Acta Societatis Botanicorum Poloniae Journal homepage: pbsociety.org.pl/journals/index.php/asbp INVITED REVIEW Received: 2012.09.18 Accepted: 2012.11.04 Published electronically: 2012.11.26 Acta Soc Bot Pol 81(4):263–270 DOI: 10.5586/asbp.2012.046 Food uses of ferns in China: a review Yujing Liu1, Wujisguleng Wujisguleng1,2, Chunlin Long1* 1 2 College of Life and Environmental Sciences, Minzu University of China, Beijing 100081, China Mongolian Medicine College, Inner Mongolia Medical University, Hohhot 010110, China Abstract Edible ferns are some of the most important wild vegetables in China. his paper reviews their food uses. he history of eating ferns in China may go back as far as 3000 years. An ethnobotanical inventory of edible ferns was created, with 52 species (including 4 varieties), which were traditionally used. he potential species number of edible ferns was estimated as 144 species (including 4 varieties). he cuisines, products and chemical components of ferns were also summarized. he most commonly eaten fern, Pteridium aquilinum var. latiusculum, was discussed in terms of its toxicity, massive productivity and development strategies. Suggestions and recommendations were proposed for the future development of edible ferns in China. Keywords: edible ferns, food uses, China, ethnobotany, Pteridium aquilinum var. latiusculum, pterosin, detoxiication Introduction Wild gathering, together with hunting, used to be the only food source for our ancestors. Although a total of 82 species commodities (or 103 species taxonomically) contribute 90% of national per capita supplies of food plants in the world [1], wild plant gathering is still a tradition that has endured in many local communities [2]. For example, the indigenous peoples of diferent countries, like Mexico [3], China [4–6], Ethiopia [7], India [8,9], Kenya [10], Palestine [11], and hailand [12] collect various wild plants for supplementary diets or substitutes for staple food in famine years. Food uses of wild plants are not only common in developing countries, but also in Japan, Europe and North America. For example many wild plants are still consumed in Spain, Portugal and Italy [13–15]. In some European countries, however, the tradition of wild food plant collection and consumption has been lost for generations. In Poland, for example, among over a hundred wild edible plant species recorded, only a few species are still commonly gathered, including two green vegetables, 15 folk species of fruits and seeds and four taxa used for seasoning, or as preservatives. he traditions of use of other species have either been forgotten or are very rarely used [16]. Both American Indians and white people have collected wild vegetables, fruits and mushrooms for consumption, in the United States and Canada [17–19]. In * Corresponding author. Email: long@mail.kib.ac.cn This is an Open Access digital version of the article distributed under the terms of the Creative Commons Attribution 3.0 License (creativecommons.org/licenses/by/3.0/), which permits redistribution, commercial and non-commercial, provided that the article is properly cited. © The Author(s) 2012 Published by Polish Botanical Society Japan, wild vegetables used to be important food resources in the cold northern parts. Local communities have developed preservation methods including pickling, salting and drying of edible wild plants to be used throughout all the seasons [20]. he number of edible wild plants occurring in Japan is estimated to be over 1000 species [21], or even around 2000 species [22]. However, only around 25 or less species were utilized on a regional scale [23]. Edible ferns are some of the most common wild food plants collected by people around the world. he fern stems, rhizomes, leaves, young fronds and shoots, and sometimes the whole plants are used for food. As early as the 1940s, Athyrium esculentum, Ceratopteris siliquosa, C. pteridoides, Dryopteris prolifera, Pteretis nodulosa, P. esculenta, and Helminthostachys sp. were reported as consumed by the indigenous Filipino [23]. In recent years, more and more research has reported the food uses of pteridophytes in diferent parts of the world. he fronds of Ophioglossum polyphyllum and those of O. nudicaule are cooked as a vegetable in Nepal. he fronds of Helminthostachys zeylanica are eaten as a salad in rural areas of Malaysia and the Philippines. Tender leaves of Botrychium lanuginosum are regarded as a delicious vegetable in Nepal [24]. Tree ferns have often been used as food and starch in Hawaii [24]. Both young fronds and underground stems of Asplenium ensiforme are used for food in the Himalayas. In Malaysia, the Blechnum orientalis rhizomes are eaten, and the fronds of Ceratopteris thalictroides and Diplazium esculentum are used as vegetables. The rhizome and young shoots of Nephrolepis biserrata are edible. Ophioglossum reticulatum is also eaten as a salad and as a vegetable [25]. In India, stems of Angiopteris sp. are eaten for starch. Pteris ensiformis, Helminthostachys zeylanica, Phymatosorus longissimus and Microsorum alternifolium fern fronds are also used for food. he Maori and Oceanic precedents collected the rhizomes