Research Article |
Corresponding author: Ana Carolina Mezzonato-Pires ( carolina.mezzonato@gmail.com ) Academic editor: Ricarda Riina
© 2018 Ana Carolina Mezzonato-Pires, Michaele Alvim Milward-de-Azevedo, Cláudia Barbieri Ferreira Mendonça, Vania Gonçalves-Esteves.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Mezzonato-Pires AC, Milward-de-Azevedo MA, Mendonça CBF, Gonçalves-Esteves V (2018) Taxonomy, palynology and distribution notes of seven new records of Passiflora L. (Passifloraceae s.s.) for Brazil. PhytoKeys 95: 1-14. https://doi.org/10.3897/phytokeys.95.22342
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Passiflora subgenus Astrophea is one of the five recognised subgenera of Passiflora. Brazil presents ca. 26 species of this subgenus with the majority distributed in the Amazon Basin. During the ongoing taxonomic revision of the Brazilian species of subg. Astrophea, seven species previously unknown for the country were recorded: Passiflora amoena, P. fuchsiiflora, P. jussieui, P. ovata, P. plumosa, P. quelchii, and P. tessmannii. The new records expand the species distribution ranges, especially for P. plumosa, which was exclusively known from its type locality and P. quelchii, which was known only for southeastern Guyana. The authors provide taxonomic and palynological descriptions, distribution maps and illustrations for these species, in the hope that the knowledge and understanding of Brazilian Passifloraceae s.s. will be improved.
Amazon basin, Astrophea , new records, Passifloraceae , pollen, taxonomy
Passiflora L. is by far the largest genus in the Passifloraceaes.s., with ca. 400 accepted species and a pantropical distribution (
Passiflora subg. Astrophea is a mainly neotropical group, with ca. 60 accepted species. The diversity of the subgenus is concentrated in lowland forest formations in the Amazon and the Guyana Shield regions (
Brazil is the most species-rich country with ca. 26 species of P. subg. Astrophea (Flora do Brasil under construction). The majority of the Brazilian species in this subgenus are recorded for the Amazon biogeographical domain (ca. 15 species), which represents 70% of the total for the country. Colombia is the second most species-rich country with 24 accepted species, including the recently described P. gironensis C.Aguirre, M.Bonilla & A.Rojas (
Pollen morphology is important in Passifloraceae species delimitation. This was also confirmed for P. subg. Astrophea by
As a result of an ongoing taxonomic revision of the Brazilian species of subgenus Astrophea, seven species were recorded for the first time in the Brazilian territory. The new records expand the distribution range for these taxa, especially for P. plumosa, which was exclusively known from its type locality and P. quelchii, which was known only from southeastern Guyana. Morphological descriptions, distribution maps and illustrations have been provided for these species, aiming to provide a better understanding of the Brazilian Passifloraceae.
The specimens analysed were deposited in the following herbaria: HAMAB, IAN, INPA, MBM, MG, NY, R, RB, SP, SPF, UB, UEC and UPCB, acronyms following Index Herbariorum (http://sweetgum.nybg.org/science/ih/). For each species, descriptions, distribution maps, illustrations of leaves, flowers and pollen grains were provided. The pollen material was processed with the acetolysis method established by
Seven species are recorded for the first time for Brazil: Passiflora amoena L.K.Escobar, P. fuchsiiflora Hemsl., P. jussieui Feuillet, P. ovata Jos.Martin ex DC., P. plumosa Feuillet & Cremers, P. quelchii N.E.Br. and P. tessmannii Harms. The distribution of each species in the Brazilian territory is shown in Figure
Lianas; tendrils thin to robust, glabrous. Stipules not seen. Petioles with two glands on the terminal end of the adaxial side. Blades 5.6–15 × 2.7–7.9 cm, chartaceous, elliptic or ovate, apex acute-mucronate or obtuse or emarginate, base cuneate, glabrous on both sides, discolorous, abaxial side greyish-brown, adaxial side purplish-vinaceous; margins non-undulate, glandular, 2–6 glands distributed on the abaxial side of the blade; 8–14 pairs of secondary veins, arcuate. Bracts diminute, triangular. Flowers arranged in racemose inflorescences, hypanthium cylindrical; sepals oblong, dark pink; petals oblong, pink; corona with 3 series of filaments, yellow to orange-yellow, filaments of first series with dolabriform-triangular, filaments of the second series with tuberculate wavy margins; operculum straight, non-tubular, included, ligulate, apex plicate; trochlea absent on the androgynophore; ovary ellipsoid, glabrous. Fruits 6.45 × 2.24 cm, ellipsoid, glabrous.
