Review article The present knowledge on soil pests and pathogens in Uganda M. B. Sekamatte1,* and M. J. N. Okwakol2 1Namulonge Agricultural and Animal Production Research Institute, PO Box 7084, Kampala, Uganda; 2Below Ground Biodiversity Project, Makerere University, PO Box 7062, Kampala, Uganda Abstract To develop an inventory of the present knowledge about soil-borne pests (insects, fungi, nematodes and bacteria) in Uganda, we review in this paper, aspects of their diversity, abundance, distribution in agro-ecosystems control approaches as well as their role in sustainable land man- agement. Knowledge gaps about the soil pests and short falls in human resource capacity are identified as possible factors affecting the development of appropriate manage- ment packages for the soil pests. Priority research areas and capacity building needs are suggested. Key words: knowledge, pathogens, soil pests, Uganda Introduction The importance of soil dwelling pests, pathogens and nematodes has often been overlooked probably because of their cryptic nature and the fact that they are practically invisible to farmers. A further explanation is that, their symptoms are commonly confused with those owing to other factors such as damage by above ground pests. This may partly explain why literature on soil-dwelling pests in Uganda and elsewhere in sub-saharan Africa is scarce. As Hillocks et al. (1996) correctly put it, good knowledge of soil pest problems and ability to integrate the disciplines of plant pathology, entomology, nematology and weed science within a socio-economic framework, are prereq- uisites for adapting the principles of integrated pest man- agement (IPM) to the needs of subsistence farmers in Africa. The need for IPM in small holder systems is increasingly being realized in Uganda. Unfortunately, in Uganda and most likely throughout East Africa, little work has addressed soil pests and pathogens. There is for example, currently no authoritative record of losses arising out of key soil pests like termites and costs of protecting crops and buildings. It is also true that apart from the work of Emechebe (1975), there are no updated lists of diag- nosed/or recorded crop disease agents in Uganda. Little is known about the roles and abundance of insect and nematode pests and pathogens as well as the interactions between/among themselves despite efforts to modernize the country’s agriculture and initiatives to manage renewable natural resources better. While the diversity, abundance and distribution of some pests and pathogens in Uganda may be implied by geographical distribution of their host plants (Hansford, 1937, 1938, 1943; Emechebe, 1975) many issues related to diversity, succession and factors determining their spatial patterns are not yet studied. This signifies the presence of probably a huge knowledge gap, requi- ring more research before sustainable integrated man- agement approaches can be formulated for the soil pest complex. Soil pests in agricultural systems For purposes of this review, the term ‘soil pests’ is used to include the complex of soil inhabiting insects, soil borne plant pathogens and root-invading nematodes, which *Correspondence: E-mail: bgbdiversity@acadreg.mak.ac.ug � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 9 affect crop plants. Soil borne diseases are defined as those caused by pathogens which invade the root or lower stem of their host and are capable of survival in the soil, in the absence of the main host, either as saprophytes or by the production of resting spores. We will deliberately restrict ourselves to those pathogens either recorded or diagnosed in Uganda. Diversity, abundance and distribution of pests and pathogens Lists of soil- borne crop pathogens and insect/nematode pests are presented in Table 1. Where possible and for purposes of this record, the table indicates agent host plant and author. The majority of these pathogens are fungi. Most of the soil pests are not specialized and therefore have a wide host range. For example Rhizoctonia bataticola, Fusarium spp. and Verticuluim dahliae infect a range of plant genera (Table 1). Some species of Fusarium, however, exhibit a considerable degree of host specialization and are more effective pathogens, being less dependent than non- specialized pathogens, on host predisposition for successful infection. In crop systems, the bacterial wilt pathogen, for example, has a wide host range but is particularly dam- aging to members of the solanaceae. Root knot nematodes (Meloidogyne spp.) also have a very wide host range but are more damaging to the solaneous and leguminous crops, particularly tomatoes. Major pest species of termites belong to the genera Pseudocanthotermes Marotermes, Odontotermes and Microt- ermes. Damage varies from superficial to death of the plant. Most damage, however, appears restricted to exotic plants, which are often stressed when grown in tropical environ- ments. Most termite species in agricultural fields do not damage native crops. There is no reliable information either in Uganda or elsewhere in sub-saharan Africa to enable a comparison of soil pests, especially pathogens, in agricultural systems to natural systems. There are examples in Uganda of in- creased infection of some pathogens to crops grown on soil converted from a forest to agricultural land. For example, the Armillaria collar rot (Armillaria mellea) as well as the Fomes root rot (Fomes lignosus), which are usually of minor importance as diseases of rubber become very severe when