Mycologia
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
DOI: 10.3852/mycologia.99.2.317
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Services
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Desjardin, D. E.
Right arrow Articles by Stevani, C.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Desjardin, D. E.
Right arrow Articles by Stevani, C.
Agricola
Right arrow Articles by Desjardin, D. E.
Right arrow Articles by Stevani, C.
Mycologia, 99(2), 2007, pp. 317-331.
© 2007 by The Mycological Society of America

Bioluminescent Mycena species from São Paulo, Brazil


Dennis E. Desjardin 1

     Department of Biology, San Francisco State University, San Francisco, California 94132, USA

Marina Capelari

     Instituto de Botânica, Caixa Postal 4005, 01061-970 São Paulo, SP, Brazil

Cassius Stevani

     Instituto de Química da Universidade de São Paulo, Caixa Postal 26077, 05599-970, São Paulo, SP, Brazil

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 

Six species of bioluminescent agarics are described and illustrated from a single site in primary Atlantic Forest habitat in the Parque Estadual Turístico do Alto Ribeira, São Paulo State, Brazil. These include two new taxa of Mycena, viz. M. asterina and M. lucentipes. Luminescence in Mycena fera, M. singeri and M. discobasis is reported for the first time. In addition an undeterminable luminescent Mycena species is described and additional specimens of Gerronema viridilucens are documented. An accounting of known bioluminescent species of Mycena and a discussion of why they luminesce are presented.

Key words: agarics, antioxidant defense, diversity, fungi, taxonomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Numerous species of Mycena form luminescent mycelium and/or basidiomes. By our count no fewer than 26 species of Mycena have been reported as bioluminescent (TABLE IGo), belonging to a least 13 taxonomic sections within Mycena sensu lato. To this accounting we add another six species of luminescent Mycena that belong to an additional three sections of the genus. The new reports represent material collected recently in old growth Atlantic Forest habitat in São Paulo State, Brazil.


View this table:
[in this window]
[in a new window]

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

 
At one time more than one million square kilometers of Brazil were covered in Atlantic Forest habitat, considered one of the three most threatened ecosystems in the world. Until relatively recently more than 82% of São Paulo State in southeastern Brazil was covered by forest, but today only about 7% of the region remains forested, primarily in mountainous regions near the coast (SOS Mata Atlantica 1998Go). In Dec–Apr 2001–2006 numerous collecting trips were made to Parque Estadual Turístico do Alto Ribeira (PETAR), São Paulo State, Brazil, in search of bioluminescent basidiomycetes. Our collecting sites were over calcareous soil in evergreen hygrophyllous forest classified as Dense Ombrophylous Forest by Joly et al (1999)Go. Dominant angiosperm families in this habitat include Myrtaceae, Leguminosae. Rubiaceae, Melastomataceae, Lauraceae, Sapotaceae, Euphorbiaceae, Moraceae and Annonaceae (Oliveira Filho and Fontes 2000Go, Aidar et al 2001Go). This forest type constitutes the most ancient and diverse ecosystem for Orchidaceae in South America (Brieger 1969Go) with high diversity and endemism indices (Mori et al 1981Go). To date we have documented the presence of eight bioluminescent species of agarics in PETAR. We are unaware of any other site in the world with equal or greater diversity of bioluminescent basidiomycetes. Herein we describe two new species of Mycena, report for the first time luminescence in Mycena fera Maas Geest. & de Meijer, M. singeri Lodge and M. discobasis Métrod, and provide data on two other luminescent agarics, viz. an undeterminable Mycena species and Gerronema viridilucens Desjardin, Capelari & Stevani.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
All basidiomes were collected at night in near total darkness and were detected in the field as sources of green luminescence. Specimens were placed in plastic collecting boxes in the field for transport back to the field laboratory. All fresh specimens then were photographed in lighted conditions with aid of a flash, and in dark conditions with 20–50 min exposures. Photos were taken with a Nikon N80 camera equipped with a Nikkor AF Zoom 28–105 mm lens, with Fuji Superia ASA 400 or ASA 800 color print film at f5.5 and f11. Fresh specimens were maintained in cool conditions until the next morning when macromorphological data were documented in daylight. Color terms and notations in parentheses are those of Kornerup and Wanscher (1978)Go. The terms used to describe lamellae spacing refer to the number of lamellae that reach from the stipe to the pileus margin (primaries) and do not include the lamellulae, whose spacing is indicated by the number of series present. All measurements and colors reported for microscopic features were made from dried material rehydrated in 100% ethanol followed by distilled water, 3% KOH, 3% KOH + Congo red, or Melzer’s reagent. Spore statistics include: x, the arithmetic mean of the spore length by spore width (± standard deviation) for n spores measured in a single specimen; xmr, the range of spore means and xmm, the mean of spore means (±SD) where more than one specimen is available; Q, the quotient of spore length and spore width in any one spore, indicated as a range of variation in n spores measured; Qm, the mean of Q-values in a single specimen; Qmr, the range of Qm values and Qmm, the mean of Qm values where more than one specimen is available. Specimens are deposited in SP and SFSU.


   TAXONOMY
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 TAXONOMY
DISCUSSION
 LITERATURE CITED
 
Mycena asterina Desjardin, Capelari et Stevani, sp. nov. FIGS. 1a–bGo, 7a–gGo


Figure 1
View larger version (105K):
[in this window]
[in a new window]

  		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 = twice natural size (2x); 5–6 = natural size (1x).

 

Figure 2
View larger version (26K):
[in this window]
[in a new window]

  		FIG. 7. Mycena asterina (DED 7821 – HOLOTYPE). a. Primordium (2x), developing (2x) and mature (1x) basidiomes. b. Basidiospores. c. Basidia and basidioles. d. Cheilocystidia. e. Cherocytes. f. Acanthocysts. g. Caulocystidium. Bar = 10 µm.

 
Primordium 0.5–1.5 mm latus x 0.2–2.0 mm altus, hemisphaericum, album pallide flavotinctum, elementis veli universalis cylindraceis dense obtectis. Pileus 1.0–3.5 mm latus, obtusus conicus raro convexus, striatus vel sulcatus, siccus, minute pulverulentus, glabrescens, albus, centro pallide flavotinctis, viridis luminosus. Caro pertenuis, alba. Lamellae adscendentes, subliberae, confertae vel subdistantes, angustatae (0.5–0.75 mm), albae, margine concolores, viridae luminosae. Stipes 10–30 x 0.2–0.5 mm, fragilis, cylindraceus, albus; apice aequali, glaber; basi pubescens, subbulbosus, haud luminosus. Basidiosporae 8.2–11.5 x 3.5–5 µm, ellipsoideae vel subfusoideae, leves, hyalinae, amyloideae. Basidia 12–15 x 9–11 µm, subglobosa vel late clavata, 2- vel 4-sporigera, fibulata. Cheilocystidia 15–22 x 8.5–14 µm, late clavata vel ovoidea, dense spinulosae, surculis cylindraceis, recti 0.5 x <0.5 µm instructa, hyalinae. Pleurocystidia nulla. Pileipellis hymeniformis ex acanthocystides 16–35 x 17–38 µm, globosae vel ovoideae, dense spinulosae. Velum universale e cherocytibus tenuitunicatis vel crassetunicatis formatum, superioribus spinuliferis 22–50 x 12–25 µm, fibulata. Trama lamellarum dextrinoidea. Hyphae stipitis corticales 4–7.5 µm latae, leves, dextrinoidea. Caulocystidia 60–275 x 5–8 µm, cylindracea, dense spinulosa. Foliicola. Holotypus hic designatus: D.E. Desjardin 7821 (SP #307997; isotypus SFSU).

