An ethnobotanical study of the less known wild edible figs (genus Ficus) native to Xishuangbanna, Southwest China

Background The genus Ficus, collectively known as figs, is a key component of tropical forests and is well known for its ethnobotanical importance. In recent decades an increasing number of studies have shown the indigenous knowledge about wild edible Ficus species and their culinary or medicinal value. However, rather little is known about the role of these species in rural livelihoods, because of both species and cultural diversity. Methods In this study we 1) collected the species and ethnic names of wild edible Ficus exploited by four cultural groups in Xishuangbanna, Southwest China, and 2) recorded the collection activities and modes of consumption through semi-structured interviews, 3) investigated the resource management by a statistical survey of their field distribution and cultivation, and 4) compared and estimated the usage intensities by the grading method. Results The young leaves, leaf buds and young or ripe syconia of 13 Ficus species or varieties are traditionally consumed. All the species had fixed and usually food-related ethnic names. All four cultural groups are experienced in the collection and use of edible Ficus species as vegetables, fruits or beverages, with the surplus sold for cash income. Different cultural groups use the Ficus species at different intensities because of differences in availability, forest dependency and cultural factors. Both the mountain and basin villagers make an effort to realize sustainable collection and meet their own and market needs by resource management in situ or cultivation. Conclusions In comparison with reports from other parts of the world, ethnic groups in Xishuangbanna exploited more edible Ficus species for young leaves or leaf buds. Most of the edible species undergo a gradient of management intensities following a gradient of manipulation from simple field gathering to ex situ cultivation. This study contributes to our understanding of the origins and diffusion of the knowledge of perception, application and managing a group of particular plant species, and how the local culture, economic and geographical factors influence the process.


Background
The genus Ficus consists of over 800 species of trees, shrubs, vines and epiphytes in the family Moraceae, which have a wide distribution and multiple uses in most tropical and subtropical regions throughout the world. They are traditionally used as medicine or food plants, ornamental trees, religious plants, lacca hosts, fodder, fuel wood, hedges or enclosures. The importance of Ficus as a global spiritual and material resource for humans has been welldocumented [1,2].
Some Ficus species are reported to be among the oldest human food sources. Fossil evidence suggests that the common fig (Ficus carica L.) has been cultivated for over 11,000 years, possibly predating cereal grains [3], and thousands of cultivars of this species have been developed worldwide. The biblical sycamore fig (F. sycomorus L.) is another old human food source and one of the largest fruit producers. It was identified as a key food source for Pliocene hominids along the Baragoi River in Nachola and Baragoi, in northern Kenya [4]. Nowadays the most well-known species is F. carica, which produces the commercial common fig (fig is also the general name of the "fruit" of the genus). Specifically, the common fig is the syconium of F. carica var. domestica, which is functionally a female individual of F. carica. However, it was only in recent decades that it became known how many more culinary uses the genus Ficus can provide beyond their nutritious raw syconia. A growing number of studies have noted the significance of the edible Ficus species as vegetables [5][6][7][8][9], for tea or beverage preparation [10][11][12], for jelly and jam production [13] or for medicinal purposes [14][15][16][17].
Our previous ethnobotanical survey conducted in southwest Yunnan, China, found that Ficus was the most frequently consumed genus (with 8 species) of the 220 plant genera which contain species used as wild vegetables [6]. Ficus was also the most frequently used genus (7 species) among the 82 genera containing wild fruits in the region [18]. Specialized studies of these wild edible Ficus species are needed to clarify their ethnobotany, including vernacular names, modes of consumption, availability and management, and possible multiple uses. Since most of the species identified in these surveys are native to the Xishuangbanna Dai Autonomous Prefecture, a cultural and biodiversity hotspot in southwest Yunnan, China, a research project was initiated to estimate the current and historic usage of edible Ficus species in Xishuangbanna, not only for their economic benefits, but also for their cultural richness and their roles in the long history of rural livelihoods.

Study area
Xishuangbanna (XSBN) is in the south of Yunnan province, southwest China, bordering Myanmar and Laos. It has an area of almost 20,000 km 2 and is biogeographically located at the transitional zone with tropical Southeast Asia to the South, subtropical East Asia to the north, the Sino-Japanese floristic region to the east and the Sino-Himalayan floristic region to the west [19]. There are three seasons: a cool and foggy winter (November-February), a warm and dry 'summer' (March-April), and a warm and wet monsoon season (May-October). The region possesses an exceptionally diverse flora and 13 indigenous cultural groups have well-established ethnobotanical knowledge. Ficus is the most speciesrich genus in the region [19], with 69 species, subspecies or varieties native to the area [20]. Because of their close relationship with natural forests, all the native culture groups in XSBN have developed knowledge systems related to the use and conservation of natural resources. Wild collection is traditionally an important subsistence activity. Four ethnic villages near natural reserves inhabited by Dai, Hani, Jinuo and Yao people were selected as sample sites ( Table 1). The exact locations of the sample sites are withheld to protect the anonymity of the interviewees.). For each village, more than 95% of the villagers are indigenous. Relevant local markets were also visited.

