Abstract
Much of our previous work documenting fungal biodiversity in Guyana has been centered in forests of Dicymbe corymbosa Spruce ex Benth., which forms monodominant stands in the white sands region of Guyana. In order to begin to assess fungal biodiversity associated with other ectomycorrhizal host trees found in Guyana, expeditions were conducted to areas containing Dicymbe altsonii and Pakaraimaea dipterocarpacea. In this paper, we describe two new species of Russula from Guyana with diminutive basidiomata: R. lilliputia and R. pakaraimaeae, found in association with these tree hosts, using a combined approach of morphological characterization and molecular analyses. Together with R. gelatinivelata, which we previously described from Guyana, R. lilliputia and R. pakaraimaeae form what appears to be a new lineage within the crown clade of Russula, sister to the subsect. Auratinae. Synapomorphies for the lineage include a pruinose to subtomentose pileus in dry conditions, suprapellis comprised of inflated cells that give rise to long cylindrical or digitate, and sinuous, thin or thick-walled pileocystidia that are strongly emergent, easily disarticulate in microscopic preparations, and have contents that are acid resistant in Basic Fuchsin, pruinose to subomentose patches on the stipe, suprahilar plage on the basidiospores, spore ornamentation of mostly isolated verrucae, and geographic distribution restricted to the Pakaraima Mountains of Guyana. Full descriptions, photos, line drawings of microscopic features, and comparisons with related species are provided.
References
- Adamčík, S., Caboň, M., Eberhardt, U., Saba, M,, Hampe, F., Slovák, M., Kleine, J., Marxmüller, H., Jančovičová, S., Pfister, D.H., Khalid, A.N., Kolařík, M., Marhold, K. & Verbeken, A. (2016a) A molecular analysis reveals hidden species diversity within the current concept of Russula maculata (Russulaceae, Basidiomycota). Phytotaxa 270 (2): 71–88. https://doi.org/10.11646/phytotaxa.270.2.1
- Adamčík, S., Slovákm, M., Eberhardt, U., Ronikier, A., Jairus, T., Hampe, F. & Verbeken, A. (2016b) Molecular inference, multivariate morphometrics, and ecological assessment are applied in concert to delimit species in the Russula clavipes complex. Mycologia 108: 716–730. https://doi.org/10.3852/15-194
- Adamčík, S., Looney, B., Caboň, M., Jančovičová, S., Adamčíková, K., Avis, P.G., Barajas, M., Bhatt, R.P., Corrales, A., Das, K., Hampe, F., Ghosh, A., Gates, G., Kälviäinen, V., Khalid, A.N., Kiran, M., De Lange, R., Lee, H., Lim, Y.W., Kong, A., Manz, C., Ovrebo, C., Saba, M., Taipale, T., Verbeken, A., Wisitrassameewong, K. & Buyck, B. (2019) The quest for a globally comprehensible Russula language. Fungal Diversity 99: 369–449. https://doi.org/10.1007/s13225-019-00437-2
- Bon, M. (1988) Monographic key for European Russulae. Documents Mycologiques 18 (71–72): 1–125.
- Buyck, B. (1990a) New taxa of tropical Russulae: Pseudoepitheliosinae subsect. nov. Mycotaxon 39: 317–327.
- Buyck, B. (1990b) Nouveaux taxons infragénériques dans le genre Russula Persoon en Afrique centrale. Bulletin Jardin Botanique National de Belgique 60: 191–211. http://dx.doi.org/10.2307/3668341
- Buyck, B. (1994a) Russula I. (Russulaceae). In Rammeloo, J. & Heinemann, P. (Eds.) Flore Illustrée des Champignons d’Afrique Centrale. Vol. 15. pp. 335–408.
- Buyck, B. (1994b) Russula II. (Russulaceae). In: Rammeloo, J. & Heinemann, P. (Eds.) Flore Illustrée des Champignons d’Afrique Centrale. Vol. 16. pp. 411–542.
