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Article • Acta Bot. Bras. 35 (3) • Jul-Sep 2021 • https://doi.org/10.1590/0102-33062020abb0259 linkcopy

Open-access Savannas of the Brazilian semiarid region: what do we learn from floristics?

AuthorshipSCIMAGO INSTITUTIONS RANKINGS

    ABSTRACT

    The Cerrado represents the largest extension of savanna in South America. It occupies large stretches of central Brazil, being fragmented towards the Northeast, Southeast, and South regions of the country. Examples of disjunct patches of vegetation with savanna physiognomy within the Caatinga can be found in the Chapada Diamantina, the Chapada do Araripe, in small areas of southern Ceará State, and also in the coastal plains. This study recorded the floristic composition of four savannas within the Caatinga in northern Ceará State and evaluated the floristic relationships between these and other savannas, Cerrado and Caatinga sites. Periodic floristic collections recorded 247 species distributed among 162 genera and 55 families. Fifty-seven percent of the recorded species were of herbaceous or sub-shrubby habit, while the majority of the flora was of the therophytic life-form. Biogeographic analyses revealed that the study sites differ from typical Cerrado in flora and life-form spectra and have closer floristic relationships with Caatinga vegetation. The presence of floristic elements from the Cerrado, together with species from the Caatinga, in the study sites allows us to conclude that these savanna enclaves in the Caatinga are composed of a mixed flora with typical elements of these two Brazilian biomes.

    Keywords: Brazil; Cerrado; floristics; savanna; semiarid; therophytes; vegetation comparisons

    Introduction

    Savannas are a group of phytophysiognomies dominated by open habitats, where trees and shrubs are found sparsely distributed in the landscape and the ground is covered by a continuous herbaceous layer, often associated with natural fires (Eiten 1982; Pennington et al. 2006; Walter et al. 2008; Townsend et al. 2009). This vegetation typically occurs under seasonal climate where rainfall is more regular and the dry season is less strong than in deciduous Seasonally Dry Forests (Pennington et al. 2006). In South America there are large expanses of savannas: the central Brazilian Cerrado, the Llanos between Venezuela and Colombia, the Gran Sabana in Venezuela, and the savannas of Northern Brazil and the Southern Guianas. The second largest biome in Brazil, the Cerrado, is represented by savannas with large numbers of endemic plant taxa (Eiten 1982; Ratter et al. 1997; Pennington et al. 2006; BFG 2015). The families with the largest number of species in the Cerrado flora are Fabaceae, Malpighiaceae, Myrtaceae, Melastomataceae, Poaceae and Rubiaceae. Nevertheless, in some localities, the vegetation can be dominated by species of Vochysiaceae (Ratter et al. 1997). The Brazil Flora Group´s current data (BFG 2018) listed 33,099 angiosperm species for the whole of Brazil and, of these, 12,113 were recorded for the Cerrado biome, with 7,800 species listed for the cerrado s.s. vegetation (Souza et al. 2018).

    The Brazilian Cerrado occupies a large area of central Brazil, also extending to Bolivia and Paraguay. It has very diversified and dynamic vegetation types and, according to the fire regime and substrate in each locality, physiognomies can vary from open grasslands (campos limpos, campos sujos, campos brejosos) to ecotonal forests known as cerradão and gallery forests (Eiten 1972; Gibbs et al. 1983; Ratter et al. 1997; Harley et al. 2005; Coutinho 2016). The most characteristic vegetation of the Cerrado domain is the cerrado sensu stricto (referred to as cerrado s.s. from here onwards), represented by a savanna with widely spaced shrubs and trees usually between 2-8 m height, displaying twisted and thickened, corky trunks, while the soil is covered by an herbaceous layer with a predominance of Poaceae and Cyperaceae and dicotyledoneous shrubs often with lignotuberous root systems (Eiten 1982; Gibbs et al. 1983; Ratter et al. 1997).

    Apart from the ‘core’ area, savannas with species typical of the cerrado s.s. vegetation also occur in disjunct patches in other biomes in the Northern, Northeastern, Southeastern and Southern regions of Brazil (Eiten 1972; Ratter et al. 2003). Along the coastal environments of Brazil, the coastal savannas (Castro 1994; Castro & Martins 1999; Moro et al. 2011) appear to be associated with the tablelands of the Formação Barreiras, a flat 400 mya deposit in the coastal geomorphological unit found from Amapá to Rio de Janeiro states (Arai 2006; Balsamo et al. 2010) that is sometimes referred to as the tabuleiros costeiros (Castro 1994).

    The best studied disjunct patches of savanna are those embedded within the Amazonian Rainforest biome (Devecchi et al. 2020). Biogeographical studies have shown that, although these sites have a typical savanna physiognomy and share very characteristic species with the cerrado vegetation of Central Brazil (like species of Byrsonima, Qualea, Salvertia and other genera), these patches of open habitats within the rainforest differ floristically from core cerrado sites, with a predominance of widespread and Amazonian species and a high species turnover from site to site (Devecchi et al. 2020).

    Less studies are available for the savanna enclaves found within the semiarid Caatinga biome (caatinga-savannas hereafter). In Northeastern Brazil, savannas are found in the Chapada Diamantina (Bahia State), Chapada do Araripe (Ceará State) and in other areas of Bahia, Piauí, Ceará, Rio Grande do Norte and Paraíba states (Figueiredo 1989; Costa et al. 2004; Juncá et al. 2005; Oliveira et al. 2012; Moro et al. 2015; 2016; Queiroz et al. 2017). While these caatinga-savannas appear to have floristic ties with the Cerrado of central Brazil, they also have species typical of the semiarid Caatinga (Castro 1994; Castro & Martins 1999).

