Garcinia in Southern China: Ethnobotany, Management, and Niche Modeling

Bo Liu, Xinbo Zhang, Rainer W. Bussmann, Robert. H. Hart, Ping Li, Yujia Bai & Chunlin Long

Economic Botany

ISSN 0013-0001 Volume 70 Number 4

Econ Bot (2016) 70:416-430 DOI 10.1007/s12231-016-9360-0

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1 23 Author's personal copy

Garcinia in Southern China: Ethnobotany, Management, and Niche Modeling

1,2,3 1 4 4 1 BO LIU ,XINBO ZHANG ,RAINER W. BUSSMANN ,ROBERT.H.HART ,PING LI , 1 ,1,5 YUJIA BAI , AND CHUNLIN LONG*

1College of Life and Environmental Sciences, Minzu University of China, Beijing, 100081, China 2Institute of Botany, Chinese Academy of Sciences, 100093, Beijing, China 3Shiwandashan National Natural Reserve, 538000, Fangchengang, China 4William L. Brown Center, Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299, USA 5Kunming Institute of Botany, Chinese Academy of Sciences, 650201, Kunming, China *Corresponding author; e-mail: [email protected]

Garcinia species are well known for being used traditionally in many different ways in Guangxi and Yunnan, China. To preserve this knowledge, this study recorded the ethnobotanical impor- tance of the genus Garcinia in this area. Ethnobotanical data were collected from seven prefec- tures in Guangxi (Baise, Chongzuo, Guilin, Fangchenggang, Hechi, Liuzhou, Qinzhou) and six prefectures in Yunnan (Dehong, Honghe, Lincang, Puer, Wenshan, Xishuangbanna) from dif- ferent ethnic groups. The data were collected in different seasons during 2008, and then again between 2010 and 2014, and 2016. A total of 250 informants were interviewed. Free listing methods, Smith’ S value, use frequency, semi-structured interviews, and potential distribution analysis were used to gather the data. Nine species were identified: Garcinia bracteata C. Y. Wu ex Y. H. Li, Garcinia cowa Roxb., Garcinia esculenta Y. H. Li, Garcinia multiflora Champ. ex Benth., Garcinia oblongifolia Champ. ex Benth., Garcinia paucinervis Chun & How, Garcinia pedunculata Roxb., Garcinia xanthochymus Hook. f. ex T. Anders., and Garcinia yunnanensis Hu. For each species, the field distribution, use knowledge, estimated usage intensities, prediction for potential distributions, and traditional management were recorded and analyzed. Conclusions are that (1) local knowledge of Garcinia species is diversified and influenced by ethnic groups. They are used as edible fruit, medicine, wood, ornamental plants, and extracting oil; (2) different ethnic groups share similar ideas regarding sustainable harvest and meeting their needs through resource management; and (3) with the rapid socio-economic changes in these areas, the traditional knowledge of the local people is being threatened.

藤黄属植物在中国广西和云南传统上有多种用途,为保护此传统知识,本研究记载了该地区 藤黄属传统用途的重要性。 我们分别自2008年、2010-2014年、2016年不同季节从广西的7 个市(百色、崇左、桂林、防城港、河池、柳州、钦州)和云南的6个市(德宏、红河、临 沧、普洱、文山、西双版纳)搜集当地不同民族的民族植物学资料。 本研究共访谈了250个 受访者,通过半结构式访谈、自由列举法、Smith’sS公式、使用频率和潜在分布区分析方法 获取和分析资料。共记载了9种:包括 Garcinia bracteata C. Y. Wu ex Y. H. Li, G. cowa Roxb., G. esculenta Y. H. Li, G. multiflora Champ. ex Benth., G. oblongifolia Champ. ex Benth.,

1 Received 9 July 2015; accepted 1 December 2016; published online 5 January 2017

Bo Liu and Xinbo Zhang contributed equally to this work.

Economic Botany, 70(4), 2017, pp. 416–430 © 2017, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. Author's personal copy

2017] LIU ET AL.: ETHNOBOTANY OF GARCINIA IN YUNNAN AND GUANGXI 417

G. paucinervis Chun & How, G. pedunculata Roxb., G. xanthochymus Hook. f. ex T. Anders., and G. yunnanensis Hu.。本文记载并分析了每个物种的分布、传统使用知识、估计使用频 度、潜在分布区预测及传统管理方式。 结果表明不同少数民族对于藤黄属植物的认知及使 用有不同的传统知识,藤黄属植物广泛用于食用水果、药物、木材、观赏植物和榨取油 脂;不同的少数民族通过就地资源管理或迁地栽培等方式来满足其自身可持续利用;如今,这 些相关传统知识随着快速的社会经济发展而受到威胁。 Key Words: Garcinia, ethnobotany, Guangxi, Yunnan, Tropical China, niche modeling.

