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

Angiospermas endêmicas da Floresta Costeira da Bahia, Brasil: uma atualização utilizando uma nova delimitação de área

Abstract:

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 2020FLORA DO BRASIL 2020 under construction. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (acessed on 09/Mar/2017)
http://floradobrasil.jbrj.gov.br/...
). 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.

Keywords:
Atlantic Forest; checklist; conservation; endemism; hotspot

Resumo:

A floresta costeira do estado da Bahia, no nordeste do Brasil, tem sido apontada como área de endemismo para diversos grupos de organismos. O primeiro levantamento de espécies de angiospermas endêmicas dessa região foi realizado há cerca de 15 anos e revelou a ocorrência de 395 táxons. Entretanto, esse número provavelmente está subestimado. Neste trabalho apresentamos uma lista atualizada de táxons de angiospermas endêmicas da Floresta Costeira da Bahia (FCB), tendo como base as informações de distribuição geográfica disponíveis na lista da Flora do Brasil. Estas informações foram posteriormente checadas em registros de herbários, estudos taxonômicos recentes e, quando necessário, revisadas por especialistas. A lista final de espécies é constituída por 547 táxons endêmicos da Floresta Costeira da Bahia, distribuídos em 69 famílias e incluindo sete gêneros endêmicos: Bahiella (Apocynaceae), Santosia (Asteraceae), Harleyodendron (Fabaceae), Cubitanthus (Linderniaceae), Anomochloa e Parianella (Poaceae), and Andreadoxa (Rutaceae). As famílias mais ricas em táxons endêmicos são Bromeliaceae (108 spp.), Fabaceae (41 spp.) e Myrtaceae (32 spp.). Apenas 143 táxons são compartilhados por esta lista atualizada e uma lista preliminar publicada há cerca de 15 anos. As duas listas diferem especialmente por ligeiras diferenças nos limites da área de estudo e também pelo acréscimo de novas espécies endêmicas descritas desde então. Espera-se que a lista seja usada como ferramenta para estudos futuros e para a conservação da rica flora costeira da Bahia.

Palavras-chave:
Checklist; conservação; endemismo; hotspot; Mata Atlântica

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. 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403(6772):853-858.). 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 2013FUNDAÇÃO SOS MATA ATLÂNTICA. 2013. Atlas dos remanescentes florestais da Mata Atlântica Período 2011-2012.). Nowadays, it is one of the eight most critically endangered hotspots, as only 12,5% of the original forest remains (Fundação SOS Mata Atlântica 2014FUNDAÇÃO SOS MATA ATLÂNTICA. 2014. Atlas dos remanescentes florestais da Mata Atlântica Período 2012-2013.). Nevertheless, it is the richest Brazilian phytogeographic domain in plant diversity, with 8,728 endemic species of angiosperms (Flora do Brasil 2020, under constructionFLORA DO BRASIL 2020 under construction. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (acessed on 09/Mar/2017)
http://floradobrasil.jbrj.gov.br/...
).

