Agronomy for Sustainable Development

, Volume 31, Issue 1, pp 233–250 | Cite as

Ionising radiation and area-wide management of insect pests to promote sustainable agriculture. A review

Review Article

Abstract

Despite the liberal use of broad-spectrum insecticides to keep many insect pests of agricultural and veterinary importance at bay, food losses, both pre- and post-harvest, due to these insect pests contribute significantly to the high prevalence of undernourishment in the world. New, innovative pest control tactics and strategies are therefore needed that are both effective and not detrimental to the environment. As part of the arsenal of environmentally-friendly control tactics, the sterile insect technique (SIT) has proven to be a very effective tool against selected insect pests when used as part of an area-wide integrated pest management (AW-IPM) approach. Likewise, the use of natural enemies for augmentative or inundative biological control is now a major component of pest control in many parts of the world. Both control tactics are complementary and even synergistic under certain circumstances, but their combined use has so far not been applied on an operational scale. Ionising radiation can be readily employed to effectively and safely induce sexual sterility in insects. Although the sterile insect technique has often been associated with an eradication strategy, major advances in rearing efficiency, and improved handling and release methods, have made the use of sterile insects economically feasible for insect pest suppression, prevention or containment. Recently, more emphasis has been placed on the quality of the sterile insect once released in the field rather than mainly assessing quality in the rearing facility. This combined with other innovations such as the development of genetic sexing strains, better understanding the impact of radiation on radio-resistant species such as Lepidoptera and the development of the F1 sterility concept, advances in monitoring the induced sterility, etc. have significantly increased the efficiency of the sterile insect technique for several insect species. The action of sterile insects is inversely dependent on the density of the target population, and sterile insects have the intrinsic capacity to actively search for and mate with the last individuals of a pest population. These two characteristics make them ideal to deal with outbreaks of invasive insect pests. The use of sterile insects presents no threat to the environment, but aspects such as diet and waste disposal in large rearing facilities or bio-security in cases where the rearing facility is located in an area that is already free of the pest require the necessary attention. Ionising radiation can also be applied to greatly improve the efficiency of mass-rearing, handling and shipment of insect parasitoids and predators. Area-wide integrated pest management programmes that use sterile insects or natural enemies are complex and management-intensive, and require a management structure that is exclusively dedicated to the programme. Past and current examples have shown the enormous benefit-cost ratios that these programmes can generate and their importance for enhanced agriculture is increasing in significance.

Keywords

natural enemies sterile insect technique area-wide integrated pest management economic benefits 

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References

  1. (APHIS/USDA) Animal and Plant Health Inspection Service/United States Department of Agriculture. (2001) Screwworm programme review, Final Report.Google Scholar
  2. Ashraf M., Chatha N., Ohinata K., Harris E.J. (1975) Melon flies: dosageresponse and sexual competitiveness after treatment with gamma irradiation in a nitrogen atmosphere, J. Econ. Entomol. 68, 838–840.Google Scholar
  3. Bakri A., Metha K., Lance D.R. (2005a) Sterilizing insects with ionizing radiation, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 233–268.Google Scholar
  4. Bakri A., Heather J., Hendrichs J., Ferris I. (2005b) Fifty years of radiation biology in entomology: lessons learned from IDIDAS, Ann. Entomol. Soc. Am. 98, 1–12.Google Scholar
  5. Barclay H.J., Hargrove J.W. (2005) Probability models to facilitate a declaration of pest-free status, with special reference to tsetse (Diptera: Glossinidae), Bull. Entomol. Res. 95, 1–11.PubMedGoogle Scholar
  6. Barclay H.J., Hargrove J.W., Clift A., Meats A. (2005) Procedures for declaring pest free status, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 363–386.Google Scholar
