Begonia isadorae E.L.Jacques

Jacques, Eliane De Lima, Pinto, Mahat Elliot Fernandes, Fernandes, Ana Luiza Borges Da Costa & Tozin, Luiz Ricardo Dos Santos, 2024, Begonia isadorae (Begoniaceae), a new endemic species from Ilha Grande, an island in southeastern Brazil, with notes on leaf anatomy, Phytotaxa 650 (3), pp. 236-248 : 237-244

Begonia isadorae E.L.Jacques , sp. nov. ( Figs. 1 , 2 , 3 )

Begonia isadorae is most similar to B. rubropilosa A.DC. (1859: 125) but differs in having puberulous to glabrescent adaxial leaf blades (vs. scabrous), puberulous tepals in the staminate and pistillate flowers (vs. squamulose) and ovaries with entire placentae (vs. bilamellate).

Type:— BRAZIL. Rio de Janeiro State: Angra dos Reis Municipality, Parque Estadual da Ilha Grande , Ilha Grande , na beira da estrada Abraão-Dois Rios , 23º00’S, 43º00’W, 1 December 2021, Wängler , M. S., Silva-Batista , I. C., Loureiro , M. & Ferreira , V. S. 3235 (holotype RBR [ RBR 00056077 ]).

Herbs, prostrate, to 15 cm tall (not including inflorescence). Cystoliths present. Stems prostrate; internodes 0.5–2.0 cm long, succulent, reddish, glabrous. Stipules persistent, subcarnose, greenish when fresh, brown, and scarious when dry, 6–10 × 5.5–10 mm, widely ovate to oblong, apex acute, acuminate to carinate, margins entire, densely puberulous along the keel, trichomes simple. Leaves simple, petioles reddish, 6–12 cm long, squamulose throughout, scales flat, fimbriate, adpressed to reflexed, rosy vinaceous, 2–4.5 mm long, leaf blades basifixed, entire, transversely ovate, asymmetrical, fleshy, 6.5–11 × 4.5–7.5 cm, apex acuminate, base cordate, lobes not overlapping the petiole, margins slightly undulate, serrulate, ciliate, adaxial surface shiny green, being light green on the veins, puberulous to glabrescent, trichomes simple, abaxial surface vinaceous, with simple trichomes, hairs with a wide base, vinaceous to reddish at the base, apex translucent, squamulose on principal veins, scales flat fimbriate, reddish, ca. 1 mm wide, fimbriae ca. 4 mm, venation actinodromous, with 6–7 primary veins. Inflorescences 3–5-branched cymes, bearing up to 7 flowers, 10–15(–17.5) cm long (including the rachis), rachis 7.5–14 cm long (the same size when fruiting), with microscopic glandular trichomes, reddish. Bracts persistent, 1.5–2.5 × 0.4–0.7(–1.5) mm, triangular, apex acute to carinate, margins ciliate, greenish, membranaceous, puberulous to glabrescent. Staminate flower: pedicels 7–10 mm long, greenish to white, puberulous, trichomes simple, hairs reddish, tepals 4, external pair white, puncticulate, 9–12 × 8–13 mm, orbiculate to widely ovate, apex rounded, margins entire at the base, ciliated in the upper half, membranaceous, pilose, simple trichomes, hairs ca. 1 mm long, hyaline, except by being reddish at the base, internal pair white, 8–12 × (2–) 3.5–6 mm, narrowly elliptic, apex acute, margins entire, membranaceous, glabrous, stamens 18–26, free, filaments 0.5–1.5 mm long, connective not projecting, obtuse, anthers 1.5–2 mm long, oblong, rimose, extrorse, yellow. Pistillate flower: pedicels 5–12 mm long, pinkish, glabrous, bracteoles 2, persistent, pinkish, located alternately on the pedicel, ovate, 1–2 × 0.5–1 mm, apex acuminate, margins fimbriate, with microscopic glandular trichomes on dorsal surface, greenish; tepals 5, white, unequal, puncticulate, broadly ovate to obovate, 4 largest, 9–11 × 5–8 mm, broadly elliptic, smallest, 6–9 × 2–5 mm, elliptic, apex acute, margins entire, membranaceous, with simple and microscopic glandular trichomes on dorsal surface, hairs 0.5–1 mm long, hyaline, except by being reddish at the base, ovary 3-locular, 7–9 × 11–12 mm (including wings), locular region 6–7 × 2.5–3 mm, ovate, light green, puberulous, with sparse microscopic glandular and simple trichomes, 3-winged, wings unequal, flat, reddish, with sparse microscopic glandular trichomes, sparsely puberulous at the margins, the largest wing 5–6 mm wide, smallest wings 2–3 mm wide, placentae entire, stigmas 3, 2.5–3.5 mm long, bifurcate, branches spiraled, yellow. Capsule 13–15 × 19–23 mm (including wings), depressed obovate, basally dehiscent, with microscopic glandular trichomes, light brown when mature, peduncles 14–18 mm long, with glandular microscopic trichomes, brown, wings 3, unequal, flat, descendant at apex, the largest wing, 10–11 × 10 mm, smallest wings 8–9 × 4 mm wide, glabrous, locular region 8–10 × 6–10 mm, ovate to broadly ovate, brown, puberulous, seeds oblong.

