Flora and similarities of a rocky outcrop in the Caatinga, eastern region of South America

Rocky environments show great habitat heterogeneity and very specific microclimatic characteristics that select for appropriately adapted floristic assemblages. A floristic survey was carried out on a rock outcrop in the driest portion of the Cariri Environmental Protection Area (APA) in Paraíba State, northeastern Brazil, to determine its similarity to other Caatinga sites. We recorded 128 species distributed among 103 genera and 52 families. Fabaceae, Convolvulaceae, Malvaceae, Euphorbiaceae, Asteraceae, Cactaceae, Bromeliaceae, Rubiaceae, and Poaceae were the most representative families in terms of numbers of species, with a high representation of herbaceous and shrub components and a predominance of typically Neotropical species, in addition to endemic taxa. Pectis linifolia L. (Asteraceae) is recorded here for the first time in the Paraíba state, Brazil. Similarity analysis evidenced that the study area, located in an extremely dry Caatinga zone, evidenced floristic relationships with other rocky outcrops in more humid areas, suggesting that habitat type is important for selecting specific groups, following the theory of refuges.


INTRODUCTION
Rocky environments are geological-geomorphological areas with significant expositions of rocky surfaces intercalated with erosional sediments (Thomas 1994).Those environments can be geologically diverse, varying in terms of their petrochemistry, size, time of formation, and the particular climate to which they are exposed (Shure 1999).Such rocky landscapes can be encountered throughout the world, especially in the dry climates found in Australia (Lima et al. 2009b), Africa (Porembski et al. 1996), and South America (Ibisch et al. 1995, Giraldo-Cañas 2008).Porembski (2007) pointed out that few plant species can survive the ecological filters found in rocky areas, and even more so if the site is associated with a semiarid climate.Rocky outcrops in semiarid regions are subject to extreme daily temperature variations, intense insolation, and water deficits (Giraldo-Cañas 2001, 2008).Many plant species occurring in these environments therefore evidence several mechanisms to avoid water losses to the external environment, with a predominance of species with C3 and CAM metabolism and dormancy mechanisms (Porembski et al. 1996, Giraldo-Cañas 2001).
When the rocky outcrops of Brazil are compared to those found in the rest of South America, or other continents, the co-occurrence of many of the same botanical families can be noted (Larson et al. 1999)predominantly those circumscribed to the order Poales (Porembski 2007, Ribeiro et al. 2007, Scarano 2007).In this context, several authors have noted that the taxonomic groups associated with Brazilian rocky outcrops are the same as those encountered in Venezuela (Barthlott et al. 1993, Sarthou andVilliers 1998) and Colombia (Giraldo-Cañas 2001, 2008), although the exact species compositions vary due to local topographic heterogeneity.
According to Oliveira and Godoy (2007), rocky environments evidence marked environmental heterogeneities with distinct microhabitats that favor the establishment of different plant assemblages and induce important speciation processes (Larson et al. 1999).Plant species in those ecosystems most commonly occur in three basic types of habitats: 1) directly on rock surfaces; 2) in fissures; or, 3) on "islands" of soil (Giraldo-Cañas 2008), reflecting the affinities of those plants with the substrate (Barthlott et al. 1993, Porembski et al. 1996, Pigott 2000, Porembski 2007).The species that grow in direct contact with rock surfaces are known as rupicolous (or saxicolous) and constitute vegetation "islands" that can cover just a few square centimeters to hundreds of square meters (Meirelles et al. 1999).
Those rocky environments are considered refuge zones for the local fauna and flora, and harbor populations very distinct from the surrounding vegetation matrix (Burke 2002, Stewart et al. 2010, Keppel et al. 2012, Speziale and Ezcurra 2015), not only from the point of view of richness, but also in terms of their intrinsic life histories, where the emergence of the biotope shaped the biocenosis that colonized the place and that undergoes constant environmental and ecological natural selections over time (Andrade-Lima 1981, Ab'Sáber 1992).
Researchers have undertaken numerous floristic inventories in these rocky areas in southeastern (Oliveira andGodoy 2007, Pifano et al. 2007) and northeastern Brazil (França et al. 1997, Agra et al. 2004, Lemos 2004, Barbosa et al. 2007, Neves and Conceição 2007, Ribeiro et al. 2007, Rodal and Sales 2007, Araújo et al. 2008, Porto et al. 2008, Costa et al. 2009, Gomes and Alves 2010) in the Caatinga biogeographic province.Data are still insufficient, however, given the continental size of that country, and information on the floristic similarities between those rocky environments are still scarce.
We present here a floristic study of a rocky outcrop located in the Cariri Environmental Protection Area (APA), Paraíba State, in northeastern Brazil, designed to characterize its flora and compare it with other Caatinga areas with similar biogeographic conditions to determine if those rocky environments evidence similar floristic compositions.

