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Checklist of ferns and lycophytes from the highlands of Pico Paraná State Park, Paraná, Brazil

Abstract

We present a checklist for the ferns and lycophytes from Pico Paraná State Park, in Southern Brazil. The Park is entirely located at the Serra do Mar mountains, and represents an important remnant of the Atlantic Rain Forest with altitude achieving 1,887 m. In this locality is the Pico Paraná, the highest mountain in Southern Brazil. This study was focused on the altitudes above 1,000 m, which are mainly represented by dwarf forests and altitudinal fields. A total of 142 species were recorded, three of them (Ceradenia maackii, Diplazium tamandarei, and Stenogrammitis wittigiana) are only found in the park in Southern Brazil. Besides of the checklist of the species, we highlight some important aspects related to endangered species, geographic distribution, and life forms. The high level of endemism, the presence of endangered species, and the phylogenetic diversity as represented by distinct families of ferns and lycophytes show the biogeographic importance of this area for the conservation of these groups of plants.

Key words:
Atlantic Rain Forest; endemism; highlands; richness; Southern Brazil

Resumo

Nós apresentamos uma compilação das espécies de samambaias e licófitas coletadas no Parque Estadual Pico Paraná, sul do Brasil. O Parque está localizando dentro da Serra do Mar paranaense, e representa um importante remanescente de Floresta Atlântica com altitude atingindo 1.887 m. Nesta localidade está o Pico Paraná, a montanha mais alta do sul do Brasil. Neste estudo foi investigado as áreas acima de 1.000 m, justamente nos pontos onde ocorrem floresta nebular e campos de altitude. No total foram registradas 142 espécies. Ceradenia maackii, Diplazium tamandarei, and Stenogrammitis wittigiana são encontradas apenas na área do parque no sul do Brasil. Além de apresentar a lista de espécies, este estudo destaca as espécies ameaçadas, distribuições geográficas e formas de vida das plantas. O alto nível de endemismo, a presença de espécies ameaçadas, a diversidade filogenética representada por várias famílias de samambaias e licófitas mostram a importância biogeográfica do Pico Paraná para a conservação destes grupos de plantas.

Palavras-chave:
Floresta Atlântica; endemismo; ambiente de altitude; riqueza; Sul do Brasil

Introduction

The mountain regions of the Neotropics present a high rate of diversity, richness and endemism for ferns and lycophytes (Tryon 1972Tryon R (1972) Endemic areas and geographic speciation in tropical American ferns. Biotropica 4: 121-131., 1986Tryon R (1986) The biogeography of species, with special reference to ferns. Botanical Review 52: 118-156.; Moran 1995Moran RC (1995) The importance of mountains to Pteridophytes, with emphasis on Neotropical montane forests. In: Churchill SP, Baslev H, Forero E & Luteyn JL (orgs.) Biodiversity and conservation of Neotropical Montane Forests. The New York Botanical Garden Press, New York. Pp. 359-363.). Particularly, this richness is in part influenced by different degrees of temperature, luminosity and humidity, which vary accordingly to the different altitudinal gradients. Likewise, these different environmental conditions require specific morphological and physiological adaptions of the species (Lieberman et al. 1996Lieberman D, Lieberman M, Peralta R & Hartshorn GS (1996) Tropical forest structure and composition on a large-scale altitudinal gradient in Costa Rica. Journal of Ecology 84: 137-152.; Kessler 2000Kessler M (2000) Elevational gradients in species richness and endemism of selected plant groups in the central Bolivian Andes. Plant Ecology 149: 181-193.; Safford 2007Safford HD (2007) Brazilian Páramos IV. Phytogeography of the campos de altitude. Journal of Biogeography 34: 1701-1722.). As a result, the upper-montane forests and the highland fields frequently harbors a high levels of endemism (Martinelli 2007Martinelli G (2007)W Mountain biodiversity in Brazil. Revista Brasileira de Botânica 30: 587-597.), and many species are also exclusive of these environments (Martinelli 2007Martinelli G (2007)W Mountain biodiversity in Brazil. Revista Brasileira de Botânica 30: 587-597.).

