Vascular epiphytes in the cloud forests of the Serra da Mantiqueira, Southeastern Region of Brazil

Abstract

Vascular epiphytes represent a remarkable characteristic of the tropical cloud forests. The Serra da Mantiqueira (SM) represents one of the main highland areas of Brazil harboring vegetation remnants, and highlighting the cloud forests. We present a checklist of the vascular epiphytes found in the cloud forests of the SM, discussing the data about taxonomic representativity, distribution in the phytogeographic domains, habits, threatened status in Brazil and the states comprising the SM (Espírito Santo-ES, Minas Gerais-MG, Rio de Janeiro-RJ, São Paulo-SP). Field expeditions were performed between 2012 and 2019, as well as data gathering from scientific collections and published articles. We found 678 species, representing approximately 20% and 30% of the species found in Brazil and Atlantic forest, respectively. The richest families (Orchidaceae, 288 spp.; Bromeliaceae, 112 spp.; Polypodiaceae 65 spp.) corroborated the patterns found in different scales. Forty-one species are threatened nationally (and regionally, there are 149 in ES, 55 in MG, six in RJ, 31 in SP). These numbers of richness and threatened species highlight the relevance of directing efforts toward knowledge and conservation of both cloud forest remnants and SM as a whole, under pain of losing of a large part of the floristic diversity of Atlantic forest.

Palavras-chave
Atlantic Forest; native species; richness; threatened species

Resumo

As epífitas vasculares representam uma característica marcante nas florestas nebulares tropicais. A Serra da Mantiqueira (SM) representa uma das principais áreas elevadas do território brasileiro, abrigando remanescentes vegetacionais, com destaque paras as florestas nebulares. Nós apresentamos uma listagem de epífitas vasculares encontradas nas florestas nebulares da SM, discutindo os dados sobre representatividade taxonômica, distribuição nos domínios fitogeográficos, hábitos, status de ameaça no Brasil e nos estados que compõem a SM (Espírito Santo-ES, Minas Gerais-MG, Rio de Janeiro-RJ, São Paulo-SP). Expedições de campo foram realizados entre 2012 e 2019, além de levantamento de dados de coleções científicas e trabalhos publicados. We found 678, representando algo em torno de 20% e 30% das espécies brasileiras e da Floresta Atlântica, respectivamente. As famílias mais ricas (Orchidaceae, 288 spp.; Bromeliaceae, 112 spp.; Polypodiaceae 65 spp.) confirmaram os padrões obtidos em diferentes escalas. Quarenta e uma espécies estão ameaçadas em nível nacional (e, regionalmente, 149 no ES, 55 em MG, seis no RJ, e 31 em SP). Os números de riqueza e de espécies ameaçadas de extinção ressaltam a relevância de direcionamento de esforços para o conhecimento e conservação tanto dos remanescentes de floresta nebular quanto da SM como um todo, sob pena de perda de grande parcela da diversidade florística da Floresta Atlântica.?

Palavras-chave
Floresta Atlântica; espécies nativas; riqueza; espécies ameaçadas

Introduction

The tropical cloud forests are ecosystems which are typically found in a relatively narrow elevation zone and are characterized by persistent, frequent, or seasonal cloud cover in the vegetation level. This cover is responsible for horizontal precipitation which provides moisture for developing both the plants and the organic humid or flooded and highly organic soils, forming humus and peat. The vegetation is often composed of small trees with sclerophyll characteristics like twisted trunks and branches, dense and compact crowns, and small and rigid leaves. There is a high proportion of biomass composed of epiphytes (both lichens and vascular and avascular plants), and a decrease in lianas. These forests also present a great diversity of epiphytes, although trees, shrubs, and terricolous herbs are also very numerous, mainly if the reduced extension of the area occupied by this type of forest is considered due to the insular distribution and compared with the lowland rainforests which have high tree richness (Hamilton et al. 1995; Bruijnzeel et al. 2010). Three types of tropical cloud forests are recognized (submontane, upper montane, and subalpine) and present variations in the high canopy, the abundance of epiphytes and lianas, and in the elevation where they occur (Scatena et al. 2010).

