Abstract

Corticioid and poroid fungi are traditional morphological groups composed of ligninolytic species. Due to their efficiency in wood decomposition process, many species have great ecological importance, especially in nutrient cycling, as well as for their biotechnological properties. Nevertheless, knowledge about these fungi is scarce in many phytogeographic regions of Brazil, as is the case of the Cerrado, since mycodiversity studies in this biome are mainly focused on areas of the São Paulo state. Here we present the taxonomic inventory of corticioid and poroid fungi from the Reserva Ecológica da Universidade Estadual de Goiás (REC-UEG), a Cerrado remnant in Anápolis, Goiás, Brazil. The area is covered by three typical Cerrado landscapes (cerrado stricto sensu, mesophilic forest, and gallery forest), widely explored for scientific and educational purposes by the academic and regional community which seeks to learn about and preserve its biodiversity. Exsiccates deposited in the fungarium of the Universidade Estadual de Goiás (HUEG-Fungi) were analyzed. They are the result of collections made over 20 years, in approximately 103 ha of the reserve. Samples were characterized macro and microscopically and identified based on specialized literature. 51 species were recognized, which are distributed in 33 genera, 15 families, and five orders. Species were most frequent in forested areas and among them, six are new occurrence records for the Cerrado, nine for the Midwest region, and nine for the Goiás state. These results contribute to increase the knowledge of these fungi in the Cerrado, as well as geographic distribution, and show the relevance of preserving the reserve for the regional Funga representativity.

Keywords
Hymenochaetaceae; inventory; macrofungi; Polyporaceae; wood decayers

Resumo

Fungos corticioides e poroides são assim agrupados com base em aspectos morfológicos e compostos por espécies essencialmente lignícolas. Por sua eficiência no processo de decomposição da madeira, muitas espécies desses grupos apresentam grande importância ecológica, especialmente na ciclagem de nutrientes, além de propriedades para aplicações biotecnológicas. Entretanto, o conhecimento sobre esses fungos é escasso em algumas regiões fitogeográficas do Brasil, como é o caso do Cerrado, uma vez que os estudos da micodiversidade no bioma estão focados principalmente em áreas do estado de São Paulo. Portanto, aqui apresentamos o inventário taxonômico de fungos corticioides e poroides da Reserva Ecológica da Universidade Estadual de Goiás (REC-UEG), um remanescente de Cerrado no município de Anápolis, Goiás, Brasil. A área é formada por três fitofisionomias típicas do Cerrado (cerrado stricto sensu, mata mesófila e mata de galeria) e é amplamente explorada para fins científicos e educacionais pela comunidade acadêmica regional, que buscam conhecer e preservar sua biodiversidade. Foram analisadas exsicatas depositadas no fungário da Universidade Estadual de Goiás (HUEG-Fungos), cujo acervo é fruto de coletas realizadas ao longo de 20 anos nos cerca de 103 hectares da reserva. As amostras foram caracterizadas macro e microscopicamente e identificadas com base na literatura especializada. Foram reconhecidas 51 espécies, distribuídas em 33 gêneros, 15 famílias e cinco ordens. As espécies são mais frequentes em áreas de mata na reserva e entre elas seis configuram novos registros de ocorrência para o Cerrado, nove para região Centro-Oeste e nove para o estado de Goiás. Desse modo, esses resultados contribuem para ampliar o conhecimento desses fungos no Cerrado, assim como da distribuição geográfica das espécies, além de mostrar a importância da preservação da reserva para a representatividade da Funga regional.

Palavras-chave
Hymenochaetaceae; inventário; macrofungos; Polyporaceae; decompositores de madeira

Introduction

Brazil is a forest country, with approximately 58% of its territory covered by natural and planted forests (SNIF 2016SNIF. 2016. Sistema nacional de informações florestais. Serviço florestal brasileiro, Brasília.). It is known that the large availability of woody resources in tropical forests promotes the presence of several species of macrofungi, as they are predominantly lignocellulolytic organisms (Zmitrovich et al. 2015ZMITROVICH, I.V., EZHOV, O.N. & WASSER, S.P. 2012. A survey of species of genus Trametes Fr. (higher Basidiomycetes) with estimation of their medicinal source potential. International Journal of Medicinal Mushrooms 14(3):307–319., Medeiros et al. 2015MEDEIROS, P.S., CATTANIO, J.H. & SOTÃO, M.P. 2015. Riqueza e relação dos fungos poroides lignolíticos (Agaricomycetes) com o substrato em floresta da Amazônia brasileira. Boletim do Museu Paraense Emílio Goeldi - Ciências Naturais 10(3):423–436.).

