Print
An amazing new Capsicum (Solanaceae) species from the Andean-Amazonian Piedmont
expand article infoGloria E. Barboza, Carolina Carrizo García§, Marisel Scaldaferro, Lynn Bohs|
‡ Universidad Nacional de Córdoba, Córdoba, Argentina
§ University of Vienna, Vienna, Austria
| University of Utah, Salt Lake City, United States of America
Open Access

Abstract

Capsicum regale Barboza & Bohs, sp. nov., a new species from the tropical wet forests of the eastern Andean slopes (Colombia, Ecuador, and Peru) is described and illustrated. This new species belongs to the Andean clade (all species 2n = 26) of Capsicum and is similar to C. longifolium Barboza & S.Leiva in its glabrescence, calyx morphology, and corolla and seed color but differs in its membranous and elliptic leaves, fleshy calyces, deeper stellate corollas, longer filaments, longer and purple fruiting pedicels, purple berries, and larger seeds. Its chromosome number was counted (2n = 26), a preliminary assessment of conservation status is given and discussed, and an updated identification key to the species of the Andean clade is provided.

Keywords

Andean clade, Capsicum, chromosomes, phylogeny, South America, taxonomy

Introduction

Capsicum L. (Capsiceae, Solanaceae), the chili pepper genus, consists of approximately 42 species distributed in temperate and tropical Central and South America, Mexico and the West Indies (Barboza et al. 2020). It includes five species cultivated worldwide as vegetables, spices, and medicines (C. annuum L., C. frutescens L., C. chinense Jacq., C. baccatum L. and C. pubescens Ruiz & Pav.). Capsicum peppers are major crops worldwide, and along with potato, tomato, and eggplant in the genus Solanum L., are amongst the most economically important members of the Solanaceae (Samuels 2015).

The Andes are one of the main centers of diversity for Capsicum, where new species continue to be discovered (Nee et al. 2006; Barboza et al. 2019). Approximately 50% of the species (ca. 20 species) occur in tropical Andean forests or in dry inter-Andean valleys (Barboza et al. in prep.). The tropical montane forest ecoregion is located on the slopes of the Andes extending north to south from southern Colombia, through Ecuador, and into northern Peru (WWF 2020). This region is characterized by a lush vegetation with evergreen seasonal broad-leaved forests and a rich fauna (Stewart et al. 2020; WWF 2020). It is one of the most biologically diverse ecosystems in the world (Gentry 1992; Bruijnzeel et al. 2010; Tapia-Armijos et al. 2015) with a high level of species endemism (Myers et al. 2000). Khoury et al. (2020) have demonstrated that the highlands of Colombia, Ecuador, Peru, and Venezuela represent one of the hotspots for Capsicum that need further investigation in terms of collecting taxa for ex situ conservation of the wild species.

During recent field explorations in the Colombian Cordillera Oriental (Dept. Caquetá), an atypical species of Solanaceae was collected. Despite the presence of several Solanaceae experts in the group, no one was sure what genus it belonged to. Its deeply stellate yellowish corollas, long-exserted stamens, and purple fruits and fruiting pedicels were striking and called to mind some characters of the poorly known genus Cuatresia Hunz., whereas its thick, triangular-compressed, and reflexed calyx appendages resembled those of some Lycianthes (Dunal) Hassler taxa, whose species are not well understood in Colombia. Puzzled, we provisionally named it “Cuatresianthes” and placed some bets on its eventual generic identity. DNA was extracted and sequenced in the Bohs lab from leaf material collected on these field trips. BLAST results indicated that the species belonged not to Cuatresia or Lycianthes, but to Capsicum. A preliminary molecular study placed the collection unequivocally in the Andean clade of Capsicum, but it did not belong to any known species. Through an exhaustive search amongst unidentified Cuatresia collections in herbaria, we found other specimens from Ecuador and Peru that matched our Colombian gatherings. Here, we describe this species as new to science and provide information on its morphology, distribution, karyology and phylogenetic position in the genus Capsicum.

Materials and methods

Two field trips were made in Colombia (Dept. Caquetá) during 2016 and 2019. Fresh material was preserved in 70% alcohol to perform measurements of reproductive organs using a Zeiss Stemi 2000-C stereomicroscope at 6.5–50× magnification. Descriptions were based on living plants observed during field work and examination of digital images of herbarium specimens housed at the following seven herbaria: BM, COAH, COL, F, MO, QCNE, US. Seeds were also examined using scanning electron microscopy (SEM); they were prepared using enzyme etching (Lester and Durrands 1984) to dissolve outer cell walls, affixed to aluminum stubs with double-sided adhesive tape, coated with gold, and examined using a FE-SEM Sigma (LAMARX, National University of Córdoba, Argentina) microscope.

