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Apiosordaria nigeriensis (Ascomycota): a new record for the Americas

Abstract

Apiosordaria is a genus of fungus with species commonly reported inhabiting soil or herbivore feces. However, studies related to the association of representatives of this genus to plants, especially in semi-arid ecosystems, are still non-existent. In this work we documented a new occurrence for Brazil of a species of Apiosordaria, associated with the palm Syagrus coronata. The collections were carried out at the Raso da Catarina Ecological Station and the analyzes were carried out at the Laboratory of Sciences of the Bahia State University, Campus VIII, Paulo Afonso. From the topographic analysis of the plant substrate in stereomicroscope and the evaluation of fungal structures under optical light microscope, the species was identified as Apiosordaria nigeriensis. This fungus was reported for the first time in Enugu, Nigeria, after being isolated from soil samples. In this work, we report the second occurrence of A. nigeriensis to the world, being the first to Brazil, representing the first record for the Americas, and highlighting the palm S. coronata as the first botanical host colonized by the species. These data broaden the knowledge about the geographic distribution of the genus, especially on the microdiversity for the caatinga biome.

Key words:
Caatinga; fungus; Syagrus coronata; taxonomy

Resumo

Apiosordaria é um gênero de fungo com espécies geralmente reportadas habitando o solo ou fezes de herbívoros. No entanto, estudos referentes à associação de representantes deste gênero às plantas, especialmente em ecossistemas semiáridos, ainda são inexistentes. Neste trabalho documentamos uma nova ocorrência para o Brasil de uma espécie de Apiosordaria, associada a palmeira Syagrus coronata. As coletas foram realizadas na Estação Ecológica Raso da Catarina e as análises ocorreram no Laboratório de Ciências, da Universidade do Estado Bahia, Campus VIII, Paulo Afonso. A partir da análise topográfica do substrato vegetal em estereomicroscópio e da avaliação das estruturas fúngicas em microscópio óptico de luz, a espécie foi identificada como Apiosordaria nigeriensis. Este fungo foi relatado pela primeira vez em Enugu, na Nigéria, após de ter sido isolado de amostras de solo. Neste trabalho, reportamos a segunda ocorrência de A. nigeriensis para o mundo, sendo a primeira para o Brasil, representando o primeiro registro para as Américas, e dando destaque a palmeira S. coronata como o primeiro hospedeiro botânico colonizado pela espécie. Estes dados ampliam o conhecimento sobre da distribuição geográfica do gênero, em especial sobre a micodiversidade para o bioma caatinga.

Palavras-chave:
Caatinga; fungos; Syagrus coronata; taxonomia

The genus Apiosordaria is a member of the family Lasiosphaeriaceae (Ascomycota) and was first described by Arx & W. Gams in 1967 (Arx & Gams 1967Arx JA & Gams W (1967) Über Pleurale verruculosa und die zugehorige Cladorrhinum-Konidienform. Nova Hedwigia 13: 199-208.). The species of the hat genus are characterized by having asci dark-brown to black, globose to piriform, ostiolate or not, sometimes having trichomes. The peridio is generally pseudoparenchymatous, membranaceous, or slightly coriaceous, with two or various layers. The asci are unitunicate, with 4 or 8-spores, cylindrical or clavate, stipitate, with ring indistinct or absent, non-amyloid. Paraphyses frequently present, filiform and hyaline when present. Ascospores with 2 cells or occasionally 3, with upper cell blackish, ellipsoidal to subglobose, dark-brown to black, with ornamentation and germinative pore; lower cell triangular to cylindrical, hyaline and smooth (Stchigel et al. 2000Stchigel AM, Cano J, Guarro J & Gugnani HC (2000) A new Apiosordaria from Nigeria, with a key to the soilborne species. Mycologia 92: 1206-1209.).

