An updated plant checklist of the Brazilian Caatinga seasonally dry forests and woodlands reveals high species richness and endemism

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An updated plant checklist of the Brazilian Caatinga seasonally dry forests and woodlands reveals high species richness and endemism Moabe F. Fernandesa,∗, Domingos Cardosob, Luciano P. de Queiroza a b

Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, Brazil Instituto de Biologia, Universidade Federal da Bahia, Salvador, Bahia, Brazil

A R T I C LE I N FO

A B S T R A C T

Keywords: Floristics SDTFW biome Semiarid Species composition Biodiversity Northeastern Brazil

Plant checklists constitute the fundamental knowledge on which further hypotheses of ecology, evolution, and biodiversity conservation are built. Here, we compiled a comprehensive and taxonomically verified checklist of the flowering plant species occurring in the Caatinga. We circumscribe Caatinga to include only the dry deciduous vegetation in Northeast Brazil, corresponding to the largest continuous nucleus of the seasonally dry tropical forest and woodland biome (SDTFW) in South America. We recorded 3347 species, 962 genera, and 153 families, of which 526 species and 29 genera are endemic, and the large contribution of its non-woody component to overall diversity. These numbers reveal a remarkably high floristic diversity in the Caatinga, representing almost two fold higher species/area ratio (4.0 × 10−3 species/km2) as compared to the Amazon rainforests (2.5 × 10−3 species/km2). Most Caatinga-inhabiting species are shared with other non-SDTFW tropical biomes, probably reflecting transition zones with surrounding savannas and rain forests. This newly assembled taxonomic checklist is expected to serve not only as an updated look at the identity and counting of the Caatinga plant diversity, but will also provide aids for better understanding the origin, evolution, and ecological function of this species-rich, but highly threatened South American vegetation.

1. Introduction Plant checklists provide the basis for instructing the hypotheses underlying large-scale analyses of ecology, biogeography, and evolution, as well as environmental assessment efforts, land use management, public policies, and applied biology (Funk, 2006; Hortal et al., 2015). Floristic information is also fundamental to establish conservation priorities, whether focused on plant taxa, sites, habitats, or ecosystems. Given their importance, the use of flawed checklists can be detrimental to further analyses, leading to erroneous conclusions concerning biodiversity (Cardoso et al., 2017). As an effort to mitigate the knowledge vacuum of global plant diversity, initiatives such as the “Global Strategy for Plant Conservation” have attempted to document the entire global flora (UNEP, 2002). Entire biomes and many countries, however, still lack a comprehensive checklist of their flora. An emblematic example is provided by seasonally dry tropical forests and woodlands (SDTFW sensu Queiroz et al., 2017) – a global meta-community that is largely found in areas with fertile soils, low annual precipitation, and high seasonality (Pennington et al., 2000). SDTFW compose one of the world's most endangered tropical biomes, and are severely threatened by multiple pressures

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wherever they occur, including fire, human occupation, conversion to agriculture or pasture, and climate change (Miles et al., 2006). Nevertheless, they have been neglected by the scientific community as compared to other tropical biomes (Hughes et al., 2013) and their flora remains poorly known. Located entirely within Northeast semiarid Brazil (Fig. 1), the Caatinga region harbours the largest SDTFW nucleus, representing approximately 31% of the total area of that biome in the Neotropics (Queiroz et al., 2017). The Caatinga seasonally dry forests and woodlands are home to highly endangered species like the Lear's macaw (Anodorhynchus leari), the Grey-breasted Parakeet (Pyrrhura griseipectus), and the Spix’ macaw (Cyanopsitta spixii), already extinct in nature. An ever-increasing number of spectacular plant discoveries has been reported in the last years; for example, data compiled from TROPICOS (http://www.tropicos.org) show that in the last ten years approximately 90 new plant species have been published for the Caatinga, including the root-parasite Prosopanche caatingicola, the giant kapok tree Ceiba rubriflora, and Stemodia perfoliata, described from a 200 year old collection. Like the entire SDTFW biome across the Neotropics, the Caatinga has also been historically neglected: only 1.2% of its total extension is included within effective protected areas (Brasil,

Corresponding author. E-mail address: moabeff[email protected] (M.F. Fernandes).

https://doi.org/10.1016/j.jaridenv.2019.104079 Received 4 March 2019; Received in revised form 20 October 2019; Accepted 5 November 2019 0140-1963/ © 2019 Elsevier Ltd. All rights reserved.

