Journal of
Entomology and Nematology

  • Abbreviation: J. Entomol. Nematol.
  • Language: English
  • ISSN: 2006-9855
  • DOI: 10.5897/JEN
  • Start Year: 2009
  • Published Articles: 139

Full Length Research Paper

Characterization of the Soil Nematode Fauna of Makerere Hill, Kampala, Uganda

Nzeako S. O.
  • Nzeako S. O.
  • Department of Animal and Environmental Biology, Faculty of Science, University of Port Harcourt, Port Harcourt, Rivers State, Nigeria
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Talwana H.
  • Talwana H.
  • Department of Agriculture Engineering, University of Cape Coast, College of Agriculture and Natural Science, School Agriculture, Cape Coast, Ghana.
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Teye E.
  • Teye E.
  • School of Agricultural Sciences, College of Agricultural and Environmental Sciences, Makerere University, Makerere, Kampala, Uganda.
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Sekanjako I.
  • Sekanjako I.
  • Department of Agriculture Engineering, University of Cape Coast, College of Agriculture and Natural Science, School Agriculture, Cape Coast, Ghana.
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Nabweteme J.
  • Nabweteme J.
  • Department of Agriculture Engineering, University of Cape Coast, College of Agriculture and Natural Science, School Agriculture, Cape Coast, Ghana.
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Businge M. A.
  • Businge M. A.
  • School of Agricultural Sciences, College of Agricultural and Environmental Sciences, Makerere University, Makerere, Kampala, Uganda.
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  •  Received: 17 June 2019
  •  Accepted: 13 August 2019
  •  Published: 31 October 2019

 ABSTRACT

Soil nematode faunal analysis is necessary to ascertain the health status of the soil ecosystem. Composite soil samples were taken at designated sites; A, B, C and D from the Makerere Hill area, Kampala and analyzed to characterize the nematode fauna status. Soil samples were collected vertically at 0-5 cm, 5-10 cm and 10-15 cm core depths with a 5 cm wide soil auger. A total of  7,900 nematodes were collected from the study out of which 1,720 (21.8%) nematodes came from 0-5 cm core depth, 5,270 (66.7) from 5-10 cm core depth and 910 (11.52) from the 10-15 cm core depth. Species diversity showed nine orders of nematodes comprising twenty four families and forty nine species. The Order; Tylenchida had eight families and twenty five species. The Dorylaimida had six families and eleven species, The Rhabditida had families and seven species. The orders; Enoplida, Desmoscolida, Monhysteriida, Chromadorida, Araeolaimida and Tetracephalida had only one family and species each. Nematode species richness and abundance were more in the sites located at the lower fringes of the hill, induced by inherent environmental characteristics that promoted organic enrichment of the soil. The top soil (0-5 cm core depth) comprised the bacterivores c-p 1 (Rhabditis spp.) and c-p 2 nematodes (Desmoscolecidae Spp.), the 5-10 cm core depth had a composite population of all the trophic guilds but dominated by specialist obligates (plant parasitic) while the wide host range obligates (Meloidogyne spp., Pratylenchus spp. and Tylenchus spp.) occurred at 10-15 cm core depth. There was a large assortment of specialist parasites; Aphelenchus spp., Aphelenchoides spp., Aphastimatylenchus nigeriennsis and Trichodorus spp., occasioned by vegetation characteristics of the study area. The study area is a compendium of divergent habitats with peculiar ecomorphological characteristics that can serve as a reference in future environmental impact evaluation studies in relation to soil nematode faunal integrity in Uganda.    

 

Key words: Soil nematodes, species diversity, abundance, bacteriovores, specialist obligates, ecomorpological characteristics.


