CIAT Research Online - Accepted Manuscript Passiflora gustaviana, a New Species of Passiflora (Supersection Laurifolia) from Colombia Revealed by Multivariate Analysis The International Center for Tropical Agriculture (CIAT) believes that open access contributes to its mission of reducing hunger and poverty, and improving human nutrition in the tropics through research aimed at increasing the eco-efficiency of agriculture. CIAT is committed to creating and sharing knowledge and information openly and globally. We do this through collaborative research as well as through the open sharing of our data, tools, and publications. Citation: Ocampo Pérez, John Albeiro; Molinari, Miguel. 2017. Passiflora gustaviana, a New Species of Passiflora (Supersection Laurifolia) from Colombia Revealed by Multivariate Analysis. Systematic Botany 42(4): 1-11 Publisher’s DOI: https://doi.org/10.1600/036364417X696555 Access through CIAT Research Online: http://hdl.handle.net/10568/89930 Terms: © 2017. CIAT has provided you with this accepted manuscript in line with CIAT’s open access policy and in accordance with the Publisher’s policy on self-archiving. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. You may re-use or share this manuscript as long as you acknowledge the authors by citing the version of the record listed above. You may not use this manuscript for commercial purposes. For more information, please contact CIAT Library at CIAT-Library@cgiar.org. 1 OCAMPO AND MOLINARI: PASSIFLORA GUSTAVIANA, A NEW SPECIES FROM 1 COLOMBIA 2 3 4 5 Passiflora gustaviana, a New Species of Passiflora (Supersection Laurifolia) from 6 Colombia Revealed by Multivariate Analysis 7 8 John A. Ocampo Péreza,b,c and Miguel Molinarid 9 10 a Universidad Nacional de Colombia sede Palmira, Facultad de Ciencias Agropecuarias, 11 Departamento de Ciencias Biológicas. Carrera 32 No. 12-00 Chapinero, vía Candelaria 12 Palmira, Valle del Cauca, Colombia. 13 b International Center for Tropical Agriculture, Recta Cali-Palmira, Km. 17 – 14 CIAT/Ecosystem Services, Palmira, Valle del Cauca, Colombia. 15 d Universidad de los Andes, Facultad de Ciencias Forestales, Associate Curator, Hebarium 16 (MER), apartado 384, Mérida 5101, Mérida, Venezuela. 17 c Correspondence author (jaocampo@unal.edu.co) 18 19 Abstract—A new species of Passiflora (supersection Laurifolia, series Laurifoliae) from 20 the Andean region of Colombia is described and illustrated using morphological descriptors 21 analysis. This species is closely related to P. popenovii Killip and can be recognized mainly 22 by its purple stem, leaf size (12.5‒16.5 × 5.0‒7.9 cm), biglandular petioles, pedicel length 23 (8-10 mm), bracts light green, glandless, flowers length (28‒30 mm), corona filaments in 24 2 five series, minute-filiform inner filaments length (1‒4 mm), fimbriate purplish operculum 25 margin, staminal filaments length (6.8‒7.1 mm), ovary glabrous, yellow mature fruits 26 mottled with irregular white dots, lightly pubescent, and total soluble solids content in fruit 27 juice (13.5%‒14.3%). The newly identified species P. gustaviana grows on the slopes of 28 high mountains between 1,900 and 2,309 m above sea level, with an annual mean 29 temperature of 16.2°C. It is considered a new endemic species of Colombia and may be 30 regarded as endangered (EN) because of its limited occurrence. This new species 31 constitutes an important unexploited genetic resource useful for the improvement of 32 cultivated Passiflora species. 33 34 Keywords—Conservation, endemism, IUCN red list, Laurifoliae, PCA, Passifloraceae, 35 Tropical Andes. 36 37 Passiflora L. is the largest genus in the family Passifloraceae Juss. ex Roussel, with more 38 than 577 species of vines, lianas, shrubs, and trees. Passiflora is split into five subgenera 39 (Astrophea (DC.) Mast., Decaloba (DC.) Rchb., Deidamioides (Harms) Killip, Passiflora 40 L., and Tetrapathea (DC.) P. S. Green) distributed mainly in the Neotropics, from coastal 41 zones up to 4,300 m above sea level in the Andean slopes at páramo limits (Ulmer and 42 MacDougal 2004; Krosnick et al. 2009). Subgenus Passiflora includes ca. 240 species and 43 is divided into six supersections with several particular features, such as having petiolar 44 nectaries, variable leaf shape, large colorful flowers, large fruits (Killip 1938; Feuillet and 45 MacDougal 2003; MacDougal and Feuillet 2004), a chromosome number that usually is n 46 = 9, and an average genome size of 1.311 pg (Snow and MacDougal 1993; Yotoko et al. 47 3 2011). Pollinators include carpenter bees, bumblebees, honeybees, wasps, birds (mostly 48 short and sword-billed hummingbirds) and bats, with specific suites of floral characteristics 49 associated with each syndrome (Ulmer and MacDougal 2004; J. Ocampo pers. obs.). 50 51 Colombia has 174 reported species of Passiflora, being the country with the highest 52 Passiflora richness and with the greatest diversity in the Andean region (Ocampo et al. 53 2007; Hernández et al. 2017). The largest number of species is found between 1,000 and 54 2,000 m above sea level and the most common species thrive in disturbed habitats, such as 55 roadsides, cultivated land, and secondary forests (Ocampo et al. 2010). Thirty three 56 inventoried species are included in supersection Laurifolia (Cervi) Feuillet & MacDougal 57 series Laurifoliae Killip ex Cervi with Colombia being the center of diversity with 12 58 species, followed by Brazil and Venezuela with 10 species each (Ocampo et al. 2011). 