REVIEW
A lag in the advancement of biotechnology: reliable control of maize stem borers in Africa
 
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Centre of Excellence in Molecular Biology, University of the Punjab, 87-West Canal Bank Road, Thokar Niaz Baig, Lahore, Pakistan
CORRESPONDING AUTHOR
Olawale Samuel Adeyinka
Centre of Excellence in Molecular Biology, University of the Punjab, 87-West Canal Bank Road, Thokar Niaz Baig, Lahore, Pakistan
Submission date: 2017-08-25
Acceptance date: 2017-12-18
 
Journal of Plant Protection Research 2018;58(1):8–24
KEYWORDS
TOPICS
ABSTRACT
The future of food security in Africa is being severely threatened due to an exponential increase in population, which is almost three times the increase of food production. Maize production is constrained by stem borers which cause significant yield losses. Yield losses can be further compounded by higher temperatures due to climate changes, which are expected to increase the population of maize stem borers. While several methods have been employed in stem borer management, there is still significant damage caused by maize stem borers. This necessitates better control methods including the adoption of recent biotechnological advancement in RNA interference (RNAi) technology. This review highlights evidence of an increase in the stem borer population as well as the foreseen decline in maize production worldwide due to the effects of climatic changes. Furthermore, we have drawn attention to improved methods that have been used to control stem borers in maize production as well as a reluctant acceptance of traditional biotechnology in Africa. Finally, we suggest the application of alternative RNA interference techniques to breed maize for efficient pest control in order to achieve food security, improve nutrition and promote sustainable maize production.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
 
REFERENCES (157)
1.
Adang M.J., Crickmore N., Jurat-Fuentes J.L. 2014. Diversity of Bacillus thuringiensis crystal toxins and mechanism of action. Advance Insect Physiology 47: 39–87. DOI: https://doi.org/10.1016/b978-0....
 
2.
Ajala S.O., Nour A.M., Ampong-Nyarko K., Odindo M.O. 2010. Evaluation of maize (Zea mays L.) genotypes as a component of integrated stem borer (Chilo partellus Swinhoe) management in coastal region of Kenya. African Journal of Agricultural Research 5 (8): 758–763. DOI: httsp://doi.org/10.5897/AJAR09.609.
 
3.
Alfaro C., Navarro-Llopis V., Primo J. 2009. Optimization of pheromone dispenser density for managing the rice striped stem borer, Chilo suppressalis (Walker), by mating disruption. Crop Protection 28 (7): 567–572. DOI: https://doi.org/10.1016/j.crop....
 
4.
Ali M.I., Luttrell R.G., Young S.Y. 2006. Susceptibilities of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) populations to Cry1Ac insecticidal protein. Journal of Economy Entomology 99: 164–175. DOI: https://doi.org/10.1093/jee/99....
 
5.
Araya A., Hoogenboom G., Luedeling E., Hadgu K.M., Kisekka I., Martorano L. G. 2015. Assessment of maize growth and yield using crop models under present and future climate in southwestern Ethiopia. Agricultural and Forest Meteorology 214–215: 252–265. DOI: http://doi.org/10.1016/j.agrfo....
 
6.
Bale J.S., Masters G.J., Hodkinson I.D., Wmack C.A., Bezemer T.M., Brown V.K., Butterfield J., Buse A., Coulson J.C., Farrar J., Good J.E.G., Harrington R., Hartley S., Jones T.H., Lindroth R.L., Press M.C., Symrnioudis I., Watt A.D., Whittaker J.B. 2002. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8 (1): 1–16. DOI: https://doi.org/10.1046/j.1365....
 
7.
Bally J., McIntyre G.J., Doran R.L., Lee K., Perez A., Jung H., Naim F., Larrinua I.M., Narva K.E., Waterhouse P.M.J. 2016. In-plant protection against Helicoverpa armigera by production of long hpRNA in chloroplasts. Frontiers in Plant Science 7: 1453. DOI: https://doi.org/10.3389/fpls.2....
 
8.
Bayram A., Tonğa A. 2016. First report of Chilo partellus in Turkey, a new invasive maize pest for Europe. Journal of Applied Entomology 140 (3): 236–240. DOI: https://doi.org/10.1111/jen.12....
 
9.
Ben-Yakir D., Chen M., Sinev S., Seplyarsky V. 2013. Chilo partellus (Swinhoe) (Lepidoptera: Pyralidae) a new invasive species in Israel. Journal of Appllied Entomology 137 (5): 398–400. DOI: https://doi.org/10.1111/j.1439....
 
10.
Berg van den J. 2017. Insect resistance management in Bt maize: wild host plants of stem borers do not serve as refuges in Africa. Journal of Economic Entomology 10 (1): 221–229. DOI: https://doi.org/10.1093/jee/to....
 
11.
Betz F.S., Hammond B.G., Fuchs R.L. 2000. Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regulatory Toxicology and Pharmacology 32 (2): 156–173. DOI: https://doi.org/10.1006/rtph.2....
 
12.
Blanc E. 2012. The impact of climate change on crop yields in sub-Saharan Africa. American Journal of Climate Change 1 (1): 1–13. DOI: https://doi.org/10.4236/ajcc.2....
 
13.
Bolognesi R., Ramaseshadri P., Anderson J., Bachman P., Clinton W., Flannagan R. 2012. Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte). PLoS ONE 7 (10): e0047534. DOI: https://doi.org/10.1371/journa....
 
14.
Bosque-Perez N.A., Mareck J.H. 1991. Distribution and species composition of lepidopterous maize borers in Southern Nigeria. Bulletin of Entomological Research 80 (4): 353–368. DOI: https://doi.org/10.1017/s00074....
 