of Petridium esculentum and made food in spring and early 264 Liu et al. / Food uses of ferns in China summer when the sweet potato or taro was not available [24,26]. he starchy paste of the sporocarps of Marsilea drummondii is made into cakes and is eaten by the natives of Australia [26]. here are about 10000–12000 species of pteridophytes in the world. In North America, 420 ferns and fern allies have been recorded. Some Asian countries are rich in pteridophyte diversity. For instance, 639 species of ferns occur in Japan, about 1000 in the Philippines, 550 in Malaysia, more than 700 in hailand, and about 600 in India [27–29]. China is one of the richest countries in pteridophyte species. About 2600 species, in 63 families and 230 genera have been reported in China, which occupies more than 20% of the global pteridophyte lora [27]. he Chinese people have traditionally used ferns for various purposes for many centuries. he indigenous uses include medicines (Cibotium barometz, Davallia mariesii and many others) [27,30,31], ornamentals (Neottopteris nidus, Nephrolepis auriculata and others) [27,32], and food as well. he food uses of ferns in China have been recorded in many ancient books. Some fern species such as Pteridium aquilinum var. latiusculum, Callipteris esculenta, Matteuccia struthiopteris, Osmunda japonica and Lygodium japonicum are very common in the country [27]. Local people, especially those from ethnic minorities in rural areas, have kept the tradition of collecting and eating ferns for many generations. So far, however, we cannot ind any ethnobotanical investigative reports on edible ferns in China. And there is no calculation of the number of fern species, which have traditionally been eaten by local people. his review will try to give an outline of edible ferns for traditional food uses in the ethnic communities of China. he species number of pteridophytes with edibility will be estimated. he future development of edible ferns will also be proposed in the present paper. Results Records of edible ferns in ancient Chinese literature Edible ferns were recorded for the irst time in “Shi-Jing” (“Book of Odes”), about 3000 years ago. Two species of ferns, Pteridium aquilinum var. latiusculum (or “juecai” in Chinese) and Osmunda japonica (or “weicai” in Chinese), appeared in the ode [33]. hese ferns are still oten collected and eaten in rural areas. he edible parts (fronds), collection time and morphology of ferns were described in the ancient books issued in the hree Kingdoms Period (called “San-Guo”, about 1800 years ago). he signiicance of edible ferns in livelihood had also been recorded in the literature of that period [33,34]. he time when eating ferns was most popular, was during the Tang Dynasty (AD 618–907). Many poets described, praised or admired edible ferns in their poems. he fronds of Pteridium aquilinum var. latiusculum and Osmanda japonica were the parts most commonly consumed by people in that period [33,35]. he irst written record of extracting starch for food from fern rhizomes was during the Song Dynasty (AD 960–1276) [36]. In the Yuan Dynasty (AD 1271–1368), the fern starch from Pteridium aquilinum var. latiusculum became very important and sometimes it became the main substitute for staple food in the famine years [33]. © The Author(s) 2012 How many species of ferns have traditionally been used for food in China? Edible ferns or fern products can be seen in local markets or supermarkets in China. However, nobody can tell how many species of ferns have traditionally been used for food in China. In Guizhou Province only, 64 edible fern species were reported in recent years, covering both traditional and potential edible species [36,37]. Based on literature studies [27,36–40], and our ield investigations over the past 20 years, we estimated that there are 52 species (including 4 varieties) of edible ferns traditionally consumed as food by various ethnic groups throughout the country (Tab. 1). Generally, ethnic minorities in the southwest region (especially Yunnan, Guangxi, Guizhou and Sichuan provinces) eat more fern species. Some species like Neottopteris nidus taste very bitter, but the local people in southern Yunnan still eat the young leaves as a precious vegetable. he most common species used as food in traditional communities are Pteridium aquilinum var. latiusculum (“juecai”), Callipteris esculenta, Osmunda japonica (“weicai”), Pteridium revolutum and Ceratopteris thalictroides. Among them, Pteridium aquilinum var. latiusculum is widely distributed in China. It grows massively and produces a lot of fronds in spring, while the rhizomes, with rich starch, can be harvested in the fall. his species has become the most popular edible fern, consumed by a billion people in China every year. For example, in the Zhuzhou County of Hunan Province only, the dry fronds of Pteridium aquilinum var. latiusculum (“juecai”) reached 1200 tons in 2011, with a value of 70 million RMB (ca. 1 million in US dollars) [41]. An estimated over 1000 companies in China produce dry “juecai” and its products. heir annual production values reach 300 million US dollars. Potential edible ferns in China he