An Ethnobotanical Survey of Medicinal Plants Used in Papantla, Veracruz, Mexico

An ethnobotanical study was performed to collect information on the use of medicinal plants in Papantla, Veracruz, Mexico. The area has a high number of endemic species, and the social importance of the medicinal plants in the community is essential for public health and the conservation of traditional knowledge. This study identified the medicinal plants currently used, registered traditional knowledge, and documented the patterns of ailments treated in the indigenous communities of Totonacas. A total of 101 medicinal plants belonging to 51 families were described by 85 local informants. Asteraceae was the family with the highest number of plant species identified by these informants. Plant parts are used to treat several ailments, including venomous bites, gastro-intestinal disorders, infectious diseases and other disorders. Informants reported that the most common plant part used was the leaf tissue (55%), and they also took the herbal remedies orally (72%), and decoctions (38%) as well as infusions (29%) were the forms used to prepare these natural remedies. This study provides documentation of medicinal plants used in the Veracruz area of Mexico. Mexican people are still dependent upon medicinal plants, and in order to avoid their loss, certain measures of conservation for medicinal plants are needed.


Introduction
Traditional medicine is considered the first health care resource to treat ailments in several countries [1][2][3], and about 80% of people in the world depend upon traditional medicine, according to the World Health Organization (WHO) [4].
Traditional medicine studies include ethnomedicine, which involves the practices most used by people that live in rural areas and indigenous communities, and this ethnomedicine is affected by factors such as age, gender, economic activity, socio-economic level, migration, access to new health care systems, new herbal products and urbanisation [5][6][7]. The diversity of medicinal plants is very high in Mexico; the country contains a wide variety of plants (30,000) which have not been explored in their totality [8], and a significant number are endemic (uniquely native) species [9].

Characteristics of the Informants
There is a high prevalence in the use of medicinal plants and traditional knowledge in the Veracruz area. Table 1 provides the socio-demographic information such as residence, gender, age, occupation and annual expenditure in plants of the informants. Of the 85 indigenous people who answered the form, men represented the highest number (53%), and people from 70 to 85 years appeared to have a more extensive knowledge of these plants. In general, the gender was not significantly correlated to age and plant knowledge [18,19]. Even though all of the respondents generally used traditional plants, it has been common that, in many parts of the world, the women always demonstrate a more extensive knowledge in the use of plants [20]. This could be due to their roles in the family.
Previous studies have shown that women usually have more knowledge about medicinal plants, and men know more about timber and handcraft species. This happens due to the sexual division of labour, and external factors resulting from the male migration of the young people inside the communities [18,21]. In our study, women on average cite two more plants and spend more money (17 plants, expenditure: $200) than their male counterparts (15 plants, expenditure: $176). Homemakers ($210 annually) generally spend more money for plants compared to those in other occupations; the lowest expenditure was observed for the sellers. The expenditure for plants during the year is equivalent to two days of work for the farmers. Case, et al. [22] mentions that local knowledge in plants increases with increasing geographical isolation; the people intensively use more plant species due to the scarcity of medical centres, specialists or medicines. Nevertheless, other studies have related family income (economic status) as the main factor in the number and the uses of known plants [23]. The keepers of the traditional knowledge were found to be the teachers (average of 22 plants), followed by farmers (18 plants), and housewives (15 plants). Academic staff (teachers) showed more knowledge of plants because they received children from different communities, and the social engagement in those schools promoted and applied different strategies to keep their costumes, languages and traditions alive inside the classroom.
In Mexico, the preservation of plant use knowledge is still carried out in oral form and transmitted generation by generation. In fact, informants declare that the origin of the traditional knowledge was given by the family (87%) and the specialist "shamans" (13%). More than half of the informants (58%) claimed to perceive a decrease (medium and high loss) in the traditional knowledge during their youth; the rest (42%) did not perceive any alarming decrease.
Seventy-eight of the informants (92%) were actively using medicinal plants in their daily lives, but 70 of these (82%) recur to the plants in the first instance to treat their ailments. Nevertheless, there were just 16% (14 people) going to specialists. The informants obtained the plants mostly from wild gathering (37%), the market (35%) and familiar gardens (28%).
Some informants (29%) expressed that they do not have any expenditure in buying plants, since they know the surrounding areas where they can find them. The informants (38%) positively emphasised the usage of medicinal plants as part of their cultural uses (38%), and they consider them as an effective and cheap resource (35%) since their childhood to treat human disorders.

