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Introduction

In Atlantic Forest of southeastern Brazil occurs a special class of residual landforms, composed predominantly by plutonic (granite) and metamorphic (gneiss) rocks, that are ecologically known as inselbergs (from German, insel = island, berg = mountain). They can occur isolated or in groups, separated by a few or many kilometers, forming inselberg landscapes (Hmeljevski, Nazareno, Bueno, Reis, & Forzza, 2017). These ecosystems differ greatly from the surrounding matrix, having unique edaphic-climatic characteristics that select for a specialized vegetation with high endemicity (see Safford & Martinelli, 2000;Porembski & Barthlott, 2000; Porembski, 2007;de Paula, Forzza, Neri, Bueno, & Porembski, 2016). However, inselberg flora is frequently overlooked in favor of other ecosystems of the Atlantic domain.

Southeastern Brazil is one of three important regions recognized globally as hotspots of plant diversity in inselberg ecosystems, alongside Madagascar and southwestern Australia (Porembski, 2007). In this context, it is worth mentioning that the inselbergs located in southern Espírito Santo, recognized for their significant biological importance, are a priority for floristic studies and ought to be prioritized for the creation of protected areas (Martinelli, 2007; Couto, Dias, Pereira, Fraga, & Pezzopane, 2016a;Couto, Francisco, Manhães, Machado, & Pereira, 2017; Kessous, Couto, Uribbe, & Costa, 2018).

Although inselbergs are not suitable for agriculture, and therefore escape its impacts, the mining industry poses the greatest threat to the flora of these environments worldwide (Porembski et al., 2016). Espírito Santo has a highly developed ornamental rock mining industry- one of the state’s main economic activities- and is among the world's leaders in mineral exploration (Sardou Filho, Matos, Mendes, & Iza, 2013). On the other hand, mining is threatening the endemic and endangered flora of the region’s inselbergs. For any proposal of conservation, sustainable use, management, and restoration of inselberg ecosystems, knowledge of their biota is essential. Thus, there is an urgent need for studies on the biodiversity of these unique environments.

This study aimed to inventory the species of vascular plants that grow on the inselbergs of the Pedra das Andorinhas Complex. We aimed to contribute to the knowledge of inselberg flora in southeastern Brazil, and document the occurrence of endemic and endangered species, to support the creation of a protected area in the locality.

Material and methods

Study site

The present study took place on private land (center point: 20° 47' 24'' S and 41° 23' 19.6'' W) between the municipalities of Cachoeiro de Itapemirim and Jerônimo Monteiro, southern state Espírito Santo, Brazil, in a region denominated by the Pedra das Andorinhas Complex (PAC) (Figure 1and2). Covering an area of approximately 360 ha, the study site features large rocky outcrops with patches of Submontane Seasonal Semideciduous Forest (Instituto Brasileiro de Geografia e Estatística [IBGE], 2012) at the base and summit, forming inselberg landscapes.

The PAC ranges from 150 to 500 m in elevation. It is surrounded by agricultural activities (cattle ranching and coffee, eucalyptus and orange plantations), mineral extraction and forest fragments. The climate has been classified as CwA, with dry winters and rainy summers, a mean annual temperature of about 24°C, and a mean annual rainfall of 1,450 mm (Couto et al., 2016b).

According to reports from local residents, the PAC has a history of bushfires (between 15 and 20 years ago) and some mineral exploration. The rocky complex consists of several inselbergs, which are generally difficult to access (Figure2). In this study, we investigated three rock outcrops, one between Cachoeiro de Itapemirim/ Jerônimo Monteiro, known as Pedra das Andorinhas (1) (20° 46’ 19” S; 41° 21’ 12” W), and two others in Jerônimo Monteiro: Parada Cristal (2) (20° 47’ 39” S; 41° 22’ 20” W), Pedra Três Irmãs (3) (20° 46’ 19” S; 41° 21’ 12” W).

Data collection

Floristic surveys of the rock outcrops in the PAC were conducted during monthly field expeditions between July 2017 and October 2018. Sampling was restricted to inselberg vegetation, which is characterized by rupicolous species that inhabit the rocky surfaces.

