MYCOTAXON. Volume 104, pp April June 2008

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1 MYCOTAXON Volume 104, pp April June 2008 Inocybe martinica: a new record from South America and type studies of allied species from the Lesser Antilles Felipe Wartchow, Leonor C. Maia & Maria A.Q. Cavalcanti fwartchow@yahoo.com.br Universidade Federal de Pernambuco, Depto. de Micologia Av. Prof. Nelson Chaves, s/nº., CEP: , Recife, PE, Brazil Abstract Inocybe martinica is recorded for the first time from South America. Type studies of three species described by Pegler from the Lesser Antilles, I. antillana, I. crassicystidiata and I. martinica, and a key for them are provided for comparison. Key words Agaricales, Inocybaceae, neotropics, taxonomy Introduction Inocybe (Fr.) Fr. is an ectomycorrhizal genus of brown spored mushrooms belonging to the family Inocybaceae Jülich, order Agaricales Clements (Matheny 2005, Matheny & Bougher 2006). In Brazil, few species have been reported. In the southern region, Singer (1953), Rick (1961) and Cortez & Coelho (2005) report I. curvipes P. Karst., I. hyperythra Rick and I. violaceolamellata Rick from the State of Rio Grande do Sul; Stijve & de Meijer (1993) and de Meijer (2001, 2006) listed I. curvipes, I. cf. australiensis Cleland & Cheel, I. aff. cingulatipes (Corner & E. Horak) Garrido, I. aff. conspicuispora Buyck & Eyssart., I. aff. crassicystidiata Pegler, I. aff. incognita (E. Horak) Garrido, I. aff. pahangi (Corner & E. Horak) Garrido and I. aff. xerophytica Pegler from Paraná State; and Giachini et al. (2000) cited I. australiensis from Santa Catarina State. In the northern region only one species was recorded, I. amazoniensis Singer & I.J. Araujo, from the State of Amazonas (Singer et al. 1983). We describe here an interesting species collected in the Atlantic Forest from the State of Pernambuco, Northeast Brazil. For a better understanding a comparison has been made with the type specimens of Antillean Inocybe spp. having stipes that are covered in metuloids. Material and methods Basidiomata were collected in forest fragments located at the Usina São José (7º50 20 S 35º00 10 W), Municipality of Igarassu, Pernambuco State, Northeast

2 44... Wartchow, Maia & Cavalcanti Brazil. The area comprises approximately ha, of which 8000 ha are forest fragments with different conservation stages (SECTMA 2001). The usual methodology for analysis of agaric fungi was followed (Singer 1986). The quotient of the length/width of basidiospores is presented as the Q value. Color naming and codes follow Maerz & Paul (1950). The specimens are deposited at Herbarium URM, Department of Mycology, Universidade Federal de Pernambuco, Recife. Taxonomy Inocybe martinica Pegler, Kew Bull. Add. Ser 9: Figs. 1-5 Pileus mm, convex sub-conical then plane with a pronounced and obtuse umbo; color of surface gold yellowish brown (between M&P 11J6 Honey-sweet and 11J7 Inca Gold ), slightly pallid in young specimens, with concolorous or slightly darker (at least in dry specimens) small fibrils, appearing distinctly fibrillose-squamulose in dried specimens, except for the somewhat glabrous centre in the larger basidiomata; margin entire when young, turning short striate in mature specimens; context thin, fleshy. Lamellae adnexed, subdistant, pale brown (M&P 15L10 Whippet ) when mature, edges slightly fimbriate, with some lamellulae. Stipe mm, central, cylindrical even, without a marginate bulb, base not at all bulbous, cortina absent, surface pale cream color then beige (M&P 11I5 Chamois ), pruinose the entire length of the stipe surface, turning more evident in dried state; context fleshy. Basidiospores (9 ) ( 12) ( 8) µm, average µm, Q = (1.25 ) ( 1.82), average Q = 1.49, elongate ellipsoid with a slight suprahilar depression in side view, with prominent subconical to more frequently obtuse nodules, brownish or ochraceous brown in KOH. Basidia µm, clavate, with four sterigmata, hyaline. Pleurocystidia µm, metuloid, fusiform to narrowly lageniform with broadly obtuse apex; irregularly thickened wall µm thick at middle then abruptly ranging up to 5 µm near the apex; hyaline with colorless wall, strongly incrusted with crystals at the apices. Cheilocystidia similar to pleurocystidia. Paracystidia difficult to distinguish. Caulocystidia metuloid in dense fasciculate tufts over entire stipe length, µm, utriform to sublageniform with broadly obtuse apex, uniformly thick walled up to 2 µm, hyaline with colorless wall, without or somewhat with slight incrustation at apex. Paracaulocystidia present, mixed with caulocystidia. Pileipellis a cutis of radially arranged filamentous hyphae ranging to 7 15 µm, distinctly incrusted, thin walled, yellowish brown. Clamp connections present. Lamellar trama regular. Habitat: sub-gregarious and scattered on soil near members of Clusiaceae, Violaceae and Annonaceae (Maria Rodal, pers. commun.) in a very wet area of a tropical forest fragment.