stems, rhizomes, fronds, young leaves and shoots, or the whole plants of many fern species can be used for food. he starch in the stems or rhizomes can be harvested, processed and cooked for food, or used to make liquor. he fronds, young leaves and shoots can be eaten as vegetables. Because of the inaccessibility of habitats, low biomass, lack of consumers, or for cultural, religious and legal reasons, many edible fern species have never, or hardly ever, been collected for food, or have not been recorded in any literature sources. For example, Metapolypodium memeiense (Christ) Ching, an epiphytic fern species in southwestern China, has been used as a taste-enhancer for cooking with vegetables by the Jinuo ethnic group in southern Yunnan. Tree ferns are CITES-listed species [42], and also listed in the “Red data book of China” [43]. hese species were not included in Tab. 1. Only Alsophila spinulosa in the tree fern group is an exception because of its larger population. Sometimes the local people collected the starch from stems which fell down in the forests. We estimated the potential species number of edible ferns, based on literature analysis [25,26,36–39], ield surveys, edibility investigation, and phylogenic or taxonomic information. he total number reaches at least 144 species, including 4 varieties (Tab. 1, Tab. 2). Among these 144 potential species (varieties) of edible ferns, the biggest groups are Allantodia (Athyriaceae, 30 spp.), Pteris (Pteridaceae, 20 spp.), Angiopteris (Angiopteridaceae, 18 spp.), Coniogramme (Hemionitiaceae, 15 spp.), Alsophila (Cyatheaceae, 14 spp.), Athyrium (Athyriaceae, 12 spp.), Asplenium (Aspleniaceae, 10 spp.) and Lygodium (Lygodiaceae, 10 spp.), in terms of species numbers in each genus. However, the fern Published by Polish Botanical Society 265 Liu et al. / Food uses of ferns in China Tab. 1 Ethnobotanical inventory of ferns used for food in China. No. 1 2 3 4 Species Name 6 Allantodia dilatata (Blume) Ching Allantodia gigantea (Bak.) Ching Allantodia himalayensis Ching Allantodia spectabilis (Wall. et Mett.) Ching Allantodia viridissima (H. Christ) Ching Alsophila spinulosa (Hook.) Tryon 7 Family Name Edible Parts Preparation Notes References Athyriaceae Athyriaceae Athyriaceae Athyriaceae Tender leaves Tender leaves Tender leaves Tender leaves Stir-fry, soup Stir-fry, soup Stir-fry, soup Stir-fry, soup Fresh or dry use Fresh or dry use Fresh or dry use Fresh or dry use [36] [36] [36] [27,36] Athyriaceae Tender leaves Sour taste [36] Cyatheaceae Starch in stems helypteridaceae 8 Angiopteris esculenta Hieron. Angiopteridaceae Young leaves and shoots Starch in rhizomes Substitute for staple food Fresh or dry use [37,39,40] Ampelopteris prolifera (Retz.) Cope. Cooked ater processing with salt Made into cakes or mixed with other food Stir-fry, soup [38–40] 9 Angiopteris fokiensis Hieron. Angiopteridaceae Starch in rhizomes 10 Asplenium unilaterale Lam. 11 Athyrium brevifrons Nakai ex Kitag. Aspleniaceae Athyriaceae Rhizomes Starch in rhizomes 12 Athyrium multidentatum (Doll) Ching 13 Athyrium pachyphyllum Ching Athyriaceae Fronds Substitute for staple food Substitute for staple food Fresh use Starch content 4050% Fragrant, tender Athyriaceae Fronds 14 Athyrium yokoscense (Franch. et Athyriaceae Sav.) Chrsit 15 Athyriopsis japonica (hunb.) Ching Athyriaceae var. oshimensis (Christ) Ching 16 Blechnum orientale L. Blechnaceae Fronds 5 17 Callipteris esculenta (Retz.) J. Sm. ex Moore et Houlst 18 Callipteris esculenta (Retz.) J. Sm. ex Moore et Houlst. var. pubescens (Link) Ching 19 Ceratopteris thalictroides (L.) Brongn. 20 Cibotium barometz (L.) J. Sm. 21 Coniogramme emeiensis Ching et Shing 22 Coniogramme intermedia Hieron. Young leaves Made into cakes or mixed with other food Made into cakes or mixed with other food Snack, salad Cakes, noodles Stir-fry, cooked with other food, soup Stir-fry, cooked with other food, soup Stir-fry, cooked with other food, soup Stir-fry, cooked with other food, soup Fried or stir-fried [36–39] [37–40] [36] [38–40] [38,39] Fresh or dry use [36,39] Fresh use or processing Fresh or dry use [36,39] Fresh or dry use [36,39] Stir-fry, soup, salad Fresh [27,36,38] [36,38] Athyriaceae Fronds and young red leaves Fronds Athyriaceae Fronds Stir-fry, soup, salad Fresh [36,39] Parkeriaceae Young leaves Stir-fry Fresh [27,37–39] Dicksoniaceae Starch in rhizomes Cakes, liquor Substitute for staple food [37–40] Hemionitiaceae Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Fronds, starch in rhizomes Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Cooked leaves as vegetable; noodles Fronds Stir-fry, soup Hemionitiaceae 23 Coniogramme intermedia Hieron. var. glabra Ching 24 Coniogramme japonica (hunb.) Diels 25 Coniogramme jingangshanensis Ching et Shing 26 Coniogramme robusta Christ Hemionitiaceae 27 Coniogramme rosthornii Hieorn. Hemionitiaceae Hemionitiaceae Hemionitiaceae Hemionitiaceae 28 Coniogramme simillima Ching ex Hemionitiaceae Shing 29 Coniogramme taipaishanensis Ching Hemionitiaceae et Y. T. Hsieh 30 Coniogramme wilsoni Hieron. Hemionitiaceae 31 Cornopteris decurrenti-alata (Hook.) Athyriaceae Nakai © The Author(s) 2012 Published by Polish Botanical