Review of literature
2. REVIEW OF LITERATURE
The systematic study of fungi in general and mushroom in particular started
with the invention of advanced version of microscope. The order Agaricales to which
the lepiotoid and termitophilous mushrooms belongs was established by Underw in
1899. In Europe, Linnaeus (1753) used the generic name Agaricus to include all the
gill bearing fungi. The Dutch Christian Hendrik Persoon (1794, 1796, 1797, 1801)
established the first classification of mushrooms with such skill so as to be considered
a founder of modern mycology. He placed the agarics and boletes under order
Hymenothecii of the class Gymnocarpii. He was the first to introduce the term
‘hymenium’ and subdivided order Hymenothecii on the basis of hymenial characters.
Later, Elias Magnus Fries (1821 - 1832) further elaborated the classification of fungi,
using spore colour and various microscopic characteristics, the methods which are
still in use by taxonomists today. Saccardo (1882-1931) also emphasized the
importance of spore colour in the taxonomy of mushrooms and thus recognized four
sub–divisions of agarics based upon their spore colour, namely – Melanosporae
(spores purple brown or black), Ochrosporae (spores ochre or rust colored),
Rhodosporae (spore rosy) and Leucospori (spores white). Singer (1986) has also laid
much emphasis on the spore colour character in mushroom taxonomy in his
monograph “The Agaricales in Modern Taxonomy”. He recognized 17 families, 230
genera and 5658 species under order Agaricales. Contrary to Singer’s (1986) concept,
Hawksworth et al., (1995) in The Dictionary of Fungi recognised the splitted version
of earstwhile order Agaricales and recognized five orders namely, Agaricales,
Boletales, Bonderzewiales, Cortinariales and Russulales. Kirk et al., (2008) in
“Dictionary of the fungi” recognized four independent orders to include agarics and
boletes, namely Agaricales, Boletales, Canthrellals and Russulales.
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Review of Literature
The
phylogenetic
classification
of
the
major
groups
within
the
Agaricomycetes to which lepiotoid and termitophilous mushrooms belongs still
remains unsettled. It has been divided into Heterobasidiomycetes (jelly fungi) and
Homobasidiomycetes (mushroom-forming fungi) based on the structure of the septal
pore apparatus and the spindle pole body. In Homobasidiomycetes, a preliminary
phylogenetic outline with 8 major clades has been revealed using nSSU (nuclear small
subunit) and mt-SSU (mitochondrial single subunit) rDNA sequences. These major
clades coincided with Polyporoid, Euagarics, Bolete, Russuloid, Thelephoroid,
Hymenochaetoid, Cantharelloid and Gomphoid-phalloid clade (Hibbett et al., 2007).
Lot of work is available in the literature on the systematics of agarics but some
of the significant contributions on mushroom systematics which also included
contributions on lepiotoid and termitophilous mushrooms are by Heim (1942 a, b, c,
1977), Smith (1949), Dennis (1952, 1953), Singer (1951, 1961, 1975, 1986),
Heinemann (1968, 1973, 1977), Largent (1973), Pegler (1972, 1977, 1983, 1986),
Sundberg (1971 a, b, 1976, 1989), Smith and Sundberg (1979), Zang (1981),
Westhuizen and Eicker (1990), Reid (1990), Pegler and Vanhaecke (1994), Akers and
Sundberg (1997, 1998, 2000, 2001), Sieger (2003), Wang (2005), Tang et al., (2005),
Vellinga and Huijser, 1997, 1998) and Vellinga (2000, 2001 a, b, 2002, 2006, 2007,
2010).
2.1 Taxonomy-The World scenario
Lepiotoid and termitophilous mushrooms are cosmopolitan in distribution.
The main work on various aspects of these mushrooms including diversity,
sociobiology, edibility, ecology and conservation aspects has been done in Europe,
North America and Africa. Some of the significant contributions on lepiotoid
mushrooms are by Morgan (1907), Kauffmann (1924), Dennis (1952), Smith (1966),
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Beeli (1936), Murrill (1911, 1912, 1914, 1922, 1939 a, b, 1940, 1941 a, b, 1942,
1943, 1945 a, b, 1946, 1949, 1951), Heinemann (1968, 1973,
1975, 1989),
Heinemann and Little Flower (1984), Reid (1990), Largent et al., 1976), Sundberg
(1971 a, b, 1976, 1989), Pegler (1972, 1983, 1986), Sieger (2003) and Vellinga
(2007), etc.