Fungi that are associated with this substrate at some stage in their life cycle are named “wood-inhabiting fungi”. The main diversity of wood-inhabiting fungi is represented by some groups of Basidiomycota (Zmitrovich et al. 2015ZMITROVICH, I.V., WASSER, S.P. & TURA, D. 2015. Wood-inhabiting fungi. In fungi from different substrates (J. K. Misra, J. P. Tewari, S. K. Deshmukh, C. V, & Ágvölgyi, eds) CRC press, p.17–74.). The decomposition of woody substrates by these fungi is possible due to enzyme production that degrades the constituents of wood (Lundell et al. 2010LUNDELL, T.K., MÄKELÄ, M.R. & HILDÉN, K. 2010. Lignin-modifying enzymes in filamentous basidiomycetes - ecological, functional and phylogenetic review. Journal of Basic Microbiology 50(1):5–20.). For this reason, some species have been used in biotechnological processes to obtain new sources of bioproducts and in bioremediation activity (Salvachúa et al. 2013SALVACHÚA, D., PRIETO, A., MARTÍNEZ, Á.T. & MARTÍNEZ, M.J. 2013. Characterization of a novel dye-decolorizing peroxidase (DyP)-type enzyme from Irpex lacteus and its application in enzymatic hydrolysis of wheat straw. Applied and Environmental Microbiology 79(14):4316–4324., Olicón-Hernández et al. 2017OLICÓN-HERNÁNDEZ, D.R., GONZÁLEZ-LÓPEZ, J. & ARANDA, E. 2017. Overview on the biochemical potential of filamentous fungi to degrade pharmaceutical compounds. Frontiers in Microbiology 8:1–17., Grassi et al. 2018GRASSI, E., ROBLEDO, G. & LEVIN, L. 2018. Influence of light on lignin-degrading activities of fungal genus Polyporus s. str. Journal of Basic Microbiology 58(11):947–956., Wehaidy et al. 2018WEHAIDY, H., EL-HENNAWI, H., AHMED, S. & ABDEL-NABY, M. 2018. Comparative study on crude and partially purified laccase from Polyporus durus ATCC 26726 in the decolorization of textile dyes and wastewater treatment. Egyptian Pharmaceutical Journal 17(2):94.).

Within the phylum Basidiomycota, several groups are traditionally defined according to morphological criteria and life habits (Ghobad-Nejhad 2011GHOBAD-NEJHAD, M. 2011. Updated checklist of corticioid and poroid basidiomycetes of the Caucasus region. Mycotaxon 117(1): 508.). Among these are the corticioid and poroid fungi, which are characterized by annual or perennial, resupinate to stipitate basidiomata and exposed hymenium. The resupinated habit (usually) is characteristic of corticioid fungi, while the presence of pores (and variants) on the hymenium is found in poroid fungi (Ryvarden 2004RYVARDEN, L. 2001. The genus Auriscalpium. Harvard Papers in Botany 6(1):193–198., Larsson 2007LARSSON, K.-H. 2007. Re-thinking the classification of corticioid fungi. Mycological Research 111(9):1040–1063.). They have worldwide distribution (He et al. 2019HE, M.Q. et al. 2019. Notes, outline and divergence times of Basidiomycota. Fungal Diversity 99(1):105–367.) and in Brazil, they occur in all six biomes (Maia et al. 2015MAIA, L.C. et al. 2015. Diversity of Brazilian fungi. Rodriguesia 66(4):1033–1045.). Most of these occurrence records come from long-term surveys, inventories, research made in important remnants of these biomes, or environmental protection areas (conservation units) (Bononi 1984BONONI, V.L. 1984. Basidiomicetos do Cerrado da Reserva Biológica de Moji-Guaçu, SP. Rickia1 11:1–25., Bononi et al. 2008BONONI, V.L.R., OLIVEIRA, A.K.M., QUEVEDO, J.R. & GUGLIOTTA, A.M. 2008. Fungos macroscópicos do Pantanal do Rio Negro, Mato Grosso do Sul, Brasil. Hoehnea 35(4):489–511., Drechsler-Santos et al. 2013DRECHSLER-SANTOS, E.R., RYVARDEN, L., BEZERRA, J.L., GIBERTONI, T.B., SALVADOR-MONTOYA, C.A. & CALVACANTI, M.A.Q. 2013. New records of Auriculariales, Hymenochaetales and Polyporales (Fungi: Agaricomycetes) for the Caatinga Biome. Check List 9(4):800–805., Motato-Vásquez et al. 2015MOTATO-VÁSQUEZ, V., PIRES, R.M. & GUGLIOTTA, A.M. 2015. Polypores from an Atlantic rainforest area in southeast Brazil: pileate species. Brazilian Journal of Botany 38(1):149–164., Bononi et al. 2017BONONI, V.L.R., OLIVEIRA, A.K.M., GUGLIOTTA, A.M. & QUEVEDO, J.R. 2017. Agaricomycetes (Basidiomycota, Fungi) diversity in a protected area in the Maracaju Mountains, in the Brazilian central region. Hoehnea 44(3):361–377., Xavier et al. 2018XAVIER, W.K.S., SOTÃO, H.M.P., SOARES, A.M.S., GIBERTONI, T.B., RODRIGUES, F.J. & RYVARDEN, L. 2018. Riqueza de Agaricomycetes poroides da Serra do Navio, Amazônia oriental, com novo registro de Oxyporus lacera para o Brasil. Boletim Do Museu Paraense Emílio Goeldi - Ciências Naturais 13(3):303–315.).

