Research, Society and Development, v. 11, n. 10, e103111032395, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i10.32395
Small reserves as hotspots for Fungi preservation in Brazil
Pequenas reservas como hotspots para preservação de fungos no Brasil
Pequeñas reservas como hotspots para la preservación de hongos en Brasil
Received: 06/07/2022 | Reviewed: 07/15/2022 | Accept: 07/17/2022 | Published: 07/24/2022
Fernando Augusto Bertazzo-Silva
ORCID: https://orcid.org/0000-0002-2179-1492
Universidade Federal do Pampa, Brazil
E-mail: fernandobertazzo@gmail.com
Aline Bezerra da Silva Santos
ORCID: https://orcid.org/0000-0001-6875-5934
Universidade Federal de Goiás, Brazil
E-mail: alinebezerradasilvasantos@gmail.com
Ana Rita Gaia Machado
ORCID: https://orcid.org/0000-0002-4255-5683
Centro Universitário Fametro, Brazil
E-mail: ana.machado@fametro.edu.br
Salomão Rocha Martim
ORCID: https://orcid.org/0000-0003-0789-2411
Universidade Nilton Lins, Brazil
E-mail: salomao.martim@uniniltonlins.edu.br
Ina de Souza Nogueira
ORCID: https://orcid.org/0000-0003-4908-6442
Universidade Federal de Goiás, Brazil
E-mail: isnogueira.ufg@gmail.com
Marisa Terezinha Lopes Putzke
ORCID: https://orcid.org/0000-0002-2004-8410
Universidade de Santa Cruz do Sul, Brazil
E-mail: marisa@unisc.br
Maria Francisca Simas Teixeira
ORCID: https://orcid.org/0000-0002-9703-1932
Universidade Federal do Amazonas, Brazil
E-mail: mteixeira@ufam.edu.br
Jair Putzke
ORCID: https://orcid.org/0000-0002-9018-9024
Universidade Federal do Pampa, Brazil
E-mail: jrputzkebr@yahoo.com
Abstract
Small conservation areas have been created in many countries usually to protect plants and animals, but no priorities
are deserved in protecting fungi. The creation of preservation areas is meeting a new problem: there are only small
remaining areas, since exploration is destroying large forests. Applying the technique of the transects in three different
areas in Brazil (Pampa and Cerrado biomes and Amazonian Forest), diversity and ecological data were collected for
Agaricomycetes fungi, mainly order Agaricales, and compared to the fungi already known and their conservation
status to understand how fungi are protected indirectly with the creation of small protected areas. The samples were
collected in differents permanent protected areas (APP – permanent protected areas) in river margins in southern
Brazil (RPAS), Saint Hilaire Forest in the Universidade de Goiás (MSH - ca. 20 ha) in Goiânia/GO and in the
Universidade Federal do Amazonas Protected Forest (Manaus/AM - MUFAM), all located in Brazil. In MUFAM, 140
specimens were collected in 2014 and 2018 resulting in 47 species. In MSH 86 specimens were collected in 2019 and
2020 with 31 species identified. In RPAS 278 new species records for the Brazilian Pampa biome were cataloged, 23
new records for the state of Rio Grande do Sul and 4 new registrations for Brazil. This demonstrates the importance
of small forest fragments to fungi preservation and maintenance, being efforts in that direction important in future
studies of new conservation areas implementation.
Keywords: Mycogeography; Mushrooms; Agaricales; Agaricomycetes; Basidiomycota; Protection areas.
Resumo
Pequenas áreas de conservação foram criadas em muitos países geralmente para proteger plantas e animais, mas
nenhuma prioridade é direcionada à proteção de fungos. A criação de áreas de preservação está enfrentando um novo
problema: restam apenas pequenas áreas, já que a exploração está destruindo grandes florestas. Aplicando a técnica
dos transectos em três diferentes áreas do Brasil (biomas Pampa e Cerrado e Floresta Amazônica), foram coletados
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Research, Society and Development, v. 11, n. 10, e103111032395, 2022
(CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v11i10.32395
dados ecológicos e de diversidade para os fungos Agaricomycetes, principalmente ordem Agaricales, e comparados
com os fungos já conhecidos e seu estado de conservação para entender como os fungos são protegidos indiretamente
com a criação de pequenas áreas protegidas. As amostras foram coletadas em diferentes áreas de proteção permanente
(APP – áreas de proteção permanente) nas margens de rios no sul do Brasil (RPAS), Floresta Saint Hilaire na
Universidade de Goiás (MSH - ca. 20 ha) em Goiânia/GO e na Floresta Protegida da Universidade Federal do
Amazognas (Manaus/AM - MUFAM), todas localizadas no Brasil. No MUFAM, foram coletados 140 exemplares em
2014 e 2018 resultando em 47 espécies. No MSH foram coletados 86 exemplares em 2019 e 2020 com 31 espécies
identificadas. No RPAS foram catalogados 278 novos registros de espécies para o bioma Pampa brasileiro, 23 novos
registros para o estado do Rio Grande do Sul e 4 novos registros para o Brasil. Isso demonstra a importância de
pequenos fragmentos florestais para a preservação e manutenção de fungos, sendo os esforços nesse sentido
importantes em estudos futuros de implantação de novas áreas de conservação.
Palavras-chave: Micogeografia; Cogumelos; Agaricales; Agaricomycetes; Basidiomycota; Áreas de proteção.
Resumen
Se han creado pequeñas áreas de conservación en muchos países, generalmente para proteger plantas y animales, pero
no se da prioridad a la protección de los hongos.. La creación de áreas de preservación está encontrando un nuevo
problema: solo quedan pequeñas áreas remanentes, ya que la exploración está destruyendo grandes bosques.
