Abstract

Hymenochaetales and Polyporales are important macrofungi for the maintenance of tropical forests, since they act directly in the nutrient cycling of the wood decomposition. In the Amazon, the largest tropical forest in the world, knowledge about Agaricomycetes is still insipient, since many areas have not yet been inventoried and new records appear each new study. To increase ecological knowledge about the Hymenochaetales and Polyporales, in the Brazilian Amazon region, collections were conducted in western Pará, Brazil, relating these fungi to the substrate they colonize and to environmental variables. 91 species were identified, with greater macrofungi richness associated with the rainy season; these fungi showed preferences for dead woods, of small diameter (class 1 = 5,9 ˫ 39 cm) and, in stages of decomposition still rigid or intermediate. The abundance and richness of Hymenochaetales and Polyporales were influenced by air humidity and the assemblage composition was influenced by temperature, air humidity and rainfall. The results indicate a rich diversity for western Pará region, these species are associated with environmental conditions, and may be threatened by the increasing pressure of human activity in the Brazilian Amazon.

Key words
Amazon; ecology; funga; fungi assemblage; polypore

INTRODUCTION

The Hymenochaetales Oberw. and Polyporales Gäum are macrofungi belonging the Phylum Basidiomycota, both popularly known as “shelf fungi” or “polypores”, which stand out for their interest in systematic and ecological studies among mycologists (Larsson et al. 2006LARSSON KH, PARMASTO E, FISCHER M, LANGER E, NAKASONE KK & REDHEAD SA. 2006. Hymenochaetales: a molecular phylogeny for the hymenochaetoid clade, Mycologia 98: 926-936., Justos et al. 2017). Currently, the constitute one of the main groups of wood-inhabiting macrofungi, comprising more than 3,182 species with very different anatomical and physiological characteristics (Larsson et al. 2006LARSSON KH, PARMASTO E, FISCHER M, LANGER E, NAKASONE KK & REDHEAD SA. 2006. Hymenochaetales: a molecular phylogeny for the hymenochaetoid clade, Mycologia 98: 926-936., Binder et al. 2013BINDER M ET AL. 2013. Phylogenetic and phylogenomic overview of the Polyporales. Mycologia 105: 1350-1373., Wijayawardene et al. 2020WIJAYAWARDENE NN ET AL. 2020 Outline of Fungi and fungus-like taxa. Mycosphere 11: 1060-1456.).

These macrofungi Hymenochaetales and Polyporales, focus of this study, are organisms of great ecological importance in tropical forests, mainly because they act in the decomposition of dead woods, facilitating nutrient cycling (Blackwell et al. 2006BLACKWELL M, HIBBETT DS, TAYLOR JW & SPATAFORA JW. 2006. Research coordination networks: a phylogeny for kingdom Fungi (Deep Hypha). Mycologia 98: 829-837., Webster & Weber 2007WEBSTER J & WEBER R. 2007. Introduction to Fungi 3 edition. Cambridge University Press: UK, 841 p.), in addition to promoting population control of plant species due to phytopathogenic and mutualistic relationships established with some plant species (Petersen 2012PETERSEN JH. 2012. The kingdom of fungi. Princeton, NJ: Princeton University Press, 272 p.).

These fungi are also important for biotechnology due to the production of cellulose and lignin degrading enzymes, with great value to the textile industry for cleaning oil-contaminated tributaries, as well as being useful in the production of pesticides (Maciel et al. 2010MACIEL MJM, CASTRO ESA & RIBEIRO HCT. 2010. Industrial and biotechnological applications of ligninolytic enzymes of the Basidiomycota: A review. Electron J Biotechnol 13: 14-15., Lomascolo et al. 2011LOMASCOLO A, UZAN-BOUKHRIS E, HERPOËL-GIMBERT I, SIGOILLOT JC & LESAGE-MEESSEN L. 2011. Peculiarities of Pycnoporus species for applications in biotechnology. Appl Microbiol Biotechnol 92: 1129-1149., Bekai et al. 2012BEKAI LH, SMANIA EDFA, SILVA RIEHL CA & SMANIA JR A. 2012. Antrodia albida (Fr.) Donk (higher Basidiomycetes) as a source of metabolites of biotechnological interest. Int J Med Mushrooms 14: 161-168.). Some species of Hymenochaetales and Polyporales are used to generate products with medicinal properties such as antiviral, anti-inflammatory substances and cancer treatment (Grienke et al. 2014GRIENKE U, ZÖLL M, PEINTNER U & ROLLINGER JM. 2014. European medicinal polypores – A modern view on traditional uses. J Ethnopharmacol 154: 564-583., Dos Reis et al. 2015DOS REIS MF. 2015. Cogumelos medicinais: uma revisão sobre compostos bioativos e efeitos biológicos. SaBios 10: 149-164., Bishop 2020BISHOP KS. 2020. Characterisation of Extracts and Anti-Cancer Activities of Fomitopsis pinicola. Nutrients 12: 609.).

Ecological information about Hymenochaetales and Polyporales is still scarce in tropical forests (e.g. Lindblad 2000LINDBLAD I. 2000. Host specificity of some wood-inhabiting fungi in a tropical forest. Mycologia 92: 399-405., 2001, Gilbert & Sousa 2002GILBERT GS & SOUSA WP. 2002. Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396-404., Gilbert et al. 2002GILBERT GS, FERRER A & CARRANZA J. 2002. Polypore fungal diversity and host density in a moist tropical forest. Biodivers Conserv 11: 947-957., 2008, Yamashita et al. 2008YAMASHITA S, HATTORI T, MOMOSE K, NAKAGAWA M, AIBA M & NAKASHIZUKA T. 2008. Effects of forest use on aphyllophoraceous fungal community structure in Sarawak, Malaysia. Biotropica 40: 354-362.). It is known that the occurrence and diversity of these fungi are directly related to environmental factors (Hawksworth & Müller 2005HAWKSWORTH DL & MÜLLER GM. 2005. Fungal Communities: Their Diversity and Distribution. In: DIGHTON J, WHITE JF & OUDEMANS P (Eds), The Fungal Community Its Organization and Role in the Ecosystem. CRC Press, p. 27-37., Hawkes et al. 2011HAWKES CV, KIVLIN SN, ROCCA JD, HUGUET V, THOMSEN MA, & SUTTLE KB. 2011. Fungal community responses to precipitation. Glob Change Biol 17: 1637-1645.), to the physical-chemical characteristics of the substrate (Boddy et al. 2008BODDY L, FRANKLAND JC & VAN WEST P. 2008. Ecology of saprotrophic Basidiomycetes, 1st ed., London: Academic Press, 371 p.), as well as to the structure habitat and environmental disturbances (Yamashita et al. 2008YAMASHITA S, HATTORI T, MOMOSE K, NAKAGAWA M, AIBA M & NAKASHIZUKA T. 2008. Effects of forest use on aphyllophoraceous fungal community structure in Sarawak, Malaysia. Biotropica 40: 354-362., Gates et al. 2011GATES GM, MOHAMMED C, WARDLAW T, RATKOWSKY DA & DAVIDSON NJ. 2011. The ecology and diversity of wood-inhabiting macrofungi in a native Eucalyptus obliqua forest of Southern Tasmania, Australia. Fungal Ecol 4: 56-67., Blaser et al. 2013BLASER S, PRATI D, SENN-IRLET B & FISCHER M. 2013. Effects of forest management on the diversity of deadwood-inhabiting fungi in Central European forests. Forest Ecol Manag 304: 42-48.).

