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

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.

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

Municipality	Location	Acronym	Vegetation	Coordinates
Granja	Papagaios	S1	Open savanna	03°11’11” S, 40°44’35” W
	São Miguel	S2	Ecotone between a savanna and typical caatinga vegetation	03°21’32” S, 41°01’24” W
	Vereda dos Tomás	S3	Savanna (both open and arboreal)	03°13’33” S, 40°55’49” W
Martinópole	Bom Princípio	S4	Tall savanna (similar to arboreal cerrado, the cerradão)	03°11’51” S, 40°41’04” W

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).

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.

Family	Species	Habit	Life-forms	PN	End	Occurrence			Voucher
						S1	S2	S3	S4
Acanthaceae	Elytraria imbricata (Vahl.) Pers.	Herb	Th	-	-				X	EBS 5819
	Ruellia paniculata L.	Shrub	Th	melosa-roxa	-			X	X	EBS 5799, 4728
Amaranthaceae	Gomphrena gardneri Moq.	Herb	He	-	BR				X	EBS 5144
Amaryllidaceae	Habranthus sylvaticus Herb.	Herb	Cr	cebola-de-calango	BR	X				EBS 3754
Anacardiaceae	Anacardium occidentale L.	Tree	Ph	cajú	-		X	X		EBS 3159, 5790
	Astronium fraxinifolium Schott.	Tree	Ph	-	-				X	EBS 5818
Annonaceae	Ephedranthus pisocarpus R.E.Fr.	Tree	Ph	conduru	BR				X	EBS 4715
Apocynaceae	Allamanda blanchetii A.DC.	Tree	Ch	alamanda-roxa	BR	X				EBS 5044
	Aspidosperma multiflorum A.DC.	Tree	Ph	-	BR		X			EBS 5439
	Himatanthus drasticus (Mart.) Plumel.	Tree	Ph	janaguba	BR				X	EBS 3741
	Mandevilla tenuifolia (J.C. Mikan) Woodson	Subshrub	Th	jalapa-do-campo	-		X			EBS 3400
	Tabernaemontana catharinensis A.DC.	Tree	Ph	leiteiro	-		X			EBS 4471
Araceae	Philodendron acutatum Schott.	Herb	Ep	imbis	-		X			EBS 5758
	Taccarum ulei Engl. & K. Krause	Herb	Th	milho-de-cobra	BR				X	EBS 5163
Arecaceae	Bactris major Jacq.	Tree	Ph	tucum	-		X			EBS 5761
	Copernicia prunifera (Mill.) H.E.Moore	Tree	Ph	carnaúba	BR	X			X	IVN 99, EBS 5839
Asteraceae	Aspilia bonplandiana (Gardner) S.F.Blake	Herb	Th	margarida	BR		X	X		EBS 5752, 3621
	Bidens pilosa L.	Herb	Th	picão-preto	-		X			EBS 3398
	Elephantopus hirtiflorus DC.	Herb	He	língua-de-vaca	BR	X	X	X		EBS 3588, 5753, 3622
	Lepidaploa sp.	Herb	Th	-			X			EBS 4145
	Pectis brevipendunculata (Gardner) Sch.Bip.	Herb	Th	chá-de-moça	BR		X			EBS 3379
	Praxelis diffusa (Rich.) Pruski	Herb	Th	cambará	-		X			EBS 4103
	Stilpnopappus cearensis Huber	Herb	Th	-	NE	X				EBS 3605
	Stilpnopappus pratensis Mart. ex DC.	Herb	Th	-	BR	X		X	X	EBS 3485, 3487, 4730
	Stilpnopappus trichospiroides Mart. ex. DC.	Herb	Th	-	BR			X		EBS 3629
Bignoniaceae	Adenocalymma subsessilifolium DC.	Shrub	Ph	-	BR			X		EBS 3628
	Adenocalymma validum L.G. Lohmann	Climber	Ph	-	-				X	EBS 4713
