The authors gratefully acknowledged the financial support for this research by the following organizations and agencies: UK's Foreign, Commonwealth & Development Office (FCDO), the Swedish International Development Cooperation Agency (Sida), the Swiss Agency for Development and Cooperation (SDC), the Federal Democratic Republic of Ethiopia, and the Government of the Republic of Kenya. For tephritid fruit fly management, biopesticides can be used for soil application, as a killing agent in bait sprays or in a lure-and-infect approach with attractants in a package that includes monitoring, the use of parasitoids, orchard sanitation, postharvest technologies, bait sprays and male annihilation technology. Strains belonging to this genus are relatively easy to mass-produce, formulate and apply, and were found to be among the most virulent against Africa's pests. A trial of a cypermethrin 'pour-on' insecticide to control Glossina pallipes, G. fuscipes and G. morsitans submorsitans (Diptera: Glossinidae) in south-west Ethiopia. J. and Duboscqia sp.). Recent pest resurgence and persistence, partly caused by widespread resistance to synthetic pesticides, has raised major concerns in the region (Potter, 2004; Fourie and Crafford, 2018). acridum strain IMI 330189, which is highly effective for controlling S. gregaria (Bateman et al., 2017). icipe's public-private partnerships are expanding to include other commercial companies. Do farmers and the environment benefit from adopting integrated pest management practices? Current status and recent developments in biopesticide use. For S. frugiperda, biopesticide development is targeted at all life stages of the pest in a package that includes effective monitoring, conservation of natural enemies and diversified cropping systems. Through public-private partnerships, icipe has developed and commercialized some biopesticides to tackle pests and vectors on crop and livestock systems that contributes to reduction in synthetic pesticides use and positively impact on animal, human and environmental health. in the pastoral zone of Samorogouan, Burkina-Faso. Further, the use of IPM, including biopesticides, generates positive effects on human health and the environment by reducing the environmental impact quotient (EIQ) by 940% (Midingoyi et al., 2019; Mwungu et al., 2020). Entomol. 2013:9. doi: 10.1155/2013/465213, Nyangau, P., Muriithi, B., Nzuma, J., Irungu, P., Gichungi, H., and Diiro, G. (2020). doi: 10.1016/j.micpath.2019.04.010, Oundo, J. W., Villinger, J., Jeneby, M., Ong'amo, G., Otiende, M. Y., Makhulu, E. E., et al. (2020) observed that Sodalis sp. Microbial characterisation of the edible grasshopper Ruspolia differens in raw condition after wild-harvesting in Uganda. Metarhizium anisopliae and Beauveria bassiana: pathogenicity, horizontal transmission, and their effects on reproductive potential of Thaumatotibia leucotreta (Lepidoptera: Tortricidae). Biopesticides are generally less toxic than conventional pesticides and therefore considered safer for human health. Five B. bassiana strains (ICIPE 284, ICIPE 279, ICIPE 281, G1LU3 and S4SU1) are being tested against S. frugiperda, T. leucotreta and Liriomyza sp. AAIS 23rd Biannual Meeting and Scientific Conference, Abidjan, Ivory Coast, 1823 November 2019 (Nairobi, Kenya: AAIS). The choice of rearing substrate is crucial, coupled with pre-treatment or sterilization of organic waste substrates before usage as well as postharvest treatments of H. illucens larvae (Khamis et al., 2019). Protecting cows in small holder farms in East Africa from tsetse flies by mimicking the odor profile of a non-host bovid. Biological pesticides for Africa: why has so little research led to new products to help africa's poor? Res. Efficacy will also be tested on diverse groups of tick species in varied ecologies, while the effect of infection on vector transmission will be studied. Recently, icipe is expanding R4D toward plant endophytes and rhizosphere inhabitants. Int. 48, 3740. J. For tsetse management, the lure-and-infect approach will be fine-tuned by combining biopesticides based on M. anisopliae strain ICIPE 30 with odor-baited traps in auto-dissemination devices and repellent collars. Development of novel biopesticides against animal pests and disease vectors focuses on G. fuscipes fuscipes (Maniania, 1998, 2002; Maniania et al., 2006). 165, 5466. During the 1990's, small-scale mass production of several insect pathogens was implemented: Hirsutella thompsoni for cassava green mite management; Nosema marucae for management of the Asian stemborer Chilo suppressalis and M. vitrata (Maniania, 1993); Metarhizium anisopliae and Beauveria bassiana for management of locusts, maize stemborers, ticks and tsetse flies; B. thuringiensis for management of the spotted stalk borer Chilo partellus, mosquitoes and filth flies; and baculoviruses for management of S. exempta. 70, 452470. (2013). J. Pest Sci. Currently, biopesticide R4D is fully integrated into buy's 4H paradigm, comprising plant, animal, environmental and human health. doi: 10.1093/jee/toz342, Mnyone, L. L., Kirby, M. J., Mpingwa, M. W., Lwetoijera, D. W., Knols, B. G., Takken, W., et al.
