Bixa atlantica Antar & Sano, 2022

Medeirosantar, Guilherme, Lírio, Elton Johnde, Pereiraalmeida, Roberto Baptista & Sano, Paulo Takeo, 2022, Bixa atlantica sp. nov. (Bixaceae), a new species of wild annatto from the Atlantic Forest of eastern Brazil, Phytotaxa 544 (2), pp. 171-184 : 173-178

Bixa atlantica Antar & Sano sp. nov.

Type:— BRAZIL. Espírito Santo: Vila Pavão.Barra da Rapadura, fazenda do sr. Wagner Scardini , Floresta Estacional Secundária , 18º42′18″S, 40º35′28″W, 157 m, 16 Fev 2014 [fl., fr.], R.C. Forzza, K. Hmeljevski & H. Medeiros 7851 (Holotype: VIES [VIES035934]; isotypes RB[ RB00856346 ], SPF). Figures 1–2 .

Bixa atlantica is most similar to Bixa excelsa , but differs in its insertion of the lowest primary vein in relation to midrib length (1/4 vs 1/ 3 in B. excelsa ), number of primary veins ((4–)5 vs. 3(–4) in B. excelsa ), corolla color (white vs. pinkish in B. excelsa ), fruit color when mature (reddish vs. greenish or brownish in B. excelsa ) and spine density in fruits (not obscuring the surface vs. obscuring the surface in B. excelsa ).

Trees or treelets 6−20 m tall, rarely shrubs. Stems with lenticels, indument with scattered peltate trichomes, becoming denser, mostly stalked and ferruginous near the inflorescence, the older stems glabrescent or glabrous, stipule scar evident, transversal, narrow, with two circular nectaries below it. Leaves simple, alternate, subcoriaceous to chartaceous, discolorous with abaxial surface lighter, blade narrow ovate, lanceolate or less commonly ovate, (7.6−)9.9−22.3 × (2.9−) 4.1−12.5 cm, margin entire, base rounded, truncate or rarely slightly cordate, apex acuminate to long acuminate, adaxial surface with scattered peltate trichomes, mostly forming depressed small pits and concentrated near the main veins, rarely densely disposed, abaxial surface with scattered peltate trichomes distributed all over the surface, venation with (4–)5 primary veins at each side of the midrib, the lowest at approximately 1/4 the length of the midrib; petioles 2.1–9.7 cm long, with swollen and dark pulvinulus at base and apex, with scattered peltate trichomes; stipules soon caducous, lanceolate, apex acuminate to long acuminate, 5.9−8.5 × 1−1.8 mm, abaxial surface with peltate trichomes externally, except at base and margins, adaxial surface glabrous. Inflorescence paniculate, terminal, branched, 25–45 flowered, densely covered with ferruginous, stalked, peltate trichomes; bracts soon caducous, 2.2–3.6 mm long, ovate, apex acute, glabrescent with few peltate hairs, mostly near the base, leaving a conspicuous scar; nectaries below bract scar, glabrous, sometimes inconspicuous due to the indumentum. Flowers 3–5 cm diam.; pedicel 5.9–11.5 mm long, densely covered with ferruginous, stalked, peltate trichomes, extrafloral nectaries at the apex of the pedicel absent, rarely inconspicuous; calyx soon caducous, cream-colored to brownish, sepals concave, 6.6–7.8 × 6.9–7.4 mm, wide ovate or orbiculate, apex obtuse, abaxial surface pubescent to glabrescent with peltate hairs, mostly near the base, adaxial surface glabrescent with peltate hairs, mostly near the base; corolla white, petals subequal, membranous, glabrous, 16–23 × 10–15 mm, obovate, apex obtuse; stamens vinaceous with the mid-portion whitish and the base yellowish, numerous, unequal, the ones at the base 3.5–6.5 mm long, the others 8.5–11.5 mm long, filaments glabrous, anther ca. 1 mm long, with two linear pores at the apex; ovary ovoid to hemispherical, densely covered with peltate trichomes, ca. 2.5 × 2–2.5 mm, style erect at anthesis, 7.0– 8.5 mm long, glabrous. Fruit dehiscent, reddish, becoming brownish when older, 1.2–1.7 × 2.0– 2.8 cm, hemispherical or widely ovoid, apex rounded, densely covered with ferruginous, stalked, peltate trichomes, spines densely disposed but not obscuring the fruit surface, 11–13 mm long, erect, subulate, base enlarged, rarely branched; peduncle 1.1–2.0 cm long. Seeds 5–5.3 × 5–5.5 mm, ellipsoid or spheroid, smooth, compressed.

