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Rodriguésia

Print version ISSN 0370-6583On-line version ISSN 2175-7860

Rodriguésia vol.69 no.3 Rio de Janeiro July/Sept. 2018

http://dx.doi.org/10.1590/2175-7860201869335 

Original Papers

Ferns and lycophytes from Serra dos Carajás, an Eastern Amazonian mountain range

Alexandre Salino1  4 

André Jardim Arruda1  2 

Thaís Elias Almeida3 

1Universidade Federal de Minas Gerais, Av. Presidente Antônio Carlos 6627, Pampulha, 31270-901, Belo Horizonte, MG, Brasil.

2Université d’Avignon et des Pays de Vaucluse, IMBE - Institut Méditerranéen de Biodiversité et d’Ecologie, CNRS, IRD, Aix Marseille Université, IUT d’Avignon, AGROPARC BP61207, 84911 Avignon, France.

3Universidade Federal do Oeste do Pará, Herbário HSTM, Avenida Vera Paz s.n., Campus Tapajós, Salé, 68035-110, Santarém, PA, Brasil.

Abstract

In the state of Pará (Brazil), until the beginning of last decade little was known about the composition of the fern and lycophyte flora. The ferruginous mountains of Carajás are located in Southeastern Pará, mostly inserted in the Floresta Nacional de Carajás. The objective of this work is to present a complete and updated list of fern and lycophyte species occurring in all vegetation types from Carajás ferruginous mountains as a contribution to the knowledge of these plant groups from the Brazilian Amazon. The species list was based on specimens collected between 2007 and 2013. About 1068 specimens deposited in the BHCB Herbarium were studied. A total of 186 species of pteridophytes were recorded, 175 species of ferns distributed in 22 families and 68 genera, and 11 species of lycophytes distributed in three families and four genera. The fern and lycophyte flora of Serra dos Carajás region corresponds to 64% of the Pará state flora of these groups and 34% of the Brazilian Amazon fern and lycophyte flora. Seven taxa are presented as new records for Pará state: Asplenium abscissum, A. otites, A. praemorsum, Blechnum lanceola, Elaphoglossum minutum, Doryopteris collina, and Hemionitis tomentosa. Three species are endemic to Serra dos Carajás, Isoetes cangae, I. serracarajensis, and Selaginella stomatoloma.

Key words: Amazonia; canga; FLONA Carajás; floristic; pteridophytes

Resumo

No estado do Pará (Brasil), até o início da última década pouco se sabia sobre a composição da pteridoflora. As serras ferruginosas de Carajás estão localizadas na região sudeste do Estado, em sua maior parte inseridas na Floresta Nacional de Carajás. O objetivo deste trabalho é apresentar uma listagem completa e atualizada das espécies de samambaias e licófitas ocorrentes em todas as formações vegetacionais das serras ferruginosas da região de Carajás como uma contribuição ao conhecimento da pteridoflora da Amazônia Brasileira. A listagem de espécies foi elaborada com base nos espécimes coletados entre 2007 e 2013 durante expedições botânicas. Foram estudados cerca de 1068 espécimes que estão depositados no herbário BHCB. Foram registradas 175 espécies de samambaias distribuídas em 22 famílias e 68 gêneros, e 11 espécies de licófitas, distribuídas em três famílias e quatro gêneros. A pteridoflora da região de Carajás corresponde a 64% da flora de samambaias e licófitas do Pará e a 34% da pteridoflora da Amazônia Brasileira. Sete táxons são apresentados como novos registros para o estado do Pará: Asplenium abscissum, A. otites, A. praemorsum, Blechnum lanceola, Elaphoglossum minutum, Doryopteris collina e Hemionitis tomentosa. Três espécies são endêmicas da região de Carajás, Isoetes cangae, Isoetes serracarajensis e Selaginella stomatoloma.

Palavras-chave: Amazonia; canga; FLONA Carajás; florística; pteridófitas

Introduction

Currently, 10,578 species of ferns and 1,338 species of lycophytes are recognized (PPG I 2016). In Brazil, according to the Brazilian Flora online, 1,330 species of ferns and lycophytes have been recorded, of which 538 occur in the Amazon and 289 in the state of Pará (Flora do Brasil 2020, under construction).

In the state of Pará, until the beginning of last decade, little was known about the composition of the fern and lycophyte flora, besides the pioneering studies of Huber (1898, 1902, 1906), Sampaio (1930), Cain et al. (1956) and Pires (1992). However, from 2003 on, there was a great advance in the knowledge about seedless vascular plants in Pará state due to several floristic and taxonomic studies carried out in forest fragments located around the state capital, Belém (Rodrigues et al. 2004; Costa et al. 2006; Costa & Pietrobom 2007, 2010; Maciel et al. 2007; Ferreira et al. 2009; Miranda 2009; Silva 2009), and also in Castanhal (Tavares 2009), Tomé-Açu (Maciel 2008; Maciel & Pietrobom 2010a,b), Portel (Silva & Rosário 2008; Pietrobom et al. 2009), Salgado (Costa 2009), Tucuruí (Fernandes et al. 2012), Redenção (Fonseca 2010), Monte Alegre (Silva 2010), and in the protected areas of “Calha Norte” (Góes-Neto 2011), as well as new records and other studies (Góes-Neto & Pietrobom 2012a,b; Almeida & Salino 2015; Pallos et al. 2016), which have contributed significantly to improve the knowledge on the fern and lycophyte flora in Pará and in the Amazon region.