Study area
The Cariri Paraibano micro-region is a sub-region of the eastern Borborema Plateau, which is located in the south-central portion of Paraiba State, with Caatinga vegetation.The climate there is characterized by high temperatures (average 25 °C), low rainfall (between 250-800 mm annually), nearly constant winds (average 20 km/h), and high levels of solar radiation (2800-3200 h/year) (Ab'Sáber 1992).The Cariri region occupies an area of approximately 13 845 km² and is considered the driest site within the Caatinga domain.Elevations vary from 400 to 600 m above sea level (Alves 2009).The rocky environment sampled was located on a low inselberg feature called "Sítio Bravo" (Figs. 1,2), which extends over an area of 7 ha (7°20'17"-7°12'10.3"S, 36°25'40"-36°10'02.2"W) with an average elevation of 478 m.a.s.l., between the municipalities of Boa Vista and Cabaceiras.
The name of the study area is "Sítio Bravo".This site is an elongated elliptical (whale-like) dome, similar to the low inselbergs (Bornhardts) initially described in Namibia, Africa (Lima et al. 2009b).Few regions in the world have geological characteristics and geomorphological features similar to the study area and there are some similarities with the Devil's Marbles in Australia, the Erongo Mountains in Namibia, and the Hoggar region of Algeria (Lima et al. 2009b, Lages et al. 2013).
Particularly in this study, it is not cliff or hillside vegetation, but a singular vegetation that appears between rock crevices or in the rock surfaces of a specific type of rocky outcrop that exists only in practically three places in the world mentioned above.This type of outcrop is called "matacão", as it became known in Brazil, being also known by the name "lajedo" (Lages et al.

2013).
The area has abundant boulders formed by the degradation of very large rocks, which present a process of monodevelopment of spheroidal exfoliation of blocks resulting from fractures.
Thin, rocky soils (neosoils, hosting saxicolous plants) cover the area, representing a typical geomorphological process of semiarid climates (van Schmus et al. 2011).According to Andrade-Lima (1981), the flora of the study area fits a type of seasonally dry Neotropical savanna, called "Cariri Paraibano", which is composed of high-medium-sized shrubs and trees.

Floristics
Field works were carried out in the area from March 2010 to October 2011, with surveys every fifteen days, to collect fertile botanical material (flowers and/or fruits) and make in situ observations.The collections and their herborization were based on the usual methodologies of floristic studies (Bridson and Forman 2004).The following data were recorded: location, date, collector and collection number, substrate type, life form (herb, sub-shrub, shrub, tree, vine, epiphytic, aquatic and its variants, such as emergent, amphibious, floating and submerged) (Velôso et al. 1992), and colors of the reproductive structures (flowers and fruits).Digital images were recorded for the individuals sampled and their habitats (rupicolous, terrestrial, aquatic, and aerial).
The habitat types were based on Velôso et al. (1992), supplemented with observations made in the field.
Species identifications were based on the specialized literature, especially in Flora and Funga do Brasil (FFB c2022) in addition to consultations with specialists.Several species were confirmed by comparisons with samples deposited in herbaria in Paraíba State (JPB -Herbarium Lauro Pires-Xavier and EAN -Herbarium Jayme Côelho de Moraes, belonging to the Campus I and II of the Federal University of Paraíba; Universidade Federal da Paraíba; UFPB) in the municipalities of João Pessoa and Areia, respectively.The floristic list was prepared following APG IV (2016).Species names and their respective authors were confirmed using the Missouri Botanical Garden (W 3 Tropicos c2019) and Flora e Funga do Brasil Online (2022) databases.The collections were incorporated into the Manuel de Arruda Câmara Herbarium (HACAM), belonging to the State University of Paraiba (Universidade Estadual da Paraíba -UEPB).
The geographical distribution of each species was verified by consulting regional floras and the online Global Biodiversity Information Facility (GBIF c2019), Global Invasive Species Database (GISD c2019), Tropicos c2019), and Flora e Funga do Brasil Online (FFB c2022) databases.When a species could not be determined to the specific level (due to the presence of fruits only, which could not provide taxonomic security), its phytogeographic information could not be determined.

