Medicinal plants used by women in Mecca: urban, Muslim and gendered knowledge

Background This study explores medicinal plant knowledge and use among Muslim women in the city of Mecca, Saudi Arabia. Ethnobotanical research in the region has focused on rural populations and male herbal healers in cities, and based on these few studies, it is suggested that medicinal plant knowledge may be eroding. Here, we document lay, female knowledge of medicinal plants in an urban centre, interpreting findings in the light of the growing field of urban ethnobotany and gendered knowledge and in an Islamic context. Methods Free-listing, structured and semi-structured interviews were used to document the extent of medicinal plant knowledge among 32 Meccan women. Vernacular names, modes of preparation and application, intended therapeutic use and emic toxicological remarks were recorded. Women were asked where they learnt about medicinal plants and if and when they preferred using medicinal plants over biomedical resources. Prior informed consent was always obtained. We compared the list of medicinal plants used by these Meccan women with medicinal plants previously documented in published literature. Results One hundred eighteen vernacular names were collected, corresponding to approximately 110 plants, including one algae. Of these, 95 were identified at the species level and 39 (41%) had not been previously cited in Saudi Arabian medicinal plant literature. Almost one half of the plants cited are food and flavouring plants. Meccan women interviewed learn about medicinal plants from their social network, mass media and written sources, and combine biomedical and medicinal plant health care. However, younger women more often prefer biomedical resources and learn from written sources and mass media. Conclusions The fairly small number of interviews conducted in this study was sufficient to reveal the singular body of medicinal plant knowledge held by women in Mecca and applied to treat common ailments. Plant availability in local shops and markets and inclusion in religious texts seem to shape the botanical diversity used by the Meccan women interviewed, and the use of foods and spices medicinally could be a global feature of urban ethnobotany. Ethnobotanical knowledge among women in Islamic communities may be changing due to access to mass media and biomedicine. We recognise the lack of documentation of the diversity of medicinal plant knowledge in the Arabian Peninsula and an opportunity to better understand gendered urban and rural knowledge.


The use of medicinal plants in urban environments
Currently, more people live in cities than in rural areas, and urban populations continue to grow: by 2050, two thirds of the world's population will live in cities [1].
Urbanisation brings new health challenges resulting from ease of contagion, maintenance of disease due to high population densities and stress-related ailments [2]. Although biomedicine is often easily available in urban settings, traditional medicines can still be the most convenient and affordable health care resource [2,3]. Similar to people in rural areas, urban dwellers can hold rich medicinal plant knowledge. Recent studies evidence the dynamism and adaptive nature of urban medicinal plant knowledge (e.g. [3][4][5][6][7]), challenging views that such knowledge is lost in cities.
Since Balick et al. [4] noted a lack of ethnobotanical studies in urban areas, urban ethnobotany has flourished. Ethnobotanical surveys in cities have focused on issues such as the change of plant use by international immigrants [4,6,[8][9][10][11][12] or the ethnobotanical diversity found in urban and peri-urban markets [13][14][15] and home gardens [16,17]. With few exceptions [7,14,15], these studies are set in Northern and Western countries. Cities in other parts of the world are equally dynamic plant knowledge hubs, and some have played an important role in the trade of medicinal plant material and knowledge historically. This is the case of cities along the silk and incense trade routes in the Middle East [18][19][20].

Women's medicinal plant knowledge
Several studies across the world have reported the pivotal role of women as holders of medicinal plant knowledge [21][22][23][24][25][26][27][28]. Medicinal plant knowledge is often women's cultural domain because of the role women play in providing household care [21-23, 29, 30]. It also stems from gendered labour and spaces, which affect plant resource harvesting and management [21,22,26]. Women are often more knowledgeable about medicinal plant identification and use than are men [21,[23][24][25], and their knowledge can be epistemologically different [22].
Moreover, the documentation of traditional knowledge as part of plant biodiversity research has historically been gender-biased towards men, which can result in misleading and incomplete results [22,31,32]. Both Howard [22] and Pfeiffer and Butz [32] claim that focus on male specialists, such as shamans and herbalists, has ignored a wealth of lay, female plant knowledge in ethnobotanical research. Historically, ethnobotanists have been predominantly male, which hampered their access to women's knowledge in societies where men are granted greater public access than women [32]. These considerations are particularly important in conducting ethnobotanical research in the Islamic world, where gendered spaces and networks are particularly strong. Women in urban Islamic contexts have so far gone unnoticed by ethnobotanical enquiry, although they are the main medicinal plant users in Saudi Arabian cities [33].

