Abstract
A new species of Puccinia with diorchidioid teliospores is described from Urochloa decumbens (Poaceae) in Panama. It differs from the other known species of Puccinia with diorchidioid teliospores by uredinia with paraphyses and urediniospores with 3–4 scattered germ pores. Twenty-one known species of rust fungi are cited for Panama for the first time. Alveolaria cordiae is a poorly known species which is reported, described and illustrated in detail for the first time on Cordia spinescens in Panama.
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Introduction
Although the Pucciniales are the largest order of plant parasitic fungi among Basidiomycota, including about 9,000 species, numerous unknown species are supposed to exist, especially in the tropics (Shivas and Hyde 1997). Up to 2005, 67 species of rust fungi were known for Panama (Piepenbring 2005, 2006). Based on recent fieldwork, 91 species of Pucciniales are now known from Panama (Hernández et al. 2007). Nevertheless, numerous new records and new species can still be expected as result of ongoing fieldwork in this country because of its high diversity of vascular plants (9,500 species; Correa et al. 2004). In the present publication, 21 species of rusts are reported for the first time from Panama as well as one new species of Puccinia.
Puccinia is the largest genus of Pucciniales, with about 3,000–4,000 species. Species of Asteraceae, Cyperaceae, Poaceae, and Liliaceae s. l., are hosts for large numbers of species, but numerous other species of Puccinia infect plant species of most other groups of vascular plants.
The descriptive term “diorchidioid” (Latin: two testicles) is used for two-celled teliospores with a vertical or near vertical septum (Cummins 1971). Rust fungi with diorchidioid teliospores on dicotyledonous host species are classified in Diorchidium, those on Poaceae in Puccinia (Cummins and Hiratsuka 2003).
Materials and methods
Specimens of rust fungi were collected in the province of Chiriquí in Western Panama during 2003–2007. The identification of host plants is based on keys in literature (Sevenso 1943; Yuncker 1950; Amshoff 1958; Mathias and Constance 1959; Dwyer 1965; Robyns 1965; Nowicke 1969; Woodson and Schery 1960; Stuessy 1975; Webster and Burch 1976; Cuatrecasas 1980; for Poaceae, Morales 2003) and comparisons with specimens in the National Herbarium in Panama City (PMA).
Spores and handmade sections of sori were mounted in lactophenol and heated to boiling. They were examined with a Leitz Ortholux II light microscope (LM). Sizes in the species description are based on at least 25 measurements of each structure. Spore measurements include mean±SD with extreme values in parentheses. For scanning electron microscopy (SEM), air-dried material was mounted directly onto a specimen stub and sputtered with gold for 60 s. Photographs were made with a Hitachi S 4500 scanning electron microscope and processed with Digital Image System 2.5. The terminology proposed by Cummins and Hiratsuka (2003) was used to describe the life-cycle states. Collections were deposited at the Herbario Nacional of the Universidad de Panamá (PMA) and at the Botanische Staatssammlung München (M).
Results
Puccinia urochloae Perd.-Sánch. & M. Piepenbr., spec. nov. (Figs. 1, 2, 3, 4, 5 and 6).
Type. On leaves of Urochloa decumbens (Stapf) R. D. Webster (Poaceae; det. M. Piepenbring). PANAMA. Chiriquí Province, Corr. Río Sereno, road to Piedra Candela, 18.I.2007, T. Trampe et al. ppMP 986 [II,III] (holotype PMA, isotype M).
Spermogonia et aecia non visa. Uredia amphigena, subepidermalia, 0.2–0.6 mm diam., erumpentia, plana, pulveracea, cinnamomea vel castanea, epidermide rupta conspicua, paraphysibus cylindricis, laevibus, tenuitunicatis, hyalinis, 70–90 × 3–7 μm. Urediosporae globosae vel subglobosae, echinulatae, (30–) 32–36 (−40) × (25–) 27–32 (−34) μm, pariete cinnamomo, 1.5–2 μm lato, 3–4 poris germinationis disjectis, pedicello deciduo, cylindrico, laevi, tenuitunicato, hyalino, 40–55 × 5–5.5 μm.
