Background

Mushrooms are fruiting bodies with distinctive carpophores of Basidiomycetes and some Ascomycetes [1]. They grow in the wild and are cultivated for food and medicines worldwide [2]. Diversity of ectomycorrhizal fungi studied from Pakistan revealed 23 species from eleven genera. Dominant mushrooms species were recorded from the genus Hymenoscyphus and Inocybe [3]. Fugal species have been identified using morphological and molecular techniques, used for food and culinary purpose [4]. Diversity studies of fungi have been carried out previously by [3,4,5] using standard methods. Targeted surveys for mushrooms species were found more efficient than random surveys [6]. Baseline fungal community data were obtained through plot-based diversity methods [7]. The quadrat method was also used to record fungal diversity and distribution [8]. The line transect method is also helpful to compare different fungal communities with each other and species conservation [9] and to gain prudence about the factors influencing the composition and association of fungal communities [10]. It also gives temporal variation in fungal growth and maturation [11].

Mushrooms have many health-promoting benefits and applications in traditional medicines [12,13,14]. Ethnomycology is a new area of research focused on the interaction of fungi with local communities. It includes cultural, recreational, and traditional uses of mushrooms [15, 16]. It is a naturally renewable and under-exploited resource contributing to improving rural livelihood [17]. Due to diverse ecological, medicinal, nutritional, and health-promoting properties, mushrooms are gaining prime importance among scientific and research communities throughout the world [18]. Wild mushrooms are non-timber forest products (NTFPs) collected as a source of food and income [19,20,21]. Collection and utilization of wild edible mushrooms (WEM) vary among the different communities [22]. These are collected and marketed for food and commercial values [23]. Folk taxonomic-based study of fungi is important because many species of fungi are going to extinct [24]. Traditional mycological knowledge is useful and transferred from one generation to other to safeguard the utilization and applications of edible mushrooms [25].

Morels are also a valuable source of food and income among the rural people of Pakistan [26]. These are used in traditional medicines against common ailments [27]. It is essential to transfer the folk knowledge of mushrooms among ethnic mountain communities to enhance the collection, utilization, and conservation of mushrooms [28].

The whole region of Azad Jammu and Kashmir (AJK) is blessed with diverse geographic and climatic conditions with a diversity of mushrooms. Despite a large number of ethnic groups in the state of Jammu and Kashmir, the ethnomycological data are poorly documented from the area and no comprehensive studies have been taken previously to explore such resources for human welfare. There is a lack of proper documentation on the diversity, specific habitat, ethnomycological uses, production, harvesting, and export of mushrooms. Present research work is designed to record species diversity of mushrooms in AJK, ethnomycological uses, and their commercial and economic importance.

Methods

Study area

The study area lies in the Western Himalayan regions of Azad Jammu and Kashmir between 32°-17′ and 36°-58′ North latitude and 73°-6′ and 80°-30′ longitude in the western part of the Indian subcontinent with an area of 13,297 square kilometres. The elevation from sea level ranges from three hundred and sixty meters in the south to 6325 m in the north. Average annual rainfall 1300 mm. The population is 4 million and the ratio between rural to urban populations is 88:12. Forestry, livestock, and agriculture are major economic activities for rural income. The climate of the study area is subtropical monsoon type in the lower range to moist temperate in the middle and subalpine to alpine in upper regions. The summer is hot at lower altitudinal zones and pleasant in upper zones with very cold winters. The area above 1200 m altitude receives heavy snowfall from November to April. The average temperature recorded in summer remains 34 to 25 °C and in winters, 10 to 4 °C. Annual rainfall (average) in the monsoon region is 900–1300 mm and in monsoon-free region it remains 35–140 mm [29].

Data collection

Consecutive field visits were carried out to selected villages, local markets, shops of the study area for gathering information about mushroom collection, and selling. A semi-structured questionnaire (Appendix 1) was used to collect the information on the wild edible mushrooms value chain, hunting, collection, preservation, and retailing [30]. Primary and secondary information was collected from all the available resources. Primary information was gathered by structured and semi-structured interviews with collectors, consumers, and sellers. Secondary information was collected from different literature, thesis, maps, and websites. Both formal and informal discussions with forestry professionals, key informants, village elders, farmers, women, schoolteachers, social workers, and shopkeepers were carried out to identify and verify the facts. Information on edibility, medicinal uses, preservation methods, and any other uses was also recorded.

