A New Species of Utricularia (Lentibulariaceae) from Chapada dos Veadeiros (Central Brazil) Author(s): Paulo Cesar Baleeiro Souza and Claudia Petean Bove Source: Systematic Botany, 36(2):465-469. 2011. Published By: The American Society of Plant Taxonomists URL: http://www.bioone.org/doi/full/10.1600/036364411X569642

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Systematic Botany (2011), 36(2): pp. 465–469 © Copyright 2011 by the American Society of Plant Taxonomists DOI 10.1600/036364411X569642

A New Species of Utricularia (Lentibulariaceae) from Chapada dos Veadeiros (Central Brazil) Paulo Cesar Baleeiro Souza1,2 and Claudia Petean Bove1 1

Laboratório de Plantas Aquáticas, Departamento de Botânica, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, Rio de Janeiro 20940-040, Brazil 2 Author for correspondence ([email protected]) Communicating Editor: Kenneth M. Cameron

Abstract—A new species, Utricularia densiflora, from the Brazilian savanna (Cerrado) is described and illustrated. This species was found growing at the Chapada dos Veadeiros National Park, and is distinguished from the other species in the genus by the presence of several rudimentary (or dormant) floral buds, sessile glands in the peduncle, and highly congested inflorescence. Utricularia densiflora is here considered a member of section Oligocista and is morphologically similar to U. erectiflora and U. meyeri. A key of the Utricularia species inhabiting the Chapada dos Veadeiros National Park is provided. Resumo—Uma nova espécie, Utricularia densiflora, do Cerrado brasileiro é descrita e ilustrada. Essa espécie foi encontrada no Parque Nacional da Chapada dos Veadeiros. Distingue-se das demais espécies do gênero pela presença de muitos botões florais rudimentares (ou dormentes), glândulas sésseis no pedúnculo e inflorescência altamente congesta. Utricularia densiflora é aqui considerada membro da seção Oligocista e morfologicamente semelhante à U. erectiflora e U. meyeri. É disponibilizada uma chave de identificação das espécies ocorrentes no Parque Nacional da Chapada dos Veadeiros. Keywords—aquatic plant, Brazil, Cerrado, Chapada dos Veadeiros, new species, taxonomy.

light microscope (LM) with capture system composed by camera Q, color 5 and software Image Pro-Express. The seed surface was airdried, mounted and coated with a gold-palladium (40–60%), and then observed using a Jeol JSM 6390 LV Scanning Electron Microscope (SEM); both process at the Museu Nacional do Rio de Janeiro (UFRJ), Brazil.

Utricularia L. is the largest genus of Lentibulariaceae and all carnivorous plants, with species distributed worldwide and diversified in tropical regions (Taylor 1989; Jobson et al. 2003; Müller and Borsch 2005; Guisande et al. 2007). According to the Brazilian species list of Lentibulariaceae undertaken by Miranda and Rivadavia (2010), Utricularia is represented by 67 species, distributed among various biomes, ca. 48 species occurring in the Brazilian Cerrado vegetation. Since Taylor’s monograph (1989), a single new species, U. cochleata C. P. Bove, has been described for this domain (Bove 2008). The Cerrado is a hotspot for conservation due to its great biological diversity and high endemic index (ca. 44% of the species), but unfortunately it has lost about 55% of their original territory due to human impacts (Klink and Machado 2005), with only small areas under protection, such as the Chapada dos Veadeiros National Park (State of Goiás), created in 1961 and which has been recognized by UNESCO as a World Natural Heritage Site since December 2001. This Park is a highland complex of 65,514 ha with altitudes ranging from 500– 1,650 m (Munhoz and Felfili 2006). The region is composed by many diverse habitats, such as open fields (grasslands) and swampy areas near streams lined with the palm tree Mauritia flexuosa L. f., a habitat known regionally as “veredas.” While undertaking a floristic survey of Utricularia in the Cerrado, a new Utricularia species was found and is here described.

