Entoloma Virescens

n Entoloma virescens

istributio Caatinga biome, Ceará, (Sacc.) Brazil E. Horak ex Courtec., 1986 D (Agaricales: Entolomataceae): The first record for the *

raphic Maria Helena Alves and Cristiano Coelho do Nascimento g eo

G Universidade Federal do Piauí, Campus Parnaíba. Avenida São Sebastião, 2819. CEP 64202-020. Parnaíba, PI, Brazil. n * Corresponding author. E-mail: [email protected] o

otes N

Abstract: Entoloma virescens

, a rare mushroom with deep blue coloring and cuboid spores, is recorded for the first time in the Caatinga biome in Brazil. The relevance of this finding is that such area is characterized by an atypical environment for the occurrence of species normally considered from temperate and humid tropical regions. The record is fully described and illustrated. Also, a brief analysis of taxonomical features and geographical distribution of the taxon are included.

The Kotl. and Pouzar family Entolomataceae (Basidiomycota, Agaricales) a.s.l.; it is irrigated by a number of water courses and is to arctic habitats is (Largent very rich 1994; in species, Noordeloos comprising and Gates over April.characterized by warm sub-humid climate with a rainy 2007;1500 recognizedNoordeloos taxa and that Hausknecht occur worldwide 2007; Noordeloos from tropical and season occurring between the months of January and Gates 2009). According to Co-David et al. (2009) semiaridIn terms climate, of physiognomic within which attributes,the highest the percentage region is anof Clitopilus area of vegetation types associated with the warm tropical Rabenh.) P. Kumm., Rhodocybe Maire and Entoloma this family (Fr.) Figueiredo 1986; Fernandes and traditionallyP. Kumm. sensu contains lato. three Though main these genera: authors commented (Fr. ex Bezerracoverage 1999) is represented. by the open shrubby Caatinga and denseField shrubby collections Caatinga took ( place in March 2011. Specimens were collected, documented and preserved using secondthat the largest latter genus genus is within a monophyletic the Agaricales. group that has high standard methods (Largent et al. 1986). The material diversityThe genus in morphological Entoloma features and is considered the a worldwide scale (Noordeloos 1980, 1981; Manimohan et al. 2006; Noordelooshas andbeen Gatesstudied 2007; by Noordeloos Noordeloos on was photographed in the field using a digital camera and and Hausknecht 2007; Noordeloos and Gates 2009; extensive notes on the basidioma were made before drying. Noordeloos and Morozova 2010). However, data are still MicroscopicAll measurements analysis of and the colors material reported was performed for microscopic using an Olympus BX41 microscope. South America, in Tolacking date, on few occurrence species have and been distribution reported of many species in +features blue cotton, were made 3% KOH from or dried Melzer’s material reagent. rehydrated At least, in Entoloma are particular recognized from (Putzke the Brazilian and Putzke territory. 2000). 2596% measurements ethanol followed were by made distilled of water, each microstructure. distilled water and only about 56 taxa of Agaricales are view and the apiculus was not considered. Spore statistics In the Northeast region, this number drops dramatically Measurements of cuboid spores were made in profile m) of basidiospore lengths since the majority of taxonomicEntoloma studies have been on described for and widths ± standard deviation measured for n objects; theconcentrated Brazilian Northeast in the south (Singer and southeast1965; 1973; of Horak the country. 1977; include arithmetic means (x 1982;Hence, Wartchow very few taxa 2006). of indicated as a range variation in n objects measured; the Entoloma virescens, meanquotient of E-values of basidiospore (Q) ± standard length deviations. by spore The width sample (E) a rare mushroom with strong blue color and cuboid spores,The which present is study deals with biome of Brazil. The latter area size (n) = total number of basidiospores measured (x) environment forrecorded the occurrence for the first of time the species,in the Caatinga which, 2011).divided by the number of basidiomata studied (y), as is considered an atypical shownDigitized in the microphotographs formula n = x/y were (Largent taken and using Abell-Davis a camera forested areas of temperate and humid tropical regions. attached to a compound light microscope. The material to theThe best specimen of our knowledge, under consideration has only been was recorded collected in in the area of Bom Gosto, features with previous studies of Romagnesi (1941), wasHorak identified (1976), Pegler by comparing (1986), Noordeloos macro and and microscopicHausknecht Fortaleza.during forays The area has an average elevationPacujá municipality, of 160 m (2007) and Largent and Abell-Davis (2011). In addition, Ceará state, approximately 248 km from the capital