Introduction recorded by Shizhen Li was utilized as medicine and pigment. Garcinia (Clusiaceae) comprises about 450 spe- Usages have not been well recorded in these two cies in a wide range of tropical habitats, often in richest areas with both biological and cultural diver- areas of great biological and ethnic diversity, includ- sity in China: Yunnan and Guangxi. In this region, ing tropical Asia, southern Africa, northeastern Aus- Garcina spp. have been used by different ethnic tralia, and tropical America. They are characterized groups such as Dai, Zhuang, Hani, Jinuo, Yi, by a brownish-yellow gum resin in the trunk, leaves, Dulong, and other local people for a long history. and fruits, which earns them the common name They developed different utilization modes and Bsap trees^ or in Chinese 藤黄 Ténghuáng (liter- management of the wild Garcinia resources. The ally means Byellow gum resin^)(Li1979). present research was carried out with the purpose of Garcinia species are well known for being tradition- recording the traditional knowledge of Garcinia ally used as fresh fruit, medicine, timber, and orna- used by different ethnic groups in Yunnan and mentation (Iwu and Igboko 1982;Yapwattanaphun Guangxi, making an assessment of the traditional et al. 2000); they are also important as animal food management modes, and using Garcinia collections sources (Wadsworth et al. 2005). Some species are to predict the potential range and provide suitable used as important plant resources by local people; areas for future utilization through cultivation. their status is an integral part of the culture and family-based economy of many traditional commu- nities. Garcinia fruits are berries with fleshy and Methods juicy mesocarps, which in most species can be eaten STUDY AREA raw. The most significant species in the genus is purple mangosteen (Garcinia mangostana L.), which Yunnan Province and Guangxi Zhuang Autono- is presumed to have originated in Southeast Asia or mous Region belong to Southwest China. This area Indonesia and has largely remained indigenous to is known as the Bkingdom of plants.^ So far, 25,998 the Malay Peninsula, Myanmar, Thailand, Cambo- species and intraspecific taxa have been recorded. Of dia, Vietnam, and the Moluccas (Akao et al. 2008). these, 9190 are endemic. The medicinal flora of Beyond the edible fruit, other widespread uses of Southwest China is composed of approximately Garcinia spp. include the use of the exocarp extract- 5751 species, representing 80% of China’smedici- ed from Garcinia multiflora (local name, h t điu nal flora (Chen 1994). màu) as a spice to flavor and to color the famous Yunnan Province is located in the far southwest bún riêu soup in Vietnam, and of Garcinia gummi- of China, bordering Vietnam, Laos, and Myanmar. gutta as a spice called kodumpulli which is widely It spans approximately 394,000 km2 and has a used in Kerala, India. population of 45.9 million. Yunnan is China’s In China, there are 19 species of Garcinia,of most diverse province, biologically as well as which 13 are endemic: 16 species occur in Yunnan culturally (Chow 2005;Yangetal.2004). Ecosys- or Guangxi (14 in Yunnan and 8 in Guangxi), tems of this province range from snow-capped Garcinia oligantha Merr. occurs in Guangdong mountains to true tropical environments, thus and Hainan, and Garcinia linii C. E. Chang and supporting an unusual full spectrum of species and Garcinia subelliptica Merr. occur in Taiwan (Li et al. vegetation types (Guo and Long 1998). The eastern 2007). The use of Garcinia spp. can be traced to half of the province is a limestone plateau with karst ancient China: the Compendium of Materia Medica landscape. Ethnic groups are widely distributed in (本草纲目 Ben cao gang mu (ca. 1592–1596) this province. Some 25 minorities live in compact Author's personal copy

418 ECONOMIC BOTANY [VOL 70 communities. Those in the tropical low mountain- management for certain Garcinias. While many ous areas with rich Garcinia plant resources include young people are moving to cities, only older people the Hani, Yao, Lahu, Wa, Jingpo, Bulang, and stay in these remote villages. Our informants only Jinuo. include around 45 young people, while the other Guangxi Zhuang Autonomous Region is immedi- 205 informants are in their 50s or older, and 60% ately east of Yunnan. It spans approximately of them are women. We had difficulty including 236,700 km2 and has a population of 52.8 million. younger informants, whereas older people are more Guangxi is in third position in terms of biodiversity patient and more willing to share their traditional in China, after Yunnan and Sichuan. It is located at knowledge. Women appear to hold more informa- low elevation below 1400 m, mostly at 100–600 m, tion about herbs, while men hold more information partly a mountainous region (calculated from Flora for trees or shrubs that grow on high mountains. of China (Wu et al. 1994–2013)). And men are more likely to transplant plants from The Nanling Mountains form the province’snorth- their natural habitat to their home gardens. east border, and the Tropic of Cancer runs through its At the beginning of the research, we conducted central region. It has a subtropical monsoon climate open interviews with tour guides and local leaders in zone. Limestone formations are widely distributed, villages. After obtaining prior informed consent with karst topography across ecotypes of subtropical from all interviewees, we asked what Garcinia spp. evergreen broad-leaved forest, subtropical evergreen they knew in the region. The composite list of monsoon forest belt, and north tropical seasonal forest. names was used to generate candidate species to Ethnic groups include the Zhuang, Yao, Miao, Dong, record uses and the cultural value. During the in- Mulao, Maonan, Jing, Shui, and Gelao. terview, we adopted the B5W + 1H^ method (Wang and Long 1995) and asked the following ETHNOBOTANICAL INVENTORY questions: What kind of wild Garcinia fruits do you eat? What is its name? Does this species have other Ethnobotanical surveys were undertaken to collect value? How do you use it? Finally, a total of nine information from local communities in seven prefectures Garcinia species were investigated as frequently used in Guangxi—Baise, Chongzuo, Guilin, Fangchenggang, species. Ethnotaxa of G. multiflora distinguished by Hechi, Liuzhou, Qinzhou—and six prefectures in locals were observed and the morphological differ- Yunnan—Dehong, Honghe, Lincang, Puer, Wenshan, ences were measured. In addition, observations of and Xishuangbanna (Fig. 1). Interviews took place in trading in Garcinia products were conducted in different seasons in 2008, and 2010–2014, 2016. local markets of all the investigated sites. During the investigations, ethnobotanical data were Specimens of target species were collected, exam- collected through different interview methods: ined, and identified by the authors and other tax- participatory rural appraisal (PRA), direct onomists and deposited in the Herbarium of the observation, semi-structured interviews, key infor- Minzu University of China (BMinzu^ for abbrevi- mant interviews, individual discussions, and focus ation) and the Institute of Botany, Chinese Acade- group discussions (FGD) (Chambers 1994; Long my of Sciences (PE). and Wang 1996). A total of ca. 250 informants were chosen using the complementary strategies of DATA ANALYSIS snowball, purposive, and convenience sampling across the investigation site and interviewed during Free listing is one of several structured group interviews (Bernard 2006). interviewing techniques designed to elicit systematic Yunnan and Guangxi host a large percentage of data about a cultural domain (Weller and Romney ethnic people (around 40–60%). Ethnic people 1988). In the present study, a total of 20 informants from the places we made investigations are mainly were randomly chosen from Zhugen village Zhuang, Yao, Miao, Yi, Dai, so on. After we got (Guangxi). This village is located near Mt. permissions from the local government, we got Shiwandashan. Local Zhuang people’s living largely recommendations from the governors for local relies on natural resources; hence, it is rich in tradi- herbal medicine doctors, and then ask them to tional knowledge and has a long history of cultivat- guide and translate for us. ing Garcinias in or near their home gardens. Local people in this region mainly rely on natural Since Garcinia are mostly known and used as resources for making a living. Different ethnic wild edible fruits, here we structured ethnobotanical groups have similar uses and traditional interviews for this use mode. Informants were asked Author's personal copy