	Fridericia dispar (Bureau ex K.Schum) L.G. Lohmann	Shrub	Ch	cipó-de-boi	BR		X			EBS 4126
	Fridericia limae (A.H. Gentry) L.G.Lohmann	Climber	Ch	cipó-de-bola	NE		X	X	X	EBS 5742, 5769, 5828
	Fridericia platyphylla (Cham.) L.G.Lohmann	Climber	Ch	cipó-una	-		X			EBS 3382
	Fridericia subverticillata (Bureau & K. Schum.) L.G. Lohmann	Climber	Ch	-	BR				X	EBS 4714
	Fridericia triplinervia (Mart. ex. DC.) L.G.Lohmann	Climber	Ch	-	-			X		EBS 3643
	Neojobertia candolleana (Mart. ex. DC.) Bureau & K. Schum.	Climber	Ph	-	BR			X		EBS 3635
Bixaceae	Cochlospermum vitifolium (Willd) Spreng	Tree	Ph	pacotê	-		X		X	FAAN 43, EBS 5809
Boraginaceae	Cordia rufescens A.DC.	Shrub	Ph	grão-de-galo	-	X				EBS 4926
Bromeliaceae	Bromelia laciniosa Mart. ex Schult. f.	Herb	He	macambira	BR		X			EBS 5762
	Encholirium spectabile Mart. ex Schult. & Schult.f.	Herb	He	macambira-de-flecha	BR		X			EBS 3158
Cactaceae	Cereus jamacaru DC.	Tree	Ph	mandacaru	BR				X	EBS 5840
	Pilosocereus catingicola (Gürke) Byles & Rowley	Shrub	Ph	facheiro	BR				X	EBS 5841
	Xiquexique gounellei (F.A.C.Weber) Lavor & Calvente	Shrub	Ph	xique-xique	BR		X			EBS 5720
Chrysobalanaceae	Hirtella ciliata Mart. & Zucc	Tree	Ph	-	-	X			X	EBS 3164, 5836
Combretaceae	Buchenavia tetraphylla (Aubl.) R.A.Howard	Tree	Ph	periquiteira	-		X			EBS 4158
	Combretum glaucocarpum Mart.	Shrub	Ph	sipaúba, vaqueta	-		X			EBS 3385
	Combretum hilarianum D. Dietr.	Shrub	Ph	imbiridiba	-	X				EBS 3464
	Combretum laxum Jacq.	Shrub	Ph	cipó-de-bugio	-	X	X	X	X	EBS 4184, 5440, 5768, 4725
	Combretum leprosum Mart.	Shrub	Ph	mufumbo	-		X		X	EBS 4147, 5821
	Combretum mellifluum Eichler	Shrub	Ph	sipaúba	-		X			FAAN 37
Convolvulaceae	Cuscuta racemosa Mart.	Herb	He	cipó-chumbo	-	X		X		EBS 5222, 3466
	Distimake cissoides (Lam.) A.R. Simões & Staples	Climber	Th	-	-			X		EBS 3632
	Evolvulus ericifolius Mart. ex. Schrank.	Herb	Th	-	BR	X		X		EBS 5051, 3748
	Evolvulus glomeratus Ness. & Mart.	Subshrub	Th	azulzinha	-	X				EBS 5052
	Evolvulus gypsophiloides Moric.	Herb	Th	-	BR	X				EBS 4186
	Evolvulus ovatus Fernauld	Herb	Th	azulzinha	-	X	X	X		EBS 5684, 4112, 3499
	Ipomoea asarifolia (Ders.) Roem. & Schult.	Climber	Th	salsa	-			X	X	EBS 3496, 5810
	Ipomoea bahiensis Willd ex. Roem. & Schult.	Climber	Th	jetirana	BR		X			EBS 4107
	Ipomoea bignonioides Sims	Climber	Th	-	-				X	EBS 5164
	Ipomoea calyptrata Dammer	Climber	Th	-	BR			X	X	EBS 5058, 5162
	Ipomoea eriocalyx (Mart. ex. Choisy) Meisn.	Climber	Th	-	BR	X	X	X	X	EBS 5246, 4138, 3618, 5812
	Ipomoea piurensis O'Donell	Climber	Th	-	-			X		EBS 3497
	Ipomoea subincana (Choisy) Meisn.	Climber	Ph	-	BR	X		X		EBS 3423, 3620
	Jacquemontia gracillima Choisy	Herb	Th	jetirana	BR	X	X			EBS 3471, 4162
