Introduction

Hawaii is one of the most remote oceanic archipelagos on the planet, with at least 4000 km distance to any continent (Wagner & Funk 1995; Fleischer & al. 1998). As a result, a unique biota has evolved on these islands, with a high degree of endemism – up to 80 % in vascular plants – and striking radiations, such as in the lobeliads and silverswords (Baldwin & Sanderson 1998; Wagner & al. 1999; Barrier & al. 2001; Wagner & Herbst 2002; Carlquist & al. 2003; Givnish & al. 2009). The lichen biota of Hawaii has presumably been rather well-studied, mainly due to the work of Adolf Hugo Magnusson and Clifford Smith (Magnusson & Zahlbruckner 1943, 1944, 1945; Magnusson 1955; Smith 1991, 1993, 2001, 2013; Smith & al. 1997), with the most recent checklists including between 884 and 890 species (Elix & McCarthy 1998, 2008; Smith 2013). Lichens on islands have generally been believed to exhibit low degrees of endemism, around 20–30 % for Hawaii (Eldredge & Miller 1995), due to their supposedly easily dispersed spores and vegetative propagules (Smith 1995). However, recent molecular studies on the genera Lobariella Yoshim. and Pseudocyphellaria Vain. in Hawaii suggest that presumably widespread taxa in reality correspond to previously unrecognized, likely endemic species (Moncada & al. 2014; Lücking & al. 2017b); therefore, endemism in these two genera in Hawaii is now estimated at 75 %, comparable to that found in vascular plants.

The family Graphidaceae is a prominent example of how molecular data have reshaped fungal classifications, now including 79 genera compared to traditionally 12 that were distributed among two families (Staiger 2002; Frisch & al. 2006; Rivas Plata & al. 2012; Lumbsch & al. 2014; Lücking & al. 2017a). In addition, phylogenetic analyses helped to refine species concepts; an exemplary case are the Ocellularia papillata (Leight.) Zahlbr., O. perforata (Leight.) Müll. Arg. and O. terebrata (Ach.) Müll. Arg. morphodemes, now containing over 70 species (Lücking 2014). Based on these findings, it is expected that the approximately 100 species of Graphidaceae currently listed for Hawaii, with many presumably widespread taxa (Elix & McCarthy 1998, 2008; Smith 2013), hide numerous unrecognized endemics. In addition, due to lack of proper identification keys, Hawaiian Graphidaceae have never been critically inventoried, and additional species may await discovery. Currently, 70 species of lirellate Graphidaceae are reported for Hawaii (Table 1); of these, 13 (19 %) are considered endemic, nine eastern palaeotropical and one palaeotropical, 21 with neotropical affinities, and 27 pantropical to subcosmopolitan. The high proportion of taxa with neotropical affinities is likely an artefact of the availability of identification keys, which for a long time were more readily available for areas in the Neotropics, particularly Mexico and Brazil (Redinger 1933a, 1933b, 1935; Wirth & Hale 1963); Hawaiian material identified with these names may not actually represent these taxa.

The genus Halegrapha Rivas Plata & Lücking is one of the numerous new genera now recognized in Graphidaceae. It is characterized by a Graphis-like morphology, with whitish thalli and lirellae featuring thick, carbonized labia, but producing a Phaeographis-like hamathecium and Phaeographis-type ascospores that are brown-grey and usually small and with rounded ends (Lücking & al. 2011). To date, eight species are recognized in this group and, with the exception of H. mucronata (Stirt.) Lücking, all recent new discoveries are from North America, Mexico, Kenya, Sri Lanka, Malaysia, the Philippines and Japan (Lücking & al. 2011; Kashiwadani & al. 2014; Weerakoon & al. 2014). The genus has not previously been reported from Hawaii, and none of the names originally listed under Phaeographis Müll. Arg. or Phaeographina Müll. Arg. in the current checklists (Table 1) belongs to this genus.

Here we describe a new species of Halegrapha for the Hawaiian archipelago, discovered during a field expedition in 2013. The species is characterized by a unique set of characters and is putatively endemic to these islands; it is also the first record of the genus for Hawaii, which makes Halegrapha a truly pantropical genus present in all major tropical regions. As a result of this study, we also update the nomenclature of the species of lirellate Graphidaceae so far reported for Hawaii.