Society [36,39] [36,39] [36,39] [36,39] [36,39] [36,39] [36,39] [36,39] [36,39] [36,39] Fresh or dry use [39] 266 Liu et al. / Food uses of ferns in China Tab. 1 (continued) No. 32 33 34 35 36 37 38 39 40 41 Species Name Cyrtomium fortunei J. Sm. Drynaria baronii (Christ) Diels Drynaria fortunei (Kunze) J. Sm. Lunathyrium acrostichoides Ching Lunathyrium coreanum (Christ) Ching Lygodium japonicum (hunb.) Sw. Marsilea quadrifolia L. Matteuccia intermedia C. Chr. Matteuccia orientalis (Hook.) Trev. Matteuccia struthiopteris (L.) Todaro 42 Nephrolepis auriculata (L.) Trimen. Family Name Edible Parts Preparation Dryopteridaceae Dryopteridaceae Drynariaceae Athyriaceae Athyriaceae Fronds Starch in rhizomes Starch in rhizomes Fronds Fronds Stir-fry, soup Source of starch Cakes, liquor Stir-fry, soup Stir-fry, soup Lygodiaceae Marsileaceae Onocleaceae Onocleaceae Onocleaceae Young leaves Young leaves Fronds Fronds Fronds, starch in rhizomes Stir-fry, soup Stir-fry, soup Stir-fry, soup Stir-fry, soup Stir-fry, soup; starch for noodle-making Nephrolepidaceae Young leaves, tubers 43 Neottopteris nidus (L.) J. Sm. Aspleniaceae 44 Ophioglossum polyphyllum A. Braun Ophioglossaceae 45 Osmunda japonica hunb. Osmundaceae Young leaves Fronds Fronds, starch in rhizomes 46 Osmundastrum cinnamomeum (L.) Osmundaceae Presl. 47 Polypodiodes niponica (Mett.) Ching Polypodiaceae 48 Pteridium aquilinum L. var. Pteridiaceae latiusculum (Desv.) Underw. Fronds 49 Pteridium revolutum (Bl.) Nakai Pteridiaceae Fronds, starch in rhizomes 50 Pteris wallichiana Agardh 51 Woodwardia japonica (L. f.) J. Sm. 52 Woodwardia unigemmata (Makino) Nakai Pteridaceae Blechnaceae Blechnaceae Tender leaves Starch in rhizomes Starch in rhizomes Tender leaves Fronds, starch in rhizomes products from these groups are rarely sold in local markets or are less consumed by the local people. Traditional fern cuisines he Chinese people in diferent areas have developed various methods to make fern dishes and food varieties. he most common dish is made of stir-fried fresh or dry fern fronds of Pteridium aquilinum var. latiusculum (“juecai”). here are various stir-fried dishes created by adding other food to the fern fronds. For example, chili peppers, Chinese leeks (Allium tuberosum), ham, or chicken can be stir-fried with fern fronds. Other species, like Allantodia gigantea, Athyrium yokoscense, Callipteris esculenta, Lygodium japonicum, Matteuccia struthiopteris, Osmunda japonica and Osmundastrum cinnamomeum have also been cooked following a similar formula. © The Author(s) 2012 Notes References Processed for storage [36,39] [39,40] [36,39,40] [39] [39] Delicious vegetable; starch content in rhizomes reaches 40–50% Cooked as vegetable, Young tubers with tuber eaten as snack sweetner Stir-fry, soup Bitter taste Soup Fresh or dry use Stir-fried or cooked with Fresh or dry uses, or other food, soup; starch processing. Delicious for making noodles, taste. Leaves contain liquor starch, too Stir-fried or cooked with Delicious taste other food, soup Cooked as vegetable Bitter taste Stir-fried or cooked with Commonly called other food, or processed. juecai. Fronds Starch used to make should be cooked noodles, liquor, cakes in boiled water and and other products then washed for a few hours. Widely distributed species in many areas Stir-fried or cooked with Makes similar other food, or processed. products as juecai Starch used to make liquor or cakes Stir-fry Fresh use Cakes, noodles, liquor Cakes, noodles, liquor [27,37,39] [27,36–39] [36,39] [36,39] [27,38–40] [36,39,40] [36] [25] [37–40] [37–40] [39] [27,37–40] [27,37–40] [27,37] [36–40] [36,39] Another popular dish is made of fern slices made from starch, either fried or steamed. he starch was usually extracted from the rhizomes of Pteridium aquilinum var. latiusculum. he slices could be prepared like Chinese bread, and then cooked in pots. Fern cakes are also common, made from fern starch. In the famine years, people collected the rhizomes in the mountains and extracted the starch as a substitute for staple food. Both fern fronds and starch are used to make porridge (congee), together with rice or millet. he fronds can be either fresh or dried, but need to be cut into small slices. Fern food products in China Both in local markets and supermarkets, there are a lot of fern food products in China. hese products can be Published by Polish Botanical Society 267 Liu et al. / Food uses of ferns in China Tab. 2 List of all edible fern genera in China. No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 Genus Name Allantodia R. Br. emend. Ching Alsophila R. Br. Ampelopteris Kunze Angiopteris Hofn. Asplenium L. Athyrium Roth Athyriopsis Ching Blechnum L. Callipteris Bory. Ceratopteris Brongn. Cibotium Kaulf. Coniogramme Fee Cornopteris Nakai Cyrtomium Presl. Drynaria (Bory) J. Sm. Gymnosphaera Bl. Lunathyrium Ching Lygodium Sw. Marsilea L. Matteuccia Todaro Metapolypodium Ching Nephrolepis Schott Neottopteris Schott Ophioglossum L. Osmunda L. Osmundastrum Presl. Polypodiodes Ching Pteris L. Sphaeropteris Bernh Woodwardia Smith Family Name Athyriaceae Cyatheaceae helypteridaceae Angiopteridaceae Aspleniaceae Athyriaceae Athyriaceae