Graphidaceae, the largest crustose family within Ostropales comprising more than 2000 species (Lücking et al. Reference Lücking, Hodkinson and Leavitt2016), is widely distributed in tropical and subtropical regions of the world. Since 2002, the taxonomy of the family has undergone major changes and, as a result, a large number of new genera have been established and several old genera resurrected based mainly on molecular studies (Staiger et al. Reference Staiger, Kalb and Grube2006; Rivas Plata et al. Reference Rivas Plata, Lumbsch and Lücking2012, Reference Rivas Plata, Parnmen, Staiger, Mangold, Frisch, Weerakoon, Hernández, Cáceres, Kalb and Sipman2013; Lücking et al. Reference Lücking, Tehler, Bungartz and Lumbsch2013; Lumbsch et al. Reference Lumbsch, Kraichak, Parnmen, Rivas Plata, Aptroot, Cáceres, Ertz, Feuerstein, Mercado Díaz and Staiger2014). Graphidaceae is now well circumscribed in terms of generic classification and species delimitation. In earlier publications, Singh & Swarnlatha (Reference Singh and Swarnlatha2009) and Singh & Singh (Reference Singh and Singh2017a) made several new combinations for Indian taxa. In the present paper a further five new combinations are proposed which are the result of our continuing study on Indian graphidioid Graphidaceae and examination of more type specimens preserved at Agarkar Research Institute, Pune, India (AMH), Botanical Survey of India, Allahabad (BSA), the Natural History Museum, London (BM), Conservatorie et Jardin botaniques de la Ville de Genève (G), Finnish Museum of Natural History, University of Helsinki, Finland (H-NYL), and National Botanical Research Institute, Lucknow (LWG). The new combinations include: Carbacanthographis garoana, Diorygma occultum, Fissurina leucocarpoides, F. parvicarpa and Pallidogramme canarensis. In addition, seven names are synonymized viz. Diorygma indicum under D. aeolum, Fissurina shivamoggensis under F. leucocarpoides, Graphis andamanica, G. longissima and G. sitapurensis to G. flavovirens, G. kollaimalaiensis under G nigrocarpa, and Phaeographina nakanishii under Schistophoron tenue.
Type specimens deposited in AMH, BM, BSA, G, H and LWG were examined morphologically, anatomically and chemically. Morphological characters of thalli (reproductive structures, colour, size and shape) were observed using a Nikon SMZ 1500 stereomicroscope. Thin hand-cut sections of thalli and ascomata were examined, mounted in an aqueous solution of KOH. All anatomical measurements were made in water mounts and examined using a Nikon Eclipse 50i compound microscope. Ascospores were mounted in water for measurements and stained with Lugol's solution to check the amyloid reaction. Secondary metabolites were identified by thin-layer chromatography (TLC) using solvent A (180 toluene: 45 dioxane: 5 acetic acid), following Orange et al. (Reference Orange, James and White2001).
New Combinations
Carbacanthographis garoana (Nagarkar & Patw.) Pushpi Singh & Kr. P. Singh comb. nov.
MycoBank No.: MB 830948
Graphis garoana Nagarkar & Patw., Biovigyanam 8, 126 (1982); type: India, Meghalaya, Garo Hills, Darugiri Reserve Forests, 6 December 1978, M. B. Nagarkar 78.387 (AMH!—holotype).
(Fig. 1A)
Fig. 1. Habitus of studied species (holotypes). A, Carbacanthographis garoana; B, Diorygma occultum; C, Fissurina leucocarpoides; D, Fissurina shivamoggensis; E, Fissurina parvicarpa; F, Pallidogramme canarensis. Scales = 1 mm. In colour online.
Thallus corticolous, greyish brown to yellowish brown, continuous, smooth; cortex indistinct.
Ascomata lirellate, conspicuous, emergent, simple to sparsely branched, covered with lateral thalline margin, 1–2 mm long, 0.2–0.3 mm wide; disc slit-like, covered laterally with whitish pruina and coated with warty periphysoids; labia entire; exciple laterally carbonized; hymenium hyaline, clear, 85–100 μm high; asci 8-spored; ascospores colourless, transversely 10–12-septate, 35–74 × 7.0–8.5 μm, I+ pale blue; norstictic and salazinic acids present.
