Strawberry may be a pseudo fruit mainly cultivated in temperate climate regions. Considering its high levels of antioxidant and phenolic compounds, the consumption of strawberry fruit is often beneficial to health. The Brazilian strawberry production revolves around 3000 tons each year, significantly influencing the grocery store and generating income for farmers. However, this product are often partially impaired by a two-spotted tetranychid (TSSM) Tetranychus urticae Koch infestations, because of decreases within the quality and quantity of fruit. Since there aren’t any data within the literature about alterations caused by TSSM infestation in strawberry plants, our work aimed towards evaluating nutritional and physicochemical parameters of TSSM-infested strawberry plants, together with the related chemical treatment (CT) (acaricide) or biological treatment (predatory mite Phytoseiulus macropilis Banks).

Strawberry fruit from TSSM-infested plants present the very best levels of acidity and exhibit low levels of anthocyanin and phenolic compounds, while fruit from TSSM-infested plants + biological control using predatory mite shows high levels of soluble solids, phenolic compounds, and water-soluble vitamin, together with a high soluble solid content/titratable (SSC/TA) acidity ratio, which indicates high-quality fruit.

Our results suggest that TSSM infestation decreases fruit quality which the biological control of TSSM employing a predatory mite may be a suitable alternative to organic production since the presence of predatory mite doesn’t affect fruit quality and development.


Biological controlPhytoseiulus macropilisTetranychus urticae

1. Introduction
Fruits play an important role in our diet since they contain vitamins, carbohydrates, and minerals, and also non-nutrient compounds as polyphenols, all of which are necessary for a healthy life. Among them, citrus fruits stand out because of the high levels of organic acids [1]. Strawberry, a widely cultivated pseudofruit (approximately 4.6 million tons in 2011) [2] consumed in natural or processed as juice and jelly, has high water-soluble vitamin (vitamin C) levels [3], yet as high levels of polyphenolic compounds (mainly ellagitannins and anthocyanins), all compounds related to health benefits [4]. Anthocyanins, the most ones to blame for the characteristic red color of the strawberry fruit, influence fruit appearance [5] and display antioxidant, anti-inflammatory, anticarcinogen, and antineurodegenerative properties [6,7,8,9,10,11].

During the fruit ripening process, organic acids are degraded, decreasing the astringency and acid taste. a decent indicator of fruit quality concerns the soluble solid content/titratable acidity ratio (SSC/TA). This value is enhanced by organic acid degradation, reducing the strawberry fruit acidity, and producing the characteristic sweetness favored by consumers [12]. in step with Resende et al. [13], the greater the SCC, the higher is that the flavor and taste of the strawberry fruit.

Several factors may affect the nutritional and physicochemical composition of strawberry fruit, mainly the planted cultivar, the maturity stage, harvest season, planting location, climatic factors, and plant management, all of which influence fruit quality [14]. consistent with the Environmental unit [15], strawberry is one among the foremost chemically treated fruits, ranking second within the “Dirty Dozen”. Such a pesticide application is critical because strawberry fruit is widely attacked by several pests, including phytophagous mites [16].

The yield and weight of strawberry fruit are often severely full of Tetranychus urticae Koch (two-spotted tetranychid — TSSM) infestations. Small smudges and/or isolated discolored areas may be seen within the infested areas. Severe infestations can cause complete leaf bronzing, displaying a reddish and/or dry aspect, characteristic of older/senescent leaves. a decent indicator of TSSM infestation is that the production of abundant webs on both leaf faces [17]. TSSM infestations can reach alarming levels and will of course cause the death of the plant, reducing fruit production by up to 80% [18].

Aiming to reduce the losses caused by TSSM infestations, acaricide chemical treatments are generally the most and first choice by farmers. However, organic cultivation supported clean production technologies has stood move into recent years [19]. In Brazil, farmers have recently began to adopt the inundative liberation of predatory mite Phytoseiulus macropilis Banks (Phytoseiidae) as another to the biological control of phytophagous mites. With such a clean approach, farmers can efficiently control TSSM infestations without using chemical treatments [19,20].

