Journal of Pest Science

, Volume 86, Issue 4, pp 635–647 | Cite as

Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies

  • Lucia Zappalà
  • Antonio Biondi
  • Alberto Alma
  • Ibrahim J. Al-Jboory
  • Judit Arnò
  • Ahmet Bayram
  • Anaïs Chailleux
  • Ashraf El-Arnaouty
  • Dan Gerling
  • Yamina Guenaoui
  • Liora Shaltiel-Harpaz
  • Gaetano Siscaro
  • Menelaos Stavrinides
  • Luciana Tavella
  • Rosa Vercher Aznar
  • Alberto Urbaneja
  • Nicolas DesneuxEmail author
Rapid Communication


The South American tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), is an invasive Neotropical pest. After its first detection in Europe, it rapidly invaded more than 30 Western Palaearctic countries becoming a serious agricultural threat to tomato production in both protected and open-field crops. Among the pest control tactics against exotic pests, biological control using indigenous natural enemies is one of the most promising. Here, available data on the Afro-Eurasian natural enemies of T. absoluta are compiled. Then, their potential for inclusion in sustainable pest control packages is discussed providing relevant examples. Collections were conducted in 12 countries, both in open-field and protected susceptible crops, as well as in wild flora and/or using infested sentinel plants. More than 70 arthropod species, 20 % predators and 80 % parasitoids, were recorded attacking the new pest so far. Among the recovered indigenous natural enemies, only few parasitoid species, namely, some eulophid and braconid wasps, and especially mirid predators, have promising potential to be included in effective and environmentally friendly management strategies for the pest in the newly invaded areas. Finally, a brief outlook of the future research and applications of indigenous T. absoluta biological control agents are provided.


Biological control Generalist predators Integrated pest management Invasive species Parasitoid community Western Palaearctic 


  1. Abbes K, Chermiti B (2012) Failure of the biological control of Tuta absoluta using the predator Nesidiocoris tenuis in a protected tomato crop: analysis of factors. IOBC/WPRS Bull 80:231–236Google Scholar
  2. Abbes K, Biondi A, Zappalà L, Chermiti B (2013) Fortuitous parasitoids of the invasive tomato leafminer Tuta absoluta in Tunisia. Phytoparasitica. doi: 10.1007/s12600-013-0341-x
  3. Al-Jboory IJ, Katbeh-Bader A, Al-Zaidi S (2012) First observation and identification of some natural enemies collected from heavily infested tomato by Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Jordan. Middle East J Sci Res 11:435–438Google Scholar
  4. Arnó 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 84:513–520CrossRefGoogle Scholar
  5. Arnó J, Sorribas R, Prat M, Matas M, Pozo C, Rodríguez D, Garreta A, Gómez A, Gabarra R (2009) Tuta absoluta, a new pest in IPM tomatoes in the northeast of Spain. IOBC/WPRS Bull 49:203–208Google Scholar
  6. Arnó J, Castañé C, Riudavets J, Gabarra R (2010) Risk of damage to tomato crops by the generalist zoophytophagous predator Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae). Bull Entomol Res 100:105–115PubMedCrossRefGoogle Scholar
  7. Balzan MV, Wäckers FL (2013) Flowers to selectively enhance the fitness of a host-feeding parasitoid: adult feeding by Tuta absoluta and its parasitoid Necremnus artynes. Biol Control 67:21–31CrossRefGoogle Scholar
  8. Baniameri V, Cheraghian A (2012) The first report and control strategies of Tuta absoluta in Iran. EPPO Bull 42:322–324CrossRefGoogle Scholar
