Journal of Ethnopharmacology 169 (2015) 335–346

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Quantitative ethnobotanical survey of medicinal flora thriving in Malakand Pass Hills, Khyber Pakhtunkhwa, Pakistan Barkatullah a, Muhammad Ibrar a, Abdur Rauf b,n, Taibi Ben Hadda c, Mohammad S. Mubarak d, Seema Patel e,nn a

Department of Botany, University of Peshawar, Peshawar 25120, Pakistan Institute of Chemical Sciences, University of Peshawar, Peshawar 25120, Pakistan c Laboratoire Chimie Matériaux, FSO, Université Mohammed Ier, Oujda 60000, Morocco d Department of Chemistry, The University of Jordan, Amman 11942, Jordan e Bioinformatics and Medical Informatics Research Center, San Diego State University, San Diego 92182, USA b

art ic l e i nf o

a b s t r a c t

Article history: Received 9 February 2015 Received in revised form 22 April 2015 Accepted 25 April 2015 Available online 4 May 2015

Study objective: Ethnobotanical knowledge is proving to be invaluable for drug discovery in the wake of effective prospecting from biodiversity. On the other hand, the escalating human pressure is threatening the endogenous flora. Situated at the foothill of the Himalayas, Pakistan boasts of rich floristic distribution. However, many lush yet imperiled regions of this country has never been explored. It inspired us to evaluate and document the taxonomic composition, significance of medicinal plants and associated traditional knowledge in the District of Malakand, Khyber Pakhtunkhwa Province. Materials and methods: Vegetation growing in Malakand pass hills, Pakistan was studied and data were collected using an open-ended questionnaire, in addition to interviewing the local elderly, knowledgeable persons, and herbal practitioners. Relative Frequency Citation (RFC) and Use Value (UV) of the medicinal plants were calculated and their correlation was determined by Pearson correlation coefficient. Results: This study encompasses 92 plant species belonging to 56 families thriving in the study area. The information gathered includes ethnobotanical inventory and their pharmacological uses. Quantitative analysis throws light on the consistence of RFC and UV. Asteraceae and Lamiaceae were the most abundant families represented by 6 species each. Shoots were the most used parts (23.6%) and wound healing (7.91%) was the most common therapeutic use. Conclusion: The result obtained from the study implies that local inhabitants rely on these plants for their medicinal requirements. Also, the statistics reveal that, the vegetation can be assessed for potential drug leads. However, urban expansion is threatening the existence of indigenous flora and old generation with ancient herbal wisdom is perishing. So, it appears imperative to preserve the traditional knowledge. This survey is expected to contribute to the discovery of novel bioactive constituents, stimulate conservation efforts of the perturbed flora and promote sustainable exploitation of the medicinal bounty. & 2015 Elsevier Ireland Ltd. All rights reserved.

Keywords: Traditional knowledge Medicinal plants Ethnobotany Malkand Pass Hills Quantitative survey

1. Introduction Since the dawn of civilization, plants are in use as sustenance and medicine. Statistics reflect that nearly 80% of the global population uses plants for their primary health care (Ajose, 2007). Promotion of primary health care is a priority agenda of World Health Organization (WHO). As per an international conference in 1978, Alma-Ata declaration was formulated to encourage community participation, self-reliance, sustainable and integrated approach for health care (WHO). Despite more than three decades of this treaty, it's far from n

Corresponding author. Corresponding author. E-mail addresses: [email protected] (A. Rauf), [email protected] (S. Patel). nn

http://dx.doi.org/10.1016/j.jep.2015.04.052 0378-8741/& 2015 Elsevier Ireland Ltd. All rights reserved.

being a success due to multiple social, political and economic factors (Gillam, 2008). However, the conceived vision still holds pertinence, especially in developing countries (Vasan et al., 2014). Another study reports that two third of the world population depends on medicinal plants for a multitude of ailments (Bibi et al., 2014a, 2014b). Though synthetic drugs and antibiotics are more effective than phytomedicines, they pose higher degree of side effects as well (Vale and Oleastro, 2014). Consequently, the quest for and reliance on herbal medicine has accelerated in recent years (Petrovska, 2012). The rising inclination of Western populace and practitioners towards herbalism has catapulted its global significance (Vickers et al., 2001). Plants are extensively being screened for therapeutic phytochemicals and lead compounds (Katiyar et al., 2012). Ethnobotany, the study of human–plant interactions is deemed crucial in success of the drug discovery pursuits (Heinrich, 2000;

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Barkatullah et al. / Journal of Ethnopharmacology 169 (2015) 335–346

Mandal et al., 2012). Ethnobotanical studies and traditional knowledge are important to set priorities in the local communities and promote sustainable development (Cámara-Leret et al., 2014). Hypotheses from ethnobotany is believed to contribute to natural product databases and expedite pharmaceutical lead compounds identification and derivatization from the pharmacophores (Albuquerque et al., 2012; Patwardhan et al., 2005). The Himalayas, one of the imposing mountain ranges of the world harbors rich floristic diversity (Sharma et al., 2014). In fact, the wonder herb Rhodiola imbricata with immune-stimulatory and radio-protective effect has been recognized here, recently (Tayade et al., 2013). Pakistan, situated at the foothills of this formidable mountain system (lesser Himalaya) has an impressive botanical repertoire due to varying climate ranging from subtropical, temperate to alpine (Abbasi et al., 2013b; Khan et al., 2013). The diversified ecological zones has resulted in 6000 species of flowering plants in Pakistan (Selin, 2008). Therefore, it is important to glean the ethnobotanical information, for conserving the floristic diversity for posterity, and utilizing them for public health management. The inhabitants of Pakistan's remote, mountainous terrain rely on these plants for easing various ailments (Ahmad et al., 2014; Khan et al., 2013). To preserve the traditional knowledge and contribute to drug prospecting, ethnobotanical studies have been conducted in different regions of this country. Literature browsing showed surveys conducted in Malam Jabba, Swat (Sher and Al Yemeni, 2011), Wana, South Waziristan Agency (Ullah et al., 2013), Naran Valley, Western Himalaya (Khan et al., 2013), Mastung of Balochistan province (Bibi et al., 2014a, 2014b), Soan Valley, Salt range (Bibi et al., 2014a, 2014b), Lesser Himalaya (Mujtaba Shah et al., 2014), Nara Desert (Qureshi and Raza Bhatti, 2008), Barawal Bandi, Upper Dir (Hussain et al., 2014), Banda Daud Shah, Karak district (Murad et al., 2013), Lakki Marwat district (Ullah et al., 2014), and Chail valley (Ahmad et al., 2014), to name a few. Khyber Pakhtunkhwa is one of the four provinces of Pakistan. Malakand constitutes a Division of this province and the districts Swat, Shangla, Buner, Chitral, Lower Dir, Upper Dir, and Malakand come under it (Khan et al., 2011a, 2011b). Malakand is a lush valley surrounded by hills. The valley has loamy soil, annual precipitation of 600–650 mm, moderate winters and summers. Malakand Pass Hills has historical relevance and it harbors floristic abundance. To the best of our knowledge, ethnobotanical documentation of flora of Malakand Pass Hills (341350 N 711570 E/34.5831N 71.951E) has never been carried out. Though, ethnoveterinary relevance of flora in Malakand valley near Dir district has been recorded (Ul Hassan et al., 2014). To bridge the gap in knowledge of botanical diversity, this study investigated the indigenous flora of Malakand Pass Hills. The study area included three adjacent villages, Malakand khas, Jaban and Banj. The original inhabitants in this area are Gujars, with native language Gujro and local language Pashto (Khan et al., 2011a, 2011b). The residents earn their livelihood by cattle rearing, selling bovine products and trading forest resources.

