Wild Edible Mushrooms Having an Important Potential in East Black Sea Region

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1 ORAL PRESENTATION Wild Edible Mushrooms Having an Important Potential in East Black Sea Region Onur Tolga Okan 1, Sibel Yildiz 2, Ayşenur Yilmaz 3, Jilber Barutçiyan 4, and Ilhan Deniz 2 Abstract: 1 Res. Asst., Karadeniz Technical University, Trabzon, Turkey; 2 Prof., Karadeniz Technical University, Trabzon, Turkey; 3 Mast. Stud., Karadeniz Technical University, Trabzon, Turkey; 4 Expert., Istanbul, Turkey. onurtolgaokan@ktu.edu.tr Wild edible mushrooms have been collected and consumed by people for their nutritional value and they are occasionally consumed for their supposed medicinal value. They have use in the treatment of disease through their immunodulatory, anti-neoplastic and lipid-reducing properties. Edible mushrooms collected from forest in ancient Greek and Roman times. They are known as highly valued non-wood forest products today, thus wild edible mushrooms have played an important role in providing new sources of income in the whole World. Turkey has also very large variety of wild edible mushroom with 21.7million hectare forest area. Especially, East Black Sea region has very rich source of wild edible mushroom. Key Terms: Wilde edible mushroom, non-wood forest, east black sea, ectomycorrhizal Introduction: Fungi are eukaryotic, heterotrophic, and osmotropic. They develop a rather diffuse, branched, tubular body (radiating hyphae making up mycelia or colonies), and reproduce by means of spores. The term mushroom describes the reproductive structure of fruiting body of a fungus (Berch et al., 2007). Mushrooms belong to the kingdom of fungi, a group very distinct from plants, animals and bacteria. Mushrooms often live in symbiosis with other plants, mostly the roots of certain trees, both profiting from this relationship (Olumide, 2007). Commercial mushrooms are either produced in cultivation or harvested from the wild, including forests. The species produced in cultivation are all decomposers (or saprobes) capable of completing their life cycles on dead organic matter. Most of the forest harvested mushrooms are ectomycorrhizal and can therefore form fruiting bodies only when growing with living host trees fungus (Berch et al., 2007). In most countries, there is a well-established consumer acceptance of cultivated mushrooms (Agaricus bisporus, Pleurotus spp., Lentinus edodes, Volveriella volvacea, Auricularia spp., etc). However, wild edible mushrooms have been traditionally eaten only by specific groups of people and seasonally (Diez and Alvez, 2001). The archaeological records reveals edible species associated with people living years ago in Chile, but it is in China where the eating of wild fungi is first reliably noted, several hundred years before the birth of Christ. Edible fungi were collected from forest in ancient Greek and Roman times and highly valued, though more by high-ranking people than by peasants (Boa, 2004). In similar way now, wild growing mushrooms have been a popular delicacy in many countries, due to a good content of proteins as well as a higher content of trace minerals (Kalac and Svoboda, 2000; Murugkar and Subbulakshmi, 2005). Nevertheless, wild mushrooms are becoming more and more important in our diet for their nutritional (Diez and Alvarez, 2001), due to the fact that they are also rich in vitamins B and D (Olumide, 2007). Wild mushrooms are a popular food source in the East Black Sea region in Turkey. The region has a high rainfall area compared to other regions in Turkey. The high humidity level during almost all season provides ideal atmospheric conditions for the mushrooms. There are several wild mushrooms that grow in the forests of Blacksea and the locals relish them. The mushrooms are collected from the forest by settlers and they generally used for the purpose of commercial. Approximately described species of the 1.5 million fungi estimated in the world 673 I n t e r n a t i o n a l C a u c a s i a n F o r e s t r y S y m p o s i u m

