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

ABSTRACT

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.

KEYWORDS:
Neotropics; biodiversity; taxonomy; Gasteromycetes; rainforest

RESUMO

A floresta amazônica é a maior floresta tropical do mundo, com alta biodiversidade de organismos. Apesar do crescente aumento sobre o conhecimento da diversidade fúngica nos últimos anos, muitos táxons de fungos, especialmente clados gasteróides, ainda são pouco conhecidos. Os fungos gasteróides são reconhecidos pela maturação dos basidiósporos no interior do basidioma e pela liberação passiva de esporos. Baseado em dados publicados, realizamos um levantamento detalhado das espécies que ocorrem na floresta amazônica. Nós confirmamos a ocorrência de 83 espécies distribuídas em 22 gêneros, 8 famílias e 4 ordens. Os gêneros mais representativos foram Geastrum, seguido por Cyathus, Lycoperdon e Phallus. Apresentamos uma chave de identificação para gêneros de gasteróides amazônicos e um mapa de distribuição de registros. Espera-se que esta revisão contribua para identificar lacunas de distribuição para futuras pesquisas sobre fungos gasteroides e para subsidiar políticas de conservação de fungos na região amazônica.

PALAVRAS-CHAVE:
Neotrópicos; biodiversidade; taxonomia; Gasteromycetes; floresta tropical

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 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). The first records of gasteroid fungi cited for the Amazon were made by Montagne (1839), who recorded Geastrum ambiguum Mont. and Phallus indusiatus Vent.: Pers. in the Bolivian Amazon forest. Since then, most records of new Amazonian genera and species were from Brazil, especially in recent years (e.g., Trierveiler-Pereira et al. 2009; Henkel et al. 2010; Alfredo et al. 2012a; Alfredo et al. 2012b; Silva et al. 2013; Cabral et al. 2014a; Smith et al. 2015; Baseia et al. 2016; Crous et al. 2016; Cabral et al. 2017; Crous et al. 2017; Accioly et al. 2018; Crous et al. 2018; Accioly et al. 2019; Assis et al. 2019; Cabral et al. 2019).

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.

RESULTS

The survey returned 54 publications resulting in 83 species of gasteroid fungi recorded for the Amazonian domain (Table 1), of which 26 have been originally described for this region, comprising 22 genera. Figure 1 shows the records of gasteroid fungi species that were observed in the Amazon domain.The most representative are Geastrum (30 species), Cyathus (10), Lycoperdon Pers. (8) and Phallus Junius ex L. (7), which represented about 65% of all records published until March 2021. All genera recorded are distributed in eight families (Agaricaceae Chevall., Boletaceae Chevall., Diplocystaceae Kreisel, Geastraceae Corda, Nidulariaceae Dumort., Phallaceae Corda, Physalacriaceae Corner, Sclerodermataceae Corda) and four orders (Agaricales Underw., Phallales E. Fisch., Geastrales K. Hosaka & Castellano and Boletales E.-J. Gilbert).

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.

