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Article

The Effect of Organic, Inorganic Fertilizers and Their Combinations on Fruit Quality Parameters in Strawberry

by
Neslihan Kilic
1,
Aysegul Burgut
2,
Muhammet Ali Gündesli
3,*,
Gozde Nogay
2,
Sezai Ercisli
4,*,
Nesibe Ebru Kafkas
2,
Halina Ekiert
5,
Hosam O. Elansary
6 and
Agnieszka Szopa
5
1
Department of Organic Farming Management, Kadirli School of Applied Sciences, Osmaniye Korkut Ata University, Osmaniye 80000, Turkey
2
Department of Horticulture, Faculty of Agriculture, University of Cukurova, Balcalı, Adana 01380, Turkey
3
Department of Plant and Animal Production, Nurdağı Vocational School, Gaziantep University, Gaziantep 27310, Turkey
4
Department of Horticulture, Faculty of Agriculture, Ataturk University, Erzurum 25240, Turkey
5
Department of Pharmaceutical Botany, Faculty of Pharmacy, Medical College, Jagiellonian University, Medyczna 9, 30-688 Kraków, Poland
6
Plant Production Department, College of Food and Agricultural Sciences, King Saud University, Riyadh 11451, Saudi Arabia
*
Authors to whom correspondence should be addressed.
Horticulturae 2021, 7(10), 354; https://doi.org/10.3390/horticulturae7100354
Submission received: 13 August 2021 / Revised: 13 September 2021 / Accepted: 27 September 2021 / Published: 2 October 2021
(This article belongs to the Special Issue Recent Advances in Horticultural Practices for Strawberries and Other Small Fruit Crops)
Browse Figures
Versions Notes

Abstract

:
Strawberry (Fragaria × ananassa Duch.) is widely grown and highly appreciated by consumers around the world for its delicious, soft, and highly nutritious fruits. Turkey is one of the most important strawberry producers in the world. Strawberry cultivation in Turkey typically involves the use of chemical fertilizers and more recently organic and organic + chemical fertilizers have been started to use in commercial production to produce healthier fruits. Therefore, in this study, we investigated the effect of organic, chemical, and organic + chemical fertilizer treatments in strawberry (cvs. ‘Albion’, ‘San Andreas’ and ‘Monterey’) fruit quality parameters including fruit color (L*, a*, b*, C and h°) parameters, soluble solids content, total acidity, fruit firmness, vitamin C, specific sugars and organic acids. Results showed that in particular fruit color parameters, soluble solid content (SSC), total acidity, fruit firmness, and vitamin C (L-Ascorbic acid) in fruits of three strawberry cultivars were significantly affected by different fertilizer applications (p < 0.05). Compared with conventional chemical fertilizer treatment, the organic fertilizer treatment produced fruit with significantly higher contents of SSC and glucose but decreased fruit firmness and vitamin C. Organic fertilizer also gave more intense colored strawberry fruits with high Chroma values (47,948 in organic fertilizer application and 39,644 and 39,931 in organic + chemical fertilizer and chemical fertilizer, respectively). Citric acid was identified to be the predominant organic acid in strawberry fruits but treatments were found insignificant on citric acid content.