Primordia (FIG. 7aGo) 0.5–1.5 mm diam x 0.5–2.0 mm tall, hemispherical to ovoid, white to pale yellowish white (<4A2) overall, covered with short universal veil spines; spines detersile, cylindrical or subcylindrical to narrowly conical, straight or curved, sometimes agglutinated together to form larger and coarser spines, base and marginal area of primordia with shorter spines or lacking spines. Pileus (FIGS. 1a–bGo, 7aGo) 1.0–3.5 mm diam, obtusely conical, seldom convex, striate or sulcate, minutely and finely granulose overall, lacking universal veil spines at maturity, dull, dry; disk pure white or pale yellowish white (<4A2), pure white elsewhere, sometimes developing pale yellowish white tones overall when dried; strongly greenish-white luminescent. Context extremely thin, white. Lamellae ascending, subfree, close to subdistant with 1–2 series of lamellulae, narrow (0.5–0.75 mm), white, nonmarginate; strongly greenish-white luminescent. Stipe 10–30 x 0.2–0.5 mm, central, filiform, terete, cylindrical for most of the length, base subclavate to subbulbous, sometimes arising from a small circular pad of mycelium, fragile, translucent, dull, dry; apex glabrous, base with scattered, white strigose hairs; pure white overall or seldom with the base faintly pale grayish white under the white hairs; not luminescent.

Basidiospores (FIG. 7bGo) 8.2–11.5 x 3.5–5 µm (xmr = 8.8–10 x 4.0–4.3 µm, xmm = 9.4 ± 0.8 x 4.1 ± 0.2 µm, Q = 2.0–3.0, Qmr = 2.22–2.34, Qmm = 2.28 ± 0.08, n = 20 spores per 2 specimens), a few spores putatively from 2-spored basidia 12.8–14.4 x 4–5 µm, elongate-ellipsoid to subfusoid, smooth, hyaline, amyloid, thin-walled. Basidia (FIG. 7cGo) 12–15 x 9–11 µm, subglobose to ovoid or broadly clavate, 2- and 4-spored, refractive, clamped. Basidioles subglobose to ovoid. Cheilocystidia (FIG. 7dGo) common, 15–22 x 8.5–14 µm, ovoid to broadly clavate, covered over the upper 1/3–1/2 with tiny spinulae; spinulae 0.5 x <0.5 µm, wart-like to obtusely cylindrical; hyaline, thin-walled. Pleurocystidia absent. Universal veil composed of chains of cherocytes, conspicuous on primordia, rarely present on mature pilei; cherocytes (FIG. 7eGo) 22–50 x 12–25 µm, subglobose to ovoid or broadly clavate, rarely subcylindrical, 3–7 per chain, terminal and penultimate cells often slightly thick-walled (0.5–1 µm) and with scattered spinulae, remaining cells thin-walled and typically smooth or with few spinulae, clamped; spinulae 1–8 x 0.5–1.5 µm, cylindrical to subconical, thin-walled; all cells hyaline, inamyloid. Pileipellis a hymeniform layer of acanthocysts; acanthocysts (FIG. 7fGo) 16–35 x 17–38 µm, globose to ovoid, thin-walled and often collapsed, hyaline, inamyloid, covered over upper 3/4 with dense spinulae; spinulae 0.5–1 x 0.5 µm, wart-like to obtusely cylindrical, hyaline; acanthocysts on pileus margin 17–25 x 10–17 mm, clavate, thin-walled, less spinulose than cheilocystidia or other pileipellis acanthocysts. Pileus and lamellar trama of dextrinoid hyphae 10–16 µm diam, hyaline, nongelatinous, nonincrusted. Stipitipellis composed of repent cortical hyphae giving rise to numerous caulocystidia; stipe cortical hyphae parallel, 4–7.5 µm diam, smooth (nonspinulose), hyaline, dextrinoid, slightly thick-walled, nongelatinous, nonincrusted; stipe medullary hyphae similar but 8–20 µm diam; caulocystidia (FIG. 7gGo) 60–275 x 5–8 µm, 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 x 0.5 µm, 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. São Paulo State, Brazil.

Specimens Examined. – BRAZIL. SÃO PAULO STATE: Mun. Iporanga, Parque Estadual Turístico do Alto Ribeira (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, S24°33.51', W048°43.54', 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 [EC] (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 = 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 Amparoina (Desjardin 1995Go), where it is allied most closely with M. propinqua Maas Geest. & de Meijer (1997)Go. The latter species was described recently from material collected in a mixed ombrophilous forest in Paraná State, due south of where the type material of M. asterina was collected. Mycena propinqua differs from M. asterina in forming pilei with gray disk and striae, thicker-walled cherocytes, cheilocystidia with fewer spinulae, slightly smaller basidiospores with Q = 2.0, and unclamped basidia. In addition M. propinqua was not reported as bioluminescent (Maas Geesteranus and de Meijer 1997Go).

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 Kobayasi (1951, Mycena daisyogunensis Kobayasi and M. pseudostylobates Kobayasi), but the taxonomic affinities of these species remain uncertain (see Desjardin 1995Go, pages 78 and 85, respectively).

Mycena discobasis Métrod, Les Mycènes de Madagascar:131. 1949. FIGS. 2a–bGo, 8a–eGo


Figure 3
View larger version (24K):
[in this window]
[in a new window]

  		FIG. 8. Mycena discobasis (Stevani 08.04.05.4). a. Basidiospores. b. Basidium and basidioles. c. Cheilocystidia. d. Pileipellis terminal cells (pileocystidia). e. Caulocystidia. Bar = 10 µm.

 
Pileus (FIGS. 2a–bGo) 7–12 mm diam, convex, soon planoconvex 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 x 1–1.5 mm, central, terete, cylindrical, ±equal 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. 8aGo) (8.5–)9–10.5(–11) x 6–7.5 µm (xm = 9.9 ± 0.6 x 6.7 ± 0.4 µm, Q = 1.3–1.6, Qm = 1.4 ± 0.11, n = 25 spores per one specimen), broadly ellipsoid, smooth, hyaline, amyloid, thin-walled. Basidia (FIG. 8bGo) 22–26 x 9.8–11.2 µm, broadly clavate, 4-spored, clamped. Basidioles broadly clavate. Lamellar edge sterile; cheilocystidia (FIG. 8cGo) 22–42(–48) x 10–19 µm, broadly clavate to ventricose-rostrate, smooth (lacking diverticula or spinulae), apex not branching, hyaline, inamyloid, lacking pigmented contents, nongelatinous, thin-walled. Pleurocystidia absent. Pileipellis a cutis of smooth to sparsely spinulose, loosely interwoven hyphae embedded in a gelatinous matrix up to 100 µm thick, giving rise to terminal pileocystidia; hyphae 1.5–3 µm diam, cylindrical or irregular in outline, branched, hyaline, inamyloid to weakly dextrinoid, thin-walled; pileocystidia (FIG. 8dGo) 22–50 x 5–10 µm, subcylindrical to clavate, densely spinulose, hyaline; spinulae 2–6 x 1–1.5 µm, cylindrical to strangulate, obtuse, sometimes branched, unevenly distributed, hyaline. Hypodermium of hyphae inflated up to 18 µm diam, dextrinoid. Pileus trama of interwoven hyphae 4–18 µm diam, cylindrical, hyaline, dextrinoid, nongelatinous. Lamellar trama regular; hyphae 5–20 µm diam, inflated, hyaline, strongly dextrinoid, nongelatinous, thin-walled. Stipe cortical hyphae 3–8 µm diam, parallel, cylindrical, smooth, hyaline, inamyloid to dextrinoid, nonincrusted, non-gelatinous. Stipe medullary hyphae similar but up to 30 µm diam. Caulocystidia (FIG. 8eGo) absent at stipe apex, scattered on stipe base, 43–165 x 11–18.5 µm, fusoid to fusoid-ventricose, obtuse or acute, smooth, hyaline, inamyloid, thin-walled. Clamp connections present in all tissues.

