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Article

Vanilla pompona Schiede (Vanilloideae-Orchidaceae): Morphological Variation of the Labellum in the Mexican Localities of Veracruz, Puebla, Jalisco and Oaxaca

by
Cecilia Viveros-Antonio
1,
Adriana Delgado-Alvarado
1,*,
Angel Bustamante-González
1,
Jesús Hernández-Ruíz
2,
Ma. de Lourdes Arévalo-Galarza
3 and
Braulio Edgar Herrera-Cabrera
1,*
1
Campus Puebla, Colegio de Postgraduados, Boulevard Forjadores de Puebla 205, Santiago Momoxpan 72760, Puebla, Mexico
2
División ciencias de la vida, Universidad de Guanajuato, Km 9 Carretera Irapuato-Silao, Ex Hacienda. El Copal, Irapuato 36500, Guanajuato, Mexico
3
Campus Montecillo, Colegio de Postgraduados, Carretera México-Texcoco Km 36.5, Montecillo, Texcoco 56230, Estado de México, Mexico
*
Authors to whom correspondence should be addressed.
Diversity 2023, 15(11), 1125; https://doi.org/10.3390/d15111125
Submission received: 8 September 2023 / Revised: 23 October 2023 / Accepted: 24 October 2023 / Published: 31 October 2023
(This article belongs to the Special Issue Genetic Diversity, Ecology and Conservation of Endangered Species)
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Abstract

:
Vanilla pompona is the third most important commercial species of the genus Vanilla, but the morphometric variation of its flowers is not well known. In orchids, infraspecific variation is expressed in the labellum. This study had the objective of analyzing the floral variation of V. pompona collections from the localities in Veracruz, Puebla, Jalisco and Oaxaca, in Mexico. During the flowering period, we obtained 55 collections of V. pompona flowers, and the labellum of each flower was dissected. We used ImageJ to measure and portray 54 lines and 7 angles in these labella. With the data obtained, we performed an analysis of variance, principal component analysis and cluster analysis. The results showed significant differences among the collections and localities in the means of the lines of the basal, middle, and apical regions of the labellum. Also, six morphotypes were obtained, and we found that variation was associated with factors such as the environment, geographic barriers, and pollinator pressure. Moreover, we observed variation in flowering periods in one locality of Veracruz. We concluded that there is infraspecific variation within and between the collection localities of V. pompona in the Atlantic region (Puebla and Veracruz) and the Pacific region (Jalisco and Oaxaca), Mexico.

1. Introduction

Vanilla pompona Schiede and Vanilla planifolia Andrews are two relevant species of the genetic reservoir of the genus Vanilla because of their economic importance [1,2,3]. Three subspecies have been reported for V. pompona: the subsp. pompona native to Mexico, subsp. grandiflora reported in Peru and Brazil and subsp. pittieri reported in Costa Rica [3,4,5,6]. The presence of V. pompona has been reported in the Guadeloupe Islands, Martinica and Dominica [1], in some regions of Guyana and Suriname [7], Costa Rica [8], Honduras and Panamá [4], Perú [9] and the state of Maranhão, Brazil [10]. In Mexico, this plant is distributed in Oaxaca, Nayarit, Puebla, Michoacán, Guerrero, Veracruz and Jalisco [6]. Vanilla pompona is a robust plant of broad leaves, resistant to diseases such as anthracnosis (Collectotrichum sp.) and root rot (Fusarium oxysporum Schltdl) [11], and tolerant to xerophyte climates [3,4], with a flowering period from April to June [3]. This species is distributed in several humid subtropical forests (deciduous, evergreen, gallery forests) and in pine and oak forests in warm climates [6,12]. Currently, V. pompona is an endangered species because its fragmented populations are decreasing [6]. However, there are reports that the processed fruits are used in the cosmetic and perfume industries [1] and in the preparation extracts for flavoring [13].
In Mexico, some morphological differences in the flower have been registered in two biological populations of V. pompona. The first population is characterized by flowers with extended segments of large dimensions, located in northern Oaxaca and Veracruz, on the slope facing the Gulf of Mexico. The second population is characterized by semi-closed flowers of smaller dimensions and is located on the Mexican Pacific coast [4].
Morphological traits of plants are used to analyze variation within and between species, particularly reproductive morphological traits, such as flowers, which are more stable than morphological traits of vegetative organs [14,15]. The labellum, as a reproductive structure of orchids, is less susceptible to the environment [14], and for this reason, it is used to identify species within this family [3,16] and analyze infraspecific variation [17,18]. It functions as a platform for insects to land on and to attract pollinators [19]. For the genus Vanilla, flowers are used to differentiate leafless species in the Southwestern Indian Ocean region, considering differences in the shape of the labellum [20]. Infraspecific variation has also been evaluated by characterizing the labellum shape of species such as V. planifolia [21] and V. pompona [22]. In the Mesoamerican region, V. planifolia variation is identified by four morphotypes in Oaxaca [23], four morphotypes in the San Luis Potosí Huastec region, Mexico [21], and five morphotypes in the Hidalgo Huastec region, Mexico [24]. For V. pompona, floral morphological variation of the labellum is still being studied; to date, there is only one study that reports four morphotypes in collections from localities in Oaxaca. This variation is explained by the constant selection pressure exerted by pollinators together with the environment [22].
Genetic diversity or genetic variation within species, referring to populations and individuals that comprise them [25], is one of the forms of biodiversity that should be conserved [26]. Knowledge and understanding of the variation within species are vital for the conservation of ecosystems and the social and cultural wellbeing of man [27,28]. Recently, studies were conducted to determine genetic variation [29,30,31] and floral morphological variation [21,22,23,26] of the most used Vanilla species, in a search for different stable populations that would increase genetic variation [31]. However, for V. pompona, detailed information on genotypes and phenotypes that make up the primary genetic pool and its interaction with the environment is limited. Its cultivation is recent, and thus, both traditional and technological knowledge of its cultivation and its infraspecific variation is also limited.
Plantations with incipient traditional management located close to natural forests maintain structural diversity, endemic species, and regional native species [32,33], contributing to the conservation of adjacent ecosystems [27]. Perennial plants, such as V. pompona, can grow in agroforestry systems where the trees that provide support and shade for this species maintain biogeochemical cycles and help preserve the local landscape and biodiversity [34]. For example, agroforestry systems where V. planifolia is cultivated in northeastern Madagascar are recognized as important areas for the conservation of birds [35]. For this reason, traditional Vanilla systems could be considered a determining factor in the preservation of this genetic resource [15,31].
In the study of morphological variation of orchid flowers, it is important to use an integrated approach, with classic taxonomy [20] and also morphometric analysis of the labellum, as has been used in different orchid species, for example, to differentiate between species of the genus Scaphyglottis [36]; and differentiate between Dryadella edwallii Luer, D. wuerstlei Luer and D. zebrina Luer [37]. The evaluation includes the morphological variation of Pseudolaelia vellozicola Hoehne populations [38] and populations of Pseudorchis straminea Fernald and P. albida Á.Love and D.Love [39]. In addition to studies on morphological variation in species of the Vanilla genus [21,22,23,24], studies of the labellum variation can be related with biotic factors (pollinators) and abiotic factors (environment). In orchids, biotic and abiotic factors, such as temperature and light, have been reported to influence the flowering period [40,41]. This study it will contribute knowledge on the labellum variation related to V. pompona flowering dates. In V. pompona, the morphological variation of flowers on the Mexican Atlantic slope and the Pacific Coast is unknown. For this reason, the study aimed to determine morphological variation of the V. pompona labellum in collections from localities of Veracruz, Puebla, Oaxaca and Jalisco. We believe that this knowledge is useful for the conservation, management and use of this species.

