Genetically Modified Crops and Biological Control with Egg Parasitoids

  • Julio S. Bernal
Part of the Progress in Biological Control book series (PIBC, volume 9)


Genetically-modified (GM) crops presently are central components of pest management strategies for several important crops worldwide. GM crops include insect-resistant varieties (expressing transgenes from the bacterium Bacillus thuringiensis, or from plant species other than the GM crop, though only the former varieties are commercially available), and herbicide-tolerant varieties (which tolerate post-emergent applications of particular herbicides). This chapter examines potential and known impacts of GM crops on egg parasitoids. Egg parasitoids can be affected by insect-active toxins or proteins produced by insect-resistant GM crops, or by herbicides applied to herbicide-tolerant crops. A review of the literature showed that very little research has addressed the impacts of GM crops on egg parasitoids, compared to the research on larval parasitoids or predatory insects. The amount and focus of research involving egg parasitoids, though, may be subject to existing factual prejudices: (i) the presence of toxins from insect-resistant varieties in herbivore eggs used as hosts by egg parasitoids is improbable, and (ii) the target of herbicide-tolerant varieties is weeds, by way of herbicide applications. However, egg parasitoids can be affected by GM crops through infrequently explored, direct or indirect pathways, such as exposure to GM crop toxins in honeydew or nectars, or pauperization of host populations in insect-resistant crops or of flowering plant communities in herbicide-tolerant crops. These pathways of GM crop effects on egg parasitoids are likely the most important, but have not been adequately addressed. A fuller understanding of any effects of GM crops on egg parasitoids is particularly significant in the context of analyses pointing to the importance of movement of natural enemy populations among crops and between seasons within a landscape, for pest management and biological control at regional scales.


Biological Control Natural Enemy Host Plant Resistance Nectar Production Pest Management Strategy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abrahamson M (2007) Minnesota pest reports (16 Feb. 2007). Available at Accessed 23 April 2008
  2. AgBios (2008) GM database. Available at Accessed 28 January 2008
  3. Agrawal A, Klein CN (2000) What omnivores eat: direct effects of induced plant resistance on herbivores and indirect consequences for diet selection by omnivores. J Animal Ecol 69:529–535CrossRefGoogle Scholar
  4. Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agric, Ecosyst Environ 74:19–31CrossRefGoogle Scholar
  5. Altieri MA, Gurr GM, Wratten SD (2004) Genetic engineering and ecological engineering: a clash of paradigms or scope for synergy. In: Gurr GM, Wratten SD, Altieri MA (eds) Ecological engineering for pest management: Advances in habitat manipulation for arthropods. Comstock Publishing Associates, Ithaca, NY, pp 13–31Google Scholar
  6. Álvarez-Alfageme F, Ferry N, Castañera P, Ortego F, Gatehouse AMR (2008) Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Res 17:943–954PubMedCrossRefGoogle Scholar
  7. Anderson PC, Broadbeck BV, Mizell RF (1989) Metabolism of aminoacids, organic acids and sugars extracted from the xylem fluid of four host plants by adult Homalodisca vitripennis. Entomologia Experimentalis et Applicatta 50:149–159CrossRefGoogle Scholar
  8. Anonymous (2001) Biopesticides registration action document for Bacillus thuringiensis (Bt) plant-incorporated protectants. U.S. Environmental Protection Agency, Office of Pesticide Programs, Biopesticides and Pollution Prevention Division (October 15, 2001), 27 pGoogle Scholar
  9. Baker HG, Baker I (1975) Studies of nectar constitution and pollinator-plant coevolution. In: Gilbert LE, Raven PH (eds) Co-evolution of animals and plants. University of Texas Press, Austin, TX, pp 100–140Google Scholar
