Mycologia, 106(3), 2014, pp. 448–455. DOI: 10.3852/12-260 # 2014 by The Mycological Society of America, Lawrence, KS 66044-8897

Tranzschelia in the Americas revisited: two new species and notes on the Tranzschelia thalictri complex Markus Scholler1

MATERIALS AND METHODS

Staatliches Museum fu ¨ r Naturkunde Karlsruhe, Abteilung Biowissenschaften, Erbprinzenstr. 13, 76133 Karlsruhe, Germany

Specimens.—We used dried herbarium specimens from these public herbaria: B, BPI, E, KR, M, MPPD, PUR, STU and Z (Holmgren, Holmgren and Barnett 1990). We also examined three specimens of T. thalictri from a private herbarium (herbarium V. Kummer; V.K.).

Mehrdad Abbasi Department of Botany, Iranian Research Institute of Plant Protection, P.O. Box 1454, Tehran 19395, Iran

Light microscopy (LM).—Spores or cross sections of sori from dried Tranzschelia specimens were mounted in lactic acid in glycerol (Kirk et al. 2001) and examined with a light microscope (Zeiss Axioskop 2 plus, Leitz Laborlux S) at 4003 or 10003 magnification. Fifty spores per specimen were selected arbitrarily and measured. Germ-pore number and position of urediniospores were evaluated with a new, simple technique: Spores were mounted in Hoyer’s medium (Cunningham 1972) and studied with phase contrast illumination at 4003 magnification. Specimens were photographed with a Jenoptik ProgRes CT3 digital camera attached to a Zeiss Axioskop 2 plus light microscope (Oberkochen) using differential interference contrast (DIC) and phase contrast as illumination techniques. Images were captured with ProgRes CapturePro 2.8.8 software.

Frank Friedrich Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces, Hermann-von-Helmholtz-Platz 1, 76344 Eggenstein-Leopoldshafen, Germany

Abstract: Two new species of Tranzschelia (Pucciniales) are described from the Americas. Tranzschelia pseudofusca is a microcyclic species on Anemone spp. (Ranunculaceae) with North American distribution. T. mexicana on Prunus salicifolia (Rosaceae) is found in Colombia, Ecuador and Mexico. It is assumed that T. mexicana is a macrocyclic host-alternating species. T. thalictri, a holarctic microcyclic species, has variable morphology and probably is an aggregate of related species. Specimens are documented with scanning electron microscopy (ESEM) and light microscopy including a simple new technique to illuminate urediniospore germ pores. Results are discussed with respect to similar species, distribution and life-cycle characters. A key for American species on telial hosts is provided. Key words: Anemone, Prunus, Pucciniales, Tranzschelia arthurii, T. mexicana, T. pseudofusca

Environmental scanning electron microscopy (ESEM).— Spores of dried specimens were placed on a holder with conductive double-sided tape (Leit-Tabs, Plano GmbH). Scanning electron microscope images were obtained with a Philips XL 30 FEG environmental microscope operated at acceleration voltages of 15 and 20 kV at a chamber pressure of 130 Pa. The design of the ESEM allows a preparation of the herbarium samples without complex drying procedures. Due to the design of the gaseous secondary electron detector (GSE), the sample preparation can be done without coating with carbon or gold, while under normal high vacuum SEM the samples would have been coated to avoid charge build up.

INTRODUCTION

TAXONOMY

The genus Tranzschelia (Pucciniales or Uredinales) was established by J.C. Arthur (1906). It consists of autoecious species on Ranunculaceae (microcyclic or macrocyclic) and of heteroecious macrocyclic species on Ranunculaceae (aecial host) and Prunoideae (telial host). A first overview of species in the Americas was published by Arthur (1934). Cummins and Stevenson (1956) and Lo´pez-Franco and Hennen (1990) reconsidered the genus Tranzschelia, and the latter authors accepted eight species. Here we describe two new species, one on Prunus salicifolia and one on Anemone spp.

Tranzschelia pseudofusca M. Scholler & M. Abbasi, sp. nov. FIG. 1 MycoBank MB805998 Spermogonia amphigenous, mainly hypophyllous, scattered among telia, black, absent in some material examined. Aecia and uredinia not produced. Telia amphigenous, mainly hypophyllous, rarely (on Anemone tetonensis) on petioles or stems, cinnamon-brown or dark brown, pulvinate and pulverulent, circular on leaves and elongated on stems. Teliospores nonfascicled, two-celled, cells not separating readily, oblong ellipsoid or broadly ellipsoid, 26.5–41.5 3 16–23.5 mm, constricted at septum, both cells more or less similar, oblate or spheroid, wall evenly 1–1.5 mm (rarely 2 mm) thick, verrucose, warts 1.0 mm high and

Submitted 16 Jul 2012; accepted for publication 13 Nov 2013. 1 Corresponding author. E-mail: [email protected]

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FIG. 1. Tranzschelia pseudofusca, on Anemone quinquefolia, teliospores. a. Ornament (USA, MIN 885893) (ESEM). b. Transverse section (USA, MIN885891) (LM, DIC).