15.
Bravo A., Gomez I., Conde J., Munoz-Garay C., Sanchez J., Miranda R., Zhuang M., Gill S.S., Soberón M. 2004. Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochimica et Biophysica Acta (BBA) – Biomembranes 1667 (1): 38–46. DOI: https://doi.org/10.1016/j.bbam....
 
16.
Bravo A., Sánchez J., Kouskoura T., Crickmore N. 2002. N-terminal activation is an essential early step in the mechanism of action of the B. thuringiensis Cry1Ac insecticidal toxin. Journal of Biological Chemistry 277 (27): 23985–23987. DOI: https://doi.org/10.1074/jbc.c2....
 
17.
Campagne P., Kruger M., Pasquet R., Le Ru B., van den B.J. 2013. Dominant inheritance of field-evolved resistance to Bt corn in Busseola fusca. PLoS ONE 8 (7): e69675. DOI: https://doi.org/10.1371/journa....
 
18.
Cairns J.E., Hellin J., Sonder K., Araus J.L., MacRobert J.F., Thierfelder C., Prasanna B.M. 2013. Adapting maize production to climate change in sub-Saharan Africa. Food Security 5 (3): 345–360. DOI: https://link.springer.com/arti....
 
19.
Calatayud P.A., Le Ru B.P., Berg van den J., Schulthess F. 2014. Ecology of the African maize stalk borer, Busseola fusca (Lepidoptera: Noctuidae) with special reference to. Insects 5 (3): 539–563. DOI: https://doi.org/10.3390/insect....
 
20.
Charles A.O., Midega Toby A., Bruce John A.P., Zeyaur R.K. 2015. Ecological management of cereal stemborers in African smallholder agriculture through behavioural manipulation. Ecological Entomology 40 (Suppl. 1): 70–81. DOI: https://doi.org/10.1111/een.12....
 
21.
Chen S., Chen X., Xu J. 2016. Impacts of climate change on agriculture: evidence from China. Journal of Environmental Economics and Management 76: 105–124. DOI: https://doi.org/10.1016/j.jeem....
 
22.
Chen J., Zhang D., Yao Q., Zhang J., Dong X., Tian H., Chen J., Zhang W. 2010. Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology 19 (6): 777–786. DOI: https://doi.org/10.1111/j.1365....
 
23.
Chinwada P., Overholt W.A. 2001. Natural enemies of maize stemborers on the highveld of Zimbabwe. African Entomology 9 (1): 67–75.
 
24.
Chinwada P., Nyamutukwa S., Marandure A., Zitsanza E.S. 2014. Biology and development of Sturmiopsis parasitica (Diptera: Tachinidae) on different species and populations of maize stem borers in Zimbabwe and an assessment of its suitability for redistribution in Africa. African Entomology 22 (4): 828–837. DOI: https://doi.org/10.4001/003.02....
 
25.
Cugala D., Schulthess F., Ogol C.P., Omwega C.O. 2006. Asessment of the impact of natural enemies on stem borer infestations and yield loss in maize using selected insecticides in Mozambique. Annales de la Société Entomologique de France (N.S.) 42 (3–4): 503–510. DOI: https://doi.org/10.1080/003792....
 
26.
Cork A., Ken D., Krishnaiah K., Casagrande E. 1996. Control of yellow stem borer, Scirpophaga incertulas (Lepidoptera: Pyralidae) by mating disruption on rice in India: Effect of unnatural pheromone blends and application time on efficacy. Bulletin of Entomological Research 86 (05): 515–524. DOI: https://doi.org/10.1017/s00074....
 
27.
De Groote H. 2002. Maize losses from stem borers in Kenya. Insect Science and its Application 22 (2): 89–96.
 
28.
Dejen A., Getu E., Azerefegne F., Ayalew A. 2014. Distribution and impact of Busseola fusca (Fuller) (Lepidoptera: Noctuidae) and Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) in Northeastern Ethiopia. Journal of Entomology and Nematology 6 (1): 1–13. DOI: https://doi.org/10.5897/jen201....
 
29.
De Maagd R.A., Bravo A., Berry C., Crickmore N., Schnepf H.E. 2003. Structure, diversity and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annual Review of Genetics 37 (1): 409–433. DOI: https://doi.org/10.1146/annure....
 
30.
Derera J., Mwimali M., Mugo S., Tongoona P., Lilian G. 2016. Evaluation of tropical maize inbred lines for resistance to two stem borer species, Busseola fusca and Chilo partellus. Journal of Plant Breeding and Crop Science 8 (2): 23–33. DOI: https://doi.org/10.5897/jpbcs2....
 
31.
Ding S.W. 2010. RNA-based antiviral immunity. Nature Reviews Immunology 10 (9): 632–644. DOI: https://doi.org/10.1038/nri282....
 
32.
Dunning C. M., Black E. C. L., Allan R.P. 2016. The onset and cessation of seasonal rainfall over Africa. Journal of Geophysical Research: Atmospheres 121(19): 11405–11424. DOI: https://doi.org/10.1002/2016jd....
 
33.
Dubelman S., Fischer J., Zapata F., Huizinga K., Jiang C., Uffman J. 2014. Environmental fate of double-stranded RNA in agricultural soils. PLoS One 9 (3): e9315. DOI: https://doi.org/10.1371/journa....
 
34.
Dykxhoorn D.M., Novina C.D., Sharp P.A. 2003. Killing the messenger: short RNAs that silence gene expression. Nature Reviews Molecular Cell Biology 4 (6): 457–467. DOI: https://doi.org/10.1038/nrm112....
 
35.
Dzitoyeva S., Dimitrijevic N., Manev H. 2001. Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Molecular Psychiatry 6: 665–670. DOI: https://doi.org/10.1038/sj.mp.....
 
