English (pdf)
Article in xml format
Article references
Automatic translation
Send this article by e-mail
Cited by SciELO 
Cited by Google 
Similars in
SciELO 
Similars in Google 
Permalink
The word mortiño is described by Castilian language as a term applied to plants of the genus Vaccinium, name imposed by the Spanish in America; the first reference of the expression mortiño dates from 1548, which was used in the region of Guaca, current province of Carchi, Ecuador, a village inhabited by the "Pastos" indigenous(Patiño, 2002).
The agraz, mortiño or vichachá, Vaccinium meridionale Swartz, is a clonal plant belonging to the tribe Vaccinieae Rehb. and Ericaceae Juss. family; it comprises about 35 genera and more than 1000 species. Also, the genus Vaccinium has registered between 400 and 450 species, distributed in the northern hemisphere and in the mountains of the tropical regions of the Andes, South Africa and Madagascar (Luteyn, 2002; Smith et al., 2004). On the other hand, the mountains of northwestern South America and especially on the Pacific slope are rich in this group of plants (Salinas and Betancur, 2007). In the High Andean Area, there is information available on five species: V. corymbodendrom Klotzsch, V. floribundum Kunth, V. meridionale Swartz, V. euryanthum A.C. Smith, and V. singularis Salinas & Betancur; the last mentioned is only known in the Pacific slope of the department of Nariño (Salinas and Betancur, 2007). According to Ligarreto (2009), the species of the genus Vaccinium are distributed in the Departments of Antioquia, Boyacá, Cauca, Chocó, Cundinamarca, Magdalena, Meta, Nariño, Norte de Santander, Putumayo, Quindío, Santander, and Tolima; with the highest number of reports in Antioquia, Boyacá and Cundinamarca.
The mortiño represents a viable alternative for fruit growing with possibilities of development in the country in similar climatic conditions. This is based on a series of aspects such as international and national demand for berries, the presence of ecological niches suitable for their production, spontaneous populations in the Andean area with various forms of agro-industrial use. It is also a plant of great agro-industrial interest for the antioxidant activity of its berries, which includes this species in the category of nutraceutical products. Additionally, the taxon provides ecosystem services in wild environments (Medina et al., 2005; Zapata et al., 2015).
Secondary metabolites, including flavonoids, play an important role in the physiology of these plants because they are synthesized in response to stress to defend against biotic and abiotic agents (Zakaryan et al., 2017). Dróżdż et al. (2017) found different phenolic compounds in the diversity of species of the genus Vaccinium, as well as in the different varieties, phenological stages and in the post-harvest of the berries. Vaccinium species are recognized as a functional food because its high content and structural diversity of secondary metabolites. They have an important content of phenolic compounds, flavonoids, and anthocyanins (Gaviria et al., 2012; Lopera et al., 2013; Maldonado et.al., 2018; Tian et al., 2017). Likewise, the previous authors, with Krikorian et al. (2010) and Liu et al. (2011), stated that these substances have beneficial effects on health; for their action at ocular level, against degenerative diseases; certain types of cancer; memory impairment; and protection of the cardiovascular system. Additionally, they act as reducing agents for donating hydrogen that inhibits singlet oxygen, metal ion chelators; preventing the formation of free radicals (Galleano et al., 2010; Ghasemzadeh and Ghasemzadeh, 2011).
Phenology is defined as the study of the periodic and repetitive phases or activities of the life cycle of plants, both in their development and in their growth, due to the diurnal and annual temporal variations (Cook et al., 2012). The knowledge of the phenology of plants is useful to identify critical periods where plants develop appropriate strategies to face the effect of biotic or abiotic factors, stressors or not (Valbuena et al., 2009). Phenology is useful to know the differences among plant’s genotypes and develop agronomic practices adjusted to plant’s requirements (Martínez-Adriano et al., 2016). Additionally, it helps to recognize the plasticity between plants and identify the different environments to which they have adapted (Harder and Johnson, 2005).
