Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 8 Number 02 (2019) Journal homepage: http://www.ijcmas.com

Original Research Article https://doi.org/10.20546/ijcmas.2019.802.050

Three Records of from Sal Forest of Central India

R.K. Verma*, V. Pandro and G.R. Rao

Tropical Forest Research Institute, Jabalpur - 482 021, Madhya Pradesh, India

*Corresponding author

ABSTRACT

K e yw or ds

Agaricomycetes, Distribution , Ecto- Three records of genus Russula namely: Russula brevipes, Russula , luteotacta and Russula silvicola were reported for the first time from Russula, Sal forest central India. These were collected from sal forest of Dindori, Article Info Madhya Pradesh. Earlier these fungi are reported from Kerala and Uttarakhand. Accepted: 07 January 2019 Available Online: 10 February 2019

Introduction edible, for example, R. crustosa, R. lutea, R. olivacea, R. parvovirescens, R. senecis, R. Family was established by Roze virescens (Atri et al., 2010; Das et al., 2002; in 1876 and it is one of the largest Bhatt and Lakhanpal, 1988a, b; Kalita et al., ectomycorrhizal families. The members of 2016; Khatua et al., 2015; Semwal et al., this family generally form ectomycorrhizal 2014). The present paper reports 3 species of association in different angiosperm and Russula, namely Russula brevipes, Russula gymnosperm trees like Abies, Acer, Betula, luteotacta and Russula silvicola as new Diospyros, Hopea, Larix, Myristica, records from sal forest of central India. Rhododendron, Shorea, , Vateria, etc. The genus is represented by about 130 taxa Materials and Methods from India (Das et al., 2014). Recently 124 species of the genus were listed from India Specimens of mushrooms were collected from and most of them including north-western sal forests of Dindori district, Madhya subtropical and temperate forests of Pradesh during rainy seasons. A part of Himalayan region of Uttarakhand (Verma et collected sample was preserved in 70% al., 2018). Many species of Russula are alcohol just after collection for microscopic

445

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455 study. The fruit bodies of fungi were dried =Russula brevipes Peck var. brevipes under the sun or in the wooden box lighted =Russula brevipes var. acrior Shaffer with 100W electric bulb. Microscopic slides =Russula brevipes var. megaspora Shaffer were prepared by using stain, mountant, =Agaricus chloroides Krombh. =Russula clearing and softening chemicals. Slides were delica var. glaucophylla Quél. observed under advanced research =Russula delicula Romagn. microscope (Leica, Germany) using 5x, 10x, 20x, 40x objectives and 10x and 15x Basidiome small sized, 4.5-6 cm diam, eyepieces. Observations under phase contrast convex to applanate often slightly depressed; and dark field were also made whenever surface grayish orange, to pinkish white, required. Photomicrography was done with hygrophanous, drying pale ochraceous, the help of a digital camera (make, Leica) weakly straite, glabrous to occasionally attached to the advanced microscope. becoming fibrillose scaly. Lamellae sub- Identification of fungi has been done with the decurrent to decurrent, pale pinkish brown to help of published literature, monographs, pale pinkish, sub-distant. 3.5- 5 cm books, keys, etc. (Abraham et al., 1980; Atri long, with 2-8 µm wide hyphae. Basidia 20- and Kour, 2003; Atri and Saini, 1986, 1990a; 32.5 ×6-7.5µm, clavate, 4-spored. 1990b; 1990c; Atri et al., 1992, 1997, 2016; Basidiopores 6-8.7×5-7.5µm, sub-globose to Bhatt et al., 1995, 2007; Buyck and Atri, globose or ellipsoid, echinulate. 2011; Chaudhary and Tripathy, 2016; Crous Macrocystidia, 38.5-45 × 5-6.5µm, et al., 2016; Das and Sharma, 2001, 2003, filamentous, hyaline, hyphae hyaline, 2.5- 2005a,b; Das et al., 2002c; 2005, 2006, 2008; 7µm wide. (uppermost layer of 2010; 2013a,b; 2014; 2017; Dhancholia, hyphae in the pileus, it covers the , 2011; Dutta et al., 2015; Farook et al., 2013; fleshy tissue of the fruit body) of interwoven Ghosh and Das, 2017; Hedawoo, 2010; Joshi with scattered fascicles of erect to sub-erect et al., 2012; Kaur et al., 2011; Kumar et al., hyphae, terminal cells slightly swollen, sub- 2014; Manimohan and Deepna, 2011; clavate or capitates, pale yellowish brown in Mohanan, 2011, 2014; Natarajan and Raman, mass. 1983; Pavithra et al., 2017; Pradeep and Vrinda, 2007, 2010; Rawla, 2001; Rawla and Collection examined Sarwal,1983; Saini et al., 2010; Saini and Atri, 1981, 1984, 1989a, b; Saini et al., 1988, On base of Shorea rubusta tree in sal forest of 1989; Sarwal, 1984; Sathe et al., 1980; Karanjiya, Dindori, Madhya Pradesh, Shaffer, 1962; Shajahan and Samajpati, 1995; 20/07/2018, specimen deposited at Mycology Sharma and Das, 2002; Varghese et al., Herbarium, Tropical Forest Research 2010; Verma et al., 2018; Vishwakarma et al., Institute, Jabalpur, TF 4047 2012; Vrinda et al., Vrinda et al., 1997a, b; Watling and Gregory, 1980). Russula luteotacta Rea (Figures 7-12)