    Despite sharing the same macroclimate of the Caatinga, where the mean annual precipitation is less than 1000 mm with a longer, less predictable and more dramatic dry season than the Cerrado core area, the caatinga-savannas found in Northeastern Brazil develop on poor and acidic soils and are subject to wild fires (Moro et al. 2016; Queiroz et al. 2017). For example, the Chapada Diamantina and the Chapada do Araripe present a variety of substrates that support diverse plant physiognomies. In the Chapada Diamantina the areas of cerrado occur on clay soils while in the Chapada do Araripe the cerradão forests are found on oxisols, a class of soil constituted from mineral material that ranges from imperfectly to heavily drained, and that are naturally acidic and variable in depth (Costa et al. 2004; Rocha et al. 2005; Ribeiro-Silva et al. 2012; Santos et al. 2018).

    Among the characteristic species commonly found between the typical cerrado and these caatinga savanna sites are Bowdichia virgilioides, Curatella americana, Byrsonima crassifolia, Hancornia speciosa, Hymenaea, Salvertia convallariodora and Vatairea macrocarpa (Costa et al. 2004; Moro et al. 2011; Oliveira et al. 2012; Moro et al. 2015; Silva-Moraes et al. 2018). All of these were listed as very widespread Cerrado species by Ratter & Dargie (1992) and Ratter et al. (2003). On the other hand, these Northeastern cerrados are also home to species that are commonly found in the Caatinga, such as Centrosema brasilianum, Chamaecrista flexuosa, Cochlospermum vitifolium and Pityrocarpa moniliformis (Castro 1994; Moro et al. 2011; Oliveira et al. 2012; Moro et al. 2014).

    Mentions of Cerrado enclaves in Northeastern Brazil were made by several authors (Eiten 1982; Castro 1994; Castro & Martins 1999; Ratter & Dargie 1992; Ratter et al. 2003), together with putative floristic elements that might characterize them. Castro (1994) attempted to establish a relationship between such ‘Cerrado areas’ in Northeastern Brazil with the core Cerrado biome and showed floristic and phytosociological differences between cerrado areas from Piauí and São Paulo. While analysing the Cerrado as a whole, Ratter et al. (2003) have shown that the Northeastern Brazilian areas formed a cohesive group; however, the relationship between the caatinga vegetation with caatinga-savannas and the cerrado vegetation was not investigated further. The present work aims to document the flora of four caatinga-savanna enclaves and increase our understanding of the biogeographical links of these caatinga-savannas with typical cerrado and caatinga sites, evaluating their biogeographical relationships.

    Materials and methods

    Study area

    The caatinga-savannas sampled by this study are located in the northeastern region of Ceará state, in the municipalities of Granja and Martinópole (Fig. 1). The coordinates of the localities studied are listed in Table 1. The predominant climate in the municipalities is hot tropical mild semiarid, varying to hot tropical sub-humid at the limits of Granja with the Ibiapaba highlands, and hot tropical semiarid in Martinópole, close to the central Ceará lowlands (IPECE 2007). The average annual temperature is around 27°C with an average annual precipitation of 1.115 mm in Granja and 1.009 in Martinópole (FUNCEME 2019).

    Figure 1
    Location of the study areas in the municipalities of Granja and Martinópole in Northern Ceará, Brazil. Source of satellite images: Google Earth 2020.

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    Table 1
    Location, acronyms, vegetation type and geographical coordinates of the study areas.

    The localities studied in Granja (S1, S2 and S3) (Figs. 2A-C), comprise sandy, clay and stony soils. The vegetation physiognomies of these localities vary from open savannas similar to the cerrado sensu stricto (cerrado s.s.), according to the classification of Walter et al. (2015), from transition zones between Caatinga-Cerrado, to forested physiognomies similar to more densely woody, ecotonal cerradão forests. S1 has soils ranging from sandy to clay, the herbaceous layer is well developed, and the trees and shrubs are sparsely distributed throughout the landscape. S2 is located over a quartzitic rock outcrop and it is a principal area of Caatinga-Cerrado ecotone studied. S3 is characterised by sandy and stony, lateritic soil with rocks formed in a process of intense weathering from the mother-rock, and rich in Fe and Al (Costa 1991). The study area in Martinópole (S4) (Fig. 2D) has predominantly sandy soils that are stony in some sections, and support arboreal vegetation resembling a cerradão.

    Figure 2
    Landscapes of the study areas in Granja (A, B, C) and Martinópole (D) in Northern Ceará. Granja, CE A) S1; B) S2; C) S3, Martinópole D) S4. Photographs: A-B) E.B. Souza, C-D) I.V. Nepomuceno.

    Floristic survey

    Fertile plant specimens were collected in the four caatinga-savannas in expeditions carried out between May 2016 and August 2019. Appropriate herborization techniques were followed (Mori et al. 1989) and the herbarium samples were deposited in the Herbarium ‘Professor Francisco José de Abreu Matos’ (HUVA) of the Vale do Acaraú State University (UVA). Duplicates, when available, were sent to the herbaria EAC and HUEFS (herbarium acronyms according to Thiers 2021, continuously updated).

