Flora of Ceará, Brazil: Rhamnaceae

Abstract

We present the floristic-taxonomic and distribution survey of the family Rhamnaceae as part of the “Flora of Ceará: knowing to conserve” project. The survey was based on the analysis of morphological characters of specimens gathered during field expeditions and from herbaria collections, as well as the specialized literature. Rhamnaceae is represented by ten species in Ceará State belonging to five genera: Colubrina (2), Crumenaria (1), Gouania (3), Rhamnidium (1), and Sarcomphalus (3). The species were encountered in various phytophysiognomies, but especially occur in Seasonal Semideciduous Forests (Mata Seca) and the Coastal Zone Vegetation Complex (Lowland Semideciduous Forest). The species with the highest number of records was Sarcomphalus joazeiro, occurring in 62 municipalities. Seven species were encountered in 14 legally protected conservation areas in Ceará. Colubrina cordifolia, Rhamnidium molle, and Crumenaria decumbens occur exclusively in the Caatinga domain, with the first two being endemic to northeastern Brazil. Identification keys, morphological descriptions, comments on distributions, ecology, phenology, and uses of the species are provided, as well as maps and illustrations.

Keywords:
diversity; Gouania ; Rosales; Sarcomphalus

Resumo

O estudo objetivou realizar o levantamento florístico-taxonômico e a distribuição dos representantes da família Rhamnaceae, como parte do projeto “Flora do Ceará: conhecer para conservar”. O trabalho foi embasado na análise de caracteres morfológicos de amostras obtidas em campo, coleções de herbário e bibliografias especializadas. No território cearense, Rhamnaceae está representada por dez espécies pertencentes a cinco gêneros: Colubrina (2), Crumenaria (1), Gouania (3), Rhamnidium (1) e Sarcomphalus (3). As espécies foram registradas em diferentes fitofisionomias, mas ocorrem preferencialmente na Floresta Estacional Semidecídua (Mata Seca) e no Complexo Vegetacional da Zona Litorânea (Mata de Tabuleiro). O táxon com o maior número de registros foi Sarcomphalus joazeiro, ocorrendo em 62 municípios. Sete espécies foram registradas em 14 Unidades de Conservação do Ceará. Colubrina cordifolia, Rhamnidium molle e Crumenaria decumbens ocorrem exclusivamente no domínio da Caatinga e as duas primeiras espécies são endêmicas da região Nordeste. Chaves de identificação, descrições morfológicas, comentários sobre distribuição, ecologia, fenologia e usos, mapas e ilustrações das espécies são apresentados.

Palavras-chave:
diversidade; Gouania ; Rosales; Sarcomphalus

Introduction

Rhamnaceae comprises 1,000 species globally, included within 52 genera with cosmopolitan geographic distributions, although they are predominantly encountered in the tropics (with some species in the temperate regions) (Hauenschild et al. 2018; Lima et al. 2020). Its representatives have habits varying from trees to herbs and climbers; the sepals have a prominent midvein on the adaxial surface, petals unguiculate, convolute, cuculate or shell-shaped, stamens opposite the petals, and a nectariferous disk surrounding the receptacle (Lima & Giulietti 2006). The family is considered an ancient taxon, with diversification dating back to the Cretaceous, circa 94 m.y.a (Crepet et al. 2004), with 25 described fossils evenly distributed over time (Correa et al. 2010; Chen et al. 2017). Rhamnaceae is monophyletic, and has been the focus of molecular phylogenetic studies (based on nuclear, plastidial, and mitochondrial genetic sequences) that have contributed to the elucidation of infrafamilial circumscriptions (Richardson et al. 2000a; Kellermann & Udovicic 2008; Hauenschild et al. 2016).

The family was initially placed within the order Rhamnales, together with Vitaceae and Leeaceae, in traditional classification systems of flowering plants (Hutchinson 1964; Takhtajan 1969; Dahlgren et al. 1980; Cronquist 1981, 1988). The current classification, however, recognizes the family as subordinated to Rosales, and related to Barbeyaceae, Cannabaceae, Dirachmaceae, Elaeagnaceae, Moraceae, Rosaceae, Ulmaceae, and Urticaceae (Stevens 2001; APG IV 2016). Three main clades have been identified within Rhamnaceae: Rhamnoideae, including more than 300 species; Ziziphoideae (more than 600 species); Ampeloziziphoids (approx. 10 species) (Richardson et al. 2000b).

Species of Rhamnaceae are utilized by human populations in northeastern Brazil for different purposes. Sarcomphalus joazeiro (Mart.) Hauenschild is used in popular medicine as an expectorant (Araújo & Agra 2018) and to treat bronchitis and gastric ulcers (Lorenzi & Matos 2002); it also has ornamental uses for providing shade, and is planted along streets and in gardens (Lorenzi 2020). Hovenia dulcis Thunberg., an Asian species, is commonly used in urban landscaping and produces edible pseudo-fruits (Souza & Lorenzi 2019). Colubrina glandulosa Perkins is used in woodworking as well as in civil, hydraulic, and naval construction due to the excellent quality of its wood (Carvalho 2005).

Rhamnaceae is represented by 14 genera and approximately 50 species in Brazil, of which 15 are endemic (Lima et al. 2020). In the Northeast region, the family is represented by five genera and approximately 20 species, of wich 10 occur in the state of Ceará. Its species were studied while preparing the flora of São Paulo State, with 15 recorded taxa (Lima & Giulietti 2005). Local floras of Brazil’s northern and south-eastern regions include the Ducke Reserve in Amazonas, with seven species (Lima 2006b), the Grão-Mogol (Lima 2006a) and Serra do Cipó in Minas Gerais State (Lima 2011), which cite two and one species respectively. Rhamnaceae species are cited in floristic lists for northeastern Brazil in: Mirandiba/ Pernambuco - Crumenaria decumbens Mart. and Ziziphus cotinifolia Reissek (Lima 2009); Arcoverde/Pernambuco (Barbosa et al. 2012) - Rhamnidium molle Reissek; Entre Rios/Bahia (Alves et al. 2015) - Ziziphus platyphylla Reissek; Cajazeiras/Paraíba (Pereira et al. 2012) - Ziziphus joazeiro Mart.; Picos/Piauí (Rocha et al. 2016) - Z. joazeiro and Macaíba/Rio Grande do Norte (Ucella Filho et al. 2017) - Z. joazeiro. It is noteworthy that a phylogenetic study by Hauenschild et al. (2016), based on molecular genetic sequences, evidenced that individuals recognized within Ziziphus are restricted to Asia; those authors also proposed the reestablishment of Sarcomphalus, comprising species previously identified as Ziziphus in the Neotropics.

Although Rhamnaceae is an important component for the flora of Ceará state, with significant biological and cultural importance, its representatives are mentioned in only a few floristic lists (Silva et al. 2012; Loiola et al. 2015, 2020; Silveira et al. 2020a, b). Continuing the studies of the Project “Flora of Ceará: knowing to conserve”, we carried out a floristic-taxonomic survey of Rhamnaceae species to better understand the diversity of this group and to expand our knowledge of its geographic distribution there.

Material and Methods

Studies were made of specimens obtained during field expeditions, as well as of collections in the EAC, HCDAL, IPA, HUVA herbaria, the online database collections of ALCB, ASE, CEN, ESAL, FURB, HDELTA, HUEFS, HVASF, INPA, JPB, MAC, MBM, NY, R, UEC and UFP herbaria (acronyms in accordance with Thiers (continuously updated), and the non-indexed CSTR and HST herbaria.

