ACTA
AMAZONICA
http://dx.doi.org/10.1590/1809-4392202100441
ORIGINAL ARTICLE
Two new species of rust fungi (Pucciniales) from
the Brazilian Amazon: Aecidium margaritariae on
Margaritaria and Uromyces amapaensis on Jatropha
Patrícia Maria Piovezan OLIVEIRA1, Helen Maria Pontes SOTÃO2* , Gabriely Serrão FREIRE2,
Josiane Santana MONTEIRO2
1
Universidade Federal Rural da Amazônia, Programa de Pós-Graduação em Ciências Biológicas, Av. Presidente Tancredo Neves 2501, 66077-830 Belém, PA, Brazil
Museu Paraense Emílio Goeldi, Coordenação de Botânica, Av. Perimetral 1901, Caixa Postal 399, 66077-830 Belém, PA, Brazil
* Corresponding author: helen@museu-goeldi.br; https://orcid.org/0000-0002-1717-9532
2
ABSTRACT
Two new species of Pucciniales fungi on plants of the Fabid clade are described from samples deposited in the herbarium of
Museu Paraense Emilio Goeldi, collected in the state of Amapá, in the Brazilian Amazon. They are Aecidium margaritariae
found on Margaritaria nobilis (Phyllanthaceae), and Uromyces amapaensis on Jatropha gossypiifolia (Euphorbiaceae). The
microstructures of the specimens were analyzed using optical and scanning electron microscopy. Aecidium margaritariae is
characterized by the presence of globose, subglobose to slightly ellipsoid aeciospores with warty walls and smooth areas usually
in the basal portion. Uromyces amapaensis is distinguished by the presence of uredinia with paraphyses which are thickened
and rounded at the tip, and pedicellate and smooth teliospores. Descriptions, illustrations, and taxonomic comments are
presented for each species.
KEYWORDS: Basidiomycota, Brazil, Euphorbiaceae, Phyllanthaceae, Pucciniomycetes
Duas novas espécies de ferrugens (Pucciniales) da Amazônia brasileira:
Aecidium margaritariae sobre Margaritaria e Uromyces amapaensis
sobre Jatropha
RESUMO
Duas novas espécies de fungos Pucciniales sobre plantas do clado das fabídeas são descritas a partir de amostras depositadas no
herbário do Museu Paraense Emílio Goeldi, coletadas no estado do Amapá, na Amazonia Brasileira. Aecidium margaritariae
ocorrendo sobre Margaritaria nobilis (Phyllanthaceae) e Uromyces amapaensis sobre Jatropha gossypiifolia (Euphorbiaceae). As
microestruturas dos espécimes foram analisadas em microscópio óptico e em microscopia eletrônica de varredura. Aecidium
margaritariae se caracteriza por apresentar eciósporos globosos, subglobosos a levemente elipsoides, parede verrugosa com áreas
lisas geralmente na extremidade basal. Uromyces amapaensis se diferencia por apresentar uredínios com paráfises engrossadas
e arredondadas no ápice e teliósporos pedicelados, lisos. São apresentadas descrições, ilustrações e comentários taxonômicos
para cada espécie.
PALAVRAS-CHAVE: Basidiomycota, Brasil, Euphorbiaceae, Phyllanthaceae, Pucciniomycetes
INTRODUCTION
In the fungi order Pucciniales, a very specific relationship
between the parasitic fungus species and its host plant is
observed. This specificity is a peculiar feature that favors the
classic taxonomy of this group of fungi that cause rust in
plants. It is used as an aid in the identification of the species,
complementing morphological and molecular studies of the
different stages of their complex life cycles (Cummins and
Hiratsuka 2003; Aparecido and Passador 2009, 2014; Aime
et al. 2006, 2018).
