Parmotrema cristiferum (Taylor) Hale (1974a: 335) 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 : 39-41

Parmotrema cristiferum (Taylor) Hale (1974a: 335) MycoBank no. 343031

Parmelia cristifera Taylor (1847: 165) MycoBank no. 120260

Type:— INDIA. West Bengal: Calcutta, s.d., N. Wallich s.n. ( FH [image!], lectotype, designated by Berry 194; BM, n.v., isolectotypes, designated by Krog & Swinscow 1981) .

( Fig. 16 )

Thallus foliose, loosely to moderately adnate, subcoriaceous to coriaceous, up to 18 × 15 cm. Lobes imbricate, irregularly branched, 5–15 mm wide, often concave, frequently ascending when sorediate; apices rounded; margins smooth or sometimes crenate, often undulated, occasionally with black rim ( Fig. 16C ); eciliate, or sometimes lateral lobes sparingly ciliate ( Fig. 16D ), rarely clearly ciliate. Cilia black, simple or 1–2 times branched, up to 1.4 mm long. Upper surface pale yellowish grey, emaculate, rarely faintly punctiform white-maculate, smooth near lobe tips, slightly cracked in older parts, sorediate, lacking schizidia, pustules, dactyls, phyllidia, lobules and isidia. Soralia marginal, linear to labriform, sometimes also submarginal to laminal and then capitate ( Fig. 16D ); very occasionally ciliate. Soredia subgranulose, (30)– 43.5 –(60) µm in diameter (n = 90, from 3 specimens, SD = 6.6 µm). Medulla white, seldom slightly pinkish orange in places. Lower surface smooth, granulate or verruculose in places, sometimes cracked, black and more or less shiny to the margin, or with a shiny, chestnut brown or buff naked marginal zone (ca. 1–10 mm wide), often mottled or fully ivory at the tip of sorediate lobes. Rhizines black, occasionally brownish with pale tip when young, in scattered groups, simple, rarely furcate, short, ca. 0.5 mm long (rarely up to 1 mm). Apothecia not present. Pycnidia rare, submarginal towards apices; only primordia seen. Conidia not found.

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 (major) and consalazinic acids (minor), ± eumitrin A (minor or trace).

Geographical distribution: A pantropical species ( Kurokawa 2006) that extends into several subtropical and temperate areas ( Brodo et al. 2001, Galloway 2007, Jayalal et al. 2013). Widely distributed in the MIOI hotspot, where it has been reported from Madagascar ( Hue 1899, as Parmelia latissima f. cristifera ; des Abbayes 1961; Aptroot 1990), Comoros ( Krempelhuber 1877, as Parmelia hildebrandtii ; Müller 1891, as Parmelia hildebrandtii f. sorediosa ), Seychelles ( Seaward & Aptroot 2009, Diederich et al. 2017), Mauritius ( Taylor 1847, Hale 1965 a, Parnell et al. 1989) and Réunion ( Hue 1899, as Parmelia latissima f. cristifera ; Hale 1965a; van den Boom et al. 2011). In Réunion, P. cristiferum was found in 18 localities in 14 UTM 1× 1 km grid cells (or 10 UTM 2× 2 km grid cells, Fig. 16A ). These localities are located in the windward part of the island, between 10 and 750 m elevation.

Ecology:— Parmotrema cristiferum was corticolous in the 11 most eastern and coastal localities. In the two most western and inland locations, however, the species was saxicolous. When corticolous, it grows preferably on smooth bark, especially that of Pandanus utilis Bory , a tree originating from the Mascarenes ( Bosser & Guého 2003) and regularly planted on the coastline in Réunion ( Blanchard 2000). It seems to favour the coastal lowlands, where more than 80% of the total human population lives ( Strasberg et al. 2005). The species is therefore almost always found in disturbed habitats. The bioclimate of the localities is pluvial tropical, with thermotype belts = lower and upper thermotropical (500 ≤ It ≤ 680) and ombrotype belts = from upper humid to ultrahyperhumid (11.2 ≤ Io ≤ 30.6) ( Fig. 16B ).

The ecology of P. cristiferum in Réunion is rather similar to what has been observed elsewhere: mainly corticolous, more rarely saxicolous ( Elix 1994, Divakar & Upreti 2005, Bungartz & Spielmann 2019). It is common at lower elevation in the Hawaiian Islands ( Smith 1991, 1993) and in India ( Divakar & Upreti 2005), but can also be found at higher elevations in Papua New Guinea ( Louwhoff & Elix 1999) and in Taiwan ( Lai 2001).