PLoS ONE 9:e109965. (2017). and polydnavirus in the indigenous stemborer parasitoid Cotesia sesamiae influences its biological control effectiveness against maize stemborers (Ngi-Song and Mochiah, 2001; Dupas et al., 2008).
217, 3450. Another immediate research thrust is expansion of the biopesticide portfolio toward animal and human diseases and vectors. doi: 10.1111/1477-9552.12306, Migiro, L. N., Maniania, N. K., Chabi-Olaye, A., and Vandenberg, J.
(2010). In the absence of effective alternative management options to tackle these pests and vectors, there is extensive dependence on synthetic pesticides for their management on crop and livestock systems, with significant negative impacts on animal and human health, and the environment. Successful application of deltamethrin pour onto cattle in a campaign against tsetse flies (Glossina spp.) Use of Metarhizium anisopliae chitinase genes for genotyping and virulence characterization. 15, 1426. 96, 3442. research articulado Currently, screening efforts are expanding beyond M. anisopliae toward other entomopathogenic fungi such as B. bassiana and Isaria fumosorosea, bacteria, microsporidia, nematodes and viruses. doi: 10.1111/jen.12634, Akutse, K. S., Maniania, N. K., Fiaboe, K. K. M., Van den Berg, J., and Ekesi, S. (2013). The manuscript was written by KA, TD, and SS.
biopesticides azadirachtin structure pests Akello, J., Dubois, T., Gold, C. S., Nakavuma, J, and Paparu, P. (2007). Branca, A., Le Ru, B., Calatayud, P. A., Obonyo, J., Musyoka, B., Capdevielle-Dulac, C., et al. has been discovered in Anopheles arabiensis (Chepkemoi, 2016) and A. gambiae (Chepkemoi et al., 2017), major vectors of Plasmodium sp. metarhizium biopesticide encapsulation Pathogenesis 131, 197204. doi: 10.1007/s10886-012-0207-6, Mburu, D. M., Ochola, L., Maniania, N. K., Njagi, P. G., Gitonga, L. M., Ndung'u, M. W., et al. Arthropod pathogen germplasm repository at the International Centre of Insect Physiology and Ecology (icipe) for biopesticides development. In Kenya, collaboration has been excellent with the Pest Control Products Board and the Directorate of Veterinary Services. (2020). Metarhizium anisopliae strain ICIPE 69 is effective against thrips, fruit flies and mealybugs; M. anisopliae strain ICIPE 78 is effective against T. urticae; M. anisopliae strain ICIPE 62 is effective against aphids. Entomol. Through collaborative R4D activities, icipe subsequently supports further enhancement of product effectiveness and use (e.g., development of autodissemination approaches, improvements in formulation and integration with other IPM options). These biopesticides were applied on >89,000 ha and nearly 133,000 ha in 2019 and 2020, respectively, indicating an exponentially expanding coverage (Figure 1). Le pige pyramidal tsetse (Diptera, Glossinidae) pour la capture et la lutte. and Globodera sp. doi: 10.1016/j.micres.2018.08.016, Bamisope, S. B., Dash, C. K., Akutse, K. S., Keppanan, R., and Wang, L. (2018b). The global market for biopesticides is valued at 3.0 billion USD, accounting for 5% of the global pesticide market (Marrone, 2014). Biocontrol 61, 741753. Arthropod vector-borne diseases inflict more than 700,000 deaths annually, with mosquito-transmitted malaria alone causing 400,000 deaths globally. Oladunmade, M. A., Feldmann, U., Takken, W., Tenabe, S. O., Hamann, H. J., Onah, J., et al. J. Invertebr. During the registration process, icipe, in collaboration with the private sector and accredited good laboratory practice (GLP) laboratories, facilitates the generation of required eco- and mammalian toxicity test data, and assures quality. PLoS Negl. 127, 11511154. Management of ticks is largely undertaken with acaricides, which is increasingly becoming ineffective due to high levels of acaricide resistance. Marrone, P. G. (2014). Biopesticides are effective and environmentally sustainable alternatives to synthetic pesticides. *Correspondence: Thomas Dubois, tdubois@icipe.org, Entomopathogens for Sustainable Food Production, Front. Using a lure-and-infect approach, M. anisopliae strain ICIPE 30 has been integrated with odor-baited traps, and reduced Trypanosoma congolensis reproduction in G. fuscipes fuscipes and its ability to acquire or transmit the parasite. This is attributed largely to more efficient R4D related to product development, better interactions with regulatory authorities and policy makers, and stronger engagement with the private sector and partnership arrangements to identify market needs.
