Seasonal Semideciduous Forest and Cerrado Floristic composition of fragments in Serra das Flores, Ibiapaba Plateau, Ceará, Brazil

Abstract The state of Ceará is located in the Northeast region of Brazil, which has a varied climatic condition, being predominantly formed by Caatinga vegetation, and there may also be remnants of Cerrado and other Semideciduous Seasonal Forest. The objective of this work was to carry out a floristic survey in vegetation fragments of Semideciduous Seasonal Forest and Cerrado found in the part of Serra das Flores located in the municipality of Viçosa do Ceará. Para tal, foram realizadas 12 coletas na área ao longo do ano de 2019. 220 species were recorded, belonging to 154 genera and 62 families. The most representative families in this area were Fabaceae (38 spp.), Rubiaceae (15 spp.) and Myrtaceae (nine spp.). The predominant habit were herbs and shrubs. The richest fragment was the Cerrado with 171 species, with the Typical Cerrado (104 spp.) phytophysiognomy being the most representative. Of the total species, most are native, 16 are new records for Ceará, 12 are endemic to the Caatinga domain and seven are endemic to the Cerrado. Thus, the present site presents a high heterogeneity of species, in addition to varied habits, new records and endemic species of Cerrado and Caatinga.


Introduction
The state of Ceará presents a great diversity of environmental and geomorphologic conditions.Five relief units are found: Coastal Region/Coastal features, River Plains, Inland Plains, Sertaneja Depression, and Residual massifs, among them there are different soil types, reliefs, and climatic factors, which allow the manifestation of various vegetational types, with several remnants of Brazilian domains (Castro et al. 2012;Moro et al. 2015), for example, the Atlantic forest and the Cerrado.
Caatinga is a phytogeographic domain that presents an area comprising about 912,000 km 2 , with an average annual rainfall that can reach 1,000 mm (Fernandes & Queiroz 2018) and has temperatures ranging from 25 to 30ºC (Tabarelli et al. 2018), which is considered exclusively Brazilian, occurring only in the Northeast and Southeast regions of the country (Ramos et al. 2020).The vegetation presents adaptations so it can survive in this predominant climate, the semiarid, as small leaves and sometimes transformed into thorns, presence of thick cuticle and succulent stems.Many species in the dry season shed their leaves to reduce transpiration (Melo & Carneiro 2021).The Caatinga vegetation is quite varied and heterogeneous, thus having several classifications (Silva & Cruz 2018).According to Fernandes et al. (2019), the Caatinga has more than 3,347 plant species, of which 526 are endemic.
The Cerrado is considered the second largest phytogeographic domain in Brazil, occupying an area of approximately 2,036,448 km 2 , about 23% of the national territory, found mainly in the Midwest region of the country, thus forming the Brazilian Central Plateau, and there also may have patches of this domain elsewhere in the country (Brazil 2019;Casella & Silva Junior 2013;Finger & Finger 2015).It is characterized by a mosaic of 11 physiognomies, such as Cerrado formations (Cerrado sensu stricto), grassland (Campo Limpo), shrubby grasslands (Campo Sujo), Cerrado Woodlands (Cerradão), ranging from herbaceous to arboreal species, with water availability, edaphic and geomorphological characteristics, nutrient availability, and incidence of fire (Silva et al. 2015b;Buttler et al. 2012;Pizoletto et al. 2018), which are the main factors responsible for the characterization of the countryside, forest, and Cerrado phytophysiognomies (Ribeiro & Walter 2008;Couto Júnior et al. 2011).In the Northeast region, Cerrado is considered marginal, being found on the edges and in ecotonal areas with other ecosystems (Souza et al. 2010), and species from Caatinga and Amazonia may also occur.The states of the Northeast region in which Cerrado occurs are: Bahia, Maranhão and Piauí (IBGE 2021).
According to Moro et al. (2015) Cerrado areas are found in the state of Ceará in the coastal tablelands, thus characterizing the Coastal Cerrados, and in the Inland Chapadas (Serra da Ibiapaba and Chapada do Araripe) that surround the Sertaneja Depression, qualifying the Inland Cerrados.The National Forest Inventory has great importance in cataloging information on forest resources in Brazil and when the study in the territory of Ceará was carried out, about 0.4% of Cerrado vegetation phytophysiognomy was found, with some endemic species of Cerrado, such as Fraunhofera multiflora Mart.(Celastraceae), Faramea nigrescens Mart.(Rubiaceae) and Heteropterys pteropetala A.Juss.(Malpighiaceae) (Brasil 2016).