2017] LIU ET AL.: ETHNOBOTANY OF GARCINIA IN YUNNAN AND GUANGXI 419

CHINA

Fig. 1. Investigated locations in Yunnan and Guangxi (dark dotted). Lower left, location of Yunnan and Guangxi in China.

questions like: Bcould you please list all the wild informant i listed in his/her user report; ROis is edible fruits you know about^ or inquire Bwhat ranking order of species s listed by informant i in kinds of fruits do you usually collect from the his/her user report; UFs is the final use frequency of ^ mountain? Data were weighted by the formula species. proposed by Smith (1993): using both the frequen- To produce an ecological niche model to assess cy of a species report across informants and the ’ possible future production of Garcinia for the po- sequence of a species report within an informant s tential distribution estimation of Garcinia, 1032 list to calculate a gross mean percentile rank for each specimen records of Garcinia collected from item across all lists. For a given informant, the Guangxi and Yunnan were retrieved from the percentile rank of an item A is calculated by the Chinese Virtual Herbarium (CVH) databases formula: (available at http://www.cvh.ac.cn). Seven hundred Total number of items in list− Rank order of S and twenty records could be georeferenced to Smith’s S Index ¼ TotalX number of items in list specific occurrence points. Nineteen bioclimatic ¼ UFXs UFis variables from global land area interpolation of UFis ¼ ðÞTNi−ROis =TNi climate point data (1950–2000 period) at a spatial resolution of 2.5 arc-min (Hijmans et al. 2005); available at http://www.worldclim.org)wereused UFs is the use frequency of species s; UFis is the as predictors for domain models embed in the use frequency of species s by informant i (ranking Diva-GIS software (Hijmans et al. 2001) to esti- from 0 to 1); TNi is the total number of items mate the potential distribution of Garcinia. Author's personal copy

420 ECONOMIC BOTANY [VOL 70

Results and Discussion groups (formerly for Jingpo people and now for Wa people) as important wild edible fruits and INVESTIGATED SPECIES AND THEIR FORM OF other uses. Garcinia paucinervis Chun & How is CONSUMPTION found only in rather dry sparse or dense forests in limestone mountains, and its only use is for its A total of 9 species were traditionally used from prestigious timber. For others not recorded in Ta- the 16 target Garcinia species. Traditional uses, ble 2, Garcinia xishuanbannaensis Y. H. Li and local names, and economic and ethnobotanical G. bracteata C. Y. Wu ex Y. H. Li have restricted applications were recorded from interviewees of distributions and no use reports have been found Dai, Yi, Yao, Han, Hani, Jinuo, and other ethnic during the investigation, while Garcinia nujiangensis groups (Table 1). The pronunciations of the C. Y. Wu & Y. H. Li in Y. H. Li, Garcinia tetralata Mandarin and ethnic names were recorded as C. Y. Wu ex Y. H. Li, and Garcinia lancilimba C. Y. accurately as possible in the Chinese phonetic Wu ex Y. H. Li were not found, nor recorded by alphabet (Table 2). local people due to their rare natural distribution Most species are traditionally most recog- areas and small populations. So we deduce that they nized and used as wild edible fruits, so most are not important economic plants due to the non- of the ethnonyms made reference to the fruit accessibility for local people. Garcinia kwangsiensis morphology, often beginning with an adjective Merr. ex F. N. Wei and Garcinia erythrosepala Y. H. and ending with a fruit type such as Bplum,^ Li have only type specimen records supplemented Bgourd,^ and Bpapaya.^ For instance, the by <10 additional specimens, all collected in the Zhuang name for G. multiflora is luowang Bbig 1930s and 1940s. gourd.^ Other ethnonyms make reference to the Among the use categories, the most frequent are branch morphology. For instance, the Zhuang edible fruits, followed by medicinal, wood, and ethnonym for Garcinia oblongifolia,whichiszhujie ornamental use (Fig. 2). Fruits are picked during guo Bbamboo-joint fruit,^ referring to opposite the period from July to December, which means leaves and vestigial stipules. that over a large part of the year fresh fruits are Seven species have relatively wider geographic available, not only for their nutritional value distribution, they are used by local people very (consisting of several vitamins, proteins, and min- often, and their individuals are abundant in the erals) (Kondo et al. 2009), but may also provide ecosystem: Garcinia bracteata, Garcinia cowa, pharmacologically active compounds. The multiple Garcinia esculenta, G. multiflora, G. oblongifolia, uses attest to the importance of these plants for and Garcinia xanthochymus. Many of these wide- subsistence and as a part of the local cultural heri- spread species can give local people substantial pro- tage (Shrestha and Dhillion 2006). ductivity, as each adult tree can produce about 60 kg fruits per year. Two species are not so com- USE FREQUENCY OF GARCINIA SPP. mon and have a restricted distribution: Garcinia pedunculata Roxb. and Garcinia yunnanensis Hu. During the ethnobotanical surveys, Garcinia spp. They serve for certain small-population ethnic were most frequently mentioned as wild useful

TABLE 1. NUMBER OF COUNTIES OF OCCURRENCE, SPECIMENS, AND USE MODE OF GARCINIA.

Species No. counties occurrence No. specimens No. use mode Garcinia bracteata C. Y. Wu ex Y. H. Li 17 111 1 G. cowa Roxb. 13 120 2 G. esculenta Y. H. Li 3 16 1 G. multiflora Champ. ex Benth. 46 255 4 G. oblongifolia Champ. ex Benth. 16 57 4 G. paucinervis Chun & How 8 64 3 G. pedunculata Roxb. 3 26 1 G. xanthochymus Hook.f.exT.Anders. 8 35 2 G. yunnanensis Hu 6 36 2 Author's personal copy

2017] LIU ET AL.: ETHNOBOTANY OF GARCINIA IN YUNNAN AND GUANGXI 421

TABLE 2. INVENTORY OF USE OF GARCINIA SPP. BY LOCAL YUNNAN AND GUANGXI PEOPLE IN CHINA.

