Parmotrema cf. clavuliferum (Räsänen) Streimann (1986: 93) MycoBank

Masson, Didier, Magain, Nicolas & Sérusiaux, Emmanuël, 2024, Small island but great diversity: thirty six species of Parmotrema (Parmeliaceae, lichenized Ascomycota), including sixteen new species, on Réunion (Mascarenes), with additional data from the Western Indian Ocean, Phytotaxa 657 (1), pp. 1-138 : 29-32

Parmotrema cf. clavuliferum (Räsänen) Streimann (1986: 93) MycoBank no 129346

Parmelia clavulifera Räsänen (1944: 4) MycoBank no 368556

Type:— FRANCE. Tahiti, ad corticem arboris, 1868, Dr. med . Bouffon vel E. Vieillard (H, n.v., lectotype; designated by Hale & Fletcher 1990)

≡ Rimelia clavulifera (Räsänen) Kurok. (1991: 158) MycoBank no. 128246

( Fig. 12 )

Thallus foliose, loosely to moderately adnate, membranaceous to subcoriaceous, up to 18 × 9 cm. Lobes irregular, contiguous to imbricate, irregularly branched, 2–10 mm wide, ± rounded axils, round to subtruncate apices; margins dentate to laciniate, ± ciliate ( Fig. 12C ). Cilia black, rare to abundant at the margin of the peripheral lobes, rare at the margin of the central sorediate lobes; simple, rarely slightly squarrose, up to 2.5 mm long. Upper surface pale greenish grey, ± conspicuously reticulate white-maculate, occasionally hypermaculate (sensu Spielmann & Marcelli 2020), ± finely reticulate cracked along the maculae; sorediate, very rarely sorediate-isidiate, lacking schizidia, pustules, dactyls and phyllidia. Soralia mainly capitate at the apex of laciniae ( Fig. 12D ), sometimes spreading marginally and/or submarginally. Soredia subgranulose, (30)– 44,5 –(70) µm in diameter (n = 120, from 4 specimens, SD = 7.2 µm). Isidia normally absent, but some present on two thalli from the same high elevation locality (no. 974.0234 and 974.0235), marginal and submarginal, simple, cylindrical to inflated, brown tipped, sometimes laterally ciliate, rapidly dissolving into soredia. Laciniae common, marginal, initially flat, ± dichotomously branched, then frequently developing digitate expansions soon bearing ± globose soralia; up to 7 mm long, 0.5–2 mm wide, ciliate or not. Lobules occasional, marginal, up to 2 × 2 mm, ciliate or not. Medulla white throughout, occasionally orange-tinged due to the alteration of salazinic acid. Lower surface smooth to punctate, ± shiny, duller in the central part, black to the margin, or with a brown marginal zone (ca. 1–4 mm wide), often mottled or fully ivory white at the tip of sorediate lobes and laciniae ( Fig. 12D ). Rhizines black, numerous, ± evenly distributed, often extending to lobe margins, simple, rarely ± squarrosely-branched, up to 2 mm long. Apothecia rather rare (fertile thalli found in four localities), submarginal, more rarely laminal, sessile to shortly stipitate, up to 10 mm in diameter, disc perforate or imperforate, margin crenate and soon sorediate. Ascospores (13)13.5– 15.8 –(18) × (7.5)– 9.1 –(10) µm, Q =(1.40)– 1.75 –(2.13,) epispore (1)–(1.5) µm thick, n = 30, from a single specimen (no. 974.4857). Pycnidia submarginal towards apices, black. Conidia not found (20 pycnidia investigated).

Chemistry:— Spot tests and fluorescence: upper cortex K+ yellow, UV−; medulla K+ yellow then dark red, C−, P+ orange, UV−. Secondary metabolites ( TLC): upper cortex with atranorin and chloroatranorin; medulla with salazinic acid (major) and consalazinic acid (minor).

Geographical distribution:—It is difficult to properly determine the global distribution of this lichen due to the uncertainty of its taxonomic status. Kurokawa (2006) considered it as a pantemperate element. It seems to be widespread in Asia (e.g. Breuβ & Brunnbauer 1997, Moon et al. 2000, Kurokawa & Lai 2001, Aptroot & Sparrius 2006, Ahn & Moon 2016, Bawingan et al. 2017), but it is also reported from Pacific islands ( Kurokawa 1979, Elix 2001b, Moon et al. 2001, Bungartz & Spielmann 2019), Australia ( Elix 2001a), Central Africa ( Killmann & Fischer 2005), Europe ( Ahn & Moon 2016), as well as South America ( Benatti & Marcelli 2008, Spielmann & Marcelli 2009).