59 Laurifoliae species include vigorous vines that often cover the trees used as support. 60 Species in this series are very easy to recognize by their filiform to linear stipules, one pair 61 of petiolar nectaries, and their generally long, dark green, glossy, unilobed and acuminate 62 leaves (Rome and Coppens d´Eeckenbrugge 2017). The pendent flowers have a corolla that 63 is often campanulate (except in P. guazumaefolia Juss., P. odontophylla Harms ex Glaziou, 64 and P. kikiana Cervi & Linsingen) and of a delicate white or cream to red and purple color, 65 frequently tinged slightly with violet (Ocampo et al. 2011). Their corona is formed of long 66 pendent filaments striated with deep violet and attached to a short hypanthium. In other 67 species, such as P. ambigua Hemsl., P. popenovii Killip, and P. pergrandis Holm-Nielsen 68 & Lawesson, the flowers are grouped on small branches with minute leaves and short 69 internodes, which gives the impression of a dense inflorescence (Ulmer and MacDougal 70 2004). The fruits are large (except in P. gabrielliana Vanderpl., 3.5–7.5 × 2.5–5.2 cm), 71 4 round to ovate, yellow to orange mottled with irregular white points, and with a thick 72 mesocarp. The arils present a firm consistency, and the whitish translucent pulp is strongly 73 aromatic. Most species have edible fruits and the seeds are dispersed by tree-climbing 74 arboreal mammals (e.g. monkeys and coatis), because the fruits do not fall after maturing. 75 The series Laurifoliae is particularly interesting for the economic development of new fruit 76 crops, while its attractive and colorful flowers also give the plant an ornamental value 77 (Ocampo et al. 2011; Rome and Coppens d´Eeckenbrugge 2017). Additionally, the 78 remarkable capacity of species in the series to grow on flooded soils (e.g. P. riparia Mart. 79 ex Mast., P. gabrielliana, P. guazumaefolia), as well their resistance to soil parasites (e.g. 80 P. nitida, P. odontophylla) are of interest for developing rootstocks and for transferring the 81 corresponding genes to other passion fruit species (Yockteng et al. 2011; Ocampo and 82 Coppens d´Eeckenbrugge 2017). 83 84 On the other hand, the general similarity in most organs frequently makes it difficult to 85 distinguish particular species, so as that the prominent Passiflora taxonomist Killip (1938) 86 and other experts of series Laurifoliae (Vásquez 1998; MacDougal and Feuillet 2004; 87 Rome and Coppens d´Eeckenbrugge 2017) have considered it as an "exceedingly difficult" 88 group. In several cases, both experts as well as amateurs may have underestimated the 89 infra-specific variation in widely distributed species, or even infra-individual variation, 90 splitting well known species into several new species only distinguished by a few 91 quantitative or qualitative traits, such as color. In series Laurifoliae, identification of 92 species into several morphological groups demands experience and caution, even for the 93 most common species such as P. ambigua, P. nitida, P. laurifolia and P. tolimana Harms, 94 5 which display high infra-specific variability and wide geographic distribution. For instance, 95 P. metae M. Bonilla, C. Aguirre & C. Caetano was recently described from Colombia 96 without taking into account the infra-specific variation; after rigorous revision based on 97 herbaria and field observations we consider it synonymous with P. tolimana (M. Rome and 98 G. Coppens, pers. comm.; J. Ocampo pers. obs.). 99 Multivariate analyses of morphological descriptors are a tool that can be used to solve 100 issues between closely related taxa. Despite the remarkable morphological diversity 101 described among species of series Laurifoliae, few studies have compared infra- and 102 interspecific variation with statistical tools. A recent and detailed list of descriptors was 103 used by Ocampo and Coppens d´Eeckenbrugge (2017) to study morphological divergence 104 of 61 species of genus Passiflora, showing a clear separation among the subgenera 105 Astrophea, Decaloba and Passiflora with special emphasis on quantitative and qualitative 106 floral traits. The morphological cladistic analysis supported the delimitation of the species 107 and with particular infra-specific morphological variation in some species, such as P. 108 popeonovii, P. nitida, P. maliformis L., and P. edulis Sims. 109 In this paper we propose a new species, P. gustaviana, belonging to subgenus Passiflora, 110 supersection Laurifolia, series Laurifoliae, discovered in Colombia. This new species is 111 described, illustrated and compared with its closest relative P. popeonovii, using a phenetic 112 approach. 113 114 MATERIALS AND METHODS 115 6 In June 2004, Gustavo Morales of the Botanical Garden of Bogotá “José Celestino Mutis” - 116 JBB (Cundinamarca, Colombia) found a mature fruit of a Passiflora plant belong to 117 Passiflora series Laurifoliae along the roadside in a secondary forest in right margin in 118 Kilometer 2 between the municipalities of Pacho and Supatá (2,079-2,150 m), department 119 of Cundinamarca. Its seeds were extracted and later germinated and two seedlings were 120 planted in the JBB at 2,550 m above sea level in June 2006. Four years later, the plants 121 bloomed for the first time in August and theirs fruits were harvested in October of that 122 same year. Afterwards, this probable new species was compared with other species of 123 Laurifoliae and based on previous studies (Ocampo et al. 2011; G. Morales. pers. obs.), P. 124 popenovii was established as its morphologically closest relative species. 