Parmotrema reticulatum, (Taylor) M. Choisy, 1952

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 : 90-94

Parmotrema reticulatum aggr. (Taylor) M. Choisy (1952: 175) MycoBank no. 357464

Parmelia reticulata Taylor (1836: 148) MycoBank no. 398165

Type:— IRELAND. Kerry County, near Dunkerron, s.d., T. Taylor s.n. ( FH, n.v., lectotype; BM, n.v., isolectotype; designated by Hale & Flechter 1990) .

≡ Rimelia reticulata (Taylor) Hale & A. Flechter (1990: 28) MycoBank no. 102567

= Parmelia acanthifolia fo. ornata Hue (1899: 171) MycoBank no. 458871

Type:— FRANCE. La Réunion: Salazie, 1889, frère Rodriguez s.n. ( PC, n.v., lectotype; designated by Hale & Flechter 1990) .

( Fig. 35 )

Morphological description, chemistry and ecology based on genetically analysed material from Réunion (seven collections). Additional information from non-genetically analysed Reunionese specimens is provided in square brackets.

Thallus foliose, loosely to moderately adnate, membranaceous to subcoriaceous, up to 14 × 11 cm. Lobes irregular, contiguous to imbricate, irregularly branched, 3–9 mm wide, ± rounded axils, round to subtruncate apices; margins crenate to laciniate, ± ciliate ( Fig. 35D ). Cilia black, rare to numerous, simple or ± squarrose, up to 2.5 mm long. Upper surface pale greenish grey, ± conspicuously reticulate white-maculate to hypermaculate, ± finely reticulate cracked along the maculae; sorediate, lacking isidia, schizidia, pustules, dactyls and phyllidia. Soralia variable, capitate at the tip of laciniae, submarginal ± linear at the apex of revolute lobes ( Fig. 35F ), sometimes also subcapitate laminal. Soredia subgranulose to granulose, (35)– 47.4 –(70) µm in diameter (n = 210, from 7 specimens, SD = 7.1 µm). Laciniae ± numerous, ± developed, marginal, flat, sometimes ± dichotomously branched, frequently bearing terminal globose soralia; generally short, but up to 8 mm long, 0.4–2 mm wide. Lobules occasional, marginal, up to 1.5 × 2 mm. Medulla white throughout, occasionally orange-tinged due to the alteration of salazinic acid. Lower surface smooth or punctate, rarely rugulose, ± shiny, duller in the central part, black to the margin, or with a brown marginal zone (ca. 0.5–4 mm wide), occasionally a little white mottled under some rare sorediate lobes. Rhizines black, numerous, ± evenly distributed, often extending to lobe margins, simple or ± squarrosely-branched, up to 2.5 mm long. Apothecia rather rare, submarginal, shortly stipitate, up to 16 mm in diameter, disc perforate or imperforate, margin ± crenate and soon sorediate, amphithecium smooth to rugose, ± sorediate ( Fig. 35E ). Ascospores (11)12– 14.1 –(17) × (7)– 8.9 –(11) µm, Q =(1.20)– 1.59 –(2.00), epispore (1)–(1.5) µm thick, n = 60, from two specimens, mean values for each thallus: 14.1 × 9.4, 14.2 × 8.5 µm [(10)11– 14.7 –18(19) × (6)– 8.9 –11(12) µm, Q =(1.14)– 1.67 –(2.69), epispore (1)–(1.5) µm thick, n = 210, from seven specimens, mean values for each thallus: 12.3 × 8.8, 13.7 × 6.9, 14.6 × 9.9, 15.0 × 8.7, 15.1 × 9.3, 15.2 × 9.8, 16.9 × 9.3 µm]. Pycnidia submarginal towards apices, black. Conidia filiform 8–12 × ca. 1 µm.