The species were identified in accordance with the morphological features of specimens observed in loco, comparative analyses of exsiccates, photographs of type collections, and consultations of the specialized literature (Jussieu 1789; Johnston 1971; Johnston & Soares 1972; Lima 2000; Lima & Giulietti 2006; Richardson et al. 2000b; Medan & Schirarend 2004). The morphological terminology used here follows Harris & Harris (2001). Additional specimens from other Brazilian states were included to complement the descriptions for some taxa when samples collected in Ceará were incomplete with respect to their floral or fruit features.

Geographic distribution maps were elaborated using QGIS software (2020). Specimens without original geographic coordinates were georeferenced using their municipal coordinates and the “geoLoc” tool (CRIA 2021).

The vegetation types where the species occurred were based on the classification system of Figueiredo (1997) for Ceará state and the Technical Manual of the Brazilian Vegetation (IBGE 2012): Vegetation Complex of the Coastal Zone (comprising Pioneer Psammophilous Vegetation, Forest behind Dunes, and Lowland Semideciduous Forests), Neotropical Savanna (Cerrado), Semideciduous Seasonal Forest (mata seca), Steppic Savanna (caatinga and/or carrasco), Dense Ombrophilous Forest (mata úmida), Forest Savanna (cerradão), and Vegetation under Fluvial and/or Lacustrine Influence (mata ciliar). Information concerning the vegetation type, popular names, and flowering and fruiting periods were obtained from the exsiccate labels.

Freehand ink drawings were made and digitized to prepare the plates in an image editing program. The Canva platform was used to create the photographic plate.

Results and Discussion

A total of 10 species of Rhamnaceae, representing five genera, were recorded for Ceará state: Colubrina cordifolia Reissek, C. glandulosa, Crumenaria decumbens, Gouania blanchetiana Miq, G. colurnifolia Reissek, G. polygama (Jacq.) Urb., Rhamnidium molle, Sarcomphalus joazeiro, S. platyphyllus (Reissek) Hauenschild, and S. undulatus (Reissek) Hauenschild. As for the conservation status, only Colubrina glandulosa and Gouania blanchetiana were evaluated and classified as LC = least concern, that is, abundant and widely distributed species (CNCFLORA 2022).

Seven species were recorded in Semideciduous Seasonal Forest, Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest), and Dense Ombrophilous Forest. Colubrina cordifolia, Crumeria decumbens, Gouania colurnifolia and the three species of Sarcomphalus occur in Steppic Savanna. Colubrina cordifolia and S. joazeiro were recorded in Forest Savanna. Crumenaria decumbens, G. colurnifolia, S. joazeiro, and S. undulatus occur in Vegetation under Fluvial and/ or Lacustrine Influence. Only C. cordifolia was recorded in Savanna vegetation. The taxon with the highest number of records was Sarcomphalus joazeiro (62 municipalities). Rhaminidium molle had only two records from the 1950s, which indicates the need for more intensive sampling efforts in the areas where it was previously collected, as well as in other sites with similar environmental conditions within Ceará.

Seven species were recorded in 14 legally protected Conservation Areas in Ceará: the Missão Velha Environmental Protection Area (1); Dunas da Lagoinha Environmental Protection Area (2); Pacoti River Environmental Protection Area (1); Aiuaba Ecological Station (1); Pecém Ecological Station (1); Araripe-Apodi National Forest (1); Quixadá Monoliths Natural Monument (1); Ubajara National Park (2); Timbaúbas Municipal Natural Park (1); Serra das Almas Private Natural Heritage Reserve (2); Cocó State Park (1); Fazenda Trussú Private Natural Heritage Reserve (1), Pedra da Andorinha Wildlife Refuge (1), and Fazenda Não Me Deixes Private Natural Heritage Reserve (1).

Taxonomic treatment

Rhamnaceae Juss., Gen. Pl.: 376. 1789.

Herbs, shrubs, trees or lianas, unarmed or spinescent, with or without tendrils. Stipules lateral or intrapetiolar, elliptic, lanceolate, oblong or lanceolate. Leaves simple, alternate, opposite or subopposite, membranaceous, carthaceous or coriaceous, margin entire or serrate, with or without glands on the abaxial surface. Inflorescences in panicle, thryse or umbel. Flowers 5-merous, usually not showy, bisexual and/or unisexual, actinomorphic, diclamydeous; sepals with a prominent midvein on the adaxial surface; petals convolute, cucullate or shell-shaped; stamens in numbers equal to the petals, anthers rimose; nectariferous disk crassous, slender or membranaceous, glabrous, pubescent or velutinous; ovary superior, semi-inferior or inferior, 2-3-carpelar, 2-3-locular, one ovule per locule. Fruits drupe, capsule, or winged schizocarp; seeds ovate, oblong, obovate or ellipsoid.

• Identification key of the species of Rhamnaceae occurring in Ceará

• Herbs or lianas; ovary inferior; winged fruits.

• Herbs decumbent; inflorescences pauciflorous; fruits with trichomes papillose ............................

• ............................................................................................................2.1. Crumenaria decumbens

• 2’. Lianas; inflorescences densiflorous; fruits glabrescent or velutinous.

• 3. Branches pubescent; stipules lobed.............................................. 3.1. Gouania blanchetiana

• 3’. Branches velutinous; stipules entire.

• Leaves chartaceous; fruits velutinous .................................... 3.2. Gouania colurnifolia

• 4’. Leaves membranaceous; fruits pubescent, except in the wings ......................................

• ................................................................................................... 3.3. Gouania polygama

• 1’. Trees or shrubs; ovary superior or semi-inferior; fruits non-winged.

• Plants unarmed; leaf blade with glands and margin entire.

• Leaves membranaceous; stipules intrapetiolar; fruits drupe ..............4.1. Rhamnidium molle

• 6’. Leaves chartaceous; stipules lateral; fruits capsule.

• Leaf with abaxial surface densely velutinous; nectariferous disk plane .........................

• ................................................................................................. 1.1. Colubrina cordifolia

• 7’. Leaf with abaxial surface pubescent to velutinous; nectariferous disk sulcate...............

• ...............................................................................................1.2. Colubrina glandulosa

• 5’. Plants spinescent; leaf blade without glands and margin serrate.

• Spines slender; leaf margin ondulate and serrate ......................5.3. Sarcomphalus undulatus

• 8’. Spines stout; leaf margin plane and serrate.

• 9. Stipules lanceolate............................................................... 5.1. Sarcomphalus joazeiro

• 9’. Stipules ovate to oblong ................................................5.2. Sarcomphalus platyphyllus

Colubrina Rich ex Brongn., Ann. Sci. Nat. 10: 368. 1827. nom. cons.

Trees or shrubs unarmed; young branches velutinous or tomentose, ferrugineous, adult branches glabrous to glabrescent, lenticellate, ferrugineous. Stipules lateral, elliptic. Leaves opposite or subopposite, petiolate, ovate or elliptic, base rounded, apex acuminate, acute or obtuse, cordate or obtuse, margin entire, chartaceous, adaxial surface velutinous to pubescent or glabrescent, abaxial surface pubescent or densely velutinous, with glands atropurpureous, conspicuous, discoid, basal on each side of the petiole and/or submarginal; venation actinodromous. Inflorescences in thyrse, densiflorous, velutinous, ferrugineous. Flowers monoclinous and diclinous (staminate), morphologically similar to monocline flowers, except for styloids; 5-merous, velutinous, ferrugineous; sepals patent; petals convolute; 5 stamens, anthers ovate or subrounded; nectariferous disk conspicuous, crass, sulcate or plane; ovary superior or semi-inferior, 3-carpelar, 3-locular, 3 ovules, 1 ovule per locule. Fruits non-winged. septicidal capsule, globose, glabrous or glabrescent. Seeds obovate or subespherical, arillate.

Colubrina cordifoliaReissek, Fl. bras. 11(1): 98, tab. 25, fig. 2. 1861.