Voucher specimen Mandarin and location Species Pinyin Ethnic name and number Mode of use/utilization Garcinia bracteata 尖叶藤黄Jiān Luo meng Shangsi, Guangxi Edible: ripe fruits eaten C. Y. Wu yè téng huáng (Zhuang people) 0729 (Minzu) raw, mesocarps tart and ex Y. H. Li sweet, for making spice, pickle and soup; seeds can be eaten when young G. cowa Roxb. 云树Yún shù Guomu bang, Geha Xishuangbanna, Edible: ripe fruit eaten raw hao (Dai people) Yunnan 0804 Medicinal (traditional Ma na (Jinuo people) (Minzu) Dai Medicine): sap of stems and leaves used externally to expel leech out of nose G. esculenta Y. 山木瓜Shān Wangdu xi man xi, di Malipo, Yunnan Edible: ripe fruit eaten raw H. Li mù guā rangxi (Jingpo 6826(PE) people),Bu nánb o (Dulong people) G. multiflora 木竹子Mù zhú Mikou, luo wang Hechi, Guangxi Edible: ripe fruit eaten raw Champ. ex zi/shānpípā) (Zhuang people) 1105(PE) Medicinal (traditional Benth. Bunang wa Lvchun, Yunnan Zhuang Medicine): (Dulong people) 0803(PE) bark medicinal, to stop bleeding, diminishing inflammation and relieving pain Wood: dark brown, hard, can be used for junk, furniture and carving use Ornamental G. oblongifolia 岭南山竹子 Chiguo, Maiya zai, Shangsi, Guangxi Edible: ripe fruit eaten raw, Champ. ex Lǐngnán shān zhujie guo & 0725 (Minzu) mesocarps tart and Benth. zhú zi/黄牙 Jiusuan Hechi, Guangxi sweet, for making spice 橘/huáng yá jú (Zhuang people) 0731 (Minzu) and pickle Medicinal (traditional Zhuang Medicine): bark for diminish inflammation and relieving pains, external use for burns and scalding Wood: hard, for making furniture and crafts Oil: the seeds oil is used as a lubricant and for manufacturing soap. Ornamental G. paucinervis 金丝李Jīnsī lǐ Mai gui, miyou bo Longzhou, Guangxi Wood: valuable timber Chun & How (Zhuang people) 0805 (PE) species, heart and Xishuangbanna, sapwood distinct, wood Yunnan 0706 hard and heavy, and (Minzu) fine structured, suitable for house beams, columns and building coffins Medicinal (traditional Zhuang Medicine): bark, branches and leaves used (Continued) Author's personal copy

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TABLE 2. (CONTINUED).

Voucher specimen Mandarin and location Species Pinyin Ethnic name and number Mode of use/utilization externally for burns and scalding Ornamental G. pedunculata 大果藤黄Dà guǒ Qini xi (Jingpo ethnic Yingjiang, Yunnan Edible: ripe fruit eaten raw Roxb. téng huáng group) 0806(PE) G. xanthochymus 大叶藤黄Dà yè Guo manda, ge mala, Xishuangbanna, Edible: ripe fruit eaten Hook.f. ex téng huáng mai mala(Dai Yunnan 1106 raw; young leaves T. Anders. people) (Minzu) cooked as vegetable Wai pi guoguo (Yi Cangyuan, Yunnan Medicinal (traditional Dai people, name for this 0608(PE) Medicine): sap of stems species or the whole and leaves used externally genus) to expel leech out of nose, Mala (Jinuo people) used orally for deworming Oil: the seeds yield up to 17% oil, which can be used for industrial purpose Ornamental G. yunnanensis 云南藤黄 Magei an Cangyuan, Yunnan Edible: ripe fruit eat raw Hu Yúnnán téng (Wa people) 1098(PE) Wood: for construction huáng/小姑 娘果Xiǎogū niáng guǒ fruits. There are three species used in Zhugen vil- reasons they were reported by most informants can lage: G. bracteata, G. multiflora,andG. oblongifolia. be summed up as follows: they are widely distribut- When free listing, people mentioned one of these ed in tropical monsoon forests near local people’s species and then immediately remembered the oth- houses, and they have multiple usages, including er two due to the morphological similarity, so dif- medicinal and ornamental uses. ferent species are treated as one entity in this We used a formula which considers the order investigation. of each informants’ free listing result, such that Fourteen wild useful fruit species are mentioned species listed earlier in the sequence are given a more than three times. Each informant has an aver- higher weight. In both ways of calculating, age list of 6.95 species, and Garcinia was mentioned Garcinia and Ficus auriculata are in the top 2, while by 70% informants first in their list (Table 3). The Passiflora edulis rises from the 6th in free listing to

Num.

8 7 6 5 4 3 2 1 0 Edible Medicinal Wood Ornamental

Fig. 2. Use mode of Garcinia in Yunnan and Guangxi, China. Author's personal copy

2017] LIU ET AL.: ETHNOBOTANY OF GARCINIA IN YUNNAN AND GUANGXI 423

TABLE 3. FREE LISTING TIMES AND USE FREQUENCY OF WILD USEFUL FRUIT SPECIES INVESTIGATED IN ZHUGEN VILLAGE, GUANGXI.