The Amazon Rainforest is the largest tropical forest on the planet and houses an invaluable biological heritage (Silva et al. 2005). Nevertheless, the biome currently has only 80% of its original coverage (Souza Jr. et al. 2013), and the creation of protected areas is vital for habitat protection and reduction of deforestation rates. In this context, the Floresta Nacional de Carajás (Flona Carajás) represents an important protected area​​ located in Southeastern Pará and was created with the basic goal of sustainable multiple uses of natural resources and scientific research. Among the mineral wealth found in Flona Carajás, there are extensive ferruginous mountains, which contain one of the largest iron resources on the planet. Together with the mountains of Quadrilátero Ferrífero in Minas Gerais state, these ferruginous outcrops represent 97% of the Brazil’s iron reserves (Porto & Silva 1989). Flona Carajás harbors a great variety of vegetation types, from rainforests to grasslands and savannas, presenting a mosaic associated with various types of soils, rocks, elevations, slopes and microclimates (Cleef & Silva 1994).

The vegetation and flora studies at Serra dos Carajás has begun around 1969 by researchers from the Museu Paraense Emílio Goeldi. The first floristic checklist of the region was published by Secco & Mesquita (1983). According to Viana et al. (2016), this work was pioneer and stimulated other floristic studies in the region, and at least five other floristics papers were published between 1986 and 1996. Still, all floristic studies carried out up to that time in Carajás region focused on angiosperms or bryophytes, and only one species of fern was cited by Silva et al. (1996).

The fern and lycophyte flora of Serra dos Carajás began to be investigated in 2007 when a group of researchers and collectors associated with the Laboratory of Plant Systematics and BHCB Herbarium from the Universidade Federal de Minas Gerais started to increase sampling of these plants following environmental impact studies at Flona Carajás. From 2009 on there was a considerable increment in fern and lycophyte collections with fieldwork been led by specialists, initially by Thaís Elias Almeida and André Jardim Arruda, and later in 2012 with Alexandre Salino. The largest collection effort was conducted between 2009 and 2013 and generated about 1,000 specimens that are housed at BHCB herbarium. From that collection six new species were described: two Blechnum (Dittrich et al. 2012), one Goniopteris (Salino et al. 2014), one Selaginella (Valdespino 2015), and two Isoetes (Pereira et al. 2016).

In 2014 a project entitled “Flora of the canga of the Serra dos Carajás, Pará, Brazil” started from a partnership between the Museu Paraense Emilio Goeldi (MPEG) and the Instituto Tecnológico Vale de Desenvolvimento Sustentável (ITVDS), in collaboration with the Universidade Federal de Minas Gerais. From this project, floristic treatments of 22 families of fern and lycophyte occurring at the canga in Carajás were published between 2016 to 2018: Aspleniaceae (Moura et al. 2016), Cyatheaceae (Salino & Arruda 2016a), Dennstaedtiaceae (Salino & Arruda 2016b), Dryopteridaceae (Moura & Salino 2016a), Lycopodiaceae (Salino & Arruda 2016c), Lygodiaceae (Salino & Arruda 2016d), Oleandraceae (Salino & Arruda 2016e), Pteridaceae (Moura & Salino 2016b), Schizaeaceae (Almeida 2017), Selaginellaceae (Góes-Neto et al. 2016), Thelypteridaceae (Moura et al. 2016), Anemiaceae (Pallos et al. 2017a), Blechnaceae (Salino et al. 2017), Gleicheniaceae (Lima & Salino 2017), Hymenophyllaceae (Pallos et al. 2017b), Isoetaceae (Pereira et al. 2017), Lindsaeaceae (Pallos et al. 2017c), Marattiaceae (Salino & Lima 2017), Nephrolepidaceae (Viveros & Salino 2017a), Polypodiaceae (Almeida et al. 2017), Tectariaceae (Viveros & Salino 2017b) and Ophioglossaceae (Salino 2018). These monographs included 70 species occurring in the open vegetation formations of the tops of the hills, known as vegetation associated with canga (Viana et al. 2016). Despite the high endemism and the importance of these unique habitats in Serra dos Carajás, areas of rainforests mostly associated with slopes and mountain bases present a great variety of microhabitats and consequently a high diversity of vascular plants. For this reason, this work aims to present a complete and updated list of fern and lycophyte species occurring in all vegetation formations at the Carajás ferruginous mountains.

Materials and methods

The Carajás ferruginous mountains are located in Southeastern Pará, 550 km south of the state capital Belém. These mountains are mostly located inside the limits of Flona Carajás and Parque Nacional dos Campos Ferruginosos (Fig. 1), between the valleys of the Tocantins and Xingu rivers (Viana et al. 2016). Flona Carajás is in the territory of Parauapebas, Canaã dos Carajás and Água Azul do Norte municipalities (STCP 2003). Parque Nacional dos Campos Ferruginosos is in Canaã dos Carajás and Parauapebas municipalities. The ferruginous outcrops are distributed along different mountains in an extension of ​​120 by 60 km. The main ranges are Serra Norte, Serra Sul and part of the Serra Leste (Ab’Saber 1986). Together, these mountains represent one of the largest iron resource in Brazil, whose magnitude and economic importance is equivalent to Quadrilátero Ferrífero resource (Porto & Silva 1989). According to Álvares et al. (2014), the region climate is Am, presenting a warm and humid moonson tropical climate. The average annual rainfall is of approximately 1600 mm, presenting a rainy season that can reach up to 1300 mm and a dry winter with average less than 320 mm, with the mean of the driest months sometimes reaching less than 60 mm (Moraes et al. 2005). The altitude range from 250 m in the foothills to 700 to 800 m in the flattened tops, where the open vegetation types associated with the iron outcrops stand out from the surrounding tropical forest. More detailed information on climate, relief and vegetation in Serra dos Carajás can be found in Mota et al. (2015) and Viana et al. (2016).

