Climbing plants from Seridó Ecological Station: diversity, interactive key and five new records from Rio Grande do Norte state, Brazil

Fernanda Gondim Lambert Moreira Víctor de Paiva Moreira Maurício Borges do Nascimento Luiza Fonseca Amorim de Paula Rodrigo de Loyola Dias Fernanda Antunes Carvalho About the authors

Abstract

In Brazil, Seasonally Dry Tropical Forests (SDTFs) are represented by Caatinga, which exhibits one of the greatest species richness and endemisms among the Neotropical SDTFs. However, studies of the flora of this biome remain deficient, especially in scientifically neglected areas, such as the Seridó region. Located between the states of Rio Grande do Norte (RN) and Paraíba, the Seridó region has an underestimated floristic diversity, especially for non-arboreal components such as climbers. Given this scenario, the study aimed to survey the climbers of the Seridó Ecological Station, a federal conservation unit located in the RN state, as well as to provide a multiple access online identification key. Collections were carried out from 2018 to 2019, as well as consultation of material deposited at the UFRN herbarium. In total, 56 species were listed, being 33 herbaceous and 23 woody climbers, respectively, adding 14 species of climbers to the previous checklist of the unit. Five new occurrences were found for the state of Rio Grande do Norte: Cuscuta globosa, Cuscuta partita (Convolvulaceae), Macroptilium bracteatum (Fabaceae), Heteropterys trichanthera and Tetrapterys longibracteata (Malpighiaceae), being the latest a new occurrence of the genus Tetrapterys for the state. Convolvulaceae is the most representative family (18 spp.), followed by Fabaceae (10 spp.), Apocynaceae (eight spp.) and Cucurbitaceae (five spp.). This is the first study that provides an interactive identification key for the Seridó region and for the RN state. The interactive identification key is published throughout the Xper³ platform, and can be accessed at <xper3.fr/xper3GeneratedFiles/publish/identification/-4505993480748774750/mkey.html>.

Key words
caatinga; seasonally dry tropical forests; lianas; virtual taxonomy

Resumo

No Brasil, as Florestas Tropicais Sazonalmente Secas (FTSS) são representadas pela Caatinga, que exibe uma das maiores riquezas de espécies e endemismos dentre as FTSS Neotropicais. Contudo, o bioma segue deficiente quanto ao estudo da flora, principalmente em áreas negligenciadas cientificamente, como a região do Seridó. Localizada entre os estados do Rio Grande do Norte (RN) e Paraíba, o Seridó possui uma diversidade florística subestimada, principalmente em componentes não arbóreos, como as trepadeiras. Diante deste cenário, o trabalho teve como objetivo realizar um levantamento das trepadeiras da Estação Ecológica do Seridó, unidade de conservação federal localizada no estado do RN, bem como disponibilizar uma chave de identificação de múltiplo acesso online. Foram realizadas coletas entre 2018 e 2019 nessa unidade, bem como consulta de material depositado no herbário UFRN. Foram listadas 56 espécies de trepadeiras, sendo 33 herbáceas e 23 lenhosas, adicionando 14 espécies de trepadeiras ao checklist anterior da unidade. Cinco novas ocorrências foram encontradas para o estado do RN: Cuscuta globosa, Cuscuta partita (Convolvulaceae), Macroptilium bracteatum (Fabaceae), Heteropterys trichanthera e Tetrapterys longibracteata (Malpighiaceae), sendo a última nova ocorrência do gênero Tetrapterys para o estado. Convolvulaceae é a família mais representativa (18 spp.), seguida de Fabaceae (10 spp.), Apocynaceae (oito spp.) e Cucurbitaceae (cinco spp.). Este é o primeiro estudo que fornece uma chave de identificação interativa para a região do Seridó e para o estado do RN. A chave interativa para identificação das espécies está hospedada na plataforma Xper³, e pode ser acessada em <xper3.fr/xper3GeneratedFiles/publish/identification/-4505993480748774750/mkey.html>.

Palavras-chave
caatinga; florestas tropicais sazonalmente secas; lianas; taxonomia virtual

Introduction

The Seasonally Dry Tropical Forests (SDTF) are formations characterized by the seasonal distribution of rainfall that result in several months of severe drought (Mooney et al. 1995Mooney HA, Bullock SH & Medina E (1995) Introduction In: Bullock SH, Mooney HA & Medina E (eds.) Seasonally dry tropical forests. Cambridge University Press, Cambridge. Pp. 1-21.). In the Neotropical region it is distributed in dispersed areas, from northwestern Mexico to northern Argentina and the Caribbean region, with 54.2% of its extension present only in South America (Linares-Palomino et al. 2011Linares-Palomino R, Oliveira-Filho A & Pennington R (2011) Neotropical seasonally dry forests: diversity, endemism, and biogeography of woody plants. In: Dirzo R, Young HS, Mooney HA & Ceballos G (eds.) Seasonally dry tropical forests: ecology and conservation. Vol. 1. Ed. Island Press, Washington D.C. Pp. 03-21.; Miles et al. 2006Miles L, Newton AC, DeFries RS, Ravilious C, May I, Blyth S, Kapos V & Gordon JE (2006) A global overview of the conservation status of tropical dry forests. Journal of Biogeography 33: 491-505.). The Caatinga, located in Northeast Brazil, is the largest fragment of Seasonally Dry Tropical Forests (SDTFs) in the neotropical region, with one of the greatest species richness and endemism among these formations (Prado 2003Prado DE (2003) As caatingas da Américas do Sul. In: Leal IR, Tabarelli M & Silva JMC (eds.) Ecologia e conservação da Caatinga. Vol. 1. Ed. Universitária UFPE, Pernambuco. Pp. 3-73. ; Dryflor 2016Dryflor (2016) Plant diversity patterns in neotropical dry forests and their conservation implications. Science 353: 1383-1387.). Considered to be the most populous semi-arid region in the world, the Caatinga remains neglected by researchers and conservationists and thus vulnerable to the impact of unsustainable use of natural resources (Santana et al. 2009Santana JADS, Pimenta AS, Souto JS, Almeida FV & Pacheco MV (2009) Levantamento florístico e associação de espécies na caatinga da Estação Ecológica do Seridó, Serra Negra do Norte - RN - Brasil. Revista Verde 4: 83-89.). Despite the high level of degradation, the Caatinga still has well-preserved regions and comprises a considerable number of rare and endemic taxa (Giulietti et al. 2004Giulietti AM, du Bocage Neta AL, Castro AAJF, Gamarra-Rojas CFL, Sampaio EVSB, Virgínio JF, Queiroz LP, Figueiredo MA & Rodal MJN (2004) Diagnóstico da vegetação nativa do bioma Caatinga In: Silva JMC, Tabarelli M, Fonseca MT & Lins LV (eds.) Biodiversidade da caatinga: áreas e ações prioritárias para a conservação. Vol. 1. Ed. Ministério do Meio Ambiente, Brasilia. Pp. 3-64.).