Aplicando la técnica de los transectos en tres áreas diferentes de Brasil (biomas de Pampa y Cerrado y Selva
Amazónica), se recolectaron datos de diversidad y ecológicos para los hongos Agaricomycetes, principalmente del
orden Agaricales, y se compararon con los hongos ya conocidos y su estado de conservación para comprender cómo
los hongos se protegen indirectamente con la creación de pequeñas áreas protegidas. Las muestras fueron recolectadas
en diferentes áreas protegidas permanentes (APP – áreas protegidas permanentes) en márgenes de ríos en el sur de
Brasil (RPAS), Bosque Saint Hilaire en la Universidade de Goiás (MSH - ca. 20 ha) en Goiânia/GO y en el Bosque de
Protección de Universidade Federal do Amazonas (Manaus/AM - MUFAM), todos ubicados en Brasil. En el
MUFAM se recolectaron 140 ejemplares en 2014 y 2018 dando como resultado 47 especies. En MSH se recolectaron
86 especímenes en 2019 y 2020 con 31 especies identificadas. En RPAS se catalogaron 278 nuevos registros de
especies para el bioma pampeano brasileño, 23 nuevos registros para el estado de Rio Grande do Sul y 4 nuevos
registros para Brasil. Esto demuestra la importancia de los pequeños fragmentos de bosque para la preservación y el
mantenimiento de hongos, siendo los esfuerzos en esa dirección importantes en futuros estudios de implementación de
nuevas áreas de conservación.
Palabras clave: Micogeografía; Hongos; Agaricales; Agaricomycetes; Basidiomycota; Áreas de protección.
1. Introduction
Even though small reserves are extremely common around the world, studies on their conservational value are
disproportionally uncommon in scientific works, which usually focus on defining their value relative to one large reserve, to
one or two taxa or ecosystem types (Volenec & Dobson, 2019). Despite many efforts being done in Europe and North America
to preserve fungi biodiversity, few initiatives are under course in South America, except for creation of preservation areas but
without referring to fungi species. Most European countries have generated red lists for fungi but this is not true for countries
in Latin America (Senn-Irlet et al., 2007).
The lack of knowledge is one of the major problems relating to fungi preservation, especially in South America,
where countries with high biodiversity numbers like Brazil and Colombia, which have incomplete fungal species lists, are still
beginning to study the complex ecological role of this group (Putzke & Putzke 2017; Putzke et al. 2020, 2021). But it is also a
problem to all the world since only 56 species of fungi have their status evaluated globally by the UCN red list (Hawksworth et
al. 2017).
Habitat reduction and pollution are considered the most important causes of worldwide loss of biodiversity, being the
creation of small reserves also of huge importance (Serengil et al., 2011; Avigliano et al., 2019). Agaricales fungi are generally
annual and popularly known as mushrooms. They began to be studied by specialists in Brazil mostly in the XIX century
(Fidalgo, 1985). The list counts for 1.011 species (Putzke, 1994) increased to ca. 1800 in 2018 (Putzke & Putzke, 2018). The
studies done so far are essentially taxonomic, and rarely ecological/conservational or involving relationships between the fungi
and the forest and rarely on preservation of fungi.
There are also citations of introduced fungi in this country and preoccupations are related to the fact that those species
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could contact native plants to form mycorrhiza, competing with the native fungi species. One recent example of such invasion
is cited in South America were Amanita muscaria (L.) Lam., usually associated with pine plantations is now found associated
with a native oak species of Colombia (Vargas et al. 2019). The impact of these exotic species to this exclusive forest and over
other native fungi needs to be better studied.
There are six terrestrial biomes recognized in Brazil: Pampa, Cerrado, Amazônia, Caatinga, Mata Atlântica and
Pantanal. The first three are among the less studied in relation to their biodiversity. The Brazilian Pampa biome covers an
average area of 176,496 km² and is characterized by being restricted only to Rio Grande do Sul State (southern Brazil),
Uruguay and parts of Argentina. The biome is formed by the phytogeographic regions Contact Savana-Steppe, Steppe,
Deciduous Seasonal Forest, Semi-deciduous Seasonal Forest and Pioneer Vegetation Areas (IBGE, 2012). The forest
formations are basically found along the watercourses in the region, and must host an unknown biodiversity since they
correspond to the last remnants of natural forest (Metzger, 2003).
The Cerrado is considered the largest hotspot in the Western Hemisphere, and the most biodiverse tropical savanna in
the world, with an approximate extension of 2 million km2, with about 99.3% of its area is in Brazil (Sawyer et al., 2016). The
cerrado is formed by a complex vegetation, including forest, grassland, and savannah formations, with a high number of
endemic species (Ribeiro & Walter, 2008). The Atlantic Forest has the largest number of fungi records (3,017 species),
followed by Amazonia (1,050), Caatinga (999), Cerrado (638) and Pampa (84) and Pantanal (35) (Maia et al. 2015). This
shows that the 3 biomes selected for this study are poorly surveyed. In a recently published work on fungi in Brazil (BFG et al.
2021), 1461 species of fungi were reported for the state of Rio Grande do Sul, 867 species for the Amazon and 189 species for
Goiás, characterizing Goiás as the seventh Brazilian state with lower occurrence of Fungi in the country. The states of Rio
Grande do Sul and Amazonas stand out as the third and fourth, respectively, with more species of fungi in Brazil, however, in
Rio Grande do Sul, most of the work was carried out in the Atlantic Forest biome, highlighting the importance of carrying out
work in the Pampa biome (Silva et al., 2020).
Many initiatives to preserve the biodiversity in Brazil have been done by universities, many of them creating and
maintaining forests inside their campus or creating and managing small areas outside. This is the case of forest inside the
Universidade Federal do Amazonas (northern Amazonian Forest), in the Universidade Federal de Goiás (UFG - Middle West
region - Bosque Auguste Saint Hilaire of the UFG has 27 hectares). It is important also the forest relicts in the river margins,
called Permanent Protected Areas and that sometimes are small forest but its fungi composition is still not well studied. In
order to better understand the importance of small areas in preserving fungi, specially Agaricomycetes, this work is proposed,
dealing with the taxonomy and distribution of this group in the small natural reserves of Brazil, choosing areas in Southern,
Central and northern Brazil.
