Prized Edible Asian Mushrooms: Ecology, Conservation and Sustainability

Fungal Diversity (2012) 56:31–47 DOI 10.1007/s13225-012-0196-3

Prized edible Asian mushrooms: ecology, conservation and sustainability

Peter E. Mortimer & Samantha C. Karunarathna & Qiaohong Li & Heng Gui & Xueqing Yang & Xuefei Yang & Jun He & Lei Ye & Jiayu Guo & Huili Li & Phongeun Sysouphanthong & Dequn Zhou & Jianchu Xu & Kevin D. Hyde

Received: 10 July 2012 /Accepted: 1 August 2012 /Published online: 24 August 2012 # Mushroom Research Foundation 2012

Abstract Mushrooms can be found in forests worldwide and threat to these and many other mushroom species is that of have long been exploited as resources in developed economies habitat loss and over-harvesting of wild stocks, thus, by cre- because of their important agro-industrial, medicinal and com- ating awareness of these issues we wish to enable a more mercial uses. For less developed countries, such as those sustainable use of these natural products. Thus our paper within the Greater Mekong Subregion, wild harvesting and provides baseline data for these fungi so that future monitor- mushroom cultivation provides a much-needed alternative ing can establish the effects of continued harvesting on mush- source of income for rural households. However, this has led room populations and the related host species. to over-harvesting and ultimately environmental degradation in certain areas, thus management guidelines allowing for a Keywords Mushroom species . Greater Mekong Sub-region . more sustained approach to the use of wild mushrooms is Medicinal foods . Non-timber forest products required. This article addresses a selection of the most popular and highly sought after edible mushrooms from Greater Mekong Subregion: Astraeus hygrometricus, Boletus edulis, Introduction Morchella conica, Ophiocordyceps sinensis, Phlebopus portentosus, Pleurotus giganteus, Termitomyces eurhizus, Mushrooms are highly prized for their value as nutritional Thelephora ganbajun, Tricholoma matsuake, and Tuber indi- (Chang and Buswell 1996; Chang and Miles 2004; Carlile cum in terms of value, ecology and conservation. The greatest and Watkinson 1994) and medicinal foods (Chang and

: : P. E. Mortimer : X. Yang : J. Guo S. C. Karunarathna P. Sysouphanthong K. D. Hyde Key Laboratory of Biodiversity and Biogeography, Kunming Mushroom Research Foundation, Institute of Botany, Chinese Academy of Sciences, 128 M.3 Ban Pa Deng T. Pa Pae, Kunming 650201, China A. Mae Taeng, Chiang Mai 50150, Thailand

P. E. Mortimer : Q. Li : H. Gui : X. Yang : J. He : L. Ye : J. Xu (*) World Agroforestry Centre, East Asia, 132 Lanhei Road, Kunming 650201, China Q. Li : X. Yang : J. He e-mail: [email protected] Centre for Mountain Ecosystem Studies, Kunming Institute of Botany, Chinese Academy of Sciences, S. C. Karunarathna : H. Gui : L. Ye : H. Li : P. Sysouphanthong : 650201, Kunming, China K. D. Hyde (*) Institute of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand e-mail: [email protected] D. Zhou S. C. Karunarathna : H. Gui : L. Ye : H. Li : P. Sysouphanthong : Faculty of Environmental Science and Engineering, K. D. Hyde Kunming University of Science and Technology, School of Science, Mae Fah Luang University, 68 Wenchang Road, Yieryi Street( Chiang Rai 57100, Thailand Yunnan Province Kunming 650093, China 32 Fungal Diversity (2012) 56:31–47