Source: Mota et al. (2018).

Figure 1 Study area, indicating the canga plateaux sampled. In black, remaining canga areas; in red, suppressed canga areas (representation based on satelite image taken in December 2016, available on Google Earth). In grey, Floresta Nacional de Carajás. In green, Parque Nacional dos Campos Ferruginosos. 

The species list was elaborated based on the collection from BHCB herbarium. Duplicates were sent mainly to the Carajás (HCJS) and the Museu Paraense Emílio Goeldi (MG) herbaria, and also to other herbaria in Brazil and abroad. The checklists contain only one voucher per species. We included in our survey four different ferruginous mountain ranges, of which two are located inside the Flona Carajás (Viana et al. 2016): i) Serra Sul (S11A, S11B, S11C, S11D), ii) Serra Norte (N1, N3, N4, N6 and N8); and two are currently included in the Parque Nacional dos Campos Ferruginosos: iii) Serra do Tarzan and iv) Serra da Bocaina (Fig. 1).

Species identification used specialized bibliographies, such as floras, taxonomic reviews, thesis, and dissertations, and as well by comparison with material already determined by specialists deposited in herbaria. When needed, materials and images were sent to specialists for confirmation and/or determination.

Results and discussion

A total of 186 species of pteridophytes were recorded for Serra dos Carajás, which places this study as one of the most representative surveys for the Brazilian Amazon. This number of species (186) corresponds to 64% of the ferns and lycophytes species recorded for Pará (289 spp.) and 34% of the fern and lycophyte flora of the Brazilian Amazon (538 spp.), making Serra dos Carajás one of the most diverse areas in Pará, and Brazilian Amazon.

The most representative families were Pteridaceae (36 spp.), Dryopteridaceae and Polypodiaceae (19 spp. each), Thelypteridaceae (18 spp.), Hymenophyllaceae (16 spp.), Aspleniaceae (13 spp.), Blechnaceae (9 spp.), and Tectariaceae (8 spp.). The expressive richness in families that are predominant in higher areas, such as Blechnaceae and Polypodiaceae, and also of families with known diversity in the Amazon region such as Pteridaceae, Hymenophyllaceae and Selaginellaceae, corroborate the results obtained in other studies in Pará (Costa et al. 2006; Costa & Pietrobom 2007; Maciel et al. 2007; Maciel 2008; Fernandes et al. 2012). Among the most representative fern genera are Adiantum (17 spp.), Asplenium (12 spp.), Trichomanes (8 spp.), Blechnum (7 spp.), Nephrolepis (6 spp.), Cyathea and Campyloneurum (5 spp. each), Elaphoglossum, Microgramma, Pteris, Triplophyllum, and Tectaria (4 spp. each) (Tab. 1). The richness observed in Adiantum and Trichomanes corroborates Tryon & Tryon (1982) remarks that the flora of Brazilian Amazon is well represented by species of those genera. Surprisingly, the richness found for Thelypteridaceae (18 spp.) contrasts greatly with results presented in other studies in the Amazon that do not found this family to be among the most representative ones (e.g., Costa & Pietrobom 2007; Maciel 2008; Costa et al. 2006b; Maciel et al. 2007; Zuquim et al. 2008).

Table 1 List of families and species of ferns occurring in the ferruginous mountains of Carajás, State of Pará, Brazil, with indication of environments and mountain ranges, life forms and vouchers. Subtitles: Habitat: DRF (dense rainforest); OF (open field); ORF (open rainforest); RV (rock vegetation), SF (swampy field); SFC (seasonal forest on canga). Life form: TE (Terrestrial); EP (Epiphytic); RU (Rupicolous); HE (Hemiepiphytic); AQ (Aquatic). (▲) = new species, (⚑) = new records for Pará, (✻) = species occurring in the canga of Carajás, (✦) = species occurring in the Quadrilátero Ferrífero (MG), (✚) = species occurring in the Maçico do Urucum (MS). 

