INTRODUCTION

Turkey has a quite rich flora with approximately 12,000 taxa.¹ Considering factors such as geographic position, topographical structure, climate, and richness of flora, forming a bridge between the east and west and hosting many civilizations and ethnic diversity, the Anatolian Peninsula is an extremely important region for folk medicines. This important knowledge, gained through trial and error for centuries and transferred from generation to generation, is also an important resource for herbal drug research. Nevertheless, this valuable knowledge is rapidly disappearing because of factors such as migration from villages to big cities, easy access to physicians and pharmacies, young people’s indifference to  folk  medicines, and industrialization and destruction of nature.^2,3,4 For the aforementioned reasons, this rapidly disappearing treasure of Turkey should be investigated and recorded by experts comprehensively.

 One of the cities that need to be studied in terms of ethnobotany in Turkey is Ankara. Despite previous investigations of the ethnobotany of some districts of Ankara, no comprehensive study was conducted in other districts. These studies, conducted in various districts of Ankara, revealed a rich ethnobotanical accumulation. For example, Şimşek et al.⁵ reported that 192 usages for 85 plant species from 31 families were recorded in 25 localities of Beypazarı, Ayaş, and Güdül districts. Sarper et al.⁶ found that 50 plant species from 18 families were used for treatment, food, and similar purposes in the Haymana district. Moreover, Elçi and Erik⁷ revealed that 23 plant species in only six localities in Güdül and Kızılcahamam districts were used for ethnobotanical purposes. Sezik et al.⁸ carried out  folk  medicine research in 28 localities with sampling method from six districts of Ankara (i.e., Yenimahalle, Kazan, Bala, Altındağ, Keçioren, and Çubuk) and stated that 47 species of 42 genera and 22 families were used as folk medicines. In the Çamlıdere district, the neighbor of Kızılcahamam, 79 plant taxa belonging to 66 genera and 33 families were used for the treatment of various disorders. Additionally, eight new  folk  medicines were included in the Turkish ethnobotanical inventory in this study.2 However, no comprehensive  folk medicine study was conducted in the Kızılcahamam district.

The Kızılcahamam district is located in the northern part of Ankara and mainly under the influence of Iran-Turan floristic area because of its location in Central Anatolia. According to taxonomic studies, the flora of Kızılcahamam is quite rich, and three floristic regions are influential in Kızılcahamam, namely, Euro-Siberian, Mediterranean, and Irano-Turanian [Eyüboğlu Ö. Kızılcahamam Soğuksu Milli Parkı’nın Florası (MSc Thesis), Ankara: Gazi University; 1991. Yıldırım A. Kocaçay Vadisi Kızılcahamam-Çeltikçi (Ankara) Arası Segetal Florası (MSc Thesis), Ankara: Gazi University; 1994]. Conversely, the district has a rich cultural heritage, as it is a transit point in Anatolia.⁹ Kızılcahamam is a remarkable study area because of its geographical location, rich biota, cultural accumulation, and significant ethnobotanical findings of neighboring districts [Eyüboğlu Ö. Kızılcahamam Soğuksu Milli Parkı’nın Florası (MSc Thesis), Ankara: Gazi University; 1991. Yıldırım A. Kocaçay Vadisi Kızılcahamam-Çeltikçi (Ankara) Arası Segetal Florası (MSc Thesis), Ankara: Gazi University; 1994. http://www.kizilcahamam.gov.tr/].⁹ To the best of our knowledge, no  folk medicine studies have covered the entire Kızılcahamam district. Thus, this study aimed to perform a comprehensive investigation of the  folk  medicine in the Kızılcahamam district.

MATERIALS AND METHODS

Research area

Kızılcahamam is one of the 24 districts of Ankara (Turkey). In history, Kızılcahamam was thought to be used as a settlement place since the Hittites and had been dominated by Phrygians, Scythians, Persians, Alexander the Great, Celts, and Roman Empire. Following the occupation by Arabs in 654, it was again dominated by Roman Empire. By the Malazgirt victory (1071), the majority of the region’s population began to be formed by Turks. In the Ottoman Empire period, the Kızılcahamam region was called “Yabanabad,” and the region was an important accommodation place that connects Asia and Europe. The first known center of the district is Demirciören village. However, in 1915, the district center moved to Şorba village and remains the center (http://www.kizilcahamam.gov.tr/).

