Soil insect crop pests and their integrated management in East Africa: A review

Crop Protection 106 (2018) 163–176

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Soil insect crop pests and their integrated management in East Africa: A review

T

I. Nyamwasaa,d,1, K. Lia,∗,1, A. Rutikangaa,b,1, D.N.T. Rukazambugac, S. Zhanga, J. Yina, C. Ya-zhonga, X.X. Zhanga, X. Sund a

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China University of Technology and Arts of Byumba, P.O. Box 25, Byumba, Gicumbi District, Northern Province, Rwanda c University of Rwanda, College of Agriculture, Animal Sciences and Veterinary Medicine, P.O. Box 210, Musanze District, Northern Province, Rwanda d Wuhan Institute of Virology, Chinese Academy of Sciences, Xiao Hong Shan No. 44, Wu Han 430071, China b

A R T I C L E I N F O

A B S T R A C T

Keywords: Soil insect pests Integrated pest management (IPM) Insecticides East Africa

Soil-dwelling pests are generally poorly documented in East Africa due to their cryptic nature, which complicates monitoring, so the aim of this review is to compile and elucidate the current soil insect pest and management situation in this region. Fifty-five (55) soil insect pests are reported from across East Africa, and twenty (36%) and seventeen (30%) species of Scarabaeidae and Termitidae, respectively, and three families (Agromyzidae, Apionidae and Curculionidae) were found to be the most notorious soil insect pests in the region by far. Multiple species within the aforementioned families have been reported as the leading soil insect pests threatening the production of major crops in East Africa and include the banana weevil, Cosmopolites sordidus Germar; the sweet potato weevil, Cylas formicarius Fabricius; the bean maggots Ophiomyia spencerella Greathead, O. phaseoli Tryon and O. centrosematis de Meij; the cutworm, Agrotis segetum Schiff; and several species of termites and white grubs. The major control options rely heavily on preventive measures and to lesser extent, on direct control as a last resort. This review provides insight into the soil insect pest communities in East Africa as well as current control options and identifies knowledge gaps, such as an insufficient understanding of insect biology and ecology, highlights the lack of action threshold values as well as localized recommended rates of insecticides and underlines the need for education on pesticide use.

1. Introduction Since the development of agriculture, crops have been prone to attack from various pests and diseases (Stukenbrock and McDonald, 2008; Balter, 2007; Corrêa et al., 2016), and despite human efforts to cope, constraints due to pests and disease remain a major agricultural concern (Oerke et al., 1994; Cynthia et al., 2001; Oerke and Dehne, 2004; Biber-Freudenberger et al., 2016; Kroschel et al., 2016; Goldman, 1996) that continues to plague humankind in its struggle to secure food, particularly in Sub-Saharan Africa (SSA) and southeastern and western Asia (Flood, 2010; Pimentel and Peshin, 2014; FAO, 2017). For instance, the efficacy of actual crop protection worldwide was estimated to be only 40% in 1997 (Oerke and Dehne, 1997), which differs slightly from the global actual crop protection efficacy published in 2004 for animal pest control (39%) and disease control (32%) (Oerke and Dehne, 2004). While potential global losses are estimated to be 26–29% for soybean (Glycine max (L.)), 50% for wheat (Triticum aestivum L.), 80% ∗

1

for cotton (Gossypium sp.), 31% for maize (Zea mays L.), 37% for rice (Oryza sativa L. and O. glaberrima) and 40% for potato (Solanum tuberosum L.) (Oerke, 2006), the yield losses due to insects, diseases, weeds and birds in SSA are erratic vary between 10 and 90% (Van Huis and Meerman, 1997). However, quantifying these losses is particularly problematic for some groups of pests such as soil insects (Amoako-Atta, 1983; Sekamwate and Okwakol, 2007; Toepfer et al., 2014). Unlike above-ground agricultural pests, studies on soil-dwelling pests are less common (Hunter, 2001; Hillocks et al., 1996a) despite their economic significance (Hill, 1987). Six soil insects are frequently reported as common agricultural pests impacting economic crops in countries across East Africa (Rwanda, Kenya, Tanzania, Uganda and Burundi), namely, the banana weevil, Cosmopolites sordidus Germar; the sweet potato weevil, Cylas formicarius Fabricius; the bean maggots Ophiomyia spencerella Greathead, O. phaseoli Tryon and O. centrosematis de Meij; the cutworm, Agrotis segetum Schiff); and several species of termites and white grubs (Wyniger, 1962;

Corresponding author. E-mail address: [email protected] (K. Li). These authors contributed equally to this work and are co-first authors.

https://doi.org/10.1016/j.cropro.2017.11.017 Received 1 March 2017; Received in revised form 26 November 2017; Accepted 28 November 2017 0261-2194/ © 2017 Elsevier Ltd. All rights reserved.

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Nyamasyo, 2011), and Tanzania (Abate and Van Huis, 2000; Mwanauta et al., 2015), although they are slightly less documented in Burundi (Autrique, 1989) and Rwanda (Gatarayiha and Gasogo, 2003; Nyabyenda, 2005; Nyamwasa et al., 2017). To our knowledge, other groups, including Gryllotalpidae, Chrysomelidae, Gryllidae, Pseudococcidae, and Tenebrionidae, are less common, and less is known about them. Among the most documented soil insect pests, it is not clear whether species exhibiting a considerable degree of host specialization (the banana weevil, sweet potato weevil and bean fly) have been given relatively more attention (Gold et al., 1999, 2001; Kaaya et al, 1992; Paparu et al., 2009; Abate and Van Huis, 2000; Smit and Van Huis, 1998; Rukarwa et al., 2013) due to crop prioritization (Wabbi, 2002), the degree of crop damage, or the ease with which these species are monitored. However, the potential ability of the Curculionidae, Apionidae and Agromyzidae species to complete several generations per year and thus likely to cause extensive damage can be hypothetically associated with the amount of effort dedicated to their study. For example, bean stem maggots (O. phaseoli, O. spencerella and O. centrosematis) are bean (Phaseolus vulgaris L.) pests across East Africa (Omunyin et al., 1984; Abate and Van Huis, 2000; Nyamwasa et al., 2017). Depending on the temperature, the life cycle of these species is between 20 and 30 days (Abate and Ampofo, 1996). Estimates of bean yield loss due to Ophiomyia spp. across the region range from 8–100% in Kenya, 33–100% in Tanzania, up to 100% in Uganda, and up to 50% in Burundi (Abate and Ampofo, 1996; Karel and Autrique, 1989; Mkenda et al., 2014). The same supposition is applicable to the sweet potato weevil and banana weevil. At optimal temperatures of 27–30 °C, C. formicarius completes its development from egg to adult in approximately 33 days, while C. puncticollis Boheman and C. brunneus Fabricius mature from egg to adult within 20–28 days and 32–41 days, respectively (Ames et al., 1996; Smit and Van Huis, 1998). Sweet potato yield loss due to Cylas sp. has been estimated at 73% (Smit, 1997a; 1997b). The maturation of C. sordidus from egg to adult takes 5–7 weeks (Bakyalire, 1992; Nankinga and Moore, 2010), and the associated maximum banana losses have been estimated at 100% (Gold et al., 2001). Agrotis sp. and the striped bean weevil, Alcidodes leucogrammus Erichs, are also major crop pests (see Tables 1 and 3) with short life cycles. While Agrotis sp. takes 32–67 days to reach maturity (from egg to adult), the egg incubation period of the striped bean weevil is approximately 4 days, with the larval development period lasting 17 days (Amoako-Atta, 1983; Allen et al., 1996). This estimate is consistent with reports by Mcgovran et al. (1965), Pedigo (2002) and Wellso and Wetzel (1987), who highlighted the importance of population size in predicting the extent of crop damage. Conversely, species in the Scarabaeidae family complete their life cycles in approximately one year. For instance, Schizonycha sp. is univoltine and requires approximately seven months to complete its life cycle, while Heteronychus sp. and Cochliotis melolonthoides Gerst undergo only one generation per year. The rhinoceros beetle, Oryctes monoceros Olivier, may live 3–4 months, while the total developmental period of Prionoryctes caniculus Arrow is estimated to be between 138 and 171 days in the laboratory (Medvecky et al., 2006; Hill, 2008; Matthew et al., 2013). Similarly, termites (Macrotermes spp.) have long life cycles that vary between 3 and 8 years (Hill, 2008), and crop yield losses due to termites have been estimated between 10 and 100% (Sekamwate et al., 2003; Nyeko et al., 2010; Ibrahim, 2013). Species belonging to the genera Odontotermes, Macrotermes, Pseudocanthotermes and Microtermes are the most abundant termites in East Africa, especially in Kenya, Uganda and Tanzania (Sekamwate and Okwakol, 2007; Mutitu et al., 2008; Hill, 2008; Sileshi et al., 2009). The sugarcane termite (Pseudocanthotermes militaris Hagen) is a major pest of sugarcane (Saccharum officinarum L.) in Kenya (Infonet-biovision, 2017a) but only a sporadic pest elsewhere (Hill, 2008). Details about the life history of the sugarcane termite, two

