Philosophical Transactions of the Royal Society B: Biological Sciences
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Integrated pest management: the push–pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry

    This paper describes the ‘push–pull’ or ‘stimulo-deterrent diversionary’ strategy in relation to current and potential examples from our own experiences. The push–pull effect is established by exploiting semiochemicals to repel insect pests from the crop (‘push’) and to attract them into trap crops (‘pull’). The systems exemplified here have been developed for subsistence farming in Africa and delivery of the semiochemicals is entirely by companion cropping, i.e. intercropping for the push and trap cropping for the pull. The main target was a series of lepidopterous pests attacking maize and other cereals. Although the area given to the cereal crop itself is reduced under the push–pull system, higher yields are produced per unit area. An important spin-off from the project is that the companion crops are valuable forage for farm animals. Leguminous intercrops also provide advantages with regard to plant nutrition and some of the trap crops help with water retention and in reducing land erosion. A major benefit is that certain intercrop plants provide dramatic control of the African witchweed (striga). Animal husbandry forms an essential part of intensive subsistence agriculture in Africa and developments using analogous push–pull control strategies for insect pests of cattle are exemplified.

    References

    • Agelopoulos N, et al.1999Exploiting semiochemicals in insect control. Pest. Sci. 55, 225–235.doi:10.1002/(SICI)1096-9063(199903)55:3<225::AID-PS887>3.0.CO;2-7. . CrossrefGoogle Scholar
    • Arimura G, Ozawa R, Kugimiya S, Takabayashi J& Bohlmann J. 2004Herbivore-induced defense response in a model legume: two-spotted spider mites, Tetranychus urticae, induce emission of (E)-β-ocimene and transcript accumulation of (E)-β-ocimene synthase in Lotus japonicus. Plant Physiol. 135, 1976–1983.doi:10.1104/pp.104.042929. . Crossref, PubMed, ISIGoogle Scholar
    • Birkett M.A, et al.2000New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc. Natl Acad. Sci. USA. 97, 9329–9334.doi:10.1073/pnas.160241697. . Crossref, PubMed, ISIGoogle Scholar
    • Birkett M.A, et al.2004The role of volatile semiochemicals in mediating host location and selection by nuisance and disease-transmitting cattle flies. Med. Vet. Entomol. 18, 313–322.doi:10.1111/j.0269-283X.2004.00528.x. . Crossref, PubMed, ISIGoogle Scholar
    • Boller, E. F. & Hurter, J. 1998 The marking pheromone of the cherry fruit fly: a novel non-toxic and ecologically safe technique to protect cherries against cherry fruit fly infestation. In Proc. Second Int. Symp. on Insect Pheromones, Wageningen, The Netherlands, 30 March3 April 1998. Google Scholar
    • Borlaug, N. E. 2004 President's Address. Sasakawa Africa association, annual report 20032004, 1–2. (Writers and eds: A. McNab & C. Dowswell). Google Scholar
    • Bouma M& Rowland M. 1995Failure of passive zooprophylaxis: cattle ownership in Pakistan is associated with a higher prevalence of malaria. Trans. R. Soc. Trop. Med. Hyg. 89, 351–353.doi:10.1016/0035-9203(95)90004-7. . Crossref, PubMed, ISIGoogle Scholar
    • Brightwell R, Dransfield R.D& Kyorku C.A. 1991Development of a low-cost tsetse trap and odour baits for Glossina pallidipes and G. longipennis in Kenya. Med. Vet. Entomol. 5, 153–164. Crossref, PubMed, ISIGoogle Scholar
    • Brooks G.T& Roberts T.R. 1999Cambridge, UK:Royal Society of Chemistry. Google Scholar
    • Bruce T, Wadhams L.J& Woodcock C.M. 2005Insect host location: a volatile situation. Trends Plant Sci. 10, 269–274.doi:10.1016/j.tplants.2005.04.003. . Crossref, PubMed, ISIGoogle Scholar