Figs. 1a; 2a-d

Shrubs or trees 1.5-7 m tall; young branches velutinous. Stipules 4-5 mm long, elliptic. Petiole 0.5-1.3 cm long. Leaves 4-13 × 2-8 cm, ovate, base cordate to obtuse, apex acute to obtuse, margin entire, slightly ondulate, chartaceous, adaxial surface glabrescent or velutinous to pubescent, opaque, abaxial surface densely velutinous with 1-6 glands discoid, submarginal. Thyrse densiflorous, 7-15 flowers per inflorescence; peduncle 1-4 mm long. Flowers 5-7 mm long, monoclinous: pedicel ca. 2 mm long; sepals ca. 1.5- 2 × 1 mm; petals ca. 1-1.5 mm long; claw 0.2-0.3 mm long; anthers subrounded; nectariferous disk plane; ovary ca. 2 mm wide, obovate, style free. Flowers staminate with filiform styloid. Capsule 1-2.1 cm long, globose, glabrous to glabrescent, fructiferous pedicel 1.2-1.5 cm long, velutinous. Seeds 5-6 mm long, obovate.

Selected examined material: Araripe, Chapada do Araripe, 07°12’45”S, 40°02’46”W, 14.IV.2015, fl., T.L. Costa & M.A. Chagas 72 (IPA). Barbalha, 07°33’36”S, 39°25’12”W, 23.V.2014, fl., M. Mayer (EAC 56775). Campos Sales, Salitre, 10.II.1984, fl., A. Fernandes & M.A. Figueiredo (EAC 12300, JPB 43105). Crateús, Reserva Particular do Patrimônio Natural Serra das Almas, 19.VI.2003, fl. and fr., R.C. Costa (EAC 35127). Crato, Floresta Nacional do Araripe-Apodi, 25.V.1999, fl. and fr., A.M. Miranda & D. Lima 3429 (EAC, HST, HUEFS, JPB, MAC). Guaraciaba do Norte, 26.V.1981, fl., A. Fernandes & P. Martins (EAC 10356). Nova Olinda, 07°05’30”S, 39°40’50”W, 10.III.2008, fl., W.N. Ferreira (HCDAL 4346). Novo Oriente, Planalto da Ibiapaba, 28.III.1990, fl., F.S. Araújo 40 (EAC, JPB). Santana do Cariri, Guritiba, 27.VII.2004, fl. and fr., A.S.F. Castro 1517 (EAC). São Benedito, Chapada da Ibiapaba, 20.VII1989, fl., A. Fernandes et al. (EAC 15789). Ubajara, Planalto da Ibiapaba, 25.IV.1994, fl. and fr., F.S. Araújo 672 (EAC, HCDAL).

Colubrina cordifolia is a notably distinct species, characterized by its leaves having the abaxial surfaces densely velutinous, with submarginal foliar glands, and plane nectariferous disk.

Colubrina cordifolia is endemic to northeastern Brazil, occurring in the states of Bahia, Ceará, Pernambuco, and Piauí (Lima et al. 2020). In Ceará, the species has been recorded in 11 municipalities in Savanna, Dense Ombrophilous Forest, Forest Savanna, and Steppic Savanna phytophysiognomies. The species has been recorded in two Conservation Areas: Araripe- Apodi National Forest and Serra das Almas Private Natural Heritage Reserve.

The species was collected flowering from February to July, and fruiting from April to July.

The popular names are guachumbo, imbiriba assú, joão vermelho.

Figure 1
a-b. Geographic distribution of Rhamnaceae in Ceará - a. Colubrina, Crumenaria, Gouania, and Rhamnidium; b. Sarcomphalus spp.

Colubrina glandulosaPerkins, Bot. Jahrb. Syst. 45: 465-466. 1911.

Figs. 1a; 2e-h

Shrubs or trees 5-15 m tall; young branches tomentose. Stipules 3-5 mm long, elliptic. Petiole 0.8-1.5 cm long. Leaves 6.5-17 × 3.5-9 cm, ovate to elliptic, base rounded to cordate, apex acute to acuminate, margin entire, revolute, chartaceous, adaxial surface glabrous to glabrescent, shiny, abaxial surface pubescent to velutinous with 1-2 glands discoid, basal, near to petiole and 3-10 glands submarginal. Thyrse densiflorous 10-40 flower per inflorescence; peduncle 1-6 mm long. Flowers 4-5 mm long, monoclinous: pedicel 2-2.5 mm long; sepals 1.5-1.8 × 1 mm; petals ca. 1.5 mm long; claw 0.1-0.2 mm long; anthers ovate; nectariferous disk sulcate, margin crenate; ovary ca. 2 mm wide, subglobose to globose, style free at apex. Flowers staminate with filiform styloid. Capsule 1-1.5 cm long, globose, glabrous; fructiferous pedicel 3.5-7 mm long. Seeds 4-4.5 mm long, subglobose, biconvex.

Selected examined material: Aratuba, Sítio Brejo, 14.V.1980, fl., P. Martins & E. Nunes (EAC 8609). Baturité, 21.VI.1976, fl., A. Fernandes & F.J.A. Matos (EAC 2786). Crato, Chapada do Araripe, 07°14’03”S, 39°24’33”W, 26.IV.2017, fr., N.B. Campos 62 (HCDAL). Fortaleza, Bairro Alagadiço Novo, 7.V.1999, fl., A.S.F. Castro 689 (EAC). Guaramiranga, Sítio Guaramiranga, 04°17’49”S, 38°55’59”W, 9.IX.1989, fr., V.S. Gomes et al. 1205 (EAC). Pacoti, Serra de Baturité, 16.X.1961, fr., M.A. Figueiredo (EAC 18470).

Two subspecies are recognized in Brazilian territory: Colubrina glandulosa subsp. glandulosa and C. glandulosa subsp. reitzii (Lima et al. 2020) and both occur in Ceará. The first has leaves membranaceous (vs. chartaceous), abaxial surface glabrescent (vs. pubescent to velutinous), wavy margin (vs. revolute) and pedicels 2-3 mm long (vs. 5-6 mm).

The species is widely distributed in Brazil, occurring in the states of Maranhão, Ceará, Paraíba, and Pernambuco in northeastern Brazil (Lima et al. 2020). It was recorded in six municipalities in Ceará, in Dense Ombrophilous Forest, Semideciduous Seasonal Forest, and the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest).

The species was collected with flowers in April and May, and with fruits in April, September and October.

These species are used in comercial wood, ornamental, reforestation (Montagna & Reis 2011). The popular names aresobraji, sobrasil, sobraju, saraguari.

CrumenariaMart., Nov. Gen. Sp. pl. 2(1): 68., t. 160. 1826.

Crumenaria decumbensMart., Nov. Gen. Sp. pl. 2(1): 68., t. 160. 1826.

Figs. 1a; 2i-j

Herbs 20-35 cm tall, decumbent, unarmed, tomentose; branches cylindric, striate. Stipules ca. 2 mm long, lateral, lanceolate, margin with trichomes simple. Petiole 0.8-1 mm long. Leaves 1-3 × 0.6-2.8 cm, simple, ovate, base cordate to obtuse, apex acute or apiculate, margin entire or serrate, membranaceous, adaxial surface with pappilose trichomes simple, abaxial surface glabrous, glands absent; venation actinodromous. Inflorescences umbelliform, axillary, pauciflorous, usually 1-3-flora; bracts linear, prematurely deciduous. Flowers 2-3 mm long, monoclinous and diclinous (staminate), 5-merous, with pubescent hypanthium; pedicel 0.6-0.8 mm long; calyx tube 1-1.4 mm long, with trichomes; lobes with acute apex; petals 0.4-0.6 mm long, cuculate, unguiculate petal ca. mm long; anthers ovate; nectariferous disk membranaceous, glabrous, plane; ovary obovate, inferior, 3-carpelar, 3-locular, one ovule per each locule, 3 style, free to the distal half, stigma obtuse. Schizocarps 5-7 mm long, winged, pubescent, obovate, with pappilose trichomes simple, fructiferous pedicel 2-3 mm long. Seeds 2.5-3 mm long, obovate, brown.

