Flora of Paraíba, Brazil: Bombacoideae Burnett (Malvaceae)

: This work presents the taxonomic study of the native species of Bombacoideae Burnett (Malvaceae) in the state of Paraíba, Northeastern Brazil. The taxonomic treatment included keys for identifying genera and species, morphological descriptions, diagnostic illustrations, comments on taxonomic affinities, and additional information on geographical distribution, habitat, and flowering and fruiting of the species. Three genera and six species were recorded: Ceiba Mill., represented by C. glaziovii (Kuntze) K. Schum., is a new record for the Atlantic Forest; Eriotheca Schott & Endl., represented by E. gracilipes (K. Schum.) A. Robyns and E. macrophylla (K. Schum.) A. Robyns, is a new record for Paraíba; and Pseudobombax Dugand, which is represented by P. marginatum (A.St.-Hil., Juss. & Cambess.) A. Robyns, P. parvifolium Carv.-Sobr. & L.P. Queiroz and P. simplicifolium A. Robyns Robyns – the last one registered for the first time in Paraíba in this study.


Introduction
Malvaceae Juss. includes about 250 genera and 4,200 species, showing predominantly a pantropical distribution (Judd et al. 2009). Morphologically, this family is primarily characterized by presenting a nectariferous tissue located at the base of the calyx (or, less often, of the petals or sepals), valvular androgynophore, mucilage channels, and leaves with primary palminervate venation (Judd & Manchester 1997, Judd et al. 1999. Bombacaceae, formally known as Bombacoideae in phylogenetic classification systems, is now inserted in Malvaceae sensu lato (s.l.) as one of its nine monophyletic subfamilies, corroborated the studies of Baum et al. (1998), APG I (1998), Alverson et al. (1999) and APG IV (2016).
Bombacoideae gathers approximately 18 genera and 187 species, most of them pantropical with a greater diversity of species in the rainforests of South America. Brazil and Colombia are the more prominent countries for their highest representativeness in relation to the number of species (Gibbs & Semir 2003). According to the BFG (2015), 13 genera and about 80 species can be found in Brazil, mainly in the North and Northeast regions of the country.
Their species of Bombacoideae usually present deciduous leaves, with sessile or petiolate leaflets; often large flowers with sepals generally concrescent and glandular trichomes at the base; the receptacle is usually glandular; the ovary is superolateral, and the fruits, to the vast majority of their representatives, are capsule opening for 3-5 valves, with plentiful silky fibers and generally oilseeds inside (Reyes 1998, Bocage-Neta & Sales 2002, Aguiar 2012.
In general, the representatives of Bombacoideae have great economic importance and the can be used for various purposes: the wood can be used for manufacturing small boats, furniture, light objects, and cellulose paste; the wool that surrounds the seeds can be used for making life jackets, filling mattresses, pillows and as a thermal insulator; some seeds can be edible; in the ornamentation of squares (Esteves 2005, Lorenzi 2002a, Lorenzi 2002b. Their representatives can also used in the reforestation of degraded areas as they are considered to be rapidly growing (Lorenzi 2002a, Lorenzi 2002b.
Considering the representativeness of Bombacoideae in Brazil and the scarcity of studies in the Northeast region (e.g., Gibbs & Semir 2003, Esteves 2005, Carvalho-Sobrinho & Queiroz 2008, Carvalho-Sobrinho & Queiroz 2010, Duarte 2010, Duarte et al. 2011, Carvalho-Sobrinho 2013, the objective of this work was to elaborate taxonomic study of this subfamily in the state of Paraíba in order to enlarge the knowledge on its richness and geographical distribution. Identification keys genera and species, morphological descriptions and illustrations, data on geographic distribution and preferred environments, in addition to the phenology of the species found in the study area are presented.

Study area
The State of Paraíba ( Figure 1) is located in the Northeast of Brazil and includes 223 municipalities. It presents a territorial extension of 56,469.744 km ² divided into four meso-regions: Zona da Mata, Agreste, Borborema and hinterland (IBGE 2018). Its vegetation consists of mangroves (on the coast), a small strip of rainforest (Mata Atlântica) that stretches along the coast and enters to the West, forming projections associated with humid areas (elevated wetlands, Caatinga) and, in most parts, the Caatinga that comprises about 80% of the territory in which the vegetation vary between closed bushy-arboreal to closed arboreal caatinga (

Collecting expeditions and preservation
Monthly expeditions from August/2016 to February/2018 were made to several municipalities of Paraíba, covering areas of the Caatinga and the Atlantic Rainforest vegetation. Vegetative samples (stems and leaves) and fertile specimens (with flowers and/or fruit) of Bombacoideae representatives were collected. These samples were herborized and/or fixed in alcohol (70%) for detailed posterior morphological analyses, according to Peixoto & Maia (2013). These analyses were made in the laboratory of Botany and the specimens were incorporated into the collection of the Herbarium Manuel de

