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Lycophytes of the Chapada das Mesas National Park, Cerrado, Maranhão, Brazil

Licófitas do Parque Nacional Chapada das Mesas, Cerrado Maranhense, Brasil

Abstract:

Despite an increase in studies involving lycophytes and ferns in recent years, Maranhão is still one of the northeastern states with a poorly known flora, mainly due to low sampling. For Chapada das Mesas National Park, a protected conservation unit in the Cerrado maranhense with phytophysiognomies that favor floristic diversity, there are no floristic studies about lycophytes. This study aimed to conduct the floristic inventory and taxonomic study of lycophytes in Chapada das Mesas National Park. Three collection expeditions, of three days each, were made between March 2017 and June 2018. Three families of lycophytes represented by three genera and six species were identified in the study area. The most diverse family was Selaginellaceae with four species: Selaginella conduplicata, S. erythropus (Mart.) Spring, S. radiata (Aubl.) Baker and S. simplex Baker. The other two families, Isoëtaceae and Lycopodiaceae, had one species each, Isoëtes sp. and Palhinhaea cernua (L.) Franco & Vasc. This study also reports two new record for the Brazilian Cerrado phytogeographic domain, S. conduplicate and S. radiata, of which the first is a new record for Maranhão State. Most specimens were found in riparian forest on rocky outcrops.

Keywords:
Riparian forest; Selaginella; Taxonomy; Waterfall

Resumo:

Embora as pesquisas envolvendo o estudo de licófitas e samambaias tenham crescido nos últimos anos, o Maranhão ainda é um dos Estados do Nordeste com sua flora menos conhecida em virtude, principalmente, da baixa amostragem. O Parque Nacional (PARNA) Chapada das Mesas, apesar de tratar-se de uma unidade de conservação protegida no Cerrado maranhense e abrigar fitofisionomias que são propícias à diversidade florística, ainda não possui estudos sobre a diversidade florística de licófitas. Este estudo teve como objetivo geral fazer um inventário e estudo florístico e taxonômico de licófitas para o PARNA Chapada das Mesas. Foram realizadas três expedições para coletas de material entre março 2017 e junho 2018 com duração de três dias cada. Na área de estudo foram identificadas as três famílias de licófitas representadas por três gêneros e seis espécies. A família com maior diversidade foi Selaginellaceae com quatro espécies Selaginella conduplicata, S. erythropus, S. radiata e S. simplex. As outras duas, Isoëtaceae e Lycopodiaceae com uma espécie cada, Isoëtes sp., e Palhinhaea cernua. Nesse estudo também são relatados dois novos registros para o domínio fitogeográfico do Cerrado, S. conduplicata e S. radiata, sendo a primeira um novo registro para o Estado do Maranhão. A maioria dos espécimes foi encontrada em ambientes de matas ciliares crescendo sobre afloramento rochoso.

Palavras-chave:
Mata ciliar; Selaginella; Taxonomia; Cachoeira

Introduction

The class Lycopodiopsida, also known as lycophytes, is a monophyletic group characterized by its main leaves that are microphylls, sporangia with transversal dehiscence in the adaxial axil of the sporophyll and, in most cases, strobili forming at the branch apex (Tryon & Tryon 1982TRYON, R.M. & TRYON, A.F. 1982. Ferns and allied plants with special reference to Tropical America. Springer - Verlag, New York, p.857., Banks 2009BANKS, J.A. 2009. Selaginella and 400 million years of separation. Annu. Ver. Plant Biol. 60: 223-238., PPG I 2016PPG I. The Pteridophyte Phylogeny Group. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54 (6): 563-603.). Among vascular plants, it is considered the most basal group (Pryer et al. 2001PRYER, K.M., SCHNEIDER, H., SMITH, A.R., CRANFILL, R., WOLF, P.G., HUNT, J.S. & SIPES, S.D. 2001. Horsetails and Ferns are a Monophyletic Group and the Closest Living Relatives to Seed Plants. Nature 409: 618-622.), with the first fossil records dating to the Paleozoic era, approximately 350-410 million years ago (Kenrick & Crane 1997KENRICK, P. & CRANE, P.R. 1997. The origin and early diversification of land plants. Smithsonian Institution Press, Washington.).

Lycophytes are herbaceous and can be terrestrial, epiphytic, rupicolous or aquatic (Prado & Sylvestre 2010PRADO, J. & SYLVESTRE, L.S. 2010. Introdução: as samambaias e licófitas do Brasil. In Catálogo de plantas e fungos do Brasil (R.C. Forzza, org). Andrea Jakobsson Estúdio: Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, Rio de Janeiro, p.69-74.). They are widely distributed in many ecosystems of tropical, subtropical, temperate and boreal regions, which demonstrates their great adaptive success (Moran & Smith 2001MORAN, R.C. & SMITH, A.R. 2001. Phytogeographic relationships between and African-Madagascar pteridophytes. Brittonia 53(2): 304-351.). According to Kenrick & Crane (1997)KENRICK, P. & CRANE, P.R. 1997. The origin and early diversification of land plants. Smithsonian Institution Press, Washington., the extant representatives of lycophytes belong to three families, Lycopodiaceae, Isoëtaceae and Selaginellaceae, of which the first is homosporous and the last two are heterosporous.

Lycopodiaceae species are distributed on practically all continents, especially in the neotropical region (Øllgaard 1995AØLLGAARD, B. 1995A. Lycopodiaceae. In Flora Mesoamericana. Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). Universidade Nacional Autónoma de México, Ciudad de México, v.1, p.5-22.). According to the classification by Øllgaard (2012)ØLLGAARD, B. 2012. Nomenclatural changes in Brazilian Lycopodiaceae. Rodriguésia 63: 479-482., the family is divided into 16 genera and represented by terrestrial, epiphytic and rupicolous plants. These taxa are highly diverse in South America, exhibiting a variety of life forms, and are found in various habitats (Arana & Øllgaard 2012ARANA, M. & ØLLGAARD, B. 2012. Revisión de las Lycopodiaceae (Embryopsida, Lycopodiidae) de Argentina y Uruguay. Darwiniana. 50(1/2): 266-295., Arana et al. 2017ARANA, M.D., GONZALEZ, H.A., BONIFACINO, M. & BRUSSA, C.A. 2017. A Revision of Lycopodiaceae from Uruguay. Int. J. Adv. Res. 3(4): 24-39.).

The family Isoëtaceae is monogeneric (Isoëtes), is distributed worldwide and comprises approximately 250 species and comprises plants that are usually submersed or emergent, including some that are seasonal with active growth during spring (Jermy 1990JERMY, A.C. 1990. Selaginellaceae. In The families and genera of vascular plants (K.U. Kramer & P.S. Green, eds). Springer Verlag, Berlin, p.39-45., Moran 2012MORAN, R.C. 2012. A Natural History of Ferns. Timber Press, Portland., Troia et al. 2016TROIA, A., PEREIRA, J.B.S., KIM, C., TAYLOR, W.C. 2016. The genus Isoetes (Isoetaceae): A provisional checklist of the accepted and unresolved taxa. Phytotaxa 277(2): 101-145. https://doi.org/10.11646/phytotaxa.277.2.1.
https://doi.org/10.11646/phytotaxa.277.2...
). Due to their morphological simplicity (Taylor & Hickey 1992TAYLOR, W. & HICKEY, R. 1992. Habitat, Evolution, and Speciation in Isoëtes. Ann. Mo. Bot. Gard. 79(3): 613-622.), reproductive structures, such as megaspore and microspore ornamentation (Pfeiffer 1922PFEIFFER, N.E. 1922. Monografia das Isoëtaceae. Ann. Mo. Bot. Gard. 9(2): 79., Hickey 1986HICKEY, R.J. 1986. Morfologia da superfície de isóteos megaspore: variação da nomenclatura e importância sistemática. Am. Fern. J. 76: 1-16., Musselman 2002MUSSELMAN, L.J. 2002. Ornamentation of Isoëtes (Isoëtaceae, Lycophyta) microspores. Bot. Rev. 68: 474.), as well as anatomical and leaf morphology diagnostic characters, are important in the classification of the species (Rolleri & Prada 2007ROLLERI, C., & PRADA, C. 2007. Caracteres diagnósticos foliares en Isoëtes (Pteridophyta, Isoetaceae). Ann. Mo. Bot. Gard. 94(1): 202-235.).

The family Selaginellaceae is also represented by one genus, Selaginella, which is cosmopolitan and widely adapted, mainly in the tropics (Moran 2012MORAN, R.C. 2012. A Natural History of Ferns. Timber Press, Portland., Tryon & Stolze 1994TRYON, R.M. & STOLZE, R.G. 1994. 22. Marsileaceae - 28. Isoëtaceae. In Pteridophyta of Peru. Fieldiana Bot. v. 32, Part 6. p.1-190). The genus is characterized by high intraspecific variability, as well as reduced interspecific variation (Schulz et al. 2013SCHULZ, C., HOMBERG, J. & STÜTZEL, T. 2013. Taxonomic revision of Selaginella subg. Ericetorum. Syst. Bot. 38: 5-14.).