Building youth and women entrepreneurship for small-scale biopesticide production are planned for the future. 6 Articles, This article is part of the Research Topic, History of Biopesticide Research-for-Development at, Biopesticide Research as a Function of Targets, Biopesticide Development and Commercialization, Partnerships, Scaling and Capacity Building, Integration of Biopesticide Research into IPM, https://doi.org/10.3389/fsufs.2020.563016, https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases, Creative Commons Attribution License (CC BY), International Center of Insect Physiology and Ecology (icipe), Nairobi, Kenya. Mwungu, C. M., Muriithi, B., Ngeno, V., Affognon, H., Githiomi, C., Diiro, G., et al. A recent research thrust centers on endophytes such as Hypocrea lixii and Trichoderma sp. Ticks (Rhipicephalus sp., Boophilus sp., Amblyomma sp.) In most cases, field efficacy trials and product formulation are conducted with private sector partners. At present, icipe's APU is a reference point for biopesticide development in sub-Saharan Africa, with a unique facility, state-of-art equipment and excellent human resources to carry out biopesticide R4D. icipe has actively engaged in research to identify virulent entomopathogens of these pests, with a greater emphasis on entomopathogenic fungi belonging to the genera of Metarhizium sp. doi: 10.1007/s10340-015-0645-3, Muvea, A. M., Meyhfer, R., Subramanian, S., Poehling, H. M., Ekesi, S., and Maniania, N. K. (2014). However, most edible insects are harvested from the wild, which may result in food safety issues for consumers. Received: 17 May 2020; Accepted: 17 August 2020; Published: 30 September 2020. biopesticides agreements diversification doi: 10.1017/S1742758414000605, Wamiti, L. G., Khamis, F. M., Abd-alla, A. M. M., Ombura, F. L. O., Akutse, K. S., Subramanian, S., et al. Distinct strains of endosymbiotic Spiroplasma sp. Following the detection of S. frugiperda in Africa, a great effort was placed on screening strains for control of this debilitating pest. Relative influence of host, Wolbachia, geography and climate on the genetic structure of the Sub-Saharan parasitic wasp Cotesia sesamiae. Parasitol. 55, 774780. An analysis of the biopesticide market now and where is going. Endophytes such as Hypocrea lixii strain F3ST1, Trichoderma harzianum strain ICIPE 709, Clonostachys rosea strain ICIPE 707 and Trichoderma atroviride strain ICIPE 710 were found to be effective against Liriomyza sp., T. absoluta, the onion thrips Thrips tabaci and O. phaseoli, as well as the plant viruses iris yellow spot virus (IYSV) and sugarcane mosaic virus (SCMV) (Akutse et al., 2013, 2014; Muvea et al., 2014, 2015, 2018; Mutune et al., 2016). The use of biopesticides needs to be fully integrated into an IPM approach. (1990). For subsequent socio-economic impact studies, icipe will strive to undertake holistic assessments of socio-economic impacts of biopesticides use. Biological control and biorational pesticides for fall armyworm management, in Fall Armyworm in Africa: A Guide for Integrated Pest Management, eds B. M. Prasanna, J. E. Huesing, R. Eddy, V. M. Peschke (Texcoco: CYMMIT), 6388. Food Microbiol. J. Invertebr. Entomol. Ecol. Focus has equally shifted toward fungi other than M. anisopliae. Front. Systematic bioprospecting for arthropod pathogens began in the 1980's leading to the establishment of an arthropod pathogen germplasm repository in 1992. Horizontal transmission of Metarhizium anisopliae between Spoladea recurvalis (Lepidoptera: Crambidae) adults and compatibility of the fungus with the attractant phenylacetaldehyde. Currently, the most virulent strains are assessed for non-target effects on natural enemies and formulations are fine-tuned for optimal field applications as a function of life stage, with field efficacy evaluation and fast-tracking of registration or label extension envisaged during 2020. soybean tabaci varieties biopesticide pests 10, 343335. icipe's future R4D thrusts include (1) developing high-throughput screening and bioassays models for rapid selection of potent biopesticide strains; (2) expanding public-private partnerships and develop biopesticides targeting emerging and invasive pests such as S. frugiperda and S gregaria; (3) expanding the portfolio of research on animal and human disease vectors, and broaden biopesticide arsenal toward bacterial, entomopathogenic nematode-, endophytes and virus-based biopesticides; (4) harnessing the benefit of IPM and pollination services; (4) build youth and women entrepreneurship for biopesticide production; and (5) assessing socioeconomic impacts of biopesticide use and inform policy makers for regional harmonization of policies enabling biopesticide registration and use. Recently, extensive bioprospecting for plant endophytes has resulted in the identification of several strains against diverse pest constraints such as Liriomyza leafminers, thrips and the bean fly Ophiomyia phaseoli. R4D into insects for food and feed is of growing interest and a new foray in which icipe has taken a lead for sub-Saharan Africa. Diverse Wolbachia sp. Biopesticides may offer an essential alternative to the indiscriminate use of synthetic pesticides. as an endophyte in beans in the laboratory and field (Akutse et al., 2013; Gathage et al., 2016), and T. asperellum strain M2RT4, H. lixii strain F3ST1, and B. bassiana strains ICIPE273 and G1LU3 controlled O. phaseoli in beans after seed inoculation (Mutune et al., 2016). doi: 10.1016/j.cropro.2015.11.014, Mutune, B., Ekesi, S., Niassy, S., Matiru, V., Bii, C., and Maniania, N. K. (2016). 