Family/Species Habitat Serra da Bocaina Serra Norte Serra Sul Serra do Tarzan Life forms Voucher
ANEMIACEAE
Anemia elegans (Gardner) C. Presl ✻ ✦ DRF S11D RU Costa 815
Anemia oblongifolia (Cav.) Sw. ✻ ✦ SFC S11A,C,D RU Salino 15567
Anemia phyllitidis (L.) Sw. ✦ ✚ SFC/ORF S11C,D RU/TE Viana 4133
ASPLENIACEAE
Asplenium abcissum Willd. ✻ ⚑ ✦ DRF N3 S11A RU Salino 15238
Asplenium cristatum Lam. ✦ DRF S11C TE Almeida 2248
Asplenium cruegeri Hieron. DRF X N1 S11C,D X RU/TE Almeida 2349
Asplenium formosum Willd. ✻ ✦ ✚ SFC/ORF X N3,4 S11A,C,D X RU Almeida 2172
Asplenium hostmanii Hieron. DRF N4,6 S11A,C,D RU Salino 15228
Asplenium juglandifolium Lam. DRF N1 Paula 528
Asplenium otites Link ⚑ ✦ ✚ DRF S11D TE Almeida 2215
Asplenium poloense Rosenst. DRF X S11A,B,D RU/TE Almeida 2181
Asplenium praermosum Sw. ⚑ ✦ DRF X S11A,B,D EP/RU Mota 1954
Asplenium salicifolium L. ✻ SFC/ORF N6,8 S11A,C,D EP/RU Salino 15229
Asplenium serratum L. ✻ ✦ SFC/ORF/DRF N4 S11A,C,D X EP/RU Arruda 579
Asplenium stuebelianum Hieron. ✻ ✦ SFC/ORF X S11A,B,D RU Arruda 222
Hymenasplenium delitescens (Maxon) L. Regalado & Prada DRF S11D TE Almeida 2347
ATHYRIACEAE
Diplazium cristatum (Desr.) Alston ✦ ✚ DRF N1 S11D TE Almeida 2206
BLECHNACEAE
Blechnum areolatum V.A.O. Dittrich & Salino ▲✻ SFC/ORF X N8 S11B,D RU Almeida 2255
Blechnum asplenioides Sw. ✦ DRF S11D RU Viana 4347
Blechnum heringeri Brade ✻ SFC/ORF X X RU/TE Mota 1921
Blechnum lanceola Sw. ⚑ DRF S11A,D RU Salino 15504
Blechnum longipilosum V.A.O. Dittrich & Salino ▲✻ SFC/ORF X N1,6 S11C,D RU Viana 4148
Blechnum occidentale L. ✻ ✦ ✚ SFC/ORF N1,6 S11C,D TE Salino 15237
Blechnum polypodioides Raddi ✻ ✦ ✚ SFC/ORF X N1,6 S11B,C,D RU Almeida 2165
Neoblechnum brasiliense (Desv.) Gasper & V.A.O. Dittrich ✻ ✦ ✚ SFC/ORF S11C,D TE Almeida 2525
Telmatoblechnum serrulatum (Rich.) Perrie, D.J.Ohlsen & Brownsey ✻ ✦ SF N1 S11A,D TE Arruda 348
CYATHEACEAE
Alsophila cuspidata (Kunze) D.S. Conant DRF X S11D TE Almeida 2350
Cyathea delgadii Sternb. ✦ ✚ DRF S11C TE Viana 4141
Cyathea macrosora (Baker ex Thurn) Domin var. reginae (P.G. Windisch) A.R. Sm. DRF S11A,B,D TE Almeida 2351
Cyathea microdonta (Desv.) Domin ✦ ✚ DRF S11D TE Arruda 349
Cyathea pungens (Raddi) Domin ✻ ORF/DRF X S11A,B,C,D TE Salino 15498
Cyathea spectabilis (Raddi) Domin var. spectabilis DRF N1 S11D TE Salino 15499
DENNSTAEDTIACEAE
Hypolepis repens (L.) C. Presl ✦ DRF N1 S11A TE Arruda 623
Pteridium arachnoideum (Kaulf.) Maxon ✻ ✦ ✚ ORF X S11 X TE Salino 15954
DRYOPTERIDACEAE
Bolbitis semipinnatifida (Fée) Alston DRF S11A,B RU/TE Almeida 2424
Bolbitis serratifolia (Mert. ex Kaulf.) Schott ✚ DRF N4 S11A,B,C,D EP/RU/TE Salino 15304
Ctenitis nigrovenia (H. Christ ) Copel. ✻ SFC/ORF N4 S11A,C X RU/TE Salino 15512
Ctenitis refulgens (Klotzsch ex Mett.) C. Chr. DRF N3,4,6 S11A,C,D TE Salino 15211
Cyclodium guianense (Klotzsch) van der Werff ex L.D. Gómez DRF X N1,6 S11A,B,C,D TE Arruda 485
Cyclodium inerme ( Fée) A. R. Sm. DRF X N1,4,6 S11A,B TE Arruda 1134
Cyclodium meniscioides (Willd.) C. Presl var. meniscioides DRF N3,4,6 S11A,C HE/TE/RU Almeida 2433
Dryopteris huberi (Christ) C. Chr. ✻ ✦ SFC/ORF/DRF S11A,C,D X RU Arruda 586
Elaphoglossum flaccidum (Fée) T. Moore DRF N1 S11A,D EP Salino 15268
Elaphoglossum glabellum J. Sm. ✻ ✦ SFC/ORF S11D EP Viana 4115
Elaphoglossum luridum (Fée) H. Christ ✦ DRF S11A,C,D EP/RU Almeida 2500
Elaphoglossum minutum (Pohl ex Fée) T. Moore ⚑ DRF S11D EP Almeida 2265
Parapolystichum effusum (Sw.) Ching ✦ DRF X N1 S11A,C,D TE Salino 15244
Mickelia guianensis (Aubl.) R.C. Moran et al. DRF N1,3 S11A,C,D HE/TE Arruda 227
Mickelia nicotianifolia (Sw.) R. C. Moran et al. DRF N1,4 S11D HE/TE Salino 15190
Olfersia cervina (L.) Kunze ✦ DRF N1 S11A HE Arruda 549
Polybotrya caudata Kunze ORF N1 S11D HE Arruda 622
Polybotrya osmundacea HuSFC. & Bonpl ex Willd. DRF S11A HE Almeida 2436
Polybotrya sorbifolia Mett. ex Kuhn ✻ DRF X N1 S11A,B,D HE/TE Arruda 1151
GLEICHENIACEAE
Dicranopteris flexuosa (Schrad.) Underw. ✻ ✦ ✚ SFC X TE Cavalcante 2155 (MG)
Gleichenella pectinata (Willd.) Ching ✻ ✦ ORF N1 S11D TE Almeida 2276
HYMENOPHYLLACEAE
