An Ethnobotanical Study of Medicinal Plants in Mersin (Turkey)

This comprehensive ethnobotanical study carried out in Mersin province, which is located in the southern part of Anatolia, east of the Mediterranean Sea, compiles details on plants used in folk medicine and ethnopharmacological information obtained through face-to-face interviews. The aim was to collect and identify plants used for therapeutic purposes by local people and to record information on traditional herbal medicine. Plant specimens were collected in numerous excursions. Additionally, informant consensus factor and use value (UV) were calculated for information gathered. This study identifies 93 plant taxa belonging to 43 families and records their usage in folk medicine; 83 taxa are wild and the remaining 10 are cultivated. The most commonly used plants belong to Lamiaceae, representing 15.0% of the total, while the Rosaceae, Malvaceae, Hypericaceae, Asteraceae and Cupressaceae families each represented another 5.4%. As a result of this investigation, we determine 189 medicinal usages of 93 taxa. The UV values indicate that the most important medicine plants are Hypericum perforatum (0.80), Cedrus libani (0.78), Quercus coccifera (0.77), Arum dioscoridis (0.76) and Juniperus drupaceae (0.74). We observed that most of the drugs are prepared using the infusion method (27.6%). As a conclusion, the study finds that traditional folk medicine usage is still common, especially among the rural population of Mersin.


INTRODUCTION
The Mediterranean area, which possesses a unique ecology with various natural features, has been inhabited for millennia and is strongly influenced by human-nature relationships (Scherrer et al., 2005). The tradition of using wild plants for medicinal reasons continues in today's small rural communities, especially among societies that maintain the cultural bridge between past and present. While the recently developed fast communication technologies connect people in seconds and spread data across vast distances, traditional knowledge still holds importance in daily life. Over the past few decades, efforts to preserve traditional knowledge have escalated around the world, especially in Europe and Mediterranean countries (Varga et al., 2019).
Besides being home to many plants in floristic terms, Turkey is rich in traditional herbal medicine, in addition to its cultural, historical and geographical heritage (Bulut et al., 2013). Ethnobotanical studies show that traditional knowledge of medicinal plants still exists in the Mediterranean Region, especially among elderly (Agelet, et al., 2003). Many scientists have focused on such studies and governmental foundations have increased financial support of this kind of research. The Turkish Ministry of Agriculture and Forestry has organized studies across the country in the scope of the "Recording of Traditional Knowledge Based on Biological Diversity Project." The Taurus Mountains are one of the highlights of the Mediterranean Region with a rich plant diversity (Everest et al., 2005). Mersin has previously been the subject of this kind of scientific research, such as a study on herbal drugs on herbal markets in Mersin, which was conducted throughout the entire province (Everest et al., 2005). Thorough documentation of the traditional use of medicinal plants across the entirety of Mersin province is not presently available. Three districts (Sargın 2015;Sargın et al., 2015;Sargin and Büyükcengiz, 2019) and some specific areas of the province have been investigated from an ethnobotanical perspective. Another study investigates a small section of the region (Akaydın et al., 2013); however, as one of the largest cities in Turkey, Mersin needs further investigation from an ethnobotanical perspective.
We aim to record the traditional usage of medicinal plants by conducting an ethnobiological study in Mersin that covers various different altitudes and areas representing all ten of its districts.
To this end, we compare the gathered ethnomedicinal data with previous findings from the Balkan and Mediterranean regions. We highlight new plants and usages from the region for future phytochemical and phytopharmacological studies. With further cultivation studies, these findings may demonstrate the potential for economic development for the benefit of local communities.
Hypothesis of this study tests; a Traditional knowledge is still being used in villages far from the city and main settlement centers, b Plants are still being used in the more isolated villages.

MATERIALS AND METHODS
Mersin is a province in southwestern Anatolia, located at a latitude of 36°37′ north and a longitude of 33°35' east; covering a 15.853 km 2 area with a population of 1,814,468 (http://www.tuik.gov.tr) ( Figure 1). The majority of the acreage is mountainous (87%) and forestland is 54%. There are ten districts: Anamur, Aydincik, Bozyazi, Camliyayla, Erdemli, Gulnar, Merkez, Silifke, Mut, and Tarsus. This ethnobotanical survey includes 91 villages located in all ten districts of Mersin ( Figure 2). The territory of the province consists primarily of the high, rugged, rocky Western and Central Taurus  Lowland forest areas usually consist of Pinus brutia Ten. (Davis, 1965;Davis et al., 1988;Güner et al., 2000).