Information about flower, fruit, and seed color was taken mainly from our own observations in the field and photographs sent by some collectors; we tested pungency in the field on immature and mature fruits.

The distribution map was produced using QGIS 3.8 (QGIS Development Team 2019) and was based on georeferenced data of all the collections analyzed. Conservation status was assessed using IUCN criteria B, geographic range in the form of B1 (EOO: extent of occurrence) and B2 (AOO; area of occupancy) (IUCN 2019). The extent of occurrence and area of occupancy were calculated using the Geospatial Conservation Assessment Tool GeoCAT (Bachman et al. 2011; GeoCAT 2020).

Somatic metaphases were examined in root tip squashes obtained from germinated seeds. The root apices were fixed in 3:1 ethanol: acetic acid mixture for 12 hr after a pretreatment in 2 mM 8-hydroxyquinoline solution for two hr at room temperature and two hr at 4 °C. The material was kept at –20 °C until examination. The root tips were macerated in pectinase-cellulase solution (Moscone et al. 1993), and chromosomes were stained with 4’–6-diamidino-2-phenylindole (DAPI) (Schweizer and Ambros 1994). Metaphase chromosomes were observed and photographed with epifluorescence using an Olympus BX61 microscope equipped with the appropriate filter sets (Olympus, Shinjuku-ku, Tokyo, Japan) and a JAI CV-M4 + CL monochromatic digital camera (JAI, Barrington, N.J., USA). Three individual seeds from the collection Orejuela et al. 3034 were germinated and grown until root tips were produced, and 10 cells from each seedling were studied in metaphases.

Phylogenetic affinities were explored using DNA sequences from four markers, namely: the intergenic spacers psbA-trnH, ndhF-rpl32 and trnL-trnF from the plastid genome, and the single-copy nuclear gene waxy (GBSSI, granule-bound starch synthase, exons 2 to 10). Representatives of different clades recognized within Capsicum and several outgroup species were included. Genomic DNA of C. regale was extracted from silica-gel dried leaves using the Qiagen DNeasy Plant mini kit (Qiagen Inc., Valencia, California, EUA) and a modified CTAB protocol. Most sequences included in this study were used in previously published analyses and therefore were retrieved from GenBank, except for a few sequences from outgroup species (see Suppl. material 1: Table S1), for which DNA extracts were already available. Amplification and sequencing protocols for the markers used were as in Carrizo García et al. (2016, 2020) and Barboza et al. (2019). PCR amplicons were sequenced on an automated capillary sequencer [University of Vienna (Vienna, Austria), and the University of Utah HSC Core Research Facility (Salt Lake City, Utah, USA)]. A single concatenated dataset was assembled in MEGA 7 (Kumar et al. 2016). Phylogenetic reconstructions were done using maximum parsimony [MP, in PAUP* 4.0b10 (Swofford 2003)], maximum likelihood [ML, in RAxML v8.2.10 (Stamatakis 2014)] and Bayesian inference [BI, in MrBayes 3.2.2 (Ronquist et al. 2012)] approaches as in Carrizo García et al. (2016, 2020). The GTR+R nucleotide substitution model was selected a priori following the Akaike Information Criteria in jModelTest 2.1.3 (Darriba et al. 2012) for ML and BI analyses.

Taxonomic treatment

Capsicum regale Barboza & Bohs, sp. nov.

Figs 1, 2, 3

Diagnosis

Capsicum regale is morphologically most similar to C. longifolium Barboza & S.Leiva, but the former differs in having membranous and elliptic leaves, fleshy calyces, more deeply stellate corollas, longer filaments, longer and purple fruiting pedicels, dark blue to purple berries, larger seeds, smooth seed coats, and spine-like projections along the seed margins.

Figure 1. 

Capsicum regale Barboza & Bohs. A fruiting apical branch B unbranched inflorescence C flower, in lateral view D opened corolla E gynoecium F fruit. From Orejuela et al. 3034. Drawn by S. Montecchiesi.

Type

Colombia. Caquetá: Mun. Florencia, Corregimiento El Caraño, Finca de Don Isauro, camino al río, en interior de bosque fuertemente inclinado, 01°44'10.6"N, 75°40'78.3"W, 1004 m, 22 Aug 2019 (fl, fr), A. Orejuela, L. Bohs, G.E. Barboza, P. González, R. Deanna, J. Urdampilleta, J. Valencia & G. Sierra 3034 (holotype: COL; isotypes: COAH, CORD, HUAZ [to be distributed]).

Figure 2. 

