PIONEERING STUDIES ON HIGH-ALTITUDE OF TRANS-HIMALAYAN (JAMMU & KASHMIR), - DISTRIBUTION, PHENOLOGY AND ETHNOMYCOLOGY

Konchok Dorjey1* and Roshi Sharma2

1Department of Botany, Eliezer Joldan Memorial College, , Ladakh, Jammu & Kashmir, India 2Department of Botany, University of Jammu, Jammu, Jammu & Kashmir, India

*Correspondence: [email protected] ABSTRACT Ladakh in Jammu and Kashmir is positioned at 30˚15΄ to 36˚15΄N latitude and 75˚15΄ to 80˚15΄E longitude in Trans- Himalayan region of Indian subcontinent. The region represents a unique geographical location with wide range of floristic and faunal composition. The present paper provides a review of the distribution of high-altitude mushrooms in Ladakh. The paper, besides providing a preliminary list of 26 macro fungi reported from Ladakh, also gives an overview of the distribution, habitat, phenology and substrate preferences of these macromycetes. A part of this, paper also contributes information on ethnomycology, edibility and molecular characterisation of mushrooms of Ladakh.

Keywords: Ladakh, High-altitude, Mushrooms, Distribution, Phenology, Ethnomycology.

INTRODUCTION 27,046 were considered to be mushrooms (Kirk et al.. Mushrooms, particularly called macrofungi, fleshy fungi 2008). However, Deshmukh (2004) mentioned the existence or macromycetes, are typical heterotrophic organisms that of as many as 41,000 mushrooms worldwide, of which consist of distinct epigeous and hypogeous fructifications approximately 850 species were recorded from India. produced from the underlying mycelial thread under Macrofungi are significant group of organism on earth. optimum climatic conditions. Being saprophytic, parasitic Edible mushrooms, for centuries, have been used for and symbiotic heterotrophs, they constitute a significant human consumption owing to the potential flavour as well component of terrestrial ecosystem in particular and earth’s as medicinal and tonic attributes of mushrooms (Manzi et biodiversity in general. Mushrooms are cosmopolitan, al., 2001). Beside food, macromycetes are known to possess seasonal moisture loving fungi, fruiting predominantly during bioactive compounds of medicinal value or secondary rainy season and sparsely in spring and autumn. Within the metabolites produced by fungi to protect themselves from the ambit of macrofungi, they produce morphologically diverse hordes of attacking microbes. These bioactive compounds fruiting bodies that consequently categorised them into with medicinal attributes of varying degree were known to popular group such as cup fungi, gilled fungi, , possess properties of antioxidant, anti tumouranti bacterial truffles, polypore, bracket fungi, etc. They have diverse and antifungal (Mizuno 1995; Mothana et al., 2000; Kim et texture, varying from fleshy to sub-fleshy or woody and al., 2004; Lindequist et al., 2005; Vishwakarma et al., 2017; sometimes leathery. Ragupathi et al., 2018). Fungi are the third significant functional section after Mushrooms represent one of the major components of fauna and flora as decomposers, symbionts and pathogens forest and grassland communities. In forest ecosystem, they demonstrating global diversity between 1.5 and 3 million represent a significant indicator of the forest life supporting species based on the recent reports in tropics (Teke et al., system (Stamets 2000). Based on their ecological role, they 2018). The estimation of world’s fungi have been the subject may be saprophytes, parasites and mycorrhizal in nature. of vigorous discussion. Tropical and sub-tropical countries While as the saprophytic fungi are the major decomposer are known to harbour more fungi than the reported number of terrestrial ecosystem, the parasitic macromycetesare and thus resulted discrepancy related to the global fungal pathogenic to plants; mycorrhizal symbionts constitute estimate. For the last couple years, numbers of studies significant component of fort ecosystem as they forma havebeen focused on enumerating the global fungal diversity mutual relationship with roots of higher plants. (Crous 2006). Of the 1.5 million world’s fungi estimated Ladakh (30˚15΄ to 36˚ N and 75˚15΄ to 80˚15΄E) in Jammu by Hawksworth (2001), as many as 98,998 species of fungi and Kashmir state is located in Trans-Himalayan region of belonging to 8283 genera have been described, of which, Indian subcontinent. The region is known as cold desert with