Abrodictyum rigidum (Sw.) Ebihara & Dubuisson ✦ DRF N1 RU Paula 527
Didymoglossum ekmanii (Wess. Boer) Ebihara & Dubuisson DRF N1 EP Salino 15131
Didymoglossum kapplerianum (Sturm) Ebihara & Dubuisson DRF X N4 S11A,B RU Salino 15254
Didymoglossum krausii (Hook. & Grev.) C. Presl ✦ DRF S11D EP Viana 4112
Didymoglossum ovale E. Fourn. DRF S11D RU Almeida 2466
Hymenophyllum polyanthos (Sw.) Sw. ✦ DRF S11B EP/RU Arruda 1183
Polyphlebium diaphanum (Kunth) Ebihara & Dubuisson ✦ DRF N1 EP Arruda 619
Trichomanes accedens C. Presl ✻ DRF S11D EP/RU/TE Arruda 464
Trichomanes ankersii C. Parker ex Hook. & Grev. DRF S11A EP Almeida 2439
Trichomanes crispum L. ✻ SFC/ORF/DRF S11D EP/RU Viana 4346
Trichomanes elegans Rich. ✻ ✦ DRF N1,4 S11A TE Almeida 2185
Trichomanes hostmannianum (Klotzsch) Kunze DRF N1,6 S11D RU Salino 15281
Trichomanes pedicellatum Desv. DRF N1 HE/RU Paula 529
Trichomanes pinnatum Hedw. ✻ ✦ SFC/ORF X N6 X RU/TE Arruda 870
Trichomanes vittaria DC. ex Poir. DRF N4 TE Arruda 990
Vandenboschia radicans (Sw.) Copel. ✻ ✦ DRF N1 S11D X RU/TE Almeida 2361
LINDSAEACEAE
Lindsaea divaricata Klotzsch ORF S11D RU/TE Arruda 350
Lindsaea guianensis (Aubl.) Dryand. ssp. Guianensis ORF S11A TE Almeida 2442
Lindsaea lancea (L.) Bedd. var. lancea✻ ✦ SF/ORF N1,4 S11B,D TE Arruda 484
Lindsaea pallida Klotzsch ORF X N1 RU/TE Arruda 554
LOMARIOPSIDACEAE
Cyclopeltis semicordata (Sw.) J. Sm. DRF S11B,D X TE Arruda 1326
Lomariopsis japurensis (Mart.) J. Sm. DRF N1 S11A,D HE Salino 15250
Lomariopsis nigropaleata Holttum ✚ DRF N1 X HE Salino 15197
Lomariopsis prieuriana Fée DRF N4 S11C HE Almeida 2339
LYGODIACEAE
Lygodium venustum Sw. ✻ ✦ ✚ ORF X S11D TP Almeida 2278
MARATTIACEAE
Danaea cartilaginea Christenh. & Tuomisto ✻ DRF N1 S11D TE Salino 15240
Danaea leprieurii Kunze ✻ DRF X S11A,C TE Arruda 1142
METAXYACEAE
Metaxya parkeri (Hook. & Grev.) J. Sm. DRF N1,6 S11B,C TE Salino 15232
NEPHROLEPIDACEAE
Nephrolepis biserrata (Sw.) Schott ORF S11C,D EP/TE Almeida 2218
Nephrolepis brownii (Desv.) Hovenkamp & Miyam. ✻ SFC/DRF X N1 TE/EP Arruda 1246
Nephrolepis hirsutula (G. Forst.) C. Presl ✻ OF/ORF X N1 RU/EP/TE Arruda 1251
Nephrolepis pectinata (Willd.) Schott ✻ ✦ SFC/DRF X RU/EP/TE Mota 2022
Nephrolepis rivularis (Vahl) Mett. ex Krug SF/ORF S11A,D EP/TE Almeida 2440
Nephrolepis undulata (Afzel. ex Sw.) J. Sm. ✻ SFC/ORF S11A,B,C RU/TE Arruda 1107
OLEANDRACEAE
Oleandra pilosa Hook. ✻ SFC/ORF S11A,C,D EP/RU Arruda 468
OPHIOGLOSSACEAE
Ophioglossum nudicaule L. ✻ SF X TE Mota 1909
POLYPODIACEAE
Campyloneurum abruptum (Lindm.) B.Leon DRF S11C,D EP/TE Almeida 2335
Campyloneurum angustifolium (Sw.) Fée DRF S11A EP Almeida 2195
Campyloneurum centrobrasilianum Lellinger ✻ ✚ SFC S11D EP Almeida 2254
Campyloneurum phyllitidis (L.) C. Presl ✻ ✚ SFC/ORF/DRF S11A,C,D EP/RU Salino 15152
Campyloneurum repens (Aubl.) C. Presl DRF N1,4 S11D EP Arruda 1149
Microgramma dictyophylla (Kunze ex Mett.) de la Sota DRF N1,4 S11B,C EP Almeida 2230
Microgramma lycopodioides (L.) Copel ✻ SFC/ORF X N1,4 S11A,C EP Arruda 833
Microgramma percussa (Cav.) de la Sota ✦ DRF S11A,B,C EP/TE Almeida 2242
Microgramma persicariifolia (Schrad.) C. Presl ✻ SFC/ORF X N4 S11A,B,D EP/TE Salino 15150
Niphidium crassifolium (L. ) Lellinger ✦ DRF X EP Salino 15141
Pecluma hygrometrica (Splitg.) M.G. Price DRF S11B,C EP Salino 15589
Pecluma plumula (Willd.) M.G. Price ✻ ✦ SFC S11A EP/RU Almeida 2495
Phlebodium decumanum (Willd.) J. Sm. ✻ ✚ ORF X N8 S11C,D EP/RU Arruda 526
Pleopeltis astrolepis (Liebm.) E. Fourn. ✦ ✚ DRF X S11A,D EP/RU Almeida 2216
Pleopeltis desvauxii (Klotzsch) Salino DRF N1 S11A,B,C,D EP/RU/TE Arruda 1228
Pleopeltis polypodioides var. burchelli (Baker) A. R. Sm. ✻ RV/SFC/ORF X N4,8 S11B,C,D EP/RU/TE Salino 15571
Polypodium flagellare Christ DRF S11C EP Almeida 2219
Serpocaulon attenuatum (C. Presl) A.R. Sm. ✻ RV/SFC/ORF N4 S11C,D X EP/RU/TE Salino 15149
Serpocaulon richardii (Klotzsch) A.R. Sm. DRF N1 S11A,B EP/RU Arruda 545
PTERIDACEAE
Acrostichum danaeifolium Langsd. & Fisch. SF S11D TE Almeida 2318
Adiantopsis radiata (L.) Fée ✻ ✦ SFC/ORF/DRF X S11A,B,C,D X RU/TE Arruda 605
Adiantum adiantoides (J. Sm.) C. Chr. DRF N1 TE Salino 15196