Amazon forest is one of the richest biomes in the world in terms of biodiversity and has been threatened by overexploitation of wood, deforestation and burning, mainly to meet the interests of agribusiness and mining (Capobianco et al. 2001CAPOBIANCO JPR, VERÍSSIMO A, MOREIRA A, SAWYER D, SANTOS IP & PINTO LP. 2001. Biodiversidade na Amazônia brasileira: avaliação e ações prioritárias para a conservação, uso sustentável e repartição de benefícios. São Paulo: Estação Liberdade - Instituto Sócio ambiental., Ritter et al. 2017RITTER CD, MCCRATE G, NILSSON RH, FEARNSIDE PM, PALME U & ANTONELLI A. 2017. Environmental impact assessment in Brazilian Amazonia: Challenges and prospects to assess biodiversity. Biol Conserv 206: 161-168.). Thus, it is denoting that the advance of deforestation and the fragmentation of habitats are the main environmental disturbances that affect fungi (Pentillä et al. 2006PENTILLÄ R, LINDGREN M, MIETTINEN O, RITA H & HANSKI I. 2006. Consequences of forest fragmentation for polyporous fungi at two spatial scales. Oikos 114: 225-240., Yamashita et al. 2008YAMASHITA S, HATTORI T, MOMOSE K, NAKAGAWA M, AIBA M & NAKASHIZUKA T. 2008. Effects of forest use on aphyllophoraceous fungal community structure in Sarawak, Malaysia. Biotropica 40: 354-362.) and considering the territorial extent of this biome, many areas have not been inventoried yet, resulting in risks to the Funga not known yet.

The most expressive studies on Hymenochaetales and Polyporales in the Amazon region were carried out by Gibertoni et al. (2016)GIBERTONI TB, MEDEIROS PS, SOARES AMS, GOMES-SILVA AC, SANTOS PJP, SOTÃO HMP, FERREIRA LV & SAVINO E. 2016. The distribution of polypore fungi in endemism centres in Brazilian Amazonia. Fungal Ecol 20: 1-6. who analyzed the distribution of Hymenochaetales and Polyporales assemblages in Amapá, Pará and Rondônia states, Gibertoni (2008)GIBERTONI TB. 2008. Polyporoid fungi (Agaricomycetes, Basidiomycota) in the Estação Científica Ferreira Penna (State of Pará, Brazilian Amazonia): diversity and ecological aspects. Sci Acta 2: 70-74. and Medeiros et al. (2015)MEDEIROS PS, CATTANIO JH & SOTÃO HMP. 2015. Riqueza e relação dos fungos poroides lignolíticos (Agaricomycetes) com o substrato em floresta da Amazônia brasileira. Bol Mus Para Emílio Goeldi 10: 423-436., observed the influence of the characteristics of the substrates on the fungal composition of the northern region of Pará, demonstrating that the richness and diversity of Hymenochaetales and Polyporales are positively related to their wood size or decomposition stage.

Our hypothesis is that the diameter and physical state of dead woods can influence the abundance and richness of Hymenochaetales and Polyporales, as well as local environmental variables. The objectives of this study were: i - investigate the influence of environmental variables on the abundance, richness and assemblage of Hymenochaetales and Polyporales, ii - determine the occurrence/preference of the abundance and richness of Hymenochaetales and Polyporales among living or dead woods, iii - evaluate the occurrence of abundance and richness of Hymenochaetales and Polyporales between the stages of decomposition and the diameter of dead woods.

MATERIALS AND METHODS

Study area

The study was carried out in an 8 km² Amazon Forest fragment near the Silvio Braga Hydroelectric Power Plant (HPP) (centroid coordinates: 2°49’11.49”S; 54°17’56.64”W), located in Santarém city, Pará state, Brazil. The study area has vegetation cover of dense ombrophylous forest (Veloso et al. 1991VELOSO HP, RANGEL FILHO ALR & LIMA JCA. 1991. Classificação da vegetação brasileira adaptada a um sistema universal. Rio de Janeiro: IBGE - Departamento de recursos naturais e estudos ambientais.) and with yellow latosol (Jati & Silva 2017JATI DA & SILVA JT. 2017. Estudos geo-hidrológicos da bacia do rio Curuá-Una, Santarém, Pará: Aplicação do modelo hidrológico de grandes bacias (MGB-IPH). Rev Bras Geogr Fís 10: 1296-1311.). The climate is classified as humid tropical, with an average annual temperature of 27 °C (± 5 ^oC). The average relative humidity of the air is 88% and the average annual rainfall is 2,200 mm, with greater rainfall occurring between the months of January to May (rainy season; monthly average of 231 mm) and lower rainfall from August to November (dry period; monthly average of 61 mm) (Alvares et al. 2013ALVARES CA, STAPE JL, SENTELHAS PC, MORAES G, LEONARDO J & SPAROVEK G. 2013. Köppen’s climate classification map for Brazil. Meteorol Z 22: 711-728.).

