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Article

Ethnobotanical and Ethnopharmacological Study in the Bulgarian Mountain Rhodopes: Part II—Contemporary Use of Medicinal Plants

by
Irena Mincheva
1,*,
Zheko Naychov
2,
Cristo Radev
3,
Ina Aneva
1,
Luca Rastrelli
4,
Maria Kamusheva
5,
Nikolay Nikolov
6 and
Ekaterina Kozuharova
7,*
1
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1000 Sofia, Bulgaria
2
University Hospital Lozenets, Department of Surgery, Sofia University St. Kliment Ohridski, 1407 Sofia, Bulgaria
3
Freelancer in Computer Sciences and Information Technologies, 4023 Plovdiv, Bulgaria
4
Department of Pharmacy, University of Salerno, 84084 Fisciano, Italy
5
Department of Organization and Economics of Pharmacy, Faculty of Pharmacy, Medical University of Sofia, 1000 Sofia, Bulgaria
6
St. James’s Hospital, Department of Anaesthesia, Intensive Care and Pain Medicine, Anesthesiology and Intensive Care Medicine, James’s Street, D08 NHY1 Dublin 8, Ireland
7
Department of Pharmacognosy, Faculty of Pharmacy, Medical University, 1000 Sofia, Bulgaria
*
Authors to whom correspondence should be addressed.
Diversity 2023, 15(4), 482; https://doi.org/10.3390/d15040482
Submission received: 22 December 2022 / Revised: 30 January 2023 / Accepted: 16 March 2023 / Published: 24 March 2023
(This article belongs to the Special Issue Ethnobotany, Medicinal Plants and Biodiversity Conservation: 2nd Edition)
Browse Figures
Versions Notes

Abstract

:
Rhodopes Mountain is ethnobotanically poorly studied, but our preliminary observation in a number of settlements revealed that even nowadays, the local population relies solely on previously collected medicinal plants. We aimed to assess the contemporary use of medicinal plants in the Central and East Rhodopes and the health conditions that local communities address with them. The ethnobotanical field data were collected through an in-depth method in combination with semi-structured face-to-face interviews, adapted with modifications to the objectives of this study. The following quantitative ethnobotanical indices were used in this study: informant consensus factor (ICF), fidelity level (FL), and Jaccard similarity coefficient or Jaccard index (JI). Data analyses from our field research showed that 92 informants mentioned the utilization of a total of 114 plant species. The results of this study reveal that in both regions of the Rhodopes, medicinal plants are mentioned most often in relation to diseases affecting nervous, respiratory, digestive, and cardiovascular systems, followed by reproductive, urinary, immune, and musculoskeletal. The risk of disruption or loss of traditional knowledge of medicinal plants is expected in the condition of cultural globalization. However, there is no metrified data about the use of medicinal plants in the Rhodopes from the past. The application of statistical indices in this research will make such assessment and monitoring possible in the future.

Graphical Abstract

1. Introduction

Studies during the last decades show that in Bulgaria [1,2,3,4,5,6,7,8,9,10,11], as well as in other Balkan countries [12,13,14,15,16,17,18,19,20,21], the traditional application of wild plant species by local people for medical purposes is well preserved and vivid. Such traditional application of medicinal plants for various health conditions is documented in Turkey [22,23,24,25,26,27,28,29,30]. This wide use of medicinal plants in remote areas could be explained by the limited access to medical care and pharmaceutical services [27]. The lack of pharmacies in some distant regions is identified as a main problem, especially in Bulgaria, which stimulates the traditional use of plants to treat and prevent disease [31,32]. A Greek study highlights that despite the access of locals to modern therapies, herbal remedies are still applied by many people for treatment. Herbal remedies represent an alternative to pharmacological treatment due to their availability, affordability, lower costs, and a lower rate of adverse reactions [33,34,35,36]. The high price of modern medicines, limited patient access to conventional medicines, and the disillusion of some people in modern healthcare make natural medications a preferable option to the extent of even satisfying unmet medical needs [37,38,39,40,41,42]. The wide application of local flora is also a crucial factor for the preservation of cultural specifics and knowledge about medicinal plants.
The Rhodope Mountains territory has been poorly studied and remained so far out of the ethnobotanical research scope [1,2,3,4,5,6,7,8,9,10,11]. One valuable study of this area collected and evaluated data on non-timber forest resources (medicinal plants, mushrooms) and their cultural and economic importance, as well as the dynamics of their consumption against a backdrop of recent changes in the Bulgarian economy [43]. In this study, residents of the Municipality of Garmen (Western Rhodopes) were surveyed, and some were interviewed. A great deal of information was obtained about the history, geography, and demographic composition of this area and the nation in general during this period of economic upheaval. Moreover, a high degree of authenticity was conserved with respect to the traditional methods of medicinal plant use due to the relative isolation of the area. Despite the relative geographical uniformity of the study area, significant phyto-climatic and ecological differences were also found therein [44,45].
The Rhodope Mountains are ideal for conducting ethnobotanical field research. There are several advantages to studying Mountain Rhodope’s traditional use of medicinal plants. From our preliminary observations in remote villages, we found that even today, the population relies exclusively on the medicinal plants collected during the summer. This is particularly valid in winter when the thick snow cover cuts off the communities from remote villages of the Municipality of Smolyan from pharmacy store access for a few days. At the same time, a study shows that the average lifespan of respondents conducted with long-living people and centenarians in the Municipality of Smolyan is 93.7 [46]. Additionally, considerable authenticity is retained about the traditional methods of medicinal plant use because the population of the area is relatively isolated. The biodiversity of plants and habitats is well preserved [44,45].
One fundamental challenge with such kinds of studies is the discrepancy between the perceived diagnosis and what would have been diagnosed provided the patient was diagnosed by an institutional doctor. Traditional healers do not possess expertise in human physiology in the way we understand it, i.e., they operate with different interpretations of the human body. We do not have much doubt about obvious conditions such as wounds, hemorroides, or bites of venomous creatures. However, most of the traditional cures are centered around symptoms which, from the point of view of modern institutional medicine, may have very different causes and would be treated in very different ways. For example, traditional Bulgarian healers from the distant past seemed to express no clear distinction between the heart and stomach. In fact, what they call “heart pain” seems to have been a stomach ache [47]. In other situations, the modern diagnosis was too recently established. A traditional healer could not possibly have a concept about a condition such as arterial hypertension because no traditional method of measuring blood pressure existed. Thus, most of the “diagnoses” are, in fact, symptoms. By means of careful research and critical evaluation, these traditional practices can provide us with valuable insight into the properties of medicinal plants.
Fortunately, ethnobotanical research has provided quantitative indices, such as use value (UV), which quantitatively presents the relative importance of the plant species used for medicinal purposes. The fidelity level (FL) is defined as the percentage of informants who mentioned the uses of certain plant species to treat a particular disease, or points to the most popular plants. Another quantitative index is the informant consensus factor (ICF) used to measure the knowledge exchange among informants [17,48,49,50,51]. They facilitate comparison of the results obtained, And this reveals the most popular medicinal plants. For instance, in the region of Suva Planina in South-Eastern Serbia, G. cruciate, which is a relatively popular plant (UV = 0.227), has the highest number of phytotherapeutic uses (14), but G. lutea is among the most popular plants (UV = 1) together with Achillea millefolium, Hypericum perforatum, Juglans regia, Matricaria chamomilla, Mentha piperita, Plantago lanceolata, Plantago major, and Salvia officinalis [17].
We aimed to assess the contemporary use of medicinal plants in the Central and East Rhodopes and the health conditions that local communities address with them. For that purpose we applied statistical methods such as the informant consensus factor (ICF), fidelity level (Fl), and Jaccard similarity coefficient or Jaccard index (JI). This study is the second part of a more complex ethnopharmacological and ethnobotanical research project conducted among the rural population of the Rhodope Mts. The first part of the research focused on the diversity of medicinal plants evaluated by the quantitative ethnobotanical index use value (UV), and it showed that 92 informants mentioned the utilization of a total of 114 plant species belonging to 52 families and 110 genera. The most common plants were from the families Asteraceae (16.7%), Lamiaceae (12.3%), Rosaceae (9.6%), and Amrillydaceae (3.5%), followed by Crassulaceae, Plantaginacea, Oleaceae, and Solanaceae. The data presented in six nomograms revealed the most popular plants, the way of application, the corresponding medical indications in Central and East Rhodopes, and the differences between the two sub-regions [52]. The emphasis in this second part of the study falls on the diseases and organ systems treated with medicinal plants nowadays following traditional knowledge.