Family/Species	Country (state/province)	Coordinates	Reference
Agaricomycetidae Parmastto.
Arachnion album Schwein.	Bolivia (Concepción)	16°07’41.4”S, 62°02’23.1”W	Calonge et al. (2000)
Castellanea pakaraimophila T.W. Henkel & M.E. Smith*	Guiana (Cuyuni-Mazaruni)	5°26’21.3”N, 60°04’43.1”W	Smith et al. (2015)
Calvatia oblongispora V.L. Suárez, J.E. Wright & Calonge	Brazil (Amazonas)	3°04’45.4”S, 60°05’18.1”W	Suárez et al. (2009)
Calvatia cyathiformis (Bose) Morgan	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
Costatisporus cyanescens T.W. Henkel & M.E. Smith*	Guiana (Potaro-Siparuni)	5°18’04.8”N, 59°54’40.4”W	Smith et al. (2015)
Cyathus amazonicus Trierv.-Per. & Baseia*	Brazil (Rondônia)	8°07’39.1”S, 63°21’52.9”W	Trierveiller-Pereira et al. (2009)
	Brazil (Amazonas)	3°14’09.0”S, 60°53’10.0”W	Accioly et al. (2018)
	Brazil (Mato Grosso)	13°05’60.0”S, 54°25’55.3”W	Assis et al. (2021)
Cyathus albinus Accioly, R. Cruz & Baseia*	Brazil (Amazonas)	3°14’09.0”S, 60°53’10.0”W	Accioly et al. (2018)
Cyathus berkeleyanus (Tul. & C. Tul.) Lloyd	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
Cyathus earlei Lloyd	Brazil (Amazonas)	3°14’09.0”S, 60°53’10.0”W	Accioly et al. (2018)
	Brazil (Amazonas)	3°05’31.0”S, 59°59’39.0”W
Cyathus helenae H.J. Brodie	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
Cyathus limbatus Tul. & C. Tul. = Cyathodes limbatum	Brazil (Amazonas)	0°18’43.1”N, 68°39’09.3”W	Berkeley and Cooke (1876)
	Brazil (Amazonas)	2°57’47.5”S, 59°55’23.2”W	Accioly et al. (2018)
	Brazil (Rondônia)	10°48’45.0”S, 61°54’51.7”W	Capelari and Maziero (1988) Trierveiler-Pereira et al. (2011b)
	Guiana	-	Brodie and Dennis (1954)
Cyathus morelensis C.L. Gómez & Pérez-Silva	Brazil (Amazonas)	2°57’47.5”S, 59°55’23.2”W	Cruz et al. (2012)
Cyathus stercoreus (Schwein.) De Toni ≡ Nidularia stercorea Schwein.	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
Cyathus striatus (Huds.) Wild	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
	Colombia (Amazonas)	1°32’00.1”S, 71°21’56.6”W	Vasco-Palacios et al. (2005)
Cyathus triplex Lloyd	Brazil (Amazonas)	3°14’09.0”S, 60°53’10.0”W	Accioly et al. (2018)
	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
	Guiana (Potaro-Siparuni)	4°58’07.2”N, 59°35’00.9”W	Brodie and Dennis (1954)
Disciseda verrucosa G. Cunn.	Bolívia (Concepción)	16°07’41.4”S, 62°02’23.1”W	Calonge et al. 2000
Guyanagaster necrorhiza, M.E. Sm & Aime*	Guiana (Potaro-Siparuni)	5°18’04.8”N, 59°54’40.4”W	Henkel et al. (2010)
Jimtrappea guyanensis T.W. Henkel, M.E. Sm. & Aime*	Guiana (Potaro-Siparuni)	5°18’04.8”N, 59°54’40.4”W	Smith et al. (2015)
Lycogalopsis solmsii E. Fisch. as Morganella rimosa Baseia & Alfredo in (Alfredo et al 2012)	Brazil (Amazonas)	2°45’27.4”S, 66°45’35.7”W	Dennis (1953)
	Brazil (Amazonas)	2°57’47.5”S, 59°55’23.2”W	Alfredo et al. (2012a)
	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