  10. Baker HG, Baker I (1983) Floral nectar sugar constituents in relation to pollinator type. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 117–141Google Scholar
  11. Begum M, Gurr GM, Wratten SD (2004) Flower color affects tri-trophic biocontrol interactions. Biological Control 30:584–590CrossRefGoogle Scholar
  12. Bell HA, Kirkbride-Smith AE, Marris GC, Edwards JP, Gatehouse AMR (2004) Oral toxicity and impact on fecundity of three insecticidal proteins on the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera:Eulophidae). Agric For Entomol 6:215–222CrossRefGoogle Scholar
  13. Benbrook CM (2004) Genetically engineered crops and pesticide use in the United States: The first nine years. BioTech InfoNet, Technical Paper Number 7, 38 pGoogle Scholar
  14. Bernal CC, Aguda RM, Cohen MB (2002) Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis. Entomol Exp Appl 102:21–28CrossRefGoogle Scholar
  15. Bernal JS, Sétamou M (2003) Fortuitous antixenosis in transgenic sugarcane: antibiosis-expressing cultivar deters oviposition by herbivore pests. Environ Entomol 32:886–894CrossRefGoogle Scholar
  16. Bernal JS, Prasifka J, Sétamou M, Heinz KM (2004) Transgenic insecticidal cultivars in integrated pest management: challenges and opportunities. In: Koul O, Dhaliwal GS, Cuperus GW (eds) Integrated pest management: Potential, constraints and challenges. CABI, Oxfordshire, pp 123–145CrossRefGoogle Scholar
  17. Bhatti MA, Duan J, Head GP, Jiang C, McKee M, Nickson TE, Pilcher CL, Pilcher CD (2005) Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on foliage-dwelling arthropods. Environ Entomol 34:1336–1345CrossRefGoogle Scholar
  18. Carter C, Graham RA, Thornburg RW (1999) Nectarin I is a novel, soluble germin-like protein expressed in the nectar of Nicotiana sp. Plant Mol Biol 41:207–216PubMedCrossRefGoogle Scholar
  19. Colazza S, Fucarino A, Peril E, Salerno G, Conti E, Bin F (2004) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J Exp Biol 207:47–53PubMedCrossRefGoogle Scholar
  20. Da Rocha L, Kolberg R, Mendonça M De S, Jr Redaelli LR (2007) Body size variation in Gryon gallardoi related to age and size of the host. BioControl 52:161–173CrossRefGoogle Scholar
  21. Degenhardt J, Gershenzonz J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14:169–176PubMedCrossRefGoogle Scholar
  22. Dobson HEM (1988) Survey of pollen and pollenkit lipids: chemical cues to flower visitors? Am J Botany 75:170–182CrossRefGoogle Scholar
  23. Eizaguirre M, Albajes R, López C, Eras J, Lumbierres B, Pons X (2006) Six years after the commercial introduction of Bt maize in Spain: field evaluation, impact and future prospects. Transgenic Res 15:1–12PubMedCrossRefGoogle Scholar
  24. Eubanks MD, Styrsky JD (2005) The effects of plant feeding on the performance of omnivorous ‘predators’. In: Wäckers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 148–177Google Scholar
  25. Faria CA, Wäckers FL, Turlings TCJ (2007) Increased susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PlosOne 2:1–11Google Scholar
  26. Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689CrossRefGoogle Scholar
  27. Fearing PL, Brown D, Vlachos D, Meghji M, Privalle L (1997) Quantitative analysis of CryIA(b) expression in Bt maize plants, tissues, and silage and stability of expression over successive generations. Mol Breed 3:169–176CrossRefGoogle Scholar
  28. Fernandes OA, Faria M, Martinelli S, Schmidt F, Carvalho VF, Moro G (2007) Short-term assessment of Bt maize on non-target arthropods in Brazil. Sci Agric 64:249–255CrossRefGoogle Scholar
  29. Ferry N, Mulligan EA, Majerus MEN, Gatehouse AMR (2007) Bitrophic and tritrophic effects of Bt Cry3A transgenic potato on beneficial, non-target beetles. Transgenic Res 16:795–812PubMedCrossRefGoogle Scholar
  30. Fox CW (1993) The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera: Bruchidae). Oecologia 96:139–146CrossRefGoogle Scholar
  31. Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369PubMedCrossRefGoogle Scholar