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:—The Parmotrema reticulatum aggregate is widespread in tropical and temperate areas ( Elix 1994), reaching latitudes of 58° N and 55° S ( GBIF 2023b). In the MIOI hotspot, it has been reported from Madagascar ( Vainio 1898, Hue 1899, Dodge 1959, des Abbayes 1961, Aptroot 1990), Comoros ( Lindau 1908), Mauritius ( Dodge 1959, David & Hawksworth 1995, Diederich & Ertz 2020) and Réunion ( Hue 1899, des Abbayes 1961, van den Boom et al. 2011). In the phylogenetic tree based on ITS sequences ( Fig. 4 ), the seven Reunionese specimens all grouped in the ‘species 2’ clade of Del-Prado et al. (2016), which also includes specimens from Spain, Portugal, the Canary Islands, Morocco, Mozambique, Kenya, India, China, Japan, and Australia ( Del-Prado et al. 2016). These seven molecularly analysed specimens come from seven localities in seven UTM 1× 1 km grid cells (or six UTM 2× 2 km grid cells, Fig. 35A ), at elevations ranging from 25 to 1930 m. Additional specimens examined with no molecular data were collected between 15 and 2325 m elevation, in 36 additional UTM 1× 1 km grid cells (or 31 UTM 2× 2 km grid cells, Fig. 35B ). Representatives of the P. reticulatum aggr. are frequently encountered in the field on Réunion, and it is clear that they have been under-collected overall.

Ecology:—The seven thalli molecularly analysed were all epiphytic [occasionally also saxicolous on volcanic rocks for the other thalli]. They developed on mosses (growing on bark) and on bark of trunks and branches of various native trees and shrubs belonging to the genera Acacia , Dombeya , Erica , Ficus , Hubertia , and Pandanus [also Hypericum , Monimia , Sophora , as well as the introduced Cryptomeria and Terminalia ]. In connection with the high elevational range, the habitats are diverse: coastal thicket, lowland dry forest, windward and leeward montane rainforests, and Acacia montane forest [also lowland rainforest, submontane mesic forest, subalpine shrubland, subalpine Sophora thicket]. Bioclimatic features of the localities are also varied ( Fig. 35C ): bioclimates = pluviseasonal tropical and pluvial tropical, thermotype belts = from lower thermotropical to lower supratropical (305 ≤ It ≤ 671), ombrotype belts = from upper subhumid to ultrahyperhumid (5.7 ≤ Io ≤ 27.7).

Notes:—According to our phylogenetic tree based on ITS sequences ( Fig. 4 ) and the work of Del-Prado et al. (2016), among the nine Reunionese specimens of the Parmotrema reticulatum aggr. molecularly analysed, seven would belong to the ‘species 2’ of Del-Prado et al. (2016), the other two to P. cf. clavuliferum (see the entry for that taxon herein). With regard to samples of the P. reticulatum complex from Réunion without molecular data, we assigned them to P. reticulatum aggr. (exclusive of P. cf. clavuliferum ) if they did not have numerous sorediate lobes (or laciniae) mottled white on the lower surface.

When measuring the size of the soredia of the seven DNA-analysed specimens, it was found that the individual mean values were significantly heterogeneous (one-way ANOVA, F 6,203 = 7.383, P = 3.7 × 10 -7). Moreover, there was a significant relationship between the mean size of the soredia of a thallus and the elevation of the locality where it was collected (Spearman’s rank correlation, n = 7, r s = −0.8929, 0.01 <P <0.025, one-tailed). The mean size of soredia decreases as elevation increases. In addition to the fact that the thalli growing at lower elevations have more granular soredia, they also tend to have a hypermaculate (sensu Spielmann & Marcelli 2020) upper surface, as well as soralia that extend into submarginal or even laminal areas.

All four accessions of the P. reticulatum aggr. and the single isidiate counterpart P. subisidiosum were resolved with strong support in our 3-locus phylogenetic analysis ( Fig. 3 ), but the relationships within this complex group remain to be discovered.

Specimens with molecular data examined:— FRANCE. Réunion: Cilaos, sentier du col du Taïbit, Plaine des Fraises, elev. 1930 m, 21°06’50”S, 55°26’21”E, in leeward montane rainforest, in an overall south orientation, on bark of an old Erica reunionensis , 17 August 2015, D. Masson 974.4702 (LG); La Possession, Cirque de Mafate, Plaine des Tamarins, elev. 1760 m, 21°04’45”S, 55°26’37”E, in Acacia montane forest, on bark of a branch of Acacia heterophylla , 22 August 2017, D. Masson 974.5069 (LG); Saint-Benoît, forêt de Bébour, les Trois Mares, elev. 1440 m, 21°06’10”S, 55°33’24”E, in windward montane rainforest, in an overall ESE orientation, on bark of a trunk of Dombeya sp. , 21 August 2015, D. Masson 974.4781 (LG); ibid., piste forestière de Takamaka, elev. 1345 m, 21°06’18”S, 55°34’06”E, in windward montane rainforest, on mossy bark of a branch of Dombeya sp. , 16 August 2017, D. Masson 974.4968 (LG); Saint-Philippe, Ravine Angot, elev. 25 m, 21°21’02”S, 55°47’38”E, in disturbed coastal thicket, on bark of a branch of Ficus sp. , 17 August 2013, D. Masson 974.4289 (LG); Saint-Pierre, Piton de Mont Vert, elev. 590 m, 21°19’40”S, 55°32’33”E, in lowland dry forest, on bark of a branch of Pandanus sylvestris , 19 August 2017, D. Masson 974.5015 (LG); 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 974.4127 (LG).

