Diversity and use of ethno-medicinal plants in the region of Swat, North Pakistan

Background Due to its diverse geographical and habitat conditions, northern Pakistan harbors a wealth of medicinal plants. The plants and their traditional use are part of the natural and cultural heritage of the region. This study was carried out to document which medicinal plant species and which plant parts are used in the region of Swat, which syndrome categories are particularly concerned, and which habitat spectrum is frequented by collectors. Finally, we assessed to which extent medicinal plants are vulnerable due to collection and habitat destruction. Methods An ethnobotanical survey was undertaken in the Miandam area of Swat, North Pakistan. Data were collected through field assessment as well as from traditional healers and locals by means of personal interviews and semi-structured questionnaires. Results A total of 106 ethno-medicinal plant species belonging to 54 plant families were recorded. The most common growth forms were perennial (43%) and short-lived herbs (23%), shrubs (16%), and trees (15%). Most frequently used plant parts were leaves (24%), fruits (18%) and subterranean parts (15%). A considerable proportion of the ethno-medicinal plant species and remedies concerns gastro-intestinal disorders. The remedies were mostly prepared in the form of decoction or powder and were mainly taken orally. Eighty out of 106 ethno-medicinal plants were indigenous. Almost 50% of the plants occurred in synanthropic vegetation while slightly more than 50% were found in semi-natural, though extensively grazed, woodland and grassland vegetation. Three species (Aconitum violaceum, Colchicum luteum, Jasminum humile) must be considered vulnerable due to excessive collection. Woodlands are the main source for non-synanthropic indigenous medicinal plants. The latter include many range-restricted taxa and plants of which rhizomes and other subterranean parts are dug out for further processing as medicine. Conclusion Medicinal plants are still widely used for treatment in the area of Swat. Some species of woodlands seem to be adapted to wood-pasture, but vulnerable to overcollecting, and in particular to deforestation. It is suggested to implement local small-scaled agroforestry systems to cultivate vulnerable and commercially valuable ethno-medicinal woodland plants under local self-government responsibility.


Introduction
Plants are an important source of traditional medicine for the treatment of various diseases [1]. It has been estimated that herbal medicines are used by more than 80% of the world's population in developing countries to meet their primary healthcare needs [2]. In Pakistan, the available modern healthcare services are either insufficient or inaccessible and unaffordable to the majority of people. In addition, due to illiteracy and poverty most of the population is dependent on traditional phytomedicine to cure various ailments. As the country has diverse socioeconomic, ethnic, linguistic and cultural areas, as well as unique biodiversity, copious knowledge of indigenous medicinal plants and their use in treating human ailments might reasonably be expected. More than 10% of the national flora of Pakistan (600-700 plant species) are used for medicinal purposes [3]. Phytomedicinal research in Pakistan is a recent activity and the documentation of ethnomedicinal plant knowledge and its applications are ongoing [3][4][5][6]. The loss of precious medicinal plant wealth due to overgrazing, agricultural expansion, environmental degradation, acculturation and deforestation, enhanced by population pressure and poverty, has been reported by various researchers [3,[7][8][9][10] but information on which medicinal plant species in particular are vulnerable, and why, is lacking.
Traditional resources of medicinal plants from Chitral, North Pakistan, have been evaluated [7,11]. Several studies exist on the ethnomedicinal use of plants in different regions of Swat, North Pakistan [8,[12][13][14][15]. In an ethnomedicinal study from the valley of Miandam, Swat, a total of 179 plant species have been listed [16], with medicinal use reported for 27 plants, but without reference to local names, habitats, and which parts of these plants are used. Recording the indigenous knowledge of medicinal plants is an urgent task. Traditional knowledge is usually passed verbally from generation to generation, and valuable information about medicinal plants is easily lost if not preserved in written form. The main objective of the present study was therefore to survey and to document the scattered indigenous knowledge of medicinal plants of the Miandam valley as basis for future phytochemical and pharmacological studies. Moreover, and for the first time in any region of Pakistan, the medicinal plants of the study area are classified according to biological and distributional properties as well as ecological preference. It is essential to know where and in which habitats ethno-medicinal plants occur, as such knowledge is a prerequisite to identify vulnerable plant species susceptible to collecting or habitat change.