Selected examined material: Aiuaba, 06°43’09’’S, 40°16’48’’W, 9.IV.1997, fl. and fr., L.W. Lima-Verde 620 (EAC 43717). Caucaia, 03°44’10”S, 38°39’11”W, 11.V.2005, fl., M. Oliveira & A. Galileu 1725 (UFP). Crateús, 28.IV.2007, fl. and fr., L.P Amaral Neto et al. 85 (EAC). Irauçuba, 03°44’46”S, 39°46’59”W, 21.IV.2001, fl. and fr., G.B. Oliveira (EAC 31804). Penaforte, Sítio Baixio dos Couros, 07°48’45”S, 39°04’32”W, 15.II.2011, fl. and fr., A.L. Alves 30 (HVASF). Quixadá, Reserva Particular do Patrimônio Natural Fazenda Não Me Deixes, 8.V.2000, fl. and fr., R.C. Costa (EAC 32021). Quixeramobim, Assentamento Vista Alegre, 22.III.2014, fl. and fr., L.Y. Oliveira 149 (CEN). Santa Quitéria, 04°10’09”S, 39°54’36”W, 14.V.2016, fl., I.S.A. Cardins 187 (IPA). Sobral, Fazenda Macapá, 20.V.1989, fl. and fr., A. Fernandes (EAC 16651).

Crumenaria decumbens is distinct from other Rhamnaceae species occurring in Ceará by its herbaceous decumbent habit, leaves highly developed in relation to other taxa of the genus, inflorescence umbelliform, pauciflorous, usually with one to three flowers, and schizocarps obovate with papillose trichomes.

Crumenaria decumbens is found only within the Caatinga domain, in the states of Alagoas, Bahia, Ceará, Paraíba, Pernambuco, Piauí, Rio Grande do Norte, and in northern Minas Gerais (Lima et al. 2020). It has been recorded in nine municipalities in Ceará, occurring preferentially in Steppic Savanna, but also in the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest) and Semideciduous Seasonal Forest. The species has been recorded in the Fazenda Não Me Deixes Private Natural Heritage Reserve.

The species was flowering and fruiting in February and May.

Figure 2
a-d. Colubrina cordifolia - a. branch with buds and fruits; b. leaf details; c. monoclinous flower; d. fruits. e-h. Colubrina glandulosa - e. branch with buds and fruits; f. leaf details; g. monoclinous flower; h. fruits. i-j. Crumenaria decumbens - i. branch with buds and fruits; j. fruits. (a-d. A.S.F. Castro 1517; e-h. A.S.F. Castro 689; i-j. R.C. Costa (EAC 32019).

GouaniaJacq., Select. Stirp. Amer. Hist.: 263. 1763.

Lianas sarmentose, unarmed; branches cylindric or subangular, velutinous or pubescent; tendrils axillary at the base of inflorescences, velutinous or pubescent. Stipules lateral, entire or lobed, velutinous to glabrescent. Leaves simple, alternate, peciolate, ovate or elliptic, apex acute, acuminate or obtuse, base acute, cordate, subcordate or obtuse, margin serrate and/or entire, each ridge ending in a conspicuous gland, glabrous or pubescent, membranaceous or chartaceous; venation actinodromous. Inflorescences paniculiform, axillary, densiflorous. Flowers monoclinous and e diclinous (staminate), 5-merous; sepals triangular, patent, sometimes erect; petals convolute or cuculate; 5 stamens, filaments laminar, anthers ovate or subrounded; nectariferous disk membranaceous, glabrous or pubescent on the proximal margin; ovary inferior, 3-carpelar, 3-locular, one ovule per locule, 3 style, free or livres or partially connate. Schizocarp 3-winged, mericarp with logitudinal wings, velutinous to glabrescent. Seeds obovate to elliptic, brown.

Gouania blanchetianaMiq., Linnaea 22: 797- 798. 1849.

Figs.1a; 3a-c

Lianas; branches cylindric, pubescent; tendrils pubescent. Stipules 3-5 mm long, lobed, pubescent. petiole ca. 1 cm long. Leaves 4.5-8.5 × 2.5-5 cm, ovate to elliptic, base cordate to obtuse, apex acuminate, margin serrate, chartaceous, adaxial surface and abaxial surface pubescent, glands marginal pubescent at apex. Flowers 4-4.5 mm long, pubescent; pedicel ca. 2 mm long; sepals 1-1.2 m long, petals ca. 1 mm long, convolute; stamens ca. 1.4 mm long, anthers ovate to subrounded; nectariferous disk pubescent, prominent on the proximal margin; ovary 1-1.5 mm wide, obovate; style 1-1.2 mm long, connate in the proximal half. Schizocarp 8-10 mm long, glabrous to glabrescent, wings 4-5 mm wide; fructiferous pedicel 3.5-4 mm long. Seeds 3-3.5 mm long, obovate.

Selected examined material: Baturité, 1860, fl. and fr., F.F. Allemão & M. Cysneiros 315 (R). Crato, Macaíbas, 27.VII.2001, fr., E.R. Silveira (EAC 30842). Guaramiranga, subida da Serra, 1.I.1996, fr., A.S.F. Castro 83 (EAC). Ibiapina, Planalto da Ibiapaba, 03°53’05”S, 40°53’42”W, 27.XII.2013, fl. and fr., E.B. Souza et al. 2947 (EAC). Maranguape, Serra de Aratanha, 14.VI.1996, fl., A.S.F. Castro 198 (EAC). Pacoti, Sítio Olho d’Água dos Tangarás, 04°14’07”S, 38°54’59”W, 17.XI.2015, fl., L.W. Lima-Verde (EAC 59677).

Gouania blanchetiana is distinct from other Rhamnaceae species occurring in Ceará by having branches cylindric, pubescent to glabrescent; leaves chartaceous, stipules lobate, and nectariferous disk pubescent along the proximal margin.

The species have a Neotropical distribution, ranging from northern South America to southeastern Brazil, in French Guiana, Suriname, Venezuela, Ecuador, and Columbia (GBIF 2021). In Brazil, Gouania blanchetiana is distributed in four northern states (Amazonas, Amapá, Pará, Tocantins) and in all states in the northeastern and southeastern regions (Lima et al. 2020). The species has been recorded in six municipalities in Ceará, in Semideciduous Seasonal Forest and Dense Ombrophilous Forest.

The species was collected with flowers in April, November, and December, and with fruits in January, July and December.

The popular name is cipó-de-caçuá.

Gouania colurnifoliaReissek, Fl. bras. 11(1): 107. 1861.

Figs.1a; 3d-f

Lianas; branches subangular, velutinous; tendrils velutinous. Stipules 7-8 mm long, entire, velutinous. Petiole 0.5-1 cm long. Leaves 4-8 × 3-6.5 cm, discolorous, ovate, base subcordate, apex obtuse to acute, margin entire on the proximal half and serrate on the distal half, chartaceous, adaxial surface velutinous to pubescent, abaxial surface velutinous, glands marginal glabrous. Flowers 2-3 mm long, velutinous; pedicel 0.7-1 mm long; sepals ca. 1 mm long; petals ca. 1 mm long, cucullate; stamens ca. 1 mm long, anthers ovate; nectariferous disk glabrous, distal margin lobate; ovary ca. 1 mm wide, obovate, style ca. 0.7 mm long, free except in the base. Schizocarp 0.8-1 cm long, velutinous, wings 1-2 mm wide; fructiferous pedicel 0.6-1 mm long, velutinous. Seeds 3-4 mm long, obovate.

