Research Article
Print
Research Article
Distribution and conservation of vanilla crop wild relatives: the value of local community engagement for biodiversity research
expand article infoNicola S. Flanagan, Andres Navia-Samboni, Eimer Norberto González-Pérez§, Hernan Mendieta-Matallana§
‡ Pontificia Universidad Javeriana Seccional Cali, Cali, Colombia
§ Unaffiliated, Otanche, Colombia
Open Access

Abstract

Natural vanilla is a high-value crop with demand increasing globally. Crop wild relatives (CWR) represent valuable agrobiodiversity and are prioritized in the Global Strategy for Plant Conservation. Vanilla species are naturally rare with historically infrequent botanical collections. Despite their importance as CWR, fewer than 10% of Vanilla species have been evaluated for the IUCN Red List. Colombia is a diversity center for Vanilla species, yet many remote regions are lacking detailed floristic characterization. We show that the participation of rural communities in scientific endeavor enhances capacity to register biodiversity. We report two Vanilla species in the under-explored region of the Serranía de las Quinchas in the mid–Magdalena River valley in Colombia, including the first report for Colombia of Vanilla karen-christianae. For this, and the second species, Vanilla dressleri, we present descriptions with photographic botanical illustrations, updated distribution maps, and preliminary conservation status assessment. Both species are of elevated conservation concern, categorized as Endangered – EN: B2a,b(ii,iii,iv,v) following IUCN criteria. Within Colombia, all recorded occurrences for both species fall outside protected areas. Vanilla crop wild relatives in Colombia have urgent conservation needs. The Serranía de las Quinchas is a priority for further botanical exploration for Vanilla, as well as other protected areas with appropriate habitat. In situ conservation should be complemented with ex situ actions. Community participation in biodiversity research is recommended in this and other remote regions as an integral step towards enhancing biodiversity research and community-based conservation.

Keywords

citizen science, Colombia, community-based participatory research, natural rarity, Red List, Serranía de las Quinchas, Tumbes–Chocó–Magdalena biodiversity hotspot, Vanilla dressleri, Vanilla karen-christianae

Introduction

Crop wild relatives (CWR) are broadly defined as undomesticated plant taxa closely related to species of socio-economic value, including crops, medicinal plants, condiments, as well as ornamental and forestry species. CWR are widely recognized as vital resources for promoting global food security and sustainable rural livelihoods in the face of climate change (Hajjar and Hodgkin 2007; Dempewolf et al. 2014; Kersey et al. 2020; Ulian et al. 2020). As such, CWR are essential to achieve the Sustainable Development Goals 2 (Zero Hunger) and 12 (Sustainable consumption & production patterns) (UNDP 2022). Accordingly, CWR were prioritized for conservation action in the Aichi Biodiversity Target 13 (Convention on Biological Diversity, CBD 2020) and Target 9 of the Global Strategy for Plant Conservation (CBD 2011). This prioritization continues in the post-2020 Global Biodiversity Framework, to ensure the conservation and management of socio-economically important wild plants in situ and ex situ (CBD 2022).

Like all wild plant species, CWR are increasingly threatened by anthropogenic activities including unsustainable agro-environmental management, habitat transformation and climate change (Heywood et al. 2007; Maxted et al. 2010). As components of agrobiodiversity, conservation actions for CWR have mainly focused on genetic diversity collection and maintenance ex situ, primarily as a means of enhancing CWR availability for crop breeding. However, despite their importance, CWR diversity is still poorly represented in gene banks (Castañeda-Álvarez et al. 2016). In addition to ex situ conservation actions, the in situ conservation of these wild species must also be prioritized to ensure the maintenance of their evolutionary potential (Meilleur and Hodgkin 2004) as well as essential ecological interactions, including the symbiotic microbiome (Murphy et al. 2019). An important preliminary step for both in situ and ex situ conservation actions for CWR is to ensure a clear understanding of species taxonomy and distributions.

Natural vanilla is the second most economically valuable spice crop. With its high value, the vanilla crop has potential for promoting rural development across tropical and sub-tropical regions (Flanagan and Mosquera-Espinosa 2016; Havkin-Frenkel and Belanger 2018) yet is historically understudied. Phytosanitary problems have risen in parallel with the expansion of cultivation (e.g. Xiong et al. 2015; Havkin-Frenkel and Belanger 2018), and crop improvement programs are urgently needed. The wild relatives of the cultivated species Vanilla planifolia offer resources for diversifying the genetic base of natural vanilla cultivation (Maruenda et al. 2013; Flanagan et al. 2018; Nascimento et al. 2019; Pérez-Silva et al. 2021; da Silva Oliveira et al. 2022), however, more research is needed in the exploration of these crop wild relatives.

The genus Vanilla Plum. ex Mill. (Orchidaceae) has a pan-tropical distribution and includes approximately 120 hemiepiphytic to epiphytic species (Soto Arenas and Cribb 2010). The secondary gene pool of the crop (Vanilla subgenus Xanata Section Xanata Soto Arenas and Cribb 2010) comprises more than 40 species, naturally distributed within the neo-tropical region. While Vanilla species frequently have broad distributions (Soto Arenas and Cribb 2010; Soto Arenas and Dressler 2010; Karremans et al. 2020), they may often be locally very rare (e.g. Ferreira et al. 2017; Barona-Colmenares 2018; Engels et al. 2020). This natural rarity explains the scarce representation of Vanilla in biological collections and has historically been an obstacle to taxonomic studies in this genus. With a recent increase in attention to Vanilla taxonomy, several species have been described in the last decade, the majority with very restricted known distributions (Soto Arenas 2010; Soto Arenas and Dressler 2010; Koch et al. 2013; Molineros-Hurtado et al. 2014; Pansarin and Miranda 2016; de Fraga et al. 2017; Barona-Colmenares 2018; Karremans and Lehmann 2018).

Despite the conservation prioritization of crop wild relatives, only nine Vanilla species within the Section Xanata (11 in total for the genus) have been evaluated for the IUCN Red List of Threatened Species (IUCN, 2022). Of these nine, one, V. cribbiana is considered critically endangered, seven are classified as endangered, with one Data Deficient. The conservation status evaluation of all Vanilla species, and particularly those within the Section Xanata, as valuable crop wild relatives, is urgently required.

Colombia is at the center of distribution for the Section Xanata, yet to date no conservation status evaluations have been undertaken for Vanilla species in this country. Recent work has documented 26 Vanilla species for the country, of which 21 belong to the Section Xanata (Flanagan et al. 2018; Barona-Colmenares et al. 2019). Both historical herbaria data, and recent fieldwork indicate that these species distributions may be highly disjunct, more so due to habitat fragmentation in the last century. Nonetheless, many regions in Colombia are botanically underexplored (Arbeláez-Cortés 2013), and while our understanding of Vanilla species distributions is increasing, much more work is needed.