Please cite this article as: Moabe F. Fernandes, Domingos Cardoso and Luciano P. de Queiroz, Journal of Arid Environments, https://doi.org/10.1016/j.jaridenv.2019.104079

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Fig. 1. Distribution of the Seasonally Dry Forests and Woodlands biome (SDTFW) in the Neotropics and the Caatinga in Northeast Brazil (red areas). Areas of rain forests (green) and savannas (grey) are also represented. The distribution of the SDTFW biome follows Queiroz et al. (2017). The Caatinga embraces the “Caatinga” and “Dry Atlantic Forest” ecoregions from Olson's classification (2001). Areas above 900 m high in the Chapada Diamantina (Bahia state) were coded as savanna due to the dominance of rupestrian grasslands. Mangrove areas near the main river mouths were coded as rainforests. The background shows the physiognomic diversity of the Caatinga SDTFW formations. Sedimentary Caatinga (A); deciduous Caatinga forests on karstic terrains (B); crystalline Caatinga woodlands during the dry season (C); and semi-deciduous Caatinga forest during rainy season (D). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

specimens through massive on-line biological databases (e.g., GBIF, http://gbif.org; INCT, http://inct.splink.org) provide the means to build on a more comprehensive checklist for the Caatinga seasonally dry forests and woodlands. In face of the ever-increasing loss of natural vegetation and the lack of effective conservation efforts, a new look is urgently needed into Caatinga plant diversity in order to allow development of future research and conservation strategies. The construction of a biome-based checklist, capable of surpassing previous methodological and conceptual conflicts, will open new perspectives into better understanding the ecology and evolution of plant communities. We present here a comprehensive checklist of the flowering plants from the highly threatened Caatinga seasonally dry forests and woodlands to provide the foundation for effective conservation planning of its extraordinary flora and facilitate future studies aimed at better understanding its ecology and evolutionary diversification.

2015). Perhaps because it was long presumed to be poor in species diversity and endemism (Andrade-Lima, 1981), few efforts have been made to study its flora, making it the least known and most threatened Brazilian vegetation (Moro et al., 2015). This scenario has been modified in the last decade, however, with exponential increases in scientific research, although a comprehensive checklist of all known flowering plants is still lacking. Available relevant checklists fail to depict its true diversity for different reasons. Some previous checklists have been based exclusively on compilations of site-based, regional/local phytosociological studies (Moro et al., 2014) that tend to underestimate full diversity as they are highly biased towards the woody component, neglecting total flowering plant diversity (Moro et al., 2015; Queiroz et al., 2015). On the other hand, the available voucher-based, taxonomically verified checklists that include all plant life forms (e.g., BFG, 2015) often use a geographic definition of the Caatinga, irrespective of the clearly distinct biomes that usually occur as scattered enclaves within the region. By not taking into account a biologically meaningful delimitation of Caatinga to capture only its elements from the SDTFW biome, such taxonomic plant lists are greatly inflated with species from other unrelated vegetation types as highland rupestrian grasslands, savannas, and rainforests. While we acknowledge the relevance and importance of taxonomically-verified regional floras or catalogues that follow geographic or political divisions, biome-based checklists should also be encouraged, as they can provide a more accurate foundation for crossbiome comparisons and serve as the basis for further analyses of the functions and evolution of the plant communities. Increasing theoretical advances in understanding and delimiting biomes (e.g., Schrire et al., 2005; Hughes et al., 2013; Dexter et al., 2015), the collaborative construction of the on-line taxonomic catalogue Flora do Brasil 2020 (http://floradobrasil.jbrj.gov.br), and easy access to herbarium

2. Materials and methods 2.1. Study area in the context of a biologically meaningful definition of Caatinga The word Caatinga has been used to refer to different phytogeographical categories, leading to misconceptions and miscommunication (Queiroz et al., 2017). Reliable diversity assessments, as well as understanding of macro-evolutionary and biogeographical patterns, will depend on how the Caatinga is defined. We argue here that Caatinga must be defined to include only the vegetation types associated with the SDTFW biome, i.e., all types of seasonally dry vegetation from Northeast Brazil, generally succulent-rich, which are not subjected to regular fire regimes due to the lack of a continuous grass-layer. This definition 2

