Vismia Atlantica (Hypericaceae)

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Vismia atlantica (Hypericaceae), a new species previously thought to be well-known from the Brazilian Atlantic Forest Author(s): Lucas Cardoso Marinho Milena Ventrichi Martins André Márcio Amorim Volker Bittrich Source: The Journal of the Torrey Botanical Society, 143(3):330-337. Published By: Torrey Botanical Society DOI: http://dx.doi.org/10.3159/TORREY-D-15-00041 URL: http://www.bioone.org/doi/full/10.3159/TORREY-D-15-00041

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of the Torrey Botanical Society 143(3): 330–337, 2016.

Vismia atlantica (Hypericaceae), a new species previously thought to be well-known from the Brazilian Atlantic Forest1 Lucas Cardoso Marinho2,3 Universidade Estadual de Feira de Santana, Programa de Po´s-Graduaçaõ em Botaˆnica, Av. Transnordestina, Novo Horizonte, 44036-900, Feira de Santana, Bahia, Brazil Milena Ventrichi Martins Universidade Estadual de Campinas, Instituto de Biologia. Departamento de Biologia Vegetal, Rua Monteiro Lobato 255, 13083-862, Campinas, Saõ Paulo, Brazil Andre´Ma´rcio Amorim2 Universidade Estadual de Santa Cruz, Departamento de Cieˆncias Biolo´gicas, Km 25 Rodovia Ilheús- Itabuna, 45662-900, Ilheús, Bahia, Brazil Volker Bittrich Rua Mario de Nucci 500, 13083-290, Campinas, Saõ Paulo, Brazil

Abstract. Vismia atlantica, a new species endemic to the central region of the Brazilian Atlantic Forest, is described and illustrated. Collections of this species were initially identified as Vismia latifolia (probably because of a misinterpretation by Reichardt in Flora brasiliensis) and, more recently, as Vismia macrophylla. Vismia atlantica is part of a group of species having large leaves with numerous secondary veins and persistent stamens on the berries, features also present in the Amazonian species Vismia sandwithii. Key words: Bahia, Brazil, Esp´ırito Santo, Malpighiales, Vismieae Resumo. Vismia atlantica, uma nova espećie endemicaˆ da regiaõ central da Mata Atlanticaˆ brasileira, e´ descrita e ilustrada. Cole¸coes˜ dessa espećie foram inicialmente identificadas como Vismia latifolia (provavelmente como resultado de uma interpreta¸caõ erroneaˆ feita por Reichardt na Flora brasiliensis) e, mais recentemente, como Vismia macrophylla. Vismia atlantica faz parte do grupo de espećies de folhas grandes, com grande numero´ de nervuras secunda´rias e estames persistentes na baga, caracter´ısticas que tambe´m saõ vistas na espećie amazonica,ˆ Vismia sandwithii. Palavras-chave: Bahia, Brazil, Esp´ırito Santo, Malpighiales, Vismieae

Vismia Vand. currently has two subgenera: a recently published phylogeny, the African Vismia subg. Vismia, which comprises the neo- species of Vismia do not form a monophyletic tropical species, and Vismia subg. Afrovismia P. group with the two species included in the analysis Bamps, including the African species. However, in emerging within the genera Harungana Lam. and Psorospermum Spach, respectively (Ruhfel et al. 1 The authors would like to thank the Conselho 2011). Vismia comprises approximately 65 species Nacional de Desenvolvimento Cient´ıfico e Tecnologico´ with neotropical distributions, occurring from (CNPq) for the PhD Fellowship awarded to L.C.M. (grant 141561/2015-7), and for the Research Productivity Mexico to southeastern Brazil (Robson 1998). Fellowship awarded to A.M.A. (grant 306992/2012-4). Twenty-eight species are known from Brazil, Laboratory and field work was financially supported by occurring mostly in the Amazon basin, although CNPq (Edital Reflora Malpighiales grant 563548/2010-0, five occur in the central region of the Atlantic Edital Universal grant 486079/2013-9, and by Edital PPBIO grant 457483/2012-1). We also thank Maria do Forest: Vismia brasiliensis Choisy, Vismia guia- Carmo Estanislau do Amaral (IB-Unicamp) for her help nensis Aubl., Vismia martiana Reichardt, Vismia with the laboratory work, Domingos Cardoso for the pentagyna (Spreng.) Ewan (Bittrich et al. 2015), photographs of the flowers, and Klei Souza for the drawings. and one species usually identified as Vismia 2 Also with Centro de Pesquisas do Cacau, Herba´rio macrophylla Kunth (Robson 1998). CEPEC, Km 16 Rodovia Itabuna-Ilheús, 45650-970, Species of Vismia are trees, treelets, or shrubs Itabuna, Bahia, Brazil that produce exudate, and they usually have 3 Author for correspondence: [email protected] ferruginous branches more or less densely covered doi: 10.3159/TORREY-D-15-00041 ÓCopyright 2016 by The Torrey Botanical Society. with dendritic and/or stellate trichomes. The leaf Received for publication July 24, 2015, and in revised blades have strongly prominent secondary veins, form October 16, 2015; first published May 27, 2016. and there are generally glandular dots on the 330 MARINHO ET AL.: A NEW SPECIES FROM BRAZIL: VISMIA ATLANTICA 2016] (HYPERICACEAE) 331

