Biology and developmental strategies of the palaearctic parasitoid bracon nigricans (Hymenoptera: Braconidae) on the neotropical moth tuta absoluta (Lepidoptera: Gelechiidae)

Journal of Economic Entomology

Volumn 106, Issue 4, 2013, Pages 1638-1647

  Biondi, Antonio ^a,b   Desneux, Nicolas ^b   Amiens Desneux, Edwige ^b   Siscaro, Gaetano ^a   Zappalà, Lucia ^a  

^a UNIVERSITY OF CATANIA   (Italy)

^b Institut Sophia Agrobiotech   (France)

Author keywords

biological control; host feeding; integrated pest management; life table; parasitoid behavior

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL CONTROL AGENT; EGG LAYING; FEMALE; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; HYMENOPTERA; INTRODUCED SPECIES; ITALY; LARVA; MALE; MOTH; OOCYTE; PARASITOLOGY; PHYSIOLOGY; POPULATION DYNAMICS; TOMATO;

ANIMALS; BIOLOGICAL CONTROL AGENTS; FEMALE; HOST-PARASITE INTERACTIONS; HYMENOPTERA; INTRODUCED SPECIES; ITALY; LARVA; LYCOPERSICON ESCULENTUM; MALE; MOTHS; OVIPOSITION; OVUM; POPULATION DYNAMICS;

EID: 84881647628     PISSN: 00220493     EISSN: None     Source Type: Journal    
DOI: 10.1603/EC12518     Document Type: Article

References (69)

