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Abstract

The “Alto da Serra de Paranapiacaba” Biological Reserve (RBASP) was created in 1909 and was the first protected area in the category of Biological Reserve in South America. We conducted samplings in large uncollected areas, considering different phyto-physiognomies, and reviewed all the bryophyte material deposited in the SP herbarium. We identified 423 species, representing the three divisions: 217 corresponding to liverworts, 203 to mosses, and three to hornworts. The Lejeuneaceae family presented the highest richness (97 species). Within the mosses, Sematophyllaceae stood out with 22 species, and hornworts were represented by three species. We recorded 46 species for the first time in the state of São Paulo. Fifty species are endemic to Brazil, of which 35 are restricted to the Atlantic Forest. Field collections yielded 78 new records for the Reserve. Our study of bryophytes is the most extensive for the locality in over a century. Therefore, the data presented here can serve as a basis for future taxonomic and ecological research on bryophytes in the Reserve.

Key words:
Atlantic Forest; floristic survey; liverworts; long-term sampling; moss

Resumo

A Reserva Biológica do Alto da Serra de Paranapiacaba (RBASP) foi criada em 1909 e foi a primeira área protegida na categoria de Reserva Biológica na América do Sul. Realizamos coletas em grandes áreas não coletadas com diferentes fitofisionomias e revisamos todo o material do grupo depositado no herbário de SP. Identificamos 423 espécies de briófitas com as três divisões representadas, sendo 217 espécies de hepáticas, 203 espécies de musgos e três espécies de antóceros. Lejeuneaceae foi a família com maior número de espécies, 97 spp. Dentro dos musgos, as Sematophyllaceae se destacaram com 22 espécies e os antóceros estavam representados por três espécies. Registramos 46 espécies pela primeira vez no estado de São Paulo. A Reserva possui 50 espécies endêmicas do Brasil, destas, 35 estão restritas à Mata Atlântica. As coletas de campo resultaram em 78 novos registros para a Reserva. Nosso estudo sobre briófitas é o mais extenso para a localidade em mais de um século. Os dados aqui apresentados podem, portanto, servir de base para futuras pesquisas taxonômicas e ecológicas sobre briófitas na Reserva.

Palavras-chave:
Floresta Atlântica; levantamento florístico; hepáticas; amostragem de longo prazo; musgos

Introduction

The “Alto da Serra de Paranapiacaba” Biological Reserve (RBASP) was created in 1909 by the physician and naturalist Hermann Friedrich Albrecht von Ihering, director of the “Museu Paulista”. In 1913, it was transferred to the São Paulo state government and was the first protected area in the category of Biological Reserve in South America. The RBASP is located between the Atlantic Plateau and the Serra do Mar, making it the only reserve near the coast of São Paulo. It covers 336 ha with vegetation of the Atlantic Forest in a secondary stage, with different variations, such as shrubs, pastures, and less dense and more fragmented forest stretches, with a more open and drier interior and canopies that reach lower heights compared to more preserved areas (Sugiyama et al. 2009). Some stretches of anthropized areas with atmospheric pollution are also observed due to industrial activities near the RBASP in the 1980s and the illegal extraction of wood and ornamental and medicinal plants (Domingos et al. 2009; Kirizawa et al. 2009; Lopes & Kirizawa 2009).

Since its foundation, the floristic diversity and richness in RBASP have been the object of fascination and studies by researchers from different countries (Lopes & Kirizawa 2009; Sugiyama et al. 2009). Because it is a fully protected Nature Conservation Unit, all human activities in the RBASP are prohibited except for previously authorized scientific studies (Brasil 2000). According to Yano et al. (2009), studies on bryophytes began with a list of 25 species by Herzog (1925). Subsequently, Hell (1969) listed 20 thalloid liverwort species, and Giancotti & Vital (1989) reviewed Schiffner & Arnell’s list (1964) and cited 30 species of thallose liverworts and 20 Lejeuneaceae species, respectively. Rebelo et al. (1995) used mosses and liverworts as bioindicators of environmental pollution in this region. In 2009, Yano et al. reviewed the literature and the specimens from RBASP deposited at SP Herbarium and listed 247 species, although the authors did not provide vouchers.

