Four new species of Capsicum (Solanaceae) from the tropical Andes and an update on the phylogeny of the genus Author Barboza, Gloria E. Author García, Carolina Carrizo Instituto Multidisciplinario de Biología Vegetal (IMBIV), CONICET, Córdoba, Argentina, & Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria, Author González, Segundo Leiva Author Scaldaferro, Marisel Instituto Multidisciplinario de Biología Vegetal (IMBIV), CONICET, Córdoba, Argentina, & Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina, Author Reyes, Ximena Centro de Investigaciones Fitoecogenéticas de Pairumani, Cochabamba, Bolivia text PLoS ONE 2019 e 0209792 2019-01-16 14 1 1 26 http://dx.doi.org/10.1371/journal.pone.0209792 journal article 10.1371/journal.pone.0209792 1932-6203 PMC6334993 30650102 12630921 Capsicum neei Barboza & X. Reyes , sp. nov. [ urn:lsid:ipni.org:names: 77192560–1]. Type : Bolivia . Chuquisaca : Prov. Hernando Siles, a 4.1 km del puente nuevo de Monteagudo viniendo desde Monteagudo , sobre mano derecha, - 19.804617 S , - 64, 019923 W , 16 Dec 2017 (fl), G . E . Barboza 4927 ( holotype , LPB; isotypes , CORD [CORD-00006935, CORD-00006956], NY) . Figs 10 and 11 Diagnosis . Like Capsicum minutiflorum Rusby (Hunz.) but differing in the non-geniculate pendent flowering pedicels and the strongly nerved calyx with 10 unequal appendages. Description . Small shrubs 0.70–2 (3) m tall, thin, erect, laxly branched above. Young stems green, slim, fragile, glabrescent, and slightly striate, without lenticels; bark of older stems light brown, glabrous, with a few oblong lenticels. Sympodial units difoliate, geminate, leaf pair not markedly anisophyllous in size and shape. Leaves simple, membranaceous, glabrescent on both surfaces and margins with 4-7-celled non glandular trichomes 0.2–0.5 mm long; the larger leaves with blades (5.5) 6.7–11 cm long, 2.1–4 (4.5) cm wide, elliptic or ovate, major veins 3–4 on each side of midvein, base attenuate, margin entire, apex acute; petioles 0.3–0.8 (1.5) cm long; the minor leaves 2.7–4.6 (6) cm long, 1.2–1.8 (2.3) cm wide, elliptic or ovate, major veins 2–3 on each side of midvein, base attenuate, margin entire, apex obtuse or acute; petioles 0.2–0.5 (0.8) cm long, with similar pubescence as in larger leaves. Flowers 2–4 per axil, rarely solitary; flowering pedicels green, filiform, striate, pendent, slightly curved, not geniculate at anthesis, (0.65) 0.8–1.5 cm long, with sparse 5-6-celled non-glandular trichomes and tiny dark glandular trichomes (stalk unicellular, head multicellular). Flower buds ovoid, greenish pale yellow. Calyx 1.7–2.5 mm long, 2–3 mm wide, cup-shaped, green, with 10 nerves clearly evident, the margin truncate, pubescent, with non-glandular trichomes 0.3–0.6 mm long outside and dense glandular pubescence inside (head multicellular, stalk unicellular), 10 unequal linear appendages, green, the five longer appendages (0.7) 0.9–1.75 (2) mm long, emerging almost from the margin, the five shorter 0.2–0.8 (1.2) mm long, emerging 0.8–1 mm below the margin, with the same non glandular trichomes of the calyx tube. Corolla (6) 8–10 mm long, 5–6 mm diam, stellate, delicate, entirely yellow or with small brownish green spots in the base of the lobes and tube inside, with a thin interpetalar tissue; tube 3–4.5 mm long, with tiny glandular trichomes (head and stalk one celled each) inside and glabrescent outside; lobes 3.5–5.5 mm long, ca. 2 mm wide, ovate, erect, glabrous adaxially and with sparse non-glandular trichomes abaxially, the