    We consulted the relevant literature, such as the monographs of the Flora of Ceará (Menezes et al. 2013; Soares-Neto et al. 2014; Lima et al. 2018; Nepomuceno et al. 2018) and specialized taxonomic databases - Flora do Brasil 2020 (Flora do Brasil 2020 2019) and CRIA (2019), to identify the specimens. Plant specialists in the families Asteraceae, Bignoniaceae, Cyperaceae, Euphorbiaceae, Poaceae and Rubiaceae were consulted. Family circumscriptions follow the classification proposed by APG IV (2016), except for the Turneraceae, which was recognised as distinct from Passifloraceae (see Tokuoka 2012). Species names, their respective authors, geographic distribution and endemism are in accordance with BFG (2018). In addition, we classified each species into Raunkiaer life-forms to obtain the biological spectrum of the areas (Martins & Batalha 2011). The classification of Raunkier's life-forms follows the classification of Martins & Batalha (2011) and was observed in the field. When the life-form could not be defined in situ, data from the literature were consulted to determine the appropriate life-form.

    To compare the life-form spectra of our sites with other vegetation types, we used an ordination analyses (NMS - non-metric multidimensional scaling using Eucliden distances) to contrast the spectra we compiled in our study sites with the spectra of other biomes, as compiled by Costa et al. (2016) (https://doi.org/10.6084/m9.figshare.12755876, Tab. S1 in supplementary material).

    Biogeographical analyses

    We built a database with floristic lists of sites harbouring caatinga-savannas, typical caatinga and typical cerrado vegetation (https://doi.org/10.6084/m9.figshare.12755876, Tab. S2 in supplementary material). We only selected from the literature studies that included both woody (trees and shrubs) and non-woody (herbs and subshrubs) plant species. We then performed grouping (UPGMA - unweighted arithmetic average) analyses using Bray-Curtis distance (Gotelli & Ellison 2011; Legendre & Legendre 2012) to compare the general floristic resemblance between sites.

    We made the UPGMA analyses for the woody component and also for the non-woody component in order to evaluate whether each vegetation layer has or has not different floristic affinities (https://doi.org/10.6084/m9.figshare.12755876, Tab. S2 in supplementary material). Lianas were removed from the analyses, because it was not possible to differentiate between woody and non-woody climbers using the Flora do Brasil 2020 (2019) database. We also compared the flora of caatinga-savannas, caatinga and cerrado sites using Venn diagrams for the woody and non-woody components using Venny 2.1 (https://bioinfogp.cnb.csic.es/tools/venny/).

    Results

    We recorded 246 species in the four sites, comprised of 162 genera and 55 families (Tab. 2, Fig. 3). The family Fabaceae (49 spp.), Rubiaceae (19 spp.), Convolvulaceae (17 spp.), Poaceae (11 spp.), Cyperaceae (10 spp.), Asteraceae (9 spp.), Lamiaceae (9 spp.) and Malvaceae (8 spp.) were the richest families, and represented 53.4 % of the flora. The genera Ipomoea and Mimosa, each with seven species, stood out as the most diverse, followed by Borreria, with six species and Chamaecrista and Combretum with five species each. Within the general flora, we found Borreria sp. nov., a new species yet to be described and 76 species endemic to Brazil, of which six are recorded only for Northeastern Brazil: Stilpnopappus cearensis, Croton anisodontus, Mimosa ulbrichiana, Schultesia angustifolia, Hexasepalum gardneri (and Mitracarpus fernandesii (BFG 2018).

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    Table 2
    Lists the species recorded in the caatinga-savannas in the Caatinga of Northern Ceará. Th - Therophytes, Cr - Cryptophytes, He - Hemicryptophytes, Ch - Chamaephytes, Ph - Phanerophytes, PN - Popular Name, END - Endemism, BR - Endemic from Brazil, NE - Endemic from Northeastern Brazil, S1, S2 and S3 - Areas situated in the municipality of Granja - CE, S4 - Area situated in the municipality of the Martinópole - CE. Collectors: EBS - Elnatan Bezerra de Souza, FAAN - Francisco Álvaro Almeida Nepomuceno, IVN - Izaíra Vasconcelos Nepomuceno.

    Figure 3
    Some species collected in the caatinga savanna studied. A-D) Species in common with the Cerrado, E-H) Species in common with the Caatinga. A) Bowdichia virgilioides Kunth., B) Byrsonima coccolobifolia Kunth., C) Curatella americana L., D) Hirtella ciliata Mart. & Zucc, E) Copernicia prunifera (Mill.) H.E. Moore, F) Combretum leprosum Mart., G) Encholirium spectabile Mart. ex Schult. & Schult.f., H) Xiquexique gounellei (F.A.C. Weber) Lavor & Calvente. Photographs: A) E.B. Souza, B-H) I.V. Nepomuceno.

    Only six species were recorded in all four study areas: Combretum laxum, Ipomoea eriocalyx, Cyperus schomburgkianus, Curatella americana, Bauhinia ungulata and Qualea parviflora. In contrast with the small number of species occurring in the four areas, 158 species were collected only in one locality, 53 exclusive to S1, 52 in S2, 20 in S3 and 33 in S4.

    The non-woody component represented 56.9 % of the total flora, with 113 herbaceous species and 27 sub-shrubby species (Fig. 4). The woody component, with trees and shrubs, is constituted by 82 species. The shrubs vary between 1-6 m in height and mostly belong to the Fabaceae (6 spp.), Combretaceae (5 spp.) and Rubiaceae (5 spp.), while the trees, ranging in size from 2-12 m height, belong to the Fabaceae (15 spp.), Ochnaceae (4 spp.) and Vochysiaceae (4 spp.). Significant numbers of vines were recorded in our sites, 24 species in total, mainly Bignoniaceae (9 spp.) and Convolvulaceae (7 spp.).

