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Efficacy of indigenous entomopathogenic fungi against the black aphid, Aphis fabae Scopoli under controlled conditions in Tanzania

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Abstract

Worldwide application of synthetic insecticides as a main way of controlling aphids on various crops has resulted in diverse problems such as failures in pest control, negative public health and environmental impacts, and a build-up of resistance against insecticides by insect pests. Entomopathogenic fungi can be used as an alternative to insecticides since they offer the benefit of being environmentally friendly, without the risk of insect pests developing resistance. This study assessed 19 different indigenous fungi in the laboratory for their ability to control Aphis fabae Scopoli at various conidial concentrations (104, 105, 106 and 107 spores/ml) using the detached leaf method. A. fabae adults were reared on potted cowpea in cages. Both the 19 fungus types and their respective conidial concentrations used to treat A. fabae differed significantly (P < 0.001) in their ability to kill the pest. The A. fabae mortality rate increased in line with the increase in the conidial concentration of the fungus type, and Aspergillus flavus Link S18 and S19 performed better than the other fungus types evaluated. Aspergillus flavus S18 and S19 are recommended for further tests in the greenhouse to validate the laboratory results. The fact that the Aspergillus strains isolated and tested were all aflatoxin-producing strains calls for caution regarding their potential impacts on human and animal health. Further studies are recommended to conduct similar experiments using non-aflatoxin-producing strains of A. flavus, in order to determine whether they have similar effects on A. fabae.

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References

  • Allan M, Christian U, Nguya MK, Sunday E (2016) Integration of entomopathogenic fungi as biopesticide for the management of cowpea aphid (Aphis craccivora Koch). Afr J Hort Sci 9:14–31

    Google Scholar 

  • Asi MR, Bashir MH, Afzali M, Imran S (2009) Effect of conidial concentration of entomopathogenic fungi on mortality of cabbage aphid, Brevicoryne brassicae L. Pak J Life Soc Sci 2:175–180

    Google Scholar 

  • Butt TM, Jackson C, Magan N (2002) Fungi as biocontrol agents: progress, problems and potential. Plant Pathol 51:518–521

    Google Scholar 

  • Carson R (1962) Silent Spring. Houghton Mifflin Company, Boston

    Google Scholar 

  • Chen B, Li ZY, Feng MG (2008) Occurrence of entomopathogenic fungi in migratory alate aphids in Yunnan Province of China. BioControl 53:317–326. https://doi.org/10.1007/s10526-006-9063-z

    Article  Google Scholar 

  • Clarkson JM, Chamley AK (1996) New insights into the mechanisms of fungal pathogenesis in insects. Trends Microbiol 4(5):197–203

    Article  CAS  Google Scholar 

  • Cotty PJ, Bhatnagar D (1994) Variability among atoxigenic Aspergillus flavus strains in ability to prevent aflatoxin contamination and production of aflatoxin biosynthetic pathway enzymes. Appl Environ Microbiol 60:2248–2251

    Article  CAS  Google Scholar 

  • de Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256

    Article  Google Scholar 

  • de Mendiburu F, de Mendiburu MF (2013) Agricolae: statistical procedures for agricultural research. R Package Version 1.1–4. http://CRAN.R-project.org/package=agricolae

  • Dharam PA, Shankar U (2012) History, overview and principles of ecologically-based Pest management. In: Dharam PA, Shankar U (eds) Integrated pest management: principles and practice. CAB International, Wallingford

    Google Scholar 

  • Domier LL, Steinlage TA, Hobbs HA, Wang Y, Herrera-Rodriguez G, Haudenshield JS, McCoppin NK, Hartman GL (2007) Similarities in seed and aphid transmission among soybean mosaic virus isolates. Plant Dis 91:546–550

    Article  CAS  Google Scholar 

  • Ehrlich KC (2014) Non-aflatoxigenic Aspergillus flavus to prevent aflatoxin contamination in crops: advantages and limitations. Front Microbiol 5:50. https://doi.org/10.3389/fmicb.2014.00050

    Article  PubMed  PubMed Central  Google Scholar 

  • Foster SP, Devine G, Devonshire AL (2007) Insecticide resistance. In: Van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, London. 716 pp