Greathead, 1971; Amoako-Atta, 1983; Smit et al., 1997; Sekamwate and Okwakol, 2007; Hill, 2008; Nyambo and Löhr, 2005; Ojwang, 2010; Okonya et al., 2014; Nyamwasa et al., 2017; Lays and Autrique, 1987). However, because soil insects are concealed in the soil, which hinders sampling efforts (Ericsson et al., 2007), it is unlikely that the below-ground crop losses from soil insects are solely associated with these species (Autrique, 1989; Kaaya et al., 1992; Trutmann and Graf, 1993; Gold et al., 2001; Gatarayiha and Gasogo, 2003; Makundi and Sariah, 2005; Kiggundu, 2007; Nyeko et al., 2010; Ochilo and Nyamasyo, 2011; Ibrahim, 2013; Mkenda et al., 2014; Kiptoo et al., 2016). (Hillocks et al., 1996a, b) and Sekamwate and Okwakol (2007) reported that although soil pests pose serious problems, research efforts focused on these pests have been marginal and limited. The economic significance of the majority of crop pests is not adequately understood (Hillocks et al., 1996a; Nyamwasa, personal communication); for instance, a recent outbreak of new species of white grubs (Anomala graueri Ohaus, Anomala sp., Hoplochelus sp., Maladera sp., Melolonthinae sp., and Trochalus sp.) in Rwanda resulted in major yield losses in vegetable crops due to a lack of well-defined local management recommendations and poor insight into the life cycles and ecology of these species (Nyamwasa et al., 2017). This problem of soil insect pests is exacerbated with regard to the use of pesticides. Insecticides must usually be applied before planting to ensure the adequate transfer of the active ingredient into the soil, which ideally should persist throughout the crop growing season (Logan et al., 1990; Vincent and Carde, 2003). Unfortunately, this scenario rarely occurs because the active ingredient is degraded or absorbed by soil particles before pests appear (Vincent and Carde, 2003; Toepfer et al., 2014). Although some studies have cast doubt on the efficacy of integrated pest management (IPM) (Abara and Singh, 1993; Van Huis and Meerman, 1997), a body of evidence (Alebeek Van and Lenteren Van, 1992; Fernandez-Cornejo, 1996; Ogrodowczyk, 1999; Bashaasha et al., 2000; Bonabana et al., 2001) has shown that IPM has the potential to reduce the likelihood of considerable yield losses due to pests while simultaneously minimizing the extent of environmental contamination (Muniappan and Heinrichs, 2016). In Africa, where farming systems are characterized by a high degree of heterogeneity (Giller et al., 2010) and thus provide shelter for the natural enemies of pests (Unger, 2014), a holistic approach to soil insect pest management involving ecofriendly options has potential as a viable approach. IPM generally seeks to optimize management by maintaining the density of a pest population below the economic injury level (EIL), at which point it is not economically justifiable to continue control because the cost of treatment exceeds the amount of damage (Pedigo et al., 1986; Peshin and Dhawan, 2009; Hill, 2008). In response to the limited research and scattered sources of knowledge on soil pests and the control thereof in East Africa, this review aims to compile and analyze information on and identify gaps in the soil insect pest research in selected East African countries (Rwanda, Kenya, Tanzania, Uganda and Burundi). 2. Occurrences of soil insect pests throughout East Africa At the core of this review, fifty-five species of soil insect pests belonging to 11 families were identified as key species that are unevenly distributed throughout Kenya, Rwanda, Tanzania, Uganda and Burundi (Table 1). Given the limited availability of references on this topic, this compilation of species presumably only covers the tip of the iceberg in terms of the soil insect pests in this region, but it bears some resemblance to the result of a previous review on soil insect pests across SSA (Hillocks et al., 1996a). Twenty (36%) and seventeen (30%) species belonging to the families Scarabaeidae and Termitidae, respectively, and three families (Agromyzidae, Apionidae and Curculionidae) are by far the most documented soil insect pests in Uganda (Kaaya et al., 1992; Söderlund, 2013; Nankinga and Moore, 2010; Paparu et al., 2009), Kenya (Smit and Van Huis, 1998; Abate and Van Huis, 2000; Ochilo and 164

165

8. Coffee mealybug

6. Stem weevil 7. Cricket

5. Sweet potato weevil

3. Striped bean weevil 4. Banana weevil

1. Cylas formicarius Fabricius 2. Cylas puncticolis Boheman 3.Cylas brunneus Fabricius 4. Peleropus batatae Marsh. 1. Gryllotalpa africana Palisot de Beauvois 1. Syagrus calcaratus Fabricius J. C. 2. Syagrus sp. 1. Brachytrupes membranaceus 1. Planococcus kenyae Le Pelley

Kenya East Africa East Africa Uganda Uganda Uganda Uganda Uganda East Africa

Chrysomelidae Chrysomelidae Gryllidae Pseudococcidae

Kenya East Africa Tanzania Rwanda Rwanda Rwanda Rwanda East Africa East Africa East Africa East Africa Kenya East Africa

Rwanda East Africa Tanzania Tanzania Tanzania Tanzania Tanzania Tanzania East Africa East Africa East Africa Uganda, Kenya

Distribution

Apionidae Apionidae Apionidae Curculionidae Gryllotalpidae

Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Agromyzidae Agromyzidae Agromyzidae Curculionidae Curculionidae

13. Schizonycha sp. 14. Idaecamenta eugenia Arrow 15. Adoretus sp. 16. Maladera sp. 17. Trochelus sp. 18. Hoplochelus sp. 19. Melolonthinae sp. 20. Prionorcytes caniculus Arrow 1. Ophiomyia spencerella Greathead 2. Ophiomyia phaseoli Tryon 3. Ophiomyia centrosematis de Meij 1. Alcidodes leucogrammus Erichs 1. Cosmopolites sordidus Germar

2. Bean fly

Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae Scarabaeidae

1. Anomala graueri Ohaus 2. Anomala sp. 3. Anomala exitialis Pér. 4. Heteronychus tenuistriatus Fairm 5. Anomala endinosa 6. Entposis impressa Kolbe 7. Adoretus versutus Harold 8. Cochliotis melolonthoides Gerst 9. Popillia sp. 10. Heteronychus consimilis Kolbe 11. Heteronychus licas Klug 12.Oryctes monoceros Olivier

1. White grubs

Family

Genus/Species

Insect Pest

Table 1 Soil insect pests recorded in the selected East African countries.