Specimens with no molecular data examined:— FRANCE. Réunion: Cilaos, sentier du Bras Rouge, elev. 1100– 1200 m, sur rocher basaltique, June 1957, J. Bosser 11229 (REN 000079); ibid., ravine des Calumets, elev. 1140 m, 21°09’34”S, 55°29’26”E, in the bottom of a ravine, in an overall south orientation, in a disturbed submontane mesic forest, at the upper subhorizontal part of a basalt rock, 21 August 2012, D. Masson 974.3955 (Hb. DM); ibid., Bras Sec, sentier Kervéguen, elev. 1435 m, 21°07’45”S, 55°29’53”E, on the edge of a leeward montane rainforest and a Cryptomeria japonica plantation, in an overall west orientation, on a 60° inclined and south oriented face of a large basalt rock, 22 August 2012, D. Masson 974.3979 (Hb. DM); ibid., above Îlet des Salazes, elev. 1730 m, 21°06’33”S, 55°26’47”E, in leeward montane rainforest, in an overall SE orientation, on bark of a branch of Hubertia ambavilla , 20 August 2012, D. Masson 974.3924 (Hb. DM); ibid., south edge of Forêt du Grand Matarum, along road to Bras Sec, picnic place, elev. 1360 m, 21°07.4’S, 55°28.9’E, big boulders and outcrops along stream, on boulder, 31 May 2008, P. & B. van den Boom 40203 ( Hb. van den Boom); La Plaine-des-Palmistes, Piton Sauvetage, près du rempart de la Rivière de l’Est, elev. 2325 m, 21°11’52”S, 55°39’54”E, in subalpine Sophora thicket, on bark of Sophora denudata , 22 August 2015, D. Masson 974.4811 (Hb. DM); La Possession, Cirque de Mafate, Plaine des Tamarins, elev. 1765 m, 21°04’48”S, 55°26’39”E, in Acacia montane forest, on bark of Acacia heterophylla , 27 July 2005, D. Masson 974.1785 (REU), 974.1786 (Hb. DM); Le Tampon, forêt de Notre-Dame de la Paix, trail at south rim, from picnic place up to 200 m inside the forest, elev. 1720 m, in rainforest, on mossy bark of Monimia sp. , 06 June 2008, P. & B. van den Boom 40770 ( Hb. van den Boom); ibid., sentier du Piton Textor, elev. 2105 m, 21°11’04”S, 55°38’23”E, in subalpine shrubland, on mossy bark of a trunk of Sophora denudata , 27 August 2012, D. Masson 974.4074 (Hb. DM); ibid., sentier du Piton de Tangues, elev. 2160 m, 21°11’32”S, 55°38’51”E, in subalpine shrubland, in an overall NNE orientation, on bark of a branch of Acacia heterophylla , 22 August 2013, D. Masson 974.4391 (Hb. DM); Petite-Île, Manapany les Hauts, elev. 800 m, 21°19.6’S, 55°35.2’E, open picnic place with some mature Cryptomeria trees, shrubs and mixed trees, including orchard with fruit trees, on Cryptomeria japonica , 07 June 2008, P. & B. van den Boom 40809 ( Hb. van den Boom); Saint-Benoît, Pointe du Bourbier, elev. 30 m, 21°01’13”S, 55°42’13”E, coastal area, picnic place with many Pandanus trees, on bark of P. utilis , 11 June 2008, P. & B. van den Boom 40993 ( Hb. van den Boom); ibid., forêt de Bébour, Piton de Bébour, elev. 1385 m, 21°07’33”S, 55°33’52”E, in windward montane rainforest, on bark of a branch of Monimia rotundifolia , a trunk of Dombeya sp. , and a dead branch of an undetermined tree, 07 April 2003, D. Masson 974.0018 (REU), 974.0021, 974.0135 (Hb. DM); ibid., elev. 1370 m, 21°07’46”S, 55°33’52”E, in windward montane rainforest, on bark of a branch of an undetermined tree, 07 April 2003, D. Masson 974.0164 (Hb. DM); ibid., elev. 1330 m, 21°07’45”S, 55°34’10”E, in windward montane rainforest, on bark of a trunk of Dombeya sp. , 07 April 2003, D. Masson 974.0037 (Hb. DM); ibid., sentier de la Rivière des Marsouins, elev. 1350 m, 21°06’51”S, 55°33’50”E, in windward montane rainforest, on bark of a mossy branch of Monimia rotundifolia , 15 April 2003, D. Masson 974.0400 (Hb. DM); ibid., north of Forêt de Bébour, picnic place near entrance of sentier de Mazerin, elev. 1570 m, NW exposed, sloping mixed forest with a.o. Dombeya trees and steep outcrops, on Terminalia , 27 May 2008, P. & B. van den Boom 39915 ( Hb. van den Boom); Saint-Denis, sentier de la Roche Écrite, elev. 1495 m, 20°58’06”S, 55°26’26”E, in windward montane rainforest, in an overall north orientation, on bark of a branch of Dombeya sp. , 20 August 2015, D. Masson 974.4753 (Hb. DM); ibid., sentier du Piton Mavouse, près de la jonction avec le sentier de la Roche Écrite, elev. 1710 m, 20°58’42”S, 55°26’45”E, in Acacia montane forest, in an overall north orientation, on bark of a trunk