Ethnopharmacological survey of medicinal plants used in Daraa-Tafilalet region (Province of Errachidia), Morocco

Ethnopharmacological survey of medicinal plants used in Daraa-Tafilalet region (Province of Errachidia), Morocco

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Author’s Accepted Manuscript Ethnopharmacological survey of medicinal plants used in Daraa-Tafilalet region (Province of Errachidia), Morocco Mohamed Eddouks, Mohammed Ajebli, Morad Hebi www.elsevier.com/locate/jep

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S0378-8741(16)32341-8 http://dx.doi.org/10.1016/j.jep.2016.12.017 JEP10613

To appear in: Journal of Ethnopharmacology Received date: 13 May 2016 Revised date: 28 November 2016 Accepted date: 10 December 2016 Cite this article as: Mohamed Eddouks, Mohammed Ajebli and Morad Hebi, Ethnopharmacological survey of medicinal plants used in Daraa-Tafilalet region (Province of Errachidia), Morocco, Journal of Ethnopharmacology, http://dx.doi.org/10.1016/j.jep.2016.12.017 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Ethnopharmacological survey of medicinal plants used in Daraa-Tafilalet region (Province of Errachidia), Morocco Mohamed Eddouks1*, Mohammed Ajebli1, Morad Hebi1

Faculty of Sciences and Tecniques Errachidia, Moulay Ismail University, BP 509, Boutalamine, Errachidia, 52000, Morocco.

* Corresponding author at: Faculty of Sciences and Tecniques Errachidia, Moulay Ismail University, BP 509, Boutalamine, Errachidia, 52000, Morocco. Phone: +212 35 57 44 97; Fax: +212 35 57 44 85. ; E-mail: [email protected] E-mail addresses: [email protected] (M.Eddouks). [email protected] (M. Ajebli) [email protected] (M. Hebi)

Abstract Ethnopharmacological relevance: we carried out an ethnobotanical survey in Tafilalet region. This region is classified by the UNESCO as a reserve of biosphere and represents an important area with important knowledge of traditional medicine, especially the use of

medicinal plants for human healthcare. Furthermore, the geographic location of this region makes this site a diverse and interesting resource of herbal biodiversity. The aim of the study: the study aimed to collect information about medicinal plants used in Tafilalet region as well as the indigenous knowledge related to the use of this natural resource in healthcare by the local population in order to preserve and protect this invaluable inheritance from loss and overlook. We aimed also to compare taxa used by the indigenous people of Tafilalet for health-care purposes in comparison with other regions of Morocco as well as neighboring countries. Material and methods: the total of informants interviewed in this study was 1616 (1500 were local inhabitants and 116 were herbalists). This inquiry was carried out through semistructured and unstructured interviews and the sampling technique used was the stratified sample (9 stratums). Data obtained were analyzed calculating 6 indices: Use Value (UV), Family Use Value (FUV), Fidelity Level (FL), Rank Order Priority (ROP), Informant Consensus Factor (Fic) and Jaccard similarity Index (JI). Results: 194 species belonging to 69 families were inventoried in this survey and 17 species were cited for the first time in an ethnobotanical survey in Morocco. The highest value of UV was obtained for Rosmarinus officinalis L. (UV=0.24) and Liliaceae was the family frequently used by inhabitants of Tafilalet (FUV=0.106). In addition, the highest value of FL was recorded for Cistus salviifolius L. and Daphne gnidium L. with FL value of 100% for both species and Origanium vulgare L. had the highest ROP with a value of 53% while the highest value of FIC was mentioned for digestive system disorders (FIC=0.29). Concerning the level of similarity between our study and other regions of Morocco, the province of Tata seems to be the most similar to Tafilalet (JI=42.97), while M’sila (Algeria) was the most similar to Tafilalet among areas in neighboring countries (JI=13.00). Conclusion: despite the richness which characterizes Tafilalet regarding diversity and effectiveness of medicinal plants as well as the largest culture and knowledge related to the

popular phytotherapy among local people in this region, several procedures must be realized to protect and to valorize this interesting inheritance.

Keywords: Ethnobotanical survey, Tafilalet, Medicinal plants, Rank Order Priority, Informant Consensus Factor, Jaccard similarity Index.

1. Introduction Modern medicine has seen during the last century an enormous progress. However, for various reasons, traditional medicine involving medicinal plants is still taking a very important position in the life of many people around the world. Actually, more than 25000 plants are used in the pharmacopoeia and more than 50 % of pharmaceutical products available on the market are of natural origin (Hamilton, 2003). Africa is known by its rich biological and cultural diversity marked by regional differences in healing practices. This continent is estimated to contain between 40 and 45,000 species of plant with a potential for development and out of which 5,000 species are used medicinally. African traditional medicine is considered as a very old therapeutic system (Mahomoodally, 2013). The most common African traditional medicine is the use of medicinal plants considered as the most easily accessible health resource. In addition, herbal therapy seems to be the preferred option for prevention and treatment of various pathologies because of the inadequate access to medical service providers and modern treatments in addition to the exorbitant cost most conventional pharmaceuticals (Gurib-Fakim, 2006). In the North of Africa, it is evident from the literature that there is currently a renewed interest in plant-based medicines in the prevention and cure of various pathologies and many studies have demonstrated that medicinal plants still play an important role in healthcare system in this region (Ramdane et al., 2015; Chermat & Gharzouli, 2015; Boudjelal et al., 2013 ; Ziyyat et al.,

1997; Jouad et al., 2001; Eddouks et al., 2002; Tahraoui et al., 2007). In this region, the

Mediterranean climate offers a rich biodiversity which has been exploited from ancient times in traditional medicine and the traditional medical system is characterized by variation and shaped by the ecological diversities, socio-cultural background of the people as well as historical developments related to migration, introduction of foreign cultures and religion throughout history. The heterogeneous ecologic conditions of Morocco have favored the proliferation of more than 42,000 species of plants, divided into 150 families and 940 genera (Hmamouchi, 1999), spread out the entire country with an area of 715,000 km2. Moroccan people have a rich and ancient tradition in the field of phytotherapy (Bellakhdar, 1997). There are numerous medicinal plants described for treatment of many diseases and herbal medicine is an integral part of Moroccan culture playing an important role in medicine, in food preparation and composition of perfumes. Ethnopharmacologic surveys conducted in Morocco revealed that up to 80% of the population uses at least temporarily the herbal medicine for healing (Fakchich & Elachouri, 2014., Ziyyat et al., 1997; Jouad et al., 2001; Rhattas et al., 2016; Eddouks et al., 2002; Salhi et al., 2010). Many studies reported that women

used phytotherapy more than men, while the educational level is tightly correlated with the use of medicinal. In addition, the most cited reasons of the use of medicinal plants are the availability of medicinal plants, their low cost and the lack of side-effects when compared to conventional therapy (Ziyyat et al., 1997; Eddouks et al., 2002; Jouad et al., 2001). Tafilalet is an important part of Daraa-Tafilalet region which is one among twelve regions of Morocco characterized by various geographic profiles including oasis, Sahara and Atlas Mountains. This region is classified by the UNESCO as a reserve of biosphere. In Tafilalet, the population consists particularly of a mixture of many ethnic groups such as Arabs and Berbers (Amazighs). The historical importance of this region as a platform of cultural and economic exchange between the sub-saharian countries from Africa in one hand and North Africa, Europe and Asia on the other hand represents a crucial factor in the cultural

richness of this site. Tafilalet is the most important oasis of the Moroccan part of the Sahara desert; it is also considered one of the largest oases in the world. The inhabitants of the oasis and region occupy fortified villages (Qsars). In Tafilalet region, the famous historical town of Sijilmassa was founded in 757. It was on the direct caravan route from the Niger to Tangier, and attained a considerable degree of prosperity. Vascular flora of the areas of the southeast of Morocco (Tafilalet) is very surprising by its richness and the diversity of its origin (Ozenda, 1991; Bellakhdar, 1992). The number of species arises to approximately 500 and a big number is common or endemic at the semi-arid and Saharan areas (Ozenda, 1983). The indigenous sources of medical knowledge are disappearing and there is a substantial inter-generational loss of traditional medical knowledge, particularly concerning the oral traditions of the world (Posey, 2000). In addition, the documentation of traditional knowledge plays a key role in bioprospecting of novel drugs from the medicinal plants and in situ conservation of medicinally valuable plants (Parimelazhagan, 2016). Thus, the purpose of this study was to elicit ethnopharmacological information about the medicinal plants used by the local population of Tafilalet in order to preserve this invaluable inheritance. We aimed also to compare local ethnomedicinal data between our area of study and other areas of Morocco as well as neighboring countries via the technique of Jaccard Similarity Index. 2. Subjects and methods 2.1. Study area This ethnobotanical survey was carried out in Tafilalet region (Errachidia province) located at the southeastern Morocco between the latitudes 29°30' and 32°30' with a surface of 60 000 km2. Established in 1956, this province is limited at the north by the province of Midelt, in the northeast by the province of Figuig, in the South and southeast by Algeria and in the west by the two provinces of Zagora and Tinghir (Figure 1). According to the latest census (2014), the number of population in this province is 418 451 inhabitants, including