The Caatinga vegetation displays unique adaptations to survive in a hostile environment, with extremely low rainfall and prolonged dry season, contrasting to those found in neighboring regions such as the Amazon and the Atlantic Forest (Queiroz et al. 2017Queiroz LP, Cardoso D, Fernandes MF & Moro MF (2017) Diversity and evolution of flowering plants of the caatinga domain. In: Silva JMC, Leal IR & Tabarelli M (eds.) Caatinga: the largest tropical dry region in South America. Ed. Springer, Cham. Pp. 23-64.). The Caatinga is described by typical features of xerophytic vegetation such as shrubby or arboreal forests, spiny and deciduous trees (Prado 2003Prado DE (2003) As caatingas da Américas do Sul. In: Leal IR, Tabarelli M & Silva JMC (eds.) Ecologia e conservação da Caatinga. Vol. 1. Ed. Universitária UFPE, Pernambuco. Pp. 3-73. ; Giulietti et al. 2004Giulietti AM, du Bocage Neta AL, Castro AAJF, Gamarra-Rojas CFL, Sampaio EVSB, Virgínio JF, Queiroz LP, Figueiredo MA & Rodal MJN (2004) Diagnóstico da vegetação nativa do bioma Caatinga In: Silva JMC, Tabarelli M, Fonseca MT & Lins LV (eds.) Biodiversidade da caatinga: áreas e ações prioritárias para a conservação. Vol. 1. Ed. Ministério do Meio Ambiente, Brasilia. Pp. 3-64.). Most of the region has precipitation between 600 and 1,200 mm annually, in a warm semi-arid climate, with an average temperature ranging from 25 to 30 °C throughout the year (Andrade et al. 2017Andrade EM, Aquino DN, Chaves LCG & Lopes FB (2017) Water as capital and its uses in the caatinga. In: Silva JMC, Leal IR & Tabarelli M (eds.) Caatinga: the largest tropical dry region in South America. Ed. Springer, Cham. Pp. 281-302.; Silva et al. 2017Silva JMC, Barbosa LCFB, Leal IR & Tabarelli M (2017) The caatinga: understanding the challenges. In: Silva JMC, Leal IR & Tabarelli M (eds.) Caatinga: the largest tropical dry region in South America. Ed. Springer, Cham. Pp. 3-19.). Its main physiographic compositions include the frequent rock outcrops, extensive intermittent drainage, and the numerous fields of inselbergs, frequent in different types of formations.

Among the eight ecoregions defined for the Caatinga biome by Velloso et al. (2002)Velloso AL, Sampaio EVSB & Pareyn FGC (2002) Ecorregiões propostas para o Bioma Caatinga. Ed. Associação Plantas do Nordeste, Recife. 76p., the Depressão Sertaneja Setentrional (DSS) is considered the most degraded one, with a small number of protected areas. The DSS includes three regions with very distinct vegetation and soil: Chapada do Apodi, Cariri Paraibano and Seridó (Velloso et al. 2002Velloso AL, Sampaio EVSB & Pareyn FGC (2002) Ecorregiões propostas para o Bioma Caatinga. Ed. Associação Plantas do Nordeste, Recife. 76p.) (Fig. 1). The Seridó region, located whithin a semi-arid area between Rio Grande do Norte and Paraíba states, is distinguished from the other areas of the DSS by having shallow soils derived from precambrian granites, gneisses and schists, with crystalline elevations up to 700 meters (Radam Brasil 1981Radam Brasil (1981) Levantamento de recursos naturais: Folhas SB. 24/25 Jaguaribe/Natal; geologia, geomorfologia, pedologia, vegetação e uso potencial da terra. Vol. 23. Ed. Ministério das Minas e Energia, Rio de Janeiro. 774p.; Velloso et al. 2002Velloso AL, Sampaio EVSB & Pareyn FGC (2002) Ecorregiões propostas para o Bioma Caatinga. Ed. Associação Plantas do Nordeste, Recife. 76p.; Varela-Freire 2002Varela-Freire AA (2002) A caatinga hiperxerófila Seridó: a sua caracterização e estratégias para sua conservação. Ed. Academia de Ciências do Estado de São Paulo, São Paulo. 39p.). The vegetation is classified as with low density and small size, which shows a predominantly open formation, typical of crystalline formations in Northeast Brazil (Radam Brasil 1981Radam Brasil (1981) Levantamento de recursos naturais: Folhas SB. 24/25 Jaguaribe/Natal; geologia, geomorfologia, pedologia, vegetação e uso potencial da terra. Vol. 23. Ed. Ministério das Minas e Energia, Rio de Janeiro. 774p.; Queiroz et al. 2015Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.). However, it is argued that its floristic diversity is underestimated because floristic surveys in the area focused on arboreous species, neglecting the importance of herbaceous and/or annual species, an important component of plant communities in arid regions, like the Caatinga biome (Mott 1972Mott JJ (1972) Germination studies on some annual species from an arid region of Western Australia. Journal of Ecology 60: 293-304.; Nash et al. 1999Nash M, Whitford W, Soyza A, Zee J & Havstad K (1999) Livestock activity and Chihuahuan Desert Annual-Plant Communities: boundary analysis of disturbance gradients. Ecological applications. Ecological Applications 9: 814-823. ; Costa et al. 2007Costa RC, Araújo FS & Lima-Verde LW (2007) Flora and life-form spectrum in an area of deciduous thorn woodland (Caatinga) in northeastern, Brazil. Journal of Arid Environments 68: 237-247. ; Queiroz et al. 2015Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.).