the crop is planted on forest land. A comparison of ecosystems in relation to diversity and abundance of soil pests especially pathogens is practically difficult, particularly for Uganda, because of lack of reported studies in ecosystems other than the agricultural ecosystems. It is probable that the forest ecosystems have the greatest diversity and abundance of soil borne pests because of their relatively stable ecological state. Ecosys- tems such as the semi-arid vegetative, savanna mountains are regularly disturbed by factors such as over grazing and bush fires (Pomeroy & Rwakaikara, 1975) and agricultural practices (Okwakol, 1994), which may have direct impact on many soil pests. Diversity, abundance and distribution of pests and pathogens It is possible that, in addition to the soil pests indicated in Table 1, many other species have not yet been identified. The present record of pests of different categories clearly shows the species richness in the agro-ecosystems. This helps to emphasize the need for an integrated approach, while designing pest management programmes. There is a body of information on the biology and dis- tribution of soil pests in Africa as well as the taxonomy of some genera. For Uganda, this is especially so for termites and pathogens (some fungi and bacteria) but many other soil borne pests are poorly understood (Hillocks et al., 1996). The most important factor influencing the spatial distribution patterns of soil pests is probably the distribu- tion of host crops. Detailed distribution maps for soil insect pests can be found in IAPSC (1995). Temporal patterns (succession) Some soil pests are widespread in Africa while others have a more limited distribution and, within areas where they occur, the severity of damage they cause may vary con- siderably (Hillocks et al., 1996). In many places, their distribution is affected by a number of factors, especially soil type, soil moisture, temperature and vegetation cover. Soil moisture Soil moisture, and therefore indirectly rainfall, is an important determinant of the distribution of soil pests both geographically and within the soil profile. There are, for example, generic or species related preferences for different levels of moisture between different termites. In Kenya, for example, micro termites predominate in well drained soils but in areas of high ground water levels, Odontotermes spp. and Psendacanthotermes spiniger are among the most 10 M. B. Sekamatte and M. J. N. Okwakol � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 Table 1 Soil-borne crop pathogens, insect and nematode pests recorded in Uganda Agent Host plant Reference Fungus Marasonius spp Bananas M. sacchari Sugar cane Hanford 1940 Rhizoctonia bataticola Sweet potato, cotton, citrus Ground nuts, roses, sorghum Pythium spp. Tobacco P. debaryanum Hesse Tobacco Verticullium dahliae Cassava, cotton, egg plant, okra Simsim Piricularia oryzae Rice Fusarium graminiaerum Maize, sorghum Fusarium spp. G.nuts, sugar cane, cotton Hansford & Hays 1940 Fusarium oxysporum Bananas Rhizoctonia bataticola Bananas, simsim, beans, okra, Capsicum spp. Sclerotinia ricini Castor Sclerotium rolfsii Soybeans, Ground nuts, lucerne, capsicum, solanum potato Sclerotium capirorum Onions Pellicularia rolfsii (sacc). West Beans Alternaria solani Tomatoes Alternaria spp. Simsim Rhizoctonia bataticola Simsim, coffee, field peas Fusarium oxysporium Simsim, g.nuts, okra, pigion pea, tomato Macrophomia phaseoli Beans, lucerne Fusarium moniliforme Maize, soyabeans Hansford 1940 Fasarium solani Cotton, onions, cow pea, Solanum potato Verticillium dahliae Passion fruit, cotton, cocoa, tomato Cercospora spp. Cotton Rhizoctonia solani Cotton, coffee, tomato Polyporus coffeae Coffee Armillaria mellea Coffee, cocoa, forest trees, roses, rubber Rhizoctonia lamellifera Rubber and tea Emechebe, 1975 Daetuliphora tarii Beans, cowpeas Phytophora spp. Citrus, sweet potato Fomes noxius (Corner) Coffee Capnodium brasiliense Coffee Rhizopus nigricans G.nuts Sphacelotheca reliana (Kuhn) Maize Gibberella fujikuroi Finger millet, maize Gibberella zeae (Petch) Maize Tolyposporium penicillariae Bulrush millet Tolyposporium enhrenbergis (Kuhn) Bulrush millet Peronospora destructor (Berk) Onions Nectria haematococca (Berk) Passion fruit Actinomyces scabies (Thax) Solanum potato Helicobasidium bagisporum (Wakef) Roses Fomes lignosus (Klotzsch) Rubber Sphacelotheca sorghi Sorghum Soil pests and pathogens in Uganda 11 � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 Table 1 Continued Agent Host plant Reference Sphacelotheca cruenta (Kuhn) Sorghum Colletotrichum glycerine Soyabeans (Lehman & Wolf) Thielayiopsis paradoxa (De seynes) Sugar cane Van Hohnel, 1937 Phytophora parasitica Var. nicotianae Tobacco Tucker, 1927 Septonia lycopersici (Speg) Tomato Bacteria Pseudomonas solanacearum Tomato, G.nuts, tobacco Smith, 1956 Pseudomonas solanacearum Solanum potato Smith, 1930, 1964 P. marginalis (Brown) Stapp Solanum potato Agrobacterium tumefaciens Roses Smith &Toms, 1942 Corynebacterium michiganense Tomato, wheat Smith & Jensen, 1974 Mealy bugs Pseudococcus latipes Coffee (symbiotically with Planococcus kenyae Polyporus coffee fungus Nematodes Radopholus similis Banana Haig, 1970 Pratylenchus goodeyi Bananas Helicotylenchus multicinctus Bananas Heterodera mariani Tobacco Melodogyne spp. Egg plant, passion fruit, pigion peas Simsim Helicotylenchus spp. Simsim Meladogyne favanice Tobacco Insects Cosmopolits sordiclus Bananas, indigeous Hargreaves, 1960 Cylas formicarius Sweet