Types of mushrooms for cultivation in Uttarakhand



Although extensive areas of the Uttarakhand state in the northwestern Himalaya of India are covered with forests, there have been relatively few taxonomic reports on the diversity of wild macrofungi (Bhatt et al., 1999, Bhatt et al., 2007a, Bhatt et al., 2007b, Chakraborty et al., 2017, Das and Sharma, 2001a, Das and Sharma, 2001b, Das and Sharma, 2002, Das and Sharma, 2003, Das and Sharma, 2004, Das and Sharma, 2005a, Das and Sharma, 2005b, Das and Sharma, 2001a, Das and Sharma, 2001b, Das et al., 2002, Das et al., 2003, Das et al., 2004a, Das et al., 2004b, Das et al., 2005a, Das et al., 2005b, Das et al., 2005c, Das et al., 2006a, Das et al., 2006b, Das et al., 2016, Semwal et al., 2005, Semwal et al., 2006, Semwal et al., 2007), and many areas remain unexplored for their rich diversity of these organisms. However, most of these published studies have been focused on a few groups, particularly members of the families Amanitaceae and Russulaceae. The primary exception is the article by Prasher and Lalita (2013), which reported 200 species of wood-decomposing nongilled fungi. Approximately 60% of the entire state is covered with forests, with the composition changing with the differences in climate which spans from the plains, to the foothills, and finally to the alpine region of the Himalaya (Chauhan 2010). There is a considerable gap in our knowledge of macrofungi as much of the diversity in this group of organisms is yet to be explored.

Bharsar is located at about 60 km southeast of the district headquarters (Pauri). The area is characterized by a temperate evergreen forest with mild summers, abundant precipitation, and severely cold, prolonged winters. The characteristic temperature, precipitation, and relative humidity, along with the range in elevation and the proximity of the region to the Himalayas, are responsible for a rich diversity of higher plants and an associated high level of diversity of different kinds of macrofungi. Many tree species are present in the general study area, with their distributions determined by the different elevations and different slope patterns of the mountains. Major species include Corylus jacquemontii Decne., Quercus leucotrichophora A. Camus, Q. floribunda Lindl. ex A. Camus, Q. semecarpifolia Smith, Aesculus indica (Wall. ex Camb.) Hook., Rhododendron arboreum Smith, Juglans regia L., Alnus nepalensis D. Don, Cedrus deodara (Robx.) G. Don, Lyonia ovalifolia (Wall.) Drude, Pinus roxburghii Sarg., and Taxus baccata L. subsp. wallichiana (Zucc.) Pilger (Bisht and Sharma 2014). The meaning of the word “Bharsar” in the local dialect is “the region rich in natural wealth” (Bisht and Sharma 2014), and this reflects the availability of different tree and plant species in the general study area. However, owing to the heavy rains that occurred during the survey reported herein, many specimens could not be collected. The primary purpose of this article was to direct some attention to the rural and remote areas of the Bharsar region of the Garhwal Himalaya for their macrofungal wealth. However, reports were available on the plant diversity from this region (Bisht and Sharma, 2014, Chauhan et al., 2014). As such, the procedures we followed to identify the specimens that are subject to further more thorough microscopic study. It should be taken into account that the list provided herein is not to be regarded as an authoritative taxonomic identification, and some names must be considered as sensu lato.

Material and methods
The survey was carried out on August 2, 2015, which is the date for collection of all the specimens listed herein. For the collection and preservation of specimens of macrofungi and for obtaining and recording macroscopic and microscopic details, standard methods were followed (Singer 1986). The color code notations correspond to the standards provided in the Methuen Handbook of Colour (Kornerup and Wanscher 1978). The study area was located between 30°03′24′N and 79° 00′15′ E, with elevations ranging from 1975 to 2290 m a.sl (GPS Mobile app—Geographical Information System). The recording of ecological data within the forest along with the photography of fruiting bodies was carried out in the field with the aid of a Nikon Coolpix P510 camera (Nikon). Species were identified based on morphological features (and spore data for few species) and other information available in the taxonomic literature and field guides (e.g., Binion et al., 2008, Lamaison and Polese, 2005, Phillips, 2010, Singer, 1986). All specimens were air-dried with the use of a commercial dryer (Ezidri, Hydraflow Inds. Ltd, New Zealand). The specimens are presently kept in the personnel herbarium of the first author (K.C.S.) but ultimately will be deposited at the HNB Garhwal University herbarium. Genera are listed in descending order of collection.