FIG. 1. Geographical distribution of Vismia atlantica in the Atlantic Forest (black circles). Abbreviations: AF ¼ Atlantic Forest; CA ¼ Caatinga (dry forest); SA ¼ Savanna (Cerrado). abaxial surface (Ewan 1962, Robson 1998). Most Taxonomic Treatment species have a paniculate inflorescence with Vismia atlantica L. Marinho & M.V. Martins, sp. nov. pentamerous flowers, and the sepals and petals Holotype: Brazil, Bahia, Mun. Valen¸ca: entronca- often show glandular dots or canals (vittae). The mento de Valen¸ca, Serra do Abia´, Faz. Bom Jesus, stamens are arranged in fascicles, the berries are propriedade do Sr. Vanderley, 138180S, 398190W, ovoid or globose, and there are often persistent September 7, 2015 [bud, fl.], L. C. Marinho et al. sepals, styles, stigmas, and stamen fascicles (Ewan 1071 (holotype: CEPEC!; isotypes: HUEFS! RB! 1962, Robson 1998). UEC! Figures 1, 2, 3). The new species described here was first Vismia atlantica is characterized by the young collected two centuries ago during reconnaissance stems as well as the rachis and axis of the expeditions into areas occupied by cocoa planta- inflorescence densely appressed-tomentose with tions (Theobroma cacao L.) (agroforest systems brownish stellate trichomes, large leaf blades know as cabruca), and specimens have been (13.5–33 3 4.5–13.5 cm), base of leaf blades deposited in herbaria throughout the world, the cordate, rarely rounded, always with 18–29 pairs plant being very common and well-known to of secondary veins; floral buds orbicular to botanists. These collections were initially identi- ellipsoid, covered by densely appressed-tomen- fied as Vismia latifolia (Aubl.) Choisy or V. tose, ferruginous dendritic and stellate trichomes; macrophylla. However, the material from the petals suberect with black dots conspicuous only in Brazilian Atlantic Forest is different in various sicco; stamen fascicles with lanose trichomes on respects from these species, requiring the descrip- their central portion but absent on the free portion tion of a new species. and base; ovary cream-colored to whitish, some- 332 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143

