Some New Records of Stinkhorns (Phallaceae) from Hollongapar Gibbon Wildlife Sanctuary, Assam, India
This research paper represents for the first time an updated list of stinkhorn family, Phallaceae, in Hollongapar Gibbon Wildlife Sanctuary, Jorhat, Assam, India. There are seven species of stinkhorns naturally present in the study area. A description of all the species is given along with images of fruiting bodies of the fungi and their microstructures; information on the ecology and general distribution and data on the literature have been documented. The seven species of stinkhorns were found in and around area of the sanctuary which include Phallus indusiatus, Phallus duplicatus, Phallus cinnabarinus, Phallus merulinus, Phallus atrovolvatus, Mutinus bambusinus, and Clathrus delicatus.
Fungi are some of the most important organisms in the world, because of their vital role in ecosystem function and influence on humans and human-related activities as discussed by Mueller and Bills . Fungi are not only beautiful but play a significant role in the daily life of human beings besides their utilization in industry, agriculture, and medicine as discussed by Cowan  and Chang and Miles . Moreover, fungi help in bioremediation, in recycling nutrients, and in decomposing the dead organic matter in soil and litter, as biofertilizers and in many other ways (Gadd ). It is necessary to estimate the taxonomic diversity for fungi that will enable fungi to be included in considerations of biodiversity conservation and land-use planning and management as discussed by Mueller and Schmit . The number of fungi recorded in India exceeds 27,000 species, the largest biotic community after insects (Sarbhoy et al. ). Recent estimates of the global species numbers of fungi suggest that the much-used figure of 1.5 million is low, and figures up to 5.1 million have been proposed in the last few years (Hawksworth ). The literature survey revealed that only a fraction of total fungal wealth has been subjected to scientific scrutiny till date. The first list on Indian fungi was published by Butler and Bisby in 1931  and then later on revised by Vasudeva in 1960 . In North East India as a part of Indo Burma biodiversity hotspot  of the world, few number of wild edible macrofungi have been reported by Sarma et al. , Tanti et al. , Khaund and Joshi, , Baruah et al. , and N. I. Sing and S. M. Sing .
The stinkhorns are easily identified due to their fetid smelling, sticky spore masses, or gleba, borne on the end of a stalk called the receptaculum or cap. The characteristic fruiting-body structure, a single, unbranched receptaculum with an externally attached gleba on the upper part, distinguishes the Phallaceae from other families in the Phallales. As discussed by Tuno , stinkhorns are short-lived, typically lasting not more than a few days. The spore mass typically smells of carrion or dung and attracts flies and other insects to help disperse the spores. All species under this family begin their development as oval or round structures known as “eggs” (young stage of basidiocarp); however, their developed structures show drastic variations in pattern and color, as discussed by Mohanan . Similarly, the structure and color of gleba also differ from one another. According to an estimate, the family comprises 21 genera and 77 species (Kirk et al. ).
2. Materials and Methods
2.1. Study Area
Hollongapar Gibbon Wildlife Sanctuary (HGWLS) (Figure 1), more popularly known as Gibbon Wildlife Sanctuary, lies between 26.40–26.45°N latitude and 94.18–94.23°E longitude and it covers an area of 20.98 km2. The sanctuary is situated at 100–130 m asl (meters above sea level) and the average annual rainfall is 249 cm. It is in the tract of rich loamy alluvial formation in the foothills of Nagaland having soil pH ranging between 5.2 and 5.5. The forest of the area as per Champion and Seth  is Assam Plain Alluvial Semi Evergreen Forest with pockets of Wet Evergreen. The vegetation is typically a tree forest mixed with bamboos and canes.
2.2. Collection, Preservation, and Examination
Gibbon Wildlife Sanctuary is composed of five compartments (Figure 1) and these compartments are not only different in size but also different in vegetation composition, topography, and soil nutrients. The size of compartments is given in Table 1. Stratified random sampling technique is used to collect data from different compartments of the sanctuary. A total of 42 transects have been studied in the sanctuary measuring 50 m 20 m for each transect and considering two transects for 1 km square area. The total number of fruit bodies in each compartment as well as in the whole sanctuary has been extrapolated with the help of data collected from different transects (Table 1).