Illustrations of leaves and flowers in longitudinal section. A, B Passiflora amoena (S.V. Costa Neto et al. 2818, HAMAB) C, D Passiflora fuchsiiflora (S. Sakagawa et al. 248, INPA) E, F Passiflora jussieui (D.C. Daly et al. 7423, UPCB) G, H Passiflora ovata (S. Sakagawa et al. 668, INPA) I, J Passiflora plumosa (C.A. Cid et al. 561, MG) K, L Passiflora quelchii (R.C. Forzza et al. 8321, RB) M, N Passiflora tessmannii (C.A. Sothers & E.C. Pereira 612, INPA).
Pollen grains medium-sized (ca. 42.8 µm), prolate spheroidal, 6-colporate, colpi long, narrow, three endoapertures lalongate (ca. 6.2 × 8.1 µm), unique for each pair of ectoaperture, sexine reticulate, heterobrochate, with muri (ca. 1.2 µm), muri simple columellate, sinuous, continuous, with perforations, without high columellae, not apparent, tectum surface mostly curved, lumina ornamented, small (ca. 6.7 µm diam.) (Fig.
Photomicrographs and electron photomicrographs of pollen grains of the species of Passiflora. A, B Passiflora amoena C, D Passiflora fuchsiiflora E, F Passiflora jussieui G, H Passiflora ovata I, J Passiflora quelchii K, L Passiflora tessmannii A, C, E, G, K general aspect of polar view B, F, H, I, L general aspect of equatorial view, D and J ornamentation detail. Scale bars: 10 µm (C, E, F, G, H, I, K, L); 5 µm (A, B, J); 1 µm (D).
BRAZIL. Amapá: Amapari, Cabeceiras of the Rio Amapari, on the left bank of the rio Anacuí, trail 5, 01°50'41"N, 52°44'29"W, 7 Mar 2006 [fl], M.O. Hamada et al. 151 (HAMAB, INPA, R); Clevelândia do Norte, Rio Oiapoque, along the road between Oiapoque and Clevelândia, 3°48'48"N, 51°51'38"W, 20 Jul 1960 [fr], B. Maguire, J.M. Pires and C.K. Maguire 47085 (NYBG); Igarapé Ponta-Narri, third waterfall, 08 Oct 1949, [fl], G.A. Black 49-8461 (IAN); Macapá, Colônia do Torrão, 0°2'20"N, 51°3'59"W, 29 Aug 1962 [bt, fl], J.M. Pires & P.B. Cavalcante 52667 (IAN); Oiapoque, BR156, road between Calçoene and Oiapoque, 17 km southeast of Oiapoque, ca. 3°50'35"N, 51°50'6"W, 3 Dec 1984 [fl], S.A. Mori, J. Reitsma and R. Cardoso 17157 (HAMAB); Rio Oiapoque, about 1 km west of Cachoeira Utussansain, 2°8’N, 52°55’W, 8 Sep 1960 [fl], H.S. Irwin et al. 48080 (IAN); Rio Oiapoque, upper slopes and hilltop Tipac, 3°36’N, 51°19’W, 200-250m, 15 Oct 1960 [bt, fl], H.S. Irwin 48731 (IAN); Porto Grande, Floresta Nacional do Amapá, rio Mutum, conglomerate 02, 0°42'48"N, 51°24'48"W, 20 Feb 2009 [fl], S.V. Costa Neto et al. 2818 (HAMAB).
It is known to occur in Guyana, French Guiana, Suriname and Brazil. It is recorded for the state of Amapá, growing near river banks, in Floresta de Terra Firme and in periodically flooded areas called Floresta de Várzea.
