Phlebopus beniensis (Boletinellaceae, Boletales) in the Brazilian Cerrado biome

Abstract

The Brazilian Cerrado is a highly diverse ecosystem, harboring a great variety of organisms; however, the mycodiversity is still poorly documented. In this study, we record for the first time the bolete Phlebopus beniensis from the Cerrado biome in the state of Goiás, located in Brazil’s Central-West Region. Description, macroscopic images, line drawings and comments, as well as the geographic distribution of the genus for Brazil are presented herein.

Key words:
Basidiomycota; boletoid fungi; distribution; fungal diversity; Neotropical Region

Resumo

O Cerrado brasileiro é considerado um ecossistema altamente diverso, incluindo uma grande diversidade de organismos; no entanto, a diversidade fúngica ainda é pouco documentada. Este trabalho apresenta o primeiro registro de Phlebopus beniensis para o bioma Cerrado no estado de Goiás, Região Centro-Oeste do Brasil. Descrição, imagens macroscópicas, ilustrações microscópicas e comentários, assim como a distribuição geográfica do gênero para o Brasil são aqui apresentados.

Palavras-chave:
Basidiomycota; fungos boletoides; distribuição; diversidade fúngica; Região Neotropical

Boletinellaceae P.M. Kirk, P.F. Cannon & J.C. David is a small family comprising only two genera, Boletinellus Murrill and Phlebopus (R. Heim.) Singer (Binder & Hibbett 2006; Kirk et al. 2008). Six species have been reported from Brazil: Phlebopus beniensis (Singer & Digilio) Heinem. & Rammeloo, P. brasiliensis Singer, P. braunii (Bres.) Heinem., P. harleyi Heinem. & Rammeloo, P. portentosus (Berk. & Broome) Boedijn and P. tropicus (Rick) Heinem. & Rammeloo, distributed in the Amazon and Atlantic forests biomes (Rick 1960; Singer & Digilo 1957, 1960; Singer et al. 1983; Putzke et al.1994; Oliveira & Sousa 1996; Watling & Meijer 1997). The Brazilian Cerrado biome is considered one of the most diverse savannas in the world, as it is an important biodiversity hotspot (Myers et al. 2000; Klink & Machado 2005) and the second largest biome in Brazil. However, only 61% of the original Cerrado vegetation remains preserved, mostly represented by savanna vegetation of different densities and layers of herbaceous grasses (Rodrigues 2005; Sano et al. 2010).

Aiming at improving the knowledge of boletoid fungi from the Brazilian Cerrado, we present the first records of Phlebopus beniensis for this biome and a compilation of geographic distribution data of Phlebopus registered in Brazil.

Specimens were collected during the rainy season in the Brazilian Cerrado biome. Basidiomata were growing on grass in disturbed areas under Duranta repens L. (Verbenaceae) at Colégio Estadual Jad Salomão (Anápolis, Goiás, Brazil), on soil in a grazing area and on soil covered by litterfall in stational semi-deciduous forest both in municipality of Rio Quente, Goiás, Brazil. Photographs and macroscopic features were described taken from fresh basidiomata. Color codes are from the Online Auction Color Chart (Kramer 2004). Freehand sections of the basidiomata were made, rehydrated in KOH 3%, dyed in Congo Red and mounted for microscopic analyses. Melzer’s reagent was used for testing amyloidity of the microstructures. Q_m refers to the quotient average of length/width ratio range from the basidiospores. All microscopic features were drawn after digital micrographs from the specimens examined. Voucher materials were deposited at HUEG Herbarium (Thiers, continuously updated). The geographic distribution for Phlebopus presented here was compiled from recent fieldwork, herbaria and literature data (Maia et al. 2015).

Phlebopus beniensis (Singer & Digilio) Heinem. & Rammeloo, Mycotaxon 15: 390 (1982). Figs. 1; 2 ≡ Phaeogyroporus beniensis Singer & Digilio, Lilloa 30: 150 (1960). Type: R. Singer B1613, Bolivia, Guayaramerím (LIL) (as cited by Heinemenn & Rammeloo 1982).

Figure 1
a-g. Phlebopus beniensis - a. fresh basidiomata; b. pileipellis; c. clamp connections from pileipellis; d. cheilocystidia; e. basidiospores; f. basidia; g. caulocystidia.

Figure 2
a-d. fresh basidiomata of Phlebopus beniensis - a. growing on grass in disturbed areas (arrows show signals of mycophagy); b. on soil covered by litterfall; c. on soil in a grazing area, with some insect larvae feeding on the basidiome; d. detail of mycophagy by insect larvae.