Buswell 1996; Kendrick 2000; Moore et al. 2011), for their represents Alpine rangelands; zone 2 depicts grasslands, use in cosmetics (Hyde et al. 2010), as well as their unique initial successional stages (0–5 years); zone 3 represents flavors. Several edible mushrooms are cultivated and are young forest stands, early successional stages (5–10 years); available in local markets and shops all year round e.g. zone 4 shows the immature forest stands, early-mid succes- oyster mushrooms (Pleurotus ostreatus (Jacq.) P. Kumm.), sional (10–20 years); zone 5 is that of older forest stands, ear mushrooms (Auricularia polytricha (Mont.) Sacc.), mid successional (20–30 years) and zone 6 depicts mature straw mushrooms (Volvariella volvacea (Bull.) Singer), forests, in the late successional stages (30 years and older). Lentinula edodes (Berk.) Pegler and Flammulina velutipes (Curt.) Singer, while a large number of edible wild mushrooms are seasonally harvested. Because these wild har- Astraeus hygrometricus (Pers.) Morgan vested mushrooms usually have a short growing season and a high demand, they may suffer from over exploitation Common names: hed torp, hed phor (Thai & Laos) and usually fetch higher prices. As an example of what a resource these mushrooms can be to local communities, in Astraeus hygrometricus is a common gasteromycete original- Yunnan Province, China, up to 700 species of wild mush- ly described from North America by Morgan in 1889.Itgrows rooms are known to be edible and are utilized by local as an ectomycorrhizal species and is associated with certain indigenous people as both a source of food and income. trees species of Dipterocarpaceae (Dell et al. 2005). A. Furthermore,localpeopleconsumeawiderangeof hygrometricus is recognized in the field by its variously mushrooms for their medicinal properties. Many mush- shaped, dark brown, globose to subglobose fruiting bodies, rooms are unique to an area, which would drive up the which can grow up to 3 cm in diameter (Fig. 1). When the market price of these species, and in turn promote over fruiting bodies mature, the outer peridium splits from the top harvesting. For example, in Laos and Thailand, Astraeus to the base, forming star-like segments, which exposes the hygrometricus (Pers.) Morgan (hed torp) and Phlebopus inner peridium or sessile spore sac with an ostiole (Miller and portentosus (Berk. & Broome) Boedijn (hed ha) are unique- Miller 1988;Dring1973). This is a highly sought after wild ly consumed in the region, while another edible species, edible species in northern Thailand and Laos (Butkrachang et Pleurotus giganteus (Berk.) Karunarathna & K.D. Hyde al. 2007; Phosri 2004) and also the most expensive ectomy- occurs abundantly but is not consumed. Thus, education of corrhizal mushroom in northern Thailand (Sanmee et al. local peoples may result in establishing new sources of 2003). It is reported as herbal medicine in China and India foods and income for these people. (Mallick 2010). Astraeus odoratus and A. asiaticus, have been Because of uncontrolled picking and habitat loss, many described from Thailand and are similar to A. hygrometricus species are being overexploited and their populations are in (Phosri et al. 2004, 2007). These Astraeus species are seasonal decline (Koune 2001). Management of wildlife habitats, andcommonlygrowinthewetseasoninThailandfromJune including forests and plantations, is important in order to to September. They are collected when the fruiting bodies are maintain wildlife populations, produce non-timber forest young, and can be sold for the relatively high price of 30–60 products as well as to support the lives of rural settlements. Baht (US$1–2) to the wholesaler in markets and 90–150 Baht The management of habitats for mushroom production is (US$3–5) by market sellers, although the price can be as high one example where more effort is needed in order to con- as 300–400Baht(US$10–13) at the beginning of season, or serve mushrooms and increase their productivity. This paper when the mushrooms are preserved in cans (Dell et al. 2005; therefore reviews the status of ten highly prized edible wild Butkrachang et al. 2007). Since the mushroom is ectomycor- mushrooms in the Greater Mekong Subregion (China, rhizal with Dipterocarp species, there are no methods for Thailand, Laos) and gives a background to their use, value, cultivation. and ecology. The mushrooms are dealt with in alphabetical order and Habitat and distribution no inference should be made to their order of importance. Astraeus species are found in Dipterocarp forests and are Habitat chart associated with Dipterocarpus alatus, D. costatus, D. obtu- sifolius, D. tuberculatus and D. turbinatus, in north east and For the purpose of this paper a descriptive chart has been northern Thailand (Dell et al. 2005; Phosri et al. 2004, 2007) adapted from the work of Cunningham and Yang (2011), (see Fig. 2). Species of Astraeus have been reported to be which depicts the change in mushroom species composition associated with Pseudotsuga, Alnus, Eucalyptus and with vegetative successional changes, see Chart 1. The chart Castanea elsewhere (Phosri et al. 2004). Dry Dipterocarp is separated into ecological zones (1–6), depicting optimal forests or Dipterocarp-oak forests are distributed in South habitats for the respective mushroom species. Zone 1 East Asia, at altitudes of 500–700 m, (Gardner et al. 2000). Fungal Diversity (2012) 56:31–47 33

Chart 1 Habitat zones (1–6) representing the various ecological hab- stages (5–10 years); zone 4 shows the immature forest stands, early- itats for the mushroom species discussed. Zone 1 represents Alpine mid successional (10–20 years); zone 5 is that of older forest stands, rangelands; zone 2 depicts grasslands, initial successional stages (0– mid successional (20–30 years) and zone 6 depicts mature forests, in 5 years); zone 3 represents young forest stands, early successional the late successional stages (30 years and older)

In Asia, Astraeus hygrometricus is distributed in China and knives or metal implements are used to find the mushrooms. India (Mallick 2010) and it is generally found in Laos and This has led to the local belief that burning should be carried Thailand (Butkrachang et al. 2007; Phosri 2004). In north- out during March to April each year before the wet season to ern Thailand, the species is distributed in Dipterocarp forests increase yields (Dell et al. 2000, 2005; Ruksawong et al. of Chiang Mai, Chiang Rai, Mae Hong Son, and Pha Yao 2001). The burning not only affects the ecology of the provinces (Dell et al. 2005). forests and destroys wildlife, but has serious consequences on the health of the human population of northern Thailand, Habitat zone 3–6 as air quality becomes extremely poor during this period. In addition, the number of people living in northern Thailand Improved management has also increased leading to an increased demand for Astraeus, thus putting further strain on the forest ecosystem Astraeus yields depend on the conservation of Dipterocarp (Dell et al. 2005). Yields of saprobic and other ectomycor- forests, and the most sustainable manner for conserving and/ rhizal mushrooms have been shown to decrease following or increasing wild production of Astraeus is to conserve the burning, while sustained or naturally conserved forests pro- Dipterocarp forest systems. Astraeus fruit bodies are half- duce a greater number of mushrooms (Sysouphanthong et hidden in the soil and thus it is difficult to find them on the al. 2010). However there is no specific data available on the ground especially when litter is present, therefore special effects of burning on Astraeus yields.