	Jacquemontia gracilis Choisy	Herb	Th	-	BR	X				EBS 3579
	Jacquemontia tamnifolia (L.) Griseb.	Herb	Th	-	-		X			EBS 4106
	Operculina hamiltonii (G. Don.) D.F.Austin & Stalpes	Climber	Cr	batatão	-			X		EBS 3498
Cyperaceae	Bulbostylis capillaris (L.) C.B. Clarke	Herb	He	-	-				X	EBS 5155
	Bulbostylis conifera (Kunth) C.B. Clarke	Herb	He	-	-	X				EBS 4930
	Bulbostylis junciformis (Kunth) C.B. Clarke	Herb	He	-	-	X				EBS 5041
	Cyperus amabilis Vahl.	Herb	Th	-	-				X	EBS 5134
	Cyperus sesquiflorus (Torr.) Mattf. & Kük.	Herb	He	junquinho	-				X	EBS 5137
	Cyperus schomburgkianus Ness.	Herb	He	tiririca	-	X	X	X	X	EBS 3477, 5348, 3492, 5145
	Fimbristylis dichotoma (L.) Vahl	Herb	He	-	BR	X			X	EBS 5239, 5169
	Rhynchospora holoschoenoides (Rich.) Herter	Herb	He	-	-	X				EBS 3476
	Rhynchospora nervosa (Vahl) Boeckeler	Herb	Cr	capim-estrela	BR	X				EBS 4916
	Scleria hirtella Sw.	Herb	Cr	-	-	X				EBS 5248
Dilleniaceae	Curatella americana L.	Tree	Ph	lixeira	-	X	X	X	X	IVN 100, EBS 5434, 5770, 4718
	Davilla cearensis L.	Climber	Ch	-	BR		X			EBS 3160
Droseraceae	Drosera sessilifolia A.St.-Hil.	Herb	Th	-	-		X			EBS 5355
Eriocaulaceae	Paepalanthus lamarckii Kunth.	Herb	Th	-	-		X			EBS 4141
	Paepalanthus cf. tortilis (Bong.) Mart.	Herb	Th	-	BR		X			EBS 5345
Erythroxylaceae	Erythroxylum laetevirens O.E. Schulz.	Shrub	Ch	-	BR			X		EBS 5061
Euphorbiaceae	Croton anisodontus Müll.Arg.	Shrub	Ch	-	NE	X	X	X		EBS 5047, 4464, 5795
	Croton glandulosus L.	Herb	Th	carvão-branco	-				X	EBS 5156
	Dalechampia scandens L.	Climber	Th	-	-			X		EBS 3640
	Euphorbia bahiensis (Klotzsch & Garke) Boiss.	Herb	Th	-	-		X			EBS 3394
	Microstachys corniculata (Vahl.) Griseb.	Herb	Th	-	-	X				EBS 4483
	Microstachys hispida (Mart. & Zucc.) Govaerts	Herb	Th	-	-	X				EBS 3417
Fabaceae	Aeschynomene benthamii (Rudd.) Afr.Fern.	Subshurb	Th	-	BR	X				EBS 3592
	Aeschynomene filosa Mart.	Subshurb	He	-	-	X				EBS 5243
	Aeschynomene histryx Poir.	Herb	Th	-	-	X	X	X		EBS 3457, 3374, 3615
	Aeschynomene mollicula Kunth.	Subshurb	Th	-	-	X				EBS 5242
	Amburana cearensis (Allemão) A.C. Sm.	Tree	Ph	cumaru	-		X			EBS 5354
	Andira cordata Arroyo ex R.T. Penn. & H.C. Lima	Tree	Ph	-	BR				X	EBS 5830
	Arachis dardani Kaprov. & W.C. Greg.	Herb	Th	amendoim-de-carcará	BR	X				EBS 3375
	Arachis pusilla Benth.	Herb	Th	-	BR		X			EBS 4458
	Bauhinia acuruana Moric.	Shrub	Ch	-	BR		X			EBS 5357
	Bauhinia cheilantha (Bong.) Steud.	Shrub	Ch	-	-		X			EBS 5366
	Bauhinia ungulata L.	Shrub	Ph	pata-de-vaca	-	X	X	X	X	EBS 3155, 5743, 5775, 4721
	Bowdichia virgilioides Kunth.	Tree	Ph	sucupira	-	X				EBS 3152
	Calopogonium mucunoides Desv.	Climber	Th	-		X				EBS 5321
	Centrosema brasilianum (L.) Benth.	Climber	Th	centrosema	-	X	X			EBS 3601, 5749