The sampling and collections of stinkhorns were done from April 2012 to September 2013 as suggested by Largent . Field characters such as habit, habitat, odour, colour, and size of the pileus (cap), veil, stipe, and volva presence, or absence of indusium or veil and so forth were noted from the fresh material and photographs were taken in its natural habitat. The colour terminology was used for identification as suggested by Kornerup and Wanscher . The specimens were dried in hot air oven at 40–50°C and stored in air tight plastic containers with some naphthalene balls and the samples of the same species were also preserved in FAA (formalin acetic acid) for further microscopic studies. The help of authentic internet website also accessed for identification of all the collected species that are cited in the reference.
3. Results and Discussion
Seven species of stinkhorns were collected and identified. All the species were found to be a new record for the study area, as well as North East India, which are described below.
3.1. Phallus indusiatus
Vent. Mém. Inst. Natl. Sci., Sci. Math. 1:520 (1798) .
3.1.1. Material Examined
India, North East India (New record), Assam, Jorhat, HGWLS, 26°41′48.57′′N latitude and 94°213′0.53′′E longitude, 123 m asl, on soil of bamboo thicket (Comp.2–4, Table 1), G. Gogoi, 27.7.2012, Accession number: HGWLS/C4/004.
3.1.2. Habit and Distribution
P. indusiatus is commonly called the bamboo fungus, bamboo pith, long net stinkhorn, crinoline stinkhorn, or veiled lady stinkhorns. It grows on dead tree trunk and beneath the soil intermittently with the formation of reproductive structures called “eggs” with a conspicuous rhizomorph at the base existing in the substratum. The eggs are hypogeous when young and become epigeous at maturity, as discussed by Alexopolous et al. . The mature basidiocarp with fetid smell survives only few hours. This fungus has been reported to grow at temperatures between 21 and 25°C in moist bamboo thickets and in tropical areas including Argentina, Australia, Brazil, Cameroon, China, Chinese Taipei, Colombia, Guinea, India, Japan, Republic of Korea, Madagascar, Mexico, New Zealand, Panama, and Singapore . In India it is reported from forest floor of Santiniketan and West Bengal, Bakshi and Mandal , and from Orissa, as described by Dash et al. .
3.1.3. Dimension of the Fruiting Body
Egg (Figure 2(b)) is 3-4 cm in diameter, white to dark brown in colour, smooth in texture, and almost round in shape. The peridium, the outer layer of the egg, is purple with three inner layers. The outer layer is thin, membranous, and elastic, while the inner layer is thicker, gelatinous, and continuous. At maturity, the peridium opens up and remains as a volva at the base of the stipe. The mature basidiocarp (Figure 2(a)) is up to 20 cm tall and girded with a net-like structure called the indusium (18 cm broad) or skirt or veil that hangs down from the conical to bell-shaped cap extending to the volva. The fertile head or cap is gelatinous up to 4 cm tall and 3.5 cm broad; cap is reticulated (pitted and ridged), surface is covered with a layer of greenish-brown and foul-smelling slime, and the gleba and it opens with an apical pore (1 cm broad). Pores or meshes of the indusium are hexagonal (≈1 cm broad); upper pores are slightly larger than the lower ones with one small pore in each side of the hexagon. The stipe is 12–15 cm long and 2.5–3 cm broad. The hollow stalk is white, roughly equal in width throughout its length, and spongy. Basidiospores of P. indusiatus are thin walled, smooth, bacillar, and hyaline and measure 2-3 μm 1–1.5 μm (Figure 2(c)).
It is eaten as a vegetable in some parts of China and Hong Kong and the cost of dried mushroom is 10 to 20 US Dollars per kg as discussed by Huang . But in the study area of Assam, India, people do not eat it, due to its fetid smell.
Eight species of Phallus have been reported from India among which five species were reported by Bilgrami et al.  which include P. impudicus, P. nanus, P. ravenelii, P. rubicundus, and P. rugulosus. Another three species, namely, P. indusiatus (Dash et al. ), Dictyophora cinnabarina (Abrar et al. ), and P. multicolour, were reported from West Bengal (Dutta et al. ). P. indusiatus is somewhat similar to P. duplicatus and P. atrovolvatus but it differs in size of indusium and cap texture. In P. indusiatus indusium is long and big which reaches the ground and cap is highly pitted but in P. duplicatus and P. atrovolvatus indusium is short and small which covers 2/3 of the stipe from the cap and the cap is somewhat smooth. Hence, P. indusiatus is a new record for Assam as well as for North East India.