Telia amphigena, maximam partem abaxialia, subepidermalia, 0.2–1.5 mm diam., interdum gregaria, erumpentia, mature exposita, pulveracea, cinnamomea vel atrobrunnea, epidermide rupta conspicua, interdum in urediis producta. Teliosporae 2-cellulares, septo longitudinali, (26–) 27–33 (−36) × (30–) 36–40 (−41) μm, ellipsoideae, late ellipsoideae, typice diorchidioideae, laeves, pallide cinnamomeae vel atrobrunneae, pariete laterali 2–2.5 μm lato, pariete apicali ca. 8 μm lato, una pora germinationis inconspicua apicali per cellulam, pedicello persistenti, cylindrico, laevi, tenuitunicato, hyalino, pallide ad apicem, 100–130 × 5–8 μm. Basidia et basidiosporae non visae.
Etymology: named after the host genus, Urochloa (Poaceae).
Spermogonia and aecia not seen. Uredinia amphigenous, subepidermal, 0.2–0.6 mm diam., erumpent, flattened, pulverulent, cinnamon-brown or chestnut-brown, ruptured epidermis conspicuous, with cylindrical paraphyses, smooth, thin-walled, hyaline, 70–90 × 3–7 μm. Urediniospores globose or subglobose, (30–) 32–36 (−40) × (25–) 27–32 (−34) μm, wall cinnamon-brown, echinulate, 1.5–2 μm thick, with three to four scattered germ pores. Pedicel deciduous, cylindrical, smooth, thin-walled, hyaline, 40–55 × 5–5.5 μm.
Telia amphigenous or mostly on abaxial surface, subepidermal, 0.2–1.5 mm diam., sometimes gregarious, becoming erumpent, early exposed, pulverulent, cinnamon-brown to dark brown, ruptured epidermis conspicuous, sometimes telia produced in the uredinia. Teliospores 2-celled by longitudinal septum (diorchidioid), (26–) 27–33 (−36) × (30–) 36–40 (−41) μm (length × breadth), ellipsoidal to broadly ellipsoidal, smooth, pale cinnamon-brown to blackish brown, lateral wall 2–2.5 μm thick, the apical wall ca. 8 μm thick, with distal inconspicuous germ pore in each cell. Pedicel persistent, cylindrical, smooth, thin-walled, hyaline, slightly yellowish next to the spore, 100–130 × 5–8 μm. Basidia and basidiospores not seen.
Discussion of the new species
Several species of Puccinia on Poaceae have diorchidioid teliospores. They are summarized in Tables 1 and 2. Urochloa species have hitherto only been reported as hosts for Puccinia negrensis.
Puccinia levis is morphologically close to Puccinia urochloae by similar teliospore size (Table 2). In Puccinia levis var. levis, P. levis var. goyazensis, and P. levis var. tricholaenae, however, the urediniospores have two pores in flattened sides and P. levis var. panici-sanguinalis has three equatorial pores. These varieties additionally differ from Puccinia urochloae by narrower urediniospores and somewhat longer teliospores. The new species is characterized by urediniospores with 3–4 scattered germ pores in contrast to the other species of Puccinia with 4–6, 6–8, 7–8, or 8 scattered germ pores. Puccinia urochloae differs from most species by abundant paraphyses in the uredinia. Only Puccinia eylesii and P. orientalis have paraphyses. The paraphyses of P. eylesii (24–50 μm long) are, however, capitate and the urediniospores have eight scattered germ pores. The paraphyses of P. orientalis are shorter and wider (45 × 13–18 μm), and the urediniospores have two pores next to the hilum. Puccinia urochloae is distinct because the paraphyses are cylindrical, long and narrow (70–90 × 3–7 μm).
New host records from Panama
Alveolaria cordiae Lagerh., Ber. Dtsch. Bot. Ges. 9: 346. 1891. (Figures 7, 8, 9, 10, 11, 12 and 13)
Type. On Cordia sp. (Boraginaceae). Ecuador, Guayas Province, Playas X.1890, Lagerheim s. n. (PUR F8749).