Results and Discussion =Russula sardonia sensu Bresadola =Russula luteotacta Rea var. luteotacta Taxonomic description =Russula luteotacta var. intactior Jul. Schäff. =Russula luteotacta var. semitalis J. Blum Russula brevipes Peck (Figures 1-6) =Russula luteotacta var. serrulata J. Blum =Russula luteotacta f. alba Fillion & Frund (Russulaceae, , Incertae sedis, =Russula luteotacta f. griseoalba Bidaud & , , Fungi) Frund 446

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

=Russula luteotacta var. cyathiformis Tropical Forest Research Institute, Jabalpur, Reumaux & Frund TF 4048. =Russula luteotacta var. duriuscula Reumaux & Frund Russula silvicola Shaffer (Figures 13-22) =Russula luteotacta var. terrifera Reumaux & Frund Basidiome small sized, cap 3-5cm diam., convex at first but becoming flattened in age, Taxonomic description sometime developing a sunken center, bright red to pinkish red, surface of cap smooth; gills Basidiome small to medium sized, pileus 5- attached to the stem; close to moderately well 7cm, fleshy, convex with a broad depression spaced; stipe 5-7cm long, 1-1.5cm thick, dry at the centre; surface grayish – pink, fairly smooth. Hyphae 5-7.5µm wide. sometimes with white tints at the place, sticky 7.5-11.2 × 7-9µm, mostly with when wet, translucent straight at the margin, isolated extending warts. Basidia 25-45 × 8.7- pellicle peels off easily up to mid radius, faint 12.5µm, clavate, 4-spored. edge smell; Margin crenate, incised, lamellae sterile; macrocystidia, 87.5-107.5 × 10- adnexed, appearing free when mature, pale 12.5µm. Sterigmata 5-7.5 µm long. pink, crowded without lamellulae, rarely bifurcated, context white, unchanging brittle, Collection examined: On soil surface under gills pale-cream, free of the stem, crowded, Shorea rubusta, in sal forest of Karanjiya, brittle to touch. Cap convex becoming Dindori, Madhya Pradesh, 20/07/2018, flattened with slight depression in the middle, specimen deposited at Mycology Herbarium, pink or pale red with white underneath, flesh Tropical Forest Research Institute, Jabalpur, white. Stipe 4-8 x 1-1.5cm, central slightly TF 4049. broader at base, stuffed; surface white, smooth with a faint red colour at the apex and Recently 124 species of Russula reported middle, stem white with pale pink, sometimes from different parts of India were listed red marks, annulus absent. Basidia, clavate, (Verma et al., 2018). Russula brevipes was 25-37.5 x 7.5-12.5 μm 4-spored. Lamellaedge reported on Monotropa uniflora, a heteromorphous, cheilocystidia and mycoheterotrophic plant found in eastern and pleurocytidia macrocystidioid, rare, 75-100 x western North America (Bidartondo and 7.5-12.5μm, broadly clavate with an apical Bruns 2001). It is a common ectomycorrhizal projection which is filled with referactive associated with several hosts (conifers contents. Basidiospores 6.2-10 x 5-7.5μm, to hardwoods) across temperate forest subglobose, ornamentation moderately thick, ecosystems. Typical hosts including trees forming a more or less complete reticulum, belonging to genera like, Abies, Picea, superhilar area in myloid, print, off- , Shorea and Tsuga. It was white. Subhymenium pseudoparanchymatous, recorded associated with , trama heteromorphous with abundant producing fruit bodies singly or in groups and sphaerocytes. Pleipellis a gelatinized fruiting season occurs from summer to trichodermium. It is a poisonous and rare autumn. This mushroom is quite commonly species. encountered in late autumn. The species has been reported from western North America Collection examined: On base of Shorea (Illinois, Québec, Pennsylvania, Michigan, rubusta tree in sal forest of Karanjiya, California, and Colorado) and Himalayan Dindori (Madhya Pradesh), 2007/2018, moist temperate forests of Pakistan (Shaffer, specimen deposited at Mycology Herbarium, 1975). 447