Adiantum argutum Splitg. DRF S11A,D X TE Almeida 2340
Adiantum cajennense Willd. ex Klotzsch DRF N4 S11B,C,D TE Arruda 1133
Adiantum cinnamomeum Lellinger & J. Prado DRF N1,8 TE Salino 15140
Adiantum deflectens Mart. ✻ ✦ ✚ SFC/ORF/DRF X S11D RU/TE Mota 2010
Adiantum dolosum Kunze DRF N4 TE Salino 15221
Adiantum glaucescens Klotzsch ✦ DRF X N1,8 X TE Arruda 1146
Adiantum humile Kunze DRF X TE Viana 4069
Adiantum lucidum (Cav.) Sw. DRF X N4 S11A,C TE Almeida 2227
Adiantum nudum A.R. Sm. DRF S11D RU Almeida 2353
Adiantum obliquum Willd. DRF N1,8 S11A,B,D RU/TE Arruda 552
Adiantum pectinatum Kunze ex Baker DRF S11A,C TE Almeida 2197
Adiantum petiolatum Desv. DRF X N4 TE Arruda 1403
Adiantum pulverulentum L. DRF N1 S11D TE Arruda 617
Adiantum terminatum Kunze ex Miq. DRF X N1 S11A TE Salino 15280
Adiantum tetraphyllum Willd. DRF N4 S11A TE Salino 15216
Adiantum villosum L. DRF X TE Mota 1211
Ananthacorus angustifolius (Sw.) Underw. & Maxon ✻ SFC/ORF/DRF S11B,C,D EP Almeida 2222
Ceratopteris pteridoides (Hook.) Hieron. DRF S11D AQ Almeida 2358
Ceratopteris thalictroides (L.) Brogn. ✻ RV/SF X AQ Mota 2578
Doryopteris collina (Raddi) J. Sm. ✻ ⚑ ✦ ✚ RV/SFC S11D X RU Arruda 776
Doryopteris varians (Raddi) J. Sm. ✦ SFC/ORF S11D RU/TE Arruda 456
Hemionitis palmata L. SFC/ORF N4,8 S11A,D X RU/TE Arruda 228
Hemionitis rufa (L.) Sw. DRF S11D X EP/RU Arruda 1315
Hemionitis tomentosa (Lam.) Raddi ✻ ⚑ ✦ ✚ SFC S11D RU Giorni 361
Lytoneuron ornithopus (Hook & Baker) J.C. Yesilyurt ✻ ✦ RV/SFC N3 S11C,D RU/TE Almeida 2410
Pityrogramma calomelanos (L.) Link ✻ ✦ ✚ OF /SF N1 S11D TE Arruda 1248
Polytaenium citrifolium (L.) Schuettp. DRF S11D EP Viana 4386
Polytaenium guayanense (Hieron.) Alston DRF S11D EP/RU Almeida 2262
Pteris biaurita L. ORF X S11D TE Arruda 524
Pteris denticulata Sw. var. denticulata✦ ✚ DRF N4 S11A X RU/TE Arruda 590
Pteris pungens (Willd.) Domin DRF N1 S11B,D X RU/TE Paula 547
Pteris quadriaurita Retz.. ✦ ✚ DRF X X TE Arruda 593
Vittaria lineata (L.) J. Sm. ✻ ✦ ✚ SFC/ORF/DRF S11A,D EP Arruda 1164
SACCOLOMATACEAE
Saccoloma chartaceum G.B. Nair DRF N1,8 S11A,B,C TE Almeida 2217
Saccoloma inaequale (Kunze) Mett. ✦ DRF N1 RU/TE Salino 15132
SCHIZAEACEAE
Actinostachys subtrijuga (Mart.) C. Presl ✻ SF S11C TE Viana 4134
TECTARIACEAE
Tectaria heracleifolia (Willd.) Underw. ✻ DRF S11C,D X RU/TE Almeida 2246
Tectaria incisa Cav. ✦ ✚ DRF X N1 RU/TE Arruda 580
Tectaria leprieurii (Mett. ex Diels) C. Chr. DRF N1 X RU/TE Salino 15500
Tectaria trinitensis Maxon DRF X TE Arruda 588
Triplophyllum dicksonioides (Fée) Holttum DRF N1,8 TE Salino 15209
Triplophyllum funestum (Kunze) Holttum DRF X N6 S11A X RU/TE Arruda 1398
Triplophyllum glabrum J. Prado & R.C. Moran ✻ DRF N6 S11A,B,D RU/TE Salino 15224
Triplophyllum hirsutum (Holttum) J. Prado DRF N1 TE Arruda 550
THELYPTERIDACEAE
Christella conspersa (Schrad.) Á. Löve & D. Löve ✦ ✚ DRF N1 S11D TE Almeida 2478
Christella hispidula (Decne.) Holttum ✻ ✦ ✚ DRF X S11C,D X TE Almeida 2342
Christella patens (Sw.) Pic.Serm. ✦ DRF N1 S11D TE Arruda 1273
Cyclosorus interruptus (Willd.) H. Ito ✻ ✦ OF/SF/ORF X N1 S11B TE Arruda 582
Goniopteris abrupta (Desv.) A.R. Sm. ✻ DRF X X TE Salino 15161
Goniopteris amazonica (Salino & R.S. Fernandes) Salino & T.E. Almeida DRF N1 X TE Salino 15246
Goniopteris biformata (Rosenst.) Salino & T.E. Almeida DRF S11D TE Almeida 2537
Goniopteris biolleyi (Christ) Brade DRF N1 S11D X TE Almeida 2371
Goniopteris indusiata (Salino) Salino & T.E. Almeida ▲ DRF N1 S11D X TE Salino 15156
Goniopteris pennata (Poir.) Pic.Serm. ✻ DRF S11A X TE Almeida 2200
Goniopteris poiteana (Bory) Ching ORF X TE Salino 15573
Goniopteris tetragona (Sw.) C. Presl ✻ DRF S11D X TE Almeida 2363
Goniopteris tristis (Kunze) Brade ✻ DRF N1 X TE Arruda 1313
Macrothelypteris torresiana (Gaudich.) Ching ✦ ✚ ORF X TE Paula 539
Meniscium chrysodioides Fée ✦ DRF N1,4 S11A,C TE Salino 15191
Meniscium maxonianum (A.R. Sm.) R.S. Fernandes & Salino ✻ ✦ SF/ORF N4,8 X TE Arruda 963
Meniscium nesioticum (Maxon & C.V. Morton) Pic.Serm. DRF X TE Salino 15584
Meniscium serratum Cav. ✦ DRF S11D TE Almeida 2359

