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Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta

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Abstract

The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) has recently invaded Mediterranean countries and is a major pest in tomato crops. Trichogrammatid oophagous parasitoids have shown promising potential for controlling the pest before the yield decreases in the greenhouse. In protected tomato crops (greenhouse), mirid predators are commonly used for biological control of whiteflies and they also prey on T. absoluta. These predators do not attack Trichogramma adults but they may partially decrease the overall impact of parasitoids on T. absoluta if intraguild predation (IGP) occurs on parasitized eggs. Under laboratory conditions, we tested if the mirid predator Macrolophus pygmaeus shows preference between parasitized and unparasitized T. absoluta eggs. We also tested if the predator reduces the number of parasitized eggs on caged tomato plants (microcosms) and assessed the efficacy of natural enemies used alone or together in limiting T. absoluta populations. We found that IGP is inflicted on the parasitoid Trichogramma achaeae by M. pygmaeus and that the risk of IGP depends on the developmental stage of T. achaeae inside the egg because the larva is at risk mostly early in its development (when parasitized egg is still yellow). In addition, we observed that non-consumptive events, likely probing of the predator on parasitized eggs, may induce mortality in parasitoid offspring without actual feeding on parasitized eggs. However, both IGP and non-consumptive events decreased when the predator was not confined with parasitized eggs in small arenas. Despite negative effects of the predator to the parasitoid, results demonstrate that adding Trichogramma parasitoids may significantly increase the level of control of the pest over what could be attained when only the mirid predator M. pygmaeus is present on tomato. Implications of results are discussed regarding potential of these natural enemies for biological control of T. absoluta in greenhouse tomato crops.

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References

  • Andrade GS, Pratissoli D, Dalvi LP, Desneux N, Gonçalves HJ (2011) Performance of four Trichogramma species (Hymenoptera: Trichogrammatidae) as biocontrol agents of Heliothis virescens (Lepidoptera: Noctuidae) under various temperature regimes. J Pest Sci 84:313–320

    Article  Google Scholar 

  • Arno J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520

    Article  Google Scholar 

  • Barrientos ZR, Apablaza HJ, Norero SA, Estay PP (1998) Temperatura base y constante térmica de desarrollo de la polilla del tomate, Tuta absoluta (Lepidoptera: Gelechiidae). Ciencia e Investigación Agraria 25:133–137

    Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012a) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812

    Article  PubMed  CAS  Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Vinuela E, Zappalà L, Desneux N (2012b) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536

    Article  PubMed  CAS  Google Scholar 

  • Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Pop Ecol. doi:10.1007/s10144-013-0371-8

    Google Scholar 

  • Bonato O, Couton L, Fargues J (2006) Feeding preference of Macrolophus caliginosus (Heteroptera : Miridae) on Bemisia tabaci and Trialeurodes vaporariorum (Homoptera : Aleyrodidae). J Econ Entomol 99:1143–1151

    Article  PubMed  Google Scholar 

  • Brodeur J, Boivin G (2004) Functional ecology of immature parasitoids. Annu Rev Entomol 49:27–49

    Article  PubMed  CAS  Google Scholar 

  • Brower JH, Press JW (1988) Interactions between the egg parasite Trichogramma pretiosum (Hym.: Trichogrammatidae) and a predator, Xylocoris Javipes (Hem.: Anthocoridae) of the almond moth Cudra cautella (Lep.: Pyralidae). J Entomol Sci 23:342–349

    Google Scholar 

  • Butler CD, O’Neil RJ (2006) Defensive response of soybean aphid (Hemiptera : Aphididae) to predation by insidious flower bug (Hemiptera : Anthocoridae). Ann Entomol Soc Am 99:317–320

    Article  Google Scholar 

  • Cabello T, Gallego JR, Vila E, Soler A, del Pino M et al (2009) Biological control of the South American tomato pinworm, Tuta absoluta (Lep.: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain. IOBC/WPRS Bull 49:225–230

    Google Scholar 

  • Cabello T, Gallego JR, Fernandez FJ, Gamez M, Vila E, Del Pino M, Hernandez-Suarez E (2012) Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes. J Eco Entomol 105:2085–2096