577 Alves and Nascimento | Entoloma virescens in the Caatinga biome

__ __ et al. (2008) was followed. The Basidiospores 9.75 m = 11.72 ± documented material has been deposited at the Herbarium __1.16 (-1.65); Q = 1.06 ± 0.136; Grazielathe terminology Barroso of (TEPB) Kirk of the Universidade Federal do 13.75 x 9.75 12.5 µm (x Piauí (UFPI). 1.16 x 11.29 ± 0.84; E = 0.90 Description of Material Collected - Entoloma virescens n = 30/2), cuboid, with four regular to irregularBasidia angles32__50 in× 14profile__ or side views, slightly yellowish in 3% KOH, with Agaricus virescens Berk. and M.A. Curtis, Proc. Amer. granular,a slightly withthickened, brownish stramineous to stramineous wall. vacuolar contents. Acad.(Sacc.) Arts E. Horak 4: 116. ex 1860, Courtec., nom. Mycotaxon Illegit. (non 27: Schaeff. 131. 1986. 1774); (= Lamelar18 µm, edge4-spored, clavate to subcylindrical, thin-walled, = Inocephalus virescens (Sacc.) Largent and Abell-Davis, present. Pseudocystidia of tramal origin, sinuous, Inopilus virescens (Sacc.) constricted-lobed with, rounded pseudocystidia , thin-walled, and cheilocystidia present Pegler, Kew Bull. Add. Ser. 12: 268.1986; = Leptonia at the edges and sides of the lamellae, 6__9.2 µmslightly diam. Mycotaxonvirescens 116: 232. 2011; = 1887). Figure 1 and 2. Cheilocystidia 28__55.5 × 11__apex Pileus 3.0__4.5 cm diam., 3.5__ Sacc., Syll. Fung. 4: 714. thin-walled. Hymenophoral trama16.75 regular,µm, cylindro-clavate, composed of 4.5 cm high, conic-convex yellowish in 3% KOH with golden brown vacuolar contents,__12.5 with a papillate umbo, then occasionally depressed at µm diam., with brownish vacuolar contents; abundant center; slightly hygrophanous, translucently striate when cylindrical, hyaline,Subhymenial thin-walled, layer inflated large, hyphae, 62.5__ 100 6 µm moist, becoming fibrillose near the wavy margin; surface at Pileipellis a cutis greenishfirst deep in blue place becoming when pressed, greenish-blue cut or tobruised. entirely Lamellae grayish- vascular hyphae. __13.5 µm diam., green when mature or drying, and staining yellow-blue wide,with abundant with abundant stramineous vascular intracellular hyphae. granules. Clamp ofconnections hyaline, cylindrical, common repent in all hyphae, tissues. 5.75Habit and habitat: adnexed, moderately spaced, with lamellulae of three lengths, ventricose, dullStipe blue 4.5 becoming__5.5 cm × a5 yellowish-green__7 mm, central, or greenish-blue on exposure or handling; margin smooth season.Solitary Material or disperse examined growing: BRAZIL on the. Ceará soil in State shady: Pacujá, area, tohollow slightly, glabrous, serrated. ; concolorous with the collected in open shrubby Caatinga zone during the rainy confluentpileus, with with white the basal pileus, fragile,. Context cylindrical, thin, flattened,dull blue slightly striated Community of Bom Gosto, 16-III-2011, collectors: Alves, mycelium Odor distinct but M. H and Nascimento,E. C.virescens C. 072/11 can (TEPB) (02°55’49.5” S; becoming darkTaste green unknown. on exposure or drying, consisting following41°40’34.1” combination W; Elev. 140 of m characters:a.s.l.). basidioma a of hyaline, thin-walled, inflated hyphae. Morphologically be recognized by the unidentifiable. t first A B

C D

Figure 1. Entoloma virescens. A and B: Basidioma; C: Basidium and basidioles; D: Basidiospores. Bars: A and B = 10 mm; C and D = 10 µm. Photos A and B: Maria Helena Alves; C and D: Cristiano Coelho do Nascimento.