2. Materials and Methods

2.1. Geographic Location

In this study, V. pompona flowers were collected in the states of Jalisco, Oaxaca, Veracruz and Puebla, Mexico (Figure 1, Table 1).
Table 1. Localities where Vanilla pompona were sampled in several states of Mexico.
Table 1. Localities where Vanilla pompona were sampled in several states of Mexico.
StateMunicipalityLocalityAltitude (m)
VeracruzPapantlaCazuelas69
Gutiérrez Zamora Paso de Barriles29
TihuatlánLa Pasadita159
Puebla Tuzamapan de GaleanaReyes de Vallarta365
JaliscoCabo CorrientesCabo Corrientes379
OaxacaSta. Cruz ItundujiaHidalgo1075
Morelos1668
Primavera651
Sta. Ma. ChimalapaSta. Ma. Chimalapa362
Pluma HidalgoPluma Hidalgo1010
At each of the sampling sites, we obtained the climate type, mean annual precipitation (mm), mean annual temperature (°C), soil moisture regime and ecological zone [42] (Table 2).
Table 2. Environmental variables of the Vanilla pompona flower collection localities.
Table 2. Environmental variables of the Vanilla pompona flower collection localities.
Locality ClimateMean Annual Precipitation (mm)Mean Annual Temperature (°C)Soil Moisture RegimeEcological Zone
CazuelasWarm subhumid 800–1200>22UsticHumid tropical
Paso de
Barriles		Warm subhumid1500–2000>22Udic type IIHumid tropical
La PasaditaWarm subhumid1200–1500>22UsticHumid tropical
Reyes de
Vallarta		Warm humid2500–4000>22Udic type IHumid tropical
Cabo
Corrientes		Warm subhumid1500–2000>22XericSubhumid tropical
HidalgoSemi-warm subhumid2000–2500>22XericSubhumid
temperate
MorelosSemi-warm subhumid2000–2500>18XericHumid temperate
PrimaveraSemi-warm subhumid2000–2500>22XericSubhumid
temperate
Sta. Ma.
Chimalapa		Warm humid1500–2000>22UsticHumid tropical
Pluma
Hidalgo		Warm subhumid1500–2000>22UsticHumid temperate
Udic type I = 330 to 365 days of rain; Udic type II = 270 to 330 days of rain; Ustic = 180 to 270 days of rain; Xeric = 90 to 180 days of rain [42].
Geographic localities of Mexico where Vanilla pompona flowers were collected.

2.2. Study Area

Vanilla pompona Schiede flowers were sampled during the flowering period (March–May) in the localities of Cazuelas, Paso de Barriles, La Pasadita, Cabo Corrientes, Hidalgo, Morelos, Primavera, Santa María Chimalapa, Pluma Hidalgo and Reyes de Vallarta. These are the places where we had the opportunity to collect flowers, since there is not much information on where specimens of this species are found. Also, the collections we obtained could represent part of the V. pompona variation that exists in Mexico (Table 1).