    Figure 4
    Spectrum of habit of the species recorded in each study area in Northern Ceará.

    Analysing the composition of the vegetation of each area separately, we observed the high richness of herbaceous species in the open habitats S1, S2, and S3, where herbs and subshrubs represent the majority of the flora (Fig. 4). Only in S4 it is possible to observe a similar number of herbaceous and tree species, 33 and 38 species, respectively, because this site has more closed vegetation. The climbers are divided between woody (9 spp.) and herbaceous climbers (15 spp.) and were recorded in higher numbers in S3.

    The UPGMA analyses of separate life-forms has demonstrated that the flora of the savannas in the Caatinga is more closely related to the Caatinga biome than to the Cerrado biome. The grouping analysis of the woody component showed that all these caatinga-savannas formed a group, and that this group was closer to the caatinga vegetation than to the cerrado vegetation. An exception was the caatinga-savanna of the Chapada do Araripe, where the woody flora shares more species with the Cerrado (Fig. 5). The non-woody species displayed a similar pattern, with the caatinga-savannas being closer to the caatinga vegetation than to the cerrado vegetation, despite sharing some species with the cerrado (Fig. 6).

    Figure 5
    Dendrogram obtained in grouping analysis UPGMA with Bray-Curtis distance for woody component (cophenetic correlation coefficient = 0.910).

    Figure 6
    Dendrogram obtained in grouping analysis UPGMA with Bray-Curtis distance for non-woody component (cophenetic correlation coefficient = 0.920).

    The Venn diagram shows that the savannas in the Caatinga have more species in common with the caatinga vegetation than with the cerrado (Fig. 7). In the database used here the caatinga-savannas shared 39 woody species with the cerrado vegetation, while 60 species are exclusive to these areas and 38 are shared with the caatinga vegetation (either on crystalline or sedimentary substrates) (Fig. 7A). In the Venn diagram for non-woody species, only 13 species from the caatinga-savannas are shared with the cerrado, while 22 species are shared with the caatinga and 90 are exclusive from the latter (Fig. 7B).

    Figure 7
    Veen diagrams showing the number species per area. A) Veen diagram for woody component. B) Venn diagram for non-woody component.

    In order to document the structure of these sites, we recorded the Raunkier life-forms and observed that the therophytes, plants survive the drought in the form of seeds (Martins & Batalha 2011), represent the majority of the local flora (42.2 %), with 104 species (Fig. 8). The phanerophytes, species with buds exposed over 50 cm above the ground (Martins & Batalha 2011), represented the second largest group of species: 72 in total (29.3 %). Hemicryptophytes, plants that protect their buds at ground level, had 36 records totalling 14.6 %. A total of 25 species was classified as chamaephytes, individuals with buds that are protected between 50 cm and just above ground level (Martins & Batalha 2011), representing 10.2 % of the total.

    Figure 8
    Spectrum of life-forms of the 246 species from the study area in Northern Ceará.

    When we compared the Raunkiaer life-form spectra of our four sites with the spectra of other Brazilian biomes (Costa et al. 2016), we noted that these caatinga-savannas had spectra similar to the caatinga on crystalline substrates (Fig. 9), with a predominance of therophytes over other life-forms for most areas (Fig. 8). Therophytic species dominate in all areas, with the exception of S4, where we found a predominance of phanerophytes (39 spp.). Therophytes, phanerophytes, hemicryptophytes and chamaephytes are present in all the areas as the main life-forms, however other types are also found in smaller numbers. Cryptophytes, species that possess underground storage structures (Martins & Batalha 2011), were recorded in S1, S3 and S4. Only in S2 did we find epiphytic species, Philodendron acutatum and Trichocentrum cepula (Tab. 2).

    Figure 9
    Non-metric multidimensional scaling (NMS) of caatinga-savannas, Caatinga and Cerrado (stress = 0.128).

    For the NMS analyses performed with the Raunkiaer life-form spectra (Fig. 9) we observed that, while the standard biological specrum of Raunkiaer is dominated by the phanerophytes, the caatinga-savanna and the caatinga in crystalline terrains are both composed of a majority of therophytes. The cerrado areas had a predominance of hemicryptophytes, as previously reported by other studies (Batalha & Martins 2002; Martins & Batalha 2011).

    Discussion

    The species richness in typical cerrado areas is variable, with a relatively low alpha diversity (number of species) while, in a few cases, it is possible to encounter more than 100 woody species occurring in a determined area (Felfili et al. 1992; Ratter & Dargie 1992; Ratter et al. 2003). When considering the four study areas we found a significant number of 82 species in the woody component, even though with low alpha diversity per area, with 22 species in S1, 35 in S2, 23 in S3 and 38 in S4. These numbers are in accordance with the average species per area that Ratter et al. (2003) obtained with the compilation of data from 376 localities of Cerrado vegetation in Brazil.

    The Vochysiaceae is probably one of the more characteristic families of cerrado vegetation (Goodland & Ferri 1979). Six genera of this family occur in Brazil, with Callisthene Mart., Qualea Aubl. and Vochysia Aubl. being strongly associated with the cerrado and occurring in the surrounding biomes, whilst Salvertia A.St.-Hil. is typical of cerrado vegetation (Goodland & Ferri 1979; BFG 2018), but although our sites are many kilometres distant from the core Cerrado domain, we recorded Callisthene minor, Qualea grandiflora and Salvertia convallariodora in our caatinga-savannas. Qualea grandiflora, Q. parviflora and Salvertia convallariodora are commonly cited as widely distributed species in the Cerrado domain (Goodland & Ferri 1979; Felfili et al. 1992; Ratter & Dargie 1992; Ratter et al. 2003; Castro et al. 2007). These same species are also recorded in the Amazonian savannas (Miranda et al. 2006; Magnusson et al. 2008). Other examples of very common species in typical cerrado sites that were recorded in the studied caatinga-savannas were Bouwdichia virgilioides, Byrsonima coccolobifolia, Curatella americana and Hirtella ciliata (Tab. 2, Fig. 3), but typical caatinga species like Cereus jamacaru, Encholirium spectabile, Copernicia prunifera and Combretum leprosum were also found in our sites, making them a mixture of floristic elements from both the Cerrado and Caatinga biomes (Moro et al. 2011).

