Flora of Espírito Santo: Barnebyoid and Bunchosioid clades (Malpighiaceae)

Barros, Paulo Henrique Dettmann; Almeida, Rafael Felipe de; Dutra, Valquíria Ferreira

doi:10.1590/2175-7860202273013

Abstract

We present the taxonomic treatment of four genera and six Malpighiaceae species from the state of Espírito Santo, Brazil. We analyzed herbarium specimens (BHCB, CRVD, MBML, RB, SPF and VIES) and collected specimens in field expeditions from January 2018 to April 2019. Bunchosia was the richest genus with three species recorded in this state, followed by Barnebya, Heladena, and Thryallis, with a single species each. We present morphological descriptions, identification keys, taxonomic notes, distribution maps, and photographic plates for all species.

Key words Atlantic Forest; Brazil; lianas; Malpighiales; taxonomy

Resumo

Apresentamos o tratamento taxonômico de quatro gêneros e seis espécies de Malpighiaceae do estado do Espírito Santo, Brasil. Analisamos exsicatas de herbários (BHCB, CRVD, MBML, RB, SPF e VIES) e espécimes coletados em expedições de campo entre janeiro de 2018 e abril de 2019. Bunchosia foi o gênero de maior riqueza com três espécies registradas neste estado, seguido por Barnebya, Heladena, e Thryallis com uma única espécie, cada. Apresentamos descrições morfológicas, chaves de identificação, comentários taxonômicos, mapas de distribuição geográfica e pranchas de imagens para todas as espécies.

Palavras-chave Floresta Atlântica; Brasil; lianas; Malpighiales; taxonomia

Introduction

Malpighiaceae comprises 77 genera and 1,300 species mainly distributed in the Neotropical region (Anderson 1981). In Brazil, this family is represented by 46 genera and 588 species recorded in all states of the federation, with 354 species endemic to this country (Almeida et al. 2020). Malpighiaceae is morphologically recognized by the presence of T-Y-V-shaped malpighiaceous hairs (i.e., unicellular hairs with a base and two lateral projections, named branches), petals clawed, and sepals bearing a pair of oil-secreting glands (i.e., elaiophores), with the anterior sepal usually eglandular (Anderson 1981). This family shows a conspicuous conserved floral morphology among all its genera, making its traditional classification heavily relied on leaf and fruit characters (Anderson 1981).

The state of Espírito Santo is entirely covered by the Atlantic Forest biome, comprising several phytophysiognomies such as pioneer formations, semideciduous forests, rainforests, inselbergs, and montane grasslands (Garbin et al. 2017). The Atlantic Forest is one the most diverse and threatened worldwide hotspots for conservation (Tabarelli et al. 2004; Mittermeier et al. 2005). This biome shows only ca. 13% of its original natural cover due to its growing urban population, reducing its natural vegetation to fragments smaller than 50 hectares within pasture, crops or urban centers (Ribeiro et al. 1999; Fundação SOS Mata Atlântica 2019). The state of Espírito Santo is currently the 7^th most diverse state of the federation in plant species with 8.3% of endemic plant species (Dutra et al. 2015). On the other hand, Malpighiaceae is the 15^th most diverse family in plant species in the state of Espírito Santo, with 129 species and 23 genera (Dutra et al. 2015).

Studies on Malpighiaceae taxonomy within the Atlantic Forest of state of Espírito Santo are relatively recent, starting about thirty years ago (Mamede 1984, 1992). For the Atlantic Forest, a synopsis of Malpighiaceae was published by Almeida et al. (2016) and Bunchosia (Almeida & Pellegrini 2016). A checklist of Malpighiaceae species from the state of Espírito Santo was published by Almeida & Mamede (2014), followed by the monographs of Stigmaphyllon (Almeida & Mamede 2016) and Banisteriopsis (Almeida 2020). Additional studies regarding new records, new species, distribution, and taxonomic notes of species occurring in the state of Espírito Santo have also been published over the last twenty years (Amorim 2003; Almeida et al. 2013, 2015, 2018; Almeida & Amorim 2015; Almeida 2017; Francener et al. 2018). And regarding taxonomic revisions, Almeida (2018) presents the monograph of Amorimia and Anderson (2014) described several new species and circumscription for Hiraea from the state of Espírito Santo.

Moving towards completing the taxonomic treatment of Malpighiaceae from the state of Espírito Santo, we present the taxonomic treatment for species of the Barnebyoid and Bunchosioid clades. These lineages were recently recovered by molecular studies in the family (Davis & Anderson 2010; Almeida & van den Berg 2021), being represented in this state by four genera [i.e., Barnebya (Barnebyoid clade), Bunchosia, Heladena, and Thryallis (Bunchosioid clade)] and six species. We present identification keys, morphological descriptions, examined specimens, comments on distribution and taxonomy, distribution maps, and photographic plates.

Material and Methods

We analyzed specimens deposited at the BHCB, CRVD, MBML, RB, SAMES, SPF, VIC, and VIES herbaria, besides additional specimens and type specimens deposited in virtual herbaria (CEPEC, ESA, HUEFS, and NY), such as speciesLink (CRIA 2021) (acronyms according to Thiers, continuously updated). Additional specimens were also collected on field expeditions from 2017 to 2019 and deposited at the VIES herbarium collection. Samples of flowers and/or fruits collected on the field were preserved in 70% alcohol for identification and description purposes. All specimens were analyzed using a stereomicroscope, specialized literature (Niedenzu 1928; Radford et al. 1974; Anderson 1981, 2001, 2005, 2014; Anderson & Gates 1981; Chase 1981; Almeida 2018; Almeida & Pellegrini 2016) and consulting nomenclatural types on virtual herbaria. Geographical distribution data were obtained from the analyzed specimens and the phytophysiognomy classification proposed by Veloso et al. (1991). Maps were elaborated with ArcGis 9.2 (ESRI 2010), with shapefiles obtained from IBGE (2015). Additionally, we used the “Lista Nacional de Espécies da Flora Ameaçadas de Extinção” (CNCFlora 2019) and “Lista das Espécies Ameaçadas do Espírito Santo” (Fraga et al. 2019) to identify threatened species.

