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Transgenic Arthropods for Pest Management Programs: Risks and Realities

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Abstract

The ability to genetically engineer arthropods using recombinant DNA meopens new opportunities for improving pest management programs but also creates new responsibilities, including evaluation of the potential risks of releasing transgenic arthropods into the environment. It is now becoming easier to transform diverse species of arthropods by a variety of recombinant DNA methods. Useful genes and genetic regulatory elements are being identified for pest arthropods, but less effort is being expended to identify genes that could improve the efficacy of beneficial arthropods. A transgenic strain of the natural enemy Metaseiulus (= Typhlodromus or Galendromus) occidentalis (Acari: Phytoseiidae) was developed using a method termed maternal microinjection. This transgenic strain was released into an experimental site on the campus of the University of Florida in 1996 after extensive reviews by the University of Florida Biosafety Committee, Florida Department of Agriculture and Consumer Services, United States Department of Agriculture Animal and Plant Health Inspection Service, and the United States Fish and Wildlife Service. The short term releases established a precedent for releasing a transgenic arthropod but, at present, no guidelines are available that would allow transgenic arthropods to be released permanently into the environment. Several scientific, environmental, and policy issues must be resolved before transgenic pests or beneficial arthropods can be deployed in practical pest management programs.

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References

  • Abbott, A. 1996. Greens attack transgenic plant trials. Nature 382: 746.

    Google Scholar 

  • Anon. 1999a. Briefing GM Crops. Assessing the threat to biodiversity on the farm. Nature 398: 654.

  • Anon. 1999b. GM foods debate needs a recipe for restoring trust. Nature 398: 639.

  • Armstrong, J.L., Wood, N.D. and Porteous, L.A. 1990. Transconjugation between bacteria in the digestive tract of the cutworm Peridroma saucia. Appl. Environ. Microbiol. 56: 1492–1493.

    Google Scholar 

  • Arnault, C. and Dufournel, I. 1994. Genome and stresses: reactions against aggressions, behavior of transposable elements. Genetica 93: 149–160.

    PubMed  Google Scholar 

  • Ashburner, M., Hoy, M.A. and Peloquin, J. 1998. Transformation of arthropods-research needs and long term prospects. Insect Mol. Biol. 7: 201–213.

    PubMed  Google Scholar 

  • Asner, M. 1990. Public relations: the scientist and the public, the government, and the media. In: Agricultural Biotechnology. Introduction to Field Testing, H.G. Purchase and D.R. MacKenzie (eds), p. 35, Office of Agricultural Biotechnology, U.S. Department of Agriculture.

  • Beard, C.B., Mason, P.W., Aksoy, S., Tesh, R.B. and Richards, F.F. 1992. Transformation of an insect symbiont and expression of a foreign gene in the Chagas' disease vector Rhodnius prolixus. Amer. J. Trop. Med. Hyg. 46: 195–200.

    Google Scholar 

  • Beckendorf, S.K. and Hoy, M.A. 1985. Genetic improvement of arthropod natural enemies through selection, hybridization or genetic engineering techniques. In: Biological Control in Agricultural IPM Systems, M.A. Hoy and D.C. Herzog (eds), pp. 167–187, Academic, Orlando.

    Google Scholar 

  • Britten, R.J. 1997. Mobile elements inserted in the distant past have taken on important functions. Gene 205: 177–182.

    PubMed  Google Scholar 

  • Brookfield, J.F.Y. 1996. Models of the spread of non-autonomous selfish transposable elements when transposition and fitness are coupled. Genet. Res. Camb. 67: 199–209.

    Google Scholar 

  • Brookfield, J.F.Y. and Badge, R.M. 1997. Population genetics models of transposable elements. Genetica 100: 281–294.

    PubMed  Google Scholar 

  • Butler, D., Reichhardt, T., Abbott, A., Dickson, D. and Saegusa, A. 1999. Long-term effect of GM crops serves up food for thought. Nature 398: 651–653.

    PubMed  Google Scholar 

  • Carareto, C.M.A., Kim,W., Wojciechowski, M.F., O'Grady, P., Prokchorova, A.V., Silva, J.C. and Kidwell, M.G. 1997. Testing transposable elements as genetic drive mechanisms using Drosophila P element constructs as a model system. Genetica 101: 13–33.

    PubMed  Google Scholar 

  • Caprio, M.A. and Hoy, M.A. 1994. Metapopulation dynamics affect resistance development in a predatory mite. J. Econ. Entomol. 87: 525–534.