Cotton (Gossypium sp.), Cotton Cotton, tobacco (Nicotiana tabacum L.) Coffee (Coffea robusta L. Linden and Coffea arabica L.), ground nut (Arachis hypogaea L.), citrus

Polyphagous Polyphagous Sugar cane (Saccharum officinarum L.) Sugarcane Sugarcane Sugarcane Sugarcane Sugarcane Forest seedling Maize (Zea mays L.), sugarcane and yam (Dioscorea L.) Maize and wheat (Triticum aestivum L.) Coconut (Cocos nucifera L.), oil palm (Elaeis guineensis Jacq.) and other types of palm Beans (Phaseolus vulgaris L.) Sugarcane plantation Beans, cabbage (Brassica oleracea var. capitata) Cabbage, beans Beans Vegetables, sweet potato(Ipomoea batatas L.), beans Irish potato (Solanum tuberosum L.), peas (Pisum sativum L.) Yam Bean Bean Bean Bean Banana (Musa sp.), plantain (Musa paradisiaca L.) and ensete (Ensete ventricosum (Welw.) Cheesman) Sweet potato Sweet potato Sweet potato Sweet potato Rice (Oryza sativa L.)

Host Plant

Sekamwate Sekamwate Sekamwate Sekamwate

and and and and

Okwakol, Okwakol, Okwakol, Okwakol,

2007 2007 2007 2007 (continued on next page)

Medvecky et al., 2006 Mugalula et al., 2005 Hill, 2008; Nyamwasa et al., 2017 Nyamwasa et al., 2017 Nyamwasa et al., 2017 Nyamwasa et al., 2017 Nyamwasa et al., 2017 Hillocks et al., 1996a and Hill, 2008 Abate and Van Huis, 2000; Kahumbu, 2007 Abate and Van Huis, 2000; Kahumbu, 2007 Abate and Van Huis, 2000; Kahumbu, 2007 Amoako-Atta, 1983 and Allen et al., 1996 Gold et al., 2001; Gold et al., 1999; Kaaya et al., 1992; Paparu et al., 2009. Smit and Van Huis, 1998; Rukarwa et al., 2013 Smit and Van Huis, 1998 Smit and Van Huis, 1998 Sekamwate and Okwakol, 2007; CIP, 1988 Sekamwate and Okwakol, 2007

Nyamwasa et al., 2017 Schabel, 2006; Hill, 2008; Nyamwasa et al., 2017 Greathead, 1971 Greathead, 1971 Greathead, 1971 Greathead, 1971 Greathead, 1971 Hill, 2008; Evans et al., 1999 Schabel, 2006 Hill, 2008 Hill, 2008 Hill, 2008; Greathead, 1971

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Crop Protection 106 (2018) 163–176

Termitidae Termitidae Termitidae Termitidae Termitidae Termitidae Termitidae Termitidae Termitidae Termitidae

8. Odontotermes badius Haviland 9. O. culturarum Sjostedt 10. O. fuller Emerson 11. O. kibarensis Fuller 12. O. latericius Haviland 13. O. monodon Gerstacker 14. O. nolaensis Sjostedt

15. O. patruus Sjostedt

16. Microtermes kasaiensis Sjostedt

17. Macrotermes sp.

166

11. Wireworms

Noctuidae Noctuidae Tenebrionidae Tenebrionidae

Termitidae Termitidae

6. Macrotermes bellicosus Smeathman 7. Odontotermes sp.

Agrotis segetum Schiff. Agrotis ipsilon Hufnagel Gonocephalum simplex F. Pedinus sp.

Termitidae Termitidae Termitidae

3. P. spiniger Sjostedt 4. Macrotermes falciger Gerstacker 5. Macrotermes subhyalinus Rambur

1. 2. 1. 2.

Termitidae

2. P. piceus Sjostedt

10. Cutworms

Termitidae

1. Pseudacanthotermes militaris Hagen

9. Termite

Family

Genus/Species

Insect Pest

Table 1 (continued)

East Africa East Africa Kenya Rwanda

East Africa

Uganda, Kenya

Uganda

Uganda Uganda Uganda Uganda Uganda Uganda Uganda

Uganda Uganda, Kenya

Uganda, Kenya Uganda, Kenya Uganda, Kenya

Uganda

Uganda, Kenya

Distribution

Vegetable and root crops Vegetable and root crops Coffee Maize

Sugarcane, fruit and forest trees

Maize, soybean, sorghum (Sorghum bicolor (L.)) and coffee

Maize

Maize Maize Maize Maize Maize Maize Maize

Maize Maize, sugarcane, coconut, tea (Camellia sinensis (L.) Kuntze)

Maize, sugarcane Maize Maize

Maize

Maize, soybean (Glycine max (L.)), sugarcane

Host Plant Nyeko and Olubayo, 2005; Hill, 2008; Wanyonyi et al., 1984 Nyeko and Olubayo, 2005; Hill, 2008; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Hill, 2008; Wanyonyi et al., 1984 Nyeko and Olubayo, 2005; Wanyonyi et al., 1984 Nyeko and Olubayo, 2005; Hill, 2008; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Nyeko and Olubayo, 2005; Wanyonyi et al., 1984 Nyeko and Olubayo, 2005; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Hill, 2008; Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Hill, 2008; Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Sekamwate and Okwakol, 2007; Hill, 2008; Wanyonyi et al., 1984 Hill, 2008; Sekamwate and Okwakol, 2007; Wanyonyi et al., 1984 Hill, 2008 Hill, 2008 Hillocks et al., 1996a; Hill, 2008 Nyamwasa et al., 2017

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1991; Mugerwa et al., 2011). Soil type, soil moisture and rainfall have also been mentioned as key factors determining the magnitude of the damage caused by soil insect pests and their distribution. Hillocks et al. (1996a) reported that Microtermes species prefer well-drained soils, whereas Odontotermes species, Macrotermes michaelseni Sjostedt and Pseudacantermes spiniger Sjostedt prevail in high-groundwater areas. Likewise, the yam beetle, Prionoryctes caniculus Arrow, prefers marshy areas for breeding (Hill, 1983); white grub species such as Anomala sp. are usually found in soils rich in organic matter content or under trees (Wightman, 1972; Nyamwasa et al., 2017); and wireworms are known to prefer cooler climates, especially in the highlands.