Results and Discussion

An identification key for all Malpighiaceae genera occurring in the Atlantic Forest biome can be found in Almeida et al. (2016).

Barnebyoid clade sensu Almeida & van den Berg (2021)

The Barnebyoid clade currently comprises a single genus, Barnebya, and two species endemic to Brazil (Davis & Anderson 2010; Almeida et al. 2020).

1. Barnebya dispar (Griseb.) W.R.Anderson & B.Gates, Brittonia 33(3): 280. 1981. Figs. 1; 4

Figure 1
a-d. Photographic plate of Barnebya dispar – a. flowering branch; b. detail of the abaxial surface of a leaf; c. flower in frontal view; d. winged mericarp in side view. Photographs by P.Sampaio.

Trees, 5–10 m tall; branches glabrous; stipules interpetiolar, 2.3–4.7 mm long, narrowly triangular, deciduous, free. Leaves reduced associated to inflorescences absent; petiole 6–15 mm long, flattened, glabrescent, eglandular; leaf blade 4–8.4 × 3.3–4.1 cm, chartaceous, oblanceolate, base cuneate, margin entire, plane, apex acute to cuspidate, both surfaces glabrous, primary vein abaxially impress, 2-glandular at base. Thyrses of 2-flowered cincinni, 6–25 flowers; main axis glabrous; bracts ca. 1.6 mm long, membrane, triangular, deciduous, eglandular; peduncles 1.3–1.5 cm long; bracteoles ca. 1 mm long, membrane, triangular, deciduous, eglandular. Flowers with pedicels 1–1.2 cm long, glabrous; sepals adpressed to the androecium, ca. 2.4 × 1.6 mm, apex rounded, both surfaces glabrous; elaiophores 2 per sepal, yellow, ca. 3.5 × 1.1 mm; petals yellow, limb obovate, margin fimbriate, glandular; lateral petals with limb ca. 4.5 × 3.4 mm, claws ca. 0.8 × 0.2 mm; posterior petal with limb ca. 4.4 × 2 mm, claws ca. 0.9 × 0.4 mm. Stamens with filaments ca. 2 mm long, connectives glandular covering the posterior part of thecae, thecae glabrous; ovary ca. 2.8 × 2 mm, fusiform, sericeous; styles ca. 2.4 × 0.1 mm, erect, divergent, cylindrical, glabrous; stigma apical, truncate. Mericarps winged, dorsal winged more developed than lateral ones, lateral wings absent, brown when mature; dorsal wing ca. 4.8 × 2.1 cm, glabrous; nut ca. 1.8–1.9 cm long, rugose, glabrescent.

Examined material: Santa Teresa, Estação Biológica de Santa Lúcia, 21.IX.1993, L.D. Thomaz 950 (MBML); 18.VIII.1993, L.D. Thomaz 1043 (VIES).

Additional examined material: BRAZIL. Minas Gerais: Carangola, Fazenda Santa Clara, 5.VIII.2006, fr., A.L.A. Faria 27 (RB). Rio de Janeiro: Nova Iguaçu, estrada para Boa Esperança, 16.I.2002, fl., S.J. Silva-Neto 1624 (RB).

Barnebya dispar is endemic to the Atlantic Forest biome of Brazil, occurring in the states of Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro, and São Paulo (Anderson 1981; Almeida et al. 2020). In the state of Espírito Santo, B. dispar occurs in rainforests, but it has never been collected with flowers and/or fruits in this state. It is also regarded as threatened in the state of Espírito Santo (Fraga et al. 2019) and not threatened in the Atlantic Forest biome (CNCFlora 2019).

Barnebya comprises only two species characterized by being trees of 2–15 m tall; stipules interpetiolar, free, deciduous; leaves alternate; petioles eglandular; base of leaf blades cuneate; thyrses of 2-flowered cincinni; and calyx 10-glandular, glands decurrent onto pedicel (Anderson 1981). In the state of Espírito Santo, Barnebya dispar is differentiated from the remaining species of Malpighiaceae by being the only tree species in this state bearing winged mericarps (personal observation). Additionally, this species only shows two sterile records from the same individual within Santa Lúcia Biological Reserve in the municipality of Santa Teresa. Nonetheless, this individual was not found during field expeditions in the abovementioned conservation unit. This species is only represented by 40 records throughout the Atlantic Forest biome of Brazil, probably due to being a rare canopy tree (personal observation).

Bunchosioid clade sensu Almeida & van den Berg (2021)

The Bunchosioid clade currently comprises three genera (i.e., Bunchosia, Heladena, and Thryallis) in the state of Espírito Santo, with only Thryallis being endemic to Brazil (Davis & Anderson 2010; Almeida et al. 2020).

2. Bunchosia Kunth, Nov. Gen. Sp. (quarto ed.) 5: 153. 1821 [1822].

Trees to shrubs; stipules epipetiolar. Leaves reduced associated to the inflorescence absent; petiole 0–2-glandular at apex; leaf blade narrowly elliptic, elliptic to lanceolate, margin entire, plane, primary vein slightly abaxially impressed to impressed, 2-glandular at base or 2–6-glandular, submarginal. Thyrses of 1-flowered cincinni, bracts and bracteoles persistent. Flowers with pedicels sessile (i.e., without peduncles); sepals adpressed to the androecium, 2-glandular; elaiophores 8–10. Drupes, 2–3-pyrenes, red to orange when mature, apex acute, glabrous.

