Introduction
The genus Fellhanera Vězda comprises more than 70 species of crustose lichens with small, thin-margined apothecia with a paraplectenchymatous exciple, branched and anastomosing paraphyses, Byssoloma-type asci (sensu Hafellner Reference Hafellner1984), ellipsoid to cylindrical, septate ascospores typically constricted at the septa, and pycnidial conidiomata that produce bacilliform to pyriform conidia. The majority of species are foliicolous (Lücking Reference Lücking2008), although corticolous and saxicolous taxa are also known. Of the eleven species reported from the USA (Esslinger Reference Esslinger2011), six are typically saxicolous (van den Boom Reference van den Boom, Nash, Ryan, Diederich, Gries and Bungartz2004; Harris & Lendemer Reference Harris and Lendemer2009). Continuing fieldwork by the authors in the south-eastern part of the Great Plains has revealed a blastidiate crustose lichen with anthraquinones associated with exposures of non-calcareous sandstones. The species was recently discovered with apothecia in Kansas and confirmed to belong to Fellhanera.
Materials and Methods
Specimens were studied dry using dissecting microscopes and subjected to chemical analysis using standard spot tests (reagents are abbreviated following Brodo et al. Reference Brodo, Sharnoff and Sharnoff2001) and thin-layer chromatography (TLC). TLC was carried out at KANU using solvent systems A, B′ and C following the methods of Orange et al. (Reference Orange, James and White2001). Mounts were prepared by hand with a razor blade and placed in water. Microscopic characters were observed on material mounted in water and images were captured and measured to the nearest hundredth µm using a Nikon Color View II soft imaging system camera with analySIS Imager 3.2. Illustrations were prepared using Adobe Photoshop. Measurements are presented as a simple range or, where sufficient material allowed, as the average (
$\bar x$
) +/− one standard deviation (SD), bounded by the smallest and largest observed values, and followed by the sample size (n) [i.e., (smallest observed)
$\bar x-1\ SD-\bar x-\bar x+1\ SD$
(largest observed) (n)].
Taxonomy
Fellhanera crucitignorum C. A. Morse & Ladd sp. nov.
MycoBank No: MB803253
Fellhanera species saxicola vel muscicola, thallo blastidiato crystalla rubra et K+ purpurea continenti, ascis 8-sporis, ascosporis submuriformibus 15·8–20·1×6·6–8·2 µm, conidiis bacilliformibus vel lageniformibus, 3·3–4·7×1·0–1·5 µm.
Typus: USA, Kansas, Woodson Co., 6 mi E of Toronto, Woodson Co State Fishing Lake & Wildlife Area on SE side, 37·79396°–37·79463°N, 95·83590°–95·83416°W, elevation 1020–1050 ft, upland, brushy to open Cross Timbers with frequent outcrops and boulders of non-calcareous sandstone on gentle, primarily W-facing slopes above artificial lake, on outcrops and small rocks and overgrowing bryophytes, occasionally on stabilized soil, 18 March 2012, C. A. Morse 23306 & K. J. Morse (KANU—holotypus).
(Fig. 1)
Fig. 1. Fellhanera crucitignorum. A, apotheciate thallus growing on rock; B, apothecial section (Morse 23306—holotype); C, ascospores after treatment with 10% KOH (Morse 23306—holotype); D, conidiospores (Morse 14523, KANU). Scales: A=1 mm; B=100 µm; C & D=20 µm. In colour online.
Thallus to 20 cm diam., whitish grey, brownish grey, greyish green, yellowish green, or (typically in areas where blastidia are developing) mottled pale to dark orange, arising as small, convex, pale greenish or greyish granules, occasionally from a white hyphal weft or a scantily developed, finely fibrous, white prothallus, granules coalescing in older areas to form a thin, effuse, continuous, granular-verrucose thallus (especially over bryophytes) or forming thicker, verrucose areoles 0·5–2·0 mm wide, or the thallus poorly developed and essentially chasmolithic, especially on coarser saxicolous substrata; blastidia produced laminally and marginally on convex areoles, initiated in small punctiform to oblong patches c. 0·5 mm diam., often coalescing to cover large areas of the older part of the thallus, pale green, pale orange, or (usually) dark orange, fine and soredia-like to coarser and globose, oblong or irregular in shape, 25–53×18–35 µm, budding apically and becoming somewhat coralloid; soralia and isidia absent. Photobiont chlorococcoid, the cells round to slightly oblong, (4·5–)6·4–8·2–9·9(–10·9) µm in diam. (n=35).