Fig. 1 Young fruit-bodies of Astraeus growing on the burnt ground of a Dipterocarp forest; Photo credit: Mr. Keegan Kennedy 34 Fungal Diversity (2012) 56:31–47

Fig. 2 Dipterocarp forest habitat where Astraeus grows in northern Thailand; Photo credit: Mr. Keegan Kennedy

Boletus edulis Bull. ex Fr north and Hainan provinces in the south and usually between 300–2000 masl. During the growing season Common names: porcini (Italian), cep and penny bun (June to September), the fruiting bodies can be easily mushroom (English), zhutui mo and dajiao gu (Chinese) found in broad-leaf or mixed forest (Fig. 3). The known host trees of Boletus edulis belong to Pinaceae, Taxodiaceae, Boletus mushrooms are ectomycorrhizal fungi known to Betulaceae, Fagaceae, Fabaceae, Dipterocarpaceae and form relationships with coniferous and deciduous tree Myrtaceae families (Zang 1997). species. Boletus edulis and related species are amongst Boletus edulis is adaptable in its growing conditions, the most highly traded mushroom species worldwide, occurring in both saline and alkaline environments reaching an annual consumption of up to100 000 tonnes/ (Liang et al. 2004). Although fruit bodies may appear year (Hall et al. 1998a, b). Not only sought after for its anytimefromsummertoautumn,theirgrowthisusu- culinary value, B. edulis is also known for its health and ally triggered by rainfall during warm periods of weath- medicinal benefits. Containing a vast array of compounds er followed by frequent autumn rain with a drop in soil used in anti-cancer treatments, as antioxidants, for blood temperature (Hall et al. 1998a, b). Furthermore, a study fat reduction, as a source of ergosterol (a vitamin D conducted by Kasparavicius (2001) concluded that the precursor) and containing anti-viral compounds known to inhibit key enzymes of the HIV virus, B. edulis is well suited for many health related issues (Daba and Ezeronye 2003; Zheng et al. 2007).

Habitat and distribution

This mushroom is widely distributed in tropical and semi-tropical areas of North America and Mexico. In Europe it is found between the Scandinavian countries in the north and Greece and Italy in the south; the range then extends through Afghanistan, India, Nepal, Tibet and into China (Hall et al. 1998a, b). In China, the distribution of B. edulis lies between Jiling in the Fig. 3 A fruiting body of Boletus edulis in the field Fungal Diversity (2012) 56:31–47 35 maximal daily growth rate of the cap (about 21 mm) dynamics, alternating between saprotrophic and symbiotic occurred when the relative air humidity was the great- behaviors (Kanwal et al. 2010). There is some debate on est, and the fruit bodies ceased growing when the air how many Morchella species are there, with some estimates humidity dropped below 40 %. as long as 3–6 species and others as many as 50 different species (Stefani et al. 2010). In China morel mushrooms Habitat zone 5 include M. esculenta, M. crassipes, M. spongiola, M. conica and M. elata (Zhao et al. 2010a). M. conica (Fig. 4) is the Fungi-vegetation succession most marketable and widely distributed across China.

Boletus edulis has the ability to grow under both young and Habitat and distribution mature stands of trees, for example, in Spain it is known to occur in conjunction with the pioneer species Cistus lada- Morels are found in a wide distribution range across the nifer, whereas it is also found in mature forests of Pinus, Northern Hemisphere, from North America, Canada, Betula and Quercus (Hall et al. 1998a, b; Li and Song 2003; through Europe and into Asia. Furthermore, within China Ponce et al. 2011). In China and the surrounding region it is they are widely distributed, ranging from Beijing to Tibet known to occur mainly in older stands and is found in (Mao 2000; Gui et al. 2002; Zhao et al. 2009), they are also association with Pinus massoniana, P. tab ula eformis, P found in Thailand and Laos and other parts of SE Asia. taiwanensis and Quercus mongolica (Li and Song 2003). Morels occur in a variety of habitats, including river- Thus, in the Greater Mekong Subregion, the habitats for this banks, mountain slopes, pastures, and burnt forests. mushroom species are generally older landscapes vegetated Linked with the numerous habitats is the fact that morels by forests in the late successional stages of development. have no special requirement for soil type, occurring in sand, moist soil with abundant organic matter, and in mud Improved management (Goldway et al. 2000; Gui et al. 2002). Two different types of environmental conditions are known In 2010 a total of 10572 tonnes of B. edulis was exported to encourage Morchella ascocarp formation. Morels can first from China worth US $71.83 m, showing a 15 % increase fructify as pioneers on recently disturbed soils. For example, from 2009 (China customs report). This increased demand they become visible in the first spring following mechanical has led to overharvesting of natural stocks, as B. edulis disturbance of the soil, after application of certain herbicides, cannot be artificially cultivated due to its mycorrhizal na- after a deposition of vegetative wastes, and after forest fires ture. The negative impacts of overharvesting, habitat frag- (Goldway et al. 2000;Zhaoetal.2010a). The second case is mentation and human induced disturbances have further the production of ectomycorrhiza with higher plants. Morels resulted in a decline of available stocks (Su et al. 2007; are observed in association with trees in undisturbed habitats, Wang et al. 2011). However, successful management prac- where only a few ascocarps are produced each spring over a tices, such as habitat protection, canopy management, and period of several years (Goldway et al. 2000). insect and disease prevention have led to increased B. edulis In China, M. conica commonly grows at altitudes ranging production in certain areas (Su et al. 2007;Wangetal. from 2900–3100 m above sea level in several types of mixed 2011). Thus, with actively applied management to the ap- forests, such as Picea likiangensis, Abies spp., Betula albo- plicable forest systems, a sustainable approach to harvesting sinensis, Sorbus sp., Salix sp., Acer sp., and Populus bonatii can be achieved.

