Checklist of Amazonian gasteroid fungi (Agaricomycetidae, Phallomycetidae, Basidiomycota)

The Amazon rainforest is the largest tropical rainforest in the world, with high biodiversity of organisms. Despite the increasing knowledge about fungal diversity in the last few years, many fungal taxa, including gasteroid clades, are still poorly known. Gasteroid fungi are recognized by the maturation of basidiospores inside the basidiomata and by the passive release of spores. We conducted a detailed survey of published data on the species that occur in Amazon forests. We confirmed the occurrence of 83 species distributed in 22 genera, eight families and four orders. The most representative genera was Geastrum, followed by Cyathus , Lycoperdon and Phallus . We present an identification key for Amazonian gasteroid genera and a map of record distribution. This review is expected to contribute to identify distribution gaps for further research on gasteroid fungi and to subsidize policies for the conservation of fungi in the Amazon region.


INTRODUCTION
The Amazon rainforest is a mosaic of different phytophysiognomies that form one of the largest and most diverse rainforests in the world (Coutinho 2006;MMA 2007).The region faces important conservation challenges, with increasingly high rates of deforestation and biodiversity loss (Oliveira-Filho and Metzger 2006;Giam 2017).In this context, the knowledge about the fungal community is essential for the conservation and restoration of these areas (Fink et al. 2021) since fungi act directly in nutrient cycling in the soil (Kirk et al. 2008).
Estimates indicate that 90% of the species of fungi are unknown to science (Antonelli et al. 2020).The Neotropical region, especially in extensive forests such as Amazonia, probably harbors many undiscovered species, mainly due to the high rate of endemic species per area (Hawswork and Lücking 2017).Recent studies reported the occurrence of about 1000 species of macrofungi for the Brazilian Amazon ACTA AMAZONICA forest (Maia et al. 2015).Despite being relatively better known than other groups, publications on gasteroid fungi, a group characterized by passive spore dispersion, are also scarce and widely dispersed throughout the Amazon domain, concentrating mainly around few research poles in the region (Maia et al. 2015).
Gasteroid fungi have various morphotypes and grow on different types of substrates, such as soil, wood, manure, and leaves, acting directly in nutrient cycling, as well as decomposition of organic matter and mycorrhizal symbiosis (Miller and Miller 1988;Alexopoulos et al. 1996).Some groups have medical and pharmacological importance.For example, Cyathus Haller species have compounds capable of reducing neurodegenerative effects (Yin et al. 2019).Geastrum Pers.has species with bactericidal efficacy and biotechnological potential for waste degradation through enzymatic activities (Kuhar et al. 2016;Sevindik et al. 2017).
In this study, we carried out a compilation of published records of gasteroid fungi in Amazonian forests and provide an identification key for Amazonian genera.

MATERIAL AND METHODS
In this study, the geographical delimitation for the Amazon domain presented by Tejada et al. (2020), which comprises the Amazon Basin, was used.Data for this checklist were obtained through an extensive search in literature records published for the Amazon domain in Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Peru, Surinam, and Venezuela until March 2021.Electronic databases such as Google Scholar, Biodiversity Heritage Library, and Web of Science were used in the research.Regarding habitat, the search terms were rainforest, moist forest, flooded forest, tropical lowland rainforest, forest of pre-Andean slopes, floodplain forest (várzea), forested stream swamps (igapó), and upland or non-flooded forest (terra firme).The search concerned mostly indexed journals, however, for older publications, we also used thesis, books and short communications that contained records of gasteroid fungi for Amazonia.Records with doubtful identification or that did not indicate any specific data about locality were not considered.
The author names and basionym of each species were obtained from Mycobank (http://www.mycobank.org/)and Index Fungorum (http://www.indexfungorum.org/),and taxonomical treatment followed Kirk et al. (2008).Records without identification at the species level were not considered.When the original manuscript did not provide geographical coordinates, points from nearby localities were used as proxies.In cases where only the country was reported, no geographic coordinates were informed, and the record was not included in the distribution map.QGISsoftware was used to produce a map of record distribution.Species were listed in alphabetical order.
Most records were from the Brazilian Amazon (64 species), followed by Bolivia and French Guiana (10 species each),   1.
Among the 83 species present in the Amazon, 26 have been originally described for this region in recent years, showing a huge potential occurrence of new taxa (Table 1).Among the 22 genera, Staheliomyces E. Fisch.had the highest number of records in all Amazonian countries, being absent only from Colombia, Peru, and Venezuela.In Brazil, most genera and species were recorded in the states of Amazonas and Pará, followed by Rondônia and Mato Grosso, while no records were found for the states of Amapá, Tocantins and Maranhão.An identification key for the genera reported from the Amazon domain is presented below.