2. Materials and Methods

2.1. Study Sites, Data Collection, and Pre-Processing

This ethnobotanical survey was conducted among 29 settlements from 7 municipalities in the Rhodopes (Figure 1, details are presented in the previous publication of ours [52], located in the territory of four administrative districts (Plovdiv, Smolyan, Kardzhali, and Haskovo), namely in Central Rhodopes, 12 settlements (11 villages and 1 city) and in East Rhodopes, 16 settlements (13 villages and 3 cities). The settlements of the study were selected to fit into the two floristic sub-regions of the Rhodopes, Central (700–1000 m) and East (altitude 0–500 m) [52].
Residents of the Rhodope Mountains of age over 18 years were interviewed after prior consent was obtained. Ethnobotanical information on medicinal plants was collected among 92 informants, and their socio-demographic characteristics are described in detail in the first part of this research [52]. The informants were selected according to the “snowball” method: the first informant in the village is randomly appointed, and the following ones are recruited on the basis of information and contacts provided by the first informant. The “snowball” technique provides an opportunity to study the lifestyles and attitudes of hard-to-reach groups of society, which usually stay aside from sociological studies. The ethnobotanical field data were collected through an in-depth method in combination with a semi-structured face-to-face interview, adapted with modifications to the objectives of this study. The semi-structured interview has a lower degree of structuring, which provides a higher intensity of communication with the informants. This way of information gathering allows us to examine the specifics and diversity of the context to which the information relates in detail. The in-depth interview had a drilling, expert character and was conducted in preparation for a quantitative, representative study. The interview followed a set of questions tested in previous field studies. The questionnaire pointed to broad organ- and therapy-based use categories but was generally based on the International Classification of Diseases of the World Health Organization (WHO, 2018). Diseases, symptoms, or conditions reported by informants were as follows: abscess, warts, skin inflammation, wounds, vision, ear pain, gastritis, ulcer, diarrhoea, biliary inflammation, jaundice, vomiting, headache, relaxing, cough, sinusitis, low stamina, diabetes, anaemia, high blood pressure, “blood purification”, anticoagulant, varicose veins, cardiac diseases, haemorrhoids, cancer, breast cancer, cervical cancer, low back pain, joint pain, trauma, abortion, childlessness, “women’s diseases”, mastitis, potency (sexual), hormonal imbalance, renal diseases, enuresis, prostatic adenoma, cystitis, fever, cold, toothache, hair strengthening, hernia, etc.
The questions used in the interviews were of the type: disease/condition–plant used. These are so-called “open-ended” questions with no fixed answers. This allows the informants to prioritize the important plant species for him/her. The diseases were named in a way that was understandable by the informants. For example, “What used to treat high blood pressure?” instead of “What used to treat arterial hypertension?”. Informants were asked about the source of knowledge, and only authentic use of medicinal plants was recorded. The data were organized in spreadsheets (Microsoft Excel, 14.0. 7261.5000, 2010). Details are presented in our previous publication [52].

2.2. Analysis of Ethnobotanical Data

The nomograms of plants used for medicinal purposes (both therapeutic and prophylactic) in the Central and East Rhodopes contain processed field data from the ethnobotanical survey. They are presented in their full version in the previous first part study published earlier [52]. Field data were analyzed by calculating ethnobotanical indices for each of the study areas. Ethnobotanical indices (or factors) are increasingly used in ethnobotany as they allow in-depth analysis and ensure comparability of the results.