It must be considered that climate is the main factor controlling and regulating phenological events (Menzel et al., 2006) since plants are affected by environmental changes, within and between years, such as temperature, relative and soil humidity, nutrient availability, light and CO2 increase (Nord and Lynch, 2009; Nijlanda et al., 2014; Martínez-Adriano et al., 2016). The phenology responds to the climate for the following reasons: for gene flow to occur between individuals for the same population and to avoid damage due to unfavorable changes over time (Jianwu et al., 2016). Besides, to face this climatic and genetic variability, plants adopt different phenological strategies (Körner et al., 2016). Rainfall is generally considered as an environmental signal for the variation of phenological events in tropical regions (Morellato et al., 2013, 2006). It is also related to the interpretation of the variability of these phases and their events, which originates the adaptation of plants to diverse environments (Martínez-Adriano et al., 2013, 2016).
For certain species of the Vaccinium group, Antunes et al. (2008) suggested that the choice of cultivars is based on the identification of the species’ phenological phases. This description can allow obtaining a staggering production and an increase of the same in strategic periods of supply and demand of the fruit. Also, Kron et al. (2002), in a study of the phylogenetic relationships carried out with the tribe of blueberry species (Vaccineae, Ericaceae) concluded that in the genus Vaccinium there is not a very clear grouping among taxa from different continents, or between those of tropical and temperate climate origin. Also, these authors tend to recognize several small groups (clades), rather than a large set of Vaccinium species, which would be essentially redundant to the Vaccinieae tribe.
Studies carried out by Ligarreto et al. (2011) revealed a wide morphological variation in the metapopulation of V. meridionale by quantitative and qualitative factors of the species, highly influenced by the environment. There is also an important wild genetic resource for V. meridionale that could cement the introduction of this species in the agricultural world. In a commercial cultivation of blueberries in Guasca (Colombia), with the Biloxi and Sharpblue cultivars, follow-ups were advanced in batches of 20 and 36 months, where it was identified that this last clone presented a superior yield because of a greater number of fruits and an increase in total soluble solids (Cortés-Rojas et al., 2014).
For this species, information on phenological studies has been obtained, such as the one described by Gómez (2004), where certain development events are detailed; among them, the sprouting of leaves, fIoral button, open flower, flowering, fruiting, and green and ripe fruits. Other works describe six stages of maturity of the berries (Buitrago et al., 2015). The peasant communities of Guarne, Antioquia, have expressed that there occurs biannual fruiting, which is a product of the bimodal rainfall of this area. For the area of the Antilles, Berazaín (2006) has identified that flowering occurs from the beginning of winter in the Ericaceae family. This phenological phase extends throughout the spring, until the beginning of summer; likewise, fruiting lasts from the beginning of autumn, continues throughout the winter, with a maximum in the spring-summer period. These are plants with abundant flowering and fruiting throughout the year.
Consequently, because the mortiño belongs to a group of species of the genus Vaccinium, it presents phenological stages and phases similar to blueberries, but not evaluated in conditions of the high Andean zone. Therefore, the objective of developing this scale was designed to describe and visually identify in the stages already known, the phenological phases that natural populations present in climatic conditions similar to the high Andean area studied.
MATERIALS AND METHODS
Locality
The monitoring in the different phenological stages of the mortiño was carried out between 2008 - 2011, in five natural populations selected in the Departments of Antioquia (Santa Rosa de Osos and Medellín, township of Santa Elena), Cundinamarca (Guachetá) and Santander (California), whose geographic coordinates and climatic characteristics are detailed in Table 1. It should be noted that precipitation is bimodal in all locations, and they are located between 2400 and 2900 masl, except California (Santander), where a natural population was identified at almost 3500 m of altitude. These locations are characterized by fluctuating minimum temperatures between 7.0 and 13.2 °C, maximum temperature from 20 to 25 °C, and relative humidity between 43 and 91%.
Identification of the phases and phenological phases of the canopy
The categorization of the growth states of Vaccinium meridionale was based on the phenological scale of blueberries, Vaccinium corymbosum (Michigan State University, 2003), which describes and includes graphs on the development of foliar, floral, flower and fruit buttons. Additionally, a scale was constructed with the description of the phenological stages of this Andean species, through a photographic record and monthly observations for 26 months in the five natural populations previously described, and on 48 individuals, between 100 to 150 buds were marked randomly. The phases of development of the berries were identified based on the photographic scale achieved by Hernández et al. (2012).
