Vaccinium bullatum (Dop) Sleumer (1941: 446)

Nuraliev, Maxim S., Fritsch, Peter W., Beer, Anton S., Tong, Yihua, Averyanov, Leonid V., Kuznetsov, Andrey N. & Kuznetsova, Svetlana P., 2020, A revision of Vaccinium bullatum (Ericaceae): floral morphology, distribution and typification, Phytotaxa 433 (1), pp. 55-66 : 56-62

publication ID	https://doi.org/ 10.11646/phytotaxa.433.1.6
persistent identifier	https://treatment.plazi.org/id/A941B756-210F-FA15-FF36-476DFCD4FAFC
treatment provided by	Felipe
scientific name	Vaccinium bullatum (Dop) Sleumer (1941: 446)
status

Treatment

Vaccinium bullatum (Dop) Sleumer (1941: 446) View in CoL ( Fig. 1–3 View FIGURE 1 View FIGURE 2 View FIGURE 3 ).

Literature: — Fang (1991: 101, Fig. 26 (2, 3)), Hiep & Ho (1996: 92, as “ Vaccinium bulbatum ”), Ho (2000: 617), Hiep (2003: 447), Fang et al. (2005: 486, Fig. 672 (2, 3)), Tang (2011: 651).

Basionym: — Agapetes bullata Dop (1930: 700) View in CoL .

TYPE: — VIETNAM. Tonkin [Hoa Binh]: [Da Bac district, Doan Ket, Phu Canh Mt.] massif de Nui bien, près Chobo , 1198 m, 1 September 1926, Poilane E. 13090 (lectotype: P, first-step lectotype designated by Sleumer 1941: 446, second-step lectotype designated here: P: P04022860!; isolectotypes: A: 00015986!; L: L0007945!; P: P04022861!). Images of lectotype and isolectotypes available at: http://mediaphoto.mnhn.fr/media/151574415835835NFsQ4JfZZ2ve7v, http://mediaphoto.mnhn.fr/media/1515744161197PKkPh96Cq0sg0Fs7, https://s3.amazonaws.com/huhwebimages/C10081C41588474/type/full/15986.jpg, http://medialib.naturalis.nl/file/id/L0007945_MLN/format/master

Description

Shrubs, epiphytic or epilithic, evergreen, to 2 m tall, sparsely branched, with fusiform swollen stem bases or roots. Branchlets, petioles, leaf blades, inflorescence rachises, bracts, pedicels, bracteoles, calyx, corolla, ovary, and fruit with white erect or ascending straight or more or less curved trichomes to 0.3(to 0.5) mm long mixed with more scattered erect to appressed ferrugineous (darkening to black on old branchlets and leaf blades) stalked glandular trichomes to 0.10(–0.15) mm long, often glabrescent. Mature branchlets reddish brown, more or less terete but irregularly ridged, 3–4 mm thick, densely lenticellate ( Fig. 2a–c View FIGURE 2 ); epidermis grayish, peeling around lenticels; perennating buds with multiple overlapping scales. Leaves alternate, scattered, distichously arranged ( Fig. 2a–c View FIGURE 2 , 3c View FIGURE 3 ); petiole 1–3 mm long, 2.3–2.8 mm in diam.; leaf blade ovate or narrowly ovate, or rarely narrowly oblong-ovate or lanceolate, larger leaves on each branch 9–16 × 3.9–8.1 cm, 2.1–3.3 times as long as wide, coriaceous, green in vivo and dark green or brown in sicco adaxially, pale green in vivo and brown in sicco abaxially, both sides slightly shiny, adaxial surface bullate, i.e., with convex sections flanked by sulcate major veins; adaxial surface glabrous except puberulous at base along major veins; abaxial surface with white trichomes mainly on major veins and glandular trichomes mainly on surface proper, with both types of trichomes when caducous leaving a faintly punctate scar; base subrounded, rounded, subtruncate, or subcordate; margin entire, slightly revolute, with one sessile dark basal gland 1.0– 1.2 mm in diam. per side that often forms a shallow lobe at margin ( Fig. 2b View FIGURE 2 ); apex acute to caudate-acuminate, or rarely obtuse; midvein sulcate adaxially but with a strong central ridge, strongly raised abaxially; secondary veins pinnately arranged, sulcate adaxially, raised abaxially, 7 to 12 on each side of midvein or to 20 when including smaller veins that do not reach the margin, more or less arc-ascending, often meeting in a closed loop before reaching margin, often some veins straighter, smaller, and not reaching margin situated between larger arching veins; tertiary veins slightly sulcate adaxially, raised abaxially.

