Bioluminescent Mycena Species from Sa˜O Paulo, Brazil

Home , Mycena, Mycena chlorophos, Mycena citricolor, Mycena haematopus

Mycologia, 99(2), 2007, pp. 317–331. # 2007 by The Mycological Society of America, Lawrence, KS 66044-8897

Bioluminescent Mycena species from Sa˜o Paulo, Brazil

Dennis E. Desjardin1 made to Parque Estadual Turı´stico do Alto Ribeira Department of Biology, San Francisco State University, (PETAR), Saõ Paulo State, Brazil, in search of San Francisco, California 94132, USA bioluminescent basidiomycetes. Our collecting sites Marina Capelari were over calcareous soil in evergreen hygrophyllous Instituto de Botaˆnica, Caixa Postal 4005, 01061-970 forest classified as Dense Ombrophylous Forest by Joly Saõ Paulo, SP, Brazil et al (1999). Dominant angiosperm families in this habitat include Myrtaceae, Leguminosae. Rubiaceae, Cassius Stevani Melastomataceae, Lauraceae, Sapotaceae, Euphorbia- Instituto de Quı´mica da Universidade de Saõ Paulo, ceae, Moraceae and Annonaceae (Oliveira Filho and Caixa Postal 26077, 05599-970, Saõ Paulo, SP, Brazil Fontes 2000, Aidar et al 2001). This forest type constitutes the most ancient and diverse ecosystem for Orchidaceae in South America (Brieger 1969) with Abstract: Six species of bioluminescent agarics are high diversity and endemism indices (Mori et al described and illustrated from a single site in primary 1981). To date we have documented the presence of Atlantic Forest habitat in the Parque Estadual eight bioluminescent species of agarics in PETAR. We Turı´stico do Alto Ribeira, Saõ Paulo State, Brazil. are unaware of any other site in the world with equal These include two new taxa of Mycena, viz. M. asterina or greater diversity of bioluminescent basidiomycetes. and M. lucentipes. Luminescence in Mycena fera, M. Herein we describe two new species of Mycena, report singeri and M. discobasis is reported for the first time. for the first time luminescence in Mycena fera Maas In addition an undeterminable luminescent Mycena Geest. & de Meijer, M. singeri Lodge and M. discobasis species is described and additional specimens of Me´trod, and provide data on two other luminescent Gerronema viridilucens are documented. An account- agarics, viz. an undeterminable Mycena species and ing of known bioluminescent species of Mycena and Gerronema viridilucens Desjardin, Capelari & Stevani. a discussion of why they luminesce are presented. Key words: agarics, antioxidant defense, diversity, fungi, taxonomy MATERIALS AND METHODS All basidiomes were collected at night in near total darkness INTRODUCTION and were detected in the field as sources of green luminescence. Specimens were placed in plastic collecting Numerous species of Mycena form luminescent boxes in the field for transport back to the field laboratory. mycelium and/or basidiomes. By our count no fewer All fresh specimens then were photographed in lighted than 26 species of Mycena have been reported as conditions with aid of a flash, and in dark conditions with bioluminescent (TABLE I), belonging to a least 13 20–50 min exposures. Photos were taken with a Nikon N80 taxonomic sections within Mycena sensu lato. To this camera equipped with a Nikkor AF Zoom 28–105 mm lens, accounting we add another six species of luminescent with Fuji Superia ASA 400 or ASA 800 color print film at f5.5 and f11. Fresh specimens were maintained in cool condi- Mycena that belong to an additional three sections of tions until the next morning when macromorphological the genus. The new reports represent material data were documented in daylight. Color terms and collected recently in old growth Atlantic Forest notations in parentheses are those of Kornerup and habitat in Saõ Paulo State, Brazil. Wanscher (1978). The terms used to describe lamellae At one time more than one million square kilo- spacing refer to the number of lamellae that reach from the meters of Brazil were covered in Atlantic Forest stipe to the pileus margin (primaries) and do not include the habitat, considered one of the three most threatened lamellulae, whose spacing is indicated by the number of ecosystems in the world. Until relatively recently more series present. All measurements and colors reported for than 82% of Saõ Paulo State in southeastern Brazil microscopic features were made from dried material was covered by forest, but today only about 7% of the rehydrated in 100% ethanol followed by distilled water, 3% KOH, 3% KOH + Congo red, or Melzer’s reagent. Spore region remains forested, primarily in mountainous statistics include: x, the arithmetic mean of the spore length regions near the coast (SOS Mata Atlantica 1998). In by spore width (6 standard deviation) for n spores measured Dec–Apr 2001–2006 numerous collecting trips were in a single specimen; xmr, the range of spore means and xmm, the mean of spore means (6SD) where more than one Accepted for publication 30 Nov 2006. specimen is available; Q, the quotient of spore length and 1 Corresponding author. E-mail: [email protected] spore width in any one spore, indicated as a range of

317 318 MYCOLOGIA

TABLE I. Species of Mycena reported as bioluminescent in the literature

Taxon1 Mycelium Basidiomes Citation Reporting Luminescence

Sect. Basipedes M. illuminans Henn. ? + Corner 1954, 1994 M. stylobates (Pers. : Fr.) Kummer + 2 Bothe 1931 Sect. Calodontes M. pura (Pers. : Fr.) Kummer + 2 Treu and Agerer 1990 M. rosea (Bull.) Gramberg + 2 Treu and Agerer 1990 Sect. Citricolores M. citricolor (Berk. & M.A. Curtis) Sacc. + 2 Buller 1934 (as Omphalia flavida) Sect. Diversae M. lucentipes ++ this paper Sect. Exornatae M. chlorophos (Berk. & M.A. Curtis) Sacc. ++ Corner 1954 M. discobasis Me´trod ? + this paper Sect. Fragilipedes M. polygramma (Bull. : Fr.) S.F. Gray + 2 Bothe 1931, Treu and Agerer 1990 M. zephirus (Fr. : Fr.) Kummer + 2 Bothe 1931, Treu and Agerer 1990 Sect. Galactopoda M. haematopus (Pers. : Fr.) Kummer ++ Treu and Agerer 1990, Bermudes et al 1992 Sect. Hygrocyboideae M. epipterygia (Scop. : Fr.) S.F. Gray + 2 Bothe 1931 Sect. Lactipedes M. galopus (Pers. : Fr.) Kummer + 2 Bothe 1931, Treu and Agerer 1990 Sect. Mycena M. inclinata (Fr.) Que´l. + 2 Wassink 1948 (as M. galericulata var. calopus) M. maculata P. Karst. + Treu and Agerer 1990 M. tintinnabulum (Fr.) Que´l. + 2 Bothe 1930 Sect. Roridae M. irritans E. Horak 2 + Horak 1978 M. lamprospora (Corner) E. Horak 2 + (spores only) Corner 1950, 1994, Horak 1978 M. pruinoso-viscida Corner ? + Corner 1954, 1994 M. pruinoso-viscida var. rabaulensis Corner ? + (spores only) Corner 1954, 1994 M. rorida (Fr.) Que´l. + 2 Josserand 1953 M. sublucens Corner 2 + Corner 1954 Sect. Rubromarginatae M. lux-coeli Corner ? + Corner 1954 M. noctilucens Corner ? + Corner 1954, 1994 M. noctilucens var. magnispora Corner ? + Corner 1994 M. olivaceomarginata (Massee apud Cooke) Massee + 2 Wassink 1978 (as M. avenacea) M. singeri Lodge ? + this paper M. species ? + this paper Sect. Sacchariferae M. asterina ? + this paper Sect. Sanguinolentae M. sanguinolenta (Alb. & Schwein. : Fr.) Kummer + 2 Bothe 1931 Sect. Supinae M. fera Maas Geest. & de Meijer ? + this paper Manipularis-group M. manipularis (Berk.) Me´trod nom. inval. ++ Corner 1954 non M. manipularis (Berk.) Sacc. 5Poromycena manipularis (Berk.) Heim 5Filoboletus manipularis (Berk.) Singer M. manipularis var. microporus Kawamura ex Corner ? + Corner 1954 nom. inval. DESJARDIN ET AL:BIOLUMINESCENT MYCENA SPECIES 319

TABLE I. Continued

Taxon1 Taxon1 Mycelium Basidiomes Citation Reporting Luminescence Incertae Sedis2 M. daisyogunensis Kobayasi ? + Kobayasi 1951 M. pseudostylobates Kobayasi + ? Kobayasi 1951