1. Introduction

Strawberries (Fragaria × ananassa Duch.) are among the widely produced and consumed berry fruit in the world. The total cultivation area of strawberries in the world was 396,401 ha and total production was 8,885.028 tons in 2019 [1]. The strawberry cultivation area in Turkey has increased in recent years and it was about 11,679 ha in 2010 to and reached 15,392 ha in 2017. The suitability of ecological conditions in different regions of the country promoted the rapid increase of strawberry production [2].
More recently strawberries have gained high praise among consumers for their unique taste, availability year-round, and health benefits. In addition, today’s consumers are more knowledgeable and they are in demand of more attractive, high quality, nutritionally versatile, and safer plant produce. Strawberry fruits are rich in minerals, vitamins, phenolic compounds, and organic acids. The high anthocyanin, total phenolic compounds especially ellagic acid contents provides anti-carcinogenic and anti-cardiovascular properties [3,4,5].
As mentioned before strawberry is an important fruit crop in Turkey, but the average annual productivity in Turkey is considerably lower than in other important strawberry-producing countries like the USA, China, Mexico, Egypt, and Spain [1]. The low productivity for strawberries in Turkey could be the result of soil fertility because most strawberry farmers in Turkey uses pesticides.
More recently organic strawberry production in Turkey has gained importance because it is well known that an organic production system could help reduce the number of chemicals that damage soils. However, in Turkey, there are very few organic strawberry plantations. It is also important to ensure that there are sufficient nutrients available to ensure the good growth of strawberry plantations when using organic fertilizers. Some previous studies suggest that the productivity of organically produced strawberries is lower than conventionally produced ones [6,7,8]. Therefore, to maximize the potential of organic strawberry production systems it is important to improve nutrient availability as well as the abundance and activity of soil microorganisms [9,10,11].
Previous studies indicated that organically produced fruits and vegetables contain higher levels of flavonoids, anthocyanins, total phenolic compounds, sugars, organic acids, and L-ascorbic acid [12,13,14,15,16]. The increased concern of the consumers about the negative effects of agro-chemicals, driven an upward trend in organic production [17,18]. This trend also changed the way of scientific studies, where most of them focused on the effects of organic production on food quality [19,20,21]. Odongo et al. [22], reported that manure (containing favorable amounts of macro and micronutrients) treatments enhanced fruit set and size in strawberries by the formation of carbohydrates compared to inorganic triple phosphate fertilizer treatment. The use of organic fertilizers plus mineral fertilizers has proven to be a sound soil fertility management strategy in many countries around the world. It is not only improving the quality of fruits but also provides sustainability in production for the long term [23]. A lot of previous studies have shown that the application of organic fertilizers in strawberry fields improves plant nutrient availability and thus promotes plant growth [24,25,26,27,28]. In addition, the latest studies have focused on the nutrient and phytochemical contents of strawberries and the factors affecting the composition of this fruit. As a result of these studies, some of the authors reported that especially organically grown strawberries showed similar or better fruit quality characteristics than conventionally grown strawberries [18,29,30]. Ateş et al. [31] reported that the positive effects of various natural fertilizers on the yield parameters of strawberry cv. Albion berries (Fragaria × ananassa L.). Reganol et al. [18] implied that the organic strawberry farms produced higher quality fruit and that their higher quality soils may have greater microbial functional capability and resilience to stress. In addition, Cayuela [32] reported that organically grown strawberry fruits had higher sugar and dry matter (DM) content, while [33] found similar sugar content between organic and conventionally grown fruits. Despite the higher content of compounds important for human health in organically grown strawberries, there is still debate about the systematic differences in nutrition and quality of parameters of organic and traditionally grown strawberry crops [33,34,35]. Moreover, the excessive usage of chemical fertilizers and pesticides is very important, particularly fruits which can be eaten without removing peels such as strawberries and organic fertilizer may have solved this problem through an organic farming system [34,35,36,37,38,39].
To increase the attractiveness of the fruits by the consumer, the fruit quality characteristics such as firmness, color, and aroma of the fruits are very important. It is now clear that strawberry production is increasing in Turkey while the studies on the feasibility of organic fertilizer treatments are insufficient. Thus, the objective of the present study was to evaluate the influence of organic fertilizer, chemical fertilizer, and organic + chemical fertilizer treatments on the color values, fruit firmness, SSC, total acidity, individual sugars, vitamin C, and organic acids of three strawberry cultivars (‘Albion’, ‘San Andreas’ and ‘Monterey’).

2. Materials and Methods

2.1. Plant Material

This study was conducted at the Experimental and Research area of Kadirli Vocational School and Instrumental Analysis laboratory of Horticulture Department at the University of Çukurova during the 2018–2019 growing periods. Plant materials of the present study are frigo plants (cold-stored bare root crowns) of ‘Albion’, ‘San Andreas’, and ‘Monterey’ cultivars. ‘San Andreas’ strawberry cultivar is a moderate day-neutral with a production pattern very similar to ‘Albion’ cultivar. Plant vigor for ‘San Andreas’ is somewhat higher than for ‘Albion’ early in the season, but berry size throughout the fruiting season is similar to ‘Albion’. The fruit color for ‘San Andreas’ is slightly lighter than ‘Albion’, and it has similar post-harvest characteristics. The flavor of ‘San Andreas’ is very good, suitable for post-harvest handling and it also shows good disease resistance. Compared to ‘Albion’, the fruit color of ‘San Andreas’ is lighter, very early, and moderate tolerance to several strawberry diseases. ‘Albion’ cultivar is a day-neutral plant characteristic and well adapted to cool temperate areas. The fruit quality is excellent. It shows a strong tolerance against anthracnose, Verticillium, and Phytophthora, which are well-known as the most common strawberry diseases. ‘Monterey’ strawberry cultivar is also a day-neutral plant characteristic and slightly stronger flowering than ‘Albion’, with a similar production pattern. Compared to ‘Albion’, fruits are larger but softer. The fruit has an attractive aroma. It is susceptible to powdery mildew disease. The plant is more vigorous and may require more space than ‘Albion’. The fruits are large, firm, slightly carved, and dark red.