Apothecia rare (observed on three specimens), widely scattered, sessile, constricted at the base, 0·2–0·5 mm diam.; disc dark reddish brown to black, plane to convex, surface slightly roughened; margin prominent and slightly elevated above the disc or becoming excluded in convex apothecia, finely papillate, concolorous with the disc or paler; epihymenium pale; hymenium 50–70 µm high, pale to yellowish, not inspersed; paraphyses moderately branched, slender, scarcely expanded distally, to c. 2·3 µm wide; proper exciple paraplectenchymatous, of globose to oblong cells 5·2–6·7 µm diam., the outer layer c. 36 µm thick, hyaline, the inner layer c. 19 µm thick, with dark reddish brown (K+ reddish) cell walls; hypothecium to 85 µm high, of globose cells with reddish brown or orange-brown walls, the orange pigments intensifying in K. Asci Byssoloma-type (outer wall I+/KI+ dark blue, tholus KI+ pale blue with a darker tubular structure), c. 43–61×13–16 µm; ascospores 8 per ascus, ellipsoid to narrowly ovoid, typically constricted at the septa and often somewhat irregular in outline, submuriform with 4 to 6 primary locules, the central 2 to 4 with (0–) 1 (–2) vertical septa, (14·1–)15·8–18·2–20·1(–23·0)×(5·9–)6·6–7·4–8·2(–9·1) µm (n=29).
Pycnidia uncommon, partially immersed, black (walls charcoal grey to blue-grey, K−); conidia bacilliform to ± lageniform or somewhat biclavate, (2·4–)3·3–4·0–4·7(–6·6)×(0·9–)1·0–1·3–1·5(–1·9) µm (n=56).
Chemistry
TLC: orange areas of thallus and blastidia contain two anthraquinones: 1) Rf class 7/6–7/7 (before charring pale yellow in daylight, UVL+ yellow to yellow-orange; after charring dull greenish yellow, UVL+ dark brownish orange in solvent A, faint yellowish, UVL+ yellowish orange in solvent B′, and yellowish grey, UVL+ dark in solvent C); 2) Rf class 6/5–6/6 (before charring pale yellow in daylight, UVL+ pure orange; after charring brownish grey, UVL+ deep pinkish orange in solvent A, nearly colourless, UVL+ red-orange in solvent B′, and brownish grey, UVL+ dark purplish in solvent C). The upper spot appears to be consistent with fragilin. Spot tests: greenish and greyish areas of thallus and apothecial discs and margins all K−, UV−; orange areas K+ magenta, UV+ deep reddish orange.
Etymology
The epithet crucitignorum is derived from the Latin words ‘crux’ (cross) and ‘tignum’ (board, and by extension timber) and translated as ‘of the Cross Timbers’, the ecogeographical region in which the majority of specimens have been collected. The Cross Timbers contains some of the last expanses of old growth oak woodlands in North America (Clark & Hallgren Reference Clark, Hallgren and Spetich2004), and fieldwork is revealing significant lichen discoveries (e.g. Ladd & Morse Reference Ladd and Morse2012).
Ecology and distribution
Fellhanera crucitignorum is known from the eastern part of the Central Mixed-Grass Prairie, Osage Plains/Flint Hills Prairie, and Cross Timbers ecoregions in eastern Kansas and central Oklahoma (The Nature Conservancy 2007), at elevations of 213–481 msm (Fig. 2), where it occurs in upland, Cross Timbers woodland or in mixed-grass and tallgrass prairie openings, often on open, south and west-facing slopes. Most specimens occurred directly on outcrops, boulders, and fragments of sandstone, or overgrowing bryophytes on sandstone. Two specimens were collected from stabilized sandy soil weathered from typical sandstone substratum. Endocarpon pallidulum (Nyl.) Nyl. and Trapelia placodioides Coppins & P. James appear to be common associates of F. crucitignorum. Other notable taxa found in close association include Agonimia opuntiella (Buschardt & Poelt) Vězda, Anisomeridium distans (Willey) R. C. Harris, Lepraria lobificans Nyl., Peltula patellata (Bagl.) Swinscow & Krog, Phaeophyscia adiastola (Essl.) Essl., Rinodina destituta (Nyl.) A. Zahlbr., R. oxydata (Massal.) Massal., R. tephraspis Tuck., Thelenella muscorum (Fr.) Vain. and Thelidium minutulum Körb.
Fig. 2. Distribution of Fellhanera crucitignorum.
The distributional pattern of F. crucitignorum in eastern Kansas tracks closely areas where surfacing sandstone is abundant, as it is throughout much of central Oklahoma; elsewhere in eastern Kansas, in the Flint Hills and eastern Osage Plains, the dominant substrata are comprised of surfacing limestones and highly calcareous soils. In combination with the relatively arid climate of the southern Plains, this surfacing sandstone gives rise to the distinctive vascular plant and lichen floras of the Cross Timbers and Smoky Hills Prairies. Mean annual precipitation across the known range of F. crucitignorum varies from c. 700–1200 mm. All of the region has a negative net evaporational value (open pan evaporation minus annual precipitation), typically ranging from 375 mm in the eastern portion of the range to 1550 mm in the west (based on Owenby et al. Reference Owenby, Heim, Burgin and Ezell1992 and NOAA 1982). Interestingly, despite intensive fieldwork (e.g. Harris & Ladd Reference Harris and Ladd2005), the species has not been found in the higher net precipitation accumulation region of the adjacent Interior Highlands, which has similar vegetation and substrata.