It is an ecosystem which is currently threatened due to the degradation of the forests as a whole (Scatena et al. 2010), but also potentially under high risk from global climate changes, as they occur in high elevation and the plant species are dependent on the formation of clouds for obtaining moisture for surviving, especially during dry seasons (Still et al. 1999; Foster 2001; Loope & Giambeluca 2002; Ponce-Reyes et al. 2012; Hu & Riveros-Iregui 2016). As these areas are highly diverse and contain several endemic species, and due to the reduced and insular occurrence, changing precipitation, the formation of clouds, temperature, as well as the deforestation or decreasing in the coverage area could be disastrous for the conservation of several species (endemic or not). Furthermore, such changes will also influence the vital role that these forests play in maintaining quality freshwater due to their capacity to capture and condense the clouds and fog which are often present (Bubb et al. 2004; Bruijnzeel et al. 2010).

The presence of these forests in the Serra da Mantiqueira (SM), a mountainous chain mainly located in the Atlantic Forest along the border of the four states of the Southeastern Region of Brazil, Espírito Santo, Minas Gerais, Rio de Janeiro, and São Paulo (Várzea 1942; Machado-Filho et al. 1983; Gonzaga & Menini Neto 2017; Moraes et al. 2020; Pereira et al. 2021), was estimated by Pompeu et al. (2018) based on modeling potential distribution and remote sensor techniques using climatic, hydrometeorological and topographical variables. According to these authors, there is a predominance of these forests above 1500 m.s.m., but they are also present in lower areas of several sites of the SM (e.g., Serra do Brigadeiro, Serra do Cruz, Serra do Ibitipoca, Serra Negra, personal observation). This estimation by Pompeu et al. (2018) was summed in the information presented by Drummond et al. (2005), Martinelli (2007), Stehmann & Sobral (2009), and Le Saout et al. (2013), thus corroborating the relevance of the SM for the Atlantic Domain biodiversity, indicating the necessity of effort for its knowledge and conservation.

As aforementioned, epiphytes are often in high abundance and richness in cloud forests (Webster 1995). This remarkable presence of epiphytes in the tropical cloud forests (Hamilton et al. 1995; Bruijnzeel et al. 2010), their ecological importance, and issues related to conservation (Benzing 1990; Zotz 2016) are responsible for several questions and highlight the necessity to better understand the diversity and distribution of this sinusya species. Thus, several recent studies have been published regarding the vascular epiphytes occurring in the SM, with part of them concentrated in the cloud forests, reinforcing its diversity (Menini Neto et al. 2009a; Barbosa et al. 2015, 2020; Alves & Menini Neto 2014; Furtado & Menini Neto 2015, 2016, 2018a,b). It is worth mentioning the checklist for the Parque Estadual do Ibitipoca in Minas Gerais state (Furtado & Menini Neto 2018a) as one of the richest published in Brazil, recording 224 species distributed in approximately 300ha of cloud forests.

There are growing efforts made in recent years to better understand the delimitation of Serra da Mantiqueira, knowledge of its floristic richness and provide subsidies for conservation (e.g., Menini Neto et al. 2009a, b; Forzza et al. 2013, 2014; Pelissari & Romaniuc-Neto 2013; Rezende et al. 2013; Salimena et al. 2013; Pompeu et al. 2018; Antunes 2020; Gonzaga et al. 2020; Moraes et al. 2020; Moreira et al. 2020a, b; Pereira et al. 2021). Thus, the present study aimed to sample and compile the vascular epiphytes in the cloud forests of this mountain chain, presenting a checklist and discussing the data about taxonomic representativity, distribution in the phytogeographic domains, habits, threat status in Brazil and the four states where the SM is located.