Islam and medicinal plants
In the Arabian Peninsula, where this study took place, the use of local plant diversity for medicines is part of the cultural heritage [34,35] and is currently embedded in Islamic medicinal practices. Islamic medicine integrates ancient Greek medicine, which first arrived to the Islamic world through translations of the works of Hippocrates, Dioscorides and Galen [36], with the teachings of the Prophet Mohamed (Hadith) referring to health, disease and medical treatment that became known as 'The Medicine of the Prophet' [37,38]. From ancient Greek medicine, understandings of the functioning of the body through the humoral system and the view of disease as a loss of balance became part of Islamic medicine [37,39,40]. Arabian physicians, such as Al Razi, Ibn Sina, Aby Al Kassin Al Zahrawi, Ibn Rushd and Ibn Naffs, further developed medicine as a scientific discipline in the Middle Ages [36].
Islamic religious practices generate specific cultural behaviours that aim to preserve health, and early Islamic medical tradition focused on preventive rather than therapeutic medicine [37][38][39]. Beliefs in jinni and Evil Eye as causes of illness are also common in the Arab world [29,36,40]. These magical features are possibly elements of the Bedouin world view that became legitimised by the Quran and the Hadith [40]. Stemming from religious teachings, Islamic medicine has a holistic view of health, where physical, spiritual, psychological, social and environmental factors are intertwined [38,39]. The maintenance of health and recovery from illness are both a physical and spiritual process, underpinned by the belief in God [38,39].

Study aims
Whilst medicinal plant uses are under-documented in the Middle East [41,42] and a trend of loss of ethnobotanical and ethnomedicinal knowledge is observed in this area [36,43], the extent of medicinal plant knowledge held by urban women remains unknown. The aim of this study was to document urban women's medicinal plant knowledge in an Islamic context, identifying the plant species used. Additionally, modes of transmission of knowledge were evaluated, evidence for change noted. The extent to which women's medicinal plant knowledge has been under-documented was inferred by comparing results from free-listing and semistructured interviews conducted with women in Mecca to selected published literature on medicinal plants used in Saudi Arabia.

Research setting: Mecca as a study site
The city of Mecca (Kingdom of Saudi Arabia) is located in a narrow valley 80 km south of Jeddah on the Red Sea coast, west of the Arabian Peninsula (Fig. 1). The city is the capital of the Mecca region, neighbouring the regions of Medina in the north, Baha and Asir in the south and Al-Riyad in the east. The region of Mecca is situated in a subtropical dry environment [44]; its vegetation is dominated by xerophytic species and composed of floristic elements from the Saharo-Arabian, Irano-Turanian and Sudano-Zambian biogeographical regions [45].
Mecca was the birthplace of the Prophet Muhammad and the site of the first Quranic revelation. It is regarded as the most holy city in Islam and the pilgrimage to Mecca, known as Hajj, is obligatory for all able Muslims. Due to the high numbers of pilgrims travelling to Mecca, the city is the most culturally diverse in the Islamic world. Saudi Arabians may use both traditional herbal and biomedical treatments [34,36,45], and a wide range of health care resources are available in Mecca: from traditional medicines and healers ( [45], Al-Qethami, pers. obs), to modern biomedical care provided by the Saudi government for free to all Muslims.

Conducting interviews with Meccan women
The ethical guidelines of the Code of Ethics of the International Society of Ethnobiology [46], the Declaration of Helsinki [47] and University of Reading ethical protocols were followed in this research. Approval from the Ethics Committee of the School of Biological Sciences, University of Reading, was obtained (Research Ethics Project Submission SBS15- 16 11).
Meccan women were interviewed by the first author from May to June 2016; individual free-listing and semistructured interviews were conducted with 32 female adults. Targeted sampling was used for selecting informants who use medicinal plants [48] from the first author's social network. Snowball sampling was later used to identify other local women who use medicinal plants [49]. All the informants were born in the Mecca region, with ages ranging between 28 and 69 years old (see Table 1 for the informants' anonymous social data). Although older informants may hold further knowledge, interviews were conducted until a saturation of information was reached. Prior informed consent was obtained verbally from each woman before they were interviewed. Interviews were conducted in Arabic and recorded when the agreement from the informants was obtained (n = 9). Firstly, women were asked to list the medicinal plants they knew, documenting plant names. Then, semistructured interviews were used to elucidate the parts used, therapeutic uses, preparation and administration processes (including use in mixtures) and perceptions of potential toxicity and side effects of plants used. Moreover, women were asked about how they had acquired this knowledge, if medicinal plants or biomedicine were preferred and when medicinal plants where preferred over biomedicine. The resulting ethnographic data were useful to understand women's attitudes, beliefs and therapeutic goals underpinning medicinal plant use.