About 3,000 species of fungi are reported for the
Brazilian Amazon, including those of the order Pucciniales
(Basidiomycota), represented by 199 known species causing
rust on plants, of which 55 occur in the northern Brazilian state
of Amapá (França et al. 2010; Carmo et al. 2016; Carvalho et
al. 2018; Furtado et al. 2018; Flora do Brasil 2020). According
CITE AS: Oliveira, P.M.P.; Sotão, H.M.P.; Freire, G.S.; MONTEIRO, J.S. 2021. Two new species of rust fungi (Pucciniales) from the Brazilian Amazon: Aecidium
margaritariae on Margaritaria and Uromyces amapaensis on Jatropha. Acta Amazonica 51: 244-249.
244
VOL. 51(3) 2021: 244 - 249
ACTA
AMAZONICA
OLIVEIRA et al. Two new rust fungi for the Brazilian Amazon
to estimates, the Brazilian Amazon harbors about 50,000
botanical species (Cardoso et al. 2017), which suggests that
many rust species likely remain undiscovered in this biome.
A taxonomic revision of Pucciniales specimens collected
on Fabids and deposited in the herbarium of Museu Paraense
Emílio Goeldi (Pará, Brazil) revealed the presence of two
undescribed species. Here we describe the two new species of
Pucciniales, which were found growing on the host species
Jatropha gossypiifolia and Margaritaria nobilis, for the Brazilian
Amazon in Amapá state.
MATERIAL AND METHODS
The Pucciniales specimens analyzed in this study were
collected in the state of Amapá (Brazil) and were deposited
in the João Murça Pires Herbarium (MG) of Museu Paraense
Emilio Goeldi (MPEG). The identification of the host plants
was carried out in collaboration with botanical taxonomists
and technicians from the MPEG, following APG IV (2016)
and Tropicos (https://www.tropicos.org/nameSearch).
The identification of the Pucciniales specimens followed
the observation of sori under a Leica EZ4 stereomicroscope
to examine the lesions on the plant tissue and the presence of
spores, and the preparation of semi-permanent slides of sori,
spores and other microstructures in slightly heated drops of
lactoglycerol (distilled water + lactic acid + glycerin) to be
analyzed using Zeiss Axiolab optical microscopy (Neergaard
et al. 2000; Aparecido and Passador 2009). Twenty-five
spores randomly selected from each specimen were measured.
Size variation was expressed by minimum and maximum
values. Illustrations of the microstructures were made using
an optical microscope attached to a digital camera. For the
examination of the surface of fungal structures in scanning
electron microscopy (SEM), the methodology of França
and Sotão (2009) was adopted. Dry leaf material with rust
fungi was hand cut with a razor blade into small pieces of
approximately 4 × 4 mm. The samples were mounted onto
aluminum stubs with adhesive carbon tape and coated with
gold. The images were obtained in a Tescan Mira3 SEM and
recorded in digital mode.
Specialized literature with descriptions of species and
identification keys was referred to subsidize the identification
and description of the new taxa (Cummins and Hiratsuka
2003; Hennen et al. 2005; Carvalho Jr and Sotão 2010). The
notations for life cycle description followed Salazar-Yepes and
Carvalho Jr (2010). The holotypes were deposited at the MG
Herbarium and registered in MycoBank (www.mycobank.
org). Author names follow the standards of Index Fungorum
(www.indexfungorum.org).
245
VOL. 51(3) 2021: 244 - 249
RESULTS
Aecidium margaritariae Sotão & Piovezan, sp. nov. (Figure 1)
MycoBank no.: MB 838085
Type: Brazil. Amapá: Mazagão, Mazagão Novo, on
Margaritaria nobilis L.f. (Phyllanthaceae), 27 July 1995,
H.M.P. Sotão et al. 95–244, sori I (Holotype: MG 230298).
Diagnosis: Aecidium margaritariae can be distinguished from
other Aecidium species occurring on Phyllanthaceae by the
presence of peridial cells with smooth outer walls and warty
inner walls, and globose, subglobose to slightly ellipsoid
aeciospores with warty walls and smooth areas usually in the
basal portion, measuring 27.5– 37.5 × 21.5–27.5 µm.