2.2. Soil Sampling and Analyses

Soil parameters of experimental area soils (Table 1) were analyzed before the experiment according to [40,41,42,43,44].
The liquid organic fertilizer (botanica) was used in current research as an organic fertilizer. It is rich in water-soluble plant nutrients, and humic-fulvic acid was also used in fertilizer applications. Liquid organic fertilizer contains 50% organic matter including 21.3% organic carbon, 3% total nitrogen, and 2.5% water-soluble potassium oxide (K2O). Chemical fertilizer application was done according to the soil analysis results.
The cold stored frigo plants of three strawberry cultivars were provided by Yaltir Agriculture company in Adana provinces of Turkey. In the planting stage, N-P-K (15-15-15) fertilizer, chemical fertilizer, and 1/2 organic + chemical fertilizer were sprinkled into the area before planting and mixed into the soil. Then the planting beds were prepared. Drip irrigation pipes were placed on the stretcher and then covered with black plastic mulch. The frigo plants were planted into 9 × 9 × 9 cm pots in August and rooted under a mist propagation system and plants were obtained and transplanted on 9 November 2018 to the field. The seedlings were cultivated on the bed with a 30 cm distance between plants and between rows, after planting; 500 g of organic liquid fertilizer was applied to the 1 da of residues. Plants were then covered with polyethylene with a low tunnel to protect them against the winter cold. Three weeks after the planting phase, weekly organic, chemical and organic + chemical fertilizer applications were started. In the organic treatments, above the mentioned liquid, organic fertilizer was used in a concentration of 500 g/da on a weekly basis. In the chemical fertilizer experiment, a total of 12.12 kg/da N, 11.35 kg/da P, 20.25 kg/da K, and 120 g/da Mg were given as chemical fertilizers during the experiment. The sources of chemical fertilizers are 21% ammonium sulfate, mono ammonium phosphate, potassium sulfate, and magnesium sulfate. In organic + conventional fertilizer application, half of the fertilizer doses of the chemical fertilizer and organic fertilizer treatment are given. Cultural maintenance was carried out regularly during the trial. Fruits were harvested at the commercial ripening stage (75% red) of strawberry fruits were immediately transferred to the laboratory under cold chain conditions and color measurement and fruit firmness of strawberries were done immediately after harvest and samples were frozen at −80 °C until analysis. For further analysis, fruits were homogenized using a kitchen hand blender. Three replicates were done per analysis total of 30 fruits were used for each replication. The following chemical parameters such as fruit firmness, fruit color, soluble solids content, total acidity (citric acid and malic acids), L-ascorbic acid (vitamin C), sucrose, glucose, and fructose were determined in strawberries using standard methods as below.

2.3. Surface Color Measurement

Color coordinates were measured as L, a*, b* using Minolta chromometer and calculated by a formula and given also as C and hue (h°) values of the outer color of the fruits [45,46].

2.4. Measurement of Fruit Firmness, Soluble Solids, and Total Acidity

At each sampling, 30 fruits per treatment with three replicates were used to measure fruit firmness. Fruit firmness was measured at the equator at two opposite spots (hence, n = 60), using a digital penetrometer (model 53205, TR). The total soluble solids content was measured on the juice of 30 fruits, by a digital table refractometer (HI96811; Hanna instruments). The total acidity was measured by titrating the same solution with 0.1 N sodium hydroxide until reaching pH 8.1 (n = 10), and the results were expressed as % acid [46].

2.5. Sugar Content Measurement

Glucose, fructose, xylose, and sucrose content in the juice obtained from the harvested strawberries were determined by [46,47]. Before analysis, frozen juice samples were thawed at 25 °C 1 mL of juice was added to 4 mL of ultrapure water (Millipore Corp., Bedford, MA, USA). The reaction mixture was placed in an ultrasonic bath and sonicated at 80 °C for 15 min and then centrifuged at 5500 rpm for 15 min and it was filtered before HPLC analysis (Whatman nylon syringe filters, 0.45 µm, 13 mm, diameter). The high-performance liquid chromatographic apparatus (Shimadzu LC 20A VP, Kyoto, Japan) consisted of an in-line degasser, pump, and controller coupled to a Refractive index detector (Shimadzu RID 20A VP) equipped with an automatic injector (20 µL injection volume) interfaced to a PC running Class VP chromatography manager software (Shimadzu, Japan). Separations were performed on a 300 mm × 7.8 mm i.d., 5 µm, reverse-phase Ultrasphere Coregel-87C analytical column (Transgenomic) operating at 70 °C with a flow rate of 0.6 mL min−1. Elution was isocratic ultrapure water. Individual sugars were calculated based on their standards and expressed in % of FW.

2.6. Organic Acid Measurement

Organic acids in strawberry fruit juice were determined by HPLC analysis developed by Bozan [48]. For organic acids extraction, 1 mL of the sample, and 4 mL of 3% metaphosphoric acid were mixed. The mixture was placed in the ultrasonic water bath at 80 °C for 15 min and it was sonicated and centrifuged at 5500 rpm for 15 min. Afterward, the mixture was filtered (Whatman nylon syringe filters, 0.45 µm, 13 mm, diameter) and the HPLC vials were removed. The extract of organic acids was analyzed using a high-performance liquid chromatographic apparatus HPLC (Shimadzu LC 20A VP, Kyoto, Japan) equipped with a UV detector (Shimadzu SPD 20A VP) and we used an 87 H column (5 μm, 300 × 7.8 mm, Transgenomic). As for the operating conditions column temperature, was set at 40 °C; injection volume, 20 μL; detection wavelength, 210 nm; flow rate 0.8 mL/min. and % 0.05 mM sulphuric acid was used as the solvent. Identification of organic acids and determination of peaks is based on the retention times of peaks and comparison of spectral data according to standards. The identified acids were evaluated according to the relevant standard calibration curves.

