Floristic and dispersion syndromes of Cerrado species in the Chapada do Araripe , Northeast of Brazil

Through this study, the objective was to contribute to the knowledge regarding floristic composition, classification and conservation status of the studied plant species as well as the dispersion syndromes of flora found in a disjoint Cerrado area in the Chapada do Araripe, Crato-CE. For the research development Rapid Survey method, applied in three walking lines (Line 1, Line 2 and Line 3) was adopted. Floriferous branches, fruits and seeds from species in the study area were collected in order to identify them and to characterize their diaspores, in view of fitting them into the corresponding dispersion syndromes. A total of 103 species were identified, the richest species taxa were: Fabaceae, Apocynaceae, Euphorbiaceae, Research, Society and Development, v. 9, n. 9, e864997934, 2020 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v9i9.7943 3 Malpighiaceae and Myrtaceae. The most abundant species in the studied area were: Cordiera myrciifolia (“bola”) Miconia albicans (“Candeiro-de-pelo”), Caryocar coriaceum (pequi) and Copaifera langsdorffii (“pau d'oleo”). Three new occurrences were also recorded for the state of Ceará: Eriope tumidicaulis, Myrciaria cf. tenella and Stachytapheta cf. crassifolia. The most frequent dispersion syndrome was zoochoria, followed by anemocoria. Considering that most of the species occurring in the study area have their dispersion diaspores transported by a fauna element, the importance of these species for the maintenance of the observed floristic richness is evident.


Introduction
The Cerrado (brazilian savannah) is considered the most diversified tropical savanna in the world regarding phytophysiognomies, possessing high biodiversity (Klink & Machado 2005;Lefebvre & Nascimento 2016) with vegetation that covers a true mosaic of environments sheltering diverse ecosystems, ranging from open formations, subdivided between rural and savanna formations, to forest physiognomies (Ribeiro & Walter 2008). It is, therefore, one of the global biodiversity hotspots due to its high degree of endemism (Myers et al. 2000;Ponciano 2015). According to Oliveira et al. (2014), this vegetation formation has phytophysiognomies delimited by the existence of an abundant partial or continuous herbaceous strip and a rich diversity of woody species. Development, v. 9, n. 9, e864997934, 2020 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v9i9.7943 5 In the Brazilian Northeast, the existence of Cerrado patches is attributed, mainly, to altitude, forming fragments resulting from the association with edaphic factors (Santos et al. 2014). In this region is the Chapada do Araripe which houses the Araripe National Forest -Apodi -FLONA Araripe, the first Brazilian National Forest, (Alves et al. 2011). The Cerrado present in this plateau occurs in the form of vegetative enclaves (Costa et al. 2004, Costa & Araújo 2007. Unfortunately, in recent years, due to the vast quantity of resources that it harbors, the Chapada do Araripe has been experiencing many forms of illegal exploitation, especially flora exploitation. Exploratory activities which have gathered attention for desolation, especially in Cerrado areas, are agricultural expansions, raising livestock and wood removal for industrial use (Andrade 2007), of which the latter, according to Barros et al. (2010), are usually extracted without management which according to Oliveira et al. 2014 can contribute to local extinction of fruit and seed dispersers affecting the interaction between species and successional dynamics, which may prevent or hinder the maintenance of certain species.
One of the main challenges for the conservation of the Cerrado is to demonstrate the importance that biodiversity plays in the functioning of ecosystems (Klink & Machado 2005).
With this, the development of studies that lead to greater knowledge regarding flora and fauna and the interspecific relations that unites them is becoming more and more urgent and necessary, especially in Cerrado environments, since studies in this area are still scarce. It is hoped that research may lead to a better understanding of existing plant species' distribution in the Cerrado in the Chapada do Araripe.
In order to fill some of this knowledge gap, this study aimed to determine the floristic composition, conservation state of the studied plant species and the dispersion syndromes of species occurring in a disjoint Cerrado area of the Chapada do Araripe, Crato-CE, Northeast of Brazil, contributing to the understanding of the ecological processes that work in this vegetative formation.