Etymology: —The specific epithet honors Isadora Jacques, daughter of the first author.

Phenology: —Flowering and fruiting November to March. Closing of the tepals of pistillate and staminate flowers was observed at dusk.

Distribution and ecology: — Begonia isadorae is only known in Ilha Grande, Angra dos Reis municipality, of the southern coast of the Rio de Janeiro state, Brazil. The island´s ecosystem can be described as a combination of natural and secondary forests. Dense Atlantic Forest covers the center of the island ( Alho et al. 2002), but there are also different vegetation formations, such as restingas, rocky slopes, mangroves, flooded and hillside forest ( Araújo & Oliveira 1988). The highest altitude places are Pico do Papagaio (959 m), Pico da Pedra d’Água (1011 m) and Serra do Retiro (1031 m) ( Barros et al. 2022; Oliveira 2022). Begonia isadorae grows in submontane forests, on outcrops of bare rocks, in the middle of the forest (“matacão”), covered with a thick layer of moss, in shady and very humid places, at an altitude of 136 to 610 meters. Currently, after centuries of devastation, the most preserved part of Ilha Grande is in the central-south portion, due to the established conservation units, the same does not happen in the north-northeast part, where numerous constructions were built to meet the growing search for activities related to tourism ( Coe et al. 2018). Begonia isadorae specimens available in herbaria coincide with the most preserved area of the island, the central-south portion, however, the lack of records in the others portions, especially on the west and south-southwest, is possibly the result of the low collection effort existing in this most remote and preserved part of the island ( Fig. 3 ).

Provisional conservation assessment:— According to IUCN Red List criteria ( IUCN Standards and Petitions Committee 2022), Begonia isadorae is provisionally assessed as VU, due to its area of occupancy (AOO) being less than 20 km ² and location number ≤ 5 (D2). Therefore, it is possible to with a plausible future threat that could take the taxon to CR or EX in a very short time, since it is found in an insular environment, with very small populations (less than 50 mature individuals) and is subject to various threats such as forest fires, invasive species, and a decline in habitat quality. The impacts of major threat factors on the B. isadorae seem to be related to the expansion of activities linked to tourism and nuclear power plants near the region, emphasizing the need for conservation actions on the island.

Additional specimens examined: — BRAZIL. Rio de Janeiro State: Angra dos Reis Municipality, Parque Estadual da Ilha Grande , Vila Dois Rios, Represa, 4 Mar 2002, A. A. M. Barros, L. A. Ribas, P. W. Feteira, L. O. F. Sousa, W. Gomes, C. C. Zysko, P. P. Vieira & S. Schneider 1431 ( RFFP) ; Morro do Cavalinho , 23°11’70.4” S, 44°11’68.7” W, 18 Aug 2012, A. A. M. Barros, L. R. Caires, E. Simonato, D. N. S. Machado, G. A. Queiroz, N. A. Pimentel & L. A. Ribas 4771 ( RFFP) ; Ilha Grande, próximo ao canal de drenagem da subida para o Pico do Papagaio, 23.148129°S, - 44.183447°W, 20 Feb 2022, I. L. O. Gomes s.n. ( RBR 00059915 ) ; Parque Estadual da Ilha Grande, Trilha T-13 para o Pico do Papagaio, 23º09´33.5”S, 44º12´39.7”W, 8 Dec 2008, A. A. M. Barros L. A. Ribas & C. R. S. Lamego 3655 ( RFFP) .

Taxonomic notes: —After field research carried out in Ilha Grande by the first author, it was possible to recognize an undescribed species of Begonia morphologically similar to B. rubropilosa de Candolle (1859: 125) in the shape of its leaf blades and habit (See Supplementary Figure 1 ). Subsequently, we analyzed all herbarium collections of Begonia available from Ilha Grande, it was observed that some samples had been mislabelled as B. rubropilosa , and determined they belonged to the undescribed species. Begonia isadorae is provisionally included the B. sect Pritzelia (Klotzsch) A.DC. (1859) , which includes all rhizomatous species in Southeast Brazil.