    Google Scholar 

  • Caprio, M. and Hoy, M.A. 1995. Premating isolation in a simulation model generates frequency-dependent selection and alters establishment rates of resistant natural enemies. J. Econ. Entomol. 88: 205–212.

    Google Scholar 

  • Caprio, M.A., Hoy, M.A. and Tabashnik, B.E. 1991. Model for implementing a genetically improved strain of a parasitoid. Amer. Entomol. 37: 232–239.

    Google Scholar 

  • Cohen, A.C., Nordlund, D.A. and Smith, R.A. 1999. Mass rearing of entomophagous insects and predaceous mites: are the bottlenecks biological, engineering, economic, or cultural? Biocontrol News and Inform. 20: 85N-90N.

    Google Scholar 

  • Droge, M., Puhler, A. and Selbitschka, W. 1998. Horizontal gene transfer as a biosafety issue: A natural phenomenon of public concern. J. Biotechnol. 64: 75–90.

    PubMed  Google Scholar 

  • Edwards, O.R. and Hoy, M.A. 1993. Polymorphism in two parasitoids detected using random amplified polymorphic DNA polymerase chain reaction. Biol. Contr. 3: 243–257.

    Google Scholar 

  • Edwards, O.R. and Hoy, M.A. 1995a. Monitoring laboratory and field biotypes of the walnut aphid parasite, Trioxys pallidus, in population cages using RAPD-PCR. Biocontrol Sci. Technol. 5: 313–327.

    Google Scholar 

  • Edwards, O.R. and Hoy, M.A. 1995b. Random amplified polymorphic DNA markers to monitor laboratory-selected, pesticide-resistant Trioxys pallidus (Hymenoptera: Aphidiidae) after release into three California walnut orchards. Environ. Entomol. 24: 487–496.

    Google Scholar 

  • Ehler, L.E. 1991. Planned introductions in biological control. In: Assessing Ecological Risks of Biotechnology, L.R. Ginzburg (ed.), pp. 231–239, Butterworth-Heinemann, Boston.

    Google Scholar 

  • Ertle, L.R. 1993. What quarantine does and what the collector needs to know. In: Steps in Classical Biological Control, R.G. van Driesche and T.S. Bellows, Jr. (eds), pp. 53–65, Thomas Say Publ. Entomol., Entomol. Soc. Amer., Lanham, MD.

    Google Scholar 

  • Ewell, J.J., O'Dowd, D.J., Bergelson, J., Daehler, C.C., D'Antonio, C.M., Gomez, L.D., Gordon, D.R., Hobbs, R.J., Holt, A., Hopper, K.R., Hughes, C.E., LaHart, M., Leakey, R.R.B., Lee, W.G., Loope, L.L., Lorence, D.H., Louda, S.M., Lugo, A.E., McEvoy, P.B., Richardson, D.M. and Vitousek, P.M. 1999. Deliberate introductions of species: research needs. Benefits can be reaped, but risks are high. BioScience 49: 619–630.

    Google Scholar 

  • Fisher, T.W. 1973. Quarantine handling of entomophagous insects. In: Biological Control of Insect Pests and Weeds, P. DeBach (ed.), pp. 53–65, Chapman and Hall, London.

    Google Scholar 

  • Goldberg, R., Rissler, J., Shand, H. and Hassebrook, C. 1990. Biotechnology's Bitter Harvest: Herbicide-tolerant crops and the threat to sustainable agriculture. Rept. Biotech. Working Group, 73 pp.

  • Goodman, B. 1993. Research community swats grasshopper control trial. Science (Washington, DC) 260: 887.

    Google Scholar 

  • Gubler, D.J. 1993. Release of exotic genomes. J. Amer. Mosq. Contr. Assoc. 9: 104.

    Google Scholar 

  • Gueiros-Filho, F.J. and Beverley, S.M. 1997. Trans-kingdom transposition of the Drosophila element mariner within the protozoan Leishmania. Science 276: 1716–1719.

    PubMed  Google Scholar 

  • Handler, A.M., McCombs, S.D., Fraser, M.J. and Saul, S.H. 1998. The lepidopteran transposon vector, PiggyBac, mediates germ-line transformation in the Mediterranean fruit fly. Proc. Natl. Acad. Sci. USA. 95: 7520–7525.

