Bradea borrerioides J.A.Oliveira & Sobrado, 2016

Oliveira, Juliana Amaral De & Sobrado, Sandra V., 2016, Bradea borrerioides (Rubiaceae), a new species from Brazilian inselbergs, Phytotaxa 243 (1), pp. 83-90 : 84-89

Bradea borrerioides J.A.Oliveira & Sobrado , sp. nov. ( Figs. 1 , 2 )

Type: — BRAZIL. Espírito Santo. Água Doce do Norte , morro da torre de celular, 22 April 2013, J. A. Oliveira, M. O. O. Pellegrini & R. C. Forzza 354 [holotype: RB! (three sheets labelled 1 of 3, 2 of 3, and 3 of 3); isotypes: K!, MBML!, CTES!] .

This species is distinguished from all other species of the genus by the frondose-bracteate synflorescence with paraclades disposed in a monocasial branch-pattern, its diminute flowers with white to pale-lilac corolla and obcordate capsules.

Herbs to sub-shrubs or shrubs, up to ca. 1.8 m tall; branches decumbent or erect, cylindrical to sub-tetragonal when young, dark greenish to brownish in older stages, glabrous to hispid or villosulous on young branches. Stipular sheath sub-triangular, 0.5–2 mm long, puberulous to villosulous externally, glabrous internally, bristle 1, 8–18 mm long, puberulous to pubescent, frequently with 1–3 pairs of lateral colleters, brownish. Leaves opposite; petioles 2–8 mm long, villosulous; blades lanceolate, narrowly elliptic to oblanceolate, (1.5–)3.1–6.3 × 0.4–0.9 cm, base narrowly cuneate and attenuate down the petiole, apex acuminate, papyraceous to chartaceous, slightly discolor, pubescent to villosulous, with hairs densely concentrated on the upper surface and on the veins underneath; midrib conspicuous on both surfaces, (3–)5–8 secondary veins on each side of the midrib, apparent only on lower surface; leaf margins scabrid to pubescent. Synflorescences terminal, 17.6–31.7(–47.8) cm long, frondose-bracteate, glabrescent to villosulous, paraclades disposed in a monocasial branch-pattern; cymules glomeruliform, many-flowered, decreasing in size towards the apex, 0.9–1.4 cm wide; bracts 1–2, leaf-like, two times longer than the glomerules, 20–50 × 6 mm at the axillary inflorescences and 8–15 × 5 at the terminal glomerule; bracteoles linear, 1.5–3.2 × 0.1–0.2 mm, villosulous, apex acuminate, colleters absent or one pair present. Flowers heterostylous, sessile; hypanthium obovoid to slightly reniform, 1.4–1.7 × 1.2–1.5 mm, laterally compressed, 0.46–0.5 mm thick, asymmetric, with one locule more developed than the other, pubescent to villosulous; point of insertion of the hypanthium displayed to the right side. Calyx 2-lobed, lobes slightly unequal, the larger one 1.4–3 × 0.4–0.6 mm, correlated with the more developed locule, the shorter one 1–2.3 x 0.2–0.6 mm, correlated with the locule less developed, lanceolate to narrowly triangular, pubescent, margins scabrid to pubescent; interlobular colleter dactiliform. Corolla 4-merous, white or pale-lilac, hypocrateriform, externally puberulous to villosulous; tube 2.7–3 mm long, 1.8–2 mm wide at base, 2–4 mm wide at mouth, lobes narrowly triangular to triangular, (1.6–)2–3.3 × 0.6–1.3 mm, internally glabrous or with sparse trichomes. Ovary bilocular, with 4–5(–6)–ovules per locule, locules unequal; style bifid, style branches papillate; nectariferous disc entire. Longistylous flowers: internally with moniliform hairs from the middle of the tube to the base of the lobes; style 5–6.4 mm long, exserted; stamens 4, included; filaments 0.2–0.3 mm long; anthers oblong, 1–1.4 × 0.2–0.5 mm. Brevistylous flowers: internally with moniliform hairs from the upper 2/3 of the tube to the base of the lobes; style 1.5–2.6 mm long, included; stamens 4, exserted; filaments 1.5–2.4 mm long; anthers oblong, 1.2–1.7 × 0.2–0.5 mm. Capsules obcordate, asymmetric, (2–)3.3–4(–5.4) × (2–) 3.1–3.7 mm, 0.5–0.8 mm thick, lignified, pubescent, dehiscent with septicidal and longitudinal dehiscence, calyx lobes persistent; one mericarp more developed than the other, larger mericarp 2–3.8 × 1–2 mm, smaller mericarp 1.6–2.8 × 0.9–1.7 mm. Seeds 3–4 per mericarp, sub-triangular to sub-obovoid, 1–2.6 × 1–1.8 mm, lightly lenticular, winged, peltate, dorsiventrally compressed, dorsal surface marginally convex, ventral surface flat, testa papillate ( Fig. 3 E–G ).