125 126 The morphological description was carried out in situ on living specimens of P. gustaviana 127 and the morphologically similar species P. popeonovii, using 42 quantitative and 51 128 qualitative vegetative and reproductive descriptors (Table 1). These descriptors were 129 assessed for individual sample taken from Colombia: two cultivated plants of P. gustaviana 130 planted in the JBB, and four plants of P. popenovii cultivated in home gardens in the 131 municipalities of Chachagui (Nariño) and Timbio (Cauca). Five measurements were taken 132 for the quantitative characters of each individual. A principal component analysis (PCA) 133 was carried out with quantitative data applying the varimax normalized rotation option, and 134 factors with an eigenvalue greater than one were retained. Additionally, Duncan's multiple 135 comparison test between means (95% confidence level) for each descriptor was used to 136 compare variation among species, using the R package (Pardo and Del Campo 2007). The 137 total soluble solids content (˚Brix) found within the fruit´s juice of quantitative characters 138 was estimated with the help of a hand held Brix refractometer (ATC). The color of the 139 7 qualitative characters was then recorded, using the Royal Colour Chart (Royal Horticultural 140 Society 2001). We followed the infrageneric classification of Feuillet and MacDougal 141 (2003). 142 143 Three expeditions to study highland Laurifoliae species in the field were carried out in 144 2010 to 2016 in 42 different localities within six departments (Antioquia, Boyacá, 145 Cundinamarca, Nariño, Tolima, and Valle del Cauca) of Colombia. Identifying data were 146 recorded for each specimen collected, which include locality, habitat, elevation and 147 geographic coordinates. Additionally, we examined specimens of series Laurifoliae from 148 the major herbaria in Colombia (AFP, CAUP, CDMB, CHOCO, COL, COAH, CUVC, 149 FAUC, FMB, HUA, HUQ, JBB, JAUM, MEDEL, PSO, SURCO, TOLI, TULV, VALLE, 150 and UIS) and other countries (F, GH, K, QCA, MA, MO, MOL, NY, P, TX, US, and 151 USM). Dried specimens were recorded and photographed to create a species description of 152 Colombian Laurifoliae. This database of field and herbaria data that we employed was 153 supplemented with specimens mentioned in various species descriptions published by 154 Killip (1938, 1960), Holm-Nielsen et al. (1988) and Ulmer and MacDougal (2004). The 155 description was created following the Passiflora morphological terminology proposed by 156 Tillett (1988). The data were gathered and cleaned with OpenRefine (Verborgh and de 157 Wilde 2013) to generate a dot map of the distribution of the P. gustaviana collections, 158 using the ArcMap 10.3 software. Finally, conservation status was assessed according to 159 IUCN (2014) categories and supported with geographic distribution data, based on the 160 extent of occurrence (EOO) and area of occupancy (AOO), found using the Geospatial 161 Conservation Assessment Tool - GeoCAT (Bachman et al. 2011). 162 163 8 164 RESULTS 165 Two specimens belonging to the new P. gustaviana were registered during the collection 166 trips, found growing mostly in disturbed habitats like road borders and secondary forest 167 margins. Regarding herbaria revisions, only four dried specimens deposited in the herbaria 168 of the Instituto de Ciencias Naturales (ICN) of the Universidad Nacional de Colombia 169 Bogotá branch (COL), and the José Celestino Mutis Botanical Garden of Bogotá (JBB) 170 were recorded as P. gustaviana. In relation its closest relative P. popenovii, 20 records from 171 herbaria (12) and field collections (8) under cultivation were registered in the departments 172 of Cauca and Nariño in the south-west of Colombia. A dot map of the spatial distribution of 173 P. gustaviana based on the six known records of the species, representing our recent field 174 collections and existing herbarium specimens, is shown in Fig. 1. 175 176 Multivariate analysis identified 31 quantitative descriptors with high interspecific variation. 177 Three principal components with an eigenvalue superior to one were retained, representing 178 96.1% of the total variation (Table 2). The first component (62%) is primarily associated 179 with 24 descriptors characterizing internode length, stipule length, lobe size, petiole 180 nectaries, bract size, flower length, longest inner filament of corona length, sepal length, 181 petal width, nectary chamber size, hypanthium diameter, androgynophore length, staminal 182 filaments length, ovary length, fruit size/weigth/total soluble solids content in juice, and 183 seed length. The second component (26%) is represented by pedicel length, the corona`s 184 outermost filament length, petal length, sepal width, hypanthium length, and styles length. 