The Caatinga phytogeographic domain can be found in the interior plateaus, characterizing the sedimentary Caatinga, and in the Depression Sertaneja, characterizing the Cristalino Caatinga (Moro et al. 2015).In Ceará we can also find fragments of Semideciduous Seasonal Forest, which can also be called Subcaducifolia Tropical Forest, being found mainly around the Humid Forests in the interior of the state (Figueiredo 1997;IBGE 2012).
The Cerrado areas in Ceará are found in areas with a sub-humid climate or on the Ibiapaba Plateau, and may also occur in a semi-arid climate, the most unique being those located in Lavras da Mangabeira, Várzea Alegre, Farias Brito, Granjeiro, Caririaçu and Aurora municipalities, and in the Serra das Flores locality (Figueiredo 1989).The Cerrado of this area are under pediplain surfaces with dense or open formations (Jordy Filho & Salgado 1981).
Thus, it is necessary to carry out more floristic studies in these remnants to better understand their floristic diversity, as well as the distribution of species and phytophysiognomies in the state.Therefore, the objective of this research was to carry out a floristic survey in vegetational fragments of Semideciduous Seasonal Forest and Cerrado found in the part of Serra das Flores located in the municipality of Viçosa do Ceará, a well-preserved area in the micro region of Ibiapaba.

Study area
The study area is located in Serra das Flores, which extends over Viçosa do Ceará and Granja municipalities; however, the research was conducted only in Viçosa do Ceará municipality, microregion of Ibiapaba, mesoregion of Northwest Ceará (Fig. 1).The Ibiapaba Plateau is part of the Sedimentary Sierras, located in the western part of Ceará (Fernandes 1990).These areas present ecotones among Cerrado, Caatinga and Semideciduous Seasonal Forest (Jordy Filho & Salgado 1981).
Viçosa do Ceará has a Warm Tropical Semiarid and Warm Tropical Subhumid climate, with an average temperature ranging from 22 to 24 ºC, and rainfall of 1,349 mm.It has reliefs formed by the Ibiapaba Plateau and Sertanejo depressions, thus having vegetation such as Carrasco, Thorny Caducifolia Forest, Subcaducifolia Tropical Rain Forest, and Subperenifolia Tropical Pluvio-Nebular Forest, in addition to soils such as Quartzaceous Distrophic Sands, Litholics, Red-Yellow Latosol, Solodic Planosol and Red-Yellow Podzolic (IPECE 2018).
The Serra das Flores plateau (03º23'05.1"S,41º09'33.4"W) is characterized by a Cerrado formation of Typical Cerrado (Cerrado Típico) phytophysiognomy, with a predominantly shrubby vegetation, with 20 to 50% tree cover, average height of 3-6 m, and presents a Quartz Sand soil, with altitudes higher than 600 m.The Sparse Cerrado (Cerrado Ralo) (03º23'43.6"S,41º09'24.8"W)occurs at altitudes of 401 to 600 m, with a predominantly shrub-herbaceous vegetation, with 5 to 20% tree cover, average height 2-3 m, and presents litholic soils with the absence of rock Rodriguésia 74: e00922022.2023 outcroppings.At altitudes that vary between 301-400 m, occurs the Rupestrian Cerrado (Cerrado Rupestre) phytophysiognomy (03º24'04.3"S,41º09'25.9"W),with a predominantly shrubherbaceous vegetation, with 5 to 20% tree coverage, average height of 2-4 m, and presents litholic soils, where the vegetation settles between the cracks in the rocks, mainly due to the presence of rocky outcrops.Therefore, such phytophysiognomies characterize the Cerrado formations (Ribeiro & Walter 1998).Serra das Flores is also home to the Semideciduous Seasonal Forest (Mata Seca), which has a seasonal climate that promotes the fall of part of the leaves during the dry season, and is located at altitudes ranging from 100-300 m (Fig. 2).