FTs (free listing UFs (use Local name Species Family times) Smith’sS frequency) Luo meng/luo Garcinia bracteata C. Y. Wu ex Y. H. Clusiaceae 14 0.928 7.473 wang/zhujie Li/G. multiflora Champ. ex guo Benth./G. oblongifolia Champ. ex Benth. Mugua rong Ficus auriculata Lour. Moraceae 12 0.857 4.864 Jidan guo Passiflora edulis Sims Passifloraceae 11 0.785 3.917 Shan lizhi Cornus hongkongensis Hemsl. Cornaceae 9 0.714 3.967 Sanyue pozi Rubus sp.(unidentified) Rosaceae 8 0.642 4.051 Zhudu guo Canthium horridum Blume Rubiaceae 6 0.571 1.514 Shan nianzi Rhodomyrtus tomentosa (Ait.) Hassk. Myrtaceae 6 0.500 2.998 Ye yangmei Myrica rubra Siebold et Zucc. Mytaceae 6 0.428 4.185 Kulu zi Melastoma dodecandrum Lour. Melastomataceae 6 0.357 1.890 Teng boluo Actinidia latifolia Actinidiaceae 5 0.285 1.500 (Gardner et Champ.) Merr. Shanlin guo Crataegus cuneata Siebold et Zucc. Rosaceae 4 0.214 2.733 Huotan mu Polygonum chinense L. Polygonaceae 4 0.142 1.005 Masha po Ficus hirta Vahl Moraceae 4 0.071 1.295 Baifan mu Saurauia tristyla DC. Actinidiaceae 4 0 0.686

3rd in use frequency. P. edulis is cultivated in many Shan zhuzi Bmountain bamboo fruit,^ so infor- home gardens for seasonal fruit and is highly valued mants who were asked Bwhat kind of fruit do you both for its edible fruit and ornamental value. This eat in the nearby mountains?^ may have been species was frequently mentioned by local people primed to recall Garcinia first. during the ethnobotanical interview. It can also In sum, Garcinia is both quickly recalled by serve as an example to show that use frequency most informants and most frequently listed as used captures well the importance of especially salient fruits in Zhugen, a typical tropical village with the items in free listing. However, it is possible that heritage of abundant traditional knowledge. These the use frequency scores for Garcinia could have species play an important role in providing local been inflated: one common name for Garcinia is people various vital nutritional elements as edible

Use Frequency

012345678 Garcinia bracteata /G. multiflora /G. oblongifolia Ficus auriculata Myrica rubra Rubus sp. Cornus hongkongensis Passiflora edulis Rhodomyrtus tomentose Crataegus cuneata Melastoma dodecandrum Canthium horridum

Fig. 3. Use frequency of species mentioned more than three times in Zhugen village, Guangxi. Author's personal copy

424 ECONOMIC BOTANY [VOL 70

FTs (Free Listing Times)

0 2 4 6 8 10 12 14 16 Garcinia bracteata /G. multiflora /G. oblongifolia

Ficus auriculata

Passiflora edulis

Cornus hongkongensis

Rubus sp.

Canthium horridum

Rhodomyrtus tomentose

Myrica rubra

Melastoma dodecandrum

Actinidia latifolia

Fig. 4. Top 10 wild edible fruit mentioned by free listing method in Zhugen, Guangxi. wild plants, and also with cheap and effective med- many Yi and Hani people do not distinguish icine. G. xanthochymus, for example, is a famous G. cowa from G. multiflora, older men are able to ethnomedicine in Xishuangbanna, southern Yun- tell the two species as different from each other nan. The Dai (called it as guomanda, guomala,or using bark characters: G. cowa is lighter and fis- mula), Hani (labie), and Jinuo (piduo)ethnicgroups sured, rough enough for easy climbing, whereas collect stem, bark, resin, leaves, and seeds for differ- G. multiflora is black and not fissured. ent purposes. The decoction of bark of During ethnobotanical interviews, the widely G. xanthochymus has been used to treat food poi- distributed species G. multiflora was classified into soning. The stems and leaves are local repellents, three ethnotaxa based on its diverse fruit morphol- especially used for anti-leeches (Figs. 3 and 4). ogy (Fig. 5). For instance, the ethnotaxon reported by a Yi person from Honghe, Yunnan, as Wai pi guo FOLK AND SCIENTIFIC CLASSIFICATION Bbeaked apex fruit^ (Fig. 5a) is oblong-ellipsoid, 3.5–5 × ca.3 cm, apex with a prominent beak, ± Local people recognized several ethnotaxa for longitudinally ridged or absent, in contrast with G. multiflora. All of these ethnotaxa were dis- Fig. 5b depressed globose, 2–2.5 × ca. 3 cm, apex tinguished using morphological characteristics. convex, prominently longitudinally six-ridged, and Although work in other regions has shown Fig. 5c depressed globose, 3–3.5 × ca. 3.8 cm, apex examples of local people using very few mor- convex, longitudinally six grooved. phological characters to identify species These different characters seem to be sta- (Tibuhwa 2012), we found most ethnotaxa to be ble in populations and appear as three quite comparable to scientific taxa. Given a similar level of different varieties from that described in taxonomic/ethnotaxonomic interest, multiple Flora of China: Bfruits ovoid to obovoid, 3–5× ethnotaxa recognized within a single scientific taxon 2.5-3 cm, smooth.^ The taxonomic status of these may be an important clue for the discovering of new ethnotaxa and the possible recognition of cryptic scientific taxa or the recognition of cryptic species species by locals remains an important avenue of (Berlin 1972;Berlinetal.1973). Morphology of future study. the fruit, the most useful part of a Garcinia tree, is considered as an important distinguishing character TRADITIONAL MANAGEMENT OF GARCINIA by locals. In all cases, people are aware of different taxa that are morphologically or phenologically iso- Economic species are commonly used in rural lated. One example of the deterioration of this areas and are essentially important to local people specificity was found in Xishuangbanna. Although, (Etkin 2002; Joshi et al. 2015;Sheretal.2015; Author's personal copy

2017] LIU ET AL.: ETHNOBOTANY OF GARCINIA IN YUNNAN AND GUANGXI 425

Fig. 5. Morphological differences in the fruits of G. multiflora.