Overexploitation and reckless clearance of the forest has put the vegetation in this area under intense pressure. Also, these anthropogenic activities are destroying wildlife habitat. This ethnobotanical study is conducted to address multiple issues, primarily, documentation of the native medicinal flora, preservation of the traditional knowledge, alerting the concerned population against the jeopardy of perturbation and motivating for conservation.

2. Materials and methods 2.1. Data collection For obtaining the data, frequent field trips were made to the investigated area from March 2013 to August 2014 (Fig. 1). The information pertaining to the ethnobotanical uses of the flora were collected by a questionnaire method. The study design consisted of interrogation of the well-versed people and local herbal practitioners on the spot. A total of 87 respondents were interviewed, which included 13.8% pansaris (herbal sellers), 50.6% elders (including both men and women above the age of 50 years), 21.8% in the age range of 20–40 years, and 12.6% young people below 20 years of age as shown in Fig. 2. The traders were questioned for they are assumed to have sound knowledge of medicinal importance of local plants (Sher et al., 2014). Majority of the selected informants were senior folks as casual discussion implied their superior indigenous knowledge compared to the younger generation (Mussarat et al., 2014). Ethnobotanical data regarding vernacular names of plants, traditional usage of plants, and other auxiliary facts was collected. The reports were considered authentic when corroborated by at least 10 interviewees. Demographic distribution of the participants (gender, age, and occupation) was also recorded. The Code of Ethics as set by ‘International Society of ethnobiology’ was adhered to while conducting the interview (The ISE Code of Ethics, 2006). The consent of the inhabitants was taken prior to the survey.

Fig. 2. Percentage of respondent groups.

Fig. 1. The site of ethnobotanical survey of the plants (Malakand Pass Hills, Khyber Pakhtunkhwa, Pakistan).

Barkatullah et al. / Journal of Ethnopharmacology 169 (2015) 335–346

337

Table 1 Plants with voucher number and frequency of uses in the District of Malakand, KPK, Pakistan. No.

Voucher no.

Name

Usage frequencya

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75

Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat

Acacia modesta Wall Acacia nilotica (L.) Willd. ex Del. Adiantum venustum Don Aerva javanica (Burm.f.) Juss. Ex Ailanthus altissima (Mill) Swingle Ajuga bracteosa Wall ex. Benth. Ajuga parviflora Benth. Alnus nitida (Spach) Endl Ammi visnaga (L.) Lam Aristida cyanantha Nees ex Steud. Artemisia scoparia Waldst Asphodelus tenuifolius Cavan Berberis lycium Royle Bauhinia variegata L. Boerhavia diffusa L. Butea monosperma (L.) Taub. Buxus wallichiana Baill. Calotropis procera (Ait) R. Br Cannabis sativa L. Caralluma fimbriata Wall. Carthamus lanatus L. Carthamus oxyacantha Bieb Chenopodium botrys L. Cichorium intybus L. Citrullus colocynthis Schrad Schrad. Conyza canadensis (L.) Cronquist Cuscuta reflexa Roxb Cynodon dactylon (L.) Pers Daphne oleoides Schreb Datura innoxia Miller Dodonaea viscosa (L.) Jacq Dryopteris crenata (Forssk.) Kuntze Dryopteris jaxtaposta Christ. Duchesnea indica (Andr.) Focke Equisetum arvensis L. Eryngium biebersteiniana Nervski Eucalyptus camaldulensis L. Euphorbia hirta Linn Euphorbia prostrata Aiton. Fagonia cretica L. Ficus carica L. Ficus racemosa Linn Fumaria indica Pugsley Geranium wallichianum D. Don E Hyoscyamus niger L. Indigofera heterantha L. Jasminum officinale L. Juglans regia L. Justicia adhatoda Linn. Lotus corniculatus L. Mallotus philippensis (Lam.) Mull. Melia azedarach Linn Mentha longifolia – (L.) Huds. Mirabilus jalapa L. Monotheca buxifolia (Falc.) Dcne ex. Engler Gargura Morus alba L. Morus nigra L. Nasturtium officinale C.Br Nerium indicum Mill. Opuntia dilleni Haw Origanum vulgare L. Otostegia limbata (Benth.) Boiss. Oxalis corniculata L. Peganum harmala L. Paeonia emodi Wall. ex Royle Periploca aphylla Dcne. Pinus roxburghii Sarg. Plantago lanceolata L. Plantago major L. Platanus orientalis L. Portulaca olearacea L. Punica granatum L. Ranunculus aquatilis L. Ricinus communis L. Robinia pseudocacia L.

4 5 2 1 2 6 2 1 2 1 4 2 3 2 2 3 3 3 2 2 2 2 2 2 2 1 3 3 1 2 2 2 2 2 1 1 1 2 1 1 2 2 3 2 3 1 1 3 2 2 1 4 2 2 2 1 2 2 2 2 1 3 1 3 2 1 2 1 2 2 2 2 1 2 2

Bot. 1 (PUP) Bot. 2 (PUP) Bot. 3 (PUP) Bot. 4 (PUP) Bot. 5 (PUP) Bot. 6 (PUP) Bot. 7 (PUP) Bot. 8 (PUP) Bot. 9 (PUP) Bot. 10 (PUP) Bot. 11(PUP) Bot. 12 (PUP) Bot. 13 (PUP) Bot. 14 (PUP) Bot. 15 (PUP) Bot. 16 (PUP) Bot. 17 (PUP) Bot. 18 (PUP) Bot. 19 (PUP) Bot. 20 (PUP) Bot. 21 (PUP) Bot. 22 (PUP) Bot. 23 (PUP) Bot. 24 (PUP) Bot. 25 (PUP) Bot. 26 (PUP) Bot. 27 (PUP) Bot. 28 (PUP) Bot. 29 (PUP) Bot. 30 (PUP) Bot. 31 (PUP) Bot. 32 (PUP) Bot. 33 (PUP) Bot. 34 (PUP) Bot. 35 (PUP) Bot. 36 (PUP) Bot. 37 (PUP) Bot. 38 (PUP) Bot. 39 (PUP) Bot. 40 (PUP) Bot. 41 (PUP) Bot. 42 (PUP) Bot. 43 (PUP) Bot. 44 (PUP) Bot. 45 (PUP) Bot. 46 (PUP) Bot. 47 (PUP) Bot. 48 (PUP) Bot. 49 (PUP) Bot. 50 (PUP) Bot. 51 (PUP) Bot. 52 (PUP) Bot. 53 (PUP) Bot. 54 (PUP) Bot. 55 (PUP) Bot. 56 (PUP) Bot. 57 (PUP) Bot. 58 (PUP) Bot. 59 (PUP) Bot. 60 (PUP) Bot. 61 (PUP) Bot. 62 (PUP) Bot. 63 (PUP) Bot. 64 (PUP) Bot. 65 (PUP) Bot. 66 (PUP) Bot. 67 (PUP) Bot. 68 (PUP) Bot. 69 (PUP) Bot. 70 (PUP) Bot. 71 (PUP) Bot. 72 (PUP) Bot. 73 (PUP) Bot. 74 (PUP) Bot. 75 (PUP)

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Barkatullah et al. / Journal of Ethnopharmacology 169 (2015) 335–346

Table 1 (continued ) No.