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

Fig.1-2 Russula brevipes: 1 fruit bodies growing in sal forest around coppiced stump, 2 broken fruit body showing gills and fleshy stem

1 2

Fig. 3-6 Russula brevipes: 3 epithelial element, 4 macrocystidia and basidia, 5-6 basidiospores

3 4

5 6

448

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

Fig.7-8 Russula luteotacta 7 fruit bodies in habit, 8 showing gills and stipe

7 8

Fig.9-12 Russula luteotacta 9 epithelial element, 10-11 basidia and macrocystidia, 12 basidiospores

ss 9 10

11 12 449

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

Fig.13-16 Russula silvicola, 13 emerging fruit body in habit, 14 young fruit body, 14 pileus upper surface and 16 arrangement of gills

13 14

15 16

450

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

Fig.17- 22 Russula silvicola, 17 epithelial element, 18 macrocystidia 19 macrocystidia and basidia, 21 macrocystidia, 22

17 18

19 20

21 22

From India it was reported from Jageshwar, Uttarakhand (Das and Sharma, 2005b), from Almora, Mayawati and Champawat, Nagaland (Kumar et al., 2014) and from

451

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

Jammu and Kashmir (Watling and Gregory, 1(22) funded by Indian Council of Forestry 1980). In the present article it is being Research & Education (ICFRE), Dehradun. reported from sal forest of Dindori, Madhya Pradesh. References