9:168. doi: 10.1186/1475-2875-9-168. Ecol. Acarol. (2011). (2020). doi: 10.4001/003.026.0073, Tumuhaise, V., Ekesi, S., Mohamed, S. A., Ndegwa, P. N., Irungu, L. W., Srinivasan, R., et al. Unexpected diversity of Wolbachia associated with Bactrocera dorsalis (Diptera: Tephritidae) in Africa. Green Muscle as well as the novel product Novacrid based on Metarhizium acridum strain EVCH 077 are commercialized and marketed by Elephant Vert. Outlook. However, a realistic comparison of biopesticides with synthetic pesticides should include cost associated with negative externalities of synthetic pesticide use, altered pricing of safer products from biopesticide use and social impacts related to employment generation. Mburu, D. M., Maniania, N. K., and Hassanali, A. Bed bugs, for example, produce large amounts of histamine as a component of their aggregation pheromone, which offers possibilities to include attractants into biopesticide products (Gries et al., 2015). 
These techniques have various limitations ranging from their efficacy, economically viability and environmental sustainability. The private sector is an essential partner, and collaboration has been and is strong with Real IPM, leading to the registration and development of several biopesticide products and application technologies. Trop. doi: 10.1006/bcon.1997.0580, Maniania, N. K. (2002). PeerJ 8:e8701. Econom. doi: 10.1007/s10526-016-9761-0, Gichuhi, J., Subramanian, S., Khamis, F., Van den Berg, J., Du Plessis, H., Ekesi, S., et al. For management of T. absoluta, biopesticides are being developed that target adults as well as induce systemic resistance through endophytic activity against larvae. In addition, key entomopathogens of reared insects for human food and animal feed need to be identified and controlled through high hygiene standards during rearing. Together with NARES and NGOs, biopesticides are scaled with farmers as part of comprehensive IPM packages. Recently, icipe has demonstrated that the vertically transmitted microsporidian symbiont Microsporidia MB in A. arabiensis can impair Plasmodium sp. Parasit. For thrips, such as Frankliniella occidentalis, T. tabaci and Megalurothrips sjostedti, biopesticides can target both larval and adult stages as direct sprays, lure-and-infect application and as endophytes enhancing systemic resistance as part of a package comprised of resistant cultivars, habitat management, the use of healthy seeds and seedlings, and the use of kairamones and pheromones for effective monitoring. Furthermore, application technologies such as lure-and-infect using pheromones may better target pests and avoid contact with bees. doi: 10.1007/BF02059896, Tumuhaise, V., Ekesi, S., Maniania, N. K., Tonnang, H. E. Z., Tanga, C. M., Ndegwa, P. N., et al. Critical insect stage- and population-dependent differences in gut bacterial communities have also been reported in S. frugiperda in Kenya (Gichuhi et al., 2020). Formulation and integration with pheromones or attractants will need to be a major focus to tackle these cryptic pests. J. Trop. Research on biopesticides for mosquito (Anopheles gambiae and Aedes aegypti) management prior to the 2000's largely focused on bioprospecting for Bt, Coelomomyces sp. Furthermore, M. anisopliae strain ICIPE 7 was found to be equally effective against both acaricide-resistant and -susceptible tick populations (Murigu et al., 2016). Most of these deaths occur in Africa and are exacerbated due to lack of capacity to effectively manage the vectors and the diseases they carry. Kibira, M., Affognon, H., Njehia, B., Muriithi, B., and Ekesi, S. (2015). biopesticide physiology r4d icipe Wolbachia sp. Resour. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). No use, distribution or reproduction is permitted which does not comply with these terms. Entomol. doi: 10.1564/20feb00, Hatting, J. L., Moore, S. D., and Maland, A. P. (2019). Sustain. Performance of a Metarhizium anisopliae-treated semiochemical-baited trap in reducing Amblyomma variegatum populations in the field. All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. Based on icipe's large arthropod pathogen repository, diverse strains are mass-screened against key target pest in laboratory bioassays. (2017). Technol. Concurrently, research focused on innovative formulations (oil-based, granular and dry spore formulations) and development of novel application strategies such as lure-and-infect, spot-sprays and autodissemination. Control 11, 248254. icipe formalized research into entomopathogens and its application for pest management with the establishment of the Insect Pathology and Pest Management Program in 1982, which subsequently transformed in the Pathology and Microbiology Department in 1994 and finally into the Arthropod Pathology Unit (APU) in 1999. Prospects of a fungus-contamination device for the control of tsetse fly Glossina fuscipes. WHO (2020). All these biopesticides are based and marketed by Real IPM and its subsidiaries across sub-Saharan Africa and beyond.
