Eugenia grandifolia O. Berg (1857: 324)

Fernandes, Thiago, Braga, João Marcelo Alvarenga, Valdemarin, Karinne Sampaio, Denardi, Vinícius Luvizotto, Prieto, Pablo Viany & Mazine, Fiorella F., 2025, Revisiting the endemic Eugenia grandifolia (Myrtaceae), a rare species from the Brazilian state of Rio de Janeiro: extended description and conservation, Phytotaxa 682 (2), pp. 170-178 : 171-176

Eugenia grandifolia O. Berg (1857: 324) .

Type:— BRAZIL. Rio de Janeiro [1817–1821], fl., H.W. Schott 5842 ([first step] lectotype W (two sheets), designated by Mazine & Souza (2015); [second step] lectotype W 0046313 !, designated here; isolectotypes W 0046314 !, W 0046315 !, F 0065183F !). Remaining syntype:— BRAZIL. Rio de Janeiro, F. Sellow s.n. (B, not seen and probably destroyed). Figures 1–4 .

Description: —Shrubs to treelets 1–3 m high, scarcely ramified ( Figure 2A ), sometimes with long, pendent branches. Trunk with bark brownish, irregularly fissured, sometimes detaching thick plates ( Figure 2B ). Apical bud sericeous, trichomes simple, whitish to greyish, ca. 0.2 mm long, glabrescent, young leaves dark-purple in vivo. Young twigs (the internode immediately below the apical bud) puberulent to glabrous, apically keeled and strongly flattened along its remaining extent, dull light-brown, dark-brown or brownish-vinaceous, with more or less conspicuous glands, the proximal region of the internode with whorled, triangular cataphylls ca. 2.3 × 2.3 mm, early deciduous, leaving conspicuous scars. Branches at intermediate stages of development light-brown to brownish-grey, lustrous, when mature brownish-grey to greyish, irregularly fissured, sometimes detaching longitudinal, slightly thick plates. Leaves decussate, subsessile, petioles 3–7 × 2.5–4.5 mm, slightly pulvinate and visible only abaxially ( Figure 2C ), when immature rugose and glandulous, when mature lustrous, corky, transversally fissured; blades 16.5–30 × 4.5–12 cm, 2.4–4 times longer than wide, discolorous, drying dull brownish-green adaxially and dull yellowish to fulvous abaxially, chartaceous, cracking easily if folded in vivo, usually elliptic-oblong or oval-oblong, sometimes lanceolate or spathulate, base cordate ( Figure 2C ), apex acute to acuminate, puberulent to glabrous, midvein adaxially sulcate, abaxially raised, secondaries and higher order veins raised and reticulate on both surfaces, marginal veins three, the innermost 4–10 mm, the middle 2–2.5 mm, the outermost 0.5–1 mm from the margin, this one usually drying undulate; glandular dots conspicuous on both surfaces, slightly darker than the surface, 0.05–0.1 mm in diameter, adaxially foveolate, abaxially raised ( Figure 2D ). Inflorescences often ramiflorous and developing exclusively from the young twigs ( Figures 2E and 2F ) or axillary at the distal nodes, racemes, with 1–2 pairs of opposite, decussate flowers, peduncles 3–6 mm long, main axis 3.5–17.5 × 1.2–1.5 mm, flattened, densely sericeous, cinereous, trichomes ca. 0.2 mm long; pedicels 3–7.5 × ca. 1 mm, the proximal ones slightly longer than the distal ones ( Figure 2F ), with the same indumentum as the main axis, flower internodes 3.7–6.4 mm, ratio pedicel/flower internode 0.8–1.2:1; bracts triangular, carinate, the ones subtending the main axis ca. 5 × 1.3 mm, dark-brown in vivo, marcescent or early deciduous ( Figure 2F ), bracts subtending flowering nodes 3–4 × 1.2–2 mm, oval-lanceolate, persisting until fruit development, green in vivo; bracteoles 3.8–4.5 × 4–4.7 mm, fused at 1/3 of their length, widely-deltoid, carenate, enclosing the ovary, ciliate, externally puberulent, internally glabrous, persisting until fruit maturation, remaining as a cup-like structure if the flower/fruit is detached; colleters in groups of 2-7, unequal euryform filaments ( Figure 3C ), located in the inner side of the bracts, between the bracts and the axis of the inflorescence, present on the bracts of axillary or apical inflorescences ( Figures 3A and 3B ), glabrous, 0.3–0.86 × 0.03–0.17 mm. Flower buds 5–5.2 × 4.3–4.5 mm, obovoid ( Figures 2E and 2F ), the ovary (hidden by the bracteoles) densely sericeous, cinereous, the trichomes ca. 0.2 mm long, markedly distinct from the puberulent calyx, the petaliferous globe appearing only at late stages of bud development; calyx lobes four, densely glandular, externally puberulent, internally glabrous, with cinereous cilia ca. 0.2 mm long, in two unequal pairs, the larger one ca. 5 × 5 mm, the smaller one 3–4.5 × 3–4.5 mm; petals narrow-elliptic to spathulate, concave, 6–15 × 4.8–5 mm, erect or involute, campanulate, partially covering the stamens ( Figures 2G and 2H ), membranaceous, glabrous and densely glandular on both surfaces; floral disk rounded, 2.5–3.2 mm in diameter; staminal ring rounded, 1–1.2 mm thick, puberulent, slightly inflated and forming a shallow cup at the central point, stamens 300–305, filaments 5–12 mm long, anthers with an apical gland; style 15–20 mm long, glabrous, stigma punctiform and minutely papilose, ovary with two locules, each with 13–15 ovules. Fruits (not seen when fully ripe, Figures 2J and 2L ) 20–27 × 13–30 mm, green in vivo, usually globose, ellipsoid or oblate, rarely pyriform, often with swellings where the seeds are lodged, the surface densely glandular and slightly costate, with variable number of longitudinal ridges, especially at early stages of maturation ( Figure 2J ), crowned by the persistent and apparently accrescent calyx lobes, pulp scarce, firm, yellowish; seeds 2–7, 17–24.5 × 17–18.5 mm, prismatic, with the shape of a hemispherical wedge, arranged spirally when four or more ( Figure 2L ), cotyledons fused, hypocotyl inconspicuous.

