Soil macrofauna research in ecosystems in Uganda
Soil is a living entity, comprising an inseparable mixture of solid, liquid and gaseous phases, and diverse fauna and flora, the below ground biodiversity. The macrofauna consists of animals longer than 4 mm or wider than 2 mm, which are easily located by the naked eye and include arthropods, molluscs and earthworms. This review is aimed at developing an inventory of the present knowledge about macrofauna in ecosystems in Uganda and identifying future priorities for research, application and capacity building. It is noted that there are a few assessments of soil macrofauna, diversity and abundance made for different habitats. Similarly, studies on their importance in ecosystems, distribution patterns, management, linkage with above ground biodiversity and effects of land use on them are deficient. Further, there is little documentation of farmers’ knowledge and practices related to soil macrofauna management and conservation. It is also noted that the current gaps in the soil macrofauna data and information have been caused by lack of capacity and expertise to identify, evaluate and manage this resource. More research and training in the taxonomy, ecology, economic evaluation and management of this fauna are suggested.
Soil is a living entity, comprising an inseparable mixture of solid, liquid and gaseous phases, and diverse fauna and flora, the below ground biodiversity. It is capable of supporting biological growth, and is in equilibrium with its environment. When devoid of its integral fauna, and flora, however, this upper layer of the earth's crust ceases to be soil (Lal, 1987). The simplest functional division of soil fauna is on the basis of body size, into micro-, meso- and macrofauna (Anderson, 1981).
The macrofauna consists of animals longer than 4 mm or wider than 2 mm, which are easily located by the naked eye (Lavelle, 1988), and include arthropods, molluscs and earthworms. The latter can be further divided into three groups, which play different roles in the ecosystem: the epigenics, anecics and endogenics (Lavelle et al., 1994). The epigeics live and feed on surface litter and include saprolhagous arthropods and pigmented small earthworms, as well as predators of this group (chilopods, ants and some coleopteran). Anacics on the other hand feed on surface litter but build subterranean burrows and nests that provide shelter. They consist of some large pigmented earthworms and the majority of termite species. The endogeics live in the soil and consist mainly of termites and unpigmented earthworms.
The majority of soil fauna studies have been made in temperate habitats. In tropical Africa, little attention has been paid to the soil animal communities (Okwakol, 1991). A few ecological studies have been undertaken on macrofauna, mainly in West Africa. Much of the soil fauna of East Africa remains for the future as many questions are still unanswered. In Uganda, soil macrofaunal studies are deficient. Works by Salt (1952, 1955) represent the first attempts of serious ecological work in the country. These were followed by observations on populations of earthworms by Block & Banage (1968). Block (1970), in addition, presented some data on the diversity of arthropods in soils of habitats with different vegetation cover. Later publications include those by Pomeroy (1976a,b),Okwakol (1976, 1987, 1991) and Bakuneeta (1993), mainly on termites. The most comprehensive study of this group of below ground biodiversity in relation to land use change was carried out in Mabira Forest (Okwakol, 1992a, 1994) on the effect of change in land use on soil macrofauna communities.
Diversity and abundance of soil macrofauna in different natural habitats
There are a few assessments of soil macrofauna diversity and abundance made for different habitats in Uganda. Okwakol (1994) recorded fourteen orders of soil macrofauna and density of 863 m−2 in natural forest. These are shown in Table 1. The forest had a much less abundant fauna than similar ecosystems elsewhere, being 2–5 times less than the Peruvian Amazon (Lavelle & Pashanasi, 1989). These variations are probably attributable to differences in environmental conditions.