 INTRODUCTION

The nematodes are ubiquitous in both aquatic and terrestrial environments; a characteristic that makes them very significant biological agents in the assessment and evaluation   of   the    environment   (Heip   et   al.,   1985; Traunspurger, 2002; Manzanilla and Hunt 2004; Traunspunger, 2002; Nzeako et al., 2014; Hagerbaumer, et al., 2015 and Nzeako et al., 2016). In the terrestrial environment  soil  nematodes  are  great  bioindicators  of soil environmental changes, due to their responses to slight alterations to the soil physicochemical dynamics (Xiaoming et al., 2013, Cesarz et al., 2015). The assemblage and community structural dynamics of the nematode meiofauna are great tools for the evaluation of soil processes and plant conditions in terrestrial ecosystems (Wang et al., 2009; Pen Mouratou et al., 2010; Traunspurger et al., 2006; Zhang et al., 2012). The abundance or scarcity of nematodes in any natural aquatic or terrestrial environment is an index of the health status of such environment (Heip et al., 2000; Ferris and Benelman, 2003; Cesarz et al., 2015). As a significant component of the environmental indicator system, the nematode meiofauna are of great use in identifying habitats with poor ecological status and relate them to chemical pollutants or other types of stressors in the environment, including; hydro-morphological modifications and climate change (Von der Ohe et al., 2007; Von der Ohe and Goedkoop, 2013; Cesarz et al., 2015). However, the close relationship between soil characteristics and nematode abundance in various functional guilds could be exploited in developing a universal standard for evaluating the faunal integrity of an ecosystem (Fiscus and Neher, 2002; Nzeako et al., 2014; Angaye et al., 2015a).
 
Relevance of the nematode fauna in environmental impact assessment
 
It is a fact that the geographical characteristics of an area contributes to its biodiversity integrity (Seiyaboh et al., 2010; Angaye et al., 2015b). Zhang et al. (2012) recognized that forest types and elevations as crucial factors in the distribution of soil nematode communities. The influence of elevation gradient as a natural force that determines ecological and evolutionary responses of biota to environmental changes cannot be over emphasized (Korner, 2007; Zhu et al., 2010). To this end; Yeates (2007) opined that higher biodiversity and species richness in forest soils at lower elevations are associated with more suitable and resilient ecosystems. However, in most prevalent ecological settings; nematode richness is not entirely influenced by elevation (Zhang et al., 2012). Although, it has a significant influence in the assortment and variations in soil nematode community composition it is not the only limiting factor to nematode biodiversity (Popovici and Ciobanu, 2000).
 
It is expected that nematode community characteristics should be included in any standard environmental assessment and monitoring study. Sadly, this envisaged inclusion of nematodes in current numerous environmental studies is yet to  be  actualized,  especially in sub Saharan Africa. The non-inclusion of the nematode meiofauna in environmental impact assessments in Sub Saharan Africa may be due to myriads of reasons, including; 1) the idiosyncrasies of environmental investigators saddled with environmental assessment studies, which may hamper objectivity and inclusiveness; 2) the flux in the taxonomy of soil nematodes;  3) the in-extensiveness of the existing taxonomy to non-parasitic species; 4) the microscopic nature of most free living nematode species that undermines sampling, collection and assortment of reasonable quantities of specific nematodes for inclusive soil analysis; and 5) the scarcity of qualified nematologists. Currently, in sub-Saharan Africa, soil nematodes are not readily considered as parasites and pests of great economic significance, due to their sublime pattern of pathogenicity (Nzeako et al., 2011). This scenery dovetails into environmental impact assessments studies conducted in Africa, where numerous environmental impact evaluation reports have been accepted without the critical nematode meiofauna component.
 