2.3. Vegetal Material

We obtained 55 collections of V. pompona flowers during the flowering period (March–May) in the years 2019 to 2022. Each collection had three to five replications, and we obtained a total of 192 flowers with pollinia and no observable damage (Figure 2). In the locality of Cazuelas, Veracruz, at the suggestion and empirical knowledge of the owner of the lot, the flowers were collected on different dates of the year. The clones were named according to the flowering period: early flowering clone (March–May), continuous-flowering clone (March–October) and late flowering clone (June–August).
The collected flowers were stored in a preservative solution. Each 150 mL recipient contained a preservative solution of ethanol (50%), lactic acid (4%), benzoic acid (0.5%, glycerin (2.5%) and distilled water (43%). The recipients were stored at room temperature (23–24 °C) in a dark room [17,22].

2.4. Morphological Characterization of the Labellum

Evaluation of the variation in the flower labellum was based on the technique of Catling [17] and Hernández-Ruíz et al. [22]. First, the flower was dissected, and the labellum was extended on a glass surface. The labellum was then impregnated with methylene blue (0.08%) and photographed with a Sony reflex alpha 65v camera, fixed on a tripod and equipped with a Sony DT macro lens 30 mm F/2.8 SAM. The images were processed with the ImageJ program to generate 54 lines and 7 angles, and to measure the lines and angles.
To generate the lines and angles, the labellum was divided into three regions, following the protocol of Hernández-Ruíz et al. [22]. The basal region was formed by lines A, A1, A2, A3, A4, A5, B1x and the angle aA (Figure 3a).
The middle region contained lines B, B2, B5, B7, B8, B9, B10, C, C1x, C2, C5, C7, C8, C9, C10, D, D1x, D2, D5, D7, D8, D9, D10, E, E1x, E2, E5, E7, E8, E9 and E10, while the angles were aB, aD, aDE22, aDE55 and aE (Figure 3b). The apical region was made up of lines F, F1x, F2, F5, F7, F8, F9, F10, G, G1x, G2, G3, G4, G6, G7 and angle aG, and to obtain the length of the labellum, the lines A, B, C, D, E, F and G were added (Figure 3c).

2.5. Statistical Analyses

With the measurements of the 54 lines and 7 angles of the labellum of the 55 collections of V. pompona obtained from different localities, we performed an analysis of variance (ANOVA). The collections were the source of variation. Fifty-five collections (treatments) were analyzed, each with different numbers of replications (labella) under a model equivalent to the completely randomized unbalanced design (PROC GLM; SAS, 2002).
In orchid flower morphometry studies, the most commonly used multivariate analyses are principal component analysis (PCA) and canonical variable analysis (CVA) [43]. Canonical variable analysis are used to explore the separation of a priori-defined groups [44,45]. (These groups should consist of 12 to more than 30 replicates [46,47]). Recently, studies have been carried out in orchids based on morphometric analysis of flowers where CVA is used to differentiate between species of the genus Epidendrum [48], to delimit the species Trichocentrum cepula, T. caatingaense and T. sprucei [49], and to distinguish species of the genus Scaphyglottis [36]. On the other hand, principal component analysis (PCA) is used to reduce dimensions and explore the overall structure of the database according to Wickens [50] and Lattin et al. [44], and is performed based on the correlation matrix between the selected variables [51].
In the study of the variation of the labellum of V. pompona, no a priori-defined groups were formed, because the necessary characters to form them do not exist, which was one of the reasons why the CVA was not used. Another reason is that among our specimens, we have three to five replicates per collection, and we could not have more due to the distance between the collection localities and because the flowers are ephemeral (they only last one day) [12]. In addition, in this study, we analyzed the infraspecific variation of the labellum of V. pompona, not the variation between species, so we considered it appropriate to perform multivariate principal component analysis (PCA) and cluster analysis with a mean distance between the clusters for the 61 traits (lines and angles) defined previously for V. pompona [22,51]. The SAS statistical software version 9.0 (2002) was used [52].

3. Results

3.1. Characterization of the Labellum

The analysis of variation showed significant differences in the 61 variables evaluated on the V. pompona labellum. For example, with line A (3.65 ***), which is at the base of the labellum, and line C1x (4.88 ***), which is on the apical part of the labellum, we found differences in the average measurements of the labellum between collections. The coefficients of variation of the lines were, in general, low; exceptions were lines A1 (10.63) and G3 (12.84%), and angle aG (10.80%). Even so, we detected variation in the measurements of the labella of the collected flowers (Table 3). Therefore, the results indicated that there are differences in the means of the lines of the basal, middle and apical regions of the labellum among the collections and localities.

