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Mycologia, 94(6), 2002, pp. 1059-1065.
© 2002 by The Mycological Society of America

Crepidotus thermophilus comb. nov., a reassessment of Melanomphalia thermophila, a rarely collected tropical agaric


Mary Catherine Aime 1

     Department of Biology, Virginia Tech, Blacksburg, Virginia 24061

T. J. Baroni

     Department of Biological Sciences, State University of New York, College at Cortland, Cortland, New York 13045

Orson K. Miller, Jr.

     Department of Biology, Virginia Tech, Blacksburg, Virginia 24061

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 

Melanomphalia thermophila (Sing.) Sing. is a rarely collected agaric previously known only from Florida and Brazil. This taxon was originally described as a species of Tubaria and much of Singer's rationale for placing Tubaria within the Crepidotaceae (Imai) Sing. was based on anatomical similarities between T. thermophila and Crepidotus (Fr.) Staude. In later works, T. thermophila was transferred to Melanomphalia M.P. Christ., again forming the basis upon which Singer placed Melanomphalia within the Crepidotaceae. Based on examination of newly collected specimens from Puerto Rico and Panama, type studies, and nuclear large subunit rDNA analysis, we conclude that this taxon is, in fact, a centrally stipitate Crepidotus. Melanomphalia thermophila is transferred to Crepidotus, fully described and illustrated.

Key words: Crepidotaceae, nuclear large subunit rDNA sequences, Tubaria, type studies


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Tubaria thermophila Sing. was originally described from Florida (Singer 1948Citation), where it held an isolated position within the genus as the only taxon with exosporial ornamentation. Tubaria Sect. Thermophila Sing. eventually came to include two species (Singer 1962Citation), and it was largely based on similarities in spore ornamentation between this section and Crepidotus Sect. Echinosporae Pilát that led to Singer's transfer of Tubaria (W.G. Smith) Gill. from the Cortinariaceae R. Heim ex Pouzar to the Crepidotaceae (Imai) Sing. (Singer 1951Citation, 1962Citation).

Melanomphalia M.P. Christ. was a monotypic genus that Singer (1955)Citation originally placed in the Cortinariaceae. Again, this decision was based on similarities in exosporial ornamentation, in this case between the type, M. nigrescens M.P. Christ., and Inocybe platensis Speg., which he transferred to Melanomphalia (Singer 1955Citation). In later works, Singer reconsidered his treatment of these genera by transferring Tubaria Section Thermophila to Melanomphalia and placing Melanomphalia in the Crepidotaceae because of the stated anatomical similarities between M. thermophila and its allies and some Crepidotus species (Singer 1967Citation, 1971Citation). Thus the Crepidotaceae sensu Singer came to include, among others, the pleurotoid genus Crepidotus (including both smooth- and ornamented-spored taxa), and the stipitate genera Melanomphalia (all members with ornamented basidiospores), Tubaria, and Simocybe Karst. (the latter two containing only smooth-spored taxa) (Singer 1986Citation).

We have made several collections of a dark reddish brown stipitate agaric from the Luquillo municipality of Puerto Rico in subtropical moist and wet forest between 70 and 110 m elevation. Anatomical features, including basidiospore ornamentation, are consistent with a diagnosis of Melanomphalia thermophila. In this paper we fully describe and illustrate M. thermophila and present the results of a phylogenetic analysis that lead us to propose a new combination, Crepidotus thermophilus.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Morphology – Color designations of basidiomata are given as general color terms, such as ochre, or in some cases color designations are from Kornerup and Wanscher (1978)Citation and are indicated in the following manner, 7C5—Brownish Orange (where "7C5" designates a plate, column, and row, respectively). Methods used to prepare microscopic structures for data collection are those of Baroni (1981)Citation. All measurements of microscopic structures were made in mounts of 3% KOH or 10% NH4OH. The measurement of basidiospores includes the hilar appendix or apiculus. The designations used for basidiospore measurements are those of Baroni and Horak (1994)Citation with the exception that the symbol E (length/width of an individual spore) is herein designated as Q (for quotient). All measurements were made with an Olympus BHS light microscope under Hoffman interference optics using a semi-automated image analysis system (a GTCO digitizer pad and Metrics5 software written by Dr. David Malloch). Descriptive statistical analysis of the measurements was obtained using EXCEL97 and/or SigmaStat 1.0. Scanning electron micrographs (SEMs) were produced with an ISI Supra IIIA scanning electron microscope generally run at 10 Kev. Methods for preparation of samples for SEM are those of Baroni (1981)Citation. Where noted, coordinates of collecting sites were obtained with a hand held GPS device and were referenced to map datum WGS84.