Figure 1
Location of the study area, the Seridó Ecological Station, a federal conservation unit inserted in the ecoregion of the Depressão Sertaneja Setentrional (DSS), northern portion of the Caatinga biome, Rio Grande do Norte state.

Climbing plants, subdivided into herbaceous and woody species, are those that need some support to grow (Gentry 1991Gentry AH (1991) The distribution and evolution of climbing plants. In: Putz FE & Mooney HA (eds.) The biology of vines. Ed. Cambridge University Press, Cambridge. Pp. 146-194.; Gerwing et al. 2006Gerwing JJ, Schnitzer SA, Burnham RJ, Bongers F, Chave J, DeWalt SJ, Ewango CEN, Foster R, Kenfack D, Martınez-Ramos M, Parren M, Parthasarathy N, Perez-Salicrup DR, Putz FE & Thomas DW (2006) A standard protocol for liana censuses. Biotropica 38: 256-261.). Plants that have this habit use the stem, tendrils, adventitious roots, or other appendages to stay suspended, ensuring sunlight and moisture necessary for their survival (Gerwing et al. 2006Gerwing JJ, Schnitzer SA, Burnham RJ, Bongers F, Chave J, DeWalt SJ, Ewango CEN, Foster R, Kenfack D, Martınez-Ramos M, Parren M, Parthasarathy N, Perez-Salicrup DR, Putz FE & Thomas DW (2006) A standard protocol for liana censuses. Biotropica 38: 256-261.; Burnham 2015Burnham RJ (2015) Climbing plants in the fossil record: Paleozoic to present. In: Schnitzer SA, Bongers F, Burnham RJ & Putz FE (eds.) Ecology of lianas. Vol. 1. Ed. John Wiley & Sons Ltd., Chichester. Pp. 205-220.). The climbing strategy emerged independently on several occasions during plant evolution (Putz 1984Putz FE (1984) The natural history of lianas on Barro Colorado Island, Panama. Ecological Society of America 65: 1713-1724.; Burnham 2015Burnham RJ (2015) Climbing plants in the fossil record: Paleozoic to present. In: Schnitzer SA, Bongers F, Burnham RJ & Putz FE (eds.) Ecology of lianas. Vol. 1. Ed. John Wiley & Sons Ltd., Chichester. Pp. 205-220.). According to Gentry (1991)Gentry AH (1991) The distribution and evolution of climbing plants. In: Putz FE & Mooney HA (eds.) The biology of vines. Ed. Cambridge University Press, Cambridge. Pp. 146-194., 26 angiosperm families include 85% of all New World climbers, which are of great floristic importance, contributing significantly to the taxonomic diversity of tropical forests. In neotropical region, woody climbing (or liana) plants account for about 25% of overall plant species richness (Schnitzer & Bongers 2002Schnitzer SA & Bongers F (2002) The ecology of lianas and their role in forests. Trends in Ecology & Evolution 17: 223-230.). Climbing species also affects the structure of tropical forests by exerting a strong selective pressure on the trees, which influences their survival rate, individuals with large number of lianas suffer higher mortality rates than liana-free trees (Putz 1984Putz FE (1984) The natural history of lianas on Barro Colorado Island, Panama. Ecological Society of America 65: 1713-1724.; Gentry 1991Gentry AH (1991) The distribution and evolution of climbing plants. In: Putz FE & Mooney HA (eds.) The biology of vines. Ed. Cambridge University Press, Cambridge. Pp. 146-194.). In contrast, lianas can also provide support to trees by anchoring each other, reducing mechanical stress, induced by wind for example (Putz 1984Putz FE (1984) The natural history of lianas on Barro Colorado Island, Panama. Ecological Society of America 65: 1713-1724.).

Despite its importance contributing to the diversity and structure of tropical forests, few studies focusing on the diversity of this life form have been carried out in the Caatinga (Araújo 2014Araújo D (2014) Trepadeiras do bioma Caatinga. In: Villagra BL, Melo MMR, Romaniuc-Neto S & Barbosa L (eds.) Diversidade e conservação de trepadeiras: contribuição para a restauração de ecossistemas brasileiros. Vol. 1. Ed. Instituto de Botânica, São Paulo. Pp. 33-58.; Oliveira et al. 2015Oliveira DG, Prata APN & Matos GMA (2015) Diversidade florística e estratégias de sobrevivência das trepadeiras em um fragmento de Caatinga em Porto da Folha, Sergipe, Brasil. Biotemas 28: 51-60.; Delgado-Junior & Alves 2017Delgado-Junior GC & Alves M (2017) Diversidade de plantas trepadeiras do Parque Nacional do Catimbau, Pernambuco, Brasil. Rodriguesia 68: 347-377.; Lucena et al. 2017Lucena DS, Lucena MDFDA & Alves M (2017) Climbers from two rock outcrops in the semi-arid region of Brazil. Check List 13: 417-427.). Given this, detailed studies are still needed to improve our understanding about the diversity of climber species, especially in underexplored areas such as the Seridó. Further studies focusing on the characterization, conservation and management of these species are also required (Ribeiro Neto et al. 2018Ribeiro Neto N, Ronqui RA, Seidinger LC & Udulutsch RG (2018) Climbers of the Estação Ecológica de Assis, state of São Paulo, Brazil: floristics and identification keys. PhytoKeys 99: 67-84.).