Specimens examined: — BRAZIL. s.l., 1859, “Herbarium Fischer” (LE!). “Brasilia”, s.d., L. Riedel 644 (LE!). Rio de Janeiro: s.l., 1817–1821, fl., H.W. Schott 5842 (F!, W!). Mun. Niterói, Piratininga , Tibau , Parque Natural Municipal de Niterói , Morro da Viração , trecho final da travessia Tupinambá , próximo à saída da trilha , 22º56’45”S, 43º5’59”W, 60 alt., 2 December 2021, fl., T. Fernandes 883 ( K!, NIT!, NY!, R!, RB!, RBR!, SORO!, SP!, SPF!) ; ibidem, 17 December 2021, fl., T. Fernandes 893 ( K!, NIT!, NY!, RB!, RBR!, SORO!) ; ibidem, 22 December 2021, fl., T. Fernandes 922 ( NIT!, RB!, SORO!) ; ibidem, 4 January 2022, fr., T. Fernandes 928 ( NIT!, RB!, SORO!) ; ibidem, 20 January 2022, fr., T. Fernandes 942 ( NIT!, RB!, SORO!). Mun. Rio de Janeiro, Corcovado , 1839, fl., M. Guillemin 766 ( G!). Morro da Babilônia , 12 October 1871, st., A.F.M. Glaziou 4989 ( P!). Botafogo , Morro Mundo Novo, Campus da Universidade Santa Úrsula , ca. 90 ms.m., 23 July 1998, st., J.M.A. Braga & J. Caruso 4960 ( RB!). Morro da Urca, Pista Cláudio Coutinho , à margem esquerda , 19 May 2022, st., M. Lacerda & P.V. Prieto 1326 ( NIT!) .

