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CSIRO PUBLISHING
www.publish.csiro.au/journals/app Australasian Plant Pathology, 2006, 35, 347–353
Additions to the Brazilian mycobiota of the grassy weed,
Hymenachne amplexicaulis, with a discussion on the taxonomic
status of Paraphaeosphaeria recurvifoliae
D. J. SoaresAand R. W. BarretoA,B
ADepartamento de Fitopatologia, Universidade Federal de Vic¸osa, 36571-000 Vic¸osa, M.G., Brazil.
BCorresponding author. Email: rbarreto@ufv.br
Abstract. Hymenachne amplexicaulis (capybara grass) has been listed among Australia’s 20 worst weeds (or weeds
of national significance) but has not been officially recognised as a target for biological control. Nevertheless,
collections are being made of fungal pathogens associated with this amphibious grassy weed and of other aquatic
weeds native to Brazil. This paper represents the second contribution towards the description of the pathogenic
mycobiota of H. amplexicaulis in Brazil. Two new fungal records are described and illustrated: Passalora barretoana
stat. et comb. nov. and Paraphaeosphaeria michotii. The latter is described in association with its anamorph, which
belongs to the genus Microsphaeropsis. The status of the taxon Phyllachora sp., recorded in a previous publication,
is elucidated and a more complete description is provided here.
Additional keywords: biological control, classical biocontrol, Passalora fusimaculans,Phyllachora minutissima,
Phyllachora acustispora, Poaceae, taxonomy.
Introduction
Hymenachne amplexicaulis (Rudge) Nees is a perennial
grassy weed with an amphibious habit, and is now considered
to be among the most noxious invasive plants in Australia
(Csurhes et al. 1999; Anonymous 2001; Houston and
Duivenvoorden 2002; Grice 2004) and was included in the list
of the twenty worst weeds for Australia (Weeds of National
Significance; Thorp and Lynch 1999). Paradoxically, it is
also considered a good cattle pasture, and this has generated
conflicts of interest (Grice 2004). Perhaps because of this, it
is, up to this date, not recognised officially as a candidate for
biological control. In Brazil, which is part of the centre of
origin of this plant, it is commonly used as a native pasture
(Nascimento and Renvoize 2001), and although included in
the main lists of Brazilian weeds (Kissmann 1997; Lorenzi
2000) it represents only a minor problem in inundated crops,
particularly rice.
Little is known about the fungal pathogens of this plant
worldwide. The world literature contained only nine fungal
records on H. amplexicaulis:Anthostomella tomicum (L´
ev.)
Sacc., Balansia paspali Henn., B. strangulans (Mont.)
Diehl, B. vorax var. paspali (Henn.) Tesdoro, Cercospora sp.
Coniothyrium sp., Leptosphaeria grisea Pass., Phyllachora
acutispora Speg. and Phyllachora hymenachnei (Chard´
on)
Arx & E. Mull., but none of these records is from Brazil
(Vi´
egas, 1961; Mendes et al. 1998; Farr et al. 2005).
Recently, Monteiro et al. (2003) published the first records
of fungal pathogens on this host from Brazil, namely
Curvularia lunata and Phyllachora sp., collected from
a single visit to the region of Corumb´
a (state of Mato
Grosso do Sul) Brazil. After the publication of this work,
R. W. Barreto was contacted by Dr Tim Heard (CSIRO
Entomology) and invited to elaborate a proposal for
thoroughly surveying potential fungal biocontrol agents
of H. amplexicaulis in its native range in South America.
Lack of official recognition in Australia of H. amplexicaulis
as a biocontrol target discouraged the funding for this
project. Nevertheless, it was decided to continue surveying
the mycobiota of H. amplexicaulis in Brazil, parallel to
surveys being performed on other aquatic target weeds. This
paper includes two additions to the known mycobiota of
H. amplexicaulis that also represent taxonomic novelties
and also includes an elucidation of the taxonomic status of
the species previously reported by Monteiro et al. (2003)
as Phyllachora sp.