2 Wild Edible Mushrooms Having an Important Potential in East Black Sea Region produce fruiting bodies that are large enough to be considered as mushrooms (Chang, 2006). But, At least 1,154 species of wild fungi are collected around the world for culinary or medicinal use (Boa 2004). China, Japan, Mexico, Turkey, several European countries, and major areas of central and southern Africa have long traditions of collecting wild edible fungi and in some of these countries collection for consumption provides significant economic return. Picking edible mushrooms is also an important, if seasonal, recreational activity (Harrington and Cullen, 2008). The world market for the mushrooms industry in 2005 was valued at over $45 billion. The mushroom industry can be divided into three main categories: edible mushrooms, medicinal mushroom products and wild mushrooms (Chang, 2006). According to research, about 40 edible mushrooms species have been collected as food in Turkey and about 25 edible mushrooms species have been commercially evaluated such as selling in markets or export abroad (OGM, 2013). In this study; it was investigated that some wild edible mushrooms having an important trade potential naturally grown in East Black Sea region and emphasized the importance of these mushrooms for the region. Wild Edible Mushroom Having Important Potential Commercial in East Black Sea Region Morel Mushroom (Morchella esculanta var. rotunda): Morel mushroom is edible mushrooms species belong to family of Morchellaceae (Duncan et al., 2002). This mushrooms are commonly known as Kuzu Göbeği Mantarı in Turkey (Fig-1). The edible mushroom Morchella esculanta is among the most highly prized and morphologically recognizable fungi in the world (Goldway et al.,2000). It is collected by the local people and sold in the local market in good price in Turkey, also it is available as fresh or dryed in the market (OGM, 2013). Ascocarps that reach the market are collected from wild, although some success has been reported in cultivating morels. In season, dryed morel mushroom wholesale in Turkey for 130 euro/kg. Figure 1. Morel mushrooms (Morchella esculanta var. rotunda) Morels are widely distributed in the temperate zone of the world. It is appear from late April until the end of May. They sometimes grow at site of a previous year s forest fire (Goldway et al.,2000).occurence of 18 species of Morchella are reported from 28 countries, wherein altogether 14 species are reported to edible or used as food and 5 are used medicinally (Negi, 2006). The most commonly observed species are M. crassipes, M. conica, M. deliciosa, M. esculenta, M. elata, M. distans in Turkey. They main components are (on dry basis): protein 32.7%, fat 2.0%, fibre 17.6%, ash 9.7% and carbohydrates 38.0% (Mulet et al., 2002). In short, they contain 42% protein on a dry weight basis, are low calories and rich in minerals. This apart, its metabolites have varied uses, viz. as adaptogens and immunostimulants and are considered to be one of the most useful antitumour agent for cilinical uses (Negi, 2006). Penny Bun Mushrooms (Boletus edulis): Boletus edulis are a group of allied ectomycorrhizal fungi with edible fruting bodies that are often grouped together as B. edulis sensu lato (Fig. 2) (Hall, 1998). Penny bun mushrooms, also called ayı mantarı or çörek mantarı in Turkey (OGM, 2013), is a popular edible musrooms in Europe, North America and Asia (Tsai et al., 2006;Agueda et 674 I n t e r n a t i o n a l C a u c a s i a n F o r e s t r y S y m p o s i u m