It is pertinent for any standard environmental study to include the nematode meiofauna because of their important roles in the food web and mineral cycle of the biota. According to Ferris et al. (2001); nematode faunal analysis based on the relative weighted abundance of c-p classes; maturity index provides a quantitative measure of the nematode community structure and the probable condition of the soil food web. Colonizer-Persister (c-p) values of nematode taxa ordinated on a 1-5 scale based on r-k life-history characteristics are useful in interpreting the trophic status of the soil food web in different habitats (Bongers et al., 1990, 1997; Ferris and Bongers, 2012). Maturity index of soil nematodes illustrates the sensitivities of soil nematode fauna to ambient ecological disturbances. It is an ecological measure for the state of colonization and succession based on the composition of the nematode fauna after interferences, including; the monitoring of xenobiotic induced stresses in the soil (Bongers et al., 1997). Maturity index analysis also comprises calculation of indices of food web enrichment (EI), structure index (SI) and channel index (CI) evaluations that provide information about below ground ecological processes. EI indicates the responses of primary decomposers (bacteria and fungi) to available resources, SI indicates the prevalence of trophic linkages in the soil food web, and CI provides information on the prevalent decomposition channels in the soil food web (Briar et al., 2012). However, Bongers et al. (1999) expressed some reservations about the adoption of nematode maturity index-values as the absolute environmental status indicator, because; it only gives a rough  indication  of the extent of disturbance, and unable
 
to identify the inherent dominant stress factors. It is clear that soil nematodes are sensitive to a wide range of environmental parameters which should unequivocally consolidate their position as a bio-indicators (Urkmez et al., 2014). For instance, it has been observed that the Rhabditis species are indicators of organic enrichment in the terrestrial environment and could play a great role in the mineralisation process as well as in the distribution of certain micro-organisms in the environment.
 
The Eastern region of sub Saharan African is a strong agrarian region and witnesses a lot of upsurge of arthropod pest evasions. However, the region’s environment is also invaded by soil nematodes of various species, which are grossly under-reported due to the reasons earlier stated (Talwana et al., 2015). This study is aimed at characterising the soil nematode of the Makerere hill area in Kampala, where the Makerere University is situated in Uganda. This has become necessary since there is dearth of literature on this subject in relation to the study area.


 MATERIALS AND METHODS

Study area
 
Makerere lies at exactly 2.5 km by road north of Kampala central business district which is part of the Kewempe Division.  Makerere is located within coordinates 0° 20' 6.00"N, 32° 34' 12.00"E (Latitude: 0.3350; Longitude: 32.5700). It is bordered by Bwaise to the north, Mulago to the east, Wandegeya and Nakasero to the southeast, Old Kampala is also located to the south, Naakulabye to the southwest. Kasubi and Kawaala lie to the west of Makerere (Aakansha, 2014).
 
Description of the study area (Makerere University)
 
The study was conducted in Makerere area, located about 5 km to the North of Kampala city, the capital of Uganda. Makerere hill is one of the several hills that make up Kampala district other hills neighboring Makerere include; Kasubi hill to the West, Nakasero hill to the East, old Kampala hill to the South, Mulago hill to the North East and Kawempe to the North. Makerere hill is the home of Makerere University main campus covering 300 acres of land area. Makerere university is the oldest and biggest University in Uganda established as early as 1922 as a technical school. Today, the University has up to 9 colleges and one school with an average number of 40,000 undergraduate students and 3,000 graduate students.
 
Makerere Hill is located 00°211001N 32°341031E covering a total land area of 300 acres. Like the rest of Kampala district, Makerere Hill has a tropical rain forest climate according to the Koppen-Geiger climate classification system. The area receives a bimodal kind of rainfall with two wet seasons; the shorter rain season that is, between February and June receives substantially heavier rainfall per month with the month of April leading with an average precipitation of 169 mm. The average annual temperature is 21.3°C and about 1293 mm of precipitation falls annually.
 
