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Combining Mutualistic Yeast and Pathogenic Virus — A Novel Method for Codling Moth Control

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Abstract

The combination of a pathogenic virus and mutualistic yeasts isolated from larvae of codling moth Cydia pomonella is proposed as a novel insect control technique. Apples were treated with codling moth granulovirus (CpGV) and either one of three yeasts, Metschnikowia pulcherrima, Cryptococcus tephrensis, or Aureobasidium pullulans. The combination of yeasts with CpGV significantly increased mortality of neonate codling moth larvae, compared with CpGV alone. The three yeasts were equally efficient in enhancing the activity of CpGV. The addition of brown cane sugar to yeast further increased larval mortality and the protection of fruit against larvae. In comparison, without yeast, the addition of sugar to CpGV did not produce a significant effect. A field trial confirmed that fruit injury and larval survival were significantly reduced when apple trees were sprayed with CpGV, M. pulcherrima, and sugar. We have shown earlier that mutualistic yeasts are an essential part of codling moth larval diet. The finding that yeast also enhances larval ingestion of an insect-pathogenic virus is an opportunity for the development of a novel plant protection technique. We expect the combination of yeasts and insect pathogens to essentially contribute to future insect management.

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References

  • Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE, Hu Y, Basinger U, Mott BM, Buck N, Wheeler DE (2012) Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol 21:2282–2296

    Article  PubMed  Google Scholar 

  • Arthurs SP, Hilton R, Knight AL, Lacey LA (2007) Evaluation of the pear ester kairomone as a formulation additive for the granulovirus of codling moth (Lepidoptera: Tortricidae) in pome fruit. J Econ Entomol 100:702–709

    Article  PubMed  CAS  Google Scholar 

  • Ballard J, Ellis DJ, Payne CC (2000a) The role of formulation additives in increasing the potency of Cydia pomonella granulovirus for codling moth larvae, in laboratory and field experiments. Biocontrol Sci Technol 10:627–640

    Article  Google Scholar 

  • Ballard J, Ellis DJ, Payne CC (2000b) Uptake of granulovirus from the surface of apples and leaves by first instar larvae of the codling moth Cydia pomonella L. (Lepidoptera: Olethreutidae). Biocontrol Sci Technol 10:617–625

    Article  Google Scholar 

  • Becher PG, Guerin PM (2009) Oriented responses of grapevine moth larvae Lobesia botrana to volatiles from host plants and an artificial diet on a locomotion compensator. J Insect Physiol 55:384–393

    Article  PubMed  CAS  Google Scholar 

  • Bengtsson JM, Trona F, Montagne N, Anfora G, Ignell R, Witzgall P, Jacquin-Joly E (2012) Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptome analysis. PLoS One 7:e31620

    Article  PubMed  CAS  Google Scholar 

  • Berendsen RL, Roeland L, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  PubMed  CAS  Google Scholar 

  • Chandler D, Bailey AS, Tatchell GM, Davidson G, Greaves J, Grant WP (2011) The development, regulation and use of biopesticides for integrated pest management. Phil Trans R Soc B 366:1987–1998

    Article  PubMed  Google Scholar 

  • Charmillot PJ, Pasquier D (2003) Combination of mating disruption and granulosis virus to control resistant stains of codling moth, Cydia pomonella. IOBC-wprs Bull 26:27–29

    Google Scholar 

  • Cross JV, Solomon MG, Chandler D, Jarrett P, Richardson PN, Winstanley D, Bathon H, Huber J, Keller B, Langenbruch GA, Zimmerman G (1999) Biocontrol of pests of apples and pears in northern and central Europe: 1. Microbial agents and nematodes. Biocontrol Sci Technol 9:125–149

    Article  Google Scholar 

  • Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as arthropod semiochemicals. J Chem Ecol (this volume)

  • Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011–2027

    PubMed  CAS  Google Scholar 

  • Fierer N, Ferrenberg S, Flores GE, Gonzalez A, Kueneman J, Legg T, Lynch RC, McDonald D, Mihaljevic JR, O’Neill SP, Rhodes ME, Song SJ, Walters WA (2012) From animalcules to an ecosystem: application of ecological concepts to the human microbiome. Annu Rev Ecol Evol Syst 43:137–155

    Article  Google Scholar 

  • Fishilevich E, Domingos AI, Asahina K, Naef F, Vosshall LB, Louis M (2005) Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr Biol 15:2086–2096

    Article  PubMed  CAS  Google Scholar 

  • Fritsch E, Undorf-Spahn K, Kienzle J, Zebitz CPW, Huber J (2005) Apfelwickler-granulovirus: erste hinweise auf unterschiede in der empfindlichkeit lokaler apfelwickler-populationen. Nachrichtenbl Deut Pfanzenschutzd 57:29–34

    Google Scholar 

  • Gildemacher PR, Heijne B, Houbraken J, Vromans T, Hoekstra ES, Boekhout T (2004) Can phyllosphere yeasts explain the effect of scab fungicides on russeting of Elstar apples? Eur J Plant Pathol 110:929–937