Fertile specimens were collected randomly, using the walk-over survey method (Filgueiras, Brochado, Nogueira, & Guala, 1994), and processed according to Mori, Berkov, Gracie, and Hecklau (2011). We accomplished taxonomic identification by consulting specialized taxonomic literature (e.g., regional and local flora monographs), images of exsiccatae available in virtual herbaria Jabot (jabot.jbrj.gov.br/) and Reflora (reflora.jbrj.gov.br/reflora/herbarioVirtual/), and experts on each taxon, to whom we sent exsiccate. The circumscription adopted for angiosperm families are in accordance with APG IV (The Angiosperm Phylogeny Group, 2016). For monilophytes and lycophytes, we followed PPG I (Pteridophyte Phylogeny Group [PPG], 2016). Accepted names, synonymy, and authors were confirmed by reference to Flora do Brasil 2020 (http://floradobrasil.jbrj.gov.br/), Missouri Botanical Garden (http://tropicos.org) and International Plant Names Index (IPNI, 2020). Additional specimens collected at other times were identified through consultation of the database of Brazilian flora.

In general, the rocky outcrops of the PAC can be organized into two main phytophysiognomies: (i) vegetation on exposed rock and (ii) woody rupicolous communities. All species were organized according to their occupation within these two rocky phytophysiognomies.

Vegetation on the exposed rock is groups of plants growing directly on and bounded by the rocky surfaces, with no or very shallow soil (epilithic or saxicolous plants respectively) (Conceição, Pirani, & Meirelles, 2007). This phytophysiognomy is composed mainly of monocot mats (Bromeliaceae and Velloziaceae mainly) and epilithic vegetation, covering large expanses of the rock outcrops. The woody rupicolous communities are composed predominantly by shrubs and small trees less than 10 m high, growing in poorly developed soil (up to 20 cm deep) in large depressions and fissures on the slopes of the inselbergs. Woody species typical of the matrix, such as epiphytes, vines, and herbs, can also occur (Couto et al., 2017).

Species were classified according to vegetative habit as trees, shrubs, subshrubs, climbing plants and herbaceous, following Couto et al. (2017). The endangered species were cited according to the official list of Centro Nacional de Conservação da Flora (cncflora.jbrj.gov.br), Red List of Espírito Santo state (Fraga, Peixoto, & Leite, 2019) and IUCN Red List (https://www.iucnredlist.org/).

Collections of botanical material were carried out for all species recorded in the study and voucher specimens were deposited in the CAP herbarium (acronym according to Thiers – continuously updated), of the Universidade Federal do Espírito Santo, in Jerônimo Monteiro, state Espírito Santo.

Results and discussion

A total of 121 species, belonging to 96 genera and 40 families, were recorded for the PAC (see supplementary material). Eudicotyledons represented the most diverse evolutionary lineage (65 spp., 54% of the total), with 25 families (62.5%), followed by Monocotyledons with 45 spp. (37%) and 10 families (25%), Monilophytes (8 spp., 6.6%) with 3 families (7.5%), Lycophytes (2 spp., 1.6%) with 1 family (2.5%), and Magnoliids (1 spp., 0.8%) with 1 family (2.5%).

The richest families in the PAC were Bromeliaceae (17 spp.), Orchidaceae (12), Fabaceae (10), Asteraceae and Euphorbiaceae (6 spp. each), Cactaceae and Pteridaceae (5 spp. each), Gesneriaceae and Myrtaceae (4 spp. each), Solanaceae and Commelinaceae (3 spp. Each) (Figure 3). These families accounted for 75 species (i.e. 62% of the total) (Table S1).

The genera represented by the most species were Tillandsia (Bromeliaceae), with five species, Pitcairnia (Bromeliaceae) and Sinningia (Gesneriaceae), both with four species each. Selaginella (Selaginellaceae), Doryopteris (Pteridaceae), Cyrtopodium (Orchidaceae), Eugenia (Myrtaceae), Centrosema, Macroptilium (Fabaceae), Cyperus (Cyperaceae), Alcantarea (Bromeliaceae), Anthurium (Araceae), Anemia (Anemiaceae), Ipomoea (Convolvulaceae), Dioscorea (Dioscoreaceae), Vellozia (Velloziaceae) and Solanum (Solanaceae) were represented by two species each (Figure 4).