Bunchosia differs from the remaining genera of Malpighiaceae from the state of Espírito Santo by drupes with acute apex and small trees or shrubs with thyrses of 1-flowered cincinni (Almeida et al. 2016). The genus comprises ca. 70 species found from Mexico to Northern Argentina (González-Gutiérrez 2010), with eleven species occurring in Brazil (BFG 2018). In this study, a total of three species of Bunchosia were recorded for the state of Espírito Santo.

Identification key for the species of Bunchosia from the state of Espírito Santo

1. Petiole eglandular...................2.3. Bunchosia maritima
1’. Petiole 2-glandular at apex.
- 2. Branches sericeous to glabrescent; leaf blade membranaceous, elliptic.........................................................2.2. Bunchosia macilenta
- 2’. Branches glabrous; leaf blades chartaceous, narrowly elliptic to lanceolate.........................................................2.1. Bunchosia acuminata

2.1. Bunchosia acuminata Dobson, Systematic Botany 8(3): 275. 1983. Figs. 2; 4

Figure 2
a-c. Photographic plate of Bunchosia acuminata – a. fruiting branch; b. detail of the inflorescence in side view; c. detail of the drupes in side view. Photographs: a, c. G.S. Siqueira; b. J.P. Zorzanelli.

Shrubs ca. 4 m tall; branches glabrous; stipules epipetiolar, 1.6–3 mm long, narrowly triangular, deciduous, free. Leaves reduced associated to the inflorescence absent; petiole 5.5–9.6 mm long, canaliculate, glabrous, 2-glandular at apex; leaf blade 8–16 × 2.8–5.6 cm, chartaceous, narrowly elliptic to lanceolate, base acute to attenuate, margin entire, plane, apex acuminate, both surfaces glabrous, primary vein abaxially impressed, 2-glandular at base. Thyrses with 11–15 flowers; main axis sparsely sericeous to glabrous; bracts 1.1–2.6 mm long, chartaceous, triangular, persistent, eglandular; peduncles up to 3 mm long; bracteoles 1.1–1.8 mm long, membrane, triangular, persistent, eglandular. Flowers with pedicels 4–10 mm long, glabrescent to glabrous; sepals adpressed to the androecium, 1.6–1.9 × 1.3–1.4 mm, apex rounded, both surfaces glabrous, 2-glandular; elaiophores 10, yellow, 2–2.5 × ca. 1.2 mm; petal yellow, limb orbicular, margin erose; lateral petals limb with 3.2–4 × 3.2–4.4 mm, claws 1.6–1.9 × ca. 0.2 mm; posterior petal ca. 2.7 × 3.2 mm, claws ca. 2 × 0.4 mm; stamens with filaments 0.9–1.2 mm long, connectives glandular, expanding at apex, thecae glabrous; ovary ca. 0.6 × 0.6 mm, conical, glabrous; styles ca. 1 × 0.1 mm, erect, parallel, cylindrical, glabrous; stigma apical, truncate. Drupes, 0.9–1.1 × 1.2–1.3 cm, 2–3-pyrenes, red when mature, glabrous.

Examined material: Conceição da Barra, Reserva Biológica do Córrego Grande, 13.II.2009, fr., L.F.T. Menezes 1899 (VIES). Pinheiros, Reserva Biológica Córrego do Veado, 23.II.2011, fr., M. Ribeiro 450 (SAMES); 1.II.2007, fl., L.M. Versieux 409 (RB); 26.X.2000, fl., V. Demuner 1513 (MBML). Sooretama, Reserva Biológica de Sooretama, 19.I.2010, fr., M. Ribeiro 74 (VIES).

Bunchosia acuminata is endemic to Brazil occurring in the states of Bahia and Espírito Santo (Almeida & Pellegrini 2016; BFG 2018). In the state of Espírito Santo, B. acuminata can be found in seasonally dry forests and rainforests. It was collected with flowers from October to April and fruit from November to May. It is also currently regarded as vulnerable by Fraga et al. (2019) and not threatened by CNCFlora (2019). B. acuminata is distinguished from the remaining species of Bunchosia from the state of Espírito Santo by its narrowly elliptic to lanceolate and glabrous leaves.

2.2. Bunchosia macilenta Dobson, Systematic Botany 8(3): 274. 1983. Figs. 3; 4

Figure 3
a-c. Photographic plate of Bunchosia macilenta – a. flowering branch; b. leaf in adaxial view; c. detail of the inflorescence. Photographs: H. Liuth.

Figure 4
Distribution map of Barnebya dispar (black stars), Bunchosia acuminata (white circles), and Bunchosia macilenta (black circles). Shades of black on the background represent montane relief. Pink = seasonally dry forest; green = rainforest; blue = open rainforest; yellow = pioneer formations.

Shrubs, 1–3 m tall; branches sericeous to glabrescent; stipules epipetiolar, 0.5–1.1 mm long, triangular, deciduous, free. Leaves reduced associated to the inflorescence absent; petiole 6–8 mm long, canaliculate, sericeous, 2-glandular at apex; leaf blade 7.9–10.3 × 4.6–5.4 cm, membrane, elliptic, base acute, margin plane, apex acute, both surfaces glabrescent, primary vein abaxially impressed, 2–4-glandular abaxially, submarginal. Thyrses with 4–8 flowers; main axis sericeous; bracts 0.9–1.1 mm long, chartaceous, triangular, persistent, eglandular; peduncles 2–2.3 mm long; bracteoles 0.6–0.8 mm long, chartaceous, triangular, persistent, eglandular. Flowers with pedicels 8–10 mm long, sericeous; sepals adpressed to the androecium, ca. 2.4 × 1 mm, apex rounded, adaxially glabrous, abaxially sericeous, 2-glandular; elaiophores 10, yellow, 1.1–1.3 × 0.8–1.1 mm; petals yellow, limb obovate, margin fimbriate; lateral petals limb with 3.4–3.7 × 2.9–3.2 mm, claws 2.2 × 0.3 mm; posterior petal limb with ca. 3.6 × 3.9 mm, claws ca. 3.3 × 1.4 mm; stamens with filaments 1.6–2.9 mm long, connectives glandular covering the posterior part of thecae, thecae glabrous; ovary ca. 1.1 × 0.7 mm, botuliform, glabrous; styles ca. 2.6 × 0.1 mm, erect, divergent, cylindrical, glabrous; stigma apical, truncate. Drupes, 0.7–1 cm long, 3-pyrenes, orange when mature, glabrous.