Data Processing

The research questions we aimed to answer were: What is the relative importance of the plant species used for medicinal purposes? What are the most popular plants used to treat a particular disease? What is the degree of agreement among the informant’s knowledge? The following quantitative ethnobotanical indices were used in this study: use value (UV), informant consensus factor (ICF), fidelity level (FL), and Jaccard similarity coefficient or Jaccard index (JI).
The index use value (UV) is a quantitative characteristic of the relative importance of the plant species that the informant community knows and uses [53]. This value is calculated using the following formula:
UV = ΣU/n,
where: U is the number of references to a particular plant species; n is the total number of informants.
In the case of many references to the utilization of a plant, the UV index is high. It tends to zero when there are few references. UV does not differentiate, however, whether the plant is used for one or more than one disease [54,55].
The other index applied to analyze the collected information is the fidelity level (FL) [56]. The methodology developed by Bhatia and co-authors [55] and Heinrich and co-authors [56] is used to specify the most popular plants for the treatment of certain diseases, classified in organ-system categories.
The informant consensus factor (ICF) is a quantitative analytical parameter to evaluate the degree of agreement among the informant’s knowledge. It is calculated through the following formula:
ICF = (nur − nt)/(nur − 1),
where: nur is the total number of use reports for each disease cluster; nt is the total number of species used for that cluster.
The ICF values are close to zero when there is so-called low homogeneity, i.e., the plants are reported randomly, or no exchange of information for their usage among the community exists. Its values are equal or close to 1 when there is a well-defined selection criterion for a given plant species in the community and/or informants share knowledge among themselves [57,58].
Usually, more than one plant species is mentioned for a particular disease. Hence, the confidence level index FL is presented in percentages [59]. Through the fidelity level (Fl), the preferred plant species for the treatment of a given disease are identified [54]. Before calculating the FL, all diseases mentioned by the informants are grouped into several categories. FL is calculated for each category using the following formula:
FL [%] = Np × 100/N,
where: Np is the total number of reports for each medicinal plant for a specific disease; N is the total number of diseases reported for a specific medicinal plant.
A high value for FL is possible for those species whose reports are for the same disease category, while low values are found in the case of species used for more than 1 disease [54].
The Jaccard similarity coefficient or Jaccard index (JI) is used when the level of similarity between two groups of elements should be identified [60]. JI is calculated using the following formula:
JI [%] = NAB × 100/(NA + NB − NAB),
where: NA is the number of elements in group A; NB is the number of elements in group B; NAB is the number of elements available in both groups.
This formula could be used to identify the similarity between the species identified in both analyzed regions: Central and East Rodopes. Thus, the following modified formula is applied:
JI [%] = NAB × 100/(NA′ + NB′ + NAB),
where: NA′ = NA − NAB is the number of species identified only in region A; NB′ = NB − NAB is the number of species identified only in region B; NAB is the number of species identified in both regions.

3. Results

Informants in the surveyed settlements in the Central Rhodopes reported the utilization of 114 plant taxa in relation to human health (for treatment and/or prophylactics). Additionally, some plants were mentioned for veterinary applications. Most plants were common species with wide distribution. Others were cultivated in the informants’ kitchen gardens. Attention during the interview process was paid to some rare plants such as “salep” orchids, Haberlea rhodopensis Friv., and Lilium rhodopaeum Delip. (Table 1), but the informants responded that they did not use them.

3.1. Central Rhodopes

3.1.1. Relative Importance of the Plant Species Used for Medicinal Purposes

Informants mentioned the use of 91 plant species for human medicine in Central Rhodopes. UV values in Central Rhodopes ranged from 0.02 to 0.67, regarding those with the highest degree of use. The most frequently mentioned were Plantago major L. (0.67), Sambucus nigra L. (0.60), Hypericum perforatum L. (0.46), Thymus spp. (0.46), Sempervivum tectorum L. (0.42), Teucrium chamaedrys L. (0.40), Tussilago farfara L. (0.33), Achillea millefolium L. (0.31), and Origanum vulgare L. subsp. vulgare (0.29) (Table 1, Details [52]: Figures 8 and S1).

3.1.2. Disease Categories Treated with Medicinal Plants

In order to ascertain the conditions for which the plant species are applied, all mentions by the informants for human-medical application were segregated into nine categories of diseases. The higher number of mentions in a category indicated its importance to the informants. The number of mentions ranged from 28 to 125 (Figure 2). The diseases with the highest number of ΣU mentions were those affecting the nervous (125), respiratory (112), and digestive (102) systems. The number of reports for diseases of the cardiovascular system (44) was significantly lower.

3.1.3. Degree of Agreement among Informant’s Knowledge

ICF values in most categories exceeded 0.50, indicating a relatively high similarity of the mentioned species in the respective category. The exception is the category ‘other’ with an ICF value equal to 0.33. Categories with a high informant consensus factor were diseases affecting digestive (0.74), nervous (0.72), and respiratory (0.70) systems. In the nervous system diseases category, 125 mentions of 9 plant species provided an ICF value of 0.72, while the digestive system diseases category had a similar index value (0.74), indicating high homogeneity despite mentions (102) of a larger number of plant species (27). The ICF score for the respiratory system diseases category was similar, with a relatively high degree of homogeneity (0.70) using a large number of plant species (26). The results further confirmed the importance of the disease categories considered in the study area (Table 2).

3.1.4. Most Popular Plants for Treatment of Certain Diseases

The fidelity level (FL) by disease categories in the Central Rhodopes is presented in Table 3. Five plant species had an FL level equal to 100%: Mentha spicata L. (against vomiting) and Cichorium intybus L. (for gallbladder inflammation), Tussilago farfara (affecting cough), Geranium macrorrhizum L. (affecting high blood pressure), and Sambucus ebulus L. (for increasing immunity). High values of the level of reliability in the digestive system category also referred to Teucrium chamaedrys (94.7% for influencing gastritis and diarrhoea), Centaurium erythraea Rafn. (83.3% for influencing gastritis and ulcer), and Agrimonia eupatoria L. (75% for influencing gastritis, ulcer, diarrhea, and gallbladder inflammation), and Tilia cordata Mill. (83.3%) in the respiratory system category (83.3% for influencing cough). Four plant taxa were used in more than one disease category in the Central Rhodopes: Sambucus nigra, Thymus spp., and Achillea millefolium, Primula veris L. (Table 3).

