1.
Introduction
The Cape gooseberry (Physalis peruviana L) is a cold-climate plant that grows in Colombia, where it may be found at elevations ranging from 1800 to 2800 meters above sea level [1]. In 2022, the harvested area was 1514.69 hectares, with a production of 20,430.86 tons and an average yield of 10.61 hectares per ton. The Department of Boyacá had the highest production in 2022, with 6589.37 tons, which is equivalent to 33.68% of the national area [2].
The exports of this fruit were valued at US 35,678,351 FOB (Free on Board), especially in European markets such as Namur, Belgium, which consider them exotic (57.6%) and value its flavor (52%). Between 2016 and 2020, exports increased by 9.1% per year to a net amount of 50,865.7 tons [3,4]. Analdex has also recorded an increasing trend, showing that the Netherlands, USA, and Germany have been the main destinies for the exportation of Cape gooseberry, with an average percentage of exportation of 70.7%, 10.9%, and 6.4%, respectively. Between 2020 and 2021, the total amount of metric tons increased by 1.2% [5]. Those values illustrate the significant importance of seeking strategies for the conservation of fruit from Colombia to Europe and North America.
On the other hand, cape gooseberries exhibit a high nutritional content, including protein (1.88–2.54 g/100 g), lipids (0.25–1.01 g/100 g), carbohydrates (10.23–14.13 g/100 g), carotenoids (13.91–22.36 μg/g), potassium (4043.56–4876.88 mg/kg), iron (7.60–20.91 mg/kg), and magnesium (91.42–455.53 mg/kg). These values were particularly observed in fruits originating from Colombia, as reported by Petkova & Popova [6]. These compounds may be responsible for the health advantages attributed to them.
Post-harvest losses, which account for 21% of all losses, are the main limiting factor in storage and spoilage by microorganisms such as Cladosporium, Phomopsis, Pestalotia, Botrytis cinerea, and Alternaria spp. [7]. To resolve this issue, a post-harvest strategy should integrate physical methods, which include dehydration, temperature, electricity techniques, and UV-C treatment, chemical treatments, namely fungicides often combined as co-formulations such as calcium chloride or calcium nitrate, and biological treatments, which have been implemented by introducing microbial antagonists such as bacterial or fungal species to control diseases [8].
Regarding chemical treatments, chlorine is the most common chemical sanitizer, mainly due to being the cheapest. The oxidation reaction contributes to pathogen inactivation, with maximum action occurring at a pH from 5 to 7, below the pH of 7.5 of HOCl. The Food and Agricultural Organization (FAO) advised free chlorine doses of 500–200 ppm as Cl2 for exposure times between 2 and 10 s to control bacteria such as Salmonella and E. coli [9].
However, some forms of chlorine might not be ideal for vegetal material. Therefore, in this paper, the analyses will be conducted using calcium chloride, which helps preserve quality by controlling physiological disturbances and potentially reducing the respiratory rate and ethylene release rate during post-harvest [10]. For example, studies like Pinzón et al. [11] evaluated the effect of calcium chloride at concentrations of 1% and 2% (w/v) on Cape gooseberry, administering it directly to the solution, both to the fruit and the calyx in pre-harvest, and monitored its effects weekly for a month following harvest. Calcium slowed the ripening of fruit, affecting both physical (diameter, hardness, and color) and chemical characteristics (total soluble solids, total acidity, and calcium content of the fruit). Besides, treatments with CaCl2 showed delayed ripening by inhibiting the activity of enzymes and genes related to cell wall degradation and ethylene signal transduction [12].
Based on this knowledge, the current study was designed to determine the effect of applying calcium hypochlorite and calcium chloride on Cape gooseberries without calyx at a medium stage of maturity, followed by refrigeration at 10 ℃ and 5 ℃. For 30 days, the quality of Cape gooseberry was monitored every 10 days.
2.