3 Onur Tolga Okan, Sibel Yildiz, Ayşenur Yilmaz, Jilber Barutçiyan, and Ilhan Deniz al., 2008). They are belong to family of Bolataceae (Tsai et al., 2006). The fungus grows in deciduous and coniferous forests and tree plantations, forming symbiotic ectomycorrhizal associations with living trees by enveloping the tree's underground roots with sheaths of fungal tissue. Some hosts for B. edulis sensu lato include Abies, Castanea, Castanopsis, Fagus, Keteleeria, Lithocarpus, Pinus, Picea, Quercus, and Tsuga, but the various component species that make up the taxonomic complex are associated with different hosts in different locations (Hall, 1998). Figure 2. Penny Bun Mushrooms (Boletus edulis) Penny bun mushrooms are found cooltemperate to subtropical zones. Fruting of penny bun mushrooms generally occur in late summer or autumn (Türkoğlu and Gezer, 2006). They main component are (on dry basis): 26.5% crude protein, 2.8% lipids, 5.3% ash and 65.4% carbonhydrates (Ouzouni and Riganakos, 2007). The mushroom is low in fat and digestible carbohydrates, and high in protein, vitamins, minerals and dietary fibre. Penny bun mushrooms have a lot of medicinal effect. In the past they were believed to have a number of medicinal properties, including the removal of freckles and blemishes, and a salve was prepared from boletes to treat dog bites (Ciesla, 2002). But, anticancer effects of penny bun mushrooms are now attested (Bovi et al., 2011). Also, they have several therapeutic effects such as stimulate blood circulation, relax muscles and jonts (Hall., 1998). Although it is sold commercially, it is very difficult to cultivate (Zheng et al., 2007). Thus, penny bun mushrooms sold 15 euro/kg in Turkey. Golden chanterelle mushroom (Cantharellus cibarius): Golden chanterelle is a highly prized edible ectomycorrhizal fungus with a worldwide distribution (Castro et al., 2002a). They are belong to family of Cantharellaceae, and this mushrooms are called yumurta mantarı (egg mushroom) in Turkey( Fig-3). Golden chanterelle always fruit in association with host trees. In forest plantations, golden chanterelle will begin to fruit when the trees are 10 to 40 years of age, depending on the climate and growth rate of the host trees. Chanterelles have a very broad host range. One species alone, the golden chanterelle, has been reported to form mycorrhizal associations with trees in 14 genera: Abies, Betula, Carpinus, Castanea, Corylus, Eucalyptus, Fagus, Picea, Pinus, Populus, Pseudotsuga, Quercus, Shorea, and Tsuga (Pilz et al., 2003). In addition they are usually found in the same places as wild blueberries. Figure 3 Golden chanterelle (Cantharellus cibarius) 675 I n t e r n a t i o n a l C a u c a s i a n F o r e s t r y S y m p o s i u m

4 Wild Edible Mushrooms Having an Important Potential in East Black Sea Region Golden chanterelles are appear from fall to early spring (Valentao et al, 2005), but some researches indicated that golden chantrelles are appear from only june and july (OGM., 2013). They main component are (on dry basis): 53.7% crude protein, 2.9% lipids, 11.5% ash and 31.9 % carbonhydrates (Barros et al.,2008). On the other hand, golden chanterelles have various medicinal effect because of it is characterized by the presence of phenolic compounds. These compounds may have a protective role against various diseases due to antioxidant activity (Valentao et al, 2005). Golden chanterelles are of great economic interest for east black sea due to delicious taste as well as medicinal properties. Although it is commercially important, it cannot be cultivated on compost or wood due to bacterial contamination (Castro and Pfeffer, 2002). In Turkey, Golden chanterelles are sold 4 euro/kg. Cauliflower coral Mushroom (Ramaria botrytis): Cauliflower coral, an ectomycorrhizal fungus grows in coniferous forests throughout the world especially in the mountains of Eastern Asia, Europe and North America (Adhikari et al., 2005). This fungus are belong to commonly known as gelin tırnağı kirmiti (Fig 4). Cauliflower coral is an edible species of coral fungus in the family