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Submitted 19 February 2019, Accepted 6 July 2019, Published 22 July 2019
Corresponding Author: Miguel Dorcino Xavier– e-mail – mdorcinoxavier@gmail.com 128
Morphological description and new record of Panaeolus acuminatus
(Agaricales) in Brazil
Xavier MD1, Silva-Filho AGS2, Baseia IG3 and Wartchow F4
1 Curso de Graduação em Ciências Biológicas, Centro de Biociências, Universidade Federal do Rio Grande do
Norte, Av. Senador Salgado Filho, 3000, Campus Universitário, 59072-970, Natal, RN, Brazil
2 Programa de Pós-Graduação em Sistemática e Evolução, Centro de Biociências, Universidade Federal do Rio
Grande do Norte, Av. Senador Salgado Filho, 3000, Campus Universitário, 59072-970, Natal, RN, Brazil
3 Departamento de Botânica e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Av.
Senador Salgado Filho, 3000, Campus Universitário, 59072-970, Natal, RN, Brazil
4 Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, Conj. Pres. Castelo Branco III, 58033-
455, João Pessoa, PB, Brazil
Xavier MD, Silva-Filho AGS, Baseia IG, Wartchow F 2019 – Morphological description and new
record of Panaeolus acuminatus (Agaricales) in Brazil. Studies in Fungi 4(1), 128–134, Doi
10.5943/sif/4/1/16
Abstract
Panaeolus acuminatus is described and illustrated based on fresh specimens collected from
Northeast Brazil. This is the second known report of this species for the country, since it was
already reported in 1930 by Rick. The species is characterized by the acuminate, pileus with
hygrophanous surface, basidiospores measuring 11.5–16 × 5.5–11 µm and slender, non-capitate
cheilocystidia. A full description accompanies photographs, line drawings and taxonomic
discussion.
Key words – Agaricomycotina – Basidiomycota – biodiversity – dark-spored – Panaeoloideae –
Rick
Introduction
Species of Panaeolus (Fr.) Quél. are commonly recognized by their typically coprophilous
or nitrophilous habitat, slender fruit-body with cartilaginous stipe and spotted gills originated by
the maturation pattern of the basidiospores, in which they are distinctly smoky to dark brown,
smooth, thick-walled, not discoloring in sulphuric acid and with a well-marked apical germ-pore
(Watling & Gregory 1987, Gerhardt 1996). This genus has worldwide distribution (Gerhardt
1996) but uncertain taxonomic position (Tóth et al. 2013).
In Brazil, Panaeolus and its allies genera (Panaeolina Maire, Copelandia Bres. and
Anellaria P. Karst.) were poorly documented and the occasional records are known from South,
Southeast, Midwest and Northeastern regions (Maia et al. 2015). Rick (1930) described P.
lignicola Rick., and reported P. acuminatus (P. Kumm.) Quél., P. atro-sanguineus Henn, P.
campanulatus (Bull.) Quél., P. solidipes (Peck) Sacc., P. semiovatus var. phalaenarum (Fr.) Ew.
Gerhardt [as P. phalaenarum (Fr.) Quél.], P. fimicola (Fr.) Quél. and P. papilionaceus (Bull.)
Quél., all from Rio Grande do Sul state. However some species need to be revised, since these
names might correspond to misidentifications, synonyms or missed specimens (Silva-Filho et al.
2019). Stijve & De Meijer (1993) recorded P. antillarum (Fr.) Dennis and P. cinctulus (Bolton)
Studies in Fungi 4(1): 128–134 (2019) www.studiesinfungi.org ISSN 2465-4973
Article
Doi 10.5943/sif/4/1/16
129
Sacc. from Paraná State. De Meijer (2001) in his first macrofungi checklist recorded P.
papilionaceus (Bull.) Quél. from the state of Paraná. Sobestiansky (2005) recorded P. antillarum
from Santa Catarina and P. cinctulus and P. papilionaceus from Rio Grande do Sul. De Meijer
(2006) in his second checklist reported P. aff. reticulatus Overh. also from Paraná. More recently
Panaeolus rickenii Hora was recorded from Mato Grosso do Sul, the first occurrence from
Midwest (Bononi 2017). More recently, P. antillarum and P. papilionaceus were recorded again
from Paraná, together with the description of P. sylvaticus Silva-Filho & Cortez (Silva-Filho et al.
2019). Synonyms of other species also were reported from Brazil: Panaolus foenisecii (Pers.) J.
