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Authentic collections of Myriostoma calongei revealed this species as occurring from Paraíba State, Brazil

Coletas autênticas de Myriostoma calongei revelaram esta espécie como ocorrendo no Estado da Paraíba, Brasil

ABSTRACT

Myriostoma is a gasteroid genus belonging to the order Geastrales, which is distinguished by its basidiomes with multiple columns/pedicels, several ostioles in its endoperidium, and predominantly subglobose basidiospores with ornamentation. Furthermore, members of the genus Myriostoma have been found in Central and South America, Europe and Africa, but are not frequently found in nature. This work aims to report the first sighting of M. calongei from the State of Paraíba, with some insights on its morphology.

Keywords:
description; earthstar fungi; taxonomy

RESUMO

Myriostoma é um gênero gasteroide pertencente à ordem Geastrales, que se distingue por seus basidiomas com múltiplas colunas/pedicelos, vários ostíolos em seu endoperídio e basidiósporos predominantemente subglobosos com ornamentação. Ademais, membros do gênero Myriostoma foram encontrados na América Central e do Sul, Europa e África, mas não são frequentemente encontrados na natureza. Este trabalho tem como objetivo relatar o primeiro avistamento de M. calongei do Estado da Paraíba, com algumas informações sobre sua morfologia.

Palavras-chave:
descrição; fungo estrela-da-terra; taxonomia

Introduction

Myriostoma Desv. is a genus treated similar to Geastrum Pers., but differing in possessing many ostioles and pedicels (Sousa et al. 2017Sousa, J.O., Suz, L.M.; García, M.A., Alfredo, D.S., Conrado, L.M., Marinho, P., Ainsworth, M., Baseia, I.G. & Martín, M.P. 2017. More than one fungus in the pepper pot: Integrative taxonomy unmasks hidden species within Myriostoma coliforme (Geastraceae, Basidiomycota). PloSONE 12(6): e0177873.). After a bibliographic revision, we found that the genus Myriostoma, which was previously described as monospecific one, has been pointed out to be actually composed by five cryptic species: M. areolatum (Calonge & M. Mata) M.P. Martín, J.O. Sousa & Baseia; M. australianum J.O. Sousa, Baseia & M.P. Martín, M. calongei Baseia, J.O. Sousa & M.P. Martín, M. capillisporum (V.J. Staněk) Suz, A.M. Ainsw., Baseia & M.P. Martín, and the putative type species M. anglicum Desv. nom. illeg., a arbitrarily described name for Lycoperdon coliforme Dickks. Myriostoma anglicum is illegitimate (Turland et al. 2018Turland, N.J., Wiersema, J.H., Barrie, F.R., Hawksworth, D.L., Herendeen, P.S., Knapp, S., Husber, W.-H., Li, D.-Z., Marhold, K., May, T.W., McNeill, J., Monro, A.N., Pradom J., Price, M.J. & Smith, G.F. (eds.). 2018. International Code of Nomenclature for Algae, Fungi and Plants (Shenzen Code): Adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Glashütten: Koeltz Scientific Books Art. 52.1) because Desvaux (1809)Desvaux, N.A. 1809. Observations sur quelques genres à établir dans la famille des champignons. Journal de Botanique (Desvaux). 2: 88-105. ignored Dickson (1785)Dickson, J. 1785. Fasciculus plantarum cryptogamicarum Britanniae. 1: 1-26. when he replaced the epithet ‘coliforme’ by ‘anglicum’. Thus, M. coliforme (Dicks.) Corda is the correct name for the species, although the name M. anglicum is the type of the genus.

Thus, field trips revealed specimens of the genus Myriostoma found in Atlantic Forest fragments from Paraíba, and later identified as M. calongei, confirming the occurrence of the species in the State of Paraíba.