Materials and methods
2.1. Vegetal material
Agrosavia provided the Corpoica Andina variety of Cape gooseberry, which was grown in the Department of Cundinamarca of the Tibaitatá Research Centre, located in the municipality of Mosquera (Latitude 4.69541°), at an altitude of 2.516 m above sea level, with an average temperature of 14 ℃. According to Colombian Technical Standard 4580, Cape gooseberries were selected at maturity stages (MS) 3 and 4, removing any fruit with quality defects such as cracks, cuts, bruises, microbiological damage, and dehydration [13].
2.2. Sodium hypochlorite and calcium chloride treatments
After removing the calyx, the selected cape gooseberries were immersed in a sodium chloride solution or calcium chloride 300 ppm solution for 2 min. The disinfected Cape gooseberries were stored in 100 g of polyethylene terephthalate (PET) boxes for 30 days at 5 ℃ and 10 ℃. Cape gooseberries were stored in PET packages at 18 ℃ as a control (room temperature).
2.3. Physical analysis
The polar diameter (PD) and equatorial diameter (ED) of the fruit were measured with a digital caliper (Caliper, Bogotá, Colombia). Weight loss was monitored with an analytical balance (Pioneer, Bogotá, Colombia) to evaluate the weight of the fruit throughout storage. Firmness was determined whit a texturometer (Chatillon digital DFIS-50, Florida, United States) by counting ten fruits per replicate, performing compression tests with a 10.92 mm plunger plate, and descending at a speed of 60 mm/min. The outcome was given in kgf.
2.4. Physicochemical analysis
Ten fruits were taken for each replicate. They were macerated to extract the juice, and their volume was calculated and filtered. An aliquot was taken and placed in an ATAGO PAL1 digital refractometer to determine the soluble solids content (SSC) expressed in °Bx. The pH of the juice was determined using a potentiometer, and the acidity was determined using the titration method with NaOH 0.1N, 5 mL sample, expressing it as percent citric acid, using the following equation [14].
Where, TA = titratable acidity, V = volume of 0.1 N NaOH used in the titration, N = normality of NaOH (0.1 N), F = milliequivalent acid factor 0.064 per citric acid, and Vs = volume of the sample to be evaluated.
2.5. Statistical analysis
The statistical model corresponded to that of a completely randomized experimental design. The variation factors were two pre-treatments before storage (sodium hypochlorite and calcium chloride), storage temperature (5, 10, and 18 ℃), and storage time (10, 20, and 30 days). The response variables were weight, polar and equatorial diameter, firmness, SSC, acidity, and pH. All samples were analyzed in triplicate.
The results of the completely randomized design with factorial arrangement were analyzed using tools such as ANOVA, with a confidence level of p < 0.05, mean values (n = 3), and standard deviation. This analysis was carried out using the statistical software StatGraphics Plus version 5.1.
3.
Results and discussion
3.1. Physical change
During storage, fruits remained in good condition, with no rot damage. Statistical analysis (Table 1) showed significant differences in Cape gooseberry equatorial diameter (p < 0.05) due to temperature, time, and their interaction, but not pre-treatment, as shown in Figure 1.
Differences were most noticeable after 30 days of storage at 5 ℃ (Figure 1), where the fruit diameter was preserved, unlike at higher temperatures that changed the fruit diameter; this may be a consequence of water decrease due to processes related to transpiration [15].
Statistical analysis showed a statistically significant (p < 0.05) effect on Cape gooseberry weight loss: Low temperatures reduced weight loss, while storage time increased weight loss, as shown in Figure 2a. According to Figure 2b, pre-treatments of Cape gooseberry with hypochlorite and chloride resulted in a higher weight loss than the control. There was a size reduction, which can be correlated with the change in equatorial diameter explained by the respiration processes, where biological factors such as transpiration cause the evaporation of water from the fruit tissue, causing direct quantitative losses such as loss of saleable weight, loss in appearance such as wilting, and loss in texture such as softening.
As previously stated, the fruit consumes the carbohydrate and lipid reserves present in the cellular tissues, resulting in a size reduction [1]. The results revealed that the greatest change occurred between day 20 and possibly day 30 when the fruit had already progressed from the ripening stage to senescence, likely due to depleted food reserves.
