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Pathogenicity of three entomopathogenic fungi on pupae and adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae)

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Abstract

The pathogenicity of local isolates of the entomopathogenic fungi (EPF) Beauveria bassiana (Balsamo) Vuillemin, Isaria fumosorosea (Wize) (formerly Paecilomyces fumosoroseus (Wise) Brown & Smith) and Metarhizium anisopliae (Metschnikoff) Sorokin (Ascomycota: Hypocreales) were evaluated under laboratory conditions against pupae and adults of Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) via different routes of exposure. Average mortality of pupae after immersing them into spore suspensions was in general low and ranged from 18.7 to 23.9 % depending on fungal species and dose applied. However, adults obtained from treated pupae appeared to have higher mortality rates compared to control with all fungi and doses tested. Adults’ average mortalities ranged from 41.9 to 88.0 % after exposing them to EPF either by feeding on a mixture of conidial suspension and artificial food or by bodily contact with conidia, depending on fungal species, dose and method of exposure. The proportion of cadavers, pupae or adults, that produced visible signs of mycosis ranged from 40.4 to 73.3 % with the exception of those that were exposed to M. anisopliae. In that case, none of the insects that died after exposure to conidia of M. anisopliae developed visible mycelium on their surface. Moreover, confining treated with untreated adults indicated horizontal conidial transmission in some cases. Our results indicate that EPF might be a promising biological control agent for the Mediterranean fruit fly and could be utilised with different modes of application: soil application against pupae and cover or bait sprays against adults.

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References

  • Ali S, Huang Z, Ren S (2010) Production of cuticle degrading enzymes by Isaria fumosorosea and their evaluation as a biological agent against diamondback moth. J Pest Sci 83:361–370

    Article  Google Scholar 

  • Altre JA, Vandenberg JD (2001) Factors influencing the infectivity of isolates of Paecilomyces fumosoroseus against diamondback moth, Plutella xylostella. J Invertebr Pathol 78:31–36

    Article  PubMed  CAS  Google Scholar 

  • Athanassiou CG, Steenberg T, Kavallieratos NG (2007) Insecticidal effect of diatomaceous earth applied alone or in combination with Beauveria bassiana and beta cyfluthrin against Sitophilus granarius on stored wheat. Integr Prot Stored Prod IOBC/WPRS Bull 30:25–36

    Google Scholar 

  • Batta YA (2007) Biocontrol of almond bark beetle (Scolytus amygdali Geurin-Meneville, Coleoptera: Scolytidae) using Beauveria bassiana (Bals.) Vuill. (Deuteromycotina: Hyphomycetes). J Appl Microbiol 103:1406–1414

    Article  PubMed  CAS  Google Scholar 

  • Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512–530

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Dembilio O, Quesada-Moraga E, Santiago-Alvarez C, Jacas JA (2010) Potential of an indigenous strain of the entomopathogenic fungus Beauveria bassiana as a biological control agent against the Red Palm Weevil, Rhynchophorus ferrugineus. J Invertebr Pathol 104:214–221

    Article  PubMed  Google Scholar 

  • Demirci F, Mustu M, Kaydan MB, Ülgentürk S (2011) Laboratory evaluation of the effectiveness of the entomopathogen; Isaria farinosa, on citrus mealybug, Planococcus citri. J Pest Sci 84:337–342

    Article  Google Scholar 

  • Dimbi S, Maniania NK, Lux SA, Ekesi S, Mueke JK (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  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    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  PubMed  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 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 

  • Faria M, Wraight SP (2001) Biological control of Bemisia tabaci with fungi. Crop Prot 20:767–778

    Article  Google Scholar 

  • Fernandez S, Groden E, Vandenberg JD, Furlong MJ (2001) The effect of mode of exposure to Beauveria bassiana on conidia acquisition and host mortality of Colorado potato beetle, Leptinotarsa decemlineata. J Invertebr Pathol 77:217–226

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Gallardo FD, Boethel DS, Fuxa FR, Richter A (1990) Susceptibility of Heliothis zea (Boddie) larvae to Nomuraea rileyi (Farlow) Samson: effects of alpha-tomatine a the third trophic level. J Chem Ecol 16:1751–1759

    Article  CAS  Google Scholar 

  • Goble TA, Dames JF, Hill MP, Moore SD (2011) Investigation of native isolates of entomopathogenic fungi for the biological control of three citrus pests. Biocontrol Sci Technol 21:1193–1211

    Article  Google Scholar 

  • Goettel MS, Eilenberg J, Glare TR (2005) Entomopathogenic fungi and their role in regulation of insect populations. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive molecular insect science, vol 6: control. Elsevier/Pergamon, Oxford, pp 361–406

