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Presence of a generalist entomopathogenic fungus influences the oviposition behaviour of an aphid-specific predator

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Abstract

The predator Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae) and the generalist entomopathogenic fungus Metarhizium brunneum Petch (Hypocreales: Clavicipitaceae) are effective biological control agents that can co-occur in pest management programmes. We exposed larvae to M. brunneum, on leaves and in soil, to explore possible outcomes of combining the two natural enemies. The number of emerging adults and their longevity were negatively affected by fungus in the soil. When exposed on leaves, adult emergence was unaffected but longevity was reduced. In choice experiments, females chose to lay eggs on fungus-free leaves: more control leaves had eggs and there were more eggs per leaf in the control. In no-choice experiments, the same frequency of females laid eggs in the treatment and control, but significantly more eggs were laid on the control leaves. Gravid A. aphidimyza can perceive M. brunneum and respond by choosing fungus-free oviposition sites, thus reducing contact between them.

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References

  • Ansari M, Shah F, Butt T (2008) Combined use of entomopathogenic nematodes and Metarhizium anisopliae as a new approach for black vine weevil, Otiorhynchus sulcatus, control. Entomol Exp Appl 129:340–347

    Article  Google Scholar 

  • Azevedo AGCd, Steinwender BM, Eilenberg J, Sigsgaard L (2017) Interactions among the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae), the fungal pathogen Metarhizium brunneum (Ascomycota: Hypocreales), and maize-infesting aphids in greenhouse mesocosms. Insects 8:44

    Article  PubMed Central  Google Scholar 

  • Choi MY, Roitberg BD, Shani A, Raworth DA, Lee GH (2004) Olfactory response by the aphidophagous gall midge, Aphidoletes aphidimyza to honeydew from green peach aphid, Myzus persicae. Entomol Exp Appl 111:37–45

    Article  Google Scholar 

  • Guo H, Meng L, Wang Y, Zheng L, Li B (2014) Oviposition behavior of the predatory midge Aphidoletes aphidimyza in response to aphid patch quality. J Insect Behav 27:816–825

    Article  Google Scholar 

  • Hodek I (1993) Habitat and food specificity in aphidophagous predators. Biocontrol Sci Technol 3:91–100

    Article  Google Scholar 

  • Jackson MA, Jaronski ST (2009) Production of microsclerotia of the fungal entomopathogen Metarhizium anisopliae and their potential for use as a biocontrol agent for soil-inhabiting insects. Mycol Res 113:842–850

    Article  PubMed  CAS  Google Scholar 

  • Jandricic S, Filotas M, Sanderson J, Wraight S (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 118:34–46

    Article  PubMed  CAS  Google Scholar 

  • Labbe R, Gillespie D, Cloutier C, Brodeur J (2009) Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly. Biocontrol Sci Technol 19:429–446

    Article  Google Scholar 

  • Madahi K, Sahragard A, Hossieni R (2013) Prey density dependent life table of Aphidoletes aphidimyza Rondani (Dip.: Cecidomyiidae) feeding on Aphis craccivora Koch (Hem.: Aphididae) under laboratory conditions. J Plant Prot Res 53:253–262

    Article  Google Scholar 

  • Madahi K, Sahragard A, Hosseini R (2015) Predation rate and numerical response of Aphidoletes aphidimyza feeding on different densities of Aphis craccivora. Biocontrol Sci Technol 25:72–83

    Article  Google Scholar 

  • Markkula M, Tittanen K (1985) Biology of the midge Aphidoletes and its potential for biological control. In: Hussey NW, Scopes N (eds) Biological pest control: the glasshouse experience. The Glasshouse Experience, Blandford, pp 78–81

    Google Scholar 

  • Markkula M, Tiitanen K, Hamalainen M, Forsberg A (1979) The aphid midge Aphidoletes aphidimyza (Diptera, Cecidomyiidae) and its use in biological control of aphids. Entomol Fenn 45:89–98

    Google Scholar 

  • Meadow R, Kelly W, Shelton A (1985) Evaluation of Aphidoletes aphidimyza [Dip.: Cecidomyiidae] for control of Myzus persicae [Hom.: Aphididae] in greenhouse and field experiments in the United States. Entomophaga 30:385–392

    Article  Google Scholar 

  • Meyling NV, Pell JK (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 31:162–171

    Article  Google Scholar 

  • Mohammed AA, Hatcher PE (2017) Combining entomopathogenic fungi and parasitoids to control the green peach aphid Myzus persicae. Biol Control 110:44–55

    Article  Google Scholar 

  • Ormond EL, Thomas AP, Pell JK, Freeman SN, Roy HE (2011) Avoidance of a generalist entomopathogenic fungus by the ladybird, Coccinella septempunctata. FEMS Microbiol Ecol 77:229–237