of Acacia heterophylla , 20 August 2015, D. Masson 974.4766 (Hb. DM); Saint-Louis, forêt des Makes, Plateau Goyaves, elev. 1710 m, 21°10’58”S, 55°24’33”E, in cultivated forest with Acacia heterophylla and Cryptomeria japonica , in an overall south orientation, on mossy bark of a trunk of a young Acacia heterophylla , 19 August 2013, D. Masson 974.4314 (Hb. DM); Saint-Paul, Le Maïdo, elev. 2180 m, 21°04’18”S, 55°23’14”E, in subalpine shrubland, on bark of stunted Acacia heterophylla , 10 April 2003, D. Masson 974.0219 (REU), 974.0223 (Hb. DM); ibid., route forestière des Tamarins des Hauts-sous-le-Vent, elev. 1710 m, 21°05’26”S, 55°21’32”E, in grazed Acacia montane forest, on bark of a trunk of Acacia heterophylla , 10 April 2003, D. Masson 974.0264 (Hb. DM); ibid., elev. 1740 m, 21°04’18”S, 55°21’42”E, in grazed Acacia montane forest, on bark of Acacia heterophylla , 10 April 2003, D. Masson 974.0240 (Hb. DM); Saint-Philippe, départ du sentier du Tremblet, elev. 135 m, 21°17’42”S, 55°47’57”E, in disturbed lowland rainforest, on bark of the trunk of an undetermined tree, 09 April 2003, D. Masson 974.0212 (Hb. DM); ibid., Mare Longue, elev. 200 m, 21°21’19”S, 55°44’24”E, in lowland rainforest, on bark of the trunk of an undetermined tree, 09 April 2003, D. Masson 974.0189 (Hb. DM); ibid., Cap Méchant, elev. 20 m, coastal picnic area with Pandanus and Palm trees, on Pandanus utilis , 03 June 2008, P. & B. van den Boom 40602 ( Hb. van den Boom); ibid., Basse Vallée, route forestière 36, elev. 120 m, 21°22’08”S, 55°42’27”E, on the road side in a disturbed lowland rainforest, in an overall south orientation, on bark of a trunk of an undetermined tree, 15 August 2015, D. Masson 974.4647 (Hb. DM); Saint-Pierre, Piton de Mont Vert, elev. 595 m, 21°19’36”S, 55°32’29”E, in lowland dry forest, on bark of a trunk of an undetermined dead tree, 19 August 2017, D. Masson 974.5014 (Hb. DM); Sainte-Marie, Plaine des Fougères, elev. 1230 m, 20°58’29”S, 55°31’04”E, in windward montane rainforest, on bark of Pandanus montanus , 17 April 2003, D. Masson 974.0447 (Hb. DM); ibid., elev. 1680 m, 21°00’01”S, 55°30’10”E, in Acacia montane forest, in an overall NE orientation, on mossy bark of a branch of Monimia rotundifolia , 31 August 2012, D. Masson 974.4146 (Hb. DM); ibid., elev. 1715 m, 21°00’03”S, 55°29’53”E, in Acacia montane forest, in an overall north orientation, on mossy bark of Hypericum lanceolatum , 31 August 2012, D. Masson 974.4158 (Hb. DM); Sainte-Rose, trail along Ravine Savane Cimetière to abri du Cassé de la Rivière de l’Est, elev. 2050 m, mixed trees including mature Acacia heterophylla , on A. heterophylla , 28 May 2008, P. & B. van den Boom 39989 ( Hb. van den Boom); ibid., E of Piton Ste-Rose, Quai de Patate, elev. 15 m, 21°09.3’S, 55°49.8’E, coastal area with Pandanus trees, on Pandanus utilis , 30 May 2008, P. & B. van den Boom 40112 ( Hb. van den Boom); ibid., les Cascades, elev. 20 m, 21°11’05”S, 55°50’01”E, coastal wood with Pandanus utilis and Casuarina equisetifolia , on bark of a trunk of P. utilis , 13 August 2013, D. Masson 974.4223 (Hb. DM); ibid., Bois Blanc, near Quai de Tigo, elev. 25 m, 21°12’18”S, 55°49’24”E, coastal wood with Pandanus utilis , on bark of a trunk of P. utilis , 13 August 2015, D. Masson 974.4620 (Hb. DM); ibid., Bois Blanc, elev. 80 m, 21°11’S, 55°49’E, in a garden along a road, on bark of a branch of an undetermined tree, 12 April 2003, D. Masson 974.5230 (Hb. DM); Salazie, Mare d’Affouches, elev. 830 m, 21°02’59”S, 55°29’46”E, disturbed thicket with Erica reunionensis and Psidium cattleianum , on a mossy volcanic rock, 13 April 2003, D. Masson 974.0295 (Hb. DM); ibid., Bélouve, sentier de l’École Normale, elev. 1440 m, 21°03’33”S, 55°33’19”E, in cultivated Acacia montane forest, on mossy bark of a branch of Acacia heterophylla , 24 August 2012, D. Masson 974.4021 (Hb. DM); ibid., elev. 1470 m, 21°04’04”S, 55°33’07”E, in cultivated Acacia montane forest, on bark of a branch of Acacia heterophylla , 24 August 2012, D. Masson 974.4007 (Hb. DM); ibid., GR-R1 trail, near Pic des Chèvres, elev. 1715 m, 21°04’38”S, 55°31’43”E, in windward montane rainforest, on bark of a branch of an undetermined tree, 25 August 2013, D. Masson 974.4476 (Hb. DM).