3.2. Phallus duplicatus
Bosc, Magazin der Gesellschaft Naturforschenden Freunde Berlin 5:86, t. 6:7 (1811) .
3.2.1. Material Examined
India (New record), North East India, Assam, Jorhat, HGWLS, 26°40′46.75′′N latitude and 94°20′29.78′′E longitude, 128m asl, decaying Bamboo stump (Comp.2, Comp.5, Table 1), G. Gogoi, 12.8.2012, Accession number: HGWLS/C2/001.
3.2.2. Habit and Distribution
The fetid gleba coating the cap of P. duplicatus attracts flies and other insects that consume it and help to disperse the spores as suggested by Roody, 2003 . P. duplicatus commonly called netted stinkhorn or wood witch is a species of fungus in the stinkhorn family. It is reported in Denmark, Norway, Spain, Sweden, United States , Brazil (Cortez et al. ), and China (Zhishu et al. ). It is documented from Tamil Nadu, India, by Soosairaj et al. .
The fungus is edible when still in the “egg” stage, before the fruit body is expanded as discussed by Roody . But there is no record of edibility in the study area and people may not know about edibility of this stinkhorn.
3.2.4. Dimension of the Fruiting Body
Fruiting body arising from a semiburied, roughly round egg (Figure 2(e)) which grows up to 2–2.5 cm broad, is brown in colour, and is attached to the substratum by a rhizomorph. The fruit body, with maturity, is ruptured and elongated to form a characteristic phallic shape. The fertile head is brown in colour and grows up to 3 cm tall, 3.5 cm broad and is not reticulated, aromatic, and coated with a fetid liquid-like material, the gleba. Fully grown fruit body (Figure 2(d)) is cylindrical and attains up to 14 cm tall. Stipe is up to 12 cm long, 2.5 cm broad and round, hollow, fragile, and straight or curved, surface being spongy-white, the apex tipped by a round to oval opening (5–10 mm broad), and base covered with a volva. A white, lacy, wavy margin, skirt-like veil hangs below the cap which extends around up to 8 cm from the cap but never reaches the ground. The pores of the veil are irregular or polygonal and lower pores are much larger than the upper ones. Basidiospores are cylindrical, hyaline, and smooth and measure 3-4 μm 1-2 μm (Figure 2(f)).
P. duplicatus is very close to P. merulinus and P. indusiatus but the skirt of P. duplicatus is short, meshes are mostly irregular and bigger in size, cap surface is somewhat smooth in texture, and unlike P. indusiatus it does not collapse due to its own body weight. In P. duplicatus the stipe is mostly curved, egg is brown, and veil is highly wavy with irregular meshes and does not collapse easily. But in P. merulinus the stipe is always straight, rarely curved, egg is white, and veil is not so wavy with hexagonal meshes and veil collapses within few hours. Moreover, sizes of the basidiospores are also differing among the three species. Till date, literature review revealed that there was no report of P. duplicatus from Assam as well as North East India. It is inferred from the study that the species P. duplicatus is the first report from Assam as well as North East India.
3.3. Phallus cinnabarinus
(W.S. Lee) Kreisel, Czech Mycology 48 (4):278 (1996) .
3.3.1. Material Examined
India, North East India (New record), Assam, Jorhat, HGWLS, 26°40′31.56′′N latitude and 94°20′40.93′′E longitude, 128 m asl, on soil of bamboo thicket (Comp.2-3, Table 1), G. Gogoi, 25.8.2013. Accession number: HGWLS/C2/005.
3.3.2. Habit and Distribution
P. cinnabarinus is attractive because of its orange coloured indusium, bell-shaped pitted-reticulated cap; this stinkhorn is recorded from Asia, Australia, Hawaii, Central America, South America, and Southern Mexico nearly worldwide . In India, P. cinnabarina is commonly found in Kuvempu University as discussed by Jamaluddin et al. , Brown et al. , and Swapna et al. 
