Wild edible plants collected by Hani from terraced rice paddy agroecosystem in Honghe Prefecture, Yunnan, China

Background The Hani people in the Honghe Prefecture of Southeastern Yunnan, China, have practiced terraced rice paddy farming for more than 1300 years. These rice fields, combined with the surrounding forests and water systems, form a special agroecosystem that has attracted both tourists and scientists. For centuries, the local people have traditionally collected wild edible plants (WEP) from the agroecosystem, but this unique traditional practice in this area has never been reported. Methods Ethnobotanical fieldwork was conducted in four counties (Yuanyang, Honghe, Jinping, and Lüchun) between 2014 and 2019. Local self-identified Hani people (186) were interviewed, and information concerning local WEP species was obtained, documented, and analyzed. Plant samples and voucher specimens were collected for taxonomic identification. Results A total of 224 WEP species, belonging to 90 families and 170 genera, were recorded as used by the Hani people in Honghe. The most common WEP parts used include fruits, stems, and leaves, and the most common preparation methods include eating as a potherb (wild vegetable) and eating fresh. Some WEPs, like Phyllanthus emblica and Dioscorea subcalva, have unique preparation methods. The use-value (UV) and frequency of utilization index (FUI) of WEP species were analyzed. The 20 WEP species with the highest UV were noted as particularly important to the Hani people’s daily life in Honghe. Conclusion A large majority of these WEP species possess tremendous economic potential for future development. However, the diversity of WEP species, the associated traditional knowledge, and the broader agroecosystem are facing challenges such as biodiversity loss and pollution from chemical pesticides and fertilizers. This study may help local people to recognize the value of local WEP species and associated traditional knowledge, as well as provide ethnobotanical information for the future development of this tourism region.

(2013) [5]. For example, Zhu et al. [6] carried out a series of experiments in the terraced rice paddy fields in Honghe Hani and found that crop heterogeneity could solve the vulnerability of monoculture crops to disease; Li et al. [7] studied the agricultural soils by molecular methods and revealed the dynamics of organic matter in Yuanyang Terrace. However, there have been no studies on the wild edible plants (WEP species) collected and consumed by the Hani people in Honghe Hani terraced rice paddy system. In addition to scientific interest, the Honghe rice terraces have attracted more than 20 million tourists since 2014 [8]. Due to their interests in local foods, tourists have driven a demand for WEP species on the menus of local restaurants.
The Hani people speak their own language, which does not have a traditional writing system. After 1957, a set of writing characters of the Hani language based on Latin was invented with the help of the Chinese government and linguists [8].
About 1300 years ago [9], the Hani people migrated to Southeast Yunnan and began the cultivation of rice paddies in terraced hillside fields, forming a sustainable agroecosystem consisting of four major components: forests, villages, terraced rice paddies, and river systems ( Fig. 1) [10,11]. The evergreen forests control the water in the soil, acting like a natural reservoir to maintain the water year long, and also provide water for the villages and terraced rice paddies in lowlands through water channels built by Hani people [10]. Also, the hot and humid valley climate frequently generates a thick fog that helps to maintain moist air throughout the year. This unique four element-based Hani agroecosystem ensures a stable water supply. Consequently, the Hani terraced rice paddy fields did not suffer any significant damage from the historic 2009-2010 drought in China [2,12].
Due to this unique and complex agroecosystem, together with its rich biodiversity, much traditional ethnobotanical knowledge has been developed and accumulated by the local people, especially knowledge about WEP species. Since WEP species have not been domesticated and grown on a large scale, they must be obtained from the natural environment in order to be used as food [13,14].
In some parts of Yunnan, there has been a rapid replacement of complex agroecosystems by intensive monocultures of commercial crops, such as bananas, which is often accompanied by the use of inorganic herbicides and pesticides [15]. Rising awareness and concern about the possible health effects of pesticides and herbicides on human health has dramatically increased demand for organic foods in China [15]. This interest extends to WEP species as they are wild harvested. For example, many WEP species have made their way into ethnic minority recipes found on highend restaurant menus. Consequently, some WEP species have tremendous market potential and are particularly popular in tourist areas because of their perceived advantages of being pesticide-free, naturally grown, high in nutrients, and fresh in taste [13,16]. According to a Web of Science search of bibliometric and mapping knowledge domains, WEP species have always been an essential hotspot in ethnobotanical research [17]. WEP species in the Hani terraced rice paddy agroecosystem are often used to supplement daily food resources or to help to overcome seasonal food shortages [18]. Additionally, some WEP species possess medicinal properties that may help protect indigenous people against diseases [18,19].
Although the Hani people have lived in the Honghe Hani terraced rice paddy system for centuries, their traditional knowledge and associated biodiversity are rapidly being lost due to socio-economic changes and access to modern technologies [4,11]. Consequently, decreasing traditional knowledge will likely lead to a decrease in biodiversity, especially the diversity of WEP species [20]. Therefore, saving local traditional knowledge and protecting biodiversity are urgent [21]. To our knowledge, no previous studies have documented the WEP species in Hani terraced rice paddy agroecosystems. Thus, this investigation on the WEP species in Hani was conducted. This study recorded traditional knowledge of WEP species, which may protect it from disappearing in a rapid-developing era. The related research results may also provide scientific guidance for WEP species consumption, information of economic benefit to local communities for future sustainable development, and application of WEP species.

