Hoehnea 32(1): 49-57, 13 fig., 2005

Manglicolous Basidiomycetes ofsouthwestern and southwestern Florida (U.S.A.)

l 3 Angel Manuel Nieves-Rivera ,4, Terry Alan Tatta~ and LeifRyvarden

Received: May 25, 2004; accepted: December 07, 2004

ABSTRACT - (Manglicolous Basidiomycetes of southwestern Puerto Rico and southwestern Florida (U.S.A.)). Field surveys ofthe Boqueron Commonwealth Forest, Boqueron Wildlife Refuge, and Magueyes Island in southwestern Puerto Rico and the Aquatic Preserves ofsouthwestern Florida from July 200 I throughout 2003 yielded 59 specimens ofmanglicolous basidiomycetes that were catalogued and taxonomically examined. All the specimens identified by observation of morphological and microscopic characters, and compared with specimens from the U.S. National Collections at Maryland (BPI), University ofPuerto Rico at Rio Piedras (UPRRP), The New York Botanical Garden at Bronx (NY), and University ofOslo at Blindern (0) herbaria. They represented eight families, 12 genera and 14 taxa. Basidiomycetes grew on dead bark and wood ofRhizophora mangle L., Avicennia gerll1inans (L.) Stearn, and Laguncularia racell10sa (L.) Gaertn. Coriolopsisjloccosa (Jungh.) Ryv., merrillii (Murrill) Ryv., and Tyromyces cf. chioneus (Fr.: Fr.) Karst. were new records for Puerto Rican and Phlebia sp. was a new record for Florida mangroves. Key words: Aphyllophorales, , Hymenomycetes, forest

RESUMEN - (Basidiomicetos manglicolas del suroeste de Puerto Rico y suroeste de Florida (U.S.A.)). Los reconocimientos de campo al Bosque Estatal de Boqueron, el Refugio de Vida Silvestre de Boqueron e Isla Magueyes en el sudoeste de Puerto Rico y a las Reservas AcuMicas del sudoeste de la Florida durante julio de 200 I a traves de 2003 produjeron 59 especfmenes de basidiomicetos manglicolas que fueron catalogados y examinados taxonomicamente. Todos los especfmenes fueron identificados mediante la observacion de los caracteres morfologicos y microscopicos,junto con la comparacion de especfmenes de los herbarios de las Colecciones Nacionales Fungica de los U.S.A. en Maryland (BPI), Universidad de Puerto Rico en Rio Piedras (UPRRP), el Jardin Botanico de Nueva York en el Bronx (NY), y la Universidad de Oslo en Blindern (0). Estos representaron ocho familias, 12 generos y 14 taxones. Los basidiomicetos crecieron en corteza muerta y madera de Rhizophora mangle L., Avicennia germinans (L.) Stearn y Laguncularia racemosa (L.) Gaertn. Coriolopsis jloccosa (Jungh.) Ryv., Phellinus lI1errillii (Murrill) Ryv. y Tyroll1yces cf. chioneus (Fr.: Fr.) Karst. fueron nuevos registros para los mangles de Puerto Rico y Phlebia sp. fue un nuevo registro para los mangles de la Florida. Palabras clave: Aphyllophorales, Caribe, himenomicetos, manglar

Introduction Galz., T. pacifica Olive, and T. violacea (Que!.) Bourd. & Galz.) from Avicennia sp., Rhizophora Until recently, there have been few mycological mangle L. or Hibiscus tiliaceus L. (Reichardt 1870, studies on the manglicolous basidiomycetes of the Baccarini 1916,Olive 1957,Cooke 1961,Kohlmeyer Caribbean region, although information on their 1969). Kohlmeyer (1969) also collected two occurrence would be of considerable value for basidiomycetes, F. avicenniae and P. gilvus from the biologists and conservationists. Previous reports Heeia Swamp, Oahu, Hawaii, on R. mangle. Lee & summarized in Kohlmeyer (1969) recorded eight Baker (1973) reported three basidiomycetes from R. manglicolous basidiomycetes (Fomes avicenniae mangle roots (Fomes sp., cinnabarinus Bacc, Phellinus gilvus (Schw.) Pat., Psathyrella sp., Jacq., and Psathyrella sp.). Schizophyllum commune (Fr.) Fr., Trametes The neotropical occurrence of manglicolous rhizophorae Reich., Tulasnella bifrons Bourd. & basidiomycetes were reported from Brazil (Sotao et al.