    PubMed  Google Scholar 

  • Hanski, I. 1998. Metapopulation dynamics. Nature 396: 41–49.

    Google Scholar 

  • Hatch, T. 1998. Chlamydia: Old ideas crushed, new mysteries bared. Science 282: 638–639.

    PubMed  Google Scholar 

  • Headley, J.C. and Hoy, M.A. 1987. Benefit/cost analysis of an integrated mite management program for almonds. J. Econ. Entomol. 80: 555–559.

    Google Scholar 

  • Henikoff, S. 1998. Conspiracy of silence among repeated transgenes. BioEssays 20: 532–535.

    PubMed  Google Scholar 

  • Hess, R.T. and Hoy, M.A. 1982. Microorganisms associated with the spider mite predator Metaseiulus (D Typhlodromus) occidentalis: electron microscope observations. J. Invert. Pathol. 40: 98–106.

    Google Scholar 

  • Houck, M.A., Clark, J.B., Peterson, K.R. and Kidwell, M.G. 1991. Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science 253: 1125–1129.

    PubMed  Google Scholar 

  • Howarth, F.G. 1991. Environmental impacts of classical biological control. Annu. Rev. Entomol. 36: 485–509.

    Google Scholar 

  • Hoy, M.A. 1976. Genetic improvement of insects: fact or fantasy. Environ. Entomol. 5: 833–839.

    Google Scholar 

  • Hoy, M.A. 1982. Aerial dispersal and field efficacy of a genetically improved strain of the spider mite predator Metaseiulus occidentalis. Entomol. Exp. Appl. 32: 205–212.

    Google Scholar 

  • Hoy, M.A. 1984. Genetic improvement of a biological control agent: multiple pesticide resistance and nondiapause in Metaseiulus occidentalis (Nesbitt) (Phytoseiidae). In: Acarology VI, D.A. Griffiths and C.E. Bowman (eds), Vol. 2, pp. 673–679, Ellis Horwood, Chichester.

  • Hoy, M.A. 1985a. Almonds: integrated mite management for California almond orchards. In: Spider Mites, Their Biology, Natural Enemies, and Control, W. Helle and M.W. Sabelis (eds), Vol. 1B, pp. 299–310, Elsevier, Amsterdam.

  • Hoy, M.A. 1985b. Recent advances in genetics and genetic improvement of the Phytoseiidae. Annu. Rev. Entomol. 30: 345–370.

    Google Scholar 

  • Hoy, M.A. 1990. Pesticide resistance in arthropod natural enemies: variability and selection responses. In: Pesticide Resistance in Arthropods, R.T. Roush and B.E. Tabashnik (eds), pp. 203–236, Chapman and Hall, New York.

    Google Scholar 

  • Hoy, M.A. 1992a. Commentary: Biological control of arthropods: genetic engineering and environmental risks. Biological Control 2: 166–170.

    Google Scholar 

  • Hoy, M.A. 1992b. Criteria for release of genetically improved phytoseiids: an examination of the risks associated with release of biological control agents. Exp. Appl. Acarol. 14: 393–416.

    Google Scholar 

  • Hoy, M.A. 1994. Insect Molecular Genetics. An Introduction to Principles and Applications. Academic Press, San Diego, 540 pp.

    Google Scholar 

  • Hoy, M.A. 1995. Impact of risk analyses on pest management programs employing transgenic arthropods. Parasitology Today 11: 229–232.

    Google Scholar 

  • Hoy, M.A. and Cave, F.E. 1985. Mating behavior in four strains of Metaseiulus occidentalis (Acari: Phytoseiidae). Ann. Entomol. Soc. Amer. 78: 588–593.

    Google Scholar 

  • Hoy, M.A. and Cave, F.E. 1988. Premating and postmating isolation among populations of Metaseiulus occidentalis (Nesbitt) (Acarina: Phytoseiidae). Hilgardia 56(6): 1–20.

    Google Scholar 

  • Hoy, M.A. and Cave, F.E. 1991. Genetic improvement of a parasitoid: response of Trioxys pallidus to laboratory selection with azinphosmethyl. Biocontrol Sci. Tech. 1: 31–41.

    Google Scholar 

  • Hoy, M.A. and Knop, N.F. 1981. Selection for and genetic analysis of permethrin resistance in Metaseiulus occidentalis: genetic improvement of a biological control agent. Entomol. Exp. Appl. 30: 10–18.

