Olacaceae and Schoepfiaceae in eastern Northeast Brazil

Abstract

This study provides descriptions, identification key and illustrations of diagnostic characters, as well as comments on the distribution and habitat of species of Olacaceae and Schoepficeae occurring in the eastern portion of northeastern Brazil, this area includes the states of Alagoas, Ceará, Paraíba, Pernambuco and Rio Grande do Norte. The morphological descriptions are based on samples collected during field expeditions (2017-2019) and analysis of herbarium specimens. Were recorded five species in four genera belonging to the family Olacaceae (Cathedra rubricaulis, Dulacia gardneriana, Heisteria ovata, H. perianthomega and Ximenia americana) and one of Schoepfiaceae (Schoepfia brasiliensis), these species occur mainly in Atlantic Forest domain (Lowland and Montane Forests) are also registered in Caatinga and Cerrado domains. The distribution of D. gardneriana and H. perianthomega was expanded, to the states of Rio Grande do Norte and Paraíba, respectively. The main vegetative characters useful for specific delimitation are presence/absence of armed branches, petiole dorso-ventrally flattened or cylindrical and nerves impressed or flat on the adaxial surface. The presence/absence of staminodes, of a pubescent ovary and hypogynous disc, as well as floral pedicel size and diameter of accrescent calyx in fruits, are the most important reproductive characters for species determination.

Key words:
Atlantic Forest; Caatinga; flora; Santalales; taxonomy

Resumo

Este estudo fornece descrições, chave de identificação e ilustrações dos caracteres diagnósticos, bem como, comentários sobre distribuição e habitat, para espécies de Olacaceae e Schoepfiaceae que ocorrem na porção oriental do Nordeste do Brasil, essa área inclui os estados de Alagoas, Ceará, Paraíba, Pernambuco e Rio Grande do Norte. As descrições morfológicas foram baseadas em amostras coletadas durante expedições de campo (2017-2019), e análise de espécimes de herbário. Foram registradas cinco espécies em quatro gêneros pertencentes à familia Olacaceae (Cathedra rubricaulis, Dulacia gardneriana, Heisteria ovata, H. perianthomega e Ximenia americana), e urna Schoepfiaceae (Schoepfia brasiliensis), essas espécies ocorrem principalmente no domínio da Floresta Atlântica (montanas e de terras baixas), sendo registradas também nos domínios da Caatinga e Cerrado. A distribuição de D. gardneriana e H. perianthomega foi ampliada para os estados do Rio Grande do Norte e Paraíba, respectivamente. Os principais caracteres vegetativos úteis à delimitação específica são, presença/ausência de ramos armados, pecíolo achatado dorso-ventralmente ou cilíndrico e nervura principal impressa ou plana na face adaxial. A presença/ausência de estaminódios, de ovário pubescente e disco hipógino, assim como, tamanho do pedicelo floral e diâmetro do cálice acrescente nos frutos, são os caracteres reprodutivos mais importantes para a determinação das espécies.

Palavras-chave:
Floresta Atlântica; Caatinga; flora; Santalales; taxonomia

Introduction

Based on molecular data, the phylogenetic relationship among the genera of Olacaceae s.l. has been changed (Malécot & Nickrent 2008). In APG III (2009), Schoepfia Schreb, traditionally placed in Olacaceae, was recognized as a separate family, Schoepfiaceae, also included in the order Santalales. Subsequent phylogenetic studies have indicated Olacaceae s.l. as polyphyletic group, from which about seven families could be recognized (Malecot & Nickrent 2008; Nickrent et al. 2010). However, changes in Santalales were avoided by APG IV (2016) and Christenhusz et al. (2015, 2017), that maintained the traditional classification for family, followed also in this study.

Olacaceae and Schoepficeae (Santalales sensu APG IV 2016) are fairly variable in life forms, being recorded as trees, shrubs, lianas and perennial herbs, autotrophic or often hemiparasites of roots (Malécot et al. 2004; Christenhusz et al. 2017). Olacaceae includes 29 genera and 170 species distributed mainly in the tropical region of Africa, Asia and America, growing especially in Lowland Forests (Heywood 1993; Christenhusz et al. 2017). Schoepfiaceae comprises three genera and 58 species distributed in America and Asia (Nickrent et al. 2010; Christenhusz et al. 2017). The Neotropics are cited as the center of diversity for these families with around 50% of their genera and species occurring in this region (Sleumer 1984).

In Brazil, 12 genera and 53 species are recorded to Olacaceae, and the family is widespread in the country with the Amazonian domain as the richest area (38 spp.) (BFG 2018). Schoepfiaceae is represented by four species of Schoepfia, one of them distributed mainly along the Brazilian coast (S. brasiliensis A.DC), two restricted to the state of Mato Grosso (S. lucida Pulle and S. velutina Sandwith) and one restricted to the state of Amazonas (S. clarkii Steyerm), in addition to Schoepfia, the genus Arjona Cav. is also recorded in the southern country, represented by one species (Farroñay et al. 2019; BFG 2018).

The species of both families are characterized by simple and alternate leaves without stipules, mainly bisexual flowers, and drupaceous fruits which can have a persistent, expanded and showy calyx in some genera of Olacaceae, such as Heisteria, Chaunochiton and Aptandra (Sleumer 1984; Heywood 1993; Malécot et al. 2004; Nickrent et al. 2010). The ovary is inferior in Schoepfiaceae but superior in Olacaceae (Sleumer 1984; Barroso et al. 2002).

The taxonomic data for Brazilian species of Olacaceae and Schoepfiaceae are limited to Sleumer (1984), and local floras (Guimarães et al. 1971; Cabral & Agra 1999; Ribeiro et al. 1999; Rodrigues & Rossi 2002; Assis 2004; Meirelles & Fernandes Júnior 2017). Northeastern Brazil is often underestimated in terms of species richness and distribution of several families; the number of species and their distribution in this region have been expanded relative to what had previously been reported (Maciel et al. 2009; Amorim & Alves 2012; Alves-Araújo & Alves 2013; Melo & Alves 2013; Santos & Alves 2013; Costa-Lima & Alves 2015; Maciel et al. 2015; Pessoa & Alves 2015; Gomes-Costa & Alves 2016). Similar results could also be expected for Olacaceae and Schoepficeae.

Thus, this study aims to update knowledge on the taxonomy, phenology, geographic distribution, and indication of occurrence in Conservation Units for species of Olacaceae and Schoepfiaceae in the eastern portion of northeastern Brazil, as well as to provide an identification key and useful illustrations of diagnostic characters to distinguish species.

Materials and Methods

Study area

The eastern portion of northeastern Brazil includes the states of Alagoas, Ceará, Paraíba, Pernambuco and Rio Grande do Norte (Lima et al. 2002). The region is located to the north of the São Francisco River and has an area of approximately 385,000 km², including portions of two phytogeographic domains, the Caatinga and Atlantic Forest (Rizzini 1997; Tabarelli et al. 2006).

In the area, the Atlantic Forest extends from the states of Alagoas to Rio Grande do Norte, with enclaves at higher altitudes (> 600 m alt.) in the northern portion of Ceará (Veloso et al. 1991; Tabarelli et al. 2006). It is mainly distributed along the coast, at elevations ranging from 50 to 800 m (Tabarelli et al. 2006; Melo & Alves 2013). The Atlantic Forest is classified into Lowland Forest (< 100 m altitude), which includes the “tabuleiros” and the “restingas”, Submontane Forest (100–600 m alt.), found to the east of the Serra da Borborema along the foothills, and Montane Forest (> 600 m alt.), which includes the “brejos de altitude” (Veloso et al. 1991; Tabarelli et al. 2006; Thomas & Barbosa 2008).