The lycophytes are represented in the area by three families: Isoetaceae (Isoetes) with two species, Lycopodiaceae (Phlegmariurus and Palhinhaea) with two species, and Selaginellaceae (Selaginella) with seven species (Tab. 2).

Table 2 List of families and species of lycophytes occurring in the ferruginous mountains of Carajás, state of Pará, Brazil, with indication of environments and mountain ranges, life forms and vouchers. Subtitles: Habitat: DRF (dense rainforest); OF (open field); ORF (open rainforest); PP (permanent pond); RV (rock vegetation), SF (swampy field); SFC (seasonal forest on canga). Life form: TE (Terrestrial); EP (Epiphytic); RU (Rupicolous); HE (Hemiepiphytic); AQ (Aquatic). (▲) = new species, (⚑) = new records for Pará, (✻) = species occurring in the canga of Carajás, (✦) = species occurring in the Quadrilátero Ferrífero (MG), (✚) = species occurring in the Maçico do Urucum (MS). 

Family/Species Habitat Serra da Bocaina Serra Norte Serra Sul Serra do Tarzan Lifeforms Voucher
ISOETACEAE
Isoetes cangae J.B.S. Pereira, Salino & Stützel ▲ ✻ SF S11D AQ Arruda 1329
Isoetes serracarajensis J.B.S. Pereira, Salino & Stützel ▲ ✻ PP X N3,4,6,7 S11B X AQ Almeida 2157
LYCOPODIACEAE
Palhinhaea cernua (L.) Vasc. & Franco ✻✦✚ SF/DRF N1 S11B TE Arruda 212
Phlegmariurus dichotomus (Jacq.) W.H. Wagner DRF N1 S11A,D EP Salino 15142
SELAGINELLACEAE
Selaginella flagellata Spring SFC/DRF N4 S11D RU/TE Arruda 500
Selaginella producta Baker DRF X RU Arruda 865
Selaginella radiata (Aubl.) Spring ✻ RV/SFC/DRF N2,3,4 S11A,D X RU Salino 15206
Selaginella simplex Baker ✻ OF/SFC/DRF S11A,C,D RU/TE Salino 15256
Selaginella sulcata (Desv. ex Poir.) Spring ex Mart. DRF N1 S11A,C,D RU/TE Almeida 2187
Selaginella stomatoloma Valdespino ▲ DRF S11D RU Almeida 2518
Selaginella tenella (P. Beauv.) Spring DRF N4 S11D RU Salino 15214

Seven taxa listed here are new records for Pará (Tab. 1, 2). Three species are endemic to Serra de Carajás: Isoetes cangae, Isoetes serracarajensis and Selaginella stomatoloma, and Goniopteris indusiata is endemic to Pará.