Russula luteotacta is distributed in moist- Abraham SP, Kachroo JL, Kaul TN (1980). deciduous to evergreen forest. The species is Fleshy fungi of Gulmarg forest -I. a poisonous mushroom and occurs solitary or Kavaka 8(1): 29-39. scattered in small-groups on soil under Hoea Atri NS, Kour H (2003). Some unrecorded ponga, H. parviflora, Vetaria indica, light spored mushrooms from Punjab. Diospyros malabarica and Shorea robusta Indian Journal of Mushrooms 21:1-4. forming ecto-mycorrhizal association. It also Atri NS, Saini SS (1990a) Studies on Russula grew in broad leaved woodland or under Pers. Section Decolorantes (Maire) individual broad leaved trees. The species is Sing. Geobios New Reports 9: 10–13. distributed in Denmark and in India. The Atri NS, Saini SS (1990b). North Indian species was reported from Kerala (Pradeep Agaricales–VIII. The section compactae and Vrinda, 2010; Mohanan, 2011, 2014). In Fr. of Russula Pers. in India. Journal of the present article it is being reported for the the Indian Botanical Society 69, 343– first time from sal forest of central India. 346. Atri NS, Saini SS (1990c). North Indian Russula silvicola was reported from Pauri Agaricales-VIII. The Section Grahwal, Uttarakhand (Bhatt et al., 2007). Compactae Fr. of Russula Pers. Journal The species was earlier recorded from oak of Indian botanical Society 69: 343-346. and beech rotten woods. It was found Atri NS, Saini SS, Saini MK (1997). Studies throughout eastern Durham, New Hampshire on genus Russula Pers. from North and North America (Michigan). The species Western Himalayas. Mushroom Res. 6: was reported to form ectomycorrhizal (1) 1-6. association with these forest trees like oak and Atri NS, Saini SS, Saini MK, Gupta AK beech (Shaffer, 1975). R. silvicola is the only (1992). Two new records of the genus species of Russula in which the cap is some Russula from India. Geobios new shade of red or pink, it is often difficult to Reports 11: 101-103. distinguish one species from another on the Atri NS, Saini, SS (1986). Further basis of features that can be observed in the contributions on the studies of field. This species is often confused with the northwest Himalayan Russulaceae. very similar species like, R. emetica, R. Geobios New Reports 5: 100–105. congoana and R. cremicolor. Atri NS, Sharma Samidha, Kaur M, Das K (2016). Researches on Russulaceous In conclusion, three new records of macro- Mushrooms - An Appraisal. Kavaka 47: fungi, namely Russula brevipes, R. luteotacta 63-82. and R. silvicola were reported from sal forest Bhatt RP, Bhatt VK, Gaur RD (1995). Fleshy of central India. fungi of Gahwal Himalaya: The genus Russula. Indian Phytopathology 48: Acknowledgements 402–411. Bhatt RP, Purnima S, Semwal KC (2007). The work presented here was conducted New records of Russula from Garhwal under project ID No. 224/TFRI/2016/Patho- Himalaya. Mushroom Research 16(2):

452

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

55– 60. Indian Journal of Forestry 26: 320–326. Bidartondo MI, Bruns TD (2001). Extreme Das K, Sharma JR (2005a). Russulaceae of specificity in epiparasitic Kumaon Himalaya. Botanical Survey of Monotropoideae: wide spread India, Ministry of Environment and phylogenetic and geographic structure. Forests, Govt. of India, Kolkata, pp 255. Molecular Ecology 10: 2285-2295. Das K, Sharma JR (2005b). Russulaceae of Buyck Bart, Atri NS (2011). A Russula Kumaon Himalaya. Botanical Survey of (Basidiomycota, Russulales) with an India, Ministry of Environment and unprecedented hymenophore Forests, Govt. of India, Kolkata, pp. configuration from northwest Himalaya 255. (India). Cryptogamie Mycologie. 32(2): Das K, Sharma JR, Atri NS (2006). Russula 185-190. in Himalaya 3: A new species of Chaudhary Rohina, Tripathy Astha (2016). subgenus Ingratula. Mycotaxon 95, Diversity of wild mushroom in 271–275. Himachal Pradesh (India). International Das K, Sharma JR, Bhatt RP (2002). Russula Journal of Innovative Research in flavida Frost – an addition to the Indian Science, Engineering and Technology ectomycorrhizic fungi. Mushroom 5(6): 10859-10886. Research 11: 9–10. Crous PW, Wingfield MJ, Richardson DM et Das K, Van de Putte K, Buyck B (2010). New al., (2016). Fungal Planet description or interesting Russula from Sikkim sheets: 400-468. Persoonia 36: 316-458 Himalaya (India). Cryptogamie Das K, Atri NS, Buyck B (2013a). Three new Mycologie 31(4): 373–387. species of Russula (Russulales) from Dhancholia S (2011). New records of genus India. Mycosphere 4(4): 707–717. Russula from dry temperate zone of Das K, Atri NS, Buyck B (2013b). Three new Lahul Valley of Himachal Pradesh. species of Russula (Russulales) from Plant Disease Research 26: 203. Sikkim (India). Mycosphere 4(4): 722– Dutta AK, Paloi S, Pradhan P, Acharya K 732. (2015). A new species of Russula Das K, Dowie NJ, Li GJ, Miller SL (2014). (Russulaceae) from India based on Two new species of Russula morphological and molecular (ITS (Russulales) from India. Mycosphere sequence) data. Turkish Journal of 5(5): 612–622. Botany 39: 850-856. Das K, Ghosh A, Chakraborty D et al., Dutta AK, Paloi S, Pradhan P, Acharya K (2017). Fungal Biodiversity Profiles 31- (2015). A new species of Russula 40. Cryptogamie Mycologie 38(3): 353- (Russulaceae) from India based on 406. morphological and molecular (ITS Das K, Miller SL, Sharma JR, Hemenway J sequence) data. Turkish Journal of (2008). Two new species of Russula Botany 39: 850-856. from Western Ghats in India. Indian Farook VA, Khan SS, Manimohan P (2013). Journal of Forestry 31(3), 473– 478. A checklist of agarics (gilled Das K, Sharma JR (2001). Russula mushrooms) of Kerala State, India. rhodomelanea Sarnari - a new record Mycosphere 4(1): 97–131. for India. Mushroom Research 10: 109– Ghosh A, Das K (2017). 111. Russula (Russulaceae) in western Das K, Sharma JR (2003). New records of Himalaya 1: Two new species from Russula from Kumaon Himalaya. subg. Russula. Phytotaxa 323(3): 337-