Collection and identification of Hymenochaetales and Polyporales

Excursions for the collection of Hymenochaetales and Polyporales were carried out quarterly in 2018 (January, April, July and October), with collections over 30 transects of 250 m each, equidistant of 250 m with the beginning of the transects at 50 m from the edge of the forest, demarcated by PA-370 (Figure 1).

The basidiomata (fruiting bodies) found along each transect were collected following the protocol of Fidalgo & Bononi (1984)FIDALGO O & BONONI VLR. 1984. Técnicas de coleta, preservação e herborização de material botânico. Instituto de Botânica, São Paulo. and Lodge et al. (2004)LODGE DJ, AMMIRATI JF, O’DELL TE & MUELLER GM. 2004. Collecting and describing macrofungi. In: MUELLER GM, BILLS GF & FOSTER MS (Eds), Biodiversity of fungi: inventory and monitoring methods. Oxford: Elsevier Academic Press, p. 128-158., which consists of photographing the basidiomata before they are removed and afterwards, perform manual removal using a chisel or pocket knife, followed by accommodation of the basidiomata in paper bags with the appropriate collection information (number of the collector, type of substrate, geographic coordinates). At the Laboratory, the specimens were dehydrated at 35 °C (± 2 °C) in a forced air circulation oven for a period of two to three days (Fidalgo & Bononi 1984FIDALGO O & BONONI VLR. 1984. Técnicas de coleta, preservação e herborização de material botânico. Instituto de Botânica, São Paulo.) and then mounted on exsiccates.

The identification of Hymenochaetales and Polyporales was based on macro and microscopic analysis. The macroscopic analysis consisted of detailed observations of the basidiomata with the naked eye and/or with the aid of a stereoscopic microscope, analyzing their insertion in the substrate, size (length, width and thickness), color, consistency, characteristics of the surfaces of the cap and pores, the tubes, the context and the margin of the basidiome. The color of the basidiome was determined by comparing the color chart by Kueppers (1982)KUEPPERS H. 1982. Color Atlas: A Practical Guide for Color Mixing. Barrons Educational Series Incorporated: New York, 171 p..

For microscopic analysis, sections of different parts of the basidiomata (pileus, context and tubes) were made with the aid of a steel blade, under a binocular optical microscope. The cuts were arranged between slides and coverslips immersed in different aqueous solutions: 3% potassium hydroxide (moisturizer), phloxin, methylene blue (dyes) and, Melzer reagent to evidence the reactions of the microstructure walls, which can be positive or negative and, which vary according to each species: hyaline (colorless tone, with visible cell wall), amyloid (blue to purple/violet tone) or dextrinoid (gold to reddish tone) (Teixeira 1995TEIXEIRA AR. 1995. Método para estudo das hifas do basidiocarpo de fungos poliporáceos. São Paulo: Instituto de Botânica, 95 p., Ryvarden 2004RYVARDEN L. 2004. Neotropical Polypores Part 1. Introduction, Ganodermataceae & Hymenochaetaceae. Synopsis Fungorum 19: 1-229.). The hyphalic system (monomitic, di-trimitic), reproductive structures (basidia and basidiospores) and sterile structures (cistidia, cystidioles, setae, among others), were also analyzed.

After analyzed, the characteristics were compared with the specialized literature of the studied taxa Reid (1965)REID DA. 1965. A monograph of the stipitate stereoid fungi. Beihefte zur Nova Hedwigia 18: 484 p., Ryvarden & Johansen (1980)RYVARDEN L & JOHANSEN I. 1980. A preliminary polypore flora of East Africa. Oslo: Fungiflora, 636 p., Furtado (1981)FURTADO JS. 1981. Taxonomy of Amauroderma (Basidiomycetes, Polyporaceae). Mem N Y Bot Gard 12: 1-109., Núñez & Ryvarden (1995)NÚÑEZ M & RYVARDEN L. 2001. East asian Polypores. Vol. 2: Polyporaceae s. lato. Synopsis Fungorum 14: 169-522., Ryvarden (2004, 2015RYVARDEN L. 2015. Neotropical polypores part 2. Polyporaceae: Abortiporus - Meripilus. Synopsis Fungorum 34: 229-443., 2016RYVARDEN L. 2016. Neotropical polypores Part 3. Polyporaceae: Obba - Wrightoporia. Synopsis Fungorum 36: 446-612.), Dai (2010)DAI YC. 2010 Hymenochaetaceae in China. Fungal Divers 45: 131-343., Gomes-Silva et al. (2014GOMES-SILVA AC, LIMA-JÚNIOR N, MALOSSO E, RYVARDEN L & GIBERTONI TB. 2015. Delimitation of taxa in Amauroderma (Ganodermataceae, Polyporales) based in morphology and molecular phylogeny of Brazilian specimens. Phytotaxa 227: 201-228., 2015GOMES-SILVA AC, MEDEIROS PS, SOARES AMS, SOTÃO HMP, RYVARDEN L & GIBERTONI TB. 2014. Two new species of Rigidoporus (Agaricomycetes) from Brazil and new records from the Brazilian Amazonia. Phytotaxa 156: 191-200.), Costa-Rezende et al. (2016)COSTA-REZENDE DH, GUGLIOTTA AM, GOES-NETO A, RECK MA, ROBLEDO GL & DRECHSLER-SANTOS ER. 2016. Amauroderma calcitum sp. nov. and notes on taxonomy and distribution of Amauroderma species (Ganodermataceae). Phytotaxa 244: 101-124., Palacio et al. (2017)PALACIO M, ROBLEDO GL, RECK MA, GRASSI E, GÓES-NETO A & DRECHSLER-SANTOS ER. 2017. Decrypting the Polyporus dictyopus complex: Recovery of Atroporus Ryvarden and segregation of Neodictyopus gen. nov. (Polyporales, Basidiomyocta). PLoS ONE 12: e0186183. and used to identify and/or confirm the species. The species classification was continuously updated according to the Index Fungorum (http://www.indexfungorum.org) and the testimony material was deposited in the collection of fungi of the Herbarium HSTM of the Universidade Federal do Oeste do Pará (UFOPA).

Environmental variables

In each excursion the light input through the canopy, the temperature, the relative humidity and the rainfall were measured. Additionally, we categorized the substrates of occurrence of fungi in live or dead woods, diameter classes and decomposition stage for dead woods.