Results and discussion
A total of 12 fruiting bodies were collected. These are listed in the following, along with notes on their ecology.
Cortinarius cf. distans Peck.

(Figures 1A and 1D)

Pileus up to 40 mm in diam., convex to flattened but slightly uplifted in the middle, brownish to tawny (6D8); margin tuberculate-sritate. Lamellae broad, distant, purplish (13D5), lamellae of various lengths. Stipe 70 × 8 mm, equal, concolorous with the pileus, lighter above to ring. Ring in the form of a creamish-brown membranous coating on stipe, soon disappearing.

Habitat. Solitary, occurring among leaf litter, under Quercus leucotrichophora (banjh oak) and Corylus jacquemontii (Turkish hazelnut).

Specimen collected. KCS 2428 (elevation 1950 m).

Remarks. This specimen was identified as Cortinarius distans Peck on the basis of the brownish cap that often splits in age, distant gills, stipe initially covered by a creamish-brown cortina, rusty brown spore print, ellipsoid spores (6.9–8.5 × 4.6–5.4 μm; L′ = 7.7 μm, W′ = 5.1 μm; Q′ = 1.53 μm), with a subfusoid end, moderately ornamented, yellowish brown in 3% KOH (Figure 1D). However, the purplish gills of the present specimens suggest that a difference exists with C. distans as depicted on the MushroomExpert.com website (Kuo 2011). However, this species was tentatively identified as Cortinarius distans for the collection number KCS 1076 (year 2007) and KCS 2420 (year 2015) in surveys carried out in Rajgarh in Himachal Pradesh and Lansdown in Uttarakhand, respectively (Semwal, unpub. data).
Gyroporus cf. cyanescens (Bull. ex. Fr.) Quél.

(Figures 2C and 1E)

Figure 2
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Figure 2. A, Blackening Hygrocybe cf. astatogala.; B, caespitose habit of Lyophyllum cf. turcicum.; C, Gyroporus cf. cyanescens with a sticky cap.

Figure 1
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Figure 1. A, Solitary fruiting body of Cortinarius cf. distans.; B, Tricholoma aurantium occurring in a group.; C, solitary fruiting body of Hebeloma mesophaeum cf. var. longipes.; D, moderately ornamented spores of Cortinarius cf. distans.; E, smooth and short-ellipsoid spores of Gyroporus cf. cyanescens; F, roughened spores of Hebeloma mesophaeum var. longipes (red arrow), spores in profile view are nonequilateral (black arrow) ovate with a snout-like apex in face view; G, rusty red cap of Lactarius sp.; H, Amanita manicata with a floccose to felty annulus; I and J, Hygrocybe cf. acutoconica with a slightly depressed (black arrow) viscid cap and a low umbo (red arrow).

Pileus up to 100 mm in diam., applanate with a depression in the middle, grayish orange (6B8) in the middle, dark towards margin as brownish orange (6C8–6C6), with a distinct cinnamon brown (6D6) half circle (but this probably does not represent a specific taxonomic character), margin smooth, uplifted, irregular, undulated-folded. Pores discolored as bluish to greenish black on handling. Stipe 50 × 8 mm, small in comparison to the cap diam., eccentric, possibly due to physiological factors during development of the fruiting body, grayish-red below (11C6), lighter toward the apex, tapering downward, stipe base observed to be linked with rootlets of the associated oak tree, context yellowish.

Habitat. Occurring under Aesculus indica (Himalayan chestnut) and Quercus leucotrichophora (banjh oak) among leaf litter.

Specimen collected. KCS 2429 (elevation 1950 m).

Remarks. This specimen was identified as Gyroporus cf. cyanescens in the family Boletaceae on the basis of the stout, thick fruiting body, the yellowish tubes that exhibit a bluing reaction on being bruised and the characteristically smooth, short-ellipsoid spores. However, the present specimen with very small spores compares rather closely with Gyroporus cyanescens as depicted in Phillips (2010).
Lactarius sp.

(Figure 1G)

Pileus 10–25 mm in diam., plano-convex with a broad-conical nipple in the middle, reddish-brown (8D–C8) to rusty red, margin recurved. Lamellae subdecurrent, close, forked, orangish white lamellulae present, edges entire. Stipe 56–82 × 5–6 mm, central, equal to twisted-compressed toward below, concolorous with the pileus. Latex milky white, unchanging.