Selected examined material: Brejo Santo, 07°34’49”S, 38°53’30”W, 17.III.2010, fl. and fr., D. Araújo 1398 (HVASF). Caucaia, 29.IV.1998, fl., R.C.M. Dourado (EAC 26336). Chaval, pedra da Carnaúba, 03°02’58”S, 41°15’17W, 10.VI.2016, fr., E.B. Souza et al. 4271 (EAC, HUEFS). Cratéus, Reserva Particular do Patrimônio Natural Serra das Almas, 8.V.2002, fr., F.S. Araújo & L.C. Girão 1577 (EAC). Crato, Prov. Ceará, 07°14’03.8”S, 39°24’33.1”W, X.1838, fl., G. Gardner 1523 (NY). Graça, 03°57’24”S, 40°49’13”W, 18.VI.2017, fr., F.F. Araújo 242 (EAC, HUEFS). Novo Oriente, Planalto da Ibiapaba, 13.VII.1991, fr., F.S. Araújo 487 (EAC). Sobral, Serra da Meruoca, 21.VI.2003, fr., E.R. Silveira (EAC 32538). Tianguá, subida da Serra, 03°40’00”S, 40°56’39”W, 7.VI.2012, fr., M.I.B. Loiola et al. 1909 (EAC). Ubajara, Jaburuna, Planalto da Ibiapaba - Sul, 03°51’16”S, 40°55’16”W, 21.VII.1994, fr., F.S. Araújo 22715 (UEC).

Figure 3
a-c. Gouania blanchetiana - a. branch with inflorescences and fruits; b. stipule; c. fruits. d-f. G. colurnifolia - d. branch with inflorescences and fruits; e. stipule; f. fruits. g-i. G. polygama - g. branch with inflorescences and fruits; h. stipule; i. fruits. j-l. Rhamnidium molle - j. branch with fruit; k. stipule; l. fruits. (a-c. E. Silveira (EAC 39433), L.W. Lima-Verde (EAC 59677); d-f. F.F. Araújo 242, M.I.B. Loiola et. al. 1909; g-.J.C.M.S.M. Sobczak 595, A. Fernandes (EAC 48575); j-l. A.M. Miranda 5336).

Gouania colurnifolia may be confused with G. polygama, as both species have branches subangulous and velutinous; G. colurnifolia, however, has chartaceous leaves (vs. membranaceous), a glabrous nectariferous disk (vs. pubescent along the proximal margin), and fruits velutinous (vs. glabrescent).

The species is distributed only in South America; occurring in Brazil, Guyana, and Venezuela (Lima & Giulietti 2006). The species occurs in northern and northeastern Brazil (Lima et al. 2020) and has been recorded in 10 municipalities in Ceará in the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest), Dense Ombrophilous Forest, Steppic Savanna, and Vegetation under Fluvial and/or Lacustrine Influence. It has been recorded only in the Serra das Almas Private Natural Heritage Reserve.

The species was collected with flowers in March, April and December, and fruits in March, May, June and July.

Gouania polygama (Jacq.) Urb, Symb. Antill. (Urban). 4(3): 378-379. 1910.

Figs. 1a; 3g-i

Lianas; branches subangular, velutinous; tendrils velutinous. Stipules 6-8 mm long, entire, velutinous. Petiole 0.8-1.5 cm long. Leaves 5-9 × 3-5 cm, elliptic, apex acute to acuminate, base obtuse to acute, margin serrate, membranaceous, adaxial surface pubescent to velutinous, abaxial surface velutinous, glands marginal glabrous. Flowers 2-4 mm long, velutinous; pedicel ca. 1 mm long; sepals ca. 1 mm long; petals ca. 1 mm long, cucullate; stamens ca. 1 mm long, anthers ovate; nectariferous disk pubescent along the proximal margin, margin proximal lobate; ovary 1-1.5 mm wide, obovate to elliptic, style ca. 0.8 mm long, connate in the proximal half. Schizocarp 0.8-1 cm long, pubescent except in the wings, wings 4-5.5 mm wide; fructiferous pedicel 1-1.5 cm long. Seeds 3-4 mm long, elliptic.

Selected examined material: Crato, 07°14’03”S, 39°24’33”W, 6.VIII.1986, fl., V.C. Lima 271 (IPA). Fortaleza, Barra do Ceará, 6.VII.1960, fl., L. Almeida (EAC 2002). Guaramiranga, Morro Alto Redondo, 10.VIII.1993, fr., M.R.L. Oliveira (EAC 21355). Meruoca, Santo Antônio, Serra da Meruoca, 8.V.1978, fl., A. Fernandes (EAC 48575). Pacoti, 04°09’49”S, 38°52’07”W, 30.IV.2017, fl. and fr., J.C.M.S.M Sobczak (EAC 60611). São Gonçalo do Amarante, 15.V.2011, fl., A.S.F. Castro (EAC 49130). Ubajara, entrada do Parque Nacional de Ubajara, 03°50’17”S, 40°53’53”W, 26.IV.2012, fl., M.I.B. Loiola et al. 1546 (EAC).

Gouania polygama is a remarkable species, characterized by having membranaceous leaves, nectariferous disk pubescent along the proximal margin, and fruits pubescent, except the wings.

Gouania polygama ranges from Mexico to southern Brazil (Lima & Giulietti 2006). The taxon is distributed in all Brazilian states having Amazonia, Cerrado, or Atlantic Forest phytogeographic domains (Lima et al. 2020). The species has been recorded in seven municipalities in Ceará state, in the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest), Semideciduous Seasonal Forest, and Dense Ombrophilous Forest. The species has been collected in only one Conservation Area in Ceará, the Ubajara National Park.

The species was collected with flowers in April and August, and with fruits in August.

The popular name is jacarei.

RhamnidiumReissek, Fl. bras. (Martius) 11(1): 94, t. 31 (1861).

Rhamnidium molleReissek in Mart., Fl. bras. 11(1): 95. 1861.

Figs. 1a; 3j-l

Shrubs or trees 4-6 m, unarmed; young branches velutinous, adult branches glabrescent, lenticellate. Stipules ca. 2 mm long, intrapetiolar, velutinous, deciduous. Petiole 2-4 mm compr., velutinous. Leaves 4-10 × 1.5-3.5 cm, simple, opposite or subopposite, elliptic to oblong, base obtuse, apex acute to obtuse, margin revolute, membranaceous, adaxial surface pubescent, shiny, abaxial surface velutinous with trichomes whitish and glands dark punctiform; venation eucamptodromous. Thyrse densiflorous, axillary, velutinous. Flowers 2-4 × 2-3.5 mm, monoclinous, velutinous, 5-merous; pedicel 3-6 mm long; sepals ca. 2 mm long, erect; petals ca. 1 mm long, cucullate; unguiculate petal ca. 0.2 cm long; 5 stamens ca. 1.5 cm long, anthers oblong; ovary ca. 1 mm wide, elliptic, superior, 2-carpelar, 2-1-locular, 2 ovules; 2 style ca. 0.8 cm long, connate, stigma oblique. Fruits non-winged. septicidal capsule, globose, glabrous or glabrescent. Seeds obovate or subespherical, arillate.

Drupe 0.8-2 × 0.4-1 cm, ellipsoid, glabrous, green when imature, vinaceous when ripe; fructiferous pedicel 3-5 mm long.

Selected examined material: Fortaleza, mata do Diogo-Cocó, 14.XI.1954, fl., A. Ducke (EAC 1018). Maranguape, Serra de Maranguape, 1.XII.1955, fl., A. Fernandes & A. Lima (EAC 1542).