Some studies have emphasized the division of the Atlantic Forest in northern and southern regions (Cracraft 1985CRACRAFT, J. 1985. Historical Biogeography and Patterns of Differentiation within the South American Avifauna : Areas of Endemism. Ornithol. Monogr. 36:49-84., Colombi et al. 2010COLOMBI, V.H., LOPES, S.R. & FAGUNDES, V. 2010. Testing the Rio Doce as a riverine barrier in shaping the atlantic rainforest population divergence in the rodent Akodon cursor. Genet. Mol. Biol. 33(4):785-789., Martins 2011MARTINS, F.M. 2011. Historical biogeography of the Brazilian Atlantic forest and the Carnaval-Moritz model of Pleistocene refugia: What do phylogeographical studies tell us? Biol. J. Linn. Soc. 104(3):499-509.) 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)OLIVEIRA‐FILHO, A. & FONTES, M. 2000. Patterns of Floristic Differentiation among Atlantic Forests in Southeastern Brazil and the Influence of Climate. Biotropica 32(4b):793-810. and Oliveira-Filho et al. (2005)OLIVEIRA-FILHO, A.T., TAMEIRÃO-NETO, E., CARVALHO, W.A.C., WERNECK, M., BRINA, A.E., VIDAL, C. V, REZENDE, S.C. & PEREIRA, J.A.A. 2005. Análise florística do compartimento arbóreo de áreas de floresta atlântica sensu lato na região das Bacias do Leste (Bahia, Minas Gerais, Espírito Santo e Rio de Janeiro). Rodriguésia 56(87):185-235., 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. 2004BERRY, P.E., HAHN, W.J., SYTSMA, K.J., HALL, J.C. & MAST, A. 2004. Phylogenetic relationships and biogeography of Fuchsia (Onagraceae) based on noncoding nuclear and chloroplast DNA data. Am. J. Bot. 91(4):601-614., Santos et al. 2007SANTOS, M.M., CAVALCANTI, D.R., SILVA, J.M.C. da & TABARELLI, M. 2007. Biogeographical relationships among tropical forests in north-eastern Brazil. J. Biogeogr. 34(3):437-446., Menini Neto et al. 2016MENINI NETO, L., FURTADO, S.G., ZAPPI, D.C., OLIVEIRA FILHO, A.T. & FORZZA, R.C. 2016. Biogeography of epiphytic Angiosperms in the Brazilian Atlantic forest, a world biodiversity hotspot. Rev. Bras. Bot. 39(1):261-273.). 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. 2009MURRAY-SMITH, C., BRUMMITT, N.A., OLIVEIRA-FILHO, A.T., BACHMAN, S., MOAT, J., LUGHADHA, E.M.N. & LUCAS, E.J. 2009. Plant diversity hotspots in the Atlantic coastal forests of Brazil. Conserv. Biol. 23(1):151-163., Thomas et al. 1998THOMAS, W.W., CARVALHO, A.M. V, AMORIM, A.M., GARRISON, J. & ARBELAÉZ, A.L. 1998. Plant endemism in two forests in southern Bahia, Brazil. Biodivers. Conserv. 7:311-322.).

Recently, Saiter et al. (2016a)SAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331. 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. 2016aSAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331.). One of the regions, referred to as Bahia Coastal Forests (BCF) by Saiter et al. (2016a)SAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331., 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. 2007MARTINI, A.M.Z., FIASCHI, P., AMORIM, A.M. & PAIXÃO, J.L. 2007. A hot-point within a hot-spot: A high diversity site in Brazil's Atlantic Forest. Biodivers. Conserv. 16(11):3111-3128.). 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. 2009CARNAVAL, A.C., HICKERSON, M.J., HADDAD, C.F.B., RODRIGUES, M.T. & MORITZ, C. 2009. Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323(5915):785-789.), birds (Silva et al. 2004SILVA, J.M.C., SOUSA, M.C. & CASTELLETTI, C.H.M. 2004. Areas of endemism for passerine birds in the Atlantic forest, South America. Glob. Ecol. Biogeogr. 13:85-92.), Myrtaceae (Murray-Smith et al. 2009MURRAY-SMITH, C., BRUMMITT, N.A., OLIVEIRA-FILHO, A.T., BACHMAN, S., MOAT, J., LUGHADHA, E.M.N. & LUCAS, E.J. 2009. Plant diversity hotspots in the Atlantic coastal forests of Brazil. Conserv. Biol. 23(1):151-163.) and trees in general (Thomas et al. 2003THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP.).

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. 1998THOMAS, W.W., CARVALHO, A.M. V, AMORIM, A.M., GARRISON, J. & ARBELAÉZ, A.L. 1998. Plant endemism in two forests in southern Bahia, Brazil. Biodivers. Conserv. 7:311-322.). 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. 2003THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP.) (Figure 1a). This list consisted of 395 endemic species of angiosperms in the region (Thomas et al. 2003THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP.), among which several are known to occur only in dry forests, such as Chrysophyllum subspinosum Monach. (Sapotaceae) and Colicodendron bahianum Cornejo & Ilts (Capparaceae). That study reported eight endemic genera in this area: Arapatiella R.S.Cowan, Brodriguesia R.S.Cowan and Harleyodendron R.S.Cowan (Fabaceae), Atractantha McClure, Anomochloa Brogn., Alvimia Calderón ex Soderstr. & Londoño, and Sucrea Soderstr. (Poaceae), and Trigoniodendron E.F.Guim & Miguel (Trigoniaceae) (Thomas et al, 2003THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP.).