3.3.3. Dimension of the Fruiting Body
Mature fruiting body (Figure 2(g)) is up to 17 cm high with a white stem that arises from a whitish to brownish, gelatinous, sac-like egg (2-3 cm across) with a laced, orange coloured veil (up to 14 cm in diameter) hanging up to 9 cm from the bottom edge of the cap; smell is unpleasant. Veil is porus, margin is wavy, semielastic, and pores are hexagonal. Cap size is 2.5 cm high and 3 cm broad, attached to stem at center by a white circlet surrounding the open pore (4 mm) at top of stem; lower margin of head is free. Stem is hollow, porus, has sponge-like structure, white, and slightly narrows towards the apex. Volva is very prominent at base of the stipe which is created from the rupturing of egg (Figure 2(h)). Basidiospores measure 3-4 1.5–2 μm, being long-elliptical to nearly cylindrical (Figure 2(i)).
This species of stinkhorn is not consumed in the study area.
This species differs from all other species reported, because of its orange coloured skirt. P. cinnabarinus is very close to P. indusiatus in all aspects except colour of fruit body and size of basidiospores. In India, a detailed study of different development stages, starting from egg to matured fruit of Dictyophora cinnabarinus, was done by Abrar et al. . Literature review revealed that there was no record of this species from North East India earlier and it is inferred that P. cinnabarinus is the first report for the region of North East India.
3.4. Phallus merulinus
(Berk.) Cooke, Greillea11 (58):57 (1882) .
3.4.1. Material Examined
India, North East India (New record), Assam, Jorhat, HGWLS, 26°40′47.94′′N latitude and 94°20′57.19′′E longitude, 118 m asl, on soil of bamboo thicket (Comp.1-2, Comp.5, Table-1), G. Gogoi, 13.6.2013. Accession number: HGWLS/C2/143.
3.4.2. Habit and Distribution
It grows solitary on road side soil and decomposing leaf litter. The white-veiled P. merulinus was described for the first time from Australia . In India, it is reported from Mangalore, Karnataka, Sridhar, and Karun  and from Kerela, Mohanan .
3.4.3. Dimension of the Fruiting Body
P. merulinus is commonly called basket stinkhorn mushroom is prolonged from single egg (Figure 2(k)), size 2.5 3 cm, semiburied soil or decomposing leaf litter and white, elastic volva attached to substrate with conspicuous 2-3 white rhizomorphs. The mature fruit body (Figure 2(j)) is 11 cm high. Cap is grey with size 2.6 2.9 cm, incurved towards the stipe, apex opens with an apical pore, sticky, gelatinous, surface smooth. Insects and ants attracted by this mushroom help in spore dispersal. Veil is white, semielastic, and 10 cm in diameter and margin wavy and hangs down to two-thirds of the stipe. The upper side pores of the veil are bigger than the lower side ones. Stipe is white, pitted, hollow, and tapering at apex with bulbous base, having size 9 2.5 cm. Basidiospores long-ellipsoid, 2.9–3.5 0.8–1.3 μm, subhyaline and smooth (Figure 2(l)).
It is unknown in the study area.
In contrast, the cap surface of P. indusiatus tends to have conspicuous reticulations that remain clearly visible under the gleba. Moreover, the indusium of P. merulinus is more delicate and shorter than that of P. indusiatus and is thus less likely to collapse under its own weight as reported by Reid . P. merulinus can be readily distinguished at all growth stages from other veiled stinkhorns reported. At maturity, it is characterized by the cap appearing smooth under the spore mass, and when old and the spores have worn away the cap is pale and granular-rugulose as per the report of Barrett and Stuckey . This species is very close to P. duplicatus. In both the species, the skirt is short and covers 2/3 of the stem from lower margin of the cap. In P. duplicatus, the veil is not so delicate, meshes size and shape of the veil are irregular and the lower meshes are bigger than the upper ones. But in P. merulinus the veil is very delicate, meshes size and shape are uniform, polygonal, and the upper meshes are bigger than the lower ones. Both the species are also differing in microstructures. Literature survey shows that there was no report of this species from North East India earlier. Hence, P. Merulinus is a new record from North East India.
3.5. Phallus atrovolvatus
Calonge et al., Boletin de la Sociedad Micologica de Madrid 29:5-8 (2005) .
3.5.1. Material Examined
India, North East India (New record), Assam, Jorhat, HGWLS, 26°39′48.51′′N latitude and 94°21′2.44′′E longitude, 120 m asl, on soil of bamboo thicket (Comp.2, Table 1), G. Gogoi, 8.8.2013. Accession number: HGWLS/C1/195.
