Wild edible plant species used in the Ağrı province, eastern Turkey ; Plantas silvestres comestibles en la provincia de Ağrı, Turquía oriental

Wild edible plant species found in Ağrı are nutritionally and economically relevant. Plants are collected by the villagers and brought to the market for sale in the spring. Interest in these plants responds to the increasing demand for organic and natural food. In this study, 350 indepth face-to-face interviews with villagers about the edible plants used in Ağrı (7 districts, 35 villages) were conducted in the region from April 2016 to October 2017. The species, parts used and their consumption and preservation techniques were analyzed and documented. Some of the wild edible plant species are consumed cured or canned, raw or cooked, dried, and some are frozen. The collected 100 wild edible species belong to 25 different plant families. Species are consumed as vegetables (91), spices (19), beverages (16), subterranean parts (5), fruits (3), seeds (3) and exudates (2). The most important species according to their cultural importance were: Amaranthus retroflexus, Beta trigyna, Gundelia tournefortii, Mentha longifolia, Polygonum persicaria, Rumex scutatus, Tragopogon porrifolius subsp. longirostris, and Urtica dioica. Leaves and young shoots were the most frequently used parts. Our study shows that wild edible plants are still well known and used by the local people of Ağrı as a food source. The documented data on these plants herein could be used as baseline information for further investigations on nutritional contents, as they could have the potential to become valuable nutrition sources.


INTRODUCTION
Edible plants that are gathered in the wild to be consumed as a drink or food have been an integral part of millions of people in rural and even urban regions in many developed countries around the world (Block 1991;Leonti & al. 2006;Behre 2008;Łukasz 2010;Hummer 2013;Schulp & al. 2014;Reyes-García & al. 2015). Indeed, wild edible plants have been reported to be sources of folic acid, vitamin, minerals, carotenoids, and other valuable chemical substances, some of them with antioxidant activity (Hasler 2002;Ogle & al. 2003;Tapsell & al. 2006). Wild edible plants are also more likely to be free of herbicide and pesticide residues than cultivated plants. Previous studies suggest that the effects of wild edible plant resources on peoples' health are still little known and that their consumption and gathering have been reduced both in diversity of species and quantity (Millennium Ecosystem Assessment 2005;Tardío & al. 2006;Łukasz 2013;Reyes-Garcia & al. 2015;Bharucha & Pretty 2010;Pardo-de-Santayana & al. 2007). This decrease in wild plants use is related to urbanization and associated rural migration, modernization of lifestyles, industrialization of food production, and extinction of natural plant habitats, among others (Pardo-de-Santayana & al. 2005 Ethnobotanical studies on European wild edible plants have been mainly conducted in the Mediterranean region (Ertuğ 2004;Tardío & al. 2006;Rivera & al. 2007;Pieroni & al. 2008;Blanco-Salas & al. 2019). All these investigations clearly indicate that wild leafy vegetables or wild culinary herbs still represent a relevant part of the local or territorial Mediterranean diet in rural areas. Furthermore, their nutritional constituents have been studied in numerous publications showing relevant human health benefits (Guil Guerrero & al. 1998;Trichopoulou & al. 2000;Couladis & al. 2003;Tarwadi & Agte 2003;Zeghichi & al. 2003). However, deep changes in feeding habits of people living in the Mediterranean rural areas have occurred and many local or traditional dietary models have already been forgotten, especially in situations where environmental and cultural transformations have led to changes in local diets (Tumino & al. 2002), and thus local people have lost their plant knowledge over time. Therefore, studies on traditional food culture should be urgently implemented. This goes particularly for those regions in countries like Turkey, where, for historical and geographical reasons, have remained relatively isolated and local food uses are still alive but at risk of disappearing (Kadıoğlu & al. 2020).
Turkey, at the crossroads between Europe and Asia, has a very rich flora in terms of wild food plants and several ethnobotanical studies have been conducted in various regions (e.g., Özgökçe & Özçelik 2004;Simsek & al. 2004;Kargıoğlu & al. 2008;Öztürk & Dinç 2005;Satıl & al. 2008;Ezer & Arisan 2006;Çakılcıoğlu & Türkoğlu 2010). However, in Ağri province (eastern Turkey) only one ethnobotanical work has been carried out in limited areas and there is a need now to update this information (Gümüş 1994). Therefore, the aim of this paper is to compile the ethnobotanical information about the gathering and consumption of wild edible plant species in the Ağrı province (Turkey) and provide a picture of their current knowledge and utilization.