Passiflora amoena belongs to P. subg. Astrophea , sect. Botryastrophea (Harms) Killip, ser. Carneae Feuillet. It is morphologically most similar to P. fuchsiiflora, being differentiated from the latter by its flowers with yellow to orange-yellow corona and dolabriform-triangular outer corona filaments. Both species possess pollen grains of the IV type (
Lianas; tendrils robust, glabrous. Stipules not seen. Petioles with two glands on the terminal end of the adaxial side. Blades 13.2–15.2 × 11.2–13.5 cm, chartaceous, widely ovate, apex round to slightly emarginate, base slightly to deeply cordate, glabrous on both sides; margins non-undulate, glandular; 11–14 pairs of secondary veins, arcuate. Bracts diminute, linear-setaceous, alternate. Flowers arranged in a racemose inflorescence, hypanthium cylindrical; sepals linear-oblong, pink; petals linear-oblong, pink; corona with 3 series of filaments, dark purple, filaments of first series subdolabriform, laterally attached filaments, filaments of second series tuberculate to tuberculate-triangular, filaments of third tuberculate; operculum straight, membranous, non-tubular, included, apex fimbriate; trochlea absent on the androgynophore; ovary obovoid to oblongoid, glabrous. Fruits not seen.
Pollen grains medium-sized (ca. 38.4 µm), prolate spheroidal, 6-colporate, colpi long, narrow, three endoapertures lalongate (ca. 7.6 × 11.0 µm), unique for each pair of ectoaperture, sexine reticulate, heterobrochate; muri (ca. 1.2 µm) simple columellate, sinuous, continuous, with perforations, without high columellae, not apparent, tectum surface mostly curved, lumina slightly ornamented, small (ca. 4.0 µm diam.) (Fig.
BRAZIL. Amazonas: Presidente Figueiredo, Rebio Uatumã, grid of PPBio, 2°2'4"S, 60°1'30"W, 16 Apr 2007 [fl, fr], S. Sakagawa et al. 248 (INPA); Rebio Uatumã, Igarapé access to camp 2, left bank rising, 2°2'4"S, 60°1'30"W, 27 Sep 2008 [fl], S. Sakagawa and J.R.M. Ferreira 512 (INPA).
It is known to occur in Guyana, French Guiana, Suriname, Venezuela and Brazil. A single specimen collected in 1993 at the Indigenous Reserve of Yanomani, state of Amazonas, by W. Miliken 1801, was originally identified as P. fuchsiiflora. Until the present contribution, this was the only specimen of P. fuchsiiflora known for Brazil. Nonetheless, this specimen actually belongs to P. balbis Feuillet. Two specimens from the state of Amazonas, municipality of Presidente Figueiredo, at the Biological Reserve of Uatumã, are here correctly identified as P. fuchsiiflora. Thus, this species is recorded for the first time in Brazil based on the aforementioned specimens. In Brazil, P. fuchsiiflora is restricted to the state of Amazonas, growing in Igarapé formations.
Passiflora fuchsiiflora belongs to P. subg. Astrophea , sect. Botryastrophea , ser. Carneae. It possesses widely ovate and chartaceous leaf-blades, with round to slightly emarginate apex, added to the three filament series of the corona, with subdolabriform outer filaments and the two inner series with tuberculate filaments. The pollen grains possess reticulate sexine with small lumina and, for this reason, the pollen was included by
Lianas; tendrils slightly robust, glabrous to slightly puberulous. Stipules not seen. Petioles with two glands on the terminal end of the adaxial side. Blades 15–23 × 8.4–12.7 cm, coriaceous, ovate to ovate-oblong to oblong to widely oblong, apex acuminate, base truncate to round, glabrous on both sides; margins conspicuous, undulate, brown to brownish-green, glandular, with 2–3 glands; 16–23 pairs of secondary veins, arcuate. Bracts diminute, linear-setaceous, alternate. Flowers arranged in a racemose inflorescence, hypanthium cylindrical; sepals linear-oblong, greenish; petals linear-oblong, white with lilac spots; corona with 4–6 series of filaments, greenish-yellow with dark red to purplish spots, filaments of first series subdolabriform, straight, laterally attached, filaments of second, third and fourth series with linear-capitate, straight, filaments of fifth series linear-capitate to hair-like, semi-straight or reflexed, filaments of sixth series hair-like, reflexed; operculum straight, tubular, membranous, exserted, apex crenulate; trochlea absent on the androgynophore; ovary narrowly oblongoid to narrowly ovoid, densely velutine. Fruits not seen.