Capsicum regale Barboza & Bohs. A habitat B apical branch, showing anisophyllous leaf pairs C abaxial surface of leaf with purple main vein D forked inflorescence; note the scars of the deciduous flowers E flower, in lateral view, on a unbranched elongate inflorescence F, G Flowers with and without pigmentation respectively H–K various stages of fruit maturity, in K mature fruit showing the constriction between the pedicel and the berry (arrow) A–F, H–K from Orejuela et al. 3034 (photos by A. Orejuela, P. Gonzáles, and G. Barboza) G from Hoyos 127 (photo by L. Coca).

Description

Slender shrubs (1–) 1.8–2.5 (–3) m tall, with the main stem somewhat thick, ca. 0.8 cm in diameter at base, sparsely branched toward apex, the branches dichotomous, weak, spreading horizontally. Stems solid and terete at base, the young stems pale green, glossy, striate, glabrous, the nodes green; bark of older stems dark brown, glabrous; lenticels present. Sympodial units difoliate, geminate, the leaf pairs markedly differing in size. Leaves simple, membranous, slightly discolorous, green adaxially, pale green with the midvein prominent and purple and the secondary veins lilac or green abaxially; adaxial and abaxial surfaces glabrous; major leaves with blades 17–20 (–24) cm long, 4.7–8 (–9.2) cm wide, elliptic, the major veins 6–8 on each side of midvein, the base unequal and attenuate, the margins entire and glabrous, the apex apiculate to long-apiculate; petioles (0.8–) 1.5–2.3 cm long, green adaxially and purple abaxially, glabrous; the minor leaves 2–5 cm long, 1–3 cm wide, ovate, the major veins 3–5 on each side of midvein, the base unequal, the margins entire, glabrous, the apex obtuse; petioles 0–0.4 cm long, green, glabrous. Inflorescence ca. 10 mm long, unbranched or rarely shortly forked, with 5–13 flowers, the axes glabrous; peduncle 0–5.5 mm; rachis 4.5–6 mm long; pedicels 1.2–1.4 cm long, thin, 2–3–edged, erect to spreading, straight, purple to green, glabrous, nearly contiguous, articulated at the base, leaving conspicuous scars. Buds ellipsoid, green. Flowers 5-merous, all perfect. Calyx 2–3 mm long, ca. 2 mm wide, cup-shaped, fleshy, green or greenish purple, the margin truncate, circular in outline, glabrous, the appendages (0–) 4–5, 1–1.8 mm long, 0.8–1.1 mm wide, purple, thick, triangular-compressed, reflexed, inserted very close to the margin. Corolla 7–8 mm long, ca. 10 mm in diameter, deeply stellate, thick, with narrow interpetalar tissue, pure yellow or yellow with maroon pigmentation abaxially and greenish yellow with lobes marginally maroon adaxially, glabrous, the tube 2–2.5 mm long, the lobes 5–5.5 mm long, ca. 2 mm wide, triangular, the tips papillose, the margins with short eglandular trichomes. Stamens subequal, one filament longer than the others; long filament 3.5–4.3 mm long, shorter filaments (2) 3–3.2 mm long, white, glabrous, inserted on the corolla ca. 1 mm from the base, with inconspicuous auricles; anthers ca. 2 mm long, elliptic, not connivent, the thecae lilac or pale bluish, opening into longitudinal slits. Ovary ca. 1.3 mm long, ca. 1 mm in diameter, light green, ovoid, glabrous; nectary ca. 0.4 mm high, paler than the ovary, conspicuous; style 4.3–4.5 mm long, white, clavate, glabrous; stigma ca. 0.1 mm long, ca. 0.8 mm wide, light green, globose or somewhat discoid. Fruit a berry, globose, 6–9 mm in diameter, green when immature, turning nearly white and translucent during transition to maturity, then becoming dark blue to purple when mature, glabrous, non-pungent, the pericarp opaque, without giant cells, the endocarp smooth; stone cells absent; fruiting pedicels ca. 1.8 cm long, 1.8–2 mm in diameter proximally, 2.5–2.6 mm in diameter distally, brilliant dark purple, erect, fleshy, slightly angled and strongly thickened distally; fruiting calyx 3.75–4.25 mm in diameter, persistent, not accrescent, discoid, brilliant purple, with a conspicuous annular constriction at the junction with the swollen pedicel, the appendages reflexed, brilliant purple, fleshy and laterally compressed. Seeds 7–17 per fruit, 2.7–3.4 mm long, 2.2–2.7 mm wide, flattened, C-shaped, black, the seed coat smooth except for small spine-like projections on the seed margin, the cells irregular in shape to polygonal at seed margins, the lateral walls sinuate to straight.

