Variation of Phenolics (Bound and Free), Minerals, and Antioxidant Activity of Twenty-Eight Wild Edible Fruits of Twenty-Three Species from Far North Region of Cameroon.

The present study is aimed at investigating the variation of phenolics (bound and free), minerals, and antioxidant potentials of the wild edible fruits (fresh and dry) native from Far North Region of Cameroon. The results showed significant (p < 0.01) differences among fruits and species for all parameters. Bound phenolic content (mgGAE/100 g) of dry fruits (DF) ranged from 95.58 to 407.72; however, the contents were varied from 28.97 to 306.04 in fresh fruits (FF). Free phenolic content varied from 46.43 to 344.73 in DF and fold from 119.54 to 315.79 for those FF. Flavonoids (4.27-256.87 mg QE/100 g), tannins (3.24-63.42 mg CE/100 g), and anthocyanin content (8.65-168.10 mg C3GE/100 g) in fruits varied also significantly in respect with DF and FF. The mineral content analysis indicates that the wild fruits are rich in valuable macro- and trace elements. For antioxidant activities, except high 2.2-diphenyl-1-picyhydrazyl (DPPH) scavenging activity obtained with free phenolics, the bound phenolics of FF and DF had significantly high ferric reducing antioxidant power (FRAP) and 2,2-azino-bis(3-ethylbenzylthiozoline-6-sulphonic acid) (ABTS) scavenging activity. Furthermore, free and bound phenolic content was highly and positively correlated with ABTS, DPPH, and FRAP activities confirmed by the principal component analysis (F1×F2: 60.17%). The present study revealed that the wild edible fruits of twenty-three species investigated are important sources of bioactive compounds, natural antioxidants, and nutraceutical potential to prevent/to treat chronic diseases which could be benefits for the consumers.

1. Introduction

Many countries in the world are paying a lot of price to the well-being of their populations because of chronic noncommunicable disease threats. Although, the preventive strategies have led to some positive results; however, overweight and obesity continue to increase in all regions of the world affecting children and adults. For example, 40 million children under five in the world were overweight, and 44% of overweight children aged 5-9 were obese [1]. In sub-Saharan Africa, 48% had hypertension, 5.1% were diabetics, and 20% were suffering from obesity [2]. In Cameroon, noncommunicable diseases were accounted for 43% of all deaths [3]. Hence, it is urgent to know how traditional plant foods can be used to manage these diseases. Therefore, to better manage this burden, human beings have forgotten that the environment in which they are living provides functional food and medicines such as nonconventional edible fruits. Fact, numerous researches demonstrated that nonconventional edible fruits are good sources of important components with potential biological activities promoting health benefits especially polyphenolic compounds such as flavonoids, anthocyanins, and tannins [4, 5] as well as minerals. For Manach et al. [6], the amounts consumed of the compounds and their bioavailability on their target organs or tissues confer their high antioxidant activities. Thus, these compounds can reduce the risk of inflammatory and degenerative/noncommunicable diseases such as cancer, cardiovascular diseases, stroke, diabetes, hypertension, and obesity [7, 8].

To date, conventional fruits have been largely used instead of the wild edible fruits as the main plant foods; though, the wild edible fruits have been recognized as good nutritional and bioactive nutrients for healthier life of human [9]. Phenolics are found in most fruits and vegetables with a significant portion of the diet [10]. The health benefits of wild edible fruits are attributed to their various phenolic compounds; however, previous works have been conducted only on their soluble fractions [6]. For example, antioxidant and DNA damage protection potentials of phenolic acids have been reported by Sevgi et al. [10], for free phenolics. However, phenolic compounds are found in different forms in plant species (free, bound, or esterified), and their antioxidant efficient depends mostly on these different forms [11-13]. Also, recent studies have shown that phenolic contents in fruits differ greatly according to the ripening stages and harvesting seasons or geographical location [14, 15]. In the case of the wild edible fruits harvested throughout different seasons, there is no information on bound and free phenolic content as well their antioxidant capacities. Furthermore, the nonconventional edible fruits are eating in fresh or dry forms, while others are eating both in their fresh and dry forms. Since these edible forms of nonconventional fruits exist, data reflecting the variation of their bioactive compounds and antioxidant potentials between these edible forms are also very scare in the literature. The wild edible fruits may be important source of bound phenolics, essential minerals, and antioxidant properties as well as nutraceutical potential to reduce diseases.

