Ethnobotanical survey of medicinal plant species used by communities around Mabira Central Forest Reserve, Uganda

The study area covered human settlement areas around Mabira CFR some of which were enclaves and others adjacent to the forest. Mabira CFR is located 20 km north of Lake Victoria shoreline immediately to the west of Victoria Nile. The forest reserve lies partly in Buikwe, Mukono and Kayunga districts and occupies an area of 306 km² with an altitudinal range of 1070 – 1340 m above sea level [25]. It is situated between latitude 0^o 22’ and 0^o 35’N and between longitude 32^o 56’and 33^o 02’E [26] (Fig. 1).

The forest reserve occupies gently undulating landscape characterised by numerous flat-topped hills (relics of the ancient African peneplain), and wide shallow valleys [27]. The topography is such that the land drains to the north, even though the reserve’s southern boundary lies only 13 km from the lakeshore. The underlying rocks are composed of micaceous schists and shales of the Buganda- Toro system with ridges of quartzite and amphibolite. The soils are generally ferralitic sandy clay loams, with black waterlogged clays in the valley bottoms. The climate is tropical with two rainfall peaks from April to May and October to November ranging between 1,250 – 1,400 mm per annum. Annual mean temperature range, minimum: 16–17 ° C, maximum: 28–29 ° C. The vegetation of Mabira CFR was classified as “medium altitude moist semi-deciduous [28].

Commercial use of the forest began when some parts were harvested in the early 1900’s and until 1988, intensive coffee/banana agricultural encroachment badly damaged parts of the forest. [27] About 21 % and 26 % of the reserve have been designated as strict nature reserve and buffer zone respectively and the forest in these areas is recovering following extensive plantings of native tree species.

The human population living in the forest enclaves was approximately 825,000 with a density of 200–230 people per Km^-2 [29]. The local people are mainly of the Bantu ethnic group of the following tribes; Baganda, Banyarwanda, Basoga, Bagisu, Bakiga, Banyankole, Bagwere and Batoro.

The reserve has tea and sugarcane plantations around. Some local people reside in settlements for labourers on the tea and sugarcane estates [30]. The extent of growing cash crops other than tea and sugar cane is limited by scarcity of land. However locals are engaged in cultivation of food crops mainly for subsistence consumption like maize, beans, bananas, ground nuts, sweet potatoes and vegetables. Livestock rearing is limited to a few households.

Ethical approval of the study was obtained from the Uganda National Council of Science and Technology (UNCST) under registration number SS 3368 after obtaining a research license from National forestry Authority (NFA).

This was a field survey targeting custodians of Traditional Medicine used in treatment of diseases. Verbal pre-informed consent was obtained from the participants before the interview. Interviews were conducted in Luganda the local language in the area using guided semi structured questionnaires and a research assistant that was conversant with the local language.

Collection of data on medicinal plants used to treat different ailments in the study area was according to a slight modification of Martin’s procedure [31]. Purposive sampling was used to identify 14 out of 27 villages that heavily depend on the forest for primary health care through a Rapid Rural Appraisal (RRA) with village leaders. Heavy dependence was defined by village council leaders’ local experience i.e. based on the number of individuals who depend wholly on herbal medicine for livelihoods. The study included villages within 1–5Km from the forest. This is because distance from the forest influence people’s use of forest products. Before entering each of the villages, permission was sought from local leaders after explaining the aim of the study who gave us the name of the first key informant while the rest of the respondents were selected by snow ball sampling technique. [32, 33] A total of 36 key informants were selected with at least two from each village and an additional eight knowledgeable herbalists recommended by the community members from Naluvule, Bukuku, Buwoola and Kalagala villages. The informants included primary collectors, vendors and traditional healers who are the custodians of indigenous knowledge on herbal medicines. Traditional healers are divided into two broad groups of herbalists who mainly use herbs while diviners also invoke ancestral spirits to guide them in their healing practice [34‐36]. They provided information on plants and parts used, ailments treated, mode of preparation and administration, habit, source and availability of medicinal plants. Field excursions were conducted along forest trails taking traditional healers as guides and voucher specimens of cited medicinal plants were collected.