Mode of Preparation and Administration of Different Plant Parts
Informants recognised 101 ethnobotanical plants belonging to 51 families distributed in 95 genera (Table 2), which were commonly used by most the of indigenous people for the treatments of 77 ailments. The most represented families were Asteraceae and Rutaceae, with eight plant species for each one, followed by Fabaceae (six species), Myrtaceae, Malvaceae and Apocynaceae (four species), and then Euphorbiaceae, Lamiaceae, Meliaceae and Poaceae with three species. Other families had two and one species each reported. Plant species of the Asteraceae family were the most used in Populoca, Veracruz [24], and not only in Papantla. This could be due to the abundance and wide variety of Asteraceae species in ecosystems in the northern and rainforest areas of Veracruz [16,18] and to their relative cultural importance. The plant list reported that a total of 61% of the species are native, 37% are exotic, and only 2% are endemic. The indigenous people keep using the local plants due to the great knowledge of the properties of these plants. The plant parts are usually consumed fresh (83%), and leaves (55%) represented the most common plant parts used by the informants to prepare their medicinal remedies. Leaves were followed by roots, bark, fruits, stems, whole plants, seeds, latex and flowers ( Figure 1). genera (Table 2), which were commonly used by most the of indigenous people for the treatments of 77 ailments. The most represented families were Asteraceae and Rutaceae, with eight plant species for each one, followed by Fabaceae (six species), Myrtaceae, Malvaceae and Apocynaceae (four species), and then Euphorbiaceae, Lamiaceae, Meliaceae and Poaceae with three species. Other families had two and one species each reported. Plant species of the Asteraceae family were the most used in Populoca, Veracruz [24], and not only in Papantla. This could be due to the abundance and wide variety of Asteraceae species in ecosystems in the northern and rainforest areas of Veracruz [16,18] and to their relative cultural importance. The plant list reported that a total of 61% of the species are native, 37% are exotic, and only 2% are endemic. The indigenous people keep using the local plants due to the great knowledge of the properties of these plants. The plant parts are usually consumed fresh (83%), and leaves (55%) represented the most common plant parts used by the informants to prepare their medicinal remedies. Leaves were followed by roots, bark, fruits, stems, whole plants, seeds, latex and flowers ( Figure 1).  The main reason for the use of leaves was the ease of collecting them. Herbal medicines are either based on single species or mixed with other plant species. Nowadays, the use of the multi-treatment (contemporary and conventional medicine) becomes a usual method for people to save money, obtain more results, and reduce the allopathic effects from the modern medicaments [25]. The mixture of two or more plants is seen in this study; and it is known that the use of more than two herbs could contain a range of different active compounds and can modify its effect, enhancing or reducing the healing effect. If we considered each mixture as one single remedy [26], the list of natural remedies could be multiplied. Nonetheless, the toxic effects should be studied in depth. Many of the plants were used in minimal concentrations by the locals, but they are still unknown and unregistered. It is remarkable that the use of exotic plants has not been well investigated against normal symptoms.
Two main routes of the administration of herbal remedies are reported: Oral (72%) and topical (28%) administration. Herbal remedies were prepared by using ten different methods. The main forms used were decoctions (38%) and infusions (29%), but raw plant material (11%) was eaten fresh in order to combat gastrointestinal disorders, for blood circulation and against local pain (tooth pain). Raw materials of leaves, whole plants or stems were used for rituals, such as bad wind and evil eye. Bath and cataplasm (7%) were applied to treat skin disorders (wounds) and to treat infective diseases such as chicken pox, smallpox and measles. Liquefied, crushed and smashed (5%) remedies were used fresh and extracted from different plant parts for the treatment of diabetes and kidney problems. Squeezed (4%), tinctured (3%) and burned (2%) remedies were mainly used to treat rheumatism, pain in the ears and wounds. The leaves of H. patens were used as therapy, where the leaves were burned and applied over the chest to promote breastfeeding in women. Bark, fruits and seeds were also fermented (2%) to prepare alcoholic drinks ( Figure 2).        such as chicken pox, smallpox and measles. Liquefied, crushed and smashed (5%) remedies were used fresh and extracted from different plant parts for the treatment of diabetes and kidney problems. Squeezed (4%), tinctured (3%) and burned (2%) remedies were mainly used to treat rheumatism, pain in the ears and wounds. The leaves of H. patens were used as therapy, where the leaves were burned and applied over the chest to promote breastfeeding in women. Bark, fruits and seeds were also fermented (2%) to prepare alcoholic drinks ( Figure 2).

