Russula herrerae, a new species with marginal veil from Mexico
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1 Mycologia, 94(2), 2002, pp by The Mycological Society of America, Lawrence, KS Russula herrerae, a new species with marginal veil from Mexico Alejandro Kong 1 Adriana Montoya Arturo Estrada-Torres Laboratorio de Sistemática, Centro de Investigaciones en Ciencias Biológicas, Universidad Autónoma de Tlaxcala, Km 10.5 autopista San Martín Texmelucan-Tlaxcala, San Felipe Ixtacuixtla, Tlaxcala, 90120, México Sing., subsection Lactarioideae Mre., characterized by the presence of a fibrillose-floccose and appendiculate marginal veil is described and illustrated. This new species was collected in a temperate Quercus forest near the village of San Francisco Temezontla in the Mexican state of Tlaxcala, where 18 species of Russula have been recorded (Montoya 1997). Abstract: Russula herrerae, a new species belonging to section Plorantes, subsection Lactarioideae, characterized by the presence of a marginal veil and collected in a temperate Quercus forest in Tlaxcala, Mexico, is described and illustrated. Key Words: Russulaceae, taxonomy, Tlaxcala INTRODUCTION Russula Pers. is one of the most abundant and widely distributed ectomycorrhizal agaric genera in the world (Singer 1986, Buyck 1993, Watling 1995). Mexican species have not received careful attention and many of the 66 species recorded from Mexico (Herrera and Guzmán 1972, Bandala-Muñoz et al 1988, Acosta and Kong 1991, Laferrière and Gilbertson 1992, Cifuentes et al 1993, Rodríguez et al 1993, Chacón 1995, Nava and Valenzuela 1997, García et al 1988, Kong 1998) are poorly understood. Mexican states with more Russula records are Tlaxcala with 34 species (Santiago et al 1990, Acosta and Kong 1991, Estrada-Torres et al 1991, Kong 1998), Oaxaca with 27 species (Singer 1957, Herrera and Guzmán 1961, Guzmán 1975), and Estado de Mexico with 21 (Zenteno et al 1955, Singer 1957, Guzmán 1961, 1966, Herrera and Guzmán 1961, Kobayasi 1979, Aroche et al 1984, Gispert et al 1984, Frutis et al 1985, Estrada- Torres and Aroche 1987, Nava and Valenzuela 1997). Russula brevipes Pk., R. cyanoxantha Schaeff. : Fr., R. foetens Pers., R. emetica (Schaeff. : Fr.) Pers., R. olivacea Schaeff. : Pers., and R. alutacea (Pers. : Fr.) Fr. are the species most frequently mentioned in the Mexican literature (Herrera and Guzmán 1972, Bandala-Muñoz et al 1988). In this paper a new species of Russula belonging to section Plorantes Bat. ex Accepted for publication May 25, Corresponding author, akongluz@hotmail.com MATERIALS AND METHODS Color codes designated as 2.5Y 8/6 are from Munsell (1975) while those delineated as 5D5 or IIa are from Kornerup and Wanscher (1978) or Romagnesi (1967), respectively. Coefficient of lamellae frequency (f) was determined using the formula of Romagnesi (1967). Basidiospore size and shape were determined in lateral view in Melzer s reagent by measuring at least thirty basidiospores from each basidiospore deposit (n number of basidiospores measured). The recorded size excludes ornamentation and is given according to Verbeken (1995, 1996) and Buyck and Verbeken (1995). Average values are in italics. Description of basidiospore ornamentation is given as it appears in Melzer s reagent. Other microscopic structures were examined in 3 10% KOH and often stained with Congo red. Basidia length excludes sterigmata length. Terminology of the hymenial cells is according to Buyck (1991). Drawings of microscopic structures were made with the aid of a drawing tube. Stippling indicates refractive contents of