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Journal of Pest Science

, Volume 89, Issue 4, pp 993–1001 | Cite as

Fungal endophytes as promising tools for the management of bean stem maggot Ophiomyia phaseoli on beans Phaseolus vulgaris

  • Beritah Mutune
  • Sunday Ekesi
  • Saliou Niassy
  • Viviene Matiru
  • Christine Bii
  • Nguya K. Maniania
Original Paper

Abstract

Common bean, Phaseolus vulgaris, is an important food and cash crop in Africa. Its production is seriously affected by the bean stem maggot (BSM), Ophiomyia spp., which attacks seedlings. We evaluated the ability of eleven fungal isolates to colonize bean plants and the effects of inoculation on BSM feeding and oviposition, pupation, and adult emergence. All fungal isolates were able to colonize different bean plant parts (root, stem, and leaves), except isolates of Metarhizium anisopliae and Beauveria bassiana isolate ICIPE 273. Colonization was generally higher on the roots than on the stem and leaves and varied significantly between the fungal isolates. BSM feeding and oviposition were significantly reduced in all the fungus-inoculated bean plants which in turn affected pupation and adult emergence as compared to the control. Metarhizium anisopliae ICIPE 20 outperformed the other isolates in interfering with BSM lifecycle. Although M. anisopliae ICIPE 78 recorded a high number of punctures similar to the control, a significant reduction in the number of pupae and adult emergence was observed, suggesting possible BSM growth inhibition. This study clearly demonstrates that fungal endophytes can be considered as promising tools for the management of BSM in East Africa.

Keywords

Entomopathogenic fungi Agromyzidae Colonization Feeding Oviposition Adult emergence 

