Flora of Ceará, Brazil: Vitaceae

Abstract We examined here the diversity and distribution of Vitaceae species in Ceará state, Brazil, as part of the “Flora of Ceará Project: knowing to conserve”, analyzing the morphological characters of specimens collected in the field, those available in the ALCB, BHCB, EAC, CEN, EAFM, HCDAL, HST, HUEFS, HUVA, HVASF, IAN, IPA, K, MBM, MOSS, NY, P, R, UEC, and US herbaria or in the specialized literature. We include here an identification key, occurrence maps, morphological descriptions, and comments concerning their ecology. The main morphological features for species delimiting were leaf type and symmetry, trichome and tendril types, presence or absence of streaks on branches, stipule, flower bud and fruit shape. Eleven species of Vitaceae included within two genera were recorded in Ceará: Cissus albida, C. blanchetiana, C. campestris, C. erosa, C. gongylodes, C. subrhomboidea, C. sulcicaulis, C. tinctoria, C. verticillata, C. xerophila, and Clematicissus simsiana. The species were registered in 45 municipalities, with C. erosa and C. verticillata being widely distributed. Those species inhabit different phytoecological areas in Ceará, although preferentially growing in Stepic Savanna (Caatinga). Six species occur in nine legally protected conservation areas. Ceará state holds 40.74% of the registered species of the family found in northeastern Brazil.


Introduction
The order Vitales is composed of only the Vitaceae family, which, in turn, comprises 14 genera and 850 species distributed in pantropical as well as temperate regions globally (Stevens, continuously updated).Cissus L. is the largest genus of the family, and its 300 species have disjunction intercontinental pantropical distributions, being encountered in all of the principal tropical regions (Liu et al. 2013).Of the 78 New World species, 64 are found in South America (Rodrigues et al. 2014).
Generic boundaries have been problematic in Vitaceae, and particularly in Cissus, as the genus shows extraordinary morphological diversity and complex geographic distributions (Rodrigues et al. 2014).Based on plastid (trnL intron, trnL-F intergenic spacer, rps16) and nuclear DNA sequences (ribosomal internal transcribed spacer -ITS), as well as in the morphological characteristics of the South American Cissus species, the genus was considered nonmonophyletic and composed of three clades: Cissus striata, Cissus trianae, and Cissus core (Rodrigues et al. 2014).New combinations for the South American species of the clade Cissus striata under Clematicissus Planch.(Lombardi 2015) apparently resolved this problem, however, Cissus trianae Planch.should remain in the genus (Zhang et al. 2015).
The Cissus core is inferred to have originated in Africa and to have diverged from its relatives in Vitaceae in the Late Cretaceous (Liu et al. 2013).The geographic disjunction between New and Old World taxa of the Cissus core has been estimated to have originated in the Late Eocene, with diversification in the Americas beginning in the Oligocene (Rodrigues et al. 2014).Those authors also highlighted that while there is leaf shape plasticity within species and individuals, this feature is still considered useful for infrageneric classifications.Some species of Vitaceae, popularly known as grapes, are consumed in natura as well as in the manufacture of jams and juices, or in the production of wine; others are cultivated as ornamentals, such as the Japanese ivy [Parthenocissus tricuspidata (Siebold & Zucc.)Planch.]commonly seen blowing on buildings and walls (Souza & Lorenzi 2019).Histochemical and pharmacological examinations of species of the genus Cissus have revealed the presence of tannins, flavonoids, alkaloids and polysaccharides with medicinal (Oliveira 2006;Navarro 2009), antimicrobial and anti-inflammatory (Garcia et al. 2000), and antidiabetic properties (Beltrame et al. 2002).Cissus verticillata (L.) Nicolson & C.E.Jarvis, commonly known as "plant insulin", has hypoglycemic activity (Souza & Guarim Neto 2009), and is still used in traditional medicinal practices in Pará state, Brazil (in association with other plants) to treat the sequels of strokes (Barbosa et al. 2002).
Although Vitaceae is an important group in the flora of Ceará state, studies there focusing on the species of this family have been scarce, and rarely mentioned in floristic surveys (see Silva et al. 2012;Loiola et al. 2015Loiola et al. , 2020;;Silveira et al. 2020a, b).In the continuity of the studies within the "Flora of Ceará Project: Knowing to Conserve", a floristic survey of Vitaceae species was undertaken to contribute to a better understanding of their diversity and distribution in Ceará.