 
b
d
Collection of samples
 
 
Four sampling stations designated;  A,  B,  C,  and  D  with  multiple sites were selected within the University campus, Station A: The University Hall- Eastern Kampala Hill (Long: N00°20'079''- 00°19'930''; Lat: E 032°34'317'' - E032°34'339''; Elevation: 1638±434 m; Total Ascent: 4168±11 m) in eastern part of the campus. Station B; Makerere Garage 2-Western Kampala Hill (Long: N00°19'865''- 00°20'118''; Lat: E 032°33'984'' - E032°33'887''; Elevation: 1237±401 m; Total Ascent: 4168±07 m) in the western part of the campus. Station C-Faculty of Food Science Area-Northern Kampala Hill (Long: N00°20'274''-00°20'309''; Lat: E 032°33'961''-E032°33'917''; Elevation: 1251±27 m; Total Ascent: 4175±03 m) in the northern part of the campus, and Sample Station D-Social Sciences Area (Long: N00°19'716''- 00°19'948''; Lat: E032°19'948''- E032°34'110''; Elevation: 1636±02 m; Total Ascent: 4134±19) in the southern part of the university.
 
Composite soil samples were collected randomly with the aid of a soil auger. Samples were collected from designated sites at depths of 0-5 cm, 5-10 cm and 10-15 cm respectively. These were put into properly labelled polythene bags to prevent dehydration. A total of 600 samples were collected, 60 from each location, these were taken to the laboratory for extraction of nematodes. The samples from each collection site were composited and subdivided in five sets. Nematodes in the subsets were extracted using the modified Bearmann’s extraction (Barker et al., 1969; Nzeako et al., 2014) and the sieving methods (Thorne, 1961; Barker et al., 1985; Kimenju et al., 2007) while identification was according to Goodey and  Goodey (1963) using the compound and stereoscopic microscopes. 
 
About 100 g of the composite soil sample from the designated sites were proceeded at soil laboratory at the college of agricultural and environmental sciences of Makerere, University for physical and chemical properties assessment. About 200 g of each composite soil sample was used for nematode extraction. Nematodes were extracted from each sample using the active method of nematode extraction as described by Coyne et al. (2007). After extraction, the nematode aliquots from each composite sample was kept in a well labeled universal sample bottle and kept in the refrigerators maintained at 4°C until further analysis. Later, the nematode extracts were fixed in 5% formaldehyde, labelled and stored in universal sample bottles for further examination.
 
Group c-p1 has generation times of only some days, high colonization ability, and tolerance to environmental stress. They have a high metabolic activity. Their population growth under conditions with rich food is explosive. Nematodes assigned to c-p 2 have a short generation time, they respond more slowly to environmental enrichment than c-p1 nematodes but increase in abundance under stressed conditions. They occur in all environments, and very tolerant of pollutants and other disturbances (Herris and Bongers, 2009). Group c-p3 is an intermediate class, has longer generation time than the previous class and includes some Chromadoridae (recalibration made at genus level) and relatively sensitive to disturbances. Nematodes assigned to the group c–p4 are characterized by a long generation time, permeable cuticle and recognized as highly sensitive to stress and pollutants. Extreme persisters are composed of larger omnivores and predators as Enoplidae and Leptosomatidae (c-p 5). They present with a generation time of one year, low colonization ability, low reproduction rates, have a permeable cuticle, are very sensitive to pollutants and other disturbances in the marine meiobenthos e.g. the r-strategists (Warwick, 1986).
 
Laboratory analysis
 
The composite soil samples were air-dried, sieved (2 mm) and subjected to physichochemical analysis following standard methods described by Okalebo et al. (2002). Soil pH was measured in a soil water solution ratio of 1:2.5; organic matter by potassium dichromate wet acid oxidation method; and particle size distribution (texture) using the Bouyoucos (Hydrometer) method.
 
Data analysis
 
Data was analyzed using (ANOVA) while the Shannon Wiener Diversity Index was used to analyzed nematodes community dynamics.