Notes

Acknowledgments

This study was funded icipe’s Innovative Seed Research Grant “Bean Stem Maggot”. The authors are very grateful to Mrs Gloria Muthoni for technical assistance. We acknowledge the statistical analysis assistance from Dr. Daisy Salifu and taxonomical assistance from Dr. Robert Copeland of icipe and Dr. Fathiya Khamis for molecular analysis.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Abate T (1991) The bean fly Ophiomyia phaseoli (Tryon) (Diptera: Agromyzidae) and its parasitoids in Ethiopia. J Appl Entomol 111:278–285CrossRefGoogle Scholar
  2. Abate T, Ampofo JKO (1996) Insect pests of beans in Africa: their ecology and management. Ann Rev Entomol 41:45–73CrossRefGoogle Scholar
  3. Akello J (2012) Biodiversity of fungal endophytes associated with maize, sorghum and Napier grass and their influence of biopriming on resistance to leaf mining, stem boring and sap sucking insect pests. Ph.D., University of Bonn, BonnGoogle Scholar
  4. Akello J, 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 129:157–165CrossRefGoogle Scholar
  5. 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 6:293–301CrossRefGoogle Scholar
  6. Ampofo JKO, Massomo SMS (1998) Some cultural strategies for management of bean stem maggots (Diptera: Agromyzidae) on beans in Tanzania. Afr Crop Sci J 6:351–356CrossRefGoogle Scholar
  7. Behie S, Jones S, Bidochka M (2014) Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13:112–119CrossRefGoogle Scholar
  8. Bing L, Lewis L (1991) Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211CrossRefGoogle Scholar
  9. Blair M, Fregene S, Beebe S, Ceballos H (2007) Marker-assisted selection in common beans and cassava. In: Guimarães E, Ruane J, Scherf B, Sonnino A, Dargie J (eds) Marker-assisted selection: current status and future perspectives in crops, livestock, forestry and fish. FAO, Rome, pp 81–115Google Scholar
  10. Cherry AJ, Banito A, Djegui D, 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 Beauveria bassiana. Int J Pest Manag 50:67–73CrossRefGoogle Scholar
  11. Ekesi S, Maniania NK (2002) Metarhizium anisopliae: an effective biological control agent for the management of thrips in Horti- and Floricultural Crops in Africa. In: Upadhyay RK (ed) Advances in microbial control of insect pests. Kluwer Academic/Plenum Publishers, The Netherlands, pp 165–180CrossRefGoogle Scholar
  12. García JE, Posadas JB, Perticari A, Lecuona RE (2011) Metarhizium anisopliae (Metschnikoff) Sorokin promotes growth and has endophytic activity in tomato plants. Adv Biol Res 5:22–27Google Scholar
  13. Goettel MS, Inglis GD (1997) Fungi: Hyphomycetes. In: Lacey L (ed) Manual techniques in insect pathology. Academic press, San Diego, pp 213–214CrossRefGoogle Scholar
  14. Greathead DJ (1969) A study in East Africa of beanflies (Diptera: Agromyzidae) affecting Phaseolus vulgaris and of their natural enemies with the description of a new species of Melanagromyza Hend. Bull Entomol Res 59:541–556CrossRefGoogle Scholar
  15. Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogen and their effects on two insect pests when in planta. Biol Control 55:34–41CrossRefGoogle Scholar
  16. Istifadah N, McGee PA (2006) Endophytic Chaetomium globosum reduces development of tanspot in wheat caused by Pyrenophora triticirepentis. Aust Plant Pathol 35:411–418CrossRefGoogle Scholar
  17. Jandricic SE, Filotas M, Sanderson JP, Wraight SP (2014) Pathogenicity of conidia-based preparations of entomopathogenic fungi against the greenhouse pest aphids Myzus persicae, Aphis gossypii, and Aulacorthum solani (Hemiptera: Aphididae). J Invertebr Pathol 118:34–46CrossRefPubMedGoogle Scholar
  18. Karel AK (1985) A Bibliography of bean flies, Ophiomyia phaseoli (Tyron), O. centrosematis (de Meij) and Melanogromyza spencerella (Greathead) (Diptera: Agromyzidae). Michigan State University East LansingGoogle Scholar
  19. Karel AK, Autrique A (1989) Insects and other pests in Africa. In: Schwarts HF, Pasto-corales MA (eds) Bean production problems in the tropics. CIAT, Cali, pp 455–504Google Scholar
  20. Kaur HP, Singh B, Kaur A, Kaur S (2013) Antifeedent and toxic activity of endophytic Alternaria alternata against tobacco caterpillar Spodoptera litura. J Pest Sci 86:543–550CrossRefGoogle Scholar
  21. Lopez DC, Sword GA (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). Biol Control 89:53–60CrossRefGoogle Scholar
  22. Mcconn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Plant Biology Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci 94:5473–5477CrossRefPubMedPubMedCentralGoogle Scholar
  23. Migiro L, Maniania N, Chabi-Olaye A, Van den Berg 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. Environ Entomol 39:468–475CrossRefPubMedGoogle Scholar
  24. Muvea AM, Meyhofer R, Subramanian S, Poehling HM, Ekesi S, Maniania NK (2014) Colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci. PLoS ONE 9(9):e108242CrossRefPubMedPubMedCentralGoogle Scholar
  25. Muvea AM, Meyhofer R, Subramanian S, Poehling HM, Ekesi S, Maniania NK (2015) Behavioral responses of Thrips tabaci Lindeman to endophyte-inoculated onion plants. J Pest Sci 88:555–562CrossRefGoogle Scholar
  26. Navarro-Meléndez A, Heil M (2014) Symptomless endophytic fungi suppress endogenous levels of salicylic acid and interact with the jasmonate-dependent indirect defense traits of their host, Lima bean (Phaseolus lunatus). J Chem Ecol 40:816–825CrossRefPubMedGoogle Scholar
  27. Nuessly GS, Nagata RT, Skiles ES, Christenson JR, Elliott C (1995) Techniques for differentially staining Liriomyza trifolii (Diptera: Agromyzidae) eggs and stipples within Cos lettuce leaves. Fla Entomol 78:258–264CrossRefGoogle Scholar
  28. Ochilo W, Nyamasyo G (2011) Pest status of bean stem maggot (Ophiomyia spp.) and black bean aphid (Aphis fabae) in Taita district, Kenya. J Trop Subtrop Bot Agroecosyst 13:91–97Google Scholar
  29. Pachico DH (1993) The demand for bean technology. Cali, ColombiaGoogle Scholar
  30. Petrini O, Fisher PJ (1987) Fungal endophytes in Salicornia perennis. Trans Soc Br Mycol 87:647–651CrossRefGoogle Scholar
  31. Pyndji MM, Trutmann P (1992) Managing angular leaf spot on common beans in Africa by supplementing farmer mixtures with resistant varieties. Plant Dis 76:1144–1473CrossRefGoogle Scholar
  32. Quesada-Moraga E, Landa BB, Muñoz-Ledesma J, Jiménez-Díaz RM, Santiago Alvarez C (2006) Endophytic colonisation of opium poppy, Papaver somniferum, by an entomopathogenic Beauveria bassiana strain. Mycopathologia 161:323–329CrossRefPubMedGoogle Scholar
  33. Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99:101–107CrossRefPubMedGoogle Scholar
  34. Schultz B, Guske S, Dammann U, Boyle C (1998) Endophyte-host interactions II. Defining symbiosis of the endophyte-host interaction Symbiosis 25:213–227Google Scholar
  35. Singh SR (1990) Fighting Insect Damage to Legumes http://www.anancy.net/tpl/fulltext.tpl.php?file_id=1088&language=english&acs 15. Accessed 25 Jul 2009
  36. Songa JM, Ampofo JKO (1998) Ecology of bean stem maggot attacking dry bean (Phaseolus vulgaris L.) in semi-arid areas of eastern Kenya. Int J Pest Manag 45:35–40CrossRefGoogle Scholar
  37. Spencer KA (1973) Agromyzidae (Diptera) of economic importance. Junk, The HagueCrossRefGoogle Scholar
  38. R Development Core Team (2013) A Language and environment for statistical computing. http://www.r-project.org/. Accessed 20 Apr 2014
  39. Tefera T, Vidal S (2009) Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. Biol Control 54:663–669Google Scholar
  40. USAID (2010) Staple foods value chain analysis. In Country report Kenya. USAID, KenyaGoogle Scholar
  41. Vega FE, Posada F, Aime MC, Pava-Ripoll M, Infante F, Rehner SA (2008) Entomopathogenic fungal endophytes. Biol Control 46:72–82CrossRefGoogle Scholar
  42. 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: news insights of their ecology. Fungal Ecol 2:149–159CrossRefGoogle Scholar
  43. Wickramasinghe N, Fernando HE (1962) Investigations on insecticidal seed dressings, soil treatments and foliar sprays for the control of Melanagromyza phaseoli (Tryon) in Ceylon. Bull Entomol Res 53:223–240CrossRefGoogle Scholar
  44. Wortmann CS, Kirkby RA, Eledu CA, Allen DJ (1999) Atlas of common bean (Phaseolus vulgaris L.) production in Africa. CIAT, CaliGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Beritah Mutune
    • 1
    • 2
  • Sunday Ekesi
    • 1
  • Saliou Niassy
    • 1
  • Viviene Matiru
    • 2
  • Christine Bii
    • 2
  • Nguya K. Maniania
    • 1
  1. 1.International Centre of Insect Physiology and Ecology (icipe)NairobiKenya
  2. 2.Jomo Kenyatta University of Agriculture and TechnologyNairobiKenya

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