    Article  Google Scholar 

  • Calvo J, Blockmans K, Stansly PA, Urbaneja A (2009) Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato. Biocontrol 54:237–246

    Article  Google Scholar 

  • Calvo FJ, Lorente MJ, Stansly PA, Belda JE (2012) Preplant release of Nesidiocoris tenuis and supplementary tactics for control of Tuta absoluta and Bemisa tabaci in greenhouse tomato. Entomol Exp Appl 143:111–119

    Article  Google Scholar 

  • Castane C, Arno J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29

    Article  Google Scholar 

  • Chacon JM, Heimpel GE (2010) Density-dependent intraguild predation of an aphid parasitoid. Oecologia 164:213–220

    Article  PubMed  Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Maignet P, Khanh HDT, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS One 7:e48068

    Article  PubMed  CAS  Google Scholar 

  • Cohen AC (1990) Feeding adaptations of some predaceous Hemiptera. Ann Entomol Soc Am 83:1215–1223

    Google Scholar 

  • Coll M, Ridway RL (1995) Functional and numerical responses of Orius insidiosus (Heteroptera: Anthocoridae) to its prey in different vegetable crops. Ann Entomol Soc Am 88:732–738

    Google Scholar 

  • Desneux N, O’Neil RJ (2008) Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions. Bull Entomol Res 98:631–639

    Article  PubMed  CAS  Google Scholar 

  • Desneux N, O’Neil RJ, Yoo HJS (2006) Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identification of a key predator, and the effects of prey dispersion, predator density and temperature. Environ Entomol 35:1342–1349

    Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  PubMed  CAS  Google Scholar 

  • Desneux N, Barta RJ, Delebecque CJ, Heimpel GE (2009a) Transient host paralysis as a means of reducing self-superparasitism in koinobiont endoparasitoids. J Insect Physiol 55:321–327

    Article  PubMed  CAS  Google Scholar 

  • Desneux N, Starỳ P, Delebecque CJ, Gariepy TD, Barta RJ, Hoelmer KA, Heimpel GE (2009b) Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae). Ann Entomol Soc Am 102:925–936

    Article  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, history of invasion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011a) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Desneux N, Pizzol J, Thomas C, Pautrat E, Bearez P, Poncet C, Tabone E, Kabiri F, Frandon J (2011b) Potential for direct interference between natural enemies of Tuta absoluta on tomato. Acta Hortic 917:31–37

  • Edwards JS (1961) The action and composition of the saliva of an assassin bug Platymeris rhadamanthus Gaerst. (Hemiptera, Reduviidae). J Exp Biol 38:61–77

    CAS  Google Scholar 

  • Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–652

    Article  Google Scholar 

  • Herrick NJ, Reitz SR, Carpenter JE, O’Brien CW (2008) Predation by Podisus maculiventris (Hemiptera: Pentatomidae) on Plutella xylostella (Lepidoptera: Plutellidae) larvae parasitized by Cotesia plutellae (Hymenoptera: Braconidae) and its impact on cabbage. Biol Control 45:386–395

    Article  Google Scholar 

  • Hoelmer KA, Osborne LS, Yokomi RK (1994) Interactions of the whitefly predator Delphastus pusillus (Coleoptera: Coccinellidae) with parasitized sweetpotato whitefly (Homoptera: Aleyrodidae). Environ Entomol 23:136–139

    Google Scholar 

  • Hoffmann MP, Pitcher SA, Cheever SA, Gardner J, Losey JE et al (2006) Efficacy of inoculative releases of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) against European corn borer Ostrinia nubilalis (Lepidoptera: Crambidae) in field corn. Biol Control 36:345–349

    Article  Google Scholar 

  • Holt RD, Huxel GR (2007) Alternative prey and the dynamics of intraguild predation: theoretical perspectives. Ecology 88:2706–2712

    Article  PubMed  Google Scholar 

  • Khanh HDT, Tiradon M, Colombel E, Bonnet A, Chailleux A, Desneux N, Tabone E (2012) Using new egg parasitoids (Trichogramma spp.) to improve integrated management against Tuta absoluta. Bull OEPP/EPPO Bull 42:249–254

    Article  Google Scholar 

  • Knutson A (2005) The Trichogramma manual: a guide to the use of Trichogramma for biological control with special reference to augmentative releases for control of bollworm and budworm in cotton. Texas A&M University System, College Station