All the major terrestrial ecological sites and hotspots for mushroom species from the state of Azad Jammu and Kashmir were selected for this study. Sampling sites were finalized through consecutive field visits based on specific geographic and ecological significance from representative vegetation zones of Azad Jammu and Kashmir. A total of 22 sites were selected from Neelum, Muzaffarabad, Hattian, Bagh, Heveli, Poonch, and Kotli districts of Azad Jammu and Kashmir during 2015–2019 to study mushroom diversity (Fig. 1 & Table 1).

Fig. 1
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Map of the study area (right) and sampling sites (left)

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Table 1 Different study sites and coordinates
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Diversity of wild mushrooms

Sporophores of fungi were collected from forest communities of Cedrus deodara and Pinus wallichiana. For the documentation of fungal diversity quadrate and transect methods were used following standard protocols [7, 31,32,33]. The collection of samples was mostly carried out by targeted surveys to record a maximum number of mushroom species as described by [34]. Density, frequency, and relative values were calculated for the application of diversity indices [35]. Shannon diversity index was also calculated [36].

Identification and preservation of Sporophores

A specific collection number was assigned to each sample in triplicate. Specific characters of habitat and associated plant species were also recorded. Sporophores were cleaned gently, soil particles were removed, and photographs were taken with a digital camera Nikon D5600. Fruiting bodies were left into the air for drying before packing for preservation. For easy drying, the larger Sporophores were cut down into many smaller pieces. Dried samples were packed and labelled with separate tag numbers for further analysis and future references. Specimens were finally cross-checked with the published material. The appropriate taxonomic literature was used for the proper identification of mushrooms [37,38,39,40,41]. Further citations were checked on MycoBank http://www.mycobank.org [42] and the index Fungorum database (http://www.indexfungorum.org/names/names.asp [43]. Final identification was made from fungal biology and systematic research laboratory Department of the Botany University of the Punjab Lahore. Specimen’s number were assigned to each sample and freeze at a temperature of − 80° for further future analysis.

Results and discussion

Diversity of mushrooms

A total of 131 mushroom species were collected and identified up to species level during the study (Table 3) using standard methods [3,4,5]. Out of 131 mushroom species, 97 species of mushrooms were recorded new to the state of Azad Jammu and Kashmir (Fig. 2); however, few of these species have been identified from different parts of Pakistan at the molecular level previously [44]. Already identified mushroom species were morphologically cross-checked with published material. The dominant mushroom family was Russulaceae with 23 species followed by Agaricaceae, 16 species, Boletaceae, 10 species, Helvellaceae, 7 species, Tricholomataceae, and Physalaeriaceae 6 species were recorded in present investigations. Amanitaceae, Hymenochaetaceae, and Pleurotaceae were identified with five species each. Russula and Lactarius were the dominant genera. Only a few species of these genera were edible, and the maximum number of sporocarps decays on substratum after maturity. Inedible species were often collected for wound healing and other medicinal purposes. Most of the mushroom species growing naturally were collected by the rural for food and medicinal purposes. The maximum diversity of fungi was calculated in the Neelum Valley followed by Las Dana, Chakar, Noon Bangla, and Leepa in Jhelum Valley. These sites have maximum forest cover and diverse ecological conditions. The Basidiomycetes constituted the major proportion, i.e. 115 species, while Ascomycetes constituted 16 species. The majority of mushrooms collected belong to gilled fungi. Species of Coprinus, Flammulina, Peziza, Armillaria, and Morchella were found in clusters while other species occur in scattered patches. In Previous studies, six species of Agaricus were reported from Rawalakot, Azad Kashmir by [45]. Similarly [45] collected and described edible mushrooms, viz. Armillaria mellea, Cantharellus cibarius, Craterellus cornucopioides, Flammulina velutipes, and Macrolepiota procera from the area. Furthermore, more they added, Amanita elliptica, A. muscaria var. alba, Ramaria aurea R. botrytis, Phallus impudicus, Morchella elata, and M. semilibera, Amanita ceciliae, A. subglobosa, A. pantherina, A. pachycolea, A. virosa, Volvariella bombycina, and V. speciosa to Kashmir [46, 47] also contributed to the mushroom flora of AJK. They reported 25 edible mushrooms from different sites of the Azad Jammu and Kashmir. Dominant species of fungi collected during this study were also common with the previous studies [48,49,50]. These mushroom species grow during early spring in April to July in most of the studied areas. This pattern of diversity and distribution of fungal species associated with coniferous forest type was studied [51]. They reported Russula and Lactarius as a dominant genus associated with Himalayan cedar. Other studies on diversity of mushrooms in the literature revealed that most of the fungal communities were composed of Basidiomycetes [52]. Diversity and community stabilization of mushrooms depends upon different ecological factors including precipitation, soil organic matter and type of specific plant community. The sites which have some common geographic features also have similar species composition. This might be due to maximum annual rainfall and enough soil organic matter that promote the diversity of mushrooms because mushrooms grow maximum during the wet and rainy season in most parts of the world on different substrates [53]. Recently, fungal biology and systematics Laboratory University of Punjab is working on establishing Mycoflora data base and added many species to Mycota of Pakistan [54, 55].