Lycophytes comprise approximately 1,338 species (PPG I 2016PPG I. The Pteridophyte Phylogeny Group. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54 (6): 563-603.) and represent only 1% of vascular plants (Moran 2008MORAN, R.C., 2008. Diversity, biogeography, and floristics. In Biology and evolution of ferns and lycophytes (T.A. Ranker & C.H. Haufler, eds). Cambridge University Press, New York, p.367-394.). In Brazil, there are 186 lycophyte species, of which 49 have been recorded in the Northeast Region, a relatively low number compared to the other regions of the country, except the Central-West region where there are only 38 species. The others Brazilian regions are better sampled, with 83 in the North, 95 in the Southeast, and 64 in the South (Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br/ (último acesso em 28 Out 2019).
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, under construction).

Although it is one of the largest states in the Northeast Region, Maranhão is still undersampled. Local floristic studies about seedless vascular plants contain few species and have recorded only eleven species of lycophytes (e.g., Bastos & Cutrim 1999BASTOS, C.C.C. & CUTRIM, M.V.J. 1999. Pteridoflora da Reserva florestal do Sacavém, São Luis - Maranhão. Bol. Mus. Para. Emílio Goeldi, sér. Botânica 15(1): 3-37., Fernandes et al. 2007FERNANDES, R.S., CONCEIÇÃO, G.M., BRITO E.S. & PAULA-ZÁRATE, E.L. 2007. Diversidade Florística de Pteridófitas da Área de Preservação Ambiental do Inhamum, Caxias, Maranhão, Brasil. Rev. bras. Bioci, 5(2): 411-413., Fernandes et al. 2010FERNANDES, R.S., CONCEICÃO, G.M., COSTA J.M. & PAULA-ZÁRATE, E.L. 2010. Samambaias e licófitas do município de Caxias, Maranhão, Brasil. Bol. Mus. Emílio Goeldi. Ciênc. Nat. (3): 345-356., Conceição & Rodrigues 2010CONCEIÇÃO, G.M. & RODRIGUES, M.S. 2010. Pteridófitas do Parque Estadual do Mirador, Maranhão, Brasil. Cad. Geociênc. (7): 47-53., Silva et al. 2017SILVA, G.S., SILVA, D.L.S., OLIVEIRA, R.R., SILVA, M.L.A. & CONCEIÇÃO, G.M. 2017. Licófitas e Samambaias no Cerrado do Leste do Maranhão, Brasil. Acta Bra. 1(2): 13-16., Santos-Silva et al. 2018SANTOS-SILVA, D.L., SILVA, G.S., OLIVEIRA, R.R. & CONCEIÇÃO, G.M. 2018. Nova ocorrência de Lycopodiaceae (lycophyta) para o Estado do Maranhão: Pseudolycopodiella carnosa (Silveira) Holub. Biota Amazônia 8(2): 58-59, Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br/ (último acesso em 28 Out 2019).
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, under construction). Maranhão State is situated in an ecotone area between the Amazon and Brazilian Cerrado phytogeographic domain and acts as an ecological corridor (called the Araguaia-Bananal) that connects these areas, as well as the Caatinga and coastal environment (ICMbio 2019ICMBIO. http://www.icmbio.gov.br (último acesso em 12 Agost. 2019).
http://www.icmbio.gov.br ...
). The Brazilian Cerrado phytogeographic domain it has high floristic diversity, including a third of the biodiversity in Brazil and around 5% in the world (Klink & Machado 2005KLINK, C. A. & MACHADO, R.B. 2005. A Conservação do Cerrado Brasileiro. Megadiversidade 1(1): 148-155.).

The protected area Chapada das Mesas National Park, created under the decree of 12 December 2005 (BRASIL 2005BRASIL. 2005. Decreto de 12 de Dezembro de 2005 http://www.planalto.gov.br/ccivil_03/_Ato2004-2006/2005/Dnn/Dnn10718.htm (último acesso em 28 Out 2019).
http://www.planalto.gov.br/ccivil_03/_At...
), mainly has phytophysiognomic features of Brazilian Cerrado, including large formations of grassland and savanna, as well as natural ecosystems of high ecological and socio-environmental value (ICMbio 2019ICMBIO. http://www.icmbio.gov.br (último acesso em 12 Agost. 2019).
http://www.icmbio.gov.br ...
). Despite being established over a decade ago and its ecological relevance, there are few published works about the plant biodiversity that support the creation of a management plan for the area (Oliveira et al. 2018, Silva et al. 2018SILVA JUNIOR, C.H.L., ANDERSON, L.O.E.I.N, ARAGÃO, L.E.O.C. & RODRIGUES, B.D. 2018. Dinâmica das Queimadas no Cerrado do Estado do Maranhão, Nordeste do Brasil. Rev. Dep. Geogr. 35: 1-14.).

The phytogeographic domain in Maranhão State are under an accelerated process of destruction (Bolfe et al. 2016BOLFE, É.L., VICTÓRIA, D.C., CONTINI, E., BAYMA-SILVA, G., SPINELLI-ARAUJO, L. & GOMES, D. 2016. Matopiba em crescimento agrícola aspectos territoriais e socioeconômicos. Rev. Polít. Agríc. 25(4): 38-62., Silva Junior et al. 2018SILVA JUNIOR, C.H.L., ANDERSON, L.O.E.I.N, ARAGÃO, L.E.O.C. & RODRIGUES, B.D. 2018. Dinâmica das Queimadas no Cerrado do Estado do Maranhão, Nordeste do Brasil. Rev. Dep. Geogr. 35: 1-14.) and studying the floristic diversity of the state is important since it is poorly sampled (Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br/ (último acesso em 28 Out 2019).
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, under construction).

Thus, the objective of the present study was to inventory and provide a taxonomic treatment of the lycophyte species in Chapada das Mesas National Park, Maranhão State, Brazil.

Material and Methods

1. Study area

The study area, Chapada das Mesas National Park, comprises approximately 160,000 ha of Cerrado divided into two polygons, one with around 120,000 ha and another with about 40,000 ha, distributed in the municipalities of Carolina, Riachão and Estreito in southeastern Maranhão State (ICMbio 2019ICMBIO. http://www.icmbio.gov.br (último acesso em 12 Agost. 2019).
http://www.icmbio.gov.br ...
).

The climate is predominantly seasonal tropical, type Aw (Köppen 1948KÖPPEN, W. 1948. Climatologia: con un estudio de los climas de la tierra. Fundo de Cultura Economica, México, p.478.), with a dry season for 3 to 5 months and a rainy season with average rainfall ranging from 1,250 to 1,500 mm, an average annual temperature between 20ºC and 27ºC and average relative air humidity of approximately 60% (Pereira et al. 2011PEREIRA, B.A.S., VENTUROLI, F. & CARVALHO, F.A. 2011. Florestas Estacionais no Cerrado: Uma Visão Geral. Pesq. Agropec. Trop. 41(3): 446-455.).

Hydrologically, the area is very rich. The main water courses are the Farinha River (norther portion) and Itapecuru River (southern portion), there are over 400 springs in the interior, and along the courses there are well-conserved gallery forests (ICMBio 2019ICMBIO. http://www.icmbio.gov.br (último acesso em 12 Agost. 2019).
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).

The relief is characterized by the presence of sandstone and typical forms of paleokarst in sandstone (e.g., hilltop arches, small cavities, canyons, paleosinkholes, sinkholes and river resurgences), which is closely related to the evolution of the subterranean drainage and river incision (Martins et al. 2017MARTINS, F.P., SALGADO, A.A.R. & BARRETO, H.N. 2017. Morfogênese da Chapada das Mesas (Maranhão Tocantins): paisagem cárstica e poligenética. Rev. Bras. Geomorfol. 18(3): 623-635.). The soil is predominantly sandy, where there are the Brazilian Cerrado sensu stricto and campo sujo physiognomies. However, there are also places with richer soils, mainly on the tops of mountains that have patches of semideciduous forest (ICMBio 2019ICMBIO. http://www.icmbio.gov.br (último acesso em 12 Agost. 2019).
http://www.icmbio.gov.br ...
).