Methods
As reported by Monteiro et al. (2003), abundant populations of
H. amplexicaulis bearing significant mycobiota were found in the
Paraguay basin, state of Mato Grosso do Sul, where capybara grass
© Australasian Plant Pathology Society 2006 10.1071/AP06037 0815-3191/06/030347
348 Australasian Plant Pathology D. J. Soares and R. W. Barreto
grows in the wetlands and is used as a natural pasture. Samples of
infected parts of H. amplexicaulis were collected, photographed and
dried in a plant press. The fungal samples were examined with a light
microscope Olympus BX 50 fitted with a camera lucida. Microscope
slides were mounted using lactophenol or lactofuchsin.
Results and discussion
The pathogenic fungi collected during this survey of the
mycobiota of H. amplexicaulis in Brazil are described below.
Passalora barretoana (U Braun & Crous) DJ Soares,
U Braun & RW Barreto stat. et. comb. nov. (Fig. 1)
≡Passalora fusimaculans (GF Atk.) U Braun & Crous
var. barretoana U Braun & Crous, in Crous & Braun,
Mycosphaerella and its anamorphs: 1. Names published in
Cercospora and Passalora. CBS Biodiversity Series 1: 453
(2003).
=Cladosporium piricularioides Dearn. & House, Circ.
New York State Mus. 24: 57 (1940), nom. inval.
Material examined:onHymenachne amplexicaulis
(Poaceae) BR 262, Km 641, between Porto Morrinho and
Fazenda Bodoquena, state of Mato Grosso do Sul, Brazil,
16 Aug. 2005, DJ Soares (VIC-29376; HAL 1885 F); Lagoa
da Pampulha, Belo Horizonte, state of Minas Gerais, Brazil,
10 May 2005, DJ Soares (VIC-29394).
Others material examined:onEchinochloa polystachya,
Rio Madeira, Nova Olinda do Norte, state of Amazonas,
Brazil, 20 Aug. 1997, RE Hanada (VIC-22048); Rio
Fig. 1. Line drawing of Passalora barretoana. Conidiophores
arranged in a fascicle and conidia. Scale bar =10 µm.
Amazonas, Parintins, state of Amazonas, Brazil, 29 Aug.
1997, RE Hanada (VIC-22023).
Lesions large on living leaves causing descending
blights, amphigenous, straw-coloured becoming brown with
age; caespituli amphigenous, brown, usually arranged in
rows; internal mycelium inconspicuous, branched, septate,
subhyaline; external mycelium absent; stromata small,
25–40 µm diam., pale brown, textura angularis, sometimes
absent; conidiophores loosely fasciculate, 4–12, arising from
stromata or internal hyphae, emerging through stomata or
sometimes erumpent, straight to slightly sinuose or curved,
subcylindrical throughout or slightly geniculate-sinuous near
the apex, 20.0–90.0 ×3.0–6.0 µm, 0–3-septate, unbranched,
pale olivaceous-brown to brown, wall thin to slightly
thickened, smooth; conidiogenous cells integrated, terminal,
holoblastic, proliferating sympodially, subcylindrical to
geniculate-sinuous, 35.0–65.0 ×4.0–5.0 µm, pale towards
the apex, occasionally subhyaline; conidiogenous loci
slightly protuberant, somewhat thickened and darkened,
2–10 per cell, 1.5–2.0 µm diam; conidia dry, solitary or
in short chains, holoblastic, cylindrical, subcylindrical-
obclavate, fusiform, straight to slightly curved, 15.0–67.0 ×
(2.5–)3.0–5.0(–6.0) µm, 0–4(–6)-septate, apex obtuse,
rounded, base obconically truncate, sometimes slightly
inflated at the basal cell, guttulate, subhyaline, thin-
walled, smooth, hila slightly thickened and darkened,
1.5–2.0 µm wide.
Passalora fusimaculans var. barretoana was introduced
for collections on Echinochloa polystachya from Brazil,
similar to Passalora fusimaculans (GF Atk.) U Braun &
Crous, but distinct from this taxon by having wider conidia.
Although P. fusimaculans has conidia 1.5–3 µm wide, var.
barretoana has conidia 3–5 µm wide (Crous and Braun
2003). Recently, Schubert and Braun (2005) recognised a
new synonym of this species, Cladosporium piricularioides
Dearn. & House (nom. inval.), based on material collected
from the USA on Panicum boreale.