1 Synonyms of the taxa listed here are not included. Ex: Mycena dilitata (Fr. : Fr.) Gillet was cited by Bothe (1931) as having luminescent mycelium, but that epithet is now considered a synonym of M. stylobates. 2 Haneda (1955) reported a number of luminescent Mycena species from Japan, referred to Kominami (M. photogena)or Kawamura (M. citrinella var. illumina, M. microillumina, M. phosphora, M. yapensis). None of these epithets were published validly and their taxonomic affinities remain uncertain.

variation in n spores measured; Qm, the mean of Q-values in lose overall, lacking universal veil spines at maturity, a single specimen; Qmr, the range of Qm values and Qmm, the dull, dry; disk pure white or pale yellowish white mean of Qm values where more than one specimen is (,4A2), pure white elsewhere, sometimes developing available. Specimens are deposited in SP and SFSU. pale yellowish white tones overall when dried; strongly greenish-white luminescent. Context extremely thin, TAXONOMY white. Lamellae ascending, subfree, close to subdistant with 1–2 series of lamellulae, narrow (0.5–0.75 mm), Mycena asterina Desjardin, Capelari et Stevani, sp. white, nonmarginate; strongly greenish-white lumi- nov. FIGS. 1a–b, 7a–g nescent. Stipe 10–30 3 0.2–0.5 mm, central, filiform, Primordium 0.5–1.5 mm latus 3 0.2–2.0 mm altus, hemisphaericum, album pallide flavo-tinctum, elementis terete, cylindrical for most of the length, base veli universalis cylindraceis dense obtectis. Pileus 1.0– subclavate to subbulbous, sometimes arising from 3.5 mm latus, obtusus conicus raro convexus, striatus vel a small circular pad of mycelium, fragile, translucent, sulcatus, siccus, minute pulverulentus, glabrescens, albus, dull, dry; apex glabrous, base with scattered, white centro pallide flavo-tinctis, viridis luminosus. Caro perte- strigose hairs; pure white overall or seldom with the nuis, alba. Lamellae adscendentes, subliberae, confertae vel base faintly pale grayish white under the white hairs; subdistantes, angustatae (0.5–0.75 mm), albae, margine not luminescent. concolores, viridae luminosae. Stipes 10–30 3 0.2– Basidiospores (FIG. 7b) 8.2–11.5 3 3.5–5 mm(xmr 5 0.5 mm, fragilis, cylindraceus, albus; apice aequali, glaber; 8.8–10 3 4.0–4.3 mm, x 5 9.4 6 0.8 3 4.1 6 basi pubescens, subbulbosus, haud luminosus. Basidios- mm 0.2 mm, Q 5 2.0–3.0, Q 5 2.22–2.34, Q 5 2.28 6 porae 8.2–11.5 3 3.5–5 mm, ellipsoideae vel subfusoideae, mr mm 5 leves, hyalinae, amyloideae. Basidia 12–15 3 9–11 mm, 0.08, n 20 spores per 2 specimens), a few spores subglobosa vel late clavata, 2- vel 4-sporigera, fibulata. putatively from 2-spored basidia 12.8–14.4 3 4–5 mm, Cheilocystidia 15–22 3 8.5–14 mm, late clavata vel ovoidea, elongate-ellipsoid to subfusoid, smooth, hyaline, dense spinulosae, surculis cylindraceis, recti 0.5 3 ,0.5 mm amyloid, thin-walled. Basidia (FIG. 7c) 12–15 3 9– instructa, hyalinae. Pleurocystidia nulla. Pileipellis hymeni- 11 mm, subglobose to ovoid or broadly clavate, 2- and formis ex acanthocystides 16–35 3 17–38 mm, globosae vel 4-spored, refractive, clamped. Basidioles subglobose to ovoideae, dense spinulosae. Velum universale e cherocyti- ovoid. Cheilocystidia (FIG. 7d) common, 15–22 3 8.5– bus tenuitunicatis vel crassetunicatis formatum, superior- 14 mm, ovoid to broadly clavate, covered over the ibus spinuliferis 22–50 3 12–25 mm, fibulata. Trama upper 1/3–1/2 with tiny spinulae; spinulae 0.5 3 lamellarum dextrinoidea. Hyphae stipitis corticales 4– ,0.5 mm, wart-like to obtusely cylindrical; hyaline, 7.5 mm latae, leves, dextrinoidea. Caulocystidia 60–275 3 5–8 mm, cylindracea, dense spinulosa. Foliicola. Holotypus thin-walled. Pleurocystidia absent. Universal veil com- hic designatus: D.E. Desjardin 7821 (SP #307997; isotypus posed of chains of cherocytes, conspicuous on SFSU). primordia, rarely present on mature pilei; cherocytes Primordia (FIG. 7a) 0.5–1.5 mm diam 3 0.5– (FIG. 7e) 22–50 3 12–25 mm, subglobose to ovoid or 2.0 mm tall, hemispherical to ovoid, white to pale broadly clavate, rarely subcylindrical, 3–7 per chain, yellowish white (,4A2) overall, covered with short terminal and penultimate cells often slightly thick- universal veil spines; spines detersile, cylindrical or walled (0.5–1 mm) and with scattered spinulae, subcylindrical to narrowly conical, straight or curved, remaining cells thin-walled and typically smooth or sometimes agglutinated together to form larger and with few spinulae, clamped; spinulae 1–8 3 0.5– coarser spines, base and marginal area of primordia 1.5 mm, cylindrical to subconical, thin-walled; all cells with shorter spines or lacking spines. Pileus (FIGS. 1a– hyaline, inamyloid. Pileipellis a hymeniform layer of b, 7a) 1.0–3.5 mm diam, obtusely conical, seldom acanthocysts; acanthocysts (FIG. 7f) 16–35 3 17– convex, striate or sulcate, minutely and finely granu- 38 mm, globose to ovoid, thin-walled and often 320 MYCOLOGIA

FIGS. 1–6. Daylight (a) and dark (b) exposures of bioluminescent species of Mycena.1.Mycena asterina.2.Mycena discobasis.3.Mycena fera.4.Mycena lucentipes.5.Mycena singeri.6.Mycena sp. Scale 1–4 5 twice natural size (23); 5–6 5 natural size (13). DESJARDIN ET AL:BIOLUMINESCENT MYCENA SPECIES 321

collapsed, hyaline, inamyloid, covered over upper 3/4 with dense spinulae; spinulae 0.5–1 3 0.5 mm, wart-like to obtusely cylindrical, hyaline; acanthocysts on pileus margin 17–25 3 10–17 mm, clavate, thin- walled, less spinulose than cheilocystidia or other pileipellis acanthocysts. Pileus and lamellar trama of dextrinoid hyphae 10–16 mm diam, hyaline, nongelatinous, nonincrusted. Stipitipellis composed of repent cortical hyphae giving rise to numerous caulocystidia; stipe cortical hyphae parallel, 4–7.5 mm diam, smooth (nonspinulose), hyaline, dextrinoid, slightly thick- walled, nongelatinous, nonincrusted; stipe medullary hyphae similar but 8–20 mmdiam;caulocystidia (FIG. 7g) 60–275 3 5–8 mm, erect to suberect, cylindrical for most of their length then gradually slightly narrowed near the obtuse apex, densely spinulose overall; spinulae 0.5–1.5 3 0.5 mm, cylindrical to subconical, evenly spaced; hyaline, inamyloid, thin-walled. Clamp connections confirmed only on basidia and universal veil cells, not observed in other tissues. Habit, habitat and distribution. Solitary, scattered on leaves of undetermined dicotyledonous plants in disturbed primary Atlantic Forest habitat. March. Sa˜o Paulo State, Brazil. Specimens Examined. BRAZIL. SA˜O PAULO STATE: Mun. Iporanga, Parque Estadual Turı´stico do Alto Ribeira (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, S24u33.519, W048u43.549, elev. ca. 500–530 m, 8 Mar 2005, coll. by C. Stevani et al, D.E. Desjardin 7821 (Holotype: SP #307997; Isotype: SFSU); same location, 7 Mar 2005, D.E. Desjardin 7812 (SFSU, SP #307988); same location, 7 Mar 2005, D.E. Desjardin 7813 (SFSU, SP #307989); same location, 26 Mar 2006, C. Stevani 26.03.06.03 (SP #380283). Commentary. Diagnostic features of Mycena asterina include: primordia covered with prominent, detersile spines forming a universal veil of catenulate cherocytes; cherocytes mostly thin-walled and sparsely spinulose; a hymeniform pileipellis of densely spinulose acanthocysts; spinulose cheilocystidia; elongate- ellipsoid to subfusoid, amyloid basidiospores with Qmm 5 2.2; clamp connections on basidia and universal veil cells; spinulose caulocystidia; and strongly luminescent pileus and lamellae. In combination these features indicate placement in sect. Sacchariferae, stirps Ampar- oina (Desjardin 1995), where it is allied most closely with M. propinqua Maas Geest. & de Meijer (1997). The latter species was described recently from material FIG.7. Mycena asterina (DED 7821 – HOLOTYPE). a. collected in a mixed ombrophilous forest in Parana´ Primordium (23), developing (23) and mature (13) State, due south of where the type material of M. basidiomes. b. Basidiospores. c. Basidia and basidioles. d. asterina was collected. Mycena propinqua differs from Cheilocystidia. e. Cherocytes. f. Acanthocysts. g. Caulocysti- M. asterina in forming pilei with gray disk and striae, dium. Bar 5 10 mm. thicker-walled cherocytes, cheilocystidia with fewer spinulae, slightly smaller basidiospores with Q 5 2.0, and unclamped basidia. In addition M. propinqua was 322 MYCOLOGIA not reported as bioluminescent (Maas Geesteranus and de Meijer 1997). The pileus and lamellae of M. asterina glow brightly at night and basidiomes look like little stars on the forest floor, hence our choice of the epithet. This is the first verified report of luminescence in Mycena sect. Sacchariferae. A report of two tiny, white luminescent Mycena species was published by Ko- bayasi (1951, Mycena daisyogunensis Kobayasi and M. pseudostylobates Kobayasi), but the taxonomic affinities of these species remain uncertain (see Desjardin 1995, p 78 and 85, respectively).