Lycoperdon albostipitatum (Baseia & Alfredo) Baseia, Alfredo & M.P. Martín* ≡Morganella albostipitata Baseia & Alfredo	Brazil (Amazonas)	2°57’47.5”S, 59°55’23.2”W	Alfredo et al. (2012a)
Lycoperdon arenicola (Alfredo & Baseia) Baseia, Alfredo & M.P. Martín* ≡Morganella arenicola Alfredo & Baseia	Brazil (Amazonas)	3°05’51.4”S, 60°01’02.8”W	Alfredo et al. (2014)
Lycoperdon costaricense (M.I. Morales) Baseia, Alfredo & M.P. Martín ≡Morganella costaricensis M.I. Morales	Bolivia (Vaca Diez)	11°00’46.2”S, 66°00’42.0”W	Suarez and Wright (1996)
Lycoperdon juruense Henn.	Brazil (Amazonas)	5°05’04.4”S, 64°47’25.8”W	Hennings (1904)
Lycoperdon fuligineum Berk. & M.A. Curtis ≡Morganella fuliginea (Berk. & M.A. Curtis) Kreisel & Dring	Brazil (Amazonas)	2°58’45.3”S, 59°57’09.9”W	Cabral et al. (2014a)
	Brazil (Pará)	1°47’37.0”S, 51°26’03.8”W	Sotão et al. (2009)
Lycoperdon fuligineum Berk. & M.A. Curtis ≡Morganella fuliginea (Berk. & M.A. Curtis) Kreisel & Dring	Brazil (Rondônia)	10°56’25.3”S, 63°11’08.5”W	Capelari and Maziero (1988)
	Brazil (Mato Grosso)	13°06’44.3”S, 54°28’35.5”W	Rodrigues et al. (2021)
	Bolivia (Manuripi)	11°17’52.6”S, 67°11’09.4”W	Suarez and Wright (1996)
	Venezuela (Aragua)	4°24’25.8”N, 65°49’25.3”W	Dennis (1953)
Lycoperdon oblongatum Accioly, Baseia & M.P. Martín*	Brazil (Amazonas)	2°58’45.3”S, 59°57’09.9”W	Alfredo et al. (2017)
Lycoperdon pyriforme (Schaeff.) Kreisel & D. Krüger ≡Morganella pyriformis (Schaeff.) Kreisel & D. Krüger	Bolivia (Santa Cruz de la Sierra)	11°31’41.5”S, 65°18’38.4”W	Rocabado et al. (2007)
Lycoperdon epixylon Berk. & M.A. Curtis	Brazil (Amazonas)	4°56’32.3”S, 64°56’29.5”W	Hennings (1904)
Sclerangium braziliense Henn	Brazil (Amazonas)	0°47’35.5”S, 67°15’48.3”W	Hennings (1904)
Scleroderma anomalosporum Baseia, B.D.B. Silva & M.P. Martín*	Brazil (Pará)	5°13’24.2”S, 55°28’01.3”W	Baseia et al. (2016)
Scleroderma camassuense M.P. Martín, Baseia & B.D.B. Silva*	Brazil (Pará)	5°13’24.2”S, 55°28’01.3”W	Baseia et al. (2016)
Scleroderma duckei B.D.B. Silva, M.P. Martín & Baseia*	Brazil (Amazonas)	2°58’45.3”S, 59°57’09.9”W	Baseia et al. (2016)
Scleroderma minutisporum Baseia, Alfredo & Cortez*	Brazil (Amazonas)	2°55’12.9”S, 59°54’15.0”W	Alfredo et al. (2012b)
Scleroderma sinnamariense Mont.	Brazil (Amazonas)	4°10’44.1”S, 67°13’45.0”W	Singer and Araújo (1979)
	Guiana (Potaro-Siparuni)	4°41’53.1”N, 59°13’01.3”W	Henkel et al. (2012)
Scleroderma stellatum Berk.	Brazil (Amazonas)	4°56’32.3”S, 64°56’29.5”W	Berkeley and Cooke (1876)
	Brazil (Pará)	1°48’13.5”S, 51°26’29.9”W	Sotão et al. (2009)
Tremellogaster surinamensis E. Fisch. *	Surinam	-	Linder (1930)
	Guiana (Bartica)	6°23’25.0”N, 58°37’55.9”W	Linder (1930)
	Guiana (Potaro-Siparuni)	4°42’23.0”N, 59°22’12.2”W	Henkel et al. (2012)
	Colombia (Amazonas)	1°23’42.6”S, 72°47’45.0”W	Vasco-Palacios et al. (2005)
Tulostoma exasperatum Mont. = Schizostoma exasperatum	Brazil (Rondônia)	11°18’09.4”S, 61°03’11.0”W	Trierveiler-Pereira et al. (2011b)