Taxonomic Treatment Utricularia densiflora Baleeiro & C. P. Bove, sp. nov.—TYPE: BRAZIL. Goiás: Município de Alto Paraíso de Goiás, Parque Nacional Chapada dos Veadeiros, Serra da Baleia, 1,100 m, 3 Jun 2009, P. C. Baleeiro 21, C. P. Bove 2020, A. L. R. Oliveira & R. Couto (hototype: R!; isotypes: K!, SPF!). Hidrostadia herbacea. Utriculi foliis, stolonibus, ramis et rhizoideis. Inflorescentia erecta, satis congesta, scapo variis glandulis essilibus, racemo ca. 15 floribus flavis, ca. 5 mm longis; ca. 20 alabastris abortivis subintelectis unusquodque bractea, inflorescentiae mox infra. Hydrophytic herb. Rhizoids few or many 2–6, from the base of the peduncle, filiform, 5–32 × 0.2–0.4 mm, bearing papillose branches up to 8 mm long, sometimes branched. Stolons numerous, filiform, branched, up to 8 cm long, ca. 0.2 mm thick. Leaves from the stolons, peduncle base and rhizoids, petiolate, lamina linear to narrowly obovate, apex rounded, 1-nerved; up to 18 × 1 mm. Traps numerous on the leaves, stolons, stolon branches, rhizoids and rhizoid branches, globose, sometimes with a prominent ventral, chin-like swelling, ca. 1 mm long, subsessile or stalked, mouth basal with double, conical, dorsal appendages, outer surface of the trap papillose, trap interior with bifid glands. Inflorescence with spirally arranged bracts and flowers, ca. 10 cm long. Peduncle sometimes sparsely branched below,

Materials and Methods The type specimen described below is deposited as spirit in R, SPF and K (acronyms after Thiers 2010). General morphology and measurements were undertaken with a stereoscope and light microscope. A paradermic section of the peduncle was done for sessile glands visualization. The image was obtained by a Olympus BX – 51

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terete, 1 mm thick, bearing numerous sessile glands densely concentrated near the base. Scales ca. 3, ovate, apex acute, 0.6–1.0 × 0.3–0.5 mm. Rudimentary (or dormant) buds below the lowermost opened flower, (7–)15–23 congested above and becoming lax towards peduncle base. Bracts strongly convex, margins curved inwards, broadly ovate with apex acute or acuminate, 1.8 × 1.5 mm. Bracteoles linear, 0.7 × 0.2 mm. Calyx lobes unequal, ovate, upper lobe 2.0 × 1.0 mm, apex rounded, lower lobe 1.8 × 1.2 mm, apex acute. Corolla pale yellow, 0.5 mm long. Filaments almost straight, 0.6 mm long, anther thecae distinct, 0.3 mm long. Ovary globose, 0.4 mm long, style very minute, stigma lower lip semicircular, upper lip inconspicuous. Flowers 5–16, located above the rudimentary buds, densely congested, pedicel erect, filiform, 1.7 mm long. Bracts basifixed, ovate to widely ovate, with apex acute 1.5–3 × 1–2 mm. Bracteoles lanceolate to narrowly ovate, ca. 1.0 × 0.4 mm. Calyx lobes subsimilar, decurrent at the base, green with winy apex, accrescent enclosing the capsule, margins strongly involute, obscurely nerved; lower lobe ovate, apex obtuse, 3 × 2.3 mm, upper lobe widely ovate with apex acute or acuminate, 3 × 3 mm. Corolla yellow, 3–5 mm long; upper lip oblong, constricted near the center, apex rounded or slightly truncate, entire; lower lip galeate, approximately circular in outline, slightly swollen near the base, entire or emarginated apex. Palate with a raised, microscopically ciliate rim. Spur subulate, curved upwards, with acute apex as long as the lower calyx lobe. Filaments almost straight, 1.1 mm long, anther thecae distinct, 0.8 mm long. Pollen 4–5-colporate. Ovary globose; style short; stigma bilabiate, lower lip semicircular, recurved, upper lip similar but smaller. Capsule globose, glabrous, up to 2.3 mm. Seeds broadly ovoid, 0.25–1.0 mm long, testa reticulate, testa cells elongated with boundaries raised, straight to somewhat sinuate, slightly granulose, large lumina longitudinally striate with bridges connecting the stria beneath. Etymology—From the Latin densus (a, um) plus flora, in reference to the extremely congested flowers on the inflorescence (Fig. 1A). Geographic Distribution and Ecology—Although extensive field work was carried out at the Chapada dos Veadeiros, as well as careful examination of Utricularia collections from central Brazil (CEN, HEPH, HMS, IBGE, NX, UB, UFG, R, RB, SP and SPF), U. densiflora is thus far only known from one locality, near the Serra da Baleia, located within the Chapada dos Veadeiros National Park, Goiás state. Utricularia densiflora occurs sympatrically with Eriocaulon aff. heteropeplon Silveira in natural pools of water ca. 7 cm deep among grasslands.