1. University of Puerto Rico, Department of Marine Sciences, P. O. Box 9013, MayagUez, Puerto Rico 00681-9013 2. University ofMassachusetts, Department ofMicrobiology, 203 Morrill Science, Center IVN, Amherst, Massachusetts 0I 003-5720 3. University of Oslo, Division of Botany and Plant Physiology, Botany Department, P. O. Box 1045, Blindem, Oslo, N-0316 Norway 4. Corresponding author: [email protected] 50 Hoehnea 32{ I), 2005

1991, Almeida Fil 0 et al. 1993, Campos & Cavalcanti mangle occasionally forms thick coastal woodland in 2000, Sotao et al. 2002), LesserAntilles (Pegler 1983a, BCF and in the rest of the southwestern coast of Minter et al. 2001), Panama (Gilbert & Sousa 2002), Puerto Rico (Cintron et al. 1978, Lugo 1989, Vazquez Puerto Rico (Stevenson 1975, Lodge 1996a, Nieves­ & Kolterman 1998). Rivera et al. 1998, Minter et al. 2001) and Venezuela The Aquatic Preserves of Southwest Florida (Dennis 1970). Minter et al. (2001) survey of (APSF) are located SE of Venice, at the Gulf of Caribbean fungi and recorded 11 taxa ofmanglicolous Mexico. The APSF have over 2,574 km ofcoastline, basidiomycetes for Puerto Rico (e.g. Gloeophyllum a network of barrier islands and mangals providing striatum (Sw.: Fr.) Murrill, Pleurotus djamor (Fr.) more than 907 km2 ofbays, lagoons, and other water Boedijn, Pleurotus sp., Polyporus fulvocinereus bodies sheltered from the open gulf. Southwest Florida (Murrill) Overh., and Tyromyces sp. on R. mangle; contains the highest density of aquatic preserves in Phellinus sp. and Trametes villosa (Fr.) Kriesel on the state. Most of the coastal waters here are Conocarpus erectus L.; Coriolopsis sp., Inonotus contained within aquatic preserves. The eight aquatic porrectus Murrill, and Phellinus sp. on Laguncularia preserves in this region are: (1) Lemon Bay; the racemosa (L.) Gaertn.; and S. commune on Charlotte Harbor Aquatic Preserves, which include Laguncularia sp.). More recently, the manglicolous (2) Cape Haze, (3) Charlotte Harbor/Gasparilla Sound, fungi surveys by Poonyth et al. (2000) and Schmit & (4) Matlacha Pass and (5) Pine Island Sound; (6) Shearer (2003) summarized what is known about Estero Bay; (7) Rookey Bay; and (8) Cape Romano/ worldwide fungal species and their mangrove hosts, Ten Thousand Islands. The collection sites at APSF and recorded about 30 species of manglicolous were: Punta Gorda (26°47'N, 82°04'W), Cape Coral basidiomycetes (e.g. Crepidotus krieglsteiner Singer, (26°45'N, 82°04'W), and Cape Haze (26°54'N, P. gilvus, Psathyrella rhizophorae Singer, 82°10'W). The Punta Gorda site was at sea level and Pycnoporus cinnabarius (Jacq.) Fr., commune S. was flooded with each tide. The Cape Coral and Cape on R. mangle, a d Dacrymyces intermedius L.S. Haze sites were on berms approximately 0.5 m above Olive on H. tiliaceus). We note here the occurrence sea level. The general environment of the region is of 14 basidiomycetes from mangrove coastal forests classified as a subtropical dry forest. APSF normally ofsouthwestern Puerto Rico and four basidiomycetes