Twelve sampling collections were carried out in the area throughout 2019.The walking collection method was used with random walks (Filgueiras et al. 1994), along the study area, from the base of the mountain range to the plateau, collecting all fertile species (flower and/or fruit) of angiosperms.Specimens were collected and stored in plastic bags during field collection and herborized according to Mori et al. (1985) and Gadelha-Neto et al. (2013).The exsiccata were deposited in the Prof. Dias da Rocha Herbarium of the Natural History Museum of Ceará (MHNCE-HER) of the State University of Ceará.Photographic records were also made to assist in the subsequent identification of specimens in the herbarium.The collected plants were classified into the types of phytophysiognomy where they occur.For the identification and characterization of the phytophysiognomies the key to identify the Cerrado phytophysiognomies from the study by Ribeiro & Walter (1998) was used, as well as the use of altimetric variation.
Identification keys, specialized bibliographies, and expert consultations were used to identify the specimens.The classification system adopted followed the Angiosperm Phylogeny Group IV (APG IV 2016), except for Turneraceae, considered independent from Passifloraceae.
To verify endemism and new records for the state of Ceará, the 2020 database of the Flora of Brazil List of Species (Flora of Brazil 2020, continuously updated) was used.Authors' names are according to IPNI (2021).To assess the conservation status of the species, the criteria of the International Union for Conservation of Nature (IUCN 2020) and CNCFlora (2018) were used.To complete the species listing, the Flora of Brazil 2020 (continuously updated) and CRIA (2021) sites were used.
In the study carried out by Ribeiro-Silva et al. (2012) with the phytophysiognomies found in the Araripe-Apodi National Forest (Flona), they verified that Fabaceae, Rubiaceae, Asteraceae, Bignoniaceae, Myrtaceae, Euphorbiaceae, Apocynaceae, Malpighiaceae, Annonaceae and Solanaceae, were the most representative families in the Araripe-Apodi Flona.According to Moro et al. (2015), the Chapada do Araripe and Serra da Ibiapaba have wet sedimentary forest, dry sedimentary forest, Cerrado and Cerrado Woodlands Interior vegetation types.Nepomuceno et al. (2021) when conducting floristic surveys in four Cerrado areas in Ceará, found that Fabaceae (49 spp.) and Rubiaceae (19 spp.) were also the families with the greatest richness.In a fragment located in southern Ceará, he also found the Fabaceae family to be the most diverse (Figueiredo & Fernandes 1987).
For Ribeiro-Silva et al. (2012) in a fragment of the Araripe Forest in Ceará state, composed of Carrasco, Cerrado Woodlands, Cerrado formations and Semideciduous Seasonal Forest, the richest genera were Borreria, Byrsonima, Casearia, Erythroxylum, Myrcia and Psychotria, with three species each, Senna with four and Solanum with five species.In the survey by Nepomuceno et al. (2021), Ipomoea and Mimosa were the genera with the highest richness in Cerrado-Caatinga areas in Ceará state.In the Araripe National Forest fragment, the genera Psidium (four spp.), Byrsonima and Solanum (three spp.each), were the richest (Costa et al. 2004).
In a Cerrado Woodlands phytophysiognomy, the most representative genera were Myrcia (six spp.), Banisteriopsis C.B.Rob.ex Small and Senna, with three species each (Silva et al. 2015a).José Neto (2018), when carrying out the study in the Pombo Municipal Natural Park in the Três Lagoas municipality, Mato Grosso do Sul state, an area with Typical Cerrado vegetation, the most representative genera were, Byrsonima, Eugenia and Miconia, each with seven species, besides Annona, Mimosa and Solanum, with five species each.
Regarding habits, herbs (35%), shrubs (25%) and trees (15.9%) were the most representative (Tab.S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.23907633.v1>).In an urban Cerrado fragment, located in Fortaleza municipality, herbs (38%) and shrubs (35%) were the most representative (Moro et al. 2011).Nepomuceno et al. (2021) when analyzing four areas of Cerrado fragments in the state of Ceará, in Granja and Martinópole municipalities, observed that the herbaceous component (113 spp.) and the subshrub (27 spp.) were the most representative, totaling more than 50% of the species inventoried.Araújo et al. (2020) when carrying out a survey in the Botanical Garden of São Gonçalo do Amarante in the state of Ceará, an area of Caatinga and Cerrado, the herbaceous layer was the most representative (53 spp.), followed by the tree (35 spp.) and shrub (34 spp.).In the Chapada das Mesas National Park, Maranhão, it was found that the trees (50.8%) and herbs (28.9%) presented the highest values.In a fragment of ecotonal Cerrado in Buriti dos Lopes-PI, it was found that the herbs and trees showed the highest richness (Silva et al. 2020).
