Agaricales Fungi from atlantic rain forest fragments in Minas Gerais, Brazil

Rosa, Luiz Henrique; Capelari, Marina

doi:10.1590/S1517-83822009000400015

Abstract

Two Atlantic Rain Forest fragments in Minas Gerais state were studied to access their Agaricales fungal richness. A total of 187 specimens were collected and 109 species, 39 genera, and eight families were identified. Thirty-three species were cited for the first time in Brazil.

Basidiomycota; biodiversity; Brazilian ecosystems; threatened environment

ENVIRONMENTAL MICROBIOLOGY

Agaricales Fungi from atlantic rain forest fragments in Minas Gerais, Brazil

Luiz Henrique Rosa^I,^* * Corresponding Author. Mailing address: Laboratório de Microbiologia, Departamento de Ciências Biológicas ICEB/UFOP. Rua Diogo Vasconcelos 122, Campus Cruzeiro, 35400-000, Ouro Preto, MG, Brazil.; E-mail: lhrosa@ufop.br ; Marina Capelari^II

^ILaboratório de Microbiologia, Departamento de Ciências Biológicas, Universidade Federal de Ouro Preto, Ouro Preto, MG, Brasil

^IISeção de Micologia e Liquenologia, Instituto de Botânica, São Paulo, SP, Brasil

ABSTRACT

Two Atlantic Rain Forest fragments in Minas Gerais state were studied to access their Agaricales fungal richness. A total of 187 specimens were collected and 109 species, 39 genera, and eight families were identified. Thirty-three species were cited for the first time in Brazil.

Key words:Basidiomycota, biodiversity, Brazilian ecosystems, threatened environment

Agaricales (Basidiomycota), the gill fungi, can live in all different terrestrial ecosystems of the world and decay organic matter. The order includes saprotrophic, mycorrhizal, and pathogenic fungi that occur in various shapes, sizes, and colors. According to Hawksworth (7), there has been some, but not enough, progress in the exploration of fungi in tropical forests; the Basidiomycota of Brazilian ecosystems are poorly known, especially those of the order Agaricales. Furthermore, the mycobiota of some ecosystems of Minas Gerais state and other Brazilian regions have never been explored.

The Agaricales, clade euagarics of Hibbett & Thorn (8), is the most diverse order in the phylum Basidiomycota, with approximately 9,387 species, 347 genus and 26 families (10). They are a critical component of the degradation of organic matter, providing habitat and food for many organisms such as bacteria, other fungi, insects, and mammals. In addition, this group has received special attention from researchers in the last years due to their potential use in biotechnology (31) as a source of several metabolites with antimicrobial, cytotoxic, immunemodulator, and antiparasitic activities (3, 22, 23, 24), and as a food source that is rich in vitamins, protein, and enzymes (11).

The first records on the Agaricales from Minas Gerais state were published by Berkeley (1), Montagne (13), and Berkeley & Cooke (2). Pegler (15, 16) reviewed the Brazilian species published by these authors listing the following taxa from Minas Gerais state: Gymnopus subpruinosus (Murril) Desjardin et al. Macrocybe praegrandis (Berk.) Pegler & Lodge, Xeromphalina tenuipes (Schwein.) A.H. Sm., Marasmiellus tricolor (Alb. & Schwein.) Singer; Marasmius ferrugineus (Berk.) Berk., M. weddellianus Mont., Trogia cantharelloides (Mont.) Pat., and Hohenbuehelia petaloides (Bull.) Schulzer. Two species of Mycena are dubious: M. asterocephala (Mont.) Sacc., which, according to Pegler (16), probably belongs to Mycena section Ianthinae, closely allied to M. pura (Pers.) Kummer; and M. atropurpurea (Mont.) Sacc.

The aim of this paper is to present a list of species of Agaricales collected in two fragments of the Atlantic Rain Forest from Minas Gerais state and to contribute to the knowledge of the mycota in tropical Brazilian ecosystems.