The Caatinga domain covers most of the study area with annual rainfall below 1,000 mm, where the vegetation presents xeromorphic features such as small, deciduous leaves thorns, succulent habit and therophytic life form (Prado 2003; Fernandes & Queiroz 2018). According to geomorphological variations, two main floristic units are found in this phytogeographical domain: crystalline caatinga, mainly located in the “depressão sertaneja”, where the soils are shallow, clayey and stony, and sedimentary Caatinga, common in the sedimentary basin of the São Francisco River, where the soils are deeper and sandy (Queiroz 2009; Silva et al. 2009; Moro et al. 2014).

Taxonomic treatment

The morphological descriptions were produced based on samples collected during field expeditions, carried out in 2017–2019, as well as on samples from collections of the herbaria ALCB, CEN, EAN, EAC, HB, HST, HUEFS, HUCPE, IPA, JPB, MAC, MUFAL, PEUFR, R, RB, UFP, UFRN, UPCB and images from NY (acronyms according to Thiers, continuously updated). The morphological terminology follows Radford et al. (1974) and Harris & Harris (2000). Protologues, floras and taxonomic revisions (Guimarães et al. 1971; Sleumer 1984; Cabrai & Agra 1999; Ribeiro et al. 1999; Rodrigues & Rossi 2002; Assis 2004; Meirelles & Fernandes Júnior 2017) were also consulted.

In the cases of only a few samples from the study area, additional materials from other Brazilian states were used. Information of habitat, phenology and geographic distribution, were retrieved from specimen labels and are presented for all species from the area. Maps with the geographical distribution of the species were elaborated using the software QGIS v.2.18.6 (QGIS Team 2015).

Results and Discussion

Five species of Olacaceae were recorded from the area, distributed in four genera: Cathedra rubricaulis Miers, Dulacia gardneriana (Benth.) Kuntze, Heisteria ovata Benth., H. perianthomega (Vell.) Sleumer and Ximenia americana L.; and one species of Schoepfiaceae: Schoepfia brasiliensis A.DC.

The richest states in number of species are Alagoas, Pernambuco and Paraíba (four spp. each), followed by Ceará and Rio Grande do Norte (three spp. each). Those three states (Alagoas, Pernambuco and Paraíba) are often the richest in plant diversity in the study area (Melo & Alves 2013; Santos & Alves 2013; Gomes-Costa & Alves 2016).

Regarding geographic distribution, Cathedra rubricaulis, D. gardneriana and H. perianthomega are endemic to Brazil (BFG 2018). Heisteria ovata and S. brasiliensis are widely distributed in South America, while X. americana has a pantropical distribution (Sleumer 1984; MacDougal 2003; Christenhusz et al. 2017; BFG 2018).

The number of species in Olacaceae and Schoepfiaceae for eastern northeastern Brazil has not changed with this study, however, the distribution of some species was updated (Figs. 1-2). The first record of D. gardneriana for Rio Grande do Norte, and of H. perianthomega for Paraíba was identified. This latter species has been cited to Ceará (BFG 2018), however, its distribution is confirmed only for Alagoas, Paraíba and Pernambuco. Heisteria blanchetiana (Engl.) Sleumer was mentioned to Alagoas by Nusbaumer et al. (2015) but no voucher was located in this study to confirm that information.

Figure 1
Geographical distribution of Cathedra rubricaulis, Dulacia gardneriana, Heisteria ovata and Heisteria perianthomega in the eastern portion of Northeastern Brazil.

Figure 2
Geographical distribution of Schoepfia brasiliensis and Ximenia americana in the eastern portion of Northeastern Brazil.

Based on the records of species occurrence some taxa have a restricted local distribution, in general growing only in relatively well preserved sites. Cathedra rubricaulis, for example, is known from only four samples collected more than 50 years ago and not collected recently despite several visits to the same sites. Nevertheless, none of the taxa studied are cited in the Brazilian Red List of Threatened Species (Martinelli & Moraes 2013), many probably due to their larger extent of occurrence, or due to lack of evaluation regarding Conservation Status. However, at least one sample of each species registered here was collected in Conservation Units, evidencing the importance of these areas for the maintenance of local biodiversity (Tab. 1).

Table 1
Species of Olacaceae and Schoepfiaceae registered in eastern northeastern Brazil (Alagoas - AL, Ceará -CE, Paraíba - PB, Pernambuco - PE and Rio Grande do Norte - RN) that occur in Conservation Units (UCs) federal and state, full protection (Ecological Station, National Park, State Park, Biological Reserve, Wildlife Refuge) or sustainable use (Environmental Protection area, National forest, Private Reserve of Natural Patrimony).

Espécies	UCs
Cathedra rubricaulis Miers	PE: State Park of Dois Irmãos
Dulacia gardneriana (Benth.) Kuntze	PB: State Park Mata do Pau Ferro
Heisteria ovata Benth.	CE: National Park Ubajara
Heisteria perianthomega (Vell.) Sleumer	AL: Ecological Station Murici, Biological Reserve Pedra Talhada. PE: Private Reserve of Natural Patrimony Fazenda Tabatinga, Private Reserve of Natural Patrimony Frei Caneca, State Park of Dois Irmãos.
Ximenia americana L.	CE: Environmental Protection area Dunas of Lagoinha, Environmental Protection area Chapada do Araripe, Environmental Protection area cachoeira da Missão Velha, Ecological Station Aiuaba, National forest of Araripe, Wildlife Refuge Pedra da Andorinha. PB: Private Reserve of Natural Patrimony fazenda almas. PE: National Park of Catimbau, State Park Dois irmãos, Wildlife Refuge mata Tapacurá, Private Reserve of Natural Patrimony fazenda tabatinga, Private Reserve of Natural Patrimony Nossa senhora do outeiro de Maracaípe. RN: Private Reserve of Natural Patrimony Garabu, Private Reserve of Natural Patrimony Stoessel de Britto, Private Reserve of Natural Patrimony Mata estrela, State Park Dunas de Natal.
Schoepfla brasiliensis A.DC.	AL: Private Reserve of Natural Patrimony Reserva Gulandim. CE: Private Reserve of Natural Patrimony Serra das Almas. PB: State Park Mata do Pau Ferro, National forest restinga de Cabedelo (known to the local population as amém), Biological Reserve Guaribas. RN: Environmental Protection area do Jenipabu.