Vascellum pampeanum (Speg.) Homrich as Lycoperdon pampeanum Speg.	Bolivia (Entre Rios)	17°42’57.5”S, 63°52’41.8”W	Rocabado et al. (2007)
Phallomycetidae K. Hosaka, Castellano & Spatafora
Clathrus crispus Turpin ≡ Clathrella crispa (Turpin) E. Fischer	French Guiana (Roura)	4°36’25.2”N, 52°17’07.1”W	Cheype (2010)
Geastrum albonigrum Calonge & M. Mata	Brazil (Mato Grosso)	10°49’31.8”S, 61°27’31.7”W	Trierveiler-Pereira et al. (2011b)
	Brazil (Mato Grosso)	13°06’19.4”S, 54°27’33.3”W	Rodrigues et al. (2021)
Geastrum ambiguum Mont.	Bolivia (Santa Cruz)	18°00’48.3”S, 59°37’39.1”W	Montagne (1839)
Geastrum baculicrystallum J.O. Sousa, Accioly, Baseia & M.P. Martín*	French Guiana (Saint-Laurent-du-Maroni)	4°12’25.8”N, 53°29’15.6”W	Accioly et al. (2019)
Geastrum echinulatum B.D.B. Silva & Baseia*	Brazil (Amazonas)	2°56’34.2”S, 60°01’08.3”W	Silva et al. (2013)
Geastrum englerianum Henn	Brazil (Amazonas)	3°07’09.7”S, 60°01’19.1”W	Hennings (1904)
Geastrum entomophilum Fazolino, Calonge & Baseia	Brazil (Pará)	1°56’53.3”S, 51°40’09.6”W	Leite et al. (2011)
	Brazil (Mato Grosso)	12°51’11.0”S, 54°28’47.3”W	Rodrigues et al. (2021)
Geastrum fimbriatum Fr.	Brazil (Pará)	1°56’53.3”S, 51°40’09.6”W	Leite et al. (2011)
	Brazil (Rondônia)	8°05’57.6”S, 63°23’08.4”W	Trierveiler-Pereira et al. (2009)
	Brazil (Pará)	1°27’39.1”S, 48°26’24.2”W	Trierveiler-Pereira et al. (2011a)
	Bolivia (Concepción)	16°07’52.1”S, 62°02’29.6”W	Calonge et al. (2000)
	Brazil (Mato Grosso)	13°06’44.3”S, 54°28’35.5”W	Rodrigues et al. (2021)
Geastrum hariotii Lloyd	Brazil (Pará)	1°47’52.9”S, 51°26’24.6”W	Sotão et al. (2009)
	Surinam (?) as Geaster hariotii	-	Coker and Couch (1928)
Geastrum hyalinum Freitas-Neto, N.M. Assis, J.O. Sousa & Baseia*	Brazil (Mato Grosso)	13°02’28.6”S, 54°33’31.6”W	Assis et al. (2019)
Geastrum hirsutum Baseia & Calonge	Brazil (Pará)	1°47’32.2”S, 51°29’39.8”W	Sotão et al. (2009)
Geastrum inpaense T.S. Cabral, B.D.B. Silva & I.G. Baseia*	Brazil (Amazonas)	3°05’46.6”S, 59°58’44.0”W	Cabral et al. (2014a)
Geastrum ishikawae Accioly, J.O. Sousa, Baseia & M.P. Martín*	Brazil (Amazonas)	3°05’46.6”S, 59°58’44.0”W	Crous et al. (2016)
Geastrum javanicum Lév.	Brazil (Pará)	1°42’09.6”S, 50°59’39.9”W	Sotão et al. (2009)
	Brazil (Mato Grosso)	13°06’44.3”S, 54°28’35.5”W	Rodrigues et al. (2021)
Geastrum juruense Henn. (as Geaster juruensis)	Brazil (Amazonas)	2°42’52.9”S, 60°09’09.3”W	Hennings (1904)
Geastrum lageniforme Vittad.	Brazil (Amazonas)	3°05’31.0”S, 59°59’39.0”W	Cabral et al. (2014a)
	Brazil (Pará)	1°56’53.3”S, 51°40’09.6”W	Leite et al. (2011)
	Brazil (Mato Grosso)	10°50’31.3”S, 61°27’37.0”W	Trierveiler-Pereira et al. (2011b)
	Bolivia (Concepción)	16°07’52.3”S, 62°02’29.9”W	Calonge et al. (2000)
Geastrum lilloi L.S. Domínguez	Brazil (Pará)	1°56’53.3”S, 51°40’09.6”W	Leite et al. (2011)
Geastrum lloydianum Rick	Brazil (Amazonas)	3°05’46.6”S, 59°58’44.0”W	Cabral et al. (2014a)