Material and methods

Collection of Myriostoma specimens were collected in March and July/2022, in two fragment of Atlantic Forest, in the municipalities of Cabedelo and João Pessoa, Paraíba State, Brazil. The region has a humid tropical Aw climate (Peel et al. 2007Peel, M.C., Finlayson, B.L. & McMahon, T.A. 2007. Updated world map of the Koppen-Geiger climate classification. Hydrology and Earth System Science 11: 1633-1644.). Color code follows Kelly (1965)Kelly, K.L. 1965. Color-Name Charts Illustrated with Centroid Colors. Supplement to NBS Circular 553. Inter-Society Color Council-National Bureu of Standards.. Microscopy was performed after removing pieces of the gleba, endoperidium, and exoperidium, using 4% KOH and Congo red, to rehydrate and stain the sample (da Silva et al. 2014Da Silva B.D.B, Sulzbacher, M.A., Baseia, I.G. 2014. Metodologia. In: I.G. Baseia, B.D.B. da Silva, R.H.S.F. Cruz (eds.). Fungos Gasteroides no Semiárido do Nordeste Brasileiro. Print Mídia Editora, Feira de Santana, pp. 25-28., Sousa et al. 2014Sousa J.O., Morais L.A., Nascimento, Y.M., Baseia, I.G. 2014. Geastraceae. In: I.G. Baseia, B.D.B. da Silva, R.H.S.F. Cruz (eds.). Fungos Gasteroides no Semiárido do Nordeste Brasileiro. Print Mídia Editora, Feira de Santana, pp. 37-55.). Basidiospores shapes are named according to Bas (1969)Bas, C. 1969. Morphology and subdivision of Amanita and a monograph of its section Lepidella. Persoonia 5: 285-579. and statistics are based in 30 measured ones. In addition the sample was respectively observed under optical microscope, using immersion oil for better visualization. The materials are being preserved in the herbarium JPB (Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba).

Results and discussion

Myriostoma calongei Baseia, J.O. Sousa & M.P. Martín, PLoS One 12: 9/19. 2017.

Basidiomata epigeous, expanded, growing solitary or in small group. Exoperidium firm-coriaceous to subcoriaceous; external surface yellowish brown (77. m.y Br) to pale buff (76. l.y Br) near at base/centre, surface dry, squamulose, squamules appressed, dark yellowish brown (75. deep y Br), open into 6-8 rays measuring 27-36 × 20-27 mm (width measured at base), acute to subobtuse terminal region; internal surface beige (72. d. O Y), dull, wrinkled. Endoperidium soft, multipedicelate, 34-43 × 18-20 mm, isodiametric in top view and ellipsoid in side view, silver gray (near 264. l. Gray), surface shiny, wrinkled, multiostiolate, ostioles erupted up to 2-3 mm in diam. Gleba spongy, pulverulent, soft, dark yellowish brown (81. d. gy. y Br). Exoperidium: outer surface, with hyphae 1.40-9.80 μm in diam., wall thickness, 0.4-1.9 μm, yellowish brown; inner surface pseudoparenchymatous, cells 19.5-46 × 16.6-39.2 μm, mostly subisodiametric, colorless, thin-walled. Endoperidium surface with abundant hyphae 1.0-3.9 μm, brown pigmented to slightly paler, slightly thick to thick-walled to 0.4-1.4 μm. Eucapilitium with plentiful hyphae 1.9-4.9 μm, strongly interwoven, brown to yellowish brown pigmented, moderately to thick-walled 0.4-1.4 μm, incrusted with somewhat resinous tuffs. Basidia not seen. Basidiospores 4.9-8.8 × (3.4-)4.4-8.3 μm (measured with ornamentation), av. 6.9 × 6.2 μm, Q = 1.00-1.40 (1.43), av.Q = 1.11, mostly subglobose, but also globose to sometimes broadly ellipsoid occasionally ellipsoid, melleous to yellowish brown, strongly ornamented, ornaments crested 0. 4-1.9 μm high, mostly yellowish.

Habitat: On soil among litter, solitary or in small group of four basidiomata in Atlantic Forest fragments.

Material examined: Brazil, Paraíba, João Pessoa, Bairro da Penha, EMEF Antônio Santos Coelho Neto, in a forest fragment behind the school, 08-III-2022, leg. G. Gomes-Filho s/n FW 01/2022 (JPB 66975); Cabedelo, Floresta Nacional Restinga de Cabedelo, 12-VII-2022, I.S. Miranda & F. Wartchow FW 06/2022 (JPB 66976).