Notes
Examination of the type material of Graphis garoana (AMH!) revealed that it belongs to the genus Carbacanthographis. Carbacanthographis indica B. O. Sharma & Khadilkar, a species from Meghalaya, India appears to be somewhat close to C. garoana in the laterally carbonized exciple and transversely septate ascospores. However, C. garoana is easily distinguished by its simple, emergent, flexuous, 3–8 mm long lirellae and in the presence of norstictic acid in addition to salazinic acid in the thallus (Nagarkar & Patwardhan Reference Nagarkar and Patwardhan1982). It also resembles C. induta (Müll. Arg.) Lücking in the laterally carbonized exciple and transversely septate ascospores but the latter species differs in its larger ascospores and the presence of stictic acid (Nakanishi et al. Reference Nakanishi, Kashiwadani, Futagami and Moon2010).
Diorygma occultum (Adaw. & Makhija) Pushpi Singh & Kr. P. Singh comb. nov.
MycoBank No.: MB 830950
Platythecium occultum Adaw. & Makhija, Mycotaxon 92, 392 (2005); type: India, Tamil Nadu, Chitteri, 14 November 1985, M. B. Nagarkar & P. G. Patwardhan 85.1446 (AMH!—holotype)
(Fig. 1B)
Thallus corticolous, crustose, epiphloeodal, greyish white, cracked, ecorticate.
Ascomata lirellate, immersed, simple to branched, covered by lateral thalline margin; disc narrow to exposed, blackish, faintly whitish pruinose; exciple uncarbonized, covered by lateral thalline margin; hymenium clear, I−; asci 6–8-spored; ascospores colourless, transversely 5–7-septate, 18–28 × 7–8 μm, amyloid, I+ blue; lichexanthone, norstictic and constictic acids (see under notes).
Notes
Examination of the type material of Platythecium occultum (AMH!) revealed that it belongs to the genus Diorygma, based on the Diorygma-like thallus and ascomata. The occurrence of both norstictic and constictic acids is exceptional and rarely found in the Graphidaceae. However, both substances were observed in TLC as mentioned in the protologue. The same rare condition was also observed by Kalb et al. (Reference Kalb, Staiger and Elix2004) for Diorygma hieroglyphicum (Pers.) Staiger & Kalb and a small number of other species in their monograph. Externally it is very similar to Diorygma hieroglyphicum, which has single-spored asci and larger ascospores (95–150(–170) × 30–45 μm; fide Kalb et al. Reference Kalb, Staiger and Elix2004). In ascospore characteristics, it closely resembles D. minisporum Kalb et al., although this contains hypostictic, hypoconstictic, stictic and constictic acids.
Fissurina leucocarpoides (Nyl.) Pushpi Singh & Kr. P. Singh comb. nov.
MycoBank No.: MB 830952
Graphis leucocarpoides Nyl., Bull. Soc. Linn. Normandie, sér. 2, 7, 176 (1873).—Graphina leucocarpoides (Nyl.) Zahlbr., Cat. Lich. Univ. 2, 412 (1923); type: India, Andaman Islands, 1867, S. W. Kurz s. n. H-NYL No. 7692 (H!—lectotype).
Fissurina shivamoggensis Pushpi Singh & Kr. P. Singh, NeBIO 8, 21 (2017); type: India, Karnataka, Shivamogga District, Sagar-Shivamogga road, Chithrate forest, 17 December 2014, K. P. Singh 9743 (BSA!—holotype).
Thallus corticolous, pale fawn or yellowish brown, smooth, glossy, effuse, continuous; corticate.
Ascomata lirellate, numerous, immersed, conspicuous, sparsely branched, closely scattered, almost straight to curved, 2–12 mm long and 0.4–0.6 mm wide; labia striate, divergent; disc exposed, whitish pruinose; exciple uncarbonized; hymenium clear; asci 1-spored; ascospores colourless, oblong, densely muriform, 100–150(–160) × 38–55 μm, with amyloid halo, 11–23 μm thick; lichen substances absent.