Begonia isadorae can be easily recognized by its transversely ovate leaf blades, squamulose petioles, staminate and pistillate tepals with red pigmented dots (i.e. puncticulate). Begonia isadorae resembles B. rubropilosa but differs in its puberulous to glabrescent adaxial leaf blades with simple trichomes (vs. scabrous, with simple trichomes sparsely distributed and scales on the principal veins); puberulous staminate and pistillate tepals, with simple hyaline, reddish at the base and microscopic glandular trichomes on dorsal surface (vs. squamulose, vinaceous scales); its ovary with entire placentae (vs. bilamellated); its capsule with glandular microscopic trichomes and a puberulous locular region (vs. squamulose, scales vinaceous, mainly in locular regions), its fruits elliptic wings with a descendant apex (vs. triangular).

Leaf anatomy:— The leaf blade of Begonia isadorae ( Fig. 4A–H ) in frontal view presents an adaxial epidermis composed of fundamental cells with a hexagonal shape of different sizes, with simple and glandular trichomes ( Fig. 4A, C ), which can be isolated or grouped in two ( Fig. 4A and inset); on the abaxial side, the epidermis is composed of fundamental cells with a hexagonal shape of varying sizes, anisocytic-type stomata, secretory simples and glandular trichomes ( Fig. 4B ), which can be located at the same level as the other epidermal cells or sunken. Simple trichomes present in Begonia isadorae could be emergences, as they form a multicellular structure with a tapered apex, and with cells apparently originating from the fundamental meristem composing its basal region ( Fig. 4C Inset, H).The distinction between trichomes and emergences is unclear, however, trichomes are formed only by epidermal protuberances, while emergences are formed from both epidermal and subepidermal cells (Evert 2006). In taxonomic studies, it is possible, that in many morphological descriptions of Begonia species, the emergences have been erroneously described as simple trichomes ( McLellan, 2005; Peng et al., 2008; Hughes et al. 2011; Karpova, 2019). Ontogeny studies may be necessary to understand the origin of the cell outgrowth (Evert 2006), especially in Begoniaceae trichomes. Improving ontogeny studies in Begoniaceae will possibly elucidate this question of morphology as to whether the simple trichomes on Begonia isadorae are in fact emergences or not. Until more in-depth studies bringing together a larger set of species can be carried out, we chose here to maintain the term simple trichomes, in order to keep anatomical comparability, even though this structure may, in fact, be emergences. Glandular trichomes have a unicellular base with a short stalk and a multicellular biseriate secretory head ( Fig. 4A and Inset). Anisocytic-type stomata occurs grouped in two or three, most commonly in three ( Fig. 4B ). Calcium oxalate drusen are lined up along the veins, and simple trichomes are found in greater quantities ( Fig. 4C ). In the cross section, the epidermal fundamental cells are small and rectangular ( Fig. 4D, E ).

The mesophyll is dorsiventral ( Fig. 4D–F ). Two to three layers of hypertrophied subepidermal cells form an aquiferous hypodermis on both sides ( Fig. 4D, F ). Subsequently, the presence of reduced-sized chlorophyll tissues is observed. Facing the adaxial surface there is a layer of palisade parenchyma with slightly elongated and narrow cells; and facing the abaxial face there are three layers of spongy parenchyma with lobed cells and containing a large amount of starch grains ( Fig. 4F ). Large-rounded idioblasts are found among the chlorophyll tissues ( Fig. 4D–F ). Histochemical tests indicated that the cell wall of the idioblasts is suberized ( Fig. 4G ), and its contents are noncellulosic polysaccharides.

In the region of the first order vein, the epidermis of the adaxial face is uniseriate, formed by flattened cells with rounded edges. Below that there is a layer of large, rounded subepidermal cells, forming the aquiferous hypodermis. Subsequently, there are three to four layers of angular collenchyma, followed by a narrow layer of palisade parenchyma. More internally, there are two collateral closed vascular bundles immersed in the fundamental parenchyma. Fibers with thick cell walls are observed above the phloem of the bundle facing the adaxial face. Next, five to six layers of fundamental parenchyma are visualized with rounded cells containing many drusen. Finally, three to four layers of angular collenchyma and uniseriate epidermis with rounded cells are visualized on the abaxial surface ( Fig. 4E ).

The petiole of Begonia isadorae in cross section has a uniseriate epidermis composed of flat cells with rounded edges ( Fig. 5A, B ), emergences that form scales ( Fig. 5C ) and glandular trichomes with a unicellular base, a short stalk and a multicellular biseriate secretory head, as described for the leaf blade. Internally, the cortex is composed of four to five layers of angular collenchyma ( Fig. 5A, B ) and four to five layers of fundamental parenchyma with large-rounded cells and idioblasts ( Fig. 5A ). No differentiation was observed in the cells forming the endodermis. The vascular cylinder is formed by approximately 19 collateral open bundles arranged in a ring surrounding the parenchymatic medulla; in the center two to three medullary vascular bundles are visualized ( Fig. 5A ). Each vascular bundle is formed by phloem, cambium and xylem ( Fig. 5D ).