On the other hand, fruit firmness was affected by all pre-treatments and time, their interaction, and the temperature–pre-treatment interaction (p < 0.05). Figure 3 represents the effect of pre-treatment and temperature on the firmness of Cape gooseberries during storage, demonstrating how a pre-treatment with sodium hypochlorite and storage at 18 ℃ preserved their firmness (0.424 kgf) after 30 days of storage, compared to cape gooseberries without pre-treatment and storage at 5 ℃.
Concerning time, the fruits lost firmness after 20 days of storage (0.397 ± 0.004 kgf compared with 0.4220 ± 0.004 kgf at day 0). These results might be explained by the enzymatic activity: Storage at 18 ℃ with hypochlorite pre-treatment is most efficient in decreasing pectinolytic enzyme activities, which are responsible for degrading the cell wall, especially in the ripening process [16,17]; fruits stored at 5 ℃ reduced in size the least, which can be explained by the significant effect of temperature on respiration rate [18]. In terms of firmness, the treatment made a significant but somewhat perplexing difference; calcium treatment was expected to confer stabilization of the cell membrane and cell wall and increase rigidity due to the binding of calcium to free carboxyl groups of polygalacturonate polymer [19].
The concentration used may have been insufficient to reduce ethylene release, which triggers the vast majority of ripening processes. Among these are polygalacturonase activation and xyloglucosyltransferase/endohydrolase (XTH) activity, which is found in the epidermis and has been linked to fruit softening. As a result, the effect of calcium on ethylene release may have been greater than on cell walls and cuticle binding to pectin, allowing the ripening process of Cape gooseberries to continue. On the other hand, studies on tomatoes have shown that proteins play a determinant role in fruit firmness and are dependent on the degree of maturity [20].
The pre-treatment had the opposite effect on weight loss. Based on the results thus far, we can conclude that the treatments had no positive effect on the preservation of the fruits' quality. This could be due to the loss of the fruit's natural wax, which was removed during immersion in both the hypochlorite and calcium chloride solutions. This wax can exert a barrier effect on both moisture loss and gas exchange during respiration, reducing the respiration rate and thus reducing spoilage factors.
It is important to note that the cell wall degradation processes produce a variety of metabolites, primarily monosaccharides [21], which increase the total soluble solids content. Sugar accumulation typically occurs at the end of the growth stage and the start of ripening, coinciding with the loss of soluble acid invertase activity [22].
Sugars account for 70%–80% of total soluble solids in ripe fruit, and they are formed primarily before the fruit development process is complete. Throughout the ripening process, soluble solids content (SSC) increases in some fruits but not in others. However, in the case of Cape gooseberry, which is a climate-sensitive fruit, the process of starch splitting continues during storage. As a result, the sugars tend to increase, improving the fruit's organoleptic properties, but they are also used as a carbon source during respiration, alongside organic acids. As a result, the balance between generation and consumption determines its dynamic during storage [21,23].
3.2. Evaluation of physicochemical changes
Figure 4a shows that temperature was the most influential factor determining SSC, which increased for the first ten days and then decreased, except for Cape gooseberries stored at 5 ℃, where SSC increased until day 30. The pre-treatments showed no significant differences. However, the temperature–pre-treatment interaction was significant, with calcium chloride pre-treatment and storage at 5 ℃ producing the highest SSC (13.2 °Bx) after 30 days. SSC values for Cape gooseberry stored at 10 ℃, regardless of treatment (Figure 4b), were similar (12–12.2 °Bx).
Therefore, storage at 5 ℃ allowed a balance between starch breakdown and the consumption of sugars and lipids to maintain the biochemical processes involved in ripening. Pre-treatments revealed that Cape gooseberries treated with calcium chloride and stored at 5 ℃ had the highest SSC. Sugar's role in the activity of enzymes like invertase in the cell wall can affect both cell wall structure and cuticle [21].