The study area
The findings for edible wild plants were collected in seven of the eight districts of the Ağrı province, namely, Diyadin, Doğubayazıt, Eleşkirt, Hamur, Patnos, Taşlıçay and Tutak (Fig. 1), a region with an old traditional background in the consumption of these plant species. The Ağrı province is situated in eastern Anatolia Region of Turkey between the latitudes 38˚59'-40˚02'N and longitudes 42˚15'-44˚36'E. It covers a total land area of 11,520 km 2 with a human population estimated at about 540,000. The climate in central districts is generally continental. According to the data from meteorological stations (Ağrı, Doğubayazıt and Patnos), which perform long term observations in Ağrı (1960Ağrı ( -2012, the annual average temperatures of the province vary between 6.2 o C and 9.2 o C. The temperature in Ağrı may rise to 39.9°C in August and go down to -45.6°C in January. The number of frosty days is 160.7 days, and mean annual rainfall is 521.8 mm/yr.

Site selection and survey
One village of each district was selected for an exhaustive biodiversity inventory based on their altitude and vegetation cover (Fig. 1). The spatial extent of the villages is highly variable and so the villages were determined with help of Development Agents and agricultural specialists in study areas. In each village, we started by inventorying these plant species. Five different villages in each district of the study area were visited for the ethnobotanical interviews (for all 7 districts = in total 35 villages or small towns).
The study was carried out between 2014 and 2015 (from April to October). We carried out fieldwork to elaborate the inventory about wild edible plants, and also interviewed native elders who were familiar with these plants. Data were collected through open in-depth interviews with local elders (Martin 2014). Elderly and experienced people who lived in this region for many years and who knew the plants very well were favoured. Older women were preferred since they are more knowledgeable about edible wild plants than men. Ten informants were interviewed in each village and therefore 350 informants (7*5*10 = 350) were recruited (290 female, 60 male; average age 65).
We asked native elders to list all the wild food plants of the region and, for each wild edible plant species listed, to indicate all relevant knowledge about its consumption and gathering: present and past use, processing techniques and mode of consumption. Knowledge regarding wild edible plants was categorized according to Kadıoğlu & al. (2016): Turkish vernacular name, part of the plant used (whole plant, leaf, stem, shoot, root, tuber, exudates, flower, seed and fruit), traditional preparation for consumption and consumption time. Wild food plant uses were organized under seven food usecategories: vegetables (including the subcategories cooked, raw, and pickles), spices, beverages, seeds, fruits, exudates and subterranean parts.
The identifications of the reported wild edible plants are based on Davis & al. (1988) and Davis (1965Davis ( -1985. Identifications were made by the Prof. Dr. Ali Kandemir. Two specimens of each wild edible plant species accompanied by detailed information on the collection locality, the characteristics of the plant, vernacular names, native culinary uses, and wild edible plants meanings were deposited in the herbarium of the Turkey Seed Gene Bank (Ankara) center and the Erzincan Horticultural Research Institute.

