Medicinal plants and herbalist preferences around Bwindi Impenetrable National Park

1 Natural Chemotherapeutics Research Institute, Ministry of Health, P.O. Box 4864, Kampala, Uganda. 2 Department of Plant Sciences, Microbiology and Biotechnology, College of Natural Sciences, Makerere University, P.O. Box 7062, Kampala, Uganda. 3 Hamilton A.C., Head, International Plants Conservation Unit, WWF-UK, Panda House, Weyside Park, Catteshall Lane, Godalming, Surrey GU7 1XR, UK. 4 Hoeft, Robert, 609 Broadway, Berlin, WI 54923-1357, Germany.


INTRODUCTION
The art of traditional medicine has been practised for many years in the third world countries including Uganda (Malini et al., 2013;Ondicho et al., 2015).In Africa, communities have relied upon the spiritual and practical skills and knowledge of the traditional medical practitioners for many years (Kiringe, 2006b;Winkler et al., 2010).Pharmacognosy has since then evolved into a sophisticated science that is emerging to the forefront of drug discovery.This knowledge has been retained in some cultures such as, the Asian culture because the information was handed down in written form unlike in Africa and South America where knowledge was passed on by word of mouth.To date, knowledge is still getting lost due to death of the elderly people who are custodians of indigenous knowledge, migrations, regional conflicts and urbanisation among other causes.Traditional medicine is more accessible than modern health facilities to most of the population in the developing world such as Uganda because it is relatively inexpensive, locally available, usually accepted by the local communities and poor healthcare delivery systems (Sambo, 2010;Osemene et al., 2011).
In Uganda, people became more aware of the importance of traditional healing systems.Medicinal plants were reportedly widely used by traditional midwives, bonesetters, spiritualists and other categories of Traditional Health Practitioners (Tabuti, 2008).There was also a marked shift from medicinal plant collection by herbalists towards commercial harvesters including international pharmaceutical companies; and this was partly due to the high potential economic value of drugs derived from medicinal plants globally (Lev, 2006a;Omonona et al., 2012).It was observed that 74% of the plant-derived compounds currently used in pharmaceuticals retained the same or similar use by traditional healers (Moran, 1997).Development of western drugs from medicinal plants, therefore, depends on cultural as well as species survival (King, 1996).
Herbalists around Bwindi Impenetrable National Park tend to believe that wild harvested medicinal plants are more effective than cultivated ones (Bekele, 2007;Cunningham, 2001;Ngarivhume et al., 2015).Alongside the global concern about the increasing need for healthcare (Bodeker, 1994;Delloite, 2015), there is need to ensure the sustainable use of wild medicinal plants, their safety and efficacy.Reports by UNESCO show that the wild harvest supply of traditional medicine is failing to meet the ever-increasing demands of the people (WHO, 2005;Bandaranayake, 2006;FAO, 2016).
A change in land use to cater for agriculture, agroforestry and fuel supply, whilst increasing weedy species used medicinally, has resulted in a decline in the total area of natural vegetation available as a source of herbal medicines, especially forest species (Cunningham, 1996).Phillips et al. (1994) demonstrated that some vegetation types are much more important to local people than others in terms of use value.However, it has not been demonstrated quantitatively that tropical medicinal plants are concentrated in primary as opposed to disturbed forest vegetation.Voeks (1996) reported that healers demonstrated a strong preference for disturbed over primary forest and that there may be an intrinsic medicinal value of disturbance species.Iwu (1993) reported that Africa has the highest rate of deforestation in the world.Habitat conversion threatens not only plant resources but also traditional and cultural diversity and the associated knowledge of medicinal value of several species.This study was carried out around Bwindi Impenetrable National Park to establish how the use of medicinal plants by traditional birth attendants is compared to that by other herbalists in terms of sustainability and habitat preference and specificity of collection.Information obtained is important in utilisation and conservation of medicinal plants used by communities around Bwindi impenetrable National Park.