Among the mountain ranges of the Serra do Mar in coastal Brazil, the Pico Paraná State Park is placed in an interesting biogeographic position. It is located in a confluence of different vegetation types, such as the Araucaria forests, grassland fields, and the Atlantic Rain Forest (Maack 2012Maack R (2012) Geografia física do estado do Paraná. 4a ed. Editora UEPG, Ponta Grossa. 526p.; Labiak 2014Labiak PH (2014) Aspectos fitogeográficos do Paraná. In: Kaehler M, Goldenberg R, Labiak PH, Ribas OS, Vieira AOS & Hatschbach GG (orgs.) Plantas vasculares do Paraná. Departamento de Botânica da Universidade Federal do Paraná, Curitiba. Pp. 7-22.). The Park is also a borderline region for the geographic distribution of many plant species (Labiak 2014Labiak PH (2014) Aspectos fitogeográficos do Paraná. In: Kaehler M, Goldenberg R, Labiak PH, Ribas OS, Vieira AOS & Hatschbach GG (orgs.) Plantas vasculares do Paraná. Departamento de Botânica da Universidade Federal do Paraná, Curitiba. Pp. 7-22.). Additionally, the Pico Paraná is the highest point in Southern Brazil and presents few botanically explored environments and peculiar geographical-climatical conformations (Maack 2012Maack R (2012) Geografia física do estado do Paraná. 4a ed. Editora UEPG, Ponta Grossa. 526p.). This prompted us to carry out a more detailed botanical survey of its environments, focusing on those areas above 1.000 meters that are the less explored botanically.

Here, we present a checklist of the species of ferns and lycophytes from Pico Paraná State Park, highlighting the most important records for Southern Brazil, reporting the endangered species, and showing the data of the geographic distribution and life forms, as a contribution to the knowledge of the diversity presented in high montane forests in the Brazilian Atlantic Rain Forest.

Materials and Methods

Study site

The Pico Paraná State Park (PEPP) is located in the cities of Campina Grande do Sul and Antonina, in Paraná state, Southern Brazil. The park comprises an area of 4.334 hectares in the Serra do Ibitiraquire, a mountain chain that is part of the main range called Serra do Mar mountains. The Park is located between the coordinates 25º12’51.68”-25º17’52.91”S and 48º46’20.46”-48º52’58.71”W (Figs. 1, 2). Within the limits of the Park is located the Pico Paraná, which is the highest mountain in Southern Brazil, reaching 1,887 m in altitude (Figs. 1, 2). The current study was carried out in the areas between 1,000-1,887 m.

Figure 1
Location of the Pico Paraná State Park, Paraná, Brazil (figure adapted from Google Earth).

Figure 2
Habitats in the Pico Paraná State Park – a. stream inside of the forest; b. cloud forest with the trunks of the tree covering by moss; c. upper montane forest; d. continuous fog in the highest latitudinal of the park; e. rocky outcrops; f. Pico Paraná; g. detail of the Pico Paraná; h. Campo de Altitude. (Photos: a. by Fernando B. Matos; b-e. by Jovani B.S. Pereira; f-h. by Paulo H. Labiak)

The PEPP is located within the Atlantic Rain Forest, and presents mainly elements of the Upper-montane and Campos de Altitude flora (sensu Veloso et al. 1992) (Fig. 2). This part of the Serra do Mar mountains is mainly composed by igneous and metamorphic rocks of pre-Cambrian origins (Bigarella 1978Bigarella JJ (1978) A Serra do Mar e a porção oriental do estado do Paraná um problema de segurança ambiental e nacional: contribuições à geografia, geologia e ecologia regional. Governo do Paraná, Secretaria de Estado do Planejamento, Associação de Defesa e Educação Ambiental, Curitiba. 248p.).

The climate in this area is considered as subtropical (Köppen 1948Köppen W (1948) Climatologia; con un studio de los climas de la tierra. Fondo de Cultura Economica, México. 478p.), with an average of annual temperature below 18 ºC in the winter, and 22 ºC in the summer (IAPAR 1994IAPAR - Instituto Agronômico do Paraná (1994) Cartas climáticas do estado do Paraná. Instituto Agronômico do Paraná, Londrina. 42p.). Frost is common during the winter, and the average annual rainfall varies from 2,000-2,500 mm, depending on the altitude (Ferretti & Britez 2006Ferretti AR & Britez RM (2006) Ecological restoration, carbon sequestration and biodiversity conservation: the experience of the Society for Wildlife Research and environmental education (SPVS) in the Atlantic Rain Forest of Southern Brazil. Journal for Natural Conservation 14: 249-259.).

