Flora of Baturité, Ceará: a Wet Island in the Brazilian Semiarid

Andréa Pereira Silvera1 0000-0001-6785-5319 Maria Iracema Bezerra Loiola2 0000-0003-3389-5560 Vaneicia dos Santos Gomes3 0000-0002-2357-992X Luiz Wilson Lima-Verde2 0000-0002-6908-1692 Teógenes Senna Oliveira4 0000-0002-9904-6708 Edison Fernandes Silva5 0000-0001-8696-6831 Adriana Tamie Otutumi2 0000-0002-7443-4720 Kátia Araújo Ribeiro2 0000-0003-3002-4049 Francisco Alisson da Silva Xavier6 0000-0002-8141-2343 Morgana Maria Arcanjo Bruno7 0000-0001-6967-4749 Sarah Sued Gomes Souza2 0000-0001-6943-7401 Francisca Soares Araújo2 0000-0003-4661-6137


INTRODUCTION AND OBJECTIVES
The mountain ranges in the semiarid domain of Northeastern Brazil stand out from the surrounding flattened landscape expressing a climatic exception (Mantovani et al., 2017;Moro et al., 2015). They occupy approximately 5% of the northeastern surface, being scattered throughout the states of Ceará, Rio Grande do Norte, Paraíba, Pernambuco, Alagoas and Bahia (Souza & Oliveira, 2006). On windward slopes and at higher altitudes, the climate is cooler and wetter, whereas drier climates occur on leeward slopes and at lower altitudes (Nimer, 1989). This climatic variation leads to a spatially heterogeneous flora along the altitudinal gradient, consequently increasing the local species richness (Ferraz & Rodal, 2006;Homeier et al., 2010).
Evergreen and Semideciduous Forests have been commonly reported along this altitudinal gradient (Rodal & Sales, 2008;Silva & Figueiredo, 2013). Since this flora is a remnant of the Brazilian Atlantic Rain Forest (Barbosa et al., 2004), these mountain ranges have been considered a priority for the conservation of Brazilian biodiversity (Lopes et al., 2017;MMA, 2000). Especially in the Brazilian Northeast, the mountainous areas are critically important for the preservation of regional ecosystems, because they represent natural refuges for biota (Silva et al., 2014).
Thirty-five percent (35%) of the mountain ranges are located within Ceará State (Sobrinho, 1971), but information on its biota composition is still incipient (Bétard et al., 2007;Kamimura et al., 2017;Lima & Mansano, 2011). Plant cover and soils of most local wetlands have suffered from intensive and chronic anthropogenic disturbances (Souza & Oliveira, 2006). Therefore, reports on floristic composition are crucial for implementing sustainable use actions, since the biodiversity degradation on the Baturité Mountain Range has been happening since the colonial period (Mantovani, 2006;Oliveira et al., 2006). Our study shows the need for registering, cataloguing and presenting the biodiversity of such peculiar environments. Thus, we aim to analyze the plant composition and species richness along the altitudinal gradient on the windward and leeward slopes of Baturité Mountain Range, in Ceará State. We also intend to spread information on the local flora and on the protected areas of Northeastern Brazil.

Study site
The Baturité Mountain Range is a residual relief with an extension of 800 km 2 and moderate altitudes (800 -1,115 m). It is a Precambrian crystalline complex located in the northeast of Ceará State, 70 km from the coast (Bétard et al., 2007;Souza & Oliveira, 2006). From the elevation of 600 m up, the mountain range is a strict protected area, the APA de Baturité. The first protected area was established by state law no. 20,956, on September 18, 1990, which was later altered by state law no. 27,290, on December 15, 2003. Currently, it encompasses 32,690 hectares.
Both the altitude and the geographical position favor an orographic effect at the top and on the windward slope (north-eastward) of the mountain, whereby a humidity of > 1,000 mm × year -1 is carried by South Atlantic trade winds. On the leeward slope (westward), the precipitation is below 1,000 mm × year -1 (Mantovani, 2006;Santos et al., 2012;Souza & Oliveira, 2006). In order to register the local species composition and richness, we selected three well-conserved areas on each slope, at the following altitudinal ranges: 400 -600 m a.s.l., 600 -800 m a.s.l. and above 800 m a.s.l. We chose these areas in order to comprise the climatic and physiognomic variations along the altitudinal range on both slopes (Table 1). The Forested Steppic Savanna (FSS; "Caatinga") is composed of a thorny deciduous vegetation, predominant at lower altitudes. Along the altitudinal range, the FSS is gradually replaced by a forest vegetation along the altitudinal range. On the windward slope, there are: i) a Seasonal Semidecidous Submountain Forest (SSSF) 400 -600 m; and ii) a Seasonal Evergreen Mountain Forest (SEMF) above 600 m. On the leeward slope, there are: i) a transition from the FSS to the SDSF (Seasonal Deciduous Submountain Forest) 400 -600 m; ii) a Seasonal Deciduous Mountain Forest (SDMF) 600 -800 m; and iii) a Seasonal Evergreen Mountain Forest (SEMF) above 800 m (see Table 1).

