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Original Paper • Rodriguésia 72 • 2021 • https://doi.org/10.1590/2175-7860202172074 linkcopy

Open-access Fern and lycophytes of the Taquari River riparian forests at different stages of succession

AuthorshipSCIMAGO INSTITUTIONS RANKINGS

    Abstract

    Riparian forests are important biodiversity corridors among groups. Such forests were greatly altered or suppressed in the state of Rio Grande do Sul. This study investigates the variation of species richness and distribution of ferns and lycophytes of eighteen study areas at different stages of succession in riparian forests of the Taquari River region. Fern and lycophyte samples were collected using the pathway methodology along the Taquari River during two years. The richness was compared at the different succession stages (advanced remnant formations, intermediate and initial) through analysis of variance and a randomized test, in which about 22 species were recorded: 19 species were at the advanced stage of succession, nine species were at the intermediate stage and seven species were at the initial stage of succession. The average richness was significantly higher in areas at advanced stage of succession. The high value of common species found at intermediate stages highlights the importance of preserving riparian forests at all stages of succession in the Taquari River as alternative for preserving the local biodiversity.

    Key words conservation; disturb; environment; pteridophytes; species richness; Subtropical Atlantic Forest

    Resumo

    As matas ripárias são importantes corredores de biodiversidade entre os grupos. Essas florestas foram muito alteradas ou suprimidas no estado do Rio Grande do Sul. Este estudo investiga a variação da riqueza de espécies e distribuição de samambaias e licófitas de dezoito áreas de estudo em diferentes estágios de sucessão em matas ripárias da região do rio Taquari. Amostras de samambaias e licófitas foram coletadas utilizando a metodologia de caminhamento ao longo do rio Taquari durante dois anos. A riqueza foi comparada nos diferentes estágios de sucessão (formações remanescentes avançadas, intermediárias e iniciais) por meio de análise de variância e um teste randomizado, no qual foram registradas cerca de 22 espécies: 19 espécies estavam em estágio avançado de sucessão, nove espécies estavam no estágio intermediário e sete espécies estavam em estágio inicial de sucessão. A riqueza média foi significativamente maior nas áreas em estágio avançado de sucessão. O alto valor das espécies comuns encontradas nos estágios intermediários destaca a importância da preservação das matas ripárias em todos os estágios de sucessão do rio Taquari como alternativa para preservação da biodiversidade local.

    Palavras-chave conservação; distúrbio; meio ambiente; pteridófitas; riqueza de espécies; Mata Atlântica Subtropical

    Introduction

    Riparian forests are vegetation around watercourses such as rivers, lakes, springs, and streams. They play an important role in protecting and maintaining riverbeds and local biodiversity (Chaves 2009), functioning as biological corridors and maintaining water quality in rivers. For the protection of watercourses, such forests act as intermediary between agricultural areas and aquatic environments by reducing negative impacts on the fauna and flora. Furthermore, they contribute to maintenance of soil porosity by favoring the infiltration of rainwater and the groundwater supply (Pessoa et al. 2000).

    Despite its recognized importance in urbanized areas (Dias et al. 2014), riparian forests are negatively affected mainly by human occupation in the vicinity of such environments (Martins 2007). In rural areas, degradation is mainly due to a disordered agricultural expansion (Rodrigues & Gandolfi 2000). Riparian forests are systems particularly fragile to erosion, watercourse sedimentation and other impacts caused by humans mainly for being located at the bottom of valleys (Van Den Berg & Oliveira-Filho 2000). Those sites have the most fertile soils, thus, being preferred for agriculture development and making riparian forests potentially more threatened (Mencacci & Schlittler 1992; Van Den Berg & Oliveira-Filho 2000).

    Studies on riparian forests have pointed out heterogeneous characteristics in their structure, composition, and dynamics (Ribeiro-Filho et al. 2009) related to several factors, such as edaphic and topographic variations, surrounding vegetation, history of disturbances, among others, which define differentiated ecological conditions (Durigan et al. 2000). Considering Brazilian rainforests, several studies have shown that the local distribution and diversity of ferns and lycophytes may be associated with several factors, including structural changes to the forest (Paciencia & Prado 2004, 2005; Nóbrega et al. 2011), and microclimatic (Paciencia & Prado 2004; Rodrigues et al. 2004) or edaphic-topographic features (Costa et al. 2005; Zuquim et al. 2007, 2009; Nóbrega et al. 2011; Nervo et al. 2019). According to Weigand et al. (2019), the richness of ferns and lycophytes is most strongly impacted at plot level or sampling point by local environmental factors.