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Schrire et al., 2005), including fire-prone, grass-rich, and succulentpoor vegetation (including Cerrado and rupestrian grasslands) that occur preferably on poor, deep, aluminium-rich soils with high waterretention capacities; and, (3) rainforest, represented by tropical wet forests that generally grow on poor, loamy soils with high water-retention capacities where rainfall is greater than 1500 mm-y, and do not experience droughts lasting more than three months. We included in our checklist only species that were recorded in SDTFW biome from Northeast Brazil (see Appendix 1). Ecological amplitude was assessed through species occurrence in those other biomes and we defined three categories (1) Caatinga endemic as those taxa that occur only at the Caatinga-SDTFW; (2) non endemic SDTFW specialists as those taxa occurring only in SDTFW biome but in at least one more SDTFW area across the Neotropics; and (3) non-specialists as those taxa that occur in Caatinga-SDTFW and additionally in savannas and/or rain forests.

highlights the greater importance of the ecology rather than the geography in structuring diversity patterns and evolutionary history of plant taxa (Pennington et al., 2009; Cardoso and Queiroz, 2011). Additionally, it stands on the original and widely usage of the term Caatinga, a word derived from the Tupi language meaning white woodland, making reference to the clear aspect of the strongly deciduous vegetation at the dry season. It embraces a broad range of structural types (Fig. 1A-E), occurring under a variety of environmental conditions (elevation, climate, soil types, and topography) that can be roughly divided into: (i) dry woodlands established over the flat landscapes of lowland crystalline Sertaneja Depression; (ii) deciduous and semi-deciduous forests, generally found on moister sites or at higher elevations on mountain slopes and plateaus; (iii) woodlands on sandy, sedimentary landscapes; (iv) scattered aquatic habitats; and (v) inselberg outcrops (Moro et al., 2014; Queiroz et al., 2017). Our definition excludes other minor biomes embedded within the vast continuous Caatinga dry vegetation that were previously treated as part of the so called “Caatinga Domain”. Therefore, the enclaves of brejos de altitude (rainforest biome), as well as the cerrado and rupestrian grasslands (savanna biome) that occur across Northeastern Brazil (but mainly in the Chapada Diamantina region of the northern Espinhaço Range in Bahia), are not considered as part of the Caatinga as defined here. A workable distribution map of the Caatinga SDTFW is depicted in Fig. 1. It is modified from Queiroz et al. (2017), and embraces the “Caatinga” and “Dry Atlantic Forest” ecoregions from Olson's classification (2001). Additionally, areas above 900 m within the Chapada Diamantina were excluded because the dominant vegetation is composed of savannas and rupestrian grasslands. Total area extension of the Caatinga, as so defined, is approximately 833,000 km2.

3. Results The new checklist assembled here revealed that Caatinga seasonally dry forests and woodlands harbour at least 3347 species, 962 genera, and 153 families of flowering plants (Appendix 1 and Fig. 2). Nonwoody components (herbs, sub-shrubs, and herbaceous climbers) represent 56.3% of the species diversity, whereas woody components (trees, shrubs, and woody climbers), represent 43.7% (Appendix 2). Non-woody climbers (333) are almost twice as frequent as woody climbers (182). Epiphytic and parasitic species account for 2.7% and 1.5% of total diversity respectively. Fabaceae (490 species/112 genera) is the most species-rich family, followed by Euphorbiaceae (199/27), Poaceae (142/56), Asteraceae (141/78), Malvaceae (140/30), Rubiaceae (113/48), Convolvulaceae (111/13), Bignoniaceae (104/22), Malpighiceae (92/25) and Apocynaceae (90/23). Except for Poaceae, and the also species-rich Cyperaceae, Orchidaceae and Bromeliaceae, which are exclusively composed of herbs, the most diverse Caatinga flowering plant families largely contribute to both woody and nonwoody species diversity. Myrtaceae (11th on the overall flora) assumes high importance when considering only its woody component (4th woody family). The main genera within Caatinga are Croton (72 species), Mimosa (44), Chamaecrista (41), Ipomoea (37), Senna (36), Eugenia (34), Jacquemontia (30), Turnera (30) and Evolvulus (26). Most part of flowering plant species in the Caatinga could be considered as non-specialist, by also occurring in rainforest and/or savanna (Appendix 3). A total of 1319 species (39.4%) occur in all three major tropical biomes, whereas 757 (22.6%) and 521 (15.5%) species are shared between Caatinga and savanna and Caatinga and rainforest biomes respectively. SDTFW specialists correspond to 22.3% (747 species) of all Caatinga species. Most SDTFW specialists (526 species, approximately 15.7% of total diversity and 70.5% of SDTFW specialists) are Caatinga endemics, including 29 endemic genera. The richest Caatinga families in terms of endemics are Fabaceae, Euphorbiaceae, Cactaceae, Bromeliaceae, Malvaceae, and Apocynaceae. The checklist for the flowering plants of the Caatinga SDTFW, as well as the summary of growth-form and distribution within major biomes are available for download at https://doi.org/10.6084/m9.figshare.10006637.