    The woody (shrubs + trees) component of our study sites is composed by many species common in cerrado vegetation of the core Cerrado biome. We recorded in our study sites Astronium fraxinifolium, Bowdichia virgilioides, Byrsonima coccolobifolia, B. crassifolia, Curatella americana, Dimorphandra mollis, Hymenaea stigonocarpa, Machaerium acutifolium, Plathymenia reticulata, Qualea grandiflora, Q. parviflora and Salvertia convallariodora, that are widely distributed in the core Cerrado areas, and compiled as common species by Ratter & Dargie (1992) and Ratter et al. (2003) and recorded in Souza et al.’s (2018) species list. Other species also common in the cerrado, such as Anacardium occidentale, Copaifera martii, Hirtella ciliata and Ouratea castaneifolia, were also recorded.

    In the herbaceous layer we found the repeated occurrence of species that are commonly listed in Cerrado floras, such the Asteraceae Elephantopus hirtiflorus, the Cyperaceae Bulbostylis junciforme, Rynchospora nervosa, Scleria hirtella, the Fabaceae Chamaecrista diphylla, C. flexuosa, Zornia reticulata and the Poaceae Aristida longifolia, Axonopus marginatus and Trachypogon spicatus (Batalha et al. 1997; Mantovani & Martins 1993; Costa et al. 2004; Tannus & Assis 2004; Magnusson et al. 2008; Moro et al. 2011; Oliveira et al. 2012; Ribeiro-Silva et al. 2012; Souza et al. 2018). We also flag here the occurrence of species typical of the Cerrado as abundant in the areas studied, with Trachypogon spicatus being widely recorded in the floristic lists of Brazilian Cerrado (Mantovani & Martins 1993; Oliveira et al. 2012; Souza et al. 2018) and in Ceará (Costa et al. 2004; Moro et al. 2011; Ribeiro-Silva et al. 2012).

    In S1, the area with the highest richness of herbaceous plants, we observed trees and shrubs distributed sparsely in the environment with an herbaceous layer dominating the landscape (Fig. 2A). This configuration resembles the cerrado s.s. of central Brazil (Walter et al. 2015). In S2, we note a transition area between Caatinga and Cerrado, with shared species typical of both biomes, such as Amburana cearensis, Combretum leprosum, Encholirium spectabile, Xiquexique gounellei and Ruellia paniculata, common in the Caatinga (Araújo et al. 2011; Moro et al. 2014), and Anacardium occidentale, Curatella americana, Byrsonima coccolobifolia, Qualea grandiflora and Q. parviflora (Ratter & Dargie 1992; Ratter et al. 2003; Moro et al. 2011) common in the Cerrado (Fig. 2B). S3 presents a woody vegetation with trees reaching approximately 10 m in height, such as Campomanesia aromatica, Curatella americana, Dimorphandra mollis, Qualea grandiflora and Q. parviflora. In this sense it is similar to the cerradão, the forest facies of the Cerrado (Walter et al. 2015). However, in other stretches of the same study area, we found open areas with widely spaced trees and shrubs, such as Anacardium occidentale, Byrsonima coccolobifolia and Myrcia splendens, and a more continuous herbaceous layer, composed principally by the species Elephantopus hirtiflorus, Cyperus schomburgkianus, Galactia jussiaeana and Streptostachys asperifolia, a physiognomy which resembles that of cerrado s.s. (Fig. 2C) (Walter et al. 2015). S4 also presents a physiognomy similar to that of the cerradão at some sites and dense cerrado s.s. in others, (Fig. 2D), with many trees, namely Andira cordata, Astronium fraxinifolium, Curatella americana, Himatanthus drasticus, Hirtella ciliata, Hymenaea stigonocarpa, Salvertia convallariodora and Stryphnodendron coriaceum composing the landscape. Herbaceous species like the Poaceae Axonopus marginatus, Mesosetum annum e Streptostachys asperifolia and the Cyperaceae Bulbostylis capilaris, Cyperus schomburgkianus and Fimbristylis dichotoma are common in the herbaceous component of S4.

    Despite sharing woody and non-woody species with the core Cerrado biome the total flora of caatinga-savanas is more similar to the surrounding caatinga vegetation. The typical savanna physiognomy that can be observed in these caatinga-savannas did not mean that typical caatinga species were excluded from these areas. We found here that most caatinga-savanna sites were floristically closer to the caatinga than to the cerrado. A remarkable exeption was the woody community in the Chapada do Araripe savanna enclave, which presented a woody flora that is more similar to geographically distant cerrado areas of Goiás and São Paulo than to the surrounding Caatinga. It is possible that the deep, acidic soils from this region, together with higher rainfall and altitude may be the cause of this similarity (Costa et al. 2004; Ribeiro-Silva et al. 2012; Santos et al. 2018).