On Cordia spinescens L. (Boraginaceae). Panama. Chiriquí Province, Corr. Río Sereno, road to Piedra Candela, 1,400 m, 8°51.4′N, 82°45.3′W, 29 Mar 2006, M. Piepenbring et al. ppMP 785 [III,IV].
Spermogonia, aecia, and uredinia not seen., leaf spots yellowish-orange of 3–9 mm diam. Intracellular haustoria observed in the mesophyll cells. Telia hypophyllous, subhypodermal, becoming erumpent as catenulate columns formed by discs of spores, 8–40 columns arranged in concentric rings. Each column approx. 1 mm long and 150–175 μm wide, formed by approx. 9–17 and more discs, columns apically breaking into groups of discs. One disc is formed by 68–84 teliospores, in lateral view 7–8 (−9) teliospores visible, firmly united in each layer, each disc 150–175 × (47–) 48–50 (−56) μm, orange-red as seen with the dissecting microscope. Teliospores oblong, 1-celled, (47–) 48–52 (−56) × (19–) 20–22 (−24) μm, lateral wall 1.5–2 μm thick, distal wall approx. 2.5–3 μm thick, the proximal wall 2–3 μm, and the corners of the proximal wall 3–5 μm, smooth, yellowish to light brown, with apical germ area. All teliospores of one disc germinate simultaneously forming a dense layer of basidia.
Basidia external, originating from the distal end of teliospores integrated in the discs, as seen with the dissecting microscope in mass yellow, hyaline as seen by light microscopy, one basidium with three septa, 54 (−63) × (12–) 15 μm, smooth, wall up to 1 μm thick. Sterigmata 20–30 × 4–5 μm, hyaline. Basidiospores oblong with prominent apiculus, (14–) 18–22 (−23) × (10–) 11–12 (−13) μm, wall 1 μm thick, smooth, hyaline.
Other specimens examined
Alveolaria cordiae Lagerh., on Cordia sp. (Boraginaceae). Ecuador. Guayas Province, X.1890, G. Lagerheim (type PUR F8749, lectotype PUR F8750) [III,IV]. On Cordia corymbosa Willd. ex Roem. & Schult. Panama. (Prov. not cited), Farm No. 1, 1.VII.1921, M. A. Carleton 276 (BPI 0150226) [III]; on Cordia ferruginea (Lam.) Roem. & Schult. Panama. Colón Province, Tumba Muerto Road, 6.I.1924, P. C. Standley 29814 (BPI 0150234) [III,IV]; Panama. Colón Province, between France Field, Canal Zone and Catival, 9.I.1924, P. C. Standley 30431 (BPI 0150236) [III,IV]; Panama Province, between Las Sabanas and Matías Hernández, 21.I.1924, P. C. Standley 31802 (BPI 0150235) [III,IV].
Alveolaria andina Lagerh., on Cordia sp. (Boraginaceae). Ecuador. Pichincha Province, Corazon, X.1981, G. Lagerheim (lectotype PUR F8753) [0,III]; on Cordia rosei Killip. Ecuador. Tungurahua Province, San Antonio, Baños, XII.1937, H. Sydow n.n. (BPI 0056142) [III,IV]; on Cordia scaberrima Kunth. Ecuador. Tungurahua Province, San Antonio, Baños, 5.XII.1937, H. Sydow 1118 (BPI 0150193) [III,IV].
Notes
Alveolaria cordiae was collected in Panama on Cordia spinescens (Boraginaceae). This rust belongs to a poorly known genus established by Lagerheim (1891) with the type species, A. cordiae Lagerh., on Cordia sp. collected in Ecuador and a further species, A. andina Lagerh., on Cordia spp. Later, only Buriticá & Hennen (1980) studied species of this genus. Species of Alveolaria differ from other rusts by disc-shaped groups of teliospores without intercalary cells. During the development of the discs, the teliospores of Alveolaria spp. are catenulate.
The identification of the specimen from Panama was difficult because up to now few specimens and data on species of this genus are available. A. cordiae is presented here with an emended description and illustrations.