R4D against animal pests and disease vectors will soon yield registration of a first product based on M. anisopliae strain ICIPE 7. Based on long-standing experience in developing M. anisopliae into biopesticides, the time taken from identification of virulent strains to commercialization as biopesticide products has considerably shortened. 77, 106117. J. Insights in the global genetics and gut microbiome of black soldier fly, Hermetia illucens: implications for animal feed safety control.
Vectors 3:80. doi: 10.1186/1756-3305-3-80. ecourse uoi 169, 367372. Biopesticides: Pest Management and Regulation (Wallingford, UK: CABI). 
86, 285292.
The focus of icipe's APU has gradually transformed from basic to applied research leading to innovative, commercial products. (2018). There is a growing interest toward understanding the role of symbionts in modulating multitrophic interactions between plants, pests and their natural enemies, and exploring their role in biological control. However, as the insect for food and feed industry takes hold, it is to be expected that entomopathogens will become a problem of large-scale rearing facilities. J. Hered. Ovicidal effects of entomopathogenic fungal isolates on the invasive fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). For instance, presence of Wolbachia sp. 81, 2029. Targets included major invasive and indigenous pests of staples, legumes, vegetables and fruit crops, as well as livestock pests such as ticks and tsetse flies. So far, a total of 8,175,957 mango growers benefited, including 49,739 growers who directly benefited through hands-on training and received IPM starter packs, 627,200 growers who benefited through parasitoid releases and 6,499,018 growers who indirectly benefited through interaction with trained growers, extension officers, NGOs and communities service providers. doi: 10.1007/s10340-012-0473-7. doi: 10.1017/S0007485300034325, Makhulu, E. E., Villinger, J., Adunga, V. O., Jeneby, M. M., Kimathi, E. M., Mararo, E., et al. Current research at icipe on avocado focuses on selection of M. anisopliae strains against tephritid fruit flies and T. leucotreca that are not pathogenic to the Western honey bee Apis mellifera and the stingless bee Meliponula ferruginea. Food Syst., 30 September 2020, View all
PLoS ONE 9:e109965. (2017). and polydnavirus in the indigenous stemborer parasitoid Cotesia sesamiae influences its biological control effectiveness against maize stemborers (Ngi-Song and Mochiah, 2001; Dupas et al., 2008). 217, 3450. Another immediate research thrust is expansion of the biopesticide portfolio toward animal and human diseases and vectors. doi: 10.1111/1477-9552.12306, Migiro, L. N., Maniania, N. K., Chabi-Olaye, A., and Vandenberg, J.
(2010). In the absence of effective alternative management options to tackle these pests and vectors, there is extensive dependence on synthetic pesticides for their management on crop and livestock systems, with significant negative impacts on animal and human health, and the environment. Successful application of deltamethrin pour onto cattle in a campaign against tsetse flies (Glossina spp.) Use of Metarhizium anisopliae chitinase genes for genotyping and virulence characterization. 15, 1426. 96, 3442. research articulado Currently, screening efforts are expanding beyond M. anisopliae toward other entomopathogenic fungi such as B. bassiana and Isaria fumosorosea, bacteria, microsporidia, nematodes and viruses. doi: 10.1111/jen.12634, Akutse, K. S., Maniania, N. K., Fiaboe, K. K. M., Van den Berg, J., and Ekesi, S. (2013). The manuscript was written by KA, TD, and SS.