  7. Barnes B.N., Eyles D.K., Franz G. (2004) South Africa’s fruit fly SIT project — the Hex River Valley pilot project and beyond, in: Barnes B.N. (Ed.), Proceedings of the 6th International Symposium on Fruit Flies of Economic Importance, 6–10 May 2002, Stellenbosch, South Africa, Isteg Scientific Publications, Irene, South Africa, pp. 131–141.Google Scholar
  8. Baumhover A.H. (1966) Eradication of the screwworm fly. An agent of myiasis, J. Am. Med. Assoc. 196, 240–248.Google Scholar
  9. Baumhover A.H., Graham A.J., Bitter B.A., Hopkins D.E., New W.D., Dudley F.H., Bushland R.C. (1955) Screwworm control through release of sterilized flies, J. Econ. Entomol. 48, 462–466.Google Scholar
  10. Bigler F., Babendreier D., Kuhlmann U. (2006) Environmental risks of invertebrate biological control agents: methods and risk assessment, CABI publishing, Wallingford, UK.Google Scholar
  11. Bloem K.A., Bloem S. (2000) SIT for codling moth eradication in British Columbia, Canada, in: Tan K.H. (Ed.), Area-wide Control of Fruit Flies and Other Insect Pests, Proceedings of an International Conference on Area-wide Control of Insect Pests and the 5th International Symposium on Fruit Flies of Economic Importance, 28 May–5 June 1998, Penang, Malaysia, Penerbit Universiti Sains, Malaysia, pp. 207–214.Google Scholar
  12. Bloem K.A., Bloem S., Carpenter J.E. (2005) Impact of moth suppression/eradication programmes using the sterile insect technique or inherited sterility, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 677–700.Google Scholar
  13. Bloem S., Bloem K.A., Carpenter J.E., Calkins C.O. (2001) Seasonlong releases of partially sterile males for control of codling moth Cydia pomonella (Lepidoptera: Tortricidae), in Washington apples, Environ. Entomol. 30, 763–769.Google Scholar
  14. Bloem S., Bloem K., Knight A.L. (1998) Oviposition by sterile codling moths, Cydia pomonella (Lepidoptera: Tortricidae) and control of wild populations with combined releases of sterile moths and egg parasitoids, J. Entomol. Soc. Brit. Columbia 95, 99–109.Google Scholar
  15. Botto E., Glaz P. (2010) Potential for controlling codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) in Argentina using the sterile insect technique and egg parasitoids, J. Appl. Entomol. 134, 251–260.Google Scholar
  16. Brown H.E. (1984) Mass production of screwworm flies, Cochliomyia hominivorax, in: King E.G., Leppla N. (Eds.), Advances and challenges in insect rearing, USDA-ARS, New Orleans, USA, pp. 193–199.Google Scholar
  17. Bushland R.C., Hopkins D.E. (1951) Experiments with screwworm flies sterilized by X-rays, J. Econ. Entomol. 44, 725–731.Google Scholar
  18. Bushland R.C., Hopkins D.E. (1953) Sterilization of screwworm flies with X-rays and gamma rays, J. Econ. Entomol. 46, 648–656.Google Scholar
  19. Cáceres C., Cayol J.P., Enkerlin W., Franz G., Hendrichs J., Robinson A.S. (2004) Comparison of Mediterranean fruit fly (Ceratitis capitata) (Diptera: Tephritidae) bisexual and genetic sexing strains: development, evaluation and economics, in: Barnes B.N. (Ed.), Proceedings of the 6th International Symposium on Fruit Flies of Economic Importance, Isteg Scientific Publications, Irene, South Africa, pp. 367–381.Google Scholar
  20. Calkins C.O., Parker A.G. (2005) Sterile insect quality, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 269–296.Google Scholar
  21. Cancino J., Ruíz L., López P., Sivinski J. (2009) The suitability of Anastrepha spp. and Ceratitis capitata (Diptera: Tephritidae) larvae as hosts of Diachasmimorpha longicaudata and Diachasmimorpha tryoni (Hymenoptera: Braconidae): Effects of host age and radiation dose and implications for quality control in mass rearing, Bio. Sci. Tech. 19, S1, 81–94.Google Scholar
  22. Cardé R.T., Minks A.K. (1995) Control of moth pests by mating disruption: successes and constraints, Annu. Rev. Entomol. 40, 559–585.Google Scholar
  23. Carpenter J.E., Gross H.R. (1993) Suppression of feral Helicoverpa zea (Lepidoptera: Noctuidae) populations following infusion of inherited sterility from released substerile males, Environ. Entomol. 22, 1084–1091.Google Scholar
  24. Carpenter J.E., Bloem S., Marec F. (2005) Inherited sterility in insects, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management. Springer, Dordrecht, The Netherlands, pp. 115–146.Google Scholar
  25. Carpenter J.E., Hidryani E., Sheehan W. (1996) Compatibility of F1 sterility and a parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae), for managing Spodoptera exigua (Lepidoptera: Noctuidae): acceptability and suitability of host, Fla. Entomol. 79, 289–295.Google Scholar