Examined material: Águia Branca, propriedade do Sr. Ailton Cortelete, 16.I.2008, fl., M.M. Saavedra 652 (MBML). Castelo, Parque Estadual Mata das Flores, 15.XII.2012, fl., M.L. Garbin 1529 (VIES). Colatina, 27.IV.1995, fr., G.F. Árbocz 1367 (VIES). Linhares, Reserva Natural da Vale, 1.VI.2001, fr., D.A. Folli 3939 (CVRD). Santa Teresa, São João de Petrópolis, 24.I.2006, fl., L. Kollmann 8597 (MBML). Serra, APA Mestre Álvaro, 13.I.2011, fl., A.M. Vago 144 (VIES).

Bunchosia macilenta is endemic to Brazil in the states of Minas Gerais, Bahia, and Espírito Santo (Almeida & Pellegrini 2016; Almeida et al. 2020). In the state of Espírito Santo, it occurs in rainforests, being collected with flowers from December to February and with fruits from January to July. B. macilenta is regarded as vulnerable by both CNCFlora (2019) and Fraga et al. (2019). This species can be confused with B. maritima by the shape of their leaves, but they are easily differentiated by branches sericeous to glabrescent (vs. glabrous in B. maritima), membrane leaf blades (vs. chartaceous in B. maritima), and the number of flowers per thyrse (4–8 flowers in B. macilenta vs. 9–13 flowers in B. maritima).

2.3. Bunchosia maritima (Vell.) J.F.Macbr., Publ. Field Mus. Nat. Hist., Bot. Ser. 13(3/3): 860. 1950. Figs. 5; 8

Figure 5
a-e. Photographic plate of Bunchosia maritima – a. flowering branch; b. detail of the petiole; c. inflorescence in side view; d. flower in frontal view; e. detail of the drupes. Photographs: a-d. M.O.O. Pellegrini; e. A. Junior.

Shrubs, ca. 3 m tall; branches glabrous; stipules epipetiolar, 0.6–0.7 mm long, triangular, deciduous, free. Leaves reduced associated to the inflorescence absent; petiole 8–11 mm long, canaliculate, sericeous, eglandular; leaf blade 11.1–25.5 × 6.3–9.1 cm, chartaceous, elliptic, base acute, margin plane, apex acuminate, both surfaces glabrous, primary vein slightly abaxially impressed, 4–6-glandular, abaxially, submarginal. Thyrses with 9–13 flowers; main axis sericeous; bracts 2.2–3 mm long, chartaceous, triangular, persistent, eglandular; peduncles 2.4–3.3 mm long; bracteoles 1.3–2.4 mm long, chartaceous, triangular, persistent, 1-glandular. Flowers with pedicels 0.4–5.3 mm long, sericeous; sepals adpressed to the androecium, ca. 2.4 × 1.7 mm, apex rounded, both surfaces glabrous, the lateral four sepals 2-glandular, the anterior eglandular; elaiophores 8, yellow, ca. 4 × 0.9 mm; petals yellow, limb elliptic to obovate, margin fimbriate, glandular; lateral petals limb with 4.3–5 × 3–4.7 mm, claws ca. 2.2 × 0.6 mm; posterior petal limb with ca. 3.7 × 3.3 mm, claws ca. 3.2 × 0.8 mm; stamens with filaments ca. 1.2 mm long, connectives glandular covering the posterior side of the thecae, thecae glabrous; ovary ca. 1.6 × 0.8 mm, ovoid, glabrous; styles ca. 1.2 × 0.2 mm, erect, parallel, cylindrical, glabrous; stigma apical, papillose. Drupe, 0.75–0.84 × 0.7–0.8 cm, 3-pyrenes, red when mature, glabrous.

Examined material: Alegre, ARIE Laerth Paiva Gama, 15.II.2008, fr., D. Couto 1391 (MBML). Aracruz, Picuã, 16.IV.2011, fr., T.F. Sagrillo 4 (MBML). Cachoeiro de Itapemirim, Floresta Nacional de Pacotuba, 5.III.2008, fr., L. Magnago 10733 (MBML). Cariacica, Reserva Biológica Duas Bocas, 16.II.2008, fr., A.M. Amorim 7142 (MBML). Linhares, lado direito da estrada indo da Encapa para Pedra Lisa, 16.III.1993, fr., V.D. Souza 454 (CVRD). Santa Leopoldina, Bragança, Rancho Chapadão, 30.VI.2006, fr., Jaqueline 2099 (MBML).

Bunchosia maritima is endemic to Brazil occurring in the states of Minas Gerais, Rio de Janeiro, Espírito Santo, São Paulo, Paraná, and Santa Catarina (Almeida & Pellegrini 2016; Almeida et al. 2020). In the state of Espírito Santo, it occurs in seasonally dry forests and rainforests, with flowers collected in January and fruits from December to July. Characters differentiating B. maritima and B. macilenta were discussed above, but B. maritima is the only species of Bunchosia with eglandular petioles.

