Entomopathogenic fungi associated with cultivated honeybush, Cyclopia spp., in South Africa and their pathogenicity towards a leafhopper pest, Molopopterus sp. (Hemiptera: Cicadellidae)
DOI:
https://doi.org/10.17159/2254-8854/2023/a14183Keywords:
insect management, microbial control, pest managementAbstract
The southern and eastern parts of the African Fynbos region favour the production of honeybush tea. Honeybush biomass and extracts are used to prepare a beverage both locally and internationally, mainly as herbal tea with health benefits. Honeybush tea is mostly grown organically requiring natural control measures for pests and diseases. The leafhopper, Molopopterus sp., is one of the most important pests of cultivated honeybush in South Africa, as its feeding compromises the quality and quantity of the yield through leaf discolouration and reduction of the photosynthetic area. Local entomopathogenic fungi (EPF) can provide a pool of potential biocontrol agents for this pest. Therefore, a total of 98 soil samples were collected from organically grown honeybush fields and vegetation surrounding the honeybush fields in the Western Cape province of South Africa. Entomopathogenic fungi were isolated using the insect bait method and were characterised using molecular techniques. Twenty fungal isolates of Metarhizium anisopliae and Fusarium oxysporum were recovered from soil samples, of which 70% were from honeybush fields and 30% were from surrounding vegetation. Fusarium oxysporum isolates comprised 20% of the recovered isolates; M. anisopliae the remainder. Laboratory bioassays of the recovered isolates against adults and nymphs of the leafhopper, showed that F. oxysporum isolates caused 10–45% mortality and M. anisopliae isolates 30–80% mortality. Metarhizium anisopliae isolates J S1, KF S3, KF S11, KF S13, LS1 and LS2 were the most virulent and induced over 60% mortality in both nymphs and adults at a concentration of 1 × 107 conidia/ml.
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References
Aatif HM, Hanif MS, Raheel M, Ferhan, M, Mansha MZ, Khan AA, Ullah, MI, Shakeel Q, ali S. 2020. Temperature dependent virulence of the entomopathogenic nematodes against immatures of the oriental fruit fly, Bactrocera dorsalis Hendel (Diptera: Tephritidae). Egyptian Journal of Biological Pest Control 30:42–48. https://doi.org/10.1186/s41938-020-00248-7
Abaajeh AR. 2014. Evaluation of entomopathogenic fungi (ascomycota) for the control of Cydia pomonella (Lepidoptera: Tortricidae). Unpublished MSc thesis, Cape Penisula University of Technology.
Abbott WS. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18:265–267. https://doi.org/10.1093/jee/18.2.265a
Albertyn S, Moore SD, Marsberg T, Coombes CA, Hill MP. 2021. The influence of citrus orchard age on the ecology of entomopathogenic fungi and nematodes. Biocontrol Science and Technology 31: 80-96. https://doi.org/10.1080/09583157.2020.1830949
Ali-Shtayeh MS, Mara’i, AB, Jamous RM. 2003. Distribution, occurrence and characterization of entomopathogenic fungi in agricultural soil in the Palestinian area. Mycopathologia 156:235–244. https://doi.org/10.1023/a:1023339103522
Andow D. 1983. The extent of monoculture and its effects on insects. Agriculture, Ecosystems and Environment 9:25–35. https://doi.org/10.1016/0167-8809(83)90003-8
Anwar W, Haider MS, Shadid AA, Mushtaq H, Hameed U, Reham MZ, Iqbal M J. 2017. Genetic diversity of Fusarium isolated from members of Sternorrhyncha (Hemiptera): Entomopathogens against Bemisia tabaci. Pakistan Journal of Zoology 49:639–645. https://doi.org/10.17582/journal.pjz/2017.49.2.639.645
Asensio L, Carbonell T, Lopez-Jimenez JA, López-Llorca LV. 2003. Entomopathogenic fungi in soils from Alicante province [Spain]. Spanish Journal of Agricultural Research 1:37–45. https://doi.org/10.5424/sjar/2003013-33
Barra P, Rosso L, Nesci A, Etcheverry M. 2012. Isolation and identification of entomopathogenic fungi and their evaluation against Tribolium confusum, Sitophilus zeamais, and Rhyzopertha dominica in stored maize. Journal of Pest Science 86:217–226. https://doi.org/10.1007/s10340-012-0460-z.