Inflorescences axillary and pseudoterminal, indeterminate (racemose and developing mostly beyond the confines of the perennating buds), 1(to 3) per axil, 1.5–9.0 cm long at anthesis, 8- to 14-flowered ( Fig. 2b View FIGURE 2 , 3e View FIGURE 3 ); peduncle and rachis green flushed red in vivo; bracts caducous, maroon to black in vivo, narrowly deltoid, cucullate, 1.6–2.5 × 0.6–1.0 mm, chartaceous, adaxially glabrous, abaxially pubescent, margin entire, apex acute. Flowers articulated with pedicel, 5-merous, 5.5–7.5 mm long ( Fig. 1a View FIGURE 1 , 2d–g View FIGURE 2 ). Pedicels green flushed red in vivo, 4–7(– 9 in fruit) mm long and 0.65–0.75(–0.80) mm thick at anthesis, slightly expanded to 1.00(–1.15) mm towards apex; bracteoles 2, borne at base of pedicel (or slightly above), opposite, caducous, maroon to black in vivo, narrowly deltoid, cucullate, 1.4–1.7 × 0.4–0.6 mm, chartaceous, margin entire, apex sharply acute. Calyx (without ovary) green flushed red in vivo, erect, cupuliform, 1.8–2.2 mm long ( Fig. 2f,i View FIGURE 2 ); connate portion (tube) 0.25–0.30 mm long; lobes 5, slightly incurved (appressed to corolla), narrowly ovate-deltoid to oblong-deltoid, 1.3–2.4 × 0.8–1.1 mm, pubescent on both sides but pubescence less dense than on ovary and tube, margin entire, smooth (e.g., without sessile glands), apex acute, without terminal gland. Corolla in bud closed and strongly 5-ribbed in line with petal midveins ( Fig. 2b View FIGURE 2 ); gamopetalous for ca. 2/3 length, at anthesis whitish except bright red along petal midveins, broadly campanulate, ca. 5–6 mm long, 4.0– 5.5 mm in diam., outside with glandular trichomes mainly within ca. 0.5 mm on each side of petal midvein and more sparsely white-puberulent closer to midvein, inside glabrous; lobes 5, reflexed in vivo, erect in sicco, deltoid or narrowly deltoid, ca. 2.0 × 2.2 mm, sometimes with several long setae adaxially near apex ( Fig. 1a View FIGURE 1 , 2d–g View FIGURE 2 ). Stamens 10, dimorphic with respect to pores and spurs, free from corolla, distinct from each other but slightly conjoined by lateral sides of thecae, ca. 4.5–5.0 mm long ( Fig. 1 View FIGURE 1 , 2d,e,g,h View FIGURE 2 ); filaments bent inwards, ca. 1.5–2.3 mm long, margins sparsely white-villous in sicco (white-lanate in vivo) with trichomes to 0.35 mm long ( Fig. 1 View FIGURE 1 ); anthers dorsifixed with filament attached at distal part of theca, ca. 3.6–4.5 mm long, introrse, with 2 spurs each ( Fig. 2g,h View FIGURE 2 ); anther thecae ca. 1 mm long, papillate; anther tubules parallel, ca. 3.5 mm long, opening by strongly oblique ventral apical pores 0.90–1.19 mm long on antesepalous anthers and 1.20–1.35 mm long on antepetalous anthers, pore apex acute ( Fig. 1 View FIGURE 1 ); anther spurs borne dorsally at base of tubules, strongly curved, ca. 0.8–1.1 mm long, those on antesepalous stamens extending laterally outside of antepetalous anthers and strongly overlapping with spurs of next antesepalous stamens, those on antepetalous anthers strongly hooked outward below spurs of antesepalous stamens ( Fig. 1 View FIGURE 1 ). Antesepalous anthers slightly closer to flower center than antepetalous anthers ( Fig. 1b View FIGURE 1 ). Ovary inferior, dark green in vivo, slightly obconic ( Fig. 1a View FIGURE 1 , 2f,g View FIGURE 2 ), 0.8–1.7 mm long, 1.7–2.0 mm in diam., terete in vivo, slightly 5-ribbed in bud in sicco, 5- locular with incomplete false septa protruding to not more than 1/2 of each locule ( Fig. 3a,b View FIGURE 3 ); disk annular, occupying the entire area within the corolla tube, 1.45–1.90 mm in diam., glabrous or pubescent ( Fig. 2g,i View FIGURE 2 ); style slightly exserted from corolla ( Fig. 2d–h View FIGURE 2 ), ca. 4.7–5.0 mm long, glabrous or basally pubescent. Infructescences 4.7–13.4 cm long. Fruit (berry) reportedly white, globose, 6.0–7.5 × 6.5–7.5 mm excluding calyx, fleshy, pubescent, pseudo-10-locular, bearing persistent calyx with erect-incurved lobes 1.5–3.5 mm long ( Fig. 3d View FIGURE 3 ).