Morchella conica Dill. ex Pers

Common names: yangdujun (Chinese), morel, sponge mushroom (English)

True morels (Morchella spp.), belonging to ascomycetous fungi, are highly prized for their edibility and appearance. Due to their unique flavor and rich nutritional value they have long being used as a food source. Morchella is also well known for its medicinal value, acting as immunostimu- lants and antitumor agents (Kanwal et al. 2010). Morels Fig. 4 Fruiting bodies of Morchella conica in the field; Photo credit: occur in different types of forests, with different mycelial Mr Qi Zhao 36 Fungal Diversity (2012) 56:31–47

(Gui et al. 2002). Morels have two fruiting periods, from April to May, and from August to September after rain (Gui et al. 2002;Zhaoetal.2010a). Furthermore, morel fruit bodies require scattered light with an optimum temperature ranging between 6 and 11 °C and relative humidity ranging from 50 to 80 % (Gui et al. 2002;Zhaoetal.2010a).

Habitat zone 2

Improved management

Over-harvesting of morels is a common problem across the morel production areas in Yunnan, China due to the fact that wild collection is unrestricted. Often forest fires are deliber- Fig. 5 Tibetan Plateau area where Ophiocordyceps sinensis prefers to ately started in the spring to promote morel production for grow high harvest (Zhao et al. 2010a). The suggested harvesting management practices for morel should be as for that of important cash income source in contemporary rural Tibet, Telephora ganbajun (He et al. 2011). Harvesting techniques making up 50–80 % of total household income in the areas include canopy pruning and removing the mushroom using where O. sinensis occurs (Winkler 2008). While it is possi- a knife followed by watering the area around the mushroom ble to cultivate the mycelium of the fungus on artificial upon harvesting (He et al. 2011). substrate, attempts to cultivate the fungus on infected caterpillars, which are perceived as most valuable and effective, Bionic cultivation have so far proven unsuccessful (Kim and Yun 2005).

After more than 100 years of trials, in 1982 the first indoor Habitat and distribution cultivation of morels was reported, with Morchella esculenta (Masaphy 2010). This was soon followed by other There are about 300–400 species of Cordyceps with a successful cases being published with regards to Morel worldwide distribution (Kobayasi 1982; Sung 1996; Sung bionic cultivation (Masaphy 2010; Cheng et al. 2009). In et al. 2007). About 68 species have been reported from China there was some success in cultivating M. conica on China and 33 species have been recognized in the Tibetan timber from Populus bonatii (Cheng et al. 2009). Plateau and Himalayan region (Zang and Kinjo 1998). The caterpillar fungus is endemic to the Tibetan Plateau including the adjoining high altitude areas of the Central and Ophiocordyceps sinensis (Berk.) G.H. Sung, J.M. Sung, Eastern Himalayas (Devkota 2009). In China, it is also Hywel-Jones & Spatafora (syn. Cordyceps sinensis) known to occur in Sichuan, Yunnan, Qinghai, and Gansu provinces, which account for over 90 % production world- Common names: Dong chong xia cao (Chinese); caterpillar wide. It is usually found in the drier parts of the alpine fungus (English); yartsa gunbu (Tibetan) region, where precipitation is below 300 mm per annum (Winkler 2008). The caterpillar fungus is among the most valuable mush- The fungus parasitizes the underground dwelling larvae room species in the world, and plays a major role for the of the ghost moth or swift moth. Hosts belong to the family local economies on the Tibetan Plateau and adjacent regions Hepialidae (Chu et al. 2004), genus Thitarodes (mostly T. (Fig. 5)(Winkler2008). Indigenous peoples utilize this armoricanus), which live in the soil of grasslands and scrub- fungus for the treatment of different ailments, such as diar- lands from an elevation of 3000 masl up to the snowline, rhea, headache, coughing, rheumatism, liver disease, and it however, the most common occurrence is between 3500 and is also used as an aphrodisiac. Research has shown that 4500 masl. The fungus converts the caterpillar host into a Cordyceps usage increases both the cellular ATP levels sclerotium, from which the fruiting body of the fungus (Namgyel and Tshitila 2003) and oxygen utilization by (Fig. 6) grows (Pegler et al. 1994; Wang 1995;Yao2004). muscles (Zhu 2004) and has anticancer properties Wang and Yao (2011) identified 57 potential host species of (Paterson 2008; Boonyanuphap 2011; De Silva et al. 2012). O. sinensis distributed throughout the Tibetan Plateau. The The collection period starts at the end of April and runs potential habitat for hosts are the high elevation grasslands into July. The tremendous increase in the price for O. and alpine meadows, consisting predominantly of sedges sinensis in recent years turned this fungus into the most (Kobresia spp.), which can cover up to 80–90 % of the Fungal Diversity (2012) 56:31–47 37

is allowed at the campsites and nature reserve staff inform collectors about market prices (Weckerle 2010).. In India and Bhutan harvesting is controlled by local government, which issues letters of permission for local collectors, for a set price. Collectors are required to hand harvested materials to the government authority where they are sold to specific agencies (Singh et al. 2010; Cannon et al. 2009). For Nepal, management issues are related to habitat protection for O. sinensis and its hosts, aiming to protect pastures from over-grazing, and other kinds of hu- Fig. 6 Stroma of Ophiocordyceps sinensis in the field man interference (Devkota 2009). subalpine grasslands (Wu 1997). Thitarodes moths prefer to Phlebopus portentosus (Berk. & Broome) Boedijn feed on young roots of plant species of the families Polygonaceae, Fabaceae, Cyperaceae (including Kobresia), Common names: hed har, hed tub tao dum (Thai); tropical Poaceae, and Liliaceae (Chen et al. 2000). black bolete (English)