Demographic Characteristics of Respondents
As mentioned above, Mersin is one of the most populous provinces of Turkey with a population density of 114.45/km 2 . Due to the migration mobility in the region, 55,779 people moved into and 61,917 people left the city center between 2017-2018. Regarding the population growth rate, there was a notable population increase in districts close to the city center. The number of men and women living in the province is almost equal, more than half of the population are under the age of 35, 38% are 35-64 and 9% of the population are over 65. The literacy rate is 97.72 (TUIK, 2020).
The villages of Mersin province have different characteristics depending on local geographical features, such as whether they are located at high or low (near the coast) altitudes, or are near to or far from the city. There are also migrant villages and a few semi-nomadic families living in the highlands. Most of the villages in Mersin are Yoruk, alongside villages consisting of Tahtacı, Cretan and Circassian peoples. As all of the participants spoke Turkish (some elderly participants could speak Cretan and Circassian languages in addition to Turkish), we did not experience language or communication problems. Most of the remaining population of these villages is elderly. Although many of them were literate, most were at the level of primary school education.

Data Collection
This study was conducted following the guidelines for best practices in ethnopharmacological research (Heinrich et al., 2018). Ethnobotanical data were collected in face-to-face interviews (Appendix 1) conducted in Turkish with inhabitants of Mersin on several trips to the province between 2018 and 2019. Field work was carried out over a total of 71 days. Plant vouchers were collected in collaboration with the informants. We adhered to The International Society of Ethnobiology Code of Ethics in interviews (International Society of Ethnobiology Code of Ethics with 2008 additions http://ethnobiology.net/code-of-ethics/).
A total of 338 interviews were performed. Of the participants, 247 were male and 91 were female.
The informants' occupations were farmers, housewives, shepherds, mukhtar (village headmen), labourers (forestry workers) and cafe owners. Interviews were performed in various settings, such as coffee houses, gardens, houses and fields. Experienced adults, patients and local healers were the main source of information about local names, part(s) of plants used, ailments treated, therapeutic effects, methods of preparation and methods of administration. Interviews also covered adverse effects of folk medicines. Although the primary focus of our study was to collect information on the folkloric use of medicinal plants, animalbased remedies were also discussed and recorded.
Collected plants were identified according to "The Flora of Turkey and East Aegean Islands" (Davis, 1965;Davis et al., 1988;Guner et al., 2000) and "Illustrated Flora of Turkey Vol 2" (Güner et al., 2018). Voucher specimens were deposited at the Herbarium of the Faculty of Pharmacy at Marmara University (MARE) and Herbarium of Konya at Selçuk University (KNYA).

Data Analyses
Informant consensus factor (Trotter and Logan, 1986;Heinrich et al., 1988) was calculated according to the following formula: FIC Nur-Nt/Nur-1, where Nur refers to the number of citations used in each category and Nt to the number of species used. This method demonstrates the homogeneity of the information: if plants are chosen randomly or if informants do not contribute information about their use, FIC values will be close to zero. If there is a well-defined selection criterion in the community and/ or if information is given between the informants' values, the value will be close to one (Afifi and Abu-Irmaileh, 2000;Abu-Irmaileh and Afifi, 2003). Medicinal plants with higher FIC values are considered to be more likely to be effective in treating a certain disease (Teklehaymanot and Giday, 2007).
A quantitative method called "use value" (UV s ), calculated according to the formula UVs (medicinal use value) parameter using the Phillips and Gentry, 1993 formula as modified and used by Thomas et al., 2009: FIGURE 7 | Age groups of participants.  in which UV s is the use value of a given species s, U is is the number of uses of species s listed by the informant i, and ns is the total number of informants. We used the most common method of dendogram clustering to demonstrate the relationship of the taxa and traditional usages in ten different districts of Mersin. The Unweighted Pair Group Method with Arithmetic Mean (UPGMA) was used for statistical analysis with v2. (Sokal and Michener, 1958;Bailey, 1994).
The proportion and pairwise-proportion (with Holm adjustment) tests were used to compare the true (population) proportions. These tests were performed in R and the significance level was fixed at 0.05.

