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Sarcodon in the Neotropics I: New Species from Guyana Puerto Rico

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Sarcodon in the Neotropics I: New Species from Guyana Puerto Rico Mycologia, 107(3), 2015, pp. 591–606. DOI: 10.3852/14-185 # 2015 by The Mycological Society of America, Lawrence, KS 66044-8897 Sarcodon in the Neotropics I: new species from Guyana, Puerto Rico and Belize Arthur C. Grupe II pakaraimensis, S. portoricensis, S. quercophilus and S. Anthony D. Baker umbilicatus and, along with morphological differ- Department of Biological Sciences, Humboldt State ences, supported their recognition as distinct species. University, Arcata, California 95521 Macromorphological, micromorphological, habitat Jessie K. Uehling and DNA sequence data from the nuc rDNA internal University Program in Genetics & Genomics, Duke transcribed spacer region (ITS) are provided for each University, Durham, North Carolina 27708 of the new species. A key to Neotropical Sarcodon species and similar extralimital taxa is provided. Matthew E. Smith Key words: Bankeraceae, Caribbean, Central Department of Plant Pathology, University of Florida, Gainesville, Florida 32611 America, ectomycorrhizal fungi, Guiana Shield, The- lephorales, tooth fungi Timothy J. Baroni Department of Biological Sciences, State University of New York—College at Cortland, New York 13045 INTRODUCTION D. Jean Lodge Sarcodon Que´l. ex P. Karst. (Bankeraceae, Thelephor- Center for Forest Mycology Research, USDA-Forest ales) is an ectomycorrhizal (ECM) basidiomycete Service, Forest Products Laboratory, PO Box 1377, genus characterized by stipitate, pileate basidiomata Luquillo, Puerto Rico 00773 with determinate development, fleshy, non-zonate context, dentate hymenophore, variably tuberculate, Terry W. Henkel1 brown basidiospores, and the presence or absence of Department of Biological Sciences, Humboldt State University, Arcata, California 95521 clamp connections (Banker 1906, Maas Geesteranus 1971). Approximately 87 species of Sarcodon have been described worldwide, mostly from high latitude Abstract: Four species of the ectomycorrhizal (ECM) forest environments (Coker and Beers 1951, Maas genus Sarcodon (Bankeraceae, Thelephorales, Basi- Geesteranus 1971, McNabb 1971, Harrison 1973, diomycota) are described as new to science. Sarcodon Baird 1986, Baird and Khan 1986, Harrison and pakaraimensis sp.nov.isdescribedfromforests Grund 1987, Agerer 1991, Stalpers 1993, Visser 1995, dominated by the ECM trees Pakaraimaea dipterocar- Shiryaev 2008, Mleczko et al. 2011, Baird et al. 2013, pacea (Dipterocarpaceae) and Dicymbe jenmanii (Fa- Vizzini et al. 2013). All known species of Sarcodon fruit baceae subfam. Caesalpinioideae) in the Pakaraima on the soil in spatial association with ECM plants and Mountains of Guyana. Sarcodon portoricensis sp. nov. is available evidence suggests that Thelephorales spe- described from lower montane wet forest within the cies, including those of Sarcodon, are ECM (Stalpers El Yunque National Forest of Puerto Rico. Sarcodon 1993, Tedersoo and Smith 2013). The ECM status of quercophilus sp. nov. and Sarcodon umbilicatus sp. nov. Sarcodon has been confirmed for Sarcodon imbricatus are described from Quercus (Fagaceae) cloud forests (L.) P. Karst. on Picea abies (L.) H. Karst. in Germany within the Maya Mountains of Belize. The discovery of (Agerer 1991), Sarcodon scabrosus (Fr.) P. Karst. on these species is significant given that the majority of Pinus banksiana Lamb. (Visser 1995) in Canada, the approximately 87 described Sarcodon species are Sarcodon leucopus (Pers.) Maas Geest. & Nannf. with north temperate or boreal in distribution and other Pinaceae hosts in Poland (Mleczko et al. 2011), frequently associate with coniferous host plants; these and Sarcodon atroviridis (Morgan) Banker on Abies constitute the most recent records for Sarcodon from pindrow (Royle ex D. Don) Royle in Pakistan (Niazi the greater Neotropics. Each of the new species is 2008). While largely Holarctic in distribution, some morphologically consistent with accepted diagnostic Sarcodon species are known from the Paleotropics characters for Sarcodon: pileate-stipitate stature, (Maas Geesteranus 1964, 1967, 1971, 1974a, Watling a dentate hymenophore, determinate basidiomatal and Lee 1995), but records from the Neotropics are development, fleshy, non-zonate context and brown, scarce (Baker and Dale 1951, Snell and Dick 1958, tuberculate basidiospores. DNA (ITS) sequence anal- Maas Geesteranus 1974b, Singer et al. 1983). Here we ysis corroborated the generic placement of S. provide new reports for the genus in the Neotropics from the Guiana Shield, northern Caribbean, and Submitted 15 Jul 2014; accepted for publication 29 Dec 2014. Central America. Sarcodon pakaraimensis sp. nov. is 1 Corresponding author. E-mail: [email protected] described from Guyana, in