Additional examined material: BRAZIL. ALAGOAS: Água Branca, RVS do Craunã e do Padre, 09°15’53.5”S, 37°53’15.2”W, 5.II.2014, fr., M.C.S. Mota et al. 12349 (MAC). BAHIA: Bom Jesus da Lapa, 13°15’32”S, 43°25’11”W, 10.II.2000, fr., L.P. de Queiroz et al. 5804 (HUEFS). PARAÍBA: São José dos Cordeiros, RPPN Fazenda das Almas, 07°28’14”S, 36°53’53.6”W, 11.III.2007, fl., M.R. Barbosa et al. 3150 (JPB). PERNAMBUCO: Custódia, 08°05’15”S, 37°38’35.2”W, 8.XII.1988, fl. and fr., M.J.N. Rodal & E.M.N. Ferras 51859 (UEC). RIO GRANDE DO NORTE: Jucurutu, RPPN Stoessel de Britto, 06°02’02”S, 37°01’13”W, 20.XII.2007, fl., A.A. Roque 379 (JPB). SERGIPE: Poço Verde, 10°42’28”S, 38°10’58”W, Fazenda Santa Maria da Lage, 16.XI.2010, fl., E.V.R. Ferreira et al. 217 (ASE). PIAUÍ: Palmeira do Piauí, Rod. PI-130, 08°43’37”S, 44°14’09”W, 27.XI.2005, fl., A.M. Miranda 5336 (MAC 53902).

Rhamnidium molle is characterized by having leaves membranaceous and bifacial, with the adaxial surface shiny and abaxial surface velutinous, with trichomes whitish, punctiform glands, and inflorescences in thyrses.

Rhamnidium molle is endemic to northeastern Brazil, occurring in the states of Bahia, Ceará, Paraíba, Pernambuco, Piauí, and Rio Grande do Norte in the Caatinga phytogeographic domain (Lima et al. 2020). Only two collections, made in the 1950s, are known from Ceará, in the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest), and Semideciduous Seasonal Forest.

The species was collected flowering and fruiting in November and December.

The popular names are mussanga, mussananga, viuvinha.

Sarcomphalus P.Browne, Civ. Nat. Hist. Jamaica: 179. 1756.

Shrubs or trees, spinescent; branches thicks, sinuate or slender; spines straight, stout or slender. Stipules lateral, ovate, oblong or lanceolate. Leaves simple, alternate, petiolate, ovate to elliptic, base cordate, rounded, obtuse or acute, apex acuminate or acute, margin serrate, plane or ondulate, membranaceous or chartaceous to coriaceous, glands absent; venation acrodromous, the two arched or straight side veins. Inflorescences in thyrse, axillary, congested or laxous. Flowers monoclinous or diclinous (staminate), 5-merous; sepals greenish, deltoid, patent; petals yellow- greenish; unguiculate petal long, laminar; stamens reflexed, filament laminar, anthers ovate; nectariferous disk slender, slightly sulcate; ovary superior, glabrous, 2-3-carpelar, 2-3-locular, 2-3 ovules, 1 ovule per locule; style glabrous, free in the distal half or only at the apex. Fruits non-winged, drupe, globose or ellipsoid. Seeds 1-2 ovate.

Sarcomphalus joazeiro (Mart.) Hauenschild, Taxon 65(1): 56. 2016.

Figs. 1b; 4a-e

Trees 4-10 m; branches thicks, glabrous to glabrescent, lenticellate; spines 1-2 cm long, straight, stout. Stipules 1-1.7 mm long, lanceolate. Petiole 0.5-1 cm long. Leaves 3-7.5 × 3-6 cm, ovate to elliptic, base cordate to obtuse, apex acuminate to acute, margin serrate, plane, membranacenous (when young) and chartaceous to coriaceous (at maturity). Thyrse congested, 10-30 flowers per inflorescence. Flowers 3-6 mm long, monoclinous; pedicel 1.5-3.5 mm long; sepals 1.1-1.5 mm long, deltoid; petals 1-1.5 mm long, conchiform; nectariferous disk slender; ovary ca. 1 mm wide, glabrous, globose, 2-carpelar, 2-locular, style free at the distal half. Flowers staminate with styloid free and erect in the distal half. Fruits 1-2 cm long, globose, glabrous, lenticellate; fructiferous pedicel 3-4.5 mm long.