Bryophytes are the oldest extant group of plants (Puttick et al. 2018; Bechteler et al. 2023), dating back to the Cambrian period (Harris et al. 2022; Woudenberg et al. 2022; McCourt et al. 2023). They constitute the second largest known plant group (Hallingbäck & Hodgetts 2000; Goffinet et al. 2009; Konrat et al. 2010), with 24,000 cataloged species (Frahm 2003; Qing-Hua et al. 2022). Phylogenetic studies have shown that bryophytes are monophyletic and are formally classified into three Divisions, distributed within two clades: the clade Setaphyta including Marchantiophyta and Bryophyta, and a second clade with the Division Anthocerotophyta (Cole et al. 2019; Delaux et al. 2019; Harris et al. 2020; Li et al. 2020; Souza et al. 2020; Harris et al. 2022).

They are present in all ecosystems except the marine one, with a high diversity and endemism in tropical forests (Pócs 1982; Delgadillo 1994), where they play an active and significant ecological role (Gradstein et al. 2001; Costa & Lima 2005; Oliveira & Bastos 2014) in stabilizing and forming moist soil that helps other vascular seedlings develop later (Bahuguna et al. 2014; Glime 2021). Bryophytes increase fixed nitrogen rates and photosynthesis in tropical forests’ epiphytic communities (Cara et al. 2018; Lai et al. 2020; Markham & Otárola 2021). Bryophyte biomass can intercept rainfall and accumulate organic matter in bogs and peatlands (Glime 2021; Vitt & House 2021).

Bryophyte communities, due to their sensitivity to microclimate shifts, can serve as excellent bioindicators of environmental quality (Acebey et al. 2003; Frahm 2003; Oliveira & Oliveira 2016) and detectors of pollutants (Govindapyari et al. 2010; Mazzoni et al. 2012; Barbosa & Carvalho 2016; Souza et al. 2017). They are pioneers in colonizing and regenerating degraded areas (Silva Filho 1988; Bononi 1989; Costa 1999; Oliveira-e-Silva et al. 2002; Rossi et al. 2009), playing a crucial role in nutrient cycling and local biodiversity increase (Alvarenga & Pôrto 2007; Barbosa & Carvalho 2016; Laranjeira et al. 2016; Cara et al. 2018; Lai et al. 2021).

It is estimated that the Neotropics contain one-third of the bryophyte species known to science (Gradstein et al. 2001; Frahm 2003), and Brazil comprises almost 12% of this value, with 1,617 cataloged species. Among the Brazilian biomes, the Atlantic Forest stands out with 1,359 species of bryophytes, of which 238 are endemic (Flora e Funga do Brasil 2024, continuously updated).

Considered a “hottest hotspot” of global biodiversity by Myers et al. (2000), the Atlantic Forest has incalculable richness and constitutes one of the 36 global hotspots, concentrating approximately 8% of the world’s biodiversity (Brooks et al. 2010; Menini Neto et al. 2015; Rezendo et al. 2018). Currently, it is in an advanced destruction process and conserves less than 13% of its original vegetation cover (Fundação SOS Mata Atlântica & INPE 2021). The Southeast Political Region of Brazil has the largest remnants of this forest and holds most of the country’s population and GDP (Peres 2010; Laranjeira et al. 2016; Rezende et al. 2018).

Although the state of São Paulo has only 16% natural coverage of the Atlantic Forest, the largest continuous fragments of this biome are concentrated in this state, mainly on its coastal slopes (Fundação SOS Mata Atlântica & INPE 2021). The state of São Paulo concentrates 56.6% of the known bryophyte species in Brazil (Flora e Funga do Brasil 2024, continuously updated). Koga & Peralta (2021) and Lima & Peralta (2021) discussed how bryophyte studies in São Paulo have increased over time and how their results have improved our knowledge about the diversity and richness of this group.

Thus, this work adds to the most recent bryophyte checklists for the state of São Paulo to reduce gaps in our knowledge about the bryophyte species found in this state, focusing primarily on the RBASP. Despite being a century old, this reserve has not been studied systematically to demonstrate its bryophyte richness and diversity. A general and updated list of bryophytes from the RBASP is provided, contributing data for this group’s future taxonomic, floristic, and/or ecological studies. Supplementary material with all the samples analyzed is available at <https://doi.org/10.6084/m9.figshare.26981167>.

Material and Methods

Study area

The Alto da Serra de Paranapiacaba Biological Reserve (RBASP) belongs to the municipality of Santo André, state of São Paulo. The RBASP (23°46’18”-23°47’05’’S and 46°20’24’’-46°18’15’’W) has a total area of 336 ha and is located between the Serra do Mar and the Atlantic Plateau (Fig. 1). The vegetation is predominantly Atlantic Forest in a secondary stage, with an evergreen, dense rainforest, which influences the coastal slope (Coutinho 2006, 2009). It has a phyto-physionomy of primarily high (composed of a denser, more structured forest with a much more continuous canopy) and low forests (more exposed to human activities, distributed on the tops of hills and slopes, without a defined canopy with less species diversity and individuals of smaller height), which occupy 81.5% of the area. In comparison, grasslands and shrubs occupy approximately 18% of the area (Sugiyama et al. 2009).