In the Cerrado (Brazilian savanna), one of the richest and most threatened biomes in the world (Myers et al. 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403(6772):853–858., Lahsen et al. 2016LAHSEN, M., BUSTAMANTE, M.M.C. & DALLA-NORA, E.L. 2016. Undervaluing and Overexploiting the Brazilian Cerrado at Our Peril. Environment: Science and Policy for Sustainable Development 58(6):4–15., Colli et al. 2020COLLI, G.R., VIEIRA, C.R. & DIANESE, J.C. 2020. Biodiversity and conservation of the Cerrado: recent advances and old challenges. Biodiversity and Conservation 29(5):1465–1475.), inventories of corticioid and poroid fungi started in the 1960s, mainly focused on areas in the state of São Paulo (Fidalgo et al. 1965FIDALGO, O., FIDALGO, M.E.P.K. & FURTADO, J.S. 1965. Fungi of the “Cerrado” region of São Paulo. Rickia 2:55–71.). Since that, research was conducted in other regions of the biome within the states of Goiás (Leonardo-Silva et al. 2020LEONARDO-SILVA, L., SILVA, L.B. & XAVIER-SANTOS, S. 2020. Poroid fungi (Agaricomycetes, Basidiomycota) from Floresta Nacional de Silvânia – a conservation unit of Brazilian Savanna. Microbial Biosystems 5(1):100–107.) and Mato Grosso do Sul (Bononi et al. 2017BONONI, V.L.R., OLIVEIRA, A.K.M., GUGLIOTTA, A.M. & QUEVEDO, J.R. 2017. Agaricomycetes (Basidiomycota, Fungi) diversity in a protected area in the Maracaju Mountains, in the Brazilian central region. Hoehnea 44(3):361–377.). However, the lack of species inventories in large areas leads to a significant gap in knowledge about the presence and distribution of the taxa.

Over two decades, collections have been made frequently in the Reserva Ecológica da Universidade Estadual de Goiás (REC-UEG), a remnant of Cerrado, located in Central Brazil. These samples are the result of academic-scientific activities carried out by both undergraduate and graduate students, also educational and recreational activities focused on environmental education for elementary school students. The collected species are presented in this study and compose the inventory of corticioid and poroid fungi from the REC-UEG, contributing to increase the knowledge about these fungi groups around the Cerrado and Midwest regions of Brazil.

Material and Methods

1.

Study area

The REC-UEG is located in the Campus Central-Sede da Universidade Estadual de Goiás, Anápolis, Goiás, Brazil (Figure 1). It comprises 134 ha while 103 ha is covered by the reserve. The REC-UEG is limited by the University Campus (north), the agro-industrial district of Anápolis (south), rural properties and cargo airport (east), and clothing industries (west).

The region’s weather is classified as tropical Cwb type according to Köppen-Geiger climate classification, with a dry cold season (April to September) and a rainy warm season (October to March). The average annual temperature is 25 ℃, altitude between 1000 and 1200 m (Cardoso et al. 2014CARDOSO, M.R.D., MARCUZZO, F.F.N. & BARROS, J.R. 2014. Climatic Classification of Köppen-Geiger for the State of Goias and Federal District. Acta Geográfica 8(16):40–55.). The area is composed almost entirely of savanna native vegetation (cerrado stricto sensu) and forest type (mesophilic forest or semideciduous dry forest and gallery forest) (Figure 2), which Myrtaceae, Rubiaceae, Leguminosae, and Asteraceae are the most dominant families. The cerrado stricto sensu has a shrub-arboreal vegetation characteristic of the phytophysiognomy. The mesophilic forest is observed as denser vegetation, where plant species are predominant with various levels of deciduousness in the dry season and is not associated with watercourses. The gallery forest is also composed of dense vegetation and evergreen following small rivers and stream courses (Ribeiro & Walter 2008RIBEIRO, J.F. & WALTER, B.M.T. 2008. As principais fitofisionomias do bioma Cerrado. In Cerrado: ecologia e flora (S.M. Sano, S.P. Almeida & J.F. Ribeiro, eds). Embrapa, Planaltina. p.151–212.). Lastly, a vegetation corridor is formed over the Barreiro stream inside the reserve.

Due to the strong environmental impact and reduction of native biodiversity caused by anthropic actions, in 2016 an area management plan was proposed by UEG. Thus, the reserve represents a means to preserve and conserve local biodiversity, native vegetation, springs, and waterways in the area encouraging academic-scientific activities; restoration of degraded areas, recompose native vegetation, and promote environmental education activities including both university community and the regional population.

2.

Data collection and analysis

Collections were carried out randomly between 2001 and 2021, in and around REC-UEG. All basidiomata found in wood and leaf litter were photographed and we took information, such as substrate type (living or dead wood) and environment (phytophysiognomy). Preservation and herborization of collected material followed the standard techniques for fungi (Gadelha-Neto et al. 2013GADELHA-NETO, P.C.G., BARBOSA, M.R.V., MENEZES, M., WARTCHOW, F., LIMA, J.R., BARBOSA, M.A., PÔRTO, K.C., GIBERTONI, T.B., PEIXOTO, A.L. & MAIA, L.C. 2013. Manual de procedimentos para herbários. Editora UFPE, Pernambuco, Recife.) and were deposited at the fungarium of the Universidade Estadual de Goiás (HUEG-Fungi) (Thiers 2021THIERS, B. 2021. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/.
http://sweetgum.nybg.org/science/ih/... [continuously updated]).