Concerning Madagascar, the material published by des Abbayes (1961) under the name Parmelia reticulata var. corniculata Abbayes may refer to Parmotrema clavuliferum , but we could not examine the specimens. On the other hand, we checked three collections made by J. Bosser, including two from the same localities as those cited by des Abbayes, whose thallus morphology is consistent with P. clavuliferum . In Réunion, eleven localities, in 10 UTM 1× 1 km grid cells (or 10 UTM 2× 2 km grid cells, Fig. 12A ), are known to host this taxon. They are distributed in both the Piton des Neiges and Piton de la Fournaise massifs, between 1330 and 2180 m in elevation.

Ecology:—On Réunion, Parmotrema cf. clavuliferum was found in cloud forests (windward and leeward montane rainforests, Acacia montane forest) and subalpine shrubland. It grows on trees ( Acacia heterophylla Willd. , Dombeya sp. ), shrubs ( Erica reunionensis E.G.H. Oliv. , Hubertia ambavilla Bory ), tree fern ( Cyathea glauca ), or volcanic rocks. When growing on trees, it was collected significantly more frequently on branches than on trunks (eight collections on branches, none on trunks, Fisher’s exact test, P = 0.038). The bioclimate of the localities ( Fig. 12B ) is pluvial tropical, with thermotype belts = from lower mesotropical to lower supratropical (294 ≤ It ≤ 470) and ombrotype belts = from lower humid to ultrahyperhumid (8.8 ≤ Io ≤ 38.8). On Réunion, P. cf. clavuliferum appears hardly thermophilous, clearly ombrophilous, and probably rather photophilous. Its elevational distribution is quite comparable to that observed in Thailand ( Moon et al. 2000) and in Taiwan ( Lai 2001), but in Hawaiian ( Moon et al. 2001) and Galapagos Islands ( Bungartz & Spielmann 2019), the species also occurs in the lowlands.

Notes:—With its upper surface strongly reticulate maculate, the presence of soralia, and a medulla with salazinic acid as major extrolite, Parmotrema clavuliferum belongs to the P.reticulatum aggr. Within this complex, P. clavuliferum has a controversial status. On the basis of phenotypic traits (capitate soralia on short laciniae, black mottled white lower surface below the sorediate lobes), it was either considered to be a distinct species (e.g. Kurokawa 1979; Moon et al. 2001; Elix 2001a, b; Benatti & Marcelli 2008; Spielmann & Marcelli 2009) or it was synonymized with P. reticulatum (Taylor) M. Choisy (e.g. Awasthi 1976, Hale & Fletcher 1990, Divakar & Upreti 2005). Recent molecular phylogenetic studies produced somewhat contradictory results. In the study by Divakar et al. (2005a), specimens of P. clavuliferum morphology and those of P. reticulatum morphology did not form two independent monophyletic groups. In Ahn & Moon (2016), specimens of P. clavuliferum morphology formed a well-supported monophyletic group while those of P. reticulatum morphology split into three clades. On the other hand, Del-Prado et al. (2011, 2016) showed that their sampled specimens of the P. reticulatum aggr. (without distinction of P. clavuliferum ) belonged to at least eight distinct species-level lineages. In our phylogenetic tree based on ITS sequences ( Fig. 4 ), nine specimens of the P. reticulatum aggr. from Réunion were recovered in two groups: seven were mixed with samples belonging to ‘species 2’ of Del-Prado et al. (2016), and two (no. 974.4027 and 974.4857) with samples belonging to their ‘species 3’ [= clade A 2 in Del-Prado et al. (2011)], as well as the specimens identified as P. clavuliferum by Ahn & Moon (2016). Furthermore, our phylogenetic tree based on 3-locus and the Stacey and bPP analyses show that these two groups are clearly distinct ( Fig. 3 ). Our two specimens from ‘species 3’ share the white, or mottled white, zone on the lower surface at the tip of numerous sorediate laciniae or lobes, a diagnostic character of P. clavuliferum according to Kurokawa (1979), Moon et al. (2001), Kurokawa & Lai (2001), Ahn & Moon (2016) and Spielmann & Marcelli (2020). The seven specimens of the ‘species 2’ group, on the other hand, have a black or brown marginal underside, the ivory-white mottled areas being totally absent or, very rarely, sporadic under some lobes. We did not find any clear differences in the location and morphology of the soralia between these two groups. Therefore, and pending a thorough taxonomic study of the P. reticulatum aggr., we assign all Reunionese specimens of this complex with numerous sorediate lobes (or lacinia) mottled white on the lower surface to P. cf. clavuliferum .

Specimens with molecular data examined:— FRANCE. Réunion: Le Tampon, le Volcan, près du rempart de la Rivière des Remparts, entre le Nez de Boeuf et le Piton de Sable, ca. 2070 m, 21°11’52”S, 55°37’37”E, recreational area in subalpine shrubland with Sophora denudata and Hypericum lanceolatum , on vertical face of a volcanic rock, 24 August 2015, D. Masson 974.4857 (LG); Sainte-Rose, sentier du Fond de la Rivière de l’Est, elev. 1805 m, 21°12’22”S, 55°41’34”E, in grazed Acacia montane forest, in overall NNE orientation, on bark of a branch of Acacia heterophylla , 25 August 2012, D. Masson 974.4027 (LG).