Figure 1
Map of the municipality of Santo André, highlighting the location of the “Alto da Serra de Paranapiacaba” Biological Reserve (RBASP) in the background. Modified from Soares et al. (2007) and adapted by Oliveira & Peralta (2022).

The Reserve is part of what Coutinho (2006) presents as “slope forests” because it is located in the “mountains along the Brazilian coast”. Within its area are sources of important water bodies (Gutjahr & Tavares 2009). The landscape relief includes hills of up to 900 m.a.s.l.; the climate is markedly humid, with an annual average of 3,300 mm of precipitation. The RBASP is influenced by Brazil’s largest “high rainfall cell” at the transition between Tropical and Subtropical climate zones (Gutjahr & Tavares 2009). Pedological studies have shown that soil is always humid, acidophilus, and poor in nutrients, although leaf litter fall is compatible with that of tropical forests at the same latitude (Lopes et al. 2009; Rossi et al. 2009).

The floristic list of phanerogams from the Reserve comprises 1,006 species distributed in 118 botanical families (Kirizawa et al. 2009). According to Chu (2009), at least 10% of the 969 angiosperm species cataloged have medicinal and economic potential. Tavares & Barros (2009) categorized 232 species present in the Reserve as having landscape potential and relevant commercial interest. From now on, the term “Reserve” will also be used synonymously with RASP.

Sample treatment and data analysis

Of the 1,105 samples analyzed (see file Table S1.xlsx, available on supplementary material <https://doi.org/10.6084/m9.figshare.26981155), 478 resulted from three new collections carried out during three expeditions in March, December 2020, and September 2021. The collections consisted of free walks, based on Frahm (2003), to explore all the environments and substrates available in the area, such as soil, rocks, leaves, tree trunks, decaying tree trunks, and artificial substrates. The remaining specimens had already been deposited in the Herbarium SP.

Species identifications were performed according to Frahm (1991), Sharp et al. (1994), Buck (1998), Gradstein et al. (2001), Gradstein & Costa (2003), Yano & Peralta (2011), Flora e Funga do Brasil 2024 (continuously updated). The floristic list is presented in alphabetical order of family, genus, and species, considering both floristic and biogeographical aspects, according to the classification system of Frey & Stech (2009). The author names’ abbreviations followed Brummitt & Powell (1992). The species occurrence in Brazilian biomes followed Valente & Pôrto (2006), Costa et al. (2011), Valente et al. (2013), Koga & Peralta (2021), Lima & Peralta (2021) and Flora e Funga do Brasil 2024 (continuously updated).

Results and Discussion

The RBASP bryophyte flora comprises 423 species, 150 genera, and 64 families (Tab. S2, available on supplementary material <https://doi.org/10.6084/m9.figshare.26981167>). The species number corresponds to 26% of the bryophytes of Brazil and 31% of the species in the Atlantic Forest biome. The bryophytes found in the Reserve reach 46% of the total reported for the State of São Paulo (Flora e Funga do Brasil 2024, continuously updated).

The 478 samples that corresponded to our collections are shown in the Supplementary material. These new samples represented 43% of the total analyzed, thus increasing by more than 75% the bryophyte specimens from the Reserve deposited in the SP Herbarium.

Forty-six species were recorded for the first time in São Paulo state (Tab. S2, available on supplementary material <https://doi.org/10.6084/m9.figshare.26981167>). Liverworts corresponded to 28 species of these new records, with Lejeuneaceae totaling 50% (14 species). In this survey, we found the three divisions of bryophytes: liverworts (Marchantiophyta), with 217 species and a slight predominance over the mosses (Bryophyta), represented by 203 species, and hornworts (Anthocerotophyta) by three species. The Lejeuneaceae family showed the highest richness with 97 species. The small size of many species of this family allows us to find more than one associated species per sample, thus increasing its representativeness in the floristic list.

Studies showed that Lejeuneales diversified in parallel with angiosperms during the Cretaceous (Fiz-Palacios et al. 2011; Bechteler et al. 2023) and have recently diversified among bryophytes in angiosperm-dominated forests, possibly explaining the colonization breadth of Lejeuneaceae species, especially in tropical forests (Gradstein et al. 2003b; Wilson et al. 2007) and the prevalence of epiphytic species (Groth-Malonek et al. 2004; Feldberg et al. 2014). Other studies in the Reserve found a high species diversity within this family, even in areas altered by human action, which highlights high adaptative plasticity (Giancotti & Vital 1989; Rebelo et al. 1995).