Notes
Examination of the type material of Graphis leucocarpoides (H!) revealed that it belongs to the genus Fissurina. Morphologically, it closely resembles Fissurina niveoalba Poengs. & Kalb, which has 8-spored asci and smaller, 17–25 μm long ascospores (Poengsungnoen et al. Reference Poengsungnoen, Manoch, Mongkolsuk and Kalb2014). In ascospore character, it also closely resembles F. submonospora B. O. Sharma et al. which has short emergent (0.5–1.0 mm long) lirellae with a slit-like disc; the labia are entire and the exciple convergent and entirely covered by a thalline margin (Sharma et al. Reference Sharma, Khadilkar and Makhija2012).
Singh & Singh (Reference Singh and Singh2017b) described Fissurina shivamoggensis (Fig. 1D) from Karnataka, India. While attempting to resolve the status of taxa reported under the name Graphina from India, we concluded that F. shivamoggensis is conspecific with F. leucocarpoides. The former is therefore synonymized here.
Fissurina parvicarpa (Makhija & Adaw.) Pushpi Singh & Kr. P. Singh comb. nov.
MycoBank No.: MB 830954
Platythecium parvicarpum Makhija & Adaw., Mycotaxon 91, 351 (2005); type: India, Andaman Islands, South Andaman, Baratang Island, Nilambur, 20 February 1985, P. G. Patwardhan 85.368 (AMH!— holotype).
(Fig. 1E)
Thallus corticolous, pale brown, smooth, glossy.
Ascomata lirellate, immersed, short, simple, blackish; disc narrow to open, dark brown, epruinose; exciple uncarbonized; hymenium clear; periphysoids indistinct; epihymenium pale brown; asci 8-spored; ascospores colourless, transversely 3-septate, 12–16 × 5.0–5.8 μm, with a thin halo, faintly I+ blue; lichen substances absent.
Notes
Examination of the type material of Platythecium occultum (AMH!) revealed that it belongs to the genus Fissurina. It closely resembles F. andamanensis B. O. Sharma et al., F. khasiana Makhija & Adaw. and F. humilis (Vain.) Staiger with its 3-septate amyloid ascospores. Fissurina andamanensis is distinguished by its fissurine lirellae, large, 20–27 μm long ascospores (Sharma et al. Reference Sharma, Khadilkar and Makhija2012) and the presence of salazinic acid, while F. khasiana has large, 16–19 × 8–10 μm ascospores and contains stictic and constictic acids. Fissurina humilis has a laterally carbonized exciple and large, 14–25 × 7–9 μm ascospores.
Pallidogramme canarensis (Patw. & C. R. Kulk.) Pushpi Singh & Kr. P. Singh comb. nov.
MycoBank No.: MB 830956
Phaeographina canarensis Patw. & C. R. Kulk., Indian J. Bot. 2(2), 135 (1979); type: India, Karnataka, Agumbe to Udupi road, Hebri, A. V. Prabhu & M. B. Nagarkar 74.3050 (AMH!— holotype).
(Fig. 1F)
Thallus corticolous, brownish, glossy, continuous, wrinkled to warty, corticate.
Ascomata lirelliform, prominent, simple to sparsely branched, 5–8 mm long, 0.4–0.5 mm wide, obtuse at the ends; disc slit-like; labia convergent, striate, blackish; exciple uncarbonized, pale brown to brown, covered by lateral thalline margin encrusted with numerous crystals; hymenium hyaline, clear, I−; epihymenium dark brown; asci 4(–8)-spored; ascospores brown, oblong, ellipsoid, muriform, (40–)60–118 × (12–)20–32 μm, I+ red; norstictic acid present.
Notes
Examination of the type material of Phaeographina canarensis (AMH!) revealed that it belongs to the genus Pallidogramme. It closely resembles P. chlorocarpoides (Nyl.) Staiger et al. which has an inspersed hymenium and stictic acid complex chemistry. In chemistry, it closely resembles P. parvicarpum (Sharma & Khadilkar) Lücking, which has an inspersed hymenium and 1–2-spored asci.
Further New Synonyms
Diorygma aeolum (Stirt.) Pushpi Singh & Kr. P. Singh
Lichenologist 49, 527 (2017).—Graphis aeola Stirt., Proc. Roy. Phil. Soc. Glasgow 11, 316 (1879) [1878]; type: India, Tamilnadu, ‘Nelghiri’ (Nilgiri hills), G. Watt, s.n. (BM 0010973831!—lectotype).