The Kızılcahamam district, which has 105 villages, is situated in north 40.46° latitude, east 32.65° longitude (northwest of Ankara), and A4 square according to Davis’s grid system (Figure 1).¹⁰ It is surrounded by Çubuk in the East, Çamlıdere and Güdül in the West, Ayaş and Kazan in the South, and Çerkeş and Gerede in the north (Figure 1). Its distance to Ankara is 79 km, with acreage of 1712 km², and altitude of 975 m. Harami Hill (2053 m) and Işık Mountain (2030 m), which are the highest places in Ankara, are within the boundaries of the district. Given its broken and mountainous physical structure, the district has plateaus, such as Yemişen, Hıdırlar, Miyala, Salın, Eldelek, Başköy, Yıldırım, and Kırık, and several streams among these plateaus (http://www.kizilcahamam.bel.tr/2103/Cografi-Konum). Aluç, Beykaya, Yıldırım, and Kavaklı Mountains are the important mountains of the district. Kızılcahamam is quite rich in water resources, in addition to three damns (namely, Kurtboğazı, Eğrekkaya, and Akyar) that satisfy the water requirement of Ankara, and it attracts attention with an abundance of underground water resources. Kocaçay, Kirmir, and Kurtboğazı are important streams of Kızılcahamam.

The region is under the influence of continental and Black Sea climate. It is cold and snowy in winters and hot and droughty in summers. As it has many forests, it is rainy in every season. The average temperature is +11°C, and the average humidity is 66%. The highest temperature is observed in August as +34°C, while the lowest temperature is observed in February at -20°C (http://www.kizilcahamam.gov.tr/). It has a population of 32,647, and the main sources of livelihood are agriculture, livestock, apiculture, and spa tourism (http://www.tuik.gov.tr/Start.do).⁹

The Soğuksu National Park, one of the most important national parks of Turkey, is located within the borders of Kızılcahamam. As it constitutes a transition between steppe and forest zones, the Soğuksu National Park, covering 1195 hectares, has an extremely rich biota [Turan M. Fayda-Maliyet Analizi Kapsaminda Kızılcahamam Soğuksu Milli Parkı İncelemesi (MSc), Ankara: Ankara University; 2007). In a study investigating  the flora of the Soğuksu National Park, a total of 474 species from 74 families were identified, and 49 of these species were endemic. Researchers also reported that the Soğuksu National Park has the floristic elements of the Euro-Siberian and Mediterranean geographical regions. Compositae, Leguminosae, Poaceae, Lamiaceae, and Brassicaceae were the most common families. Forest vegetation mainly consists of Pinus sylvestris L., Pinus nigra J. F. Arnold, Abies nordmanniana (Steven) Spach subsp. equi-trojani (Asch. & Sint. ex Boiss.) Coode & Cullen, and Quercus pubescens Willd. [Eyüboğlu Ö. Kızılcahamam Soğuksu Milli Parkı’nın Florası (MSc Thesis), Ankara: Gazi University; 1991].

Field trips

Nine scientific field trips were organized to Kızılcahamam between April 2007 and July 2008. Generally, brief information about the aim and scope of the study was given to the local authority (called mukhtar) at each settlement area. Afterward, people that are knowledgeable about the folk remedies and elders of villages were reached through mukhtars. Face-to-face interviews were conducted in a suitable setting with 57 people by using open and semi-structured questionnaires. Data obtained during the interviews were recorded. General questions (local name of medicinal plants, used parts, purpose of usage, preparation and application method, source of information, etc.) were asked. After each interview, the plants that used as folk medicines were  found for in the field under the guidance of the informants. Subsequently, plant samples were taken and appropriately prepared as herbarium materials. To increase the accuracy in identification, flowering or fruiting plants were collected. Therefore, scientific trips were organized to the region between April and July to coincide with the flowering or fruiting period. Plant specimens were identified by Prof. Dr. Galip Akaydın, through Davis’s “Flora of Turkey and the East Aegean Islands,”^1,10,11 and the Latin names of identified plant species were updated according to The Plant List (http://www.theplantlist.org/, revision date: 23.02.2021), while the endemism status were checked from “Türkiye Bitkileri Listesi”¹² After botanical identification, plant specimens were preserved in Gazi University Faculty of Pharmacy Herbarium (GUEF). Visited locations are shown in Figure 1.