  9. Bernardo U, Pedata PA, Viggiani G (2006) Life history of Pnigalio soemius (Walker) (Hymenoptera: Eulophidae) and its impact on a leafminer host through parasitization, destructive host-feeding and host-stinging behavior. Biol Control 37:98–107CrossRefGoogle Scholar
  10. Biondi A, Desneux N, Siscaro G, Zappalà L (2012) 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 87:803–812PubMedCrossRefGoogle Scholar
  11. Biondi A, Zappalà L, Stark JD, Desneux N (2013a) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8(9):e76548. doi: 10.1371/journal.pone.0076548 (in press)
  12. Biondi A, Chailleux A, Lambion J, Zappalà L, Desneux N (2013b) Indigenous natural enemies attacking Tuta absoluta (Lepidoptera: Gelechiidae) in Southern France. Egypt J Biol Pest Control 23:117–121Google Scholar
  13. Biondi A, Desneux N, Amiens-Desneux E, Siscaro G, Zappalà L (2013c) Biology and developmental strategies of the Palaearctic parasitoid Bracon nigricans on the Neotropical moth Tuta absoluta. J Econ Entomol 106:1638–1647PubMedCrossRefGoogle Scholar
  14. Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55:433–440CrossRefGoogle Scholar
  15. Boualem M, Allaoui H, Hamadi R, Medjahed M (2012) Biologie et complexe des ennemis naturels de Tuta absoluta à Mostaganem (Algérie). EPPO Bull 42:268–274CrossRefGoogle Scholar
  16. Cabello T, Gallego JR, Fernandez-Maldonado FJ, Soler A, Beltran D, Parra A, Vila E (2009) The damsel bug Nabis pseudoferus (Hem.: Nabidae) as a new biological control agent of the South American Tomato Pinworm, Tuta absoluta (Lep.: Gelechiidae), in tomato crops of Spain. IOBC/WPRS Bull 49:219–223Google Scholar
  17. Cabello T, Gallego JR, Fernandez FJ, Gamez M, Vila E, Del Pino M, Hernandez E (2012) Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes. J Econ Entomol 105:2085–2096PubMedCrossRefGoogle Scholar
  18. Cagnotti CL, Viscarret MM, Riquelme MB, Botto EN, Carabajal LZ, Segura DF, López SN (2012) Effects of X-rays on Tuta absoluta for use in inherited sterility programmes. J Pest Sci 85:413–421CrossRefGoogle Scholar
  19. Calvo J, Blockmans K, Stansly PA, Urbaneja A (2009) Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato. Biocontrol 54:237–246CrossRefGoogle Scholar
  20. 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 143:111–119CrossRefGoogle Scholar
  21. Canale A, Benelli G (2012) Impact of mass-rearing on the host seeking behaviour and parasitism by the fruit fly parasitoid Psyttalia concolor (Szepligeti) (Hymenoptera: Braconidae). J Pest Sci 85:65–74CrossRefGoogle Scholar
  22. Caparros Megido R, Haubruge E, Verheggen FG (2012) First evidence of deuterotokous parthenogenesis in the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci 85:409–412CrossRefGoogle Scholar
  23. Castañé C, Arnó J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29CrossRefGoogle Scholar
  24. Castañé C, Agustí N, Arnó J, Gabarra R, Riudavets J, Comas J, Alomar O (2013) Taxonomic identification of Macrolophus pygmaeus and Macrolophus melanotoma based on morphometry and molecular markers. Bull Entomol Res 103:204–215PubMedCrossRefGoogle Scholar
  25. Chailleux A, Desneux N, Seguret N, Do Thi Khanh H, Maignet P, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7:e48068. doi: 10.1371/journal.pone.0048068 PubMedCrossRefGoogle Scholar
  26. Chailleux A, Biondi A, Han P, Tabone E, Desneux N (2013a) Suitability of the pest-plant system Tuta absoluta (Lepidoptera: Gelechiidae)-tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. J Econ Entomol. doi: 10.1603/EC13092
  27. Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013b) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest, Tuta absoluta. J Pest Sci 86:533–541CrossRefGoogle Scholar