Preference ranking [31] of the 10 most available medicinal plant species and diseases commonly treated by each were shortlisted by the 12 key informants according to importance attached to the species as per frequency of use and effectiveness (number of days taken to healing in treating particular diseases successfully). The values assigned for each species across were summed up for all the informants to get an overall rank value. The species were then ranked in descending order with the species that had the highest total ranked first.

Plant identification was partly carried out in the field based on field manuals for plant identification [37, 38]. Voucher specimens were collected and later identified at Makerere University Herbarium. Correctness of scientific names of species were also checked according to Tropicos:http://​www.​tropicos.​org database accessed on 12/05/2015.

Descriptive statistics using frequencies and percentages were used to summarize data using Microsoft excel 2013. The ailments treated by the medicinal plants were classified into different categories [39].

The informant consensus factor (F_ic) was calculated to indicate the homogeny of information using the formula;

N_taxa = Number of species in each use category. It estimates the relationship between the number of use reports (N_ur) minus the number of taxa used (N_taxa) and the number of use reports in each category minus one [40].

F_ic values are low if plants are chosen randomly or if informants do not exchange information about their use or disagree about the species used in treatment of an ailment category. The values are high (close to one) if the species are used by a large proportion of informants and there is a well-designed criterion in community or if information is exchanged between informants. Therefore the medicinal plants are presumed to be effective in treating a certain disease have higher F_ic values [41].

Fidelity Level [42] was calculated for each of the 10 preferred species for their popularity according to the key informants who cited them in the treatment of particular ailments. Fidelity Level (FL) = Ip/I_u x 100 %, where I_p is the number of informants who suggested the use of a species for the same major ailment, I_u is the total number of informants who mentioned the species for any use.

The communities around Mabira CFR use diverse flora in treatment of various ailments and local people possess rich traditional knowledge on medicinal plants (Table 1). Both males and females used medicinal plants but males were dominant representing 70 % of the respondents. The age of the respondents ranged between 25–80 years. Generally 46 % of the respondents were below 50 years.

A total of 190 plant species distributed in 61families and 152 genera were identified as used. Fabaceae contributed 27 species, followed by Asteraceae (17), Euphorbiaceae (13), Solanaceae (10) and Lamiaceae (9). Genera Solanum and Indigofera contributed five species each while Ficus, Vernonia, and Acacia contributed four species each.

Vernonia amygdalina was highly ranked and regarded most important in treatment of malaria in the study area. Table 2 shows ranking of the ten most important plant species according to key informants in decreasing order together with values assigned by each informant. The key ailments treated by the preferred medicinal plants were mentioned by the key informants during the interviews.

Different plant parts of medicinal plants are used to make herbal preparations (Table 3). A high number of herbal medicine are made using leaves (77 %) and roots 40 %. Other parts of the plants are not commonly used. Regarding the 10 preferred medicinal plant species, the bark was predominantly used in seven species, followed by leaves (5) and least roots (3) (Table 3 ), although more than one part was used in some cases. For instance leaves, bark and root of Spathodea campanulata and leaves, roots and fruits of Tamarindus indica and Phytolaca dodecandra are used to prepare remedies. Herbs made up the highest proportion of medicinal plants species (41 %), followed by trees (28 %), shrubs (22 %), climbers and grasses (4 %).

Of the recorded medicinal plants, 56 % are from the forest, 14 % are cultivated 12 % grow in grasslands/woodlands and farmlands (18 %). The low incidence of medicinal plant gardens was attributed to the need to maintain secrecy of traditional knowledge and the argument that cultivated medicinal plants are less potent compared to plants collected from the wild and therefore the latter are preferred. Medicinal plant species from the forest were mostly members of Fabaaceae (40 %) and Euphorbiaceae (54 %) while species from family Asteraceae were dominant in grasslands (25 %) and fallow (44 %). Most of the medicinal plants grown in home gardens are introduced species and have not been domesticated. These include: Callistemon citrinus, Capsicum frutescens, Moringa oleifera, plus fruit tree species that are also medicinal such as Mangifera indica, Persea americana, Carica papaya and Psidium guajava. Fifty percent of medicinal plant users who harvest for commercial purposes collect plants form the forest.

