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Two new species of the staurosporous hyphomycetous genera Ceratosporium and Diplocladiella from Taiwan

     J.W. Goethe-Universität Frankfurt, Botanisches Institut, Senckenberganlage 31-33, 60054 Frankfurt, Germany

Chee-Jen Chen

     Southern Taiwan University of Technology, Department of Biotechnology, Nantai-Street 1, Yungkang, Tainan 71043, Taiwan R.O.C.

	ABSTRACT

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Ceratosporium verrucosum and Diplocladiella alta are described as new species. Ceratosporium verrucosum was found on a dead bamboo culm and D. alta on rotting wood in Taiwan. Compared with the other species of Ceratosporium, C. verrucosum differs by the verrucose ornamentation covering the arms of the conidia. Diplocladiella alta is easily distinguished by the length of its conidiophores. For comparison with the previously described species of Ceratosporium, type material of C. fasciculare first was reexamined and Bactrodesmium submoniliforme recognized as the correct name for this species.

Key words: Hirudinaria, hyphomycetes, SEM, spore dispersal, stauroconidia, taxonomy

	INTRODUCTION

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Because of their exotic appearance it is tempting to think of staurosporous hyphomycetes as being taxonomically related. That is not necessarily the case. In this paper we describe staurosporous species in genera that differ in conidium morphology and conidiogenesis. Species of Ceratosporium, Diplocladiella and Hirudinaria produce pigmented stauroconidia. Species of Ceratosporium and Hirudinaria produce conidia by monoblastic conidiogenesis from micronematous conidiophores. Finally, species of Diplocladiella produce conidia by sympodial conidiogenesis from macronematous conidiophores (Ellis 1971, 1976). Conidium secession in the species of these genera leads to large, circular scars without further special features that could be used for the separation of genera. The development of the conidia and the taxonomy of species of Ceratosporium and Hirudinaria were investigated in detail by Hughes (1951). The two genera were differentiated on the basis of the smooth wall of the conidia, the saprophytic habitats in Ceratosporium and the ornamented conidia and plant parasitic behavior in Hirudinaria (Hughes 1951). Some species of Ceratosporium described later produce ornamented conidia (Matsushima 1981, 1993, Rao and Rao 1970). One of the species of Ceratosporium listed by Hughes (1951), C. fasciculare (Preuss) Sacc., was not available for study at that time. To our knowledge, the specimen described by Preuss has not been reexamined, although the specimens collected by Preuss were rediscovered in 1960 (Jülich 1974). A list of these specimens was compiled by Jülich (1974).

The genus Diplocladiella is characterized mainly by pigmented, simple, mononematous conidiophores and pigmented, "2-horned", septate conidia sympodially borne on integrated, cicatrized conidiogenous cells (Ellis 1976). The genus was erected by Arnaud (1954), with D. scalaroides as type species but without a Latin description. Valid and complete descriptions of the genus and the species were provided by Ellis (1976). The complicated typification of the type species was clarified by Mouchacca and Zucconi (1994). A table with conidium characteristics of five species was compiled by Cazau et al (1993). A key to Diplocladiella species was given by Santos-Flores and Betancourt-López (1997). An additional species was described by Lee et al (1998).

Stauroconidia appear to be adapted to dispersal by water (Bandoni 1972) and attachment to submersed substrata (Webster 1959). Whereas conidia of species of Diplocladiella G. Arnaud ex M.B. Ellis frequently are found in water samples (Santos-Flores and Betancourt-López 1997), species of Ceratosporium Schwein. and Hirudinaria Ces. predominantly are known from terrestrial habitats (Hughes 1951). Among these three genera, teleomorphs have been reported only for members of Ceratosporium, namely the pyrenomycetes Iodosphaeria polygoni W.H. Hsieh, C.Y. Chen & Sivan., I. phyllophila (Mouton) Samuels, E. Müll. & Petrini, and I. rigoponi Samuels, E. Müll. & Petrini (Hsieh et al 1997, Samuels et al 1987).

Our studies of saprophytic hyphomycetes in Taiwan revealed in the discovery of new reports and new species also including fungi with branched or appendaged conidia (Kirschner and Chen 2002, Kirschner et al 2001). In this study, two new species of staurosporous hyphomycetes are described and the taxonomic status of C. fasciculare is clarified.

	MATERIALS AND METHODS

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Microfungi on dead plant material on the ground in different areas of Taiwan were collected in 2002. The material was dried immediately after collecting. For light microscopy, material was mounted in 5% KOH. Measurements of conidia are reported as the maximum and minimum values of 20 measurements as well as the mean value—standard deviation—and the mean value plus the standard deviation. Free-hand drawings were made using scaled paper. For scanning electron microscopy, air-dried material was mounted directly and sputtered with gold for 60 s. Photographs were made with a Hitachi S 4500 scanning electron microscope (SEM) and processed with Digital Image Processing System 2.5.

	TAXONOMY

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Ceratosporium verrucosum R. Kirschner et C.-J.