The dried material was identified taxonomically by macro and microscopic analysis using relevant taxonomic identification keys (Ryvarden 2001PARMASTO, E. 2001. Hymenochaetoid fungi (Basidiomycota) of North America. Mycotaxon 79:107–176., Núñez & Ryvarden 2001NÚÑEZ, M. & RYVARDEN, L. 2001. East Asian Polypores 2. Polyporaceae s. lato. Synopsis Fungorum 14:166–574., Ryvarden 2004RYVARDEN, L. 2001. The genus Auriscalpium. Harvard Papers in Botany 6(1):193–198., 2015RYVARDEN, L. 2004. Neotropical polypores Part 1. Introduction, Ganodermataceae & Hymenochaetaceae. Synopsis Fungorum 19:1–238., 2016WANG, P.M. & YANG, Z.L. 2019. Two new taxa of the Auriscalpium vulgare species complex with substrate preferences. Mycological Progress 18(5):641–652., Ţura et al. 2008ŢURA, D., ZMITROVICH, I.V., WASSER, S.P. & NEVO, E. 2008. The genus Stereum in Israel. Mycotaxon 106:109–126., Abrahão et al. 2009ABRAHÃO, M.C., GUGLIOTTA, A.M. & GOMES, E. 2009. Poliporóides (Basidiomycota) em fragmentos de mata no perímetro urbano de São José do Rio Preto, São Paulo, Brasil. Revista Brasileira de Botânica 32(3):427–440., Gomes-Silva et al. 2010GOMES-SILVA, A.C., RYVARDEN, L. & GIBERTONI, T.B. 2010. Notes on Trametes from the Brazilian Amazonia. Mycotaxon 113(1):61–71., Nogueira-Melo et al. 2012NOGUEIRA-MELO, G.S., MEDEIROS, P.S., GOMES-SILVA, A.C., RYVARDEN, L., SOTÃO, H.M.P. & GIBERTONI, T.B. 2012. Coriolopsis psila comb. nov. (Agaricomycetes) and two new Coriolopsis records for Brazil. Mycotaxon 120(1):223–230., Zmitrovich et al. 2012ZMITROVICH, I.V., EZHOV, O.N. & WASSER, S.P. 2012. A survey of species of genus Trametes Fr. (higher Basidiomycetes) with estimation of their medicinal source potential. International Journal of Medicinal Mushrooms 14(3):307–319., Gorjón 2020GORJÓN, S.P. 2020. Genera of corticioid fungi: keys, nomenclature, and taxonomy. Studies in Fungi 5(1):125–309.). For macroscopic characters, we considered the shape, consistency, texture, color, dimension, hymenophore morphology, and the number of pores per mm (in poroid species) of basidiomata. For observations and measurements of microscopic characters, freehand sections were made from dried basidiomata and mounted in 2% potassium hydroxide (KOH) and 1% phloxine (Teixeira 1995TEIXEIRA, A.R. 1995. Métodos para estudo das hifas do basidiocarpo de fungos poliporáceos. São Paulo, Instituto de Botânica, p. 22.). The hyphal system, basidia, basidiospores, and cystidia were observed in Olympus CX31 optical microscope while measurements were performed using the Piximètre software version 5.10 R 1541 (Henriot & Cheype 2017HENRIOT, A. & CHEYPE, J.L. 2017. Piximètre, la measure des dimensions sur images. http://www.piximetre.fr. (last access in 25 may 2022).
http://www.piximetre.fr... ). Melzer’s reagent and cotton blue were used to test the amyloid or dextrinoid and cyanophilic reactions of the microscopic structures, respectively. The color classification was based on Kornerup & Wansher (1978)KORNERUP, A. & WANSHER, J.H. 1978. Handbook of colour. 3 ed. Eyre Methuen, London.. Nomenclature and classification system followed Index Fungorum (http://www.indexfungorum.org) and Mycobank (https://www.mycobank.org/) databases. Global Geographical distribution was based on recent literature, and, in Brazil, we used the List of Brazilian Algae, fungi, and plants (http://floradobrasil.jbrj.gov.br).

We performed the interpolation and extrapolation curve for the data for the area. The curve was based on specimen’s abundance (Hill number q = 0; 95% confidence interval), and the extrapolation estimated for double sample size (Chao et al. 2014CHAO, A., GOTELLI, N.J., HSIEH, T.C., SANDER, E.L., MA, K.H., COLWELL, R.K. & ELLISON, A.M. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84(1):45–67.). The analysis was performed using the iNEXT package (Hsieh et al. 2016HSIEH, T.C., MA, K.H. & CHAO, A. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7(12):1451–1456.) in R software version 3.6.1 (R Core Team 2017R CORE TEAM. 2017. A language and environment for statistical computing, Version 3.6.1. R Foundation for Statistical Computing.) and RStudio environment version 1.2.1335 (RStudio Team, 2019RSTUDIO TEAM. 2019. RStudio: Integrated Development for R, Version 1.2.1335. RStudio, PBC.).

Results

We found 253 specimens, 51 species, distributed in 33 genera, 15 families, and five orders (Figure 3). Polyporales (39 species) and Hymenochaetales (6 species) were the most representative orders, comprising 88% of the total. Polyporaceae was the most frequent family (47% of occurrences; 24 species), followed by Hymenochaetaceae (10%; 5 species), Ganodermataceae (8%; 4 species), and Panaceae (6%; 3 species). Trametes was the best-represented genus (12%; 6 species) and the most common species with 10 or more occurrences are Funalia caperata, Lentinus berteroi (both with 9.5%; 24 specimens), Pycnoporus sanguineus (8%; 20 specimens), Coriolopsis floccosa, Favolus brasiliensis (both with 6%; 15 specimens), Hymenochaete rheicolor, Polyporus tricholoma (both with 4.7%; 12 specimens), and Hexagonia variegata (4.3%; 11 specimens) (Figure 3). Six of the sampled species are new occurrences for the Cerrado, nine for the Midwest region, and nine for the state of Goiás. We observed that 98% of the species occurred in forest formations, and the rarefaction and extrapolation curve suggest that sampling in the area was satisfactory, although new collections indicate an increase in diversity (Figure 4).

