Eur. J. Entomol. 109 (4): 561-568, 2012 | 10.14411/eje.2012.070

Dispersal of Aphytis melinus (Hymenoptera: Aphelinidae) after augmentative releases in citrus orchards

Lucia ZAPPALÀ1, Orlando CAMPOLO2, Saverio Bruno GRANDE2, Francesco SARACENO3, Antonio BIONDI1, Gaetano SISCARO1, Vincenzo PALMERI2
1 Department of Agri-food and Environmental Systems Management, University of Catania, via Santa Sofia 100, 95123 Catania, Italy; e-mails: lzappala@unict.it; antonio.biondi@unict.it; gsiscaro@unict.it
2 Department of Agricultural and Forest Systems Management, University of Reggio Calabria, loc. Feo di Vito, 89122 Reggio Calabria, Italy; e-mails: orlando.campolo@unirc.it; saverio.grande@unirc.it; vpalmeri@unirc.it
3 Sicilian Regional Food and Agriculture Assessorship, Department of Structural Intervention in Agriculture, Plant Protection Serv ice U.O. 42, Via Sclafani 34, 95024 Acireale (CT), Italy; e-mail: fsaraceno@regione.sicilia.it

The efficacy of natural enemies in controlling pests under field conditions is largely correlated with their capacity to spread within infested crops. In this study the spatial dispersal of the California red scale parasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae) was evaluated in the field after augmentative releases. The experiment was conducted in 2007 in six 1-ha plots in a Sicilian citrus orchard under integrated pest management. A total of 180,000 A. melinus adults was released in each of three plots and the other plots were left as untreated control. The flight range of the parasitoid was evaluated, for 35 days after the release, on 16 trees per each plot, located at 20 and 40 m from the central release point using yellow sticky traps activated with Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae) sexual pheromone and by monitoring the percentage parasitism of the scale on fruits and twigs. The effects of the distance from the release point and density of susceptible stages of host on parasitoid dispersal were evaluated. The number of wasps captured during the whole trial was greater in the traps located 20 m from the release point than in those at 40 m and in the control plots. Aphytis melinus dispersed over distances less than 40 m based on both the lower percentage parasitism and numbers captured recorded at distances of 40 m. The results are discussed in the context of the biological control of California red scale in citrus orchards by means of wasp releases. In particular, the release points should be no more than 40 m apart for a quick and homogeneous colonization of the area treated.

Keywords: Aphelinidae, California red scale, biological control, parasitoid, flight range, spatial interpolation