Therefore, the present study is aimed at investigating the phenolics (free and bound) and minerals of twenty-eight wild edible fruits of twenty-three species harvested both for dry and fresh forms throughout dry and rainy seasons and also to evaluate their antioxidant potentials. To the best of our knowledge, the present study is the first report regarding the contents of bioactive compounds (bound and free) and minerals of the most consumed wild fruits among 68 species collected and linked to the traditional diet of the population from Far North Region of Cameroon.

2. Material and Methods

2.1. Samples and Sampling Sites

Twenty-three species among 68 of wild edible fruits investigated because these are mostly appreciated and consumed, and there are also usually transformed in some byproducts as well for selling across other regions or countries by local population from Far North Region of Cameroon (Figure 1). Fruits were picked throughout the different locations from 23rdApril 2019 to 25th April 2020 during the dry (November to April: 23-45°C) and rainy (May to October: 20-35°C) seasons. These fruits have been selected because of their many therapeutic effects to treat headache, diabetes types 2, obesity, kidney failure, cancer, and hypertension and have potential antioxidant and antimicrobial properties as results of the survey conducted by our teams in 2019 (Table 1). Two types of fruits forms were used for the present study. Fruits eaten only in the fresh form were Vitex diversifolia, Vitellaria paradoxa, Haematostaphis barteri, Annona senegalensis, Ximenia americana, Ziziphus mauritiana, Cordia sinensis, Hyphaene thebaica, Carissa edulis, Ziziphus sipna-christi, Ficus dicranostyla, Afrostyrax lepidophyllus, Hexabolus monopetalus, Borassus aethiopium, Diospyrus mespiliformis, and Phoenix reclinatum; however, those eaten in the dry form were Detarium microcarpum, Parkia biglobosa, Ziziphus mauritiana, Balanites aegyptiaca, Diospyrus mespiliformis, Tamarindus indica, Adansonia digitata, Ziziphus spina-christi, Phoenix reclinatum, and Hyphaene thebaica, while,fruits from Z. mauritiana, H. thebaica, Z. sipna-christi, D. mespiliformis, and P. reclinatum species were consumed both in dry and fresh forms. Eleven species of fruits such as V. diversifolia, V. paradoxa, H. monopetalus, B. ethiopium, V. doniana, V. grandifolia, H. barteri, A. senegalensis, X. americana, A. lepidophyllus, and C. edulis were harvested in rainy season, whereas twelve other fruits were harvested in the dry season. Fresh fruits were harvested at the last stage of the maturity; however, the dry fruits were picked in dried form from the trees plant directly. Some samples of twenty-eight fruits of twenty-three species are presented in Figure 2. The fresh fruits were kept in cooler box; however, the dry fruits were packed in polystyrene bags before transporting to the Laboratory of Biochemistry and Biological Chemistry (LabBBC) of the University of Maroua, Cameroon.

Figure 1

Site location map from Far North Region of Cameroon.

Table 1

Ethnopharmacological effects of different wild edible fruits.

Botanical names	Family	Morphology	Ethnopharmacology effects
Ziziphus mauritiana	Rhamnaceae	Shrub	Antidysentery, against jaundice, Amibiae
Ziziphus spina-christi		Tree	Against jaundice, antibacterial
Carissa edulis	Boraginaceae	Shrub	Abdominal pain reliever, against jaundice and constipation
Tamarindus indica	Caesalpiniaceae	Tree	Antihypertension, against constipation and indigestion, antipyretic, aphrodisiac
Detarium microcarpum		Tree	Antianorexia, against kidney problem, antiamenorrhea
Parkia biglobosa	Mimosaceae	Tree	Against constipation and cough, antibacterial
Balanites aegyptiaca	Balanitaceae	Tree	Against constipation and kidney failure, antidysentery, against undigestion, aphrodisiac, abdominal pain reliever, antileprotic, antidiabetic
Phoenix reticulatum	Arecaceae	Tree	Antidiarrheal, abdominal pain reliever
Hyphaene thebaica		Tree	Antihypertension, against constipation, indigestion and asthenia
Borassus eathiopium		Tree	Against constipation and anemia
Vitex grandifolia	Verbenaceae	Shrub	Abdominal pain reliever
Vitex doniana		Shrub	Againts asthenia and constipation, abdominal pain reliever, antiemetic
Vitex diversifolia		Shrub	Against cough and anorexia
Vitellaria paradoxa	Sapotaceae	Tree	Antidiarrheal, against anemia
Ximenia Americana	Olacaceae	Shrub	Against constipation and anemia, undigestion
Afrostyrax lepidophyllus	Huaceae	Shrub	Antibacterial, antistomachic, preservative, antimeasles and against mumps
Haematostaphis Barteri	Anacardiaceae	Tree	Anemia, antigastritis, headache
Ficus dicranostyla	Moraceae	Tree	Antianorexia, against jaundice
Annona senegalensis	Annonaceae	Shrub	Against constipation
Hexabolus monopetalus		Tree	Against kidney problems, anti-inflammatory
Adansonia digitata	Bombacaceae	Tree	Antiagalactia, against asthenia
Diospyros mespiliformis	Ebenaceae	Tree	Antidiarrheal, against jaundice
Cordia sinensis	Apocynaceae	Shrub	Antianemia, antiscurvy