Study area
The Chapada do Araripe is a plateau located within the Caatinga (Seasonally Dry Tropical Forest) domain in the Brazilian Northeast, more precisely between the states of Ceará, Pernambuco and Piauí, and covers 38 municipalities, 15 in Ceará, 12 in Pernambuco and 11 in Piauí (Siebra et al. 2011;Novaes & Laurindo 2014). According to Loiola et al. 2015 the Cerrado occurs in the eastern area of the top of the plateau, being recognized as a semi-deciduous Savannah vegetation, with soils classified as aluminized leachate. It has a BSw'h' type climate, characteristic of a Hot and semi-arid climate (köeppen 1948) with annual average precipitation around 760 mm and average annual temperature of 24.1ºC (Costa et al., 2004).

Transect allocation, collection and identification of botanical material
For the species listing, the Rapid Survey (RS) method developed by Ratter et al. 2001 and improved by Walter and Guarino 2006 with a quantitative-qualitative approach was used.
The RS was applied in three walking lines, called "Line 1" (L1), "Line 2" (L2) and "Line 3" (L3) where new species were recorded at each five minutes interval. This process continued until no new species were found, with the aim of detailing a construction data of the species × time curve. The three walking lines were distanced roughly 400 m from each other. The field of vision for each side of the walking line was arbitrated as up to 5 m, allowing better species visualization. Since L1 and L2 were separated by the BR-122 (a motorway), 100 m either side of the border were taken into account of the inside fragment in Development, v. 9, n. 9, e864997934, 2020 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v9i9.7943 7 order to minimize its possible impacts (Figure 1). Whilst RS is a method of immediate data collection, bi-monthly and/or monthly visits to the field were necessary since it was not possible to allocate all transects in a single day and not all plant species were in the reproductive period at the same time (Schierolz 1991, Alves-junior et al. 2006. The collected plant species were herborized following procedures described by (Mori et al. 1989) and later identified by comparison with previously identified specimens, specialized bibliography and submission to specialists. Families were identified according to  Research, Society and Development, v. 9, n. 9, e864997934, 2020 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v9i9.7943 8 All collected species were incorporated into the collection at the Caririense Dárdano de Andrade-Lima Herbarium (HCDAL) of the Regional University of Cariri (URCA).

Classification and conservation status of the studied plant species
Classification of species' conservation status followed recommendations of the Brazilian Institute of Geography and Statistics (2012) and the criteria adopted by Morellato & Leitão-Filho 1992, with adaptations, where species found along the walking lines were categorized into: Rare (species rarely found on walking lines, restricted to a single line) (<5 individuals); Occasional (species sporadically found on walking lines) (>5 up to 20 individuals); Frequent (species often found on two or all walking lines) (>20 up to 100 individuals); and Abundant (predominant species in all walking lines) (>100 individuals).
To verify the conservation status of the species, two databases were consulted: the IUCN Red List of Threatened Species (2017) and the List of Species from the Brazil Flora 2020 (2018).

Fruit collection and characterization of dispersion syndromes
Five to ten fruits from each species were collected (immature and mature). These were analyzed morphologically and structurally, according to the methodology proposed by Domingues et al. (2013). The fruits were previously classified according to their characteristics in the categories: Artrocarpic; Follicular; Nucoid; Samaroid; Bacoid; Drupoid; Schizocarpic and Capsular, followed by their subtypes, as recommended by Barroso et al. (1999).
Diaspora dispersal syndromes were classified, taking into account the morphological analysis of fruits and seeds, specialized literature and direct observation in the field, and were grouped according to Pilj (1972) in the following categories: I -Anemocoria: when the diaspores present morphological adaptations for wind dispersal, such as wings, feathers or winged appendages; II-Zoocoria: when the diaspores present attractive structure and/or food source, allowing their dispersion by animals; III -Autocoria, when the diaspores did not fit into the anemocoria or zoocoria categories, spreading through diaspores with explosive dehiscence (ballistic) or by the action of gravity (barocoria). Research, Society and Development, v. 9, n. 9, e864997934, 2020 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v9i9.7943 9