Received: February 3, 2012; Accepted: June 20, 2012; Published: October 5, 2012

Download citation

References

  1. BERNAL J.S. & LUCK R.F. 2007: Mate finding via a trail sex pheromone by Aphytis melinus De Bach (Hymenoptera: Aphelinidae) males. J. Insect Behav. 20: 515-525 Go to original source...
  2. BROWN M.W. & CAMERON E.A. 1979: Effect of disparlure and egg mass size on parasitism by the gypsy moth egg parasite, Ooencyrtus kuwanai. Environ. Entomol. 8: 77-80 Go to original source...
  3. CORBETT A. & ROSENHEIM J.A. 1996: Quantifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biol. Control 6: 35-44 Go to original source...
  4. DEBACH P. & SISOJEVIC P. 1960: Some effects of temperature and competition on the distribution and relative abundance of Aphytis lingnanensis and A. chrysomphali. Ecology 41: 153-160 Go to original source...
  5. DEBACH P. & WHITE E.B. 1960: Commercial mass culture of the California red scale parasite Aphytis lignanensis. Calif. Agric. Exp. St. Bull. 770: 4-58
  6. DESNEUX N., FAUVERGUE X., DECHAUME-MONCHARMONT F.X., KERHOAS L., BALLANGER Y. & KAISER L. 2005: Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in Oilseed Rape. J. Econ. Entomol. 98: 9-17. Go to original source...
  7. DESNEUX N., DECOURTYE A. & DELPUECH J.M. 2007: The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52: 81-106 Go to original source...
  8. GRAFTON-CARDWELL E.E., LEE J.E., STEWART J.R. & OLSEN K.D. 2006: Role of two insect growth regulators in integrated pest management of citrus scales. J. Econ. Entomol. 99: 733-744 Go to original source...
  9. HARE J.D., MILLAR J.G. & LUCK R.F. 1993: A caffeic acid ester mediates host recognition by a parasitic wasp. Naturwissenschaften 80: 92-94 Go to original source...
  10. HASSELL M.P. 1980: Foraging strategies population models and biological control: a case study. J. Anim. Ecol. 49: 603-628 Go to original source...
  11. HASSELL M.P. & MAY R.M. 1974: Aggregation of predators and insect parasites and its effect on stability. J. Anim. Ecol. 43: 567-594 Go to original source...
  12. HEADS P.A. & LAWTON J.H. 1983: Studies on the natural enemy complex of the holly leafminer: the effects of scale on detection of aggregative responses and the implication for biological control. Oikos 40: 267-276 Go to original source...
  13. HEIMPEL G.E. & ASPLEN M.K. 2011: A "Goldilocks" hypothesis for dispersal of biological control agents. BioControl 56: 441-450 Go to original source...
  14. HEIMPEL G.E., ROSENHEIM J.A. & KATTARI D. 1997: Adult feeding and lifetime reproductive success in the parasitoid Aphytis melinus. Entomol. Exp. Appl. 83: 305-315 Go to original source...
  15. HOUGARDY E. & MILLS N.J. 2006: The influence of host deprivation and egg expenditure on the rate of dispersal of a parasitoid following field release. Biol. Control 37: 206-213 Go to original source...
  16. JACAS J., KARAMAOUNA F., VERCHER R. & ZAPPALA L. 2010: Citrus pest management in the Northern Mediterranean basin (Spain, Italy and Greece). In Ciancio A. & Mukerji K.G. (eds): Integrated Management of Arthropod Pests and Insect Borne Diseases. Springer, Dordrecht, pp. 3-26
  17. JAMES D.G., STEVENS M.M. & O'MALLEY K.J. 1997: The impact of foraging ants on populations of Coccus hesperidum L. (Hem., Coccidae) and Aonidiella aurantii (Maskell) (Hem., Diaspididae) in an Australian citrus grove. J. Appl. Entomol. 121: 257-259 Go to original source...
  18. KELLER M.A., LEWIS W.J. & STINNER R.E. 1985: Biological and practical significance of movement by Trichogramma species - a review. Southwest. Entomol. 8: 138-155
  19. KOLLIKER-OTT U.M., BIGLER F. & HOFFMANN A.A. 2004: Field dispersal and host location of Trichogramma brassicae is influenced by wing size but not wing shape. Biol. Control 31: 1-10 Go to original source...
  20. LANGHOF M., MEYHOFER R., POEHLING H. & GATHMANN A. 2005: Measuring the field dispersal of Aphidius colemani (Hymenoptera: Braconidae). Agr. Ecosyst. Environ. 107: 137-143 Go to original source...
  21. LAVANDERO B., WRATTEN S., HAGLER J. & JERVIS M. 2004: The need for effective marking and tracking techniques for monitoring the movements of insect predators and parasitoids. Int. J. Pest Manag. 50: 147-151 Go to original source...