The medicinal plants for treatment of different ailments were prepared and administered using various methods. Decoction was commonly used (29 %), followed by crushing and mixing with water (24 %), use of fresh crushed material (14 %) and burning (9 %) (Fig. 2). In the current study, additives used in herbal medicine preparation included silver fish, ash, salt, alcohol, tea and onions. Salt was used in remedies against toothache and oral wounds where it is believed to kill germs. For external application vaseline, paraffin and ghee were used to reduce friction during application of the remedy.

Different routes were used in administration of herbal preparations. Oral route contributed 61 % of the total species, followed by herbal bath (28 %), rubbing leaves on affected parts (14 %) and inhalation of smoke (5 %). The least used route of herbal administration was steam bath (2 %).

The 58 health conditions recorded were grouped into 25 categories of which gynecological conditions, digestive disorders and skin infections featured prominently (Table 4). The number of species used to treat different ailments are summarized in Table 4.

Species treated a wide range of ailments varying from one to six per plant. Species that treated the highest number of ailments were Balanites aegyptiaca, Carica papaya, Dracaena steudneri that were used in management of six health conditions each. On the other hand Allium sativum, Cissampelos macronata, Kalanchoe crenata, Lantana trifolia, Solanum anguvi, Tagetes minuta and Vernonia lasiopus were each used in management of five health conditions. Taxonomic analysis revealed that members of family Fabaceae were used to treat the highest percentage (28 %) of ailments. This was followed by Solanaceae (24 %), Asteraceae and Euphorbiaceae (19 %) each, Amaranthaceae, Balanitaceae and Rutaceae 14 % each, Anarcadiaceae, Moraceae, Poaceae, Bignoniaceae 12 % each while families Alliaceae, Caricaceae, Dracaenaceae, Lamiaceae, Minespermaceae, Rosaceae, Rubiaceae, Verbenaceae and Zingiberaceae 10 % each and the rest treated less than 10 %.

This technique is designed to highlight species that have healing potential for specific major purposes. The relative importance of each plant species in treatment of different ailments as categorized in Table 5 was analysed using the Factor Informant Consensus (F_ic) [41]. F_ic values range from 0–1 where values close to one (1) indicate a high rate of informant consensus on a plant species used against an illness category. F_ic values close to zero (0) mean low degree of agreement among the informants about the use of a plant species for treatment of a particular ailment. F_ic for different ailment categories was calculated to test for homogeneity or consistency of informants’ knowledge about a particular remedy for an ailment category. F_ic indicated which plants are widely used and thus merit further pharmacological and phytochemical studies. The highest F_ic (0.9) was scored for blood system disorders. The important plants used for anaemia were Amaranthus dubius and Hibiscus acetosella while those for high blood pressure included Oxalis corniculata, Canarium schweinfurthi, Sesbania sesban, Vangueria apiculata, Citrus limon and, Solanum anguivi. Seven ailment categories had F_ic of zero (0) since each respondent reported a different species used for the same ailment (Table 5).

For each of the 10 most preferred plant species a fidelity level (Table 6) was calculated to quantify their importance to treat a major ailment [42]. It was calculated based on the number of users of a given plant species to treat a major ailment. FL shows the proportion in percentage of informants claiming the use of a plant species for the same major ailment to the total number of informants who mention the plant for any use. FL = (I_p/ I_u) x 100 where I_p = Number of informants who suggested the use of a species for the same major purpose (therapeutic use), (I_u) = Total number of informants who mentioned the plant species for any use.

Table 6 shows high fidelity levels of greater than 50 % for seven plant species which highlights the importance of these species in treatment of the mentioned diseases in the study area. Vernonia amygdalina and Erythrina abyssinica had a fidelity level of 100 % in treatment of malaria and vomiting respectively. High FL levels for these species indicated their outstanding preference for treating malaria and vomiting.

