Some ecophysiological characteristics of the higher altitude tropics

The Andean region offers growing conditions for numerous fruit species that may thrive up to 3,000 masl or more, whether they are frost-resistant crops or avoid frost during the flowering season or in recently set fruits (Fischer and Orduz-Rodríguez, 2012). For instance, in Colombia frost does not occur below 2,400 masl, and banana passion fruits are found up to an altitude of 3,200 masl (Angulo and Fischer, 1999). Solar radiation in the highlands encourages the thickening of the fruit epidermis and a greater number of parenchyma layers, and the high ultraviolet (UV) radiation results in a greater formation of antioxidants, factors that favor the quality of these fruits (Fischer et al., 2016; Fischer, 2000). Therefore, trellis systems (sistema de conducción or emparrado) are recommended in areas with excessive radiation (Fischer et al., 2009).

As thermal altitude classification confirms, temperature is the most influential climatic factor, which changes as altitude increases, with a decrease of about 0.6 °C per 100 m of elevation, mainly affecting the duration of growth cycles and the phenology of fruit trees (Fischer et al., 2009). Likewise, with an increase in altitude, the partial pressure of gases, such as O₂, CO₂ and N_2, and air humidity decrease, along with a reduction in precipitation, from the altitude of 1,300-1,500 m (Fischer and Orduz-Rodríguez, 2012). On the contrary, these authors indicated that ultraviolet, visible, and infrared radiation increase with altitude, along with wind speed.

The leaf thickness increases, and the leaves become smaller when exposed to the UV light, which may be due to the stress caused by increasing altitude (Fischer et al., 2016). In addition, UV radiation affects the production of auxins (Fischer and Melgarejo, 2014). Buchanan et al. (2015) stated that UV light causes a lower synthesis of gibberellins in internodes, which means that high- altitude fruit trees reduce the longitudinal growth of the stem, compared to plants in the lower areas.

Passifloraceae

Rodríguez et al. (2020a) and Ocampo et al. (2021) reported that South America is the center of diversity for most cultivated Passiflora species. The high biodiversity of Passiflora in South America puts the continent as a region of great potential for utilization of these species (Hurtado-Salazar et al., 2021). There are about 520 species of passion flowers, and approximately 96% of these are distributed in the Americas, being Colombia and Brazil the centers of the diversity with 30% (Cerqueira-Silva et al., 2014). These species include herbaceous and woody vines, usually with tendrils, and a few are shrubs or trees (Ocampo et al., 2021). The species of this family are native to tropical and subtropical regions of both hemispheres and grow in low- and high-altitude habitats, where temperatures are moderate (Paull and Duarte, 2012). Ocampo et al. (2007) stated that the passion fruit plants are originated in the edges of humid forests in tropical valleys, with 20 to 30 °C average air temperature and high environmental humidity and precipitation rates but these conditions does not appear, in all cases, to be optimal for growth and production (Hurtado-Salazar et al., 2021). These are semi-perennial fruit-bearing species of a climbing habit (Primot et al., 2005).

This family, given its permanent production in the interior tropics because of its indeterminate growth habit, requires well-distributed rainfall throughout the year (Fischer et al., 2018). Jackson et al. (2010) recommended areas that are not too cold for these species, with high solar brightness and winds that are not strong. However, as these authors pointed out, regions with very hot summers decrease crop longevity, and frost below -2 °C causes severe damage to plants.

Colombia has the greatest diversity of passion fruit species (Ocampo et al., 2007), where nine species are cultivated to meet the needs of local markets and export demands (Ligarreto, 2012), with greater production in the departments of Antioquia and Huila, especially for yellow passion fruit, sweet granadilla and gulupa (Fischer et al., 2018). The species requirements for altitude and temperature vary widely. The banana passion fruit plants are well-adapted to the cold climate (Table 1).

Table 1: Origin of four important passion fruit trees cultivated in the Andean region.

In addition to these four commercially important passion fruits, Colombia has other species of great importance, such as giant granadilla "badea" (P. quadrangularis) and stone granadilla "cholupa" (P. maliformis) (Rodríguez et al., 2020b).

Yellow passion fruit

The most cultivated and well-known passion fruit species is the yellow passion fruit (Passiflora edulis f. flavicarpa Degener), also known as acid passion fruit; it is a product of great commercial and economic importance in Brazil, thanks to the quality of its fruits and its high industrial yield (Faleiro et al., 2020). It can be cultivated between 0-1,300 masl (Table 1), according to Fischer et al. (2009), it is the most tropical passion fruit with better adaptation to the lower marginal zone of the coffee region in Colombia.