cystidia. Acronyms for herbaria follow Holmgren et al (1990) or Holmgren and Holmgren (1995). TAXONOMY Russula herrerae Kong, Montoya et Estrada, sp. nov. FIGS Pileus mm latus, convexus et umbilicatus in centro, dein planus et depressus vel subinfundibuliformis, cum velo marginali appendiculato; margo haud striatus, acutus, appendiculatus, frustulo veli fibrilloso vel floccoso; pileipellis secernens, impolita, sicca, subglaber in centro, versus marginem fibrillosa et rimosa, alba et locali colore pallido vel flavobrunneo tincta. Trama rigida, alba, immutabilis, ochraceobrunnescens per actionem vermium, odore grato, sapore miti vel leviter acri. Lamellae adnatae vel decurrentes, distantes, versus pilei marginem acutae, 3 8 mm latae, albidae vel cremeae, sapore acri; lamellulae numerosae; acies integra, concolora. Sporae albidae vel pallide cremeae in cumulo (Romagnesii Ib IIa). Stipes mm longus, mm crassus, cylindratus sed basim versus paulatim attenuatus, impolitus, siccus, longitudinaliter ridulosus, pruinosus in apice, albus sed versus basim flavobrunneus, 290
2 KONG ET AL: ANEW MEXICAN RUSSULA 291 interdum cum velo, frustulo veli fibrilloso vel floccoso; intus plenus vel cavernosus. Basidiosporae ( 12.4) m, ellipsoidae vel breviter ellipsoidae [Q (1.12 ) ; V m 3 ; n 153], elementis hemisphaericis, cylindratis vel conicis, usque ad 1.3 m altis, valde amyloideis, in reticulo incompleto subtiliter connexis vel catenulatis et cristis brevibus formantibus ornatae; macula suprahilaris amyloidea. Basidia ( 14.5) m, clavata, tetrasterigmata; sterigmata usque ad 9( 10) 2 m. Cystidia (30 )45 160( 175) (7.5 ) m, numerosa, clavato-fusiformia ad ventricosa, obtusa, mucronata vel interdum constricta in apice, tenuitunicata, intus contentu granuloso-fibrilloso-refringentie repleta; 5 50 m emergentia. Cellulae marginales non differentiatae. Pileipellis non gelatinosa, ex hyphis 2 9 m latis, cylindratis, intertextis, tenuitunicatis vel subtilissime incrassatis, interdum pariete incrustata praediti composita, cellula terminalis obtusa; pileocystidia sparsa, ( 155) (3.5 ) m, cylindrata ad subfusiformem, apice obtusa, mucronata vel interdum constricta, tenuitunicata, intus partim refringente-granuloso-fibrillosa. Solitario vel subgregatim. Habitat in solo non calcareo, sub Quercis caducis, in collibus. Pileus mm broad, convex-umbilicate to convex-depressed when young, soon plano-depressed and finally subinfundibuliform; margin not striate, acute, incurved to arched in section, with floccose to fibrillose appendiculate marginal veil; pellis separable 1/4 1/2 way to disc, dull, dry, radially rugulose, unpolished, radially fibrillose-rimose, often laciniate at margin, smooth or minutely velvety at disc, at times becoming areolate around disc or forming concentric fibrillose squamules on margin in dry weather; initially white, soon developing pale yellow (4A3), yellow (2.5Y 8 7/6, 5Y 8/6; 10YR 8 7/6), brownish yellow (10YR 6/6), greyish yellow (4B4), light yellowish brown (10YR 6/4), yellowish brown (5E5, 5F5, 10YR 5/8), dark yellowish brown (10YR4/6), very pale brown (10YR 8 7/4), light brown (5D5, 5D6, 7D5), brown (6D7, 6E6), greyish brown (6E3), light reddish brown (2.5YR 6/4, 5yR 6/4) or reddish brown (8D5, 8C6) tints in age; remnants of the marginal veil with very pale brown (10YR 7/4), light yellowish brown (10YR 6/4), yellowish brown (10YR 5/4), light brown (5D5, 6D5, 6D6), brown (6E6), dark brown (6F7) tints, squamules with brownish yellow (10YR 6/6), yellowish brown (10YR 5/6), dark yellowish brown (10YR 4/6, 3/6) tints. Trama 3 8 mm thick at midradius, hard; white, unchanging