To understand how strawberry fruit is nutritionally stricken by TSSM infestations, the plants were subjected to different treatments: criterion (no infestation); TSSM infestation; TSSM infestation + chemical treatment (CT — acaricide); and TSSM infestation + biological treatment (BT — P. macropilis). This study reports the physicochemical and nutritional alterations of strawberry fruit and leaves subjected to the above-mentioned conditions. The results provide evidence that TSSM infestation has deleterious effects on the nutritional parameters of strawberry fruit, while the biological control of TSSM infestations using predatory mite will be an efficient method to regulate T. urticae development without negative effects on fruit quality.

2. Materials and methods
2.1. material and mite infestation
Strawberry seedlings (Fragaria × Ananassa Duch, cv. Camarosa) were planted in vases with peat-based substrates and carbonized rice hulls. The plants were grown in greenhouse conditions at 25°C and ratio was maintained at 60%. Four treatments (with four plants per treatment) were administered: Treatment 1, plants without contact with TSSM (Control); Treatment 2, TSSM-infested plants, without control (TSSM); Treatment 3, TSSM-infested plants + CT 1% abamectin (TSSM + CT); Treatment 4, TSSM-infested plants + BT using P. macropilis releasing (TSSM + BT). TSSM specimens used for infestations were maintained on strawberry leaves under BOD conditions at the Acarology Laboratory (Centro Universitário UNIVATES).

Urea was applied as nitrogen fertilizer at 40 d, right before the primary harvest. In Treatments 2, 3, and 4, 20 d before the primary harvest, ten TSSM specimens were applied per plant, while chemical and biological controls were applied 5 d before the primary harvest. The fruit was harvested when their ripe area reached 2/3 of their total area. Young and mature leaves were also collected within the last fruit harvest. All the experiments were repeated twice within the same year with similar results.

2.2. Fresh strawberry fruit extract

Juice fruits were extracted in step with Pelayo-Zaldívar et al. [21], with minor modifications. Each sample was homogenized employing a mini-processor and therefore the fruit mass was diluted 1:1 with H2O. Four samples from each treatment were analyzed in triplicates.

2.3. Fruit analyses
The pH determination was performed with pH meter DM-20 (Digimed). Titratable acidity (TA) was performed by titration with NaOH 0.1 N and therefore the results were expressed like of acid equivalents.

SSC, (expressed as °BRIX) was analyzed employing a refracto meter (Abbé Digital, 0–95 Brix NOVA WYA-2S). The SSC/TA relates to °Brix/% of acid equivalents.

Ascorbic acid amounts were determined consistent with Terada et al. [22], with minor modifications suggested by Moretti et al. [23]. This analysis relies on the reduction of two,6-dinitrophenol–indophenol sodium salt by an vitamin C solution.

Anthocyanins were quantified using the differential pH method proposed by Giusti and Wrolstad [24], during which anthocyanin pigments are structurally transformed, followed by a pH alteration that may be detected by absorbance difference.

The Folin–Ciocalteu method was wont to assess the full phenolic content. Extracts were heated for two h at 85°C to eliminate antioxidant interference and assayed in keeping with Georgé et al. [25] using acid because the standard. the full phenolic content was expressed in mg of acid equivalents · 100 g fruit- 1.

2.4. Dry strawberry leaf extract
Strawberry leaves collected at the tip of the experiment were dried at 37°C for 18 h. Dried samples were ground to a fine powder to be employed in methylxanthine and phenolic analyses.

2.5. Leaf analyses
To analyze methylxanthine, 250 mg of dried samples were extracted with 20 mL of two.5% (v/v) sulfuric acid under constant agitation for 15 min. This procedure was repeated fourfold. The samples were spectrophotometrically analyzed at 271 nm, in line with Farmacopedia Brasileira [26]. Results were expressed in mg of caffeine equivalents/g of dry weight.

Phenolic compounds in strawberry leaves were quantified using the identical methodology used for quantification in fruit (Folin–Ciocalteu method) [25].