Habit, habitat and distribution. – Solitary, scattered on bark and rotten wood of dead undetermined dicotyledonous plants in disturbed primary Atlantic Forest habitat. April. São Paulo State, Brazil.

Specimen Examined. – BRAZIL. SÃO PAULO STATE: Mun. Iporanga, Parque Estadual Turístico do Alto Ribeira (PETAR), Núcleo Santana, S24°32.048', W048°42.071', elev. ca. 250 m, 8 Apr 2005, coll. by C. Stevani et al, C. Stevani 08.04.05.4 [EC] (SP #308010; SFSU).

Commentary. – Métrod (1949)Go described M. discobasis from 5 basidiomes collected by Roger Heim in Madagascar in 1934 (stored in alcohol at P) and because of the stipe basal disk include it in sect. Basipedes. Diagnostic features of Mycena discobasis include: a white, planoconvex, striate, umbilicate pileus; nearly free, close, white lamellae; a white, sparsely pubescent stipe that arises from a flattened pad of radiating mycelium; relatively large, amyloid basidiospores with mean 9.9 x 6.7 µm; broadly clavate to ventricose-rostrate cheilocystidia lacking diverticula or spinulae; dextrinoid lamellar trama; a gelatinized, loosely interwoven pileipellis with densely spinulose pileocystidia; smooth stipe cortical hyphae giving rise to fusoid-ventricose, nonspinulose caulocystidia; clamp connections; and green luminescence of the stipe apex, stipe base and lamellar edges. Our material from São Paulo State, Brazil, differs only subtly from the Madagascar material in forming slightly larger basidiospores. Mycena discobasis was reported by Métrod to have basidiospores measuring 7.5–9.5 x 6.5 µm. In addition the species was not reported as luminescent. As far as we are aware this is only the second published report of M. discobasis. We cannot explain the disjunct distribution.

In combination the taxonomically significant features of M. discobasis indicate that it is closely allied with M. chlorophos (Berk. & M.A. Curtis) Sacc. in sect. Exornatae. Mycena chlorophos, a widespread luminescent species reported from Japan (type from Bonin Islands, Berkeley and Curtis 1860Go), Sri Lanka (Pegler 1986Go), Borneo, Malaysia and Micronesia (Corner 1954Go, 1994Go) and Brazil (Maas Geesteranus and de Meijer 1997Go) differs by forming fuscous brown to pale grayish brown pilei, has cheilocystidia near the pileus margin with apical appendages and forms smaller basidiospores of 7–9 x 5–6 µm (ibid; isotype FH!). The European M. rhenana Maas Geest. & Winterh. and the Australasian M. interrupta (Berk.) Sacc. are similar to M. discobasis; although neither of the former species have been reported as luminescent. Mycena rhenana, currently placed in sect. Basipedes, differs in lacking cheilocystidia, and in forming smaller pilei (<6 mm broad), smaller basidiospores (6.5–8 x 3.7–5 µm) and marginal pileocystidia with nonspinulose, acuminate apices ( fide Maas Geesteranus and Winterhoff 1985Go, Robich 2003Go). Mycena interrupta, currently placed in sect. Cyanocephalae (synonymous with M. cyanocephala Singer, type of sect. Cyanocephalae), differs in forming pilei, lamellar edges and stipe basal disk with pale blue pigmentation, and differs in forming spinulose cheilocystidia and a nongelatinized pileipellis (fide Singer 1969Go, Grgurinovic 2002Go). Based on overall phenetic similarities, we suggest that M. rhenana and M. interrupta are better placed with M. chlorophos and M. discobasis in sect. Exornatae and both should be checked for luminescence.

Mycena fera Maas Geest. & de Meijer, Verh. Kon. Ned. Acad. Wetensch., Afd. Natuurk., Tweede Reeks 97:31. 1997. FIGS. 3a–bGo, 9a–eGo


Figure 4
View larger version (24K):
[in this window]
[in a new window]

  		FIG. 9. Mycena fera (Stevani 04.01). a. Basidiomes (1x). b. Basidiospores. c. Basidia and basidiole. d. Cheilocystidia. e. Pileipellis and stipitipellis hyphae. Bar = 10 µm.

 
Pileus (FIGS. 3a–bGo, 9aGo) 4–8 mm diam, obtusely conical to campanulate or convex with a small rounded umbo, rugulose, striate, dull to subshiny, dry to moist (rarely subviscid), glabrous; disk pale grayish yellow (5D3) to pale yellowish brown (5E4-6) or brown (6E5-8), margin pale grayish orange (5B3) to light brown (5-6D4-5), grayish brown (6D3) or beige. Context thin, white. Lamellae ascending, broadly adnate, distant (8–11 primaries) with 0–1 series of lamellulae, broad (1–1.25 mm), white to pale grayish white or buff, nonmarginate. Stipe 10–15 x 1 mm, central, terete, ±equal, cylindrical, hollow, dull, dry, glabrous, noninsititious, arising from a pad of white mycelium; pale grayish orange (5B3) to light yellowish brown (5D4-5) or beige. Entire basidiome emitting a bright, greenish-white luminescence.

Basidiospores (FIG. 9bGo) (9–)9.5–11.5(–12.5) x 9–11(–12) µm [xmr = 10.3–10.6 x 10.1–10.3 µm, xmm = 10.5 ± 0.2 x 10.2 ± 0.1 µm, Q = 1.0–1.1, Qmr = 1.02–1.03, Qmm = 1.02 ± 0.01, n = 20–25 spores per 2 specimens], globose to slightly subglobose, smooth, sometimes with a single large guttule, hyaline, amyloid, thin-walled. Basidia (FIG. 9cGo) 31–35 x 11–12.5 µm, clavate, 4-spored, clamped. Basidioles clavate. Cheilocystidia (FIG. 9dGo) common, lamellar edge sterile; main body 25–50 x 8.5–16 µm, clavate to broadly clavate with 3–6 apical projections, hyaline, thin-walled; projections 5–22 x 2.5–4.5 µm, irregularly cylindrical, sometimes lobed or knobby, obtuse. Pleurocystidia absent. Pileipellis (FIG. 9eGo) a cutis of repent, cylindrical hyphae 3–8 µm diam, with scattered diverticula, slightly gelatinous to gelatinous, nonincrusted, hyaline, inamyloid; diverticula 5–20 x 1–4 µm, irregularly cylindrical, sometimes forked, often curved. Hypodermium well developed, composed of short-celled hyphae 12–34 µm diam, hyaline, dextrinoid, thin-walled, sometimes with brown plasmatic pigments. Pileus trama of loosely interwoven hyphae 6–17 µm diam, cylindrical to inflated, non-gelatinous, nonincrusted, hyaline, inamyloid to weakly dextrinoid, thin-walled. Lamellar trama of inflated hyphae 7–30 µm diam, dextrinoid, otherwise similar to pileus trama hyphae. Stipe cortical hyphae (FIG. 9eGo) parallel, 3–6 µm diam, cylindrical, with scattered diverticula, nongelatinous, nonincrusted, hyaline, dextrinoid; diverticula 4–22 x 1.5–4 µm, irregularly cylindrical, often forked, thin-walled. Stipe medullary hyphae parallel, 4–16 µm diam, cylindrical, hyaline, dextrinoid; with scattered, refractive, yellow oleiferous hyphae 2–4 µm 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. São Paulo State, Brazil.