In addition to Lejeuneaceae, the most representative liverworts were Plagiochilaceae (17 spp.), Lepidoziaceae (16 spp.), Metzgeriaceae (16 spp.), and Frullaniaceae (13 spp.). These families account for 73% of the total collections of this division in the Reserve (Fig. 2). Various floristic surveys in the Atlantic Forest have shown the significant contribution of these families to the bryophyte diversity (Santos & Costa 2010; Oliveira & Bastos 2014; Costa & Peralta 2015; Flora & Funga do Brasil 2024, continuously updated).

On the other hand, the mosses showed the highest representativeness of genera for the Reserve, with 90 genera identified. The families Sematophyllaceae (22 spp.) and Pilotrichaceae (20 spp.), both with eight genera, showed the greatest richness (Fig. 3).

Sematophyllaceae is one of the most diverse families of pleurocarpous mosses, distributed worldwide with extremely rapid diversification during the first 20% of the evolutionary history of the order Hypnales (Han & Jia 2020). It is the most represented moss family in tropical regions, lowland forests, and sub-montane forests, and it is also of great importance in the bryophyte diversity of high-montane forests (Costa & Lima 2005). It has a wide distribution throughout Brazil, with 53 spp, of which 17 are endemic (Costa & Peralta 2015). Its species has the highest occurrence in the Atlantic Forest, colonizing different substrates and presenting high plasticity of life forms (Flora e Funga do Brasil 2024, continuously updated). The southeastern region is a diversification center for various genera of this family (Buck & Vital 1992). In the Reserve, we recorded 41% of the species of this family listed for the country.

Pilotrichaceae represents a large and diverse family of mosses in America, with approximately 200 recognized species (Vaz-Imbassahy et al. 2008). In Brazil, 51 species are confirmed, of which nine are endemic (Flora e Funga do Brasil 2024, continuously updated). They are distributed in all biomes, especially in the Atlantic Forest, the leading biome in the number of species found. Reaffirming this data, the Reserve has 72% of the genera, and 37% of the species of this family recorded for Brazil, as previously documented (Visnadi 2005; Peralta & Yano 2008; Santos & Costa 2008; Valente et al. 2009; Koga & Peralta 2021; Lima & Peralta 2021).

Following the Sematophyllaceae and Pilotrichaceae, the Leucobryaceae (19 spp.), Fissidentaceae (14 spp.), Sphagnaceae (13 spp.), and Brachytheciaceae (10 spp.) were the most species-rich families (Fig. 3). They comprise 48% of the Reserve’s moss collections and are one of the most representative families in Neotropical floristic inventories (Gradstein & Pócs 1989; Gradstein et al. 2001). Our findings align with previous studies by Costa (1999), Molinaro & Costa (2001), Costa et al. (2005), Oliveira & Bastos (2014), Carmo & Peralta (2016), Koga & Peralta (2021), and Lima & Peralta (2021), which also identified these families as major contributors to Neotropical moss diversity, although not necessarily in the same order of importance.

Costa (1999), Santos et al. (2011), Oliveira & Bastos (2014), and Batista & Santos (2016) have observed a pattern of greater richness of liverworts and mosses in Atlantic Forest areas. The Atlantic Forest stands out in the Neotropics with a high liverwort species richness due to the complexity and diversity of microhabitats for species colonization (Gradstein et al. 2001; Santos & Costa 2010; Oliveira & Bastos 2014). However, our results showed a similar species number in the two divisions, as observed by Peralta & Yano (2008), Koga & Peralta (2021), and Lima & Peralta (2021). This similarity can be explained by the heterogeneity of available microhabitats with forest formations in different successional stages, allowing various morphoclimatic conditions for bryophytes to establish.

Figure 2
Richness of liverwort families (Marchantiophyta) with more than three species recorded in the “Alto da Serra de Paranapiacaba” Biological Reserve (RBASP), São Paulo, Brazil.
Figure 3
Richness of moss families (Bryophyta) with more than three species recorded in the Alto da Serra de Paranapiacaba Biological Reserve (RBASP), São Paulo, Brazil.