  28. Cicero L, Sivinski J, Aluja M (2012) Effect of host diet and adult parasitoid diet on egg load dynamics and egg size of braconid parasitoids attacking Anastrepha ludens. Physiol Entomol 37:177–184CrossRefGoogle Scholar
  29. Cocco A, Deliperi S, Delrio G (2013) Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. J Appl Entomol 137:16–28CrossRefGoogle Scholar
  30. Cornell HV, Hawkıns BA (1993) Accumulation of native parasitoid species on introduced herbivores: a comparison of hosts as natives and hosts as invaders. Am Nat 141:847–865PubMedCrossRefGoogle Scholar
  31. Delvare G, Lacordaire AI, Ramel JM (2011) Necremnus artynes (Walker, 1839) (Eulophidae), a potential beneficial for the biological control of Tuta absoluta (Meyrick). EPPO/IOBC/NEPPO joint international symposium on management of Tuta absoluta (Tomato Borer), 16–18 November 2011, Agadir, Morocco. Book of abstract:73Google Scholar
  32. 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 98:631–639PubMedCrossRefGoogle Scholar
  33. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106PubMedCrossRefGoogle Scholar
  34. Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009a) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160:387–398PubMedCrossRefGoogle Scholar
  35. Desneux N, Stary P, Delebecque CJ, Gariepy TD, Barta RJ, Hoelmer KA, Heımpel GE (2009b) Cryptic species of parasitoids attacking the Soybean Aphid (Hemiptera: Aphididae) in Asia: Binodoxys communis and Binodoxys koreanus (Hymenoptera: Braconidae: Aphidiinae). Ann Entomol Soc Am 102:925–936CrossRefGoogle Scholar
  36. Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narvaez-Vasquez CA, Gonzalez-Cabrera J, Catalan 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 83:197–215CrossRefGoogle Scholar
  37. Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) 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 84:403–408CrossRefGoogle Scholar
  38. Desneux N, Blahnik R, Delebecque CJ, Heimpel GE (2012) Host phylogeny and specialisation in parasitoids. Ecol Lett 15:453–460PubMedCrossRefGoogle Scholar
  39. Doğanlar M, Yiğit A (2011) Parasitoid complex of the Tomato Leaf Miner, Tuta absoluta (Meyrick 1917), (Lepidoptera: Gelechiidae) in Hatay, Turkey. KSÜ Doğa Bil Derg 14:28–37Google Scholar
  40. El-Arnaouty A, Kortam MN (2012) First record of the Mired predatory species, Nesidiocoris tenuis Reuter (Heteroptera: Miridae) on the Tomato Leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt. Egypt J Biol Pest Control 22:223–224Google Scholar
  41. Ferracini C, Ingegno BL, Navone P, Ferrari E, Mosti M, Tavella L, Alma A (2012a) Adaptation of indigenous larval parasitoids to Tuta absoluta (Lepideoptera: Gelechiidae) in Italy. J Econ Entomol 105:1311–1319PubMedCrossRefGoogle Scholar
  42. Ferracini C, Ingegno BL, Mosti M, Navone P, Tavella L, Alma A (2012b) Promising native candidates for biological control of Tuta absoluta in Italy. IOBC/WPRS Bull 80:51–55Google Scholar
  43. Gabarra R, Arnó J (2010) Resultados de las experiencias de control biológico de la polilla del tomate en cultivo de invernadero y aire libre en Cataluña. Phytoma-España 217:66–68Google Scholar
  44. Gabarra R, Arnó J, Lara L, Verdú MJ, Ribes A, Beitia F, Urbaneja A, Téllez MM, Mollá O, Riudavets J (2013) Native parasitoids associated with Tuta absoluta in the tomato production areas of the Spanish Mediterranean Coast. Biocontrol. doi: 10.1007/s10526-013-9545-8 (in press)
  45. Gardiner MM, Landis DA, Gratton C, Di Fonzo CD, O’Neal M, Chacon JM, Wayo MT, Schmidt MP, Mueller EE, Heimpel GE (2009) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol Appl 19:143–154PubMedCrossRefGoogle Scholar