1. Al-Jboory, I. J., A. Katbeh-Bader, and S. Al-Zaidi. 2012. First observation and identifcation of some natural enemies collected from heavily infested tomato by Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Jordan. Middle East J. Sci. Res. 11: 435-438.
2. Andrade, G. S., D. Pratissoli, L. P. Dalvi, N. Desneux, and H. J. Goncalves. 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.
3. Arno, J., and R. Gabarra. 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.
4. Bernardo, U., P. A. Pedata, and G. Viggiani. 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: 98-107. (Pubitemid 43340351)
5. Beltra A., A. Tena, and A. Soto. 2013. Reproductive strategies and food sources used by Acerophagus n. sp. near coccois, a new successful parasitoid of the invasive mealybug Phenacoccus peruvianus. J. Pest Sci. 86: 253-259.
6. Biondi, A., N. Desneux, G. Siscaro, and L. Zappala. 2012a. Using organic-certifed 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.
7. Biondi, A., V. Mommaerts, G. Smagghe, E. Vinuela, L. Zappala, and N. Desneux. 2012b. The non-target impact of spinosyns on benefcial arthropods. Pest Manag. Sci. 68: 1523-1536.
8. Birch, L. C. 1948. The intrinsic rate of natural increase of an insect populaton. J. Anim. Ecol. 17: 15-26.
9. Bompard, A., C. C. Jaworski, P. Bearez, and N. Desneux. 2013. Sharing a predator: can an invasive alien pest affect the predation on a local pest? Pop. Ecol. 55: 433-440.
10. Cabello, T., J. R. Gallego, F. J. Fernandez, M. Gamez, E. Vila, M. Del Pino, and E. Hernandez. 2012. Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes. J. Econ. Entomol. 105: 2085-2096.
11. Cagnotti, C. L., M. M. Viscarret, M. B. Riquelme, E. N. Botto, L. Z. Carabajal, D. F. Segura, and S. N. Lopez. 2012. Effects of X-rays on Tuta absoluta for use in inherited sterility programmes. J. Pest Sci. 85: 413-421.
12. Caparros Megido, R., E. Haubruge, and F. J. Verheggen. 2012. First evidence of deuterotokous parthenogenesis in the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J. Pest Sci. 85: 409-412.
13. Chailleux, A., N. Desneux, J. Seguret, H. Do Thi Khanh, P. Maignet, and E. Tabone. 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).
14. Chailleux, A, P. Bearez, J. Pizzol, E. Amiens-Desneux, R. Ramirez-Romero, and N. Desneux. 2013. Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest, Tuta absoluta. J. Pest Sci. (in press). (doi:10.1007/s10340-013- 0498-6).
15. Cocco, A., S. Deliperi, and G. Delrio. 2012. Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. J. Appl. Entomol. 137: 16-28.
16. Daane, K. M., X. Wang, S. S. Duerr, E. J. Kuhn, Y. Son, and G. Y. Yokota. 2013. Biology of Habrobracon gelechiae (Hymenoptera: Braconidae), as a parasitoid of the Obliquebanded leafroller (Lepidoptera: Tortricidae). Environ. Entomol. 42: 107-115.
17. Desneux, N., X. Fauvergue, F. X. Dechaume-Moncharmont, L. Kerhoas, Y. Ballanger, and L. Kaiser. 2005. Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J. Econ. Entomol. 98: 9-17. (Pubitemid 40328459)
18. Desneux, N., A. Decourtye, and J. M. Delpuech. 2007. The sublethal effects of pesticides on benefcial arthropods. Annu. Rev. Entomol. 52: 81-106. (Pubitemid 46133563)
19. Desneux, N., R. J. Barta, K. A. Hoelmer, K. R. Hopper, and G. E. Heimpel. 2009. Multifaceted determinants of host specifcity in an aphid parasitoid. Oecologia 160: 387-398.
20. Desneux, N., E. Wajinberg, K.A.G. Wyckhuys, G. Burgio, S. Arpaia, C. A. Narvaez-Vasquez, J. Gonzalez-Cabrera, D. Catalan Ruescas, E. Tabone, J. Frandon, et al. 2010. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J. Pest Sci. 83: 197-215.
21. Desneux, N., M. G. Luna, T. Guillemaud, and A. Urbaneja. 2011. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond. J. Pest Sci. 84: 403-408.
22. Desneux, N., R. Blahnik, C. J. Delebecque, and G. E. Heimpel. 2012. Host phylogeny and specialisation in parasitoids. Ecol. Lett. 15: 453-460.
23. Eliopoulos, P. A., and G. J. Stathas. 2008. Life Tables of Habrobracon hebetor (Hymenoptera: Braconidae) parasitizing Anagasta kuehniella and Plodia interpunctella (Lepidoptera: Pyralidae): effect of host density. J. Econ. Entomol. 101: 982-988. (Pubitemid 351955964)