Voucher no.

76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92

Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat Barkat

a

Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot. Bot.

76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92

(PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP) (PUP)

Name

Usage frequencya

Rosa webbiana Wall ex Royle Rubus ellipticus Smith. Rubus fruticosus L. Rumex hastatus D. Don Salix babylonica L. Salvia plebeia R. Brown Sarcococca saligna (D. Don) Muell. Solanum nigrum L. Solanum surattense Burm.f. Tamarix aphylla (L) Karst. Tribulus terrestris L. Verbascum thapsus L. Verbena officinalis Linn Vitex negundo L. Withania somnifera (L) Dunal Zizyphus mauritiana L. Zizyphus nummularia (Burm. f.) Wight et Arn

1 2 2 1 2 2 2 3 4 2 2 1 3 3 3 1 1

Usage frequency is the statistical term for the preference for usage in the study area, irrespective of the participant count for the survey.

The plants parts were collected, dried, preserved, and identified using ‘Flora of Pakistan’, the encyclopedia of the plants of Pakistan (Ali, 1982). After verification, they were deposited in the Herbarium of the Botany Department, University of Peshawar, Pakistan, and all species were given voucher specimen numbers for future reference. The plants arranged alphabetically have been listed in Table 1. Frequently used medicinal plants with their traditional uses have been summarized in Table 2.

2.2.3. Pearson correlation coefficient Pearson product-moment correlation coefficient is a quantitative metric of the strength of the linear relationship between two variables. It is the ratio of the covariance between two variables to their standard deviations (Mukaka, 2012). The coefficient can be given by formula n P

2.2. Quantitative ethnomedicinal data analysis

ðxi  xÞðyi yÞ i¼1 ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi r ¼ v" #" # u n n u P P 2 2 t ðxi  xÞ ðyi yÞ

Conversion of the qualitative data into quantitative is essential for hypothesis-testing, statistical validation, and comparative analysis (Hoffman and Gallaher, 2008). Quantitative information increases the probability of identifying the promising pharmacologically important plants (Andrade-Cetto and Heinrich, 2011). Estimation of the importance of each plant is pivotal for its pharmaceutical candidacy. Several canonical metrics exist for ethnobotanical data analysis and interpretation.

where r is the Pearson correlation coefficient for the given sample, x and y are the variables, xi and yi are the values of x and y for the ith individual. The r value of 0 indicates no association between the x and y, whereas a value greater than 0 indicates a positive association. Larger absolute value signifies higher correlation (Zhang et al., 2014). The square of correlation (r2) is the metric of cross species variability in RFC that is explained by the variance in UV (Bano et al., 2014).

2.2.1. Relative Frequency Citation (RFC) The collected ethnomedicinal data was quantitatively analyzed using the Relative Frequency Citation (RFC) index. This indicator shows the local importance of each species and is calculated from the frequency of citation (FC, the number of informants mentioning the usage of the species) divided by the total number of informants in the survey (N), without considering the usecategories (Kayani et al., 2014). RFC can be defined by formula RFC ¼ FC=N RFC value ranges from zero (none of the informant cites the plant as useful) to one (every informant report the plant to be useful) (Sadeghi and Mahmood, 2014).

2.2.2. Use Value (UV) The Use Value (UV) demonstrates the relative importance of locally known plants (Ong and Kim, 2014). It is calculated using formula X UV ¼ Ui =N where Ui is the number of use mentioned by each informant for a given species and N is the total number of informants.

i¼1

i¼1

3. Results and discussion 3.1. Ethnobotanical data from informant reports The present ethnobotanical survey in the Malakand Pass Hills documented 92 species from 82 genera. These plants with voucher numbers and frequency of usage by the locals are summarized in Table 1. Usage frequency is the statistical term for the preference for usage in the study area, irrespective of the participant count for the survey (Jamila and Mostafa, 2014). Other supporting information such as the botanical names, family, plant parts used, applications, administration routes, RFC and UV are presented in Table 2. The collected species belonged to 56 families, 89.3% of which were dicots (50 families), 3.6% monocot (2 families), 5.4% pteridophytes (3 families), and 1.8% gymnosperms (1 family). Among the dicots, Asteraceae and Lamiaceae were the mostrepresented families with 6 species in each, followed by Rosaceae and Solanaceae with 5 species, and then Moraceae with 4 species, Euphorbiaceae, and Apocynaceae with 3 species each. The number of species in the rest of the families ranged from 2 to 1. Monocots were represented by the family Poaceae and Liliaceae (1 species each). Pteridophytes were represented by Dryopteridaceae (2 species), Equisetaceae (1 species), and Adiantaceae

Table 2 Medicinal plants with their family name, local name, parts used, applications, route of usage, FC, RFC and Use values. No. Name

P Ui Use value

References

Parts used

Applications

Route

FC RFC

1 Acacia modesta Wall

Mimosaceae

Palosa

Ullah et al. (2014)

Tonic, aphrodisiac, for backache relief, wound healing

Oral

18 0.22 48

0.56

2 Acacia nilotica (L.) Willd. ex Del.

Mimosaceae

Keekar

Ullah et al. (2014)

9

0.11 22

0.26

Adiantaceae Amaranthaceae Simaroubaceae

Sumbal Spairay Backyanra

Oral Oral Oral

5 0.59 8 2 0.26 5 25 0.29 42

0.94 0.59 0.49

6 Ajuga bracteosa Wall ex. Benth.

Lamiaceae

7 Ajuga parviflora Benth.

Lamiaceae Betulaceae Apiaceae Poaceae Asteraceae

Khwaga Bootei Khwaga Bootei Sharol Jaukay

12 Asphodelus tenuifolius Cavan 13 Berberis lycium Royle

Liliaceae Berberidaceae

Kwaray

14 15 16 17 18 19 20 21 22 23 24

Bauhinia variegata L. Boerhavia diffusa L. Butea monosperma (L.) Taub. Buxus wallichiana Baill. Calotropis procera (Ait) R. Br Cannabis sativa L. Caralluma fimbriata Wall Carthamus lanatus L. Carthamus oxyacantha Bieb Chenopodium botrys L. Cichorium intybus L.