36.
Ebenebe A.A., van den Berg J., van der Linde T.C. 1999. Effect of planting date of maize on damage and yield loss caused by the stalk borer, Busseola fusca (Fuller) (Lepidoptera: Noctuidae) in Lesotho. South African Journal of Plant and Soil 16 (4): 180–185. DOI: https://doi.org/10.1080/025718....
 
37.
Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494–498. DOI: 10.1038/35078107.
 
38.
El-Sayed A.M., Suckling D.M., Wearing C.H., Byers J.A. 2006. Potential of mass trapping for long term pest management and eradication of invasive species. Journal of Economic Entomology 99 (5): 1550–1564. DOI: https://doi.org/10.1093/jee/99....
 
39.
El-Wakeil N.E., Awadallah K.T., Farghaly H., Ibrahim A.A.M., Ragab Z.A. 2008. Efficiency of the newly recorded pupal parasitoid Pediobius furvus (Gahan) for controlling Sesamia cretica (Led.) pupae in Egypt. Archives of Phytopathology and Plant Protection 41 (5): 340–348. DOI: https://doi.org/10.1080/032354....
 
40.
Emana G., Overholt W.A., Kairu E. 2001. Ecological management of cereal stemborers in Ethiopia. p. 55–99. In: 7th Eastern and Southern Africa Regional Maize Conference 11–15th February 2001, Nairobi Kenya.
 
41.
EPA. 2017. Enviromental protection Agencies. Registers innovative tool to control corn rootworm. Available on: www.epa.gov/pesticide-registra... Accessed: October 27, 2017.
 
42.
Estes L.D., Beukes H., Bradley B.A., Debats S.R., Oppenheimer M., Ruane A.C., Tadross M. 2013. Projected climate impacts to South African maize and wheat production in 2055: A comparison of empirical and mechanistic modeling approaches. Global Change Biology 19 (12): 3762–3774. DOI: https://doi.org/10.1111/gcb.12....
 
43.
FAOSTAT. 2017. Food and agriculture commodities production. Rome, Italy. Available on: http:// fenix.fao.org/faostat/beta/en/.... Accessed: April 24, 2017.
 
44.
Félix A., Genestier E., Malosse G., Calatayud C., Le Ru P.A., Silvain B., Frérot J.F. 2009. Variability in pheromone communication among different haplotype populations of Busseola fusca. Journal of Chemical Ecology 35 (5): 618–623. DOI: https://doi.org/10.1007/s10886....
 
45.
Fire A.Z. 2007. Gene silencing by double-stranded RNA (Nobel Lecture). ChemInform 38 (50). DOI: https://doi.org/10.1002/chin.2....
 
46.
Fischer S., Jorg S., Silvia D. 2004. Host location of a pupal parasitoid in a tritrophic system compared to a model offering mechanosensory cues only. Journal of Insect Behavior 17 (2): 192–199. DOI: https://doi.org/10.1023/b:joir....
 
47.
Galdeano D.M., Breton M.C., Lopes J.R.S., Falk B.W., Machado M.A. 2017. Oral delivery of double-stranded RNAs induces mortality in nymphs and adults of the Asian citrus psyllid, Diaphorina citri. PLoS ONE 12 (3): e0171847. DOI: https://doi.org/10.1371/journa....
 
48.
Gatehouse A.M.R., Ferry N., Edwards M.G., Bell H.A. 2011. Insect-resistant biotech crops and their impacts on beneficial arthropods. Philosophical Transactions: Biological Sciences 366 (1569): 1438–1452. DOI: https://doi.org/10.1098/rstb.2....
 
49.
Gill S.S., Cowles E.A., Pietrantonio P.V. 1992. The mode of action of Bacillus thuringiensis endotoxins. Annual Review of Entomology 37 (1): 615–636. DOI: https://doi.org/10.1146/annure....
 
50.
Gould F. 2000. Testing Bt refuge strategies in the field. Nature Biotechnology 18 (3): 266–267. DOI: https://doi.org/10.1038/73693.
 
51.
Gounou S., Jiang N., Schulthess F. 2009. Long-term seasonal fluctuations of Lepidopteran cereal stem borers and their natural enemies on maize and wild host plants in southern Benin. Insect Science 16 (4): 329–341. DOI: https://doi.org/10.1111/j.1744....
 
52.
Hammond S.M., Boettcher S., Caudy A.A., Kobayashi R., Hannon G.J. 2001. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293 (5532): 1146–1150. DOI: https://doi.org/10.1126/scienc....
 
53.
Harrington R., Fleming R.A., Woiwod I.P. 2001. Climate change impacts on insect management and conservation in temperate regions: can they be predicted? Agricultural and Forest Entomology 3 (4): 233–240. DOI: https://doi.org/10.1046/j.1461....
 
54.
Hauptfleisch K., Yonow T., Kriticos D.J., Ota N. 2014. Busseola fusca. HarvestChoice Pest Geography. St. Paul, MN: InSTePP-HarvestChoice (September): 1–6.
 
55.
Howse P.E. 2004. Mechanism of exosex auto-confusion system of mating disruption. International Pest Control 45 (6): 321–322.
 
56.
Hui X.M., Yang L.W., He G.L., Yang Q.P., Han Z.J., Li F., Yang L.W., He G.L., Yang Q.P. 2011. RNA interference of ace1 and ace2 in Chilo suppressalis reveals their different contributions to motor ability and larval growth. Insect Molecular Biology 20 (4): 507–518. DOI: https://doi.org/10.1111/j.1365....
 
57.
John D., Mwimali M., Stephen M., Pangirayi T., Gichuru L. 2016. Evaluation of tropical maize inbred lines for resistance to two stem borer species, Busseola fusca and Chilo partellus. Journal of Plant Breeding and Crop Science 8 (2): 23–33. DOI: https://doi.org/10.5897/jpbcs2....
 
