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Additions and update to the knowledge of the genus Hysterographium (Ascomycota, Hysteriaceae) in southern South America/Adiciones y actualizacion al conocimiento del genero Hysterographium (Ascomycota, Hysteriaceae) en el sur de Sudamerica.

INTRODUCTION

The genus Hysterographium Corda belongs to the family Hysteriaceae (Dothideomycetes, Ascomycota). It is characterized by its muriform, brown to reddish brown or yellowish or yellowish brown ascospores, with one to several longitudinal septa, ovoid to ellipsoid-fusoid, usually constricted at the first-formed septa. Zogg (1962) and Kirk et al. (2001) recognized four species in the genus, meanwhile Linde (1992) six. Since then, an additional three species have been described (Boehm et al., 2009). The species of Hysterographium are widespread, mostly lignicolous, corticolous, saprobic or hemibiotrophic (Barr, 1990).

Previous reports on the taxonomy of this genus in southern South America are found in Spegazzini (1887, 1910), Rehm (1899), Mujica Richatt & Vergara Castillo (1980), and Messuti & Lorenzo (2003). Many species of Hysterographium described from Argentina and Chile by Spegazzini and Rehm were listed as doubtful species in Zogg (1962). However, we found the type material of the doubtful species of this genus was accessible and in well conditions at LPS.

The central theme of this revision was the examination of Spegazzini's types that was needed to resolve some taxonomical problems regarding uncertain species cited by Zogg (1962). The objective of this study was to evaluate some taxonomic aspects that still had not been treated sufficiently in previous studies including some reports from Paraguay.

MATERIALS AND METHODS

Spegazzini's specimens were loaned from LPS. The microscopic characteristics of the specimens were obtained from free-hand sections of hysterothecia mounted in tap water or in Lactophenol Cotton Blue (LCB) (Hawksworth, 1974).

RESULTS AND DISCUSSION

Until now, seven species have been recognized for the genus Hysterographium (Boehm et al., 2009). Three of them, H. flexuosum, H. mori and H. subrugosum, have been found in the study area. In this work, three species, H. andicola, H. australe and H. praeandinum, considered as doubtful ones by Zogg (1962) are confirmed as valid species, bringing the total number of species of the genus to ten according with the recent studies published (Boehm et al., 2009). Moreover, H. cumingii and H. cuyanum, are set as doubtful and H. bonaerense was proposed as a synonym of H. mori.

Valid and distinct species

Hysterographium andicola Speg., Anal. Mus. Nac. Bs. As. 23: 85. 1912. TYPE: Argentina, Mendoza, Potrerillos, on dead branches of Tricycla spinosa, 22-IV-1910, C. Spegazzini s. n. (lectotype LPS 1288-a!, here designated). Figs. 1A-B.

Hysterothecia gregarious, erumpent, superficial, straight to flexuous, irregular in shape especially when crowded, 0.47-1.80 x 0.28-0.57 mm, lips more or less open exposing a narrow red disc; pseudoparaphyses hyaline, abundant, filiform, branched, longer than asci; epithecium ferrugineous to red-brown, 3 % KOH staining purple; asci cylindrical-claviform, (4-)8-spored, 110-180 x 14-20 [micro]m; ascospores reddish brown, uniseriate to biseriate, muriform, appearance not parenchymatic, with 4-6 transverse and 1 longitudinal septa, ellipsoid, constricted at the median septum, 16-26(-28) x 8-10 [micro]m.

Geographical distribution and habitat. The species is only known for the type locality. Hysterographium andicola was collected from Argentina, Mendoza Province at Potrerillos, Andes Mountains at 1,469 m altitude (32[degrees]57'00''S, 69[degrees]10'60''W), a region where xerophytic vegetation is predominant. Hysterographium andicola was collected on branches of endemic shrubs Condalia microphylla Cav. (Rhamnaceae, V. n. "Piquillin negro") and Bougainvillea spinosa (Cav.) Heimerl (Nyctaginaceae, V. n. "Monte negro") [= Condalia lineata A. Gray and Tricycla spinosa Cav., respectively, "fide" Spegazzini (1912)].