Pollen grain morphology: — Bradea borrerioides pollen grains are 3-colporate, medium (P= 44.97 (49.69) 54.48 μm; E= 43.7 (48.37) 51.67 μm), and prolate-spheroidal (P/E= 0.92 (1.03) 1.11). The outline is slightly triangular in polar view with apertures situated at the angles. The ectoaperture is a long colpus (37.67 (39.86) 42 μm long; LC/P= 87.3), slit-like, with sharp ends and margins with tufts of nanospines. The colpi have an apertural membrane, 6–14 μm long, with granulate surface. The endoaperture is a pore lalongate, which width is ca. 1/4 the length of the ectoaperture. The pori are 10.51 (15.17) 17.63 μm in diameter at the ectocolpus area and 4.86 (6.37) 9 μm at the mesocolpium area. The exine is 2.89 (3.57) 4.35 μm thick, the nexine 1.37 (1.96) 2.49 μm thick, and the sexine 1.29 (1.96) 2.49 μm thick. Both are separated in a vestibule (3.84 (5.09) 6.35 μm) at the aperture area. The exine is semitectate with inconspicuous nanospines, and the tectum is microreticulate. The lumina are 1.07 (1.35) 1.8 μm in diameter and have nanospines arranged in groups at the center. There is no difference between the mesocolpium and apocolpium exine pattern ornamentation. ( Fig. 3 A–D ).

Morphological observations: —The capsules in Bradea borrerioides are obcordate as in B. brasiliensis Standley (1932: 123) and B. kuhlmannii Brade (1950: 14) , and its flowers are small like the ones of B. bicornuta Brade (1950: 15) . However, B. borrerioides can be recognized by possessing the longest synflorescences in the genus (commonly 17.6–31.7 cm long, rarely up to 47.8 cm long), which are frondose-bracteose, with its paraclades disposed in a monocasial branch-pattern, a feature exclusive to the species. In addition, it can be distinguished by its herbaceous to sub-shrub growth-form, with decumbent branches and flowers with white to pale-lilac corollas.

Etymology: —The epithet “ borrerioides ” makes reference to the similarity in habit, inflorescence form and the diminutive white to pale-lilac corollas as in some species of the genus Borreria Meyer (1818: 79) ( Spermacoceae ).

Distribution and Habitat: —The species is known from northeastern Minas Gerais and northern Espírito Santo state, Brazil ( Fig. 4 ). Unlike other species of the genus, Bradea borrerioides is not heliophylous. It occurs in semishaded understory in open forests on granitic outcrops or on the margins, at elevations between 144 and 620 m.

Phenology: —Collected with flowers and fruits from February through April.