185 The third component (7.4%) is only associated with operculum length. Fig. 2 shows the 186 9 individuals in the principal plane (88.3% variance total), showing a clear grouping by 187 species and geographic origin. The representatives of P. gustaviana are placed on the right 188 side along the first axis in relation to their larger size of leaves, flowers and fruits, and 189 greater total soluble solids content in fruit juice (˚Brix), in relation to individuals of P. 190 popenovii. Additionally, the 31 descriptors selected by PCA showed significant differences 191 according to Duncan's multiple comparison test between the individuals of P. gustaviana 192 and P. popenovii (Table 2). 193 194 Qualitative descriptors analysis identified 10 of the 51 descriptors evaluated on the basis of 195 their potential to discriminate among species. These descriptors were associated with stem 196 color (mature branch), and bract color and glandless, shape and color of inner filaments of 197 the corona, operculum margin, ovary pubescence, and color of mature fruits. Table 3 198 synthesizes the observations for quantitative and qualitative descriptors between P. 199 gustaviana and its closest relative P. popenovii. 200 201 202 TAXONOMIC TREATMENT 203 Passiflora gustaviana Ocampo & Molinari, sp. nov.—TYPE: COLOMBIA. 204 Cundinamarca: Bogotá D.C, frutales de clima frío, de semillas colectadas en Supatá vía 205 Pacho (Cundinamarca). Alt. 2,550 m.s.n.m, 17 August 2010, Gustavo Morales 3190 206 (holotype: JBB!); 207 208 10 Plant woody vine or liana. Stem terete, slender, striate, glabrous, purple colored (mature 209 branch) to green colored (young branch). Stipules narrowly linear, 8‒13 mm long, 0.5 mm 210 wide, not glandular, green, soon deciduous. Tendrils glabrous, red to purple colored and up 211 to green. Petioles 1.5‒2.7 cm long, slightly canaliculate adaxially, glabrous, a pair of round 212 sessile glands (about 1.5 mm long), located on the middle of the petiole, green. Leaves 213 unlobed, oblong-ovate, 12.5‒16.5 cm long, 5‒7.9 cm wide, mucronate and generally 214 acuminate, rounded at base, lustrous on both surfaces, penninerved (lateral nerves 7 or 8 215 pairs), subcoriaceous, margins entire, glabrous, green. Peduncles terete, slender, solitary 216 (sometimes in pairs), 10.5‒12.8 cm long (including pedicel 0.8‒1.0 cm long). Bracts ovate, 217 concave, 3.5‒4 cm long, 2‒2.4 cm wide, rounded, entire, free, glabrous, persistent (until 218 fruit maturity), light-green, glandless. Flowers pendulous, fragrant, 2.8‒3.0 cm long (from 219 the base of the nectary chamber to the ovary apex) × 6.0‒7.2 cm wide, sometimes seen in 220 clusters on pseudoracemes (small branches with short internodes ca. 2‒3 cm, small leaves, 221 and flowers at each node). Nectary chamber glabrous, 4‒5 mm long x 20‒20.1 mm wide, 222 green outside and white inside. Hypanthium campanulate, 6‒7.8 mm long x 22‒24 mm 223 diameter (at the base of the sepals), glabrous, green outside and white inside. Sepals 224 oblong, 4‒4.5 cm long x 2.0‒2.3 cm wide, adaxial surface light-green, abaxial surface 225 white, slightly concave, glabrous, keeled dorsally just below the apex, the keel terminating 226 in a light-green awn about 2 mm long, glabrous. Petals white, linear-oblong, 3.8‒4.1 cm 227 long x 1.4‒1.8 cm wide, glabrous, reflexed. Corona filaments in five series, two major outer 228 series, white, banded (4‒7 bands) purplish blue, the bands purple near base, thickened, 229 fleshy, the second outer series filaments longer (3.6‒3.9 cm long) than the outermost series, 230 the three inner series 1.0‒4.0 mm long, minute, filiform, purplish. Operculum 231 membranaceous, 3.6‒4.5 mm long, slightly recurved, white, fimbriated-filamentous at the 232 11 margin, purplish. Limen none. Androgynophore white (sometimes speckled with dark 233 purple), 16‒17 mm long, trochlea 5‒7 mm long. Gynophore white, 1 mm long. Staminal 234 filaments white (sometimes finely speckled with dark purple), 9.0‒10.0 mm long. Ovary 235 glabrous, ovoid, 5‒6 mm long, olive green. Styles white (occasionally finely speckled with 236 dark purple at base), 6‒7 mm long, stigmas greenish-white. Fruit ovoid, 8.1‒8.5 cm long × 237 6.5‒6.7 cm diameter, lightly pubescent, immature green mottled with irregular white dots; 238 mature weights 78‒120 g, yellow mottled with irregular white dots, pericarp 1.1‒1.3 cm 239 thick; pulp aromatic, pleasant odor, flavor slightly sweet and acidic, total soluble solids 240 content in fruit juice 13.5‒14.3 (˚Brix), edible. Seeds obovate, 9‒10 mm long × 4‒5 mm 241 wide, dark brown, testa reticulate, acute at apex, 78‒84 seeds per fruit, surrounded by a 242 translucent white aril. Figures 3, 4. 243 244 Geographical Distribution—Rare, endemic to the Colombian Department of Cundinamarca 245 (4,3853˚ to 5,0712˚ North and 74,2048˚ to 74,4339˚ West), Municipalities of Albán (2,309 246 m), Silvania (1,900 and 2,000 m), Pacho (2,079 m), and Supatá (2,150 m) on the Eastern 247 flank of the Cordillera Oriental in the Andean region (Fig. 1). 248 Etymology—The specific epithet honors the Colombian botanist Gustavo Morales, who 249 discovered this new species, has spent most of his life enriching the knowledge of 250 Colombian botany, and has constantly fought for the conservation of plant resources, 251 especially passion flowers. 