Ferns and lycophytes are significant components of tropical and temperate floras, occupying a variety of ecological niches (Holttum 1938; Tryon & Tryon 1982; Windisch 1992; 1996; 2002; Page 2002; Sharpe et al. 2010), and having patterns of geographical distribution that are associated with the long distance dispersal capacity of their spores (Tryon 1970; Smith 1972; Barrington 1993; Wolf et al. 2001).
In the meridional portion of South America (the "Southern Cone"), centers of species diversity and endemism, as well as limits to floristic distributions, have been related to paleogeographical alterations that produced climatic barriers and interrupted floristic continuity (Sota 1973; Ponce et al. 2002). At a local scale, climatic factors, such as temperature and humidity (Kessler 2001; Kessler et al. 2011), variation in the chemical composition of the edaphic matrix (Tuomisto & Ruokolainen 1993; Tuomisto & Poulsen 1996; Tuomisto et al. 2003a; Tuomisto et al. 2003b; Tuomisto et al. 2014), variation in pH (Ranal 1995a), environmental heterogeneity (Sylvestre & Windisch 2003; Dittrich et al. 2005; Nettesheim et al. 2014), and fragmentation and edge effect (Paciencia & Prado 2005) have been implicated in determining fern and lycophyte distribution.
There are about 140 lycophyte and 1,100 fern species in Brazil (Prado & Sylvestre 2015), with the greatest number occurring in the montane regions of the Atlantic Forest biome (Windisch 2002; Dittrich et al. 2005; Prado & Labiak 2009). The presence of a center of diversity and endemism of ferns and lycophytes in the Atlantic Forest of southeastern Brazil (Tryon 1972), is relevant for the diversity of southern Brazil, including the Coastal Region of the state of Rio Grande do Sul. This diversity within Rio Grande do Sul is represented by approximately 397 species (Sehnem 1977), mainly known from regional surveys (Mondin & Silveira 1989; Bueno & Senna 1992; Senna & Waechter 1997; Athayde-Filho & Windisch 2006; Schmitt et al. 2006; Lehn et al. 2009; Santos & Windisch 2008 Schmitt & Goetz 2010; Becker et al. 2013; Silva et al. 2013; Gonzatti et al. 2014a; Gonzatti et al. 2014b; Mallmann & Schmitt 2014), phytogeographic and palynological reviews (Sehnem 1977; Lorscheitter et al. 1998; 1999; 2001; 2002; 2005; 2009), and research on ecology, phenology and development (Schmitt & Windisch 2010; Schneider & Schmitt 2011; Schmitt & Windisch 2012; Rocha et al. 2013; Neumann et al. 2014; Quevedo et al. 2014; among others).
The Coastal Region possesses distinct phases of vegetational succession, featuring a mosaic of floristic communities from open grassland and wet areas to arboreal communities (Waechter 1990; Waechter & Jarenkow 1998; Müller & Waechter 2001). This mosaic is determined mainly by edaphic conditions, but also by wind action and extreme insolation (Rambo 1956). However, there is general transition in vegetation cover from it being scarce and sparse at the coastline, to gradually giving rise to forests with tropical characteristics in the continental interior (Rambo 1951; 1954; Klein 1984; Waechter 1990).
A marked change in vegetation cover is mainly determined by climatic changes close to the 30° S parallel, where abrupt differences in rainfall and temperature regimes occur, resulting in a north-to-south reduction of species richness, especially with regard to tropical elements (Rambo 1951; Waechter 1990). This north-to-south change from a tropical to a temperate climate induces floristic changes including the substitution of the Atlantic Forest biome by the Pampa biome in this portion of Rio Grande do Sul (Waechter 1985; Fiaschi & Pirani 2009; Overbeck et al. 2012).
Considering that only about 15% of the original Coastal Region vegetation coverage remains (Cordeiro & Hasenack 2012), and that area is a priority for conservation for the state of Rio Grande do Sul (MMA 2000), an increase in the knowledge of flora in this transitional vegetation formation would be valuable. Through this inventory, we seek to understand the distribution patterns of ferns and lycophytes among different vegetation physiognomies and along a latitudinal gradient in the study area, and the relationships of these plants with adjacent plant communities.
Materials and methods
The study area comprises the entire Coastal Region of the state of Rio Grande do Sul (CRRS hereafter), situated between the latitudes of 29°17'S to 33°41'S and the longitudes of 49°43'W to 53°31'W. The area encompasses about 33,000 km², and is characterized by extensive lowlands and several shallow freshwater lakes (Fig. 1), extending from the municipality of Torres in the north, to Chuí in the south. The CRRS is limited to the west, continental, side by the geomorphological formations of the "Sulriograndense" Plateau (a.k.a. "Serra Geral"), to the north, by the Central Depression and by the Sulriograndense Shield to the south. The origin of the Coastal Region is discussed by Tomazelli et al. (2000), Villwock & Tomazelli (2007) and Buchmann et al. (2009).
Despite the relative uniformity of these coastal areas, microtopographic variation allows for two main soil types: well drained sandy soils at low elevations, and poorly drained sandy, clayish or peaty soils in the lowlands. Most of the terrain is covered by Solodic Planosol derived from alluvial and lacustrine depositions or sandstone decomposition. These Planosol areas are poorly drained and have low fertility, with forest growing on peat. The northern portion is characterized by Hydromorphic Humic Quartz-Soil type (Neosol) of sedimentary origin formed during the Holocene and featuring a high accumulated-carbon content and poor drainage. Also in the northern portion, shallow and highly fertile Chernosols are present, with rock mixtures in the A horizon. Red Latosol can also be found, constituting deep soils, rich in iron and nutrient poor in the A horizon. Dune banks of depositional origin prevail along the coastline, composed of quartz sands of low pedogenetic structuration, low fertility and high wind mobility (Moser 1990; Embrapa 2006).
According to the Köppen classification, the climate is Cfa type, subtropical with hot summers with the coldest monthly mean temperature higher than −3 °C and the warmest above 22 °C, with an annual average of around 17.6ºC. Monthly precipitation varies between 100 and 170 mm, heterogeneously distributed between the extreme north and south of the Coastal Region (annual average: 1,423 mm in Torres and 1,186 and in Santa Vitória do Palmar). These climate conditions occur in most regions with altitudes below 600-650 m alt., and cover all the Coastal Region, reaching the limit at the Cfb climate type being found at the highest elevations (Moreno 1961; Alvares et al. 2013).
Sampling and data processing
Field work was conducted between March 2013 and December 2014 in 19 municipalities (Fig. 1). Spot inventories were conducted in different vegetation formations with random sampling following the procedure described by Filgueiras et al. (1994), from the seaside and up to 50 m alt. in regions with slope. The samples were collected and preserved following Windisch (1992). Voucher specimens were deposited in the ICN and HUCS herbaria (acronyms based on Thiers 2015).
