Threatened Flora of Ilha Grande, Rio de Janeiro State, Brazil

Hoehnea 47: e772019. http://dx.doi.org/10.1590/2236-8906-77/2019. ABSTRACT – (Threatened Flora of Ilha Grande, Rio de Janeiro State, Brazil) This study documents the occurrence of threatened plant species on Ilha Grande, Rio de Janeiro State, Brazil. This survey acquired data from herbaria, living collections and field sampling. A total of 49 threatened species distributed among 27 families and 38 genera were recorded in the scientific collections, of which 43 are cited on official lists of threatened plant species for the State of Rio de Janeiro and Brazil. Twelve species recorded on the island are on an international list of endangered species, 30 on the national list for Brazil, and 11 on the State List of Rio de Janeiro. The IUCN Red List categories of Vulnerable and Endangered were the predominant categories for the plant species of Ilha Grande, with the main historical threat factors being deforestation and logging. Most of the threatened species of the island are arboreous. The families with the greatest number of threatened species are also among the richest in Dense Ombrophilous Forest: Melastomataceae, Myrtaceae, Meliaceae, Bromeliaceae and Orchidaceae. Four species registered on the island also appear on the list of endemic species in the State


Introduction
Brazil is the most botanically diverse country in the world (Forzza et al. 2012), with about 50% of its seed plants being endemic to the country (BFG 2015). These are just two of the reasons why Brazil was one of the signatories of the Convention on Biological Diversity (GSPC 2011).
This initiative requires the development of local checklists, which are fundamental to accomplishing the targets of the Global Strategy for Plant Conservation (GSPC). Lists of endangered species in particular help to guide political, conservation and scientific actions aimed at protecting biodiversity (Mittermeier & Scarano 2013). The species included in the list of threatened species of Brazilian flora (MMA), established under Ordinance 443 (MMA 2014), and in the list of threatened endemic species of the State of Rio de Janeiro, CONEMA 80 (CONEMA 2018), are examples of red lists of species that have subsequently been protected by law.
The Atlantic Forest of Brazil is one of the world's biodiversity hotspots (Mittermeier et al. 2011). Located within this hotspot is the continental island Ilha Grande, which, with 19,300 ha, is the largest island in Ilha Grande Bay and one of the largest islands on the Brazilian coast. Ilha Grande belongs to the municipality of Angra dos Reis of the State of Rio de Janeiro (Rocha 2018). Throughout the last century, Ilha Grande was marked by fishing activities and the establishment of prisons in the villages of Abraão and Dois Rios (Prado 2003). With a significant reduction in fishing activity since the 1970s, and with the closure of prisons in the 1990s, tourism became the most important economic activity of the island (Mello 1987, Prado 2003, Santiago et al. 2009).
The first studies focusing on plants of Ilha Grande were those of Maciel et al. (1984), Araujo & Oliveira (1988), Almeida et al. (1998), and Oliveira (1999Oliveira ( , 2002. More recent plant inventories (Callado et al. 2009, Nunes-Freitas 2009, Manão 2011, Pederneiras et al. 2012, Rosa et. al. 2016 have added new records to the flora of the island. Ilha Grande is a mosaic of several conservation units covered by secondary forest, but also functions to conserve significant habitats (Alho 2002).
Red lists are essential tools for environmental governance, and so they must be supported by documented information to assure that risk categories are appropriately employed and that the reliability of the assessments can be checked (IUCN 2011, Penedo et al. 2015. The flora of Ilha Grande contains 1143 plant species, including 25 that are under threat according to the most comprehensive botanical inventory of the island to date (Callado et al. 2009). Maurenza et al. (2018) published a checklist of all the conservation units of the State of Rio de Janeiro in a review of the previous checklists of Ilha Grande. Because of the richness of plant species in the Atlantic Forest and the advances of research carried out on Ilha Grande, the threat status of the flora of the island required reassessment. Thus, we compiled and summarized information on threatened plant species of Ilha Grande. The aim was to present an updated red list of flowering plants of Ilha Grande of the municipality of Angra dos Reis, State of Rio de Janeiro, and to document the occurrence of threatened species in order to strengthen the argument for preserving this priority area for conservation.