DISCUSSION
Throughout the twentieth century, publications on gasteroid fungi in the Amazon were scarce and scattered among the domain countries.However, in the 21st century, publications have undergone a significant increase, and most are concentrated in the Brazilian Amazon.Despite the significant increase in data on the gasteroid mycota, knowledge about these organisms in the Amazon domain is still scarce relative to the extent and large biodiversity in this region.Although Amazonian centers of endemism are widely known for animals and plants (Silva et al. 2005), for fungi there are no studies with quantitative data on endemism rates, even with some species being found in the same regions, e.g Scleroderma species (Baseia et al. 2016).
Studies carried out in the Neotropical region involving integrative taxonomy have revealed a great diversity of species hidden within cosmopolitan taxa and contributed to the description of new species and new genera (Alfredo et al. 2017;Sousa, et al. 2017;Accioly et al. 2018;Accioly et al. 2019;Cabral et al. 2019;Sousa, et al. 2019).These works, besides solving taxonomic conflicts, show the great diversity of species that remain undetected, especially in poorly sampled areas.Some species found in the Amazon have morphological features that suggest possible adaptations to the region, such as Geastrum verrucoramulosum T.S. Cabral, J.O. Sousa & Baseia and Cyathus albinus Accioly, R. Cruz & Baseia (Cabral et al. 2017;Accioly et al. 2018).
The analysis of species distributions is frequently complicated by taxonomic problems, mainly in groups where interspecific differences are inconspicuous, as in species complexes and cryptic species (Vizzini et al. 2013).This is a recurrent problem for gasteroid fungi, and recent studies merging classical taxonomy with molecular techniques (e.g., barcoding) have shown that there is a high diversity of hidden species for groups that were considered as well known (Accioly et al. 2019).This is the case for Geastrum hirsutum Baseia & Calonge, G. schweinitzii and G. triplex, which have already been proven to be species complexes (Kasuya et al. 2012;Accioly et al. 2019).Likewise, the genus Myriostoma Desv.was thought to be monospecific, but more recent revisions revealed a diversity of five species for the genus (Sousa et al. 2017;Sousa et al. 2019).Lycoperdon is another genus that had recent changes in its classification.Due to the high morphological similarity between Lycoperdon and closely related genera, such as Morganella Zeller and Vascellum, many species were incorrectly identified, showing the need for molecular data to delimit species with higher reliability (Larsson and Jeppson 2008;Phosri et al. 2014;Rusevska et al. 2014;Alfredo et al. 2017).Using molecular and morphological data, Alfredo et al. (2017) also demonstrated the existence of new species and new combinations of previously identified materials, evidencing that there was a hidden diversity of Lycoperdon species under the name Morganella.Most records for these groups occur in the Amazon, highlighting that low geographical coverage of fungal surveys and taxonomic uncertainity allow the assumption that the diversity and distribution of gasteroid fungi in Amazonian forests is still widely underestimated.
The need for more studies to increase the knowledge of gasteroid diversity is made more urgent by the accelerating anthropic impacts on the region.For example, Baseia et al. (2016) identified three new species of Scleroderma Pers.and classified them as endangered.Two of these species were found in areas that are now flooded by hydroelectric dams.Greater knowledge on the Amazonian funga is necessary to better evaluate its diversity, ecosystemic roles and conservation strategies.

CONCLUSIONS
This checklist contributes to the expansion and summarization of the current knowledge of gasteroid fungi in the Amazon region.The data presented here highlight the necessity to expand collection efforts, especially in little or unexplored areas, to improve the representativeness of gasteroid fungi in herbaria and reduce the unknown component of Amazonian fungi.However, an increase in publications on Amazonian gasteroid fungi over the past two decades provided data on unexplored areas and revealed ACTA AMAZONICA taxonomic novelties.In this context, continuing biodiversity surveys are the foundation for an increase of the knowledge on these fungi and the design of more effective conservation strategies for the promotion of forest preservation.

Figure 1 .
Figure 1.Records of gasteroid fungi species (red circles) in the Amazon domain.Each dot represents a species record, and there may be more than one dot for the same species.Records for which it was not possible to estimate the geographic coordinates are not shown on the map.The green line represents the limits of the Amazon biome.AC = Acre state; AM = Amazonas state; AP = Amapá state; PA = Pará state; RO = Rondônia state; RR = Roraima state; MT = Mato Grosso state.This figure is in color in the electronic version.

Table 1 .
Species of gasteroid fungi recorded for the Amazon rainforest.Asterisks (*) represent species originally described based on types from the Amazon.(-) indicates that the location indicated by the authors was too vague to approximate geographical coordinates.