58.
Jones P., Thornton P. 2003. The potential impacts of climate change on maize production in Africa and Latin America in 2055. Global Environmental Change 13 (1): 51–59. DOI: https://doi.org/10.1016/s0959-....
 
59.
Kakule T.O., Latigo M.W., Okoth V.A.O. 1997. Distribution and damage by Chilo partellus (Swinhoe), Busseola fusca (Fuller), Eldana saccharina (Waller) and Sesamia calamistis (Hampson) in two locations in Uganda. African Crop Science Journal 5 (4): 385–393.
 
60.
Karaya H., Njoroge K., Mugo S., Nderitu H. 2009. Combining ability among twenty insect resistant maize inbred lines resistant to Chilo partellus and Busseola fusca stem borers. International Journal of Plant Production 3 (1): 115–127.
 
61.
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 (11): 957–962. DOI: https://doi.org/10.1002/1526-4...<957::aidps236>3.0.co;2-t.
 
62.
Khan Z.R., Chiliswa P., Ampong-Nyarkko K., Smart L.A., Polaszek A., Wandera J., Mulaa M.A. 1997 Utilization of wild gramineous plants for management of cereal stem borers in Africa. International Journal of Tropical Insect Science 17 (1): 143–150. DOI: https://doi.org/10.1017/s17427....
 
63.
Kfir R. 1997. Natural control of the cereal stem borers Busseola fusca and Chilo partellus in South Africa. International Journal of Tropical Insect Science 17 (1): 61–67. DOI: https://doi.org/10.1017/s17427....
 
64.
Kfir R. 1990. Parasites of the spotted stalk borer, Chilo partellus [Lepidoptera: Pyralidae] in South Africa. Entomophaga 35 (3): 403–410. DOI: https://doi.org/10.1007/bf0237....
 
65.
Kfir R. 1995. Parasitoids of the African maize stem borer, Busseola fusca (Lepidoptera: Noctuidae), in South Africa. Bulletin of Entomological Research 85 (3): 369–377. DOI: https://doi.org/10.1017/s00074....
 
66.
Khadioli N., Tonnang Z.E.H., Muchugu E., Ong’amo G., Achia T., Kipchirchir I., Le Ru B. 2014. Effect of temperature on the phenology of Chilo partellus (Swinhoe) (Lepidoptera, Crambidae); simulation and visualization of the potential future distribution of Chilo partellus in Africa under warmer temperatures through the development of life-table parameters. Bulletin of Entomological Research 104 (6): 809–22. DOI: https://doi.org/10.1017/s00074....
 
67.
Knox J., Hess T., Daccache A., Wheeler T. 2012. Climate change impacts on crop productivity in Africa and South Asia. Environmental Research Letters 7 (3): 34032. DOI: https://doi.org/10.1088/1748-9....
 
68.
Kocsis M., Hufnagel L. 2011. Impacts of climate change on lepidoptera species and communities. Applied Ecology and Environmental Research 9 (1): 43–72. DOI: https://doi.org/10.15666/aeer/....
 
69.
Kola V.S.R., Renuka P., Madhav M.S., Mangrauthia S.K. 2015. Key enzymes and proteins of crop insects as candidate for RNAi based gene silencing. Frontiers Physiology 6: 119. DOI: https://doi.org/10.3389/fphys.....
 
70.
Kola V., Sudhakara R., Renuka P., Ayyagari P.P., Satendra K.M., Sena M.B., Babu V.R. 2016. Silencing of CYP6 and APN genes affects the growth and development of rice yellow stem borer, Scirpophaga incertulas. Frontiers in Physiology 7: 20. DOI: https://doi.org/10.3389/fphys.....
 
71.
Le Ru B.P., Ong’amo G.O., Moyal P., Ngala L., Musyoka B., Abdullah Z., Cugala D., Defabachew B., Haile T.A., Kauma Matama T., Lada V.Y., Negassi B., Pallangyo K., Ravololonandrianina J., Sidumo A., Omwega C., Schulthess F., Calatayud P.-.A, Silvain J. 2006. Diversity of lepidopteran stem borers on monocotyledonous plants in eastern Africa and the islands of Madagascar and Zanzibar revisited. Bulletin of Entomological Research 96 (6): 555–563. DOI: https://doi.org/10.1017/ber200....
 
72.
Li H., Ruobing G., Huimin G., Xuexia M. 2015. New insights into an RNAi approach for plant defence against piercingsucking and stem-borer insect pests. Plant, Cell and Environment 38 (11): 2277–2285. DOI: https://doi.org/10.1111/pce.12....
 
73.
Liebmann B., Ileana B., George M.K., Leila M.V., Carvalho G., Senay B. 2009. Seasonality of African precipitation from 1996 to 2009. Journal of Climate 25 (12): 4304–4322. DOI: https://doi.org/10.1175/jcli-d....
 
74.
Liu S., Ding Z., Zhang C., Yang B., Liu Z. 2010. Gene knockdown by introthoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochemistry and Molecular Biololgy 40: 666–671. DOI: https://doi.org/10.1016/j.ibmb....
 
75.
Lin Y., Jia-Hsin H., Yun L., Xavier B. 2017. Oral delivery of dsRNA lipoplexes to German cockroach protects dsRNA from degradation and induces RNAi response. Pest Management Science 73 (5): 960–966. DOI: https://doi.org/10.1002/ps.440....
 
76.
Lobell D.B., Bänziger M., Magorokosho C., Vivek B. 2011. Nonlinear heat effects on African maize as evidenced by historical yield trials. Nature Climate Change 1 (1): 42–45. DOI: https://doi.org/10.1038/nclima....
 