Selected examined material: Acarape, 04°13’26”S, 38°42’28”W, 28.IX.2020, fl., L.M. Sousa 22 (EAC). Aiuaba, Estação Ecológica de Aiuaba, 10.IV.2014, fr., C. Lima & T. Renato (EAC 56036). Antonina do Norte, 06°46’30”S, 39°59’21”W, 3.III.2015, fl., F.F.S. Sousa 32 (JPB). Apuiarés, 12.XI.2011, fl., A.S.F. Castro 2555 (EAC). Aquiraz, trilha das Sucurujubas, 03°58’28”S, 38°16’43”W, 15.I.2016, fr., A.P Negreiros et al. 15 (EAC). Aracati, 04°33’43”S, 37°46’12”W, 23.X.2020, fl., L.M. Sousa 29 (EAC). Aracoiaba, 04°22’23”S, 38°48’40”W, fl., 22.I.2021, M.I.B. Loiola 2854 (EAC). Arneiroz, 11.IV.2016, fr., A.M.C. Araújo 4 (EAC). Assaré, 06°52’28”S, 39°52’30”W, fl., D.A. Ribeiro (HCDAL 8346). Aurora, estrada de barro, 15.I.2008, fl., A.M. Miranda et al. 5605 (ALCB, HST). Barbalha, margem do rio Oití, 22.X.1965, fl., J.S. Sobrinho 115 (IPA). Barro, Pitombeira dos Luiz, 07°12’32”S, 38°52’01”W, 12.II.2015, fr., A.P. Fontana et al. 9027 (HUEFS). Baturité, 10.III.2010, fr., A.M.M. Carvalho (EAC 46859). Beberibe, 04°10’48”S, 38°07’51”W, 23.X.2020, fl., L.M. Sousa 27 (EAC). Brejo Santo, Sítio Ipueiras, Chapada do Araripe, 07°28’54”S, 39°01’47”W, 29.XI.2017, fl. and fr., J.C. Andrade (HCDAL 13346). Canindé, 11.II.1989, fl., M.A. Figueiredo et al. (EAC 17171). Capistrano, Serra de Baturité, 5.VIII.1993, J.B.L.P. Medeiros & F.S. Araújo (EAC 21518). Caridade, Povoado do Pendanga, 04°11’41”S, 38°58’58”W, 29.IX.2009, fl., A.C. Bezerra 86 (EAC). Caririaçu, Parque da Macaúba, 07°02’00”S, 39°17’00”W, 18.IV.2009, fr., A.C.B. Santos et al. (HCDAL 4435). Cascavel, 04°07’51”S, 38°14’09”W, 20.XI.2020, fl., L.M. Sousa 30 (EAC). Caucaia, 03°46’48”S, 38°42’00”W, 21.X.2013, fl., W. Batista 13 (EAC). Cratéus, Reserva Particular do Patrimônio Natural Serra das Almas, 27.II.2002, fr., F.S. Araújo & S.F. Vasconcelos 1354 (EAC). Crato, 7°14’19”S, 39°24’58”W, 18.IV.2012, fl. and fr., F.N. Bezerra et al. 01 (HCDAL). Fortaleza, Parque Estadual do Cocó, 03°74’51”S, 38°48’63”W, 13.XII.2019, fl., F.F.S. Lopes & S.M. Morais (EAC 64241). Guaiúba, 04°02’24”S, 38°38’13”W, 20.XI.2020, fl., L.M. Sousa 38 (EAC). Ibaretama, Fazenda Triunfo, 04°44’34”S, 38°45’14”W, 27.III.2012, fl. and fr., A. Uhlmann 569 (FURB). Ibiapina, 03°55’24”S, fl., A.S.F. Castro 2573 (EAC). Iguatu, Reserva Particular de Patrimônio Natural da Fazenda Trussu, 06°21’34”S, 39°17’55”W, 15.I.2018, fr., P.H.G. Bezerra & B.G. Lima (ESAL 30433). Independência, Escola Família Agrícola Dom Fragoso, 29.III.2014, fl., A.C. Cavalcante 133 (CEN). Ipaumirim, S of Itó, 13.II.1985, fl., H. Gentry 50083 (NY). Ipu, Bica do Ipu, 04°19’20”S, 40°42’38”W, 21.IV.2019, A.S. Sousa 8 (HDELTA). Itaiçaba, 04°40’26”S, 37°49’19”W, 21.X.2020, fl., L.M. Sousa 33 (EAC). Itapajé, 03°41’13”S, 39°35’09”W, 21.VIII.2020, fl., L.M. Sousa 09 (EAC 64546). Jaguaribe, margem da estrada, 10.III.1997, fl., F.S. Cavalcanti (EAC 24728). Jaguaruana, 04°50’02”S, 37°46’51”W, 24.X.2020, fl., L.M. Sousa 32 (EAC). Jardim, Distrito de Jardimirim, 07°36’00”S, 39°12’01”W, 12.XII.2012, fl. and fr., R.A. Silva 2400 (HVASF). Jati, Sítio Santana, 07°42’05”S, 39°00’09”W, 29.I.2013, fl., D.G. Oliveira 879 (HVASFw367). Juazeiro do Norte, Parque Ecológico das Timbaúbas, 07°12’47”S, 39°18’55”W, 13.I.2010, fr., G.C. Alves et al. 04 (HCDAL). Lavras da Mangabeira, 06°45’12”S, 38°57’51”W, 2.XI.2008, fl., A.L. Jorge & J.J. Santana 05 (HCDAL). Mauriti, 07°26’36”S, 38°43’31”W, 4.VIII.2009, fl., J.G. Carvalho-Sobrinho 10 (HVASF). Meruoca, Sítio São Gonçalo, 12.V.2018, fr., A.F.B. Silva 204 (EAC). Milagres, 07°17’52”S, 38°56’26”W, 24.X.2011, fl., C.G. Silva (CSTR 3065). Missão Velha, Área de Proteção Ambiental Cachoeira da Missão Velha, 07°13’21”S, 39°08’38”W, 18.VIII.2011, fl., E. Melo et al. 10212 (HCDAL, HUEFS). Monsenhor Tabosa, margens do Rio Poti, 23.X.1997, fl., A. Fernandes (EAC 25941). Nova Olinda, 07°05’31’’S, 39°40’50’’W, 18.I.2013, fl., D.A. Ribeiro (HCDAL 9836). Ocara, 04°29’27”S, 38°35’49”W, 22.I.2021, fl., M.I.B. Loiola 2859 (EAC). Pacoti, 04°11’37”S, 38°54’26”W, 22.X.2003, V. Gomes et al. 982 (EAC). Paraipaba, Área de Proteção Ambiental Dunas da Lagoinha, 19.X.2003, fl., Djane (EAC 33019, HUEFS 80731). Penaforte, Sítio Cabloco, 07°49’45”S, 39°04’46”W, 12.III.2013, fr., D.G. Oliveira 950 (HVASF). Pentecoste, Fazenda Experimental Vale do Curú, 03°49’06”S, 39°20’19”W, 17.VI.2015, fl., C.C. Oliveira 18 (EAC). Porteiras, 07°31’50”S, 39°07’21”W, 8.X.2018, fl., A.P. Fontana 10404 (HUEFS). Quixadá, Monumento Natural dos Monólitos de Quixadá, 04°58’17”S, 39°00’55”W, 5.IX.2017, fr., E.D. Lozano et al. 3788 (MBM). Redenção, 04°12’57”S, 38°44’07”W, 11.X.2015, fl., J.C.M.S.M. Sobczak 112 (EAC). Russas, 04°56’47”S, 38°73’88”W, 10.XII.2018, fl. and fr., L.Q.V. Braga et al. (EAC 62448). Santa Quitéria, 04°33’16”S, 39°47’47”W, 22.IV.2012, fr., J. Paula-Souza et al. 10757b (SPF). Santana do Cariri, 07°12’15”S, 39°44’05”W, 23.I.2014, fl. and fr., B.M.T. Walter et al. 6604 (CEN, EAC, UFP). São Gonçalo do Amarante, Estação Ecológica do Pecém, 8.XII.2011, fr., R.G. Ferreira (EAC 50533). Sobral, Refúgio da Vida Silvestre Pedra da Andorinha, 04°04’17”S, 39°59’59”W, 8.XI.2017, fl., E.B. Souza 4844 (EAC, HUEFS). Tabuleiro do Norte, Olho d’água da Bica, 05°15’15”S, 38°07’29”W, 11.III.2014, fl., L.M. Versieux 674 (HUEFS). Tauá, 05°51’96”S, 40°32’89”W, 17.V.2015, fr., H.G.A. Loiola (EAC 58097). Umari, 06°38’52”S, 38°42’00”W, 21.VIII.2020, fl., L.M. Sousa 08 (EAC). Viçosa do Ceará, X.1909, fl., A. Lisbôa (INPA 12450).

Figure 4
a-e. Sarcomphalus joazeiro - a. leaf; b. spines; c. monoclinous flower; d. diclinous (staminate) flower; e. fruits. f-j. S. platyphyllus - f. leaf; g. spines; h. monoclinous flower; i. diclinous (staminate) flower; j. fruits. k-o. S. undulatus - k. leaf; l. spines; m. monoclinous flower; n. diclinous (staminate) flower; o. fruits. (a-e. L.M. Sousa & M.I.B. Loiola 01; f-j. L.M. Sousa 40; k-o. L.M. Sousa 18).

Sarcomphalus joazeiro resembles S. undulatus by the overall arrangement of its branches and by fruits lenticellate. Sarcomphalus joazeiro, however, bears leaves that are chartaceous when mature (vs. membranaceous), with margins finely serrate and flat (vs. serrate and undulate), stipules lanceolate (vs. ovate), thyrse congested, 10-30 flowers per inflorescence (vs. lax, 5-10 flowers), and fruits globose (vs. ellipsoid).

Sarcomphalus joazeiro is endemic to northeastern Brazil in the states of Bahia, Ceará, Maranhão, Paraíba, Pernambuco, Piauí, Rio Grande do Norte, and Sergipe in the Caatinga phytogeographic domain (Lima et al. 2020). The species is widely distributed in Ceará, having been recorded in 62 municipalities in the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest), Semideciduous Seasonal Forest, Dense Ombrophilous Forest, Forest Savanna, Steppic Savanna, and Vegetation under Fluvial and/or Lacustrine Influence. It has been collected in 10 Conservation areas in Ceará: the Dunas da Lagoinha Environmental Protection Area, Missão Velha Environmental Protection Area, Aiuaba Ecological Station, Pecém Ecological Station, Quixadá Monoliths Natural Monument, Timbaúbas Ecological Park, Cocó State Park, Pedra da Andorinha Wildlife Refuge, Fazenda Trussú Private Natural Heritage Reserve, and the Serra das Almas Private Natural Heritage Reserve.

The species was collected with flowers from August to March, and with fruits from November to May.

The species is used in popular medicine, ornamental, recovery of degraded areas, wood (Araújo & Agra 2018).

The popular names are joá-mirim, joazeiro, juá-de-boi, juá-de-espinho, juá-fruta, juazeiro, laranja-de-vaqueiro, loquiá.

Sarcomphalus platyphyllus (Reissek) Hauenschild, Taxon 65(1): 57. 2016.