According to the Index Fungorum online database (2018)Index Fungorum Online Database (2018) Available at <http://www.indexfungorum.org/Names/Names.asp>. Access on 12 February 2018.
http://www.indexfungorum.org/Names/Names...
, there are currently 23 accepted species. Generally encountered in the soil or in the feces of herbivores (Krug et al. 1983Krug JC, Udagawa S & Jeng RS (1983) The genus Apiosordaria. Mycotaxon 17: 533-549.; Guarro et al. 1984Guarro J, Martínez AT & von Arx JA (1984) A new Apiosordaria from soil. Journal, Persoonia - Molecular Phylogeny and Evolution of Fungi 12: 181-184.; Udagawa 1990Udagawa SH (1990) A new species of Apiosordaria and some interesting ascomycetes from Nepal. Cryptogams of the Himalayas (National Science Museum, Tsukuba) 2: 73-84.; Mukerji et al. 1995Mukerji KG, Kumar RN & Singh N (1995) Studies on Indian coprophilous fungi: IV. species of genera Apiosordaria and Cercophora. Phytomorphology 45: 87-105.; Stchigel et al. 2000Stchigel AM, Cano J, Guarro J & Gugnani HC (2000) A new Apiosordaria from Nigeria, with a key to the soilborne species. Mycologia 92: 1206-1209., 2003Stchigel AM, Guarro J & Mac Cormack W (2003) Soil ascomycetes from Spain. XIII. Two new species of Apiosordaria. Mycologia 95: 134-140.). However, studies related to the association of representatives of this group with plant species, especially in semi-arid climate ecosystems, are still non-existent.

Among the vegetables, palm trees have been showing interesting results regarding interactions with fungal species. According to the work carried out by Hyde (1996)Hyde KD (1996) Measuring biodiversity: diversity of microfungi in north Queensland. In: Bolye TJB & Boontawee B (eds.) Measuring and monitoring biodiversity in tropical and temperate forest. Vol. 1. Cifor, Bogor. Pp. 271-286. in Queensland, the palm/fungus ratio of 1:26 species was proposed to provide estimates of diversity, which is higher than the generally accepted ratio of 1:6 for other plants (Hawksworth 1995Hawksworth DL (1995) Presidential address 1990: The fungal dimension of biodiversity magnitude, significance, conservation. Mycological Research 95: 641-655.). Subsequently, the ratio of 1:26 was revised to 1:33, based on the more detailed palm tree study in Australia and Brunei, suggesting that the global estimate of palm-associated fungi may become even larger (Fröhlich & Hyde 1999).

The Brazil is very rich in species of the family Arecaceae Juss., Being the third largest flora of the world in diversity of native palms, with about 38 genera and 511 species (BFG 2018BFG - The Brazil Flora Group (2018) Brazilian Flora 2020: innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 69: 1513-1527.). Among the species of the caatinga biome, the palm tree Syagrus coronata (Martius) Beccari, popularly known as licuri or ouricuri (Kiill 2011Kiill LHP (2011) Caatinga: patrimônio brasileiro ameaçado. Available at <https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/899060>. Access on 31 July 2012.
https://www.infoteca.cnptia.embrapa.br/i...
) stands out. It is an endemic plant of the northeastern semi-arid region, occurring in the states of Bahia, North of Minas Gerais, Sergipe, Alagoas and Pernambuco (Noblick 1986Noblick LR (1986) Palmeiras das caatingas da Bahia e suas potencialidades econômicas. In: Simpósio sobre a caatinga e sua exploração racional. Feira de Santana. Anais. UEFS, Feira de Santana. Pp. 99-115.).

Because of its extreme socioeconomic and ecological importance, licuri has been considered the “life-saving tree” in natural occurrence areas, as it is a palm tree that withstands prolonged droughts and blooms and fruit for a long period of the year, providing resources for the subsistence of the population and animals of these regions (Lorenzi 1992Lorenzi H (1992) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Vol. 1. Plantarum, Nova Odessa. 287p. ; Drumond 2007Drumond MA (2007) Licuri Syagrus coronata (Mart.) Becc. Embrapa Semiárido, Petrolina. Pp. 7-11.). In addition, it is of particular importance for Lear’s Macaw (Anodorhynchus leari), endemic to the Raso Ecoregion of Catarina, since its fruits constitute the main food item for this bird, extremely endangered due to the traffic and the absence of specific native diet (Ramalho 2008Ramalho CI (2008) Estrutura da vegetação e distribuição espacial do licuri (Syagrus coronata (Mart.) Becc.) em dois municípios do centro norte da Bahia, Brasil. Tese de Doutorado. Universidade Federal da Paraíba, Areia. Pp. 30.; Rocha 2009Rocha KMR (2009) Biologia reprodutiva da palmeira licuri (Syagrus coronata (Mart.) Becc.) (Arecaceae) na Ecorregião do Raso da Catarina, Bahia. Dissertação de Mestrado. Universidade Federal Rural de Pernambuco, Recife. 82p. ).