Nomenclatural notes: —The protologue of Agapetes bullata ( Dop 1930) includes a description of the species together with the type locality as “ Tonkin: massif de Nui-bien, près Cho-bo” and a collector name as “Poilane”. In publishing the combination under the genus Vaccinium, Sleumer (1941) indicated the collection number of the type specimen as well as the herbarium of its deposition: “Poilane n. 13090, Typus in Herb. Mus. Paris”, which appears to fulfill the conditions of lectotypification (Art. 7.11 of ICN, Turland et al. 2018; see also McNeill 2014). However, we have found that there are two specimens of the collection Poilane E. 13090 deposited in P (P 04022860 and P 04022861) and thus Sleumer’s choice (1941) was the first-step for lectotypification (Art. 9.17). We have selected the specimen at P with barcode P 04022860 as the lectotype in the second-step because it has the original label, unlike the other one. The specimens at A (00015986) and L (L0007945) were distributed from P, which is evident from the notes that they contain. These two specimens as well as P 04022861 at P are isolectotypes.

Morphological notes: —1. Although the original label of the lectotype states “fleurs blanchatres”, the flowers are in fact absent from the four type specimens that we have studied. This is consistent with the treatment in the Flora of China ( Fang et al. 2005) which states “Flowers unknown”. Among the specimens that we were able to locate, several contain flowers, i.e., Averyanov L.V. et al. HAL 12808, Averyanov L.V. et al. LX-VN2334, Averyanov L.V., Hiep N.T. VH 4961, Chinese Botany United Guangxi Team 1698, Huang Y.S., Nong D.X. Y0684, Nuraliev M.S. 1071, Phuong 2043, Qin H.N. et al. 603033, Xu W.B. et al. 9608, most of them made after the publication of Flora of China ( Fang et al. 2005). As far as we are aware, the flowers of this species have not been described nor illustrated to date, and thus this is accomplished in our work for the first time.

2. Uncertainty exists regarding the distinction between 5-locular, 10-locular and pseudo-10-locular ovaries in several taxa of Vaccinium . It is most likely that gynoecia of 10 carpels, i.e., the truly 10-locular ones, are not found in Vaccinium s.str. (excluding Rigiolepis Hooker f. 1873: 54 , t. 1160) ( Stevens et al. 2004, Fang et al. 2005, Vander Kloet 2005, Argent 2019), and the indications of 10-locular ovaries in Vaccinium (e.g., Vander Kloet 2005, Vander Kloet & Dickinson 2009), including V. bullatum ( Vander Kloet & Dickinson 2005) , are errors likely from inaccurate observations. The absence or presence of false septa, i.e., a 5-locular vs. pseudo-10-locular ovary, has been widely used in the taxonomy of Vaccinium (see below). However, these conditions appear not to be perfectly discrete, as follows from our investigation. Indeed, in V. bullatum , the anthetic false septa are considerably incomplete, and the ovary can be described as 5-locular with V-shaped locules ( Fig. 3a,b View FIGURE 3 ). The pseudo-10-locular condition that is usually assigned to this species ( Fang et al. 2005, Vander Kloet & Dickinson 2009) apparently becomes more evident in fruits. Therefore, this character depends on the stage of the flower/fruit under study, and we thus argue that examination of a range of phenological stages is needed for its reliable evaluation.