Spermogonia adaxial, subcuticular, gregarious, punctate,
brown to black. Aecia abaxial, on irregular leaf spots, forming
galls, grouped, cup-shaped, with white to pale yellow peridia;
peridial cells oblong to ellipsoid, 30–40 × 15–17.5 µm, with
smooth outer wall and warty inner wall, 1 µm thick, hyaline;
aeciospores catenulate, 27.5–37.5 × 21.5–27.5 µm, globose,
subglobose to slightly ellipsoid, wall thin, 0.5–1 µm thick,
warty with smooth areas usually in the basal portion, hyaline.
Uredinia and telia unknown. Life cycle (0/Icv,?,?).
Etymology: the epithet refers to the genus of the host plant,
Margaritaria, on which the described rust was found.
Known distribution: Brazil
Uromyces amapaensis Sotão & Piovezan, sp. nov. (Figure 2)
MycoBank no.: MB 838086
Type: Brazil. Amapá: Cutias, on Jatropha gossypiifolia L.
(Euphorbiaceae), 05 December 2005, H.M.P. Sotão H2005–
02, sori II, III (Holotype: MG 230259).
Diagnosis: Uromyces amapaensis is characterized by presenting
paraphysate uredinia and telia whose paraphyses have
thickened and rounded tips, and pedicellate and smooth
teliospores, different from Uromyces cnidoscoli Henn. which
has no paraphyses in uredinia and telia, and has minutely
ornamented teliospores.
Spermogonia and aecia not seen. Uredinia scattered over
the abaxial surface, orangish, subepidermal, pulverulent,
grouped; paraphyses clavate, aseptate, 20–36 × 5–13.5 µm,
smooth-walled, thickened and rounded at the tip (3–4 µm),
light brown; urediniospores broadly globose, subglobose to
ellipsoid, pedicellate, 20–30 × 19–20 µm, wall hyaline to
light brown, 2–3 µm thick, moderately or densely echinulate,
echinulations throughout the spore surface, but slightly
irregular, germ pores not seen. Telia in uredinia, teliospores
pedicellate, ellipsoid, 20–32 × 16–20 µm, lateral wall 1.5–2
µm, thickened at the apex, 3–5 µm, smooth. Life cycle (?/?/
IIpe/III).
Etymology: The specific epithet refers to the Brazilian state
of Amapá.
Known distribution: Brazil
ACTA
AMAZONICA
OLIVEIRA et al. Two new rust fungi for the Brazilian Amazon
Figure 1. Aecidium margaritariae (MG 230298, holotype). A – Superficial view of an aecium (SEM); B–C – Peridial cells; D – Peridial cells on aecium (SEM); E – Inner wall of
peridial cells (SEM); F – Outer wall of peridial cells (SEM); G–H – Aeciospores in superficial view (left) and medium focus (right); I – Aeciospores (SEM); J–K – Aeciospores
with smooth areas in the basal portion. Scale bars: A = 50 μm; B–H, J = 20 μm; I, K = 10 μm. This figure is in color in the electronic version.
Figure 2. Uromyces amapaensis (MG 230259, holotype). A – Paraphyses, urediniospore and teliospores; B – Paraphyses and teliospores; C – Urediniospores in medium
focus; D – Superficial view of uredinium with urediniospores, paraphyses and teliospores (SEM); E – Detail of paraphyses and teliospores (SEM); F – Urediniospores
(SEM). Scale bars: A = 50 μm; B–D= 20 µm; E–F = 10 µm. This figure is in color in the electronic version.
246
VOL. 51(3) 2021: 244 - 249
ACTA
AMAZONICA
OLIVEIRA et al. Two new rust fungi for the Brazilian Amazon
DISCUSSION
Aecidium margaritariae on M. nobilis is the second record
of rust on this host genus. The first is A. entebbense Cummins,
found on Margaritaria discoidea (Baill.) G.L. Webster (=
Phyllanthus discoideus (Baill.) (Cummins 1945). Unlike A.
margaritariae, in A. entebbense the peridial cells are smaller
(13–19 × 18–25 µm), oblong to polyhedral, with striate outer
walls and warty inner walls, and the aeciospores are smaller
(13–18 × 16–23 µm), with apically thickened (3–8 µm) and
uniformly warty walls (Cummins 1945).