2.6. Statistical analysis
Data were subjected to variance analyses (One-way ANOVA) and therefore the means were compared by the Tukey HSD (Honestly Significant Differences) test (P ≤ 0.05) using SPSS Base 17.0 for Windows (SPSS Inc., USA). Levene’s test (for homogeneity of variance) was used before ANOVA.

3. Results and discussion
3.1. Fruit analyses
TSSM + CT or BT presented strawberry fruit with the best pH values (Figure 1a). the info were confirmed by very cheap titratable acidity found in these samples (Figure 1b). in line with Pelayo-Zaldívar et al. [21], consumer preferences were mainly associated with higher sugar (sweetness) and volatile contents. Thus, fruit derived from TSSM-infested plants displayed inferior quality. Acidity/sweetness in strawberry fruit is expounded to the ripening process. During this process, organic acids are degraded, astringency and acidity are reduced, sugar levels continually increase and also the widely accepted sweet taste is enhanced [27,28]. Such pH alteration seems to be directly linked to plant treatment since control and TSSM-infested plants (without any treatment) showed high acidity levels. Such data indicate that treated plants can produce higher levels of natural organic acids, or the presence of TSSM for a extended period of your time can inhibit the degradation of organic acids since TSSM was extinct on the treated plants (either chemically or biologically). The sequential analysis (through time course harvesting) of those parameters could shed some light on this assumption. The pH values found in our samples (from 3.6 to 3.8) concur with previous reports [29,30].

Fig. 1. Chemical and nutritional parameters in strawberry fruit. (a) pH value; (b) Titratable Acidity; (c) SSC; (d) Anthocyanins (e) Phenolic Compounds; (f) vitamin C. TSSM: Two-spotted mite; TSSM + CT: Two-spotted mite + Chemical Treatment; TSSM + BT: Two-spotted Spider Mite + Biological Treatment. The values are averages of 4 samples ± SE. Different letters indicate that the means are different in keeping with the Tukey HSD test (P ≤ 0.05). Error bars is also too small to be visible within the figure.

Strawberry fruit from TSSM-infested + BT plants presented the very best sugar levels, while TSSM + CT fruit presented all-time low levels (Figure 1c — SSC, °BRIX). This index is directly associated with fruit quality since the most indicators of pleasant flavors are SSC [31]. in keeping with Resende et al. [13], SSC is accountable for the pleasant taste and flavor of strawberry fruit and, additionally to organic acids and soluble pectins, sugars are the most contributors of SSC in strawberries [21]. Again, fruit from TSSM-infested plants displayed lower levels than fruit from TSSM + BT, suggesting that the presence of TSSM ends up in low-quality fruit.

One of the widely accepted parameters accustomed verify strawberry fruit quality and consumer acceptability [32] concerns the relation between SSC/TA. As shown in Figure 2, TSSM + BT plants presented the best fruit quality (9.60), while TSSM and TSSM + CT plants yielded fruit with very cheap quality levels (5.5 and 5.2, respectively). per Green [33], a sugar/acid ratio of 5.3 is taken into account rock bottom acceptable level for strawberry fruit. Cordenunsi et al. [34] showed that cv. Oso Grande, which is taken into account a wonderful option for fresh consumption in terms of nutritional value and quality parameters, contains a sugar/acid ratio of 9.2. Recently, Reganold [35] found a difference of roughly 16% within the SSC/TA ratio between chemically treated and organically cultivated strawberries. Yet, Camargo et al. [36] found that cv. Aromas have the next (approximately 9%) SSC/AT ratio when organically cultivated as compared with traditional cultivation using chemical treatment. Our datum to a very high difference (approximately 78%) between TSSM + BT and TSSM + CT.


Fig. 2. Quality assessment of strawberry fruit through SSC/TA ratio. TSSM: Two-spotted mite; TSSM + CT: Two-spotted mite + Chemical Treatment; TSSM + BT: Two-spotted Spider Mite + Biological Treatment. The values are averages of 4 samples ± SE. Different letters indicate that the means are different in step with the Tukey HSD test (P ≤ 0.05). Error bars could also be too small to be visible within the figure.