Material and Methods

Study area

The study area comprises the cloud forests of the Serra da Mantiqueira with its delimitation according to Pompeu et al. (2018) and Pereira et al. (2021) (Fig. 1), respectively, comprising part of the states of Espírito Santo, Minas Gerais, Rio de Janeiro, and São Paulo. Two sectors are recognized for this mountain chain, namely Septentrional Mantiqueira and Meridional Mantiqueira, defined by Machado-Filho et al. (1983) (see Gonzaga & Menini Neto (2017) for a more detailed panorama about this delimitation).

Figure 1
Delimitation of the study area and distribution of records used in the list of vascular epiphytes of the cloud forests of the Serra da Mantiqueira, Southeast Region of Brazil. The dashed line represents the separation between the two sectors, Meridional Mantiqueira and Septentrional Mantiqueira.

Dataset

The dataset was partly constructed by field expeditions performed between the years 2012 and 2019, concentrated in some of the main conservation units (CUs) with integral protection located in the Serra da Mantiqueira: Parque Estadual (PE) do Ibitipoca, PE Serra do Papagaio, PE Serra do Brigadeiro, PE Campos de Jordão, Parque Nacional (PN) do Caparaó, and PN do Itatiaia. Apart from these areas, other types of conservation units or areas outside these CUs were also sampled such as Monumento Natural Estadual da Pedra do Baú, Serra da Bandeira, Serra do Cruz, Serra Negra, Maciço Marins e Itaguaré. The specimens collected in those expeditions are deposited in the CESJ Herbarium of the Universidade Federal de Juiz de Fora (acronym according to Thiers et al. 2019, continuously updated).

We also gathered records of vascular epiphytes in the SpeciesLink (<http://splink.org.br/>) and SiBBr (<https://sibbr.gov.br/>) virtual data banks and also used the data published by Ramos et al. (2019) in first filtering of the data inside the delimitation of the SM proposed by Pereira et al. (2021) (Fig. 1) in order to complement this field sampling. Next, the resulting records were refined according to the probability of occurrence of cloud forests presented by Pompeu et al. (2018).

The data preparation steps after the filtering in the databanks were: 1) try to minimize misidentification (by using specimens identified by specialists in the families or consultation with specialists when doubts arose); 2) consulting genera and species nomenclature on the Flora do Brasil 2020 (continuously update); 3) georeferencing the specimens when the sheet labels allowed this.

The presented list is composed of native vascular epiphytes occurring in the cloud forests of the Serra da Mantiqueira and one voucher was selected for each species (or cited Ramos et al. (2019) as a reference in some cases where specimens were not found at the above indicated sites). We did not consider the Moraceae, often occurring as hemiepiphytes in at least part of their lifecycle, due to the difficulty to obtain information only from sheet labels, since the majority of collections are performed when the plants present arboreous habits and phorophytes are not present. We also disregarded the Clusiaceae and Marcgraviaceae, both with hemiepiphytic species, since the sheet labels did not present complete information, despite the field observation of some species. The preferred vouchers are those collected by the authors. The acronyms of the herbaria where the vouchers are deposited are according to Thiers et al. (2019, continuously updated). The Angiosperm families are according to APG IV (2016), while those of ferns are according to PPG I (2016).

The data regarding habits and phytogeographic domains in Brazil were obtained from the Flora do Brasil 2020 (continuously update), and threat status were obtained from Centro Nacional de Conservação da Flora (CNCFlora) (<http://www.cncflora.jbrj.gov.br>). We considered all those species indicated in the aforementioned site as ‘epiphyte’ or ‘hemiepiphyte’, including facultative epiphytes (whose habits also included ‘rupicolous’ and ‘terricolous’, beyond epiphyte). For some species without indication of epiphytic habitat in the Flora do Brasil 2020, we took into account the field observations made by the authors and considered them on the list. The data regarding threat status for each state were obtained from the respective red lists: Espírito Santo (Fraga et al. 2019), Minas Gerais (COPAM-MG 2008), Rio de Janeiro (Martinelli et al. 2018), and São Paulo (SMA-SP 2016).