Data collection

Fieldworks were carried out from April 2007 to March 2009, usually each two months (collection permit IAP 37/07, 2007). The specimens were deposited in the herbaria UPCB and MBM, and duplicates were also sent to other herbaria, when available. Also, collections of the herbaria MBM, an RB were consulted to search for potential collections from PEPP. The plants were identified using the literature, by comparison to the collections in UPCB, MBM and RB, as well as by consulting specialists (see acknowledge). The geographic distributions of the species are established using available data in the literature. This study followed the classification system of PPG I (2016)PPG I - The Pteridophyte Phylogeny Group (2016) A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563-603..

Results

A total of 142 species were recorded, corresponding to 64 genera and 19 families (see Table avaiable in <https://dx.doi.org/10.6084/m9.figshare.5899600>). The ferns comprised 128 species in 58 genera and 17 families, whereas the lycophytes were represented by 14 species in six genera and two families. The families with the highest number of species were Polypodiaceae (29 spp.), Hymenophyllaceae (21 spp.), Dryopteridaceae (16 spp.), Aspleniaceae and Lycopodiaceae (12 spp., respectively), and Pteridaceae (11 spp.). The most representative genera in number of species were Hymenophyllum (13 spp.), Asplenium (11 spp.), Elaphoglossum (8 spp.), and Phlegmariurus (7 spp.).

Special mention is given to Ceradenia maackii (Fig. 3a), an endemic species from PEPP, which was described from recent collections in the studied area (Labiak & Pereira 2016Labiak PH & Pereira JBS (2016) A new species of Ceradenia (Polypodiaceae) from Southern Brazil. Systematic Botany 41: 902-905.). Besides C. maackii, other two species are exclusively found in the PEPP in Southern Brazil: Diplazium tamandarei, and Stenogrammitis wittigiana (Fig. 3b).

Figure 3
Ferns species found in the Pico Paraná State Park – a. Ceradenia maackii. b. Stenogrammitis wittigiana. c. Doryopteris paradoxa. d. Dicksonia sellowiana. e. Jamesonia insignis. f. Grammitis fluminensis. g. Doryopteris crenulans. h. Hymenophyllum magellanicum. i. Melpomene albicans. j. Hymenophyllum rufum. k. Hypolepis rugulosa. l. Plagyogiria fialhoi. Scale bars: a,e,g,j = 10 cm; b = 2 cm; c,f,h,i,k = 5 cm; d = 1 m; l = 15 cm. (Photos: a,b,e-g,k. by Paulo H. Labiak; c,d. by Fernando B. Matos; h-j,l. by Jovani B.S. Pereira)

As for endangered species, we found that Doryopteris paradoxa (Fig. 3c), Dicksonia sellowiana (Fig. 3d), Jamesonia insignis (Fig. 3e), Grammitis fluminensis (Fig. 3f), Phlegmariurus nudus and P. christii are currently considered endangered species in Brazil (Martinelli & Moraes 2013Martinelli G & Moraes MA (orgs.) (2013) Livro vermelho da flora do Brasil. Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, Rio de Janeiro. 1100p.). Furthermore, the poorly known species Doryopteris crenulans (Fig. 3g), Hymenophyllum magelanicum (Fig. 3h), H. peltatum, and Trichomanes luces are species considered as having priority in taxonomic studies, in order to access their actual conservation status (IBAMA 2008IBAMA - Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (2008) Lista oficial de espécies da flora brasileira ameaçada de extinção. Portaria Nº 37-N, 03/04/92. Avaiable at <http://www2.ibama.gov.br/flora/extincao/htm>. Access on 11 September 2010.
http://www2.ibama.gov.br/flora/extincao/...
; Martinelli & Moraes 2013Martinelli G & Moraes MA (orgs.) (2013) Livro vermelho da flora do Brasil. Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, Rio de Janeiro. 1100p.).

As for the species distribution ranges (Fig. 4a), we found that 40 species (28%) are endemic to the Brazilian Atlantic Rain Forest (sensuOliveira-Filho & Fontes 2000Oliveira-Filho AT & Fontes MAL (2000) Patterns of floristic differentiation among Atlantic forests in Southeastern Brazil and the influence of climate. Biotropica 32:793-810.), whereas 10% (14 spp.) are Pantropical, 60% (85 spp.) are Neotropical, and 1% (2 spp.) are widely distributed in Brazil.