The Andean foothills of the Serranía de Las Quinchas cover 860 km2 of rugged terrain between 200 and 1,700 m. a. s. l. on the Western slope of the Eastern Cordillera of the Andes in Colombia, in the mid–Magdalena River valley. This region is at the eastern edge of the Tumbes–Chocó–Magdalena Biodiversity Hotspot (Mittermeier et al. 2011), which ranges from the mid–Magdalena River valley, across northwest Colombia, and down the pacific coast of Colombia and Ecuador to northern Peru. Although forest cover was once continuous to the Darién region to the northwest and into Central America, the natural ecosystems of the Magdalena River valley have been highly fragmented by expanding cattle ranches and palm oil plantations (Mayaux et al. 2005). The Serranía de las Quinchas is now one of the last remnants of humid tropical forest in the mid watershed of the Magdalena River valley (Etter et al. 2006).

The Serranía de las Quinchas has been recognized as an Important Bird Area, requiring focused habitat conservation strategies (Laverde Rodríguez et al. 2005). A floristic survey undertaken two decades ago registered significant diversity, with 1036 species belonging to 496 genera in 118 families (Balcázar-Vargas et al. 2000). Nonetheless, the region has been neglected in terms of biodiversity studies. Recently, however, several new orchid species have been described in neighbouring, higher altitude regions (Gutiérrez-Morales et al. 2018, 2021; Hágsater et al. 2018).

To ensure success, conservation research and management approaches must effectively engage local communities, as well as ensuring their livelihood needs are adequately met (Bajracharya et al. 2006; Lentijo et al. 2008). Citizen science, defined as the engagement of non-professionals in authentic scientific research (Dickinson et al. 2012), combines robust capacity-building experiences with enhanced power to further scientific research objectives. In Colombia, a mega biodiverse country, a study in coffee growing areas in the Andes found that farmers believed that a lack of environmental awareness and lack of knowledge were the main barriers to practices to promote bird conservation (Lentijo and Hostetler 2013). Community-based participatory research strategies facilitate the construction of knowledge systems that integrate both scientific and empirical perspectives. Such an inclusive approach with indigenous people & local communities (IPLC) promotes dialogue and knowledge exchange and has a key role in local biodiversity research and management strategies, by strengthening effective ties with biodiversity, and promoting awareness among local communities and thereby actions in favour of the conservation and sustainable use of biodiversity (Soacha-Godoy and Gómez 2016; IPBES 2019).

Through participatory research practice involving local community members (ENG-P and HM-M) in the Municipality of Otanche, Boyacá, Colombia and scientists (NSF and AN-S), we here report two Vanilla species in the Serranía de las Quinchas, including the first report in Colombia of the species Vanilla karen-christianae Karremans and P.Lehm., 2018 (Orchidaceae, Vanilloideae). With these new reports we provide updated distributions, contribute additional details to the species descriptions and provide the first evaluations of conservation status following IUCN criteria for these species. We also provide recommendations for conservation of these species at the national level in Colombia.

Methods

Study site and specimens

The vanilla plants were found in the Municipality of Otanche, Department of Boyacá, Colombia. The locality falls within the buffer zone of the Regional Forest Reserve Las Quinchas. Sub-Andean tropical life zones are present under 1,000 m elevation, where pastures and agricultural areas form a mosaic with small relicts of tropical humid forest. The average temperature is 24–26 °C, with average annual precipitation of 2500–3000 mm (IDEAM 2022).

The local community members (ENG-P and HM-M) discovered Vanilla vines during routine activities on their agricultural smallholdings in the villages of Altazor and San José de Nazareth, and made contact with researchers through the online platform https://www.inaturalist.org.

The plants of Vanilla dressleri were monitored by ENG-P until flowering. At the time of detection, the V. karen-christianae individual had several inflorescences. Flowers were collected, dissected, and photographed in the field, and plant morphological measurements taken from live material. Composite photographic plates were prepared using Adobe Photoshop v. 21.0.3, with light and brightness correction in Adobe Photoshop Lightroom Classic v. 9.0 (Adobe Systems Incorporated). Floral parts were measured using the program ImageJ bundled with Java 1.8.0_172 (Schneider et al. 2012). Species identification was achieved following Soto Arenas and Cribb (2010), Soto Arenas and Dressler (2010) and Karremans and Lehmann (2018).

Species distributions

We compiled a dataset of all occurrence records for both Vanilla karen-christianae and V. dressleri from sources including Soto Arenas and Dressler (2010), Karremans et al. (2020), Karremans and Lehmann (2018), Rojas-Álvarez (2020), Rodríguez-Salamanca (2020), Navia-Samboni (2021) and the new records from this study. In addition, online databases and herbaria were searched, including GBIF (https://www.gbif.org), TROPICOS (https://www.tropicos.org), SiB (https://sibcolombia.net) and iNaturalist (https://www.inaturalist.org). Based on the records found, three maps were constructed in ArcGIS Pro 2.8.0 (https://www.esri.com/): the global distribution of Vanilla karen-christianae and of Vanilla dressleri, and the distribution of both species in Colombia. Distinct shape files were used for each country, including layers for elevation, political boundaries, and rivers (https://www.diva-gis.org), protected areas (https://www.protectedplanet.net), the Tumbes–Chocó–Magdalena hotspot and presence of humid tropical forest (https://globalforestwatch.org) [All websites accessed April–July 2021], with the application of a final layer with the coordinates of the occurrences for the species studied (Tables 1 and 2).

Table 1.

Global records of Vanilla karen-christianae. Herbariums: MO (Missouri Botanical Garden); SEL (Marie Selby Botanical Gardens); USM (Herbarium Hattiesburg, The University of Southern Mississippi); JBL-Spirit (Jardín Botánico Lankester, Universidad de Costa Rica); MOL (Herbarium Weberbauer, Universidad Nacional Agraria La Molina); CEN (Embrapa Recursos Genéticos e Biotecnologia); MG (Museu Paraense Emílio Goeldi); N/A - Not Available.