Collections of the following herbaria were reviewed: Herbário do Instituto de Ciências Naturais, Universidade Federal do Rio Grande do Sul (ICN), Instituto Anchietano de Pesquisas, Universidade do Vale do Rio dos Sinos (PACA), Herbário Alarich Schultz, Fundação Zoobotânica do RS (HAS), Herbário da Universidade de Caxias do Sul (HUCS), Herbário da Universidade Federal de Pelotas (PEL) and Herbário da Universidade Federal de Rio Grande (HURG). All exsiccates from the study area were annotated with updated identifications and nomenclature, and their location and habitat information were added to our database.
The taxonomic delimitation of families and genera follows Smith et al. (2008), with the genus Deparia Hook. & Grev. belonging in Athyriaceae (Rothfels et al. 2012). Adaptations to Lycopodiaceae followed Øllgaard (2012). For the genus Blechnum L. we followed Perrie et al. (2014). For Tryonia J. Prado, A. T. Cochran we followed Cochran et al. (2014), and for Mickelia R. C. Moran et al. we followed Moran et al. (2010). Abbreviations of the names of the authors of species follow the Species List of the Flora of Brazil (Prado & Sylvestre 2015).
Species habits were categorized as terrestrial, epiphytic or aquatic and assigned to habitats: forest, grassland, wetland or combinations thereof. Species distribution patterns were categorized based on Waechter (2002) and Cabrera & Willink (1980), as follows:
Cosmopolitan: widely distributed across the five continents;
Amphipacific: disjunct distribution in the tropical and subtropical regions of America and Asia;
Holarctic: wide distribution in the temperate regions of the Northern Hemisphere and Eurasian region;
Pantropical: distribution in the American, African and Asian tropical regions;
Neotropical: distribution restricted to the American tropical and subtropical region;
Neotropical-Antarctic: distribution in the Neotropical region, with eventual occurrence in temperate South-American regions;
Neotropical-Atlantic: restricted to the Atlantic province;
Neotropical-Paranaense: restricted to the Paranaense province;
Neotropical-Pampeana: restricted to the Pampa biome.
The latitudinal distributions of the taxa within the study area were verified by their presence or absence in five latitudinal ranges, according to Waechter (1998). In this study, Ranges I and V were smaller than Ranges II, III and IV, as only areas within the state of Rio Grande do Sul were evaluated, and did not extend into the state of Santa Catarina or Uruguay (Fig. 1).
Range I (extreme North): species occurring from 29°17' south to 30ºS;
Range II (North): species occurring between the parallels 30º01' and 31ºS
Range III (Middle center): species occurring between the parallels 31°01' and 32°S;
Range IV (South): species occurring between the parallels 32°01' and 33°S;
Range V (extreme South): species occurring beside the parallel 33°01' and 33º41'S.
The floristic similarity among distinct latitudinal ranges was evaluated by applying the Sørensen Similarity Index using the Unweighted Pair-Group Method with Arithmetic Logarithm (UPGMA). This analysis was processed by the Past 3.04 software (Hammer et al. 2001).
A total of 3,450 herbarium records were evaluated, including 520 collected during our field work and 2,930 previously existing in collections. In total the records represented 223 species in 79 genera and 28 families, of which 17 were species of lycophytes and 206 were species of ferns (Tab. 1).
The largest values for species richness were for the families: Pteridaceae (34), Polypodiaceae (29), Thelypteridaceae (23), Dryopteridaceae (22), Aspleniaceae (18) and Blechnaceae (13). Marattiaceae, Psilotaceae, Lygodiaceae, Isoetaceae and Equisetaceae had one species each (Tab. 1). The genera with the largest values for species richness were: Thelypteris (22), Asplenium (17), Blechnum (12), Elaphoglossum (nine), Pecluma (eight), Pleopeltis (seven) and Doryopteris (seven), with the remaining genera varying from one to six species (Tab. 1).
Richness differed among the evaluated latitudinal ranges, with the number of taxa gradually decreasing from north-to-south with Range I having 198 species, while Range V had only 28. Of the total 223 species, only 21 occurred throughout the entire study area (Tab. 1). Large reductions in floristic richness occurred between latitudinal Ranges III and IV, and between Ranges IV and V, with a decrease of 46% and 51%, respectively. A 43 % reduction in floristic richness was observed between Ranges I and II. At the northern extreme of the study area (Range I), 34% of the richness corresponded to species that occur exclusively in that portion of the area, while in ranges to the south exclusive species comprised less than 10%, reaching 0% in the extreme South (Range V) (Fig. 2).