2.7. Statistical Analysis

All the result data were processed with the SPSS package program version 16.0 (SPSS Inc., Chicago, IL, USA). All data were presented as the mean ± standard error (SE) and analyzed by one-way analysis of variance (ANOVA). Differences were considered significant at p < 0.05. Additionally, principal component analyses (PCA) were also performed to show the relationships between the parameters and the cultivars. As an output of the PCA, in a biplot, the length of the lines approximates the variances of the variables. The longer the line, the higher is the variance. The cosine of the angle between the lines approximates the correlation between the variables they represent. The closer the angle is to 90, or 270 degrees, the smaller the correlation. An angle of 0 or 180 degrees reflects a correlation of 1 or −1, respectively. Cut-points far off in the direction of the variable line indicate high values, while cut-points far off on the variable line, which has been extended through the origin, represent low values. Finally, the distance between two points approximates the Euclidean distance between two observations in the multivariate space. Observations that are far away from each other have a high Euclidean distance, and vice versa [49].

3. Results and Discussion

3.1. Surface Color Measurement

Color is one of the most significant quality parameters for evaluating strawberries. The color in strawberries has been attributed to many factors, including maturity, ecology, genotype, and cultivar [26,32].
Results showed that there is a significant difference among the treatments (Table 2). The brightness (L) color was noted from the ‘San Andreas’ cultivar (35.619) which had been fertilized with the chemical fertilizer. On the other hand, the lowest external lightness was found in the ‘Albion’ fruits (19.403) with organic fertilizer treatment. As the average of three cultivars, the organic fertilizer treatment was then noted to have the lowest L value (24.764) where the highest L value (33.407) was obtained from the chemical fertilizer treatment (Table 2). In a previous study by Crecente-Campo [13], similar results were noted where they compared the external color brightness value of the strawberry fruits and reported low L values for organic (27.30) and high L values for conventional strawberry cultivations (32.60). When the L value increases as the color is lighten [50]. Pilanalı and Kaplan [51] in their experiments, reported that solid humic acid treatments significantly affect the fruit color. They noted that solid humic acid treatments increased the organic matter content of the soil, and this also cause an increase in the L value. However, in this study, the highest lightness values were obtained while chemical fertilizer treatment.
Fruit outer color a* value indicates the intensity of the color. The lower the a* value, the lower the red intensity; and the increase in a* value increases the red color intensity [50,51]. The highest external color a* value (green-red) of the fruits had been noted from the ‘Albion’ cultivars (46.83) treated with organic fertilizer. Thus, the lowest value (32.62) was obtained from the fruits of the ‘Monterey’ cultivar with chemical fertilizer treatment. Overall, the ‘Monterey’ cultivar was noted to have the lowest a* value (32.66); where the organic treated plants had the highest a* values (41.26). In a similar study Ates [31] noted that ‘Monterey’ had the lowest a* value as compared with ‘Albion’, ‘Aromas’, ‘Camarosa’ and ‘Sweet Charlie’.
The data obtained for the CIE L* a* b* color (Table 2) was similar to those recorded by Wang and Camp [25]. In addition, present results are similar to those of Ayala-Zavala [52] for the surface color for strawberries: L 33.90, C 35.10, and Hue 28.50. Similar to a* values, the highest b* values were noted from the organic fertilizer treatment. Gulbag and Ilgin [53] similarly investigated the effects of potassium humate, vegetable origin liquid humic acid, and seaweed as organic fertilizer in ‘Camarosa’ and ‘Elsanta’ strawberry cultivars. In that study, researchers found that the highest b* value was obtained from the ‘Elsanta’ cultivar treated with seaweed (26.65), and the lowest b* value was obtained from the ‘Camarosa’ cultivar treated with potassium humate (22.75).
The highest C value (58.66) was then noted from the ‘San Andreas’ cultivar fertilized with organic fertilizer. The lowest color density value (36.45) of the outer fruit was obtained from the ‘Monterey’ strawberry cultivar with chemical fertilizer treatment (Table 2). In a study, yield and some quality parameters of ‘Monterey’, ‘Albion’, ‘Aromas’, ‘Camarosa’ and ‘Sweet Charlie’ cultivars fertilized with different organic fertilizers were examined. The lowest average C values were determined from the ‘Monterey’ cultivar and the highest from the ‘Aromas’ cultivar [52]. Moreover, in our experiment the highest value of Hue (color angle value) was noted from the organic treated fruits, while the comparison of the cultivars for Hue resulted in decreasing order of ‘San Andreas’ > ‘Albion’ > ‘Monterey’.

