Introduction

The Seasonal Semideciduous Forest is one of the most extensive forest vegetation types in Brazil, included in Domain of the Atlantic Rainforest, stretches along the Brazilian coast and inland to Paraguay and Argentina (Instituto Brasileiro de Geografia e Estatística [IBGE], 2012). The high levels of species richness and endemism associated with the destruction in the past included the Atlantic Rainforest as one of the 34 biodiversity hotspots on Earth (Mittermeier et al., 2004). Currently, there are

only 8% of the original territory and what is left is becoming increasingly fragmented (Mittermeier et al., 2004). In the Atlantic Rainforest, approximately 49.5% of the Brazilian flowering plants species are endemic (Brazil Flora Group [BFG], 2015).

Brazil holds 95% of Seasonal Semideciduous Forest, corresponding to 13% of its territory (Stehmann et al., 2009). This vegetation type is characterized by the dual climate seasonality and the partial leaf shedding between 20 and 50% individuals, which takes place annually in the unfavorable dry period in the tropics or intense cold in the subtropical region (Veloso, Rangel Filho, & Lima, 1991; IBGE, 2012).

In the State of Paraná, Seasonal Semideciduous Forest occurs in the North, Northwest and West, down from 800 m high (Roderjan, Galvão, Kuniyoshi, & Hatschbach, 2002). In such areas, the forest is characterized by presenting canopy between 15 and 20 m high, with emerging individual trees about 30 m high. Currently not much is left of this phytophysionomy because it is in the region that was most deforested in the State of Paraná over the past 75 years, for the establishment of monocultures of coffee, soybeans, wheat, sugarcane and corn. The vegetation was poorly studied before the profound disturbances, so there is little existing data on the original floristic composition.

Thus, the objective of this study was to characterize the floristic diversity of vascular species of one of the largest remnants of Seasonal Semideciduous Forest in southern Brazil, the ‘Reserva Biológica das Perobas’.

Material and methods

Study area

The ‘Reserva Biológica das Perobas’ (Figure 1) was located in the northwestern State of Paraná (23º 47’ S, 23º 55’ W). It was established in 2006 as a Federal Integral Protection Conservation Unit and covers the municipalities of Tuneiras do Oeste and Cianorte. The total surface area is approximately 8.716 ha (Instituto Chico Mendes de Conservação da Biodiversidade [ICMBio], 2013), being the second largest continuous remnant of the Seasonal Semideciduous Forest in the State of Paraná, smaller only than the ‘Parque Nacional do Iguaçu’, which is located approximately 160 km to the southwest of the study area. The symbol species of this protected area are the ‘peroba’ (Aspidosperma polyneuron Müll.Arg., Apocynaceae), an emergent tree that was very common in the region and an important logging product.

The climate of the study area is, according to the Köppen–Geiger climate classification system, Cfa, characterized by a humid subtropical climate with hot, humid summers and mild to cool winters, with rainfall concentrated in summer (Instituto Agronômico do Paraná [Iapar], 2000). Soils are derived from sandstone (Arenito Caiuá) and have a high vulnerability to erosion (Iapar, 1999).

The predominant phytogeographic formation in this area are the Seasonal Semideciduous Forest. However, near the Reserve there are two remnants of differentiated vegetation: one, about 5 Km east, covered by Subtropical Mixed Forest, with great abundance of Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae); and another less than 100 m from the unit, in the east, with characteristic elements of Tropical Savanna (Cerrado) (unpubl. data, M.G. Caxambú).

According to Castella and Britez (2004), this forest can be classified as forest in intermediate stage of succession. Although this area has not been clear-cut, intense logging for more than four decades promoted the development of features of this succession stage.

Data collection and data analysis

Fieldwork on ‘Reserva Biológica das Perobas’ was carried out during field trips from August 2011 to November 2015. During our surveys, we compiled a complete species list of vascular plants. Hiking have been covered along the entire area and covering all phytophysionomy, according to Filgueiras, Brochado, Nogueira, and Gualla II (1994). All species were collected and deposited with a voucher number in the herbarium of ‘Universidade Tecnológica Federal do Paraná, campus Campo Mourão’ (HCF). Species that were not found fertile but are vegetatively easily recognized were also included in the list with ‘no voucher’. Taxonomic identification was conducted using specialized references, comparisons to material deposited in herbaria, and consultation with experts.