  26. Celmer-Warda K. (2004) Preliminary studies on suitability and acceptability of irradiated host-larvae (Plodia interpunctuella) by larval parasitoids Venturia canescens (Gravenhorst), Ann. Warshaw Agr. Univ-SGGW, Horticulture, Landscape Architecture 25, 67–73.Google Scholar
  27. Clift A., Meats A. (2002) When does zero catch in a male lure mean no tephritid flies in the area? in: Barnes B.N. (Ed.), Proceedings of the 6th International Symposium on Fruit Flies of Economic Importance, 6–10 May 2002, Stellenbosch, South Africa, Isteg Scientific Publications, Irene, South Africa, pp. 183–188.Google Scholar
  28. Courschee R.J. (1960) Some aspects of the application of insecticides, Annu. Rev. Entomol. 5, 327–352.Google Scholar
  29. Dame D.A. (1970) Control by sterilization of Glossina, in: Mulligan H.W. (Ed.), The African trypanosomiasis, Allen and Unwin Ltd, London, UK, pp. 533–542.Google Scholar
  30. Dove W.E. (1937) Myiasis of man, J. Econ. Entomol. 30, 29–39.Google Scholar
  31. Dowell R.V., Worley J., Gomes P.J. (2005) Sterile insect supply, emergence and release, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 297–324.Google Scholar
  32. Dyck V.A., Hendrichs J., Robinson A.S. (2005) Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands.Google Scholar
  33. Economopoulos A.P. (1977) Gamma-ray sterilization of Dacus oleae (Gmelin). Effect of nitrogen on the competitiveness of irradiated males, Z. Ang. Entomol. 83, 86–95.Google Scholar
  34. Enkerlin W.R. (2005) Impact of fruit fly control programmes using the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 651–676.Google Scholar
  35. EPPO European and Mediterranean Plant Protection Organization (EPPO) (2000) Safe use of biological control: import and release of exotic biological control agents, EPPO Standard PM6/2(1), http://www.eppo.org.
  36. Fatima B., Ahmad N., Memon R.M., Bux M., Ahmad Q. (2009) Enhancing biological control of sugarcane shoot borer, Chilo infuscatellus (Lepidoptera: Pyralidae), through use of radiation to improve laboratory rearing and field augmentation of egg and larval parasitoids, Bio. Sci. Tech. 19, S1, 277–290.Google Scholar
  37. Food and Agriculture Organization of the United Nations (FAO) (1992) The New World screwworm eradication programme, North Africa (1988–1992), FAO, Rome, Italy.Google Scholar
  38. Food and Agriculture Organization of the United Nations (FAO) (1995) Glossary of phytosanitary terms, ISPM, Publication number 5, IPPC, FAO, Rome, Italy.Google Scholar
  39. Food and Agriculture Organization of the United Nations (FAO) (2005) International standards for phytosanitary measures, Guidelines for the export, shipment, import and release of biological control agents and other beneficial organisms (revision adopted at the 7th session of the ICPM, April 2005), Publication No. 3, Secretariat of the International Plant Protection Convention, FAO, Rome, Italy.Google Scholar
  40. Food and Agriculture Organization of the United Nations (FAO) (2008) FAOSTAT, http://www.fao.org/faostat/foodsecurity/index_en.htm.
  41. Fisher K. (1997) Irradiation effects in air and in nitrogen on Mediterranean fruit fly (Diptera: Tephritidae) pupae in Western Australia, J. Econ. Entomol. 90, 1609–1614.Google Scholar
  42. Fisher K., Cáceres C. (2000) A filter rearing system for mass reared medfly, in: Tan K.H. (Ed.), Area-Wide Control of Fruit Flies and Other Insect Pests, Proceedings of an International Conference on Area-Wide Control of Insect Pests, and the 5th International Symposium on Fruit Flies of Economic Importance, 28 May–5 June 1998, Penang, Malaysia, Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia, pp. 543–550.Google Scholar
  43. Follet P.A., Duan J.J. (2000) Non-target effects of biological control, Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  44. Ford J., Nash T.A.M., Welch J.R. (1970) Control by clearing of vegetation, in: Mulligan H.W. (Ed.), The African trypanosomiasis, Allen and Unwin Ltd, London, UK, pp. 543–556.Google Scholar
  45. Franz G. (2005) Genetic sexing strains in Mediterranean fruit fly, an example for other species amenable to large-scale rearing for the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 427–251.Google Scholar
  46. Franz G., Gencheva E., Kerremans P. (1994) Improved stability of genetic sex-separation strains for the Mediterranean fruit fly, Ceratitis capitata, Genome 37, 72–82.PubMedGoogle Scholar
  47. Genchev N.P., Michelva-Dimitrova R.Y., Kozhuharova M.V. (2007) Use of gamma radiation for suppression of the hemocytic immune response in larvae of Galleria mellonella (Lepidoptera) against Venturia canescens (Hymenoptera), J. Balkan Ecol. 10, 411–419.Google Scholar