Geastrum mirabile Mont.	Guiana (Upper Demerara-Berbice)	5°26’12.8”N, 58°15’39.1”W	Dennis (1953)
Geastrum neoamericanum J.O. Sousa, Accioly, M.P. Martín & Baseia	Brazil (Rondônia)	9°34’53.4”S, 65°23’06.3”W	Accioly et al. (2019)
	French Guiana	4°56’13.92’’N, 52°19’33.60’’W	Accioly et al. (2019)
Geastrum ovalisporum Calonge & Mor.-Arr.	Bolivia (Concepción)	16°07’52.1”S, 62°02’29.6”W	Calonge et al. (2000)
Geastrum pusillipilosum J.O. Sousa, Alfredo, R.J. Ferreira, M.P. Martín & Baseia	Brazil (Mato Grosso)	12°59’52.8”S, 54°38’28.6”W	Rodrigues et al. (2021)
Geastrum rubellum P.-A. Moreau & C. Lécuru*	Brazil (Acre)	9°56’39.1”S, 69°40’04.1”W	Accioly et al. (2019)
Geastrum rusticum Baseia, B.D.B. Silva & T.S. Cabral	Brazil (Mato Grosso)	12°57’29.2”S, 54°35’38.7”W	Rodrigues et al. (2021)
Geastrum saccatum Fr.	Brazil (Amazonas)	3°05’46.6”S, 59°58’44.0”W	Cabral et al. (2014a)
	Brazil (Amazonas)	3°07’09.7”S, 60°01’19.1”W	Hennings (1904)
	Brazil (Pará)	1°56’53.3”S, 51°40’09.6”W	Leite et al. (2011)
	Bolivia (Concepción)	16°07’52.1”S, 62°02’29.6”W	Calonge et al. (2000)
	Colombia (Caquetá)	0°34’15.7”N, 73°49’07.1”W	Vasco-Palacios et al. (2005)
Geastrum schweinitzii (Berk. & M.A. Curtis) Zeller	Brazil (Amazonas)	3°05’46.6”S, 59°58’44.0”W	Cabral et al. (2014a)
	Brazil (Pará)	1°42’09.6”S, 50°59’39.9”W	Sotão et al. (2009)
	Brazil (Mato Grosso)	13°04’38.9”S, 54°32’35.7”W	Rodrigues et al. (2021)
	Surinam (Paramaribo)	5°50’00.0”N, 55°10’00.0”W	Zeller (1948)
Geastrum scleroderma Mont.	Brazil (Amazonas)	3°07’09.7”S, 60°01’19.1”W	Hennings (1904)
Geastrum triplex Jungh.	Brazil (Amazonas)	3°05’46.6”S, 59°58’44.0”W	Cabral et al. (2014a)
	Brazil (Mato Grosso)	13°21’24.6”S, 54°35’01.2”W	Rodrigues et al. (2021)
	Venezuela	10°28’23.0”N, 66°59’44.0”W	Coker and Couch (1928)
Geastrum trichifer Rick	Guiana (Cuyuni-Mazaruni)	7°04’00.0”N, 59°51’00.0”W	Dennis (1953)
Geastrum velutinum Morgan	Brazil (Pará)	1°42’09.6”S, 50°59’39.9”W	Sotão et al. (2009)
Geastrum verrucoramulosum T.S. Cabral, J. O Sousa & Baseia*	Brazil (Amazonas)	3°07’09.9”S, 60°01’40.4”W	Cabral et al. (2017)
	Brazil (Acre)	7°56’14.6”S, 72°47’23.2”W	Cabral et al. (2017)
Lysurus arachnoideus (E. Fisch.) Trierv.-Per. & Hosaka ≡ Aseroe arachnoidea E. Fisch.	Brazil (Amazonas)	3°23’00.8”S, 59°45’23.2”W	Cabral et al. (2015)
Mutinus bambusinus (Zoll.) E. Fisch.	Bolivia (Vaca Diez)	10°49’26.7”S, 65°22’19.2”W	Wright (1960)
Mutinus fleischeri Penz.	Brazil (Amazonas)	3°05’31.0”S, 59°59’39.0”W	Cabral et al. (2014a)
Mutinus verrucosusT.S. Cabral, B.D.B. Silva, K. Hosaka, M.P. Martín & Baseia *	Brazil (Pará)	3°55’43.8”S, 54°37’22.8”W	Crous et al. (2017)
Mutinus caninus (Huds.) Fr.	Brazil (Rondônia)	11°00’13.4”S, 61°11’15.7”W	Trierveiler-Pereira et al. (2011b)
Phallus aff. multicolor (Berk. & Broome) Cooke ≡ Dictyophora multicolor Berk. & Broome	French Guiana (Cayenne)	4°53’57.4”N, 52°19’12.2”W	Cheype (2010)