In addition to the natural vegetation cover typical of the Brazilian Cerrado phytogeographic domain that contains many phytophysiognomies, among which savanna and forest aspects are notable, there are also Caatinga and Amazonian species, which help characterize the high diversity of the area (ICMBio 2019ICMBIO. http://www.icmbio.gov.br (último acesso em 12 Agost. 2019).
http://www.icmbio.gov.br ...
). These vegetation characteristics, including the presence of well-conserved gallery forests along water courses, large patches of cerradão and other types of phytophysiognomies, are essential for maintaining the biodiversity in the region (Marques 2012MARQUES, A.R. 2012. Saberes geográficos integrados aos estudos territoriais sob a ótica da implantação do Parque Nacional da Chapada das Mesas, sertão de Carolina - MA. Tese de doutorado. Universidade Estadual Paulista, Presidente Prudente.).

2. Data collection

Samples of lycophytes were collected in Chapada das Mesas National Park and the surrounding area under permit number 50167-4 issued by the Sistema de Autorização e Informação em Biodiversidade do Instituto Chico Mendes de Conservação da Biodiversidade- Sisbio/ICMBio.

The species were collected during three expeditions, in March and October 2017, and June 2018, which were three days each and included the dry and rainy seasons. Collecting was based on the methods proposed by Filgueiras et al. (1994)FILGUEIRAS, T.S., NOGUEIRA, P.E., BROCHADO, A.L., & GUALA, G.F., 1994. Caminhamento: um método expedito para levantamentos florísticos qualitativos. Cad. Geociênc. 12(1): 39-43.. Microenvironments in the study area were selected and explored randomly, with the goal of visiting the greatest number of microenvironments where taxa might occur. The sampling points were mapped (Figure 1).

Figure 1
Collecting sites in the Chapada das Mesas National Park, Maranhão State, Brazil.

Herbarium specimens were made base on standard techniques used for seedless vascular plants (Silva 1989SILVA, A.T., 1989. Pteridófitas. In Técnicas de coleta, preservação e herborização de material botânico (O. Fidalgo & V.L.R. Bononi, Eds). Instituto de Botânica, São Paulo p. 32-34., Windisch 1992WINDISCH, P.G. 1992. Pteridófitas da Região Norte-Ocidental do Estado de São Paulo: guia para excursões. 2 ed. Universidade Estadual Paulista, São José do Rio Preto, p.110.). All the material was deposited in the herbarium CCAA (RBH 2019RBH. https://www.botanica.org.br/catalogo-da-rede-brasileira-de-herbarios/ (último acesso em 27 Set 2019).
https://www.botanica.org.br/catalogo-da-...
), at the Federal University of Maranhão, Campus Chapadinha. When available, duplicates were sent to the following institutions: MG, HBRA and BHCB (Thiers 2019THIERS, B. 2019. [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/ (último acesso em 05 Agost 2019)
http://sweetgum.nybg.org/science/ih/...
).

The identification and distribution of the species and genera were based on specialized literature, such as Alston et al. (1981)ALSTON A.H.G., JERMY A.C. & RANKIN J.M. 1981. The genus Selaginella in tropical South America. Bull. Brit. Mus. (Nat. Hist.) Bot. 9: 233-330., Fraile et al. (1995)FRAILE, M.E., SOMERS, P. & MORAN, R.C. 1995. Selaginella. In Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). In Flora Mesoamericana (G. Davidse, M.S. Sousa & S. Knapp, eds.). Universidad Nacional Autónoma de México, Ciudad de México, v.1, p.22-42., Øllgaard (1995 AØLLGAARD, B. 1995A. Lycopodiaceae. In Flora Mesoamericana. Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). Universidade Nacional Autónoma de México, Ciudad de México, v.1, p.5-22., BØLLGAARD, B. 1995B. Lycopodiaceae. In Flora of the Venezuelan Guayana, 2. Pteridophytes, Spermatophytes: Acanthaceae-Araceae (P.E. Berry, B.K. Holst & K. Yatskievych , eds). Timber Press, Portland, p.190-206.), Smith (1995)SMITH, A.R. 1995. Selaginellaceae. In Flora of the Venezuelan Guayana 2. Pteridophytes, Spermatophytes: Acanthaceae-Araceae (P.E. Berry, B.K. Holst & K. Yatskievych , eds). Timber Press, Portland, p.296-314., Hirai & Prado (2000)HIRAI R.Y. & PRADO, J. 2000. Selaginellaceae Willk. no Estado de São Paulo, Brasil. Rev. bras. Bot. 23(3): 313-339., Góes-Neto et al. (2016)GÓES-NETO, L.A.A., PALLOS, J. & SALINO, A. 2016. Flora das cangas da Serra dos Carajás, Pará, Brasil: Selaginellaceae. Rodriguésia 67(5) (Especial): 1177-1180., Heringer et al. (2016)HERINGER G., VALDESPINO I.A. & SALINO, A. 2016 Selaginella P. Beauv. from Minas Gerais, Brazil. Acta Bot. Bras. 30(1): 60-77., Øllgaard & Windisch (2016)ØLLGAARD, B. & WINDISCH P.G. 2016. Lycopodiaceae no Brasil. Conspectus da família II. Os gêneros Lycopodiella, Palhinhaea, e Pseudolycopodiella. Rodriguésia 67 (3): 691-719., Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br/ (último acesso em 28 Out 2019).
http://floradobrasil.jbrj.gov.br/...
(under construction), as well as revisions and neotropical floras (e.g., Tryon & Stolze 1994TRYON, R.M. & STOLZE, R.G. 1994. 22. Marsileaceae - 28. Isoëtaceae. In Pteridophyta of Peru. Fieldiana Bot. v. 32, Part 6. p.1-190, Moran & Riba 1995MORAN, R.C & RIBA, R. 1995. Flora Mesoamericana. Psilotaceae a Salviniaceae. Universidade Nacional Autônoma do México, México, v.1, p.470., Mickel & Smith 2004MICKEL, J.T. & SMITH, A.R. 2004. The Pteridophytes of Mexico. Memoirs of the New York Botanical Garden 88: 1-1054.). When needed, some species were sent to specialists to confirm the identification. The morphological study, inspection and descriptions were based only on examined material (see results).

The terminology follows Lellinger (2002)LELLINGER, D.B. 2002. A modern multilingual glossary for taxonomic pteridology. American Fern Society, Washington, p.263.. Family and genus delimitations are based on PPG I (2016)PPG I. The Pteridophyte Phylogeny Group. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54 (6): 563-603.. Nomenclature and authors of the species follow the International Plant Names Index (IPNI 2019) and Tropicos (2019)TROPICOS. http://www.tropicos.org/Name/26616606 (último acesso em 01 Out 2019)
http://www.tropicos.org/Name/26616606 ...
.

Results

1. Diversity

Six species of lycophytes were recorded in Chapada das Mesas National Park, including three families and three genera: Selaginellaceae with 4 species, Selaginella conduplicata Spring, S. erythropus (Mart.) Spring, S. radiata (Aubl.) Baker and S. simplex Baker; Isoëtaceae, Isoëtes sp.; and Lycopodiaceae, Palhinaea cernuna (L.) Franco & Vasc.

2. Identification key to the lycophyte species in Chapada das Mesas National Park

  • 1. Plant homosporous; microphylls arranged in alternate whorls, not ligulate, acicular; lateral branches patent; strobili pendent at the apex of branches………………………........................................................................................................................…………….......Palhinhaea cernua

  • 1’. Plant heterosporous; microphylls arranged in four rows or forming a rosette, ligulate, linear, lanceolate, ovate-lanceolate to ovate-elliptic; lateral branches not patent; strobili absent or erect at the apex of branches.......................................................................................................................................2

  • 2. Microphylls linear, 9.5–21.5 cm long, with four air chambers in transversal section, deposited in the form of a rosette on a corm stem type; sporangia fused in the base of the sporophyll..............................................................................................................................................Isoëtes sp.

  • 2’. Microphylls not linear (< 1 cm long), without air chambers in transversal section, arranged in four rows on aerial and prostrate branches; sporangia not fused, in strobili at the apex of branches..............................................................................................................................................................3

  • 3. Stem articulate; lateral microphylls with two denticulate auricles; base of dorsal microphylls with an auricle on the outer side; axillary microphylls with two dentate auricles with sparsely denticulate margin…………………………………………………………...........Selaginella conduplicata

  • 3’. Stem not articulate; lateral microphylls without auricles; base of dorsal microphylls without auricles, rounded to slightly cuneate; axillary microphylls without auricles, truncate, rounded or sometimes subcordate, margin ciliate to serrate, rarely entire ……………….............…….....4

  • 4. Base of stem reddish; dorsal microphylls with ciliate margin; axillary microphylls with acuminate to attenuate apex........................................................................................................................................................................................................................................Selaginella erythropus

  • 4’. Base of stem stramineous; dorsal microphylls with denticulate-eciliate margin; axillary microphylls with acute apex......................................5

  • 5. Lateral microphylls with ciliate margin on the basal acroscopic side; dorsal microphylls with strongly aristate apex; axillary microphylls with ciliate margin at the base................................................................................................................................................................Selaginella radiata

  • 5’. Lateral microphylls with denticulate margin on the basal acroscopic side; dorsal microphylls with acuminate to long-acuminate apex; axillary microphylls with sparsely serrate-eciliate margin……………………...…………………..……………………………....………...Selaginella simplex

3. Taxonomic treatment, distribution and comments

Palhinhaea Franco & Vasc., Bol. Soc. Brot., sér. 2, 41: 24. 1967.