Blechnaceae Athyriaceae Parkeriaceae Dicksoniaceae Hemionitiaceae Athyriaceae Dryopteridaceae Drynariaceae Cyatheaceae Athyriaceae Lygodiaceae Marsileaceae Onocleaceae Polypodiaceae Nephrolepidaceae Aspleniaceae Ophioglossaceae Osmundaceae Osmundaceae Polypodiaceae Pteridaceae Cyatheaceae Blechnaceae Edible Parts Young leaves Starch in stems Young leaves Rhizomes Young leaves Young leaves Young leaves Fronds Young leaves Young leaves Starch in rhizomes Young leaves, starch in rhizomes Fronds Fronds, Satrch in rhizomes Starch in stems Fronds Young leaves Young leaves Fronds Leaves Young leaves, tubers Young leaves Fronds Young leaves, starch in rhizomes Young leaves, starch in rhizomes Tender leaves Tender leaves Starch in stems Starch in rhizomes stored or preserved for later. Common products include dried fronds, salted fronds, packaged fronds, fern starch, fern starch noodles, fern starch cakes, and fern leaf tea. When making fern starch noodles and cakes, wheat lour can be added and mixed. he fronds are mostly from two species, Pteridium aquilinum var. latiusculum (“juecai”) and Osmunda japonica (“weicai”). he former occupies more than 80% of the fern food market. Both species are exported to international markets. he starch for making food products comes mainly from the rhizomes of Pteridium aquilinum var. latiusculum. he season for harvesting rhizomes is from September to November, when the aerial parts of the ferns become withered. People use the fern starch to produce other products, such as liquor and soft drinks. Before they make liquor, other materials like rice, sweet potato or corn lour can be added to the fern starch. Nowadays, many varieties of fern products have been developed. he canned ferns, spicily seasoned ferns, dehydrated ferns, salted ferns and other products can easily brought in the markets in all seasons. Chemical components of edible ferns and their bioactivities Many researchers have reported the chemical constituents of diferent edible ferns. Nine compounds have been isolated © The Author(s) 2012 Species No. in China Edible species (estimated number) 73 14 (incl. 2 varieties) 1 20 110 82 10 1 3 (incl. 1 variety) 2 2 20 11 40 9 9 48 (incl. 10 varieties) 10 3 3 1 6 11 5 3 2 12 50 2 5 30 14 1 18 10 12 3 1 2 2 1 15 6 4 8 9 5 10 1 3 1 2 2 1 3 2 3 20 2 5 from the fronds of Pteridium aquilinum var. latiusculum, the most common edible fern in China. hey are daucosterol, trans-tiliroside, adenosine, wallichoside, inkosterone, rutin, pterosin A, ponasterone A and quercetin [44]. Matteuccia struthiopteris is also a commonly consumed edible fern species. he compounds found in this species include 1-O-β-D-glucopyranosyl-(2S, 3R, 4E, 8z)-2-N-(2'-hydroxydocosanoyl) eicosasphinga-4,8-dienine, 1-O-β-galactosyl-(6→1)α-β-galactosyl-2,3-O-dihexadecanoyl-glycerol, succinic acid, D-mannitol, demethoxymatteucinol, matteucinol, pinosylvin, matteuorien, pinosylvin 3-O-β-D-glucopyranoside, matteuorienate A [45,46]. Many chemical compounds are reported in Pteris [47,48]. These are, for example, apigenin-7-O-β-Dglucopyranosyl-4'-O-α-L-rhamnopyranoside, luteolin-7-Oβ-D-glucopyranoside, apigenin-7-O-β-D-glucopyranoside, apigenin, luteolin, naringenin-7-O-β-D-neohesperidoside, apigenin-7-O-β-D-neohespedoside, apigenin-4'-Oα-L-rhamnopyranoside, (2S,3S)-pterosin C, isovanillic acid, ferulic acid, 2β,16α-dihydroxy-ent-kaurane 2-O-β-D-glucoside, 2β,6β,15α-trihydroxy-ent-kaur-16-ene, 9-hydroxy-15-oxo-ent-kaur-16-en-19-oic acid 19β-Dglucoside, 2β,14β,15α,16α,17-pentahydroxy-ent-kaurane, and 9-hydroxy-ent-kaur-16-en-19-oic acid. Some extracts from Pteris showed antitumor, antifungal and antibacterial activity. Published by Polish Botanical Society 268 Liu et al. / Food uses of ferns in China Some of the compounds had an inhibitory efect on platelet aggregation, as well as an anti-inlammatory efect [49]. Pterosins, terpenoids, sterides, lavones, glucosides, aromatic, and pyrone compounds were isolated from Cibotium barometz [50]. heir pharmacological efects, such as antihaemorrhagic, bacteriostatic, antiosteoporotic, anticancer, and hepatoprotective, have been tested [31]. A representative species in Athyriaceae, Callipteris esculenta, has also been studied phytochemically. Such compounds as β-sitosterol, stigmast-4-ene-6β-ol-3-one, stigmast-4-ene-3,6-dione, benzeneacetic acid, glycerol-1,3dihexadecanoate, 3β-hydroxy-5α,8α-epidioxyergosta-6,22diene, stigmast-4-ene-3β,6β-diol, stigmast-5-ene-3β,7α-diol, stigmast-4-ene-6α-o1-3-one, and daucosterol have been isolated from the fronds of this species [49]. Chemicals from Nephrolepls cordifolia have also been isolated. hey were identiied as β-si-tosterol, fern-9(11)-ene, oleanolic acid, myristic acid octadecylester, hentriacontanoic acid and triacontanol [51]. Discussion and suggestions Toxicity of Pteridium aquilinum var. latiusculum Bracken fern, or Pteridium aquilinum, is the most controversial species. Its fronds and starch have been eaten by billions of people in the world. However, it is a problematic, dangerous and poisonous plant due to its special chemical composition, especially the content of ptaquiloside (PT), a highly carcinogenic compound. It has been found that