Mycosphere 6 (2): 195–200(2015)
www.mycosphere.org
Copyright © 2015
ISSN 2077 7019
Article
Mycosphere
Online Edition
Doi 10.5943/mycosphere/6/2/9
New records and an updated checklist of lichenicolous fungi from
India
Joshi Y1, Upadhyay S1, Shukla S1, Nayaka S2 and Rawal RS3
Lichenology laboratory, Department of Botany, S.S.J. Campus, Kumaun University, Almora – 263601, Uttarakhand,
India dryogeshcalo@gmail.com
2
Lichenology laboratory, National Botanical Research Institute, Rana Pratap Marg, Lucknow – 226001, Uttar
Pradesh, India
3
G.B. Pant Institute of Himalayan Environment and Development, Kosi-Katarmal, Almora – 263643, Uttarakhand,
India
1
Joshi Y, Upadhyay S, Shukla S, Nayaka S, Rawal RS 2015 – New records and an updated checklist
of lichenicolous fungi from India. Mycosphere 6(2), 195–200, Doi 10.5943/mycosphere/6/2/9
Abstract
The present paper describes three new records of lichen inhabiting fungi belonging to the
genera Biatoropsis, Homostegia and Lichenodiplis, and also report new hosts for Homostegia
hertelii and range extensions of Lichenodiplis lecanorae, Pyrenidium actinellum and Sphinctrina
tubaeformis in India. An updated checklist of all lichenicolous fungi known so far from India is
also provided.
Key words – Biodiversity – checklist – distribution – mycobiota – parasymbiont
Introduction
Lichens are known to host a wide range of microorganisms including lichenicolous fungi
that are parasitic fungi living on lichens. They are most commonly specific to a given fungus as the
host, but also include a wide range of pathogens, saprotrophs and commensals. In the world so far
about 1800 species of lichenicolous fungi have been identified and an occurrence of more than
3000 is being estimated (Lawrey & Diederich 2011). In India, lichenicolous fungi were hardly
studied by lichenologists and the literature is scattered and scanty. Recently, Zhurbenko (2013)
published the first list of lichenicolous fungi for India with 42 species including some taxa
identified only up to generic level. However, few species of lichenicolous fungi reported earlier
from India were missing in Zhurbenko’s (2013) list, while, few are discovered recently. The list of
missing fungi includes - Arthonia diorygmae S. Joshi & Upreti (Joshi et al. 2013), Carbonea
vitellinaria (Nyl.) Hertel (Awasthi 1991), Sphinctrina anglica Nyl. and Sphinctrina tubaeformis A.
Massal. (Pant & Awasthi 1989). Recently, Joseph and Sinha (unpbl.) reported two species of
Melaspilea (M. amarkantakensis S. Joseph & G.P. Sinha and M. insitiva Stirt.) as lichenicolous
fungi from India. In the present communication, we are reporting six interesting species of the
lichenicolous fungi based on fresh collections from Kumaun Himalaya and herbarium specimen
lodged at National Botanical Research Institute (LWG). Out of six species, three are new to India,
while five are new to Uttarakhand (including two new records for India), and described in brief
along with their host species and distribution within and outside India. After including the species
missed out by Zhurbenko (2013) along with recent records, the total tally of lichenicolous fungi in
Submitted 2 November 2014, Accepted 25 February 2015, Published online 30 March 2015
Corresponding Author: Yogesh Joshi – e-mail – dryogeshcalo@gmail.com
195
India raises up to 51 (Table 1). This updated checklist would act as baseline information for further
studies on lichenicolous fungi of India.
Materials & Methods
The study is based on 11 samples collected from Kumaun Himalaya during 2013-14 and
one herbarium specimen deposited at LWG. The external morphology of the samples was
examined under stereozoom microscope (OLYMPUS SZ2-ILST). The anatomical studies were
carried out using hand cut sections using CX21iLEDFS1 microscope. Studied specimens are
deposited in the herbarium of Kumaun University, Almora (ALM) and CSIR-National Botanical
Research Institute, Lucknow (LWG).
Results
Biatoropsis usnearum Räsänen, Ann. Bot. Soc. Zool.-Bot. Fenn. “Vanamo” 5: 8 (1934).
Basidiomata club shaped, flat to convex, yellowish to brownish, constricted at base or
subsessile, rarely with prominent short stalk. Hymenium hyaline, basidia clavate, up to 3 septate,
25–30 × 3–5 µm. Basidiospores subglobose to ellipsoidal, 4–7 × 3.5–7.5 µm.
