Opuscula Philolichenum, 11: 11-18. 2012. *pdf available online 3January2012 via (http://sweetgum.nybg.org/philolichenum/)

The identity of Hypogymnia delavayi (Parmeliaceae) and its impact on H. alpina and H. yunnanensis

1 BRUCE MCCUNE

ABSTRACT. – The type of Hypogymnia delavayi, together with the two associated specimens collected by Delavay, fit perfectly the distinctive species currently known as H. yunnanensis. Accordingly, H. yunnanensis is placed in synonymy with the older name H. delavayi; this species is now known only from southwest China. Many specimens representing the common subalpine to alpine ground-dwelling species in northern India and Nepal, previously placed in H. delavayi, are referred to H. alpina Awasthi. Reports of H. delavayi from Far East Russia belong to other species.

KEYWORDS. - China, Hengduan Mountains, Himalaya Mountains, India, Lecanorales, lichenized ascomycetes, lichenized fungi, Yunnan Province.

INTRODUCTION

The name Hypogymnia delavayi (Hue) Rassad. has been applied broadly in Asia. Rassadina (1956, 1971) included it in the far east Russian lichen flora as a species with narrow lobes (0.5-1 up to 4 mm wide) that are perforate below and lacking soredia and isidia. Most of this material has since been segregated as H. sachalinensis Tchab. & McCune (Tchabanenko & McCune 2001). The name has also been applied to the common subalpine to alpine brownish, perforate species occurring on many substrates in the Himalayas (Elix & Jenkins 1989). Studies of the type material of H. delavayi revealed that neither the far east Russian nor the Himalayan applications are correct. The purpose of this paper is to clarify the identity of H. delavayi.

MATERIALS AND METHODS

This study is based on herbarium specimens deposited in the following herbaria: BM, C, CANL, COLO, E, GZU, H, H-NYL, HMAS-L, KUN, LWG, MAF, NY, PC, S, UPS, and US, as well as specimens collected by the author. Thin-layer chromatography (TLC) was performed to detect lichen substances using standard methods of Culberson (1972). Fragments of specimens were extracted in acetone at room temperature, spotted on aluminum-backed silica gel plates (Merck 5554/7 Silica gel 60 F254), run in solvent systems A o and C, lightly brushed with 10% H2SO4, and charred in an oven at 100 C. No attempt was made to distinguish chloroatranorin from atranorin.

RESULTS

Examination of the type of Hypogymnia delavayi from PC revealed that it, plus the two associated specimens collected by Delavay, fit perfectly what is currently known as H. yunnanensis Y. M. Jiang and J. C. Wei. The morphology and chemistry of the types of these two species are the same as is described below. The older name, H. delavayi takes precedence and H. yunnanensis is here placed in synonymy with that name. The type of Hypogymnia yunnanensis is from Lijiang in Yunnan Province, China and was collected at 3000 meters (Jiang 286, HMAS-L!). The original description of H. yunnanensis (Jiang & Wei 1990)

1 BRUCE MCCUNE – Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331-2902, U.S.A. – e-mail: [email protected]

11 stated that it was P- but contained physodalic acid and atranorin. TLC of the holotype of H. yunnanensis revealed the following compounds: atranorin and physodic, 3-hydroxyphysodic, and vittatolic acid. Thus the type of H. yunnanensis is chemically identical to that of H. delavayi. The common saxicolous/terricolous species in India, Nepal, Tibet, and SW China that has been commonly referred to as Hypogymnia delavayi in the past (e.g., Awasthi 1984, Elix & Jenkins 1989) is here identified as H. alpina based on differences in chemistry and morphology. Hypogymnia delavayi has a verrucose, pale greenish gray upper surface; frequent lateral adventitious budding and pinnate branching; major lobes that are often considerably broader than thick; and it is epiphytic or on low woody substrates. In contrast, H. alpina has a rather smooth, dark brown upper surface (except when occurring in deeply shaded habitats, then grayer) with prominent black mottling; predominantly isotomic dichotomous to irregular branching; major lobes that are subcylindrical to cylindrical in cross section; and it is commonly terricolous or saxicolous, in addition to being epiphytic. Furthermore, the lower surface of H. alpina is jet black and glossy, browning only at the tips, while the lower surface of H. delavayi is commonly matte and pale to mid brown in a broad zone, though some specimens are mostly black below. Hypogymnia alpina also differs greatly in habitat. Hypogymnia alpina occurs at high elevations, mostly above 4000 meters in the Himalayas and Hengduan Mountains. Hypogymnia delavayi is apparently endemic to Yunnan and Sichuan, where it is so far known from only moderate elevations (mostly 2000-3200 m). The type specimen of H. delavayi was collected at only 2000 meters elevation in Yunnan Province. Although in describing Hypogymnia alpina Awasthi (1984) attempted to distinguish it from H. delavayi, his concept of H. delavayi clearly differed from the type, which he had not seen. His proposed differences between the newly described H. alpina and what he thought represented H. delavayi were slight, being based on the size of the apothecia and the reaction with P. Size of apothecia is an unreliable character in most Hypogymnia species, with small to large apothecia being commonly present on thalli of fertile species. Although Awasthi separated H. alpina as being P+, he also stated that P- forms exist. This agrees with my observations: by TLC 25% of 40 specimens lacked physodalic acid and gave P- spot tests. The original specimens of Hypogymnia alpina were stored for a long time in Awasthi's personal herbarium but are now deposited in LWG (D.D. Awasthi pers. comm. 1998). Examination of the type of H. alpina confirms that the common brownish ground-dwelling species of the Himalayas is H. alpina.