Mycena discobasis Me´trod, Les Myce`nes de Madagas- car:131. 1949. FIGS. 2a–b, 8a–e Pileus (FIGS. 2a–b) 7–12 mm diam, convex, soon plano-convex with a broad, centrally flattened umbilicus, striate to the umbilicus, shiny, dry to subviscid, minutely pruinose, white overall or with a hint of pale gray to grayish white in the umbilicus. Context less than 1 mm thick, white. Lamellae horizontal to ascending, shallowly adnexed, seceding and becoming free in age, sometimes with a poorly developed pseudocollarium, close (23–27 primaries) with 1 series of lamellulae, moderately broad (1–1.5 mm), white, nonmarginate. Stipe 10–18 3 1–1.5 mm, central, terete, cylindrical, 6equal above an enlarged base, hollow, dull, dry, apex glabrous, base pubescent, noninsititious and arising from a broad (2–3 mm), flattened basal disk of radiating white mycelium; pure white overall or with a pale grayish white base. Stipe apex, stipe base and lamellar edges emitting a bright, greenish-white luminescence. Basidiospores (FIG. 8a) (8.5–)9–10.5(–11) 3 6– 7.5 mm(xm 5 9.9 6 0.6 3 6.7 6 0.4 mm, Q 5 1.3– 1.6, Qm 5 1.4 6 0.11, n 5 25 spores per one specimen), broadly ellipsoid, smooth, hyaline, amyloid, thin-walled. Basidia (FIG. 8b) 22–26 3 9.8– 11.2 mm, broadly clavate, 4-spored, clamped. Basi- dioles broadly clavate. Lamellar edge sterile; cheilocystidia (FIG. 8c) 22–42(–48) 3 10–19 mm, broadly clavate to ventricose-rostrate, smooth (lacking diverticula or spinulae), apex not branching, hyaline, inamyloid, lacking pigmented contents, nongelati- FIG.8. Mycena discobasis (Stevani 08.04.05.4). a. Basi- diospores. b. Basidium and basidioles. c. Cheilocystidia. d. nous, thin-walled. Pleurocystidia absent. Pileipellis Pileipellis terminal cells (pileocystidia). e. Caulocystidia. Bar a cutis of smooth to sparsely spinulose, loosely 5 10 mm. interwoven hyphae embedded in a gelatinous matrix up to 100 mm thick, giving rise to terminal pileocys- distributed, hyaline. Hypodermium of hyphae inflated tidia; hyphae 1.5–3 mm diam, cylindrical or irregular up to 18 mm diam, dextrinoid. Pileus trama of in outline, branched, hyaline, inamyloid to weakly interwoven hyphae 4–18 mm diam, cylindrical, hya- dextrinoid, thin-walled; pileocystidia (FIG. 8d) 22–50 line, dextrinoid, nongelatinous. Lamellar trama reg- 3 5–10 mm, subcylindrical to clavate, densely spinu- ular; hyphae 5–20 mm diam, inflated, hyaline, strongly lose, hyaline; spinulae 2–6 3 1–1.5 mm, cylindrical to dextrinoid, nongelatinous, thin-walled. Stipe cortical strangulate, obtuse, sometimes branched, unevenly hyphae 3–8 mm diam, parallel, cylindrical, smooth, DESJARDIN ET AL:BIOLUMINESCENT MYCENA SPECIES 323 hyaline, inamyloid to dextrinoid, nonincrusted, non- similar to M. discobasis; although neither of the gelatinous. Stipe medullary hyphae similar but up to former species have been reported as luminescent. 30 mm diam. Caulocystidia (FIG. 8e) absent at stipe Mycena rhenana, currently placed in sect. Basipedes, apex, scattered on stipe base, 43–165 3 11–18.5 mm, differs in lacking cheilocystidia, and in forming fusoid to fusoid-ventricose, obtuse or acute, smooth, smaller pilei (,6 mm broad), smaller basidiospores hyaline, inamyloid, thin-walled. Clamp connections (6.5–8 3 3.7–5 mm) and marginal pileocystidia with present in all tissues. nonspinulose, acuminate apices ( fide Maas Geester- Habit, habitat and distribution. Solitary, scattered on anus and Winterhoff 1985, Robich 2003). Mycena bark and rotten wood of dead undetermined di- interrupta, currently placed in sect. Cyanocephalae cotyledonous plants in disturbed primary Atlantic (synonymous with M. cyanocephala Singer, type of Forest habitat. April. Saõ Paulo State, Brazil. sect. Cyanocephalae), differs in forming pilei, lamellar Specimen Examined. BRAZIL. SA˜ O PAULO STATE: edges and stipe basal disk with pale blue pigmenta- Mun. Iporanga, Parque Estadual Turı´stico do Alto Ribeira tion, and differs in forming spinulose cheilocystidia (PETAR), Nućleo Santana, S24u32.0489, W048u42.0719, elev. and a nongelatinized pileipellis (fide Singer 1969, ca. 250 m, 8 Apr 2005, coll. by C. Stevani et al, C. Stevani Grgurinovic 2002). Based on overall phenetic simi- 08.04.05.4 (SP #308010; SFSU). larities, we suggest that M. rhenana and M. interrupta Commentary. Me´trod (1949) described M. discobasis are better placed with M. chlorophos and M. discobasis from 5 basidiomes collected by Roger Heim in in sect. Exornatae and both should be checked for Madagascar in 1934 (stored in alcohol at P) and luminescence. because of the stipe basal disk include it in sect. Basipedes. Diagnostic features of Mycena discobasis include: a white, plano-convex, striate, umbilicate Mycena fera Maas Geest. & de Meijer, Verh. Kon. Ned. pileus; nearly free, close, white lamellae; a white, Acad. Wetensch., Afd. Natuurk., Tweede Reeks sparsely pubescent stipe that arises from a flattened 97:31. 1997. FIGS. 3a–b, 9a–e pad of radiating mycelium; relatively large, amyloid Pileus (FIGS. 3a–b, 9a) 4–8 mm diam, obtusely basidiospores with mean 9.9 3 6.7 mm; broadly clavate conical to campanulate or convex with a small to ventricose-rostrate cheilocystidia lacking diverticula rounded umbo, rugulose, striate, dull to subshiny, or spinulae; dextrinoid lamellar trama; a gelatinized, dry to moist (rarely subviscid), glabrous; disk pale loosely interwoven pileipellis with densely spinulose grayish yellow (5D3) to pale yellowish brown (5E4-6) pileocystidia; smooth stipe cortical hyphae giving rise or brown (6E5-8), margin pale grayish orange (5B3) to fusoid-ventricose, nonspinulose caulocystidia; clamp to light brown (5-6D4-5), grayish brown (6D3) or connections; and green luminescence of the stipe beige. Context thin, white. Lamellae ascending, broad- apex, stipe base and lamellar edges. Our material from ly adnate, distant (8–11 primaries) with 0–1 series of Saõ Paulo State, Brazil, differs only subtly from the lamellulae, broad (1–1.25 mm), white to pale grayish Madagascar material in forming slightly larger basi- white or buff, nonmarginate. Stipe 10–15 3 1 mm, diospores. Mycena discobasis was reported by Me´trod to central, terete, 6equal, cylindrical, hollow, dull, dry, have basidiospores measuring 7.5–9.5 3 6.5 mm. In glabrous, noninsititious, arising from a pad of white addition the species was not reported as luminescent. mycelium; pale grayish orange (5B3) to light yellow- As far as we are aware this is only the second published ish brown (5D4-5) or beige. Entire basidiome report of M. discobasis. We cannot explain the disjunct emitting a bright, greenish-white luminescence. distribution. Basidiospores (FIG. 9b) (9–)9.5–11.5(–12.5) 3 9– In combination the taxonomically significant fea- 11(–12) mm[xmr 5 10.3–10.6 3 10.1–10.3 mm, xmm 5 tures of M. discobasis indicate that it is closely allied 10.5 6 0.2 3 10.2 6 0.1 mm, Q 5 1.0–1.1, Qmr 5 1.02– with M. chlorophos (Berk. & M.A. Curtis) Sacc. in sect. 1.03, Qmm 5 1.02 6 0.01, n 5 20–25 spores per 2 Exornatae. Mycena chlorophos, a widespread lumines- specimens], globose to slightly subglobose, smooth, cent species reported from Japan (type from Bonin sometimes with a single large guttule, hyaline, Islands, Berkeley and Curtis 1860), Sri Lanka (Pegler amyloid, thin-walled. Basidia (FIG. 9c) 31–35 3 11– 1986), Borneo, Malaysia and Micronesia (Corner 12.5 mm, clavate, 4-spored, clamped. Basidioles cla- 1954, 1994) and Brazil (Maas Geesteranus and de vate. Cheilocystidia (FIG. 9d) common, lamellar edge Meijer 1997) differs by forming fuscous brown to pale sterile; main body 25–50 3 8.5–16 mm, clavate to grayish brown pilei, has cheilocystidia near the pileus broadly clavate with 3–6 apical projections, hyaline, margin with apical appendages and forms smaller thin-walled; projections 5–22 3 2.5–4.5 mm, irregular- basidiospores of 7–9 3 5–6 mm(ibid; isotype FH!). ly cylindrical, sometimes lobed or knobby, obtuse. The European M. rhenana Maas Geest. & Winterh. Pleurocystidia absent. Pileipellis (FIG. 9e) a cutis of and the Australasian M. interrupta (Berk.) Sacc. are repent, cylindrical hyphae 3–8 mm diam, with scat- 324 MYCOLOGIA