 


 RESULTS

Physicochemical characteristics of sampling stations
 
Assessments of the physicochemical parameters in the study were restricted to the pH, % organic matter (OM) and soil aggregates (soil grain composition) of the sampling stations. There was inconsistency in acidity (Table 1). The mean pH values oscillated between recorded values for forest soil and humid arable soil types based on the reports of McCauley et al. (2017). The organic matter (OM) composition of all the sampling stations indicated high humus contents with slight variability across the stations; however, the highest (OM) values were recorded in station A. The soil aggregate composition of the sampling stations or collection points showed bulky constitution with relatively high ratios of clay and silt to sand in all stations except in sampling station A. The derived soil aggregate ratio in the study deviates from the proportionately high ratio of sand to clay and silt characteristic of normal forest soil (Table 1).
 
 
Composition of soil nematode fauna in Makerere Hill Uganda
 
About nine orders of soil nematodes were recovered from the sampling stations comprising twenty four families and forty nine species. The order; Tylenchida had eight families and twenty five species. The Dorylaimida had six families and eleven species, The Rhabditida had four families and seven species. The orders; Enoplida, Desmoscolida, Monhysteriida, Chromadorida, Araeolaimida and Tetracephalida had only one family and one species each. Out of the  twenty  five  species  in  the order Tylenchida; five genera; Aphenlenchoides spp., Aphenlenchus spp., Liaphelenchoides Spp., Metaphelenchoides Spp. and Seniura Spp., were free living with variable trophic affiliations while the remaining were obligate herbivores (plant parasitic). Aside, Trichodorus spp., and Xiphenema spp., all the members of the orders; Dorylaimida (Cobbonchus spp., Caloosia spp., Dorylaimus spp., Trachypleurosum spp., Trichorus spp., Longidorus spp., Sectinema spp., Paralongidorus spp., and Xiphenema spp.) and Rhabditida, in the study were free living with different trophic affiliations ranging from bacteriovore to fungivore or predatory. This situation was also encountered in the order; Desmoscolida, Chromadorida, Araeolaimida, and Tetraocephalida. There was no significant difference (P>0.05) in nematode occurrence within different sampling stations and sites in the study. 
 
There was great variability in population of nematodes recovered from the various sampling sites, which was greatly associated with the plant cover type (vegetation) of the ecosystem.  A total of 990 nematodes (12.64%) was recovered from sampling station/site A; comprising 5 orders. Station A was made up of relatively undisturbed vegetation with canopy trees between 20-30 m high and undergrowth of compact grass except for the mono cropping of Musa species of plants in the area. The soil was bulky due to high retention of water and poor light penetration. Sampling station/ site B had a total of 600 (7.66%) nematodes comprising 5 orders and 23 species. The area possessed similar characteristics with site A except that is it is located at a relatively high altitude. Sampling station/ site C comprised mainly of grasses that are frequently disturbed antropologically. Here, 5080 (65.25%) nematodes were recovered, comprising 4 orders and 15 species. The nematode fauna domiciled in site C were mainly plant obligates. Site D, characterized by open grass planes with isolated clusters of undisturbed deciduous trees (between 20-30 m) had a total of 1130 (14.43%) nematodes; comprising 6 orders and 23 species (Tables 4 to 8).
 
Vertical variation in the nematodes distribution and concentration showed that 21.77% of the total population of nematodes occurred at the top soil comprising mainly the bacterivore c-p 1 (Rhabditis spp.) and c-p 2 nematodes.  The 5-10 cm core depth harbored 66.71% of the total population comprising nematodes of all guilds especially the specialist obligates (plant parasitic), while the 10-15 cm core depth had 11.52% comprising mainly the w ide host range obligates that parasitize tap root systems (Meloidogyne spp., Pratylenchus spp. and Tylenchus spp.). The 0-5 cm core depth recorded the highest abundance of nematodes in the sampling stations except in sampling station C. Nematode species diversity in the different sampling stations was highest in 0-5 cm core depth (Table 2). Cumulatively, thirty nine genera and species of nematode were recovered from the 0-5 cm core depth, 22 from the 5-10 cm core depth and 15 from the 10-15 cm core depth from the entire study (Table 2). The species diversity and richness of nematode meiofauna in Makerere Hill, Kampala was high (Table 4a and b).
 