Ceasalpinaceae Nyctaginaceae Fabaceae Buxaceae Asclepiadaceae Cannabaceae Apocynaceae Asteraceae Asteraceae Chenopodiaceae Asteraceae

Kaliar Pandraoosh palasa Shamshad Spalmakka Bangey -

Khan et al. (2013) Ullah et al. (2014) Sher and Al Yemeni (2011) Sher and Al Yemeni (2011) Sher and Al Yemeni (2011) Sheikh (1993) Habib and Waheed (2013) Sher and Al Yemeni (2011) Sheikh (1993) Ullah et al. (2014) Sheikh (1993) Sheikh (1993) Ullah et al. (2014) Ullah et al. (2014) -

Wound healing, to treat headache, anti-cough, tonic, antitoothache Aphrodisiac, anti-stomachache Anti-stomachache Anthelmintic, anti-diarrheal

Oral

3 Adiantum venustum Don. 4 Aerva javanica (Burm.f.) Juss. Ex 5 Ailanthus altissima (Mill) Swingle

Gum, leaves, bark Gum, leaves, bark Shoot Seed Bark

25 26 27 28 29 30 31

Citrullus colocynthis Schrad Schrad. Conyza canadensis (L.) Cronquist Cuscuta reflexa Roxb Cynodon dactylon (L.) Pers Daphne oleoides Schreb Datura innoxia Miller Dodonaea viscosa (L.) Jacq

Cucurbitaceae Asteraceae Cuscutaceae Poaceae Thymeleaceae Solanaceae Sapindaceae

Maraghoonra Dhnyabotey Chambalwaa -

Ullah et al. (2014) Ullah et al. (2014) -

32 33 34 35 36 37 38 39 40 41 42 43 44 45

Dryopteris crenata (Forssk.) untze, Dryopteris jaxtaposta Christ. Duchesnea indica (Andr.) Focke Equisetum arvensis L. Eryngium biebersteiniana Nervski Eucalyptus camaldulensis L. Euphorbia hirta Linn Euphorbia prostrata Aiton. Fagonia cretica L. Ficus carica L. Ficus racemosa Linn Fumaria indica Pugsley Geranium wallichianum D. Don E Hyoscyamus niger L.

Dryopteridaceae Dryopteridaceae Rosaceae Equistaceae Asteraceaee Myrtaceae Euphorbiaceae Euphorbiaceae Zygophylaceae Moraceae Moraceae Fumariaceae Geraniaceae Solanaceae

Kwanjay Lachi Azghakey Inzar Srazela Khurasani

Khan et al. (2013) Sheikh (1993) Hussain et al. (2014) Hussain et al. (2014) Khan et al. (2013) Khan et al. (2013)

8 9 10 11

Alnus nitida (Spach) Endl Ammi visnaga (L.) Lam Aristida cyanantha Nees ex Steud. Artemisia scoparia Waldest

Shoot, root

Oral

27 0.32 88

1.03

Shoot, root

Blood purifier, carminative, anti-cough, anti-asthma, antijaundice, coolant Carminative and anti-jaundice

Oral

12 0.14 16

0.19

Bark Whole plant Whole plant Shoot

Boils softener For cough relief, anti-asthma Anti-nose bleeding Febrifuge, cure for kidney and liver ailments, blood purifier

Oral Oral Paste Oral

4 17 17 32

4 23 17 46

0.05 0.27 0.20 0.54

Leaf Aphrodisiac, condiment Fruit, root, shoot Tonic, cure for wound healing, anti-jaundice

Oral Oral

7 0.08 8 78 0.92 93

0.09 1.09

Root Shoot, seed Flower Leaf Latex Shooot Stem Seed Leaf, seed Seed Shoot, inflorescence Fruit Fruit, seed Stem Shoot Fruit, bark Latex Seed, Stem, Latex Shoot Shoot Fruit Stem Inflorescence Seed Latex, shoot Stem Whole plant Fruit, bark, latex Fruit, latex Shoot Root Leaf, seed

Antidote for snake poison, cure for skin disease Cure for wounds, diuretic Anti-Jaundice, anti- hepatitis, coolant Anti-rheumatic, diaphoretic, febrifuge Anti-stomachache, muscular pain relief, diuretics For wound healing, sedative Anti-pyretic, anti-diabetic Anti-stomachache Antiseptic, to prevent skin inflammation Febrifuge, anti- stomachache, anti-eczema Aphrodisiac, coolant

Paste Oral Oral Oral Oral Oral Oral Oral Oral Oral Oral

3 19 10 22 18 16 41 44 8 15 10

0.04 0.22 0.12 0.26 0.21 0.19 0.48 0.52 0.09 0.18 0.12

5 27 14 66 27 19 53 53 11 32 16

0.06 0.32 0.16 0.78 0.32 0.22 0.63 0.62 0.13 0.40 0.19

To treat digestive disorders, anti-dropsy Coolant Wound healing, urination control, anti- sciatica Blood purifier, wound healing, nose bleeding control Anti-inflammatory Wound healing, narcotic Wound healing, to discharging pus

Oral Oral Oral Oral Oral Oral Paste

9 17 15 11 5 21 35

0.11 0.20 0.18 0.13 0.06 0.24 0.41

12 17 18 15 5 31 57

0.14 0.20 0.21 0.18 0.06 0.41 0.67

Aphrodisiac, febrifuge Aphrodisiac, febrifuge Tonic, eye infection treatment To remove kidney stone Anti-ring worm Cough relief To treat skin disease To treat itching, anti- ring worms Anti-diabetic, febrifuge, jaundice Anti-stomachache, to remove warts from body Anti-stomach, cure for wasp sting Febrifuge, anti-inflammation,body coolant To cure for mouth ulcer, astringent Narcotic, anodyne and cough relief

Oral Oral Oral Oral Powder Oral Paste Paste Oral Oral Oral Oral Oral Oral

4 3 17 13 8 3 1 4 52 9 11 35 26 37

0.05 0.04 0.20 0.15 0.09 0.04 0.01 0.05 0.61 0.11 0.13 0.41 0.31 0.43

7 5 25 13 8 3 1 7 101 13 12. 49 33 80

0.08 0.06 0.29 0.15 0.09 0.04 0.01 0.08 1.19 0.15 0.14 0.57 0.39 0.94

0.05 0.20 0.20 0.38

339

Local name

Barkatullah et al. / Journal of Ethnopharmacology 169 (2015) 335–346

Family

340

Table 2 (continued ) Local name

References

Parts used

Applications

Route

FC RFC

P Ui Use value

Papilionaceae Oleaceae Juglandaceae Acanthaceae Fabaceae Euphorbiaceae Meliaceae

Ghvareja Ghuz Tora-Shandae

Khan et al. (2013) Khan et al. (2013) Hussain et al. (2014)

Shoot Root Seed, bark, leaf Leaf, flower Seed Fruit Fruit, leaf

Oral Paste Oral Oral Oral Oral Oral

4 3 26 12 3 19 21

4 3 29 13 4 19 31

0.47 0.03 0.30 0.10 0.05 0.22 0.36

53 Mentha longifolia (L.) Huds. 54 Mirabilis jalapa L. 55 Monotheca buxifolia (Falc.) Dcne ex. Engler Gargura 56 Morus alba L. 57 Morus nigra L. 58 Nasturtium officinale C.Br 59 Nerium indicum Mill. 60 Opuntia dilleni Haw 61 Origanum vulgare L.

