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Prospects of fungal endophytes in the control of Liriomyza leafminer flies in common bean Phaseolus vulgaris under field conditions

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Abstract

Field trials were carried out for two seasons in two sites (Sagana and Naromoru, Central province of Kenya) to evaluate the prospects of endophyte isolates of Beauveria bassiana (Balsamo) Vuillemin G1LU3 and Hypocrea lixii Patouillard F3ST1 for the control of Liriomyza leafminer in common bean Phaseolus vulgaris L. crops through seeds inoculation. Autodissemination device (AD) treated with conidia of Metarhizium anisopliae (Metschnikoff) Sorokin ICIPE 20 was also added as a treatment. Leafminer infestation was not significantly different during the first season but was higher in the controls than in endophtyte treatments at both sites during the second season. Three key Liriomyza species [(L. huidobrensis Blanchard, L. sativae Blanchard and L. trifolii (Burgess)] and six parasitoid species [(Opius dissitus Muesebeck, Phaedrotoma scabriventris Nixon, Diglyphus isaea Walker, Neochrysocharis formosa Westwood, Hemiptarsenus varicornis Girault and Halticoptera arduine (Walker)] were identified during the trials. Leafminer infestation, number of pupae, leafminer flies and parasitoids emergence and yield were the parameters evaluated. Both isolates successfully colonized different parts of P. vulgaris plants, although the colonization was higher with H. lixii F3ST1 than B. bassiana G1LU3 at both sites. The mean number of pupae from the infested leaves varied between 141–252 and 331–416 in endophyte and control treatments, respectively, during the first season and from 110–223 to 366–523, respectively, in endophyte and control treatments during the second season. There were no significant differences among the treatments in the number of parasitoids that emerged from pupae. Higher yield of P. vulgaris seeds was obtained in endophyte than in control treatments. The inclusion of AD treatment did not have significant effect on all the parameters evaluated, except yield. Results of the present study suggest that both fungal isolates hold potential for pest management and could be considered for the control of leafminer flies. However, there is the need to confirm these results on large-scale trials.

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References

  • Akello JT (2012) Biodiversity of fungal endophytes associated with maize, sorghum and Napier grass and their influence of biopriming on the resistance of leaf mining, stem boring and sap sucking insect pests. PhD thesis, University of Bonn, Ecology and Development Series No. 86, 2012, ZEF Bonn, Germania, p. 137

  • Akello JT, Dubois T, Coyne D, Kyamanywa S (2008) Effect of endophytic Beauveria bassiana on populations of the banana weevil, Cosmopolites sordidus, and their damage in tissue cultured banana plants. Entomol Exp Appl 129:157–165

    Article  Google Scholar 

  • Akutse KS, Maniania NK, Fiaboe KKM, van den Berg J, Ekesi S (2013) Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecol 6:293–301

    Article  Google Scholar 

  • Akutse KS, Fiaboe KKM, van den Berg J, Ekesi S, Maniania NK (2014) Effects of endophyte colonization of Vicia faba (Fabaceae) plants on the life–history of leafminer parasitoids Phaedrotoma scabriventris (Hymenoptera: Braconidae) and Diglyphus isaea (Hymenoptera: Eulophidae). PLoS ONE 9(10):e109965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bixby-Brosi AJ, Potter DA (2012) Endophyte-mediated tritrophic interactions between a grass-feeding caterpillar and two parasitoid species with different life histories. Arthropod Plant Interactions 6:27–34

    Article  Google Scholar 

  • Chabi-Olaye A, Mujica N, Löhr B, Kroschel J (2008) Role of agroecosystems in the abundance and diversity of Liriomyza leafmining flies and their natural enemies. In: Abstracts of the XXIII International Congress of Entomology 6–12 July 2008, Durban, South Africa. Abstract No. 1765

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

    Article  Google Scholar 

  • Clay K (1990) Fungal endophytes of grasses. Ann Rev Ecol Syst 21:255–297

    Article  Google Scholar 

  • Dingle J, McGee PA (2003) Some endophytic fungi reduce the density of pustules of Puccinia recondita f. sp. tritici in wheat. Mycol Res 107:310–316