Table 1. The density of macrofauna (m−2 ± SE) in natural forest within the Mabira Forest Reserve
|Annelida||283.2 ± 45.4|
|Gastropoda||11.2 ± 5.1|
|Arachnida||28.8 ± 5.6|
|Symphla||56.0 ± 9.1|
|Chilopoda||46.4 ± 14.5|
|Diplopoda||163.2 ± 31.2|
|Thysanura||16.0 ± 6.5|
|Orthoptera||9.6 ± 4.7|
|Isoptera||48.4 ± 16.3|
|Hemiptera||3.2 ± 0.09|
|Coleoptera||24.0 ± 3.5|
|Diptera||6.4 ± 1.4|
|Lepidoptera||1.6 ± 0.9|
|Hymenoptera (ants)||132.0 ± 9.1|
|Others||32.0 ± 4.2|
Estimates of abundance of mounds of some species of termites have been recorded by various authors in different natural habitats in the country and are shown in Table 2. In Savannas and pastures, both of which are functionally similar, the densities of large mounds of Macrotermitinae, which support millions of individuals, range between 2.02 per hectare and 13.25 per hectare and those of the smaller mounds of Cubitermes spp. to be 167 per hectare (Table 2). Because of wide variations in the figures for abundance of mounds, it is not yet possible to make valid generalizations on the relative population density of termites in any habitat (Okwakol, 1991).
The effects of conversion from natural to agricultural systems
Soil communities are strongly influenced by environmental and edaphic factors, and any change in land use may change the soil fauna communities (Wallwork, 1976). The effects of clearing, however, and of change in land use, on soil fauna have not been widely quantified (Lal, 1987). The tropical rain forests, for instance, are known for their richness in soil fauna (Matsumoto, 1976; Lavelle, 1988). Large areas of these forests, the world over, are annually being cleared for agricultural production, among other reasons. Once they are cleared, all aspects of soil fertility decline rapidly, a phenomenon that may be partially attributable to destruction of soil fauna (Lavelle, 1984). In Uganda, very substantial areas of natural forest have been lost since the 1970s because of agricultural encroachment and commercial exploitation (Hamilton, 1984). The net loss of forest cover in the Mabira Forest Reserve during the 1973–1988 period has been estimated at 29% (Westman, Strong & Wilcok, 1989).
Studies on the effects of land use on soil fauna populations include work relating to clearing and cultivating savanna woodland in Nigeria (Wood, Johnson & Ohiagu, 1977), clearing and grazing in tropical savanna woodlands (Wood & Sands, 1978), and slash and burn in Amazonia (Barros et al., 2002). Published studies that address effects of clearing and cultivating tropical rain forests include those of Abe & Watanabe (1983) and Watanabe & Takeda (1984) in subtropical areas of Japan and Thailand respectively, and Abe & Matsumoto (1979) in Posoh Forest in Malaysia. Faunal populations often decline when natural habitats are cleared (Watanabe et al., 1983). Work in the Mabira Forest Reserve in Uganda showed that forest clearance and cultivation have deleterious effects on soil macrofauna communities (Okwakol, 1994, 2000). In a few instances, however, faunal densities and diversity increase following clearing of forest or woodland. Okwakol (1994) reported soil macrofaunal density of 1247 per square meter in cleared and uncultivated site compared with 863 m−2 in the natural forest. Most of the gain was attributed to a dramatic increase in the density of termites as well as increase in the density of predatory surface-active fauna such as spiders, ants and centipedes. This trend was partly attributed to the abundant food supply for wood and litter feeding species.
In a survey of termites in natural forest, a cleared but not cultivated site and six sites cultivated for over different periods distinct differences between systems were observed. Twenty-four species, including Odontotermes amanicus (Sjostedt) and Microtermes luteus (Harris), both not previously identified in Uganda, were recorded in natural forest (Okwakol, 2000). Forest clearance resulted in drastic reduction in the number of species to about 40% of what existed in natural forest while cultivation led to further reduction to <20%. Clearance of forests has both direct and indirect effects on termites as disturbance removes vegetation, destroys nest sites, alters the soil environment and food sources and leads to exposure to predators and parasites (Black & Okwakol, 1997).
