Parmotrema nemorum D.M. Masson, Magain & Sérus., 2024

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 : 69-72

Parmotrema nemorum D.M. Masson, Magain & Sérus. , sp. nov. MycoBank no. 853873

Diagnosis. Similar to Parmotrema amaniense (J. Steiner & Zahlbr.) Krog & Swinscow , but differs by the constant presence of protolichesterinic acid in addition to alectoronic and protocetraric acids as major medullary extrolites, the amphithecium developing prominent veins with coarse isidioid structures, the occasional presence of laminal isidia, and the occasional occurrence of a reddish purple pigment in the medulla.

Holotype:— FRANCE. Réunion: Sainte-Rose, Bois Blanc , route forestière 18, elev. 185 m, 21°11’40”S, 55°48’47”E, landscaped lowland rainforest with tree plantations and recreation areas, on bark of a trunk of an unidentified tree, 13 August 2015, D. Masson 974.4634 (MNHN-PC-PC0088076).

GenBank accession numbers: ITS ( PP 840447), mtSSU ( PP 842572), EF1-α ( PP 852834).

( Fig. 28 )

Thallus foliose, loosely to moderately adnate, subcoriaceous to coriaceous, up to 28 cm long, 20 cm wide. Lobes irregular, contiguous or imbricate, apices ± rounded, 5–18 mm wide, lateral lobes often ± revolute to somewhat erect and partly convolute; margins sinuate or crenate, rarely dentate, laciniate or lobulate, ciliate ( Fig. 28E ), occasionally tinged with a reddish purple pigment. Cilia always present but with variable density and ± irregular distribution at the lobes margins, also occasionally laminal or on isidioid protuberances of the amphithecium, black, very often with coppery red glints (pigments), simple, rarely 1–(2) times branched, ca. 0.04–0.10 mm in diameter at the base, up to 3.5 mm long. Upper surface pale yellowish grey centrally, more greenish towards the periphery, ± dull, more shiny towards lobe tips, generally emaculate, rarely faintly white-maculate, maculation more conspicuous near apothecia, smooth to rugose, occasionally isidiate, lacking schizidia, pustules, dactyls, soralia. Isidia present in 7 of the 12 thalli examined, laminal or submarginal, irregularly distributed, never abundant, granular, verrucose, ± cylindrical or flattened, rather stout, simple, often apically ciliate or with pycnidia, up to 1 mm high ( Fig. 28D ). Laciniae rare, marginal, up to 0.5 × 1 mm. Lobules occasional, marginal or laminal, ciliate, up to 3.5 × 4.5 mm. Medulla usually white throughout, but may be tinged with a reddish purple pigment (K+ purple), especially when exposed. Lower surface smooth or rugulose, dull, shinier towards the periphery; black to the margin, or with a buff erhizinate marginal zone (ca. 1–8 mm wide) at main lobe tips, lateral lobes sometimes with an erhizinate, ivory white or cream- mottled marginal zone (1–4 mm wide); often becoming ivory or cream under apothecia. Rhizines sparse, in ± scattered groups, concolor to the lower surface, simple or fasciculate, rarely 1–2 times branched, up to 2 mm long, generally rather stout, exceptionally some at the periphery are slender and copper-red pigmented like cilia. Apothecia quite common, submarginal, on swollen stipes becoming ± constricted with age, or at the tip of convoluted and erect lateral lobes, first concave, then flattening with age, up to 20 mm in diameter; disc imperforate, orange brown; amphithecium and stipe strongly white-maculate, developing a network of ± prominent and anastomosing veins with coarse, irregular, ± flattened, and ± branched isidioid protuberances (up to 2.5 mm long) quite often bearing cilia and/or pycnidia ( Fig. 28C ); thalline margin dentate to fringed with isidioid protuberances or lobules, sometimes with cilia and/or pycnidia; hymenium s. lat. (82)– 89.0 –(102) µm high, proper exciple with hyaline layer (4)– 6.1 –(9) µm high, intermediate layer (18)– 23.2 –(27) µm high, cortex-like basal layer (22)– 26.9 –(35) µm high. Ascospores 8 per ascus, simple, colourless, ellipsoidal, (22)22.5– 25.6 –29(30) × 11– 13.7 –16.5(19) µm, Q = (1.37)1.53– 1.89 –2.25(2.42), epispore (2)– 2.7 –(3.5) µm thick, n = 240, from 8 thalli, mean values for each thallus: 24.7 × 12.6, 24.8 × 12.9, 25.1 × 13.5, 25.4 × 13.3, 25.4 × 13.5, 26.3 × 13.6, 26.3 × 16.3, 26.8 × 13.7 µm. Pycnidia common, mostly submarginal on lobes, black. Conidia clearly sublageniform 5–7 × ca. 1 µm. Upper cortex palisade plectenchymatous, not fragile, (15)– 21.9 –(32) µm thick. Algal layer continuous, (15)– 18.3 –(20) µm thick. Medulla (140)– 149.3 –(162) µm thick. Lower cortex prosoplectenchymatous, (15)– 16.1– (18) µm thick.