3.5.2. Habit and Distribution
The fruit body is granular or cap is smooth, never reticulated, and the indusium hangs down from the lower margin of the cap about halfway the length of fruit body; volva or egg is always black in colour; stipe is white spongy. These are the distinguishing characteristics of the fungus which place the present species under P. atrovolvatus as suggested by Calonge . This species was first described from Costa Rica (Barrett and Stuckey ) and later reported from India (Das et al. ).
3.5.3. Dimension of the Fruiting Body
Oval shaped egg (Figure 2(n)), size 2 3 cm, exoperidium thin membranous, almost black, volva smooth. Odor is strong, sweet, and aromatic (never fetid). The stalk in a fully expanded fruit body (Figure 2(m)) measures 10–13 2–2.5 cm and is cylindrical, gradually broader towards base with an apical pore in the apex, hollow, spongy, white, with head 2–2.5 cm long and 2-3 cm broad at base. Indusium hangs 5-6 cm down below the cap (midway between cap and volva). It is white in colour and becomes yellowish white on drying. Basidiospores are cylindrical, smooth, hyaline, and measure 3–4.2 μm 1.1–1.7 μm (Figure 2(o)).
It is unknown in the study area.
P. merulinus and P. indusiatus both are very close to the present species but P. merulinus can only be separated from P. atrovolvatus by showing volva which is always white, never blackish or black as discussed by Calonge et al. , Das et al. , whereas P. indusiatus can easily be distinguished from the species in discussion by showing coarsely reticulate receptacle and typically longer indusium (Calonge ). Literature review revealed that there was no report of this fungus from North East India earlier. Hence, P. atrovolvatus is reported as a new record for North East India.
3.6. Mutinus bambusinus
(Zoll.) E. Fisch., Annales du Jardin Botanique de Buitenzorg 6:30, Tables 4 & 5, Figures 26–31 (1886) .
3.6.1. Material Examined
India, North East India (New record), Assam, Jorhat, HGWLS, 26°42′5.79′′N latitude and 94°21′19.82′′E longitude, 126 m asl, soil of bamboo thicket and decaying bamboo stump (Comp.1-Comp.5, Table 1), G. Gogoi, 14.7.2012. Accession number: HGWLS/C4/017.
3.6.2. Habit and Distribution
M. bambusinus is commonly known as the dog stinkhorn, the headless stinkhorn. The fruit body begins its development in an “egg” form, resembling somewhat a puffball partially submerged in the ground. As the fruit body matures, the egg ruptures and the spongy spore-bearing stalk emerges. The stalk is hollow, porus, and pinkish white in colour; its shape is cylindrical below, but it gradually tapers to a narrow apex with a small opening at the tip. The stalk is generally straight, sometimes slightly curved. Fruit bodies are attached to the substrate by whitish hyphal cord called “rhizomorph” that resembles plant roots. The upper half of the stalk is red in colour, covered with a foul-smelling slimy green spore mass called gleba. The fungus is listed in the red data list of Ukraine as discussed by Sarkina et al. . It is found in Costa Rica, Guinea, Japan, Republic of Korea, and Mexico . In India, the species was reported from Uttar Pradesh, Eastern Ghat, and West Bengal (Mahapatra et al. , Das et al. ).
It is unknown in the study area, although there are reports of the immature eggs of Mutinus species being consumed as suggested by Arora .
3.6.4. Dimension of the Fruiting Body
The matured fruit body (Figure 2(p)) is around 10–15 cm length grows from a egg (Figure 2(q)) and it is 1.5–3 cm 1-2 cm in size. Cap is red in colour, soft, and hollow and opens with an apical pore and cap is 5–8.5 cm long, 1-2 cm wide. Stipe is continuous with the cap, pink in colour, fragile, porus, and hollow. The spores are greenish-brown in color. The basidiospores (Figure 2(r)) are 4–7 2-3 μm, oblong-elliptical, smooth, and embedded in the gleba.