1.2 mm wide, conical to echinulate, germ pore in upper cell apical or subapical and in lower cell near the pedicel, pedicels up to 40 mm, colorless, dehiscent, typically broken 2.5–3 mm below hilum. Onecelled teliospores present. Paraphyses marginal, rarely formed, hyaline, club-shaped to capitate, 25–35 3 8– 10.5 mm, wall 1.5–2.5(–4) mm thick, at apex sometimes up to 6.5 mm. Mycelium systemic, host plants sterile, deformed and etiolated. Etymology: The name refers to the similar species Tranzschelia fusca.

Holotype: On Anemone quinquefolia L., USA, MICHIGAN, Lima, 19.5.1917, C.A. Ludwig sub Polythelis fusca (PUR 6962), 0+III. Other material examined: Anemone lithophila Rydb.: USA, WYOMING, Jerry Park, 11 Jul1923, E.B. Payson, G.M. Armstrong, III (PUR 38992). A. nemorosa L., USA, NEW YORK, Alcove, Mai1893, C.L. Shear (BPI 067605), III; USA, IOWA, Decorah, May 1883, E.W. Holway, 0+III (M 100149); USA, WISCONSIN, Madison on campus, May 1887, leg. Anonymous, 0+III (BPI 0112620); USA, WISCONSIN, Madison, 19 May 1883, leg. Anonymous (from Missouri Botanical Garden), 0+III (BPI 0112621). A. parviflora Michx.: USA, IDAHO, Elk River, 13 Aug 1923, C.R. Stillinger, 0+III (PUR 6929). A. piperi Britt. ex Rydb.: USA, IDAHO, Pierce, Clearwater County, 15 Jul 1920, Posey, Stillinger, 0+III (PUR 6930). A. quinquefolia L., USA, OHIO, Carey, Wyandor County, 4 May 1902, T. Bonser (Z), III; USA, INDIANA, 5 miles E of Michigan, La Porte County, 5 Jun 1920, C.C. Deam, 0+III (M 100148); USA, MICHIGAN, Ann Arbor, 10.6.1913, E.B. Mains, 0+III (PUR 6953); USA, MINNESOTA, Hubbard County, one-half mile east of Badoura Nursery, 8 Jun 2003, J.V. Groth (MIN 885891), 0+III; Minnesota, Pine County, 30 May 2004, J.V. Groth (MIN 885893), III; USA, MINNESOTA,

Hubbard County, Lake George, 9 Jun 2011, J.V. Groth (MIN 885887) 0+III, mixed infection with Ochropsora ariae (Fuckel) Ramsb. 0+I. (MIN 885887). A. tetonensis Porter ex Britt.: USA, UTAH, Wasatch Mountains, near Emerald lake, Mount Timpanogos, 27 Jul 1925, Briant, Decker, III (PUR 6983, PUR 44637); USA, UTAH, Wasatch Mountains, Mount Timpanogos, Grinnell Lake, 27 Jul 1925, Briant, Decker, III (PUR 44636). Tranzschelia fusca specimens on Anemone nemorosa from various European countries (M-100150 (type), BPI 067602, BPI 067603, BPI 067624, KR-M-6780, KRM-10958, KR-M-12289, KR-M-0015320, M-100170, M100155) were used for comparative studies. Commentary: Autoecious microcyclic rusts on Anemone spp. in North America always were considered conspecific with the European T. fusca (G. Winter) Dietel on A. nemorosa (e.g. Sydow and Sydow 1904, Arthur 1934, Lo´pez-Franco and Hennen 1990). Our studies, however, have shown clear differences between the two species. T. pseudofusca sp. nov. has lighter and thinner teliospore walls (mostly 1–1.5 mm compared to. 2–2.5 mm) and slimmer and shorter warts and with conical instead of echinulate tips. Teliospore cells do not separate readily in T. pseudofusca, whereas in T. fusca they easily break at the septum (see TABLE I). We found club-shaped to capitate paraphyses in most specimens. But we cannot confirm the observation of Lo´pez-Franco and Hennen (1990 FIG. 34), that hypha-like septate paraphyses are formed as shown with PUR 6983. We restudied this specimen and found that these hyphal structures are not part of the rust but belong to a moldy nonparasitic hyphomycete. In the same specimen, however, we also found true paraphyses that are typical for this species. Often paraphyses are rare (e.g. in the holotype material). Telial paraphyses are never

450 TABLE I.

MYCOLOGIA Tranzschelia pseudofusca sp. nov. and T. fusca: host range, distribution and teliospore features T. pseudofusca a

Anemone host range

lithophila, nemorosa, parviflora, piperi, oregana, quinquefolia, tetonensis Distribution (natural range) North America Teliospores: length 3 width (mm) 26.5–41.5 3 16.5–23.5 wall thickness (mm) wall color wall ornamentation