Demographic Features of the Informants
Details on the demographic characteristics of the participants were asked in face-to-face interviews. Among 338 participants, 16 were 19-35 years of age, 40 were 36-49, 194 were 50-70 and 88 were over the age of 70. The majority of the respondents were male (247) and 91 were female.
The occupational groups of the participants consist of farming, animal husbandry, beekeeping, shepherding, retired, tradesmen and housewives. We gained access to four local healers, who can be regarded as practitioners of traditional medicine, for this study.
It should be noted that the reason women informants constituted only one third of the total number is that the study started mostly in the coffeehouses, which were generally in the center of the villages and in Turkey are frequented only by men.

Medicinal Plants and Related Knowledge
The plants used for medicinal treatment of human beings in Mersin are listed in Table 1, while Table 2 shows the plants that see veterinary use. Both are arranged alphabetically by botanical name and include relevant information. Taxonomic changes according to The Plant List (The Plant List, 2013) are shown in parentheses with scientific names in Table 1. In total, 324 plant specimens were collected in the research area during the study period. Among these, 93 medicinal plants belonging to 43 families were identified; of these 83 taxa were wild and 10 were cultivated. The most commonly used medicinal plants were in the Lamiaceae (14 taxa), Rosaceae (5 taxa), Malvaceae (5 taxa), Hypericaceae (5 taxa), Asteraceae (5 taxa) and Cupressaceae (5 taxa) families.
The UV data is summarized in the statistical data analysis section. Amongst the most commonly used plants were Hypericum species. During our interviews, participants shared that they learned about using the oleate of Hypericum species for external wound treatment from their ancestors, emphasizing that it was even used for sword wounds in ancient times. We even observed that many of the participants' kept this oleate in their homes.
The fruit of Arum dioscoridis Sm, is the leading herb used in the treatment of haemorrhoids in the region. The leaves are boiled and consumed as food while fruits are used as toys.
We recorded that the latex of Euphorbia helioscopia L., E. kotschyana Fenzl, E. rigida M. Bieb., Glaucium flavum Crantz and Ficus carica L. are used for the treatment of warts in the region. F. carica latex is also used for toothaches.
Molasses "pekmez" prepared from the fruits of C. siliqua and J. drupaceae, which are very common in the flora of the region, was traditional product used in children and adults, especially in upper respiratory tract diseases, and was also sold in the local markets.
Female participants over 60 years of age, who contributed to our research in the region, mentioned that the roots of Malva species were previously used to terminate pregnancies when birth control methods were not common, and that their mothers frequently applied this method.
Helichrysum compactum Boiss., S. cilicica and S. congesta P. H. Davis et Hub.-Mor. are endemic species of the region with therapeutic usages (presented in Table 1). S. cilicica and S. congesta were the most consumed herbal teas in the region and are cultivated in the gardens of some participants.
Euphorbia helioscopia L., Glaucium flavum Crantz, J. foetidissima, H. perforatum, N. oleander, Mentha longifolia (L.) Hudson subsp. typhoides (Briq.) Harley var. typhoides, Punica granatum L. and Rhus coriaria L. are used in the treatment of both humans and animals. Among the medicinal plants used for veterinary purposes, we found that only Salix alba L. is used exclusively for the treatment of animals ( Table 2).
A total of 189 drugs were recorded in this study. Most were used internally (55.7%) ( Table 1, Table 2). Olive oil, flour, honey and sugar were used as additional ingredients in the preparation of these remedies.
The medicinal plants used in multiherbal recipes containing two or more species are presented in Table 3. A decoction prepared from R. coriaria and Q. coccifera is used in the treatment of warts and a mixture prepared from P. brutia and H. perforatum is used in stomach disorders.

Plant Names
Local names of medicinal plants are also recorded in this study. The names of the all plants in Turkish, as well as some Cretan plant names, were recorded during the study. Some of these plants have vernacular names that are also used for different plant species, potentially leading to complications. These are presented in Table 4, where we see that in some cases different species of the same genus have the same common names.