The raising of this variety to the species rank was based
on new observations made on the samples collected on
Hymenachne amplexicaulis from Brazil. This material bears
conidia that were consistently wider than those of var.
fusimaculans. This proposal emanates from a suggestion
made by the world authority on this group (U. Braun, personal
communication). The specimens on H. amplexicaulis agree
well with those on Echinochloa polystachya except for
some differences in symptoms (lesions in H. amplexicaulis
are foliar blights whereas lesions on E. polystachya
are punctiform).
Another characteristic, previously reported by Barreto
(1991), was that the primary conidia, in conidial chains in
populations of this fungus attacking E. polystachya, had
a distinctly inflated apex. The illustrations provided by
Barreto clearly show such inflated apices. Specimens of the
holotype and paratype were deposited in the IMI herbarium
Mycobiota of the weed Hymenachne amplexicaulis Australasian Plant Pathology 349
(IMI 345388 and IMI 345389). Although Crous and Braun
(2003) examined those specimens later they did not mention
this character. This character-state was not present in the
specimen obtained from H. amplexicaulis.
The placement of this fungus in the genus Passalora, rather
than in Cercospora, is considered here as preferable because
in the current concept of the latter genus, the formation
of conidial chains is regarded as abnormal and conidia
are generally hyaline and not subhyaline. If the colourless
conidia or the formation of chains are to be regarded as more
indicative of the generic affinity, this can only be eventually
answered by the use of molecular methods. A molecular
analysis of this taxon will be useful to confirm its placement
in Passalora (U. Braun, personal communication).
Paraphaeosphaeria michotii (Westend.) OE Erikss.
Cryptogams of the Himalayas 6: 405 (1967) (Figs 2–4)
Anamorph: Microsphaeropsis H¨
ohn.
Material examined: Brazil, BR 262, Km 641, between
Porto Morrinho and Fazenda Bodoquena, state of Mato
Grosso do Sul, 16 Aug. 2005, DJ Soares (VIC 29377).
Lesions on living leaves, circular to elliptic,
0.5–2.0 cm diam., pale grey, surrounded by a purple
halo; ascomata pseudothecial, isolated, immersed, globose,
80.0–210.0 µm diam., walls 3–5 cells, 5.0–13.0 µm thick,
yellowish brown, textura angularis;dehiscence ostiolate,
10.0–30.0 µm wide; pseudoparaphyses moniliform,
60.0–80.0 ×3.0–7.0 µm, guttulate, septate, constricted or
not at septa, hyaline, smooth; asci bitunicate, cylindrical
to clavate, short-pedicellate, 50.0–65.0 ×10.0–15.0 µm.
Ascospores cylindrical to fusiform, biseriate to inordinate,
slightly constricted at the septa, with rounded ends,
mostly 2-septate, sometimes 3–5 secondarily septate,
Fig. 2. Symptoms of Paraphaeosphaeria michotii on Hymenachne
amplexicaulis. Scale bar =2cm.
19.0–24.0(–35.0) ×5.0–7.0(–10.0) µm, golden brown,
punctate, guttulate, surrounded by a mucilaginous
sheath with constrictions in the regions where septa are
located; conidiomata equivalent in shape to the ascomata,
100.0–170.0 µm diam.; conidiogenous cells phiallidic,
subglobose to doliiform, 3.0–7.0 ×3.0–5.0 µm, hyaline;
conidia ovoid to obovoid, apically rounded, base somewhat
truncate, 6.0–9.0 ×3.5–5.0 µm, pale brown, smooth.
The genus Paraphaoesphaeria has been recently revised
in a series of publications (Wong et al. 2000; Cˆ
amara
et al. 2001, 2003; Checa et al. 2002) and two new genera,
based on molecular data and on anamorph features were
segregated, Neophaeosphaeria and Phaeosphaeriopsis
(Cˆ
amara et al. 2003). The genus Paraphaeosphaeria is now
restricted to two species, P. michotii and P. pilleata, having
2-septate ascospores, the first-formed septum being
submedian and having anamorphs belonging to
Microsphaeropsis (Wong et al. 2000; Cˆ
amara et al. 2003).