    Google Scholar 

  • Kuhar TP, Wright MG, Hoffmann MP, Chenus SA (2002) Life table studies of European corn borer (Lepidoptera: Crambidae) with and without inoculative releases of Trichogramma Ostriniae (Hymenoptera: Trichogrammatidae). Environ Entomol 31:482–489

    Article  Google Scholar 

  • Langellotto GA, Denno RF (2006) Refuge from cannibalism in complex-structured habitats: implications for the accumulation of invertebrate predators. Ecol Entomol 31:575–581

    Article  Google Scholar 

  • Lu YH, Wu KM, Jiang YY, Guo YY, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    Google Scholar 

  • Mbata GN, Shapiro-Ilan DI (2010) Compatibility of Heterorhabditis indica (Rhabditida: Heterorhabditidae) and Habrobracon hebetor (Hymenoptera: Braconidae) for biological control of Plodia interpunctella (Lepidoptera: Pyralidae). Biol Control 54:75–82

    Article  Google Scholar 

  • Mills N (2010) Egg parasitoids in biological control and integrated pest management. In: Consoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma, vol 9. Springer, Berlin Heidelberg New York, pp 389–411

  • Moses DN, Harreld JH, Stucky GD, Waite JH (2006) Melanin and glycera jaws: emerging dark side of a robust biocomposite structure. J Biol Chem 281:34826–34832

    Article  PubMed  CAS  Google Scholar 

  • Mouttet R, Bearez P, Thomas C, Desneux N (2011) Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLoS One 6:e18840

    Article  PubMed  CAS  Google Scholar 

  • Müller CB, Brodeur J (2002) Intraguild predation in biological control and conservation biology. Biol Control 25:216–223

    Article  Google Scholar 

  • Nannini M, Foddi F, Murgia G, Pisci R, Sanna F (2007) Natural enemies for tomato pest control in Sardinian greenhouses. Acta Hortic 747:415–423

    Google Scholar 

  • Parra JRP, Zucchi RA (2004) Trichogramma in Brazil: feasibility of use after twenty years of research. Neotrop Entomol 33:271–281

    Article  Google Scholar 

  • Philip MM, Orr DB, Hain FP (2005) Evaluation of biological and biorational control tactics for suppression of Nantucket pine tip moth damage in Virginia pine Christmas trees. J Econ Entomol 98:409–414

    Article  PubMed  Google Scholar 

  • Pintureau B, Petinon S, Nardon C (1999) Rôle possible des substances excrétées par les Trichogrammes et assombrissant leur hôtes. Bull Soc Zool France 124:261–269

    Google Scholar 

  • Pizzol J, Pintureau B, Khoualdia O, Desneux N (2010) Temperature-dependent differences in biological traits between two strains of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). J Pest Sci 83:447–452

    Google Scholar 

  • Pizzol J, Desneux N, Wajnberg E, Thiery D (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J Pest Sci 85:489–496

    Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • Poncet C, Mailleret L, Desneux N, Muller MM, Bout A, Brun R, Pizzol J, Boll R, Bresch C, Parolin P, Fatnassi H (2012) Ecological approach of greenhouse agro-ecosystem: practical interest for IPM. Acta Hortic 927:173–185

    Google Scholar 

  • Pratissoli D, Thuler RT, Andrade GS, Zanotti LCM, Silva AF (2005) Estimate of Trichogramma pretiosum to control Tuta absoluta in stalked tomato. Pesq Agropecu Bras 40:715–718

    Article  Google Scholar 

  • Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399

    Article  PubMed  CAS  Google Scholar 

  • Roger C, Coderre D, Vigneault C, Boivin G (2001) Prey discrimination by a generalist coccinellid predator: effect of prey age or parasitism? Ecol Entomol 26:163–172

    Article  Google Scholar 

  • Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335

    Article  Google Scholar 

  • Rouechdi KA, Voegelé J (1981) Prédation des trichogrammes par les chrysopides. Agronomie 1:187–190

    Article  Google Scholar 

  • Ruberson JR, Kring JT (1991) Predation of Trichogramma pretiosum by the anthocorid Orius insidiosus. In: Trichogramma and other Egg Parasitoids, vol 56. Les Colloques de l’INRA, pp 41–43