2. Methodology
There were chosen two small reserves (one in Amazonia and other in central Brazil) and Permanent Protected Areas
near rivers in Southern Brazil. The areas are described below:
2.1 Sampling in the Amazonas (Northern Brazil):
The area of the UFAM campus is 6.7 million meters square, with a perimeter of 16.9km of land. This area is the third
largest natural fragment in an urban area in the world and the first in the country, which contributed for the creation of the
Environmental Protection Area - APA UFAM. The APA was created in 2012, totaling 759.15ha, encompassing fragments of
the Amazonian Forest, now totally isolated (Caldas, 2016). The field survey was done from February 19 to 24 2018, in the
forest preserved inside the campus of the Universidade Federal do Amazonas (UFAM). The samples were collected using the
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“walking methodology” (Filgueiras et al., 1994), searching for Agaricomycetes fungi. The samples were studied in the
Mycology Laboratory of the UFAM and all collections dehydrated and deposited in the JP herbarium.
2.2 Sampling in Goiás (Center Brazil):
Samples were collected during the rainy seasons 2018/2019 and 2020/2021 in the Bosque Auguste Saint Hilaire of the
Universidade Federal de Goiás (UFG - Campus II), located in Goiânia city, the capital of Goiás state in the coordinates 16º
36’11” S and 49º15’39” W, at 695 m alt. and has ca. 20 ha. One of the few areas with primitive vegetation in the municipality
of Goiânia, it is located on Campus II of the UFG. It is a remnant of the semideciduous forest of the Cerrado biome plant
formation. The site, which is protected by a screen and has ecological trails, and is used for the development of Environmental
Education activities, visitation of students of different levels and development of numerous scientific researches. The samples
were also collected using the walking methodology and were dehydrated and deposited in the Herbarium of the UFG.
2.3 Sampling in Rio Grande do Sul (Southern Brazil):
The collections in the Pampa biome were carried out in the state of Rio Grande do Sul, southern Brazil, in all seasons
of the year 2019. 10 collection points were selected in a longitudinal gradient between the municipalities of São Gabriel and
Porto Alegre (the capital), in which riparian vegetation occurs, with an approximate distance of 20 km from one point to
another. In all three areas the samples were collected using the walking methodology. All the mushrooms found were collected
and taken to the local laboratories for identification and samples were dehydrated and deposited in the herbarium housed in
each university. All samples from these three collecting areas photographed following the Macrofunge Image Capture Protocol
(Bittencourt et al., 2022) and the identification was made using microscopes and usual morphological/anatomical techniques,
as well as the specific bibliography available for the area (Putzke & Putzke, 2018).
3. Results
3.1 Manaus – MUFAM
There were collected 140 specimens, being identified 41 species (29.3%) (Table 1). The list is incomplete mostly
because of the poorly known large genera like Marasmius, Marasmiellus and Mycena abundant in the mentioned forest. The
12 taxa (29.2%) not identified to species level are not cited to the country or represent new species to science. The Agaricales
fungi have received little attention in the Amazon region, especially in relation to basic taxonomic surveys. The works of
Singer (1973; 1976; 1989), Singer and Araujo (1979), Araújo (1984) and Singer & Aguiar (1986) demonstrate that diversity is
very large and adapted to regional conditions, but since then few studies have dedicated greater attention to this giant Brazilian
region (despite disperse in other surrounding countries). In the beginning of this century, basic agaricology has returned to be
the subject of studies, especially from the surveys carried out by Souza and Aguiar (2004) involving the Agaricales of the
Walter Egler Reserve, where 39 species are mentioned, but only 6 have been identified to the specific level, being many
specimens identified with a cf., aff. or sp.. Souza and Aguiar (2007) describe Marasmius species to the same area. Oliveira et
al. (2009) neotypify Marasmius amazonicus Henn. Since then, few surveys have been carried out, leaving the immense
agaricine flora of the state of Amazonas largely ignored.
3.2 Riparian Vegetation in Southern Brazil - RPAS
The riparian vegetation of the Brazilian Pampa Biome has been scarcely studied in terms of its agaricobiota, with
forest formations remaining rare in a predominantly herbaceous/shrub ecosystem. Studying these areas may allow establishing
new parameters for the distribution of Fungi. In this sense, 10 riparian forest formations were studied along a 200 km (east to
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west) transect in the center of Rio Grande do Sul state – Southern Brazil, in seasonal expeditions in 2019 to collect and identify
the agaricoid fungi species. 278 new species records for the Brazilian Pampa biome were cataloged, 23 new records for the
state of Rio Grande do Sul and 4 new registrations for Brazil (Table 2). Among the families found, there was a higher
incidence of Marasmiaceae (77 species), followed by Agaricaceae (45 species), Tricholomataceae (30 species) and
Mycenaceae (30 species), covering a total of approximately 65% of the collected species (Table 2).
3.3 Saint Hilaire Forest in the Universidade de Goiás (MSH) in Goiânia municipality - Goiás State
From the 86 samples collected, 31 were identified to species level and 51 to genus, the remaining only to family rank
(Table 1). The unidentified species were probably new citations or new species to science. Identified species related to the
place of occurrence. Table 1 - List of species collected in the forest preserved inside the campus of the Universidade Federal de
Manaus (UFAM) and Saint Hilaire Forest in the Universidade de Goiás (MSH) in Goiânia municipality - Goiás State.
3.4 Identified species related to the place of occurrence
Table 1 - List of species collected in the forest preserved inside the campus of the Universidade Federal de Manaus (UFAM)
and Saint Hilaire Forest in the Universidade de Goiás (MSH) in Goiânia municipality - Goiás State.
Species
Family
Agaricus dulcidulus Schulz.
Agaricaceae
X
Agaricus sp. 1
Agaricaceae
X
Agaricus sp. 2
Agaricaceae
X
Agaricus sp. 3
Agaricaceae
X
Agaricus sp. nov. 1
Agaricaceae
X
Agaricus sp. nov. 2
Agaricaceae
X
Agaricus porphyrizon P.D. Orton
Agaricaceae
Agrocybe sp. nov.
Strophariaceae
Bolbitius mexicanus (Murrill) Murrill
Bolbitiaceae
Callistosporium luteoolivaceum (Berk. & M.A. Curtis) Singer
Callistosporiaceae
X
Callistosporium sp.
Callistosporiaceae
X
Camarophyllopsis tetraspora (Singer) Raithelh.