Fig. 2
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Mushrooms reported new to study area AJK

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Table 2 Demographic characteristics of Mushroom collectors in 6 districts of AJK (N = 923)
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Principal component analysis

PCA is used to determine and analyse the relationship between species distribution and the underlying environmental factors and habitat types. It is an advanced technique that maximizes the species scores concerning sampling sites having linear and appropriate weights. PCA identified the major species-specific to the sites and put them close to the sites of distribution. The sites grouped by the PCA based upon their species interrelationship are Peer Chinasi, Haji Peer and Peer Hasimar, Toolipeer, and Leepa. All these sites have little variations in the biotic factors including species composition and topography. These sites have some common geographic features which are responsible for similar species composition. Major mushroom species collected from these sites and grouped by the PCA are Coprinus comatus, Lactarius sanguifluus, Amanita fulva, Armillaria gallica, Lycoperdon perlatum, Lycoperdon pyriforme, and Russula creminicolor, these sites have shown a little correlation with a village Khawaja bandi kahuta Havali. The mushroom species grouped by the PCA are the common fungi that are present in these sites. On the other hand, Nagdar (Upper Neelum), Dawarian, Sharda, Taobut, Chakar (Noonbangla), Sudhan Gali, and Banjosa are grouped near to each other. These sites are almost lying in the temperate forest of AJK and have same topography, Forest cover, and precipitation pattern so their mushroom composition is nearly like each other. Major fungal species of these sites were Amanita muscaria, Lactarius deliciosus, Gyromitra esculenta, Armillaria sp, Agaricus campestris, Russula brevipes, Polyporus squamosus, Trametes versicolor, and Laccaria sp. Other mushroom species grouped at the centre of the PCA axis showed equal distribution and association with all the sites of the study area. These species have no specific distribution pattern. PCA identified five major keystone species from the data matrix and separated them along X-axis. Lactarius piperatus, L. deliciosus, L. torminosus, Hygrocybe flavescens, and Russula delica were extracted as most significant vectors having maximum Eigenvalue scores represented by their distinct placement on PCA biplot. These five species were characterized by the higher IVI values in the species dataset and enjoyed abundance and broad distribution across the study area. The major bulk of the fungal elements were clustered in the centre of the PCA biplot showing their random distribution without specific site or habitat preference. These species are most common and grow almost equally in different geographic conditions with slight changes in their growth period and maturation (Fig. 3).

Fig. 3 
figure 3

Expression of principal component analysis

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Detrended correspondence analysis

We subjected our species dataset to the DCA to extract the trends in species distribution and identify the specific habitat preference of the species represented by the sites. Our analysis results revealed uniform and continued species distribution patterns along specific environmental gradients with interpretable species-site assemblages. DCA separated the dataset into diffused but identifiable clusters. The Kotli site was separated at the top of X-axis with the characteristic species Coprinellus micaceus. This site lies in the subtropical zone with limited mushroom species growing during the monsoon. This specific microhabitat reflects the dominance of Pinus roxburghii and different grasses. Along the X-axis at the right side of the plot, different sites with similar species of mushrooms are grouped. These sites are Shaheed gali, Peer Chinasi, Sharda, Arangkeil, Noonbangla, Leepa Valley, Haji Peer, Dawarian, and Peer Hasimar. The Khurshidabad site in Havali was separated at the base of biplot and placed near to the Forward Kahuta with the characteristic mushroom species Ganoderma lucidum and Hygrocybe flavescens. Another identifiable cluster appeared at the left most of the biplot in the X-axis consisting of Chakar, Nagdar, and Upper Neelum placed with the Sharda site. While the left lowest groups are placed on the plot are the sites sharing the similar species composition these are Sudhan Gali, Banjosa, and Plandri (Figs. 4 and 5).