Study area
The valley of Miandam, Swat, is a well-known summer resort in northern Pakistan. Located about 50 km northeast of Saidu Sharif, the valley lies between 35°4' N and 72°2 9-32' E in the mountain range of Hindu Raj [17]. The study area ranges between 1400 to 3900 m a.s.l. It is a narrow valley with a number of gorges, bounded on the north, east and south by high mountains. Its western boundary is the river Swat. Gujars (Indian Aryans) and Yousafzai (Pakhtoon) are the two main tribes residing in the area. Their main source of income is agriculture (nearly 41%) [18] and most of the population of the study area is directly or indirectly engaged in it. Miandam is a mountainous region and the cultivated land is insufficient for subsistence. Additional sources of income are daily wages and salaries (20%), foreign and domestic remittances (17%), forest products including medicinal plants (12%) and other professions (10%). Findings from [19] reveal that 59% of the households in north-western Pakistan derive their income from the forests.
Due to its considerable variation in altitude, temperature, topography, soil type and moisture, the vegetation of Miandam Valley can be classified into a series of altitudinal belts, namely dominated by Olea ferruginea and Quercus oblongata (submontane), Pinus wallichiana, Abies pindrow, Picea smithiana and Quercus semecarpifolia (montane), and alpine-subalpine flora, respectively [16]. See also the vegeation maps of the northern Pakistan regions of Chitral and Hunza [20,21].

Methods
Regular field surveys were carried out in the Miandam valley from September 2010 through July 2011 in order to document the habitats and indigenous uses of ethnomedicinal plants of the valley. The surveys were carried out at different seasons so as to obtain identifiable plants and multiple information and also to cross-check the information provided by the local informants during earlier visits. We interviewed a small group of chiefly elder people of both Gujars and Yousufzai tribes who were highly esteemed in their societies due to their sound knowledge of medicinal plants. Structured questionnaires, formal and informal interviews and participatory observations were used to inquire about vernacular names, used plant parts and the process of remedy preparation. We did not encounter controversial issues among the informants but commonly received complementary information. Moreover, for each plant species growth forms (tree, shrub, woody climber, perennial herb, annual or biennial herb), plant status (indigenous, established alien, cultivated), abundance in the area (common, scattered, rare) and habitat preferences (arable fields, ruderal sites, wetland, woodland, mountain grassland) were recorded. Voucher specimens were identified using relevant standard literature [22][23][24][25] and submitted to the Herbarium PUP at the Department of Botany, University of Peshawar. Plant nomenclature was updated using the World Checklist of

Results and discussion
Plant diversity, use and applications A total of 106 ethno-medicinal plant species belonging to 96 genera and 54 plant families were recorded. The plants have been used to treat a wide range of diseases from simple headache to complex disorders of kidney and liver. The results are presented in Table 1 with family names in alphabetical order, taxon name, local name, parts used, medicinal use, growth form, plant status, frequency and habitat preference. Perennial herbs were the most common growth form among medicinal plants (43%), followed by annuals and biennials (23%), shrubs (16%) and trees (15%) As far as documented the use of herbs for remedy preparation in the study area is in consistence with other studies [11,[26][27][28][29][30][31][32][33][34][35][36][37][38][39][40].
Ninety-nine of the species (93%) are used for human ailments, three species (3%) for livestock cure and four (4%) to treat both human and livestock ailments. No less than 44 plant species were used to treat gastro-intestinal disorders such as dyspepsia, dysentery and stomach-ache followed by the treatment of dermatological diseases with more than 25 herbal remedies. Ten species were used against skeleto-muscular complaints like rheumatism, backache and muscular pain. Sixteen species were used to cure respiratory problems such as cough and asthma, fourteen for urinary complaints, twelve for cardio-vascular complaints and circulatory diseases, twelve to treat fever and headache, eleven for genital and sexual diseases, six for dental problems, six for ear, nose, throat (ENT) and eyes diseases, two for nerve disorders, one species (Spiraea spec.) was used to ease childbirth, and eighteen species for other purposes (wounds, cuts, narcotic, tonic, anticancer and tumor) ( Table 2). The leaves of Skimmia laureola are used for spiritual purposes.
A single plant species may be used to cure several human ailments ( Table 2). Some of the remedies were prepared by combining different plants such as the powdered rhizome of Dioscorea deltoidea mixed with powdered root of Berberis lycium for the treatment of jaundice and ulcers. Similarly, root decoction of Geranium wallichianum with pods of Pistacia chinensis was used for curing urinary complaints, cough and fever. According to traditional healers, complex medicines of two or more plant species are more potent than those prepared with single species. This has been attributed to interactive effects of the plants [41]. The most common medicinal recipe preparation was in powder form followed by decoction, infusion, juices, poultice and paste.
The traditional healers and local herbalists of the region usually utilize every part of the plant. However, the use of a particular plant part depends on the plant habit and user's needs. The most frequently used plant parts in the preparation of herbal remedies were leaves (29%), followed by fruit (18%), roots and rhizomes (17%), and whole plants (7%). Seeds (9%), flowers (8%), bark (7%), bulbs (2%), capsules, floral shoots and insect galls (1% each) have also been used. The use of specific plant parts suggests that these parts have strongest medicinal properties but it needs biochemical analysis and pharmaceutical screening to cross-check the local information. Our findings of the frequent use of green leaves in the preparation of remedies corroborate the results of [42][43][44][45][46].
Different liquids such as water, juices, sugar, tea, honey, mustard oil, desi ghee (butter) and milk are mixed with plants or plant parts during the preparation of the remedies. The prepared remedies are mostly administered orally (77%), less frequently dermally (10%) or both orally and dermally (12%). Only 1% is administered through ears or eyes.