Clavariaceae
X
Collybia sp.1
Tricholomataceae
X
Collybia sp.2
Tricholomataceae
X
Collybia sp.3
Tricholomataceae
X
Crinipellis perpusilla (Speg.) Singer
Marasmiaceae
X
Cyptotrama asprata (Berk.) Redhead & Ginns
Physalacriaceae
X
Cystoderma sp. 1
Agaricaceae
X
Cystoderma sp. 2
Agaricaceae
X
5
UFAM
MSH
X
X
X
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Cystolepiota sp. 1
Agaricaceae
X
Cystolepiota sp. 2
Agaricaceae
X
Entoloma sp. 1
Entolomataceae
X
Filoboletus gracilis (Klotzsch ex Berk.) Singer
Mycenaceae
Filoboletus sp. 1
Mycenaceae
X
Filoboletus sp. 2
Mycenaceae
X
Gerronema sp. 1
Marasmiaceae
X
Gymnopus dryophilus (Bull.) Murrill
Omphalotaceae
X
Hohenbuehelia paraguayensis (Speg.) Singer
Pleurotaceae
X
Hohenbuehelia testudo (Berk.) Pegler
Pleurotaceae
X
Hydropus floccipes (Fr.) Singer
Marasmiaceae
X
Hydropus sp. 1
Marasmiaceae
X
Hydropus sp. 2
Marasmiaceae
X
Hydropus sp. 3
Marasmiaceae
X
Hygrocybe sp. 1
Hygrophoraceae
X
Lactocollybia epia (Berk. & Broome)
Marasmiaceae
X
Lactocollybia sp.
Marasmiaceae
Lentinus crinitus (L.) Fr.
Polyporaceae
X
Lentinus sp1
Polyporaceae
X
Lepiota azurea Singer
Agaricaceae
X
Lepiota brunneoannulata Rick
Agaricaceae
X
Lepiota colorada A.B. Pereira
Agaricaceae
Lepiota micropholis (Berk. & Broome) Sacc.
Agaricaceae
X
Lepiota rickiana Speg.
Agaricaceae
X
Lepiota sp. 1
Agaricaceae
X
Lepiota sp. 2
Agaricaceae
X
Lepista glabella (Speg.) Singer
Tricholomataceae
X
Lepista sordida
Tricholomataceae
Lepista sp. 1
Tricholomataceae
Leucoagaricus confusus (Rick) Singer
Agaricaceae
Leucoagaricus lilaceus Singer
Agaricaceae
X
Leucoagaricus sp. 1
Agaricaceae
X
Leucocoprinus sp. 1
Agaricaceae
X
Leucocoprinus sp. 2
Agaricaceae
X
6
X
X
X
X
X
X
X
X
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Leucopaxillus gracillimus Singer & A.H. Sm.
Tricholomataceae
Macrolepiota sp.
Agaricaceae
X
Marasmiellus schiffneri (Bres.) Singer
Omphalotaceae
X
Marasmiellus spp.
Omphalotaceae
X
Marasmius bambusiniformis Singer
Marasmiaceae
X
Marasmius cecropiae Dennis
Marasmiaceae
X
Marasmius cladophyllus Berk.
Marasmiaceae
X
Marasmius ferrugineus Berk. & Broome
Marasmiaceae
X
Marasmius haematocephalus (Mont.) Fr.
Marasmiaceae
X
Marasmius inaequalis Berk. & M.A. Curtis
Marasmiaceae
X
Marasmius spp.
Marasmiaceae
X
Melanoleuca sp.1
Tricholomataceae
X
Melanophyllum sp.1
Agaricaceae
X
Mycena arcangeliana Bres.
Mycenaceae
X
Mycena epipterygia (Scop.) Gray
Mycenaceae
X
Mycena sp. 1
Mycenaceae
X
Mycena sp. 2
Mycenaceae
X
Mycena spinosissima (Singer) Desjardin
Mycenaceae
X
Mycobonia flava (Sw.) Pat.
Polyporaceae
X
Nalonea sp. 1
Entolomataceae
X
Nalonea sp. 2
Entolomataceae
X
Neoclitocybe byssiseda (Bres.) Singer
Tricholomataceae
X
Neopaxillus dominicanus Angelini & Vizzini
Serpulaceae
X
Nolanea pinna (Romagn.) Dennis
Entolomataceae
X
Nothopanus candidissimus (Sacc.) Kühner
Pleurotaceae
X
Nothopanus eugrammus (Mont.) Singer
Pleurotaceae
X
Oudemansiella canarii (Jungh.) Höhn.
Physalacriaceae
X
Oudemansiella steffenii (Rick) Singer
Physalacriaceae
X
Panellus pusillus (Pers. ex Lév.) Burds. & O.K. Mill.
Mycenaceae
X
Panus neostrigosus Drechsler-Santos & Wartchow
Panaceae
X
Pleurotus albidus (Berk.) Pegler
Pleurotaceae
X
Pleurotus macropus Bagl.
Pleurotaceae
X
Pluteus sp. 1
Pluteaceae
X
7
X
X
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Pluteus sp. 2
Pluteaceae
X
Psilocybe sp. 1
Strophariaceae
X
Rhodocybe gilvoides (Rick) Singer
Entolomataceae
Ripartitella brasiliensis (Speg.) Singer
Agaricaceae
X
Rugosospora pseudorubiginosa
(Cifuentes & Guzmán) Guzmán & Bandala
Agaricaceae
X
Schizophyllum commune Fr.
Schizophyllaceae
X
Schyzophyllum sp.
Schizophyllaceae
X
Stropharia sp.
Strophariaceae
X
Tetrapyrgos nigripes (Fr.) E. Horak
Marasmiaceae
X
Trichopilus sp. 1
Entolomataceae
Trogia cantharelloides (Mont.) Pat
Marasmiaceae
Volvariella sp. 1
Pluteaceae
X
X
X
X
X
X
X
Source: Authors (2022).
Table 2 – Species collected in the riparian vegetation point 1 to 10 with new citations to the state to Rio Grande do Sul (*) and
to Brazil (**).