Statistical analysis
Statistical analysis of the data and graphical representation of the results were performed using the Paleontology Analysis Statistic 2.0 (PAST 2.0) and Microsoft Excel 2010 software.
Among the families with the greatest representativiness, Fabaceae has been evidenced as one of the species with the highest number of species in the area, as shown by other studies carried out (Costa et al. 2004;Souza et al. 2007;Loiola et al. 2015;Silva et al. 2015).
Many of these species also presented a wide distribution in Central Plateau Cerrado areas, such as R. montana (Reis et al. 2012;Ferreira et al. 2017); A. occidentale and C.
langsdorffii (Ferreira et al. 2017); C. brasiliense and M. albicans (Torres et al. 2017); A. coriacea and H. speciosa (Bordino et al. 2018); P. reticulata (Reis et al. 2012); B. virgilioides (Medeiros et al. 2007); L. pacari and M. guianensis (Lima et al. 2015). According to Ferreira et al. (2017), species with a wide distribution can be used in recovery plans in regions with similar characteristics.  (Table 2). Pielou's equability obtained a value of 0.87, showing that species are relatively well distributed in the studied area. According to Rocha, Netto & Lozi (2005) the great species diversity found in the Cerrado is associated with a vast heterogeneity, since it includes several types of plant formations.       number of meters traveled per time interval was observed, this difference being possibly due to a narrowing of the trail, making it difficult to see and differentiate the species in the area. In L3, a gradual increase in the number of species was observed between the 1 -5 min interval up to the 3 -5 min interval, where in total 70 species were found in 40 min and 1030 m (Table   3). The sum of the three walking lines (L1+L2+L3) ( Table 3) indicates the plant community is rather uniform in floristic composition. The species/time curve indicates sample adequacy since stability was achieved for all walking lines. The significance of the sampling is paramount for the real knowledge regarding plant richness of the studied area (Amaral et al. 2000). The species distribution by area was similar to Cerrado areas from the Federal District sampled by the same method (Walter & Guarino 2006). TI  L1  L2  L3  L1 + L2 + L3  (min)  MT  NNS  MT  NNS  MT  NNS  AMT  NSA  5  68  39  28  13  66  33  54  60  10  61  12  30  9  78  20  56  19  15  64  11  31  7  97  9  64  5  20  89  5  25  8  149  3  88  4  25  100  2  24  7  143  3  89  4  30  102  2  31  5  164  1  99  4  35 118 1   were observed for the state of Ceará (Table 4).

Species conservation status
With regards to the species abundance classification in the conservation status for the studied areas, 41.75% of the species were classified as frequent, 32.04% as occasional, Pirita sidifolia with only two individuals, were found. According to Aquino & Miranda (2008); Sano et al. (2014) and Macêdo (2015), while several factors exist to consider a species as rare, in conservation biology the most commonly used criteria are associated with a low frequency and distribution of these in their area of occurrence.
Determinants for the conservation of rare species are the same which justify those for other species, however, the extinction of these species may possibly represent an ecological imbalance in the ecosystem, which would be associated with both the factors related to its evolutionary process and the perspective of representing a potential source for the discovery of medicinal drugs or even constitute a food source for future generations (Oliveira et al. 2018).
Among the abundant, frequent and occasional species a greater predominance of species with zoocoric dispersion syndrome was observed, these being 11.65%, 24.27% and 15.53%, respectively. For the other conservation statuses, 2.91% of abundant species were found to have an autocratic/zoocoric dispersion and 0.97% anemocoric; 8.84% of species classified as frequent were found to be anemocoric, 6.80% autocratic and 1.94% autocratic/zoocoric; meanwhile 8.74% of species classified as occasional were anemocoric and 7.77% were autocratic. For the rare species, 3.88% presented a zoocoric dispersion, with the same percentage being observed for autocratic species, moreover it is worth mentioning that only 2.91% were classified as anemocoric. The large number of rare and occasional species with zoocoric dispersion, demonstrates the increasingly urgent need for local fauna preservation, since the elimination of frugivorous animals from the environment tends to compromise the reproduction and dynamics of several species (Almeida et al. 2008;Stefanello et al. 2010).
In the studied area, Bowdichia virgilioides and Smilax japicanga are classified as endangered while Caryocar coriaceum has an endangered status, which corroborates with data from IUCN (2017) and Flora do Brasil 2020 (2018). These species were classified in the studied area as frequent, occasional and abundant, respectively. It is believed the progressive disappearance of these species in nature can be attributed not only to their own evolutionary processes, but to anthropic factors since they have food value, medicinal properties, ornamental and timber potential, which have been affected by predatory extractivism, without the competent bodies having a future concern for their preservation (Ribeiro & Rodrigues 2006). In addition, Machado et al. (2004); Klink & Machado (2005) point out that other factors such as loss of habitat and poor soil management are preponderant for the extinction of plant species in the Cerrado.  (2004) and Silva et al. (2015) exists in studies carried out in Cerrado areas in the Chapada do Araripe in the municipalities of Barbalha and Nova Olinda, which, despite having a relative proximity to the site of this study, registered zoocoria followed by autocoria and anemocoria as the prevailing dispersion methods.