Myriostoma used to be a monospecific genus, but recent phylogenies found five species (Sousa et al. 2017Sousa, J.O., Suz, L.M.; García, M.A., Alfredo, D.S., Conrado, L.M., Marinho, P., Ainsworth, M., Baseia, I.G. & Martín, M.P. 2017. More than one fungus in the pepper pot: Integrative taxonomy unmasks hidden species within Myriostoma coliforme (Geastraceae, Basidiomycota). PloSONE 12(6): e0177873., 2018). Among the known species, M. calongei was described as lacking areolate ostioles in the endoperidium, and the presence of silver-gray endoperidium that seems more verrucose than other species with these warts measuring 0.13±0.28 mm high (Sousa et al. 2017Sousa, J.O., Suz, L.M.; García, M.A., Alfredo, D.S., Conrado, L.M., Marinho, P., Ainsworth, M., Baseia, I.G. & Martín, M.P. 2017. More than one fungus in the pepper pot: Integrative taxonomy unmasks hidden species within Myriostoma coliforme (Geastraceae, Basidiomycota). PloSONE 12(6): e0177873.). Another question that arose here was regarding to basidiospores shape: all specimens of the three additional species analyzed by Sousa et al. (2017)Sousa, J.O., Suz, L.M.; García, M.A., Alfredo, D.S., Conrado, L.M., Marinho, P., Ainsworth, M., Baseia, I.G. & Martín, M.P. 2017. More than one fungus in the pepper pot: Integrative taxonomy unmasks hidden species within Myriostoma coliforme (Geastraceae, Basidiomycota). PloSONE 12(6): e0177873. presented as globose or nearly so, while in M. calongei they found sometimes ranging to ellipsoid (see Bas 1969Bas, C. 1969. Morphology and subdivision of Amanita and a monograph of its section Lepidella. Persoonia 5: 285-579.: 321 for basidiospores shape). Myriostoma coliforme sensu Baseia & Galvão (2002)Baseia, I.G. & Galvão, T.C.O. 2002. Some interesting Gasteromycetes (Basidiomycota) in dry areas of Northeastern Brazil. Acta Botanica Brasilica 16: 1-8. is suspected to be conspecific to M. calongei, but described as having globose basidiospores. However, the drawings depicted by them (p. 4, fig. 6) showed broadly ellipsoid ones (est. Q = 1.25). Thus, we can conclude that the basidiospore’ shape also can be used for segregate M. calongei from the other species.

Myriostoma australianum is also a species that producing basidiospores with a certain variability of basiospores shape, with (6.5-) 7.1-8 × (6.3-) 6.7-8.3 mm [x = 7.9 ± 0.5 × 7.5 ± 0.5, Qm = 1.05, n = 30], but it probably presents a smaller range, according to Sousa et al. (2019)Sousa, J.O., Baseia, I.G. & Martín, M.P. 2019. Strengthening Myriostoma (Geastraceae, Basidiomycota) diversity: Myriostoma australianum sp. nov. Mycoscience 60: 25-30..

Thus, considering the Neotropical distribution of M. calongei, we also propose the use of the basidiospores shapes range as additional feature for species characterization. In addition, we confirm the occurrence of this taxon from urban fragments of Atlantic Forest in Paraíba, Brazil.

Known from Argentina and Brazil, in the States of Goiás, Pernambuco, São Paulo, and Rio Grande do Norte (Sousa et al. 2017Sousa, J.O., Suz, L.M.; García, M.A., Alfredo, D.S., Conrado, L.M., Marinho, P., Ainsworth, M., Baseia, I.G. & Martín, M.P. 2017. More than one fungus in the pepper pot: Integrative taxonomy unmasks hidden species within Myriostoma coliforme (Geastraceae, Basidiomycota). PloSONE 12(6): e0177873., Camilo-Cotrim et al. 2020Camilo-Cotrim, C.F., Leonardo-Silva, L. & Xavier-Santos, S. 2020. First records of Myriostoma calongei Baseia, Sousa & Martin (Geastraceae, Basidiomycota) in central Brazil. Check List 16: 53-57., Trierveiler-Pereira & Gugliotta 2020Trierveiler-Pereira, L. & Gugliotta, A.M. 2020. Primeiro registro do gênero Myriostoma (Geastraceae, Basidiomycota) no Parque Estadual das Fontes do Ipiranga (PEFI), São Paulo, SP, Brasil. Hoehnea 47: e512019.), this work points a new perspective of including the distribution of this gasteroid genus, more specifically the first record of M. calongei in the State of Paraíba, in the cities of Cabedelo and João Pessoa.

Figure 1
Myriostoma calongei Baseia, J.O. Sousa & M.P. Martín. a. Basidiomata. b, c, d. Glebal eucapilitia and basidiospores.