Record No. Coordinates (Latitude, Longitude) Country State or Province Locality Elevation (m.a.s.l) Collector Record Year Records herbarium Source
1 13.700027, -84.573888 Nicaragua Matagalpa Cerro Kana Coperna 250 D. Neill 1978 MO 457 TROPICOS, GBIF, Karremans et al. (2020)
2 13.65, -84.808333 Nicaragua Matagalpa Cerro Waylawás 100–270 W. Stevens 1978 MO 7385 TROPICOS, GBIF
3 13.058, -85.72 Nicaragua Matagalpa La Dalia, Cerro Waylawás 250 D. Neill 1978 SEL - MO 4219 GBIF, Karremans et al. (2020)
4 12.740750, -85.437972 Nicaragua Matagalpa Siuna, Río Matis <100 F. Ortiz 1982 MO 172 Karremans et al. (2020)
5 11.006339, -84.962492 Nicaragua Río San Juan Refugio los Guatuzos 30 E. van den Berghe 2021 Photograph by van den Berghe iNaturalist
6 10.130094, -83.604406 Costa Rica Limón Siquirres, Germania 250 A. Karremans 2020 JBL Spirit 8356 Karremans et al. (2020)
7 8.538000, -82.850528 Costa Rica Puntarenas Corredores, Canoas 130 A. Karremans 2017 JBL Spirit 8123 GBIF, Karremans et al. (2020)
8 8.577222, -82.873056 Costa Rica Puntarenas Corredores, Canoas 130 A. Karremans et al. 2017 USJ - JBL Spirit - MO 8087 GBIF, Karremans et al. (2020)
9 5.8090, -74.1139 Colombia Boyacá San José de Nazareth, Otanche 770 This study 2020 Fig. 1; This study This study
10 -1.578667, -55.685250 Brasil Pará Río Branco de Óbidos N/A A. Goeldi 1927 N/A TROPICOS
11 -7.340667, -66.415722 Brasil Amazonas Río Purús N/A J. Huber 1904 MG-007302 s.n. TROPICOS
12 -9.416028, -64.698972 Brasil Rondonia Cachoeira de Jirau 90 G. Pereira-Silva et al. 2010 CEN-00078538 15128 TROPICOS
13 -6.454639, -76.656917 Peru San Martín N/A 400 R. Ferreyra, Rauh and Bismarck 1973 USM 18265 Karremans et al. (2020)
14 -6.951028, -76.350222 Peru San Martín Puerto Rico 200 A. Damián and M. León 2018 USM 906 Karremans et al. (2020)
15 -9.131972, -74.496500 Peru Ucayali Reserva Comunal el Sira 180 J. Janovec, J. Ushinawa and H. Behar 2015 MOL 4006, 4009 Karremans et al. (2020)
16 -10.838556, -75.289750 Peru Junín Puente Paucartambo 200 D. Aliaga 2018 USM s.n. Karremans et al. (2020)
17 -11.102, -75.349917 Peru Junín Chanchamayo Fundo la Genova 1100 A. Damián and Botanic’s students UCSUR 2016 USM 905 Karremans et al. (2020)
18 -12.256611, -70.898 Peru Madre de Dios Boca Manú 280–320 J. Householder, A. Balarezo and J. Huinga N/A USM 941 Karremans et al. (2020)
19 -12.599306, -69.052944 Peru Madre de Dios Sandoval, Lago Sandoval 150 N/A N/A No Voucher GBIF
20 -12.695000, -69.469306 Peru Madre de Dios Comunidad Mercedes 200–250 J. Householder, A. Balarezo and J. Huinga 2007 USM 14 Karremans et al. (2020)
21 -12.487097, -68.95488 Peru Madre de Dios Concesión Inkaterra 180 M.A. Rodríguez-Salamanca 2020 Photograph by Rodriguez-Salamanca Rodríguez-Salamanca (2020)
22 -12.479953, -68.954190 Peru Madre de Dios Concesión Inkaterra 150 M.A. Rodríguez-Salamanca 2020 Photograph by Rodriguez-Salamanca Rodríguez-Salamanca (2020)
Table 2.

Global records of Vanilla dressleri. Herbariums: MO (Missouri Botanical Garden); INBio (Herbario del Insituto Nacional de Biodiversidad de Costa Rica); CUVC (Herbario Luis Sigifredo Espinal Tascón, Universidad del Valle); QCNE (Museo Ecuatoriano de Ciencias Naturales); N/A - Not Available.

Record No. Coordinates (Latitude, Longitude) Country State or Province Locality Elevation (m.a.s.l.) Collector Record Year Records for herbarium Source
1 10.978611, -85.11 Costa Rica Alajuela San José de Upala 40 Gerardo Herrera 1988 MO 1840 TROPICOS, GBIF
2 10.333333, -84.716666 Costa Rica Alajuela Reserva Monteverde 820 William Haber and Eladio Cruz 1987 INBio - MO 7243 TROPICOS, GBIF
3 10.316666, -84.716666 Costa Rica Alajuela Reserva Monteverde 900 William Haber and Eladio Cruz 1988 INBio - MO 8471 TROPICOS, GBIF
4 9.8, -83.7 Costa Rica Cartago Jiménez 700 Ronald Liesner 1983 MO 14435 TROPICOS, GBIF
5 9.446388, -83.987222 Costa Rica Puntarenas Rafiki Safari, Aguirre 250 Joaquín Sánchez González 2002 MO 1219 TROPICOS, GBIF
6 9.67, -83.02 Costa Rica Limón Reserva Hitoy Cerere 400 Gerardo Carballo 1990 INBio - MO 325 TROPICOS, GBIF
7 8.671611, -83.567666 Costa Rica Puntarenas Rancho Quemado 100 N/A 1990 No Voucher GBIF
8 8.7666666, -83.25 Costa Rica Puntarenas Parque Natural Piedras Blancas 100 Marianela Segura 1993 MO 121 TROPICOS, GBIF
9 9.201666, -79.84444 Panama Canal Área Península Bohío 40 Sandi Knapp and Jim Mallet 1982 MO 4621 TROPICOS, GBIF
10 9.4, -79.65 Panama Colón Parque Natural Chagres 550 Gordon McPherson 1986 MO 9196 TROPICOS, GBIF
11 6.333333, -77.333333 Colombia Chocó Playa Huaca, Bahía Solano 100 Felipe García-Cossio, and Enzo Agualimpia 1990 MO 325 TROPICOS, GBIF, SiB
12 6.177694, -77.387944 Colombia Chocó El Cedro, Bahía Solano 40 Nicola Flanagan and Andres Navia-Samboni 2020 Photograph by N. Flanagan Navia-Samboni (2021)
13 6.182697, -77.393739 Colombia Chocó El Cedro, Bahía Solano 40 Camilo Rojas Álvarez 2020 No Voucher Rojas-Álvarez (2020)
14 6.161027, -77.371222 Colombia Chocó El Cedro, Bahía Solano 100 Sean Higgins 2017 Photograph by S. Higgins iNaturalist, GBIF
15 6.150000, -77.350897 Colombia Chocó Río Valle, Bahía Solano 20 Camilo Rojas Álvarez 2020 No Voucher Rojas-Álvarez (2020)
16 6.078699, -77.330135 Colombia Chocó El Cedro, Bahía Solano 50 Camilo Rojas Álvarez 2020 No Voucher Rojas-Álvarez (2020)
17 6.033333, -75.133333 Colombia Antioquia La Piñuela, Cocorná 830 Diego Giraldo Cañas 1993 HUA - MO 1731 GBIF
18 5.8247, -74.1303 Colombia Boyacá Altazor, Otanche 400–950 This study 2020 Fig. 2; This study. This study
19 4.071277, -77.087861 Colombia Valle del Cauca La Trojita, Río Calima 30 José Cuatrecasas 1944 CUVC - MO 16650 TROPICOS, GBIF, Soto Arenas and Dressler (2010)
20 3.630916, -76.928166 Colombia Valle del Cauca Anchicaya 270 José Cuatrecasas 1943 No Voucher GBIF, Soto Arenas and Dressler (2010)
21 0.933333, -78.6 Ecuador Esmeraldas Alto Tambo 250 Daniel Rubio, Carlos Quelal and Cleto Pai 1991 QCNE - MO 1131 TROPICOS, GBIF

Conservation status

We evaluated the conservation risk status of Vanilla karen-christianae and V. dressleri according to the IUCN Guidelines for Using the IUCN Red List Categories and Criteria version 15 (IUCN Standards and Petitions Committee 2022). The Extent of Occurrence (EOO) and Area of Occupancy (AOO) of each species were calculated with GeoCAT (http://geocat.kew.org). The EOO value obtained is a clear overestimation, as the polygon includes marine areas as well as habitats at higher elevation, where these species do not occur. To approach a more precise value for EOO, the terrestrial areas below 1500 m.a.s.l. within the minimal convex polygon were calculated in ArcGIS Pro, version 2.8.0 (https://www.esri.com/). Nonetheless, this value still does not consider the contemporary prevalence of suitable humid tropical forest habitat, and so the area of humid tropical forest remaining within the polygon was also calculated.