Study area
Before the field survey, a literature review was conducted to obtain information about the region of Hani terraced rice paddy fields, including climates, topography, vegetation types, and culture [22]. During 2014-2019, ethnobotanical studies were carried out in four counties (Yuanyang, Lüchun, Honghe, and Jinping), which cover more than 47, 000 ha, including most of the area containing Hani terraced rice paddy fields (Fig. 2) [23]. All study sites and their visit times are recorded in detail in Table 1. In consideration of local landscape diversity, this investigation was conducted in almost every landscape of this agroecosystem, including farming areas, forests, villages, home gardens, and water source areas [23]. Additionally, local markets in different villages and counties were surveyed repeatedly, as the  The data collected in the Honghe area was collated into an inventory containing all the WEP species and related information. The use-value (UV) of each WEP was calculated to evaluate the relative importance of each plant based on the number of times cited and the number of informants [28,29]. The formula for UV is UV ¼ U i is the times cited by each informant for a certain WEP, while N is the total number of informants [29]. The frequency of utilization index (FUI) of WEP species was graded according to the frequency of consumption by local people. FUI can also reflect the degree of closeness between WEP species and the local community [29]. The FUI scores range from 0 to 5 and varied by the consumption frequency (Table 2) [29].  Table 4). All WEP species were also classified by their edible parts ( Table 5). The recorded edible parts of WEP species included the whole plant, root, stem and leaf, flower, fruit, seed and shoot, and other parts like bark and tuber. For several WEP species, like Bauhinia acuminata var. candida and Senna tora, multiple parts can be consumed. These results embody the diversity of edible parts of WEP species in Honghe terraced rice paddy fields and indicate that local people have become well adapted to the local environment for centuries. The various uses and preparation methods are recorded in Table 6.
The plant stems and leaves are also collected widely (Table 6), and these are mostly consumed as a potherb, which is generally referred to as "wild vegetables" locally. The Hani people usually consume potherbs by stir-frying or by boiling them in a soup. The blended vegetables in soups are usually mixed with natural spices before eating. There are 16 species with edible flowers (Table 5), including Musa itinerans (bracts only). These edible flowers could be an essential source of nutrition for local people. It has been previously reported that edible flowers are rich in nutrients and micronutrients and that some of their extracts are useful as medicines [30][31][32]. Potherb is the most consumed group (Table 6) of WEP species in Honghe with 75 species (33.5%). In China today, wild vegetables, or "ye cai," have become popular food products that are increasingly being served in restaurants due to their flavor and a widespread perception of their superior nutritional values [33]. In the Honghe area, wild vegetables also play a vital role in local livelihood as food and dietary supplements. These wild vegetables are mainly collected in the mountains above the rice paddy fields and forest lands, and the collection time lasts from January to October but mainly occurs in the spring. Some plants, like Houttuynia cordata and Oenanthe javanica, can be collected throughout the year.
According to Table 5, edible fruit is the most popular group (98 species, 43.8%). These are usually consumed freshly without processing, which is the second most common food preparation method for the Hani WEP species (Table 6). Also, fruits can be consumed in several different ways. For example, Amomum maximum fruits are used locally as a natural spice that can help infirm people regain their appetite; the fruits of Ligustrum sinense are used by the local Hani people to brew a unique alcoholic drink, and Canarium album's fruits can be preserved into pickles.
Ten species of bamboo shoots can be made into different dishes that are high in nutritious fibers. Some WEP species in the Honghe region can also be used as natural flavoring agents (16 species), nuts (12), tea substitutes (11), liquor-brewing ingredients (8), grain substitutes (2), and special tofu (2). Exceptionally, there is only one species, Capparis masaikaii, that is used as a natural sweetener by local communities. The locals usually remove the seed coat and chew the kernel directly. C. masaikaii contains high levels of mabinlin, a sweet protein with 400 times the sweetness of sucrose but with meager calories, and consequently, this plant has a high potential for future application in the food industry [34].