Specimens Examined. – BRAZIL. SÃO PAULO STATE: Mun. Iporanga, Parque Estadual Turístico do Alto Ribeira (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, S24°33.51', W048°43.54', 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 [EC] (SP #380147; preserved in alcohol); same location, 26 Mar 2006, C. Stevani 26.03.06.05 [EC] (SP#380285); PETAR, Núcleo Santana, S24°32.048', W048°42.071', elev. ca. 250 m, 8 Apr 2005, coll. by C. Stevani et al, C. Stevani 08.04.05.1 [EC] (SP #308007); same location, 8 Apr 2005, coll. by C. Stevani et al, C. Stevani 08.04.05.2 [EC] (SP #308008); PETAR, Poço Veado, Poço da Viúva, 26 Mar 2006, C. Stevani 26.03.06.02 [EC] (SP #380282).

Commentary. – Mycena fera was described recently from a single specimen collected on a decayed branch of a dicotyledonous tree in Paraná State, just south of where we collected it on fern rootlets and tree bark in São Paulo State, Brazil. Maas Geesteranus and de Meijer (1997)Go 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 lamellar edges. Pileus coloration is variable, with some basidiomes showing pale grayish yellow tones whereas others are brown.

Mycena lucentipes Desjardin, Capelari et Stevani, sp. nov. FIGS. 4a–bGo, 10a–dGo


Figure 5
View larger version (27K):
[in this window]
[in a new window]

  		FIG. 10. Mycena lucentipes (DED 7828 – HOLOTYPE). a. Basidiomes (1x). b. Basidiospores. c. Basidia and basidiole. d. Caulocystidia. Bar = 10 µm.

 
Pileus 4–12 mm latus, conicus vel convexus, dein campanulatus vel planoconvexus, papillatus vel umbonatus, pellucid-striatus, hygrophanus, glaber, siccus, brunneus vel fulvus, dein umbrinus. Caro pileo concolor. Lamellae 8–13 stipitem attingentes, arcuatae vel decurrentae, distantes vel subdistantes, usque ad 1.5 mm latae, dein subintervenosae, pallide griseoaurantiaceae vel fulvae, margine concolores. Stipes 8–25 x 1–1.5 mm, fragilis vel flexibilis, aequalis, cylindraceus, pruinosus vel hispidulus, siccus, cremeus vel pallide fulvus, denum brunneus, fibrillis fulvis substrato affixus, viridis luminosus. Basidiosporae 7.5–10 x 3.5–5 µm, inaequilateraliter ellipsoideae, leves, hyalinae, amyloideae. Basidia 32–38 x 7.5–10 µm, clavata, 4-sporigera, fibulata. Cheilocystidia nulla. Pleurocystidia nulla. Hyphae pileipellis 5–12 µm latae, leves, haud gelatinosae, inamyloidae, fibulatae. Trama lamellarum iodi ope haud vinescens. Hyphae stipitis corticales 3–8 µm latae, leves, inamyloidea, haud gelatinosae. Caulocystidia 15–40 x 7.5–11.5 µm, clavata vel ventricosa, geniculata, tenuitunicata. Ramulicola. Holotypus hic designatus: D.E. Desjardin 7828 (SP #308004; isotypus SFSU).

Pileus (FIGS. 4a–bGo, 10aGo) 4–15(–20) mm diam, at first conical to convex-papillate, soon becoming campanulate to planoconvex with a prominent papilla or umbo; papilla or umbo conical to obtuse; margin decurved, entire, pellucid-striate to striate; surface hygrophanous, glabrous, moist to dry; when young 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 x 1–1.5(–1.75) mm, central, terete, ±equal 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. 10bGo) (6.0–)6.5–10 x 3.5–5.5 µm (xmr = 7.4–8.9 x 4.2–4.9 µm, xmm = 8.3 ± 0.6 x 4.5 ± 0.3 µm, Q = 1.3–2.6, Qmr = 1.5–2.1, Qmm = 1.86 ± 0.3, n = 20–25 spores per 8 collections), ellipsoid to broadly ellipsoid or elongate-ellipsoid, inequilateral, smooth, hyaline, amyloid or weakly amyloid, thin-walled, white in deposit. Basidia (FIG. 10cGo) 32–38 x 7.5–10 µm, clavate, 4-spored with sterigmata up to 5 µm long, clamped. Basidioles clavate. Cheilocystidia absent; lamellar edge fertile. Pleurocystidia absent. Pileipellis a cutis of repent, smooth hyphae 5–12 µm diam, nondiverticulate, occasionally with one or more low, broad bumps, nongelatinous, nonincrusted, hyaline, inamyloid, thin-walled; overlaying a poorly developed or undifferentiated hypodermium of broader (12–20 µm diam), weakly dextrinoid hyphae. Pileus trama of hyphae 8.5–18 µm diam, little differentiated from the pileipellis or hypodermium, loosely interwoven, hyaline, inamyloid. Lamellar trama regular; hyphae 6–15(–18) µm diam, subparallel, hyaline, inamyloid or weakly dextrinoid in some basidiomes, nongelatinous, thin-walled. Stipitipellis composed of repent hyphae giving rise to numerous erect caulocystidia; stipe cortical hyphae 3–8 µm diam; stipe medullary hyphae 6–13 µm diam; stipe hyphae parallel, smooth, nongelatinous, nonincrusted, hyaline, inamyloid, thin-walled. Caulocystidia (FIG. 10dGo) solitary or clustered, 15–40 x 7.5–11.5 µm, irregularly clavate or ventricose, obtuse, often geniculate, as terminal cells or intercalary outgrowths, hyaline, inamyloid, thin-walled. Clamp connections common in all tissues.

Habit, habitat and distribution. – Solitary to subcespitose or in cespitose clusters of 5–30 basidiomes, lignicolous on rotted sticks or on rootlets of undetermined dicotyledonous plants in disturbed primary Atlantic Forest habitat or in riparian habitats. Dec–Apr in Brazil; Oct–Jan in Puerto Rico.