Linkage of soil macrofauna with above ground biodiversity
Changes in the below-ground biodiversity are often thought to track those of plants, although there is evidence that the soil community may be more functionally resilient than the above ground biota. The type of vegetation has often been shown to be a major determining factor of soil fauna abundance (Collins, 1980). As land conversion occurs, the above-ground biodiversity is reduced. This impacts the associated soil macrofauna thus lowering the biological capacity of the ecosystem for self regulation. The result is reduced production of above-ground biodiversity.
Studies on linkage of macrofauna with above ground biodiversity in Uganda have been mostly carried out on earthworms. Wasawo & Visser (1959) made some observations on swamp worms, which are abundant in waterlogged habitats of Teso. Block & Banage (1968) carried out a survey of the earthworms of seven sites at Kabanyolo University Farm near Kampala and found that mean estimates of terrestrial earthworm populations ranged from 7.40 m−2 in swamp forest to 101.79 m−2 in banana plantation soil (Table 3). Zake et al. (1994) noted that banana plantations also supported estimated weight biomass of 4.55 g m−2 and that infiltration rate and macrofauna biomass formed a relatively similar trend to that of organic matter and banana yield.
Table 3. Mean estimates of earthworm populations (m−2) under different habitats at Kabanyolo Farm in Uganda
Scientists have begun to quantify the causal relationships between (i) the composition, diversity and abundance of soil organisms, (ii) sustained soil fertility and associated crop production, and (iii) environmental effects, including soil erosion, greenhouse gas emissions and soil carbon sequestration (Lavelle et al., 1997). There is therefore great need for the Ugandan scientists to focus on actions that target the joint conservation of both above- and below-ground components of biological diversity, for environmental benefits at ecosystem, landscape and global scales. In this regard, actions that link soil macrofauna and above-ground biodiversity, including faunal manipulation, should be undertaken.
Distribution patterns and the determining factors
The distribution pattern of macrofauna depends on several factors and is sometimes eco-region-specific. Okwakol (1976) reported that grass species, soil depth and clay content of the soil were among the factors that determined the distribution of Cubitermes mounds. Pomeroy (1976a)) observed that although large termite mounds were not obviously correlated with soil, climate or vegetation, they were absent in areas of lower temperature like forest and swamps. He also noted that Macrotermes subhyalinus was absent where temperature was below 9°C and M. bellicosus where it was below 12°C. In Uganda, these figures correspond to altitudes of about 1600 and 1300 m respectively. Pomeroy (1976b)) further observed that the distribution of M. bellicosus was correlated very strongly with temperature, and higher rainfall seemed to favour the emergence of new mounds. Pomeroy (1977) studied the distribution and abundance of large termite mound builders, and noted that they were wide spread (Table 4), but their distribution was not correlated with soils, climate and vegetation, M. bellicosus and M. subhyalinus occurred in the central, eastern, western and northern regions while Pseudocanthotermes species were recorded only in the central region.
Table 4. Distribution of large termites mould builders in Uganda
|Central (Mukono, Mpigi, Kampala, Masaka and Mubende)||Macrotermes bellicosus|
| ||M. subhyalinus|
| ||Pseudacanthotermes sp.|
|Eastern (Iganga, Jinja, Tororo and Soroti)||M. bellicosus|
| ||M. subhyalinus|
|Western (Mbarara, Bushenyi, Kasese, Fort Portal and Masindi)||M. bellicosus|
| ||M. subhyalinus|
|Northern (Gulu, Lira and Karamoja)||M. bellicosus|
| ||M. subhyalinus|
Block & Banage (1968) observed that a high population of earthworms in the upper soil layers throughout the year in a banana plantation, was attributed to high moisture due to mulches. This observation is in agreement with that of Okwakol (1994) who noted that density and biomass of the total soil macrofauna and the individual major groups increased in the wet season and decreased in the dry season for all the habitats studied.
Importance of soil macro fauna in the ecosystems
The different ecological categories of soil macrofauna play different roles in the ecosystem. Epigeics progressively fragment litter and participate in decomposition in situ. The main effect of anecics is to remove litter from the litter system and transport it to different environments, such as the subsoil or a termite nest, thus changing the kinetics of decomposition and the spatial distribution of its products. The endogenics are geophagus, feed on soil organic matter, and live on dead roots. They produce casts and faecal pellets, which are the component elements of macroaggregate soil structures. They build galleries, nests and chambers and eventually egest the soil at the surface as earthworm casts, termite sheetings or epigeic nests of termites or ants. These processes have an important influence on the physical organization of the soil.