From systematic point of view, the world over lepiotoid mushrooms are
represented by 400 species of Lepiota, 10 species of Cystolepiota, 30 species of
Macrolepiota, 40 species of Leucocoprinus, 90 species of Leucoagaricus, 8 species of
Chlorophyllum, 2 species of Hiatulopsis, 1 species of Janauaria, and 1 species of
Ripartitella (Kirk et al., 2008). The Genus Lepiota is relatively well investigated in
Europe (Bon, 1993, Candusso and Lanzoni, 1990, Kelderman, 1994 and numerous
other articles especially by Italian authors). Following the recognition of segregate
genera within the family Lepiotaceae, the genus Lepiota has received various
sectional treatments. The different sections recognized are Ovisporae, Fuscovinacae,
Stenosporae and Lilaceae (Bon 1981, Singer 1986, Candusso and Lanzoni, 1990).
Two more sections, namely Cristatae and Sericellae for those with hymeniform layer
and radially arranged filamentous hyphae, devoid of differentiated terminal elements,
respectively have been recognized in Lepiota by Kühner (1936) and Singer (1986).
Morgan (1907) described Northern American species of Lepiota. Kauffman (1924)
investigated major group of Lepiota in United States. Murrill (1941 a, b, 1942, 1943,
1944, 1945 a, b, 1946, 1949, 1951) made marked additions in genus Lepiota and
fleshy basidiomycetes of Florida. Smith (1966) made a significant contribution
towards a monograph on genus Lepiota. Heinemann (1968) described Macrolepiota
from Congo-Kinshasa.
Pazmany (1984) described 7 species of Leucoagaricus from Romania. Zheng
(1985) described 13 species of Lepiota in macrofungus flora of China’s Guangdong
Province. Akers and Sundberg (1997, 2001) made taxonomic observations on
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Review of Literature
Leucoagaricus hortensis and some synonyms from Florida and also elaborated the
critical taxonomic characters of stenosporic species of Lepiota. Reid (1990, 1993)
described leucocoprinoid fungi from Britain and provided a key to the Leucocoprinus
badhamii complex in Europe. Reid and Eicker (1991) gave a detailed account on
Chlorophyllum molybdites. Reid and Eicker (1991), Bougher (1998) and Young
(1989) discussed poisonous qualities of Chlorophyllum molybdites. Reid (1995) gave
an account on Leucoagaricus melanotrichus and similar species from South Africa.
Sundberg (1989) discussed Lepiota species with hymeniform pileus covering.
Vellinga (2003 a, b, c, 2004) worked out the phylogeny and taxonomy of
Macrolepiota and lepiotaceous fungi of California. Vellinga (2003 c) while working
on the complex of Chlorophyllum rhacodes, gave a checklist and key to seven species
of Chlorophyllum and Macrolepiota from Australia. Vellinga (2010) discussed eight
species of Lepiota with a hymenial pileus covering. Ge and Yang (2006), gave an
illustrated account of genus Chlorophyllum in China.
As compared termitophilous mushrooms represent a smaller group with only a
single genus Termitomyces with 30 species on worldwide basis (Kirk et al., 2008).