Regarding the number of species and the diversity of habits found in each of the phytophysiognomic forms, the one that stood out the most was the Typical Cerrado, with 104 spp.(47.2%), followed by Semideciduous Seasonal Forest with 49 spp.(27.2%), and Rupestrian Cerrado with 37 spp.(16.8%) (Figs.4-5).
In the study by Saraiva et al. (2020), in a Cerrado area in Maranhão state, of the 242 vascular plant species listed, Typical Cerrado (113 spp.), Cerrado Woodlands (65 spp.) and Rupestrian Cerrado (63 spp.) were the phytophysiognomies that presented the highest numbers of species, resembling the results in this study.
In the Rupestrian Cerrado phytophysiognomy of Serra das Flores, the most representative families were Fabaceae with 11 spp., Poaceae with four species, and Lamiaceae and Maranthaceae with three spp.each.The richest habits were herbs (14 spp.) shrubs and subshrubs (nine spp.each), as can be seen in Fig. 4. The Sparse Cerrado is one of the three forms of Cerrado formations, and is the lowest form of this phytogeographic domain, thus presenting the lowest number of species among the physiognomic forms (Ribeiro & Walter 2008;IBGE 2004).In this study, the Sparse Cerrado presented low species richness, with only 30 species, of which 14 are herbs, eight are shrubs, three trees, four climbers and one subshrub (Fig. 4).Fabaceae and Ochnaceae were the richest families in this phytophysiognomy with three species each and Orchidaceae with four (Tab.S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.23907633.v1>).In the study carried out by Rodrigues & Conceição (2014) in Mirador State Park, Maranhão, in a Sparse Cerrado physiognomy, it also showed low richness, with only 13 species of the 140 listed, with the shrub form being the most predominant.The authors state that the arboreal habit presented low stature with sparse individuals.According to Ribeiro & Walter (2008) the most predominant habits in this physiognomy are herbs and shrubs.
The Typical Cerrado is an intermediate phytophysiognomy between the Dense Cerrado and the Sparse Cerrado, with low tree density, making the other strata richer in number of species (IBGE 2004).The Typical Cerrado in this study showed the highest species richness and strata richness, with 47.27% (104 spp.) of the species (Fig. 5).The herbaceous habit was similar to that which occurred in the Semideciduous Seasonal Forest phytophysiognomy, with a difference of three fewer species.The arboreal habit showed the highest value of all the phytophysiognomic forms, with 80% of the arboreal species.The other habits were also the most prominent.In this phytophysiognomy the climbers showed the greatest richness, with 11 species (Fig. 4).
The richest families in the Typical Cerrado phytophysiognomy were Fabaceae with 17 species, Rubiaceae, Myrtaceae with 7 species  each, and Malpighiaceae with 5. Most species of the Malpighiaceae family were collected in this phytophysiognomy, five from the genus Byrsonima and one from the genus Stigmaphyllon (Tab.S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.23907633.v1>).This is similar to that observed by Rodrigues & Conceição (2014) in which all species of the Malpighiaceae family were collected in this phytophysiognomy, as well as the species of the genus Byrsonima that presented 12 species.It also presented Typical Cerrado species, such as Hancornia speciosa Gomes, Himatanthus drasticus (Mart.)Plumel, Curatella americana L and Agonandra brasiliensis Miers ex Benth.& Hook.f.The latter species has also been found in five Typical Cerrado areas in Ceará state (Figueiredo 1989).Curatella americana, Krameria tomentosa A. St. Hil and Ouratea fieldingiana Engl are considered Cerrado species (Jordy Filho & Salgado 1981).According to Ratter et al. (2003) and Ratter & Dargie (1992) the Salvertia convallariodora, Byrsonima crassifólia, Curatella americana species are widespread in Cerrado areas in Brazil.
In the floristic and phytosociological study conducted by Ribeiro et al. (2008) in a Cerrado formations phytophysiognomy, in the Nova Xavantina municipality, Mato Grosso, of 240 individuals, 42 species are from the Typical Cerrado, thus corroborating its richness.In the study carried out by José Neto et al. (2015) in a fragment of Typical Cerrado in the same state, 78% of the species surveyed were herbs and shrubs, with Annonaceae, Asteraceae, Bignoniaceae, Euphorbiaceae, Fabaceae and Malvaceae, Myrtaceae and Poaceae being the richest families in the study area.This low representation of tree species, since this physiognomy is of a forest nature, may be related to the location of this remnant, which is in an urban area.