3.2. Measurement of Soluble Solids, Total Acidity, and Firmness

The soluble solid content (SSC), total acidity, and fruit firmness values of three strawberry cultivars fertilized with different fertilizers are shown in Table 3. We found statistically significant differences (p < 0.05) among treatments. The lowest SSC was determined as 8.87% (Organic + Chemical-‘San Andreas’ cultivar) and the highest as 10.73% (Organic + Chemical-‘Monterey’ cultivar) (Table 3). Reganold et al. [18] reported that the dry matter content of organically grown strawberries is higher (8.3%) than conventionally cultivated crops. Similarly, Mahedeen [54], determined that organic farming improves fruits’ soluble solids contents of strawberries. Ozguven and Yilmaz [55] reported that the amount of SSC in the ‘Fern’ strawberry cultivar varied from 6.30% to 8.44% in their experiments on different conditions in Adana. In another study, Ozkan [37] reported that the SSC amount varied between 8.42% and 8.66% on the ‘Fern’ strawberry cultivar in different organic fertilizer treatments. Our results differed from previous studies. This situation is thought to be caused by the cultivar, soil, and climate differences of experimental areas.
The highest total acidity of the fruits was obtained from the ‘Albion’ cultivar from the chemical fertilizer treatment (1.63%) and the lowest from the organic fertilizer treatment of the ‘Monterey’ cultivar (1.14%) and we found statistically significant differences (p < 0.05) among treatments (Table 3). Abu-Zahra [56] reported similar findings for the ‘Honor’ strawberry cultivar where the amount of total acidity was higher in conventionally grown fruits. According to Camargo [57] organic and conventionally cultivated ‘Camarosa’ and ‘Sweet Charlie’ cultivars have significant differences in terms of the amount of total acidity, where the conventional growing system have higher values for ‘Sweet Charlie’ cultivar, but organic growing systems have higher values for ‘Camarosa’ strawberry cultivar. These results are similar to the findings obtained in our study.
The effects of organic and chemical fertilizers on fruit firmness were also examined in the present study (Table 3). According to the results obtained, chemical fertilizer treatment was found to have the highest fruit firmness (1.16 N) than the other fruits. It was then found that fruits treated with organic fertilizer were softer (0.91 N) than other treatments. ‘Albion’ had the hardest flesh fruit under the application of three types of organic fertilizers and ‘San Andreas’ was found to be the softest cultivar.

3.3. Organic Acids

The organic acid content of the fruits varies according to the species, cultivars, and cultivated conditions, etc. Especially sugar-acid balance and contents are the primary determinants of the taste properties of fruits. The most widespread acids evaluated in fruits are tartaric acid, malic acid, and citric acid, known to affect taste-aroma formation and many physiological processes are known as “fruit acids” [58,59].
The changes in the organic acids that are quantitatively the most important difference in determining fruit acidity are shown in Table 4. The organic acids (L-ascorbic acid, citric acid, malic acid, succinic acid, and fumaric acid) were identified and quantified by the HPLC method. Statistically significant differences (p < 0.05) occurred among strawberry fruits in terms of the content of organic acids. The highest amount (43.193 mg/100 g) of L-ascorbic acid was noted from the ‘Albion’ cultivar fertilized with chemical fertilizer while ‘San Andreas’ had the lowest (21.678 mg/100 g) L-ascorbic acid content with organic treatment. Likewise, Odriozola-Serrano [60] found that the vitamin C value of strawberry cultivar was 49.5 mg/100 g. These values are within the range observed in other studies. Klopotek [61] reported that vitamin C contents were ranged between 37 and 69 mg/100 g in diverse strawberry juices. The U.S recommended daily intake (RDI) of vitamin C is currently revised recommended to should not be below 60 mg [52]. Reganold [18] report that organically grown strawberries have higher levels of vitamin C than conventionally grown strawberries. Abu-Zahra [47] similarly noted that the organic fertilized strawberry fruits have higher vitamin C than the control and conventionally grown fruits. Cayuela [30] did not show the relationship between a higher level of vitamin C and organic cultivation. In the study of Hagg [62], the strawberry samples of the cultivar ‘Senga Sengana’ contained 52–64 mg vitamin C per 100 g. The findings of our study conducted on vitamin C in strawberries are also generally in agreement with the findings of the other researchers [62,63]. Ozkan [37] reported that the organic treatment of the ‘San Andreas’ cultivar has the lowest value of vitamin C than the others.
The most common acids found in fruits are tartaric, malic, and citric acid. In the present experiment, the highest citric acid amount (1.184%) was observed in the ‘Albion’ cultivar with chemical fertilizer treatment while ‘Monterey’ had the lowest (0.655%) citric acid content with chemical fertilizer treatment. The highest amount of malic acid content (0.769%) of ‘Albion’ fruits were detected under chemical fertilizer treatment. ‘San Andreas’ cultivated with organic fertilizer was found to have the lowest amount malic acid content (0.244%) among the strawberry cultivars. The highest amount of succinic acid content (0.299%) of ‘Monterey’ fruits was detected under organic fertilizer treatment (Table 3). In this study, the highest total acid content in the ‘Albion’ cultivar was obtained from chemical fertilizer treatment while the lowest acid content was obtained from organic fertilized fruits of the ‘San Andreas’ cultivar (Table 3). Holcroft and Kader [64] and Mahmood [65], reported that citric acid is the most abundant organic acid in strawberry fruits, followed by malic acid. In addition, Kafkas [46] reported that the main organic acid is citric acid and its concentration varied between 9.15 and 20.27 g/kg frozen weight based on the maturation stages in strawberries. Kafkas [66] found the amount of citric acid was 0.61% in the ‘Camorosa’ strawberry cultivar and 0.91% in the ‘Dorit’ cultivar. Koyuncu and Dilmaçünal [59], reported that the amount of citric acid in the strawberry fruits decreased during storage and it was found to as 5.27 mg/g at the end of the storage. Kafkas [66] examined the organic acid content in three different maturity periods in strawberries and they found that malic acid content varies between 0.10% and 0.43% in the green period. Some research found that the content of total acids in strawberries amounted to 1.00%, while other research found that this value was within the range from 0.98–1.20% [67,68,69,70,71]. While some of the data obtained from this study were close to the values reported in other studies, it was observed that they were higher than the values in some studies and lower than others. These differences can be attributed to different genetic characteristics of the study materials, as well as climatic conditions and other environmental factors.