    Batalha & Martins (2002 and 2004) compiled data from Raunkiaer life-forms in seven areas of Cerrado in Brazil and observed the predominance of hemicryptophytes, followed by phanerophytes and chamaephytes (Costa et al. 2004; Martins & Batalha (2011)), recording the largest occurrence of phanerophytes and hemicyptophytes in the Chapada do Araripe (CE) and in Itirapina (SP), respectively, and Tannus & Assis (2004) who established that hemicryptophytes were dominant in an area with open grassland. In our study areas, phanerophytes (29.3 %) and hemicryptophytes (15 %) have significant representativeness, although they are less rich than the therophytic life-form, which represented 42.3 % of the plant species. Therophytes are predominant in desertic areas according to the Raunkiaer spectrum (Martins & Batalha 2011), whilst in Brazilian biomes they are more representative of the caatinga vegetation (Pennington et al. 2000; Costa et al. 2016), as seen in studies by Araújo et al. (2011) and Queiroz et al. (2015).

    Despite being classified as phygsionomically similar to the cerrado vegetation, our study areas had biological spectra different from other cerrado areas in Brazil and closer to the caatinga, with a high number of therophytic species. This fact could be related to the environmental conditions of the Caatinga biome, where these sites are located, with high temperatures and erratic rain regime and distribution, which favours therophytes, having short life-cycles that are adapted to water restriction and short or unpredictable growing seasons (Martins & Batalha 2011). Thus, the flora of the four studied caatinga-savannas is more similar to the caatinga vegetation than to the cerrado. Of the 247 species recorded in our areas, 150 are listed as occurring in the Caatinga biome as compiled by Moro et al. (2014). Also, we found that the therophytic life-form predominates, a similar situation with that recorded in caatinga vegetation (Araújo et al. 2011; Costa et al. 2016; Queiroz et al. 2015). The large number of therophytes found in the caatinga-savannas is very likely connected to the semiarid climate of the region with lower, less predictable precipitation in these savannas than in cerrados of central Brazil. Nevertheless, these caatinga-savannas share a significant number of typical cerrado species do not present in typical caatinga sites.

    Conclusion

    The caatinga-savanna enclaves studied here are not fragments of typical cerrado vegetation, although possessing savanna physiognomy. The proximity of caatinga vegetation, which surrounds the patches, and the influence of the semiarid climate explain the larger number of therophytic species in relation to the phanerophytes and hemicryptophytes, since therophytes are the dominant life-form in the caatinga. Many species typical of the cerrado vegetation were found in our study areas. Apart from presenting a physiognomy similar to the cerrado s.s. and the taller and more closed cerradão, these areas have various typical species that occur in the ‘core’ Cerrado domain. Nevertheless, the local flora as a whole is closer to the caatinga vegetation than to the cerrado, with the exception of the Araripe savanna enclave. The flora of these enclaves is therefore characterised by a mixture of species typical of the Brazilian cerrado, widespread species and species typical from the caatinga vegetation.

    Acknowledgements

    We would like to thank the specialists Nádia Roque, Regina Célia, Daniela Carneiro-Torres, Cassio van den Berg and Rubens Queiroz for taxonomic identifications. We are very grateful to Nigel Taylor for reviewing the English language and improving the manuscript. EBS and IVN thank the FUNCAP for financing the Projeto Inventário Florístico do Noroeste do Estado do Ceará: Diversidade e Potencialidades do Bioma Caatinga (processo: BP2-0107-00081.01.02/16.) and the MSC grant for IVN. DCZ is a holder of a CNPq productivity grant.