At 5 ℃, the metabolic activities related to respiration in the fruit might have been decelerated, leading to a slower breakdown of sugars to produce energy. This slower metabolic rate, combined with dehydration processes, as evidenced by changes in the equatorial diameter (ED) (Figure 1), could have contributed to the observed increase in SSC. Conversely, fruits stored at 18 ℃ exhibited the lowest ED, indicating greater moisture loss to the environment, which likely influenced the positive change in SSC.
Fruits stored at 18 ℃ tended to continue ripening, converting starches into sugars to utilize them as an energy source. Consequently, there was a near-equilibrium between the sugars released from starches and those consumed by respiration [24]. On the other hand, at a temperature of 10 ℃, the degradation of sugars occurred more rapidly than the conversion of starches into sugars, resulting in a slight reduction in available sugars [25]. This behavior can have significant implications for the quality and flavor of fruit stored at different temperatures, as well as its shelf life and suitability for human consumption.
The data obtained in this study are similar to those obtained by Pinzón et al. [11] during an experiment regarding the behavior of the Cape gooseberry fruit, Physalis peruviana L., at different storage temperatures. Researchers found that the control treatment at 20 ℃ produced a maximum of 17.3 ± 0.96 °Bx, while the 2 and 4 ℃ treatments produced maximum values of 14.5 ± 0.40 °Bx and 15.8 ± 0.46 °Bx, respectively. As a result of the low temperature, the fruit's respiratory rate was reduced.
The data depicted in Figure 4b indicate that, in addition to the impact of low temperatures, the application of CaCl2 treatments led to an increase in SSC. This effect aligns with previous research indicating that CaCl2 can mitigate the respiration process, thereby slowing down fruit ripening [26]. Our study further elucidated that the combined effect of calcium chloride treatment and a temperature of 5 ℃ promoted an augmentation in SSC levels within the fruit. Understanding these interactions is pivotal for optimizing fruit preservation methods and enhancing overall fruit quality during storage.
Table 1 shows the degrees of freedom, T value, which describes the relationship between a sample and its population, and the probability value for the parameters equatorial diameter, firmness, polar diameter, weight loss, soluble solids content, and total acidity for the different treatments regarding preservation method, temperature, time, and the interactions pre-treatment vs. temperature, pre-treatment vs. time, and temperature vs. time. As shown in Table 1, pre-treatment vs. temperature was significant for firmness, SSC, and AT (Table 2A, Table 2B). Pre-treatment vs. time was significant for weight loss (Table 3), and temperature vs. time was significant for polar diameter, equatorial diameter, soluble solids, acidity, and weight loss (Table 4A, 4B).
3.3. Cape gooseberry pH
Temperature, time, and their interaction contributed significantly (p < 0.05) to the change in Cape gooseberry pH. According to Figure 5, the pH of cape gooseberries stored at 18 ℃ increased from 3.76 to 4.12 at the end of day 30, whereas Cape gooseberries maintained at 10 and 5 ℃ ended with a pH of 3.9 and 3.8, respectively.
Cape gooseberry fruits, and all fruits in general, become less acidic over time as a result of the use of organic acids as a respiratory substrate and carbon skeletons for the synthesis of new compounds during ripening [27]. As we have seen in this paper, Cape gooseberry has the behavior of a climacteric fruit; hence, fruits stored at least at 10 ℃ do not show any change because the respiratory process stops.
The findings of this study are similar to those of Olivares-Tenorio et al. [28], who discovered an increase in pH in Cape gooseberry, obtaining maximum values of 4.7 after 76 d at 12 ℃. The authors explained that the trend was caused by the Cape gooseberry having the behavior of climacteric fruits.
However, this paper shows that, although the increase in ascorbic acid could start at the first moment of post-harvest at 12 ℃, such an increase only happened on day 44. After this, the compound started to decrease, which could be due to the oxidation process, which explains the behavior of the pH at 5 and 10 ℃.