matic pigments. Pileus trama of loosely interwoven hyphae 6–17 mm diam, cylindrical to inflated, nongelatinous, nonincrusted, hyaline, inamyloid to weakly dextrinoid, thin-walled. Lamellar trama of inflated hyphae 7–30 mm diam, dextrinoid, otherwise similar to pileus trama hyphae. Stipe cortical hyphae (FIG. 9e) parallel, 3–6 mm diam, cylindrical, with scattered diverticula, nongelatinous, nonincrusted, hyaline, dextrinoid; diverticula 4–22 3 1.5–4 mm, irregularly cylindrical, often forked, thin-walled. Stipe medullary hyphae parallel, 4–16 mm diam, cylindrical, hyaline, dextrinoid; with scattered, refractive, yellow oleifer- ous hyphae 2–4 mm diam. Caulocystidia absent. Clamp connections present in all tissues. Habit, habitat and distribution. Solitary or in small clusters, scattered on fern rootlets and on bark of undetermined dicotyledonous trees in disturbed primary Atlantic Forest habitat. December thru April. Saõ Paulo State, Brazil. Specimens Examined. BRAZIL. SAÕ PAULO STATE: Mun. Iporanga, Parque Estadual Turı´stico do Alto Ribeira (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, S24u33.519, W048u43.549, elev. ca. 500–530 m, Apr 2001, coll. by C. Stevani et al, C. Stevani 04.01 (SP #380146; dried material); same location, 1 Dec 2004, coll. by Joaquim Mendes Filho, C. Stevani 01.12.04.01 (SP #380147; preserved in alcohol); same location, 26 Mar 2006, C. Stevani 26.03.06.05 (SP#380285); PETAR, Nućleo San- tana, S24u32.0489, W048u42.0719, elev. ca. 250 m, 8 Apr 2005, coll. by C. Stevani et al, C. Stevani 08.04.05.1 (SP #308007); same location, 8 Apr 2005, coll. by C. Stevani et al, C. Stevani 08.04.05.2 (SP #308008); PETAR, Poço Veado, Poço da Viu´va, 26 Mar 2006, C. Stevani 26.03.06.02 (SP #380282). Commentary. Mycena fera was described recently from a single specimen collected on a decayed branch of a dicotyledonous tree in Parana´ State, just south of where we collected it on fern rootlets and tree bark in Saõ Paulo State, Brazil. Maas Geesteranus and de Meijer (1997) placed the species in sect. Supinae because of the arcuate lamellae, globose basidiospores and coarsely diverticulate cheilocystidia, pileipellis and stipitipellis hyphae. They did not report the species as being luminescent. This is the second report of the species from Brazil and the first report of it emitting a strong greenish luminescence from all parts of the basidiome, although strongest in the stipe and 3 FIG.9. Mycena fera (Stevani 04.01). a. Basidiomes (1 ). lamellar edges. Pileus coloration is variable, with some b. Basidiospores. c. Basidia and basidiole. d. Cheilocystidia. basidiomes showing pale grayish yellow tones whereas e. Pileipellis and stipitipellis hyphae. Bar 5 10 mm. others are brown. tered diverticula, slightly gelatinous to gelatinous, nonincrusted, hyaline, inamyloid; diverticula 5–20 3 Mycena lucentipes Desjardin, Capelari et Stevani, sp. 1–4 mm, irregularly cylindrical, sometimes forked, nov. FIGS. 4a–b, 10a–d often curved. Hypodermium well developed, com- Pileus 4–12 mm latus, conicus vel convexus, dein posed of short-celled hyphae 12–34 mm diam, hyaline, campanulatus vel planoconvexus, papillatus vel umbonatus, dextrinoid, thin-walled, sometimes with brown plas- pellucid-striatus, hygrophanus, glaber, siccus, brunneus vel DESJARDIN ET AL:BIOLUMINESCENT MYCENA SPECIES 325