more than 224 317 in rural areas. The climate is semi-arid and rainfall is generally less to 100 mm/year while temperature oscillates between 8 °C (December-January) and 31.5 °C (July-August). 2.2. Ethnobotanical survey Ethnobotanical data were collected from 1616 informants who were 18 years and older from nine different areas or stratums of Tafilalet (Errachidia, Jorf, Rissani, Tinghir, Goulmima, Rich, Tinjdad, Aoufous and Arfoud). 116 herbalists called “Achaba” in local dialect were questioned through semi-structured and structured interviews (Table 1). Thus, the herbalists were introduced in this investigation in order to guarantee the authenticity of information obtained from the population (i.e. as key respondents). The ethnobotany of medicinal plants used in Tafilalet areas has been investigated through two separate studies: one in 2013-2014 interviewing 649 persons and another in 2015-2016 performed in the same areas interviewing 967 persons, but we have ensured that the villages, oasis and Qsours that were visited in the first enquiry (2013-2014) should not be visited in the last one (2015-2016). The interviews have been realized by graduated students and the questionnaires were translated into national language. The technique sampling used in this study was the “stratified sample”. This sampling has the main advantage of ensuring representativeness regarding the characteristics of the population (Gil, 1999). The sample size (N=1616) has been selected as being representative of the population. The sample must be composed of a sufficient number of cases. The number of cases depends also on the four essential following factors: the size of the sampling population, the established level of confidence, the maximum allowable error, and the percentage in which the phenomenon occurs (Gil, 1999). To record information obtained from interviewees, an uncomplicated questionnaire that gathered the following data has been elaborated:

·

Socio-demographic data: §

Age, gender, familial situation, cultural and educational level, income and economic situation.

·

Botanical data: §

Vernacular name of the used plants (Arab and/or Berber), their origin (local or imported) and their nature (cultivated or spontaneous).

§

Part used of the plants, their form of use and their mode of preparation.

§

Therapeutic and traditional uses of the plants.

§

Data about toxicity of the plant.

Specimens were collected and scientifically identified and a voucher specimen was deposited at Faculty of Sciences and Techniques Errachidia (Fennane et al., 1999; Fennane and Ibn Tattou, 2005; Hmamouchi, 1999). The scientific names of all the plants were checked on the website (www.theplantlist.org). Ethical approval and consent written permission was obtained from the local authority of health. The project was approved at national level by CNRST under number PPR/2015/35. Oral and signed consent was obtained from the study participants. In this study, the national rights on biodiversity of Morocco were followed.

2.3. Data analysis tools Medicinal plants cited in this study used were organized in a table according to an alphabetic order by family and the following data are listed: Family, scientific name, local name, English name, part used, preparation used, origin of the plant, frequency of use, therapeutic use and Use Value (UV). For better interpret the results of our ethnobotanical survey, we adopted these following specific quantitative techniques to analyze data:

Use value (UV): this technique is used to show the relative importance of each plant species known locally to be used as herbal remedy, and it was calculated using the following formula (Rossato et al., 1999):  =

∑ 

Where: UV= use value of species U= number of quotations per species n= number of informants The botanical family use value (FUV): can be calculated using the following formula:

Where: FUV= family use value, which equals the average total use value for each species in the family UV= use value of the species belonging to the family n= number of species in the family (Hoffman and Gallaher, 2007). Fidelity level (FL): FL is used to determine the most frequently used plant species for treating a particular ailment category by the informants. The FL is calculated using the following formula (Martin, 1995):

Where: Np: is the number of use-reports cited for a given species for a particular ailment category.

N: is the total number of use-reports cited for any given species. Rank order priority (ROP): This index combines FL, the previously calculated index and the RP (relative popularity). It is calculated using the following formula:

Where: ROP = rank order priority. FL= fidelity level. RP = relative popularity. A simplified calculation of RP has been proposed (Amorozo, 1988) in which the ratio of the number of informants who cite a given species to the number of informants who cite the most frequently cited species is determined. Informant consensus factor (Fic): Fic is used to see whether there is an agreement in the use of plants in the ailment categories between the plant users in the study area. The Fic was calculated using the following formula (Bağcı, 2000):

Where: Nur: is the number of use-reports for a particular ailment category. Nt: refers to the number of taxa used for a particular ailment category by all informants. Jaccard index (JI): Jaccard index (JI) is calculated by comparison of previously published studies from regional and other areas as well as at global countries by analyzing the percentages of quoted species and their medicinal uses by using the following formula (Gonza et al., 2008):

Where: a: is the number of species of the area A. b: is the number of species of the area B. c: is the number of species commune to both areas A and B. In the present study, we calculated a similarity index between our survey and other studies which were carried out in different regions of Morocco and in neighboring countries (Algeria, Mauritania and Spain) during the last ten years. Accordingly, we used the previously formula (JI), where in our case, a is the number of species of our area study; b is the number of species in a given study of a Moroccan region and c is the number of species commune to our area of study (Tafilalet) and the other areas of study. 3. Results In this survey, 1616 persons were interviewed and the totality (100%) of them is originated from the area of study (Tafilalet). We quoted 194 species belonging to 63 families. Results of our survey can be presented in four grand sections. 3.1. Socio-demographic data Results concerning this section are illustrated in Table 2 and show that the majority of interviewed persons belonged to the age range of 30 to 60 years (70%) and fifty three percent (53%) of them are women. All informants are originated from the area of study. On another hand, nearly 92% of interviewed belong to the rural area and the primary study level formed the majority of educational level of them with a rate of 40%. Finally, heritage concerning traditional medicine is the mainly source of knowledge (45%) for the population of Tafilalet. 3.2. Medicinal plants in Tafilalet 3.2.1. The Use Value (UV)

Results concerning this index are presented in Table 3 as follows: 194 plant species belonging to 69 botanical families were quoted in this survey. The ten highest values of UV correspond to the following species: Rosmarinus officinalis (UV=0.24), Origanum vulgare (UV=0.22), Artemisia herba alba (UV=0.17), Mentha pulegium L. (UV=0.16), Trigonella foenum graecum (UV=0.12), Lippia citriodora (UV=0.12) and Allium sativum (UV=0.10). While, the lowest values of UV were assigned to the following species: Aquilaria malaccensis, Hyoscyamus muticus, Datura stramonium, Smilax aspera, Galium aparine (UV=0.0007). In order to well understand the relationship between people and plants in this study, two tables were given (Tables 4 and 5). In this context, the ten most cited species in this survey were chosen for this purpose. Table 4 represents information about medicinal plants: species code (SP), scientific name, mode of preparation, ailments treated by this species and number of citation. While, Table 5 represents information about informants who cited these species: age, gender, stratum for which informant belongs, educational level and function (ordinary people or herbalist). Each group of informants who cited one of the ten species is presented in Table 4 by a code of informant (CI). For example, I1 is the group of informants who cited Rosmarinus officinalis L. (SP1) in the present investigation. For all groups the percentage of each slice of age, the percentage of gender, the percentage of each stratum for which informants belong, the percentage of educational level and the percentage of each function were calculated and presented in Table 5. 3.2.2. The botanical Family Use Value (FUV) Relating to this parameter, the highest values of UF have been observed in the families: Liliaceae (FUV=0.106), Lamiaceae ((FUV=0.059), Verbenaceae (FUV=0.051), Lythraceae (FUV=0.043), Ranunculaceae (FUV=0.038), Oleaceae (FUV=0.034), Zygophyllaceae (FUV=0.031), Punicaceae (FUV=0.030), Iridaceae (FUV=0.028) and Chenopodiaceae (FUV=0.027).