3.4. Titratable acidity
The fruits remained in good condition, with no rot damage. Statistical analysis (Table 1) showed significant differences in Cape gooseberry equatorial diameter (p < 0.05) due to temperature, time, and their interaction, but not pre-treatment. The differences were most noticeable after 30 days of storage at 5 ℃, where the fruit diameter was preserved, unlike at higher temperatures that changed the fruit diameters; this may be a consequence of the decrease in water due to processes related to transpiration [15].
The findings revealed that the acidity of cape gooseberry was affected by time, temperature, and their interaction; therefore, significant differences (p < 0.05) were found in the fruit stored at 18 ℃ at 20 and 30 days of storage.
According to Figure 6a, acidity decreased with time, and the effect of temperature was observed after 20 days of storage. The lowest acidity values were found in fruits stored at 18 ℃ for 20 days (1.23%) and after 30 days (1.12%). On the other hand, Cape gooseberry pre-treated with hypochlorite was the only one whose acidity was affected by storage temperature (Figure 6b). The highest values were found in Cape gooseberries stored at 5 ℃ (1.96%), while the lowest value was observed in Cape gooseberries stored at 18 ℃ (1.21%).
As already seen in pH changes, acidity decreases as the ripening process progresses because organic acids are used as substrates during respiration; another compound like ascorbic acid might degrade due to oxidation processes. Bravo et al. [29] investigated genotype effects at two different harvest times. Fruits were stored for 18 h at 4 ℃; before analysis, the average TA was 1.88% ± 0.39%. A similar result is found in the findings of this paper; they concluded that ripening processes are one of the main factors in the change of this variable.
Previous works have also shown that the chemical agent does not play a very important role in the change of titratable acidity; instead, the factor that most affects acidity is high temperature, due to its utilization in the hydrolysis of polysaccharides and non-reducing sugars [30]. On the other hand, fruits were kept at a low temperature, causing the acidity to increase, possibly due to an adaptation of the metabolism at 5 ℃ and 10 ℃ [31]. The acidity was 1.36% ± 0.065% at 18 ℃ with the calcium chloride treatment, which was below the range due to a decrease in respiratory activity caused by an increase in calcium in the fruit cells, causing a blockage of the conversion of organic acids [32].
4.
Conclusions
Temperature and time are the two factors that most influence the quality and physicochemical properties such as polar diameter, equatorial diameter, soluble solids content, acidity, and weight loss of the Andean variety of Cape gooseberries. The interaction between storage method and temperature had a significant influence on firmness, soluble solids content, and total acidity. The interaction between storage method and time had a significant influence on firmness, soluble solids content, and total acidity. The interaction between storage method and time had a significant influence on Cape gooseberry weight loss.
The barrier method (calcium chloride in a solution of 300 ppm) was the best preservation method for the Andean variety Cape gooseberry in terms of physical and chemical properties. Calcium chloride assisted the fruit in retaining properties like polar and equatorial diameters, controlling weight loss, and strengthening the berry (penetration resistance). It also aids in the preservation of soluble solids, pH, and acidity under storage at 10 ºC, preserving the quality of the Cape gooseberry fruit for up to 20 days.
The treatment with the greatest impact was sodium hypochlorite pre-treatment at 18 ℃. The fruit was significantly impacted by this disinfectant because its respiratory intensity increased, resulting in a tendency to ripen.
Acknowledgments
The authors thank the Ministry of Agriculture and Rural Development for financing the project which led to the creation of this article. The authors also wish to thank Agrosavia, the project's executing institution, and Jorge Tadeo Lozano University for the technical support.
Conflict of interest
All authors declare that they have no conflict of interest.
Author contributions
Conceptualization: M.C.G.; data curation: A.C.D.; formal analysis: M.C.G and M.P.T.; investigation: M.C.G. and M.P.T.; methodology: M.C.G; chemical analysis: A.C.D.; statistical analysis: M.C.G and M.P.T. writing original draft: M.C.G, M.P.T and A.C.D.; writing review and editing: M.P.T. All authors have read and agreed to the published version of the manuscript.