    Article  CAS  Google Scholar 

  • Gilmer PM (1933) The entrance of codling moth larvae into fruit, with special reference to the ingestion of poison. J Kansas Entomol Soc 6:19–25

    CAS  Google Scholar 

  • Granado J, Thürig B, Keiffer E, Petrini L, Fliebach A, Tamm L, Weibel FP, Wyss GS (2008) Culturable fungi of stored ‘Golden Delicious’ apple fruits: a one-season comparison study of organic and integrated production systems in Switzerland. Microb Ecol 56:720–732

    Article  PubMed  Google Scholar 

  • Hall JA (1934) Observations on the behavior of newly hatched codling moth larvae. Can Entomol 66:100–102

    Article  Google Scholar 

  • Hoerner JL (1925) Notes on codling moth larvae. J Econ Entomol 18:423–424

    Google Scholar 

  • Hughes WO, Gailey DD, Knapp JJ (2003) Host location by adult and larval codling moth and the potential for its disruption by the application of kairomones. Entomol Exp Appl 106:147–153

    Article  Google Scholar 

  • Jackson DM (1979) Codling moth egg distribution on unmanaged apple trees. Ann Entomol Soc Am 72:361–368

    Google Scholar 

  • Jacques RP, Laing JE, Laing DR, Yu DSK (1987) Effectiveness and persistence of the granulosis virus of the codling moth Cydia pomonella (L.) (Lepidoptera: Olethreutidae) on apple. Can Entomol 119:1063–1067

    Article  Google Scholar 

  • Jones VP, Unruh TR, Horton DR, Mills NJ, Brunner JF, Beers EH (2009) Tree fruit IPM programs in western United States: the challenge of enhancing biological control through intensive management. Pest Manag Sci 65:1305–1310

    Article  PubMed  CAS  Google Scholar 

  • Jumean Z, Gries R, Unruh T, Rowland E, Gries G (2005) Identification of the larval aggregation pheromone of codling moth, Cydia pomonella. J Chem Ecol 31:911–924

    Article  PubMed  CAS  Google Scholar 

  • Knight AL (2008) Codling moth areawide integrated pest management. In: Koul O, Cuperus GW, Elliot N (eds) Areawide pest management: theory and implementation. CAB International, Wallingford, pp 159–190

    Chapter  Google Scholar 

  • Knight AL, Light DM (2001) Attractants from Bartlett pear for codling moth, Cydia pomonella (L.), larvae. Naturwissenschaften 88:339–342

    Article  PubMed  CAS  Google Scholar 

  • Knight AL, Brunner JF, Alston D (1994) Survey of azinphos-methyl resistance in codling moth (Lepidoptera: Tortricidae) in Washington and Utah. J Econ Entomol 87:285–292

    CAS  Google Scholar 

  • Kreher SA, Kwon JY, Carlson JR (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46:445–456

    Article  PubMed  CAS  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 53:121–144

    Article  PubMed  CAS  Google Scholar 

  • Lacey LA, Arthurs SP, Knight AL, Huber J (2007) Microbial control of lepidopteran pests of apple orchards. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology. Springer, Dordrecht, pp 527–546

    Chapter  Google Scholar 

  • Lacey LA, Thomson D, Vincent C, Arthurs SP (2008) Codling moth granulovirus: a comprehensive review. Biocontrol Sci Technol 18:639–663

    Article  Google Scholar 

  • Landolt PJ, Hofstetter RW, Biddick LL (1999) Plant essential oils as arrestants and repellents for neonate larvae of the codling moth (Lepidoptera: Tortricidae). Environ Entomol 28:954–960

    CAS  Google Scholar 

  • Light DM, Beck JJ (2010) Characterization of microencapsulated pear ester, (2E,4Z)-ethyl-2,4-decadienoate, a kairomonal spray adjuvant against neonate codling moth larvae. J Agric Food Chem 58:7836–7845

    Article  Google Scholar 

  • Light DM, Beck JJ (2012) Behavioral responses of codling moth (Lepidoptera: Tortricidae) neonate larvae on surfaces treated with microencapsulated pear ester. Environ Entomol 41:603–611

    Article  PubMed  Google Scholar 

  • Light DM, Knight AL (2011) Microencapsulated pear ester enhances insecticide efficacy in walnut for codling moth (Lepidoptera; Tortricidae) and navel orangeworm (Lepidoptera: Pyralidae). J Econ Entomol 104:1309–1315

    Article  PubMed  CAS  Google Scholar 

  • Lombarkia N, Derridj S (2008) Resistance of apple trees to Cydia pomonella egg-laying due to leaf surface metabolites. Entomol Exp Appl 128:57–65

    Article  CAS  Google Scholar 

  • Martin D, Bedel de Buzareingues F, Barry B, Derridj S (1993) An epiphytic yeast (Sporobolomyces roseus) influencing in oviposition rpeference of the European corn borer (Ostrinia nubilasis) on maize. Acta Oecologia 14:563–574