Lamiaceae Nyctaginaceae Sapotaceae

Enaley Gwargwara

Hussain et al. (2014) -

Leaf Leaf, seed Fruit

Cure for digestive disorder Cure for ring worms Brain tonic, anti-toothache, and teeth cleaner Tonic and expectorant. Ahrodisiac, cure for backache Anti-diarrheal Carminative, to treat gastric problems, children fever, and cough Anti-stomachache, carminative Wound healing and discharging pus Laxative, cure urinary disorders

Oral Paste Oral

29 0.34 49 61 0.72 81 13 0.15 19

0.57 0.95 0.22

Moraceae Moraceae Tropaeolaceae Apocynaceae Cactaceae Lamiaceae

Sheikh (1993) Sheikh (1993) Hussain et al. (2014) Ullah et al. (2014) Khan et al. (2013)

Fruit, leaf Fruit, leaf Shoot Shoot Fruit Shoot

Anti-stomachache Anti-stomachache, cure for skin disease Febrifuge and anti-stomachache Analgesic, cure for piles Anti-inflammation, expectorant Diuretic

Oral Oral Oral Oral Paste Oral

7 5 10 7 21 4

0.08 0.05 0.12 0.08 0.25 0.05

7 8 13 10 30 4

0.08 0.09 0.15 0.12 0.35 0.47

62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82

Lamiaceae Oxalidaceae Rutaceae Paeoniaceae Apocynaceae Pinaceae Plantaginaceae Plantaginaceae Platanaceae Portulaceae Punicaceae Ranunculaceae Polygonaceae Papilionaceae Rosaceae Rosaceae Rosaceae Polygonaceae Salicaceae Lamiaceae Buxaceae

Tut Tut Tarmera Gandaraye Jangali majorum Taruke Mamekh Nakhtar Jabae Jabae Chinar Anaar JaghaghaSh Randa Kekar Karwara Tarokey Wala Ladanrr

Hussain et al. (2014) Khan et al. (2013) Sheikh (1993) Khan et al. (2013) Khan et al. (2013) Sheikh (1993) Ullah et al. (2014)

Wound curing, cure for gum diseases Anti-stomachache Emetic, narcotic Analgesic, wound healing To cure gum diseases For discharging pus from wounds Anti-diarrheal Wound healing, laxative For discharging pus from wound Cure for kidney and liver disorder Cure for mouth ulcer, diuretic Anti-ring worm Aphrodisiac, anti- constipation Anti-asthma and febrifuge Cure for piles Diuretic, antidiarrheal Aphrodisiac, carminative Anti-stomachache To treat jaundice and febrifuge Anti-diarrheal, cure for skin and urinary tract irritation Laxative, analgesics

Topical Oral Oral Paste Oral Paste Oral Oral Paste Oral Oral Paste Oral Oral Oral Oral Oral Oral Oral Oral Oral

7 3 19 14 6 19 29 64 9 1 21 12 17 15 4 11 8 3 2 14 11

0.08 0.04 0.22 0.16 0.07 0.22 0.34 0.75 0.11 0.01 0.25 0.14 0.20 0.18 0.05 0.13 0.09 0.04 0.02 0.16 0.13

10 3 34 19 6 29 29 103 13 2 25 12 21 25 4 19 12 3 3 19 12

0.12 0.04 0.40 0.22 0.07 0.34 0.34 1.21 0.15 0.02 0.29 0.14 0.25 0.29 0.05 0.22 0.14 0.04 0.04 0.22 0.14

83 Solanum nigrum L.

Solanaceae

Kachmachu

Shoot

Tonic, febrifuge and anti-rheumatic

Oral

9

0.11 12

0.14

84 85 86 87

Solanaceae Tamaricaceae Zygophylaceae Scrophulariaceae

Maraghoonra Ghaz Speena Khardag

Seed Bark Shoot Leaf

Anti-diabetic, anti-headache, febrifuge Wound healing Tonic, anti-rheumatic Anti-rheumatic

Oral Paste Oral Oral

17 5 17 6

0.20 0.06 0.20 0.07

0.29 0.06 0.211 0.07

88 Verbena officinalis Linn

Verbenaceae

Shamakay

Shoot

Anti-diarrheal, blood purifier and febrifuge

Oral

24 0.28 31

0.36

89 Vitex negundo L. 90 Withania somnifera (L) Dunal

Verbenaceae Solanaceae

Khamazoora

Ullah et al. (2014) Hussain et al. (2014) Hussain et al. (2014) Hussain et al. (2014) Hussain et al. (2014) Sher and Al Yemeni (2011) Sher and Al Yemeni (2011) Ullah et al. (2014) Ullah et al. (2014) Ullah et al. (2014) Sher and Al Yemeni (2011) Sher and Al Yemeni (2011) Ullah et al. (2014)

Leaf Leaf Seed Shoot Leaf Gum Seed Leaf, fruit, seed Bark Shoot Fruit Leaf Seed Leaf Fruit, shoot Fruit Shoot Shoot Shoot Shoot Leaf, flower

Leaf Seed

Oral Oral

4 0.04 9 11 0.13 16

0.11 0.19

Baira Baira

Ullah et al. (2014) Ullah et al. (2014)

Anti-allergic, antidote, chest pain alleviation Aphrodisiac, wound healing, maintenance of body temperature Anti-diabetic Anti-diabetic

Oral Oral

30 0.35 30 4 0.04 4

0.35 0.04

46 47 48 49 50 51 52

Indigofera heterantha L. Jasminum officinale L. Juglans regia L. Justicia adhatoda Linn. Lotus corniculatus L. Mallotus philippensis (Lam.) Mőll. Melia azedarach Linn

Otostegia limbata (Benth.) Boiss. Oxalis corniculata L. Peganum harmala L. Paeonia emodi Wall. ex Royle Periploca aphylla Dcne. Pinus roxburghii Sarg. Plantago lanceolata L. Plantago major L. Platanus orientalis L. Portulaca olearacea L. Punica granatum L. Ranunculus aquatilis L. Ricinus communis L. Robinia pseudocacia L. Rosa webbiana Wall ex Royle Rubus ellipticus Smith. Rubus fruticosus L. Rumex hastatus D. Don Salix babylonica L. Salvia plebeia R. Brown Sarcococca saligna (D. Don) Muell.

Solanum surattense Burm.f. Tamarix aphylla (L) Karst. Tribulus terrestris L. Verbascum thapsus L.

91 Ziziphus mauritiana L. Rhamnaceae 92 Ziziphus nummularia (Burm. f.)Wight et Arn Rhamnaceae

Leaf Fruit, leaf

0.47 0.03 0.31 0.14 0.03 0.22 0.25

25 5 18 6

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Family

No. Name

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Fig. 5. Plant species with highest RFC. Fig. 3. Percentage of parts used in the local area.

Fig. 6. Plant species with highest UV.

Fig. 4. Percentage usage of plants for various ailments by the locals.