1) Hypogymnia alpina D.D. Awasthi, Kavaka, 12(2): 91. 1984. TYPE: INDIA. UTTAR PRADESH: Uttarkashi District, Gomukh area, right bank, 6th moraine, 3750 m, on twigs of scandent shrubs, 5 July 1976, D. D. Awasthi & S. R. Singh 8567B (LWG!, holotype). FIGURES 1 AND 2A .

SYNOPSIS. – Thallus loosely appressed to suberect with separate, rarely contiguous lobes; brown to dark brown, uniformly blackening or blackish mottled, lobe tips frequently perforate, lobe cavity white above and dark below or tan to gray above and below; soredia and isidia lacking.

DESCRIPTION. – Thallus to 10 cm diam, appressed to suberect; branching mostly isotomic dichotomous; lateral budding and narrow perpendicular adventitious lobes infrequent; lobes imbricate, mostly 1-2(3) mm broad, strongly inflated, separate on the thallus periphery but subcontiguous to contiguous internally; upper surface greenish gray to brown or dark brown, with black mottling or uniformly blackening, often glossy, epruinose, smooth to weakly rugose; lower surface black, usually glossy, dark brown near the lobe tips, occasionally perforate; lobe tips and axils commonly perforate, the holes lacking a differentiated rim; ceiling of lobe cavity white to grayish; floor of lobe cavity grayish to dark brown; soredia and isidia lacking; apothecia sessile to substipitate, the receptacle urn- or funnel-shaped; disk brown, to 4 mm diameter; ascospores simple, hyaline, 8/ascus, 5-10 x 4-6 µm; spermatia rod-shaped to weakly bifusiform, 4-8-6.5 x 0.5-0.7 µm.

CHEMISTRY. – Atranorin, physodic acid, +/- physodalic (75% of 40 specimens) acid, +/- protocetraric acid (always with physodalic acid but sometimes in low concentrations), +/- 2'-O- methylphysodic acid (23%), and +/- 3-hydroxyphysodic acid (60%). Spot tests (medulla): K- or K+ slow reddish brown, KC+ orange red, usually P+ orange, sometimes P-.

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Figure 1, Hypogymnia alpina. A, habit (Sharma et al. AC42; scale = 2.0 mm). B, perforations in lobes (Watson 23; scale = 1.0 mm).

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Figure 2, lobe cavities of Hypogymnia alpina and H. delavayi. A, H. alpina (Watson 23; scale = 2.0 mm). B, H. delavayi (holotype, Delavay 1599; scale = 2.0 mm).

14 TLC of the holotype revealed all of the substances listed above.

SUBSTRATE. – Commonly on soil and rock, also on bark and wood; subalpine and alpine.

DISTRIBUTION. – Apparently along the whole length of the Himalayas, including Bhutan, northern India, Nepal, and Tibet, and extending into the Hengduan Mountains of Sichuan and Yunnan (figure 4).

DISCUSSION. – Hypogymnia laccata J.C.Wei & Y.M.Jiang from southwestern China is similar in chemistry and the tendency to become dark brown. But H. laccata tends to form appressed rosettes rather than separate lobes, though some separate lobes are common. H. laccata is less strongly blackened, develops a rugose upper surface, is normally corticolous, and is less conspicuously perforate.