Habitat zone 1 Phlebopus belongs to the family Boletinellaceae (suborder Sclerodermatineae of the Boletales) (Binder and Hibbett Improved management 2006) and this genus was originally described as a subgenus of Boletus by Heim (1936), and raised to generic Several human practices are a major threat to the caterpillar status by Singer (1936). In 1944 Singer reclassified it as fungus (Fig. 7). These include excessive livestock grazing; Phaeogyroporus braunii and this name was used until uncontrolled collection and trampling. Intentional burning 1981 (Singer 1944, 1986). The taxon differs from other with the purpose of getting fuel wood, obtaining better boletes as its hyphae produce clamp connections and this regeneration of O. sinensis and securing grass production may be the reason why it can be grown in culture. for grazing in the following season is a major threat Phlebopus portentosus is only eaten in southern China, (Devkota 2006). Laos, northern Thailand and Myanmar, where it is con- With the dramatic increase in value, there has been a sidered a highly prized mushroom in local cuisines sharp rise in demand for the caterpillar fungus, leading (Sanmee et al. 2010; Ji et al. 2011). The fungus is avail- to unsustainable harvesting. Throughout its distribution able from May through to September during the wet range various management measures have been imple- season, although occasional fruit bodies are produced after mented (Weckerle 2010; Singh et al. 2010; Cannon et rains in November through to February. al. 2009;Devkota2009). Examples of management measures implemented in China include the prohibition Habitat and distribution of tree cutting for fuel wood; prohibition of digging out living caterpillars; use of standardized digging tools; Phlebopus portentosus is known from northern Thailand and an obligation to close up the digging holes. In (see Fig. 8), Laos and southern China (Sanmee et al. addition, only trade with locally collected O. sinensis 2010; Ji et al. 2011) as well as Australia, New Zealand, Indonesia, Malaysia, Sri Lanka and Vietnam (Heinemann and Rammeloo 1982;Pegler1986; Segedin 1987; Watling and Gregory 1988; Watling 2001; Bandala et al. 2004; Neves and Capelari 2007; Ji et al. 2009; Lei et al. 2009). In northern Thailand this mushroom grows in association with Artocarpus heterophyllus; Elaeocarpus hygrophilus, Syzygium cumini, Mangifera indica, Mimosa pigra, Salix tetrasperma, Coffea arabica, Citrus grandis and Dimocarpus longan (Bonmark et al. pers. comm.; Sanmee et al. 2010;Jietal.2011). It often grows in association with it hosts in mixed forests and orchards and is thought to be facultative mycorrhizal, although Ji et al. (2011)showedthe Fig. 7 Removed caterpillar fungus with soil fungus to be saprobic. 38 Fungal Diversity (2012) 56:31–47

treated as a special food since ancient times and is men- tioned in Buddhist literature (Udugama and Wickramaratna 1991; Berkeley 1847). When mature, the basidiome is typ- ically infundibuliform measuring up to 35 cm in diameter and 28 cm high (Udugama and Wickramaratna 1991; Berkeley 1847). The mushroom may be solitary but often forms in groups on the ground (Fig. 1). This species has a thick, radicant stipe (Fig. 2) and subdistant broad lamellae which is typical of Lentinus (Pegler 1983). However, Pleurotus giganteus possesses many structures which are not characteristic of the genus Lentinus, and hence its taxo- nomic placement remains uncertain (Pegler 1983).

Habitat and distribution

Pleurotus giganteus is a saprobe, one of the largest edible mushrooms which grows on the ground, is mostly solitary, but can be found in groups, rooting often around stumps, from buried wood, dead roots, in the open and in lowland and Fig. 8 Fruiting body of Phlebopus portentosus grows under Quercus mountain forest up to 3000 masl. It is mostly associated with spp. at the Mushroom Research Centre northern Thailand Artocarpus heterophyllus but it can also be found in mixed vegetation (see Fig. 9)(Pegler1983; Berkeley 1847; Udugama Habitat zone 4–5 and Wickramaratna 1991). This species has been recorded in Australia, the Malay Peninsula, Sabah, Sri Lanka, Vietnam Improved management (Pegler 1983), Oceania (Zhishu et al. 1997), China (Yang and Zang 2003;Zhishuetal.1997), and Thailand (Karunarathna et Since the distribution and occurrence of Phlebopus is not al. 2011a). It is a local delicacy in China, Taiwan, Thailand, Sri well documented it is difficult to suggest ways to improve Lanka and Laos (Peng 2006; Udugama and Wickramaratna collecting management. However, Ji et al. (2011) state that 1991; Karunarathna et al. 2011b; Chandrasrikul 2011; the production of the mushroom has declined in Yunnan in Tapingkae 2005). recent years due to unrestricted commercial harvesting. Thus research is needed to establish the hosts with which Habitat zone 3–4 it is associated, the forest types in which it occurs and the occurrence of fruiting bodies. Improved management Evidence for the cultivation of Phloebopus is mixed, although it is clear that there is potential to produce inoculum for P. giganteus was successfully domesticated in the 1980’s, this fungus and thus inoculate host tree species with it (Sanmee however it has only been cultivated commercially in et al. 2010;Jietal.2011). Sanmee et al. (2010)werealsoto china in recent years (Chen and Hu 2002; Huang 2005; produce low yields of basidiomes in culture and other groups Peng 2006). Despite the popularity of this mushroom in are reportedly experimenting to increase yields (Thongklang et China it is not yet commercially cultivated in Thailand, al. 2010;Jietal.2011). Furthermore, Kumla et al. (2012) have Laos or Sri Lanka (Udugama and Wickramaratna 1991; shown that this putatively ectomycorrhizal fungus has the Karunarathna et al. 2011b). There are no major threats to ability to produce basidiomes without a host plant. P. giganteus as this species is saprobic and can grow in mixed forest habitats (see Fig. 10).