3.4. Sugar Contents

Together with acids, sugars are the main ingredient in the fruit’s flavor. The content of total sugar varies depending on the variety, degree of maturity, and growing conditions. The most common sugars in strawberry fruits are sucrose, glucose, and fructose [62,63]. There were statistically significant differences between treatment and cultivars in terms of sugar contents (p < 0.05) (Table 5). In this research, the amount of fructose and glucose was determined at the highest level (4.044%) and (3.535%) in fruits of organic + chemical treated ‘Albion’ cultivar, respectively (Table 5). Urun et al. [72], Montero [73], and Perkins-Veazie [74] also found higher concentrations of fructose than other sugars in ripe strawberry fruits. On the other hand, both the results of the present study and other published literature had found quantitative small differences between glucose and fructose. While the highest amount of glucose (3.535%) was found in the organic + chemical treated ‘Albion’ strawberry fruits, the lowest glucose content (2.713%) was noted from the organic + chemical treated ‘San Andreas’ strawberry fruits. In this study, the sucrose content of organically fertilized ‘San Andreas’ strawberry fruits was found to be 1.032%, while the organic fertilized ‘Monterey’ cultivar was found to be 1.741%. Cayuela [30] found that organic berries have a higher sugar content than conventionally grown fruits. Pérez [75] reported 5.15, 17.77, and 19.40 g/kg values for sucrose, glucose, and fructose, respectively, for the ‘Chandler’ strawberry cultivar. Al-Karawi and Al-Rawi [76] found that organic fertilizer treatments increased sugar content in strawberry fruits. Similarly, Neri [77] reported that long-term organic fertilizer treatments increased the sugar content of fruits of the ‘Onda’ strawberry cultivar. Mahmood [65] reported that amounts of sucrose, glucose, and fructose are in the immature to fully mature stages in strawberry cultivars were 1.79–2.86%, 1.79–2.25%, and 0.01–0.25%, respectively. The findings of the present study are generally in agreement with the findings of the other researchers [71,72,75,78].

3.5. Statistical Analyses Results

Correlation analysis was also conducted to statistically reveal the effect of organic and chemical fertilizer treatments on organic acid, fruit firmness, and sugar content of strawberry fruits (Figure 1). Results showed that the organic acid contents have negligible to moderate negative correlation with the a*, b*, C, and Hue values of color. The highest negative correlation for color values was noted to be with the sucrose content. So, it can be concluded that the increase in sucrose content reduces the a*, b*, C, and Hue values, or vice versa. On the other hand, L-ascorbic acid was found to have a strong positive correlation with the malic and fumaric acid contents. Stojanov [79] reported MCB (aged mature cattle manure as organic fertilizer) and Scotts (water-soluble granulated compound fertilizer, commercially named) significantly improved single and total sugars contents. Ozkan, [37] reported the effect of organic fertilizers and chemical fertilizer treatment on the strawberry cultivar ‘Fern’. Sugar content is an important criterion of taste in strawberry fruits and attracts consumers [66,80].
Principal component analysis (PCA) was conducted to determine the relationships among the quality parameters and cultivars (Figure 2). As a result of this statistical analysis, the most important parameters that define the ‘Albion’ cultivar were found to be the L-ascorbic acid, fructose, and glucose. On the other hand, the ‘Monterey’ cultivar was found to be highly affected based on sucrose and succinic acid content, while the ‘San Andreas’ cultivar was found to having no strong relationships with any of the tested parameters. Maybe the most important results of the present study are presented in Figure 2 where the color values have a strong relationship with the organic fertilizer treatments. These results support our above-discussed effects of organic fertilization on the color values. It was presented in the figure that the organic acids are highly improved by the chemical fertilizer treatment. Finally, the combination of organic and chemical fertilizers has been found to provide the highest sucrose content to the strawberries.

4. Conclusions

There are a limited number of studies in the literature on the biochemical contents of strawberry fruits in organic fertilizer conditions. Specifically, the study involved a range of comparative fertilizer treatments and therefore this study is considered a valuable reference to determine the most suitable treatments and cultivars for commercial production. The findings of the present study also suggested that the organic fertilizer significantly improves the color of the strawberry fruits and it is also required to apply chemical fertilizers together to obtain high-quality strawberries. In conclusion, we need standardized testing, extraction, and analysis protocols to compare cultivars grown in different countries. This research will certainly be helpful in better understanding the organic farming package for strawberries as a holistic and sustainable approach to improve soil health as well as increase the productivity and profitability of quality fruits.