Habitat. Occurring under Aesculus indica (Himalayan chestnut), Quercus leucotrichophora (banjh oak), and Corylus jacquemontii (Turkish hazelnut).

Specimen collected. KCS 2430 (elevation 1950 m).

Remarks. This specimen was identified as Lactarius sp. and grouped within the family Russulaceae on the basis of the latex produced when the fruiting body was cut and the brittle texture of the entire fruiting body. This fruiting body is unique and interesting in the genus Lactarius on account of the ratio of cap size and stipe length (i.e., a small cap and a long slender stipe) and twisted-glabrous stipe. Furthermore, on the basis of this distinctive fruiting body ratio among the rusty red cap group of species of Lactarius such as L. rubidus, L. sanjappae, and L. hepaticus, it appears to be morphologically different. It is likely that this specimen represents a species new to science.
Hebeloma mesophaeum cf. var. longipes A.H. Sm., V.S. Evenson & Michel

(Figures 1C and 1F)

Pileus 45–65 mm in diam., broadly convex with flat broad disc in the middle, appearing as campanulate in some specimens, surface viscid; brownish orange (6C8) in the middle, salmon to light orange (6C4) toward the margin, margin regular, faintly striate. Lamellae pinkish grey or reddish grey (7B2), to pinkish white, becoming darker in aged specimens, close to crowded, with various lengths of lamellulae, adnate. Stipe 140–170 × 7–12 mm, terete but becoming slightly expanded toward the base, off white to orange grey (5B2), fibrous stuffed, base with whitish hyphae, possibly ectomycorrhizal with R. arboreum. Ring persistant, thin, adhere to the stipe, brownish orange to reddish orange.

Habitat. Gregarious to solitary, occurring under Rhododendron arboreum and Quercus leucotrichophora (banjh oak).

Specimen collected. KCS 2431 (elevation 1950 m).

Remarks. This specimen was identified as Hebeloma mesophaeum var. longipes A.H. Sm., V.S. Evenson & Michel on account of the tricholomatoid fruiting body, viscid cap, brownish orange to light orange cap color, the presence of a thin cortina and roughened spores that are nonequilateral in profile view and ovate with snout-like apex in face view (Figure 1F). The range in size of basidiospores was 6.84–9.12 × 4–6.9 μm; L′ = 7.98 μm, W′ = 5.5 μm; Q′ = 1.47 μm. However, the present specimen has slightly smaller spores that (8–10 × 5–6 μm) are reported in the original description of the species by Smith et al. (1983).
Cantharellus cibarius Fr.

(Figure 3A)

Figure 3
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Figure 3. A, Edible yellow Cantharellus cibarius; B, wood-inhabiting Cyptotrama asprata; C, edible Amanita hemibapha.

Pileus 40–80 mm in diam., shallowly depressed, lemon yellow to deep yellow (4A8), margin wavy, split, nonstriate. Hymenium with ribs or ridges, these reaching down the stipe, forked, concolorous with the cap. Stipe 40–110 × 8–3 mm, concolorous with the cap, tapering downward, compressed.

Habitat. Occurring under Aesculus indica (Himalayan chestnut) and Quercus leucotrichophora (banjh oak).

Specimen collected. KCS 2432 (elevation 1950 m).

Remarks. This specimen was identified as Cantharellus cibarius Fr. on the basis of the yellow to deep yellow fruiting body, the shallowly depressed cap, a hymenium without true gills, and a very pleasant, apricot smell. This species is a very common edible macrofungus in the Uttarakhand Himalaya.
Hygrocybe cf. acutoconica (Clem.) Singer

(Figures 1I and 1J)

Pileus 35–60 mm in diam., plano-convex to plane, with a rather insignificant umbo in some specimens, and the pileus slightly depressed in few specimens, (Figures 1I and 1J), scarlet red at the middle and orangish red to orange (8A8 to 5A7) toward the margin, surface glabrous, glossy, margin entire, slightly split in older specimens. Lamellae subdistant, orangish white to creamish, adnate to emarginate, lamellulae of various lengths. Stipe 35–60 × 3–5 mm, central, equal or slightly tapering upward, cylindrical or twisted-compressed, dry, glossy bright red in the middle, progressively orangish toward the apex and base. No color change.

Habitat. Occurring among living grasses under Aesculus indica (Himalayan chestnut) and Quercus leucotrichophora (banjh oak).

Specimen collected. KCS 2433 (elevation 1950 m).