2.2. Assembling the checklist and data standardization We compiled informative data from previously published local and regional scale checklists for the Caatinga (e.g. Moro et al., 2014; BFG, 2015) together with complementary information derived from online databases. We retrieved information about species occurrences and plant growth form from the Flora do Brasil 2020 Project (http:// floradobrasil.jbrj.gov.br) and virtual herbarium collections provided by the INCT - Virtual Herbarium of Flora and Fungi (http://inct.splink. org) and the Rio de Janeiro Botanic Garden (JABOT, http://jabot.jbrj. gov.br). We took into account the reliability of the identifications, including only types and vouchered specimens annotated by specialists in each taxonomic group. Recently-published species were also included in our list. We excluded any taxa below the species rank (such as variety, subspecies), natural hybrids, specimens assigned only to genus or family levels, those with uncertain identifications (confer and affinis), as well as exotic species. The family-level classification system follows APG IV (2016). Synonyms, scientific names, and authors were updated according to Flora do Brasil 2020. 2.3. Species distributions and ecological amplitudes We gathered information about the distribution of species within distinct tropical biomes from relevant literature sources (taxonomic revisions, monographs, and papers of recently described species) as well as available vegetation type information in Flora do Brasil 2020. We also used data from herbarium labels digitized in the following online databases: INCT (http://inct.splink.org); JABOT (http://jabot.jbrj. gov.br); and TROPICOS (http://www.tropicos.org). We converted all available information into the following biomes as globally defined by Schrire et al. (2005): (1) SDTFW (= succulent biome sensu Schrire et al., 2005) encompassing succulent-rich, dry tropical vegetation that is not fire tolerant, occurring associated with fertile soils and erratic rainfall with at least five months receiving less than 100 mm (Pennington et al., 2000); (2) savannas (= grass-rich biome, sensu

4. Discussion 4.1. The Caatinga plant diversity Our checklist revealed exceptional species richness and endemism in Caatinga seasonally dry forests and woodlands, sharply contrasting previous views that the Caatinga flora was relatively well known and species poor, and with few endemics (Andrade-Lima, 1981). The total species count (3347 species) is greater than estimates derived from rarefaction curves (Moro et al., 2014), and represents roughly 10% of the total plant diversity recorded for Brazil (BFG, 2015). The approach 3

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Fig. 2. Representatives of some families of the Caatinga Seasonally Dry Tropical Forest and Woodlands: (A) Acanthaceae (Harpochilus neesianus); (B) Apocynaceae (Aspidosperma pyrifolium); (C) Boraginaceae (Cordia incognita); Cactaceae: (D) Arrojadoa penicillata and (E) Brasilicereus estevesii; Euphorbiaceae: (F) Jatropha mutabilis and (G) Jatropha ribifolia; Fabaceae: (H) Amburana cearensis, (I) Libidibia ferrea, (J) Lonchocarpus obtusus, (K) Tabaroa caatingicola, (L) Trischidium molle; (M) Malvaceae (Ceiba pubiflora); (N) Polygonaceae (Ruprechtia ramiflora).

to provide suitable diversity estimates. The BFG (2015) checklist, on the other hand, reported 1304 more species (~39% higher) than recorded here. This is largely due to the use of more broadly defined and geographically delimited concept of Caatinga as they considered it as an ecologically heterogeneous region encompassing different vegetation types of other tropical biomes, such as rainforests and savannas (BFG, 2015). Some inland rainforest enclaves (locally known as brejos de altitude) share most of their species with the Atlantic rainforests (Rodal et al., 2008). The fire-prone savanna (cerrado) found scattered across certain mountain ranges, particularly in Araripe, Ibiapaba, and Chapada Diamantina, are largely distinguished by their floristic/phylogenetic compositions, functional traits, and physiognomies, as well as by the presence of regular fire disturbances (Hughes et al., 2013). The highly endemic flora of the rupestrian grasslands of the Espinhaço Range are connected to other rupestrian grasslands in central Brazil and also to the Pantepuis in the

adopted here explicitly attempts to establish a more biologically meaningful, biome-based concept of the Caatinga that includes only seasonally dry vegetation and resulted in higher (Moro et al., 2014) or lower (BFG, 2015) figures for species diversity than previous checklists dealing with the Caatinga flora. Incongruent species count can be the result of differences in the methods and concepts applied in previous aggregated checklists. Moro et al. (2014) based their checklist exclusively on the compilation of sitebased floristic and/or phytosociological data, resulting in a large underestimation of species richness (approximately 50% of overall diversity reported here). The high proportion of newly assembled species highlights the fact that herbarium collections and taxonomic monographs are fundamental to the construction of regional checklists (Forzza et al., 2012). Because floristic and ecological surveys are highly biased towards collecting woody components (Moro et al., 2015; Queiroz et al., 2015), they should be used together with other sources 4