Heim (1942 a) was the first to recognize Termitomyces as an independent genus with
10 species and 6 forms. As a matter of fact a number of species of this genus have
been described mainly from tropical areas particularly Southern Africa, South East
Asia and throughout the equator (Pegler and Vanhaecke 1994). Some significant
contributions on these mushrooms have been made from Africa by Heim (1941, 1942
a, b, c, 1951, 1952, 1958, 1977), Morris (1986), Otieno (1964, 1969), Sands (1970),
Westhuizen and Eicker (1990), Pegler and Piearce (1980), Pegler (1986), Pegler and
Vanhaecke (1994) and from China by Zang (1981) and Wei et al., (2004). The genus
Termitomyces was placed within Tricholomataceae by Singer (1986), on the basis of
siderophilous granulation in basidia which is close to Lyophyllaceae. Later, on the
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Review of literature
basis of the pluteoid habitat, densely crowded free lamellae and pink spore deposit,
the genus was placed in Lyophyllaceae (Kirk et al., 2008). Batra and Batra (1966)
worked on the subject of association of fungi with termites. Heim (1977) published a
monograph with 28 taxa of these mushrooms covering Africa, Asia (Reid, 1975;
Saarimäki et al., 1994), Cameroon (Mossebo et al., 2002) and South America
(Gómez, 1995). In total, 68 taxa have been published in Termitomyces, with 81 names
including combinations and autonames. According to Index Fungorum database,
currently 55 names published in Termitomyces based on 53 types are reported to be
distributed throughout the equatorial and Sothern Africa and widely in South East
Asia.
Zang (1981, 1992) proposed a new Genus Sinotermitomyces including five
species, namely S. carnosus, S. cavus, S. griseus, S. rugosiceps and S. taiwansis. Later
on the genus Sinotermitomyces was merged with Termitomyces by Wei et al., (2006).
In China 25 taxa of Termitomyces, including three new species have been reported
from 17 provinces within China (Wei and Yao, 2003). Tang et al., (2005) revised
three Termitomyces species from India and concluded T. longiradicatus and T.
quilonensis and T. poonensis to be synonyms of T. heimii and T. eurhizus.
2.2 Taxonomy-The Indian scenario
In India various mycologists have made significant contributions in mycodiversity, some of these are Berkeley (1839, 1856, 1867), Montagne (1842, 1846),
Sathe and Rahalkar (1975, 1976), Sathe and Sasangan (1977), Sarwal and Rawla
(1983), Natarajan (1995), Purkayastha and Chandra, (1974, 1975). Linnaeus (1753)
for the first time reported few mushrooms from India. Verma et al., (1995) recorded
the results of a macrofungal survey of the north-eastern hills. Berkeley (1876) was
probably the first to report larger fungi from Kashmir valley. Sustained work carried
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Review of Literature
out by Kaul, Kachroo and Abraham for over two decades resulted in the recording of
262 larger fungi from this region. A significant contribution to this study was by
Watling and Gregory (1980) as they published a list of 119 species from area.
Natarajan (1995) started a series entitled “South Indian Agaricales” and presented a
list of 230 agaric and bolete species distributed among 67 genera from southern
Indian states excluding Kerela. Status of Indian Agaricales was reviewed first by
Sathe and Rahalkar (1975) taking 1825 as the base year and then by Manjula (1983),
providing a very exhaustive list of Agaricoid and Boletoid fungi from India and
Nepal. This is so far the best comprehensive list, which enumerates 538 valid genera
and 20 families in the order Agaricales from India. From a survey of mushrooms in
the North West Himalayas, Lakhanpal (1995, 1997) and Lakhanpal et al., (2010)
recorded agarics belonging to 300 species, 59 genera and 15 families of Agaricales.
This survey provides an inventory of the species occurring in the Himalayas, a list of
species of mushrooms, which enter into mycorrhizal relationship with forest trees and
a list and description of nonconventional edible species discovered during the surveys.
Doshi and Sharma (1997) provided a detailed list of macrofungi consisting of 173
species belonging to 95 genera recorded from Rajasthan. Saini and Atri (1995)
reviewed exploratory work on mushrooms from Punjab and listed 94 taxa spread over
24 genera. Patil et al., (1995) listed 212 species of agarics spread over 63 genera from
Maharashtra.