potatoes, indigeous C. puncticolis Sweet potatoes Peleropus batatae (curculionidae) Sweet potatoes Marshall Gryllotalpus africana Rice Hargreaves, 1940 Syagrus calcaratus (Fab.) Cotton Taylor, 1940 Brachytrypes membranaceaus Cotton, tobacco Gwynn, 1940 Syagrus Cotton Psuedococcus citri (Coccidae) Coffee Hargreaves G.nuts Hansford & Hages, 1940 Alemu, 1996 Pseudacanthotermes militaris (Hagen) Maize, Soy P. piceus (Sjostedt) Maize Psendacanthotermes spiniger (Sjostedt) Maize Pseudacanthotermes bellicosus (Smeathman) Maize M. falciger (Gerstacker) Maize M. subhyalinus (Rambur) Maize Odontoterms badius (Haviland) Maize O. culturarum (Sjostedt) Maize O. fulleri (Emerson) Maize O. kibarensis (Haviland) Maize O. latericius (Haviland) Maize O. monodon (Gerstacker) Maize O. nolaensis (Sjostedt) Maize O. patruus (Sjostedt) Maize Microterms kasaiensis (Sjostedt) Maize, soy, sorghum Sekamatte, 1998 12 M. B. Sekamatte and M. J. N. Okwakol � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 common (Kooyman & Onck, 1987). Soil moisture and rainfall levels also affect other insects. Dry conditions for example, are reported to favour Gonocephalum simplex (Milambo, 1983). In case of pathogens and nematodes, adequate soil moisture and high temperatures allow for many genera- tions of microorganisms to be produced relatively quickly and the disease potential is therefore greater than in lower temperature environments. Thus the distribution of many soil borne pathogens is strongly influenced by the pre- dominating moisture status of the soil. Temperature patterns The distribution of soil pests can also be affected by general temperature patterns which are influenced by altitude (Villan & Wright, 1990). For instance, in Kenya, P. spiniger is not found above 1700 m while Microtermes is absent above 1900 m (Kooyman & Onck, 1987). Crops grown in arid regions suffer fewer diseases than those in humid areas. Many pathogens are, however, adapted to causing disease under hot, dry conditions (Hillocks et al., 1996). For example, the fungus Macro- phomina phasiolina causes root and stem rots in a very wide range of hosts under arid conditions. Crops grown in wet, warm environments are susceptible to seedling disease and crown rot caused by Sclerotium rolfsii where conditions are cool and wet, root disease and damping off caused by Pythium and Phytophora may be found. Plant parasitic nematodes are found almost everywhere crops are grown. Survival and invasion by plant parasitic nematodes, however, are favoured by moist soils. Nematodes are not adapted to very wet conditions and, allowing for some variation between genera, greater populations are to be found in well drained sandy loam soils than in clay soils which are poorly drained. Cultivation regimes The density of soil pest populations and intensity of pest attack on crops is often related to prior cultivation practices. For instance, wire worms and white grabs are often present in greater numbers in land, which has been left fallow or which has been sown to pasture or cereal crop (Belcher, 1989). Clearing of woodland removes food and nesting sites, while mechanical cultivation destroys mounds and termite nests in the upper soil layers altering termite numbers and species composition. Several studies have reported a decline in certain termite species with the introduction of agricul- ture as nest sites are destroyed and preferred food sources removed (Wood, Johnson & Ohiagu, 1977; Okwakol, 1994). Continuous cultivation, which is normally practiced out of necessity owing to land shortages in many parts of Uganda and elsewhere in Africa, leads to a build up of soil borne pathogens and nematodes especially, where traditional mixed cropping systems have been abandoned in favour of monoculture (Hillocks et al., 1996). In Uganda, this has been documented as especially serious with bacterial wilt of tomatoes (Pseudomonas solanaceurum) and also with the root-knot nematode (Meladogyne spp.) attacking egg-plants. The build-up in inoculum of soil-borne fungal pathogens can further be exacerbated by planting infected seed. As a traditional practice, subsistence farmers in Uganda retain their own seed for planting over seasons. This continues the cycle of infection for commonly seed borne pathogens such as Fusarium spp. In general, nematodes and soil borne pathogens tend to build up under cultivation, especially if land is continually planted one or a few crops (Hillocks et al., 1996). Some diseases can occur on land in the first year of cultivation after bush clearing, indicating the presence of the causal organisms of the indigenous flora. For instance, vascular wilt caused by the Verticilium dahliae (Evans, 1968), root rot caused by the fungi, Armilleria mellea, can be a problem on cassava when it is planted immediately after forest clearance but quickly declines in successive crops. Inter or mixed cropping Another land use practice that possibly affects the tem- poral patterns of soil pests is inter-cropping or mixed cropping. The practice has been shown to reduce above ground insect pest numbers and damage in a wide variety of situations but very few studies have focussed on inter- cropping with respect to soil pests. Examples in inter- cropping sweet potato with maize or soybean or maize, in Guinea reduced weevil damage to tubers but also decreased the overall yield and value of the crop (Yaker, Hill & Chiasson, 1992). In Uganda, inter-cropping maize with soybeans reduces maize attack by Pseudacanthotermes but not Macrotermes. The maize/sorghum