Most of the respondents were men with an average age of 52 years. African belief is that traditional healers should be male [43‐45]. A high proportion of key informants being male of 50 years and above is in line with studies in Rwanda [46, 47]. Old people (aged 51–80 years) in society have more knowledge on medicinal plants and their uses due to long direct contact with plant resources. In contrast, younger people have little interest in traditional medicine in general and there appears to be a risk of knowledge loss if nothing is done to motivate them. Younger people are exposed to modern education and hence not interested in learning and practicing ethnomedicinal wisdom that would perpetuate indigenous knowledge. Differences in medicinal plants knowledge among age groups was also reported in other studies [48, 49] in Ethiopia.

The high number of species documented indicates that the study area has diverse flora used in treatment of various ailments and rich traditional knowledge on medicinal plants in the community. This makes Mabira CFR an important source of herbal medicine for the rural communities since more than half of the mentioned medicinal plants were harvested from the forest. High utilisation of medicinal plant species from forests has been reported among the Bakonjo and Bamba in Mt. Rwenzori and Semiliki forest areas in Bundibugyo, Western Uganda [50, 51].

Families Fabaceae, Asteraceae, Euphorbiaceae, Lamiaceae, and Solanaceae are widely reported in herbal preparations in different parts of Uganda [1, 8, 19, 52, 53] and their widespread use could be attributed to their wide range of bioactive compounds. Asteraceae is reported to have a large number of bioactive compounds [54, 55] thus contributing to the high utilization rates of members of the family for medicinal purposes.

A majority of plant species documented treated more than one condition. The use of one plant to treat several ailments is probably attributed to presence of many metabolites in one particular plant and also the fact that the same molecule can be active against different pathogens. In other instances a combination of plants were used in preparation of a herbal remedy against a certain ailment which illustrates the synergistic effects of such plants. As an example Amaranthus spinosus and Cleome gynandra leaves were used against fungal infections of the scalp, Balanites aegyptica roots are mixed with leaves of Citrus limon against diarrhoea. On the other hand some remedies were monotherapies based on preparations from a single plant. Such plants could be palatable, nontoxic and highly effective against ailments they are used to treat based on experience of users.

Most of the medicinal plant species collected and identified in the study area were also medically used in other areas of Uganda [1, 19, 56] and other parts of Africa [57] to treat the same or different ailments. The use of the same plant species for similar or different ethnomedicinal uses in different countries is a reliable indication of the bioactivity potential of the documented plant species [58]. Of the 190 medicinal plant species identified in the current study, 34 species were identified earlier in Iganga Eastern Uganda [59], 82 species in Mukono and Mabira forest areas [60], 22 species in Western Uganda [1], 40 species in Mpigi [52] and 30 species in Oyam Northern Uganda [8]. A comparison of ethomedicinal uses of some plant species used in Mabira CFR communities with other parts of Uganda and in other countries is presented in Table 7. Bioactivity studies previously conducted on some of the identified plant species collaborate their ethnobotanical uses. For instance Capsicum frutescens is used in management of different cancers – an activity attributed to presence of capsaicin which possesses antimutagenic and anticarcinogenic activities [61]. Also Prunus africana has been found to possess anti-inflammatory and antioxidative activities and compounds like cytotoxic phenolics and beta sitostenone, n-docosanol [62] which are important in management of cancer. The ethnomedicinal reports of the same plant species across geographical regions and different cultural groups is indicative of the medicinal properties of the species.