Study area
Bwindi Impenetrable National Park is located in South-Western Uganda at longitude 29° 35 I to 29° 50 Í E and latitude 0° 53 I to 1° 8 I S. It is situated at the edge of the Western Rift Valley and occupies the highest block of Rukiga Highlands.It lies at the Ugandan border with the Democratic Republic of Congo, about 29 km north of Kabale town, 18 km north of Kisoro and 40 km South-East of Lake Edward.The park shares boundaries with three districts in southwestern Uganda (Kanungu, Kisoro and Kabale).It is bordered by parishes with high population density and agricultural activity which is particularly notable in the districts of Kanungu and Kabale.The communities in these areas are composed primarily of two ethnic groups dominated by Bakiga who are a group of Bantu speaking agriculturalists with a long history of association with the forest and still use many forest products.The other group are the Abayanda who are concentrated in the extreme south-western corner of Uganda within 2 parishes of the park boundary (Kabananukye and Willy, 1996).In this study, information was collected from five parishes around the park namely; Kitojo, Nteko, Mpungu, Nyamabale and Rutugunda.
Participatory rural appraisal (PRA) methods were the main methods employed in obtaining the ethnobotanical information required for this study.Both qualitative and quantitative approaches were used to collect information on medicinal use of the plants.The qualitative methods included informal conversations, semistructured interviews, free listing, field excursions and visits to local markets while the quantitative methods included preference ranking and pairwise ranking.Local authorities and established TMP and TBA committees were used to identify and locate the locally recognised herbalists in each of the selected parishes.A total of 100 people were interviewed.
Informal conversations involved participating in conversations with local people and directing the conversations towards the issue of medicinal plant use without formally explaining the intention to carry out a study and the information collected would be recorded immediately after the conversations.Meeting places included churches, women-group meetings, homes, drinking places, pathways and gardens.Field excursions involved a walk together with herbalists as they went to collect herbal medicines especially from the forest.This was mainly possible in multiple-use zones where group arrangements were made for collection of medicinal plants from the forest from time to time.The information gathered on such occasions supplemented that from other methods on local plant names, parts used and other aspects of medicinal plant use.In each of the parishes visited during this study, there is at least one market place recognised by the local people and there is a market day at least once a week.This provided an opportunity to carry out market surveys in each of the parishes visited.In each of the markets visited, the local names, growth forms and parts of the medicinal plants being sold as well as the gender of the vendor were recorded.Semi-structured interviews were conducted in the local language (Rukiga) with each of the respondents selected for this study by use of interview schedules.The place and time of the interview were arranged well in advance at the interviewee's convenience to avoid inaccuracy resulting from inconveniencing the respondents.Free listing was carried out to obtain a list of medicinal plants given by each of the 100 people interviewed in the study.For each of the plants listed, the part(s) used and, where possible, the disease(s) treated were recorded.With each interviewee, voucher specimens of the plants listed were collected and identified at Makerere University herbarium and deposited there.Pair wise and preference ranking techniques were used to study the ranking given to each of the different types of habitats.The ranking was done with 80 respondents, 20 from each of the categories of herbalists.Each respondent ranked six different types of habitats in their order of preference.Preference ranking was done in order of preference of medicinal plant collected to obtain total ranks by the total number of rankers.While pair wise ranking was done to obtain a total score computed for each type of habitat.The higher the total score, the more preferred, the given type of habitat.

Ethical approval
Ethical clearance was received from the Faculty Ethical Review Committee of Kyambogo University.

Data analysis
Epi-Info version 6 was used for both data entry and analysis.Frequencies were produced and Chi-square test was used to test for association between herbalist categories and growth forms of plants, habitats and parts used.The rest of the data were summarised and analysed manually.

RESULTS
Majority of the respondents (99%) revealed that they use medicinal plants to treat themselves and/or other people in or outside their families.Only one person said she did not use medicinal plants though she was able to list some plants that she knew were medicinal.Most of the respondents (90%) had used medicinal plants for at least five years.Majority of the respondents (58%) were above 50 years of age.Many of these (51%) were not educated, only 2% had secondary education.

Medicinal plants in and around Bwindi
About 288 medicinal plant species were listed.Of these, 257 were identified belonging to 204 genera in 84 families.Sixty-nine species could not be collected as most of them were reported to be so rare and difficult to get.Thirteen species could not be identified and have, therefore, been represented by their local names given by respondents.The average number of plants mentioned per herbalist was 20, while the highest and least numbers of species mentioned by herbalist were 165 and 2, respectively.
According to Table 1, the most frequently mentioned genera by respondents were Vernonia (8 species), Solanum (6 species), Pentas, Ficus, Crotalalia and Crassocephalum respectively.Hibiscus fuscus was the most frequently mentioned species.The plants were collected in different habitats including; garden, early fallow, mature fallow, bushy thicket and forest.Most (30%) species mentioned by respondents were collected from the mature fallow; followed by the bushy thicket and forest at 21.5 and 21.2%, respectively.Among the respondents, the male non-specialists (MNS) mentioned Rytiginia species more often than all the other herbalist categories.
All plant parts were found to be harvested for medicine in different proportions.Leaves were the most frequently harvested (70.9%) plant part, followed by roots (10.8%) as shown in Figure 1.