Species
Family
Autum
Winter
Spring
Summer
Agaricus bisporus (J.E. Lange)
Agaricaceae
1
Agaricus dennisii Heinem.*
Agaricaceae
4,8
Agaricus endoxantus Berk. & Br.
Agaricaceae
6,9
Agaricus purpurellus
Agaricaceae
3,5,9
(Muell.) Muell.*
Agaricus sp
Agaricaceae
5
Agrocybe puiggarii (Speg.) Singer
Strophariaceae
6
Agrocybe underwoodii (Murrill) Singer*
Strophariaceae
1
Agrocybe sp. 1
Strophariaceae
10
Agrocybe sp. 2
Strophariaceae
Armillariella puiggarii (Speg.) Singer
Physalacriaceae
Bolbitius mesosporus Singer*
Bolbitiaceae
Bolbitius vitelinus (pers.) Fr.
Bolbitiaceae
4
Camarophyllus sp. 1
Hygrophoraceae
8
Campanella alba (Berk. Curt.) Singer
Marasmiaceae
Campanella aeruginosa Sing.*
Marasmiaceae
Cantharellus sp..
Cantharellaceae
2
4
3,6
3
3,9
6
8
2
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Chaetocalathus liliputianus (Mont.) Singer
Marasmiaceae
7
4,6
Cheimonophyllum candidissimum (B. & C.) Sing.
Marasmiaceae
9
3,5,7,10
Clitocybe dealbata (Sow. ex Fr.) Kummer
Tricholomataceae
Clitocybe radicellata Godey**
Tricholomataceae
Clitopilus scyphoides (Fr.) Singer
Entolomataceae
4
Clitopilus sp. 1
Entolomataceae
8
Collybia apiahyna Speg.
Tricholomataceae
Collybia dryophila (Bull. ex Fr.) Kummer
Tricholomataceae
3,4,6,7,8,10
Collybia jamaicensis (Murr.) Murr.*
Tricholomataceae
4,5,9
Collybia johnstonii (Murr.) Dennis *
Tricholomataceae
8,9
Collybia subfumosa Speg.
Tricholomataceae
4,5,6,7,8,10
Collybia sp. 1
Tricholomataceae
Collybia sp.2
Tricholomataceae
Collybia sp. 3
Tricholomataceae
Collybia sp. 4, sp.5, sp.6, sp.7
Tricholomataceae
5
Collybia sp. 8
Tricholomataceae
4
Conocybe pubescens (Gillet) Kuehner
Bolbitiaceae
5
Conocybe tenera (Schaeff. ex Fr.) Kuehner
Bolbitiaceae
5,6
Conocybe sp. 1
Bolbitiaceae
2
Copelandia sp. 1
Bolbitiaceae
Coprinus disseminatus (Pers.) Gray
Agaricaceae
1,2,3,4,7,8,9
Coprinus jamaicensis Murr.
Agaricaceae
6
Coprinus (Parasola) plicatilis (Curt.: Fr.) Fr.*
Agaricaceae
5,6,7,9,10
Coprinus sp. 1
Agaricaceae
9
Coprinus sp. 2
Agaricaceae
6
Coprinus sp. 3
Agaricaceae
5
Coprinus sp. 4
Agaricaceae
Crepidotus albidus Ellis & Everh.*
Inocybaceae
Crepidotus quitensis Pat.
Inocybaceae
Crepidotus sp. 1
Inocybaceae
9
Crinipellis macrosphaerigera Singer
Marasmiaceae
6,10
Crinipellis myrti Pat.
Marasmiaceae
Crinipellis stupparia (Berk. & Curtis) Pat.
Marasmiaceae
5
2
6
10
8
7
7
3
7
4,7
7
3
9
2
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Crinipellis sp. 1
Marasmiaceae
10
Crinipellis sp. 2
Marasmiaceae
7
Crinipellis sp. 3
Marasmiaceae
1
Crinipellis stupparia (Berk. & Curtis) Pat
Marasmiaceae
1
Cyptotrama asprata (Berk.) Redhead & Ginns
Physalacriaceae
Cyptotrama sp. 1
Physalacriaceae
5
Cystoderma sp. 1
Agaricaceae
6
Cystolepiota albogilva Sing. *
Agaricaceae
Cystolepiota sp. 1
Agaricaceae
7
Cystolepiota sp. 2
Agaricaceae
5
Cystolepiota sp. Nov.
Agaricaceae
5
Dictyopanus pusillus (Lév.) Singer
Mycenaceae
Dictyopanus sp. 1
Mycenaceae
Entocybe haastii (G. Stev.) Largent
Entolomataceae
Entoloma lampropus (Fries) Hesler
Entolomataceae
Entoloma ripartitoides Horak*
Entolomataceae
6
Entoloma sp. 1
Entolomataceae
10
Entoloma sp. 3
Entolomataceae
9
Entoloma sp. 4
Entolomataceae
8
Entoloma sp. 5
Entolomataceae
2
Fayodia sp. 1
Marasmiaceae
Filoboletus gracilis (Klotzsch ex Berk.) Singer
Mycenaceae
Filoboletus sp. 1
Mycenaceae
Flammulina velutipes (Curt. ex. Fr.) Singer
Physalacriaceae
Galerina stylifera (Atk.) A.H.Sm. & Sing.*
Hymenogastraceae
Galerina sp. 1
Hymenogastraceae
Gerronema fibula (Fr.) Singer
Marasmiaceae
Gerronema icterinum (Singer) Singer
Marasmiaceae
8
Gerronema stuckertii (Speg.) Singer
Marasmiaceae
4
Gerronema sp. 1
Marasmiaceae
10
Gerronema sp. 2
Marasmiaceae
Gymnopilus earlei Murrill
Hymenogastraceae
Gymnopilus pampeanus (Speg.) Singer
Hymenogastraceae
3,6,7,8,9
3,4,5,7,8,9
3,4,7
3,4,5,7,8,9,10
9
8
6
5
2,3,5,6,8
4
10
8
4
3
3,5,10
4
4
3
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Gymnopilus spectabilis (Weinm.) A. H. Smith
Hymenogastraceae
5,6,9
Gymnopilus sp. 1
Hymenogastraceae
Gymnopilus sp. 2
Hymenogastraceae
Gyroporus sp. 1
Gyroporaceae
Hemimycena perone (Berk. & Br.) Pegler
Mycenaceae
Hemimycena sp. 1
Mycenaceae
Hemimycena sp. 2
Mycenaceae
Hohenbuehelia atrocaerulea (Fries) Singer
Pleurotaceae
3,9
Hohenbuehelia nigra (Schw.) Singer
Pleurotaceae
6
Hohenbuehelia petalodes (Bull.) Schulzer
Pleurotaceae
Hohenbuehelia phalligera (Mont.) Singer
Pleurotaceae
10
Hohenbuehelia portegna (Spegazzini) Singer
Pleurotaceae
8,10
Hydropus riograndensis Singer
Marasmiaceae
Hydropus sp. 1, sp. 2
Marasmiaceae
10
Hydropus sp. 3
Marasmiaceae
7
Hydropus sp 4, sp.5, sp. 6
Marasmiaceae
5
Hydropus sp.7
Marasmiaceae
4
Hydropus sp. 8 Singer
Marasmiaceae
4,7,8,10
Hygrocybe coccinea (Schaeff.) ex Fr. Kum.*
Hygrophoraceae
4,5,10
Hygrocybe miniata (Fr.) Kummer
Hygrophoraceae
4,5,6,8
Hygrocybe viridis Capelari & Maziero *
Hygrophoraceae
3
Hygrocybe sp. 1, sp. 2, sp. 3
Hygrophoraceae
7
Hypholoma puiggarii (Speg.) Raithelh.
