88urn:lsid:arphahub.com:pub:84CAD438-4D58-581C-86A1-48EF43C3EC79Neotropical Biology and ConservationNBC2236-3777Pensoft Publishers10.3897/neotropical.17.e8679286792Research ArticleAngiospermaePlantaeBiodiversity & ConservationPlants and Botany: GeneralDistribution and conservation of vanilla crop wild relatives: the value of local community engagement for biodiversity researchFlanaganNicola S.nsflanagan@javerianacali.edu.cohttps://orcid.org/0000-0002-4909-87101ConceptualizationData curationInvestigationMethodologyProject administrationResourcesSupervisionValidationVisualizationWriting - original draftWriting - review and editingNavia-SamboniAndreshttps://orcid.org/0000-0002-3317-41171Data curationFormal analysisInvestigationMethodologyValidationVisualizationWriting - original draftWriting - review and editingGonzález-PérezEimer Norberto2Data curationInvestigationMethodologyResourcesMendieta-MatallanaHernan2InvestigationMethodologyResourcesDepartamento de Ciencias Naturales y Matemáticas, Pontificia Universidad Javeriana Seccional Cali, Calle 18 No. 118-250, Cali, ColombiaFinca La Cajita, Vereda Altazor, Otanche, Boyacá, ColombiaFinca La Esperanza, Vereda San José de Nazareth, Otanche, Boyacá, Colombia
Corresponding author: Nicola S. Flanagan (nsflanagan@javerianacali.edu.co)
Academic editor: Monika Lipińska
2022290920221732052270A3F3D57-A55E-5F4E-85B2-1CB82B4AAFBF2205202220082022Nicola S. Flanagan, Andres Navia-Samboni, Eimer Norberto González-Pérez, Hernan Mendieta-MatallanaThis is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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 Vanillakaren-christianae. For this, and the second species, Vanilladressleri, 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 scienceColombiacommunity-based participatory researchnatural rarityRed ListSerranía de las QuinchasTumbes–Chocó–Magdalena biodiversity hotspotVanilladressleriVanillakaren-christianaeIntroduction
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 Vanillaplanifolia 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 XanataSoto 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 SectionXanata, as valuable crop wild relatives, is urgently required.
Colombia is at the center of distribution for the SectionXanata, 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 SectionXanata (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 Vanillakaren-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.
MethodsStudy 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 Vanilladressleri 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 Vanillakaren-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 Vanillakaren-christianae and of Vanilladressleri, 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).
Global records of Vanillakaren-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)
Global records of Vanilladressleri. 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 Vanillakaren-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 Vanillakaren-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.
Vanillakaren-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.
Vanilladressleri 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.
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.
Type. Costa Rica. Puntarenas: Corredores. Canoas, 27 Sept. 2017, A.P. Karremans et al. 8087 (holotype: USJ; isotypes: JBL-spirit, CR).
New record.Vanillakaren-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.
Vanillakaren-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 Vanillakaren-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.
Vanillakaren-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.
Maps showing A global distribution of Vanillakaren-christianaeB global distribution of VanilladressleriC distributions of V.karen-christianae and V.dressleri in Colombia with respect to Protected areas (A–J) covering humid tropical forest.
https://binary.pensoft.net/fig/750578
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.
Type. Panama, Colón: End of Pipeline Road, Gamboa, 15 April 1982, S. Knapp 4621 & J. Mallet (holotype: MO 3032952).
New record.Vanilladressleri 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).
Vanilladressleri 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 Vanilladressleri 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.
Vanilladressleri 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 Vanillakaren-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 Vanillakaren-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.ensifoliaRolfe (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 Vanillaensifolia to be a synonym of V.odorata.
The species Vanilladressleri 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 XanataSoto Arenas and Cribb 2010, and these reports bring the total number of Vanilla species in Colombia to 27, with 22 in the SectionXanata. 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 Vanillakaren-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, Vanillakaren-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 Vanilladressleri 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 Vanilladressleri, 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 – Vanillacalyculata, 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).
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