Shrestha and Dhillion 2006;Yangetal.2015). It is and near the villages both in fresh fruits and pickles generally believed that local people are more likely made from the fruit mesocarp. The fruit price to support and participate in conservation initiatives ranges from 6 to 10RMB/kg(0.9 to 1.5 US dol- if they can receive direct benefits from such efforts lars/kg), and pickled mesocarp ranges from 12 to (Zou et al. 2010). Mountain villagers in the inves- 16RMB/kg(1.8 to 2.4 US dollars/kg). tigated area retain and protect the wild edible Jinuo people in Xishuangbanna, Yunnan, culti- Garcinia spp. growing around the village in situ. vate G. xanthochymus in traditional agroforestry sys- Although some species are common and sometimes tems on sunny slopes as the shade tree for tea are frequently seen in nearby tropical forests (Ta- (Camellia sinensis (Linn.) O. Kuntze). The area ble 2), local people prefer to cultivate them to get a around G. xanthochymus is covered by hay on the more steady harvest. ground, which informant A Mei told us is placed Zhuang, Jinuo, and Dai people have had con- both to prohibit the growth of weeds and to cushion ventions of cultivating Garcinia for a long time. In the falling of the fruit during harvest. Fangchenggang, Hechi, Guilin, and Guangxi, Patterns of use among species also reflect species about 40% of Zhuang people’shouseholdscultivate traits.InFangchenggang,southernmostGuangxi,local G. bracteata, G. multiflora,andG. oblongifolia,while Zhuang people cultivate all three of the local species: in Xishuangbanna, 60% of Dai and Jinuo people’s G. bracteata, G. multiflora,andG. oblongifolia.They households cultivate G. cowa, G. multiflora, and reported no taste difference in fruits from the three G. xanthochymus. species, but explained that the sequential phenol- Different ethnic groups have similar ogies of the three species provide fresh fruit for a methods for retrieving trees or saplings from longer time: G. bracteata usually have fruits in Au- mountains nearby: they will taste fruits from gust–October, G. oblongifolia in September–De- wild trees and choose the one they prefer, and cember, and G. multiflora in October–December. then transplant saplings to their home garden or backyard. There are no reports for people CURRENT AND PREDICTED SUITABLE using seeds to cultivate Garcinias. In 2 to 3 years, DISTRIBUTION FOR GARCINIA RESOURCES saplings are mature enough to bear fruits. Most households cultivate two to five trees in traditional Many different kinds of species distribution models home gardens to provide for themselves, while in have been used to predict potential distribution of Fangchenggang and Hechi, Guangxi, some house- species, including Classification and Regression Trees holds cultivate about 1 of 10 h of Garcinia trees in (CART), Bioclim (Busby 1991;Nix1986), Domain or near their homegarden to serve for local people in (Carpenter et al. 1993), and Genetic Algorithm for Author's personal copy

426 ECONOMIC BOTANY [VOL 70

0-1500 m 1500-8843 m

Fig. 6. Distribution map of Garcinia spp. in Yunnan and Guangxi.

Rule-Set Prediction (GARP) (Stockwell 1999). As Figure 8 shows the percent of suitable area pre- Domain is a relatively earlier modeling, the algo- cisely. In this map, the suitable area is much larger rithm is easy to understand and to operate with than the natural distribution. This may suggest the Diva-GIS (Busby 1991). existence of unsampled populations or places that Specimen collections of nine Garcinia spp. were are suitable for future cultivation. Most areas in retrieved, together with the distributions we Guangxi and south and west Yunnan bear suitable mapped during the ethnobotanical surveys. All data environments for one or more species as natural were coordinated on the map of Yunnan and populations or places for cultivation. Guangxi (Fig. 6). As we can see, the suitable distri- bution altitude for Garcinia is 200 to 400 m in most PHARMACOLOGICAL ACTIVITIES COMPARED WITH parts of Guangxi, while in Yunnan, most species are THE ETHNOBOTANICAL USES distributed from 400 to 1500 m in valleys in the southern part of the province. In North Yunnan Multidisciplinary approaches give ethnobotanists where the altitude is higher, there are a few more insight into the understanding of traditional specimen records belonging to three knowledge and indigenous usage. For instance, the species—G. multiflora, G. pedunculata,and medicinal chemistry of natural products can reveal the G. esculenta—all found in Gongshan County, dis- active compounds of edible and medicinal species, tributed in low elevations along the upstream of the and give reasonable explanations for usage patterns Lancangjiang River. (Cox 1994; Liu et al. 2014; Prance et al. 1994). In Seen from the richness map (Fig. 7), our analysis, we checked the traditional uses against Xishuangbanna is the richest in all areas with six the phytochemistry literature. Several phyochemical species, with Lincang and Honghe each having five studies show Garcinia spp. to diminish inflamma- species. Counties with more species are mostly lo- tion and relieve pains effects, as was reported by our cated in the southern part of the map where the informants. In addition, studies show many other climate is more tropical. The richness shows that properties not reported in our study, including Garcinia is a tropical distributed genus, and that it antifungal, anti-HIV, antimicrobial, antioxidant, plays an important role for ethnic groups living in antiviral, and cytotoxic (Shen et al. 2014;Thoison the low elevations near rivers. et al. 2000;Wuetal.2014). Thongtheeraparp et al. Author's personal copy

2017] LIU ET AL.: ETHNOBOTANY OF GARCINIA IN YUNNAN AND GUANGXI 427

<1<1 1-21-2 3-53-5 >6>6

Fig. 7. Number of Garcinia species calculated in county level in Yunnan and Guangxi.

(1994), Panthong et al. (2006), and Shen and Yang activity against food-borne pathogens and spoilage (2006) isolated xanthones from G. cowa which were bacteria. But for some species, especially shown by Negi et al. (2008) to have antibacterial G. yunnanensis and G. xanthochymus, there was little

Fig. 8. Suitable area (showed by dark gray girds) predicted for garcinias in Yunnan and Guangxi by Domain Modeling (True/False) in Diva-GIS. Author's personal copy

428 ECONOMIC BOTANY [VOL 70 phytochemical research reported, and their medici- knowledge and biological resources is of great nal use seems not fully recognized. significance.