578 Alves and Nascimento | Entoloma virescens in the Caatinga biome

the E. holocyaneum (Romagn.) Noordel. and Co-David. A Horakbasionym (1976) of considered the new combination R. holocyaneus together with C E. hochstetteri (Reichardt) G. Stev. as well as E. aeruginosum

A. virescens from the Bonin Islands, proposing a new Hiroë (species found in Japan) as being conspecific with B combination: E. virescens (Berk. and M.A Curt.) E. Horak, but Coutecuisse (1986) validated the combination. However, without referring the full citation of the basionym. Later, the epithet ‘virescens (LargentBerkeley and CurtisAbell-Davis authority 2011). is an Romagnesi illegitimate (1941), name since who ’was already used by Schaffer in 1774 E D emphasizes that A. virescens has a conical pileus, differing studied the type collection preserved at Kew Herbarium

fromHongo the center-depressed (1990), differing frompileus Horak that is(1976), specified prefers in the to considerdiagnosis E.of hochstetteriBerkeley and and Curtis. E. aeruginosum as separate due to the differences in the spore size and shape of the Entoloma aeruginosum has spores measuringtaxa, 10.5__ __ F pseudocystidia. E. hochstetteri basidospores measure 12.5__5.512.5 × 12 __ x 9.5 12 µm and pseudocystidia subcylindricalsubfusoid to subclavate. to clavate; whileIn these aspects, our specimens of E. virescens 15 µm and presents pseudocystidia measuring 9.75__ __12.5 µm and sinuous collectedconstricted-lobed in Pacujá/CE,, differing Brazil, in have relation spores to Figure 2. Entoloma virescens: A, basidioma; B, spores; C, basidia; D, 13.75 x 9.75. and 10 µm (microscopic characters). pseudocystidia, pseudocystidia; E, cheilocystidia; F, pileipellis. Bars = 10 mm (basidioma) E.the aeruginosum two taxa mentioned, found some above morpho-anatomical features Courtecuisse (1986), who examined two collectionsA. virescens of deep blue becoming greenish-blue to entirely grayish- blue greenish in places when pressed, cut or bruised; fordiffering R. holocyaneus from those. The observed author in emphasized the analysis simple of cuboid green when mature or drying, and staining yellow- pileus sporesholotype of andthe the descriptions A. virescens made by Romagnesi (1941) shape of the spores of E. aeruginosum, also highlighting conico-convex with a papillate umbo; strictly type in contrast to the complex R. 4-angled basidiospores; cheilocystidia cylindro-clavate; abundant and clamp connections common in all tissues. holocyaneus and E. aeruginosum. In this manner, it seems pseudocystidia of tramal origin; vascular hyphae very Entoloma with differencesthat the correspondence in the subhymenial of E. aeruginosum layer with between A. virescens cuboid spores published and R. holocyaneus ; however, CurtisThis described species it was for Bonin the first Island, record however, of these authors in 1857, when Berkeley and. is not absolutely perfect Courtecuisse (1986), in possession of restricted taxonomic did not recognize yet the peculiar shape of the spores Paris, discovered the particular data,Pegler corroborated (1986) described the terms Inopilus proposed virescens by Horak (Berk. (1976), and Only 80 years later, Romagnesi (1941), studying parts of cuboid spores (Horak 1976). Curt.)highlighting Pegler, the comb. inaccuracy inval. forof some the central synonymies. province of Sri abovethe collection mentioned, type Romagnesi kept in (1941) Examining the publication the “Les Rhodophylles de set of features lead Lanka as a distinct species in young In this stages new by combination, virtue of the Madagascar”, and using the key contained in this work, to the species Rhodophyllus holocyaneus Romagn. in the uniformly blueA. coloration virescens of the basidioma withE. virescensthe blue of the material examined in this study Psittacine section, which is also observed in the material tintsunder disappearing . Pegler at maturity. (1986) recongnized R. chloroconus of Noordeloos and Hausknecht (2007) from La Réunion. Pegler defined as basionym, putting The referred species greenish- relatedsynonymy to I. virescens blue color of the basidioma, conical pileus, cuboid spores Romagn. and Gilles from Ivory Coast as a species closely is characterized by the facets. Inopilus virescens, although was the also first recorded species for lacks South the vascular blue color, and the cuboid spores; being have described strongly as depressed a species and abundant pseudocystidia originated from the tramal with cuboid spores [10__ __11µm], quadratic in hyphae that reach the hymenial layer. The latter America, lamellae by Pegler deep (1997) blue; basidioma at feature is strongly evident in the material examined from E. virescens blue becoming 