  48. Gonzalez J., Troncoso P. (2007) The fruit fly exclusion programme in Chile, in: Vreysen M.J.B., Robinson A.S., Hendrichs J. (Eds.), Area-wide control of insect pests. From research to field implementation, Springer, Dordrecht, The Netherlands, pp. 614–651.Google Scholar
  49. Hamed M., Nadeem S., Riaz A. (2009) Use of gamma radiation for improving the mass-production of Trichogramma chilonis and Chrysoperla carnea, Bio. Sci. Tech. 19, S1, 43–48.Google Scholar
  50. Hamilton G. (2000) When good bugs turn bad, New Scientist, 30–33.Google Scholar
  51. Hendrichs J., Franz G., Rendón P. (1995) Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons, J. Appl. Entomol. 119, 371–377.Google Scholar
  52. Hendrichs J., Kenmore P., Robinson A.S., Vreysen M.J.B. (2007) Areawide integrated pest management (AW-IPM): principles, practice and prospects, in: Vreysen M.J.B., Robinson A.S., Hendrichs J. (Eds.), Area-wide control of insect pests. From research to field implementation, Springer, Dordrecht, The Netherlands, pp. 3–33.Google Scholar
  53. Hendrichs J., Vreysen M.J.B., Enkerlin W.R., Cayol J.P. (2005) Strategic options in using sterile insects for area-wide integrated pest management, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 563–600.Google Scholar
  54. Hendrichs J., Bloem K.A., Hoch G., Carpenter J.E., Greany P., Robinson A.S. (2009) Improving the cost-effectiveness, trade and safety of biological control for agricultural insect pests using nuclear techniques, Bio. Sci. Tech. 19, 3–22.Google Scholar
  55. Herren H.R., Neuenschwander P., Hennesey R.D., Hammond W.N.O. (1987) Introduction and dispersal of Epidinocarsis lopezi (Hym., Encyrtidae), an exotic parasitoid of the cassava mealybug, Phenacoccus manuhoti (Hom., Pseudococcidae), Africa, Agric. Ecosyst. Environ. 19, 131–144.Google Scholar
  56. Herren H.R., Neuenschwander P. (1991) Biological control of cassava pests in Africa, Annu. Rev. Entomol. 36, 257–283.Google Scholar
  57. Hokkanen H.M.T., Lynch J.M. (1996) Biological control — benefits and risks, Cambridge University Press, UK.Google Scholar
  58. Hooper G.H.S. (1989) The effect of ionizing radiation on reproduction, in: Robinson A.S., Hooper G. (Eds.), World crop pests, Vol. 3A, Fruit flies, their biology, natural enemies and control, Elsevier, Amsterdam, The Netherlands, pp. 153–164.Google Scholar
  59. International Atomic Energy Agency (IAEA) (2008) Model business plan for a sterile insect production facility, 978-92-0-110007-8, IAEA, Vienna, Austria.Google Scholar
  60. International Atomic Energy Agency/Food and Agriculture Organization of the United Nations (IAEA/FAO) (1997) Control of the Mediterranean fruit fly in the Near East region using the sterile insect technique, STI/PUB/1020, IAEA, Vienna, Austria.Google Scholar
  61. Klassen W. (2005) Area-wide integrated pest management and the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique, Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 39–68.Google Scholar
  62. Klassen W., Creech J.P. (1973) Population suppression with dominant and conditional lethal mutations; some important considerations and approaches, in: Computer models and application for the sterile male technique, IAEA, Vienna, Austria, pp. 65–79.Google Scholar
  63. Knipling E.F. (1955) Possibilities of insect population control through the use of sexually sterile males, J. Econ. Entomol. 48, 443–448.Google Scholar
  64. Knipling E.F. (1959) The sterile male method of population control, Science 130, 902–904.PubMedGoogle Scholar
  65. Knipling E.F. (1960) The eradication of the screwworm fly, Sci. Am. 203, 54.PubMedGoogle Scholar
  66. Knipling E.F. (1966) Some basic principles in insect population suppression, Bull. Entomol. Soc. Am. 12, 7–15.Google Scholar
  67. Knipling E.F. (1972) Entomology and the management of man’s environment, J. Aust. Entomol. Soc. 11, 153–167.Google Scholar
  68. Knipling E.F. (1979) The basic principles of insect population suppression and management, Agriculture Handbook Number 512, SEA, USDA, Washington DC, USA.Google Scholar
  69. Knipling E.F. (1992) Principles of insect parasitism analyzed from new perspectives: practical implications for regulating insect populations by biological means, USDA Agriculture Handbook No. 693, USA.Google Scholar
  70. Koul O., Cuperus G., Elliott N. (2008) Areawide pest management. Theory and implementation, Cab International, UK.Google Scholar
  71. Kovaleski A., Mumford J. (2007) Pulling out the evil by the root; the codling moth Cydia pomonella eradication programme in Brazil, in: Vreysen M.J.B., Robinson A.S., Hendrichs J. (Eds.), Areawide control of insect pests. From research to field implementation, Springer, Dordrecht, The Netherlands, pp. 581–590.Google Scholar