FIG.2. Vismia atlantica L. Marinho & M. V. Martins. (A) Stem with young inflorescence. (B) Detail of trichomes on inflorescence. (C) Abaxial surface of leaf blade. (D) Detail of abaxial surface of leaf blade. (E) Floral bud. (F) Floral bud in preanthesis. (G) Sepals in outer and inner views. (H) Flower with two sepals and petals removed. (I) Petals in outer and inner views. (J) Gynoecium and staminodes (glands). (K) Fascicles of stamens in inner and outer views. (L) Mature berry. MARINHO ET AL.: A NEW SPECIES FROM BRAZIL: VISMIA ATLANTICA 2016] (HYPERICACEAE) 333 times with black dots, and horseshoe-shaped cream-colored to whitish, sometimes with black stigmas; sepals straight on mature berries, fascicles dots; stigmas horseshoe-shaped. Berries 1–1.5 3 persistent. 0.7–1 cm, whitish-green when immature, olive and Trees or treelets up to 12 m tall; stem 12–40 cm brown-purplish-dotted when mature, ovate or in diameter at breast height, branches brownish, rarely spherical; sepals, stamen fascicles, and leaf blades densely appressed-tomentose with styles persistent; sepals straight 6 patent on dendritic and stellate trichomes, and diminutive mature berries. Seeds ca. 100, approximately 20 whitish papillae; exudate orange to reddish. Leaves per locule, 1.8–2 3 0.5–0.7 mm, oblong to petiolate, opposite; petiole 15–22 mm long; leaf elliptical, curved, smooth. blades 13.5–33 3 4.5–13.5 cm, chartaceous to subcoriaceous, ovate to elliptic, apex acute, Distribution, Habitat, and Conservation sometimes acuminate, margin entire, sinuous, base Status. Vismia atlantica occurs in areas of cordate, rarely rounded, adaxial surface green and submontane and montane Atlantic Forest but shiny, abaxial surface pale olive-green; venation may also be found on coastal plains. The brochidodromous without additional intramarginal conservation status of V. atlantica was analyzed veins; surface brownish with stellate trichomes, according to the categories and criteria established densely appressed-tomentose abaxially, densely by IUCN (2012), combined with the GeoCAT tomentose and glabrescent when older adaxially; website (Moat 2007). The species can be consid- secondary veins 18–29 pairs; glandular black dots ered of Least Concern because it is widespread and present often covered by trichomes on abaxial abundant along the coast of Bahia State and northern Esp´ırito Santo State, Brazil, in secondary surface. Inflorescence terminal, paniculate, pyra- forest formations, cocoa plantations, and forest midal, up to 60 flowers, rachis 2.5–5.5 cm long (to edges. first primary lateral axis), densely appressed- tomentose, primary lateral axis 4–7 cm long, Comments. Vismia atlantica had been misiden- secondary lateral axis 1.7–4 cm long; bracts and tified as either V. latifolia or V. macrophylla. Its bracteoles absent; floral buds orbicular to ellipsoid. misidentification as V. latifolia was probably Flowers homostylous, pedicel 1.5–2.5 (4) mm because Reichardt (1878) incorrectly described long; sepals 5, unequal, 6–6.5 3 2.5–3 mm, elliptic and illustrated specimens of V. macrophylla as V. to ovate, apex acute to rounded, base truncate, latifolia in the Flora Brasiliensis. Vismia macro- abaxially densely appressed-tomentose with ferru- phylla can be confused with the new species ginous stellate trichomes, whitish papillae present because it has a similar leaf shape (ovate to elliptic on outer surface with four