ENVIS Bulletin Himalayan Ecology, Vol 26, 2018 59 unique topography, climate and distinct culture and tradition. families of , dominant being (6), Although sub-zero temperature of winter to scorching heat Thelephoraceae (3), Cortinariaceae (2) while as of summer with little precipitation and low relative humidity (1), Fomitopsidaceae (1), (1) and Phallaceae (1) makes the plateau inhospitable terrain, the region constitutes an were least represented. important home for the luxurious growth of diverse group of Distribution of species varies in different fruiting high altitude macrofungi in addition to green plants. seasons as well as collection sites of study area. Mushrooms The macrofungal diversity of Ladakhis poorly explored.For collected in 10 different collection sites of such couple years, researchers (Dorjey et al., 2013a, b, 2015, 2016a, as , Skurbuchan, Tya-Tingmosgang, Phyang, Gangless, b, c; Yangdol et al., 2014, 2015, 2016a, b; Kour et al., 2016; Sumoor, Khardong, , Nimmo, Gonpa were reported to Sharma et al., 2017a, b) at Botany Department, University exhibit variation in species distribution. of Jammu, initiated a pioneering studies on the mushrooms The number of species recorded area wise (Table 3) and of Ladakh to understand distribution, habitat, and (Fig. 1) showed maximum number of seven species in Wanla other aspects of these unique high-altitude organism, and to area which include olla, acetabulum, H. set a database for future study. The present paper, therefore, corium, H. macropus, H. queletii, setosavar. was designed to analyse and discuss the taxonomy, diversity, muscivorum var. nov. and ampliata. Pheyarea was distribution, substrate, phenology and ethnomycology of larger second in species richness with five species (Inocybe curvipes, fungal diversity of this cold arid region. I. sororia, Laetiporus sulphureusvar, Himalayan sisvar. nov., Phallus macrosporus and Thelephora japonica), followed by Species distribution and diversity three macrofungal species reported each from Tya-Tingmosgang From the list of different macrofungal species (Table 1) (Peziza succosa, P. vesiculosa and conjunctipes) and reported from Leh district of Ladakh in Jammu and Kashmir, Gonpa (Scutellinia setosa, Thelephora regularis and Thelephora it is revealed that the region is rich repository of diverse vialis). Likewise two species- Peziza ammophila and Peziza fungal groups. Till date, as many as 26 macrofungal species badia as well as plumbea and Bovista plumbea var. dens- and varieties representing 12 genera and 10 families were caulis var. nov. were recorded from Skurbuchan and Gangless reported from Ladakh (Table 2). Of these, 11 fungal species respectively. However, areas like Phyang, Nimoo, Summor and were represented by three families- Khardong showed least macro fungal richness with one species being dominant (5), followed by (4) and reported from each area including Bovista minor, Psathyrella (2). Likewise, 15 taxa were belonged to seven spadicea, bovista and Bovista pusill are respectively.

Table 1. Members of wild macrofungi recorded from Leh district of Ladakh

S. No Species Date of collection Accession No. Sources 1 Bovista minor Morgan July 2012 HBJU-266 Dorjey et al., 2016c 2 Bovista plumbea Pers. July 2012 HBJU-267 Dorjey et al., 2016c 3 Bovista plumbea Var. dens-caulis var. nov. August 2012 HBJU-268 Dorjey et al., 2016c 4 Bovista pusilla (Batsch) Pers. August 2011 HBJU-269 Dorjey et al., 2016c 5 Calvatia bovista (L.) Pers. August 2011 HBJU-270 Dorjey et al., 2016c 6 Cyathusolla (Batsch) Pers. August 2011 HBJU-201 Dorjey et al., 2013b 8 Helvella corium (O. Weberb.) Massee July 2010 HBJU-185 Dorjey et al., 2013a 7 Helvella acetabulum (L.) Quél. July 2010 HBJU-182 Dorjey et al., 2013a 9 Helvella macropus (Pers.) P. Karst. July 2010 HBJU-186 Dorjey et al., 2013a 10 Helvella queletii Bres. July 2010 HBJU-190 Dorjey et al., 2013a 11 Inocybe curvipes P. Karst. August 2014 HBJU-493 Yangdol et al., 2016a 12 Inocybe sororia Kauffman September 2014 HBJU-494 Yangdol et al., 2016a 13 Laetiporus sulphureus Var. September 2012 HBJU-245 Yangdol et al., 2014a Himalayan sisvar Nov. 14 Peziza ammophila Durieu& Lev. August 2011 HBJU-257 Dorjey et al., 2016b 15 Peziza ampliata Pers. July 2011 HBJU-258 Dorjey et al., 2016b 16 Peziza badia Pers. August 2012 HBJU-259 Dorjey et al., 2016b

