BioControl

, Volume 61, Issue 6, pp 639–647 | Cite as

Molecular characterization of parasitoids from armored scales infesting citrus orchards in Corsica, France

  • Margarita C. G. Correa
  • Ferran Palero
  • Noémie Dubreuil
  • Laure Etienne
  • Mathieu Hulak
  • Gilles Tison
  • Sylvie Warot
  • Didier Crochard
  • Nicolas Ris
  • Philippe Kreiter
Article
  • 207 Downloads

Abstract

Armored scales (Hemiptera: Diaspididae) are important pests in citrus orchards worldwide. Augmentative releases of Aphelinidae wasps (Hymenoptera) have been performed in Corsica, France to control the California Red Scale (Aonidiella aurantii (Maskell, 1879)) and the arrowhead scale (Unaspis yanonensis (Kuwana, 1923)), but biological control of armored scales requires the identification of their parasitoids to evaluate their potential as biological control agents. In order to circumvent this issue, parasitoids emerging from four armored scale species were characterized through DNA barcoding. All the parasitoids identified belong to the Aphelinidae (Hymenoptera) and included a total of five Aphytis (including A. melinus), four Encarsia (including cryptic species) and one Ablerus (hyperparasitoid) species. Host-specificity was found to be strong among primary parasitoids, with Encarsia inquirenda Silvestri, 1930 and an unidentified Encarsia being the sole taxa able to parasitize the two subfamilies (Aspidiotinae and Diaspidinae).

Keywords

Diaspididae Armored scale Parasitoid DNA barcoding Cryptic species 

Supplementary material

10526_2016_9752_MOESM1_ESM.docx (27 kb)
Supplementary material 1 (DOCX 26 kb)