3. Heladena multiflora (Hook. & Arn.) Nied., Arbeiten Bot. Inst. Königl. Lyceums Hosianum Braunsberg 5: 16. 1914. Figs. 6; 8

Figure 6
a-c. Photographic plate of Heladena multiflora – a. fruiting branch; b. flower in frontal view; c. mericarp in side view. Photographs: A. Francener.

Woody lianas; branches sparsely velutine to glabrescent; stipules epipetiolar, ca. 0.8 mm long, falcate, persistent, free. Leaves reduced associated to the inflorescence present; petiole 3–4.1 mm long, canaliculate, glabrous, eglandular; leaf blade 4.7–13.8 × 1.9–7.1 cm, membrane, elliptic, base attenuate, margin entire, plane, apex acute, both surfaces glabrous, primary vein abaxially impressed, 2-glandular at base. Thyrses of 1-flowered cincinni, 12–27 flowers; main axis sparsely sericeous; bracts 1.3–2 mm long, membrane, triangular, persistent, eglandular; peduncle 1.3–5.4 mm long; bracteoles 0.6–0.8 mm long, membrane, triangular, persistent, eglandular. Flowers with pedicels 2–4.5 mm long, sericeous; sepals parallel to the androecium, 1.9–2.3 × ca. 1.1 mm, apex rounded, both surfaces glabrous, the lateral four 2-glandular, the anterior eglandular; elaiophores 8, stipitate, green, 1.6–1.9 × 1.3–0.6 mm; petals yellow, limb obovate, margin partially lacerate; lateral petals limb with 2.6–2.9 × 2–2.3 mm, claws ca. 1.6 × 0.2 mm; posterior petal limb with ca. 5 × 4.5 mm, claws ca. 2.7 × 0.4 mm; stamens with filaments 1.7–2.5 mm long, connectives glandular covering the posterior part of the thecae, thecae glabrous; ovary ca. 1 × 0.7 mm, botuliform, sericeous; styles ca. 1.3 × 0.15 mm, erect, divergent, cylindrical, sericeous; stigma apical, truncate. Mericarp wingless, brown when mature, sericeous; nut 2.3–3.5 mm long.

Examined material: Boa Esperança, 16.XII.2007, fl., L. Kollmann 10205 (MBML). Santa Teresa, beira da estrada para o 25 de Julho, 3.XII.1998, fr., L. Kollmann 1215 (MBML); estrada do 25 de julho, 13.XII.2016, fr., L. Kollmann 13218 (MBML).

Heladena multiflora occurs in seasonally dry to rainforests from Argentina, Paraguay, and Brazil (states of Mato Grosso, Mato Grosso do Sul, Minas Gerais, and Espírito Santo) (Almeida et al. 2020). It was collected in flower and fruit in December, being regarded as endangered by both CNCFlora (2019) and Fraga et al. (2019). H. multiflora is distinguished from the remaining species of Malpighiaceae in the state of Espírito Santo by stipitate elaiophores, present since the floral bud and by wingless mericarps resembling those of Thryallis.

4. Thryallis brachystachys Lindl., Bot. Reg. 14: 1162. 1828. Figs. 7; 8

Figure 7
a-d. Photographic plate of Thryallis brachystachys – a. flowering branch; b. detail of the petiole; c. flower in frontal view; d. mericarps with expanded sepals. Photographs: a-b. M. Ferreira; c-d. W.R. Anderson.

Figure 8
Distribution map of Bunchosia maritima (black circles), Heladena multiflora (white triangles), and Thryallis brachystachys (white star). Shades of black on the background represent montane relief. Pink = seasonally dry forest; green = rainforest; blue = open rainforest; yellow = pioneer formations.

Woody lianas; branches sericeous to glabrescent; stipules epipetiolar, 0.6–0.7 mm long, triangular, deciduous, free. Leaves reduced associated to the inflorescence absent; petiole 1–1.1 cm long, canaliculate, tomentose, eglandular; leaf blade 5.2–6.1 × 2.9–3.5 cm, chartaceous, elliptic to ovoid, base obtuse, margin plane, apex acute to rounded, adaxially glabrous, abaxially tomentose, primary vein abaxially impressed, 2–4-glandular at base of leaves. Thyrses of 1-flowered cincinni, 6–16 flowers; main axis tomentose; bracts 1.6 mm long, chartaceous, triangular, deciduous; peduncles 3–3.7 mm long, tomentose; bracteoles 1.2 mm long, chartaceous, triangular, deciduous. Flowers with pedicels 6–9 mm long, tomentose; sepals 0.3–0.4 × ca. 1.1 cm, apex rounded, adaxially glabrous, abaxially tomentose, eglandular; petals yellow, margin erose; lateral petals flabellate, limb with 5.1–5.3 × 9–9.3 mm, claws ca. 4.1 × 1.2 mm; posterior petal orbicular with limb ca. 6 × 9 mm, claws ca. 3.3 × 0.9 mm; stamens with filaments 1 mm long, connectives glandular, thecae glabrous; ovary ca. 1.1 × 1.5 mm, conical, sericeous; styles ca. 3 × 0.1 mm, erect, divergent, cylindrical, glabrous; stigma apical, pedaliform. Mericarps wingless, 3–3.4 × 4.8–5.3 mm, sepals expanded in fruits, brown when mature, rugose, tomentose.

Examined material: Vila Velha, 6.V.1946, fr., A.C. Brade 18083 (RB).

Additional examined material: BRAZIL. Rio de Janeiro: Maricá, Serra do Camburi, 1.II.2017, fl., D.N.S. Machado 1196 (RB).