Statistical Data Analysis
Analysis of the diversity and similarity among districts, based on the ten districts, using species abundance and amount of information on treatment usage, was carried out by hierarchical clustering (Figure 9). The analysis resulted in five main clusters at the truncation point of 20. Erdemli, Mut, Gulnar and Silifke, which are close to one another, showed greater similarity among themselves. Similarly, Aydincik and Bozyazi, which are proximate to one another, also displayed very similar characteristics. Interestingly, there was a close similarity between Anamur and Camliyayla, despite them being far apart. Merkez and Tarsus were both different from the other districts, but Tarsus was the most distinct among the districts.
The p-value was 0.0005773 < 0.05. We conclude that there is a significant difference between the districts in terms of awareness of the species. The pairwise comparison with Holm adjustment was conducted to detect the differences between the districts. The difference between 5-3 (p value 0.044) and 5-6 (p value 0.042) are significant. This result indicates that the major source of difference was the district (Anamur). We can interpret this to mean that Anamur uses fewer species in the traditional treatments than the other districts.
The proportion test was also used to compare the true (population) UV index for the species. As a result of our analysis, the plants with the highest UV values are H. perforatum (0.80), C. libani (0.78), Q. coccifera (0.77), Arum dioscoridis (0.76) and J. drupaceae (0.74), which are presented in Table 1.
After analysis, the p-value is obtained as 0.4423 > 0.05. It is concluded that there is no significant difference between the five most commonly used species in terms of UV.

Folk Remedies and Related Knowledge Originating From Animals
This research determines that some animals, which constitute an important part of biological diversity, are used for medical purposes in addition to plants used as traditional folk medicine in Mersin. Because animal-based folk remedies are a part of traditional therapy, we present them in this study alongside plants. The folk remedies derived from animals (n 110) recorded during fieldwork via interviews with informants are presented in Table 6.
We observed that local people dealing with animal husbandry and hunting as a hobby in the area reaching from villages near the coast to the slopes of the Taurus Mountains were more knowledgeable in this regard.
We found that the use of hedgehog meat for haemorrhoid treatment is very common in the region. The participants added that it is very tasty alongside its therapeutic properties. In addition to the use of animals or animal products for human health, it is very common to use tortoize shell against the evil eye, especially among Yoruks. Furthermore, women and young girls of the village were said to knit with hair from the tails of horses when they could not find thread in Camliyayla, where needle lace is a common traditional handicraft. For this reason, the owners of white horses have to keep their horses tied up in their barns.
We were also informed that the calabash (Lagenaria sp.), known as "Kaplankabak" in the Gülnar area, is used as an instrument to make sound that keeps predators away to protect people living in tents. A piece of tanned goat skin is stretched across the calabash and a rope is inserted into a hole in  the skin. An intense noise is produced when the rope is pulled (Supplementary Video S1).
In previous studies, widely distributed species A. cilicica, C. libani, C. siliqua, H. perforatum, J. drupaceae, J. oxycedrus, L. nobilis, M. communis and O. syriacum subsp. bevanii were found to be the major plants used in traditional folk medicines. The most commonly used method for preparation in Mersin is infusion (Akaydın et al., 2013;Sargin, 2015;Sargın et al., 2015;Sargin and Büyükcengiz, 2019). Sargın et al., 2015;Sargin, 2015;Sargin and Büyükcengiz, 2019 noted that the fruits of C. siliqua and J. drupaceae in particular were used for "molasses" in the region. In addition, L. nobilis,  locally known as "teynel," is commonly used for medicinal purposes. Its leaves are used as a spice and during summer in the process of drying fruits to be eaten in winter. The plant is also commonly used in herbal soaps and sold in local markets. Our results agree with these previous findings. Sargın et al., 2015;Sargin, 2015, Sargin and Büyükcengiz, 2019 collected species belonging to the genera Dactylorhiza, Ophrys, Orchis and Serapias and noted that they were used in salep and ice cream production. Unfortunately, we were not able to collect these plants, although we also received information on their usage. We are able to contribute information not recorded previously on the widely cultivated plant Citrus lemon L. (Osbeck), which is used to make ice cream in Kaleburcu village under the leadership of the mukhtar.
Besides corroborating previous data in our study, we record new 36 plant taxa with medicinal usages in Mersin (Table 1). Furthermore, nine plants used for applications in animal health were also recorded in this study for the first time in this region.
Plants that have been recorded in previous ethnobotanical studies in Turkey and other Balkan and Mediterranean countries are also presented in Table 1,   Table 1; however, of the folk medicinal plants with veterinary uses ( Table 2), Euphorbia helioscopia, H. perforatum, N. oleander and S. alba have also been listed in other studies in the field Viegi et al., 2003).