60 ENVIS Centre on Himalayan Ecology S. No Species Date of collection Accession No. Sources 17 Peziza succosa Berk. August 2012 HBJU-260 Dorjey et al., 2016b 18 Peziza vesiculosa Pers. August 2012 HBJU-261 Dorjey et al., 2016b 19 Phallus macrosporus B. Liu, Z.Y. Li & Du September 2014 HBJU-402 Kour et al., 2016 20 Psathyrella spadicea P. Kumm. Singer, September 2014 HBJU-498 Yangdol et al., 2016b 21 Ramaria conjunctipes Coker Corner July 2011 HBJU-314 Dorjey et al., 2016a 22 Scutellinia setosa Nees Kuntze August 2011 HBJU-263 Dorjey et al., 2015 23 Scutellinia setosa Var. muscivorum var. nov. June 2011 HBJU-264 Dorjey et al., 2015 24 Thelephora japonica Yasuda August 2012 HBJU-320 Yangdol et al., 2015 25 Thelephora regularis Schwein August 2012 HBJU-321 Yangdol et al., 2015 26 Thelephora vialis Schwein August 2012 HBJU-322 Yangdol et al., 2015

Table 2. Distribution of different species and families among class Agaricomycetes and Pezizomycetes S. No. Family Species Total Class: Pezizomycetes 01 Helvellaceae Hevella acetabulum, H. corium, H. macropus, H. queletii 04 02 Pezizaceae Peziza ammophila, P. ampliata, P. badia, P. vesiculosa, P. succosa 05 03 Pyronemataceae Scutellinia setosa, S. setosa var. muscivorum 02 Class: Agaricomycetes Calvatia bovista, Bovista plumbea, B. plumbea var. dens-caulis var. nov, B. minor, 04 Agaricaceae 06 B. pusilla, Cyathusolla 05 Gomphaceae Ramaria conjunctipes 01 06 Fomitopsidaceae Laetiporus sulphurous var. himalayan sisvar. nov. 01 07 Thelephoraceae Thelephora japonica, T. regularies, T. vialis 03 08 Psathyrellaceae Psathyrella spadicea 01 09 Cortinariaceae Inocybe curvipes, I. sororia 02 10 Phallaceae Phallus macrosporus 01

Table 3. Distribution of wild macrofungi in district Leh S. No Species Collection sites WL SK TT PH GL SU KH PY NM GN 1 Bovista minor Morgan - - - + ------2 Bovista plumbea Pers. - - - - + - - - - - 3 Bovista plumbea Var. dens-caulis var. nov. - - - - + - - - - - 4 Bovista pusilla Batsch Pers. ------+ - - - 5 Calvatia bovista L. Pers. - - - - - + - - - - 6 Cyathus olla Batsch Pers. + ------7 Helvella acetabulum L. Quel. + ------8 Helvella corium O. Weberb. Massee + ------

9 Helvella macropus Pers. P. Karst. + ------

10 Helvella queletii Bres. + ------11 Inocybe curvipes P. Karst. ------+ - - 12 Inocybe sororia Kauffman ------+ - - Laetiporus sulphureus Var. 13 ------+ - - Himalayan sisvar. Nov. 14 Peziza ammophila Durieu & Lev. - + ------