    References

    • Arai M. 2006. A grande elevação eustática do Mioceno e sua influência na origem do Grupo Barreiras. Geologia USP, Série Científica 6: 01-06.
    • Araújo FS, Costa RC, Lima JR, et al 2011. Floristics and life-forms along a topographic gradient, central-western Ceará, Brazil. Rodriguésia 62: 341-366.
    • Balsamo F, Storti F, Salvini F, Silva AT, Lima CC. 2010. Structural and petrophysical evolution of extensional fault zones in low-porosity, poorly lithified sandstones of the Barreiras Formation, NE Brazil. Journal of Structural Geology 32: 1806-1826.
    • Batalha MA, Aragaki S, Mantovani W. 1997. Florística do Cerrado em Emas (Pirassununga, SP). Boletim de Botânica da Universidade de São Paulo16: 49-64.
    • Batalha MA, Martins FR. 2002. Life-form spectra of Brazilian cerrado sites. Flora 197: 452-460.
    • Batalha MA, Martins FR. 2004. Floristic, frequency and vegetation life-form of a Cerrado site. Brazilian Journal of Biology 64: 203-209.
    • BFG - The Brazil Flora Group. 2015. Growing knowledge: An overiew of Seed Plant diversity in Brazil. Rodriguésia 66: 1085-1113.
    • BFG - The Brazil Flora Group. 2018. Brazilian flora 2020: Innovation and collaboration to meet target 1 of the global strategy for plant conservation (GSPC). Rodriguésia 69: 1513-1527.
    • Castro AAJF. 1994. Comparação florística-geográfica (Brasil) e Fitossociológica (Piauí-São Paulo) de amostras de cerrado. PhD Thesis, Universidade Estadual de Campinas, Campinas.
    • Castro AAJF, Castro NMCF, Costa JM, et al 2007. Cerrados Marginais do Nordeste e Ecótonos Associados. Revista Brasileira de Biociências 5: 273-275.
    • Castro AAJF, Martins FR. 1999. Cerrados do Brasil e do Nordeste: caracterização, área de ocupação e considerações sobre a sua fitodiversidade. Pesquisa em Foco 7: 147-178.
    • Costa ACM, Moro MF, Martins FR. 2016. Raunkiaerian life-forms in the Atlantic forest and comparisons of life-form spectra among Brazilian main biomes. Brazilian Journal of Botany 39: 833-844.
    • Costa IR, Araújo FS, Lima-Verde LW. 2004. Flora e aspectos auto-ecológicos de um encrave de cerrado na chapada do Araripe, Nordeste do Brasil. Acta Botanica Brasilica 18: 759-770.
    • Costa ML. 1991. Aspectos geológicos dos lateritos da Amazônia. Revista Brasileira de Geociências 21: 146-160.
    • Coutinho LM. 2016. Biomas brasileiros. 1st. edn. São Paulo, Oficina de Textos.
    • CRIA - Centro de Referência e Informação Ambiental. 2019. SpeciesLink. http://www.splink.org.br 14 Jun. 2019.
      » http://www.splink.org.br
    • Devecchi M, Lovo J, Moro M, et al 2020. Beyond forests in the Amazon: biogeography and floristic relationships of the Amazonian savannas. Botanical Journal of the Linnean Society 193: 478-503.
    • Eiten G. 1972. The Cerrado Vegetation of Brazil. The Botanical Review 38: 201-341.
    • Eiten G. 1982. Brazilian “Savannas”. In: Huntley HJ, Walker BH. (eds.) Ecology of Tropical Savannas. Berlin, Heidelberg, Springer-Verlag. p. 25-47.
    • Felfili JM, Silva-Júnior MC, Rezende AV, et al 1992. Análise comparativa da florística e fitossociologia da vegetação arbórea do Cerrado sensu stricto na Chapada Pratinha, DF-Brasil. Acta Botanica Brasilica 6: 27-46.
    • Figueiredo MA. 1989. Nordeste do brasil: relíquias vegetacionais no semi-árido cearense (cerrado). Coleção Mossoroense, Série B 646: 3-13.
    • Flora do Brasil 2020. 2019. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/ 14 Jun. 2019.
      » http://floradobrasil.jbrj.gov.br/
    • FUNCEME - Fundação Cearense de Meteorologia e Recursos Hídricos. 2019. Dados Históricos. http://www.funceme.br/produtos/script/chuvas/Download_de_series_historicas/DownloadChuvasPublico.php 27 Jul. 2019.
      » http://www.funceme.br/produtos/script/chuvas/Download_de_series_historicas/DownloadChuvasPublico.php
    • Gibbs PE, Leitão-Filho HF, Sheperd G. 1983. Floristic Composition and Community Structure in an Area of Cerrado in SE Brazil. Flora 173: 433-449.
    • Goodland RJA, Ferri MG. 1979. Ecologia do Cerrado. São Paulo, Editora Itatiaia.
    • Gotelli NJ, Ellison AM. 2011. Princípios de Estatística em Ecologia. Porto Alegre, Artmed.
    • Harley RM, Giulietti AM, Grilo AS, et al 2005. Cerrado. In: Juncá F, Funch L, Rocha W. (eds.) Biodiversidade e Conservação da Chapada Diamantina. Brasília, Ministério do Meio Ambiente. p. 121-152.
    • IPECE - Instituto de Pesquisa e Estratisgia Econômica do Ceará. 2007. http://www2.ipece.ce.gov.br/atlas/lista/index.htm 14 Jun. 2019.
      » http://www2.ipece.ce.gov.br/atlas/lista/index.htm
    • Juncá FA, Funch L, Rocha W. 2005. Biodiversidade e Conservação da Chapada Diamantina . Brasília, Ministerio do Meio Ambiente.
    • Legendre P, Legendre L. 2012. Numeral Ecology. 3rndn. Oxford, Elsevier.
    • Lima IG, Albuquerque AML, Dias ACA, Loiola MIB. 2018. Flora do Ceará, Brasil: Polygalaceae. Rodriguésia 69: 673-692.
    • Magnusson WE, Lima AP, Albernaz ALKM, Sanaiotti TM, Guillaumet JL. 2008. Composição florística e cobertura vegetal das savannas na região de Alter do Chão, Santarém - PA. Revista Brasileira de Botânica 31: 165-177.
    • Mantovani W, Martins FR. 1993. Florística do Cerrado na Reserva Biológica de Moji Guaçu, SP. Acta Botanica Brasilica 7: 33-60.