Habitats and conservation of ethno-medicinal plants
Eighty-two out of 106 medicinal plants are indigenous to the area while the others are cultivated (19) or established alien plants (5). The latter groups are of no conservation concern as they are common (17) or scattered (7) in the study area. Also among the indigenous medicinal plants the majority of species is common (59%) or scattered (35%) in the area, thus neither of immediate conservation concern. Only five medicinal plant species (6%) are rare in the study area: Aconitum violaceum, Colchicum luteum, Elaeagnus umbellata, Jasminum humile and Sambucus wightiana. Sambucus and Elaeagnus are woodland shrubs of which leaves and fruits or leaves and flowers, respectively, are collected for medicinal purposes. Since this kind of harvesting is non-destructive, the rarity of the shrub species is apparently not caused by overcollection. In contrast, populations of Aconitum violaceum, Colchicum luteum and Jasminum humile may be harmed since rhizomes, corms or whole plants are collected, respectively. In these cases, plant populations should be monitored to avoid overcollection.
The synanthropic flora (i.e., occurring in arable fields or ruderal sites) contains a high proportion of the ethno-medicinal plants. Slightly under 50% (51) out of the 106 ethno-medicinal plant species occur in manmade habitats (in arable fields 27 species, most of which being cultivated; another 24 in ruderal sites). Since they can be expected to grow abundantly in or near settlements, or are even cultivated and harvested, they may be collected without much effort, and in suitable quantities. Slightly more than 50% (55) of the ethno-medicinal plant species encountered in the study area occur in seminatural habitats (though extensively grazed or otherwise used). Most species of the latter group (47) occurred in different kinds of woodland, while only few occur in wetlands (4) and mountain grasslands (4). Mountain grassland medicinal plants known in the Miandam valley comprise Colchicum luteum, Corydalis stewartii, Nepeta cataria and Thymus linearis. Since Himalayan mountain floras are rich [45][46][47] and the local almost certainly contains more species of pharmaceutical value, we assume that the habitat is too remote and too difficult to access to be of much interest as a "medicinal plant hunting area" for the people in the Miandam valley.
Woodlands are the main source for non-synanthropic indigenous medicinal plants. They comprise 21 woody plants (apart from the climber Hedera nepalensis, seven trees and thirteen shrubs), two short-lived and 24 perennial herbs. Almost half of the perennial herbs are dug to collect the stem base (Primula denticulata) or chiefly the rhizomes (Aconitum violaceum, Arisaema jacquemontii, Bergenia stracheyi, Delphinium denudatum, Dioscorea deltoidea, Paeonia emodi, Podophyllum hexandrum, Polygonatum multiflorum, Polygonatum verticillatum). Except the latter Table 2 List of ethno-medicinal plants applied with different syndromes two, these species are range-restricted taxa of Himalayan or narrower distribution. Due to their biochemical components they are largely unpalatable for livestock, hence fairly resistant under the widespread practice of wood-pasture, but may be vulnerable to overcollecting for medicinal purposes, although so far only Aconitum violaceum is considered rare in the study area. A currently more serious threat to the ethno-medicinal plant wealth of the woodlands as well as to the social and economic basis of the rural population in northern Pakistan is excessive timber exploitation leading to deforestation and habitat destruction.

Conclusion
The Miandam valley in northern Pakistan is very rich in commercially and pharmaceutically important ethnomedicinal plant species. The locals, in particular traditional healers, have centuries-old knowledge regarding the uses of the plants, and the locals use these species in a traditional way for curing a wide spectrum of diseases. Few species were found to be vulnerable probably due to overcollection. Especially perennial woodland herbs with rhizomes are of conservation concern. The local inhabitants depend on plants for the treatment of diseases but not all are familiar with the proper collection, parts to be used, preservation and storage. In contrast, local traditional healers are familiar with proper collection and use of medicinal plants, and they should be involved in efforts of conservation and sustainable use of ethnomedicinal plant resources. In view of the outstanding importance and ecosystem services of woodlands and forests in northern Pakistan the currently widespread and uncontrolled deforestation is a serious threat both to ecological and social sustainability as well as to the long-term economic basis of the local population [19]. It is also a threat to the ethno-medicinal plant wealth. For purposes of plant conservation and to increase the locals' income we suggest to cultivate vulnerable woodland medicinal plants of commercial value in newly designed and locally administered self-government agroforestry systems. Due to the specific habitat demands of many woodland plant species better results may be obtained through well managed agroforestry systems than in ex-situ sites [48].