Gomphaceae (Humpert et al., 2001). it is considered as one of the excellent edible ectomycorrhizal mushroom by some mycophagists (Bhanja et al., 2013). Fruting of cauliflower coral generally occur in Agust and September (Gonzales et al., 2002). Figure 4. Cauliflower coral Mushroom (Ramaria botrytis) Chemical analysis shows cauliflower coral to have a crude protein 39.0%, lipids 1.4%, ash 8.8%, carbohydrates 50.8% (Barros et al.,2008). This fungus also used for medicinal properties. Especially, cauliflower coral extracts have anticancer activity and immunomodulating activity (Lee and Han, 2001). On the other hand, it was found used to get relief from muscles pain (Adhikari et al., 2005). Cauliflower coral contain several bioactive compounds such as p-hidroxybenzoic acid or protocateuic acids, thus this fungus have high antioxidant properties (Barros et al., 2009). Cauliflower coral mushrooms are commercially valuable but it cannot be cultivated. In season it sold 9 euro/kg (Roman et al., 2004). Lactarius species: The species of Lactarius are belong to Russulaceae family. All species of Lactarius, when fresh, are characterized by the unique ability to produce a milky fluid, if cut or broken. The color and taste of the milk varies between the species and are considered of great taxonomical value (Athanasakis et al., 2013). Some of this species are very common edible mushroom. They are wide distribution, from Asia, America and Europe (Flores et al., 2004). Species of Lactarius is represent to East Black Sea Region (Fig 5): L. helvus (locally name Fındık Mantarı), L. volemus (locally name Geyik Mantarı), L. vellereus (locally name Acı Mantar), L. salmanicolor (locally name Kanlıca, Çıntar, Melki), and L. deliciosus (locally name Kanlıca, Çıntar, Melki). L. deliciosus and L. salmanicolor are known to occur under conifer, while L. helvus, L. volemus and L. vellereus are known to occur mixed forest (Barutçiyan, 2012). 676 I n t e r n a t i o n a l C a u c a s i a n F o r e s t r y S y m p o s i u m

5 Onur Tolga Okan, Sibel Yildiz, Ayşenur Yilmaz, Jilber Barutçiyan, and Ilhan Deniz Figure 5. Species of lactarius Fruting of Lactarius generally occur in Summer after rain and September (Gonzales et al., 2002). Local people consume this mushroom and also sell it at the open markets (Doğan and Aydın., 2013). Species of lactarius main component are shows diversty species to species. For example, L. salmanicolor s main component are (on dry basis): 37.28% crude protein, 2.3% lipids, 23.28% ash and % carbonhydrates (Heleno et al.,2009) while, L. deliciosus main component are shows 0.47 g/100 total fat, 1.29 g/100 crude protein, 1.30 g/100 ash and 7.32 g/100 carbohydrates (Barros et al., 2007). Some of lactarius species have medicinal properties. Especially, L. deliciosus and L. vellereus antimicrobial and antioxidant activity was reported and correlated to the phenol and flavanoid contents (Barros et al., 2006;Doğan and Aydın, 2013). Wood Blewit (Lepista nuda): The blewit is a wild edible mushroom and it is belong to Tricholomataceae family (Eyüpoğlu et al., 2011). This mushrooms called mavi cincile or mor mantar in Turkey (Fig 6). It is found throughout mainland Europe and in many other parts of the world including North America. Also, Lepista nuda grows in leaf litter in deciduous and mixed woodland, under hedgerows and gardens during autumn and winter, often fruiting well into December during mild weather (Semreen and Enein,2013). Wood blewit is very important economicly, thus they are recently cultivated by Mushroom Research Center in France (Suberville et al., 1996; Barutçiyan, 2012), but cultivated wood blewit mushrooms are not delicious compared to wild wood blewit mushrooms (Barutçiyan, 2012). Fig 6. Wood Blewit (Lepista nuda) 677 I n t e r n a t i o n a l C a u c a s i a n F o r e s t r y S y m p o s i u m