Although less represented than the other two bryophyte divisions, the RBASP showed 16% of the hornwort species recognized in Brazil. This value is equivalent to a quarter of the total richness in Brazil when only the species found in São Paulo are considered (Flora e Funga do Brasil 2024, continuously updated). The Anthoceros species found were Anthoceros hispidus Steph., Nothoceros vincentianus (Lehm. & Lindenb.) J.C. Villarreal, and Phaeoceros carolinianus (Michx.) Prosk.. Hornworts are geographically widespread in the tropical region (Frangedakis et al. 2020); however, its low species occurrence in the Reserve followed the pattern observed by Visnadi (2005), Peralta & Yano (2008), Carmo & Peralta (2016), Carmo et al. (2016), and Lima & Peralta (2021). This pattern could be because they occur when there is little specific competition, and they mainly colonize mineral substrates, such as those found in anthropized areas (Renzaglia et al. 2009). Therefore, the Reserve’s environmental dynamics do not seem to favor the development of a high species richness in this division.

As shown in Table S2 (available on supplementary material <https://doi.org/10.6084/m9.figshare.26981167>), 41% of the species (176 spp.) have a moderate distribution, occurring in five to nine Brazilian states, and 28% (120 spp.) have a restricted occurrence in the country and are present in up to four states (adapted from Valente et al. 2013). Fifty species (11% of the floristic list) are endemic to Brazil, and 35 are restricted to the Atlantic Forest, showcasing the region’s unique biodiversity.

Regarding the Brazilian biomes, 44% (189 spp.) of the species listed are also present in the Amazon (AM), 40% (172 spp.) in the Cerrado (CE), 15% (65 spp.) in the Caatinga (CA), 11% (50 spp.) in the Pantanal (PL) and 9% (39 spp.) in the Pampa (PAM). As shown in Figure 4, 38% (161 spp.) are restricted to the Atlantic Forest (AF).

Our field expeditions yielded 78 species collected for the first time in the Reserve (Tab. S3, available on supplementary material <https://doi.org/10.6084/m9.figshare.26981167>). Among these, 26 species (33%) have a limited occurrence in the country (adapted from Valente et al. 2013), and 20 species are restricted to the Atlantic Forest. The newly collected specimens included two species of hornworts, Anthoceros hispidus and Phaeoceros carolinianus, and 37 species of mosses (47% of the samples) grouped into 19 families, with Fissidentaceae being the richest (eight species). Specimens of Amblystegiaceae and Cryphaeaceae were collected for the first time in the Reserve. The endemic Brazilian mosses collected for the first time in Reserve were Daltonia bilimbata Hampe, Dicranella juliformis Broth, Fissidens pseudoplurisetus Bordin, Pursell & O. Yano, Fissidens yanoae Pursell, Lepidopilidium brevisetum (Hampe) Broth., and Sematophyllum subdepressum (A. Jaeger) Broth. Liverworts represented 50% (39 spp.) of our collections, distributed among ten families. Lejeuneaceae was the richest family (27 spp.) and showed the same general pattern observed for liverworts, with four endemic species collected for the first time in the Reserve: Cheilolejeunea caducifolia (Gradst. & Schäf.-Verw.) W. Ye & R.L. Zhu; Cololejeunea jamesii (Austin) M.E. Reiner & Pócs; Drepanolejeunea grollei M.E. Reiner & Schäf.-Verw. and Lejeunea deplanata Nees and Lejeunea pulchra C.J. Bastos & Gradst.. Metzgeriaceae was the second family with the highest species richness (four species) collected in this division, with Metzgeria subaneura Schiffn. being an endemic species. The Fossombroniaceae family was collected for the first time in the Reserve.

Although the southeastern region of Brazil has a high number of floristic inventories, with bryophytes documented in fragments of the Atlantic Forest, the new records for the state of São Paulo and for this biome (even with the presence of several species whose distribution is considered restricted or endemic to Brazil), highlight this type of research as an important instrument to understand the biodiversity of this group. Therefore, the data presented here can serve as a basis for future taxonomic and ecological research on bryophytes in the Reserve. The bryophytes presented here add to the flora of other plant groups already known in the Reserve. It demonstrates how this Reserve represents a crucial green belt of environmental protection for the Rainforest and its diversity, thus reinforcing the need to maintain its protective nature, guaranteed by law.

Figure 4
Percentage of species recorded in the “Alto da Serra de Paranapiacaba” Biological Reserve and also present in other Brazilian Phytogeographic Domains.

Acknowledgements

We are grateful to “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil” (CAPES), for funding this study. Process number (88882.444244/2019-01).

Data availability statement

In accordance with Open Science communication practices, the authors inform that all data are available within the manuscript

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