A new species of Araceae (Anthurium genus) recorded during fieldwork (voucher: J. M. C. Covre 93), is in description phase. On the other hand, Alcantarea patriae Versieux & Wand (Versieux & Wanderley, 2007), Anthurium martinellii Nadruz & Theófilo (Coelho & Valadares, 2019), Coleocephalocereus uebelmanniorum (Braun & Esteves) Braun, Esteves & Hofacker, Pitcairnia azouryi Martinelli & Forzza (Martinelli & Forzza, 2006), and Stigmatodon attenuatoides (Couto, Manhães & Costa, 2020) were described from collections obtained in the PAC. Of these species, Alcantarea patriae, Anthurium martinellii, Coleocephalocereus uebelmanniorum and Stigmatodon attenuatoides are endemic to the inselbergs of Jerônimo Monteiro and Cachoeiro de Itapemirim.

As for the distribution of species according to vegetative habit (supplementary material), herbaceous species were predominant, with 72 species (60%), followed by climbing plants with 15 species (12%), shrubs with 14 species (12%), trees with 13 species (11%) and subshrubs with 6 species (5%). The occurrence of species according to phytophysiognomy showed a higher prevalence of species in exposed rocky vegetation than in woody rupicolous communities, with 79 species (65.29%) and 42 species (34.71%), respectively. In total, 18 species (15%) are included on official endangered species lists (Table 1).

The flora of the Pedra da Andorinha Complex is characterized by genera typical of the inselbergs of southeastern Brazil, such as Alcantarea, Coleocephalocereus, Encholirium, Selaginella and Vellozia (Porembski, Martinelli, Ohlemüller, & Barthlott, 1998;Meirelles, Pivello, & Joly, 1999; Couto et al., 2017;de Paula, Mota, Viana, & Stehmann, 2017), and includes endemic and endangered species. The survey results corroborate previous studies that recognize the southeastern region of Brazil as one of the global centers of richness and endemism among inselberg plants, a distinction shared by Madagascar and eastern Australia (Porembski, 2007).

The survey results differ from some other studies conducted previously in various regions of Brazil (Table 2). In general, the number of species was higher, especially in comparison to inselbergs in the Caatinga Domain, but it was lower compared to inselbergs of the Atlantic Forest, with rare exceptions. These variations can be explained, according to Porembski (2007), by the clear pattern of distinction between different geographic regions, in which environmental filtering differentially shapes inselberg species composition and structure (Yates et al., 2019).

When compared to other inselbergs researched in Espírito Santo, the species richness recorded for the PAC was inferior (Table 2). Compared to montane inselbergs, such as Alto Misterioso (Esgario, Fontana, & Silva, 2009) in the state’s midwestern region, and Pedra dos Pontões (Couto et al., 2017) in its south, the differences in climate (temperature and precipitation) and altitudinal gradient may be the main causes of this distinction. The PAC is a submontane inselberg under the influence of the surrounding Submontane Seasonal Semideciduous Forest and its dry climate. Alto Misterioso and Pedra dos Pontões are situated between a seasonal and humid (ombrophilous) phytophysiognomy and patches of cloud forest (Esgario et al., 2009;Couto et al., 2017).

However, the distinction in species richness was most notable concerning submontane inselbergs of Pedra do Elefante in northern Espírito Santo (Pena & Alves-Araújo, 2017). Although the Pedra do Elefante complex covers a large area (2,562.31 ha), its higher species richness compared to the PAC seems to be due only to the greater collection effort in that locality. Historically, it was subject to mineral extraction, but it is now a Protected Area (Conservation Unit – Law 9985/00 SNUC).