inter-crop, on the other hand, reduces damage to maize by both genera (M. B. Sekamatte and A. Russel-Smith, unpublished data). Gold & Wightman (1991) found no effect of inter-cropping groundnuts with sunhemp on termite abundance or damage to groundnuts in India. Soil pests and pathogens in Uganda 13 � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 Soil fertility While soil of low fertility is not necessarily more attractive to soil borne pathogens, crops which are stressed due to nutrient deficiency are often prone to disease (Hillocks et al., 1996). Many soil borne fungi are capable of only invading only slowly growing plants or plants already under stress (e.g. seedling infection by Rhizoctonia solani), or they may invade a vigorous plant but the infection remains latent until the plant becomes stressed, as with M. phaseolina. Survival of soil pests is directly linked to soil fertility. Pomeroy & Rwakaikara (1975) noted positive correlations between soil organic matter and populations of termites. In related studies, Okwakol (1989), found a positive relationship between termite survival rates and soil organic matter content. Crop residue management The methods of crop residue disposal may have an impact on the prevalence of both insect pests and pathogens in the soil. Continuous removal of crop residues from a field leads to rapid decline in fertility and deterioration of soil struc- ture. Low levels of organic matter in the soil lead to a de- cline in populations of both macrofauna (Okwakol, 1989; Okwakol 1991) and microorganisms, which compete with pathogenic fungi and nematodes and possibly also ad- versely affect the activity of Mycorrhiza fungi (Hillocks et al., 1996). The resulting loss in vigour renders crop and plants susceptible to soil borne fungi and nematodes. The loss of soil structure results in poor holding capacity and increased soil temperatures, both of which predispose crops to charcoal rot caused by Macrophomina phaseolina (Odvody & Dunkle, 1979). Maintaining maize stovers in the fields has shown variable responses to levels of termite infestation of maize. While in some cases the stover may increase termite populations in the field, a recent work in Uganda indicates that certain quantities of mulch may significantly reduce termite attack on growing maize (Sekamatte, Ogenga-Latigo & Russell-Smith, 1998a,b). It is possible that the mulch, apart from serving as alternative food source especially to subterranean termite species, may also provide an ideal nesting site for predatory (especially Myrmicinae and Componotine) ants (Sekamatte et al., 1998a,b). Burying stover together with fish bone – based bait significantly reduced Pseudacanthotermes attack on maize (Sekamatte et al., 1998a,b). Burying crop residues by making ridges in furrows of the previous season’s crop, may tend to increase disease. This might occur if ridging is carried out late, or under dry conditions, un-decomposed crop residues can increase the incidence of seedling disease caused by R. solani, Sdepotium rolfii and M. phaseolina (Hillocks et al., 1996). Water management Water lodging retards plant growth and predisposes the crop to infection by soil fungi, which are favoured by wet conditions. Pythium and Phytophora for instance, are favoured by cooler temperatures. Infections by S. rolfii are greatest under warm, humid conditions but the fungus is sensitive to oxygen depletion and does not thrive in water logged soil. In Uganda, Pseudomonas solanacearum attack- ing groundnuts and Solanum potatoes, is associated with water logged soils (Emechebe, 1975). Importance of soil borne pests and patho- gens in the ecosystem At the landscape level, soil pests, notably termites, constitute an important component of soil because of their role as de- composers. Termites are known to be responsible for the decomposition of up to one-third of annual grass, wood and leaf litter in their habitats (Collins, 1979). They contribute to the homogenization and regeneration of the entire soil body (Hesse, 1955; Nye, 1955; Watson, 1962). Experiments conducted to determine soil fertility of termite mounds in Africa, however, have sometimes given rise to divergent views as to the importance of termites in soil fertility. Mod- uakor, Okere & Onyeanuforo (1995) for example, estab- lished that nutrient levels were greater in Cubitermes mounds than in surrounding soils but less in Macrotermes mounds, with Ca : Mg ratio being lower for both. On the contrary, the K : Mg ratios were generally lower in crops grown on the termite modified soils of both species, than in the surrounding soils. Termites, especially the alates, are an important food source in many parts of Uganda. Except for their known pest status, the importance of many pathogens and other soil dwelling life forms remains largely unknown. Indigenous knowledge about soil pests and pathogens An on-going study recently evaluated farmers’ perceptions of termite damage and available control practices in maize. It was found that in most parts of Uganda, farmers have good 14 M. B. Sekamatte and M. J. N. Okwakol � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 knowledge of termite species that are pests to crops and those that damage buildings. Of the interviewed farmers (70– 100%) across five districts ably named the various termite categories in local languages (Achola, Sekamatte & Russell- Smith, 1999). In some cases, however, the farmers indicated that it was the subterranean termite species, which were pests of crops. This was probably