Following the new arrangement proposed by Cˆ
amara et al.
(2003) and the key of Paraphaeosphaeria species provided
by Wong et al. (2000), the specimen on Hymenachne
amplexicaulis fits well within P. michotii.
In the specimen described here, a pronounced
mucilaginous sheath surrounding the ascospores was
observed. Interestingly, this sheath has clear constrictions
on parts corresponding internally to places where the septa
of the ascospores are located. The only previous mention
of mucilaginous sheaths surrounding the ascospores of
P. michotii was made by Wong et al. (2000) but these
authors mentioned those sheaths as present only in young
ascospores, whereas we found the sheaths also in mature
ascospores. Although the specimen described here shows
some additional differences from previous descriptions
of P. michotii, such as the presence of ascospores that
sometimes have more than two septa and that are somewhat
wider, we decided not to propose any new name based on
these observations, even at the infra-specific level. In our
opinion this would be premature since there is considerable
variation between separate descriptions given for P. michotii
in the literature (Table 1). Additional investigations including
a wide range of isolates subjected to molecular analysis may
further clarify this situation in the future.
Recently, Lee et al. (2005) described Paraphaeosphaeria
recurvifoliae from Yucca recurvifolia. Only the anamorph
(Microsphaeropsis-like) was found and the new species was
described based on the results of the molecular analysis of the
ITS regions. The new species grouped with P. obtusispora
(Speg.) Cˆ
amara, ME Palm & AW Ramaley, P. glauco-
punctata (Grev.) Cˆ
amara, ME Palm & AW Ramaley,
P. nolinae (AW Ramaley) C ˆ
amara, ME Palm & AW Ramaley
and P. agavensis (AW Ramaley, ME Palm & ME Barr)
Cˆ
amara, ME Palm & AW Ramaley, all of which are known
to infect Yucca spp. and are now placed in the new genus
Phaeosphaeriopsis.
350 Australasian Plant Pathology D. J. Soares and R. W. Barreto
(a)
(b)
(e)
(g)
(c)
(d)
(f)
Fig. 3. Line drawing of Paraphaeosphaeria michotii.(a) Ascoma wall. Scale bar =50 µm. (b) Asci and
paraphyses. (c) Immature ascospores. (d) Mature ascospores. (e) Mature ascospores with mucilaginous
sheaths. (f) Abnormal ascospores showing secondary septation. (g) Conidiogenous cells and conidia. Scale
bar =10 µm.
One of the key characters of Phaeophaeriopsis,
according to Cˆ
amara et al. (2003), is that the anamorph is
placed in either Coniothyrium Corda or Phaeostagonospora
AW Ramaley. Paraphaeosphaeria recurvifoliae has,
according to its authors, a Microsphaeropsis-like
anamorph. Therefore, if only morphology were taken
into consideration, the new species was correctly placed
in Paraphaeosphaeria. Controversially, the molecular data
placed it in the Phaeosphaeriopsis clade, agreeing with
the new circumscription proposed by Cˆ
amara et al. (2003),
together with the species occurring on Yucca spp.
In the same paper, Lee et al. (2005) mistakenly
mentioned Cˆ
amara et al. (2002) as having segregated
the new genera Neophaeosphaeria and Phaeosphaeriopsis.
In fact, that publication dealt only with fungi in the
Leptosphaeria/Phaeosphaeria complex without any mention
of Paraphaeosphaeria and its segregates Neophaeosphaeria
and Phaeosphaeriopsis. A possible explanation for the
controversial situation of Para. recurvifoliae might be a
misinterpretation of the morphology of the fungus. The
conidiogenous cells of anamorphs in this group of fungi
are minute and hard to observe and interpret. Perhaps the
authors misinterpreted the nature of the conidiogenesis as
phialidic (as for Microsphaeropsis) instead of proliferating
percurrently (as for Coniothyrium). So, in this case, the
correct name to be applied to the specimen on Yucca
recurvifolia should be Phaeosphaeriopsis recurvifoliae.