Known distribution – Cosmopolitan, known from all continents except Antarctica
(Diederich 2004a). New to India.
Material examined – INDIA, Tamil Nadu, Kanya Kumari, Upper Kodayar, alt. 1050 m, on
thallus of corticolous Usnea austroindica, May 2011, Ravichandran, s.n. (LWG).
Homostegia hertelii D. Hawksw., V. Atienza & M.S. Cole, Biblioth. Lichenol. 88: 189 (2004).
Stroma arising on the surface of the host thallus, black, matt to slightly shiny, orbicular to
irregular. Perithecioid locules arising deep in the stroma. Hamathecium well developed. Asci
elongate to clavate, 8 spored. Ascospores 3 septate, olivaceous brown, the tips of the end cells often
somewhat paler to subhyaline, smooth walled, 20–27.5 × 7–13.5 µm.
Known distribution – U.S.A. (Hawksworth et al. 2004). New to Asia and India.
Material examined – INDIA, Uttarakhand, Almora district, Jhakar Saim Forest, on thallus
of Flavoparmelia caperata and Punctelia rudecta colonizing Quercus tree, 06 July 2014, M.
Tripathi, K. Chandra & S. Upadhyay, s.n. (ALM); Dol Ashram, on thallus of Punctelia rudecta
colonizing Quercus tree, 15 March 2014, M. Tripathi & party, s.n. (ALM).
Lichenodiplis lecanorae (Vouaux) Dyko & D. Hawksw., Lichenologist 11(1): 52 (1979).
Pycnidia present, arising singly, dark brown, subglobose, 50–120 µm in diameter.
Conidiophores absent, conidiogenous cells hyaline to pale brown, lageniform to subcylindrical,
5.5–12 × 2–3 µm. Conidia pale brown, 1 septate, elongate to ellipsoid, 4–7.5 × 2–3 µm.
Known distribution – Europe, North and South America, possibly cosmopolitan (Diederich
2004b). Previously the species was reported by Zhurbenko (2013) from Jammu & Kashmir, where
it was colonizing on apothecia and thallus of Caloplaca cerina and Xanthoria candelaria
respectively. It is new to Uttarakhand and found growing on apothecial discs of Lecanora species.
Material examined – INDIA, Uttarakhand, Almora district, G.B. Pant Institute of
Himalayan Environment and Development, on apothecia of Lecanora sp. colonizing bark of
Ligustrum nepalense, 16-18 March 2014, G. Bhakuni, s.n. (ALM).
Lichenodiplis lichenicola Dyko & D. Hawksw., Lichenologist 11(1): 56 (1979).
Pycnidia present, arising singly, dark brown, subglobose, 50–60 µm in diameter.
Conidiophores absent, conidiogenous cells hyaline to pale brown, lageniform to subcylindrical, 5–
10 × 2–3 µm. Conidia pale brown, 1 septate, elongate to ellipsoid, 9–12 × 4–5 µm.
Known distribution – Alaska (Zhurbenko et al. 1995), British Isles (Coppins & Coppins
1996), Norway (Hawksworth & Dyko 1979), Spain (Calatayud et al. 1995). New to Asia and India.
196
Table 1 Updated checklist of lichenicolous fungi from India along with their host lichens and distribution
S. No.
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
Lichenicolous fungi
Abrothallus peyritschii (Stein) I. Kotte
Arthonia diorygmae S. Joshi & Upreti
A. molendoi (Heufl. ex Frauenf.) R. Sant.
Biatoropsis usnearum Räsänen
Carbonea vitellinaria (Nyl.) Hertel
Cercidospora macrospora (Uloth) Hafellner & Nav.-Ros.
C. melanophthalmae Nav.-Ros., Calat. & Hafellner
C. xanthoriae (Wedd.) R. Sant.
Cercidospora sp.
Cladosporium licheniphilum Heuchert & U. Braun
Corticifraga peltigerae (Fuckel) D. Hawksw. & R. Sant.
12.
13.
Endococcus incrassatus Etayo & Breuss
E. rugulosus (Borrer ex Leight.) Nyl.
14.
Homostegia hertelii D. Hawksw., V. Atienza & M.S. Cole
15.
16.
H. piggotii (Berk. & Broome) P. Karst.
Intralichen christiansenii (D. Hawksw.) D. Hawksw. &
M.S. Cole
Lichenoconium usneae (Anzi) D. Hawksw.
L. xanthoriae M.S. Christ.
Lichenodiplis lecanorae (Vouaux) Dyko & D. Hawksw.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
L. lichenicola Dyko & D. Hawksw.
Lichenopeltella swaminathaniana Harih., Mibey & D.