ENVIS Bulletin Himalayan Ecology, Vol 26, 2018 61 15 Peziza ampliata Pers. + ------16 Peziza badia Pers. - + ------17 Peziza succosa Berk. - - + ------18 Peziza vesiculosa Pers. - - + ------19 Phallus macrosporus B. Liu, Z.Y. Li & Du ------+ - - 20 Psathyrellas padicea P. Kumm. Singer, ------+ - 21 Ramaria conjunctipes Coker Corner - - + ------22 Scutellinia setosa Nees Kuntze ------+ Scutellinia setosa Var. muscivorum 23 + ------var. nov. 24 Thelephora japonica Yasuda ------+ - - 25 Thelephora regularis Schwein ------+ 26 Thelephora vialis Schwein ------+

species validates the fact that humic soil serves as a reservoir of minerals and nutrients required for the proliferation of the mycelium and sporophores of fleshy fungi. These results substantiate the findings of other researchers who recognized humus as the most preferred habitat for most of the macrofungi from various regions of India (Natarajan et al., 1982; Saini et al., 1988; Kour 2013). Four fungal species were bryophilous (P. ammophila, P. ampliata, P. badia and Scutellinia setosa var. muscivorum var. nov.), found growing in association with mosses. Possibly, in absence of tree vegetation in Ladakh, the bryophytes particularly mosses might well have provided a unique ecological niche with sufficient soil moisture, temperature and organic nutrients that probably caused Fig. 1. Distribution of macrofungi in different study sites in Leh (Ladakh) emergence of fruiting bodies of these macrofungi. Since tree component of vegetation is sparsely represented in study area, only single fungal species-Laetiporus sulphureus var. Himalayan sisvar nov. was exclusively lignicolous growing on trunk of Salix alba. Three species of Thelephora Habitat and phenology (T. japonica, T. regularis and T. vialis) were recorded as Owing to the extreme climatic conditions, mushrooms in ectomycorrhizal as well as humicolous in nature. Likewise, Ladakh exhibit a wide array of habitat preferences (Table Cyathus olla was lignicolous as well as humicolous and 4). These macromycetes were found in areas with good Ramaria conjunctipes were reported to grow humus soil as water source and high humus rich in organic content, wet well as in association with bryophytes (Fig. 2). grasslands, areas inhabited by bryophytes, cultivated fields of Occurrence of wild macrofungi tends to fluctuate widely and , mixed forest of Salix and Populus species. from one month to another within the seasons of a year due They are preferably, due to different nutritional and ecological to varying seasonal and climatic factors. Some species begin needs, adapted to specific habitats and consequently grouped to form sporophores earlier while others prop up later. Thus, as humicolous, bryophilous, ectomycorrhizal and lignicolous considering fungal phenology is significant to guide the (Fig. 2). Out of 26 reported macrofungi, majority of fungi design of fruiting body studies and to infer their results. The consisting of as many as 16 species were reported to be seasonal period of life-history events of organisms, generally exclusively humicolous, found growing on decomposed moist depends on climatic conditions and has wide implications for soil rich in organic matter and humus. Availability of water species communication, ecosystem processes and ecological resources, humus, cultivated land and sparse vegetation might communal structure. The timing of phenological events can have resulted in fructification of abundant humicolous (16) be quite sensitive to environmental conditions and is thought forms found growing on terrestrial moist and humid sandy- to be determined by substrate moisture and temperature. loam soil. Incidence of high diversity of humicolous fungal Data presented in Table 4 and Fig. 3 revealed that maximum

62 ENVIS Centre on Himalayan Ecology fructification of sporophores observed during the month The sharp variation in phenology of macrofungal of July, August and September. In the month of July, the fructification is principally due to soil temperature,moisture, appearance number of fruiting bodies of macrofungi occur vegetation and water availability. In Ladakh, after the long with record of as many as eight taxa while as the fruiting and freezing winter, moderately warm climate in spring becomes availability of the macrofungi increased remarkably during apparent which, subsequently, resulted in melting of snow and the month of August with record of as many as twelve taxa glaciers. This natural process might have caused the nutrients during this period. However, the emergence of sporophores mobility and moisture availability for these macrofungi in gradually declined in the month of September and, the nutrient and moisture deficient soil which might have consequently, only four macrofungal species were recorded. triggered the emergence of sporophores in temperate and cold arid climate of Ladakh.

