Use of Ethnomedicinal Plants by the People Living in the Middle Atlas Mountains in Morocco

Morocco has a high level of biodiversity and endemism of medicinal plants. However, these plants are threatened by the growing human population and climate change. The loss of medicinal plants will have a potential negative impact on the population who rely heavily on these plants for the treatments of diseases. The objective of the present study was to document ethnomedicinal knowledge use to treat different human ailments from people living in the Middle Atlas Mountains of Morocco. Field work was conducted between March and May of 2017. Data was collected from 320 users through a questionnaire survey. Results of the study indicate that people of the Middle Atlas use 44 plant species mostly herbs (66%) for ethnomedicinal purposes. The highest the Informant Consensus Factor value (0.93) was obtained for gastrointestinal problems followed by respiratory infections (0.92), and neurological problems (0.82), and based on the species Use Value, the five most commonly used ethnomedicinal plants species were Thymus vulgaris, Mentha pulegium, Aloysia citriodora, Rosmarinus officinalis, Lavandula dentata and M. rotundifolia. The present study showed that traditional treatment using medicinal plants in widespread in the study area. Protection measures should be taken to conserve precious multipurpose species that are facing overexploitation. Moreover, medicinal plants treating major ailments in the region may be subjected to phytochemical and pharmacological investigations for the identification of bioactive compounds.


INTRODUCTION
Traditional medicine, as defined by the World Health Organization (WHO), is the knowledge, skills and practices based on the theories, beliefs and experiences indigenous to different cultures, whether explicable or not, used in the maintenance of health, as well as in the prevention, diagnosis, improvement or treatment of physical and mental illnesses [1]. Traditional medical knowledge is seeing increased attention worldwide considering global health acre demand and the significant role of traditional medicine in meeting the public health needs of developing countries. Approximately 80% of the population in developing countries depends on traditional medicine for primary health care needs [2][3][4][5][6]. In addition, the pharmaceutical and biotechnological industries are much interested in using this knowledge for the discovery and development and application for new active products on health and new genes with properties for food improvement.
The flora of Morocco is the second most biological diverse country in the Mediterranean region after Turkey, in terms of species, and the richest in North Africa [7], with about 4200 taxa including 1282 subspecies of which 22% (879 taxa) are endemic [8]. The number of medicinal and aromatic plants (MAP) in Morocco is estimated at about 800 species. The MAP sector plays a very important socio-economic role, with annual revenues generated from MAP export of about 500 million Moroccan Dirhams (about US $56 million) and provides employment to local and rural communities generating an estimated 500.000 work-day per year. However, this diversity is threatened by numerous factors including destruction of natural habitats, cleaning of vegetation for agricultural expansion, and climate change. These factors lead to a serious decline in the number of medicinal plant species available, which in turn lead to a decline in annual revenues generated from the MAP industry and more importantly a loss of traditional medical knowledge associated with these plants.
plants in different parts of Morocco have been documented previously, including the Rif and the High Atlas Mountains [9][10][11][12][13][14][15][16][17][18][19][20][21]. There is only one published report on the use of MAP in the Middle Altas Mountain areas, and it covered only the city Khenifra [22]. The present study aimed at investigating the traditional utilization of MAP by the people living in different areas in the Middle Atlas Mountains of Morocco. The study area is part of the country's richest biodiversity center, presents a particularly high rate of endemism and is a rich source of ethnobotanical knowledge. Specific objectives of the study were: (i) to identify plant species used in the treatment of various diseases, and (ii) to document traditional recipes from medicinal plants including modes of preparation, dosage, mode of administration and potential side effects associated with medicinal plant uses. This study identified the most widely used plants, which can be used as stating plant materials for the identification and development of new and useful medicinal substances.