Functional role of nematodes in the study
 
There was great variability in the functional roles of soil nematodes encountered in the study. Nematode occurrence and abundance was both site and depth related. The top soil showed relatively more nematode diversity and species richness, with little abundance. The 5-10 cm core depth recorded the highest population of nematodes in the study with Rhabditis terresteris having the greatest occurrence. Nine genera and species of soil nematodes occurred in the three core depths considered in this study; nineteen in two depth categories and twenty nine in only one depth category in no particular order (Tables 2 and 3). However, the obligate herbivores occurred more below the 10-15 cm depth while the free living species were common at the top soil (0-10 cm). The maturity index evaluation nematodes of the Makerere Hills showed variability in the sampling areas. The four sampling stations designated; Station A had MI value of 2.1 and PPI of 3; Station B; Makerere Garage 2.4 had MI of 2.4 and PPI of 5.85, Station C-Faculty of Food Science Area-Northern Kampala Hill had MI of 0.75 and PPI of 5.25, and Sampling Station D- Social Sciences Area had MI value of 0.26 and PPI value of 0.21. Nematode diversity and species richness were high as indicated in Tables 2 to 4 in the study. 
 
 
 
 


 DISCUSSION

Physicochemical characteristics of the sampling stations
 
The study areas and sampling sites in the Makerere hill ecosystem showed great variability in physichochemical properties consequently, influencing the general distribution and vertical population dynamics of the nematode fauna in the respective sampling stations. The ambient  pH   values  of  the  various   sampling   stations exhibited slight discrepancies, which concurred with result from a study in forested soil by Mulder et al. (2005) who stated very minute alterations in the ambient physicochemical characteristics of a habitat usually lead to great disparities in the endemic meiofaunal population dynamics in ecological settings. The pH values obtained from the various sampling sites influenced nematode community composition (Tables 1 to 8).
 
The association between organic content of the soil and nematodes assemblage was clear in the study as nematode specificity was disproportionately monospecific in sites that were frequently naturally enriched (e.g. bird droppings etc). However, none-anthropologic enrichment processes were observed in study stations; 1-4, which influenced the vertical nematode faunal distribution pattern; a similar trend to the observation of Nzeako et al. (2015) in turf grass fields in Port Harcourt. It was observed that Rhaditis species exhibited relatively high abundance due to the continuous none-anthropologic enrichment of the environment (leaf litter and excreta of birds). This occurrence confirmed reports by Ferris and Bongers (2006) that nematodes are clear indicators of organic enrichment thereby are reliable bioindicators of organic influx in both the aquatic and terrestrial environments. The study opines that Rhaditis terrestrix; a bacteriovore in c-p 1 with short generation life span indicated continuous enrichment of the sampling sites. The observed variability in organic matter augmentation due to natural processes in this study was directly associated with vegetation type which comprised mainly top storey ornamental plants that housed many domestic and exotic avian species (Zhang et al., 2012). It was observed that the rich array of canopy trees, averaging 20-25 m in height had great ornithological significance as they harboured great diversity of domestic and exotic birds. Organic content had the greatest influence on the top-down control of microbes by soil nematode and the vertical distribution of the nematode fauna (Figures 3 to 6) in the study (Yeates, 2007) as evidenced by the abundance of bacterivores on the top segment of the soil. The topography of the study area and sampling stations also influenced the distribution and diversity of soil nematodes fauna. Zhang et al. (2012), stated that forest types and elevations greatly influence the distribution of soil nematodes communities. Although, Popvici and Ciobanu (2000) asserted that nematode species richness is not entirely dependent on elevation; a point this study up-holds because, the variability in population dynamics of the nematode meiofuana was greatly patterned by site specific characteristics such as vegetation, moisture content, pH, temperature, and organic content, that were not strictly dependent on elevation. In this survey, soil grain composition and elevation were considered as contributory factors to nematodes population dynamics (Figure 6). Nematode species richness (Tables 6 to 8) and abundance (Figure 1) were more in the sites located within the lower fringes of the  hill  (Korner,  2007;  Zhu et
 