The classification system used for angiosperms was based on Angiosperm Phylogeny Group IV (APG, 2016) and for families and genera of lycophytes and ferns, we followed the classification of Pteridophyte Phylogeny Group I (PPG, 2016).

Species status (native, exotic), life form (climber, herb, shrub, subshrub, tree) and use of substrate (aquatic, epiphytic, hemiepiphytic, hemiparasitic, mycoheterotroph, rupicolous, terrestrial) was assigned according to the observed on the field and database of Flora do Brasil (2017).

Results

A total of 425 species was recorded for ‘Reserva Biológica das Perobas’ (414 native and eleven exotic) belonging to 295 genera and 101 families (Table 1). Ferns were represented by 44 species, 29 genera and 17 families; Lycophytes, with only one species, Palhinhaea cernua (L.) Franco & Vasc. (Lycopodiaceae); Gymnosperms, with one species, Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae); and Angiosperms with 379 species, 264 genera and 82 families.

Fourteen families of angiosperms had more than 10 species, represented in Figure 2. The families with the highest number of species were Fabaceae (27 spp.), Asteraceae (21 spp.), Bignoniaceae (19 spp.), Poaceae (19 spp.) and Orchidaceae (16 spp.). Twenty-six families were represented by only one species.

Among the ferns, Polypodiaceae (8 spp.), Pteridaceae (7 spp.), Dryopteridaceae and Aspleniaceae (4 spp. each) were the families with the highest number of species.

The genera with the highest number of species were Piper L., Solanum L. (8 spp. each), Peperomia Ruiz & Pav. (7 spp.), Psychotria L. (6 spp.), Myrcia DC., Ocotea Aubl. (5 spp. each), Cyperus L., Miconia Ruiz & Pav. and Asplenium L. (4 spp. each). Fifty-one genera were represented by three species, 46, by two species and 221 by one species.

Life form and use of substrate are summarized in Table 2. Most species were herbs and trees, followed by shrubs and climbers. Subshrubs had a lower number of species in the study area. Nearly 22% of species showed variable life forms. Concerning the use of substrate, terrestrial was the most representative, followed by epiphytic species that accounted for 10% of all recorded species. Aquatic, hemiepiphytic, mycoheterotroph and hemiparasitic species were poorly represented in this area. The number of species with variable use of substrate was low (1.7%).

Two species recorded in the study area have unique records in the State of Paraná: Bulbophyllum rupicolum Barb.Rodr. (Orchidaceae) and Heladena multiflora (Hook. & Arn.) Nied. (Malpighiaceae).

Eleven species are exotic to the State of Paraná; six are Poaceae species and other five are in Anacardiaceae, Bignoniaceae, Euphorbiaceae, Marantaceae and Orchidaceae (Table 1).

Discussion

The study area contains about 6.5 to 7.0% of the vascular plant species registered for the State of Paraná (Kaehler et al., 2014; BFG, 2015) and about 25.5% of the species listed for the Seasonal Semideciduous Forest on this State (Flora do Brasil, 2017). Therefore, it is a large remnant with high specific diversity for the region.

Geologist Reinhard Maack was the pioneer in describing and mapping the Paraná vegetation in the 1950s and 1960s, before the deep changes in the post-colonization landscape. According to Maack (1968), one of the elements that characterized the vegetation on the sandstone soil ‘Arenito Caiuá’ was the abundance of palm specimens, especially Euterpe edulis (Arecaceae), constituting dense clusters in original forest. In the study area, adults are rare and occur sparsely in border areas. Dense clusters of this species are still found in interior of forest and in more conserved areas. After the creation of Conservation Units, in 2006, and prohibition of selective logging, great regeneration and nuclei formation with many young individuals are visible.