The entry of light through the canopy into the forest (canopy opening), temperature and relative humidity were measured every 50 m of each transect. Light input was estimated by canopy photographs taken at 1.30 m from the ground, transformed into black and white, of which white pixels were counted using Adobe Photoshop CC 2015© software, with the threshold function and the luminosity histogram (Marsden et al. 2002MARSDEN SJ, FIELDING AH, MEAD C & HUSSIN MZ. 2002. A technique for measuring the density and complexity of understorey vegetation in tropical forests. Forest Ecol Manag 165: 117-123.). Air temperature and relative humidity were measured with a digital thermo-hygrometer (Hikari, model HTH-240). And the rainfall was measured with the aid of handmade rain gauges composed of a 27.60 cm diameter funnel coupled to gallons of 20 L installed 125 m from the beginning of the 5^th, 15^th and 25^th transects (Figure 1).

The diameter of the woods with the occurrence of Hymenochaetales and Polyporales were measured using a tape measure and grouped in a class interval table according to Sturges (1926)STURGES HA. 1926. The choice of a class interval. Journal of the american statistical association 21: 65-66., with eight classes being established: class 1 (5.9 ˫ 39 cm), class 2 (39 ˫ 72 cm), class 3 (72 ˫ 105 cm), class 4 (105 ˫ 139), class 5 (139 ˫ 172 cm), class 6 (172 ˫ 205 cm), class 7 (205 ˫ 238 cm) and class 8 (271 ˫ 305 cm).

The decomposition stages of the woods were also verified (D1 to D3) and determined according to Nordén & Paltto (2001)NORDÉN B & PALTTO H. 2001. Wood-decay fungi in hazel wood: species richness correlated to stand age and dead wood features. Biol Conserv 101: 1-8.. In the D1 stage, the wood fell recently, therefore, still rigid, so that a knife with the strength of the hand penetrates less than 2 mm. In the stage D2 the knife easily penetrates from 2 to 20 mm and in the stage D3 the knife easily penetrates more than 20 mm.

Data analysis

For data analysis, we built a spreadsheet with all the information in Microsoft Excel 2019© software relating abundance and richness, with the environmental variables collected in each sample period. As that the environmental variables inhibit or not the growth of fungi (Núñez 1996NÚÑEZ M. 1996. Fructification of Polyporceae s.l. (Basidiomycotina) along a gradient of altitude and humidity in the Guanacaste Conservation Area (Costa Rica). J Trop Ecol 12: 893-898., Meier et al. 2010MEIER CL, RAPP J, BOWERS RM, SILMAN M & FIERER N. 2010. Fungal growth on a common wood substrate across a tropical elevation gradient: temperature sensitivity, community composition, and potential for above-ground decomposition. Soil Biol Biochem 42: 1083-1090.), the differences among the variables registered in each sample period was considered as a sample and not a pseudo-reply, that is, each transect per excursion was considered a sample, totaling 120 samples, except for comparisons among substrates (live or dead wood, decomposition index and trunk diameter), in which each substrate was considered a sample.

Regarding fungi, we considered richness as the total number of species found and abundance as the sum of the occurrence of specimens found in different substrates. Data on light input, temperature and air humidity were measured by transect. Rainfall data were measured by month, using the sampling months for this study.

The relative frequency of species (F) was calculated using the function: F = n / N x 100, where n is the number of specimens of a species and N is the total number of specimens found (Lindblad 2001LINDBLAD I. 2001. Diversity of poroid and some corticioid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. J Trop Ecol 17: 353-369.), in order to present the dominance of the species found in the study area.

For all data, we tested the assumptions of normality (shapiro-wilk) and homogeneity (Breuch-Pagan). To remove the multicollinearity of the variables (linear relationship between the explanatory variables with a value above 10) we used a Variation Inflation Factor (VIF) and a correlation in order to remove the instability from the regression model and eliminate correlated variables (correlation above 70%). The Variation Inflation Factor analysis did not show multicollinearity or correlation between environmental variables.

The relationships between richness (total number of species) and abundance (total number of specimens) of Hymenochaetales and Polyporales with environmental variables (canopy opening, temperature and air humidity) were analyzed by multiple linear regressions, with the stepwise method using the Vegan package (Oksanen et al. 2015OKSANEN J ET AL. 2015. Vegan: Community Ecology Package. R package version 2.3-0.), all analyzes were performed on R 3.5.2 (R Core Team 2012R CORE TEAM 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.).

To relate the assemblage (species composition) of Hymenochaetales and Polyporales with the environmental variables, a simple regression analysis was used. For this, the representative matrix of the assemblage of Hymenochaetales and Polyporales was reduced to the first axis of a Principal Coordinate Analysis (PCoA) based on Bray-Curtis dissimilarity, using the MASS (Ripley et al. 2013RIPLEY B ET AL. 2013. Package ‘mass’. Cran r 538: 113-120.) and Vegan package (Oksanen et al. 2015OKSANEN J ET AL. 2015. Vegan: Community Ecology Package. R package version 2.3-0.). A similarity analysis (ANOSIM) based on Bray-Curtis dissimilarity, with 1,000 randomizations was used to assess the relationship between the collection periods, we used the Vegan package (Oksanen et al. 2015OKSANEN J ET AL. 2015. Vegan: Community Ecology Package. R package version 2.3-0.).

Environmental data, richness and abundance were compared between sample periods by one-way Analysis of Variance (ANOVA), followed by Tukey’s test when necessary, using the Vegan package (Oksanen et al. 2015OKSANEN J ET AL. 2015. Vegan: Community Ecology Package. R package version 2.3-0.) and Car (Fox & Weisberg 2011FOX J & WEISBERG S. 2011. An R Companion to Applied Regression, 2nd ed. Los Angeles: Sage Publication.), to indicate significant differences between standard deviation pairs we used the agricolae package (Mendiburu & Mendiburu 2019MENDIBURU F & MENDIBURU MF. 2019. Statistical Procedures for Agricultural Research: Package “agricolae”. Vienna, Austria.) and the Sciplot package (Morales & Morales 2017MORALES M & MORALES MM. 2017. Sciplot: Scientific Graphing Functions for Factorial Designs. R package version 1.2-0. Vienna, Austria.) for making graphs with standard deviation bars. These analyzes reinforced the results observed in the aforementioned regressions.