Material and methods

The work to describe the new species was done mostly by the first author, as part of a structured internship program between the Paulsen Gymnasium and the Botanischer Garten und Botanisches Museum, Freie Universität Berlin. The new taxon was detected as part of a revision by the first author of all specimens of Graphis Adans. collected during a 2013 field expedition to Hawaii by the second author and Bibiana Moncada (Universidad Distrital, Bogotá, Colombia) and locally coordinated by Clifford Smith (Oahu Army Natural Resources Program, Honolulu, Hawaii), Timothy Flynn (National Tropical Botanical Garden, Kauai, Hawaii), Patrick Bily (The Nature Conservancy Hawaii), Daniel Pomaika‘i (Maui Soil and Water Conservation Districts, Maunalei Arboretum) and Philip Thomas (Research Corporation of the University of Hawaii and the Hawaiian Ecosystems at Risk Project). The material was examined with a LEICA Zoom 2000 dissecting microscope and sections of thallus and lirellae mounted in tap water were examined under a ZEISS Axioscop compound microscope. Secondary chemistry was initially assessed using KOH spot tests and subsequently verified with standardized thin-layer chromatography (TLC) using solvent system C (Orange & al. 2010). To update the nomenclature of the lirellate Graphidaceae reported from Hawaii, we consulted type material, in part via JSTOR Global Plants ( https://plants.jstor.org) and protologues, partly via the Biodiversity Heritage Library ( https://www.biodiversitylibrary.org), in addition to the monographic treatments by Magnusson & Zahlbruckner (1943) and Magnusson (1955).

Results and Discussion

Halegrapha paulseniana Luch & Lücking, sp. nov. – MycoBank MB 828103. – Fig. 1D–F.

Holotype: U.S.A., Hawaii, Maui, East Maui, Haleakalā Volcano, lower Waikamoi Preserve (The Nature Conservancy), 5 km SE of Pukalani and 18 km SE of Kahului, lower access trail to preserve off Olinda Road, 20°48′23″N, 156°15′19″E, 1200–1300 m, disturbed primary forest dominated by Acacia koa and Campanulaceae, with invasive Hedychium gardnerianum in lower portions, 11 Jun 2013, R. Lücking, B. Moncada & P. Bily 35834 (BISH; isotypes: B, F).

Diagnosis — Differing from Halegrapha mexicana A. B. Peña & Lücking in the much larger lirellae featuring an apically complete, thin thalline margin, and from all other species in the genus in its laterally mostly uncarbonized excipulum.

Fig. 1.

A–C: Waikamoi Preserve, Maui, Hawaii, U.S.A., 11 June 2013; A: natural habitat of Halegrapha paulseniana; B: invasive ginger, Hedychium gardnerianum; C: persistent rhizomes of Hedychium gardnerianum; D–F: Halegrapha paulseniana; D: thallus with lirellae (type collection); E: section through lirella showing carbonized upper and basal excipulum; F: mature and (in lower left frame) post-mature (shrivelled) ascospores. – Scale bars: D = 1 mm; E = 100 µm; F = 10 µm.

Description — Thallus corticolous, to 5 cm in diam., 100–150 µm thick, continuous; surface uneven, creamwhite; prothallus absent. Thallus in section with thick, prosoplectenchymatous upper cortex, irregular algal layer and distinct medulla, partially encrusted with greyish crystals, when covering lirellae with a layer of large calcium oxalate crystal clusters. Photobiont Trentepohlia; cells rounded to irregular in outline, in irregular groups, yellowish green, 8–11 × 7–10 µm. Lirellae flexuose, irregularly branched, erumpent, with complete, laterally thick and apically thin thalline margin, 3–8 mm long, 0.3–0.5 mm wide, 0.25–0.35 mm high; disc partially exposed, dark brown to blackish brown, labia entire. Excipulum entire, ± completely carbonized but lateral portions partially uncarbonized and then leaving an apically carbonized and basally massively carbonized portion, 50–150 µm wide and high, laterally covered by corticate, algiferous thallus including a thick layer of calcium oxalate crystal clusters; hypothecium prosoplectenchymatous, 10–20 µm high, pale brownish; hymenium 100–120 µm high, colourless, strongly inspersed along paraphyses, inspersion composed of rather large, irregular droplets, dissolving in K (Phaeographis type or type B according to Lücking 2009), epihymenium granulose, 5–10 µm high, brownish. Paraphyses unbranched; asci fusiform to clavate, 100–110 × 20–25 µm. Ascospores 8 per ascus, oblongoval, 5(–7)-septate, 20–25 × 7–8 µm, 2.5–3.5 × as long as wide, becoming brown when mature and dark brown and shrivelled when post-mature, I+ violet-blue when immature and hyaline, I+ red-brown when mature and pigmented. Secondary chemistry: no substances detected by TLC.