24. Ferracini, C., B. L. Ingegno, P. Navone, E. Ferrari, M. Mosti, L. Tavella, and A. Alma. 2012. Adaptation of indigenous larval parasitoids to Tuta absoluta (Lepidoptera: Gelechiidae) in Italy. J. Econ. Entomol. 105: 1311-1319.
25. Fuester, R. W., K. S. Swan, K. Dunning, P. B. Taylor, and G. Ramaseshiah. 2003. Male-biased sex ratios in Glyptapanteles flavicoxis (Hymenoptera: Braconidae), a parasitoid of the gypsy moth (Lepidoptera: Lymantriidae). Ann. Entomol. Soc. Am. 96: 553-559. (Pubitemid 37348041)
26. Gauld I., and B. Bolton. 1988. The hymenoptera. Oxford University Press, Oxford, United Kingdom.
27. Ghimire, M. N., and T. W. Phillips. 2010. Suitability of different lepidopteran host species for development of Bracon hebetor (Hymenoptera: Braconidae). Environ. Entomol. 39: 449-458.
28. Godfray, H. C. 1994. Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Princeton, NJ.
29. Gontijo, P. C., M. C. Picanco, E.J.G. Pereira, J. C. Martins, M. Chediak, and R.N.C. Guedes. 2013. Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann. Appl. Biol. 152: 50-59.
30. Hardy, I.C.W. 1992. Non-binomial sex allocation and brood sex-ratio variances in the parasitoid Hymenoptera. Oikos 65: 143-158. (Pubitemid 23396739)
31. Hardy, I.C.W., N. T. Griffiths, and H. C. Godfray. 1992. Clutch size in a parasitoid wasp: a manipulation experiment. J. Anim. Ecol. 61: 121-129.
32. Heimpel, G. E., and T. R. Collier. 1996. The evolution of host-feeding behaviour in insect parasitoids. Biol. Rev. 71: 373-400. (Pubitemid 26283770)
33. Heimpel, G. E., and J. G. de Boer. 2008. Sex determination in the Hymenoptera. Annu. Rev. Entomol. 53: 209-30. (Pubitemid 351341939)
34. Heimpel, G. E., M. F. Antolin, R. A. Franqui, and M. R. Strand. 1997. Reproductive isolation and genetic variation between two "strains" of Bracon hebetor (Hymenoptera: Braconidae). Biol. Control 9: 149-156. (Pubitemid 27275335)
35. Heimpel, G. E., M. F. Antolin, and M. R. Strand. 1999. Diversity of sex-determining alleles in Bracon hebetor. Heredity 82: 282-291. (Pubitemid 29198510)
36. Jervis, M. A., and N.A.C. Kidd. 1986. Host-feeding strategies in hymenopteran parasitoids. Biol. Rev. 61: 395-434.
37. Jervis, M. A., B. A. Hawkins, and N.A.C. Kidd. 1996. The usefulness of destructive host feeding parasitoids in classical biological control: theory and observation conflict. Ecol. Entomol. 21: 41-46.
38. Jervis, M. A., J. Ellers, and J. A. Harvey. 2008. Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 53: 361-385. (Pubitemid 351341946)
39. Landis, D. A., S. D. Wratten, and G. M. Gurr. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45: 175-201. (Pubitemid 30187859)
40. Loni, A., E. Rossi, and K. van Achterberg. 2011. First report of Agathis fuscipennis in Europe as parasitoid of the tomato leafminer Tuta absoluta. Bull. Insectol. 64: 115-117.
41. Luna, M. G., N. E. Sanchez, and P. C. Pereyra. 2007. Parasitism of Tuta absoluta (Lepidoptera, Gelechiidae) by Pseudapanteles dignus (Hymenoptera, Braconidae) under laboratory conditions. Environ. Entomol. 36: 887-893. (Pubitemid 47311038)
42. Lu, Y. H., K. M. Wu, Y. Y. Jiang, Y. Y. Guo, and N. Desneux. 2012. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487: 362-365.
43. Meyer, J. S., C. G. Ingersoll, L. L. McDonald, and M. S. Boyce. 1986. Estimating uncertainty in population growth rates: Jackknife vs. Bootstrap techniques. Ecology 67: 1156-1166.
44. Molla, O., J. Gonzalez-Cabrera, and A. Urbaneja. 2011. The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. BioControl 56: 883-891.
45. Olson, L. J. 2006. The economics of terrestrial invasive species: a review of the literature. Agric. Resour. Econ. Rev. 35 178-194. (Pubitemid 43844471)
46. Papaj, D. R. 2000. Ovarian dynamics and host use. Annu. Rev. Entomol. 45: 423-448. (Pubitemid 30187868)
47. Pennacchio, F., and M. R. Strand. 2006. Evolution of developmental strategies in parasitic Hymenoptera. Annu. Rev. Entomol. 51: 233-258. (Pubitemid 43107822)