Sequence analysis – To ascertain the natural affinities of M. thermophila, DNA was extracted from two Puerto Rican collections made in consecutive years. Methods for extraction of DNA, amplification, and sequencing follow Aime (1999)Citation. Primers LR0R, LR3R, LR5, and LR7 (Moncalvo et al 2000Citation) were used to sequence a portion from the 5'-end of the nuclear large subunit rDNA (nLSU). For sequence analysis, we assembled a data set of previously published sequences (Table 1), by selecting two generic exemplars from each family following the classification of Singer (1986)Citation in order to approximate the range of diversity found within the dark-spored Agaricales. Three taxa of white-spored agarics were included for rooting purposes, with Gymnopus dryophilus chosen as the outgroup. Taxa within Crepidotus were selected to include a broad cross-section of the phenotypic diversity inherent in the genus.


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  		TABLE I. Taxa selected for sequencing analysis

 
Sequences were manually aligned and analyzed in Paup* 4.0b2 (Swofford 2001Citation). Sequence alignments are deposited in TreeBASE S791. The data matrix included a total of 1193 characters (including gaps), 139 of which were parsimony-informative. Parsimony analyses were performed using heuristic search algorithms with multiple (10) random sequence additions to generate starting trees, and tree-bisection-reconnection (TBR) branch-swapping. Bootstrapping frequencies (Hillis and Bull 1993Citation) were calculated using TBR branch swapping with 1000 replicates; support of greater than 50% was considered significant. Jackknifing frequencies (Lanyon 1985Citation) were calculated using TBR branch swapping with 1000 replicates; support of greater than 50% was considered significant. Decay values (Bremer 1988Citation) were calculated with AutoDecay 4.0.1 (Eriksson 1998Citation) in PAUP 3.1.1 (Swofford 1993Citation).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Type examinations show our Puerto Rico collections to be identical to Melanomphalia thermophila (Sing.) Sing. To infer the natural position of this taxon within the Crepidotaceae, DNA was isolated and sequenced from two Puerto Rican collections. Analysis of nLSU sequences, within both an extensive dataset of over 154 agaric taxa (Moncalvo et al 2000Citation, dataset available at http://www.botany.duke.eeu/fungi/mycolab), and within the pruned dataset presented (Fig. 1) show this taxon to be a component of Crepidotus. This species is described and illustrated, and a new combination proposed as follows.



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  		 FIG. 1. Phylogenetic assignment of Crepidotus thermophilus within Crepidotus (Fr.) Staude. Analysis based on a portion from the 5'-end of the nuclear DNA encoding the large ribosomal subunit. The first of six most parsimonious trees is depicted (length = 587, RI = 0.54, CI = 0.50). Branches with strong statistical support are indicated by a bold line. Bootstrapping values (1000 replicates) are given as first number above supported branch; jackknifing values (1000 replicates) follow; decay values are indicated below branch

 

   TAXONOMY
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 TAXONOMY
DISCUSSION
 LITERATURE CITED
 
Crepidotus thermophilus (Sing.) Aime, Baroni, et O.K. Miller, comb. nov. Figs. 2–13



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  		 FIG. 2. Crepidotus thermophilus TJB 8496. Basidiomata

 
{equiv} Tubaria thermophila Sing., Papers Mich. Acad. Sci., Arts & Letters 32:145. 1948.

{equiv} Melanomphalia thermophila (Sing.) Sing., Atas Instituto de Micologia 5:481. 1967.