blackish linear glands with a cordate or rounded base) and persistent (vittae) on inner surface; corolla campanulate, stamen fascicles, which helps explain the large cochleate, petals 5, 9–10 3 4.5–5 mm, pale olive to numbers of historical misidentifications. cream-colored, elliptic, suberect with apical half In the field, V. atlantica can be distinguished slightly reflexed, subequal, straight, apex rounded, from V. macrophylla especially by the color of the base decurrent, lanose on inner surface, brown- trichomes on the abaxial surface of the leaves and purplish glandular dots on outer surface, becoming the outer surfaces of the sepals. The trichomes of V. visible only in sicco; stamen fascicles 5, 8–9 (11) macrophylla are grayish papillose, and there are mm long, white, compressed, filaments connate tiny papillae on the epidermis of leaves and floral except for apical portion, free portion 1.2–1.7 mm buds, resulting in the whitish color typical of its long, base wider than apex, lanose trichomes on structures. Light-colored papillae (whitish) also central portion, glabrous on the free portion and occur in V. atlantica, but its much denser indument base; anthers ca. 0.3 mm long, black gland of brownish stellate trichomes cover the whitish between thecae, apical portion of thecae often papillae resulting in distinctly dark brown buds (in blackish, ovary cream-colored to whitish, 1.8–2.5 contrast to the whitish coloration typical of V. mm long, ovate, lanose on apex; staminodes macrophylla). (glands) ca. 1 mm long, cream-colored to whitish, Vismia atlantica is associated with a group of oblong, the apex obtuse, with trichomes in the species (including the Amazonian species Vismia apical portion, persistent on berries; styles 1.8–2 sandwithii Ewan) that have persistent stamen mm long, sometimes with black dots, persistent on fascicles on their berries and large leaves with berries; ovary glabrous, 2–3 mm long, ovate, numerous secondary veins. Vismia sandwithii can 334 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143 be distinguished by its rounded to cuneate, but CEPEC, April 19, 1983 [bud, fl.], T. S. dos Santos never cordate, leaf blades bases; a complete 3861 (CEPEC, INPA); Rodovia Ilheús/Japu, absence of tiny, whitish epidermal papillae; and March 1987 [bud, fl.], M. Sobral et al. 5556 the presence of lanose trichomes on the free (CEPEC); Rodovia Ilheús/Serra Grande, July 20, stamen filaments. Different from both species 1995 [ste.], T. S. Santos et al. 4580 (CEPEC, mentioned above, the petals of V. atlantica are HUESC); Mamoan, November 15, 1995 [ste.], N. suberect with their apex slightly reflexed (vs. G. de Jesus and L. C. Queires 132 (HRB); Fazenda suberect with apical half strongly reflexed), with Nossa Senhora de Fa´tima, 148470S, 398020W, lanose trichomes on the central portion of the March 25, 1997 [fr.], L. A. Mattos-Silva et al. stamen fascicles (vs. absent), and generally without 3525 (ALCB, CEPEC, HUEFS, HUESC, NY); glands or canals (vittae) on the ovary and styles Fazenda Santa Maria, 148420S, 398110W, April 9, (vs. black dots) (Table 1). 2001 [ste.], R. H. R. Sambuichi 1380A (HUESC); Vismia atlantica differs from other species of the Assentamento Bom Gosto, 148410S, 398070W, central region of the Atlantic Forest by having leaf June 23, 2001 [ste.], M. L. Guedes et al. 9388 blades with cordate to rounded bases, secondary (ALCB); Fazenda Almada, 148470S, 398100W, July and intersecondary veins strongly prominent on 31, 2001 [fr.], R. H. R. Sambuichi s/n (CEPEC the abaxial surface, and fascicles of stamens with 89165, HUESC 6512); Salobrinho, 148470S, lanose trichomes persisting on the berries. 