Chen, sp. nov. FIGS. 1–5

View larger version (70K): [in this window] [in a new window]   FIGS. 1–3. Ceratosporium verrucosum. 1. Conidiophores and hyphae. 2. Developing conidia. Left: young conidia; right: two mature conidia, one of them apparently with only one arm (arrow), the other with three divergent arms (arrowhead). 3. Detached conidia. Note the conidium with three convergent arms (arrow) (and with a separate scale bar). One two-armed conidium is shown from the base (arrowhead). Scale bars in 1, 2 = 10 µm, 3 = 20 µm.

View larger version (131K): [in this window] [in a new window]   FIGS. 4, 5. SEM photographs of Ceratosporium verrucosum. 4. Conidium seen from the base with divergent, verrucose arms and the smooth basal cell with a hilum. 5. Two conidia with convergent arms that are completely covered by verrucose ornamentation. Scale bars = 20 µm.

HOLOTY PE: TAIWAN. HSINCHU. Chudong, Qingquan ("Clear Spring"), ca. 800 m, on dead bamboo culm, 3 Apr 2002, R. Kirschner & C.-J. Chen 1110 (TNM).

Colonies effuse, dark brown because of the presence of pigmented conidia. Hyphae pale brown, smooth, 1.5–2 µm diam. Conidiogenous cells intercalary or lateral, pale brown when young, dark brown when old, oblong or irregularly lobed, smooth, 6.5–8 x 4–6.5 µm (FIGS. 1, 2). Conidia solitary (FIGS. 2), basal cell single, smooth, with a large, hyaline hilum ca 2 µm diam, (1–)2–3 arms arising from the apex, easily detached from the basal cell. Arms divergent or convergent, dark brown, with terminal 1–3 cells pale brown, strongly verrucose over the length of the arms, (34–)39–46(–56) µm long, (12–)12.5–13.5 (–14) µm wide at base, tapering to apex, with 7–10 (–11) transverse septa, septa 1–2 µm thick, dark, apical 1–2 septa thinner and paler, distances between septa 1–6 µm (FIGS. 2–5).

Diplocladiella alta R. Kirschner et C.-J. Chen, sp. nov. FIGS. 6–12

View larger version (54K): [in this window] [in a new window]   FIGS. 6–8. Diplocladiella alta. 6. Habit sketch of conidiophores, some of them bearing conidia in different stages of development. Scale bar = 100 µm. 7. Details of conidiophores at higher magnification. Scale bar = 10 µm. Left: terminal and intercalary conidiogenous cells and a conidium seen from the side; middle: apex of a young conidiophore with a single, terminal conidiogenous cell and a developing conidium; right: base of a conidiophore. 8. Conidia. Scale bar = 20 µm.

View larger version (141K): [in this window] [in a new window]   FIGS. 9–12. SEM photographs of Diplocladiella alta. 9. Apical region of a conidiophore showing several conidiogenous scars and one developing conidium. 10. A cluster of detached conidia. 11. A conidium with one arm with an apical, short, filiform outgrowth. 12. Typical conidium. Scale bars in 9, 11, 12 = 10 µm, in 10 = 50 µm.

HOLOTY PE: TAIWAN. NANTOU. Hui Sun Lin Chang, ca. 700 m, on rotting wood on the ground, 21 Jul 2002, R. Kirschner & C.-J. Chen 1409 (TNM; ISOTY PE, FR).

Colonies dark brown, hair y. Mycelium light brown, hyphae 1.0–2.5 µm diam. Conidiophores macronematous, mononematous, smooth, erect, straight or slightly bent, apically geniculate, brown, becoming paler from the base to the tip, 116–329 µm long, 4–7.5 µm wide, septa 8–33 µm apart (FIGS. 6). Conidiogenous cells intercalary or terminal, 16–21 x 4–6 µm, forming a geniculate rachis 12.5–125 µm long, covered with flat, round, 3–4 µm wide conidiogenous scars (FIGS. 7, 9). Developing conidia subhyaline to pale brown, becoming brown during septation (FIGS. 6–8). Mature conidia (24–)32.5–42(–42.5) x (19–21.5–26(–26.5) µm, approximately trapeziform, each composed of 8 cells: one paler basal cell with a truncate, 3–4 mm wide basal scar, one central dark brown cell above the basal cell, supporting two arms each composed of two dark brown cells and of an apical cell that is light brown and mostly rounded, rarely extended into a filament (FIGS. 8–12). Cell walls of the dark cells of the conidia thickened.

Bactrodesmium submoniliforme Hol.-Jech., Folia Geobot. Phytotax. 7:416. 1972. FIGS. 13

View larger version (76K): [in this window] [in a new window]   FIGS. 13. Conidiophores and conidia of Bactrodesmium submoniliforme (type of Sporidesmium fasciculare Preuss). Scale bar = 10µm.

Colonies in the material mixed with pigmented hyphae and spores of other fungi. Conidiophores aggregated in sporodochia, micronematous, hyaline or pale brown, composed of subglobose or doliform cells 3–5 x 2–5 µm. Conidia arising directly from apparently undifferentiated cells, light to medium brown, cell walls swollen, with 6–9 transversal septa, (28.5–)35–45.5(–48) x (8–)9–10(–11) µm, distances between septa 3.0–6.5 µm.