Discussion
Fellhanera crucitignorum is characterized by the combination of a blastidiate thallus with localized areas of anthraquinone deposition, red-brown to black apothecia with concolorous proper margins, 8-spored asci with submuriform ascospores, bacilliform to lageniform conidia, and its association with non-calcareous sandstone. Several saxicolous members of the F. silicis group and F. nashii van den Boom regularly produce blastidia (van den Boom Reference van den Boom, Nash, Ryan, Diederich, Gries and Bungartz2004; Harris & Lendemer Reference Harris and Lendemer2009), which are characterized as granular to soredioid or isidoid, but those species produce narrower, transversely septate spores. Secondary chemistry is unknown from members of the F. silicis group, but van den Boom (Reference van den Boom, Nash, Ryan, Diederich, Gries and Bungartz2004) reported atranorin and probably divaricatic acid from F. nashii.
Fellhanera borbornica Sérus. et al., recently described from material collected from basalt on the island of La Réunion in the Indian Ocean (Lumbsch et al. Reference Lumbsch, Ahti, Altermann, Amo de Paz, Aptroot, Arup, Bárcenas Peña, Bawingan, Benatti and Betancourt2011), differs in its slightly broader muriform spores, as well as features of the apothecia and pycnidia, does not produce vegetative diaspores, and evidently lacks chemistry. Fellhanera includes several foliicolous species with submuriform or muriform spores in the F. fuscatula aggregate, circumscribed by the presence of fusiform or bacilliform conidia and the absence of secondary chemistry (Lücking Reference Lücking1997, Reference Lücking2008). Fellhanera crucitignorum is not close to any one of them in thallus and apothecial morphology and chemistry.
Sterile specimens of F. crucitignorum are most likely to be confused with sorediate species of Caloplaca, such as C. xanthostigmoidea (Räs.) Zahlbr., a species producing isidioid protruberances bearing aggregations of soredia-like elements (Søchting & Tønsberg Reference Søchting and Tønsberg1997). However, that species is typically corticolous, with a distinctly yellow to orange thallus and orange pycnidia, and occurs in cool temperate regions in North America (Wetmore Reference Wetmore2001). Its range is not known to overlap with that of F. crucitignorum.
The presence of anthraquinones in the thallus of Fellhanera crucitignorum constitutes a first report for the genus and is of some interest. Various pigments have been reported from Fellhanera, including the xanthone asemone in F. bouteillei (Desm.) Vězda (Spier et al. Reference Spier, Aptroot and van Herk2002), an unknown orange pigment in the pycnidial wall of F. ochracea Sparrius & Aptroot (Sparrius & Aptroot Reference Sparrius and Aptroot2000) and substances described as K+ purple or purplish brown in the hypothecium and exciple of other species (Lücking Reference Lücking2008; Harris & Lendemer Reference Harris and Lendemer2009). Otherwise, secondary chemistry in this genus appears to be limited to usnic acid, isousnic acid, zeorin, and a few fatty acids or orcinol para-depsides (Lücking et al. Reference Lücking, Lumbsch and Elix1994; Aptroot et al. Reference Aptroot, Brand and Spier1998; Sérusiaux et al. Reference Sérusiaux, Coppins, Diederich and Scheidegger2001; van den Boom Reference van den Boom, Nash, Ryan, Diederich, Gries and Bungartz2004; Lücking Reference Lücking2008).
Anthraquinones are known from some other genera of Pilocarpaceae and related taxa. Flavo-obscurin B1 has been isolated from the apothecial margins of Byssoloma rubromarginatum Messuti & de la Rosa (Messuti & de la Rosa Reference Messuti and de la Rosa2007) and emodin, 7-chloremodin, and fragilin from B. tricholomum (Mont.) Zahlbr. (Santesson Reference Santesson1970). Although Byssoloma and Fellhanera are closely related (Lücking Reference Lücking2008), the majority of Fellhanera species, including F. crucitignorum, are readily distinguished from Byssoloma by differences in exciple structure (Lücking Reference Lücking1997, Reference Lücking2008). Members of the genus Malmidea Kalb et al. (Malmideaceae), a genus recently erected to accommodate the greater part of Malcolmiella Vězda, have been shown to produce norsolorinic acid and other anthraquinones (emodin, emodin bisanthron) and several additional constituents in the medullary tissue (Lücking Reference Lücking2008; Kalb et al. Reference Kalb, Rivas Plata, Lücking and Lumbsch2011). Malmidea was found to occupy an isolated position within the Lecanorales in the study of Kalb et al. (Reference Kalb, Rivas Plata, Lücking and Lumbsch2011), and its members are distinct from F. crucitignorum (and from other Pilocarpaceae) in features of the ascus, as well as in having a partially medullary exciple and simple spores. Malcolmiella cinereovirens Vězda, the type of the genus, which was found by Kalb et al. (Reference Kalb, Rivas Plata, Lücking and Lumbsch2011) to be distinct from Malmidea, has an ascus structure similar to that of Pilocarpaceae but differs from the new species and other members of Fellhanera in having 0–1-septate ascospores with warty ornamentation (Kalb et al. Reference Kalb, Rivas Plata, Lücking and Lumbsch2011).