|Families/Species||Habit||Habitat||Geographic pattern||Latitudinal occurrence||Herbarium voucher|
|Anemia ferruginea Humb. & Bonpl. ex Kunth||T||F||NEO||I||PACA 100902|
|Anemia phyllitidis (L.) Sw.||T||F||NEO||I, II, III, IV||HUCS 41492|
|Anemia tomentosa (Sav.) Sw.||T||G/F||NEO||I, II, III, V||HUCS 41507|
|Anemia warmingii Prantl||T||F||NEO-ATL||I||ICN 107595|
|Asplenium abscissum Willd.||T||F||NEO||I, III||ICN 171238|
|Asplenium bradei Rosenst.||T||F||NEO-ATL||I, II||HUCS 41361|
|Asplenium brasiliense Sw.||T||F||NEO-PAR||I, II||ICN 161392|
|Asplenium claussenii Hieron.||T||F||NEO||I, II, III, IV||ICN 176197|
|Asplenium gastonis Fée||T/E||F||NEO-PAR||I, II, III, IV||HUCS 41374|
|Asplenium harpeodes Kunze||T||F||NEO||I, II||ICN 171237|
|Asplenium inaequilaterale Willd.||T||F||PAN||I, II, III||HUCS 41399|
|Asplenium incurvatum Fée||E||F||NEO-ATL||I, II||PACA 72760|
|Asplenium kunzeanum Klotzsch ex Rosenst.||T||F||NEO-ATL||I||ICN 176481|
|Asplenium martianum C. Chr.||T||F||NEO-ATL||I||ICN 176746|
|Asplenium mucronatum C.Presl||E||F||NEO-PAR||I||HUCS 40582|
|Asplenium oligophyllum Kaulf.||T||F||NEO||I||ICN 171106|
|Asplenium scandicinum Kaulf.||E||F||NEO-PAR||I, II, III||HUCS 39487|
|Asplenium sellowianum (Hieron.) Hieron.||T||F||NEO-PAR||I, II, III, IV, V||HUCS 41134|
|Asplenium serra Langsd. & Fisch.||T||F||NEO||I, II, III||ICN 161365|
|Asplenium ulbrichtii Rosenst.||T||F||NEO-PAR||II, III, V||HUCS 41523|
|Asplenium uniseriale Raddi||T||F||NEO||I||ICN 124310|
|Hymenasplenium triquetrum (N. Murak. & R.C. Moran) L. Regalado & Prada||T||F||NEO||I||ICN 124318|
|Deparia petersenii (Kunze) M. Kato||T||F||ANP||I, II, III, V||HUCS 41400|
|Diplazium ambiguum Raddi||T||F||NEO||I||ICN 126284|
|Diplazium cristatum (Desr.) Alston||T||F||NEO||I, II, III||ICN 176745|
|Diplazium herbaceum Fée||T||F||NEO-ATL||I, II||ICN 107001|
|Diplazium plantaginifolium (L.) Urb.||T||F||NEO||I, II||ICN 161430|
|Blechnum acutum (Desv.) Mett.||T/E||F||NEO||I, II, III, IV||HUCS 41401|
|Blechnum auriculatum Cav.||T||F||NEO-PAR||I, II, III, IV, V||HUCS 41084|
|Blechnum austrobrasilianum de la Sota||T||F||NEO-PAR||I, II, III, IV||HUCS 41067|
|Blechnum brasiliense Desv.||T||F/W||NEO||I, II, III, IV, V||HUCS 41069|
|Blechnum cordatum (Desv.) Hieron.||T||G/F/W||NEO-ANT||I, II, III, IV, V||HUCS 41055|
|Blechnum gracile Kaulf.||T||F||NEO||I||ICN 173499|
|Blechnum laevigatum Cav.||T||G||NEO-PAR||I, II, III||ICN 170402|
|Blechnum lehmannii Hieron.||T||F||NEO||I||ICN 114698|
|Blechnum occidentale L.||T||F||NEO||I, II, III, IV||ICN 176486|
|Blechnum polypodioides Raddi||T||G||NEO||I, II, III||HUCS 38878|
|Blechnum schomburgkii (Klotzsch) C. Chr.||T||G/W||NEO||I, II, III||HUCS 37970|
|Blechnum spannagelii Rosenst.||T||W||NEO-ATL||I, II||ICN 172982|
|Telmatoblechnum serrulatum (Rich.) Perrie, D.J. Ohlsen & Brownsey||T||G/F/W||NEO||I, II, III, IV, V||HUCS 37962|
|Alsophila setosa Kaulf.||T||F||NEO-PAR||I, II, III||ICN 176724|
|Cyathea atrovirens (Langsd. & Fisch.) Domin||T||F||NEO-PAR||I, II, III, IV||ICN 176726|
|Cyathea corcovadensis (Raddi) Domin||T||F||NEO-ATL||I||HUCS 41403|
|Cyathea delgadii Sternb.||T||F||NEO||I, II||HUCS 39883|
|Cyathea phalerata Mart.||T||F||NEO-ATL||I||ICN 176725|
|Dennstaedtia dissecta T. Moore||T||F||NEO||I||HUCS 41285|
|Dennstaedtia globulifera (Poir.) Hieron.||T||F||NEO||I, IV||HUCS 41521|
|Dennstaedtia obtusifolia (Willd.) T. Moore||T||F||NEO||I||PACA 77670|
|Hypolepis acantha Schwartsb.||T||F||NEO-ATL||III||-|
|Hypolepis stolonifera Fée||T||F||NEO-ATL||III||HUCS 41535|
|Pteridium arachnoideum (Kaulf.) Maxon||T||G||NEO||I, II, III, IV, V||HUCS 41078|
|Dicksonia sellowiana Hook.||T||F||NEO||I, II, III||HUCS 41394|
|Lophosoria quadripinnata (J.F. Gmel.) C. Chr.||T||G/F||NEO-ANT||I||ICN 176734|
|Ctenitis falciculata (Raddi) Ching||T||F||NEO||I||HUCS 41548|
|Ctenitis submarginalis (Langsd. & Fisch.) Ching||T||F||NEO||I, II, III||HUCS 41310|
|Didymochlaena truncatula (Sw.) J. Sm.||T||F||PAN||I, II||HUCS 161411|
|Elaphoglossum burchellii (Baker) C. Chr.||T/E||F||NEO||I||ICN 126301|
|Elaphoglossum glaziovii (Fée) Brade||T/E||F||NEO-ATL||I||HUCS 41537|
|Elaphoglossum lingua (C. Presl) Brack.||E||F||NEO-ATL||I||ICN 172999|
|Elaphoglossum luridum (Fée) Christ||T/E||F||NEO||I||HUCS 41538|
|Elaphoglossum macahense (Fée) Rosenst.||T/E||F||NEO-ATL||I||PACA 79232|
|Elaphoglossum macrophyllum (Mett. ex Kuhn) Christ||T||F||NEO-ATL||I||ICN 51347|
|Elaphoglossum pachydermum (Fée) T. Moore||T||F||NEO-ATL||I||ICN 126307|
|Elaphoglossum scolopendrifolium (Raddi) J. Sm.||T/E||F||NEO-ATL||I, II||ICN 166160|
|Elaphoglossum vagans (Mett.) Hieron.||T/E||F||NEO-ATL||I||ICN 166343|
|Lastreopsis amplissima (C. Presl) Tindale||T||F||NEO||I, II, III||ICN 176493|
|Lastreopsis effusa (Sw.) Tindale||T||F||NEO||I, II||ICN 161394|
|Megalastrum abundans (Rosenst.) A.R. Sm. & R.C. Moran||T||F||NEO-ATL||I||ICN 126310|