Among the richest families found in the PAC, six (Fabaceae, Orchidaceae, Asteraceae, Bromeliaceae, Myrtaceae, and Euphorbiaceae) were also among the richest families in the Atlantic Forest (The Brazil Flora Group [BFG], 2015) and are well represented in inselberg vegetation in Brazil (e.g. França, Melo, & Santos, 1997;Esgario et al., 2009;Couto et al., 2017;Pena & Alves-Araújo, 2017). Fabaceae, for example, has a species richness in the PAC similar to that found on inselbergs in the Caatinga Domain (Araújo, Oliveira, & Lima-Verde, 2008; Tölke, Silva, Pereira, & Melo, 2011;Paulino, Silveira, & Gomes, 2018). This finding contradicts the results of other floristic surveys conducted in Espírito Santo, in which the most-represented families were Orchidaceae, Bromeliaceae, Asteraceae, Melastomataceae, Cyperaceae, Poaceae, Polypodiaceae, Cactaceae and Araceae (Esgario et al., 2009;Couto et al., 2017). Porto, Almeida, Pessoa, Trovão, and Felix (2008) explained this high number of Fabaceae species in Caatinga as evidence of greater variation in its species’ survival strategies in xeric environments. Porembski and Barthlott (2000), in studies conducted in African inselbergs, also showed this family’s ability to adapt effectively to rocky environments.

Of the 96 genera recorded in the present study, 66% were represented by a single species. This finding contradicts results found in floristic surveys conducted on the African continent, where 48% of the collected species belonged to genera represented by a single species (e.g. Porembski & Brown, 1995; for Costa do Marfim). We found a total of 40 families, 16 of which were represented by a single species. This large number has also been observed in other floristic surveys of rocky outcrops in Espírito Santo (Esgario et al., 2009;Couto et al., 2017;Pena & Alves-Araújo, 2017) and is characteristic of high diversity sites (Ratter, Bridgewater, & Ribeiro, 2003). Families such as Bromeliaceae and Orchidaceae were more relevant in terms of species richness among the rock outcrops studied here, possibly due to adaptive strategies that contribute to their survival in these environments, such as the presence of systems that accumulate water, specialized trichomes, thick and crass leaves and the presence of bulbs or pseudobulbs (Porembski, Seine, & Barthlott, 1997; Benzing & Bennett, 2000; Menini Neto, Forzza, & van den Berg, 2013).

Many of the plant species specific to inselberg ecosystems are known as ‘resurrection plants’ because of their desiccation tolerance, a common survival strategy in these environments. In the present study, this survival mechanism was observed in the Velloziaceae (Vellozia candida and Vellozia variegata) family and the monilophytes and lycophytes genera Anemia, Cheilanthes, Doryopteris, and Selaginella. All of these genera have been described as desiccation tolerant in previous studies (Porembski & Barthlott, 2000; Porembski, 2007). Species identified as Encholirium horridum (Bromeliaceae), Coleocephalocereus uebelmanniorum (Cactaceae) and Cyrtopodium glutiniferum (Orchidaceae) possessed adaptive mechanisms such as stems that store water or an underground caudex (Porembski, 2007).

Typical genera of Bromeliaceae, such as Alcantarea, Encholirium, Pitcairnia, Stigmatodon, and Tillandsia, were found on rocky outcrops. These genera have been found in high abundance in Brazil's inselberg landscapes (de Paula et al., 2016; Couto et al., 2017). We also recorded Coleocephalocereus (Cactaceae), Sinningia (Gesneriaceae) and Vellozia (Velloziaceae), which, despite comprising only a few species, are equally important genera typical of South American inselbergs (Porembski, 2007).

In this study, we observed that the woody rupicolous species - Ceiba erianthos (Malvaceae), Eugenia punicifolia (Myrtaceae), Pseudobombax aff. petropolitanum (Malvaceae), Tabebuia reticulata (Bignoniaceae) and Wunderlichia azulensis (Asteraceae) - hosted 12 species of vascular epiphytes, mainly Bromeliaceae (Tillandsia gardneri, T. loliacea, T. recurvata, T. stricta and T. usneoides), and Orchidaceae (Brassavola tuberculata, Cattleya cernua and Laelia gloriosa). Of the phorophytes mentioned, Pseudobombax aff. petropolitanum is recognized as an important facilitator tree in inselberg vegetation of Espírito Santo (Couto et al., 2016a;Francisco, Couto, Evans, Garbin, & Ruiz-Miranda, 2018). Owing to its architecture and size, including the large roots exposed on the rock surface, this phorophyte hosts an impressive diversity of vascular epiphytes, particularly on montane inselbergs (Couto et al., 2016a;Couto et al., 2019). Although these woody rupicolous communities are an important component of inselberg vegetation, they are scarcely studied (Couto et al., 2017;Francisco et al., 2018). More research ought to be focused on these communities, as they are an essential component in restoration strategies for globally threatened inselberg ecosystems (Porembski et al., 2016).