Material and methods
Plants were studied in their natural habitats and from herbaria vouchers. For the latter the authors visited herbaria with significant representations of specimens from Ilha Grande: HB, HBR, RFFP, R and RB). The field study and the collections of biological material in Parque Estadual da Ilha Grande (PEIG), Rio de Janeiro, Brazil were registered with, and authorized by, SISBIO-IBAMA (number 53321/2014 andINEA-RJ 006/2015). Living specimens were also included from the living collection of Parque Botânico do Ecomuseu Ilha Grande (PaB), located in Vila de Dois Rios, Ilha Grande, Rio de Janeiro, Brazil, with voucher samples being deposited in the herbarium of Universidade do Estado do Rio de Janeiro (HRJ). Life forms were based on Raunkiaer (1934), while conservation status and types of threat followed IUCN (2011).
A combination of databases -Brazilian Flora Checklist (BFG 2015), INCT Virtual Herbarium (INCT 2019), JABOT (JBRJ 2018), and Flora do Brasil 2010 (2019) -was used to prepare the checklist. Initially a filtered list of angiosperm species that occur on Ilha Grande was downloaded from the available databases. This initial list consisted of 4,966 records (infraspecific taxa were not included). Our survey included of all available vouchers cited by the databases. Vouchers with provenance of Ilha Grande and identified by specialists were prioritized, aided by information provided by the contributors to the Brazilian list (Martinelli & Morais 2013).
The study considered species under some degree of threat in at least one of the latest red lists: IUCN (2011), MMA (2014) or CONEMA (2018). Consequently, Critically Endangered (CR), Endangered (EN) and Vulnerable (VU) categories were considered in this work, and are collectively referred to herein as 'threatened'. Globally threatened species were cited according to the IUCN (IUCN 2011), nationally threatened species followed the Brazilian Red List of Threatened Plant Species (Martinelli & Morais 2013), while State threatened species followed the Red Book of Endemic Flora of the State of Rio de Janeiro , MMA (2014) and CONEMA (2018).
Both the national red list and the red list of the State of Rio de Janeiro received the value of law upon their publication, as does the guide Wanted: Endemic Flora of the State of Rio de Janeiro (Rosa et. al. 2018), published by CONEMA (2018). Global risk assessments are according to IUCN categories (IUCN 2011).

Results and discussion
Number of species -Of the 680 species of angiosperms listed for Ilha Grande, 60 are considered threatened to some degree. Vouchers were located for 49 of these species, distributed among 27 families and 38 genera, cited in the official lists of threatened plants species of the State of Rio de Janeiro and the country of Brazil (table 1).
The 11 other species were indicated by other inventories (table 2) and do not have related herbarium material, which should be sought out in future floristic inventories. It should be emphasized that vouchers provide a means for other  Martinelli & Moraes (2013) and State (Rio de Janeiro) threat for endemic plants is based on Martinelli et al. (2018). Categories -VU: vulnerable; EN: endangered; CR: critically endangered; *: Rare species according to Giulietti et al. (2009  continue researchers to verify published taxonomic determinations and ensure that taxonomic works are reliable and reproducible (Culley 2013). In some cases, target species are rare in the wild, and new records of occurrence are difficult to obtain (Giulietti et al. 2009). Such insufficient quantity of samples makes it challenging to make precise taxonomic determinations (Knapp 2002, Penedo et al. 2015. Of the forty-nine species registered and vouchered for Ilha Grande, 12 are on the IUCN Red List (IUCN 2011), 23 on the Brazilian national list (Martinelli & Moraes 2013), upon which the national red list of endangered species was based (MMA 2014), and 14 as endemic threatened species for the State of Rio de Janeiro (Martinelli et al.2018), which were legally recognized by CONEMA (2018).