Acknowledgements

The authors wish to acknowledge Dr. Rivete S. Lima, Coordinator of the Laboratório de Anatomia Vegetal, for authorizing the use of the microscope; the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for funding the projects Programa de Pesquisa em Biodiversidade (PPBio Proc. 60/2009), Fungos agaricoides em áreas de Mata Atlântica e Caatinga no Estado da Paraíba (Edital Universal Proc. 420.448/2016-0), for providing a scholarship for GM (Proc. 140541/2018-7), and Produtividade em Pesquisa’ (Proc. 307922/2014-6, Proc. 307947/2017-3 and Proc. 309652/2020-0), grants for Felipe Wartchow. The experiments performed here comply with the current Brazilian laws.

Literature cited

  • Bas, C. 1969. Morphology and subdivision of Amanita and a monograph of its section Lepidella Persoonia 5: 285-579.
  • Baseia, I.G. & Galvão, T.C.O. 2002. Some interesting Gasteromycetes (Basidiomycota) in dry areas of Northeastern Brazil. Acta Botanica Brasilica 16: 1-8.
  • Camilo-Cotrim, C.F., Leonardo-Silva, L. & Xavier-Santos, S. 2020. First records of Myriostoma calongei Baseia, Sousa & Martin (Geastraceae, Basidiomycota) in central Brazil. Check List 16: 53-57.
  • Desvaux, N.A. 1809. Observations sur quelques genres à établir dans la famille des champignons. Journal de Botanique (Desvaux). 2: 88-105.
  • Dickson, J. 1785. Fasciculus plantarum cryptogamicarum Britanniae. 1: 1-26.
  • Da Silva B.D.B, Sulzbacher, M.A., Baseia, I.G. 2014. Metodologia. In: I.G. Baseia, B.D.B. da Silva, R.H.S.F. Cruz (eds.). Fungos Gasteroides no Semiárido do Nordeste Brasileiro. Print Mídia Editora, Feira de Santana, pp. 25-28.
  • Kelly, K.L. 1965. Color-Name Charts Illustrated with Centroid Colors. Supplement to NBS Circular 553. Inter-Society Color Council-National Bureu of Standards.
  • Peel, M.C., Finlayson, B.L. & McMahon, T.A. 2007. Updated world map of the Koppen-Geiger climate classification. Hydrology and Earth System Science 11: 1633-1644.
  • Sousa J.O., Morais L.A., Nascimento, Y.M., Baseia, I.G. 2014. Geastraceae. In: I.G. Baseia, B.D.B. da Silva, R.H.S.F. Cruz (eds.). Fungos Gasteroides no Semiárido do Nordeste Brasileiro. Print Mídia Editora, Feira de Santana, pp. 37-55.
  • Sousa, J.O., Suz, L.M.; García, M.A., Alfredo, D.S., Conrado, L.M., Marinho, P., Ainsworth, M., Baseia, I.G. & Martín, M.P. 2017. More than one fungus in the pepper pot: Integrative taxonomy unmasks hidden species within Myriostoma coliforme (Geastraceae, Basidiomycota). PloSONE 12(6): e0177873.
  • Sousa, J.O., Baseia, I.G. & Martín, M.P. 2019. Strengthening Myriostoma (Geastraceae, Basidiomycota) diversity: Myriostoma australianum sp. nov. Mycoscience 60: 25-30.
  • Trierveiler-Pereira, L. & Gugliotta, A.M. 2020. Primeiro registro do gênero Myriostoma (Geastraceae, Basidiomycota) no Parque Estadual das Fontes do Ipiranga (PEFI), São Paulo, SP, Brasil. Hoehnea 47: e512019.
  • Turland, N.J., Wiersema, J.H., Barrie, F.R., Hawksworth, D.L., Herendeen, P.S., Knapp, S., Husber, W.-H., Li, D.-Z., Marhold, K., May, T.W., McNeill, J., Monro, A.N., Pradom J., Price, M.J. & Smith, G.F. (eds.). 2018. International Code of Nomenclature for Algae, Fungi and Plants (Shenzen Code): Adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Glashütten: Koeltz Scientific Books
Associate Editor: Elaine Malosso

Publication Dates

  • Publication in this collection
    01 Mar 2024
  • Date of issue
    2024

History

  • Received
    10 Mar 2023
  • Accepted
    17 Nov 2023
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