6 Wild Edible Mushrooms Having an Important Potential in East Black Sea Region Wood blewits are collected around the East Black Sea region for culinary or medicinal use. Because, it is one of the nutritional mushroom. They main component are (on dry basis): 44.2% crude protein, 9.0% lipids, 5.4% ash and 41.4 % carbonhydrates (Colak et al.,2007). Also, the sporophore of Wood blewit contain vit B 1 infusion of macrofungus is used for preventing beriberi. In addition the decoction is used for treatment of abcesses and wounds (Dulger et al., 2002). The methanolic extract revealed antimicrobial and antioxidant properties. Neverthless, chemical or bioactive properties can be affected by mushroom habitat (Pinto et al., 2013). Conclusions: Economy of East Black Sea region depends on the tea and hazelnuts. A small but active market exists for wild edible fungi in East Black Sea region, due to the fact that most of the forested land of East Sea Black Region have commercially important mushroom and these mushroom are collected by amateur local people. The collected wild edible mushrooms are nutritious and therapeutic. Therefore, wild edible mushroom can be a source of nutritional components of food such as protein, carbohydrate, fats, inorganic compounds and essential vitamins. As sources of biologically active agents which contain ingredients that can aid specific body functions, in addition to being nutritious. Hence terms like mushroom neutraceuticals, dietary supplements have emerged. References Adhikari, M.K., Devkota, S., and Tiwari, R.D Ethnomycolgical knowledge on uses of wild mushrooms in western and central Nepal. Our Nature, 3: Agueda, B., Parlade, J., Toiran F.M.L, Cisneros, O., Miguel, A.M., Modrego, M.P., Pena, F.M., and Pera, J Mycorrhizal synthesis between Boletus edulis species complex and rockroses (Cistus sp.). Mycorrhiza, 18: Athanasakis, G., Aligiannis, N., Zagou, G.Z., Skaltsounis, A.L., and Fokialakis, N., Antioxidant properties of the wild edible mushroom Lactarius salmonicolor. Journal of Medicinal Food, 16(8): Barros, L., Baptista, P.,Estevinho, M.L, and Ferriera, I.C.F.R Effect of Fruiting Body Maturity Stage on Chemical Composition and Antimicrobial Activity of Lactarius sp. Mushrooms. J. Agric. Food Chem. 55: Barros, L., Duenas, M., Ferreira I.C.F.R., Baptista P., Buelga, C.S Phenolic acids determination by HPLC DAD ESI/MS in sixteen different Portuguese wild mushrooms species. Food and Chemical Toxicology Barros, L., Venturini, B. A., Baptista, P., Estevinho, L. M., and Ferreira, I. C. F. R Chemical composition and biological properties of Portuguese wild mushrooms: A comprehensive study. Journal of Agricultural and Food Chemistry. 56: Barutçiyan, J.,2012.Türkiye nin Mantarları-1. Oğlak Yayınları.İstanbul Berch, S.M., Ka, K.H., Park, H. and Winder, R Development and potential of the cultivated and wild-harvested mushroom industries in the Republic of Korea and British Columbia. Journal of Ecosystems and Management 8 (3); Bhanja, S.K., Rout, D., Patra, P., Nandan, K.C., Behera, B., Maiti, K.T., Islam, S.S Structural studies of an immunoenhancing glucan of an ectomycorrhizal fungus Ramaria botrytis. Carbohydrate Research 374: Boa, E Wild edible fungi a global overview of their use and importance to people, Non-Wood Forest Products 17, Fao Press, Rome, Italy. Bovi, M., Carrizo, M.E., Capaldi, S., Perduca, M., Chiarelli, L.R., Galliano M., Monaco, H.,L Structure of a lectin with antitumoral properties in king bolete (Boletus edulis) mushrooms. Glycobiology 21 (8): Castro R.I.J, Danell, E., Taylo, A.F.S Use of different nitrogen sources by the edible ectomycorrhizal mushroom Cantharellus cibarius. Mycorrhiza 12: Castro, R.I.J., and Pfeffer, E.P A 13 C-NMR study of exudation and storage of carbohydrates and amino acids in the ectomycorrhizal edible mushroom 678 I n t e r n a t i o n a l C a u c a s i a n F o r e s t r y S y m p o s i u m

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