Figure 1
a) Study area in which Thomas et al. (2003)THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP. based their list of endemic species. b) Bahia Coastal Forest (BCF) according to Saiter et al. (2016a)SAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331.. 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)IBGE. 1993. Mapa de Vegetação do Brasil. 2nd ed. Diretoria de Geociências, Rio de Janeiro. (dark grey). Coordinates: UTM. Datum WGS 84.

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. 2005WHITTAKER, R.J., ARAÚJO, M.B., JEPSON, P., LADLE, R.J., WATSON, J.E.M. & WILLIS, K.J. 2005. Conservation biogeography: Assessment and prospect. Divers. Distrib. 11(1):3-23.). 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. 1998THOMAS, W.W., CARVALHO, A.M. V, AMORIM, A.M., GARRISON, J. & ARBELAÉZ, A.L. 1998. Plant endemism in two forests in southern Bahia, Brazil. Biodivers. Conserv. 7:311-322., Martini et al. 2007MARTINI, A.M.Z., FIASCHI, P., AMORIM, A.M. & PAIXÃO, J.L. 2007. A hot-point within a hot-spot: A high diversity site in Brazil's Atlantic Forest. Biodivers. Conserv. 16(11):3111-3128., Murray-Smith et al. 2009MURRAY-SMITH, C., BRUMMITT, N.A., OLIVEIRA-FILHO, A.T., BACHMAN, S., MOAT, J., LUGHADHA, E.M.N. & LUCAS, E.J. 2009. Plant diversity hotspots in the Atlantic coastal forests of Brazil. Conserv. Biol. 23(1):151-163.).

We aimed to provide a list of endemic species of angiosperms in Bahia Coastal Forest following Saiter et al. (2016a)SAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331. to verify whether the current list agrees with the preliminary checklist by Thomas et al. (2003)THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP.. We expect this updated list to further highlight the importance of BCF as a critical area for biodiversity conservation in the Brazilian Atlantic forest.

Material and Methods

1. Study area

To delimit the study area we used the BCF sensuSaiter et al. (2016a)SAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331. (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)SAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331. (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 1993IBGE. 1993. Mapa de Vegetação do Brasil. 2nd ed. Diretoria de Geociências, Rio de Janeiro.) (Figure 1c).

The resulting area comprised 156 municipalities, which account for approximately 99,000 km2 (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 km2 at southern Bahia which included more inland areas, and northen Espírito Santo with a southern limit at the Doce River (Thomas et al. 2003THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP.) (Figure 1a).

2. 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 2020FLORA DO BRASIL 2020 under construction. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (acessed on 09/Mar/2017)
http://floradobrasil.jbrj.gov.br/...
) 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 2016QUANTUM GIS DEVELOPMENT TEAM. 2016. Quantum GIS Geographic Information System. Open Source Geospatial Found. Proj.) 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.F.Morales (Apocynaceae), Santosia R.M.King & H.Rob. (Asteraceae), Harleyodendron (Fabaceae, Figure 2f), Cubitanthus Barringer (Linderniaceae), Anomochloa and Parianella Hollowell, F.M.Ferreira & R.P.Oliveira (Poaceae), and Andreadoxa Kallunki (Rutaceae). The genera with the highest number of endemic species in the BCF were Aechmea Ruiz & Pav. (Bromeliaceae) (33 spp.), Pavonia Cav. (Malvaceae) and Myrcia DC. (Myrtaceae), each with 16 species. The three families with the highest numbers of endemic taxa (species + infraspecific taxa) were Bromeliaceae (108), Fabaceae (41) and Myrtaceae (32).

Table 1
Checklist of angiosperms endemic to Bahia Coastal Forest sensu Saiter et al. (2016a)SAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331..