While,

Cucuribitaceae

(FUV=0.0003),

Solonaceae

(FUV=0.0004),

Asparagaceae (FUV=0.0007), Geraniaceae (FUV=0.0007), Smilacaceae (FUV=0.0007) and Fagaceae (FUV=0.0007) had the lowest values of FUV among the recorded families. 3.3. Traditional medicine knowledge 3.3.1. Part used, mode of preparation and utilization of drugs Leaves represent the most utilized part for preparation of drugs from medicinal plants and the seeds occupy the second place followed by whole plant (Table 3). In addition, regarding the manner of preparation of medicinal plants, the most cited was represented by decoction followed by the infusion mode, the powder mode and mask. 3.3.2. Fidelity Level and Rank Order Priority Results concerning Fidelity Level and Rank Order Priority and illustrated in Table 6 show that 57 species were reported by informants with their FL and ROP, values and taxa with the total number of use-reports inferior to 20 (N<20) were excluded. The ten highest values of FL were: Cistus salviifolius (FL=100%) for treating gastrointestinal disorders, Daphne gnidium L. (FL=100%) for treating care hair loss and dandruff, Pennisetum typhoides (FL=93%) for treating heal bone diseases, Herniaria fontanesii (FL=87%) for treating Kidney disorders, Rosa damascene (FL=86%) for cosmetic applications, Zingeber officinalis (FL=86%) for treating gastrointestinal disorders, Camellia sinensis (FL=80%) for caring gastrointestinal illness, Mentha puligium (FL=77%) for treating respiratory diseases, Lavandula multifida (FL=72%) for treating disorders related to nervous system and finally, Chenopodium ambrosioides (FL=72%) for healing fever. Concerning values of ROP, Origanum vulgare (ROP=53%), Mentha puligium (ROP=51%), Rosmarinus officinalis (ROP=31%), Artemisia herba alba (ROP=30%) and Allium sativum (ROP=28%) had the highest values. 3.3.3. Informant Consensus Factor (FIC)

Table 7 listed ailments that were cited in this study. The highest values of Informant Consensus Factor were recorded for digestive system disorders (FIC=0.29), respiratory system diseases (FIC=0.29), nervous disorders (FIC=0.22), urogenital and gynecological diseases (FIC=0.22). While, illnesses such as microbial infections (FIC=0.03) and skeleton– muscular system problems (FIC=0.06) had the lowest values of FIC. 3.4. Jaccard similarity index (JI) 3.4.1. Jaccard similarity index for Tafilalet and the other regions of Morocco The Jaccard similarity index (Table 8) was calculated for nine regions of Morocco and the results revealed that the region of Tata is the most similar to Tafilalet region with JI=42.97. Whereas, oriental Morocco (JI=40.33), Agadir Ida Outanan (JI=34.07) and Haute Mlouya (JI=31.62) have respectively the second, third and fourth positions concerning similarity related to species used in traditional medicine by local populations in Morocco. 3.4.2. Jaccard Similarity Index between Tafilalet and neighboring countries Results concerning the Jaccard Similarity Index obtained from the comparison between Tafilalet and three neighboring countries (Algeria, Spain and Mauritania) are shown in Table 9. This index was calculated for five areas of study for Algeria (Haggar, Djbel Zdiim, Mascara, Tiaret and M’sila), three areas of study for Spain (Arribes del Duero, South of Alava and Riverside of Navarra) and one area of study for Mauritania (Assaba). Among these three neighboring countries, Algeria has the highest similarity with Tafilalet (JI=13.00), this value was observed for the ethnobotanical survey carried out in M’sila. The second value of Jaccard Index Similarity was observed also in Algeria for the region of Tiaret (JI=8.79), the third in Spain at the level of Arribes del Duero (JI=7.67), while the lowest value of JI corresponded to Mauritania (JI=0.88).

3.4.3. Novel taxa and toxic herbs reported in this survey In the present study, 17 new species were quoted for the first time and were never mentioned in a previous ethnobotanical survey carried out in Morocco (Table 3), while 28% of species cited in this study are toxic. 4. Discussion This study demonstrated that Tafilalet region is very rich regarding traditional medicine, popular phytotherapy and botanical patrimony. This richness is reflected via the indigenous knowledge of interviewees that demonstrated a wide culture concerning the use of medicinal plants, especially herbalists who have enriched the present study with precious information. Results found in this enquiry are discussed in detail below. 4.1. Socio-demographic data Informant is a central element in the ethnobotanical survey. Therefore, a better understanding of informants ensures good and reliable study. Consequently, collecting sociodemographic information (age, gender, ethnicity, study level, occupation…) about participants is very useful in such investigations and this factor plays an important role in order to analyze and interpret responses obtained. Furthermore, differences in age, gender, social position and ethnicity affect the quality of the interaction (Gary, 1995). Table 1 summarizes all socio-demographic data collected from participants. In our study, the main age range of participants is between 30 and 60 years (73%). Generally, people at this age are involved in responsibility related to the health of the family. Moreover, the knowledge about medicinal plants is more important especially in rural environment. Informants aged over 60 years occupy the 3rd position (12%). Thus, elders play a particular role in an ethnobotanical survey because they have an extensive experience accumulated over time. According to Justin & Nancy (2011), community elders are frequently the bearers of the

largest amounts of native plant knowledge. Nonetheless, this finding did not exclude the other age groups as possessing a valuable knowledge about medicinal plants. Female gender surrogated 53% of all participants. Thus, some similar studies carried out in Morocco showed that Moroccan women are interested in traditional medicine more than men with respectively 71%, 75%, 69% and 59% (Eddouks et al., 2002; Fakchich & Elachouri, 2014; Tahraoui et al., 2007; Ziyyat et al., 1997), several hypotheses may be involved to give an interpretation of this result: the relative frequency of analphabetism of women in the society, the attachment of the women to traditional knowledge (Hamdani, 1984; Jaouad, 1992) and the possibility that women were most often at home during the hours of the survey (Jouad et al., 2001). This inquiry reported that the totality of interviewees (100%) were native to Tafilalet, this factor has affected positively this investigation. Thus, indigenous people are a reliable source of knowledge related to folk medicine and local natural resources. Almost, 26 years ago the World Health Organization (WHO) estimated that “in many countries, 80% or more of the population living in rural areas are cared for by traditional practitioners and birth attendants” (Bannerman, 1983). In the present study, the majority of informants were from rural area (92%). The rural inhabitants are most resort to herbal medicine. Moreover, it is widely known that the majority of ethnobiological studies have focused on rural and/or indigenous communities (Anderson et al., 2011; Balick et al., 2000; Cunningham et al., 2001). In fact, according to results of the last census (2014), the number of rural people is greater than the urbanites in this area of study. Where, 224317 in rural area against 193922 in the urban one (Errachidia province or Tafilalet), this also could explain the important rate of this category of informants envisaged in this enquiry. Furthermore, socioeconomic situation of the urban area of the South-East of Morocco generally and Tafilalet particularly is well characterized by its fragility; a lack of health facilities and health frameworks qualified. And even if there are hospitals and clinics in the urban areas, people encounter several problems,

such as lack of infrastructure, especially paved roads; rarity of means of transport, lack of logistical means and the high cost of medication and synthetic drugs constitute also an obstacle. Indeed, the economic situation of the majority of population in such areas that is based mainly on personal agricultural activities and limited income for this category of society is not neglected. All the previous elements create decidedly a major impulse for rural people to move towards traditional healthcare, especially the use of medicinal herbs. Concerning the study level of informants, the majority of them had a primary level (40%), while proportions of other levels (Illiterate, High school and University) were 17%, 32% and 12% respectively. Educational level is reflected by cultural level and people with high study level possess more information about primary healthcare and modern medicine. Nonetheless, this finding did not mean that this category of society owns more knowledge related to traditional medicine or botanical folk. In contrary, several previous studies showed that people with lower educational level have more expertise in this field of traditional medicine and medical folk botany (Fajardo et al., 2008). The results show that heritage is the main source of acquisition of knowledge for inhabitants of Tafilalet (more than 44%), followed by experience from other people (28%), personal experience (21%) and literature (7%) (Table 2). Heritage represents an essential tool for transferring knowledge which is not written in books from one generation to other (Fajardo et al., 2008). Family, friends and neighbors play also a crucial role in transferring information according to informants. While, for herbalists the main source of acquisition of knowledge is literature (42%), followed by experience from other people (31%), heritage (18%) and personal experience (8%). Literature is an interesting mean of acquisition of knowledge in any field. Thus, literature is a powerful source of information about past and contemporary cultural uses of plants (De Carvalho, 2011). 4.2. Medicinal plants in Tafilalet