Areas of occurrence -Most of the threatened species are Atlantic Forest endemics (82%), while , others are distributed in both the Atlantic Forest and Cerrado (16%); a single species, Cedrela odorata L., Meliaceae, is broadly distributed among the Amazon Forest, Atlantic Forest, Caatinga and Cerrado biomes (2%) (figure 1). Cedrela odorata is a species of concern due to reductions in its populations due to harvesting for timber, which has been used by traditional populations of Ilha Grande for boat construction.
No species have been described as endemic to Ilha Grande until now. Two species of Bromeliaceae described for the island -Vriesea aff. bituminosa (Moura 2011) and Canistropis aff. microps -when legitimately described, can be considered endemic.
Categories of threat -The predominant threat category for the threatened species of Ilha Grande is Vulnerable (24 spp.), followed by Endangered (21 spp.) and Critically Endangered (4 spp.) (figure 2). No extinct species emerged from the survey.
Some threatened species of Ilha Grande were treated as rare by Giulietti (2009)     threatened flora of Ilha Grande by Maurenza et al. (2018). However, it was not possible to obtain vouchers for 11 of the species (table 2) recorded by Maurenza et al. (2018). The proportion of threatened species (49) of all registered flowering plant species for the island (680) is 7.2%, which is below the equivalent proportion of 43.8% for the entire State of Rio de Janeiro . There are three hypotheses that can explain this low proportion: (1) the sampling effort has not yet reached its maximum, and there are still species to be documented; (2)  Taxonomic groups -The families with the greatest number of species under some degree of threat were Melastomataceae, Myrtaceae and Orchidaceae, with five species each, which together represented 30% of the threatened species of the island. These were followed by Bromeliaceae and Meliaceae with three species each and together representing 12% of the total (table 1). Over a third of the families (eight families, together representing 55% of the threatened species) are represented by only a single species (figure 4). Most species were trees, of which the families with the highest number of threatened species were also among the richest families in Dense Ombrophilous Forest: Melastomataceae (5), Myrtaceae(5) and Meliaceae (3). The second most speciose group according to habit was herbs, which was represented by the families Orchidaceae (6) and Bromeliaceae (3), which were also specious in the Dense Ombrophilous Forest, with some species also in Restinga vegetation near sea level (table 3).
In general, tree families, like Fabaceae, Myrtaceae, Lauraceae and Melastomataceae, receive more attention in floristic inventories, and thus there is a greater number of species of this habit recognized as threatened (Whitmore 1990, Lieberman 1996, Lomolino 2001. Some herbaceous threatened species occur near sea level in Restinga and in Dense Ombrophilous Forest along the trail to Pico do Papagaio at 800-1000 m.s.a.l. (table 3). This finding may reflect the fact that these regions are more accessible on the island (vs. sites without trails).    Of these families, Bromeliaceae, and Orchidaceae are important families, comprising epiphyte species (5 species, and 3 species), with some species occurring at elevations of up to 900 m.
Occurrence in vegetation types -Dense Ombrophilous Forest was the phytophysionomy with the greatest richness of threatened species (figure 5). Some more speciose families in Dense Ombrophilous Forest with a high percentage of threatened species for the State of Rio de Janeiro (according to CONEMA 2018) do not have a proportional number of threatened species on the island (e.g., Bromeliaceae). This may be due to the fact that some species are epiphytic and more difficult to collect.
Most threatened species of Ilha Grande are terrestrial species (figure 6), although epiphytic species would be expected in areas of Atlantic Forest, especially in areas at higher elevations. It is believed that the low representation of epiphytes is due to a lack of collection effort since most inventories were based on terrestrial plant species (figure 7).
Threat factors influencing the conservation status of the flora of Ilha Grande -The main historical threat factors in Ilha Grande have been logging, deforestation for agriculture and surveillance, which were usual practices during the prison period, which ceased in 1994.