    Google Scholar 

  • Hoy, M.A., Groot, J.J.R. and van de Baan, H.E. 1985. Influence of aerial dispersal on persistence and spread of pesticide-resistant Metaseiulus occidentalis in California almond orchards. Entomol. Exp. Appl. 37: 17–31.

    Google Scholar 

  • Hoy, M.A., Cave, F.E., Beede, R.H., Grant, J., Krueger, W.H., Olson, W.H., Spollen, K.M., Barnett,W.W. and Hendricks, L.C. 1990. Release, dispersal, and recovery of a laboratoryselected strain of the walnut aphid parasite Trioxys pallidus (Hymenoptera: Aphidiidae) resistant to azinphosmethyl. J. Econ. Entomol. 83: 89–96.

    Google Scholar 

  • Hoy, M.A., Gaskalla, R.D., Capinera, J.L. and Keierleber, C. 1997. Laboratory containment of transgenic arthropods. Amer. Entomol. 43: 206–209, 255–256.

    Google Scholar 

  • Hurst, G.D.D., Hammarton, T.C., Bandi, C., Majerus, T.M.O., Bertrand, D. and Majerus, M.E.N. 1997. The diversity of inherited parasites of insects: the male-killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria. Genet. Res. Camb. 70: 1–6.

    Google Scholar 

  • Jehle, J.A., Nickel, A., Vlak, J.M. and Backhaus, H. 1998. Horizontal escape of the novel Tc1-like lepidopteran transposon TCp3.2 into Cydia pomonella granulovirus. J. Mol. Evol. 46: 215–224.

    PubMed  Google Scholar 

  • Jeltsch, A. and Pingoud, A. 1996. Horizontal gene transfer contributes to the wide distribution and evolution of type II restriction-modification systems. J. Mol. Evol. 42: 91–96.

    PubMed  Google Scholar 

  • Jeyaprakash, A. and Hoy, M.A. 1995. Complete sequence of a mariner transposable element from the predatory mite Metaseiulus occidentalis isolated by an inverse PCR approach. Insect Mol. Biol. 4: 31–39.

    PubMed  Google Scholar 

  • Jeyaprakash, A., Lopez, G. and Hoy, M.A. 1998. Extrachromosomal plasmid DNA transmission and amplification in Metaseiulus occidentalis (Acari: Phytoseiidae) transformants generated by maternal microinjection. Ann. Entomol. Soc. Amer. 91: 730–736.

    Google Scholar 

  • Johanowicz, D.J. and Hoy, M.A. 1996. Wolbachia in a predator-prey system: 16S ribosomal DNA analysis of two phytoseiids (Acari: Phytoseiidae) and their prey (Acari: Tetranychidae). Ann. Entomol. Soc. Amer. 89(3): 435–441.

    Google Scholar 

  • Johanowicz, D.L. and Hoy, M.A. 1998. Experimental induction and termination of nonreciprocal reproductive incompatibilities in a parahaploid mite. Entomol. Exp. Appl. 87: 51–58.

    Google Scholar 

  • Johanowicz, D.L. and Hoy, M.A. 1999. Wolbachia infection dynamics in experimental populations of Metaseiulus occidentalis. Entomol. Exp. Appl. (in press).

  • Kaiser, J. 1999. Stemming the tide of invading species. Science 285: 1836–1839.

    Google Scholar 

  • Kidwell, M.G. and Lisch, D.R. 1997. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 94: 7704–7711.

    PubMed  Google Scholar 

  • Lawrence, J.G. and Ochman, H. 1998. Molecular archaeology of the Escherichia coli genome. Proc. Natl. Acad. Sci. USA 95: 9413–9417.

    PubMed  Google Scholar 

  • Li, J. and Hoy, M.A. 1996. Adaptability and efficacy of transgenic and wild-type Metaseiulus occidentalis (Acari: Phytoseiidae) compared as part of a risk assessment. Exp. Appl. Acarol. 20: 563–574.

    Google Scholar 

  • Lundholm, B. and Stackerud, M. (eds). 1980. Environmental protection and biological forms of control of pest organisms. Ecol. Bull. (Stockholm) 31: 1–171.

    Google Scholar 

  • Macilwain, C. 1999. U.S. sets up 'round-table' talks with scientists. Nature 398: 641.

    Google Scholar 

  • Malakoff, D. 1999. Fighting fire with fire. Science 285: 1841–1843.