Bayissa W, Ekesi S, Mohamed SA, Kaaya GP, Wagacha JM, Hanna R, Maniania NK. 2017. Selection of fungal isolates for virulence against three aphid pest species of crucifers and okra. Journal of Pest Science 90:355–368. https://doi.org/10.1007/s10340-016-0781-4.
Bidochka MJ, Kamp AM, Lavender M, Dekoning J, Croos ADE. 2001. Habitat association in two genetic groups of the insect-pathogenic fungus. Society 67:1335–1342. https://doi.org/10.1128/AEM.67.3.1335-1342.2001
Bidochka NJ, Kasperski JE, Wild GA. 1998. Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Canada Journal of Botany 76:1198–1204. https://doi.org/10.1139/b98-115
Boomsma JJ, Jensen AB, Meyling NV, Eilenberg J. 2014. Evolutionary interaction networks of insect pathogenic Fungi. Annual Review of Entomology 59:171–220. https://doi.org/10.1146/annurev-ento-011613-162054
Department of Agriculture, Forestry and Fisheries (DAFF). 2014. Honebush Tea. Pretoria. [accessed 20/01/2022]. https://www.dalrrd.gov.za/Portals/0/Brochures%20and%20Production%20guidelines/honey%20bush%20tea.pdf
Dlamini BE, Malan AP, Addison P. 2020. Entomopathogens from agricultural soil and their potential to control the banded fruit weevil, Phlyctinus callosus (Schönherr) (Coleoptera: Curculionidae). African Entomology 28:374–384. https://doi.org/10.4001/003.028.0374
Feng-Yan B, Quing-Tao C. 1991. Fusarium species on some insects from China. Acta Mycologica 10:120–128. https://doi.org/10.3390/pathogens7040093
Ganassi S, Moretti A, Stornelli C, Fratello B, Bonvicini Pagliai AM, Logrieco A, Sabatini MA. 2001. Effect of Fusarium, Paecilomyces and Trichoderma formulations against aphid Schizaphis graminum. Mycopathologia 151:131–138. https://doi.org/10.1023/A:10179406 04692
Goble TA, Dames JF, Hill MP, Moore SD. 2010. The effects of farming system, habitat type and bait type on the isolation of entomopathogenic fungi from citrus soils in the Eastern Cape Province, South Africa. BioControl 55:399–412. https://doi.org/10.1007/s10526-009-9259-0
Gul HT, Freed S, Akmal M, Malik MN. 2015. Vulnerability of different life stages of Bactrocera zonata (Tephritidae: Diptera) against entomogenous fungi. Pakistan Journal of Zoology 47:307–317.
Habibi J, Backus EA, Coudron TA, Brandt SL. 2001. Effect of different host substrates on hemipteran salivary protein profiles. Entomologia Experimentalis et Applicata 98:369–375. https://doi.org/10.1023/A:1018971827110
Hatting JL. 2017. Major insect pests and their natural enemies associated with cultivation of Rooibos, Aspalathus linearis ( Burm . f .) R. Dahlgren , in South Africa : A review. South African Journal of Botany 110:118–123. https://doi.org/10.1016/j.sajb.2016.07.01
Hazarika L, Puzari KC. 2001. Microbials in tea pest management. Ignacimuthu I, Sen A, editors. Microbials in Insect Pest Management. Oxford, New Dehli. 98–104 pp.
Hussain A, Rizwan-Ul-Haq M, Al-Ayedh H, Al-Jabr A. 2014. Mycoinsecticides: Potential and future perspective. Recent Patents on Food, Nutrition & Agriculture 6:45–53. https://doi.org/10.2174/2212798406666140613113905
Inglis GD, Enkerli J, Goettel MS. 2012. Laboratory techniques used for entomopathogenic fungi. Hypocreales. Manual of Techniques in Invertebrate Pathology (2nd ed). Elsevier. 189–253 pp.