Besides size and shape, color is another important component of the looks of strawberry fruit, and it’s mainly defined by its anthocyanin content [34]. Anthocyanins are quantitatively the foremost important form of phenolic compound present in strawberries [37]. All strawberry fruit analyzed in our work presented anthocyanin values in agreement with previous studies (Figure 1d) (from 13 to 60 mg · 100 g of fruit- 1), in step with Cordenunsi et al. [34], Cordenunsi et al. [38] and Blando et al. [39]. However, TSSM-infested plants still produced the bottom quality fruit (34.4 mg · 100 g of fruit- 1), containing an occasional quantity of red pigments, giving an unhealthy impression, and, consequently, less attractiveness to consumers. in step with Naumann and Seipp [40], color and texture are the foremost important characteristics of the retail market and may strongly influence consumer choices. Fruit from control plants (no contact with TSSM) showed the very best anthocyanin level (51.4 mg · 100 g- 1), suggesting that TSSM infestation can reduce anthocyanin concentration in strawberry fruit, even when followed by chemical or biological treatment. consistent with Musilová et al. [41], one amongst the most factors affecting anthocyanin accumulation in strawberry fruit is that the cultivar, since they showed different anthocyanin levels for seven cultivars under the identical soil, management, and harvesting conditions. Our results (from 34.4 to 51.4 mg · 100 g of fruit- 1) are in agreement with Castro et al. [42], which found 48 mg · 100 g of fruit- 1 within the same cultivar utilized in our work.

Several studies have identified a good range of phenolic compounds in strawberry fruit [37,43], but anthocyanins remain quantitatively the foremost important type. Fruit from TSSM-infested plants showed extremely low phenolic compound levels (158.9 mg · 100 g of fruit- 1 — Figure 1e), while TSSM + BT fruit had the best phenolic level (343.5 mg · 100 g of fruit- 1, not statistically different from control and TSSM + CT treatments). The presence of TSSM for extended periods of your time leads to low phenolic levels in strawberry fruit since TSSM-infested plants showed lower levels than the opposite samples. we are able to suggest that TSSM extinction (or the absence of contact with TSSM within the control condition) stimulates the synthesis of phenolics, allowing higher levels of those compounds in strawberry fruit. Luczynski et al. [44] demonstrated that the event of TSSM T. urticae Koch is negatively correlated to concentrations of phenolic compounds in strawberry leaves, which mite development is delayed on leaves with higher concentrations of phenolic compounds. supported these data obtained in leaves [44], we could also hypothesize that the low level of phenolic compounds seen on TSSM-infested plants may be associated with higher catabolism of phenolic compounds, rather than stimulation on the control or treated plants. To the most effective of our knowledge, the relation between phenolic compounds in strawberry fruit and therefore the presence of TSSM has not yet been reported. However, more in-depth studies would be needed to test which of the above-mentioned hypotheses is correct.

In the water-soluble vitamin analysis (AA, Figure 1f), fruit from TSSM-infested + BT plants showed the very best AA levels (106.6 mg · 100 g of fruit- 1). On the opposite hand, fruit from TSSM-infested + CT plants presented all-time low AA levels (66.3 mg · 100 g of fruit- 1, not statistically different from control treatment). Thus, our results suggest that TSSM extinction using CT (acaricide) isn’t the foremost suitable alternative. The presence of phytophagous and/or predatory mites on the strawberry plants might be linked to high levels of vitamin C as a unconscious process since we will clearly note a relation between mite presence and high water-soluble vitamin levels. Krajnc [45] showed that concentrations of total AA were slightly increased by the moderate attack of Ips typographus in Norway spruce, while total AA values remained at control levels after the huge attack. in line with Schijlen et al. [46], vitamin C is an efficient oxygen radical scavenger, acting in plants as antioxidants and protective agents against several sources of harm (including mite infestation). Our data also suggest that biological control was highly satisfactory, generating fruit with high vitamin C levels. It seems that biological control using predatory mite can influence vitamin C accumulation, allowing the event of high-quality fruit. Amodio et al. [47] verified that organically cultivated kiwis accumulate higher vitamin C levels than chemically treated ones. However, Cayuela et al. [48] weren’t able to find any differences in vitamin C accumulation in organically or conventionally Fragaria ananassa fruit. per Lee and Kader [49], the quantity of ascorbic acid in fruits and vegetables depends on various factors like genotypic differences, preharvest climate, and postharvest handling procedures.