    • Martins FR, Batalha MA. 2011. Formas de vida, espectro biológico de Raunkiaer e fisionomia da vegetação. In: Felfili JM, Eisenlohr PV, Melo MMRF, Andrade LA, Meira-Neto JAA. (eds.) Fitossociologia no Brasil - Métodos e estudos de caso. Vol. 1. Viçosa, Editora UFV. p. 44-85.
    • Menezes MOT, Taylor NP, Loiola MIB. 2013. Flora do Ceará, Brasil: Cactaceae. Rodriguésia 64: 757-774.
    • Miranda IS, Almeida SS, Dantas PJ. 2006. Florística e estrutura de comunidades Shróreas em cerrados de Rondônia, Brasil. Acta Amazonica 36: 419-430.
    • Mori SA, Silva LAM, Lisboa G, Coradin L. 1989. Manual de manejo do herbário fanerogâmico. 2nd. edn. Ilhéus, Bahia, CEPLAC.
    • Moro MF, Castro ASF, Araújo FS. 2011. Composição florística e estrutura de um fragmento de vegetação savânica sobre os tabuleiros pré-litorâneos na zona urbana de Fortaleza, Ceará. Rodriguésia 62: 407-423.
    • Moro MF, Macedo MB, Moura-Fé MM, Castro ASF, Costa RC. 2015. Vegetação, unidades fitoecológicas e diversidade paisagística do estado do Ceará. Rodriguésia 66: 717-743.
    • Moro MF, Lughadha EN, Araújo FS, Martins FR. 2016. A Phytogeographical Metaanalysis of the Semiarid Caatinga Domain in Brazil. The Botanical Review 82: 91-148
    • Moro MF, Lughadha EN, Filer DL, Araújo FS, Martins FR. 2014. A catalogue of the vascular plants of the Caatinga Phytogeographical Domain: a synthesis of floristic and phytosociological surveys. Phytotaxa 160: 1-118.
    • Nepomuceno FAA, Souza EB, Nepomuceno IV, Miguel LM, Cabral EL, Loiola MIB. 2018. The genus Borreria (Spermacoceae, Rubiaceae) in the state of Ceará, Brazil. Rodriguésia 69: 715-731.
    • Oliveira ACP, Penha AS, Souza RF, Loiola MIB. 2012. Composição florística de uma comunidade savânica no Rio Grande do Norte, Nordeste do Brasil. Acta Botanica Brasilica 26: 559-569.
    • Pennington RT, Prado DE, Pendry CA. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. Journal of Biogeography 27: 261-273.
    • Pennington RT, Lewis GP, Ratter JA. 2006. An Overview of the Plant Diversity, Biogeography and Conservation of Neotropical Savannas and Seasonally Dry Forests. In: Pennington RT, Lewis GP, Ratter JA. (eds.) Neotropical Savannas and Seasonally Dry Forests. Boca Raton, CRC Press. p. 1-24.
    • 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.
    • Queiroz 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 Forest Region in South America. Switzerland, Springer International Publishing AG. p. 23-63.
    • Ratter JA, Bridgewater S, Ribeiro JF. 2003. Analysis of the Floristic Composition of the Brazilian Cerrado Vegetation III: Comparison of the Woody Vegetation of 376 Areas. Edinburgh Journal of Botany 60: 57-109.
    • Ratter JA, Dargie TCD. 1992. An analysis of the floristic composition of 26 Cerrado areas in Brazil. Edinburgh Journal of Botany 49: 235-250.
    • Ratter JA, Ribeiro JF, Bridgewater S. 1997. The Brazilian Cerrado Vegetation and Threats to its Biodiversity. Annals of Botany 80: 223-230.
    • Ribeiro-Silva S, Medeiros MB, Gomes BM, Naiana E. 2012. Angiosperms from the Araripe National Forest, Ceará, Brazil. Check List 8: 744-751.
    • Rocha WJSF, Chaves JM, Rocha CC, Funch L, Juncá FA. 2005. Avaliação ecológica rápida da Chapada Diamantina. In: Juncá F, Funch L, Rocha W. (eds.) Biodiversidade e Conservação da Chapada Diamantina . Brasília, Ministisrio do Meio Ambiente. p. 29-45.
    • Santos HG, Jacomine PKT, Anjos LHC, et al 2018. Sistema brasileiro de classificação de solos. 5th. edn. Brasília, DF, Embrapa Solos.
    • Silva-Moraes HG, Cordeiro I, Figueiredo N. 2018. Flora and floristic affinities of the Cerrados of Maranhão state, Brazil. Edinburgh Journal of Botany 76: 1-21.
    • Soares-Neto RL, Cordeiro LS, Loiola MIB. 2014. Flora do Ceará, Brasil: Combretaceae. Rodriguésia 65: 685-700.
    • Souza VC, Flores TB, Colletta GD, Coelho RL. 2018. Guia das Plantas do Cerrado. 1st. edn. Piracicaba, Taxon Brasil.
    • Tannus JLS, Assis MA. 2004. Composição de espiscies vasculares de campo sujo e campo úmido em área de cerrado, Itirapina - SP, Brasil. Revista Brasileira de Botânica 27: 489-506.
    • Townsend CR, Begon M, Harper JL. 2009. Fundamentos em Ecologia. Porto Alegre, Artmed .
    • APG IV - The Angiosperm Phylogeny Group. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20.
    • Thiers B. 2021; continuously updated.. Index Herbariorum: A global directory of public herbaria and associated staff. http://sweetgum.nybg.org/science/ih/ 10 Aug. 2019.
      » http://sweetgum.nybg.org/science/ih/
    • Tokuoka T. 2012. Molecular phylogenetic analysis of Passifloraceae sensu lato (Malpighiales) based on plastid and nuclear DNA sequences. Journal of Plant Research 125: 489-497.
    • Walter BMT, Carvalho AM, Ribeiro JF. 2008. Conceito de Savanna e de seu Componente Cerrado. In: Ribeiro JF, Almeida SP, Sano SM. (eds.) Cerrado: ecologia e flora. Brasília, Embrapa. p.21-45.
    • Walter BMT, Durigan G, Munhoz CBR, Ribeiro JF. 2015. Fitofisionomias do Cerrado: classificação, métodos e amostragens fitossociológicas. In: Eisenlohr PV, Felfili JM, Melo MMRF, Andrade LA, Neto JAAM. (eds.) Fitossociologia no Brasil: mistodos e estudos de casos. Vol. 2. Viçosa, Editora UFV . p.183-212.

    Publication Dates

    • Publication in this collection
      12 Nov 2021
    • Date of issue
      Jul-Sep 2021

    History

    • Received
      03 June 2020
    • Accepted
      16 Nov 2020
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