Data collection
In order to list the plants, we sampled 200 quadrants in each of the six areas, according to the procedures suggested by Araújo et al. (2006). In addition, we completed our list researching the samples of the EAC Herbarium of the Universidade Federal do Ceará. We also revised and updated the taxonomic identifications with the aid of specialists from the following herbaria: EAC, PEUFR, IPA and CEPEC. The taxonomic classification that we used follows the APG IV system (2016). The names of botanical families, genera, species and authorships were confirmed in the International Plant Names Index (Royal Botanic Gardens, Kew et al., 2015) and in the list of Brazilian Flora 2020 (JBRJ, 2016).
To categorize the vegetation physiognomy, we used Whittaker's classification of plant growth forms (1975). The growth forms are adequate indicators of communities, since they can reflect global and local climatic conditions. We adjusted Whittaker's (1975) system as following: i) trees: > 3 m-height woody plants; ii) shrubs: > 3 m-height woody plants with main branches developing at approximately 50 cm above ground; iii) subshrubs: < 2 m-height plants with a woody main stem and herbaceous secondary branching; iv) terrestrial herbs: land plants with herbaceous aerial stems; v) epiphytes: plants with herbaceous stems that use other plants as support; vi) vines: plants with prolonged stems that twine around a substrate; and vii) hemiparasites: photosynthetic plants that withdraw sap from their host plants.
We obtained precipitation data from the Fundação Cearense de Meteorologia e Recursos Hídricos (FUNCEME, 2017), at the following local stations, close to our studied areas: Baturité-n22, Pacoti-n105, Guaramiranga-54, Mulungu-n98 and Caridade-n31. Data showed a seasonal rainfall regime with precipitation concentrated from January to May, driven by the Intertropical Convergence Zone. However, stations located at distinct altitudes and different mountain slopes showed remarkable differences in the annual rainfall regime.
Greater precipitation was found in the northeastern slope and at higher portions of the mountain range. The soil classification of the studied areas followed that of Oliveira et al. (2006). Altitudinal ranges and coordinates were measured in the field with a GPS navigation device (Table 1).

Data analysis
We organized our list by family, species, vernacular name, growth form, altitudinal range, phytophysiognomy and collector number. Samples are deposited at EAC. We estimated the global richness, as well as the richness at family and species levels, and by phytophysiognomy. We analyzed the relationship between species richness, growth form (dependent variable), and altitude (independent or predictive variable) through a simple linear regression using the Bioestat 5.0 Software (Ayres et al., 2007)