    Chapter  Google Scholar 

  • Hendrichs J, Ortiz G, Liedo P, Schwarz A (1983) Six years of successful medfly program in Mexico and Guatemala. In: Cavalloro R (ed.) Proceedings, symposium: fruit flies of economic importance. CEO/IOBC international symposium, 16–19 November 1982, Athens, Greece. A.A. Balkema, Rotterdam, pp 353–365

  • Inglis GD, Johnson DL, Goettel MS (1996) Effects of temperature and thermoregulation on mycosis by Beauveria bassiana in grasshoppers. Biol Control 50:324–328

    Google Scholar 

  • Katsoyannos BI, Kouloussis NA, Carey JR (1998) Seasonal and annual occurrence of Mediterranean fruit flies (Diptera: Tephritidae) on Chios island, Greece: differences between two neighboring citrus orchards. Ann Entomol Soc Am 91:43–51

    Google Scholar 

  • Konstantopoulou MA, Mazomenos BE (2005) Evaluation of Beauveria bassiana and B. brongniartii strains 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 DI (2008) Microbial control of insect pests in temperate orchard systems: potential for incorporation into IPM. Annu Rev Entomol 3:121–144

    Article  Google Scholar 

  • Malacrida AR, Gomulski LM, Bonizzoni M, Bertin S, Gasperi G, Guglielmino CR (2007) Globalization and fruit fly invasion and expansion: the medfly paradigm. Genetica 131:1–9

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Ferrer MT, Campos JM, Fibla JM (2012) Field efficacy of Ceratitis capitata (Diptera: Tephritidae) mass trapping technique on clementine groves in Spain. J Appl Entomol 136(3):181–190

    Article  Google Scholar 

  • Meadow R, Vandenbergs JD, Shelton AM (2000) Exchange of inoculum of Beauveria bassiana (Bals.) Vuill. (Hyphomycetes) between adult flies of the cabbage maggot Delia radicum L. (Diptera: Anthomyiidae). Biocontrol Sci Technol 10:479–485

    Article  Google Scholar 

  • Ovruski SM, Schliserman P, Aluja M (2004) Indigenous parasitoids (Hymenoptera) attacking Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in native and exotic host plants in Northwestern Argentina. Biol Control 29:43–57

    Article  Google Scholar 

  • Papachristos DP, Papadopoulos NT (2009) Are citrus species favorable hosts for the Mediterranean fruit fly? A demographic perspective. Entomol Exp Appl 132:1–12

    Article  Google Scholar 

  • Papadopoulos NT, Katsoyannos BI, Carey JR, Kouloussis NA (2001) Seasonal and annual occurrence of the Mediterranean fruit fly (Diptera: Tephritidae) in northern Greece. Ann Entomol Soc Am 94:41–50

    Article  Google Scholar 

  • Perry AS, Yamamoto I, Ishaaya I, Perry RY (1998) Insecticides in agriculture and environment: retrospects and prospects. Springer, Berlin

    Book  Google Scholar 

  • Poprawski TJ, Jones WJ (2001) Host plant effects on activity of the mitosporic fungi Beauveria bassiana and Paecilomyces fumosoroseus against two populations of Bemisia whiteflies (Homoptera: Aleyrodidae). Mycopathologia 151:11–20

    Article  PubMed  CAS  Google Scholar 

  • Poprawski TJ, Robert PH, Majchrowicz I, Boivin G (1985) Susceptibility of Delia antique (Diptera: Antomyiidae) to eleven isolates of entomopathogenic Hyphomycetes. Environ Entomol 14:557–561

    Google Scholar 

  • Poprawski TJ, Greenberg SM, Comperlik MA (2000) Effect of host plant on Beauveria bassiana- and Paecilomyces fumosoroseus-induced mortality of Traileurodes vaporariorum (Homoptera: Aleyrodidiae). Environ Entomol 29:1048–1053

    Article  Google Scholar 

  • Prokopy RJ, Hendrichs J (1979) Mating behavior of Ceratitis capitata on a field-cage host tree. Ann Entomol Soc Am 72:642–648

    Google Scholar 

  • Quesada-Moraga E, Ruiz-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  PubMed  CAS  Google Scholar 

  • Ramoska WA, Todd T (1985) Variation in efficacy and viability of Beauveria bassiana in the chinch bug (Hemiptera: Lygaeidae) as a result of feeding activity on selected host plants. Environ Entomol 14:146–148

    Google Scholar 

  • Rehner SA, Minnis AM, Sung GH, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073