Specimens Examined. – BRAZIL. SÃO PAULO STATE: Mun. Iporanga, Parque Estadual Turístico do Alto Ribeira (PETAR), Núcleo Santana, S24°32.048', W048°42.071', elev. ca. 250 m, 9 Mar 2005, coll. by C. Stevani et al, D.E. Desjardin 7828 (Holotype: SP #308004, Isotype: SFSU); same location, 1 Dec 2004, C. Stevani 01.12.04.02 [EC] (SP #380148); same location, 9 Apr 2005, C. Stevani 09.04.05.5 [EC] (SP #308011); same location, 9 Apr 2005, C. Stevani 09.04.05.6 [EC] (SP #308012); PETAR, ca. 12 km from Bairro da Serra on Lajeado Road, S24°33.51', W048°43.54', elev. ca. 500–530 m, 8 Mar 2005, coll. by C. Stevani et al, D.E. Desjardin 7820 (SFSU, SP #307996); MATO GROSSO DO SUL STATE: Mun. Costa Rica, Cachoeira Salto, 8 Dec 2002, 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, S18°18'33'', W65°46'30'', 4 Oct 1997, coll. by S. Cantrell, A. Perez and mycology class, PR-4678 (SFSU, CFMR); same location, 13 Jan 1998, coll. by S. Cantrell, PR-5726 (SFSU)

Commentary. – Mycena lucentipes currently is known from Puerto Rico south to São Paulo, Brazil. It is characterized by basidiomes with these combination of features: campanulate-papillate pilei colored yellowish or orangish brown to brown; arcuate to decurrent, light brown to yellowish brown lamellae; subcespitose to cespitose, hispidulous stipes; pileipelles of nondiverticulate, repent hyphae; relatively undifferentiated pileus tissues; an absence of hymenial cystidia; ellipsoid, amyloid basidiospores; abundant caulocystidia; and strongly luminescent stipes. Pileus coloration and spore size varies with geographical area. In the southern populations from old growth primary Atlantic Forest area in São Paulo State, pilei are yellowish brown to brown and basidiospores show mean size 8.7 x 4.2 µm with a Q-value of 2.07. In the population from a riparian habitat in a secondary forest in the more northerly Mato Grosso do Sul State, Brazil, pilei show orange to orangish brown colors, and the basidiospores are smaller and less elongate with mean size 7.6 x 4.5 µm and a Q-value of 1.66. In Puerto Rico populations the pilei range from orangish brown to olive brown, and basidiospores are typically intermediate in length but broader with mean size 8.0 x 4.9 µm with a Q-value of 1.61. Until more specimens throughout the range of the species become available, and definitive molecular data are generated, we accept the populations as representing a widely distributed, morphologically variable species.

Mycena lucentipes is phenetically most similar to M. diversa Maas G. & de Meijer, the type species of a new section Diversae Maas G. & de Meijer (1997)Go, and we tentatively accept M. lucentipes in that section. Mycena diversa differs from M. lucentipes in forming grayish brown to pale gray, planoconvex pilei, white lamellae, and prominent lageniform cheilocystidia. In addition M. diversa was not reported as luminescent. Only the stipes and mycelia are luminescent in M. lucentipes, but they glow so brightly that the pileus and lamellae appear faintly luminescent in photographs. Maas Geesteranus and de Meijer (1997)Go suggested that sect. Diversae is allied with sect. Exornatae Maas G., a monotypic section based on M. chlorophos (Berk. & M.A. Curtis) Sacc. (see commentary for M. discobasis above). Mycena chlorophos is a widely distributed luminescent species, reported by Corner (1954)Go and Maas Geesteranus and de Meijer (1997)Go from Brazil. We have not seen material of the latter species from São Paulo State.

Mycena singeri Lodge, Trans Brit Mycol Soc 91:111. 1988. FIGS. 5a–bGo, 11a–eGo


Figure 6
View larger version (20K):
[in this window]
[in a new window]

  		FIG. 11. Mycena singeri (Stevani 08.04.05.3). a. Basidiospores. b. Basidia and basidiole. c. Cheilocystidia. d. Pileus marginal cells. e. Caulocystidia. Bar = 10 µm.

 
Only two mature basidiomes studied. Pileus (FIG. 5a–bGo) 8–10 mm diam, obtusely conical, expanding to nearly plane with or without a low obtuse umbo, sulcate, dull, dry, glabrous or minutely granulose; disc pinkish brown, margin pinkish red, elsewhere pinkish buff. Context thin, white. Lamellae adnate with a decurrent tooth to subdecurrent, distant (8–9 primaries) with one series of lamellulae, moderately broad, white with red margins. Stipe 18–22 x 1 mm, central, terete, cylindrical, dull, dry, glabrous to minutely pruinose overall, noninsititious, arising from white basal mycelium; white to buff overall. Stipe and lamellar edges emitting a bright, greenish-white luminescence.

Basidiospores (FIG. 11aGo) 7–9.5 x 6.5–8.5 µm (xm = 8.3 ± 0.8 x 7.5 ± 0.6 µm, Q = 1.0–1.2, Qm = 1.1 ± 0.07, n = 25 spores per one specimen), globose to subglobose, hyaline, amyloid, thin-walled. Basidia (FIG. 11bGo) 25–32 x 9.5–11 µm, clavate, 4-spored with sterigmata up to 5 µm long, clamped. Basidioles broadly clavate. Cheilocystidia (FIG. 11cGo) common, 24–45 x 8–22 µm, versiform, vesiculose to broadly clavate, lageniform, fusoid or irregular in outline, often bifid, with 1–3 broadly rounded lobes or projections, hyaline or with pinkish brown contents, inamyloid, thin-walled. Pleurocystidia present as a few cells similar to the cheilocystidia near the lamellar edges, absent further back on lamellar faces. Pileipellis a thin cutis of repent hyphae with uncommon projections, terminal pileocystidia and marginal cells; hyphae 3–7 µm diam, cylindrical, smooth or with a few scattered knob-like projections, nongelatinous, nonincrusted, hyaline, inamyloid; pileocystidia as terminal cells or intercalary projections, erect to repent, clavate to irregular in outline, similar to pileus marginal cells; edge of pileus with distinctive marginal cells (FIG. 11dGo) like the cheilocystidia, 28–45 x 5–24 µm, broadly clavate, ventricose, fusoid or irregular and often bifid, hyaline, inamyloid, thin-walled. Hypodermium well developed, composed of hyphae inflated up to 30 µm diam, hyaline, strongly dextrinoid, thin-walled, nongelatinous. Pileus trama of interwoven hyphae 3–7 µm diam, sometimes inflated up to 20 µm, weakly dextrinoid. Lamellar trama regular; hyphae 6–38 µm diam, hyaline, strongly dextrinoid. Stipe cortical hyphae 3–10 µm diam, parallel, cylindrical, hyaline, dextrinoid, nongelatinous, nonincrusted; giving rise to abundant terminal caulocystidia and intercalary projections (FIG. 11eGo), 8–40 x 5–10 µm, clavate, broadly rounded, sometimes bifid, hyaline, lacking pigmented contents, inamyloid, thin-walled. Stipe medullary hyphae 6–18 µm 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. São Paulo State, Brazil.

Specimens Examined. – BRAZIL. SÃO PAULO STATE: Mun. Iporanga, Parque Estadual Turístico do Alto Ribeira (PETAR), Núcleo Santana, S24°32.048', W048°42.071', elev. ca. 250 m, 8 Apr 2005, coll. by Stevani et al, C. Stevani 08.04.05.3 [EC] (SP 308009).