PT is present in all parts of the plant, including fronds, leaves, rhizomes, and roots. he highest concentration of PT (average at 3800 μg/g) is in the frond growing season, while the PT contents of roots are the lowest (5–230 μg/g). In the rhizomes, the PT contents are less than 1200 μg/g in general [52]. Diferent types of human carcinomas (oesophageal, gastric cancers, etc.) are produced by ingestion of bracken fern or milk from bracken-fed cattle [53]. Even nowadays, because of its wide distribution and easy accessibility, bracken fern has been collected as part of the diet by many poor people, from south Paciic islands to northern, temperate prairies. Botanically, the taxon massively collected by local people in China as food is a variety of Pteridium aquilinum. Unfortunately, this lower taxon (Pteridium aquilinum var. latiusculum, in Chinese it is also called “juecai”, “longzhuacai” or “ruyicai” commonly) has also been proven to be poisonous because PT has been detected in this subspecies [54]. hus, we should warn the public that “juecai” (including fronds, starch and their products) is poisonous and harmful to human health. However, it is a strong part of traditional food culture to collect and eat ferns in the most rural regions of China. And “juecai” (Pteridium aquilinum var. latiusculum) is the most important food fern among all edible pteridophytes for both household consumption and commercial purposes. We cannot stop Chinese people eating juecai. he only solution is to remove toxins from “juecai” in an easy and cost-efective way. Fortunately, PT is unstable in water. his compound will also decompose under acidic or alkaline conditions. his is the reason why very few people have sufered from eating “juecai”, because people usually wash it in water for hours or even a few days to remove the bitter lavor. herefore detoxiication is very easy when processing “juecai” and its products, even in the © The Author(s) 2012 countryside. It is strongly encouraged that the fresh fronds or starch from Pteridium aquilinum var. latiusculum are washed in water, or placed under acidic or alkaline conditions, for a few hours before eating or making products. Further research Among China's 196 edible fern species, including the potentially edible species (144 spp.) and those traditionally used as food (52 spp.), only 10% have been studied phytochemically. Chemical constituents of other edible fern species, in particular the possible toxins, should be examined carefully. he contents of PT in the Pteridium aquilinum var. latiusculum (“juecai”) plant may be diferent from one place to another. Studies carried out in New Zealand, Australia, Costa Rica and Venezuela revealed that the PT contents for bracken fern fronds (from 12 stands of four geographically distinct habitats) were found between 210 and 2150 μg/g, this variation was positively correlated with development phases and altitudes [55]. herefore, it is necessary to study the PT contents in diferent populations or geographical origins of “juecai”. Most fern species grow slowly (“juecai” is an exception). It is necessary to grow edible ferns for commercial development artiicially or semi-artiicially. As ferns produce numerous spores, mass propagation and production of edible ferns from spores for commercial production should be studied. he micropropagation techniques of edible ferns (especially the rare species) can be encouraged, too. Suggestions for production and toxicity examination of edible ferns In China, there are thousands of companies producing edible fern products. he contents of PT and other poisonous compounds in edible ferns and fern products should carefully be examined before they appear in commercial markets. hose with higher PT content must not be allowed onto the market. Raw materials from Pteridium aquilinum var. latiusculum and allied species should be double-checked. he governmental food and drug administrative authorities at diferent levels should issue criteria for quality/safety control of edible fern products. Every edible fern enterprise should follow the criteria, especially the content limitation of PT in the products. It will be helpful to identify the origin of raw fern materials, because the contents of PT are very diferent based on their geographical locations. he practice of placing a certiicate of origins with low PT contents on edible fern products should be encouraged. Recommendations of a few fern species Based on our investigation, we recommend the following edible fern species for future commercial development in China: (i) Athyrium multidentatum is a common fern species in northeast China. It is called “houtui” in Chinese, which means monkey legs because of the yellow hairs on the petioles. he fronds of Athyrium multidentatum are very tasty and fragrant. Both fresh and processed fronds can be stir-fried or cooked for soup. (ii) Matteuccia struthiopteris also occurs in northeast China. In Chinese it is called “Huanggua Xiang”, which means it has a cucumber (“Huanggua”) lavor. he young leaves can be cooked as a delicious dish or used to make dumplings. (iii) Osmunda japonica is a widely distributed species. Its production, however, has