biopesticides azadirachtin structure pests Akello, J., Dubois, T., Gold, C. S., Nakavuma, J, and Paparu, P. (2007). Branca, A., Le Ru, B., Calatayud, P. A., Obonyo, J., Musyoka, B., Capdevielle-Dulac, C., et al. has been discovered in Anopheles arabiensis (Chepkemoi, 2016) and A. gambiae (Chepkemoi et al., 2017), major vectors of Plasmodium sp. metarhizium biopesticide encapsulation Pathogenesis 131, 197204. doi: 10.1007/s10886-012-0207-6, Mburu, D. M., Ochola, L., Maniania, N. K., Njagi, P. G., Gitonga, L. M., Ndung'u, M. W., et al. Arthropod pathogen germplasm repository at the International Centre of Insect Physiology and Ecology (icipe) for biopesticides development. In Kenya, collaboration has been excellent with the Pest Control Products Board and the Directorate of Veterinary Services. (2020). Metarhizium anisopliae strain ICIPE 69 is effective against thrips, fruit flies and mealybugs; M. anisopliae strain ICIPE 78 is effective against T. urticae; M. anisopliae strain ICIPE 62 is effective against aphids. Entomol. Through collaborative R4D activities, icipe subsequently supports further enhancement of product effectiveness and use (e.g., development of autodissemination approaches, improvements in formulation and integration with other IPM options). These biopesticides were applied on >89,000 ha and nearly 133,000 ha in 2019 and 2020, respectively, indicating an exponentially expanding coverage (Figure 1). Le pige pyramidal tsetse (Diptera, Glossinidae) pour la capture et la lutte. and Globodera sp. doi: 10.1016/j.micres.2018.08.016, Bamisope, S. B., Dash, C. K., Akutse, K. S., Keppanan, R., and Wang, L. (2018b). The global market for biopesticides is valued at 3.0 billion USD, accounting for 5% of the global pesticide market (Marrone, 2014). Biocontrol 61, 741753. Arthropod vector-borne diseases inflict more than 700,000 deaths annually, with mosquito-transmitted malaria alone causing 400,000 deaths globally. Oladunmade, M. A., Feldmann, U., Takken, W., Tenabe, S. O., Hamann, H. J., Onah, J., et al. J. Invertebr. During the registration process, icipe, in collaboration with the private sector and accredited good laboratory practice (GLP) laboratories, facilitates the generation of required eco- and mammalian toxicity test data, and assures quality. PLoS Negl. 127, 11511154. Management of ticks is largely undertaken with acaricides, which is increasingly becoming ineffective due to high levels of acaricide resistance. Marrone, P. G. (2014). Biopesticides are effective and environmentally sustainable alternatives to synthetic pesticides. *Correspondence: Thomas Dubois, tdubois@icipe.org, Entomopathogens for Sustainable Food Production, Front. Using a lure-and-infect approach, M. anisopliae strain ICIPE 30 has been integrated with odor-baited traps, and reduced Trypanosoma congolensis reproduction in G. fuscipes fuscipes and its ability to acquire or transmit the parasite. This is attributed largely to more efficient R4D related to product development, better interactions with regulatory authorities and policy makers, and stronger engagement with the private sector and partnership arrangements to identify market needs. 
Building youth and women entrepreneurship for small-scale biopesticide production are planned for the future. 6 Articles, This article is part of the Research Topic, History of Biopesticide Research-for-Development at, Biopesticide Research as a Function of Targets, Biopesticide Development and Commercialization, Partnerships, Scaling and Capacity Building, Integration of Biopesticide Research into IPM, https://doi.org/10.3389/fsufs.2020.563016, https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases, Creative Commons Attribution License (CC BY), International Center of Insect Physiology and Ecology (icipe), Nairobi, Kenya. Mwungu, C. M., Muriithi, B., Ngeno, V., Affognon, H., Githiomi, C., Diiro, G., et al. A recent research thrust centers on endophytes such as Hypocrea lixii and Trichoderma sp. Ticks (Rhipicephalus sp., Boophilus sp., Amblyomma sp.) In most cases, field efficacy trials and product formulation are conducted with private sector partners. At present, icipe's APU is a reference point for biopesticide development in sub-Saharan Africa, with a unique facility, state-of-art equipment and excellent human resources to carry out biopesticide R4D. icipe has actively engaged in research to identify virulent entomopathogens of these pests, with a greater emphasis on entomopathogenic fungi belonging to the genera of Metarhizium sp. doi: 10.1007/s10340-015-0645-3, Muvea, A. M., Meyhfer, R., Subramanian, S., Poehling, H. M., Ekesi, S., and Maniania, N. K. (2014). However, most edible insects are harvested from the wild, which may result in food safety issues for consumers. Received: 17 May 2020; Accepted: 17 August 2020; Published: 30 September 2020. biopesticides agreements diversification doi: 10.1017/S1742758414000605, Wamiti, L. G., Khamis, F. M., Abd-alla, A. M. M., Ombura, F. L. O., Akutse, K. S., Subramanian, S., et al. Distinct strains of endosymbiotic Spiroplasma sp. Following the detection of S. frugiperda in Africa, a great effort was placed on screening strains for control of this debilitating pest. Relative influence of host, Wolbachia, geography and climate on the genetic structure of the Sub-Saharan parasitic wasp Cotesia sesamiae. Parasitol. 