Endemic angiosperms in Bahia Coastal Forests , Brazil : an update using a newly delimited area

The forest along the coast of Bahia state, in northeastern Brazil, has been acknowledged as an area of endemism for several groups of organisms. The first study concerning endemic angiosperm species in this region, through which 395 taxa were registered, was conducted 15 years ago. However, this number is probably underrated. In this article, we present an updated checklist of angiosperm taxa in Bahia Coastal Forests (BCF) based on geographic distribution data available from the Brazilian Plant List (Flora do Brasil 2020). The records were checked in herbaria, recent taxonomic literature, and, when necessary, reviewed by experts. The final checklist consists of 547 taxa endemic to BCF, distributed in 69 families, with seven endemic genera: Bahiella (Apocynaceae), Santosia (Asteraceae), Harleyodendron (Fabaceae), Cubitanthus (Linderniaceae), Anomochloa and Parianella (Poaceae), and Andreadoxa (Rutaceae). The families with highest richness in endemic taxa were Bromeliaceae (108 spp.), Fabaceae (41 spp.) and Myrtaceae (32 spp.). This updated checklist shares only 143 taxa with a previous list published about 15 years ago. Those two lists differ mostly due to slightly different area limits, and to the large number of additional endemic species described since then. We hope our list will be used as a resource in future studies and contributes to the conservation of the highly diverse Bahia Coastal Forest.


Introduction
The Atlantic Forest is considered a biodiversity hotspot due to the occurrence of a high number of endemic and threatened species (Myers et al. 2000).The natural distribution of the Atlantic Forest was originally continuous along the Brazilian coast and extended to some areas in Argentina and Paraguay (Fundação SOS Mata Atlântica 2013).Nowadays, it is one of the eight most critically endangered hotspots, as only 12,5% of the original forest remains (Fundação SOS Mata Atlântica 2014).Nevertheless, it is the richest Brazilian phytogeographic domain in plant diversity, with 8,728 endemic species of angiosperms (Flora do Brasil 2020, under construction).
Some studies have emphasized the division of the Atlantic Forest in northern and southern regions (Cracraft 1985, Colombi et al. 2010, Martins 2011) with a limit along the Doce river, in the north of Espírito Santo state.The floristic differences between these two regions were highlighted by Oliveira-Filho & Fontes (2000) and Oliveira-Filho et al. (2005), who observed several taxa with Amazonian affinities occuring in the northern region, while taxa with subtropical Andean affinities are mostly found in the southern region (Berry et al. 2004, Santos et al. 2007, Menini Neto et al. 2016).Other authors recognize three main centers of endemism in the Atlantic Forest: northern (Pernambuco and Alagoas states), southern (from Rio de Janeiro to Santa Catarina states), and central (southern Bahia and Espírito Santo states) (Murray-Smith et al. 2009, Thomas et al. 1998).
Recently, Saiter et al. (2016a) divided the central region of the Atlantic Forest in three subregions based on the composition of tree species, indicating the most important abiotic factors affecting that division.Contrary to previous knowledge, the rivers did not play an important role in this division, which lies about 100 km north of the Doce river and is best explained by climatic factors, such as moisture, elevation and temperature (Saiter et al. 2016a).One of the regions, referred to as Bahia Coastal Forests (BCF) by Saiter et al. (2016a), encompasses the northern extreme of Espírito Santo and most of the coast of the state of Bahia.Due to high biodiversity and the incidence of endemic and threatened species, this region has been designated as a hot-point within the Atlantic Forest hotspot (Martini et al. 2007).Many studies to this date on different groups of organisms support this claim, as the region is considered an area of endemism for frogs (Carnaval et al. 2009), birds (Silva et al. 2004), Myrtaceae (Murray-Smith et al. 2009) and trees in general (Thomas et al. 2003).
An estimate of endemic vascular plant species present in two protected areas in southern Bahia showed that the distribution of 59% of the species is restricted to Bahia and Espírito Santo states (Thomas et al. 1998).These results motivated the compilation of a preliminary list of endemic angiosperm species in the region comprising Espírito Santo to the north of the Doce river and the south of Bahia, including inland Seasonal Dry Forests (Thomas et al. 2003) (Figure 1a).This list consisted of 395 endemic species of angiosperms in the region (Thomas et al. 2003) (Thomas et al, 2003).
Checklists of endemic taxa are critical to overcome issues that hinder conservation strategies in highly biodiverse regions, such as: 1) basic taxonomic information (Linnean shortfall, or "which species are there?"),and 2) lack of geographic information (Wallacean shortfall, or "where do these species occur?") (Whittaker et al. 2005).Both shortfalls are part of reality in Bahia Coastal Forests, world-renowned as one of the highest diversity areas in tree species (Thomas et al. 1998, Martini et al. 2007, Murray-Smith et al. 2009).
We aimed to provide a list of endemic species of angiosperms in Bahia Coastal Forest following Saiter et al. (2016a) to verify whether the current list agrees with the preliminary checklist by Thomas et al. (2003).We expect this updated list to further highlight the importance of BCF as a critical area for biodiversity conservation in the Brazilian Atlantic forest.

Study area
To delimit the study area we used the BCF sensu Saiter et al. (2016a) (Figure 1b) with a slight modification to include the municipalities whose territory was at least 50% inside that perimeter.Municipalities were used as a base for the retrieval of taxonomic information from online datasets (see data collection).To remove the arbitrary northern limit from Saiter et al. (2016a) (Figure 1b), the study area was expanded to include seven municipalities complying with the 50% territory criterion (Figure 1c).Municipal limits were defined based on data from the Brazilian Institute for Geography and Statistics (IBGE 1993) (Figure 1c).
The resulting area comprised 156 municipalities, which account for approximately 99,000 km 2 (Figure 1c) at southern Bahia state, and a small fraction from northern Espírito Santo state and northeastern Minas Gerais state, contrasting with an area of about 119,000 km 2 at southern Bahia which included more inland areas, and northen Espírito Santo with a southern limit at the Doce River (Thomas et al. 2003) (Figure 1a).