Pleurotus giganteus (Berk.) Karunarathna & K.D. Hyde Termitomyces eurhizus (Berk.) R. Heim Common names: uru paha (Sri Lanka); judarensen, judaxianggu, dabeixianggu, daloudoujun, daloudougu Common names: jizong, zhen gen yichaosan (China), (China); hed thoeng fon (Thai and Laos) Jirousigu (Taiwan), Baijigu (Japan)

Pleurotus giganteus was originally described from Sri Termitomyces eurhizus, also known as T. albuminosus, was Lanka as Lentinus giganteus Berkeley (1847). It has been first recorded in the Compendium of Material Medical (Ben Fungal Diversity (2012) 56:31–47 39

Fig. 9 Mixed forest habitat where P. giganteus grows in northern Thailand

CaoGangMu)400yearsagoinChina(TanandMiao Habitat and distribution 2009). It is a species of basidiomycetes fungi belonging to Tricholomataceae. Termitomyces eurhizus is known to grow in broad-leaved The color of pileus surface is usually grey with a forests of tropical Africa and Asia (Mondal et al. 2004). In diameter ranging from 5 to 20 cm (Fig. 11). There is China, it is located in tropical and subtropical areas of usually no ring around the stipe (Shao-Yu 2006). T. Yunnan and Sichuan provinces (Kone et al. 2011). T. eurhi- eurhizus is renowned for its taste and high nutritional zus is a symbiotic fungus, growing in association with value, with a high protein, polysaccharide, and amino termites of the subfamily Macrotermitinae and their nests. acid content (Chandra and Purkayastha 1977; Mondal et Fruiting bodies of T. eurhizus usually occur after rain or in al. 2004). Past studies have shown that it has anti- high humility areas, and the fruit body matures rapidly oxidant and anti-tumor activities (Lin 2005). Due to its (Shao-Yu 2006). The habitat of T. eurhizus is very diverse, nutritional and medicinal properties T. eurhizus is a ranging from low moisture forests in India to the humid and sought after mushroom species. To date, no cultivation moist subtopic oceanic regions of China. The vegetation and has been possible due to its mycorrhizal nature (Wang et soil type also varies greatly, most likely due to the wide al. 2005; Lu et al. 2007;Sun2006; Wang and Du 2005). range of habitats suitable for the termites (Batra 1979;Wei and Yao 2003).

Fig. 10 Fruiting bodies of P. giganteus growing in mixed vegetation in northern Thailand Fig. 11 A fruiting body of Termitomyces eurhizus in the field 40 Fungal Diversity (2012) 56:31–47

Habitat zone 2–6

Improved management

T. eurhizus has not been domestically cultured, so its management and conservation focuses on the preservation of natural habitats at present. Furthermore, it is difficult to advise on reforestation species as this mushroom is reliant on termite mounds and not just vegetative cover for production. Currently several projects are attempting to cultivate T. eurhizus in China. Firstly via the use of wood decomposi- tion to generate the fungal bodies and secondly by encour- Fig. 13 Fruiting bodies of Thelephora ganbajun in the field aging the production of termite mounds to house the fungal colonies, both approaches have yet to yield commercially viable production values (Chang and Miles 2004; Shao-Yu Habitat and distribution 2006; Yujin et al. 2010). Thelephora ganbajun is endemic to Yunnan Province, China, and grows primarily in association with pine forests, Thelephora ganbajun M. Zang at altitudes between 800 and 2200 masl (Gui et al. 2005;He et al. 2010). Vegetation cover associated with the occurrence Common names: gangbajun, songmajun and xiuqiujun of T. ganbajun include pure stands of Pinus yunannensis (China) and P. kesiya, and to a lesser extent Keteleeria evelyniana and Cunninghamia lanceolata as well as mixed broad leaf/ Thelephora ganbajun isahighlyprizedmushroomdeli- conifer forests (Gui et al. 2005). This species is not com- cacyinYunnanProvincewhereitiseatenforitsgood mercially cultivated and hence only wild harvesting takes taste and medicinal properties such as the high amino- place. Thelephoras grow in Laos and Thailand but no phenol content which is used in the production of para- reports are available regarding T. ganbajun. However cetamol (Zhou 1992). The mushroom grows in whorls Thelephora species are not generally eaten in these in natural vegetation (see Figs. 12 and 13)andis countries, which may indicate an unutilized opportunity collected from the end of June to early September, for local people. when it fetches prices ranging between US$ 120–200 depending on the quality. The demand for T. ganbajun Habitat zone 3–4 is particularly high in Yunnan Province and with the increase in affluence in the Chinese population, demand Improved management is likely to further increase, placing pressure on natural populations (He et al. 2011). The mushroom is ectomy- The landscape of Yunnan Province has to a large extent, corrhizal and there are presently no methods to com- been altered by human influence, primarily due to agricul- mercially farm it. ture, resulting in habitat loss for T. ganbajun. However, with new measures being taken in reforestation, new habitats for T. ganbajun are being created, though this is a lengthy process as T. ganbajun requires forest stands 10 years or older. Furthermore, many of the new trees being planted for reforestation are not species which host T. ganbajun on their roots, but rather trees of economic value. Due to the fact that wild harvesting is the only option, certain management techniques have been suggested to improve production and allow for a more sustainable approach to wild harvesting (He et al. 2011). Harvesting techniques include canopy pruning and removing the mushroom using a knife followed by watering the area around the mushroom upon harvesting (He et al. 2011). In addition to Fig. 12 Pine forest where Thelephora ganbajun grows harvesting techniques, management of the land users Fungal Diversity (2012) 56:31–47 41 themselves was initiated; this included training in the correct harvesting techniques; ownership/harvesting rights being granted to user groups for a given area; and controlling the number and size of harvests per season (He et al. 2011). T. ganbajun is an economically important species for the region, with an annual harvest of 10 000 tonnes for Yunnan province, and can account for up to 37 % of household incomes in areas of high mushroom density (He et al. 2011; Zhao et al. 2009).

