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The foliicolous lichen flora of Mexico IV: a new, foliicolous species of Pyrenothrix (Chaetothyriales: Pyrenothrichaceae)

     Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Apdo. Postal 70-233, Coyoacán 04510, Cd., Universitaria, México, D. F., México

Sabine Huhndorf
Robert Lücking ¹

     Department of Botany, The Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, Illinois 60605-2496

	ABSTRACT

TOP ABSTRACT INTRODUCTION TAXONOMY KEY TO THE SPECIES... DISCUSSION LITERATURE CITED

 

Pyrenothrix mexicana Herrera-Campos, Huhndorf & Lücking spec. nova is described from leaves in the upper montane rainforest of Oaxaca State, Mexico. It is the second species in the genus Pyrenothrix Riddle, established at the beginning of the twentieth century for the single species, P. nigra Riddle, a corticolous lichen restricted to southeastern United States. Both taxa have the same thallus and perithecial morphology and anatomy, but P. mexicana differs by its longer, transversally septate ascospores. The perithecial anatomy of Pyrenothrix is documented and its systematic affinities are discussed, and we conclude that the family Pyrenothrichaceae Zahlbr. should be placed in the order Chaetothyriales.

Key words: Ascomycota, Los Tuxtlas, Oaxaca, Veracruz

	INTRODUCTION

TOP ABSTRACT INTRODUCTION TAXONOMY KEY TO THE SPECIES... DISCUSSION LITERATURE CITED

 
In 1917 Riddle established the new genus Pyrenothrix, based on the single species, P. nigra, an enigmatic lichen characterized by perithecioid ascomata and an appressed filamentous thallus with cyanobacterial photobiont (Scytonema). The species was found abundantly on the bark of various trees in southeastern United States and documented by numerous, well-developed collections mostly held at Farlow Herbarium, Harvard University (FH).

Zahlbruckner (1926) erected the family Pyrenothrichaceae (as Pyrenothricaceae) for Pyrenothrix and another genus, Cyanoporina Groenh. These lichens had been forgotten completely until Pyrenothrix was restudied by Henssen (1964). Riddle (1917) had already discussed whether the perithecia could be parasitic on a sterile, filamentous thallus, but concluded that they could not. However, Henssen (1964) suggested P. nigra to be composed of two distinct elements: a filamentous, sterile lichen resembling a Cystocoleus, and a pyrenocarpous, parasymbiontic fungus. For unknown reasons, she described both elements as new, the filamentous lichen as Lichenothrix riddlei A. Henssen, and the supposedly parasymbiontic fungus as Pleosphaeria lichenothricis A. Henssen. One of the two names is illegitimate, because the correct procedure is to select one of the two elements as lectotype for Pyrenothrix nigra. In his extensive survey on bitunicate ascomycete families, Eriksson (1981) contradicted Henssen’s view and confirmed that P. nigra sensu Riddle is a lichen, including all elements originally assigned to it, i.e., filamentous thallus and perithecia. Thus, both Lichenothrix riddlei and Pleosphaeria lichenothricis are synonyms of Pyrenothrix nigra.

During an ongoing inventory of crustose microlichens in the tropical rainforests of Mexico, we came across a second species of Pyrenothrix, described herein as P. mexicana. This new species differs from P. nigra with its transversally septate ascospores and foliicolous growth habit. Pyrenothrix includes two species, P. nigra (corticolous, ascospores muriform) in the southeastern United States and P. mexicana (foliicolous, ascospores transversally septate) in the lowland rainforest of Veracruz State and in the upper montane rainforest of the state of Oaxaca, Mexico. Detailed studies on all available material of the two species confirm Riddle’s and Eriksson’s view of Pyrenothrix representing an autonomous lichen, and the observed characters suggest placement of Pyrenothrichaceae in the order Chaetothyriales sensu Eriksson et al (2004) and Lutzoni et al (2004).

	TAXONOMY

TOP ABSTRACT INTRODUCTION TAXONOMY KEY TO THE SPECIES... DISCUSSION LITERATURE CITED

 
Pyrenothrichaceae Zahlbr.

Pyrenothrichaceae Zahlbr. (as Pyrenothricaceae) in Engler & Prantl, Nat. Pflanzenfam. 8:91. 1926; Eriksson, Opera Bot. 60:144. 1981.

TYPE. Pyrenothrix Riddle (holotype).

Thallus corticolous or foliicolous, composed of densely arranged, but not conglutinated, appressed filaments (FIG. 1A–C); filaments formed by unbranched or falsely branched photobiont threads wrapped in a sheath of fungal hyphae (FIG. 2A–C); hyphae branched and anastomosing, formed by elongate, often strongly curved and terminally inflated, pale brownish cells. Photobiont cyanobacterial (Scytonema). Ascomata perithecioid, sessile or immersed between thallus filaments, globose to pear-shaped with short neck, glabrous; ostiole indistinct. Excipulum (peridium) thin, paraplectenchymatous, grayish brown, innermost 2–3 layers composed of very narrow, thin-walled and periclinally elongate, almost hyaline cells, median 1–2 layers composed of broader, rather large, thick-walled and strongly pigmented cells, and outermost 2–3 layers composed of isodia-metric to irregular, thin-walled and paler cells (FIG. 2D–F); involucrellum absent. Hamathecium (FIG. 3D) aparaphysate (but empty asci resembling paraphyses often present), gel I+ very faintly bluish, KI+ faintly bluish; asci fissitunicate, broadly clavate to saccate (FIG. 3E–F), I–, KI– but lumen I+ yellow and KI+ pale yellow (color of iodine itself); periphyses absent from ostiolar channel but rather long, hyaline periphysoids reaching down from below ostiolar channel into perithecial chamber. Ascospores 8 per ascus, transversally septate to muriform, pale to dark grayish brown (FIG. 3A–C). Conidiomata not observed. Comprises the single genus, Pyrenothrix.

View larger version (110K): [in this window] [in a new window]   FIG. 1. A–C. Pyrenothrix mexicana, appressed filamentous thallus with perithecia (A, isotype; B, paratype; C, ho-lotype). Scale = 1 mm.

View larger version (131K): [in this window] [in a new window]   FIG. 2. A–C. Pyrenothrix mexicana, photobiont filaments with hyphal sheath (A, syntype; B–C, isotype). D–F. P. mexicana (isotype), section through perithecium showing parts of lateral wall and neck. Scale in A–E = 10 µm, in F = 25 µm.

View larger version (135K): [in this window] [in a new window]   FIG. 3. A–B. Pyrenothrix mexicana, ascospores (A, isotype; B, syntype). C. P. nigra (lectotype), ascus and ascospores. D. P. mexicana (isotype), nucleus with mature and empty asci. E–F. P. nigra (lectotype), young and mature asci with ascospores. Scale in A–C and E–F = 10 µm, in D = 25 µm.

Pyrenothrix Riddle, Bot. Gaz. 64:513. 1917; Henssen, Ber. Dt. Bot. Ges. 77:317. 1964; Eriksson, Opera Bot. 60:144. 1981.

TYPE. Pyrenothrix nigra Riddle (holotype).

Lichenothrix A. Henssen, Ber. Dt. Bot. Ges. 77:318. 1964 (nom. illeg., ICBN Art. 9); Eriksson, Opera Bot. 60:144. 1981.

TYPE. Lichenothrix riddlei A. Henssen ( = Pyrenothrix nigra Riddle p.p.) (holotype).

	KEY TO THE SPECIES OF PYRENOTHRIX

TOP ABSTRACT INTRODUCTION TAXONOMY KEY TO THE SPECIES... DISCUSSION LITERATURE CITED

 

1. Ascospores transversally 3-septate, (17–)25–32 x (5–) 7–8 µm, 3.5–4.5x as long as broad; thallus foliicolous; Southern Mexico Herrera-Campos, Huhndorf & Lücking 1. Pyrenothrix mexicana 1. Ascospores (sub)muriform, with (3–)5 transversal and 0–1 longitudinal septa per segment, 17–25 x 6–9 µm, 2.5–3.5 times as long as broad; thallus corticolous; southeastern United States 2. Pyrenothrixnigra Riddle

1. Pyrenothrix mexicana Herrera-Campos, Huhndorf & Lücking, sp. nov. FIGS. 1–2

Sicut Pyrenothrice nigra sed ascosporis transversaliter septatis differt.

TYPE. Mexico. OAXACA. Community forest of Ixtlán de Juárez, 22 km on road toward Tuxtepec, then 39 km on gravel road toward San Juan Yagila (sector El Rincón), then 5 km on gravel road toward La Luz, 17°30'N, 96°23'W, 2300 m, cloud forest (’bosque mesófilo templado), on leaves of Saurauria in forest understory, 14 Feb 2002, Herrera-Campos et al s.n. (MEXU, holotype; F, isotype).

SYNTYPE. MEXICO. VERACRUZ. Los Tuxtlas Tropical Biology Station, 18°35'N, 95°07'W, 150–250 m, May 2001, Herrera-Campos et al s.n. (MEXU).

Thallus foliicolous, epiphyllous, composed of densely arranged, but not conglutinated, appressed filaments, continuous, 3–10 mm across, dark grayish brown (FIG. 1A–C); individual filaments yellowish to light olive brown under the microscope, composed of photobiont threads wrapped in sheath of fungal hyphae (FIG. 2A–C); extruded photobiont threads bluish, cells very applanate, 2–5 x 10–15 µm. Perithecia sessile, subglobose to pear-shaped with short neck, 0.13–0.17 mm diam and 120–150 µm high, dark grayish brown. Excipulum (peridium) 10–15 µm thick, dark grayish brown (FIG. 2D–F). Asci 60–80 x 15–20 µm (FIG. 3D). Ascospores 8 per ascus, fusiform, transversally 3-septate, with slight constrictions at septa, (17–)25–32 x (5–)7–8 µm, median cells grayish brown and in fresh condition with one large, globose oil vacuole each, terminal cells paler to almost hyaline (FIG. 3A–B).

Additional specimens examined. – MEXICO. OAXACA. Community forest of Ixtlán de Juárez, 22 km on road toward Tuxtepec, then 39 km on gravel road toward San Juan Yagila (sector El Rincón), then 5 km on gravel road toward La Luz, 17°30'N, 96°23'W, 2300 m, cloud forest (’bosque mesófilo templado), on leaves of Cestrum in forest under-story, 14 Feb 2002, Herrera-Campos et al s.n. (FH, MEXU); ibid., on leaves of Arbutus in forest understory, 14 Feb 2002, Herrera-Campos et al s.n. (hb. Lücking).

2. Pyrenothrix nigra Riddle FIGS. 1–2

Pyrenothrix nigra Riddle, Bot. Gaz. 64:513. 1917; Eriksson, Opera Bot. 60:144. 1981.

TYPE. U.S.A. FLORIDA. West Palm Beach, on shrub oaks, Dec 1897, Thaxter s.n. (FH, lectotype: specimen A in small gray envelope marked as ‘type’, here selected!).

Pleosphaeria lichenothricis A. Henssen, Ber. Dt. Bot. Ges. 77:320. 1964 (nom. illeg., ICBN Art. 9); Eriksson, Opera Bot. 60:144. 1981.

TYPE. U.S.A. FLORIDA. West Palm Beach, on shrub oaks, Dec 1897, Thaxter s.n. (FH, lectotype: perithecial elements of specimen A in small gray envelope marked as ‘type’, here selected!).

Lichenothrix riddlei A. Henssen, Ber. Dt. Bot. Ges. 77:318. 1964 (nom. illeg., ICBN Art. 9); Eriksson, Opera Bot. 60:144. 1981.

TYPE. U.S.A. FLORIDA. West Palm Beach, on shrub oaks, Dec 1897, Thaxter s.n. (FH, lectotype: vegetative thallus elements of specimen B in larger brown envelope annotated by A. Henssen 1968, here selected!).

Thallus corticolous, composed of densely arranged, but not conglutinated, appressed filaments, continuous, up to 100 mm across, dark grayish brown; individual filaments yellowish to light olive brown under the microscope, composed of photobiont threads wrapped in sheath of fungal hyphae; extruded photobiont threads bluish, cells applanate to rectangular, 3–8 x 8–14 µm. Perithecia sessile, pear-shaped with distinct neck, 0.2–0.3 mm diam and 150–250 µm high, dark grayish brown. Excipulum (peridium) 15–25 µm thick, dark grayish brown. Asci 50–70 x 12–18 µm (FIG. 3E–F). Ascospores 8 per ascus, fusiform, (sub)muriform with (3–)5 transversal and 0–1 longitudinal septa per segment, with slight constrictions at septa, 17–25 x 6–9 µm, median cells pale to dark grayish brown, terminal cells paler to almost hyaline (FIG. 3C).

Additional specimens examined. – U.S.A. FLORIDA. Coconut Grove, on Oleander, 11.1897, Thaxter s.n. (FH).

	DISCUSSION

TOP ABSTRACT INTRODUCTION TAXONOMY KEY TO THE SPECIES... DISCUSSION LITERATURE CITED

 
Taxonomy.— – Pyrenothrix mexicana and P. nigra closely resemble each other in thallus and perithecial morphology and anatomy but differ in their ascospores, being transversally 3-septate in the first as opposed to (sub)muriform in the latter. Both species conform to the concept of sporomorphs in the sense of Wirth & Hale (1978) and Lücking & Kalb (2001).

A probable third species was found in material from the lowland rainforest at Los Tuxtlas Biological Station (here designated as syntype of Pyrenothrix mexicana). It exhibits the same morphology and anatomy as the other material but has distinctly smaller ascospores than the specimens from Oaxaca (17–25 x 5–6 µm versus 25–32 x 7–8 µm). The material is too scant to conclude whether these differences are significant, and therefore at this moment we consider this an aberrant form of P. mexicana.

Nomenclature.— – Henssen (1964) did not accept Riddle’s (1917) concept of Pyrenothrix nigra representing an autonomous lichen. Instead, she considered the perithecia as fruit bodies of a lichenicolous fungus invading a sterile, filamentous lichen thallus. In doing so, the correct way would have been to select one of the two disparate elements, either perithecia or thallus, as lectotype of Pyrenothrix nigra (ICBN, Art. 9). However, Henssen (1964) described both elements as new and cited Pyrenothrix nigra in both cases as synonym, thus creating an unfortunate situation, because the nomenclatural status of both superfluous names cannot be established with certainty, and both have to be considered illegitimate names.

We consider that a fungal taxon is best characterized by its teleomorphic stage. Therefore, if Henssen’s view would be correct and Riddle’s lichen composed of two different elements, lectotypification of Pyrenothrix nigra with the perithecial component (‘Pleosphaeria lichenothricis’) of the original type material would be the logical choice. This lectotypification has been done here formally, to avoid any further confusion. Also, because the original type material (clearly indicated as type by Riddle 1917:515) consists of four envelopes containing parts of the same collection, we also selected a lectotype for Lichenothrix riddlei (the specimen actually annotated by A. Henssen in 1968) and designated the other two envelopes as isolectotypes.

Morphology and anatomy.— – A very characteristic feature of Pyrenothrix is the hyphal sheath surrounding the filaments of the Scytonema photobiont (FIG. 1A–C). At first glance, they seem to form a closed, almost paraplectenchymatous layer, but closer examination reveals that they consist of a distinct, though greatly branched and anastomosing, septate hyphae. The shape of the individual cells, often curved and terminally inflated (these inflations possibly representing haustoria; see Henssen 1964:319), is peculiar. The interspaces between these hyphal cells have more or less similar shapes and are easily mistaken for proper cells. Although the thallus filaments have a yellowish to olive brown color, the photobiont cells themselves appear bluish-green when extruded from their gelatinous sheath.

Similar taxa.— – Species of Psoroglaena in the Verrucariaceae (Verrucariales) are similar to Pyrenothrix in having perithecia resting on a filamentous thallus, but differ in a number of important anatomical details: a green photobiont belonging to the true green algae, a papillose hyphal sheath around the photobiont threads, an often microsquamulose rather than filamentous thallus, perithecia with a clearly three-layered wall, hemiamyloid hamathecium (I+ reddish, KI+ bluish), and hyaline ascospores. Most similar is Psoroglaena epiphylla Lücking, a common foliicolous species which apart from the mentioned characters can be distinguished from Pyrenothrix mexicana by the more appressed, green thallus and the yellowish perithecia.

Sterile specimens of Pyrenothrix are also similar to Dictyonema, a genus of lichenized fungi in the Basidiomycota. Both share the cyanobacterial photobiont (Scytonema), and the mostly foliicolous Dictyonema phyllogenum (Müll. Arg.) Zahlbr. also has a closed hyphal sheath composed of branched, septate hyphae, but the thallus has a distinctly bluish tinge and often forms a whitish prothallus.

Systematic placement.— – Thus far, the systematic placement of Pyrenothrix and Pyrenothrichaceae has been unresolved. Henssen (1964) referred the fungus producing the perithecia to Pleosporales, while Eriksson (1981) suggested close relationship to the sooty molds, in particular Coccodiniaceae, now placed in Capnodiales. In the most recent Outline (Eriksson et al 2004), Pyrenothrichaceae are listed under Dothideomycetes and Chaetothyriomycetes incertae sedis. Recent phylogenetic studies indicate that these two classes are not closely related: While Dothideomycetes are basal in the inoperculate Pezizomycotina, Chaetothyriomycetes are on a derived clade together with Eurotiomycetes and Lecanoromycetes (Lutzoni et al 2001, 2004; Lumbsch et al 2002). The perithecial anatomy of Pyrenothrix clearly indicates placement in Chaetothyriomycetes, but it is open to question whether this family is to be placed in Chaetothyriales or Verrucariales. Both orders are monophyletic sister groups and share a typically hemiamyloid, rarely amyloid hamathecium lacking paraphyses but usually producing long periphysoids. Verrucariales are chiefly lichenized, whereas Chaetothyriales are mostly non-lichenized. So far, no molecular data exist for lichenized fungi currently placed in Chaetothyriales, such as Arthopyreniaceae and Microtheliopsidaceae, to confirm that placement. However, it seems that Chaetothyriales differ from Verrucariales in their simpler perithecial wall anatomy, which, by contrast, could be correlated with the non-lichenized versus lichenized life cycle, because in Verrucariales, thallus elements often are included in the perithecial walls. On account of the rather simple perithecial wall characteristic of Pyrenothrix, we suggest placing Pyrenothrichaceae within Chaetothyriales.

	ACKNOWLEDGMENTS

 
This study was financially supported by a grant of the Mexican CONACYT (no. 35008-V) to M.A. Herrera-Campos and R. Lücking. We would like to thank the Instituto de Biología (UNAM) for logistic support, Rosa Emilia Pérez, Paola Martínez Colín and Álvaro Campos for their assistance in the field, and our colleagues at UNAM, in particular M. Ulloa and C. Delgadillo, for scientific advice.

	FOOTNOTES

 
Accepted for publication April 12, 2005.

¹ Corresponding author. E-mail: rlucking{at}fieldmuseum.org

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION TAXONOMY KEY TO THE SPECIES... DISCUSSION LITERATURE CITED

 
Eriksson OE. 1981. The families of bitunicate ascomycetes. Opera Bot 60:1–209.

———, Baral HO, Currah RS, Hansen K, Kurtzman CP, Rambold G, Laessøe T. 2004. Outline of Ascomycota—2004. Myconet 10:1–99.

Henssen A. 1964. Was ist Pyrenothrix nigra? Ber Deutsch Bot Gesell 77:317–322.

Lücking R, Kalb K. 2001. Echinoplaca vezdana (Ostropales: Gomphillaceae): a new lichenized fungus. Taxon 50: 837–840.[CrossRef]

Lumbsch HT, Wirtz N, Lindemuth R, Schmitt I. 2002. Higher level phylogenetic relationships of euascomycetes (Pezizomycotina) inferred from a combined analysis of nuclear and mitochondrial sequence data. Mycol Progress 1:57–70.[CrossRef]

Lutzoni F, Pagel M, Reeb V. 2001. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411: 937–940.[CrossRef][Medline]

———, Kauff F, Cox C, McLaughlin D, Celio G, Dentinger B, Padamsee M, Baloch E, Grube M, Hibbett D, Spatafora J, Lücking R, Hofstetter V, Reeb V, Binder M, Shcoch C, Schmitt I, Lumbsch HT, James T, Hosaka K, Sung G-H, Liu Y, Hall B, Lim Y-W, Matheny B, Gueidan C, Ertz D, Diederich P, Miadlikowska J, Arnold AE, Vilgalys R. 2004. Where are we in assembling the fungal tree of life, classifying the fungi, and understanding the evolution of their subcellular traits? Am J Bot 91:1446–1480.[Abstract/Free Full Text]

Riddle LW. 1917. Pyrenothrix nigra gen. et spec. nov. Bot Gaz 64:513–515.[CrossRef]

Wirth M, Hale ME Jr. 1978. Morden-Smithsonian Expedition to Dominica: the lichens (Graphidaceae). Smiths Contr Bot 40:1–64.

Zahlbruckner A. 1926. Catalogus Lichenum Universalis. Borntraeger, Leipzig.

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