252 Ecology—Passiflora gustaviana was observed on hillsides, along roadsides and along 253 secondary cloud forest margins, climbing onto trees found in thickets, at elevations ranging 254 from 1,900 to 2,309 m above sea level in the department of Cundinamarca. This species 255 12 grows in areas with soils derived of volcanic ashes with middle organic matter content 256 levels, and with a sandy-clay-loam texture; the annual mean temperature is 16.2°C and the 257 annual rainfall is 1,241 mm (regular rainfall); and on average 4‒5 sunshine hours per day 258 (Ideam 2016). 259 Phenology—This new species has been observed flowering in the months of March-April 260 to August-September, and fruiting from May-June to October-November. Carpenter bees 261 (Xylocopa sp.) were observed visiting open flowers and may be associated as a pollinator of 262 the species. 263 Conservation Status—Passiflora gustaviana is known only from few collections and would 264 likely be classified as endangered (EN) based on two assessment criteria, B2a and D, if we 265 had fully conducted its conservation assessment using IUCN (2014) guidelines. Within 266 category B, the new species is classified as B2a, as its area of occupancy is estimated as 267 less than 500 km2 (20 km2), and its extended range of occurrence is less than 5,000 km2 268 (890.9 km2); habitats are severely fragmented and it is known to exist at five locations. 269 Regarding criterion D, the population size is estimated to be less than 50 mature 270 individuals, with just three plants observed during the collection trips. 271 272 Additional Collections Examined—COLOMBIA. Cundinamarca: Silvania, Cordillera 273 Oriental, vertiente occidental; estribaciones de la Cuchilla de la Cruz Grande, Km 5-6, 274 arriba de Fusagasugá, La Aguadita, 1,900-2,000 m, 28 May 1954, J.M. Idrobo & J. 275 Hernández 1660 (COL); Albán, frente a la estación del ferrocarril, 2,309 m, 1 Jul 1945, H. 276 García-Barriga 11610 (COL); Pacho, 2 km vía a Supatá, vereda la Esmeralda, 2,150 m, 20 277 June 2004, G. Morales, M. Quintero & C. González 2369 (JBB). 278 13 279 Additional Collections Examined of Passiflora popenovii—COLOMBIA. Cauca: El 280 Tambo, 1,700 m, 15 January 1938, K. von Sneiden 1444 (US); Gazaabarita, 14 January 281 1965, J.M. Idrobo 5636 (COL); entre el Tambo y el Alto del Rey, cultivada, 1,800 m, 11 282 January 1979, L.K. Escobar & D. Escobar-Uribe 1017 (HUA); corregimiento San Joaquín, 283 vereda Pomoroso, finca los Naranjos, cultivada, 1,767 m, 6 February 2004, C. M. Caetano, 284 L. Barrios, M. Restrepo & J. Ocampo 009 (VALLE); Timbío, zona urbana Barrio Boyacá, 285 cultivada, 1,875 m, 5 May 2002, C.A. Chicangana 22 (CAUP); Vereda Santa María, n.v. 286 Granadillo de Quijos, 1,700 m, 1990, R. Durán & J. Otálora 01 (TOLI). Cundinamarca: 287 Bogotá D.C., enredadera procedente de Timbío Cauca, cultivada, 2,550 m (4.66788 N; 288 74.09977 W), 16 August 2013, G. Morales 3630 (JBB). ECUADOR. Rio Jamboya, 2,000 289 m, 1882, A. Mille 223 (US); Pichincha: Quito, L. Sodiro s.n (P); Tunguragua: Baños, 1,850 290 m (introduced), 3 June 1921, W. Popenoe 1271 (US, type); EL Oro, 24 January 1995, 1,400 291 m, V. Eynden 218 (MO), Piñas, Sambotambo, cultivada, 2 September 1997, V. Eynden 927 292 (QCA). 293 294 295 DISCUSSION 296 A shorter list of 33 quantitative and 10 qualitative traits showed a high variability according 297 to a morphological characterization analysis (Table 3). This analysis supports the 298 classification of P. gustaviana as a new species of Passiflora, subg. Passiflora, supersect. 299 Laurifolia, series Laurifoliae (Ocampo et al. 2011). Passiflora gustaviana is distinguishable 300 from other highland Laurifoliae species that occur in the Andean region in Colombia 301 14 (>1,000 m.a.s.l.) such as P. ambigua, P. pergrandis Holm-Nielsen & Lawesson, and P. 302 tolimana Harms by the position (on the middle) and shape (round) of the petiole glands, 303 large and slender peduncles (10.5‒12.8 cm long), corona filaments in five series, operculum 304 margin with short fimbriate filaments (purplish), and distinct size of the flowers (2.8‒3.0 305 cm long x 6‒7.2 cm wide) and fruits (8.1‒8.5 cm long x 6.5‒6.7 cm diameter). 306 Additionally, the new species was compared to its putative closest relative P. popenovii, 307 using information gathered from specimens that were recorded during collection trips and 308 herbaria visits, as well as found within the literature (Killip 1938, 1960; Holm-Nielsen et al. 309 1988; Ulmer and MacDougal 2004). Passiflora gustaviana is related to P. popenovii, but 310 differs by its stem color (mature branch, purple vs. green); stipule length (8‒13 mm vs. 10‒311 17 mm); leaf size (12.5‒16.5 cm long × 5.0‒7.9 cm wide vs. 10.0‒12.5 cm long × 3.9‒5.1 312 cm wide); petiole glands (one pair vs. glandless); pedicel length (8‒10 mm vs. 5‒8 mm); 313 bract, sepal and petal size (see Table 3); bract color (light-green vs. reddish-purple), grands 314 (glandless vs. 3‒4 pairs); corona filaments (5-series vs. 6-series), outermost longest 315 filament length (3.6‒3.9 cm vs. 3.0‒4.4 cm), inner longest filament length (3‒4 mm vs. 316 4.0‒5.5 mm), shape of the inner filament (minute-filiform vs. capillary) and color (purplish 317 vs. white and purplish-blue at apex); also in its operculum margin (fimbriated and purplish 318 vs. entire and white); staminal filaments length (9.0‒10.0 mm vs. 6.8‒8 mm); ovary 319 (glabrous vs. pubescent); color of mature fruits (yellow, mottled with irregular white dots 320 vs. yellow-orange); percentage of total soluble solids content in fruit juice (13.5‒14.3 % vs. 321 14.8‒16.8 %); and flavor (slightly sweet-acidic vs. sweet). 