  46. Gontijo LM, Nechols JR, Margolies DC, Cloyd RA (2012) Plant architecture and prey distribution influence foraging behavior of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). Exp Appl Acarol 56:23–32PubMedCrossRefGoogle Scholar
  47. Gontijo PC, Picanço MC, Pereira EJG, Martins JC, Chediak M, Guedes RNC (2013) Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann Appl Biol 152:50–59CrossRefGoogle Scholar
  48. Gordh G, Bearsley JH (1999) Taxonomy and biological control. In: Bellows TS, Fischer TW (eds) Handbook of biological control. Academic Press, San Diego, pp 45–56CrossRefGoogle Scholar
  49. Grabenweger G, Kehrli P, Zweımüller I, Augustın S, Avtzıs N, Bacher S, Freıse J, Girardoz S, Guıchard S, Heitland W, Lethmayer C, Stolz M, Tomov R, Volter L, Kenis M (2010) Temporal and spatial variations in the parasitoid complex of the horse chestnut leafminer during its invasion of Europe. Biol Invasion 12:2797–2813CrossRefGoogle Scholar
  50. Guedes RNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42:211–216CrossRefGoogle Scholar
  51. Guenaoui Y, Bensaad R, Ouezzani K (2011a) Importance of native polyphagous predators able to prey on Tuta absoluta Meyrick (Lep: Gelechiidae) on tomato crops. EPPO/IOBC/FAO/NEPPO joint international symposium on management of Tuta absoluta, 16–18 November 2011, Agadir-Marocco. Book of abstract, 38Google Scholar
  52. Guenaoui Y, Bensaad R, Ouezzani K, Vercher R (2011b) Emerging opportunities to use native entomophagous against Tuta absoluta Meyrick (Lepidoptera: Gelechidae) infesting tomato in unheated greenhouse in Northwestern Algeria. Between benefits and risks. 9eme Conference Internationale sur les Ravageurs en Agriculture, SupAgro, Montpellier, France, 25–27 October 2011:324–334Google Scholar
  53. Haddi K, Berger M, Bielza P, Cifuentes D, Field LM, Gorman K, Rapisarda C, Williamson MS, Bass C (2012) Identification of mutations associated with pyrethroid resistance in the voltage-gated sodium channel of the tomato leaf miner (Tuta absoluta). Insect Biochem Mol Biol 42:506–513PubMedCrossRefGoogle Scholar
  54. Harwood JD, Desneux N, Yoo HJS, Rowley DL, Greenstone MH, Obrycki JJ, O’Neil RJ (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol Ecol 16:4390–4400PubMedCrossRefGoogle Scholar
  55. Heimpel GE, Antolin MF, Franqui RA, Strand MR (1997) Reproductive isolation and genetic variation between two “strains” of Bracon hebetor (Hymenoptera: Braconidae). Biol Control 9:149–156CrossRefGoogle Scholar
  56. Hokkanen H, Pimentel D (1984) New approach for selecting biological-control agents. Can Entomol 116:1109–1121CrossRefGoogle Scholar
  57. Ingegno BL, Goula M, Navone P, Tavella L (2008) Distribution and host plants of the genus Dicyphus in the Alpine valleys of NW Italy. Bull Insectol 61:139–140Google Scholar
  58. Ingegno BL, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control 58:174–181CrossRefGoogle Scholar
  59. Ingegno BL, Ferracini C, Gallinotti D, Alma A, Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biol Control 67:246–252CrossRefGoogle Scholar
  60. Juen A, Hogendoorn K, Ma G, Schmidt O, Keller M (2012) Analysing the diets of invertebrate predators using terminal restriction fragments. J Pest Sci 85:89–100CrossRefGoogle Scholar
  61. Karabuyuk F (2011) Determination of tomato leafminer [Tuta absoluta (Meyrick)] host, population development with parasitoid and predators in the vegetable fields of the Eastern Meditterranean. MSc Thesis, Natural and Applied Sciences Institute of Cukurova University, Adana-Turkey, (in Turkish with English abstract)Google Scholar