Figure 3. 

Seed of C. regale Barboza & Bohs viewed under SEM. A Seed B Seed coat sculpture. From Orejuela et al. 3034.

Distribution

Capsicum regale occurs in southern Colombia, eastern Ecuador, and northern Peru, known mainly on the eastern slopes of the Andes (the Andean-Amazonian Piedmont), between 700–1900 m elevation (Fig. 4).

Figure 4. 

Distribution of Capsicum regale Barboza & Bohs.

Ecology

The small populations inhabit the understory of the premontane or montane humid tropical forests of the Amazonian slopes of the Andes.

Phenology

The species has been collected in flower and fruit in April and from August to December.

Etymology

The specific epithet comes from the Latin regalis, royal or regal, referring to the regal, princely, or magnificent appearance of this special plant and also making reference to the royal purple color that suffuses the leaves, fruits, and fruiting pedicels.

Preliminary assessment of conservation status

Assessment using the IUCN Red List Criteria (IUCN 2019) suggests a status of Endangered (EN) B2ab(iii) for C. regale. Although this species has an extent of occurrence (EOO) of 47,806.378 km2, its area of occupancy (AOO) is calculated to be 32 km2 (criterion B2 < 500 km2), and the habitat quality has experienced a continuing decline, especially associated with fragmentation and deforestation.

Chromosome number

The somatic chromosome number found in C. regale is 2n = 2x = 26 (Fig. 5), as for all of the species of the Andean clade (Scaldaferro and Moscone 2019; Barboza et al. 2019).

Figure 5. 

Mitotic metaphase chromosomes of Capsicum regale Barboza & Bohs, 2n = 26. Scale bar: 10 µm

Phylogenetic affinities

Capsicum regale is strongly resolved within the Andean clade of Capsicum in all analyses. Within the Andean clade, C. regale is moderately supported in a clade with C. rhomboideum and C. hookerianum. Within this clade, it is weakly supported as sister to C. rhomboideum (Fig. 6).

Figure 6. 

Bayesian majority-rule consensus tree of Capsicum showing the placement of C. regale Barboza & Bohs. The Andean clade is highlighted in colored branches. Support values are indicated by each branch (bootstrap support maximum parsimony/bootstrap support maximum likelihood/posterior probabilities; dashes indicate support values < 50%). Key support values that indicate the position of C. regale are shown in bold. Asterisks indicate different resolutions using maximum parsimony.

Specimens examined

Colombia. Caquetá: Mun. Florencia, Corregimiento El Caraño, Km 20, finca Las Brisas, propiedad de Isauro Trujillo, 01°44'11.80"N, 75°40'37.8"W, 1002 m, 7 Oct 2017 (fl, fr), D. Hoyos, E. Trujillo & J. Sánchez 118 (COAH, COL); same locality, 9 Dec 2017 (fl, fr), D. Hoyos, M. Cuellar & F. Vallejo 146 (COL); Finca de don Isauro, camino al río, en interior de bosque fuertemente inclinado, 01°44'01.4"N, 75°40'35.4"W, 1000 m, 16 Apr 2016 (fl, fr), A. Orejuela, L. Bohs, G.E. Barboza, E. Trujillo, J. D. Tovar & J. Castillo 2640 (COL); same locality, 01°44'09.1"N, 75°40'40.3"W, 932 m, 22 Aug 2019 (fl, fr), A. Orejuela, L. Bohs, G.E. Barboza, P. González, R. Deanna, J. Urdampilleta, J. Valencia & G. Sierra 3035 (COL); finca Las Brisas, debajo de la casa, vereda La Cascada, 01°37'5"N, 75°40'50"W, 1000 m, 7 Nov 2015 (fl, fr), D. Sanín 6236 (COL); Mun. San José del Fragua, vereda La Peneya-camino hacia El Jardín, zona amortiguadora PNN Alto Fragua Indi Wasi, 01°17'31"N, 76°08'0.64"W, 700–850 m, 23 Oct 2017 (fl, fr), D. Hoyos et al. 127 (COAH, COL).

ECUADOR. Morona-Santiago: along new road Mendez-Morona, km 30–35, 800 m, 18 Aug 1989 (fl, fr), H. van der Werff & E. Gudiño 11196 (BM, MO, QCNE). Napo: Archidona Cantón, Reserva Ecológica Antisana, Comunidad Shamato, entrada por km 21-Shamato, 00°44’S, 77°48’W, 1700 m, 27 Apr 1998 (fl), J. L. Clark et al. 5337 (BM, MO); Parroquia Ahuano, Estación Biológica Jatun Sacha, 8 km E of Misahuallí, Finca Acaro, 01°17'17"S, 77°52'54"W, 910 m, 17 Aug 2005 (fl, fr), J. L. Clark et al. 9403 (BM, US). Sucumbíos: Río Bermejo to Cerro Sur Pax, Cofan community of Alto Bermejo, NW between Lumbaqui and Cascales, vicinity of Oso Ridge Camp, 00°19'17.7"N, 77°25'10"W, 1700–1920 m, 2 Aug 2001 (fr), R. Aguinda et al. 1537 (F).