Figure 2

Some samples of wild edible fruits (dry and fresh forms) among 23 species.

2.2. Sample Preparation

Plant species and fruits were identified and authenticated at the Department of Biological Sciences of the University of Maroua (Cameroon) by Prof. Tchopsala (botanist). After this, at least 30 fruits of each species were combined in three repetitions. Then, they were washed three times with tap water, and the pulps of each fruit samples were separated from kernels and pericarps using stainless steel knives (Koch Messer, Germany). Then, pulp of each fruit samples was weighted in triplicates and dried in an air oven (Binder, USA) at 60°C for 24 hours. After that, samples were powdered using a mortar, sieved (200 μm), and stored in airtight polystyrene bags, then put into opaque box at room temperature until analysis.

2.3. Reagents and Chemicals

Standard (98% >) such as Gallic acid, Quercetin, Catechin, Trolox, Cyanidin-3-glucoside, and also Vanillin, Trolox, ABTS, and DPPH was purchased through Sigma-Aldrich Chemical Company (Mumbai, India). Sodium carbonate, methanol, ethanol, and other solvents were obtained from Fisher commercial source (New Jersey, USA).

2.4. Extraction of Free and Bound Phenolic Compounds

The polyphenols were extracted as described by Laya and Koubala [13]. The amount of 0.2 g of fruit powder was mixed with 10 mL of 80% methanol and stirred for 24 hours at room temperature. After shaking, the mixture was filtered with No. 4 Whatman filter paper, and the filtrate was collected. Then, the residue was washed one more before combining the filtrates for the free phenolic fraction and kept at -4°C. For the bound phenolics, the residues were hydrolyzed with 4 mL of 2 M NaOH and incubated for 15 min in a water bath at 80°C. The mixture were cooled at room temperature and added to 2.5 mL of 2 M HCl before incubating again in a water bath for 45 min at 80°C. Then, 2.5 mL of 95% methanol was added, and the mixture was stirred for 15 min. The mixture was filtered through Whatman No. 4 filter paper before washing two times with 2.5 mL of 95% methanol. The filtrates obtained were combined for the bound phenolics and kept at -4°C until analysis.

2.5. Determination of Phenolic (Bound and Free) Compounds

2.5.1. Total Polyphenol Content

Polyphenol (bound and free) content of the methanolic extract was determined using the Folin-Ciocalteu colorimetric method described by Singleton et al. [16]. The absorbance of phenolic compounds was measured at 745 nm using UV-VIS spectrophotometer (PRIM Light & Advanced, Germany). The calibration curve was plotted with gallic acid (0-250 μg/mL; R2 = 0.9921). The results were expressed in milligram gallic acid equivalent per 100 grams edible portion (mg GAE/100 g).

2.5.2. Flavonoid Content

Flavonoid (bound and free) contents of the methanolic extract were determined using the vanillin-HCl reagent as described by Brainbridge et al. [17]. The absorbance was measured at 430 nm. The calibration curve was plotted with quercetin (0-100 μg/mL; R2 = 0.9924). The results were expressed in milligram quercetin equivalent per 100 grams edible portion (mg QE/100 g).

2.5.3. Tannin Content

Tannin (bound and free tannin) contents of the methanolic extract were determined using aluminium chloride as described by Gaytan-Martínez et al. [18]. The tannin content was measured at 500 nm. The calibration curve was plotted with catechin (0-100 μg/mL; R2 = 0.9879), and the results were expressed in milligram catechin equivalent per 100 grams edible portion (mg CE/100 g).