The list of corticioid and poroid fungi species occurring in the REC-UEG is described below. Following we provide data on substrates, occurring phytophysiognomy, and fungarium voucher of each species, as well as taxonomic remarks of those cited for the first time for the Cerrado or with nomenclatural conflicts. An asterisk (*) before the name of the species indicates that the taxon is reported for the first time for the Cerrado, two asterisks (**) Midwestern region, or three asterisks (***) Goiás state.

Agaricales

Schizophyllaceae

Gloeophyllales

Gloeophyllaceae

Hymenochaetales

Hymenochaetaceae

Incertae sedis

Polyporales

Fomitopsidaceae

Ganodermataceae

Incertae sedis

Remarks: The genus Rickiopora Westph., Tomšovský & Rajchenb. was described by Westphalen et al. (2016)WESTPHALEN, M.C., RAJCHENBERG, M., TOMŠOVSKÝ, M. & GUGLIOTTA, A.M. 2016. Extensive characterization of the new genus Rickiopora (Polyporales). Fungal Biology 120(8):1002–1009. to accommodate the species Daedalea latemarginata and Antrodiella angulatopora Ryvarden, previously considered synonymous (Rajchenberg 1987RAJCHENBERG, M. 1987. Type studies of Polyporaceae (Aphyllophorales) described by J. Rick. Nordic Journal of Botany 7(5):553–568.), in R. latemarginata. The species is characterized by pileate to effused-reflex basidiomata, rigid and curled when dried, poroid hymenophore with larger angular to irregular pores (2–4 per mm), sometimes forming daedaloid to hydnoid areas in old, dried specimens; monomitic to pseudo-dimitic hyphal system, and subglobose, hyaline, smooth, thin-walled basidiospores.

Our specimen was found only once in the collection area, even after years of sampling, growing on dead wood from an unidentified angiosperm. Currently, R. latemarginata is recorded in Argentina, Brazil, Costa Rica, and Venezuela (Rajchenberg 1987RAJCHENBERG, M. 1987. Type studies of Polyporaceae (Aphyllophorales) described by J. Rick. Nordic Journal of Botany 7(5):553–568., Ryvarden 2015RYVARDEN, L. 2015. Neotropical Polypores Part 2. Polyporaceae. Abortiporus-Nigroporus. Synopsis Fungorum 34: 232–443., Westphalen et al. 2016WESTPHALEN, M.C., RAJCHENBERG, M., TOMŠOVSKÝ, M. & GUGLIOTTA, A.M. 2016. Extensive characterization of the new genus Rickiopora (Polyporales). Fungal Biology 120(8):1002–1009.). Previously cited for Brazil in the Amazonia and Atlantic Forest biomes (Maia et al. 2015MAIA, L.C. et al. 2015. Diversity of Brazilian fungi. Rodriguesia 66(4):1033–1045., Motato-Vásquez et al. 2015MOTATO-VÁSQUEZ, V., PIRES, R.M. & GUGLIOTTA, A.M. 2015. Polypores from an Atlantic rainforest area in southeast Brazil: pileate species. Brazilian Journal of Botany 38(1):149–164.), the occurrence in the present study is the first for the Cerrado.

Irpicaceae

Meripilaceae

Meruliaceae

Remarks: Climacodon pulcherrimus is characterized by the dimidate and flattened basidioma; pilear surface light orange (5A4), finely tomentose; hymenial surface light orange (5A4) becoming reddish orange (7A8) in some parts, hydnoid, spines up to 4 mm long, 2–5 per mm; basidiospores ellipsoid, hyaline, smooth, thin-walled (4) 4.6 – 5.6 (6.7) × (1.8) 2 – 3 (3.1) µm. We found our species strongly attached to decaying wood near the stream. Interestingly, after a long herborization period, some regions of the hymenial surface show darker regions (caramelized appearance). Climacodon pulcherrimus has a cosmopolitan distribution (Bononi 1979BONONI, V.L. 1979. Basidiomicetos do Parque Estadual da Ilha do Cardoso: I. Espécies Hidnóides. Rickia 8:63–74., Moreno et al. 2007MORENO, G., BLANCO, M.N., OLARIAGA, I. & CHECA, J. 2007. Climacodon pulcherrimus a badly known tropical species, present in Europe. Cryptogamie, Mycologie 28(1):3–11.) and, in Brazil, occurs in the Amazonia and Atlantic Forest biomes (Maia et al. 2015MAIA, L.C. et al. 2015. Diversity of Brazilian fungi. Rodriguesia 66(4):1033–1045.), and is now cited for the first time for the Cerrado.