The predominant current threat types include deforestation and/or logging (table 1). Numerous areas throughout the island have become regenerated areas after abandonment in the 1990s. The primary areas of current impact are along the shoreline, especially in the surroundings of larger villages (Abraão, Araçatiba, Provetá), belonging to the conservation unit Area de Proteção Ambiental (APA) Tamoios.  The presence of exotic species is also a potential problem for the maintenance of native species populations. Recent systematic surveys on different environments within the island recorded the occurrence of exotic species outside anthropic and peri-anthropic habitats (Callado et al. 2009). Invasive alien species have significant negative impacts on the recipient environment (Jeschke et al. 2014, Russell & Blackburn 2017, Russel et al. 2017, primarily on biodiversity values and ecosystem services. Collection efforts -The herbaria with the greatest holdings of botanical collections from Ilha Grande are: Jardim Botânico do Rio de Janeiro (RB), with 48% of the surveyed species, Universidade do Estado do Rio de Janeiro (HRJ, RFFP and HB), with 35%, and Universidade Rural do Rio de Janeiro (RBR) with 12%.
Rare and threatened plants are usually found in places that are difficult to access. Coincidentally or not, areas without access by road and steep access are the places with  more rare species. These species are typically present in areas at middle/advanced (climax) stages of development.
Flagship species and species conservation -In conservation biology, a flagship species is a species selected to raise support for biodiversity conservation. Flagship species projects have sometimes been successful in saving species and their habitats (Barua 2011, Ducarne et al. 2011, Walpole 2002. Flagship species can be selected, depending on what is valued by the audience, and the goals of the project, such as conservation awareness, fundraising, ecotourism promotion, community-based conservation, and promotion of funded research (Barua 2011). Threatened species lists is therefore, an important indicator for new flagships species.
The most popular species among the endangered species of Ilha Grande is the palm jussara palm (Euterpe edulis Mart.). Exploitation of the heart of jussara palms is illegal (Brazil, 2008), but difficult to combat, and is in need of greater enforcement effort. The remaining populations, along the Abraão-Dois Rios road, serve as an active seedbank for seedling production, which is monitored by the Parque Botânico's staff.
Other species with appeal to become flagship species are the Bromeliad and Orchid species, as well as Couratari pyramidata (Vell.) Kunth (Lecythidaceae), a rare and singular tree, endemic to the Rio de Janeiro State.

Conclusions
Ilha Grande hosts 49 species that are under different degrees of threat at different geographic scales (global, national and state). These species reveal the importance of the island and its conservation units to the conservation of native plant diversity. Conservation programs that focus on endangered species are recommended, and will depend on scientific efforts in other scientific areas, as reproductive biology, demography, ecology, among others. Fifteen species documented by previous studies for the island play a complementary role, for a potential total of 60 threatened species occurring on Ilha Grande (Araujo e Oliveira 1988, BFG 2015, Callado et al. 2009, INEA 2010, Manão 2011, Maurenza et al. 2018. Being unvouchered, these 11 species are not represented in herbarium collections (table 2), and so initial survey efforts to document these species by primary data (herbaria, photographs, and living collections) should spearhead future survey efforts. Due to the constant increase in knowledge about botanical species of the Atlantic Forest, species categorized as Near Threatened or in less severe categories may, in the future, be transferred to more severe categories of threat by upcoming assessments. With regard to long-term conservation of the populations of threatened species within protected areas of Ilha Grande, genetic exchanges with populations beyond the island are essential. Such exchanges require the maintenance of ecological corridors and mosaics of conservation units along the continental shoreline in Baía da Ilha Grande.
Conservation approaches focused on threatened species may benefit the entire biota of Baía da Ilha Grande, including the island itself and in its buffer area. There certainly remain gaps in the knowledge of the non-arborous flora of Ilha Grande, and so studies focused on less-studied groups should be encouraged for a more proper assessment of the threat level to this component of the biodiversity of Ilha Grande.