because the subterranean termite species are more easily seen in foraging parties. In general, there is almost total lack of indigenous knowledge about nematodes (Namaganda, Personal Communication) and soil pathogens (Kangire, Personal Communication) affecting crops, among farmers in Uganda. Country capacity for pests and pathogen studies Analysis of research projects within the National Agri- cultural Research Organization (NARO) and Makerere University Faculty of Agriculture indicates that there are relatively few studies directed at solving soil pest problems compared with above ground crop pests (Naro Projects Manual, 1998). In terms of availability of human capacity, there is a huge deficiency in both the research institutes and university system. Within NARO, for example, there are currently only five entomologists and less than ten plant pathologists dis- tributed within the various commodity programmes over four crop and one forest research institute (Naro Staff Book, 1999). Within the NARO system, there is currently one nematologist at Kawanda and one soil microbiologist based at Serere. At the Makerere University Faculty of Agriculture, there are two entomologists and two plant pathologists. None of them is currently involved in soil pest pathogen management research. Analysis of on-going research shows that it is probably the banana and to some extent horticul- ture research programmes focusing on nematodes and the cereals programme focusing on termites in maize. This leaves a lot to be desired in terms of national capacity for research in soil pests and pathogens. A major constraint in soil pest research in Uganda is probably the absence of taxonomic services, and as such, apart from small collections of banana nematodes at Kawanda, collections of some common termites at the Makerere University Zoology Department and recently at Namulonge Agricultural Research Institute (NAARI), no reference collections exist for identification services. There is also no impetus for young scientists and stu- dents at university to specialize in biosystematics. This, in addition to prohibitive costs of taxonomic services outside the country, makes research in this area less attractive. Pests and pathogens and sustainable land management A review of the past studies on the impact of crop diseases and pests on Uganda agriculture (e.g. Emechebe, 1974, Emechebe & Mukiibi, 1974; cited by Emechebe, 1975; Robinson, 1940; Kangire, 1998; Rukazambuga, 1996) indicates that few reliable estimates of crop losses due to soil borne pests exist in Uganda. For example, of 13 crop loss studies listed by Emechebe (1975), none dealt with soil borne pathogens. The only figures available are those of Rukazambuga (1996) indicating up to 50% yield loss in bananas due to weevils at 4th ratoon and Kangire (1998) reporting, 100% yield loss in bananas due to Fusarium wilt. In all studies undertaken to address soil pest problems in Uganda, the approach has been to tackle individual pests, diseases and weed problems. All organisms form part of an interactive complex and should be studied as such, if sus- tainable management strategies are to be developed. Else- where, Hillocks et al. (1996), associations between nematodes and soil borne diseases, is well documented particularly with respect to Fusarium wilt and root knot nematodes, on a wide range of crops. Where the fungal pathogen and nematode occur together, the incidence of Fusarium wilt is higher than in the absence of the nema- todes (Hillocks & Bridge, 1992). Less is known about the effect of nematodes such as Melodogyne javanica, on infec- tion by nonspecialized pathogens. Damage caused by soil-inhabiting insects such as ter- mites also enhances infection by soil borne fungi. Charcoal rot of maize, caused by M. phaseolina often occurs too late in crop development, to cause yield loss but the consequent lodging allows termites to destroy the crop as it lies on the ground. Termites have been shown to carry, on their bodies, spores of various pathogens such as Fusarium spp. (Johnson & Gumel, 1981). Similarly, Upadhyay & Rai (1982) showed that termite carrying spores of Fusarium spp could infect pigeon peas with Fusarium wilt. No such studies have been carried out in Uganda, but their results could yield essential information for the management of pests and diseases in agro-ecosystems. Damage to roots by plant pathogens may predispose the plant to attack by soil pests. Mercer (1978) considered that Soil pests and pathogens in Uganda 15 � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 groundnuts, in Malawi, were more susceptible to termite attack if they were infected by fungi such as Fusarium solani. Research on termites in annual crop systems in Uganda, is still in its infancy and based on design of on-going projects. Few aspects are likely to be addressed. Given the increasing importance of these pests, the above mentioned interactions among soil inhabiting pests and the need for integrated packages, a lot of gaps are already evident. The practice of inter/mixed cropping is still dominating small- holder agriculture in Uganda. While some studies have been undertaken to evaluate the practice of inter-cropping in respect to aphid infestation (Sekamatte, 1994), the interactions between various above ground organisms within these crop complexes remain anecdotal. Management of soil pests and pathogens There are several restrictions on small holder farmers in Uganda to adopt modern crop protection. These include, for example, shortage of