PERU. Loreto: Datem del Marañón, Morona District, Pongo Chinim, valley between the eastern and western ridges of the Kampankis range, ca.14 km south of the Peru-Ecuador border, 3 Aug 2011 (fl, fr), I. Huamantupa 15251 (V0387079F color photo, F).

Discussion

Capsicum regale belongs to the Andean clade of Capsicum (Carrizo García et al. 2016; see below). It is a very striking species due to its unbranched (Figs 1B, 2E, J) or forked inflorescence (Fig. 2D) with 5–13 deciduous flowers on an elongate rachis (Fig. 2D), fleshy and laterally compressed calyx appendages (Fig. 2D, E), deeply stellate corollas (Fig. 2F, G), strongly thickened and brilliant purple fruiting pedicels (Fig. 2H–K), dark blue to purple fruits (Fig. 2J, K), and flattened black seeds with spine-like projections at the margins (Fig. 3). This species is morphologically most similar to C. longifolium (Barboza et al. 2019) with which it shares lack of pubescence, multi-flowered inflorescences, yellow corollas, laterally compressed calyx appendages, and black seeds (see contrasting characters in the key below).

Capsicum regale possesses unusual characters of the genus. Normally, Capsicum species have unbranched inflorescences lacking peduncles, with the flowers solitary or congested on a very short axis. Flowers can be arranged on a short or relatively elongated rachis in a few species, e.g., C. rhomboideum (Dunal) Kuntze, C. coccineum (Rusby) Hunz., C. lycianthoides Bitter (Barboza pers. obs.), C. longifolium (Barboza et al. 2019), and C. regale, but none of them have short peduncles or forked inflorescences as occurs occasionally in C. regale. In most Capsicum species the calyx appendages, when present, are usually cylindrical or subulate, and green-colored. It is very rare to find laterally compressed calyx appendages that appear as wing-like structures, as occur in C. longifolium (Barboza et al. 2019), in some plants of C. dimorphum (Miers) Kuntze (Barboza, pers. obs.), and in C. regale. Stellate corollas lobed about halfway to the base are common in the genus; exceptions to this are found in C. benoistii Barboza (Barboza et al. 2019) and C. regale, both of which have deeply stellate corollas lobed more than halfway to the base. In most Capsicum species, the fruiting pedicels and fruiting calyx are generally green or green with purple tones or lines; only C. caatingae Barboza & Agra (Carrizo García et al. 2016) and sometimes C. dimorphum and C. geminifolium (Dammer) Hunz. (Jarret et al. 2019) have pedicels and calyces uniformly violet-colored, while those of C. regale are uniformly purple-colored. An unusual constriction at the junction of the thickened fruiting pedicels with the fruiting calyx is clearly evident in C. regale (Fig. 2K), a character also present in some other species, i.e., C. chinense Jacq. (Baral and Bosland 2004), C. caatingae (Carrizo García et al. 2013), C. minutiflorum (Rusby) Hunz. (Carrizo García et al. 2016), and C. lanceolatum (Greenm.) C.V. Morton & Standl. (Barboza pers. obs.). The dark blue to purple fruits are unique to C. regale among the wild Capsicum species, which have red, orange-red, or greenish-golden yellow fruits at maturity (Hunziker 2001; Carrizo García et al. 2016).

Carrizo García et al. (2016) were the first to provide an extensive phylogenetic analysis of Capsicum using broad sampling of 34 of the approximately 35 species of the genus known at the time. They identified and named 11 well supported clades within Capsicum. One of these is the Andean clade, which includes species native to Central America and the Andes in northwestern South America. Morphological characters of the Andean clade species include leaves borne in anisophyllous pairs, flowering pedicels straight (not geniculate), corollas mainly yellow, fruits red to orange-red and non-pungent with the pericarp lacking giant cells, seeds black or blackish-brown, and chromosome base numbers of x = 13 (Jarret et al. 2019; Scaldaferro and Moscone 2019). Capsicum regale exhibits all of these characters except for its dark blue or purple fruits and the occasional forked inflorescences, which are not known in any other wild Capsicum species. Molecular data from both chloroplast and nuclear regions place Capsicum regale within the Andean clade (Fig. 6). Although C. regale is morphologically most similar to C. longifolium, the combined molecular data places it in a clade with C. rhomboideum and C. hookerianum with moderate support. Nevertheless, its closest specific affinities need to be further studied using additional data.