55, 774780. An analysis of the biopesticide market now and where is going. Endophytes such as Hypocrea lixii strain F3ST1, Trichoderma harzianum strain ICIPE 709, Clonostachys rosea strain ICIPE 707 and Trichoderma atroviride strain ICIPE 710 were found to be effective against Liriomyza sp., T. absoluta, the onion thrips Thrips tabaci and O. phaseoli, as well as the plant viruses iris yellow spot virus (IYSV) and sugarcane mosaic virus (SCMV) (Akutse et al., 2013, 2014; Muvea et al., 2014, 2015, 2018; Mutune et al., 2016). The use of biopesticides needs to be fully integrated into an IPM approach. (1990). For subsequent socio-economic impact studies, icipe will strive to undertake holistic assessments of socio-economic impacts of biopesticides use. Biological control and biorational pesticides for fall armyworm management, in Fall Armyworm in Africa: A Guide for Integrated Pest Management, eds B. M. Prasanna, J. E. Huesing, R. Eddy, V. M. Peschke (Texcoco: CYMMIT), 6388. Food Microbiol. J. Invertebr. Entomol. Ecol. Focus has equally shifted toward fungi other than M. anisopliae. Front. Systematic bioprospecting for arthropod pathogens began in the 1980's leading to the establishment of an arthropod pathogen germplasm repository in 1992. Horizontal transmission of Metarhizium anisopliae between Spoladea recurvalis (Lepidoptera: Crambidae) adults and compatibility of the fungus with the attractant phenylacetaldehyde. Currently, the most virulent strains are assessed for non-target effects on natural enemies and formulations are fine-tuned for optimal field applications as a function of life stage, with field efficacy evaluation and fast-tracking of registration or label extension envisaged during 2020. soybean tabaci varieties biopesticide pests 10, 343335. icipe's future R4D thrusts include (1) developing high-throughput screening and bioassays models for rapid selection of potent biopesticide strains; (2) expanding public-private partnerships and develop biopesticides targeting emerging and invasive pests such as S. frugiperda and S gregaria; (3) expanding the portfolio of research on animal and human disease vectors, and broaden biopesticide arsenal toward bacterial, entomopathogenic nematode-, endophytes and virus-based biopesticides; (4) harnessing the benefit of IPM and pollination services; (4) build youth and women entrepreneurship for biopesticide production; and (5) assessing socioeconomic impacts of biopesticide use and inform policy makers for regional harmonization of policies enabling biopesticide registration and use. Recently, extensive bioprospecting for plant endophytes has resulted in the identification of several strains against diverse pest constraints such as Liriomyza leafminers, thrips and the bean fly Ophiomyia phaseoli. R4D into insects for food and feed is of growing interest and a new foray in which icipe has taken a lead for sub-Saharan Africa. Diverse Wolbachia sp. Biopesticides may offer an essential alternative to the indiscriminate use of synthetic pesticides. as an endophyte in beans in the laboratory and field (Akutse et al., 2013; Gathage et al., 2016), and T. asperellum strain M2RT4, H. lixii strain F3ST1, and B. bassiana strains ICIPE273 and G1LU3 controlled O. phaseoli in beans after seed inoculation (Mutune et al., 2016). doi: 10.1016/j.cropro.2015.11.014, Mutune, B., Ekesi, S., Niassy, S., Matiru, V., Bii, C., and Maniania, N. K. (2016). 9:168. doi: 10.1186/1475-2875-9-168. Ecol. Acarol. (2011). (2020). doi: 10.4001/003.026.0073, Tumuhaise, V., Ekesi, S., Mohamed, S. A., Ndegwa, P. N., Irungu, L. W., Srinivasan, R., et al. Unexpected diversity of Wolbachia associated with Bactrocera dorsalis (Diptera: Tephritidae) in Africa. Green Muscle as well as the novel product Novacrid based on Metarhizium acridum strain EVCH 077 are commercialized and marketed by Elephant Vert. Outlook. However, a realistic comparison of biopesticides with synthetic pesticides should include cost associated with negative externalities of synthetic pesticide use, altered pricing of safer products from biopesticide use and social impacts related to employment generation. Mburu, D. M., Maniania, N. K., and Hassanali, A. Bed bugs, for example, produce large amounts of histamine as a component of their aggregation pheromone, which offers possibilities to include attractants into biopesticide products (Gries et al., 2015). 