Basidiomycetes specimens were collected in the rainy season from November-1999 to March-2000 in two areas that represent important reservoirs for biodiversity and conservation research in Minas Gerais: the Ecological Station of the Universidade Federal of Minas Gerais (EEco), located at 19°52'S and 43º58'W, and the Rio Doce State Park (PERD), located at 19°48'18''-19°29'24''S and 42°32'30''-48°28'18''W. (9).

The basidiomata were examined in the field for macroscopic characteristics such as color, shape, surface and margin of pileus; color, density and characteristics of lamellae; and size, surface and color of stipe. The specimens were air-dried at temperatures between 38 and 55°C for later examination. The dried material was rehydrated with 70% ethanol and examined in 5% KOH and Melzer's reagent. Microscopic characters (hyphal system, cystidia, basidia, and basidiospores) were observed with a light microscope (Olympus BX50). The identification was made using the pertinent literature and comparison with collections present at the State Herbarium Maria Eneyda P. Kauffmann Fidalgo (SP). The classification of families follows Singer (27). The descriptions of taxa and the key to the species are given by Rosa (21). All material was deposited at SP and BHCB herbaria (http://sciweb.nybg.org/science2/IndexHerbariorum.asp).

In this study a total of 187 specimens were identified, resulting in 109 species in 39 genera, and eight families of agaricoid fungi. Thirty-three species are new records for Brazil and 50 are new for Minas Gerais state, some of which are interesting references for the Atlantic Rain Forest. According to Pegler (16) the agaric mycota of the Atlantic Rain Forest is similar to that found in the Caribbean, other regions in tropical America, and in the Lesser Antilles. The species, number of collections, substrate, national references, and locality are presented in Table 1.

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The families in order of the highest number of species were Agaricaceae (41.3%) and Tricholomataceae (36.7%), followed by Pluteaceae (6.4%), Coprinaceae (5.5%), Entolomataceae (4.6%), Cortinariaceae (2.8%), Hygrophoraceae (1.8%), and Crepidotaceae (0.95%). In the family Agaricaceae, Lepiota was the genus with the largest number of species collected [with 14 specimens], followed by Agaricus [11], Leucocoprinus [10], Leucoagaricus [6],Macrolepiota [3], and Rugosospora [1].

Agaricus sp. 1 was the taxon with the highest number of collections [14] and it is possibly a new species, although more investigation is needed to name it. Leucocoprinus needs further study, especially considering that five species remained unidentified in this work. According to molecular studies, which are very important tools in elucidating relationships among species within this genus (29, 30), Leucoagaricus forms a monophyletic clade. Members of the Agaricaceae are distributed worldwide with many representatives in tropical and temperate regions, and a few species in artic-alpine areas and in deserts. However, the number of taxa and the species composition differ considerably by region (30).

In the family Tricholomataceae, 16 of the collected species belong to Marasmius, and 13 collections of Lactocollybia epia were found. Marasmius is important in decaying leaves and twigs in the litter of forests. Marasmius represent approximately 500 species and frequently found in tropical regions (5, 10) with ca. 115 species mentioned for Brazil (6, 16, 18, 19), excluding the new citations presented herein. The most common species in this genus was M. leoninus, which was described from Amazonas state (2) and is also known from the states of Rio Grande do Sul (26), São Paulo (16), and Paraná (12). L. epia has been reported in Pernambuco (25, 4), São Paulo (16), and Paraná (12).