Chi-square adjustment tests (χ² ) were used to compare the abundance and richness of Hymenochaetales and Polyporales between live and dead woods, between the stages of decomposition and diameter classes of the wood using the Vegan package (Oksanen et al. 2015OKSANEN J ET AL. 2015. Vegan: Community Ecology Package. R package version 2.3-0.). An individual Indication Value (IndVal, Dufrêne & Legendre 1997DUFRÊNE M & LEGENDRE P. 1997. Species assemblages and indicator species: the need for flexible asymmetrical approach. Ecol Monogr 67: 345-366.) with 1,000 randomizations was used to assess the relationship between species abundance with dead and live woods.

In order to observe all species of Hymenochaetales and Polyporales found in wood with different stages of decomposition, we generated an ordination chart using Comunidata 1.6. Finally, we performed analyze the association of Hymenochaetales and Polyporales with the stages of decomposition and with the diameter classes of the wood, utilization indices were applied (Kruys et al. 1999KRUYS N, FRIES C, JONSSON BG, LAMAS T & STAL G. 1999. Wood-inhabiting cryptogams on dead Norway spruce (Picea abies) trees in managed Swedish boreal forests. Can J For Res 29: 178-186.), using the labdsv package (Roberts 2016ROBERTS DW. 2016. labdsv: Ordination and Multivariate Analysis for Ecology. R package version 1.8-0.). When U _i = 1, there is no preference for a certain condition; U _i > 1, indicates preference for a certain condition. This analysis was performed for species with an abundance equal or greater than 10 specimens in woods with different stages of decomposition, due to the impossibility of inferring ecological patterns with low abundance of individuals (Yamashita et al. 2009YAMASHITA S, HATTORI T, OHKUBO T & NAKASHIZUKA T. 2009. Spatial distribution of the basidiocarps of aphyllophoraceous fungi in a tropical rainforest on Borneo Island, Malaysia. Mycol Res 113: 1200-1207.).

RESULTS

A total of 545 specimens of Hymenochaetales and Polyporales were collected, identified and represented in 91 species. The species with the greatest abundance and frequency of occurrence were Cerrena hydnoides (Sw.) Zmitr. with 34 specimens, Trametes elegans (Spreng.) Fr. with 31 specimens and Rigidoporus lineatus (Pers.) Ryvarden with 30 specimens, corresponding to 22.5% of the specimens collected and occurring in 29 samples (24%) (Figure 2, Table I).

The abundance and the richness of Hymenochaetales and Polyporales were positively influenced by air humidity, although with low determination coefficient values of the multiple regression (Table II). These results were indirectly confirmed by comparing the abiotic variables, the abundance and richness of Hymenochaetales and Polyporales between the rainy (January and April) and dry (July and October) periods (Figures 3, 4, Tables III, IV).

The assemblage of Hymenochaetales and Polyporales was influenced by air humidity, temperature and rainfall in the study area (Table II), with emphasis on temperature that significantly contributed to the species distribution (Figure 5, Table V). These results were directly confirmed with the comparison between rainy and dry periods (r = 0.24, p < 0.001).

The abundance of Hymenochaetales and Polyporales differed significantly between live and dead woods (r ² = 154.63, df = 1, p < 0.0001), being significantly higher in dead woods (n = 210) than in live woods (n = 21). Likewise, Hymenochaetales and Polyporales richness was significantly higher in dead than live woods (r ² = 28.45, df = 1, p < 0.001), with 52 species of Hymenochaetales and Polyporales found in dead substrates and only 10 species in living substrates. However, a significant occurrence of the species in these substrates, only for Rigidoporus lineatus (Indival = 0.44, p < 0.02) and Trametes elegans (Indival = 0.44, p < 0.02) associated with dead woods and Phylloporia chrysites (Indival = 039, p < 0.03) associated with live woods.

Significant differences in abundance and richness of Hymenochaetales and Polyporales were also observed in relation to the decay stage of the dead woods (χ ² _abundance = 254.94, gl = 2, p = 0.001; χ ² _richness = 38.87, gl = 2, p < 0.001). Hymenochaetales and Polyporales were more abundant and representative in richness in the decomposition stage D1 (n = 179, richness = 51), compared to D2 (n = 19; richness = 12) or D3 (n = 12; richness = 7), being Lenzites betulina, Perenniporia medulla-panis, Ranadivia modesta, Trametes elegans and T. variegata were found in the three stages of decomposition (D1-D2-D3), while Fomitopsis rosoealba, Ganoderma resinaceum, Lentinus crinitus, Rigidoporus lineatus and Truncospora ochroleuca were found in two stages of decomposition (D1-D2), with emphasis on Megasporporia setulosa, Nigrofomes melanoporus and Podoscypha nitidula found in a single stage of decomposition, D2 and D3, respectively (Figure 6).

Regarding the abundant species (10 ≥ specimens) with the stages of wood decomposition Perenniporia medulla-panis, Ranadivia modesta, Lenzites betulina and Trametes elegans are related to the stage of decomposition (D2-D3), with the last two species being strongly related to stage of decomposition (D3), that is, soft substrate. Cerrena hydnoides, Fuscoporia gilva and Rigidoporus lineatus are related to the decomposition stage (D1), tough substrate. We did not record species that are related to the three stages of decomposition at the same time (Table VI).

Hymenochaetales and Polyporales were more abundant and representative in class 1 in diameter of woods (n = 97, richness = 95) and class 2 (n = 61; richness = 59), compared to the class 3 (n = 34; richness = 32), class 4 (n = 6; richness = 6), class 5 (n = 2; richness = 2), class 6 and 7 (n = 4; richness = 4) and class 8 (n = 1; richness 1). However, most species with more than ten specimens showed wood use pattern in class 3, the Ranadivia modesta species occurs in five diameter classes, with the preference strongly related to class 5, followed by Rigidoporus lineatus occurring in four classes in diameter and strongly related to class 6, and Trametes elegans occurring in three diameter classes with greater relation in class 8, four species were related in classes 1 (Table VII).