when cut, often yellow (10YR 7/8) brownish yellow (10YR 6/8), light brown (5D6), yellowish brown (5E6, 10YR 5/8) or brown (6D7) around larva channels or at stipe base; odor indistinct, aromatic or fruity, at times disagreeable or fishy in age; taste mild or slightly acrid. Lamellae adnate to decurrent, distant to subdistant (60 lamellae reaching the stipe: f ), not or infrequently forked near stipe, intervenose, anastomosing near stipe or near pileus margin, with numerous lamellulae [mostly one lamellula between two lamellae: (0 )1( 3)]; acute or subacute in front, 2 8 mm broad, slightly thick, brittle; milk white (1A2), whitish (Ib), cream (IIc) to pale yellow (2A3), without bluish green tints; edge even, concolorous; taste acrid. Basidiospore deposit whitish to pale cream (Ib IIa). Stipe mm long, mm thick, equal or tapered downward; surface dull, dry, longitudinally rugulose, unpolished, pruinose at apex, at times with brownish remnants of the marginal veil as floccose or fibrillose cortina-like structure; white, developing grayish yellow (2B5), straw yellow (3B4), very pale brown (10YR 8 7/6, 7/4), brownish yellow (10YR 6/6), yellowish brown (10YR 5/8), light brown (6D6) yellowish brown (5F7) or dark brown (6F7) tints in age; solid becoming cavernous. Basidiospores ( 12.4) m, ellipsoid to shortly ellipsoid, rarely subglobose [Q (1.12 ) ; V m 3 ;n 153]; ornamentation partly to completely amyloid, up to 1.3 m high, mostly m high, consisting of hemispherical, cylindrical or conical elements, with connecting lines of lower height, some elements fused in short ridges or subcatenulate, usually forming a partial to nearly complete reticulum; plage weakly amyloid. Basidia ( 14.5) m, clavate, four-sterigmate, hyaline in KOH; sterigmata m. Pleurocystidia ( 175) (7.5 ) m, usually clavate-fusoid or narrowly ventricose, with rounded or mucronate apices, at times with subapical constrictions, rather abundant ( /mm 2 ), projecting 5 50 m beyond basidioles, rarely embedded in hymenium, completely filled with needle-like, yellowish contents in KOH, grayish brown to blackish brown in sulfovanillin (SV). Cheilocystidia m, similar to pleurocystidia, projecting 5 50 m beyond marginal cells. Marginal cells m broad, cylindrical to clavate, more slender than basidioles, intermixed with basidia and cheilocystidia. Subhymenium composed of short hyphae, filamentous to pseudoparenchymatous. Lamellar trama heteromerous, consisting of nests of sphaerocytes, connective hyphae and abundant oleiferous hyphae; sphaerocytes ( 48) m broad, hyaline in KOH; connective hyphae ( 6.4) m broad, hyaline in KOH; oleiferous hyphae (3.1 ) m broad, with refractive contents in KOH. Pileipellis undifferentiated, without gelatinous matrix, m thick on disc; hyphae 2 9 m broad, repent, interwoven, branched, thin- to slightly thick-walled (1.5 m), some with encrusted pigment; extremities of the hyphae not aggre-
3 292 MYCOLOGIA FIGS Russula herrerae. 1. Basidiomes. 2. Stipe with remnants of the marginal veil. 3. Pileus margin showing the marginal veil. Scale bars 1 cm. All from A. Kong 2622, HOLOTY PE. gated, 3 9 m in diam., filamentous, with rounded apices, often intermixed with inflated hyphae 6 20( 25) m in diam. on margin; oleiferous hyphae m broad, scattered near trama; pileocystidia ( 155) (3.5 ) m, cylindrical to subfusoid, with rounded to mucronate apices or at times with subapical constrictions, thin-walled, not septate, partially filled with needle-like, yellowish contents
