Abstract
Push-pull, a novel approach for integrated management of insect pests, weed and soil fertility, was developed through the exploitation of chemical ecology and agro-biodiversity to address agricultural constraints facing millions of resource-poor African farmers. The technology was developed by selecting appropriate plants that naturally emit signalling chemicals (semiochemicals) and influence plant-plant and insect-plant interactions. Plants highly attractive for egg laying by lepidopteran cereal stemborer pests were selected and employed as trap crops, to draw pests away from the main cereal crops. Among these, Pennisetum purpureum produced significantly higher levels of volatile cues (stimuli), used by gravid stem borer females to locate host plants, than maize (Zea mays) or sorghum (Sorghum bicolor). Despite its attractiveness to stemborer moths, P. purpureum supported minimal survival of the pests’ immature stages. Plants that repelled stem borer moths, notably Melinis minutiflora and forage legumes in the genus Desmodium, were selected as intercrops, which also attracted natural enemies of the pests through emission of (E)-β-ocimene and (E)-4,8-dimethyl-1,3,7-nonatriene. Desmodium intercrop suppressed parasitic weed, Striga hermonthica, through an allelopathic mechanism. Their root exudates contain novel flavonoid compounds which stimulate suicidal germination of S. hermonthica seeds and dramatically inhibit its attachment to the host roots. We identified and selected new drought- and temperature-tolerant trap [Brachiaria ( B. brizantha × B. ruziziensis ) cv. mulato] and intercrop plants (Desmodium, e.g. D. intortum) suitable for drier agroecologies. The new trap and intercrop plants also have appropriate chemistry in controlling stemborers, a new invasive pest, fall armyworms and parasitic striga weeds. Opportunities for semiochemical delivery by companion plants, including plant-plant signalling and early herbivory alert, are explored for developing future smart integrated pest management (IPM) strategies.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- BBSRC:
-
Biotechnology and Biological Sciences Research Council
- BIRE:
-
Biological Interactions in The Root Environment
- DFID:
-
Department for International Development
- FAW:
-
Fall armyworm
- GC-EAG:
-
Coupled gas chromatography–electroantennography
- GDP:
-
Gross domestic product
- HIPVs:
-
Herbivore-induced plant volatiles
- IPM:
-
Integrated pest management
- OPV:
-
Open pollinated varieties
- SDC:
-
Swiss Agency for Development and Cooperation
- SDG:
-
Sustainable Development Goals
- SSA:
-
Sub-Saharan Africa
References
Al-Sarar, A., Hall, F. R., & Downer, R. A. (2006). Impact of spray application methodology on the development of resistance to cypermethrin and spinosad by fall armyworm Spodoptera frugiperda (J.E. Smith). Pest Management Science, 62, 1023–1031.
Arimura, G., Ozawa, R., Shimoda, T., Nishioka, T., Boland, W., & Takabayashi, J. (2000). Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature, 406, 512–515.
Bebawi, F. F., & Metwali, E. M. (1991). Witch-weed management by sorghum–Sudan grass seed size and stage of harvest. Agronomy Journal, 83, 781–785.
Birkett, M. A., Chamberlain, K., Khan, Z. R., Pickett, J. A., Toshova, T., Wadhams, L. J., & Woodcock, C. M. (2006). Electrophysiological responses of the lepidopterous stemborers Chilo partellus and Busseolafusca to volatiles from wild and cultivated host plants. Journal of Chemical Ecology, 32, 2475–2487.
Bruce, T. J. A., Wadhams, L. J., & Woodcock, C. M. (2005). Insect host location: A volatile situation. Trends in Plant Science, 10, 269–274.
Bruce, T. J. A., Midega, C. A. O., Birkett, M. A., Pickett, J. A., & Khan, Z. R. (2010). Is quality more important than quantity? Insect behavioral responses to changes in a volatile blend after stemborer oviposition on an African grass. Biology Letters, 6, 314–317.
Burke, M. B., Lobell, D. B., & Guarino, L. (2009). Shifts in African crop climates by 2050, and the implications for crop improvement and genetic resources conservation. Global Environmental Change, 19, 317–325.
CABI. (2017). Fall armyworm: Impacts and implications for Africa. Evidence note (2), September 2017. CAB International.
Chamberlain, K., Khan, Z. R., Pickett, J. A., Toshova, T., & Wadhams, L. J. (2006). Diel periodicity in the production of green leaf volatiles by wild and cultivated host plants of stemborer moths, Chilo partellus and Busseola fusca. Journal of Chemical Ecology, 32, 565–577.