DISCUSSION

Data obtained show that the Hymenochaetales and Polyporales fungi from this region of the Amazon have a preference for dead woods with reduced diameters, in addition to the richness, abundance and assemblage of these fungi being influenced by the effects of environmental variables such as relative humidity, temperature and rainfall.

The relative humidity of the air is a factor that facilitates the growth of fungi (Núñez 1996NÚÑEZ M. 1996. Fructification of Polyporceae s.l. (Basidiomycotina) along a gradient of altitude and humidity in the Guanacaste Conservation Area (Costa Rica). J Trop Ecol 12: 893-898., Hawkes et al. 2011HAWKES CV, KIVLIN SN, ROCCA JD, HUGUET V, THOMSEN MA, & SUTTLE KB. 2011. Fungal community responses to precipitation. Glob Change Biol 17: 1637-1645.), so that humid forests can serve as refuges for Hymenochaetales and Polyporales, facilitating their spread. The diversity of Hymenochaetales and Polyporales varies along a gradient or factors related to rainfall between dry and wet periods (Lindblad 2001LINDBLAD I. 2001. Diversity of poroid and some corticioid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. J Trop Ecol 17: 353-369.), a fact observed in the present study, in which the greatest richness and abundance occurs in the rainy period (January and April).

However, it is not always possible to establish a direct correlation between environmental variables and the Hymenochaetales and Polyporales assemblage (e.g. Lindblad 2001LINDBLAD I. 2001. Diversity of poroid and some corticioid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. J Trop Ecol 17: 353-369., Laganà et al. 2002LAGANÀ A, SALERNI E, BARLUZZI C, DE DOMINICIS V & PERINI C. 2002. Fungi (macromycetes) in various types of Mediterranean forest ecosystems (Tuscany, Italy). Pol Bot J 47: 143-165., Gibertoni 2008GIBERTONI TB. 2008. Polyporoid fungi (Agaricomycetes, Basidiomycota) in the Estação Científica Ferreira Penna (State of Pará, Brazilian Amazonia): diversity and ecological aspects. Sci Acta 2: 70-74.), this relationship depends on the characteristics of each occurrence of these fungi. Gibertoni et al. (2007)GIBERTONI TB, SANTOS PJP & CAVALCANTI MAQ. 2007. Ecological aspects of Aphyllophorales in the Atlantic rain forest in northeast Brazil. Fungal Divers 25: 49-67., for example, reported significant differences in the assemblage of Hymenochaetales and Polyporales found in different sample periods in thirteen areas of Atlantic Forest in the Northeast of Brazil, similar to that found in the present study, although it has diverged as to the period of the year in which these fungi were most often. Other studies were similar, comparing fungal assemblages, and did not observe significant differences between periods of greater or lesser drought (Núñez 1996NÚÑEZ M. 1996. Fructification of Polyporceae s.l. (Basidiomycotina) along a gradient of altitude and humidity in the Guanacaste Conservation Area (Costa Rica). J Trop Ecol 12: 893-898., Gibertoni et al. 2015GIBERTONI TB, NOGUEIRA-MELO GS, LIRA CR, BALTAZAR JM & SANTOS PJ. 2015. Distribution of poroid fungi (Basidiomycota) in the Atlantic Rain Forest in Northeast Brazil: implications for conservation. Biodivers Conserv 24: 2227-2237.).

The richness and abundance of Hymenochaetales and Polyporales species were clearly higher in dead wood. This type of substrate allows greater use by fungi in relation to live woods, it indicates that are functional according to their ability to decompose by the conditions of the substrate found, and what varies according to the physical and chemical properties of the substrate (Adarsh et al. 2015ADARSH CK, KUMAR V, VIDYASAGARAN K & GANESH PN. 2015. Decomposition of Wood by Polypore Fungi in Tropics-Biological, Ecological and Environmental Factors-A Case Study. Res J Agr Forest Sci 3: 15-37.). Thus, there is a generalization of the use of dead woods by species of fungi (Lindhe et al. 2004LINDHE A, ASENBLAD N & TORESSON HG. 2004. Cut logs and high stumps of spruce, birch, aspen and oak – 9 years of saproxylic fungi succession. Biol Conserv 119: 443-454., Tikkanen et al. 2006TIKKANEN OP, MARTIKAINEN P, HYVÄRINEN E, JUNNINEN K & KOUKI J. 2006. Red-listed boreal forest species of Finland: associations with forest structure, tree species, and decaying wood. Ann Zool Fenn 43: 373-383., Wong 2009WONG DWS. 2009. Structure and action mechanism of ligninolytic enzymes. Biotechnol Appl Biochem 157: 174-209.).

Species of the genus Amauroderma, Coltricia and Phylloporia spathulata were found in the soil, demonstrating specialization in accessing another niche, possibly ectomycorrhizal relationships with living tree roots or in buried debris (Tedersoo et al. 2007TEDERSOO L ET AL. 2007 Ectomycorrhizas de Coltricia e Coltriciella (Hymenochaetales, Basidiomycota) em Caesalpiniaceae, Dipterocarpaceae e Myrtaceae em Seychelles. Mycol Progress 6: 101-107., Ryvarden 2004RYVARDEN L. 2004. Neotropical Polypores Part 1. Introduction, Ganodermataceae & Hymenochaetaceae. Synopsis Fungorum 19: 1-229., Yamashita et al. 2009YAMASHITA S, HATTORI T, OHKUBO T & NAKASHIZUKA T. 2009. Spatial distribution of the basidiocarps of aphyllophoraceous fungi in a tropical rainforest on Borneo Island, Malaysia. Mycol Res 113: 1200-1207.). In addition, the physical properties of soils can cause these species to occur in the study area (O’Hanlon & Harrington 2012O’HANLON R & HARRINGTON TJ. 2012. Macrofungal diversity and ecology in four Irish forest types. Fungal Ecol 5: 499-508.).