Identification key to the species of Olacaceae and Schoepfiaceae in eastern northeastern Brazil

• 1. Branchs often armed; leaf apex apiculate; calyx or hypogynous disk not accrescent in fruits 6. Ximenia americana

• 1’. Branchlets without thorns; leaf apex acute to/or acuminate; calyx or hypogynous disk accrescent in fruits 2

  • 2. Petiole dorso-ventrally flattened; staminodes present; ovary pubescent; fruit apex tomentose 2. Dulacia gardneriana

  • 2’. Petiole cylindrical; staminodes absent; ovary glabrous; fruit completely glabrous 3

    • 3. Main nerve strongly impressed on the adaxial surface; stamens ca. 0.4 mm long; hypogynous disk accrescent, enveloping 1/2 of the fruit 1. Cathedra rubricaulis

    • 3’. Main nerve slightly impressed on adaxial surface; stamens 1.5–5.5 mm long; hypogynous disk absent 4

      • 4. Petals fused forming a tube; stamens 4–5; ovary inferior; calyx involving 11/12 of the fruit when mature 5. Schoepfia brasiliensis

      • 4’. Petals free; stamens 10; ovary superior; calyx patent to fruits when mature 5

        • 5. Pedicel 2–3 mm long; calyx in fruits 7–8 mm long and 10–15 mm diameter 3. Heisteria ovata

        • 5’. Pedicel 0.5–1 mm long; calyx in fruits ca. 20 mm long and 27–40 mm diameter 4. Heisteria perianthomega

1. Cathedra rubricaulis Miers, Ann. Mag. Nat. Hist., ser. 2, 7:458. 1851. Fig. 3a-e Trees, 6–8 m tall. Bark scaly; branches glabrous, no thorns. Petiole 5–11 mm long, cylindrical, slightly canaliculate, not winged, glabrous, longitudinally striate; blades (8–)9.5–14 × 3.5–5 cm, glabrous, narrow-elliptic to oblong, margin entire, apex acute to acuminate, base rounded to obtuse, main nerve strongly impressed on the adaxial and prominent on the abaxial, secondary nerves 8–11, broquidodromous venation. Inflorescences in axillary fascicles, sessile, glabrous, 3–13 flowers, bisexuals, bracts ca. 0.5 mm long, sessile; calyx inconspicuously pentamerous or hexamerous, gamosepal, 1 mm long; corolla 5–6-mera, dialipetal, petals 1.1–1.2 × 0.7–0.8 mm, triangulars to lanceolate, concaves, apex adaxially sericeous; stamens 5–6, ca. 0.4 mm long, staminodes absent, filaments free, anthers basifixed, poricidal; gynoecium 1 mm long, ovary superior, umbonate, glabrous, 2-locular, 2-ovulate, hypogynous disk present, accrescent in fruit. Drupe 12–25 × 14–20 mm, subgloboid, hypogynous disk involved 1/2 of the fruit, apex free, glabrous; calyx accrescent, ca. 4 mm long; bracts at the base of the calyx 1 mm long; pedicel ca. 5 mm long.

Figure 3
a-e. Cathedra rubricaulis – a. branch with flowers; b. detail of the midvein on the adaxial surface; c. inflorescence; d. longitudinal view of the flower, evidencing the sepals, petals, sessile stamens, hypogynous disk and gynoecium; e. fruit. f-k. Dulacia gardneriana – f. branch with flowers and fruits; g. detail of the petiole; h. corolla, evidencing stamens and staminodes; i. gynoecium; j. fruit; k. detail of the tomentose apex. l-q. Ximenia americana – 1. branch with flowers; m. detail of apiculate leaf apex; n. flower; o. gynoecium of a functionally pistillate flower; p. gynoecium of a functionally staminate flower; q. fruit. (a-e. D. Andrade-lima 68-5444, J.G. Jardim 5456; f-k. D. Andrade-lima 57-2840, R.R.F. Xavier 104; l-q. I. Meunier et al. (HST 16079), P.Y. Ojima 112).

Materials examined: ALAGOAS: São Miguel dos Campos, 26.X. 1968, fl., M.T. Monteiro 22823 (PEUFR, RB). PERNAMBUCO: Recife, Areias, 6.X.1949, fl., D. Andrade-Lima 49-334 (IPA); Parque Estadual de Dois Irmãos, 11.X.1968, fl., D. Andrade-Lima 68-5444 (IPA). Sirinhaém, Engenho Lage, 1.XI.1968, fl., D.P. Lira 12618 (HSL, IPA).

Additional material: BRAZIL. BAHIA: Ilhéus/Una, Reserva Biológica de Una, 1.II.2009, fr., J.G. Jardim 5456 (CEPEC).

Cathedra bahiensis Sleumer, cited to Bahia and Espirito Santo (BFG 2018), is the species most similar to C. rubricaulis, however, these two species are distinguished by the pedicel length in the flowers (1.5 mm vs. sessile) and shape of the drupe (oblongoid to rarely obovoid vs. subgloboid).

The genus Cathedra it is recognized morphologically mainly by the calyx and hypogynous disk accrescent in the fruits. The proportion of the hypogynous disk to the fruit and its shape are also important in the delimitation of the species (MacDougal 2003). Comprises five species endemics to South America (Sleumer 1984; Christenhusz et al. 2017). Cathedra rubricaulis is restricted to the Brazilian Atlantic Forest (Sleumer 1984), and in the study area only a few individuals were recorded to Lowland Forests of Alagoas and Pernambuco (Fig. 1). The small number of samples and absence of recent collections may be related to the severe forest fragmentation that has occurred over recent decades, mainly caused by sugarcane monoculture and urban growth (Tabarelli et al. 2005). It is possible that C. rubricaulis no longer exist in the study area.

The flowering and fruiting period from October to February.

2. Dulacia gardneriana Kuntze, Revis. Gen. Pl. 1: 111.1891. Fig. 3f-k Trees, 8–10 m tall. Bark longitudinally striate; branches glabrous, no thorns. Petiole 2–3 mm long, dorso-ventrally flattened, not canaliculate, slightly winged, glabrous, smooth; blades 3.8–7.5 × 1.8–4 cm, glabrous, ovate to lanceolate, margin entire, apex acute, base rounded, attenuate to the petiole, main nerve flat on the adaxial and prominent on the abaxial, secondary nerves 4–7, broquidodromous venation. Inflorescences in axillary racemes, peduncle 3–4 mm long, glabrous, 3–7 flowers, bisexuals, bracts absent, pedicel ca. 3 mm long; calyx incospicuously pentamerous, gamosepal, ca. 0.2 mm long; corolla 5-mera, dialipetal, petals 5.5–6 × ca. 1.5 mm, oblong, base adaxially pubescent; stamens 3, 2–2.5 mm long, staminodes 6, both filaments adnates at the corolla, anthers dorsifixed, rimose; gynoecium ca. 3 mm long, ovary superior, conical, pubescent, 1-locular at apex and 3-locular at base, 1-ovulate at apex and 3-ovulate at base, hypogynous disk absent. Drupe 13–17 × 11–12 mm, oblongoid, apex free, tomentose, apiculate, hypogynous disk absent; calyx accrescent, involving 9/10 the fruit; bracts at the base of the calyx absent; pedicel ca. 5 mm long.

Materials examined: CEARÁ: Serra do Araripe, 1957, fl., G. Gardner (IPA 39199); fl., F. Allemão & M. Cysneiros 170 (R). PARAÍBA: Areia, 17.V.1953, fr., J.C.M. Vasconcelos (EAN 1055); 9.XII.2011, fl., E. Melo 10746 (UFRN); Parque Estadual da Mata do Pau Ferro, 7.VI.2001, fr., E. Cunha (JPB 27466); 8.II.2001, fr., I.S. Nascimento (JPB 26471); 20.XII.1953, fr., G.S.B. Pickel (EAN 1063). Dona Inês, Mata do Caboclo, 20.V.2008, fr., R.R.F. Xavier 104 (EAN). PERNAMBUCO: Timbaúba, Engenho Bela Vista, 4.XII.1957, fl., D. Andrade-Lima 57-2840 (IPA). RIO GRANDE DO NORLE: Ceará Mirim, Fazenda Diamante, 14.III.2012, fr., A.A. Roque 1288 (UFRN).