This survey has recorded a total of 194 species belonging to 69 families (Table 3). Large variations in climate and topography make Morocco one of the richest countries floristically in the Mediterranean (Aafi et al., 2002). In this area, the number of species is approximately 500 and a significant number is common or endemic to pre-desert and Saharan zones (Ozenda, 1983). The medicinal plants of the region are well known at national scale by their high healing effectiveness. The efficiency of these medicinal plants is related to the climate typical of the region which is arid to semi-arid; this characteristic leads to increase concentration of bioactive molecules in flora (Eddouks et al., 2002). In order to better analyze and estimate quantitatively data collected concerning the use of species and families by people, two indices were calculated: the Use Value (UV) and the Botanical Family Use Value (FUV) (Table 3). 4.2.1. The Use Value (UV) The ten highest values of UV correspond to the following species (Table 3): Rosmarinus officinalis L. (UV=0.24), it has been used in traditional medicine of numerous Mediterranean and Asian countries (Turkey, Tunisia, Algeria, Spain, French, Italy, India, etc.) as an antispasmodic, in renal colic and dysmenorrheal treatment, as well as in prevention of relieving respiratory disorders. It has also been used as an analgesic, antirheumatic, carminative, cholagogue, diuretic, expectorant, antiepileptic agent and has beneficial effects on human fertility. Furthermore, this plant is used as an insecticide and herbicide and it is also known as a general tonic in case of excessive physical or intellectual works and in heart diseases. In addition it is known as a rubefacient, stimulant of hair growth. Finally, this plant is also used for the treatment of eczema, scalp, boils and wounds (Ashoor, 1985). Origanum vulgare L. (O. Vulgare) (UV=0.22); traditionally, this herb is used in Spain against enterobiasis and stomach ache, it is also used for treating coughs, colds and sore throat and various disorders of respiratory system as bronchitis and asthma (González et al., 2010; Alarcόn et al., 2015). In Italy, it is used for heartburn and asthma, it is also used as appetizer,

carminative, depurative, digestive and sedative (Vitalini et al., 2015). In Turkey O. vulgare is used as antidiabetic, for treatment of Colds, flu and urinary inflammations (Özdemir and Alpinar, 2015; Cakilcioglu et al., 2011). Artemisia herba alba (UV=0.17): in Tunisia, this plant is widely used in traditional medicine to treat diabetes, bronchitis, diarrhea, hypertension and neuralgias (Marrif et al., 1995; Said et al., 2002; Tahraoui et al., 2007). In Algeria, it is used as antidiabetic, antihypertensive agent and against digestive disorders as well as intestinal bloating and intestinal parasites (Benarba et al., 2015; Chermat et al., 2015). In Spain, Artemisia herba alba is used for caring some respiratory diseases (Calvo et al., 2011). Mentha pulegium L. (M. Pulegium) (UV=0.16); this medicinal plant is known in traditional phytotherapy of numerous countries particularly in Mediterranean area and Asia. In Algeria, M. Pulegium is well known as an antihypertensive and antispasmodic agent, it is also known as a remedy for respiratory tract diseases (Boudjelal et al., 2013; Benarba, 2015). In Italy, M. Pulegium is used against Hematomas, wounds and swelling (Tuttolomondo et al., 2014). In Portugal, this plant is popularly used as an antihypercholesterolaemic agent, a gastric analgesic, and it is also used against sea-sickness, for headache and colds treatment and as intestinal analgesic and hepatic protector (Novais et al., 2004). Trigonella foenum graecum (UV=0.12); traditional uses of this herb are well popular in whole world, for example in Algeria, Trigonella foenum graecum has many local therapeutic uses: it is known as aperitif, tonic, emollient and purgative, it is also useful for diabetes treatment. In Iran, this plant is useful against respiratory complains, infection, blood fat and women infertility (Ghorbani, 2005; Miara et al., 2013), while this same plant is used in India to treat allergy, appetite loss as well as against hypercholesterolemia (Rajendra & Estari, 2012). Lippia citriodora (Palau) Kunth (UV=0.12); this aromatic and medicinal plant is considered as an efficacy remedy against respiratory diseases in Algeria (Benarba, 2015). In Portugal, it

is used as a sedative agent, a gastric analgesic, an intestinal´ anti-inflammatory and against sea-sickness (Novais, 2004). Allium sativum L. (A. sativum) (UV=0.10); in Jordan, this edible plant is used against stomach soothing, as an antiemetic; it strengthens heart and lowers cholesterol (Efraim, 2002). In Spain, A. sativum is used for treating chilblains, helminthiasis and toothache, to prevent heartattack and circulatory problems, as a remedy against warts, mouth infections, muscle pain and rheumatism (Benítez et al., 2010). The results show that there is a significant similarity between uses of species cited in our survey and those cited in other regions particularly those belonging to Mediterranean area. This index (UV) was used to show the relative importance of each plant species known locally to be used as herbal remedy. Effectively, the plants mentioned above are very popular among Moroccans generally and among the population of Tafilalet particularly. Thus, we can rarely find someone who does not know at least one use in phytotherapy for one of these plants. Therefore, values of UVs found in this study confirm the place of the cited species within the popular culture and heritage knowledge of Tafilalet’s population. The lowest values of UV were assigned to the following species: Aquilaria malaccensis Lam, Hyoscyamus muticus L, Datura stramonium L, Smilax aspera L, Galium aparine L (UV=0.0007). This means that these species are less common within the traditional healthcare of the Tafilalet’s population. Tables 4 and 5 illustrate the relationship between informants and the ten most cited species. For example, the group of informants (I3) who cited the species Artemisia herba-alba Asso (SP3) is distributed into the ranges of age as follows: 23% of them are aged of least of 30 years, 37% are aged between 30 years and 60 years, 40% between 60 and 80 years, while the rest are aged of more than 80 years, 73% of them are women, 41% of them are illiterate and 36% belongs to the primary educational level. Concerning their distribution according to the

stratum, 31% of them belong to Errachidia and 23% to Jorf. In fact, this indicates that the group of informants is constituted especially from women and situated in the range of age between 60 and 80 years belong to Errachidia’s stratum and most of them are illiterate. This category has recourse often to SP3 for treating a list of ailments such as gastrointestinal disorders, diabetes, ulcer, fever, intestinal parasites, rheumatism, constipation, heart diseases, menstruation pains, cough, liver diseases, etc. The same comparison that was carried out between I3 and SP3 above can be made between I1 and SP1, I2 and SP2, I4 and SP4, I5 and SP5, I6 and SP6, I7 and SP7, I8 and SP8, I9 and SP9 and I10 and SP10. 4.2.2. The botanical Family Use Value (FUV) In this study, 69 families were recorded (Table 3). In this framework, Moroccan flora is distributed in 150 families (Hmamouchi, 1999), this means that 46% of known botanical families of Morocco are cited in this enquiry. The panel of medicinal herbs used in Tafilalet is very rich and diversified when compared to many recent Moroccan enquiries in which the numbers of families were respectively 60, 56, 43 and 41 ( Fakchich & Elachouri, 2014; Abouri et al., 2012; Doukkali et al., 2015; Mikou et al., 2015). The botanical Family Use Value (FUV) is a quantitative technique which allows to better understand the relation between the botanical families and users of species belonging to these families in herbal remedies. Liliaceae (FUV=0.106), Lamiaceae ((FUV=0.059), Verbenaceae (FUV=0.051),

Lythraceae (FUV=0.043), Ranunculaceae (FUV=0.038),

Oleaceae (FUV=0.034), Zygophyllaceae (FUV=0.031), Punicaceae (FUV=0.030), Iridaceae (FUV=0.028) and Chenopodiaceae (FUV=0.027) were the ten popular families recorded in the present investigation. While, Cucuribitaceae (FUV=0.0003), Solonaceae (FUV=0.0004), Asparagaceae (FUV=0.0007), Geraniaceae (FUV=0.0007), Smilacaceae (FUV=0.0007) and Fagaceae (FUV=0.0007) had the lowest values of FUV among the recorded families. The family of Liliaceae had the highest value of the Family Use Value (FUV=0.106) and was

represented by just one species; Allium sativum (garlic). This plant is much known in the traditional folk knowledge in Morocco as an effective antihypertensive plant and natural antibiotic which is also used against pests and hair loss and against other more health problems. It is currently used locally in food plates not only as a flavor but particularly for his therapeutic virtues. The family of Lamiaceae occupied the second position regarding the FUV (FUV=0.059). Species of this family are widely known as aromatic plants. Species belonging to this family as Origanum vulgare, Origanum majorana, Thymus vulgaris, Rosmarinus officinalis or Mentha viridis are daily used by inhabitants of Tafilalet not only in traditional medicine but also to prepare foods. Several recent investigations undertaken in different regions of Morocco demonstrate that the Lamiaceae occupied advanced ranking in the list of botanical families used by informants for a medicinal purpose (Teixidor-Toneu et al., 2016; Mikou et al., 2015; Benlamdini et al., 2014; Salhi et al., 2010). In the same context, an ethnobotanical survey carried out in 2012 in Algeria, demonstrated that Lamiaceae dominated the botanical families that were quoted in this survey with a percentage of 22.4% (Boudjelal et al., 2013). Another recent enquiry realized in Turkey showed that Lamiaceae occupied the first place in the list of botanical families used by local population in this region for a traditional therapeutic purpose (Güzel et al., 2015). In this framework, and according to Parveen et al. (2007), many other reasons may be interfere to elucidate the frequent use of traditional medicine in rural areas: the strong association of people with local flora and their belief on traditional knowledge regarding plants as medicine, easy availability of local medicinal plants, poor access to allopathic drugs and their high cost and lower economic profile of the rural people. 4.3. Traditional medicine knowledge 4.3.1. Part used and mode of preparation and utilization of drugs

The leaves represent the most utilized part for preparation of drugs from medicinal plants and the seeds occupy the second place followed by whole plant. This could be explained by the quickness and ease of medicinal plants harvesting and by the fact that aerial parts of plants are the center of the photosynthetic phenomenon. Furthermore, it has been reported that root and bark plant materials are not sustainable for the development of traditional medicines or for drug discovery (Geoffrey, 2015). Mode of preparation of a drug in traditional medicine practice is a crucial step in the operation of treatment of an illness. Thus, it can interfere at different levels as follows: -

It is a limiting factor in the extraction of bioactive molecules from the matrix of the plant material and some substances require a specific technique to be extracted.