    Despite the taxonomic advance regarding this group in Rio Grande do Sul (e.g., Sehnem 1967a, b, c, d, 1968a, b, 1970a, b, 1971, 1972, 1974, 1978, 1979a, b, c, d, e, f, g, 1984; Nervo & Windisch 2010, among others), fern and lycophyte species in riparian forests are not completely known. Few studies have contributed to their understanding (Diesel & Siqueira 1991; Mallmann & Schmitt 2014). There is a lack of floristic and ecological studies evaluating their composition. Moreover, surveys of local fern and lycophyte flora in forest fragments at different stages of succession may provide important information on environmental ecosystems conditions and help with conservation and exploitation of natural resources in such locations (Gonzatti 2018).

    In this study, we performed a floristic fern and lycophyte survey in eighteen fragments of riparian forests of the Taquari River, Rio Grande do Sul state (RS), Brazil, which belongs to the Taquari-Antas river basin. In addition, we analyzed the relations between species composition and different stages of succession. Our hypothesis is that the species composition change between successional stages and areas at advanced stages of succession have greater richness of ferns and lycophytes. Thus, upon verifying the composition of species at different stages of succession, this study seeks to answer the following questions: (1) what is the composition of ferns and lycophytes in Taquari River riparian forests? (2) How does species richness of riparian forests vary at different stages of succession? (3) Are there species restricted to particular stages? (4) How do floristic similarities vary at different stages of succession?

    Materials and Methods

    Study area

    This study was conducted on the banks of the Taquari River, which belongs to the Taquari-Antas River basin (BHRTA). It is located in the Northeast Region of the state of Rio Grande do Sul between the municipalities of Muçum and Taquari (Fig. 1). We selected eighteen study areas at different stages of ecological succession according to the Classification of the National Environment Council (CONAMA) (Brasil 1994): six areas were at an initial stage of forest succession (INI), measuring between 20 and 25 meters wide and 100 and 200 meters long, with a history of less than three-year use by agropastoral activities, and considered the most disturbed areas in our study. Six areas were at an intermediate stage of succession (INT), with 10 and 20 meters wide and 280 and 860 meters long, and other six areas at a late (advanced) stage of succession (LAT), measuring 70 and 150 meters wide and 280 and 1,000 meters long. The study area is inside the Atlantic Forest biome, and the vegetational type is Deciduous Seasonal Forests. The soil is characterized by a complex association of Eutrophic Litholic soils (IBGE 2017). According to the Köppen classification, the regional climate is humid subtropical (Cfa) (Alvares et al. 2013). The region’s annual rainfall is about 1,300–1,400 mm, and the average annual temperature is 19–20 °C (66 to 68 °F), varying between the warmest and the coldest months (see details in Tab. 1).

    Figure 1
    Map of eighteen study areas of the Taquari-Antas River Basin. Created by Gabriela Reis-Avila.
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    Table 1
    Characteristics of the different study sites in remnants of the Taquari-Antas River Basin in Rio Grande do Sul state, Brazil, in three forest sucession – INI = initial stage of forest succession; INT = intermediate stage of forest succession; LAT = late stage of forest succession. AP = Annual Precipitation; MAT = Mean Annual Temperature.

    Data collection

    The floristic survey was performed through unsystematic hiking in the areas (Filgueiras et al. 1994). All ferns and lycophytes were sampled from October 2012 to December 2014. Species identification was carried out using specialized bibliography, through expert consultation and comparison with herbaria species. The material was deposited at the HVAT Herbarium of the Museum of Natural Sciences of the Universidade do Vale do Taquari - Univates. Families and genera were classified according to PPG I (2016), and we chose to follow the International Plant Name Index (IPNI). In each study area, all species of fern and lycophyte were estimated considering three habits and based on the occupied substrate (by Nervo et al. 2016): terrestrial (species with roots in the soil), rupicolous (species that grow in rocks) and epiphytes (species that grow on tree trunks up to 2 meters), as it was performed by Tuomisto & Ruokolainen (1994).