decreased over the last two decades. Published by Polish Botanical Society Liu et al. / Food uses of ferns in China People overharvested it because the products made from its tasty fronds were exported to Japan as well as consumed in domestic markets. Artiicial cultivation of this fern will hopefully meet the demands of international markets. (iv) Ophioglossum polyphyllum is distributed in the tropical and subtropical areas. In Tibet it is eaten in summer as a vegetable but also dried and stored for further consumption in winter. Previous studies revealed that it contains high levels of essential amino-acids that can complement the local diet [25]. It can be developed as a cultivated species in southern China. Acknowledgements his study was supported by the National Natural Science Foundation of China (Nos. 31161140345 & 31070288), the Ministry of Education of China through its 111 and 985 projects (Nos. B08044, MUC985-9 & MUC98506-01000101), and the Ministry of Science and Technology of China (2012FY110300). References 1. Prescott-Allen R, Prescott-Allen C. How many plants feed the world? Conserv Biol. 1990;4(4):365–374. http://dx.doi.org/10.1111/j.1523-1739.1990. tb00310.x 2. Turner NJ, Łuczaj ŁJ, Migliorini P, Pieroni A, Dreon AL, Sacchetti LE, et al. Edible and tended wild plants, traditional ecological knowledge and agroecology. Cr Rev Plant Sci. 2011;30(1–2):198–225. http://dx.doi.org/ 10.1080/07352689.2011.554492 3. Quelites BR. Ethnoecology of edible greens. Past, present and future. J Ethnobiol. 1981;1(1):109–123. 4. Wujisguleng W, Khasbagen K. An integrated assessment of wild vegetable resources in Inner Mongolian Autonomous Region, China. J Ethnobiol Ethnomed. 2010;6(1):34. http://dx.doi.org/10.1186/1746-4269-6-34 5. Ge XG, Ning W, Fan WL. he status and development of wild vegetable in China. Applied Engineering Technology in Rural Areas: Greenhouse Horticulture. 2005(7):14–16. 6. Wang JR, Long CL. Ethnobotanical study of traditional edible plants of Jinuo nationality. Acta Bot Yunnan. 1995;17(2):161–168. 7. Balemie K, Kebebew F. Ethnobotanical study of wild edible plants in Derashe and Kucha Districts, South Ethiopia. J Ethnobiol Ethnomed. 2006;2:53. http://dx.doi.org/10.1186/1746-4269-2-53 8. Misra S, Maikhuri RK, Kala CP, Rao KS, Saxena KG. Wild leafy vegetables: a study of their subsistence dietetic support to the inhabitants of Nanda Devi Biosphere Reserve, India. J Ethnobiol Ethnomed. 2008;4(1):15. http://dx.doi.org/10.1186/1746-4269-4-15 9. Jain A, Sundriyal M, Roshnibala S, Kotoky R, Kanjilal PB, Singh HB, et al. Dietary use and conservation concern of edible wetland plants at indoburma hotspot: a case study from northeast India. J Ethnobiol Ethnomed. 2011;7(1):29. http://dx.doi.org/10.1186/1746-4269-7-29 10. Orech FO, Aagaard-Hansen J, Friis H. Ethnoecology of traditional leafy vegetables of the Luo people of Bondo district, western Kenya. Int J Food Sci Nutr. 2007;58(7):522–530. http://dx.doi. org/10.1080/09637480701331163 11. Ali-Shtayeh MS, Jamous RM, Al-Shaie' JH, Elgharabah WA, Kherfan FA, Qarariah KH, et al. Traditional knowledge of wild edible plants used in Palestine (Northern West Bank): a comparative study. J Ethnobiol Ethnomed. 2008;4(1):13. http://dx.doi.org/10.1186/1746-4269-4-13 12. Cruz-Garcia GS, Price LL. Ethnobotanical investigation of “wild” food plants used by rice farmers in Kalasin, Northeast hailand. J Ethnobiol Ethnomed. 2011;7(1):33. http://dx.doi.org/10.1186/1746-4269-7-33 © The Author(s) 2012 269 13. Pardo-de-Santayana M, Tardío J, Blanco E, Carvalho A, Lastra J, San Miguel E, et al. Traditional knowledge of wild edible plants used in the northwest of the Iberian Peninsula (Spain and Portugal): a comparative study. J Ethnobiol Ethnomed. 2007;3(1):27. http://dx.doi. org/10.1186/1746-4269-3-27 14. Ghirardini M, Carli M, Del Vecchio N, Rovati A, Cova O, Valigi F, et al. he importance of a taste. a comparative study on wild food plant consumption in twenty-one local communities in Italy. J Ethnobiol Ethnomed. 2007;3(1):22. http://dx.doi.org/10.1186/1746-4269-3-22 15. Lentini F, Venza F. Wild food plants of popular use in Sicily. J Ethnobiol Ethnomed. 2007;3(1):15. http://dx.doi.org/10.1186/1746-4269-3-15 16. Łuczaj Ł, Szymański WM. Wild vascular plants gathered for consumption in the Polish countryside: a review. J Ethnobiol Ethnomed. 2007;3(1):17. http://dx.doi.org/10.1186/1746-4269-3-17 17. Cavender A. Folk medical uses of plant foods in southern Appalachia, United States. J Ethnopharmacol. 2006;108(1):74–84. http://dx.doi. org/10.1016/j.jep.2006.04.008 18. Turner NJ. Food plants of interior First Peoples. Victoria: Royal British Columbia Museum; 2006. 19. Kuhnlein HV, Turner NJ. Traditional plant foods of Canadian indigenous peoples: nutrition, botany, and use. In: Katz S, editor. Food and nutrition in history and anthropology. Philadelphia PA: Gordon and Breach Sicnece Publishers; 1991. (vol 8). 20. Cetinkaya G. Challenges for the maintenance of traditional knowledge in the Satoyama and Satoumi ecosystems, Noto Peninsula, Japan. Hum Ecol Rev. 2009;16(1):27–40. 21. Miyazawa B, Tanaka C. Illustrated handbook of useful wild plants. Tokyo: Yokendo Press; 1948. 