receive 1,376 mm on average of precipitation each for southwestern Florida (U.S.A.); this marks the year. The driest months are November, December and second formal documentation of manglicolous April with precipitation is less than 50 mm. Wildfires basidiomycetes for Puerto Rico, and the sixth are common in late spring, since April is dry and hot, neotropical occurrence ofmanglicolous fungi ofthis and sometimes-rainy season does not begin in June. group. In these cases, the fire season can also extend into Material and methods June. Further details on climatology, geology, and edaphic formations of APSF are discussed in Davis The Puerto Rican study areas were located at (1940), Craighead (1971), and Kangas & Lugo (1990). the Boqueron Commonwealth Forest (BCF, 18°01 'N, Avicennia germinans (L.) Stearn forms thick coastal 67°10'W, secondary road PR-307, next the town of woodland in APSF and in the rest ofthe southwestern Boqueron, Barrio Boqueron, Cabo Rojo), Boqueron coast ofFlorida (Davis 1940, Craighead 1971, Kangas Wildlife Refuge (BWR, 18°01 'N, 67°09'W, secondary & Lugo 1990). road PR-30 1, near to the town of Boqueron, Cabo As a result ofthree field surveys to the BCF, BWR, Rojo), and Magueyes Island (MI, 17°58'N, 67°02'W, and MI in southwestern Puerto Rico and the Aquatic secondary road PR-304, close to the town of La Preserves ofsouthwest Florida from July 2001 through Parguera, Barrio La Parguera, Lajas), all at mean sea 2003, 59 specimens of manglicolous basidiomycetes level, southwestern Puerto Rico. The general were catalogued and taxonomically examined, using the environment ofthe region is classified as a subtropical works of Cooke (1961), Dennis (1970), Gilbertson & dry forest (Ewel & Whitmore 1973). Further details Ryvarden (1986, 1987), Pegler (1983a, b), and Larsen on climatology, geology, and edaphic formations of & Cobb-Poulle (1990). Each taxon newly recorded for BCF, BWR, and MI are discussed in Glynn (1973), Puerto Rico and Florida is marked with an asterisk at Vazquez (1983), Toro & Colon (1986), Winter et al. the head ofthe specific name. To study the material the (1998), and Nieves-Rivera et al. (2002). Rhizophora slides were mounted in 5 % KOH, Melzer reagent or A.M. Nieves Rivera. T.A. Tallar & L. Ryvarden: Manglicolous Basidiomycetes of Puerto Rico and Florida 51 lactophenol, following Largent et af. (1977). All the Material studied: PUERTO RICO. CABO RoJO: specimens were identified by observation of Boquer6n Wildlife Refuge, on R. mangle leaf litter, morphological and microscopic characters, along with position aboveground 0.1 m, 13-III-1995, A.M. Nieves­ comparison with specimens from the U.S. National Rivera PR-641.1 (UPRRP). Fungus Collections at Maryland (BPI), University of Remarks: this taxon grew on decayed plant material Puerto Rico at Rio Piedras (UPRRP), The New York (leaf litter of R. mangle and Thespesia populnea Botanical Garden at Bronx (NY), and University ofOslo (L.) Soland.: Correa, and blades of Thalassia at Blindem (0) herbaria. testudinum Banks. & Soland.).