Results

We report the first record of the species Vanilla karen-christianae Karremans & P.Lehm. (Figs 1, 3A) in Colombia, as well as a new report for V. dressleri Soto Arenas (Figs 2, 3B), both in the Serranía de las Quinchas, Department of Boyacá, Colombia.

Figure 1. 

Vanilla karen-christianae from the Serranía de las Quinchas, Boyacá, Colombia. A. Habit B and C. Two separate flowers viewed from different perspectives D. Dissected perianth E. Lip and ovary lateral view F. surface of the central lobe of the labellum showing abundant trichomes G. Longitudinal dissection of the labellum, with the apex to the right, showing the retrorse position and form of the penicillate callus H. Individual combs of the penicillate callus I. Column, ventral and lateral view J. Fruit K. Anther cap and pollinia.

Figure 2. 

Vanilla dressleri from the Serranía de las Quinchas, Boyacá, Colombia. A. Habit B and C. Two separate flowers viewed from different perspectives D. Dissected perianth E. Penicillate callus F. Lip and ovary lateral and dorsal view G. Flower bract H. Column, ventral and lateral view I. Anther cap.

Figure 3. 

New records for Vanilla spp. from the Serranía de las Quinchas, Boyacá, Colombia A. Inflorescence of V. karen-christianae with flower and developing fruit B. Inflorescence of V. dressleri with buds C. View of rugged terrain where both species are found in secondary forest between plots opened for cacao cultivation on smallholder properties D. Community member (ENG-P) undertaking monitoring of V. dressleri.

Vanilla karen-christianae Karremans & P.Lehm. Orchids (West Palm Beach) 87(4): 305 (2018)

Type. Costa Rica. Puntarenas: Corredores. Canoas, 27 Sept. 2017, A.P. Karremans et al. 8087 (holotype: USJ; isotypes: JBL-spirit, CR).

New record. Vanilla karen-christianae Colombia. Boyacá Department, Municipality of Otanche; coordinates: 5.8090, -74.1139; 400 m.a.s.l.; 11 Oct. 2020; NS Flanagan et al. (Figs 1, 3A).

Hemiepiphytic, scandent vine, up to 20 m long. Stems flexuous, sulcate, ca. 4–10 mm thick; internodes, 6.5–16.5 cm long. Aerial roots attaching, flattened 1.0–3.7 mm wide. Leaves alternate, coriaceous, petiolate, the petiole canaliculate, 5.5–11.0 mm long, ca. 3 mm wide; blade linear to sub-lanceolate, acuminate, conspicuously recurved at apex, 11–17.5 × 1.8–3.5 cm. Inflorescence 1–8 per plant, axillar, up to +30 flowers per raceme; rachis ca. 9 cm long, congested. Floral bracts sheathing, ovate, concave ca. 5–6 mm long. Flowers successively 1 to 2 days apart, one open at a time, ephemeral, segments not spreading, ovary basal half white, apical half green, sepals and petals light green, shiny, lip white to cream with the side veins and appendages cream to pale yellow, penicillate callus white, column white and appendages cream to pale yellow. Ovary subterete, smooth, arcuate, 30–35 mm long, 3–4 mm thick. Dorsal sepal oblanceolate, apex acute 41–55 × 10–14 mm. Lateral sepals broadly oblanceolate, apex acute, 46–55 × 14–19 mm. Petals obliquely linear to lanceolate, apex acute, with a conspicuous, elevated, longitudinal keel on abaxial surface; 42–51 × 7–14 mm. Lip fused to the column along the margins for ca. 2.5 cm, tubular, concave, inflated near the middle, becoming deeply saccate; axially grooved on the abaxial surface; the apex deeply emarginate, with or without a recurved tip; when spread out 48–50 × 41–47mm; conspicuously trilobed; central lobe cuadrate, bilobed, margins crenulate, strongly undulate, ca. 16–veined, the veins thickened forming low, papillose keels, trichomes taller towards the apex, 20–27 × 15–18 mm; lateral lobes subrhombic, obtuse, margins entire, sub-undulate; penicillate callus retrorse, 30–35 mm from the base, 9–10 obdeltate to cuadrate, scales with sinuate distal edge, progressively smaller from apex 4–7 × 2–5 mm. Column subterete, ventrally flattened, 25–30 × 4–6mm; densely pilose on apical ¾ of ventral surface, with trichomes of increasing length apically. Stigma trilobed, lateral lobes erect, oblong, margin subcrenate, rostellum, transversely oblong 4.5 × 2.5 mm. Anther versatile, 3.4 × 4.8mm. Pollen 2 cuadrate, bilobed granular masses. Fruit sub–trigonous 6.5× 1.6 cm immature, lightly fragrant.

Vanilla karen-christianae can be distinguished from other species present in Colombia with similar narrow leaves, V. odorata and V. phaeantha. Leaves of V. odorata are more petiolate, while those of the latter are equally or more sessile, and more linear-oblong. Both lack the recurved apex on the leaf. In the flower, the lip of V. karen-christianae is strikingly adorned, compared to both similar species: V. odorata has an entire lip, with a minimally papillose surface; V. phaeantha has a less congested rachis, a somewhat trilobed lip, conspicuously unguiculate, with only two rows of trichomes. This record of V. karen-christianae differs from the type description in having larger dimensions in the flower, with less intense coloration. Notably, the lip of this new record is conspicuously trilobed, compared with obscurely trilobed in the type specimen. The penicillate callus comprises 9 or 10 scales.

A single plant of Vanilla karen-christianae was found on the agricultural smallholding, La Esperanza, belonging to Hernan Mendieta-Matallana in the village of San José de Nazareth. The vines of this plant cover an area of approximately 20 m2 either side of a footpath. This site presents disturbed secondary forest cover. The specimen had several inflorescences on discovery, and subsequent monitoring revealed that flowering occurs during the months of August and October.

Vanilla karen-christianae, described in 2018 (Karremans and Lehmann 2018), has a total of 22 occurrence records globally from 19 localities, with an altitude distribution between 30 and 1100 m.a.s.l. This species has a highly disjunct distribution, with occurrences in Central America, from northern Nicaragua, through Costa Rica and Panama, as well as across the Amazon basin from Madre de Diós, Peru to Pará, Brazil (Table 1; Fig. 4A). Our new report for this species in Colombia provides a connection between these disjunct distributions in Mesoamerica and the Amazon basin.

Figure 4. 

Maps showing A global distribution of Vanilla karen-christianae B global distribution of Vanilla dressleri C distributions of V. karen-christianae and V. dressleri in Colombia with respect to Protected areas (A–J) covering humid tropical forest.

The total Extent of Occurrence (EOO) for this species calculated with GeoCAT was 4,447,442 km2. When only terrestrial areas below 1,500 m.a.s.l. were considered, this was reduced to 3,488,798 km2. Within this area 2,484,296 km2 corresponds to humid tropical forest, of which 421,222 km2 occurs in Colombia. The Area of Occupancy (AOO) calculated for this species is 88 km2.