Panaceae

Phanerochaetaceae

Polyporaceae

Remarks: Polyporus dictyopus was placed in Neodictyopus Palacio, Robledo, Reck & Drechsler-Santos based on morphological and phylogenetic analyses (Palacio et al. 2017PALACIO, M., ROBLEDO, G.L., RECK, M.A., GRASSI, E., GÓES-NETO, A., & DRECHSLER-SANTOS, E.R. 2017. Decrypting the Polyporus dictyopus complex: Recovery of Atroporus Ryvarden and segregation of Neodictyopus gen. nov. (Polyporales, Basidiomyocta). Plos one 12(10): e0186183.), and recently transferred to Picipes Zmitr. & Kovalenko by Ji et al. (2022)JI, X., ZHOU, J.L., SONG, C.G., XU, T.M., WU, D.M. & CUI, B.K. 2022. Taxonomy, phylogeny and divergence times of Polyporus (Basidiomycota) and related genera. Mycosphere 13(1): 1–52.. Despite that, we will use N. dictyopus as the current name since Ji et al. (2022)JI, X., ZHOU, J.L., SONG, C.G., XU, T.M., WU, D.M. & CUI, B.K. 2022. Taxonomy, phylogeny and divergence times of Polyporus (Basidiomycota) and related genera. Mycosphere 13(1): 1–52. did not include South American specimens of the specie in their analyses.

Remarks: The genus Perenniporiella was proposed in 2003 by Decock and Ryvarden segregated from Perenniporia Murrill (Decock & Ryvarden 2003DECOCK, C. & RYVARDEN, L. 2003. Perenniporiella gen. nov. segregated from Perenniporia, including a key to neotropical Perenniporia species with pileate basidiomes. Mycological Research 107(1):93–103.). Currently, the genus has six species and P. micropora differs from the others by the thin, flexible, effused reflexed basidioma, smaller pores, circular to irregular, 8–10 per mm, and basidiospores globose, thick-walled (4.4) 4.5 – 5.6 (5.8) × (3) 3.1 – 4.4 (4.5) µm. The species has been recorded in Belize, Brazil, Costa Rica, Cuba, and Peru (Decock & Ryvarden 2003DECOCK, C. & RYVARDEN, L. 2003. Perenniporiella gen. nov. segregated from Perenniporia, including a key to neotropical Perenniporia species with pileate basidiomes. Mycological Research 107(1):93–103., Drechsler-Santos et al. 2015DRECHSLER-SANTOS, R.E., SALVADOR-MONTOYA, C.A., ALVES-SILVA, G., FERNANDES, M., RECK, M., PALACIO, M., NUNES, P., ELIAS, S.G., BATISTELLA, D.A., SMIDERLE, E.C., MACHINER, M., KORPANBARBOSA, G.C. & BARBOSA, F.R. 2015. Macrofungos: aspectos preliminares sobre a diversidade de Basidiomycota. In Biodiversidade do Parque Estadual Cristalino Áttema, Sinop, Mato Grosso, p.54–67.). In Brazil, it is cited for the Amazonia and Atlantic Forest biomes (Drechsler-Santos et al. 2015DRECHSLER-SANTOS, E.R., CAVALVANTI, M.A.Q., LOGUERCIO-LEITE, C. & ROBLEDO, G.L. 2012. On Neotropical Daedalea species: Daedalea ryvardenica sp. nov. Kurtziana 37(1):65–72., Maia et al. 2015MAIA, L.C. et al. 2015. Diversity of Brazilian fungi. Rodriguesia 66(4):1033–1045.) and the occurrence reported here is the first for the Cerrado.

Remarks: Trametes marianna is characterized by the pileate, flattened, semicircular to flabeliform basidioma; pilear surface light orange (5B4) to light brown (5D4), concentrically zoned with sulcate zones; hymenial surface greyish orange (5B3) to brownish orange (5C3), pores circular to irregular, 6–7 per mm; basidiospores cylindrical to ellipsoid, hyaline, smooth, thin-walled (6.5) 7.4 – 9.4 (10.2) × 4 – 5.1 (5.8) µm. A tropical species (Ryvarden 2016RYVARDEN, L. 2016. Neotropical polypores Part 3. Polyporaceae. Obba-Wrightoporia. Synopsis Fungorum 36: 447–613.) and, in Brazil, occurs in Amazonia and Atlantic Forest biomes (Maia et al. 2015MAIA, L.C. et al. 2015. Diversity of Brazilian fungi. Rodriguesia 66(4):1033–1045.) and is now cited for the first time for the Cerrado.

Remarks: Trametes pavonia (Hook.) Ryvarden is an illegitimate name because this binomial was already used since 1851: T. pavonia (Berk.) Fr [= T. elegans (Spreng.) Fr.]. Despite that, we have chosen to use the name since some authors have frequently used it as current. Although the focus of our paper is to explore the fungal diversity in the study area, and not to solve nomenclatural problems of specific taxa, we point out that a new name should be proposed for the species after a review of the type material.

Remarks: A dense layer of thick, matted, light orange (6A5) to reddish brown (8D4) tomentum covering the pileus and small pores (6–7 per mm) invisible to the naked eye on the hymenial surface are characteristic of the species. Trametes psila was described in 1915 by Lloyd as Fomes psila Lloyd from material collected in Brazil and, currently, it is also recorded in Mexico. In Brazil, its occurrence was known for the Amazon and Atlantic Forest biomes (Nogueira-Melo et al. 2012NOGUEIRA-MELO, G.S., MEDEIROS, P.S., GOMES-SILVA, A.C., RYVARDEN, L., SOTÃO, H.M.P. & GIBERTONI, T.B. 2012. Coriolopsis psila comb. nov. (Agaricomycetes) and two new Coriolopsis records for Brazil. Mycotaxon 120(1):223–230.), and the record of the present study is the first for the Cerrado.