Analysis of medicinal plant's salience
Data collected during interviews were structured in 'use reports'. A 'use report' is one citation of one plant use by   [50]. The software anthropac [51] was used to analyse free-lists, obtaining the frequency of citation and Smith's index for each plant [52]. Smith's index is a measure of the cultural importance of each plant depending on the frequency of citation and its rank in the free-lists [52].

Plant collection and identification
Most voucher specimens were obtained directly from informants. When this was not possible, they were obtained from local shops and supermarkets (Atar AlKuwait, Atar Alamana and Matager Alsudia; Fig. 2). Voucher specimens were not obtained for two plants; specimens from the Umm Al-Qura University herbarium were used to identify these according to vernacular names. Voucher specimens (including market samples) were deposited in the Umm Al-Qura University herbarium. Since no plants were collected from the wild directly, collection permits were not necessary. Plant identification was carried out by the first author in the herbarium of Umm Al-Qura University using the Flora of Saudi Arabia [53], and identifications were validated by a plant taxonomist in Umm Al-Qura University. Nomenclature and family adscriptions follow The Plant List [54], and the list was contrasted with the online checklist of the Flora of Saudi Arabia [55].

Literature review
In order to assess the documented Saudi Arabian medicinal plant knowledge, a systematic literature review was conducted. Google Scholar, the Saudi Digital Library,

Medicinal plants used by women in Mecca
In total, 753 use reports were collected during interviews and 118 medicinal plant vernacular names were documented, belonging to approximately 110 botanical taxa (43 families; Table 2), including one algae (Fucus vesiculosus). Ninety-five medicinal plants were identified at the species level, 12 were identified at the genus level, one at the family level and two could not be identified. The most common medicinal families are Apiaceae (10%; 11 taxa), Fabaceae (9%; 10 taxa) and Lamiaceae (7%; eight taxa). Asteraceae, Brassicaceae and Poaceae were represented by five taxa each; Myrtaceae, Rosaceae and Zingiberaceae by four taxa each; and Amaranthaceae, Apocynaceae, Burseraceae and Rutaceae by three taxa each. Seven families were represented by two taxa and 24 families were represented only by one taxon. The most cited salient medicinal plants during the interviews are helba (Trigonella foenum-graecum), kamun (Cuminum cyminum), yansun (Pimpinella anisum), qurfa (Cinnamomum verum) and zanajabil (Zingiber officinale) ( Table 2). Interestingly, we observed that one third (32%) of the plants mentioned in the interviews are common vegetable and fruit crops, and almost one fifth (17%) are spices. More than half of the taxa were not native to Saudi Arabia (54%; Table 2). The modes of preparation and administration for each plant can be found in Table 2. The most used plant parts    are leaves (35%), fruits (21%) and seeds (18%). Underground parts (9%), flowers (8%), resin (5%), oil (2%), the whole plant (2%) and bark (1%) are also used. Infusion is the most used mode of preparation (26%), followed by decoction (22%), grinding (22%), mixing with food (7%) and maceration (6%). Plants are sometimes used as they were sourced without any (further) preparation process (5%), juiced (4%) or mixed with dates (2%), milk (1%), honey (1%) or fruits (1%). The most popular modes of administration are oral ingestion as a drink (63%) and eaten (21%). Plants are also administered as poultices (7%) or applied directly on the teeth (2%). They are rarely (1%) used in mouthwash, fumigation and lotions, inhaled, chewed, rubbed or used as washes.
A total of 67 mixtures were documented including combinations of two to four plant ingredients (Table 3).

Ailments treated with medicinal plants by women in Mecca and remarks on side effects
Medicinal plant uses were documented for 13 etic therapeutic use categories (Table 4). Almost half of the use reports referred to digestive, general and unspecified and respiratory issues, which are common children's, as well as adult's, complaints, but do not reflect the most important diseases afflicting the Saudi Arabian population (cardiovascular diseases, diabetes, neuro-psychiatric conditions and injuries [57]). Gynaecological problems, which encompass menstrual cramps and other menstrual disorders, polycystic ovaries, pregnancy and postpartum issues, are fourth in importance both in number of use reports and number of plant taxa used.
Informants indicated potentially toxic or side effects for almost half of the medicinal plants (n = 52, 47%), often associated with inappropriate use (especially overdosing; Table 2). Many observations on plants' side effects or toxicology made by informants referred to the negative effects of plants on pregnant or breastfeeding women (53% of the plants with noted side effects), or children (11%), and as causing digestive issues (37%) amongst other problems (30%).