MADAGASCAR. Alaotra-Mangoro : Sahamaloto, à l’ouest du lac Alaotra, elev. 800 m, en lisière de vestige forestier, sur tronc, June 1955, J. Bosser 8175 ( REN 000080 ) .

MAURITIUS. Moka District: Réduit, State House Park, elev. 280 m, 20.22875°S, 57.48705°E, on palm tree, Ficus microcarpa and undetermined tree, 30 August 2019, P. Diederich 18715, 19279, 19287 & D. Ertz (Hb. Diederich); Rivière Noire District, Chamarel, near the Seven Coloured Earth, Ebony Forest, around the viewpoint, elev. 350 m, 20.43034°S, 57.37412°E, on bark, 08 August 2016, P. Diederich 18544 (Hb. Diederich). Rodrigues, Grande Montagne Nature Reserve, elev. 330 m, 19.70512°S, 63.46596°E, on exposed rocky outcrop surrounded by forest rich in Pandanus trees, 04 September 2019, P. Diederich 19518 & D. Ertz (Hb. Diederich).

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 35. Parmotrema reticulatum aggr. A: Distribution (UTM 2×2 km grid system) of specimens with molecular data on Réunion [= species 2 of Del-Prado et al. (2016)]; B: Distribution of specimens without molecular data on Réunion (UTM 2×2 km grid system); C: Bioclimatic characteristics of collection sites of specimens with molecular data (abbreviations and threshold values for thermotype and ombrotype horizons from Rivas-Martínez et al. 2011: 17–18); D: Gross morphology of thallus (Masson 974.4781); E: Part of thallus with apothecia of various ages (Masson 974.5069); F: Sorediate lobes with soralia capitate at the tip of marginal short laciniae, or submarginal ± linear at the apex of revolute lobe (Masson 974.4289). Scale bars: A, B = 10 km; D, E = 10 mm; F = 4 mm.