12(-14) x 9 40__120 sensuPacujá/CE, lato Brazil, differing from the material described profile first pale to deep by Noordeloos and Hausknecht (2007) as tramal origin is not cited. pigment. yellowish green; pleurocystidia , in which the presence of pseudocystidia from Co-David et al. µm long, cylindrical to ventricose, with brown vascular, Pegler Considering the taxonomic (2009), which deal with the (1997) cited the occurrence of and nomenclatural changes presented by Entolomataceae; R. holocyaneus becomes howeverIn the threcord for Campos do Jordão/SP, Brazil phylogenetic reconstruction robust pleurocystidia; of the family is feature was not reported by Pegler (1986)579 Alves and Nascimento | Entoloma virescens in the Caatinga biome for I. virescens and was not observed in the material Abell-Davis 2011). Therefore, we consider that molecular recorded for the Brazilian Northeast. With regard to spore of morphological characters helping to establish the __ __12.5 µm) are closer to speciessequence limits analyses and its would geographical help to interpret range. the significance dimensions, values measured in__ 12(-14) the material × 9__11 examined µm) for from Pacujá/CE (9.75 13.75 x 10 those(8.5__11 cited × 8 by__ Pegler (1997) (10 Acknowledgments: Biodiversidade do Semiárido – PPBio grants from Conselho Nacional Campos do Jordão/SP, differing from the basidiospores This study was partially supported by the program those mentioned10.5 above. µm) observed by Pegler (1986) in the Federal do Piauí – UFPI. material from Sri Lanka that are slightly smaller than de Desenvolvimento Científico e Tecnológico – CNPq and Universidade Literature Cited from Northeastern Queensland and New South Wales Co-David, D., D. Langeveld, and M.E. Noordeloos. 2009. Molecular (Australia),Based on Largent recent and examination Abell-Davis of (2011) several proposed collections the Entolomataceae. Persoonia 23(4): 147-176. new combination, Inocephalus virescens, for E. virescens. Courtecuisse,phylogeny and R. spore 1986. evolution Notes deof nomenclature concernant les Our collections from the Brazilian Northeast, for the most part, match the description of I. virescens; however, Mycotaxon 27: 127-145. Fernandes,hyménmycètes A. and IV. Bezerra, Sur quelques P. 1990. epithets Estudo spécifiques fitogeográfico preoccupies do Brasil 3.. the I. virescens Figueiredo, M.A. 1997. A cobertura vegetal do Ceará (Unidades sensu 4-5-angled Largent and basidiospores Abell-Davis from and our cylindro-clavate material, which Fortaleza: StylusIn Comunicações.: Atlas do Ceará 205. Fortaleza: p. IPLANCE, p. 28-29. 65p. pileocystidia and caulocystidia differentiate Mapas coloridos – Escala 1:1.500.000. Fitoecológicas). Reports of the Tottori Mycological Institute 28: 129-134. thatlacks the cylindro-clavate correspondence pileocystidia of our material and caulocystidia with I. virescens and HorakHongo, E. T. 1976. 1990. On New cuboids and noteworthy pored species agarics of Entoloma. from New Sydowia Zealand. 28(1-6): all basidiospores are strictly 4-angled. Therefore, it seems 171-236. sensu Largent and Abell-Davis is not well supported. In this Horak, E. 1977. Additions to “On cuboid-spored species of Entoloma Sydowia 29(1-6): 289-299. that E. virescens sensu Noordeloos and Hausknecht are Horak, E. 1982. Entoloma in South America. II. Sydowia 35: 75-99. ”. manner, based on morphological similarity, we consider Kirk, P.M., P.F. Cannon, J.C. David and J.A. Stalpers . 2008. Ainsworth and Bisby’s dictionary of fungi. 10. ed. Wallingford: CABI Publishing. 771 Regarding the distribution, Horak (1976) considered p. more closely related with our findings. Largent, D.L., D. Johnson and R. Watling. 1986. How to identify mushrooms to genus III: microscopic features. California: Mad River Press. 273p. the center of dispersion for Entoloma species with cuboid Largent, D.L. 1994. Entolomatoid fungi of the Pacific Northwest and the region between Malaysia and New Zealand as being Alaska. Eureka: Mad River Press Incorporated. 516 p. the African continent. The author also showed that these Largent, D.L and S.E. Abell-Davis. 2011. Observations on Inocephalus spores, assuming the occurrence of numerous taxa for virescens comb. nov. and Alboleptonia stylophora from northeastern Queensland. Mycotaxon 116: 231-245. zones.species occur mainly in the tropical and subtropical range, genus Entoloma (Basidiomycetes, Agaricales) in Kerala State, India. with many species also occurring in forests in temperate Manimohan,Persoonia P., 19(1): M.E. Noordeloos45-93. and A.M. Dhanya. 2006. Studies on the With respect to E. virescens in the wide sense, it has Noordeloos, M.E. 1980. Entoloma subgenus Nolanea in the Netherlands