Schröt. (currently a member of Panaeolina) by Stijve & De Meijer (1993), and P.
cambodginiensis Oláh & R. Heim and P. aff. tropicalis Olah, (synonym of species of Copelandia)
by De Meijer (2006). Recently, Panaeolus cyanescens (Berk. & Broome) Sacc. synonym of
Copelandia cyanescens (Berk. & Broome) Singer was recorded from Paraná and Pernambuco (De
Meijer 2001, Wartchow et al. 2010, Silva-Filho et al. 2018). From northeast Brazil, only
Panaeolus antillarum is known (Alves & Cavalcanti 1996, Melo et al. 2016).
Here we report the second occurrence of P. acuminatus from Brazil, and a revision of the
Rick’s exsicates of P. acuminatus and recent collection of P. rickenii from Brazil described as a
variety of P. acuminatus. The species collected in northeast of Brazil and represents a new record
in tropical region of America.
Materials & Methods
The specimen was found on sandy soil in a grassland of an urban area (5°54'59.9" S and
35°13'02.9" W), in the municipality of Parnamirim, located in the metropolitan region of Natal,
Rio Grande do Norte (Fig. 1). Methods for analysis and description of agarics were made
following Singer (1986) and macro- and microstructures were described according to terminology
used by Largent (1986) and Largent et al. (1977). To determine the names and color codes we
used Kornerup & Wanscher (1978).
Fig. 1 – Map showing the collection site of the new report to Rio Grande do Norte, Parnamirim,
collected in 2015, and the two collections of Rick to Rio Grande do Sul, São Leopoldo, collected
in 1929 and Salvador do Sul, collected in 1944.
The length × width in face-view × width in side-view of basidiospores were measured; the
length of the basidia were measured excluding sterigmata. The value of Q was calculated as the
quotient between the length and width, ‘Qm’ is the value averaged from ‘Q’ and ‘n’ is the number
of measured basidiospores/number of analyzed basidiomata/number of collections (Bas 1969).
130
Specimens were deposited at the Fungal Collection of the Universidade Federal do Rio Grande do
Norte (UFRN-Fungos). Identification was made through keys proposed for the genus (Ola’h 1969,
Watling & Gregory 1987, Young 1989, Gerhardt 1996) and by comparison with Rick materials
loaned by the herbarium PACA (Thiers continuously updated). Generic taxonomical concepts
followed Gerhardt (1996).
Results
Panaeolus acuminatus (P. Kumm.) Quél., Mém. Soc. Émul. Montbéliard 5: 257 (1872). Figs 2–3
≡ Agaricus acuminatus Schaeff. Fung. Bavar. Palat. nasc. 4: 44, t. 202 (1774).
Facesoffungi Number: FoF 05841
Pileus 13–15 mm diam., conic-campanulate, with a prominent rounded apex, surface
smooth, dry, hygrophanous, margin slightly crenate, brownish-beige (6E3) to light brown (6D5).
Lamellae adnexed, ventricose, brownish grey (5F2) with darker spots, crowded, narrow,
lamellulae not observed. Stipe 20–70 × 1.8–2 mm, central, equal, cylindrical, fistulose, surface
slightly longitudinally-striated, consistency cartilaginous, ranging from brown (5C4) to brownish
orange (5B6). Context thin (< 1 mm), pale yellow (4A3). Veil absent. Spore print dark grey brown
(1F1).
Basidiospores 11.5–14.5 × 5.5–9.5 × 5.5–8 µm, (average = 12.6 × 8.6 × 7.3 µm, Q = 1.2–
1.7, Qm = 1.4, n = 30/2/2), limoniform to sublimoniform, rhomboid in face view, ellipsoid in side-
view, smooth, thick-walled (0.6–1.4 µm), strongly flattened, apically truncate by a central germ-
pore, dark brown in KOH (Figs 2c, 3d). Basidia 15–20.5 × 8–11.5 µm, broadly clavate to
cylindric-clavate, 1-2-4 spored, predominantly 2-spored, hyaline (Fig. 3e). Pleurocystidia absent.
Lamellae edge sterile. Cheilocystidia 24.5–33.1 × 7–8 µm, slender, slightly lageniform, slightly
flexuous, abundant, thin walled, hyaline. Lamellae trama regular with filamentous to inflated
hyphae 6.5–14.5 µm diam., thin-walled, hyaline. Subhymenium cellular composed by
isodiametric cells 3–7.5 × 3–7 µm, thin-walled, hyaline, light brown. Pileipellis an epithelium
composed by isodiametric to broadly clavate cells, 11.5–43 × 11.5–37.5, thin walled, hyaline
(Fig. 3b). Pileocystidia 10.5–35.5 × 5.5–8.5, cylindrical to slightly lageniform, sometimes with
subcapitate apex, scattered, thin-walled, predominately brownish, sometimes hyaline.