3.2. Distribution of the Variation

To identify the variation of the measurements of the 54 lines and 7 angles in the V. pompona flower labellum, we used principal component analysis. The dispersion of the 55 collections represented by the first three principal components together explained 75% of the accumulated variation. The first principal component (PC1) explained 43% of the general variation and was associated with the labellum length (0.187) (Table 4). For this reason, this variable determined part of the morphological variation of the labellum of the V. pompona specimens found at the collection sites.
The second principal component (PC2) expressed 20% of the total variation and was associated with the variables aD (0.205), E7 (0.196), E10 (0.196), F1x (0.209), F2 (0.191), F7 (0.211), F9 (0.195), F10 (0.205) and G7 (0.187). The third principal component (PC3) defined 12% of the variation, explained by the variables D (0.264), D2 (0.274), D5 (0.275), D7 (0.208), D8 (0.214), D9 (0.205), D10 (0.217), E2 (0.251), E5 (0.249) and aE (−0.188) (Table 4). Thus, the variables that explain PC2 and PC3 contribute to the shape, width and amplitude of the V. pompona labellum.
In accordance with the first three principal components, the spatial distribution of the evaluated collections revealed six groups (six morphotypes) (Figure 4). The distribution of the collections based on principal component 1 (PC1) placed the collections with the longest labella on the positive axis from the center upward (Groups I, II, III). The rest of the groups (Groups IV, V, VI) were on the negative axis, from −5 to −20.
Principal component 2 (PC2) concentrated the collections that have the shortest lines in the apical region of the labellum (E7, E10, F1x, F2, F7, F9, F10 and G7) on the negative axis (Groups IV, V and VI), while collections with longer and wider edges on the lateral lobes and wider labellum were placed in the callus region (aD) on the positive axis (Groups I, II and III).
Principal component 3 (PC3) was represented by the collections with a smaller amplitude (aE) of the middle region of the labellum and short lines in the middle region of the labellum (D, D2, D5, D7, D8, D9, D10, E2 and E5). These collections were placed on the negative axis (Groups IV, V and VI). Likewise, the collections with acute angles of 88–89° in the middle region of the labellum (aE) and some lines of the middle region of the labellum (D, D2, D5, D7, D8, D9, D10, E2 and E5), which define the shape and size of the labellum, were placed on the positive axis (Groups I, II and III).
We identified six morphological groups (morphotypes) in functions of the labellum.
Group I included collections 1, 8, 10, 22, 34, 40, 51, 52, 53, 50, 2, 7, 35, 5, 38, 39, 55, 41, 42, 24, 30, 28, 32, 33, 25, 26, 3, 4, 6, 31, 54, 23, 27, 9, 21 and 43. These collections are from the localities of Cazuelas, Papantla; Barriles and Gutiérrez Zamora, state of Veracruz; and from Cabo Corrientes, state of Jalisco. Among these collections are early, continuous and late-flowering clones.
Group II was made up of collections 20 and 46 of the locality Cazuelas, and are continuous-flowering clones, which begin flowering in March and continue into October.
Group III included collections 29, 36, 37, 44, 45, 47, 48 and 49 from La Pasadita, Tihuatlan, Veracruz; Reyes de Vallarta, Tuzamapan de Galeana, Puebla; and Cabo Corrientes, Jalisco. This group also included collections from Cazuelas land Papantla, Veracruz, that are early-flowering (March–May).
Group IV was represented by collections 12, 13, 14, 15, 18 and 19 from Hidalgo, Morelos, and Primavera, municipality of Santa Cruz Itundujia, and Pluma Hidalgo, state of Oaxaca.
Group V included collections 16 and 17 from the municipality of Santa María Chimalapa, Oaxaca.
Group VI was made up of only collection 11 from the municipality of Santa María Chimalapa, Oaxaca.

3.3. Grouping Diversity

The cluster analysis, with a distance between the clusters of 0.9, confirmed the identification of the six groups defined according to the principal component analysis. These groups were denominated morphotypes (Figure 5).
Morphotype I (MI) included 36 collections that were distinguished by an irregular pentagon shape and a rounded shape of the lateral lobes. The total length of the labellum was 76.00 mm and its angles in the middle region were 146° and 146°. The lengths of each region were the following: basal region (B1x) 4.88 mm, middle region (D1x) 33.22 mm, and apical region (F1x) 32.90 mm.
Morphotype II (MII) was represented by collections 20 and 46 from the locality of Cazuelas. This morphotype was characterized by a longer labellum (81.44 mm) and by rounded lateral lobes that significantly differentiate them from the apical lobe of the labellum. The labellum lengths, by region, were basal region (B1x) 4.94 mm, middle region (D1x) 34.50 mm, and apical region (F1x) 36.33 mm. The amplitudes of the middle labellum region were 147° and 149°.
Morphotype III (MIII) included collections 29, 36, 37, 44, 45, 47, 48 and 49. These collections were distinguished by the rhomboid shape of their labellum; the length was 80.74 mm and the amplitudes of the middle region were 149° and 149°. The length of each region of the labellum was as follows: basal region (B1x) 4.49 mm, middle region (D1x) 33.72 mm, and apical region (F1x) 29.99 mm.
Morphotype IV (MIV) was represented by collections 12, 13, 14, 15, 18 and 19, which had oval-shaped lateral lobes. This shape was defined by a labellum 68.28 mm long and angles of the middle region of 146° and 142°. They had the following lengths of each region of the labellum: basal region (B1x) 5.31 mm, middle region (D1x) 31.45, and apical region (F1x) 30.85 mm.
Morphotype V (MV) was made up of collections 16 and 17, which had a shape with marked lateral lobes, compared with the lobes of the apical region. The labellum length was 71.34 mm, and the angles of the lateral lobes were 140° and 149°. The lengths of each region were the following: basal region (B1x) 4.44 mm, middle region (D1x) 29.85 mm, and the apical region (F1x) 26.28 mm.
Morphotype VI (MVI) was represented by collection 11, which was differentiated from the other morphotypes by a shorter labellum (60.65 mm) and smaller amplitude in the angles of the lateral lobes (129° and 137°). The different regions of the labellum were defined by the following lengths: basal region (B1x) 4.69 mm, middle region (D1x) 26.47 mm, and apical region (F1x) 22.34 mm.