Results Lentinaceae

Manglicolous basidiomycetes represented eight Lentinus crinitus (L.: Fr.) Fr., Syst. Orb. Veg. 77. families, 12 genera and 14 taxa. Basidiomycetes 1825. occurred on host trees R. mangle (II species), Figure 8 A. germinans (two species) and L. racemosa (two Material studied: PUERTO RICO. CABO RoJO: species). Coriolopsis floccosa (Jungh.) Ryv., Boquer6n Wildlife Refuge, on R. mangle fallen trunk, Phellinus merrillii (Murrill) Ryv., and Tyromyces cf. position aboveground> 1 m, 15-III-2002, A.M. Nieves­ chioneus (Fr.: Fr.) Karst. were new records for Puerto Rivera (BPI863546). Rican mangroves, and Phlebia sp. was a new record for Florida mangroves. Remarks: this extremely common species has a basidioma which is extremely variable and difficulty Crepidotaceae is experienced in delimiting the species (Pegler Crepidotus uber (Berk. & M.A. Curtis) Sacc., Syll. 1983a, b). Lentinus crinitus is found single or Fung. 5: 878.1887. gregarious on moist dead hardwoods logs or stumps. Figures 1-5 Coriolaceae Material studied: PUERTO RICO. CABO RoJO: Coriolopsis badius (Cooke) Murrill, Bull. Torrey Bot. Boquer6n Commonwealth Forest, next to Puerto Real, Club 34: 466.1907. boardwalk that passes through a mangrove forest and reaches the lagoon on the Boquer6n-Guaniquilla Material studied: UNITED STATES. FLORIDA: Aquatic mangrove forest, on Rhizophora mangle L. on bark Preserves of Southwest Florida, Cape Coral, on and dead wood, also on rotting aerial roots, and upright Avicennia germinans (L.) Steam dead wood, position tree trunks, position aboveground 0.3-1.5 m, aboveground> 1m, 5-1-2003, T.A. Tattar(BPI843741); 14-IV-2003, A.M. Nieves-Rivera (BPI843767). CAPE HAZE, on A. germinans dead wood, position Remarks: the main character that distinguishes this aboveground> I m, 20-X-2002, TA. Tattar form from the type species Crepidotus moWs (BPI843742). (Schaeff.: Fr.) Kummer is the lack of encrusting­ Remarks: this species is common in the Caribbean. pigmented hyphae on the cutis, an epicutis C. badius had a position aboveground from 25 cm to undifferentiated from the underlying context, and a 2 111 and also grew on Conocarpus erectus L. dead gelatinized layer reaching the surface (Pegler 1983a). wood. In general, C. uber appears to be widespread in the tropics and subtropics and sequencing data suggest *Coriolopsis jl.occosa (Jungh.) Ryv., Genera Polyp. that it may be a complex ofspecies; microscopically Syn.Fung.5:316.1991. it is indistinguishable from C. uber from Madagascar Figure 9 (M.e. Aime unpublished data). C. uber has been Material studied: PUERTO RICO. LAJAS: Magueyes collected from Bonin Island, Dominica, and Island, on R. mangle bark, position aboveground Guadeloupe in the Lesser Antilles (Pegler 1983a). < 2 m, 14-IV-2003,A.M. Nieves-Rivera PR-979 (0). Coprinaceae Remarks: spores ofthis species were non-amyloid in Psathyrella sp. Melzer's reagent. Coriolopsis jl.occosa cause white Figures 6-7 rot in R. mangle. 52 Hoehnea 32( I), 2005

4

) .~

1.5cm

5

Figures 1-5. Crepldo/us uber collected on southwestern Puerto Rico. 1-2. Young basidiomata on dead upright Rhi::ophora mangle tree trunk. 3-5. Mature basidiomata on branchs. A.M. Nieves Rivera, T.A. Tattar & L. Ryvarden: Manglicololls Basidiomycetes of Puerto Rico and Florida 53