Capsicum regale inhabits the Andean-Amazonian Piedmont, encompassing the eastern slopes of the Cordillera Oriental from southern Colombia to the Cerros de Kampanquis, the easternmost branch of the Andes in northern Peru. This area is home to a transitional ecosystem with a distinctive vegetation and biodiversity due, in part, to the juxtaposition between the Amazon basin and the Andean forests (Gentry 1992; Pitman et al. 2002); this unique biodiversity is rapidly disappearing due to intense deforestation, clearing, and fragmentation (Pitman et al. 2002; Mulligan 2010; Tapia-Armijos et al. 2015; Alvarez-B et al. 2019). Some localities where C. regale has been collected are protected areas (Parque Nacional Natural Alto Fragua Indi Wasi, Colombia; Reserva Ecológica Antisana, Ecuador; Estación Biológica Jatun Sacha, Ecuador), and it is expected that in these reserves it is not under serious threat. Other sites in which it occurs are susceptible to human disturbance such as crop planting and high levels of deforestation; these locations include Correg. Caraño (Caquetá, Colombia, Alvarez-B et al. 2019, our observations), Río Bermejo to Cerro Sur Pax (Sucumbíos, Ecuador, Pitman et al. 2002), and Cuenca del Río Morona, Pongo Chinim (Loreto, Peru, Pitman et al. 2012). In these areas, C. regale is considerably threatened, and a conservation strategy is urgently needed to protect these species-rich ecoregions.

Artificial key to the species of Andean clade of Capsicum

1 Flowers solitary, rarely paired; pedicels (15–) 25–43 mm long; calyx with 5 subequal reflexed appendages; corolla white or yellowish-white lined with purple; Mesoamerica C. lanceolatum (Greenm.) C.V.Morton & Standl.
Flowers 2–10 (–13), rarely solitary; pedicels 3–28 mm long; calyx lacking appendages or with up to 10 subequal or unequal, recurved, spreading or erect appendages; corolla pure yellow or yellowish with maroon or purple pigmentation; South America (C. rhomboideum also in Mesoamerica) 2
2 Calyx appendages absent, or appearing as 1–3 small 0.5–1.8 mm long mucronate protuberances below the margin, or well-developed, 2–5, triangular-compressed and wing-like, 2–2.5 mm long 3
Calyx appendages (2–) 5–10, subulate or linear-subulate, (0.9–) 2–7 mm long 5
3 Plants usually pubescent, rarely glabrescent; flowers up to 5, axillary, the rachis very reduced or lacking; calyx with 0–3 small mucronate appendages 0.5–1.5 mm long C. dimorphum (Miers) Kuntze
Plants completely glabrous; flowers 3–13, on a developed rachis; calyx with 2–5 thick triangular-compressed wing-like appendages 1–2.5 mm long 4
4 Leaves coriaceous; major leaves narrowly elliptic (ratio length/width 6–10.8); corolla stellate-campanulate, lobed about halfway to base; calyx tube membranous; stamens equal, 2–2.6 mm long; fruits 8–13 mm in diameter, orange at maturity; fruiting pedicels 1–1.6 cm long, green, pendent; fruiting calyx green-purple or green; seeds 1.7–2.3 mm long, 1.7–2.2 mm wide, not flattened, tear drop-shaped, the surface reticulate C. longifolium Barboza & S.Leiva
Leaves membranous; major leaves elliptic (ratio length/width 2.5–4); corolla deeply stellate, lobed more than halfway to base; calyx tube fleshy; stamens subequal (one longer), (2–) 3–4.3 mm long; fruits 6–9 mm in diameter, dark blue to purple at maturity; fruiting pedicels ca. 1.8 cm long, brilliant dark purple, erect; fruiting calyx entirely brilliant purple; seeds 2.75–3.40 mm long, 2.25–2.70 mm wide, flattened, C-shaped, the surface smooth with small spine-like projections C. regale Barboza & Bohs
5 Calyx with 8–10 unequal appendages, the longer 4–6 (–7) mm long, the shorter 1.3–4 mm long C. hookerianum (Miers) Kuntze
Calyx with 2–5 equal or subequal appendages 0.9–6.5 mm long 6
6 Flowers 1–3, axillary; corolla long tubular-campanulate, 14.5–17 mm long, the tube 11–12 mm long, the lobes broadly ovate, 3.5–5 mm long, 4.5–5 mm wide; stone cells 2 C. piuranum Barboza & S.Leiva
Flowers (2–) 3–10 (–13), axillary or on a short rachis; corolla deeply stellate or campanulate to broadly campanulate, (6–) 7–15 mm long, the tube 3–12 (–15) mm long, the lobes absent or incipient to well developed, narrowly triangular or ovate to broadly ovate, (3–) 5–9 mm long, 2–5.5 mm wide; stone cells absent or 5–6 (fruits unknown in C. benoistii) 7
7 Corolla deeply stellate, 12–13 mm long, the lobes narrowly triangular C. benoistii Barboza
Corolla nearly entire, campanulate to broadly campanulate, (6–) 7–15 mm long, the lobes absent or incipient, ovate to broadly ovate 8
8 Corolla campanulate, stellate in outline, with a thin interpetalar membrane connecting the lobes in the proximal half C. geminifolium (Dammer) Hunz.
Corolla broadly campanulate, pentagonal in outline, with a wide interpetalar membrane connecting the lobes up to the distal end 9
9 Inflorescence up to 13-flowered; major leaves membranous, (4–) 4.8–12 cm long, 2–5 cm wide, ovate, elliptic, or rhomboid-ovate; corolla 6–9.5 mm long, 8–12 mm in diameter; fruits up to 0.9 cm in diameter, dark red at maturity; stone cells absent; trees or erect shrubs; trichomes simple, branched, and dendritic on the same plant C. rhomboideum (Dunal) Kuntze
Inflorescences (2–) 3–8 (–10)-flowered; major leaves coriaceous, (10–) 11–22.5 cm long, (3–) 4–8.5 cm wide, ovate to broadly ovate; corolla 8–15 mm long, 15–18 mm in diameter; fruits up to 1.2 cm in diameter, bright orange or red at maturity; stone cells 0–6; scandent or slender shrub or subshrub; mostly glabrous or sparse, simple trichomes present on young stems only C. lycianthoides Bitter

