Original Paper / Artigo Original The genera Turnera and Piriqueta (Passifloraceae sensu lato ) in the state of Pernambuco, Brazil

A taxonomic treatment of the genera Turnera and Piriqueta in the state of Pernambuco, northeastern Brazil, is presented. Fourteen species of Turnera and six species of Piriqueta were found in the Atlantic Forest and Caatinga , of which nine are endemic to Brazil. Turnera pernambucensis is threatened and restricted to the Atlantic Forest of Pernambuco, while T. joelii is a new record for the state. The species predominate in steppe savanna and semideciduous seasonal forest, but several of them grow naturally in anthropized areas. Catimbau National Park is the locality with the highest species richness. Tristyly is recorded for the first time in Piriqueta guianensis . Identification keys, descriptions, illustrations, distribution maps, and comments about habitat, flowering, fruiting, and morphological relationships are provided.


Introduction
Turnera L. and Piriqueta Aubl. are the only genera of the former Turneraceae Kunth ex DC. (Passifloraceae sensu lato according to APG IV 2016) that occur in Brazil. Turnera comprises 143 species  disjunctly distributed in America and Africa, although its greatest diversity is found in tropical South America (Thulin et al. 2012). Piriqueta is an essentially Neotropical genus with 46 species distributed from the southern United States to northern Argentina and Uruguay (Thulin et al. 2012;Cabreira et al. 2015). Both genera have centers of diversity in Brazil (Arbo & Mazza 2011), where 120 native species of Turnera and 39 of Piriqueta occur (Arbo 2015;BFG 2018;Cabreira et al. 2015). The Brazilian Northeast region is particularly rich in terms of diversity, especially the state of Bahia (Rocha & Rapini 2016). In the state of Pernambuco 13 species of Turnera and six of Piriqueta were recorded in the Lista de Espécies da Flora do Brasil (BFG 2018).
According to the Virtual Herbarium of Plants and Fungi (2015), most specimens of Turnera and Piriqueta from Pernambuco were collected in only five localities and there are collection gaps in many regions. Moreover, the genera are poorly represented in regional floristic and phytosociological surveys and sometimes the identification does not reach the species level or it needs revision, as in Rodal & Nascimento Rodriguésia 70: e04152017. 2019 Gomes et al. (2006) and Gomes et al. (2011). Taxonomic studies involving the species occurring in Pernambuco are restricted to the Flora of Mirandiba (Agra et al. 2009), which includes a few species. The existence of taxonomic complexes in both genera also make species identification difficult.
Considering these points, this study provides a taxonomic treatment of the genera Turnera and Piriqueta from the state of Pernambuco, including identification keys, morphological descriptions, illustrations, geographical distribution maps, and information about morphological relationships, habitat, timing of flowering, and fruiting. Thus, it is expected to contribute to the recognition of the species in areas of the Caatinga and Atlantic Forest of Pernambuco and to expand knowledge about these genera in northeastern Brazil.

Materials and Methods
The state of Pernambuco spans 98,076,109 km 2 and is located in northeastern Brazil (IBGE 2015). The relief is predominantly flat, including lowlands along the Atlantic Coast and along the São Francisco River in the west (the Sertaneja Depression) separated by upland plateaus in the central (the Borborema Plateau) and northwest (the Chapada of Araripe) portions of the state (Ferreira et al. 2014). The dominant climates are Tropical Monsoon (Am sensu Köppen's climate) in a narrow band along the coast, Tropical with dry summer (As) just inland from the coast toward the central region of the state and Semi-arid (BSh) throughout the western region, forming strong rainfall gradients east to west, from 2,200 to 400 mm (Alvares et al. 2013). The vegetation comprises the Atlantic Forest and Caatinga phytogeographical domains, ranging from restinga, dense ombrophilous forest, open ombrophilous forest, and semideciduous seasonal forest in the east to steppe savanna in the west (adapted from IBGE 2012).
Fieldwork was conducted monthly from March 2015 to April 2016, including areas with different vegetation types found within conservation units or outside of them. A total of 14 areas were sampled, of which 10 are protected within conservation units. The collected specimens were processed according to the usual techniques in taxonomy (Mori et al. 1989) and deposited at UFP herbarium, with duplicates sent to RB and K herbaria (acronyms according to Thiers, continuously updated). The study also included an analysis of the previously collected specimens from the study area and deposited at ASE, HST (Herbário Sérgio Tavares), HTSA (Herbário do Trópico Semi-Árido), HVASF, INPA, IPA, JPB, MAC, MBM, PEUFR, RB, UB, UEC, UFP, and UFRN herbaria. Altogether 15 species were collected during the fieldwork and 573 vouchers were analysed for taxonomic treatment.
Morphological analyses were conducted under a stereomicroscope from specimens either dried or conserved in 70% ethanol. For taxonomic identification, protologs, revisions (Arbo 1995(Arbo , 2000(Arbo , 2005(Arbo , 2008, and images from type specimens available online were consulted. Morphological terminology follows Radford et al. (1974) and Arbo (1995Arbo ( , 2000Arbo ( , 2005Arbo ( , 2008, while Harris & Harris (2001) was used for indument characterization. Descriptions were based on specimens from the state of Pernambuco and supplemented with additional material when available. Data about geographic distribution, habitat and timing of flowering and fruiting were obtained from field observations, herbarium labels and literature. The vegetation types were standardized according to IBGE (2012, adapted) and checked in the Mapa de Vegetação do Brasil (IBGE 2004) when lacking. Distribution maps were generated using the SimpleMappr software (Shorthouse 2017). Illustrations were made from the examined material.

