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Hypogeous Fungus Alpova Austroalnicola Sp. Nov Mycologia, 97(3), 2005. pp. 598-604. © 2005 by The Mycological Society of America, Lawrence, KS 66044-8897 Morphological, molecular and ecological aspects of the South American hypogeous fungus Alpova austroalnicola sp. nov. Eduardo R. Nouhra gon. Beaton et al (1985) broadened it even further Laura S. Dominguez by placing several new Australian Eucalyptus-associ- Alejandra G. Becerra ated species in Alpova. Instituto Multidisciplinario de Biologia Vegetal Molecular data now have demonstrated that the (CONICET), C.C. 495, 5000, Cordoba, Argentina morphological criteria formerly considered impor- James M. Trappe tant in defining genera of hypogeous fungi can be Department of Forest Science, Oregon State University, inadequate for that purpose. Grubisha et al (2001) Corvallis, Oregon 97331-5752 have shown that Alpova diplophloeus relates to the Boletaceae, whereas the Rhizopogon-related species placed by Trappe (1975) in Alpova subgen Alpova sec Abstract: Field studies in Argentinas Yunga District Rhizopogonella belongs in the "suilloid radiation," in revealed Alpova austroalnicola sp. nov., a hypogeous the Rhizopogonaceae. Bougher and Lebel (2002) fungus associated with Alnus acuminata ssp. acumi- transferred the Australian species earlier assigned to nata. Morphological and molecular studies based on Alpova to their new genus Amarrendia. Accordingly, amplification and sequencing of the nuclear LSU the concept of Alpova must revert to the strict sense rDNA gene showed its unique identity within Alpova. of its original description. This concept would in- Related genera included in the analyses were Boletus clude two, perhaps four, of the morphologically sim- edulis, Rhizopogon spp., Suillus luteus and Truncocol- ilar species in Trappes (1975) Alpova subgen. Alpova umella citrina. Additional observations of animal dig- sec. Alpova: A. diplophloeus, A. nauseosus (Coker and gings around the sites and microscopic examination Couch) Trappe, possibly A. mollis (Lloyd) Trappe of fecal pellets of the nine-banded armadillo (Dasy- and A. trappei. However A. mollis is known only from pus novemcinctus novemcinctus) indicate A. austroal- the type collection and A. trappei differs strongly nicola is consumed and its spores dispersed by ani- from the others in its peridial structure; neither is mals. known to be associated with Alnus spp. Grubisha et Key words: Alnus acuminata, Boletales, Dasypus, al (2001) suggested that Alpova might not be mono- molecular systematics, mycophagy, phylogeny phyletic but recognized the need for new studies in- cluding more taxa. A new species of Alpova recently was collected in INTRODUCTION the Yunga District of Argentina in an Alnus acumi- nata Kunth ssp. acuminata forest. The distribution of The genus Alpova originally was described with a sin- A. acuminata ssp. acuminata ranges from Venezuela gle species, A. cinnamomeus C.W. Dodge (1931). to the Andes in Argentina (Furlow 1979, Cabrera and Trappe (1975) discovered it had been described ear- Willink 1980, Aceflolaza 1995). Molecular phyloge- lier as Rhizopogon diplophloeus Zeller & G.W. Dodge netic analysis can be useful for testing whether spe- and recombined it as A. diplophloeus (Zeller C.W. cies with disjunctive ranges are within the same lin- Dodge) Trappe A.H. Sm. The species is character- eage (Koufopanou et al 1977). This is particularly ized by its hypogeous to sometimes emergent habit; important when morphological characters are few or strict association with Alnus spp; solid, gelatinous gle- apparently have converged enough that it is difficult ba that darkens when exposed to air; smooth, thin- to separate similar taxa (Rizzo et al 2003). The nuc- walled, small, ellipsoid to oblong, hyaline CO pale LSU-rDNA gene has been used previously to investi- brown spores; presence of clamp connections; lack gate phylogenetic relationships, particularly in the of a hymenial palisade; and a layer of large, inflated cells in the peridium. Trappe (1975) broadened the Boletales, providing suitable resolution for identify- concept of Alpova to include taxa with similar macro- ing lineages of fungi with good support for terminal branches (Bridge 2002, Grubisha et al 2001, Hum- morphology that were related to the genus Rhizopo- pert et al 2001, Moncalvo et al 2000, Wang et al Accepted for publication 6Jan 2005. 