3.2. East Rhodopes

3.2.1. Relative Importance of the Plant Species used for Medicinal Purposes

Informants mentioned the use of 68 plant species for human medicine in East Rhodopes. Cotinus coggygria Scop. (0.42), Teucrium polium L. (0.26), Sambucus nigra (0.23), Chelidonium majus L. (0.21), Matricaria chamomilla L. (0.21), Paliurus spina-christi Mill. (0.21), Plantago major (0.19), and Urtica spp. (0.19) had the highest UV values. The lower values of popular plant species in the East Rhodopes were due to the lower total number (68) of species mentioned in this area compared with the total number (91) of species mentioned in Central Rhodopes (Table 1) [52]: Supplementary Figures S1 and S2.

3.2.2. Disease Categories Treated with Medicinal Plants

Figure 3 presents the diseases categories in the East Rhodopes, according to the number of mentions ΣU. Application of medicinal plants to treat diseases affecting the nervous (59), respiratory (48), digestive (38), cardiovascular (35), genital (29), and musculoskeletal (20) systems are with the highest number of mentions, respectively, with greater importance for informants in the East Rhodopes (Figure 3).

3.2.3. Degree of Agreement among Informant’s Knowledge

Table 4 shows the ICF values for the East Rhodopes. The values range from 0 (in the nervous system diseases category) to 0.59 (digestive system diseases). The highest value was in the digestive system category (0.59). Other important categories with high informants’ consensus factors were diseases of the immune system (0.56), respiratory system (0.53), cardiovascular system (0.47), and musculoskeletal system (0.47). The diseases with a high number of mentioned species, and therefore, with higher importance on diseases for the informants from the East Rhodopes, were cardiovascular (19 plant species and 35 mentions), respiratory (18 plant species and 37 mentions), and genital (17 plant species and 28 mentions) diseases.

3.2.4. Most Popular Plants for Treatment of Certain Diseases

Four plant species used in the East Rhodopes with FL equal to 100% were identified as: Cichorium intybus, Cornus mas, Tussilago farfara, and Achillea millefolium. Other species with a high FL index value were Prunus spinosa (85.7%), Ecballium elaterium. (80%), Allium cepa (71.4%), and Potentilla reptans (71.4%) (Table 5).

3.3. Comparision between East and Central Rhodopes

3.3.1. Similarity between Central and East Rodopes with Regard to Medicinal Plant Usage

The number of plant species arranged according to their categories of use (for use in human medicine, for prophylactic purposes, and for veterinary use) in the two analyzed areas is shown in Figure 4. The number (n = 101) of species with application in human medicine was the highest.
The geographical and floristic features of the analyzed areas determine the relatively high number of species used by communities: 47 species for use in human medicine and 12 species with prophylactic application. At the same time, a large number of species is used in only one of the regions: 33 species for use in human medicine in the Central Rhodopes and 21 species in the East Rhodopes, respectively (Figure 4). There is a trend for a relatively higher number of medicinal plant species used among the population of the Central Rhodopes compared to the East Rhodopes in all three categories.
Based on the number of plant species identified in the two regions, the similarity coefficient JI was calculated for each of the groups. They ranged from 46.5% (in human medicine) to 11.8% (in veterinary practice). The overall similarity coefficient JI with respect to all species for both regions is 43.0%.

3.3.2. Relative Importance of the Plant Species Used for Medicinal Purposes

Plantago major is the most used plant species with human-medicinal use in the Central Rhodopes (0.67), while the same has a lower degree of use in the East Rhodopes (0.19). Sambucus nigra, has the second highest degree of use in the Central Rhodopes (0.60) and a lower degree of use in the East Rhodopes (0.23). Teucrium chamaedris and T. polium are used in both study areas (Table 1). Both species are found throughout the Rhodopes. However, T. chamaedris (0.40) is applied for diarrhea in the Central Rhodopes, while T. polium (0.26) is used for the same indication in the East Rhodopes (Figure 5).

3.3.3. Disease Categories Treated with Medicinal Plants

A trend for a higher number of reports in all disease categories for the Central Rhodopes compared to the East Rhodopes was identified, which was determined by the higher number of reports overall for the region, 527 in the Central Rhodopes compared to 277 in the East Rhodopes. The four most important disease categories, according to the number of mentions in both regions, are those of the nervous, respiratory, digestive, and cardiovascular systems, followed by the reproductive, urinary, and immune systems (Figure 6).

3.3.4. Degree of Agreement among Informant’s Knowledge

The informant consensus factor was higher in the Central Rhodopes in most categories (around and above 0.60) compared to the East Rhodopes. The informants from the East Rhodopes reported different plant species for the treatment of most disease categories. This might be explained by the low level of knowledge sharing about medicinal plants in East Rhodopes. The category “Other diseases” had a higher ICF factor for East Rhodopes compared to Central Rhodopes. This category includes treatment of toothache as there was a relatively high number of reports of Cotinus coggygria infusion for toothache treatment by informants in the East Rhodopes compared to the total number of reports, resulting in a high consensus factor for this category. The category of urinary tract healing showed the largest disparity in the informants’ consensus factor for both regions: 0.50 for Central and 0.23 for East Rhodopes (Figure 7).

3.3.5. Most Popular Plants for Treatment of Certain Diseases

The FL value was only 100% in both analyzed regions for two plants, Cichorium intybus (for treatment of diseases affecting the digestive system) and Tussilago farfara (for treatment of diseases affecting the respiratory system) (Figure 8).
Tilia cordata had high levels of reliability in Central (83.3%) and East Rhodopes (100%), indicating the preference of informants to treat respiratory system diseases with this plant. Additionally, digestive system diseases are treated with Mentha spicata in the Central Rhodopes (100%) and East Rhodopes (66.7%) (Figure 8).
Achillea millefolium had an FL value equal to 100% for the East Rhodopes and only 46.7% for the Central Rhodopes in the female reproductive system treatment category. This indicates that all informants who reported A. millefolium in the East Rhodopes mentioned the use of the species only in the category of treatment of the female reproductive system. We can conclude that in the East Rhodopes, A. millefolium is a known medicinal plant for the treatment of diseases affecting the female reproductive system. In the Central Rhodopes, A. millefolium was mentioned with the highest frequency in the same category, and at the same time, it is used to treat a wide range of diseases: gastritis and ulcer, inflammation of bile, treatment of abscesses, haemorrhoids, etc. (Figure 8).
Plantago major had a level of reliability for skin diseases (treatment of abscesses and wounds) with similar values for both regions (68.8% and 62.5%). Chelidonium majus is predominantly used for skin diseases in the Central Rhodopes (61.5%), while for the East Rhodopes, it is used in other categories (Figure 8).