Conservation status: — Bradea borrerioides is classified as Endangered, EN B1ab(i,ii,iii,iv,v)+2ab (i,ii,iii,iv,v); C2ai; D1 ( Negrão 2014), according to IUCN Standards ( IUCN 2001). The species presents EOO of 1.925 km ² and AOO of 24 km ², and since it only occurs on rocky outcrops, its habitat is naturally and severely fragmented leading to isolation of the subpopulations. Six subpopulations of this species are known, the largest one is composed of approximately 50 mature individuals, and none of them are protected by Conservation Units. The global population suffers impact from several human activities that imply continuous decline of EOO, AOO, habitat quality, and number of subpopulations. The threats are: granite mining based in implosion of inselbergs; vegetation suppression for installation of mobile phone towers, TV antennas and other technologies; and the current use of the outcrops for cultivation of coffee and Eucalyptus . In addition, the invasion of exotic grasses, tourism and recreational activities on inselbergs involving the installation of paragliding ramps or opening of trails and trampling of vegetation imply declining habitat quality and the number of mature individuals. Whereas the endemic plants of inselbergs rarely survive in ex situ collections due to the climatic and ecological conditions of these environments, investment is required in the creation and expansion of protected areas that include the species’ habitats ( Negrão 2014).

Additional specimens examined (paratypes): — BRAZIL. Espírito Santo: Água Doce do Norte, Córrego Havaí , torre de celular/rampa de vôo livre, topo, afloramento rochoso, 27 April 2008, A. P. Fontana, L. Kollmann, E. Leme, M. Zanoni, O. Ribeiro & N.F.B. Botelho 5077 ( K, MBML!) ; idem, Santa Luzia do Córrego Azul , 28 April 2008, L. Kollmann, A. P. Fontana, E. Leme & M. Zanoni 10975 ( MBML!) ; Nova Venécia, Distrito de Cristalina , 15 February 2014, R. C. Forzza, K. Hmeljevski & H. Medeiros 7807 ( RB!) ; idem, inselbergue, 14 February 2014, R. C. Forzza, K. Hmeljevski & H. Medeiros 7790 ( RB!) ; Vila Pavão, Barra da Rapadura, Fazenda do Sr. Wagner Scardini , 16 February 2014, R. C. Forzza, K. Hmeljevski & H. Medeiros 7874 ( RB!) . Minas Gerais: Teófilo Otoni , afloramento rochoso ao lado esquerdo da MG-418, cerca de 30 km ao N de Teófilo Otoni, 16 April 2011, L. F. A. De Paula & M. D. F. Augsten 303 ( BHCB, CTES!) ; idem, L. F. A. De Paula & M. D. F. Augsten 355 ( BHCB, CTES!) .

Figures

FIGURE 1. Bradea borrerioides. A. Habit. B. Stipular sheath. C. Glomeruliform cymule. D. Detail of the cymule with foliate bracts. E. Flower bud. F. Longistylous flower (=LF). G. Hypanthium, style and stigma of LF.H. Open corolla of LF. I. Brevistylous flower (=BF). J. Hypanthium, style and stigma of BF. K. Open corolla of BF. L. Capsule. M. Internal view of a mericarp to display septicidal dehiscence. N. Open mericap showing the placenta and seeds. O. Dorsal view of seed. P. Ventral view of seed. (A–H, L–P from L. F. M. De Paula & M. D. F. Augsten 303; I–K from L. F. A. De Paula & M. D. F. Augsten 355). Illustration by L. Simón.

FIGURE 2. Bradea borrerioides. A. Type locality. B. Inselberg in Nova Venécia. C. Habit. D. Leaf. E. Stipular sheat. F. Synflorescence. G. Detail of a lilac brevistylous flowers. H. Detail of lilac longistylous flowers. I. Detail of white longistylous flowers. J. Capsules. (Photos B–C, E, I by H. Medeiros; A, D, F–H, J by M. O. O. Pellegrini).

FIGURE 3. Scanning electron microscopy (SEM) micrographs of pollen grains and seeds of Bradea borrerioides. Pollen: A. Polar view. B. Equatorial view. C. Detail of the compound aperture. D. Detail of exine ornamentation at the apocolpium. Seed: E. Dorsal view. F. Ventral view. G. Detail of the papillate testa and digitate cells. (A–G from L. F. M. De Paula & M. D. F. Augsten 303). Pollen scale bar 5 μm; seed scale bar 100 μm.

FIGURE 4. Distribution of Bradea borrerioides in Brazil. Produced by Centro Nacional de Conservação da Flora (CNCFlora). 2014.