land, labour and cash (Hillocks et al., 1996). These restrictions on small holder capabilities mean that technical solutions to pest problems cannot be produced solely on the research station premises. Farmers’ own needs and capabilities must be considered. A major knowledge gap in the case of Uganda is that no clear understanding of traditional pest control techniques exists. This is clearly shown by the absence of mention of any such techniques in all available literature (Emechebe, 1975) and all crop production brochures prepared by research and extension staff. This has probably been as a result of the low involvement of social/rural economists in technology development in the past. Traditional soil pest/pathogen management practices include the use of agents such as wood ash against soil pests termites and banana weevils. Various plant extracts (e.g., neem) are also used against termites in many parts of Uganda. The extracts are used against a range of symp- toms due to various pathogens. Detailed surveys need to establish a complete list of plants traditionally used as pesticides. Through long-term selection/maintenance of their own seed, farmers have always selected varieties resistant to major pests and diseases. This has probably accounted for the low adoption rates of new high yielding varieties from research stations e.g. the new millet and sorghum varieties at Serere (Anon, 1999). Other tradi- tional methods include directing storm water into Mac- rotermes mounds, application of tobacco in/on soil, pouring fish soup, or putting dead snakes into mounds as well as rotation of crops where land size permits (Achola et al., 1999). It is, however, not documented how much farmers in Uganda know about particular crop symptoms of pest/ disease infestation/infection and some of the agronomic practices, which influence crop responses. Elsewhere, for example, in Malawi, farmers were able to distinguish precisely which maize plants in a field were affected by pre-emergent striga and which parts of the plant (Hillocks et al., 1996). They were well aware of the link between low fertility and striga damage to maize. Such information needs to be documented for Uganda before extensive control methods are evaluated. Hillocks et al. (1996) discussed in detail the modern approaches to soil pests and pathogen management in sub-saharan Africa. These include host plant resistance or crop tolerance, modification of cultural control, multiple cropping, biological control, chemical control (including fungicides, nematicides and insecticides) and use of pheromones to control soil-dwelling insects. They elabor- ated the role of IPM in small holder agriculture noting that the challenge is to provide recommendations for control of a range of pests, pathogens and weeds within one system. Apart from nondeliberate use of multiple cropping e.g. maize/legumes (maize/cow peas) which decrease soil pop- ulations of root-knot nematodes, it is probably chemical control using a range of fungicides for seed dressing and long persistent termiticides (e.g. lindane, Marshal suscon) that has dominated soil pest control in Uganda’s agricul- ture (Alemu, 1996). It is not known what impact the banning of organochlorines has had on soil-borne pest/ pathogens and what factors are contributing to the regu- lation of the pest complex in the absence of these chemi- cals. This applies to other ecosystems e.g. rangelands and forest systems where organochlorines were applied against ticks, tsetse and other pests. Policy relationships Recent advances in termite research have singled out biological control as a possible solution to these soil pests (Grace, 1997). While this may equally be true for a range of other soil pests, there are still several policy issues to be addressed before full scale research in biological control can be undertaken. For instance, there are no regulatory guidelines for importation, testing or application of biolo- gical control agents in Uganda (Mugoya, Uganda National Council of Science and Technology – Personal Communi- 16 M. B. Sekamatte and M. J. N. Okwakol � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 cation). The many existing policy gaps directly hinder progress on this type of research. A policy framework needs to be worked out to harmonize issues involving stakeholders notably, the Uganda National Council for Science and Technology, the National Environment Man- agement Authority, the National Agricultural Research System (NARS) and the political authority. Future priorities for research application and capacity building In the past decade, the need to embrace the philosophy of IPM in Uganda became eminent. Till now, however, most if not all, crop protection programmes continue to focus on single pests in single crops; a situation that rarely exists in the majority of farming communities in Uganda. Mixed cropping and mixed pest infestations are what exist. Future research therefore, needs to be re-oriented to focus on integrating the various component technologies within the farmers, socio-economic framework. In the light of the pest complex and the unknown interactions with a range of soil pests, the various technologies should be integrated into packages for a particular cropping situation. On the basis of comparatively low on-going research on soil pests as reflected by NARO’s current projects, it can be concluded that little focus is placed on soil pests. This is largely because of insufficient human resource within the research system. In this review, therefore, we