Figure 2
Some species found in the checklist of endemic angiosperms of BCF: a) Kuhlmanniodendron macrocarpum (Achariaceae). b) Quesnelia koltesii (Bromeliaceae). c) Dichorisandra leucophtalmos (Commelinaceae). d) Tapura zei-limae (Dichapetalaceae). e) Arapatiella psilophylla (Fabaceae). f) Harleyodendron unifoliolatum (Fabaceae). g) Pavonia goetheoides (Malvaceae). h) Pleiochiton amorimii (Melastomataceae). i) Anomochloa marantoidea (Poaceae). Photos: a, b, d, g, h) A.Amorim; c) L.Aona; e, f) D.Cardoso; i) J.Jardim.

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 2015BFG. 2015. Growing knowledge: An overview of Seed Plant diversity in Brazil. Rodriguésia 66(4):1085-1113.). Thomas et al. (2003)THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP. reported Fabaceae (53 spp.) as the richest family of a total of 65 families in the previous list. Compared with the BFG (2015)BFG. 2015. Growing knowledge: An overview of Seed Plant diversity in Brazil. Rodriguésia 66(4):1085-1113., 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.

Among the 20 richest angiosperm genera in Brazil (BFG 2015BFG. 2015. Growing knowledge: An overview of Seed Plant diversity in Brazil. Rodriguésia 66(4):1085-1113.), Aechmea and Myrcia are also among the genera with the highest number of endemic species in the BCF. In a preliminary list of the endemic angiosperm species from southern Bahia and northern Espírito Santo, Thomas et al. (2003)THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP. cited Conchocarpus J.C.Mikan (Rutaceae) (19 spp.) as the richest genus, followed by Pavonia Cav. (Malvaceae) (13 spp.), Couepia Aubl., and Erythroxylum P.Browne (seven spp. each). 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 1998KALLUNKI, J.A. & PIRANI, J.R. 1998. Synopses of Angostura Roem. & Schult. and Conchocarpus J. C. Mikan (Rutaceae). Kew Bull. 53(2):257-334.).

Among the endemic genera from southern Bahia and northern Espírito Santo reported by Thomas et al. (2003)THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP., 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. 2014AMORIM, A.M., JARDIM, J.G. & GOLDENBERG, R. 2014. Physeterostemon gomesii (Melastomataceae): the fourth species of this endemic genus in Bahia, Brazil. Phytotaxa 175(1):45-50., Goldenberg et al. 2016GOLDENBERG, R., MICHELANGELI, F.A., AONA, L.Y.S. & AMORIM, A.M. 2016. Angiosperms and the Linnean shortfall: three new species from three lineages of Melastomataceae at one spot at the Atlantic Forest. PeerJ 4:1824-1833., Goldenberg & Amorim 2006GOLDENBERG, R. & AMORIM, A.M. 2006. Physeterostemon (Melastomataceae): a new genus and two new species from the Bahian Atlantic Forest, Brazil. Taxon 55(4):965-972.), 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. 2014AMORIM, A.M., JARDIM, J.G. & GOLDENBERG, R. 2014. Physeterostemon gomesii (Melastomataceae): the fourth species of this endemic genus in Bahia, Brazil. Phytotaxa 175(1):45-50.), which lies slightly outside our study area.