Pollen grains large-sized (ca. 67.6 µm), prolate spheroidal, 6-colporate, colpi short, narrow, three endoaperture lalongate (ca. 5.5 × 9.2 µm) unique for each pair of ectoaperture, sexine partially tectate as small pieces of remnant muri can be observed; muri (ca. 2.8 µm) duplicolumellate, columellae high, apparent, without perforations and most of the tectum surface curved or with spines (ca. 4.8 × 4.6 µm), not forming lumina. A large part of the surface is ornamented with sparsely distributed bacula and conspicuous pila (Fig.
BRAZIL. Acre: Cruzeiro do Sul: Reserva Extrativista do Alto Juruá, Rio Juruá, Seringal São João, placing Tapaúna, [7°37'52"S, 72°40'12"W], 14 Mar 1992 [fl], D.C. Daly et al. 7423 (INPA, UPCB). Rondônia: Serra do Balaterio, 7 km from the village Campo Novo, 10°35'0S, 63°39'0"W, 24 Apr 1987 [fl], C.A. Cid et al. 8915 (INPA).
It is known to occur in French Guiana, Suriname and Brazil, being also cultivated at the ORSTOM Botanical Garden in Cayenne, in the UK by R.J.R. Vanderplank (
Passiflora jussieui belongs to P. subg. Astrophea sect. Capreolata J.M.MacDougal & Feuillet. It can be characterised by its leaf-blades with conspicuous margins, flowers with corona arranged in 4–6 filament series with dark red to purplish spots, the outer series with subdolabriform filaments, the inner series with linear-capitelate and straight filaments and the sixth series with hair-like and reflexed filaments. The pollen grains of the closely related P. cerradensis Sacco present semitectate exine and reticulate sexine with large and ornamented lumina; which differ greatly from the mostly non-tectate exine, not producing lumina, pollen grains of P. jussieui. The pollen grains of P. jussieui are included in the type II pollen group, while the ones of P. cerradensis are included in the type III pollen group (
Lianas; tendrils not seen. Stipules diminute, linear to linear-falcate. Petioles with two glands on the terminal end of the adaxial side. Blades 9.5–19.3 × 4.3–8.7 cm, chartaceous, oblong to obovate, apex attenuate to abruptly attenuate, base obtuse to round, glabrous on both sides; margins slightly undulate, with 4–6 glands; 22–25 pairs of secondary veins. Bracts diminute, linear to linear-falcate, alternate. Flowers solitary, hypanthium widely campanulate; sepals oblong, light green; petals oblong, white; corona with 4–6 series of filaments, filaments of first series dolabriform, with apex narrowly linear, margins slightly undulate, yellow below the inflated portion of the filaments, orange-yellow in the inflated portion, filaments of second series linear, filaments of third and fourth series with hair-like, filaments of fifth and sixth series with hair-like, reflexed; operculum straight, tubular, exserted, filamentous with a fimbriate apex, papillose; trochlea absent on the androgynophore; ovary obovoid to oblong-ovoid, densely tomentose. Fruits 5.5 × 3.5 cm, ellipsoid, glabrous.
Pollen grains large-sized (ca. 56.6 µm), prolate spheroidal, 6-colporate, colpi short, narrow, three endoaperture lalongate (ca. 10.0 × 15.5 µm) unique for each pair of ectoaperture, sexine reticulate, heterobrachate; muri (ca. 1.9 µm) duplicolumellate, sinuous, continuous, without perforations, without high columellae, not apparent, tectum surface mostly slightly curved, lumina slightly ornamented with pila, large (ca. 13.4 µm diam.) (Fig.
BRAZIL. Acre: Acrelândia, PAE Porto Dias (placing Bibi), 9°49'40"S, 66°53'0"W, 09-15 Nov 2006 [fl, fr], F. Obermuller et al. 102 (RB). Amazonas: São Gabriel da Cachoeira: Highway BR-307, SGC-Cucuí km 50, [0°16'25"N, 66°39'35"W], 27 Oct 2008 [fl], S. Sakagawa et al. 668 (INPA); Highway BR-307, SGC-Cucuí km 50, [0°15'49"N, 66°40'56"W], 22 Apr 2008, R.L. Assis et al. 93 (INPA).
It is known to occur in French Guiana, Venezuela and Brazil. It is recorded here for the states of Acre (municipality of Acrelândia) and Amazonas (municipality of São Gabriel da Cachoeira), growing in Floresta Ombrófila Densa formations, along roadsides, reaching up to 10 m high.