|Megalastrum connexum (Kaulf.) A.R. Sm. & R.C. Moran||T||F||NEO-PAR||I, II, III, IV||HUCS 41520|
|Megalastrum oreocharis (Sehnem) Salino & Ponce||T||F||NEO-PAR||I||ICN 126282|
|Mickelia scandens (Raddi) R.C.Moran et al.||T/E||F||NEO-ATL||I||HUCS 41289|
|Olfersia cervina (L.) Kunze||T/E||F||NEO||I||ICN 126305|
|Polybotrya cylindrica Kaulf.||T/E||F||NEO-ATL||I, II, III||ICN 176730|
|Polystichum platyphyllum (Willd.) C. Presl||T||F||NEO||I, II||ICN 107475|
|Rumohra adiantiformis (G. Forst.) Ching||T||G/F/W||PAN||I, II, III, IV, V||HUCS 41080|
|Equisetum giganteum L.||T||G/F/W||NEO-ANT||I, II, III, IV, V||HUCS 41128|
|Dicranopteris flexuosa (Schrad.) Underw.||T||G||NEO||I, II, III||HUCS 41311|
|Gleichenella pectinata (Willd.) Ching||T||G||NEO||I, II, III||HUCS 41498|
|Sticherus bifidus (Willd.) Ching||T||G||NEO||I, II||HUCS 41386|
|Sticherus lanuginosus (Fée) Nakai||T||G||NEO||I, II, III||HUCS 41312|
|Sticherus nigropaleaceus (J.W.Sturm) J.Prado & Lellinger||T||G||NEO||II||HUCS 39492|
|Sticherus pruinosus (Mart.) Ching||T||G||NEO||I||ICN 107002|
|Abrodictyum rigidum (Sw.) Ebihara & Dubuisson||T||F||NEO||I||ICN 176711|
|Didymoglossum hymenoides (Hedw.) Desv.||T/E||F||NEO||I, II, III||HUCS 41365|
|Didymoglossum reptans (Sw.) C. Presl||T/E||F||NEO||I, II||ICN 178344|
|Hymenophyllum caudiculatum Mart.||T/E||F||NEO-ANT||I||ICN 178347|
|Hymenophyllum polyanthos (Sw.) Sw.||E||F||PAN||I||ICN 42361|
|Hymenophyllum pulchellum Schltdl. & Cham.||E||F||NEO||I||ICN 85305|
|Polyphlebium angustatum (Carmich.) Ebihara & Dubuisson||E||F||NEO||I, II, III||ICN 161400|
|Polyphlebium pyxidiferum (L.) Ebihara & Dubuisson||E||F||PAN||I, II, III||ICN 178355|
|Trichomanes cristatum Kaulf.||T||F||NEO||I, II||ICN 176748|
|Trichomanes pilosum Raddi||T||G||NEO||I||HUCS 41308|
|Trichomanes polypodioides Raddi||E||F||NEO||I||ICN 178349|
|Vandenboschia radicans (Sw.) Copel.||T/E||F||PAN||I, II||ICN 41391|
|Vandenboschia rupestris (Raddi) Ebihara & K.Iwats.||T/E||F||NEO||I||ICN 178356|
|Isoetes weberi Herter||T||W||NEO-ATL||II||PACA 98839|
|Lindsaea lancea (L.) Bedd.||T||F||NEO||I, II||ICN 166179|
|Lindsaea quadrangularis Raddi||T||F||NEO||I, II||HUCS 41383|
|Lomariopsis marginata (Schrad.) Kuhn||T/E||F||NEO-ATL||I||ICN 146209|
|Nephrolepis cordifolia (L.) C. Presl||T||G||ANP||I, III||HUCS 41387|
|Nephrolepis exaltata (L.) Schott||T||G||NEO||III||PACA 74470|
|Nephrolepis pectinata (Willd.) Schott||T||G||NEO||II||ICN 129296|
|Diphasiastrum thyoides (Willd) Holub||T||G||NEO||I||ICN 176735|
|Lycopodiella alopecuroides (L.) Cranfill||T||G||NEO||I, II, III, IV, V||HUCS 41053|
|Lycopodiella tupiana (B. Øllg. & P.G. Windisch) B. Øllg.||T||G||NEO-PAR||II||HAS 78174|
|Lycopodium clavatum L.||T||G||COS||I, III||HUCS 41395|
|Palhinhaea cernua (L.) Franco & Vasc.||T||G/W||PAN||I, II, III||HUCS 41396|
|Phlegmariurus acerosus (Sw.) B.Øllg.||E||F||NEO||I||ICN 89978|
|Phlegmariurus fontinaloides (Spring) B.Øllg.||E||F||NEO-ATL||I||HAS 40598|
|Phlegmariurus heterocarpon (Fée) B.Øllg.||E||F||NEO-PAR||I, II||HAS 40596|
|Phlegmariurus mandiocanus (Raddi) B.Øllg.||E||F||NEO-PAR||I, II||ICN 178336|
|Phlegmariurus quadrifariatus (Bory) B.Øllg.||E||F||NEO-ATL||I||ICN 44523|
|Phlegmariurus reflexus (Lam.) B.Øllg.||T||F||NEO||II||PACA 905|
|Pseudolycopodiella caroliniana (Silveira) Holub||T||G||NEO||I, II, III, V||HUCS 41054|
|Lygodium volubile Sw.||T||F||NEO||I||HUCS 41393|
|Eupodium kaulfussii (J.Sm.) J.Sm.||T||F||NEO||I||ICN 124279|
|Marsilea ancylopoda A. Braun||T||W||NEO||I, III, IV||HUCS 41269|
|Regnellidium diphyllum Lindm.||T||W||NEO-PAM||I, II, III, IV, V||HUCS 41468|
|Cheiroglossa palmata (L.) C.Presl||E||F||PAN||I, II||ICN 178367|
|Ophioglossum crotalophoroides Walter||T||G||NEO||I, IV||HURG 115|
|Ophioglossum nudicaule L. f.||T||G||PAN||I, II, III, IV||ICN 47377|
|Ophioglossum reticulatum L.||T||G||PAN||I, II, III||ICN 45109|
|Osmunda regalis L.||T||G/F/W||HOL||I, II, III, IV, V||HUCS 41052|
|Osmundastrum cinnamomeum (L.) C. Presl||T||G/F/W||HOL||III, IV||HUCS 41466|
|Campyloneurum acrocarpon Fée||T||F||NEO-ATL||I||HUCS 41286|
|Campyloneurum austrobrasilianum (Alston) de la Sota||E||F||NEO-PAR||I, II, III||HUCS 39495|
|Campyloneurum lapathifolium (Poir.) Ching||T/E||F||NEO||I||ICN 152403|
|Campyloneurum nitidum (Kaulf.) C. Presl||T||F||NEO||I, II, III, IV||HUCS 41482|
|Campyloneurum rigidum Sm.||E||F||NEO-ATL||I||PACA 91198|
|Microgramma squamulosa (Kaulf.) de la Sota||T/E||G/F||NEO||I, II, III, IV, V||HUCS 38881|
|Microgramma vacciniifolia (Langsd. & Fisch.) Copel.||T/E||G/F||NEO||I, II, III, IV, V||HUCS 37778|
|Niphidium crassifolium (L.) Lellinger||E||F||NEO||I, II||ICN 143984|
|Niphidium rufosquamatum Lellinger||E||F||NEO||I, II, III, IV||HUCS 38943|
|Pecluma chnoophora (Kunze) Salino & Costa Assis||T||F||NEO-PAR||I||HUCS 41545|
