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Pathogenicity of Beauveria bassiana isolated from Moroccan Argan forests soil against larvae of Ceratitis capitata (Diptera: Tephritidae) in laboratory conditions

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Abstract

The Mediterranean fruit fly, Ceratitis capitata Wiedemann (Diptera: Tephritidae), is the major tephritid pest in Morocco. This pest survives in Moroccan forests Argania spinosa and continually invades the nearest agricultural areas. Entomopathogenic fungi are an interesting tool for fruit fly control and hold a useful alternative to conventional insecticides. However, primary selection of effective pathogens should be taken in laboratory condition prior to applying them in the field. Here, we used third late instar larvae of C. capitata to investigate the effectiveness of 15 local Beauveria bassiana isolates. Results showed that all isolates were able to infect the larval stage, producing a large mortality rate in puparia ranging from 65 to 95 % and caused significant reduction in adult emergence. The fungal treatments revealed that the mycosis occurred also in adults escaping infection as pupariating larvae. The percentage of mycosed puparia was highest in strain TAM6.2 (95 %) followed by ERS4.16 (90 %), therefore they were the most virulent. Median lethal concentration (LC50) was studied for five isolates at four concentrations ranging from 105 to 108 conidia ml−1. The results showed that the slopes of regression lines for B. bassiana ERS4.16 (slope = 0.386) and TAM6.2 (slope = 0.41) were the most important and had the lowest LC50 values (2.85 × 103 and 3.16 × 103 conidia ml−1 respectively). This investigation suggests that the soil of Argan forests contains pathogenic B. bassiana isolates and highlights for the first time their potential as biological control toward C. capitata larval stage in Morocco.

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References

  • Bidochka MJ, Menzies FV, Kamp AM (2002) Genetic group of the insect-pathogenic fungus Beauveria bassiana are associated with habitat and thermal growth preference. Arch Microbiol 178:531–537

    Article  CAS  Google Scholar 

  • Bukhari T, Takken W, Koenraadt JMC (2011) Development of Metarhizium anisopliae and Beauveria bassiana formulations for control of malaria mosquito larvae. Parasit Vectors 4:1–14

    Article  Google Scholar 

  • Butt TM, Jackson CW, Magan N (2001) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford

    Book  Google Scholar 

  • Castillo MA, Moya P, Hernandez E, Fera EPY (2000) Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biol Control 19:274–282

    Article  Google Scholar 

  • Coombes CA, Hill MP, Moore SD, Dames JF, Fullard T (2013) Persistence and virulence of promising entomopathogenic fungal isolates for use in citrus orchards in South Africa. Biocontrol Sci Techn 23:1053–1066

    Article  Google Scholar 

  • Cossentine J, Thistlewood H, Goettel M, Jaronski S (2010) Susceptibility of preimaginal western cherry fruit fly, Rhagoletis indifferens (Diptera: Tephritidae) to Beauveria bassiana (Balsamo) Vuillemin Clavicipitaceae (Hypocreales). J Invertebr Pathol 104:105–109

    Article  CAS  Google Scholar 

  • Daniel C, Wyss E (2009) Susceptibility of different life stages of the European cherry fruit fly, Rhagoletis cerasis, to entomopathogneic fungi. J Appl Entomol 133:473–483

    Article  Google Scholar 

  • Dimbi S, Maniania NK, Lux SA, Ekesi S, Mueke JM (2003) Pathogenicity of Metarhizium anisopliae (Metsch.) Sorokin and Beauveria bassiana (Balsamo) Vuillemin, to three adult fruit fly species: Ceratitis capitata (Weidemann), C. rosa var. fasciventris Karsch and C. cosyra (Walker) (Diptera: Tephritidae). Mycopathologia 156:375–382

    Article  Google Scholar 

  • Dowd PF, Vega FE (2003) Autodissemination of Beauveria bassiana by sap beetles (Coleoptera: Nitidulidae) to overwintering sites. Biocontrol Sci Technol 13:65–75