Study area
In the heart of northern Morocco, between the Rif and the High Atlas, the Middle Atlas is a major component of the Moroccan terrain. It runs about 450 km from the Southwest to the Northeast and covers a total area of 27,550 km 2 , which is 15% of the country's total mountain area. The Middle Atlas is 100 km wide in the North and only 30 km wide in the South.
This study was carried out between the months of March and May of 2017. Eight towns and villages were investigated (Figure 1), they were: Azrou, Boulmane, El Hajeb, Ifrane, Khenifra, Midelt, Mrirt, and Zaouiat-Cheikh, and 320 people participated in this study.

Data collection
A questionnaire was used to collect information from individuals about the MAP they use in the treatment of diseases. The questions focused on local names of the medicinal plants, types of diseases treated, mode and method of remedy preparation, parts of the plants used, use of fresh or dry plants, use of single or a mixture of plants for remedy preparation, mode of administration, dose requirement, and usable duration regarding each medicine, and any side effect of medicinal plant use. Questionnaires also contained information on the sociocultural aspect of the respondents.

Data organization
Data were organized using Microsoft Excel software. The habits of the plants were categorized into three groups, that is, herbaceous, shrubs, and trees. The status of recorded plants was divided into three groups of wild, cultivated, and both wild and cultivated. The parts used by the healers were categorized into 6 groups, that is, fruits, leaves, leaves and stems, seeds, roots, or the whole plant. Human ailments treated by the traditional healers were divided into 7 categories such as gastrointestinal, respiratory, cardiovascular, dermatology, metabolic, neurology, and osteology. Route of administration of plant remedies was classified into three groups such as oral, dermal, and both oral and dermal. Questionnaire data were analyzed for basic categorization of the respondents' gender, age groups, education level, and occupation.

Data analysis
The Informant Consensus Factor (ICF): The informant consensus factor (ICF) was calculated to estimate the user variability of medicinal plants [23,24]. The ICF ranges from 0.00 to 1.00 and it has been used in prioritizing medicinal plants for further scientific validation of plants and plant products [25,26], as pharmacologically effective remedies are expected from plant with higher ICF values [27]. High ICF values are obtained when only one or a few plant species are reported to be used by a high proportion of informants to treat an ailment, whereas low ICF values indicate that informants disagree over which plant to use [23]. High ICF values can thus be used to identify particularly interesting species for the search of bioactive compounds [24]. ICF is calculated using the following formula: Bouiamrine et al. [29] who reported that Lamiaceace, Apiaceae, and Asteraceae are widely used as MAP in the Middle Atlas Mountains, although their use in treatment of specific major aliments was not indicated. The use of members of the above families in herbal medicine is known the city of Khenifra [22], and in other parts of Morocco [10][11][12][13][14][15][17][18]20], indicating their importance in medicinal applications. In fact, several plants species belonging to Lamiaceae, Apiaceae, and Asteraceae are known for their antimicrobial, antibacterial, anti-inflammatory, and antioxidant activities [30,31].
Moreover, the residents mostly use herbs (66%) for their remedies (Table 2), which are widely distributed in the Middle Atlas Mountains and can easily be harvested [29]. Of the 44 species, 66% were wild while 27% were cultivated. This study thus highlights the dependence of traditional healers on the Middle Atlas Mountains in obtaining their ethnomedicines from the natural environment.
Different parts of medicinal plants are used by the respondents in the treatment of illnesses. Leaves and stems (43%) or leaves only (27%) are the most frequently used plant parts for the treatment of diseases, due to their richness in bioactive compounds compared to other plant parts. Seven disease categories were identified in this investigation. Most respondents have indicated that they take herbal medicines orally using decoction or infusion.
The highest ICF values were obtained for gastrointestinal (ICF=0.93) and respiratory diseases (ICF=0.92), followed by cardiovascular (ICF=0.9), neurological (ICF=0.82) and metabolic problems (ICF=0.8) ( Table 2). Boiled water is commonly believed to serve as a vehicle to transport the remedies. Boiling both helps extract the active components from plants, but also helps eliminate impurities. In general, decoction and infusion are the most common methods used to prepare the plant material, which is used fresh or dried (Table 3).