Ethnobotanical data collection
Semi-structured interviews were conducted with 10-27 key informants in each village in March-October 2012, for details about the wild edible Ficus species, including their local nomenclatures, collection techniques and modes of consumption. The number of interviewees selected in each village mainly depended on the integrity and uniformity of information we obtained. Only those who could give details independently and according to their own experience, or could give a practical demonstration, were counted as key informants. Interviewees were first shown a group of sample species (photographs or fresh specimens) that were expected to be used. Species mentioned by informants that were not included in the samples were given special attention as new records. The Yao villagers living in Dazhai are monolingual, with only the village school students and staff able to speak Mandarin, so our interviews were conducted in the school with Yao students and teachers. Dai, Hani and Jinuo interviews were conducted in the villagers' homes, farming plots or collection sites using Mandarin or their own language, with the help of local field assistants.
Field investigations were designed to assess the availability of edible fig resources, including their field distribution and home cultivation. Since the mountain villages (Bakaxiaozhai, Dazhai and Nanbang) do not have private homegardens, they consume only wild Ficus. We chose Nanbang as a representative mountain village to assess the distribution of the fig individuals they use.
Six key informants were asked to guide field travel in the area surrounding their village in March 2012. Ficus individuals in dietary use and within one-hour walking distance (along twisting narrow footpaths in five directions) from the village site were recorded, including   F. tikoua Bur. Di ban teng, Di shi liu (ground pomegranate) -----muduoniang S121029009 F. vasculosa Wall. ex Miq. Tu mai rong, Shan tian cai (sweet mountain greens) pàk dé gái ------S120518004 F. virens Ait. Lv huang ge shu, Suan bao shu (sour buds tree) pàk yī niza bao neme adao gelong den S131201021 F. virens Ait. var. sublanceolata (Miq.) Corner Huang ge shu, Suan bao shu (sour buds tree) pàk yī -neme adao --S130901016 A Botanical names in brackets are frequently seen synonyms. B Name in brackets is English equivalent of the Mandarin name. C "--" means that the species is not reported as edible by the ethnic group. *Quote according to Wang and Long [21].
their species names, the numbers of plants, and their diameters at breast height (DBH). We chose "one-hour walking distance" to include most plots where the daily collection activities happen and the distance was accessible for all of our local guides. The Dai, who settle in valleys, basins or on river banks at lower elevations, are the major culture group in XSBN and have developed diverse homegardens. Most Ficus parts they eat come from these or from around their courtyards. We visited 107 households in Manlun village in May-June 2012 to collect data regarding the species, numbers of plants, and DBH of all edible Ficus species cultivated.
Observations of trading in Ficus products were conducted in three local markets related to the selected villages. They are the farm products market of 1) Menglun township, 2.2 km to Manlun and 5.7 km to Bakaxiaozhai, 2) Mengla township, 31 km to Nanbang, and 3) Jinghong city, which assemble farm products and wild collections from multiple ethnic groups and wide areas. All the villages can access their markets by motor vehicles. We selected Menglun market for long-term (November 2013 to April 2014) monitoring to collect basic data (species, price, sources, etc.) and determine the amounts sold and peak season, because the market has the most diverse Ficus products and modest size. We did market survey in Mengla and Jinghong during peak season to assess the universality of the trading activities. Only part of the result is shown in this study. More details on the amounts sold and their sources will be included in another publication because it needed additional investigations.

Data analysis
Based on the usage intensity classification for wild fruits of Chen et al. [18], we defined five levels of usage intensity according to our work described above. The five levels are coded as 1) -, no usage record; 2) +, consumed occasionally or just by children and hunters; 3) + +, frequently consumed and often gathered regularly during harvest season; 4) + + +, frequently consumed and the surplus may be sold in the local market or processed for out-of-season use, sources protected; 5) + + + +, cultivated in homegardens for consumption and sale.
All voucher specimens collected in our field work were deposited in the herbarium of the Xishuangbanna Tropical Botanical Garden (HITBC), Chinese Academy of Sciences.