In comparison with the preliminary list of Thomas et al. (2003)THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP., 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. 2003THOMAS, W.W., JARDIM, J.G., FIASCHI, P. & AMORIM, A.M. 2003. Lista preliminar das Angiospermas localmente endêmicas do Sul da Bahia e Norte do Espírito Santo, Brasil. In Corredor de Biodiversidade da Mata Atlântica do Sul da Bahia (PRADO, P.I., LANDAU, E.C., MOURA, R.T., PINTO, L.P.S., FONSECA, G.A.B. & ALGER, K. orgs.). Published in CD-ROM, Ilhéus, IESB/ CI/ CABS/ UFMG/ UNICAMP., Rolim et al. 2016ROLIM, S.G., MAGNAGO, L.F.S., SAITER, F.Z., AMORIM, A.M. & ABREU, K.M.P. de. 2016. São as florestas do norte do espírito santo e sul da bahia as mais ricas em espécies arbóreas no domínio da floresta atlântica? In Floresta Atlântica de Tabuleiro: diversidade e endemismo na Reserva Natural Vale (A. C. Rolim, Samil Gonçalves; Menezes, Luis F. T. de; Srbek-Araujo, ed.). Editora Rona, Belo Horizonte, p.91-100.). Despite being geographically close and having several species in common (Saiter et al. 2016bSAITER, F.Z., ROLIM, S.G. & DE OLIVEIRA-FILHO, A.T. 2016b. A floresta de Linhares no contexto fitogeográfico do leste do Brasil. In Floresta Atlântica de Tabuleiro: diversidade e endemismo na Reserva Natural Vale (A. C. Rolim, Samil Gonçalves; Menezes, Luis F. T. de; Srbek-Araujo, ed.). Editora Rona, Belo Horizonte, p.61-69.), the vegetation of Linhares and the Doce River floodplain are ecologically different from the BCF (Rolim et al. 2005ROLIM, S.G., JESUS, R.M., NASCIMENTO, H.E.M., DO COUTO, H.T.Z. & CHAMBERS, J.Q. 2005. Biomass change in an Atlantic tropical moist forest: The ENSO effect in permanent sample plots over a 22-year period. Oecologia 142(2):238-246., 2006ROLIM, S.G., IVANAUSKAS, N.M., RODRIGUES, R.R., NASCIMENTO, M.T., GOMES, J.M.L., FOLLI, D.A. & COUTO, H.T.Z. do. 2006. Composição Florística do estrato arbóreo da Floresta Estacional Semidecidual na Planície Aluvial do rio Doce, Linhares, ES, Brasil. Acta Bot. Brasilica 20(3):549-561.). In floristic terms, the Linhares region may be more similar to northern Rio de Janeiro, southern Espírito Santo (Silva & Nascimento 2001SILVA, G.C. da & NASCIMENTO, M.T. 2001. Fitossociologia de um remanescente de mata sobre tabuleiros no norte do estado do Rio de Janeiro (Mata do Carvão). Rev. Bras. Botânica 24(1):51-62., Saiter et al. 2016bSAITER, F.Z., ROLIM, S.G. & DE OLIVEIRA-FILHO, A.T. 2016b. A floresta de Linhares no contexto fitogeográfico do leste do Brasil. In Floresta Atlântica de Tabuleiro: diversidade e endemismo na Reserva Natural Vale (A. C. Rolim, Samil Gonçalves; Menezes, Luis F. T. de; Srbek-Araujo, ed.). Editora Rona, Belo Horizonte, p.61-69.) and eastern Minas Gerais states (see Krenák-Waitaká Forests sensuSaiter et al. 2016aSAITER, F.Z., BROWN, J.L., THOMAS, W.W., DE OLIVEIRA-FILHO, A.T. & CARNAVAL, A.C. 2016a. Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. J. Biogeogr. 43(12):2322-2331.).