From India the genus Lepiota is known by 92 species (Vasudeva, 1960;
Bilgrami et al., 1991; Kaur, 2000; Kour, 2005; Jamalludin et al., 2001, Kumar and
Manimohan 2009 a). Prominent Indian contributions are by Rawla et al., (1982,
1983), Natarajan and Raman (1981), Natarajan and Manjula (1983), Sarwal (1984),
Atri et al., (1996, 2000). Abraham and Kaul (1985), Kumar and Manimohan (2004,
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Review of literature
2009 c), Dhancholia and Sinha (1990) and Vrinda et al., (1999, 2003) documented
and described number of species of Leucocoprinus from Jammu and Kashmir, North
West India, Orissa and Kerala, respectively. Butler and Bisby (1931), Vasudeva,
(1960), Bilgrami et al., (1991) and Jamalludin et al., (2001) listed number of agarics
including species of Leucocoprinus and Macrolepiota in Fungi of India. Mondel and
Purkayastha (1983) documented Leucocoprinus meleagris from West Bengal. Sathe
and Sasangan (1977) and Sathe et al., (1981) are significant contributors on
mushroom systematics from South West India. Ghosh and Pathak (1965), Ghosh et
al., (1976) and Sharma et al., (1977) documented species of Macrolepiota and
Chlorophyllum from India. Natarajan and Manjula (1983) described 14 species and 2
new varieties of Lepiota from Madras. Manimohan and Leelavathy, (1988) recorded
and described 5 taxa new to India, including Lepiota vindicta. Kumar and Manimohan
(2004) described one new species of Leucocoprinus from Kerala.
Atri et al., (1996) published six species of Lepiota of which two were new
varieties and three were first time reports from India. Atri and Saini (2000) provided
detailed information regarding mushroom systematics for beginners. Atri et al. (2000)
gave a taxonomic account of six species of Lepiota collected from Punjab. Vrinda et
al., (2003) gave an illustrated account of some leucocoprinoid mushrooms from
Western Ghats. Narayanan and Natarajan (2004) illustrated some interesting agarics
from South India. Deepa et al., (2006) described some leucocoprinoid fungi from
Western Ghats of Kerala. Kumar and Manimohan (2009 a) documented twenty-two
taxa belonging to the agaric genus Lepiota from Kerala, including eight new species
and one new variety, namely L. ananya, L. anupama, L. babruka, L. babruzalka, L.
harithaka, L. nirupama, L. shveta, L. zalkavritha and L. brevipes var. distincta. Kour
et al., (2010) published 7 species of Lepiota from North West India. There is hardly
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Review of Literature
any documentation of other lepiotoid genera from any part of India, including the
present area of investigation.
While working on termitophilous mushrooms Atri and Kour (2003) and Atri et
al., (2005 b) documented 12 species of Termitomyces and one species of
Sinotermitomyces from India and gave a key to their determination. Purkayastha and
Chandra (1975) described Termitomyces eurhizus from West Bengal. Chakaravarty
and Khatua (1979) described Termitomyces microcarpus from India for the first time.
Natarajan (1975, 1977 a, b, 1979) described number of species of these mushrooms
including some new species from South India. Rawla et al., (1983) described
Termitomyces from India. Leelavathy et al., (1983) described genus Termitomyces in
India. Other Indian contributors are Doshi and Sharma (1990) from Rajasthan and
Bhavani Devi et al., (1980) from Kerala. Atri et al., (1995) published taxonomic
studies on the genus Termitomyces. Vrinda et al., (2002) described Termitomyces
umkowaani from Western Ghats. Vrinda and Pradeep (2009) described an edible
species T. sagittiformis - a lesser known edible mushroom from the Western Ghats.
2.3 Taxonomy- A molecular approach
Molecular techniques are becoming increasingly important as means for
obtaining characters for studying taxonomic and phylogenetic relationships among
fungi (Zambino and Szabo, 1993). The limitation of identification of mushroom
strains based on a few morphological characters can be overcome by the use of DNA
based techniques like RAPD, AFLP, RFLP or DNA sequence analyses (ITS, nLSU,
nSSU, mtSSU and RPB2). Any of the molecular methods could be combined with
morphological methods to make identification of fungal species reliable (Khush et al.,
1992; Calonje et al., 1997). Little information is available on the use of ITS in the
taxonomy of some of these mushroom isolates. Johnson and Vilgalys (1998)
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Review of literature
investigated the phylogenetic relationships among lepiotoid and closely related taxa
using DNA sequence data. Results from parsimony analysis were reported to be
consistent with the exclusion of the tribe Cystodermateae (Cystoderma and
Ripartitella) from the family Agaricaceae, and the retention of the tribes Lepioteae
and Leucocoprineae. Johnson (1999), Johnson and Vilgalys (1998) and Vellinga
(2004) found phylogenetic relationship within Lepiota sensu lato based on
morphological and molecular data and resolved the taxonomy and phylogenetic
relationship among many species of Leucoagaricus, Lepiota and Leucocoprinus.