Commentary. – Only two mature basidiomes of M. singeri were collected from old growth Atlantic Forest habitat in São 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 1954Go). 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 µm long), more numerous pileocystidia and darker pilei (pale purplish brown; fide Corner 1954Go). Mycena noctilucens differs also in forming slightly smaller and more ellipsoid basidiospores, and numerous ventricose-subulate pleurocystidia (fide Corner 1954Go). Lodge (1988)Go did not report M. singeri as luminescent; hence this is the first report of luminescence for this species.

A description of the following species, known at present from a single immature or sterile basidiome, is presented below because it represents another bioluminescent Mycena species from the Atlantic Forest habitat of São Paulo State, Brazil. Sporulating specimens of this interesting species are required before a definitive identification can be made.

Mycena sp. FIGS. 6a–bGo, 12a–cGo


Figure 7
View larger version (26K):
[in this window]
[in a new window]

  		FIG. 12. Mycena species (Stevani 27.03.04). a. Basidiomes (1x). b. Basidioles. c. Cheilocystidia. Bar = 10 µm.

 
Macroscopic features compiled from several photographs of a fresh basidiome. Pileus (FIGS. 6a–bGo, 12aGo) 10 mm diam, acutely conical, striate, dull, dry, glabrous; dark brown to nearly black overall. Lamellae adnexed, close, narrow, white. Stipe 20 x 2 mm, central, terete, cylindrical, dull, dry, glabrous, noninsititious, base with white mycelium; dark gray to dark grayish brown or nearly black overall. Only the stipe apex and stipe base emit a green luminescence.

Exsiccata preserved in alcohol. Basidiospores not observed; specimen immature or sterile. Basidia not observed. Basidioles (FIG. 12bGo) 28–32 x 6–8 µm, clavate, unclamped. Cheilocystidia (FIG. 12cGo) common (lamellar edge sterile), 12–22 x 8.5–12.5 µm, broadly clavate to vesiculose or irregular in outline, sometimes lobed, with or without 2–5 broadly rounded knobs, nongelatinous, hyaline, thin-walled, unclamped. Pleurocystidia absent. Pileipellis a cutis of smooth or sparsely diverticulate hyphae 3.5–8 µm diam, nongelatinous, nonincrusted, hyaline, inamyloid, thin-walled, overlaying a well developed pseudo-parenchymatous hypodermium. Hypodermium composed of short-celled hyphae up to 20 µm diam, pale grayish brown, strongly dextrinoid, thin-walled. Pileus trama of interwoven hyphae 4–18 µm diam, hyaline, inamyloid to weakly dextrinoid. Lamellar trama regular; hyphae similar to those in pileus trama, dextrinoid. Stipe cortical hyphae parallel, 3–6 µm diam, cylindrical, smooth (nondiverticulate), nongelatinous, nonincrusted, hyaline to grayish brown, inamyloid to weakly dextrinoid, thin-walled. Stipe medullary hyphae parallel, 6–20 µm 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. São Paulo State, Brazil.

Specimen Examined. – BRAZIL. SÃO PAULO STATE: Mun. Iporanga, Parque Estadual Turístico do Alto Ribeira (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, S24°33.51', W048°43.54'', 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 a single, immature or sterile basidiome lacking basidiospores. Distinctive features include a nearly black basidiome with white, adnexed lamellae, relatively small, broadly lobed or knobby cheilocystidia, smooth to sparsely diverticulate pileipellis hyphae, smooth stipe cortical hyphae, and an absence of clamp connections, pleurocystidia and caulocystidia. In combination these features suggest that the species belongs in Mycena sect. Fragilipedes, where it might be allied with M. deusta Maas G. & de Meijer (1997Go: 59). Of interest, only the stipe apex and stipe base of Mycena sp. are green-luminescent.

To date only two species of sect. Fragilipedes have been reported as bioluminescent, viz. M. polygramma (Bull. : Fr.) S.F. Gray (Bothe 1931Go) and M. zephirus (Fr. : Fr.) Kummer (Bothe 1931Go). For both of the latter species, only the mycelium was reported as luminescent.

Gerronema viridilucens Desjardin, Capelari & Stevani, Fungal Diversity 18:10. 2005.

This species, described recently from material collected at PETAR, is common on the bark of living Eugenia fluminensis O. Berg. trees. It is characterized by these features: small, reddish brown basidiomes (reminiscent of Xeromphalina) with decurrent, distant lamellae, basidiospores in the range 7–9.5 x 4.5–5.5 µm, the absence of hymenial cystidia, the presence of clamp connections, negative KOH reactions on all basidiome surfaces, and an intense green luminescence. We currently are analyzing the metabolic pathway resulting in luminescence in this species based on cultures isolated from fresh material. Additional specimens include: BRAZIL. SÃO PAULO STATE: Mun. Iporanga, Parque Estadual Turístico do Alto Ribeira (PETAR), ca. 12 km from Bairro da Serra on Lajeado Road, S24°33.51', W048°43.54', elev. ca. 500–530 m, 7 Mar 2005, D.E. Desjardin 7814 (SFSU, SP #307990); same location, 8 Mar 2005, D.E. Desjardin 7822 (SFSU, SP #307998).

Additional taxon. – One additional potentially new bioluminescent species of Mycena has been collected in PETAR. Unfortunately it is represented by a single collection lacking macromorphological and ecological notes. The species (SP #380281) has a viscid pale yellowish brown pileus and viscid white stipe and belongs in sect. Euspeireae where it is allied with M. euspeirea (Berk. & M.A. Curtis) Sacc. Until more material of this interesting species is located, no formal description will be presented. (It is not accounted for in TABLE IGo).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 TAXONOMY
 DISCUSSION
LITERATURE CITED
 
Collecting specimens at night is a productive, albeit potentially dangerous, method of documenting the diversity of bioluminescent fungi. Our field studies in PETAR yielded seven species of Mycena and Gerronema viridilucens from remnant old growth Atlantic Forest habitat over calcareous soil. These species add to a growing list of Mycena s.l. reported to produce luminescent mycelium and/or basidiomes, currently totaling no fewer than 33 taxa belonging to 16 taxonomic sections (TABLE IGo). Molecular data (Moncalvo et al 2002Go) indicate that the genus Panellus nests within Mycena s.l.; hence we can add five more taxa to the list of bioluminescent mycenoid fungi, viz. Panellus stypticus (Bull. : Fr.) P. Karst., P. pusillus (Pers. ex lév.) Burdsall & O.K. Miller, Dictyopanus pusillus var. sublamellatus Corner (not yet transferred to Panellus), P. gloeocystidiatus (Corner) Corner and P. luminescens (Corner) Corner. We contend that there are many more described species of mycenoid fungi with bioluminescent properties that have remained undetected. As noted by Bermudes et al (1992)Go, although photometers have been used in other disciplines to detect bioluminescence, in mycology the perception of light emitted by mycelium and basidiomes has been largely by human eye. As a result we might be grossly underestimating the number of bioluminescent taxa. For example, in M. haematopus, where previous accounts failed to perceive bioluminescence, when studied photometrically, both mycelium and basidiomes emitted light (Bermudes et al 1992Go). Moreover when taxonomists describe euagarics they rarely record macromorphological data at night, so luminescent properties go undetected. Herein we report three species of Mycena that heretofore were unknown as being luminescent, viz. M. discobasis, M. fera and M. singeri. Approximately 500 species currently are recognized in Mycena s.l. (Kirk et al 2001Go). A review of TABLE IGo where we document 33 bioluminescent species of Mycena s.l. spread over 16 sections raises the question, did bioluminescence evolve in the mycenoid fungi independently numerous times, or did it evolve once (or only a few times) early on and was subsequently lost numerous times? We suspect that the metabolic pathway leading to bioluminescence in mycenoid fungi serves an important biological role (see below) and that it evolved once early in the evolutionary history of the lineage and that the final light-emitting step(s) was lost numerous times. Ongoing molecular phylogenetic and biochemical studies in our labs are addressing this hypothesis.