Discussion Conclusion

In this article, we made field investigations to From the present study, we can conclude that understand traditional knowledge and traditional Garcinia species are well-known resources and used management for Garcinia. Niche modeling was in various ways by local people in Yunnan and used to explore more suitable areas for cultivating Guangxi. They are used as edible fruit, medicine, Garcinia in future development. wood, ornamental, and for extracting oil. The Traditionally, Garcinia canbeusedindifferent knowledge is diversified and dependent on sex, ’ categories. Among the use categories, the most fre- age, and ethnic group. Garcinias edible fruits and quent are edible fruits, followed by medicinal, other use modes are highly appreciated by the in- digenous people in Yunnan and Guangxi. They are wood, and ornamental use (Fig. 2). For the fruits collected from wild populations in the mountains, category, Garcinia is both quickly recalled by most cultivated in traditional home gardens, and sold in informants and most frequently listed as used as markets. They have great numbers of natural indi- fruits in local areas. Local people recognized their viduals and a large potential distribution area for own ethnotaxa and several ethnotaxa for cultivation. G. multiflora. All of these ethnotaxa were distin- Some phytochemical studies have been done to guished using morphological characteristics. help explain traditional uses of Garcinia. Future In our study, men generally knew more tradi- studies should focus on phytochemical investiga- tional use modes than women. One reason for this tions of less-studied but traditionally used species, may be that men go to the forest more frequently as well as taxonomic investigations of Garcinia than women to collect wild food and medicine and ethnotaxa. tend to range farther from home. Interviewees over the age of 50 years tended to have much more Acknowledgements – traditional knowledge. Those in the group of 30 We are grateful to all interviewed local people in 50 years of age occasionally appeared unsure, mis- Yunnan and Guangxi, leaders and local guides, and took one species for another, and were more likely colleagues and students at the Ethnobotanical Lab to use the same name for two different ethnotaxa. of Minzu University of China and Missouri Botan- Most of the people under 30 years old have left to ical Garden for their helpful comments and discus- find jobs in urban areas. Few remain in the villages. sions. We also thank Dr. Bo Pan from As suggested above, traditional knowledge asso- Xishuangbanna Tropical Botanical Garden, and ciated with Garcinia spp. shows a tremendous de- Hui An from Shiwandashan National Natural Re- crease with age: most young informants can only tell serve helped us to design and carry out field work. the local name of the three most frequently sold This work was financially supported by the Nation- cultivated species in the market and do not know al Natural Science Foundation of China other less used species. Nearly 90% of people in (31400182,31161140345,31400474), Minzu Zhugen village under 30 years of age migrate to University of China (YLDX01013), Ministry of large cities for college study or jobs and have little Science and Technology of China chance to go to the mountains collecting wild fruits, (2012FY110300), State Administration of Foreign preferring to buy fruit from the market. The erosion Experts Affairs of China (B08044), and China of ethnobotanical knowledge among the young is Scholarship Council. repeated not among the other villages in Guangxi, China, but also has been reported in eastern Brazil and southern Benin (Sogbohossou et al. 2015; Authors’ Contributions.CLL designed the Voeks and Leony 2004). This phenomenon can study, BL drafted the manuscript, XBZ, RWB, be found the nearly everywhere in the tropical RHH, CLL revised and finalized the manuscript, realm. Therefore, as in similar areas across the world BL, XBZ, PL, YJB and CLL participated in the field (Acharya and Acharya 2010; Acharya and Acharya surveys. All authors read and approved the final 2009), systematic documentation of indigenous manuscript. Author's personal copy

2017] LIU ET AL.: ETHNOBOTANY OF GARCINIA IN YUNNAN AND GUANGXI 429 Literature Cited Hijmans, R., Cruz, M., Rojas, E. and Guarino, L. 2001. DIVA-GIS version 1.4: a geographic in- Acharya, R. and K. P. Acharya. 2009. Ethnobotan- formation system for the analysis of biodiversity ical study of medicinal plants used by Tharu data, manual. community of Parroha VDC, Rupandehi dis- Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. trict, Nepal. Scientific World 7:80–84. Jones, and A. Jarvis. 2005. Very high resolution Acharya, K. P. and R. Acharya. 2010. Eating from interpolated climate surfaces for global land areas. the wild: indigenous knowledge on wild edible International Journal of Climatology 25:1965– plants in Parroha VDC of Rupandehi district, 1978. Central Nepal. International Journal of Social Iwu, M. and O. Igboko. 1982. Flavonoids of Forestry 3:28–48. Garcinia kola seeds. Journal of Natural Products Akao, Y., Y. Nakagawa, and N. Yoshinori. 2008. 45:650–651. Anti-cancer effects of xanthones from pericarps Joshi, N., M. Siwakoti, and K. Kehlenbeck. of mangosteen. International Journal of Molec- 2015. Wild vegetable species in Makawanpur ular Sciences 9:355–370. District, Central Nepal: Developing a priori- Berlin, B. 1972. Speculations on the growth of ty setting approach for domestication to im- ethnobotanical nomenclature. Language in So- prove food security. Economic Botany 69:1– ciety 1:51–86. 10. ———, D. E. Breedlove, and P. H. Raven. 1973. Kondo, M., L. L. Zhang, H. P. Ji, Y. Kou, and B. X. General principles of classification and nomen- Ou. 2009. Bioavailability and antioxidant effects clature in folk biology. American Anthropologist of a xanthone-rich mangosteen (Garcinia 75:214–242. mangostana) product in humans. Journal of ag- Bernard, H. R. 2006. Research methods in anthro- ricultural and food chemistry 57:8788–8792. pology: qualitative and quantitative approaches. Li, X. W. 1979. Guttiferae. Pages 1–112 in C. Y. Wu AltaMira Press, Oxford. and X. W. Li, eds., Flora Republicae Popularis Busby, J.R. 1991. BIOCLIM-a bioclimate analysis Sinicae. Beijing Academic Press, Beijing. and prediction system. In Nature Conservation: ———, J. Li, N. K. B. Robson, and P. F. Stevens. eds. Margules, C.R. and M.P. Austin. 1990. 2007. Clusiaceae through Araliaceae. in Z. Y. Cost Effective Biological Surveys and Data Anal- Wu, P. H. Raven, and D. Y. Hong, eds., Flora of ysis, 64-68. Melbourne: Canberra: CSIRO. China. Science Press & Missouri Botanical Gar- Carpenter, G., A. N. Gillison, and J. Winter. 1993. den Press, Beijing & St. Louis. DOMAIN: a flexible modelling procedure for Liu, B., Y. J. Liu, J. Q. Li, R. H. Gu, W. Cao, P. Li, mapping potential distributions of plants and ani- and F. F. Li. 2014. Aromatic lichen resources in mals. Biodiversity & Conservation 2:667–680. Guizhou Province, China. Medicinal & Aro- Chambers, R. 1994. Participatory rural appraisal matic Plants 3:1000146. doi:10.4172/2167- (PRA): challenges, potentials and paradigm. 0412.1000146 World development 22:1437–1454. Long, C. L. and J. R. Wang. 1996. The principle, Chen, S.K., 1994. Medicinal plant resources in method and application of participatory rural southwest China, and their exploitation and uti- assessment. Yunnan Science and Technology lization, Journal of Natural Resources 9(2):107- Press, Kunming. 111 Negi, P. S., G. K. Jayaprakasha, and B. S. Jena. Chow, C.S. 2005. Cultural diversity and tourism 2008. Antibacterial activity of the extracts from development in Yunnan Province, China. Ge- the fruit rinds of Garcinia cowa and Garcinia ography: 294-303. pedunculata against food borne pathogens and Cox, P. A. 1994. The ethnobotanical approach to spoilage bacteria. LWT-Food Science and Tech- drug discovery: strengths and limitations. Eth- nology 41:1857–1861. nobotany and the search for new drugs: 25-41. Nix, H.A. 1986. A biogeographic analysis of Aus- Etkin, N. L. 2002. Local knowledge of biotic diver- tralian elapid snakes. In Atlas of Elapid Snakes of sity and its conservation in rural Hausaland, Australia.(Ed.) R. Longmore, 4-15. Northern Nigeria. Economic Botany 56:73–88. Panthong, K., W. Pongcharoen, S. Phongpaichit, Guo, H. J. and C. L. Long. 1998. Biodiversity of and W. C. Taylor. 2006. Tetraoxygenated xan- Yunnan, SW China. Yunnan Science & Tech- thones from the fruits of Garcinia cowa. Phyto- nology Press, Kunming. chemistry 67:999–1004. Author's personal copy