tips papillose and cucullate. Stamens 5, subequal, filaments 1.4–1.75 mm long, cream, glabrous, inserted on the corolla ca. 1.2 mm from the base, with inconspicuous auricles at point of insertion; anthers (1.5) 1.8–2 mm long, not connivent, elliptic, light yellow. Ovary ca. 1.2 mm long, 1.3 mm diam, ovoid or subglobose, light green, glabrous; nectary ca. 0.3 mm tall, style 3.75 mm long, cream, widening distally, glabrous; stigma ca. 0.2 mm long, 0.3 mm wide, light green, somewhat bilobed. Berry 0.4–0.75 cm diam, globose, green when immature, red at maturity, glabrous; fruiting pedicels (1.3) 1.8–2.3 cm long, pendent, striate and widened distally; the fruiting calyx persistent, non-accrescent, ca. 4 mm diam, discoid, the appendages spreading 1–2 mm long, subulate. Seeds unknown. Fig 10. Capsicum neei Barboza & X. Reyes. (A) Flowering branch. (B) Inflorescence. (C) Flower bud. (D) Flower. (E) Calyx. (F) Opened corolla.(G) Gynoecium (H) Fruit. (I) Glandular trichome of the inside calyx. (J) Glandular trichome of the pedicels.(K) Glandular trichome of the inside corolla. (L) Non-glandular trichome of the outside calyx. (M) Non-glandular trichome of the outside corolla lobes. Drawn by S. Montecchiesi. https://doi.org/10.1371/journal.pone.0209792.g010 Distribution and ecology. Endemic to southeastern Bolivia ( Fig 12 ), mainly in the Serranías Iñao, Yahuañanca and Khaskha Orkho (Dpt. Chuquisaca ). A few collections have been recorded from the Yungas (Dpt. Santa Cruz ). Capsicum neei is most commonly collected in the Boliviano-Tucumano Forest in both Departments [ 35 ] from understories at the foot of cloud forest hillsides and deciduous forests, between 1100–1750 m elevation. It grows associated with members of Juglandaceae , Lauraceae , Myrtaceae, Leguminosae , ferns and bryophytes. Fig 11. Capsicum neei Barboza & X. Reyes. (A) Plant. (B) Flower bud. (C) Flowering branch. Photos by G. E. Barboza. https://doi.org/10.1371/journal.pone.0209792.g011 Fig 12. Distribution of Capsicum neei Barboza & X. Reyes. https://doi.org/10.1371/journal.pone.0209792.g012 Phenology . Flowering and fruiting from October to May. Etymology. The epithet is in honor to Dr. Mike Nee ( NY ), a solanaceous specialist who carried out extensive explorations in the Bolivian territory and separated specimens of this species as a rare or probable new species in various herbaria. Species Conservation Assessment. According to IUCN criteria [ 15 ], C . neei is proposed as Near Threatened species. The species meets the area requirements under criterion B for threatened (EOO: 16912 km 2, B1 < 20000 km 2, Vulnerable; AOO: 44 km 2, B2 < 500 km 2, Endangered) and is declining, but the population is not severely fragmented and occurs in more than 10 locations. Capsicum neei has been collected many times in the last 23 years in a recently Protected Area: National Park and Integrated Management Natural Area “Serranía Iñao” [ 36 ], and in nearby areas which suggests that both the decline in its geographic range (EOO and AOO) and the population size will not be significantly affected in the forthcoming years. Affinities . Capsicum neei is nested within the Bolivian clade, strongly resolved as sister to C . caballeroi ( Fig 6 ). Additional specimens examined. BOLIVIA . Chuquisaca : Hernando Siles , ca. 7 km de Monteagudo , inicio del cañón Heredia , 19˚47’17’’S, 64˚02’08’’W, 1127 m, 13 Dec 2006 (fl, fr), H . Huaylla et al . 