322 Passiflora gustaviana has only been encountered in the Department of Cundinamarca in 323 Colombia on the Eastern flank of Cordillera Oriental in the Andean region between 1,900 324 15 to 2,309 m above sea level, along roadsides, in secondary forest margins and climbing onto 325 trees found in thickets. Passiflora popenovii was proposed as a new species by Killip in 326 1922 based on a plant cultivated in the municipality of Baños at 1,850 m.a.s.l. 327 (Tungurahua, Ecuador), with seeds brought from the Eastern slopes of the Andes in 328 Ecuador by W. Popenoe (W. Popenoe 1271, US, type), but there is no record on whether 329 these seeds came from wild or cultivated plants. This species has only been found 330 cultivated in home gardens in the south-western part of Colombia (Cauca and Nariño 331 Departments) and Ecuador (El Oro, Loja, Pichincha and Tungurahua Provinces) under the 332 vernacular names of Curubejo, granadilla de Quijos or granadilla Caucana, and where it is 333 regularly propagated by cuttings (National Research Council 1989). Currently, its origin is 334 unknown and no wild representative of P. popenovii has been reported, so some authors 335 consider it extinct outside of cultivation (Ocampo et al. 2007; Yockteng et al. 2011). 336 The discovery of this new rare endemic species increases to 12 the number of species 337 (Table 4) belonging to the series Laurifoliae reported in Colombia (Ocampo et al. 2007, 338 2010, 2011), and suggests that this country concenters the highest species diversity, 339 followed by Brazil. However, Colombia might still harbor many more unknown species, 340 given the low level of exploration in various zones of the Andes, the Caribbean, the 341 Amazon, the Orinoquia and the Pacific (Ocampo et al. 2007, 2010, 2015). Additionally, the 342 discovery of this new species in Colombian territory brings into question the putative 343 Ecuadorian origin of P. popenovii due to its morphological proximity and similar 344 ecological habitat to P. gustaviana. We here hypothesize that P. popenovii may be an 345 undiscovered species of Colombia that could be found growing on the slopes of high 346 mountains of the Colombian Andes. 347 16 348 349 Passiflora is considered as a biodiversity indicator in Colombia as its species have multiple 350 ecological interactions with many types of organisms (Ocampo et al. 2010), as such, it can 351 be considered to indirectly provide an ecosystem service through the regulation of 352 populations of other species. However, the species distributions have been drastically 353 affected mainly by the deforestation of rain and cloud forests in the Andean, Amazon, and 354 Pacific regions. This has occurred mainly due to extensive livestock production (pasturing), 355 plantations of illicit crops, hydroelectric dams, illegal gold mines, and agricultural practices 356 that currently support extensive coffee, sugar cane, rice, banana, and potato plantations 357 (Ocampo et al. 2007, 2010). 358 Indeed, the disappearance of Passiflora species from the ecosystem would entail the loss of 359 other organisms that depend on these, such as butterflies (Heliconius species) and many 360 nectar feeding insects, mammals (bats), and birds (Yockteng et al. 2011). In this context, 361 not only the species of the genus Passiflora, but also most of the Colombian Passifloraceae 362 (71%) are under some degree of threat according to the IUCN criteria (Ocampo et al. 363 2007). The discovery of P. gustaviana during field surveys growing on road edges in 364 severely fragmented habitats, as well as the fact that it has been classified as a probably 365 threatened species within the Endangered (ED, B2a, D) status, emphasizes the need for 366 conservation. Ex situ conservation techniques at botanical gardens and seed banks (e.g. 367 cryopreservation) are strategies that must be implemented in case critical habitats are 368 destroyed. These strategies have already begun to be implemented by the Botanical Garden 369 17 of Bogotá “José Celestino Mutis”, where individuals of the new species are under 370 cultivation. 371 372 In conclusion, statistical analysis allowed for the classification and determination of a new 373 species of Passiflora from 41 discriminant morphological descriptors, as well as its fruit 374 properties, P. gustaviana constitutes a promising new genetic resource and ecosystem 375 service as a wild relative useful for the improvement of cultivated Passiflora species. 376 377 ACKNOWLEDGEMENTS. The authors wish to thank the curators of the herbaria that 378 provided specimens for this study, as well as the Botanical Garden of Bogotá “José 379 Celestino Mutis” for its generosity and assistance with the cultivation of P. gustaviana. The 380 first author gratefully acknowledges the financial support of the Gines-Mera Fellowship 381 Foundation (CIAT-CBN). This author would also especially like to thank Grupo de 382 Investigaciones en Recursos Fitogenéticos Neotropicales (GIRFIN/UNAL Palmira) for 383 their persistent and inspirational efforts to use and value our plant resources. Our most 384 grateful appreciation and thanks to Hernán Dario Bernal and Jorge Julián Restrepo for their 385 assistance during some collection trips carried out in Cundinamarca and Antioquia, 386 respectively. We also thank our anonymous reviewers, James Smith (our chief editor) and 387 Natalie Orentlicher (for copy editing) for their contributions to the last version of the 388 manuscript. 