	Centrosema pascuorum Mart. ex. Benth.	Climber	Th	centrosema, jetirana	-	X		X		EBS 5335, 3490
	Chamaecrista diphylla (L.) Greene	Herb	Th	-	-	X				EBS 3369
	Chamaecrista flexuosa (L.) Greene	Subshrub	He	-	-	X	X	X		EBS 5228, 3373, 5801
	Chamaecrista linearis (H.S. Irwin & Barneby) Afr.Fern. & E.P. Nunes	Subshrub	Te	-	-	X				EBS 5319
	Chamaecrista rotundifolia (Pers.) Greene	Herb	Th	-	-	X	X			EBS 5240, 4457
	Chamaecrista supplex (Benth.) Britton & Ross ex Britton & Killip.	Herb	Th	-	-		X			EBS 4117
	Chloroleucon foliolosum (Benth.) G.P.Lewis	Tree	Ph	arapiraca	-		X			EBS 5721
	Copaifera martii Hayne	Tree	Ph	pau-d’óleo	-				X	EBS 5820
	Dalbergia cearensis Ducke.	Shrub	Ph	jacarandá-violeta	BR				X	EBS 5148
	Dimorphandra mollis Benth.	Tree	Ph	fava-danta	-			X		EBS 5779
	Galactia jussiaeana Kunth	Subshrub	He	-	-	X	X	X		EBS 4488, 4462, 3624
	Hymenaea stigonocarpa Mart. ex Hayne	Tree	Ph	jatobá-do-cerrado	-				X	EBS 5714
	Machaerium acutifolium Vogel.	Tree	Ph	jacarandá-do-campo	-				X	EBS 5817
	Macroptilium lathyroides (L.) Urb.	Climber	Ch	feijão-de-rola	-	X				EBS 5241
	Mimosa camporum Benth.	Subshurb	Th	-	-	X				EBS 4487
	Mimosa hirsutissima Mart.	Subshurb	Th	-	-	X			X	EBS 5229, 5153
	Mimosa misera Benth.	Subshurb	Th	-	BR	X				EBS 3467
	Mimosa modesta Mart.	Subshurb	Ch	-	BR	X				EBS 3450
	Mimosa pigra L.	Subshurb	Th	calumbi-d’água	-				X	EBS 5158
	Mimosa somnians Humb. & Bonpl. ex. Willd.	Subshurb	Ch	malícia	-	X				EBS 4484
	Mimosa ulbrichiana Harms	Subshurb	Th	-	NE	X		X		EBS 3463, 3489
	Peltogyne confertiflora (Mart. ex Hayne) Benth.	Tree	Ph	jatobá-de-brinco	-		X			EBS 5437
	Piptadenia stipulacea (Benth.) Ducke	Tree	Ph	jurema-branca	BR		X			EBS 5347
	Pityrocarpa moniliformis (Benth) Luckow & R.W.Jobson	Tree	Ph	angico-de-bezerro	BR	X	X	X		EBS 4914, 4467, 5763
	Plathymenia reticulata Benth.	Tree	Ph	candeia	-	X			X	EBS 5236, 5827
	Senna alata (L.) Roxb.	Shrub	Ch	fedegoso-gigante, matapastão	-		X			EBS 5721
	Senna gardneri (Benth.) H.S.Irwin & Barneby	Subshrub	Ch	-	-	X				EBS 3608
	Senna splendida (Vogel) H.S.Irwin & Barneby	Shrub	Ch	-	-			X		EBS 5787
	Senna trachypus (Benth.) H.S.Irwin & Barneby	Shrub	Ch	besouro	BR	X	X	X		EBS 5245, 4120, 3634
	Stryphnodendron coriaceum Benth.	Tree	Ph	barbatimão-do-cerrado	BR				X	EBS 5824
	Stylosanthes angustifolia Vogel	Herb	Th	-	-	X	X			EBS 3448, 4120
	Stylosanthes scabra Vogel	Herb	Th	-	-			X		EBS 3627
	Tephrosia purpurea (L.) Pers.	Herb	He	-	-			X		EBS 3500
	Vatairea sericea (Ducke) Ducke	Tree	Ph	angelim-amargoso	-				X	EBS 5815
	Zornia reticulata Sm.	Herb	He	-	-	X				EBS 4922
Gentianaceae	Chelonanthus purpurascens (Aubl.) Struwe, S.Nilsson & V.A.Albert	Herb	Th	-	-	X				EBS 4181