2.5.4. Determination of Total Anthocyanins

Total anthocyanins (TA) were determined by the differential pH method as described by Lee et al. [19]. Shortly, 0.100 g of powder samples was mixed with 20 mL of acidic ethanol (HCl 0.001 N; pH 4.0), and the mixture was shaken for 1 h at room temperature. Then, the mixture was filtered through No. 4 Whatman paper filter. The filtrate was diluted with HCl/KCl (0.025 M; pH 1.0) and acetate (0.4 M; pH 4.5) buffers. After that, 200 μL of diluted sample was pipetted and mixed in 1.8 mL of 25 mM HCl/KCl (pH 1.0) and 0.4 M acetic acid/sodium acetate (pH 4.5). Cyanidin-3-glucoside was used as standard, and the absorbance (A) of sample was measured at 520 and 700 nm at pH 1.0 and 4.5 buffers after 30 min of incubation, respectively, according to the following formula:

where A = (A520 − A700)pH 1.0 − (A520 − A700)pH4.5

The calibration curve was plotted with cyanidin-3-glucoside (0-250 μg/mL; R2 = 0.9966). The results were expressed in milligram cyanidin-3-glucoside equivalent per 100 grams edible portion (mg C-3G E/100 g).

2.6. Minerals Determination

Mineral content in all fruits was determined using AAS wet digestion as described by Pinta et al. [20].

2.7. Evaluation of Antioxidant Activities of Phenolic (Free and Bound) Content

2.7.1. DPPH (2.2-Diphenyl-1-Picyhydrazyl) Radical Scavenging Activity

DPPH was carried out as described by Sun et al. [21] with some modifications. Briefly, 500 μL of methanolic sample (0.1 g/mL) or standard was mixed with 1500 μL of 1 mM DPPH, and the mixture was stirred for 2 min before incubating for 40 min at room temperature in the dark place. The experiments were done in four repetitions. Absorbance of the mixture was measured at 517 nm. The calibration curve was plotted with trolox (0-200 μg/mL; R2 = 0.9882), and the results were expressed in milligram trolox equivalent per 100 grams edible portion (mg TE/100 g).

2.7.2. ABTS (2,2-Azino-Bis(3-Ethylbenzylthiozoline-6-Sulphonic Acid)) Radical Scavenging Activity

ABTS was performed as described by Re et al. [22]. Briefly, 500 μL of each methanolic sample (0.1 g/mL) or standard was mixed with 1500 μL of 7 mM ABTS+, and the mixture was shaken for 2 min before incubating for 40 min at room temperature. The experiments were done in four repetitions. Then, the absorbance was measured at 745 nm. The calibration curve was plotted with trolox (0-200 μg/mL; R2 = 0.9883), and the results were expressed in milligram trolox equivalent per 100 grams edible portion (mg TE/100 g).

2.7.3. FRAP (Ferric Reducing Antioxidant Power)

FRAP was determined as described by Benzie and Strain [23]. Briefly, 500 μL of methanolic sample (0.1 g/mL) or standard was mixed with 1500 μL of FRAP reagent (250 μL of acetate buffer 0.3 M, pH 3.6, 225 μL of TPTZ 0.01 M in 40 mM HCl, and 225 μL of FeCl3 140 mM). The experiments were done in four repetitions. Then, the mixture was shaken and incubated for 40 min at room temperature. The absorbance of the mixture was measured at 593 nm. The calibration curve was plotted with trolox (0-50 μg/mL; R2 = 0.9884), and the results were expressed in milligram trolox equivalent per 100 grams edible portion (mg TE/100 g).

2.8. Statistical Analysis

Data were analyzed using one-way analysis of variance (ANOVA) performed by SPSS 20.0 (Inc., Chicago, IL, USA) and Graph Pad Prism 5.03, and the significance at p < 0.01 between all parameters was done using Tukey's tests. Pearson's correlation and principal component analysis (PCA) using XLSTAT (version 16) were done in order to establish the relationship between antioxidant activities and polyphenol content. The results are the mean of four replications expressed as mean ± standard error.