Acquiring medicinal plant knowledge and choosing health care
Social and family networks, as well as mass media, were the two sources of medicinal plant knowledge mentioned by the Meccan women interviewed, who were all responsible for the household health. The same sources have been documented for herbal knowledge among the population of Riyadh [33]. Most elderly women interviewed mentioned that they had learned about medicinal plants from their mothers, grandmothers and neighbours (Table 1). Mecca's everyday social interactions among women provide plenty of opportunities for the younger generation to learn from older women's experience about medicinal plant use. Informant 18 (age 60, housewife) mentioned: 'We always encourage our daughters to help us in the preparation of medicinal plants from early age'. Although some younger women interviewed acknowledged learning about medicinal plant knowledge from their elders, written sources, such as popular books on medicinal plants, were also mentioned as sources of medicinal plant knowledge (Table 1). Women of all ages also mentioned television programs as a source of knowledge about medicinal plants; mass media is put forward by biomedical practitioners as a tool for educational programs to modernise health concepts and make aware of available treatments among the poorly educated [34].
Overall, most of the women interviewed (n = 21, 66%) preferred to use medicinal plants rather than biomedicine, but others (n = 11, 34%) preferred biomedicine. Medicinal plants were more often preferred by older than younger women (Table 1). However, preference for medicinal plants also varied depending on the ailment that needed treating. Plants were often preferred to treat general malaise, digestive, respiratory, nutritional, neurological, musculoskeletal, cardiovascular, urological, skin and pregnancy-related ailments, some gynaecological problems and anaemia. The women interviewed preferred to use biomedicine in cases of psychological illnesses, eye problems, cancer, unusual gynaecological bleeding, wounds and infectious diseases. Often, they would prefer biomedicine when they suffer an illness for the first time but use medicinal plants for minor, common or chronic ailments. Informant 22 (45 years old) explained: 'I usually prefer to use medicinal plants to treat my family for diseases that happen continuously such as headache, abdominal pains and menstruation, as well as those that occur due to climate changes such as flu and cough. I use biomedical resources with infectious and psychological diseases, such as depression'. A similar observation was made by Ghazanfar [36] when describing medicinal plant use in the Arabian Peninsula as a whole.  (Table 5), including six studies that did not mention the geographical area in which they were conducted. Of the 11 studies reviewed,

Edible, traded and Muslim medicinal plants
Urbanisation is often considered an aspect of modernisation that leads to the erosion of medicinal plant knowledge [6], but urban contexts may have vibrant medicinal plant use traditions [3][4][5][6][7]. In the Middle East, urban male herbalists are acclaimed for their specialist medicinal plant knowledge [43]. In this study, we evidence a rich body of female, lay medicinal plant knowledge, supporting the observation by Elolemy and AlBedah [33] that women commonly use herbal therapies in Saudi Arabian cities. Although only 32 Meccan women participated in this study, more than 100 medicinal plants were documented to treat a wide range of health complaints. The knowledge held by women in cities is markedly different from knowledge previously documented, with 41% of the plants cited by Meccan women not in the literature we sourced. This points to the underdocumentation of knowledge of medicinal plants in Saudi Arabia but cannot be attributed to male versus female knowledge or urban versus rural knowledge in the absence of further studies. Existing studies may also exclude foods, spices and culinary herbs from ethnobotanical listings of medicinal plants, making less visible knowledge held by women and contributing to the difference we find between published studies and our results.
A third (32%) of the medicinal plants used by the Meccan women interviewed are food plants. Salient food plants cited in this study include onion, celery, cabbage, coriander, lemon, olive oil and dates ( Table 2). The use of food plants as medicines by urban populations is widespread [6] and may be due to the easy access to these plants. Medicinal foods are also an important feature of the Mediterranean medical tradition, observed specifically in the Greek Hippocratic texts that influenced Dioscorides' Materia Medica [60], which in turn influenced Arabic medicinal texts [36]. Specific health beliefs associated with foods have also been observed in Arabia [36]. Along with food plants, many medicinal plants reported are spices (17%), which have played a double role as flavouring and medicinal products since the Middle Ages [61]. The most salient medicinal plants identified here are also all spices (Trigonella foenum-graecum, Cuminum cyminum, Pimpinella anisum, Cinnamomum verum and Zingiber officinale). Spices are both grown in the Middle East and imported from Africa and Southeast Asia (including plants from the Zingiberaceae, Piperaceae, Theaceae, Costaceae, Fucaceae and Musaceae families). This use of imported spices may be a legacy from trade Roman times, when black pepper, ginger, turmeric and cardamom were transported from Southeast Asia into the Mediterranean through Arabian incense trade routes [18,20]. Moreover, medicinal plant use in urban environments biased towards exotic plants has been observed in Brazil [5] and could also be attributed to easier access to these plants in urban areas. The important use of foods and spices medicinally in cities may be a global characteristic of urban ethnobotanical knowledge, since these are often easily available in urban environments.
Plant availability is a key factor shaping traditional plant use. In urban areas, this does not necessarily reflect the region's native plant diversity but the plant diversity traded and available in shops and markets. Differences in plant availability between rural and urban contexts may also account for the differences in plant lists reported in this study and published literature. El-Ghazali et al. [58] observed that native plants used by  Ethnobotanical data collection the list provided by Al-Yahya [63]. Of these, only safarjil (Cydonia oblonga) had not been documented already in the Saudi Arabian medicinal plant literature, which indicates a widespread influence of the Hadith in traditional Saudi Arabian medicine both in urban and rural environments. Moreover, the common use of mixtures among the research participants matches the recommendation made in 'the Medicine of the Prophet' that 'city dwellers' require the use of compound drugs (according to Deuraseh [39]). Specific modes of administration recorded among women in Mecca are also recommended by prophetic medicine [37], specifically the use of food, milk, honey and dates as excipients. This further evidences the influence of Islamic medicine in lay medicinal plant use.