Thryallis brachystachys occurs in Paraguay and Brazil in the states of Bahia, Espírito Santo, Minas Gerais, Rio de Janeiro, São Paulo, Paraná, and Santa Catarina (Almeida et al. 2020). In the state of Espírito Santo, it is represented by a single collection from the restingas of Vila Velha dated from 1946. It was found in fruit in May, and it is regarded as critically endangered by Fraga et al. (2019). T. brachystachys is distinguished from the remaining species of Malpighiaceae from the state of Espírito Santo by stellate hairs, expanded and eglandular sepals in fruits, and wingless mericarps.

Acknowledgements

This study was carried out with the support of CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil, finance code 001). The authors would like to thank the curators and staff of all consulted herbaria, for their help during this study; and A. Francener, A. Junior, G.S. Siqueira, H. Liuth, J.P. Zorzanelli, M.O.O. Pellegrini, P. Sampaio, and W.R. Anderson, for allowing us to use their photographs in this study. PHDB thanks Capes, for his Master’s fellowship. Field and herbarium studies were financed by the CNPQ Universal project (422747/2016-5).

References

Almeida RF (2017) Amended description and conservation status of Stigmaphyllon carautae (Malpighiaceae). Rodriguésia 68: 1471-1477.
Almeida RF (2018) Taxonomic revision of Amorimia W.R.Anderson (Malpighiaceae). Hoehnea 45: 238-306.
Almeida RF & Amorim AMA (2015) Stigmaphyllon mikanifolium (Malpighiaceae), a new species from Espírito Santo state, Brazil. Kew Bulletin 70: 1-7.
Almeida RF & Mamede MCH (2014) Checklist, conservation status, and sampling effort analysis of Malpighiaceae in Espírito Santo state, Brazil. Brazilian Journal of Botany 37: 329-337.
Almeida RF & Mamede MCH (2016) Sinopse de Malpighiaceae no estado do Espírito Santo, Brasil: Stigmaphyllon A.Juss. Hoehnea 43: 601-633.
Almeida RF & Pellegrini MOO (2016) Synopsis of Bunchosia Kunth (Malpighiaceae) from the Atlantic Forest. Phytotaxa 257: 158-166.
Almeida RF & van den Berg C (2021) Molecular phylogeny and character mapping support generic adjustments in the Tetrapteroid clade (Malpighiaceae). Nordic Journal of Botany 39: e02876.
Almeida RF, Dal Col ACS & Amorim AMA (2015) Notes on Stigmaphyllon (Malpighiaceae) from southeastern Brazil. Boletim do Museu de Biologia Professor Mello Leitão 37: 427-436.
Almeida RF, Francener A, Pessoa C, Sebastiani A, Oliveira YR, Amorim AMA & Mamede MCH (2020) Malpighiaceae. In: Flora do Brasil 2020. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB155>. Access on 3 May 2021.
» http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB155
Almeida RF, Francener A & Amorim AMA (2016) A generic synopsis of Malpighiaceae in the Atlantic Forest. Nordic Journal of Botany 34: 285-301.
Almeida RF, Francener A & Sebastiani R (2013) New records on endangered and endemic species of Stigmaphyllon A.Juss. (Malpighiaceae) in Brazil. Check List 9: 1084-1086.
Almeida RF, Negrão R, Rosa P, Baez C, Maurenza D & Martinelli G (2018) Rediscovery of Banisteriopsis magdalenensis (Malpighiaceae): notes on morphology, distribution, and ecology of an endemic and threatened species from the Atlantic Forest of Brazil. Brittonia 70: 337-341.
Amorim AMA (2003) Five new species of Heteropterys (Malpighiaceae) from central and south America. Brittonia 54: 217-232.
Anderson CE (2014) Hiraea cuneata, H. macrophylla, and four new species confused with them: H. hatschbachii, H. occhionii, H. reitzii, and H. restingae (Malpighiaceae). Edinburgh Journal of Botany 71: 361-378.
Anderson WR (1981) Malpighiaceae. In: The botany of the Guayana Highland - Part XI. Memoirs of the New York Botanical Garden 32: 21-305.
Anderson WR & Gates B (1981) Barnebya, a new genus of Malpighiaceae from Brazil. Brittonia 33: 275-284.
Anderson WR (2001) Monograph of Lophopterys (Malpighiaceae). Contribution from the University of Michigan Herbarium 23: 83-105.
Anderson WR (2005) The Mascagnia cordifolia group (Malpighiaceae). Contribution from the University of Michigan Herbarium 24: 33-44.
Chase MW (1981) A revision of Dicella (Malpighiaceae). Systematic Botany 6: 159-171.
CNCFlora (2019) Malpighiaceae. In: Lista vermelha da flora brasileira. Versão 2012.2. Centro Nacional de Conservação da Flora. Available at <http://cncflora.jbrj.gov.br/portal/pt-br/listavermelha/MALPIGHIACEAE>. Access on 2 November 2019.
» http://cncflora.jbrj.gov.br/portal/pt-br/listavermelha/MALPIGHIACEAE
CRIA - Centro de Referência e Informação Ambiental (2021) SpeciesLink - simple search. Available at <http://www.splink.org.br>. Access on 3 May 2021.
» http://www.splink.org.br
Davis CC & Anderson WR (2010) A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. American Journal of Botany 97: 2031-2048.
Dutra VF, Alves-Araújo A & Carrijo TT (2015) Angiosperm checklist of Espírito Santo: using electronic tools to improve the knowledge of an Atlantic Forest biodiversity hotspot. Rodriguésia 66: 1145-1152.
ESRI-Environmental Systems Research Institute (2010) ArcGIS, version 9.3.1. Environmental Systems Research Institute, Redlands.
Fraga CN, Formigoni MH & Chaves FG (2019) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Instituto Nacional da Mata Atlântica, Santa Teresa. 432p.
Francener A, Almeida RF & Mamede MCH (2018) Assembling the puzzle of Byrsonima fanshawei (Malpighiaceae): emended description and new records for a rare species. Brittonia 70: 356-363.
Fundação SOS Mata Atlântica (2019) Atlas dos remanescentes florestais da Mata Atlântica período 2017-2018. Available at <https://especiais.gazetadopovo.com.br/wp-content/uploads/sites/19/2019/05/23120219/Atlas-mata-atlantica_17-18.pdf>. Access on 27 July 2019.
» https://especiais.gazetadopovo.com.br/wp-content/uploads/sites/19/2019/05/23120219/Atlas-mata-atlantica_17-18.pdf
Garbin ML, Saiter FZ, Carrijo TT & Peixoto AL (2017) Breve histórico e classificação da vegetação capixaba. Rodriguésia 68: 1883-1894.
González-Gutiérrez PA (2010) A revision of Cuban Bunchosia (Malpighiaceae), with description of a new subspecies from Hispaniola. Willdenowia 40: 55-61.
IBGE - Instituto Brasileiro de Geografia e Estatística (2015) Mapa de vegetação do Brasil. Instituto Brasileiro de Geografia e Estatística. Rio de Janeiro, Brasil. Available at <http://www.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm> Access on 22 April 2021.
» http://www.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm
Mamede MCH (1984) Flora fanerogâmica da Reserva do Parque Estadual das Fontes do Ipiranga (São Paulo, Brasil): 125. Malpighiaceae. Hoehnea 11: 108-113.
Mamede MCH (1992) Malpighiaceae. In: Melo MMRF, Barros F, Chiea SAC, Wanderley MGL, Jung-Mendaçolli SL & Kirizawa M (orgs.) Flora fanerogâmica da Ilha do Cardoso. Vol. 3. Instituto de Botânica, São Paulo. Pp. 73-87.
Mittermeier RA, Gil PR & Hoffman M (2005) Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. Conservation International, Washington. 392p.
Niedenzu F (1928) Malpighiaceae. In: Engler A (ed.) Das Pflanzenreich IV 141: 1-870.
Radford AE, Dickison WC, Massey JR & Bell CR (1974) Vascular plant systematics. Harper & Row, New York. 891p.
Ribeiro JELS, Hopkins MJG, Vicentini A, Sothers CA, Costa MAS, Brito JM, Souza MAD, Martins LHP, Lohmann LG, Assunção PACL, Pereira EC, Silva CF, Mesquita MR & Procópio LC (1999) Flora da Reserva Ducke: guia de identificação das plantas vasculares de uma floresta de terra-firme na Amazônia Central. INPA, Manaus. 799p.
Veloso HP, Rangel-Filho AL & Lima JCA (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. IBGE, Rio de Janeiro. 124p.
Tabarelli M, Silva J & Gascon C (2004) Tropical forest fragmentation, synergisms, and the impoverishment of neotropical forests. Biodiversity and Conservation 13: 1419-1425.
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 7 April 2021.
» http://sweetgum.nybg.org/science/ih/