Figs. 1b; 4f-j

Trees 9-15 m; branches sinuate, striate, spinescent; spines 0.8-3 cm long, straight, stout. Stipules 1.5-2 mm long, ovate to oblong. Petiole 0.8-1.6 cm long. Leaves 7-13 × 3.5-7 cm, ovate, apex acuminate to acute, base rounded to obtuse, margin serrate, plane, chartaceous to coriaceous. Thyrse congested, 5-30 flowers per inflorescence. Flowers 4-5 mm long, monoclinous; pedicel 1.5-3 mm long; sepals 1.2-1.6 mm long, deltoid; petals 1.4-1.5 long, conchiform; unguiculate petal 0.9-1 mm long; nectariferous disk slightly sulcate; ovary ca. 1 mm wide, glabrous, globose, 2-3-carpelar, 2-3-locular, style free above distal half. Flowers staminate with styloid erect. Fruits ca. 2 cm long, globose, glabrous, lenticellate; fructiferous pedicel ca. 4 mm long.

Selected examined material: Acarape, 04°13’26”S, 38°42’28”W, 20.XI.2020, fl., L.M. Sousa 40 (EAC). Aquiraz, Área de Proteção Ambiental do Rio Pacoti, 03°83’56”S, 38°40’84”W, 11.X.2018, fl., S.T. Rabelo & M.S.D. Branco 114 (EAC). Canindé, 04°19’12”S, 39°14’24”W, 11.II.2014, fr., W. Batista 238 (EAC). Capistrano, Serra do Vicente, 18.X.1979, fl., E. Nunes & A.J. Castro (EAC 7127). Fortaleza, Campus do Pici, 22.I.2016, fl., G.S. Pinto 203 (EAC). General Sampaio, 6.VIII.1998, A. Fernandes (EAC 26857). Maranguape, Gereraú, 1.VII.2001, fl., A.S.F. Castro 995 (EAC). Meruoca, 31.X.1999, fl., A. Fernandes (EAC 28567). Paraipaba, Área de Proteção Ambiental de Dunas da Lagoinha, 19.X.2003, fl., D.V. Azevedo (EAC 22019). São Gonçalo do Amarante, Pecém, 21.X.2007, fl., M.F. Moro et al. 271 (EAC). Sobral, São José do Torto, 14.XI.2011, fl., A.S.F. Castro 2556 (EAC).

Sarcomphalus platyphyllus is distinct from other species of Rhamnaceae found in Ceará by its large leaves (7-13 × 3.5-7 cm), stipules ovate to oblong, and styles free above distal half.

The species is endemic to Brazil, occurring in the northeastern (Alagoas, Bahia, Ceará, Pernambuco, and Rio Grande do Norte) and southeastern regions (Espírito Santo and Rio de Janeiro) of that country (Lima et al. 2020). It has been recorded in 11 municipalities in Ceará, in the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest), Semideciduous Seasonal Forest, Steppic Savanna, and Vegetation under Fluvial and/or Lacustrine Influence. It has been collected in two Conservation Areas: Pacoti River Environmental Protection Area and the Dunas da Lagoinha Environmental Protection Area.

The species was collected with flowers in January, July, October and November, and with fruits in February.

The popular names are joazeiro, juazeiro.

Sarcomphalus undulatus (Reissek) Hauenschild, Taxon 65(1): 57. 2016.

Figs. 1b; 4k-o

Shrubs or trees 4-7 m; branches slender, brown, glabrous to glabrescent, spinescent; spines 3-4 mm long, straight, slender. Stipules 1.3-2 mm long, ovate. Petiole 0.5-1 cm long. Leaves 5-9 × 3.8- 7 cm, ovate to elliptic, apex acute, base rounded to acute, margin serrate and ondulate, membranaceous. Thyrse laxous, 5-20 flowers per inflorescence. Flowers 4.8-6 mm long, monoclinous; pedicel ca. 2 mm long; sepals 1.2-1.5 mm long, deltoid; petals 1.1-1.5 mm long, conchiform; unguiculate petal ca. 0.8 mm long; nectariferous disk slender, slightly sulcate; ovary ca. 1 mm wide, globose, glabrous, 2-carpelar, 2-locular, style free at the apex. Flowers staminate with filiform styloid. Fruits 1-1.5 cm long, elliptic, glabrous, lenticellate; fructiferous pedicel-0.6 cm long.

Selected examined material: Acarape, 04°13’26”S, 38°42’28”W, 28.IX.2020, fl., L.M. Sousa 23 (EAC). Caucaia, Cumbuco, 8.X.1999, fl., L.Q. Matias 209 (EAC). Crato, Villa do Crato, 07°14’19”S, 39°24’58”W, 1938, fl., G. Gardner 1522 (NY). Fortaleza, 15.X.1999, fl., G.N. Maia (EAC 28561). Iguatu, Sítio Catingueira, 06°18’21”S, 39°05’43”W, 15.III.2017, fr., A.M. Rodrigues (EAC 60248). Quixadá, 28.IX.1992, fl., L.P. Félix (EAC 19846). Redenção, 04°13’33”S, 38°43’50”W, 28.IX.2020, fr., L.M Sousa 18 (EAC). Ubajara, Planalto da Ibiapaba, Parque Nacional de Ubajara, 14.IX.1998, A. Fernandes & E. Nunes (EAC 27499). Umari, 06°38’52”S, 38°42’00”W, 21.VIII.2020, fl., L.M. Sousa 07 (EAC).

Sarcomphalus undulatus is characterized by having leaves membranaceous, with margins serrate and undulate; stipules ovate; thyrse lax, with 5-20 flowers, and fruits ellipsoid. It is similar to Sarcomphalus joazeiro; to differentiate between the species, refer to the comments above concerning the latter taxon.

Sarcomphalus undulatus is endemic to Brazil, being distributed in the central-western, northeastern, and southeastern regions of that country in the Cerrado, Caatinga, and Atlantic Forest phytogeographic domains (Lima et al. 2020). The samples collected in the Federal District and Rio de Janeiro State were probably cultivated. The species was recorded in nine municipalities in Ceará, in the Vegetation Complex of the Coastal Zone (Lowland Semideciduous Forest), Semideciduous Seasonal Forest, Dense Ombrophilous Forest, and Steppic Savanna. It has been collected only in the Ubajara National Park conservation area.

The species was collected with flowers in August and October, and with fruits in March and September.

The species is used as edible, and for forage (Santos 2006).

The popular names are joazeiro, juazeiro, joá mirim.

Acknowledgments

We are grateful for the scholarship awarded by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the first author. To PPGERN/PROAP, for the financial contribution for the field expeditions. LMS is grateful to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), for the schorlaship (Financial Code 001). RTMR to the Pernambuco Research Foundation - FACEPE, for the Postdoctoral scholarship granted (Process BFP-0160-2.03/20); RLSN to FUNCAP by the Postdoctoral scholarship granted (Process PD2-0175-00083.01.01/20); MIBL to CNPq, for the research productivity scholarship granted (Process 308685/2020-2).

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Edited by

7

Area Editor: Dr. Marcelo Trovó

Data availability

Data citations

CNCFLORA - Centro Nacional de Conservação da Flora (2022) Lista Vermelha. Available at <http://www.cncflora.jbrj.gov.br/portal/pt-br/listavermelha> Access on 10 March 2022.

Stevens PF (2001 onwards) Angiosperm Phylogeny Website. Version 14, July 2017 [and more or less continuously updated since] . Available at <Available at http://www.mobot.org/MOBOT/research/APweb/ >. Access on 16 October 2021.

Thiers B (continuously updated) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at <http://sweetgum.nybg.org/science/ih/> Access on 19 February 2021.

Publication Dates

• Publication in this collection
  06 Jan 2023
• Date of issue
  2022

History

• Received
  23 Dec 2021
• Accepted
  28 July 2022