Etymology: —The specific epithet refers to its occurrence in the coastal Brazilian Atlantic Forest. Being the only large tree species of Bixa native to this Domain.

Habitat, distribution and phenology: — Bixa atlantica is endemic to the Atlantic Forest in Bahia, Espírito Santo and Minas Gerais states ( Figure 3 ). The species can be found from 50 to 400 meters above sea level, in semideciduous forest, tabuleiro forest and hygrophilous Southern Bahian forest (without a dry season) physiognomies. It has also been reported as a pioneer, fairly common species that can grow in disturbed secondary forest or along forest borders ( Lopes et al. 2002) and even disturbed ground in savannah-like physiognomies. It can grow between rocks in the bottom of valleys. The species was found flowering during the rainy season, from December to March, especially in February, and in fruit in all months except January, February and June, but especially in April and May ( Figure 4 ).

Preliminary Conservation status:— Bixa atlantica is known from 34 unique occurrences and 20 subpopulations. The EOO is 59,972 km ² and the AOO is 124 km ². The species falls within the territory of the following Protected Areas: Parque Estadual do Rio Doce, Reserva Biológica de Sooretama, Reserva Biológica Córrego do Veado, and Reserva Natural Vale (Linhares). Despite this significant distribution and populations collected in degraded areas, the Atlantic Forest is heavily threatened, with less than 30% of its original vegetation remaining. Consequently, the known subpopulations are mostly fragmented and isolated, which is especially true for the subpopulations from Minas Gerais state, located in an area that has suffered heavy deforestation ( Carvalho & Scolforo 2008) and in which the only wellconserved remnants are in the Parque Estadual do Rio Doce area. With the available information we assess the species as Near Threatened NT B1a+B2a ( IUCN 2012, 2019). However, we need to highlight that the species in Minas Gerais could be regionally assessed in a more endangered classification.