Statistical analysis

Initially, the distribution of  folk medicines among 11 pharmacological categories was determined. Subsequently, the informant consensus factor (FIC), use value (UV), and cultural importance index (CI) were calculated using previously described formulas.² High FIC degrees (close to 1) correlate with the consent for the use of folk medicine in specific situations by the informant, while the high UV and CI signifies the importance of a plant and high frequency of declaration.^13,14,15,16

RESULTS

Kızılcahamam folk remedies have not been investigated in detail previously. Thus, the ones that are still not forgotten in  the folk medicine accumulation of the district were determined and recorded by field studies. During our research, nine field trips were organized to the district, and 51 localities were visited (Figure 1). After the study, people knowledgeable about folk  medicine could be reached in 30 of these locations, while there were no knowledgeable people in the other 21 locations. After the identification of plant specimens, 65 species (69 taxa) from 58 genera and 31 families were  determined to be used as  folk medicines. While seven of the species used as folk medicines in the district were cultivated plants, the rest were wild. The plants used as folk medicine in Kızılcahamam are compiled together and presented in Table 1. In this table, the Latin names of the medicinal plants are given alphabetically (by family and species name) with other relevant data (GUEF numbers, local names, purpose of usages, preparation, and administration methods).

Table 1 shows that Compositae (13 genera, 12 species, and 13 taxa), Lamiaceae (6 genera, 9 species, and 10 taxa), and Rosaceae (7 genera, 9 species, and 9 taxa) are the most commonly referred families in Kızılcahamam as  folk  medicines (Figure 2). In addition, the most cited plant species are Malva neglecta, Urtica dioica, Pinus nigra subsp. pallasiana, Pinus sylvestris, and Rosa canina (with UV values of 0.29, 0.28, 0.21, 0.17, and 0.17, respectively). Some differences were noted in this order according to the CI, Urtica dioica at the first place (CI: 0.98), Malva neglecta and Rosa canina at the second place (CI: 0.43), and Cota tinctoria and Viscum album at the third rank (CI: 0.35) (Table 1).

Folk medicines are generally used after certain preparation methods in the area, while only 32% of them are used directly. For example, half of the folk medicines used internally are prepared as tea (33.9% decoction and 16.7% infusion) in Kızılcahamam. Some of the internally used folk remedies were prepared as meals (e.g., Beta lomatogona and Malva neglecta), jam (e.g., Rosa canina), or poultice (e.g., Malva neglecta and Quercus robur) before use. Interesting uses such as intrauterine administration of Malva neglecta for women’s infertility were also noted (Table 1). Regarding forms of administration, folk medicines were generally used orally (83.4%) (Table 2).

Folk remedies identified in Kızılcahamam are generally monocomponent and process in a simple preparation. The most preferred plant parts in Kızılcahamam folk medicine are aerial parts, leaf, and fruit. However, inflorescence (e.g., Tilia rubra subsp. caucasica), fresh shoot (e.g., Pinus nigra subsp. pallasiana), phloem (the tissue that appears after peeling the peridem tissue of Pinus sylvestris stem), and whole plant (e.g., Viscum album) are the least used parts (Figure 3).

During the field studies, diseases that local people tried to treat with folk remedies were classified into 11 groups (Table 3). The distribution of folk medicines according to pharmacological categories in Kızılcahamam is as follows: Respiratory system disorders, 18 medicines and 47 citations; gastrointestinal problems, 28 medicines and 44 citations, and urinary tract problems, 17 medicines and 29 citations (Table 3). Shortness of breath is the most referenced respiratory system disorder that is treated by folk medicines, while hemorrhoid and prostate disorders are illnesses that are attempted to be cured by folk medicines among gastrointestinal system and urinary tract problems. However, this order changes when FIC values are considered; dental diseases have the highest FIC value (1.00), followed by skeletomuscular system disorders (0.69) and respiratory system disorders (0.63) that ranked second and third, respectively. FIC is accepted as being the degree of agreement among the people interviewed concerning the use of a given taxon.¹⁴ Thus, differences according to citation and FIC value were thought to be based on the disagreement among informants and the use of the same folk medicine for very different purposes. Dental disorders have the highest FIC value because of the citation of the same plant twice for dental illness, rather than being popular.