Soil animal activities have profound effects on soil properties and physical and chemical soil processes (Hole, 1981). Macrofauna activities that affect soil include: humification and formation of organo-mineral complexes; soil mixing and turnover; casting, mounding and nest building; burrowing and tunneling, leading to creation of channels and interconnected pores. These influence processes such as aggregation, water movement, gaseous exchange, humification, mineralization and nutrient availability (Lavelle, 1988). Soil macro-invertebrates influence processes, which may affect both the physical and chemical fertility of soils (Lavelle & Pashanasi, 1989). They thus contribute to the maintenance and productivity of agrosystems. Okwakol (1994) observed a declining trend in fauna biomass and soil chemical properties, indicating that soil macrofauna had a direct effect on soil properties. Earthworms and termites can be considered the most important ecosystem engineers in soil, because of their far-reaching and lasting effects on other species by modulating soil physical and chemical properties (Lavelle et al., 1992). In Uganda, the majority of farmers have limited access to inputs and therefore maintenance and enhancement of soil macrofauna diversity may be relevant to them.
Termites constitute a very important group of soil fauna, and play a major role in many tropical ecosystems (Wood & Sands, 1978). They are ecologically important as they function as scavengers boring into, breaking up and digesting the vegetable material that results in enhanced soil fertility (Hickin, 1971; Wood & Pearce, 1991). Termite diversity can influence nutrient cycling, vegetation and energy fluxes at various scales from rhizosphere to watershed level, and from diurnal interval to long-term effects over 100 years (Black & Okwakol, 1997). Termite diversity and biological stability of natural ecosystems may be mutually reinforcing phenomena. Consequently, a reduction in termite diversity as a consequence of clearance and cultivation, is likely to have a negative impact on ecosystem function through changes in termite influenced processes.
Termite effects on the physical nature of soil are mostly exerted as a result of their burrowing and mounding activities. Selecting and sorting of certain particles by worker termites result in altered soil structure and particle size distribution. They also further result in soil erosion by bringing to the surface soil with reduced organic matter and removing plant matter (Harris, 1949).
In Uganda, a number of termite species have been recorded as chemically affecting the soil by concentrating nutrients. Among them are species of Macrotermes species (Pomeroy, 1983) and Cubitermes (Okwakol, 1987). In most cases, higher nutrient concentrations in mound soil than adjacent soil were noted. These nutrients, however, remain unavailable to plants until the mounds are either destroyed or eroded (Okwakol, 1992b).
Although soil macrofauna effects on the physical and chemical properties are considered important, studies that have manipulated this fauna in Uganda are limited. In a split-plot experiment, soil fauna was eliminated from some plots by application of carbofuran (Okwakol, 1992a) and chemical and physical properties were monitored. Soil without fauna had lower organic matter content, total nitrogen, exchangeable cations, water infiltration rates and gravimetric moisture content, and higher bulk density than that with soil fauna, suggesting faunal influence on the soil properties.
Indigenous knowledge (IK) of macrofauna
There is little documentation of farmers’ knowledge on soil macrofauna. So far, one report on such knowledge is by Pomeroy (1976b)). He noted that local farmers had mixed feelings about termites, but on balance they regard Pseudocanthotermes as harmless whereas M. bellicosus was a pest. They recognize two types of Pseudocanthotermes presumably corresponding to P. spiniger and P. minterts. The alates of both are caught and often eaten alive as they emerge and the queens are considered useful for medical purposes. M. bellicosus, on the other hand, is considered to be a major pest of graminaceous crops such as maize and millet, and to a lesser extent, of cassava. The damage is most serious when the plants are young. Okwakol (1995), in a household survey of the ecological role of termites in Uganda, noted that some crops, not damaged by termites, were considered to perform well on termite-modified soil. Mamanunu (2004) noted farmers’ acknowledgement that termites play a role in soil formation, improve soil fertility, contribute to soil aeration, improve soil structure, improve water percolation and play a role in decomposition.
