Introduction

The associations between fungi and Bryophyte species can be as pathogens, parasites, saprobes, or commensals (^{Davey and Currah, 2006}); however, these are poorly documented or understood (^{Döbbeler and Hertel, 2013}; ^{Kowal et al., 2018}). In the case of endophytic bryophyte fungi, it is known that these can help them resist certain stressors such as extreme pH levels and promote protonema growth (^{During and Van Tooren, 1990}). Of these symbioses between bryophytes and fungi, the best known and most documented in the world correspond to parasitic fungi (^{Döbbeler, 1997}; ^{Döbbeler and Hertel, 2013}). The ecological niche that bryophytes provide for parasitic fungi is quite restricted to a few taxa, mainly Ascomycota genera that are phylogenetically not related (^{Döbbeler and Hertel, 2013}).

The family Dactylosporaceae is characterized by superficial blackish apothecia, excipulum of texture angularis to globose cells, hymenium consisting of a thick gelatinous matrix, paraphyses with swollen and pigmented apices, cylindrical to clavate amyloid octosporic asci with I- tholus covered by a I+ blue external gelatinous cap; subglobose to ellipsoid ascospores, and one to several transverse septa (^{Hafellner, 1979}; ^{Bellemère and Hafellner, 1982}; ^{Döbbeler and Buck, 2017}; ^{Ekanaya et al., 2019}). This family presents species with variable ecological habits; among the main ones are saprobes on bark and wood, parasites, or lichenized taxa (^{Wijayawardene et al., 2018}; ^{Ekanayaka et al., 2019}). In this family, only the genus Dactylospora Körb has been reported with species with a briophilous habit. However, the phylogenetic reconstruction of the genus using the molecular markers nrLSU and mtSSU has resulted in the transfer of numerous species to the genus Sclerococcum Fr. (^{Diederich et al., 2013}, ²⁰¹⁸; ^{Pang et al., 2014}). In Mexico only Dactylospora stygia var. stygia (Berk. and M.A. Curtis) Hafellner and D. stygia var. tenuispora (Dennis) Hafellner are registered as saprophytic species in tropical forest and tropical cloud forest in the states of Tabasco and Veracruz (^{Chacón and Tapia, 2016}). In contrast, most of the species of the family have been indicated as lichenicolous; Sclerococcum montagnei Hafellner and S. pleiospermum (Triebel) Ertz & Diederich on Lecanora Ach. and Pertusaria DC.; S. athallinum (Müll. Arg.) Ertz & Diederich on Baeomyces Pers., S. parasiticum (Flörke) Ertz & Diederich on Pertusaria DC. and Ochrolechia A. Massal., and Sclerococcum saxatile (Schaer.) Ertz & Diederich on Pertusaria DC. (^{Diederich, 2004}; ^{Hafellner, 2004}), all for the Sonoran Desert region in northern Mexico.

According to ^{Index Fungorum (2021)}, there are two species included in Paruephaedria Zukal, another genus in this family. Paruephaedria heimerlii Zukal is a species with a bryoparasitic habit, traditionally classified within the genus Dactylospora (^{Döbbeler and Triebel, 1985}). We consider here the name P. heimerlii, originally proposed by ^{Zukal (1891)}, due to the lack of available sequences of the species that will allow to clarify its phylogenetic position and its relationship with other genera with similar characteristics such as Sclerococcum or Dactylospora. The latter is concerning, since it has recently been pointed out by various authors that it is not a monophyletic genus (^{Pang et al., 2014}; ^{Diederich et al., 2018}; ^{Xian-Dong et al., 2018}). Another briophilous species in Dactylosporaceae is Dactylospora inopina Döbbeler and W.R. Buck, differing from P. heimerlii by its polysporous asci and four-celled spores (^{Döbbeler and Buck, 2017}). Consequently, the objective of this work is to present with pictures and description the first record of the species P. heimerlii both in Mexico and the tropics.