Remarks. The specimen was identified as Hygrocybe cf. acutoconica (Clem.) Singer (Figure 1I) on the basis of the fleshy fruiting body, the lack of any color change when handled, the scarlet red to orangish-red viscid cap with low umbo in the middle, and the subdistant orangish white gills with a concolorous stipe. However, the present specimen differs from original description of H. acutoconica as reported from North America (Hesler and Smith 1963) on the basis of having an insignificant low umbo to slightly depressed cap (Figures 1I and 1J). This species has been reported from Kerala, India by Leelavathy et al (2006).
Hygrocybe cf. astatogala (R. Heim) Heinem.

(Figure 2A)

Pileus 25–33 mm in diam., conico-plane with an acute conical umbo in the middle, surface deep orange (6A8) to orangish yellow (4A8), dark blackish at the center, with black, radial, appressed fibrils, viscid, sticky, margin uplifted, split, translucently striate. Lamellae free, creamsih white, blackening when handled, close to subdistant, broad, lamellulae of 1–3 different lengths. Stipe 45–60 × 2–4 mm, terete to slightly tapering toward the apex, striate-twisted, light lemon yellow toward the apex, off white below, surface covered with thin black, appressed fibrils, remarkably blackening when handled.

Habitat. Occurring among green grasses under Aesculus indica (Himalayan chestnut) and Quercus leucotrichophora (banjh oak).

Specimen collected. KCS 2434 (elevation 1950 m).

Remarks. This specimen was identified as Hygrocybe cf. astatogala (R. Heim) Heinem. (Figure 2A) on the basis of the fleshy fruiting body with an acute conical umbo in the middle of the cap coupled with the orangish to orangish yellow, viscid cap, the latter covered with radial blackish fibrils, and the subdistant creamish-white gills. Moreover, the fruiting body blackened when handled or being bruised. However, it is slightly different morphologically from the specimen reported from Kerala, India (Leelavathy et al 2006) because of the different stipe color.
Cyptotrama asprata (Berk.) Redhead & Ginnson

(Figure 3B)

Pileus 40 mm in diam., convex, saffron yellow (4A8) in the middle and lemon yellow (3A8) outward, surface dry, covered with yellowish small, spike-like scaly projection in the middle, hairy to woolly toward the margin. Lamellae adnate, white, distant, broad, lamellulae of various lengths. Stipe 43 × 5 mm, terete, slightly broadened at the base, concoloros with the cap, covered with lemon yellow hairy scales.

Habitat. Occurring on unidentified dead wood in a forest dominated by Quercus leucotrichophora (banjh oak).

Specimen collected. KCS 2435 (elevation 1950 m).

Remarks. This specimen was identified as Cyptotrama asprata (Berk.) Redhead & Ginnson in the family Marasmiaceae on the basis of the saprobic habitat, bright lemon yellow cap, the latter covered with characteristic acute pointed scaly projections, distant whitish gills, a stipe covered with concolorous scaly-wooly elements and a white spore print. Cyptotrama asprata is one of the more widely distributed wild fungi in the world, having been reported from India (Nidhi and Chowdhry 2013), the United States (Redhead and Ginns 1980). This species has been given 28 names and placed in 14 different genera (Redhead and Ginns 1980). This reflects the distribution of this common wild mushroom throughout the world. From the Uttarakhand Himalaya, it was collected earlier in 2009 (KCS1287, Semwal, unpub. data).
Amanita hemibapha (Berk. & Broome) Sacc.

(Figure 3C)

Pileus 75–130 mm in diam., applanate, often slightly umbonate in the middle, orange (5A7) at the center, orange red (8A8) to deep orange (6A8) outward, yellowish orange (4A8-7) to deep yellow at the extreme margin, striations on the margin tuberculate-striate. Lamallae free subdistant, lamellulae truncate, of various lengths. Stipe 80–120 × 15–20 mm, terete, slightly expanded at the apex, yellowish orange to deep yellow downward, covered with appressed yellowish fibrils. Ring superior, membranous, pendant, orangish yellow. Volva white, saccate, membranous, lobed.

Habitat. Occurring under Quercus leucotrichophora (banjh oak) and Rhododendron arboreum.

Specimen collected. KCS 2436 (elevation 1950 m).

Remarks. This specimen was identified as Amanita hemibapha (Berk. & Broome) Sacc. on the basis of gross morphology (i.e., truncate gills, a stipe with an distinct ring, and saccate volva at the base of the stipe). This species has been reported from various parts of the India (e.g., Upadhyay et al., 2008, Vrinda et al., 2005) and is the best edible example among the mostly poisonous members of the family Amanitaceae (Semwal et al 2014). It is very common in the Uttarakhand Himalaya.
Lyophyllum cf. turcicum Sesli, Vizzini & Contu.