found it appropriate before proposing future research imperatives to identify the needs for capacity building. Capacity building needs For sustainable management of soil pests and pathogens, a capacity building initiative is required to re-orient prac- tising crop protection scientist to begin addressing soil pest problems in a holistic manner, as opposed to the single problem approach. To achieve this, in the medium–long term, the training of pest management scientists (ento- mologists and pathologists) at university should include, as part of the curriculum, concepts and practices of agro- ecology probably as a stand-alone course unit. This should produce scientists who view every pest problem as an integral part of a large and dynamic system. • Existing and upcoming crop protection projects ought to offer agro-ecology training for practicing crop protection scientists within the NARS and universities. This is considered an essential step if the entire research system is to make a change that suits the requirements of the IPM philosophy. • A critical mass of young scientists be trained as specialist taxonomists of soil pests. They should then constitute staff of the pest identification centre which could be appropriately located within the NARS centers. This capacity building should coincide with the development of appropriate infrastructure notably laboratories. Future research imperatives 1 Nation-wide survey to enable a clear understanding of the abundance, species diversity, factors affecting dis- tribution, factors predisposing host crops to specific soil pests. The only available source of information showing what plant pathogens occur in Uganda is probably that of Emechebe (1975) and termite species by Wanyonyi (1984), both of which are overdue for revision. 2 Research on the indigenous knowledge and soil pest control systems. These should be given high priority because even in the absence of high technology in-puts e.g. pesticides and fertilizers, farmers managed to pro- duce crops. It is also possible that they were developed from sound understanding of the agro-ecosystem. 3 Analyses of interaction of soil pests (pathogens, nema- todes, insects and weeds) within themselves and between them and critical factors in the environment such as soil fertility, moisture, local natural enemies etc. Most reported soil pest control studies have focused on chemical control, using nematicides and long persist- ence organochlorines against termites (Alemu, 1996) but none recorded has considered assessments of treat- ment impact on the natural enemies of pests. This is, however, a critical issue in view of the increasing con- cern on soil health and environment in general. 4 Investigating the causes of dramatic increase in inci- dence of soil borne pests and diseases in recent years. What linkages? Recently, termites have been named as a factor in the desertification problem in the cattle corridor especially the Nakasongola area (Anon, 1999). Difficulties, however, have arisen in explaining the principal factors contributing to the upsurge of termites as drought, bush fires and grazing have always been common factors. Now that people in the cattle corridor have embarked on crop agriculture, serious soil pest problems are envisaged. Consequently, long-term ecological studies are required to guarantee sustaina- bility of mixed farming in this ecosystem. Soil pests and pathogens in Uganda 17 � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 5 Impact studies of the new generation pesticides, com- monly branded as ‘safe pesticides’ on soil pests and associated natural enemies within Uganda’s agro-eco- systems. In a recent survey of eastern Uganda, elders linked the raising termite problem and low abundance of predatory ant species to aerial sprays of dieldrin against tsetse flies which went on up to around the late 1970s. This needs investigation. 6 Together with socio scientists, crop protection scientists ought to formulate appropriate methods of integrating existing component technologies such as resistant cultivars, effective crop mixtures such as maize/cow pea against nematodes, as well as suitable rotations to be transferred to farmers through appropriate extension methods such as Farmer Field School Models. 7 Crop loss studies to enable a logical ranking of the various pests in importance. Crop loss studies have not been conducted or updated for almost the whole pest complex in Uganda. References Achola, G., Sekamatte, M.B. & Russell-Smith, A. (1999) Farmer Perceptions of Termite Damage and their Control in Five Districts in Uganda. Namulonge Agricultural and Animal Production Research Institute (NAARI) Report. Alemu, S.O. (1996) Assessment of Damage and Loss in Maize by Termites (Isoptera) in Namulonge Research institute (NAARI), Uganda. MSc thesis, submitted to Makerere University, Kampala, Uganda. ANON (1999) Assessment of termite status in Nakasongola Dis- trict. A back to office report submitted to the Ministry of agri- culture, May, 1999. Belcher, D.W. (1989) Influence of cropping systems on the number of wire worms (Coleoptera: Elateridae) collected in baits in Missouri corn fields. J. Akans. Entomol. Soc. 62, 590–592. Collins, N.M. (1979) A comparison of the soil macrofauna of the lowland forest types in Sarawak. Sarawak Mus. J. 17, 267–282. Emechebe, A.M. (1975) Some Aspects of Crop Diseases in Uganda. Makerere University Printery, Uganda. Emechebe, A.M. & Mukiibi, J. (1974) Fungicidal control of brown spot of passion fruit in Uganda. Acta. Hort. 23, 112–119. Evans, G. (1968) Infection of Xanthium pungens by seed borne Verticillum dahliae. Plant Disease Reporter 52, 976–978. Gold, C.S. & Wightman, J.A. (1991) Effects of intercropping ground nuts with sunhemp on termite incidence and damage in India. Insect Sci. Appl. 12, 177–182. Grace, J.K. (1997) Biological control for suppression of termites. J. Agric. Entomol. 