RESULTS AND DISCUSSION
According to Halle et al. (1978), the mortiño presents a simplified branch, by abortion of the terminal buds at the end of each growth period. This model was called George Mangenot, which is initially orthotropic. Then, it leads to a plagiotropic development of the branches by replacing the lateral buds, which simultaneously show different phenological stages (Medina, 2010). Consequently, in this set of taxa, during the growth periods, reproductive and vegetative stems are observed simultaneously (Kawamura and Takeda, 2002).
The growth periods were continuous; so that in the dry season 75% of the structures were in the vegetative stage (VB), and the rainy season they increased up to 80% (Figure 1). On the other hand, in the dry season, 25% were reproductive structures, of which 15% were in the development of the inflorescence (ID), 7% were floral development (FD), and 8% were the development of the berries (BD). Besides, in the rainy season, the proportion of these was 20%, of which 6% was DI, 7% FD and 7% BD (Figure 2).
Figure 1 Percentage of mortiño’s structures in vegetative stage (VB) according to both dry and rainy seasons.
Figure 2 Percentage of moritño’s reproductive structures according to both dry and rainy seasons. BD: development of the berries; FD: floral development; ID: inflorescence.
The canopy of the Vaccinium has the property of being evergreen (Kawamura and Takeda, 2002), and to last all year long (Gómez, 2004); as foliage, its main characteristic is the predominance of mature leaves in all phases of tree development, which last around one to four years in tropical forests (Coley, 1988).
On the other hand, the role of leaves, besides carrying out the photosynthetic process, is the storage of nutrients and photo-assimilates and as a source of nutrients in the process of remobilization during senescence (Severino and Auld, 2013). It is also important to identify the period of foliage formation since this process has consequences in the interactions between plants and herbivores (Novotny et al., 2006); it is the case between the natural populations and the phytophagous insects where the present study was carried out.
For the mortiño, a detailed description of the evolution of the canopy is not known. In research carried out in the municipality of Guarne, Antioquia, it was found that the growth and development of the foliage are permanent. However, it increases up to a maximum in the rainy season and high relative humidity, which coincides with the decrease in flowering and the formation of new berries (Gómez, 2004); unlike the mortiño, cranberry in Chile has two marked periods in leaf development, one for induction of leaf shoots and another for vegetative development (Bañados et al., 2007).
Stages and phases of canopy development
Under the climatic conditions of this study (Table 1), the phenological development of mortiño’s canopy extended from the sprouting of the meristems, with the later formation of the vegetative structures until the maturity of the fruits. The first stage included the development of vegetative bud (VB) or foliar shoots and the formation of leaves and branches, which was subdivided into 5 phases. The second was related to the evolution of the inflorescence (ID), also distributed in 5 phases. In the third, floral development (FD) occurred, which extended into 5 phases. Finally, the berries were formed through 4 phases (BD).
Vegetative bud (VB) or foliar sprouts. The development phases of the vegetative buds originated from the point of non-visible growth (VB0), which is characterized by being dormant axillary buds (meristems) and ended with the formation of young buds (YB), not lignified, located in the terminal part of the branches (Figure 3). They do not possess dominant apical bud, with anthocyanin pigments in the leaves, very sensitive to the attack of foliage-eating insects and the damage caused by frost; from these young buds, reproductive shoots will be formed (Medina, 2010).
Figure 3 Stage of development of vegetative bud (VB) or foliar sprouts, where the leaves and branches are formed subdivided into 5 phases.
The growth phases of the VB were characterized by the budding of the lateral buds (VB1), which can reach up to 5 mm in length. The late green buds (VB2) expanded with the corresponding separation of the leaf blades that formed the buds. It continues with the bud’s expansion (VB3), leaves development, and the separation of the leaf blades present in the axils. Finally, they became young buds (YB), characterized by having non-leathery leaves, prominent elongation of the branch and leaves, and formation of other axillary buds that can be differentiated into vegetative or reproductive. YB leads to the senescence of the apical meristem; in some cases, anthocyanin pigments were present in the leaf blades from the VB3. Feng et al. (2017) and Mazza and Miniati (1993) stated that these secondary metabolites are important in plants because they serve as attractants, protect against ultraviolet rays. They are correlated with an increase in the concentration of them regarding altitude, are associated with resistance of pathogens, are enhancers of photosynthesis in plants of tropical forests, and they regulate gas exchange in woody plants.