430 ECONOMIC BOTANY [VOL 70

Prance, G.T., Chadwick, D.J. and Marsh, J. 1994. Ngorongoro and Serengeti National Park, Tan- Ethnobotany and the search for new drugs: John zania. Journal of Ethnobiology and Ethnomedi- Wiley & Sons Limited. cine 8:36. Shen, J. and J. S. Yang. 2006. Two new xanthones Voeks, R. A. and A. Leony. 2004. Forgetting the from the stems of Garcinia cowa.Chemicaland forest: Assessing medicinal plant erosion in East- Pharmaceutical Bulletin 54:126–128. ern Brazil. Economic Botany 58:S294–S306. Shen, T., W. Li, Y. Y. Wang, Q. Q. Zhong, S. Y. Wadsworth, J.W., Story, S.P., Zhou, B.N., Ogden, Wang, X. N. Wang, D. M. Ren, and H. X. Lou. R.V., Godbee, R.G., Palu A. K. and Jensen, C.J. 2014. Antiproliferative activities of Garcinia 2005. Garcinia mangostana L. enhanced animal bracteata extract and its active ingredient, food product. U.S. Patent Application. USA. isobractatin, against human tumor cell lines. Wang, J. R. and C. L. Long. 1995. Ethnobotanical Archives of Pharmacal Research 37:412–420. study of traditional edible plants of Jinuo nation- Sher, H., A. Aldosari, and R. W. Bussmann. 2015. ality. Acta Botanica Yunnanica 17(2):161–168. Morels of Palas Valley, Pakistan: A potential Weller, S.C. and A.K. Romney 1988. Systematic source for generating income and improving Data Collection: Sage. livelihoods of mountain communities. Econom- Wu, Z.Y., Raven P.H. and Hong, D.Y. 1994-2013. ic Botany 69:345–359. Flora of China. Beijing & St. Louis: Science Shrestha, P. M. and S. S. Dhillion. 2006. Diversity Press & Missouri Botanical Garden Press. and traditional knowledge concerning wild food Wu, S. B., C. L. Long, and E. J. Kennelly. 2014. species in a locally managed forest in Nepal. Structural diversity and bioactivities of natural Agroforestry Systems 66:55–63. benzophenones. Natural Product Reports 31: Smith, J. J. 1993. Using ANTHOPAC 3.5 and a 1158–1174. spreadsheet to compute a free-list salience index. Yang, Y. M., K. Tian, J. M. Hao, S. J. Pei, and H. Field Methods 5:1–3. X. Yang. 2004. Biodiversity and biodiversity Sogbohossou, O. E. D., E. G. Achigan-Dako, F. A. conservation in Yunnan, China. Biodiversity & Komlan, and A. Ahanchede. 2015. Diversity Conservation 13:813–826. and differential utilization of Amaranthus spp. Yang, L. X., S. Ahmed, J. R. Stepp, Y. Q. Zhao, M. along the urban-rural continuum of Southern J. Zeng, S. J. Pei, D. Y. Xue, and G. Xu. 2015. Benin. Economic Botany 69:9–25. Cultural uses, ecosystem services, and nutrient Stockwell, D. 1999. The GARP modelling system: profile of flowering quince (Chaenomeles speciosa) problems and solutions to automated spatial in the Highlands of Western Yunnan, China. prediction. International Journal of Geographi- Economic Botany 69:273–283. cal Information Science 13:143–158. Yapwattanaphun, C, Subhadrabandhu, S., Sugiura, Thoison, O., J. Fahy, V. Dumontet, A. Chiaroni, A., Yonemori, K. and Utsunomiya, N. 2000. C. Riche, M. V. Tri, and T. Sévenet. 2000. Utilization of some Garcinia species in Thailand. Cytotoxic prenylxanthones from Garcinia International Symposium on Tropical and Sub- bracteata. Journal of Natural Products 63:441– tropical Fruits 575, 563-570. Cairns, Australia. 446. Zou, X. B., F. Q. Huang, L. M. Hao, J. W. Zhao, Thongtheeraparp, W., P. Wiriyachitra, and W. C. H. P. Mao, J. C. Zhang, and S. Y. Ren. 2010. Taylor. 1994. Xanthones of Garcinia cowa. The socio-economic importance of wild vegeta- Planta Medica 60:365–368. ble resources and their conservation: a case study Tibuhwa, D. D. 2012. Folk taxonomy and use of from China. Kew Bulletin 65:577–582. mushrooms in communities around