In New occurrences are quite common in floristic surveys, mainly due to the scarcity of studies in little known areas, thus showing the importance of these studies, which can provide subsidies for future conservation research.
According to Meyer & Schwirkowski (2019), state species listings are constantly changing due to new findings, thus being considered an ongoing process.Saraiva et al. (2020)    Because the state of Ceará is included within the Caatinga domain, many of the species end up invading the remnants, hence their occurrence.According to Nepomuceno et al. (2021), Some areas of Ceará's Cerrado are floristically more like Caatinga vegetation than the Cerrado one, due to the occurrence of a larger number of species of this domain, some of which are exclusive.
Praxelis diffusa, Staurochlamys burchellii, Rourea induta Planch., Harpalyce brasiliana Benth., Byrsonima stannardii, Ouratea hexasperma (A.St.-Hil.)Baill., Trichocentrum cepula are endemic to Cerrado (Fig. 8).The other species may occur in more than one of these domains and in various vegetational types.Almost all of the species collected in Serra das Flores are native to Brazil (97.7%), with the exception of Emilia sonchifolia (L.) DC. which is considered naturalized (BFG 2018).This shows the importance of the conservation of this area, due to the presence of native and endemic species of the remnants of these Brazilian domains, including the presence of the new records.
The Cerrado has been greatly degraded in recent years, mainly by the strong expansion of the agricultural frontier and by anthropic actions, such as the replacement of native forest for pasture production, besides the fires.The knowledge of its biodiversity, especially its flora, brings several benefits for the understanding of its plant community as a whole, mainly concerning conservation and management (Andrella & José Neto 2017).
Regarding the conservation status of species, nine (4.5%) are classified in the category of Least Concern (LC), while the others have not been evaluated (NE) up to date (Tab.S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.23907633.v1>).According to Pinheiro et al. (2020), the species conservation data show the importance of floristic surveys in forest remnants, since from them it is possible to classify the taxon, and thus identify vulnerable species.From the knowledge of a particular location flora, especially in little known areas or areas that have suffered from anthropic actions, these data help in the creation of conservation programs for certain species, especially endemic species or even the creation of conservation units.
Serra das Flores is an area of high species diversity, with the herbaceous and shrubby habit being the most predominant, where almost all of them are native to Brazil.It presented species endemic to the Cerrado and Caatinga domains and 16 new occurrences for the state of Ceará, thus increasing the list of species in the state.This also proves the high diversity of environmental conditions that Ceará presents.
The Semideciduous Seasonal Forest phytophysiognomy showed similarity in the number of species when compared to the Typical Cerrado.It was possible to detect floristic differences between the studied phytophysiognomies, mainly marked by environmental and altimetric factors, as well as species richness, families and habits.
Therefore, more sample collections in little known areas such as the Serra das Flores are necessary to better understand the distribution of vegetational types and species of Cerrado and Semideciduous Seasonal Forest flora in the state of Ceará, helping to update the taxons and the distribution of vegetation for the state, helping to maintain the harmony of these ecosystems, avoiding future environmental damage.

Figure 2
Figure 2 -a-h.Phytophysiognomies of Serra das Flores, Viçosa do Ceará-CE -a.Semideciduous Seasonal Forest in the rainy season; b.Semideciduous Seasonal Forest in the dry season; c.Rupestrian Cerrado in the rainy season; d.Rupestrian Cerrado in the dry season; e. Sparse Cerrado in the wet season; f.Sparse Cerrado in the dry season; g.Typical Cerrado in the rainy season; h.Typical Cerrado in the dry season.

Figure 3 -
Figure 3 -Number of species of the most representative botanical families of Serra das Flores, Viçosa do Ceará-CE.

Figure 5 -
Figure 5 -Distribution of the number of species by phytophysiognomy occurring in Serra das Flores, Viçosa do Ceará-CE.
Calliandra surinamensis Benth.(Fig.6d)only occurred in the Amazon region, thus being the first record for the Northeastern region, for a Cerrado area, in the Rupestrian Cerrado phytophysiognomy, where there are rocky outcrops.The other new occurrences already happened in other states of the Northeast region, thus being only new records for Ceará.