|Pecluma paradiseae (Langsd. & Fisch.) M.G. Price||T||F||NEO-ATL||I, II, III||HUCS 41542|
|Pecluma pectinatiformis (Lindm.) M.G.Price||E||F||NEO-PAR||I, II, III||ICN 168848|
|Pecluma recurvata (Kaulf.) M.G.Price||E||F||NEO-PAR||I||ICN 184455|
|Pecluma robusta (Fée) M. Kessler & A.R. Sm.||T||F||NEO-PAR||I, III||ICN 152424|
|Pecluma sicca (Lindm.) M.G.Price||E||F||NEO-PAR||I, II, III||ICN 184456|
|Pecluma singeri (de la Sota) M.G.Price||E||F||NEO-PAR||I, II, III||ICN 173093|
|Pecluma truncorum (Lindm.) M.G.Price||E||F||NEO-PAR||I||ICN 184452|
|Phlebodium aureum (L.) J.Sm.||E||F||NEO||I, III||ICN 184469|
|Pleopeltis astrolepis (Liebm.) E.Fourn.||E||F||NEO||I, II||ICN 89945|
|Pleopeltis hirsutissima (Raddi) de la Sota||E||F||NEO-PAR||I, II, III, IV, V||HUCS 39386|
|Pleopeltis lepidopteris (Langsd. & Fisch.) de la Sota||T/E||G/F||NEO-PAR||I, II, III, IV||HUCS 41489|
|Pleopeltis macrocarpa (Bory ex Willd.) Kaulf.||E||F||NEO||I, II, III||ICN 178372|
|Pleopeltis minima (Bory) J. Prado & R.Y. Hirai||E||F||NEO||I, II, III, IV||HAS 48577|
|Pleopeltis pleopeltidis (Fée) de la Sota||E||F||NEO-PAR||I||ICN 124179|
|Pleopeltis pleopeltifolia (Raddi) Alston||E||F||NEO||I, II, III, IV, V||ICN 178389|
|Serpocaulon catharinae (Langsd. & Fisch.) A.R. Sm.||T/E||G/F||NEO-PAR||I, II, III, V||ICN 161377|
|Serpocaulon fraxinifolium (Jacq.) A. R. Sm.||T||F||NEO||III||ICN 176740|
|Serpocaulon latipes (Langsd. & L. Fisch.) A.R. Sm.||T||F||NEO-PAR||I, II, III||HUCS 41318|
|Serpocaulon menisciifolium (Langsd. & Fisch.) A.R. Sm.||T/E||F||NEO-ATL||I, II||HUCS 41317|
|Psilotum nudum (L.) P. Beauv.||T/E||G/F||COS||I, II, IV||HUCS 41402|
|Acrostichum danaeifolium Langsd. & Fisch.||T||W||NEO||I, II, III, IV||HUCS 41048|
|Adiantopsis cheilanthoides R.M.Senna||T||G||NEO-ATL||II||PACA 87639|
|Adiantopsis chlorophylla (Sw.) Fée||T||G/F||NEO||I, II, III, IV, V||HUCS 41476|
|Adiantopsis dichotoma (Cav.) T. Moore||T||G/F||NEO-PAR||II||PACA 76701|
|Adiantopsis occulta Sehnem||T||F||NEO-ATL||I, III||PACA 76714|
|Adiantopsis perfasciculata Sehnem||T||G/F||NEO-ATL||II, III||HUCS 41509|
|Adiantopsis radiata (L.) Fée||T||F||NEO||II||HAS 55620|
|Adiantum digitatum Hook.||T||F||NEO||II, III||ICN 170488|
|Adiantum lorentzii Hieron.||T||F||NEO-PAR||I, II, III||HUCS 41278|
|Adiantum pentadactylon Langsd. & Fisch.||T||F||NEO-ATL||I||ICN 161367|
|Adiantum pseudotinctum Hieron.||T||F||NEO-PAR||I||ICN 170491|
|Adiantum raddianum C.Presl||T||F||NEO||I, II, III, IV, V||HUCS 41283|
|Anogramma leptophylla Link||T||F||PAN||III, IV||HUCS 41381|
|Anogramma lorentzii (Hieron.) Diels||T||F||NEO-PAR||II, IV||HUCS 41453|
|Doryopteris concolor (Langsd. & Fisch.) Kuhn||T||G/F||PAN||I, II, III, IV, V||HUCS 41085|
|Doryopteris lomariacea Klotzsch||T||G||NEO||I, II||HUCS 41370|
|Doryopteris lorentzii (Hieron.) Diels||T||G/F||NEO||I, II, III, IV||HUCS 41358|
|Doryopteris nobilis (T. Moore) C. Chr.||T||F||NEO||IV||HUCS 41464|
|Doryopteris pentagona Pic. Serm.||T||F||NEO||I, II, III, IV||HUCS 41470|
|Doryopteris stierii Rosenst.||T||F||NEO-ATL||IV||PACA 78525|
|Doryopteris triphylla (Lam.) Christ||T||G||NEO||I, II||ICN 30816|
|Hemionitis tomentosa (Lam.) Raddi||T||F||NEO||II||ICN 30814|
|Jamesonia osteniana (Dutra) J.G.Gastony||T||F||NEO-PAR||II||HAS 44935|
|Pityrogramma calomelanos (L.) Link||T||G/F||PAN||I, II||HUCS 38768|
|Pityrogramma chaerophylla (Desv.) Domin||T||G/F||NEO||I, II, III, IV||HUCS 41291|
|Polytaenium lineatum (Sw.) Kaulf.||E||F||NEO||I||ICN 89959|
|Pteris brasiliensis Raddi||T||F||NEO||I, II||HUCS 41275|
|Pteris decurrens C. Presl||T||F||NEO||I||HUCS 41277|
|Pteris defexa Link||T||F||NEO||I, III||HUCS 41512|
|Pteris denticulata Sw.||T||F||NEO||I, II, III||HUCS 41477|
|Pteris splendens Kaulf.||T||F||NEO||I, II||ICN 14804|
|Tryonia myriophylla (Sw.) Schuettp., J.Prado & A.T.Cochran||T||F||NEO-PAR||I||ICN 124325|
|Vittaria graminifolia Kaulf.||T||G||NEO||I||HUCS 41534|
|Vittaria lineata (L.) Sm.||E||F||NEO||I, II, III, IV, V||HUCS 42510|
|Azolla filiculoides Lam.||A||W||NEO||I, II, III, IV||HUCS 39104|
|Salvinia auriculata Aubl.||A||W||NEO||I, II, III, IV||HUCS 38703|
|Salvinia biloba Raddi||A||W||NEO||I, II, III, IV||HUCS 41527|
|Salvinia minima Baker||A||W||NEO||II, III, IV||HUCS 41271|
|Actinostachys subtrijuga (Mart.) C.Presl||T||F||NEO||III||ICN 66739|
|Schizaea elegans (Vahl) Sw.||T||F||NEO||I||ICN 66739|
|Selaginella marginata (Humb. & Bonpl. ex Willd.) Spring||T||F||NEO||I, II, III||HUCS 41506|
|Selaginella microphylla (Kunth) Spring||T||F||NEO||I, II||HUCS 67584|
|Selaginella muscosa Spring||T||F||NEO||I, II, III||HUCS 41479|
|Selaginella tenuissima Fée||T||F||NEO-ATL||I||PACA 89923|
|Tectaria incisa Cav.||T||F||NEO||I||ICN 176738|
|Tectaria pilosa (Fée) R.C. Moran||T||F||NEO||I||ICN 176714|
|Macrothelypteris torresiana (Gaudich.) Ching||T||G/F/W||PAN||I, II, III||HUCS 41076|
|Thelypteris abbiattiae C.F. Reed||T||F||NEO-PAR||I, III||HUCS 41117|