Hypodermium a layer of interwoven, filamentous hyphae, 1.5–4.5 µm diam., anticlinal, smooth,
thin-walled, light brown. Pileus trama composed by interwoven hyphae 5.5–16.5 µm diam.,
anticlinal, thin walled hyaline. Stipitipellis a cutis, composed of filamentous hyphae 1.5–6 µm
diam., smooth, hyaline. Stipe trama regular, with longitudinally oriented hyphae 4.5–12.5 µm
diam., smooth, hyaline. Caulocystidia 18.5–39 × 3.5–12 µm, lageniform, slender, slightly
flexuous, frequent to abundant, thin walled, hyaline. (Fig. 3a). Clamp connections absent in all
tissues examined.
Habitat – Scattered to gregarious, in a lawn without herbivorous dung, and on sandy soil in a
sheltered location near urban area.
Distribution – Worldwide: Africa (Pegler 1977), Asia (Vrinda et al. 1999), Europe (Watling
& Gregory 1987, Gerhardt 1996), North America (Morgan 1907), South America (Rick 1930,
Niveiro & Albertó 2012), and Australia (Cleland 1934).
Material examined – Brazil, Rio Grande do Norte, Parnamirim, Parque das Árvores, on
grassland, 24 April 2015, M.D. Xavier MDX-001, (UFRN-Fungos 3072).
Additional material examined – Panaeolus acuminatus: Brazil, Rio Grande do Sul, Salvador
do Sul, São Salvador, 19 January 1944, J. Rick s/n (PACA 20917); and São Leopoldo collected in
1929, J. Rick s/n (PACA 14494); Panaeolus rickenii: Brazil, Mato Grosso do sul, Maracaju
Mountains, Corguinho, 12 November 2014, A.K.M. Oliveira et. al. (SP466286).
131
Fig. 2 – Panaeolus acuminatus (UFRN-Fungos 3072): a-b Basidiomata. c Basidiospores. Scale
bars: a-b = 10 mm, c = 10 μm.
Fig. 3 – Panaeolus acuminatus (UFRN-Fungos 3072): a Cheilocystidia. b Pileipellis showing the
epithelium structure with one pileocystidium indicated with an arrow. c Caulocystidia.
d Basidiospores. e Basidia and basidioles. Scale bars: a-e = 10 μm.
132
Discussion
Panaeolus acuminatus was originally described by Schaeffer (1774) as Agaricus
acuminatus. However, there are no exsiccates associated with the name, leaving only the
Schaeffer’s illustration as a lectotype (Gerhardt 1996). The species has many synonyms. It was
also named as Coprinarius acuminatus (Quél.) Quél., Stropharia acuminata (Scop.) Murrill. and
Agaricus carbonarius Batsch. Other authors described the same species under other names, all
also synonyms. Junghuhn described in 1830 A. caliginosus Jungh., in which was interpreted later
as P. caliginosus (Jungh.) by Gillet (1878). In addition, the epithet caliginosus was recombined to
Chalymmota caliginosa (Jungh.) P. Karst. and Coprinarius caliginosus (Jungh.) Quél. in 1879 and
1886 respectively. They also are synonyms of P. acuminatus. Unfortunately the material
described by Junghuhn has not been found so far (Gerhardt 1996). Gerhardt (1996) reviewed
many specimens belonging to this species and proposed an epitype (Gerhardt 83049) for P.
acuminatus, deposited in Botanisches Museum Berlin.
Our specimens agree with in many aspects the descriptions provided by Gerhardt (1996) due
its acuminate, very pointed or rounded pileus, hygrophanous pileus surface, dark-brown flattened
basidiospores, absence of pleurocystidia and slender cheilocystidia (Gerhardt 1996). We also
compared our description with the ones performed by Watling & Gregory (1987) and Gerhardt
(1996) as shown in the Table 1.
Table 1 Morphologic comparison among Brazilian collection of P. acuminatus, Gerhardt (1996)
and Watling & Gregory (1987).