Although it is not among the palm trees included among endangered species, licuri has been exploited indiscriminately by agricultural practices that include fires for the formation of new pastures and sanitary landfills, victimizing several licurizeiros (Siqueira-Filho 2012Siqueira-Filho JA (2012) Flora das caatingas do Rio São Francisco: história natural e conservação. Vol. 1. Andrea Jakobsson Estúdio Editorial, Rio de Janeiro. 552p.). Therefore, the adoption of management techniques and sustainable use, together with biodiversity conservation policies, are fundamental to protect plants such as licuri, which is so significant for the caatinga biome and has a practically unknown associated mycobiota.

Given the information above and the relevance of this question, the objective of this study was to document the first occurrence of A. nigeriensis Stchigel Guarro to the American continent, colonizing the Syagrus coronata palm and increasing the distribution data on the representatives of this genus, providing new information for Brazilian mycological biodiversity.

Study Site

Collections were undertaken on a monthly basis between May/2014 and January/2015 in the Raso da Catarina Ecological Station in Bahia state, Brazil, located between the parallels 09º33’-9º54’S and meridians 38º27’-38º44’W. Samples of entire leaves, bracts, inflorescences, fruits, and sections of the trunk from the aerial portion of Syagrus coronata (locally “licurizeiro”), as well as the leaf litter around it, were harvested to survey their mycota.

Collection, morphological characterization and identification

The botanical material was fragmented using a pruning shears and machete into pieces 10 to 20 cm long to facilitate their handling and transport. The samples were sterilized with 70% alcohol and 2% sodium hypochlorite and then placed in plastic trays whose sides and bottoms were covered with moist paper towels to be held inside humid chambers. The trays were opened every two days and sprayed with distilled water to maintain their humidity. The botanical material was held for seven days at room temperature under a natural light regime to evaluate fungal growth.

The materials were examined under a stereomicroscope and fragments of any fungal structures were removed using a thin needle (the type used for insulin injections) and mounted on slides and stained with lactophenol cotton blue. The fungal structures were observed under a Zeiss Primo Star microscope, photographed using an attached Samsung 8.0 megapixel digital camera, and measured using a 40x micrometric objective lens (using a 2.5x µm correction).

Identifications were made based on fungal morphology and the reproductive structures, consulting the specialized literature (Krug et al. 1983Krug JC, Udagawa S & Jeng RS (1983) The genus Apiosordaria. Mycotaxon 17: 533-549.; Stchigel et al. 2000Stchigel AM, Cano J, Guarro J & Gugnani HC (2000) A new Apiosordaria from Nigeria, with a key to the soilborne species. Mycologia 92: 1206-1209.). The identified specimens were deposited in the Padre Camille Torrend (URM) at the Mycology Department of the Federal University of Pernambuco (UFPE).

Taxonomy

Apiosordaria nigeriensis Stchigel & Guarro, in Stchigel, Cano, Guarro & Gugnani, Mycologia 92(6): 1206 (2000). Fig. 1a-g

Figure 1
a-g. Apiosordaria nigeriensis – a. habit; b. ascomata; c-d. asci; e-g. ascospores. Barras de escala: b. 100 μm; c. 50 μm; d-g. 25 μm.

Asci superficial, solitary or aggregated, translucent, not ostiolate, globose, 250-337.5 × 250-330 µm. Peridio membranaceous, fragile, pseudoparenchymatous, covered by hyphae 2.5-3 µm thick. Asci 92.5-100 × 25-32.5(-40) µm, 8-spores, unitunicate, clavate, pedicelate, with a non-amyloid ring. Paraphyses not observed. Ascospores 35-37.5 × 17.5-18.5 µm, llipsoidal, with germinative pore, 1 transversal septum; upper cell 25-27.5 × 17.5-18.5 µm, hyaline when young, becoming dark brown when mature, spiny, with apex acuminate and base truncate; lower cell 6-7.5 × 6-7 µm, triangular, hyaline, smooth or subtly spiny.