Materials and Methods

The specimens studied were collected in the pine-oak forest in the town of Atotonilco in the municipality Calcahualco (19°08'40.0''N, 97°11'38.8''W, 2180 m a.s.l.) and in the tropical cloud forest in the municipality Huatusco (19°10'34.4''N, 96°58'40.6''W, 1340 m a.s.l.), in the state of Veracruz, Mexico (Fig. 1). The material was herborized and decontaminated by cooling (-10° C), and it was deposited in the fungal collections of the herbaria ENCB of the Instituto Politécnico Nacional and XALU (acronyms according to ^{Thiers, 2021}+) of the Facultad de Biología, Universidad Veracruzana. Ascomata histological sections were made freehand with a stereoscopic microscope (Carl Zeiss model Stemi Dv4, Jena, Germany), and mounted in water. The determination of the briophilous fungus was following the key proposed by ^{Marsh et al. (2010)} . Their structures were measured in water with an optical microscope (Carl Zeiss Primo Star HAL / LED model, Jena, Germany) at the Environmental Quality Laboratory of the Facultad de Biología of the Universidad Veracruzana, Xalapa, Mexico. The reaction of amyloid compounds in the hymenium was tested with Lugol’s solution (IKI). The photographs were taken with an iPhone SE 2020 cell phone (Zhengzhou, China).

Figure 1: Sampled localities of Paruephaedria heimerlii Zukal reported in Veracruz, Mexico. 

The specimens studied were collected in the pine-oak forest in the town of Atotonilco in the municipality Calcahualco (19°08'40.0''N, 97°11'38.8''W, 2180 m a.s.l.) and in the tropical cloud forest in the municipality Huatusco (19°10'34.4''N, 96°58'40.6''W, 1340 m a.s.l.), in the state of Veracruz, Mexico (Fig. 1). The material was herborized and decontaminated by cooling (-10° C), and it was deposited in the fungal collections of the herbaria ENCB of the Instituto Politécnico Nacional and XALU (acronyms according to ^{Thiers, 2021}+) of the Facultad de Biología, Universidad Veracruzana. Ascomata histological sections were made freehand with a stereoscopic microscope (Carl Zeiss model Stemi Dv4, Jena, Germany), and mounted in water. The determination of the briophilous fungus was following the key proposed by ^{Marsh et al. (2010)} . Their structures were measured in water with an optical microscope (Carl Zeiss Primo Star HAL / LED model, Jena, Germany) at the Environmental Quality Laboratory of the Facultad de Biología of the Universidad Veracruzana, Xalapa, Mexico. The reaction of amyloid compounds in the hymenium was tested with Lugol’s solution (IKI). The photographs were taken with an iPhone SE 2020 cell phone (Zhengzhou, China).

Results

Taxonomy

Lecanoromycetes

Lecanorales

Dactylosporaceae

Paruephaedria heimerlii^{Zukal, Flora, Regensburg 74: 98. 1891}. Fig. 2.

TYPE: GERMANY. Bayern. Hochland, Lahn bei der Jachenau, Sendtner s.n. (neotype: M-M0041422).

= Dactylospora heimerlii (Zukal) ^{Döbbeler and Triebel Bot. J. 107(1-4): 509. 1985}.

Figure 2: Paruephaedria heimerlii Zukal; A-C. apothecia growing in a gametophyte of a leafy liverwort; D. hymenium in Lugol’s solution; E. spores showing different septation. 