Wood decomposition is a dynamic process linked to an ecological succession of the fungal community or assemblage (Rajala et al. 2012RAJALA T, PELTONIEMI M, PENNANEN T & MÄKIPÄÄ R. 2012. Fungal community dynamics in relation to substrate quality of decaying Norway spruce (Picea abies (L.) Karst.) logs in boreal forests. FEMS Microbiol Ecol 81: 494-505., Siitonen & Stockland 2012SIITONEN J & STOKLAND JN. 2012. Chapter 8, Tree size. In: STOKLAND JN, SIITONEN J & JONSSON BG (Eds), Biodiversity in Dead Wood. Cambridge: University Press, p. 183-193.). The preferential occurrence of fungi at a given stage of decomposition is related to the degradation capacity of the fungus itself (Gibertoni 2008GIBERTONI TB. 2008. Polyporoid fungi (Agaricomycetes, Basidiomycota) in the Estação Científica Ferreira Penna (State of Pará, Brazilian Amazonia): diversity and ecological aspects. Sci Acta 2: 70-74.). In species of Hymenochaetales and Polyporales were observed occurring preferentially in woods in stages of decomposition D1 and D2, that is, in more intact woods.

The decomposition process starts from the wood dense (D1), with low moisture content, low decomposition rate and have a higher amount of sapwood, facilitating the development of wood degrading fungi, the decay rate gradually increases to a peak during the intermediate stages (D2) which are characterized by a high diversity of basidiomata (Lindblad 2001LINDBLAD I. 2001. Diversity of poroid and some corticioid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. J Trop Ecol 17: 353-369., Mäkinen et al. 2006MÄKINEN H, HYNYNEN J, SIITONEN J & SIEVÄNEN R. 2006. Predicting the decomposition of Scots pine, Norway spruce, and birch stems in Finland. Ecol Appl 16: 1865-1879., Gibertoni et al. 2007GIBERTONI TB, SANTOS PJP & CAVALCANTI MAQ. 2007. Ecological aspects of Aphyllophorales in the Atlantic rain forest in northeast Brazil. Fungal Divers 25: 49-67.). However, the decomposition rate gradually decreases (D3) to a minimum and wood decomposing fungi can no longer be detected, and the remaining wood contains only the most recalcitrant compounds (Mäkinen et al. 2006MÄKINEN H, HYNYNEN J, SIITONEN J & SIEVÄNEN R. 2006. Predicting the decomposition of Scots pine, Norway spruce, and birch stems in Finland. Ecol Appl 16: 1865-1879., Rajala et al. 2012RAJALA T, PELTONIEMI M, PENNANEN T & MÄKIPÄÄ R. 2012. Fungal community dynamics in relation to substrate quality of decaying Norway spruce (Picea abies (L.) Karst.) logs in boreal forests. FEMS Microbiol Ecol 81: 494-505.), this entire process depends on abiotic factors such as relative humidity, temperature and even the floristic composition in a given place (Stokland et al. 2012STOKLAND JN, SIITONEN J & JONSSON BG. 2012. Biodiversity in dead wood. Cambridge University Press: UK, 509 p.). The same occurrence aspect was observed in the studies carried out in the Caxiuanã National Forest (Gibertoni 2008GIBERTONI TB. 2008. Polyporoid fungi (Agaricomycetes, Basidiomycota) in the Estação Científica Ferreira Penna (State of Pará, Brazilian Amazonia): diversity and ecological aspects. Sci Acta 2: 70-74.) and in the RAPELD sample system (Medeiros et al. 2015MEDEIROS PS, CATTANIO JH & SOTÃO HMP. 2015. Riqueza e relação dos fungos poroides lignolíticos (Agaricomycetes) com o substrato em floresta da Amazônia brasileira. Bol Mus Para Emílio Goeldi 10: 423-436.), both environments of the Amazon Forest, but it was different in areas of the Atlantic Forest (Gibertoni et al. 2007GIBERTONI TB, SANTOS PJP & CAVALCANTI MAQ. 2007. Ecological aspects of Aphyllophorales in the Atlantic rain forest in northeast Brazil. Fungal Divers 25: 49-67.), the majority of Hymenochaetales and Polyporales species occurring on substrates in stages D2 and D3 of decomposition.

The knowledge about the decomposition stage still demands a greater study time, was also observed in Pasanen et al. (2014)PASANEN H, JUNNINEN K & KOUKI J. 2014. Restoring dead wood in forests diversifies wood-decaying fungal assemblages but does not quickly benefit red-listed species. For Ecol Mana 312: 92-100. and Kwaśna et al. (2017)KWAŚNA H ET AL. 2017. Abundance and diversity of wood-decay fungi in managed and unmanaged stands in a Scots pine forest in Western Poland. For Ecol Mana 400: 438-446. where the study time was relatively short, and the perception of dead wood in different stages of decomposition in the study area was greater than the others, this factor being a tendency to find fungal species in the first stages of succession decomposition. Most Hymenochaetales and Polyporales have a strong tendency to produce basidiome at a certain stage of decomposition (Lindblad 1998, Gibertoni 2008GIBERTONI TB. 2008. Polyporoid fungi (Agaricomycetes, Basidiomycota) in the Estação Científica Ferreira Penna (State of Pará, Brazilian Amazonia): diversity and ecological aspects. Sci Acta 2: 70-74.), as species found mainly from pioneer decomposers, and lack of wood at advanced stages of decomposition other fungal species (Junninen & Komonen 2011JUNNINEN K & KOMONEN A. 2011. Conservation ecology of boreal polypores: A review. Biol Conserv 144: 11-20.), which corresponds to this study.