389 390 LITERATURED CITED 391 18 Bachman, S., J. Moat, A. Hill, J. de la Torre, and B. Scott. 2011. Supporting red list threat 392 assessments with GeoCAT: Geospatial conservation assessment tool. Zookeys 150: 393 117–126. 394 395 Feuillet, C. and J. M. MacDougal. 2003 [2004]. A new infrageneric classification of 396 Passiflora L. (Passifloraceae). 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Passiflora. Pp. 129-483 171 in Wild crop relatives: Genomic and breeding resources. Tropical and 484 subtropical fruits. ed. K. Chittaranjan. Berlin: Springer Verlag. 485 486 Yotoko, SC., M. C. Dornelas, P. D. Togni, T. C. Fonseca, F. M. Salzano, S. L. Bonatto, and 487 F. B. Freitas. 2011. Does variation in genome sizes reflect adaptive or neutral 488 processes? new clues from Passiflora. PLoS ONE 6: e18212. 489 doi:10.1371/journal.pone.0018212.t001 490 491 492 TABLE 1. List of 93 morphological descriptors evaluated in this study. Scales for qualitative characteristics: B 493 (binary), O (Ordinal), and N (Nominal). 494 Organ Qualitative characters (51) Quantitative characters (42) Stem Pubescence (N) Internode length (mm) Color (N) Tendril Pubescence (N) Color (N) Anthocyanin (O) Stipule Permanence (B) Length (mm) Color (N) Width (mm) Pubescence (N) Shape (N) Margin (N) Anthocyanin (O) Color (N) Leaf Margin (N) Petiole length (mm) Base shape (N) Petiole nectaries (number) Apex shape (N) Lobe length (mm) Presence of acumen (B) Lobe width (mm) Pubescence – adaxial (N) Margin nectaries (number) Pubescence – abaxial (N) Anthocyanin – lamina (O) Anthocyanin – nerves (O) Color – adaxial (N) Presence of laminar nectaries (B) Peduncle Pubescence (N) Length (mm) Color (N) Diameter (mm) Anthocyanin (O) Pedicel length (mm) Bract Permanence (B) Length (mm) Pubescence (N) Width (mm) Color (N) Margin nectaries (number) 23 Anthocyanin (O) Shape (N) Flower Color sepals (N) Length (mm) Sepal awn (B) Width (mm) Color petals (N) Sepal length (mm) Color filaments at base (N) Sepal width (mm) Color of filaments at apex (N) Petal length (mm) Color hypanthium (N) Petal width (mm) Hypanthium pubescence (N) Outer filaments series of corona - radii (number) Color androgynophore (N) Outer longest filament of corona length (mm) Color staminal filaments (N) Inner filaments series of corona – pali (number) Color of ovary (N) Inner longest filament of corona length (mm) Ovary pubescence (N) Hypanthium length (mm) Color of styles (N) Hypanthium diameter at base (mm) Color operculum (N) Hypanthium diameter at above (mm) Color operculum margin (N) Nectary chamber length (mm) Nectary chamber diameter (mm) Operculum length (mm) Androgynophore length (mm) Gynophore length (mm) Staminal filaments length (mm) Ovary length (mm) Styles length (mm) Fruit Shape (N) Weight (g) Color fruit immature (N) Length (mm) Color fruit mature (N) Diameter (mm) Pubescence (N) Seeds per fruit (number) Color aril (N) Total soluble solids (˚Brix %) Seed Shape seed (N) Length (mm) Color seed (N) Width (mm) 495 TABLE 2. Factor loadings from the principal component analysis (varimax normalized rotation) carried out on 496 37 quantitative descriptors. Bold values (Eigenvalues) contribute most to proportion of variance explained 497 Descriptors Components 1 2 3 Internodes length 0.870 -0.144 0.427 Stipule length -0.826 -0.437 0.329 Lobe length 0.888 0.387 -0.009 Lobe width 0.926 0.276 0.069 Petiole length 0.688 0.633 0.337 Petiole nectaries 0.999 -0.014 0.027 Penduncle length 0.392 -0.678 -0.606 Pedicel length 0.005 0.809 0.580 Bract length 0.962 -0.265 -0.058 Bract width 0.948 -0.307 0.024 Flower length -0.729 -0.192 0.588 Flower width 0.097 -0.626 0.418 Outermost filament of corona length -0.175 0.928 -0.095 Inner filaments series of corona -0.998 -0.012 0.039 24 Inner longest filament of corona length -0.999 0.014 -0.027 Petal length 0.346 0.918 0.175 Petal width 0.849 0.470 0.229 Sepal length 0.905 0.400 0.093 Sepal width 0.232 0.917 0.323 Nectary chamber length 0.815 0.105 0.561 Nectary chamber diameter 0.944 -0.327 -0.013 Hypanthium length 0.179 0.940 -0.100 Hypanthium diameter at base 0.960 -0.271 -0.017 Hypanthium diameter above 0.984 -0.156 -0.049 Operculum length 0.348 0.365 0.845 Androgynophore length 0.782 0.464 0.403 Staminal filaments length -0.999 0.014 -0.027 Ovary length -0.869 -0.461 -0.042 Styles length -0.204 0.949 0.232 Fruit weigth 0.999 0.023 0.011 Fruit length 0.924 0.215 0.080 Fruit diameter 0.936 0.301 0.041 Number seeds per fruit -0.650 -0.067 -0.395 Total solid solubles content (˚Brix) -0.898 0.015 -0.275 Seed length 0.986 -0.113 0.068 % Total variance 62.425 25.964 7.740 Eigenvalue 23.097 9.607 2.864 498 TABLE 3.Summary and comparison of morphological characters between P. gustaviana (Pg) and P. popenovii 499 (Pp). 500 25 501 502 TABLE 4. List of Laurifoliae species inventoried in Colombia according to Ocampo et al. (2007, 2010, 2011). 503 504 FIG. 1. Geographical distribution of P. gustaviana (red dots) on Eastern Cordillera in the Colombia`s Andean 505 region from herbarium and field collections. 