  32. Fuchsberg JR, Yong TH, Losey JE, Carter ME, Hoffmann AA (2007) Evaluation of corn leaf aphid (Rhopalosiphum maidis; Homoptera: Aphididae) honeydew as a food source for the egg parasitoid Trichogramma ostriniae (Hymenoptera: Trichogrammatidae). Biol Control 40:230–236CrossRefGoogle Scholar
  33. Gatehouse AMR (1999) Biotechnological applications of plant genes in the production of insect-resistant crops. In: Clement SL, Quisenberry SS (eds) Global plant genetic resources for insect-resistant crops. CRC Press, BocaRaton, pp 263–280Google Scholar
  34. Geng J, Shen Z, Song K, Zheng L (2006) Effect of pollen of regular cotton and transgenic Bt+CpTI cotton on the survival and reproduction of the parasitoid wasp Trichogramma chilonis (Hymenoptera: Trichogrammatidae) in the laboratory. Environ Entomol 35:1661–1668CrossRefGoogle Scholar
  35. Giolo FP, Grutzmacher AD, Procopio SO, Manzoni CG, Lima CAB, Nornberg SD (2005a) Side-effects of glyphosate formulations on Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Planta Daninha 23:457–462CrossRefGoogle Scholar
  36. Giolo FP, Grutzmacher AD, Manzoni CG, Fachinello JC, Nornberg SD, Stefanello GJ Jr (2005b) Side-effects of pesticides used in integrated production of peach on Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Revista Brasileira de Fruticultura 27:222–225CrossRefGoogle Scholar
  37. Giolo FP, Grutzmacher AD, Manzoni CG, De Lima CAB, Noernberg SD (2007a) Toxicity of pesticides used in peach orchard on adults Trichogramma pretiosum. Bragantia 66:423–431CrossRefGoogle Scholar
  38. Giolo FP, Grutzmacher AD, Manzoni CG, Harter WR, Castilhos RV, Muller C (2007b) Toxicity of pesticides used in peach production on the egg parasitoid Trichogramma atopovirilia Oatman and Platner, 1983 (Hymenoptera: Trichogrammatidae). Ciencia Rural 37:308–314CrossRefGoogle Scholar
  39. Gonzalez D (1971) Sampling as a basis for pest management strategies. In: Proceedings of the Tall Timbers Conference on Ecological Animal Control by Habitat Management. Tall Timbers Research Station, Tallahassee, USA, pp 83–101Google Scholar
  40. Gordh G, Legner EF, Caltagirone, LE (1999) Biology of parasitic Hymenoptera. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic, San Diego, CA, pp 355–381CrossRefGoogle Scholar
  41. Groot AT, Dicke M (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant J 31:387–406PubMedCrossRefGoogle Scholar
  42. Gurr GM, van Emden HF, Wratten SD (1998) Habitat manipulation and natural enemy efficiency: implications for the control of pests. In: Barbosa P (ed) Conservation biological control. Academic, UK, pp 155–183CrossRefGoogle Scholar
  43. Gurr GM, Wratten SD, Luna JM (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl Ecol 4:107–116CrossRefGoogle Scholar
  44. Hare JD (2002) Plant genetic variation in tritrophic interactions. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 8–43CrossRefGoogle Scholar
  45. Hawes C, Haughton AJ , Osborne JL, Roy DB, Clark SJ, Perry JN, Rothery P, Bohan DA, Brooks DR, Champion GT, Dewar MS, Heard MS, Woiwod IP, Daniels RE, Young MW, Parish AM, Scott RJ, Firbank LG, Squire GR (2003) Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the farm scale evaluations of genetically modified herbicide-tolerant crops. Philos Trans R Soc Lan B Biol Sci 358:1899–1913CrossRefGoogle Scholar
  46. Head G, Brown CR, Groth M, Duan JJ (2001) Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: implications for secondary exposure risk assessment. Entomol Exp Appl 99:37–45CrossRefGoogle Scholar
  47. Heimpel GE, Jervis MA (2005) Does floral nectar improve biological control by parasitoids? In: Wäckers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 267–304CrossRefGoogle Scholar
  48. Hilbeck A, Schmidt JEU (2006) Another view on Bt proteins – how specific are they and what else might they do? Biopestic Int 2:1–50Google Scholar