A. cordiae was reported from Cordia acuta Pittier, C. boissieri C. DC., C. curassavica (Jacq.) Roem. & Schult., C. cylindrostachya (Ruíz & Pav.) Roem. & Schult., C. ferruginea (Lam.) Roem. & Schult., C. laxiflora Kunth, C. riparia Kunth, C. sp., C. spinescens L., C. tarmensis Krause, and Gerascanthus bicolor (A. DC.) Borhidi (Arthur 1916, 1918a, b; Berndt 2004; Buriticá 1991; Buriticá and Pardo Cardona 1996; Chardon and Toro 1930; Dale 1955; Gallegos and Cummins 1981; Jackson 1931; Kern et al. 1933; Mains 1939; Minter et al. 2001; Pardo Cardona 1994, 1998a, b; Salazar and Buriticá 2002; Spaulding 1961).
The telia of Alveolaria andina are rather similar to those of A. cordiae as seen by the dissecting microscope. A. andina differs from A. cordiae by more teliospores per disc and longer teliospores (Table 3 and Figs. 14, 15, 16 and 17). Basidia and basidiospores of A. cordiae are reported, described and illustrated here for the first time.
New records of species of rusts in Panama
During fieldwork in Panama in 2003–2007 the following species were collected, identified, and are reported here for the first time from Panama.
Aecidium psychotriae Henn., on Psychotria cf. carthagenensis Jacq. (Rubiaceae). Panama. Chiriquí Province, Corr. Dolega, Los Algarrobos, border of Río Majagua, 140 m a.s.l., 8.X.2005, M. Piepenbring 3607 [I].
Coleosporium verbesinae Dietel & Holw., on Verbesina gigantea Jacq. (Asteraceae). Panama. Chiriquí Province, Volcán, Balneario, 11.III. Mar 2004, M. Piepenbring & O. Cáceres 3397 and 3398 [II]; Chiriquí Province, Corr. Río Sereno, road to Piedra Candela, 8°51.4′N, 82°45.3′W, 1,400 m a.s.l., 08.X.2005, M. Piepenbring et al. ppMP 620 [II]; ibidem, 21.VI.2006, R. Mangelsdorff et al. ppMP 279 [II]; ibidem 18.I.2007, R. Mangelsdorff et al. ppMP 1436 [II].
Crossopsora byrsonimatis (Henn.) R. S. Peterson, on Byrsonima crassifolia Steud. (Malpighiaceae). Panama. Chiriquí Province, Corr. Río Sereno, road to Piedra Candela, 20.XI.2004, M. Piepenbring et al. 3463 [II,III,IV]; ibidem, 8.X.2005, M. Piepenbring et al. 3637 [I,II,III,IV]; ibidem, 29.III.2006, M. Piepenbring et al. 3735 [I]; ibidem 31.I.2007, M. Piepenbring et al. 3861 [I,III,IV]. Only asexual stage: Uredo notata Arthur. Chiriquí Province, close to the town Caldera, 20.XI.2004, M. Piepenbring et al. 3463b [II].
Puccinia caricis-polystachyae Dietel, on Carex polystachya A. Rich. (Cyperaceae). Panama. Chiriquí Province, close to Boquete, Finca Arco Iris, 24.III.2006, M. Piepenbring et al. ppMP 763 [II,III].
Puccinia cordiae Arthur, on Cordia alliodora (Ruiz & Pav.) Oken (Boraginaceae). Panama. Chiriquí Province, Corr. Dolega, Los Algarrobos, 04.X.2005, M. Piepenbring et al. ppMP 0608 [II,III]; ibidem, 21.III.2006, M. Piepenbring et al. ppMP 726 [III].
Puccinia cyperi-tagetiformis (Henn.) F. Kern, on Cyperus odoratus L. (Cyperaceae). Panama. Chiriquí Province, close to Boquete, Finca Arco Iris, next to brook, 8°48′N, 82°25.6′W, 1,270 m a.s.l., 27.VI.2006, R. Mangelsdorff et al. ppMP 212 [II,III].
Puccinia enixa Cummins, on Baccharis cf. pedunculata (Miller) Cabrera (Asteraceae). Panama. Chiriquí Province, road from Gualaca to Almirante, Fortuna Reserve, 8°41,9′N, 82°13,75′W, 1,270 m a.s.l., 23.II.2007, R. Mangelsdorff et al., ppMP 1500 [I,II,III].