Moncalvo et al., (2000, 2002) and Hoffstetter et al., (2002) have shown the classical
circumscriptions of both Tricholomataceae and Lyophyllaceae as recognized by
Singer (1986) to be problematic. Rouland Lefevre et al., (2002) reconstructed a
phylogeny of some termitophilic fungi from sequences of South African data and
postulated with evidence Termitomyces to be a monophyletic group. Vellinga et al.,
(2003) determined the position and composition of Macrolepiota within the
Agaricaceae and its phylogenetic relationships with other members of the family by
using both molecular (ITS and LSU rDNA sequences) and morphological characters.
Froslev et al., (2003) found phylogenetic relationship of Termitomyces and related
taxa and sequenced portions of nuclear LSU rDNA and mitochondrial SSU rDNA
from fruitbodies of termitophilous mushrooms representing the total range of
morphological variation and geographical distribution. Later on Wei et al., (2006)
revised taxonomic status of Sinotermitomyces and merged the genus with the
representatives of known Termitomyces species on the basis of phylogenetic studies.
Ge et al., (2010) made investigations on the six species of the genus Macrolepiota on
the basis of morphology and DNA sequences data. No attempt so far has been made
to work out the molecular phylogeny of Indian lepiotoid and termitophilous
mushrooms.
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2.4 Ethno-mycological information
Collection and consumption of wild edible mushrooms is an important source
of healthy nutrition for the rural communities during the rainy season in several parts
of Africa, Asia, Europe and South America (Nakalembe et al., 2009). All the
Termitomyces species are in use as preferred food by locals in different parts of
tropical and subtropical regions because of their unique texture, flavour and taste.
Mushrooms are integral part of everyday life of such people during monsoon season
and many interesting stories are reported to be associated with these (Oso, 1975).
Adhikari et al., (2005) documented many beliefs and ideas about edibility of wild
mushrooms in Western and Central Nepal.
Nakalembe et al., (2009) recorded
mycological knowledge and usage of termitophilous mushrooms in Mid-Western
Uganda. Ethno-mycological findings by Akapaja et al., (2003) showed that the
Termitomyces species were used as traditional food and good source of nutrients
including proteins, fat, fibers and minerals and alternative source of income and
employment to women and old people. Harkönen (2002) reported the selling of edible
species of Termitomyces, Cantharellus, Lactarius, Russula and Amanita in Tanzania
and road side markets. Atri et al., (2005 b, 2010) elaborated the edibility and
sociobiological aspects of these mushrooms in Punjab state. Rajak and Rai (2005)
made a documentary file on edible tribal mushroom resources of Central India and
their ethnological aspects.
2.5 Nutritional and Nutraceutical value of mushrooms
Mushrooms have long been valued as nutritional foods by many scientists
throughout the world (Chang and Miles, 2004). They have received an incredible
interest in recent decades with the realization that these are good sources of delicious
food with excellent flavor, aroma, exotic tasteful appeal and high nutritional traits
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because they contain good quality proteins, unsaturated fatty acids, minerals and
vitamins (Wahid et al., 1998). Wild edible mushrooms are traditionally used by many
Asian countries as food and medicine and are becoming more and more important in
our diet for their nutritional characteristics (Manzi et al., 1999; Sanmee et al., 2003).
Some edible mushroom species are sources of bioactive compounds for medicinal
applications, possessing antitumour, cardiovascular, antiviral, antibacterial and other
activities (Chang, 1996; Helpern and Miller, 2002; Wasser, 2002; Ferreira et al.,
2009, 2010). Still there are several varieties of wild mushrooms whose nutritive
profiles have not been described well. Several workers have estimated nutritional
value of fruiting bodies of Termitomyces species from Africa and Asia (Bano et al.,
1964; Mukiibi, 1973; Purkayastha and Chandra, 1976; Parent and Theon, 1978; Botha
and Eicker, 1992). They have found superior nutritional value of Termitomyces
species in general when compared with other edible mushroom species. Termitomyces
species are highly ranked mushrooms followed by Pleurotus species and Polyporus
tenuiculus and among the Termitomyces species most favoured species are T.
microcarpus, T. tyleranus, T. aurantiacus, T. microcarpus, T. eurhizus and T.
clypeatus (Nakalembe et al., 2009). Botha and Eicker (1992) reported that the
proteins of T. umkowanii has very high sulphur containing amino acids which exceeds
the essential amino acid content of the reference protein by 150%. Aletor and
Aladetimi (1995) found highest protein contents in T. robustus (33.8%) followed by
other edible species.