Tricholomataceae sensu Singer (27) is a very a diverse family of Agaricales and represents a significant component of the mycobiota of temperate and tropical areas. Several taxonomic studies have showed that Tricholomataceae and Agaricaceae are dominant in tropical forests (4, 16). Some of the most common species of Tricholomataceae collected in this work are Cyptotrama asprata, previously mentioned for Paraná state (12) and Rio Grande do Sul (28), Gymnopus neotropicus, mentioned for São Paulo state as Collybia neotropica (16, 17), and Xeromphalina tenuipes of which synonym has two types collected in Brazil, viz. Agaricus rheicolor Berk. described from Minas Gerais [= Micromphale rheicolor (Berk.) Dennis)] and A. citriceps Mont. described from Espírito santo state. This species is also known from the states of Rio Grande do Sul [Rick (20) as Collybia rheicolor (Berk.) Sacc.], São Paulo (16), and Paraná (12). The remaining families are represented by fewer species. However, this does not imply that they are infrequent in the studied areas, but only that more frequent collection trips to the sites are necessary to improve the collections.

All of the collected and identified species in this study were grouped in three classes of substrates: soil, leaves, and wood. The majority of species collected were found growing on wood and soil. Only four species were collected on dead leaves (Table 1). Knowledge of the distribution, dynamics and activities of Agaricales is crucial to understanding how can influence and modify the soil and the organic matter present in the tropical environments.

Much more extensive observation, sampling, recording, inventory taking, and analysis will be necessary to understand the ecological role of Agaricales in tropical ecosystems. The broad diversity and taxonomic spectrum exhibited by these fungi make them especially interesting for taxonomic and ecological studies as well as biotechnological screening programs. Thus, more research is required to increase our knowledge for conservation planning on Agaricales in Brazilian tropical ecosystems.

ACKNOWLEDGEMENTS

L.H. Rosa thanks CAPES, CNPq and FAPEMIG for financial support and the Instituto Estadual of Florestas of Minas Gerais (IEF/MG) for collect permission. The authors are grateful to Ms. Vagner G. Cortez, Dr. Maria A. Neves, and Dr. Bernardo E. Lechner for skillful comments on the contents and style of the manuscript.

Submitted: August 08, 2008; Returned to authors for corrections: December 05, 2008; Approved: June 28, 2009.