  49. Irvin NA, Hoddle MS, Castle SJ (2007) The effect of resource provisioning and sugar composition of foods on longevity of three Gonatocerus spp., egg parasitoids of Homalodisca vitripennis. Biol Control 40:69–79CrossRefGoogle Scholar
  50. James C (2007) Global status of Commercialized biotech/GM Crops: 2007. ISAAA Brief, No. 37. ISAAA: Ithaca, NYGoogle Scholar
  51. Jervis MA, Kidd NAC, Heimpel GE (1996) Parasitoid adult feeding behavior and biocontrol – a review. Biocontrol News Inf 17:11 N–26 NGoogle Scholar
  52. Jouanin L, Girard C, Bonadé-Bottino M, Le Metayer M, Picard Nizou A, Lerin J, Pham-Delègue M (1998) Impact of oilseed rape expressing proteinase inhibitors on coleopteran pests and honeybees. Cahiers Agric 7:531–536Google Scholar
  53. Kareiva P (1990) The spatial dimension in pest-enemy interactions. In: Mackauer M, Ehler L and Roland J (eds), Critical issues in biological control. Intercept Press, Andover, UK, pp 213–226Google Scholar
  54. Kanrar S, Venkateswari J, Kirti PB, Chopra VL (2002) Transgenic Indian mustard (Brassica juncea) with resistance to the mustard aphid (Lipaphis erysimi Kalt.). Plant Cell Rep 20:976–981CrossRefGoogle Scholar
  55. Keller MA, Lewis WJ, Stinner RE (1985) Biological and practical significance of movement by Trichogramma species: a review. Southwest Entomol 8:138–155Google Scholar
  56. Knesevic SZ, Cassman KG (2003) Use of herbicide-tolerant crops as a component of an integrated weed management program. Crop Manage J (online
  57. Koptur S (2005) Nectar as fuel for plant protectors. In: Wäckers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 75–108CrossRefGoogle Scholar
  58. Kozeil MG, Beland GL, Bowman C, Carozzi NB, Crenshaw R, Crossland L, Dawson J, Desai N, Hill M, Kadwell S, Launis K, Lewis K, Maddox D, McPherson K, Meghji MR, Merlin E, Rhodes R, Warren GW, Wright M, Evola SV (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Bio/Technology 11:194–200CrossRefGoogle Scholar
  59. 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
  60. Losey JE, Calvin DD, Carter ME, Mason CE (2001) Evaluation of noncorn host plants as a refuge in a resistance management program for European corn borer (Lepidoptera: Crambidae) on Bt-corn. Environ Entomol 30:728–735CrossRefGoogle Scholar
  61. Lövei GL, Arpaia S (2005) The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomol Exp Appl 114:1–14CrossRefGoogle Scholar
  62. Lumbierres B, Albajes R, Pons X (2004) Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance. Ecol Entomol 29:309–317CrossRefGoogle Scholar
  63. Malone LA (2002) Literature review on genetically modified plants and bee products. MAF Technical Paper No: 2002/05Google Scholar
  64. Malone LA, Pham-Delègue M (2002) Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.). Apidologie 32:287–304CrossRefGoogle Scholar
  65. Manachini B, Lozzia GC (2004) Studies on the effects of Bt corn expressing Cry1Ab on two parasitoids of Ostrinia nubilalis Hb. (Lepidoptera: Crambidae). Bulletin OILB/SROP - WPRS/SROP 27:109–116Google Scholar
  66. Mansfield S, Dillon L, Whitehouse MEA (2006) Are arthropod communities in cotton really disrupted? An assessment of insecticide regimes and evaluation of the beneficial disruption index. Agric Ecosyst Environ 113:326–335CrossRefGoogle Scholar
  67. Manzoni CG, Grutzmacher AD, Giolo FP, Harter WR, Muller C (2006) Side effects of pesticides used in integrated production of apple in adults of Trichogramma pretiosum. Pesquisa Agropecuaria Brasileira 41:1461–1467CrossRefGoogle Scholar
  68. McDougall SJ, Mills NJ (1997) The influence of hosts, temperature and food sources on the longevity of Trichogramma platneri. Entomol Exp Appl 83:195–203CrossRefGoogle Scholar
  69. Moreau J, Benrey B, Thiery D (2006) Assessing larval food quality for phytophagous insects: are the facts as simple as they appear? Funct Ecol 20:592–600CrossRefGoogle Scholar
  70. Moreau J, Thiery D, Troussard JP, Benrey B (2007) Grape variety affects female but also male reproductive success in wild European grapevine moths. Ecol Entomol 32:747–753CrossRefGoogle Scholar