Europe. Persoonia 10(4): 427-534. been characterized as a widely distributed species, and adjacent regions with a reconnaissance of its remaining taxa in Entoloma sensu lato (Agaricales). Persoonia 11(2): 121-151. Guineabeing reported and Sri by Lanka. Horak Pegler (1976) (1986) for Bonin added Island collections (type), Noordeloos, M.E. M.E. 1981. and A. Introduction Hausknecht. to 2007. the taxonomy The genus of theEntoloma genus New Zealand, Japan, Malaysia, Madagascar, Papua New (Basidiomycetes, Agaricales Fungal Diversity 27(1): 111-144. Noordeloos, M.E. and G.M. Gates.) 2007. of theStudies Mascarenes in the genus and Entoloma Seychelles. of andfrom subtropical Zambia and forests. Thailand. In South In all America, of these E . reportsvirescens the is Tasmania I. Persoonia 19(2): 157-226. species is cited occurring mainly in the soil of tropical Entoloma in Tasmania II. Cryptogamie, Mycologie 30(2): 107-140. Noordeloos, M.E. and G.M. Gates. 2009. Preliminary studies in the genus cited by Pegler (1997) for the municipality of Campos do Entoloma Jordão/SP, Brazil, which is characterized by altitudinal Noordeloos,Mycotaxon M.E.112(1-6): and 231-255. O.V. Morozova. 2010. New and noteworthy Pegler, D.N. 1986. species Agaric from Flora the Primorsky of Sri Lanka Territory, Russian Far East. tropicalThe climate record and herein by vegetation presented constituting registers E. of virescensa typical field and forest mosaic. Pegler, D.N. 1997. The agarics of São Paulo, Brazil. London: Her Majesty’s StationeryGardens, Kew Office.. 68 519p. p. for the first time for the Caatinga biome in the Brazilian Putzke, J. and M.T.L. Putzke. 2000. Revisão da família. London: Entolomataceae Royal Botanic (Basidiomycota, Agaricales Northeast. Such area represents an atypical environment lista de espécies. Caderno de Pesquisa Série Botânica 12(1-2): 29-47. according to physiognomic aspects of the environments ) no Brasil. I. Chaves de Prodrome identificação à une e mentioned thus far for the taxon, showing that the species flore mycologique de Madagascar 2(2): 1-164. without showing large morphological changes. Singer,Romagnesi, R. 1965. H. 1941. Interesting Les Rhodophylles and new agarics de Madagascar. from Brazil. Atas do Instituto is widelyWe conclude, distributed as and did able Noordeloos to occur in different and Hausknecht habitats de Micologia da Universidade do Recife 2: 15-47. (2007) for their material, Singer, R. 1973. Diagnoses Fungorum Novorum Agaricalium III. Beihefte zur Sydowia 7: 1-106. basidiospores and blue-colored basidiomata from Wartchow, F. 2006. The Neotropical Entoloma dragonosporum (Agaricales, the that the taxon withE. virescens cuboid Basidiomycota): new record from Northeast Brazil. Biociências 14(1): sensu lato 93-94. Brazilian Northeast fits the concept of E. virescens and occurs within a very wide geographical diverserange. However, morphological the clarification characters and alone elucidation have not of been the : December 2011 complex is very complicated when highly Received : June 2012 (Largent and Accepted: May 2012 : Matias Cafaro enough to establish specific limits due to the absence or Published online Editorial responsibility poor condition of many holotype collections 580