3 Type studies: Inocybe martinica & allied species Figures 1-5. Inocybe martinica. 1. Basidioma. 2. Basidium. 3. Basidiospores. 4. Caulocystidia 5. Pleurocystidia. Scale bar 10 mm for basidioma and 10 µm for microstructures.

4 46... Wartchow, Maia & Cavalcanti Material examined: BRAZIL. Pernambuco, Igarassu, Usina São José ( Mata de Piedade ), 07-VI-2005, F. Wartchow 09/2005 (URM 78851). Remarks: The absence of a cortina, the pruinose stipe, presence of metuloids and the nodulose basidiospores place Inocybe martinica in section Marginatae Kühner, a group that Singer (1986) considered well defined. However, Matheny et al. (2002) and Matheny (2005) showed that sect. Marginatae is not a monophyletic group. Inocybe martinica was originally described from Martinique in the Lesser Antilles with a pale yellowish brown pileus, thick-walled cystidia and pileipellis covered by filamentous hyphae 3-4 µm thick without incrustations. It has similar features with our collection mainly in the size of the basidiospores, viz µm [average µm, average Q = 1.46], and the shape of cystidia (Pegler 1983). Direct examination of the holotype of I. martinica [MARTINIQUE. Le Chapelle, Anse a l Ane, , J.P. Fiard 756A (K)] reveals several similarities with our material: in addition to size and shape of the basidiospores (8 )9 11 (5 )5.5 7 µm [average µm, Q = (1.35 ) ( 1.81), average Q = 1.59], the type specimen shows the filamentous hyphae in the pileipellis (as described by Pegler) also mixed with several incrusted hyphae 8-12 (18) µm as observed in the Brazilian collection; in the dried specimens, the pileus surface is very distinctly fibrillose-squamulose. This discrepancy in the description of the pileipellis as given by Pegler in the protologue (1983: 539) may be accepted. However, Pegler equivocally uses this information to differentiate I. martinica from I. crassicystidiata (see below). Generally, the differentiation of the pileipellis is not sufficiently informative and can vary on where the section is made and the stage of development of the particular specimen (Matheny pers. corr.). Inocybe crassicystidiata, which was described with radially arranged brown incrusted pileipellis hyphae, differs from I. martinica in its ochraceous ( Ochraceous-Tawny ) pileus, shorter basidiospores [ µm, average µm and average Q = 1.30], and smaller cystidia having walls up to 5 µm thick (Pegler 1983). Examination of the type and an additional collection of I. crassicystidiata [MARTINIQUE. Point Jean Claude, , J.P. Fiard 850 (K Holotype); La Caravelle, , J.P. Fiard 851 (K)] do not agree with the description: several cystidia have metuloids with walls 2-4 µm thick and then somewhat irregularly thickening to µm, mostly near the apex, like the Brazilian collection of I. martinica. However the distinctly smaller basidiospores [7 9( 10) (4.5 ) ( 7) µm, average µm, Q = (1.23 ) ( 1.77) average Q = 1.44] and a dried pileus surface that is less fibrillose-squamulose