4. Discussion

4.1. Characterization of the V. pompona Labellum

The analysis of variance indicated that there were differences in the means of the lines in the basal, middle and apical regions of the labellum and the lengths of the labellum among the collections and localities. This agrees with Hernández-Ruiz et al. [22], who reported that for V. pompona from Oaxaca, Mexico, the differences were highly significant in 58 of the variables of the labellum evaluated.
The coefficients of variation of the lines and angles evaluated oscillated between 3.29 and 12.84%, percentages that are lower than those found in other studies on orchid variables [21,23]. These results show that the labellum is an important structure of the vanilla flower in the analysis of variation and has been used to analyze infraspecific morphological variation in orchids [18,53]. Also, the labellum has been used to differentiate between subspecies, as reported for Vanilla pompona Schiede subsp. pompona, for which one of the main characteristics that distinguishes this subspecies was the length of the labellum (50 to 80 mm), while the length of Vanilla pompona subsp. grandiflora Lindl. was more than 80 mm [3].

4.2. Distribution of the Variation

The dispersion of the labella of the V. pompona collections from the Gulf of Mexico slop and the Pacific coast was represented by the first three principal components, which together explained 75% of the accumulated variation, a percentage that is lower than that in the study conducted by Hernández Ruíz et al. [22], who detected 81% of the variation in V. pompona collected only in Oaxaca, suggesting that the variation in floral traits of the first three components of this study is due to the use of collections from localities in different states of Mexico.
The horizontal length of the labellum, the variable that determines the size of the flowers, separated the PC1 groups and explained most of the variation (43%). This contrasts with Hernández-Ruíz et al. [22], who state that, for the populations of V. pompona from Oaxaca, PC1 is associated with the variation in shape and size of some sections of the middle region of the labellum and with a variable of the apical region of the labellum.
The variables of the apical region of the labellum and one angle of the middle region differentiated the PC2 groups. This was similar to the variables reported that defined the PC2 groups from the V. pompona populations of Oaxaca, the apical region together with the dimension of the basal region [22]. For PC3, the morphological variables that separated the groups were those of the middle region of the labellum, which was likewise one of the variables that influenced the definition of groups of the third component within the V. pompona collections from Oaxaca [22].
In our study, the variables that explain PC2 and PC3 determined the shape, size and amplitude of lateral and apical lobes of the V. pompona labellum from localities of Veracruz, Jalisco, Puebla and Oaxaca. In studies on V. planifolia, with the PCA, it was found that PC2 and PC3 were explained by variables that form part of the labellum shape and size of the middle lobes, aperture and size of the lateral lobes labellum [23], also in the shape of the labellum in the apical region and amplitude of the lobes [21]. Thus, in the V. pompona collections evaluated in our study, the middle and apical regions and the length of the labellum explain the variation. According to the studies conducted on variation of the labellum of the genus Vanilla [21,22,23,24], the variables used are suitable since, despite differences in the measures, shapes and size of the labellum in V. pompona and V. planifolia, these traits allow for the analysis of infraspecific variation and the variation between species.