Acknowledgements

We are indebted to the curators and assistants of the herbaria cited who provided digital images of their collections, to E. Trujillo, A. Orejuela and C. I. Orozco for their assistance in field explorations, to S. Montecchiesi and G. Aburrá for preparing the illustrations, to V. Palchetti for her assistance with the map, to L. Coca, D. Hoyos, D. Sanín, P. Gonzáles, and A. Orejuela for providing photographs or specimen vouchers, to the reviewers for their helpful suggestions and critical reading of the manuscript, and to the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 0100147 and joint project 2014-0401 PCB-FWF AI2119), the Secretaría de Ciencia y Técnica (SECyT-UNC), and the U.S. National Science Foundation ARTS program (DEB 1457366) for funding.

References

  • Alvarez-B C, Castaño D, Hoyos D, Velasco G, Peña JL, Sanín D (2019) Angiospermas no arbóreas de un bosque húmedo tropical en el piedemonte andino-amazónico colombiano. Boletin Cientifico Museo de Historia Natural Universidad de Caldas 23(2): 62–94.
  • Bachman S, Moat J, Hill AW, de Torre J, Scott B (2011) Supporting Red List threat assessments with GeoCAT: Geospatial conservation assessment tool. ZooKeys 150: 117–126. https://doi.org/10.3897/zookeys.150.2109
  • Baral JB, Bosland PW (2004) Unravelling the species dilemma in Capsicum frutescens and C. chinense (Solanaceae): A multiple evidence approach using morphology, molecular analysis, and sexual compatibility. Journal of the American Society for Horticultural Science 129(6): 826–832. https://doi.org/10.21273/JASHS.129.6.0826
  • Barboza GE, Carrizo García C, Leiva González S, Scaldaferro M, Reyes X (2019) Four new species of Capsicum (Solanaceae) from the tropical Andes and an update on the phylogeny of the genus. PLoS One 14(1): e0209792. https://doi.org/10.1371/journal.pone.0209792
  • Bruijnzeel LA, Kappelle M, Mulligan M, Scatena FN (2010) Tropical montane cloud forests: state of knowledge and sustainability perspectives in a changing world. In: Bruijnzeel LA, Scatena FN, Hamilton LS (Eds) Tropical Montane Cloud Forests. Science for Conservation and Management. Cambridge University Press, New York, 691–740. https://doi.org/10.1017/CBO9780511778384.074
  • Carrizo García C, Sterpetti M, Volpi P, Ummarino M, Saccardo F (2013) Wild capsicums: identification and in situ analysis of Brazilian species. In: Lanteri S, Rotino GL (Eds) Breakthroughs in the genetics and breeding of Capsicum and eggplant. Eucarpia, Turin, 205–213.
  • Carrizo García C, Sehr EM, Barfuss MHJ, Barboza GE, Samuel R, Moscone EA, Ehrendorfer F (2016) Phylogenetic relationships, diversification and expansion of chili peppers (Capsicum, Solanaceae). Annals of Botany 118(1): 35–51. https://doi.org/10.1093/aob/mcw079
  • Carrizo García C, Fernández L, Kapetanovic V, Reyes X (2020) Rare Bolivian wild chile Capsicum eshbaughii (Solanaceae) located again: Open ending on its identity and conservation. Plant Systematics and Evolution 306(5): e85. https://doi.org/10.1007/s00606-020-01712-5
  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: More models, new heuristics and parallel computing. Nature Methods 9(8): 772. https://doi.org/10.1038/nmeth.2109