The knowledge of a region’s flora is a fundamental part of the evaluation and monitoring of its biodiversity, which supports the information used for elaboration of conservation measures and the use of natural resources (Cerqueira 2001Cerqueira R (2001) Um sistema de monitoramento da biodiversidade terrestre do Brasil: explorando possibilidades. In: Garay I & Dias B (eds.) Conservação da biodiversidade em ecossistemas tropicais: avanços conceituais e revisão de novas metodologias de avaliação e monitoramento. Vol. 1. Ed. Vozes, Petrópolis. Pp. 277-285.). However, such measures should be based on correct species identification (Urbanetz et al. 2010Urbanetz C, Tamashiro JY & Kinoshita LS (2010) Chave de identificação de espécies lenhosas de um trecho de Floresta Ombrófila Densa Atlântica, no sudeste do Brasil, baseada em caracteres vegetativos Introdução Material e Métodos. Biota Neotropica 10: 349-398.). Taxonomy has traditionally used numerous terminologies that are difficult for non-botanists to understand, and taxonomic information is not always accessible to the whole society, which makes it difficult to properly identify species. Therefore, the use of modern taxonomic tools can contribute significantly to the adequate dissemination of the knowledge about diversity and, consequently, to the flora maintenance of a specific region, especially in protected areas. One of the tools available today is the interactive identification key, which abandons the dichotomy of traditional identification keys. The interactive keys are relatively friendly platforms that use images in order to illustrate terms and species, besides the fact that are available online and, therefore, facilitate the process of identifying taxa, especially by non-specialists. From this point of view, anyone can learn about biodiversity beyond a collection of taxon names by gathering taxonomic information into a reliable, easily accessible, up-to-date source (Hardisty & Roberts 2013Hardisty A & Roberts D (2013) A decadal view of biodiversity informatics: challenges and priorities. BMC Ecology 13: 1-23.).

Considering the above, the objective of the present work is to list, describe and illustrate the flora of climbing plants in Seridó Ecological Station (ESEC Seridó), one of the few conservation units of the Caatinga in Rio Grande do Norte state. This study aims to make use of virtual taxonomic tools, which combines the basic principles of taxonomy and modern digital resources, facilitating access to data and dissemination of knowledge about the local flora.

Material and Methods

Study site

Seridó Ecological Station (ESEC Seridó) is a conservation unit (CU) located in the municipality of Serra Negra do Norte, state of Rio Grande do Norte, in the Seridó microregion (coordinates: maximum latitude: 06º36’40”S, minimum latitude: 06º33’50”S, west longitude: 37º17’10”W, east longitude: 37º14’20”W). Created in 1982, ESEC Seridó has 11,2361 km² and, although is one of the smallest strict protection areas in the country, is also the second largest CU of Rio Grande do Norte and the first for the Caatinga biome in this state (ICMBio 2019ICMBio (2019) Esec do Seridó. Avaidable at <https://www.gov.br/icmbio/pt-br/assuntos/biodiversidade/unidade-de-conservacao/unidades-de-biomas/caatinga/lista-de-ucs/esec-do-serido>. Access on 24 November 2019.) (Fig. 1).

Inside the ESEC Seridó, the hyperxerophilous Caatinga, typical vegetation of the region that develops on a shallow and stony soil, presents distinct physiognomies related to soil type, presence of water and relief (Fig. 2) (Moreira 1990Moreira OCS (1990) Contribuição ao zoneamento da estação ecológica do Seridó (estudos pedológicos, fitogeográficos e hidrológicos). Trabalho de conclusão de curso. Universidade Federal do Rio Grande do Norte, Natal. 30p.; IBAMA 2004IBAMA (2004) Plano de Manejo ESEC do Seridó. Avaidable at <https://www.gov.br/icmbio/pt-br/assuntos/biodiversidade/unidade-de-conservacao/unidades-de-biomas/caatinga/lista-de-ucs/esec-do-serido>. Access on 23 November 2019. ). The unit has three main terrestrial habitats, as mentioned by Queiroz et al. (2015)Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.: Open caatinga (Fig. 2a), with sparse deciduous woody plants and herbaceous plants that cover the soil during the rainy season; closed Caatinga (Fig. 2b), which is a dense scrubland or woodland, being the most widespread habitat in the unit; finally, the rocky outcrops (Fig. 2c), including inselbergs and lagedos, with the presence of rupicolous vegetation. In addition to these habitats, aquatic environments can be observed, such as the artificial reservoir (Fig. 2d) and temporary ponds during the rainy season. According to the Köppen-Geiger classification, ESEC Seridó has a Bsh type climate (warm semi-arid), with the rainy season concentrated from January to May (Alvares et al. 2013Alvares CA, Stape JL, Sentelhas PC, Moraes GJL & Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.). The CU is inserted in the morphodynamic domains of the Depressão Sertaneja, Jucurutu Formation, where it presents luvisols, organosols and neosols soils (the latter two being less frequent) (IBAMA 2004IBAMA (2004) Plano de Manejo ESEC do Seridó. Avaidable at <https://www.gov.br/icmbio/pt-br/assuntos/biodiversidade/unidade-de-conservacao/unidades-de-biomas/caatinga/lista-de-ucs/esec-do-serido>. Access on 23 November 2019. ). In the buffer zone of the CU there are isolated communities, mostly family farmers.

Figure 2
a-d. Overview of distinct habitats in Seridó Ecological Station, a federal conservation unit located in the Caatinga biome, Rio Grande do Norte state – a. open caatinga at the beginning of the dry season; b. closed caatinga in rainy season; c. rock outcrop during the dry season; d. artificial reservoir during the rainy season. Photographs: a-d by L.F.A. de Paula.