Besides Dulacia gardneriana, four other species are recorded from northeastern Brazil: D. candida (Poepp.) Kuntze and D. guianensis (Engl.) Kuntze from Maranhão; D. papillosa (Bastos) Sleumer and D. pauciflora (Benth) Kuntze from Bahia (BFG 2018). Dulacia candida is distinguished from D. gardneriana by the apex of the leaves acuminate to long acuminate (vs. acute) and D. guianensis differs by the shape and size of the fruits, (ellipsoid, 20–27 × 15–24 mm vs. oblongoid, 13–17 × 11–12 mm). Dulacia papillosa and D. pauciflora have papillose or pubescent trichomes on the branches, while in D. gardneriana the branches are glabrous or rarely with sparse indument (Sleumer 1984).

The genus is morphologically recognized mainly by its six staminodes and the accrescent calyx that almost completely covers the fruits, just the free apex (MacDougal 2003). Dulacia comprises 13 species restricted to South America (MacDougal 2003; Christenhusz et al. 2017). Dulacia gardneriana is endemic to northeastern Brazil (BFG 2018), and in the study area it is found in Atlantic Forest in Paraíba, Pernambuco and Rio Grande do Norte, mainly in “tabuleiros” and “brejos de altitude” (Fig. 1). It is also recorded from Ceará, in moist forest phytophysiognomies in Chapada do Araripe (Moro et al. 2015). It is popularly known as “pimenta de cotia”.

The flowering and fruiting period from December to June.

3. Heisteria ovata Benth., Hooker's J. Bot. Kew Gard. Misc. 3: 366. 1851. Fig. 4a-d

Figure 4
a-d. Heisteria ovata – a. flowering branch; b. flower; c. internal view of the flower, showing the androecium and gynoecium; d. fruit. e-h. Heisteria perianthomega – e. branch with flowers and fruits; f. inflorescences; g. internal view of the flower, showing the androecium and gynoecium; h. fruit. i-o. Schoepfia brasiliensis – i. flowering branch; j. leaf; k. inflorescence; l. internal view of the flower, showing the androecium; m. gynoecium; n. fruit; o. detail of the fruit apex. (a-d. L.Z. Almeida (EAC 2027), A.S.F. Castro (EAC 28354); e-h. D. Cavalcanti 619, M.T. Monteiro 22704; i-o. A.S.F. Castro 629 (EAC), R.C. Costa 312).

Shrubs or trees, 3–6 m tall. Bark longitudinally striate, round lenticels; branches glabrous, no thorns. Petiole 6–10 mm long, cylindrical, canaliculate, not winged, glabrous, rugose; blades 7.7–10.2 × 2–4.1 cm, glabrous, elliptic, oblong, margin entire, revolute, apex acute to acuminate, base rounded or cuneate, attenuate to the petiole, main nerve flat to slightly impressed on adaxial and prominent on abaxial, secondary nerves 7–10, broquidodromous venation. Inflorescences in axillary fascicles, sessile, glabrous, 12–15 flowers, bisexuals, bracts ca. 0.2 mm long, pedicel 2–3 mm long; calyx pentamerous, gamosepal up to 0.5 mm long, lobus 0.5 mm long, ca. 1 mm long, triangular, apex acuminate; corolla 5-mera, dialipetal, petals 2.5–3 × ca. 1 mm, elliptic, adaxially pubescent; stamens 10, 1.5–2 mm long, staminodes absent, filaments free, anthers basifixed, rimose; gynoecium ca. 1.5 mm long, ovary superior, depressed-globose, glabrous, 3-locular, 3-ovulate, hypogynous disk absent. Drupe 8.5–10 × 5–7 mm, oblongoid, apex apiculate, hypogynous disk absent; calyx accrescent, involving the fruits when immature and patent when mature, 7–8 mm long, diameter 10–15 mm, 5-lobed, coned at base up to ca. 3.2 mm, lobes free ca. 2 × 4.2–7 mm, apex rounded to acute; bracts at the base of the calyx absent; pedicel 5–8 mm long.

Materials examined: CEARÁ: Aquiráz, Serrote da Preaoca, 4.VII. 1999, fl., A.S.F. Castro (EAC 28354). Cascavel, Serra de Mataquiri, 12.VIII.2001, fr., A.S.F. Castro 1017 (EAC). Crateús, Reserva Particular do Patrimonio Natural Serra das Almas, 19.VIII.2003, fr., R.C. Costa 285 (EAC); R.C. Costa 310 (EAC). Fortaleza, 21.X.1960, fr., L.Z. Almeida (EAC 2027). Tianguá, 22.VIII.2004, fr., L.W. Lima-Verde 2961 (EAC). Ubajara, Parque Nacional de Ubajara, 23.IX. 1978, fr., A. Fernandes (EAC 5025).

It differs from H. perianthomega, which also occurs in the study area (Fig. 1), by its longer floral pedicel, 2–3 mm long (vs. 0.5–1 mm long) and fruit with a smaller diameter calyx, 10–15 mm (vs. 21–40 mm). For both it is also important to emphasize that the size of the pedicel is taxonomically important when in flower because it expands during frutification and becomes similar in size.

Heisteria can be recognized by inflorescences in axillary fascicles, persistent and accrescent calyx in the fruits, often patent when mature (Sleumer 1984). The genus is composed of 33 species, which occur almost exclusively in the Neotropical region, except for three African species (MacDougal 2003; Nickrent et al. 2010; Christenhusz et al. 2017). It Heisteria ovata is widely distributed in South America, with records from Bolivia, Brazil, Colombia, Guyana, Peru and Venezuela (Sleumer 1984; MacDougal 2003). In Brazil, it is cited from phytogeographics domains Amazon, Caatinga, Cerrado and Atlantic Forest (BFG 2018). However, in the study area, it is found only in Ceará, in areas of Lowland Atlantic Forest such as “tabuleiros” and “restingas”, Submontane and Montane Forest, and in areas of crystalline Caatinga (Fig. 1).

The flowering and fruiting period is from April to October.

4. Heisteria perianthomega (Vell.) Sleumer, Fl. Neotrop. Monogr. no. 38: 76. 1984. Fig. 4e-h

Trees, 8–20 m tall. Bark longitudinally striate; branches glabrous, no thorns. Petiole 5–11 mm long, cylindrical, canaliculate, not winged, glabrous, rugose; blades 6.5–16 × 2.5–6.5 cm, glabrous, elliptic to oblong, margin entire, revolute, apex acuminate, occasionally subfalcate, base obtuse to rounded, attenuate to the petiole, main nerve flat to slightly impressed on adaxial and prominent on abaxial, secondary nerves 7–12, broquidodromous venation. Inflorescences in axillary fascicles, sessile, glabrous, 7–9 flowers, bisexuals, bracts ca. 0.2 mm long, pedicel 0.5–1 mm long; calyx pentamerous, gamossepal up to 0.3 mm long, lobus ca. 1.5 mm long, ca. 1.8 mm long, lanceolate to ovad, apex acuminate; corolla 5-mera, dialipetal, petals ca. 2 × ca. 0.7 mm, elliptic, adaxially pubescent; stamens 10, 1.5–2 mm long, staminodes absent, filaments free, anthers basifixed, rimose; gynoecium ca. 1 mm long, ovary superior, depressed-globose, glabrous, 3-locular, 3-ovulate, hypogynous disk absent. Drupe 7–11 × 5.5–8.5 mm, ovoid to oblongoid, apex apiculate, hypogynous disk absent; calyx accrescent, involving the fruits when immature and patent when mature, ca. 20 mm long, diameter 27–40 mm, 5-lobed, coned at base up to 4–11 mm, lobes free 11–15 × 11–13 mm, apex rounded to acute; bracts at the base of the calyx absent; pedicel 4–7 mm long.