The genus is represented by 25 species (PPG I 2016PPG I. The Pteridophyte Phylogeny Group. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54 (6): 563-603.). In Brazil, there are six species, which occur in all five regions politic and in the Amazon, Brazilian Cerrado, Atlantic Forest, Pampa and Pantanal phytogeographic domain. Of these, two species have been recorded in the Northeast Region and one in Maranhão.

1. Palhinhaea cernua (L.) Franco & Vasc., Bol. Soc. Brot., sér. 2, 41: 25. 1967. (Figure 2F)

Figure 2
Habitat of the lycophytes in Chapada das Mesas National Park. A. Selaginella conduplicata. B. Selaginella erythropus. C. Selaginella radiata. D. Selaginella simplex. E. Isoëtes sp. F. Palhinhaea cernua.

Plant terrestrial or rupicolous, 47.5-187 cm long. Stem erect to long-scandent, flagelliform at the apex, stoloniferous, greenish to stramineous, glabrous; lateral branches dichotomously branched, lateral branches patent; terminal branches 4-5 mm wide (including microphylls); sterile microphylls isophyllous, microphylls arranged in alternate whorls, 3-4 mm long, acicular, gradually changing on the main axis from reflexed to patent, curved in the direction of the apex, apex cuneate, base decurrent, margin entire, glabrous or with sparse trichomes; strobili 3-20 × 1-2 mm, pendent at the apex of lateral branches; sporophylls 1.5-2 mm long, ovate-deltoid, apex long-cuspidate to acuminate, base coalescent, margin erose to laciniate; not ligulate; plant homosporous.

  • Specimens examined: BRAZIL, MARANHÃO, PARNA Chapada das Mesas, Carolina, Cachoeira da Ponta da Serra, Riacho Lages, 6º58’47,4” S, 47º22’25” W, 235 m, 11 de March de 2017, L.R. Silva & M.R. Pietrobom 31 (CCAA807); idem, L.R. Silva & M.R. Pietrobom78 (CCAA806); idem, Riacho Corrente, 7º04’25,6” S, 47º05’26,6” W, 284 m, 13 de March de 2017, F.C. Almeida et al. 71 (CCAA854); idem, 7º04’25,0” S, 47º05’26,2” W, 277 m, 7 de June de 2018, F.C. Almeida et al. 75 (CCAA855).

  • Distribution: The species has a Pantropical distribution (Øllgaard & Windisch 2016ØLLGAARD, B. & WINDISCH P.G. 2016. Lycopodiaceae no Brasil. Conspectus da família II. Os gêneros Lycopodiella, Palhinhaea, e Pseudolycopodiella. Rodriguésia 67 (3): 691-719.) and occurs in Asia, Africa, the Antilles, Belize, Bolivia, Brazil, Cameroon, Costa Rica, Colombia, El Salvador, United States of America, Ecuador, Guatemala, Guinea, Honduras, Madagascar, Mexico, Nicaragua, Oceania, Paraguay, Peru, Suriname, Trinidad, and Venezuela (Øllgaard 1995BØLLGAARD, B. 1995B. Lycopodiaceae. In Flora of the Venezuelan Guayana, 2. Pteridophytes, Spermatophytes: Acanthaceae-Araceae (P.E. Berry, B.K. Holst & K. Yatskievych , eds). Timber Press, Portland, p.190-206.). In Brazil, it is widely distributed and occurs in all of the regions: North (Amazonas, Amapá, Pará, Rondônia, Roraima, Tocantins); Northeast (Alagoas, Bahia, Ceará, Maranhão, Paraíba, Pernambuco); Central-West (Distrito Federal, Goiás, Mato Grosso do Sul, Mato Grosso); Southeast (Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo); and South (Paraná, Rio Grande do Sul, Santa Catarina).

  • Comments:Palhinhaea cernua is characterized by its dichotomously branched, patent lateral branches and pendent strobili. The strobili have been described as being 4-20 mm long and 2.5-3 mm wide (Øllgaard 1995AØLLGAARD, B. 1995A. Lycopodiaceae. In Flora Mesoamericana. Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). Universidade Nacional Autónoma de México, Ciudad de México, v.1, p.5-22., Øllgaard & Windisch 2016ØLLGAARD, B. & WINDISCH P.G. 2016. Lycopodiaceae no Brasil. Conspectus da família II. Os gêneros Lycopodiella, Palhinhaea, e Pseudolycopodiella. Rodriguésia 67 (3): 691-719.); however, in the samples examined from Chapada das Mesas National Park variations starting at 3 mm long and 1-2 mm wide were recorded.

The most similar species to P. cernua that also occurs in the Northeast Region is P. camporum (B. Øllg. & P.G. Windisch) Holub, since it has an erect, branched stem and pendent strobili. However, P. cernua has recurved distal branches and a more flexible stem, while P. camporum has non-recurved distal branches and a rigid stem (Øllgaard & Windisch 2016ØLLGAARD, B. & WINDISCH P.G. 2016. Lycopodiaceae no Brasil. Conspectus da família II. Os gêneros Lycopodiella, Palhinhaea, e Pseudolycopodiella. Rodriguésia 67 (3): 691-719.).

In the study area, P. cernua was collected in an open environment, with a lot of or little sun, on soil and rock near a stream and waterfall.

Isoëtes L., Sp. Pl. 2: 1100. 1753.

The genus is represented by around 250 species (PPG I 2016PPG I. The Pteridophyte Phylogeny Group. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54 (6): 563-603.). In Brazil, 28 species have been recorded, which are distributed in the five regions in the Amazon, Brazilian Cerrado, Altantic Forest, Pampa and Pantanal phytogeographic domain. From these 28 species, three have been recorded for the Northeast Region, Isoëtes gigantea U. Weber, I. luetzelburgii U. Weber, I. panamensis Maxon & C. V. Morton, the latter one also for Maranhão.

1. Isoëtes sp.

(Figure 2E)

Plant amphibious, 10.2-22.3 cm long. Stem globose, corm type, 2-3 lobate; microphylls imbricate, forming a rosette, with four air chambers in transversal section, deposited in the form of a rosette, 9.5-21.5 cm long, linear, erect, laminated, subula distal and with wings restricted to the proximal portion, septum with stellate, greenish cells; strobili absent; sporangia fused in the base of the sporophyll; megaspores trilete, distal and proximal surfaces baculate, whitish; plant heterosporous.

  • Specimens examined: BRAZIL, MARANHÃO, PARNA Chapada das Mesas, Carolina, Cachoeira do Prata, Rio Farinha, 6º59’36,9” S, 47º9’58,5” W, 198 m, 12 March 2017, L.R. Silva & M.R. Pietrobom 45 (CCAA808).

  • Comments: The material collected of Isoëtes is sterile, but 4 or 5 megaspores were found loose in the substrate near the stem. Thus, even by a specialist, it is not possible to determine the species (personal communication by Dr. Jovani Bernardino de Sousa Pereira) since the taxonomy of the group is mainly based on reproductive structures, such as sporangia and spores (Hickey 1986HICKEY, R.J. 1986. Morfologia da superfície de isóteos megaspore: variação da nomenclatura e importância sistemática. Am. Fern. J. 76: 1-16.). The specimen analyzed is similar to Isoëtespanamensis Maxon & C.V.Mort in microphyll and megaspore characters, such as the presence of hyaline wings on the proximal portion of the microphyll, triquetrous subula and baculate surface of the megaspore. However, additional collections are needed to confirm the species.

In the study area, it was collected in an open, sunny environment near a waterfall, growing as an amphibious plant where there is seasonal flooding.

Selaginella P. Beauv. Mag. Encycl. 9(5): 478. 1804.

The genus is represented by around 700 species (PPG I 2016PPG I. The Pteridophyte Phylogeny Group. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54 (6): 563-603.). In Brazil, 96 species have been recorded, which are distributed in the five regions of the country and in the Amazon, Caatinga, Brazilian Cerrado, Atlantic Forest and Pantanal phytogeographic domain. Of these, 22 species are cited for the Northeast region and four are cited for Maranhão.