  62. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  63. Kerzhner IM, Josifov M (1999) Cimicomorpha II Miridae. In: Aukema B, Rieger C (eds) Catalogue of the Heteroptera of the Palaearctic region, vol 3. The Netherlands Entomological Society, Amsterdam, pp 1–577Google Scholar
  64. King RA, Read DS, Traugott M, Symondson WOC (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol Ecol 17:947–963PubMedCrossRefGoogle Scholar
  65. Kolai N, Cherifa A, Berkani A, Saiah F, Badaoui M (2011) Observations on the biology of Necremnus artynes; new parasitoids of Tuta absoluta in Mostaganem (Algeria). EPPO/IOBC/NEPPO joint international symposium on management of Tuta absoluta (Tomato Borer), 16–18 November 2011, Agadir, MoroccoGoogle Scholar
  66. Lambert L, Chouffot T, Tureotte G, Lemieux M, Moreau J (2005) Biological control of greenhouse whitefly (Trialeurodes vaporariorum) on interplanted tomato crops with and without supplemental lighting using Dicyphus hesperus (Quebec, Canada). IOBC/WPRS Bull 28:175–178Google Scholar
  67. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201PubMedCrossRefGoogle Scholar
  68. Lara L, Aguilar R, Salvador E, Téllez MM (2010) Estudios de control biológico de la polilla del tomate Tuta absoluta Meyrick (Lepidoptera: Gelichiidae) en cultivos hortícolas de invernadero del Sureste Español. Phytoma España 221:39Google Scholar
  69. Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 35:387–408CrossRefGoogle Scholar
  70. Loni A, Rossi E, Van Achterberg C (2011) First report of Agathis fuscipennis in Europe as parasitoid of the tomato leafminer Tuta absoluta. Bull Insectol 64:115–117Google Scholar
  71. Luna MG, Wada VI, La Salle J, Sánchez NE (2011) Neochrysocharis formosa (Westwood) (Hymenoptera: Eulophidae), a newly recorded parasitoid of the Tomato Moth, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), in Argentina. Neotrop Entomol 40:412–414PubMedCrossRefGoogle Scholar
  72. Luna MG, Sanchez NE, Pereyra PC, Nieves E, Savino V, Luft E, Virla E, Speranza S (2012) Biological control of Tuta absoluta in Argentina and Italy: evaluation of indigenous insects as natural enemies. EPPO Bull 42:260–267CrossRefGoogle Scholar
  73. Madadi H, Parizi EM, Allahyari H, Enkegaard A (2011) Assessment of the biological control capability of Hippodamia variegata (Col.: Coccinellidae) using functional response experiments. J Pest Sci 84:447–455CrossRefGoogle Scholar
  74. Martinez-Cascales JI, Cenis JL, Cassis G, Sanchez JA (2006) Species identity of Macrolophus melanotoma (Costa 1853) and Macrolophus pygmaeus (Rambur 1839) (Insecta: Heteroptera: Miridae) based on morphological and molecular data and bionomic implications. Insect Syst Evol 37:385–404CrossRefGoogle Scholar
  75. Mollá O, Monton H, Beitia Crespo FJ, Urbaneja A (2008) La polilla del tomate Tuta absoluta (Meyrick), una nueva plaga invasora. Terralia 69:36–42Google Scholar
  76. Mollá O, Alonso M, Monton H, Beitia F, Verdù MJ, Gonzàlez-Cabrera J, Urbaneja A (2010) Control Biologico de Tuta absoluta. Catalogacion de enemigos naturales y potencial de los mıridos depredadores como agentes de control. Phytoma Spain 217:42–46Google Scholar
  77. Mollá O, González-Cabrera J, Urbaneja A (2011) The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. Biocontrol 56:883–891CrossRefGoogle Scholar
  78. Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. Biocontrol (under revision)Google Scholar
  79. Nannini M, Atzori F, Murgia G, Pisci R, Sanna F (2012) Use of predatory mirids for control of the tomato borer Tuta absoluta (Meyrick) in Sardinian greenhouse tomatoes. EPPO Bull 42:255–259CrossRefGoogle Scholar
