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 2

Catalogue of the species of plant rust fungi (Uredinales) of Brazil

By

Joe F. Hennen Botanical Research Institute of Texas, 509 Pecan Street, Fort Worth, Texas 76102-4060, United States of America

Mario B. Figueiredo Instituto Biológico de São Paulo Rua Cons. Rodrigues Alves 1252, Vila Mariana, São Paulo, S.P., Brazil, 04014-002

Aníbal A. de Carvalho, Jr. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro Rua Pacheco Leão, 915, Jardim Botânico, Rio de Janeiro, R. J., Brazil, 22260-030

Philip G. Hennen Botanical Research Institute of Texas, 509 Pecan Street, Fort Worth, Texas 76102-4060, United States of America

Support:

FAPESP CNPq FAPERJ N S F USDA

2005

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Acknowledgements. The authors wish to thank the many people and Institutions who have helped them during the years that they have been doing research on the plant rust fungi of Brazil. For financial aid this includes FAPESP, CNPq, and FAPERJ in Brazil, and NSF, and USDA in the United States of America. Our institutions: Instituto Biológico de São Paulo, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Purdue University and the Arthur Herbarium, and The Botanical Research Institute of Texas have provided many essential herbarium, laboratory, and library facilities. For assistance in field work we have had the permissions and help of Instituto Florestal de São Paulo, Fundacão Florestal de São Paulo, Instituto de Botânica de São Paulo, Museu Costa Lima of Macapa, Amapá, and Museo Goeldi of Belém do Para. We thank especialy Mary M. Hennen, coauthor of the first “Index of the rusts (Uredinales) of Brazil”, who continued to help throughout the development of this new work, Vera Lucia Bononi for aid in various ways, and Silvana D’Agostini of the Instituto Biológico for artistic work.

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TABLE OF CONTENTS Pg. Introdution 007 Genera of rusts in Brazil 007 A list of genera and the number of species of rusts reported from Brazil 007 Rust genera with most species 009 A catalogue of the rusts (Uredinales) of Brazil 010 Bibliography 433 Host Families / Rust Genera Index for Rust fungi in Brazil 448 Plant rust fungi of Brazil, HOST – RUST INDEX 452

KEYS TO HELP IDENTIFY VARIOUS GROUPS OF RUSTS

Key to help identify anamorph gerera of Phakopsoraceae, Uredinales (Buriticá, 1994) 012 Key to help identify anamorph genera of Uredinales (modified from Cummins and Hiratsuka, 2003) 013 Key to help identify Aecidium species on Guatteria, Annonaceae, in Neotropics 014 Key to help identify Aecidium species on Diospyros, Ebenaceae, in Neotropics 017 Key to help identify Aecidium species on Jacaranda from Brazil, Bignoniaceae 018 Key to help identify unconnected species of Aecidium on Loranthaceae in Neotropica 022 Key to help identify species of Cerotelium in the Neotropics (modified from Buriticá, 1999) 046 Key to help identify species of Crossopsora in the Neotropics on Apocynaceae 062 Key to help identify Dicheirinia spp. based on urediniospores 073 Key to help identify Dicheirinia spp. based on telia and paraphyses 074 Key to help identify species of Didymopsora 077 Key to help identify species of Kuehneola on Rosaceae: Dryas, Rosa, and Rubus 092 Key to help identify species of Maravalia in Brazil 098 Key to help identify three rust species on Erythroxylum, Erythroxylaceae, in Latin America 100 Key to help identify five rust species on Olyra and Parodiolyra , Poaceae 126 Key to help identify Phakopsora species on Phyllanthus, Euphorbiaceae, in the Neotropics 129 Key to help identify species of Phragmidiella in the Neotropics based on anamorph sori 132 Key to help identify the two species of Phragmidium on Rosa in Brazil 134 Key to help identify Porotenus and Uredo on Memora, Bignoniaceae 139 Key to help identify the species of Prospodium (all in the Neotropics, all on Bignoniaceae or Verbenaceae) 144 Key to help identify three microcyclic species of Puccinia on Asclepiadaceae subfamily Cynanchoideae 168 Key to help identify species of Puccinia on Malpighiaceae 173 Key to help identify species of Puccinia on Hyptis, Lamiaceae, in the Americas 182 Key to help identify species of Puccinia on Cordia, Boraginaceae, in the Americas 192 Key to help identify species of Puccinia on Piptocarpha and Vanilosmopsis, Asteraceae 203 Key to help identify species of Puccinia on Piptocarpha based mainly on paraphyses 203 Key to help identify microcyclic species of Puccinia on Malvaceae 222 Key to help identify varieties of Puccinia levis, on Poaceae 238 Key to help identify species of Puccinia on Wedelia, Asteraceae in the Americas 255 Key to help identify varieties of Puccinia schileana on Verbesina and Vigiera, Asteraceae 282 Key to help identify varieties of Puccinia substriata, Poaceae (after Ramachar and Cummins, 1965) 291 Key to help identify species of Pucciniosira in Neotropica 304 Keys to help identify species of Ravenelia in the Americas 1. Key to Ravenelia on Caesalpiniodeae (Caesalpiniaceae) in the Americas (host leaves mostly once pinnate) 307 2. Key to Species of Ravenelia on Papillionoideae in the Americas (22 species) 308 3. Key to help identify Species of Ravenelia on Lonchocarpus and Derris spp 311 4. Key to help identify species of Ravenelia on Caesalpinia and Cenostigma based on teliospores in the Neotropics 316