|Thelypteris amambayensis Ponce||T||F||NEO-PAR||I, II, III, IV||HUCS 41129|
|Thelypteris berroi (C.Chr.) C.F. Reed||T||F||NEO-PAR||III||ICN 166493|
|Thelypteris conspersa (Schrad.) A.R. Sm.||T||F/W||NEO||I, II, III, IV||HUCS 41116|
|Thelypteris decurtata (Link) de la Sota||T||F||NEO||I, IV, V||HUCS 41115|
|Thelypteris dentata (Forssk.) E.P. St. John||T||G/F||PAN||I, II, III, IV, V||HUCS 41113|
|Thelypteris hispidula (Decne.) C.F. Reed||T||F||PAN||I, II, III, IV||HUCS 41111|
|Thelypteris interrupta (Willd.) K. Iwats.||T||G/F/W||PAN||I, II, III, IV, V||HUCS 41083|
|Thelypteris metteniana Ching||T||F/W||NEO-PAR||I||ICN 170570|
|Thelypteris oligocarpa (Humb. & Bonpl. ex Willd.) Ching||T||F||NEO||I||ICN 126273|
|Thelypteris opposita (Vahl) Ching||T||G||NEO||I||HUCS 38963|
|Thelypteris pachyrhachis (Mett.) Ching||T||F||NEO||I||ICN 172983|
|Thelypteris patens (Sw.) Small||T||F||NEO||I, II, III||ICN 14182|
|Thelypteris ptarmica (Mett.) C.F. Reed||T||F||NEO-ATL||I||HUCS 41118|
|Thelypteris raddii (Rosenst.) Ponce||T||F||NEO-ATL||I, III||ICN 107220|
|Thelypteris recumbens (Rosenst.) C.F. Reed||T||F||NEO-PAR||I, II||ICN 14806|
|Thelypteris regnelliana (C. Chr.) Ponce||T||F||NEO-PAR||I||HAS 43507|
|Thelypteris retusa (Sw.) C.F. Reed||T||F||NEO-ATL||I, II, III||ICN 183474|
|Thelypteris riograndensis (Lindm.) C.F. Reed||T||F||NEO-PAR||I, III||ICN 176183|
|Thelypteris rivularioides (Fée) Abbiatti||T||G/F/W||NEO-PAR||I, II, III, IV||HUCS 41127|
|Thelypteris scabra (C. Presl) Lellinger||T||F||NEO-PAR||I, II||HUCS 41389|
|Thelypteris serrata (Cav.) Alston||T||F||NEO||I, II||ICN 161403|
The gradual decrease in species richness along the Coastal Region was observed for all families, but particularly Polypodiaceae, Pteridaceae, Aspleniaceae and Thelypteridaceae, which represented more than 80% of the reduction. Some families such as Lygodiaceae, Marattiaceae and Tectariaceae were restricted to the extreme north. Others, such as Lindsaeaceae, Hymenophyllaceae, Lomariopsidaceae, Selaginellaceae, Dicksoniaceae and Schizaeaceae, occurred exclusively in the three northern-most latitudinal ranges (Fig. 3). Terrestrial taxa predominated with 162 species (75%), followed by epiphytes with 33 species (12%), while 24 species (10%) exhibited two different habits (epiphytic and terrestrial). Aquatic taxa were represented by four species (7% of total) (Fig. 4). With an increase in latitude, there was an increase in terrestrial species richness and a reduction in epiphytes. At the extreme north, the contingent of terrestrial species reached 70%, while at the extreme South it amounted to 78%, with a reduction of ca. 6% of epiphytic species in the north-to-south direction. Species that exhibited more than one habit were found mostly (80%) in forest environments.
A total of 159 (71%) species occurred exclusively in forest environments, while 26 were found in grassland formations. Some species were found both in forest and grassland habitats (15 spp., 15%). Nine species were present in wetland environments, and an equal number of species occurred in all three environments (forest, grassland and wetland). Blechnum brasiliense, Thelypteris conspersa and Thelypteris metteniana, occurred in forest and wetland habitats, whereas Blechnum schomburgkii and Palhinhaea cernua were found in grassland and wetland environments (Tab. 1). Differences in preference patterns for vegetation formations were identified over the studied profile (Fig. 5), with a decrease of forest species (-40%) and the increase in grassland/forest (+20%) and grassland/forest/wet land (+18%) species in the north-to-south direction.
Taxa with wide global distributions were the most commonly observed with 140 species (63%), of which 113 were neotropical (51%), 17 pantropical, and two (Lycopodium clavatum and Psilotum nudum) cosmopolitan. The species Deparia petersenii and Nephrolepis cordifolia are amphipacific; Osmunda regalis and Osmundastrum cinnamomeum are Holarctic; and Blechnum cordatum, Lophosoria quadripinnata, Hymenophyllum caudiculatum and Equisetum giganteum are Neotropical-Antarctic. Species with restricted distributions represented 37% (83 species) with 44 being Neotropical-Paranaense, 38 Neotropical-Atlantic and one Neotropical-Pampean (Regnellidium diphyllum) (Tab. 1).
Floristic similarity analysis among the five latitudinal ranges revealed two floristically distinct regions in the CRRS: one formed by Ranges IV and V (South center and extreme South) and another formed by Ranges I, II and III (Middle center, North center and extreme North) (Fig. 6). Although they are grouped together, Ranges IV and V had low floristic similarity (53%), as did Ranges I, II and III (41%). Ranges I and II had 70% similarity, while ranges II and III were 73% similar. Only 21 species were common to all areas (Tab. 1).