Fig. 4
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Expression of detrended correspondence analysis

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Fig. 5
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Expression of correspondence analysis among the different site

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Demographic characteristics and community involvement

Wild mushroom value chain is seen to be gender oriented dominated by women in collection (61.1%, n = 564) while men occupy only 38%, n = 359 out of the 923 respondents (Table 2). Women were found to participate in every mushroom activity such as collection to preservation while men contributed only to collection and selling. Similar findings were reported by [57] where female was found dominant in WEM collection. However, it was found that men dominated in selling of mushrooms (70%) to local shops, restaurant, markets, and local mushrooms entrepreneurs. The preponderance of female collectors in present study is supported by another research [58,59,60]. Every stage of mushroom activities from collection to processing and even marketing was led by women in this study. Poor involvement of men in mushroom activities might be due to the belief that mushroom collection is only art for remote areas of women. In remote areas of studied districts of AJK, women are mostly unemployed, dedicating themselves to household and subsistence activities. Mushroom collection and selling are one of their sources of food and income. The study revealed that collection activities are dominated by people of middle age (53.9%) especially those of 31–50 years old between the ages ranged 14–85, followed by 19–30 (25.8%), by 14 and over (17.6%), and by 50 and above (13.3%) (Table 2). Similar findings were also reported from the Finland [61] where it was shown that middle aged people by 30 (96.6%) or above involved in mushrooms collection activity. It revealed the participation of older, more experienced people in mushroom collection. Similar results on age distribution were also reported by [22]. Among 923 respondents, 25.8% had an education level of primary school, 22.8% middle school, 20.9% % secondary or high school, 17% illiterate, and 13.5% higher secondary, university, or colleges (Table 2). There were 41% housewives 39.7% farmers and entrepreneur, 12.6% employed, 6.7% retired from 923 respondents (Table 2). Data on education in the present study revealed that almost 83% of informants had a middle school education per the findings of [15] who indicated that mushroom collection or cultivation was mostly managed by less educated people in the rural areas.

Socio-economic and ethnomycological importance of wild mushrooms

A total of 923 informants from 22 sites of selected districts were interviewed based on the harvesting, selling, and consumption of wild edible mushrooms. Mushrooms play a significant role in rural development. Many species of edible mushrooms and morels have been collected by the poor rural for a socio-economic purpose and rural livelihood in terms of economic development. Morels are collected by the people of rural areas of AJK for medicinal and commercial purposes. Morchella conica, M. costata, M. esculanta, M. elata, and M. tridentina were considered highly prized morel species. These morel species widely grow under the dense forest cover of Pinus wallichiana and Cedrus deodara in association with Viburnum grandiflorum. Among morels, Morchella esculanta and M. tridentina were valuable morels and considered good for export due to compact fruiting bodies, less moisture, and higher nutritional contents. M. conica has more water contents than the M. esculanta and turns dark black, which affects the preservation as well as its marketing. One kilogram of dried morel is solid in the market up to 32 thousand (Pakistani rupees) PKR. One kilogram of dry morels can fulfil the basic needs of a family of an average size. Prices of dried morels vary from market to market. In a village (Neelum) average price of 1 kg of dried morel is between 30,000 and 32,000 PKR. Other edible mushroom species Pleurotus ostreatus and Agaricus campestris were supplied to the famous hotels of the city. One Kg of dried mushroom is sold in 1500-2000PKR. These mushrooms are mostly used in dishes for foreign visitors. Mushrooms are collected worldwide as a source of food and income. Edible fungi, i.e. Cantharellus cibarius, Lactarius deliciosus, and Russula sp., were collected and sold in the market for food purposes [62]. More than 300 species of mushrooms were collected by different ethnic groups in Mexico for nutritional and medicinal purposes [63]. In China, local farmers earn up to 62% of their cash income through mushroom export [30]. Mushrooms play a significant role in rural development. Many species of edible mushrooms and morels have been collected by the rural for a socio-economic purpose [56, 64] and rural livelihood in terms of economic development [63]. Prices of dry mushrooms are higher than fresh mushrooms. Similarly, those mushrooms which are exported showed higher prices. The most common species collected and used for trade-in neighbouring countries of Pakistan are, for example, Boletus spp. Lactarius sp., Suillus bovinus, Russula sp., and Termitomyces sp. [46, 65]. In the present investigation, the socio-economic data showed that a family collects an average of 3–4 kg morels with an average income of about PKR 0.1-0.120 million in a season. Fifty-six species of mushrooms were reported as edible previously from Pakistan and unfortunately because of over-collection, urbanization, and deforestation some species are threatened [66].