    To identify differences between species richness for each successional stage of the riparian forest, richness data were compared between the three successional stages by analysis of variance (ANOVA) with a permutation testing (Pillar & Orlóci 1996). To evaluate habitat specificity, we compared common and exclusive species at different areas of different successional stages (INI, INT and LAT) using Venn diagram (Oliveros 2007). We considered common species those occurring in two or more fragments with different successional stages, and as exclusive species those occurring only one type of successional fragment of different stages forest. Differences in species composition among sites were tested using Non-metric multidimensional scaling (NMDS), with Bray-Curtis index as distance measure. The similarity of floristic composition at different successional stages was analyzed by the Sørensen Index of Similarity. The composition similarity of ferns and lycophytes on each study area was compared by the Bray-Curtis index using the Ward method. Values of co-phenetic relationship of the cluster above 0.7 were adopted as satisfactory correspondence indicator (Visnadi & Vital 2001). The analyses were performed using the MULTIV (Pillar 1997), Paleontological Statistic (PAST) (Hammer et al. 2003), and the R software (R Development Core Team 2013).

    Results

    We sampled 22 species were sampled in the riparian forests of the Taquari River. They belong to eight families and thirteen genera (Tab. 2). The most representative family was Pteridaceae (seven species), followed by Aspleniaceae (four species), and Thelypteridaceae and Polypodiaceae (three species, each family). Among the less representative families, Anemiaceae stands out with two species, followed by Blechnaceae, Lomariopsidaceae. And in the lycophytes, Selaginellaceae stands out with a single species. The four most representative families corresponded to 77% of sampled species.

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    Table 2
    Fern and lycophyte species occurring in Taquari-Antas River drainage base, with indication of – ST = substrat types; e = epiphyte; r = rupicolous; t = terrestrial; INI = initial stage of forest succession; INT = intermediate stage of forest succession; LAT = late stage of forest succession; HVAT = voucher number.

    Nine species were found in both terrestrial and rupicolous habitats (Tab. 2). According to the Species List of the Brazilian Flora, 21 species recorded are native (Flora do Brasil 2020, under construction). The only species regarded as non-native, naturalized and sub-spontaneous was Macrothelypteris torresiana, which belongs to the family Thelypteridaceae (Tab. 2) (Flora do Brasil 2020, under construction).

    The remnants at the advanced succession stage showed the greatest species richness (19), followed by the remnants at the intermediate successional stage (nine species) and at the initial stage (seven species) (Tab. 2).

    The average species richness was significantly different (Q = 59.11; p = 0.03) between the stages of succession. Formations at the advanced (late) stage showed significantly higher average richness (5.6 species) than those at the early stage of succession (1.66 species). In turn, formations at the intermediate sucessional stage showed average richness similar to those in the other areas.

    Four species of those recorded occurred at all stages of succession (Adiantum raddianum, Anemia phyllitidis, Doryopteris pentagona, Selaginella muscosa), while 13 species were unique only to one type of area (Fig. 2). Formations at the late successional stage had the highest number of exclusive species (ten) (Tab. 2), followed by those areas at intermediate stage of succession (three species). No exclusive species was recorded in areas at the initial successional stage. Riparian forests at late and initial succession stages were more similar in terms of floristic composition than those at intermediate succession areas, as evidenced by the Sørensen Index mean value calculated for all pairs of areas (Tab. 3).

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    Table 3
    Floristic similarity of ferns and lycophytes in three formations forest in different sucession stage in the remnants of the Taquari-Antas River Basin, in Rio Grande do Sul state, Brazil, indicated by the Sørensen Index. INI = initial stage of forest succession; INT = intermediate stage of forest succession; LAT = late stage of forest succession; IHM = internal heterogeneity measure (= Sørensen index calculated for all pairs of areas within one formation).
    Figure 2
    Venn diagram – number of shared and exclusive species among the three succession stages. Succession stages: INI = initial stage of forest succession; INT = intermediate stage of forest succession; LAT = late stage of forest succession.

    The Non-metric multidimensional scaling ordination (NMDS, Fig. 3) using species composition did not indicate a clear separation among the three forest successional stages in remnants of the Taquari-Antas River basin (co-phenetic relationship > 0.9). This result was also observed for floristic similarity (Bray-Curtis index) shown in Figure 4, using the composition of each study areas. The areas 8, 11, 12 e 17 formed an external group in the analysis. The study areas numbered two and six showed a hundred percent in the floristic similarity. The lowest floristic similarity was in the study area number one.