Cˆ
amara et al. (2003) comment that sometimes the
anamorphs of species of Phaeosphaeropsis produce only
bacillar microconidia from simple and apparently non-
proliferating phialides. Lee et al. (2005) did not include
any illustrations of the conidiogenesis cells. Until the
Mycobiota of the weed Hymenachne amplexicaulis Australasian Plant Pathology 351
Fig. 4. Asci and ascospores of Paraphaeosphaeria michotii. Scale
bar =20 µm.
type is re-examined, and the status of conidiogenesis
cells elucidated, this taxon should be regarded as having
a dubious status.
Leptosphaeria grisea and Coniothyrium sp. were
previously recorded on Hymenachne from Cuba (Urtiaga
1986) and Venezuela (Urtiaga 2004), respectively.
Unfortunately, it is unknown whether Urtiaga left his
material deposited in a herbarium for consultation, but it
is likely that those two records would correspond to older
records of Para. michotii on H. amplexicaulis. As there
is no way to verify that possibility, the present record
should be regarded as the first record of Para. michotii on
H. amplexicaulis.
Phyllachora minutissima (Welw. & Curr.) AL Sm., J. Bot.,
London 36: 179 (1898) (Fig. 5)
Material examined: River Paraguay, Corumb´
a, state of
Matogrosso do Sul, Brazil, June 12, 2001 (VIC 26506);
BR 262, Km 641, between Porto Morrinho and Fazenda
Table 1. Biometric data from descriptions of P. michotii worldwide
Publication Asci (µm) Ascospores (µm) Conidia (µm)
Sivanesan (1984) 55.0–100.0 ×12.0–15.0 14.0–22.0 ×4.0–5.0 5.0–13.5 ×3.0–5.0
Wong et al. (2000) 60.0–80.0 ×12.0–18.0 16.0–24.0 ×4.0–5.0 –
Cˆ
amara et al. (2001) 40.0–60.0 ×7.0–15.5 11.5–20.5×3.5–6.5 4.0–8.0 ×2.5–4.5
Fukuhara (2002) 65.0–80.0 ×10.5–15.0 15.0–19.0 ×5.0 1.5–3.0 diam.
This publication 50.0–65.0 ×10.0–15.0 19.0–24.0 ×5.0–7.0 6.0–9.0×3.5–5.0
Bodoquena, state of Mato Grosso do Sul, Brazil, 16 Aug.
2005, DJ Soares (VIC-29375).
Lesions adaxially on leaves, as tar-spots surrounded
by a chlorotic halo, 0.1–0.3 cm wide, up to 0.6 cm long;
ascomata perithecial, immersed, isolated, sub-spherical
to variously distorted, 99.0–192.0 ×93.0–225.0 µm, wall
thickness variable 4.0–75.0 µm, of dark brown textura
angularis, smooth; clypeus well developed; dehiscence
ostiolate, indistinct; hamathecium of filiform paraphyses, up
to 200.0 µm long, 2.0–4.5 µm wide, aseptate, unbranched,
thin walled, hyaline, smooth; asci unitunicate, 8-spored,
non-fasciculate, cylindrical 64.0–155.0 ×8.0–12.5 µm;
ascospores usually uniseriate, sometimes biseriate, ovoid,
apically pointed, 15.0–18.0 ×5.5–7.5 µm, aseptate, thin-
walled, hyaline, smooth; spermogonia stromatic pycnidial
amphigenous, either produced close to the ascomata
or separate from teleomorph, subepidermal, isolated,
sometimes aggregated, usually flattened to lenticular,
sometimes distorted when produced close to ascomata, walls
of dark brown textura angularis, smooth; spermatiophores
obclavate, flexuous, single, 10.0–28.0×1.0–2.5 µm;
spermatia mucilaginous, enteroblastic, acicular, usually
slightly curved, 10.0–15.0 ×1.0–1.5 µm, aseptate, thin-
walled, hyaline, smooth.
The Phyllachora species occurring on grasses with higher
morphological affinity to the fungus on H. amplexicaulis and
having an acuminate apex to their ascospores are Phyllachora
acutispora Speg. and P. minutissima.