The species richness observed in this study corresponds to about 36% of the pteridophytic flora listed by Sehnem (1977) for the Southern Region of Brazil and 49% of that listed in Prado & Sylvestre (2015) for the state of Rio Grande do Sul. Most floristic studies on coastal ferns have been restricted to vegetation fragments, parks, conservation units or some specific synusiae (Behar & Viégas 1992; Labiak & Prado 1998; Kersten & Silva 2001; Santos et al. 2004; Dittrich et al. 2005; Athayde Filho & Windisch 2006; Gonzatti et al. 2014b). Despite having an extensive survey area, the richness observed in the present study is lower than that found by other authors in smaller tropical rain and Araucaria forest areas (Mynssen & Windisch 2004; Schwartsburd & Labiak 2007; Salino & Almeida 2008; Prado & Labiak 2009; Gasper & Sevegnani 2010; Souza et al. 2012), all of which were in lower latitudes.
In spite of the existence of a mountain chain (Serra do Mar), which harbors high fern and lycophyte species richness and serves as a corridor connecting the Southeastern and Southern Regions of Brazil (Tryon & Tryon 1982; Windisch 1996), a pronounced floristic reduction is evident between the two regions (Fig. 7). As an example, several fern and lycophyte genera, such as Doryopteris (Tryon 1942), Phlegmariurus (Windisch 1996) and Asplenium (Sylvestre & Windisch 2003), have high species richness and endemism in the Atlantic Forest of southeastern Brazil, but are strongly affected by latitudinal changes and experience a reduction in floristic richness towards the southern sector of the Atlantic Forest. However, the floristic richness found in CRRS is 82% higher than the fern and lycophyte flora of Uruguay further to the south (Legrand & Lombardo 1958; Zuloaga et al. 2008), indicating the continuation of floristic reduction through Uruguay to southern Argentina (Ponce et al. 2002).
In the Neotropics, plant species richness is more strongly correlated with precipitation than edaphic variation (Gentry 1988). In the Atlantic Forest, patterns of floristic change of arboreal vegetation along latitudinal gradients have been attributed to variation in temperature and rainfall distribution. These climatic variables are important in differentiating richness and floristic composition of families, genera and species (Oliveira-Filho & Fontes 2000). The same authors verified that rainfall and temperature increments influence processes of tropicalization and changes in vegetation types, mostly when associated with increased latitude. For Atlantic Forest ferns and lycophytes, variables such as precipitation and evapotranspiration determine plant species composition in distinct vegetation types, as also discussed by Gasper et al. (2013).
Large-scale changes in diversity related to latitudinal gradients have been previously reported for ferns and lycophytes by Moran (2008), with several examples of the concentration of species richness in tropical regions with accentuated decreases towards both poles. According to this author, in South America, particularly in the tropical region, fern and lycophyte richness can reach 2,000 species, while in temperate regions it is only 79 species. Sato (1982) points out that in Japan, species richness decreases with increasing latitude, mostly due to climatic conditions.
Through the southern portion of CRRS, there was a reduction of the floristic richness of most families and genera. In addition to the reduction of fern and lycophyte total diversity, the incidence of species with Neotropical-Atlantic and Neotropical-Paranaense geographical distribution patterns was strongly affected. Taxa that maintain their distributions along the profile (21 spp.) have a wide Neotropical or global distribution (Tab. 1), and their occurrence extends to Uruguay (Legrand & Lombardo 1958; Zuloaga et al. 2008).
The extended distribution of many tropical species in the CRRS can be interrupted by alterations to the north-to-south forest continuity. The transition from tropical rain forest to other vegetation types such as grasslands, peat forests, sandy forests, seasonal forests and riparian habitats (Waechter 1990) can affect distribution patterns and inhibit dispersal of ferns and lycophytes. In Rio Grande do Sul, tropical rain forest reaches its southern limit at the 30º S parallel in the region of Osório - RS (Rambo 1951; 1954; Lorscheitter 2003). These formations develop on the extreme southern slopes of the "Serra do Mar" and on the eastern face of "Serra Geral". Due to the climatic conditions of temperature and precipitation, as well as the environmental heterogeneity of vegetation and substrates, the development of larger forests with tropical species are allowed, as is the dispersal of northern floristic components (Rambo 1951; Klein 1984; Waechter 1985; Waechter 1990). These characteristics of environment heterogeneity are fundamental to increasing fern and lycophyte diversity in the Atlantic Forest (Windisch 1992; Dittrich et al. 2005), and they were not observed in CRRS Ranges III, IV and V.
Phytogeographically, the latitude 30º S defines the limit between the Atlantic and Paranaense provinces where pluvial and subtropical forests (Atlantic Forest) find their southern limit, and are gradually replaced by herbaceous elements of the Pampa biome (Cabrera & Willink 1980). Sota (1973) considers that the Pampa, along with the Chaco, are barriers separating the center of fern and lycophyte diversity in southern Brazil from the Argentinian and Chilean centers of diversity. According to Prado & Hirai (2014), the Pampa biome is the poorest in fern and lycophyte diversity, with only 0.5% of the floristic richness found in the Atlantic Forest.
This same reduction in diversity has been reported previously by other authors. Rambo (1950; 1951; 1954; 1956) observed structural and floristic modifications to vegetation along the Coastal Region, attributing the decrease in species richness to the dispersal processes that occurred throughout the region he referred to as "Porta de Torres" ("Torres migrational gate"). This latitudinal gradient was later observed by Waechter (unpublished data) in a study of vascular epiphytes, who found a 93.7% reduction in richness between latitudinal Range I and Range V. In his work with epiphytic orchids, Waechter (1998) found that there is a total reduction in species richness along the CRRS, a 88% reduction between Range I and Range II, and that no species reached south of parallel 33° S. Of the 61 genera he studied, only four are found in Uruguay and one in the province of Buenos Aires (Argentina).
Among the factors that influence floristic change in the north-to-south direction of the CRRS, Waechter (1990) highlights climatic discontinuity along the region. The author noted that the decrease in rainfall and temperature going south causes an increase in the number of cold days and annual frost events. This, in turn, results in changes to vegetation communities, causing insularization and discontinuity of the arboreal component, thus interfering in the dispersal routes of tropical plant species.
Although a strong floristic discontinuity has been reported for the region of parallel 30° S (Waechter 1990; 1998), our data indicate that for ferns and lycophytes this discontinuity occurs mostly from parallel 31° southwards (Fig. 7), where a reduction in species richness and the differentiation of the floristic elements in Ranges I, II, and II vs. Ranges IV and V were observed. These results can be associated with the high dispersal capacity of fern and lycophyte spores, thereby finding niches with favorable conditions for their establishment and reproduction (Tryon 1970; Wolf et al. 2001), or simply forest connections (present and past) that allowed for a broader distribution.