1. Selaginella conduplicata Spring, Fl. Bras. 1(2): 129. 1840.

(Figures 2A; 3A-C)

Figure 3
A-C. Selaginella conduplicata (F.C. Almeida et al. 03 (CCAA852)). A. Lateral microphyll. B. Dorsal microphyll. C. Axillary microphyll. D-F. Selaginella erythropus (L.R. Silva & M.R. Pietrobom 39 (CCAA819)). D. Lateral microphyll. E. Dorsal microphyll. F. Axillary microphyll.

Plant terrestrial or rupicolous, 10-130 mm long. Stem articulate, 2-4(-5)-pinnate, not flagelliform, repent to erect, not stoloniferous, stramineous at the base, glabrous, distal branches 3-4(-5) mm wide (including microphyll); dorsal rhizophores throughout the extension of the decumbent stem, stramineous; microphylls not overlapping before the first bifurcation, heterophyllous; microphylls not linear, without air chambers in transversal section, microphylls arranged in four rows on aerial and prostrate branches; lateral microphylls arranged in two rows, 2-3(-4) mm long, lanceolate, ascending, apex acute, base with two denticulate auricles, smaller auricle on the external acroscopic margin widely denticulate, whitish, basioscopic margin entire to rarely widely denticulate in the direction of the apex, basioscopically greenish; dorsal microphylls arranged in two rows, 1-2.5(-3) mm long, ovate-lanceolate, asymmetric, apex long-acute to acuminate, base with one denticulate auricle on the external side, margin sparsely denticulate, whitish; axillary microphylls 1.5-2.5 mm long, lanceolate, apex acute, base with two long, dentate auricles, margin sparsely denticulate, whitish; strobili erect at the apex of branches, 3-15 mm long; sporangia not fused, in strobili at the apex of branches; megasporophylls 1(2), at the base of the strobilus; megaspores white; plant heterosporous.

  • Specimens examined: BRAZIL, MARANHÃO, PARNA Chapada das Mesas, Carolina, Cachoeira do Prata, Rio Farinha, 6º59’36,9” S, 47º9’58,5” W, 198 m, 12 March 2017, L.R. Silva & M.R. Pietrobom 40 (CCAA820); idem, L.R. Silva & M.R. Pietrobom 43 (CCAA814); idem, 6º59’37,4” S, 47º09’58,0” W, 194 m, 29 October 2017, L.R. Silva & F.C. Almeida 84 (CCAA826); idem, 6º59’37” S, 47º09’57” W, 197 m, 6 June 2018, F.C. Almeida et al. 03 (CCAA852); idem, 6º59’36,7” S, 47º9’53,1” W, 210 m, F.C. Almeida et al. 29 (CCAA853).

  • Distribution: This species has a South American distribution, including Brazil, Guyana, French Guiana, Suriname, Colombia, and Peru (Alston et al. 1981ALSTON A.H.G., JERMY A.C. & RANKIN J.M. 1981. The genus Selaginella in tropical South America. Bull. Brit. Mus. (Nat. Hist.) Bot. 9: 233-330., Smith 1995SMITH, A.R. 1995. Selaginellaceae. In Flora of the Venezuelan Guayana 2. Pteridophytes, Spermatophytes: Acanthaceae-Araceae (P.E. Berry, B.K. Holst & K. Yatskievych , eds). Timber Press, Portland, p.296-314.). In Brazil, it is cited for the North (Acre, Amapá, Amazonas, Pará, Roraima), Northeast (Ceará, Pernambuco), and Central-West (Mato Grosso) regions (Paula-Zárate 2005PAULA-ZÁRATE, E.L. 2005. Florística e fitogeografia das pteridófitas do Estado do Ceará, Brasil. Tese de doutorado, Universidade de São Paulo, São Paulo., Silva 2014SILVA, I.A.A. 2014. Composição e riqueza de samambaias e licófitas em florestas serranas do Nordeste do Brasil: influência de fatores físicos e conservação. Tese de doutorado. Universidade Federal de Pernambuco, Recife.). This is the first record of Selaginella conduplicata for the Brazilian Cerrado and the state of Maranhão.

  • Comments:Selaginella conduplicata differs from the other species collected in the study area by its articulate stem, microphylls with auricles, and presence of one megasporangium (rarely two) on the strobili.

In the study area, it was collected near a waterfall, in an open to partially shaded environment, and was rupicolous or sometimes terrestrial.

2. Selaginella erythropus (Mart.) Spring, Fl. Bras. 1(2): 125. 1840.

(Figures 2B; 3D-F)

Plant terrestrial or rupicolous, 15-170 mm long. Stem not articulate, 2-3-pinnate, flagelliform, erect, stoloniferous, reddish at the base, glabrous, distal branches 1.5-2 mm wide (including microphylls); ventral rhizophores present on the lower half of the erect stem, reddish; microphylls overlapping before the first bifurcation, isophyllous at the base, heterophyllous above the first bifurcation; microphylls not linear, without air chambers in transversal section, microphylls arranged in four rows on aerial branches; lateral microphylls arranged in two rows, 1.8-2 mm long, lanceolate to ovate-lanceolate, slightly falcate, slightly ascending at the apex, apex acuminate to attenuate, base truncate, slightly rounded acroscopically, not auriculate, acroscopic and basioscopic margins ciliate to serrate, rarely entire, slightly hyaline; dorsal microphylls arranged in two rows, 1-1.5 mm long, ovate-lanceolate, symmetric, apex long-aristate to long-acuminate, base rounded, margin ciliate to long-dentate, hyaline to slightly hyaline; axillary microphylls (1.2-)1.8-2 mm long, similar to lateral microphylls, apex acuminate, base rounded or sometimes slightly truncate on the acroscopic or basioscopic side, not auriculate, margin ciliate to denticulate, serrate toward the apex, greenish; strobili erect at the apex of branches, (1-)2-5(-6) mm long; sporangia not fused, in strobili at the apex of branches; megasporophylls ventral, throughout the extension of the strobilus; megaspores white; plant heterosporous.

  • Specimens examined: BRAZIL, MARANHÃO, PARNA Chapada das Mesas, Carolina, Cachoeira do Prata, Rio Farinha, 6º59’36,9” S, 47º9’58,5” W, 198 m, 12 March 2017, L.R. Silva & M.R. Pietrobom 39 (CCAA819); idem, 6º59’41,3” S, 47º09’57,4” W, 213 m, L.R. Silva & M.R. Pietrobom 37 (CCAA818); idem, 6º59’37,4” S, 47º09’58,0” W, 194 m, 29 October 2017, L.R. Silva & F.C. Almeida 90 (CCAA823); idem, L.R. Silva & F.C. Almeida 91 (CCAA825); idem, 6º59’37,3” S, 47º09’58,0” W, L.R. Silva & F.C. Almeida 100 (CCAA824); idem, 6º59’37” S, 47º09’57” W, 197 m, 6 June 2018, F.C. Almeida et al. 08 (CCAA851); F.C. Almeida et al. 09 (CCAA859); F.C. Almeida et al. 14 (CCAA846); idem, Cachoeira São Romão, 7º01’15,4” S, 47º02’28,2” W, 241 m, 31 October 2017, L.R. Silva & F.C. Almeida 183 (CCAA822); idem, 7º01’17,1” S, 47º02’27,1” W, 256 m, 7 June 2018, F.C. Almeida et al. 65 (CCAA847); idem, Cachoeira Ponta da Serra, Riacho Lages, 6º58’47,4” S, 47º22’25” W, 235 m, 11 March 2017, L.R. Silva & M.R. Pietrobom 24 (CCAA817); idem, L.R. Silva & M.R. Pietrobom 29 (CCAA816); idem, Estreito, Cachoeira do Prata, Rio Farinha, 6º59’36,7” S, 47º9’53,1” W, 210 m, 6 June 2018, F.C. Almeida et al. 26 (CCAA849); idem, F.C. Almeida et al. 28 (CCAA848).

  • Distribution: This species has a neotropical distribution, including Costa Rica, Colombia, Ecuador, Peru, Bolivia, and Brazil (Fraile et al. 1995FRAILE, M.E., SOMERS, P. & MORAN, R.C. 1995. Selaginella. In Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). In Flora Mesoamericana (G. Davidse, M.S. Sousa & S. Knapp, eds.). Universidad Nacional Autónoma de México, Ciudad de México, v.1, p.22-42.). For Brazil, it is cited for the North (Pará, Tocantins, according to Góes-Neto 2016GÓES-NETO, L.A.A. 2016. Estudos taxonômicos em Selaginellaceae Willk. (Lycopodiophyta) no Brasil. Tese de doutorado. Universidade Federal de Minas Gerais. Belo Horizonte.), Northeast (Bahia, Ceará, Maranhão, Paraíba, Piauí, Rio Grande do Norte), Central-West (Distrito Federal, Goiás, Mato Grosso, Mato Grosso do Sul) and Southeast (Minas Gerais, Rio de Janeiro) regions.