Material and Methods
The morphological analyses were based on specimens obtained during field expeditions conducted as part of the Flora do Ceará Project: Knowing to Conserve (2012-2019), which were subsequently deposited in the ALCB, BHCB, CEN, EAC, EAFM, HCDAL, HUEFS, HUVA, HVASF, IAN, IPA, K, MBM, NY, MOSS, P, R, UEC and US herbaria (acronyms according to Thiers [continuously updated] and HST, not indexed).
Specimen identifications were performed with the aid of the specialized literature (Lombardi 2000(Lombardi , 2013(Lombardi , 2016;;Araújo et al. 2020) and confirmed by the analysis of images of type collections available on the NY, P and R herbaria, Reflora -Virtual Herbarium (2021+), and Flora do Brasil online sites (Picanço & Lombardi 2020).
A stereomicroscope Nikon SMZ 1500 was used for the analysis of morphological structures.The descriptions of the family, genera, and species, as well as the identification key were prepared based on samples recorded within Ceará State.The terminologies of the vegetative and fertile morphological characters follow Harris & Harris (2001).Data referring to the growth forms (habits), habitats, phenology (period of flowering/fruiting), and popular names were obtained from the herbarium labels.

Results and Discussion
The species is endemic to Brazil, occurring at elevations between 400-1,800 masl (Lombardi 2000), in the states of Piauí, Ceará, Pernambuco, Bahia, Minas Gerais, Goiás, and Rio de Janeiro, in the Caatinga, Cerrado, and Atlantic Forest phytogeographic domains (Picanço & Lombardi 2020).The species has been recorded in six municipalities in Ceará in Stepic Savanna vegetation known as Caatinga and Carrasco (Fig. 1a).
The species was flowering in March, April, and June; and fruiting in March and June.The species differs from the others occurring in Ceará by having compound leaves, bi-or tripinnate; trichomes malpighiaceous and eglandular; tendrils bifurcate; flowers with petals greenish-yellow and berry botuliform.

Cissus blanchetiana
Cissus blanchetiana is endemic to Brazil and has been recorded in the states of Bahia, Ceará, Paraíba, Pernambuco, Sergipe, Minas Gerais, Espírito Santo, in the Caatinga and Atlantic Forest phytogeographic domains (Picanço & Lombardi 2020).Its distribution in Ceará is restricted, having been recorded in only two municipalities in Dense Ombrophilous Forest (Fig. 1a).
The species was flowering in November and fruiting in March.Cissus campestris is widely distributed in northern, northeastern, southern, and midwestern Brazil, and in Paraguay (Lombardi 2000;Picanço & Lombardi 2020).In the northeastern region it was recorded only in Bahia and Ceará.It has been recorded in three municipalities in Ceará, in Stepic Savanna and Savanna vegetation (Fig. 1a).

Cissus campestris
The species was flowering in January and June; and fruiting in June.

Cissus erosa
Cissus erosa is widely distributed from Mexico to South America and in the Caribbean region (Lombardi 2000).It has been reported in all Brazilian states (except Santa Catarina and Rio Grande do Sul), in the Amazon, Caatinga, Cerrado, Atlantic Forest, and Pantanal phytogeographic domains (Picanço & Lombardi 2020).It has been collected in 15 municipalities in Ceará in Semideciduous Forest, Ombrophilous Dense Forest, Savanna, Stepic Savanna, Forested Savanna, and the Vegetation Complex of the Coastal Zone (Fig. 1a).
Cissus gongylodes is a South American species, occurring in Colombia, Venezuela, Peru, Brazil, and Bolivia (Lombardi 2000).It is widely distributed in Brazil, occurring in all of the Brazilian geopolitical regions and in the Amazon, Caatinga, Cerrado, Atlantic Forest, and Pantanal phytogeographical domains (Picanço & Lombardi 2020).The species has been recorded in four municipalities in Ceará, in Semi-deciduous Forest and Stepic Savanna vegetation (Fig. 1a).
The species was flowering in April, May, and July; fruiting from May to July.