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 in collecting and studying plants in the Atlantic Forest in Bahia. For instance, about 41.5% of all new angiosperms in the Brazilian flora described between 1990 and 2006 are endemic to the Atlantic Forest (Sobral & Stehmann 2009SOBRAL, M. & STEHMANN, J.R. 2009. An analysis of new angiosperm species discoveries in Brazil (1990-2006). Taxon 58(1):227-232.). Moreover, 23 species of angiosperms endemic to BCF were described between 2015 and 2017 (e.g., Araújo et al. 2015ARAÚJO, T., FIASCHI, P. & AMORIM, A.M. 2015. Erythroxylum riparium (Erythroxylaceae), a new species from the Brazilian Atlantic Forest. Phytotaxa 230(1):75-80., Santos et al. 2015SANTOS, M.F., LUCAS, E., SOBRAL, M. & SANO, P.T. 2015. New species of Myrcia s.l. (Myrtaceae) from Campo Rupestre, Atlantic Forest and Amazon Forest. Phytotaxa 222(2):100-110., Abreu & Giulietti 2016ABREU, I.S. & GIULIETTI, A.M. 2016. Aristolochia brunneomaculata, a new threatened species of Aristolochiaceae from the Atlantic Forest in Bahia, Brazil. Sitientibus 16:10.13102/scb1060.
https://doi.org/10.13102/scb1060...
, Amorim et al. 2016AMORIM, A.M., LISBOA, D.S., MARINHO, L.C. & FIASCHI, P. 2016. Novelties in Tapura (Dichapetalaceae) from the Brazilian Atlantic Forest. Syst. Bot. 41(3):747-757., Côrtes et al. 2016CÔRTES, A.L.A., DANIEL, T.F. & RAPINI, A. 2016. Taxonomic revision of the genus Schaueria (Acanthaceae). Plant Syst. Evol. 302:819-851., Ferreira et al. 2016FERREIRA, F.M., HOLLOWELL, V.C. & OLIVEIRA, R.P. 2016. Eremitis linearifolia and E. robusta (Poaceae, Bambusoideae, Olyreae): two new species of herbaceous bamboos from Brazil first collected over 30 years ago. Phytotaxa 280(2):179-189., Marinho & Lucas 2016MARINHO, L.C. & LUCAS, E. 2016. A New Species of Myrcia sect. Aulomyrcia (Myrtaceae) from the restingas of Bahia, Brazil. Phytotaxa 280(3):285-291., Popovkin et al. 2016POPOVKIN, A. V, FARIA, A.D.D.E. & SWENSON, U.L.F. 2016. Pouteria synsepala (Sapotaceae: Chrysophylloideae): a new species from the northern littoral of Bahia, Brazil. Phytotaxa 286(1):39-46., Ribeiro et al. 2016RIBEIRO, M., MORI, S.A., ALVES-ARAÚJO, A. & PEIXOTO, A.L. 2016. A new species of Eschweilera (Lecythidaceae) from the Brazilian Atlantic Forest. Phytotaxa 255(3):267-273., Terra-Araujo et al. 2016TERRA-ARAUJO, M.H., FARIA, A.D. & SWENSON, U. 2016. A taxonomic update of Neotropical Pradosia (Sapotaceae, Chrysophylloideae). Syst. Bot. 41(3):634-650., Daly & Melo 2017DALY, D.C. & MELO, M. da F. 2017. Four new species of Trattinnickia from South America. Studies in Neotropical Burseraceae XXII. Brittonia 69(3):376-386., Gonçalez et al. 2017GONÇALEZ, V.M., PFEIL, B.E., ANTONELLI, A. & DUARTE, M.C. 2017. Two new species of Pavonia (Malvoideae, Malvaceae) from southern Bahia, Brazil. Phytotaxa 305(2):97-103.).

Compared to the results of a search in the Brazilian Plant List (Flora do Brasil 2020, under constructionFLORA DO BRASIL 2020 under construction. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (acessed on 09/Mar/2017)
http://floradobrasil.jbrj.gov.br/...
) using the following filters: "group: angiosperms", "endemism: only endemic to Brazil", "occurrence: only occurs in", "origin: native", "state: Bahia", and "phytogeographic domain: Atlantic Forest", the number of species in our checklist (547 spp.) was much smaller than the 795 species identified by the search engine. Among the reasons for this large difference (248 spp.) it is worth mentioning that a) more than 50 taxa from our list had to be removed due to lack of precise geospatial data, such as the municipality name, which precluded us from citing them as endemic to BCF; b) among the taxa exclusive to the Brazilian Plant List (Flora do Brasil 2020, under constructionFLORA DO BRASIL 2020 under construction. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (acessed on 09/Mar/2017)
http://floradobrasil.jbrj.gov.br/...
) that are not restricted to BCF, several occur in more inland seasonally dry forests in the Atlantic Forest, such as Chrysophyllum subspinosum Monach. (Sapotaceae) and Colicodendron bahianum Cornejo & Iltis (Capparaceae); and c) at least 29 species exclusive to the Brazilian Plant List search occur close to, but outside the study area, such as Canistrum camacaense Martinelli & Leme (Bromeliaceae), Inga grazielae (Vinha) T.D.Penn. (Fabaceae), and Bertolonia carmoi Baumgratz (Melastomataceae), all from the municipality of Boa Nova, and Aechmea bicolor L.B.Sm. (Bromeliaceae), Heteropterys jardimii Amorim (Malpighiaceae), and Passiflora timboensis T.S.Nunes & L.P.Queiroz (Passifloraceae), from the municipality of Santa Teresinha.