    Figure 3
    NMDS analysis (Stress = 16.1) performed for samples of ferns and lycophytes collected in 18 study areas, occurring in environments of initial succession (circle) and intermediate succession (triangle) and late succession (square) in riparian forests of the river Taquari region, Rio Grande do Sul, Brazil.
    Figure 4
    Similarity dendrogram by the UPGMA algorithm, based on the Bray-Curtis Index (group co-phenetic correlation > 0.9) for the species of ferns and lycophytes sampled in 18 study areas, occurring in the environments of initial stage of forest succession (1 to 6); intermediate stage of succession (7 to 12) and late stage of succession (13 to 18) in riparian forests of the Taquari River region, Rio Grande do Sul, Brazil.

    Discussion

    The number of recorded species for the region studied agrees with that generally found in riparian forests in the Atlantic Forest (Diesel & Siqueira 1991; Mallmann & Schmitt 2014; Padoin et al. 2015). When compared to the other studies of Rio Grande do Sul state, the total richness of ferns and lycophytes found in the Taquari River riparian forests (22 species) is similar as that recorded by Diesel & Siqueira (1991) in the Sinos River riparian forests (24 species), and lower than that found by Mallmann & Schmitt (2014) in three fragments of the Cadeia River riparian forest (with 0.3 ha sampled), i.e., forty species.

    The high species richness observed in Pteridaceae corroborates that observed by Gonzatti et al. (2014), who evaluated the deciduous forests remnants of the state of Rio Grande do Sul, Brazil. The vast area for occurrence of this family as an element for greater floristic richness is contradictory if compared to other studies surveying seasonal stationary or rain forests, in which Polypodiaceae was the richest family (Steffens & Windisch 2007; Santos & Windisch 2008; Nervo 2012). Doryopteris J.Sm. was the genus with the highest richness recorded, i.e., four species. The high number of species of Doryopteris in the study region draws attention to the presence of potentially suitable environments for the development of this genus.

    We observed a significant tendency of high species richness at more advanced stages of plant succession. The highest and most significant average species richness was observed in the late succession stage. According to Custódio et al. (2015), late forests generally have wider and more intact margins. Thus, the continuous flows of streams make margins safe by increasing the diversity of habitats with appropriate conditions for establishment of different fern and lycophyte species. As stated by Miguez et al. (2013), the increase in environmental heterogeneity favors the increased diversity of fern and lycophyte species. Such formations generally have greater diversity in soil drainage capacity, a thicker surface (concentration of sand in the soil), and higher contents of organic carbon and nitrogen (Galindo 2008).

    Additionally, it is well known that ferns can persist and compete for nutrients on sites with varying fertility (Nervo et al. 2019). This behavior can drive the variation among species and help to determine how species are distributed across landscapes (Callaway 2007; Grime 2002; Nervo et al. 2019). Furthermore, one study by Hack et al. (2005) indicated that areas at advanced (or late) stage of succession usually have a uniform distribution of individuals in a specific occurrence.

    Most species (60%) had a restrict ecological range (Fig. 2). They were observed in only one type of successional stage or one study area (for example, Doryopteris nobilis was present in only one late formation area), while some species (18%) occurred in more than one stage of succession with wide distribution. In contrast, the predominance of some species extensively throughout the studied areas, such as Anemia phyllitidis (occurring in 50% of the surveyed areas), Adiantum raddianum (34%), Doryopteris pentagona and Selaginella muscosa (both with a 28% occurrence), corroborate the results of Nervo et al. (2010), who recognized them as species of wide distribution in the state of Rio Grande do Sul with tolerance to several different environments (Nervo et al. 2016).

    According to Michelon & Labiak (2012), Anemia phyllitidis can be found inside forest formations whose substrate is earthy and rupicolous, being common in riparian forest areas of the Iapó River in Paraná. Mynssen & Windish (2004), studying forests in the Atlantic Forest of Rio de Janeiro, stated that the A. phyllitidis growth may be related to shaded environments or to greater exposure to sunlight, facilitating a widespread occurrence. In a study conducted by Schwartsburd & Labiak (2007), the authors recorded A. phyllitidis inside an Araucaria Forest, riparian forests and silviculture (Pinus sp. and Eucalyptus sp.) in Paraná. In this study, Adiantum raddianum was observed on a rupicolous soil substrate. According to Michelon & Labiak (2012), A. raddianum inhabits rocks alongside waterfalls and waterways within gallery forests. Doryopteris pentagona is often reported as terrestrial species within forest formations and anthropogenic environments (Michelon & Labiak 2012; Nervo et al. 2010). The frequent recording of Selaginella muscosa in the study areas may be related to the presence of humid and shaded environments (Mynssen & Windisch 2004) and the desiccation-tolerant ability of this species (Mehltreter et al. 2010). In addition, Selaginella, Adiantum and Anemia species have wide ecological and geographic distribution (Gonzatti et al. 2014), justifying the occurrence of species of genera in all areas.