Chemistry:— Spot tests and fluorescence: upper cortex K+ yellow, UV−; medulla K−, C−, KC + fleeting purple pink, then pink-orange, P+ orange, UV+ blue-white, pigmented medulla and cilia K+ purple. Secondary metabolites ( TLC): upper cortex with atranorin and chloroatranorin; medulla with alectoronic acid (major), protocetraric acid (major), protolichesterinic acid (major), lichesterinic acid (minor), ± α-collatolic acid (minor/trace), ± an undetermined pink-purple pigment: P1; ± 1–2 undetermined ciliary pigments: P1, O1.

Etymology: — From the Latin nemus: forest with glade or pasture. The specific epithet refers to the open woodlands where the taxon was found.

Geographical distribution:—So far only known with certainty from Réunion. The oldest collection dates to 1840, and since then, Parmotrema nemorum has been found at four localities in four UTM 1× 1 km grid cells (or four UTM 2× 2 km grid cells, Fig. 28A ). The recent occurences were clustered in two low elevation areas (155–380 m), on the northeastern and southern slopes of the Piton de la Fournaise massif. However, it is quite possible that the species is more widespread in the windward zone, as potential habitats (lowland parks, vanilla plantations or wooded gardens), often with private access, have been under-prospected.

This lichen may also exist in Mauritius. Indeed, in addition to the thallus collected in 1840 on Réunion by Lepervenche-Mézières, and examined by us, Hue (1899: 197) cited, under the name Parmelia proboscidea Tayl. in Mack., a specimen from the Bory de Saint-Vincent herbarium (PC) collected on Mauritius in the year X [French Republican calendar; probably between December 1801 and March 1802, during Bory’s second stay on Mauritius ( Bory de Saint-Vincent 1804)], and which could also belong to P. nemorum . However, it has not been possible to examine it.

Ecology:— Parmotrema nemorum typically grows on the rather well-lit bark of tree trunks and branches in secondary lowland rainforests. It is a thermophilous and ombrophilous lichen, as shown by the bioclimatic characteristics of its localities: bioclimate pluvial tropical, with thermotype belt = lower thermotropical (600 ≤ It ≤ 620) and ombrotype belts = from lower to upper hyperhumid (14.5 ≤ Io ≤ 19.7) ( Fig. 28B ). Its ecology appears to be broadly similar to that of P. odontatum , and both taxa can occur at the same locality.

Notes:—According to our molecular analyses using three loci, Parmotrema nemorum constitutes a well-supported clade, phylogenetically close to that of P. subdeflectens , but quite distinct ( Fig. 3 ). To our knowledge, these two new Parmotrema species are the only ones whose medulla contains the combination of protocetraric, alectoronic and protolichesterinic acids as major extrolites. Parmotrema subdeflectens is a sorediate taxon, whereas P. nemorum is commonly fertile with, occasionally, some isidia-like outgrowths ( Fig. 28D ), most likely not functioning as vegetative propagules. In the current state of knowledge, the distribution and ecology of these two lichens appear to be quite distinct. Parmotrema nemorum is confined to the Piton de la Fournaise massif at low elevations (<400 m), in hot and very humid localities, while P. subdeflectens is confined to the Piton des Neiges massif at higher elevations (> 1000 m), in cooler and drier localities.

Two sexually reproducing species are phenotypically close to P. nemorum : P. amaniense , described from Tanzania ( Zahlbruckner 1926), and P. pachysporum (Hale) Hale , described from Angola ( Hale 1965a) ( Table 8). According to their broad concept of P. amaniense, Krog & Swinscow (1981) reduced P. pachysporum to synonymy with P. amaniense . However, P. pachysporum differs from both P. amaniense and P. nemorum by the longer ascospores, the type of conidia, and the medullary chemistry. Parmotrema nemorum differs from P. amaniense s. str. by its tendency to develop isidia-like protuberances, that are often ciliate, on the surface of the amphithecium and, to a lesser extent, on the upper surface of the lobes. In addition, its medullary chemistry is distinctive in that it includes protocetraric, alectoronic and protolichesterinic acids as constant major substances, as well as an accessory reddish purple pigment (also often present on cilia).A thallus from the type collection of P. amaniense (W-1909/8386) that we could examine has some cilia with reddish pigmentation, but the medulla is entirely white. No author, to our knowledge, has reported any medullary pigmentation in the P. amaniense group. Another similar taxon, but with protocetraric and protolichesterinic acids in the medulla, was included as a chemotype in Krog & Swinscow’s concept of P. amaniense . It was cited from Tanzania and Uganda by Krog & Swinscow (1981) and Alstrup et al. (2010). We found a collection from Rwanda and one from Tanzania that could correspond to it. However, the conidia are clearly sublageniform (6–7 µm long) in the first, and bacilliform (rarely weakly sublageniform, 7–9 µm long) in the second. The specimens from Papua New Guinea cited by Louwhoff & Elix (1999) under the name P. elacinulatum (Kurok.) Streimann (including P. submerrillii Elix in the opinion of these two authors) also seem to fit with this taxon. According to Louwhoff & Elix (1999), these specimens contain protocetraric, protolichesterinic and lichesterinic acids as major medullary substances. However, in the protologues of Parmelia elacinulata and Parmotrema submerillii, Kurokawa (1979) and Elix (1993) report only protocetraric acid in the medulla, without any mention of fatty acids. We examined a specimen of P. submerrillii , collected near the type locality, which also contained only protocetraric acid in the medulla. The other phenotypic characters match the diagnosis of P. submerillii perfectly, including the 5–6 µm long sublageniform conidia [and not the conidia ‘bacilliform, 6–7 × 1 µm’ cited by Elix (1998) and Louwhoff & Elix (1999)]. Interestingly, we found the undetermined pigment PV in the cilia of this Australian specimen. This overview, albeit not complete, of the P. amaniense group shows that we can only hope to make progress in our understanding of this complex by acquiring molecular data on each of its representatives, and by analysing them globally.