Similarity
Based on published articles (including floristic inventories undertaken in the Caatinga domain using the methodology adopted in the present work), a table of all the plant species (plateaus, sedimentary environments, and other rocky environments) was compiled (including this study)generating a binary data matrix (presence/absence) that was then used to analyze the floristic similarities between the areas following Hubálek (1982).The publications used in this analysis were found using the Google Scholar platform, based on the following bibliometric descriptors: "rocky environments", "Caatinga flora", and "floristic survey".
Cluster analysis was subsequently performed based on an area dendrogram to detect similarities between them (Kent and Coker 1995).The dendrogram was constructed using the UPGMA (unweighted pair group method with arithmetic mean) cluster algorithm applied to the referred index of similarity (Jaccard IDJ).The Jaccard coefficient was used to avoid giving weight to the most common species (as the Sörensen index would) (Gotelli and Ellison 2004).Values above the 25 % cut-off were marked as "most significantly" related to each other (Muller-Dombois and Ellenberg 1974).PAST software version 4.1 was used for the statistical analyses (Gotelli and Ellison 2004).

RESULTS
A total of 128 species, 103 genera, and 52 families were identified in the study area, being 18 % monocots and 82 % eudicots.Most specimens were identified at the species level (91 %), 7 % at the generic level, and 2 % at the family level (Table 1).The families with the largest representativeness were Fabaceae (fourteen species), Euphorbiaceae, Malvaceae, and Convolvulaceae (nine species each), accounting for nearly 30 % of the recorded species (Fig. 3).
Other families noteworthy for their representativeness in the study area were: Cactaceae (six species), Asteraceae, Poaceae, and Bromeliaceae (five species each), and Rubiaceae (four species).
Pectis linifolia L. is recorded for the first time in Paraíba state, Brazil, in this study.
The stratum composed of herbaceous species, which accounts for 37 % of the species richness, completely disappears during the dry season, disappears a marked seasonality to the region (Fig. 4).Arboreal (22 %), sub-shrub (13.4 %), and shrub (8.6 %) individuals together account for 44 % of the total species, followed by aquatic plants (10 %), lianas (5 %), epiphytes (3 %), and a single hemiparasite The results show that species colonizing dry soils, full of rocks broken by weathering and rocky crevices composed of a type of neosoil (Table 1) correspond to 72 % of the total species, with preferential occupation of terrestrial habitats.Furthermore, in situ observations indicated that most tree species (Aspidosperma pyrifolium, Cochlospermum vitifolium, Commiphora leptophloeos, Erythroxylum caatingae, Handroanthus impetiginosus, and all Fabaceae arboreal species recorded) occurred mainly in cracks between the rocks, taking advantage of those waterretaining sites and creating distinct microclimates.
Rupicolous species accounted for only 6 % of the total number of species in the study area Regarding the geographic distributions of the taxa analyzed (Fig. 5), it can be seen that Neotropical species (40 %) predominate, followed by endemic (27 %), cosmopolitan (16 %), and pantropical (10 %) taxa; plants having uncertain distributions, for cases of plants identified only at the generic level or for indeterminate plants, accounted for 7 % of the taxa.
The cophenetic correlation coefficient for the dendrogram was 95.6 %, based on Jaccard's SI, indicating a construct with high explanatory power.The studied area is strongly floristically connected to the other typically rocky/stony areas of the Caatinga, indicating common floristic clusters (Fig. 6).A comparative synoptic is presented (Table 2), as well as comparisons of the richness of the different areas analyzed here (Fig. 7).