Chidawanyika, F. (2015). Effects of drought on the production of ectrophysiologically active biogenic volatiles important for cereal pest management. University of the Witwatersrand, South Africa (p. 172). Ph.D. Dissertation.
Chidawanyika, F., Midega, C. A. O., Bruce, T. J. A., Duncan, F., Pickett, J. A., & Khan, Z. R. (2014). Oviposition acceptance and larval development of Chilo partellus stemborers in drought-stressed wild and cultivated grasses of East Africa. EntomologiaExperimentalis et Applicata, 151, 209–217.
Chitere, P. O., & Omolo, B. A. (1993). Farmers’ indigenous knowledge of crop pests and their damage in western Kenya. International Journal of Pest Management, 39, 126–132.
Cock, M. J. W., Beseh, P. K., Buddie, A. G., Cafá, G., & Crozier, J. (2017). Molecular methods to detect Spodoptera frugiperda in Ghana, and implications for monitoring the spread of invasive species in developing countries. Scientific Reports, 7(4103), 10.
Cook, D. R., Leonard, B. R., & Gore, J. (2004). Field and laboratory performance of novel insecticides against armyworms (Lepidoptera: Noctuidae). Florida Entomologist, 87, 433–439.
Cook, S. M., Khan, Z. R., & Pickett, J. A. (2007). The use of ‘push–pull’ strategies in integrated pest management. Annual Review of Entomology, 52, 375–400.
Dicke, M., & Sabelis, M. W. (1988). Infochemical terminology: Based on cost-benefit analysis rather than origin of compounds? Functional Ecology, 2, 131–139.
Frizzas, M. R., Neto, S. S., de Oliveira, C. M., & Omoto, C. (2014). Genetically modified corn on fall armyworm and earwig populations under field conditions. Ciência Rural, 44, 203–209.
Frost, D. L., Gurney, A. L., Press, M. C., & Scholes, J. D. (1997). Striga hermonthica reduces photosynthesis in sorghum: The importance of stomatal limitations and a potential role for ABA? Plant, Cell & Environment, 20, 483–492.
Gethi, J. G., Smith, M. E., Mitchell, S. E., & Kresovich, S. (2005). Genetic diversity of Striga hermonthica and Striga asiatica populations in Kenya. Weed Research, 45, 64–73.
Goergen, G., Kumar, P. L., Sankung, S. B., Togola, A., & Tamò, M. (2016). First report of outbreaks of the fall armyworm Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS One, 11(10), e0165632. https://doi.org/10.1371/journal.pone.0165632.
Gressel, J., Hanafi, A., Head, G., Marasas, W., Obilana, A. B., Ochanda, J., Souissi, T., & Tzotzos, G. (2004). Major heretofore intractable biotic constraints to African food security that may be amenable to novel biotechnological solutions. Crop Protection, 23, 661–689.
Gurney, A. L., Press, M. C., & Scholes, J. D. (1999). Infection time and density influence the response of sorghum to the parasitic angiosperm Striga hermonthica. New Phytologist, 143, 573–580.
Gurney, A. L., Slate, J., Press, M. C., & Scholes, J. D. (2006). A novel form of resistance in rice to the angiosperm parasite Striga hermonthica. New Phytologist, 169, 199–208.
Hardie, J., Isaacs, R., Pickett, J. A., Wadhams, L. J., & Woodcock, C. M. (1994). Methyl salicylate and (−) -(1R,5S)-myrtenal are plant derived repellents for black bean aphid, Aphis fabae Scop. (Homoptera: Aphididae). Journal of Chemical Ecology, 20, 2847–2855.
Hassanali, A., Herren, H., Khan, Z. R., Pickett, J. A., & Woodcock, C. M. (2008). 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. Philosophical Transactions of the Royal Society B, 363, 611–621.
Hilker, M., & Meiners, T. (2006). Early herbivore alert: Insect eggs induce plant defense. Journal of Chemical Ecology, 32, 1379–1397.
Hoerling, M., & Kumar, A. (2003). The perfect ocean for drought. Science, 299, 691–694.
Hooper, A. M., Caufield, J. C., Hao, B., Pickett, J. A., Midega, C. A. O., & Khan, Z. R. (2015). Isolation and identification of Desmodium root exudates from drought tolerant species used as intercrops against Striga hermonthica. Phytochemistry, 117, 380–387.
International Assessment of Agricultural Knowledge, Science and Technology for Development (IAASTD). (2009). Global report: Agriculture at a crossroads. Washington, DC: Island Press.
International Fund for Agricultural Development (IFAD). (2011). Rural poverty report: New realities, new challenges: New opportunities for tomorrow’s generation. Rome: IFAD.