References

  1. Abd-Rabou S, Shalaby H, Germain J, Ris N, Kreiter P, Malausa T (2012) Identification of mealybug pest species (Hemiptera: Pseudococcidae) in Egypt and France, using a DNA barcoding approach. Bull Entomol Res 102:1–9CrossRefGoogle Scholar
  2. Agreste (2015) Agreste, statistique agricole annuelle. Retrieved from http://www.agreste.agriculture.gouv.fr/enquetes/statistique-agricole-annuelle-saa/
  3. Babcock CS, Heraty JM (2000) Molecular markers distinguishing Encarsia formosa and Encarsia luteola (Hymenoptera: Aphelinidae). Ann Entomol Soc Am 93:738–744CrossRefGoogle Scholar
  4. Beardsley JW, Gonzalez RH (1975) The biology and ecology of armored scales. Annu Rev Entomol 20:47–73CrossRefPubMedGoogle Scholar
  5. Beltrà A, Addison P, Ávalos JA, Crochard D, Garcia-Marí F, Guerrieri E, Giliomee JH, Malausa T, Navarro-Campos C, Palero F, Soto A (2015) Guiding classical biological control of an invasive mealybug using integrative taxonomy. PLoS ONE 10(6):e0128685CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ben-Dov Y, Miller DR, Gibson GAP (2010) Scale Net. Retrieved from http://scalenet.info/
  7. Boyero JR, Vela JM, Wong E, Garcia-Ripoll C, Verdu MJ, Urbaneja A, Vanaclocha P (2014) Displacement of Aphytis chrysomphali by Aphytis melinus, parasitoids of the California Red Scale, in the Iberian Peninsula. Span J Agric Res 12:244–251CrossRefGoogle Scholar
  8. De León JH, Neumann G, Follett P, Hollingsworth RG (2010) Molecular markers discriminate closely related species Encarsia diaspidicola and Encarsia berlesei (Hymenoptera: Aphelinidae): biocontrol candidate agents for white peach scale in Hawaii. J Econ Entomol 103:908–916CrossRefPubMedGoogle Scholar
  9. Ebrahimi E (2014) Parasitoid and hyperparasitoid wasps of scale insects in Hayk Mirzayans Insect Museum, Iran. J Entomol Soc Iran 34:73–83Google Scholar
  10. Etienne L, Jaloux B (2014) Incidence de lâchers inondatifs du parasitoïde Aphytis melinus sur la biodiversité en vergers d’agrumes en Corse. Université d’Angers, FranceGoogle Scholar
  11. Flint M, Kobbe B, Clark J, Dreistadt S, Pehrson J, Flaherty D, O’Connell NV, Phillips PA, Morse J (1991) Integrated pest management for citrus, 2nd edn. University of California, OaklandGoogle Scholar
  12. Gariepy TD, Haye T, Zhang J (2014) A molecular diagnostic tool for the preliminary assessment of host-parasitoid associations in biological control programmes for a new invasive pest. Mol Ecol 23:3912–3924CrossRefPubMedGoogle Scholar
  13. Gómez-Marco F, Urbaneja A, Jaques JA, Rugman-Jones PF, Stouthamer R, Tena A (2015) Untangling the aphid-parasitoid food web in citrus: can hyperparasitoids disrupt biological control? Biol Control 81:111–121CrossRefGoogle Scholar
  14. Grafton-Cardwell EE, Ouyang Y, Striggow R, Vehrs S (2004) Role of esterase enzymes in monitoring for resistance of California Red Scale, Aonidiella aurantii (Homoptera: Diaspididae), to organophosphate and carbamate insecticides. J Econ Entomol 97:606–613CrossRefPubMedGoogle Scholar
  15. Grafton-Cardwell EE, Lee JE, Stewart JR, Olsen KD (2006) Role of two insect growth regulators in integrated pest management of citrus scales. J Econ Entomol 99:733–744CrossRefPubMedGoogle Scholar
  16. Grafton-Cardwell E, Ouyang Y, Striggow R, Vehrs S (2008) Armored scale insecticide resistance challenges San Joaquin Valley citrus growers. Calif Agric 55:20–25CrossRefGoogle Scholar
  17. Hardy NB (2008) Systematic studies of scale insects (Hemiptera: Coccoidea). University of California, Davis, USAGoogle Scholar
  18. Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321CrossRefPubMedPubMedCentralGoogle Scholar
  19. Heraty J, Woolley J, Polaszek A (2007) Catalog of the Encarsia of the World (2007). http://cache.ucr.edu/~heraty/Encarsia.cat.pdf
  20. Kattari D, Heimpel GE, Ode P, Rosenheim J (1999) Hyperparasitism by Ablerus clisiocampae Ashmead (Hymenoptera: Aphelinidae). Proc Entomol Soc Wash 101:640–644Google Scholar
  21. Liang W, Meats A, Beattie GAC, Spooner-Hart R, Jiang L (2010) Conservation of natural enemy fauna in citrus canopies by horticultural mineral oil: comparison with effects of carbaryl and methidathion treatments for control of armored scales. Insect Sci 17:414–426CrossRefGoogle Scholar
  22. Malausa JC, Rabasse JM, Kreiter P (2008) Les insectes entomophages d’interet agricole acclimates en France metropolitaine depuis le debut du 20ème siecle. Bull OEPP/EPPO 38:136–146CrossRefGoogle Scholar
  23. Malausa T, Fenis A, Warot S, Germain JF, Ris N, Prado E, Botton M, Vanlerberghe-Masutti F, Sforza R, Cruaud C, Couloux A, Kreiter P (2011) DNA markers to disentangle complexes of cryptic taxa in mealybugs (Hemiptera: Pseudococcidae). J Appl Entomol 135:142–155CrossRefGoogle Scholar
  24. Monti MM, Nappo AG, Giorgini M (2005) Molecular characterization of closely related species in the parasitic genus Encarsia (Hymenoptera: Aphelinidae) based on the mitochondrial cytochrome oxidase subunit I gene. Bull Entomol Res 95:401–408CrossRefPubMedGoogle Scholar
  25. Munro JB, Heraty JM, Burks R, Hawks D, Mottern J, Cruaud A, Rasplus JY, Jansta P (2011) A molecular phylogeny of the Chalcidoidea (Hymenoptera). PLoS ONE 6(11):e27023CrossRefPubMedPubMedCentralGoogle Scholar
  26. Murdoch WW, Swarbrick SL, Briggs CJ (2006) Biological control: lessons from a study of California Red Scale. Popul Ecol 48:297–305CrossRefGoogle Scholar
  27. Pina T, Verdú MJ, Urbaneja A, Sabater-Muñoz B (2012) The use of integrative taxonomy in determining species limits in the convergent pupa coloration pattern of Aphytis species. Biol Control 61:64–70CrossRefGoogle Scholar
  28. Rosen D (1994) Advances in the study of Aphytis (Hymenoptera: Aphelinidae). Intercept Limited, AndoverGoogle Scholar
  29. Rosen D, DeBach P (1979) Species of Aphytis of the world. Springer, NetherlandsCrossRefGoogle Scholar
  30. Rugman-Jones PF, Forster LD, Guerrieri E, Luck RF, Morse JG, Monti MM, Stouthamer R (2011) Taxon-specific multiplex-PCR for quick, easy, and accurate identification of encyrtid and aphelinid parasitoid species attacking soft scale insects in California citrus groves. BioControl 56:265–275CrossRefGoogle Scholar
  31. Schmidt S, Polaszek A (2007) Encarsia or Encarsiella?—redefining generic limits based on morphological and molecular evidence (Hymenoptera, Aphelinidae). Syst Entomol 32:81–94CrossRefGoogle Scholar
  32. Sorribas J, Garcia-Marí F (2010) Comparative efficacy of different combinations of natural enemies for the biological control of California Red Scale in citrus groves. Biol Control 55:42–48CrossRefGoogle Scholar
  33. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035CrossRefPubMedPubMedCentralGoogle Scholar
  34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  35. Tena A, Garcia-Marí F (2011) Current situation of citrus pests and diseases in the Mediterranean basin. IOBC/WPRS Bull 62:365–378Google Scholar
  36. Tison G, Kreiter P, Giuge L, Thaon M, Jeanne Y, Lemay V, Daoux F, Bénaouf G, Balajas J, Duval X, Borelli JG (2007) Pou rouge de Californie et agrumiculture corse. Phytoma-La Défense des végétaux 606:18–21Google Scholar
  37. Zaldívar-Riverón A, Martínez JJ, Ceccarelli FS, De Jesús-Bonilla VS, Rodríguez-Pérez AC, Reséndiz-Flores A, Smith MA (2010) DNA barcoding a highly diverse group of parasitoid wasps (Braconidae: Doryctinae) from a Mexican nature reserve. Mitochondrial DNA 21(Suppl 1):18–23CrossRefPubMedGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2016

Authors and Affiliations

  • Margarita C. G. Correa
    • 1
  • Ferran Palero
    • 1
    • 4
  • Noémie Dubreuil
    • 2
  • Laure Etienne
    • 2
  • Mathieu Hulak
    • 2
  • Gilles Tison
    • 3
  • Sylvie Warot
    • 1
  • Didier Crochard
    • 1
  • Nicolas Ris
    • 1
  • Philippe Kreiter
    • 1
  1. 1.INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia AgrobiotechSophia AntipolisFrance
  2. 2.AREFLEC, Corsic’AgropôleSan GiulianoFrance
  3. 3.INRA Centre de San Giuliano, Unité citrus, Pôle agronomiqueSan GiulianoFrance
  4. 4.Centre d’Estudis Avançats de Blanes (CEAB-CSIC)BlanesSpain

Personalised recommendations