Specimens with no molecular data examined:— FRANCE. Réunion: La Possession, la Grande Montagne , sentier des Lataniers, près du Piton Ravine à Marquet, elev. 1330 m, 20°58’13”S, 55°23’38”E, in leeward montane rainforest, in an overall NW orientation, on bark of a branch of Erica reunionensis , 19 August 2015, D. Masson 974.4739 (Hb. DM); Saint-Benoît, Piton de Bébour, elev. 1390 m, 21°07’33”S, 55°33’52”E, in windward montane rainforest, on bark of a dead branch fallen from an undetermined tree, 07 April 2003, D. Masson 974.0013 (REU), 974.0024, 974.5224 (Hb. DM); ibid., forêt de Bébour, small paved road from the main road to Échelles (Takamaka), elev. 1370 m, in windward montane rainforest, on Dombeya sp. , 08 June 2008, P. & B. van den Boom 40897 ( Hb. van den Boom); Saint-Denis, Plaine d’Affouches, elev. 1710 m, 20°59’15”S, 55°25’58”E, in Acacia montane forest, at the base of a stipe of Cyathea glauca , 18 August 2012, D. Masson 974.3890 (Hb. DM); Saint-Joseph, haut de la forêt de la Crête, elev. 2010 m, 21°17’37”S, 55°41’04”E, in Acacia montane forest, in an overall SSW orientation, on bark of a branch of Acacia heterophylla , 23 August 2012, D. Masson 974.3991 (Hb. DM); ibid., le Petit Mapou, sentier de la Rivière des Remparts, elev. 1700 m, 21°12’01”S, 55°37’54”E, in windward montane rainforest, in an overall SSE orientation, on bark of a branch of Acacia heterophylla , 24 August 2015, D. Masson 974.4852 (Hb. DM); Saint-Paul, Le Maïdo, elev. 2180 m, 21°04’18”S, 55°23’14”E, in subalpine shrubland, on volcanic rocks and on the bark of a stunted Acacia heterophylla , 10 April 2003, D. Masson 974.0225 (REU), 974.0234, 974.0235 (Hb. DM); Sainte-Marie, Plaine des Fougères, entre la Ravine Sèche et la Ravine Mère Canal, elev. 1275 m, 20°58’42”S, 55°30’58”E, in windward montane rainforest, in an overall NE orientation, on mossy bark of Hubertia ambavilla , 30 August 2012, D. Masson 974.5229 (Hb. DM); Salazie, Bélouve, sentier de l’École Normale, elev. 1470 m, 21°04’04”S, 55°33’07”E, in managed Acacia montane forest, on bark of a branch of Acacia heterophylla , 24 August 2012, D. Masson 974.4008 (Hb. DM).

MADAGASCAR. Analamanga : environs de Tananarive, PK 26 de la route de Tamatave, Ambatovory, sur rocher dans une plantation d’ Eucalyptus , April 1957, J. Bosser 11011 ( REN 000081 ) ; Tananarive , Tsimbazaza, elev. 1300 m, sur rocher ensoleillé, April 1959, J. Bosser 12709 ( REN 000089 ) . Vakinankaratra : Ankaratra, Manjakatompo, elev. 2200 m, en lisière de forêt ombrophile d’altitude, sur tronc, 1957, J. Bosser 10713 ( REN 000082 ) .

Figures

FIGURE 3. Phylogeny of the Parmotrema species studied. Best ML tree resulted from a RaxML analysis of three loci (EF1-α, ITS, mtSSU) and 102 specimens. Punctelia toxodes was selected as the outgroup. Bootstrap values are represented above the branches, and thick branches have bootstrap support value ≥ 70. Results of the species delimitation analyses are summarized to the right of the terminal labels of the tree. The first column corresponds to the results of the Stacey analysis, while the second column corresponds to the results of the bPP analysis. Specimens attributed the same colour were reconstructed as part of the same putative species by the species delimitation analysis. Major medullary extrolites are also shown for each specimen.

FIGURE 4. Global tree (best scoring maximum likelihood tree) of Parmotrema based on the fungal ITS barcoding marker. Figure can be enlarged for a better reading of labels. Accessions in black are those retrieved from GenBank on June 2023. Those in red are those produced by the authors for this study. Bootstrap support is indicated on branch when ≥ 70%.

FIGURE 12. Parmotrema cf. clavuliferum. A: Distribution on Réunion (UTM 2×2 km grid system); B: Bioclimatic characteristics of collection sites (abbreviations and threshold values for thermotype and ombrotype horizons from Rivas-Martínez et al. 2011: 17–18); C: Gross morphology of thallus (Masson 974.4027); D: Sorediate lobes with soralia mainly capitate at the apex of laciniae, and lower surface with ivory-white marginal zone (Masson 974.4027). Scale bars: A = 10 km; C = 10 mm; D = 5 mm.