Vanilla dressleri Soto Arenas. Lankesteriana 9: 303–305 (2010)

Type. Panama, Colón: End of Pipeline Road, Gamboa, 15 April 1982, S. Knapp 4621 & J. Mallet (holotype: MO 3032952).

New record. Vanilla dressleri Colombia. Boyacá Department, Municipality of Otanche; Vereda Altazor. Coordinates: 5.8247, -74.1303; 770 m a.s.l.; 11 Oct. 2020; NS Flanagan et al. (Figs 2, 3B).

Hemiepiphyte, scandent vine, poorly branching, up to 20 m long. Stems flexuous, terete, 4.0–6.4 mm thick; internodes 3.0–16.5 cm long. Aerial roots attaching, flattened 0.6–2.8 mm thick. Leaves alternate, petiolate, the petiole canaliculate, 7–18 mm long, ca. 4 mm wide; blade entire, variable lanceolate to ovate–elliptic, shortly acuminate–cuspidate, with a conspicuous central axial canal on adaxial surface, fleshy, pendant to spreading, commonly larger than the internodes 11.5–18.3 × 3.7–5.5 cm. Inflorescence ca. 12 per plant, axillar, racemose, a 3–13 flowered raceme, lax, bracts distant up to 20 mm, rachis up to 75 mm long. Floral bracts sheathing to spreading, obtusely deltate-ovate, concave, 7–8 × 13–19 mm; Flowers open successively 3 to 6 days apart, 1 to 3 open at a time, ephemeral, big and showy, tepals pendant to spreading, cream to greenish–yellow on outer surface, lip orange yellow on basal 2/3 of the inner surface, fading to white towards the apex, orange color more intense on the elevated veins, column white basally, with yellow apex; fragrance principally on sepals also petals, mentholate. Ovary subterete, greenish–white, straight to curved, thickened towards the base, 35–37 mm long, 4–5 mm thick; calyculate. Dorsal sepal narrowly elliptic, apex broadly acute, subcalyptrate, base canaliculate, 67–79 × 13–14 mm. Lateral sepals narrowly elliptic, apex broadly acute–rounded, calyptrate, base canaliculate, 69–75 × 11–13 mm. Petals narrowly elliptic, apex broadly acute–rounded, calyptrate, basally canaliculate, with a conspicuous elevated, longitudinal keel on abaxial surface; 69–75 × 11–15 mm. Lip attached to the column along the margins of the basal two thirds (ca. 25 mm), tubular, concave, axially grooved on the abaxial surface; when spread out 66–69 × 47–49 mm; blade subrhombic, margin entire, apex obtuse–rounded, very slightly notched, ca. 25–veined; central 3 veins in an elevated section from callus to apex, slightly warty at apex; penicillate callus retrorse, at ca. 30 mm from the lip base, made up by ca. 4–6, obdeltate, fimbriate scales, 4–6.5 × 2–3.5 mm. Column, subterete, ca. 36–38 × 3.5–4.0 mm; densely pilose with short trichomes on mid 1/3 of the ventral surface, trichomes changing in colour from white basally to dark orange and ending abruptly, glabrous for 6 mm below the stigma. Stigma lateral lobes erect, obtusely deltate, lower apex acute, ca. 1.5 × 3 mm.subrhombic; rostellum, narrow, cuadrate, sharply convex 2 × 2.4 mm. Anther, versatile, oval, obtuse 3 × 3 mm. Fruits subterete at base to subtrigonous at apex, 12–15 × 1–2 cm (3 months after pollination).

Vanilla dressleri can be distinguished from similar species, including the partially sympatric V. cribbiana and V. rivasii, as well as V. ruiziana and V. weberbaueriana known from the Amazon (Damián and Janovec 2018), by the lax inflorescence with patent bracts, and an entire lip with subrhombic blade. This record differs in morphological traits from the type description of V. dressleri in the following ways: it has a laxer inflorescence, with a longer rachis and more separated bracts; the lip coloring is less intense, lacking the prominent brownish colored veins of the type specimen; notably, the lip has an entire margin compared to the undulate, pleated margin described in the type specimen.

In total, fifteen different plants of Vanilla dressleri were found by ENG-P over an area of approximately 8 km2 of secondary forest between plots opened for cacao cultivation on smallholder properties in Altazor (Fig. 3C). In this rugged terrain the plants ranged over elevations of between 400 and 950 m.a.s.l. Flowering occurs principally in March to April, with a less productive event in July, with only 1–4 inflorescences per plant.

Vanilla dressleri was first described for science in 2010 (Soto Arenas and Dressler 2010) and has only 21 records in 17 known occurrence localities. These are distributed from northern Costa Rica through Panama, and southwards through the Chocó biogeographic region on the Colombian and Ecuadorian pacific coast. Altitude distribution ranges between 20 and 950 m.a.s.l.. In Colombia, the species is known from the Chocó biogeographic region on the Pacific littoral. A single record from 1993 is located in the foothills of the Central Cordillera, to the west of the Magdalena River (Table 2; Fig. 4B).

The total Extent of Occurrence (EOO) calculated from GeoCAT for this species was 539,730 km2. When only terrestrial areas below 1,500 m.a.s.l. were considered, this was reduced to 186,235 km2. Of this area, 111,693 km2 corresponds to humid tropical forest, with only 52,414 km2 present in Colombia. The Area of Occupancy (AOO) for this species with such a small number of localities is 80 km2.

IUCN Red List evaluation

In the countries in which these two species occur, average forest cover loss averaged 10% over the 25 years from 1990 to 2015 (Keenan et al. 2015). In Colombia, more than 50% of the remnant area of humid tropical forest in the Magdalena River watershed is at risk of deforestation (Etter et al. 2006), and the Mid-Magdalena region is considered a deforestation hotspot (Sanchez-Cuervo and Aide 2013). In the Chocó biogeographic region, areas of humid tropical forest are still relatively intact with 68% forest cover remaining, however deforestation due to illicit crops and alluvial mining has increased in recent years (Anaya et al. 2020).

Given the low current AOO and past and projected future decline in habitat, under the IUCN criterion B, Geographic range, both Vanilla karen-christianae and V. dressleri would be categorized as Endangered–EN: B2a,b(ii,iii,iv,v), with an AOO of less than 500 km2, a severely fragmented population, and continuing decline inferred and projected in (ii) area of occupancy; (iii) area, extent and/or quality of habitat; (iv) number of locations or subpopulations; (v) number of mature individuals.

Discussion

Species of the genus Vanilla (Orchidaceae) represent the crop wild relatives of natural vanilla and are a global priority for conservation actions (Flanagan et al. 2018). Nonetheless, their natural rarity in the wild, together with their infrequent flowering, has hindered the necessary taxonomic and species distribution studies for this economically important genus. Research approaches that encourage local community participation offer an important means to enhance capacity to further scientific research and conservation objectives in biodiverse countries and regions (Dickinson et al 2012; IPBES 2019). In a participatory scientific endeavour with local community members (Fig. 3D), we report the occurrence of two recently described species of Vanilla in the under-explored region of the Serranía de las Quinchas, Department of Boyacá, Colombia. These reports represent an important contribution to our understanding of Vanilla species distributions, strengthening the evidence base to develop species conservation and management strategies.