Two special cases of WEP species
During our investigation, some unique cases of utilizing and processing WEP species were observed. In the Honghe area, Phyllanthus emblica bark is prepared in an unusual way (Fig. 4a). Local Hani people collect the P. emblica from mountainous forests, remove the branches, and peel off the outer layer of bark, grating off the bitter-tasting inner bark by using pottery shards. Traditionally, they adjust the bitter taste by mixing rice porridge paste with the tender inner bark. Then, the grated inner bark is mixed with roasted ribs, sliced pork liver, salt, and spices and eaten as a traditional dish. Besides its culinary use, P. emblica is also used medicinally for its potential anti-microbial, antioxidant and anti-tumor, hypolipidemic, hypoglycemic, and antihypertensive properties [35].
The traditional preparation of Dioscorea subcalva in cuisine is also distinctive. Local women first peel the thin skin from the D. subcalva tubers (Fig. 4). They then use a special tool to grate the peeled tubers into a container with a hot water-ash solution. When the solution has cooled, all of the grated tubers congeal into a sticky and elastic clump. These clumps can be cut into slices and stir-fried with meat. In another use of D. subcalva,              [36,37]. The exudate has high polysaccharide content and possesses good antioxidant bioactivity [36,37].

The UV and FUI value of WEP species in the Honghe area
Quantitative analyses were calculated to determine the local importance of each wild edible species. The use values (UV) and frequency of utilization indices (FUI) of each species were calculated. The 20 WEP species with the highest UV are listed along with their average FUI in Table 7.
Litsea pungens had the highest UV and average FUI ( Table 7). Because of its unique flavor and positive effects on human health, it has become the most commonly used edible species as a spice. Some local people even use the oil extracted from this species to repel mosquitos. Based on both local medical theory and scientific research, L. pungens can help to promote appetite and improve digestion [38]. Mentha canadensis is also a popular spice among local people, especially for cooking meat. However, its average FUI value and UV are relatively lower than for L. pungens. The second highest UV belongs to Phyllanthus emblica, while its average FUI value is similar to that of L. pungens. The high UV and average FUI values of   P. emblica may be attributed to its juicy and tasty fruits and its special cultural property: its tender bark is consumed in every October Festival and God Walled Festival. Several other plants were found to be popular as wild vegetables in our study area based on their high UV and average FUI, including the following: Acacia pennata, Ixeris polycephala, Amaranthus viridis, Centella asiatica, Colocasia gigantea, Crassocephalum crepidioides, Dregea volubilis, Elatostema involucratum, Houttuynia cordata, Oenanthe javanica, and Zingiber striolatum. For example, H. cordata is the most common wild vegetable in Southern China. Many modern scientific studies have indicated that this species possesses excellent antimicrobial, anti-cancer, anti-inflammatory, and immunoenhancement bioactivities [39,40]. C. gigantea is also a popular food plant, especially in Southwest China, and we found that the stem of C. gigantean contains high levels of nutrients and no heavy metals [41]. In addition, the inflorescence of Musa acuminata and Zingiber striolatum and the fruits of Ficus auriculata, Baccaurea ramiflora, and Musa acuminata are all relatively popular and important in local daily life.