The use of leaves to make herbal medicine preparations followed by roots and barks is a common practice in many communities in Uganda as reported in Mukono [60], Sango bay in Southern Uganda [16], Western Uganda [1], communities around Kibale National Park [63], Mpigi [52] and other countries like Kenya [64], Ethiopia [65] and Bolivia [66]. The high utilisation rates of leaves could be attributed to the ease with which they can be obtained in large quantities compared to other plant parts. Leaves are the main photosynthetic organ in plants and considered to be a key component of the natural pharmacy for synthesis of constituents particularly those that are more pharmacologically active against diseases [67]. The preference of leaves to other plant parts is thus thought to be due to accumulation of active ingredients like tannins and other alkaloids [67]. In contrast, in Oyam district of Northern Uganda, roots were the common plant parts used in herbal medicine preparations and the other parts were underutilized [8]. However, as noted [68] a clear relationship exists between the parts of the plant collected, or the collection method and the impact on the harvested plant. Collection of the bark and root is damaging and makes species vulnerable to overexploitation. Harvesting the bark in large quantities can destroy the plant because the protective role of the bark to the plant will be curtailed. On the other hand uprooting plants especially in case of herbs and shrubs causes total destruction of the plant. Debarking and uprooting of medicinal plant species negatively affects the sustainability of the species in use. For species like Spathodea campanulata, Tamarindus indica and Phytolaca dodecandra in which more than one parts is used; sustainability would probably be achieved if the harvesting of bark and root is avoided and harvesting of leaves which is less destructive is promoted. The use of leaves is less destructive if small quantities are collected but not so if large quantities are harvested. As noted [69], overharvesting of leaves can lead to deterioration of medicinal plants since removal of leaves limits the transformation of vegetative to reproductive development such as flower production and seed/fruit development which in turn limits the natural regeneration of plants. Harvesting of roots on the other hand is more destructive as it often involves uprooting whole plants which consequently affects regeneration for sustainable use.

Herbal preparations made from more than two plant parts of the same plant such as the bark and roots of Psedospondias microcarpa, leaves, bark and roots of Spathodea camapnulata and the leaves, roots and vines of Croton macrostachyus (Table 1) may endanger the species unless mechanisms for sustainable utilisation are put in place. Many studies have showed that leaves of different plants possess bioactive ingredients against different diseases and pathogens [69‐72]. Since harvesting of leaves is less destructive than harvesting roots or barks, it is necessary to test leaves for efficacy against different ailments in plants where roots and barks are mostly harvested to minimize dangers of overexploitation. As an example the leaves of Vernonia amygdalina have been found to be effective against malaria [73] and thus the harvesting of roots of this species can be avoided.

Herbs were the most common plant life forms used for medicinal purposes. Harvesting of herbs that are in most cases annual is an indicator that collection of medicinal plants from the forest is not a big threat to conservation. This could be attributed to their abundance throughout the year as reported previously in Uganda [15, 19, 53, 63] although shrubs were reported to be commonly used in northern Uganda [12] and in Ethiopia [74]. The popularity of herbs as a source of herbal therapies is often attributed to their high pharmacologically active ingredients as compared to woody plants [8]. Shrubs are preferred due to their availability all year round since they are relatively draught resistant and are not affected by seasonal variations [65].

Traditional healers interviewed lacked medicinal plant gardens and collected medicinal plants from the forest. A similar trend was reported in Zimbabwe [75] but cultivated plants have been used from ancient times such as in Iran and various studies have confirmed potency of chemical constituents in them [14]. However, commercial collectors require large volumes which put pressure on the plant population. Consequently, overexploitation may lead to disappearance of many species of economic value and other uses pausing challenges to their conservation in Uganda’s forests [76] and the African continent as a whole [77].

The main route of herbal medicine administration was oral. This mode of administration is commonly used in many herbal remedies as reported elsewhere [8, 78, 79]. The choice of oral administration may be related to the use of some solvents or additives such as water and food that are commonly believed to serve as a vehicle to transport the remedies. The additives enhance extraction of bioactive molecules during remedy preparation. The additives are also important to minimize discomfort, improve taste and reduce adverse effects such as vomiting and diarrhoea. [80] Decoctions were cited as the most common method of preparation of herbal remedies. Boiling is effective in extracting plant materials and at the same time preserves the herbal remedies for a longer period compared to cold extraction. However, both decoctions and cold extracts do not offer long shelf life for the preparations [81]. As such users continuously harvest medicinal plants which puts them under a lot of pressure that may lead to over exploitation.