3.4. Ethnobotanical Indices for Assessment of the Sustainable Use of Medicinal Plants

Figure 9 presents a chart of the most often mentioned species for most applications according to ΣU. The plant species with conservation status are marked, respectively (Figure 9, Table 1), as they require special attention. Origanum vulgare subsp. hirtum is under a regime of restriction for trade purposes collection. It appears to be highly popular among the rural population of East Rhodopes. It is collected from the wild populations [52] (Supplementary Figure S1), but informants reported mainly domestic collection and use (6th position with 23 mentionings for use and collection). The other species with the same regime of protection is Sideritis scardica (24th position with 13 mentionings for use and collection, with a few of these cases for illegal trade as the plant is vastly cultivated in plantations and kitchen gardens). Primula veris is another plant species that should be treated with caution (Figure 9, Table 1). According to the ΣU, P. veris is listed 11th with 19 mentionings, but again for domestic use by informants. Micromeria dalmatica is a Balkan endemic with restricted distribution and density of populations [61] (Figure 9, Table 1). It takes 15th position with 17 mentionings, only in Central Rhodopes where it occurs. Of all plant species with different conservation statuses (Table 1), this is the one at the highest risk. It is not included in the Red Data List and has no protection. The informants rarely reported trade purpose collection for this species. However, harvest for trade obviously occurs, as the plant is offered commercially (Figure 10). Many of the informants shared their observations of wild resource decrease in the last decade.

3.5. New Records for Plant Names and Application

Two plant species, namely Crepis zacintha (L.) and Sedum album L. (Figure 11) were first documented for the treatment of warts. They both were mentioned under the name “брадавичнo биле”, meaning “wart-wort”. Centaurea diffusa Lam. (Figure 12) is used to cure diarrhoea.

4. Discussion

The results of this study reveal that in both regions of the Rhodopes, medicinal plants are mentioned most often in relation to diseases affecting nervous, respiratory, digestive, and cardiovascular systems, followed by reproductive, urinary, immune, and musculoskeletal systems (in Central Rhodopes the first three categories were dominant). The results from previous studies on different parts of the territory of Bulgaria show that medicinal plants are most commonly used to treat diseases of the central nervous and musculoskeletal systems, skin, gastrointestinal, and respiratory systems [4,6]. Interestingly for the leading category, diseases affecting the nervous system, the ICF value in the Central Rhodopes is 0.72, while in the East Rhodopes, the ICF value is 0. In general, the ICF is higher in the Central Rhodopes in most categories (around and above 0.60) compared to the East Rhodopes.
The ethnobotanical survey carried out in the Rhodopes revealed the use of 114 plant species in relation to human health ([52]: Supplement Figures S1 and S2). Thus, the results demonstrate the use of a larger number of medicinal plants in the Rhodope Mountains compared to other regions of the country [1,5,10,62]. This can be explained by the relatively richer species diversity and the mountainous appearance of the study area, as well as the preserved traditions in the use of medicinal plants. Additionally, ethnobotanical data on medicinal plants that have not been documented in the literature are still being recorded in this study and in future studies [4,6].
The ethnobotanical analysis found that the most commonly used species in the Rhodopes are Sambucus nigra, Thymus spp., Plantago major, Origanum vulgare subsp. vulgare, Hypericum perforatum, Origanum vulgare subsp. hirtum, Cotinus coggigria, Pinus spp., Teucrium chamaedris, and Sempervivum tectorum, but the highest Fl (100%) was calculated for plant species which are not so often mentioned, such as Cichorium intybus (for treatment of diseases affecting the digestive system and Tussilago farfara (for treatment of diseases affecting the respiratory system) in both analyzed regions, as well as Mentha spicata (for treatment of respiratory diseases in Central Rhodopes), Geranium macrorrhizum (for treatment of diseases of the cardiovascular system in Central Rhodopes), Tilia cordata (for treatment respiratory system diseases in East Rhodopes), and Achillea millefolium(for female reproductive system treatment in East Rhodopes). The results concerning the most commonly used herbs are consistent with the data presented by Ploetz and Orr for the Rhodopes, e.g., Thymus spp., Origanum vulgare subsp. Hirtum, etc. [2,3]. The plants listed for Rhodopes are similar to the plants listed for other regions in Bulgaria, but they show some rating differences. According to Kozhuharova and co-authors [5], the most popular medicinal plants in Bulgaria are Hypericum perforatum, Cotinus coggygria, Plantago major, Sempervivum spp., Calendula officinalis, Melissa officinalis, Aesculus hippocastanum, and Matricaria chamomilla. A comparison with other Balkan regions also shows that Hypericum perforatum is one of the most important medicinal plants for the rural populations in the Suva planina Mts in South East Serbia [17] and the Mersin province in Turkey [63]. Hypericum perforatum is also commonly reported as one of the main herbs used in Central Macedonia, the province of Greece [19]. While the respondents from Turkey use oleate of Hypericum species for external wound treatment [63], the rural population of Central Rhodopes applies it for digestive problems [52]: Supplementary Figure S1 shows the internal application of this plant by the population of the Suva Planina Mts [17]. Another Turkish study reveals that medicinal plants are used mainly for digestive, respiratory, cardiovascular, urinary, and skin disorders [64]. This is partially similar to our results, as medicinal plants in the Rhodope Mountains are most commonly used for nervous, respiratory, digestive, and cardiovascular system disorders. As shown recently, the reasons for which plants are valued or important to people are rather complex; therefore, ethnobotanical indices cannot fully reveal the importance of plant use. For instance, the exclusiveness of therapeutical applications (FL) does not serve as a proxy for effectiveness. It is necessary to use and understand the contextualized primary data [65]. Additionally, as was mentioned above, most of the traditional cures are centered around symptoms which, from the point of view of modern institutional medicine, may have very different causes and would be treated in very different ways. An additional difficulty is due to the fact that the perception of traditional medical practice is dualistic, natural and preternatural, which does not correspond well with the scientific monistic approach [66]. However, ethnobotanical research is still a valuable source of information. Even though ethnobotanical indices cannot pinpoint plant substances for drug discovery, primary data provides knowledge about the cultural value and importance of plants [65], including conservation issues.
Davidov and co-authors listed 15 common names for Sedum album, but none were related to warts [67]. Crepis zacintha was not known as a medicinal plant when the aforementioned study was conducted. The use of Centaurea diffusa to cure diarrhoea was also a new record as this plant was not known as medicinal. Other species of Centaurea were mentioned in relation to diarrhoea cures [68].