Another five species of Aecidium are known to parasitize
other plant genera of Phyllantaceae: Aecidium detritum
(Phyllanthus sellowianus (Klotzsch) Müll. Arg.), A. fluggeae
(Flueggea virosa (Roxb. ex Willd.) Royle, = F. microcarpa
(Blume) Müll. Arg.), A. luzoniense (Phyllanthus sp.),
A. phyllanthi (Phyllanthus sp.), A. phyllanthi-floribundi
(Phyllanthus floribundus Müll. Arg.) and A. phyllanthinum
(Phyllanthus reticulatus Poir.) (Hennings 1892, 1900; Sydow
et al. 1907; Doidge 1927; Viennot-Bourgin 1954; Buriticá et
al. 2014), with distinct characteristics from those of the new
species presented here.
Other rust species registered on Phyllanthaceae have
uredinia only, namely, Uromyces phyllanthi Henn., U.
phyllanthi-longifolii Petch, U. phyllanthi-niruris M.S. Patil, and
U. phyllanthi-reticulati Petch (Hennings 1896; Petch 1917,
1922; Patil 1991). Teleomorphic species include Coleosporium
phyllanthinum Syd. (Sydow 1937), Masseeella capparis
(Hobson bis ex Cooke) Dietel (Liberato et al. 2014), Masseeella
narasimhanii Thirum. (Thirumalachar 1943), Phakopsora
fenestrala (Arthur) Arthur (Arthur 1917), P. phyllanthi Dietel
(Dietel 1910), P. phyllanthi-discoidei Vienn.-Bourg. (ViennotBourgin 1954), P. purdueae Buriticá & J.F. Hennen, P. tijucae
Buriticá & J.F. Hennen, and P. ulei (Syd. & P. Syd.) Buriticá
& J.F. Hennen (Buriticá 1999).
Uromyces amapaensis represents a new species of rust
fungi occurring on Jatropha. Five species are known to affect
these plants: Phakopsora arthuriana Buriticá & J.F. Hennen,
Uromyces agnatus Arthur, U. cnidoscoli, U. jatrophae Dietel. &
Holw. and U. oaxanacus Dietel & Holw. (Monoson & Prose
1983, Hennen et al. 2005). Uromyces amapaensis is easily
differentiated from the other Uromyces species mentioned
earlier by the presence of a few paraphyses with thickened
tips and pedicellate and smooth teliospores.
Berndt (2002) recorded U. cnidoscoli on Jatropha sp. in
Argentina. The Argentinean specimen presented transversely
ellipsoidal, grossly warty, dark brown teliospores and pedicels
whose apical parts dilated appreciably in aqueous medium.
Before that, only the type had been reported from Brazilian
collections (Goiás state), in which only teliospores had been
observed, however, Berndt (2002) was able to report the
presence of spermogonia, aecia and uredinia in the species.
Hennings (1895) described U. cnidoscoli on Cnidoscolus
247
VOL. 51(3) 2021: 244 - 249
vitifolius (Mill.) Pohl and commented that Aecidium cnidoscoli
Henn. probably belonged to the life cycle of this species.
Phakopsora arthuriana differs from U. amapaensis by
presenting subepidermal, non-erumpent telia with 6 to 12
layers of sessile spores, and numerous paraphyses (Hennen
et al. 2005). The urediniospores of U. amapaensis are
morphologically similar to those of P. arthuriana, but they are
pedicellate. The paraphyses are similar in the two species, but
in P. arthuriana they are numerous and have larger dimensions
(20–50 × 9–12 µm vs. 20–36 × 5–13.5 µm in U. amapaensis)
and the teliospores are smaller (10–27 × 7–13 µm) (Hennen
et al. 2005).
Monoson and Prose (1983) listed 20 autoecious Uromyces
species infecting Euphorbiaceae plants in the new world. They
presented a key that differentiated them primarily based on the
smooth or ornamented walls of the teliospores. Only Uromyces
cisneroanus Speg. on Sapium sp. has a smooth wall like that
of U. amapaensis, but it presents as distinctive characteristics
teliospores with hyaline outer wall and dark inner wall and
thickened apex (5–18 µm), and urediniospores measuring
30–50 × 14–24 µm.