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plants within Caatinga are made by therophytes, which escape harsher conditions as resistant seeds, being thus mostly negligible during the dry season and treated as virtually absent in many studies (Costa et al., 2016). Cyperaceae is exceptionally well-represented within aquatic communities established in temporary lakes and ponds that also support an essentially aquatic flora composed of species of Pontederiaceae, Nympheaceae, and Cabombaceae (Queiroz et al., 2017). Among climbing forms, Convolvulaceae confirms the same trend of high numbers of herbaceous climbers in SDTFW, as previously highlighted by Gentry (1995). The high diversity of that family is also reflected at the genus level, with Ipomoea, Jacquemontia, and Evolvulus being among the most species rich genera in the Caatinga. The relatively low recorded numbers of epiphytes (90 species, 2.7% of total diversity) is a commonplace pattern within neotropical SDTFW, which have always been considered poor in epiphytes (Moro et al., 2014). This is in strong contrast to the Atlantic rainforest, where epiphytes represent more than 15% of the total vascular plant richness, with 78% of their total diversity being composed of endemics (Freitas et al., 2016). Seasonal climates with erratic rainfall do not favour epiphytes, which are highly limited by water and nutrient availabilities (Lüttge, 2008). Epiphytic species are related to moister sites in forest physiognomies, particularly those close to the Atlantic Rain Forest (e.g., Cardoso and Queiroz, 2008). Most Caatinga epiphytes belong to Orchidaceae and Bromeliaceae, which are highly diverse in eastern Brazil and are the main epiphytic families in the rainforests of the Atlantic domain (Freitas et al., 2016).

Guyana shield (Conceição et al., 2016). The uncritical inclusion of those biomes as part of the Caatinga would inevitably inflate species richness as they harbour quite distinct floras that were assembled by different ecological and historical processes (Schrire et al., 2005; Hughes et al., 2013). The lack of floristic studies of the overall diversity of any of other neotropical SDTFW nuclei makes cross-flora assessments difficult. In a rough comparison of the woody component, our species count (1462 woody species) stands slightly higher than the previous number reported for the dry forests of central Brazil (1344 woody species DRYFLOR, 2016), reinforcing the view of the Caatinga as the most species rich nucleus of the SDTFW biome (Queiroz et al., 2017). The vast extension of the Caatinga (c. 31% of the entire biome in the Neotropics) represents a potential explanation for such high diversity (DRYFLOR, 2016; Queiroz et al., 2017). Additionally, the SDTFW biome is characterized by high floristic turnover between and within each nucleus (DRYFLOR, 2016). In the Caatinga, the disparate floristic groups are mainly distinguishable by the geological substrates they occupy, causing high floristic variation even in local scales (Cardoso and Queiroz, 2007; Santos et al., 2012; Moro et al., 2016). Arboreal Caatinga, a forest form occurring in areas where soil fertility and annual precipitation are both higher than average, presents an unusually high proportion of dry-adapted Myrtaceae lineages that greatly contribute to their overall diversity (Cardoso and Queiroz, 2008). Other island-like areas also greatly increase diversity, with their elevated plant endemism. The continental dune system in the middle of São Francisco river, for example, harbours an exceptionally high number of endemic plant species (Rocha et al., 2004; Queiroz et al., 2017). The species diversity of the Caatinga is far lower than those of other neotropical regions in absolute numbers, but it appears exceptionally diverse if we look at the species/area ratio. A recently published taxonomically vetted checklist for the lowland Amazon rainforest (Cardoso et al., 2017), for example, suggests the existence of ~14,000 species in an area of ~5,500,000 km2 (2.5 × 10−3 species/km2). Caatinga, in turn, harbours approximately one fourth of the Amazon plant diversity in an area six times smaller, resulting in a ratio of 4.0 × 10−3 species/ km2. Aspects that are thought to influence diversity and species assemblages such as altitudinal, climatic, and soil gradients are much less pronounced in the lowland Amazon (Hoorn et al., 2010). If other nuclei of SDTFW have proportional number of species, it is likely that the whole SDTFW harbours species diversity as impressive as any other tropical biome.