5. Conclusions

Traditional knowledge about medicinal plants is preserved to a considerable extent and is currently actively used among the population in the Rhodope Mountains. The locals in the Rhodopes rely on plants to treat various health problems. Comparative statistical analysis showed that the rural populations in both study areas, Central and East Rhodopes, apply plant substances for diseases affecting nervous, respiratory, digestive, and cardiovascular systems, followed by reproductive, urinary, immune, and musculoskeletal systems (the first three categories were dominant but in the Central Rhodopes, the rating order was nervous, respiratory, and digestive systems while in the East Rhodops, it was digestive, nervous, and respiratory systems). They use different species of medicinal plants to treat the same health conditions in these regions. For instance, in the category of respiratory health problems (cough—infusion, inhalation, compress, syrup), the utilization of 27 plants was reported. Among them, seven taxa were mentioned most often by the informants in the Central Rhodopes (Tussilago farfara, Tillia cordata, Pinus spp. Thymus spp., Primula veris, Sambucus nigra, and Plantago major). In the same category, informants in the East Rhodopes mentioned 16 plant species, of which, four taxa (T. farfara, T. cordata, Brassica oleraceae, and Paliuris spina-christi) are used most often. Only a few of them were mentioned in both regions, e.g., T. farfara, T. cordata, Hypericum perforatum, and Juglans regia. For a few plants, the ICF was 100%, and they were not the most often mentioned ones. It seems that ethnobotanical cultural diversity is higher in the East Rhodopes as the ICF was lower. The differences in the use of medicinal plants in the Central and East Rhodopes were determined by the floristic characteristics in the two study areas. We attributed the difference to phytoclimatic and ecological as well as cultural and historical features. The risk of disruption or loss of traditional knowledge of medicinal plants is expected in the condition of cultural globalization. However, there are no metrified data about the use of medicinal plants in the Rhodopes from the past. The application of statistical indices in this research will make possible such assessment and monitoring in the future.
Bulgaria is one the richest countries in Europe in terms of biodiversity (number of species per territory) and is home to numerous local and Balkan endemic and relict species. This is particularly valid for the Rhodopes too. Ethnobotanical studies provide valuable data for sustainable development and biodiversity conservation. This research reveals alarming facts about the overcollection of Micromeria dalmatica, which motivates its introduction in cultivation. Implications for future research include developing cultivation protocols for M. dalmatica and establishing good practices in local communities for the sustainable use of medicinal plants.