In the southern hemisphere, in Vaccinium corymbosum L., Rivadeneira and Carlazara (2011) described four stages of growth of the vegetative buds: One with short internodes, later the lengthening of these and leaf expansion occurs. Finally, the branches are fully formed. The vegetative growth is usually by periods, and it stops to start the development of inflorescences and subsequently, the flowers (Bañados et al., 2007).
In other evergreen Vaccinium spp., as in the case of V. bracteatum, the branches do not necessarily grow every year (Kawamura and Takeda, 2002), an aspect that also occurs in V. meridionale. It may be affected by climatic events such as the global warming that has affected both the distribution of species and leaf senescence and reproduction (Menzel et al., 2006). The most critical factor that affects plant cycles for high-latitude areas is temperature. However, in the tropics, it is the periodicity between dry and rainy seasons (Mendoza et al., 2017).
Development of the inflorescence (ID). As seen in Figure 4, in this stage, the inflorescence develops. It extends from the budding of the floral bud (ID1) to a fully developed elongated structure (ID5), to start flowering later.
Figure 4 Stage of development of the inflorescence (ID) where the emergence of individual flowers occurs subdivided into 5 phases.
During inflorescence’s growth and development, the budding of the floral bud (ID1) occurred because of its hydration and swelling. Subsequently, the elongated and differentiated inflorescence was observed in the different floral structures (ID2); after which, the development of the buds (ID3) and all floral structures was triggered, causing the thickening of the bunches. Once this happened, the floral apices emerged (ID4), with the separation of the bracteoles and emergence of some flowers. In the fully developed inflorescence (ID5) appeared the separated flowers, whose bracteoles were in the process of opening with the corresponding emergence of individual flowers.
In other Vaccinium, it has been expressed that the periods of flowering and ripening of fruits may vary according to the year and the location (Antunes et al., 2008). In the zone of San Miguel de Sema (Boyacá), there are two periods of flowering, the first from February to April and the second from July to September; likewise, the individuals that bloom in each period are different (Chamorro, 2014). In V. corymbosum a swollen bud that will give rise to the flowers was described as the beginning of the inflorescence formation (Meyer and Prinsloo, 2003). These structures are bunches of simple lateral buds that are found in the ending part of the branch; an inflorescence is formed by a knot, but in thick buds, it can be up to two (Gil, 2006).
Floral development (FD). In this stage, the evolution of flower development was described. It elapses from fIorescence (FD1) to corollas fall, and the beginning of the berries formation (FD5).
During the floral development (FD) (Figure 5), the closed corollas were observed white with slight reddish tints and grouped in bunches (FD1). Later, the flowers separated from the main axis, and reddish tones appeared on the upper half of the floral apices (FD2). Then, the opening of some flowers of the bunches (FD3) began; followed by a number of open flowers in most of the inflorescences, whose apices are curved upwards (FD4). In the last phase, the fall of the senescent corollas was observed, whose rudimentary pistils remained adhered to the pedicel, and the green fruit exhibition occurred (FD5). Although, Chamorro (2014) described ten floral states that range from its opening to floral senescence, under the conditions of this research, only 5 phases were seen in the FD.
Figure 5 Stage of floral development (FD) subdivided into 5 phases, which end with the formation of the berries.
The flowers’ colors are signals given by plants to interact with pollinators and seed dispersers. In addition, another of these colors functions is the protection against abiotic stressors that could interfere with their signaling function to pollinate and disperse animals (Stournaras and Schaefer, 2017).
For the area of eastern Antioquia, Corantioquia (2003) reported that the mortiño flowers twice a year, from February to May and from August to November, which coincides with what was found in this research. According to Gómez (2004), the flowering coincides with the dry seasons and is inversely related to the foliage sprouting and expansion in this region. In San Miguel de Sema (Boyacá) and Guachetá (Cundinamarca), the presence of mortino’s blooms is identified between January to March and June to August (Chamorro and Nates-Parra, 2015). Studies conducted in Japan suggested that individuals with early blooms are disadvantaged by the availability of pollinators (Suzuki, 2002).