    Article  Google Scholar 

  • Driouchi A, Buycks EJ (1990) “Rapport d’une réunion des agro-économistes nationaux sur l’évolution des pertes économiques causes par la cératite”, RAF/5/013- enquête sur l’étendue de l’infestation par la cératite en Afrique du nord. Meknès (Maroc)

  • Edwards JW, Lee SG, Heath LM, Pisaniello DL (2007) Worker exposure and a risk assessment of Malathion and Fenthion used in the control of Mediterranean fruit fly in South Australia. Environ Res 103:38–45

    Article  CAS  Google Scholar 

  • Ekesi S, Maniania NK, Lux SA (2002) Mortality in three African tephritid fruit fly puparia and adults caused by the entomopathogenic fungi, Metarhizium anisopliae and Beauveria bassiana. Biocontrol Sci Technol 12:7–17

    Article  Google Scholar 

  • Ekesi S, Maniania NK, Lux SA (2003) Effect of soil temperature and moisture on survival and infectivity of Metarhizium anisopliae to four tephritid fruit fly puparia. J Invertebr Pathol 83:157–167

    Article  CAS  Google Scholar 

  • Ekesi S, Maniania NK, Mohamed SA, Lux SA (2005) Effect of soil application of different formulations of Metarhizium anisopliae on African tephritid fruit flies and their associated endoparasitoids. Biol Control 35:83–91

    Article  Google Scholar 

  • Ekesi S, Dimbi S, Maniania NK (2007) The role of entomopathogenic fungi in the integrated management of tephritid 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, Kerala, pp 239–274

    Google Scholar 

  • Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Garrido-Jurado I, Santiago-Álvarez C, Quesada-Moraga E (2009) Efecto de la humedad y temperatura del suelo sobre la virulencia de hongos entomopatógenos frente a puparios de Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). VI Congreso Nacional de Entomología Aplicada, Palma de Mallorca, p 54

    Google Scholar 

  • Garrido-Jurado I, Torrent J, Barrón V, Corpas A, Quesada-Moraga E (2011) Soil properties affect the availability, movement, and virulence of entomopathogenic fungi conidia against puparia of Ceratitis capitata (Diptera: Tephritidae). Biol Control 58:277–285

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gutiérrez RL, De-La-Luz AT, Ochoa JM, Dominguez OR, Pescador AR et al (2000) Virulence of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) on Anastrepha ludens (Diptera: Tephritidae): Laboratory and field trials. J Econ Entomol 93:1080–1084

    Article  Google Scholar 

  • Imoulan A, Alaoui A, El Meziane A (2011) Natural occurrence of soil-borne entomopathogenic fungi in the Moroccan Endemic forest of Argania spinosa and their pathogenicity to Ceratitis capitata. World J Microbiol Biotechnol 27:2619–2628

    Article  Google Scholar 

  • Jackson TA, Alves SB, Pereira RM (2000) Success in biological control of soil-dwelling insects by pathogens and nematodes. In: Gurr G, Wratten S (eds) Biological control: measures of success. Kluwer Academic Public Publishers, Boston, pp 271–296

    Chapter  Google Scholar 

  • Konstantopoulos MA, Mazomenos BE (2005) Evaluation of Beauveria bassiana and B. brongniartii and four wild-type fungal species against adults of Bactrocera oleae and Ceratitis capitata. Biocontrol 50:293–305

    Article  Google Scholar 

  • Lacey LA, Shapiro-Ilan D (2003) The potential role for microbial control of orchard insect pests in sustainable agriculture. Food Agr Environ 1:326–331

    Google Scholar 

  • Lezama-Gutierrez R, la Trujillo-De LA, Molina-Ocha J, Rebolledo-Dominguez O et al (2000) Virulence of Metarhizium anisopliae on Anastrepha ludens: Laboratory and field trials. J Econ Entomol 93:1080–1084

    Article  CAS  Google Scholar 

  • Lux SA, Ekesi S, Dimbi S, Mohamed S, Billah M (2003) Mango infesting fruit Flies in Africa-Perspectives and limitations of biological approaches to their management. In: Neuenschwander P, Borgemeister C, Langewald J (eds) Biological control in integrated pest management systems in Africa. CABI, Wallingford, pp 277–293