disk brown (6E5-6) to yellowish brown (5E5-6) or orangish brown with a light yellowish brown (5D5-6) margin, in age becoming dark yellowish brown (5F4) to brown (6E4-6), olive brown or dark brown (6F4-6) overall, sometimes retaining a light yellowish brown margin, fading overall with moisture loss to dingy cream (4A3) or pinkish buff. Context up to 1 mm thick, watery-concolorous with pileus surface. Odor not distinctive. Taste mild, slightly sour. Lamellae arcuate to decurrent, distant to subdistant (8–14 primaries) with 1–2 series of lamellulae, moderately broad (1–1.5 mm), sometimes slightly interwoven in age, pale grayish orange (5B4) to light yellowish brown (5D4-5), light brown (6D4-5) or pale tawny olive. Stipe 8–25 3 1–1.5(–1.75) mm, central, terete, 6equal or with a slightly flared apex, typically cylindrical above a slightly enlarged base, solid to stuffed, fragile to pliant, pruinose to hispidulous overall (more densely so at the apex), dull, dry; cream (4A3) to light yellowish brown (5D5-6) or clay color overall when young, becoming grayish orange (5B4-5) or brown (6E4-6) overall in age, sometimes with a darker base; noninsititious, arising from yellowish brown tomentose mycelium; stipe emitting a bright, greenish-white luminescence, observed easily in the dark. Basidiospores (FIG. 10b) (6.0–)6.5–10 3 3.5–5.5 mm (xmr 5 7.4–8.9 3 4.2–4.9 mm, xmm 5 8.3 6 0.6 3 4.5 FIG. 10. Mycena lucentipes (DED 7828 – HOLOTYPE). a. 6 0.3 mm, Q 5 1.3–2.6, Qmr 5 1.5–2.1, Qmm 5 1.86 6 Basidiomes (13). b. Basidiospores. c. Basidia and basidiole. 0.3, n 5 20–25 spores per 8 collections), ellipsoid to d. Caulocystidia. Bar 5 10 mm. broadly ellipsoid or elongate-ellipsoid, inequilateral, smooth, hyaline, amyloid or weakly amyloid, thin- fulvus, dein umbrinus. Caro pileo concolor. Lamellae 8–13 walled, white in deposit. Basidia (FIG. 10c) 32–38 3 stipitem attingentes, arcuatae vel decurrentae, distantes vel 7.5–10 mm, clavate, 4-spored with sterigmata up to subdistantes, usque ad 1.5 mm latae, dein subintervenosae, 5 mm long, clamped. Basidioles clavate. Cheilocystidia pallide griseoaurantiaceae vel fulvae, margine concolores. absent; lamellar edge fertile. Pleurocystidia absent. Stipes 8–25 3 1–1.5 mm, fragilis vel flexibilis, aequalis, Pileipellis a cutis of repent, smooth hyphae 5–12 mm cylindraceus, pruinosus vel hispidulus, siccus, cremeus vel diam, nondiverticulate, occasionally with one or more pallide fulvus, denum brunneus, fibrillis fulvis substrato low, broad bumps, nongelatinous, nonincrusted, affixus, viridis luminosus. Basidiosporae 7.5–10 3 3.5–5 mm, hyaline, inamyloid, thin-walled; overlaying a poorly inaequilateraliter ellipsoideae, leves, hyalinae, amyloideae. developed or undifferentiated hypodermium of Basidia 32–38 3 7.5–10 mm, clavata, 4-sporigera, fibulata. broader (12–20 mm diam), weakly dextrinoid hyphae. Cheilocystidia nulla. Pleurocystidia nulla. Hyphae pileipellis Pileus trama of hyphae 8.5–18 mm diam, little differ- 5–12 mm latae, leves, haud gelatinosae, inamyloidae, fibula- tae. Trama lamellarum iodi ope haud vinescens. Hyphae entiated from the pileipellis or hypodermium, loosely stipitis corticales 3–8 mm latae, leves, inamyloidea, haud interwoven, hyaline, inamyloid. Lamellar trama regu- gelatinosae. Caulocystidia 15–40 3 7.5–11.5 mm, clavata vel lar; hyphae 6–15(–18) mm diam, subparallel, hyaline, ventricosa, geniculata, tenuitunicata. Ramulicola. Holoty- inamyloid or weakly dextrinoid in some basidiomes, pus hic designatus: D.E. Desjardin 7828 (SP #308004; nongelatinous, thin-walled. Stipitipellis composed of isotypus SFSU). repent hyphae giving rise to numerous erect caulo- Pileus (FIGS. 4a–b, 10a) 4–15(–20) mm diam, at first cystidia; stipe cortical hyphae 3–8 mmdiam;stipe conical to convex-papillate, soon becoming campan- medullary hyphae 6–13 mm diam; stipe hyphae parallel, ulate to plano-convex with a prominent papilla or smooth, nongelatinous, nonincrusted, hyaline, ina- umbo; papilla or umbo conical to obtuse; margin myloid, thin-walled. Caulocystidia (FIG. 10d) solitary decurved, entire, pellucid-striate to striate; surface or clustered, 15–40 3 7.5–11.5 mm, irregularly clavate hygrophanous, glabrous, moist to dry; when young or ventricose, obtuse, often geniculate, as terminal 326 MYCOLOGIA cells or intercalary outgrowths, hyaline, inamyloid, Mycena lucentipes is phenetically most similar to M. thin-walled. Clamp connections common in all tissues. diversa Maas G. & de Meijer, the type species of a new Habit, habitat and distribution. Solitary to subcespi- section Diversae Maas G. & de Meijer (1997), and we tose or in cespitose clusters of 5–30 basidiomes, tentatively accept M. lucentipes in that section. Mycena lignicolous on rotted sticks or on rootlets of un- diversa differs from M. lucentipes in forming grayish determined dicotyledonous plants in disturbed prima- brown to pale gray, plano-convex pilei, white lamel- ry Atlantic Forest habitat or in riparian habitats. Dec– lae, and prominent lageniform cheilocystidia. In Apr in Brazil; Oct–Jan in Puerto Rico. addition M. diversa was not reported as luminescent. Specimens Examined. BRAZIL. SAÕ PAULO STATE: Only the stipes and mycelia are luminescent in M. Mun. Iporanga, Parque Estadual Turı´stico do Alto Ribeira lucentipes, but they glow so brightly that the pileus (PETAR), Nućleo Santana, S24u32.0489, W048u42.0719, elev. and lamellae appear faintly luminescent in photo- ca. 250 m, 9 Mar 2005, coll. by C. Stevani et al, D.E. graphs. Maas Geesteranus and de Meijer (1997) # Desjardin 7828 (Holotype: SP 308004, Isotype: SFSU); suggested that sect. Diversae is allied with sect. same location, 1 Dec 2004, C. Stevani 01.12.04.02 (SP Exornatae Maas G., a monotypic section based on #380148); same location, 9 Apr 2005, C. Stevani 09.04.05.5 (SP #308011); same location, 9 Apr 2005, C. Stevani M. chlorophos (Berk.&M.A.Curtis)Sacc.(see 09.04.05.6 (SP #308012); PETAR, ca. 12 km from Bairro commentary for M. discobasis above). Mycena chlor- da Serra on Lajeado Road, S24u33.519, W048u43.549, elev. ophos is a widely distributed luminescent species, ca. 500–530 m, 8 Mar 2005, coll. by C. Stevani et al, D.E. reported by Corner (1954) and Maas Geesteranus and Desjardin 7820 (SFSU, SP #307996); MATO GROSSO DO de Meijer (1997) from Brazil. We have not seen SUL STATE: Mun. Costa Rica, Cachoeira Salto, 8 Dec 2002, material of the latter species from Saõ Paulo State. coll. by C. Stevani, C. Stevani 08.12.02 (SP #380149). PUERTO RICO. Mun. Rio Grande, Luquillo Mountains, La Mina Recreation Area, Big Tree Trail, S18u189330, Mycena singeri Lodge, Trans Brit Mycol Soc 91:111. W65u469300, 4 Oct 1997, coll. by S. Cantrell, A. Perez and 1988. FIGS. 5a–b, 11a–e mycology class, PR-4678 (SFSU, CFMR); same location, 13 Only two mature basidiomes studied. Pileus Jan 1998, coll. by S. Cantrell, PR-5726 (SFSU) (FIG. 5a–b) 8–10 mm diam, obtusely conical, expand- Commentary. Mycena lucentipes currently is known ing to nearly plane with or without a low obtuse from Puerto Rico south to Saõ Paulo, Brazil. It is umbo, sulcate, dull, dry, glabrous or minutely characterized by basidiomes with these combination of granulose; disc pinkish brown, margin pinkish red, features: campanulate-papillate pilei colored yellowish elsewhere pinkish buff. Context thin, white. Lamellae or orangish brown to brown; arcuate to decurrent, adnate with a decurrent tooth to subdecurrent, light brown to yellowish brown lamellae; subcespitose distant (8–9 primaries) with one series of lamellulae, to cespitose, hispidulous stipes; pileipelles of nondi- moderately broad, white with red margins. Stipe 18–22 verticulate, repent hyphae; relatively undifferentiated 3 1 mm, central, terete, cylindrical, dull, dry, pileus tissues; an absence of hymenial cystidia; glabrous to minutely pruinose overall, noninsititious, ellipsoid, amyloid basidiospores; abundant caulocysti- arising from white basal mycelium; white to buff dia; and strongly luminescent stipes. Pileus coloration overall. Stipe and lamellar edges emitting a bright, and spore size varies with geographical area. In the greenish-white luminescence. southern populations from old growth primary Atlan- Basidiospores (FIG. 11a) 7–9.5 3 6.5–8.5 mm(xm 5 tic Forest area in Saõ Paulo State, pilei are yellowish 8.3 6 0.8 3 7.5 6 0.6 mm, Q 5 1.0–1.2, Qm 5 1.1 6 brown to brown and basidiospores show mean size 8.7 0.07, n 5 25 spores per one specimen), globose to 3 4.2 mm with a Q-value of 2.07. In the population subglobose, hyaline, amyloid, thin-walled. Basidia from a riparian habitat in a secondary forest in the (FIG. 11b) 25–32 3 9.5–11 mm, clavate, 4-spored with more northerly Mato Grosso do Sul State, Brazil, pilei sterigmata up to 5 mm long, clamped. Basidioles show orange to orangish brown colors, and the broadly clavate. Cheilocystidia (FIG. 11c) common, basidiospores are smaller and less elongate with mean 24–45 3 8–22 mm, versiform, vesiculose to broadly size 7.6 3 4.5 mm and a Q-value of 1.66. In Puerto Rico clavate, lageniform, fusoid or irregular in outline, populations the pilei range from orangish brown to often bifid, with 1–3 broadly rounded lobes or olive brown, and basidiospores are typically interme- projections, hyaline or with pinkish brown contents, diate in length but broader with mean size 8.0 3 inamyloid, thin-walled. Pleurocystidia present as a few 4.9 mm with a Q-value of 1.61. Until more specimens cells similar to the cheilocystidia near the lamellar throughout the range of the species become available, edges, absent further back on lamellar faces. Pileipellis and definitive molecular data are generated, we accept a thin cutis of repent hyphae with uncommon the populations as representing a widely distributed, projections, terminal pileocystidia and marginal cells; morphologically variable species. hyphae 3–7 mm diam, cylindrical, smooth or with a few DESJARDIN ET AL:BIOLUMINESCENT MYCENA SPECIES 327