al., 2010).  The study partly agrees with Yeates (2007), that higher diversity and species richness occurred in forest soils at lower elevations occasioned by suitable and resilient ambient conditions. In the Makerere hill, nematode assemblage at the lower elevations was occasioned by the sedimentation, leaching and drainage pattern of the ecosystem that accumulate nutrients at water-hold pockets in the lower reaches of the hill. Consequently, there was an abundance of c-p1 nematodes (Coloosia paxi, Cryptonchus spp., Desmoscolecidae spp., Paracyatholaimus spp., Swageria spp., Tetracephalus spp. and Trophinenema arenarium) in sampling sites (A and D) located at the lower fringes of the study area (Tables 4 and 6). This scenario accentuates the claim by several researches that the c-p1 guild of nematodes are short lived, tolerant to pollutants and indicate organic matter decomposition (Ferris, 2010, Ferrris and Bongers, 2006, 2009; Ferris et al., 2004; Yeates, 2007; Popvici and Ciobanu, 2000). 
 
Composition of soil nematode fauna in Makerere Hill Uganda
 
The  study   revealed    the    great    biodiversity   of   soil nematodes in Makerere hill, Kampala, however, the variability in distribution in relation to the sampling stations indicated different ambient limiting factors on the soil nematode faunal integrity (Figures 1 and 2.). The recorded high species richness and abundance observed in all the sampling sites indicated favorable environmental conditions such as high organic content, relatively acidic pH and even composition of soil aggregate that enhanced nematode community bionomics (Xiaoming et al., 2013). The abundance of plant parasitic nematodes in all the sample sites confirmed the abundance of suitable plant hosts for the obligate nematode species. The study revealed a large assortment of specialist parasites of the foliar region of plants such as; Aphelenchus spp., Aphelenchoides spp., Aphastimatylenchus nigeriennsis and Trichodorus spp. Also, the presence of obligate herbivores like the Meloidogyne spp., and Pratylenchus spp., with wide host range showed divergent trends in the functional roles of the soil nemafauna of the rhizosphere. This scenario may have been occasioned predominantly by enhanced soil fertility and availability of variable suitable hosts (Renco and Kovack, 2012). The observed trend is in agreement with Bongers et al. (1997) who opined that high plant parasitic nematode index (PPI) andmaturity index  (MI)  in  a habitat showed divergent trends in the functional roles of soil nemafauna community composition due to multiple sources of nourishment. The variability in vegetation pattern of the sampling stations induced by anthropologic influences are contributory to the nematode faunal distribution and this predisposed some sites to the abundance of specific nematode e.g. the Aphelenchoides and the free living species (geographical specificity).
 
 
 
 
Organic enrichment of the soil can stimulate the development of great population of micro-organisms that interact with free living stages of soil nematodes of different taxa. This interaction greatly impedes the plant parasitic nematodes infectivity and improve soil nutrient status, physical properties of soil, water retention, water infiltration, permeability, aeration and plant growth (Von der Ohe et al., 2007; Von der Ohe and Goedkoop, 2013; Urkmez et al., 2014). Many studies have focused on the different types of organic  amendments  as  suppressants of plant parasitic nematodes, especially root-knot nematodes, because of their large host range and biological potential (Raquel, 2012; Angaye et al., 2015b; Imafidor, et al., 2016; Elele et al., 2017).
 