Johnson, S. J. (1987). Migration and the life history strategy of the fall armyworm, Spodoptera frugiperda in the western hemisphere. Insect Science and its Application, 8(4–6), 543–549.
Kessler, A., & Baldwin, I. T. (2001). Defensive function of herbivore-induced plant volatile emissions in nature. Science, 291, 2141–2144.
Kfir, R., Overholt, W. A., Khan, Z. R., & Polaszek, A. (2002). Biology and management of economically important lepidopteran cereal stemborers in Africa. Annual Review of Entomology, 47, 701–731.
Khan, Z. R., Chilishwa, P., Ampong-Nyarko, K., Smart, L. E., Polaszek, A., Wandera, J., & Mulaa, M. A. (1997a). Utilisation of wild gramineous plants for the management of cereal stemborers in Africa. Insect Science and its Application, 17, 143–150.
Khan, Z. R., Ampong-Nyarko, K., Chilishwa, P., Hassanali, A., Kimani, S., Lwande, W., Overholt, W. A., Pickett, J. A., Smart, L. E., Wadhams, L. J., & Woodcock, C. M. (1997b). Intercropping increases parasitism of pests. Nature, 388, 631–632.
Khan, Z. R., Pickett, J. A., van den Berg, J., Wadhams, L. J., & Woodcock, C. M. (2000). Exploiting chemical ecology and species diversity: Stemborer and striga control for maize and sorghum in Africa. Pest Management Science, 56, 957–962.
Khan, Z. R., Pickett, J. A., Wadhams, L. J., et al. (2001). Habitat management strategies for the control of cereal stemborers and Striga in maize in Kenya. Insect Science and Applications, 21, 375–380.
Khan, Z. R., Hassanali, A., Overholt, W., Khamis, T. M., Hooper, A. M., Pickett, A. J., Wadhams, L. J., & Woodcock, C. M. (2002). Control of witchweed Striga hermonthica by intercropping with Desmodium spp., and the mechanism defined as allelopathic. Journal of Chemical Ecology, 28, 1871–1885.
Khan, Z. R., Midega, C. A. O., Hutter, N. J., Wilkins, R. M., & Wadhams, L. J. (2006a). Assessment of the potential of Napier grass (Pennisetum purpureum) varieties as trap plants for management of Chilo partellus. EntomologiaExperimentalis et Applicata, 119, 15–22.
Khan, Z. R., Midega, C. A. O., Pickett, J. A., Wadhams, L. J., Hassanali, A., & Wanjoya, A. (2006b). Management of witchweed, Striga hermonthica, and stemborers in sorghum, Sorghum bicolor, through intercropping with greenleaf Desmodium, Desmodium intortum. International Journal of Pest Management, 52, 297–302.
Khan, Z. R., Midega, C. A. O., Wadhams, L. J., Pickett, J. A., & Mumuni, A. (2007). Evaluation of Napier grass (Pennisetum purpureum) varieties for use as trap plants for the management of African stemborer (Busseola fusca) in a push-pull strategy. Entomologia Experimentalis et Applicata, 124, 201–211.
Khan, Z. R., Midega, C. A. O., Amudavi, D. M., Hassanali, A., & Pickett, J. A. (2008). On-farm evaluation of the ‘push-pull’ technology for the control of stemborers and striga weed on maize in western Kenya. Field Crops Research, 106, 224–233.
Khan, Z. R., Midega, C. A. O., Bruce, T. J. A., Hooper, A. M., & Pickett, J. A. (2010). Exploiting phytochemicals for developing a push – pull crop protection strategy for cereal farmers in Africa. Journal of Experimental Botany, 61, 4185–4196.
Khan, Z. R., Midega, C. A. O., Pittchar, J. O., Murage, A. W., Birkett, M. A., Bruce, T. J. A., & Pickett, J. A. (2014). Achieving food security for one million sub-Saharan African poor through push–pull innovation by 2020. Philosophical Transactions of the Royal Society B, 369, 20120284.
Khan, Z. R., Midega, C. A. O., Hooper, A., & Pickett, J. A. (2016). Push-pull: Chemical ecology-based integrated pest management technology. Journal of Chemical Ecology, 42(7), 689–697.
Midega, C. A. O., Khan, Z. R., van den Berg, J., Ogol, C. K. P. O., & Pickett, J. A. (2006). Maize stemborer predator activity under ‘push-pull’ system and Bt-maize: A potential component in managing Bt resistance. International Journal of Pest Management, 52, 1–10.
