Open Access Open Access  Restricted Access Subscription or Fee Access


New sources of taxonomic information for earthstars (Geastrum, Geastraceae, Basidiomycota): phenoloxidases and rhizomorph crystals

Juan Carlos Zamora, Francisco De Diego Calonge, María Paz Martín


The taxonomic utility of two characters not previously used for identification of Geastrum species is evaluated. First, macrochemical spot tests with chemicals detecting phenoloxidase enzymatic activity (1-naphthol, guaiac gum, and syringaldazine), are performed. In addition, the usefulness of the crystalline deposits from the rhizomorphs, formed by calcium oxalate as monohydrate or whewellite, and dihydrate or weddellite, was evaluated. These features provide valuable data to distinguish some taxa difficult to separate using traditional morphology, such as G. lageniforme, G. saccatum, and G. triplex.


Geastrum; Geastraceae; phenoloxidases; rhizomorph crystals; taxonomy


Agerer, R. (1999) Never change a successful principle: the evolution of Boletales s.l. (Hymenomycetes, Basidiomycota) as seen from below ground features. Sendtnera 6: 5–91.

Agerer, R. & Beenken, L. (1998) Geastrum fimbriatum Fr. + Fagus sylvatica L. Descriptions of Ectomycorrhizae 3: 13–18.

Agerer, R. & Iosifidou, P. (2004) Rhizomorph structures of Hymenomycetes: a possibility to test DNA-based phylogenetic hypotheses? In: R. Agerer, M. Piepenbring & P. Blanz (eds.) Frontiers in Basidiomycote Mycology. IHW-Verlag, Berchtesgaden, pp. 249–302.

Batsch, A.J.G.K. (1783) Elenchus fungorum. Halae, Magdeburgicae, 183 pp.

Baseia, I.G. & Milanez, A.I. (2002) Geastrum setiferum (Gasteromycetes): a new species with a setose endoperidium. Mycotaxon 84: 135–139.

Berkeley, M.J. & Curtis, M.A. (1853) Exotic fungi from the Schweinitzian Herbarium, principally from Surinam. Journal of the Academy of Natural Sciences of Philadelphia 2: 277–294.

Bidaud, A., Moėnne-Loccoz, P. & Reumaux, P. (1994) Atlas des Cortinaires: clé générale des sous-genres, sections, sous-sections et series. Éditions Fédération Mycologique Dauphiné-Savoie, Annecy-Seynod, 102 pp.

Bonorden, H.F. (1851) Handbuch der allgemeinen Mykologie. Schweizerbart'sche Verlagshandlung, Stuttgart, 336 pp.

Bourquelot, E. & Bertrand, G. (1896) Les ferments oxydants dans les Champignons. Bulletin de la Société Mycologique de France 12: 18–26.

Calendini, F. & Martin, J.-F. (2005) PaupUp v1.0.3.1 A free graphical frontend for PAUP* Dos software. Available from (accessed: 1 Jul 2012).

Calonge, F.D. (1998) Gasteromycetes. I. Lycoperdales, Nidulariales, Phallales, Sclerodermatales, Tulostomales. Flora Mycologica Iberica 3: 1–271.

Calonge, F.D. & Mata, M. (2004) A new species of Geastrum from Costa Rica and Mexico. Boletķn de la Sociedad Micológica de Madrid 28: 331–335.

Calonge, F.D., Moreno-Arroyo, B. & Gómez, J. (2000) Aportación al conocimiento de los Gasteromycetes, Basidiomycotina de Bolivia. Geastrum ovalisporum sp. nov. Boletķn de la Sociedad Micológica de Madrid 25: 271–276.

Coker, W.C. (1924) The geasters of the United States and Canada. Journal of the Elisha Mitchell Scientific Society 39: 170–224.

Cunningham, G.H. (1944) The Gasteromycetes of Australia and New Zealand. Bibliotheca Mycologica 67: 1–239.

Czerniaiev, B.M. (1845) Noveaux cryptogames de l’Śkraine et quelques mots sur la flore de ce pays. Bulletin de la Société Impériale des Naturalistes de Moscou 18(2): 132–157.

Desvaux, N.A. (1809) Observations sur quelques genres į établir dans la famille des champignons. Journal de Botanique (Desvaux) 2: 88–105.

Dissing, H. & Lange, M. (1962) Gasteromycetes of Congo. Bulletin du Jardin Botanique de l’État ą Bruxelles 32: 325–416.

Donk, M.A. (1933) Revisie van de Nederlandse Heterobasidiomycetae en Homobasidiomycetae - Aphyllophoraceae I. Mededelingen van de Nederlandse Mycologische Vereeniging 18–20: 67–200.

Douanla-Meli, C., Langer, E. & Calonge, F.D. (2005) Geastrum pleosporus sp. nov., a new species of Geastraceae identified by morphological and molecular phylogenetic data. Mycological Progress 4(3): 239–250.

Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.