  80. Noyes JS (2013) Universal Chalcidoidea Database. World Wide Web electronic publication.
  81. O’Connell DM, Wratten SD, Pugh AR, Barnes AM (2012) ‘New species association’ biological control? Two coccinellid species and an invasive psyllid pest in New Zealand. Biol Control 62:86–92CrossRefGoogle Scholar
  82. Parolin P, Bresch C, Poncet C, Desneux N (2012a) Functional characteristics of secondary plants for increased pest management. Int J Pest Manag 58:369–377CrossRefGoogle Scholar
  83. Parolin P, Bresch C, Desneux N, Brun R, Bout A, Boll R, Poncet C (2012b) Secondary plants used in biological control: a review. Int J Pest Manag 58:91–100CrossRefGoogle Scholar
  84. Parra JRP, Zucchi RA (2004) Trichogramma in Brazil: feasibility of use after 20 years of research. Neotrop Entomol 33(3):271–281CrossRefGoogle Scholar
  85. Perdikis D, Favas C, Lykouressis D, Fantinou A (2007) Ecological relationships between non-cultivated plants and insect predators in agroecosystems: the case of Dittrichia viscosa (Asteraceae) and Macrolophus melanotoma (Hemiptera: Miridae). Acta Oecol 31:299–306CrossRefGoogle Scholar
  86. Perdikis D, Fantinou A, Lykouressis D (2011) Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biol Control 59:13–21CrossRefGoogle Scholar
  87. Ramirez-Romero R, Sivinski J, Copeland CS, Aluja M (2012) Are individuals from thelytokous and arrhenotokous populations equally adept as biocontrol agents? Orientation and host searching behavior of a fruit fly parasitoid. Biocontrol 57:427–440CrossRefGoogle Scholar
  88. Riciputi C (2011) Pomodoro, contro la Tuta tre nuovi predatori naturali. Colture Protette 40:32–34Google Scholar
  89. Rizzo MC, Margiotta V, Caleca V (2011) Necremnus artynes parassitoide di Tuta absoluta su pomodoro, melanzana e Solanum nigrum in serra a conduzione biologica. Atti XXIII Congr Naz Ital Entomol, 13–16 June 2011, Genova, ItalyGoogle Scholar
  90. Savino V, Coviella CE, Luna MG (2012) Reproductive biology and functional response of Dineulophus phtorimaeae, a natural enemy of the tomato moth, Tuta absoluta. J Insect Sci 12:153CrossRefGoogle Scholar
  91. Stacey DL (1977) Banker plant production of Encarsia formosa Gahan and its use in control of glasshouse whitefly on tomatoes. Plant Pathol 26:63–66CrossRefGoogle Scholar
  92. Stouthamer R (2008) Molecular tools. In: van Driesche R, Hoddle M, Center T (eds) Control of pests and weeds by natural enemies: an introduction to biological control, Blackwell Publishing, Oxford, pp 167–180Google Scholar
  93. Tabone E, Bardon C, Desneux N (2012) Study of dispersal as a selection criterion for Trichogrammatidae for biological control in cauliflower greenhouses. Acta Hortic 927:227–235Google Scholar
  94. Tena A, Pekas A, Wäckers K, Urbaneja A (2013) Energy reserves of parasitoids depend on honeydew from non-hosts. Ecol Entomol 38:278–289CrossRefGoogle Scholar
  95. Tropea Garzia G, Siscaro G, Biondi A, Zappalà L (2012) Tuta absoluta, an exotic invasive pest from South America now in the EPPO region: biology, distribution and damage. EPPO Bull 42:205–210CrossRefGoogle Scholar
  96. Trottin-Caudal Y, Baffert V, Leyre JM, Hulas H (2012) Experimental studies on Tuta absoluta (Meyrick) in protected tomato crops in France: biological control and integrated crop protection. EPPO Bull 42:234–240CrossRefGoogle Scholar
  97. Urbaneja A, Montón H, Mollá O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus caliginosus and Nesidiocoris tenuis. J Appl Entomol 133:292–296CrossRefGoogle Scholar