    Article  PubMed  Google Scholar 

  • Duarte RT, Gonçalves KC, Espinosa DJL, Moreira LF, De Bortoli SA, Humber RA, Polanczyk RA (2016) Potential of entomopathogenic fungi as biological control agents of diamondback moth (Lepidoptera: Plutellidae) and compatibility with chemical insecticides. J Econ Entomol 109:594–601

    Article  CAS  PubMed  Google Scholar 

  • Ekesi S, Dimbi S, Maniania NK (2007) The role of entomopathogenic fungi in the integrated management of fruit flies (Diptera: Tephritidae) with emphasis on species occurring in Africa. In: Ekesi S, Maniania NK (eds) Use of entomopathogenic fungi in biological pest management. Research Signpost Publishers, Trivandrum, pp 239–274

    Google Scholar 

  • EPPO (European and Mediterranean Plant Protection Organization) (2006) Distribution maps of quarantine pests of Europe A2 list: Annex II/A2. https://www.eppo.int/QUARANTINE/listA2.htm. Accessed July 2016

  • EUROPHYT (European Union Notification System for Plant Health Interceptions) (2014) Interceptions of harmful organisms in commodities imported into the EU Member States and Switzerland. http://ec.europa.eu/geninfo/query/resultaction.jsp?QueryText=European+Union+Notification+System+for+Plant+Health+Interceptions%2C+2014&sbtSearch=Search&swlang=en. Accessed July 2016

  • FVO (Food and Veterinary Office) (2013) Final report of an audit carried out in Kenya from 12 to 22 November 2013 in order to evaluate the system of official controls for the export of plants and plant products to the European Union. European Commission Health and Consumers Directorate-General. DG (SANCO) 2013-6817—MR FINAL. http://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&ved=0CB0QFjAA&url=http%3A%2F%2Fec.europa.eu%2Ffood%2Ffvo%2Fact_getPDF.cfm%3FPDF_ID%3D10858&ei=_oO3VMnGNIKv7Aav_4H4Ag&usg=AFQjCNHODtE6itpls1ZwATHG4eaxhPNlsQ. Accessed December 2015

  • Gitonga ZM, Chabi-Olaye A, Mithofer D, Okello JJ, Ritho NC (2010) Control of invasive Liriomyza leafminer species and compliance with food safety standards by small scale snow pea farmers in Kenya. Crop Prot 29:1472–1477

    Article  Google Scholar 

  • Goettel MS, Inglis GD (1997) Fungi: Hyphomycetes. In: Lacey L (ed) Manual of techniques in insect pathology. Acadmic Press, San Diego, pp 213–248

    Chapter  Google Scholar 

  • Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363

    Article  PubMed  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Istifadah N, McGee PA (2006) Endophytic Chaetomium globosum reduces development of tan spot in wheat caused by Pyrenophora triticirepentis. Aust Plant Pathol 35:411–418

    Article  Google Scholar 

  • Kennedy GG (2003) Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Ann Rev Entomol 48:51–72

    Article  CAS  Google Scholar 

  • KEPHIS (Kenyan Plant Health Inspectorate Service) (2006) Kenya Plant Health Inspectorate Service. Annual Report and Financial Statements July 2005–June 2006, Nairobi-Kenya, p 14

  • KNBS (Kenya National Bureau of Statistics) (2014) Kenya facts and figures 2014. Government of Kenya http://www.knbs.or.ke/index.php?option=com_phocadownload&view=category&id=20:kenya-facts-figures&Itemid=595,%2030%20June%202014. Accessed July 2016

  • Maniania NK, Ekesi S, Odulaja A, Okech MA, Nadel DJ (2006) Prospects of a fungus-contamination device for the control of tsetse fly Glossina fuscipes fuscipes. Biocontrol Sci Technol 16:129–139

    Article  Google Scholar 

  • Migiro L, Maniania J, Olaye CA, van den Berg J (2010) Pathogenicity of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana (Hypocreales: Clavicipitaceae) to the adult pea leafminer Liriomyza huidobrensis (Diptera: Agromyzidae) and prospects of an autoinoculation device for infection in the field. Environ Entomol 39:468–475