Fitch, W.M. & Margoliash, E. (1967) Construction of phylogenetic trees. Science 155: 279–284.

Frey-Wyssling, A. (1981) Crystallography of the two hydrates of crystalline calcium oxalate in plants. American Journal of Botany 68(1): 130–141.

Fries, E. (1821) Systema mycologicum, vol. 1. Lund, LVII + 520 pp.

Fries, E. (1829) Systema mycologicum, vol. 3. Greifswald, VIII + 259 pp.

Fries, E. (1838) Epicrisis Systematis Mycologici, seu Synopsis Hymenomycetum. Uppsaliae, 610 pp.

Fries, E. (1863) Monographia Hymenomycetum Sueciae, vol. 2. C.A. Leffler, Uppsala, 355 pp.

Gilbertson, L., Lombard, F.F. & Canfield, E.R. (1975) Guaiac gum in field tests for extracellular phenol oxidases of wood-rotting fungi and other basidiomycetes. USDA Forest Research Paper FPL 269: 1–23.

Gower, J.C. (1971) A general coefficient of similarity and some of its properties. Biometrics 27: 857–874.

Gray, S.F. (1821) A natural arrangement of British plants. Baldwin, Cradock and Joy, London, 824 pp.

Harkin, J.M. & Obst, J.R. (1973) Syringaldazine, an effective reagent for detecting laccase and peroxidase in fungi. Experientia 29: 381–387.

Harkin, J.M., Larsen, M.J. & Obst, J.R. (1974) Use of syringaldazine for detection of laccase in sporophores or wood rotting fungi. Mycologia 66(3): 469–476.

Hillis, D.M & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Botany 42(2): 182–192.

Hollós, L. (1904) Die Gasteromyceten Ungarns. Oswald Weigel, Leipzig, 278 pp.

Horner, H.T., Tiffany, L.H & Cody, A.M. (1985) Calcium oxalate bipyramidal crystals on the basidiocarps of Geastrum minus (Lycoperdales). The Proceedings of the Iowa Academy of Science 92(2): 70–77.

Horner, H.T., Tiffany, L.H. & Knaphus, G. (1995) Oak-leaf-litter rhizomorphs from Iowa and Texas: Calcium oxalate producers. Mycologia 87(1): 34–40.

Jiménez-Mejķas, P. & Martinetto, E. (2013) Toward an accurate taxonomic interpretation of Carex fossil fruits (Cyperaceae): A case study in section Phacocystis in the Western Paleartic. American Journal of Botany 100(8): 1580–1603.

Junghuhn, F. (1840) Nova genera et species plantarum florae Javanicae. Tijdschrift voor Natuurlijke Geschiedenis en Physiologie 7: 285–317.

Karsten, P. (1890) Fragmenta mycologica XXIX. Hedwigia 29: 147–149.

Kasuya, T., Hosaka, K., Uno, K. & Kakishima, M. (2012) Phylogenetic placement of Geastrum melanocephalum and polyphyly of Geastrum triplex. Mycoscience 53(6): 411–426.

Keller, J. (1979) Ustrastructure des hyphes incrustées dans le genre Skeletocutis. Persoonia 10(3): 347–355.

Keller, J. (1985) Les cystides crystallifčres des Aphyllophorales. Mycologia Helvetica 1(5): 277–340.

Kerrigan, R.W. (1986) The Agaricales (Gilled Fungi) of California. 6. Agaricaceae. Mad River Press Inc. Eureka, California, 62 pp.

Kirk, P.M., Cannon, P.F., Minter, D.W. & Stalpers, J.A. (2008) Ainsworth and Bisby’s Dictionary of the Fungi, 10th edition. CABI Europe, UK, Wallingford, 771 pp.

Kitching, I.J., Forey, P.L., Humphries, C.J., Williams, D.M. (1998) Cladistics: the theory and practice of parsimony analysis. Oxford University Press, Oxford, New York, Tokyo.

Kotlaba, F. & Pouzar, Z. (1958) Polypori novi vel minus cogniti Cechoslovakiae III. Ceskį Mykologie 12(2): 95–104.

Krisai, I. & Mrazek, E. (1986) Calcium oxalate crystals in Geastrum. Plant Systematics and Evolution 154: 325–341.

Lamarck, J.-B. & de Candolle, A.P. (1805) Flore franēaise, ou Descriptions succinctes de toutes les plantes qui croissent naturellement en France: disposées selon une nouvelle Méthode d’Analyse, et précédées par un Exposé des Principes élémentaires de la Botanique, vol. 2. Chez H. Agasse, Paris, 600 pp.

Largent, D.L. & Benedict, R.G. (1970) Studies in the Rhodophylloid fungi II: Alboleptonia, a new genus. Mycologia 62(3): 437–452.

Larsson, K.-H. (1994) Poroid species in Trechispora and the use of calcium oxalate crystals for species identification. Mycological Research 98(10): 1153–1172.

Linnaeus, C. (1753) Species Plantarum. Salvius, Stockholm, 1200 pp.