Selected specimens examined. – BHUTAN. PARO DIST.: Chele la pass, subalpine zone, 27.3667oN 89.3317oE, 3900 m, U. Søchting 9062 (C, THIM). CHINA. SICHUAN PROV.: JIULONG CO.: Ji Chou Mt., 29.75oN 101.5oE, 4300 m, L. S. Wang 96-16555b (KUN). KANGDING CO.: Zhe Duo Mt., 30oN 102oE, 4000 m, L. S. Wang 96-16338 (KUN); Weilong Balang Mountain, 4400 m, Li Li-ja 5507 (CANL). YANYUAN CO.: Daling Village, Huo Lu Mt., 27.5oN 101.5oE, 4150 m, L. S. Wang 83-1232 (KUN). SIKANG: KANGTING (TACHIENLU) DISTR.: Yara, 4200 m, Harry Smith 14036 (UPS). TIBET: NIE LA MU CO., 28.1oN 85.9oE, 3950 m, Chen S.-k. 26 (KUN). YUNNAN PROVINCE: DEQIN CO., Bei Ma Xue Shan, Ya Kou, 28.38oN 99oE, 4300 m, L. S. Wang 94-15344 (KUN); GONG SHAN CO., Yen Niu Gu, 27.801oN 98.825oE, 2950 m, L. S. Wang 00-19362 (KUN); LIJIANG CO., Yu-long-xue Mt., 27.033oN 100.267oE, 4100 m, L. S. Wang 9240 (KUN); LUQUAN CO. Jiaozixue Mt., 26.100oN 102.867oE, 4200 m, B. McCune 25560 (OSC); ZHONGDIAN CO., Daxue Mt., 28.567oN 99.817oE, 4500 m, L. S. Wang 01-20760 (KUN); Big Snowy Mt, Da Xae Shan, summit of pass, on humus among moss on calcareous rock, 3350 m, M. F. Watson 23 (E). INDIA. NORTH SIKKIM: Chubuk, above Thanngu, 4250 m, P. K. Divakar & D. K. Upreti 04-003924 (LWG, duplicate in MAF); Yangdi, after Thanngu, 4250 m, P. K. Divakar & D. K. Upreti 04-003952 (LWG, duplicate in MAF). SIKKIM: Chaunrikhiang, 4500 m, M. F. Watson 55 (E); towards East Rathong Glacier, 4500 m, M. F. Watson 60 (E). UTTARANCHAL: 16 km SE of Gangotri, Tabovan, 30.9oN 79.1oE, 4500 m, L. Tibell 22038 (UPS). NEPAL. Above Yala, 28.211o85.613oE, 5120 m, G. & S. Miehe. 4680c (GZU); East Nepal, Sankhuwasabha Dist., SE ridge of Maklu, 27.86667oN - 87.08334oE, 5025 m, D. G. Long 20954 (E); Himalaya: ad marginem glaciei concretae "Barun Khola superior", 27.68oN 87.26oE, 4900 m, M. Daniel 23.V.1973 (GZU); Jikeapsa NE of Kiangjin, 28.221oN 85.676oE, 4090 m, G. & S.Miehe 4352 (GZU); Khumbu Himal, Umgebung des Ngozumpa-Glac., Berggruppe N Chhugyuma, 27.999o86.692oE, 5400 m, W. Brandstetter, 4.1977 (GZU); Kyangen River, 28.2239oN 85.5768oE, 4595 m, R. Sharma et al. AC 19, AC21, AC42 (E); Kyanjan ri, 28.2205oN 85.5767oE, 4400 m, R. Sharma, et al. L4 (E); Langsuhisa Glacier, lateral E moraine, 28.208oN 85.666oE, 4530 m, G. & S. Miehe 12017 (GZU); Langtang area, near Kyangjin, 28.213oN 85.567oE, 3750 m, J. Poelt N86-L258 (GZU); Niang Tscha, 28.182oN 85.625oE, 4820 m, G. & S. Miehe 14002 (GZU); Ost-Nepal, Khumbakarna- Himal, Dhankuta Distr: Barun Glacier-Valley, 27.848oN 87.076oE, 5100 m, T. Wraber 124-88 (GZU); Surdscha Kunda, 28.107oN 85.48oE, 4850 m, G. & S. Miehe 8728 (GZU).