(FIG. 11d) like the cheilocystidia, 28–45 3 5–24 mm, broadly clavate, ventricose, fusoid or irregular and often bifid, hyaline, inamyloid, thin-walled. Hypoder- mium well developed, composed of hyphae inflated up to 30 mm diam, hyaline, strongly dextrinoid, thin- walled, nongelatinous. Pileus trama of interwoven hyphae 3–7 mm diam, sometimes inflated up to 20 mm, weakly dextrinoid. Lamellar trama regular; hyphae 6–38 mm diam, hyaline, strongly dextrinoid. Stipe cortical hyphae 3–10 mm diam, parallel, cylindrical, hyaline, dextrinoid, nongelatinous, nonincrusted; giving rise to abundant terminal caulocystidia and intercalary projections (FIG. 11e), 8–40 3 5–10 mm, clavate, broadly rounded, sometimes bifid, hyaline, lacking pigmented contents, inamyloid, thin-walled. Stipe medullary hyphae 6–18 mm diam, parallel, cylindrical, hyaline, dextrinoid, nongelatinous, nonincrusted. Clamp connections present in all tissues. Habit, habitat and distribution. Solitary among epiphytic mosses on the bark of a living dicotyledonous tree in disturbed primary Atlantic Forest. April. Saõ Paulo State, Brazil. Specimens Examined. BRAZIL. SAÕ PAULO STATE: Mun. Iporanga, Parque Estadual Turı´stico do Alto Ribeira (PETAR), Nućleo Santana, S24u32.0489, W048u42.0719, elev. ca. 250 m, 8 Apr 2005, coll. by Stevani et al, C. Stevani 08.04.05.3 (SP 308009). Commentary. Only two mature basidiomes of M. singeri were collected from old growth Atlantic Forest habitat in Saõ Paulo State, Brazil, and our analysis is based on data from this single specimen. Mycena singeri, described originally from material collected in Puerto Rico, is similar to two Asian species with luminescent stipes and lamellae that belong in sect. Rubromarginatae, viz. Mycena lux-coeli Corner and Mycena noctilucens Corner. Both of the latter species differ from M. singeri in forming cheilocystidia, pileipellis and stipitipellis hyphae with narrower and more numerous projections, and they differ by forming closer lamellae (12–28 primaries) that are ascending-adnate (fide Corner 1954). In comparison M. singeri forms relatively few, broadly rounded and knob-like projections on cystidia and cuticular hyphae, and has distant (8–9 primaries), adnate-decurrent lamellae. Mycena lux-coeli differs also in forming larger cheilocystidia (40–100 mm long), more numerous FIG. 11. Mycena singeri (Stevani 08.04.05.3). a. Basidio- pileocystidia and darker pilei (pale purplish brown; spores. b. Basidia and basidiole. c. Cheilocystidia. d. Pileus fide Corner 1954). Mycena noctilucens differs also in marginal cells. e. Caulocystidia. Bar 5 10 mm. forming slightly smaller and more ellipsoid basidiospores, and numerous ventricose-subulate pleurocysti- scattered knob-like projections, nongelatinous, non- dia (fide Corner 1954). Lodge (1988) did not report incrusted, hyaline, inamyloid; pileocystidia as terminal M. singeri as luminescent; hence this is the first report cells or intercalary projections, erect to repent, clavate of luminescence for this species. to irregular in outline, similar to pileus marginal cells; A description of the following species, known at edge of pileus with distinctive marginal cells present from a single immature or sterile basidiome, 328 MYCOLOGIA