4 KONG ET AL: ANEW MEXICAN RUSSULA 293 FIGS Russula herrerae. 4. Basidiospores. 5. Basidia. 6. Marginal cells. 7. Pleurocystidia. 8. Cheilocystidia. Scale bars: 4 10 m, m. All from A. Kong 2622, HOLOTY PE. in KOH, grayish brown, blackish brown to purplish brown in SV, scattered; without primordial hyphae; oleiferous hyphae often intermixed between pileipellis and trama, 2 9 m broad, contorted irregularly, thin-walled, completely filled with homogeneous, refractive, yellowish contents in KOH, pink in SV, blue in cresyl blue, partially cyanophilous. Pileus trama heteromerous, consisting of nests of sphaerocytes, connective hyphae and oleiferous hyphae; sphaerocytes (21 ) m broad; connective and oleiferous
5 294 MYCOLOGIA FIGS Russula herrerae. 9. Extremities of pellis hyphae at pileus center including pileocystidia from upper portion. 10. Extremities of pellis hyphae at pileus margin including pileocystidia from lower portion. 11. Pileipellis hyphae with encrusted walls. 12. Extremities of veil hyphae. Scale bar 20 m. All from A. Kong 2622, HOLOTY PE. hyphae similar to lamellar trama. Marginal veil composed of hyphal strands intermixed with inflated elements and sphaerocytes; cylindrical hyphae ( 11.5) m broad, some with yellowish, encrusted pigment; inflated elements m broad, thin- to slightly thick-walled (1.5 m), regularly septate; sphaerocytes m broad, thin- to thick-walled (2.0 m). Stipitipellis undifferentiated, without gelatinous matrix; hyphae ( 9.0) m broad, repent, interwoven, branched, thin- to slightly thick walled (1.5 m), some with encrusted pigment; extremities of hyphae erect, with rounded, mucronate or rostrate
6 KONG ET AL: ANEW MEXICAN RUSSULA 295 apices, at times with subapical constrictions; caulocystidia ( 220) m, subcylindrical to fusoid, with rounded to mucronate apices, thin-walled, not septate, completely or partially filled with needle-like, yellowish contents in KOH, grayish brown, blackish brown to purplish brown in SV, rather abundant; oleiferous hyphae similar to those of the pileipellis. Velar remnants comprising hyphal strands and chains of sphaerocytes, similar to those of the marginal veil. Clamp connections absent from all tissues. Macrochemical reactions (trama). -naphthol: grayish magenta (13 14E6), grayish violet (15 17E6) to dark violet (18F6); FeSO 4 : peach (7A4) to shell pink (8A3); guaiacol: brownish red (8C6), reddish brown (8D-E6), jasper red (9B7), photo brown (9F8), bluish red (12A6), grayish rose (12B6) or dusky red (0R 3/4); phenol: dark brown (8F8) or photo brown (9F8); sulfoformol: no reaction or pale orange (6A3). TY PE. MEXICO, TLAXCALA: Municipality of Panotla, 1 km E of San Francisco Temezontla, N, W, m alt., Quercus forest, 10- VIII-1993, A. Kong 2622 (HOLOTYPUS TLXM). Specimens examined. MEXICO. TLAXCALA: Municipality of Panotla, 1 km E of San Francisco Temezontla, m alt., Quercus forest, 10-VIII-1993, A. Kong 2622 (HOLOTYPE TLXM). PARATYPE: 9-X-1992, A. Kong 2498 (TLXM); 10-IX- 1993, A. Kong 2626 (MEXU, TLXM); 17-VIII-1993, A. Kong 2636 (MICH, TLXM); 9-VII-1994, A. Kong 2725 (PC, TLXM); 10-IX-1994, A. Kong 2773 (PC, TLXM); 4-VII-1995, A. Kong 2842 (TLXM); 20-VII-1995, A. Kong 2873 (K, NY, TLXM); 26-VII-1996, A. Kong 2906 (EIU, TLXM). Etymology. Dedicated to Dr. Teófilo Herrera for his contributions to Mexican mycology. Habitat and distribution. Solitary to scattered, in small groups of 2 4 basidiomes or subgregarious. On soil. In deciduous Quercus forest at m above sea level. Jul to Oct. Presently known only from the type locality ( N, W). Edibility and vernacular name. People from San Francisco Temezontla gather edible mushrooms in two forest types: the ocotal (Pinus forest) and the encinal (Quercus