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Conservation Status—According to the IUCN (IUCN 2001) U. densiflora is here classified as Near Threatened (NT). Discussion Oligocista A. DC. is the largest section in the genus Utricularia (37 species), but only a few species occur in the neotropics (six species). Utricularia densiflora is here considered a member of this section, due to its galeate lower lip corolla, divergent spur, calyx lobes subsimilar enclosing the capsule, external morphology and internal glands of the traps, and pollen morphology. Additional features include simple leaves, basifixed relatively broad bracts, bracteoles present, and seed morphology (Fig. 2B). Utricularia densiflora is morphologically most similar to U. erectiflora and U. meyeri due to the upper corolla lobe shape, involute calyx margin, with decurrent base, and narrow leaf lamina with rounded apex. The lower corolla lobe of U. densiflora resembles that of U. meyeri, which has less congested inflorescences. Utricularia densiflora is unique in having rudimentary buds subtended by bracts along the peduncle; strongly congested raceme, numerous sessile glands near the peduncle base (Fig. 2A) becoming scarce towards the apex; spur as long as the lower calyx lobe and rhizoid branches somewhat ramified (Table 1). The rhizoids in Utricularia densiflora are the biggest of the section (up to 3.5 cm long while those of U. meyeri Pilg. are up to 2 cm long); interestingly, these rhizoids branch profusely, a rare feature in the genus. In section Oligocista branching rhizoids are only seen to a lesser degree in U. letestui P. Taylor (Taylor 1989). Presumably the size of the rhizoids and the number of branches enhance the anchoring function of the relatively large inflorescences of U. densiflora in its shallow water habitat. The rudimentary buds resemble large scales at first glance (Fig. 1A). The bracts are wider than the calyx lobes, although somewhat shorter, bearing a minute corolla, gynoecium, and androecium. Taylor (1989:18) mentioned just one rudimentary bud in several species of section Pleiochasia (Kamien´ski) Barnhart, U. simplex R. Br. in section Australes P. Taylor and U. warmingii Kamien´ski in section Utricularia P. Taylor. The single rudimentary buds described by Taylor are rare occurrences in the species cited, which was not mentioned by him in the specific detailed descriptions. All U. densiflora inflorescences studied at the type population presented numerous rudimentary buds, thus clearly an autapomorphy. Twenty two species of Utricularia have been recorded for Chapada dos Veadeiros National Park (P. C. Baleeiro, pers. obs.). An identification key for this region is provided below.

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Fig. 1. Utricularia densiflora. A – B. Habit. A. Apex of plant with raceme and rudimentary buds. B. Base of plant with scales and peduncle base with: B1 – rhizoids, B2 – stolon and stolon branches, B3 - leaf and traps. C. Trap detail. D. Aerial inflorescence view. E. Rudimentary bud lateral view. F. Rudimentary bud longitudinal section. G. Bract. H. Bracteoles. I. Flower with bract and bracteoles. J. Corolla lateral view. K. Corolla upper lobe. L. Calyx. M. Pistil and stamens. N. Calyx enclosing the young capsule. (P. C. Baleeiro 21 et al.).

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SYSTEMATIC BOTANY

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Utricularia densiflora. A. LM of peduncle base showing the sessile glands (white arrow in one of them). B. SEM of seed.

Key to Species of UTRICULARIA from Chapada dos Veadeiros, Goiás State, Brazil 1.