	Schultesia angustifolia Griseb	Herb	Th	-	NE	X				EBS 5225
	Schultesia guianensis (Aubl.) Malme	Herb	Th	mata-zombando	-	X				EBS 5223
Iridaceae	Cipura paludosa Aubl.	Herb	Cr	alho-do-mato	-	X				EBS 5033
	Trimezia martinicensis (Jacq.) Herb.	Herb	Cr	íris-amarela	-	X			X	EBS 5034, 5131
Krameriaceae	Krameria tomentosa A.St.-Hill.	Subshrub	Ch	carrapicho-de-cavalo	-	X	X		X	EBS 5036, 4463 5146
Lamiaceae	Amasonia campestris (Aubl.) Moldenke	Subshurb	Ch	flor-de-urubu	-	X			X	EBS 4485, 5143
	Cyanocephalus rugosus (Benth.) Harley & J.F.B.Pastore	Subshrub	Ch	-	-	X				EBS 4177
	Eriope macrostachya Mart. ex. Benth.	Herb	He	-	-			X		EBS 3633
	Hypenia salzmannii (Benth.) Harley	Subshrub	He	canela-de-urubu	-	X				EBS 5336
	Hyptis atrorubens Poit.	Subshrub	He	mentinha	-	X	X		X	EBS 5331, 5757, 5833
	Hyptis lanceolata Poir.	Subshrub	He	-	-	X				EBS 5233
	Marsypianthes montana Benth.	Herb	He	alfavaca-de-cheiro	BR	X	X		X	EBS 3475, 4459, 5140
	Rhaphiodon echinus Schauer	Herb	Th	betônica, falsa-menta	BR	X	X	X		EBS 3447, 4176, 3638
	Vitex polygama Cham.	Tree	Ph	tarumã	BR				X	EBS 5838
Lythraceae	Ammannia auriculata Willd.	Herb	Th	-	-	X				EBS 5317
	Cuphea campestris Koehne	Herb	Th	-	-	X	X		X	EBS 4475, 3406, 5138
	Cuphea impatientifolia A.St.-Hill	Herb	Th	-	BR	X			X	EBS 4477, 5154
Malpighiaceae	Byrsonima coccolobifolia Kunth.	Subshrub	Ph	murici-rosa	-		X	X		EBS 5744, 5805
	Byrsonima crassifolia (L.) Kunth.	Tree	Ph	murici-da-praia	-	X		X	X	EBS 4929, 3750, 5268
	Janusia sp.	Shrub	Ph	-			X			EBS 4128
	Peixotoa sp.	Climber	Ch	-			X			EBS 4146
	Stigmaphyllon paralias A.Juss.	Shrub	Ph	-	BR		X	X		EBS 5358, 5063
Malvaceae	Helicteres heptandra L.B.Sm.	Shrub	Ch	saca-rolha	-	X				EBS 5318
	Pavonia cancellata (L.) Cav.	Herb	He	-	-			X	X	EBS 3639, 5808
	Sida ciliaris L.	Herb	Th	-	-	X	X	X		EBS 3442, 4156, 3495
	Sida cordifolia L.	Subshrub	Th	-	-	X	X			EBS 4169, 4123
	Sida linifolia Cav.	Subshurb	Th	-	-			X	X	EBS 5796, 5834
	Sterculia striata A.St.-Hill & Naudin	Tree	Th	chichá	BR		X			EBS 3156
	Waltheria indica L.	Subshrub	He	douradinha	-	X	X	X		EBS 3611, FAAN 40, EBS 3641
	Waltheria operculata Rose	Herb	Th	-	-	X	X	X		EBS 3472, 3381, 3493
Melastomataceae	Comolia villosa (Aubl.) Triana	Herb	He	-	-		X			EBS 4461
	Pterolepis perpusilla (Naudin) Cogn.	Herb	Th	-	BR	X	X			EBS 5322,5751
Myrtaceae	Campomanesia aromatica (Aubl.) Griseb	Shrub	Ph	guabiraba	-			X		EBS 5057
	Campomanesia dichotoma (O. Berg.) Mattos	Shrub	Ph	guabiraba	BR	X				EBS 4918
	Myrcia guianensis (Aubl.) DC.	Shrub	Ph	araçazinho	-	X			X	EBS 3755, 4726
	Myrcia splendens (Sw.) DC.	Shrub	Ph	guamirim-miúdo	BR		X	X	X	EBS 5435, 5804, 5829
Moraceae	Ficus sp.	Tree	Ph	-			X			EBS 4470