  • Rutledge CE, O’Neil RJ (2005) Orius insidiosus (Say) as a predator of the soybean aphid, Aphis glycines Matsumura. Biol Control 33:56–64

    Article  Google Scholar 

  • Smith SM (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41:375–406

    Article  PubMed  CAS  Google Scholar 

  • Suckling DM, Brockerhoff EG (2010) Invasion biology, ecology, and management of the light brown apple moth (Tortricidae). Annu Rev Entomol 55:285–306

    Article  PubMed  CAS  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Google Scholar 

  • Tabone T, Bardon C, Desneux N, Wajnberg E (2010) Comparative assessment of parasitism of different Trichogramma spp.on Plutella xylostella L. on greenhouse cauliflower. J Pest Sci 83:251–256

    Article  Google Scholar 

  • Tabone E, Bardon C, Desneux N (2012) Dispersal study as Trichogrammatidae selection criteria for biological control in cauliflower greenhouses. Acta Hortic 927:227–235

    Google Scholar 

  • Thomas MB (1999) Ecological approaches and the development of ‘truly integrated’ pest management. Proc Natl Acad Sci USA 96:5944–5951

    Article  PubMed  CAS  Google Scholar 

  • Thomson LJ, Bennett DM, Glenn DC, Hoffmann AA (2003) Developing Trichogramma as a pest management tool. In: Koul O, Dhaliwal GS (eds) Predators and parasitoids. Taylor and Francis, London, pp 65–85

  • Trottin-Caudal Y, Chabriere C, Baffert V, Leyre JM, Terrentroy A, Hulas N (2011) Etudes expérimentales sur Tuta absoluta (Meyrick) en cultures de tomate sous serre et abri: protection biologique et démarche de protection intégrée. In: AFPP—8eme Conférence Internationale sur les méthodes alternatives en protection des cultures, Lille, France, 8–10 Mars 2011

  • Urbaneja A, Monton H, Molla O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133:292–296

    Article  Google Scholar 

  • Yuan XH, Song LW, Zhang JJ, Zang LS, Zhu L, Ruan CC, Sun GZ (2012) Performance of four Chinese Trichogramma species as biocontrol agents of the rice striped stem borer, Chilo suppressalis, under various temperature and humidity regimes. J Pest Sci 85:497–504

    Google Scholar 

  • Zappala L, Bernardo U, Biondi A, Cocco A, Deliperi S, Delrio G, Giorgini M, Pedata P, Rapisarda C, Garzia GT, Siscaro G (2012) Recruitment of native parasitoids by the exotic pest Tuta absoluta in Southern Italy. Bull Insectol 65:51–61

    Google Scholar 

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Acknowledgments

We thank Dr. David Ragsdale for helpful comments on the manuscript, Emmanuelle Pautrat and Cécile Thomas for technical assistance, Méline Beal and Jacques Frandon (Biotop) for providing some biological materials, ANRT and InVivo AgroSolutions for funding to AC (PhD fellowship), and the Plant Health & Environment Department of INRA and the French Ministry of Agriculture for funding to ND (CASDAR Project 10063).

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  1. French National Institute for Agricultural Research (INRA), UMR1355-ISA, Sophia-Antipolis, France

    Anaïs Chailleux, Philippe Bearez, Jeannine Pizzol, Edwige Amiens-Desneux & Nicolas Desneux

  2. InVivo AgroSolutions, 83 Avenue de la Grande Armée, 75782, Paris, France

    Anaïs Chailleux

  3. Departamento de Producción Agrícola, Universidad de Guadalajara, CUCBA, Jalisco, Zapopan, Mexico

    Ricardo Ramirez-Romero

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  1. Anaïs Chailleux
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  2. Philippe Bearez
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  3. Jeannine Pizzol
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  4. Edwige Amiens-Desneux
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  5. Ricardo Ramirez-Romero
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  6. Nicolas Desneux
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Correspondence to Nicolas Desneux.

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Communicated by M. Traugott

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Chailleux, A., Bearez, P., Pizzol, J. et al. Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta . J Pest Sci 86, 533–541 (2013). https://doi.org/10.1007/s10340-013-0498-6

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