Notes: Dodge (1959) described Parmelia sieberi from Mauritius and Madagascar. According to the protologue, this taxon seems morphologically very similar to Parmotrema cristiferum but with ‘margins of the sides of the lobes (…) with an occasional marginal cilium up to 2 mm long’ ( Dodge 1959: 149). Hale (1965a) regarded it as a synonym of P. dilatatum (Vainio) Hale , and later as a synonym of P. cristiferum ( Hale & DePriest 1999) . Krog & Swinscow (1981) examined the holotype of Parmelia sieberi and considered it conspecific with the lectotype of Parmotrema cristiferum . Spielmann & Marcelli (2020), on the other hand, recognised Parmelia sieberi as a species and proposed the new combination Parmotrema sieberi (C.W. Dodge) Spielmann & Marcelli. Their treatment was based on the comparative examination of type collections. According to them, the holotype of P. sieberi differs from the lectotype of P. cristiferum by the presence of cilia (up to 2 mm long) at the margins of the lobes and the absence of eumitrins in the medulla. Of the 21 thalli from Réunion examined, eight (including 974.4637 and 974.4641) are completely devoid of cilia, 12 have less than forty (generally concentrated at the margins of a few lateral lobes), and one (974.4631) has clearly ciliated lobes. The comparison of the ITS sequences of the three specimens (974.4631, 974.4637 and 974.4641) shows that they are identical. Concerning the presence of eumitrin A in the medulla, we detected it in three of the 16 Reunionese specimens that were analysed by TLC. These observations lead us to consider that the presence of cilia at the margin of the lobes and that of eumitrin A in the medulla are two variable characters in P. cristiferum , and we therefore attribute all the Réunion specimens examined to this species.

The morphology and chemistry of Parmotrema stuppeum (Taylor) Hale are very similar to those of P. cristiferum ( Hale 1965a, Krog & Swinscow 1981, Spielmann & Marcelli 2020). However, P. stuppeum generally has more developed cilia and its rhizines are significantly longer: ca. 1mm long (up to 2.5 mm) in the two collections examined (see also Divakar & Upreti 2005, Egan et al. 2016).

Parmotrema cristiferum is part of a poorly supported clade including three other taxa: P. dilatatum , P. robustum (Degel.) Hale and P. cf. clavuliferum . All these species are strongly supported as different by bPP and Stacey analyses ( Fig. 3 ). One GenBank accession (MK722211, from Thailand), identified as P. cristiferum , was resolved as sister to two accessions of P. gardneri (C.W. Dodge) Sérus. with strong support ( Fig. 4 ). The relevant material has not been examined.