    • Bruce-Chwatt L.J2nd edn1985London, UK:Heinemann. Google Scholar
    • Chamberlain K, Khan Z.R, Pickett J.A, Toshova T& Wadhams L.J. 2006Diel periodicity in the production of green leaf volatiles by wild and cultivated host plants of stemborer moths, Chilo partellus and Busseola fusca. J. Chem. Ecol. 32, 565–577.doi:10.1007/s10886-005-9016-5. . Crossref, PubMed, ISIGoogle Scholar
    • Dudareva N, Martin D, Kish C.M, Kolosova N, Gorenstein N, Fäldt J, Miller B& Bohlmann J. 2003(E)-β-Ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell. 15, 1227–1241.doi:10.1105/tpc.011015. . Crossref, PubMed, ISIGoogle Scholar
    • Fäldt J, Arimura G.I, Gershenzon J, Takabayashi J& Bohlmann J. 2003Functional identification of AtTPS03 as (E)-β-ocimene synthase: a monoterpene synthase catalyzing jasmonate- and wound-induced volatile formation in Arabidopsis thaliana. Planta. 216, 745–751. Crossref, PubMed, ISIGoogle Scholar
    • Frey M, et al.1997Analysis of a chemical plant defense mechanism in grasses. Science. 277, 696–699.doi:10.1126/science.277.5326.696. . Crossref, PubMed, ISIGoogle Scholar
    • Gatsby Charitable Foundation 2005 The quiet revolution: push-pull technology and African farmer. Gatsby Occasional Paper. The Gatsby Charitable Foundation, Allington House, London SW1E 5AE, UK. Google Scholar
    • Gikonyo N.K, Hassanali A, Njagi P.G.N& Saini R.K. 2000Behaviour of Glossina morsitans morsitans Westwood (Diptera: Glossindae) on waterbuck Kobus defasa Ruppel and feeding membranes smeared with waterbuck sebum indicates the presence of allomones. Acta Trop. 77, 295–303.doi:10.1016/S0001-706X(00)00153-4. . Crossref, PubMed, ISIGoogle Scholar
    • Gikonyo N.K, Hassanali A, Njagi P.G.N, Gitu P.M& Midiwo J.O. 2002Odour composition of preferred (buffalo and ox) and non-preferred (waterbuck) hosts of some savanna tsetse flies. J. Chem. Ecol. 28, 961–973.doi:10.1023/A:1015205716921. . Crossref, ISIGoogle Scholar
    • Gikonyo N.K, Hassanali A, Njagi P.G.N& Saini R.K. 2003Responses of Glossina morsitans morsitans to blends of electroantennographically active compounds in the odors of its preferred (buffalo and ox) and non-preferred (waterbuck) hosts. J. Chem. Ecol. 29, 2331–2345.doi:10.1023/A:1026230615877. . Crossref, PubMed, ISIGoogle Scholar
    • Glen D.M, Greaves M.P& Anderson H.M. 1995Chichester, UK:Wiley. Google Scholar
    • Gurr G.M, Wratten S.D& Altieri A. 2004Wallingford, UK:CAB International. Google Scholar
    • Hall D.R, Beevor P.S, Cork A, Nesbitt B.F& Vale G.A. 19841-Octen-3-ol: a potent olfactory stimulant and attractant for tsetse isolated from cattle odours. Insect Sci. Appl. 5, 153–163. ISIGoogle Scholar
    • Hardie J& Minks A.K. 1999Wallingford, UK:CAB International. Google Scholar
    • Hester R.E& Harrison R.M. 2005Cambridge, UK:Royal Society of Chemistry. Google Scholar
    • Howse P.E, Stevens I.D.R& Jones O.T. 1998London, UK:Chapman and Hall. Google Scholar
    • Jensen K.-M.V, Jespersen J.B, Birkett M.A, Pickett J.A, Thomas G, Wadhams L.J& Woodcock C.M. 2004Variation in the load of the horn fly, Haematobia irritans, in cattle herds is determined by the presence or absence of individual heifers. Med. Vet. Entomol. 18, 275–280.doi:10.1111/j.0269-283X.2004.00506.x. . Crossref, PubMed, ISIGoogle Scholar
    • Jones, O. T. 2002 An analysis of potential barriers to the commercial development of semiochemicals for crop protection. Defra deskop study. Google Scholar
    • Kato T, Sato S, Nakamura Y, Kaneko T, Asamizu E& Tabata S. 2003Structural analysis of a Lotus japonicus genome. V. Sequence features and mapping of sixty-four TAC clones which cover the 6.4 Mb regions of the genome. DNA Res. 10, 277–285.doi:10.1093/dnares/10.6.277. . Crossref, PubMed, ISIGoogle Scholar