4.3. Species endemism and distribution with respect to other neotropical biomes An unexpected pattern found here is that a high number of species inhabiting the Caatinga are shared with other tropical biomes (rainforest, savanna, or both). Plant communities of the Caatinga SDTFW can be largely influenced by the surrounding vegetation of other biomes (Apgaua et al., 2015). The Caatinga is bordered by the Atlantic rainforest to the east and Cerrado savannas to the west. Particularly important in this context are the regions known as agreste (where dryadapted and typically rainforest elements mix) and Campo Maior (characterized as an ecotonal region where Caatinga occurs together with different forms of cerrado) that are both considered here as part of the Caatinga. Major mountain ranges embedded within the vast drylands can also be regarded as potential borders as they are generally associated with a mosaic of different vegetation types that include rainforests, cerrado, and rupestrian grasslands (depending on rainfall and soil features). The adjacency and connectivity of different biomes within such a small area provide geographic opportunities for ecologically labile species to expand their ranges and be recorded in different biomes even within a small geographic area. The high numbers of shared species between Caatinga seasonally dry vegetation and savannas, as compared to those shared with rainforests, can be explained by climatic features. Recent ordination analysis segregated moist versus dry formations, with both SDTFW and savannas as subgroups within the latter (Dexter et al., 2015). It is evident therefore that some Caatinga-inhabiting species could occupy savanna sites, which also exhibit low annual precipitation and high seasonality (despite some differences in the amounts of precipitation and the duration of the dry period). Those biomes are mainly segregated by ecological drivers such as nutrient poor soils and regular fires in savannas (Hughes et al., 2013). Although edaphic features and regular fire regimes are strong evolutionary constraints, some Caatinga species tolerant of poor soils are likely to survive on savannas when fires remain absent - similar to what has been proposed by Dexter et al. (2018) in a broad continental scale - and some savanna lineages are already adapted to survive long periods with water deficits. Additionally, in the circumscription used here, Caatinga also occupies sedimentary areas, which can potentially harbour lineages pre-adapted to deep, poor,

4.2. Main plant growth forms, families, and genera The most species-rich plant families in the Caatinga as reported here are the same as those presented in other studies, supporting the existence of an oligarchy of families that are ecologically dominant across neotropical SDTFW (Gentry, 1995; Pennington et al., 2009; Moro et al., 2014). The overwhelmingly high diversity of Fabaceae, Euphorbiaceae, Asteraceae, Rubiaceae, and Malvaceae stands out no matter which floristic component is analyzed (overall, woody, or non-woody; Appendix 2), reflecting their wide range of growth-forms and consequent ability to occupy different niches. The impressive contribution of the non-woody component to overall plant species diversity in the Caatinga was anticipated in local scale inventories and previous catalogues (BFG, 2015; Moro et al., 2014, 2015; Queiroz et al., 2015; Queiroz et al., 2017). Encompassing about 70% of total area of the Caatinga, the woodlands growing within the crystalline basement are expected to harbour much higher proportions of herbs than other physiognomies (Moro et al., 2014). Besides the aforementioned families, essentially herbaceous taxa (such as Poaceae and Cyperaceae) greatly contribute to non-woody species diversity. These families are generally referred as minor components of SDTFW flora (Pennington et al., 2009), our data, however, show that it should reflect the emphasis on woody flora inventories. Most of the herbaceous 5

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et al., 2016). The mangrove trees Conocarpus erectus and Laguncularia racemosa (Combretaceae) are additional mistakes. The list of errors detected in Silva and Souza (2018) can be downloaded at https://doi. org/10.6084/m9.figshare.10006637. The inclusion of non-Caatinga SDTFW species is deleterious and can lead to serious implications to our understanding of plant biodiversity patterns and the bioregionalization of the Caatinga. While Silva and Souza (2018) clearly intended to use a biome-specific approach to the Caatinga (“the largest block of seasonally dry forest in South America”), their plant dataset makes clear that it was not the case. We think that any conclusions derived from such a flawed dataset should not be expanded to the Caatinga seasonally dry woodlands. It is unrealistic, for example, to establish conservation planning for the Caatinga based on a bioregionalization analysis where almost 50% of the primary dataset is inaccurate because of negligence in terms of both the use of biologically non-meaningful biome delimitation and the lack of taxonomic validation of the component species.