Floristic study

A preliminary list of species was initially generated by accessing public repositories (SpeciesLink, <http://splink.cria.org.br/>; BFG (2018); and GBIF, <https://www.gbif.org/>). The names have been updated and the data were managed to remove errors and duplicates using BRAHMS software (<https://herbaria.plants.ox.ac.uk/bol/>). Thereafter, periodic expeditions were carried out to obtain botanical samples, from April 2018 until December 2019, covering both wet and dry seasons. The specimens were georeferenced using a GPS (Garmin Gpsmap 78s). Individuals in reproductive stage were collected and photographed using a Nikon Coolpix P600 digital camera.

The botanical material was processed according to the usual techniques for vascular plants (Fidalgo & Bononi 1989Fidalgo O & Bononi VLR (1989) Técnicas de coleta, preservação e herborização de material botânico. Vol. 1. Ed. Instituto de Botânica, São Paulo. 61p.). Taxonomic identification was accomplished by means of specialized taxonomic literature, herborized collections and, when necessary, consultation with specialists. Additionally, the collection of the UFRN herbarium, which concentrates a large volume of botanical material from ESEC Seridó including those from Queiroz et al. (2015)Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376., was consulted and served as the basis for coding of morphological characteristics used in the determinations and in the interactive identification key.

For the determination of new occurrences and endemism, we consulted BFG (2018) and previous studies about the flora of Rio Grande do Norte that cited some of the listed species: Versieux et al. (2017)Versieux LM, Dávila N, Delgado GC, Sousa VF, Moura EO, Filgueiras T, Alves MV, Carvalho E, Piotto D, Forzza RC, Calvente A & Jardim JG (2017) Integrative research identifies 71 new plant species records in the state of Rio Grande do Norte (Brazil) and enhances a small herbarium collection during a funding shortage. PhytoKeys 86: 43-74. , Soares (2018)Soares AMM (2018) Diversidade de Convolvulaceae Juss. no Estado do Rio Grande do Norte, Brasil. Dissertação de Mestrado. Universidade Federal Rural de Pernambuco, Recife. 107p., Medeiros et al. (2010)Medeiros MA, Grangeiro LC, Torres SB & Freitas AVL (2010) Maturação fisiológica de sementes de maxixe (Cucumis anguria L.). Revista Brasileira de Sementes 32: 17-24., Roque et al. (2010)Roque AA, Rocha RM & Loiola MIB (2010) Uso e diversidade de plantas medicinais da Caatinga na comunidade rural de Laginhas, município de Caicó, Rio Grande do Norte (nordeste do Brasil). Revista Brasileira de Plantas Medicinais 12: 31-42. , Amorim et al. (2016)Amorim LDM, Sousa LOF, Oliveira FFM, Camacho RGV & Melo JIM (2016) Fabaceae na Floresta Nacional (FLONA) de Assú, semiárido potiguar, nordeste do Brasil. Rodriguésia 67: 105-124. and Santos et al. (2019)Santos MO, Cordeiro WPFS, Sales MF & Santos Silva J (2019) The genera Bernardia Houst. ex Mill. and Tragia L. (Euphorbiaceae, Acalyphoideae) in Northeastern Brazil. Biota Neotropica 19: 1-15. . Species cited in previous studies that are not yet in BFG (2018) were highlighted (Tab. 1).

Table 1
Climbers from Seridó Ecological Station, Rio Grande do Norte, Brazil. Habit: H (Herbaceous), W (Woody). Endemic from Brasil (End). Habitat: Ro (Rock outcrop), Oc (Open Caatinga), Cc (Closed Caatinga), Unk (Unknown). Distribution (Distrib.): N (Native), E (exotic). Collectors: M = Moreira VP; Mo = Moura EO; Ma = Marinho AM; Me = Melo JI; N = Nascimento MB; Q = Queiroz RT. Voucher = Collector Number / Catalog Number. First records for the Rio Grande do Norte state are in bold. Names preceeded by “*” were previously cited in the literature, but not on the BFG (2018). Ancistrotropis peduncularis is cited by Versieux et al. (2017) Ipomoea cynanchifolia by Soares (2018), Cucumis anguria by Medeiros et al. (2010), Luffa operculata by Roque et al. (2010) and Tragia cearensis by Santos et al. (2019).

Interactive key

The interactive identification key for woody and herbaceous climber species in ESEC Seridó was developed using the open access software Xper², version 2.3.2 (<http://www.infosyslab.fr/>). The software was developed in Java language and is compatible with the major operating systems (i.e. Windows, MacOS and Linux), is free and has a user-friendly interface available in several languages, including Portuguese (Ung et al. 2010Ung V, Dubus G, Zaragüeta-Bagils R & Vignes-Lebbe R (2010) Xper2: Introducing e-taxonomy. Bioinformatics 26: 703-704.). Therefore, the key was later transferred to the online platform Xper³ (<http://www.xper3.fr>), facilitating access for the public.

The organization of characters and character states, as well as their description, was based on specialized literature (Vidal & Vidal 2000Vidal WN & Vidal MRR (2000) Botânica: organografia. Vol. 1. Ed. Imprensa Universitária UFV, Viçosa. 124p.; Gonçalves & Lorenzi 2011Gonçalves EG & Lorenzi H (2011) Morfologia vegetal: organografia e dicionário ilustrado de morfologia das plantas vasculares. Vol. 2. Ed. Instituto Plantarum de Estudos da Flora, São Paulo. 512p.). The characters used in the key were grouped into four main sections: “Leaf”, “Flower”, “Other Vegetative Characters”, “Fruits and Seeds”. In Xper³, these characters are ordered according to their respective discriminating power, based on the efficiency indices of the Xper (Ung et al. 2010Ung V, Dubus G, Zaragüeta-Bagils R & Vignes-Lebbe R (2010) Xper2: Introducing e-taxonomy. Bioinformatics 26: 703-704.), Jaccard (1901)Jaccard P (1901) étude Comparative de la distribuition florale dans une portion des Alpes et des Jura. Bulletin de la Société Vaudoise des Sciences Naturelles 7: 547-579. and Sokal & Michener (1958)Sokal RR & Michener CD (1958) A statistical methods for evaluating relationships. University of Kansas Science Bulletin 38: 1409-1448. descriptors. All images are from species found in the study site, being used to illustrate the species, the characters and character states. In some cases, it was not possible to acquire images of the species in the field; therefore, we used photographs of public domain. All images were properly referenced with the photographer’s name and/or link that gave permission to use them.