Regarding the flowering registered in the present study, it was observed that it occurred between February to May and August to November in Santa Elena (Antioquia), and from November to January and April to June in Santa Rosa de Osos (Antioquia). Likewise, from January to April and from June to August in Guachetá (Cundinamarca), and from March to May in California (Santander).
Development of berries (BD). The phases of this stage (Figure 6) were exhibited from the beginning of the fructification (BD1) to the harvest maturity of the berries (BD4). It began with the elongation of the green fruits (BD1) of variable size. Later, the berries began to develop anthocyanins (BD2), which were identified by their reddish coloration from the apical to the basal part of the fruit. They reached their physiological maturity when 25% of the bunch berries had developed reddish, anthocyanin colorations; covering 75 to 100% of the epicarp (BD3). This phase is considered by Hernández et al. (2012) as the state III of fruit development.
Figure 6 Stage of development of the berries (BD) subdivided into 4 phases, from the beginning of the fructification to the harvest. Adjusted by Hernández et al. (2012).
The last phenological phase is harvest maturity of the fruits (BD4), which is characterized by the purple color throughout the epicarp and indicates the appropriate time for collection and consumption. The harvest is carried out periodically in the months of production because of formation of the reproductive structures of this perennial plant. According to these ripeness states of the berry, Hernández et al. (2012) identified that the seeds increase their weight as they develop, and the BD4 phase is the most appropriate time for their extraction.
According to Maldonado et al. (2018) and Gaviria et al. (2012), the berries in BD4 have high anthocyanin content and antioxidant activity. They also have a content of total phenols and natural colors comparable or superior to other Vaccinium; therefore, it is a promising fruit for its production and sale as a nutraceutical source to develop functional foods, or for the fresh fruit market.
The fruit is a rounded-shape and fleshy berry of 8-14 mm, with peduncle of 1 cm long. The fruits are green in the immature state (BD1) and purple or black when ripe (BD4). In certain occasions, they are covered by a waxy layer, they conserve rudiments of the calyx in the apex, and they possess numerous small seeds (Toro, 2012). The size of the berries is also related to the increase of seeds per fruit (Retamales and Hancock, 2012). Fruiting occurs in eastern Antioquia in two main periods, from April to June and September to December (Corantioquia, 2003); however, Gómez (2004) found that in natural populations, fruiting occurred throughout the year, with percentages ranging from 17% to 39%.
Regarding the reproductive phase of this plant (FD and BD), Chamorro and Nates-Parra (2015), in Guachetá (Cundinamarca) and San Miguel de Sema (Boyacá), found that a bud develops completely when its flowers bloom, 18 days after beginning its formation and six days later the senescence of this organ occurs. However, Chamorro (2014) stated that the flowers’ duration was only six to ten days, which it is considered a long floral longevity characteristic of the Ericaceae family (Primack, 1985), and these are mechanisms to increase the attraction of pollinators. Rathcke (2003), Torres-Díaz et al. (2011), Chamorro (2014) and Chamorro and Nates-Parra (2015) found that the species produces a high quantity of flowers and low fruit production, which has been evidenced by selective abortion of self-pollinated fruits.
The growth stages in V. corymbosum were identified in leaves, inflorescences, flowers, and fruits. Thus, the development of the vegetative or foliar bud presented four phases, the floral button four, flowering five, and the development of the fruits five phases as well (Michigan State University, 2003). This scale served as the basis for the categorization of the growth stages of Vaccinium meridionale.
CONCLUSIONS
The growth periods were continuous, such that in the dry season the proportion of vegetative structures was 75% and the other 25% were reproductive organs distributed in the following proportions: 15% ID, 7% FD, 8% BD. In the rainy season, the vegetative organs reached 80% and 20% the reproductive organs, whose proportions were 6% ID, 7% FD and 7% BD. V. meriodionale Swartz expressed four phenological stages similar to V. corymbosum: development of vegetative buds, basic tissues for the formation of leaves and branches, development of the inflorescence, floral and berry development. Each of these stages was made up of five phases, except the last one that only exhibited four phases. The V. meridionale expressed a growth by continuous periods, in such a way that different vegetative and reproductive phases were appreciated, simultaneously. The phenological scale achieved in the five evaluated Colombian high Andean natural populations can be applied to other regions with similar climatic characteristics.