77.
Losley J.E., Rayor L.S., Carter M.E. 1999. Transgenic pollen harms monarch larvae. Nature 399 (6733): 214. DOI: https://doi.org/10.1038/20338.
 
78.
Luttrell R.G., Wan L., Knighten K. 1999. Variation in susceptibility of noctuid (Lepidoptera) larvae attacking cotton and soybean to purified endotoxin proteins and commercial formulations of Bacillus thuringiensis. Journal of Economics Entomology 92 (1): 21–32. DOI: https://doi.org/10.1093/jee/92....
 
79.
Lv X., Wang H., Zeng X.,Yang X., Weng J., Di H., Guo Y., Wang Z., Li X. 2013. Research and application of transgenic Bt corn for insect resistance. Crops 2: 7–12.
 
80.
Mailafiya M.D., Le Ru P.B., Kairu E.W., Calatayud P.-A., Dupas S. 2010. Factors affecting stem borer parasitoid species diversity and parasitism in cultivated and natural habitats factors affecting stem borer parasitoid species diversity and parasitism in cultivated and natural habitats. Environmental Entomology 39 (1): 57–67. DOI: https://doi.org/10.1603/en0919....
 
81.
Mailafiya D.M., Le Ru P.B., Kairu E.W., Dupas S., Calatayud P.-A. 2011. Parasitism of lepidopterous stem borers in cultivated and natural. Journal of Insect Science 11 (15): 1–19. DOI: https://doi.org/10.1673/031.01....
 
82.
Malik H.J., Amir R., Imran A., Jodi A., Scheffler B., Scheffler E., Judith K.B. 2016. RNAi-mediated mortality of the whitefly through transgenic expression of double-stranded RNA homologous to acetylocholinesterase and ecdysone receptor in tobacco plants. Scientific Report 6 (1): 38469. DOI: https://doi.org/10.1038/srep38....
 
83.
Mao J., Zeng F. 2012. Feeding-based RNA intereference of a gap gene is lethal to the pea aphid, Acyrthosiphon pisum. PLoS ONE 7 (11): e48718. DOI: https://doi.org/10.1371/journa....
 
84.
Mao Y.B., Cai W.J., Wang J.W., Hong G.J., Tao X.Y., Wang L.J., Huang Y.P., Chen X.Y. 2007. Silencing a cotton bollworm P450 monooxygenase gene by plant mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnology 25 (11): 1307–1313. DOI: https://doi.org/10.1038/nbt135....
 
85.
Mello C.C., Conte Jr. D. 2004. Revealing the world of RNA interference. Nature 431: 338–342. DOI: https://doi.org/10.1038/nature....
 
86.
Meister G, Tuschl T. 2004. Mechanisms of gene silencing by double-stranded RNA. Nature 431: 343–349. DOI: https://doi.org/10.1038/nature....
 
87.
Midingoyia S.G., Hippolyte D.A., Ibrahim M., Georges O., Esther A., Gerphas O., Hugo D. 2016. Assessing the long-term welfare effects of the biological control of cereal stemborer pests in East and Southern Africa: Evidence from Kenya, Mozambique and Zambia Agriculture. Ecosystems and Environments 230: 10–23. DOI: https://doi.org/10.1016/j.agee....
 
88.
Mihm J. 1997. Insect resistance maize; Recent advances and utilization. Proceedings of an International Symposium Held at the International Maize and Wheat Improvement Center (CIMMYT), 27 November–3 December, 1994, 156 pp.
 
89.
Mir K. 2000. Chemical control of maize stem Borer (Chilo partellus Swin.). Pakistan Journal of Biological Sciences 3 (12): 2116–2118. DOI: https://doi.org/10.3923/pjbs.2....
 
90.
Moolman H.J., van den Berg J., Conlong D., Cugala D., Siebert S.J., Le Ru B.P. 2013. Diversity of stem borer parasitoids and their associated wild host plants in South Africa and Mozambique. Phytoparasitica 41 (1): 89–104. DOI: https://doi.org/10.1007/s12600....
 
91.
Mugo S.N., Bergvinson D., Hoisington D. 2001. Options in developing stem borer-resistant maize: CIMMYT’s approaches and experiences. Insect Science and its Application 21 (4): 409–415. DOI: https://doi.org/10.1017/s17427....
 
92.
Muller C., Cramer W., Hare W.L., Lotze-Campen H. 2011. Climate change risks for African agriculture. Proceedings of the National Academy of Sciences of the United States of America 108 (11): 4313–4315. DOI: 10.1073/pnas.1015078108.
 
93.
Mwalusepo S., Tonnang H.E.Z., Massawe E.S., Okuku G.O., Khadioli N., Johansson T., Calatayud P.-A., Le Ru B.P. 2015. Predicting the impact of temperature change on the future distribution of maize stem borers and their natural enemies along East African mountain gradients using phenology models. PLoS ONE 10 (6): 1–23. DOI: https://doi.org/10.1371/journa....
 
94.
Mwimali M., Derera J., Mugo S., Tongoona P., Lilian G. 2016. Combining ability for stem borer resistance and heterotic orientation of maize inbred lines using CIMMYT single cross testers under Busseola fusca infestation. Euphytica 208: 323–335. DOI: https://doi.org/10.1007/s10681....
 
95.
Mwimali M., Derera J., Tongoona P., Mugo S., Gichuru L. 2015. Combining ability for stem borer resistance and heterotic orientation of maize inbred lines using CIMMYT single cross testers under Chilo partellus infestation. Journal of Plant Breeding and Crop Science 7 (11): 310–326. DOI: https://doi.org/10.5897/jpbcs2....
 
96.
Mwololo J.K., Munyiri S.W., Semagn K., Mugo S., Okori P. 2015. Genetic diversity analysis in tropical maize germplasm for stem borer and storage pest resistance using molecular markers and phenotypic traits. Molecular Plant Breeding 6 (15): 1–22.
 