Puccinia inaudita H.S. Jacks & Holw., on Wedelia inconstans D’Arcy (Asteraceae). Panama. Chiriquí Province, close to Boquete, Finca Arco Iris, 1,400 m a.s.l., 27.VI.2006, R. Mangelsdorff et al. ppMP 197 [I,III]; Chiriquí Province, Corr. Río Sereno, road to Piedra Candela, 8°51.4′N, 82°45.3′W, 1,400 m a.s.l., 21.VII.2006, R. Mangelsdorff et al. ppMP 1440 [I,III].
Puccinia paupercula Arthur, on Elephantopus mollis H. B. & K. (Asteraceae). Panama. Chiriquí Province, Corr. Dolega, Los Algarrobos, 4.X.2005, M. Piepenbring et al. ppMP 602 [III]; on Pseudelephantopus spicatus (Juss. ex Aubl.) C. F. Baker (Asteraceae). Chiriquí Province, Corr. Dolega, Los Algarrobos, 8°50′N, 82°29′W, 140 m a.s.l., 13.IX.2005, O. Perdomo et al. 1722 [II,III]; ibidem, 8°29′N, 82°29.9′W, 140 m a.s.l., 8.I.2007, R. Mangelsdorff et al. ppMP 282 [III].
Puccinia psidii G. Winter, on Syzygium jambos (L.) Alston, (Myrtaceae). Panama. Chiriquí Province, Corr. Río Sereno, road to Piedra Candela, 29.III.2002, M. Piepenbring et al. 3736 [II]; ibidem, 8°51,4′N,82°45.3′W, 1,400 m a.s.l., 21.VII.2006, R. Mangelsdorff et al. ppMP 275 [II,III]; ibidem, 8°48.5′N, 82°25.6′W, 1,270 m a.s.l., 12.I.2007, R. Mangelsdorff et al. ppMP 1412 [II,III]; ibidem, 8°51.4′N, 82°45.3′W, 1,400 m a.s.l., 18.I.2007, R. Mangelsdorff et al. ppMP 1443 [II,III]; Chiriquí Province, David, UNACHI, 140 m a.s.l., 6.II.2007, O. Perdomo 1862 [II,III]; ibidem, 1.III.2007, M. Piepenbring & C. Iglesia 3885 [II,III].
Pucciniosira dorata Buriticá & Hennen, on Triumfetta bogotensis DC. (Malvaceae). Panama. Chiriquí Province, Boquete, Bajo Mono, close to entrance, 6.XI.2005, M. Piepenbring et al. 3682 [III]; Chiriquí Province, Boquete, Finca Arco Iris, 24.III.2006, M. Piepenbring et al. ppMP 754 [III].
Uredo hydrocotyles (Link) Buriticá, on Hydrocotyle mexicana Cham. & Schltdl. (Apiaceae). Panama. Chiriquí Province, close to Boquete, Finca Arco Iris, 10.XI.2005, M. Piepenbring et al. ppMP 0658 [II].
Uredo incomposita F. Kern, on Eleocharis sp. (Cyperaceae). Panama. Chiriquí Province, Bajo Mono, 8°49′N, 82°29′ W, 1,503 m a.s.l., IX. 2005, M. Vega 415 [II].
Uredo jatrophicola Arthur, on Jatropha curcas L. (Euphorbiaceae). Panama. Chiriquí Province, Corr. Dolega, Los Algarrobos, close to Casa de la Alemana, 25.VIII.2005, M. Piepenbring 3508 [II].
Uredo kyllingae Henn., on Kyllinga cf. odorata Vahl. (Cyperaceae). Panama. Chiriquí Province, Corr. Dolega, Los Algarrobos, XII.2006, M. Vega 418 [II].
Uredo melinidis F. Kern, on Melinis minutiflora P. Beauv. (Poaceae). Panama. Chiriquí Province, Corr. Río Sereno, 29.III.2006, M. Piepenbring et al. ppMP 772 [II]; Chiriquí Province, road to Piedra Candela, 1,400 m a.s.l., 8°51.4′N,82°45.3′W, 18.I.2007, R. Mangelsdorff et al. ppMP 1441 [II].