Distribution and ecology — The new species is a putative Hawaiian endemic, so far known only from the Waikamoi Preserve on Maui (Fig. 1A). Parts of this preserve are heavily threatened by the invasive ginger Hedychium gardnerianum Sheppard ex Ker Gawl. (Fig. 1B, C), which can quickly overtake entire forest ecosystems and lead to extinction of local, endemic species (Holt 1992; Medeiros & al. 1995; Wood 2012).

Eponymy — The new species is dedicated to Friedrich Paulsen (1846–1909), a German pedagogue and philosopher, one of the founders of modern higher school education in Germany and name giver of the Paulsen-Gymnasium.

Remarks — The genus Halegrapha until now included eight species, which can be distinguished mainly based on hymenial inspersion, ascospore septation and secondary chemistry, together with aspects of thallus and lirellae morphology (Lücking & al. 2011; Kashiwadani & al. 2014; Weerakoon & al. 2014). Three species differ from H. paulseniana in the clear hymenium, namely H. kenyana Kalb & Lücking, H. mucronata A. B. Peña & Lücking and H. yakushimensis M. Nakan. & al.; the first also deviates by its smaller, 3–5-septate ascospores, the stictic acid chemistry, and the smaller lirellae with concealed disc and exposed, black labia. Halegrapha mucronata has much longer, 7–9-septate ascospores, norstictic acid, and black lirellae with only a basal thalline margin, while H. yakushimensis lacks secondary compounds, produces small, submuriform ascospores, and its much shorter lirellae have a concealed disc and exposed, black labia. Among the five taxa with inspersed hymenium, as in H. paulseniana, H. masoniana G. Weerakoon & al. can be distinguished by its much longer, 9–13-septate ascospores, the norstictic acid chemistry, and the lirellae with concealed disc and exposed, black labia. The remaining three species all lack secondary compounds, as in H. paulseniana, with H. chimaera Rivas Plata & Lücking and H. floridana Common & Lücking having slightly smaller ascospores and largely exposed, black labia, whereas H. mexicana differs chiefly in the much smaller lirellae lacking a thalline margin. Halegrapha paulseniana differs from all other species in the genus also by its often laterally uncarbonized excipulum, a pattern found in a few Graphis species, namely G. gregmuelleri Sipman & Lücking, G. immersoides Lücking and G. mirabilis Lücking & al. (Lücking & al. 2009).

The massively carbonized basal excipulum is reminiscent of species of Leiorreuma Eschw. (Staiger 2002), which differ from Halegrapha in the thin, indistinct labia and lack of lateral or apical carbonization. The only two species of Leiorreuma reported from Hawaii, L. exaltatum (Mont. & Bosch) Staiger and L. sericeum (Eschw.) Staiger (Table 1), both differ from the new species in the fully carbonized excipulum and the weakly developed labia, and L. sericeum also in the much smaller, often stellate ascomata and the smaller, consistently 3-septate ascospores (Staiger 2002). The well-developed, carbonized labia of the new species are shared with the genus Platygramme Fée (Staiger 2002), which lacks basal carbonization and the thallus is usually not whitish and Graphis-like. An exception is P. pachnodes (Fée) Fée (Tripp & Lendemer 2010), which has a Graphis-like appearance; it differs from the new species in the consistently exposed, thickly whitepruinose disc and the larger, submuriform ascospores. Thus far, two species of Platygramme are known from Hawaii: P. kaalensis (Tuck.) Luch & Lücking and P. tumulata (Nyl.) Luch & Lücking (Table 1; see also below). Both differ from the new species in the yellowish thallus and completely concealed disc, and P. kaalensis also in the thallus-covered labia appearing bluish, whereas P. tumulata deviates in the very small, submuriform ascospores. Phylogenetic relationships in the clade that includes these and other genera with brown ascospores (Halegrapha, Phaeographis, Platygramme, Sarcographa Fée, Thecaria Fée, Thecographa A. Massal.) are far from being settled (Rivas Plata & al. 2013) and it is possible that these genus concepts will not hold up.