2) Hypogymnia delavayi (Hue) Rassad., Bot. Mater. Gerb. Bot. Inst. V. A. Komarova, 11: 5. 1956. Parmelia delavayi Hue, Bull. Soc. Bot. France, 34: 21. 1887.2 TYPE: CHINA. YUNNAN PROV.: dans la bois de Mao-kou-tchong, au dessus Tapin-tze, 2000 m, 15.v.1885, A. Delavay 1599 (PC!).

Hypogymnia yunnanensis Y.M.Jiang & J.C.Wei, Acta Mycol. Sin. 9:293. 1990.

FIGURES 2B AND 3.

Although Elix and Jenkins (1989) selected a lectotype from a set of four related specimens collected by Delavay (PC0124209, 10, 11, and 12; the first two collected on the same day), this was unnecessary since the number on one specimen (Delavay 1599, PC0124210) matches that given for the holotype by Hue (1887). PC0124209 has a different number (Delavay 1609), while the other two were

2Cited as “Hue apud Nyl., Flora 72:135. 1887” by Awasthi (1984) and Rassadina (1956). Note that the description of P. delavayi in Hue (1899) is much more complete than his original description (Hue 1887).

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Figure 3, holotype of Hypogymnia delavayi (Delavay 1599). A, habit (scale = 2.0 cm). B, lobes showing adventitious lobules and verrucose upper surface (scale = 2.0 mm).

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Figure 4, world distributions of Hypogymnia alpina (above) and H. delavayi (below) based on specimens examined for this study.

apparently not numbered by Hue. In any case, all four specimens are the same species and TLC showed uniform results (atranorin, 2'-O-methylphysodic, physodic, 3-hydroxyphysodic, and vittatolic acids).

SYNOPSIS. – Lobes weakly to strongly pinnately branched; adventitious lobes present; upper surface slightly to extremely verrucose; cavity ceiling white, floor white to dark; lower surface often brown rather than black. This species has swollen, rather closely set lobes with abundant marginal budding of lobules, in places almost pectinate.

DESCRIPTION. – Thallus appressed, to 15 cm diam; branching variable but often somewhat pinnate; lobes commonly (0.5)1-3(10) mm broad, short and strongly inflated or elongate; lobes contiguous centrally, separate or contiguous at the margins; lateral budding and narrow perpendicular adventitious lobes often abundant, but sometimes nearly absent; upper surface becoming distinctly verrucose; lower surface near lobe tips brown to dark brown, less often black, matte or rarely glossy, usually perforate; holes in lower surface large, gaping, conspicuous, also common in lobe tips and axils, lacking a differentiated rim; ceiling of lobe cavity white; floor of lobe cavity white to brown; soredia and isidia lacking; apothecia common,

17 sessile to substipitate, the receptacle urn- or funnel-shaped; disk reddish brown, to 8(13) mm diameter; ascospores 5.5-7.5 x 4-5 µm.

CHEMISTRY. – Atranorin, physodic, 3-hydroxyphysodic, and accessory 2'-O-methylphysodic and vittatolic acids; cortex K+ yellow, C-, KC-, P+ pale yellow; medulla K+ slow reddish brown, C-, KC+ orange-red, P-.

SUBSTRATE. – On bark and wood.

DISTRIBUTION. – Apparently endemic to SW China (figure 4), mainly at middle elevations (below 3200 m).