Ochnaceae	Ouratea castaneifolia (DC.) Engl.	Tree	Ph	farinha-seca	-				X	IVN 89
	Ouratea cuspidata (A. St.-Hil.) Engl	Tree	Ph	-	BR				X	IVN 77
	Ouratea fieldingiana (Garnder) Engl.	Tree	Ph	batiputá	-				X	IVN 81
	Ouratea glaucescens (A.St.-Hil.) Engl.	Tree	Ph	flor-de-ouro	BR			X	X	EBS 3749, 3735
Olacaceae	Ximenia americana L.	Tree	Ph	ameixa	-		X	X	X	EBS 5729, 5786, 3740
Orchidaceae	Habernaria sp.	Herb	Th	-				X		EBS 5054
	Trichocentrum cepula (Hoffmanns.) J.M.H.Shaw	Herb	Ep	dama-dançante	-		X			EBS 5759
Orobanchaceae	Agalinis hispidula (Mart.) D'Arcy	Herb	Th	-	-	X	X			EBS 5329, 4132
	Buchnera rosea Kunth	Herb	Th	-	-	X		X		EBS 5325, 3491
Oxalidaceae	Oxalis divaricata Mart. ex Zucc.	Herb	Th	azedinha	BR		X			EBS 4104
	Oxalis psoraleoides Kunth	Herb	Th	trevo	-	X	X			EBS 3670, 4460
Passifloraceae	Passiflora foetida L.	Climber	Th	maracujá-de-cheiro	-	X				EBS 4923
Phytolacaceae	Microtea paniculata Moq.	Herb	Th	-	-		X			EBS 3392
Plantaginaceae	Bacopa angulata (Benth.) Edwall	Herb	Th	-	BR	X	X			EBS 5237, 5360
	Bacopa sessiliflora (Benth.) Edwall	Herb	Th	-	-		X			EBS 5748
	Tetraulacium veroniciforme Turcz.	Herb	Th	-	BR	X	X			EBS 3441, 5756
Poaceae	Andropogon angustatus (J. Presl). Steud	Herb	He	-	-		X			EBS 4122
	Aristida longifolia Trin.	Herb	He	-	-	X				EBS 5320
	Axonopus marginatus (Trin.) Chase	Herb	He	capim-mimoso	-				X	EBS 5157
	Isachne sp.	Herb	Th	-			X			EBS 4152
	Mesosetum annuum Swallen	Herb	Th	-	-	X			X	EBS 5038, 5152
	Paspalum maculosum Trin.	Herb	He	canafístula	-	X				EBS 5037
	Paspalum sp.1	Herb	Th	-					X	EBS 5135
	Paspalum sp.2	Herb	Th	-					X	EBS 5147
	Paspalum sp.3	Herb	Th	-					X	EBS 5150
	Streptostachys asperifolia Desv.	Herb	Th	-	-			X	X	EBS 5055, 5159
	Trachypogon spicatus (L. f.) Kuntze	Herb	He	-	-	X				EBS 5050
Polygalaceae	Asemeia cf. monticola (Kunth.) J.F.B. Pastore & J.R. Abbott.	Herb	Th	-	-			X		EBS 5060
	Bredemeyera floribunda Willd.	Tree	Th	botica-inteira	-				X	EBS 4723
	Polygala boliviensis A.W.Benn.	Herb	Th	-	-	X	X			EBS 3488, 3363
	Polygala glochidata Kunth	Herb	Th	-	BR	X				EBS 3407
	Polygala longicaulis Kunth	Herb	Th	-	BR	X				EBS 5049
	Polygala trichosperma Jacq.	Herb	Th	-	-		X		X	EBS 4115, 5167
Rhamnaceae	Gouania colurnifolia Reissek	Climber	Ph	-	-		X			EBS 5350
Rubiaceae	Borreria latifolia (Aubl.) K.Schum.	Herb	Th	-	-		X			EBS 4153
	Borreria scabiosoides Cham. & Schltdl.	Herb	He	-	-	X				EBS 5343
	Borreria spinosa Cham. et Schltdl.	Herb	He	vassourinha-de-botão	-	X		X		EBS -, 3503
	Borreria verticillata (L.) G. Mey.	Subshrub	He	falsa-poaia	-	X			X	EBS 4479, 4724
	Borreria tenella (Kunth) Cham. & Schltdl.	Herb	Th	-	-		X	X		EBS 4150, 3612
	Borreria sp.nov.	Subshurb	He	-	-	X				EBS 5341