22. Sugiura T. Present situation of use of edible wild plants in our country and its possibilities in the future. Tokusan Joho. 2007;28(9):28–31. 23. Copela EB. Edible ferns. Am Fern J. 1942;32(4):121–126. 24. Leach H. Fern consumption in Aotearoa and its oceanic precedents. J Polyn Soc. 2003;112(2):141–156. 25. Lognay G, Haubruge E, Delcarte E, Wathelet B, Mathieu F, Marlier M, et al. Ophioglossum polyphyllum A. Braun in Seub. (Ophioglossaceae, Pteridophyta), a rare potherb in south central Tibet (T. A. R., P. R. China). Geo Eco Trop. 2008;32:9–16. 26. Mannan M, Maridass M, Victor B. A review on the potential uses of ferns. Ethnobotanical Lealets. 2008;12:281–285. 27. Lu SG. Pteridology. Beijing: Higher Education Press; 2007. 28. Tryon RM. Ferns and allied plants, with special reference to tropical America. New York NY: Springer; 1983. 29. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R. Ferns diversified in the shadow of angiosperms. Nature. 2004;428(6982):553–557. http://dx.doi.org/10.1038/nature02361 30. Chang HC, Huang GJ, Agrawal DC, Kuo CL, Wu CR, Tsay HS. Antioxidant activities and polyphenol contents of six folk medicinal ferns used as “Gusuibu”. Botanical Studies. 2007;48:397–406. 31. Xu JX, Wang YL, Wang JJ, Tang W, Chen LJ, Long CL. Chemical constituents of Cibotium barometz and their bioactivities: a review. Natural Product Research and Development. In press; 32. Shi L. Ornamental ferns. Beijing: China Forestry Press; 2002. 33. Zhang YM. A preliminary investigation of the history of pteridophyte eating in China. Journal of Southwest Agricultural University (Social Science Edition). 2007;5(4):103–106. 34. Wu LJ. Notes to plants and animals in the Book of Odes. Shanghai: Shanghai Ancient Bookstore; 1937. 35. Peng DQ, Yang ZN. Collected poems of Tang Dynasty. Beijing: Zhonghua Book Company; 1985. 36. Yun XL, Zhao NW, Pan LT, Zhao JH. Resource distribution and exploitation of edible ferns in Guizhou (II). Journal of Anhui Agricultural Science. 2009;37(33):16317–16319. 37. Yun XL, Zhao NW, Pan LT, Zhao JH. Resource distribution and Published by Polish Botanical Society 270 38. 39. 40. 41. 42. 43. 44. 45. 46. 47. Liu et al. / Food uses of ferns in China exploitation of edible ferns in Guizhou (I). Journal of Anhui Agricultural Science. 2009;37(32):15911–15912. Cui GY. Edible fern resources and development in China. Chinese Cuisine Research. 1998;6(1):21–28. Dai XL, Li XG, Wu SF. List of Chinese edible pteridophytes. Quarterly of Forest By-Product and Speciality in China. 2003;4:5–6. Cao QM, Zhong HY, Li ZH, Sun CB. Exploitation and utilization study of fern starch in China. Food Research and Development. 2007;28(12):168–171. Pteridium fern [Internet]. 2012 [cited 2012 Sep 10]; Available from: http:// www.csh.gov.cn/article_384784.html CITES appendices [Internet]. 2012 [cited 2012 Sep 10]; Available from: http://www.cites.org Li YY, editor. National protected wild plants in Yunnan Province, China. Kunming: Yunnan Science and Technology Press; 2005. Zhang F, Luo SZ, Gao BC, Ding LS. Chemical constituents from the sprout of Pteridium aquilinum var. latiusculum. Natural Product Research and Development. 2004;16(2):121–123. Yang L, Wang MY, Zhao YY, Tu YY. Chemical constituents of the rhizome of Matteuccia struthiopteris. Yao Xue Xue Bao. 2005;40(3):252–254. Zhang D, Yang L, Fu MH, Tu YY. Chemical constituents of the rhizome of Matteuccia struthiopteri III. China Journal of Chinese Materia Medica. 2008;33(14):1703–1705. Ouyang DW, Yang PM, Kong DY. Chemical constituents from Pteris multiida Poir. Chinese Journal of Pharmaceuticals. 2008;39(12):898–900. © The Author(s) 2012 48. Gong XL, Chen ZH, Liang NC. Advances in study on chemical constituents and pharmacological activities of plants of genus Pteris. Zhongguo Zhong Yao Za Zhi. 2007;32(14):1382–1387. 49. Wang ZJ, Zhao QS, Peng LY, Cheng X. Study on the chemical constituents of Callipteris esculenta (Athyriaceae). Natural Product Research and Development. 2009;21:960–962. 50. Wu Q, Yang XW, Yang SH, Zou L, Yan J. Chemical constituents of Cibotium barometz. Natural Product Research and Development. 2007;19:240–243. 51. Liang ZY, Yang XS, Zhu HY, Hao XJ. Chemical constituents of Nephrolepis cordifolia. Guihaia. 2008;28(3):420–421. 52. Rasmussen LH, Lauren DR, Smith BL, Hansen HCB. Variation in ptaquiloside content in bracken [Pteridium esculentum (Forst. f) Cockayne] in New Zealand. N Z Vet J. 2008;56(6):304–309. http://dx.doi. org/10.1080/00480169.2008.36851 53. Alonso-Amelot ME, Castillo U, Smith BL, Lauren DR. Bracken ptaquiloside in milk. Food and Chemical Toxicology. 1996;34(11–12):1187. http:// dx.doi.org/10.1016/S0278-6915(97)89368-4 54. Ojika M, Wakamatsu K, Niwa H, Yamada K. Ptaquiloside, a potent carcinogen isolated from bracken fern var.: structure elucidation based on chemical and spectral evidence, and reactions with amino acids, nucleosides, and nucleotides. Tetrahedron. 1987;43(22):5261–5274. http:// dx.doi.org/10.1016/S0040-4020(01)87702-4 55. Smith BL, Seawright AA. Bracken fern (Pteridium spp.) carcinogenicity and human health – a brief review. Nat Toxins. 1995;3(1):1–5. http:// dx.doi.org/10.1002/nt.2620030102 Published by Polish Botanical Society