- Buyck, B., Hofstetter, V., Eberhardt, U., Verbeken, A. & Kauff, F. (2008) “Walking the thin line between Russula and Lactarius: the dilemma of Russula sect. Ochricompactae”. Fungal Diversity 28: 15–40.
- Buyck, B., Zoller, S. & Hofstetter, V. (2018) Walking the thin line ten years later: The dilemma of above-versus below-ground features to support phylogenies in the Russulaceae (Basidiomycota). Fungal Diversity 89: 267–292. https://doi.org/10.1007/s13225-018-0397-5
- Buyck, B., Hofstetter, V., Horak, E., Cooper, J. & Bougher, N. (2023) The search for Australian relatives of the eucalypt-associated Russula prolifica (Russulales) from Madagascar reveals new Oceanian taxa in subsection Auratinae. Australian Journal of Taxonomy 47: 1–25. https://doi.org/10.54102/ajt.1rdyq
- Das, K., Gosh, A., Bhatt, R.P., Chakraborty, D., Hofstetter, V. & Buyck, B. (2017) Fungal Biodiversity Profiles 41–50. Cryptogamie, Mycologie 38: 527–547.
- Gosh, A., Buyck, B., Chakraborty, D., Hembrom, M.E., Bera, I. & Das, K. (2023) Three new species of genus Russula Pers. from Sal dominated forests of tropical India based on morphotaxonomy and multigene phylogenetic analysis. Cryptogamie, Mycologie 44 (3): 27–50.
- Heim, R. (1937a) Les Lactario-Russulés du domaine oriental de Madagascar. Prodrome à une flore mycologique de Madagascar et dépendances 1: 1–196.
- Heim, R. (1937b) Observations sur la flore mycologique malgache V. Les Lactario-Russules a anneau: Ontogenie et phylogenie III. Revue de Mycologie (Paris) 2: 61–75.
- Heim, R. (1938) Diagnoses latine d’espèces et variéte Nouvelles de Lactario-russulés du domaine oriental de Madagascar. Candollea 7: 374–393.
- Heim, R. (1970) Particularités remarquables des Russules tropicales Pelliculariae lilliputiennes; les complexes annulate et radicans. Bulletin. Sociéte Mycologique de France 86: 59–77.
- Henkel, T.W., Aime, M.C. & Miller, S.L. (2000) Systematics of pleurotoid Russulaceae from Guyana and Japan, with notes on their ectomycorrhizal status. Mycologia 92: 1119–1132. http://dx.doi.org/10.2307/3761479
- Henkel, T.W., Aime, M.C., Chin, M., Miller, S.L., Vilgalys, R. & Smith, M. (2012) Ectomycorrhizal fungal sporocarp diversity and discovery of new taxa in Dicymbe monodominant forests of the Guiana Shield. Biodiversity and Conservation 21: 2195–2220. http://dx.doi.org/10.1007/s10531-011-0166-1
- Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35 (2): 518–522. https://doi.org/10.1093/molbev/msx281
- Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & and Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285
- Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
- Kornerup, A. & Wanscher, J.H. (1981) Methuen handbook of colour. 3rd ed. London: Eyre Methuen. 252 pp.
- Looney, B.P., Ryberg, M., Hampe, F., Sánchez-García, M. & Matheny, P.B. (2016) Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi. Molecular Ecology 25: 630–647.
- Lücking, R & Hawksworth, D.L. (2018) Formal description of sequence-based voucherless Fungi: promises and pitfalls, and how to resolve them. IMA Fungus 9: 143–165.
- Maire, R. (1919) Russula romellii. Bulletin de la Société mycologique de France 26: 105.