In the Begoniaceae it is common to find anatomical characteristics in the leaf, as observed here for Begonia isadorae , such as: uniseriate epidermis, glandular trichomes, anisocytic stomata, glandular trichomes, aquiferous hypodermis, dorsiventral mesophyll, collateral bundle and calcium oxalate crystals along the veins ( Deguen et al. 2012; Suffan et al. 2021; Jacques et al. 2023). However, it is possible to highlight anatomical characteristics in B. isadorae that are different from those commonly found in the leaves of Begoniaceae species, such as: glandular trichomes grouped in two, large and rounded idioblasts found among the chlorophyll tissues and drusen lined up on the veins.

Figures

FIGURE 1. A–O. Begonia isadorae E.L.Jacques.A, Habit; B, Details of the internodes, showing the stipules; C, Petiole scales; D, Details of indumentum in abaxial leaf surface; E–G, Staminate flowers, different periods of anthesis; H, Stamen; I, Apex of the tepals of the pistillate flower, showing the indumentum; J–K, Pistillate flowers, different periods of anthesis; L, Stigmas; M, Bracteoles of pistillate flowers; N, Ovary, cross section; O, Capsule. Illustrations by Maria Alice Rezende from Wängler et al. 3235.

FIGURE 2. A–J. Begonia isadorae E.L.Jacques. A, Habitat; B, Petioles; C, Details of indumentum in adaxial leaf surface; D, Staminate flowers; E, Staminate flowers, showing the indumentum; F–H, Pistillate flowers, different periods of anthesis; I, Capsule. (A, I from Gomes s.n (RBR 00059915); B–H Wängler et al. 3235). (Scale bars: A= 35 cm; B= 3 cm; C= 1.5 cm; D–E= 10 mm; F= 8 mm, G= 3 cm, H, 10 mm; I= 10 mm) Photos A, I.L.O. Gomes; B–I, E.L. Jacques.

FIGURE 3. Distribution map of Begonia isadorae E.L.Jacques (dark dots).

FIGURE 4. Leaf blade anatomy of Begonia isadorae (Begoniaceae). A. Frontal view of epidermis (Ep) on the adaxial surface showing common cells and glandular trichomes (Gt). Inset shows cross section of glandular trichome occurring sunken on the epidermis. B. Frontal view of epidermis (Ep) on the abaxial surface showing glandular trichomes (Gt) and stomata (St) in groups of two or three. C. Frontal view of epidermis (Ep) on the midrib region showing lines of druses (Dr), emergences forming simple trichomes (Tr) and glandular trichomes (Gt). Inset shows detail of simple trichome. D. Cross section showing unistratified epidermis (Ep) on both sides with emergences forming simple trichomes (Tr), wide layer of hypodermis on both sides, and thin chlorophyll parenchyma (Cp). E. Midrib showing unistratified epidermis (Ep), wide hypodermis (Hp), collenchyma (Co), a continuous layer of chlorophyll parenchyma, formed by spongy (Sp) and palisade (Pp) parenchyma, and two collateral vascular bundles facing each other immerse in a fundamental parenchyma (Fp) with druses (Dr). Fi: fibers, Ph: phloem, Xy: xylem. F. Detail showing the leaf blade with wide hypodermis (Hp), tiny palisade parenchyma (Pp) and spongy parenchyma (Sp) with idioblast (Id). G. Detail of idioblast (Id) submitted to Sudan III test, showing suberized cell walls. H. Emergence forming a simple trichome with tapered apex. Scale bars: A, B, C, H = 50 µm; D = 200 µm; E, F, G = 100 µm.

FIGURE 5. Petiole cross section of Begonia isadorae (Begoniaceae).A. Overview of the petiole, showing epidermis (Ep), cortex formed by collenchyma (Co) and parenchyma (Pa), and vascular bundles (Vb) forming a ring around the parenchymal pith. Dashed circle is highlighting medullary vascular bundles. Id: idioblast. B. Detail showing epidermis (Ep) and collenchyma (Co) with druses (Dr). C. Detail of emergence forming scales (Sc) on the epidermis (Ep). D. Detail of collateral open vascular bundles with phloem (Ph), cambium (Ca) and xylem (Xy). Scale bars:A = 200 µm; B, D = 50 µm; C = 100 µm.