    • Kfir R, Overholt W.A, Khan Z.R& Polaszek A. 2002Biology and management of economically important lepidopteran cereal stemborers in Africa. Annu. Rev. Entomol. 47, 701–731.doi:10.1146/annurev.ento.47.091201.145254. . Crossref, PubMed, ISIGoogle Scholar
    • Khan Z.R& Pickett J.AThe ‘push–pull’ strategy for stemborer management: a case study in exploiting biodiversity and chemical ecology. Ecological engineering for pest management: advances in habitat manipulation for arthropods, Gurr G.M, Wratten S.D& Altieri M.A. 2004pp. 155–164. Eds. Wallingford, UK:CAB International. Google Scholar
    • Khan Z.R& Polaszek AHost plants. African cereal stemborers: economic importance, taxonomy, natural enemies and control& Polaszek A. 1998pp. 3–10. Eds. Wallingford, UK:CAB International. Google Scholar
    • Khan Z.R, Chiliswa P, Ampong-Nyarko K, Smart L.E, Polaszek A, Wandera J& Mulaa M.AUtilisation of wild gramineous plants for the management of cereal stemborers in Africa. Insect Sci. Appl. 17, 1997a143–150. Google Scholar
    • Khan Z.R, et al.Intercropping increases parasitism of pests. Nature. 388, 1997b631–632.doi:10.1038/41681. . Crossref, ISIGoogle Scholar
    • Khan Z.R, Pickett J.A, Vandenberg J, Wadhams L.J& Woodcock C.M. 2000Exploiting chemical ecology and species diversity: stemborer and Striga control for maize and sorghum in Africa. Pest Man. Sci. 56, 957–962.doi:10.1002/1526-4998(200011)56:11<957::AID-PS236>3.0.CO;2-T. . Crossref, ISIGoogle Scholar
    • Khan Z.R, Pickett J.A, Wadhams L.J& Muyekho F. 2001Habitat management strategies for the control of cereal stemborers and Striga in maize in Kenya. Insect Sci. Appl. 21, 375–380. Google Scholar
    • Khan Z.R, Hassanali A, Overholt W, Khamis T.M, Hooper A.M, Pickett J.A, Wadhams L.J& Woodcock C.M. 2002Control of witchweed Striga hermonthica by intercropping with Desmodium spp. and the mechanism defined as allelopathic. J. Chem. Ecol. 28, 1871–1885.doi:10.1023/A:1020525521180. . Crossref, PubMed, ISIGoogle Scholar
    • Kouchi H, et al.2004Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus. DNA Res. 11, 263–274.doi:10.1093/dnares/11.4.263. . Crossref, PubMed, ISIGoogle Scholar
    • Lamblin A.F.J, et al.2003MtDB, a database for personalized data mining of the model legume Medicago truncatula transcriptome. Nucleic Acids Res. 31, 196–201.doi:10.1093/nar/gkg119. . Crossref, PubMed, ISIGoogle Scholar
    • Matthes, M., Napier, J. A., Pickett, J. A. & Woodcock, C. M. 2003 New chemical signals in plant protection against herbivores and weeds. In Proc. BCPC Int. CongressCrop Science & Technology 2003, 1012 November, SECC Glasgow, 9C-4, pp. 1227–1236. Google Scholar
    • Midega C.A.O, Khan Z.R, Vandenberg J, Ogol C.K.P.O, Pickett J.A& Wadhams L.J. 2006Maize stemborer predator activity under ‘push–pull’ system and Bt-maize: a potential component in managing Bt-resistance. Int. J. Pest Man. 52, 1–10.doi:10.1080/09670870600558650. . Crossref, ISIGoogle Scholar
    • Miller J.R& Cowles R.S. 1990Stimulo-deterrent diversionary cropping: a concept and its possible application to onion maggot control. J. Chem. Ecol. 16, 3197–3212.doi:10.1007/BF00979619. . Crossref, PubMed, ISIGoogle Scholar
    • Nedorezov, L. V., Hassanali, A. & Sadykov, A. M. 2005 Individual-based model of mosquito choices up odour plumes to alternative hosts. In Proc. Fifth Eur. Conf. on Ecological Modelling (ed. A. S. Komarov), pp. 136–137. Google Scholar
    • Owaga M.L.A, Hassanali A& McDowell P.G. 1988The role of 4-cresol and 3-n-propylphenol in the attraction of tsetse to buffalo urine. Insect Sci. Appl. 9, 95–100. ISIGoogle Scholar