  72. Koyama T., Kakinohana H., Miyatake T. (2004) Eradication of the melon fly Bactrocera cucurbitae in Japan: importance of behaviour, ecology, genetics and evolution, Annu. Rev. Entomol. 49, 331–349.PubMedGoogle Scholar
  73. Krafsur E. (1998) Sterile insect technique for suppressing and eradicating insects; 50 years and counting, J. Agric. Entomol. 15, 303–317.Google Scholar
  74. Kuznetsova V.G., Petropavlovskaia M.B. (1976) Behaviour of holokinetic chromosomes in the spermatogenesis of bugs, Tsitologiia 18, 702–711.PubMedGoogle Scholar
  75. LaChance L.E. (1979) Genetic strategies affecting the success and economy of sterile insect release method, in: Hoy M.A., McKelvey J.J. Jr. (Eds.), Genetics in relation to insect management, Rockefeller Foundation, NY, WA, USA, pp. 8–18.Google Scholar
  76. LaChance L.E. (1985) Genetic methods for the control of lepidopteran species: status and potential, ARS-28, USDA/ARS, Washington DC, USA.Google Scholar
  77. LaChance L.E., Schmidt C.H., Bushland R.C. (1967) Radiation induced sterilization, in: Kilgore W.W., Doutt R.L. (Eds.), Pest control: biological, physical and selected chemical methods, Academic Press, New York, USA, pp. 147–196.Google Scholar
  78. Lance D.R., McInnis D.O. (2005) Biological basis of the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 69–94.Google Scholar
  79. Lance D.R., McInnis D.O., Rendón P., Jackson C.G. (2000) Courtship among sterile and wild Ceratitis capitata (Diptera: Tephritidae) in field cages in Hawaii and Guatemala, Ann. Entomol. Soc. Am. 93, 1179–1185.Google Scholar
  80. Lindquist D.A., Abusowa M., Hall M.J.R. (1992) The New World screwworm in Libya: review of its introduction and eradication, Med. Vet. Entomol. 6, 2–8.PubMedGoogle Scholar
  81. Loomans A.J.M. (2006) Regulation of invertebrate biological control agents in Europe: review and recommendations in its pursuit of a harmonised regulatory system, Report of REBECA, http://www.rebeca-net.de/downloads/.
  82. Louda S.M., Pemberton R.W., Johnson M.T., Follett P.A. (2003) Nontarget effects: the Achilles’ heel of biological control? Annu. Rev. Entomol. 48, 365–396.PubMedGoogle Scholar
  83. (MAG/SAG) Ministerio de Agricultura/Servicio Agricola y Ganadero. (1995) Chile; a medfly-free country, Pamphlet, Government of Chile, Santiago, Chile.Google Scholar
  84. Mannion C.M., Carpenter J.E., Gross H.R. (1994) Potential of the combined use of inherited sterility and a parasitoid, Archytas marmoratus (Diptera: Tachinidae) for managing Helicoverpa zea (Lepidoptera: Noctuidae), Environ. Entomol. 23, 41–46.Google Scholar
  85. Marroquin R. (1985) Mass production of screwworms in Mexico, in: Symposium on eradication of the screwworm from the United States and Mexico, Proceedings of a Symposium Presented at the National Meeting of the Entomological Society of America, 9–13 December 1984, San Antonio, Texas, Entomological Society of America, MD, USA, pp. 31–36.Google Scholar
  86. Mastro V.C. (1993) Gypsy moth F1 sterility program: current status, in: Radiation Induced F1 Sterility in Lepidoptera for Area-Wide Control, Proceedings of the Final Research Coordination Meeting, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, 9–13 September 1991, Phoenix, AZ, USA, STI/PUB/929. IAEA, Vienna, Austria, pp. 125–129.Google Scholar
  87. McInnis D.O., Tam S.Y.T., Grace C., Miyashita D. (1994) Population suppression and sterility rates induced by variable sex-ratio, sterile insect releases of Ceratitis capitata (Diptera: Tephritidae) in Hawaii, Ann. Entomol. Soc. Am. 87, 231–240.Google Scholar
  88. Meyer N.L. (1994) History of theMexico-United States screwworm eradication program, Vantage Press, New York, USA.Google Scholar
  89. Miyatake T., Yamagishi M. (1993) Active quality control in mass reared melon flies. Quantitative genetic aspects, in: Management of Insect Pests: Nuclear and Related Molecular and Genetic Techniques, Proceedings of an IAEA/FAO International Symposium, 19–23 October 1992, Vienna, Austria. STI/PUB/909, IAEA, Vienna, Austria, pp. 201–213.Google Scholar
  90. Mumford J.D. (2005) Application of benefit/cost analysis to insect pest control using the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 481–498.Google Scholar
  91. Nagel P., Peveling R. (2005) Environment and the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique, Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 499–524.Google Scholar
  92. Nakashima Y., Hirose Y., Kinjo K. (1996) Rearing Orius sauteri (Poppius) on diet of freeze-dried larval powder of melon fly, Bactrocera cucurbitae Coquillett, Jap. J. Appl. Entomol. Zool. 40, 80–82.Google Scholar