1–1.5(2.0), evenly thick light chestnut-brown conical warts or echinulae, warts up to 1 mm high and 1.2 mm wide at base

T. fusca nemorosa Europec 31–46 3 17–27b, (29.5–)33–48(51–) 3 15.5(17–25(28)d 3b, 2–3d chestnut-brown echinulae, up to 1.5 mm high and wide at based

a

Anemone spp. within the nemorosa group of subgenus Anemone after Hoot and Recnizek (1994). After Ga¨umann (1959). c After Dupias (1971). d Our studies. b

formed in T. fusca. Lo´pez-Franco and Hennen (1990) measured pedicels up to 80(100) mm long, whereas we measured up to only 40 mm. Of note, the introduced European A. nemorosa also was found infected by T. pseudofusca. In its original range (Europe) this plant species is the principal host of T. fusca. Most probably T. pseudofusca is distributed all over the United States and southern Canada (see the records of T. anemones in Arthur 1934 p 73). Further studies are necessary to determine its current range. Teliospores of the Asian T. fusca separate easily and the wall is dark brown, which resembles T. fusca s.str., according to Hiratsuka et al. (1992). The difference between T. fusca and T. pseudofusca obtained from morphological data also is supported by rDNA (28S and ITS) sequence data. This will be published elsewhere (M. Scholler and M.C. Aime in prep). Tranzschelia mexicana M. Scholler & M. Abbasi, sp. nov. FIG. 2 MycoBank MB805999 Spermogonia and aecia unknown. Uredinia hypophyllous, orbicular, 0.2–0.4 mm, scattered on the entire leaf surface, soon naked, pulverulent, cinnamon or dark cinnamon brown, with intermixed and peripheral cylindrical, clavate or capitate paraphyses, paraphyses straight or incurved, mostly light chestnut brown, wall 1–3 mm thick, or up to 6.5 mm at apex. Urediniospores clavate, elongate-obovoid or fusiform, 28.5–53.5 3 (14.5–)17.5–22.5 mm, wall 1.5–2.5 mm thick at sides, 5–9.5 mm thick at apex, dark golden brown apically, clearly paler to hyaline below germ pores, wall echinulate except for the apex; distance between echinulae 2 mm near pedicel to 3 mm around germ pores, mostly upright, longest near base, shortest below apex, germ pores (2–)3–5(–6), mostly in equatorial or supra-equatorial position, sometimes scattered or bizonate. Telia hypophyllous, orbicular,

0.2–0.4 mm, dark chestnut brown with paraphyses like those in uredinia. Teliospores formed in uredinia or telia, in fascicles, two-celled, not separating readily, broadly obovoid, oblong or broadly ellipsoid, scarcely constricted at septum, (26.5–)30.5–40(–43.5) 3 (17.5–)20.5–24(–29) mm, wall light chestnut brown, 2.5–3.5 mm thick, slightly thicker around germ pores, uniformly verrucose, verrucae often wider, flatter and less dense in the lower cell, germ pore of upper cell apical or subapical, of lower cell equatorial, sometimes subequatorial, free part of pedicel 10–25 mm long, 7.5–11.5 mm wide, thin-walled, hyaline, dehiscent, breaking at the hilum or somewhat below. Etymology: Referring to southern Mexico, the natural area of distribution of the species.

Holotype: On Prunus salicifolia Kunth (5 P. capuli Cav. ex Spreng. 5 P. serotina ssp. capuli [Cav.] McVaugh), Mexico, Hidalgo, near Tula, 6 Oct 1896, E.W.D. Holway, II+III, E. Bartholomew, North American Uredinales 182 sub T. punctata (Pers.) Arthur (E 203123). All other specimens of the exsiccatae Bartholomew, North American Uredinales 182 including both, II and III, are proposed isotypes. The selected holotype includes numerous telia, although only uredinia are mentioned on the label. Also, duplicates in MIN (MIN 318931, 318937) include both spore types. Other material examined: Prunus salicifolia Kunth, MEXICO, Oaxaca, 22 Oct 1899, E.W.D. Holway (Sydow Uredineen 1530 as Puccinia pruni Pers., B 700010318, MIN 318934), II. ECUADOR, Pichincha, Guapulo, 9 Sep 1937, H. Sydow sub T. pruni-spinosae (Pers.) Diet. (ZT), II+(III); COLOMBIA, Bogota´, Jardı´n Bota´nico, Jul 1986, J. Hennen, R.M. Lo´pez-Franco (PUR 1090 sub T. arthurii), II+III. For comparison T. arthurii s. str. specimens from North America on Prunus serotina s. str. (PUR N1680, PUR N1682, PUR N1679, PUR 49609) and on P. virginiana (PUR no number!) were studied.