    Google Scholar 

  • Magaña C, Hernandez-Crespo P, Brun-Barale A, Couso-Ferrer F et al (2008) Mechanisms of resistance to malathion in the Medfly Ceratitis capitata. Insect Biochem Mol Biol 38:756–762

    Article  Google Scholar 

  • Meyling NV, Eilenberg J (2006) Occurrence and distribution of soil borne entomopathogenic fungi within a single organic agroecosystem. Agric Ecosyst Environ 113:336–341

    Article  Google Scholar 

  • Mochi DA, Monteiro AC, De Bortoli SA, Doria HOS, Barbosa JC (2006) Pathogenicity of Metarhizium anisopliae for Ceratitis capitata (Wied.) (Diptera: Tephritidae) in soil with different pesticides. Neotrop Ent 35:382–389

    Article  CAS  Google Scholar 

  • Ortu S, Cocco A, Dau R (2009) Evaluation of the entomopathogenic fungus Beauveria bassiana strain ATCC 74040 for the management of Ceratitis capitata. Bull Insectology 62:245–252

    Google Scholar 

  • Quesada-Moraga E, Ruíz-García A, Santiago-Álvarez C (2006) Laboratory evaluation of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae against puparia and adults of Ceratitis capitata (Diptera: Tephritidae). J Econ Entomol 99:1955–1966

    Article  CAS  Google Scholar 

  • Rath AC, Koen TB, Anderson GC, Worledge D (1995) Long term efficacy of the entomogenous fungus, Metarhizium anisopliae against the subterranean scarab, Adoryphoru s couloni. Aust J Agric Res 46:429–440

    Article  Google Scholar 

  • Sevim A, Demir I, Höfte M, Humber RA, Demirbag Z (2010) Demirbag Isolation and characterization of entomopathogenic fungi from hazelnut-growing region of Turkey. Biocontrol 55:279–297

    Article  Google Scholar 

  • Sookar P, Bhagwant S, Ouna EA (2008) Isolation of entomopathogenic fungi from the soil and their pathogenicity to two fruit fly species (Diptera: Tephritidae). J Appl Entomol 132:778–788

    Article  Google Scholar 

  • Steel R, Torrie J (1980) Principles and procedures of statistics, a biometrical approach, 2nd edn. McGraw-Hill, New York, p 33

    Google Scholar 

  • Toledo J, Campos SE, Flores S, Liedo P, Barrera J, Villasenor A, Montoya P (2007) Horizontal transmission of Beauveria bassiana in Anastrepha ludens (Diptera: Tephritidae) under laboratory and field cage conditions. J Econ Entomol 100:291–297

    Article  Google Scholar 

  • Vontas J, Hernández-Crespob P, Margaritopoulosc JT, Ortego F et al (2011) Insecticide resistance in Tephritid flies. Pestic Biochem Physiol 100:199–205

    Article  CAS  Google Scholar 

  • White IM, Elson-Harris M (1992) Fruit flies of economic significance: their identification and bionomics. Int Inst Entomology, London, p 601

    Google Scholar 

  • Yee WL, Lacey LA (2005) Mortality of different life stages of Rhagoletis indifferens (Diptera: Tephritidae) exposed to the entomopathogenic fungus Metarhizium anisopliae. J Entomol Sci 40:167–177

    Google Scholar 

  • Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Tech 17:553–596

    Article  Google Scholar 

Download references

Acknowledgments

This work was financially supported by PROTARS II grant (P51/02) from the Moroccan Ministry of Higher Education and Scientific Research. A. Imoulan wishes to acknowledge CNRST for Doctorate research fellowship (b3/018).

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Correspondence to Abdessamad Imoulan.

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Imoulan, A., Elmeziane, A. Pathogenicity of Beauveria bassiana isolated from Moroccan Argan forests soil against larvae of Ceratitis capitata (Diptera: Tephritidae) in laboratory conditions. World J Microbiol Biotechnol 30, 959–965 (2014). https://doi.org/10.1007/s11274-013-1514-y

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