398100W, October 28, 2008 [fl.], L. A. Mattos- Silva and S. L. dos Santos 5063 (HUESC). Mun. Etymology. The species epithet refers to its Itacare´: estrada para Ubaitaba, September 4, 1970 endemic distribution in the Atlantic Forest. [fl.], T. S. dos Santos 1082 (CEPEC, NY); Fazenda Capitaõ, 148200S, 398050W, November 4, 2001 Studied Material (paratypes). BRAZIL:BAHIA: [fr.], W. W. Thomas et al. 12768 (CEPEC, NY); Mun. Amargosa, Serra do Timbo,´ 138100S, 8 0 8 0 398090W, January 25, 2007 [fl., fr.], D. Cardoso RPPN Capitaõ, 14 41 S, 39 10 W, January 24, 2015 [fr.], L. C. Marinho et al. 959 (CEPEC). et al. 1583 (CEPEC, HUEFS). Mun. Arataca, Serra 0 0 0 Mun. Itaju´ıpe: Rodovia Banco Central, 14840 S, do Peito de Mo¸ca, 15810 S, 39820 W, January 19, 0 2007 [fr.], A. M. Amorim et al. 6669 (CEPEC, 39822 W, November 18, 1971 [bud, fl.], T. S. HUEFS, NY). Mun. Belmonte, Ramal para o Rio Santos 2179 (CEPEC). Mun. Itubera´, Fragmento 0 0 Ubu, 158570S, 398060W, September 27, 1979 [bud, da Faz. Biriba, 13843 S, 39808 W, September 23, fl.], L. A. Mattos-Silva and J. L. Hage 609 2006 [fl.], R. Valadaõ and M. L. Guedes 728 (CEPEC). Mun. Cairu, Rodovia Nilo/Cairu, (ALCB). Mun. Medeiros Neto, Agrovila Pano- 0 0 138290S, 398020W, December 9, 1980 [fr.], A. M. rama, 17826 S, 40811 W, December 18, 2008 [fl.], Carvalho et al. 373 (ALCB, CEPEC, HRB). Mun. L. S. Almeida et al. 10 (HUEFS). Mun. Nova 0 0 Camacan: Rio Branco, 158250S, 398290W, July 11, Vi¸cosa, Aracruz, 17853 S, 39822 W, August 22, 1964 [fr.], C. M. Magalha˜es et al. 92 (CEPEC); 1993 [bud, fl.], M. L. Guedes et al. 2582 (HUEFS); Rodovia Camacan/Canavieiras, July 28, 1965 Mun. Aracruz, August 22, 1993 [fl.], M. L. Guedes [bud, fl.], R. P. Bele´m et al. 1398 (CEPEC, NY); et al. 2981 (ALCB, CEEPC, HRB). Mun. Porto Bisco,´ July 14, 1978 [bud], T. S. dos Santos and L. Seguro: PARNA Monte Pascoal, June 27, 1967 A. Mattos-Silva 3315 (CEPEC, INPA); RPPN [bud], J. P. Lanna Sob. et al. 1558 (CEPEC); Serra Bonita, 158230S, 398330W, July 17, 2009 January 15, 1973 [bud, fl.], T. S. dos Santos 2705 [fr.], A. M. Amorim et al. 7894 (CEPEC). Mun. (CEPEC); September 20, 1989 [fr.], G. Hatsch- Camamu, Barcelos do Sul, 138560S, 398060W, July bach 1989 (CEPEC); 158150S, 408340W, Novem- 18, 2005 [bud, fl.], A. M. Miranda et M. I. Silva ber 14, 1996 [fr.], W. W. Thomas et al. 11340 5166 (HUEFS, UEC). Mun. Entre Rios, RPPN (CEPEC, NY). Mun. Prado, PARNA do Desco- Fazenda Lontra/Saudade, 128540S, 408120W, Sep- brimento, 178110S, 398200W, November 3, 2009 tember 21, 1997 [fr.], N. G. Jesus 140 (HUESC). [fr.], L. Daneu et al. 214 (CEPEC, RB). Mun. Mun. Euna´polis: BR 5, 168220S, 398340W, Sep- Santa Cruz Cabra´lia, 168160S, 398010W, May 17, tember 28, 1966 [fl.], P. R. Bele´m and R. S. 1994 [fr.], M. L. Guedes et al. 3142 (ALCB). Mun. Pinheiro 2647 (CEPEC, NY); October 16, 1994 Santa Luzia, Fazenda Corrego´ Verde, 158250S, [fr.], A. J. Ribeiro et al. 427 (ALCB). Mun. Ilheús: 398200W, June 15, 1988 [bud], L. A. Mattos-Silva Rodovia BR-415, March 15, 1979 [fr.], L. A. et al. 2443 (ALCB, CEPEC, HRB, HUEFS). Mun. Mattos-Silva and J. L. Hage 311 (CEPEC, NY); Saõ Sebastiaõ do Passe´, Fazenda Panema, 128330S, 2016]