1. Berkeley, M.J. (1843). Notices on some Brazilian fungi; being a sequel to the contributions towards a Flora of Brazil by G. Gardner, Esq. Hooker. London J. Bot. 2, 629643.
2. Berkeley, M.J.; Cooke, M.C. (1876). The fungi of Brazil, including those collected by J.W.H. Trail, Esq., M.A., in 1874. J. Linn. Soc. Bot 15, 363398.
3. Cota, B.B.; Rosa, L.H.; Fagundes, S.E.M.; Martins-Filho, A.O.; Correa-Oliveira, R.; Romanha, A.J.; Rosa, C.A.; Zani, C.L. (2008). A pontent trypanocidal component from the fungus Lentinus strigosus inhibits trypanothione reductase and modulates PBMC proliferation. Mem. Inst. Oswaldo Cruz 103, 263270.
4. Dennis, R.W.G. (1970). Fungus flora of Venezuela and adjacent countries. Kew Bull. Add. Ser 3, 1485.
5. Desjardin, D.E.; Retnowati, A.; Horak, E. (2000). Agaricales of Indonesia. 2. A preliminary monograph of Marasmius from Java and Bali. Sydowia 52, 92193.
6. Grandi, R.P.G.; Guzmán, G.; Bononi, V.L. (1984). Adiçőes ŕs Agaricales (Basidiomycetes) do Parque Estadual das Fontes do Ipiranga, Săo Paulo, SP, Brasil. Rickia 11, 2733.
7. Hawksworth, D.L. (2004). Fungal diversity and its implications for genetic resource collections. Stud. Mycol 50, 918.
8. Hibbett, D.S.; Thorn, R.G. (2001). Basidiomycota: Homobasidiomycetes In: Esser, K., Lemke PA (eds.) The Mycota: a comprehensive treatise on fungi as experimental systems for basic and applied research Vol. 7, part B: Systematics and Evolution. Springer-Verlag, Berlin, p. 121168.
⁹
IBGE (1992). Manual técnico da vegetação brasileira. Rio de Janeiro: Fundação Instituto Brasileiro de Geografia e Estatística
10. Kirk, P.M.; Cannon, P.F.; David, J.C.; Stalpers, J.A. (2001). Ainsworth & Bisby's Dictionary of the Fungi 9th ed. Wallingford: CAB International.
11. Mattila, P.; Suonpaa, K.; Pirronen, V. (2000). Functional properties of edible mushrooms. Nutrition 16, 694696.
12. Meijer, A.A.R. (2001). Mycological work in the Brazilian state of Paraná. Nova Hedw 72, 105159.
13. Montagne, J.P.F.C. (1856). Septieme centurie de plantes cellulaires nouvelles, tant indigenes qu' exotiques. Ann. Sci. Nat. Bot 5, 333374.
14. Müller-Dombois, D.; Ellemberg, H. (1974). Aims and Methods of Vegetation Ecology John Wiley & Sons, New York, USA.
15. Pegler, D.N. (1988). Agaricales of Brazil described by M.J. Berkeley. Kew Bull 43, 453473.
16. Pegler, D.N. (1990). Agaricales of Brazil described by J.P.F.C. Montagne. Kew Bull 45, 161177.
17. Pegler, D.N. (1997). The agarics of Săo Paulo, Brazil: an account of the agaricoid fungi (Holobasidiomycetes) of Săo Paulo State, Brazil Kew: Royal Botanic Garden, London, United Kingdon.
18. Puccinelli, C.; Capelari, M. (2006). Two new species of Marasmius (Basidiomycota, Marasmiaceae) from Brazil. Mycotaxon 95, 295300.
19. Puccinelli, C.; Capelari, M. (2007). A new species of Marasmius (Basidiomycota, Marasmiaceae) and the first record of M. foliiphilus from Brazil. Crypt. Mycol 28, 263268.
20. Rick, J. (1907). Contributio ad monographiam Agaricearum et Polyporacearum brasiliensium. Broteria 6, 6592.
21. Rosa, L.H. (2002). Diversidade de fungos Agaricales (Basidiomycota) em dois fragmentos de Mata Atlântica do estado de Minas Gerais Minas Gerais, Brasil, 216p. (M.Sc. Dissertation. Instituto de Cięncias Biológicas, UFMG).
22. Rosa, L.H.; Machado, K.M.G.; Jacob, C.C.; Capelari, M.; Rosa, C.A.; Zani, C.L. (2003). Screening of Brazilian Basidiomycetes for antimicrobial activity. Mem. Inst. Oswaldo Cruz 98, 967974.
23. Rosa, L.H.; Cota, B.B.; Machado, K.M.G.; Rosa, C.A.; Zani, C.L. (2005). Antifungal compound produced by Oudemansiella canarii (Basidiomycota). World J. Microbiol. Biotechnol 21, 983987.
24. Rosa, L.H.; Souza-Fagundes, E.M.; Machado, K.M.G.; Alves, T.M.A.; Martins-Filho, A.O.; Romanha, A.J.; Oliveira, R.C.; Rosa, C.A.; Zani, C.L. (2006). Cytotoxic, immunosuppressive and trypanocidal activities of agrocybin, a polyacetylene produced by Agrocybe perfecta (Basidiomycota). World J. Microbiol. Biotechnol 22, 539545.
25. Singer, R. (1961). Fungi of northern Brazil. Publ. Inst. Micol. Univ. Recife 304, 126.
26. Singer, R. (1976). Marasmieae (Basidiomycetes Tricholomataceae). Flora Neotropica 17, 1106.
27. Singer, R. (1986). The Agaricales in Modern Taxonomy Koeltz Scientific Books, Koenigstein, Germany.
28. Sulzbacher, M.A.; Putzke, J.; Putzke, M.T.L.; Cortez, V.G. (2007). Nota sobre os fungos Agaricales (Basidiomycota) da Estaçăo Ecológica de Aracuri, Esmeralda, Rio Grande do Sul, Brasil. Biocięncias 15, 143153.
29. Vellinga, E.C. (2004a). Ecology and distribution of Lepiotaceous fungi (Agaricaceae): a review. Nova Hedw 78, 273-299.
30. Vellinga, E.C. (2004b). Genera in the family Agaricaceae: evidence from nrITS and nrLSU sequences. Mycol. Res 108, 354377.
31. Wasser, S.P.; Weis, A.L. (1999). Therapeutic effects of substances occurring in higher Basidiomycetes mushrooms: A modern perspective. Crit. Rev. Immunol 19, 6596.