A characteristic tree species is ‘peroba’ (Aspidosperma polyneuron, Apocynaceae), reaching up to 40 m high (Maack, 1968). Currently, the largest individuals of ‘peroba’ found on this area (30-33 m in height and about 1.3 m in diameter) do not form a continuous canopy and in rare cases are found groups of 4-5 individuals side by side. The selective cut in the past has removed most of the larger trees, used for the construction of houses, very common in the region. The remaining individuals are those with deformities in the trunks, with no interest in commercial exploration. Species of Meliaceae (Cedrela L. species) and Lauraceae (Nectandra Rol. ex Rottb. and Ocotea species) are other typical flora elements (Maack, 1968) and still can be found with abundance in the study area.

Other typical species of submontane Seasonal Semideciduous Forest (Roderjan et al., 2002) present in the study area are: Astronium graveolens Jacq. (Anacardiaceae), Balfourodendron riedelianum (Engl.) Engl. (Rutaceae), Diatenopteryx sorbifolia Radlk. (Sapindaceae), Peltophorum dubium (Spreng.) Taub. and Parapiptadenia rigida (Benth.) Brenan (Fabaceae), among the trees; Syagrus romanzoffiana (Cham.) Glassman (Arecaceae), Inga marginata Willd. (Fabaceae) and Jacaratia spinosa (Aubl.) A.DC. (Caricaceae), in the understory layer.

In relation to the families with higher species diversity, this and several studies in Seasonal Semideciduous Forest in the State of Paraná point to Fabaceae in remnants of diverse sizes (Souza, Kawakita, Slusarski, & Pereira, 2009; Costa, Estevan, Bianchini, & Fonseca, 2011; Slusarski & Souza, 2012; Rossetto & Vieira, 2013; Garcia, Romagnolo, & Souza, 2017). Asteraceae appears in second place in the study area and in Souza et al. (2009), Rossetto and Vieira (2013) and Garcia et al. (2017). The other following families, more diverse and which can be considered characteristics of the Seasonal Semideciduous Forest in Paraná remnants are Rubiaceae, Euphorbiaceae, Myrtaceae, Bignoniaceae, Poaceae, Orchidaceae, Solanaceae and Sapindaceae.

Herbaceous species were more numerous in this area (34%) and in the Upper Paraná River floodplain (32%), a vegetation with several riparian environments and a large area sampled (235 ha) (Souza et al., 2009). In other remnants of Seasonal Semideciduous Forest in the State of Paraná, tree species are dominant, between 38 and 53% of the total flora (Costa et al., 2011; Slusarski & Souza, 2012; Rossetto & Vieira, 2013; Garcia et al., 2017).

According to Roderjan et al. (2002), the presence of climbers is expressive in the Seasonal Semideciduous Forest, with Bignoniaceae, Sapindaceae, Cucurbitaceae and Asteraceae as the most common families. In the study area, 23.5% of the native species are climbers and the dominant families are Bignoniaceae, Fabaceae, Apocynaceae, Malpighiaceae and Sapindaceae, as in several studies in nearby areas (Carneiro & Vieira, 2012; Santos, Caxambú, Silva, Hoppen, &Villagra, 2014). This study demonstrates the highest proportion of climbers (23.5%) in relation to other surveyed remnants of Seasonal Semideciduous Forest in Paraná, which recorded less than 18% of the total flora (Souza et al., 2009; Costa et al., 2011; Slusarski & Souza, 2012; Rossetto & Vieira, 2013; Garcia et al., 2017).

The occurrence of epiphytes is extremely low in Seasonal Semideciduous Forest (Roderjan et al., 2002), being Philodendron bipinnatifidum Schott (Araceae) the most characteristic species. In the study area, 43 epiphytes were recorded (30 angiosperms, 13 ferns), about 18% of epiphytes occurring in Seasonal Semideciduous Forest in the State of Paraná (Flora do Brasil, 2017) and approximately 10% of local flora, showing that epiphytes are an important component of this forest. Orchidaceae, Polypodiaceae and Piperaceae are the most common families, which are the families often found as more diverse in studies in the region (Borgo, Silva, & Petean, 2002; Cervi & Borgo, 2007; Dettke, Orfrini, & Milaneze-Gutierre, 2008; Bonnet, Curcio, Lavoranti, & Galvão, 2011).