The potential roles of bioluminescence in the biology of fungi have been reviewed recently by Bermudes et al (1992)Go, Herring (1994)Go and Weitz (2004)Go. Sivinski (1981Go, 1998)Go, reiterating the ideas of numerous earlier workers (e.g. McAlpine 1900Go, Ewart 1906Go, Johnson 1919Go, Lloyd 1974Go), suggested that luminescent basidiomes attract invertebrates to aid in fungal spore dispersal. Sivinski (1981)Go hypothesized also that luminescence might attract predators of fungivores or might serve as a warning signal to repel nocturnal fungivores. Sivinski’s hypotheses are difficult to prove because fungivores could be attracted by the odors of basidiomes instead of by their bioluminescence. The question whether invertebrates associated with bioluminescent fungi actually see the light emitted by the fungus must be verified with electroretinography (e.g. Lall et al 2000Go). Of course luminescence as an adaptation to promote spore dispersal by visiting invertebrates does not explain why nonsporulating mycelium of many species is luminescent.

Bioluminescence is an oxygen-dependent metabolic process. Lingle (1989Go, 1993)Go and Bermudes et al (1992)Go have hypothesized that fungal bioluminescence is involved in lignin degradation through the detoxification of peroxidases formed during ligninolysis. As far as we know all luminescent Mycena species are white-rot fungi capable of lignin degradation (Treu and Agerer 1990Go; Desjardin unpubl). We favor the hypothesis that fungal bioluminescence is an advantageous biochemical process that provides antioxidant protection against deleterious effects of reactive oxygen species (ROS) produced mainly by mitochondria during respiration. McElroy and Seliger (1962)Go hypothesized that bioluminescence might have evolved as an ancient oxygen detoxifying mechanism with the exclusive purpose of oxygen consumption. As so eloquently stated by Herring (1994)Go: "perhaps the light of luminous fungi is really no more than an incidental by-product of an enzyme-mediated oxidation reaction." Seliger (1975)Go first suggested that the bioluminescence catalyzing enzymes named luciferases arose from mixed-function oxygenases involved in the removal of unsaturated compounds during the early life history. Later Wood (1995)Go proposed instead that the luminescent phenotype drove the evolution of new oxygenase functions. Concomitant induction of the antioxidant enzyme superoxide dismutase (SOD) and luciferase occurs in the bioluminescent bacterium Xenorhabdus luminescens under hyperoxia (Colepicolo-Neto et al 1992Go). Moreover Rees et al (1998)Go and Barros and Bechara (1998Go, 2000Go, 2001Go), reported the role of luciferins (i.e. the name given for a class of substrates of luciferase) as antioxidant molecules in jellyfish, Aequorea sp., and in the click beetle, Pyrearinus termitilluminans, respectively. Finally, Shimomura (1992)Go studied the influence of SOD and catalase (CAT) on luciferin production and bioluminescence intensity using luminescent mycelia and fruiting bodies of Armillaria mellea, Mycena citricolor, Mycena lux-coeli, Omphalotus olearius, Panellus stypticus and Pleurotus japonicus (=Lampteromyces japonicus). Both SOD and CAT activities as well as the ratio CAT/SOD (20–30-fold) are higher in all mycelia, where the consumption of oxygen is more pronounced due to the lignin degradation and consequent H2O2 production. In addition results have shown that the lower the SOD activity the higher is the light emission intensity, suggesting a possible connection of superoxide anion with the bioluminescent pathway. To address the question of why these mushroom-forming species bioluminesce, we currently are studying the influence of antioxidant and ligninolytic enzymes on the luminescence intensity of M. lucentipes and G. viridilucens.


   ACKNOWLEDGMENTS
 
We are grateful to FAPESP (Grant #01/04753-6) for providing financial support to C.V. Stevani for this research. We thank Antônio Modesto and Tadeu Gonçalves from PETAR administration for facilitating access to the collecting sites and the Instituto Florestal for authorizing permission to collect in PETAR. We thank João R.L. Godoy, Luiz Fernando Mendes, Ricardo Braga Neto and José Sanches for accompanying us in the field, for discovering interesting specimens and for keeping us entertained. We especially thank Joaquim B. Mendes Filho for guiding us in the dark through the forest without getting us lost. We are grateful that Drs D. Jean Lodge and Sharon Cantrell let us include their specimens of Mycena lucentipes from Puerto Rico in this study, and we thank Dr Jefferson Prado (Instituto de Botânica) for reviewing the Latin diagnoses.


   FOOTNOTES
 
Accepted for publication November 30, 2006.

1 Corresponding author. E-mail: ded{at}sfsu.edu


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Aidar MPM, Godoy JRL, Bergmann J, Joly CA. 2001. Atlantic Forest succession over calcareous soil, Parque Estadual Turístico do Alto Ribeira—PETAR, SP. Revta Brasil Bot São Paulo 24(4):455–469.

Barros MP, Bechara EJH. 1998. Bioluminescence as a possible auxiliary oxygen detoxifying mechanism in elaterid larvae. Free Radic Biol Med 24(5):767–777.[CrossRef][Medline]

———, ———. 2000. Luciferase and urate may act as antioxidant defenses in larval Pyrearinus termitilluminans (Elateridae: Coleoptera) during natural development and upon 20-hydroxyecdysona treatment. Photochem Photobiol 71(5):648–654.[CrossRef][Medline]

———, ———. 2001. Daily variations of antioxidant enzyme and luciferase activities in the luminescent click-beetle Pyrearinus termitilluminans: cooperation against oxygen toxicity. Insect Biochem Mol Biol 31:393–400.[CrossRef][Medline]

Berkeley MJ, Curtis MA. 1860. Characters of new fungi collected in the North Pacific Exploring Expedition by Charles Wright. Proc Amer Acad Arts 4:111–130.

Bermudes D, Petersen RH, Nealson KH. 1992. Low-level bioluminescence detected in Mycena haematopus basidiocarps. Mycologia 84:799–802.[CrossRef]

Bothe F. 1930. Ein neuer einheimischer Leuchtpilz, Mycena tintinnabulum. Ber Deutsch Bot Ges 48:394–399.

———. 1931. Ueber das Leuchten verwesender Blätter und seine Erreger. Planta 14:752–765.[CrossRef]

Brieger FG. 1969. Patterns of evolutionary and geographical distribution in Neotropical orchids. J Linn Soc, Biol 1: 197–217.[CrossRef]

Buller AHR. 1934. Omphalia flavida, a gemmiferous and luminous leafspot fungus. In: Buller AHR, ed. Researches in Fungi. Vol. IV. London, New York, Toronto: Longmans, Green & Co. p 397–454.