  93. North American Plant Protection Organization (NAPPO) (2008) http://www.nappo.org/newsletter/2008/September.
  94. Neuenschwander P. (1993) Human interactions in classical biological control of cassava and mango mealy bugs on subsistence farms in tropical Africa, in: Altieri M.A. (Ed.), Crop protection strategies for subsistence farmers, IT Publications, London, Westview Press, San Francisco, USA, pp. 143–177.Google Scholar
  95. North D.T. (1967) Radiation-induced male sterility exhibited in the P1 and F1 generations in Lepidoptera, Rad. Res. 31, 615.Google Scholar
  96. North D.T. (1975) Inherited sterility in Lepidoptera, Annu. Rev. Entomol. 20, 167–182.PubMedGoogle Scholar
  97. North D.T., Holt G.G. (1969) Population suppression by transmission of inherited sterility to progeny of irradiated cabbage looper, Trichoplusia ni, Can. Entomol. 101, 513–520.Google Scholar
  98. Parker A.G. (2005) Mass-rearing for sterile insect release, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 209–232.Google Scholar
  99. Parker A.G., Mehta K. (2007) Sterile insect technique: a model for dose optimization for improved sterile insect quality, Fla. Entomol. 90, 88–95.Google Scholar
  100. Pimentel D. (2007) Area-wide pest management: environmental, economic and food issues, in: Vreysen M.J.B., Robinson A.S., Hendrichs J. (Eds.), Area-wide control of insect pests. From research to field implementation, Springer, Dordrecht, The Netherlands, pp. 35–47.Google Scholar
  101. Proverbs M.D. (1962) Progress on the use of induced sexual sterility for the control of codling moth Carpocapsa pomonella (L.) (Lepidoptera: Olethreutidae), Proc. Entomol. Soc. Ontario 92, 5–11.Google Scholar
  102. Proverbs M.D., Newton J.R., Campbell C.J. (1982) Codling moth: a pilot programme of control by sterile insect release in British Columbia, Can. Entomol. 114, 363–376.Google Scholar
  103. Rendón P., McInnis D., Lance D., Stewart J. (2000) Comparison of medfly-male only and bisexual releases in large scale field trials, in: Tan K.H. (Ed.), Area-Wide Control of Fruit Flies and Other Insect Pests, Proceedings of an International Conference on Area-Wide Control of Insect Pests, and the 5th International Symposium on Fruit Flies of Economic Importance, 28 May–5 June 1998, Penang, Malaysia, Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia, pp. 517–525.Google Scholar
  104. Rendón P., McInnis D., Lance D., Stewart J. (2004) Medfly (Diptera: Tephritidae) genetic sexing: large scale field comparison of malesonly and bisexual sterile fly releases in Guatemala, J. Econ. Entomol. 97, 1547–1553.PubMedGoogle Scholar
  105. Robinson A.S. (2002) Mutations and their use in insect control, Mut. Res. 511, 113–132.Google Scholar
  106. Robinson A.S., Hendrichs J. (2005) Prospects for the future development and application of the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 727–760.Google Scholar
  107. Rössler Y. (1979) The genetics of the Mediterranean fruit fly: a “white pupae” mutant, Ann. Entomol. Soc. Am. 72, 583–585.Google Scholar
  108. Runner G.A. (1916) Effect of röntgen rays on the tobacco, or cigarette beetle and the results of experiments with a new form of röntgen tube, J. Agric. Res. 6, 383–388.Google Scholar
  109. Sakurai H., Murakami Y., Kohama T., Teruya T. (2000) Sterilizing mechanism of gamma-radiation in the female ofWest Indian potato weevil, Euscepes postfasciatus, Res. Bull. Fac. Agric. Gifu University, Japan 65, 13–20.Google Scholar
  110. Seth R.K., Barik T.K., Chauhan S. (2009) Interactions of entomopathogenic nematodes Steinernema glaseri (Rhabditida: Steinernematidae) cultured in irradiated hosts, with F1 sterility: towards management of a tropical pest Spodoptera litura (Fabr.) (Lepidoptera: Noctuidae), Bio. Sci. Tech. 19, 139–155.Google Scholar