Selected specimens examined. – CHINA. SICHUAN PROV.: DU KOU CO.: Yan Di, Yan Kou Village, Shi Bo Mt, 27.5oN 101.5oE, 2000 m, L. S. Wang 83-544 (KUN). LUDING CO.: Gongga Mt., Hai Luo Gou, Camp, 29.83oN 102.3oE, 3100 m, L. S. Wang 96-16252 (KUN). MI YI CO.: Ma Long Village, Bei Puo Mt., 26.83oN 102oE, 3000 m, L. S. Wang 83-810 (KUN). COUNTY UNKNOWN: Reg. bor.-occid., Sankar-won-ma, Harry Smith 5246 (UPS). SIKANG: KANGTING (TACHIENLU) DIST.: Chungo Valley, Yara, 4050 m, Harry Smith 14011 (UPS). TIBET: Cha Yu Ca, Cawarong , Song Ta Xue Mt, N slope, 28.667oN 97.833oE, 3400 m, L. S. Wang 98-18440 (KUN). YUNNAN PROV.: BI JIANG CO.: Gao Li Gong Mt., 26.55oN 98.97oE, Zang Mu 975 (KUN). BINCHUAN CO.: Ji-zhu Mt., 25.97oN 100.45oE, 3000 m, L. S. Wang 94-15947 (KUN). DALI CO.: near trailhead to Mt. Cang Shan, 25.687oN 100.108oE, 3150 m, B. McCune 26765, 26766 (OSC). FU GONG CO.: Shang Pa Village, 26.917oN 98.883oE, 2100 m, L. S. Wang 82-589 (KUN). GONG SHAN CO.: Xi Shao Fang to Qiqi, 27.7oN 98.445oE, 2600 m, L. S. Wang 00- 19275 (KUN). JIANCHUAN CO.: Shi Bao Shan Park, 75 km S of Lijiang, 26.359oN 99.840oE, 2490 m, B. McCune 26735, 26741 (OSC). JINDONG CO.: Xu-jia-ba, Ai-lao Shan, 24.25oN 101.3oE, 2550 m, L. S. Wang 94-14608 (KUN). LIJIANG CO.: Yu Feng Temple, 27.083oN 100.167oE, 3150 m, L. S. Wang 93- 13631 (KUN). WEI XI CO.: Ye Zhi Village, Ba Di, 27.717oN 99.05oE, 2850 m, L. S. Wang 82-134 (KUN). YONG DE CO.: Ming Lan Village, 23.867oN 99.217oE, 2500 m, L. S. Wang 83-2722 (KUN). ZHONGDIAN CO.: Daxue Mt., 28.503oN 99.817oE, 3400 m, L. S. Wang 00-19904 (KUN).

ACKNOWLEDGEMENTS

I thank the curators of BM, C, CANL, COLO, E, GZU, H, H-NYL, HMAS-L, KUN, LWG, MAF, NY, OSC, PC, S, UPS, and US who kindly coöperated with loans and visits; as well as Louise Olley and Ulrik Søchting for sharing their collections. Wang Li-song kindly shared his voluminous collections from southwest China. P. K. Divakar and D. K. Upreti assisted with specimens from India. Alexander Mikulin kindly provided an English translation of Hypogymnia from the Russian flora. Thanks to anonymous reviewers for their suggestions. Jessica Allen, Elisa Alphandary, Lalita Calabria, Corinne Duncan, Erin Martin, and Christina Wesseler ably assisted with TLC.

LITERATURE CITED

Awasthi, D.D. 1984. The lichen genera Hypogymnia and Menegazzia from India and Nepal. Kavaka, 12(2): 87–97. Culberson, C.F. 1972. Improved conditions and new data for the identification of lichen products by a standardized thin- layer chromatographic method. Journal of Chromatography, 72: 113–125. Elix, J.A. and G.A. Jenkins. 1989. New species and new records of Hypogymnia (lichenized Ascomycotina). Mycotaxon, 35: 469–476. Hue, A.M. 1887. Lichenes Yunnanenses a claro Delavay anno 1885 collectos, et quorum novae species a celeb. W. Nylander descriptae fuerunt. Bulletin de la Societé Botanique de France, 34: 16–24. Hue, A.M. 1899. Lichenes extra-Europaei. A pluribus collectoribus ad Museum Parisiense Miss. Nouvelles Archives du Muséum D’histoire Naturelle [Paris], ser. IV, 1: 27–220. Jiang, Y.M. and J.C. Wei. 1990. [title originally in Chinese, English translation: A new species of Hypogymnia]. Acta Mycologica Sinica, 9(4): 293–295. Rassadina, K.A. 1956. Species Lichenum novae et curiosae. II. Botanicheskie Materialy Otd. Spor Rast Akad Nauk SSSR, 11: 5–12. Rassadina, K.A. 1971. Hypogymnia. Pages 285-301 in Kopaczevskaja, E. G., M. F. Makarevicz, A. N. Oxner, and K. A. Rassadina, Handbook of the Lichens of the U.S.S.R. 1. Pertusariaceae, Lecanoraceae and Parmeliaceae. Nauka. Leningrad. 412 pp. Tchabanenko, S. and B. McCune. 2001. Hypogymnia arcuata and H. sachalinensis, two new lichens from east Asia. Bryologist, 104: 146–150.

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