Medicinal plants for gastrointestinal diseases
The most reported plant species uses for gastrointestinal diseases include Thymus vulgaris (126 times ), Rosmarinus officinalis (44 times), Aloysia citriodora (40 times), Mentha rotundifolia (30 times), Lavandula dentata (20 times), Artemisia absinthium (18 times), T. zygis (18 times) and Salvia officinalis (16 times). These results support the previous finding of El Midaoui et al. [22] who reported the use of these plants in the treatment of gastrointestinal diseases in the city of Khenifra, which in situated in the Middle Atlas Mountains. These plant species are also used to treat gastrointestinal diseases in other parts of Morocco including the city of Kenitra [12], Settat [13], the North East [14], the High Atlas [15], Agadir [17], and the Moroccan central plateau [32].

Medicinal plants for respiratory diseases
People living in the Middle Atlas use four main plants species to treat respiratory diseases; M. pulegium (100 times), T. vulgaris (31 times), R. officinalis (22 times) and L. dentata (16 times). El-Midaoui et al. [22] reported the use of M. pulegium and T. vulgaris by people living in the city of Khenifra to treat indigestion and respiratory infections, respectively. These plant species are used to treat respiratory diseases by people living in other parts of Morocco [12][13][14][15]17,20].
Where "Nur" refers to the total number of use reports for each disease cluster and "Nt" refers to the total number of species used for that cluster.

The Use Value (UV):
The Use Value (UV) was calculated according to Phillips et al. [28] using the following formula: Where "∑ " refers to the number of uses mentioned by the informants for a given species and "N" refers to the total number of informants interviewed. If a pant secures a high UV score, that indicates that there are many use reports for that plant, while a low score indicates fewer use reports cited by the respondents.

RESULTS AND DISCUSSION
Among the 320 respondents, 184 (57.5%) were male and 136 (42.5%) were female. The largest proportion of the respondents (25%) was quadragenarian (40-49 years old) ( Table 1). Most of the respondents were illiterate (34%) followed by those who received primary education (25.6%). Most of the respondents are jobless (46%), followed by students (12.8%) and salesperson (11.8%) ( Table 1). There was no correlation between the age of the respondent and the number of medicinal plants known.

Medicinal plants for cardiovascular diseases
Aloysia citriodora (10 times) and S. officinalis (2 times) are the only plant species used by the people of the Middle Atlas to treat cardiovascular diseases. It has been reported that S. officinalis is used by the people of the High Atlas and Izarene region to treat hypertension [12,20,33], and by the people of the Rif Mountains to treat anemia [34].

Medicinal plants for dermatological diseases
The most reported plants for dermatology use include L. dentata (6 times), Allium sativum (5 times), and Olea europea (4 times).
Previous ethnobotanical studies conducted in other parts of Morocco have reported the use of these plants for dermatological uses [9,15,20]. Allium sativum and O. europea are used by the people living in the Tafilalt region to treat cutaneous leishmaniasis [35] and in the province of Tan-Tan to treat renal lithiasis [36].

Medicinal plants for metabolic diseases
The most reported pants for metabolic are Trigonella foenum graecum (21 times), followed by Chenopodium ambrosioides (4 times) and Petroselinum sativum (4 times). Previous studies have reported the use of T. foenum graecum and C. ambrosioides to cure metabolic diseases in the city of Khenifra [22] and in other areas of Morocco [12,18,20,32]. Specifically, P. sativum is used by the people of Tan-Tan province in Morocco to treat kidney stones [36].  Many medicinal activities of these plants can be attributed to their essential oils. Previous studies on the chemical composition of essential oils from these medicinal plants in Morocco have indicated that Thymol is the major constituent of essential oil from T. vulgaris [37]. Menthol and Piperitone are the major constituents of M. rotundifolia, and M. pulegium essential oils, respectively [38]. Rosmarinus officinalis essential oil is rich in 1,8-Cineole, alph-Pinene and Camphor [39]. 1,8-Cineol is also the major constituent of L. dentata essential oil [40].

CONCLUSION
The present study showed that the use of MAP for treatment purposes is prevalent in the study areas, which underlines the importance in