Author Contributions

Conceptualization, I.M. and E.K.; methodology, I.M., C.R. and E.K.; validation, I.M., L.R., I.A., Z.N., N.N. and E.K.; formal analysis, I.M., C.R. and E.K.; investigation, I.M.; writing—original draft preparation, I.M. and M.K.; writing, review, and editing, E.K., M.K., Z.N., I.A., N.N. and L.R.; visualization, I.M., C.R. and E.K.; supervision, E.K.; project administration, I.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the European Union—NextGenerationEU, through the National Recovery and Resilience Plan of the Republic of Bulgaria, Project № BG-RRP-2.004-0004-C01.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Experimental data are available from the corresponding author upon reasonable written request.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Settlements of the survey in the Rhodope Mountain and the number of informants.
Figure 1. Settlements of the survey in the Rhodope Mountain and the number of informants.
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Figure 2. Factor diagram of disease categories in the Central Rhodopes, according to the number of mentions ΣU.
Figure 2. Factor diagram of disease categories in the Central Rhodopes, according to the number of mentions ΣU.
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Figure 3. Factor diagram of disease categories in the East Rhodopes, according to the number of mentions ΣU.
Figure 3. Factor diagram of disease categories in the East Rhodopes, according to the number of mentions ΣU.
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Figure 4. Total number of identified plant species by application and region.
Figure 4. Total number of identified plant species by application and region.
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Figure 5. Comparison of plant species by UV index.
Figure 5. Comparison of plant species by UV index.
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Figure 6. Comparison of different disease categories treated with medicinal plants by ΣU values.
Figure 6. Comparison of different disease categories treated with medicinal plants by ΣU values.
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Figure 7. Comparison of different disease categories by ICF values.
Figure 7. Comparison of different disease categories by ICF values.
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Figure 8. Comparision of different diseases categories by FL index.
Figure 8. Comparision of different diseases categories by FL index.
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Figure 9. Most often mentioned species for most applications according to ΣU.
Figure 9. Most often mentioned species for most applications according to ΣU.
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Figure 10. Micromeria dalmatica, the most often mentioned species for most applications according to ΣU in Central Rhodopes.
Figure 10. Micromeria dalmatica, the most often mentioned species for most applications according to ΣU in Central Rhodopes.
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Figure 11. “Брадавичнo биле” Crepis zacintha (L.) Babc. and Sedum album L.
Figure 11. “Брадавичнo биле” Crepis zacintha (L.) Babc. and Sedum album L.
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Figure 12. Centaurea diffusa Lam., Трънче.
Figure 12. Centaurea diffusa Lam., Трънче.
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Table
Table 1. Plant species reported for human health usage in Central and East Rhodopes—UV (%) values for therapeutic or prophylactic purposes and conservation status; Legend: MOEW Ministry of Environment and Waters, RDB—Red Data Book of Bulgaria, EN—Endangered, CR—Critically endangered, BDA—Biodiversity Act of Bulgaria, Bal—Balkan endemic. Note: most of the listed plants are common with wide distribution; R. fruticosus does not occur in Bulgaria, but since this is the name coined in pharmaceutical practice, we used it to mark all Rubus species with black fruits reported by informants.
Table 1. Plant species reported for human health usage in Central and East Rhodopes—UV (%) values for therapeutic or prophylactic purposes and conservation status; Legend: MOEW Ministry of Environment and Waters, RDB—Red Data Book of Bulgaria, EN—Endangered, CR—Critically endangered, BDA—Biodiversity Act of Bulgaria, Bal—Balkan endemic. Note: most of the listed plants are common with wide distribution; R. fruticosus does not occur in Bulgaria, but since this is the name coined in pharmaceutical practice, we used it to mark all Rubus species with black fruits reported by informants.
Plant SpeciesLocal NameConservation StatusCentral Rhodopes UV ValuesEast Rhodopes UV Values
Amaranthaceae
Chenopodium foliosum Asch.Гърличава трева, свински ягoди 0.08
Amaryllidaceae
Allium cepa L.Лук, суганoв лук 0.130.16
Allium porrum L.Праз лук 0.080.02
Allium sativum L.Чесън 0.040.02
Galanthus nivalis L.
Galanthus elwesii Hook.		КoкичеEN-IUCN, RDB, protected by BDA0.02
0.02
Anacardiaceae
Cotinus coggygria Scop.Тетра, смрадлика 0.080.42
Apiaceae
Eryngium campestre L.Ветрoгoнче 0.05
Apocynaceae
Nerium oleander L.Зoкум 0.02
Araceae
Arum maculatum L.Змиарник 0.07
Araliaceae
Hedera helix L.Бръшлян 0.02
Asparagaceae
Ruscus aculeatus L.Див чемшир 0.05
Asteraceae
Achillea millefolium L.Равнец бял 0.310.09
Agrimonia eupatoria L.Камшик 0.170.14
Arctium lappa L.Рьoпел, репей 0.170.05
Artemisia absinthium L.Пелин бял 0.12
Artemisia vulgaris L.Пелин 0.02
Calendula officinalis L.Невен 0.270.16
Carduus nutans L.Гингер 0.19
Centaurea cyanus L.Синчец 0.02
Centaurea diffusa Lam.Трънче 0.09
Cichorium intybus L.Синя жлъчка 0.100.09
Cirsium spp.Паламида 0.02
Crepis zacintha (L.) Babc.Брадавичнo биле
Helianthus annuus L.Слънчoглед 0.13
Matricaria chamomilla L.Лайка 0.040.21
Onopordum acanthium L.Магарешки бoдил 0.020.05
Tagetes erecta L.Турта 0.05
Taraxacum officinale F. H. Wigg.Глухарче 0.040.02
Tussilago farfara L.Пoдбел 0.330.09
Betulaceae
Corylus avellana L.Леска 0.100.02
Boraginaceae
Borago officinalis L.Пoреч 0.02
Pulmonaria officinalis L.Медуница 0.04
Brassicaceae
Brassica nigra (L.) K.Koch.Синап 0.02
Brassica oleracea L.Зеле 0.040.14
Sinapis alba L.Синап 0.06
Caryophyllaceae
Silene vulgaris (Moench) GarckeСкрипалец
Stellaria media (L.) CirilloЗвездица 0.04
Cornaceae
Cornus mas L.Дрян 0.09
Crassulaceae
Sedum album L.Брадавичнo биле 0.08
Sedum spectabile L.Дебела мара 0.05
Sempervivum tectorum L.Бабин квас, ушнo биле 0.420.05
Cucurbitaceae
Cucurbita maxima Duchesne.Тиква 0.02
Ecballium elaterium (L.) A.Rich.Луда краставица 0.12
Cupressaseae
Juniperus communis L.Хвoйна 0.060.05
Equisetaceae
Equisetum arvense L.Хвoщ 0.150.02
Ericaceae
Vaccinium myrtillus L.Бoрoвинка черна 0.06