RESULTS AND DISCUSSION
We registered 400 morphospecies distributed within 92 families. A total of 23 taxa (13%) were identified only to the genus due to the lack of or inadequacy of reproductive organs. The families with greatest species richness were Myrtaceae (43 spp.), Fabaceae (38 spp.), Euphorbiaceae (21 spp.), Rubiaceae (20 spp.), Melastomataceae (14 spp.), and Bromeliaceae, Erythroxylaceae and Orchidaceae, with 10 species each (Appendix A). The high richness of vascular plants confirms the documented pattern for mountainous areas of the Brazilian semiarid: they are more diverse than the surrounding Caatinga, since they contain a mix of Caatinga and Atlantic Forest species (Carnaval et al., 2009;Leite et al., 2016;Lopes et al., 2017). In addition, the richness of 400 species of vascular plants, found on the Baturité Mountain Range, is higher than the species richness registered for other similar Brazilian forests, e.g., Pau-Ferro Ecological Reserve, with 309 species, in Paraíba State (Barbosa et al., 2004), Brejo Madre de Deus, with 293 species, in Pernambuco State (Nascimento et al., 2012) and Meruoca Sierra, with 100 species, in Ceará State (Silva & Figueiredo, 2013), highlighting the importance of this montane forests for the conservation of tropical biodiversity.
Our results show that the richness increases towards the top of the mountain, and that it is greater on the windward slope at the Evergreen Forest. We registered a total of 255 species (64%) and 69 families (75%) at higher altitudes, above 800 m in the Baturité Mountain Range -joined data from Arvoredo and Lagoa sites. On the windward slope, below 800 m-on Sinimbu and Taveiras sites together-, we registered 175 species (44%) and 62 families (67%); whereas, on the leeward slope, below 800 m-on Jardim and Salva-Vidas sites together-, we registered 127 species (32%) and 50 families (54%) (Appendix A). Such differences reflect the combined effects of ocean winds, altitudinal variation and position of the slope. These results also corroborate the pattern documented by Lopes et al. (2008), Lima et al. (2011), Kamimura et al., (2017) and BFG (2015, that indicates dry forests have significantly less species and families compared to humid-forests. In the Seasonal Evergreen Forest located both on the windward and leeward slopes-above 600 m and 800 m, respectively (Table 1) In the former, Mimosoideae (8 spp.) and Faboideae (7 spp.) predominated, whereas in the latter the most representative were Mimosoideae (13 spp.) and Caesalpinioideae (11 spp.).
In the Baturité Mountain Range leeward slope, where Deciduous Forests and Forested Savannas were the most representative (see Alcoforado-Filho et al., 2003;Cestaro & Soares, 2004;Ferraz et al., 2004), the subfamilies Mimosoideae and Caesalpinioideae, predominated. Even though Myrtaceae was among the most diverse families on the leeward slope, its richness was higher on the windward slope. Furthermore, most of its species (84%) occur above 600 m, indicating that the richness of Myrtaceae in the Brazilian semiarid is more associated with areas with higher water availability than with the surrounding Caatinga. The area of occurrence of Myrtaceae in the Evergreen Forest, both on the windward and on the leeward slopes, above 600 m and 800 m, respectively, confirms the pattern reported by Peixoto & Gentry (1990), also observed in the Atlantic Domain as a whole. Furthermore, Myrtaceae, Fabaceae, Rubiaceae, Bromeliaceae, Melastomataceae, Euphorbiaceae and Orchidaceae are abundant in Tropical Rainforests as well, including lowland and highland Seasonal Evergreen Forests in the States of Pernambuco and Paraíba (Rodal & Nascimento, 2002;Andrade & Rodal, 2004;Barbosa et al., 2004;Ferraz & Rodal, 2006;Nascimento et al., 2012;Rodal & Sales, 2008). Species and family similarities to this type of forest are likely associated with water availability on the soil, from rainfall or dew.
Aspidosperma pyrifolium Mart., Bauhinia cheilantha (Bong.) Steud., Cordia glazioviana (Taub.) Gottschling & J. S. Mill., Croton blanchetianus Baill., and Mimosa caesalpiniifolia Benth. occurred below 600 m on the windward slope. These taxa are commonly found in the Caatinga. Some species are strictly distributed in wetter areas, above 800 m on the windward slope and above 600 m on the leeward slope, such as: Concerning growth forms, the studied flora was composed of 214 trees (54%), 82 shrubs, 49 terrestrial herbs, 23 epiphytic herbs, 18 vines, 10 subshrubs and 4 hemiparasites. There was a positive correlation between altitude and richness of trees, shrubs, subshrubs, epiphytic herbs and terrestrial herbs (R 2 > 0.60 and p < 0.05). However, for vines and hemiparasites, the correlation was not statistically significant ( Figure 1). The richness of tree species is one of the most striking characteristics of the Tropical Forest typologies, a pattern documented in other Brazilian Atlantic forests (BFG, 2015;Nascimento et al., 2012).
The species richness and composition found in our study showed that, on the windward slope above 600 m, and on the leeward slope above 800 m, the flora is more similar. In contrast, below these altitudinal levels, on both slopes, the flora differed. The positive correlation between diversity and altitude is likely a response to greater water availability in higher elevations of the altitudinal gradient. The mountains of Northeastern Brazil are relatively low, with some altitudes of approximately 1,000 m a.s.l. However, they have a more favorable water balance, milder temperatures, and lower rates of evapotranspiration and evening condensation than the lower area of the countryside depression (Mantovani et al., 2017;Moro et al., 2015;Souza & Oliveira, 2006). This may explain why the plant species richness in the semiarid domain of Northeastern Brazil increases with higher altitudes.
It is also worth mentioning that the greater richness of epiphytic herbs (18 out of 23 species) at altitudes above 800 m reflects a higher humidity. According to Gentry (1988), there is a positive correlation between diversity and

CONCLUSION
In conclusion, 273 species (68%) were found exclusively at the top of the mountain and on the windward slope; 81 species (20%) were exclusively found on the leeward slope; and 46 species (12%) were found on both slopes, with a total of 400 species on the Baturité Mountain Range, in Ceará State. Our results highlight that the management actions, the restoration of degraded areas and the establishment of integral conservation on the Baturité Mountain Range must consider the spatial heterogeneity described in our work; that is, the differential plant distribution and richness both along the altitudinal gradient and between slope positions. Adequate conservation efforts should consider the total richness and the local heterogeneity.

ACKOWLEGMENTS
We are grateful to the taxonomists who gently identified the botanical material; to the land owners for allowing the data collection (Arvoredo, Lagoa, Sinimbu, Labirinto dos Taveiras, Jardim and Salva-Vidas sites); and to the Companhia de Eletricidade do Estado do Ceará (COELCE) for funding this study. Special thanks to teacher Maria Angélica Figueiredo (in memory), idealizer of the studies referring to Flora of Ceara, in special of the mountain range of Baturite.    Myrsine umbellata Mart.