species commonly known as bark-eating termites (Odontotermes sp. (Termes) and Macrotermes sp.) and Odontotermes badius (Haviland) have been thoroughly reviewed elsewhere (Hill, 2008) and thus are not discussed here. Clearly, studies of soil insect pests seem to be centered on a limited number of individual pests across different families, and numerous species (including Popillia sp., Anomala exitialis Pér., Entyposis impressa Kolbe, Gryllotalpa africana Palisot de Beauvois, Maladera sp., Adoretus versutus Harold, Peleropus batatae Marsh, Syagrus calcaratus Fabricius J.C., Pedinus sp., and Planococcus citri Risso) as well as various Odontotermes (Nyeko and Olubayo, 2005; Sekamwate and Okwakol, 2007) are mentioned in the literature with little information related to the quantification of economic damage, biology or ecology, which limits the development of management recommendations. Difficulties arising in the diagnosis of soil insect pests at immature stages (Šípek and Dirk, 2011; Doskocil et al., 2008; Smit and Van Huis, 1998) may impair correct identification by less-experienced or less-skilled farmers. This is likely because the larvae that generally damage crops, such as white grub species, exhibit a distinct morphology from that at mature stages and occupy a different ecological niche from that of their corresponding adult form (Jackson and Klein, 2006; Dindal, 1991; Ritcher, 1957). For example, farmers in Kenya were unable to match the larvae of Cylas spp. (C. puncticollis and C. brunneus) to the adult stage, therefore, the larvae and adults were considered to be different species (Smit and Van Huis, 1998). Sixteen species of soil insect pests from the Dynastinae family, 17 species from the Melolonthidae family and 17 species from the Rutelinae family compiled by Le Pelley (1959) in East Africa were not all included in Table 1 due to the lack of additional documentation supporting their existence in the region of interest. These omissions are not the result of questioning the authenticity of the source; rather, these species were omitted simply to avoid overloading the table with species for which details were too limited. From a species diversity perspective, however, this gap in knowledge indicates a potentially broad spectrum of unexplored soil insect pest species across East Africa. Smith (2003) and Miller and Rogo (2001) stressed the rich biodiversity of insects (more than 100,000 described species), especially in resource-poor African countries, of which only a limited number employ taxonomists or house insect collections (Scholtz and Mansell, 2009). Although it is difficult to understand all the factors favoring the wide occurrence of soil insects given the limited empirical records, several generalizations may potentially justify the proliferation of soildwelling insect pests throughout the study area: (1) the pests are associated with a restricted range of host crops that are primarily grown in East Africa (beans, sweet potatoes and bananas (Musa sp.)); (2) cropping systems that favor a single crop planted over a large area are likely to become havens for outbreaks (Wallner, 1987; Wyniger, 1962; Yaker et al., 1992; Nyamwasa et al., 2017; Oyafuso et al., 2002); (3) root-feeding insects (e.g., scarab beetles) are able to extract nutrients from nutrient-poor plant tissue as a result of symbiotic relationships with a range of bacteria, which tends to favor their survival (Egert et al., 2003, 2005; Cazemier et al., 1999a, 1999b, 2003; CalderonCortes et al., 2012; Douglas, 2013; Johnson and Rasmann, 2015); (4) the focus on easily observed foliage pests is greater than on soil insect pests (Hunter, 2001; Amoako-Atta, 1983); (5) soil insect pests synergistically interact with other pests (Nderitu et al., 1997); (6) some insects are physiologically able to cope with harsh environmental conditions (Barnett and Johnson, 2013); (7) there is a lack of subterranean pest-tracking methods (Nyamwasa et al., 2017); and (8) soil buffers the effects of soil temperature fluctuations (Villani and Wright, 1990) while soil pests can build nests or burrow into deeper soil layers. For instance, Wood et al. (1977) reported that some termites in Kenya with deep underground nests (Microtermes sp.) as well as those that build large mounds (Macrotermes, Pseudocanthotermes and some Odontotermes) are not easily destroyed; the species that are most affected by overgrazing or land clearing and cultivation include those with shallow subterranean nests as well as those that erect small mounds (Wood,

3. Integrated pest management of key soil insect pests in East Africa The adoption of IPM in East Africa appears to be fragmented and dependent on the economic status of farmers. An investigation into the use of IPM in six East African countries (Kenya, Tanzania, Rwanda, Burundi, Uganda and Ethiopia) showed that the adoption rate of smallholder farmers is low compared to that of export-oriented farmers (Dijkxhoorn et al., 2013). The study classified Rwanda, Burundi and Uganda as countries with minimal IPM, while Kenya, Tanzania and Ethiopia possess export-oriented farmers who are well trained and actively implement IPM principles, especially in vegetable production. Due to market incentives from the EU and its strict regulation of pesticide use, only export-oriented farmers can afford to adhere to such stringent food safety standards, including the use of IPM (DAI, 2007; Dijkxhoorn et al., 2013); for example, one-fifth of Kenya's vegetable exports to the European market were not accepted simply because they contained traces of banned chemicals (Sambu, 2013). There are three reasons underlying the slow uptake of IPM. First, IPM is not a homegrown technology in developing countries and was designed for largescale farming in developed countries, therefore, any attempt to directly transfer these technologies with little or no study to promote adaptation to local conditions (small-scale farming, sometimes with multiple crops) would fail (Muniappan and Heinrichs, 2016). Second, poor knowledge of IPM and limited resources present bottlenecks in IPM adoption by a large proportion of farmers (smallholders) in East Africa (Dijkxhoorn et al., 2013; Hillocks et al., 1996a). Third, most poor farmers in SSA do not have access to any reliable, effective pest control technologies (Grzywacz et al., 2014). Thus, improving the knowledge of smallholder farmers about IPM is imperative for its successful adoption, which could lead to increased crop production in East Africa. With this context, this part of the review seeks to provide an overview of IPM strategies specific to soil insect pests. Because the IPM packages are incomplete for most of the pests recorded here, only key soil insects (termites, cutworms, bean flies, white grubs, sweet potato weevils and banana weevils) are addressed (Tables 2–7). The recommendations were developed by considering the economic and social environment of local farmers. 3.1. Prevention The use of preventive measures has long been an aspect of traditional knowledge in Africa, and these measures likely evolved locally and have been passed down across generations (Unger, 2014; Van Huis and Meerman, 1997). Muniappan and Heinrichs (2016) reported that preventive methods have historically evolved in parallel with agriculture as there has always been a need to protect crops to maximize food production. In East Africa, understanding the effects of temperature and seasonal changes seems to be one of the prerequisites for developing preventive measures and forecasting pest outbreaks (Tables 2 and 6). For instance, Smit and Van Huis (1998) found that temperatures during the dry season cause soil cracking that exposes the fleshy roots of sweet potato, which are prone to banana weevil oviposition and infestation. 167

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Table 2 Pest management recommendations for termites. Soil Insect Pest Common Names: Termites, Imiswa (Kinyarwanda/Kirundi), Mchwa (Swahili), Enkuyege (Luganda) Scientific Names: Ancistrotermes sp., Amitermes sp., Macrotermes sp., Microtermes sp., Coptotermes sp., Odontotermes sp., Pseudocanthotermes sp. Main Host Plants: Maize, soybean, fruit and forest trees, bean, coffee, mango (Mangifera indica L.), sorghum, sugarcane, tea, maize, rice, coconut, ground nut.13,11,6

Prevention fields to destroy • Plow termite nests, expose them

• • • • •

to predators, and remove residues from field before planting.5,1 Ensure proper irrigation, fertilization, and weeding because stressed plants are more susceptible to termites.8 Harvest on time as termites tend to attack mature plants (maize, beans) left in the field. a,2,3 Practice crop rotation to reduce the build-up of termites, and intercrop maize with legumes, such as beans (repellent).a,3 Apply organic matter (cattle manure, crop residues) to divert termites from the plants and act as an alternative source of food.3,12 Coat planting materials with waste vehicle oil (Nyamwasa Pers. comm.).