*

Corresponding Author. Mailing address: Laboratório de Microbiologia, Departamento de Ciências Biológicas ICEB/UFOP. Rua Diogo Vasconcelos 122, Campus Cruzeiro, 35400-000, Ouro Preto, MG, Brazil.; E-mail:

lhrosa@ufop.br

Publication Dates

Publication in this collection
08 Oct 2009
Date of issue
Dec 2009

History

Accepted
28 June 2009
Received
08 Aug 2008

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 1. Berkeley, M.J. (1843). Notices on some Brazilian fungi; being a sequel to the contributions towards a Flora of Brazil by G. Gardner, Esq. Hooker. London J. Bot. 2, 629643.

[2] 2. Berkeley, M.J.; Cooke, M.C. (1876). The fungi of Brazil, including those collected by J.W.H. Trail, Esq., M.A., in 1874. J. Linn. Soc. Bot 15, 363398.

[3] 3. Cota, B.B.; Rosa, L.H.; Fagundes, S.E.M.; Martins-Filho, A.O.; Correa-Oliveira, R.; Romanha, A.J.; Rosa, C.A.; Zani, C.L. (2008). A pontent trypanocidal component from the fungus Lentinus strigosus inhibits trypanothione reductase and modulates PBMC proliferation. Mem. Inst. Oswaldo Cruz 103, 263270.

[4] 4. Dennis, R.W.G. (1970). Fungus flora of Venezuela and adjacent countries. Kew Bull. Add. Ser 3, 1485.

[5] 5. Desjardin, D.E.; Retnowati, A.; Horak, E. (2000). Agaricales of Indonesia. 2. A preliminary monograph of Marasmius from Java and Bali. Sydowia 52, 92193.

[6] 6. Grandi, R.P.G.; Guzmán, G.; Bononi, V.L. (1984). Adiçőes ŕs Agaricales (Basidiomycetes) do Parque Estadual das Fontes do Ipiranga, Săo Paulo, SP, Brasil. Rickia 11, 2733.

[7] 7. Hawksworth, D.L. (2004). Fungal diversity and its implications for genetic resource collections. Stud. Mycol 50, 918.

[8] 8. Hibbett, D.S.; Thorn, R.G. (2001). Basidiomycota: Homobasidiomycetes In: Esser, K., Lemke PA (eds.) The Mycota: a comprehensive treatise on fungi as experimental systems for basic and applied research Vol. 7, part B: Systematics and Evolution. Springer-Verlag, Berlin, p. 121168.

[9] ⁹
IBGE (1992). Manual técnico da vegetação brasileira. Rio de Janeiro: Fundação Instituto Brasileiro de Geografia e Estatística

[10] 10. Kirk, P.M.; Cannon, P.F.; David, J.C.; Stalpers, J.A. (2001). Ainsworth & Bisby's Dictionary of the Fungi 9th ed. Wallingford: CAB International.

[11] 11. Mattila, P.; Suonpaa, K.; Pirronen, V. (2000). Functional properties of edible mushrooms. Nutrition 16, 694696.

[12] 12. Meijer, A.A.R. (2001). Mycological work in the Brazilian state of Paraná. Nova Hedw 72, 105159.

[13] 13. Montagne, J.P.F.C. (1856). Septieme centurie de plantes cellulaires nouvelles, tant indigenes qu' exotiques. Ann. Sci. Nat. Bot 5, 333374.