Data Analysis
The Cultural Importance (CI) index (Tardío & Pardode-Santayana 2008) was used to express the importance of the studied species: where N is the total number of informants interviewed in the survey (350) and UR is the number of informants that mention each use-category for the species. For example, in the case of Anthriscus sylvestris (L.) Hoffm., 31 informants mentioned its use as a cooked vegetable, 48 as a raw vegetable, 61 as pickles, 14 as spice. Therefore, CI = (31+48+61+14)/ 350 = 0.44.
We also calculated the total CI of each use-category, adding the CI of all the species included in each category and the average CI of the category dividing the total CI of the category between the number of species reported for the category. For example, there are three species in the usecategory seeds (Cephalaria syriaca (L.) Schrad., Gundelia tournefortii L., and Vicia cracca L.). As these uses were mentioned by 46, 35 and nine people, respectively, their CI as seed was 0.13, 0.10 and 0.03. The total CI of seeds was 0.26, the result of adding 0.13, 0.10 and 0.03 and the average CI of seeds was 0.09, 0.26 divided by three, i.e. the number of species of the use-category seeds.

RESULTS AND DISCUSSION
The ethnobotanical survey showed a great diversity of plant species used as wild foods in Ağrı. A total of 100 wild plant species and 25 families were documented and inventoried (Appendix 1). Among the 25 families, the four most important were Asteraceae (17 species), Lamiaceae (14 species), Apiaceae (12 species), and Polygonaceae (10 species  All are vegetables, and most of them are eaten cooked. These data show that there is still a considerable number of species that are widely known, since most of them were cited by more than 90% of the people interviewed (Appendix 1).

Vegetables
The most diverse use-category, with 91 species, was clearly vegetables. The high global CI of the category (42.84) and its high average (0.47) indicate that they are also the most widely used. As in previous studies, our results confirm the high diversity and intensive use of wild vegetables in east Turkey   Many of these vegetables are rich in valuable nutrients. For instance, Malva neglecta, eaten cooked or raw, is rich in vitamins A, B and C (Yeşil & al. 2019). It has substantial local value as a vegetable (CI cooked: 0.8 and CI raw 0.11) both in bordering countries and Turkey (Yeşil & Akalın 2010;Pieroni & al. 2017;Yeşil & al. 2019). As in the other parts of Turkey and in bordering countries, roots, young stems and petioles of Gundelia tournefortii, a good source of vitamins A, C and E are consumed cooked or raw in the study region (Şimşek & al. 2004;Yeşil & Akalın 2010;Karaaslan & al. 2014;Ahmad & al. 2015;Pieroni & al. 2017;Yeşil & al. 2019).
Most species are gathered in spring (mainly May and June), although there are also species that can be gathered earlier (e.g., Crocus biflorus subsp. tauri young leaves are consumed in March and April), later (e.g., Rheum ribes flower stems are eaten in July) or even all year round (e.g., Stachys lavandulifolia Vahl., Ziziphora clinopodioides Lam.). The plant parts most commonly used are young leaves and shoots. They are usually eaten fresh, mainly cooked (61 species), or raw (48) Besides leaves and young shoots, flowers are also consumed. This is the case of the young flowers of Iris persica, that are valued for their mild taste. Interestingly, they are known as the heralds of the arrival of spring (Yeşil & al. 2019). Other interesting species is Echinops pungens Trautv. which immature receptacle of the inflorescences are consumed in a similar way as the heart of the artichokes.
The other important category of vegetables are those used to elaborate pickles. While only nine species are used, its average CI is high (0.32). Their shoots are placed in a sterilized jar along with salt, as well as spices, and are then allowed to mature until the desired taste is obtained. In general, tartness has a very important place in making pickles for people in the region, as the tart taste of these plants is perceived as a special flavor in the sense of "a different taste" and "good for the food". For instance, Ferula orientalis L. and Prangos platychlaena Boiss. are especially valuable for the inhabitants of the Ağrı region and their taste is described as "tart or sour" (Heliz or Çakşur in Ağrı). While Ferula orientalis (0.75) and Prangos platychlaena (0.78) are culturally important species in the study region, their usage is not very common in other areas of Turkey (Kadıoğlu & al. 2016(Kadıoğlu & al. , 2020. Taste has an important place in the selection of wild edibles for local communities and people pay attention to collect tart/sour wild edible plant species to obtain a balanced taste of the meals. On the other hand, the taste of plants or foods is often an important criterion for categorizing, characterizing and detecting food plants (Johns 1986;Nebel 2001;Grivetti 1981).