Growth forms
All plant growth forms of medicinal plants including herb, shrub, tree, liana and grass were mentioned by respondents.One fungus was mentioned among the medicinal plants as seen in Figure 2. Majority (49.1%) of the plant species mentioned by respondents were in form of herb, followed by shrubs (26.1%).

Commercial harvest of medicinal plants
Some medicinal plants sold in the local markets around Bwindi Impenetrable National Park that were visited during the study were listed; and their habitats and parts sold are documented as shown in Table 2.

Differential medicinal plant use by herbalists
Differences in medicinal plant use between the different categories of respondents were observed.The categories included male herbalists (MH), traditional birth attendants (TBA), female herbalists (FH) and male non-specialists (MNS).The differences were noted in the following aspects: average number of plants mentioned per respondent, number of species used singly, plant parts used, habitats from which herbalists collect medicinal plants and growth forms of plants used by respondents.The differences in the numbers mentioned are given in Table 3.
The specialist herbalist categories (TBA and MH) listed more plant species than the non specialist categories (FH and MNS).The male herbalists mentioned more medicinal plants than the rest of the categories.The number of plants used singly by non-specialists is higher than that used singly by other herbalist categories.
Although, the p value does not indicate significant differences between the different categories of herbalist as far as the use of various growth forms of plants is

Plant growth form
Species use (%) concerned, the herb is the most used growth form for all herbalist categories.It can also be seen from Table 4 that the specialist herbalist categories (TBA and MH) collect more proportions of herbaceous plants than the non specialist categories (FH and MNS) that, comparatively, collect more proportions of trees than the former.

Differences in use of plant parts
The p value < 0.05 indicates highly significant differences between various herbalist categories.Although, leaves are the most frequently used plant part in all the herbalist categories, they are most frequently used by traditional birth attendants (TBA) and women herbalists (FH) than their male counterparts.It can also be seen that the male herbalist categories (MNS and MH) collect more from the root and bark parts of the plant as compared to their female counterparts.

Differential habitat preference by herbalists
The proportions of plants collected by the different   6 indicate significant differences between the various herbalist categories regarding their use of the various habitats for collection of medicinal plants.The highest percentage of plants used by the male herbalists and non-specialists are commonly collected from the forest.On the other hand, most plants used by TBA and women herbalists are collected from mature fallow and bushy thicket, respectively.The garden is the least source of medicinal plants for all the herbalist categories.Of the four herbalist categories, the male non specialists mentioned the least number of plant species from gardens followed by the male specialists.While plants mentioned by the female herbalist categories (TBA and FH) were evenly distributed among various habitat categories, more than 50% of those mentioned by their male counterparts (MH and MNS) were collected from the bushy thicket and forest vegetation habitats.The MNS mentioned the highest percentage of plants from the forest.

Habitat categories
Positions of the various habitat categories (stages of succession) as obtained from preference and pairwise ranking by the respondents are given in Table 7. Similarity was observed in the habitat preferences of traditional birth attendants and the women herbalists ranking mature fallow and bushy thicket, respectively, in the first position.On the contrary, both male herbalists   Category of respondents: TBA-traditional birth attendants; MH-male herbalist; FHfemale herbalist; MNS-male non-specialist.Habitats: GP ground prepared for planting; MF-mature fallow; BT-bushy thicket; F-forest, EF-early fallow; G-garden and the male non-specialists ranked the forest highest, while habitats ground prepared for planting and garden were ranked last and second last, respectively, by all the herbalist categories.Results from pair wise ranking further reveal that these scored more highly with TBA than with the rest of the herbalist categories.