Materials examined: ALAGOAS: Flexeiras, Fazenda Triunfo, 9.II.2011, fr., R.C. Pinto 112 (MAC); 16.VIII.1968, fr., M.T. Monteiro 22704 (HST). Murici, Estação Ecológica de Murici, 20.XI.2012, fr., M.C.S. Mota & E.C.O. Chagas 11791 (MAC). Quebrangulo, Reserva Biológica de Pedra Talhada, 9.XII.1994, fr., A. Cervi et al. 7280 (NY). São Miguel dos Campos, Fazenda Sinimbú, 17.IX.1968, fr., M.T. Monteiro 22765 (HST, IPA). PARAÍBA: Areia, 9.XII.2011, fr., E. Melo et al. 10767 (HUEFS). PERNAMBUCO: Goiana, Reserva Particular do Patrimônio Natural Fazenda Tabatinga, 14.X.2011, fr., D. Cavalcanti et al. 619 (UFP). Jaqueira, Reserva Particular do Patrimônio Natural Frei Caneca, Mata do Ageró, 20.IX.2011, fl., B.S. Amorim 1079 (JPB, UFP). Recife, Parque Estadual de Dois Irmãos, 13.X.1967, fr., O.C.Lira 83-67 (UFP). São Vicente Férrer, Mata do Estado, 2.XII.2017, fr., D.S. Lucena et al. 835 (HUEFS, JPB, MBML, RB, UFP). Sirinhaém, Engenho Lage, 30.X.1968, fr., D.P. Lima 12613 (HST, IPA).

Among Heisteria recorded in northeastern Brazil, H. blanchetiana, from Bahia, is morphologically similar to H. perianthomega. However, its floral pedicel ranges from 4–6 mm long (vs. 0.5–1 mm long) and fruit with a larger calyx 45–70 mm (vs. 27–40 mm diam.).

Heisteria perianthomega is endemic to Brazil and distributed in the Northeast and Southeast regions (Sleumer 1984; BFG 2018). In the study area, it is found in Alagoas, Paraíba and Pernambuco, from Lowland to Montane Forests including “brejos de altitude” (Fig. 1). The species is often found along perennial or temporary rivers. It is popularly known as “canelinha”.

The flowering and fruiting period from August to February.

5. Schoepfia brasiliensis A.DC., Prodr. [A.P. de Candolle] 14(2): 622. 1857. Fig. 4i-o

Shrubs or trees, 1–6 m tall. Bark longitudinally striate, round lenticels; branches glabrous, no thorns. Petiole 2–5 mm long, cylindrical, canaliculate, not winged, glabrous; blades 4.5–14 × 2.5–4.6 cm, glabrous, lanceolate, elliptic or ovate, margin entire, apex acute to acuminate, base cuneate to rounded, main nerve flat on adaxial and prominent on abaxial, secondary nerves 5–8, broquidodromous. Inflorescences in axillary monocasios, peduncle 1–3 mm long, glabrous or rarely with indument puberulent, 2–4 flowers, bisexuals, distylous, bracts ca. 1 mm long, sessile; epicalyx 2-lobate, 0.8–1 mm long; calyx inconspicuous; corolla 4–5-mera, gamopetal, 5–8 mm long, slightly urceolate, lobus reflexes or rarely erect, tuft of trichomes inserted behind each anther; stamens 4–5, 4–5.5 mm long, staminodes absent, filaments adnate to corolla tube, anthers basifixed, rimose; ovary inferior, 1–1.5 × 1.2–1.7 mm, obconic, glabrous, epigynous disc ca. 1 × 1–2 mm, 1-locular at apex e 3–4-locular at base, 1-ovulate at apex e 3–4-ovulate at base, hypogynous disk absent; longistylous form: stigma 2.5–4 mm long; brevistylous form: stigma ca. 1 mm long. Drupe 7–14 × 4–10 mm, obovoid, apex free, glabrous, hypogynous disk absent; calyx involving 11/12 the fruit; subtended by persistent epicalyx; pedicel ca. 5 mm long.