97.
Nair R., Kalia V., Aggarwal K.K., Gujar G.T. 2010. Inheritance of Cry1Ac resistance and associated biological traits in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology 104: 31–38. DOI: https://doi.org/10.1016/j.jip.....
 
98.
Newmark P.A., Reddien P.W., Cebria F., Alvarado A.S. 2003. Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proceedings of the National Academy of Sciences 100 (Suppl. 1): 11861–11865. DOI: https://doi.org/10.1073/pnas.1....
 
99.
Ndemah R., Schulthess F., Le Ru B., Bame I. 2007. Lepidopteran cereal stem borers and associated naturel enemies on maize and wild grass hosts in Cameroon. Journal of Applied Entomology 131 (9–10): 658–668. DOI: https://doi.org/10.1111/j.1439....
 
100.
Ndemah R., Gounouand S., Schulthess F. 2002. The role of wild grasses in the management of lepidopterous stem borers on maize in the humid tropics of western Africa. Bulletin of Entomological Research 92 (6): 507–519. DOI: https://doi.org/10.1079/ber200....
 
101.
Ndemah R., Schulthess F., Poehling M., Borgemeister C. 2001. Natural enemies of lepidopterous borers on maize and elephant grass in the forest zone of Cameroon. Bulletin of Entomology Research 91 (3): 205–212. DOI: https://doi.org/10.1079/BER200....
 
102.
Nikpay A. 2016. Improving biological control of stalk borers in sugarcane by applying silicon as a soil amendment. Journal of Plant Protection Research 56 (4): 12–22. DOI: https://doi.org/10.1515/jppr-2....
 
103.
Ntiri E.S., Calatayud P.A., van den Berg J., Schulthess F., Le Ru B.P. 2016. Influence of temperature on intra- and interspecific resource utilization within a community of lepidopteran maize stem borers. PLoS ONE 11 (2): 1–19. DOI: https://doi.org/10.1371/journa....
 
104.
Nyukuri R.W., Wanjala F.M., Kirui S.C., Cheramgoi E. 2014. Amage of stem borer species to Zea mays L., Sorghum bicolor L., and three refugia graminae. Advance in Agriculture and Biology 1 (2): 6–11. DOI: https://doi.org/10.15192/pscp.....
 
105.
Oberemok V.V., Kateryna V.L., Yuri I.G., Aleksei S.Z., Palmah M.N. 2015. A short history of insecticides. Journal of Plant Protection Research 55 (3): 221–226. DOI: https://doi.org/10.1515/jppr-2....
 
106.
Okrikata E., Anaso C. 2008. Influence of some inert diluents of neem kernel powder on protection of sorghum against pink stalk borer (Sesemia calamistis, homps) in Nigerian Sudan savanna. Journal of Plant Protection Research 48 (2): 162–168. DOI: https://doi.org/10.2478/v10045....
 
107.
Okweche S.I., Ogunwolu E.O., Adeyemo M.O. 2013. Parameters, interrelationships with yield and use of carbofuran to control stem borers in maize (Zea mays L.) at Makurdi in the Nigerian Southern Guinea Savanna. Greener Journal of Agricultural Sciences 3 (10): 702–708. DOI: https://doi.org/10.15580/gjas.....
 
108.
Omoyo N.N., Wakhungu J., Oteng’i S. 2015. Effects of climate variability on maize yield in the arid and semi arid lands of lower eastern Kenya. Agriculture and Food Security 4 (8): DOI: https://doi.org/10.1186/s40066....
 
109.
Omwega C.O., Muchugu E., Overholt W.A., Schulthess F. 2006. Release and establishment of Cotesia flavipes Cameron (Hymenoptera: Braconidae) an exotic parasitoid of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) in East and Southern Africa. Annales de la Société Entomologique de France (N.S.) 42: 511–518. DOI: https://doi.org/10.1080/003792....
 
110.
Ong’amo G.O., Le Rü B.P., Stéphane D., Pascal M., Eric M., Silvan J.F. 2006. The role of wild host plants in the abundance of lepidopteran stem borers along altitudinal gradient in Kenya. Annales de la Société Entomologique de France (N.S.) 42 (3–4): 363–370. DOI: https://doi.org/10.1080/003792....
 
111.
Otieno N.A., Le Ru B.P., George O.O., Pascal M., Stéphane D. 2008. Diversity and abundance of wild host plants of lepidopteran stem borers in two agro-ecological zones of Kenya. International Journal of Biodiversity Science and Management 4 (2): 92–103. DOI: https://doi.org/10.3843/biodiv....
 
112.
Owiti Z., Zhu W. 2012. Spatial distribution of rainfall seasonality over East Africa. Journal of Geography and Regional Planning 5 (15): 409–421. DOI: https://doi.org/10.5897/jgrp12....
 
113.
Pickett J.A., Woodcock Ch.M., Midega Ch.A.O., Khan Z.R. 2014. Push–pull farming systems. Current Opinion in Biotechnology 26: 125–132. DOI: https://doi.org/10.1016/j.copb....
 
114.
Renner R. 1999. Will Bt-based pest resistance management plans work? Environmental Science and Technology 33 (19): 410–415. DOI: https://doi.org/10.1021/es9930....
 
115.
Resende D.Ch., Mendes S.M., Marucci R.C., de Carvalho Silva A., Campanha M.M., Waquil J.M. 2016. Does Bt maize cultivation affect the non-target insect community in the agro ecosystem? Revista Brasileira de Entomologia 60 (1): 82–93. DOI: https://doi.org/10.1016/j.rbe.....
 
116.
Saxena D., Flores S., Stotzky G. 2002. Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biology and Biochemistry 34 (1): 133–137. DOI: https://doi.org/10.1016/s0038-....
 