Bracts basisolute . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2. Bracteoles present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. pubescens 2. Bracteoles absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3. Corolla yellow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 4. Spur of corolla twice as long as the lower lip . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. nigrescens 4. Spur of corolla as long as the lower lip or smaller . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 5. Nerves of calyx lobes obscure or absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. trichophylla 5. Nerves of calyx lobes prominent or distinct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 6. Nerves of calyx prominent, extending to the rounded apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. triloba 6. Nerves of calyx distinct, not extending to the rounded apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. subulata 3. Corolla violet or white . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7. Leaves divided into capillary segments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. neottioides 7. Leaves not divided into capillary segments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 8. Trap mouth with a single ventral appendage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. cucullata 8. Trap mouth with no appendage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. myriocista 1. Bracts basifixed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 9. Bracteoles and scales absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 10. Peduncle distinct, ca. 2 mm long, bract boat-shaped, hyaline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. biovularioides 10. Peduncle extremely short, ca. 0.5 mm long or apparently absent, bract transversally oblong, not hyaline . . . . . . . . . . . . . . . . . . . . U. olivacea 9. Bracteoles and scales present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 11. Corolla yellow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 12. Bracts, bracteoles and scales margins fimbriate-dentate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. simulans 12. Bracts, bracteoles or scales margins laciniate or entire . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 13. Leaves dimorphic, corolla 1.5–2.0 cm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. praelonga 13. Leaves not dimorphic, corolla up to 1.0 cm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 14. Spur conical, wider than long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. guyanensis 14. Spur subulate, much longer than wide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 15. Traps without appendages, long stalked, upper calyx lobe with prominently raised nerves . . . . . . . . . . . . . . . . . U. nana 15. Traps with two dorsal appendages, stalked or sessile, upper calyx lobe without prominently raised nerves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 16. Dormant buds present on the peduncle, pedicel about half as long as the calyx . . . . . . . . . . . . . . . . . . . U. densiflora 16. No dormant buds on the peduncle, pedicel about as long as the calyx . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. laxa 11. Corolla violet or white . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 17. Bracts and bracteoles basally connate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 18. Lower corolla lip ca. 2 cm wide, not lobed or very shallowly 3- lobed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. tricolor 18. Lower corolla lip 0.25–1 cm wide, distinctly 3-lobed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. amethystina 17. Bracts and bracteoles not basally connate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 19. Calyx with raised, prominent nerves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. purpureocaerulea 19. Calyx nerves not prominent or raised . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 20. Capsule narrowly ellipsoid to very narrowly ovoid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. tenuissima 20. Capsule globose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 21. Lower corolla lip 4-lobed and upper lip 2-lobed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. laciniata 21. Lower corolla lip slightly 3-lobed and upper lip entire . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . U. hispida

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Comparative diagnostic characters among Utricularia densiflora, U. erectiflora, and U. meyeri.

Rhizoids Peduncle and stolon Leaves Traps

Bracteoles Bracts with rudimentary (or dormant) floral buds Corolla Calyx lower lobe apex Relationship between spur and lower calyx lobe

U. densiflora

U. erectiflora

Few to numerous With several sessile glands Few from the peduncle base and numerous from the stolons Numerous on the leaves, stolons and stolon branches, few on rhizoids

Few Glabrous None from the peduncle and numerous from the stolons Occasionally on leaves, numerous on the stolons, apparently absent from rhizoids As long as the bract. Linear

Numerous Glabrous None from the peduncle and few from the stolons Few on the stolons and rhizoids

None

None

3–5 mm Entire, reddish

8–12 mm Shortly bifid, green

15–20 mm Shortly bifid, green

Equal in length

2 times longer

3–4 times longer

Shorter than the bract. Lanceolate to narrowly ovate (7-)15–23

Acknowledgments. This research was carried out with financial support of Postgraduate Program in Biological Sciences (Botany) – National Museum of Universidade Federal do Rio de Janeiro and Conselho Nacional de Pesquisa e Desenvolvimento- CNPq (grant to P. C. Baleeiro). We thank Dr. Pedro Carauta for the Latin diagnosis, Dr. Gabriel Bernadello for suggestions on the manuscript, Fernando Rivadavia for English revision, Ricardo Moura for aid in choosing the plant name, Adriana Oliveira for the Eriocaulon identification and for aiding Figure 2 organization. Fieldwork could not have been conducted without the valuable assistance of Adriana Oliveira and Ricardo Couto. We also thank SISBIO/IBAMA for the license to carry out our fieldwork, and Daniel Reis, director of Veadeiros National Park, for field work facilities. We thank the curators of the following herbaria for kindly providing access to their collections: CEN, HEPH, HMS, IBGE, NX, UB, UFG, R, RB, SP, and SPF. Finally, we thank two reviewers for the excellent suggestions. Literature Cited Bove, C. P. 2008. A new species of Utricularia (Lentibulariaceae) from Central Brazil. Revista Brasileira de Botânica 31: 555–558. Guisande, C., C. Granado-Lorencio, C. Andrade-Sossa, and S. R. Duque. 2007. Bladderworts. Functional Plant Science and Biotechnology 1: 58–68. IUCN. 2001. IUCN red list categories and criteria, version 3.1. IUCN, Gland, Switzerland & Cambridge: Information Press.

U. meyeri

Slightly shorter than the bract. Linear

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