Distribution, habitat and phenology: — Eugenia grandifolia is endemic from the Brazilian state of Rio de Janeiro, occurring in the municipalities of Niterói and Rio de Janeiro (capital city). It inhabits the understory of coastal forests growing on shallow, rocky soils, at elevations of 20–200 m (potentially up to 300–400 m). Flowers were collected from mid to late December, fruits from early to late January.

Conservation status: Eugenia grandifolia presents a very restricted geographic range (EOO = 9.8 km ² and AOO = 16 km ²) within the Rio de Janeiro metropolitan region, one of the largest in the world with ca. 13 million inhabitants. The species is currently known from five localities that are here assumed to be four distinct locations (19 th century records from unspecified localities were not considered). All localities except one ( Morro Mundo Novo ) are included in strictly protected areas ( Parque Nacional da Tijuca, Parque Natural Municipal Paisagem Carioca, Monumento Natural dos Morros Pão de Açúcar e da Urca and Parque Natural Municipal de Niterói). However, even these protected areas can suffer a decline in habitat area, extent, and/or quality due to the urban heat island effect ( Peres et al. 2018), fire ( Matos et al. 2002), pollution ( Mello 2001), and soil compaction, introduction of exotic species, and removal of individuals that border the paths, consequences of the intense frequency of visitors to the parks ( Mendes et al. 2024). All localities are separated from each other by densely urbanized areas, which is expected to impose a strong barrier to gene flow between them. Fortunately, the two localities recently visited by us ( Urca and Parque Natural Municipal de Niterói) comprise subpopulations of reasonable sizes (at least 30–40 individuals each, potentially> 100). Conservation of the species is more challenging at Morro Mundo Novo , a small hill with a disturbed forest fragment, where E. grandifolia was collected in 1998. The species may be prone to local extinction in this locality due to forest degradation and associated loss of typical understory conditions, which would lead to a decline in the extension of occurrence, area of occupancy and the number of locations and subpopulations. We recommend that the presence of E. grandifolia in the Morro Mundo Novo should be confirmed currently in the field. Based on these evidences, we assess E. grandifolia as Endangered (EN), following criteria B1ab(i,ii,iii,iv)+2ab(i,ii,iii,iv) of IUCN (2012). We recommend the cultivation of E. grandifolia as an ornamental shrub in shade gardens to promote its ex situ conservation.

Taxonomic notes: —The inflorescences in racemes with pedicels less than twice as long as the flower internodes (ratio pedicel length/flower internodes 0.8–1.2:1), and with the main axis ending in a terminal bud, are morphological evidence to reliably assign E. grandifolia to E. sect. Racemosae O.Berg (see Mazine 2006; Mazine & Souza 2015; Mazine et al. 2016). The species can be promptly distinguished from all others of the same section in virtue of its large, subsessile leaves with cordate bases. Within Eugenia sect. Racemosae , leaves with cordate bases appear only in E. capparidifolia De Candolle (1828: 281) . Eugenia grandifolia differs by its leaf blades 16.5–30 × 4.5–12 cm ( vs. 2.5–7.5 cm long in E. capparidifolia ), chartaceous (vs. strongly coriaceous), inflorescences mostly ramiflorous ( vs. mostly axillary), and fruits slightly costate when young ( vs. smooth); another distinguishing feature between the two species is the presence of colleters found only in E. grandifolia .

Eugenia grandifolia shares subsessile leaves with cordate bases and ramiflorous inflorescences with E. monosperma Vellozo (1829: 209) , also endemic from the Atlantic Forest in southeastern Brazil (Mazine et al. 2020). In some localities of Rio de Janeiro State (e.g., municipality of Niterói), these two species co-occur, making misidentifications possible when vegetative. The main differences are that E. grandifolia has inflorescences in racemes ( vs. in glomerules or fascicles in E. monosperma ), ovaries with cinereous indumentum ( vs. ochraceous), and fruits 13–30 mm diam. when dry ( vs. ca. 10 mm diam. when dry). There are also some features that, while not diagnostic, can help to distinguish these species. Our field observations suggest that they differ in crown architecture, with E. grandifolia having longer branches that are more curved and may become pendent toward the apex (vs. shorter, straight and upward or tortuous in E. monosperma ). Leaf blades are usually longer in E. grandifolia ( 16.5–30 cm long vs. 7–21 cm long in E. monosperma ), always with opposite phyllotaxis (vs. phyllotaxis varying from opposite to verticillate). Interestingly, E. grandifolia often has more than one seed per fruit (2–7, Figure 2L ), while E. monosperma is known to have a single seed per fruit, like the vast majority of Eugenia species. Morphological descriptions and other information on E. monosperma , see Martius (1837: 81, under E. compactiflora Spring ex Martius [1837: 81] ), Valdemarin et al. (2020, 2024) and Mazine et al. (2020).