  22. LESSELLS C.M. 1985: Parasitoid foraging: should parasitism be density dependent? J. Anim. Ecol. 47: 27-41 Go to original source...
  23. LIZZIO S., SISCARO G. & LONGO S. 1998: Analisi dei principali fattori di mortalitL di Aonidiella aurantii (Maskell) in agrumeti della Sicilia. Boll. Zool. Agr. Bachic. (Ser. II.) 30: 165-183
  24. LUCK R.F. & PODOLER H. 1985: Competitive-exclusion of Aphytis-lingnanensis by Aphytis-melinus - potential role of host size. Ecology 66: 904-913 Go to original source...
  25. MCCLURE M.S. 1977: Parasitism of the scale insect, Fiorinia externa (Homoptera: Diaspididae), by Aspidiophagus citrinus (Hymenoptera: Eulophidae) in a hemlock forest: density dependence. Environ. Entomol. 6: 551-555 Go to original source...
  26. MEATS A. & WHEELER S. 2010: Dispersion, contagion, and population stability of red scale, Aonidiella aurantii, in citrus orchards with low or zero insecticide use. Entomol. Exp. Appl. 138: 146-153 Go to original source...
  27. MORENO D.S., GREGORY W.A. & TANIGOSHI L.K. 1984: Flight response of Aphytis melinus (Hymenoptera: Aphelinidae) and Scirtothrips citri (Thysanoptera: Thripidae) to trap color, size and shape. Environ. Entomol. 13: 935-940 Go to original source...
  28. MORENO D.S. & LUCK R.F. 1992: Augmentative releases of Aphytis melinus (Hymenoptera: Aphelinidae) to suppress California red scale (Homoptera: Diaspididae) in Southern California lemon orchards. J. Econ. Entomol. 85: 1112-1119 Go to original source...
  29. MORGAN D.J.W. & HARE J.D. 1998: Volatile cues used by the parasitoid, Aphytis melinus, for host location: California red scale revisited. Entomol. Exp. Appl. 88: 235-245 Go to original source...
  30. MORRISON G. & STRONG D.R. 1980: Spatial variations in host density and the intensity of parasitism: some empirical examples. Environ. Entomol. 9: 149-152 Go to original source...
  31. MURDOCH W.W., REEVE J.D., HUFFAKER C.B. & KENNETT C.E. 1984: Biological control of olive scale and its relevance to ecological theory. Am. Nat. 123: 371-392 Go to original source...
  32. MURDOCH W.W., CHESSON J. & CHESSON P.L. 1985: Biological control in theory and practice. Am. Nat. 125: 344-366 Go to original source...
  33. PEKAS A., AGUILAR A., TENA A. & GARCIA-MARI F. 2010a: Influence of host size on parasitism by Aphytis chrysomphali and A. melinus (Hymenoptera: Aphelinidae) in Mediterranean populations of California red scale Aonidiella aurantii (Hemiptera: Diaspididae). Biol. Control 55: 132-140 Go to original source...
  34. PEKAS A., TENA A., AGUILAR A. & GARCIA-MARI F. 2010b: Effect of Mediterranean ants (Hymenoptera: Formicidae) on California red scale (Hemiptera: Diaspididae) populations in citrus orchards. Environ. Entomol. 39: 827-834 Go to original source...
  35. PLANES L., CATALAN J., TENA A., PORCUNA J.L., JACAS J.A., IZQUIERDO J. & URBANEJA A. 2012: Lethal and sublethal effects of spirotetramat on the mealybug destroyer, Cryptolaemus montrouzieri. J. Pest Sci. in press doi: 10.1007/s10340-012-0440-3 Go to original source...
  36. RACITI E., SARACENO F. & SISCARO G. 2003: Mass rearing of Aphytis melinus for biological control of Aonidiella aurantii in Sicily. IOBC/WPRS Bull. 25: 125-134
  37. REEVE J.D. & MURDOCH W.W. 1985: Aggregation by parasitoids in the successful control of the California red scale: a test of theory. J. Anim. Ecol. 54: 797-816 Go to original source...
  38. REEVE J.D. & MURDOCH W.W. 1986: Biological control by the parasitoid Aphytis melinus, and population stability of the California red scale. J. Anim. Ecol. 55: 1069-1082 Go to original source...
  39. ROELOFS W.L., GIESELMANN M.J., CARDE A.M., TASHIRO H., MORENO D.S., HENRICK C.A. & ANDERSON R.J. 1977: Sex pheromone of the California red scale, Aonidiella aurantii. Nature 267: 698-699 Go to original source...
  40. ROSEN D. & DEBACH P. 1979: Species of Aphytis of the World (Hymenoptera: Aphelinidae). W. Junk, The Hague, 801 pp
  41. SAMWAYS M.J. 1986: Spatial and temporal population patterns of Aonidiella aurantii (Maskell) (Hemiptera, Diaspididae) parasitoids (Hymenoptera, Aphelinidae and Encyrtidae) caught on yellow sticky traps in citrus. Bull. Entomol. Res. 76: 265-274 Go to original source...