(Figure 2B)

Pileus 20–75 mm in diam., broadly convex to applanate, depressed or umbilicate in the middle, grayish yellow (4C4-4B3) to grayish orange (5B4), darker in the middle as beige-brown, smooth, glabrous and shiny, margin regular. Lamellae close, adnate but easily separable from the stipe junction, white, lamelluale of various lengths, edge toothed. Stipe 15–45 × 5–12 mm, equal but increasingly wider near base (25 mm in width) due to the caespitose growth habit, at least three fruiting bodies arise from a single stipe, the latter glabrous, whitish like the lamellae.

Habitat. Occurring in clusters, caespitose, under Quercus leucotrichophora (banjh oak).

Specimen collected. KCS 2437 (elevation 1950 m).

Remarks. The specimen was identified as Lyophyllum cf. turcicum Sesli, Vizzini & Contu. (Figure 2B; Sesli et al 2015) on the basis of the tricholomatoid habit, fragile fruiting body, beige-brown cap, whitish gills that are easily removable from the stipe, whitish stipe, and the caespitose growth habit. However, the present specimens also are morphologically similar to L. fumosum on the basis of cluster growth habit, somewhat similar cap, stipe and lamellae color combination, but can be differentiate on overall small fruitbody.
Tricholoma aurantium (Fr.) (Schaeff.) Ricken

(Figure 1B)

Pileus up to 100–160 mm diam, at first convex and then umblicate, sticky to viscid, smooth to appressed fibrillose-scaly, cinnamon brown (6D6) in the center, brownish orange, reddish golden (6C8) to orange red in the middle, brownish yellow (5C8) to grayish orange (5C5) toward the margin, margin smooth, irregular, undulated-folded. Lamellae adnate to adnexed, crowded to close, off white to orangish grey (5B2) in young specimens, rusty brown in old specimens. Stipe 110–160 × 12–26 mm, terete to tapering toward the base, in some specimens swollen, concolorous with the cap but significantly white at the junction to the stipe, making a clear whitish circular patch, surface covered with orangish scales. Taste slightly acrid and the odor strong soil-like.

Habitat. Gregarious to scattered, occurring under Cedrus deodara, Quercus leucotrichophora (banjh oak), and Rhododendron arboretum.

Specimen collected. KCS 2438 (elevation 1950 m).

Remarks. This specimen was identified as Tricholoma aurantium (Fr.) Ricken (Figure 1B) on account of the stout, dark orangish-red to reddish golden fruiting body with a viscid cap, close gills that are whitish at first but become brownish with age, and a stipe that characteristically has orangish scales that disappear near the apex, leaving a white zone. This species has been reported previously from Kashmir, India (Zahoor and Zafar 2014).
Amanita manicata (Berk. & Broome) Pegler

(Figure 1H)

Pileus 140 mm in diam., convex to applanate, whitish, brownish orange (5C3) in the middle (possibly due to rain or other environmental factors), covered with cottony, small, ash grey to off white floccose-felted universal veil remnants, dense in younger specimens, sparse in aged specimens, universal veil remnants often adhere to the fingers when handled; margin appendiculate, tuberculate-striate. Lamallae free, close, whitish to yellowish grey (4B2), lamellulae of various lengths, edges fringed with floccose universal veil fragments. Stipe 140–220 × 20–25 mm, terete to slightly expanded toward base, surface white, covered with floccose-squamules, concolorous with the universal veil remnants at the cap, dense toward the base. Ring superior, felted, soon disappearing. Volva consisting of floccose-felted patches on a slightly expended stipe base.

Habitat. Solitary to scattered, occurring in a Pinus roxburghii (chir pine) forest, among grasses.

Specimen collected. KCS 2439 (elevation 1950 m).

Remarks. This specimen was identified as Amanita manicata, which has been assigned to the section Lepidella of the genus Amanita on the basis of having amyloid spores, an appendicuate cap margin, and an elongated, broadened stipe base. However, an earlier DNA molecular sequencing study of collection number KCS 1388, collected from the Shiwalik Himalaya indicated 99% similarities with A. manicata and A. nauseosa (Semwal and Stephenson, unpub. data). On the basis of the macromorphological and ecological characteristics, the present specimen was referred to the former species.