    Article  CAS  PubMed  Google Scholar 

  • Murphy ST, La Salle J (1999) Balancing biological control strategies in the IPM of New World invasive Liriomyza leafminers in field vegetable crops. Biocontrol News Inf 20:91–104

    Google Scholar 

  • Mutune B, Ekesi S, Niassy S, Matiru V, Bii C, Maniania NK (2016) Fungal endophytes as promising tools for the management of bean stem maggot Ophiomyia phaseoli on beans Phaseolus vulgaris. J Pest Sci. doi:10.1007/s10340-015-0725-4

    Google Scholar 

  • O’Hara RB, Kotze DJ (2011) Do not log-transform count data. Methods Ecol Evol 1:118–122

    Article  Google Scholar 

  • Petrini O, Fisher PJ (1987) Fungal endophytes in Salicornia perennis. T Brit Mycol Soc 87:647–651

    Article  Google Scholar 

  • Price JF, Nagle CA (2002) Pesticide mode of action to aid ornamental growers in developing control programs to manage pest resistance. Proc Fla State Hortic Soc 115:130–133

    Google Scholar 

  • Rathouz DK, Gao L (2009) Generalised linear models with unspecified reference distribution. Biostatistics 10:205–218

    Article  PubMed  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/

  • Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Schultz B, Guske S, Dammann U, Boyle C (1998) Endophyte-host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227

    Google Scholar 

  • Sikora RA, Pocasangre L, Felde AZ, Niere B, Tam TV, Dababat AA (2008) Mutualistic endophytic fungi and in-planta suppressiveness to plant parasitic nematodes. Biol Control 46:15–23

    Article  Google Scholar 

  • UNCED (United Nations Conference on Environment and Development) (1992) AGENDA 21: Rio de Janeiro, Brazil. https://sustainabledevelopment.un.org/content/documents/Agenda21.pdf. Accessed July 2016

  • Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzo’n A, Ownley BH, Pell JK, Rangell DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159

    Article  Google Scholar 

  • Zhang L (2014) Colonization pattern of crop plants by endophytic fungi. PhD Thesis, International PhD Program for Agricultural Sciences in Goettingen (IPAG) at the Faculty of Agricultural Sciences, Georg-August-University Göttingen, Germania, p 116

Download references

Acknowledgments

This study was conducted with the financial support from the Federal Ministry for Economic Cooperation and Development, Germany (BMZ), through the German Federal Enterprise for International Cooperation (GIZ) (Grant number: 09.7860.1-001.00; Contract number: 81121261). We are grateful to the Leafminer Project for providing research facilities under Dissertation Research Internship Programme (DRIP) of International Center of Insect Physiology and Ecology (ICIPE), Nairobi, Kenya. The authors are also grateful to Dr. D. Salifu for statistical analysis, F. Nyamu, G. Muthoni, S. Wafula, P. Githui, A. Macharia and R. Muchoki for their technical assistance.

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  1. Komivi Senyo Akutse

    Present address: Institute of Applied Ecology (IAE), Fujian Agriculture and Forestry University (FAFU), Jinshan, Fuzhou, 350002, People’s Republic of China

Authors and Affiliations

  1. International Centre of Insect Physiology and Ecology (ICIPE), P. O. Box 30772-00100, Nairobi, Kenya

    Jane Wairimu Gathage, Komi Kouma Mokpokpo Fiaboe, Komivi Senyo Akutse, Sunday Ekesi & Nguya Kalemba Maniania

  2. Jomo Kenyatta University of Agriculture and Technology (JKUAT), P.O. Box 62000-00200, Nairobi, Kenya

    Jane Wairimu Gathage & Zipporah Osiemo Lagat

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  1. Jane Wairimu Gathage
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Correspondence to Nguya Kalemba Maniania.

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Gathage, J.W., Lagat, Z.O., Fiaboe, K.K.M. et al. Prospects of fungal endophytes in the control of Liriomyza leafminer flies in common bean Phaseolus vulgaris under field conditions. BioControl 61, 741–753 (2016). https://doi.org/10.1007/s10526-016-9761-0

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