During our field study, a mushroom (Morchella sp.) was used for ethnobotanical purposes. It was named as “Kuzugöbeği, ayı mantarı” among local people and used for knee pain, inducing sleep, sedation, and foodstuff by cooking as meal. As it is a member of Kingdom Fungi, it was not listed in the table with other plant-sourced medicines.

DISCUSSION

The result of field studies conducted in the Kızılcahamam district provided important contributions to Turkish Folk Medicine literature. To the best of our knowledge, folk medicinal usage of Beta lomatogona, Ballota larendana, Tripleurospermum elongatum, and Verbascum insulare are recorded firstly within this research in Turkey (Table 1). In addition, four endemic plants, namely, Arum euxinum, Ballota larendana, Sideritis germanicopolitana, and Verbascum insulare, were used as folk remedies in the district.

Folk medicines used in Kızılcahamam have similar usages  in different parts of Turkey. The similarity is quite high with Çamlıdere, a border neighboring district of Kızılcahamam. Moreover, 27 of the 69 taxa used as folk medicines in Kızılcahamam have similar uses in Çamlıdere. For example, Cota tinctoria (urinary tract inflammation), Juglans regia (diabetes), Viscum album (shortness of breath and urinary tract disorders), Malva neglecta (hemorrhoid and rheumatism), Cydonia oblonga (shortness of breath, bronchitis, and cough), Prunus spinosa (diabetes) are used for same conditions in both districts. The utilization of Salix alba is an interesting example of this similarity, as the ash obtained from its root or leaf is applied to the head for the treatment of headache.² In Güdül, another border neighboring district of Ankara, Paliurus spina-christi was used for kidney stone similar to its use in Kızılcahamam.⁷ Similar utilizations were also discovered with other remote districts of Ankara. For example, Malva neglecta, one of the most cited plants in our study area, is used for the treatment of hemorrhoids in Haymana and Beypazarı districts as in Kızılcahamam.^5,6 Taraxacum scaturiginosum was used for diabetes (or hyperglycemia) in both Beypazarı and Kızılcahamam districts.⁵ Echium italicum, Thymus leucostomus, and Sorbus domestica were used with the same purposes in different districts of Ankara.⁵ Similarities were observed with different provinces as well; for example, Crataegus orientalis is utilized for hypertension or hyperglycemia in different parts of Anatolia (e.g., Ağrı, Manisa) as in Kızılcahamam.^17,18,19 Plantago major is used for the treatment of abscess in almost every part of Turkey as in Kızılcahamam.^{4,5,6,17,19,20,21,22,23} Furthermore, Ajuga chamaepitys subsp. chia, Morus nigra, Centaurea solstitialis, Echium italicum, and Sanguisorba minor were used in different provinces similarly as determined in our study area.^{4,19,20,23,24,25,26} Similar usages in nearby districts/provinces are already expected. Having similar flora and the ease of idea exchange could be the reasons for this situation. The similar use of folk  medicines at different locations may be considered an indication of the accuracy of the identified  folk medicinal knowledge. Besides, domestic migration, development of communication, and transport facilities may contribute to the dissemination of information to remote areas.