Adejumo and Awosanya (2005) reported highest protein content in T.
mammiformis (36.8%) followed by Lactarius triviralis and other mushroom species.
Several workers screened the antioxidant properties of mushrooms (Puttaraju et al.,
2006; Alvarez- Parrilla et al., 2007; Oboh and Shodehinde, 2009). Puttaraju et al.,
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(2006) analyzed the total antioxidative status, employing multimechanistic
antioxidative assays such as inhibition of lipid peroxidation, determination of
reducing power, and free radical scavenging ability, in addition to determination of
total phenolics in 23 species of mushrooms collected from Indian forests. AlvarezParrilla et al., (2007) determined the total phenols and antioxidant activity of three
commercial and wild mushrooms (Agaricus sp., Boletus sp. and Macrolepiota sp.)
from Chihuahua, Mexico. Oboh and Shodehinde (2009) evaluated the distribution of
nutrients, polyphenols and antioxidant activities between the pilei and stipes of three
commonly consumed edible mushrooms in Nigeria namely: T. robustus, Coprinus sp.
and Volvariella esculenta. Signore et al., (1997) reported considerable amount of
phenolic compounds in Macrolepiota procera, Leucoagricus pudicus, Lepiota
clypeolaria, L. erminea and in other basidiomycetes fungi. Gbolagade et al., (2007)
investigated antagonistic effect of crude and purified extracts of Nigerian fungi
against selected pathogenic microorganisms in which pure extracts of Termitomyces
microcarpus and T. robustus fungi and reported best antibacterial activity in
comparison to others. Mukherjee, (2002) and Mukherjee et al., (2006) evaluated
cellobiase activity and secretion in the presence of glycosylation inhibitors or by coaggregation with sucrase in the extracellular, intracellular and cell bound fractions of
Termitomyces clypeatus. Mukhopadhyay et al., (1997) reported the production of
acetyl esterase in case of T. clypeatus when stimulated by xylan, cellulose, arabinose
and arabinose-containing polysaccharides.
Oboh and Shodehinde (2009) found higher protein in T. mammiformis than
other edible mushrooms of Nigeria and more protein were recorded in pileus than
stipe (28.6% and 24.8%, respectively). Oboh and Shodehinde (2009) also found
higher phenolic contents in pileus than stipe and no difference in carbohydrates in
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stipe and pileus of T. robustus. The protein, fat and fiber content have been estimated
in T. letestui (3.9%, 0.7% and 0.5%, respectively on fresh wt. basis) by Masamba and
Mwale (2010). Highest mineral concentration in dry matter ash was evaluated in
young Macrolepiota procera cap by Olfati et al., (2009). Nabubuya et al., (2010)
evaluated the nutritional properties of T. microcarpus and reported protein, lipid,
crude fiber, potassium, calcium and phosphorus in this mushroom.
Conservation of biological diversity has been the subject of intense debate all
over the world. Not much has been done to conserve fungal diversity in general and
mushrooms in particular. Conservation studies on fungal diversity are a recent
development on the world scene. Some of the contributions in this regard are by
Arnolds, 1991; Kaul, 1992; Atri and Lakhanpal, 2002.
Perusal of the literature reveals that lepiotoid and termitophilous mushrooms
have received scattered attention in India. They represent an important group of fungi,
many of which are most preferred because of their edibility and nutraceutical utility
(Munyanziza and Ngaga, 2006). In view of their importance and meager amount of
work on systematics, sociobiology, nutritional and nutraceutical aspects, ecology and
conservation, present research problem have been undertaken for investigation.
19