Additional specimens examined (paratypes):— BRAZIL, BAHIA: Guaratinga, Rodovia Itabela / Guaratinga (BA089), com 28 km de extensão, coletas entre os km 20 e 25, margem da rodovia, 31 Mar 1989, L.A. Mattos-Silva et al. 2673 ( CEPEC, MBML, SPF) ; Itanhaém, estrada Itanhaém a Batinga , ca. 16 km, ramal à direita, dando acesso fazenda Pedra Grande , de propriedade de Etevaldo Rezende da Silva , 17° 8’ 17’’ S, 40° 25’ 34’’ W, 29 Dec 2004, A.M. Amorim et al. 4609 ( CEPEC, MO, NY, SPF) ; Porto Seguro, Ramal de São José do Panorama , 18 Jan 1972, R.S. Pinheiro 1727 ( RB, SPF) . Espírito Santo: Água Doce do Norte , 27 Apr 2008, L. Kollmann et al. 10952 ( MBML, SPF) ; Águia Branca , assentamento 16 de Abril., 18° 54’ 25.3’’ S, 40° 44’ 5’’ W, 150–200 m, 15 Mar 2006, V. Demuner et al. 1953 ( MBML, SPF) ; Águia Branca , assentamento 16 de Abril, fragmento à esquerda do campo, 18° 54’ 25.3’’ S, 40° 44’ 5’’ W, 200–400 m, 16 Mar 2006, V. Demuner et al. 2011 ( MBML, SPF) ; Águia Branca, córrego do Trinta (CEIER), proprietário: Alex Sandro , 19° 1’ 22.2’’ S, 40° 38’ 52.8’’ W, 170–500 m, 25 Apr 2006, V. Demuner et al. 2187 ( MBML, SPF) ; Águia Branca, córrego Taquaral, Santa Luzia , propriedade José Rocinha , 18° 59’ 39’’ S, 40° 41’ 46’’ W, 200–350 m, 2 Apr 2007, V. Demuner et al. 3442 ( MBML, SPF) ; Águia Branca, Rochedo, propriedade Arlindo Breda , 18° 56’ 45’’ S, 40° 48’ 10’’ W, 400–550 m, 16 May 2007, V. Demuner et al. 3912 ( MBML, SPF) ; Águia Branca, Rochedo, trilha do córrego, propriedade Ailton Corteleti , 18° 56’ 39’’ S, 40° 47’ 55’’ W, 380–560 m, 6 Sep 2006, L.F.S. Magnago et al. 1317 ( MBML, SPF) ; Águia Branca, Santa Luzia, Propriedade Ciro Ferreira , 18° 58’ 40’’ S, 40° 39’ 56,1’’ W, 170–300 m, 4 Jul 2007, R.R. Vervloet et al. 2789 ( MBML, SPF) ; Colatina, Jequitibá ( Torre 45/2—LT 230 Kv ) Mascarenhas x Verona , 19° 14’ 2.3’’ S, 40° 38’ 16.1’’ W, 240 m, 15 Jul 2008, A.M. Assis & K.F.O. Faria 1703 ( MBML, SPF) ; Colatina, Jequitibá ( Torre 45/2—LT 230 Kv ), 19° 15’ 2.3’’ S, 40° 38’ 16.1’’ W, 240 m, 23 May 2008, A.M. Assis & K.F.O. Faria 1674 ( MBML, SPF) ; Colatina, São João Grande ( Torre 15/2—LT 230 Kv Mascarenhas x Verona ), 19° 26’ 50.1’’ S, 40° 47’ 11’’ W, 300 m, 16 Oct 2008, A.M. Assis & V. Pereira 1823 ( MBML, SPF) ; Colatina, São João Grande ( Torre 18/1—LT 230 Kv Mascarenhas x Verona ), 19° 26’ 25.5’’ S, 40° 46’ 16.9’’ W, 200 m, 15 Oct 2008, A.M. Assis & V. Pereira 1810 ( MBML, SPF) ; Conceição da Barra, Cobraice—Fazenda Jundiá , 18° 25’ 14.3’’ S, 39° 55’ 31.6’’ W, 50 m, 28 Sep 1998, A.M. Assis & L.F.D. Valentin 1804 ( MBML, SPF) ; Governador Lidemberg, Alto Moacir, propriedade Vitório Salomão , 19° 18’ 42’’ S, 40° 32’ 15’’ W, 350–630 m, 21 Fev 2006, L.F.S. Magnago et al. 682 ( MBML, SPF) ; Itaguaçu , localidade de Cachoeirão, 27 Fev 2006, R.C. Britto et al. 26 ( MBML, SPF) ; Itarana, Fragmento localizado na comunidade do Baixo Sossego , 15 Fev 2011, C. Hencker et al. 56 ( MBML, SPF) ; Linhares, Reserva da Companhia Vale do Rio Doce, Borda da trilha da Bicuíba, 55 m, 4 Apr 2006, J.G. Rando et al. 150 ( ESA) ; Linhares, Reserva de Linhares, Docemade , 1 Fev 1972, D. Sucre 8350 ( MO, NY, RB) ; Linhares, Reserva Florestal da Companhia Vale do Rio Doce, córrego João Pedro , aceiro com José Velascio , 26 Apr 1990, L.P. Queiroz 2479 ( CEN, HUEFS) ; Linhares, Reserva Florestal da CVRD, acesso à casa de hóspedes, 22 Aug 1996, A.L.B. Sartori et al. 213 ( CVRD, UEC) ; Linhares, Reserva Florestal de Linhares-Cia. Vale do Rio Doce, estrada do Flamengo , ca. 500 m da sede, 19° 9’ 6’’ S, 40° 4’ 8’’ W, 64 m, 11 May 2000, J.R. Pirani et al. 4674 ( RB, SPF) ; Linhares, Reserva Natural da Vale, trecho de mussununga próximo ao nativo do contorno do Roxinho , 17 Apr 2011, D.F. Lima et al. 210 ( BHCB, CTES, CVRD, ESA, HUEFS, RB) ; Marilândia, Alto Liberdade, propriedade Deuclecio Lorenzini , 19° 21’ 13’’ S, 40° 31’ 1’’ W, 300–400 m, 19 Apr 2006, L.F.S. Magnago et al. 899 ( MBML, SPF) ; Pinheiros, Reserva Biológica Córrego do Veado , trilha de educação ambiental, 18° 22’ 15’’ S, 40° 8’ 32’’ W, 113 m, 1 Fev 2007, L.M. Versieux et al. 399 ( SP, SPF) ; Pinheiros, Santa Rita , 18° 18’ 37’’ S, 40° 8’ 49’’ W, 107 m, 31 Jan 2008, L. Kollmann & L. Magnago 10521 ( MBML, SPF) ; Rio Bananal, Alto município de Rio Bananal , 19° 14’ 56’’ S, 40° 24’ 59’’ W, 300–450 m, 1 Aug 2007, R.R. Vervloet et al. 3106 ( MBML, SPF) ; Rio Bananal, Arredores de São Jorge de Tiradentes , 19° 5’ 48.2’’ S, 40° 19’ 4.9’’ W, m, 7 Oct 2017, E.D. Lozano et al. 3882 ( MBM, SPF) ; São Domingos do Norte, São Gonçalo ( Torre 48/2—LT 230 kv Mascarenhas x Verona ), 19° 12’ 17.8’’ S, 40° 38’ 12.3’’ W, 244 m, 3 May 2008, A.M. Assis & K.F.O. Faria 1656 ( MBML, SPF) ; São Domingos do Norte, Trevo para Águia Branca ( Torre 58/2—LT230 Kv Mascarenhas x Verona ), 19° 7’ 37’’ S, 40° 36’ 41’’ W, 150 m, 2 May 2008, A.M. Assis & K.F.O. Faria 1611 ( MBML, SPF) ; São Gabriel da Palha, Fazenda Rondeli , próximo ao clube campestre, 19° 1’ 8’’ S, 40° 33’ 19.5’’ W, 200 m, 26 Apr 2008, A.M. Assis & V.G. Demuner 1565 ( MBML, SPF) ; Soretama, Reserva Biológica de Sooretama , 74 m, 9 Oct 2012, M.B. Costa 18 ( VIES) . Minas Gerais: Marliéria, Parque Estadual do Rio Doce , 19° 45’ 30’’ S, 42° 37’ 33’’ W, 295 m, 21 Fev 1996, L.V. Costa s.n. ( BHCB, SPF) ; Marliéria, Parque Estadual do Rio Doce , estrada para o restaurante, 19° 46’ 49’’ S, 42° 37’ 10’’ W, 311 m, 4 Sep 2000, M.M. Silva-Castro et al. 1484 ( HUEFS) ; Timoteo, Parque Estadual do Rio Doce , estrada para o restaurante, 4 Nov 1999, E.J. Leite et al. 5 ( CEN) .