4.3. Morphotype Grouping

Variation of the V. pompona labellum grouped in six morphotypes by PCA and cluster analysis indicates that these morphotypes represent the variation that exists in the localities of Veracruz, Jalisco, Puebla, and Oaxaca.
Morphotype I is represented by collections from localities of Veracruz and Jalisco. The collections from Veracruz are influenced by the slope of the Gulf of Mexico on the Atlantic side, while Cabo Corrientes is found on the Pacific coast on the other side of Mexico. However, despite their geographic separation by the Sierra Madre Oriental and the Sierra Madre Occidental [54] both have warm subhumid climate (Table 2) and are located on the same latitude. This could indicate that environmental and geographic characteristics have an influence in the fact that the collections from Veracruz and Jalisco are the same labellum morphotype (Figure 5).
The collections from Cazuelas, Papantla, Veracruz, are morphotype II, which stands out because the labellum (81.44 mm) is longer than that of the other morphotypes. This coincides with Soto-Arenas [4], who reported that V. pompona is made up of two population sets in Mexico, one in Veracruz on the Gulf of Mexico slope, characterized by its flower with extended segments of large dimensions.
Morphotype III is the widest and comprises collections from Cabo Corrientes, Jalisco; and Papantla and Tihuatlán, Veracruz; and Tuzamapan de Galeana, Puebla. The localities of the collections from Veracruz and Puebla belong to the humid tropical ecological zone, while Cabo Corrientes belongs to the sub-humid tropical ecological zone, but the climate is warm subhumid, like that of Veracruz (Table 2), and allows them to share the same labellum morphotype.
Morphotypes IV, V and VI of the Oaxaca localities have smaller labella. This coincides with Soto-Arenas [4], who mention that the second V. pompona population is found on the Mexican Pacific coast and is characterized by smaller semi-closed flowers, while Hernández-Ruíz et al. [22] reported similar findings in the study of floral morphological variation in the Oaxaca populations, where the morphotype CAZ is found. This morphotype was the smallest labellum.
Morphotypes IV, V and VI are found on the Mexican Pacific coast, and localities where the flowers were collected are in the Sierra Madre del Sur [54], which facilitates the isolation of biological communities and separates ecological zones [55]. Moreover, the collection sites are found in the humid temperate, subhumid, and humid tropical zone (Table 2), which explains the variation found in Oaxaca. Also, a study of the V. pompona labellum from Oaxaca reports four morphotypes, and the variation found was due to the mountain complex belonging to the Sierra Madre del Sur, which separates the ecological zones where the species is found and functions as a geographic barrier [22], while for V. planifolia, the study reports that some characteristics of the upper and apical regions of the labellum are related to environmental factors [23].
Specifically, morphotype VI from Oaxaca has a horizontally narrower labellum (60.65 mm) and is different from morphotype II from Veracruz, with a horizontal length of 81.44 mm. Morphotype VI is found on the Pacific coast and is in the Sierra Madre del Sur [54], while morphotype II is found on the Gulf of Mexico slope and belongs to the Sierra Madre Oriental [56]. These mountain chains function as geographic barriers and could partly explain the genetic diversity and speciation in orchids [57]. Moreover, it has been documented that the Gulf of Mexico has greater influence in the warm subhumid climate [55] where morphotype II is found, while morphotype VI is found in a warm humid climate (Table 2). It should be considered that the longer labellum of morphotype II could be influenced by the slope of the Gulf of Mexico since it is more humid than the Pacific coast [58]. V. pompona is considered a wild plant because it has not undergone the process of domestication that leads to changes in plant morphology [59]. Another cause of variation in the V. pompona labellum could be the environment, caused by the geographic location different from the collection sites. In Vanilla, the environment where the plants are found plays a highly important role in terms of availability of resources such as water, carbon and nutrients, and only the apical region of the labellum can be modified by the availability of these resources [24].
Vanilla pompona has a reward strategy to attract pollinators by offering them both nectar and fragrance [60]. Different studies have documented the presence of specific pollinators for this species, as in some populations in Brazil, where Eulaema bombiformis Packard, E. cingulate Fabricius and E. meriana Olivier have been described [60]. While in Costa Rica and Peru, males of the species E. cingulata Fabricius have been reported as the specific pollinators of this plant [61]. The variation in the six V. pompona labellum morphotypes identified in this study could be associated in part by pollinator pressure, as has already been reported for other orchids [62]. However, pollinator pressure in V. pompona is only one possibility, which needs to be tested.
The collections that form morphotypes I, II and III are early-flowering (March–May), continuous-flowering (March–October) and late-flowering (June–August) floral labella from the locality of Cazuelas, Papantla, Veracruz. Studies have reported that V. pompona flowering in Mexico is April to June [3], but in V. pompona populations in Costa Rica and Peru, they found two flowering periods, one January to February and another in September [61]. In V. pompona populations in the state of Maranhão, Brazil, flowering occurs in July and August [11], and in the Amazonian wetlands of Madre de Dios, Peru, the V. pompona subsp. grandiflora populations have two flowering periods [9] that can vary depending on their geographic location, responding to specific environmental conditions, such as temperature and light during the flowering period [40,41]. It is interesting in Mexico that in a collection locality (established approximately 10 years ago) in Veracruz, specimens of V. pompona can be found with different flowering dates.
This study contributes knowledge on the variation of the V. pompona labellum in the states of Veracruz, Puebla, Jalisco and Oaxaca. The knowledge generated will help producers to better use the plant by selecting which plants to cultivate with different flowering dates. Growers will also be able to decide which specimens to plant according to the morphotype that is found near the area where they live. Moreover, the information contributes to the conservation of genetic diversity. However, more studies are needed on genetic variation and with floral ecology of the V. pompona germplasm in Mexico.

5. Conclusions

Six morphotypes of the labellum of V. pompona were obtained from localities in the states of Veracruz, Puebla, Oaxaca and Jalisco, Mexico. Each morphotype was distinguished mainly by size and shape, which shows that there is infraspecific variation in the germplasm of V. pompona. The variation that exists in the labels of this species was possibly associated with pollinator pressure and the presence of geographic barriers, which play very important roles in the types of environments in which the specimens of V. pompona develop. This plant is wild; therefore, the environment plays a very important role in the variation related to phenological factors, since, for the locality of Cazuelas, Papantla Veracruz, plants with different flowering dates during the year were found. Knowledge of the infraspecific variation of the species is important for the conservation and preservation of this species in Mexico.

Author Contributions

Conceptualization, A.D.-A., C.V.-A. and B.E.H.-C., methodology, A.D.-A., C.V.-A. and B.E.H.-C.; validation, A.D.-A., C.V.-A., B.E.H.-C., A.B.-G., J.H.-R. and M.d.L.A.-G.; investigation, C.V.-A. and A.D.-A.; resources, A.D.-A. and B.E.H.-C.; writing—original draft preparation, C.V.-A. and B.E.H.-C.; writing—review and editing, A.B.-G., J.H.-R. and M.d.L.A.-G. All authors have read and agreed to the published version of the manuscript.