Further nomenclatural novelties

Updating the nomenclature of the lirellate Graphidaceae reported from Hawaii (Table 1) requires the following new combinations:

Allographa gracilescens (Redinger) Luch & Lücking, comb. & stat. nov. [MycoBank MB 828104] ≡ Graphina incerta var. gracilescens Redinger in Ark. Bot. 26A(1): 60. 1935.

Fissurina homichlodes (Redinger) Luch & Lücking, comb. nov. [MycoBank MB 828105] ≡ Graphis homichlodes Redinger in Ark. Bot. 27A(3): 61. 1935.

Fissurina stromatoides (H. Magn.) Luch & Lücking, comb. nov. [MycoBank MB 828106] ≡ Graphis stromatoides H. Magn. in Ark. Bot., n.s., 3(10): 260. 1955.

Fissurina zahlbruckneriana Luch & Lücking, nom. nov. [MycoBank MB 828119] ≡ Graphis triticea f. lactea Zahlbr. in Denkschr. Kaiserl. Akad. Wiss., Wien Math.-Naturwiss. Kl. 88: 27. 1911 [non Fissurina lactea Fée, Essai Crypt. Écorc.: 47. 1825].

Phaeographis caesiohians (Nyl.) Luch & Lücking, comb. nov. [MycoBank MB 828107] ≡ Graphis caesiohians Nyl., Sert. Lich. Trop. Labuan Singapore: 13. 1891 ≡ Phaeographina caesiohians (Nyl.) Redinger in Rev. Bryol. Lichénol. 9: 100. 1936.

Phaeographis faurieana (Zahlbr.) Luch & Lücking, comb. nov. [MycoBank MB 828108] ≡ Phaeographina faurieana Zahlbr. in Ark. Bot. 31A(1): 40. 1943.

Phaeographis fulgurata (Fée) Luch & Lücking, comb. nov. [MycoBank MB 828109] ≡ Graphis fulgurata Fée, Essai Crypt. Écorc.: 35, t. XI, fig. 4. 1825 ≡ Phaeographina fulgurata (Fée) Müll. Arg. in Mém. Soc. Phys. Genève 29: 51. 1887.

Phaeographis oscitans (Tuck.) Luch & Lücking, comb. nov. [MycoBank MB 828110] ≡ Graphis oscitans Tuck. in Proc. Amer. Acad. Arts 7: 231. 1868 ≡ Phaeographina oscitans (Tuck.) Zahlbr., Cat. Lich. Univ. 2: 442. 1923.

Phaeographis rhodoplaca (Müll. Arg.) Luch & Lücking, comb. nov. [MycoBank MB 828111] ≡ Phaeographina rhodoplaca Müll. Arg. in Bull. Soc. Roy. Bot. Belgique 32: 157. 1893.

Platygramme kaalensis (Tuck.) Luch & Lücking, comb. & stat. nov. [MycoBank MB 828120] ≡ Graphis discurrens var. kaalensis Tuck. in Proc. Amer. Acad. Arts 7: 230. 1868 ≡ Phaeographis discurrens var. kaalensis (Tuck.) Zahlbr., Cat. Lich. Univ. 2: 371. 1923.

Platygramme tumulata (Nyl.) Luch & Lücking, comb. nov. [MycoBank MB 828112] ≡ Graphis tumulata Nyl. in Ann. Sci. Nat., Bot., sér. 4, 20: 266. 1863 ≡ Phaeographina tumulata (Nyl.) Müll. Arg. in Hedwigia 31: 285. 1892.

Sarcographa dendroides (Leight.) Tabaquero, Bawingan & Lücking, comb. nov. [MycoBank MB 828113] ≡ Platygrapha dendroides Leight. in Trans. Linn. Soc. London 27: 179. 1869 ≡ Phaeographis dendroides (Leight.) Müll. Arg. in Flora 65: 336. 1882.

– “Sarcographa dendroides” Tabaquero & al. in Philipp. J. Syst. Biol. 7: 27. 2013, nom. inval. (Turland & al. 2018: Art. F.5.1).

Table 1.

Species of lirellate Graphidaceae reported from Hawaii (Elix & McCarthy 1998, 2008; Smith 2013), under their traditional classification and with updated nomenclature; origin of the type and presumed world distribution are indicated. Nomenclatural novelties are formally introduced in the Results and Discussion section. Names not included here (e.g. Gyrostomum dactyliferum Zahlbr.) do not belong in Graphidaceae.

Continued