- Miller, S.L. & Buyck, B. (2002) Molecular phylogeny of the genus Russula in Europe with a comparison of modern infrageneric classifications. Mycological Research 106: 259–276. https://doi.org/10.1017/S0953756202005610
- Miller, S.L. & Henkel, T.W. (2004) Biology and molecular ecology of subiculate Lactarius species from Guyana. In: Cripps, C.L. (Ed.) Fungi in Forest Ecosystems– Systematics, Diversity, and Ecology. Memoirs of the New York Botanic Garden, vol. 89. pp. 297–313.
- Miller, S.L., Aime, M.C. & Henkel, T.W. (2002) Russulaceae from the Pakaraima Mountains of Guyana. I. New species of pleurotoid Lactarius. Mycologia 94: 545–553. http://dx.doi.org/10.2307/3761789
- Miller, S.L., Aime, M.C. & Henkel, T.W. (2012) Russulaceae of the Pakaraima Mountains of Guyana 2. New Species of Russula and Lactifluus. Mycotaxon 121: 233–253.
- Miller, S.L., Larsson, E., Larsson, K.-H., Verbeken, A. & Nuytinck, J. (2006) Perspectives in the new Russulales. Mycologia 98: 960–970. http://dx.doi.org/10.3852/mycologia.98.6.960
- MycoBank (2024) “Mycobank: Russula”, International Mycological Association. Available from: https://www.mycobank.org (accessed 1 May 2024)
- Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300
- Okonechnikov, K., Golosova, O., Fursov, M. & the UGENE team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28: 1166–1167. https://doi.org/10.1093/bioinformatics/bts091
- Persoon, C.H. (1796) Descriptiones tam novorum quan notabilium fungorum. Observations Mycologicae 1: 1–221.
- Romagnesi, H. (1985) Les Russules d’Europe et d’Afrique du Nord. Reprint with supplement. J. Cramer, Lehre. 1030 pp.
- Singer, R. (1952) Russulaceae of Trinidad and Venezuela. Kew Bulletin 7: 295–301. http://dx.doi.org/10.2307/4109329
- Singer, R. (1986) The Agaricales in modern taxonomy. 4th ed. Koeltz Scientific Books, Koenigstein, Germany. 981 pp.
- Singer, R., Araujo, I. & Ivory, M.H. (1983) The ectotrophically mycorrhizal fungi of the neotropical lowlands, especially central Amazonia. Beihefte Nova Hedwigia 77: 1–352.
- Smith, M.E., Henkel, T.W., Uehling, J.K., Fremier, A.K., Clarke, H.D. & Vilgalys, R. (2013) The ectomycorrhizal fungal community in a neotropical forest dominated by the endemic dipterocarp pakaraimaea dipterocarpacea. PLoS ONE 8 (1): e55160. https://doi.org/10.1371/journal.pone.0055160
- Species Fungorum (2024) “Search Page”, Royal Botanic Garden. Available from: www.speciesfungorum.org (accessed May 1 2024)
- Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B.Q. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44 (W1): W232–W235. https://doi.org/10.1093/nar/gkw256
- Vidal, J.M., Alvarado, P., Loizides, M., Konstantinidis, G., Chachuła, P., Mleczko, P., Moreno, G., Vizzini, A., Krakhmalnyi, M., Paz, A., Cabero, J., Kaounas, V., Slavova, M., Moreno-Arroyo, B. & Llistosella, J. (2019) A phylogenetic and taxonomic revision of sequestrate Russulaceae in Mediterranean and temperate Europe. Persoonia 42: 127–185. https://doi.org/10.3767/persoonia.2019.42.06
- Zhou, H., Cheng, G.-Q., Wang, Q.-T., Guo, M.-J., Zhuo, L., Yan, H.-F., Li, G.-J. & Hou, C.-L. (2022) Morphological Characteristics and Phylogeny Reveal Six New Species in Russula Subgenus Russula (Russulaceae, Russulales) from Yanshan Mountains, North China. Journal of Fungi 8 (12): 1283–1316. https://doi.org/10.3390/jof8121283