cylindrical, smooth (nondiverticulate), nongelatinous, nonincrusted, hyaline to grayish brown, inamyloid to weakly dextrinoid, thin-walled. Stipe medullary hyphae parallel, 6–20 mm diam, strongly dextrinoid, otherwise like cortical hyphae. Caulocystidia absent. Clamp connections absent in all tissues. Habit, habitat and distribution. Solitary on rootlets of undetermined plants in disturbed primary Atlantic Forest habitat. March. Saõ Paulo State, Brazil. Specimen Examined.BRAZIL.SA˜ O PAULO STATE: Mun. Iporanga, Parque Estadual Turı´stico do Alto Ribeira (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, S24u33.519, W048u43.540, elev. ca. 500–530 m, 27 Mar 2004, coll. by C. Stevani et al, C. Stevani 27.03.04 (SP #380150; preserved in alcohol). Commentary. This species is known at present from FIG.12. Mycena species (Stevani 27.03.04). a. Basi- a single, immature or sterile basidiome lacking diomes (13). b. Basidioles. c. Cheilocystidia. Bar 5 10 mm. basidiospores. Distinctive features include a nearly black basidiome with white, adnexed lamellae, relatively small, broadly lobed or knobby cheilocystidia, is presented below because it represents another smooth to sparsely diverticulate pileipellis hyphae, bioluminescent Mycena species from the Atlantic smooth stipe cortical hyphae, and an absence of clamp Forest habitat of Saõ Paulo State, Brazil. Sporulating connections, pleurocystidia and caulocystidia. In com- specimens of this interesting species are required bination these features suggest that the species before a definitive identification can be made. belongs in Mycena sect. Fragilipedes, where it might be allied with M. deusta Maas G. & de Meijer (1997: Mycena sp. FIGS. 6a–b, 12a–c 59). Of interest, only the stipe apex and stipe base of Macroscopic features compiled from several photo- Mycena sp. are green-luminescent. graphs of a fresh basidiome. Pileus (FIGS. 6a–b, 12a) To date only two species of sect. Fragilipedes have 10 mm diam, acutely conical, striate, dull, dry, been reported as bioluminescent, viz. M. polygramma glabrous; dark brown to nearly black overall. Lamellae (Bull. : Fr.) S.F. Gray (Bothe 1931) and M. zephirus adnexed, close, narrow, white. Stipe 20 3 2mm, (Fr. : Fr.) Kummer (Bothe 1931). For both of the central, terete, cylindrical, dull, dry, glabrous, non- latter species, only the mycelium was reported as insititious, base with white mycelium; dark gray to luminescent. dark grayish brown or nearly black overall. Only the stipe apex and stipe base emit a green luminescence. Gerronema viridilucens Desjardin, Capelari & Stevani, Exsiccata preserved in alcohol. Basidiospores not Fungal Diversity 18:10. 2005. observed; specimen immature or sterile. Basidia not This species, described recently from material collected observed. Basidioles (FIG. 12b) 28–32 3 6–8 mm, at PETAR, is common on the bark of living Eugenia clavate, unclamped. Cheilocystidia (FIG. 12c) common fluminensis O. Berg. trees. It is characterized by these (lamellar edge sterile), 12–22 3 8.5–12.5 mm, broadly features: small, reddish brown basidiomes (reminiscent of clavate to vesiculose or irregular in outline, some- Xeromphalina) with decurrent, distant lamellae, basidios- times lobed, with or without 2–5 broadly rounded pores in the range 7–9.5 3 4.5–5.5 mm, the absence of knobs,nongelatinous,hyaline,thin-walled,un- hymenial cystidia, the presence of clamp connections, clamped. Pleurocystidia absent. Pileipellis a cutis of negative KOH reactions on all basidiome surfaces, and an intense green luminescence. We currently are analyzing the smooth or sparsely diverticulate hyphae 3.5–8 mm metabolic pathway resulting in luminescence in this species diam, nongelatinous, nonincrusted, hyaline, inamy- based on cultures isolated from fresh material. Additional loid, thin-walled, overlaying a well developed pseudo- specimens include: BRAZIL. SAÕ PAULO STATE: Mun. parenchymatous hypodermium. Hypodermium com- Iporanga, Parque Estadual Turı´stico do Alto Ribeira posed of short-celled hyphae up to 20 mm diam, pale (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, grayish brown, strongly dextrinoid, thin-walled. Pileus S24u33.519, W048u43.549, elev. ca. 500–530 m, 7 Mar 2005, trama of interwoven hyphae 4–18 mm diam, hyaline, D.E. Desjardin 7814 (SFSU, SP #307990); same location, 8 inamyloid to weakly dextrinoid. Lamellar trama Mar 2005, D.E. Desjardin 7822 (SFSU, SP #307998). regular; hyphae similar to those in pileus trama, Additional taxon. One additional potentially new dextrinoid. Stipe cortical hyphae parallel, 3–6 mm diam, bioluminescent species of Mycena has been collected DESJARDIN ET AL:BIOLUMINESCENT MYCENA SPECIES 329 in PETAR. Unfortunately it is represented by a single lost numerous times? We suspect that the metabolic collection lacking macromorphological and ecological pathway leading to bioluminescence in mycenoid notes. The species (SP #380281) has a viscid pale fungi serves an important biological role (see below) yellowish brown pileus and viscid white stipe and and that it evolved once early in the evolutionary belongs in sect. Euspeireae where it is allied with M. history of the lineage and that the final light-emitting euspeirea (Berk. & M.A. Curtis) Sacc. Until more step(s) was lost numerous times. Ongoing molecular material of this interesting species is located, no formal phylogenetic and biochemical studies in our labs are description will be presented. (It is not accounted for addressing this hypothesis. in TABLE I). The potential roles of bioluminescence in the biology of fungi have been reviewed recently by DISCUSSION Bermudes et al (1992), Herring (1994) and Weitz (2004). Sivinski (1981, 1998), reiterating the ideas of Collecting specimens at night is a productive, albeit numerous earlier workers (e.g. McAlpine 1900, Ewart potentially dangerous, method of documenting the 1906, Johnson 1919, Lloyd 1974), suggested that diversity of bioluminescent fungi. Our field studies in luminescent basidiomes attract invertebrates to aid in PETAR yielded seven species of Mycena and Gerro- fungal spore dispersal. Sivinski (1981) hypothesized nema viridilucens from remnant old growth Atlantic also that luminescence might attract predators of Forest habitat over calcareous soil. These species add fungivores or might serve as a warning signal to repel to a growing list of Mycena s.l. reported to produce nocturnal fungivores. Sivinski’s hypotheses are diffi- luminescent mycelium and/or basidiomes, currently cult to prove because fungivores could be attracted by totaling no fewer than 33 taxa belonging to 16 the odors of basidiomes instead of by their bio- taxonomic sections (TABLE I). Molecular data (Mon- luminescence. The question whether invertebrates calvo et al 2002) indicate that the genus Panellus nests associated with bioluminescent fungi actually see the within Mycena s.l.; hence we can add five more taxa to light emitted by the fungus must be verified with the list of bioluminescent mycenoid fungi, viz. electroretinography (e.g. Lall et al 2000). Of course Panellus stypticus (Bull. : Fr.) P. Karst., P. pusillus luminescence as an adaptation to promote spore (Pers. ex le´v.) Burdsall & O.K. Miller, Dictyopanus dispersal by visiting invertebrates does not explain pusillus var. sublamellatus Corner (not yet transferred why nonsporulating mycelium of many species is to Panellus), P. gloeocystidiatus (Corner) Corner and luminescent. P. luminescens (Corner) Corner. We contend that Bioluminescence is an oxygen-dependent metabol- there are many more described species of mycenoid ic process. Lingle (1989, 1993) and Bermudes et al fungi with bioluminescent properties that have (1992) have hypothesized that fungal biolumines- remained undetected. As noted by Bermudes et al cence is involved in lignin degradation through the (1992), although photometers have been used in detoxification of peroxidases formed during lignino- other disciplines to detect bioluminescence, in lysis. As far as we know all luminescent Mycena species mycology the perception of light emitted by mycelium are white-rot fungi capable of lignin degradation and basidiomes has been largely by human eye. As (Treu and Agerer 1990; Desjardin unpubl). We favor a result we might be grossly underestimating the the hypothesis that fungal bioluminescence is an number of bioluminescent taxa. For example, in M. advantageous biochemical process that provides haematopus, where previous accounts failed to per- antioxidant protection against deleterious effects of ceive bioluminescence, when studied photometrical- reactive oxygen species (ROS) produced mainly by ly, both mycelium and basidiomes emitted light mitochondria during respiration. McElroy and Seliger (Bermudes et al 1992). Moreover when taxonomists (1962) hypothesized that bioluminescence might describe euagarics they rarely record macromorpho- have evolved as an ancient oxygen detoxifying logical data at night, so luminescent properties go mechanism with the exclusive purpose of oxygen undetected. Herein we report three species of Mycena consumption. As so eloquently stated by Herring that heretofore were unknown as being luminescent, (1994): ‘‘perhaps the light of luminous fungi is really viz. M. discobasis, M. fera and M. singeri. Approxi- no more than an incidental by-product of an enzyme- mately 500 species currently are recognized in Mycena mediated oxidation reaction.’’ Seliger (1975) first s.l. (Kirk et al 2001). A review of TABLE I where we suggested that the bioluminescence catalyzing en- document 33 bioluminescent species of Mycena s.l. zymes named luciferases arose from mixed-function spread over 16 sections raises the question, did oxygenases involved in the removal of unsaturated bioluminescence evolve in the mycenoid fungi in- compounds during the early life history. Later Wood dependently numerous times, or did it evolve once (1995) proposed instead that the luminescent phe- (or only a few times) early on and was subsequently notype drove the evolution of new oxygenase func- 330 MYCOLOGIA tions. Concomitant induction of the antioxidant ———, ———. 2000. Luciferase and urate may act as enzyme superoxide dismutase (SOD) and luciferase antioxidant defenses in larval Pyrearinus termitillumi- occurs in the bioluminescent bacterium Xenorhabdus nans (Elateridae: Coleoptera) during natural develop- luminescens under hyperoxia (Colepicolo-Neto et al ment and upon 20-hydroxyecdysona treatment. Photo- 1992). Moreover Rees et al (1998) and Barros and chem Photobiol 71(5):648–654. ———, ———. 2001. Daily variations of antioxidant enzyme Bechara (1998, 2000, 2001), reported the role of and luciferase activities in the luminescent click-beetle luciferins (i.e. the name given for a class of substrates Pyrearinus termitilluminans: cooperation against oxy- of luciferase) as antioxidant molecules in jellyfish, gen toxicity. Insect Biochem Mol Biol 31:393–400. Aequorea sp., and in the click beetle, Pyrearinus Berkeley MJ, Curtis MA. 1860. Characters of new fungi termitilluminans, respectively. Finally, Shimomura collected in the North Pacific Exploring Expedition by (1992) studied the influence of SOD and catalase Charles Wright. Proc Amer Acad Arts 4:111–130. (CAT) on luciferin production and bioluminescence Bermudes D, Petersen RH, Nealson KH. 1992. Low-level intensity using luminescent mycelia and fruiting bioluminescence detected in Mycena haematopus basi- bodies of Armillaria mellea, Mycena citricolor, Mycena diocarps. Mycologia 84:799–802. lux-coeli, Omphalotus olearius, Panellus stypticus and Bothe F. 1930. Ein neuer einheimischer Leuchtpilz, Mycena Pleurotus japonicus (5Lampteromyces japonicus). Both tintinnabulum. Ber Deutsch Bot Ges 48:394–399. SOD and CAT activities as well as the ratio CAT/SOD ———. 1931. Ueber das Leuchten verwesender Bla¨tter und seine Erreger. Planta 14:752–765. (20–30-fold) are higher in all mycelia, where the Brieger FG. 1969. Patterns of evolutionary and geographical consumption of oxygen is more pronounced due to distribution in Neotropical orchids. J Linn Soc, Biol 1: the lignin degradation and consequent H2O2 pro- 197–217. duction. In addition results have shown that the lower Buller AHR. 1934. Omphalia flavida, a gemmiferous and the SOD activity the higher is the light emission luminous leafspot fungus. In: Buller AHR, ed. Re- intensity, suggesting a possible connection of super- searches in Fungi. Vol. IV. London, New York, Tor- oxide anion with the bioluminescent pathway. To onto: Longmans, Green & Co. p 397–454. address the question of why these mushroom-forming Colepicolo-Neto P, Camarero VCCP, Eickstein J, Hastings species bioluminesce, we currently are studying the JW. 1992. Induction of bacterial luciferase by pure influence of antioxidant and ligninolytic enzymes on oxygen. J Gen Microbiol 138:1–6. the luminescence intensity of M. lucentipes and G. Corner EJH. 1954. Further descriptions of luminous agarics. viridilucens. Trans British Mycol Soc 37:256–271. ———. 1994. Agarics in Malesia. I. Tricholomatoid, II. Mycenoid. Beih Nov Hedwig 109:1–271. ACKNOWLEDGMENTS Desjardin DE. 1995. A preliminary accounting of the worldwide members of Mycena sect. Sacchariferae. We are grateful to FAPESP (Grant #01/04753-6) for Biblio Mycol 159:1–89. providing financial support to C.V. Stevani for this research. Ewart AJ. 1906. Note on the phosphorescence of Agaricus We thank Antoˆnio Modesto and Tadeu Gonçalves from (Pleurotus) candescens Mu¨ll. Victorian Nat 23:174. PETAR administration for facilitating access to the collect- Grgurinovic CA. 2002. The genus Mycena in South-Eastern ing sites and the Instituto Florestal for authorizing Australia. Hong Kong, PRC: Fungal Diversity Press. permission to collect in PETAR. We thank Joaõ R.L. Godoy, 329 p. Luiz Fernando Mendes, Ricardo Braga Neto and Jose´ Haneda Y. 1955. Luminous organisms of Japan and the Far Sanches for accompanying us in the field, for discovering East. In: Johnson FH, ed. The Luminescence of interesting specimens and for keeping us entertained. We Biological Systems. Washington, DC: American Associ- especially thank Joaquim B. Mendes Filho for guiding us in ation for the Advancement of Science. p 335–386. the dark through the forest without getting us lost. We are Herring PJ. 1994. Luminous fungi. Mycologist 8:181–183. grateful that Drs D. Jean Lodge and Sharon Cantrell let us Horak E. 1978. Mycena rorida (Fr.) Que´l. and related include their specimens of Mycena lucentipes from Puerto species from the southern hemisphere. Ber Schweiz Rico in this study, and we thank Dr Jefferson Prado Bot Ges 88(1/2):20–29. (Instituto de Botaˆnica) for reviewing the Latin diagnoses. Johnson MEM. 1919. On the biology of Panus stypticus. Trans British Mycol Soc 6:348–353. Joly CA, Aidar MPM, Klink CA, McGrath DG, Moeira AG, LITERATURE CITED Moutinho P, Nepstad DC, Oliveira AA, Pott A, Rodal Aidar MPM, Godoy JRL, Bergmann J, Joly CA. 2001. MJN, Sampaio EVSB. 1999. Evolution of the Brazilian Atlantic Forest succession over calcareous soil, Parque phytogeography classification systems: implications for Estadual Turı´stico do Alto Ribeira—PETAR, SP. Revta biodiversity conservation. Cieˆn Cultura 51:331–348. Brasil Bot Saõ Paulo 24(4):455–469. Josserand M. 1953. Sur la luminescence de ‘‘Mycena rorida’’ Barros MP, Bechara EJH. 1998. Bioluminescence as en Europe occidentale. Bull Mens Soc Linn Lyon 22: a possible auxiliary oxygen detoxifying mechanism in 99–102. elaterid larvae. Free Radic Biol Med 24(5):767–777. Kirk PM, Cannon PF, David JC, Stalpers JA. 2001. Dictionary DESJARDIN ET AL:BIOLUMINESCENT MYCENA SPECIES 331