  • Gentry A (1992) Diversity and floristic composition of the Andean forest of Peru and adjacent countries: Implications for their conservation. Memorias del Museo de Historia Natural 21: 11–31. [Biogeografía, Ecología y conservación del bosque Montano en el Perú. Universidad Nacional Mayor de San Marcos, Lima]
  • Hunziker AT (2001) Genera Solanacearum. The genera of Solanaceae illustrated, arranged according to a new system. A.R.G. Gantner Verlag K. -G., Ruggell, 500 pp.
  • Jarret RL, Barboza GE, Da Costa Batista FR, Berke T, Chou Y-Y, Hulse-Kemp A, Ochoa-Alejo N, Tripodi P, Veres A, Carrizo García C, Csillery G, Huang Y-K, Kiss E, Kovacs Z, Kondrak M, Arce-Rodriguez ML, Scaldaferro MA, Szoke A (2019) Capsicum. An Abbreviated Compendium. Journal of the American Society for Horticultural Science 144(1): 3–22. https://doi.org/10.21273/JASHS04446-18
  • Khoury CK, Carver D, Barchenger DW, Barboza GE, van Zonneveld M, Jarret B, Bohs L, Kantar M, Uchanski M, Mercer K, Nabhan GP, Bosland PW, Greene SL (2020) Modelled distributions and conservation status of the wild relatives of chile peppers (Capsicum L.). Diversity & Distributions 26(2): 209–225. https://doi.org/10.1111/ddi.13008
  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054
  • Moscone EA, Lambrou M, Hunziker AT, Ehrendorfer F (1993) Giemsa C-banded karyotypes in Capsicum (Solanaceae). Plant Systematics and Evolution 186(3–4): 213–229. https://doi.org/10.1007/BF00940799
  • Mulligan M (2010) Modeling the tropics-wide extent and distribution of cloud forest and cloud forest loss, with implications for conservation priority. In: Bruijnzeel LA, Scatena FN, Hamilton LS (Eds) Tropical Montane Cloud Forests. Science for Conservation and Management. Cambridge University Press, New York, 14–38. https://doi.org/10.1017/CBO9780511778384.004
  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403(6772): 853–858. https://doi.org/10.1038/35002501
  • Pitman N, Moskovits DK, Alverson WS, Borman AR (2002) Ecuador: Serranías Cofán-Bermejo, Sinangoe. The Field Museum, Chicago. Rapid Biological Inventories Report 3: 1–225.
  • Pitman N, Ruelas IE, Alvira D, Vriesendorp C, Moskovits DK, del Campo Á, Wachter T, Stotz DF, Noningo SS, Tuesta CE, Smith RC (2012) Perú: Cerros de Kampankis. The Field Museum, Chicago. Rapid Biological and Social Inventories Report 24: 1–452.
  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient bayesian phylogenetic inference and model choise across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
  • Scaldaferro MA, Moscone EA (2019) Cytology and DNA content variation of Capsicum genomes. In: Ramchiary N, Kole C (Eds) Compendium of Plant Genomes. The Capsicum Genome. Springer Nature Switzerland AG, Cham, 57–84. https://doi.org/10.1007/978-3-319-97217-6_4
  • Schweizer D, Ambros PF (1994) Chromosome banding. Stain combinations for specific regions. In: Gosden JR (Ed.) Methods in molecular biology 29. Chromosome analysis protocols. Humana Press, Totowa, 97–112. https://doi.org/10.1385/0-89603-289-2:97
  • Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland.
  • Tapia-Armijos MF, Homeier J, Espinosa CI, Leuschner C, de la Cruz M (2015) Deforestation and forest fragmentation in South Ecuador since the 1970s – Losing a hotspot of biodiversity. PLoS One 10(9): e0133701. https://doi.org/10.1371/journal.pone.0133701