Data collection
To compile the checklist of endemic species of angiosperms in BCF, we started by performing a data search in the Brazilian Plant List (Flora do Brasil 2020) on March 9, 2017, using the following filters simultaneously: "group: angiosperms", "endemism: only endemic to Brazil", "origin: native", "state: Bahia", and "phytogeographic domain: Atlantic Forest".We decided not to search only for species endemic to the Atlantic Forest in Bahia to avoid excluding species that could also occur in the north of Espírito Santo and in a small area in northeastern Minas Gerais (Figure 1c).The initial search resulted in 3,338 species, 59 subspecies and 154 varieties (3,551 taxa).These records were then checked in the SpeciesLink database (splink.cria.org.br).Each taxon map generated by the SpeciesLink website was visually checked, first to remove taxa that were clearly not endemic to BCF, i.e. those with several records outside the study area.Each of the 1,336 remaining taxa were then mapped with QGis 2.14 (Quantum GIS Development Team 2016) and we verified whether the points of occurrence were enclosed in the limits of the study area, which resulted in the further removal of 701 taxa.From the 635 taxa left, the records with incongruent data were verified by experts or checked using recent taxonomic studies (Appendix 1).This step resulted in 30 additional non-endemic species discarded from the list.The taxa for which no scientific records were found in Google Scholar (scholar.google.com),Biodiversity Heritage Library (biodiversitylibrary.com), SpeciesLink (splink.cria.org.br), and the Brazilian Plant List (Flora do Brasil 2020) were complemented by a search for location records in the CEPEC herbarium.Once this verification was completed, 53 species from the list had to be removed because no records were available and a further five species were removed due to lack of precise geographic information.

Results
The final checklist consisted of 547 angiosperm taxa endemic to BCF (535 species, six subspecies, and six varieties) in 69 families (none endemic) and 230 genera (Table 1).Seven genera are endemic to BCF: Bahiella J.

Discussion
The families with the highest numbers of endemic taxa in BCF are also among the ten richest angiosperm families in Brazil and in the Atlantic Forest (BFG 2015).Thomas et al. (2003) reported Fabaceae (53 spp.) as the richest family of a total of 65 families in the previous list.Compared with the BFG (2015), it is remarkable that Orchidaceae, one of the three richest families in Brazil and in the Atlantic Forest, was not among the richest families in this study, with only 25 taxa.This may be due to the lack of geographic records for 14 species in this family, which had to be discarded.

Acanthaceae
Aphelandra ignea Nees ex Steud.The occurrence of only 12 endemic species of Conchocarpus in the present checklist probably indicates that several endemic species of this genus are exclusively found at more inland seasonally dry forests (Kallunki & Pirani 1998).

Malvaceae
Among the endemic genera from southern Bahia and northern Espírito Santo reported by Thomas et al. (2003), such as Arapatiella and Brodriguesia (Fabaceae), Atractantha, Alvimia and Sucrea (Poaceae), and Trigoniodendron (Trigoniaceae), several are not endemic to BCF.For example, Brodriguesia, Atractantha and Trigoniodendron have been recorded outside our study area, respectively, in Sergipe, Amazonas, and near the Doce River.Similarly, Physeterostemon R.Goldenb.& Amorim (Melastomataceae), a recently described endemic genus from the Atlantic Forest of Bahia state (Amorim et al. 2014, Goldenberg et al. 2016, Goldenberg & Amorim 2006), was not considered endemic to BCF in this checklist, as among its species P. gomesii Amorim & R.Goldenb.occurs in the municipality of Boa Nova (Amorim et al. 2014), which lies slightly outside our study area.
In comparison with the preliminary list of Thomas et al. (2003), which included 395 endemic angiosperm taxa from an area that covered a larger part of northern Espírito Santo state, as far as the Doce River, and the southern Bahia Atlantic Forest, including more inland areas, and almost reaching the municipality of Salvador (i.e., an area ca.20% larger than ours) (Figure 1a), the list presented here surprisingly shares only 143 taxa (Table 1).If we had used the Doce River as our area southern limit, it would have included at least 45 additional species restricted to the Linhares region, such as Cryptanthus beuckeri E.Morren (Bromeliaceae), Rourea luizalbertoi Forero, L.A.Vidal & Carbonó (Connaraceae), Simira eliezeriana Peixoto (Rubiaceae) and the endemic genus Riodocea Delprete (Thomas et al. 2003, Rolim et al. 2016).Despite being geographically close and having several species in common (Saiter et al. 2016b), the vegetation of Linhares and the Doce River floodplain are ecologically different from the BCF (Rolim et al. 2005(Rolim et al. , 2006)).In floristic terms, the Linhares region may be more similar to northern Rio de Janeiro, southern Espírito Santo (Silva & Nascimento 2001, Saiter et al. 2016b) and eastern Minas Gerais states (see Krenák-Waitaká Forests sensu Saiter et al. 2016a).
Another difference between the two checklists is due to the time gap of about 15 years between studies.A total of 174 species in our checklist were described after 2003, probably due to increased efforts

Figure 1 .
Figure 1.a) Study area in which Thomas et al. (2003) based their list of endemic species.b) Bahia Coastal Forest (BCF) according to Saiter et al. (2016a).c) Municipalities with at least 50% of its area within the BCF (light grey), and those added to the study area based on IBGE (1993) (dark grey).Coordinates: UTM.Datum WGS 84.

Table 1 .
Checklist of angiosperms endemic to Bahia Coastal Forest sensu