-

The rates of yield of the bioactive substances are strongly related to the mode of preparation.

-

This could act on the pharmacological and biological activity of the drug extracted from the herbal matter. In the present study, the most frequently quoted manner of preparation of medicinal

plants was represented by decoction followed by the infusion mode, the powder mode and mask. The mode of preparation is also related to the type of use (external or internal), normally for an external mask use, massage or suppository modes are applied while decoction, infusion, maceration, and the other modes are involved for an internal use. Preparations using some foods such as honey, olive oil and milk in mixture with herbal drugs were also cited in this enquiry. These foods especially honey and olive oil are very popular in the Moroccan Pharmacopeia because they occupied an exceptional place in the holistic medicine. Otherwise, seeing their chemical composition which is rich in bioactive compounds these important foods are used in several cases only as remedies. Enormous

studies have targeted these two foods (Kaškonienė et al., 2009; Ma˘rghitas et al., 2008; Mustafa and Hajdari, 2010; Mascitelli and Goldstein, 2013; Bouarroudj et al., 2016).

4.3.2. Fidelity Level and Rank Order Priority In Table 6, 57 species were reported by informants with their FL and ROP values and taxa with the total number of use-reports inferior to 20 (N<20) were excluded. FL is a technique which relies on agreement among informant responses for a principal therapeutic indication (Friedman et al., 1986). Hence, in this inquiry we reported that, the species cited in Table 6 are the most reliable for treating the ailments. For example, Cistus salviifolius (FL=100%) is well known in some regions of Morocco as remedy against gastrointestinal disorders (Ouhaddou et al., 2014; Akdime et al., 2014). It is also used in Turkey against constipation (Fakir et al., 2009). Concerning Daphne gnidium L. which had a FL equal to 100%, all informants are in agreement about the use of this specie to care hair loss and dandruff, this result is in concordance with a study performed in Mascara (North West of Algeria), where the same herb (Daphne gnidium L.) had also a FL value of 100% for a hair care purpose (Benarba et al., 2015). Contrarily, among the lowest values of FL, the results showed the use of Rosmarinus officinalis L. to treat cardiovascular disorders with FL=31%, Lepidium sativum L. for care hair loss and dandruff with a FL=33% and the use of Myrtus communis L. as a treatment for gastrointestinal disorders with FL=34% (Table 6). Rank Order Priority (ROP) is an index calculated to explain the distribution of knowledge of the species in relation to the richness of the resources cited in the studied use category (Da Silva et al., 2014). This survey revealed that Origanium vulgare L. (ROP=53%), Mentha puligium L. (ROP=51%), Rosmarinus officinalis L. (ROP=31%), Artemisia herba alba Asso. (ROP=30%)

and Allium sativum L. (ROP=28%) had the highest values of ROP, this means that these species are the most known in Tafilalet. While herbs such as Capparis spinosa L. (ROP=2%) and Ammoducus leucatrichus Cosson & Durieu. (ROP=3%) had a lower priority among medicinal plants used by the local population (Table 6). 4.3.3. Informant Consensus Factor (FIC) Ailments recorded in this survey were grouped into 15 main categories as shown in Table 7 with their FIC values. This factor is calculated to see whether a category of ailment is commonly treated with herbs by the local population. Ailments with highest values of Informant Consensus Factor were: digestive system disorders (FIC=0.29), respiratory system diseases (FIC=0.29), nervous disorders (FIC=0.22) and urogenital and gynecological diseases (FIC=0.22). Results concerning digestive system disorders and respiratory system diseases are in line with those established in a recent survey carried out in Oriental Morocco (Fakchich et al., 2014), in Fez (Central Morocco) (Mikou et al., 2015), in Algeria (Banarba et al., 2015) and in Libanon (Baydoun et al., 2015) . Thus, illnesses related to gastrointestinal tract, respiratory system, nervous system and urogenital tract were the most treated by medicinal plants in the whole world, because this category of diseases is known since antiquity. Furthermore, these results demonstrated that the knowledge exchange about the use of medicinal herbs between informants seems to be a good way for treating these ailments. In the same context, the high values of FIC assigned to gastrointestinal disorders may be explained by the fact that relative clinical signs are common and are more easily identified by the traditional healers (Punnam Chander et al., 2014). Whereas, illnesses such as microbial infections (FIC=0.03) and skeleton–muscular system problems (FIC=0.06) had the lowest values of FIC. Then, these illnesses are the least known to be treated in traditional medicine of local population. Consequently, knowledge related to the popular healing of these illnesses is poorly distributed among the local

population of Tafilalet. The lowest value of FIC was recorded for microbial infections (FIC=0.03). Nonetheless, this finding does not reflect the importance of this ailment because gastrointestinal, respiratory, urogenital or skin diseases may have microbial origin. This finding reflects the ignorance of informants related to the causes of a given illness. 4.3.4. Novel taxa and toxic herbs reported in this survey The present survey reported that 17 new species among the 194 recorded were quoted for the first time and were never mentioned in a previous ethnobotanical survey carried out in Morocco (Table 3). These 17 new species were used from inhabitants of Tafilalet to remedy 14 categories of ailments. In addition, the study reported that about 28% of medicinal plants used by the local population of Tafilalet are toxic. 4.3. Jaccard similarity index (JI) 4.3.1. Jaccard similarity index for Tafilalet and the other regions of Morocco Table 8 illustrates the calculated values of Jaccard similarity index which translates the degree of similarity regarding species cited between our study and other studies carried out in other Moroccan regions during the latest ten years, these regions are respectively Tata, Agadir Ida Ou Tanane, Oriental Morocco, Settat, Haute Mlouya, Kenitra, Ain Elouh, Occidental Rif and Ifrane (Abouri et al., 2012; Ouhaddou et al., 2014; Fakchich & Elachouri, 2014; Tahiri et al., 2012; Benlamdini et al., 2014; Salhi et al, 2010; Akdime et al., 2014; Rhattas et al , 2016; Rhafouri et al., 2014). The Jaccard similarity index was calculated for nine regions of Morocco to make this comparison and the results revealed that the region of Tata is the most similar to Tafilalet region with JI=42.97. This result may be explained by several reasons. Firstly, geographical factors: the distance between Tafilalet and Tata is the second smallest between Tafilalet and all other regions interfering in this study (417 km). It is known that geography influences phytogeography climate and reliefs. This similarity in JI between

Tafilalet and Tata can be explained by the similarity existing between these factors. In addition, the continental Saharan climate is similar in these two regions. Moreover, these two regions are both characterized by oasis ecosystem. Secondly, socio-cultural, historical factors: factors as language, costumes, folklore and history have a strong impact on the ethnopharmacological status. Thus, Tata and Tafilalet regions have several common threads. Both regions belonging to the south of Morocco which is marked by the “Tribal oasian regime” and the system of traditional habitat locally called “Qsours” as a regime of housing typical of the south of Morocco. Furthermore, both Tata and Tafilalet are inhabited by two ethnic populations: Berbers (Amazighs) and Arab. All these common points are involved for facilitating the transfer of knowledge related to the healthcare with medicinal plants and consequently increased the similarity concerning the taxa used for traditional healing. Thirdly, socio-economic factors; actually, the southern regions of Morocco are characterized by a low socioeconomic level. Economy of these regions is based on agriculture which occupies about 80% of the workforce in Tata and 60% of the workforce for Tafilalet despite the rigidity of climatic conditions. Tourism also contributes to the economy of these regions. Furthermore, geographical situation of these regions contributes to their isolation. All these elements underwrite to this similarity in the use of medicinal plants for healthcare purposes between Tafilalet and Tata. Traditional use of plants is influenced by economic factors such as displacement and urbanization processes, changing lifestyles, social transformations, etc (Mustafa & Hajdari, 2014). On the other hand, oriental Morocco (JI=40.33), Agadir Ida Outanan (JI=34.07) and Haute Mlouya (JI=31.62) have respectively the second, third and fourth positions concerning similarity related to species used in traditional medicine by local populations in Morocco. The distance between Tafilalet and Oriental Morocco is the smallest between Tafilalet and all other regions interfering in this study (384 km). Thus, oriental region of Morocco had common borders with the region Drâa-Tafilalet. In addition, this region is linked to Tafilalet