Pileus (Fig. 2) a deep rich reddish brown (6D5-7 to 7D8—Sienna, Brick Red or Terra Cotta) slightly fading with age and expansion to Cinnamon Brown (6D6), 20–50 mm broad, convex becoming broadly convex, occasionally broadly umbonate, then plane, eventually uplifted, undulate and incised around the margin with age, moist or dry, becoming appressed fibrillose squamulose with age. Lamellae pale tan (5A2 to 5B3—Orange White or Greyish Orange), short decurrent, close to crowded (2–3 tiers of lamellulae), narrow (up to 2 mm), edges concolorous or slightly paler and fimbriate. Stipe pale creamy white (4A2–3—Yellowish White or Cream), 1.5–4.0 mm wide at apex, 20–35 mm long, equal, terete, often flexuous, central or very slightly eccentric, glabrous except for white fibrillose-pruinose apex, white mycelioid or strigose covering at base, solid and white context. Odor and Taste not distinctive. Spore deposit light reddish-brown. Basidiospores (Figs. 4, 8–9, 13) 7.0–10.7 x (4–)4.8–5.9(–6.3) µm (n/6 = 136, Lm = 8.7 ± 0.83, Wm = 5.4 ± 0.38, Q = 1.29–2.12, Qm = 1.62 ± 0.17; HOLOTYPE n = 21, 7.9–10.7 x 4.5–6, Lm = 9.6 ± 0.69, Wm = 5.3 ± 0.37, Q = 1.56–2.05, Qm = 1.82 ± 0.14), amygdaliform in profile view, broadly fusiform-elliptical in face view, round in polar view, verrucose, yellow brown in 3% KOH. Basidia mostly 2-sterigmate, some 1 or 4 sterigmate, clavate, 17.8–24.3 x 6.4–8.0 µm. Cheilocystidia (Figs. 3, 10) abundant, hyaline, versiform, but mostly inflated, clavate, obpyriform, sphaeropedunculate, or broadly fusiform, some cells with apical digiform projections, 22–44 x 11–23 µm. Pleurocystidia absent. Lamella trama composed of a ± parallel, hyaline, cylindric or mostly inflated hyphae, (3.2) 8–17 µm in diam. Pileus context a hyaline layer of loosely interwoven, cylindric or slightly inflated, frequently branched hyphae, 4–14 µm in diam. Pileipellis a rich yellow brown layer of loosely entangled, cylindric or slightly inflated hyphae, 6–18 µm in diam, producing ascendant versiform pilocystidiate end cells (Fig. 12), cylindrical or slightly inflated or some tapered fusoid, 30–120 x 6–18 µm, all cells with dense dark yellow brown vacuolar pigments. Stipitipellis a dingy yellowish brown layer of repent, cylindric hyphae, 2.4–5.6 µm in diam, with abundant versiform caulocystidia ( Figs. 5– 7, 11) at apex, quite variable, on young specimens mostly cylindrical-contorted, narrowly fusoid or narrowly clavate, on mature specimens mostly composed of clusters of inflated clavate or spherical end cells, 14.6–46 x 9.7–18 µm, sometimes with these spherical end cells sitting atop chains of 2–4 swollen spherical subtending cells. Clamp connections present in all tissues.



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  		 FIGS. 3–5. Crepidotus thermophilus TJB 8496. 3. Cheilocystidia. 4. Basidiospores. 5. Caulocystidia. Scale bar = 10 µm

 


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  		 FIGS. 8–9. Crepidotus thermophilus scanning electron micrographs of basidiospores. 8. Basidiospores of TJB 8496. 9. Basidiospores of Singer F20 (Syntype). Scale bars equal 2.5 µm

 


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  		 FIGS. 10–13. Tubaria thermophila. 10. Cheilocystidia Singer F20 (Syntype). 11. Caulocystidia Singer F20/III. 12. Pilocystidia Singer F20 (Syntype). 13. Basidiospores Singer F20 (Syntype). Scale bar = 10 µm

 


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  		 FIGS. 6–7. Crepidotus thermophilus Ovrebo 3808. 6. Caulocystidia from young basidiomata. 7. Caulocystidia from mature basidiomata. Scale bar = 10 µm

 
Habitat, habit, fruiting period. Scattered in leaf litter, soil, sandy soil, or on well decomposed woody debris in subtropical moist and borderline wet forests at low elevations. May through August and January. Known from Puerto Rico, Florida, Brazil, and Panama.