Strophariaceae
5
Hypholoma subviride (Berk. & Curt.) Dennis
Strophariaceae
6,7
Hypholoma sp. 1
Strophariaceae
10
Hygrocybe viridis (G. Stev.) A.M.
Hygrophoraceae
3
Laccaria fraterna (Cooke & Mass.) Pegler
Hydnangiaceae
Laccaria laccata (Scop.) Cooke
Hydnangiaceae
Lactocollybia aurantiaca Singer
Marasmiaceae
Lactocollybia sp. 1
Marasmiaceae
Lentinus crinitus (L.) Fr.
Polyporaceae
4
Lentinus velutinus Fr.
Polyporaceae
4,9,10
Lepiota clypeolaria sensu Rea
Agaricaceae
1,3,6
7
4
7
5
7
5
3,4,5,8
11
5
6
5
4,7
3
9
5,9
7
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Lepiota cf. citrophylla (Berk. & Broome) Sacc
Agaricaceae
5
Lepiota hypholoma Rick
Agaricaceae
9
Lepiota lilacea Bres.*
Agaricaceae
9
Lepiota parvannulata (Lasch. ex Fr.) Gill.
Agaricaceae
3,4,9,10
Lepiota pseudoignicolor Dennis
Agaricaceae
5,10
Lepiota serena (Fr.) Sacc.*
Agaricaceae
4,5,6,7,9
Lepiota sp. 1
Agaricaceae
10
Lepiota sp 2, sp. 3, sp. 4
Agaricaceae
9
Lepiota sp. 5, sp. 6
Agaricaceae
8
Lepiota sp. 7
Agaricaceae
7
Lepiota sp. 8
Agaricaceae
5
Lepiota sp. 9
Agaricaceae
4
Lepiota sp. 10
Agaricaceae
Lepista glabella (Speg.) Sing.
Tricholomataceae
Leucoagaricus americanus (Peck) Vellinga*
Agaricaceae
1,4,7
Leucoagaricus lilaceus Singer
Agaricaceae
3,9
Leucoagaricus rubrotinctus (Peck) Singer
Agaricaceae
8
Leucoagaricus sp. 1
Agaricaceae
8
Leucoagaricus sp. 2
Agaricaceae
7
Leucocoprinus cepistipes (Sow. ex Fr.) Pat.
Agaricaceae
5
Leucocoprinus birnbaumii (Corda) Singer
Agaricaceae
9
Leucocoprinus fragilissimus (Rav.) Pat.
Agaricaceae
5
Leucocoprinus sp. 1
Agaricaceae
Leucopaxillus brasiliensis (Rick) Sing.&Smith
Tricholomataceae
Leucopaxillus sp. 1
Tricholomataceae
Marasmiellus coilobasis (Berk.) Singer
Marasmiaceae
10
Marasmiellus defibulatus Sing
Marasmiaceae
3,10
Marasmiellus eburneus (Theissen) Singer
Marasmiaceae
3,5,7,10
Marasmiellus inconspicuus Murr.
Marasmiaceae
4,7
Marasmiellus juniperinus Murr.
Marasmiaceae
5,6,7,8,9
Marasmiellus picipes (Murr.) Singer
Marasmiaceae
8
Marasmiellus purpureus (Berk. & Curt.) Murr.
Marasmiaceae
4,8,9
Marasmiellus pygmaeus (Rick) Sing.
Marasmiaceae
4,6,8,9
1
1
4
9
12
8
2
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Marasmiellus subpumilus (Rick) Sing.
Marasmiaceae
Marasmiellus sp. 1
Marasmiaceae
8
Marasmiellus sp. 2
Marasmiaceae
7
Marasmiellus sp. 3
Marasmiaceae
3
Marasmiellus sp. 4
Marasmiaceae
9
Marasmius asemiformis Singer*
Marasmiaceae
4
Marasmius berteroi (Lév.) Murr.
Marasmiaceae
Marasmius cladophyllus Berk.
Marasmiaceae
Marasmius cohortalis Berk.
Marasmiaceae
7,8,9
Marasmius echinatulus Singer
Marasmiaceae
8,9
Marasmius ferrugineus (Berk.) Berk. & Curt.
Marasmiaceae
7,8
3,8,9,10
Marasmius haematocephalus (Mont.)