    • Pickett J.A& Poppy G.M. 2001Switching on plant genes by external chemical signals. Trends Plant Sci. 6, 137–139.doi:10.1016/S1360-1385(01)01899-4. . Crossref, PubMed, ISIGoogle Scholar
    • Pickett J.A, Wadhams L.J& Woodcock C.M. 1997Developing sustainable pest control from chemical ecology. Agric. Ecol. Environ. 64, 149–156.doi:10.1016/S0167-8809(97)00033-9. . Crossref, ISIGoogle Scholar
    • Pickett J.A, Rasmussen H.B, Woodcock C.M, Matthes M& Napier J.A. 2003Plant stress signalling: understanding and exploiting plant–plant interactions. Biochem. Soc. Trans. 31, 123–127. Crossref, PubMed, ISIGoogle Scholar
    • Powell W& Pickett J.A. 2003Manipulation of parasitoids for aphid pest management: progress and prospects. Pest Man. Sci. 59, 149–155.doi:10.1002/ps.550. . Crossref, PubMed, ISIGoogle Scholar
    • Pyke B, Rice M, Sabine B& Zalucki M. 1987The push–pull strategy—behavioural control of Heliothis. Aust. Cotton Grower. 4, 7–9. Google Scholar
    • Rebe M, Vandenberg J& McGeoch M.A. 2004Colonization of cultivated and indigenous graminaceous host plants by Busseola fusca (Fuller) (Lepidoptera: Noctuidae) and Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) under field conditions. Afr. Entomol. 12, 187–199. ISIGoogle Scholar
    • Royal Society policy statements and reports 2001 The use of genetically modified animals. Ref 05/01. Google Scholar
    • Royal Society policy statements and reports 2002 Genetically modified plants for food use and human health—an update. Ref 04/02. Google Scholar
    • Seyoum A, Balcha M, Balkew A.A& Gebre-Michael T. 2002Impact of cattle keeping on human biting rate of Anopheline mosquitoes and malaria transmission around Ziway, Ethiopia. East Afr. Med. J. 79, 485–490. PubMedGoogle Scholar
    • Smart L.E, Pickett J.A& Powell W. 1997Push–pull strategies for pest control. Grain Legumes. 15, 14–15. Google Scholar
    • Torr S.J, Mangwiro T.N.C& Hall D.R. 1996Responses of Glossina pallidipes (Diptera: Glossinidae) to synthetic repellents in the field. Bull. Entomol. Res. 86, 609–616. Crossref, ISIGoogle Scholar
    • Trumble J.T, Cardé R& Minks A. 1997pp. 397–410. Eds. London, UK:Chapman and Hall.ch. 35. Google Scholar
    • Trumble J.T& Alvarado-Rodriguez B. 1993Development and economic evaluation of an IPM program for fresh market tomato production in Mexico. Argric. Ecol. Envion. 43, 267–284.doi:10.1016/0167-8809(93)90091-3. . Crossref, ISIGoogle Scholar
    • Turlings T.C.J, Tumlinson J.H& Lewis W.J. 1990Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science. 250, 1251–1253.doi:10.1126/science.250.4985.1251. . Crossref, PubMed, ISIGoogle Scholar
    • Vale G.A, Lovemore D.F, Flint S& Cockbill G.F. 1988Odour-baited targets to control tsetse flies, Glossina spp. (Diptera: Glossindae), in Zimbabwe. Bull. Entomol. Res. 78, 31–49. Crossref, ISIGoogle Scholar
    • Van Emden H.F& Peakall D.BBeyond silent spring, integrated pest management and chemical safety. 1996London, UK:Chapman and Hall. Google Scholar
    • Wanzala W, Sika N.F.K, Gule S& Hassanali A. 2004Attractive and repellent host odours guide ticks to their respective feeding sites. Chemoecology. 14, 229–232.doi:10.1007/s00049-004-0280-6. . Crossref, ISIGoogle Scholar
    • Waterlow J.C, Armstrong D.G, Fowden L& Riley R. 1998Oxford, UK:Oxford University Press. Google Scholar
    • Weatherston I& Minks A.K. 1995Regulation of semiochemicals—global aspects. Integr. Pest Manage. Rev. 1, 1–13.doi:10.1007/BF00140330. . CrossrefGoogle Scholar
    • WHOManual on environmental management for mosquito control with special emphasis on malaria vectors. 1982Geneva, Switzerland:World Health Organisation. Google Scholar