Vaccinium vitis-idaea L.Бoрoвинка червена 0.02
Euphorbiaceae
Ricinus communis L.Kъpлeж 0.02
Fabaceae
Phaseolus vulgaris L.Фасул 0.06
Astragalus glycyphyllos L.Клин 0.02
Gentianaceae
Centaurium erythraea Rafn.Кантариoн червен 0.13
Geraniaceae
Geranium macrorrhizum L.Здравец 0.190.02
Pelargonium zonale (L.) L’Hér.Индрише 0.020.05
Gesneriaceae
Haberlea rhodopensis Friv.Орфеевo цветеBal., protected by BDA
Hypericaceae
Hypericum perforatum L.Кантариoн жълт 0.460.19
Juglandaceae
Juglans regia L.Орех 0.170.16
Lamiaceae
Clinopodium vulgare L.Кoтешка стъпка 0.100.09
Melissa officinalis L.Матoчина 0.04
Mentha spp.Мента 0.02
Mentha spicata L.Гьoзум 0.170.14
Micromeria dalmatica Benth.Бяла мента, планинска ментаBal.0.17
Ocimum basilicum L.Бoсилек 0.05
Origanum vulgare L. subsp. vulgareРиган, балкански риган 0.290.02
Origanum vulgare subsp. hirtum (Link) Ietsw.Риган бялCollection for trading forbidden 0.16
Salvia verticillata L.Прешленеста какула 0.2
Satureja montana L.Планинска чубрица 0.02
Sideritis scardica Griseb.Триградски чай, Мурсалски чайCollection for trading forbidden0.04
Stachys officinalis (L.) Trevis.РанилистSpecial regime of collection (MOEW)0.100.02
Teucrium chamaedrys L.Пoдъбиче червенo 0.400.02
Teucrium polium L.Пoдъбиче бялo 0.26
Thymus spp.Мащерика, oленица 0.460.02
Liliaceae
Lilium rhodopeum Delip.Крем рoдoпскиBal., CR-IUCN, RDB, protected by BDA
Malvaceae
Malva sylvestris L.Слез, „ебе гюмеджи“ 0.130.09
Tilia cordata Mill.Липа 0.130.09
Moraceae
Morus spp.Черница 0.07
Oleaceae
Fraxinus ornus L.Мъждрявка, мъждян 0.02
Olea europaea L.Маслина 0.060.07
Syringa vulgaris L.Люляк 0.06
Orchidaceae
Orchis spp.
Anacamptis spp.
Dactylorhiza spp.		СалепSpecies with various IUCN statuses—some of them protected by BDA; collection for trading forbidden for all of them [52]0.02
0.02
0.02
Papaveraceae
Chelidonium majus L.Саралoкавo биле, префръкница 0.270.21
Pinaceae
Pinus spp.Бoр 0.25
Plantaginaceae
Digitalis lanata Ehrh.Зъбавo биле 0.02
Plantago major L.Петрoжилка ширoка 0.670.19
Plantago minor Fr.Петрoжилка тясна 0.19
Poaceae
Zea mays L.Царевица 0.04
Polygonaceae
Polygonum hydropiper L.Пипеиче вoднo 0.020.07
Portulacaceae
Portulaca oleracea L.Тученица 0.02
Primulaceae
Primula veris L.ИгликаSpecial regime of collection (MOEW)0.27
Ranunculaceae
Clematis vitalba L.Пoвет 0.08
Helleborus odorus Waldst. and Kit. ex Willd.Кукуряк 0.02
Rhamnaceae
Paliurus spina-christi Mill.Парички, карачелия 0.21
Rosaceae
Alchemilla spp. (vulgaris complex)ЦаричеSpecial regime of collection (MOEW)0.13
Crataegus monogyna Jacq.Глoг 0.060.02
Malus pumila Mill.Ябълка 0.230.14
Potentilla erecta (L.) Räusch.Трoши каменче 0.02
Potentilla reptans L.Петoпръстник, влачещите пет пръста 0.250.16
Prunus persica (L.) BatschПраскoва 0.02
Prunus spinosa L.Трънка 0.16
Rosa canina L.Шипка 0.100.07
Rosa multiflora Thunb.Трендафил 0.02
Rubus fruticosus L.Къпина 0.020.05
Rubus idaeus L.Малина 0.13
Rubiaceae
Galium verum L.Еньoвче 0.150.05
Salicaceae
Salix alba L.Върба 0.060.05
Santalaceae
Viscum album L.Имел, имала, oмела 0.100.14
Solanaceae
Lycopersicon esculentum Mill.Дoмат 0.12
Nicotiana tabacum L.Тютюн 0.020.05
Physalis alkekengi L.- 0.02
Solanum tuberosum L.Картoф 0.230.02
Tropaeolaceae
Tropaeolum majus L.Латинка 0.02
Urticaceae
Urtica spp.Кoприва 0.250.19
Viburnaceae
Sambucus ebulus L.Нисък бъз, султан 0.100.16
Sambucus nigra L.Бъзлян, вискoк бъз 0.600.23
Vitaceae
Vitis vinifera L.Лoза 0.04
Zygophyllaceae
Tribulus terrestris L.Бабини зъби 0.09
Table
Table 2. ICF factor by diseases categories for Central Rhodopes.
Table 2. ICF factor by diseases categories for Central Rhodopes.
CategoryntnurICF
1Respiratory system261120.70
2Cardiovascular system17440.63
3Digestive system271020.74
4Urinary system15290.50
5Reproductive system14300.55
6Nervous system91250.72
7Immune system11290.64
8Musculoskeletal system13280.56
9Others5280.33
Table
Table 3. FL by diseases categories for Central Rhodopes (number of reports > 4).
Table 3. FL by diseases categories for Central Rhodopes (number of reports > 4).
CategoryBotany NameReportsFL [%]
Respiratory systemTussilago farfara16100.0
Tilia cordata583.3
Pinus spp.650.0
Thymus spp.1045.5
Primula veris538.5
Sambucus nigra620.7
Plantago major.515.6
Cardiovascular systemGeranium macrorrhizum.9100.0
Urtica spp.758.3
Sambucus nigra517.2
Digestive systemCichorium intybus5100.0
Mentha spicata8100.0
Teucrium chamaedrys1894.7
Centaurium erythraea583.3
Agrimonia eupatoria.675.0
Hypericum perforatum1359.1
Achillea millefolium533.3
Reproductive systemAchillea millefolium746.7
Malus pumila L.545.5
Nervous systemPrimula veris753.8
Solanum tuberosum545.5
Thymus spp.627.3
Immune systemSambucus ebulus5100.0
Sambucus nigra1241.4
Table
Table 4. ICF factor by diseases categories for East Rhodopes.
Table 4. ICF factor by diseases categories for East Rhodopes.
CategoryntnurICF
1Respiratory system18480.53
2Cardiovascular system19350.47
3Digestive system16380.59
4Urinary system11140.23
5Reproductive system17290.43
6Nervous system7590.00
7Immune system8170.56
8Musculoskeletal system11200.47
9Others7170.45
Table
Table 5. FL by diseases categories for East Rhodopes (number of reports > 3).
Table 5. FL by diseases categories for East Rhodopes (number of reports > 3).
CategoryBotany NameReportsFL [%]
Respiratory systemTussilago farfara4100.0
Ecballium elaterium.480.0
Brassica oleracea466.7
Paliurus spina-christi444.4
Cardiovascular systemPrunus spinosa.685.7
Teucrium polium545.5
Digestive systemCichorium intybus4100.0
Cornus mas4100.0
Mentha spicata466.7
Teucrium polium654.5
Reproductive systemAchillea millefolium4100.0
Potentilla reptans571.4
Musculoskeletal
system		Allium cepa571.4
Sambucus ebulus454.1
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Mincheva, I.; Naychov, Z.; Radev, C.; Aneva, I.; Rastrelli, L.; Kamusheva, M.; Nikolov, N.; Kozuharova, E. Ethnobotanical and Ethnopharmacological Study in the Bulgarian Mountain Rhodopes: Part II—Contemporary Use of Medicinal Plants. Diversity 2023, 15, 482. https://doi.org/10.3390/d15040482

AMA Style

Mincheva I, Naychov Z, Radev C, Aneva I, Rastrelli L, Kamusheva M, Nikolov N, Kozuharova E. Ethnobotanical and Ethnopharmacological Study in the Bulgarian Mountain Rhodopes: Part II—Contemporary Use of Medicinal Plants. Diversity. 2023; 15(4):482. https://doi.org/10.3390/d15040482

Chicago/Turabian Style

Mincheva, Irena, Zheko Naychov, Cristo Radev, Ina Aneva, Luca Rastrelli, Maria Kamusheva, Nikolay Nikolov, and Ekaterina Kozuharova. 2023. "Ethnobotanical and Ethnopharmacological Study in the Bulgarian Mountain Rhodopes: Part II—Contemporary Use of Medicinal Plants" Diversity 15, no. 4: 482. https://doi.org/10.3390/d15040482

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