Ethnomycology and Edibility Understanding local mycological knowledge is critical for conserving ecological system and promoting sustainable livelihoods. Though, traditional mycological knowledge of Ladakh region of Jammu and Kashmir was not given due attention by the mycologist, Ladakh seemed to be a repository of folk mycological knowledge given the rich traditional cultural heritage, ethnic diversity and geographical isolation of the region. Dorjey et al. (2013) reported an interesting ethnomycological knowledge of a bird’s nest , Cyathus olla from Leh district of Ladakh. The authors have revealed that the local inhabitants compared Cyathus olla, locally termed as Fig. 2. Substrate preferences of mushroom fungi in Leh district ‘Nasi-bangah’, with a traditional granary used for storing

Table 4. Substrate, phenology and Edibility of wild mushrooms of district Leh Species Habit, Habitat and Phenology Vernaculars and Edibility in study area Fruiting Habit Habitat Plant associations Vernacular Edible Non-edible month

Solitary deciduous forests of Populus Bovista minor Morgan Humicolous July Landeh-sButpa - + scattered nigra and Salix alba,

Bovista plumbea Pers. Scattered Humicolous Open grass land July - +

Bovista plumbea Var. Dens Solitary Humicolous Open grass land August - + caulis var. nov. scattered

Bovista pusilla Batsch Pers. Scattered Humicolous Open grass land August - +

temperate forests of Salix Calvatia bovista L. Pers. Scattered Humicolous August Fargolokpa + alba and Populus nigra,

field of Hordeum vulgare Humicolous and mixed forests of Salix Cyathus olla Batsch Pers. Scattered August Nasi-baangah - + Lignicolous excelsa, S. alba, Populus nigra and P. caspica, mixed forests of Salix Helvella corium O. Weberb. excelsa, S. alba, Populus Scattered Humicolous July Koreh - + Massee nigra and P. caspica

ENVIS Bulletin Himalayan Ecology, Vol 26, 2018 63 mixed forest of Salix alba, Helvella acetabulum L. Quél. Scattered Humicolous July Koreh - + S. excelsa. Populus nigra mixed forests of Salix Helvella macropus Pers. P. Scattered Humicolous excelsa, S. alba, Populus July Koreh - + Karst. nigra and Mentha longifolia mixed forests of Populus Helvella queletii Bres. Scattered Humicolous July LandehKoreh - + nigra, Prunus armeniaca

Inocybe curvipes P. Karst Scattered Humicolous on soil under Salix alba tree August - +

Inocybe sororia Kauffman Scattered Humicolous on soil under Salix alba tree September - + Laetiporus sulphureus Var. growing on the trunk of Salix Lignicolous September Chasha + - Himalayan sisvar. nov. alba Peziza ammophila Durieu & Among mosses under Scattered Bryophilous August - + Lev. Populus Among mosses in deciduous Peziza ampliata Pers. Scattered Bryophilous July Balti Koreh - + forest of Salix Peziza badia Pers. Scattered Bryophilous Among mosses August Koreh - + Peziza succosa Berk. Scattered Humicolous Deciduous forest August - + Scattered Peziza vesiculosa Pers. Humicolous Among temperate forest August - + gregarious Phallus macrosporus B. Liu, Solitary Humicolous In cultivated field of barley September - - Z.Y. Li & Du Psathyrella spadicea P. Kumm. Gregarious Humicolous at the base of Populus nigra September + - Singer, caespitose Ramaria conjunctipes Coker humicolou humus soil inhabited by caespitose July - + Corner sbryophilous mosses Gregarious Deciduous forest of Salix Scutellinia setosa Nees Kuntze Humicolous August Koreh - + caespitose alba Scutellinia setosa Var. mus- Scattered Bryophilous Areas dominated by mosses June Koreh - + civorum var. nov. gregarious Ectomycor- mixed forest of Populus Thelephora japonica Yasuda Gregarious rhizal August - + nigra and Salix alba Humicolous Ectomy- mixed forests of Salix ex- Thelephora regularis Schwein Scattered corrhizal August - + celsa, S. alba, Populus nigra Humicolous Ectomy- Mixed forest of Populus Scattered- Thelephora vialis Schwein corrhizal nigra Salix alba Hippophaer- August - + Gregarious Humicolous hamnoides