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5. Key to help identify species of Ravenelia reported on Calliandra 317 6. Key to help identify Ravenelia species on Cassia sensu lato, genera: Cassia, Chamaecrista, and Senna, in the Neotropics 319 Key to help identify species of Uromyces on Leguminosae in Brazil based on uredinia and telia 373 Key to help identify species of Uredinales on Cucurbitaceae in the Americas 377 Key to help identify rust fungi on Bauhinia in Brazil 378 Key to help identify species of Uromyces on Desmodium, Leguminosae, in Brazil 387 Key to help identify species of Uromyces on Cestrum, Solanaceae 390 Key to help identify species of Uromyces on Loranthaceae in the tropics or subtropics of the New World 390 Key to help identify species of Uromyces on Juncus in the Americas 406

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Sphaerophragmium sorghi Batista & Bezerra, Nova Hedw. 2: 347. 1960. Not a rust.

SPHENOSPORA Dietel, Ber. Dtsch. Bot. Ges. 10: 63. 1892. TYPE SPECIES Sphenospora pallida (Winter) Dietel, see below. Family Raveneliaceae. Sphenospora is characterized by telia that are waxy-oily cushions when moist, hard when dry, teliospores are pedicellate with two probasidial cells separated by a vertical septum. The probasidial cells are thin-walled, without sculpturing, colorless or very pale, and germinate without dormancy to produce well differentiated metabasidia. The metabasidia are straight, not curved as most other metabasidia. Several teliospores arise from a well differentiated teliosporogenous cell. Free hand sections or mounts of teliospores have abundant oily droplets. Uredinia are pulverulent and yellowish to brownish, often cinnamon-brown. Spermogonia and aecia are unknown for the genus. About ten species are known, most of them in the tropics of the Americas. The basic structure of the teliospores of Sphenospora is the same as that of Diorchidium but up to now only two-celled teliospores are known. Sphenospora differs from Diorchidium because its telia contain a gelatinous-oily matrix that upon drying is hard or leathery. Hennen et al. (1998) discuss the relation of Sphenospora to Diorchidium..

A comparison of the urediniospores of three species Sphenospora on Orchidaceae: 1. Urediniospores a little smaller: (20-)22-26(-29) x (17-)19-22(-23) µm, pores 3(-4), equatorial Sphenospora mera. 2. Urediniospores a little larger: (22-)24-33 x 18-26 µm, pores 1, 2, or 4, equatorial Sphenospora kevorkianii. 3. Urediniospores larger: (26-)30-40(-45) x (18-)20-23(-25) µm, pores 3, equatorial, obscure. Sphenospora saphena.

Sphenospora copaiferae P. Sydow & H. Sydow, see DIORCHIDIUM COPAIFERAE (P. Sydow & H. Sydow. ) Cummins & Y. Hiratsuka.

SPHENOSPORA KEVORKIANII Linder, Mycologia 36: 464. 1944. TYPE on Epidendrum difforme Jacquin from Nicaragua, Capo: Bilwas Karma, 6 Apr 1943, Kevorkian s.n. (?/?,IIpe/III). Anamorph Uredo nigropunctata P. Hennings, Hedwigia 35: 254. 1896. TYPE on Cyrtopodium sp.( published as “Stanhopea sp.”) from Brazil, Rio de Janeiro, July (?Aug) 1887, Ule-652. (This name has priority because it was published just above Uredo epidendri on the same page). = Uredo epidendri P. Hennings, Hedwigia 35: 254. 1896. TYPE on Epidendrum sp. from Brazil, Santa Catarina: Tuberão, Feb 1889, Ule-1267. = Uredo cyrtopodii H. Sydow & P. Sydow, Bull. Herb. Boiss. II, 1: 77. 1901. TYPE on Cyrtopodium sp. from Brazil, Rio de Janeiro: Maua, 18 Aug 1896, Ule-( ?2447) or -2457. = Uredo wittmackiana P. Hennings & Klitzing in P. Hennings, Gartenflora 53: 397. 1904. TYPE from Mexico, other data not available. = Uredo guacae Mayor, Mem. Soc. neuchâteloise Sci. nat. 5: 583. 1913. TYPE on Epidendrum sp. from Colombia, Antioquia: near Guaca 12 Sept 1910, Mayor- 108. See also Uredo carnosa Spegazzini which probably belongs here. On Orchidaceae. Catasetum sp., São Paulo (IBI-16795). Cyrtopodium punctatum (Linaeus) Lindley, Mauá (Sydow, 1924: 503). Cyrtopodium sp.,(published as Stanhopea sp.), Rio de Janeiro (Hennings, 1896: 254). Epidendrum sp., Santa Catarina (Hennings, 1896: 254). Natylia lyrata, Brasil (PUR-F16894). Prescottia sclerophylla, Rio de Janeiro (PUR-F19210), São Paulo (IBI-12052).