Phallus atrovolvatus Kreisel & Calonge	Brazil (Amazonas)	2°58’19.6”S, 60°03’35.0”W	Cabralet al. (2014a)
	French Guiana (Cayenne)	4°52’17.0”N, 52°14’51.6”W	Cheype (2010)
Phallus cinnabarinus (W.S. Lee) Kreisel ≡ Dictyophora cinnabarina W.S. Lee	Brazil (Pará)	1°25’50.8”S, 48°27’26.8”W	Cabral et al. (2015)
	Brazil (Pará)	1°27’07.8”S, 48°28’37.7”W
	French Guiana (Cayenne)	4°56’41.7”N, 52°19’00.9”W	Cabral et al. (2015)
Phallus denigricans T.S. Cabral, B.D.B. Silva & Baseia*	Brazil (Amazonas)	2°01’39.8”S, 64°58’53.0”W	Cabral et al. (2019)
	Brazil (Amazonas)	0°02’18.9”N, 66°12’25.8”W
Phallus indusiatus Vent.: Pers. ≡ Dictyophora indusiata (Vent.) Desv.	Brazil (Amazonas)	3°46’54.9”S, 62°06’56.7”W	Cabral et al. (2019)
	Brazil (Pará)	1°47’54.5”S, 51°29’13.7”W	Sotão et al. (2009)
	Brazil (Pará)	2°48’60.0”S, 55°01’48.7”W	Cabral et al. (2019)
	Brazil (Rondônia)	8°06’27.5”S, 63°24’56.4”W 8°41’09.0”S, 63°52’04.7”W	Trierveiler-Pereira et al. (2009)
	Brazil (Rondônia)
	Brazil (Mato Grosso)	13°14’41.1”S, 54°30’29.7”W	Rodrigues et al. (2021)
	Colombia (Amazonas)	‘0°01’20.8”S, 74°12’55.9”W	Vasco-Palacios et al. (2005)
	Colombia (Caquetá)	‘0°20’57.9”S, 72°17’18.8”W
	French Guiana (Cayenne)	4°33’48.2”N, 52°12’23.5”W 4°37’54.0”N, 52°20’14.4”W	Cheype (2010)
	French Guiana (Cayenne)
	Bolivia (Vaca Diez)	10°49’26.7”S, 65°22’19.2”W	Wright (1960)
	Bolivia	-	Montagne (1839)
Phallus merulinus (Berk.) Cooke ≡ Dictyophora merulina Berk.	Brazil (Amazonas)	3°05’31.6”S, 59°59’42.2”W	Cabral et al. (2014a)
	Brazil (Amazonas)	3°05’31.0”S, 59°59’39.0”W
	Brazil (Amazonas)	3°01’52.4”S, 59°50’35.7”W
	Brazil (Amazonas)	3°01’52.4”S, 59°50’35.7”W
	French Guiana (Cayenne)	4°52’28.6”N, 52°15’37.8”W	Cheype (2010)
	French Guiana (Cayenne)	4°56’46.1”N, 52°18’28.5”W
	French Guiana (Tonnégrande)	4°49’50.4”N, 52°26’42.4”W	Cheype (2010)
Phallus purpurascens T.S. Cabral, B.D.B. Silva & Baseia*	Brazil (Amazonas)	3°05’31.0”S, 59°59’39.0”W	Cabral et al. (2019)
	Brazil (Mato Grosso)	11°50’02.7”S, 55°30’02.3”W
Staheliomyces cinctus E. Fisch., Mitt.	Brazil (Amazonas)	3°47’29.5”S, 62°10’28.9”W	Cabral et al. (2014a)
	French Guiana (Cayenne)	4°33’04.6”N, 52°21’49.2”W	Cheype (2010)
	Bolivia (Madre de Dios)	11°19’56.8”S, 66°10’22.6”W	Wright (1960)
	Ecuador (Rio Napo)	2°14’07.4”S, 76°36’05.0”W	Burr et al. (1996)
	Surinam	-	Dennis (1970)
Xylophallus xylogenus (Mont.) E. Fisch	French Guiana (Cayenne)	4°52’17.0”N, 52°14’51.6”W	Cheype (2010)
	French Guiana (Cayenne)	4°56’39.0”N, 52°19’25.6”W
	Peru (Madre de Dios)	12°21’50.6”S, 70°24’60.0”W	Gómez and Gazis (2006)
Xylophallus xylogenus (Mont.) E. Fisch	Ecuador (Sucumbíos/ Orellana)	0°18’53.3”S, 75°42’22.7”W
	Brazil (Mato Grosso)	13°06’44.3”S, 54°28’35.5”W	Rodrigues et al. (2021)
Xylophallus clavatus T.S. Cabral, M.P. Martín, C.R. Clement, K. Hosaka & Baseia*	Brazil (Amazonas)	0°02’18.9”N, 66°12’25.8”W	Crous et al. (2018)
	Brazil (Amazonas)	2°38’04.2”S, 56°42’29.6”W
	Brazil (Pará)	2°57’11.0”S, 54°58’27.7”W