Monitoring

Safe Direct Control

plants in the infested plants and • Inspect • Remove morning or late evening kill termites . Heap ash 11

for termite infestation.b

wilted plants, • Remove and check for hollowed

•

and soil-filled roots to confirm the presence of termites.7 Check plants covered by soil sheeting, which may contain termites. a, b,9

galleries for • Observe woody plants to reveal the presence of termites.2

• • • •

around the bases of tree trunks, or mix ash into seedling beds.3 Apply neem (Azadirachta indica A. Juss.) seed extracts (for field crops), and apply neem oil and neem leaves (for woody plants). 14, 3,10,4 Use extract from Lantana camara (tusepo) leaves.14 Destroy termite mounds and burn plant debris over the tunnels to kill the queen and remaining termites.3 Apply Beauveria bassiana (Balsamo-Crivelli) (e.g., Botanigard® ES)9

Direct Control of economic • Lack threshold studies prevents recommendation of pesticides.

1

Kranz et al., 1977; 2 Hill, 1983 and Hill, 2008; 3 Logan et al., 1990; 4 Schmutterer, 1990; 5 Schwab et al., 1995; 6 Abate and Ampofo, 1996; 7 Pearce, 1997; 8 Abate and Van Huis, 2000; 9 Roy and Gupta, 2000; 10 Schmutterer, 2002; 11 KENGAP Horticulture, 2011; 12 Hirpa et al., 2013; 13 Sekamwat and Okwakol, 2007; Hill, 2008; Nyeko and Olubayo, 2005; 14 Mulenga and Matimero, 2014; a CABI, 2017; b Infonet-Biovision. (http://www.infonet-biovision.org/PlantHealth/Pests/Termites).

Therefore, filling gaps on the soil surface around plants is recommended. Similarly, Logan et al. (1990) reported outbreaks of termite species in the dry period in East Africa, so farmers are advised to conduct timely crop harvesting since termites tend to damage mature crops later in a season (Logan et al., 1990; Schabel, 2006). Outbreaks may be associated with the responses of pests to temperature changes, which can increase the number of generations per year or lengthen the reproductive season of the pests (Kiritani, 2012; Kroschel et al., 2016), both of which may lead to severe crop damage. However, soil insect pest solutions drawn from insights into the environmental factors affecting soil insect pest population dynamics, particularly temperature and rainfall, are not the only components of prevention. A number of agronomic practices including cropping patterns (crop rotation and intercropping), proper plowing, earthing up, the use of clean planting materials, field sanitation, mulching, treating planting materials in hot water, planting trap crops, destroying termite mounds, removing termite queens, flooding with water and the use of hot ash are additional preventive measures that are extensively applied throughout East Africa (Kranz et al., 1977; Siddig, 1987; Tinzaara et al., 2002; Autrique, 1989; Hill, 1983; Schwab et al., 1995; Abate and Ampofo, 1996; Hillocks et al., 1996b; Abate and Van Huis, 2000; Kagezi et al., 2002; Rukazambuga et al., 2002; Tinzaara et al., 2002; Masanza, 2003; Tinzaara, 2005; Kahumbu, 2007; Hirpa et al., 2013; Murage et al., 2013). Investing in the breeding of high-yield crop varieties with resistance to abiotic (temperature extremes, drought and flooding) and biotic (phytophagous insects, plant pathogens, weeds, nematodes and vertebrates) stresses constitutes a key building block in the foundation of a durable IPM program (Nicholas et al., 2011). To date, varieties that are resistant to soil insect pests in East Africa are less documented or likely to remain in the crop breeding pipeline. Except for varieties resistant to the sweet potato weevil (Mwanauta et al., 2015; Stevenson et al., 2009; Muyinza et al., 2012; Anyanga et al., 2013) and bean fly (Abate, 1990; Mwangi et al., 2013; NEMC, 2013), cultivars that are resistant to the

remaining pest species have yet to be identified. 3.2. Monitoring Prior to the selection of IPM strategies for soil insect pests, gathering information on pest dynamics is critically important. For example, knowledge of the emergence period of adult insect pests requires monitoring insect pest population dynamics before oviposition (Majumdar, 2011; Allsopp and Logan, 1999). Such information could help prevent the population from establishing on a crop or inform the planning of control tactics targeting first instars. Likewise, knowledge of the period during which larvae are expected to feed actively is relevant to the timing of the cultivation of sensitive crops (Oyafuso et al., 2002; Arakaki et al., 2004); Porter et al. (1991) stressed this crop–pest synchrony relationship as a determining factor determining the extent of pest damage. At the East African scale, a number of studies have shown that soil insect pests are most destructive at the larval stage (Raman, 1987; Abate and Ampofo, 1996; Jackson and Klein, 2006; Sadik et al., 2010; Gold et al., 2001; Chernoh, 2014). Riekert and Van den Berg (2003) noted that maize damage due to termites begins at the seedling stage and can intensify during the onset of senescence, while the bean fly (O. phaseoli Tryon and O. spencerella Greathead) and cutworm (Agrotis sp.) are occasionally reported as causing significant damage to beans and lettuce (Lactuca sativa L.), usually during the plant seedling stage (Makundi and Sariah, 2005; Njoroge et al., 2016). Clearly, gaining insight into pest dynamics and the regular monitoring of crop growth immediately after seedling emergence are critical steps in making the right decisions and identifying appropriate tactics as part of an IPM program. For instance, based on knowledge of the growth stages of beans, farmers in some parts of Kenya and Tanzania have learned that plants sown earlier experience substantially lower rates of bean stem maggot infestations than beans planted later (Sariah and Makundi, 2007; Songa, 2010; Makundi and Sariah, 2005). In Rwanda, farmers usually practice hand picking of white grubs 168

1,2,6,10

cutworms from encircling and cutting the plants (Nyamwasa pers. comm.).

weeds, and plow deep to expose • Destroy larvae and pupae to sun and predators. delay transplantation until stems • Slightly have become wide and hardy to prevent

Prevention

•

•

•

hairless caterpillars 7–50 mm long.2,4,10 Caterpillars are also found close to cut plants near the soil surface. When disturbed, they curl up.2,4,5 Make control decisions when 1 to 2 cutworms are found per 20 to 30 plants or if damage is expected from empirical evidence.7 Control is not needed when plants are 25–30 cm tall.1

stage, dig into the • Atsoilthe(rootseedling zone) to check for dull,

Monitoring

8

®

nicotinic acetylcholine receptor

Imidacloprid EC (e.g., Admire ), a • systemic neonicotinoid acting as a

Direct Control (Caution)