Material examined: BRAZIL. BAHIA: Paulo Afonso, Raso da Catarina Ecological Station (ESEC), on the fruit of S. coronata in the leaf litter, 10.VI.2014, N.G.S. Fortes (URM 91151).

Registered in soil samples (Stchigel et al. 2000Stchigel AM, Cano J, Guarro J & Gugnani HC (2000) A new Apiosordaria from Nigeria, with a key to the soilborne species. Mycologia 92: 1206-1209.) and in Syagrus coronata.

It is distributed in Nigeria and Brazil.

The material examined was morphologically identical to A. nigeriensis, although with slightly smaller asci 250-337.5 µm (vs. 300-600 µm) and asci 92.5-100 × 25-32.5(-40) µm (vs. 160-180 × 29-36 µm). The different sizes of the above-mentioned structures are probably related to the nutritional conditions for isolation used by Stchigel et al. (2000)Stchigel AM, Cano J, Guarro J & Gugnani HC (2000) A new Apiosordaria from Nigeria, with a key to the soilborne species. Mycologia 92: 1206-1209.. The combined characteristics that allowed the identification of that species included: ascomata globose, translucent, not ostiolate; asci clavate; ascospores with germinative pore, spiny, 35-37.5 µm long and 17.5-18.5 µm wide. Additionally, Stchigel et al. (2000) reported that some species of Apiosordaria appear similar in terms of the characteristics of the upper cell of the ascospores of A. nigeriensis, including: Apiosordaria effusa (Morinaga et al.) J.C. Krug, Udagawa & Jeng, Apiosordaria microcarpa Udagawa & T. Muroi, Apiosordaria terrestris (S.C. Jong & E.E. Davis) J.C. Krug, Udagawa & Jeng, Apiosordaria tuberculata J.C. Krug, Udagawa & Jeng, Apiosordaria vermicularis (Morinaga et al.) J.C. Krug, Udagawa & Jeng, and Apiosordaria verruculosa (C.N. Jensen) Arx & W. Gams. Those species differ, however, in terms of the characteristics of their ascomata and asci. Although Brazil presents a great biodiversity in species of the family Arecaceae, research on the micota that colonize the palms in the cerrado biomes, atlantic forest and caatinga are still very scarce, compared to the studies carried out in the Asian countries. new occurrences and several new species. In the caatinga, studies carried out by Santos et al. (2016)Santos MAL, Vitória NS & Bezerra JL (2016) Fungos colonizando palmeiras em áreas de caatinga do sertão da Bahia. Agrotrópica (Itabuna) 28: 37-46. and Vitória et al. (2016)Vitória NS, Santos MAL & Fortes NGS (2016) Comunidade fúngica de Syagrus coronata (Mart.) Becc.: Ascomycota anamórficos e teleomórficos. In: Andrade MJG, Nogueira EMS & Santos CAB (orgs.) Ecologia e biodiversidade do semiárido nordestino. Vol. 1. Botânica. Editora SABEH, Paulo Afonso. Pp. 35-45 registered 28 taxa, distributed in 25 genera, colonizing only the S. coronata palm. Of these records, 7 comprise new occurrences for the state of Bahia and 5 new ones for Brazil. The present work, in addition to reporting the first record of A. nigeriensis to Brazil and the second one of this species to the world, suggests the need for new investigations to increase knowledge about fungi recorded in areas of caatinga, exclusively Brazilian biome. In addition, it reinforces understanding of the relationships between these organisms and plants, which are still poorly understood, and the encouragement of strategies for biodiversity conservation.

The authors thank the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) for financial support; and the Universidade do Estado da Bahia (UNEB) and the Programa de Pós-graduação em Biodiversidade Vegetal (PPGBVeg) for the use of their laboratories and equipment.