Gloeophyllum striatum (Sw.: Fr.) Murrill, Bull. Torrey Material studied: PUERTO RICO. CABO RoJO: Bot. Club 32: 370. 1905. Boquer6n Commonwealth Forest, next to Puerto Real, Material studied: PUERTO RICO. CABO RoJO: boardwalk that passes through a mangrove forest and reaches the lagoon on the Boquer6n-Guaniquilla Boquer6n Commonwealth Forest, next to Puerto Real, mangrove forest, on R. mangle bark, position boardwalk that passes through a mangrove forest and aboveground 60 em, 19-IV-2003, Nieves-Rivera reaches the lagoon on the Boquer6n-Guaniquilla A. M. PR-984.3 (UPRRP). mangrove forest, on R. mangle bark, position aboveground 0.5-2 m, 19-IV-2003, Nieves­ A.M. Remarks: this cosmopolitan species is found single or Rivera (BPI843744). gregarious on dead hardwoods and occasionally on Remarks: G. striatum has also been found on conifers. Tyromyces sp. has been previously collected R. mangle decay wood in the Boquer6n Wildlife from Rhizophora sp. (SoHio et al. 2002). Refuge in Cabo Rojo. Hexagonia hydnoides (Fr.: Sw.) M. Fidalgo, Mem. N. Y. Bot. Gdn. 17: 69. 1968. Phellinus cf. gilvus (Schw.) Pat., Essai Taxon. Figure 10 Hymenon., p. 97.1900. Material studied: UNITED STATES. FLORIDA: Aquatic Material studied: UNITED STATES. FLORIDA: Aquatic Preserves of Southwest Florida, Punta Gorda, on Preserves of Southwest Florida, Punta Gorda, on Laguncularia racemosa (L.) Gaertn. dead wood, L. racemosa dead wood, position aboveground 50 m, position aboveground 50 em, 20-X-2002, TA. Tattar 20-X-2002, TA. Tattar (BPI843747). (BPI843745); position aboveground I m, 20-X-2002, Remarks: basidiomata badly eaten by insects and TA. Tattar (BPI843746). shows almost no pores left. This species also has Remarks: specimen BPI843746 is young. This species been collected on A. germinans. is common in the Caribbean and is found especially in *Phellinus merrillii (Murrill) Ryv., Norw. J. Bot. 19: xeric localities. It has been found growing on 234.1972. R. mangle dead wood in Boquer6n Wildlife Refuge in Cabo Rojo. Material studied: PUERTO RICO. LAJAS: Magueyes Island, on R. mangle bark and dead wood, position Pycnoporus sanguineus (L.: Fr.) Murrill, Bull. Torrey aboveground 1.2-3 m, 8-V-2003, A.M. Nieves-Rivera Bot. Club 31: 421. 1904. PR-985 (0). Figure II Remarks: it was originally described from the Phi lippine Material studied: PUERTO RICO. CABO RoJO: Islands. The globose, pigmented spores, lustrous Boquer6n Commonwealth Forest, next to Puerto Real, context, and lack of setae characterized P merrillii. boardwalk that passes through a mangrove forest and reaches the lagoon on the Boquer6n-Guaniquilla Meruliaceae mangrove forest, on R. mangle dead wood, position *Phlebia sp. aboveground 50 em, 19-1V-2003, A.M. Nieves-Rivera Material studied: UNITED STATES. FLORIDA: Aquatic PR-984.2 (UPRRP). Preserves of Southwest Florida, Cape Haze, on Remarks: P sanguineus is the one ofcausative agents R. mangle bark on dead aerial roots, position ofthe white rot ofdead hardwoods. This species has aboveground 25 em, April 2003, TA. Tattar FL-9 (0). hyphal contents in some areas oftramal tissue strongly Remarks: this species has a very striking color (bright dextrinoid in Melzer's reagent. P sanguineus is widely orange towards center with white margins) and very distributed throughout the subtropical and tropical large spores; it was sent to Dr. Kurt Hjortstam for regions ofthe world. further study. A similar specimen (UPRRP PR-982) *Tyromyces cf. chioneus (Fr.: Fr.) Karst., Rev. Mycol. also growing on R. mangle dead bark and decay wood 3: 17. 1881. was collected from Boquer6n Commonwealth Forest Figure 12 in Cabo Rojo. Phlebia acanthocystis Gilbn. & 54 Hoehnea 32( I), 2005

Figures 6-13. Further manglicolous basidiomycetes collected on southwestern Puerto Rico and Florida (U.S.A.). 6-7. Psathyrella sp. (Pr = primordium; Bs = basidioma) on Rhizophora mangle leaf litter. 8. Len/inus crini/us. 9. Cori%psis jloccosa. 10. He.xagonia hyclnoides. II. Pycnoporus sanguineus. 12. Tyromyces cf. chioneus on R. mangle wood. 13. Daclyopinax spa/hularia on R. mangle wood. A.M. Nieves Rivera, T.A. Taltar & L. Ryvarden: Manglicolous Basidiomycetes of Puerto Rico and Florida 55