  71. Nepi M, Franchi GG (2000) Cytochemistry of mature angiosperm pollen. In: Dafni A, Hesse M, Pacini E (eds) Pollen and pollination. Springer, Vienna, pp 45–62CrossRefGoogle Scholar
  72. Nicholls CI, Altieri MA (2004) Agroecological bases of ecological engineering for pest management. In: Gurr GM, Wratten SD, Altieri MA (eds) Ecological engineering for pest management: Advances in habitat manipulation for arthropods. Comstock Publishing Associates, Ithaca, pp 33–54Google Scholar
  73. Obrycki JJ, Ruberson JR, Losey JE (2004) Interactions between natural enemies and transgenic insecticidal crops. In: Ehler LE, Sforza R, Mateille T (eds) Genetics, evolution, and biological control. CAB International, Oxon, UK, pp 183–206CrossRefGoogle Scholar
  74. Orr DB, Landis DA (1997) Oviposition of European corn borer (Lepidoptera: Pyralidae) and impact of natural enemy populations in transgenic versus isogenic corn. J Econ Entomol 90:905–909Google Scholar
  75. Peumans WJ, Smeets K, van Nerum K, van Leuven F, van Damme EJM (1997) Lectin and alliinase are the predominant proteins in nectar from leek (Allium porrum L.) flowers. Planta 201:298–302PubMedCrossRefGoogle Scholar
  76. Picard-Nizou AL, Kerguelen V, Douault P, Marilleau R, Blight M, Jouanin L, Renard M, Pham-Delègue M (1993) Contribution to the study of honey bee-transgenic oilseed rape interactions. Apidologie 24:457–459Google Scholar
  77. Picard-Nizou AL, Pham-Delègue M, Kerguelen V, Douault P, Marilleau R, Olsen L, Grison R, Toppan A, Masson C (1995) Foraging behavior of honey bees (Apis mellifera L.) on transgenic oilseed rape (Brassica napus L. var. oleifera). Transgenic Res 4:270–276CrossRefGoogle Scholar
  78. Poppy GM, Sutherland JP (2004) Can biological control benefit from genetically-modified crops? Tritrophic interactions on insect-resistant transgenic plants. Physiol Entomol 29:257–268CrossRefGoogle Scholar
  79. Rahat R, Gurr GM, Wratten SD, Mo J, Neeson R (2005) Effect of plant nectars on adult longevity of the stinkbug parasitoid, Trissolcus basalis. Int J Pest Manage 51:321–324CrossRefGoogle Scholar
  80. Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the non target herbivore Rhopalosiphum padi (Homoptera: Aphididae) for presence of Cry1Ab. Mol Ecol 10:525–534PubMedCrossRefGoogle Scholar
  81. Romeis J, Babendreier D, Wäckers FL (2003) Consumption of snowdrop lectin (Galanthus nivalis agglutinin) causes direct effects on adult parasitic wasps. Oecologia 134:528–536PubMedGoogle Scholar
  82. Romeis J, Babendreier D, Wäckers FL, Shanower TG (2005) Habitat and plant specificity of Trichogramma egg parasitoids - underlying mechanisms and implications. Basic Appl Ecol 6:215–236CrossRefGoogle Scholar
  83. Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71PubMedCrossRefGoogle Scholar
  84. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. In: Dafni A, Hesse M, Pacini E (eds) Pollen and pollination. Springer, Vienna, pp 187–211CrossRefGoogle Scholar
  85. Roy DB, Bohan DA, Haughton AJ, Hill MO, Osborne JL, Clark SJ, Perry JN, Rothery P, Scott RJ, Brooks DR, Champion GT, Hawes C, Heard MS, Firbank LG (2003) Invertebrates and vegetation of field margins adjacent to crops subject to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. Philos Trans R Soc Lan B Biol Sci 358:1879–1898CrossRefGoogle Scholar
  86. Sachs ES, Benedict JH, Stelly DM, Taylor JF, Altman DW, Berberich SA, Davis SK (1998) Expression and segregation of genes encoding CryIA insecticidal proteins in cotton. Crop Sci 38:1–11CrossRefGoogle Scholar
  87. Schüler TH, Poppy GM, Kerry BR, Denholm I (1998) Insect-resistant transgenic plants. Trends Biotechnol 16:168–175CrossRefGoogle Scholar
  88. Schmidt MH, Thies C, Tscharntke T (2004) Landscape context of biological control. In: Gurr GM, Wratten SD, Altieri MA (eds) Ecological engineering for pest management: Advances in habitat manipulation for arthropods. Comstock, Ithaca, NY, pp 55–63Google Scholar