Uromyces amapaensis also presents urediniospores with
significant differences in relation to some Uredo species that
parasitize Euphorbiaceae plants. Uredo alchorneae Henn.
(Alchornea sp.) and Uredo paulistana Speg. (Acalypha sp.) do
not have paraphyses and have slightly angular urediniospores
which are smaller than those of U. amapaensis (Saccardo and
Trotter 1912; Hennen et al. 2005). Uredo saviae Arthur &
J.R. Johnst. (Savia sp.) has angularly obovoid urediniospores,
usually triangular (Arthur and Johnston 1918). Uredo
valentula H.S. Jacks & Holw. (Croton spp.) has spermogonia,
aecia and uredinia in their life cycle, with urediniospores
presenting thickened apical wall (3–5.5 µm) and three slightly
supraequatorial germ pores (Hennen et al. 2005). In turn,
Uredo maceiensis Henn. (Maprounea sp.) presents uredinia
with paraphyses thickened at the tip just like U. amapaensis,
but in U. maceiensis the paraphyses are larger (30–50 ×
15–16 µm vs. 20–36 × 5–13.5 µm in U. amapaensis), the
urediniospores are usually ovoid, 4–6 µm thick at the apex,
showing three equatorial germ pores (Hennen et al. 2005).
Until now, nine species and two varieties of rust fungi have
been described on Euphorbiaceae in the Brazilian Amazon,
occurring on Maprounea Aubl. (Aecidium maprouneae var.
maprouneae Henn., Aecidium maprouneae var. noncrassatum
J.F. Hennen & Sotão, Chaconia maprouneae (Viégas) Y.
Ono & J.F. Hennen, and Uredo maceienses); Alchornea Sw.
(Olivea capituliformis (Henn.) Arthur and U. alchorneae); and
Jatropha L. (Phakopsora arthuriana, Uromyces cnidoscoli, and
U. jatrophae) (Hennen and Sotão 1997; Hennen et al. 2005;
Carvalho et al. 2018).
ACTA
AMAZONICA
OLIVEIRA et al. Two new rust fungi for the Brazilian Amazon
CONCLUSIONS
This study adds two new species of rust fungi to the
Brazilian and Amazonian mycobiota. Aecidium margaritariae
is the second species of rust fungus found on Margaritaria
nobilis, while Uromyces amapaensis is the fifth species of rust
fungi described on Jatropha gossypiifolia. Our finds increase
the known Brazilian mycobiota, highlighting the need to
explore new areas in the Amazon region, where fungal diversity
remains underestimated.
ACKNOWLEDGMENTS
PMPO thanks the Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq) for the scholarship received;
JSM thanks the Programa de Capacitação Institucional (Museu
Paraense Emílio Goeldi/MCTIC) (Process 300646/2019–4);
all authors thank the Programa de Pesquisa em Biodiversidade
(PPBio) Amazônia Oriental, for financial and logistic support,
the Instituto Chico Mendes de Conservação da Biodiversidade
(ICMBio) for logistic support, and Dr. Ricardo Secco and
Luiz Carlos Lobato for the identification of the host plants.
Cardoso, D.; Särkinen, T.; Alexander, S.; Amorim, A.M.; Bittrich,
V.; Celis, M.; et al. 2017. Amazon plant diversity revealed by a
taxonomically verified species list. PNAS, 114: 10695–10700.
Carmo, L.T.; Sotão, H.M.P.; Brito, F.M.; Moura, M.F.; Oliveira,
J.R. 2016. Riqueza de fungos causadores de ferrugens em plantas
hospedeiras da Região Metropolitana de Belém, PA, Brasil.
Hoehnea, 43: 557–573.
Carvalho-Jr., A.A.; Sotão, H.M.P. 2010. Pucciniales. In: Forzza, R.C.
et al. (Orgs.). Catálogo de plantas e fungos do Brasil. 1. ed. Andrea
Jakobsson Estúdio: Instituto de Pesquisas Jardim Botânico do
Rio de Janeiro, Rio de Janeiro, p.210-. (http://www.jbrj.gov.br).