Harmful Effects of Medicinal Plants
The harmful effects of the medicinal plants were also discussed during the interviews. The informants stated that E. elaterium and Drimia maritima (L.) Stearn should be used carefully due to side effects and contra-indications.
In addition, we recorded that the fruits of Atropa belladonna L., a medicinal plant that is not used medicinally in the region, were eaten by T. G. (age 23), who had seen his father eat this plant to quench his thirst in Inkoyu. T.G. said that he ate many fruits of this plant while he was traveling with his cousin, but his cousin only tasted it. He noted that he experienced poisoning (hallucinations, dry mouth, poor vision) in the hours after consuming the fruit and that he had to go to a hospital far from the village.
Although Turkish is spoken in all settlements in the region, some villages were established after migration events. For example, a village of Circassian immigrants has preserved their language and the elders speak Circassian among themselves. There is also a village formed by Cretan immigrants after the population exchange with Greece. The villagers speak Cretan among themselves, which allowed us to record the Cretan names of some plants during our research.
Greek plant names are recorded and transcribed in the Latin alphabet. Some of these names were included in a study conducted on the island of Lemnos .

Review of Traditional Healing With Animals
Comparing our limited data on zootherapy in the Balkans and the Mediterranean region with the study of Pieroni et al., 2011; we find that the use of donkey milk against cough is common, unlike the use of donkey urine and beeswax. Though limited, we believe these data will contribute to future studies to be conducted by the experts in this field.

Quantitative Findings
Comparing our UV values with those of other studies conducted in Mersin, we see that while C. libani was 0.64 in our study, Sargın et al., 2015 recorded a value of 0.36 for this plant. Our value for Q. coccifera was 0.77 UV, but 0.50 in the study of Akaydın et al., 2013. Another high UV value in our study was 0.87 for T. polium (0.71), which was determined to be 0.57 and 0.35, respectively, in previous studies (Akaydın et al., 2013;Sargin and Büyükcengiz, 2019). H. perforatum, which has the highest value in our study, was calculated as 0.53 in Sargın, 2015 and0.42 in Akaydın et al., 2013. FIC (ICF) values have also been investigated for Mersin in previous studies and were found to be highest for analgesics (0.78), cardiovascular diseases (0.76) and kidney problems (0.70) (Sargın et al., 2015); while another study had the highest value (0.74) for haemorrhoids, followed by gastrointestinal diseases, nutrition disorders, obesity (0.53) and cardiovascular diseases (0.51) (Sargın 2015). In a recent study the highest FIC value calculated was for the treatment category of livestock diseases (0.78), followed by analgesics (0.67) and kidney problems (0.62) (Sargin and Büyükcengiz, 2019). In another study carried out in Mersin (Akaydın et al., 2013), the FIC ratios recorded were: respiratory system (0.88), gastrointestinal diseases (0.79), dermatological disorders (0.76) and urinary disorders (0.69).
The most common usages of the plants we found were for stomach disorders, wound, haemorrhoids and colds, although the previous studies found different rates of usage (Akaydın et al., 2013;Sargin et al., 2015;Sargın 2015;Sargin and Büyükcengiz, 2019).

CONCLUSION
In this comprehensive ethnobotanical study which for the first time evaluates the entire province, we find that 93 folk medicinal plants belonging to 43 families are still being used in Mersin. Among these, the medicinal usages of 36 taxa are new records in Mersin. The usage of nine taxa in veterinary medicine are also recorded. People living in rural areas who could also benefit from modern facilities and technology, maintain a connection, which we regard as a cultural bridge in this study, to traditional knowledge in their daily lives. We also note that the younger generation living in villages more freely shared their knowledge while participating in the study. Although we can say that the transfer of traditional knowledge continues despite visual and electronic culture and the increased use of technology reaching even the most remote villages, we must also note that if this research had been carried out a few decades ago, it would have obtained more comprehensive results in terms of the use of traditional knowledge based on botanical diversity. A connection between the old and young generations that is key to the preservation of important knowledge was established during the interviews. Performing ethnobotanical studies could revitalize this bridge of knowledge between old and new generations and help form solid foundation for its preservation. As a conclusion, study also demonstrates that a historically and culturally important Frontiers in Pharmacology | www.frontiersin.org province with a rich flora such as Mersin has great potential as a source of traditional ethnobotanical knowledge.

DATA AVAILABILITY STATEMENT
The raw data supporting the conclusion of this article will be made available by the authors, without undue reservation, to any qualified researcher.

ETHICS STATEMENT
Ethical review and approval was not required for the study on human participants in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.