Results and Discussion

The vascular epiphytes are represented in the cloud forests of the Serra da Mantiqueira by 678 species, distributed in 131 genera and 23 families (Tab. S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.19597192>). This value corresponds to approximately 30% of all richness of vascular epiphytes of the Atlantic Forest (Freitas et al. 2016) and almost 20% of all vascular epiphytes recorded for Brazil (Flora do Brasil 2020 (continuously updated)).

The monocots stand out among the evolutionary lineages with 427 species (63%), distributed in four families, while the ferns (monilophytes) are represented by 153 species (22.5%), belonging to eight families, followed by eudicots (48 spp., 7,1%) in nine families, magnoliids (36 spp., 5.3%), only represented by Piperaceae, and lycophytes (14 spp., 2.1%), having Lycopodiaceae as an exclusive representative. The great representativeness of monocots is mainly due to Orchidaceae and Bromeliaceae, two of the richest families of vascular epiphytes. Polypodiaceae and Cactaceae stand out, respectively, among the ferns and eudicots, with both being globally well-represented in those groups (Benzing 1990; Zotz 2013, 2016).

The richest families are Orchidaceae (288 spp., 42,5%), Bromeliaceae (112 spp., 16,6%), and Polypodiaceae (65 spp., 9,6%), comprising approximately 69% of all recorded vascular epiphytes (Fig. 2). These are the three richest families in vascular epiphytes (Zotz 2013) in the Tropical Region (Gentry & Dodson 1989) and in the Atlantic Forest (Freitas et al. 2016), and repeat a common pattern often found in local studies in Brazil in different physiognomies (e.g., Borgo & Silva 2003; Buzzato et al. 2008; Mania & Monteiro 2010; Bonnet et al. 2013; Alves & Menini Neto 2014; Barbosa et al. 2015; Couto et al. 2016; Furtado & Menini Neto 2016; Joanitti et al. 2017). It is worth mentioning the fact that SM concentrates 23 of the 33 families with epiphytic representatives found in the Atlantic Forest (Freitas et al. 2016) or approximately 1/3 of those that harbor species of vascular epiphytes (Zotz 2016). Furthermore, approximately half of the families (11) are represented by only one or two species, reinforcing the existence of strong uneven distribution of richness among the families, as observed by Benzing (1990) and Zotz (2016).

Figure 2
Richness and percentage of the 23 families of vascular epiphytes recorded in the cloud forests of the Serra da Mantiqueira, Southeastern Region of Brazil.

A total of 23 genera presented more than 10 species (representing 394 spp. or 58.3% of the total), with Vriesea and Peperomia as the richest ones (with 37 and 36 species, respectively) (Fig. 2). Vriesea as the richest genus is justified since it is the more diverse genus of Bromeliaceae in Brazil, with approximately 200 species (Gomes-da-Silva & Souza-Chies 2017; BFG 2018) and the Atlantic Forest is an important diversity and endemism center (Martinelli et al. 2008). The relevance of Peperomia was highlighted by Menini Neto et al. (2009a) and its representativeness in the cloud forests of SM is justified since it is the richest genera of vascular epiphytes if not considering Orchidaceae (Zotz 2016).

A relevant percentage (68.8%) of the species recorded is endemic to the Atlantic Forest, with 466 species. This phytogeographic domain is the richest in plant species as a whole (BFG 2018) and also the richest in vascular epiphytes in Brazil (Freitas et al. 2016), with high rates of endemic species. It is remarkable that the Serra da Mantiqueira only protects a high number of endemic species for this phytogeographic domain in cloud forests (meaning a small portion of the mountain chain and even smaller in the Atlantic Forest), mainly if we take into account that several species are restricted to the SM such as Aechmea aiuruocensis Leme (Bromeliaceae), Anthurium leonii E.G.Gonç. (Araceae), Codonanthe gibbosa Rossini & Chautems and Nematanthus kautskyi Chautems & Rossini (Gesneriaceae), Hatiora herminiae (Porto & A.Castell.) Backeb. ex Barthlott and Schlumbergera lutea Calvente & Zappi (Cactaceae), and Thysanoglossa jordanensis Porto & Brade (Orchidaceae), among others.