References

  • Arx JA & Gams W (1967) Über Pleurale verruculosa und die zugehorige Cladorrhinum-Konidienform. Nova Hedwigia 13: 199-208.
  • BFG - The Brazil Flora Group (2018) Brazilian Flora 2020: innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 69: 1513-1527.
  • Drumond MA (2007) Licuri Syagrus coronata (Mart.) Becc. Embrapa Semiárido, Petrolina. Pp. 7-11.
  • Frohlich J & Hyde KD (1999) Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodiversity and Conservation 8: 977.
  • Guarro J, Martínez AT & von Arx JA (1984) A new Apiosordaria from soil. Journal, Persoonia - Molecular Phylogeny and Evolution of Fungi 12: 181-184.
  • Hawksworth DL (1995) Presidential address 1990: The fungal dimension of biodiversity magnitude, significance, conservation. Mycological Research 95: 641-655.
  • Hyde KD (1996) Measuring biodiversity: diversity of microfungi in north Queensland. In: Bolye TJB & Boontawee B (eds.) Measuring and monitoring biodiversity in tropical and temperate forest. Vol. 1. Cifor, Bogor. Pp. 271-286.
  • Index Fungorum Online Database (2018) Available at <http://www.indexfungorum.org/Names/Names.asp>. Access on 12 February 2018.
    » http://www.indexfungorum.org/Names/Names.asp
  • Kiill LHP (2011) Caatinga: patrimônio brasileiro ameaçado. Available at <https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/899060>. Access on 31 July 2012.
    » https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/899060
  • Krug JC, Udagawa S & Jeng RS (1983) The genus Apiosordaria. Mycotaxon 17: 533-549.
  • Lorenzi H (1992) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Vol. 1. Plantarum, Nova Odessa. 287p.
  • Mukerji KG, Kumar RN & Singh N (1995) Studies on Indian coprophilous fungi: IV. species of genera Apiosordaria and Cercophora. Phytomorphology 45: 87-105.
  • Noblick LR (1986) Palmeiras das caatingas da Bahia e suas potencialidades econômicas. In: Simpósio sobre a caatinga e sua exploração racional. Feira de Santana. Anais. UEFS, Feira de Santana. Pp. 99-115.
  • Ramalho CI (2008) Estrutura da vegetação e distribuição espacial do licuri (Syagrus coronata (Mart.) Becc.) em dois municípios do centro norte da Bahia, Brasil. Tese de Doutorado. Universidade Federal da Paraíba, Areia. Pp. 30.
  • Rocha KMR (2009) Biologia reprodutiva da palmeira licuri (Syagrus coronata (Mart.) Becc.) (Arecaceae) na Ecorregião do Raso da Catarina, Bahia. Dissertação de Mestrado. Universidade Federal Rural de Pernambuco, Recife. 82p.
  • Santos MAL, Vitória NS & Bezerra JL (2016) Fungos colonizando palmeiras em áreas de caatinga do sertão da Bahia. Agrotrópica (Itabuna) 28: 37-46.
  • Siqueira-Filho JA (2012) Flora das caatingas do Rio São Francisco: história natural e conservação. Vol. 1. Andrea Jakobsson Estúdio Editorial, Rio de Janeiro. 552p.
  • Stchigel AM, Cano J, Guarro J & Gugnani HC (2000) A new Apiosordaria from Nigeria, with a key to the soilborne species. Mycologia 92: 1206-1209.
  • Stchigel AM, Guarro J & Mac Cormack W (2003) Soil ascomycetes from Spain. XIII. Two new species of Apiosordaria Mycologia 95: 134-140.
  • Udagawa SH (1990) A new species of Apiosordaria and some interesting ascomycetes from Nepal. Cryptogams of the Himalayas (National Science Museum, Tsukuba) 2: 73-84.
  • Vitória NS, Santos MAL & Fortes NGS (2016) Comunidade fúngica de Syagrus coronata (Mart.) Becc.: Ascomycota anamórficos e teleomórficos. In: Andrade MJG, Nogueira EMS & Santos CAB (orgs.) Ecologia e biodiversidade do semiárido nordestino. Vol. 1. Botânica. Editora SABEH, Paulo Afonso. Pp. 35-45

Edited by

Area Editor: Dr. Mauricio Salazar-Yepes

Publication Dates

  • Publication in this collection
    05 Oct 2020
  • Date of issue
    2020

History

  • Received
    11 Mar 2018
  • Accepted
    13 May 2019
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