Figure 4
Number of species of ferns and lycophytes in the Pico Paraná State Park by geographic range and life form (percentage of the species in bracketss) – a. geographic ranges; b. life forms. The geographic distributions of the taxa are the following: Pantropical (PA), America (including Nearctical plus Neotropical) (AM), Neotropical (NE), widely distributed in Brazil (BR), endemic from Brazilian Atlantic rain forest (ED). The life forms are classified as terrestrial (TE), epiphyte (EP), rupiculous (RU), and more than one type of habitat (GE).

Concerning the life forms (Fig. 4b), 24% (34 spp.) were epiphytes (sensuBenzing 1990Benzing DH (1990) Vascular epiphytes. Cambridge University Press, New York. 354p.; including one terrestrial climber species, Lomaridium acutum), 18% (26 spp.) were rupiculous, 39% (55 spp.) of the species were exclusively terrestrials, and 19% (27 spp.) were found in more than one type of habitat.

Discussion

The PEPP has shown a high taxonomic diversity of ferns and lycophytes. This diversity is similar to more species-rich environments such as montane forests, as recorded by Matos et al. (2010)Matos FB, Amorin AM & Labiak PH (2010) The ferns and lycophytes of a montane tropical forest in Southern Bahia, Brazil. Journal of the Botanical Research Institute of Texas 4: 333-346., and Schwartsburd & Labiak (2007)Schwartsburd PB & Labiak PH (2007) Pteridófitas do Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Hoehnea 34: 159-209..

The richness of the Polypodiaceae species found in PEPP can be related to the presence of grammitid ferns such as Ceradenia (Fig. 3a), Cochlidium, Grammitis (Fig. 3f), Melpomene (Fig. 3i), Stenogrammits (Fig. 3b), Lellingeria, Terpsichore, Leucotrichum and Moranopteris, which are particularly well distributed at high elevations in the New World (Parris 2009Parris BS (2009) New genera of Malesian Grammitidaceae (Monilophyta). Blumea 54: 217-219.). Moreover, the richness of the Hymenophyllaceae, especially of Hymenophyllum (Fig. 3h,j), appears to be related to the cloud forests at higher altitudes where the genus is well diverse (Morton 1968Morton CV (1968) The genera, subgenera and sections of the Hymenophyllaceae. Contributions from the United States National Herbarium 38: 153-214.).

The Paraná State is a borderline region for the geographic distribution of many plant species. Particularly, the PEPP seems to be the southern borderline for the geographic distribution of the Diplazium tamandarei, and Stenogrammitis wittigiana (Fig. 3b). It must also be pointed out the occurrences of Doryopteris paradoxa (Fig. 3c), Phlegmariurus nudus, Hypolepis rugosula (Fig. 3k), and Amauropelta tamandarei, which are only known from few collections in Southern Brazil. Another interesting record is Plagiogyria fialhoi (Fig. 3l), which is found at high altitudinal environments in Southeastern Brazil, and occurs only in the PEPP within the state of Paraná.

Regarding the percentage of the endemics species finding in the PEPP (28%, see Fig. 4a), it is higher than those recorded in areas at lower altitudes in Southern Brazil, such as 4% (8 spp.) by Gasper & Sevegnami (2010)Gasper AL & Sevegnani L (2010) Lycophyta e samambaias do Parque Nacional da Serra do Itajaí, Vale do Itajaí, SC, Brasil. Hoehnea 37: 755-767., 9% (14 spp.) by Schwartsburd & Labiak (2007)Schwartsburd PB & Labiak PH (2007) Pteridófitas do Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Hoehnea 34: 159-209., and 25% (15 spp.) by Labiak & Prado (1998)Labiak PH & Prado J (1998) Pteridófitas epífitas da Reserva Volta Velha, Itapoá, Santa Catarina, Brasil. Boletim do Instituto de Botânica da Universidade de São Paulo 11: 1-79.. We attribute the high level of endemism in the PEPP to the varied number of environments, such as highlands fields, cloud forests, and rocky outcrops (Fig. 2a-h), which require of the species specific morphological and physiological adaptations to occur in these habitats (Safford 1999Safford HD (1999) Brazilian Páramos I. An introduction to the physical environment and vegetation of campos de altitude. Journal of Biogeography 26: 693-712.; Porembski 2007Porembski S (2007) Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Revista Brasileira de Botânica 30: 579-586.).