DISCUSSION
Ethnobotany research that explicitly tests hypotheses facilitates its conceptual development.However, most documented studies simply on total uses reported by respondents; assign importance values by subjective a posteriori processes; or simply calculate the percentage of useful plants.Yet quantitative ethnobotanical surveys can be powerful diagnostic tools for conservationists (Phillips et al., 1994).This study used both qualitative and quantitative approaches to conceptualise the output.Many communities worldwide, Uganda inclusive continue to use herbal medicine in health care delivery.This is because communities believe that plants are efficacious and safe and hence widely acceptable to the people (WHO, 2005).Cunningham (1996) found that TBAs around Bwindi Impenetrable National Park used 154 plant species.According to him, TBAs around BINP use medicinal plants for symbolic purposes; preventing premature labour, facilitating labour, removal of placenta, treating swollen breasts or improving lactation and treatment of internal parasites among other treatments.In this study, more plant species (184) used by TBAs were documented.Reasons for the higher number of plants used could be the increased population, as well as the enlarged actual needs of the people.The individual medicinal plant lists in this study indicate a high level of medicinal plant use and knowledge around BINP as indicated by the high average number of medicinal plant species mentioned per respondent.An average number of plants mentioned by the male non-specialist herbalists and the fact that none of the respondents in the study failed to give any medicinal plant names, may indicate that every person in the study area has at least some knowledge on medicinal plants.Some of the people contacted during this study testified that the people around BINP use medicinal plants to treat many ailments since the health centres are located very far from most communities in the area.Only one respondent in this study revealed that she did not use medicinal plants, her husband was a medical assistant and always provided western medicine whenever a family member was sick.Still other people revealed that there are certain illnesses which cannot be cured in hospitals but can be cured using traditional medicine.
The study indicated that most of the medicinal plants mentioned were used in mixtures.This means that respondents collect portions from several plant species in order to make a mixture which is given to the patient.It is believed that, in this case, less amounts of plant material are collected from the individual plant species as compared to the case where a particular plant is used singly to treat an ailment.This indicates, in part, that the amount collected from each plant species may be small enough to allow for the sustainable use of the medicinal plant species.It is also evident from the study that the most frequently used growth form of plants is herbs.Most of the medicinal plant species listed in the study were found to grow mainly in the mature fallow.The reason for this could be accessibility of the habitat as well as the tendency for herbalists to believe that the older the habitat, the stronger the medicine collected from such a habitat.On the other hand, the forest and bushy thicket did not contribute as much as the mature fallow probably because these habitats are commonly far away from homes.People in Kigezi are agriculturalists and tend to cultivate the areas around their homes.This makes it difficult to find vegetation older than what is termed mature fallow in this study.It has been reported that clearing of forests in the Rukiga highlands is thought to have coincided with the influx of Bantu-speaking agriculturalists about 2,200 years ago (Taylor, 1990).According to some of the people contacted in this study, it is traditionally believed that the older the plant, the more important is the medicine prepared from it.This view was expressed by both male and female herbalists.Consequently, herbalists tend to collect medicinal plants from the oldest type of vegetation nearest to their reach.The same reasons could have accounted for the least number of medicinal plants from gardens which also agree with earlier findings by Fuller (1991) and Omonona et al. (2012) that herbalists tend to believe that wild harvested plants are more effective than cultivated plants in herbal medicine.These results are similar to earlier findings by, for instance, Voeks (1996), who observed that secondary forest, was the preferred habitat for local healers and that secondary forests medicinal plants were prescribed for a greater number of ailments.
In earlier studies, it was found that leaves were the most used plant part by herbalists' around BINP (Cunningham, 1996).This study revealed that leaves are the most frequently used plant part by all the herbalist categories, although the females use more leaves as compared to their male counterparts who use more stem bark and roots.There is a possibility, therefore, that medicinal plant collection around BINP is still dominated by collection of leaf material which is less likely to endanger the growth of most of the medicinal plants involved.In Africa, in general and Uganda in particular, women are traditionally considered to be weaker than the men in terms of energy.Consequently, men tend to perform more energy-requiring tasks than women.In reality, harvesting the bark and roots requires more energy than harvesting leaves from plants, especially trees.Biologically, the collection of roots and stem bark from plants endangers the plant life more than collection of leaves.This means that, in this context, medicinal plant use by female herbalists may be more sustainable than that by their male counterparts.
The study showed that the highest percentage of plants used by male herbalists are collected from the forest vegetation while that by the female herbalist are collected from the mature allow and bushy thicket.One of the reasons for these differences maybe because women are always busy at home and do not have enough time to move to the forest to collect medicinal plants.It has been observed that in addition to being providers and promoters of health through their reproductive and productive roles, and related activities, women are actually over burdened in terms of workload and long periods of work (Nakyanzi, 1997;Bezner et al., 2016).It could also be due to the fact that women are always in contact with agricultural and land and can, therefore easily identify medicinal plants in these habitats.The male respondents tend to spend much of their time with forest vegetation while they hunt wild animals, look for timber, and open up ground for agriculture and other activities.This makes them know more about forest vegetation and consequently they collect most of their medicines from this vegetation.The forest in this area is the national park where only registered traditional medical practitioners are allowed to harvest medicinal plant material.It appears that people who are not allowed to get plant material from the national park actually harvest bigger proportions of their medicinal plants from there as compared to those that are allowed to do so, that is, the TBA and MH.However, the actual numbers show that MNS use the least number of plant species.
Looking at the harvest of different growth forms of plants by various herbalist categories and in the light that herbs produce more individuals than trees at a given time, it appears that the plant harvest by non-specialist herbalist categories (FH and MNS) may be more dangerous to the plant species than that by the specialist categories (MH and TBA).This is because the former collect higher proportions of trees than the latter who, in turn, collect higher proportions of herbs.The fact that MNS registered the least number of medicinal plants used may mean a big burden of harvesting on these few plants.Moreover, almost all plants used by the MNS are also used by other categories as well.In this study, Tephrosia vogeli and Raphiostylis beniensis were the only species mentioned exclusively by the MNS.Since the MNS were not allowed to harvest from the park under the multiple-use system, it means that the plant material they harvested was not recorded in the system.This could mean that the amount of Rytiginia species material actually harvested exceeded that expected to be harvested per year in the multiple use zones.This has also been found to exceed the amount allowed per year by far (Kamatenesi, 1997).The fact that female herbalists use more herbaceous plants than their male counterparts may be another reason to believe that medicinal plant use by female herbalist maybe more sustainable than that by their male counter parts.
Results from pair wise and preference ranking also indicate that there are differences in habitant preferences between male and female herbalists.By observation that habitat category(GP) ground prepared for planting scored higher in female herbalists than in their male counterparts, is likely to stem from the fact that these habitats are more important in gardens which occupies the women most of the time.The male herbalists ranked the forest vegetation first, while this was ranked second last and third last by FH and TBAs, respectively.The reasons given for preferring the forest by some of the men were that the forest harbours the strongest and most important medicines and that there is enough secrecy in this environment.The women on the other hand indicated that they go to the forest to harvest those medicinal plants that cannot be obtained outside the forest.The study indicates that the female medicinal plant habitat preference tends to decrease with stages of vegetation succession, while that of their male counter parts tends to increase as the vegetation grows older.The kinds of ailments and diseases treated by men and women also tend to vary bringing about some of the differences observed in habitant preferences.From observation, men try to handle more complicated cases which may have failed in allopathic medicine but do not necessarily require emergency.Women, on the other hand, mainly attend to emergency cases such as births and child sicknesses that do not allow time for someone to move a long distance in order to collect medicinal plants.Consequently women have learnt about many medicinal plants in their surroundings which mainly consist of younger stages of succession in vegetation.