453

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

252. Peck CH (1890). Report of the Botanist Hedawoo GB (2010). Wild mushroom flora (1889). Annual Report on the New from Amravati Region, Maharashtra, York State Museum of Natural History. India. Journal of Mycology and Plant 43:51-97 Pathology 40(3): 441–444. Pradeep CK, Vrinda KB (2007). Some Joshi S, Bhatt RP, Stephenson SL (2012). The noteworthy agarics from Western Ghats current status of the family Russulaceae of Kerala. Journal of Mycopathological in the Uttarakhand Himalaya, India. Research 45(1): 1-14. Mycosphere 3(4): 486–501. Pradeep CK, Vrinda KB (2010). Kaur M, Atri NS, Sharma S, Singh Y (2011). Ectomyrrhizal fungal diversity in three Three taxa of genus Russula Pers types and their association with section Tenellae from India. Journal of endemic, indigenous and exotic species Mycology and Plant Pathology 41(4): in the Western Ghar forests of 524-527. Thiruvanthapuram district Kerala. Kumar R, Tapwal A, Pandey S, Raja-Rishi R, Journal of Mycopathological Research Mishra G, Giri K. (2014). Six 48(2): 279-289. unrecorded species of Russula Pradeep CK, Vrinda KB (2010). (Russulales) from Nagaland, India and Ectomyrrhizal fungal diversity in three their nutrient composition. Nusantara types and their association with Bioscience 6(1): 33-38 endemic, indigenous and exotic species Manimohan P, Deepna Latha KP (2011). in the Western Ghar forests of Observations on two rarely collected Thiruvanthapuram district, Kerala. species of Russula. Mycotaxon 116: Journal of Mycopathological Research 125-131. 48(2): 279-289. Mohanan C (2011). Macrofungi of Kerala. Rawla GS (2001). Himalayan Species of Kerala Forest Research Institute, Hand Russula Pers. Ex S.F. Gray, 1-48. In: Book # 27, Kerala, India, 597pp. Plant Diversity of the Himalaya (eds. Mohanan C (2011). Macrofungi of Kerala. PC Pande, SS Samant). Gyanodaya Kerala Forest Research Institute, Hand Prakashan, Nainital, India, pp 1– 48. Book # 27, Kerala, India, 597pp. Rawla GS, Sarwal BM (1983). Taxonomic Mohanan C (2014). Macrofungal diversity in studies on Indian Agarics 1. the Western Ghats, Kerala, India: Russulaceae. Bibliotheca Mycologica members of Russulaceae. Journal of 91: 23–46. Threatened Taxa 6(4): 5636–5648. Rea C (1922). British Basidiomycetae: A Mohanan C (2014). Macrofungal diversity in handbook to the larger British fungi. Pp the Western Ghats, Kerala, India: 1-799 members of Russulaceae. Journal of Saini MK, Atri NS, Sharma Samidha, Priya Threatened Taxa 6(4): 5636–5648. Janki (2010). Taxonomic Studies on the Natarajan K, Raman N (1983). South Indian Genus Russula Pers. from Himachal Agaricales. J. Cramer, Vaduz, Pradesh, India. Journal of Mycology Germany. and Plant Pathology 40 (1): 52-54. Pavithra M, Sridhar KR, Greeshma Saini SS, Atri NS (1981). Russula foetens AA (2017). Macrofungi in two (Pers.) Fr. – A new record for India. botanical gardens in southwestern India. Current Science 10: 460-461. Journal of Threatened Taxa 9(3): 9962– Saini SS, Atri NS (1984). Studies on the 9970. North-West Himalayan Russulaceae.