Our findings represent the first report of Vanilla karen-christianae Karremans & P.Lehm. for Colombia, illuminating the trans–Andean connection between the previously known disjunct distributions of this species in Mesoamerica, and the Amazon basin. Recently, Chiron et al. (2021) proposed the synonymy of V. karen-christianae with V. ensifolia Rolfe (1892). The latter was described from imperfect material collected in the Andean region of Colombia (Cauca and Patia). In the characters for which data is available for V. ensifolia, our material clearly differs from the taxonomic description of V. ensifolia in the deeply emarginate, conspicuously trilobed lip compared with the entire, rounded lip described for V. ensifolia. Currently (2022-07-21), the World Checklist of Selected Plant Families (WCSP - https://wcsp.science.kew.org/), follows the consensus in the literature and considers the name Vanilla ensifolia to be a synonym of V. odorata.

The species Vanilla dressleri Soto Arenas was previously recorded in Mesoamerica and the Chocó biogeographic region on the Colombian and Ecuadorian pacific coast. This is the first report for this species to the east of the Magdalena River, thereby extending the species range within the Andean region. The distribution for V. dressleri encompasses both the Tumbes–Chocó–Magdalena and the Mesoamerican biodiversity hotspots (Mittermeier et al. 2011).

Both species pertain to Vanilla subgenus Xanata Section Xanata Soto Arenas and Cribb 2010, and these reports bring the total number of Vanilla species in Colombia to 27, with 22 in the Section Xanata. This clade represents the secondary gene pool of the vanilla crop, and these new occurrences further highlight the importance of Colombia as a centre of diversity for vanilla crop wild relatives (Flanagan et al. 2018; Barona-Colmenares et al. 2019).

Despite relatively wide distributions, both Vanilla karen-christianae and V. dressleri, like many species in the genus, are naturally rare. These recently described species each have fewer than 25 occurrence reports in widely separated localities over their total distributions, with resulting Areas of Occupancy (AOO) of less than 100 km2. The once continuous lowland humid forest cover from Central America through the Darién region and into northern South America is now severely fragmented, and decline continues in both the extent and quality of habitat (Mayaux et al. 2005; Sanchéz-Cuervo and Aide 2013; Keenan et al. 2015). Our preliminary conservation status evaluation following IUCN criteria indicates both species can be considered Endangered–EN, based on IUCN category B2a,b(ii,iii,iv,v).

Of the 11 Vanilla species within the Section Xanata now evaluated under the IUCN Red List criteria (IUCN 2022), ten are considered threatened, and one data deficient. This underlines the urgent need for conservation actions for these economically important wild plants at the international and national levels, in accordance with global policy (CBD 2022).

While IUCN Red List species conservation assessments are preferentially undertaken at a global level, conservation management plans are more commonly developed and implemented at a national or even regional scale. Despite vanilla crop wild relatives being a national conservation priority, no Vanilla species is listed as a conservation concern in Colombia (Ministerio de Ambiente y Desarrollo Sostenible and Universidad Nacional de Colombia 2015). Although neither species is endemic to the country, Vanilla karen-christianae is known from a single locality and V. dressleri from only six localities in the country. Data available for population size reveal a small number of individuals, with no evident recruitment of juvenile individuals. These observations would suggest that for the national Red List evaluation, both species would be categorized as Critically Endangered – CR based on IUCN Criterion C (Population size): C2a (i,ii), with fewer than 250 mature individuals in total registered, fewer than 50 (more than 90%) mature individuals in each subpopulation.

For conservation in situ it is essential that populations of Vanilla species are present within protected areas. All recorded occurrences for both Vanilla dressleri and V. karen-christianae fall outside Colombian protected areas (Fig. 4C). The distributions of both species correspond to the biomes of ´tropical humid zonobiome of the Magdalena River and Caribbean region´ and ´tropical humid zonobiome of the Pacific and Atrato´, which have only 5.8% and 2.7% protected area respectively (Forero-Medina and Joppa 2010).

Further botanical exploration for Vanilla species is strongly recommended within protected areas covering the humid tropical forest biome. Those protected areas of highest priority for Vanilla exploration include the National Nature Parks PNN Los Katios, in the Darién region, and PNN Paramillo in the central Andean cordillera. At the regional level, within the departments of Boyacá and Santander further exploration is needed with the Regional Forest Reserve Las Quinchas, as well as the Cuchilla de San Antonio, and the Regional Districts for Integrated Management of the Serranía de los Yariguies and Del Rio Minero y sus Zonas Aledañas (see Fig. 4C). Additionally, for Vanilla dressleri, we recommend further exploration along the Pacific coastal region, in the PNN Utría in the Chocó department and in the regional protected areas around Buenaventura in the Valle del Cauca department, including the National Forest Reserve of Río Anchicaya, and the Regional Nature Park La Sierpe.

Given the small size of these Vanilla populations, and the ease of vegetative propagation of these plants we also recommend the implementation of programs of population augmentation in existing occurrence localities, together with managed introduction into neighboring protected areas. The introduction of material from known populations into ex situ conservation germplasm banks is a priority, in order to complement in situ conservation, and also permit further bioprospecting of these valuable crop wild relatives (Flanagan et al. 2018). Currently, only three Vanilla species are contained in ex situ collections in Colombia – Vanilla calyculata, V. planifolia and V. pompona (Ministerio de Ambiente y Desarrollo Sostenible and Universidad Nacional de Colombia 2015).

In addition to conventional in situ and ex situ conservation approaches, the promotion of participatory, community-based circa situm conservation strategies is also recommended. Circa situm conservation refers to those actions carried out within the native geographical range of a species but outside natural habitats (Dawson et al. 2013). In the case of vanilla, such actions may include the establishment of community germplasm banks, as well as cultivation in agroforestry systems or home gardens (Flanagan and Mosquera-Espinosa 2016). Circa situm conservation of Vanilla aligns directly with international policy which recognizes that the active participation of indigenous people and local communities (IPLC) as essential for effective conservation, restoration, and sustainable use of orchid biodiversity, while simultaneously offering avenues for improving local livelihoods and wellbeing (IPBES 2019).