Functional role of nematodes in the study
 
The Makerere hill ecology depicts great environmental heterogeneity that provides species with diverse habitats and niches that host diverse species occasioned by adaptation, convergence, divergence selectivity and speciation in evolutionary processes (Manzanilla- Lopez and Hunt, 2004). The study showed the structural and functional roles of soil nematodes in the ecosystem (Ferris and Bongers, 2006; Haegeman et al., 2012; Raquel, 2012).  The study is a low budget evaluation of the  nematode  fauna  in  the  tropics,   yet   indicates;  an assemblage of soil nematodes within the equatorial band and particularly the African region. This assessment is in no way a generalized assessment of the nematode community composition of the equatorial Uganda as only a small but unique segment of the Ugandan topology was covered and the limited time of the survey imposes a limitation.  However, it is a schematics of what the nematode community of equatorial Uganda presents. Soil disturbances (tillage, synthetic inputs, organic enrichment, etc.) influenced  nematode  communities.  The  nematode assemblage of the Makerere Hill comprised a rich assay of fast-growing, r-strategist bacterivores that, over time, transform to a more diverse community including slower-growing higher c-p (2 and 3) value bacterivores and fungivores. Ultimately, these basal community populations are succeeded by higher c-p (4 and 5) omnivore and carnivore nematodes, once the level of disturbance is minimized or eliminated (Yeates et al., 1999; Briar et al., 2012 and Mwamba, 2016).  The great diversity and abundance of nematodes  in  the  various  sampling  sites depicts a responsive ecosystem in relation to biotic and abiotic conditions. The vertical variation in the studied sites depicted an ecosystem with complex trophic cycles majorly due to continuous organic enrichment. In the study the bactriovores and fungivores were not restricted to the top soil which indicated presence of organic matter beyond the 0-5 cm stratum. It is viewed in that such a  scenario   could   be    due    to   anthropogenic  influence that incorporates organic matter beyond the top soil. There was top-down abundance of nematodes, although, majority of the deep soil occurrences were obligates. The population of the lower c-p nematodes (c-p 1-2; colonizers) was relatively higher than those in the higher c-p (c-p 4 and 5; persisters). This suggested a trophic balance for sustainability of the food web in the ecosystem.   The    study    agrees   with   inferences    by (Bongers et al. 1991, 1995; Bongers and Bongers, 1998; Berkelmans et al., 2003) that if an assemblage is exposed to pollution, colonisers are more tolerant than persisters. If k-strategists disappear their resources will then serve as food for more tolerant species, resulting in increase of the number of colonisers under disturbed conditions.


 CONCLUSION

The Makerere hill ecosystem accommodates a sustainable nematode faunal population that exhibits dynamism in nematode population structure due to the various extraneous influences including, vegetation, enrichment pathways, elevation, topography and anthropogenic activities. The study documents some of the characteristics of the ecosystem that modify the organismal morphology, especially; the nematode fauna community composition in relation to disturbances. The nematode meiofaunal idiosyncrasies in the study; the maturity index, abundance, species richness and response to physicochemical patterns are indices of soil health status and can be included in future environmental evaluations in Uganda. In this study it has been established that the Makerere ecosystem is prone to disturbances that modify the meiofaunal structure and could be used to predict the health status of the environment in future. The most influential physic-chemical parameter encountered in the study was the organic content (OM) which influenced and sustained the functional characteristics of the nematodes community. The Makerere hill ecosystem is stable and composed of divergent habitats with peculiar ecomorphological characteristics which could be utilized as a reference in future nematode faunal analyses studies in Uganda. 


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.

 


 ACKNOWLEDGEMENTS

The authors appreciate Prof. Paul Kibuki and Mrs Dorcas Loga Okello of the Intra ACP Staff Mobility Scheme, 2016. The dean and staff of the School of Agricultural Sciences, College of Agricultural and Environmental Sciences (CAES), Makerere University, Kampala, Uganda and also thanked  Mr. Balikuddembe, Bonny the technician; Soil laboratory (CAES). Similar appreciation goes to the Department of Animal and Environmental Biology, Faculty of Science, and the Graduate school, University of Port Harcourt, Nigeria.



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