Results and Discussion
The genus Turnera is represented in Pernambuco by 14 species and Piriqueta by six species. Nine species (45%) are endemic to Brazil, of which Turnera pernambucensis Urb. is restricted to Pernambuco and has recently been rediscovered (Zelenski et al. 2016). Turnera joelii is recorded for the first time in the state.
Species of both genera occur in the Atlantic Forest and Caatinga areas. Most species of Turnera (12) grow in the Caatinga, of which six are found only in this domain, while T. annularis Urb. and T. pernambucensis are exclusive to the Atlantic Forest; these phytogeographical domains share six species. In relation to Piriqueta, all species occur in the Caatinga, of which P. cistoides (L.) Griseb., P. duarteana (A. St.-Hil., A. Juss. & Cambess.) Urb., and P. sidifolia (A. St.-Hil., A. Juss. & Cambess.) Urb. are exclusive to that domain.
The species predominate in seasonal vegetation types, such as steppe savanna with 18 species and semideciduous seasonal forest with 10 species, but there are also representatives in ombrophilous forest (5 spp.) and restinga (3 spp.). Thirteen species grow naturally in anthropized areas, of which T. subulata Sm., T. chamaedrifolia Cambess., and P. racemosa (Jacq.) Sweet are the most common. A significant number of species (11) were found on soil islands accumulated on crystalline or sandstone rock outcrops.
The highest species richness was recorded in the Catimbau National Park, a protected area of sedimentary Caatinga located in central Pernambuco, where six species of Turnera and three of Piriqueta occur. Some species, such as P. sidifolia, T. cearensis Urb., and T. hermannioides Cambess. exhibit large populations in this area. Turnera coerulea Moç. & Sessé ex DC. was recorded only in one locality within the study area, despite its wide Neotropical distribution. Most species (85%) have populations protected within federal, state, or private conservation units in Pernambuco, except T. annularis, T. blanchetiana Urb., and T. joelii Arbo. Only T. pernambucensis was evaluated in terms of conservation status and categorized as Critically Endangered (Zelenski et al. 2016), all other species have not yet been assessed.
The most relevant morphological characters to distinguish species of Turnera were the trichomes types, bracteoles shapes, corollas colors, and seeds shapes. For species of Piriqueta, the trichomes and inflorescence types were especially useful. Heterostyly with two floral morphs, brevistylous and longistylous, is found in 75% of species, while four species (20%) are tristylous with homostylous, brevistylous and longistylous flowers. Only P. viscosa Griseb. is homostylous. Tristyly is described for the first time in a population of P. guianensis N.E. Br. found in Catimbau National Park.

Turnera subulata
Figs. 4j; 5t; 8b Herbs or subshrubs, 20-70 cm tall; branches covered with simple trichomes and microcapitate glandular trichomes. Leaves papyraceous, concolorous or discolorous; stipules 0.4-1 mm long; petioles 2-11 mm long; nectaries basilaminar, 1 pair; blades 15-85 × 10-38 mm, elliptical, obovate or obtrullate, bases cuneate or attenuate, margins  marginally adnate 2-4 mm to tube from the base up to the throat; filaments 5-6 mm long in longistylous flowers, 8-10 mm long in brevistylous flowers; anthers 3-5 mm long; ovaries 1.5-2.2 mm long; styles 7-10 mm long in longistylous flowers, 3.5-6 mm long in brevistylous flowers; stigmas 1.5-3 mm long. Capsules 2.5-5 × 3-6 mm, verrucose, pubescent. Seeds 2.5-3 × 0.8-1.3 mm, straight or slightly curved, reticulate; chalazas rounded, not prominent. Widely distributed from Panama to Bolivia and Brazil (Arbo 2005). In Pernambuco, it was recorded in the Atlantic Forest and Caatinga, occurring in all vegetation types and soils, from just above sea level to 849 m elevation. This species grows in open areas, being very common in anthropized areas. Turnera subulata belongs to the T. ulmifolia complex (Arbo 2005). It is morphologically related to T. scabra, that also is part of complex, and similar to T. joelii, but can be distinguished from them by its flowers with a dark spot from the throat up to the base of the petals (vs. flowers without a dark spot) and seeds with rounded, not prominent chalaza (vs. concave, prominent chalaza in T. joelii). This species is often misidentified as T. ulmifolia in herbaria, which is distributed from the southern United States to Central America, including the Caribbean islands (Arbo 2005). Flowering and fruiting throughout the year, but most specimens were collected from December to May. The common name is arrancaestrepe, chanana, mentrasto-branco, saca-estrepe. a b