Use Reports, Informant's Consensus Factor and Fidelity Level
Given the results of our observations, the studied communities had a significant variety of traditional uses, with a specific frame of ailments. A total of 77 ailments were grouped into 17 usecategories (Table 3) based upon the information gathered from those interviewed.

Use Reports, Informant's Consensus Factor and Fidelity Level
Given the results of our observations, the studied communities had a significant variety of traditional uses, with a specific frame of ailments. A total of 77 ailments were grouped into 17 use-categories (Table 3) based upon the information gathered from those interviewed. The ICF was calculated for each ailment category, and the highest value was calculated for poisonous animal bites (ICF = 0.92), which was for the roots of two plant species, Pentalinon andrieuxii (Müll.Arg.) B. F. Hansen & Wunderlin (13 UR) and Allium sativum L. (1 UR), which were reported by informants to be used in tinctures for the treatment of snakebites. These species are the same species used to treat snakebite in Central America [27].
Problems related with different types of cancer (oncology use-category) showed an ICF of 0.91 with 5 species and 44 URs, followed by gastro-intestinal disorders (ICF = 0.89), with 29 species and 247 URs. Infective diseases and fever had an ICF of 0.87 with 13 species and 93 URs; kidney disorders and genital-urinary disorders reported a similar ICF, with 17 species associated with each. The use-category of liver disorders showed the lowest degree of consensus; only three informants mentioned three plant species to treat ailments belonging to this category (cirrhosis, hepatitis and liver disorders); probably informants had not exchanged their information. Malnutrition, poverty and environmental conditions are the main factors causing common ailments (digestive, respiratory and skin disorders), as previously reported [28,29]. This study also found that cancer (in the stomach, skin and gallbladder) and diabetes cases have increased recently, and this problem could be related to the diet in the region. Decoctions and infusions of leaves from Asclepias curassavica (16 URs), Rauvolfia tetraphylla (11 URs) and Hamelia patens (9 UR) were used to treat cancer, whereas plants, such as Tecoma stans, Psidium guajava, Hamelia patens, Persea americana and Anacardium occidentale, were included within the treatments for diabetes [30]. Matricaria recutita, Mentha spicata, Psidium guajava, and Chenopodium ambrosioides, are consumed in nine other Mexican states [5,31,32]. Aloe vera, Piper auritum, Rutha chalepensis, Citrus limon, Annona reticulate, and Cocos nucifera have been recorded to be widely used by indigenous people in central-southern Mexico [28,33].
The most commonly used species was Hamelia patens Jacq, with 77 URs. It is a large perennial shrub that has been used against a range of ailments by other indigenous communities in Mexico [34]. Totonacs use Hamelia patens to treat problems related to diabetes (UR = 18), gastrointestinal disorders (gastritis, colitis, and ulcers) (UR = 17), cancer (UR = 9), high blood pressure and blood circulation, respiratory problems, anaemia, breastfeeding, menstruation, skin disorders and wounds. Its medical effects has been proved in another countries, including India [35], in treatments of nervous shock for its antidepressant properties, athletes' foot, skin lesions, insect bites, inflammation, rheumatism, headache, asthma and dysentery.
The leaves of Persea americana are commonly used by the Mexicans in infusions to treat gastrointestinal problems; nevertheless, previous reports have shown an increased use of the bark and seeds against diabetes, cholesterol and kidney problems in Central America [36,37]. Currently, Aloe vera plays an important role for its pharmacological effectiveness in treating a large number of ailments, such as skin problems, gastrointestinal problems, blood circulation problems, kidney problems and malnutrition, but it has been widely used by people with diabetes in Central America [30]. The use of Aloe vera has been spread throughout Latin America; and its ease of management and reproduction provided a cheap option for industry and people to grow it.
Additionally, the prevalence of new health problems that are present in tropical areas, such as dengue and Chikungunya, is getting more common around the world, and the way to combat them is a challenge for the people. The local people use coconut water as a strategy to reduce the impact of dehydration with the effects caused by Chikungunya. They also boil the mango leaves and mix them with the coconut water to drink and manage the fever caused by mosquito-borne diseases.
Our findings are in line with Alonso-Castro, et al. [29], where the main reasons of why people use medicinal plants in Mexico are related to their effectiveness and the low cost of usage and acquisition. However, they use traditional medicine as a complementary alternative to modern medicine, which is becoming more commonly used to treat diseases in Mexico in the past few decades [38].
The present study shows FL values varying from 23.4% to 100% ( Table 2). The results reported 50 medicinal plant species having maximum 100% FL. The high FL shows the preference of these plant species by informants for the treatment of specific diseases [39].