There are additional reasons to anticipate that the difference in species numbers between the Brazilian Plant List and our list could be even greater, as the list presented here includes 84 taxa that also occur in northern Espírito Santo and in a small area in northeastern Minas Gerais (Figure 1c). Moreover, the Brazilian Plant List (Flora do Brasil 2020, under constructionFLORA DO BRASIL 2020 under construction. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ (acessed on 09/Mar/2017)
http://floradobrasil.jbrj.gov.br/...
) is an ongoing project on which new taxa can be continuously added and identified as endemic, what could bring the total number of endemic angiosperm species using the same filters even larger. Alternatively, if the native distribution of several taxa is shown to extend beyond the Atlantic Forest domain in Bahia, the difference between the lists could decrease, as fewer species from the Brazilian Plant List would appear as endemic while applying the same search filters.

Developing knowledge on patterns of endemism for plant species is extremely important and must be taken into account in conservation strategies. This information is relevant for the establishment of new protected areas (Kerr 1997KERR, J.T. 1997. Species Richness, Endemism, and the Choice of Areas for Conservation. 11(5):1094-1100.), restoration policies (Chazdon 2008CHAZDON, R.L. 2008. Beyond Deforestation: Restoring Forests and Ecosystem Services on Degraded Lands. Science 320(5882):1458-1460.) and in directing additional studies (Francisco-Ortega et al. 2010FRANCISCO-ORTEGA, J., WANG, F.G., WANG, Z.S., XING, F.W., LIU, H., XU, H., XU, W.X., LUO, Y.B., SONG, X.Q., GALE, S., BOUFFORD, D.E., MAUNDER, M. & AN, S.Q. 2010. Endemic Seed Plant Species from Hainan Island: A Checklist. Bot. Rev. 76(3):295-345.). Considering the key role of endemic species in the design of conservation policies (Myers et al. 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403(6772):853-858., Van Der Werff & Consiglio 2004VAN DER WERFF, H. & CONSIGLIO, T. 2004. Distribution and conservation significance of endemic species of flowering plants in Peru. Biodivers. Conserv. 13(9):1699-1713., Moraes et al. 2005, Lamoreux et al. 2006LAMOREUX, J.F., MORRISON, J.C., RICKETTS, T.H., OLSON, D.M., DINERSTEIN, E., MCKNIGHT, M.W. & SHUGART, H.H. 2006. Global tests of biodiversity concordance and the importance of endemism. Nature 440(7081):212-214., Martinelli et al. 2008MARTINELLI, G., VIEIRA, C., GONZALEZ, M., LEITMAN, P.M., PIRATININGA, A., COSTA, A.F. & FORZZA, R.C. 2008. Bromeliaceae da Mata Atlântica Brasileira: lista de espécies, distribuição e conservação. Rodriguésia 59(1):209-258., Essl et al. 2009ESSL, F., STAUDINGER, M., STÖHR, O., SCHRATT-EHRENDORFER, L., RABITSCH, W. & NIKLFELD, H. 2009. Distribution patterns, range size and niche breadth of Austrian endemic plants. Biol. Conserv. 142(11):2547-2558., Nowak & Nobis 2010NOWAK, A. & NOBIS, M. 2010. Tentative list of endemic vascular plants of the Zeravshan Mts in Tajikistan: distribution, habitat preferences and conservation status of species. Biodivers. Res. Conserv. 19:65-80.), we expect this checklist could guide future studies and conservation strategies, as well as emphasize the importance of the BCF region as a key area for plant conservation.

Acknowledgements

The authors thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for awarding a Master Fellowship to POB, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Research Productivity Fellowship to AMA (grant # 310717/2015-9), and PF (grant # 306228/2016-5), and all specialists that provided updated information on endemic species distribution.

Supplementary material

The following online material is available for this article:

Appendix 1 - Taxonomic studies and specialists consulted by family.

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Publication Dates

  • Publication in this collection
    16 Aug 2018
  • Date of issue
    2018

History

  • Received
    29 Mar 2018
  • Reviewed
    11 July 2018
  • Accepted
    12 July 2018
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