Conclusion
Medicinal plants are an important source of health care for almost all the people around Bwindi Impenetrable National Park.Most of the medicinal plants are not planted in gardens but harvested from fallows, thickets and forests.The study also found out that some habitats are more important to herbalists than others as far as collection of medicinal plants is concerned.There is gender distinction in habitat preference for medicinal plant collection by herbalists.Gender also influences parts of medicinal plants used by herbalists in Bwindi area.It was observed that male herbalists often use more destructive plant collection methods than their female counterparts.

Figure 1 .
Figure 1.Preference of the different medicinal plant parts used by the respondents around Bwindi Impenatrable National Park.

Figure 2 .
Figure 2. Percentage of species use with the various medicinal plant growth forms mentioned by the respondents around Bwindi Impenetrable National Park.N=288.

Table 1 .
Species scientific name, local name, family, habitat and part used of thirty medicinal plant species most frequently mentioned by the respondents around Bwindi impenetrable National Park.

Table 2 .
Scientific name, habit and plant part sold in the local markets around Bwindi Impenetrable National Park.
Most of the plants involved in the commercial harvest were trees.In all the plants except Anisopappus africanus, Cissus adenacaulis and Piper guineense, the stem bark was sold.

Table 3 .
Plants used singly in treatments and frequency of mention of medicinal plants used by the different categories of respondents around Bwindi Impenetrable National Park.

Table 4 .
Percentage of plant growth forms mentioned by different categories of herbalist respondents around Bwindi Impenetrable National Park.

Table 5 .
Percentage of medicinal plant/ part used by different herbalist categories around Bwindi Impenetrable National Park.

Table 5 .
The value of p<0.05 from the Chi-square comparison results in Table

Table 6 .
Percentage of plants collected from the various habitants mentioned by the different herbalist categories around Bwindi Impenetrable National Park.

Table 7 .
Average positions of the habitats as ranked by different herbalist categories around Bwindi Impenetrable National Park.