  98. Urbaneja A, González-Cabrera J, Arnó J, Gabarra R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68:1215–1222PubMedCrossRefGoogle Scholar
  99. Xiao Y, Chen J, Cantliffe D, Mckenzie C, Houben K, Osborne LS (2011) Establishment of papaya banker plant system for parasitoid, Encarsia sophia (Hymenoptera: Aphelinidae) against Bemisia tabaci (Hemiptera: Aleyrodidae) in greenhouse tomato production. Biol Control 58:239–247CrossRefGoogle Scholar
  100. Yu DSK, Van Actherberg C (2010) Taxapad Ichneumonoidea (May 2009 Version). In: Bisby FA, Roskov YR, Orrell TM, Nicolson D, Paglinawan LE, Bailly N, Kirk PM, Bourgoin T, Baillargeon G (eds) Species 2000 & Itis catalogue of life: 2010 annual checklist. Dvd, Species 2000, Reading, UKGoogle Scholar
  101. Zappalà L, Bernardo U, Biondi A, Cocco A, Deliperi S, Delrio G, Giorgini M, Pedata PC, Rapisarda C, Tropea Garzia G, Siscaro G (2012a) Recruitment of native parasitoids by the exotic pest Tuta absoluta (Meyrick) in Southern Italy. Bull Insectol 65:51–61Google Scholar
  102. Zappalà L, Siscaro G, Biondi A, Mollà O, Gonzàlez-Cabrera J, Urbaneja A (2012b) Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J Appl Entomol 136:401–409CrossRefGoogle Scholar
  103. Zappalà L, Campolo O, Grande S, Saraceno F, Biondi A, Siscaro G, Palmeri V (2012c) Dispersal of Aphytis melinus (Hymenoptera: Aphelinidae) after augmentative releases in citrus orchards. Eur J Entomol 109:561–568Google Scholar
  104. Zouba A, Chermiti B, Kadri K, Fattouch S (2013) Molecular characterization of Trichogramma bourarachae strains (Hymenoptera: Trichogrammatidae) from open field tomato crops in the South West of Tunisia. Biomirror 4:13–19. Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Lucia Zappalà
    • 1
  • Antonio Biondi
    • 1
    • 2
  • Alberto Alma
    • 3
  • Ibrahim J. Al-Jboory
    • 4
  • Judit Arnò
    • 5
  • Ahmet Bayram
    • 6
  • Anaïs Chailleux
    • 2
  • Ashraf El-Arnaouty
    • 7
  • Dan Gerling
    • 8
  • Yamina Guenaoui
    • 9
  • Liora Shaltiel-Harpaz
    • 10
  • Gaetano Siscaro
    • 1
  • Menelaos Stavrinides
    • 11
  • Luciana Tavella
    • 3
  • Rosa Vercher Aznar
    • 12
  • Alberto Urbaneja
    • 13
  • Nicolas Desneux
    • 2
    Email author
  1. 1.Department of Agri-food and Environmental Systems ManagementUniversity of CataniaCataniaItaly
  2. 2.French National Institute for Agricultural Research (INRA)Sophia-AntipolisFrance
  3. 3.Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA)University of TorinoGrugliascoItaly
  4. 4.Department of Plant ProtectionsUniversity of BaghdadAbu GhraibIraq
  5. 5.Department of EntomologyIRTACabrilsSpain
  6. 6.Plant Protection Department, Agriculture FacultyDicle UniversityDiyarbakirTurkey
  7. 7.Department of Economic Entomology and PesticidesCairo UniversityGizaEgypt
  8. 8.Department of ZoologyTel Aviv UniversityTel AvivIsrael
  9. 9.Department of AgronomyUniversity Ibn Badis of MostaganemMostaganemAlgeria
  10. 10.Northern R&DMigal–Galilee Research InstituteKiryat ShmonaIsrael
  11. 11.Department of Agricultural Sciences, Biotechnology and Food ScienceCyprus University of TechnologyLimassolCyprus
  12. 12.Instituto Agroforestal del Mediterráneo (IAM)Universitat Politècnica de ValènciaValenciaSpain
  13. 13.Departamento de Entomología, Centro de Protección VegetalInstituto Valenciano de Investigaciones Agrarias (IVIA)MoncadaSpain

Personalised recommendations