Midega, C. A. O., Khan, Z. R., van den Berg, J., Ogol, C. K. P. O., Dippenaar-Schoeman, A. S., Pickett, J. A., & Wadhams, L. J. (2008). Response of ground-dwelling arthropods to a push–pull habitat management system: Spiders as an indicator group. Journal of Applied Entomology, 132, 248–254.
Midega, C. A. O., Khan, Z. R., Van den Berg, J., Ogol, C. K. P. O., Bruce, T. J., & Pickett, J. A. (2009). Non-target effects of the ‘push–pull’ habitat management strategy: Parasitoid activity and soil fauna abundance. Crop Protection, 28, 1045–1051.
Midega, C. A. O., Khan, Z. R., Amudavi, D. A., Pittchar, J., & Pickett, J. A. (2010). Integrated management of Striga hermonthica and cereal stemborers in finger millet (Eleusine coracana (L.) Gaertn.), through intercropping with Desmodium intortum. International Journal of Pest Management, 56, 145–151.
Midega, C. A. O., Jonsson, M., Khan, Z. R., & Ekbom, B. (2014). Effects of landscape complexity and habitat management on stemborer colonization, parasitism and damage to maize. Agriculture, Ecosystems and Environment, 188, 289–293.
Midega, C. A. O., Bruce, T. J. A., Pickett, J. A., & Khan, Z. R. (2015a). Ecological management of cereal stemborers in African smallholder agriculture through behavioral manipulation. Ecological Entomology, 40(Suppl. 1), 70–81.
Midega, C. A. O., Bruce, T. J. A., Pickett, J. A., Jimmy, J. O., Murage, A., & Khan, Z. R. (2015b). Climate-adapted companion cropping increases agricultural productivity in East Africa. Field Crops Research, 180, 118–125.
Midega, C. A. O., Wasonga, C. J., Hooper, A. M., Pickett, J. A., & Khan, Z. R. (2017). Drought- tolerant Desmodium species effectively suppress parasitic striga weed and improve cereal grain yields in western Kenya. Crop Protection, 98, 94–101.
Midega, C. A. O., Pittchar, J. O., Pickett, J. A., Hailu, G. W., & Khan, Z. R. (2018). A climate-adapted push-pull system effectively controls fall armyworm, Spodoptera frugiperda (J E Smith), in maize in East Africa. Crop Protection, 105, 10–15.
Nordlund, D. A., & Lewis, W. J. (1976). Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. Journal of Chemical Ecology, 2, 211–220.
Oswald, A. (2005). Striga control technologies and their dissemination. Crop Protection, 24, 333–342.
Oswald, A., Ransom, J. K., Kroschel, J., & Sauerborn, J. (2001). Transplanting maize and sorghum reduces Striga hermonthica damage. Weed Science, 49, 346–353.
Parker, C., & Riches, C. R. (1993). Parasitic weeds of the world: Biology and control. Wallingford: CAB International.
Päts, P. (1991). Activity of Chilo partellus (Lepidoptera: Pyralidae): Eclosion, mating and oviposition time. Bulletin of Entomological Research, 81, 93–96.
Pickett, J. A., & Khan, Z. R. (2016). Plant volatile-mediated signalling and its application in agriculture: Successes and challenges. New Phytologist, 212, 856–870.
Pickett, J. A., Hamilton, M. L., Hooper, A. M., Khan, Z. R., & Midega, C. A. O. (2010). Companion cropping to manage parasitic plants. Annual Review of Phytopathology, 48, 161–177.
Pinstrup-Andersen (Ed.). (2010). The African food system and its interaction with human health and nutrition. New York: Cornell University Press.
Pretty, J., Noble, A. D., Bossio, D., Dickson, J., Hine, R. E., Penning de Vries, F. W. T., & Morrison, J. I. L. (2006). Resource-conserving agriculture increases yields in developing countries. Environmental Science and Technology, 40(4), 1114–1119.
Pretty, J., Toulmin, C., & Williams, S. (2011). Sustainable intensification in African agriculture. International Journal of Sustainable Agriculture, 9, 5–24.
Rodenburg, J., Bastiaans, L., Weltzien, E., & Hess, D. E. (2005). How can selection for striga resistance and tolerance in sorghum be improved. Field Crops Research, 93, 34–50.
Sanchez, P. (2002). Soil fertility and hunger in Africa. Science, 295(5562), 2019–2020.
Solomon, D., Lehmann, J., Kinyanjui, J., Amelung, W., Lobe, I., Ngoze, S., Riha, S., Pell, A., Storer, N. P., Babcock, J. M., Schlenz, M., Meade, T., & Thompson, G. D. (2010). Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda(Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology, 103, 1031–1038.