Edible species and their ethnic nomenclature
Thirteen edible Ficus species or varieties and their corresponding local names were recorded. For F. maclellandii var. rhododendrifolia and F. vasculosa, the details were collected from the local markets. For the other 11 species, information was obtained by interviews of key informants in the four sample villages. The pronunciations of the Mandarin and ethnic names were recorded as accurately as possible in the Chinese phonetic alphabet ( Table 2).
In the Dai language, names of wild plants used as vegetables are often preceded by "pàk". The words "liāng" (reddish), "xiū" (green), "háo" (white), "núi" (smaller) and "lōng"  distinguished by local people are apparently not yet recognized taxonomically. Sometimes, the flavor is reflected in the plant name. For example, the Dai word for chicken, "gái." is used in the Dai name for F. vasculosa, describing the chicken-soup like taste of the young leaves used in vegetable soup. In the Hani language, "xibu" refers to the fig fruits borne in clusters on the trunk or thick leafless branches, while "xigu" refers to fruits borne in long and slender leafless braches from the trunk and near the ground. The words "ha" (bitter, here means inedible male figs), "ma" (bigger) and "qi" or "misi" (smaller) are often added after the formal name. The Hani word "niza" means a guest who stayed too long and can't be driven away, and is used for strangling fig trees! Typical strangler species, such as F. virens, are disliked by the Hani even though they know the leaf buds are edible.
In the Jinuo language, "neme" refers to leaf buds with a sour taste and "adao" is the common name for leaves. In the Yao language, "nuoge" is a common name for edible plants with white latex. The words "lumu" and "zamu" refer to "bigger" and "smaller" fig fruits. "Biu" is a common name for edible fruits, and "den" means young leaves or leaf buds.

Collection and form of consumption
All four culture groups use the young or ripe female figs and young leaves or leaf buds of multiple Ficus species as fruits, beverages or vegetables, with only minor differences in modes of consumption. Surplus young female figs of F. auriculata and young leaves or buds of six species are sold for cash income in local markets ( Figure 1). Generally, the appropriate harvest season for young leaves or buds is late winter to summer and for fruits the monsoon season (Table 3), but there are exceptions to this timing under both natural conditions and with human intervention, such as frequent pruning to prolong the crop life of young leaves or buds.

Resource management
Mountain villagers in Nanbang retain and protect the wild edible Ficus trees growing around the village in situ, and sometimes transplant individuals away from new farmland or road construction sites. Seventy four individuals of 7 species or varieties growing within one-hour walking distance from the village were recorded, mostly with a DBH of 0.10-0.15 m (Figure 2a). The villagers increase the production of young leaves and leaf buds by pruning during or out of the harvest season.
In the basin village of Manlun, 4 edible Ficus species and 1 variety were cultivated and 70 households (65% of the total) had them. The trees were grown in kitchen gardens or in and surrounding the home yard (Figure 3b, c, d). They were grown from branch cuttings or from seedlings transplanted from nature, except that most F. racemosa and a few F. virens individuals grew spontaneously from seed. The number of Ficus individuals owned by each household range from 1 to 9 (Table 4). Most are young trees and their DBH is less than 0.1 m (Figure 2b). The other two cultivated species, F. maclellandii var. rhododendrifolia and F. vasculosa, were not found in Manlun but in two other Dai villages according to the people who sold them in the market. Field surveys showed that F. maclellandii var. rhododendrifolia was planted as individuals by some households (Figure 3a), while F. vasculosa was planted in groups of small trees that can be managed and picked like tea (see lower part of the photo in personal cover page), so they are also known as "tea-leaf vegetables".

Comparative evaluation of the usage intensities and preference
Among the 13 edible Ficus, five species (F. auriculata, F. oligodon, F. semicordata, F. semicordata var. montana and F. virens) are common to all four culture groups. Only two of these (F. auriculata and F. virens), however, are cultivated for home and commercial use, and reached the highest usage intensities (+ + + +). The other four "+ + + +" species (F. callosa, F. maclellandii var. rhododendrifolia, F. vasculosa and F. virens var. sublanceolata) are mainly used by Dai people (Table 5).