48. Pereyra, P. C., and N. E. Sanchez. 2006. Effect of two solanaceous plants on developmental and population parameters of the Tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop. Entomol. 35: 671-676. (Pubitemid 44954083)
49. Pizzol, J., N. Desneux, E. Wajnberg, and D. Thiery. 2012. Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J. Pest Sci. 85: 489-496.
50. Price, P.W. 1975. Reproductive strategies of parasitoids, pp. 87-111. In P. W. Price (ed.), Evolutionary Strategies of Parasitoids Plenum, New York, NY.
51. Ragsdale, D. W., D. A. Landis, J. Brodeur, G. E. Heimpel, and N. Desneux. 2011. Ecology and management of the soybean aphid in North America. Annu. Rev. Entomol. 56: 375-99.
52. Sanchez, N. E., P. C. Pereyra, and M.G.A. Luna. 2009. Spatial patterns of parasitism of the solitary parasitoid Pseudapanteles dignus (Hymenoptera: Braconidae) on Tuta absoluta (Lepidoptera: Gelechiidae). Environ. Entomol. 38: 365-374.
53. Smart, C. B., and P. J. Mayhew. 2009. A comparative study of sex ratio and clutch size in gregarious ichneumonoid wasps. J. Insect Behav. 22: 273-288.
54. Sime, R., K. Daane, J.W.Andrews, K. Hoelmer, C. H. Pickett, H. Nadel, M.L.W. Johnson, and R. H. Messing. 2006. The biology of Bracon celer as a parasitoid of the olive fruit by Karen. BioControl 51: 553-567. (Pubitemid 44510971)
55. Spanoudis, C. G., S. S. Andreadis, and S. Stefanos. 2012. Temperature- dependent survival, development, and adult longevity of the koinobiont endoparasitoid Venturia canescens (Hymenoptera: Ichneumonidae) parasitizing Plodia interpunctella (Lepidoptera: Pyralidae). J. Pest Sci. 85: 75-80.
56. Symondson, W.O.C., K. D. Sunderland, and M. H. Greenstone. 2002. Can generalist predators be effective biocontrol agents? Annu. Rev. Entomol. 47: 561-594. (Pubitemid 34108591)
57. Tena, A., A. Kapranas, F. Garcia-Mari, and R. F. Luck. 2009. Larval cannibalism during the late developmental stages of a facultatively gregarious encyrtid endoparasitoid. Ecol. Entomol. 34: 669-676.
58. Tome, H.V.V., E.M.G. Cordeiro, J. F. Rosado, and R.N.C. Guedes. 2012. Egg exposure to pyriproxyfen in the tomato leaf miner Tuta absoluta: ovicidal activity or behavioural- modulated hatching mortality? Ann. Appl. Biol. 160: 35-42.
59. Tropea Garzia, G., G. Siscaro, A. Biondi, and L. Zappala. 2012. Tuta absoluta, an exotic invasive pest from South America now in the EPPO region: biology, distribution and damage. Bull. OEPP 42: 205-210.
60. Urbaneja, A., J. Gonzalez-Cabrera, J. Arno, and R. Gabarra. 2012. Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag. Sci. 68: 1215-1222.
61. Van Driesche, R. G., and T. S. Bellows. 1996. Biological control. Chapman & Hall, New York, NY.
62. Van Lenteren, J. C. 2012. The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57: 1-20.
63. Walde, S. J., and W. M. Murdoch. 1988. Spatial density dependence in parasitoids. Annu. Rev. Entomol. 33: 441-466.
64. Wharton, R. A. 1993. Bionomics of the Braconidae. Annu. Rev. Entomol. 38: 121-143. (Pubitemid 24413911)
65. Wratten, S. D., M. Gillespie, A. Decourtye, E. Mader, and N. Desneux. 2012. Pollinator habitat enhancement: benefts to other ecosystem services. Agric. Ecosyst. Environ. 159: 112-122.
66. Yu, D.S.K., and C. Van Actherberg. 2010. Taxapad Ichneumonoidea. In F. A. Bisby, Y. R. Roskov, T. M. Orrell, D. Nicolson, L. E. Paglinawan, N. Bailly, P. M. Kirk, T. Bourgoin, and G. Baillargeon (eds.), Species 2000 & IT IS catalogue of life: 2010 annual checklist. DVD, Species 2000, Reading, United Kingdom.
67. Zappala, L., G. Siscaro, A. Biondi, O. Molla, J. Gonzalez-Cabrera, and A. Urbeneja. 2012a. Effcacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J. Appl. Entomol. 136: 401-409.
68. Zappala, L., U. Bernardo, A. Biondi, A. Cocco, S. Deliperi, G. Delrio, M. Giorgini, P. A. Pedata, C. Rapisarda, G. Tropea Garzia, et al. 2012b. Recruitment of native parasitoids by the exotic pest Tuta absoluta (Meyrick) in Southern Italy. Bull. Insectol. 65: 51-61.
69. Zappala, L., O. Campolo, S. B. Grande, F. Saraceno, A. Biondi, G. Siscaro, and V. Palmeri. 2012c. Dispersal of Aphytis melinus (Hymenoptera: Aphelinidae) after augmentative releases in citrus orchards. Eur. J. Entomol. 109: 561-568.