by history-geographical, cultural, socio-economic and demographic factors. All these points are common between two regions and contribute to the similarity in medical knowledge and practice related to the use of plants for treating illness. 4.3.2. Jaccard Similarity Index between Tafilalet and neighboring countries Table 9 shows results of the Jaccard Similarity Index obtained from the comparison between Tafilalet and three neighboring countries (Algeria, Spain and Mauritania). This similarity was carried out for five areas of study for Algeria (Haggar, Djbel Zdiim, Mascara, Tiaret and M’sila), three areas of study for Spain (Arribes del Duero, South of Alava and Riverside of Navarra) and one area of study for Mauritania (Assaba) (Rhattas et al., 2016; Ramdane et al., 2015). Among these three neighboring countries, Algeria has the highest similarity with Tafilalet (JI=13.00), this value was observed for the ethnobotanical survey carried out in M’sila (Boudjelal et al., 2013). The second value of Jaccard Index Similarity was observed also in Algeria for the region of Tiaret (JI=8.79), the third in Spain at the level of Arribes del Duero (JI=7.67), while the lowest value of JI corresponded to Mauritania (JI=0.88). The similarity between our area of study and those carried out in Algeria (JI=13.00; JI=8.79) are not surprising because Tafilalet has common borders with Algeria. In reality, several common grounds exist between Moroccan and Algerian societies. Both societies have the same languages (Arabian and Tamazight), same religion (Islam), similar costumes and traditions; even at the coking and artisanal craft we find great resemblance. Moreover, both countries are belonging to the Mediterranean macroclimate. With these enormous sociocultural, geographical, lifestyle and ethnic similarity, all these common elements were reflected in the inheritance related to ethnobotanical knowledge. Then, it is normal to find this similarity in taxa used for medicinal purposes in both countries.

Concerning the similarity found between Tafilalet and the three areas of study in Spain, the highest value of JI was observed for Arribes del Duero (JI=7.67) followed by Riverside of Navarra (JI=7.17) and South of Alava (JI=2.16). Although enormous differences exist between Morocco and Spain concerning language, religion, habitudes, traditions and lifestyles the values of JI especially for Arribes del Duero and Riverside of Navarra are not negligible. Both Morocco and Spain are belonging to the Mediterranean climate, this natural factor plays an important role in phytogeography and consequently it influences the similarity between the two areas concerning richness of medicinal plants; Arribes del Duero is characterized by the dominance of a Mediterranean mesoclimate (Gonzalez et al., 2010), while for the Riverside of Navarra, the seasonal-rainfall Mediterranean bioclimate occupies most of the territory (Calvo et al., 2011). Historically, there is a very old historical relationship between Morocco and Spain during the Golden Age of Arab-Islamic civilization (seventh to fifteenth century), Morocco and Andalusia (Spain) were both under the governance of this latter civilization. Even if it is assumed that these two areas are situated away of Andalusia (In the North of Spain, while Andalusia in the South), however, these zones known as parts of Western Europe were absolutely influenced by this civilization during this called Golden Age; according to Bashar & Omar (2011). Therefore, it is normal to find similarity related to medicinal plants between Tafilalet and regions from Spain. Finally, the lowest value of Jaccard Similarity Index calculated in this study was established for the region of Assaba in Mauritania (JI=0.88). However, this finding does not reflect the reality, because of the lack of ethnobotanical survey carried out in Mauritania. The common ethnopharmacological heritage of the various Moroccan ethnic groups is well preserved and passed on from generation to generation by oral tradition and through written records and is still blossoming. The Moroccan pharmacopoeia was further developed and enriched by the knowledge brought in by various ethnic groups that migrated to Morocco from many areas, including the Arabs from the Middle East, the Andalusians and Jews from

Europe, and the Africans from Sudan, Senegal, and Niger. Interestingly, Greco-Arab and Islamic medicine was taught in Moroccan-Islamic universities, such as Quarawin until 1893, when the practice was banned by the French colonialists (Bashar & Omar, 2011). The set of these interactions distributed absolutely in the flourishing of the ethnopharmacological inheritance of the region of Tafilalet. The present Ethnobotanical survey highlighted the richness of medicinal plants and their utilization from the population of Tafilalet for managing different ailments. This inquiry quoted 194 species belonging to 69 families used to manage more than sixty health problems. The results reflect the richness, diversity and effectiveness of medicinal plants used by the indigenous population of Tafilalet as well as the great expertise that characterizes inhabitants of Tafilalet and particularly herbalists belonging to this region. Several factors are interfering to construct this great knowledge related to medicinal plants practices. Thus, Tafilalet is an important historical site in Morocco which was in past times a crossroad for caravans from South African Sahara and Soudan. Moreover, this richness is also related to historical events and to mixing of Amazigh, Arab, Jewish, Saharan and Arab-Islamic civilizations at this oasis ecosystem. These historical elements play certainly a crucial role in the transfer and the sharing of knowledge related to the traditional practices of taxa in the traditional healthcare system from one generation to another in Tafilalet. The social life in oasis and “Qsours” system is typical in Tafilalet and is characterized by solidarity which allows and facilitates the spread of information among inhabitants, especially among housewives and from herbalists and traditional healers to consumers, particularly because this system is characterized by its mutualism and its closure on his external environment. Thus, fragile economic situation of population of Tafilalet, especially in rural areas where the majority of informants (91.70%) were from, the mediocre socioeconomic level consisting mainly on agricultural activities and lack of infrastructures push people to practice traditional medicine more than the conventional one, and consequently to develop their own popular medicinal system. Geographic situation

of Tafilalet makes it one of the important sites of biodiversity in Morocco. This is reflected without doubt in the richness of the local taxa. We conclude that, despite the enormous richness of medicinal plants and knowledge related to the popular and local phytotherapy which characterizes Tafilalet, as well as the similarity and resemblance between results found in the present study and others that were undertaken either in other regions of Morocco or further areas from neighboring countries, several procedures remain to consider for a best valorization of this inheritance and more investigations related to phytochemical studies, pharmacological tests, biological activities and toxicity are required. Furthermore, quality control of herbal medicines is a crucial step to develop this field and to ensure their quality, safety, and efficacy. Finally, it is time to develop novel approaches to conserve this heritage coming from our ancestors.

Competing interest The authors declare that they have no competing interests.

Author's contributions Mohamed Eddouks, designed the study, performed the ethnobotanical survey and contributed to the writing of the manuscript. Mohammed Ajebli, contributed to the writing of the manuscript and drawing of graphics. Morad Hebi, contributed to the botanical identification and data analysis.

Author's information ME, Pharmacology, Ph.D., Professor. MA, Pharmacology, Phytochemistery, Ph.D. MH, Pharmacology, Ph.D.

ME, MA and MH are all researchers at Faculty of Sciences and Techniques Errachidia, Team of Physiology and Endocrine Pharmacology. The objectives of the team is identifying plants of interest by ethnobotanical surveys, evaluating their pharmacological activity and isolating active molecules in the aim of providing new active principles for the production of new medicines. The main aimed pathologies are diabetes, hypertension and obesity. Funding

This work was supported by the CNRST under grant N° PPR/2015/35.

Acknowledgements The authors would like to express their thanks to Youssef Alaoui, said Hamdaoui, Fatima Aouragh, Mohamed Oulaanzi, Ismail Bouadid, Bouchra Sadiki Amari, Rabha Ouhajjou, Karima Boudiyani, Mohamed

Sahih, Fatima Zahra Sghiri,

Ismail Khrouch for their

contribution to this survey and all the informants from population of Tafilalet and herbalists who have participated to this survey.

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Tables and Figures legend Table 1. Number of informants in each stratum. Table 2. Socio-demographic data of the informants. Table 3. List of species used for the human ailments recorded in Tafilalet. NCEC: number of citations for each category of informants, TNC: total number of citations, UV: use value, FUV: family use value. P: people, H: herbalist. Table 4. The ten most cited medicinal plants in the present survey. SC: species code, IC: informant code, NC: number of citations. Table 5. Relationship between informants and ten most cited medicinal plants. Table 6. FL and ROP values for the main species and their principal uses. Table 7. Ailments categories and their FIC values.

Table 8. Jaccard similarity index for Tafilalet and the other regions of Morocco. Table 9. Jaccard similarity for Tafilalet and neighboring countries (Algeria, Mauritania and Spain).

Figure 1. Geographical location of the study area. Figure 2. Number of citations and frequency of parts used of medicinal plants in Tafilalet. Figure 3. Number of citation concerning the modes of preparation of medicinal plants in Tafilalet.