Description of the Study Area
The study area, geographically known as Totonacapan, is located in the northern part of Veracruz ( Figure 3). It is a part of the Northern Gulf Coastal Plain with an area of 4300 km 2 . This region represents about 5.97% of the total area of the state of Veracruz, and comprises 15 municipalities.
The study area belongs to the municipality of Papantla, known as Papanteca, with coordinates 20 • 27 39" S and 97 • 19 39", W, and it lies at 180 m above sea level. It has an area of 1458.50 km 2 , which represents 2.03% of the state.

Socio-Economic Description
The municipal territory is mainly devoted to agriculture (68%), followed by 11% livestock, 13% housing; the remaining 8% are occupied by trade, public offices and public spaces. The total population in the Totonacapan amounts to 622,846 inhabitants, of which 204,934 people form the economically active population (32.9%). Nevertheless, it should be noted that 32.5% of Totonac's population work in the primary sector (agriculture, fisheries and forestry), and around 66,000 people in Papantla have indigenous roots. According to Rivera and Ruiz-Ramírez [40], 77 of the 212 municipalities in the state have moderate poverty.
The ethnic composition of Veracruz is quite diverse and complex. Veracruz is the third-highest state in terms of the number of indigenous people (1,037,424) in México (CDI: National Commission for the Development of Indigenous Peoples) [41]. The state is divided into seven ethnic regions, and ethnic linguistic groups are located in the state of Veracruz. These groups still speak 14 different languages [Huasteco (Tenek), Popoluca, Mixe, Zoque, Chinanteco, Zapoteco, Mazateco, Mixteco, Otomí, Totonaca, Tepehua, Náhuatl from the Huasteca, Náhuatl from the Sierra de Zongolica, and Nahua from the south]. The most representative groups are Mazatecos, Totonacos and Zapotecos [40].
The Totonacos group lives in the city of Papantla and the surrounding areas; the tourism in this area helps them to sell handcrafts. Moreover, the performances of the sky dancers (Papantla flyers), and shamans are the main reason for tourism throughout the Mexican territory. It also has a remarkably high number of tourists who travel from different parts of the country to visit the shamans and buy the medicinal plants. The agriculture, livestock, forestry, traditional textile clothes, plants, fruits, practicing of traditional medicine and informal employment are the base of the local economy. Corn, beans, coffee, vanilla, bananas, citrons and oranges are the main crops produced in the region [7, 18,42].
Previous studies performed in neighbour municipalities [18] have shown the number of farmers depending on the farm products, and discuss migration and a lack of good opportunities causing a loss of interest to preserve the traditional knowledge in the new generation. The study area is highly interesting, and represents a special combination of different factors to study the patterns of traditional medicine. The climate is humid-warm, with an average annual temperature between 22 and 26 • C. The annual rainfall in the area varies between 1000 and 1500 mm. Totonacapan has a humid warm vegetation in most of its areas. The most common soils are Phaeozem-type Regosols and Vertisols, which are susceptible to erosion.

Socio-Economic Description
The municipal territory is mainly devoted to agriculture (68%), followed by 11% livestock, 13% housing; the remaining 8% are occupied by trade, public offices and public spaces. The total population in the Totonacapan amounts to 622,846 inhabitants, of which 204,934 people form the economically active population (32.9%). Nevertheless, it should be noted that 32.5% of Totonac's population work in the primary sector (agriculture, fisheries and forestry), and around 66,000 people in Papantla have indigenous roots. According to Rivera and Ruiz-Ramírez [40], 77 of the 212 municipalities in the state have moderate poverty.
The ethnic composition of Veracruz is quite diverse and complex. Veracruz is the third-highest state in terms of the number of indigenous people (1,037,424) in México (CDI: National Commission for the Development of Indigenous Peoples) [41]. The state is divided into seven ethnic regions, and ethnic linguistic groups are located in the state of Veracruz. These groups still speak 14 different languages [Huasteco (Tenek), Popoluca, Mixe, Zoque, Chinanteco, Zapoteco, Mazateco, Mixteco, Otomí, Totonaca, Tepehua, Náhuatl from the Huasteca, Náhuatl from the Sierra de Zongolica, and Nahua from the south]. The most representative groups are Mazatecos, Totonacos and Zapotecos [40].
The Totonacos group lives in the city of Papantla and the surrounding areas; the tourism in this area helps them to sell handcrafts. Moreover, the performances of the sky dancers (Papantla flyers), and shamans are the main reason for tourism throughout the Mexican territory. It also has a remarkably high number of tourists who travel from different parts of the country to visit the shamans and buy the medicinal plants. The agriculture, livestock, forestry, traditional textile clothes, plants, fruits, practicing of traditional medicine and informal employment are the base of the local economy. Corn, beans, coffee, vanilla, bananas, citrons and oranges are the main crops produced in the region [7, 18,42].
Previous studies performed in neighbour municipalities [18] have shown the number of farmers depending on the farm products, and discuss migration and a lack of good opportunities causing a loss of interest to preserve the traditional knowledge in the new generation. The study area is highly interesting, and represents a special combination of different factors to study the patterns of traditional medicine.