The yellow passion fruit grows optimally in temperatures between 23 and 25 °C, while in regions with temperatures below 15 °C and a photoperiod with less than 11 h light per day, there is little flowering stimulation (Faleiro et al., 2020) (Table 2). Regions with average temperatures higher than 28 °C, accelerate vegetative growth but with a reduction in production because of dehydration of the stigmatic fluid (Fischer et al., 2009). Cleves (2012) recommended a minimum of 5 h of direct sunlight on plantations and highlighted that fruits directly exposed to the sun have a higher concentration of ascorbic acid and total soluble solids, with a thinner rind, however, growers always have to avoid sunburn damage.

Table 2: Climatic factors for the growth and production of passion fruits in Colombia (modified according to Fischer et al., 2018)

Relative humidity below 30% reduces pollination and fruit development (Faleiro et al., 2020); these very dry conditions inhibit photosynthesis by closing stomata and burning the tender shoots of plants (Fischer et al., 2009). Faria et al. (2020) irrigated yellow passion fruit seedlings with 25, 50, 75 and 100% of the capacity of the pot substrate, and found that, in 50%, the plant height and the stem diameter were very similar to those plants with greater amounts of water (up to 175%) and stated that the plants possibly have water reserves in the stem and roots. Likewise, these authors observed that the number of leaves, the transpiration and the biomass of the plants constantly increased up to 100% of the capacity of the pot substrate.

Yellow passion fruit plants do not tolerate waterlogging for more than four days, which especially affects roots and stem growth (Basso et al., 2019). As shown in Table 3, flooded yellow passion fruits increase the relative water content, but the photosynthetic and transpiration rates decrease, along with the stomatal conductance (Govêa et al., 2018; Faria et al., 2020). Nonetheless, because of the formation of an aerenchyma in the cortex of flooded plants (Govêa et al., 2018), passion fruits have mechanisms of adaptation to higher humidity conditions in the root environment for a time; thus, Faria et al. (2020) classified this fruit as moderately sensitive to water excess in the soil.

Table 3: Effect of waterlogging on the physiological response of yellow and purple passion fruits.

Sweet granadilla

In Colombia, the sweet granadilla crop (Passiflora ligularis Juss.) is the second one in species of the genus Passiflora because of its economic importance (Ocampo et al., 2015). It adapts well to elevations between 1,800 and 2,600 masl, with optimal temperatures between 18 and 20 °C (Table 1) (Miranda, 2020). Temperatures higher than 23 °C cause thermal stress, and those between 15 and 18 °C increase the duration of the production cycle but decrease the productivity (Miranda, 2012). As this author affirmed, there are problems with temperatures below this range, namely those between 12 and 15 °C, which increase the abortion of flowers, reduce fecundation, and cause cracking of recent set fruits. Rivera et al. (2002) reported that below 1,800 masl, the incidence of insect-pests increases, and smaller fruits develop. Also, below 1,500 masl, the viability of pollen is low.

In the municipality of Santa María, Department of Huila (Colombia), Fernández et al. (2014) ecophysiologically characterized sweet granadilla in situ at 2,060 masl (average temperature 17.15 °C, PAR (photosynthetic active radiation) 1,186.2 μmol photons m^-2 s^-1) and at 2,270 masl (16.24 °C, PAR 470.9 μmol photons m^-2 s^-1). At 2,060 masl, the maximum photosynthetic rate (A_max) 23.6 μmol m^-2 s^-1 of CO₂, the darkness respiration rate (DR) 2.24 μmol m^-2 s^-1 of CO₂ , and the compensation point per light (I_c) 34.6 μmol m^-2 s^-1, were higher than at 2,270 masl (17.5 A_max; 1.34 DR and an I_c of 21, respectively), while for the two locations, the foliar water potential (about -0.2 MPa), the edaphic one (about -0.01 MPa) and the predawn values of maximum photochemical efficiency of photosystem II (Fv/Fm; >0.86) indicated that the plants did not suffer any stress, concluding that both sites are suitable for the commercial cultivation of sweet granadilla (Fernández et al., 2014).

Among the physiological disorders of sweet granadilla, sunburn is the most important physiopathy, caused by excess solar radiation in fruits unprotected by leaves, accentuated after pruning of branches in the fruitful part of the plant or by a drought that also reduces the leaf area (Rivera et al., 2002). Fruit cracking is a physiopathy related to sudden changes in day to night temperature but can also be caused by a high Ca deficiency (Miranda, 2020), irrigation or a heavy rain after a prolonged dry season that increases the senescence of the epidermis and its extensibility (Fischer and Orduz-Rodríguez, 2012).