Marasmiaceae
8
1,2
Marasmius leoninus Berkeley
Marasmiaceae
5,10
Marasmius puttemansii Henn.*
Marasmiaceae
5
Marasmius rhabarbarinus Berk.*
Marasmiaceae
6
Marasmius rotalis Berk. & Br. **
Marasmiaceae
3,5,9
Marasmius rubroflavus (Theissen) Singer
Marasmiaceae
4
Marasmius similis Berk. & Curt.
Marasmiaceae
4
Marasmius sp. 1, sp. 2, sp. 4
Marasmiaceae
Marasmius sp. 3
Marasmiaceae
Marasmius sp. 5
Marasmiaceae
Marasmius sp. 6
Marasmiaceae
Marasmius sp. 7
Marasmiaceae
Marasmius sp. 8
Marasmiaceae
Marasmius sp. 9, sp. 10
Marasmiaceae
Marasmius sp. 11, sp. 12, sp. 13
Marasmiaceae
5
Marasmius sp. 14, sp. 15
Marasmiaceae
3
Marasmius sp. 16
Marasmiaceae
2
Marasmius sp. 17, sp. 18, sp.19, sp.20
Marasmiaceae
1
Melanoleuca spegazzinii (Sacc. & Sacc.) Sing.
Tricholomataceae
1
Melanotus alpiniae (Berk.) Pilát
Strophariaceae
8
Melanotus sp. 1
Strophariaceae
7
Micromphale sp. 1
Marasmiaceae
7
13
9
3,6,7
1
3,5,6,7,8,9
10
10
9
9
8
7
6
4
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Mycena alcalina Fr.
Mycenaceae
3,4,6,8,9,10
Mycena basibardis Rick
Mycenaceae
6,8,10
Mycena citrinella Pers.
Mycenaceae
4,5,6
Mycena dissiliens (Fr.) Quél.
Mycenaceae
5,9
Mycena epipterygia (Scop.) Gray **
Mycenaceae
Mycena leptocephala (Fr.) Gill.
Mycenaceae
3,4,5,8
Mycena nivea Quél.
Mycenaceae
9
Mycena pura (Pers.: Fr.) Quél.
Mycenaceae
3,5,7,8,9,10
Mycena sp. 1, sp. 2, sp. 3
Mycenaceae
10
Mycena sp. 4
Mycenaceae
9
Mycena sp. 5
Mycenaceae
8
Mycena sp. 6, sp. 7
Mycenaceae
7
Mycena sp. 8, sp. 9, sp. 10
Mycenaceae
6
Mycena sp. 11, sp. 12
Mycenaceae
5
Mycena sp. 13
Mycenaceae
4
Mycena sp. 14
Mycenaceae
Mycobonia flava
Polyporaceae
Neoclitocybe byssiseda (Bres.) Sing.
Tricholomataceae
10
Neoclitocybe sp. 1
Tricholomataceae
10
Neoclitocybe sp. 2
Tricholomataceae
9
Neoclitocybe sp. 3
Tricholomataceae
8
Neoclitocybe sp. 4
Tricholomataceae
5
Neoclitocybe sp. 5
Tricholomataceae
6
Neopaxillus echinospermus (Speg.) Singer
Serpulaceae
7,8
Nolanea pinna (Romagn.) Dennis
Entolomataceae
6,10
Oudemansiella platensis (Speg.) Speg.
Physalacriaceae
2,5,8,9,10
Oudemansiella steffenii (Rick) Sing.
Physalacriaceae
Oudemansiella sp. 1
Physalacriaceae
2
Pholiota sp. 1
Strophariaceae
10
Pholiota sp. 2
Strophariaceae
Pholiota sp. 3
Strophariaceae
Pholiota sp. 4
Strophariaceae
Pholiota sp. 5
Strophariaceae
5
4
2
4,6,7,10
14
10
4,5,7,8,9
8
3
3,5
1,2,3,5,8,9
2,4
9
6
5
2
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Pleurocollybia apoda Singer
Tricholomataceae
5
Pleurotus djamor (Fr.) Boedijn
Pleurotaceae
Pleurotus ostreatus (Jacq. ex Fr.) P. Kummer
Pleurotaceae
Pleurotus sp. 1
Pleurotaceae
Pleurotus sp. 2
Pleurotaceae
Pluteus cervinus (Schaeff.: Fr.) Fr.
Pluteaceae
Pluteus glaucotinctus Horak
Pluteaceae
2
Pluteus iguazuensis Singer
Pluteaceae
6
Pluteus jamaicensis Murr.*
Pluteaceae
Pluteus pulverulentus Murr.*
Pluteaceae
Pluteus viscidulus Singer
Pluteaceae
Pluteus sp. 1
Pluteaceae
10
Pluteus sp. 2, sp. 3
Pluteaceae
9
Pluteus sp.4
Pluteaceae
8
Pluteus sp. 5
Pluteaceae
7
Pluteus sp. 6
Pluteaceae
4
Polyporus alveolares (DC.) Bond. & Sing.
Polyporaceae
10
Polyporus biskeletalis Corner*
Polyporaceae
10
Polyporus ciliatus Fr. ex Fr.
Polyporaceae
Polyporus guianensis Mont.
Polyporaceae
10
Polyporus tenuiculus (P. Beauv.) Fr.
Polyporaceae
5,10
Polyporus tricholoma Mont.
Polyporaceae
Polyporus sp.1
Polyporaceae
Polyporus sp. 2
Polyporaceae
Polyporus sp. 3
Polyporaceae
Psathyrella candolleana (Fr.) A. H. Smith
Psathyrellaceae
Psathyrella coprinoceps (Berk &Curt.) Dennis
Psathyrellaceae
Psathyrella lignatilis Sing. *
Psathyrellaceae
Psathyrella sp. 1
Psathyrellaceae
6
Psathyrella sp. 2
Psathyrellaceae
3
Resupinatus subrhacodium Sing.
Tricholomataceae
Schizophyllum sp. 1
Schizophyllaceae
2
Stropharia sp. 1
Strophariaceae
9
9
5,7
4
9
3
4
4,9,10
4,8
2
4
4,7
4,6,7,8,9
5
8
8
7
2
15
5,7
6,8
5
5
2
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Tetrapyrgos nigripes (Fr.) E. Horak
Marasmiaceae
2,3,5,6
Tricholoma sulphureum (Bull.) P. Kumm.