Our results indicate that more species occur in more than one environment (forest/grassland or forest/grassland/wet land) with increasing latitude, and that there is a decrease of strict forestalls. The strong dependence of ferns on forest environments can be related to the group's evolutionary history, which suggests that 80% of current ferns evolved in forest environments after the angiosperm radiation ca. 100-65 mya (Schneider et al. 2004).
Another north-to-south floristic change in the CRRS can be seen in the reduction of epiphytic species in Range V with the concomitant prevalence of terrestrial species (Fig. 5). Beyond the need for adequate ecological conditions (Sota 1971; Benzing 1987), there is the requirement of host plant availability for the establishment of epipytic species (Waechter unpublished data).
Some species restricted to Range I, such as Vandenboschia radicans, Lomariopsis marginata, Mickelia scandens, Polybotrya cylindrica, Olfersia cervina, are hemiepiphytes, that begin development on the ground and later climb host plants. These species are extremely dependent on environments with high levels of humidity such as is found in the interior of forests without edge effects and external light incidence (Orihuela & Waechter 2010; Orihuela et al. 2013).
Decreased amounts of rainfall and the existence of a drier season in the extreme south can limit the establishment and development of fern and lycophyte flora. Ranal (1995a) points out that fern spore germination, as well as the development of the gametophyte and sporophyte, are strongly affected by desiccation. In experiments focusing on survival, Ranal (1995b) shows that 30% of fern gametophyte deaths are due to desiccation. Watkins et al. (2007) demonstrated that the gametophytes of xerophytic species, as well as epiphytic and some terrestrial species, are better adapted to survive conditions of scarce water, contrary to mesophytic species, which cannot undergo periodic variations in their water content.
Other features inherent to the reproductive success of many ferns and lycophytes can be decisive in their establishment in particular habitats. Although this group of plants is capable of dispersing spores over long distances (Holttum 1938) and can form spore banks in the ground (Ranal 2003), the spores may not encounter the microclimatic (temperature, humidity and luminosity) and biotic conditions (mycorrhizal associations) needed for germination (Williams 1938; Sheffields 1996). Furthermore, gametophytes, even when possessing adaptations to desiccation and variable conditions of pH, soil nutrition, temperature and luminosity (Farrar et al. 2008), can suffer from insufficient availability of free water in the environment, which in and of itself can be a limiting factor to their establishment. Despite the fact that some fern species have strategic adaptations for independent gametophytic reproduction (apogamy, clonal reproduction by gemmae, pH metamorphosis) the presence of water is still a requirement for the successful sexual reproduction of the gametophyte of most fern and lycophyte species (Page 2002). According to Holttum (1938), the majority of fern and lycophyte spores germinate in forest environments, and to occupy other environments with adverse conditions they need specific adaptations.
The occurrence of ferns in wetland and grassland environments is also related to expansion of these vegetation formations in the north-to-south direction, with the expansion of water bodies in wetland-region lagoons and natural grasslands most frequent in Range V. For example, Blechnum brasiliense has adapted to a variety of environments that differ in their edaphic composition, vegetation formations and microclimate conditions (Silva et al. 2013).
Data compiled by Nimer (1990) and Moreno (1961), point out clear differences in the climatic patterns of the two extremes of CRRS. According to these authors, the average annual precipitation can be up to 300 mm/year lower and the average temperature about 2ºC lower in Range V. Furthermore, the average number of days with frost increases from three to 15 days in the extreme south (Range V). This southern, more temperate climate can explain the presence of species with Neotropical-Antarctic or Holarctic distribution patterns in the floristic composition of Range V, such as Osmunda regalis and Equisetum giganteum.
Studies published by Bremer & Jongejans (2010) on the population dynamics of Asplenium scolopendrium show the negative effect of frost on the survival and, consequently, the retrogression of this species. According to these authors, frost affects fern sporophytes in three ways: direct mortality by freezing caused by wind, soil freezing, and hydric unavailability caused by ice. In populations submitted to 22 continuous days with frost, mortality reached 38%. In order for this species to occur in these regions of low temperatures and frost, adaptations at all development stages are required. In several cases phenological changes take place that permit survival and ensure the reproductive success during cold periods (Sato & Sakai 1980; Sato & Sakai 1981; Sato 1982).
Although the best temperatures for spore germination and gametophyte growth are generally considered to be between 20° and 30°C (Miller 1968), various exceptions have been observed. In northeastern United States, gametophytes of the genus Vittaria Sm. can become established in certain environments, form extensive populations through asexual reproduction by apogamy and persist during prolonged frost while the sporophytes do not survive, dying at the beginning of their development (Farrar 1978). These reports were also corroborated by Sato & Sakai (1980) for many Asiatic species, where the gametophytic phase can resist temperatures below -40°C, while their sporophytes do not survive in temperatures below 0°C. This limiting factor can be associated with the decrease of species richness (at least in the sporophyte phase) in the extreme south of CRRS, where the species are more adapted to such conditions, such as Osmundastrum cinnamomeum whose sporophyte can resist -10°C (Sato 1982).
Sehnem (1977) suggested that the low richness of ferns and lycophytes in some regions of the state of Rio Grande do Sul is influenced by the reduced amount of time for the migration of additional species (recent paleogeographic evolution) and, consequently, the limited distribution of these species in the extreme south. This phenomenon may explain the decrease of fern and lycophyte species in the temperate floras of the "Southern Cone", which can have three to four times fewer species than tropical floras such as in southeastern Brazil (Ponce et al. 2002).
The impoverishment of the extreme southern flora of CRRS may also be related to past paleoenvironmental conditions. Paleogeographic and palynological evidence point to the existence of an arid climate and the prevalence of grassland vegetation across southern Brazil that persisted at least until the beginning of the Holocene, when the migration of the tropical vegetation of southeastern Brazil to CRRS started (Ab'Sáber 1977; Ledru et al. 1998; Lorscheitter 2003).
Rising humidity patterns in the past 4,000 years show the expansion of fern and lycophyte communities in "Laguna dos Patos" (Middle center of the Coastal Region) (Lorcheitter 2003 ), which could not have occurred in the extreme South, due to climatic conditions. Recent palynological data from the Holocene period (Masetto & Lorcheitter 2014) establish the presence of taxa currently not found in the region, indicating alterations in the current floristic composition, or in the process of long distance dispersal.
The most striking outcome of our study was the high floristic richness present in the Coastal Region of the state of Rio Grande do Sul and the high reduction in species richness of ferns and lycophytes along the north-south extremes of RCRS. There are a variety of factors, including climatic limitations, dynamic phytogeography and the biology of ferns and lycopods themselves that have been considered in explaining these observations.