Fig. 14 Habitat of Tricholoma matsuake Tricholoma matsuake (S. Ito & S. Imai) Singer

Common names: matsu-take (Japanese), pine mushroom habitat factors (Amaranthus et al. 1998; Hosford et al. (English), songrong (Chinese) 1997; Yang et al. 2006b). In general, middle-aged host trees, slightly opened canopies, sparse understory coverage and Matsu-take literally means “pine mushroom” in Japanese; moderate litter cover are good for fruiting. the equivalent Chinese name is songrong indicating the association of this mushroom with pine trees. It includes a Habitat zone 5–6 group of edible species from the genus Tricholoma. They occur in Asia (with T. matsuake as principal species), North Improved management America (with T. magnivelare as principal species), Europe and North Africa (with T. caligatum as principal species) In Yunnan Province, China, forests producing T. matsutake (Wang et al. 1997). Matsutake mushrooms are soil-borne generally range from 30 to 60 years, thus requiring mature and perennial mycorrhizal fungi. Favored by the Japanese as stands of forest for production (Chen et al. 2011). Japanese a delicacy, matsutake is one of the most expensive mush- researchers have focused on matsutake cultivation for more rooms in the world. Depending upon the quality, the than a century, yet no successful method has been reported. wholesale price in Japan varies from US$ 27–560 per The resource supply depends only on the natural system. A kilogram (Wang et al. 1997). On average, the total con- dramatic productivity decline occurred in Japan since the sumption in Japan is 3000 tonnes per year, of which one mid-twentieth century due to pinewood nematode blight third comes from Yunnan Province, China, and rest from outbreak of pine forests and forest structure and composition other parts of China and America, Europe, Japan and alteration due to shifting of management away from tradi- Korea. Export of matsutake from Yunnan to Japan in- tional practices (Wang et al. 1997; Hosford et al. 1997). In creased from 20 t in 1985 to 1420 tonnes in 2005 Japan, practices to modify the forest canopy structure, forest (Menzies and Li 2010) with annual proximal value of floor and soil drainage condition were used to enhance US$ 44 million (Yang et al. 2008). production. In China, governance policy and regulations were implemented at multiple levels (Menzies and Li Habitat and distribution 2010) and local communities crafted different strategies on managing resource use conflict and balancing equity needs In China, five species (and one variety) of Tricholoma are (Yang et al. 2006a). found in at least eight provinces (Liu et al. 1999), of which T. matsutake is the most valuable and intensively exploited. Tricholoma species are also distributed in China, Japan, Korea, and Russia (Amaranthus et al. 1996). In China, T. matsutake is listed as a protected species (Yang et al. 2006b). As a mycorrhizal fungus, the distribution and habitat of matsutake is highly dependent on host tree species. T. matsutake mainly grow under pine (Pinus)andoak (Quercus) forests, and occasionally under Picea and Castanopsis (Figs. 14 and 15) (Wang et al. 1997). Apart from host trees, forest structure (including canopy cover, stand age and stand vitality), understory coverage, litter cover, soil and topographic characteristics are important Fig. 15 Tricholoma matsuake fruiting body in the field 42 Fungal Diversity (2012) 56:31–47