Ecology and phenology:— Vaccinium bullatum grows in mountainous areas and limestone hills, in broad-leaved forests, at 600–2000 m a.s.l. Flowering: (February)May–June; fruiting: (July)August–March.

Distribution: — Vaccinium bullatum is distributed in Guangxi Zhuang Autonomous Region, China and the Vietnam provinces of Lao Cai, Cao Bang, Tuyen Quang, Vinh Phuc, Phu Tho and Hoa Binh as well as in the Tam Dao massif (without precise location).

The distribution of V. bullatum is presented in Fig. 4 View FIGURE 4 , based exclusively on the specimens examined in our study (see Appendix).

Vernacular names: — Chinese : 泡泡叶•橘; Vietnamese: Sõn trâm phồng; Việt quất lá bọt.

Sectional placement: —There is some uncertainty as to the sectional placement of Vaccinium bullatum . Sleumer (1941) placed the species in V. sect. Galeopetalum J.J.Sm. in Boerlage (1912: 101), characterized by this author as having large evenly scattered evergreen leaves with multiple secondary veins and entire margins, axillary indeterminate racemose inflorescences that develop mostly beyond the confines of the perennating bud, campanulate corolla divided to ca. the middle, two prominent spurs per anther, long-erect anther tubules, and pseudo-10-locular ovaries. Sleumer’s decision was adopted by Fang (1991). Vander Kloet & Dickinson (2005) separated some of the species in this section into the new section V. sect. Calcicolus Kloet in Vander Kloet & Dickinson (2005: 451) on the observation that the species in the latter section actually have determinate inflorescences and these develop entirely within the confines of an enlarging perennating bud, unlike the species remaining in V. sect. Galeopetalum . This separation is supported by phylogenetic analysis based on DNA sequence data ( Kron et al. 2002 and unpubl. data, in Vander Kloet & Dickinson 2005), although species sampling within the two sections was limited. Moreover, although not noted by Vander Kloet & Dickinson (2005, 2009), the species of V. sect. Calcicolus lack swollen stem bases or roots (Y.-H. Tong, pers. obs.), whereas those of V. sect. Galeopetalum possess them ( Sleumer 1967; Vander Kloet & Dickinson 2005).

Vander Kloet & Dickinson (2005) excluded Vaccinium bullatum from V. sect. Calcicolus perhaps based on its indeterminate inflorescence, and this exclusion is supported by the presence of swollen stem bases or roots in the species (Y.-H. Tong, pers. obs.). They indicated several additional features of this species distinctive from those of V. sect. Calcicolus, namely, a 10-locular ovary and seeds with thin white testa surrounding a green embryo (drying black). However, our study clearly shows that V. bullatum possesses a pseudo-10-locular ovary rather than a 10-locular ovary; this feature thus appears to be consistent with both V. sect. Calcicolus and V. sect. Galeopetalum s.str. Vander Kloet & Dickinson (2009) subsequently referred V. bullatum to V. sect. Euepigynium Schlechter (1919: 174) . The basis for this decision, however, is not clear because the members of this section have palmate leaf venation whereas V. bullatum has pinnate venation. The retention of V. bullatum in V. sect. Galeopetalum (excluding the species of V. sect. Calcicolus) appears to be justified in our investigation on the basis of the above characters as well as its slightly conjoined anthers, which also are possessed by some species of this section ( Vander Kloet 2002). However, V. bullatum appears to key to couplet 28 in the key to Vaccinium sections in Vander Kloet & Dickinson (2009) (which unites sections Bracteata Nakai (1927: 234) , Eococcus Sleumer (1941: 420) and Euepigynium ) and both leads in this couplet appear to be false for V. bullatum because of leaves with entire margin and pinnate venation in the species. Moreover, within the key, V. bullatum does not fit V. sect. Galeopetalum because this species possesses a long inflorescence rachis; notably, the assumed character of a short rachis in V. sect. Galeopetalum is in fact not mentioned in any other source. Thus, similar to Stevens (1969), we assert that the species of this section need more detailed morphological documentation. In this regard, our expanded description of V. bullatum can serve as a model for such documentation to make further progress on the delimitation of these and related sections in Vaccinium .