Joubert E, Joubert ME, Bester C, De Beer D, De Lange JH. 2011. Honeybush (Cyclopia spp.): From local cottage industry to global markets - The catalytic and supporting role of research. South African Journal of Botany 77:887–907. https://doi.org/10.1016/j.sajb.2011.05.014
Keller S, Kessler P, Schweizer C. 2003. Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metharhizium anisopliae. BioControl 48:307–319. https://doi.org/10.1023/A:1023646207455.
Khan S, Guo L, Maimaiti Y, Mijit M, Qiu D. 2012. Entomopathogenic fungi as microbial biocontrol agent. Molecular Plant Breeding 3:63–79. https://doi.org/10.5376/mpb.2012.03. 0007
Klingen I, Eilenberg J, Meadow R. 2002. Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agriculture, Ecosystems and Environment 91:191–198. https://doi.org/10.1016/s0167-8809(01)00227-4
Marzachi C, Veratti F, Bosco D. 1998. Direct PCR detection of phytoplasmas in experimentally infected insects. Annals of Applied Biology 133:45–54. https://doi.org/10.1111/j.1744-7348.1998.tb05801.x
Mascarin GM, Lopes RB, Delalibera Í, Fernandes ÉKK, Luz C, Faria M. 2019. Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil. Journal of Invertebrate Pathology 165:46–53. https://doi.org/10.1016/j.jip.2018 .01.001
Mbangcolo MM. 2008. Aspects of honeybush tea (Cyclopia Species) propagation. [MSc thesis]. Stellenbosch: Stellenbosch University
Mcgregor GK. 2018. The wild Honeybush harvesting field guide. Capetown. [accessed 7 May 2019]. https://gouritz.com/wp-content/uploads/2019/02/Honeybush-harvesting-Eng_Wild-honey bush-harvesting-field-guide_McGregor-2018-compressed.pdf
Mendiburu F, Muhammad Y. 2020. agricolae: Statistical procedures for agricultural research.R package version 1.4.0.
Metcalf E, Sephton M, Lands L, Brunette D. 2018. Overview of the keurboom moth’ (Leto venus) and its Impact on Cultivated Cyclopia ( Honeybush ) plantations in South Africa. Grounded, Cape Town. [accessed 21 May 2019]. https://grounded.co.za/what-is-so-great-about-honeybush/
Meyling N. 2007. Methods for isolating entomopathogenic fungi from the soil environment. Department of Ecology, Faculty of Life Sciences, University of Copenhagen, Denmark. [accessed: 12 January 2021] http://orgprints.org/11200/1/11200.pdf
Meyling NV, Elenberg J. 2006. Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agriculture, Ecosystems and Environment 113:336–341. https://doi.org/10.1016/j.agee.2005.10.011
Mochi DA, Monteiro CA, Barbosa JC. 2005. Action of pesticides to Metarhizium anisopliae in soil. Neotropical Entomology 34:961–971. https://doi.org/10.1590/S1519-566X2005000600013
Navarro-Velasco GY, Prados-Rosales RC, Oritz-Urquiza A, Quesada-Moraga E, Di Pietro A. 2011. Gallleria mallonella as model host for the trans-kingndom pathogen Fusarium oxysprorum. Fungal Genetics and Biology 48:1124–1129. https://doi.org/10.1016/j.fgb .2011.08.004
North MS, Joubert E, Beer DE, Kock K, Joubert ME. 2017. Effect of harvest date on growth, production and quality of Honeybush (Cyclopia genistoides and C. subternata). South African Journal of Botany 110:132–137. https://doi.org/10.1016/j.sajb.2016.08.002
O’Donnell K, Mccormick SP, Busman M, Proctor RH, Todd JW, Gail D, David MG, Johanna FA, John PR. 2018. Marasas et al. 1984 “Toxigenic Fusarium Species: Identity and Mycotoxicology” revisited. Mycologia 52:1–23. https://doi.org/10.1080/00275514.2018. 1519773
Olivier CY, Vincent C, Saguez J, Galka B, Weintraub PG, Maixner M. (2012). Leafhoppers and Planthoppers: Their Bionomics, Pathogen Transmission and Management in Vineyards, In Bostanian NJ, Vincent C, Isaacs R, editors Arthropod Management in Vineyards: Pests, Approaches, and Future Directions, Springer Dordrecht, The Netherlands, p. 253-270.