The discriminatory power of the key descriptors was evaluated using analytical tools of Xper², which include three indexes that quantitatively evaluate the efficiency of each descriptor in distinguishing species. Analyses of these indexes were helpful to check the efficiency of each character, allowing us to review the key in order to keep only the most useful characters.

Results

Climber diversity in the study area

We recorded a total of 56 climbing species in the study area, belonging to 13 families and 34 genera (Tab. 1; Fig. 3). Only two species belonged to monocotyledons (Dioscorea campestris, Dioscoreaceae and Aristolochia birostris, Aristolochiaceae). Among the eudicotyledons, Convolvulaceae is the most representative family (18 species; five genera), followed by Fabaceae (10 species; six genera), Apocynaceae (eight species; six genera) and Cucurbitaceae (five species; five genera) (see Fig. 4). Within the species, 33 were classified as herbaceous climbers or vines (about 58,9%), and most of them belonged to the Convolvulaceae family (18 species). The remaining 23 species (41,1% of the total species number) were classified as woody climbers or lianas, with the Apocynaceae family being the most representative (totaling eight species) (Fig. 4).

Figure 3
a-h. Some climbers of the Seridó Ecological Station, a federal conservation unit located in the Caatinga biome, Rio Grande do Norte state – a. Canavalia brasiliensis, flower; b-c. Allamanda blanchetii, flower and fruit; d. Ibatia harleyi, flower; e. Jacquemontia evolvuloides, flower; f. Myruopus rubicundus, flower; g. Cardiospermum corundum, fruit and seed; h. Passiflora foetida, flower. Photographs: a, b by V.P. Moreira; c, d, e, h by M.B. Nascimento; f, g by F.G.L. Moreira.
Figure 4
Richest families (a) and genera (b) of the Seridó Ecological Station, a federal conservation unit located in the Caatinga biome, Rio Grande do Norte state.

Five new occurrences were found for the state of Rio Grande do Norte (Tab. 1): Cuscuta globosa, Cuscuta partita, (Convolvulaceae), Macroptilium bracteatum (Fabaceae), Heteropterys trichanthera and Tetrapterys longibracteata (Malpighiaceae), being the latest a new occurrence of the genus Tetrapterys for the state. Five other species, although mentioned in previous studies, are not cited for the state of Rio Grande do Norte in BFG (2018): Ancistrotropis peduncularis (Versieux et al. 2017Versieux LM, Dávila N, Delgado GC, Sousa VF, Moura EO, Filgueiras T, Alves MV, Carvalho E, Piotto D, Forzza RC, Calvente A & Jardim JG (2017) Integrative research identifies 71 new plant species records in the state of Rio Grande do Norte (Brazil) and enhances a small herbarium collection during a funding shortage. PhytoKeys 86: 43-74. ), Ipomoea cynanchifolia (Soares 2018Soares AMM (2018) Diversidade de Convolvulaceae Juss. no Estado do Rio Grande do Norte, Brasil. Dissertação de Mestrado. Universidade Federal Rural de Pernambuco, Recife. 107p.), Cucumis anguria (Medeiros et al. 2010Medeiros MA, Grangeiro LC, Torres SB & Freitas AVL (2010) Maturação fisiológica de sementes de maxixe (Cucumis anguria L.). Revista Brasileira de Sementes 32: 17-24.), Luffa operculata (Roque et al. 2010Roque AA, Rocha RM & Loiola MIB (2010) Uso e diversidade de plantas medicinais da Caatinga na comunidade rural de Laginhas, município de Caicó, Rio Grande do Norte (nordeste do Brasil). Revista Brasileira de Plantas Medicinais 12: 31-42. ) and Tragia cearensis (Santos et al. 2019Santos MO, Cordeiro WPFS, Sales MF & Santos Silva J (2019) The genera Bernardia Houst. ex Mill. and Tragia L. (Euphorbiaceae, Acalyphoideae) in Northeastern Brazil. Biota Neotropica 19: 1-15. ). Some listed species have economic, medicinal and ornamental importance: Cucumis anguria, popularly known as maxixe, is widely consumed and cultivated in the region; Momodica charantia and Luffa operculata have several uses in traditional medicine (Silva & Freire 2010Silva TS & Freire EMX (2010) Abordagem etnobotânica sobre plantas medicinais citadas por populações do entorno de uma unidade de conservação da caatinga do Rio Grande do Norte, Brasil. Revista Brasileira de Plantas Medicinais 12: 427-435.) as in the pharmaceutical industry (Champney et al. 1978Champney R, Ferguson NM & Ferguson GG (1978) Selected pharmacological studies of luffa operculata. Journal of Pharmaceutical Sciences 63: 942-943.); and Alamanda blanchetti (Fig. 3e) stands out for its ornamental use because its flowers are very showy.

Interactive key

The interactive key database includes 16 reproductive characters and 29 vegetative characters, totaling 45 characters and 209 character states. In total, 281 images were used to illustrate the key. To illustrate the species, 88 photos were used, including habit, main structures and exsiccates used in the description. The key was later transferred to the online platform Xper³ [<http://www.xper3.fr> (Fig. 5)], where it is published and freely accessible to the public through the link: <http://www.xper3.fr/xper3GeneratedFiles/publish/identification/-4505993480748774750/mkey.html>.

Figure 5
Interactive Key for climbers species of the Seridó Ecological Station, Rio Grande do Norte, Brazil. The left column presents the characters and their respective states, and the right column presents the species and their respective families.