3. Results and Discussion

3.1. Phenolic Compounds of 28 Wild Edible Fruits of the Twenty-Three Species

3.1.1. Variation of Total Phenolic (Free and Bound) Content of Wild Edible Fruits

The bound fraction of polyphenols of 28 fruits studied ranged between 95.58 (A. digitata) and 407.72 mg GAE/100 g (B. eagyptiaca); however, the free fraction of polyphenol content varied from 46.43 (T. indica) to 344.73 mg GAE/100 g (B. eagyptiaca) among the dry fruits (Table 2), while the bound polyphenol content ranged from 28.97 (V. grandifolia) to 306.04 mg GAE/100 g (H. thebaica) among the fresh fruits. These variations may be due to the plant species which may able to accumulate less or more the bound and the free phenolics. In comparison to the other studies, the values of the bound polyphenol content of all fruits were higher than those for miracle fruits (5.63 mg/100 g) reported by Inglett and Chen [24]. However, H. monopetalus (119.54 mg GAE/100 g) and Z. mauritiana (315.79 3 mg GAE/100 g) showed the highest and the lowest free polyphenol content (Table 2). Additionally, miracle fruit (16.95 mg/100 g) had higher content of free polyphenols than H. monopetalus (119.54 mg GAE/100 g) and lower than the other fresh fruits as compared to the present study. This result can be related to the methods used for quantification of the phenolics from fruits collected in different areas.

Table 2

Polyphenolic (bound and free) compounds (mg/100 g EP) of twenty-eight wild edible fruits of twenty-three species.