3.2. Leaf analyses

Most of the studies on nutritional parameters and chemical composition in strawberries are restricted to fruit analyses, with few exceptions [44,50,51]. However, strawberry leaves are important for photosynthesis and their role in sugar accumulation is well-known since sugars are primarily accumulated within the developing fruit by translocation from leaves [52]. Besides, strawberry leaves are known for his or her efficient antioxidant capacity [50].

As seen in Figure 3a, young strawberry leaves showed higher phenolic compound levels than mature (older) leaves altogether treatments. the identical pattern is additionally seen in young tea leaves, which are the selection leaves utilized in the assembly of tea thanks to their high polyphenol content [53]. We hypothesize that younger leaves produce higher levels of phenolics as a psychoanalytic process since mature strawberry leaves are after all more attacked and damaged by TSSM. Young and mature leaves under the criterion presented the very best phenolic levels, and every one other plants which had contact with TSSM (TSSM, TSSM + CT, and TSSM + BT) presented low levels of phenolic compounds. These data partially believe the abovementioned report [44], which verified a correlation between phenolic compounds and TSSM development.

Fig. 3. Phenolic Compounds (a) and Methylxanthines (b) in strawberry leaves. TSSM: TSSM + CT: Two-spotted tetranychid + Chemical Treatment; TSSM + BT: Two-spotted mite + Biological Treatment. The values are averages of 4 samples ± SE. Different letters indicate that the means are different consistent with the Tukey HSD test (P ≤ 0.05). Error bars is also too small to be visible within the figure. DW = dry weight.

Methylxanthines – namely caffeine, theobromine, and theophylline – inhibit insect feeding and are pesticides at concentrations known to occur in plants, functioning as natural insecticides [54]. In our experiments, young and mature leaves showed similar methylxanthine concentrations (Figure 3b). However, TSSM-infested leaves presented the very best values, suggesting that the synthesis of methylxanthines is stimulated by the presence of TSSM since the sole treatment with live mites at the harvesting period concerned the TSSM-infested plants. In fact, high concentrations of caffeine in young leaves of tea and occasional species act as a defense reaction to guard young soft tissues from pathogens and herbivores [55]. it’s been demonstrated that spraying tomato leaves with caffeine deters feeding by tobacco hornworms, and caffeine acts as a neurotoxin while treating cabbage leaves and orchids, killing or repelling slugs and snails [56].

In summary, this study suggests that the infestation of strawberry plants with TSSM can alter several physicochemical and nutritional properties, decreasing the standard of the fruit. On the opposite hand, plants infested with TSSM then treated with the predatory mite P. macropilis actually showed even better performance than the control plants, displaying excellent fruit quality. Therefore, the biological control of TSSM may be a safe and efficient manner to cut back the infestation of phytophagous mites and also to extend the standard of the strawberry fruit. it’s important to think about that just one cultivar was used. A study with a bigger number of cultivars could reveal other significant changes in physicochemical and nutritional parameters. However, the changes presented during this study do provide a start line for a more in-depth analysis of nutritional and physicochemical changes caused by mite infestation on strawberry plants.

Conflict of interest

Financial support
Agency/Institution: Centro Universitário UNIVATES.

The authors thank Catiane Dameda and Maira Martini for his or her technical assistance during TSSM infestation and physicochemical analyses, respectively.

Author contributions
Proposed the theoretical frame: EL, RAS, NJF, CFVS; Conceived and designed the experiments: RAS, NJF, CFVS; Contributed reagents/materials/analysis tools: EL, RAS, NJF, CFVS; Wrote the paper: EL, RAS, NJF, CFVS; Performed the experiments: EL, RAS; Analyzed the data: EL, RAS.

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