Accessed on 07 Feb 2021.
Carvalho, A.C.; Sotão, H.M.P.; França, I.F. 2018. Fungos causadores
de ferrugens (Pucciniales) em plantas da Reserva Florestal
Adolpho Ducke, Amazônia Central, Brasil. Rodriguésia, 69:
663–672.
Cummins, G.B. 1945. Descriptions of tropical rusts. VII. Bulletin
of the Torrey Botanical Club, 72: 205–222.
Cummins, G.B.; Hiratsuka, Y. 2003. Illustrated Genera of Rust
Fungi. 3rd ed. The American Phytopathological Society Press,
St. Paul., 225p.
Dietel, P. 1910. Zwei neue Arten der Gattung Phakopsora. Annales
Mycologici, 8: 469–469.
REFERENCES
Aime, C.M.; Matheny, P.B.; Henk, D.A.; Frieders, E.M.; Nilsson,
R.H.; Piepenbring, M.; et al. 2006. An overview of the higher
level classification of Pucciniomycotina based on combined
analyses of nuclear large and small subunit rDNA sequences.
Mycologia, 98: 896–905.
Aime, C.M.; Bell, C.D.; Wilson, A.W. 2018. Deconstructing the
evolutionary complexity between rust fungi (Pucciniales) and
their plant hosts. Studies in Mycology, 89: 143–152.
Aparecido, C.C.; Passador, M.M. 2009. Metodologia para estudos
biológicos em Uredinales. Infobibos - Informações Tecnológicas.
(http://www.infobibos.com/Artigos/2009_2/Uredinales/index.
htm). Accessed on 15 Oct 2020.
Aparecido, C.C.; Passador, M.M. 2014. Estudos biológicos de
espécies de Puccinia utilizando “germinatélios”. Bioscience Journal
30: 440–447.
APG IV. 2016. An update of the Angiosperm Phylogeny Group
classification for the orders and families of flowering plants:
APG IV. Botanical Journal of the Linnean Society, 181: 1–20.
doi.org/10.1111/boj.12385
Arthur, J.C. 1917. Relationship of the genus Kuehneola. Bulletin of
the Torrey Botanical Club, 44: 501–511.
Arthur, J.C.; Johnston, J.R. 1918. Uredinales of Cuba. Memoirs of
the Torrey Botanical Club, 17: 97–175.
Berndt, R. 2002. Additions to the rust fungi of Argentina. Mycologia,
94: 523–534.
Buriticá, P. 1999. La familia Phakopsoraceae en el Neotrópico
III, Géneros: Batistopsora y Phakopsora. Revista de la Academia
Colombiana de Ciencias Exactas, Físicas y Naturales, 23: 271–305.
Buriticá, P.; Salazar-Yepes, M.; Pardo-Cardona, V.M. 2014.
Pucciniales (Fungi), Royas de Colombia. Revista Facultad
Nacional de Agronomía Medellín, 67 (suppl. 1): 1–93.
248
VOL. 51(3) 2021: 244 - 249
Doidge, E.M. 1927. A preliminary study of the South African rust
fungi. Bothalia, 2: 1–228.
Flora do Brasil 2020. 2021. Jardim Botânico do Rio de Janeiro.
(http:// floradobrasil.jbrj.gov.br/). Accessed on 15 Feb 2021.
França, I.F.; Sotão, H.M.P. 2009. Novos registros de ferrugens
(Uredinales) sobre Fabaceae para o Brasil. Acta Botanica Brasilica,
23: 860–863.
França, I.F.; Sotão, H.M.P.; Costa-Neto, S.V. 2010. Fungos
causadores de ferrugens (Uredinales) da Reserva Biológica do
Lago Piratuba, Amapá, Brasil. Rodriguésia, 61: 211–221.
Furtado, R.G.; Sotão, H.M.P.; Monteiro, J.S.; Brito, F.M. 2018.
