.org/10.1016/j.biocontrol.2010.06.011
[54]
Cherry, A.J., Banito, A., Djegui, D. and Lomer, C. (2004) Suppression of the Stem-Borer Sesamia calamistis (Lepidoptera: Noctuidae) in Maize Following Seed Dressing, Topical Application and Stem Injection with African Isolates of B. bassiana. International Journal of Pest Management, 50, 67-73. https://doi.org/10.1080/09670870310001637426
[55]
Bacon, C.W. and Hinton, D.M. (1996) Symptomless Endophytic Colonization of Maize by Fusarium moniliforme. Canadian Journal of Botany, 74, 1195-1202. https://doi.org/10.1139/b96-144
[56]
Jaber, L.R. (2015) Grapevine Leaf Tissue Colonization by the Fungal Entomopathogen Beauveria bassiana and Its Effect against Downy Mildew. Biocontrol, 60, 103-112. https://doi.org/10.1007/s10526-014-9618-3