Specimens examined. USA: Kansas: Chautauqua Co., 3·0 mi N, 0·75 mi E Hale, West Liberty Cemetery and environs, 37·28°N, 96·04°W, 2007, Morse 15761 (KANU), 2009, Morse 20258 & Logan (KANU); Douglas Co., 1·75 mi N, 0·5 mi W junction of US Hwy 56 & Douglas Co. Rd 1057 in Baldwin City, University of Kansas Ecological Reserves: Breidenthal Biological Reserve, 38·81°N, 95·20°W, 2006, Morse 14539 & Morse (KANU); 2010, Morse 22126 & Logan (KANU), Morse 23189 & Logan (KANU, fertile specimen); c. 0·25–0·45 mi N, 1·75 mi E junction of Douglas Co. Rd 1055 & US Hwy 56 in Baldwin City, property of Ralph & Roma Earles, 38·78°–38·79°N, 95·15°W, 2012, Morse 23262 & Morse (KANU); Ellsworth Co., 2 mi S, 0·5 mi W Carneiro, Wildlife Management Area along E side 25th Ave, 2·5 mi S junction with KS Hwy 140, 38·70°N, 98·03°W, 2005, Morse 12189 (KANU, fertile specimen); 4 mi S, 2 mi E of Carneiro, Kanopolis State Park: Horsethief Canyon area, 38·67°N, 98·00°W, 2010, Morse 20357 & Logan (KANU); Franklin Co., 3 mi S, 1 mi E Homewood, Ottawa University Natural History Reservation, 38·47°N, 95·36°W, 2008, Morse 16346 & Logan (KANU); Montgomery Co., 0·5 mi N, 5·5 mi W Liberty, S side of Montgomery Co. State Lake, 37·16°N, 95·69°W, 2006, Morse 14367 (KANU); 2012, Morse 23343 & Morse (KANU); Woodson Co., 6 mi E Toronto, Woodson Co. State Fishing Lake and Wildlife Area on SE side, 37·79°N, 95·84°W, 2006, Morse 14523 & Roth (KANU); 2008, Morse 18045a & Logan (KANU); 2011, Morse 23098 & Morse (KANU). Oklahoma: Caddo Co., c. 2·5 mi S Hinton, Red Rock Canyon State Park, S end, 35·44°N, 98·35°W, 2007, Morse 14852 & Ladd (KANU); Red Rock Canyon State Park, N end, 35·46°N, 98·35°W, 2007, Morse 14900 & Ladd (KANU), Ladd 28568 & Morse (hb. Ladd), Ladd 28581 & Morse (hb. Ladd); Love Co., c. 8·5 mi N, 1 mi E of Marietta, Lake Murray State Park, 34·06°N, 97·09°W, 2009, Morse 18435 & Ladd (KANU); Okmulgee Co., 0·50–0·75 mi N, 6 mi W of junction of US Hwys 62 & 75 on S side of Okmulgee, Okmulgee State Park, 35·62°N, 96·07°W, 2009, Morse 20185 & Logan (KANU); Osage Co., c. 9 mi N of Pawhuska, Tallgrass Prairie Preserve, along Wild Hog Creek, 36·81°N, 96·77°W, 1996, Ladd 19888 (hb. Ladd); 7·5 mi N, 3 mi E Barnsdall, Woolaroc Wildlife Preserve, 36·66°N, 96·11°W, 2007, Morse 14632c & Ladd (KANU).
We thank Robert Lücking (F) and two anonymous referees for their careful review of the manuscript and helpful comments. Thanks to land owners for access to, and permission to collect on, their property, Katherine Morse for assistance in the field, Cindy Pessoni for map preparation, and Anthony Corbeill (Professor of Classics, University of Kansas) for assistance with the Latin. Fieldwork was made possible by anonymous contributions to the McGregor Herbarium Endowment Fund and The Nature Conservancy.