References

  • Anaya JA, Gutiérrez-Vélez VH, Pacheco-Pascagaza AM, Palomino-Ángel S, Han N, Balzter H (2020) Drivers of forest loss in a megadiverse hotspot on the pacific Coast of Colombia. Remote Sensing 12(8): e1235. https://doi.org/10.3390/rs12081235
  • Bajracharya SB, Furley PA, Newton AC (2006) Impacts of community-based conservation on local communities in the Annapurna Conservation Area, Nepal. Biodiversity and Conservation 15(8): 2765–2786. https://doi.org/10.1007/s10531-005-1343-x
  • Balcázar-Vargas MP, Rangel-Churio JO, Linares-Castillo EL (2000) Diversidad florística de la Serranía de Las Quinchas, Magdalena medio (Colombia). Caldasia 22(2): 191–224.
  • Barona-Colmenares AA (2018) Two new records in Orchidaceae (Vanillinae) from southernmost Colombian Amazonia: Vanilla javieri, a new species, and Vanilla appendiculata. Phytotaxa 375(4): 261–273. https://doi.org/10.11646/phytotaxa.375.4.2
  • Barona-Colmenares AA, Rodríguez-Castañeda M, Castaño-Arboleda N, Sua-Tunjano S, Cárdenas-López D (2019) The genus Vanilla (Orchidaceae) in the Colombian Amazonia: preliminary results. In: Pridgeon AM, Arosemena-RA (Eds) Proceedings of the 22nd World Orchid Conference, Guayaquil (Ecuador). Asociación Ecuatoriana de Orquideologia, Guayaquil, 167–178.
  • Castañeda-Álvarez NP, Khoury CK, Achicanoy HA, Bernau V, Dempewolf H, Eastwood RJ, Guarino L, Harker RH, Jarvis A, Maxted N, Müller JV, Ramírez-Villegas J, Sosa CC, Struik PC, Vincent H, Toll J (2016) Global conservation priorities for crop wild relatives. Nature Plants 2(4): 1–6. https://doi.org/10.1038/nplants.2016.22
  • Chiron GR, Sambin A, Krahl AH (2021) Taxonomic notes on Vanilla odorata, Vanilla fimbriata and related species (Orchidaceae). Richardiana 5: 76–115.
  • Convention on Biological Diversity (2011) Global Strategy for Plant Conservation – Targets 2011–2020. https://www.cbd.int/sp/targets/ [Accessed on 17.04.2022]
  • Damián A, Janovec JP (2018) El género Vanilla en el Perú. Universidad Científica del Sur, Lima, Perú, 165 pp.
  • Dawson IK, Guariguata MR, Loo J, Weber JC, Lengkeek A, Bush D, Cornelius J, Guarino L, Kindt R, Orwa C, Russell J, Jamnadass R (2013) What is the relevance of smallholders’ agroforestry systems for conserving tropical tree species and genetic diversity in circa situm, in situ and ex situ settings? A review. Biodiversity and Conservation 22(2): 301–324. https://doi.org/10.1007/s10531-012-0429-5
  • Dempewolf H, Eastwood RJ, Guarino L, Khoury CK, Müller JV, Toll J (2014) Adapting agriculture to climate change: A global initiative to collect, conserve, and use crop wild relatives. Agroecology Sustainable Food 38(4): 369–377. https://doi.org/10.1080/21683565.2013.870629
  • Dickinson JL, Shirk J, Bonter D, Bonney R, Crain RL, Martin J, Phillips T, Purcell K (2012) The current state of citizen science as a tool for ecological research and public engagement. Frontiers in Ecology and the Environment 10(6): 291–297. https://doi.org/10.1890/110236
  • Engels ME, Dias DC, Koch AK (2020) Increased morphological variation and a new record of Vanilla labellopapillata (Orchidaceae) from the Mato Grosso State, Brazil. Phytotaxa 472(1): 63–68. https://doi.org/10.11646/phytotaxa.472.1.8
  • Etter A, McAlpine C, Wilson K, Phinn S, Possingham H (2006) Regional patterns of agricultural land use and deforestation in Colombia. Agriculture, Ecosystems & Environment 114(2–4): 369–386. https://doi.org/10.1016/j.agee.2005.11.013
  • Ferreira AWC, de Oliveira MS, Silva EO, Campos DS, Pansarin ER, Guarçoni EAE (2017) Vanilla bahiana Hoehne and Vanilla pompona Schiede (Orchidaceae, Vanilloideae): Two new records from Maranhão state, Brazil. Check List 13(6): 1131–1137. https://doi.org/10.15560/13.6.1131
  • Flanagan NS, Mosquera-Espinosa AT (2016) An integrated strategy for the conservation and sustainable use of native Vanilla species in Colombia. Lankesteriana 16(2): 201–218. https://doi.org/10.15517/lank.v16i2.26007
  • Flanagan NS, Chavarriaga P, Mosquera-Espinosa AT (2018) Conservation and sustainable use of vanilla crop wild relatives in Colombia. In: Havkin-Frenkel D, Belanger FC (Eds) Handbook of vanilla science and technology, Second Edition. Wiley-Blackwell, Oxford, UK, 85–110. http://doi.org/10.1002/9781119377320.ch6
  • Gutiérrez-Morales N, Harding P, Dalström S, Moreno JS (2018) A new species of Cyrtochilum (Orchidaceae: Oncidiinae) from the eastern cordillera of Colombia. Lankesteriana 18(1): 63–68. https://doi.org/10.15517/lank.v18i1.33098
  • Gutiérrez-Morales N, Vieira-Uribe S, Moreno JS (2021) Lepanthes marielana (Orchidaceae, Pleurothallidinae), a new species from the eastern Andes in Colombia. Phytotaxa 484(1): 113–120. https://doi.org/10.11646/phytotaxa.484.1.5
  • Hágsater E, Gutiérrez N, Santiago E (2018) Epidendrum moralesii. In: Hágsater E, Santiago E (Eds) The Genus Epidendrum, Part 12, Icones Orchidacearum 16(1). Instituto Chinoin, AC, México, t. 1646.
  • Heywood V, Casas A, Ford-Lloyd B, Kell S, Maxted N (2007) Conservation and sustainable use of crop wild relatives. Agriculture, Ecosystems & Environment 121(3): 245–255. https://doi.org/10.1016/j.agee.2006.12.014
  • IPBES (2019) Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. In: Brondizio ES, Settele J, Díaz S, Ngo HT (Eds) IPBES secretariat, Bonn, 1148 pp. https://doi.org/10.5281/zenodo.3831673
  • Karremans AP, Lehmann C (2018) A highly threatened new species of Vanilla from Costa Rica. Lindleyana 87(4): 304–307.
  • Karremans AP, Chichilla IF, Rojas-Alvarado G, Cedeño-Fonseca M, Damian A, Léotard G (2020) A reappraisal of neotropical Vanilla with a note on taxonomic inflation and the importance of alpha taxonomy in biological studies. Lankesteriana 20(3): 395–497. https://doi.org/10.15517/lank.v20i3.45203
  • Keenan RJ, Reams GA, Achard F, de Freitas JV, Grainger A, Lindquist E (2015) Dynamics of global forest area: Results from the FAO Global Forest Resources Assessment 2015. Forest Ecology and Management 352: 9–20. https://doi.org/10.1016/j.foreco.2015.06.014
  • Kersey PJ, Collemare J, Cockel C, Das D, Dulloo EM, Kelly LJ, Lettice E, Malécot V, Maxted N, Metheringham C, Thormann I, Leitch IJ (2020) Selecting for useful properties of plants and fungi: Novel approaches, opportunities and challenges. Plants, People, Planet 2(5): 409–420. https://doi.org/10.1002/ppp3.10136
