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.

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

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.

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.

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).