Conversely, different species of some genera used in Kızılcahamam were detected to have similar usages in different parts of Turkey. When the border neighboring districts were examined, interesting similar utilizations were encountered; one of them is Tripleurospermum callosum (Boiss. & Heldr.) E. Hossain used for bronchitis in Çamlıdere, similar to Tripleurospermum elongatum. Similarities in the usage between Prunus avium (L.) L. and Prunus cerasus (diabetes and hyperglycemia), and between Juniperus oxycedrus L. and Juniperus communis var. saxatilis (for eczema) are among other examples.² Similarly, in Güdül, Rumex tuberosus L. is used for hyperglycemia just as Rumex crispus is used in Kızılcahamam.⁷ Similar usages were also observed in remote districts of Ankara, such as between Onopordum turcicum and Onopordum acanthium L., and between Salix alba and Salix babylonica, which were used in Haymana.⁶ The same situation applies for other provinces  of Turkey: Some different Hypericum species (e.g., Hypericum polyphyllum Boiss. & Balansa and Hypericum empetrifolium Willd.) are utilized for the treatment of stomach disorders in Ağrı and Muğla, as in Kızılcahamam.^17,27 Arum species are other examples. The root of Arum euxinum is used for hemorrhoid treatment in Kızılcahamam, and different Arum species (e.g., Arum balansanum R. R. Mill. and Arum italicum Mill.) are also used for the same purpose in different regions of Anatolia.^4,28,29 This may result from local people’s assumption that different species of a genus are the same because of morphological similarities. Moreover, different species of a genus are likely to show phytochemical similarity. Thus, based on the information obtained from different regions by information exchange, people may have tried to prepare the same medicine with morphologically similar plants that are grown nearby, seen the same effect, and continued to use them.

Contrary to the abovementioned similarities, quite different usages for the same species were also determined in different parts of Ankara. These differences were observed even in border neighboring districts; for instance, Cirsium arvense is used for urinary tract and prostate disorders in Kızılcahamam, while it is used for shortness of breath in Çamlıdere. Sinapis arvensis is used for kidney stones in our research area, but it is recommended for shortness of breath in Çamlıdere.² Another example is Crataegus orientalis, which is used for diarrhea, stomach disorders, hypertension, and hyperglycemia. Unlike the usages detected in Kızılcahamam, this plant is used for shortness of breath and heart disorders in the Güdül district.⁷ Arctium minus, Cichorium intybus, and Sinapis arvensis are other examples, which were used for different purposes in different districts of Ankara.⁸

The Anatolian Peninsula has hosted quite different cultures throughout history, and this situation has been inevitably reflected in folk medicinal knowledge. Communities, migrating from different regions throughout history, have blended their  folk medicinal knowledge, which was obtained in the region where they came from, with local folk medicine knowledge. Therefore, the usage of the same plant as a folk remedy may vary by region.

Folk medicines are mostly cited for the treatment of gastrointestinal system disorders (especially hemorrhoid and stomach ache), respiratory (especially shortness of breath, asthma, and common colds), and urogenital system problems (especially, prostate disorders) in Kızılcahamam. Considering these results, the aforementioned disorders could be considered the most common health problems in the study area.

When the cited folk medicines are examined, some plants attract attention with their usage in the treatment of disorders which could be hardly noticed by common people. For example, Cirsium arvense, Citrullus lanatus, Malva neglecta, Tripleurospermum elongatum, Urtica dioica, and Viscum album are used for the treatment of prostate disorders, but the recognition of this disorder and use of folk medicine for its treatment are interesting. Likewise, informants expressed that they use various  folk medicines to treat some illnesses, such as cancer (Arum euxinum, Urtica dioica, and Portulaca oleracea), hypercholesterolemia (Juglans regia), hyperglycemia (Prunus spinosa, Rosa canina, and Juglans regia), goiter (Juglans regia), and vascular occlusion (Cyanus depressus). Recently, these disorders are becoming increasingly widespread. In addition, at present, reaching a physician has become quite easy. Hence, these situations suggest that people start to search for solutions by themselves after being diagnosed by physicians. Moreover, this information could be obtained from various sources. Nevertheless, interviewees indicated that they learned these uses from their ancestors. Therefore, the mentioned usages were included in the present work. In addition, there may be some uses that may result from information pollution obtained from books, television, newspaper, etc., such as the use of Citrullus lanatus against prostate disorders. It is rich in lycopene³⁰ that reduces the risk of prostate disorders.³¹ Methanol extract of seeds were demonstrated to cause a significant reduction in the size of the enlarged prostate.³² However, this usage could be interpreted as a result of information pollution of  folk medicine knowledge.