This study
Gerhardt (1996)
Watling & Gregory (1987)
Pileus size
13–15 mm
10–40 mm
20–40 mm
Pileus shape
Conic-campanulate, with
a rounded apex
Convex, with
pronounced pointed to
rounded apex
Never parabolic, with pointed
or rounded apex
Stipe size
20–70 × 1.8–2 mm
30–25 × 1.5–3 mm
35–50 × 2–3 mm
Basidiospore size
11.5–14.5 × 5.5–9.5 ×
5.5–8 µm
13–15 × 9–11 × 7–8
µm
12–15 × 9–11× 7–9 µm
Number of
sterigmata
mostly 2
2 and 4
4
Basidia size
15–20.5 × 8–11.5 µm
25–30 x 10–13 µm
27.5–35(–40) x 8.5–12.5 µm
Cheilocystidia size
24.5–33.1 × 7–8 µm
Not informed
25–35 x 8.5–12.5 µm
Cheilocystidia
shape
Slightly lageniform,
slightly flexuous
Slightly lageniform
Filiform-cylindric, slightly
swollen towards the apex
Furthermore, we examined two Rick’s collections, PACA 20917 and PACA 14494. The
tissues did not rehydrate satisfactorily. However, the identification of the species was confirmed
from the characteristics of the basidiospores [limoniform to sublimoniform, rhomboid in face
view, ellipsoid in side-view, smooth, thick-walled (0.6–1.4 µm), strongly flattened, apically
truncate by a central germ-pore; basidiospores size; 10.5–15 (–15.5) × 5–9 × 6.5–11 µm], and the
chemical reaction, on which they do not discolor in sulphuric acid.
According to Gerhardt (1996), P. acuminatus belongs to subgen. Panaeolus sect.
Laevispora sensu Gerhardt (1996), due to dry, hygrophanous pileus, lack of veil remnants, smooth
basidiospores, absence of metuloids and cheilocystidia with yellowish droplets or content. Among
the species of the sect., P. bernicis A.M. Young, P. fimicola (Pers.) Gillet and P. microsporus
Ola'h & Cailleux have sulphidia (Gerhardt 1996). Panaeolus fraxinophilus A.H. Sm. is a
lignicolous species that grows on Fraxinus sp. (Gerhardt 1996). Panaeolus alcidis M.M. Moser
and P. subfirmus P. Karst have larger basidiospores, measuring 16–18 × 11–12.5 × 8.5–10 µm and
16–20 × 10–11 × 9–10 µm respectively, while P. reticulatus Overh. has smaller ones 8.5–11 ×
6.5–8 × 5–6 µm (Gerhardt 1996). Panaeolus cinctulus (Bolton) Sacc. resembles only the flattened
133
spores (7–8 µm in side view), but it is easily distinguished by having much fleshier basidiomes
and larger and broader often capitaded cheilocystidia 30–50 × 8–12 µm (Gerhardt 1996).
Panaeolus paludosus Cleland is the most similar species, in which also shares the dark,
hygrophanous and campanulate pileus tending to be hemispherical to convex, without veil
remnants. However, P. paludosus has rhomboid transparent basidiospores (11.4–14 × 9–10 × 6–7
µm) and more bulbous cheilocystidia 25–40 × 7–10 µm (Gerhardt 1996).
Panaeolus rickenii is other similar species distinguished by Hora (1960) based in collections
with capitate-clavate cheilocystidia. This species was described as a variety of P. acuminatus by
Gerhardt (1996), although Watling & Gregory (1987) considered as an autonomous taxon. More
recently, P. rickenni was reported from Mato Grosso do Sul by Bononi et al. (2017), and we
checked its exsiccate SP 466286. The Brazilian collection of P. rickenii has larger 20–30 mm and
non-acuminated pileus (see the picture in Bononi et al. 2017: 364), light brown to brown
basidiospores, basidia predominantly with four sterigmata, and sphaeropenduculate to ventricose-
fusoid then cylindrical with mucronated apex cheilocystidia (20–34 × 9–14 µm). On the other
hand, our collections of P.acuminatus presents smaller (13–15 mm diam.) and slightly acuminated
pileus, brown basidiospores, basidia predominantly bi-spored and lageniform thin-walled
cheilocystidia 24.5–33.1 × 7–8 µm.
There are two records of P. acuminatus in South America: one from Argentina and another
from the subtropical region of and Brazil (Rick 1930, Niveiro & Albertó 2012). Now we recorded
for the first time Northeast of Brazil, proving that in South America, this species is not restricted
to subtropical regions. In addition, P. acuminatus and its related species, probably form a species-
complex that need a molecular and phylogenic analysis for understand the positioning of the
species and the validity of some of the names used in their taxonomy.
Acknowledgements
The authors would like to express their thanks to Dra. Maria Salete Marchioretto from
PACA herbarium and Adriana de Mello Gugliotta from SP herbarium for loan of the specimens,
CNPq (Brazilian National Council for Scientific and Technological Development) for the
scientific initiation scholarship and CAPES-(Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior) for the PhD scholarship awarded to Alexandre G. S. Silva-Filho.
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