Fruits		Total polyphenols (mg GAE/100 g)		Total flavonoids (mg QE/100 g)		Total tannins (mg CE/100 g)		Anthocyanins (mg C3GE/100 g)
		Free fraction	Bound fraction	Free fraction	Bound fraction	Free fraction	Bound fraction
Dry	Zma	94.00 ± 0.15n	142.41 ± 0.38k	26.42 ± 0.07l	107.20 ± 0.11e	8.28 ± 0.15g	4.76 ± 0.08f	14.01 ± 0.55ij
	Pbi	247.83 ± 0.25f	270.79 ± 0.21d	189.88 ± 0.33b	159.37 ± 0.11c	16.05 ± 0.06e	57.79 ± 0.16a	129.38 ± 0.30b
	Dmi	146.43 ± 0.10l	194.96 ± 0.23h	116.46 ± 0.04e	135.73 ± 0.34c	6.26 ± 0.06fg	41.18 ± 0.03b	168.10 ± 0.53a
	Bae	344.73 ± 0.33b	407.72 ± 0.12a	208.56 ± 0.64a	256.87 ± 0.43a	63.42 ± 0.95a	3.24 ± 0.63f	164.18 ± 0.64a
	Pre	309.59 ± 0.22cd	159.05 ± 0.60jk	203.76 ± 0.93a	89.59 ± 0.39g	27.87 ± 0.62c	10.28 ± 0.76e	167.98 ± 0.57a
	Ada	296.02 ± 0.36d	95.58 ± 0.04m	187.34 ± 0.82b	45.68 ± 0.87j	42.35 ± 0.43b	22.31 ± 0.06d	86.45 ± 0.56d
	Zsp	169.12 ± 0.81k	271.40 ± 0.16d	98.65 ± 0.03f	127.56 ± 0.93d	11.56 ± 0.34ef	32.64 ± 0.53cd	100.76 ± 0.94c
	The	238.54 ± 0.65f	332.45 ± 0.43b	176.23 ± 0.63c	214.62 ± 0.21b	20.51 ± 0.67d	52.78 ± 0.68ab	126.65 ± 0.32b
	Dme	56.43 ± 0.06o	178.71 ± 0.08i	22.48 ± 0.02lm	104.70 ± 0.05ef	4.19 ± 0.02gh	4.29 ± 0.07f	39.76 ± 0.75g
	Tam	46.43 ± 0.10o	208.03 ± 0.23gh	14.90 ± 0.07n	135.23 ± 0.08c	12.51 ± 0.02ef	56.83 ± 0.08a	23.96 ± 0.56h
Fresh	Vdi	138.14 ± 0.09l	214.26 ± 0.01g	19.46 ± 0.07f	29.81 ± 0.11j	12.47 ± 0.04ef	13.17 ± 0.03e	94.15 ± 0.24cd
	Vpa	272.35 ± 0.18e	230.21 ± 0.08ef	40.71 ± 0.08j	7.53 ± 0.02lm	21.04 ± 0.03d	8.10 ± 0.02ef	20.40 ± 0.57hi
	Hba	214.25 ± 0.01hi	137.54 ± 0.02k	35.66 ± 0.00k	26.40 ± 0.01jl	1.04 ± 0.00i	8.73 ± 0.01ef	19.15 ± 0.90hi
	Ase	246.02 ± 0.12f	216.57 ± 0.12gf	19.44 ± 0.05mn	95.08 ± 0.09f	17.01 ± 0.04ed	7.39 ± 0.04ef	45.39 ± 0.60g
	Xam	252.69 ± 0.06f	223.39 ± 0.04f	63.54 ± 0.04hi	17.17 ± 0.03l	4.84 ± 0.01gh	1.29 ± 0.01g	8.65 ± 0.15j
	Pre	209.30 ± 0.31i	149.15 ± 0.37jk	143.73 ± 0.45d	4.27 ± 0.03m	29.56 ± 0.23c	3.46 ± 0.52f	98.95 ± 0.86c
	Afl	189.48 ± 0.44j	229.75 ± 0.02ef	27.45 ± 0.65kl	89.34 ± 0.34g	12.36 ± 0.42ef	26.62 ± 0.12c	79.55 ± 0.10df
	Vdo	184.07 ± 0.11j	169.36 ± 0.38ij	56.46 ± 0.18i	28.92 ± 0.41j	9.35 ± 0.21gf	2.67 ± 0.38fg	48.59 ± 0.37g
	Fid	230.75 ± 0.25g	203.32 ± 0.12h	77.36 ± 0.82g	68.46 ± 0.56i	14.24 ± 0.25ef	7.35 ± 0.08ef	49.76 ± 0.83g
	Csi	292.30 ± 0.17d	234.06 ± 0.01e	43.93 ± 0.52j	12.45 ± 0.73kl	22.40 ± 0.27dc	1.95 ± 0.46fg	15.84 ± 0.30i
	Vgr	202.60 ± 0.42i	28.97 ± 0.15n	77.23 ± 0.30g	9.34 ± 0.37l	16.20 ± 0.52e	3.85 ± 0.74f	11.35 ± 0.77ij
	Boe	168.62 ± 0.12k	212.18 ± 0.32g	23.42 ± 0.76lm	79.56 ± 0.45hi	6.15 ± 0.65g	13.16 ± 0.86e	12.01 ± 0.84ij
	Dme	269.50 ± 0.31e	295.18 ± 0.16c	79.43 ± 0.34g	14.67 ± 0.25k	17.42 ± 0.23ed	11.98 ± 0.67e	79.97 ± 0.43df
	Hmo	119.54 ± 0.43m	143.87 ± 0.52k	67.34 ± 0.52h	8.21 ± 0.17l	13.14 ± 0.39ef	2.35 ± 0.07b	15.31 ± 0.41i
	Hte	378.39 ± 0.09a	306.04 ± 0.42c	82.36 ± 0.10g	135.37 ± 0.61c	35.72 ± 0.50bc	14.32 ± 0.35e	73.67 ± 0.48e
	Zsp	229.50 ± 0.13g	121.89 ± 0.34l	93.03 ± 0.45fg	74.30 ± 0.12hi	12.23 ± 0.65ef	4.56 ± 0.29f	67.85 ± 0.12e
	Zma	315.79 ± 0.23c	270.46 ± 0.17d	76.35 ± 0.17g	32.18 ± 0.72j	6.89 ± 0.26fg	3.51 ± 0.18f	25.17 ± 0.16h
	Ced	218.12 ± 0.14h	154.90 ± 0.04j	69.45 ± 0.23gh	25.86 ± 0.24jl	17.38 ± 0.60ed	8.23 ± 0.54ef	19.89 ± 0.76hi

Dmi: Detarium microcarpum; Pbi: Parkia biglobosa; Zma: Ziziphus mauritiana; Bae: Balanites eagyptiaca; Dme: Diospyrus mespiliformis; Tam: Tamarindus indica; Ada: Adansonia digitata; Zsp: Ziziphus spina-christi; Pre: Phoenix reclinatum; Hts: Hyphaene thebaica; Vdi: Vitex diversifolia; Vpa: Vitellaria paradoxa; Hba: Haematostaphis barteri; Ase: Annona senegalensis; Xam: Ximenia americana; Csi: Cordia sinensis; Ced: Carissa edulis; Fid: Ficus dicranostyla; Ale: Afrostyrax lepidophyllus; Hmo: Hexabolus monopetalus; Boe: Borassus aethiopium. Values are the means ± SE with four replicates per specie. mgEGA/100 g: milligrams equivalent gallic acid per 100 grams edible portion; mgEQ/100 g: milligram equivalent quercetin per 100 grams edible portion; mgECat/100 g: milligram equivalent catechin per 100 grams edible portion; mg C3GE/100 g: milligram equivalent cyanidin-3-glucoside per 100 grams edible portion. In the same column, values followed by different superscript letters are significantly different (p < 0.01).