    Google Scholar 

  • Mazel, D., Dychinco, B., Webb, B.A. and Davies, J. 1998. A distinctive class of integron in the Vibrio cholerae genome. Science 280: 605–608.

    PubMed  Google Scholar 

  • McDermott, G.J. and Hoy, M.A. 1997. Persistence and containment of Metaseiulus occidentalis (Acari: Phytoseiidae) in Florida: risk assessment for possible releases of transgenic strains. Fla. Entomol. 80: 42–53.

    Google Scholar 

  • Medigue, C., Rouxel, T., Vigier, P., Henaut, A. and Danchin, A. 1991. Evidence for horizontal gene-transfer in Escherichia coli speciation. J. Mol. Biol. 222: 851–856.

    PubMed  Google Scholar 

  • Miller, W.J., McDonald, J.F. and Pinsker, W. 1997. Molecular domestication of mobile elements. Genetica 100: 261–270.

    PubMed  Google Scholar 

  • NABC. 1994. Agricultural Biotechnology and the Public Good. National Agricultural Biotechnology Council Report 6, Ithaca, NY, 213 pp.

  • NABC. 1997. Resource Management in Challenged Environments. National Agricultural Biotechnology Council Report 9, Ithaca, NY, 167 pp.

  • Nielsen, K.M., Bones, A.M., Smalla, K. and van Elsas, J.D. 1998. Horizontal gene transfer from transgenic plants to terrestrial bacteria-a rare event? FEMS Microbiol. Rev. 22: 79–103.

    PubMed  Google Scholar 

  • O'Brochta, D.A. and Handler, A.M. 1988. Mobility of P elements in drosophilids and nondrosophilids. Proc. Natl. Acad. Sci. USA 85: 1068–1080.

    Google Scholar 

  • OECD. 1998. Issues and recommendations from a workshop on Safe Utilization of New Organisms in Biological Control, Montreal, Canada, September 1998. Phytoprotection 79(Suppl): 1–155.

    Google Scholar 

  • Palca, J. 1988. Mosquito release blocked by fearful California residents. Nature 335: 7.

    Google Scholar 

  • Pennisi, E. 1998. Versatile gene uptake system found in cholera bacterium. Science 280: 521–522.

    PubMed  Google Scholar 

  • Petrov, D.A., Schutzman, J.L., Hartl, D.L. and Lozovskaya, E.R. 1995. Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc. Natl. Acad. Sci. USA 92: 8050–8054.

    PubMed  Google Scholar 

  • Presnail, J.K. and Hoy, M.A. 1992. Stable genetic transformation of a beneficial arthropod, Metaseiulus occidentalis (Acari: Phytoseiidae), by a microinjection technique. Proc. Natl. Acad. Sci. USA 89: 7732–7736.

    PubMed  Google Scholar 

  • Presnail, J.K. and Hoy, M.A. 1994. Transmission of injected DNA sequences to multiple eggs of Metaseiulus occidentalis and Amblyseius finlandicus (Acari: Phytoseiidae) following maternal microinjection. Exp. Appl. Acarol. 18: 319–330.

    PubMed  Google Scholar 

  • Presnail, J.K. and Hoy, M.A. 1996. Maternal microinjection of the endoparasitoid Cardiochiles diaphaniae (Hymenoptera: Braconidae). Ann. Entomol. Soc. Amer. 89: 576–580.

    Google Scholar 

  • Presnail, J.K., Jeyaprakash, A., Li, J. and Hoy, M.A. 1997. Genetic analysis of four lines of Metaseiulus occidentalis (Nesbitt) (Acari: Phytoseiidae) transformed by maternal microinjection. Ann. Entomol. Soc. Amer. 90: 237–245.

    Google Scholar 

  • Purchase, H.G. and MacKenzie, D.R. 1990. Agricultural Biotechnology Introduction to Field Testing. Office of Agricultural Biotechnology, USDA, Washington, DC, 58 pp.

    Google Scholar 

  • Rasmussen, P.E., Goulding, K.W.T., Brown, J.R., Grace, P.R., Janzen, H.H. and Korschens, M. 1998. Long-term agroecosystem experiments: assessing agricultural sustainability and global change. Science 282: 893–896.

    PubMed  Google Scholar 

  • Robertson, H.M. 1997. Multiple mariner transposons in flatworms and hydras are related to those of insects. J. Hered. 88: 195–201.