sandy soils such as those found in the savanna biome. Indeed, the Carrasco (a local name for sedimentary Caatinga) is sometimes referred to as being composed of a mix of SDTFW and savanna elements (Araújo et al., 1998). Remarkably, few species are shared by Caatinga and other neotropical SDTFW nuclei, and most of those occur in adjacent dry forests in central Brazil (DRYFLOR, 2016). The lack of a large set of dominant and widespread SDTFW species, and high floristic turnover, are among the most relevant features of the biome (DRYFLOR, 2016). SDTFW species tend to be confined to each nucleus due to high stability, niche conservatism, and limited dispersal associated with their island-like distributions (Pennington et al., 2009; Queiroz et al., 2017). Ecological barriers imposed by vast expanses of Amazon rainforest and Central South American Cerrado must have limited migration to other ecologically similar areas in the neotropical region (DRYFLOR, 2016; Queiroz et al., 2017). The Caatinga is largely isolated from the remaining patches of the SDTFW meta-community, which can be taken as potential explanation for the high floristic divergence (Sarmiento, 1975), the few shared species, and the high rates of endemism reported here. The existence of different habitats related to geological substrates is also an important factor influencing endemism rates. Sedimentary and karstic surfaces are particularly rich in endemics confined to a single fragment or disjunctly distributed between geologically similar areas (Queiroz et al., 2017).

4.5. Conclusions and future prospects This work represents a starting point for filling in floristic gaps in our knowledge of plant biodiversity across the neotropical SDTFW biome, and especially the Brazilian Caatinga. By comprehensively addressing all known flowering plants, the taxonomically-verified checklist assembled here reveals an impressively high species diversity and endemism in the Caatinga seasonally dry forest and woodlands. Sampling efforts in the Caatinga have been spatially biased, with most specimens being concentrated near access routes and major cities (Oliveira et al., 2016), while vast expanses still await botanical inventories. Collecting deficits and consequent poor taxonomic knowledge can have serious implications, especially in terms of underestimating total diversity. Many newly described taxa, including the new legume genus Tabaroa and the euphorb genus Gradyana, are emblematic of how little we still know about Caatinga plant diversity. Further botanical exploration with increased collecting efforts and taxonomic revisions of poorly studied families may potentially reveal even greater numbers of flowering plants in those spectacular dry forests. The discovery of new taxa is inevitable in light of the myriad of unidentified specimens in Brazilian herbaria. Examinations of herbarium specimens have revealed new Caatinga species that remained unnamed for long periods after they were first collected (e.g., Oliveira et al., 2013). Additionally, high levels of genetic divergence are common in the SDTFW biome (e.g., Särkinen et al., 2011) and the everincreasing use of molecular phylogenetic analyses broadly sampled at species levels may also uncover new species that have remained hidden in cryptic species complexes (Queiroz and Lavin, 2011; Särkinen et al., 2011). Although no study has yet specifically addressed Caatinga plant lineages, the broader SDTFW pattern suggests that plant diversity (and endemism) in the Caatinga has been substantially underestimated. The Flora do Brasil 2020 website records more than 550 taxa below the species level for the Caatinga that were not included in our checklist. Those taxa potentially represent genuinely new species that have never been investigated within molecular phylogenetic or genetic structure frameworks. The lack of primary information related to biome-focused plant catalogues is still one of the main impediments to more detailed analyses of SDTFW biodiversity. The only available plant list for the whole neotropical SDTW biome is a compilation of tree species from site-based phytosociological studies (e.g., DRYFLOR, 2016), and new insights into the conservation and high floristic turnover of SDTFW have already emerged from the analysis of that still incomplete dataset. Likewise, all previous attempts to assemble a plant species list for the Caatinga seasonally dry forests and woodlands of northeastern Brazil have failed either by underestimating the true species diversity (e.g. Moro et al., 2014), because of considerable numbers of misidentifications (e.g. Silva and Souza, 2018), or by largely inflating plant diversity due to the use