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Sauroglossum nitidum (Velloso) Schlechter, São Paulo (IBI-17379). Spiranthes sp., São Paulo (IBI-13881). Stanhopea graveolens Lindley, São Paulo (PUR-F52698). Stenorrhynchus sp., Serra dos Orgãos (Dietel, 1899: 256). Zygostates lunata Lindley, Brasil (PUR-F16442). Sphenospora kevorkiani, or as one of its anamorph synonyms, a native rust widespread in the tropics of the Americas, has been reported to infected at least twelve genera of Orchidaceae including Bletia and Oncidium, not listed above But the identifications of the hosts in most cases require confirmation. Most of the specimens in PUR and IBI have come from plant quarantine interceptions or submitted by orchid growers for identification Infections by Sphenospora kevorkianii on different host genera result in different symptoms. Infected leaves have powdery, yellow rust sori that are associate with small reddish or blackish discolored leafspots. This latter trait was the source of the epithet for the anamorph name Uredo nigropunctata. Variability in symptoms may have influenced the naming of the different synonyms listed above.. Telial sori have a waxy, yellow-brown to blackish appearance. Management includes the removal and destruction of the infected leaves. Spermogonia and aecia unknown. Uredinia on the abaxial side of leaves, subepidermal in origin, blister-like at first, erumpent, yellowish brown; urediniospores (22-)24-33 x 18-26 µm, broadly ellipsoid or obovoid, wall 1.5-3 µm thick, yellowish, echinulate, pores 1, 2 or 4, equatorial. Telia on the abaxial side of leaves, erumpent, scattered or often circinately arranged, pulvinate, blackish- brown or black, waxy, hard when dry, teliospores 23-28 x 13-16 µm, ellipsoid or oval, wall uniformly 1 µm thick, colorless, smooth, germ pore 1 in each cell, apical, if differentiated, pedicel colorless, 40-65 µm long 6-8 µm wide, persistent.

SPHENOSPORA MERA Cummins, Bull. Torrey Bot. Club 72: 214. 1945. TYPE on Cycnoches chlorochilum Rolfe, from Venezuela, unknown locality, intercepted in Plant Quarantine at San Juan, Puerto Rico, 16 Nov 1943 by L. J. Mc Connell 8719, PUR (isotypes PAC, US). (?/?,IIpe/III). On Orchidaceae Eulophidium maculatum (Lindley) Pfitzer; Brazil, (BPI US 042051). Sphenospora mera has been reported also on seven other genera of Orchidaceae and from Peru, Central America, Mexico, and The West Indies, all intercepted in Plant Quarantine. Host identification requires confirmation. Spermogonia and aecia unknown. Uredinia on the abaxial side of leaves, scattered, subepidermal becoming erumpent, pale cinnamon-brown, urediniospores (20-)22-26(-29) x (17-)19-22(-23) µm obovoid or broadly ellipsoid, wall 2-2.5 µm thick, yellowish to nearly cinnamon-brown, echinulate, pores 3(4), equatorial, with slight cuticular caps. Telia on the abaxial side of leaves, pulvinate, scattered or circinately disposed, dark brown, waxy when fresh, hard when dry, paraphyses or some kind of sterile elements present, cylindrical, colorless, teliospores (20-)23-28(-30) x 11-14(-15) µm, more or less oblong-ellipsoid, wall uniformly 0.5 µm thick, colorless, smooth, pedicel 30-45 µm long, nearly as wide as the spore at the hilum, persistent.

SPHENOSPORA PALLIDA (Winter) Dietel in Engler & Prantl, Nat. Pfl. 1(1): 70. 1897. (?/?,IIpe/III). 9 Diorchidium pallidum Winter, Grevillea 15: 86. 1887. TYPE on Dioscorea sp., originally reported as an unidentified vine, from Brazil, Santa Catarina: São Francisco, August 1884, Ule-143. 9 Puccinia sphenospora P. Sydow & H. Sydow. , Mon. Ured. 1: 838. 1907. Nom. nov. for Diorchidium pallidum Winter, not Puccinia pallida Tracy. Anamorph Uredo dioscoreae P. Hennings, Hedwigia 35: 255. 1896. TYPE on Dioscorea grandiflora from Brazil, Rio de Janeiro: Rio de Janeiro, August 1887, Ule-1342. [not Uredo dioscoreae (Berkeley & Broome) Petch, 1912, on Dioscorea sp. from Sri Lanka, an anamorph of Goplana dioscoreae Cummins]. = Uromyces taubertii P. Hennings, Bot. Jahrb. Syst. 15: 14. 1892. TYPE on Dioscorea piperifolia Willdenow from Brazil, Rio de Janeiro: Rio de Janeiro, date not reported, Glaziou-4266. Only urediniospores. = ?Uredo aristolochiae Albuquerque, Pesq. Agropec. Bras. Ser. Agron. 6: 147. 1971 (Not U. aristolochiae DeCandolle from Europe).?may be OK as sp. nov.