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FIG. 2. Tranzschelia mexicana, on Prunus salicifolia. a. Urediniospores, transverse section, (Ecuador, ZT) (ESEM). b. Urediniospores, transverse section (Mexico, E203123, holotype, also 2C–F), (LM, DIC). c. Urediniospores, arrows indicate five germ pores in one spore (right, below) in equatorial position (LM, phase contrast). d. Teliospores in fascicules, surface, ornament (LM, DIC). e. Teliospores in fascicles, transverse section (LM, DIC). f. Teliospores in fascicles, transverse section, arrows refer to germ pores in apical (upper cell) and equatorial (lower cell) position (LM, phase contrast). Bars 5 10 mm.

Commentary: In most specimens studied, uredinia were hyperparasitized by Eudarluca caricis (Biv.) O.E. Erikss. In these specimens, III were rarely or not formed at all. Arthur (1934 p 72) placed all Tranzschelia species on Prunus serotina s.l. (i.e. including Prunus salicifolia) and P. virginiana in T. pruni-spinosae. Later, Tranzschel and Litvinov (1939) described the rust on P. serotina from USA as separate species, Tr. arthurii. Lo´pez-Franco and Hennen (1990) accepted T. arthurii and, in addition, placed material on P. salicifolia in T. arthurii. T. mexicana seems to be restricted to P. salicifolia. Morphologically it differs from T. arthurii, which infects P. serotina s. str. and P. virginiana. Major morphological differences are teliospore features, such as size (T. arthurii 36.5–51 3 23–29 mm compared to 30.5–40 3 20.5–24 mm in T. mexicana), wall thickness at sides (2 mm compared to 2.5–3.5 mm), wall color (lighter brown in T. arthurii) and the constriction at the septum (deeply constricted in T. mexicana and weakly constricted in T. arthurii). Also

germ-pore number and position in the urediniospores are different (mostly three pores in supraequatorial position in T. arthurii compared to mostly 3–5 pores in equatorial or supra-equatorial position in T. mexicana). Finally, teliospores in T. arthurii are formed within uredinia and quickly replace urediniospores. Therefore, there are no urediniospores in most specimens including the lectotype (PUR 49609). In contrast true uredinia and telia are formed by T. mexicana. Sori are formed side by side that contain one spore type only (see TABLE II). It seems that the description of uredinia and urediniospores of T. arthurii by Lo´pez-Franco and Hennen (1990 p 570) is based on those specimens with P. salicifolia as telial host, (i.e. on material which we describe as a new species, T. mexicana). This is because, according to Lo´pez-Franco and Hennen (1990), T. arthurii has uredinia (although urediniospores are formed only rarely within telia) and because of the germ pore characters in urediniospores (‘‘3–5, commonly 4’’; however there are 2–4

452 TABLE II.

MYCOLOGIA Tranzschelia mexicana sp. nov. and T. arthurii: host range, distribution, sori and spore features T. mexicana a

Prunus host range Distribution (natural range) Sori Urediniospores: germ pore number (position) Teliospores: length 3 width (mm) wall thickness at sides (mm) constriction at septum a

salicifolia Central America II and III formed separately side by side 3–5 (equatorial to supra-equatorial) 30.5–40.0 3 20.5–24.0 2.5–3.5 weakly constricted

T. arthurii serotina, virginiana North America teliospores formed in II, III replace II (2)3(4) (supra-equatorial) 36.5–51.0 3 23.5–29 2 deeply constricted

Prunus spp. after Lo´pez-Franco & Hennen (1990).

with mostly 3 pores in T. arthurii). As mentioned above, T. mexicana has mostly brown cylindrical peripheral paraphyses that are present in telia as well. A cross section of telia in T. arthurii showed only some hypha-like and colorless paraphyses, which are different from those of T. mexicana. Transzchelia asiatica Y. Ono, a species from Japan (Ono 1994), bears some resemblance to T. mexicana as well. But there is a clear difference in teliospore and urediniospore size. These spores are larger in T. mexicana, and the urediniospore wall is thicker at the apex. Prunus salicifolia (capulin, Mexican black cherry) is an evergreen species with edible cherries native from Sonora to Chiapas and Veracruz and possibly also indigenous to western Guatemala. It has been cultivated in other parts of Central America and in Colombia, Ecuador, Peru and Bolivia and is extensively and abundantly naturalized (Morton 1987). T. mexicana spread and is established in other countries of the Americas where capulin is cultivated. We assume the species has a much wider distribution in the Americas than only those countries represented by our specimens. All specimens listed by Lo´pez-Franco and Hennen (1990 p 570) on P. salicifolia may belong to T. mexicana, including records from Guatemala, Peru and USA. The full life cycle of T. mexicana is unknown as is also true for several other Tranzschelia species forming II and III on Prunus. For such species we assume they are host-alternating when aecial hosts are in the vicinity of infected Prunus hosts, and, like T. discolor (a species of worldwide distribution with western Mediterranean origin), T. mexicana might have spread without its aecial host. In the Valley of Mexico there is one native species of Anemone, namely A. mexicana Kunth. (5 Anemonidium mexicanum (Kunth) Starod.). This species might be the aecial host. Tranzschelia thalictri (Chevall.) Dietel, Annales mycologici 20:31 (1922) ; Puccinia thalictri Chevall., Fl. Ge´n. Env. Paris (Paris) 1:417 (1826) ; Polythelis thalictri (Chevall.) Arthur, Res. Sci. Congr. Bot. Vienna 341 (1906)

; Tranzschelia thalictri (Chevall.) F. Kern & Thurst., Bulletin of the Pennsylvania Agricultural Experiment Station: 15 (1929) (nom. superfl.)