    Google Scholar 

  • Robertson, H.M. and Zumpano, K.L. 1997. Molecular evolution of an ancient mariner transposon, Hsmar1, in the human genome. Gene 205: 203–217.

    PubMed  Google Scholar 

  • Roush, R.T. and Hoy, M.A. 1981a. Genetic improvement of Metaseiulus occidentalis: selection with methomyl, dimethoate, and carbaryl and genetic analysis of carbaryl resistance. J. Econ. Entomol. 74: 138–141.

    Google Scholar 

  • Roush, R.T. and Hoy, M.A. 1981b. Laboratory, glasshouse, and field studies of artificially selected carbaryl resistance in Metaseiulus occidentalis. J. Econ. Entomol. 74: 142–147.

    Google Scholar 

  • Ruesink, J.L., Parker, I.M., Groom, M.J. and Kareiva, P.M. 1995. Reducing the risks of nonindigenous species introductions: guilty until proven innocent. BioScience 45: 465–477.

    Google Scholar 

  • Schlimme, W., Marchiani, M., Hanselmann, K. and Jenni, B. 1997. Gene transfer between bacteria within digestive vacuoles of protozoa. FEMS Microbiol. Ecol. 23: 239–247.

    Google Scholar 

  • Simberloff, D. 1992. Conservation of pristine habitats and unintended effects of biological control. In: Selection criteria and ecological consequences of importing natural enemies, W.C. Kauffman and J.E. Nechols (eds), pp. 103–117, Proc. Thomas Say Publ. Entomol., Lanham, MD.

    Google Scholar 

  • Simberloff, D. and Stilling, P. 1996. How risky is biological control? Ecology 77: 1965–1974.

    Google Scholar 

  • Smaglik, P. 1999. Drosophila sequenced-now the tricky part. The Scientist 13(19): 7.

    Google Scholar 

  • Thomas, M.B. and Willis, A.J. 1999. Biocontrol-risky but necessary? TREE 13: 325–328.

    Google Scholar 

  • Tiedje, J.M., Colwell, R.K., Grossman, Y.L., Hodson, R.E., Lenski, R.E., Mack, R.N. and Regal, P.J. 1989. The planned introduction of genetically engineered organisms: ecological considerations and recommendations. Ecology 70: 298–315.

    Google Scholar 

  • Turrelli, M., Hoffman, A.A. and McKechnie, S.W. 1992. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132: 713–723.

    PubMed  Google Scholar 

  • Watanabe, K. and Sato, M. 1998. Plasmid-mediated gene transfer between insect-resident bacteria, Enterobacter cloacae, and plant-epiphytic bacteria, Erwinia herbicola, in guts of silkworm larvae. Current Microbiol. 37: 352–355.

    PubMed  Google Scholar 

  • Watanabe, K., Hara, W. and Sato, M. 1998. Evidence for growth of strains of the plant epiphytic bacterium Erwinia herbicola and transconjugation among the bacterial strains in guts of the silkworm Bombyx mori. J. Invert. Pathol. 72: 104–111.

    Google Scholar 

  • Werren, J.H. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 432: 587–609.

    Google Scholar 

  • Williams, R.J. and Heymann, D.L. 1998. Containment of antibiotic resistance. Science279: 1153–1154.

    PubMed  Google Scholar 

  • Wilson, L.T., Hoy, M.A., Zalom, F.G. and Smilanick, J.M. 1984. Sampling mites in almonds: I.Within-tree distribution and clumping patterns of mites with comments on predator-prey interactions. Hilgardia 52(7): 1–13.

    Google Scholar 

  • Witte,W. 1998. Medical consequences of antibiotic use in agriculture. Science 279: 996–997.

    PubMed  Google Scholar 

  • Wood, S.N. and Thomas, M.B. 1999. Super-sensitivity to structure in biological models. Proc. R. Soc. Lond. B 266: 575–570.

    Google Scholar 

  • Zalom, F.G., Hoy, M.A., Wilson, L.T. and Barnett, W.W. 1984. Sampling mites in almonds: II. Presence-absence sequential sampling for Tetranychus mite species. Hilgardia 52(7): 14–24.

    Google Scholar 

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Hoy, M.A. Transgenic Arthropods for Pest Management Programs: Risks and Realities. Exp Appl Acarol 24, 463–495 (2000). https://doi.org/10.1023/A:1006401225083

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