Cissus subrhomboidea
Cissus subrhomboidea is distributed in Brazil and Paraguay (Lombardi 2000).In Brazil, the species is widely distributed, but has not been recorded in the southern region (Picanço & Lombardi 2020).It was collected in only one county in Ceará, in Ombrophilous Dense Forest vegetation (Fig. 1a).
Cissus sulcicaulis is a South American species occurring in Brazil, Bolivia, Paraguay, and Argentina (Lombardi 2000).In Brazil, it has been recorded in the Amazon, Caatinga, Cerrado and Atlantic Forest phytogeographical domains (Picanço & Lombardi 2020).It is known from six municipalities in Ceará, in Stepic Savanna and Semi-deciduous Forest vegetation (Fig. 1b).
The species was flowering from April to June and fruit in May.The leaflets are cooked to treat edema and rheumatism; its fruits are acidic, but edible (Côrrea 1931).The species vernacular name is roma.Spix & Martius, Reise Bras. 1: 368 (1823) The species is distributed in Brazil and Bolivia (Lombardi 2000).It occurs in the northern, northeastern, southeastern, and midwestern geopolitical regions of Brazil in the Amazonia, Caatinga, Cerrado, and Atlantic Forest phytogeographic domains (Picanço & Lombardi 2020).It has been recorded in 12 municipalities in Ceará, in Semi-deciduous Forest, Stepic Savanna, and the Vegetation Complex of the Coastal Zone (Fig. 1b).
Cissus verticillata can be recognized by having leaves simple and symmetric, stipules falcate, and petioles 1-2.5 cm long.Four subspecies are recognized for this taxon, but only C. verticillata subp.verticillata occurs in Brazil.For their morphological differences, refer to the comments in the descriptions of C. campestris and C. tinctoria.
Cissus verticillata is widely distributed in the neotropical region (Lombardi 2000) and is found in all Brazilian phytogeographic domains (Picanço & Lombardi 2020).It has been recorded in 17 municipalities in Ceará, in the Vegetation Complex of the Coastal Zone, Ombrophilous Dense Forest, and Stepic Savanna (Fig. 1b).
The species was flowering from April to August and from October to December; fruiting from April to July, and from October to December.

Cissus xerophila
Cissus xerophila is easily recognized in the study area, as it is the only one that presents simple leaves, branches terete, striate, and flower buds rounded.
Cissus xerophila is endemic to Brazil, with disjunct distributions in the states of Ceará, Minas Gerais and Rio de Janeiro (Picanço & Lombardi 2020), being registered in the first two states in the semi-arid domain.It has been recorded in only one municipality in Ceará, in the Vegetation Complex of the Coastal Zone (Fig. 1b).
The species was flowering in February, June, September, October, and December; fruiting in February, April, June, July, September and October.The species vernacular name is calorde-figo.

Figure 1 -
Figure 1 -Geographic distribution of the Vitaceae species occurring in the state of Ceará.

Figure 3
Figure 3 -a-d.Cissus albida -a.detail of a branch bearing the inflorescence; b. detail of the branch highlighting the indumentum; c. open flower; d. top view of flower, highlighting the disk.e-f.Cissus blanchetiana -e.branch with compound leaves; f. open flower highlighting the disk and style.g-i.Cissus erosa -g.young leaf; h.open flower highlighting the disk; i. infrutescence.j-k.Cissus gongylodes -j.leaf; k. open flower highlighting the disk and style.l-m.Cissus sulcicaulis -l.detail of a branch, highlighting the winged petioles; m. flower buds and open flower highlighting the disk and style.[a-d.Costa (EAC 35008); e-f.Souza et al. (EAC 28262); g-i.Loiola & André Neto 2834; j-k.Loiola et al. 1593].
A d d i t i o n a l m a t e r i a l e x a m i n e d : B R A Z I L .MARANHÃO: Lorêto, "Ilha de Balsas" region, between the rios Balsas and Parnaiba, about 30 km S of Loreto, ca.6 km S of main of Fazenda Sao Raimundo, trail from "Veados" to São Raimundo, 5.IV.1962, fl., G. Eiten & L.T. Eiten 4059 (US).
Cissus tinctoria is characterized by the presence of leaves oblong to cordiform with base cordate or subcordate and tendrils never branched.It is similar to C. campestris and C. verticillata by having simple leaves and branches terete not striate, and can be distinguished from both species by flower buds conical (vs.ellipsoid).