Taxonomy, palynology and distribution notes of seven species of Passiflora L. (Passifloraceae s.s.) newly recorded from Brazil

Abstract 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.

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 (Ulmer and MacDougal 2004). Feuillet and MacDougal (2003)  The subgenus is characterised by its well-developed woody stems generally reaching the canopy way above 30 m, entire leaves, the presence of two petiolar glands and diminute stipules and bracts. Difficulties in the collection of plant material due to the lianoid habit of these species are reflected in the small number of collections available in herbaria.
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 speciesrich country with 24 accepted species, including the recently described P. gironensis C.Aguirre, M.Bonilla & A.Rojas (Aguirre- Morales et al. 2016). Nonetheless, the species of Passiflora from the Amazon domain are currently poorly understood, with P. subg. Astrophea being especially problematic.
Pollen morphology is important in Passifloraceae species delimitation. This was also confirmed for P. subg. Astrophea by Mezzonato-Pires et al. (2017), who found that amongst all pollen characters, the most significant was the sexine ornamentation.
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.
Palynology. 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. 3C, D). Distribution and ecology. 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.
Taxonomic comments. 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 Mezzonato-Pires et al. (2017) in the type IV pollen group. 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 linearoblong, 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.
Palynology. 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. 3E, F). Distribution and ecology. 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 (Feuillet 2010) and in the USA by L. Gilbert. It is recorded for the states of Acre (municipality of Cruzeiro do Sul) and Rondônia (municipality of Porto Velho). According to Feuillet (2010), P. jussieui can be found growing in lowland rainforests, whereas in Brazil, it is found in Floresta de Terra Firme formations, in sandy and rocky soils.
Taxonomic comments. 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 (Mezzonato-Pires et al. 2017).  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.
Taxonomic comments. 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 Escobar (1990), the straight and tubular operculum of P. ovata, probably favours hummingbird pollination. The most morphologically similar species is P. costata, which can be easily distinguished from P. ovata by the presence of a trochlea in the androgynophore, operculum declinate at base with a straight upper part and corona with non-reflexed filaments in the inner series. According to Mezzonato-Pires et al. (2017), P. ovata is included in the type III pollen group, due to its reticulate sexine and large lumina. Fig. 2I, J Descriptions. 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.

Passiflora plumosa Feuillet & Cremers, Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C: Biological and Medical Sciences 87(3): 381, f. 2. 1984.
Palynology. Pollen grains not seen. Distribution and ecology. 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.
Taxonomic comments. 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. Descriptions. 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, ver-ticillate, 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.
Taxonomic comments. 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 (Mezzonato-Pires et al. 2017 (Fig. 3K, L). Distribution and ecology. 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.
Taxonomic comments. 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 Mezzonato-Pires et al. (2017), the pollen is included in the type IV pollen group.