Apothecia 100-300 μm diameter, superficial, solitary or gregarious, sessile, pulvinate, black to pale brown in KOH, smooth or finely granulated surface; ectal excipulum 25-40 μm wide, angular to globular texture composed of polygonal cells, thin-walled, brown to dark brown; medullary excipulum 10-15 μm wide, intricate texture composed of hyaline intertwined hyphae, embedded in a gelatinous matrix; hymenium hyaline to brownish, enclosed in a thick gelatinous matrix; pseudoepithecium composed of hyaline to brown amorphous matter surrounding the paraphysis tips; paraphyses 1.4-2 μm wide, filiform, septate, swollen, slightly branched and pigmented at the apex, extending beyond the asci and apices attached together to develop a pseudoepithecium; asci 45-50 × 17-20 μm, unitunicate, sessile, cylindric-clavate, rounded at the apex, inoperculate with an amyloid gelatinous cap, octosporic; ascospores 10-18 × 5-6 μm, spores ellipsoid when immature to fusoid when mature, with a transverse septum, hyaline to olivaceous, guttulate, smooth, thin-walled, multiseriate.

Habit and habitat: growing on phyllidia of a leafy liverwort.

Distribution: according to ^{Döbbeler and Hertel (2013)} , Paruephaedria heimerlii is known from Alaska, Japan, Tasmania, and various localities in Europe, with an altitudinal range of 570 to 1250 m a.s.l. This is the first record for Mexico and for the tropics.

Material examined: MEXICO. Veracruz, municipality Calcahualco, Atotonilco, 2180 m a.s.l., 19°08'40.0''N, 97°11'38.8''W, 06.II.2021, P. Sorcia-Navarrete 405 (XALU), 406 (XALU), 407 (XALU). Municipality Huatusco, 1340 m a.s.l., 19°10'34.4''N, 96°58'40.6''W, 03.XII.2021, J. Guzmán-Guillermo, 2305 (XALU), 2306 (ENCB).

Taxonomic notes: this species grows exclusively on the phyllidia of leafy liverworts of the order Jungermanniales in forested regions with high humidity. Morphologically it is characterized by having a dark brown to black discoid apothecium, with asci that have a blue I + gelatin at the tip, spindle spores that vary in size and that can have one to three septa.

Discussion

According to ^{Döbbeler and Hertel (2013)} , the largest number of records of P. heimerlii have been made mainly in temperate forested regions of Europe, with some records in Alaska, Japan, and Tasmania. Such climate characteristics coincide with the pine-oak forest vegetation present in localities of the specimens Sorcia-Navarrete 405 (XALU), 406 (XALU) and 407 (XALU), although at an elevation of almost 1000 m higher than that registered in other sampled localities (^{Döbbeler and Hertel, 2013}). However, the specimens Guzmán-Guillermo 2305 (XALU) and 2306 (XALU) were collected in a tropical cloud forest vegetation which is a confluence zone between tropical and temperate floristic elements. This suggests that the presence and reproduction of P. heimerlii are not conditioned to the temperature and other factors determined by altitude of the habitat in which it is found, but to the availability of hosts. However, it is necessary to carry out studies to affirm this. Regarding the host, all the specimens studied here were found parasitizing phyllidia of leafy liverworts, which coincides with the records previously made by other authors (^{Zukal, 1891}; ^{Marsh et al., 2010}; ^{Döbbeler and Hertel, 2013}).

The collection of bryoparasitic fungi is commonly accidental and its scarce study is related to the lack of cooperation between bryologists and mycologists (^{Döbbeler, 1997}), which has a high relevance if we consider the specificity of these fungi to a related species or genera of marchantiophytes (^{Döbbeler and Hertel, 2013}). As has happened with this finding, the specimens analyzed here correspond to leafy liverworts that were accidentally collected among lichens.

Finally, it is highlighted that this new record for Mexico represents one more element to indicate the importance of continuing with field explorations that allow progress in the taxonomic knowledge of certain groups (^{Wilson, 2017}). The discovery presented here is made in the state of Veracruz which has a long tradition of field studies. However, it is evident that there are biological groups like this one whose findings of new species or expansion of distribution ranges result in increasing diversity for this state, which agrees with the worldwide trend for this group since it is estimated that only 7% of the estimated diversity of fungi is known (^{Mora et al., 2011}).