Discussion

This study added 14 species of climbers to the previous checklist of ESEC Seridó made by Queiroz et al. (2015)Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.. It also contributes to a reassessment of the knowledge about the diversity of Caatinga climbing plants, which is an understudied life form group, especially in this region. The insufficient biodiversity knowledge of an area, especially of a CU, hinders several measures that would enable the preservation and sustainable use of the natural resources, and prevents society from having access to correct estimates of species numbers. This work is the first to cover climbers in the CU and throughout the Seridó region, as well as in the state of Rio Grande do Norte. This is also the first online interactive key publication for the flora of Seridó.

None of the climbing plants have any degree of threat according to the Oficial List of Endangered Species of the Brazilian Flora (MMA 2014MMA - Ministério do Meio Ambiente - Brasil (2014) Portaria n° 443, de 17 de dezembro de 2014. Lex: reconhece como espécies da flora brasileira ameaçadas de extinção aquelas constantes da “Lista Nacional Oficial de Espécies da Flora Ameaçadas de Extinção”. Avaidable at <http://cncflora.jbrj.gov.br/portal/static/pdf/portaria_mma_443_2014.pdf> Access on 10 November 2019.). However, conservation status is unknown for most of the species as they have not been evaluated due to the absence of data or because are negleted groups. The three most representative families in the study area (Convolvulaceae, Fabaceae and Apocynaceae, respectively) are also the most characteristic families found in a previous survey in ESEC Seridó (Queiroz et al. 2015Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.). These families were also reported as the most representative for the Caatinga in general, as seen in Araújo (2014)Araújo D (2014) Trepadeiras do bioma Caatinga. In: Villagra BL, Melo MMR, Romaniuc-Neto S & Barbosa L (eds.) Diversidade e conservação de trepadeiras: contribuição para a restauração de ecossistemas brasileiros. Vol. 1. Ed. Instituto de Botânica, São Paulo. Pp. 33-58.. Although Convolvulaceae is the most representative family, not only in the study area but also in the whole Caatinga biome, the knowledge about its environmental and ecological importance is insufficient (Simão-Bianchini & Pirani 2005).

Previous studies carried out at ESEC Seridó have determined the zoning of the area, identifying rock outcrops, temporary pounds, preserved vegetation and degraded areas (Borges 1989Borges JC (1989) Áreas vulneráveis à desertificação no Rio Grande do Norte. Caderno Norte-Rio-Grandense de Temas Geográficos 4: 18-25.; Moreira 1990Moreira OCS (1990) Contribuição ao zoneamento da estação ecológica do Seridó (estudos pedológicos, fitogeográficos e hidrológicos). Trabalho de conclusão de curso. Universidade Federal do Rio Grande do Norte, Natal. 30p.). Later, other studies performed more detailed floristic, ethnobotanical, phytosociological and/or phytogeographic surveys (Camacho 2001Camacho RGV (2001) Estudo fitofisiográfico da caatinga do Seridó - Estação Ecológica do Seridó, RN. Tese de Doutorado. Universidade de São Paulo, São Paulo. 190p.; Camacho & Baptista 2005Camacho RGV & Baptista GMM (2005) Análise geográfica computadorizada aplicada à vegetação da caatinga em unidades de conservação do Nordeste: Estação Ecológica do Seridó-ESEC/RN/Brasil, In: Epiphanio JCN & Banon GJF (eds.) Anais XII Simpósio de Sensoriamento Remoto. Ed. INPE, São José dos Campos. Pp. 2611-2618.; Lacerda & Kageyama 2003Lacerda CMB & Kageyama PY (2003) Estrutura genética espacial de duas populações naturais de Myracrodruon urundeuva M. Allemão na região semi-árida, Brasil. Revista Árvore 27: 145-150.; Santana & Souto 2006Santana JAS & Souto JS (2006) Diversidade e estrutura fitossociológica da caatinga na Estação Ecológica do Seridó-RN. Revista de Biologia e Ciências da Terra 6: 232-242.; Santana et al. 2009Santana JADS, Pimenta AS, Souto JS, Almeida FV & Pacheco MV (2009) Levantamento florístico e associação de espécies na caatinga da Estação Ecológica do Seridó, Serra Negra do Norte - RN - Brasil. Revista Verde 4: 83-89.; Silva & Freire 2010Silva TS & Freire EMX (2010) Abordagem etnobotânica sobre plantas medicinais citadas por populações do entorno de uma unidade de conservação da caatinga do Rio Grande do Norte, Brasil. Revista Brasileira de Plantas Medicinais 12: 427-435.; Queiroz 2006Queiroz RT (2006) Diversidade floristica do componente herbáceo da Estação Ecológica do Seridó Serra Negra do Norte - RN. Dissertação de Mestrado. Universidade Federal do Rio Grande do Norte, Natal. 66p.; Queiroz et al. 2015Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.). Most of these studies focused on trees and shrubs or concentrated on phytotherapic species. More specifically, one investigation in the ESEC Seridó focused on the family Poaceae, in which a taxonomic treatment accepted 57 species of grasses in the area (Ferreira et al. 2009Ferreira CGT, Oliveira RC, Valls JFM & Loiola MIB (2009) Poaceae da Estação Ecológica do Seridó, Rio Grande do Norte. Hoehnea 36: 679-707.). The management plan of ESEC Seridó was implemented only in 2004 (22 years after its creation), displaying a floristic survey with 164 species (IBAMA, 2004). More thorough surveys were performed by Queiroz (2006)Queiroz RT (2006) Diversidade floristica do componente herbáceo da Estação Ecológica do Seridó Serra Negra do Norte - RN. Dissertação de Mestrado. Universidade Federal do Rio Grande do Norte, Natal. 66p. and Queiroz et al. (2015)Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.. The first comprised 300 species of angiosperms in the area, including woody and herbaceous species, while the latter recorded 335 angiosperm species. In a comprehensive analysis of the life forms found in ESEC Seridó, Queiroz et al. (2015)Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376. showed that herbaceous species constituted over 80% of the reserve’s flora, suggesting that the richness estimates in the Seridó region are underestimated by the lack of studies focusing on non-arboreal species. In addition to the herbaceous species (which comprise 209 species), 16 trees, 39 shrubs/sub-shrubs and 42 woody/herbaceous climbers were cataloged in the respective study (Queiroz et al. 2015Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.). Our study cataloged 56 species of woody and herbaceous climbers, emphasizing the need for longer inventories in different areas of the Seridó region.