14, 3, 281–298. Hansford, C.G. (1937) Annotated host list of Uganda parasitic fungi and plant diseases (Part IV). E. Afric. Agric. J. 3, 235–240. Hansford, C.G. (1938) Annotated host list of Uganda parasitic fungi and plant diseases (Part V). E. Afric. Agric. J. 3, 319–324. Hansford, C.G. (1943) Host list of parasitic fungi of Uganda. Part I. E. Afric.Agric. J. 8, 248–252. Hesse, P.R. (1955) Physical and chemical study of the soils of termite mounds. East Afr. J. Ecol. 43, 449–461. Hillocks, R.J. & Bridge, J. (1992) The role of nematodes in Fusa- rium wilt of Cotton in Tanzania. Afro-Asian J. Nematol. 2, 35–40. Hillocks, R.J., Logan, J.W.M., Riches, C.R., Russell-Smith, A. & Shason L.J. (1996) Soil pests in traditional farming systems in Sub-Saharan Africa: a review part 1 &2. IAPSC (1995) Distribution Maps of Major Crop Pests and Diseases in Africa. OAU Inter-African phytosanitary counsil, Yaunde, Cameroon 320 maps. Johnson, R.A. & Gumel, H. (1981) Termite damage and crop loss in Nigeria. The incidence of termite scarified groundnut pods and resulting kernel contamination in field and market samples. Tropical pest manage. 27, 343–350. Kangire, A. (1998) Fusarium (Panama disease) of exotic bananas and wilt of East African highland bananas (Musa AAA EA) in Uganda. Thesis submitted for the degree of Doctor of Philoso- phy, Department of Agriculture, Reading University, 304. Kooyman, C.K. & Onck, R.F.M. (1987) The Interactions Between Termites Activity, Agricultural Practices and Soil Characteristics in Kissi district, Kenya. Agric. University Wageningen papers 87–3. Western Kenya, East Africa. Mercer, P.C. (1978) Pests and diseases of groundnuts in Malawi II. Disorders of posd, kernels and seedlings. Oleagineux 33, 119–122. Milambo, S.S. (1983) Occurrence and pest status of the dusty surface beetle (Gonocephalum simplex). Zimbabwe Agric. J. 80, 235–238. Moduakor, H.O., Okere, A.N. & Onyeanuforo, C.C. (1995) Termite mounds in relation to the surrounding soils in the forest and derived savanna zones of S.E. Nigeria. Biol. Fertil. Soils 20, 157– 162. Naro Projects Manual (1998) Naro Projects Manual. Published by Agric Information centre, Kawanda. Naro Staff Book (1999) Naro Staff Book. Published by Agric Information centre, Kawanda, January, 1999. Nye, P.H. (1955) Some soil forming processes in the humid tropics: 4 the action of soil fauna. J. soil sci. 6, 73–83. Odvody, G.N. & Dunkle, L.D. (1979) Charcoal rot of sorghum: effect of environment on host parasite relations. Phytopathology 69, 250–254. Okwakol, J.M.N. (1989) Survival rates of humus-feeding Cubiter- mes testaceus (Wil.) (Isoptera: termitidae) in relation to organic matter content. Insect Sci. Applic. 4, 497–501. Okwakol, J.M.N. (1991) Soil fauna and wildlife conservation in east Africa. In: African Wildlife: Research and Management (Eds F.I.B. Kayanja & E. Edroma). International council of Scientific Unions. Okwakol, J.M.N. (1994) The effect of change in land use on macrofauna communities in Mabira Forest, Uganda. Afr. J. Ecol. 32, 273–282. 18 M. B. Sekamatte and M. J. N. Okwakol � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19 Pomeroy, D.E. & Rwakaikara, D. (1975) Soil arthropods in relation to grassland burning. E. Afri. For. J. 41, 114–118. Rukazambuga, N.D.T.M. (1996) The effects of banana weevil (Cosmopolites sordidus Germar) on growth and productivity of bananas (Musa AAA EA) and the influence of host vigor on attack-Unpublished Ph.D Thesis, University of Reading, UK 249. Sekamatte, M.B. (1994) Studies on the Pest Status and Control of the Cotton Aphid, Aphis gossypii Glov. In Uganda. MSc thesis, submitted to Makerere University, Kampala, Uganda. Sekamatte, M.B., Ogenga-Latigo, M.W. & Russell-Smith A (1998a) The effect of sorghum-maize intercrop on termite infestation of maize in Uganda – unpublished report of Namulonge Agricultural and Animal Production research institute, Uganada. Sekamatte, M.B., Ogenga-Latigo, M.W. & Russell-Smith A (1998b). Termite project annual report-submitted to Natural resource institute (NRI), October, 1998. Upadhyay, R.S. & Rai, B. (1982) A possible mode of dispersal of Fusarium udum Butler in soil by termites. Science and Culture 48, 206–280. Villan, M.G. & Wright, R.J. (1990) Environmental influences on soil macroathropod behavior in Agricultural systems. Annual review of Entomology 35, 249–269. Wanyonyi, K., Darlingion, J.P.E. & Bagine, R.K.N. (1984) Checklist of the species of termites (Isoptera) recorded from East Africa . J East African Natural Hist. 181, 1–11. Watson, J.P. (1962) The Soil below a termite mound. Journal of Soil Science 13, 4–51. Wood, T.G., Johnson, R.A. & Ohiagu, C.E. (1977) Populations of termites (Isoptera: termitidae) in natural and agricultural eco- systems in southern Guinea savannah near Mokwa, Nigeria. Geo-eco.- Tropical 1, 139–148. Yaker, A., Hill, S.B. & Chiasson, H. (1992) Effects of intercropping on a population of sweet potato weevil, Cylas formicarius (F) (Coleoptera: Curculionidae). Sci. New Guinea 18, 123–132. Soil pests and pathogens in Uganda 19 � 2007 The Authors. Journal compilation � 2007 African Journal of Ecology, Afr. J. Ecol., 45 (Suppl. 2), 9–19