Gomesa lietzei (Regel) M.W.Chase & N.H.Williams and Miltonia flavescens (Lindl.) Lindl. (Orchidaceae) are the most common epiphytes in the area and Pechuma sicca (Lindm.) M.G. Price and Microgramma squamulosa (Kaulf.) de la Sota (Polypodiaceae) are the common among ferns. The occurrence of epiphytes is significant in the canopy of large tree species, especially in the emergent branches of ‘perobas’, where several species of Tillandsia L. can be found. Inside the forest, in more shady areas and with larger trunks, Philodendron bipinnatifidum is often found, as Cactaceae species.

Five species found in ‘Reserva Biológica das Perobas’ are in official list of threatened species of Brazil (Ordinance 443/dez 2014) (Brasil, 2014): Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae) and Heladena multiflora (Hook. & Arn.) Nied. (Malpighiaceae) in Endangered status and Euterpe edulis Mart. (Arecaceae), Zeyheria tuberculosa (Vell.) Bureau ex Verl. (Bignoniaceae) and Cedrela fissilis Vell. (Meliaceae) in Vulnerable status.

Two species are unique records in the State of Paraná in the study area: Bulbophyllum rupicolum (Orchidaceae), recently cited for Paraná (Barros et al., 2015) and Heladena multiflora (Malpighiaceae), a new occurrence by this study. Bulbophyllum rupicolum occurs preferentially as rupicolous in areas of Tropical Savanna (Cerrado), Central Brazil (Barros et al., 2015); in the study area, it was collected as epiphytic and probably represents an influence of the nearby Cerrado, although it has not yet been found in this area (unpubl. data, M.G. Caxambú). Heladena multiflora was a liana or shrub, distributed in Brazil, Paraguay and northeastern Argentina (Anderson, Anderson, & Davis, 2016). In Brazil, it occurs in Central-West and Southeast regions, and according Amorim, Kutschenko, Judice, and Barros (2013), the occupation area has suffered a continuous decline and the species is included as Endangered in Brazil.

On the other hand, the presence of exotic species points out this area as vulnerable, especially in areas of forest edges under human influence. Seven out of the eleven species recorded for the area are indicated as invasive species by State laws (Ordinance IAP 59/April 2015) (Paraná, 2015). Mangifera indica L. (Anacardiaceae), Tecoma stans (L.) Juss. ex Kunth (Bignoniaceae), Ricinus communis L. (Euphorbiaceae) and Oeceoclades maculata (Lindl.) Lindl. (Orchidaceae), are invasive, but few individuals were found in the area. However, three herbaceous species of Urochloa P. Beauv. (Poaceae) are common in forest edges, in contact with monocultures areas. For other species, Ctenanthe setosa (Roscoe) Eichler (Marantaceae), which is not treated as invasive to the State of Paraná, was found locally and is very common on the trails and spreads quickly, being potential invasive in the study area.

Conclusion

The ‘Reserva Biológica das Perobas’ presents a quarter of the species listed for the Seasonal Semideciduous Forest in the State of Paraná, including two exclusive species. Therefore, it is a large remnant with high specific diversity for the region. The most representative families are Fabaceae, Asteraceae, Bignoniaceae, Poaceae and Orchidaceae. The predominant life forms are herbs and trees, and terrestrial plants represented the majority of species. Eleven species in this area are exotic to the flora of the State of Paraná, points out this as vulnerable area.

Acknowledgements

The authors would like to thank the researchers who helped in the identification of the material collected in this study, the Instituto Chico Mendes de Conservação da Biodiversidade – ICMBio for the authorization for research, under number 48840, especially to Carlos Alberto Ferraresi De Giovanni (In Memorian) and Antônio Guilherme Cândido for the support and help at all times. To professor Heron de Oliveira dos Santos Lima, director of the Universidade Tecnológica Federal Paraná Campus Campo Mourão for his support and Federal Deputy Rubens Bueno for the parliamentary amendment that allowed the acquisition of equipment and vehicles used in this study.

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Author notes

gretadet@yahoo.com.br