4.4. Taxonomically verified databases open new perspectives to our understanding of plant ecology, evolution, and biogeography in the Caatinga Floristic lists do not merely count plant species in certain environments or regions. The fundamental knowledge they represent can be employed in constructing large-scale hypotheses in the fields of ecology, biogeography, and evolution (Hortal et al., 2015). With the increase of easily available georeferenced biological data through online databases, tools are now available for rapidly assembling species lists. While we acknowledge the paramount importance of online databases and their revolutionary effects on how we look at macro-evolutionary patterns in biodiversity (eg., Oliveira et al., 2016; Antonelli et al., 2018; Silva and Souza, 2018), drawing conclusions based on uncritical uses of such online plant specimen data can have serious consequences, as it is widely known that most tropical specimens in herbarium collections worldwide are likely to be incorrectly named (Funk, 2006; Goodwin et al., 2015). Macro-evolutionary, ecological, and biogeographical studies can be severely compromised by the use of datasets that have not been taxonomically verified, leading to erroneous conclusions about the function and evolutionary history of biodiversity (Cardoso et al., 2017). As an illustrative example, we reviewed the primary data of a recent biogeographic study of the Caatinga (Silva and Souza, 2018) that relied on a dataset comprising 2666 species occurring in 260 different sites. Amazingly, more than 45% (1205) of the species in that dataset were not congruent with our newly assembled taxonomic checklist (Appendix 4). We found that 179 names (~15% of total incongruence) reported in Silva and Souza (2018) are mistakes involving duplicate species entries (citation of synonyms), spelling variants resulting from typographical errors, and illegitimate names – with several individual species being cited more than once. More important, however, was a total of 1026 species that are demonstrably non-Caatinga SDTFW species, including widely cultivated, naturalized, and invasive species, in addition to many species that occur in other distinct biomes (savannas, rupestrian grasslands, rainforest enclaves) that have been widely discussed here and elsewhere (e.g., Pennington et al., 2000, 2009; Queiroz et al., 2017) as not representing a biologically meaningful concept of Caatinga seasonally dry forests and woodlands. Emblematic errors in that dataset are the listing of Gaylussacia (Ericaceae), Microlicia (Melastomataceae), Paepalanthus (Eriocaulaceae), and Vellozia (Velloziaceae) – all genera highly nested in rupestrian grasslands (Conceição 6

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of biogeographically erroneous concepts of the Caatinga (e.g. BFG, 2015). Despite this contribution of a taxonomic checklist for the Caatinga, most SDTFW nuclei across the Neotropics still lack comprehensive checklists that explicitly incorporate a biologically meaningful concept of biome based on climatic, soil, geological, physiognomic, and floristic characteristics. Ecological or physiognomic heterogeneity is not exclusive to the Caatinga. The Bolivian Chiquitania, another important nuclei of SDTFW (Pennington et al., 2000; Queiroz et al., 2017), is located in a transition zone that mix elements of SDTFW, Amazon rainforest, temperate dry woodlands (Chaco), and savanna (Killeen et al., 1998). Similarly, the island-like distributions of seasonally dry forests in inter-Andean valleys are equally floristically heterogeneous, as they border different surrounding biomes (Särkinen et al., 2012). All such important South American SDTFW nuclei, however, also lack biomefocused taxonomic checklists that could enable more realistic comparisons of diversity patterns across all floristic components, not just (for example) trees. We believe that in order to properly enhance our understanding of plant biodiversity using the massive quantities of information available in online databases, it must first pass through the collaborative filters of evolutionary ecologists, biogeographers, and taxonomists (Baker et al., 2017). Taxonomically verified checklists could then be used as a first large step in the growth of the scientific knowledge, especially in terms of the still poorly known Caatinga and SDTFW biome. We expect that the present study will encourage more SDTFW-biome-focused checklists and open new perspectives for a better understanding of the extraordinary plant diversity, biogeography, and ecology of neotropical seasonally dry forests and woodlands.

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Funding This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico [grant numbers 141560/ 2015-0; 306736/2015-2, and 303585/2016-1], Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [grant numbers 88881.133545/2016-01 and 23038.009148/2013–19], Fundação de Amparo à Pesquisa do Estado da Bahia [grant number APP0037/2016], Fundação de Amparo à Pesquisa do Estado de São Paulo [grant number 2015/50488-5] and The Royal Society [Newton Advanced Fellowship number NAF/R1/180331]. Declaration of competing interest The authors declare that they have no conflict of interest. Acknowledgements We are grateful to all taxonomists that reviewed parts of our checklist. Roy Funch for performing language review. The anonymous reviewers for constructive comments and suggestions on the manuscript; and Lucas Marinho for making the plate with plant species. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.jaridenv.2019.104079. - References Andrade-Lima, D., 1981. The caatinga dominium. Rev. Bras. Bot. 4, 149–153. APG IV, 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181, 1–20. Antonelli, A., Zizka, A., Carvalho, F.A., Scharn, R., Bacon, C.D., Silvestro, D., Condamine, F.L., 2018. Amazonia is the primary source of Neotropical biodiversity. Proc. Natl. Acad. Sci. 115, 6034–6039. Apgaua, D.M.G., Pereira, D.G.S., Santos, R.M., Menino, G.C.O., Pires, G.G., Fontes,

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