(1 species). Gymnosperms were represented by a single family Pinaceae. The vegetation distribution was 51 herbs (55.4%), 20 shrubs (21.7%), and 21 trees (22.8%). The parts of the recorded plants used by the locals are summarized in Fig. 3. Shoots were the most used parts (23.6%) followed by leaves (21.8%), fruits (16.4%), and seeds (7.2%). Apart from that, whole plant, stems, roots, bark, flowers, inflorescence, gum and latex were used for various purposes. As per medicinal uses, the plants were grouped into 12 therapeutic classes as showed in Fig. 4. Results from this survey revealed that 7.91% of the plants were used for wound healing. Responses revealed that plant leaves are generally applied as poultice on stings, bruises and lesions. Other studies have also reported similar uses of plants for nursing injuries (Rajaei and Mohamadi, 2012). Febrifuge (7.34%), aphrodisiac (6.21%), and stomach cure (5.64%) were the next prominent applications. Berberis lycium (barberry sp.) from Berberidaceae, Plantago major (broadleaf plantain) from Plantaginaceae, Mirabilis jalapa (four o'clock flower) from Nyctaginaceae and Fagonia critica (Virgin's mantle) from Zygophyllace family were the most cited plants by the locals with RFC values of 0.92, 0.75, 0.72, and 0.61, respectively (Fig. 5). Shown in Fig. 6 are the plants with highest UV. P. major, Ajuga bracteosa from Lamiaceae, M. jalapa, Hyosymus niger (henbane) from Solanaceae and Adiatum venustum from Adiantaceae family had the UV 1.21, 1.03, 0.95, 0.94 and 0.94, respectively.

3.2. Statistical analysis showing relationship of RFC and UV Pearson correlation coefficient r was calculated to be 0.8682. This is a strong positive correlation, which means that high x variable scores correlate with high y variable scores. The value of r2, the coefficient of determination was 0.7538 (Fig. 7). The robust

correlation implies that RFC and UV share a linear relation across species (Bano et al., 2014). 3.3. Interpretation of the results and literature validation From the data analysis, it came forth that one species could be used for a multitude of ailments. A similar study conducted in Fars Province of Iran also convey the versatile uses of medicinal plants (Dolatkhahi et al., 2014). The therapeutic spectrum of the documented flora was vast. As per interviewee response they were used as antiseptic, tonic, aphrodisiacs (any food or potion, capable of elevating sexual desire, potency and pleasure.), blood purifier, carminative (any supplement preventing flatulence), sedative, cooling agent, diuretics and laxative. For easing inflammation, wounds, stomach disorder, diarrhea, constipation, headache, backache, tooth cavities, cough, asthma, worms, jaundice, boils, eczema, bleeding, snake venom, menstrual pain, liver and kidney problems, the plant concoctions were used. A. bracteosa (bugleweed) was the most reported species locally used for curing six types of health problems. It was used as blood purifier, carminative, anti-cough, anti-asthma, anti-jaundice and as a cooling agent. The literature survey revealed the antiplasmodial (Chandel and Bagai, 2010) effect of leaf extract and antiinflammatory (Gautam et al., 2011), cytotoxicity (Pal et al., 2014), immune-stimulatory (Nisar et al., 2014), and anti-arthritic (Kaithwas et al., 2012) effect of the whole plant. Acacia nilotica (gum Arabic tree) from Fabaceae family was reported for five therapeutic uses such as wound healing, anti-headache, cough treatment, tonic, and as anti-toothache agent. The literature browsing revealed the anti-fertility (Lampiao, 2013) and antiulcer (Bansal and Goel, 2012) effect of pods; anticancer Meena et al., 2006, hypoglycaemic and anti-platelet aggregation Asad et al., 2011 of leaves, and anti-diarrheal effect of bark (Misar et al., 2007). Acacia modesta, growing abundant in Pakistan, was reported to heal backache and wound, while showing usefulness as aphrodisiac and tonic. Validation of its anti-inflammatory, analgesic and

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Fig. 7. Relationship between RFC and UV (respondents interviewed¼ 85).

anti-platelet (Bukhari et al., 2010) activities exist. Research evidence of aphrodisiac does not exist, but many literature review have discussed the usage of Acacia products as an aid to treat impotence and erectile dysfunction-related problems in various geographical regions, mostly in Africa (Auwal et al., 2014; Kamatenesi-Mugisha and Oryem-Origa, 2005). Artemisia scoparia (redstem wormwood) from Asteraceae family was reported to have four applications such as febrifuge, cure for kidney, liver ailment alleviation and blood purifier. Anti-nociceptive, antiinflammatory and antipyretic (Habib and Waheed, 2013) effect, amelioration of obesity-related insulin resistance (Yahagi et al., 2014) and attenuation of non-alcoholic fatty liver disease (Wang et al., 2013) by this plant has been scientifically verified. Melia azedarach (Chinaberry tree) from Meliaceae was reported to act as carminative, treatment for gastric problems, children fever, and cough. Validations for antibacterial of seed (Khan et al., 2011a, 2011b), antiviral (Petrera and Coto, 2009) effect of leaves; antifungal (Jabeen et al., 2011), dermatoprotective (Saleem et al., 2008) effect of flowers use exist in literature. Solanum surattense (Yellowfruit nightshade) from Solanaceae family was reported to have anti-diabetic, anti-headache and febrifuge properties. Empirical studies have authenticated the antioxidant effect of leaves (Muruhan et al., 2013) and cytotoxicity of aerial parts (Lu et al., 2011). Most of the plants were reported to have three applications whereas some plants were stated to have two or a single use (Table 2). It was observed that 7.91% of the plants were used for wound healing and that A. modesta, A. nilotica, and B. lycium were the mostfrequently used species for this purpose, whereas M. jalapa, Tamarix aphylla from Tamaricaceae, and Withania somnifera (Indian ginseng) from Solanaceae family were seldom used species. The lesion amelioration potency of A. nilotica (Kannan et al., 2013), B. lycium (Asif et al., 2007) and M. jalapa (Gogoi et al., 2013) was documented in the literature. About 7.34% of the total documented species, including A. bracteosa, A. scoparia, and Solanum nigrum were used as antipyretic. Therapeutic validations were obtained for A. scoparia aerial part (Habib and Waheed, 2013) and S. nigrum leaf (Zakaria et al., 2009) extracts. This survey revealed that 6.21% of the recorded plants were used as aphrodisiacs (Malviya et al., 2011). Adiantum venustum (Himalayan maidenhair) from Pteridaceae, Lotus corniculatus (Bird's-foot-trefoil) from Fabaceae and Tribulus terrestris (puncture vine) from Zygophyllaceae were considered effective cure for male erectile dysfunction and impotency. The relevance of T. terrestris in treatment of sexual disorder in both males (Do et al., 2013; Singh et al., 2012) and females (Akhtari et al., 2014; Gama et al., 2014) is well-substantiated. B. lycium was ingested to treat uterine and vaginal infections. About 5.64% of the plants such as Calotropis procera (apple of Sodom) from Apocynaceae, Mentha longifolia