Primeiro registro para o Brasil de Maravalia bolivarensis Y. Ono
(Pucciniales) parasitando Manilkara sp. (Sapotaceae). Hoehnea,
45: 129–133.
Hennen, J.F.; Figueiredo, M.B.; Carvalho Jr., A.A.; Hennen, P.G.
2005. Catalogue of the Species of Plant Rust Fungi (Uredinales) of
Brazil. Jardim Botânico do Rio de Janeiro, Rio de Janeiro, 490p.
(http://aplicacoes.jbrj.gov.br/publica/livros_pdf/catalogue.pdf ).
Accessed on 09 Jun 2021.
Hennen, J.F.; Sotão, H.M.P. 1997. Aecidium maprouneae var.
noncrassatum (Uredinales) sobre Maprouneae sp., novo táxon do
estado do Amapá, Brasil. Fitopatologia Brasileira, 22: 444–447.
Hennings, P. 1892. Fungi novo-guineenses. Botanische Jahrbücher für
Systematik Pflanzengeschichte und Pflanzengeographie, 15(Beibl.
33): 4–8.
Hennings, P. 1895. Fungi blumenavienses, a cl. Alfr.Moller lecti.
Hedwigia, 34: 335–558.
Hennings, P. 1896. Beiträge zur Pilzflora Südamerikas I. Uredineae.
Hedwigia, 35: 202–262.
Hennings, P. 1900. Fungi monsunenses. Monsunia, 1: 1–38.
ACTA
AMAZONICA
OLIVEIRA et al. Two new rust fungi for the Brazilian Amazon
Liberato, J.R.; McTaggart, A.R.; Shivas, R.G. 2014. First report of
Masseeëlla capparis in Australia. Australasian Plant Disease Notes,
9: 121. doi.org/10.1007/s13314-013-0121-y
Salazar-Yepes, M.A.; Carvalho, A.A. 2010. Ferrugens: Diversidade de
Uredinales do Parque Nacional do Itatiaia, Brasil. Ed. Technical
Books, Rio de Janeiro, 201p.
Monoson, H.L.; Prose, S.E. 1983. Autoecious Uromyces that infect
New-World Euphorbiaceae. Mycologia, 75: 436–450.
Sydow, H. 1937. Novae fungorum species. XXV. Annales Mycologici,
35: 244–286.
Neergaard, E.; Lyshede, O.B.; Gahoonia, T.S.; Care, D.; Hooker, J.E.
2000. Anatomy and histology of roots and root-soil boundary.
In: Smit, A.L.; Bengough, A.G.; Engels, C.; Noordwijk, M.;
Pellerin, S.; Geijn, S.C. (Eds.). Root Methods: A Handbook.
Springer-Verlag, Berlin, p.33–73.
Sydow, H.; Sydow, P.; Butler, E.J. 1907. Fungi Indiae orientalis pars
II. Annales Mycologici, 5: 485–515.
Patil, M.S. 1991. Rust fungi from Maharashtra - IV. Indian
Phytopathology, 44: 433–439.
Petch, T. 1917. Additions to Ceylon fungi. Annals of the Royal Botanic
Gardens Peradeniya, 6: 195–256.
Petch, T. 1922. Additions to Ceylon fungi II. Annals of the Royal
Botanic Gardens Peradeniya, 7: 279–322.
Saccardo, P.A.; Trotter, A. 1912. Sylloge Fungorum, 21: 1–928.
Thirumalachar, M.J. 1943. Masseeella narasimhanii, a new species
of rust on Flueggea leucopyrus Willd. Proceedings of the Indian
Academy of Sciences Section B, 18: 36–40.
Viennot-Bourgin, G. 1954. Urédinales d’Afrique. 4. Urédinales de
Côte d’Ivoire. 3. Bulletin de la Société Mycologique de France,
70: 410–419.
RECEIVED: 19/02/2021
ACCEPTED: 30/05/2021
ASSOCIATE EDITOR: Nelson Menolli Junior
This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
249
VOL. 51(3) 2021: 244 - 249