Fig. 3. Seasonal occurrence of mushroom fungi in Leh district

64 ENVIS Centre on Himalayan Ecology barley grains. They believed that vase-shaped peridium Dorjey K, Kumar S, Sharma, YP (2013b). Cyathus olla from the of fungus was resembles with traditional storage granary cold desert of Ladakh. Mycosphere, 4: 256-259. and the peridioles inside them were considered as grains. In addition, Cyathus is also considered as lucky charm Dorjey K, Kumar S, Sharma YP (2015). New record of two mushroom and its appearance during harvesting season was interesting taxa of Scutellinia from Ladakh (Jammu & believed to be a sacred omen that would bring good fortunes Kashmir), India. Indian Journal of Forestry, 38: 125-128. to the community in the form of bumper grain production. In another attempt at ethnomycological studies in the Dorjey K, Kumar S, Sharma YP (2016a). New record of Ramaria region, Yangdol et al. (2014) reported culinary potential conjunctipes from Ladakh (Jammu and Kashmir) and an of a wood inhabiting fungus, Laetiporus sulphureus var. update list of Indian ramaria. Indian Journal of Forestry, 39: Himalayan sisvar nov., from Phey village of Leh district. The 51-56. fungus was locally termed as ‘Chasha’ meaning ‘Chicken’ due to meat like texture and taste of its fruiting body; Dorjey K, Kumar S, Sharma YP (2016b). Desert puffballs from particularly used in traditional recipes like ‘skyu’, ‘mok- Ladakh trans-Himalaya (J&K), India-the bovistaand mok’ and ‘thukpa’. Besides, two more edible macrofungi calvatia. Indian Phytopathology, 69: 87-92. reported from the region include Calvatia bovista and Psathyrella spadicea (Dorjey et al., 2016; Yangdol et al., Dorjey K, Kumar S, Sharma YP (2016c). Studies on genus 2016) which have been consumed by the local community. peziza from Ladakh (Jammu & Kashmir), India. Kavaka, 46: Ladakh also witnessed a rich folk taxonomy of macrofungi 18-22. that existed and helped local communities to differentiate diverse macofungal groups (Dorjey et al., 2013; Dorjey, Hawksworth DL (2001). The magnitude of fungal diversity: the 2014; Yangdol et al, 2014). 1.5 million species estimate revisited. Mycological Research, 105: 1422-1432. Molecular and biochemical studies Yangdol et al. (2016) made an attempt to understand the Kim SH, Song YS, Kim SK, Kim BC, Lim CJ, Park EH (2004). morphological, anatomical and molecular features along Anti-inflammatory and related pharmacological activities with the biochemical, physical and antioxidative properties of the n-BuOH subfraction of mushroom Phellinus linteus. of edible macrofungal species- Psathyrella spadicea Journal of Ethnopharmacology, 93: 141-146. collected from Phey village of Ladakh region. Various parameters such as molecular characterization, HPLC, Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008). Ainsworth antioxidant activity, fluorescence analysis were studied. and Bisby’s “Dictionary of the Fungi” (10th edition). CAB The result indicated that P. spadicea extract exhibited a International, Wallingford, UK, 771. substantial amount of antioxidant activity with significant amounts of flavonoids, ascorbic acid, β-carotene, total Kour H (2013). Taxonomic studies on some wild fleshy fungi phenolics and high ability to scavenge DPPH radical. of district Poonch (J&K). M. Phil. Dissertation, University of Therefore, the studied wild macrofungus can be used an Jammu. available source of natural antioxidants to treat various oxidative stresses related diseases and constitutes Kour H, Yangdol R, Kumar S, Sharma YP (2016). Three species ansignificant food supplement among the nutrient deficient of Phallus (: Agaricomycetes: Phallaceae populations of Ladakh region of Indian sub-continent. (Jammu & Kashmir), India. Journal of Threatened Taxa, 8: 8403-8409. REFERENCES Crous PW (2006). How many species of fungi are there in tip of Lindequist U, Niedermeyer THJ Julich WD (2005). Africa. Studies in , 55: 13. The pharmacological potential of mushrooms e CAM., 2: 285-299. Deshmukh SK, Mishra JK, Jalpa PT, Papp T (2004). Nutritional profile of wild edible mushrooms of North India. Fungi Manzi P, Aguzzi A, Pizzoferrato L (2001). Nutritional value of Application and Management Strategies, 24. mushrooms widely consumed in Italy. Food Chemistry, 73: 321-325. Dorjey K, Kumar S, Sharma YP (2013a). Four helvella (: : Helvellaceae) species from cold Mizuno T (1995). Bioactive biomolecules of mushrooms: Food desert of Leh, Ladakh, (J&K), India. Journal of Threatened function and medicinal effect of mushroom fungi. Food Taxa, 5: 3981-3984. Reviews International, 11: 7-12.

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