Steccherinaceae

Russulales

Auriscalpiaceae

Remarks: Auriscalpium is a genus described by Gray in 1821 based on Hydnum auriscalpium L. Currently, the genus comprises 10 widely distributed species, some of which are known to grow on pinecones (Ryvarden 2001RYVARDEN, L. 2001. The genus Auriscalpium. Harvard Papers in Botany 6(1):193–198., Wang & Yang 2019WANG, P.M. & YANG, Z.L. 2019. Two new taxa of the Auriscalpium vulgare species complex with substrate preferences. Mycological Progress 18(5):641–652.). Of these, A. villipes is characterized by the central or laterally stipitate basidioma, flabelliform to reniform pileus; pilear surface greyish orange (5B4) to light bown (5D5), velutine near the union with the stipe, becoming glabrous towards the margin; hymenial surface concolor to pilear surface, hydnoid, spines up to 80 mm long, stipe cylindrical, velutine to tomentose; dimitic hyphal system and basidiospores ellipsoid, hyaline and finely ornamented (3.8) 4.1 – 4.9 (5.1) × (3) 3.3 – 3.9 (4.3) µm. It is a species of neotropical distribution (Ryvarden 2001RYVARDEN, L. 2001. The genus Auriscalpium. Harvard Papers in Botany 6(1):193–198., Wang & Yang 2019WANG, P.M. & YANG, Z.L. 2019. Two new taxa of the Auriscalpium vulgare species complex with substrate preferences. Mycological Progress 18(5):641–652.) and the only one of the genus that occurs in Brazil. The records in the country come from studies carried out in the Atlantic Forest (Gibertoni et al. 2004GIBERTONI, T.B., RYVARDEN, L. & CAVALCANTI, M.A.Q. 2004. New records of Aphyllophorales (Basidiomycota) in the Atlantic Rain Forest in Northeast Brazil. Acta Botanica Brasilica 18(4):975–979.), which is the first record for the Cerrado biome.

Stereaceae

Discussion

The corticioid and poroid Funga of the Cerrado is historically recognized as one of the less studied in the country, a result of poor sampling efforts and few trained taxonomists in the region. According to our recent studies 223 species are known in the biome and the present inventory has about 19% of these species. Furthermore, these records add 24 new species known in Goiás and rank the state as the second richest in corticioid and poroid fungi in the Cerrado, just behind the state of São Paulo.

The diversity of these fungal groups in the REC-UEG is higher in the number of families, genera, and species than those recorded by other inventories of Cerrado macrofungi that included the same taxa (Quevedo et al. 2012QUEVEDO, J.R., BONONI, V.L.R., OLIVEIRA, A.K.M. & GUGLIOTTA, A.D.M. 2012. Agaricomycetes (Basidiomycota) em um fragmento florestal urbano na cidade de Campo Grande, Mato Grosso do Sul, Brasil. Revista Brasileira de Biociências 10(4):430–438., Bononi et al. 2017BONONI, V.L.R., OLIVEIRA, A.K.M., GUGLIOTTA, A.M. & QUEVEDO, J.R. 2017. Agaricomycetes (Basidiomycota, Fungi) diversity in a protected area in the Maracaju Mountains, in the Brazilian central region. Hoehnea 44(3):361–377., Leonardo-Silva et al. 2020LEONARDO-SILVA, L., SILVA, L.B. & XAVIER-SANTOS, S. 2020. Poroid fungi (Agaricomycetes, Basidiomycota) from Floresta Nacional de Silvânia – a conservation unit of Brazilian Savanna. Microbial Biosystems 5(1):100–107.). Although the area is formed by a fragment of the biome and part of it has been deforested by anthropic actions, its species richness may be influenced by the varied vegetation found in the Cerrado physiognomic forms, especially the forest formations, and the sampling period, showing the importance of long-term studies to evidence the regional diversity.