Conservation of Pedra das Andorinhas complex

PAC has a high diversity of known species, some of which are endemic to the complex itself and nearby outcrops. Some of those species have been described only recently, using botanical materials from the site. Collection efforts are fundamental to filling research gaps and expanding the floristic and phytogeographic knowledge of the rocky outcrops in the Atlantic Forest in the state of Espírito Santo. Also, conservation policies are essential for protecting this unique vegetation, including many endangered species, some of which are rare (e.g. Tabebuia reticulata; see Lohmann & Silva-Castro, 2009) or restricted to rock outcrops (e.g. Pitcairnia decidua, Pitcairnia azouryi, Coleocephalocereus uebelmanniorum, Encholirium horridum). These species are recognized worldwide as prevalence indicators for the creation of protected areas (Brooks et al., 2006).

Because the PAC is an outcrop of granite origin and close to one of Brazil's most important ornamental stone beneficiation industries (Xavier, Azevedo, Alexandre, Monteiro, & Pedroti, 2019), the locale is extremely vulnerable to speculative mining. Despite the importance of the mining sector for the Espírito Santo economy, mining activity is the biggest threat to inselberg vegetation, not only in Brazil but also around the world (Porembski et al., 2016). Historically, inselberg vegetation has been neglected by environmental agencies during the environmental licensing of mining activities, causing irreparable damage to these important ecosystems of the Atlantic Forest (Couto et al., 2019). Now, the populations of many inselberg plant species (e.g. Pitcairnia azouryi) are under serious threat of extinction (Manhães, Couto, Miranda, & Carrijo, 2016). For these reasons, we call the attention of public authorities to the importance of inselberg vegetation.

Furthermore, the PAC is surrounded by an anthropized matrix, where exotic grasses, mainly Panicoideae genera (e.g. Panicum and Urochloa) (observed), grow extensively and are used widely for cattle grazing. The existence of these grasses, their persistence, and high abundance in seed banks (Correia & Martins, 2015) is worrying. Wherever they manage to colonize natural areas, these grasses impair the development and establishment of native monocotyledons on rocky outcrops due to their hardiness in competition for resources. Another aggravation associated with colonization by grass species is the deposition of combustible material, which leaves the PAC high susceptible to fire. Inselberg fires modify community structure and composition and lead to the loss of endemic species, resulting in homogenization of the flora of these important refuges (Hunter, 2017).

Occurrence and distribution data on invasive alien species are essential for developing appropriate control measures and management strategies for natural areas protected under Brazilian law 9985/00. Much of the work on protected areas neglect this information despite invasive species being a major cause of global biodiversity loss (Haddad et al., 2015). Therefore, to guide conservation policy makers, we have incorporated the occurrence of exotic species with invasive potential into our plant list.

Finally, a few characteristics and particularities of the existing flora in the PAC justify and support the creation of a Protected Area that would preserve a significant portion of the flora in the South Espírito Santo region, mainly the inselberg vegetation.

Conclusion

This study provides important knowledge about the flora of the Pedra da Andorinha Complex and justifies the need to create a Conservation Unit in the locality, defining it as a priority for conservation due to the recorded wealth, the number of endangered, endemic species and new species that are being described for this location.

It is worth mentioning that the carrying out of more regional inventories is highly recommended to improve the quality of knowledge and, consequently, the efforts to conserve the vegetation of these singular areas and the Atlantic Forest.

Acknowledgements

We are grateful to the owners who authorized us to study their private properties, and to the Municipality of Jerônimo Monteiro and the Instituto Capixaba de Pesquisa, Assistência Técnica e Extensão Rural (Incaper) for their support. The second author thanks the Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), for granting a postdoctoral Scholarship (PROPPG 04/2019). Thanks to Universidade Federal do Espírito Santo (UFES), Herbarium CAP and Nupemase for the logistic support. We emphasize that this work was carried out with the support of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) - Financing Code 001. To Megan F. King for the English revision. Finally, we want to thank the two anonymous reviewer and the editor Dr. Ricardo Massato Takemoto for their comment and advise that greatly improved the article.

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Notas de autor

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IR