5 Type studies: Inocybe martinica & allied species are good characters helpful in separating I. martinica from I. crassicystidiata. Pegler (1983) described a third Antillean species from Martinique, I. antillana Pegler, which he noted as having a rimose chestnut brown pileus with an underlying ochraceous context and metuloids with thinner (3 µm) walls than those found in I. martinica and I. crassicystidiata. Examination of the type [MARTINIQUE. Le Chapelle, Anse a l Ane, , J.P. Fiard 746A (K Holotype)] shows basidiospores [(7 )7.5 9( 10) (5 ) ( 7) µm, average µm, Q = (1.36 ) ( 1.80) average Q = 1.49] and metuloids having walls up to 4.5 µm thick. The rimose pileus cited in the original description is not sufficiently distinct in the exsiccatum. There are other species with a pruinose stipe and metuloid caulocystidia known in tropical America. I. matrisdei Singer from the Bolivian Amazon is distinguished by a reddish-grayish brown pileus, smaller basidiospores [ µm], and distinctly marginate stipe bulb (Singer 1961, Singer et al. 1983). I. tequendamae Singer from Colombia and I. aff. angustifolia (Corner & E. Horak) Garrido and I. neotropicalis Singer from Costa Rica are associated with Quercus (Singer 1961, 1963; Singer et al. 1983). In summary, I. martinica differs from the other two Antillean species by having a yellowish brown and distinctly fibrillose-squamulose pileus with squamules that persist in dried specimens and more elongated basidiospores. Inocybe crassicystidiata and I. antillana share a similar basidiospore size, but differ in the color and texture of the pileus surface. In our estimation, the thickness of cystidial walls is not sufficiently informative for species differentiation. African members of Inocybe with nodulose basidiospores are quite different than I. martinica. Heim (1968) described I. sclerotiicola R. Heim & Gilles from Gabon, and Buyck & Eyssartier (1999) described two new species, I. conspicuispora and I. glaucodisca Byuck & Eyssart. However, they differ in several aspects (e.g. color of pileus, size and shape and number of nodules on the basidiospores, not to mention their distant habitats). Other species of Inocybe are known in the neotropics: I. hyperythra from Rio Grande do Sul State, South Brazil and I. lasseri Dennis from Trinidad have isodiametric basidiospores with crested protuberances; both are members of sect. Calosporae (Dennis 1953, Singer 1953, Singer et al. 1983), although this has not been demonstrated using molecular evidence (Matheny 2005), and the stipe of I. amazoniensis and I. epidendron Matheny et al. lack metuloid caulocystidia (Singer et al. 1983, Matheny et al. 2003). Mycorrhizal associations of I. martinica were not observed for our collections; in the study area, however, trees of Caesalpiniaceae, Euphorbiaceae, Mimosaceae, Myrtaceae and Nyctaginaceae occur (Silva & Andrade 2005), which are potentially ectomycorrhizal (Smith & Read 1997).