Materials selected examined: ALAGOAS: Coqueiro Seco, 31.IX.2011, fr., O.J. Pereira et al. 7916 (MAC). Ibateguara, Coimbra, 27.X.2003, fr., M. Oliveira et al. 1438 (MAC). Igreja Nova, Usina Marituba, X.2007, A. Costa 257 (MAC). Inhapi, Serra do Grude, 23.IV.2009, fl., M.C.S. Mota & E.C.O. Chagas et al. 2922 (MAC). Japaratinga, 16.X.2009, fl., A.M. Bastos et al. 110 (MAC). Maceió, Serra da Saudinha, 5.II.2009, fl., M.C.S. Mota & E.C.O. Chagas 1928 (MAC). Marechal Deodoro, Restinga do Leprosário, 13.VII.2007, fl., W.S.R. Ferreira Júnior (MUFAL 3979). São Luís do Quintude, Reserva Particular do Patrimonio Natural Garabu, 21.VIII.2004, fl., R. Lemos et al. 8448 (MAC). Tanque D'Arca, Reserva Particular do Patrimonio Natural Cachoeira, 20.XI.2010, fr., M.C.S. Mota & E.C.O. Chagas 9532 (MAC). Teotônio Vilela, Reserva Particular do Patrimonio Natural Gulandim, 20.VII.2012, fr., I.A. Bayma et al. 2366 (MAC). Traipu, Serra das Mãos, 22.VIII.2010, fr., R.P. Lyra-Lemos et al. 13242 (MAC). CEARÁ: Aquiráz, Preaoca, 22.XII.1998, fr., A.S.F. Castro 629 (EAC). Aratuba, Pico do Mussum, 30.VI.2017, fl., E.C. Tomaz et al. 130 (UFRN). Caucáia, 16.VIII.2009, fl., A.S.F. Castro 2211 (EAC). Crateús, Reserva Particular do Patrimonio Natural Serra das Almas, 20.VIII.2003, fl., R.C. Costa 312 (EAC). Crato, subida de Belomonte, 21.VII.2014, fl., F.C.L. Pinto & E.R. Silveira 51 (ALCB). Fortaleza, BNB do Passaré, 23.VIII.2002, fl., A.S.F. Castro (EAC 32264). Guaramiranga, Sitio S inimbu, 8.VII.2004, fr., V. Gomes & A. Xavier 8071 (EAC). Pacoti, Serra de Baturité, 12.VIII.2009, fl., F.S. Gomes et al. 980 (ALCB, EAC). Santana do Cariri, estrada para Crato, 24.V.2011, fl., E. Melo et al. 9848 (HUEFS). PARAÍBA: Areia, Parque Estadual da Mata do Pau Ferro, 5.X. 1999, fl., M.R. Barbosa 1823 (JPB). Cabedelo, Mata da Amém 17.IX.1999, fr., A.E Pontes 141 (JPB). Itabaiana, fazenda de Aguinaldo Velozo, 9.VIII. 1952, fl., F. Melo (JPB 1999). João Pessoa, Estação da Prata, 27.VII.1989, fl., A.O. Dias (JPB 15777). Mamanguape, Reserva Biológica Guaribas, Área II-Cabeça de boi, 27.XI.2002, fr., A.C. Sevilha & G. Pereira-Silva 2579 (CEN). Mataraca, Milennium Inorganic Chemicals Mineração LTDA, 4.X.2007, fl., P.C. Gadelha Neto et al. 1844 (JPB). Umbuzeiro, 22.VIII. 1952, L. Xavier (JPB 1616). PERNAMBUCO: Brejo da Madre de Deus, Mata da Rita, 4.IX.1999, fr., A.G. Silva & I.M. Nascimento 161 (HUEFS). Buíque, 19.X.2007, fl. and fr., R. Pereira et al. 1066 (HUEFS). Cabo de Santo Agostinho, Área do Projeto Suape, 9.XI. 1977, fl., D. Andrade-Lima et al. 80 (IPA). Igarassu, Usina São José, 4.IX.2007, fl., A. Alves-Araújo 545 (UFP, UPCB). Garanhuns, Alto do Magano, 27.V2011, fl., E. Pessoa (UFP 60605). São Vicente Férrer, Mata do Triunfo, 6.V2006, fl., C.G. Lopes 656 (PEUFR). Taquaritinga do Norte, 11.XI.1983, fl., V.C. Lima et al. (IPA 32337). Triunfo, Sítio Lagoa Nova, 18.VI.1992, fl., E.M.N. Ferraz 176 (IPA). RIO GRANDE DO NORTE: Baía Formosa, Mata Estrela, 10.IX.2011, fl., J.L. Costa-Lima & W.M.B São-Mateus 562 (UFRN). Ceará-Mirim, Fazenda Diamante, 8.II.2014, fl., J. Jardim et al. 6718 (UFRN). Extremoz, Área de Preservação Ambiental Jenipapu, 7.V2011, fl., J.G. Jardim 5966 (UFRN). Natal, 29.VIII. 1992, fr., L.P. Félix 5199 (EAN). Nísia Floresta, 26.VIII.2012, fl., W.M.B. São-Mateus et al. 206 (UFRN). Parnamirim, Fazenda EMPARN, Mata Jiqui, 25.V2015, fr., P.P.A.C. Mello (JPB 62557). Tibau do Sul, praia de Pipa, 6.II. 1984, fl., R. Pereira et al. 233 (UFRN).

Besides Schoepfia brasiliensis, three other species occur in Brazil. Schoepfia velutina Sandwith differs from the others by its branches and leaves with velutinous indument (vs. glabrous in S. clarkii Steyerm, S. lucida Pulle and S. brasiliensis), while S. clarkii Steyerm, S. lucida Pulle and S. brasiliensis are distinguished from each other by corolla size, being 1.8–2 mm, 4–4.5 mm and 5.5–8 mm long, respectively (Sleumer 1984; Farroñay et al. 2019).

Most species in the genus are hemiparasites of roots, characterized morphologically by the presence of an epicalyx with 2–3 lobes on the pedicel of the flowers and fruits, stamens adnate to the corolla tube and calyx almost completely enveloping the fruits (MacDougal 2003). Schoepfia comprises 25 species distributed in Asia (six spp.) and America (19 spp.) (Nickrent et al. 2010; Christenhusz et al. 2017). Schoepfia brasiliensis occurs in Argentina, Brazil and Venezuela. In Brazil, it grows in the phytogeographics domains Amazon, Caatinga, Cerrado and Atlantic Forests (BFG 2018). In the study area it is widespread and found in crystalline and sedimentary Caatinga, as well as, in Atlantic Forest (Lowland to Montane Forests, “restingas”, “tabuleiros” and “brejos de altitude”) and Cerrado in Ceará (Fig. 2). Considerable variation in leaf size and shape was observed, which could be the result of plasticity related to its wide range of habitats.

The flowering and fruiting periods are throughout the year.

6. Ximenia americana L., Sp. Pl. 2: 1193. 1753.

Fig. 3l-q

Trees to shrubs, 2–5 m tall. Bark with lenticels round and spaced; branches glabrous, often armed, thorn 0.5–3.5 cm long. Petiole 3–9 mm long, cylindrical, slightly canaliculate, not winged, glabrous or rarely with simple and spaced trichomes along the canal; blades 2.5–7 (7.5–9) × 1.7–4.1 cm, glabrous, elliptic, oval or ovate, margin entire, apex apiculate, base cuneate to obtuse, main nerve flat to slightly impressed on adaxial and prominent on abaxial, secondary nerves 3–6, broquidodromous venation. Inflorescences in axillary racemes umbellate, peduncle 5–12 mm long, glabrous, 3–7 flowers, functionally unissexuals, bracts absent, pedicel 4–9 mm long; calyx inconspicuously tetramer, gamosepal, ca. 0.5 mm long; corolla 4-mera, dialipetal, petals 7–12 × 1.5–2.5 mm, linear, adaxially villous; stamens 8, 3–10 mm long, staminodes absent, filaments free, anthers basifixed, longitudinal; gynoecium 2–7 mm long, ovary superior, oblongoid, glabrous, 4-locular, 4-ovulate, hypogynous disk absent. Drupe 15–40 × 10–30 mm, subglobose, hypogynous disk absent; no persistent calyx; bracts at the base of the calyx absent; pedicel 5–10 mm long.