Hawksw.
Lichenostigma alpinum (R. Sant., Alstrup & D. Hawksw.)
Ertz & Diederich
L. cosmopolites Hafellner & Calat.
L. cf. elongatum Nav.-Ros. & Hafellner
L. subgen. Lichenogramma sp.
Marchandiomyces corallinus (Roberge) Diederich & D.
Hawksw.
Melaspilea amarkantakensis S. Joseph & G.P. Sinha
M. insitiva Stirt.
Host
Vulpicida pinastri
Diorygma junghuhnii
Xanthoria elegans
Usnea austroindica
Candelaria vitellina
Lecanora sp.
Rhizoplaca melanophthalma
Xanthoria elegans
Lecanora sp.
Xanthoria Candelaria
Peltigera
elisabethae
&
ponojensis
Endocarpon pusillum
Rhizocarpon disporum
Aspicilia sp.
Flavoparmelia
caperata
Punctelia rudecta
Parmelia sp.
Candelariella aurella
P.
Distribution
Himachal Pradesh
Tamil Nadu
Jammu & Kashmir
Tamil Nadu
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Reference(s)
Alstrup & Ahti (2007)
Joshi et al. (2013)
Zhurbenko (2013)
This manuscript
Awasthi (1991)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
&
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Uttarakhand
Zhurbenko (2013)
Triebel (1989)
Zhurbenko (2013)
This manuscript
Uttarakhand
Jammu & Kashmir
Alstrup & Ahti (2007)
Zhurbenko (2013)
Flavoparmelia caperata
Melanelixia subargentifera
Caloplaca cerina & Xanthoria
candelaria
Lecanora sp.
Rinodina sp.
Porina sp.
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Uttarakhand
Uttarakhand
Tamil Nadu
This manuscript
This manuscript
Hariharan et al. (1996)
Pertusaria albescens
Jammu & Kashmir
Zhurbenko (2013)
Xanthoparmelia stenophylla
Lecanora sp. & Lobothallia
praeradiosa
Seirophora contortuplicata
Physcia aipolia & Xanthoria
candelaria
Pertusaria amarkantakana
Pertusaria leioplaca
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Zhurbenko (2013)
Zhurbenko
(2013)
Zhurbenko (2013)
Zhurbenko (2013)
Madhya Pradesh
West Bengal
Joseph & Sinha (unpbl.)
Joseph & Sinha (unpbl.)
197
S. No.
29.
30.
31.
Lichenicolous fungi
Monodictys epilepraria Kukwa & Diederich
Muellerella erratica (A. Massal.) Hafellner & Volk. John
M. pygmaea (Körb.) D. Hawksw.
Host
Lepraria sp.
Lecidea lapicida & Lecanora sp.
Xanthoria elegans & Acarospora
sp.
Peltigera elisabethae & P. scabrosa
Heterodermia leucomelos
Distribution
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Reference(s)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
32.
33.
Nectriopsis lecanodes (Ces.) Diederich & Schroers
Opegrapha foreaui (Moreau) Hafellner & R. Sant.
Jammu & Kashmir
Tamil Nadu
Xanthoria elegans
Parmotrema perforatum
Xanthoria elegans
Physcia dubia
Punctelia borreri
Peltigera
elisabethae
praetextata
Punctelia rudecta
Lecanora argopholis
Candelariella sp.
Ochrolechia trochophora
Lecanora muralis
Jammu & Kashmir
Tamil Nadu
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Zhurbenko (2013)
Coppins & Kondratyuk
(1998)
Zhurbenko (2013)
Moreau (1951)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
34.
35.
36.
37.
38.
39.
Phoma sp.
Phyllosticta galligena Moreau
Polycoccum clauzadei Nav.-Ros. & Cl. Roux.
P. pulvinatum (Eitner) R. Sant.
Pronectria subimperspicua (Speg.) Lowen
Pyrenidium actinellum Nyl.
40.
41.
42.
43.
44.
Rosellinula frustulosae (Vouaux) R. Sant..
Sarcogyne sphaerospora J. Steiner
Skyttea fusispora Sherwood, D. Hawksw. & Coppins
Sphaeropezia cf. lecanorae (Diederich & G. Marson)
Baloch & Wedin
Sphinctrina anglica Nyl.
Uttarakhand
Jammu & Kashmir
Jammu & Kashmir
Assam
Jammu & Kashmir
This manuscript
Zhurbenko (2013)
Zhurbenko (2013)
Sherwood et al. (1981)
Zhurbenko (2013)
Pertusaria sp.