    Google Scholar 

  • Frisvad JC, Hubka V, Ezekiel CN, Hong S-B, Nováková A, Chen AJ, Arzanlou M, Larsen TO, Sklenár F, Mahakarnchanakul W, Samson RA, Houbraken J (2019) Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins. Stud Mycol 93:1–63. www.studiesinmycology.org

    Article  CAS  Google Scholar 

  • Gogo EO, Saidi M, Ochieng JM, Martin T, Baird V, Ngouajio M (2014) Microclimate modification and insect pest exclusion using Agronet improve pod yield and quality of French bean. Hortscience 49(10):1298–1304

    Article  Google Scholar 

  • Gomes EA, Kasuya MCM, de Barros EG, Borges AC, Araújo EF (2002) Polymorphism in the internal transcribed spacer (ITS) of the ribosomal DNA of 26 isolates of ectomycorrhizal fungi. Genet Mol Biol 25:477–483

    Article  CAS  Google Scholar 

  • Gong YY, Watson S, Routledge MN (2016) Aflatoxin exposure and associated human health effects, a review of epidemiological studies. Food Saf 4:14–27

    Article  Google Scholar 

  • Gourama H, Bullerman LB (1995) Aspergillus flavus and Aspergillus parasiticus: aflatoxigenic fungi of concern in foods and feeds: a review. J Food Protect 58(12):1395–1404

    Article  CAS  Google Scholar 

  • Guchi E (2015) Implication of aflatoxin contamination in agricultural products. Am J Food Nutr 3(1):12–20

    CAS  Google Scholar 

  • Harmanto HJT, Salokhe VM (2006) Influence of insect screens with different mesh sizes on ventilation rate and microclimate of greenhouses in the humid tropics. Agricultural Engineering International: the CIGR Ejournal. Manuscript BC 05 017. Vol. VIII

  • Henry T, Iwen PC, Hinrichs SH (2000) Identification of Aspergillus species using internal transcribed spacer regions 1 and 2. J Clin Microbiol 38:1510–1515

    Article  CAS  Google Scholar 

  • Hogenhout SA, Ammar E-D, Whitefield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359

    Article  CAS  Google Scholar 

  • Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems, and potential. CAB International, Wallingford, pp 23–69

    Chapter  Google Scholar 

  • Karungi J, Nampala MP, Adipala D, Kyamanywa S, Ogenga-Latigo MW (1999) Population dynamics of selected cowpea insect pests as influenced by different management practices in eastern Uganda. Afr Crop Sci J 7(4):487–495

    Google Scholar 

  • Lacey L, Grzywacz D, Shapiro-Ilan D, Frutos R, Brownbridge M, Goettel M (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41

    Article  CAS  Google Scholar 

  • Lewis I, Onsongo M, Njapau H, Schurz-Rogers H, Luber G, Kieszak S, Nyamongo J, Backer L, Dahiye AM, Misore A, DeCock K, Rubin C (2005) Aflatoxin contamination of commercial maize products during an outbreak of acute aflatoxicosis in eastern and Central Kenya. Environ Health Perspect 113:1763–1767

    Article  CAS  Google Scholar 

  • Maina UM, Galadima IB, Gambo FM, Zakaria D (2018) A review on the use of entomopathogenic fungi in the management of insect pests of field crops. J Entomol Zool Stud 6(1):27–32

    Google Scholar 

  • Makoko BR (2008) Assessment of cowpea, Vigna unguiculata (L) Walp. cultivars against Alectra vogelii (Benth) (Witchweed) collected from Dodoma, Tanzania. Dissertation, Sokoine University of Agriculture, Morogoro, Tanzania

  • Marin S, Ramos AJ, Cano-Sancho G, Sanchis V (2013) Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem Toxicol 60:218–237

    Article  CAS  Google Scholar 

  • Mfeka N, Mulidzi RA, Lewu FB (2019) Growth and yield parameters of three cowpea (Vigna unguiculata L. Walp) lines as affected by planting date and zinc application rate. S Afr J Sci 115(1/2), Art. #4474, 8 pages. https://doi.org/10.17159/sajs.2019/4474