	Cordiera myrciifolia (K. Schum.) C. Press. & Deplrete	Shrub	Ph	-	-				X	EBS 3737
	Cordiera rigida (K. Schum.) Kuntze	Shrub	Ph	-	BR				X	EBS 3733
	Guettarda viburnoides Cham. & Schlltdl.	Shrub	Ph	angislica	-			X	X	EBS 5783, 5161
	Hexasepalum apiculatum (Willd.) Delprete & J.H. Kirkbr.	Herb	Th	-	-	X		X		EBS 3478, 3614
	Hexasepalum gardneri (K. Schum.) J.H. Kirkbr.	Subshrub	Th	-	NE		X	X	X	EBS 4119, 3619, 4720
	Hexasepalum teres (Walter) J.H. Kikbr.	Herb	Th	-	-		X			EBS 4143
	Mitracarpus fernandesii E.L. Cabral, Sobrado & E.B. Souza	Herb	Th	-	NE	X	X	X		EBS 5323, 5356, 3646
	Oldenlandia filicaulis K.Schum.	Herb	Th	-	-		X			EBS 5351
	Richardia grandiflora (Cham & Schltdl.) Steud	Herb	Th	-	-		X			MCPT 14
	Richardia scabra L.	Herb	Th	-	-			X		EBS 3630
	Rosenbergiodendron longiflorum (Ruiz & Pav.) Fagerl.	Shrub	Ch	estrela-do-norte	-	X				EBS 5332
	Staelia virgata (Link ex. Roem. & Schult.) K.Schum.	Herb	Th	-	-	X	X	X		EBS 3598, 4116, 3623
	Tocoyena sellowiana (Cham. & Schltdl.) K.Schum.	Shrub	Th	jeniparana	BR		X		X	EBS 4468. 4719
Santalaceae	Phoradendron sp.	Herb	Th	erva-de-passarinho				X		EBS 3752
Simaroubaceae	Homalolepis cedron (Planch.) Devecchi & Pirani	Shrub	Ph	-	-			X		EBS 5789
	Simarouba versicolor A. St.-Hil.	Tree	Ph	mata-cachorro	-				X	EBS 5816
Solanaceae	Brunfelsia uniflora (Pohl.) D.Don.	Shrub	Ch	manacá-de-jardim	-			X		EBS 5056
	Schwenckia americana Rooyen ex L.	Herb	Th	-	-		X			EBS 5731
	Solanum crinitum L.	Shrub	Ph	-	-		X			EBS 5740
	Solanum paniculatum L.	Shrub	Ph	jurubeba	-		X			EBS 5734
Turneraceae	Turnera coerulea DC.	Herb	Th	-	-	X	X			EBS 5231, 4455
	Piriqueta sp.	Herb	Th	-		X				EBS 5235
Urticaceae	Cecropia concolor Willd.	Tree	Ph	embaúba	BR		X			EBS 5738
Verbenaceae	Lantana camara L.	Shrub	Ph	camará-chumbinho	-	X				EBS 4925
	Stachytarpheta cayennensis (Riech.) Vahl.	Herb	He	gervão-azul	-	X				EBS 3456
	Stachytarpheta coccinea Schauer	Herb	He	-	BR	X				EBS 3482
Violaceae	Hybanthus albus (A. St.-Hill) Baill	Herb	Th	-	BR	X				EBS 3410
	Pombalia calceolaria (L.) Paula-Souza	Herb	Th	ipeca-da-praia	-				X	EBS 5161
Vochysiaceae	Callisthene minor Mart.	Tree	Ph	pau-de-pilão	BR		X		X	EBS 5738, 5822
	Qualea grandiflora Mart.	Tree	Ph	pau-terra-de-folha-larga			X	X		EBS 5723, 5778
	Qualea parviflora Mart.	Tree	Ph	pau-terra	-	X	X	X	X	EBS 5417, 5438, 3751, 3738
	Salvertia convallariodora A.St.-Hill.	Tree	Ph	pau-de-colher	-	X			X	EBS 5415, 3746
Xyridaceae	Xyris cf. paradisiaca Wand	Herb	Cr	-	BR		X			EBS 5353

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.

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Publication Dates

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

History

• Received
  03 June 2020
• Accepted
  16 Nov 2020