    Article  PubMed  Google Scholar 

  • Roessler Y (1989) Control; insecticides; insecticidal bait and cover sprays. In: Robinson AS, Hooper G (eds) World crop pests 3(B). Fruit flies; their biology, natural enemies and control. Elsevier, Amsterdam, pp 329–336

    Google Scholar 

  • Shah PA, Pell JK (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413–423

    PubMed  CAS  Google Scholar 

  • Shimazu M (1994) Potential of the cerambycid-parasitic type of Beauveria brongniartii (Deuteromycotina: Hyphomycetes) for microbial control of Monochamus alternates Hope (Coleoptera: Cerambycidae). Appl Entomol Zool 29:127–130

    Google Scholar 

  • Shimazu M, Takatsuka J (2006) Factors affecting poor mycelial growth on cadavers of Monochamus alternatus infected with an entomopathogenic fungus, Beauveria bassiana. Bull For For Prod Res Inst 5:235–242

    CAS  Google Scholar 

  • Shimazu M, Zhang B, Liu Y (2002) Fungal pathogens of Anoplophora glabripennis (Coleoptera: Cerambycidae) and their virulences. Bull FFPRI 1:123–130

    Google Scholar 

  • Singha D, Singha B, Dutta BK (2011) Potential of Metarhizium anisopliae and Beauveria bassiana in the control of tea termite Microtermes obesi Holmgren in vitro and under field conditions. J Pest Sci 84:69–75

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman and Company, New York

    Google Scholar 

  • SPSS (2004) SPSS 14 for Windows User’s Guide. Copyright 2004 by SPSS Inc., SPSS, Chicago

  • Stark JD, Vargas R (2009) An evaluation of alternative insecticides to diazinon for control of Tephritid fruit flies (Diptera: Tephritidae) in soil. J Econ Entomol 102:139–143

    Article  PubMed  Google Scholar 

  • Toledo J, Campos SE, Flores S, Liedo P, Barrera JF, 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  PubMed  Google Scholar 

  • Ugine TA, Wraight SP, Sanderson JP (2007) A tritrophic effect of host plant on susceptibility of western flower thrips to the entomopathogenic fungus Beauveria bassiana. J Invertebr Pathol 96:162–172

    Article  PubMed  Google Scholar 

  • Urbaneja A, Chueca P, Montón H, Pascual-Ruiz S, Dembilio O, Vanaclocha P, Abad-Moyano R, Pina T, Castañera P (2009) Chemical alternatives to Malathion for controlling Ceratitis capitata (Diptera: Tephritidae), and their side effects on natural enemies in Spanish citrus orchards. J Econ Entomol 102:144–151

    Article  PubMed  Google Scholar 

  • Vontas J, Hernández-Crespo P, Margaritopoulos JT, Ortego F, Feng H-T, Mathiopoulos KD, Hsu J-C (2011) Insecticide resistance in Tephritid flies. Pestic Biochem Physiol 100:199–205

    Article  CAS  Google Scholar 

  • White IM, Elson-Harris MM (1992) Fruit flies of economic significance their identification and bionomics. C.A.B. International, Wallingford

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Wraight SP, Ramos ME, Avery PB, Jaronski ST, Vandenberg JD (2010) Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops. J Invertebr Pathol 103:186–199

    Article  PubMed  CAS  Google Scholar 

  • Zenil M, Liedo P, Williams T, Valle J, Cancino J, Montoyab P (2004) Reproductive biology of Fopius arisanus (Hymenoptera: Braconidae) on Ceratitis capitata and Anastrepha spp. (Diptera: Tephritidae). Biol Control 29:169–178

    Article  Google Scholar 

  • Zimmermann G (1986) The Galleria bait method for detection of entomopathogenic fungi in soil. J Appl Entomol 102:213–215

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zimmermann G (2008) The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): biology, ecology and use in biological control. Biocontrol Sci Technol 18:865–901

    Article  Google Scholar 

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Acknowledgments

We thank Professor C. Tkaczuk (University of Podlasie) for morphological identification of the EPF used in the study. We also thank two anonymous reviewers and subject editor for their valuable and constructive suggestions. This study was funded by the Greek State Scholarship Foundation (I.K.Y.).

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Correspondence to Dimitrios P. Papachristos.

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Communicated by S.T. Jaronski

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Beris, E.I., Papachristos, D.P., Fytrou, A. et al. Pathogenicity of three entomopathogenic fungi on pupae and adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). J Pest Sci 86, 275–284 (2013). https://doi.org/10.1007/s10340-012-0468-4

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