Together with T. pulsatillae (Opiz) Rostrup, T. thalictri is the only microcyclic species forming telia in fascicles. In the following, material from North America, Europe and Asia on various hosts is compared morphologically. Material examined: Thalictrum aquilegiifolium L., Germany, Sachsen, Erzgebirge, nature reserve ‘‘Zechengrund’’, 4 Aug 2004, W. Dietrich (KR-M-12349), III. Th. dasycarpum Fisch. & Ave´-Lall., USA, Kentucky, Lexington, 19 Aug 1916, F.J. McFarland (PUR 6985) 0+III. Th. dioicum L., USA, Wisconsin, 10 Jun 1920 (PUR 7003), 0+(II)+III. Th. exaltatum Gaudin, Germany, Wu¨rttemberg, Oberschwaben, Kressbronn am Bodensee, Jul 1923, K. Bertsch (STU), III. Th. fendleri Engelm. ex A. Gray, Arizona, Point Imperial, North Rim, Grand Canyon National Park, 27 Aug 1957, G.B. Cummins (PUR 56819), 0+III. Th. flavum L., Russian Federation (Russia), Karelia, Olonets, Gakrusk, at the river Svir, Jul 1898, J.I. Lindroth (BPI 107191), III; Germany, Wu¨rttemberg, Oberschwaben, Kressbronn am Bodensee, 17 Jun 1919, K. Bertsch (STU), 0+III; UK, Norfolk, wheat fen, 5 Aug 1958, R.W.G. Dennis (BPI 114233), III. Th. minus L., Germany, Mecklenburg-Vorpommern, prope Go¨hren in insula Ru¨gen, Fungi Europaei 2907, 7.1885, 0. Pazschke (BPI 114234) III; Germany, Thu¨ringen, Bad Frankenhausen, Napptal, 8 Jun 2001, V. Kummer (KR-M-2927) II+III; Switzerland, Tessin, Airolo, 3.10.1940, A. Volkart (ZT) III; China, Sichuan, Wuxi, 04 Aug 1994, S.X. Wie, J.Y. Zhuang (KR-M-14294 5 HMAS 70919), III; Beijing, Zoological Garden, 31 May 1934, Y.C. Wang (KR-M-14295 5 HMAS 8593), III; Japan, Kamikawa-mura, Prov. Ishikari, 13 Sep 1926, N. Hiratsuka (PUR 12046), III; Japan, Shiritori, S. Saghalien, 3 Aug 1928, N. Hiratsuka (PUR 625/ PUR F12047), III; Germany, Sachsen-Anhalt, Bad Frankenhausen, Napptal, 8 Jun 2001, V. Kummer (V.K. 156/4), III; Switzerland, Nante, Airolo, 1450 m, 3 Oct 1940, A. Volkart (ZT), III; Austria, Niedero¨sterreich, Hohe Wand, ca. 850 m, 21 Jun 1984, J.