Diorygma indicum (Müll. Arg.) S. Joseph & G. P. Sinha, Indian J. For. Add. Ser. VI, 155 (2018).—Enterodictyon indicum Müll. Arg., J. Linn. Soc., Bot. 29, 230 (1892); type: India, Manipur, 1881–1882, G. Watt s. n. (G!—lectotype).
Notes
Müller-Argoviensis (Reference Müller-Argoviensis1892) described Enterodictyon indicum as a new species from Manipur, India. Joseph et al. (Reference Joseph, Sinha and Ramchandran2018) transferred it to the genus Diorygma as D. indicum. After a critical study it was found that the latter agrees well with D. aeolum, in morphology, anatomy and chemistry. Diorygma indicum is, therefore, synonymized here.
Graphis flavovirens Makhija & Adaw.
Mycotaxon 91, 374 (2005); type: India, Andaman Islands, Middle Andaman, Parlobjig Island, 23 December 1985, M. B. Nagarkar & P. K. Sethy 85.2264 (AMH!—holotype).
Graphis sitapurensis Makhija & Adaw., Mycotaxon 91, 378 (2005); type: India, Andaman Islands, North Andaman, Diglipur Range, Sitapur, in moist deciduous forest, 2 January 1986, P. K. Sethy & P. G. Patwardhan 86.145 (AMH!—holotype).
Graphis longissima Makhija & Adaw., Mycotaxon 91, 377 (2005); type: India, Andaman Islands, North Andaman, Pathar Thikri, Tugapur Range, deciduous forest, 29 December 1985, P. K. Sethy & P. G. Patwardhan 85.2715 (AMH!—holotype).
Graphis andamanica Swarnal., Phytotaxa 313, 144–146 (2017); type: India, Andaman Islands, South Andaman, Wright Myo, alt. c. 30 m, 18 April 1961, A. Singh 88290 (LWG—holotype).
(Fig. 2A)
Fig. 2. Habitus of studied species (holotypes). A, Graphis flavovirens; B, G. longissima; C, G. sitapurensis; D, G. nigrocarpa; E, G. kollaimalaiensis; F, Schistophoron tenue (holotype of Phaeographina nakanishii). Scales = 1 mm. In colour online.
Thallus corticolous, yellowish brown to whitish grey.
Ascomata lirellate, erumpent; exciple completely carbonized with entire labia; hymenium inspersed; asci 2–8-spored; ascospores colourless, transversely 10–18-septate, 48–60 × 7–10 μm, amyloid; stictic and constictic acids present.
Notes
Makhija & Adawadkar (Reference Makhija and Adawadkar2005) simultaneously described three species, namely Graphis flavovirens, G. longissima (Fig. 2B) and G. sitapurensis. (Fig. 2C), from the Andaman Islands (AMH!). Lücking et al. (Reference Lücking, Archer and Aptroot2009), in their world key, assigned G. flavovirens to ‘Group 8’, G. longissima to ‘Group 17’ and G. sitapurensis to ‘Group 4’, based on details given in the protologues. We have examined the types of the above species and found that all agree in morphology, anatomy (such as the inspersed hymenium) and chemistry. Compared to the protologues (Makhija & Adawadkar Reference Makhija and Adawadkar2005), G. flavovirens has 14–18-septate, 49–54 μm long ascospores and not 3–9-septate, 16–42 × 4–6 μm large ascospores; G. sitapurensis has a completely instead of laterally carbonized exciple; G. longissima has entire labia and rarely shows striae. Therefore, both G. longissima and G. sitapurensis are synonymized here under Graphis flavovirens and a revised brief description is provided above.
Recently, Swarnlatha (Reference Swarnlatha2017) described G. andamanica from the Andaman Islands. The author mentioned cinnamon red granules in the hymenium but this is not a constant character. Our examination of the type material revealed that this taxon is also conspecific with G. flavovirens and is therefore synonymized here.
In the worldwide key to the genus Graphis (Lücking et al. Reference Lücking, Archer and Aptroot2009), G. flavovirens is correctly keyed out under ‘Group 10’, where it is most similar to G. gloriosensis A. W. Archer & Elix, but the latter differs in its smaller ascospores (50–90 × 10–12 μm).