of the Fungi. 9th ed. United Kingdom: CAB Interna- and conservation of eastern Brazilian coastal forest tree tional. 655 p. species. Brittonia 33:233–245. Kobayasi Y. 1951. Contributions to the luminous fungi from Oliveira Filho A, Fontes MA. 2000. Patterns of floristic Japan. J Hattori Bot Lab 5:1–6. differentiation among Atlantic Forests in southeastern Kornerup A, Wanscher JH. 1978. Methuen handbook of Brazil, and the influence of climate. Biotropica 32:793– colour. 3rd ed. London: Eyre Methuen. 252 p. 810. Lall AB, Ventura DSF, Bechara EJH, de Souza JM, Pegler DN. 1986. Agaric flora of Sri Lanka. Kew Bull Add Colepicolo-Neto P, Viviani VR. 2000. Spectral corre- Ser 12:1–519. spondence between visual spectral sensitivity and bio- Rees JF, de Wergifosse B, Noiset O, Dubuisson M, Janssens luminescence emission spectra in the click beetle B, Thompson EM. 1998. The origin of marine bio- Pyrophorus punctatissimus (Coleoptera: Elateridae). luminescence: turning oxygen defense mechanisms J Insect Physiol 46:1137–1141. into deep-sea communication tools. J Exp Biol 201: Lingle WL. 1989. Effects of veratryl alcohol on growth and 1211–1221. bioluminescence of Panellus stypticus. Mycol Soc Am Robich G. 2003. Mycena d’Europa. Trento, Italy: Associa- Newslett 40:36. (Abstract) zione Micologica Bresadola. 728 p. ———. 1993. Bioluminescence and ligninolysis during Seliger HH. 1975. The origin of bioluminescence. Photo- secondary metabolism in the fungus Panellus. chem Photobiol 21:355–361. J Biolumin Chemilumin 8:100. Shimomura O. 1992. The role of superoxide dismutase in Lloyd JE. 1974. Bioluminescent communication between regulating the light emission of luminescent fungi. fungi and insects. Florida Entomol 57:90. J Exp Bot 43:1519–1525. Lodge DJ. 1988. Three new Mycena species (Basidiomycota: Singer R. 1969. Mycoflora Australis. Beih Nov Hedwig 29:1– Tricholomataceae) from Puerto Rico. Trans Brit Mycol 405. Soc 91:109–116. ———. 1986. Agaricales in Modern Taxonomy. 4th ed. Maas Geesteranus RA. 1992. Mycenas of the Northern Koenigstein, Germany: Koeltz Scientific Books. 981 p. Hemisphere II. Conspectus of the Mycenas of the Sivinski JM. 1981. Arthropods attracted to luminous fungi. northern hemisphere. Verh Kon Ned Acad Wetensch, Psyche 88:383–390. Afd Natuurk, Tweede Reeks 90:1–493. ———, de Meijer AAR. 1997. Mycenae paranaenses. Verh ———. 1998. Phototropism, bioluminescence and the Kon Ned Acad Wetensch, Afd Natuurk, Tweede Reeks diptera. Florida Entomol 81:282–292. 97:1–164. SOS Mata Atlaˆntica. 1998, Evoluçaõ dos remanescentes ———, Winterhoff W. 1985. Eine neue Mycena-Art aus der florestais e ecossistemas associados do domıńio Mata Sektion Basipedes. Z Mykol 51(2):247–249. Atlaˆntica no perıódo 1990–1995. Saõ Paulo: Fundaçaõ McAlpine D. 1900. Phosphorescent fungi in Australia. Proc SOS Mata Atlaˆntica/INPE. Linn Soc New South Wales 25:548–558. Treu R, Agerer A. 1990. Culture characteristics of some McElroy WD, Seliger HH. 1962. Origin and evolution of Mycena species. Mycotaxon 38:279–309. bioluminescence. In: Kasha M, Pullman B, eds. Wassink EC. 1948. Observations on the luminescence in Horizons in Biochemistry. New York: Academic Press. fungi I, including a critical review of the species p 91–101. mentioned as luminescent in literature. Recueil Trav Me´trod G. 1949. Les Mycenes de Madagascar (Mycena, Bot Neérl 41:150–212. Corrugaria, Pterospora). Prod Flora Mycol Madagascar ———. 1978. Luminescence in fungi. In: Herring PJ, ed. 3:1–146. Bioluminescence in action. London: Academic Press. Moncalvo J-M, Vilgalys R, Redhead SA, Johnson JE, James p 171–197. TY, Aime MC, Hofstetter V, Verduin SJW, Larsson E, Weitz HJ. 2004. Naturally bioluminescent fungi. Mycologist Baroni TJ, Thorn RG, Jacobsson S, Cle´mencon H, 18:4–5. Miller OK Jr. 2002. One hundred and seventeen clades Wood KV. 1995. The chemical mechanism and evolutionary of euagarics. Mol Phylog Evol 23:357–400. development of beetle bioluminescence. Photochem Mori SA, Boom BM, Prance GT. 1981. Distribution patterns Photobiol 62(4):662–673.