Discussion
Comparison of the wild edible Ficus species uses among the four culture groups that they are widely accepted food resources rather than a narrow cultural preference. All the species had fixed and usually food-related ethnic names, which indicates the long history of indigenous consumption.
Different cultural groups use the wild edible Ficus species to different extents, depending on their availability, the group's dependence on forest resources, and cultural factors. Generally, the Dai people use them at the highest intensity because (i) they have been permanent inhabitants in XSBN for centuries, and have established homegardens for small-scale wild food or medicinal plant cultivation or domestication, and (ii) they live in basins and have better access to markets. The other three mountain culture groups have more recently established permanent living spaces in the region and do not have a culture of homegarden cultivation, depending more on forest collection. Our data show that the Hani people in Nanbang prefer fruits of F. auriculata and F. oligodon ("Xibu"). One of their orally transmitted legends tells that the first Hani people were born in a "Xibu" and survived by sucking the "milk" in it (the milky latex that characterizes figs). In addition, their ethnic epic records that "Xibu" is one of the first edible fruit plants they discovered in the forest during hunting activities. The villagers do not like strangling figs, such as F. alltissima and F. virens, since they often encounter huge strangling figs in the forest which have killed their host trees, and believe this is an omen of disaster. They therefore remove most of spontaneous seedlings around the village.
The significance of the cultivation and commercialization of the wild edible Ficus species The possibility of a wild plant resource continuing to meet both subsistence and market demands largely depends upon sustainable harvest by appropriate management, and the domestication of wild resources is crucial for resource management [22]. Domestication of common fig is thought to have started in the Mediterranean region in Early Neolithic period [3] and then spread worldwide. In XSBN, the Hani, Jinuo and Yao protect wild edible Ficus species while the Dai cultivate them. Except for the species traditionally cultivated in or around courtyards for ornamental and consumption purpose (such as F. auriculata), the cultivation of most Ficus species was triggered by the expansion of rubber plantations and resulting sharp decline in wild resource accessibility since the early 1980s. The indigenous villagers prefer to plant these species for their wide adaptability, high productivity, easy management and pleasant palatability. Ficus species are cultivated as tree fodder in many parts of the Himalaya region, with F. auriculata the most widely used species. Its fodder quality is far superior to paddy straw [23]. In the Bamileke region of Cameroon, Ficus species are propagated by pole cuttings and are an important part  of agrarian system management [24]. These examples show that wild Ficus species undergo a gradient of management intensities from simple gathering, to nonselective incipient management, selective incipient management and occasionally ex situ cultivation [25]. But whether or not the incipient domestication has occurred is unknown. The commercialization of wild edible Ficus species in XSBN is an important source of cash income for indigenous villagers. The leaves, buds and fruits of several Ficus species are sold in local markets and the whole plants are sold as ornamental trees. In other regions, however, only in north and central Vietnam are the near-ripe peeled or unpeeled fruits and young leaves of elephant figs (F. auriculata Lour. or F. oligodon Miq.) on sale in the market, and in Papua New Guinea the young leaves of dinner-plate figs (F. dammaropsis Diels.) are commonly sold in highland markets [8]. As Sawian et al. [26] reported, these products seldom appear to contribute a large share of a household's total income generation, but are often important in bridging seasonal or other cash flow gaps.

The characteristics of the wild edible Ficus species in Xishuangbanna compared to those in other regions
The use of wild Ficus species as food is widespread in areas where the genus occurs, especially in the Himalaya region, which is floristically similar to our study area. For the 13 edible Ficus species in this study, the consumption of 6 species has either not been reported from elsewhere (F. altissima, F. callosa, F. maclellandii var. rhododendrifolia and F. vasculosa), or only from South China (F. tikoua and F. virens var. sublanceolata). Consumption of the other 7 species had been reported from Nepal [7,27] and some were reported as eaten in India [9,13,28,29], North Laos [18], Vietnam [8] or Pakistan [16,30].
No other region appears to consume the diversity of wild Ficus species eaten in XSBN. Moreover, in the species consumed only in XSBN as well as those used most intensively, leaves and buds are the major parts consumed. These are concentrated sources of vitamin E, vitamin B 1 (thiamin), vitamin B 2 (riboflavin), protein and minerals [31], and are apparently also rich sources of naturally occurred antioxidants [32], suggesting that they may make a significant contribution to the health and well-being of the consumers. Antioxidant potential has also been demonstrated in some other Ficus leaf samples [33].

Conclusions
Our studies of wild, managed in situ and cultivated edible Ficus populations showed that their edible products are highly appreciated by the indigenous people of Xishuangbanna. We found that in both mountain villages, which have forest access but are far from markets, and basin villages, which have market access but no forests, figs are used as vegetables, fruits or beverages. Moreover, people in both situations invest effort in promoting the use of these species through artificial management. The Dai people who live in basin villages cultivate preferred species in and around their kitchen gardens and courtyards, encouraging intensive usage, with the possibility of artificial selection of plants with preferred characteristics. Further studies should be conducted to determine if these species are or can be ongoing incipient domestication. Finally, this study of a small geographic area suggests that the genus Ficus represents a largely untapped source of potential food resources for tropical people.