Comments:— Bixa atlantica can be distinguished from B. orellana , the best represented species of the genus in herbaria, and the only other one that also occurs in the Atlantic Forest domain, due to the absence of nectaries in the pedicel apex (rarely inconspicuous) near the calyx (vs. conspicuous in B. orellana ), the leaf base rounded truncate or rarely slightly cordate (vs. cordate or truncate in B. orellana ), the habit of trees up to 20 m, rarely treelets or shrubs (vs. shrubs or treelets 5–6 m tall in B. orellana ) and fruit shape wider than long (vs. longer than wide in B. orellana ). The absence of nectaries in the pedicel apex can also be used to promptly differ the new species from another two species, Bixa urucurana (usually treated as a synonym of B. orellana ) and Bixa platycarpa Ruiz & Pavon (1959: 383) , both of which have nectaries.

Although Bixa atlantica specimens have been frequently referred to as B. arborea , the species can be easily distinguished as the former presents spiny fruits (vs. spineless fruits). The most closely related species is B. excelsa ( Figure 5 ), differing by the leaf venation, petal and fruit color (in vivo and in sico) and morphology. Although Baer (1976) states that the fruits of B. excelsa are reddish-green, we have never been able to confirm this color from all specimens’ label descriptions and photos examined. Further differences between B. atlantica and these two species are presented in Table 1 .

Figures

FIGURE 1. Bixa atlantica Antar & Sano.A. Branch in flower. B. Node with stipule scar and circular nectaries below it, also an immature branch with a stipule. C. Leaf, abaxial surface. D. Flower at anthesis. E. Flower at anthesis without petals. F. Stamen. G. Branch with fruits. H. Fruit. I. Detail of fruit surface and spines. A–F Illustration by Klei Sousa based on R.C. Forzza et al. 7851. G–I. Illustration by Klei Sousa based on Assis & Demuner 1565.

FIGURE 2. Bixa atlantica Antar & Sano. A. Branch in flower. B. Branch in fruit. C. Flowers. D. Branch with older fruits. A–C. Photos by Geovane S. Siqueira. D. Photo by Eduardo D. Lozano.

FIGURE 3. Distribution maps showing: A. Bixa atlantica Antar & Sano and Bixa excelsa Gleason & Krukoff. The orange shape shows the extension of the Amazonian domain and the green shape shows the extension of the Atlantic Forest domain; B. Bixa atlantica Antar & Sano (BA, Bahia; ES, Espírito Santo; MG, Minas Gerais).

FIGURE 4. Phenology in Bixa atlantica Antar & Sano and Bixa excelsa Gleason & Krukoff. White slices denote flowering specimens and gray slices, fruiting specimens; The size represents the relative number of specimens from the total which was blooming or fruiting in that month.

FIGURE 5. Bixa excelsa Gleason & Krukoff.A. Vegetative branch; B. Trunk bark; C. Inflorescence. D. Branch with flowers and older fruits. E. Fruits. F. Older fruits and seeds.A–D. Photos by Marcelo F. Simon. E–F. Photos by Narcísio C. Bigio.