2178 ( HSB , MO); Parque Nacional y área natural de manejo integrado de la Serranía del Iñao , cuenca del río Limón , 19˚44’01"S, 63˚54’52"W, 1247 m, 15 Dec 2006 (fr), E . Portal et al . 108 ( HSB , MO); foot of Cerro Urkhal path before 2nd river crossing, 19˚48’S 63˚ 57’W, 1300 m, 4 Oct 2000 (fl), K . Wendelberger 170 ( HSB , MO); Luis Calvo, Ticucha, serranía del Iñao, 12 km al NO de la comunidad de Ticucha , 19˚35’0.4”S, 63˚53’12.7”W, 1431 m, 11 Apr 2003 (fl), A . Carretero et al . 824 ( HSB , MO, NY); Entierrillos, aprox. a 5 km de la escuela de Entierrillos , serranía del Iñao, 19˚31’S, 63˚52’W, 1700 m, 18 Dec 2003 (fl), A . Carretero et al . 939 ( HSB , MO); Serranía del Iñao, pasando la Laguna, 19˚31’S, 63˚52’W, 18 Dec 2003 (fl), A . Carretero et al . 998 ( HSB , MO, NY); Las Frías, ca. a la la cima de la serranía de Ñahuañanca, 19˚09’30.6"S, 63˚50’40.6"W, 1930 m , 22 Dec 2003 (fl, fr), A . Carretero et al . 1067 ( HSB , MO, NY); Las Frías, ca. 1/ 2 km de la vivienda de Sr. Severino Daza, hacia la cima de la serranía de Yahuañanca, 19˚09’31"S, 63˚50’23"W, 1600 m , 23 Dec 2004 (fl), A . Carretero et al . 1085 ( HSB , MO, NY); Sud Cinti, ca. 3 horas en caballo al NW de la comunidad de Orocote entre los ríos Limonal y Cochayo, 20˚47’S, 64˚21’W, 1650 m , 29 Apr 2005 (fr), R . Lozano 1207 ( HSB , MO); Tomina, aprox. 800 m . antes de llegar a Llantoj, de La Florida subiendo hacia el E de la Serranía de Kaska Orcko, 19˚09’46"S, 64˚03’42"W, 1750 m , 11 Oct 2004 (fl, fr), J . Gutiérrez R . 1004 ( HSB , MO); Llantoj, aprox. 800 m antes de llegar a Llantoj, de la Florida subiendo hacia el E de la Serranía de Kaska Orcko, 19˚09’46"S, 64˚03’42"W, 1750 m , 15 Dec 2004 (fr), J . Gutiérrez R . 1072 ( HSB , MO); Rio Limón Valley between Padilla and Monteagudo, 1500 m , 1 Jan 1995 (fl), J . R . I . Wood 9104 ( NY ). Santa Cruz . Prov. Florida, Mairana, La Yunga de Mairana , 18˚04’13”S, 63˚55’08”W, 2190 m , 15 Nov 2004 (fl), M . Serrano et al . 5482 ( NY ). Capsicum neei is morphologically most similar to the Bolivian C . minutiflorum in having stellate yellow corolla and red fruit at maturity. It can be distinguished by the non-geniculate pendent flowering pedicels and the strongly nerved calyx with 10 unequal appendages ( Figs 10C, 10E and 11B ) versus the geniculate and erect flowering pedicels and the calyx weakly nerved and with 5 equal short appendages in C . minutiflorum (Rusby) Hunz. The flowers in C . neei often appear to be solitary but the remains of 2–3 early deciduous bud or flower scars can be seen in the axils. Fruit features as pungency, presence of giant cells and sclerotic granules in the pericarp and mature seeds are unknown at present but it is probable that the fruits are pungent and have giant cells in the innermost layer of the pericarp as occur in the remaining species of the Bolivian clade where C . neei is positioned. This new species is sympatric with C . baccatum L. var. baccatum , a taxon with a much wider distribution in South America, that has geniculate pedicels, calyx with 5 equal appendages, white corollas with greenish yellow spots inside and ovoid or globose red fruits. Capsicum neei has been resolved as a new member of the Bolivian clade, which is coherent with its geographic range and the main common feature recognized for the clade, the yellow corollas [ 1 ]. However, the Bolivian clade has a weak support, most likely due to the apparent divergence of C . coccineum from the rest of the species; indeed, C . coccineum would deserve more attention considering some morphological variability observed in the species (GEB, pers. obs.).