  111. Simmons G., Carpenter J.E., Suckling D.M., Addison M., Dyck V.A., Vreysen M.J.B. (2010) Improved quality management to enhance the efficacy of the sterile insect technique for lepidopteran pests. J. Appl. Entomol. 134, 261–273.Google Scholar
  112. Suckling D.M., Barrington A.M., Chhagan A., Stephens A.E.A., Burnip G.M., Charles J.G., Wee S.L. (2007) Eradication of the Australian painted apple moth Teia anartoides in New Zealand: trapping, inherited sterility and male competitiveness, in: Vreysen M.J.B., Robinson A.S., Hendrichs J. (Eds.), Area-wide control of insect pests. From research to field implementation, Springer, Dordrecht, The Netherlands, pp. 603–615.Google Scholar
  113. Staten R.L., Rosander R.W., Keaveny D.F. (1993) Genetic control of cotton insects: the pink bollworm as a working programme, in: Management of Insect Pests; Nuclear and Related Molecular and Genetic Techniques, Proceedings of a Symposium Organised by the FAO and IAEA, 19–23 October 1992, Vienna, Austria, IAEA, Vienna, Austria, pp. 269–284.Google Scholar
  114. Toledo J., Rull J., Oropeza A., Hernández E., Liedo P. (2004) Irradiation of Anastrepha obliqua (Diptera: Tephritidae) revisited: optimizing sterility induction, J. Econ. Entomol. 97, 383–389.PubMedGoogle Scholar
  115. Tween G. (2002) MOSCAMED-Guatemala: an evolution of ideas, in: Barnes B.N. (Ed.), Proceedings of the 6th International Symposium on Fruit Flies of Economic Importance, 6–10 May 2002, Stellenbosch, South Africa, Isteg Scientific Publications, Irene, South Africa, pp. 119–126.Google Scholar
  116. US Working Group on the Food Crisis (2009) http://www.usfoodcrisisgroup.org/.
  117. Vale G.A., Torr S.J. (2005) User-friendly models of the costs and efficacy of tsetse control: application to sterilizing and insecticidal techniques, Med. Vet. Entomol. 19, 293–305.PubMedGoogle Scholar
  118. Van Borstel R.C. (1962) Effects of radiation on germ cells of insects: dominant lethals, gamete inactivation and gonial-cell killing, in: Radiation and Radioisotopes Applied to Insects of Agricultural Importance, Proceedings of a Symposium organised by FAO/IAEA, Athens, IAEA, Vienna, Austria, pp. 367–384.Google Scholar
  119. Van der Vloedt A.M.V., Taher M., Tenabe S.O. (1978) Effect of gamma radiation on the tsetse fly Glossina palpalis palpalis (Rob. Desv.) (Diptera: Glossinidae) with observations on the reproductive biology, Int. J. Appl. Radiat. Isot. 29, 713–716.PubMedGoogle Scholar
  120. van Driesche R., Hoddle M., Center T. (2008) Control of pests and weeds by natural enemies, Wiley-Blackwell, USA.Google Scholar
  121. van Lenteren J.C., Bale J., Bigler F., Hokkanen H.M.T., Loomans A.J.M. (2006) Assessing risks of releasing exotic biological control agents of arthropod pests, Annu. Rev. Entomol. 51, 609–634.PubMedGoogle Scholar
  122. Vargas-Terán M., Hofmann H.C., Tweddle N.E. (2005) Impact of screwworm eradication programmes using the sterile insect technique, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 629–650.Google Scholar
  123. Vreysen M.J.B. (1995) Radiation induced sterility to control tsetse flies. The effect of ionising radiation and hybridisation on tsetse biology and the use of the sterile insect technique in integrated tsetse control, Ph.D. dissertation, Wageningen Agricultural University, Wageningen, The Netherlands.Google Scholar
  124. Vreysen M.J.B. (2005) Monitoring sterile and wild insects in areawide integrated pest management programmes, in: Dyck V.A., Hendrichs J., Robinson A.S. (Eds.), Sterile insect technique. Principles and practice in area-wide integrated pest management, Springer, Dordrecht, The Netherlands, pp. 325–361.Google Scholar
  125. Vreysen M.J.B., Van der Vloedt A.M.V. (1995) Radiation sterilisation of Glossina tachinoides Westw. pupae: 1. The effect of dose fractionation and nitrogen during irradiation in the mid-pupal phase, Rev. Elev. Méd. Vét. Pays Trop. 48, 45–51.Google Scholar