Spices
Plants used for seasoning food are also commonly used. Nineteen species with a total CI of 5.38 and an average CI of 0.28 were reported, being Mentha longifolia L. (CI = 0.89), Thymus sipyleus Boiss. (0.63) and Ziziphora clinopodioides Lam. (0.58) the species with highest CI. These species are used freshly in salads called Turkish Shepherd's Salad, Rezepte, Mamzana. Additionally, dried parts of them are cooked and consumed in yogurt soups such as Turkish Yogurt Soup. Many of them are members of the Lamiaceae family and are also consumed raw and to prepare herbal teas (e.g., Nepeta italica L., Satureja hortensis L.). An interesting group of six species are used to flavor cheese, mainly Allium species and several Apiaceae (e.g., Anthriscus sylvestris, Chaerophyllum bulbosum L.).

Beverages
In the studied region, 16 taxa were used for preparing herbal teas, being Alyssum peltarioides Boiss the most cited species (0.49). All their parts are consumed as a tea, but also as salad and spice. Another widely consumed beverage is the sherbet (diluted syrups produced with the addition of sugar) made from the flowers of Papaver argemone L.  Kadıoğlu & al. 2016Kadıoğlu & al. , 2020. Another interesting common beverage in Ağrı, also previously cited, is the herbal tea prepared with flowers of Iris persica (0.06) (Akgül & al. 2018).

Subterranean parts
Roots and tubers from five species are eaten in the region, being Arctium tomentosum the most cited (0.66). Its root collar is peeled and consumed raw. The roots of two thistles (Cirsium rhizocephalum C.A Mey., 0.26; Onopordum acanthium, 0.21) are consumed after cooking and the roots of Lathyrus tuberosus L. (0.06) and the corms (bulbiferous tubers) of Crocus biflorus subsp. tauri (0.27) raw.

Fruits
The fruits of three taxa, including Lathyrus tuberosus L.  Mehmet & al. 2018). In addition, Rubus idaeus L. fruits are used to elaborate jams and the leaves of Rosa pimpinellifolia are dried and used to prepare a drink.

Seeds
The use-category seeds includes three species. From our knowledge, Cephalaria syriaca (0.1) has been recorded as edible in the present study for the first time. The seeds are ground and used for making bread mixed with wheat flour. Gundelia tournefortii seeds (0.13) are cooked and consumed as grain/kernel substitutes. The seeds of the plant are dried with a paper towel and placed in a bowl. Then olive oil and salt are added. It is spread on a baking sheet and baked for 5-10 minutes until browned and crispy. Given their lipid content they have been studied as a source of edible oil (Khanzadeh & al. 2012). Finally, Vicia cracca raw seeds are eaten as in southeastern Turkey (Yeşil & al. 2019).
Additionally, because villagers in the local community are usually migrating to large cities or towns and benefiting from the facilities of modern agriculture or different food products, the heritage of traditional wild edible plant species information is decreasing dramatically. Moreover, the younger generation in the local community tends to migrate to large cities in an effort to earn more money and find steady jobs. Consequently, villages in the region are rapidly emptying of their new generations or young population and such a situation raises the danger of losing regional knowledge about wild edible plant species.
The results of our work indicate a very rich ethnobotanical knowledge about wild edible plant species in rural areas of Ağrı. It is vital to document local usages as food through further studies before it is too late. Some of the wild edible plant species of Ağrı are endangered by over grazing, use of chemical herbicides in farming, inattentive picking of edible wild plant species to generate revenue, and expansion of new agricultural lands. Given the nutritional interest of many of these species, the documented data could be used as baseline information for further investigations on nutritional contents, as they could have the potential to become valuable nutrition sources for people. These uses could help to promote the sustainable development of the area, once inappropriate gathering techniques are excluded.