Passiflora ovata belongs to P. subg. Astrophea sect. Pseudoastrophea (Harms) Killip. It can be easily differentiated due to its oblong to obovate leaf-blades, glands restricted to the abaxial side of the petiole near the blade, flowers with widely campanulate hypanthium, and dolabriform filaments on the first corona series. According to
Lianas; tendrils thin, glabrous. Stipules diminute, linear. Petioles with two glands on the terminal end of the adaxial side. Blades 14.2–22 × 6.3–8.5 cm, membranous, oblong, apex attenuate, base obtuse, glabrous on both sides; margins inconspicuous, with two glands at base; 13–19 pairs of secondary veins, arcuate. Bracts diminute, deltoid, alternate. Flowers solitary or arranged in racemose inflorescences, hypanthium cylindrical to slightly funnelform; sepals linear-oblong; petals linear-oblong; corona with 4 series of filaments, white, filaments of first series liguliform, filaments of second series linear or liguliform, filaments of third and fourth series liguliform, plumose, reflexed or not; operculum straight, tubular exserted, apex crenulate; trochlea absent in the androgynophore; ovary oblongoid, densely velutine. Fruits not seen.
Pollen grains not seen.
BRAZIL. Amazonas: Itapiranga: rio Uatumã, the left bank, in front of the Rio Pitinga, [2°44'56"S, 58°1'19"W], 27 Aug 1979 [fl], C.A.Cid et al. 561 (MG); Presidente Figueiredo, Rebio Uatumã, 1°00’S, 59°00"W, grid of PPBio s.n., portion L3/500, [2°2'4"S, 60°1'30"W], 11 Jul 2008 [fl], F.A. Carvalho 31UAT (INPA).
The species was hitherto known to occur exclusively in its type locality, in the central-southern forests of French Guiana. Two specimens were identified by the authors, occurring in the state of Amazonas, municipalities of Itapiranga and Presidente Figueiredo. The new-found specimens were collected growing in Floresta Ombrófila Densa and Floresta de Terra Firme formations, on river edges with clay soil, at 600 m elevation.
Passiflora plumosa belongs to P. subg. Astrophea sect. Leptopoda Killip ex Feuillet & Cremers. It can be differentiated by its glabrous and membranous leaf-blades, corona with four series of filaments, all of them being liguliform in shape and the second and fourth or the third and fourth series with reflexed filaments. The apex of the operculum of P. plumosa can easily distinguish this species from P. cauliflora Harms and P. cerradensis, due to its crenulate apex.
Shrubs; tendrils absent. Stipules diminute, narrowly triangular, glabrous. Petioles with two glands on the terminal end of the adaxial side. Blades 11.3–18.8 × 2.6–4.8 cm, chartaceous, narrowly oblong to oblong-lanceolate, apex acute, base cuneate, glabrous on both sides; margins strongly undulate, with ca. three glands; 29–33 pairs of secondary veins, arcuate, conspicuous. Bracts diminute, triangular, verticillate, with marginal glands. Flowers arranged in racemose inflorescences, hypanthium cylindrical; sepals oblong-lanceolate; petals oblong-lanceolate; corona with 2 series of filaments, filaments of first series dolabriform, filaments of second series hair-like, apex entire or bifid, straight; operculum straight, non-tubular, included, filamentous with a fimbriate apex, 3.4–3.5 cm long; trochlea absent on the androgynophore; ovary oblongoid, glabrous. Fruits ca. 3.11 × 2.93 cm, orbicular, glabrous, green.
Pollen grains medium-sized (ca. 47.8 µm), prolate spheroidal, 6-colporate, colpi short, narrow, three endoaperture lalongate (ca. 8.7 × 17.0 µm) unique for each pair of ectoaperture, sexine reticulate, heterobrochate; muri (ca. 2.0 µm) duplicolumellate, sinuous, continuous, without perforations, columellae high, apparent, tectum surface mostly slightly curved, lumina ornamented with pila, large (ca. 15.2 µm diam.) (Fig.
BRAZIL. Roraima: Cantá, Serra Grande, 2°32'53"S, 60°47'10"W, 554 m, 12 Nov 2014 [fl], R.C. Forzza et al. 8321 (RB).