Mushrooms are natural sources of bioactive compounds used in alternative traditional medicines. Today, in parallel with the increase in the number of diseases, alternative medicine, and their usage is also increasing. It might be due to the disadvantages or side effects of drugs. Mushrooms have compounds that decrease oxidative stress and improve health [67, 68]. Many unexplored species of medicinally and commercially important mushrooms were widely distributed in the forests of Azad Jammu and Kashmir. Mushroom species growing naturally were collected by the rural people for food and medicines. In previous studies, medicinally significant mushrooms from the Neelum Valley have been reported [27, 77]. They are also collected in different countries of the world like the UK, Sweden, France, and Mexico [62, 74]. In the present study, twenty-six species of mushrooms were recorded as medicinally important which are used for the treatment of some common ailments. Among these mushrooms Fistulina sp., Hericium erinaceus, Laetiporus sulphureus, Polyporus squamosus, Ramaria fennica, Sparassis crispa, Morchella elata, M. conica, M. tridentina, and M. deliciosa were the most delicious and widely used species as a nutritive food by the rural people of Neelum Valley and Jhelum Valley. Morchella esculanta is reported to contain antioxidant, anticancer, and anti-inflammatory properties and is used as delicious food [68]. Soup of dried fruiting bodies of Ramaria fennica is used by women during breastfeeding to improve lactation. Ramaria fennica and morel species were considered effective against common cough and cold. Many mushroom species are considered medicinally important and used against stomach problems, heart burning, and wound healing without considering any side effects or toxicity. Previously, it is reported that extract and powder of mushrooms are used in traditional medicines and have reported uses as a liver tonic, blood purifiers, fertility issue, and diabetes [69]. Fruiting bodies of Laetiporus sulphureus are dried into a fine powder and used with milk as a portion of healthy food and anti-seminal weakness. Previously, it is reported that Laetiporus sulphureus is used against speedy recovery of wounds and common cold [6]. In another study, it is found that dry powder of this mushroom is helpful to expel a retained placenta in women and against stomach pain [30]. Use values of mushrooms species recorded during the study are given in (Table 3). In the present study, we have found the use of morels in different traditional home remedies against common ailments, fever, cough, and cold. Soup of Morchella is considered nutritious and used to treat the common cold. Extract of many edible species of mushrooms is effective against different human diseases like coronary disorders, oxidative stress, and cancer and provides different physiological benefits to consumers [64]. Sparassis crispa and Polyporus squamosus were used to treat stomach issues and considered healthy food. Old villagers prefer to use these mushrooms as a source of food. People use Morchella species, Hydnum repandum, Sparassis crispa, and Polyporus squamosus against stomach problems, Lycoperdon perlatum, and Auricularia auricula in wound healing and as anti-hypertension agents. Armillaria mellea, Boletus badius, Cantharellus cibarius, Pleurotus ostreatus, and Lactarius deliciosus contain bioactive organic contents with reported uses in traditional medicines [70]. Sher and Shah [26] reported that morels were utilized both for food as well as medicines to cure different diseases.

Table 3 List of Mushrooms species with their Ethno-mycological uses
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Ethno-mycological uses of mushrooms vary from region to region and even among the communities of the same area [71]. In Poland, edible mushroom species are used as food and medicines. Folk taxonomy is very important to share the knowledge and use of these mushroom species. Extract of mushrooms can be used due to cosmeceutical and nutricosmetic ingredients to treat inflammatory skin disease and hyperpigmentation [72]. Aqueous Extracts of Polyporus squamosus, Morchella spp., and Sparassis crispa are considered more effective against common diseases of the stomach by the rural informants of Kashmir. As it is reported that mushrooms are effective against different diseases, but the chemical evaluation is very important before using an extract of mushroom species [73]. Mushrooms are used in culinary traditional medicines and sometimes cooked in oil [74]. It is concluded that mushrooms potentially can provide opportunities to rural communities to generate income for household development in rural areas of Azad Jammu and Kashmir. Mushroom collection can provide opportunities to the low-income areas to improve their living standards in terms of income generation and socio-economic development. It is very important to raise awareness among the local communities/mushroom collectors, about the importance of mushrooms as food and medicines. Mushrooms, if well addressed in society, are a potential source of traditional medicines, anti-cancer compounds, food, and nutrition security specifically in developing countries.

Mushrooms edibility in the study area

The state of Azad Jammu and Kashmir (AJK) is blessed with a fertile land, rich with diversity of mushrooms. Among the identified wild mushrooms, 54 (48%) were identified as edible, 24 (21%) inedible, 14 (12%) edible and medicinal (Fig. 6). Lactarius deliciosus, Morchella sp., Pleurotus ostreatus, Polyporus squamosus Sparassis crispa,, and Laetiporus sulphureus were collected by the rural people of the area as a source of food.  Edible mushrooms have been collected and consumed as food worldwide [4, 14, 27, 74]. Edible mushrooms like Lactarius deliciosus and Ramaria sp. have been collected and consumed in the neighbouring countries of Pakistan [78].

Fig. 6
figure 6

Category, number, and percentage use value of edible mushrooms of the study area

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