Pileus 80−100 mm diam., hemispheric at first to convex to plane convex when mature, slightly depressed in the center, smooth, slightly viscid in wet weather, light brown, caramel to sepia yellow colored (OAC 840, 838); straight margin, irregular, splitting when mature. Tubes 5−12 mm long centrally, yellow (OAC 895, 888) to yellow olive under pressure (OAC 887, 859), adnate to depressed; pores 2−3 per mm, rounded. Stipe 30−70 × 11−23 mm, central to slightly eccentric, subequal, tapering upwards, downwards to bulbous base, dark greysih brown (OAC 866, 868) yellowish near the apex, surface glabrous. Context pale yellow (OAC 899), unchanging when exposed. Spore print olive brown. Basidiospores 5.6-7.3 × 4.6-5 µm (Q_m = 1.40), short ellipsoid, yellow brown, inamyloid, guttulate, smooth, thick walled. Basidia 16.6-23 × 6-10 µm, clavate, thin walled, hyaline, guttulate, 4-sterigmate, 3−5 µm long. Pleurocystidia and cheilocystidia both with (15.5-)20.5−21.7 × (5-)7−10 µm, clavate to obclavate with obtuse tip, hyaline, inamyloid, smooth, thin walled. Pileipellis trichodermal, terminal elements 4.3−6.5 µm wide, round apex, hyaline, inamyloid, smooth, thin walled. Pileus trama parallel to subparallel, hyphae 2.5−10 µm wide, hyaline. Stipitipellis composed by clavate, fusiform to cylindrical caulocystidia, 3−13 µm, hyaline, inamyloid, thin walled. Stipe trama of vertically arranged hyphae, cylindrical, hyphae 4−9 µm wide, hyaline, inamyloid. Hymenophoral trama boletoid, gelatinized mediostratum with narrow hyphae 3−5(-5.3) µm wide, hyaline, inamyloid, oleiferous hyphae not observed; medium stratum with irregular to inflated hyphae 6−10 µm wide, divergent. Clamp connection present in all septa. (Figs. 1; 2).

Distribution in Brazil: Paraíba (Oliveira & Sousa 1996), Paraná (Watling & Meijer 1997) and Goiás (present study).

Worldwide distribution: Once that Phlebopus is a genus of tropical boletes, P. beniensis occurs in Argentina, Bolivia, Brazil, Colombia, Costa Rica, Ecuador, Martinique, Puerto Rico, Venezuela in the Neotropics and from Liberia in Africa (Heinemenn & Rammeloo 1982; Ovrebo 1983; Singer et al. 1983; Miller et al. 2000; Guzmán et al. 2007; Palacio et al. 2014).

Specimens examined: BRAZIL. GOIÁS: municipality of Anápolis, Colégio Estadual Jad Salomão, 16º19’10.14’’S, 48º57’55.98’’W, growing gregariously on grass in disturbed areas under Duranta repens L. (Verbenaceae), with some signals (Fig. 2a) of mycophagy (probably by insect, like shown in Fig. 2c,d), 12.XI.2014, F.J.S. Calaça FJSC48 (HUEG 10043). Municipality of Rio Quente, 17º46’S, 48°45’W, growing on soil covered by litterfall (Fig. 2b) in a stational semi-deciduous forest, in a particular area, 17º47’35’’S, 48º47’36’’W, 22.I.2008, S. Xavier-Santos SXS3549, SXS2215 and SXS2189. Growing on soil in a grazing area, with some insect larvae feeding on the basidiomes (Fig. 2c,d).

Additional specimens examined: BRAZIL. PARAÍBA: João Pessoa, UFPB/CCEN/DSE, Mata do Biotério, 7º8’18.9”S, 34º50’40.1”W, 7.II.2009, M.A. Neves MAN357 (ICN 184809); 7º8’18.5”S, 34º50’38.4”W, 11.III.2011, A.C. Magnago ACM 265, 267 (ICN 184911, 184912); 20.VI.2011, A.C. Magnago ACM 285 (ICN 184910).

Comments: These are the first records of Phlebopus beniensis for the Brazilian Cerrado, increasing the knowledge about fungi diversity in Brazil’s Central-West Region. Before this study, P. beniensis had been recorded only along the coastal Atlantic Forest (Oliveira & Sousa 1996; Watling & Meijer 1997). The current distribution in Brazil of P. beniensis and other Phlebopus species are shown on Table 1.

Table 1
Geographic distribution data of Phlebopus occurring in Brazil.