DISCUSSION
Bromeliaceae, Cyperaceae, Poaceae, Cactaceae, Euphorbiaceae, and Asteraceae are the families most frequently reported in rocky environments in both Brazil (Porembski 2007, Ribeiro et al. 2007, Scarano 2007) and Colombia (Giraldo-Cañas 2001, 2008), with families in the monocotyledon clade being the most common (Pigott 2000, Giraldo-Cañas 2008).Although the families grouped in the monocotyledon clade (17 %) are most common in this type of environment (Pigott 2000, Giraldo-Cañas 2008), we found that the Fabaceae, Euphorbiaceae, Malvaceae, and Convolvulaceae families evidenced greater diversity.It is worth mentioning that the families Bromeliaceae and Cactaceae had significant representativeness in this environment, mainly due to their tendencies to form dense monospecific assemblages in the cracks between the rock surfaces.
The predominance of Fabaceae species in the present study (11 % of the total) reflects the fact that this family has developed effective strategies for survival in xeric and nitrogen-poor environments (N2 fixation clade), corroborating the findings of Pereira et al. (2001) and Barbosa et al. (2007) in other Caatinga areas.Fabaceae is a large cosmopolitan family occurring in a wide variety of habitats (Judd et al. 2007), and the third largest family of plants in the study area.
Euphorbiaceae is one the most taxonomically diverse angiosperm families in the flora do Brazil, evidencing morphological adaptations to dry environments (Judd et al. 2007 (Judd et al. 2007).Acmella uliginosa (Sw.)Cass. is not encountered under those conditions, being common only in humid areas (Silva and Santos 2010).
Information on the synecological characteristics of Cactaceae species in northeastern Brazil is still restricted in floristic studies (Fabricante et al. 2010).However, according to Rocha and Agra (2002), the family is very common in seasonally dry areas in northeastern Brazil, and its species are well adapted to rocky environments.
The woody flora of the Cariri APA was quite notorious, reaching heights of up to 10 m and contradicting the common view that the seasonally dry vegetation in Brazil does not usually feature tall trees (Alves 2009).This more robust vegetation was encountered mainly in sedimentary valleys among cracks in the rocks, where the richest soils are presumably found (Lenza et al. 2011), and in areas of difficult access (which diminishes deforestation).Andrade-Lima (1981) suggested that there would be a subtype of tall Caatinga growing on crystalline soils in the Brazilian semiarid region (although without clearly defining it).That study also stated that this biocenosis was mainly associated with the Borborema Plateau, where the study area was located.
The Bromeliaceae family stood out among epiphytic species (Tillandsia spp.), confirming the observations of Porembski (2007), and reaffirming that this family is extremely common in treetops or on bare rock environments throughout the world.Although the study region has a low annual rainfall rate and evidences variations in tree canopy spacing, the epiphyte community was present throughout the area and formed dense populations.
Based on the habitat preferences of the species inventoried, it is interesting to note that their richness in these low rainfall and rocky environments is related to the variety of microhabitats found there.Species with adaptations that allow them to occupy similar habitats are thought to share similar biological adaptations in response to their common life history attributes (Gentry 1991).Rocky habitats can be considered "favorable" or "safe location" environments for many plant species (Barthlott et al. 1993).
The similarity analysis showed a cophenetic correlation coefficient of 90.55 %.The analysis of flora in plateau areas (16), inselbergs (4), and sedimentary environments (2) in the Caatinga domain showed an average floristic sharing of 20 % of its species.The floristic similarity dendrogram demonstrated that the study area flora was grouped into a subgroup composed of inselbergs ("lajedos", as they are known locally).Although those geomorphological features are also found in plateau areas, their floras are subject to very complex microhabitat restrictions, such as the absence of a well-defined soil layer, a high insolation rate, and high reflection of the sun's rays, extreme daily thermal amplitudes; all selective factors for species that can colonize those areas (Porembski 2007).The windward flank of the low inselberg studied here has microclimatic conditions with higher levels of relative humidity, while the study area had a leeward position (in addition to being in the driest Caatinga area).
These observed links between the floras of rocky areas reinforce the "theory of refuges" (Ab'Sáber 1992), which is used to explain the distributions of certain floristic groups by their predilection habitats that select for similar advantageous evolutionary traits, but also provide protection against predators.Although this theory is strongly related to both the historical and current distributions of species that reflect Pleistocene events (Burke 2002, Stewart et al. 2010), there are scientific proposals defining those zones as areas of stability "protecting" species from anthropic disturbances (Birks and Willis 2008).Today, those spaces could shelter regional biodiversity from the threats of climate change projected for coming years (Keppel et al. 2012).
Regarding the richness of rocky outcrops as compared to other Caatinga areas, the floristic diversity of these ecosystems, which despite evidencing similar floristic assemblies as other areas, demonstrate species diversities intermediate between plateau and mountainous Caatinga regions (Fig. 7; Agra et al. 2004, Rodal et al. 2005, Rodal and Nascimento 2005, Rodal and Sales 2007, Barbosa et al. 2007), terrestrial ecosystems, and regenerating areas (Pereira et al. 2001, Andrade et al. 2005, Andrade et al. 2007, Neves and Conceição 2007, Costa et al. 2009).This mesic richness is closely related to the severe environmental conditions found in rocky environments that act to filter for species having appropriate adaptations to survive extreme environmental conditions (such as abrupt temperature variations, water scarcity, and shallow soils with low nutrient contents) (Porembski et al. 1996(Porembski et al. , 2006;;Giraldo-Cañas 2001, 2008).