[14] 14. Müller-Dombois, D.; Ellemberg, H. (1974). Aims and Methods of Vegetation Ecology John Wiley & Sons, New York, USA.

[15] 15. Pegler, D.N. (1988). Agaricales of Brazil described by M.J. Berkeley. Kew Bull 43, 453473.

[16] 16. Pegler, D.N. (1990). Agaricales of Brazil described by J.P.F.C. Montagne. Kew Bull 45, 161177.

[17] 17. Pegler, D.N. (1997). The agarics of Săo Paulo, Brazil: an account of the agaricoid fungi (Holobasidiomycetes) of Săo Paulo State, Brazil Kew: Royal Botanic Garden, London, United Kingdon.

[18] 18. Puccinelli, C.; Capelari, M. (2006). Two new species of Marasmius (Basidiomycota, Marasmiaceae) from Brazil. Mycotaxon 95, 295300.

[19] 19. Puccinelli, C.; Capelari, M. (2007). A new species of Marasmius (Basidiomycota, Marasmiaceae) and the first record of M. foliiphilus from Brazil. Crypt. Mycol 28, 263268.

[20] 20. Rick, J. (1907). Contributio ad monographiam Agaricearum et Polyporacearum brasiliensium. Broteria 6, 6592.

[21] 21. Rosa, L.H. (2002). Diversidade de fungos Agaricales (Basidiomycota) em dois fragmentos de Mata Atlântica do estado de Minas Gerais Minas Gerais, Brasil, 216p. (M.Sc. Dissertation. Instituto de Cięncias Biológicas, UFMG).

[22] 22. Rosa, L.H.; Machado, K.M.G.; Jacob, C.C.; Capelari, M.; Rosa, C.A.; Zani, C.L. (2003). Screening of Brazilian Basidiomycetes for antimicrobial activity. Mem. Inst. Oswaldo Cruz 98, 967974.

[23] 23. Rosa, L.H.; Cota, B.B.; Machado, K.M.G.; Rosa, C.A.; Zani, C.L. (2005). Antifungal compound produced by Oudemansiella canarii (Basidiomycota). World J. Microbiol. Biotechnol 21, 983987.

[24] 24. Rosa, L.H.; Souza-Fagundes, E.M.; Machado, K.M.G.; Alves, T.M.A.; Martins-Filho, A.O.; Romanha, A.J.; Oliveira, R.C.; Rosa, C.A.; Zani, C.L. (2006). Cytotoxic, immunosuppressive and trypanocidal activities of agrocybin, a polyacetylene produced by Agrocybe perfecta (Basidiomycota). World J. Microbiol. Biotechnol 22, 539545.

[25] 25. Singer, R. (1961). Fungi of northern Brazil. Publ. Inst. Micol. Univ. Recife 304, 126.

[26] 26. Singer, R. (1976). Marasmieae (Basidiomycetes Tricholomataceae). Flora Neotropica 17, 1106.

[27] 27. Singer, R. (1986). The Agaricales in Modern Taxonomy Koeltz Scientific Books, Koenigstein, Germany.

[28] 28. Sulzbacher, M.A.; Putzke, J.; Putzke, M.T.L.; Cortez, V.G. (2007). Nota sobre os fungos Agaricales (Basidiomycota) da Estaçăo Ecológica de Aracuri, Esmeralda, Rio Grande do Sul, Brasil. Biocięncias 15, 143153.

[29] 29. Vellinga, E.C. (2004a). Ecology and distribution of Lepiotaceous fungi (Agaricaceae): a review. Nova Hedw 78, 273-299.

[30] 30. Vellinga, E.C. (2004b). Genera in the family Agaricaceae: evidence from nrITS and nrLSU sequences. Mycol. Res 108, 354377.

[31] 31. Wasser, S.P.; Weis, A.L. (1999). Therapeutic effects of substances occurring in higher Basidiomycetes mushrooms: A modern perspective. Crit. Rev. Immunol 19, 6596.