    Google Scholar 

  • Martinez-Rocha L, Beers EH, Dunley JE (2008) Effect of pesticides on integrated mite management in Washington State. J Entomol Soc Br Columbia 105:97–107

    Google Scholar 

  • Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Entomol 36:563–595

    Google Scholar 

  • Piesik D, Rochat D, van der Pers J, Marion-Poll F (2009) Pulsed odors from maize or spinach elicit orientation in European corn borer neonate larvae. J Chem Ecol 35:1032–1042

    Article  PubMed  CAS  Google Scholar 

  • Poivet E, Rharrabe K, Monsempes C, Glaser N, Rochat D, Renou M, Marion-Poll F, Jacquin-Joly E (2012) The use of the sex pheromone as an evolutionary solution to food source selection in caterpillars. Nat Comm 3:1047

    Article  Google Scholar 

  • Poivet E, Gallot A, Montagne N, Glaser N, Legeai F, Jacquin-Joly E (2013) A comparison of the olfactory gene repertoires of adults and larvae in the noctuid moth Spodoptera littoralis. PLoS One 8:e60263

    Article  PubMed  CAS  Google Scholar 

  • Raman A, Wheatley W, Popay A (2012) Endophytic fungus-vascular plant-insect interactions. Environ Entomol 41:433–447

    Article  PubMed  CAS  Google Scholar 

  • Sauphanor B, Brosse V, Bouvier JC, Speich P, Micoud A, Martinet C (2000) Monitoring resistance to diflubenzuron and deltamethrin in French codling moth populations (Cydia pomonella). Pest Manag Sci 56:74–82

    Article  CAS  Google Scholar 

  • Sauphanor B, Berling M, Toubon JF, Reyes M, Delnatte J, Allemoz P (2006) Carpocapse des pommes. Cas de ressitance au virus de la granulose en vergers biologique. Phytoma Déf Veg 590:24–27

    Google Scholar 

  • Schisler DA, Janisiewicz WJ, Boekhout T, Kurtzman CP (2010) Agriculturally important yeasts: biological control of field and postharvest diseases using yeast antagonists, and yeasts as pathogens of plants. In: Kurtzman CP, Fell JW, Boekhaut T (eds) The yeasts, a taxonomic study. Elsevier, New York, pp 45–52

    Google Scholar 

  • Schmidt S, Tomasi C, Pasqualini E, Ioriatti C (2008) The biological efficacy of pear ester on the activity of granulosis virus for codling moth. J Pest Sci 81:29–34

    Article  Google Scholar 

  • Sharma RR, Singh D, Singh R (2009) Biological control of postharvest diseases of fruits and vegetables by microbial antagonisists: a review. Biol Control 50:205–221

    Article  Google Scholar 

  • Slaviková E, Vadkertiova R (2003) Effects of pesticides on yeasts isolated from agricultural soil. Z Naturforsch 58:855–859

    Google Scholar 

  • Sutherland ORW, Hutchins RFN (1972) α-farnesene, a natural attractant for codling moth larvae. Nature 239:170

    Article  CAS  Google Scholar 

  • Trona F, Anfora G, Balkenius A, Bengtsson M, Tasin M, Knight A, Janz N, Witzgall P, Ignell R (2013) Neural coding merges sex and habitat chemosensory signals in an insect herbivore. Proc R Soc B 280:20130267

    Article  PubMed  Google Scholar 

  • Vasquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7(3):e33188

    Article  PubMed  CAS  Google Scholar 

  • Walter M, Frampton CM, Boyd-Wilson KS, Harris-Virgin P, Walpara NW (2007) Agrichemical impact on growth and survival of non-target apple phyllosphere microorganisms. Can J Microbiol 53:45–55

    Article  PubMed  CAS  Google Scholar 

  • Witzgall P, Stelinski L, Gut L, Thomson D (2008) Codling moth management and chemical ecology. Annu Rev Entomol 53:503–522

    Article  PubMed  CAS  Google Scholar 

  • Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pest management. J Chem Ecol 36:80–100

    Article  PubMed  CAS  Google Scholar 

  • Witzgall P, Proffit M, Rozpedowska E, Becher PG, Andreadis S, Coracini M, Lindblom TUT, Ream LJ, Hagman A, Bengtsson M, Kurtzman CP, Piskur J, Knight A (2012) “This is not an apple” — yeast mutualism in codling moth. J Chem Ecol 38:949–957

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank several co-workers at the Agricultural Research Service, U.S.D.A. in Wapato, WA. Duane Larson and Lee Ream provided technical assistance in the laboratory and field, and Dave Horton provided statistical advice. Cletus Kurtzman, U.S.D.A. in Peoria, IL provided the molecular identifications of the yeast species. P. W. is supported by the Linnaeus environment “Insect Chemical Ecology, Ethology, and Evolution” IC-E3 (Formas, SLU).

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Correspondence to Alan L. Knight.

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Knight, A.L., Witzgall, P. Combining Mutualistic Yeast and Pathogenic Virus — A Novel Method for Codling Moth Control. J Chem Ecol 39, 1019–1026 (2013). https://doi.org/10.1007/s10886-013-0322-z

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