  • Comments: The main characteristics of Selaginella erythropus are the reddish stem and overlapping microphylls before the first bifurcation (Fraile et al. 1995FRAILE, M.E., SOMERS, P. & MORAN, R.C. 1995. Selaginella. In Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). In Flora Mesoamericana (G. Davidse, M.S. Sousa & S. Knapp, eds.). Universidad Nacional Autónoma de México, Ciudad de México, v.1, p.22-42.). Among the material analyzed, on some specimens there was a stolon emerging at the apex of the branches; however, according to Fraile et al. (1995)FRAILE, M.E., SOMERS, P. & MORAN, R.C. 1995. Selaginella. In Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). In Flora Mesoamericana (G. Davidse, M.S. Sousa & S. Knapp, eds.). Universidad Nacional Autónoma de México, Ciudad de México, v.1, p.22-42., the stolons of S.erythropus are restricted to the base of the branches.

In the study area, this species was collected near a waterfall and margin of a river, in an open or sometimes partially shaded environment, mostly as a rupicolous plant.

3. Selaginella radiata (Aubl.) Spring, Bull. Acad. Roy. Sci. Bruxelles 10: 143, no. 54. 1843.

(Figures 2C; 4A-C)

Figure 4
A-C. Selaginella radiata (L.R. Silva & M.R. Pietrobom 47 (CCAA809)). A. Lateral microphyll. B. Dorsal microphyll. C. Axillary microphyll. D-F. Selaginella simplex (F.C. Almeida et al. 25 (CCAA845)). D. Lateral microphyll. E. Dorsal microphyll. F. Axillary microphyll.

Plant terrestrial or rupicolous, 15-205 mm long. Stem not articulate, 2-3-pinnate, not flagelliform, erect, stoloniferous, stramineous, glabrous, distal branches 3-10 mm wide (including microphylls); rhizophores abaxial, only at the base of the main stem, stramineous; microphylls not overlapping before the first bifurcation, anisophyllous; microphylls not linear, without air chambers in transversal section, microphylls arranged in four rows on aerial branches; lateral microphylls arranged in two rows, (1.2-)2-2.8 mm long, ovate-lanceolate, ascending, apex acute, base cordate, not auriculate, basal acroscopic margin strongly ciliate and serrate toward the apex, basioscopic margin slightly serrate, greenish; dorsal microphylls arranged in two rows, (1-)1.5-2 mm long, ovate-elliptic, asymmetric, apex strongly aristate, base slightly cuneate, margin denticulate, denticles larger at the base on the acroscopic side, hyaline; axillary microphylls (1.3-)1.5-2(-2.1) mm long, lanceolate, apex acute, base truncate, not auriculate, margin ciliate in the proximal region and slightly serrate toward the apex, hyaline at the base and greenish toward the apex; strobili erect at the apex of branches, 2-6 mm long; sporangia not fused, in strobili at the apex of branches; megasporophylls 2(-4), at the base of the strobilus; megaspores whitish; plant heterosporous.

  • Specimens examined: BRAZIL, MARANHÃO, PARNA Chapada das Mesas, Estreito, Cachoeira do Prata, Rio Farinha, 6º59’36,7” S, 47º9’53,1” W, 210 m, 12 March 2017, L.R. Silva & M.R. Pietrobom 47 (CCAA809); idem, Carolina, Cachoeira São Romão, 7º1’17,2” S, 47º2’27,8” W, 258 m, 13 March 2017, L.R. Silva & M.R. Pietrobom 55 (CCAA815); idem, L.R. Silva & M.R. Pietrobom 59 (CCAA811); idem Cachoeira São Romão, Rio Farinhas, 7º01’17,1” S, 47º02’27,1” W, 256 m, 7 June 2018, F.C. Almeida et al. 47 (CCAA839); idem, Cachoeira Ponta da Serra, Rio Lages, 6º58’47,4” S, 47º22’25” W, 235 m, 11 March 2017, L.R. Silva & M.R. Pietrobom 22 (CCAA810); idem, 6º58’47,1” S, 47º22’25,5” W, 238 m, 8 June 2018, F.C. Almeida et al. 114 (CCAA840); idem, Pousada Mansinha, riacho da Mansinha, 7º07’36,5” S, 47º25’18,2” W, 286 m, 8 June 2018 F.C. Almeida et al. 120 (CCAA842); idem, F.C. Almeida et al. 126 (CCAA841).

  • Distribution: This species is distributed in South America, including Brazil, Bolivia, Colombia, Ecuador, Guyana, French Guiana, Peru, Suriname and Venezuela (Alston et al. 1981ALSTON A.H.G., JERMY A.C. & RANKIN J.M. 1981. The genus Selaginella in tropical South America. Bull. Brit. Mus. (Nat. Hist.) Bot. 9: 233-330.). In Brazil, it has been recorded in the North (Amapá, Amazonas, Pará, Rondônia), Northeast (Bahia, Maranhão, Piauí), and Central-West (Mato Grosso) regions (Góes-Neto et al. 2016GÓES-NETO, L.A.A., PALLOS, J. & SALINO, A. 2016. Flora das cangas da Serra dos Carajás, Pará, Brasil: Selaginellaceae. Rodriguésia 67(5) (Especial): 1177-1180.). This is the first record of Selaginella radiata for the Brazilian Cerrado.

  • Comments: Selaginella radiata is characterized by the base of the lateral and axillary microphylls strongly ciliate, as well as strongly aristate dorsal microphylls. Selaginella decomposita Spring is similar to S. radiata because of the non-articulate stem, non-auriculate microphylls and aristate dorsal microphylls. However, S. decomposita differs from S. radiata by the denticulate lateral and axillary microphyll bases and acuminate to slightly aristate dorsal microphylls (Hirai & Prado 2000HIRAI R.Y. & PRADO, J. 2000. Selaginellaceae Willk. no Estado de São Paulo, Brasil. Rev. bras. Bot. 23(3): 313-339., Heringer et al. 2016HERINGER G., VALDESPINO I.A. & SALINO, A. 2016 Selaginella P. Beauv. from Minas Gerais, Brazil. Acta Bot. Bras. 30(1): 60-77.).

In the study area, S. radiata was collected near a waterfall and source of streams, in an open environment and less often in the shade, as a rupicolous and rarely terrestrial plant on sandy slopes.

4. Selaginella simplex Baker,J. Bot. 23: 293, no. 304. 1885.

(Figures 2D; 4D-F)

Plant terrestrial or rupicolous, 10-28 mm long. Stem not articulate, 1-2 pinnate, not flagelliform, suberect, not stoloniferous, stramineous, glabrous, distal branches 1.8-2 mm wide (including microphylls); rhizophores adaxial, restricted to the basal part of the stem, stramineous; microphylls not overlapping before the first bifurcation, heterophyllous; microphylls not linear, without air chambers in transversal section, microphylls arranged in four rows on aerial branches; lateral microphylls arranged in two rows, 1.2-2 mm long, ovate to ovate-elliptic, ascending, apex acute, base rounded, not auriculate, acroscopic margin denticulate at the base and serrate toward the apex, greenish, basioscopic margin serrate on the apical half; dorsal microphylls arranged in two rows, 1-1.2 mm long, ovate-lanceolate to ovate-elliptic, asymmetric, apex acuminate to long-acuminate, base rounded to slightly cuneate, margin denticulate, greenish; axillary microphylls 1.2-2 mm long, ovate-elliptic, apex acute, base rounded to subcordate, not auriculate, margin sparsely serrate, greenish; strobili erect at the apex of branches, (2-)3-10(-13) mm long; megasporophylls numerous, ventral at the base of the strobilus; sporangia not fused, in strobili at the apex of branches; megaspores yellow; plant heterosporous.

  • Specimens examined: BRAZIL, MARANHÃO, PARNA Chapada das Mesas, Estreito, Cachoeira do Prata, Rio Farinha, ca. 6º59’36,7” S, 47º9’53,1” W, 210 m, 6 June 2018, F.C. Almeida et al. 25 (CCAA845); idem, F.C. Almeida et al. 27 (CCAA843); idem, F.C. Almeida et al. 30 (CCAA844); idem, 12 March 2017, L.R. Silva & M.R. Pietrobom 46 (CCAA813); idem, L.R. Silva & M.R. Pietrobom 48 (CCAA812); idem, Carolina, Cachoeira São Romão, 7º1’17,2” S, 47º2’27,8” W, 258 m, 13 March 2017, L.R. Silva & M.R. Pietrobom 58 (CCAA821).