Materials selected examined: ALAGOAS: Piaçabuçu, próximo a Potengi, 17.III.1982, fr., R.F. Almeida 187 (MAC). Umbuzeiro, 26.XI.1971, D. Andrade-Lima et al. (MAC 1714). CEARÁ: Aiuaba, Estação Ecológica de Aiuaba, 14.V.1998, N.M. Gerda (EAC 27042). Aquiraz, Trilha das Sucurujubas, 15.1.2016, fl., A.P. Negreiros et al. 23 (EAC). Caridade, Fazenda Feijão, 18.XI.1990, fl., B. Freitas (EAC 22905). Caucaia, Parque Botânico do Ceará, 26.IV.1997, fl., A. Fernandes et al. (UFC 25726). Crato, Chapada do Araripe, 20.XI.2001, fl., F.S. Cavalcante (EAC 31008). Graça, 19.XII.2007, fr., P.M. Teixeira et al. 31 (HUEFS). Granja, Fazenda Recanto, 13.X.1989, fr., F. Cavalcante & E. Nunes (EAC 16242). Guaiúba, Fazenda da UECE, 5.II.2017, fl. and fr., O. Mesquita (EAC 39619). Horizonte, estrada Coluna-Cascavel, 13.XI.2008, fl., J.E. Alves (EAC 43881). Iguatu, 4.III.2013, fr., L.R. Pereira Júnior (EAN 22712); 16.IV.2014, L.P. Félix 14883 (EAN). Independência, estrada para Quiterianópolis, 10.IV.1998, E.B. Sousa (EAN 26394). Maracanaú, Aldeia indígena Pitaguary, 13.X.2011, fr., P. Pantoja (EAC 50435). Missão Velha, 4.I.2009, fr., M.F. Moro et al. 698 (EAC). Pacujá, 20.XII.2007, fr., I.M. Andrade 3111 (HUEFS). Paraipaba, Área de Preservação Ambiental Dunas de Lagoinha, 19.X.2003, fl., D.V. Azevedo (EAC 33020). Pentecoste, Fazenda Experimental, 9.XI.2016, fl., N.C. Rebouças et al. 06 (UFC). Pombal, 15.IX.1953, J. Carneiro (JPB 1654 A). Poranga, 19.IV.2014, E.M. Almeida et al. 1112 (EAN). Quixadá, comunidade São João, 4.II.2010, fr., V. Gomes et al. 1373 (EAC). Senador Pompeu, Serrote do Patu, 18.I.1995, E.B. Sousa et al. (EAC 21906). São Gonçalo do Amarante, Estação Ecológica do Pecém, 12.X.2011, fl., R.G. Ferreira (EAC 49904). Tauá, Bacia do Riacho Carrapateira, 10.XII.2014, fl., A.C. Gomes (57387). Venturoza, Serra da Meruoca, 8.X.2002, fl., A. Fernandes (EAC 32193). PARAÍBA: Cabaçeiras, Sitio Bravo, 18.II.1992, fr., V.L. Nascimento et al. 23 (JBP). Cabedelo, 15.XII.1999, fr., A.F. Pontes 346 (JPB). Campina Grande, 29.IX.1986, fr., A. Fernandes (EAC 14779). Caturité, 20.XII.2012, fl., L.P. Félix 14218 (EAN). Itaporanga, Serra Água Branca, 7.I.1994, fr., M.F. Agra 2512 (EAN). João Pessoa, Falésia de Cabo Branco, 12.XI.1986, fl., C.A.B. Miranda 202 (JPB). Junco do Seridó, 20.XII.2012, L.P. Félix 14220 (EAN). Lucena, 2.XII.1997, fl., R. Pereira et al. 1307 (JPB, IPA). Mamanguape, Tarana, Sema II, 22.XI.1991, fl., L.P. Félix et al. 4572 (EAN). Mataraca, Millennium Inorganic Chemicals Mineração, 4.X.2007, fl., P.C. Gadelha Neto et al. 1861 (JBP). Nazarezinho, Serra do Pico, 9.I.2000, fr., P.C. Gadelha Neto et al. 503 (JPB). Pocinhos, 31.X.2007, fl., P.C. Gadelha Neto et al. 1939 (JPB). Sapé, Inhana, 10.VIII.1991, fl., O.T. Moura 626 (JPB). São José dos Cordeiros, Reserva Particular do Patrimonio Natural Fazenda Almas, 24.I.2008, fr., M.C. Pessoa et al. 267 (JPB). São Sebastião de Lagoa de Roça, 29.III.2013, L.P. Félix 14230 (EAN). Sousa, Sítio Lamarão, 13.VI.1996, H.M. Moreira 36 (JPB). PERNAMBUCO: Águas Belas, Mata do Paredão, 13.II.2008, G.T. Soldati et al. 160 (IPA). Arcoverde, Serra das Varas, 22.II.2006, fr., R. Pereira et al. 2658 (IPA). Buíque, Parque Nacional Serra do Catimbaú, 26.VI.2007, R.M. Santos et al. 1630 (HUEFS). Exu, Serra do Araripe, 30.IX.2013, fl., M.E. Saraiva 194 (EAC); Fazenda Taboquinha, 19.I.2006, fr., I. Meunier et al. (HST 16079). Goiana, Reserva Particular do Patrimonio Natural Fazenda Tabatinga, 28.XII.2010, fl., A. Melo et al. 717 (IPA, UFP). Igarassu, Usina São José, 26.XII.2008, fl., A. Alves-Araújo & B. Amorim 1086 (UFP); 10.XII.2007, fl., P.Y. Ojima 112 (UFP). Ipojuca, Área do Projeto Suape, 23.XI.1977, fl., A. Lima et al. 100 (IPA). Itamaracá, 31.V.1994, P. Coelho(IPA 55547). Moreilândia, 19.I.2006, fr., F.S. Cavalcanti (EAC 38605). Pombos, Assentamento Cervo Mendes, 1.II.2008, fr., L.R. Silva 181 (HST). Recife, 23.XI.1963, fl., S Tarares 869 (HST). Serra Talhada, Serra da Carnaubeira, 22.V.1971, E.P. Heringer (IPA 19707). São Lourenço da Mata, Refúgio de Vida Silvestre Mata Tapacurá, 11.XII.2013, fl., M.S. Sobrinho 443 (UFP). Vitória de Santo Antão, Engenho Pombal, 25.XI.1997, fl., A. Laurênio 678 (UFRN). RIO GRANDE DO NORTE: Alto dos Rodrigues, Comunidade Barrocas, 30.V.2010, D.F.Torres et al. 34 (UFRN). Baía Formosa, Reserva Particular do Patrimonio Natural Mata da Estrela, 26.IV.2015, fl., P.P.A.C. Melo (JPB 62574). Ceará-Mirim, Dunas de Mariú, 11.II.2016, fr., E.O. Moura et al. (UFRN 20388). Cerro Corá, Conglomerado RN 76 4-7-2, 10.IX.2014, fl., A.F. Silva et al. 103 (UFRN). Extremoz, 28.XI.2013, fl., O.J. Pereira 8001 (UFRN). Goianinha, Fazenda Nossa Senhora do Carmo, 12.II.2011, J.L. Costa-Lima et al. 383 (EAN, UFRN). Jucurutú, Reserva Particular do Patrimonio Natural Stoessel de Brito, 22.XII.2017, fl., A.A. Roque 340 (JPB). Maxaranguape, Maracajaú, 22.XII.2016, fr., D.S. Lucena & M. Alves 861 (UFP). Natal, 31.X.1992, fl., L.P. Félix 5447 (EAN). Parnamirim, Riacho Águas Vermelhas, 21.IX.2005, A. Ribeiro et al. 166 (UFRN). São Miguel do Gostoso, Novo Horizonte, 14.V2007, M.I.B. Loiola et al. 1191 (UFRN).

Besides Ximenia Americana, two other species occur in Brazil. Ximenia coriacea Engl. differs from the others by presenting flowers solitary or in axillary fascicles (vs. racemes or cymes in X. americana, subumbel in X. intermedia (Chodat & Hassl.) De Filipps (Sleumer 1984).

The genus is characterized morphologically mainly by the presence of armed branches, apiculate leaf apex and petals with long trichomes on the adaxial surface (MacDougal 2003). Ximenia is composed of 10 species of roots hemiparasites with a pantropical distribution (Nickrent et al. 2010; Christenhusz et al. 2017). Ximenia americana is widely distributed in Brazil (BFG 2018). In the study area it grows in all states, in areas of crystalline and sedimentary Caatinga, as well as in Atlantic Forest but it is most common in Lowland Forests such as “restingas”, “tabuleiros”, “brejos de altitude” and Cerrado enclaves (Fig. 2). It is popularly known as “ameixa-da-caatinga”, “ameixa-brava” ou “ameixa-de-espinho”. The species differs from the other species of Olacaceae in the study area by its armed branches, and absence of a calyx or hypogynous disk accrescent in the fleshy fruits.