6 48... Wartchow, Maia & Cavalcanti Artificial key for Inocybe species with nodulose basidiospores and an even stipe covered with metuloid caulocystidia from Lesser Antilles and northern Brazil: 1 Pileus dark chestnut brown, distinctly rimose, splitting to show an underlying ochraceous context I. antillana 1 Pileus yellowish brown to ochraceous, fibrillose-squamulose Pileus yellowish brown, surface distinctly squamulose (at least in dried state); basidiospores average µm I. martinica 2 Pileus ochraceous, only slightly fibrillose (in dried state); basidiospores average µm I. crassicystidiata Acknowledgments The authors thank Dr. Roy Watling and Dr. P. Brandon Matheny for critically reviewing the manuscript, Dr. Vagner G. Cortez for preparation of the plate, Kew Herbarium for loan of the type specimens of Inocybe used in this study and Dr. Maria Jesus N. Rodal for providing tree family names. This is a contribution to the project Sustainability of remnants of the Atlantic rainforest in Pernambuco and its implications for conservation local development, a Brazilian-German scientific cooperation within the program Science and Technology for the Atlantic Rainforest funded by CNPq (590039/2006-7) and BMBF (01 LB 0203 A1), permitted and logistically supported by Usina São José S. A/Grupo Cavalcanti Petribú. CNPq is also acknowledged for providing grants to L.C. Maia (PP-Proc /2005-4) and F. Wartchow (PROTAX/MCT /05-9). This project was supported by CNPq (Proc /02-5). References Buyck B, Eyssartier G Two new species of Inocybe (Cortinariaceae) from African woodland. Kew Bull. 54: Cortez VG, Coelho G Additions to the mycobiota (Agaricales, Basidiomycetes) of Rio Grande do Sul, Brazil. Iheringia 60: Dennis RWG Les Agaricales de l Île de Trinité. Bull. Soc. Mycol. Fr. 69: Giachini AJ, Oliveira VL, Castellano MA, Trappe JM Ectomycorrhizal fungi in Eucalyptus and Pinus plantations in southern Brazil. Mycologia 92: Heim R Breves diagnoses latinae novitatum genericarum specificarumque nuper descriptarum. Cinquième série. Rev. Mycol. 33: Maerz AJ, Paul MR A Dictionary of Color. 2nd ed., McGraw-Hill Book Company, Inc., New York. Matheny PB Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe, Agaricales). Mol. Phylogen. Evol. 35: Matheny PB, Bougher NL The new genus Auritella from Africa and Australia (Inocybaceae, Agaricales): molecular systematics, taxonomy and historical biogeography. Mycol. Progress 5: Matheny PB, Liu YJ, Ammirati JF, Hall BD Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am. J. Bot. 89: Matheny PB, Aime MC, Henkel TW New species of Inocybe from Dicymbe forests of Guyana. Mycol. Res. 107:

7 Type studies: Inocybe martinica & allied species de Meijer AAR Mycological work in the Brazilian state of Paraná. Nova Hedwigia 72: de Meijer AAR A preliminary list of the macromycetes from the Brazilian State of Paraná. Bol. Mus. Bot. Municipal 68: Pegler DN Agaric flora of Lesser Antilles. Kew Bull. Add. Ser. 9: Rick J Basidiomycetes Eubasidii in Rio Grande do Sul Brasilia. 5. Iheringia Ser. Bot. 8: Secretaria Estadual de Ciência, Tecnologia e Meio Ambiente (SECTMA) Diagnóstico das Reservas Ecológicas: Região Metropolitana do Recife. Recife, Secretaria Estadual de Ciência, Tecnologia e Meio Ambiente do Estado de Pernambuco. Silva AJR, Andrade LHC Etnobotânica nordestina: estudo comparativo da relação entre comunidades e vegetação na Zona do Litoral Mata do Estado de Pernambuco, Brasil. Acta Bot. Bras. 19: Singer R Type studies on Basidiomycetes. VI. Lilloa 26: Singer R Monographs of South American Basidiomycetes especially those of the east slope of the Andes and Brazil. IV. Inocybe in Amazon region and a supplement to part I (Pluteus in South America). Sydowia 15: Singer R Oak mycorrhiza fungi in Colombia. Mycopathol. Mycol. Appl. 20: Singer R The Agaricales in Modern Taxonomy. 4th ed. Koeltz Scientific Books, Stuttgart. Singer R, Araujo IJA, Ivory MH The ectotrophically mycorrhizal fungi of the neotropical lowlands, especially Central Amazonia. Beih. Nova Hedw. 77: Smith SE, Read DJ Mycorrhizal Symbiosis. Academic Press, San Diego. Stijve T, de Meijer AAR Macromycetes from the State of Paraná, Brazil. 4. The Psychoactive species. Arq. Biol. Tecnol. 36:

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