•

(braconid wasps), Cotesia sp. and tachinid flies can be used. Predators (ground beetles, lacewings, praying mantises, birds) can also be effective.2 Bacillus thuringiensis (kenyae) Berliner.5

•

•

stomach action. 6,b Lambda Cyhalothrin (e.g., Karate 2.5 WG), a pyrethroid with contact and stomach action. 6,b Azadirachtin 0.003% EC (e.g., Nimbecidine).3,6

agonist. tirucalli L. sap can be used • Euphorbia the assistance of skilled technicians, the Alpha-cypermethrin EC (e.g., • With • biological agents Snellenius manila Ashmead Fastac), a pyrethroid with contact and

fields.7,2

beginning of a cutworm infestation, • Athandthepicking may be helpful in small-sized

Safe Direct Control

169 11

•

• •

1004, KK 8, GLP 585 and KK 15 (Kenya) and Exl 52, Exl 55, and MLAMA 49 (Tanzania).4,13,12,15 Earth up around already affected stems, allowing the beans to send out more roots.7 Plant early (1–2 weeks) in the season, as bean flies tend to peak late in the season (seedling stage). Apply organic manure and practice earthing up.13,10 Practice bean-maize or bean-sorghum rotation or intercrop beans with cereals.11,6,16,17

bean varieties, such as Mwezi moja, that are • Use resistant to bean fly including Chelalang, Tasha, GLP

deep (15-20 cm) to bury and expose maggots.3

Do not plant beans near soybeans or cowpeas as • they share a common pest complex. Plow slightly

Prevention

Safe Direct Control

•

•

•

and yellow maggots in split stems.5 Observe young seedlings under stress that wilt and die. Older plants are tolerant but have stunted growth.5 Monitoring should be conducted weekly with particular attention paid to the seedling stage.11 Take control measures at a 5–10% infestation level.11

•

attacks and destroy them outside of the field.1,13 Apply extract from neem leaves11,13,12

for shiny, black-bluish, tiny plant parts or residues • Look • Remove flies, yellow blotches on leaves with symptoms of bean fly

Monitoring

®

•

acting as a nicotinic acetylcholine receptor agonist.13,8,2 Acephate products and systemic organophosphates (e.g., ACE WSP, ASATAF).11,13,9,2

®

Imidacloprid EC (e.g., Confidor , • Admire ), a systemic neonicotinoid

Direct Control (Caution)

Mbutia, 1944; 2 Lays and Autrique, 1987; 3 Autrique, 1989; 4 Abate, 1990; 5 Allen et al., 1996; 6 Seif et al., 2001; 7 Kahumbu, 2007; 8 Paul and Trutmann, 1987; 9Paparu et al., 2009; 10 Buruchara et al., 2010; 11Murage et al., 2013; 12 NEMC, 2013; Mwangi et al., 2013; 14Mwangi, 2014; 15 Kiptoo et al., 2016; 16 Mugambi, 2013; 17 Trutmann et al., 1993.

13

1

Common Names: Bean flies, bean stem maggots (English), Urunyo rw'ibishyimbo/ibiharage (Kinyarwanda/Kirundi), Funza wa Inzi wa mahalage (Swahili), Empunyu yebijanjaro (Luganda) Scientific Name: Ophiomyia spp. Main Host Plants: Beans, soybean, cowpea (Vigna unguiculata (L.) Walp). 8,14

Soil Insect Pest

Table 4 Pest management recommendations for the bean fly.

1

Hill, 1983; 2 Siddig, 1987; 3 Schwab et al., 1995; 4 Buruchara et al., 2010; 5 Stevenson et al., 2009; 6 Njoroge et al., 2016; 7 Massawe et al., 2013; 8 Unger, 2014; 9 Hill, 2008; 10 Infonet-biovision, 2017b; a CABI, 2017; b Rice knowledge bank (http:// www.knowledgebank.irri.org).

Common Names: Cutworm, Inanda (Rwanda/ Burundi), Sota (Swahili) Scientific Names: Agrotis segetum, A. ipsilon Main Host Plants: Beans, potato, cabbages/kale (Brassica oleracea var. sabellica), carrot (Daucus carota L.), coffee, eggplant (Solanum melongena L.), amaranth (Amaranthus L.), peas, maize, tomato (Solanum lycopersicum L.). 9,4,6,a

Soil Insect Pest

Table 3 Pest management recommendations for cutworms.

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Crop Protection 106 (2018) 163–176

Crop Protection 106 (2018) 163–176

•

• •

• • •

• 5,10,11,12

Waiyaki, 1980; 2 Glare and Milner,1991; 3 Anne, 2011; 4 Behary et al., 2012; 5 Cock and Allard, 2013; 6 Omer et al., 2014; 7 Xun et al., 2016; 8 Agritt, unpublished data; 9 Hill, 2008; 10 Nyamwasa et al., 2017; 11 Le Pelley, 1959; 12 Medvecky et al., 2006.

•

• •

them to sun and predators (e.g., birds).3,6 Ensure proper fertilization because strong plants resist damage.3,6 Ensure drainage because white grubs prefer wet or humid soil.3 Plant trap crops such as marigolds and sunflowers.3 Practice rotation with lesssusceptible crops (e.g., cotton).3,6

toward the end of the dry season, during which white grubs move upward to feed (Nyamwasa et al., 2016 unpublished data). 3.3. Safe direct control options East Africa has not lagged behind the current shift in emphasis in IPM toward more safe and sustainable practices (Bielza et al., 2008; Grzywacz et al., 2014). Several safe direct control alternatives including biological control, crude plant-derived products, various cultural management strategies and the use of pheromones or other traps (e.g., baits or light-based traps) have been tested against various soil insect pests (Logan et al., 1990; Roy and Gupta, 2000; Schmutterer, 2002; Unger, 2014). The first biological control attempt in the study area was performed in Kenya against an aphid, Schizaphis graminum (Rondani), in 1911(Neuenschwander et al., 2003). Although this approach has been reluctantly embraced since that time (Neuenschwander et al., 2003; Cherry and Gwynn, 2007; Rutikanga, 2015), it has been used to successfully control numerous soil insect pests. Successes have been reported with Metarhizium anisopliae against O. monoceros Olivier (Greathead, 1971), termites (Nyeko and Olubayo, 2005) and C. puncticollis (Ondiaka et al., 2008). The entomopathogenic fungus Beauveria bassiana Balsamo-Crivelli is a known pathogen of the banana weevil (Cosmopolites sordidus Germar) in Uganda (Gold et al., 2001; Tumuhaise et al., 2004; Nankinga et al., 2005) and Kenya (Kaaya et al., 1992; Nankinga et al., 2002; Nankinga et al., 2005; Tinzaara et al., 2007), and the fungus Cordyceps barnesii Thwaites as well as the endophytic nonpathogenic fungus Fusarium oxysporum Schlecht have demonstrated efficacy against white grub species (Greathead, 1971; Evans et al., 1999) and banana weevils (Gold et al., 2001; Griesbach, 2000). Bacillus thuringiensis (Bt) proteins have been shown to be toxic to sweet potato weevil larvae, but transgenic sweet potato varieties expressing such toxins have not yet been developed (Ekobu et al., 2010) Entomopathogenic nematodes (EPNs) are among the most promising non-microbial natural enemies of soil-dwelling insect pests, and some have been identified (Waturu, 1998; Xun et al., 2016), tested and applied against the banana weevil, sweet potato weevil (Waiyaki, 1980; Nderitu et al., 2009; Ndiritu et al., 2016; Waturu et al., 1998) and white grubs (Agritt, unpublished data). In addition to EPNs and fungus-based control strategies, natural enemies, including Campsomeris erythrogaster Dalm., C. phalerata Sauss., C. lachesis Sauss., Scolia carnifex Sauss. and Tiphia parallela Smith, are reported to be effective against Schizonycha sp. (Greathead, 1971). Biological control agents are not the only promising solutions for soil insect pest management; there is hope that indigenous botanical insecticides can also play a role equivalent to that of synthetic pesticides (Belmain and Stevenson, 2001; Unger, 2014; Logan et al., 1990; Floice et al., 1997; Murage et al., 2013; NEMC, 2013; Mwangi et al., 2013; Belmain, 2015). Plants that express botanical insecticides constitute a rich source of biochemicals (Qin et al., 2010) with a wide spectrum of activity, are easy to process, and appear to be affordable to smallholder farmers (Philip and Robert, 1998; Mugisha-Kamatenesi et al., 2008). However, even if these alternatives are derived from plants, their safety to humans and the environment are not guaranteed (Grzywacz et al., 2014; Belmain et al., 2013). Some plant compounds, such as nicotine and rotenoids, can be toxic to humans, birds and fish (Copping and Menn, 2000; Gupta, 2007; Regnault-Roger and Philogène, 2008; Ryan, 2002), and there is great concern about the scientific validation of their effectiveness. Resource-poor smallholder farmers typically use botanicals as crude plant materials or extracts, which can lead to the use of lower concentrations of the active ingredients and reduced efficacy compared to synthetic chemical pesticides (Isman, 2008; Grzywacz et al., 2014). Interestingly, a list of African pesticidal and deterrent species has been compiled (Stoll, 2000), and resource-poor farmers would greatly benefit from the successful exploitation and promotion of these species with optimized