    Unlike expected, the NMDS calculated for all study remnants showed no distinct pattern among the three forest successional stages. This result is also supported by the those of floristic similarity (Bray-Curtis index) shown in by Figure 4. The species present at the initial stage of forest succession share their occurrence with remnants of at the intermediate and late stages of succession. Initial and late stages are more similar according to species composition than to intermediate stages (Tab. 3). Therefore, not only late stages are important for species conservation, but also intermediate stages, which present a similar richness as late stages, but a more dissimilar species composition compared to initial stages. For ferns and lycophytes, the degradation of riparian forests and the changes in springs and watercourses caused by human activities are among the main threats.

    Seven species were observed at initial successional stages (Tab. 2). In our study, we observed that these species develop in environments strongly disturbed by human action. Anemia phyllitidis, Doryopteris pentagona, and Macrothelypteris torresiana are species with ruderal behavior, and quick to establish themselves in anthropized environments. Adiatum raddianum, Goniopteris riograndensis, Pteris brasiliensis and Selaginella muscosa were observed distributed close to the water streams, in places with higher soil moisture. None of them occurred exclusively in this formation. According to Walker & Sharpe (2010), ferns and lycophytes are sensitive to changes in environment, which affects their establishment, growth and reproduction in certain areas (Walker & Sharpe 2010). Most species are water-dependent for requiring high moisture level to grow and reproduce (Barrington 1993). Therefore, the recent disturbances in such initial succession areas may have considerably changed the structure of initial succession fragments, to which few species have specific adaptations to establish themselves in the environment.

    We must also consider the natural disturbance of the areas at initial succession, since water disturbance remains as a factor, considering that the study areas are riverbanks. Comparisons of floristic similarities among formations, as valued by the Sørensen Index (initial versus intermediate, initial versus late, intermediate versus late), evidenced a moderate floristic similarity (Tab. 2). The floristic proximity observed between late and early succession formations (54%) is related to the common distribution of three species (Macrothelypteris torresiana, Pteris brasiliensis and Christella hispidula), which have a wide distribution in Rio Grande do Sul (Lorscheitter et al. 2001; Nervo et al. 2010). These species, which have greater survival adaptability, establish themselves at initial successional formation and may remain for years within the community, forming extensive populations and contributing to the process of secondary and late succession. On the other hand, the presence of alien species (Macrothelypteris torresiana) can be a negative indicator of competition and replacement of native species.

    Knowledge of biodiversity in degraded fostered areas by floristic inventories provides key information for advanced studies in taxonomy, ecology, phytogeography, conservation, and reforestation of degraded areas (Souza et al. 2009; Nervo 2012). For the group of ferns and lycophytes, the degradation of riparian forests and changes in springs and watercourses caused by human activities are among the main threats. It is worth mentioning that areas at late stage of succession have more than three times as many exclusive species as those at initial successional stages. Thus, the importance of preserving riparian forests of the Taquari River becomes evident for also preserving the local biodiversity.

    Continuous government actions that act in synergy with scientific actions are essencial to improve biodiversity knowledge, to promote conservation, and control biodiversity loss (Dias 2017; BFG 2018).

    Acknowledgments

    The authors are grateful to FAPERGS, for its support to the project “Strategies for the Restoration of Riparian Forests of the Taquari River Basin” (project nº 12/0014-0); to EMF; and to the grant awarded to FB. MHN thanks the PhD scholarship by CAPES. We would like to thank the “Federal University of Rio Grande do Sul” (UFRGS) and the “Postgraduate Program in Botany”, for allowing using their facilities. We would like to thank the owners of the areas who allowed access to study sites and to fellows and volunteers who collaborated in field activities.

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    Edited by

    • Area Editor: Dra. Thaís Almeida

    Publication Dates

    • Publication in this collection
      20 Sept 2021
    • Date of issue
      2021

    History

    • Received
      10 Dec 2019
    • Accepted
      04 June 2020
    Creative Common - by 4.0
    This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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