The flowering and fruiting periods are throughout the year, but most fertile specimens were collected from April to October.

Because of its history of use in traditional communities, X. americana is the most widely known species of Olacaceae. It has anti-inflammatory and antimicrobial uses, with proven efficacy against bacteria (Escherichia coli (Migula) Castellani and Chalmers) and Pseudomonas aeruginosa (Schroeter) Migula) and fungus (Candida albicans (C.P. Robin) Berkhout) (Ogunleye & Ibitoye 2003). It is traditionally prepared as teas and infusions of the bark (Brasileiro et al. 2008).

Acknowledgments

To the Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, for the grant awarded to the first author. To the curators and technicians of the visited herbaria, for the space given for the consultation of the botanical collections.

List of exsicates

A Alves-Araújo 1086 (6), 457 (5), 545 (5), 632 (5). A Cervi 7280 (5). AC Sevilha 2579 (5). AJC Aguiar 37 (6). AM Bastos 110 (5). A Costa 257, 528 (5). AG Silva 161 (HUEFS). ASF Castro 1017, EAC 28354, EAC 30078 (3), EAC 32264, 629 (5). AO Dias 01 (5). A Fernandes EAC 5025 (3), EAC 13965, 14779, 25726, 32193 (6). AC Gomes EAC 57387 (6). A Laurênio 678 (6). A Melo 717 (6). AP Negreiros 23 (6). AF Pontes 279, 346 (6), 95, 141, 219 (5). A Ribeiro 166 (6). AA Roque 1288 (2), 340, 1671 (6). A Silva IPA 58817 (6). AF Silva 10, 103 (6). AG Silva 161, 138 (5). BS Amorim 1079 (4). B Freitas EAC 22905 (6). B Pickel 3184, IPA 974, IPA 3685, IPA 3687 (6). CAB Miranda 202 (6). CAM Oliveira 29 (5). C Ferreira IPA 66438 (6). CEB Nobre 01 (5). CG Lopes 656 (5). D Andrade-Lima 49-334, 68-5444 (1), 57-2840 (2), 49-393, 54-1903 (4), MAC 1714, 49-398, 68-5446, 100 (6), 80, 51-938 (5). D Cavalcanti 637 (6). DF Torres 34 (6). DP Lima 12618 (1), 12613 (4). DS Lucena 835 (4), 861 (6). EB Almeida 507 (6). EB Souza EAC 21906, 26394 (6), 2190 (5). ECO Chagas 1928, 2922, 4662, 5900, 9532, 29222 (5). E Cunha JPB 27466 (2). EC Tomaz 130 (5). EMN Ferraz 550 (4), 239, 803 (6), 176, 439, 504 (5). E Melo 10746 (2), 10767 (4), 10220 (6), EAC 31879 (5). EMP Fernando 720 (5). EO Moura 573 (6), 84, 977 (5). EM Almeida 1112 (6). F Cavalcante EAC 16242 (6). F Allemão & M Cysneiros 170 (2). FCL Pinto 51 (5). FF Araújo 91 (6). F Melo JPB 1999 (5). FS Cavalcante 929, EAC 33010, 38605 (6). FS Gomes 980 (5). G Gardner 1957 (2). GC Pereira UFP 45322, IPA 73349 (6). G Teixeira 2886 (4), 2898, 2964 (6). GT Soldati 160 (6). HM Moreira 36 (6). IA Bayama 2303, 2366, 2383, MAC 57084 (5). IM Andrade 3111, 4015, 4028 (6). I Meunier HST 16079 (6). IB Lima 931, 937, 1178 (6), 1001 (5). IS Moreira 168 (5). JAN Souza 464 (6). JCM Vasconcelos EAC 666, 1055 (2). JC Sousa Jr 55 (6). JE Alves EAC 43881 (6). JG Jardim 5456 (1), 6165 (2), 5603 (6), 5832, 5966, 6092, 6718 (5). JL Costa-Lima 383, 1908 (6), 562 (5). JLH Alves UFP 7382 (6). JR Lemos 509 (5), EAC 38235 (6). JS Marques 232 (5). JS Sobrinho 354 (6). J Soares HST 2016 (4), IPA 75026, IPA 75724, PEUFR 15451 (4). LZ Almeida EAC 2027 (3). LMR Melo 136 (6). LA Cestaro 99-0215 (6), 99-0196 (5). LA Pereira 226 (5). LQ Matias 210 (6). LP Félix 4572, 5447, 14218, 14220, 14230, 14883 (6), 2994, 10593, 15138, EAN 7775 (5). LR Pereira Júnior EAN 22712 (6). LR Silva 181 (6). L Xavier JPB 1412 (2), 1137 (6), 1616, 1739 (5). LW Lima-Verde 2961 (3), 1775, 1823, 1879, 3085 (6). MF Agra 0401, 2512 (6). MJG Andrade 375 (5). MR Barbosa 1823, 1854 (5). MA Figueiredo EAC 16469, 426 (6). MOT Menezes 130 (5). MT Monteiro 22704, 22765, 22806, 22823 (4). MF Moro 698 (6). MN Rodrigues 2849 (5). ME Saraiva 194 (6). MIB Loiola 854, 1191 (6), 2567 (5). MS Sobrinho 443 (6). MSC Mota 11791 (4). M Oliveira 1438 (5). MR Oliveira 20984 (5). MC Pessoa 267 (6). MB Sousa 162 (6). NA Albuquerque 642 (6), 463 (5). NM Gerda EAC 27042 (6). NT Amazonas 2005 (5). NT Medonça 86 (5). NC Rebouças 6 (6). OC Lira 83-67 (4). OJ Pereira 8001 (6), O Mesquita EAC 39619 (6). 7916 (5). OT Moura 585, 628, 722, 925 (6). P Coelho IPA 55547 (6). PC Gadelha Neto 244, 985. 1861, 1902, 1939, 2012, 3119 (6), 979, 980, 1229, 1231, 1577, 1578, 1819, 1844 (5). PM Teixeira 31 (6). PPAC Mello 62574 (6), 62557 (5). PV Luetzelburg EAC 25841 (6). PY Ojima 112 (6). P Pantoja EAC 50435 (6). R Coelho 369 (6). RA Pontes 679 (6). RC Costa 285, 310 (3), 312 (5). RC Pinto 112, 243 (5). RF Almeida 187, 513 (6). RM Santos 1630 (6). RG Ferreira EAC 49904 (6). R Lemos 8848 (5), RP Lyra-Lemos 4636, 9904, 11487, 11525, 11535, 12727, 13242 (5). R Pereira 1307, 2658 (6), 233, 1066, (5). RRF Xavier 11, 104 (2). SA Lima 47 (5). S Tavares 869 (6). VGR Cardoso 8 (5). V Gomes 1373 (6), 807-1, 807-5 (5). VC Lima 432 (6), IPA 32337, IPA 32347 (5). VM Mascena C69 (6). VL Nascimento 23 (6). WMB São Mateus 03, 206 (5). WSR Ferreira Júnior MUF AL 3979 (5).

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Edited by

Area Editor: Dr. João Iganci

Publication Dates

• Publication in this collection
  11 June 2021
• Date of issue
  2021

History

• Received
  17 Sept 2019
• Accepted
  19 May 2020