1

•

as a nicotinic acetylcholine receptoragonist.6,1 Alpha-cypermethrin EC (e.g., Fastac), a pyrethroid with contact and stomach action6 community workers and farmers' associations.3,6 Use entomopathogenic nematodes (EPNs) (Steinernema carpocapsae Weiser, Heterorhabditis bacteriophora Poinar) at 750,000,000 IJ/ha.7,8 Metarhizium anisopliae Metchnikoff (e.g., Met52, Salem); apply 108 to 109 conidia per mL of water to soil around plants.2,3 and have legs on the thorax. They are found in the root zones of plants from 20–40 cm under the soil.6 Infested plants wilt, turn yellow, and dry out. Uproot symptomatic plants, and note white grub damage on roots or tubers.3,1 Use light traps to capture adult beetles.1,9,4 Action thresholds vary with crops; take control action at an economic damage level of 2 ± 2.5 larvae per stool (8000 ± 10,000/acre).5

®

fields for white, C-shaped larvae with hard, by handpicking, and destroy • Monitor • Control yellow to brown heads. These larvae are soft bodied collected white grubs with support from 6

and destroy previous • Remove plants. deeply to bring white • Plow grubs to soil surface, exposing

Common Names: White grub (English), Ibishorobwa (Kinyarwanda), Ibikogoshi (Kirundi), Ebisukunu (Luganda) Scientific Name: Phyllophaga spp. Main Host Plants:Beans, sugarcane, maize, potato, eggplant.

Prevention Soil Insect Pest

Table 5 Pest management recommendations for the white grub.

Monitoring

Safe Direct Control

Direct Control (Caution)

®

Imidacloprid EC (e.g., Confidor , • Admire ), a systemic neonicotinoid acting

I. Nyamwasa et al.

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Table 6 Pest management recommendations for the sweet potato weevil. Soil Insect Pest

Prevention

Monitoring

Safe Direct Control

Direct Control (Caution)

and turning over the soil Monitor fields for adult weevils pheromone• Plowing • tunneled • Mass-trap • Combine exposes pupae to predators. tuber roots using decyl (E)-2baited traps with a and the presence of butenoate. clean and resistant planting preplanting application • Use larvae. materials such as the New Dip planting materials in a of chlorpyrifos granules • Kawogo variety (sweet potato) solution of Beauveria . Use pheromone traps • . (decyl (E)-2bassiana or Metarhizium butenoate) to capture volunteer plants and anisopliae for 30 min • Remove adult weevils. crop debris. Apply Heterorhabditis and • Steinernema sp. to control timely and deep planting, Use green-light traps • Use • larvae. and hill up to prevent or fill to capture adult cracks around plants in dry weevils. Plant Tephrosia vogelii Hook. • season due to increased f. around the field as a

Common Names: Sweet potato weevil (English), Imungu y’Ibijumba (Kinyarwanda), Imungu y’Ibijumpu (Kirundi), Amajimiji (Luganda), Fukusi wa Viazi vitamu (Swahili) Scientific Names: Cylas puncticollis, Cylas brunneus, Cylas formicarius.4 Main Host Plants:Sweet potato.6

6

4,5,14

11,10,7

1

4,5

13,9

3,2,15

6

4,5,6

3,2,12,13

8

• •

temperature.11,5 Practice rotation with lesssusceptible crops such as cereals (e.g., maize) for 2-3 seasons.3 Early harvesting helps prevent damage because sweet potatoes become more susceptible to weevils as they mature.3

repellent.1

Allard, 1993; 2 Skoglund and Smit, 1994; 3 Ames et al., 1996; 4 Smit et al., 1997; 5 Smit, 1997; 6 Smit et al., 2001; 7 Magira, 2003; 8 Stathers et al., 2003; Muyinza et al., 2010; 11 Okonya et al., 2014; 12 Nderitu et al., 2009; 13 Mwanauta et al., 2015; 14 Hue and Low, 2015; 15 Korada et al., 2010.

1

9

Stevenson et al., 2009;

10

reasons. On one hand, the lack of an action threshold value limits the recommendation of pesticides for the majority of soil pests; thus far, action thresholds have been established for only three of the six notorious soil insect pests (Tables 3–5). Van Huis and Meerman (1997) discussed at length a number of hurdles hindering the application of economic threshold concepts by resource-poor farmers; thus, their findings are not repeated here. Another major constraint on IPM feasibility is the underuse and misuse of pesticides (Ngowi et al., 2007; Grzywacz et al., 2014; Dijkxhoorn et al., 2013). Input misuse in agriculture was identified by (Hillocks et al. 1996a, b) as a critical challenge that is relatively common in SSA, and the experience of small-scale farmers in the region is that synthetic products are sometimes adulterated or sold beyond their expiration date (Stevenson et al., 2012; Dijkxhoorn et al., 2013). The limited use of chemical alternatives for prevention as well as safe direct control can be partly blamed on the relatively high cost to small-scale farmers, who mainly invest in subsistence agriculture (Okonya et al., 2014). For example, a survey conducted by Njuki et al. (2004) in armyworm-endemic areas of Tanzania reported that 70% of farmers were unable to afford pesticides during African armyworm (Spodoptera exempta Walker) outbreaks, and reports