It is difficult to list a set of species indicative of this type of forest, however we can cite some which are often found in the cloud forests of the SM, although they are not exclusive to this physiognomy, such as: Anthurium minarum Sakur. & Mayo, A. scandens (Aubl.) Engl. (Araceae), Asplenium auritum Sw. (Aspleniaceae), Billbergia distachia (Vell.) Mez, Vriesea bituminosa Wawra, V. heterostachys (Baker) L.B.Sm. (Bromeliaceae), Hatiora salicornioides (Haw.) Britton & Rose, Rhipsalis floccosa Salm-Dyck ex Pfeiff. (Cactaceae), Elaphoglossum vagans (Mett.) Hieron., Rumohra adiantiformis (G.Forst.) Ching (Dryopteridaceae), Nematanthus crassifolius (Schott) Wiehler, N. strigillosus (Mart.) H.E.Moore (Gesneriaceae), Griselinia ruscifolia (Clos) Taub. (Griseliniaceae), Hymenophyllum polyanthos (Sw.) Sw., Polyphlebium angustatum (Carmich.) Ebihara & Dubuisson (Hymenophyllaceae), Fuchsia regia (Onagraceae), Acianthera saundersiana (Rchb.f.) Pridgeon & M.W.Chase, Anathallis rubens (Lindl.) Pridgeon & M.W.Chase, Bulbophyllum granulosum Barb.Rodr., Cattleya coccinea Lindl., Epidendrum chlorinum Barb.Rodr., Gomesa ranifera (Lindl.) M.W.Chase & N.H.Williams, Octomeria crassifolia Lindl., Stelis megantha Barb.Rodr., S. papaquerensis Rchb.f. (Orchidaceae), Peperomia tetraphylla (G.Forst.) Hook. & Arn. (Piperaceae), Cochlidium punctatum (Raddi) L.E.Bishop, Lellingeria apiculata (Kunze ex Klotzsch) A.R.Sm. & R.C.Moran, Pecluma pectinatiformis (Lindm.) M.G.Price, Pleopeltis macrocarpa (Bory ex Willd.) Kaulf., Serpocaulon catharinae (Langsd. & Fisch.) A.R.Sm. (Polypodiaceae), and Dyssochroma viridiflorum (Sims) Miers (Solanaceae) (Figs. 3-4).

Figure 3
a. Araceae: Anthurium scandens (Aubl.) Engl.; b. Aspleniaceae: Asplenium auritum Sw.; c-d. Bromeliaceae: c. Billbergia distachia (Vell.) Mez, d. Vriesea heterostachys (Baker) L.B.Sm.; e. Cactaceae: Hatiora salicornioides (Haw.) Britton & Rose; f. Dryopteridaceae: Rumohra adiantiformis (G.Forst.) Ching; g. Gesneriaceae: Nematanthus crassifolius (Schott) Wiehler (photos: L. Menini Neto).

Figure 4
a. Griseliniaceae: Griselinia ruscifolia (Clos) Taub.; b. Hymenophyllaceae: Hymenophyllum polyanthos (Sw.) Sw.; c. Onagraceae: Fuchsia regia (Vell.) Munz; d-f. Orchidaceae: d. Anathallis rubens (Lindl.) Pridgeon & M.W.Chase; e. Cattleya coccinea Lindl.; f. Stelis megantha Barb.Rodr.; g. Piperaceae: Peperomia tetraphylla (G.Forst.) Hook. & Arn.; h. Polypodiaceae: Lellingeria apiculata (Kunze ex Klotzsch) A.R.Sm. & R.C.Moran; i. Solanaceae: Dyssochroma viridiflorum (Sims) Miers (photos: L. Menini Neto).

Regarding the habits, 391 species are characteristic epiphytes (those listed in the site Flora do Brasil 2020  (continuously updated) only with the ‘epiphyte’ habit), 18 are hemiepiphyte, and the remaining species (268) are facultative epiphytes (species also presenting rupicolous and terricolous habits) (Supplementary material).