Nakasone was reported from mangroves Bruguiera species than indicated by the previous published gymnorrhiza (L.) Lam. and Rhizophora mucronata records. Lam. in Japan (Maekawa et al. 2003). The basidiomycetes ofthe forests in Puerto Rico, especially the Agaricales are poorly known, and Schizophyllaceae 15-25% is undescribed taxa (Lodge 1996b). For Schizophyllum commune Fr.: Fr., Syst. Mycol. I: 330. instance, Lodge (1996b) mentioned that 30 taxa of 1831. Entolomataceae found by Dr. Timothy 1. Baroni (State University of New York at Cortland) in Puerto Rico Material studied: PUERTO RICO. LAJAS: Magueyes were not previously listed by Stevenson (1975). Island, on R. mangle bark, position aboveground Examples such as these shows that much remains to 0.5-3 m, 5-XI-1998, A.M. Nieves-Rivera (BPI843748). be learned and it will be a monumental task to produce Remarks: this species is commopolitan. S. commune a reasonably complete mycobiota for Puerto Rico. has been seen on a liana in R. mangle canopy at 5 m Therefore, it would seem important to continue in height in Magueyes Island. Causes wood rot and is studying such habitats, in order to contribute to the pathogenic to humans. conservation and knowledge of the biodiversity of basidiomycetes ofPuerto Rico. Dacrymycetaceae Dacryopinax spathularia (Schw.) G.W. Martin, Acknowledgement L10ydia II: 116. 1948. Thanks are extended to Dr. M.e. Aime (USDA­ Figure 13 ARS, Maryland) for the identification ofCrepidotus. Material studied: PUERTO RICO. CABO RoJO: This project was partially supported by the University Boquer6n Commonwealth Forest, on Rhizophora of Puerto Rico Alliance for the Graduate Education mangle decay wood, sometimes in bark, position and the Professorate (AGEP) fellowship for small aboveground 0-1.2 m, 13-III-1995, A.M. Nieves­ projects to AMNR. Digitalization offigure was done Rivera (BPI843743). by P. Rocafort (Dept. of Marine Sciences, Univ. of Remarks: BWR specimens of D. spathularia were Puerto Rico at Mayagtiez). also found on R. mangle wood subjected once or twice a year to brackish water, with an annual surface salinity Literature cited range on to 31 ppt (A.M. Nieves-Rivera, unpublished Almeida-Filho, a.M., Bueno, R. & Bononi, V.L.R. 1993. data). Algumas especies de fungos basidiomicetos dos manguezais do Estado de Sao Paulo. Hoehnea 20: 87-92. Discussion Baccarini, P. 1916. Eumycetes. In: E. Chiovenda (ed.). Le When compared with the assemblage of taxa collezioni botaniche della missione Stefanini-Paoli nella Somalia italiana. Pubblicazioni del Regio Istituto di Studi reported from the Caribbean Islands, the Florida Superiori e di Perfezionamiento di Firenze. L'Erbario records were lower in basidiomycete diversity (e.g., Tropicale di Firenze, Roma, pp. 1-241. Coriolopsis badius, Hexagonia hydnoides, Campos, E.L. & Cavalcanti, M.A.Q. 2000. Primeira Phellinus cf. gilvus, Phlebia sp.). In general, all ocorrencia de Phellinus mangrovicus (Imaz.) Imaz. para basidiomycetes collected showed a tendency of o Brasil. Acta Botanica Brasilica 14: 263-265. dominant species adapted to coastal surroundings and Cintron, G, Goenaga, e. & Gonzalez-Liboy, J. 1978. a few limited unreported species demonstrate an Ecologia del manglar en una zona arida: exposici6n al interesting local distribution ofbasidiomycetes in both oleaje y estructura del manglar. In: Departamento de collection sites. Although many of these Recursos Naturales de Puerto Rico (ed.). Quinto basidiomycetes have been reported previously from Simposio de los Recursos Naturales. Estaci6n Puerto Rico (Stevenson 1975, Lodge 1996a, Nieves­ Experimental Agricola de la Universidad de Puerto Rico, Rivera et al. 1999, Lodge et at. 2000, Minter et al. Rio Piedras, pp. 57-86. 2001), their presence on R. mangle, A. germinans, Cooke, W.B. 1961. The Schizophyllum. Mycologia and L. racemosa suggests that mangroves, although 53: 575-599. usually neglected as a potential substrate for Craighead, F.e. 1971. The trees of South Florida. v.I. basidiomycetes, may support a larger assemblage of University ofMiami Press, Coral Gables, 212 p. 56 Hoehnea 32( I), 2005

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