Found in savannahs from southwestern Guyana, being here recorded in the state of Roraima, municipality of Cantá, in the Serra Grande inselberg, around 554 m elevation. Beside the type specimens and the one recorded for Brazil, P. quelchii is only known by another specimen (i.e., Graham 342) from the Ireng District in Guyana (
Passiflora quelchii belongs to P. subg. Astrophea sect. Capreolata. It can be distinguished by its shrubby habit and leaf-blades with undulate margins and inconspicuous in sicco. The included, non-tubular, filamentous operculum with fimbriate apex is characteristic to P. quelchii and easily differentiates it from closely related species. Passiflora quelchii possess type III pollen grains, with reticulate sexine forming large lumina (
Lianas; tendrils absent. Stipules not seen. Petioles with two glands on the terminal end of the adaxial side. Blades 6.2–11 × 4–8 cm, chartaceous, elliptic to ovate to oblong-elliptic, apex emarginate, mucronate, base cuneate to round, abaxially puberulous, adaxially glabrous, except for the midvein; margins revolute, non-undulate, glands not seen; 10–14 pairs of secondary veins, arcuate. Bracts diminute, triangular, alternate. Flowers arranged in pairs, hypanthium campanulate-cylindric; sepals linear-lanceolate, green; petals linear-lanceolate, white; corona with 2 series of filaments, white at base, yellowing at mid length, with vinaceous spots at apex, filaments of first series linear, apex widely falcate, attenuate, filaments of second series subulate, apex acute; operculum straight, with irregular slits, non-tubular, included, filaments with fimbriate apex, papillose; androgynophore with trochlea; ovary oblongoid to obovoid, velutine to pilose, with hairs restricted to the veins. Fruits 6.3–6.4 × 2.3–2.4 cm, ellipsoid, puberulous.
Pollen grains medium-sized (ca. 46.0 µm), oblate spheroidal, 6-colporate, colpi long, narrow, three endoaperture lalongate (ca. 4.3 × 20.4 µm) unique for each pair of ectoaperture, sexine reticulate, heterobrochate; muri (ca. 1.0 µm) simple columellate, sinuous, continuous, with perforations, without high columellae, not apparent, tectum surface slightly curved, lumina not ornamented, small (ca. 2.4 µm diam.) (Fig.
BRAZIL. Amazonas: Manaus, Igarapé do Crespo, [3°6'7"S, 60°1'30"W], 04 Sep 1945 [fl], A. Ducke 1749 (IAN, NYBG, R); Itacoatiara-Manaus, Reserva Florestal Ducke, km 26, 2°53'0"S, 59°58'0"W, 10 Oct 1995 [bt, fl], C.A. Sothers and E.da C. Pereira 612 (INPA, MBM, MG, UEC); km 26, 2°53'0"S, 59°58'0"W, 27 Nov 1996, [bt, fl], M.J.G. Hopkins et al. 1609 (IAN, INPA, NYBG, SP, UB); next to road the Acará, [3°8'35"S, 58°26'39"W], 19 Dec 1997 [bt, fl], M.A.D. Souza and M.J.G. Hopkins 514 (INPA, SPF).
It is known for Ecuador and Peru, being herein recorded for the state of Amazonas, municipality of Manaus, localities of Igarapé do Crespo and Adolpho Ducke Forest Reserve. It is found growing in lowland forests and Terra Firme and Campinarana formations, in sandy soils, reaching 18 m.
Passiflora tessmannii belongs to P. subg. Astrophea sect. Pseudoastrophea. Until the present study, the Brazilian specimens of P. tessmannii were erroneously identified as P. hexagonocarpa, due to conflicting taxonomic characters. This confusion caused this species to be treated as P. hexagonocarpa in the Flora da Reserva Ducke (Hopkins and Sousa 1999). Passiflora tessmannii possesses conical trochlea with undulated margins, corona clearly composed of two series, outer filaments linear in shape, with apex widely falcate and attenuate and inner filaments subulate. The pollen grains possess reticulate sexine with small lumina, similarly to most species of P. subg. Astrophea sect. Pseudoastrophea and, according to
The first author thanks the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for a Doctoral scholarship. All researchers thank the FAPERJ (APQ1-E-26/111.214/2014) for financial support, Rodrigo Theófilo Valadares for the map, Monique Goes for the illustration and Marcelo Sales for his help with the SEM photomicrographs. V. Gonçalves-Esteves and C.B.F. Mendonça thank the CNPq for a Productivity Grant. We thank Pablo Muñoz-Rodríguez and Ricarda Riina for their helpful comments and suggestions.