Specimens examined. PANAMA. PROVINCE OF PANAMA: Barro Colorado Island, Gatun Lake, W.M. Wheeler Trail, 14 May 2000, C.L. Ovrebo 3808 (CSU). PUERTO RICO. MUNICIPIO LUQUILLO: between Luquillo and Sabana, off of Rt. 991, above Rio Sabana and a private chicken farm, N 18° 21' 3.4'', W 65° 43' 50'', approx. 70 m elev., 7 June 1997, T.J. Baroni 8496 (CORT); same local, 14 Nov. 1996, T.J. Baroni 8309 (CORT); same local, 15 January 1998, O.K. Miller, Jr. 27270 (VPI); Luquillo Mts., CNF, near Sabana in borderline subtropical wet forest, 18° 19' 34'', W 65° 43' 22'', 14 July 1998, collected by J. Mercado, comm. S. A. Cantrell PR4887 (NY). UNITED STATES. FLORIDA: Highlands Co., near Seabring, Highlands Hammock State Park, 2 August 1942, R. Singer F 20 (SYNTYPE, FH); same local, August 1942, R. Singer F 20/III ("authentic", FH).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 TAXONOMY
 DISCUSSION
LITERATURE CITED
 
Crepidotus thermophilus is recognized in the field by the combination of its reddish brown subtomentose to fibrillose-punctate pileus surface, decurrent tan lamellae, pale creamy-white central stipe, and light reddish-brown spore deposit. Although the vast majority of described Crepidotus species are pleurotoid in form, the generic definition does not exclude taxa with a well-developed stipe. One other species of Crepidotus possesses a prominent stipe, C. nyssicola (Murr.) Sing. (Hesler and Smith 1965Citation, Bigelow 1980Citation). Crepidotus nyssicola lacks pigmentation in the pileus, has globose, echinulate spores and is known from temperate North America. Crepidotus thermophilus is differentiated by its amygdaliform, verrucose basidiospores and a Neotropical distribution. The inflated cheilocystidia and 2-sterigmate basidia of C. thermophilus are also distinctive for this species. Singer (1971)Citation previously had reported this species from Florida in the United States and from Pernambuco in Brazil. We now have documented further collections from Puerto Rico and Barro Colorado Island in Panama. We suspect this rarely collected and apparently saprotrophic agaric will eventually be found widely distributed in subtropical and tropical habitats throughout the Caribbean basin and in the northern areas of South America.

Much of Singer's evolving concept of the Crepidotaceae was based on similarities in exosporial ornamentation between Tubaria (later Melanomphalia) thermophila and Crepidotus Sect. Echinosporae. Not surprisingly, basidiospore ornamentation in C. thermophilus as revealed by SEM (Figs. 8–9) falls well within the range of variation for Crepidotus, consisting of low, distinct, verruculae, intermediate between that found in C. variabilis (Fr.) Kumm. (in Pegler and Young 1972Citation) and C. subverrucisporus (Pilát) (in Senn-Irlet 1993Citation). Previous work has suggested that the nature of exosporial ornamentation combined with the shape of basidiospores may be the best phenotypic indicator of phylogenetic relationships in the Crepidotaceae (Aime 1999Citation). Significantly, neither basidiospore ornamentation nor shape in C. thermophilus share similarities with those published for the generic type of Tubaria, T. furfuracea (Pers. ex Fr.) Gill. (in Clémençon 1977Citation), or with M. nigrescens (in Horak 1968Citation, Montag 1996Citation), the type species of Melanomphalia. Fresh material of M. nigrescens was not available for DNA analysis.

This study has raised questions regarding the natural phylogenetic affinities of both Tubaria and Melanomphalia that we are currently working to address. In addition, we are re-examining other species currently placed in Melanomphalia to determine whether they also belong in Crepidotus. If and when these taxa are transferred it would increase the number of species with well-developed central stipes currently placed in Crepidotus.


   ACKNOWLEDGMENTS
 
Field work in Puerto Rico was funded by grant DEB-95-25902 to the State University of New York College at Cortland from the National Science Foundation, Biotic Surveys and Inventories Program. Our research was facilitated also by the USDA-Forest Service's International Institute of Tropical Forestry (IITF), especially the International Forestry Program. The lead author (MCA) also received funding in part from a Sigma Xi Grants-in-Aid-of-Research. The authors are indebted to Dr. Rytas Vilgalys, Dr. Jean-Marc Moncalvo, and the mycology lab of Duke University for the generous use of facilities and databases for the sequencing portion of this study. The logistic support for fieldwork in Puerto Rico was arranged by Dr. D. Jean Lodge and Dr. Sharon Cantrell. We also thank Drs. Donald H. Pfister (FH), D. Jean Lodge (CFMR) and Clark L. Ovrebo (CSU) for kindly arranging loans of collections for our studies. Dr. Sharon Cantrell and Mr. J. Mercado contributed to this study by providing field notes and collections as well. Finally, we thank Dr. D. Jean Lodge for suggesting improvements to an earlier version of this manuscript. This paper is based in part on a dissertation submitted by the first author to Virginia Tech as a requirement for a Ph.D. degree.