    Article  PubMed  CAS  Google Scholar 

  • Poprawski TJ, Legaspi JC, Parker PE (1998) Influence of entomopathogenic fungi on Serangium parcesetosum (Coleoptera: Coccinellidae), an important predator of whiteflies (Homoptera: Aleyrodidae). Environ Entomol 27:785–795

    Article  Google Scholar 

  • Poprawski T, Parker P, Tsai J (1999) Laboratory and field evaluation of hyphomycete insect pathogenic fungi for control of brown citrus aphid (Homoptera: Aphididae). Environ Entomol 28:315–321

    Article  Google Scholar 

  • Powell JR, Webster JM (2004) Interguild antagonism between biological controls: impact of entomopathogenic nematode application on an aphid predator, Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Biol Control 30:110–118

    Article  Google Scholar 

  • Rännbäck L-M, Cotes B, Anderson P, Rämert B, Meyling NV (2015) Mortality risk from entomopathogenic fungi affects oviposition behavior in the parasitoid wasp Trybliographa rapae. J Invertebr Pathol 124:78–86

    Article  PubMed  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/

  • Roy H, Steinkraus D, Eilenberg J, Hajek A, Pell J (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357

    Article  PubMed  CAS  Google Scholar 

  • Ruzicka Z, Havelka J (1998) Effects of oviposition-deterring pheromone and allomones on Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Eur J Entomol 95:211–216

    Google Scholar 

  • Sigsgaard L, Steinwender BM, Dimitrova D, Hansen EW, Eilenberg J (2012) Technical protocol for tests of direct and indirect side effects of new BCA formulations on non-target invertebrates. http://inbiosoil.uni-goettingen.de/fileadmin/INBIOSOIL/Deliverables/3.1%20Defined%20technical%20protocol%20for%20test%20of%20side%20effects%20....pdf. Accessed 10 Nov 2016

  • Spollen KM, Isman MB (1996) Acute and sublethal effects of a neem insecticide on the commercial biological control agents Phytoseiulus persimilis and Amblyseius cucumeris (Acari: Phytoseiidae) and Aphidoletes aphidimyza (Diptera: Cecidomyiidae). J Econ Entomol 89:1379–1386

    Article  CAS  Google Scholar 

  • Titi AE (1974) Auswirkung von der räuberischen gallmücke Aphidoletes aphidimyza (Rond.)(Itonididae: Diptera) auf blattlauspopulationen unter glas. Zeitschrift für Angewandte Entomologie 76:406–417

    Article  Google Scholar 

  • van Lenteren JC, Schettino M, Isidoro N, Romani R, Schelt J (2002) Morphology of putative female sex pheromone glands and mating behaviour in Aphidoletes aphidimyza. Entomol Exp Appl 102:199–209

    Article  Google Scholar 

  • van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen H, Kuske S, Loomans A, Menzler-Hokkanen I, van Rijn P, Thomas M (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38

    Article  Google Scholar 

  • Watanabe H, Katayama N, Yano E, Sugiyama R, Nishikawa S, Endou T, Watanabe K, Takabayashi J, Ozawa R (2014) Effects of aphid honeydew sugars on the longevity and fecundity of the aphidophagous gall midge Aphidoletes aphidimyza. BioControl 78:55–60

    CAS  Google Scholar 

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Acknowledgements

The study was part of the EU project INBIOSOIL (Grant agreement 282767), funded by means of the 7th Framework Programme of the European Union. The authors would like to thank Erik W. Hansen and Desislava Dimitrova, EWH BioProduction for the cohorts; the laboratory technician Kristian Hanse; Judith K. Pell for the support with the proofreading. We also thank two anonymous reviewers for comments that helped us improve a previous version of this manuscript. This study was supported by the EU FP7 INBIOSOIL project and Science without Borders—Brazil (1260-13-8).

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Authors and Affiliations

  1. Department of Plant and Environmental Science, University of Copenhagen, 1871, Frederiksberg C, Denmark

    A. G. C. de Azevedo & L. Sigsgaard

  2. Department of Mathematical Sciences, University of Copenhagen, Copenhagen, Denmark

    R. M. Stuart

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  1. A. G. C. de Azevedo
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  2. R. M. Stuart
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  3. L. Sigsgaard
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Correspondence to L. Sigsgaard.

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Handling Editor: Marta Montserrat.

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de Azevedo, A.G.C., Stuart, R.M. & Sigsgaard, L. Presence of a generalist entomopathogenic fungus influences the oviposition behaviour of an aphid-specific predator. BioControl 63, 655–664 (2018). https://doi.org/10.1007/s10526-018-9889-1

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  • DOI: https://doi.org/10.1007/s10526-018-9889-1

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