Ethnobotanical Analysis
Fieldwork was carried out from March to August of 2017 in 16 communities in the Papantla region (Adolfo López, Arroyo Grande, Carrizal, Cedros, Lahuas, Natividad, Panti, Papantla, Polutla, Poza Rica, Pozo Verde, San Antonio Xital, Veracruz, Spoupat, Volador and Zapotal). Before starting the survey, ethical approval for the study was first obtained from the indigenous organised group "Consejo de Ancianos de la Sabiduria Ancestral". Likewise, the president of the indigenous group, Miss María Luisa Santes Santes, supported and accompanied the visits to the people interviewed; this was in order to explain to them the investigation's purpose and to ask for their participation in this study. The questionnaires were supplied in the Spanish language and translated into the local language (Totonaco dialect) for the indigenous people who did not speak Spanish. Two translators accompanied the interviewer. Ethnobotanical information was collected from local inhabitants by using semi-structured questionnaires. A total of 85 informants were selected by snowball sampling. The informants were interviewed in their houses, in the streets and in local markets. Participant observation was also part of the interview, in order to have a better interpretation and analysis of the data reported by these informants.
The informants were asked to provide knowledge about the plant uses (local names, indication of use, used plant parts, places/methods/rituals of harvesting and administration mode). The informants were asked to show the place where they usually collect the plants. Many visits were conducted with the interviewed informants in order to collect, press and identify the medicinal plants. The plant material was collected by the authors and taxonomically identified. The botanical names of the species were verified with The Plant List (2013) (http://www.theplantlist.org) and voucher specimens were deposited in the Herbarium at the Chapingo Autonomous University.

Use Categories
Based on the information obtained from the indigenous people in the study area, all of the reported ailments were categorised into use-categories. The basic structure of ethnobotanical information is the use-report (UR) and this can be considered as an individual report of a specific taxon/drug for a certain use-category. When a plant is cited as "used", it is considered as one "use-report", but if one informant mentions the same plant to treat more diseases in the same category, it is considered as a single use-report.

Informants' Consensus Factor (ICF)
In this study, the level of homogeneity among the information collected from diverse informants for plant species in treating particular diseases was calculated by the informants' consensus factor (ICF). It was estimated using the following formula [43]: where, Nur is the number of UR in each disease category and Nt is number of species used. Low ICF values suggest that the plant is used randomly, or information on its use is not exchanged among informants, whereas a high exchange of information and a well-defined selection criterion in the community is reported for a plant with high ICF values.

Fidelity level (FL)
Fidelity level (FL) represents the percentage of informants claiming the use of a certain plant for the same major purpose, which can be calculated for the most frequently reported diseases or ailments as: FL (%) = (Np/N) × 100 where "Np" is the number of informants that claim a use of a plant species to treat a particular ailment, and "N" is the number of informants that use the plants as a medicine to treat any given disease or category [44].

Conclusions
The collected information indicates that the study area is rich in medicinal plants, and the results contribute to spread their uses. The social importance of the medicinal plants in the community is quite important for the public health and the conservation of traditional knowledge, and good management is required. In Papantla (Veracruz, Mexico), the indigenous population still depends upon medicinal plants to treat several ailments. The plants used have a mostly native origin. The species most frequently mentioned by the informants was Hamelia patens followed by Persea americana, Bursera simaruba, Matricaria chamomilla, Mentha spicata and Aloe vera. The safety and efficacy of cited plants needs to be investigated by phytochemical and pharmacological analysis, as it has been previously performed on several other traditionally used plant species [45][46][47].