Funding

This study is a product of the doctoral dissertation of the first author, who is grateful to the Consejo Nacional de Humanidades Ciencias y Tecnologías (CONAHCyT) for grant number 594733 in support of her doctoral studies.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank the people in the collection localities in the states of Puebla, Veracruz, Oaxaca and Jalisco, Mexico, for their support.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Geographical location of the collection sites of Vanilla pompona flowers in Mexico. The red dots show the collection sites: Cabo Corrientes (Jalisco), Santa Cruz Itundujia, Pluma Hidalgo and Santa María Chimalapa (Oaxaca), Tuzamapan de Galeana (Puebla), Papantla, Tihuatlán and Gutiérrez Zamora (Veracruz).
Figure 1. Geographical location of the collection sites of Vanilla pompona flowers in Mexico. The red dots show the collection sites: Cabo Corrientes (Jalisco), Santa Cruz Itundujia, Pluma Hidalgo and Santa María Chimalapa (Oaxaca), Tuzamapan de Galeana (Puebla), Papantla, Tihuatlán and Gutiérrez Zamora (Veracruz).
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Figure 2. Phenological stages of Vanilla pompona; flowering in April and mature fruits in December.
Figure 2. Phenological stages of Vanilla pompona; flowering in April and mature fruits in December.
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Figure 3. Vanilla pompona flower, labellum separated and dyed, fragmentation of the labellum into the (a) basal region, (b) middle region and (c) apical region.
Figure 3. Vanilla pompona flower, labellum separated and dyed, fragmentation of the labellum into the (a) basal region, (b) middle region and (c) apical region.
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Figure 4. (A) Variables that define each of the first three principal components. (B) Dispersion of the 55 collections of the flower labellum of Vanilla pompona based on the first three principal components from the localities of Veracruz, Jalisco, Puebla and Oaxaca, Mexico. The colors in the labellum diagram correspond to the PCs, the blue color corresponds to the PC1 variables, yellow colors correspond to the PC2 variables, and the red color correspond to the PC3 variables. GI to GVI: Group I to Group IV. Each group had a different color to differentiate them.
Figure 4. (A) Variables that define each of the first three principal components. (B) Dispersion of the 55 collections of the flower labellum of Vanilla pompona based on the first three principal components from the localities of Veracruz, Jalisco, Puebla and Oaxaca, Mexico. The colors in the labellum diagram correspond to the PCs, the blue color corresponds to the PC1 variables, yellow colors correspond to the PC2 variables, and the red color correspond to the PC3 variables. GI to GVI: Group I to Group IV. Each group had a different color to differentiate them.
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Figure 5. Dendrogram of the labellum morphotypes of Vanilla pompona from the localities of Veracruz, Jalisco, Puebla and Oaxaca, Mexico, based on the average of 61 variables and grouping by similarity distance. MI to MVI: Morphotype I to Morphotype IV. Each morphotype had a different color to differentiate them.
Figure 5. Dendrogram of the labellum morphotypes of Vanilla pompona from the localities of Veracruz, Jalisco, Puebla and Oaxaca, Mexico, based on the average of 61 variables and grouping by similarity distance. MI to MVI: Morphotype I to Morphotype IV. Each morphotype had a different color to differentiate them.
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Table 3. Coefficients of variation and mean squares of the 61 variables of the Vanilla pompona labella analyzed.
Table 3. Coefficients of variation and mean squares of the 61 variables of the Vanilla pompona labella analyzed.
VariableMean (mm)Coefficient of
Variation		Mean Squares
ErrorLocalityCollection
I. Labellum basal region
A23.333.800.7934.08***3.64***
A12.1810.630.051.53***0.30***
A223.373.850.8133.58***3.64***
A323.383.820.8033.17***3.57***
A423.594.150.9634.14***3.61***
A523.574.130.9534.86***3.73***
aA17.178.191.9850.91***5.15***
B1x4.878.030.153.09***0.51***
II. Labellum middle region
B11.634.750.318.64***0.93***
B213.254.720.399.58***1.14***
B513.404.720.408.06***1.12***
B714.574.580.458.69***1.15***
B811.924.540.297.36***0.83***
B911.874.570.298.09***0.97***
B1014.764.560.456.77***1.16***
aB23.678.163.73153.82***16.61***
C11.624.780.318.65***0.93***
C1x17.787.071.5818.58***4.88***
C213.865.380.5613.41***1.57***
C513.955.420.579.71***1.96***
C720.085.261.1120.64***2.26**
C814.694.650.475.90***1.02**
C914.624.510.449.45***1.17***
C1020.235.001.0214.39***2.97***
D8.357.370.385.29***1.57***
D1x32.905.953.8457.94***9.48***
D28.746.870.364.43***1.25***
D58.776.740.354.31***1.28***
D711.847.370.7611.70***2.37***
D811.615.660.436.49***0.93**
D911.645.250.376.61***0.84**
D1011.847.270.7411.37***2.53***
aD88.254.5316.00230.14***102.01***
aDE22146.004.3239.71321.71***118.57***
aDE55145.984.4742.55348.61***120.61***
E8.126.390.274.75***0.78***
E1x37.454.673.0578.02***6.58**
E28.656.330.303.59***0.92***
E58.636.370.304.25***1.03***
E711.375.980.4614.08***1.49***
E811.474.530.277.35***0.51**
E911.434.650.287.81***0.54**
E1011.416.320.5213.18***1.48***
aE89.694.2514.5576.97***62.19***
III. Labellum apical region
F6.227.450.225.62***0.70***
F1x32.025.062.6296.25***11.02***
F27.257.820.325.76***0.94***
F57.208.110.346.49***0.88***
F717.205.640.9428.32***3.39***
F813.826.070.7021.96***2.64***
F913.926.270.7619.98***3.15***
F1017.135.330.8328.96***2.92***
G6.259.310.345.55***1.23***
G1x24.776.142.3165.83***10.69***
G211.309.461.1417.49***4.06***
G36.1612.840.6322.79***3.90***
G411.209.401.1126.84***4.78***
G66.929.750.467.23***1.53***
G76.989.600.455.43***1.19***
aG51.9910.8031.551168.06***221.56***
Labellum length75.473.296.17286.36***21.27***
***: p ≤ 0.0001 highly significant, **: p ≤ 0.005 moderately significant.
Table 4. Eigenvalues, eigenvectors and accumulated proportion of the variation explained by each variable in the first three dimensions of the characterization of the 55 collections of Vanilla pompona.
Table 4. Eigenvalues, eigenvectors and accumulated proportion of the variation explained by each variable in the first three dimensions of the characterization of the 55 collections of Vanilla pompona.
VariablePrincipal Component (PC)VariablePrincipal Component (PC)
PC1PC2PC3PC1PC2PC3
I. Labellum basal region D90.150−0.0470.205
A0.156−0.123−0.133D100.097−0.1350.217
A10.101−0.055−0.026aD0.0110.205−0.232
A20.156−0.123−0.134aDE220.047−0.055−0.052
A30.156−0.122−0.134aDE550.034−0.092−0.075
A40.159−0.121−0.130E0.1290.0920.180
A50.158−0.122−0.130E1x0.1390.1370.084
aA−0.0620.0830.107E20.1170.0250.251
B1x−0.0250.0730.069E50.1170.0380.249
II. Labellum middle region E70.1250.1960.029
B0.157−0.118−0.133E80.1610.1240.115
B20.168−0.116−0.065E90.1590.1250.123
B50.158−0.113−0.066E100.1260.1960.021
B70.165−0.101−0.033aE−0.0060.017−0.188
B80.156−0.119−0.132III. Labellum apical region
B90.159−0.115−0.128F0.1210.1820.047
B100.151−0.099−0.026F1x0.1250.209−0.058
aB−0.0930.1040.110F20.1100.1910.065
C0.157−0.118−0.133F50.1090.1750.046
C1x0.064−0.0130.146F70.1250.211−0.036
C20.166−0.098−0.088F80.1320.186−0.067
C50.153−0.080−0.091F90.1250.195−0.050
C70.170−0.0770.020F100.1290.205−0.050
C80.160−0.096−0.033G0.1130.176−0.087
C90.161−0.105−0.029G1x0.1260.185−0.084
C100.149−0.0540.020G20.0920.148−0.066
D0.095−0.1370.264G30.0340.1110.040
D1x0.132−0.0250.092G40.1220.119−0.097
D20.110−0.0840.274G60.1040.181−0.064
D50.109−0.0770.275G70.1050.187−0.056
D70.101−0.1430.208aG−0.0270.0270.072
D80.148−0.0420.214Long_lab0.187−0.044−0.029
Eigenvalues26.12612.1747.401
Proportion 0.430.200.12
Accumulated 0.430.630.75
Values in bold indicate variables that have the most influence within each principal component.
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Viveros-Antonio, C.; Delgado-Alvarado, A.; Bustamante-González, A.; Hernández-Ruíz, J.; Arévalo-Galarza, M.d.L.; Herrera-Cabrera, B.E. Vanilla pompona Schiede (Vanilloideae-Orchidaceae): Morphological Variation of the Labellum in the Mexican Localities of Veracruz, Puebla, Jalisco and Oaxaca. Diversity 2023, 15, 1125. https://doi.org/10.3390/d15111125