According to Parbery (1967), ‘Phyllachora acuminata
is different from P. minutissima in ascospore shape and
width, as well as in spermatiophore shape and size. The
general shape of each of these characters is similar in
each species but whereas P. acuminata has narrow elongate
spores, P. minutissima has broader, shorter ones. Similarly, the
spermatiophores of the two species are generally similar, but
there are slight differences in shape and marked differences
in size between them’.
P. minutissima is better known on Panicum and
Pennisetum in Africa, Asia and Oceania, but is also known
on Paspalum,Setaria and other grass hosts from the
Americas (Farr et al. 2005). P. acutispora is known to infect
mostly Paspalum spp. in the Americas and it was already
recorded on H. amplexicaulis from Venezuela (Farr et al.
2005). P. acustipora was originally described by Spegazzini
on Panicum sp. from Argentina in 1891. In 1899, the same
352 Australasian Plant Pathology D. J. Soares and R. W. Barreto
(a)(b)
Fig. 5. Line drawing of Phyllachora minutissima.(a) Asci, ascospores
and paraphyses. (b) Spermatiophores and spermatia. Scale bar =20 µm.
author described P. apiculata (now known as P. minutissima)
on Panicum grumosum also from Argentina. Recently
Gabel et al. (1999) gave new host records for P. acutispora
and P. minutissima from Argentina. The descriptions of
the morphology of the specimens included in these new
records indicated that there were no clear differences
between them.
Therefore, although Parbery (1967) considered
P. acutispora (as P. acuminata) and P. minutissima to
be distinct species, we believe that these fungi are the
same and would be better placed under a single name.
In this case the correct name is Phyllachora minutissima
(Welv. & Curr.) AL Sm., which would have priority over
P. acutispora. However, a final position on this matter will
have to be left for a future occasion on the condition that
the type material for the two species is located and in good
condition for a proper re-examination. The world authority
on the genus Phyllachora on grasses (Dr D Parbery)
is of the opinion that more reliance should be given to
ascospore shape than to small differences in size. He stated
that in P. acustipora, ascospores are regularly ellipsoid to
ovate-acuminate and somewhat more slender than those
of P. minutissima (D. Parbery, personal communication).
Perhaps only with molecular analysis and cross-inoculation
studies will we finally clarify this taxonomic puzzle
(D. Parbery, personal communication).
The fungus recently collected, by D. J. Soares, on
H. amplexicaulis has ascospores measuring 15–18 ×
5.5–7.5 µm agreeing well with P. acutispora, but the shape
of the ascospores, as well as the spermatiophore size,
10–28 ×1–2.5 µm, fit better within P. minutissima.
By following Parbery’s views we preferred to place the
specimen on H. amplexicaulis in P. minutissima.
The status of P. hymenachnei (Chard´
on) Arx & E M¨
ull.
is uncertain. Von Arx and M ¨
uller (1954) proposed the new
combination based only on a previous description of the
fungus. No herbarium specimen was seen by those authors.
The size of asci and ascospores is equivalent to those of
P. acutispora/P. minutissima, but there is no information on
ascospore shape, and Parbery did not include this fungus
in his monograph (Parbery 1967). It is, nevertheless, likely
that this taxon is conspecific with one of the two species
being discussed.
None of these fungi emerge from the field observations
and the literature studies as of particular interest for biological
control since they appear to have little impact on their hosts
and a host-range that is too wide. The survey work is still
continuing and it is hoped that novel fungi with more obvious
potential for classical introductions will be found attacking
this host.
Acknowledgements
The work forms part of a research project submitted
as a DSc dissertation to the Departamento de
Fitopatologia/Universidade Federal de Vic¸osa by DJ Soares.
The authors thanks the Fundac¸˜
ao de Amparo `
a Pesquisa
do Estado de Minas Gerais (FAPEMIG) and the Conselho
Nacional de Desenvolvimento Cient´
ıfico e Tecnol ´
ogico
(CNPq) for financial support. The authors would also like to
thank Dr Uwe Braun and Dr Douglas Parbery for their very
helpful suggestions and comments.
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