On Réunion, P. nemorum can be confused with P. odontatum , an equally large and fertile species that shares the same distribution and ecology, and displays a similar morphology. However, P. nemorum can be differentiated by the presence of marginal cilia, the outgrowths often present on the amphithecium, the stipes of the young apothecia that are swollen and not constricted, the larger ascospores with wider epispore, and the occurrence in the medulla of alectoronic and protolichesterinic acids in addition to protocetraric acid, as well as an occasional reddish purple pigment.

Specimens examined:— FRANCE. Réunion: without locality, 1840, M.E. Mézières de Lépervanche 7 ( PC 0009290 ) ; Saint-Philippe, Basse Vallée , route forestière 36, elev. 265–280 m, 21°21’29–34”S, 55°42’24–28”E, roadside in a secondary lowland rainforest with vanilla plantations, in an overall SE orientation, on bark of trunk and a dead branch of unidentified trees, 16 August 2013 & 15 August 2015, D. Masson 974.4287 ( LG) , 974.4654 (Hb. DM); ibid., elev. 310–350 m, 21°21’14–22”S, 55°42’19–24”E, roadside in a secondary lowland rainforest with vanilla plantations, in an overall SE orientation, on bark of trunks and a branch of unidentified trees, 16 August 2013 & 15 August 2015, D. Masson 974.4285 ( REU) , 974.4650, 974.4653 ( Hb. DM), 974.4652 ( LG) ; ibid., elev. 380 m, 21°21’09”S, 55°42’15”E, roadside in a secondary lowland rainforest with vanilla plantations, in an overall SE orientation, on bark of the trunk of a young unidentified tree, 15 August 2015, D. Masson 974.4649 (Hb. DM) ; Sainte-Rose, Bois Blanc , route forestière 18, elev. 155–185 m, 21°11’39–41”S, 55°48’47–53”E, landscaped lowland rainforest with tree plantations and recreation areas, on bark of trunks of unidentified trees, 13 August 2015, D. Masson 974.4628 ( REU) , 974.4630, 974.4633 ( Hb. DM), 974.4635 ( LG) .

Specimens studied for comparison:

Parmotrema amaniense — TANZANIA. Ost-Usambara , Amani , 800 m, im Regenwald, an Stämmen häufig, July 1909, Brunnthaler s.n. (W, type collection) .

Parmotrema amaniense s. lat. [with protocetraric and protolichesterinic acids]— RWANDA. Forêt de Rugege , entre Garamba et la plantation de Gisakura, ca. 1900 m, lisière de la forêt de montagne ± secondarisée, en bordure d’un défrichement de fond de vallon, branche tombée, 1 September 1974, J. Lambinon 74/1039 ( LG) .

TANZANIA. Tanga: Amani, Usambara Mts, Karimi Estate (road towards Monga), elev. 800–900 m, 5°07’S, 38°37’E, on Grevillea along a road, 10 January 1971, R. Moberg 1485b ( UPS) .

Parmotrema pachysporum s. str. — ANGOLA. Huila : Sá da Bandeira [= Lubango], c. 10 km N of the town, elev. 2000 m, Brachystegia (etc.) forest by the road, on trees, 03 February 1960, G. Degelius s.n. ( UPS, holotype) .

Parmotrema submerrillii .— AUSTRALIA. Queensland: Paluma village, Palluma Range , 40 km S of Ingham, elev. 830 m, 19°01’S, 146°13’E, regrowth on old quarry site, on semi-shaded treelet stem ( Sloanea ), 27 October 1995, H. Streimann 57903 (B) .

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 28. Parmotrema nemorum. 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: Amphithecium of a mature apothecium developing prominent and anastomosing veins with coarse and ciliate isidioid structures (holotype); D: Submarginal isidia, ± cylindrical or flattened, rather stout, simple, often with pycnidia, some apically ciliate (holotype); E: Gross morphology of thallus (Masson 974.4635). Scale bars:A = 10 km; C = 4 mm; D = 1 mm; E = 20 mm.