AMA Style

Viveros-Antonio C, Delgado-Alvarado A, Bustamante-González A, Hernández-Ruíz J, Arévalo-Galarza MdL, Herrera-Cabrera BE. Vanilla pompona Schiede (Vanilloideae-Orchidaceae): Morphological Variation of the Labellum in the Mexican Localities of Veracruz, Puebla, Jalisco and Oaxaca. Diversity. 2023; 15(11):1125. https://doi.org/10.3390/d15111125

Chicago/Turabian Style

Viveros-Antonio, Cecilia, Adriana Delgado-Alvarado, Angel Bustamante-González, Jesús Hernández-Ruíz, Ma. de Lourdes Arévalo-Galarza, and Braulio Edgar Herrera-Cabrera. 2023. "Vanilla pompona Schiede (Vanilloideae-Orchidaceae): Morphological Variation of the Labellum in the Mexican Localities of Veracruz, Puebla, Jalisco and Oaxaca" Diversity 15, no. 11: 1125. https://doi.org/10.3390/d15111125

APA Style

Viveros-Antonio, C., Delgado-Alvarado, A., Bustamante-González, A., Hernández-Ruíz, J., Arévalo-Galarza, M. d. L., & Herrera-Cabrera, B. E. (2023). Vanilla pompona Schiede (Vanilloideae-Orchidaceae): Morphological Variation of the Labellum in the Mexican Localities of Veracruz, Puebla, Jalisco and Oaxaca. Diversity, 15(11), 1125. https://doi.org/10.3390/d15111125

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