SCHOLLER ET AL.: TRANZSCHELIA Poelt, P. Zwetko (ZT), III. Th. occidentale A. Gray, Jesophus Lakes, Custer County, 7000 ft., 3 Aug 1916, J.F. McBride, E.B. Payson (PUR 7021) ?0+III. Th. polycarpum S. Watson, USA, California, Hettenshaw Valley, 3000 feet, 3 Jul 1942, H.E. Parks, J.P. Tracy (PUR 53925), 0?+III. Th. simplex L., China, Heilongjiang, Yichun, 25 Jul 1956, T.N. Liou (KR-M-0014282 5 HMAS 43033), III; Russian Federation (Russia), Amur region, in a meadow on the river Char, flowing into river Amur, Jul 1895, Komarov (Fungi Rossiae Exsicc. 162, B 70-10320, BPI 107267), (II)+III, Th. simplex L. subsp. galioides (Nestl.) Korsh. (5 Th. bauhinii Crantz), Hungary, Budapest, Petnehazy, Jun 1927, G. von Moesz (F. Petrak, Mycotheca generalis, No. 910, ZT, M100265, M100266), III; Switzerland, St Gallen, Wegrain o¨stlich Sevelen, ca. 460 m, 15 May 1952, Walokoch (Z), III. Th. thunbergii DC, Japan, Tokachi, Shintoku, 5 Jul 1925 (BPI 114285), III. Th. sp., China, Shanxi, Mt Wutaishan, 13 Sep 1959, J.H. Yu, R. Liu (KR-M-0014297 5 HMAS 33551), III. Russian Federation (Russia), Uljanovsk (Simbirsk), Karsun Distr., 1885, W. Karjinsky (BPI 107119), III; Switzerland, Zu¨rich, Jul 1880, G. Winter (BPI 107120), III. Mycelium systemic, locally in leaves or rarely in whole plant. Spermogonia rarely present, hypophyllous, rarely epiphyllous, sometimes growing along the leaf veins, subcuticular, prominent, hemispherical, light brown when young to dark brown when mature in material from USA and Canada, according to Lo´pez-Franco and Hennen (1990). Uredinia not seen, urediniospores rarely in telia, few, broadly ellipsoid, 20.5–27.5 3 13.5–15.5 mm, wall golden, 1 mm, sometimes apically thickened, distantly echinulate, germ pores 1(–2) in supra-equatorial position. Telia hypophyllous, small, circular, dark brown or cinnamon brown, surrounded by host tissue as a cuplike structure, teliospores in fascicles, 27–57 3 16– 26 mm, variable size and shape, broadly obovoid, broadly ellipsoid or clavate, upper cell broadly ellipsoid, oblong, rarely globose, lower cell broadly obovoid or clavate, pore of upper cell apical or subapical, of lower cell from near pedicel to near the septum, encircled by a ring-like wall thickening, wall chestnut brown or brown (lower cell somewhat lighter), densely verrucose to echinulate, cones tend to be smaller and more widespread in lower cells, wall 2–2.5 mm thick, in some spores wall of upper cells are slightly thicker, in addition to two-celled spores, oneor three-celled spores may be formed as well. Pedicel hyaline, thin-walled, attenuated toward base. Peripheral paraphyses not common, yellowish and mostly clavate, wall evenly thick or thicker at apex. Commentary: The species is variable with respect to teliospore morphology. Also urediniospore morphology seems variable, although urediniospores are

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formed only rarely. The species originally was described from France on Th. flavum. Whereas germ-pore position in the lower teliospore cell and number of cells per teliospore is variable in specimens from all continents, some features seem to be restricted to North American specimens. Urediniospores have apically thickened cell walls in North American specimens, according to Lo´pez-Franco and Hennen (1990). We could not confirm this for European specimens. On the other hand, thickened cell walls were found in one specimen from easternmost Russia (BPI 107267; see Specimens examined). In general, urediniospore formation is more common in European material. Also, the cell wall around the lower cell teliospore germ pores seems different. Often it is conspicuously thickened in American material, whereas in Eurasian specimens it is less thickened or not thickened at all. Finally, spermogonia were found in some North American specimens but never in European ones. The type was reported from France on Th. flavum (Chevallier 1826). In his diagnosis (‘‘P. Thalictri N. pustulis hypogenis subrotundis epidermide cinctis demum passim confluentibus, sporidiis pallide rufis obtusis, pedicellis brevibus’’), Franc¸ois Fulgis Chevallier did not provide information on the features discussed. No type collections are available. They were either lost or Chevallier did not collect specimens at all. His collections are deposited in Paris (P) according to Index herbariorum (Holmgren, Holmgren and Barnett 1990). However, the specimen could not be traced by curators in either this or in the major French cryptogamic collection (PC). So in a future study of this complex an evaluation of molecular data and a neotypification will be necessary. Also, hostalternating ‘‘correlated species’’ according to the concept of Arthur (1921) have to be considered. In his ‘‘Manual of the rusts in United States and Canada’’ Arthur (1934 p 72) lists Thalictrum spp. as aecial hosts (of T. pruni-spinosae). In addition, three specimens are in KR (KR 27579, 27580, 27581) from Colorado (Boulder County, leg. E. Bethel as T. punctata Arthur) with 0 and I on Th. sp. and Th. dasycarpum. This aecidium is most probably neither T. punctata nor T. pruni-spinosae but part of the life cycle of a so far unknown host-alternating species (hetereu-form) and might be the ‘‘correlated species’’ of the North American T. thalictri. KEY TO TRANZSCHELIA SPECIES ON TELIOSPORE HOSTS FROM THE AMERICAS

1

19 2

Often formation of 0, not or only very rarely formation of II; on Anemone (incl. Hepatica and Pulsatilla), Clematis, Thalictrum (Ranunculaceae) . . . . . . . . . . . 2 Never formation of 0, always formation of II; on Prunus (Rosaceae) . . . . . . . . . . . . . . . . . . . . . . . 7 Teliospores not in fascicles, no eu-forms . . . . . . . 3