  89. Senthil Nathan S, Kalaivani K, Mankin RW, Murugan K (2006) Effects of millet, rice, and sorghum diets on development of Corcyra cephalonica (Stainton) (Lepidoptera: Galleriidae) and its suitability as a host for Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae). Environ Entomol 35:784–788CrossRefGoogle Scholar
  90. Sétamou M, Bernal JS, Legaspi JC, Mirkov TE, Legaspi B (2002) Evaluation of lectin-expressing transgenic sugarcane against stalkborers (Lepidoptera: Pyralidae): effects on life history parameters and damage. J Econ Entomol 95:469–477PubMedCrossRefGoogle Scholar
  91. Shi Y, Wang MB, Powell KS, van Damme E, Hilder VA, Gatehouse AMR, Boulter D, Gatehouse JA (1994) Use of the rice sucrose synthase-1 promotor to direct phloem-specific expression of β-glucuronidase and snow drop lectin genes in transgenic tobacco plants. J Exp Botany 45:623–631CrossRefGoogle Scholar
  92. Solberg Y, Remedios G (1980) Chemical composition of pure and bee-collected pollen. Medlinger fra Norges Landbruksshoegskole 59:2–12Google Scholar
  93. Spitzen J, van Huis A (2005) Effect of host quality of Callosobruchus maculates (Coleoptera: Bruchidae) on performance of the egg parasitoid Uscana lariophaga (Hymenoptera: Trichogrammatidae). Bull Entomol Res 95:341–347PubMedCrossRefGoogle Scholar
  94. Tesoriero D, Sgolastra F, Dall’Asta S, Venier F, Sabatini A, Burgio G, Porrini C(2004) Effects of Bt-oilseed rape on the foraging activities of honey bees in confined environment. Redia 87:195–198Google Scholar
  95. Treacy MF, Benedict JH, Walmsley MH, Lopez JD, Morrison RK (1987) Parasitism of bollworm (Lepidoptera: Noctuidae) eggs on nectaried and nectariless cotton. Environ Entomol 16:420–423Google Scholar
  96. Tscharntke T (2000) Parasitoid populations in the agricultural landscape. In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, NY, pp 235–253Google Scholar
  97. van Huis A, Rooy Mde (1998) The effect of leguminous plant species on Callosobruchus maculates (Coleoptera: Bruchidae) and its egg parasitoid Uscana lariophaga (Hymenoptera: Trichogrammatidae). Bull Entomol Res 88:93–99CrossRefGoogle Scholar
  98. Wäckers FL (2005) Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. In: Wäckers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 17–74CrossRefGoogle Scholar
  99. Wäckers FL, van Rijn PCJ, Heimpel GE (2008) Honeydew as a food source for natural enemies: Making the best of a bad meal? Biol Control 45:176–184CrossRefGoogle Scholar
  100. Wang Z, Wu Y, He K, Bai S (2007) Effects of transgenic Bt maize pollen on longevity and fecundity of Trichogramma ostriniae in laboratory conditions. Bull Insectol 60:49–55Google Scholar
  101. Wellinga S, Wysoki M (1989) Preliminary investigation of food source preferences of the parasitoid Trichogramma platneri Nagarkatti (Hymenoptera, Trichogrammatidae). Anzeiger für Schädlingskunde Pflanzenschutz Umweltschutz 62:133–135CrossRefGoogle Scholar
  102. Whitehouse MEA, Wilson LJ, Fitt GP (2005) A comparison of arthropod communities in transgenic Bt and conventional cotton in Australia. Environ Entomol 34:1224–1231CrossRefGoogle Scholar
  103. Whitehouse MEA, Wilson LJ, Constable GA (2007) Target and non-target effects on the invertebrate community of Vip cotton, a new insecticidal transgenic. Aust J Agric Res 58:273–285CrossRefGoogle Scholar
  104. Yang YZ, Yu YS, Ren L, Shao YD, QianK, Zalucki MP (2005) Possible incompatibility between transgenic cottons and parasitoids. Aust J Entomol 44:442–445CrossRefGoogle Scholar
  105. Zhang GR, Zimmermann O, Hassan SA (2004) Pollen as a source of food for egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae). Biocontrol Sci Technol 14:201–209CrossRefGoogle Scholar
  106. Zimmermann O, Ren Z, Hassan SA (2004) Risk assessment of culturing transgenic crops: testing side effects of Bt corn on Microhymenoptera of the genus Trichogramma (Hym., Trichogrammatidae). Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 14:431–434Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of EntomologyTexas A&M UniversityCollege StationUSA

Personalised recommendations