Tamil Nadu & Uttar Pradesh
S. tubaeformis A. Massal.
Pertusaria sp.
Stigmidium gyrophorarum (Arnold) D. Hawksw.
S. pumilum (Lettau) Matzer & Hafellner
S. tabacinae (Arnold) Triebel
Vouauxiella lichenicola (Linds.) Petr. & Syd.
Zwackhiomyces coepulonus (Norman) Grube & R. Sant.
Z. cf. kiszkianus D. Hawksw. & Miadl.
Umbilicaria vellea
Phaeophyscia ciliata
Toninia tristis
Lecanora sp.
Xanthoria elegans
Peltigera elisabethae
Assam, Manipur,
Nadu
Uttarakhand
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Jammu & Kashmir
Pant & Awasthi (1989)
and Awasthi & Singh
(1975)
Pant & Awasthi (1989)
45.
46.
47.
48.
49.
50.
51.
&
P.
Tamil
This manuscript
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Zhurbenko (2013)
Material examined – INDIA, Uttarakhand, Champawat district, Shivalaya temple, on apothecia of Rinodina sp. colonizing rocks, 17 July 2014,
K. Chandra, s.n. (ALM).
198
Pyrenidium actinellum Nyl., Flora (Regensburg) 48: 210 (1865).
Gall forming fungi on host thalli. Ascomata perithecioid pseudothecia. Ascomata wall
entirely brown to dark brown. Paraphysoids filiform, hyaline, septate. Periphyses hyaline, green
pigmented at ostiolar region. Asci cylindrical to clavate, 4-8 spored. Ascospores brown with the
tips of the end cells often pale brown to subhyaline, ellipsoid to broadly fusiform, 3 septate, rarely 2
or 4, 22.5–25 × 7.5–10 µm.
Known distribution – Cosmopolitan (Navarro-Rosinés & Roux 2007). Previously
Zhurbenko (2013) reported the species from Jammu & Kashmir, where it was colonizing thallus of
Peltigera elisabethae and P. praetextata. It is new to Uttarakhand and found growing on thallus of
Punctelia rudecta, thus extending its range distribution as well as host preference.
Material examined – INDIA, Uttarakhand, Almora district, Syahi Devi Forest, on thallus of
Punctelia rudecta colonizing Quercus tree, 27 July 2014, S. Upadhyay & N. Rana, s.n. (ALM).
Sphinctrina tubaeformis A. Massal., Memor. Lich.: 155 (1853).
Apothecia immersed in the host thallus. Stalk absent to short. Capitulum spherical, shiny
black or dark brown. Asci cylindrical. Ascospores ellipsoid with pointed ends, non septate, (9–)12–
15.5(–20) × 6–8(–9) µm.
Known distribution – Europe, Asia, Africa, North and Central America (Tibell 2004).
Previously Pant & Awasthi (1989) and Singh (1981) reported the species from Assam, Manipur
and Tamil Nadu states of India, where it was colonizing thallus of Pertusaria. It is new to
Uttarakhand and found growing on thallus of Pertusaria sp., thus extending its range distribution
within India.
Material examined – INDIA, Uttarakhand, Almora district, Jhakar Saim Forest, on thallus
of Pertusaria colonizing Quercus tree, 06 July 2014, M. Tripathi, K. Chandra & S. Upadhyay, s.n.
(ALM); Syahi Devi Forest, on thallus of Pertusaria colonizing Quercus tree, 27 July 2014, S.
Upadhyay & N. Rana, s.n. (ALM).
Discussion
The present study raises the tally of lichenicolous fungi up to 51 in India and opens a new
horizon to study this group since there are several possibilities of finding new species and new
records of lichenicolous fungi from India, because a lot of work has been conducted on lichens of
India, but this group has remained untouched. Besides this, this group need to be explored out
extensively for their host preference, since they are generally named after the host lichen on which
they colonize, but there are some species that colonizes various lichens. For example, Homostegia
hertelii and Pyrenidium actinellum were previously reported by earlier workers colonizing
Flavoparmelia spp. and Peltigera spp. respectively, but present study extends their host range to
Punctelia rudecta.
Acknowledgements
One of the authors (YJ) would like to thank University Grants Commission [41488/2012(SR)] and Scientific and Engineering Research Board [SB/FT/LS-313/2012] for financial
assistance, while another author (SN) would like to thank Dr. Paul Diederich for identifying
Biatoropsis usnearum. Thanks are also extended to Director, G.B. Pant Institute of Himalayan
Environment and Development for allowing us to collect lichen samples from the institute.