  • Milner RJ (1997) Prospects for biopesticides for aphid control. Entomophaga 42:227–239

    Article  Google Scholar 

  • Moral J, Garcia-Lopez MT, Camiletti BX, Jaime R, Michailides TJ, Bandyopadhyay R, Ortega-Beltran A (2020) Present status and perspective on the future use of aflatoxin biocontrol products. Agronomy 10:491. https://doi.org/10.3390/agronomy10040491

    Article  CAS  Google Scholar 

  • Mureithi DM, Mworia JK, Meyhoefer R, Murungi LK, Losenge T, Akutse KS, Ekesi S, Fiaboe KKM (2015) Survey for pest and natural enemies of Amaranth and African nightshades in Kenya and Tanzania. Tropentag, September 16–18, 2015, Berlin, Germany. https://www.researchgate.net/publication/283730494_Survey_for_Pest_and_Natural_Enemies_of_Amaranth_and_African_Nightshades_in_Kenya_and_Tanzania

  • Nordey T, Ochieng J, Ernest Z, Mlowe N, Mosha I, Fernandes P (2020) Is vegetable cultivation under low tunnels a profitable alternative to pesticide use? The case of cabbage cultivation in northern Tanzania. Crop Prot 134:105–169

    Article  Google Scholar 

  • Norlia M, Jinap S, Nor-Khaizura MAR, Radu S, Samsudin NIP, Azri FA (2019) Aspergillus section Flavi and aflatoxins: occurrence, detection, and identification in raw peanuts and peanut-based products along the supply chain. Front Microbiol 10:2602. https://doi.org/10.3389/fmicb.2019.02602

    Article  PubMed  PubMed Central  Google Scholar 

  • Nyambo B (2009) Integrated pest management plan (IPMP). The United Republic of Tanzania, agricultural sector development program (ASDP). AFSP, Dar es Salaam, Tanzania. https://www.kilimo.go.tz/uploads/IPMP_Plan.pdf

  • Oduor GI, Lohr B, Seif AA (1996) Seasonality of major cabbage pests and incidence of their natural enemies in Central Kenya, pp 37–42. In: Sivapragasam A, Kole WH, Hassan AK, Lim GS (eds) The Management of diamondback moth and other crucifer pests: Proceedings of the 3rd International Workshop. 29th October–1st November 1996, Kuala Lumpur, Malaysia

  • Pell JK, Eilenberg J, Hajek AE, Steinkraus DC (2001) Biology, ecology and pest management potential of entomophthorales. In: Magan N, Butt TM, Jackson C (eds) Fungi as biocontrol agents. CAB International, Wallingford, pp 71–153

    Google Scholar 

  • Roy HE, Brodie EL, Chandler D, Goettel MS, Pell JK, Wajnberg E, Vega F (2010) Deep space and hidden depths: understanding the evolution and ecology of fungal entomopathogens. Biol Control 55:1–6

    Article  Google Scholar 

  • Sandhu SS, Sharma AK, Beniwal V, Goel G, Batra P, Kumar A, Jaglan S, Sharma A, Malhotra S (2012) Myco-biocontrol of insect pests: factors involved, mechanism, and regulation. J Pathog Article ID 126819, 10 pages. https://doi.org/10.1155/2012/126819

  • Sandhu SS, Shukla H, Aharwal RP, Kumar S, Shukla S (2017) Efficacy of entomopathogenic fungi as green pesticides: current and future prospects. In: Panpatte D, Jhala Y, Vyas R, Shelat H (eds) Microorganisms for green revolution. Microorganisms for sustainability, vol 6. Springer, Singapore

    Google Scholar 

  • Sani I, Ismail SI, 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 11:619. https://doi.org/10.3390/insects11090619

    Article  PubMed Central  Google Scholar 

  • Scholte E-J, Ng'Habi K, Kihonda J, Takken W, Paaijmans K, Abdulla S, Killeen GF, Knols BG (2005) An entomopathogenic fungus for control of adult African malaria mosquitoes. Science 308:1641–1642