Table 1. Stratum

Errachidia Jorf Rissani Tinghir Goulmima Rich Tinjdad Aoufous Arfoud Total

Number of informants Population 426 100 156 255 283 67 113 100 0 1500

Herbalists 33 17 21 16 1 20 2 2 4 116

Table 2. Socio-demographic variables

Age (years)

Gender Origin Habitat

Study level

Source of acquisition of knowledge

Percentage (%) < 30

15

30 - 60

73

60-80 > 80

10 2

Mal

47

Female

53

Tafilalet

100

Other

0

Urban

8. 3

Rural

91.70

Illiterate

16.70

Primary

40

High school

31.7

University

11.7

Heritage

44.77

Reading

6.75

Personal experience

20.82

Experience from other people

27.86

Table 3. Supplement material.

43

Table 4. SC SP1

IC I1

Plant species Rosmarinus officinalis L.

preparation Decoction, infusion, powder and mask

SP2

I2

Origanum vulgare

Decoction, infusion, maceration, powder and mask

SP3

I3

Artemisia herba-alba Asso.

Decoction, Poudre, Infusion

SP4

I4

Mentha pulegium L.

Decoction, infusion and mask

SP5

I5

Trigonella foenum graecum

Decoction, infusion, maceration, powder and mask

SP6

I6

Lippia citriodora (Palau) Kunth

Decoction, infusion, maceration and powder

44

Ailments Cardiovascular disorders, migraine, pains, fever, menstruation and hepatic disorders, nervous disorders, gynecological and sexual disorders, rheumatism, ulcer, hair loss and dandruff, intestinal parasites, hemorrhoids, skin and respiratory diseases, kidney disorders, diabetes, hypertension, constipation and cough Constipation, ulcer, diabetes, gastrointestinal and kidney disorders, diarrhea, vomiting, hair loss and dandruff, influenza, tonsillitis, gingivitis, tonsillitis, skin diseases, anemia, sexual and gynecological disorders, respiratory and cardiac disorders, cough, fever, nervous disorders, intestinal parasites Gastrointestinal disorders, diabetes, ulcer, fever, Intestinal parasites, rheumatism, constipation, heart diseases, menstruation pains, cough, liver diseases, skin diseases, kidney diseases, cancer, hair loss and anemia Influenza, rheumatism, migraine, infertility, ulcer, pains, gastrointestinal disorders, fever, diabetes, obesity, nervous and cardiac disorders, constipation, respiratory diseases and cough Obesity, ulcer, pains, fever, cosmetic, diabetes, gastrointestinal and cardiovascular disorders, skin and kidney diseases, appetite stimulation, intestinal parasites, gynecological and nervous disorders, hemodialysis, rheumatism, hair loss and dandruff Gastrointestinal an gynecological disorders, fever, insomnia, rheumatism, ulcer, nervous disorders and relaxation, hypertension, diabetes, vomiting,

NC 364

343

263

242

180

179

SP7

I7

Allium sativum L.

Decoction, Infusion, powder and mask

SP8

I8

Lavandula multifida L.

Decoction, infusion, powder, bouillon and mask

SP9

I9

Chenopodium ambrosioidesL.

Decoction, powder, infusion and mask

SP10

I10

Salvia officinalis L.

Decoction, infusion and powder

45

bladder diseases, influenza, migraine, kidney disorders, hair loss, cough and cardiac disorders Respiratory and eye diseases, influenza, hemorrhoids, diabetes, cough, hypertension, ear diseases, kidney disorders, intestinal parasites, hair loss and dandruff Rheumatism, migraine, diabetes, fever, kidney and nervous disorders, skin diseases, influenza, cardiac and gastrointestinal disorders, ulcer, hepatic and gynecologic disorders, hypertension, cough, hair loss and dandruff, rheumatism and hemodialysis Fever, cough, vomiting, rheumatism, diarrhea, migraine, nervous, respiratory and hepatic disorders, gynecological disorders, bladder diseases, influenza, hematoma, diabetes, hair loss and gastrointestinal disorders Rheumatism, cardiovascular disorders, ulcer, diabetes, hypertension, fever, obesity, gastrointestinal and sexual disorders, kidney disorders, nervous and gynecological disorders, hair loss and dandruff

160

124

123

94

Table 5. Code of group of informants

I1

Age group (years)

Gender

< 30 (21%)

M (43%)

30-60 (35%)

F (57%)

60-80 (42%) > 80 (4%)

I2

< 30 (18 %)

M (39%)

30-60 (46%)

F (61%)

60-80 (36%) > 80 (1%)

I3

< 30 (23 %)

M (27%)

30-60 (37%)

F (73%)

60-80 (40%) > 80 (1%)

I4

< 30 (20 %)

M (29%)

30-60 (13%)

F (71%)

60-80 (67%) > 80 (0%)

I5

< 30 (11%)

M (35%)

30-60 (51%)

F (65%)

60-80 (37%) > 80 (1%)

Stratum

Education level

Errachidia (26%) Rissani (14%) Jorf (13%) Tinjdad (12%) Rich (10%) Tinghir (9%) Goulmima (7%) Aoufouss (7%) Arfoud (2%)

Illiterate (45%)

Errachidia (29%) Rissani (7%) Jorf (11%) Tinjdad (9%) Rich (15%) Tinghir (11%) Goulmima (10%) Aoufouss (7%) Arfoud (1%)

Illiterate (39%)

Errachidia (31%) Rissani (17%) Jorf (23%) Tinjdad (9%) Rich (8%) Tinghir (4%) Goulmima (3%) Aoufouss (5%)

Illiterate (41%)

Errachidia (19%) Rissani (11%) Jorf (15%) Tinjdad (17%) Rich (10%) Tinghir (11%) Goulmima (9%) Aoufouss (7%) Arfoud (1%)

Illiterate (35%)

Errachidia (17%) Rissani (13%) Jorf (22%) Tinjdad (12%) Rich (6%) Tinghir (11%) Goulmima (9%) Aoufouss (10%) Arfoud (0%)

Illiterate (39%)

46

Function Herbalists (15%)

High school (31%) Primary (15%)

Ordinary inhabitant (85%)

University (9%)

Herbalists (13%)

High school (26%) Primary (19%)

Ordinary inhabitant (87%)

University (16%)

Herbalists (13%)

High school (21%) Primary (36%)

Ordinary inhabitant (87%)

University (2%) Herbalists (16%)

Primary (32%) High school (17%)

Ordinary inhabitant (84%)

University (16%)

Herbalists (0%)

High school (24%) Primary (30%) University (7%)

Ordinary inhabitant (100%)

I6

< 30 (7%)

M (26%)

30-60 (59%)

F (74%)

60-80 (34%) > 80 (0%)

I7

< 30 (12%)

M (81%)

30-60 (51%)

F (19%)

60-80 (33%) > 80 (4%)

I8

< 30 (13%)

M (71%)

30-60 (51%)

F (29%)

60-80 (36%) > 80 (0%)

I9

< 30 (17%)

M (73%)

30-60 (45%)

F (27%)

60-80 (37%) > 80 (1%)

I10

< 30 (7%)

M (81%)

30-60 (63%)

F (19%)

60-80 (27%) > 80 (3%)

Errachidia (26%) Rissani (13%) Jorf (19%) Tinjdad (8%) Rich (16%) Tinghir (7%) Goulmima (10%) Aoufouss (1%) Arfoud (0%)

Illiterate (39%)

Errachidia (31%) Rissani (14%) Jorf (12%) Tinjdad (11%) Rich (10%) Tinghir (8%) Goulmima (6%) Aoufouss (7%) Arfoud (1%)

Illiterate (29%)

Errachidia (22%) Rissani (20%) Jorf (8%) Tinjdad (10%) Rich (6%) Tinghir (12%) Goulmima (9%) Aoufouss (9%) Arfoud (4%)

Illiterate (32%)

Errachidia (41%) Rissani (8%) Jorf (8%) Tinjdad (12%) Rich (14%) Tinghir (8%) Goulmima (5%) Aoufouss (4%) Arfoud (0%)

Illiterate (29%)

Errachidia (24%) Rissani (16%) Jorf (11%) Tinjdad (9%) Rich (15%) Tinghir (9%) Goulmima (7%) Aoufouss (8%)

Illiterate (37%)

47

Herbalists (20%)

High school (24%) Primary (30%)

Ordinary inhabitant (80%)

University (7%)

Herbalists (17%)

High school (15%) Primary (52%)

Ordinary inhabitant (83%)

University (4%)

Herbalists (5%)

High school (22%) Primary (38%)

Ordinary inhabitant (95%)

University (8%)

Herbalists (17%)

High school (15%) Primary (52%)

Ordinary inhabitant (83%)

University (4%)

Herbalists (22%)

High school (11%) Primary (47%) University (5%)

Ordinary inhabitant (78%)

Arfoud (1%)

48

Table 6. Species

Principal use

Cistus salviifolius

Gastrointestinal disorders

54

54

100%

0.15

15%

Daphne gnidium L.