  126. Vreysen M.J.B., Barclay H.J., Hendrichs J. (2006a) Modeling of preferential mating in area-wide control programs that integrate the release of strains of sterile males-only or both sexes, Ann. Entomol. Soc. Am. 99, 607–616.Google Scholar
  127. Vreysen M.J.B., Hendrichs J., Enkerlin W. (2006b) The sterile insect technique as a component of sustainable area-wide integrated pest management of selected horticultural insect pests, J. Fruit Ornam. Plant Res. 14, 107–131.Google Scholar
  128. Vreysen M.J.B., Gerardo-Abaya J., Cayol J.P. (2007b) Lessons from area-wide integrated pest management (AW-IPM) programmes with an SIT component: an FAO/IAEA perspective, in: Vreysen M.J.B., Robinson A.S., Hendrichs J. (Eds.), Area-wide control of insect pests. From research to field implementation, Springer, Dordrecht, The Netherlands, pp. 723–744.Google Scholar
  129. Vreysen M.J.B., Robinson A.S., Hendrichs J. (2007a) Area-wide control of insect pests, From research to field implementation, Springer, Dordrecht, The Netherlands.Google Scholar
  130. Vreysen M.J.B., Saleh K.M., Ali M.Y., Abdullah M.A., Zhu Z-R., Juma K.G., Dyck V.A., Msangi A.R., Mkonyi P.A., Feldmann H.U. (2000) Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja (Zanzibar), using the sterile insect technique, J. Econ. Entomol. 93, 123–135.PubMedGoogle Scholar
  131. Vreysen M.J.B., Van der Vloedt A.M.V., Barnor H. (1996) Comparative gamma radiation sensitivity of Glossina tachinoides Westw., Glossina fuscipes fuscipes Newst. and Glossina brevipalpis Newst. (Diptera, Glossinidae), Int. J. Radiat. Biol. 69, 67–74.PubMedGoogle Scholar
  132. Wajnberg E., Scott J.K., Quimby P. (2001) Evaluating indirect ecological effects of biological control, CABI Publishing, CAB International, Oxon, UK.Google Scholar
  133. Walters M.L., Staten R.T., Roberson R.C. (2000) Pink bollworm integrated management using sterile insects under field trial conditions, Imperial Valley, California, in: Tan K.H. (Ed.), Area-Wide Control of Fruit Flies and Other Insect Pests, Proceedings of an International Conference on Area-Wide Control of Insect Pests, and the 5th International Symposium on Fruit Flies of Economic Importance, 28 May–5 June 1998, Penang, Malaysia, Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia, pp. 201–206.Google Scholar
  134. Wong T.T.Y., Ramadan M.M., Herr J.C., McInnis D.O. (1992) Suppression of the Mediterranean fruit fly population with concurrent parasitoid and sterile fly releases in Kula, Maui, Hawaii, J. Econ. Entomol. 85, 1671–1681.Google Scholar
  135. Wyss J. (2000) Screwworm eradication in the Americas — an overview, in: Tan K.H. (Ed.), Area-Wide Control of Fruit Flies and Other Insect Pests, Proceedings of an International Conference on Area-Wide Control of Insect Pests, and the 5th International Symposium on Fruit Flies of Economic Importance, 28 May–5 June 1998, Penang, Malaysia, Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia, pp. 79–86.Google Scholar
  136. Zapater M.C., Andiarena C.E., Pérez Camargo G., Bartoloni N. (2009) Use of irradiated Musca domestica pupae to optimize mass rearing and commercial shipment of the parasitoid Spalangia endius (Hymenoptera: Pteromalidae), Bio. Sci. Tech. 19,S1, 261–270.Google Scholar
  137. Zeddies J., Schaab R.P., Neuenschwander P., Herren H.R. (2001) Economics of biological control of cassava mealybug in Africa, Agric. Econ. 24, 209–219.Google Scholar

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© INRA and Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Entomology Unit, FAO/IAEA Agriculture and Biotechnology LaboratoryJoint FAO/IAEA ProgrammeViennaAustria

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