Ashard (1981) observed that it was potentially possible to use termite soil as fertilizers. Logan, Cowie & Wood (1990) also observed that large mounds of M. subhyalinus may provide augmentation of the total bases (calcium, sodium, magnesium and potassium). Mamanunu (2004) recorded Ugandan farmers’ knowledge of the potential use of termite mound soil as fertilizer. Accordingly, they plant crops such as pumpkins, tomatoes, onions and maize adjacent to termite mounds.
Macrofauna and sustainable land management
It has been hypothesized that activities of many soil animals could be better managed to promote sustainable production in tropical agro-ecosystems. There are two possible approaches to management of soil macrofauna: direct manipulation such as introduction or exclusion of particular species, and indirect ecological control such as choice of habitat components. The indirect approach appears to hold more promise as a management focus. Earthworms and termites are considered key groups that have a major impact on soil processes and a high potential for manipulation at the community level (Lavelle et al., 1994). Implementation of this is constrained by a shortage of information on the activity, behavior and environmental tolerances of many species of this fauna and by the limited understanding of the structural and functional stability of soil fauna communities in general.
Soil from termitaria is sometimes used as fertilizers in tropical cropping systems. The potential role of mounds as soil amendments has been emphasized by Mamanunu (2004) who studied the performance of crops around termite mounds in selected districts of Uganda. He observed that maize grown within a radius of three meters had better yield than that grown ten meters away. Similarly, crops such as cassava and sorghum have been noted to do well on termite modified soil. There is, however, no literature on soil amendment using termite modified soil in Uganda. More research is therefore needed before sustainable application of this termite modified soil is realized.
Plant production has also been significantly improved by earthworm activities (Lavelle et al., 1994). Pashanasi (1994) observed significant correlation between earthworm biomass and production of maize and rice. The only study involving manipulation of earthworms is by Okwakol & Kagole (1993) who noted that earthworm biomass was highly correlated with banana yield.
The current gaps in the soil macrofauna knowledge have been caused by lack of capacity and expertise in Uganda to identify, evaluate and manage this resource. There is therefore need to study the taxonomy, ecology, economic evaluation and management of this fauna. In view of the inadequacy of data and information on this group of soil biodiversity, the following research priorities have been identified:
- 1Inventory of key functional groups of soil macrofauna across selected ranges of natural and agricultural systems. Survey and documentation of this fauna in a range of ecosystems is an essential component of the information required for assessment of this resource in the country.
- 2Collection of data on changes in soil macrofauna diversity within different natural and agricultural landscapes.
- 3Determination of the relationships between aboveground diversity and abundance and soil macrofauna diversity in agro-ecosystems at different stages of agricultural intensification.
- 4Evaluation of the impact of agricultural management practices on this resource base. This will go a long way in elucidating the assumption that there is necessarily a trade- off between soil macrofauna diversity loss and agricultural production.
- 5Identification of soil macrofaunal indicators of sustainable soil fertility, and development of technologies of manipulating soil macrofauna, to enhance agricultural production particularly of degraded lands.
- 6Documentation of IK and practices on manipulating soil macrofauna, and processes to enhance soil fertility with a view to harmonizing traditional and modern knowledge in the conservation of soil macrofauna.
- 7Reviewing existing policies and legislation relating to management of below ground biodiversity. This will enable identification of gaps and synergies and subsequent development of appropriate policies and laws that will reconcile the needs for ensuring food-sufficiency and environmental protection.
Inadequacies in knowledge and awareness among stakeholders have also been identified as hampering sustainable management and conservation of soil macrofauna. It is therefore necessary that, key participants in the agricultural and environmental sectors, including practitioners and decision makers are made aware of existing knowledge.