Species	Localities	References
Phlebopus beniensis	Paraíba (João Pessoa), Paraná (Paranaguá, Pontal do Paraná, Vera Cruz do Oeste), Goiás (Anápolis and Rio Quente, present study)	Oliveira & Sousa 1996; Watling & Meijer 1997
Phlebopus brasiliensis	Amazonas (Manaus)	Singer et al. 1983
Phlebopus braunii	Rio Grande do Sul (São Leopoldo, Vera Cruz), Santa Catarina (Itapiranga)	Putzke et al. 1994; Singer & Digilo 1960; Sulzbacher et al. 2013
Phlebopus harleyi	Paraíba (João Pessoa)	Oliveira & Sousa 1996
Phlebopus portentosus	Paraíba (João Pessoa)	Oliveira & Sousa 1996
Phlebopus tropicus	Rio Grande do Sul (São Leopoldo, Vera Cruz), Rio de Janeiro	Putzke et al. 1994; Rick 1960; Sulzbacher et al. 2013; Singer & Digilo 1960
Phlebopus sp.	Bahia (Paulo Afonso)	CEPEC-Fungi 2458
Phlebopus sp.	Pernambuco (Recife)	IPA 39030

Phlebopus beniensis is morphologically very similar to P. brasiliensis, overlapping in many features, and differing by a few subjective characteristic: the bluing oxidation of pileus and stipe context when exposed, which are more visible when the material is quite fresh and humid, however, depending on dryer weather conditions this characteristic can be not so evident, like the ones observed in the examined specimens as an unchanging reaction in the context. The size of the basidiomata is another differentiating characteristic: P. brasiliensis has pileus < 65 mm wide and P. beniensis usually larger when mature, reaching 130 mm wide. The cystidia in P. beniensis are more evident and numerous than in P. brasiliensis (Singer et al. 1983).

Singer et al. (1983) reported Phlebopus brasiliensis in the state of Paraíba, however, Oliveira & Sousa (1996) examined many collections of Phlebopus from the same area of Singer’s collections, and concluded that all these were misidentifications of P. beniensis. The species also differs from other Phlebopus found in Brazil for its wide, subgyrose to boletinoid pores, and larger basidiospores (8-9 × 6-7 µm) in P. tropicus; the darker colors of the basidiomes and most of all for its basidiospores larger than 7.5 µm in P. portentosus; stipe finely ornamented and globose to subglobose badiospores in P. harleyi; and pileus surface with olive tones and larger basidiospores [6.5-9.5(-11) × 5-7 µm] in P. braunii (Singer et al. 1983; Singer & Digilo 1960; Oliveira & Sousa 1996; Watling & Meijer 1997; Baroni et al. 2015).

Phlebopus beniensis is regarded as a species that develops in moister tropical forests (Singer et al. 1983), but some works have recorded this species in many locations in Neotropical Regions and in Africa (Singer & Digilio 1960; Heinemenn & Rammeloo 1982; Guzmán et al. 2007; Palacio et al. 2014), like dry, semi-deciduous, seasonal subtropical forests in montane or sub-montane areas. Recently, Palacio et al. (2014) recorded P. beniensis in a tropical dry forest, in the northeast region of Colombia. As shown in Table 1, species of this genus seem to be more generalists with regard to its habitat since it has already occurred in Brazil, in tropical Atlantic and Amazonian Forests and seasonal savanna (Cerrado), as indicated in the present study. Moreover, as shown by our data, P. beniensis can be found in urban areas, associated or not to distinct plants species.

An interesting aspect of our work, is the mycophagy of basidiomes by insect larvae (probably Diptera) (Fig. 2a,c,d). The mycophagy by small animals in Brazil is poorly known, with some sparse records. Recently, Trierveiler-Pereira et al. (2016) reported mycophagy in Brazilian Amazon Forest and Blumenau, Santa Catarina, Brazil [Ascopolyporus spp. by black capped squirrel monkey (Saimiri boliviensis I. Geoffroy & Blainville 1834) and Itajahya galericulata Möller by Azara’s agouti (Dasyprocta azarae Lichtenstein 1823)] and Sulzbacher et al. (2015) reported mycophagy of Descomyces albus (Berk.) Bougher & Castellano by the invertebrate Balloniscus sellowii Brandt 1833 (Isopoda).

Once fungi are a rich source of nutrients (Fogel & Trappe 1978) for these animals, fungi can contribute to structure food webs, mainly to insect community (Yamashita et al. 2015), being a key components to maintenance of ecosystems. Our results highlight the importance of studies involving these ecological interactions between mycophagous invertebrates and fungi.

Although molecular data has not been addressed in this work, it should be investigated to better understand the relationship among species within Phlebopus, especially with the inclusion of Neotropic specimens, since morphological features which distinguish the species are generally subjective and confusing. As pointed out by Maia et al. (2015), it is still necessary to encourage new collection expeditions in Brazilian forests, especially in savanna areas in the Central-West Region in order to increase our knowledge about the mycodiversity for Brazil, as for the Neotropics, as well as including molecular data of Brazilian specimens in phylogenies.

• Editor de área: Dr. Anibal de Carvalho Junior

Acknowledgements

The authors wish to thank Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) for their financial support. ACM, FJSC and RLMA wish to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their fellowships. The authors also wish to thank the anonymous reviewers for their comments and suggestions, which greatly improved the quality of the manuscript.

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Publication Dates

• Publication in this collection
  Apr-Jun 2018

History

• Received
  11 Feb 2016
• Accepted
  23 May 2017