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.

Most records were from the Brazilian Amazon (64 species), followed by Bolivia and French Guiana (10 species each), Guiana (7 species), Surinam (4 species), Colombia (3 species), Venezuela and Ecuador (2 species each) and Peru (1 species). All species are listed in Table 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.

Identification key to Amazon genera of gasteroid fungi

1 - Presence of stipe or pseudostipe.....................................2

1’- Absence of stipe............................................................3

2 - Pulverulent gleba...........................................................4

2’- Mucilaginous gleba.......................................................5

3 - Gleba stored in peridioles.....................................Cyathus

3’ - Mucilaginous, pulverulent or spongy gleba, not stored in peridioles......................................................................10

4 - Dehiscence of the peridium through the formation of an apical pore.............................................................Tulostoma

4’ - Irregular dehiscence of the peridium..................................21

5 - Pseudostipe with arms or gleba......................................6

5’- Pseudostipe without arms................................................7

6 - Basidiomata vertical; Arms triangular-shaped without any connections.................................................................Lysurus

6’- Basidiomata in a form of a cage, with connected arms..........................................................................Clathrus

7 - Receptacle conical and campanulate, located in the apical portion of the pseudostipe; Pseudostipe reticulate....................8

7’- Void pseudoestipe; Gleba located at the apex of the basidiomata on the pseudostipe or forming a constriction above the center and below the apex on the pseudostipe...................9

8 - Gleba on a receptacle fixed on the apical portion of the pseudostipe; Pseudostipe cylindrical and reticulate.......Phallus

8’- Small basidiomata (up to 15 mm); Receptacle smooth with umbilicated apex and attached to the pseudostipe... Xylophallus