(peppermint), and Rumex hastatus (arrowleaf dock) from Polygonaceae family were used for the treatment of stomach and digestive disorders. Stem bark extract of C. procera demonstrated antiinflammatory and gastroprotective effect (Tour and Talele, 2011). Digestive role of M. longifolia has been reviewed (Mikaili et al., 2013). Alleviation of gastro-intestinal ailments by R. hastatus has been reported by another ethnobotanical study conducted in Nepal (Rokaya et al., 2010). Though no empirical study exists so far to validate the gastro-protective mechanism of R. hastatus, an in vivo study demonstrates the hepatic and testicular protection offered by its methanolic extract (Sahreen et al., 2013). Antioxidant enhancement was implicated as the therapeutic mechanism. It can be inferred that gastric mucosa benefits from the R. hastatus-bolstered antioxidant level. Apart from usage as herbal medications, the local dwellers depend on the flora for their sustenance. Various plant parts were consumed raw, dried, cooked or pickled. Asphodelus tenuifolius (a weed) from Liliaceae, Bauhinia variegata (orchid tree) from Fabaceae, Caralluma fimbriata (a succulent) from Apocyanaceae, Chenopodium botrys (Jerusalem Oak Goosefoot) from Amaranthaceae, Malva neglecta (common mallow) from Malvaceae, and Nasturtium officinale (watercress) from Brassicaceae were the most valued vegetables. A. tenuifolius is ubiquitous plant of Unani medication system. It is considered edible, regarded to possess oxidative DNA damage preventive and diuretic activity (Kalim et al., 2010). B. variegata constitutes a major wild food plant among different communities (Ghorbani et al., 2012). Its antioxidant, anticancer, antibacterial (Mishra et al., 2013) and anti-diabetic (Patel et al., 2012) properties have been validated. C. fimbriata is an edible cactus, widely consumed in different cultures. A clinical trial showed that it has the capability to suppress hunger and improve endurance (Kuriyan et al., 2007). Further, its anti-obesity and anti-lipemic properties have been validated (Kamalakkannan et al., 2010). In vitro anti-hyperglycemic activity of a related species Caralluma umbellata has also been reported (Bellamakondi et al., 2014). These metabolic syndrome management properties raise its market prospects. C. botrys essential oil extracted by hydrodistillation of its aerial parts, exhibited significant bactericidal and fungicidal activity against pathogens (Maksimović et al., 2005). Though the literature on its nutritional importance is scanty, its related species Chenopodium quinoa Willd. (quinoa) is garnering immense popularity as nutrient-laden functional food. This pseudocereal has consolidated its position in nutraceutical sector with an abundance of minerals, vitamins, antioxidants, fatty acids, phytohormones (Abugoch James, 2009; Vega-Gálvez et al., 2010). Therefore, C. botrys is expected to possess physiologically-relevant compounds. M. neglecta is traditionally used as a therapeutic against cough, respiratory and digestive disorders. Rich in mucilage, malvin, tanen and glucose, it has been verified to exert antioxidant and anti-ulcerogenic properties (Güder and Korkmaz, 2012). N. officinale (watercress) is well-known as a wild vegetable (Abbasi et al., 2013b). Its antioxidant activity has been validated (Ozen, 2009). B. lycium, Daphne oleoides from Thymelaeaceae, Ficus carica (common fig) from Moraceae, Ficus racemosa (cluster fig) from Moraceae, Fragaria indica (wild strawberry) from Rosaceae, Punica granatum (pomegranate) from Lythraceae, Juglans regia (Percian walnut) from Juglandaceae, Monotheca buxifolia from Sapotaceae, Morus alba (white mulberry) from Moraceae, Morus nigra (black mulberry) from Moraceae, Olea ferruginea (Indian oilve) from Oleaceae, and Ziziphus mauritiana (Chinese apple or jujube) from Rhamnaceae family, were the frequently-used fruit plants. Most of the above fruits are commercially-important such as fig, pomegranate, mulberry and jujube. The less popular fruits are also

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nutrition-rich and palatable, yet languishing in obscurity due to their local production, perishability and lack of awareness. A study on fruit consumption pattern of tribal inhabitants of Lesser Himalayas-Pakistan showed the utilization of M. alba, F. carica, O. ferruginea, B. lycium, and Z. mauritiana (Abbasi et al., 2013a). In vitro assay of the J. regia fruit extract revealed its antioxidant and anti-proliferative activity (Negi et al., 2011). O. ferruginea Royle fruit-derived oil was analyzed to be rich in monounsaturated oleic acid (61–67%). Potential of its fruits for olive oil extraction came forth (Joshi, 2012). The above cited literature reports reinforce the nutritional importance of vegetation in Malakand Pass Hills. Apart from the ethnobotanical salience of the flora of the study site, the interview sheds light on other crucial aspects as well. The vegetation was found to be vulnerable to overgrazing, deforestation, urbanization, and unsustainable harvesting (Mahmood et al., 2013). The inhabitants were socio-economically unprivileged and very much dependent on the forest resources for fuel woods, timber, furniture, fodder etc. It was leading to reckless consumption of the botanicals resources. Related ethnobotanical studies carried out in near-by areas have also reported the constraints put on the flora (Murad et al., 2013). Dodonaea viscosa (hopbush) from Sapindaceae and Pinus roxburghii (chir pine) from Pinaceae family were the most-preferred species as fuel. It is deplorable as D. viscosa has been validated to possess antimicrobial, antiprotozoal and hepatoprotective property (Ali et al., 2014; Muhammad et al., 2012; Naidoo et al., 2012); whereas P. roxburghii is recognized to treat skin, eye, ear and throat problems (Kaushik et al., 2013). Other medicinally-pertinent plants cut indiscreetly include A. modesta, B. variegata, Dalbergia sissoo, M. azedarach, and Zizyphus mauritiana. It has been documented that the impoverished inhabitants fell the trees to supply fuel to the brick kilns in Pakistan (Tahir et al., 2010). A similar study conducted on the flora of Soan Valley, Salt Range, Pakistan have voiced the same concern about the depleting number of the above trees (Bibi et al., 2014a, 2014b). The rampant deforestation must be restrained by persuading the local short-sighted communities. Legislations should be should be put into effect to protect the unique, medicinallyvaluable vegetation of Malakand Pass Hills.