Although there is a wide variety of wood-inhabiting corticioid and poroid fungi species, most belong to the orders Hymenochaetales and Polyporales (Kirk et al. 2008KIRK, P.M., CANNON, P.F., MINTER, D.W. & STALPERS, J.A. 2008. Dictionary of the Fungi. 10 ed. CABI, Wallingford, UK.). Both orders have species widely distributed worldwide and are known for their wood degrading ability (Lundell et al. 2010LUNDELL, T.K., MÄKELÄ, M.R. & HILDÉN, K. 2010. Lignin-modifying enzymes in filamentous basidiomycetes - ecological, functional and phylogenetic review. Journal of Basic Microbiology 50(1):5–20., He et al. 2019HE, M.Q. et al. 2019. Notes, outline and divergence times of Basidiomycota. Fungal Diversity 99(1):105–367.). These fungi obtain their energy demands by metabolizing the constituents of wood, living or dead, such as cellulose and lignin. This process is only possible due to the broad enzymatic profile of these species, evidencing the potential for biotechnological applications (Zmitrovich et al. 2015ZMITROVICH, I.V., WASSER, S.P. & TURA, D. 2015. Wood-inhabiting fungi. In fungi from different substrates (J. K. Misra, J. P. Tewari, S. K. Deshmukh, C. V, & Ágvölgyi, eds) CRC press, p.17–74., El-Gendi et al. 2022EL-GENDI, H., SALEH, A.K., BADIERAH, R., REDWAN, E.M., EL-MARADNY, Y.A. & EL-FAKHARANY, E.M. 2022. A Comprehensive Insight into Fungal Enzymes: Structure, Classification, and Their Role in Mankind’s Challenges. Journal of Fungi 8(1):23.). Currently, some genera and species found in the corticioid and poroid Funga of the REC-UEG are already considered as having potential for biotechnological processes. Trametes and Polyporus are largely used (or studied) for obtaining enzymes and degrading potential environmental pollutants (Cruz-Morató et al. 2013CRUZ-MORATÓ, C., FERRANDO-CLIMENT, L., RODRIGUEZ-MOZAZ, S., BARCELÓ, D., MARCO-URREA, E., VICENT, T. & SARRÀ, M. 2013. Degradation of pharmaceuticals in non-sterile urban wastewater by Trametes versicolor in a fluidized bed bioreactor. Water Research 47(14):5200–5210., Olicón-Hernández et al. 2017OLICÓN-HERNÁNDEZ, D.R., GONZÁLEZ-LÓPEZ, J. & ARANDA, E. 2017. Overview on the biochemical potential of filamentous fungi to degrade pharmaceutical compounds. Frontiers in Microbiology 8:1–17., Wehaidy et al. 2018WEHAIDY, H., EL-HENNAWI, H., AHMED, S. & ABDEL-NABY, M. 2018. Comparative study on crude and partially purified laccase from Polyporus durus ATCC 26726 in the decolorization of textile dyes and wastewater treatment. Egyptian Pharmaceutical Journal 17(2):94.). In addition, previous studies focusing on biotechnological aspects of some species from the reserve have shown potential results (Leonardo-Silva et al. 2018LEONARDO-SILVA, L., MOREIRA, I.C., SILVA, T.M., SILVA, L.B., SANTOS, T.A.A., OLIVEIRA, L.M., SOUZA, D.F., BRITO, A.O. & XAVIER-SANTOS, S. 2018. Bioprospecção de Fungos de um Fragmento de Cerrado no Brasil Central para Aplicações Biotecnológicas. Fronteiras: Journal of Social, Technological and Environmental Science 7(1):288–305., Naves et al. 2019NAVES, L.R., LEONARDO-SILVA, L., CUNHA, E.L., ALMEIDA, V.F.R., SÁ, A.S.F., SENA, B.L., MOREIRA, I.C. & XAVIER-SANTOS, S. 2019. Filamentous fungi as promising agents for the biodegradation of biosolids compounds. Fronteiras: Journal of Social, Technological and Environmental Science 8(2):35–51.).

Species widely distributed in Brazil (Maia et al. 2015MAIA, L.C. et al. 2015. Diversity of Brazilian fungi. Rodriguesia 66(4):1033–1045.) also dominated the data recorded at the REC-UEG. On the other hand, 32% of the low-occurrence species in the area, including all the new records reported here, may be related to substrate specificity; production of inconspicuous basidiomata, especially the corticioid fungi; physiological and nutritional aspects of each species for basidioma development, which reduce their sampling on the field. The higher richness found in forest formations was expected since this vegetation presents ideal environmental conditions and varied substrate availability for fungi growth. Differently, the herbaceous vegetation of cerrado stricto sensu exposes the community to high temperatures, low humidity levels, and the entrance of winds, reducing the growth and colonization of species that are more sensitive to these climatic variations.

Although the REC-UEG suffers a strong environmental impact due to its location, it is still possible to observe expressive biodiversity that resists. Besides the richness of corticioid and poroid fungi that we reported, previous studies in the area also presented new occurrences for the Cerrado (Alvarenga & Xavier-Santos 2017ALVARENGA, R.L.M. & XAVIER-SANTOS, S. 2017. New records of Dacrymycetes (Fungi: Basidiomycota) from the Cerrado Biome (Brazilian Savanna) and Midwest Region, Brazil. Check List 13(4):335–342., Camilo-Cotrim et al. 2020CAMILO-COTRIM, C.F., LEONARDO-SILVA, L. & XAVIER-SANTOS, S. 2020. First records of Myriostoma calongei Baseia, Sousa & Martin (Geastraceae, Basidiomycota) in central Brazil. Check List 16(1):53–57., Ferreira-Sá et al. 2023FERREIRA-SÁ, A.S., LEONARDO-SILVA, L., CORTEZ, V.G. & XAVIER-SANTOS, S. 2023. Second world record for two Calvatia species (Agaricaceae: Basidiomycota). Brazilian Journal of Biology 83:e247840.). Thus, the number of specimens collected over the years, as well as the species richness shows the importance of preservation for regional Funga representativeness. Ditto, it is necessary to establish measures to protect the area, which is also used as a didactic resource by graduate, undergraduate and elementary school students who carry out research activities and educational excursions. In addition, some species collected in the area have been identified, conserved ex situ, and represent part of the genetic and biotechnological heritage of the Cerrado.

Acknowledgments

We are grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for Ph.D. scholarship provided to L. Leonardo-Silva (88882.448042/2019-01) and I. C. Moreira (88887.483359/2020-00); To the Universidade Estadual de Goiás (UEG), for permanence scholarship provide to G. Pereira-Silva (202100020014432); to Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) for funding (proc 201810267001553); to Dr. Tatiana Baptista Gibertoni by the identification and taxonomic confirmation of some species; to MSc. Ana Beatriz Lobo-Moreira for the English review.

References

Edited by

Publication Dates

History