Author Contributions

Conceptualization, N.K.; N.E.K.; G.N.; A.B. and M.A.G.; writing—original draft preparation, N.E.K., N.K.; S.E.; A.B., G.N. and M.A.G.; writing—review and editing, N.K., A.B., M.A.G., H.E.; A.S.; S.E.; H.O.E. and N.E.K.; methodology, N.K., N.E.K., G.N., M.A.G., and A.B.; executed the experiment, M.A.G., N.K.; N.E.K.; G.N.; A.B. and S.E.; formal analysis, M.A.G., N.E.K.; A.B.; N.K. and G.N. All authors have read and agreed to the published version of the manuscript.

Funding

This research received external funding from Researchers Supporting Project number (RSP-2021/118), King Saud University.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All-new research data were presented in this contribution.

Acknowledgments

The authors extend their appreciation to King Saud University (RSP-2021/118), Riyadh, Saudi Arabia, for their support of the present research manuscript.

Conflicts of Interest

The authors declare that they have no conflict of interest.

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Figure 1. Correlation graphic for organic acids, sugars, and color parameters of strawberry fruits as affected by different organic or chemical fertilizer applications.
Figure 1. Correlation graphic for organic acids, sugars, and color parameters of strawberry fruits as affected by different organic or chemical fertilizer applications.
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Horticulturae 07 00354 g002 550
Figure 2. PCA-Biplot graph for organic acids, sugars, and color parameters of strawberry fruits as affected by different organic or chemical fertilizer treatments, grouping for cultivars (up), and grouping for fertilizers (down).
Figure 2. PCA-Biplot graph for organic acids, sugars, and color parameters of strawberry fruits as affected by different organic or chemical fertilizer treatments, grouping for cultivars (up), and grouping for fertilizers (down).
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Table
Table 1. Basic soil data of the experimental site.
Table 1. Basic soil data of the experimental site.
Soil Properties Depth (0–20 cm)Depth (20–40 cm)
TextureClay-loamClay-loam
pH7.507.50
Saliniy (%)0.0010.001
Lime (%)38.6836.75
Organic Matter (%)1.361.23
P2O5 (kg/da)2.172.06
K2O (kg/da)39.3332.14
Ca (%)0.090.08
Mg (%)0.040.03
Na (%)0.330.29
Fe (mg kg−1)0.80.44
Cu (mg kg−1)0.620.59
Mn (mg kg−1)1.641.91
Zn (mg kg−1)0.240.24
Table
Table 2. Color values of strawberry fruits as affected by different fertilizer treatments.
Table 2. Color values of strawberry fruits as affected by different fertilizer treatments.
Cultivars, Treatments, and CombinationL*a*b*C*h°
Organic * ‘Albion’19.403 c46.831 a33.744 a57.835 a35.521 ab
Organic + Chemical * ‘Albion’32.763 a35.612 b19.589 bc40.729 bc28.543 cd
Chemical * ‘Albion’33.435 a35.321 b20.673 bc41.014 bc30.227 bc
Organic * ‘San Andreas’24.186 bc46.307 a29.265 ab52.106 ab36.815 a
Organic + Chemical * ‘San Andreas’33.398 a34.808 b20.169 bc39.933 bc29.100 cd
Chemical * ‘San Andreas’35.619 a36.230 b24.227 abc42.269 bc30.306 bc
Organic * ‘Monterey’30.704 ab30.652 b14.398 c33.902 c25.056 cd
Organic + Chemical * ‘Monterey’31.249 ab34.710 b15.974 c38.270 bc24.377 d
Chemical * ‘Monterey’31.167 ab32.621 b16.213 c36.511 c26.131 cd
‘Albion’28.534 a39.254 a24.669 a46.526 a31.430 a
‘San Andreas’31.068 a39.115 a24.554 a44.769ab32.074 a
‘Monterey’31.040 a32.661 b15.528 b36.228 b25.188 b
Organic24.764 b41.263 a25.802 a47.948 a32.464 a
Organic + Chemical32.470 a35.043 b18.577 b39.644 b27.340 b
Chemical33.407 a34.724 b20.371 b39.931 b28.888 b
L*: brightness; a*: red–green axis; b*: yellow–blue axis; C*: color intensity; h°: tone. * Kruskal Wallis p value, Different capital letters indicate statistically significant difference among varieties and application at p < 0.05.
Table
Table 3. Effect of different fertilizer treatments on SSC, total acidity, and fruit firmness of strawberry cultivars.
Table 3. Effect of different fertilizer treatments on SSC, total acidity, and fruit firmness of strawberry cultivars.
TreatmentsCultivarsSSC
(%)		Total Acidity
(%)		Fruit
Firmness (N)
Organic‘Albion’10.53 a1.45 a0.95 a
‘San Andreas’9.57 b1.32 b0.86 b
‘Monterey’10.50 a1.14 c0.93 a
Organic + Chemical‘Albion’9.17 b1.30 b1.16 b
‘San Andreas’8.87 c1.37 a1.20 a
‘Monterey’10.73 a1.17 c1.12 c
Chemical‘Albion’9.67 c1.63 a1.55 a
‘San Andreas’10.60 a1.46 b1.25 b
‘Monterey’9.97 b1.35 c0.92 c
Organic 10.20 a1.31 b0.91 c
Organic + Chemical 9.59 b1.24 c1.16 b
Chemical 10.08 a1.48 a1.24 a
Values are the average of triplicates ± standard deviation. Different letters in each row show the significant statistical difference (p < 0.05) between the samples.
Table
Table 4. The organic acid content of strawberry fruits is affected by different fertilizer treatments.
Table 4. The organic acid content of strawberry fruits is affected by different fertilizer treatments.
Cultivars, Treatments, or CombinationL-Ascorbic Acid (mg/100 g)Citric Acid (%)Malic Acid (%)Succinic Acid (%)Fumaric Acid (%)
Organic * ‘Albion’29.835 bc0.920 abc0.315 ab0.278 a0.009 NS
Organic + Chemical * ‘Albion’28.703 bc0.852 abc0.269 ab0.225 a0.009
Chemical * ‘Albion’43.193 a1.184 a0.384 a0.265 a0.010
Organic * ‘San Andreas’21.678 c0.816 bc0.244 b0.218 a0.007
Organic + Chemical * ‘San Andreas’24.362 bc0.893 abc0.267 ab0.255 a0.008 NS
Chemical * ‘San Andreas’34.533 ab1.137 ab0.371 ab0.287 a0.001
Organic * ‘Monterey’26.748 bc0.678 c0.312 ab0.299 a0.009
Organic + Chemical * ‘Monterey’29.803 bc0.723 c0.320 ab0.290 a0.010
Chemical * ‘Monterey’31.607 bc0.655 c0.328 ab0.266 a0.015
‘Albion’33.911 a0.986 a0.322 a0.254 a0.009 NS
‘San Andreas’26.858 a0.948 a0.294 a0.255 a0.080
‘Monterey’29.386 a0.689 b0.319 a0.285 a0.010
Organic26.087 b0.809 NS0.288 b0.262 NS0.009 NS
Organic + Chemical27.623 b0.8230.285 b0.2570.009
Chemical36.444 a0.9930.361 a0.2720.015
Values are the average of triplicates ± standard deviation. * Kruskal Wallis p value, Different capital letters indicate statistically significant difference among cultivars at p < 0.05. NS: Non-Significant.
Table
Table 5. The sugar content of strawberry fruits is affected by different fertilizer treatments.
Table 5. The sugar content of strawberry fruits is affected by different fertilizer treatments.
Cultivars, Treatments, or CombinationSucrose (%)Glucose (%)Fructose (%)
Organic * ‘Albion’1.283 NS3.263 NS3.757 NS
Organic + Chemical * ‘Albion’1.4023.5354.044
Chemical * ‘Albion’1.3283.1233.573
Organic * ‘San Andreas’1.032 2.8203.239
Organic + Chemical * ‘San Andreas’1.308 NS2.713 NS3.165 NS
Chemical * ‘San Andreas’1.3083.0063.494
Organic * ‘Monterey’1.7413.2723.724
Organic + Chemical * ‘Monterey’1.6463.0413.455
Chemical * ‘Monterey’1.4322.7663.170
‘Albion’1.338 ab3.307 a3.791 a
‘San Andreas’1.216 b2.846 b3.299 b
‘Monterey’1.606 a3.027 ab3.450 ab
Organic1.352 NS3.118 NS3.573 NS
Organic + Chemical1.4523.0963.555
Chemical1.3562.9653.412
* Kruskal Wallis p value, Different capital letters indicate statistically significant difference among cultivars at p < 0.05. NS: Non-Significant.
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Kilic, N.; Burgut, A.; Gündesli, M.A.; Nogay, G.; Ercisli, S.; Kafkas, N.E.; Ekiert, H.; Elansary, H.O.; Szopa, A. The Effect of Organic, Inorganic Fertilizers and Their Combinations on Fruit Quality Parameters in Strawberry. Horticulturae 2021, 7, 354. https://doi.org/10.3390/horticulturae7100354