506 Organs Descriptors Minimum Maximum Mean Std.Dev. Coef.Var. Minimum Maximum Mean Std.Dev. Coef.Var. Pg Pp Stem Internodes length mm 32.0 - 80.0 61.6 13.9 22.6 22.0 - 46.0 35.4 5.5 15.6 a b Stem color (mature branch) Stipules Stipule length mm 8.0 - 13.0 10.2 1.4 13.7 10.0 - 17.0 11.9 1.5 12.5 a b Leaves Lobe length mm 125.0 - 165.0 143.4 15.6 10.9 100.0 - 125.0 116.2 8.1 6.9 a b Lobe width mm 50.0 - 79.0 63.1 9.3 14.7 39.0 - 51.0 46.1 3.9 8.4 a b Petiolar glands Pedicel Pedicel length mm 8.0 10.0 9.2 0.8 8.3 5.0 9.0 6.9 1.2 18.1 a b Flowers Flower length mm 28.0 - 30.0 29.0 0.9 3.3 30.0 - 31.0 30.5 0.5 1.7 a b Flower width mm 60.0 72.0 65.5 4.3 6.5 60.0 80.0 71.7 7.1 9.9 a b Bract length mm 35.0 - 40.0 37.2 1.3 3.5 20.0 - 30.0 23.4 2.7 11.7 a b Bract width mm 20.0 - 24.0 21.9 1.2 5.4 11.0 - 18.0 14.8 1.9 12.9 a b Bract glands Color bract Petal length mm 38.0 41.0 39.1 1.0 2.5 25.0 44.0 36.0 5.5 15.2 a b Petal width mm 14.0 - 18.0 15.8 1.1 7.0 10.0 - 15.0 11.8 1.7 14.3 a b Sepal length mm 40.0 - 45.0 43.0 1.3 3.1 36.0 - 42.0 40.0 1.7 4.2 a b Sepal width mm 20.0 23.0 21.8 0.9 4.1 16.0 24.0 20.6 3.2 15.4 a b Outer longest filament of corona length mm 36.0 39.0 37.8 0.9 2.4 30.0 44.0 39.0 4.2 10.8 a b Inner filaments series of corona Inner longest filament of corona length mm 3.0 4.0 3.4 0.5 13.6 4.0 5.5 4.5 0.5 12.3 a b Shape inner filaments Color of inner filaments Hypanthium length mm 12.4 14.0 13.1 0.5 3.8 8.2 11.5 9.9 1.2 11.8 a b Hypanthium diameter at base mm 20.0 - 21.0 20.7 0.4 2.2 12.0 - 16.0 13.5 1.4 10.3 a b Hypanthium diameter above mm 22.0 - 24.0 23.1 0.7 3.1 14.0 - 19.0 15.9 1.4 8.6 a b Nectary chamber length mm 7.0 - 9.0 8.2 0.6 7.0 3.0 - 5.6 4.4 0.6 14.1 a b Nectary chamber diameter mm 20.0 - 21.0 20.7 0.4 2.2 12.0 - 17.0 14.3 1.6 10.9 a b Operculum length mm 3.6 4.3 4.1 0.2 5.6 3.0 5.0 3.9 0.6 14.4 a b Operculum margin Color operculum margin Androgynophore length mm 16.0 - 17.0 16.6 0.3 2.0 9.0 - 16.0 12.5 2.1 16.8 a b Staminal filaments length mm 6.8 - 7.1 6.9 0.1 1.3 6.0 - 9.9 8.4 1.2 14.5 a b Ovary length mm 5.0 - 6.0 5.7 0.3 5.4 6.0 - 7.8 6.8 0.9 12.3 a b Ovary pubescense Styles length mm 6.0 7.0 6.3 0.3 5.1 5.0 9.0 6.9 1.6 22.9 a b Fruits Fruit weigth g 199.0 - 210.0 203.3 3.1 1.5 78.0 - 120.0 100.4 12.7 12.7 a b Fruit length mm 81.0 - 85.0 82.8 1.2 1.5 63.0 - 88.0 69.9 5.6 8.0 a b Fruit diameter mm 65.0 - 67.0 66.3 0.6 0.9 50.0 - 63.0 54.3 3.2 5.9 a b Color mature fruits Seeds Seeds per fruit # 78.0 - 84.0 80.1 1.6 2.0 74.0 - 117.0 97.9 13.4 13.7 a b Seed length mm 9.0 10.0 9.3 2.2 1.6 7.0 8.0 7.2 4.8 5.1 a b Aril Total soluble solids ˚Brix 13.5 - 14.3 14.0 0.2 1.8 14.8 - 16.8 15.4 0.5 3.2 a b Duncan's test (p≤0.05) fimbriated-purplish entire-white glabrous pubescent Passiflora gustaviana Passiflora popenovii one pair yellow mottled with irregular white dots yellow-orange purplish white 3-seriate purplish white and purplish-blue at apex purple green 4-seriate minute-filiform capillary glandless absent - (rarely with a scarlike gland near base) light-green reddish-purple glandular Species Elevation m.a.s.l. Distribution in the Biogeographic regions Observations P. ambigua Hemsl, 1902 10 – 1,500 Andean, Caribbean, Orinoquian, Pacific Edible fruit P. sp. nov. 1,800 – 1,880 Andean Endemic, D. Sánchez et al. 1378 and L. K. Escobar & F. J. Roldán 8662 (COL, CUVC, HUA, MEDEL) P. gleasonii Killip, 1924 130 – 172 Amazonian Unknown fruit, endemic P. guazumaefolia Juss., 1805 6 – 70 Caribbean, Orinoquian Edible fruit, synonymous P. theobromifolia DC. P. gustaviana Ocampo & Molinari, 2017 1,924 – 2,309 Andean Edible fruit, endemic P. killipiana Cuatr., 1960 216 Amazonian, Orinoquian Edible fruit, endemic P. laurifolia L., 1753 79 – 237 Amazonian, Orinoquian Edible fruit, synonymous P. tinifolia Juss. P. nitida HBK., 1817 0 – 826 Amazonia, Andean, Orinoquian, Pacific Edible fruit, synonymous P. nymphaeoides H. Karst. P. pergrandis Holm-Niels. & Lawesson, 1987 1,020 – 1,417 Andean Edible fruit P. popenovii Killip, 1938 1,500 – 1,900 Andean Edible fruit, cultivated in home gardens P. riparia Mart ex. Mast., 1872 180 – 300 Amazonian, Orinoquian Edible fruit P. tolimana Harms, 1894 250 – 1,800 Andean, Orinoquian Edible fruit, synonymous P. metae M. Bonilla, C. Aguirre & C. Caetano 26 507 508 FIG. 2. Plot of the scores obtained by P. gustaviana and P. popenovii accessions for the principal plane 509 quantitative variation components of the PCA. 510 27 511 FIG. 3. Passiflora gustaviana Ocampo & Molinari. Drawing of a mature plant. A. Stipules, young bud, tendril, 512 petiole, petiolar glands and leaf. B. Stipule. C. Flower, pendent. D. Longitudinal section of a flower. E. Fruit, 513 mature. F. Seed. Drawn by Jairo Larrahondo, of the type (Gustavo Morales 3190, JBB). 514 28 515 FIG. 4. Passiflora gustaviana Ocampo & Molinari. Photographs of a mature plant. A, stipules, young bud and 516 tendril. B, petiole and petiolar glands. C, mature leaf. D, terminal branch, E, frontal view of a flower. F, flower, 517 29 pendent. G, floral bracts. H, longitudinal section of a flower. I, fruit, immature. J, fruit, becoming mature. K, 518 fruit mature, cross section showing mesocarp and pulp. L, seeds. Photographs by John Ocampo and Gustavo 519 Morales, of the type (Gustavo Morales 3190, JBB). 520 521