Graphis nigrocarpa Adaw. & Makhija
Mycotaxon 96, 56 (2006); type: India, Tamil Nadu, Munnar to Kodai, 24 January 1976, M. B. Nagarkar & Gole 76.623 (AMH!—holotype).
Graphis kollaimalaiensis Adaw. & Makhija, Mycotaxon 96, 55 (2006); type: India, Tamil Nadu, Kollaimalai, 15 October 1985, M. B. Nagarkar & P. G. Patwardhan 85.1526 (AMH!—holotype).
Thallus corticolous, greenish to yellowish, cracked, uneven, thick.
Ascomata lirellate, partially raised to emergent, prominent, black, simple to triradiate or irregularly branched, straight to flexuose, wavy with obtuse ends, 1–10 mm long, 0.15–0.8 mm wide; disc narrowly closed, blackish brown; exciple carbonized, present at the base; labia completely carbonized, entire, convergent with lateral thalline margin; hymenium inspersed with small granules, 125–175 μm high, KI−, I−; asci (4–)6–8-spored; ascospores hyaline, 8–13 transversely septate, ellipsoidal, 35–65 × 5–9 μm, I+ blue; norstictic acid; thallus UV−.
Notes
Adawadkar & Makhija (Reference Adawadkar and Makhija2006) simultaneously described Graphis kollaimalaiensis Adaw. & Makhija and G. nigrocarpa Adaw. & Makhija as new species from India. We have examined the types (AMH!) of both taxa and found that they are similar in morphology, anatomy (such as the inspersed hymenium) and chemistry, except there is variation in the length of the lirellae (1–10 mm long) in G. nigrocarpa. When comparing the protologues (Adawadkar & Makhija Reference Adawadkar and Makhija2006), G. kollaimalaiensis has a hyaline hymenium which is not inspersed, while G. nigrocarpa has a clear to sometimes inspersed hymenium with crystals. However, we observed a distinct inspersed hymenium in both the taxa. Therefore, in the worldwide key to the species of Graphis (Lücking et al. Reference Lücking, Archer and Aptroot2009), this species is keyed out under ‘Group 10’, where it is most similar to G. desquamescens (Fée) Zahlbr. although this species lacks a thalline margin and has smaller ascospores (25–50 μm long). As it represents better material, G. nigrocarpa is adopted here as the name for the taxon while G. kollaimalaiensis is synonymized and a revised brief description is given above.
Schistophoron tenue Stirt.
Proc. Nat. Hist. Soc. Glasgow 4, 165 (1876).
Phaeographina nakanishii Patw. & Nagarkar, Biovigyanam 5, 136 (1979); type: India, West Bengal, Darjeeling District, 10 km to Teesta on Rangpo road, in evergreen forest, November 1977, P. G. Patwardhan & M. B. Nagarkar 77.1977 (AMH!—holotype).
(Fig. 2F)
Notes
Patwardhan & Nagarkar (Reference Patwardhan and Nagarkar1979) described Phaeographina nakanishii as a new species from India. We examined the type (AMH!) and found that it agrees with Schistophoron tenue in morphology, anatomy and chemistry. The former is therefore synonymized here. In India, this species is distributed in Andhra Pradesh, Orissa and Tamil Nadu (Singh & Sinha Reference Singh and Sinha2010).
Acknowledgments
The authors are grateful to Dr A. Mao, Director, Botanical Survey of India, Kolkata, for encouragement and to Dr G. P. Sinha, Head of Office, Botanical Survey of India, Central Regional Centre, Allahabad, for providing facilities. The curators of the herbaria AMH, BSA, BM, G, H and LWG are thanked for the loan of type specimens. We also thank Dr Robert Lücking for providing a corrected and revised version of the manuscript and two anonymous reviewers for their useful comments and suggestions. Financial assistance provided to PS under a National Post Doctoral fellowship (PDF/2016/002035) by the Science and Engineering Research Board (SERB), New Delhi, and to KPS under a Senior Scientist Platinum Jubilee fellowship (NAS/443/12/2016–17) by the National Academy of Sciences, India (NASI) is gratefully acknowledged.