454

Int.J.Curr.Microbiol.App.Sci (2019) 8(2): 445-455

Geobios New Reports 3: 4-6. robusta G.G. from West Bengal. Indian Saini SS, Atri NS (1989a). North Indian Journal of Mycological Research 33: Agaricales–IX section Ingratae Quel. of 105-117. Russula Pers. Kavaka 17: 21–27. Sharma JR, Das K (2002). New records of Saini SS, Atri NS (1989b). North Indian Russulaceae from India. Agaricales XI-Section Russula Pers. in Phytotaxonomy 2: 11-15. India, Indian Journal of Mycology and Varghese SP, Pradeep CK, Vrida KB (2010). Plant Pathology 19: 44-49. Mushrooms of tribal importance in Saini SS, Atri NS, Bhupal M (1988). North Wayanad area of Kerala. Journal of Indian Agaricales V. Indian Mycopathological Research 48(2): 311- Phytopathology 41: 622-625. 320. Saini SS, Atri NS, Saini MK (1989). North Verma RK, Pandro V, Pyasi A (2018). Indian Agaricales VI. Journal of the Diversity and distribution of Russula in Indian Botanical Society 68: 205–208. India with reference to central Indian Sarwal BM (1984). Taxonomic studies on species. International Journal of Current Indian Agarics II. Indian Microbiology and Applied Science Phytopathology 37: 228-233. 7(10): 3078-3103. Sathe AV, Deshpande S, Kulkarni SM, Daniel Vishwakarma MP, Bhatt RP, Joshi Sweta J (1980) (1981). Agaricales (2012). Macrofungal diversity in moist (Mushrooms) of South-west India - Part temperate forests of Garhwal Himalaya. I: Agaricales (Mushrooms) of Indian Journal of Science and Maharashtra State (MACS, Pune). Pp. Technology 5(1): 1928-1932. 1-114. Vrinda KB, Pradeep CK, Abraham TK Shaffer RL (1964). The subsection (1997a). A new species of Russula from Lactarioideae of Russula. Mycologia. Kerala, India. Mycotaxon 62: 87-96. 56(2):202-231 Vrinda KB, Pradeep CK, Abraham TK Shaffer RL (1975). Some common North (1997b). A new species of Russula from American species of Russula subsect. Kerala, India. Mycotaxon 62: 389-394. Emeticinae. Beihefte zur Nova Watling R, Gregory NM (1980). Larger fungi Hedwigia 51: 207-237. from Kashmir. Nova Hedwigia 32(2-3): Shajahan M, Samajpati N (1995). 493-564. Ectomycorrhizal fungi of Shorea

How to cite this article:

Verma, R.K., V. Pandro and Rao, G.R. 2019. Three Records of Russula Mushroom from Sal Forest of Central India. Int.J.Curr.Microbiol.App.Sci. 8(02): 445-455. doi: https://doi.org/10.20546/ijcmas.2019.802.050

455