Tricholomataceae
8
Tricholoma sp. 1
Tricholomataceae
7
Tricholoma sp. 2
Tricholomataceae
3
Trogia cantharelloides (Sacc.) Singer
Marasmiaceae
Xeromphalina tenuipes (Schwein.) A.H. Sm.
Mycenaceae
1,6,10
2,4
2,4,5,7,9,10
Source: Authors (2022).
4. Discussion
The predominance of individuals of the Marasmiaceae in the Brazilian Pampa was expected, since specimens of this
family are found in different studies on fungi for Brazil. Coimbra (2013) analyzed the diversity of Agaricales fungi in the
Atlantic Forest area of Pernambuco and verified the presence of 17 species, 36% of which belonged to the Marasmiaceae
family. Drechsler-Santos et al. (2007), in studies in native forest areas of Rio Grande do Sul, analyzed the presence of 22
agaricoid specimens, of which about 40% belong to the Marasmiaceae. Souza & Aguiar (2004), in collections in the
Amazonian Forest, verified the presence of 49 species of Agaricales fungi, most of them individuals of the Marasmiaceae, at
that time considered members of the Tricholomataceae.
In the studies presented here, the organisms of the represented about 30% of the cataloged species, a lower number
than other works, but it is still the family with the highest incidence. There are species that are characterized by their greater
resistance to drier environments, since they show reactivation, the ability to stop their growth in times of drought and grow
again later when the environment presents a certain humidity (Singer 1986). This character may explain the high rate of
species of this family in studies on taxonomy and diversity.
In MUFAM and MSH, the family with the highest occurrence was Agaricaceae, family that has a considerable rate of
specimens in the Brazilian mycota, with 85 genera and about 1340 species distributed throughout the world (Kirk et al., 2008).
This family is characterized by hosting a variety of edible individuals, including some species of the genus Agaricus, popularly
known as champignons (Wartchow, 2018). Rosa & Capelari (2009) identified 109 species of agaricoids from the Atlantic
Forest in Minas Gerais, of which 41.3% belong to the Agaricaceae. Filho (2017) collected Agaricales fungi in fragments of the
seasonal deciduous forest of Paraná and also identified a high rate belonging to the Agaricaceae family. The family is so
common in surveys that some authors prefer to work only with this family. For example, a list was published with descriptions
of edible species of the Agaricaceae family found in a natural regeneration area in Rio Grande do Sul, southern Brazil (Putzke
& Putzke 2014). Wartchow et al. (2008), Rother & Silveira (2008) and Albuquerque et al. (2010) carried out taxonomic studies
with this family in Pernambuco, Rio Grande do Sul and Rio de Janeiro, respectively.
The Agaricaceae has a worldwide distribution, with a range of representatives in tropical and temperate regions, as
well as in arctic-alpine and desert areas. However, the diversity of individuals in the family has a certain disparity in the
occurrence from one region to another (Vellinga 2004), which requires more studies on the specimens of this family found in
the Brazilian biomes, to elucidate more information on ecology and diversity of this family in the area.
The Southeast, Northeast and South regions of Brazil lead numbers of research on Agaricales in Brazil, on the other
hand, the North and Midwest regions have a reduced number of research on this group of fungi (Carvalho et al., 2022).
Agaricales studies for the Cerrado are rare, highlighting some works at specific level. Calaça et al. (2020) presented the first
16
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records of the genus Agrocybe for the Cerrado biome, represented by the species A. pediades (Fr.) Fayod, found in cattle
manure in the state of Goiás, central Brazil.
Bononi et al. (2017) reported 18 species of basidiomycete fungi not yet cited or listed nationally and 36 species with
first citation for the state in the central region of the state of Mato Grosso do Sul (MS), in the Cerrado biome, Braga & Prado
(2020) in a review study of species of the Cerrado biome, verified research with reports of new discoveries especially in the
states of Goiás, Minas Gerais, Mato Grosso and Mato Grosso do Sul. Some of the findings showed possible biotechnological
properties of the isolates found, indicating the need for actions aimed not only at the conservation of the biome, but also more
bioprospective research. This reinforces the importance of fungal conservation and the concentration of mycologists in
studying the Cerrado.
The most common genera of fungi recorded in this research were Marasmius (40 species), Mycena (27 species),
Lepiota (26 species), Collybia (17 species), Marasmiellus (14 species) and Pluteus (14 species). The genus Marasmius, the
largest number of species in this study, is one of the most diverse of the Agaricales and plays a fundamental ecological role in
the tropical regions, given its potential to litter decomposition (Antonín 2007).
In addition, specimens of Agaricus, Cantharellus, Flammulina, Gymnopilus, Macrolepiota, Oudemansiella and
Pleurotus, known for their edibility, were also identified in the study areas, highlighting the possible biotechnological
application and cultivation of the mycota found in the three biomes studied.
Among the collected species, ca. 50% were identified only to the genus level, which requires further studies to
confirm new occurrences or the registration of new species to science. Furthermore, from the list, 10% represents new
confirmed occurrences for the state of Rio Grande do Sul or Brazil and 99% are cited for the first time for the Pampa biome.
5. Conclusion or Final Considerations
The high number of species mentioned for the first time for the Pampa and Cerrado biomes, mainly, can be explained
because there are only a few studies on the Agaricales fungi in these regions of Brazil. Also, areas with a reasonable number of
studies, such as the Amazon biome, presented new occurrences not yet reported to science, showing the need for current
studies on Agarics in these areas. Therefore, due to the high number of specimens collected in this work, there are indications
that the biomes may have a greater diversity of Agaricales fungi, which requires further studies to estimate the richness and
diversity of these organisms in the areas. This corroborates the idea that small areas can resume a great fungal diversity,
deserving preservation at any coasts.
Acknowledgments
We thank professor Isa Morais, curator of the Jose Angelo Rizzo Herbarium of the State University of Goiás Campus Sudoeste for the infrastructure provided for the sorting of the mushrooms in the Bosque Auguste Saint Hilaire
preservation area. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior –
Brasil (CAPES) – Finance Code 001.
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