applications serving as benign, lasting solutions for soil insect pest management. 3.4. Direct control with restrictions The implementation of crop intensification programs via monoculture and increased inputs in some African countries often intensifies pest problems (Nyamwasa et al., 2017; Kathiresan, 2012; SP-IPM, 2008; USAID NUR LUC CIP PROJECT, 2013; Sola et al., 2013; Tadele, 2017). According to a recent projection of pest distributions and a risk atlas of Africa, the expansion and abundance of crop pests will remain steady until 2050 (Kroschel et al., 2014, 2016). Thus, increased pest problems inevitably require a broad, sustainable crop protection strategy that involves direct control practices with curative effects (Nonga et al., 2011), such strategies emphasize the use of IPM-compatible pesticides as a last resort (Bale et al., 2007). For a successful IPM program, the use of insecticides typically requires a prior establishment of economic thresholds (Bale et al., 2007; Peshin and Dhawan, 2009). In East Africa, it is important to realize however, that developing a complete IPM package that includes pesticides remains problematic for various Table 7 Pest management recommendations for the banana weevil. Soil Insect Pest Common Name: Banana weevil (English), Ibivumvuri by’Insina (Kinyarwanda), (Kirundi), Ekivumvumira (Luganda), Fukusi wa Ndizi (Swahili) Scientific Name: Cosmopolites sordidus Main Host Plants: Musa sp. 2

Prevention clean planting • Use materials such as tissue

• • • • •

cultures or chop off roots/ outer layer of corms.3,9 Dip suckers into hot water (55 °C) or use a neem seed solution or chlorpyrifos before planting.8,10 Use proper fertilization, and apply organic manure (20 kg/mat).3 Maintain clean area around plants.3 Apply mulch.7 Cut pseudostems at the base after harvesting and cover the corm with soil.3

Monitoring

Safe Direct Control

corms for irregular chopped • Monitor • Place tunnels that may contain 1–1.5-cm pseudostems on soil 4,1

black weevils.

pheromone lures (Cosmolure • Use +) hung on the top of a pitfall

•

made of a 10-L bucket with liquid detergent as a trapping agent, and check traps every 3 days to capture weevils.3 Damaged banana plants dry out and can easily fall off.4,2

• •

around banana plants to trap and kill weevils.5,9 Use EPNs.11,12 Apply a maize soil-based formulation of Beauveria bassiana (2 × 1014/ha) at the base of mats.6,5,9

Direct Control of economic threshold • Lack studies prevents recommendation of pesticides.

1 Gold and Messiaen, 2000; 2 Gold et al., 2000; 3 Kagezi et al., 2002; 4 Musabyimana et al., 2001; 5 Gold et al., 2002; 6 Nankinga et al., 2002; 7Rukazambuga et al., 2002; 8 Tinzaara et al., 2002; 9 Masanza, 2003; 10 Tinzaara, 2005; 11 Xun et al., 2016 unpublished; 12 Ndiritu et al., 2016.

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by REMA (2011) and Sekamwate and Okwakol (2007) associated the underuse of synthetic pesticides with low levels of literacy among farmers and a lack of local recommendations for use. A case study conducted in the Lake Manyara Basin (Tanzania) showed that 84% of the farmers were not able to read or understand pesticide labels or instructions as this information was written in English (Nonga et al., 2011). Similar observations were reported by Mwanthi and Kimathi (1990), who found that 60% of farmers in Kenya did not understand the pesticide labeling or instruction.

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Seasonal flight activity of scarab beetles (Coleoptera: Scarabaeidae) associated with sugarcane in southern Queensland. Aust. J. Entomology 38, 219–226. Ames, T., Smit, N.E.J.M., Braun, A.R.O., Sullivan, J.N., Skoglund, L.G., 1996. Sweetpotato: Major Pests Diseases, and Nutritional Disorders. International Potato Center (CIP), Lima, Perú, pp. 152. Amoako-Atta, 1983. Observations on the pest status of the striped bean weevil Alcidodes leucogrammus on cowpea under intercropping systems in Kenya. Int. J. Trop. Insect Sci. 4, 04. Anne, K.A., 2011. White Grub (Bio Net International). http://www.infonet-biovision.org, Accessed date: July 2015. Anyanga, M.O., Muyinza, Talwana, H., Talwana, R., Hall, D., Farman, I.D., Gorrettie, N.S., Mwanga, R.O.M., Stevenson, P.C., 2013. Resistance to the weevils cylas puncticollis and cylas brunneus conferred by sweetpotato root surface compounds. J. Agric. Food Chem. 61, 34. Arakaki, N., Sadoyama, Y., Kishita, M., Nagayama, A., Oyafuso, A., et al., 2004. 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4. Conclusions and recommendations This review illuminates the status of soil insect pests throughout East Africa in detail and shows how farmers are coping with threats from these species. This review lays the groundwork for more targeted, timely, and effective control of soil insect pests and underlines the need for more research. Thus far, only a small number of species have been studied comprehensively. Knowledge gaps, particularly related to life cycles, factors predisposing host crops to specific pests, and species diversity and dynamics, are factors driving difficulties in preventing damage by a number of soil pests in East Africa, which emphasizes the need to expand research. Likewise, much effort is still needed to develop effective monitoring tools to track the movement of larval insect pests within the soil. In addition to the need for more research, efforts to expand and improve the transfer of knowledge to beneficiaries (farmers) are necessary. Farmers do not always recognize the different life stages exhibited throughout the development cycles of soil-dwelling pests, so we argue that there a knowledge gap remains with regard to linking larval stages to adult forms, not only for farmers but extension staff as well. Such education must accompany the incorporation of IPM into the national policies of East African countries to ensure the rapid and widespread use of these strategies. Given that EPN use is considered a promising tool for the biological control of root pests (Lacey et al., 2001), the slow pace of EPN adoption throughout the region needs to be increased, and more focus is needed on the selection of highly infective local nematode strains and plants that can recruit EPNs after herbivore attacks. It is also paramount to expand research on novel control tactics, such as integrating CO2-based baits and root volatile compounds into soil insect pest management to entice and kill the underground developmental stages (larvae and pupae) of these pests. Finally, inadequate use and misuse of pesticides in East Africa will require educating farmers on proper handling and the related detrimental side effects of these chemicals on the environment. Suitable localized recommendations on application rates and specific action threshold values for the use of pesticides still need to be determined and narrowed to specific pest species and crops to support correct and economically sound decisions. Acknowledgments The authors are indebted to Professor Stefan Toepfer for his profound advice, and we thank the Chinese Academy of Sciences and the Chinese Academy of Agricultural Sciences for allowing us to use their huge electronic databases. This work was supported by the Natural Science Foundation of China via grant numbers 31371997 and 31572007. References Abara, O.C., Singh, S., 1993. Ethics and biases in technology adoption: the small farm argument. Technol. Forecast. Soc. Change 43, 289–300. https://doi.org/10.1016/ 0040-1625 (93)90057-E. Abate, T., 1990. Studies on Genetic, Cultural and Insecticidal Controls against the Bean Fly, Ophiomyia Phaseoli (Tryon) (Diptera: Agromyzidae). PhD Thesis. (Ethiop). Abate, T., Ampofo, J.K.O., 1996. Insect pests of beans in Africa: their ecology and management. Annu. Rev. Entomol. 41, 45–73.

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