Hair loss and dandruff

32

32

100%

0.09

9%

Pennisetum typhoides

Bone diseases

40

43

93%

0.12

11%

Herniaria fontanesii

Kidney disorders

46

53

87%

0.15

13%

Rosa damascena

Cosmetic

36

42

86%

0.12

10%

Zingeber officinalis

Gastrointestinal disorders

36

42

86%

0.12

10%

Camellia sinensis

Gastrointestinal disorders

28

35

80%

0.10

8%

Mentha puligium

Respiratory diseases

186

242

77%

0.66

51%

Lavandula multifida

Nervous disorders

89

124

72%

0.34

25%

Chenopodium ambrosioides

Fever

88

123

72%

0.34

24%

Cassia italica

Gastrointestinal disorders

26

39

67%

0.11

7%

Rubia tinctorum

Anemia

22

34

65%

0.09

6%

Punica granatum

Kidney disorders

29

45

64%

0.12

8%

Delphinium staphysagria

Rheumatism

16

25

64%

0.04

7%

Allium sativum

Microbial infections

102

160

64%

0.44

28%

Np

49

N

FL

RP

ROP

Anabasis aretioides Moq. & Coss. ex Burge.

Diabetes

14

22

64%

0.06

4%

Olea europaea

Diabetes

63

101

62%

0.28

17%

Anisosciadium orientale

Respiratory diseases

20

33

61%

0.09

6%

Matricaria camomilla

Nervous disorders

30

51

59%

0.14

8%

Ammoducus leucatrichus

Gastrointestinal disorders

11

19

58%

0.05

3%

Thymus vulgaris

Respiratory diseases

61

107

57%

0.29

17%

Lippia citriodora

Fever

102

179

57%

0.49

28%

Nigella sativa

Diabetes

51

90

57%

0.25

14%

Origanium vulgare

Gastrointestinal disorders

192

343

56%

0.94

53%

Foeniculum vulgare

Gastrointestinal disorders

32

58

55%

0.16

9%

Glycine max

Nutritional disorders

12

22

55%

0.06

3%

Carum carvi

Gastrointestinal disorders

58

110

53%

0.30

16%

Corrigiola telephiifolia Pourret

Rheumatism

35

68

51%

0.19

10%

Cuminum cyminum

Diarrhea

62

123

50%

0.34

17%

Warionea saharae

Diabetes

14

29

48%

0.08

4%

Allium cepa

Kidney disorders

12

25

48%

0.07

3%

Petroselinum sativum

Kidney disorders

32

67

48%

0.18

9%

Eugenia caryoihillaia

Tooth diseases

16

35

46%

0.10

4%

50

Lavandula dentata

Fever

14

31

45%

0.09

4%

Capparis spinosa L.

Sexual problems

9

20

45%

0.05

2%

Cinnamomum cassia

Bloodstream activator

17

38

45%

0.10

5%

Salvia officinalis

Hypertension

42

94

45%

0.26

12%

Lawsonia inermis L.

Hair loss and dandruff

29

65

45%

0.18

8%

Glycyrrhiza glabra

Hypertension

15

34

44%

0.09

4%

Zygophyllum gaetulum

Ulcer

11

25

44%

0.07

3%

Zizyphus lotus

Gastrointestinal disorders

17

40

43%

0.11

5%

Artemisia herba alba

Diabetes

111

263

42%

0.72

30%

Mentha rotundifolia (L) Huds.

Gastrointestinal disorders

42

100

42%

0.27

12%

Citrullus colocynthis L.

Diabetes

14

34

41%

0.09

4%

Peganum harmala

Eczema

28

68

41%

0.19

8%

Juniperus oxyderus

Hair loss and dandruff

36

88

41%

0.24

10%

Trigonella foenum graecum

Diabetes

73

180

41%

0.49

20%

Crocus sativus

Cardiovascular problems

17

42

40%

0.12

5%

Linum usitatissimum

Gastrointestinal disorders

14

37

38%

0.10

4%

Marrubium vulgare

Diabetes

13

35

37%

0.10

4

Myrtus communis L.

Gastrointestinal disorders

10

29

34%

0.8

3%

51

Lepidium sativum

Hair loss and dandruff

13

40

33%

0.11

4%

Rosmarinus officinalis

Cardiovascular problems

112

364

31%

1

31%

FL: the fidelity level. ROP: the rank order priority. Np: the number of use-reports cited for a given species for a particular ailment category. N: the total number of use-reports cited for each species.

52

Table 7.

Ailments categories

Ailments

Nur

Nut

FIC

Digestive system problems

Gastrointestinal problems, vomiting, ulcer, constipation,

158

112

0.29

Respiratory system diseases

Cough, insomnia, influenza, asthma

83

59

0.29

Nervous system disorders

Migraine, vertigo, relaxation, headache

79

62

0.22

Cardiovascular system problems

Cardiac problems, hypertension, hemorrhoids, angina

66

56

0,15

Urogenital and gynecological disorders

Kidney disorders, bladder disorders, sexual disorders, menstruation disorders, menstruation pains, birthing pains, hemodialysis, infertility, facilitation of childbirth, delay of menses

112

88

0.22

Endocrine problems

Diabetes, obesity, liver disorders

110

91

0.17

Cancer

Cancer

22

18

0.19

90

85

0.06

6

5

0.2

Rheumatism, articular problems, Skeleton– muscular system problems arthritis, muscular tear, bone diseases

Antidote

Ophidians' poison, snake and scorpion bites

Dermocosmetology

Skin diseases, hair loss and dandruff, care face, burn and scars, vitiligo, acne, eczema, sun burn

114

97

0.15

Anti-inflammatory

Pains

23

21

0.09

53

Fever

Fever

44

39

0.12

Tooth problems

Gingivitis, sore tooth

7

6

0.17

Blood and nutritional problems

Anemia, hemorrhage, hematoma, appetite stimulation, nutritional disorders

22

20

0.1

Microbial infections

Intestinal parasites, typhoid, diarrhea, mildew

36

35

0.03

Ear, eye and nose problems

Ear, eye and nose

16

14

0,13

Others

Improving immunity, maternal milk

3

2

0.5

FIC: the informant consensus factor Nur: the number of use-reports for a particular ailment category. Nut: the number of taxa used for an ailment category by all informants.

54

Table 8.

Other regions of Morocco

Region of similarity

Area of study

Indices

A Occidental B Rif C A Ifrane B C a Ain Elouh b

Kenitra

Haute Mlouya Agadir Ida Ou Tanane Settat

Tata

Oriental Morocco

103 194 31 46 194 33 123

c a b c a

194 55 62 194 48 115

b c a b c a b c a b c a

194 74 110 194 77 90 194 40 163 194 107 148

b

194

c

98

JI

References

11.65

(Rhattas et al., 2016)

18.23

(Rhafouri et al., 2014)

20.99

(Akdime et al., 2014)

23.08

(Salhi et al., 2010)

(Benlamdini et al., 2014) 31.49 33.92

(Ouhaddou et al., 2014)

16.39

(Tahiri et al., 2012) (Abouri et al., 2012)

42.80

40.16

(Fakchich & Elachouri, 2014)

JI: Jaccard index. a: the number of species of the area of similarity (in Morocco). b: the number of species in our area of study. c: the number of species commune to both our area of study and the other area of study.

55

Table 9.

Region of similarity

Area of study

Algeria

Haggar Djbel Zdimm (Setif) Mascara

Tiaret

M'Sila

Spain

Arribes del duero South of Alava

Mauritania

Riverside of Navarra

Indices A B C A B C A

31 194 3 93 194 18 141

B C A B C A B C A B C A B C A B C

194 14 66 194 21 58 194 29 156 194 22 184 194 8 90 194 19

A

148

JI

References

1.35

(Ramdane et al., 2015)

6.69

(Chermat & Gharzouli, 2015)

4.36

(Benarba et al., 2015)

8.79

(Miara et al., 2013)

13.00

(Boudjelal et al., 2013)

7.67

(Gonzalez et al., 2010)

2.16

(Alarcon et al., 2015)

7.17

(Calvo et al., 2011)

0.88 Assaba

B

194

C

3

(Vall et al., 2011)

JI: Jaccard index. a: the number of species of the area of similarity (in neighboring countries) . b: the number of species in our area of study. c: the number of species commune to both our area of study and the other areas of study.

56

Figure 1.

Rich Errachidia Aoufous Goulmima Tinjdad Jorf Tinghir Arfoud Rissani

57

Figure 2.

58

Figure 3.

59

Daraa-Tafilalet region (Morocco)

Ethnopharmacological survey (1616 informants)

Daraa-Tafilalet is a very rich area of medicinal plants: 194 species belonging to 69 families were inventoried

Graphical Abstract

Cistus salviifolius (highest value of FL )

Daphne gnidium (highest value of FL )

Rosmarinus officinalis (Highest value of UV )

Journal of Ethnopharmacology