The effect of WEP species on communities' economic income
Based on our interviews with key informants in local markets, the trading volume of WEP species was on a very small scale (less than 15 yuan each stall), which means selling WEP species could only bring a small income supplement and was usually unstable for local people. Therefore, driven by economic profits, many villagers have switched from growing rice to other economic plants like bananas in Hani terraced rice paddy fields. Many Hani informants reported that planting bananas can bring more income than growing rice. While in the short term, Hani farmers can get a higher income by growing bananas; they have to dry the rice paddy fields before planting bananas, which is against the Hani traditional ideas of sustainability. In doing so, the original construction and wetland habitats, as well as biodiversity, will be destroyed in the long term. Nevertheless, according to our observations, drying rice paddy to plant others was shown in different places in the Honghe region, especially in Jinping County.
The sources of and threats to the diversity of WEP species in the Honghe region Our investigation revealed the diversity of WEP species in the Honghe area. Several reasons contributing to local biodiversity and WEP diversity have been analyzed   5). The varied natural geographic environments and weather conditions are two of the main reasons for the diversity of WEP species. Secondly, the sustainable landscape structure constructed by the locals, including the four critical elements of forests, villages, terraces, and rivers, has a robust regulating ability, particularly for the regulation of essential water resources. Additionally, with the guidance of abundant traditional knowledge concerning reasonable agricultural management, excellent ecological benefits have been made to improve and maintain stability and biodiversity in the whole agroecosystem. Some Hani taboos, village regulations, and non-  5 The relationship between local biodiversity and its effect factors governmental agreements, as well as local religious beliefs like the worship of the mountain deity and magic woods, have restrained the behaviors of local people and protected the surroundings. However, the stability of Hani terraced rice paddy fields, which has been maintained for centuries, is now facing a series of challenges (Fig. 5). In our research area, traditional rice planting methods have been damaged by modernization. Based on our investigation, local young people prefer to work in urban areas to make more money instead of doing farm works in their hometowns. Traditional knowledge related to farmland management is only mastered by the older generation and is fading away rapidly (Table 3), and 18% of recorded species lack local Hani names. One reason for this lack of local names is that the Hani people are traditionally illiterate so that traditional knowledge can only be passed on orally by generations, so this knowledge is vulnerable to loss via acculturation. Although a writing system of the Hani language has been in place since 1957, it has not been widely adopted in the Hani communities. In addition, large-scale growing of hybrid rice requires less use of traditional agricultural methods and instead relies on pesticides and chemical fertilizers. Furthermore, the excessive exploitation of natural resources and the drying and changing of traditional rice terraces fields into economic fields are becoming increasingly frequent in the Honghe area nowadays. These phenomena are leading to a sharp decrease in the diversity of traditional knowledge and local biodiversity, which might damage the agroecosystem in this region [42,43].
Since 2013, when the Hani agroecosystem was elected into the UNESCO World Heritage List, tourism has increased markedly. In 2015, the tourism industry generated about 191.5 billion yuan and accounted for about 70% of local government revenues (out of 275.6 billion yuan). However, the local villagers have obtained minimal economic benefits from the local tourism industry. The traditional agroecosystem cannot sustain the daily food needs of the local people anymore. The Hani are now turning to the tourism industry, which may help to protect the traditional knowledge and biodiversity in this agroecosystem.

Conclusion
An ethnobotanical study on WEP species from the Hani terraced rice paddy agroecosystems in Southeast Yunnan, China, was conducted. Two hundred and twentyfive species (belonging to 170 genera and 90 families) of wild edible species and the information of their life forms, edible parts, and preparation methods were documented. Based on our analysis, the most widely eaten parts of WEP species are fruits, stem, and leaves. The most common processing methods for WEP species are cooking them as a potherb or eating them fresh. These results are closely related to the local lifestyle and reflect the local biodiversity. The use values (UV) of WEP species were also calculated, and the 20 species with the highest use value were listed. Compared with other WEP species, these 20 species are relatively more important to local daily life, and Litsea pungens, a local common natural spice, is the most popular WEP based on its high UV metric.
The reasons for local biodiversity and the challenges for local agroecosystem have been analyzed. This agroecosystem is facing severe problems concerning natural resource conservation, environmental protection, and the economic development of local communities in this agroecosystem. Prestigious designations like UNESCO World Heritage Site have helped to promote ecotourism, which has begun to improve the livelihood of local people while sustaining the operation of this agroecosystem.
In conclusion, there are abundant plant resources in the Hani terraced rice paddy field system because it is an ancient sustainable agroecosystem. However, in modern times, this region has suffered a series of threats. It is, therefore, critical to develop an effective way to protect it and to ensure its sustainability for its inhabitants.