3.Taxonomic study
Morpho-taxonomic analyses were carried out between September/2016 and February/2018. During this stage, vegetative and reproductive structures were examined and resulted in the indentification of genera and species.
For morphological descriptions, specimens (vouchers) from the herbaria of Paraíba (CSTR, EAN, HACAM and JPB), Pernambuco (IPA and PEUFR) and Rio de Janeiro (RB), complemented by its own collections were used. Due to the lack of diagnostic structures such as flowers and fruits, the descriptions of some taxa were also based on additional specimens. The diagnosis of Eriotheca gracilipes, E. macrophylla and Pseudobombax simplicifolium were complemented by plant specimens from the online collections of herbaria online CEPEC, JPB and RB. Approximately 800 samples were analyzed from both physical holdings and scanning-based materials (Reflora). The herbaria acronyms follow Thiers et al. (continuously updated).
An identification key and illustrations of the main diagnostic charactres were prepared. The taxonomic treatment includes morphological descriptions, illustrations in Nankin ink and images of species and environments, the period of flowering and fruiting (phenology), geographic distribution, preferred environments and taxonomic, and taxonomic comments.
Ceiba glaziovii had already been registered in areas of the Caatinga of the state of Paraíba, but, through this research, its istribution is now extended to areas of the Atlantic Forest.
Pseudobombax Robyns] all of them associated with the phytophysiognomy of Caatinga, followed by Eriotheca Schott & Endl., with two species (E. gracilipes and E. macrophylla), both associated with the Atlantic Forest (elevated wetlands), and Ceiba Mill., with the species C. glaziovii (Kuntze) K. Schum., associated with both the Caatinga and Atlantic Forest areas (elevated wetlands).
The genus includes 22 species, most of them restricted to seasonally dry forests of Brazil (Gibbs & Semir 2003). In the Brazilian territory, Ceiba occurs from Mato Grosso do Sul to the northern Caatingas of the states of Minas Gerais and Bahia (Flora do Brasil 2020 in preparation), almost always associated with rocky outcrops, rock fields, and limestone fields.
Morphologically, Ceiba can be characterized by presenting: robust and aculeate stems, with aculeous that propagating all over the branches, without longitudinal streaks, large canopy, leaves alternate, compounddigitate with long petioles, leaflets 5-7, with serrate margins; flowers solitary or in few-flowered inflorescences, pentamerous, diclamydeous, the outside surface of the petals covered with simple trichomes, stamens 5, anthers bithecae, stem tube with or without appendages. Capsule 5-valvate, with abundant wool, seeds numerous, subglobose, without streaks; hilum protruding (Gibbs & Semir 2003). In the study area, Ceiba is represented by the species C. glaziovii, recorded in Caatinga vegetation (Agreste and Borborema). Trees, 14-15 m high; large canopy. Aculeate stem, including the young branches, with protuberance in the middle. Stipules absent. Compound leaves, digitate, 5-7 foliolated; petiole 80 mm long, 12.5 × 5 cm leaflets, oblanceolate, elliptical, membranaceous, acuminate apex, base cuneate to attenuated, entire margin from basis until the median region, serrate from median region until the apex, main vein salient on both sides propagating until the apex, glabrescent, secondary veins evident on both sides propagating until the apex, glabrescent, craspedodromous venation; solitary flowers, axillary, 8 cm long, scales absent, oblong and imbricate buds; pedicel 26 mm long; calyx 2.5 × 1.8 cm, campanulate, lobes 5, lightly apiculate, externally glabrous and internally with simple trichomes, nectariferous glands at the base of the receptacle; corolla 5.2 × 2.2 cm, spatulate, obovate apex, white, lilac to pink macules on the inner surface and simple trichomes in lower density; white exterior face, covered with simple trichomes, staminal tube 5 cm long, constricted to the median portion; stamens 5, distally free among each other, longitudinal fillaments 4.3 cm long, anthers 0.6-0.7 cm long, rimose, bitheca, glabrous, stigma 5-lobed; super ovary, with oil glands between the locules. Capsule 11-15 × 7 cm, oblong, 5-valvate, glabrous, valves 0.9-1.0 diam, epicarp porous, abundant wool. Seeds 0.7-0.6 mm long, reniforms. Ceiba glaziovii (Figure 3 and 4) is a Brazilian endemic species from the northeastern region, in the states of Bahia, Ceará, Paraíba, Pernambuco, Rio Grande do Norte and Sergipe (Flora do Brasil 2020 in preparation). The species can be easily recognized especially for presenting aculeate stems with, a protuberance in the middle region, five stamens, and by the white petals with lilac to pink macule sparsely arranged on the inner surface. This species had already been registered in the Caatinga vegetation of the study area; however, during the execution of this work, it was also recorded under the Atlantic Forest domain, which represents a new occurrence for this environment ( Figure 5). In the study area, it was found flowering in January and from May to December, and fruiting in November.
Eriotheca macrophylla is endemic from Brazil, occurring in the Northeast (Alagoas, Bahia, Pernambuco and Paraíba) and Southeast (Espírito Santo, Minas Gerais and Rio de Janeiro) regions, associated with the Atlantic Forest domain (Flora do Brasil 2020 in preparation). This species is a new record for the State of Paraíba (Figure 7) can be easily recognized by the carthaceous leaflets; oblong flower buds, and the externally flocculent ferrugineous trichomes on the calyx. In the study area, it was found with flowers in June and with fruits in May, July and August. Dugand, Caldasia 2(6): 65. 1943. This genus has 23 species, restricted to the Neotropical region (Duarte 2015). In Brazil, the species can be found in all the regions, inhabiting Ombrophylous forests, Semideciduous forests, Restinga, Caatinga, Cerrado, rocky field and ciliary forest, including in rocky outcrops (Flora do Brasil 2020 in preparation).
Pseudobombax simplicifolium (Figure 12) is endemic from Brazil, occurring in the Northeast (Bahia, Pernambuco, Piauí, Sergipe) and Southeast (Minas Gerais) regions, associated with the Caatinga domain (Flora do Brasil 2020 in preparation). In this work, it is reported as a new occurrence for Paraíba and inhabits the Caatinga vegetation ( Figure 10). Morphologically, P. simplicifolium is characterized by presenting 3-leaflets leaves united at the apex in braquiblasts. In the study area, it was found flowering in November. A. Robyns, Bull. Jard. Bot. l'État 33: 81. 1963.