Implications for conservation
Despite being established in rocky environments under semiarid conditions typical of the Caatinga ecosystem, the study area community exhibited significant floristic diversity, with a flora typical of seasonally dry areas in South America (the Xeric corridor).Fabaceae, Convolvulaceae, Malvaceae, Euphorbiaceae, Asteraceae, Cactaceae, Bromeliaceae, Rubiaceae, and Poaceae are the most significant plant families in this type of environment, and the herbaceous and shrub strata are the richest in terms of species numbers (although the former are ephemeral in the highly seasonal

Caatinga domain).
The species composition found in the study area differed substantially from other surveys carried out in environments of the Caatinga itself, confirming a distinct flora of the western plateau of Borborema, as predicted by Andrade-Lima (1981).This implies that wetlands, mountains, and rocky outcrops areas are the habitats most indicated by botanists as shelters for biodiversity (Birks and Willis 2008;Speziale and Ezcurra 2015), and will require greater attention in terms of public policies due to their species richness and uniqueness environment (Rose and Burton 2011).
Our results suggest that historical factors (dispersal and floristic connections) are important elements in Caatinga fragments, although ecological factors, such as the interactions between plants and their physical environment, especially rock outcrops, need to be further studied for a greater understanding their floras and their autecological aspects.

Conceptualization
(1 %) belonging to the family Loranthaceae [Struthanthus syringifolius (Mart.)Mart.].This parasitic species is widely distributed in Brazil and is hosted mainly by tree species.It was found in the present study on two species of Fabaceae (Erythrina velutina Willd.and Libidibia ferrea Mart.) and on one species of Rubiaceae [Tocoyena formosa (Cham.and Schltdl.)K. Schum.].
, Lucena and Alves 2009), and represents a well-represented group in the study area.Two species of the genus Croton L. (C.blanchetianus Baill.and C. heliotropiifolius Kunth) were frequently encountered in the study area on rocky outcrops, confirming the findings of Alcoforado-Filho et al. (2003).Those authors emphasized a high frequency of Croton individuals in areas of Caatinga and on inselbergs in Colombian Guyana (Giraldo-Cañas 2008).Still considering the Euphorbiaceae, Jatropha Baill.species have wide distributions in Brazil, occurring in all of the northeastern states of that country, particularly in semiarid areas with both sedimentary and crystalline Caatinga in hypo-xerophytic and hyper-xerophytic regions (Lucena and Alves 2009) as well as in the Colombian Guyana (Giraldo-Cañas 2008).Jatropha mollissima (Pohl) Baill.was recorded in this study as occurring widely in sedimentary areas, corroborating the findings of Alcoforado-Filho et al. (2003); Andrade et al. (2005) noted that it showed high densities in degraded areas (as was also seen in the present study).On the other hand, Asteraceae species − Ageratum conyzoides L., Centratherum punctatum Cass., Conocliniopsis prasiifolia (DC.)R.M. King and H. Rob., Eclipta prostrata (L.) L., Pectis linifolia L., Tridax procumbens L. − are representative in the vegetation of open spaces, as well as those impacted by anthropic activities : HMF; data curation: HMF; formal analysis: HMF; funding acquisition: JIMM; investigation: HMF; methodology: HMF, JIMM; project administration: JIMM; resources: JIMM; software: HMF; supervision: JIMM; DAGC; validation: JIMM; DAGC; visualization: HMF; JIMM; DAGC; writingoriginal draft: HMF; JIMM.writingreview & editing: HMF; JIMM.

Figure 1 .
Figure 1.Location map of the "Sítio Bravo" study site, Environmental Conservation Area (APA) of Cariri, municipality of Boa Vista, Paraíba state, Brazil, and the areas considered in the similarity analysis.

Figure 3 .Figure 4 .Figure 5 .Figure 6 .
Figure 3. Distribution of the representativeness of genera and species by family of Angiosperms in the "Sítio Bravo" study site, Environmental Conservation Area (APA) of Cariri, municipality of Boa Vista, Paraíba state, Brazil.