Colepicolo-Neto P, Camarero VCCP, Eickstein J, Hastings JW. 1992. Induction of bacterial luciferase by pure oxygen. J Gen Microbiol 138:1–6.[Free Full Text]

Corner EJH. 1954. Further descriptions of luminous agarics. Trans British Mycol Soc 37:256–271.

———. 1994. Agarics in Malesia. I. Tricholomatoid, II. Mycenoid. Beih Nov Hedwig 109:1–271.

Desjardin DE. 1995. A preliminary accounting of the worldwide members of Mycena sect. Sacchariferae. Biblio Mycol 159:1–89.

Ewart AJ. 1906. Note on the phosphorescence of Agaricus (Pleurotus) candescens Müll. Victorian Nat 23:174.

Grgurinovic CA. 2002. The genus Mycena in South-Eastern Australia. Hong Kong, PRC: Fungal Diversity Press. 329 p.

Haneda Y. 1955. Luminous organisms of Japan and the Far East. In: Johnson FH, ed. The Luminescence of Biological Systems. Washington, DC: American Association for the Advancement of Science. p 335–386.

Herring PJ. 1994. Luminous fungi. Mycologist 8:181–183.

Horak E. 1978. Mycena rorida (Fr.) Quél. and related species from the southern hemisphere. Ber Schweiz Bot Ges 88(1/2):20–29.

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, Moutinho P, Nepstad DC, Oliveira AA, Pott A, Rodal MJN, Sampaio EVSB. 1999. Evolution of the Brazilian phytogeography classification systems: implications for biodiversity conservation. Ciên Cultura 51:331–348.

Josserand M. 1953. Sur la luminescence de "Mycena rorida" en Europe occidentale. Bull Mens Soc Linn Lyon 22: 99–102.

Kirk PM, Cannon PF, David JC, Stalpers JA. 2001. Dictionary of the Fungi. 9th ed. United Kingdom: CAB International. 655 p.

Kobayasi Y. 1951. Contributions to the luminous fungi from Japan. J Hattori Bot Lab 5:1–6.

Kornerup A, Wanscher JH. 1978. Methuen handbook of colour. 3rd ed. London: Eyre Methuen. 252 p.

Lall AB, Ventura DSF, Bechara EJH, de Souza JM, Colepicolo-Neto P, Viviani VR. 2000. Spectral correspondence between visual spectral sensitivity and bioluminescence emission spectra in the click beetle Pyrophorus punctatissimus (Coleoptera: Elateridae). J Insect Physiol 46:1137–1141.[CrossRef][Medline]

Lingle WL. 1989. Effects of veratryl alcohol on growth and bioluminescence of Panellus stypticus. Mycol Soc Am Newslett 40:36. (Abstract)

———. 1993. Bioluminescence and ligninolysis during secondary metabolism in the fungus Panellus. J Biolumin Chemilumin 8:100.

Lloyd JE. 1974. Bioluminescent communication between fungi and insects. Florida Entomol 57:90.[CrossRef]

Lodge DJ. 1988. Three new Mycena species (Basidiomycota: Tricholomataceae) from Puerto Rico. Trans Brit Mycol Soc 91:109–116.

Maas Geesteranus RA. 1992. Mycenas of the Northern Hemisphere II. Conspectus of the Mycenas of the northern hemisphere. Verh Kon Ned Acad Wetensch, Afd Natuurk, Tweede Reeks 90:1–493.

———, de Meijer AAR. 1997. Mycenae paranaenses. Verh Kon Ned Acad Wetensch, Afd Natuurk, Tweede Reeks 97:1–164.

———, Winterhoff W. 1985. Eine neue Mycena-Art aus der Sektion Basipedes. Z Mykol 51(2):247–249.

McAlpine D. 1900. Phosphorescent fungi in Australia. Proc Linn Soc New South Wales 25:548–558.

McElroy WD, Seliger HH. 1962. Origin and evolution of bioluminescence. In: Kasha M, Pullman B, eds. Horizons in Biochemistry. New York: Academic Press. p 91–101.

Métrod G. 1949. Les Mycenes de Madagascar (Mycena, Corrugaria, Pterospora). Prod Flora Mycol Madagascar 3:1–146.

Moncalvo J-M, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime MC, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ, Thorn RG, Jacobsson S, Clémencon H, Miller OK Jr. 2002. One hundred and seventeen clades of euagarics. Mol Phylog Evol 23:357–400.[CrossRef][Medline]

Mori SA, Boom BM, Prance GT. 1981. Distribution patterns and conservation of eastern Brazilian coastal forest tree species. Brittonia 33:233–245.[CrossRef]

Oliveira Filho A, Fontes MA. 2000. Patterns of floristic differentiation among Atlantic Forests in southeastern Brazil, and the influence of climate. Biotropica 32:793–810.

Pegler DN. 1986. Agaric flora of Sri Lanka. Kew Bull Add Ser 12:1–519.

Rees JF, de Wergifosse B, Noiset O, Dubuisson M, Janssens B, Thompson EM. 1998. The origin of marine bioluminescence: turning oxygen defense mechanisms into deep-sea communication tools. J Exp Biol 201: 1211–1221.[Abstract]

Robich G. 2003. Mycena d’Europa. Trento, Italy: Associazione Micologica Bresadola. 728 p.

Seliger HH. 1975. The origin of bioluminescence. Photochem Photobiol 21:355–361.[Medline]

Shimomura O. 1992. The role of superoxide dismutase in regulating the light emission of luminescent fungi. J Exp Bot 43:1519–1525.[Abstract/Free Full Text]

Singer R. 1969. Mycoflora Australis. Beih Nov Hedwig 29:1–405.

———. 1986. Agaricales in Modern Taxonomy. 4th ed. Koenigstein, Germany: Koeltz Scientific Books. 981 p.

Sivinski JM. 1981. Arthropods attracted to luminous fungi. Psyche 88:383–390.

———. 1998. Phototropism, bioluminescence and the diptera. Florida Entomol 81:282–292.[CrossRef]

SOS Mata Atlântica. 1998, Evolução dos remanescentes florestais e ecossistemas associados do domínio Mata Atlântica no período 1990–1995. São Paulo: Fundação SOS Mata Atlântica/INPE.

Treu R, Agerer A. 1990. Culture characteristics of some Mycena species. Mycotaxon 38:279–309.

Wassink EC. 1948. Observations on the luminescence in fungi I, including a critical review of the species mentioned as luminescent in literature. Recueil Trav Bot Néerl 41:150–212.

———. 1978. Luminescence in fungi. In: Herring PJ, ed. Bioluminescence in action. London: Academic Press. p 171–197.

Weitz HJ. 2004. Naturally bioluminescent fungi. Mycologist 18:4–5.[CrossRef]

Wood KV. 1995. The chemical mechanism and evolutionary development of beetle bioluminescence. Photochem Photobiol 62(4):662–673.[CrossRef]





This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Services
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Desjardin, D. E.
Right arrow Articles by Stevani, C.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Desjardin, D. E.
Right arrow Articles by Stevani, C.
Agricola
Right arrow Articles by Desjardin, D. E.
Right arrow Articles by Stevani, C.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS