On the Basket Stinkhorn Mushroom Phallus merulinus (Phallaceae) in Mangalore, Karnataka, India
K.R. Sridhar 1 & N.C. Karun 2
1,2 Department of Biosciences, Mangalore University, Mangalagangotri, Mangalore, Karnataka 574199, India
1 email@example.com (corresponding author), 2 firstname.lastname@example.org
The mushroom family Phallaceae (commonly called stinkhorns) comprises 77 species belongs to 21 genera (Kirk et al. 2008). The genus Phallus is cosmopolitan in the tropics (e.g., Australia, China, Hawaii, India, Malaysia, Mexico, South America, Thailand and Taiwan) (Lee 1957; Grgurinovic et al. 2001; Li et al. 2002; Barrett & Stuckey 2008; Hemmes & Dsejardin 2009; Dash et al. 2010; Mohanan 2011). Among the Phallales of southern Australia, 76% are soil saprophytes, 29% are litter saprophytes and 10% are ecotomycorrhizal (Grgurinovic et al. 2001). In India, Phallus species are known from the eastern Himalaya (Sikkim, Churra and Khasi), West Bengal (Santhiniketan), Odisha (Kutrumali), Maharashtra (Khandala), Karnataka (Kodagu and Shimoga) and Kerala (Anamudishola, Athirappally, Erampadam and Sholayar) (Bhagwat et al. 2005; Bakshi & Mandal 2006; Abrar et al. 2007; Swapna et al. 2008; Dash et al. 2010; Mohanan 2011).
All Phallaceae members begin their development with a gelatinous spherical or oval basidium, however, their developed structures show drastic variations in pattern and color. For instance, some have no indusium (basket or skirt) (e.g., Phallus anamudii) and some possess white or colored indusium (e.g., Phallus indusiatus and P. merulinus) (Mohanan 2011). Similarly, the structure and color of gleba (cap) also differ from one another. Phallus indusiatus (commonly known as bamboo fungus) is wide spread in the tropics and considered to be an edible mushroom in China and commercially cultivated since 1979 (Huang 2002). Interestingly, the highest mycelial growth was seen during the cultivation of P. indusiatus on bamboo leaf as the sole substrate (Cheong et al. 2000).
On routine forays to investigate mushrooms at the Mangalore University Campus, our attention was drawn towards 3ha of a 20 year-old arboretum (12048’50’’N & 74055’38’’E) established with the support of the McArthur Foundation (Shetty & Kaveriappa 2001). The arboretum encompasses 57 tree species, two bamboo species and 23 shrub species of the Western Ghats (some of them are endangered). We collected a Phallus sp. growing in the basins of the monocots of the arboretum during the monsoon (August–October 2011). Phallus has been considered as a partial saprobe by Ainsworth et al. (1971) and this genus accounts for 168 records in ‘Index Fungorum’ (http://www.indexfungorum.org/names/names.asp). The present note deals with Phallus merulinus found in the arboretum. Besides the arboretum, this fungus is known in the basins of organically cultivated monocots (e.g., coconut and banana) during the monsoon and post-monsoon seasons. The description of this fungus is based on the observations of several individuals in and around the arboretum and the dimensions are based on the mean of 10 mature basidiocarps.
Dictyophora merulina Berk. Intellectual Observer 9: 404 (1886)
Clautriavia merulina (Berk.) Lloyd, Synopsis of the known Phalloids: 24 (1909). Mycol. Writings 3, fig. 19 (1909)
Dictyophora irpicina Pat. Bull. Soc. Mycol. Fr. 14: 190 (1898)
Phallus irpicinus (Pat.) Lloyd. Mycol. Notes (26): 331 (1907); Mycol. Writings 2 (1907)
Phallus merulinus (Berk.) Cooke (Grevillea 11 (58): 57, 1882)
Basionym: Dictyophora merulina Berk. (1866)
Phallus merulinus (Berk.) Cooke has expanded from solitary basidiocarp (egg), partially embedded in soil or decomposing leaf litter, subglobose, 2.6x3.2 cm, egg white, 0.1cm thick elastic volva attached to substrate with conspicuous 2-3 white rhizomorphs (4–6x0.1–0.2 cm) and mature basidiocarp 10.6cm high. Gleba (cap) yellowish-grey, subglobose, 2.6x2.9 cm, with or without volval remnants, lower margin wavy, incurved towards the stipe, apex round to conical with an apical pore (which opens up widely later), sticky, gelatinous, surface smooth and partially undulate. Indusium (basket) white, semielastic and forming polyhedral to round net, 9.4cm in diameter, margin wavy and hangs down to two-thirds of the stipe. Stipe (stalk) white, pitted, cylindrical to partially fusoid, slightly tapering at apex with bulbous base, 9.2x2.3 cm, hollow, spongy and wall composed of chambers partially opened outwards. Partial veil white, inconspicuous on the stipe. Volva egg white outside, light caramel inside, 3.2x3.8 cm. Basidiospores long-ellipsoid, 2.9–3.5x0.8–1.3 Ķm, subhyaline and smooth.
Herbarium No. MUBSNCKKRS-001, Department of Biosciences, Mangalore University, Mangalagangotri, Mangalore.
Substrates and growth: Substrates of Phallus merulinus are usually the dead monocot debris embedded in soil in the basins of the monocots [(Caryota urens L., Cocos nucifera L., Ensele superbum (Roxb.) Cheesman, Musa paradisiaca L., Ochlandra scriptoria (Dennst.) C. Fischer and O. travancorica Benth. ex Gamble)]. Usually the unopened basidiocarps are prominently visible in the evening (17:00–19:00 hr) and fully matured mushrooms are seen next day early morning, requiring about 6–8 hr to transform from egg to matured mushroom. Conspicuous basidium emerges, enlarges by rupturing (Image 1a), the stipe extension takes place in 3–4 hr (Image 1b-d), indusium emerges in the next 2–3 hr and the indusium fully opens up within 1–2 hr (Image 1e). Subsequently (within 4–5 hr) the indusium shrinks, stipe bends and presses into the soil in the next 2–3 hr (Image 1f). Unlike other Phallus sp. (e.g., P. indusiatus), none of the matured individuals of P. merulinus collapsed due to their own weight in our observations. The indusium of P. merulinus is shorter than P. indusiatus and thus there are less chances to collapse (Reid 1977). The cap of Phallus merulinus is smooth unlike conspicuous reticulations in P. indusiatus (Burk & Smith 1978). The life cycle of P. merulinus in our study was approximately 25–30 days, which includes vegetative and reproductive phases. Phallus merulinus was devoid of specific odor. The red-eyed Drosophila was the major insect attracted by this mushroom at egg stage, their congregation was highest on gleba than on stipe and indusium facilitating spore dispersal. Some red and black ants were also attracted towards the mature basidiocarp.
Metabolites: A variety of metabolites has been reported from P. indusiatus (e.g., enzymes, polysaccharides, non-volatile compounds and antioxidants). Cellulase and amylase were active at 450C and the activity of the latter was comparable to potent thermophilic Bacillus sp. (Bakshi & Mandal 2006). Tyrosinase inhibitor (5-hydroxymethyl-2-furfural) could serve as skin depigmenting and lightening agent (Sharma et al. 2004; Parvez et al. 2006). Two glucans were isolated from P. indusiatus [b (1-3)-D-glucan; (1-6)-branched (1-3)-b-D-glucan (T-5-N)] (Hara et al. 1982; Wang et al. 2009) and fucomannogalactan (glycan) has been considered an immunomodulator (Wasser 2002; Zhang et al. 2007). The polysaccharides isolated from P. indusiatus also showed antitumor activities (Ukai et al. 1983). Non-volatile taste components have been reported by Guo et al. (2005). Total polyphenols were considered to be the major antioxidant components by Mau et al. (2002). Excellent reducing power, radical-scavenging effects and ferrous ion-chelating effects have been reported (Mau et al. 2002). Hot water extract also showed good antioxidant properties (Oyetayo et al. 2009). Ker et al. (2007) hypothesized that the soluble polysaccharide and monosaccharide profiles (e.g., galactoglucan, galactan, riboglucan, myoinositol and mannogalactans) influence the antioxidant capabilities, which in turn are responsible for other biological activities like anti-inflammatory, immune-enhancing and anticancer properties. Riboglucan (801 kDa) of P. indusiatus exhibited the most potent antioxidant activity. Ker et al. (2007) also indicated that a large amount of myoinositol has good immunobioactivity. Hot water extract also showed broad spectrum antibacterial and antifungal principles (Oyetayo et al. 2009). Phalus indusiatus is historically known to treat many inflammatory, gastric and neural disorders since 618AD in China (Ker et al. 2011). As seen in P. indusiatus, alternatively a wide range of bioactive metabolites of medicinal and therapeutic potential are likely to exist in P. merulinus.
Conclusions: Degradation and fragmentation of forests lead to a considerable decline of the diversity of flora and fauna. After flora and fauna, saprophagus fungi constitute the third important component of forest ecosystems involved in detritus transformation, turnover and mineralization. Compared to flora and fauna, our knowledge on the diversity, distribution and impact of forest detritus degradation by fungi is meager. Rehabilitation of forest communities needs considerable duration as macrofungi prefers old-growth microhabitats than new microhabitats (Norden & Appelqvist 2001; Brown et al. 2006). If we attempt to preserve the gene pool of macrofungi in situ, we need to preserve the old-growth forests, which are endowed with ample quantity of diverse detritus (e.g., wood stubs, fallen logs, twigs/bark/leaves and termite mounds) suitable for fungal existence and perpetuation. The occurrence of P. merulinus in the 20-year old arboretum of Mangalore University justifies its preference for old-growth forests for its growth and perpetuation.
Abrar, S., S. Swapna & M. Krishnappa (2007). Dictyophora cinnabarina. Current Science 92: 1219–1220.
Ainsworth, G.C., P.W. James & D.L. Hawksworth (1971). Ainsworth and Bisby’s Dictionary of The Fungi, 6th Edition. Commonwealth Mycological Institute, Kew, 166pp.
Bakshi, D. & N.C. Mandal (2006). Activities of some catabolic and anabolic enzymes of carbohydrate metabolism during developmental phases of fruit-bodies of Dictyophora indusiata and Geastrum fornicatum. Current science 90: 1062–1064.
Barrett, M. & B. Stuckey (2008). Phallus merulinus newly reported for the top end. Fungimap Newsletter 36: 16.
Bhagwat, S.A., C.G. Kushalappa, P.H. Williams & N.D. Brown (2005). The Role of Informal Protected Areas in Maintaining Biodiversity in the Western Ghats of India. Ecology and Society 10: 1–40.
Brown, N., S. Bhagwat & S. Watkinson (2006). Macrofungal diversity in fragmented and disturbed forests of the Western Ghats of India. Journal of Applied Ecology 43: 11–17.
Burk, W.R. & D.R. Smith (1978). Dictyophora multicolor, new to Guam. Mycologia 70: 1258–59.
Cheong, J.C., G.P. Kim, H.K. Kim, J.J. Park & B.K. Chung (2000). Cultural characteristics of veiled lady mushroom, Dictyophora spp. Mycobiology 28: 165–170.
Dash, P.K., D.K. Sahu, S. Sahoo & R. Das (2010). Phallus indusiatus Vent. & Pers. (Basidiomycetes) - a new generic record from Eastern Ghats of India. Journal of Threatened Taxa 2(8): 1096–1098.
Grgurinovic, C.A. & I.A. Simpson (2001). Conservation Status of the known Agaricales, Bolelales, Canlharellales, Lycoperdales, Phallales and Russulales of South Australia. Fungal Diversity 8: 97–127.
Guo, Y.N., B. Xiong, B. Tang, J. Fan & H. Chen (2005). Effect of zhusuntuogai oral solution in repairing immune function of damaged rats by radiation. Chinese Journal of Clinical Rehabilitation 9: 116–117.
Hara, C., T. Kiho, T. Tanaka & S. Ukai (1982). Anti-inflammatory activity and conformational behavior of a branched (1 leads to 3)-beta-D-glucan from an alkaline extract of Dictyophora indusiata Fisch. Carbohydrate Research 110: 77–87.
Hemmes, D.E. & D.E. Desjardin (1999). International Botanical Congress. San Francisco, USA, 59pp.
Huang, N.L. (2002). Current status and future prospects of mushroom industry in China. Edible Fungi of China 107: 6–8.
Ker, Y.B., K.C. Chen, C.C. Peng, C.L. Hsieh & R.Y. Peng (2011). Structural characteristics and antioxidative capability of the soluble polysaccharides present in Dictyophora indusiata (Vent. Ex Pers.) Fish Phallaceae. In: Corporation Evidence-Based Complementary and Alternative Medicine, Hindawi Publishing, Article # 396013, doi:10.1093/ecam/neq041
Kirk, P.M., P.F. Cannon, D.W. Minter & J.A. Stalpers (2008). Ainsworth & Bisby’s Dictionary of the Fungi. 10th Edition, CAB International, Willingford, UK, 771pp.
Lee, W.S. (1957). Two new phalloids from Taiwan. Mycologia 49: 156-158.
Li, T.R., B. Song & B. Liu (2002). Three taxa of Phallaceae in HMAS, China. Fungal Diversity 11: 123–127.
Mau, J.L., H.C. Lin & S.F. Song (2002). Antioxidant properties of several specialty mushrooms. Food Research International 35: 519–526.
Mohanan, C. (2011). Macrofungi of Kerala. Kerala Forest Research Institute, Hand Book # 27, Kerala, India, 597pp.
Norden, B. & T. Appelqvist (2001). Conceptual problems of ecological continuity and its bioindicators. Biodiversity and Conservation 10: 779–791.
Oyetayo, V.O., C.H. Dong & Y.L. Yao (2009). Antioxidant and antimicrobial properties of aqueous extract from Dictyophora indusiata. Open Mycology Journal 3: 20–26.
Reid, D.A. (1977). Some Gasteromycetes from Trinidad and Tobago. Kew Bulletin 31: 657–90.
Sharma, V.K., J. Choi, N. Sharma, M. Choi & S.Y. Seo (2004). In vitro anti-tyrosinase activity of 5-(hydroxymethyl)-2-furfural isolated from Dictyophora indusiata. Phototherapy Research 18: 841–844.
Shetty, B.V. & K.M. Kaveriappa (2001). An arboretum of endemic plants of Western Ghats at Mangalore University Campus, Karnataka, India. Zoos’ Print Journal 16(3): 431–438.
Swapna, S., S. Abrar & M. Krishnappa (2008). Diversity of macrofungi in semi-evergreen and moist deciduous forest of Shimoga District, Karnataka, India. Journal of Mycology and Plant Pathology 38: 21–26.
Ukai, S., T. Lojp, C. Hara, M. Morita, A. Gao, A. & H.Y. Naomi (1983). Polysaccharides in fungi XIII - antitumor activity of various polysaccharides isolated from Dictyophora indusiata, Ganoderma japonicum, Cordyceps cicadae, Auricularia auricula-Judae and Auricularia species. Chemical & Pharmaceutical Bulletin 31: 741–744.
Wang, J., X. Xu, H. Zheng, J. Li, C. Deng, Z. Xu & J. Chen (2009). Structural Characterization, Chain Conformation, and Morphology of a β-(1→3)-d-Glucan Isolated from the Fruiting Body of Dictyophora indusiata. Journal of Agricultural and Food Chemistry 57: 5918–5924.
Wasser, S.P. (2002). Medicinal mushrooms as a source of antitumor and immunomodulatory polysaccharides. Applied Microbiology and Biotechnology 60: 258–274.
Zhang, M., S.W. Cui, P.C.K. Cheung & Q. Wang (2007). Antitumor polysaccharides from mushrooms: a review on their isolation process, structural characteristics and antitumor activity. Trends in Food Science and Technology 18: 4–19.