forests dominated by the 591 592 MYCOLOGIA endemic ECM trees Pakaraimaea dipterocarpaceae a forced-air drying oven. Micromorphological features of Maguire & P.S. Ashton (Dipterocarpaceae) and dried specimens were examined with an Olympus BX51 Dicymbe jenmanii Sandw. (Fabaceae subfam. Caesalpi- microscope with light and phase contrast optics. Fungal nioideae). Sarcodon portoricensis sp. nov. is described tissue was mounted in H2O, 3% potassium hydroxide from a lower montane wet forest of the El Yunque (KOH), or Melzer’s solution. At least 20 individual basidiospores, basidia and other structures were measured National Forest of Puerto Rico. Sarcodon quercophilus per collection; for basidiospores measurements were taken sp.nov.andSarcodon umbilicatus sp.nov.are from spore deposits when possible, with dimensional described from ECM Quercus-dominated (Fagaceae) measurements including ornamentation. Range and mean cloud forests of the Maya Mountains of Belize. quotients of basidiospore length divided by width (Q) were All of the new species are morphologically similar calculated. Outlying measurements observed in less than but distinguishable from each other, and similar to 5% of the measured population are indicated in parenthe- a group of previously described species defined by ses. Line drawings were made with tracing paper and their non-scaly pilei, overall somber basidioma colors, modified with Photoshop CS5 (Adobe, San Jose, Califor- and KOH-soluble bluish green pigments (Maas nia). Specimens were deposited in these herbaria (Holm- Geesteranus 1971), in particular Sarcodon atroviridis grenetal.1990):BRG,UniversityofGuyana;HSU, Humboldt State University; CORT, State University of New (Morgan) Banker from temperate North America, York at Cortland; NY, New York Botanical Garden; BRH, Europe, and East Asia, Sarcodon thwaitesii (Berk. & Forest Department Herbarium, Ministry of Natural Re- Br.) Maas G. from the Asian tropics, and Sarcodon sources, Local Government and the Environment of Belize; bambusinus (Baker & Dale) Maas G. from the UPRRP, University of Puerto Rico at Rio Piedras. Neotropics (Berkeley and Broome 1873, Morgan 1895, Baker and Dale 1951, Maas Geesteranus 1964, DNA extraction, amplification, sequencing and phylogenetic 1974b, 1975). Variation in key morphological char- analyses.—DNA extraction, polymerase chain reactions acteristics corroborated by molecular phylogenetic (PCR), cloning and sequencing protocols followed Gardes analysis warrant the erection of the four new species, and Bruns (1993), with the following modifications. DNA and indicate their close relationship within the genus. was extracted from dried basidiomata by placing tissue Macromorphological, micromorphological, habitat, samples into 1.5 mL tubes with 0.1 mm glass beads and 400 and DNA sequence data from the nuc rDNA internal mL CTAB heated to 60 C. Tissues were ground with a plastic micropestle, incubated overnight at 57 C with 700 rpm transcribed spacer region (ITS) are provided for each shaking on an Eppendorf Thermomixer R (Eppendorf of the new species. A key to Neotropical Sarcodon International, http://www.eppendorf.com). This resulted species and similar extralimital taxa is provided. in dark samples, presumably from the copious pigments present in the basidiomata. The tubes were centrifuged at 8 MATERIALS AND METHODS 000 rpm to pelletize debris, and the supernatant was transferred to a new tube and brought to 500 mL with Collections.—Guyana collections were made during the CTAB. Eight hundred microliters chloroform was added Dec–Jan rainy season of 201022011 from the Upper and the tubes inverted for 1 min before centrifuging at full Mazaruni River Basin in the Pakaraima Mountains, in the speed 10 min. The supernatant was removed and extracted vicinity of a base camp at 5u26921.30N, 60u04943.10W; , 800 in 800 mL chloroform. DNA was precipitated with two m. This area is , 15 km west of Mount Ayanganna (2200 m) volumes of 100% isopropanol and 1/10 volume ammonium and characterized by a mixture of open savannas and closed acetate at 220 C overnight. DNA was pelleted by centrifu- canopy forests on white sand soils (Smith et al. 2013). gation at full speed for 10 min. The DNA pellet was washed Collections were made in forests co-dominated by the ECM in 70% ethanol and resuspended in 13 TE buffer. trees P. dipterocarpacea and D. jenmanii.PuertoRico PCR reactions were performed with 1 mL DNA diluted collections were made Jun–Jul 1998 in a lower montane 1:10, 0.4 mM primer and 12.5 mL EconoTaq Plus 23 wet forest along the Pico El Toro Trail in the El Yunque Mastermix as per manufacturer’s recommendations (Luci- National Forest (previously known as the Caribbean gen Corp., Middleton, Wisconsin). Cycling temperatures National Forest) in the general locality of 18u179N were: initial denaturation at 94 C for 10 min; cycle
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