Regarding the water factor, a commercial sweet granadilla plantation requires rainfall between 1,500 and 2,500 mm year^-1 and an atmospheric humidity of 60 to 80%, which favors the activity of pollinators, while higher humidity increases the incidence of fungal pathogens (Rivera et al., 2002; Miranda, 2020). As in other passion fruit species, water stress in the reproductive stages, from the pre-flowering stage to the filling of the fruit, causes the abscission of the floral structures and considerably reduces yield (Miranda, 2020). Likewise, this detrimental effect in the reproductive phase is related to the deficiency of nutrients, such as P, K, Ca and B. Under a moderate water stress in sweet granadilla plants generated a decrease in leaf area, number of leaves and longitudinal growth of branches, while the root/aerial ratio of the plants increased with the duration of water stress (Casierra-Posada and Roa, 2006).

According to Table 2, the light in a technical cultivation of sweet granadilla requires 1,500 to 1,600 h year^-1 of sunshine (Miranda, 2020) because this luminosity highly encourages the differentiation of floral primordia, flowering and fruit coloration (Miranda, 2009).

On the other hand, excessive winds are detrimental to this passion fruit species since they affect pollination agents, bees and bumblebees, and can damage flowers and pollen germination as a result of drying of the stigmatic surface, while calm environments ensure better fruit set (Miranda, 2009).

Purple passion fruit

While Blancke (2016) confirmed that the purple passion fruit (Passiflora edulis f. edulis) is cultivated not only in the subtropics but also in high Andean areas, in Colombia, Ocampo et al. (2020) reported that crops are found from 1,600 to 2,300 masl, avoiding very steep slopes, with the best results in terms of production and quality found in areas from 1,700 to 2,000 masl. Ocampo and Posada (2012) specified this as the optimal range to develop good genetic vigor, good pollination and fecundation, and low incidence of pests and diseases. Interestingly, Rodríguez et al. (2019), who studied 50 purple passion fruit genotypes at two different altitudinal locations, Pasca (Cundinamerca, 1,800 masl, 18 °C) and Susacón (Boyacá, 2,500 masl, 13.1 °C), found that the 34 landraces had a better adaptive physiological response at the higher altitude than the commercial genotypes, which is because they are more suitable for plant breeding programs in the current climate change scenario. Carr (2013) observed that the purple passion fruit can be cultivated up to 3,000 masl in the tropics.

Optimal temperatures for purple passion fruits are in the range of 15-22 °C day and 12-14 °C night (Table 2) (Pérez and Melgarejo, 2012), tolerating temperatures ranging between 10 and 24 °C (Ocampo et al., 2020). In their ecophysiological study at three different locations in Cundinamarca (Colombia), Pérez and Melgarejo (2015) concluded that climatic conditions similar to those in the municipality of Granada (2,230 masl, 15 °C), which has a day/night temperature of 18/13 °C, a vapor pressure deficit close to 0.05 kPa and radiation that does not exceed 1,000 μmol photons m^-2 s^-1, greatly favor the physiological performance of purple passion fruits. Temperatures over 30/25 °C day/night affect flower production (Jiménez et al., 2012); adult plants resist low temperatures but can be damaged by temperatures between -1 and -2 °C (Paull and Duarte, 2012).

Sunlight from 7 to 9 h day^-1 favors fruit quality (Pérez and Melgarejo, 2012), while Ocampo and Posada (2012) stated that excessive cloudiness during fruiting delays ripening, and decreases the content of soluble solids (° Brix) and the quality of the juice. The purple passion fruit is very susceptible to changes in solar radiation because they affect the productivity of plants; thus, cloudy days decrease growth, induction of flower buds and flower opening. A reduction of light of 1-4 weeks decreases flowering and plant production. Besides, an excess radiation generates sunburning on fruits and decreases normal plant development (Jiménez et al., 2012).

Ocampo et al. (2020) recommended relative humidity (RH) between 60 and 70% for cultivation, which sustains effective pollination and fecundation, so the stigmas remain hydrated and adhesive. Rain during flowering affects the functionality of pollen because it can burst and cause abscission of flowers (Jiménez et al., 2012). Carr (2013) reported that rain up to 2 h after pollination prevents fruit set. Sánchez et al. (2013) found a negative correlation between RH and stomatal opening on a purple passion fruit plantation, but positive correlations between solar radiation and temperature with stomatal opening.

According to Ocampo et al. (2020), well-distributed rainfall between 1,800 and 2,300 mm year^-1, is favorable for the growth and production of the purple passion fruit, while for the reproductive phases, i.e. between the sprouting of flower buds and fruit enlargement, water stress causes very small fruits or aborted fruits (Jiménez et al., 2012). Paull and Duarte (2012) reported that a water stress less than -1.3 MPa leads to a strong reduction in the development of the foliar area, flowering and plant yield, pointing out that the lack of water can be one of the environmental factors responsible for production fluctuations in these passion fruits.