Observations. The original collection of Hysterographium andicola includes two packets designated here as LPS 1288-a and -b. When Spegazzini (1912) published the species, he did not assign the holotype, thus the collection LPS 1288-a is selected here as lectotype.

The type material exists and the collections are in good condition, therefore, we see no reason to consider this species as doubtful as it was cited by Zogg (1962).

The species resembles Hysterographium mori (Schwein.) Rehm in the morphology of ascospores with a similar length/width ratio (l:w = 2:1), but H. mori has a variable number of transverse septa (3 to 7) and smaller ascospores. (Zogg, 1962; Linde, 1992). Furthermore, two other species of this genus besides H. andicola are cited as having a brick-red epithecium (Linde, 1992; Checa et al., 2007): H. pulchrum Checa, Shoemaker & Umana and H. spinicola Doidge (as "spinicolum"), but Spegazzini's species differs from those two in the size and shape of ascospores. Nevertheless, the taxonomic importance of the colour of the centrum of ascomata is not yet clear.

Specimens examined

ARGENTINA. Mendoza. Potrerillos, on dead branches of Condalia lineata, 24-III-1910, C. Spegazzini s.n. (LPS 1288-b).

Hysterographium australe Speg., Anal. Soc. Cient. Arg. 12: 189. 1881. TYPE: Argentina, Buenos Aires, Las Conchas, on wood of Erythrina crista-galli, I-V-1881, C. Spegazzini s. n. (holotype LPS 1291!). Fig. 1C.

Hysterothecia gregarious, superficial, straight or flexuous, 0.57-2.28 x 0.19-0.38 mm; pseudoparaphyses hyaline, abundant, filiform, longer than asci; asci cylindrical-claviform, 4-5(-6-8)-spored, 100-105 x 18-20 [micro]m; ascospores brown, muriform, not parenchymatic, with 6-8 transverse and 1 longitudinal septa, broadly ellipsoid, tapered to the lower part, constricted at the median septum, slightly inequilateral, 22-28 x 6-10 [micro]m.

Geographical distribution and habitat. The species was recorded solely to Argentina. The type material of H. australe was collected on decorticated wood of Erythrina crista-galli L. (Fabaceae, V. n. "Ceibo"), from Las Conchas, Buenos Aires Province (at present the locality name corresponds to Tigre). Another collection of this species was obtained by Spegazzini (1912) growing on branches of an unknown species of shrubs in Catamarca Province.

Observations. At first sight the ascospores of H. australe resemble those of Hysterographium subrugosum (Cooke & Ellis) Sacc. in size, with similar ratios of length to width (l:w = 3-3.5:1). However, we find that ascospores of H. australe differ in their form, being broadly ellipsoid rather than fusiform, and in their smaller size (Spegazzini, 1881; Zogg, 1962; Linde, 1992). Zogg (1962) included this species in his list of doubtful ones, but gave no reason for this placement. Spegazzini (1881) described this species as "aparaphysati". However, when the type material (LPS 1291) was observed, the presence of abundant pseudoparaphyses was clear.

Hysterographium flexuosum (Schwein.) Sacc., Syll. Fung. (Abellini) 2: 781. 1883. Hysterium flexuosum Schwein., Schriften Naturf. Ges. Leipzig 1: 49. 1833 [Syst. Mycol. 2: 585. 1823 fide Barr (2009)]. TYPE: not located [fide Bisby (1932) the co-type is deposited in K]. Figs. 1F y 3A.

References. For description, comments and synonymy see Zogg (1962), Messuti & Lorenzo (2003) and Barr (2009).

Geographical distribution and habitat. Cosmopolitan (Barr, 1990). The species was described from Argentina, in the Patagonian Provinces of Neuquen, Rio Negro and Tierra del Fuego, mainly found on wood and bark of Nothofagus Blume species (Messuti & Lorenzo, 2003). In this contribution, the known distribution of H. flexuosum is expanded to Santa Cruz Province, Los Glaciares National Park, growing on fallen branches of Nothofagus pumilio (Poepp. & Endl.) Krasser (Fagaceae, V. n. "Lenga").

Specimens examined

ARGENTINA. Santa Cruz. Parque Nacional Los Glaciares, entrance to the drift, ca. 1 km on the right side of the road at the base of Cerro Mitre, 50[degrees]27'39''S, 72[degrees]47'10''W, on fallen branches of Nothofagus pumilio, 10-XII-2003, M. I. Messuti s.n. (BCRU 4811).

Hysterographium mori (Schwein.) Rehm, Ascom. 26. Bericht d. Nat. hist. Vereins Augsburg: 90. 1881 [Ascomyceten: no. 363 (1876) fide Index Fungorum]. Hysterium mori Schwein., Syn. Fung. Amer. bor.: no. 2087. 1834. [1832 fide Index Fungorum]. TYPE: sine data (K) ["fide" Bisby (1932)]. Figs. 2A-B.

Hysterographium portenum Speg., Anal. Soc. Cient. Arg. 9: 185. 1880. [as "portenum" "fide" Index Fun gorum]. TYPE: Argentina, Buenos Aires, Flores, on Melia azedarach, sine data, C. Spegazzini s.n. (holotype LPS 1284!).

Hysterographium bonaerense Speg., Anal. Soc. Cient. Arg. 12: 208. 1881, syn. nov. [as "bonariense" "fide" Index Fungorum]. TYPE: Argentina, Buenos Aires, Palermo, on Salix humboldtiana, V-1881, S. Ambrosetti s.n. (holotype LPS 1283!).

Hysterographium guaraniticum Speg., Anal. Soc. Cient. Arg. 26: 56. 1888. TYPE: Paraguay, Guarapi, on decomposed wood, VIII-1883, B. Balansa 3953 (holotype LPS 1273!).

[FIGURE 1 OMITTED]

References. For additional synonymy see Zogg (1962), Rosato (2007) and Barr (2009).

Hysterothecia single or gregarious, erumpent, superficial, straight to flexuous, surface usually striate, 0.4-2 x 0.2-0.4 mm; pseudoparaphyses hyaline, abundant, filiform, branched, longer than asci; epithecium compact; asci clavate to cylindrical, 8-spored, (55-)70-170 x 10-18 [micro]m; ascospores yellow-brown to reddish brown, uniseriate to partially biseriate, muriform, not parenchymatic, with [3-5(-7)] transverse and 1 longitudinal septa, ellipsoid to obovoid, sometimes slightly inequilateral, constricted at the median septum, (12-)15-24(-26) x (5-)6-10(-11) [micro]m.

Geographical distribution and habitat. Cosmopolitan (Barr, 1990). The specimens examined of this species were the type material of H. guaraniticum, H. bonaerense and H. portenum. In Argentina, H. mori was reported from Buenos Aires Province, Buenos Aires City, San Jose de Flores as H. portenum (Spegazzini, 1880) and Palermo as H. bonaerense (Spegazzini, 1881); in San Luis Province, Alto Grande as Tryblidaria argentinensis Speg. (Rosato, 2007), and in Tucuman and Catamarca Provinces (Catania, 2009). From Paraguay the species was registered in Pacu Cua (Spegazzini, 1921) and in Asuncion (Spegazzini, 1922) as H. portenum and in Guarapi as H. guaraniticum (Farr, 1973). Hysterographium bonaerense was found growing on old bark of Salix humboldtiana Willd. (Salicaceae, V. n. "Sauce criollo"). Hysterographium guaraniticum was detected on decaying decorticated logs of unidentified plants. Hysterographium portenum was collected on sticks of Melia azedarach L. (Meliaceae, V. n. "Arbol de paraiso"), on wood of Brosimum gaudichaudii Trecul (Moraceae, V. n. "Mama-cadela" or "Sweet cotton") and on decorticated trunk of Citrus bigaradia Risso (Rutaceae, V. n. "Naranjo amargo"). Catania (2009) cited H. mori growing on bark and wood of Podocarpus parlatorei Pilg. (Podocarpaceae, V. n. "Pino del cerro"). For more substrates for Hysterographium mori, see Zogg (1962).

Observations. Spegazzini (1881) described Hysterographium bonaerense (as " H. bonariense" on the label of type packet) as having the following characteristics: hysterothecia gregarious, superficial, straight to flexuous, 1-1.5 x 0.2-0.22 mm; pseudoparaphyses present; asci cylindrical, 8-spored, 100-120 x 12 [micro]m in the sporogenus portion; ascospores pallid olivaceous, uniseriate to partially biseriate, with 3 transverse and 1 longitudinal septa, ellipsoid to ovate, 20-22 x 8-10 [micro]m (Fig. 1D). The following differences were found between the original description of the species and our examination of the type material (LPS 1283): hysterothecia 0.5-2 x 0.3-0.4 [micro]m, ascospores reddish brown, with 3-4 transverse septa. Zogg (1962) cited this species in his list of doubtful ones. Because we did not find significant differences in features between H. mori and Spegazzini's species we regard both taxa as synonymous.

There are two other species of the genus Hysterographium described by Spegazzini, H. guaraniticum (Fig. 2A) and H. portenum (Fig. 2B) that Zogg (1962) proposed as synonyms of Hysterographium mori. Our analyses of the type material (LPS 1284 and LPS 1273) allowed us to confirm those synonyms.

Hysterographium praeandinum Speg., Anal. Mus. Nac. Hist. Nat. Bs. As. 23: 87. 1912. TYPE: Argentina, Mendoza, Potrerillos, on Tricycla spinosa, 24-IV-1910, C. Spegazzini s.n. (lectotype LPS 1290-a!, here designated). Figs. 2C y 3B.

Hysterothecia gregarious, erumpent, superficial, straight, 0.21-0.56 x 0.12-0.16 mm; pseudoparaphyses hyaline, abundant, filiform, branched, longer than asci; epithecium ferrugineous to redbrown; asci cylindrical, 8-spored, 100-120 x 12-14 um; ascospores reddish brown, uniseriate to partially biseriate, muriform, not parenchymatic, with (1-2-)3 transverse and 1 longitudinal septa (?), obovoid, constricted at the median septum, lower cell conical and lighter than the upper ones, 10-14 x 4-6 [micro]m [18-20 x 8-10 [micro]m, fide Spegazzini (1912)].

Geographical distribution and habitat. The species is only known in Argentina for the type locality and San Juan Province. Hysterographium preandinum was recorded only from Argentina in arid areas of Mendoza and San Juan Provinces, growing on decorticated wood of xeromorphic schrubs.

[FIGURE 2 OMITTED]

Observations. The type collection LPS 1290, contains two packets, one of them on wood of Tricycla spinosa (LPS 1290-a) and other on Bulnesia retama (Gill. ex Hook.) Griseb. (Zygophyllaceae, V. n. "Retamo") (LPS 1290-b). Because Spegazzini (1912) did not assign the holotype, the material LPS 1290-a, is selected here as lectotype. Spegazzini (1912) noted that the ascospores are longitudinally 1-septate and transversally (4-5)3-septate, which was not found by us in either collection (LPS 1290 a, b) with one exception where we detected only one longitudinal septum. The size of ascospores that we registered from the type specimens was remarkably smaller than the one published in the original description. Therefore, it can be presumed that we observed material that was not completely mature.

Specimens examined

ARGENTINA. San Juan. Pie de Palo, on fallen branches of Bulnesia retama, II-1910, C. Spegazzini s.n. (LPS 1290-b).

Hysterographium subrugosum (Cooke & Ellis) Sacc., Syll. Fung. 2: 780. 1883. Hyste rium subrugosum Cooke & Ellis, Grevillea 5: 54. 1876. TYPE: sine data (K) ["fide" Bisby (1932)].

References. For description, comments and synonymy see Zogg (1962), Messuti & Lorenzo (2003) and Barr (2009).

Geographical distribution and habitat. This species grows in northern as well as in southern temperate areas of the world (Barr, 1990; Messuti & Lorenzo, 2003). Hysterographium subrugosum is additionally reported from Argentina, Neuquen Province, near Pichi Traful River, and also in Paso Cordoba, Road 63, growing on unidentified dead twigs. Previously, the species was recorded from Rio Negro Province and Tierra del Fuego Province (Argentina), growing on Nothofagus species and on Drimys winteri J.R. Forst. & G. Forst. (Winteraceae, V. n. "Canelo") (Messuti & Lorenzo, 2003).

Specimens examined

ARGENTINA. Neuquen. Rio Pichi Traful, Sec. Guardaparques, on decorticated twigs, 27.IV.2001, L. E. Lorenzo s.n. (BCRU 5015); "ibid.", on decorticated twigs, 27-IV-2001, L. E. Lorenzo s.n. (BCRU 5018); Paso Cordoba, Ruta 63 in direction to San Martin de los Andes, 23 km after Limay-Traful confluence, Nothofagus pumilio forest, on decorticated wood, 24-IV-2001, L. E. Lorenzo s.n. (BCRU 5019).

Uncertain species

Hysterographium cumingii Speg., Rev. Fac. Agron. Vet. La Plata 6: 119. 1910. TYPE: Not located.

Observations. This species was described and reported by Spegazzini (1910) to be found in Chile, Valparaiso, Cerro Alegre, growing on rotten culms of bamboo, Chusquea cumingii Nees (Poaceae, V. n. "Quila chica"). The species has not been reported on any other occasion. In agreement with Zogg (1962) this species must be considered as a doubtful one, because the type material is missing and it is not registered in the database of type specimens in LPS (Rosato, pers. com.) and no information about it could be found in other herbaria.

Hysterographium cuyanum Speg., Anal. Mus. Hist. Nat. Bs. As. 23: 86. 1912. TYPE: Argentina. San Juan, Pie de Palo, on bare wood of Bulnesia retama, II-1910, C. Spegazzini s.n. (holotype LPS 1286!). Fig. 1E.

Observations. Spegazzini (1912) characterized this species by: hysterothecia superficial, 0.4-1 x 0.2 -0.25 mm; pseudoparaphyses abundant, dichotomously branched; asci cylindrical, 120 x 17-18 [micro]m; ascospores subclaviform, with (5-)7(-9) transverse and 1 longitudinal septa, light brown, 28-32 x 12-14 [micro]m.

Hysterographyum cuyanum bears the closest resemblance to H. subrugosum mainly by its ascospore size and septal numbers. However, as the type material (LPS 1286) is scant and immature, Spegazzini's observations cannot be confirmed. Therefore this taxon must be considered doubtful, as it was proposed by Zogg (1962).

[FIGURE 3 OMITTED]

Invalid names

Hysterographium subfuscum Speg.

Apparently this taxon is an unpublished herbarium name (Farr, 1973). Zogg (1962), based on a specimen collected by Balansa in Paraguay, Guarapi, in August 1883 (deposited in B), proposed this species to be a synonym of Hysterographium mori. We asked for the loan of these specimens from B but they were not found there (Gerhardt, pers. com.). The species is neither present at LPS (Rosato, pers. com.).
Key to species of Hysterographium recorded
from Argentina, Chile and Paraguay

1. Ascospores muriform, parenchymatic                     H. flexuosum

1. Ascospores muriform, not parenchymatic                             2

2(1). Ascoma with a ferruginous to red-brown epithecium               3

2. Ascoma without a coloured epithecium                               4

3(2). Ascospores with 4-6 transversal septa and 1 longitudinal
septum 16-28 x 8-10 [micro]m                                H. andicola

3. Ascospores with (1-2-)3 transversal septa and 1 longitudinal
septum 10-14 x 4-6 [micro]m                              H. praeandinum

4(2). Ascospores with 3-5(-7) transversal septa and 1
longitudinal septum                                             H. mori

4. Ascospores with 6-11 transversal septa and 1-2 longitudinal
septa                                                                 5

5(4). Ascospores fusiform, with 7-11 transversal septa
and 1-2 longitudinal septa  H. subrugosum

5. Ascospores ellipsoid to broadly ellipsoid, with 6-8
transversal septa and 1 longitudinal septum                 H. australe


ACKNOWLEDGEMENTS

We are grateful to the curators, V. G. Rosato (LPS) for loaning the Spegazzini's material, A. L. Anderberg (S), M. N. Cabello (Instituto Spegazzini), E. Gerhardt and R. Vogt (B), R. Marcucci (PAD), and P. Mario (Universita di Padova) for their helpful collaboration and suggestions. To M. A. Valente (Instituto de Botanica Darwinion) for her assistance with the edition of the figures. The Universidad Nacional del Comahue and CONICET provided funds for this research.

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Boehm, E. W. A.; C. L. Schoch & J. W. Spatafora. 2009. On the evolution of the Hysteriaceae and Mytilinidiaceae (Pleosporomycetidae, Dothideomycetes, Ascomycota) using four nuclear genes. Mycological Research 113: 461-479.

Catania, M. 2009. Diversidad de Hymenoascomycetes y Loculoascomycetes sobre Podocarpus parlatorei Pilg. en las Provincias de Tucuman y Catamarca. Tesis Doctoral, Universidad Nacional de Tucuman.

Checa, J.; R. A. Shoemaker & L. Umana. 2007. Some new hysteriaceous fungi from Costa Rica. Mycologia 99: 285-290.

Farr, M. L. 1973. An annotated list of Spegazzini's fungus taxa. BibliothecaMycologica 35: 1-1661.

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Kirk, P. M.; P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby's dictionary of Fungi. 9th ed. Wallingford: CAB International.

Linde, E. J. van der. 1992. Notes on the South African Hysteriaceae (Ascomycetes: Mycotina). South African Journal of Botany 58: 491-499.

Messuti, M. I. & L. E. Lorenzo. 2003. Notes on the genus Hysterographium (Ascomycota) in southern South America. Nova Hedwigia 76: 451-458.

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Rosato, V. G. 2007. Observaciones sobre las especies argentinas de Tryblidaria (Dothideomycetes, Patellariaceae). Boletin de la Sociedad Argentina de Botanica 42: 55-58. Spegazzini, C. 1880. Fungi Argentini.1. Anales de la Sociedad Cientifica Argentina 9: 158-192.

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Spegazzini, C. 1912. Mycetes argentinenses 6. Anales del Museo Nacional de Historia Natural de Buenos Aires 23: 1-130.

Spegazzini, C. 1921. Sobre algunas enfermedades y hongos que afectan las plantas de "Agrios" en el Paraguay. Anales de la Sociedad Cientifica Argentina 90: 155-188.

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Laura E. Lorenzo (1) & Maria I. Messuti (2)

(1) Departamento de Botanica, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Quintral 1250, 8400 San Carlos de Bariloche, Provincia de Rio Negro, Argentina; llorenzo@crub.uncoma.edu.ar (author for correspondence).

(2) Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), CONICET - Universidad Nacional del Comahue, Quintral 1250, 8400 San Carlos de Bariloche, Provincia de Rio Negro, Argentina.
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