117.
Saxena D., Stotzky G. 2001. Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biology and Biochemistry 33 (9): 1225–1230.
 
118.
Saxena D., Stotzky G. 2000. Insecticidal toxin from Bacillus thuringiensis is released from roots of transgenic Bt corn in vitro and in situ. FEMS Microbiology Ecology 33 (1): 35–39. DOI: https://doi.org/10.1111/j.1574....
 
119.
Schulthess F., Bosque-Perez N.A., Chabi-Olaye A., Gounou S., Ndemah R., Goergen G. 1997. Exchange of natural enemies of Lepidopteran cereal stemborers between Africa regions. Insect Science and its Application 17 (1): 97–108. DOI: https://doi.org/10.1017/s17427....
 
120.
Schulthess F., Chabi-Olaye A., Goergen G. 2001. Seasonal fluctuations of noctuid stem borer egg parasitism in southern Benin with special reference to Sesamia calamistis Hampson (Lepidoptera: Noctuidae) and Telenomus spp. (Hymenoptera: Scelionidae) on maize. Biocontrol Science Technology 11 (6): 745–757. DOI: https://doi.org/10.1080/095831....
 
121.
Sears M.K., Hellmich R.L., Stanley-Horn D.E., Oberhauser K.S., Pleasants J.M., Mattila H.R., Siegfriedi B.D., Galen D.P. 2001. Impact of Bt corn pollen on monarch butterfly populations: A risk assessment. Proceedings of the National Academy of Sciences 98 (21): 11937–11942. DOI: https://doi.org/10.1073/pnas.2....
 
122.
Seshu Reddy K.V., Walker P.T. 1990. A review of the yield losses in graminaceous crops caused by Chilo spp. Insect Science and its Application 11 (4–5): 563–569. DOI: https://doi.org/10.1017/s17427....
 
123.
Sezonlin M., Dupas S., Le Rü B., Le Gall P., Moyal P., Calatayud P.A., Giffard I., Faure N., Silvain J.F. 2006. Phylogeography and population genetics of the maize stalk borer Busseola fusca (Lepidoptera, Noctuidae) in sub-Saharan Africa. Molecular Ecology 15 (2): 407–420. DOI: https://doi.org/10.1111/j.1365....
 
124.
Shuangxia J., Nameirakpam D., Singh L., Xianlong Z., Henry D. 2015. Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V-ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa armigera larval development and pupation. Plant Biotechnology Journal 13 (3): 435–446. DOI: https://doi.org/10.1111/pbi.12....
 
125.
Samayoa L.F., Malvar R.A., Butrón A. 2017. QTL for maize midparent heterosis in the heterotic pattern American dent × European flint under corn borer pressure. Frontiers in Plant Science 8: 573. DOI: https://doi.org/10.3389/fpls.2....
 
126.
Songa J.M., Guofa Z., Overholt W.A. 2001. Relationship of stem borer damage and plant physical condition to maize yield in a semi-arid zone of eastern Kenya. Insect Science and its Application 21 (3): 243–249. DOI: https://doi.org/10.1017/s17427....
 
127.
Songa J.M., Overholt W.A., Okello R.O., Mueke J.M. 2002. Control of Lepidopteran stem borers in maize by indigenous parasitoids in semi-arid areas of eastern Kenya. Biological Agriculture and Horticulture 20 (1): 77–90. DOI: https://doi.org/10.1080/014487....
 
128.
Sultan B., Gaetani M. 2016. Agriculture in West Africa in the twenty-first century: climate change and impacts scenarios, and potential for adaptation. Frontiers in Plant Science 7: 1–20. DOI: https://doi.org/10.3389/fpls.2....
 
129.
Tamiru A., Bruce T.J.A., Woodcock C.M., Caulfield J.C., Midega C.A.O., Ogol C.K.P.O., Mayon P., Birkett M.A., Pickett J.A., Khan Z.R. 2011. Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecology Letters 14: 1075–1083. DOI: https://doi.org/10.1111/j.1461....
 
130.
Tamiru A., Getu E., Jembere B., Bruce T. 2012. Effect of temperature and relative humidity on the development and fecundity of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae). Bulletin of Entomological Research, 102 (1): 9–15. DOI: https://doi.org/10.1017/s00074....
 
131.
Tomoyasu Y., Miller S.C., Tomita S., Schoppmeier M., Grossmann D. 2008. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biology 9 (1): R10. DOI: https://doi.org/10.1186/gb-200....
 
132.
Ubuoh E.A., Akhionbare S.M.O., Akhionbare W.N. 2012. Effects of pesticide application on soil microbial spectrum: case study- fecolart demonstration farm. International Journal of Multidisciplinary Sciences and Engineering 3 (2): 34–39.
 
133.
Ullah F., Anwar S., Badshah H., Mashwani M.A., Khan M.H. 2010. Effect of different planting dates of maize on infestation of maize stem borer Chilo partellus (swinhoe) Pyralidae: Lepidoptera. Sarhad Journal of Agriculture 26 (4): 621–625.
 
134.
Urban D., Roberts M.J., Schlenker W., Lobell D.B. 2012. Projected temperature changes indicate significant increase in interannual variability of U.S. maize yields. Climatic Change 112 (2): 525–533. DOI: https://doi.org/10.1007/s10584....
 
135.
Schlenker W., Lobell D.B. 2010. Robust negative impacts of climate change on African agriculture. Environmental Research Letters 5 (1): 14010. DOI: https://doi.org/10.1088/1748-9....
 
136.
van Rensburg J.B.J., Klopper J. 2004. Recurrent selection for resistance in maize to the African stalk borer, Busseola fusca (Fuller). South African Journal of Plant and Soil 21 (1): 59–62. DOI: http://doi.org/10.1080/0257186....
 