Regarding life forms, we observed that most species are exclusively terrestrial (70 spp or 37.5%), followed by species sharing rupicolous/terrestrial habit (28 spp. or 15%), exclusively rupicolous (22 spp or 11.8%), epiphytic (18 spp. or 9.7%), and species sharing rupicolous/epiphytic habits (14 spp or 7.5%). Species exclusively hemiepiphytic or aquatic represented only 3.2% (six spp.) and 2.2% (four spp.) of total, respectively. It is also noteworthy that only 35% of the species present more than one habit (65 ssp.), while most species (121 spp. or 65%) have an exclusive habit. From the non-terrestrial species with exclusive habit we highlight four aquatic species: Isoetes cangae, I. serracarajensis, Ceratopteris pteridoides and C. thalictroides; five hemiepiphytic species: Polybotrya caudata, P. osmundacea, Lomariopsis japurensis, L. nigropaleata and L. prieuriana; and one climbing species: Lygodium venustum.

The low percentage of exclusively epiphytic species found in Carajás (18 spp. or 10%) may be related to the marked presence of savanna and grassland formations, which start at 600 m altitude and occupy most of the higher parts of the mountains, thus not favoring the epiphytism due to low density of tree hosts. In addition, a possible predominance of epiphytes that are restricted to the forest canopy, which is generally inaccessible and difficult to observe, may have directly influenced the reduced number of epiphytes recorded.

Regarding the vegetation types, we observed that most species (130 spp. or 70%) were found exclusively in forest environments. From the 130 species that occurs exclusively in forest environments, 88.5% (115 spp.) occur exclusively in Dense Ombrophilous Forest, followed by 13 (10 %) occurring in Open Ombrophylous Forest. Four species are exclusive from seasonal forest canga on the hilltops: Anemia oblongifolia, Campyloneurum centrobrasilianum, Pecluma plumula, and Hemionitis tomentosa. Only 13 species (7%) are unique to non-forest environments. In addition, three species are exclusive of swampy fields: Telmatoblechnum serrulatum, Acrostichum danaeifolium, and Actinostachys subtrijuga. We also found two species growing exclusively in ponds: Isoetes cangae and Isoetes serracarajensis, which occurs exclusively in permanent and temporary ponds, respectively.

The occurrence of ferns and lycophytes in Carajás was not uniform. From the 186 recorded species, 153 (82%) occurred at Serra Sul, of which 60 species (32%) recorded only exclusive at this mountain range, followed by 99 species (53%) recorded in Serra Norte, with 16 exclusive species (8.5%); 44 species (23%) recorded in Serra da Bocaina, with only three exclusive species (1.5%); and 37 species (20%) in Serra do Tarzan, with only five exclusive species (2.5%). These values may be biased due to an unbalanced sample effort in these mountains, with bigger sampling effort at Serra Sul and Serra Norte. In Serra do Tarzan, for example, the sampling effort was not exhaustive due to difficulties accessing the most preserved areas. In addition, the mountain ranges differed as to their conservation status. During the sampling period, Serra Sul presented more preserved vegetation formations than Serra da Bocaina that was at the time outside the limits of a protected area and showed bigger anthropic influence in its vegetation.

Along with the mountain ranges of Serra dos Carajás, two other regions in Brazil stand out as the most relevant mountain formations with ferruginous substrate: Quadrilátero Ferrífero (QF) in Minas Gerais state and Maciço do Urucum (MU) in Mato Grosso do Sul state. Salino & Almeida (2008) recorded the occurrence of 380 species of ferns and lycophytes in QF and Assis (2007) recorded 83 species in the MU. From the 186 species recorded in the Carajás region, 65 (35%) also occur in QF and 32 (17%) in MU (Tab. 1, 2).

The surveys and studies focusing on ferns and lycophytes from Serra dos Carajás over the last 12 years revealed a high diversity of species and yielded the discovery of six new species, three ferns (Dittrich et al. 2012; Salino et al. 2014) and three lycophytes (Valdespino 2015; Pereira et al. 2016), as well as three new records for Brazil (Almeida & Salino 2015) and seven new records for Pará state. The knowledge about ferns and lycophytes from Serra dos Carajás contributed to the increase of 31 species known to Pará state. These data reinforce the importance of floristic studies as tools to support and direct conservation policies and emphasize the importance of preserving ecosystems associated with ferruginous outcrops, not only in the Amazon. Additionally, the high number of taxa and new records for Pará reinforces the existence of collection gaps not only in the state but mainly in the Amazon region (Almeida & Salino 2016).

Editor de área: Dr. Pedro Viana

Acknowledgements

We thank the Graduate Program in Plant Biology of the Universidade Federal de Minas Gerais (UFMG) for general support to the project. Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for the Master’s degree scholarship to A.J. Arruda. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the research grants to A. Salino (201414/2017-1 and 307115/2017-8) and for the research project financing (455505 / 2014-4). To the project MPEG/ITV/FADESP (01205.000250 / 2014-10). The companies Golder Associates and Vale for supporting the development of the field part of the project. Instituto Chico Mendes de Biodiversidade (ICMBio) for the granting of collecting license and support, especially the biologist Frederico Drumond Martins (Director of the Flona Carajás). To the biologists P.L. Viana, N.F.0. Mota, L.S. Viana, V. Giorni, M. Pivari, F.M. Santos for the samples collections made in the Serra dos Carajás. To the pteridologists V. Dittrich, L. Góes-Neto, J. Costa, R. Viveros, R. Fernandes, F.C. Assis, J. Pereira, L. Sylvestre, D. Sanin and J. Prado for the support in the identification of some taxa.

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Received: March 18, 2018; Accepted: May 02, 2018

4 Author for correspondence: salinobh@gmail.com

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