AMA Style

Kilic N, Burgut A, Gündesli MA, Nogay G, Ercisli S, Kafkas NE, Ekiert H, Elansary HO, Szopa A. The Effect of Organic, Inorganic Fertilizers and Their Combinations on Fruit Quality Parameters in Strawberry. Horticulturae. 2021; 7(10):354. https://doi.org/10.3390/horticulturae7100354

Chicago/Turabian Style

Kilic, Neslihan, Aysegul Burgut, Muhammet Ali Gündesli, Gozde Nogay, Sezai Ercisli, Nesibe Ebru Kafkas, Halina Ekiert, Hosam O. Elansary, and Agnieszka Szopa. 2021. "The Effect of Organic, Inorganic Fertilizers and Their Combinations on Fruit Quality Parameters in Strawberry" Horticulturae 7, no. 10: 354. https://doi.org/10.3390/horticulturae7100354

APA Style

Kilic, N., Burgut, A., Gündesli, M. A., Nogay, G., Ercisli, S., Kafkas, N. E., Ekiert, H., Elansary, H. O., & Szopa, A. (2021). The Effect of Organic, Inorganic Fertilizers and Their Combinations on Fruit Quality Parameters in Strawberry. Horticulturae, 7(10), 354. https://doi.org/10.3390/horticulturae7100354

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