Sparks, A. N. (1979). A review of the biology of the fall armyworm. Florida Entomologist, 62(2), 82–87.
Storer, N. P., Babcock, J. M., Schlenz, M., Meade, T., & Thompson, G. D. (2010). Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology, 103, 1031–1038.
Tamiru, A., Bruce, T. J. A., Woodcock, C. M., et al. (2011). Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecology Letters, 14, 1075–1083.
Tamiru, A., Bruce, T., Midega, C. A. O., et al. (2012). Oviposition-induced volatile emissions from African smallholder farmers’ maize varieties. Journal of Chemical Ecology, 38, 231–234.
Tamiru, A., Khan, Z. R., & Bruce, T. J. A. (2015). New directions for improving crop resistance to insects by breeding for egg induced defence. Current Opinion in Insect Science. https://doi.org/10.1016/j.cois.2015.02.011.
Tenebe, V. A., & Kamara, H. M. (2002). Effect of Striga hermonthica on the growth characteristics of sorghum intercropped with groundnut varieties. Journal of Agronomy and Crop Science, 188, 376–381.
Todd, E. L., & Poole, R. W. (1980). Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the Western Hemisphere. Annals of the Entomological Society of America, 73(6), 722–738.
Tsanuo, M. K., Hassanali, A., Hooper, A. M., Khan, Z. R., Kaberia, F., Pickett, J. A., & Wadhams, L. (2003). Isoflavanones from the allelopathic aqueous root exudates of Desmodium uncinatum. Phytochemistry, 64, 265–273.
Turlings, T. C. J., Scheepmaker, J. W. A., Vet, L. E. M., Tumlinson, J. H., & Lewis, W. J. (1990a). How contact experiences affect preferences for host-related odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae). Journal of Chemical Ecology, 16, 1577–1589.
Turlings, T. C. J., Tumlinson, J. H., & Lewis, W. J. (1990b). Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250, 1251–1253.
Turlings, T. C. J., Loughrin, J. H., McCall, P. J., Rose, U. S. R., Lewis, W. J., & Tumlinson, J. H. (1995). How caterpillar-damaged plants protect themselves by attracting parasitic wasps. InProceedings of the National Academy of Sciences of the United States of America (Vol. 92, pp. 4169–4174).
World Bank. (2007). World development indicators. Washington, DC.
World Bank. (2008). World development report 2008: Agriculture for development. Washington, DC: The World Bank.
World Resources Institute; Department of Resource Surveys and Remote Sensing, Ministry of Environment and Natural Resources, Kenya; Central bureau of Statistics, Ministry of Planning and National Development, Kenya; and International Livestock Research Institute. (2007). Nature’s benefits in Kenya: An Atlas of ecosystems and human well-being. Washington, DC and Nairobi: World Resources Institute.
Yoder, J. I. (1999). Parasitic plant responses to host plant signals: A model for subterranean plant–plant interactions. Current Opinion in Plant Biology, 2, 65–70.
Young, R. (1979). Fall armyworm: Control with insecticides. Florida Entomologist, 62, 130–133.
Yu, S. J. (1992). Detection and biochemical characterization of insecticide resistance in fall armyworm (Lepidoptera: Noctuidae). Journal of Economic Entomology, 85, 675–682.
Acknowledgements
We gratefully acknowledge financial support to ICIPE provided by the following organizations and agencies: the European Union, Biovision Foundation, UK Department for International Development (DFID), Swedish International Development Cooperation Agency, the Swiss Agency for Development and Cooperation (SDC) and the Kenyan Government. The views expressed herein do not necessarily reflect the official opinion of these donors. The studies within the push-pull program are conducted in collaboration with Rothamsted Research of the UK, which receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council (BBSRC), with additional funding provided under the Biological Interactions in the Root Environment (BIRE) initiative. Various roles played by all partners and collaborators, including farmers, are greatly acknowledged too.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Khan, Z.R., Midega, C.A.O., Pittchar, J., Pickett, J.A. (2019). Exploiting Chemical Ecology for Developing Novel Integrated Pest Management Strategies for Africa. In: Peshin, R., Dhawan, A. (eds) Natural Resource Management: Ecological Perspectives . Sustainability in Plant and Crop Protection. Springer, Cham. https://doi.org/10.1007/978-3-319-99768-1_10
Download citation
DOI: https://doi.org/10.1007/978-3-319-99768-1_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-99767-4
Online ISBN: 978-3-319-99768-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)