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Teliospores in fascicles or eu-form forming loose fascicles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 3 Telia not pulvinate, also formation of II (in the telia); USA (Texas), on Clematis pitcheri . . . . . . . . . . . . . . . . . . . . . . . T. viorniae (Arthur) Arthur 39 Telia pulvinate, no uredinia . . . . . . . . . . . . . . . . 4 4 Teliospore wall thin, up to 1(–1.5) mm, light brown, with widespread verrucae; Canada, USA, on Anemone spp. . . . . T. pseudofusca M. Scholler & M. Abbasi 49 Teliospore wall thicker, up to 2.5 mm, brown; native of Europe, not yet found but expected to be introduced in North America; on introduced Anemone nemorosa (and other species of the nemorosa group?) . . . . . . . . T. fusca (Pers.) Dietel 5 Eu-form: formation of aecia. Teliospores in loose fascicles, also one- and three-celled, SW USA and adjacent Mexico, on Anemone tuberosa, A. decapetala . . . . . . . . . . . . . . . T. cohaesa (Long) Arthur 59 Micro-form: no formation of aecia; USA, Canada . . . 6 6 Wall thickened around teliospore germ pores, germ pores apical, near the pedicel or equatorial; on Thalictrum spp. . . . T. thalictri (Chevall.) Dietel 69 Wall not thickened around teliospore germ pores, germ pores apical or near the pedicel, never equatorial; on Anemone patens. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T. pulsatillae (Opiz) Rostrup 7 Teliospores not in fascicles . . . . . . . . . . . . . . . . . 8 79 Teliospores in fascicles . . . . . . . . . . . . . . . . . . . . 9 8 Teliospore echinulae connected, wall 2–3 mm at sides; urediniospores 26–34 3 15–24 mm; USA, on Prunus spp. . . . . . . . . T. ornata Lo´pez-Franco & J. F. Hennen 89 Teliospore echinulae isolated, wall 1–2 mm at sides; urediniospores 22–40 3 15–23 mm, USA, Canada on Prunus spp. . . . . . . . . . T. prunispinosae var. americana Lo´pez-Franco & J.F. Hennen 9 Telia often not formed, teliospore germ pore of both cells near the septum, strongly thickened apically, wall of lower cell thickened at sides; urediniospores 22–40 3 12–20 mm, introduced, on Prunus spp., common on P. persica . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T. discolor (Fuckel) Tranzschel & M. A. Litv. 99 With other teliospore features, wall not strongly thickened apically; on Prunus serotina s.l. . . . . . 10 10 Teliospores strongly constricted at septum, pore of lower cell equatorial, subequatorial or by the pedicel, wall up to 2 mm, 36.5–51 3 23–29 mm; USA, Prunus spp., foremost on P. serotina s.str. . . . . . . . . . T. arthurii Tranzschel & M.A. Litv. 109 Teliospores hardly constricted, pore of lower cell mostly equatorial, wall 2.5–3.5 mm, 26.5–43.5 3 17.5–29 mm; Americas, outside Mexico rarely forming III, on P. salicifolia . . . . . . . . . . . . . . . . . . . . . . . . . . . T. mexicana M. Scholler & M. Abbasi

DISCUSSION Taxonomy and life cycles.—With the microcyclic T. pseudofusca sp. nov. (replacing T. fusca, a species restricted to Europe) and the host-alternating T.

mexicana described above, the number of known species is nine in the Americas and 16 worldwide (considering Cummins and Hiratsuka 2003, who accept ‘‘about 15 species’’ worldwide). All nine American species are known from North America, so this continent may be considered the center of diversity of the genus Tranzschelia. With this study, however, the taxonomic knowledge and species diversity in the Americas is still not complete. On the one side we do not know the aecial hosts of potentially heteroecious species (T. mexicana, T. ornata, T. pruni-spinosae var. americana), on the other side Tranzschelia aecia on Anemone species, in particular on A. quinquefolia and A. caroliniana (see Lo´ pez-Franco and Hennen 1990) and on Thalictrum (see commentary on T. thalictri) may not yet be assigned to a certain species. Future studies must emphasize species, which to date have been considered conspecific with Eurasian species. For example the North American T. thalictri might be different from T. thalictri from Europe, in parallel with the T. fusca complex. However, morphological differences are not as clear as in T. fusca/T. pseudofusca and additional studies and data (including sequence data) will be necessary to decide whether a splitting is necessary. This also may be considered for another microcyclic species, T. pulsatillae, and for the host-alternating T. prunispinosae s.l. Urediniospore germ pores.—Position and number of germ pores in urediniospores is an important morphological feature of rust species (e.g. Cummins 1956). A terminology of germ-pore position was compiled by Cummins and Hiratsuka (2003). Germpore characters may be most important for identification of rusts when teliospores are still not formed or not formed at all. Formation of III may be prevented by hyperparasites such as Eudarluca caricis (as shown for T. mexicana). There are also numerous hostalternating species that fail to form III in the absence of aecia host; for example the ‘‘plum rust’’ T. discolor, a species with worldwide distribution, often does not form III when Anemone coronaria is missing (e.g. Blumer 1960). Germ pores often may not be visible with common light microscopy techniques or it is time-consuming and laborious to evaluate a greater amount of spores, which is necessary to get statistically sound data. By using phase contrast light microscopy and Hoyer’s medium we could clearly visualize urediniospore germ pores of Tranzschelia (FIG. 2c) and many germ pores of T. mexicana and T. arthurii were counted and evaluated within a short time. Comparative studies with other media (water, lactophenol)