In another purple passion fruit maypop (P. incarnata), García-Castro et al. (2017) found a moderate tolerance to short water deficit periods because of its stomatal mechanism and other non-stomatal factors (up to 10% of evapotranspiration, ET), with an exponential reduction in the photosynthetic rate with a water stress more negative than -1.0 MPa; however, the plants quickly recovered their gas exchange properties when they were irrigated again at 100% ET. Also, Crane et al. (2019) classified passion fruits as moderately water-stress tolerant plants that can withstand this stress for several days but with reduced plant growth and yield. Carr (2013) observed that the production of new leaves ceases at a leaf water potential -2.0 MPa, and the expansion of new leaves is considerably reduced to -1.5 MPa in P. edulis.

In general, the purple passion fruit, like the other passion fruits, does not resist periods of waterlogging (Crane et al., 2019); however, Chebet et al. (2020) found that mycorrhized plants (with a mixture of Glomus caledonium, G. etunicatum, Gigaspora magarita and Scutellospora sp.) better tolerate this adversity, producing more osmoprotectant proline and chlorophyll and thus, retaining their leaves and foliar N and P for longer than non-mycorrhized ones (Table 3).

Strong winds affect pollinating insects, which do not fly at high wind speeds (Fischer and Orduz-Rodríguez, 2012) and can damage flower structures and dehydrate pollen and stigma, along with damage to plantations and conduction systems (Ocampo et al., 2020).

Banana passion fruit

The banana passion fruit (Passiflora mollissima f. tripartita) is favored by altitude because UV radiation promotes the thickness of the epidermis, increasing resistance to diseases, mainly anthracnose (Campos and Quintero, 2012). There are commercial plantations between 1,800 and 3,200 masl in Colombia (Fischer et al., 2020), with the best conditions between 2,000 and 3,000 masl (Angulo, 2003). In countries such as Bolivia and Peru, there is cultivation up to 3,300 and 3,400 masl (Blancke, 2016; National Research Council, 1989). Mayorga et al. (2020) studied banana passion fruits at altitudes of 2,498 and 2,006 m in Pasca (Cundinamarca, Colombia), observing that, in the higher altitude, larger fruits were formed, with higher levels of citric and ascorbic acid but with less total soluble solids (°Brix), and recorded temperature and photosynthetic active radiation (PAR) as the climatic factors that exerted the greatest effect on plant development. To resist large fluctuations in temperature and high radiation (UV) in high Andean zones, plants develop soft hairs on the entire vegetative part (Angulo and Fischer, 1999). Sunlight between 1,300 and 1,600 h year^-1 are necessary to guarantee favorable growth and production conditions for plants (Angulo, 2003).

This species is the commercial passion fruit most adapted to cold tropical and subtropical regions (Blancke, 2016). Mayorga et al. (2020) established the base (minimum) temperatures for the growth of primary branches, flower buds and fruits as 4.3, 3.1 and 0.01 °C, respectively. Zones with temperatures between 13 and 16 °C are recommended for cultivation, but temperatures below 0 °C can affect flower buds, flowers, fruit set and non-lignified vegetative parts of the plant (Campos and Quintero, 2012). Given that this fruit grows at altitudes higher than the frost limit, P. mollissima f. tripartita lines have formed tolerance to temperatures of -5 °C for a short time (National Research Council, 1989).

Rainfall of 1,000 to 1,500 mm year^-1, well-distributed throughout the year, is optimal for commercial crops (Fischer et al., 2009); therefore, supplying moisture in dry periods with artificial irrigation is necessary, especially in the reproductive phases. Climatic events such as prolonged rain (waterlogging), intense droughts and hail can affect the cultivation and production of plants (Fischer et al., 2020). Campos and Quintero (2012) recommended a relative humidity between 70 to 80%, which favors pollination and pollen germination; considering that drier airs increase the risk of frost in the high Andean zone, while a higher atmospheric humidity benefits some diseases, especially anthracnose. Light winds facilitate the transport of pollen through the air and the flight of pollinating insects, which are necessary since the banana passion fruit is an allogamous plant. Strong winds must be controlled by planting windbreak barriers using native plants (Fischer et al., 2020) that also protect against flower fall (Angulo, 2003).

The cultivation of passion fruit plants in Colombia reveals a positive impact of plastic roofing oriented over the plant rows with a PE plastic (175 µm thickness) 1.50 m wide, which is placed on a "T" type structure located at 2.2 m above the ground. This structure protects the plants from heavy rains and direct solar radiation and regulates the circulation of air inside the canopy, reducing relative humidity. These factors improve the production and quality of the fruits and contribute to reduce the incidence of critical fungal diseases, such as Alternaria sp. and Cladosporium sp. Nevertheless, the use of this technique is still scarcely reported since it is necessary to carry out physiological studies of these crops that explain the variables of yield and quality of the fruit production.