  42. SAMWAYS M.J. 1988: Comparative monitoring of red scale Aonidiella aurantii (Mask.) (Hom., Diaspididae) and its Aphytis spp. (Hym., Aphelinidae) parasitoids. J. Appl. Entomol. 105: 483-489 Go to original source...
  43. SANCHEZ N.E., PEREYRA P.C. & LUNA M.G. 2009: Spatial patterns of parasitism of the solitary parasitoid Pseudapanteles dignus (Hymenoptera: Braconidae) on Tuta absoluta (Lepidoptera: Gelechiidae). Environ. Entomol. 38: 365-374. Go to original source...
  44. SISCARO G., LONGO S. & LIZZIO S. 1999: Ruolo degli entomofagi di Aonidiella aurantii (Maskell) (Homoptera, Diaspididae) in agrumeti siciliani. Phytophaga 9: 41-52
  45. SORRIBAS J. & GARCIA-MARI F. 2010: Comparative efficacy of different combinations of natural enemies for the biological control of California red scale in citrus groves. Biol. Control 55: 42-48 Go to original source...
  46. SORRIBAS J., RODRIGUEZ R. & GARCIA-MARI F. 2010: Parasitoid competitive displacement and coexistence in citrus agroecosystems: linking species distribution with climate. Ecol. Appl. 20: 1101-1113 Go to original source...
  47. STERNLICHT M. 1973: Parasitic wasps attracted by the sex pheromone of their coccid host. Entomophaga 18: 339-342 Go to original source...
  48. STILING P.D. 1987: The frequency of density dependence in insect host-parasitoid systems. Ecology 68: 844-856 Go to original source...
  49. STILING P.D. & STRONG D.R. 1982: Egg density and the intensity of parasitism in Prokelisia marginata (Homoptera: Delphacidae). Ecology 63: 1630-1635 Go to original source...
  50. SUMA P., ZAPPALA L., MAZZEO G. & SISCARO G. 2009: Lethal and sub-lethal effects of insecticides on natural enemies of citrus scale pests. BioControl 54: 651-661 Go to original source...
  51. SUVERKROPP B.P., BIGLER F. & VAN LENTEREN J.C. 2009: Dispersal behaviour of Trichogramma brassicae in maize fields. Bull. Insectol. 62: 113-120
  52. TABONE E., BARDON C. & DESNEUX N. 2012: Study of dispersal as a selection criterion for Trichogrammatidae for biological control in cauliflower greenhouses. Acta Hort. 927: 227-236 Go to original source...
  53. TABONE E., BARDON C., DESNEUX N. & WAJNBERG E. 2010: Parasitism of different Trichogramma species and strains on Plutella xylostella L. on greenhouse cauliflower. J. Pest Sci. 83: 251-256 Go to original source...
  54. VANACLOCHA P., VIDAL-QUIST C., OHEIX S., MONTON H., PLANES L., CATALAN J., TENA A., VERDU M.J. & URBANEJA A. 2012: Acute toxicity in laboratory tests of fresh and aged residues of pesticides used in citrus on the parasitoid Aphytis melinus. J. Pest Sci. in press doi: 10.1007/s10340-012-0448-8 Go to original source...
  55. VAN VEEN F.J., MULLER C.B., ADRIAANSE I.C. & GODFRAY H.C. 2002: Spatial heterogeneity in risk of secondary parasitism in a natural population of an aphid parasitoid. J. Anim. Ecol. 71: 463-469 Go to original source...
  56. VASQUEZ C.J. & MORSE J.G. 2012: Fitness components of Aphytis melinus (Hymenoptera: Aphelinidae) reared in five California insectaries. Environ. Entomol. 41: 51-58 Go to original source...
  57. WRIGHT M.G., HOFFMANN M.P., CHENUS S.A. & GARDNER J. 2001: Dispersal behavior of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) in sweet corn field: inplications for augmentative releases against Ostrinia nubilalis (Lepidoptera: Crambidae). Biol. Control 22: 29-37 Go to original source...
  58. YU D.S. & LUCK R.F. 1988: Temperature-dependent size and development of California red scale (Homoptera: Diaspididae) and its effect on host availability for the ectoparasitoid, Aphytis melinus DeBach (Hymenoptera: Aphelinidae). Environ. Entomol. 17: 154-161 Go to original source...
  59. YU H., ZHANG Y., WU K.M., WYCKHUYS K.A.G. & GUO Y. 2009: Flight potential of Microplitis mediator, a parasitoid of various lepidopteran pests. BioControl 54: 183-193 Go to original source...
  60. ZAPPALA L., CAMPOLO O., SARACENO F., GRANDE S.B., RACITI E., SISCARO G. & PALMERI V. 2008: Augmentative releases of Aphytis melinus (Hymenoptera: Aphelinidae) to control Aonidiella aurantii (Hemiptera: Diaspididae) in Sicilian citrus groves. IOBC/WPRS Bull. 38: 49-54