  • Distribution: This species has a neotropical distribution, including Brazil, Bolivia, Costa Rica, Mexico, Trinidad and Tobago, and Venezuela (Alston et al. 1981ALSTON A.H.G., JERMY A.C. & RANKIN J.M. 1981. The genus Selaginella in tropical South America. Bull. Brit. Mus. (Nat. Hist.) Bot. 9: 233-330., Fraile et al. 1995FRAILE, M.E., SOMERS, P. & MORAN, R.C. 1995. Selaginella. In Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). In Flora Mesoamericana (G. Davidse, M.S. Sousa & S. Knapp, eds.). Universidad Nacional Autónoma de México, Ciudad de México, v.1, p.22-42.). In Brazil, it occurs in the North (Pará, Tocantins), Northeast (Bahia, Ceará, Maranhão Piauí, Pernambuco, Sergipe), and Central-West (Goiás, Mato Grosso) regions (Góes-Neto et al. 2016GÓES-NETO, L.A.A., PALLOS, J. & SALINO, A. 2016. Flora das cangas da Serra dos Carajás, Pará, Brasil: Selaginellaceae. Rodriguésia 67(5) (Especial): 1177-1180.).

  • Comments:Selaginella simplex is similar to S. minima because of the lateral microphylls with a rounded base and acute apex. However, it has greenish microphyll margins, dorsal microphylls with a rounded to slightly cuneate base and a yellow megaspore, while S. minima has hyaline microphyll margins, dorsal microphylls with an auricle on the external side and a white megaspore (Fraile et al. 1995FRAILE, M.E., SOMERS, P. & MORAN, R.C. 1995. Selaginella. In Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). In Flora Mesoamericana (G. Davidse, M.S. Sousa & S. Knapp, eds.). Universidad Nacional Autónoma de México, Ciudad de México, v.1, p.22-42.). Both Selaginella simplex and S. minima Baker are neotropical, but S. minima occurs in Argentina, Guyana, French Guiana, Honduras, Nicaragua and Panama, where S. simplex has not been recorded. In Brazil, both species occur in the North and Central-West regions, while only S. simplex occurs in the Northeast Region (Alston et al. 1981ALSTON A.H.G., JERMY A.C. & RANKIN J.M. 1981. The genus Selaginella in tropical South America. Bull. Brit. Mus. (Nat. Hist.) Bot. 9: 233-330., Fraile et al. 1995FRAILE, M.E., SOMERS, P. & MORAN, R.C. 1995. Selaginella. In Psilotaceae a Salviniaceae (R.C. Moran & R. Riba, eds). In Flora Mesoamericana (G. Davidse, M.S. Sousa & S. Knapp, eds.). Universidad Nacional Autónoma de México, Ciudad de México, v.1, p.22-42., Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br/ (último acesso em 28 Out 2019).
    http://floradobrasil.jbrj.gov.br/...
    , under construction).

In the study area, S. simplex was collected as a rupicolous plant, both in open and shaded environments. Some individuals grow with leafy liverworts.

Discussion

This inventory has around 22% of the species recorded for the Brazilian Cerrado (Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br/ (último acesso em 28 Out 2019).
http://floradobrasil.jbrj.gov.br/...
under construction). The diversity of lycophytes listed in this work (six species) is greater in number of families and species than recorded by Bastos & Cutrim (1999)BASTOS, C.C.C. & CUTRIM, M.V.J. 1999. Pteridoflora da Reserva florestal do Sacavém, São Luis - Maranhão. Bol. Mus. Para. Emílio Goeldi, sér. Botânica 15(1): 3-37., Fernandes et al. (2010)FERNANDES, R.S., CONCEICÃO, G.M., COSTA J.M. & PAULA-ZÁRATE, E.L. 2010. Samambaias e licófitas do município de Caxias, Maranhão, Brasil. Bol. Mus. Emílio Goeldi. Ciênc. Nat. (3): 345-356., Conceição & Rodrigues (2010)CONCEIÇÃO, G.M. & RODRIGUES, M.S. 2010. Pteridófitas do Parque Estadual do Mirador, Maranhão, Brasil. Cad. Geociênc. (7): 47-53., Silva et al. (2017)SILVA, G.S., SILVA, D.L.S., OLIVEIRA, R.R., SILVA, M.L.A. & CONCEIÇÃO, G.M. 2017. Licófitas e Samambaias no Cerrado do Leste do Maranhão, Brasil. Acta Bra. 1(2): 13-16. Santos-Silva et al. (2018)SANTOS-SILVA, D.L., SILVA, G.S., OLIVEIRA, R.R. & CONCEIÇÃO, G.M. 2018. Nova ocorrência de Lycopodiaceae (lycophyta) para o Estado do Maranhão: Pseudolycopodiella carnosa (Silveira) Holub. Biota Amazônia 8(2): 58-59, which cite between one or three species, in the Lycopodiaceae and Selaginellaceae. The other published studies conducted in the Maranhão state did not record lycophytes (e.g. Fernandes et al. 2007FERNANDES, R.S., CONCEICÃO, G.M., COSTA J.M. & PAULA-ZÁRATE, E.L. 2010. Samambaias e licófitas do município de Caxias, Maranhão, Brasil. Bol. Mus. Emílio Goeldi. Ciênc. Nat. (3): 345-356., Conceição & Ruggieri 2010CONCEIÇÃO, G.M. & RUGGIERI, A.C. 2010. Pteridófitas do município de Tufilândia, Estado do Maranhão, Brasil. Pesquisa em Foco 18(1): 59-68., Conceição et al. 2015CONCEIÇÃO, G.M., PAULA-ZARATE, E.L., RUGGIERI, A.C., SILVA, E.O. & SILVA, M.F. 2015. Pteridoflora e seus aspectos ecológicos no município de Timon, Maranhão, Brasil. Braz. Geogr. J. 6(1): 74-81., Santos-Silva et al. 2019).

This study reports an increase in the distribution of two species in the Brazilian Cerrado, S. conduplicata and S. radiata of which the first species is a new record for Maranhão State. Starting in 2015, there has been an increase in the number of studies about the Brazilian Cerrado, which has resulted in an increase in the number of lycophyte and fern species known for the phytogeographic domain (see BGF 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(4): 1513-1527.). However, the known diversity for Maranhão State is still low. It is thought that the diversity of the state is greater than estimated, since it is a transition area between phytogeographic domain (mainly the Brazilian Cerrado and Amazon). Thus, there should be more and systematic sampling of the environments in this region.

Most of the species cataloged in this study are widely distributed in nearly all phytogeographic domain, such as Palhinhaea cernua (Amazon, Brazilian Cerrado , Atlantic Forest, as well as mangrove ecosystems), Selaginella erythropus (Caatinga, Brazilian Cerrado, Atlantic Forest,), S. simplex (Amazon, Caatinga, Brazilian Cerrado) (Bastos & Cutrim 1999BASTOS, C.C.C. & CUTRIM, M.V.J. 1999. Pteridoflora da Reserva florestal do Sacavém, São Luis - Maranhão. Bol. Mus. Para. Emílio Goeldi, sér. Botânica 15(1): 3-37., Azevedo & Silva 2001AZEVEDO, A.C.G. & SILVA, W.M. 2001. Ocorrência de Lycopodiella cernua (L.) Pic. Serm. (Pteridophyta: Lycopodiopsida: Lycopodiaceae) nas bordas de manguezal, São Luís - Maranhão - Brasil. Bol. Lab. Hidrobiol. 14(1): 111-114., Pietrobom & Barros 2003PIETROBOM M.R. & BARROS I.C.L. 2003. Pteridófitas de um fragmento florestal na Serra do Mascarenhas, Estado de Pernambuco, Brasil. Insula 32: 73-118., Fernandes et al. 2007FERNANDES, R.S., CONCEIÇÃO, G.M., BRITO E.S. & PAULA-ZÁRATE, E.L. 2007. Diversidade Florística de Pteridófitas da Área de Preservação Ambiental do Inhamum, Caxias, Maranhão, Brasil. Rev. bras. Bioci, 5(2): 411-413., Maciel et al. 2007MACIEL, S., SOUZA, M.G.C. & PIETROBOM, M.R. 2007. Licófitas e monilófitas do Bosque Rodrigues Alves Jardim Botânico da Amazônia, município de Belém, estado do Pará, Brasil. Bol. Mus. Para. Emílio Goeldi. Ciências Naturais 2(2): 69-83., Conceição & Rodrigues 2010CONCEIÇÃO, G.M. & RODRIGUES, M.S. 2010. Pteridófitas do Parque Estadual do Mirador, Maranhão, Brasil. Cad. Geociênc. (7): 47-53., Fernandes et al. 2010FERNANDES, R.S., CONCEICÃO, G.M., COSTA J.M. & PAULA-ZÁRATE, E.L. 2010. Samambaias e licófitas do município de Caxias, Maranhão, Brasil. Bol. Mus. Emílio Goeldi. Ciênc. Nat. (3): 345-356., Prado & Sylvestre 2010PRADO, J. & SYLVESTRE, L.S. 2010. Introdução: as samambaias e licófitas do Brasil. In Catálogo de plantas e fungos do Brasil (R.C. Forzza, org). Andrea Jakobsson Estúdio: Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, Rio de Janeiro, p.69-74., Barros 2013BARROS, S.C.A. 2013. Similaridade e composição das samambaias e licófitas em fragmentos de floresta atlântica no nordeste do Brasil. Dissertação de mestrado, Universidade Estadual da Paraíba, Campina Grande., Santiago et al. 2014SANTIAGO, A.C.P., SOUSA, M.A., SANTANA, E.S. & BARROS, I.C.L. 2014. Samambaias e licófitas da Mata do Buraquinho, Paraíba, Brasil. Biotemas 27(2): 9-18., Farias et al. 2017FARIAS, R., SILVA, I., PEREIRA, A.F, SANTIAGO, A. & BARROS, I. 2017. Inventário de samambaias e licófitas da RPPN Pedra D’Antas, Pernambuco, nordeste do Brasil. Biota Neotrop. 17(4): e20170364. http://dx.doi.org/10.1590/1676-0611-BN-2017-0364
http://dx.doi.org/10.1590/1676-0611-BN-2...
, Prado & Sylvestre 2010PRADO, J. & SYLVESTRE, L.S. 2010. Introdução: as samambaias e licófitas do Brasil. In Catálogo de plantas e fungos do Brasil (R.C. Forzza, org). Andrea Jakobsson Estúdio: Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, Rio de Janeiro, p.69-74., Silvestre et al. 2019SILVESTRE L.C., MENDONÇA, J.D.L., XAVIER, S.R.S. & JADIM, J.G. 2019. Riqueza e similaridade florística de samambaias e licófitas na Floresta Atlântica no Nordeste do Brasil. Oecol. Aust. 23(3): 480-495.). The exception is S. conduplicata that, until now, was cited to Amazonia and Atlantic Forest in Northeastern (Ceará e Pernambuco) (Silva 2014SILVA, I.A.A. 2014. Composição e riqueza de samambaias e licófitas em florestas serranas do Nordeste do Brasil: influência de fatores físicos e conservação. Tese de doutorado. Universidade Federal de Pernambuco, Recife.). However, in this study it was collected in Brazilian Cerrado.