Quesada-Moraga E, Navas-Cortés JA, Maranhao EAA, Ortiz-Urquiza A, Santiago-Álvarez C. 2007. Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycological Research 111:947–966. https://doi.org/10.1016/j.mycres.2007.06.006
Rath AC, Koen TB, Yip HY. 1992. The influence of abiotic factors on the distribution and abundance of Metarhizium anisopliae in Tasmanian pasture soils. Mycological Research 96:378–384. https://doi.org/10.1016/S0953-7562(09)80956-8
Sain SK, Monga D, Kumar R, Nagrale DT, Kranthi S, Kranthi KR. 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 29:1–11. https://doi.org/10.1186/s41938-019-0130-z
Santos AC, Da S, Diniz AG, Tiago PV, Oliveira NT . 2020. Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects. Fungal Biology Reviews 34:41–57. https://doi.org/10.1016/j.fbr.2019.12.002
Schutte AL. 1995. Systematics of the genus Cyclopia vent. (Fabaceae, Podalyrieae). Edinburgh Journal of Botany 54:125–170. https://doi.org/10.1017/S0960428600004005
Sharma L, Marques G. 2018. Fusarium, an entomopathogen—a myth or reality? Pathogens 7: 93–100. https://doi.org/10.3390/pathogens7040093.
Slabbert EL, Malgas RR, Veldtman R, Addison P. 2019. Honeybush (Cyclopia spp.) phenology and associated arthropod diversity in the Overberg region, South Africa. Bothalia 49:a2430. https://doi.org/10.4102/abc.v49i1.2430
Thangam SD, Selvakumar G, Verghese A, Kamala Jayanthi PD. 2014. Natural mycosis of mango leafhoppers (Cicadellidae: Hemiptera) by Fusarium sp. Biocontrol Science and Technology 24:229–232. https://doi.org/10.1080/09583157.2013.851171
Thomas MB, Read AF. 2007. Can fungal biopesticides control malaria? Nature Reviews Microbiology 5:377–383. https://doi.org/10.1038/nrmicro1638
Tkaczuk C, Krzyczkowski T, Wegensteiner R. 2013. The occurrence of entomopathogenic fungi in soils from mid-field woodlots and adjacent small-scale arable fields. Acta Mycologica 47:191–202. https://doi.org/10.5586/am.2012.024
Tounou AK, Agboka K, Poehling HM, Raupach K, Langewald J, Zimmermann G, Borgemeister C. 2003. Evaluation of the entomopathogenic fungi Metarhizium anisopliae and Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) for control of the Green Leafhopper Empoasca decipiens (Homoptera: Cicadellidae) and potential side effects on the egg parasitoid Anagrus atomus (Hymenoptera: Mymaridae). Biocontrol Science and Technology 13:715–728. https://doi.org/10.1080/09583150310001606534
van Diepeningen AD, de Hoog GS. (2016). Challenges in Fusarium, a Trans-Kingdom Pathogen. Mycopathologia, 181:161–163. https://doi.org/10.1007/s11046-016-9993-7
Wang Q, Gong X, Li P, Lai D, Zhou L. 2018. Structural diversity and biological activities of cyclic depsipeptides form fungi. Molecules 23:169–172. https://doi.org/10.3390/molecules 23010169
Wang Q, Xu L. 2012. Beauvericin, a bioctive compound produced by fungi: A short review. Molecules 17:2367–2377. https://doi.org/10.3390/molecules17032367.
Zimmermann G. 2007. Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Science and Technology 17:879–920. https://doi.org/10.1080/09583150701593 963
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