Lloyd, C.G. (1901) Mycological Notes by C.G. Lloyd. No. 8. Mycological Writings 1: 73–78.

Lloyd, C.G. (1902) The Geastrae. Bulletin of the Lloyd Library of Botany, Pharmacy and Materia Medica 2: 1–43.

Maechler, M. Rousseeuw, P., Struyf, A., Hubert, M., Hornik, K. (2013) cluster: Cluster Analysis Basics and Extensions. R package version 1.14.4.

Marr, C.D. (1979) Laccase and tyrosinase oxidation of spot test reagents. Mycotaxon 9(1): 244–276.

Marr, C.D., Grund, D.W & Harrison, K.A. (1986) The taxonomic potential of laccase and tyrosinase spot tests. Mycologia 78(2): 169–184.

Methven, A.S. (1990) The genus Clavariadelphus in North America. Bibliotheca Mycologica 138: 1–192.

Morgan, A.P. (1887) The genus Geaster. The American Naturalist 21: 1026–1029.

Morgan, A.P. (1895) New North American fungi. Journal of the Cincinnati Society of Natural History 18: 36–45.

Parra, L.A. (2008) Agaricus L. Allopsalliota Nauta & Bas. I. Fungi Europaei 1: 1–824.

Pérez-Daniėls, P. (2002) Estudio biosistemįtico del orden Gomphales (Basidiomycota, Fungi) en la Penķnsula Ibérica. Ph. D. [unpublished]. Universidad Complutense de Madrid.

Persoon, C.H. (1794) Neuer Versuch einer systematischen Einteilung der Schwämme. Neues Magazin für die Botanik 1: 63–128.

Persoon, C.H. (1795) Observationes mycologicae. Annalen der Botanik (Usteri) 15: 1–39.

Persoon, C.H. (1796) Observationes mycologicae, vol. 1. Wolf, Leipzig, 116 pp.

Persoon, C.H. (1801) Synopsis Methodica Fungorum. Göttingen, 106 pp.

Ponce de León, P. (1968) A Revision of the Family Geastraceae. Fieldiana. Botany 31(14): 301–349.

Quélet, L. (1886) Enchiridion fungorum in Europae mediae et praesertim in Gallia virgentium. Lutetiae, Paris, 352 pp.

Rambaut, A. (2007) Molecular evolution, phylogenetics and epidemiology. FigTree. Available from: (accessed: 1 Oct 2012).

Rick, J.E. (1906) Pilze aus Rio Grande do Sul (Brazilien). Brotéria. Série Botānica 5: 4–53.

Sarnari, M. (1998) Monografia illustrata del Gčnére Russula in Europa. Tomo Primo. AMB, Centro Studi Micologici, Trento, 800 pp.

Schweinitz, L.D. (1822) Synopsis fungorum Carolinae superioris. Schriften der Berlinische Gesellschaft Naturforschender Freunde 1: 20–131.

Singer, R. (1962) The Agaricales in modern taxonomy. Ed. 2. J. Cramer, Weinheim, 915 pp + 75 pl.

Spegazzini, C. (1899, “1898”) Fungi Argentini novi vel critici. Anales del Museo de Historia Natural de Buenos Aires 6: 81–288.

Staněk, V.J. (1956) Hvezdovka Smardova – Geastrum smardae sp. n. Ceskį Mykologie 10(1): 18–23.

Staněk, V.J. (1958) Geastraceae. In: A. Pilįt (ed.) Flora ČSR B1, Gasteromycetes. Praha, pp. 392–526, 777–795.

Sunhede, S. (1986) Notes on the type material of Geastrum congolense. Windahlia 16: 113–122.

Sunhede, S. (1989) Geastraceae (Basidiomycotina). Morphology, ecology and systematics with special emphasis on the North European species. Synopsis Fungorum 1: 1–534.

Suzuki, R. & Shimodaira, H. (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22(12): 1540–1542.

Swofford, D.L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sunderland, Massachusetts: Sinauer Associates.

Tulloss, R.E. & Rodrķguez-Caycedo, C. (2011) Amanita Workshop, 6th edition. New Jersey Mycological Association. Available from (accessed: 07 Feb 2013).

Vittadini, C. (1842) Monographia Lycoperdineorum. Torino, 93 pp.

Whitney, K.D. & Arnott, H.J. (1986) Calcium oxalate crystals and basidiocarp dehiscence in Geastrum saccatum (Gasteromycetes). Mycologia 78(4): 649–656.

Zamora, J.C. & Calonge F.D. (2007) Geastrum parvistriatum, una nueva especie encontrada en Espańa. Boletķn de la Sociedad Micológica de Madrid 31: 139–149.

Zeller, S.M. (1948) Notes on certain Gasteromycetes, including two new orders. Mycologia 40(6): 639–668.


  • There are currently no refbacks.

ISSN 1179-3155 (print); ISSN 1179-3163 (online)

Published by Magnolia Press, Auckland, New Zealand