forest). All species of Russula in subsection Lactarioideae, including the new species where described are considered edible mushrooms by most of the inhabitants of this village. Basidiomes of these taxa are more abundant in the Pinus forest than in the Quercus forest. People apply the names hongo blanco (white mushroom) or hongo blanco de ocote (pine white mushroom) to all species of Russula subsection Lactarioideae whether they grow in the Quercus forest (e.g., R. delica var. centroamericana and R. herrerae) or in the Pinus forest (e.g., R. delica and R. romagnesiana Shaffer). DISCUSSION Russula herrerae belongs to section Plorantes, subsection Lactarioideae due to its lactarioid habit, white pileus color, acute and non-striate pileus margin, hard and unchanging trama, numerous lamellulae, and amyloid basidiospore plage (Shaffer 1964, Romagnesi 1967, Singer 1986). This taxon is distinguished from other species in section Plorantes by the presence of a well-developed, appendiculate marginal veil, which at times remains in part as a fibrillose-floccose annulus on the stipe surface. It resembles Russula delica Fr. in having the same basidiome color, broad and distant lamellae, white to pale cream basidiospore deposit color, and similar basidiospore ornamentation. R. delica var. centroamericana Sing., described from a Quercus-Magnolia forest of Costa Rica (Singer 1989), is also similar. This new species differs from taxa of the R. delica group in its relatively small basidiomes, number of lamellulae between two lamellae, marginal veil and inflated hyphae of pileipellis margin. In the field, basidiomes of R. herrerae might be confused with species of the Lactarius deceptivus Pk. or L. pubescens Fr. group, due to the basidiome color and fibrillose margin, however, R. herrerae lacks the typical pseudocystidia present in the hymenium of all Lactarius species. The ontogeny of the veil is unknown, but probably is similar to the annulus development described by Heim (1937) for R. radicans Heim. ACKNOWLEDGMENTS We wish to thank Drs. Bart Buyck (PC) and Andrew S. Methven (EIU) who kindly reviewed the manuscript and made valuable suggestions. Profs. Lourdes Santiago and Patricia Villaseñor (UNAM) kindly improved the Latin diagnosis. Dr. Rodham E. Tulloss (NJ) reviewed an earlier draft of this manuscript. We are grateful to Drs. Robert L. Shaffer (MICH), Bart Buyck (PC), and Gregory M. Mueller (F) for the loan of some Russula section Plorantes collections. This work was partially supported by CONACyT (Project 4690). LITERATURE CITED Acosta R, Kong A Guía de las excursiones botánicas y micológicas al Cerro El Peñón y Cañada Grande del estado del Tlaxcala. IV Congreso Nacional de Micología. Tlaxcala, Tlaxcala: Jardín Botánico Tizatlán p. Aroche RM, Cifuentes J, Lorea F, Fuentes P, Bonavides J, Galicia H, Menéndez E, Aguilar O, Valenzuela V Macromicetos tóxicos y comestibles de una región comunal del Valle de México, I. Bol Soc Mex Mic 19: Bandala-Muñoz VM, Guzmán G, Montoya-Bello L Especies de macromicetos citadas de México, VII. Agaricales, parte II ( ). Rev Mex Mic 4:
7 296 MYCOLOGIA Buyck B The study of microscopic features in Russula 2. Sterile cells of the hymenium. Russulales News 1: Russula I (Russulaceae). In: Rammeloo J, Heinemann P. eds. Flore illustrée des champignons d Afrique Centrale 15. Brussels, Belgium: Ministère de l Agriculture, Jardin Botanique National de Belgique. p , Verbeken A Studies in tropical African Lactarius species. 2. Lactarius chromospermus Pegler. Mycotaxon 56: Chacón S Nuevos registros de Agaricales (Fungi) de México. Acta Bot Mex 30:9 12. Cifuentes J, Villegas M, Pérez-Ramírez L Hongos macroscópicos. In: Luna Vega I, Llorente Bousquets J. eds. Historia Natural del Parque Ecológico Estatal Omiltemi, Chilpancingo, Guerrero, México. México D.F.: CONA- BIO-UNAM. p Estrada-Torres A, Aroche RM Acervo etnomicológico en tres localidades del Municipio de Acambay, Estado de México. Rev Mex Mic 3: Estrada-Torres A, Kong A, Montoya A, Santiago G Listado preliminar de la micobiota del estado de Tlaxcala. Tlaxcala, Tlaxcala: Jardín Botánico Tizatlán 12: Frutis I, Chio RE, Estrada-Torres A Nuevos registros de macromicetos del Estado de México. Rev Mex Mic 1: García J, Pedraza D, Silva CI, Andrade RL, Castillo J Hongos del estado de Querétaro. Santiago de Querétaro, Querétaro: Universidad Autónoma del Querétaro. 263 p. Gispert M, Nava O, Cifuentes J Estudio comparativo del saber tradicional de los hongos de dos comunidades de la Sierra del Ajusco. Bol Soc Mex Mic 19: Guzmán G Notas sobre algunas especies de agaricáceos no citadas en México. An Esc Nal Cienc Biol 10: Hongos (macromicetos) comunes en la ruta Amecameca-Tlamacas (Volcán Popocatépetl), México. Guías de Excursiones. México D.F.: III Congreso Mexicano de Botánica Hongos mexicanos (macromicetos) en los herbarios del extranjero, III. Bol Soc Mex Mic 9: Heim R Observations sur la flore mycologique malgache V. Les Lactario-Russulés à anneau: Ontogénie et phylogenie III. Rev Mycol 2: Herrera T, Guzmán G Taxonomía y ecología de los principales hongos comestibles de diversos lugares de México. An Inst Biol Mex 32: , Especies de macromicetos citadas de México, III. Agaricales. Bol Soc Mex Mic 6: Holmgren PK, Holmgren NH Additions to index herbariorum (Herbaria), 8th ed, 4 th series. Taxon 44: ,, Barnett LC Index herbariorum. Part I. The herbaria of the world. 8th ed. Regnum Veg 120: Kobayasi Y Mycological survey of Mexican volcano Popocatepetl (II). J Jap Bot 54: Kong A Ectomycorrhizal Agaricales from Tlaxcala, Mexico. McIlvainea 13(2): Kornerup A, Wanscher JH Methuen handbook of color. 3rd ed. London: Eyre Methuen Ltd. 252 p. Laferrière JE, Gilbertson RL Fungi of Nabogame, Chihuahua, Mexico. Mycotaxon 44: Montoya A Estudio etnomicológico en San Francisco Temezontla, Estado de Tlaxcala. [MS Dissertation]. México D.F.: Universidad Nacional Autónoma de México. 133 p. Munsell Munsell soil color charts. Baltimore, Maryland. unpaginated. Nava R, Valenzuela R Los macromicetos de la sierra de Nanchititla, I. Polibotánica 5: Rodríguez O, Guzmán-Dávalos L, Vázquez LS Nuevos registros de hongos para México. Micol Neotrop Apl 6: Romagnesi H Les Russules d Europe et d Afrique du Nord. Paris: Bordas. 998 p. Shaffer RL The subsection Lactarioideae of Russula. Mycologia 56: Santiago G, Kong A, Montoya A, Estrada-Torres A Micobiota del estado de Tlaxcala. Rev Mex Mic 6: Singer R Fungi mexicani, series prima, Agaricales. Sydowia 11: The Agaricales in modern taxonomy. 4th ed. Koenigstein, Germany: Koeltz Scientific Books. 981 p New taxa and new combinations of Agaricales (Diagnoses fungorum novorum Agaricalium IV). Fieldiana Bot 21: Verbeken A Studies in tropical African Lactarius species. 1. Lactarius gymnocarpus R. Heim ex Singer and allied species. Mycotaxon 55: Studies in tropical African Lactarius species. 3. Species described by P. Hennings and M. Beeli. Edinb J Bot 53: Watling R Assessment of fungal diversity: macromycetes, the problem. Can J Bot 73(Suppl 1):S15 S24. Zenteno M, Yerkes WD, Niederhauser JS Primera lista de hongos de México. México D.F.: Oficina de Estudios Especiales, SAG, Folleto Técnico 14.
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