Edited by

Area Editor: Dr. Anderson Alves-Araújo

Publication Dates

Publication in this collection
07 Mar 2022
Date of issue
2022

History

Received
15 Mar 2021
Accepted
13 May 2021

This is an open-access article distributed under the terms of the Creative Commons Attribution License.

[1] Almeida RF (2017) Amended description and conservation status of Stigmaphyllon carautae (Malpighiaceae). Rodriguésia 68: 1471-1477.

[2] Almeida RF (2018) Taxonomic revision of Amorimia W.R.Anderson (Malpighiaceae). Hoehnea 45: 238-306.

[3] Almeida RF & Amorim AMA (2015) Stigmaphyllon mikanifolium (Malpighiaceae), a new species from Espírito Santo state, Brazil. Kew Bulletin 70: 1-7.

[4] Almeida RF & Mamede MCH (2014) Checklist, conservation status, and sampling effort analysis of Malpighiaceae in Espírito Santo state, Brazil. Brazilian Journal of Botany 37: 329-337.

[5] Almeida RF & Mamede MCH (2016) Sinopse de Malpighiaceae no estado do Espírito Santo, Brasil: Stigmaphyllon A.Juss. Hoehnea 43: 601-633.

[6] Almeida RF & Pellegrini MOO (2016) Synopsis of Bunchosia Kunth (Malpighiaceae) from the Atlantic Forest. Phytotaxa 257: 158-166.

[7] Almeida RF & van den Berg C (2021) Molecular phylogeny and character mapping support generic adjustments in the Tetrapteroid clade (Malpighiaceae). Nordic Journal of Botany 39: e02876.

[8] Almeida RF, Dal Col ACS & Amorim AMA (2015) Notes on Stigmaphyllon (Malpighiaceae) from southeastern Brazil. Boletim do Museu de Biologia Professor Mello Leitão 37: 427-436.

[9] Almeida RF, Francener A, Pessoa C, Sebastiani A, Oliveira YR, Amorim AMA & Mamede MCH (2020) Malpighiaceae. In: Flora do Brasil 2020. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB155>. Access on 3 May 2021.
» http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB155

[10] Almeida RF, Francener A & Amorim AMA (2016) A generic synopsis of Malpighiaceae in the Atlantic Forest. Nordic Journal of Botany 34: 285-301.

[11] Almeida RF, Francener A & Sebastiani R (2013) New records on endangered and endemic species of Stigmaphyllon A.Juss. (Malpighiaceae) in Brazil. Check List 9: 1084-1086.