References
Alstrup V, Ahti T. 2007 – New reports of lichenicolous fungi, mainly from Finland and Russia.
Karstenia 47, 1–4.
Awasthi DD, Singh KP. 1975 – Additions to the lichen flora of India – III. Geophytology 5, 110–
112.
199
Awasthi DD. 1991 – A key to microlichens of India, Nepal and Srilanka. Bibliotheca Lichenologica
40, 1–337.
Calatayud V, Atienza V, Barreno E. 1995 – Lichenicolous fungi from the Iberian Peninsula and the
Canary Islands. Mycotaxon 55, 363–382.
Coppins BJ, Coppins AM. 1996 – New, rare and interesting British lichen and lichenicolous fungus
records. Bulletin British Lichen Society 78, 60.
Coppins BJ, Kondratyuk SY. 1998 – Opegrapha trassii sp. nov., a new lichenicolous fungus on
Heterodermia. Folia Cryptogamica Estonica 32, 9–14.
Diederich P. 2004a – Biatoropsis Räsänen (1934). In: Lichen Flora of the Greater Sonoran Desert
Region. Vol. 2. (eds TH Nash III, BD Ryan, P Diederich, C Gried, F Bungartz). Lichens
Unlimited, Arizona State University, Tempe, Arizona, pp. 633.
Diederich P. 2004b – Lichenodiplis Dyko & D. Hawksw. (1979). In: Lichen Flora of the Greater
Sonoran Desert Region. Vol. 2. (eds TH Nash III, BD Ryan, P Diederich, C Gried, F
Bungartz). Lichens Unlimited, Arizona State University, Tempe, Arizona, pp. 661–663.
Hariharan GN, Mibey RK, Hawksworth DL. 1996 – A new species of Lichenopeltella on Porina in
India. Lichenologist 28, 294–296.
Hawksworth DL, Dyko BJ. 1979 – Lichenodiplis and Vouauxiomyces: two new genera of
lichenicolous coelomycetes. Lichenologist 11, 51–61.
Hawksworth DL, Atienza V, Cole MS. 2004 – Lichenicolous species of Homostegia
(Dothideomycetes), with the description of H. hertelii sp. nov., a new fungus on
Flavoparmelia species. Bibliotheca Lichenologica 88, 187–194.
Joshi S, Upreti DK, Nayaka S. 2013 – A new lichenicolous Arthonia species (Arthoniaceae) on
Diorygma from India. Lichenologist 45, 323–327.
Lawrey JD, Diederich P. 2011 – Lichenicolous fungi – worldwide checklist, including isolated
cultures and sequences available. http://www.lichenicolous.net (accessed 13 September
2014).
Moreau F. 1951 – Un champignon lichenicole cecidogene, Phyllosticta galligena, sp. nov. Bulletin
de la Société Botanique de France 98, 100–102.
Navarro–Rosinés P, Roux Cl. 2007 – Pyrenidium Nyl. (1865). In: Lichen Flora of the Greater
Sonoran Desert Region. Vol. 2. (eds TH Nash III, BD Ryan, P Diederich, C Gried, F
Bungartz). Lichens Unlimited, Arizona State University, Tempe, Arizona, pp. 404–405.
Nylander W. 1865 – Novitatiae quaedum lichenum Europaeorum variorum tribuun. Flora 48,
209–213.
Pant G, Awasthi DD. 1989 – Caliciales from India and Nepal. Biovigyanam 15, 3–27.
Sherwood MA, Hawksworth DL, Coppins BJ. 1981 – Skyttea, a new genus of odontotremoid
lichenicolous fungi. Transactions of the British Mycological Society 75, 479–490.
Singh KP. 1981 – Microlichens from Manipur, India. Geophytology 11, 242–256.
Tibell L. 2004 – Sphinctrina Fr. (1825). In: Lichen Flora of the Greater Sonoran Desert Region.
Vol. 2. (eds TH Nash III, BD Ryan, P Diederich, C Gried, F Bungartz). Lichens Unlimited,
Arizona State University, Tempe, Arizona, pp. 699–701.
Triebel D. 1989 – Lecideicole Ascomyceten. Eine Revision der obligat lichenicolen Ascomyceten
auflecideoiden Flechten. Bibliotheca Lichenologica 35, 1–278.
Zhurbenko MP, Santesson R, Walker DA, Auerbach NA, Lewis B. 1995 – New and interesting
lichenicolous fungi and lichens from Alaska. Evansia 12, 92–97.
Zhurbenko MP. 2013 – A first list of lichenicolous fungi from India. Mycobiota 3, 19–34.
200