Tuber indicum Cooke & Massee “burnt area” or brulé around the host species. Recent studies found that the brulé may also effect the dynamics of other Common names: truffle (English), truffe (French), ectomycorrhizal fungal populations (Napoli et al. 2009). yidukuaijun (Chinese) Potential habitat maps were constructed for T. indicum using the weight of evidence method (Yang et al. 2012). Habitat and distribution Cultivation and management There are more than 60 truffle species reported worldwide (Trappe 1979), with most being distributed in Spain, France The first truffle plantations were established in Italy and and Italy (Wang et al. 2005). The natural habitat spans from then in France (Chevalier and Grente 1979), later introduced the Northern to the Southern Hemisphere (Weden et al. to New Zealand, United States and Hungary. In China, it is 2004; Trappe et al. 2009; Bonito et al. 2011). In China, 35 reported that the first plantation was planted in Taiwan in truffle species have been described (Ren et al. 2005), and 1989 (Hu et al. 2005). The main cultivation method still most of them have high economic value. Tuber indicum is depends on inoculating host tree seedlings with truffle one of the renowned commercial truffles in Yunnan spores, and then growing them in their natural environment Province, China and it has been exported to Japan, United (Samils et al. 2008; Bonito et al. 2011). The fruit bodies of States, Europe and Australia since the 1980’s (Tao and Liu truffle can be collected after about 5–8 years. 1990; Hall et al. 1998a, b; Chen et al. 2009). Chinese truffle host trees mainly belong to Betulaceae, Fagaceae, and Pinaceae. These ectomycorrhizal fungi occur in calcareous Discussion to non-calcareous soils at around 1200–3200 masl. Usually, the fruiting season lasts from August to November (García- Wild edible mushrooms are one of the higher valued Montero et al. 2010). non-timber forest products in northern Thailand (Sysouphanthong et al. 2010; Karunarathna et al. 2011a), Habitat zone 3–5 Laos, China, and most Asian countries (Boa 2007). They offer local people a source of seasonal food, medicine, and Fungi-vegetation succession an alternative income, while maintaining forest health (Sysouphanthong et al. 2010). The abundance of wild mush- The Chinese truffle species (see Fig. 16) are always associ- rooms is also a bioindicator of ecosystem health (Dai et al. ated with 10–40 years old secondary-growth coniferous 2009; Du et al. 2011a, b; Sysouphanthong et al. 2010; Egli forests, which develop from evergreen board-leaved forests 2011). In Thailand and Laos, wild mushrooms are taxonom- (García-Montero et al. 2010). The most productive host ically poorly known and recent studies focusing on specific trees are 10–20 years old (Zhang and Wang 1990). An genera have resulted in a large number of new species (Zhao another interesting phenomenon emerges from the allelo- et al. 2008, 2010b, 2011a, b;Leetal.2007a, b; Sanmee et pathic behaviour of truffle species, limiting the growth of al. 2008; Kerekes and Desjardin 2009; Wannathes et al. surrounding vegetation with the aid of volatile organic com- 2009a, b; Van de Putte et al. 2010; Karunarathna et al. pounds produced from truffle fruit bodies, mycelia and 2011a, b), indicating how little we actually know about the ectomycorrhizal roots (Zappa et al. 2004; Tarkka and organisms and the role they play. Even in Yunnan Province Piechulla 2007). This is indicated from the appearance of a of China, relatively little is known, as apparent in recent

Fig. 16 Fruiting bodies of truffles Fig. 17 Bad impacts of improper truffle harvesting Fungal Diversity (2012) 56:31–47 43 publications (Ge et al. 2010; Zhang et al. 2010; Li et al. tempora scales. In: Paper presented at the Forest Soils Biology 2011; Yang 2011). There is a need to preserve these land- and Forest Management Symposia, Sacramento, CA scapes, before as yet unknown mushroom species and their Amaranthus MP, Weigand JF, Abbott R (1998) Managing high- elevation forests to produce American matsutake (Tricholoma related benefits are lost. magnivelare), high-quality timber, and nontimber forest products. There has been a steady decline in mushroom productiv- West J Appl For 13(4):120–128 ity and the disappearance of certain species of mushrooms is Arnolds E (1995) Conservation and management of natural popula- – an ongoing issue for much of the Greater Mekong tions of edible fungi. 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Trans Br Mycol Soc 69(1):63–70 healthy forest is necessary to maintain a high diversity and Chandrasrikul A (2011) Checklist of Mushrooms (Basidiomycetes) in productivity of wild mushrooms (Boa 2007; Moore and Thailand, Open Biodiversity series, Vol. 30 Chang ST, Buswell JA (1996) Mushroom nutriceuticals. World J Chiu 2001; Pilz and Molina 1996). Microbiol Biotechnol 12(5):473–476 Chang S, Miles PG (2004) Mushrooms Cultivation, Nutritional Value, Medicinal Effect, and Environmental Impact. ISBN: 978-0-8493- Acknowledgments We acknowledge and thank CGIAR Research Pro- 1043-0:27–37 doi: 10.1201/9780203492086.ch2 gram 6 on Forests, Trees and Agroforestry-Mekong Sentinel Landscapes Chen CJ, Hu WH (2002) SX330 and culture techniques of Clitocybe for funding this project. Also, value added products from basidiomycetes: maxima. Edible Fungi 24(2):15 Putting Thailand’s biodiversity to use (BRN049/2553), the French-Thai Chen SJ, Yin DH, Li L, Zha X, Shuen JH and Zhama C (2000) cooperation PHC SIAM 2011 (project 25587RA), the National Research Resources and distribution of Cordyceps sinensis in Naqu Council of Thailand (NRCT), the project—Taxonomy, Phylogeny and Tibet. Zhong Yaocai 2311:673–675 (Chinese, English cultivation of Lentinus species in northern Thailand (NRCT/ abstract) 55201020007), Thailand Research Fund (TRF) project number Chen J, Deng X, Liu P (2009) Research status and significant progress BRG5580009 and Mae Fah Luang University, the project—Taxonomy, on the genus Tuber. Microbiol 36:1013–1018 Phylogeny and cultivation of Lentinus species in northern Thailand Chen G, Zhou D, Yang Y, Yang X (2011) Fruiting pattern of Tricho- (MFU/54 1 01 02 00 48) are thanked for providing support to this study. loma matsutake and its relationship with meteorological factors in Yunnan, China. 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