2002). Corresponding author. E-mail: [email protected] We here describe Alpova austroalnicola based on 598 NOUHRA ET AL: ALPOVA AUSTROALNICOLA SP. NOV. 599 its unique morphological characters and molecular MasterAmp Enhancer, Epicentre Technologies, Madison, data obtained from nuc-LSU-rDNA gene analysis. We Wisconsin) and 0.5 pi of 5 U/p.L Taq polyrnerase. The also obtained data on its use as food and spore dis- DNA was amplified with a PTC Programmable Thermal Controller and thermal cycling, as follows: 94 C (2 min), persal by the Argentine nine-banded armadillo, Da- [94 C (30 s), 51 C (30 s), 72 C (45 s)] X 30, [94 C (30 s), sypus novemcinctus novemcinctus, known by the com- 53 C (30 s), 72 C (45 s + 5 s per cycle)] x 5, 72 C (5 min), mon name of mulita grande or armadillo de nueve 4 C (15 min). PCR products were viewed on 1% agarose bandas. This subspecies inhabits northern Argentina: gels (Gibco-BRL ultra PURE, Life Technologies) in a UV light transilluminator (UVP Laboratory products), stained with ethidium bromide and quantified with a low DNA mass METHODS ladder (Gibco-BRL Ultra PURE, Life Technologies). The Sporocarp sampling and morphological description.-Sporo- amplified DNA was purified with a PCR purification kit carps were collected in Mar 2001 in a forest dominated by (QIAquick, QIAGEN Inc.). Purified PCR products were se- Alnus acuminate ssp. acuminata in northwestern Argentina. quenced with LROR primer on a 373 DNA Sequencer (Ap- Plots had been established previously near Los Toldos in plied Biosystems). Salta Province, site M28 (eroded area with isolated groups LSU rDNA sequences were assembled with SegEditor ver- of Alnus trees), elevation 1702 m; 22°14'93"S, 64°40'79"W, sion 1.0.3 (Applied Biosystems) and visually aligned with and site M42 (Alnus dominated forest), elevation 1778 m, PAUP* 4.0blO (Swofford 1999). Two collections of Alpova " 22°16 ' 57 S, 64°43 ' 13 'W. The average annual precipitation is austroalnicola and three collections of A. diplophloeus se- 1300 mm. Sites are characterized by the dominant A. acu- quences were compared with closely related taxa sequences minata spp. acuminata ca. 45 y old, plus other relatively selected from GenBank: A. diplophloeus, A. trappei Fogel., abundant species: Amomyrtella guili (Speg.) Kausel, Clethra Boletus edulis Fr, Rhizopogon occidentalis Zeller & C.W. scabra Pers., Ilex argentina Lillo, Maytenus cuezzoi Legname, Dodge, R. truncatus Linder, R. villosulus Zeller, Suillus lu- Myrica pubescens var. glabra Chev. and Podocarpus parlatorei teus (Fr.) Gray and Truncocolumella citrina Zeller. Herbari- Pilg. Soils are Inseptisols (Haplumbreptes enticos), with um, collector and GenBank accession numbers are provid- high organic matter content (site M28 = 9.77%, site M42 ed (TABLE I). = 9.61%). Ambiguous insertion/deletions (indels) and gaps were Sporocarps were photographed with a Leica M420 stereo treated as missing data. Phylogenetic analyses were per- microscope. Color reactions and microscopic characters formed in PAUP* 4.0blO. Most parsimonious trees (MPTs) were determined from hand-sectioned mounts in 15% were recovered by the heuristic search option (TBR and KOH, Melzer's reagent, cotton blue and FeSO4 and pho- MulTrees on) and 1000 replicates of random sequence ad- tographed with a Zeiss Axiophot light microscope. Voucher dition. Support for individual branches was estimated specimens were deposited in the Museo Botanico de Cor- through 1000 bootstrap replicates by the heuristic search doba Herbarium (CORD). option with 100 random sequence additions per replicate, TBR and MulTrees on. Characters were of type "unord " Fecal pellet analysis. Armadillo fecal pellets were collected - and have equal weight. Of the total number of 646 char near animal diggings on the sites where Alpova austroalni- acters, 586 were uninformative; due to gaps 60 were infor- cola sp nov. was sampled. Twelve samples of collected pellets mative for parsimony. were analyzed microscopically (25 fields randomly selected per sample at 600X). Fungal elements (spores and hyphae), plant, animal and mineral material were counted following TAXONOMY procedures of McIntire and Carey (1989). Molecular and phylogenetic analysis.-A small amount of Alpova austroalnicola L.S. Dominguez, sp. nov. sporocarp tissue was ground with a drill-driven plastic pestle FIGS. 1-9 in an Eppendorf tube containing 200 µL of 2X CTAB lysis Basidiomata subhypogaea vel hypogaea, globosa vel irre- buffer. Additional buffer was added up to 500 p.L and gularia, 4-11 X 6-15 pm. Peridiunr 400-570 µm .crassum, mixed; the tubes were frozen and thawed twice, alternating pseudoparenchymatum, fibulatum, brunneolum, ube con- between dry ice and a 65 C water bath. The tubes were tusum fuscescens. Rhizomorphae concolores, ad peridium incubated in the bath 30-60 min. Chloroform was added adpressae. Gleba solidi, lenta vet gelatinosa; loculis 0.4-0.65 to the mixture, which was spun 15 min at 13 000 rpm. The mm latis, venis brunneolis separati. Odor nullus. Basidio- aqueous phase was removed and cleaned with a glass-milk sporae hyalinae, laeves, ellipsoideae vel oblongae, tunicis solution (GENECLEAN III ® , BIO 101); the extracted DNA pal-um incrassatus,
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