These techniques have various limitations ranging from their efficacy, economically viability and environmental sustainability. The private sector is an essential partner, and collaboration has been and is strong with Real IPM, leading to the registration and development of several biopesticide products and application technologies. Trop. doi: 10.1006/bcon.1997.0580, Maniania, N. K. (2002). PeerJ 8:e8701. Econom. doi: 10.1007/s10526-016-9761-0, Gichuhi, J., Subramanian, S., Khamis, F., Van den Berg, J., Du Plessis, H., Ekesi, S., et al. For management of T. absoluta, biopesticides are being developed that target adults as well as induce systemic resistance through endophytic activity against larvae. In addition, key entomopathogens of reared insects for human food and animal feed need to be identified and controlled through high hygiene standards during rearing. Together with NARES and NGOs, biopesticides are scaled with farmers as part of comprehensive IPM packages. Recently, icipe has demonstrated that the vertically transmitted microsporidian symbiont Microsporidia MB in A. arabiensis can impair Plasmodium sp. Parasit. For thrips, such as Frankliniella occidentalis, T. tabaci and Megalurothrips sjostedti, biopesticides can target both larval and adult stages as direct sprays, lure-and-infect application and as endophytes enhancing systemic resistance as part of a package comprised of resistant cultivars, habitat management, the use of healthy seeds and seedlings, and the use of kairamones and pheromones for effective monitoring. Furthermore, application technologies such as lure-and-infect using pheromones may better target pests and avoid contact with bees. doi: 10.1007/BF02059896, Tumuhaise, V., Ekesi, S., Maniania, N. K., Tonnang, H. E. Z., Tanga, C. M., Ndegwa, P. N., et al. Critical insect stage- and population-dependent differences in gut bacterial communities have also been reported in S. frugiperda in Kenya (Gichuhi et al., 2020). Formulation and integration with pheromones or attractants will need to be a major focus to tackle these cryptic pests. J. Trop. Research on biopesticides for mosquito (Anopheles gambiae and Aedes aegypti) management prior to the 2000's largely focused on bioprospecting for Bt, Coelomomyces sp. Furthermore, M. anisopliae strain ICIPE 7 was found to be equally effective against both acaricide-resistant and -susceptible tick populations (Murigu et al., 2016). Most of these deaths occur in Africa and are exacerbated due to lack of capacity to effectively manage the vectors and the diseases they carry. Kibira, M., Affognon, H., Njehia, B., Muriithi, B., and Ekesi, S. (2015). biopesticide physiology r4d icipe Wolbachia sp. Resour. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). No use, distribution or reproduction is permitted which does not comply with these terms. Entomol. doi: 10.1564/20feb00, Hatting, J. L., Moore, S. D., and Maland, A. P. (2019). Sustain. Performance of a Metarhizium anisopliae-treated semiochemical-baited trap in reducing Amblyomma variegatum populations in the field. All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. Based on icipe's large arthropod pathogen repository, diverse strains are mass-screened against key target pest in laboratory bioassays. (2017). Technol. Concurrently, research focused on innovative formulations (oil-based, granular and dry spore formulations) and development of novel application strategies such as lure-and-infect, spot-sprays and autodissemination. Control 11, 248254. icipe formalized research into entomopathogens and its application for pest management with the establishment of the Insect Pathology and Pest Management Program in 1982, which subsequently transformed in the Pathology and Microbiology Department in 1994 and finally into the Arthropod Pathology Unit (APU) in 1999. Prospects of a fungus-contamination device for the control of tsetse fly Glossina fuscipes. WHO (2020). All these biopesticides are based and marketed by Real IPM and its subsidiaries across sub-Saharan Africa and beyond. 
R4D against animal pests and disease vectors will soon yield registration of a first product based on M. anisopliae strain ICIPE 7. Based on long-standing experience in developing M. anisopliae into biopesticides, the time taken from identification of virulent strains to commercialization as biopesticide products has considerably shortened. 77, 106117. J. Insights in the global genetics and gut microbiome of black soldier fly, Hermetia illucens: implications for animal feed safety control.
Vectors 3:80. doi: 10.1186/1756-3305-3-80. ecourse uoi 169, 367372. Biopesticides: Pest Management and Regulation (Wallingford, UK: CABI). 
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The focus of icipe's APU has gradually transformed from basic to applied research leading to innovative, commercial products. (2018). There is a growing interest toward understanding the role of symbionts in modulating multitrophic interactions between plants, pests and their natural enemies, and exploring their role in biological control. However, as the insect for food and feed industry takes hold, it is to be expected that entomopathogens will become a problem of large-scale rearing facilities. J. Hered. Ovicidal effects of entomopathogenic fungal isolates on the invasive fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). For instance, presence of Wolbachia sp. 81, 2029. Targets included major invasive and indigenous pests of staples, legumes, vegetables and fruit crops, as well as livestock pests such as ticks and tsetse flies. So far, a total of 8,175,957 mango growers benefited, including 49,739 growers who directly benefited through hands-on training and received IPM starter packs, 627,200 growers who benefited through parasitoid releases and 6,499,018 growers who indirectly benefited through interaction with trained growers, extension officers, NGOs and communities service providers. doi: 10.1007/s10340-012-0473-7. doi: 10.1017/S0007485300034325, Makhulu, E. E., Villinger, J., Adunga, V. O., Jeneby, M. M., Kimathi, E. M., Mararo, E., et al. Current research at icipe on avocado focuses on selection of M. anisopliae strains against tephritid fruit flies and T. leucotreca that are not pathogenic to the Western honey bee Apis mellifera and the stingless bee Meliponula ferruginea. Food Syst., 30 September 2020, View all