With respect to the life forms (Fig. 4b), the percentage of the epiphytic species was higher than the ones found in the Araucaria forest (19.7%; 30 spp.) by Schwartsburd & Labiak (2007)Schwartsburd PB & Labiak PH (2007) Pteridófitas do Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Hoehnea 34: 159-209., and in the lowlands coastal forests (19.3%; 16 spp.) by Salino et al. (2005)Salino A, Silva SM, Dittrich VAO & Britez RM (2005) Flora pteridofítica. In: Marques MCM & Britez RM História natural e conservação da Ilha do Mel. Ed. UFPR, Curitiba. Pp. 85-101.. This is not an unexpected result, considering the presence of streams and continuous fog in the highest altitudes (Fig. 2a-e), which make the altitudinal environments very humid (as evidenced by trees with trunks covered with moss; see Fig. 2a-c), and provide the necessary humidity for these ferns (Kessler 2000Kessler M (2000) Elevational gradients in species richness and endemism of selected plant groups in the central Bolivian Andes. Plant Ecology 149: 181-193.). This factor may explain the amount of epiphytic species that was recorded in the PEPP.

It is also important to note the high percentage of the species which were found exclusively as rupiculous (18%; Fig. 4b). This value is higher than those recorded in other vegetation formations such as in the montane forest in Paraná (2.5%; 2 spp.) and in southern Bahia (5%; 9 spp.) (Dittrich et al. 2005Dittrich VAO, Waechter JL & Salino A (2005) Species richness of pteridophytes in a montane Atlantic rain forest plot of Southern Brazil. Acta Botanica Brasilica 19: 519-525.; Matos et al. 2010Matos FB, Amorin AM & Labiak PH (2010) The ferns and lycophytes of a montane tropical forest in Southern Bahia, Brazil. Journal of the Botanical Research Institute of Texas 4: 333-346.; respectively), in the lowland and in the montane forest (4.2%; 8 spp.) (Gasper & Sevegnani 2010Gasper AL & Sevegnani L (2010) Lycophyta e samambaias do Parque Nacional da Serra do Itajaí, Vale do Itajaí, SC, Brasil. Hoehnea 37: 755-767.), and in the restinga (2.6%; 3 spp) (Salino et al. 2005Salino A, Silva SM, Dittrich VAO & Britez RM (2005) Flora pteridofítica. In: Marques MCM & Britez RM História natural e conservação da Ilha do Mel. Ed. UFPR, Curitiba. Pp. 85-101.). The number of rupiculous species may be related to the existence of markedly altitudinal environments such as rocky outcrop and rocky cliffs in the cloud forests as well as streams over rocks within the forest (Fig. 2e-h).

In conclusion, the altitudinal environment of the PEPP appears to offer the ideal conditions for the establishment of the various groups of ferns and lycophytes which results not just in the number of species, but also in the diversity of life forms. Furthermore, the high level of endemism, the presence of endangered species, and the phylogenetic diversity (as represented by distinct families of ferns and lycophytes) highlight the biogeographic importance of this area for the conservation of these groups of plants.

  • Editora de área: Dra. Lana Sylvestre

Acknowledgments

The authors thank Fabrício Meyer, Felipe Marinero, Fernando Matos, Marcelo Reginato, Mathias Meyer and Pedro Schwartsburd, for their help during the fieldworks. We are also grateful to the following specialists for identifications: Jefferson Prado (Megalastrum), Claudine Mynssen (Diplazium), Fernando Matos and Alejandra Vasco (Elaphoglossum), Mónica Ponce and Alexandre Salino (Thelypteridaceae), Pedro Schwartsburd (Hypolepis). We also thank Lana Sylvestre and two anonymous reviewers for helpful comments on the manuscript. This research was partially funded by grants from CNPq to Paulo Labiak (304835/2013-7), and to Jovani Pereira (245951/2012-1).

References

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Publication Dates

  • Publication in this collection
    Apr-Jun 2018

History

  • Received
    05 Feb 2017
  • Accepted
    29 May 2017
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