137.
van Rensburg J.B.J. 2007. First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. South African Journal of Plant and Soil 24 (3): 147–151. DOI: https://doi.org/10.1080/025718....
 
138.
van den Berg J., van Rensburg J.B.J., Pringle K.L. 1991. Comparative injuriousness of Busseola fusca (Lepidoptera: Noctuidae) and Chilo partellus (Lepidoptera: Pyralidae) on grain sorghum. Bulletin of Entomology Research 82 (2): 137–143. DOI: https://doi.org/10.1017/s00074....
 
139.
Vélez A.M., Khajuria C., Wang H., Narva K.E., Siegfried B.D. 2016. Knockdown of RNA interference pathway genes in western corn rootworms (Diabrotica virgifera virgifera Le Conte) demonstrates a possible mechanism of resistance to lethal dsRNA. PLoS ONE 11 (6): e0157520. DOI: https://doi.org/10.1371/journa....
 
140.
Wang G., Alo C.A. 2012. Changes in precipitation seasonality in West Africa predicted by RegCM3 and the impact of dynamic vegetation feedback. International Journal of Geophysics: 1–10. DOI: https://doi.org/10.1155/2012/5....
 
141.
Wang Y., Zhang H., Li H., Miao X. 2011. Second-generation sequencing supply aneffective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS ONE 6 (4): e18644. DOI: https://doi.org/10.1371/journa....
 
142.
Wang P., He K.L., Wang Z.Y., Wang Y.L. 2012. Evaluating transgenic Cry1Ac maize for resistance to Ostrinia furnacalis (Guenée). Acta Phytophylacica Sinica 5: 395–400.
 
143.
Wang Y., Kang-La H., Jiang F., Wang Y., Zhang T., Wang Z., ShuXion B. 2014. Resistance of transgenic Bt corn variety BT-799 to the Asian corn borer. Chinese Journal of Applied Entomology 3: 636–642.
 
144.
Whangbo J.S., Hunter C.P. 2008. Environmental RNA interference. Trends in Genetics 24 (6): 297–305. DOI: 10.1016/j.tig.2008.03.007.
 
145.
Willcox M.C., Khairallah M.M., Bergvinson D., Crossa J., Deutsch J.A., Edmeades G.O., González-de-León D., Jiang C., Jewell D.C., Mihm J.A., Williams W.P., Hoisington D. 2002. Selection for resistance to southwestern corn borerusing marker-assisted and conventional backcrossing. Crop Science 42 (5): 1516–1528. DOI: https://doi.org/10.2135/cropsc....
 
146.
Woiwod I.P. 1997. Detecting the effects of climate change on Lepidoptera. Journal of Insect Conservation 1: 149–158.
 
147.
Wu F.C. 2014. Evaluated of transgenic maize for resistance to the Ostrinia furnacalis. Journal of Maize Science 6: 148–150.
 
148.
Xu H., Twine T.E., Girvetz E. 2016. Climate change and maize yield in Iowa. PLoS ONE 11 (5): 1–20. DOI: https://doi.org/10.1371/journa....
 
149.
Yang Z., Lang Z., Zhang J. 2012. Studies on insect-resistant transgenic maize (Zea mays L.) harboring Bt cry1Ah and cry1Ie genes. Journal of Agricultural Science and Technology 4: 39–45.
 
150.
Yang G., You M., Vasseur L., Zhao Y., Liu C. 2011. Development of RNAi ininsects and rnai-based pest control, pesticides. p. 27–38. In: “Pesticides in the Modern World – Pests Control and Pesticides Exposure and Toxicity Assessment” (M. Stoytcheva, ed.). INTECH, USA. DOI: 10.5772/17260.
 
151.
Zahid S., Javed I., Sabir G.K., Muhammad K., Niaz M., Zahid I., Fahim U. Khan., Hina F. 2012. Effect of different insecticides against maize stem borer infestation at Barani Agricultural Research Station, Kohat, KPK Pakistan. International Journal of Life Sciences Research 2 (1): 23–26.
 
152.
Zhang J., Sher A.K., Claudia H., Stephanie R., David G., Heckel R.B. 2015. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347 (6225): 991–994. DOI: https://doi.org/10.1126/scienc....
 
153.
Zhang X., Candas M., Griko N.B., Taussig R., Bulla L.A. 2006. A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proceedings of National Academy of Science 103 (26): 9897–9902. DOI: https://doi.org/10.1073/pnas.0....
 
154.
Zhang Y., Zhao Y., Chen S., Guo J., Wang E. 2015. Prediction of maize yield response to climate change with climate and crop model uncertainties. Journal of Applied Meteorology and Climatology 54 (4): 785–794. DOI: https://doi.org/10.1175/jamc-d....
 
155.
Zhou G., Baumgartner J., Overholt W.A. 2001. Impact of an exotic parasitoid on stemborer (Lepidoptera) populations dynamics in Kenya. Ecological Applications 11 (5): 1554–1559. DOI: https://doi.org/10.2307/306093....
 
156.
Zhou G., Overholt W.A., Kimani-Njogu S.W. 2003. Species richness and parasitism in assemblage of parasitoids attacking maize stem borer in coastal Kenya. Ecology Entomology 28 (1): 109–118. DOI: https://doi.org/10.1046/j.1365....
 
157.
Zhu J.Q., Liu S., Ma Y., Zhang J.Q., Qi H.S., Wei Z.J., Yao Q., Zhang W.Q., Li S. 2012. Improvement of pest resistance in transgenic tobacco plants expressing dsRNA of an insectassociated gene EcR. PLoS ONE 7 (6): e38572. DOI: https://doi.org/10.1371/journa....
 
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