  • Koch AK, Fraga CND, dos Santos JUM, Ilkiu-Borges AL (2013) Taxonomic notes on Vanilla (Orchidaceae) in the Brazilian Amazon, and the description of a new species. Systematic Botany 38(4): 975–981. https://doi.org/10.1600/036364413X674706
  • Laverde Rodríguez O, Stiles FG, Múnera Roldan C (2005) Nuevos registros e inventario de la avifauna de la Serranía de las Quinchas, un área importante para la conservación de las aves (AICA) en Colombia. Caldasia 27(2): 247–265.
  • Lentijo GM, Hostetler ME (2013) Effects of a participatory bird census project on knowledge, attitudes and behaviors of coffee farmers in Colombia. Environment, Development and Sustainability 15(1): 199–223. https://doi.org/10.1007/s10668-012-9383-3
  • Lentijo GM, Arbeláez D, Castellanos O, Franco NG, López AM, Botero JE (2008) Enfoques participativos en investigación como una herramienta de conservación de las aves en zonas cafeteras de Colombia. Ornitologia Neotropical 19(Suppl): 567–574.
  • Maruenda H, del Lujan Vico M, Householder JE, Janovec JP, Cañari C, Naka A, Gonzalez AE (2013) Exploration of Vanilla pompona from the Peruvian Amazon as a potential source of vanilla essence: Quantification of phenolics by HPLC-DAD. Food Chemistry 138(1): 161–167. https://doi.org/10.1016/j.foodchem.2012.10.037
  • Maxted N, Kell S, Toledo Á, Dulloo E, Heywood V, Hodgkin T, Hunter D, Guarino L, Jarvis A, Ford-Lloyd B (2010) A global approach to crop wild relative conservation: Securing the gene pool for food and agriculture. Kew Bulletin 65(4): 561–576. https://doi.org/10.1007/s12225-011-9253-4
  • Mayaux P, Holmgren P, Achard F, Eva H, Stibig HJ, Branthomme A (2005) Tropical forest cover change in the 1990s and options for future monitoring. Philosophical Transactions of the Royal Society of London – Series B, Biological Sciences 360(1454): 373–384. https://doi.org/10.1098/rstb.2004.1590
  • Ministerio de Ambiente y Desarrollo Sostenible and Universidad Nacional de Colombia (2015) Plan para el estudio y la conservación de las orquídeas en Colombia. In: Betancur J, Sarmiento H, Toro-González L, Valencia J (Eds) Ministerio de Ambiente y Desarrollo Sostenible, Colombia; Universidad Nacional de Colombia, Bogotá D. C., Colombia, 336 pp.
  • Mittermeier RA, Turner WR, Larsen FW, Brooks TM, Gascon C (2011) Global biodiversity conservation: the critical role of hotspots. In: Zachos FE, Habel JC (Eds) Biodiversity hotspots: distribution and protection of conservation priority areas. Springer, Heidelberg, 3–22. https://doi.org/10.1007/978-3-642-20992-5_1
  • Molineros-Hurtado FH, González-Mina RT, Flanagan NS, Otero JT (2014) Vanilla rivasii (Orchidaceae), a new species from the Colombian pacific region. Lankesteriana 13(3): 353–357. https://doi.org/10.15517/lank.v13i3.14423
  • Murphy BR, Doohan FM, Hodkinson TR (2019) Prospecting crop wild relatives for beneficial endophytes. In: Endophytes for a Growing World, Cambridge University Press, 390–410. http://doi.org/10.1017/9781108607667.019
  • Nascimento TAD, Furtado MDSC, Pereira WC, Barberena FFVA (2019) Vanilla bahiana Hoehne (Orchidaceae): Studies on fruit development and new perspectives into crop improvement for the Vanilla planifolia group. Biota Neotropica 19(3): e20180696. https://doi.org/10.1590/1676-0611-bn-2018-0696
  • Navia-Samboni A (2021) Optimización de primers de PCR para el diagnóstico de especies de orquídeas en Colombia mediante Código de Barras de la Vida. Undergraduate Thesis. Pontificia Universidad Javeriana Sede Cali, Facultad de Ingeniería y Ciencias. Cali, Colombia, 81 pp.
  • Pansarin ER, Ferreira AWC (2022) Evolutionary disruption in the pollination system of Vanilla (Orchidaceae). Plant Biology 24(1): 157–167. https://doi.org/10.1111/plb.13356
  • Pérez-Silva A, Nicolás-García M, Petit T, Dijoux JB, de los Ángeles Vivar-Vera M, Besse P, Grisoni M (2021) Quantification of the aromatic potential of ripe fruit of Vanilla planifolia (Orchidaceae) and several of its closely and distantly related species and hybrids. European Food Research and Technology 247(6): 1489–1499. https://doi.org/10.1007/s00217-021-03726-w
  • Rodríguez-Salamanca MA (2020) Patrones de colonización de hongos micorrízicos de Vanilla en dos ecosistemas distintos en Madre de Dios, Perú. Undergraduate Thesis. Pontificia Universidad Javeriana Sede Cali, Facultad de Ingeniería y Ciencias. Cali, Colombia, 63 pp.
  • Rojas-Álvarez C (2020) Caracterización y georreferenciación de poblaciones naturales, cultivos de vainilla en territorios colectivos de la cuenca del Río Valle, Bahía Solano – Chocó. Undergraduate Thesis. Universidad Nacional Sede Medellín, Facultad de Ciencias Agrarias. Medellín, Colombia, 65 pp.
  • Sanchez-Cuervo AM, Aide TM (2013) Identifying hotspots of deforestation and reforestation in Colombia (2001–2010): Implications for protected areas. Ecosphere 4(11): 1–21. https://doi.org/10.1890/ES13-00207.1
  • Soacha-Godoy K, Gómez N (2016) Reconocer, conectar y actuar: porque la ciencia la hacemos todos. Memorias del primer encuentro de ciencia participativa sobre biodiversidad. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, 53 pp. https://doi.org/10.21068/r.2017.01 [Accessed on 25.01.2022]
  • Soto Arenas MA, Cribb P (2010) A new infrageneric classification and synopsis of the genus Vanilla Plum. Ex. Mill. (Orchidaceae: Vanillinae). Lankesteriana 9(3): 355–398. https://doi.org/10.15517/lank.v0i0.12071
  • Soto Arenas MA, Dressler RL (2010) A revision of the Mexican and Central American species of Vanilla Plumier ex Miller with a characterization of their ITS region of the nuclear ribosomal DNA. Lankesteriana 9(3): 285–354. https://doi.org/10.15517/lank.v0i0.12020
  • Ulian T, Diazgranados M, Pironon S, Padulosi S, Liu U, Davies L, Howes MJR, Borrell JS, Ondo I, Pérez-Escobar OA, Sharrock S, Ryan P, Hunter D, Lee MA, Barstow C, Luczaj L, Pieroni A, Cámara-Leret R, Noorani A, Mba C, Womdim RN, Muminjanov H, Antonelli A, Pritchard HW, Mattana E (2020) Unlocking plant resources to support food security and promote sustainable agriculture. Plants, People, Planet 2(5): 421–445. https://doi.org/10.1002/ppp3.10145
  • Xiong W, Zhao Q, Zhao J, Xun W, Li R, Zhang R, Wu H, Shen Q (2015) Different continuous cropping spans significantly affect microbial community membership and structure in a vanilla-grown soil as revealed by deep pyrosequencing. Microbial Ecology 70(1): 209–218. https://doi.org/10.1007/s00248-014-0516-0