As taxonomy is a gateway to all biological knowledge, and it has become increasingly essential for taxonomic information to be organized, up-to-date, and readily available to society at large by electronic means (Bisby et al. 2002Bisby F, Shimura J, Ruggiero M, Edwards J & Haeuser C (2002) Taxonomy, at the click of a mouse. Nature 418: 367.; Carvalho et al. 2015Carvalho FA, Filer D & Renner SS (2015) Taxonomy in the electronic age and an e-monograph of the papaya family (Caricaceae) as an example. Cladistics 31: 321-329.). The use of interactive keys meets this need, as they allow constant updating in addition to the large-scale dissemination provided by the internet, allowing the access of diverse audiences. The interactive key of the climbers in ESEC Seridó favors not only researchers in the area, but also managers of the conservation units, local communities (including schools) and visitors, which may have access to species identification, spreading, therefore, the knowledge about the region’s flora. In addition, the key allows the users to obtain information about the flora during the dry season, which must be considered in the context of the Caatinga vegetation, where many plants are annual or deciduous.

Although there are already published interactive keys for the Atlantic Forest (Carmo & Simões 2017Carmo JAM & Simões AO (2017) Rubiaceae no município de Camanducaia, Serra da Mantiqueira, Minas Gerais: sinopse e chave interativa. Rodriguésia 68: 1411-1429.), Cerrado (Peres & Fagg 2011Peres MK & Fagg CW (2011) Chave interativa para diásporos do Cerrado do Jardim Botânico de Brasília, DF, atrativos para a fauna. Heringeriana 5: 32-46.; Zanatta et al. 2015Zanatta MRV, Kuhlmann M, Cota MRC, Santos ABP & Proença CEB (2015) Chave interativa ilustrada para famílias de angiospermas no bioma Cerrado. Heringeriana 10: 91-112.) and Amazon (Zuquim et al. 2017Zuquim G, Tuomisto H & Prado J (2017) A free-access online key to identify Amazonian ferns. PhytoKeys 78: 1-15.; Bittrich et al. 2012Bittrich V, Souza, CSD, Coelho RLG, Martins MV, Hopkins MJG & Amaral MCE (2012) An interactive key (Lucid) for the identifying of the genera of seed plants from the Ducke Reserve, Manaus, AM, Brazil. Rodriguésia 63: 55-64.), the Caatinga so far has no exclusive interactive keys for its flora, as well as the state of Rio Grande do Norte. There is only an available interactive key for Bignoniaceae species occurring in the Caatinga biome within the state of Bahia (Espirito Santo et al. 2013). This deficiency of studies that includes new taxonomic tools obstructs the process of disseminating the knowledge of Caatinga biodiversity. By contrast, making interactive keys available online facilitates the identification process, making it more accessible not only to researchers but also to the general public, especially in more remote areas such as the Seridó region (Brach & Boufford 2011Brach AR & Boufford DE (2011) Why are we still producing paper floras? Annals of the Missouri Botanical Garden 98: 297-300. ).

The results here support previous studies (Queiroz 2006Queiroz RT (2006) Diversidade floristica do componente herbáceo da Estação Ecológica do Seridó Serra Negra do Norte - RN. Dissertação de Mestrado. Universidade Federal do Rio Grande do Norte, Natal. 66p.; Queiroz et al. 2015Queiroz RT, Moro MF & Loiola MIB (2015) Evaluating the relative importance of woody versus non-woody plants for alpha-diversity in a semiarid ecosystem in brazil. Plant Ecology and Evolution 148: 361-376.), which emphasized that the Seridó region is still neglected concerning basic floristic knowledge, especially about non-arboreal species. Besides the updated checklist including new records for the Rio Grande do Norte state, we also provided an interactive key for identification of climbing plants. ESEC Seridó is suffering with historical antropic actions such as huntering and farming sourrounding it (Caldas et al. 2016Caldas FLS, Costa TB, Laranjeiras DO, Mesquita DO & Garda AA (2016) Herpetofauna of protected areas in the Caatinga V: Seridó Ecological Station (Rio Grande do Norte, Brazil). Check List 12: 1-14.). Besides the use by the academic community, the detailed information and images used in the virtual identication key may be used for educational purposes showing schools and sourrounding communities the importance the ESEC Seridó has for the conservartion of the floristic diversity of the region.

Acknowledgements

We thank the grant from Conselho Nacional de Pesquisa Científica (CNPq) and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) (process 421374/2017-9) given to F.A. Carvalho. We are grateful to the experts A. Marinho (Convolvulaceae), M. Kirizawa, R. Couto (Dioscoreaceae) and S.S. Matos (Fabaceae), for help in identifying the species. We express our gratitude to A. Fontes, for logistic support in the UFRN herbarium, and Dr. R.T. Queiroz for providing images of Fabaceae species. We thankful to George S. Batista, the manager of ESEC Seridó, who provided logistics in the conservation unit and were also very cooperative in sharing information about the flora of the region. We are also thankful to Dr. C.P. Bruniera and an anonymous reviewer. Finally, we thank the scholarship granted to F.G.L. Moreira by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and L.F.A. de Paula thanks the grants from CNPq (DTI-A, 421374/2017-9) and CAPES (88887.569558/2020-00).

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Publication Dates

  • Publication in this collection
    20 Sept 2021
  • Date of issue
    2021

History

  • Received
    23 Dec 2019
  • Accepted
    29 Aug 2020
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