In the study area, the phytophysiognomy with the greatest diversity of species was riparian forest. According to Lehn et al. (2018)LEHN, C.R., ASSIS, E.L.M.D & SALINO, A. 2018. Check-list das samambaias e licófitas do estado de Mato Grosso do Sul, Brasil. Iheringia, Sér. Bot. 73:255-263., this environment is typical of the Brazilian Cerrado phytogeographic domain and favors the establishment of these species. According to Silvestre (2018)SILVESTRE, L.C. 2018. Samambaias e Licófitas: florística e aspectos biogeográficos na Floresta Atlântica no Nordeste do Brasil. Tese de doutorado, Universidade Federal do Rio Grande do Norte, Natal., independent areas of humid forest, characteristic of transition areas, are points of species exchange, which is corroborated by the distribution of lycophytes and ferns in the region.

The Brazilian Cerrado in the Northeast Region contains ecotones, which is reflected in the floristic diversity of these areas (Walter 2006WALTER B.M.T. 2006. Fitofisionomias do bioma Cerrado: síntese terminológica e relações florísticas. Tese de doutorado, Universidade de Brasília, Brasília.) that exhibit heterogeneous vegetation, such as gallery forest or riparian forest, and rocky outcrop vegetation (Eiten 1994EITEN, G. 1994. Duas travessias na vegetação do Maranhão. UNB, Brasília, p.76.). In a study of the vascular flora by Mendonça et al. (2008)MENDONÇA, R.C., FELFILI, J.M., WALTER, B.M.T., SILVA JÚNIOR, M.C., REZENDE, A.V., FILGUEIRAS, T.S., NOGUEIRA, P.E. & FAGG, C.W. 2008. Flora vascular do cerrado: Chechlist com 12.356 espécies. In Cerrado: ecologia e flora (S.M. Sano, S.P. Almeida & J.F. Ribeiro , eds). Embrapa-CPAC, Planaltina, p.417-1279., it was estimated that the phytogeographic domain of the Brazilian Cerrado contains 390 taxa of seedless vascular plants in its diverse phytophysiognomies. Of this total, a little more than half occur in forest formations, and less than 8% occur in rocky environments and on the edges of streams and rivers, where nearly all of the taxa listed here occur. Further, compared to the present study, pioneering works about this Brazilian Cerrado that treat the floristic composition of lycophytes and ferns (e.g., Simabukuro et al. 1994SIMABUKURO, E.A., ESTEVES, L.M. & FELIPPE, G.M. 1994. Lista de pteridófitas da mata ciliar da Reserva Biológica de Moji Guaçu, SP. Insula 23: 91-98., Forsthofer & Athayde Filho 2012FORSTHOFER, M. & ATHAYDE-FILHO, F.P. 2012. Florística e aspectos ecológicos de samambaias e licófitas ao longo do córrego cachoeirinha, Nova Xavantina-MT. Pesqui. Bot. 63: 149-164., Pallos et al. 2016PALLOS, J., GÓES-NETO, L.A.A., COSTA J.M., SOUZA, F.S. & PIETROBOM M.R. 2016. Licófitas e samambaias da Serra do Itauajuri, PA, Brasil. Rodriguésia 67(4): 997-1009.) cite a lower diversity of lycophytes and have only two species in common: Selaginella erythropus and Palhinhaea cernua.

Therefore, given the relevance of the data presented here, the importance of this study in relation to the Brazilian Cerrado and Chapada das Mesas National Park is evident, mainly because it increases what is known about the floristics and taxonomy of lycophytes from the Brazilian Cerrado phytogeographic domain, contributing to the biodiversity knowledge of this Protection area, and, in the future, possibly allowing appropriate conservation strategies. It is important to emphasize that the Chapada das Mesas National Park comprises half (six species) of lycophyte’s diversity recorded for the Maranhão state (twelve species including the results of this study). The other six species were not found in the Chapada das Mesas National Park during our survey: Lycopodiella geometra B.Øllg. & P.G.Windisch, Pseudolycopodiella carnosa (Silveira) Holub, P. caroliniana (L.) Holub, P. meridionalis (Underw. & Loyd) Holub, Selaginella flagellata Spring, S. marginata (Humb. & Bonpl. ex Willd.) Spring (Fernandes et al. 2010FERNANDES, R.S., CONCEICÃO, G.M., COSTA J.M. & PAULA-ZÁRATE, E.L. 2010. Samambaias e licófitas do município de Caxias, Maranhão, Brasil. Bol. Mus. Emílio Goeldi. Ciênc. Nat. (3): 345-356., Conceição & Rodrigues 2010CONCEIÇÃO, G.M. & RODRIGUES, M.S. 2010. Pteridófitas do Parque Estadual do Mirador, Maranhão, Brasil. Cad. Geociênc. (7): 47-53., Santos-Silva et al. 2018SANTOS-SILVA, D.L., SILVA, G.S., OLIVEIRA, R.R. & CONCEIÇÃO, G.M. 2018. Nova ocorrência de Lycopodiaceae (lycophyta) para o Estado do Maranhão: Pseudolycopodiella carnosa (Silveira) Holub. Biota Amazônia 8(2): 58-59, Flora do Brasil 2020FLORA DO BRASIL 2020. http://floradobrasil.jbrj.gov.br/ (último acesso em 28 Out 2019).
http://floradobrasil.jbrj.gov.br/...
, under construction). In addition, this protected area houses one species which had never been registered previously for the state, Selaginella conduplicata, and other species and genus possessing a restrict geographic distribution, such as: S. radiata and Isoëtes.

Acknowledgments

We thank the specialists Dr. Luiz Armando de Araújo Góes-Neto, for confirming the identification of some species of Selaginella, and Dr. Jovani Bernardino de Sousa Pereira, for examining the specimens of Isoëtes. We also thank Dr. Felipe Polivanov Ottoni and Dr. Fredgarson Costa Martins for helping to collect the material; Dr. Felipe Polivanov Ottoni for the critical revision of the manuscript before its submission; and Dr. Samuel Vieira Brito for helping with the photos. This project was financially supported by FAPEMA, Fundação de Amparo em Pesquisa do Estado do Maranhão (Processo universal nº 01271/2016).

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Publication Dates

  • Publication in this collection
    06 July 2020
  • Date of issue
    2020

History

  • Received
    27 Jan 2020
  • Reviewed
    20 Apr 2020
  • Accepted
    29 May 2020
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