Among the threatened species (considering the CR – critically endangered, EN – endangered, and VU – vulnerable categories), 41 were cited for Brazil (Martinelli & Moraes 2013), 149 for the Espírito Santo (Fraga et al. 2019), 55 for Minas Gerais (COPAM 2008), six for the Rio de Janeiro (Martinelli et al. 2018) considering only the species endemic to this state, and 31 for São Paulo (SMA-SP 2016) (Supplementary material). At least 15 species are cited in three of the five aforementioned red lists and 46 species are considered on two lists. The great number of threatened vascular epiphytes, both globally and regionally, is a reflection of the fragility of several species of this synusia to environmental impacts like the transformation of forest areas into cropland and pastures, climatic changes, a decreasing number of pollinators (Hietz 1999; Köster et al. 2009; Zotz & Bader 2009; Werner et al. 2011; Böhnert et al. 2016). However, it is also related to the fact that several species are considered ornamental and have high appeal among ecotourists, tradespeople, and plant collectors, whose removal has the potential to significantly impact their populations whether on a large scale or not (Mondragón Chaparro & Ticktin 2011; Toledo-Aceves et al. 2014; Wraith & Pickering 2017; Delgado 2019). The red lists are characterized by being dynamic and the need for this method is clear in the indication of species which should have their threat status reviewed both regionally and globally, as highlighted in the studies of Cactaceae (Gonzaga et al. 2020) and Gesneriaceae (Pereira et al. 2021) in the SM environment.

The conservation potential of much of the biodiversity of the Atlantic Forest in a mountain chain as the SM is corroborated and reinforced in this study about the vascular epiphytes occurring in their cloud forests. Unfortunately, large extensions of the SM land have become highly modified over time from pastures for cattle, monocultures of eucalyptus and pine, and/or varied crops for food purposes (such as coffee and banana, among others), real estate speculation, mining, etc. (Hueck 1972; Joly et al. 1991; Mendes Júnior et al. 1991; Gonzaga & Menini Neto 2017). The less impacted areas or those which have been regenerating for longer are found in mountainous regions, and were generally transformed in the last century in conservation units, seeking to save at least a part of the remaining biodiversity, but several other priority areas were indicated to direct conservation and/or research efforts (Drummond et al. 2005; Gonzaga & Menini Neto 2017). The cloud forests are in these mountainous areas, a relatively small part of the Atlantic Forest, but have high relevance for preserving the diversity of the country, since this region is also recognized for harboring great diversity and endemism of other taxonomic/functional groups (Drummond et al. 2005; Martinelli 2007; Versieux & Wendt 2007; LeSaout et al. 2013; Stehmann & Sobral 2009; Pelissari & Romaniuc Neto 2013; Gonzaga et al. 2020; Pereira et al. 2021).

The urgent need to safeguard what remains of natural environments is evident, especially due to the speed at which the degradation is currently occurring, so that efforts must be made to produce knowledge and provide subsidies so that decision-makers can take into account elements to perform their functions properly.

Acknowledgements

We wish to thank the Programa de Pós-graduação em Ecologia of Universidade Federal de Juiz de Fora. This study was financed in part by the Coordenação de Aperfeiçoamento e Pessoal de Nível Superior - Brasil (CAPES), Finance Code 001. We also thank to Carlos Mariano Alvez-Valles, Dayvid Rodrigues Couto, Diego Rafael Gonzaga, Andrea Pereira Luizi-Ponzo, Talita Mota Machado, and Flávio Nunes Ramos.

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Supplementary Material

See supplementary material at <https://doi.org/10.6084/m9.figshare.19597192 >

Edited by

Area Editor: Dra. Tatiana Carrijo

Publication Dates

• Publication in this collection
  27 May 2022
• Date of issue
  2022

History

• Received
  10 Sept 2020
• Accepted
  19 Aug 2021