SCHOLLER ET AL.: TRANZSCHELIA have demonstrated that Hoyer’s works best. When using mature urediniospores this simple method works well with many species of the Pucciniaceae, whereas for species of the families Phragmidiaceae, Melampsoraceae and Coleosporiaceae visualization is poor or does not work at all and other techniques have to be developed. ACKNOWLEDGMENTS We thank the curators of public herbaria (B, BPI, PUR, M, MIN, STU, ZT) for loans, and W. Dietrich and Volker Kummer for providing specimens from personal collections, Roger Peterson and Greg Shaner for critically reading the manuscript and Studienstiftung Mykologie (Germany) for supporting a 6 mo stay of the second author at the Natural History Museum at Karlsruhe to study Tranzschelia.

LITERATURE CITED Arthur JC. 1906. Eine auf die Struktur und Entwicklungsgeschichte begru¨ndete Klassifikation der Uredineen. Re´sultats Scientifiques du Congres International de Botanique Vienne, 1905. Vienna. p 331–348. ———. 1921. New species of Uredineae XIII. Bull Torrey Bot Club 48:31–42, doi:10.2307/2480021 ———. 1934. Manual of the rusts in United States and Canada. Lafayette, Indiana: Purdue Research Foundation. Blumer S. 1960. Untersuchungen u¨ber die Morphologie und Biologie von Tranzschelia pruni-spinosae (Pers.) Dietel und T. discolor (Fuck.) Tranz. et Litv. Phytopathol Z 38:355–388, doi:10.1111/j.1439-0434.1960. tb03938.x Chevallier FF. 1826. Flore ge´ne´rale des environs de Paris. 1:1–674. Cummins GB. 1956. Host index and morphological characterization of the grass rusts of the world. Plant Dis Rep 237:1–52.

IN THE

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———, Hiratsuka N. 2003. Illustrated genera of rust fungi. 3rd ed. St Paul, Minnesota: APS Press. 240 p. ———, Stevenson JA. 1956. A check list of the North American rust fungi (Uredinales). Plant Dis Rep Suppl 240:109–193. Cunningham JL. 1972. A miracle mounting fluid for permanent whole mounts of microfungi. Mycologia 64:906–911, doi:10.2307/3757946 Dupias G. 1971. Essai sur la bioge´ographie des Ure´dine´es. Son apport a` la syste´matique. Bull Trimest Soc Mycol Fr 87:129–412. Ga¨umann E. 1959. Die Rostpilze Mitteleuropas mit besonderer Beru¨cksichtigung der Schweiz. Beitr Kryptogamenflora Schweiz 12:1–1407. Hiratsuka N, Sato S, Katsuya K, Kakishima M, Hiratsuka Y, Kaneko S, Ono Y, Sato T, Harada Y, Hiratsuka T, Nakayama K. 1992. The rust flora of Japan. Ibaraki, Japan: Tsukuba Shuppankai. 1207 p. Holmgren PK, Holmgren NH, Barnett LC. 1990. Index herbariorum 1. 8th ed. New York: New York Botanical Garden. 693 p. Kirk PM, Cannon PF, David JC, Stalpers JA. 2001. Dictionary of the Fungi. 9th ed. Egham, UK: CABI Bioscience. 655 p. Lo´pez-Franco RM, Hennen JF. 1990. The genus Tranzschelia (Uredinales) in the Americas. Syst Bot 15:560–591, doi:10.2307/2419155 Morton J. 1987. Capulin. In: Fruits of warm climates. Miami, Florida: Julia F. Morton. (Online: http://www.hort. purdue.edu/newcrop/morton/capulin.html#Origin and Distribution). p 108–109. Ono Y. 1994. Tranzschelia asiatica sp. nov. and its taxonomic relationship to Tranzschelia arthurii. Can J Bot 72:1178–1186, doi:10.1139/b94-144 Sydow P, Sydow H. 1904. Monographia Uredinearum. Vol. I, Genus Puccinia. Leipzig, Germany: Gebru¨der Borntra¨ger. 972 p. Tranzschel W, Litvinow M. 1939. Rust fungi of the genus ˇ urn SSSR 24:247– Tranzschelia Arth. on Prunus. Bot Z 253.

Tranzschelia in the Americas revisited: two new species and notes on the Tranzschelia thalictri complex.

Two new species of Tranzschelia (Pucciniales) are described from the Americas. Tranzschelia pseudofusca is a microcyclic species on Anemone spp. (Ranu...
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