3.4. Quantitative ethnomedicinal uses Quantitative value indices were calculated to analyze the ethnomedicinal information. Fig.5 shows the 12 plant species with highest RFC and Fig. 6 shows the 13 plant species with highest UV, as reported by the informants. RFC and UV obtained in this survey are statistical indicators of the ethnobotanical knowledge of the local people. These recorded values of RFC and UV were found to be higher for some important medicinal species, which could be attributed to the trend of utilization of herbal drugs in the valley. RFC values ranged from 1–92%. The former is associated with Portulaca oleracea from the family Portulaceae whereas the latter is associated with B. lycium from family Berberidaceae. However, on the average, their frequency citation (FC) is 15.04%. Likewise, the UV of medicinal plants range from 0.05 to 1.21 which showed the least relative importance of Alnus nitida (Himalayan alder) from the family Betulaceae and the highest importance for P. major (broadleaf plantain) from family Plantaginaceae. These findings are consistent with those obtained from RFC. Strong positive correlation between RFC and UV as determined by Pearson correlation coefficient implied that their patterns match, across species. The degree to which RFC and UV vary was measured numerically by r2. The finding implied the empirical robustness among these two indices (Table 2). This is also supported by the shape of the scattered plot reflecting a strong positive relationship between RFC and UV values (Fig. 7). The quantitative calculations

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contributed to the novelty of the results compared with those obtained from other similar studies. This study illuminated on multiple aspects of the flora of Malkand Pass Hills, the composition, the folkloric uses, the dominant species and the status of the exploited plants. Pharmacological validations of the findings were conducted by the literature survey which revealed that most of the traditional and ethnobotanical information gathered are supported by empirical verifications. However, plenty of novel uses were revealed. This amassed traditional knowledge can be put to validation for screening potential drug leads. From another perspective, the vulnerability of the vegetation came forth. The mounting human pressure and resultant hostile effects on the indigenous botanical resources was visible. As delineated by another study, the unregulated commercial exploitation of these plants might threaten or wipe out important plant species and cause conflicts among concerned people (Ghorbani et al., 2012). The degradation must be halted and the perturbed forests must be allowed to regenerate (Adnan and Hölscher, 2011). This study generated a wealth of information worthy of guiding future course of action.

3.4.1. Limitations of the study, insights gained and approaches for improvement The study design fulfilled most of the objectives in ethnobotanical data collection and analysis; however, it had some bottlenecks too. The vernacular names of some of the plants could not be gathered, as often, multiple plants go by same name. Also, the opposite holds true when the same plant goes by multiple vernacular names (Powell et al., 2014). Consequently, some reported names could not be verified with reliable references. Analysis of the informant report revealed that some of the reported medicinal uses could not be verified with existing literature. On the contrary, experimentally-tested medicinal plants were not necessarily used for treatment of same health disorders by the informants. It implied that usage of plant can vary depending on culture, region, prevalent ailment, and availability of alternative plants with similar therapeutic effects. This discordant finding can be explained by the fact that the medicinal usage of the plants were instinctive and adopted by experience (Petrovska, 2012). The questionnaire did not include any queries on possible illegal export of medicinal plants, which could have reflected on sustainability threat of the indigenous flora. As similar study has reported that Pakistan exported plant parts over US$10.5 million in 2012, with a substantial supply procured from adjoining regions (Sher et al., 2014). Another impediment of the investigation was that it did not probe into the menace of invasive species. Deleterious impact of alien species on resident communities has been well-documented (Hejda et al., 2009). Identification and distribution of the introduced species would have been purposeful. This facet could be pursued in future work. Risk assessment of the reported plants is beyond the scope of this quantitative study, yet the study would be incomplete without the discussion of risks and corrective measures. Despite the litany of health benefits, plants contain many harmful compounds that may lead to morbidity to mortality when consumed in unsupervised manner. Phytoestrogens are vilified as endocrine disruptors (Patisaul and Jefferson, 2010), aconites are cardiotoxins and neurotoxins (Chan, 2009), colchicine causes gastric cramp (Eddleston and Persson, 2003), ricin causes visceral damage (Al-Tamimi and Hegazi, 2008) etc. Hepatotoxicity continues to be a major challenge caused by herbal drug intake. A case study reports the severe liver injury resultant of high dose senna fruits consumption in the form of herbal tea (Vanderperren et al., 2005). Kava (Piper methysticum)

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taken as anxiyolytic agent has been shown to cause liver lesions and malfunction (Teschke and Wolff, 2011). Increasing numbers of studies are reporting the heavy metal and pesticide traces in herbal products. Urinary concentration of lead, arsenic, mercury, chromium cadmium is another concern regarding the unsupervised usage of the plant products (Harris et al., 2011). Adulteration of herbal products with prescription drugs is a prevalent malpractice, thought strictly banned by Food and Drugs Administration (FDA). The consequences of interactions between herbal product and drugs have been studies extensively. The adverse reactions can range from hormonal imbalance to allergy (Girard and Vohra, 2011). Also, the instances of pathogenic (Salmonella typhi, Shigella spp., Escherichia coli and Staphylococcus aureus) (Abba et al., 2008) and mycotoxin (aflatoxin, ochratoxin, zearalenone) (Efuntoye, 1999) contamination of the herbal product has been witnessed. Even the ancient and most popular herbal pharmacopeia, Traditional Chinese Medicine (TCM) and Ayurveda have been unveiled to pose myriad health hazards (Patwardhan et al., 2005). The above evidences sums up the health risks associated with chronic abuse of herbal supplements. So, caution should be taken while taking or administering them and future strategies should focus on safety studies of the herbal drugs. Awareness must be created among the concerned population. As they are mostly socio-economically challenged and deprived of access to scientific information, they should be educated. Publicizing the inherent risks of the herbal products appears to be a robust step towards alerting the concerned group. Based on works done in this area and successes achieved, some control measures have been proposed. Quality standardizations is of paramount importance for dietary supplements, the materialization of which relies on manufacturers and regulatory agencies (Teschke et al., 2013). Strict surveillance must be implemented to minimize quality breaches as batch variability, impurities, adulterants and herb misidentifications (Teschke et al., 2013). Training of traditional herbalists on the cardinal rules of Good Manufacturing Practices (GMF) will lower chances of quality deterioration (Temu-Justin et al., 1998). Reports from across the globe have highlighted the importance of statutory regulation in quality assurance of herbal preparations and improvement of the standards of practice (Abba et al., 2008; Brink, 2009). Legitimate integration of the herbal and other traditional forms of therapeutics in health care system is suggested (Zhang et al., 2011). Close supervision is needed to ensure that herbal product retailers and practitioners are adhering to the ethics and regulations. Financial exploitation of the local people in the name of standardized drugs is going to crumble the regulatory system. Government oversight and active pharmaco-vigilance is required to protect the health unsuspecting consumers from the perils of herbal drugs (Genuis et al., 2012). On the contrary, the folkloric usage of the medicinal plants is passed down from generation to generation, so they are assumed to be generally safe. Accumulation of the fast-eroding traditional knowledge, utilization for effective drug discovery and stimulating preservation of the flora is the cardinal goal of this investigation. Conflict of interest The authors declare no conflict of interest in submission of this manuscript. Authors' contributions Muhammad Ibrar supervised this work, guided the final writeup and checked the manuscript. Abdur Rauf supervised the

ethnobotanical survey and participated in the collection of data. Taibi Ben Hadda and Mohammad S Mubarak assisted in editing the manuscript and provided technical expertise in compiling data into the draft. In addition, Taibi Ben Hadda undertook the quantitative data analysis and other technical issues pertaining to the manuscript. Seema Patel revised and produced the final draft. All authors have read and approved the final manuscript.

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Quantitative ethnobotanical survey of medicinal flora thriving in Malakand Pass Hills, Khyber Pakhtunkhwa, Pakistan.

Ethnobotanical knowledge is proving to be invaluable for drug discovery in the wake of effective prospecting from biodiversity. On the other hand, the...
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