Specimens examined:— FRANCE. Réunion: Saint-Benoît, Pointe du Bourbier, elev. 20 m, 21°01’13”S, 55°42’13”E, coastal recreational area with many Pandanus utilis , on bark of P. utilis , 12 August 2013, D. Masson 974.4216 (Hb. DM); ibid., vallée de Grand Fond, elev. 750 m, on lava rock, 06 October 1956, H. des Abbayes s.n. (REN 000041); Saint-Philippe, Ravine Angot, elev. 25 m, 21°21’02”S, 55°47’38”E, anthropized coastal thicket with Casuarina equisetifolia , Pandanus utilis , etc., on bark of a branch of Ficus sp. , 17 August 2013, D. Masson 974.4290 (Hb. DM); ibid., elev. 25 m, 21°21’05”S, 55°47’33”E, anthropized coastal thicket with Casuarina equisetifolia and Pandanus utilis , on bark of a branch of P. utilis , 17 August 2013, D. Masson 974.4291 (Hb. DM); ibid., coast near Petite Vache, elev. 15 m, 21°21’43”S, 55°46’40”E, anthropized coastal thicket, on bark of the trunk of a young Terminalia catappa , 14 August 2015, D. Masson 974.4643 (Hb. DM); ibid., coast near Petite Vache, elev. 15 m, 21°21’46”S, 55°46’38”E, coastal grove of Pandanus utilis , on bark of a branch of P. utilis , 14 August 2015, D. Masson 974.4641 (LG); Sainte-Rose, la Marine, elev. 10 m, 21°07’31”S, 55°47’26”E, anthropized coastal thicket, on bark of the trunk of Pandanus utilis , 15 August 2013, D. Masson 974.4241 (Hb. DM); ibid., elev. 10 m, 21°07’31”S, 55°47’32”E, anthropized coastal thicket, on bark of the trunk of Pandanus utilis , 15 August 2013, D. Masson 974.4243 (Hb. DM); ibid., between Pointe de Sainte-Rose and Bassin des Harengs, elev. 10 m, 21°07’43”S, 55°48’04”E, anthropized coastal thicket with Casuarina equisetifolia and Pandanus utilis , on bark of a branch of P. utilis , 14 August 2015, D. Masson 974.4637 (LG); ibid., Bois Blanc, route forestière 18, elev. 105 m, 21°11’41”S, 55°49’06”E, landscaped park with forestry plantations, on bark at the base of a trunk of an undetermined tree, 13 August 2015, D. Masson 974.4626 (Hb. DM); ibid., elev. 165 m, 21°11’40”S, 55°48’52”E, landscaped park with forestry plantations, on bark of a trunk of an undetermined tree, 13 August 2015, D. Masson 974.4631 (LG); ibid., Bois Blanc, near Quai de Tigo, elev. 25 m, 21°12’18”S, 55°49’24”E, coastal grove of Pandanus utilis , on bark of an adventitious root of P. utilis , 13 August 2015, D. Masson 974.4621 (Hb. DM); ibid., Bois Blanc, near Roche du Pas de Cabri, elev. 20 m, 21°12’08”S, 55°49’29”E, coastal grove of Pandanus utilis , on bark of a branch of P. utilis , 13 August 2015, D. Masson 974.4624 (Hb. DM); ibid., Pointe Rouge, elev. 30 m, 21°10’30”S, 55°49’58”E, anthropized coastal grove with Casuarina equisetifolia , Pandanus utilis , etc., on bark of a branch of an undetermined tree, 13 August 2013, D. Masson 974.4229 (Hb. DM); ibid., les Cascades, elev. 30 m, 21°11’07”S, 55°49’52”E, anthropized coastal thicket, on bark of the trunk of an undetermined tree, 13 August 2013, D. Masson 974.4218 (Hb. DM); ibid., les Cascades, elev. 20 m, 21°11’05”S, 55°50’01”E, anthropized coastal grove with Casuarina equisetifolia and Pandanus utilis , on bark of a trunk of P. utilis , 13 August 2013, D. Masson 974.4224 (Hb. DM); ibid., les Cascades, elev. 20 m, 21°10’51”S, 55°50’06”E, anthropized coastal grove with Casuarina equisetifolia and Pandanus utilis , on bark of a branch of P. utilis , 13 August 2013, D. Masson 974.4226 (REU), 974.4227 (Hb. DM); ibid., les Cascades, elev. 10 m, coastal area with Pandanus trees, on Pandanus , 30 May 2008, P. & B. van den Boom 40147 ( Hb. van den Boom); Salazie, between Mare à Citrons and Mare à vieille Place, roadside D52, elev. 690 m, 21°02’00”S, 55°31’22”E, cultivated area (mainly sugar cane), on a large exposed block of volcanic breccia, 14 April 2003, D. Masson 974.0432 (Hb. DM).

Specimens studied for comparison:

Parmotrema cristiferum .— FRANCE. Guadeloupe: Vieux-Habitants, Grande Rivière valley, elev. 400 m, degraded mesophilous forest, corticolous, 15 November 1989, J. Vivant 24 (Hb. DM); ibid., Marigot, Rivière de Beaugendre valley , elev. 150–200 m, degraded mesophilous forest with cocoa and coffee plantations, on isolated dead tree trunks near the stream, December 1988, J. Vivant 76 (Hb. DM) .

Parmotrema stuppeum .— FRANCE. Pyrénées-Atlantiques: Alçay-Alçabéhéty-Sunharette, vallon d’Azaléguy, elev. 445 m, 43°04’53”N, 0°59’35”W, wooded valley with Fagus , Fraxinus and Acer , on bark of a fallen branch of Fagus , 18 May 2007, D. Masson 64.2449 (Hb. DM); ibid.: Musculdy, vallon de la Bidouze, elev. 370 m, 43°08’29”N, 1°01’25”W, on the boundary of a riparian forest and a beech forest, on mossy bark of a fallen branch of Fagus , 26 April 2005, D. Masson 64.1317 (Hb. DM).

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 16. Parmotrema cristiferum. 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 974.4243); D: Sparingly ciliate sorediate lobes with marginal linear and submarginal ± capitate soralia (Masson 974.4631). Scale bars: A = 10 km; C = 10 mm; D = 4 mm.