TABLE 1. Morphological comparisons between Vismia atlantica, Vismia latifolia, Vismia macrophylla, and Vismia sandwithii. MARINHO

V. atlantica V. latifolia V. macrophylla V. sandwithii Geographical domain Atlantic Forest Amazon Forest Amazon Forest Amazon Forest Papillae on leaf blades Present Absent Present Absent Indument type in young stems Densely appressed- Densely to sparsely appressed- Densely to sparsely appressed- Densely spreading-tomentose AL ET and inflorescence tomentose, tomentose, sometimes tomentose, sometimes

glabrescent glabrescent BRAZIL: FROM SPECIES NEW A .: Types of trichomes Stellate Dendritic and stellate Dendritic and stellate Stellate Base of leaf blades Cordate, rarely rounded Obtuse to rounded, sometimes Cordate to rounded Rounded to cuneate slightly cordate

Number of secondary veins (pairs) 18–27 14–18 10–22 9–14 (HYPERICACEAE) Shape of inflorescence Broadly pyramidal Slightly pyramidal Broadly pyramidal Narrowly pyramidal Shape of floral buds Orbicular to ellipsoid Oblong to ellipsoid Ellipsoid to ovoid Ovoid Papillae color on floral buds Whitish Papillae absent Grayish Grayish Color and density of trichomes on Densely ferruginous Scattered ferruginous Scattered ferruginous Spreading rufous external surface of sepals Petal orientation Suberect, with apical Suberect, not seen in vivo Suberect, with apical half Suberect, with apical half half slightly reflexed strongly reflexed strongly reflexed Trichomes on the central portion Present Present Absent Absent of fascicles

Trichomes on the free portion of Absent Absent Absent Present ATLANTICA VISMIA stamens Color of ovary and styles (in vivo) Cream-colored to Not seen White Yellowish whitish Glands on ovary and styles Black dots present on Not seen Dots present on ovary and Canals (vittae) present on ovary and styles, or styles ovary and styles only on styles, or black dots absent Persistence of fascicles on fruits Present Absent Present Present 335 336 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 143

FIG.3. Vismia atlantica L. Marinho & M. V. Martins. (A) Adaxial surface of leaf blade. (B) Abaxial surface of leaf blade. (C) Inflorescence with floral buds and flowers. (D) Detail of flowers. (E) Mature berries. (F) Detail of mature berries (A–B, E–F ¼ L. C. Marinho; C–D ¼ D. Cardoso).

388230W, March 27, 2001 [est.], G. Carvalho et al. 15, 2003 [fr.], R. N. Querino et al. 11 (ALCB, 24 (ALCB, CEPEC). Mun. Una: Esta¸caõ Experi- CEPEC, HUESC); Rodovia Uru¸cuca/Serra mental Lemos-Maia, Aug 27, 1980 [fr.], A. Grande, 148290S, 398060W, April 21, 2004 [bud], Rylands 22/1980 (CEPEC, INPA, RB); REBIO A. M. Amorim et al. 3972 (CEPEC, NY); Rodovia do Mico-leaõ, 158170S, 398040W, September 14, Serra Grande/Uru¸cuca, 148280S, 398040W, Sep- 1993 [bud, fl.], A. M. Amorim et al. 1381 (ALCB, tember 13, 2006 [fr.], M. C. Souza et al. 387 CEPEC, HRB, HUEFS, NY); REBIO de Una, (CEPEC). Mun. Valen¸ca: Rodovia Valen¸ca/Guai- September 26, 1996 [fr.], A. M. Amorim et al. 2003 bim, August 13, 1980 [bud, fl.], J. L. Hage et al. (CEPEC, NY); 158100S, 398080W, March 20, 1999 399 (CEPEC); Estrada para Maricultura, 138160S, [fr.], A. Martini et al. 97 (CEPEC, HUESC); 398590W, October 30, 2011 [fr.], E. Matos and G. Ecopark de Una, 158100S, 398030W, December 6, Vidal 710 (CEPEC, HUEFS); Serra do Abia´, Faz. 2006 [fr.], E. J. Lucas 1100 (CEPEC). Mun. Bom Jesus, propriedade do Sr. Vanderley, 138180S, Uru¸cuca: Serra Grande, 148350S, 398170W, Sep- 398190W, September 17, 2015 [bud, fl.], L. C. tember 7, 1991 [bud, fr.], A. M. Carvalho et al. Marinho 1072 et al. (CEPEC, RB). Mun. Wences- 3653 (CEPEC, HUEFS, NY); Rodovia Uru¸cuca/ lau Guimara˜es: Assentamento Oziel Alves, Serra Grande, August 24, 1992 [fr.]. A. M. Amorim 138370S, 398370W, August 13, 2001 [fl.], D. L. et al. 611 (CEPEC, NY); Serra Grande, November Santana et al. 763 (ALCB); 138410S, 398280W, MARINHO ET AL.: A NEW SPECIES FROM BRAZIL: VISMIA ATLANTICA 2016] (HYPERICACEAE) 337

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