[12] Almeida RF, Negrão R, Rosa P, Baez C, Maurenza D & Martinelli G (2018) Rediscovery of Banisteriopsis magdalenensis (Malpighiaceae): notes on morphology, distribution, and ecology of an endemic and threatened species from the Atlantic Forest of Brazil. Brittonia 70: 337-341.

[13] Amorim AMA (2003) Five new species of Heteropterys (Malpighiaceae) from central and south America. Brittonia 54: 217-232.

[14] Anderson CE (2014) Hiraea cuneata, H. macrophylla, and four new species confused with them: H. hatschbachii, H. occhionii, H. reitzii, and H. restingae (Malpighiaceae). Edinburgh Journal of Botany 71: 361-378.

[15] Anderson WR (1981) Malpighiaceae. In: The botany of the Guayana Highland - Part XI. Memoirs of the New York Botanical Garden 32: 21-305.

[16] Anderson WR & Gates B (1981) Barnebya, a new genus of Malpighiaceae from Brazil. Brittonia 33: 275-284.

[17] Anderson WR (2001) Monograph of Lophopterys (Malpighiaceae). Contribution from the University of Michigan Herbarium 23: 83-105.

[18] Anderson WR (2005) The Mascagnia cordifolia group (Malpighiaceae). Contribution from the University of Michigan Herbarium 24: 33-44.

[19] Chase MW (1981) A revision of Dicella (Malpighiaceae). Systematic Botany 6: 159-171.

[20] CNCFlora (2019) Malpighiaceae. In: Lista vermelha da flora brasileira. Versão 2012.2. Centro Nacional de Conservação da Flora. Available at <http://cncflora.jbrj.gov.br/portal/pt-br/listavermelha/MALPIGHIACEAE>. Access on 2 November 2019.
» http://cncflora.jbrj.gov.br/portal/pt-br/listavermelha/MALPIGHIACEAE

[21] CRIA - Centro de Referência e Informação Ambiental (2021) SpeciesLink - simple search. Available at <http://www.splink.org.br>. Access on 3 May 2021.
» http://www.splink.org.br

[22] Davis CC & Anderson WR (2010) A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. American Journal of Botany 97: 2031-2048.

[23] Dutra VF, Alves-Araújo A & Carrijo TT (2015) Angiosperm checklist of Espírito Santo: using electronic tools to improve the knowledge of an Atlantic Forest biodiversity hotspot. Rodriguésia 66: 1145-1152.

[24] ESRI-Environmental Systems Research Institute (2010) ArcGIS, version 9.3.1. Environmental Systems Research Institute, Redlands.

[25] Fraga CN, Formigoni MH & Chaves FG (2019) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Instituto Nacional da Mata Atlântica, Santa Teresa. 432p.

[26] Francener A, Almeida RF & Mamede MCH (2018) Assembling the puzzle of Byrsonima fanshawei (Malpighiaceae): emended description and new records for a rare species. Brittonia 70: 356-363.

[27] Fundação SOS Mata Atlântica (2019) Atlas dos remanescentes florestais da Mata Atlântica período 2017-2018. Available at <https://especiais.gazetadopovo.com.br/wp-content/uploads/sites/19/2019/05/23120219/Atlas-mata-atlantica_17-18.pdf>. Access on 27 July 2019.
» https://especiais.gazetadopovo.com.br/wp-content/uploads/sites/19/2019/05/23120219/Atlas-mata-atlantica_17-18.pdf

[28] Garbin ML, Saiter FZ, Carrijo TT & Peixoto AL (2017) Breve histórico e classificação da vegetação capixaba. Rodriguésia 68: 1883-1894.

[29] González-Gutiérrez PA (2010) A revision of Cuban Bunchosia (Malpighiaceae), with description of a new subspecies from Hispaniola. Willdenowia 40: 55-61.

[30] IBGE - Instituto Brasileiro de Geografia e Estatística (2015) Mapa de vegetação do Brasil. Instituto Brasileiro de Geografia e Estatística. Rio de Janeiro, Brasil. Available at <http://www.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm> Access on 22 April 2021.
» http://www.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm

[31] Mamede MCH (1984) Flora fanerogâmica da Reserva do Parque Estadual das Fontes do Ipiranga (São Paulo, Brasil): 125. Malpighiaceae. Hoehnea 11: 108-113.

[32] Mamede MCH (1992) Malpighiaceae. In: Melo MMRF, Barros F, Chiea SAC, Wanderley MGL, Jung-Mendaçolli SL & Kirizawa M (orgs.) Flora fanerogâmica da Ilha do Cardoso. Vol. 3. Instituto de Botânica, São Paulo. Pp. 73-87.

[33] Mittermeier RA, Gil PR & Hoffman M (2005) Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. Conservation International, Washington. 392p.

[34] Niedenzu F (1928) Malpighiaceae. In: Engler A (ed.) Das Pflanzenreich IV 141: 1-870.

[35] Radford AE, Dickison WC, Massey JR & Bell CR (1974) Vascular plant systematics. Harper & Row, New York. 891p.

[36] Ribeiro JELS, Hopkins MJG, Vicentini A, Sothers CA, Costa MAS, Brito JM, Souza MAD, Martins LHP, Lohmann LG, Assunção PACL, Pereira EC, Silva CF, Mesquita MR & Procópio LC (1999) Flora da Reserva Ducke: guia de identificação das plantas vasculares de uma floresta de terra-firme na Amazônia Central. INPA, Manaus. 799p.

[37] Veloso HP, Rangel-Filho AL & Lima JCA (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. IBGE, Rio de Janeiro. 124p.

[38] Tabarelli M, Silva J & Gascon C (2004) Tropical forest fragmentation, synergisms, and the impoverishment of neotropical forests. Biodiversity and Conservation 13: 1419-1425.

[39] 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 7 April 2021.
» http://sweetgum.nybg.org/science/ih/