The abundance and richness of Hymenochaetales and Polyporales decreased with the increase in the diameter of the wood, with the largest records being in woods with a diameter class of 5 to 39 cm, data that corroborate studies conducted in tropical forests in other parts of the Amazon and also in Malaysia (Yamashita et al. 2009YAMASHITA S, HATTORI T, OHKUBO T & NAKASHIZUKA T. 2009. Spatial distribution of the basidiocarps of aphyllophoraceous fungi in a tropical rainforest on Borneo Island, Malaysia. Mycol Res 113: 1200-1207., Medeiros et al. 2015MEDEIROS PS, CATTANIO JH & SOTÃO HMP. 2015. Riqueza e relação dos fungos poroides lignolíticos (Agaricomycetes) com o substrato em floresta da Amazônia brasileira. Bol Mus Para Emílio Goeldi 10: 423-436.). In the rainforest of Costa Rica and in the alder forest in Argentina, Hymenochaetales and Polyporales occur preferably in woods over 40 cm in diameter (Lindblad 2001LINDBLAD I. 2001. Diversity of poroid and some corticioid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. J Trop Ecol 17: 353-369., Urcelay & Robledo 2009URCELAY C & ROBLEDO G. 2009. Positive relationship between wood size and basidiocarp production of polypore fungi in Alnus acuminata forest. Fungal Ecol 2: 135-139.), as in boreal and temperate forests (Junninen & Komonen 2011JUNNINEN K & KOMONEN A. 2011. Conservation ecology of boreal polypores: A review. Biol Conserv 144: 11-20., Abrego & Salcedo 2013ABREGO N & SALCEDO I. 2013. Variety of woody debris as the factor influencing wood-inhabiting fungal richness and assemblages: Is it a question of quantity or quality? Forest Ecol Manag 291: 377-385.). The abundance and richness of fungi in larger diameter class woods is probably due to the greater availability of resources, microhabitat, space and humidity (Bader et al. 1995BADER P, JANSSON S & JONSSON BG. 1995. Wood-inhabiting fungi and substratum decline in selectively logged boreal spruce forests. Biol Conserv 72: 355-362., Lindblad 2001LINDBLAD I. 2001. Diversity of poroid and some corticioid wood-inhabiting fungi along the rainfall gradient in tropical forests, Costa Rica. J Trop Ecol 17: 353-369., Stokland et al. 2012STOKLAND JN, SIITONEN J & JONSSON BG. 2012. Biodiversity in dead wood. Cambridge University Press: UK, 509 p., Halme et al. 2013HALME P, VARTIJA N, SALMELA J, PENTTINEN J & NORROS V. 2013. High within-and between-trunk variation in the nematoceran (Diptera) community and its physical environment in decaying aspen trunks. Insect Conserv Divers 6: 502-512.).

The abundance and richness of Hymenochaetales and Polyporales in dead wood depend on sample size (Fukasawa 2021FUKASAWA Y. 2021. Ecological impacts of fungal wood decay types: A review of current knowledge and future research directions. Ecol Res: 1-22.). Our sample data by diameter classes is an attempt to make a compromise in relation to wood diameter at large and small scales, thus providing conditions for producing adequate and reliable results on fungal abundance and richness for future studies. For example, our data corroborate Medeiros et al. (2015)MEDEIROS PS, CATTANIO JH & SOTÃO HMP. 2015. Riqueza e relação dos fungos poroides lignolíticos (Agaricomycetes) com o substrato em floresta da Amazônia brasileira. Bol Mus Para Emílio Goeldi 10: 423-436. and Gibertoni (2008)GIBERTONI TB. 2008. Polyporoid fungi (Agaricomycetes, Basidiomycota) in the Estação Científica Ferreira Penna (State of Pará, Brazilian Amazonia): diversity and ecological aspects. Sci Acta 2: 70-74. in relation to species with more than ten records, all have a wide distribution of frequency and preference in the first class of dead wood diameter (5.9 ˫ 39 cm), with the exception of Lenzites betulina which has preference only by one diameter class, data that differ from those obtained by Kwaśna et al. (2017)KWAŚNA H ET AL. 2017. Abundance and diversity of wood-decay fungi in managed and unmanaged stands in a Scots pine forest in Western Poland. For Ecol Mana 400: 438-446. where fungal species are found in larger diameters. Diameter size is important in studies of dead wood and wood-dwelling fungi (Juutilainen et al. 2011JUUTILAINEN K, HALME P, KOTIRANTA H & MÖNKKÖNEN M. 2011. Size matters in studies of dead wood and wood-inhabiting fungi. Fungal Ecol 4: 342-349.).

Among the species found in the present study, the only one common to the work of Medeiros et al. (2015)MEDEIROS PS, CATTANIO JH & SOTÃO HMP. 2015. Riqueza e relação dos fungos poroides lignolíticos (Agaricomycetes) com o substrato em floresta da Amazônia brasileira. Bol Mus Para Emílio Goeldi 10: 423-436. was Fuscoporia gilva, Rigidoporus lineatus and Ranadivia modesta that presented a wide frequency distribution in the different diameter classes in both. This could be explained by the fact that the species are perennial and, therefore, could be found in the same wood throughout its decomposition process (Halbwachs et al. 2016HALBWACHS H, SIMMEL J & BÄSSLER C. 2016. Tales and mysteries of fungal fruiting: How morphological and physiological traits affect a pileate lifestyle. Fungal Biol Rev 30: 36-61., Maurice et al. 2021MAURICE S, ARNAULT G, NORDÉN J, BOTNEN SS, MIETTINEN O & KAUSERUD H. 2021. Fungal sporocarps house diverse and host-specific communities of fungicolous fungi. ISME J 15: 1445-1457.).

Our standardized sampling indicates that environmental variables influence the richness, abundance and assemblage of Hymenochaetales and Polyporales in this region of the Amazon. The data on substrates demonstrate that the studied richness and abundance is affected by the quality and diameter of the substrate, thus indicating a possible diversity of broad-lived strategies, since these species are capable of occupying all types of substrates available. In addition, the knowledge about Hymenochaetales and Polyporales for the Brazilian Amazon region has been expanded, as well as the certainty of the importance of encouraging mycological research in such a little-explored location.

These data may promote subsidies and framework for assessing the state of conservation at the community/assemblage level and in making decisions about the management of natural resources.

Our data emphasize the need for collections elsewhere, whether in fragmented forest areas or in Conservation Units (UC) such as Private Natural Heritage Reserve (RPPN), Biological Reserves (REBIO), National Forest (FLONA) and National Park (PARNA), explore these places in short and long-term monitoring projects to understand the funga as well as its successional role in wood decomposition, unify these data and promote subsidies and structure to assess the conservation status for each species found in the decisions about the management of natural resources.

ACKNOWLEDGMENTS

The authors thank Universidade Federal do Oeste do Pará (UFOPA) for the infrastructure offered to carry out this work and Eletrobrás Santarém for the support during the collections in the study area. The first author thanks the Programa de Pós-Graduação em Biodiversidade and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the Master’s degree scholarship. We thank Dr. Genivaldo Alves for his assistance in identifying some species of Hymenochaetaceae. We also thank Dr. Rato Fraga for his help in using the R software, and his friend MSc. Marcos Santana for collecting fungi and reviewing this manuscript.

REFERENCES

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