Uredo peperomiae Henn., on Peperomia cf. glabella A. Dietr. (Piperaceae). Panama. Chiriquí Province, Alto Chiquero, 10.XI.2005, M. Pipenbring et al. ppMP 638 [II].
Uredo proeminens DC., on Euphorbia heterophylla L. (Euphorbiaceae). Panama. Chiriquí Province, La Barqueta, 5 m a.s.l., 18.X.2005, M. Piepenbring ppMP 676 [II]. On Euphorbia hyssopifolia L., (Euphorbiaceae); ibidem, 19.X.2005, R. Mangelsdorff et al., ppMP 70 [II]; Chiriquí Province, Corr. Dolega, Los Algarrobos, 8°29.7′N, 82°25.9′W, 140 m a.s.l., 21.VI. 2006, R. Mangelsdorff et al. ppMP 176 [II]; ibidem, 21.VI.2006, R. Mangelsdorff et al. ppMP 177 [II].
Uredo rubescens Arthur, on Dorstenia contrajerva L. (Moraceae). Panama. Chiriquí Province, Corr. Dolega, Los Algarrobos, Quebrada Cermeño, 140 m a.s.l., 9.XI.2004, T. Trampe & R. Mangelsdorff 9 [II]; ibidem, 8°50′N, 82°29′W, 13.IX.2005, O. Perdomo et al. 1725 [II]; ibidem, 8.IX.2007, T. Hofmann TH 529 (II).
Uromyces bidenticola Arthur, on Bidens pilosa L. (Asteraceae). Panama. Chiriquí Province, Volcan Barú National Park, Los Quetzales trail, 2,000–2,450 m a.s.l., 15.II.2003, M. Piepenbring & R. Kirschner 3141 [0,II]; Chiriquí Province, Corr. Río Sereno, 8.X.2005, T. Hofmann et al. ppMP 360 [II]; Chiriquí Province, close to Boquete, Finca Arco Iris, 1,270 m a.s.l., 8°48.5′N, 82°25.6′W, 10.XI.2005, M. Piepenbring et al. ppMP 647 [II,III]; ibidem, 24.III.2006, T. Hofmann et al. ppMP 495 [II,III]; ibidem, 27.VI.2006, R. Mangelsdorff et al. ppMP 199 [II,III]; Chiriquí Province, Corr. Río Sereno, road to Piedra Candela, 29.III.2006, M. Piepenbring et al. ppMP 773 [II,III]; Chiriquí Province, Piedra Candela, 1,400 m a.s.l., 8°51′N, 82°45.3′W, 21.VII.2006, R. Mangelsdorff et al. ppMP 280 [II,III]; ibidem, 18.I.2007, R. Mangelsdorff et al. ppMP 1434 [II,III].
Uromyces trifolii-repenti (Castagne) Liro, on Trifolium repens L. (Fabaceae). Panama. Chiriquí Province, close to Boquete, Finca Arco Iris, 24.III.2006, M. Piepenbring et al. ppMP 764 [II,III].
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Acknowledgements
We are grateful to R. Berndt for helpful for confirming the new species. We thank R. Kirschner for critically reading the manuscript and for the Latin diagnosis. M. Ruppel is thanked for technical work of SEM, and the Herbaria BPI and PUR for loan of material. M. Vega, T. Trampe, R. Mangelsdorff, and T. Hofmann are thanked for contributing collections of rusts and R. Mangelsdorff for identification of host plants. The present study was supported by the DAAD (German Academic Exchange Service), DFG (German Research Society), the UNACHI (Universidad Nacional Autónoma de Chiriquí, Panama) and the ANAM (Autoridad Nacional del Ambiente, Panama).
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Perdomo-Sánchez, O., Piepenbring, M. A new species of Puccinia (Pucciniales, Basidiomycota) and new records of rust fungi from Panama. Mycol Progress 7, 161–168 (2008). https://doi.org/10.1007/s11557-008-0561-5
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DOI: https://doi.org/10.1007/s11557-008-0561-5