Materials from the Brazilian state of Bahia ( Silva 2178 and Mori 11491) are strikingly similar to E. grandifolia , especially in vegetative features, but these are rather most related to E. longifolia DC. (1828: 269) . These specimens differ as E. grandifolia have inflorescences in racemes (vs. fascicles), flowers with ovary densely covered with sericeous or cinereous trichomes (vs. brownish) and hidden (vs. not hidden) by the widely-deltoid bracteoles 3.8–4.5 mm long (vs. ovate bracteoles 1–1.5 mm long), fused at 1/3 of their length (vs. fused at the base). It is worth noting that we hypothesize that E. monosperma and those two specimens from Bahia are nested on Eugenia sect. Umbellatae O. Berg (1856: 204) based on their floral morphology (see Mazine et al. 2016 for the sections diagnostic key), being not closely related with E. grandifolia .

We have failed to find mature fruits of E. grandifolia , even after bagging fruiting branches in the field. A single fruit near maturation was found, with a firm, yellowish pulp. Interestingly, the species has a high number of seeds (up to 7) in comparison to its congeneric relatives, most of which have single-seeded fruits. Efforts for finding the mature fruits of this species is highly desirable, and their potential ecological and economical importance should be further investigated, especially considering that this endeavour could ultimately prompt the collection of seeds for ex situ conservation purposes.

In this study, the presence of colleters is first recorded in E. grandifolia ( Figure 3 ). Colleters can be associated with various parts of the plant, such as petioles, stipules, sepals, cataphylls, bracts, and bracteoles ( Silva 2010). However, in Eugenia sect. Racemosae , colleters have been found exclusively in reproductive structures, such as flowers, fruits, and bracts of inflorescences (Denardi et al. in prep.), which is consistent with the colleters observed in E. grandifolia .

Figures

FIGURE 1. Representative specimen of Eugenia grandifolia (Fernandes 922, RB). Image reproduced with the consent of RB Herbarium.

FIGURE 2. Morphology of Eugenia grandifolia in fresh state. A. Habit. B. Trunk. C. Detail of leaf base and petioles in the abaxial surface. D. Detail of leaf abaxial surface. E. Flowering branch with ramiflorous inflorescences and flower buds at early stages of development, notice the marcescent bracts (arrowhead). F. Detail of the racemes and flower buds at late stages of development. G. Flowers at anthesis with campanulate corolla. H. Detail of post-anthetic flowers with dry stamens. J. A pair of immature fruits with longitudinal ridges. K. Fruit near maturation with persistent and apparently accrescent calyx. L. Fruit near maturation with prismatic seeds spirally arranged. Photos: A–F and J–L by Thiago Fernandes, G–H by Marco Lacerda.

FIGURE 3. Morphology of the colleters in Eugenia grandifolia. A. Ramiflorous inflorescence with a single pair of flowers, bearing colleters (white arrows) in the axil of a bract scar (Fernandes 883, RB). B. Detail of the group of colleters showing the size inequality in the axil of a bract scar (black arrow) (Fernandes 883, NIT). C. Detail of the colleters (white arrows) located between the bracts and the axis an axillary inflorescence (Fernandes 893, RB). Photos by Thiago Fernandes.

FIGURE 4. Known distribution of Eugenia grandifolia within Rio de Janeiro State, Brazil.