M. bambusinus is very close to M. elegans but the former has a distinct and abrupt demarcation between red coloured upper half (cap) of the fruit body and white to pinkish lower half (stipe), whereas the latter is orange-red in colour from top to bottom. Both the species are also different in size of basidiospores. Till date, three species of Mutinus have been reported from India, namely, M. bambusinus (Mahapatra et al.), M. caninus var. caninus (Huds.) Fr., and M. caninus var. albus Zeller (Dutta et al. ). There was no report of M. bambusinus from North East India earlier. So, this is a new report of M. bambusinus for North East region of India.
3.7. Clathrus delicates
Berkelly and Broome, Botanical Journal of the Linnean Society 14:77 (1875) .
3.7.1. Material Examined
India, North East India (New record), Assam, Jorhat, HGWLS, 26°40′37.90′′N latitude and 94°20′25.16′′E longitude, 118 m asl, leaf litter of bamboo (Comp.2, Table 1), G. Gogoi, 1.9.2013. Accession number: HGWLS/C2/224
3.7.2. Habit and Distribution
C. delicatus is commonly called Shuttlecock mushroom and it is one of a few white (rather than red or orange) species of Clathrus and it can be separated from the other white species on the basis of its arms, which are smooth, white, and flattened but with deep groove on the outer surface, more or less rounded in the inner portion, and reduced to a single tube. The species is being characterized by considerably smaller size, simplification of the tubular structure of the arms and presence of specialized “glebifers” (structures that produced the spore slime, located on the inner surfaces of the arms), and the bright yellow rhizomorphs attached to its base. This species was reported from Sri Lanka (Berkeley and Broome ) and India (Roy , Pradhan et al. , and Swapna et al. ).
It is unknown in the study area.
3.7.4. Dimension of the Fruit Body
Mature receptacle (Figure 2(t)) is 1.7 cm high, 1.2 cm broad, oval to egg-shaped, cage-like, latticed structure composed of slender arms that are joined near the base, white, 0.6 cm long stipe; meshes 8 in number more or less isodiametric above and vertically below. Basidiospores (Figure 2(s)) are 3.5–4 1.8–2.2 μm, elongated to cylindrical, hyaline, and smooth.
Literature review revealed that three species of Clathrus have been reported from India so far which include C. concellatus, C. pusillus, and C. delicatus. The present species C. delicatus was reported from West Bengal [54, 55] and from Karnataka  and C. cancellatus (synonym: C. ruber) was reported from West Bengal, Pradhan [55, 57]. Literature survey showed that there was not any report on C. delicatus from Assam as well as North East India. Hence, this species is the first record of occurrence, not only in Assam but also in Northeast region of India.
In the above study, it is concluded that there are seven species of stinkhorns, namely, Phallus indusiatus, Phallus duplicatus, Phallus cinnabarinus, Phallus merulinus, Phallus atrovolvatus, Mutinus bambusinus, and Clathrus delicatus, naturally occurring in the said sanctuary. All the seven species are reported to be a new record for Assam as well as North East India. Some fruit bodies of elucidated stinkhorn species were also collected from fringe villages of the sanctuary. M. bambusinus is distributed in the entire sanctuary with 75 fruit bodies. P. indusiatus and P. merulinus are distributed in three compartments with 40 and 6 fruit bodies, respectively. P. duplicatus and P. cinnabarinus are distributed in two compartments with 15 and 5 fruit bodies, respectively. P. atrovolvatus and C. delicatus are distributed only in one compartment only with 4 and 2 fruit bodies, respectively. Due to illicit felling, encroachment, heavy grazing, and browsing, the natural forests are being degraded and fragmented that resulted into a considerable decline of mycofloral diversity. Like other saprophagous fungi, stinkhorns also play a significant role in recycling nutrients and decomposing the dead organic matter specially plants and litter in soil which helps in the improvement of soil health . Rehabilitation of forest communities needs considerable duration as macrofungi prefers old microhabitats over new microhabitats, as discussed by Nordén and Appelqvist . The fungi are also key functional components of forest ecosystems . In order to preserve the macrofungal gene pool in situ, there is necessityto conserve old growth forests through sustainable approach which is endowed with ample quantity of diverse detritus suitable for fungal existence and perpetuation  and Hollongapar Gibbon Wildlife Sanctuary is also one of them.
Conflict of Interests
The authors declare that there is no conflict of interests regarding the publication of this paper.
The authors thank Assam State Forest Department particularly for providing required information about the Hollongapar Gibbon Wildlife Sanctuary.
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