    Article  CAS  Google Scholar 

  • Sevim A, Demir I, Sönmlez E, Kocacevik S, Demirbag Z (2013) Evaluation of entomopathogenic fungi against the sycamore lace bug, Corythucha ciliata (say) (Hemiptera: Tingidae). Turk J Agric For 37:595–603

    Article  Google Scholar 

  • Sevim A, Sevim E, Demirbağ Z (2015) General biology of entomopathogenic fungi and their potential to control pest species in Turkey (Entomopatojenik fungusların genel biyolojileri ve Türkiye’de zararlı böceklerin mücadelesinde kullanılma potansiyelleri). Erzincan Üniversitesi Fen Bilimleri Enstitüsü Dergisi 8(1):115–147

    Article  Google Scholar 

  • Seye F, Bawin T, Boukraa S, Zimmer JY, Ndiaye M, Delvigne F, Francis F (2014) Effect of entomopathogenic Aspergillus strains against the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae). Appl Entomol Zool 49:453–458

    Article  Google Scholar 

  • Shi WB, Feng MG (2004) Lethal effect of Beauveria bassiana, Metarhizium anisopliae, and Paecilomyces fumosoroseus on the eggs of Tetranychus cinnabarinus (Acari: Tetranychidae) with a description of a mite egg bioassay system. Biol Control 30:165–173

    Article  Google Scholar 

  • Silva AX, Jander G, Samaniego H, Ramsey JS, Figueroa CC (2012) Insecticide resistance mechanisms in the green peach aphid, Myzus persicae (Hemiptera: Aphididae) I: a transcriptomic survey. PLoS One 7(6):e36366. https://doi.org/10.1371/journal.pone.0036366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Emden HF, Harrington R (2007) Aphids as crop pests. CABI, Cromwell Press, Trowbridge. 717pp. ISBN-13: 978 0 85199 819 0. www.cabi.org

    Book  Google Scholar 

  • Vega FE, Meyling NV, Luangsa-ard JJ, Blackwell M (2012) Fungal entomopathogens. Insect Pathol 2:171–220

    Article  Google Scholar 

  • Visconti A, Perrone G (2008) The EU MycoGlobe project: global integration of mycotoxin and toxigenic fungal research for enhanced food safety. In: Leslie JF, Bandyopadhyay R, Visconti A (eds) Mycotoxins: detection methods, management, public health and agricultural trade. CAB International, Cromwell Press, Trowbridge, pp 3–9

    Chapter  Google Scholar 

  • Yokomi R, Gottwald T (1988) Virulence of Verticillium lecanii isolates in aphids determined by detached-leaf bioassay. J Invert Pathol 51:250–258

    Article  Google Scholar 

Download references

Funding

This research was financially supported by GIZ (German Corporation for International Cooperation) through a BMZ grant (12.1003.8-204.11) and the long-term strategic donors to the World Vegetable Center: Taiwan, the Foreign, Commonwealth & Development Office (FCDO) from the UK government, United States Agency for International Development (USAID), Australian Centre for International Agricultural Research (ACIAR), Germany, Thailand, Philippines, Korea, and Japan. Beneficiary companies: Kwekerij Lankhaar B.V. and Multiflower Ltd.

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  1. Robert Abraham Mwashimaha

    Present address: Multiflower Ltd, P. O. Box 14387, Arusha, Tanzania

Authors and Affiliations

  1. The World Vegetable Center, Eastern and Southern Africa, P. O. Box 10, Duluti, Arusha, Tanzania

    Simon Boniface Boni, Robert Abraham Mwashimaha, Nickson Mlowe & Thibault Nordey

  2. The World Vegetable Center, 60 Yi Ming Liao, Shanhua, Tainan, 74151, Taiwan, Republic of China

    Paola Sotelo-Cardona

  3. CIRAD - UR HortSys, Montpellier University, Montpellier, France

    Thibault Nordey

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  1. Simon Boniface Boni
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Correspondence to Simon Boniface Boni.

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Boni, S.B., Mwashimaha, R.A., Mlowe, N. et al. Efficacy of indigenous entomopathogenic fungi against the black aphid, Aphis fabae Scopoli under controlled conditions in Tanzania. Int J Trop Insect Sci 41, 1643–1651 (2021). https://doi.org/10.1007/s42690-020-00365-8

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