   FOOTNOTES
 
1 Corresponding author, present address: Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, U.K., cathie.aime{at}plants.ox.ac.uk Back

Accepted for publication May 8, 2002.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Aime MC., 1999 Generic concepts in the Crepidotaceae as inferred from nuclear large subunit ribosomal DNA sequences, morphology, and basidiospore dormancy patterns [MSc Thesis]. Blacksburg, Virginia: Virginia Polytechnic Institute and State Univ. 127 p

Baroni TJ., 1981 A revision of the genus Rhodocybe Maire (Agaricales). Beih Nova Hedwigia 67:1-194

———, Horak E., 1994 Entolomataceae in North America III: new taxa, new combinations and notes on species of Rhodocybe. Mycologia 86:138-145

Bigelow HE., 1980 Crepidotus nyssicola. Mycologia 72:1227-1231

Bremer K., 1988 The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795-803

Chapela IH, Rehner SA, Schultz TR, Mueller UG., 1994 Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691-1694[Abstract/Free Full Text]

Clémençon H., 1977 Die wandstrukturen der basidiosporen VII Tubaria. Zeitschrift für Pilzkunde 43:283-289

Eriksson T., 1998 AutoDecay ver. 4.0.1. (Program distributed by author). Department of Botany, Stockholm University, Stockholm

Hesler LR, Smith AH., 1965 North American species of Crepidotus. New York: Hafner Publishing Company. 168 p

Hillis DM, Bull JJ., 1993 An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42:182-192

Horak E., 1968 Synopsis generum Agaricales (Die gattungstypen der Agaricales). Wabern-Bern, Germany: Beiträge zur Kryptogamenflora der Schweiz. Band 13. 741 p

Hopple JS., 1994 Phylogenetic investigations in the genus Coprinus based on morphological and molecular characters [PhD Dissertation]. Durham, North Carolina: Duke Univ. 402 p

Johnson J., 1997 Phylogenetics of the basidiomycete genus Lepiota sensu lato: a framework for studying the evolution of insect-cultivated fungi [PhD Dissertation]. Durham, North Carolina: Duke Univ. 150 p

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

Lanyon S., 1985 Detecting internal inconsistencies in distance data. Systematic Zoology 34:39-403

Moncalvo J-M, Lutzoni FM, Rehner SA, Johnson J, Vilgalys R., 2000 Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Systematic Biology 49:278-305[Medline]

Montag IK., 1996 Zur kenntnis von Melanomphalia nigrescens Christiansen 1936 ein seltener braunsporer, erstmals in Deutschland gefunden. Zeit. für Mykologie 62:75-78

Pegler DN, Young TWK., 1972 Basidiospore form in British species of Crepidotus. Kew Bulletin 27:311-323

Senn-Irlet B., 1993 Type studies in Crepidotus-II. Persoonia 15:155-167

Singer R., 1948 New and interesting species of basidiomycetes. II. Papers of the Michigan Academy of Science, Arts and Letters 32:103-151

———. 1949) 1951 The "Agaricales" (mushrooms) in modern taxonomy. Lilloa 22:590-599

———. 1955 Le genre Melanomphalia Christiansen. Revue de Mycologie 20:12-17

———. 1962 The Agaricales in modern taxonomy. 2nd ed. Germany: J. Cramer. 915 p

———. 1967 The genus Melanomphalia. Atas do Instituto de Micologia 5:476-488

———. 1971 A revision of the genus Melanomphalia as a basis of the phylogeny of the Crepidotaceae. In: Petersen RH, ed. Evolution in the higher Basidiomycetes. Knoxville Tennessee: The University of Tennessee Press. p 441–474

———. 1986 The Agaricales in modern taxonomy. 4th ed. Germany: Koeltz Scientific Books. 981 p

Swofford DL., 1993 PAUP: phylogenetic analysis using parsimony ver. 3.1.1. Champaign, Illinois: Illinois National History Survey

———. 2001 PAUP*: phylogenetic analysis using parsimony (*and other methods), beta version 4.0b2. Sinauer Associates, Sunderland, Massachusetts




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