Specimen examined – GERMANY. SACHSEN. Pinka near Hoyerswerda, on rotting conifer wood, C.G.T. Preuss No. 184 (= No. 223 in Jülich 1974) (HOLOTY PE of Sporidesmium fasciculare Preuss, B).

	DISCUSSION

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The conidia of the type species of Ceratosporium, C. fuscescens Schwein., are smooth (Ellis 1971, Hughes 1951, Matsushima 1975). Most of the species described later produce smooth conidia, namely C. caribense Hol.-Jech. (Holubová-Jechová 1988), C. cornutum Matsush. (Matsushima 1975, Matsushima 1981), C. palmiforme Matsush. (Matsushima 1971), C. productum Petch (Ellis 1971, Hughes 1951), and C. rilstonii S. Hughes (Hughes 1951). According to the illustrations of the unnamed Ceratosporium anamorphs of species of Iodosphaeria Samuels, E. Müll. & Petrini (Hsieh et al 1997, Samuels et al 1987), these anamorphs also have smooth conidia. The remaining three species of Ceratosporium produce verrucose conidia, namely C. aequatoriale Matsush. (Matsushima 1993), C. gracile Matsush. (Matsushima 1981), and C. indicum V. Rao & D. Rao (as "C. indica," Rao and Rao 1970). Compared with the ornamented conidia of C. verrucosum, however, the arms of the conidia of C. aequatoriale arise from a two-celled basal body of the conidium, are shorter and narrower and have fewer septa (Matsushima 1993); the arms of conidia of C. gracile and C. indicum are ornamented only at the base and are longer and narrower than in the new species (Matsushima 1981, Rao and Rao 1970).

To clarify the taxonomic status of Ceratosporium fasciculare, the type material was reexamined. The name C. fasciculare (Preuss) Sacc. was based on Sporidesmium fasciculare Preuss, which is a later homonym of S. fasciculare Corda and, therefore, invalid. The specimen deposited by Preuss is identical to Bactrodesmium submoniliforme Hol.-Jech.

Hirudinaria macrospora Ces. differs from the new species of Ceratosporium by narrower arms (6–8 µm at the base) and in being a leaf parasite (Hughes 1951). Because the genus Ceratosporium presently contains four species with verrucose conidia, this characteristic no longer can be used for separating Ceratosporium and Hirudinaria. Species of Ceratosporium, however, appear to be saprophytic, whereas H. macrospora is a specialized parasite on leaves of members of the Rosaceae, which seems to justify the separation of the genera (Hughes 1951).

Dwibahubeeja indica N. Srivastava, A.K. Srivastava & Kamal is another hyphomycete inhabiting living leaves and producing conidia similar to those of species of Ceratosporium (Srivastava et al 1995). In contrast to C. verrucosum, however, the conidia of the single species of Dwibahubeeja N. Srivastava, A.K. Srivastava & Kamal, are smooth (Srivastava et al 1995).

Diplocladiella alta differs from all other known species in Diplocladiella by having conidiophores longer than 100 µm. The conidiophores of the other known species do not exceed 90 µm (TABLE I). Conidiophore length appears to be a constant character in species of Diplocladiella in vivo, which was confirmed by several investigators for specimens of D. scalaroides collected in America, Asia and Europe (TABLE I). The conidiophores of Weufia tewoldei D.J. Bhat & B.C. Sutton, a species similar to those of Diplocladiella, exceed 200 µm in length and bear several conidiogenous scars on the conidiogenous cells (Bhat and Sutton 1985). The conidia of W. tewoldei are distoseptate in contrast to the euseptate conidia of species of Diplocladiella and have a different septation pattern (Bhat and Sutton 1985). The conidial shape of D. alta is most similar to that of D. scalaroides, the type species of the genus, because this is the only other species within Diplocladiella not regularly producing filiform appendages from the apical cells of the arms of the conidia (Santos-Flores and Betancourt-López 1997). The presence or absence of appendages in D. scalaroides may depend on the age of the conidia (Santos-Flores and Betancourt-López 1997). Although we examined many conidia of D. alta, we rarely found conidia with filiform appendages (FIG. 12). The conidia of D. scalaroides are narrower, and their arms are more distinctly marked off from each other and the central body (Arnaud 1954, Ellis 1976, Mouchacca and Zucconi 1994, Santos-Flores and Betancourt-López 1997).

	ACKNOWLEDGMENTS

 
We thank M. Piepenbring for critically reading the manuscript, W. Gams for providing data about the genera discussed here from his literature database, M. Ruppel for technical work with the SEM, and the Herbarium of Berlin (B) for the loan of type material. The study in Taiwan was supported by the Alexander von Humboldt Foundation and the National Science Council of Taiwan (NSC 91-2311-B-218-001).

	FOOTNOTES

 
Accepted for publication January 21, 2004.

¹ Corresponding author. E-mail: kirschner{at}em.uni-frankfurt.de

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This Article Abstract Full Text (PDF) Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Kirschner, R. Articles by Chen, C.-J. Search for Related Content PubMed Articles by Kirschner, R. Articles by Chen, C.-J. Agricola Articles by Kirschner, R. Articles by Chen, C.-J.