Dispersion syndromes and fruit characterization
The dispersal of diaspores by animals is of great adaptive advantage for several plant species since this relation allows them to be carried away from the mother plant, and the animals can deposit them in favorable places for their germination (leal 2003). Dispersal by anemocoria is restricted to a few families, which confirms the advanced succession stage of the studied areas, since according to Liebsch &Acra (2007) this syndrome is associated with open areas with a predominance for pioneer species, as this structure favors the passage of the wind and consequent diaspore dispersion. Although the proportion of autocoric species has been shown to be low for the study, it has been characterized as one of the largest ever found in Cerrado areas, which may be related to a local pattern.
The zoocoria was predominant for the arboreal (32.35%), shrub (10.78%), subarbustive (6.96%) and hemiparasite (1.9%) components, however in the climbing and herbaceous components autocoria (10.78%) and anemocoria ( Araripe by Costa et al. (2004). Harms et al. (2000) and Jordano & Godoy (2002) observed dispersal patterns by animals with seed accumulation at specific points, while much of the study area was not affected by dissemination, contrasting with generally more uniform anemocoric species patterns. Seed distribution is spatially heterogeneous due to animal behavior, which can cause deposits in preferred sites, such as burrows and nests, or in routine paths of passage (Schupp et al. 2002). For zoocoric species, the distance achieved should be more important than the possible advantages that could be provided by a spatially more uniform dispersion, since there would be less intraspecific competition.
For Silva, Assad & Evangelista (2008) the representative percentage of anemocoric species in Cerrado formations may be a consequence of the strong seasonality of this vegetation, which presents a well defined dry season, allowing the occurrence of abiotic dispersion.
The drupa and loculative capsule types were identified as the most recurrent in a central Cerrado area by Stefanello, Fernandes-Bulhão & Martins (2009) and in the Perennial Seasonal Forest located in the municipality of Querência-MT by Stefanello et al. (2010). The large proportion of these fruit types in the studied area may be related to dispersion patterns in the studied Cerrado area.

Final Considerations
The Fabaceae, Euphorbiaceae, Malpighiaceae, Apocynaceae, Myrtaceae and Rubiaceae families showed a greater number of species richness in the Cerrado area studied.
The studied vegetation has a higher occurrence of arboreal and shrub species, respectively.
Most of the species occurring in the transects are considered frequent when they are classified according to their conservation status. Moreover, rare species highlighted due to their low density were: Blepharodon pictum, Jacquemontia velutina, Ipomoea blanchetii, Eriope tumidicaulis, with three individuals each, and Piriqueta sidifolia with only two individuals. In this study the presence of three new species for the state of Ceará were verified: Eriope tumidicaulis, Myrciaria cf. tenella and Stachytarpheta cf. crassifolia.
The predominant dispersion syndrome among the studied species is zoocoria, followed by anemocoria and autocoria. Zoocoria was the most frequent among arboreal and shrub strata, which may be related to the drupa and berry fruits types, which were predominant among the identified species. In this way, the natural regeneration of forests is highly dependent on the fauna, evidencing that it must be protected for the maintenance of existing ecological processes, such as the propagation of propagules.
Considering the high number of endemic species that occur in the studied Cerrado area and the species that are in danger of being extinct in nature, this study is hoped to serve as a subsidy for conservation programs in order to aid a greater local preservation.
Considering the high number of endemic species that occur in the studied Cerrado area and the species that are at risk of extinction in the wild, it is hoped that this study will serve as a subsidy for conservation programs in order to help greater local preservation.
Thus, it is necessary to carry out further studies that can identify as local fauna species responsible for the spread of propagules, a better end to the interspecific ecological processes occurring in the Araripe National Forest-Apodi.