Dynamic female knowledge
As in other Islamic countries, Meccan women are responsible for dealing with most health issues within the household and their medicinal plant knowledge is gender-specific. Gynaecological problems were frequently mentioned and toxicology and remarks about side effects often concerned women's reproductive or children's health, which are all references to genderspecific knowledge.
Meccan women may learn about medicinal plants from their family and social networks, but increasingly, written sources and mass media are becoming important sources of knowledge. This, along with a higher preference for biomedical services amongst the younger generation, could result in the erosion of medicinal plant knowledge. Ethnobotanical knowledge erosion has been observed in the Middle East both among herbalists [43] and the general population [36]. The diffusion of nonlocal knowledge about medicinal plants through mass media is characteristic to urban settings [64] and has a homogenizing effect on oral pharmacopoeias [65]. Mass media often disseminates information on the uses and properties of commercial plants, increasing their visibility [66] and, alongside availability factors, could also contribute to explain the high proportion of food and spices used among the Meccan women interviewed.
Mass media is also used in Saudi Arabia to communicate biomedical education programs [34]. Although these campaigns may be necessary, they favour biomedical knowledge over traditional therapies. Loss of ethnomedicinal and ethnobotanical knowledge may result from different treatment preferences between generations. Higher preference for biomedical treatments among younger Meccan women reflects the same trend among rural Arabic populations elsewhere in Saudi Arabia [36,43,58]. Although Press [2] argues that the disregard of faith and the role of family in biomedical diagnosis and treatment are often sufficient to hamper the utilisation of biomedicine, Ghazanfar notes that in the Arabian Peninsula, 'modern and traditional medicine may be tried [simultaneously], or if one fails the other will be triedbut where modern medicine achieves results, traditional medicine tends to disappear' [36, p. 1]. Biomedicine in Islamic countries integrates faith and has a religious viewpoint on caring [38], but people may still prefer home remedies for treating minor ailments [30,36] as observed in this study. Even when biomedicine is growing and herbal remedies may be in decline, medicinal plant use still plays an important role in urban health care [2,29,30].

Conclusion
We join Emery and Hurley [67] in highlighting the vibrant botanical knowledge and practices in urban areas. Women in Mecca are the primary household health carers and hold a singular, lay body of medicinal plant knowledge to treat mostly common ailments. Plant availability in shops and markets, as well as religious texts, seem to play an important role shaping the urban medicinal flora of women in Mecca; we highlight the important medicinal role in urban environments of foods, spices and traded plants in general. Much of this knowledge had not yet been documented, and gender and geographical biases in research may account for the under-representation of urban women's knowledge in Saudi Arabian medicinal plant literature. However, medicinal plant knowledge among Meccan women may be eroded and changed with the spread of new knowledge through mass media and preference for biomedical care. Documentation efforts are urgent for the preservation of the diversity of medicinal plant knowledge in the Arabian Peninsula. We propose that scientifically rigorous ethnobotanical and ethnomedicinal research 'acknowledging the sociocultural heterogeneity within the community being researched' [32, p. 242] in Islamic settings can be achieved by teams with both female and male ethnobiologists. Al-Sodany et al. [41] have reported that medicinal plants in rural Saudi Arabia are vastly underdocumented, but so far, ethnobotanical enquiry of women's medicinal plants has been even more overlooked.
Abbreviations MW: Meccan women; NA: Not available