9 - Gleba located at the apex of the basidiomata, directly on the pseudostipe.........................................................Mutinus

9’- Gleba forming a constriction above the center and below the apex on the pseudostipe.................................Staheliomyces

10 - Pulverulent gleba...........................................................11

10’- Mucilaginous or spongy gleba...................................12

11 - Dehiscence through the formation of a pore....................16

11’- Dehiscence through irregular peridium disruption..........19

12 - Epigeous habit; Subglobose basidiomata....................13

12’- Hypogeous or semi-hypogeous habitat; Subglobose to ovoid basidiomata...............................................................14

13 - Exoperidium black and verrucous; Gleba reddish orange; Spores ornamented.............................................Guyanagaster

13’- Exoperidium white and with a little ornamentation; Spores smooth.......................................................Lycogalopsis

14 - Peridium glabrous to subtomentose; Columella absent.................................................................Costatisporus

14’- Peridium glabrous to subglabrous; Columella present....15

15 - Gleba brown in color; Basidiospores subfusiform, yellowish brown, often dextrinoid; Basidia subclavate and cystidia absent.................................................... Castellanea

15’- Gleba pink in color; Basidiospores subfusiform, pink to reddish brown and inamyloid; Basidia clavate and cystida present..................................................................Jimtrappea

16 - Dehiscence through the exoperidium, shattering into rays, star-shaped basidiomata; Subgleba absent..........Geastrum

16’- Dehiscence does not result in a star-shaped basidiomata; Subgleba present or absent………....……......................... 17

17 - Subgleba absent.................................................Disciseda

17’- Subgleba present........................................................18

18 - Presence of a membrane separating the gleba from the subgleba (diaphragm)................................................Vascelum

18’- Absence of diaphragm.....................................Lycoperdon

19 - Capillitium absent.........................................................20

19’- Capillitium present.............................................Calvatia

20 - Peridium three-layered.................................Tremellogaster

20’- Peridium one-layered.......................................Arachnion

21-Basidiospores with reticulate or spiny ornamentation ................................................................................ Scleroderma

21’- Basidiospores with subreticulate ornamentation ............................................................................. Sclerangium

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).

Genera such as Arachnion Schwein., Castellanea T.W. Henkel & M.E. Smith, Costatisporus T.W. Henkel & M.E. Smith, Clathrus P. Micheli ex L., Disciseda Czern., Guyanagaster T.W. Henkel, M.E. Smith & Aime, Jimtrappea T.W. Henkel, M.E. Smith & Aime, Lysurus Fr., Sclerangium Lév., Tulostoma Pers., and Vascellum F. Šmarda have been recorded only once, which reflects sampling effort rather than restricted distribution. Some records, especially the older ones, lack detailed information on the collection site and other aspects, such as habitat. Geastrum hariotii Lloyd was recorded for South Guiana (currently Guiana, French Guiana, and Surinam), but the authors did not mention the specific collection locality of the species (Coker and Couch 1928). Likewise, Geastrum schweinitzii (Berk. & M.A. Curtis) Zeller is only mentioned for Surinam (Zeller 1948), and Geastrum triplex Jungh. only for Venezuela (Coker and Couch 1928).

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 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.

ACKNOWLEDGMENTS

The authors would like to express their thanks to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Brazil) for the scholarships awarded to Nathalia M. Assis, Jefferson S. Góis and Julimar F. Freitas-Neto.

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• CITE AS:

  Assis, N.M.; Góis, J.S.; Freitas-Neto, J.F.; Barbosa, F.R.; Baseia, I.G. 2022. Checklist of Amazonian gasteroid fungi (Agaricomycetidae, Phallomycetidae, Basidiomycota). Acta Amazonica 52: 131-141.

Edited by

ASSOCIATE EDITOR:

Nelson Menolli Junior

Publication Dates

• Publication in this collection
  04 July 2022
• Date of issue
  Apr-Jun 2022

History

• Received
  02 Oct 2021
• Accepted
  19 Jan 2022