Some interesting folk remedies were encountered in the study area. For example, the phloem of Pinus sylvestris is consumed with honey as treatment of stomachache, or the knee is bitten by green thin hornets for the treatment of knee pain and rheumatism. Echium italicum is used for wound healing in Kızılcahamam, and according to previous bioactivity research, the ethanol extract of Echium italicum root increased wound tensile strength by 37%.³³ Similarly, Hypericum perforatum, Phlomis sp., Malva neglecta, and Rosa canina are used as folk medicines in peptic ulcer symptoms, and in the literature, these plants have a strong in vivo anti-ulcerogenic effect.^34,35,36 In addition, Pinus nigra subsp. pallasiana and Pinus sylvestris are interestingly used for removing foreign objects from the skin. When their resins were applied to the affected area, foreign materials such as splinters could be removed. The usage of Cota tinctoria for weight loss is also interesting. To the best of our knowledge, no study has examined this effect. The investigation of the mentioned effect of Cota tinctoria can be a new research topic. It is possible  to increase the number of these examples. This situation is a good example to unroll the possible high potential of folk medicines as the starting point for new drug discovery.

Conversely, Onopordum turcicum flower is used against hyperglycemia in the research area. In our previous study, this plant species was used to treat diabetes in Çamlıdere, a neighboring district, and local names of this plant are very similar in both districts (called as “galgan” in Kızılcahamam and “Kalkan” in Çamlıdere).² The usage of the same folk medicines for the same purposes in two neighboring regions increases the reliability of the data obtained in this study.

In Kızılcahamam, folk medicines are generally preferred if prepared from a single plant species; only 17 of 69 taxa are included in the mixtures. These mixtures are usually prepared as decoction/infusion (e.g., Cota tinctoria, Cydonia oblonga, and Rosa canina), but there are some ointment (e.g., Echium italicum) or poultice (e.g.,  Malva neglecta) formulations, as well. These results are consistent with the folk medicine data previously obtained in Turkey because folk remedies are generally prepared as simple formulations and used as a single component.

In this study, although investigations aimed at folk remedies, other ethnobotanical usages of plants rather than their usage in folk medicine were also detected and recorded on the field. For example, Achillea sp. is used as perfume  by  applied on hands; Arum euxinum, Morchella sp., Polygonum cognatum, Rumex scutatus, Thymus longicaulis subsp. chaubardii, and Urtica dioica are used as foodstuff, and Verbascum insulare is used for fishing.

As a result of interviews, the majority of informants in the research area preferred to use modern medicine for the treatment of their illnesses; by contrast, some of the informants expressed that they do not want to use modern medicines because of their side effects, so they try treating illnesses with herbal remedies. However, people who know about folk medicines are limited; in 51 villages, no knowledgeable people or folk medicine users were found in 21 villages (41% of visited locations). However, if this survey was conducted 20 years ago, ethnobotanical information could probably be obtained from all villages. This situation is a very important indicator of the loss of ethnobotanical knowledge owing to modern life.

CONCLUSION

To the best of our knowledge, this is the first study to explore folk medicines in the Kızılcahamam district. This study provided important contributions to the inventory of Turkish Folk Medicines. This study also highlights the rapid disappearance of folk medicine knowledge and urgent need for recording it in all parts of Turkey. Folk remedies are important resources, as they provide advantages on modern drug research. They could be considered as sources that have been shown to be effective on humans and tested for toxicity because they have been used for centuries, and useless or toxic ones were discarded throughout history. In previous bioactivity studies based on folk medicines conducted by our research group, many herbs used as folk remedies in different regions of Anatolia have been shown to be effective against the mentioned bioactivities in vivo.^{34,35,37,38,39,40} Many drugs have been developed based on their traditional use worldwide; aspirin (Salix sp.), artemisinin (Artemisia annua L.), galantamine (Galanthus woronowii Losinsk.) are some examples of compounds developed from plants that were used traditionally.^41,42,43 Besides recording new folk medicines to the ethnobotanical heritage of Turkey, this study is a valuable source of data for future bioactivity studies and discovery of new drug candidate molecules.

Conflict of interest: No conflict of interest was declared by the authors. The authors alone are responsible for the content and writing of the paper.