The free and bound polyphenol content evaluated for these edible fruits showed that free and bound polyphenol content varied significantly (p < 0.01) among fruit species (Table 2), which is in agreement with what have been observed by many authors [14, 25]. Moreover, all the dry fruits showed the highest values of bound polyphenol contents than the fresh edible fruits (Table 2). Similarly, Imeh and Khokhar [25] have reported in the literature that the amounts of bound polyphenol fraction of cultivated fruits were higher in dry fruits than in fresh fruits. Besides, Arruda et al. [26] found that the bound polyphenol content was the main polyphenol fraction in fresh A. crassiflora pulp. In contrast, Inglett and Chen [24] and Su et al. [14] found that the free phenolic compounds were higher in fresh miracle and litchi fruits than their bound fractions, respectively, suggesting that the free and bound polyphenol content varied according to the fruit species. In addition, Su et al. [14] found that litchi pulp contained higher content (190.69 mg GAE/100 g) of free polyphenols.

Therefore, P. biglobosa pulp has higher free polyphenol content (247.83 mg GAE/100 g) than that in litchi pulp as compared to the results reported by Su et al. [14]. According to its bound fraction, litchi pulp has the lowest bound polyphenol content (61.27 mg GAE/100 g) compared to that obtained in A. senegalensis (216.57 mg GAE/100 g). Furthermore, except P. biglobosa among the dry fruits and V. paradoxa and X. americana among the fresh fruits, other fruits show higher bound polyphenol content than their free fraction (Table 2). The difference for both fractions of polyphenol content may be due to the different factors such as climatic variations, ripeness at the harvest time, genetic factors, and variations in sunlight exposure [12, 27]. This higher content of bound phenolics in fruits may be benefit for the consumers because this fraction of phenolics is more active than the free [28]. Furthermore, many researchers reported that the bound phenolics can be released continuously through the gastrointestinal tract [13] and after bacterial fermentation, their bioaccesssibility and bioavailability will be high which can be used for long time for positive effects [29, 30].

3.1.2. Total Flavonoid (Bound and Free) Content of Wild Edible Fruits

Total flavonoid content was also significantly (p < 0.01) varied among the different fruits species (Table 2). Bound flavonoid content ranged from 45.68 (A. digitata) to 256.87 mg QE/100 g (B. aegyptiaca); however, the free flavonoid content varied between 14.90 (T. indica) and 208.56 mg QE/100 g (B. aegyptiaca) among the dry fruits, while the bound flavonoid content of fresh fruits ranged from 4.27 (P. reticulatum) to 95.08 mg QE/100 g (A. senegalensis). Total free flavonoid content ranged between 19.44 (A. senegalensis) and 143.73 mg QE/100 g (P. reticulatum) (Table 2). The results showed that total bound flavonoid content of all fruits in the present study was higher than that observed in A. crassiflora pulp (0.28 mg QE/100 g) by Arruda et al. [26]. Except P. biglobosa among the dry fruits and V. paradoxa among the fresh fruits, other fruits had higher total bound flavonoid content than their free fraction of flavonoid content (Table 2). This result is in agreement with Arruda et al. [26], who found that A. crassiflora had higher total flavonoid content in its bound form. The difference in bound and free flavonoid content in plants was attributed to the genetic factors and environmental factors [12].

3.1.3. Total Tannin (Bound and Free) Contents of Wild Edible Fruits

Total tannin content was significantly (p < 0.01) varied in respect with the dry and fresh edible fruits (Table 2). The bound fraction of tannin content ranged between 3.24 (B. aegyptiaca) and 57.79 mg CE/100 g of edible portion (Z. mauritiana) for the dry fruits, while its free forms ranged from 4.19 (D. mespiliformis) to 63.42 mg CE/100 g (B. aegyptiaca). However, the fresh fruits showed free tannin content ranging from 1.04 to 35.72 mg CE/100 g (H. thebaica), while the bound tannin content ranged between 1.29 (X. america) and 26.62 mg CE/100 g (A. lepidofillus) (Table 2). The results showed that H. thebaica has higher free tannin content than those found in litchi fruit (14.32 mg CE/100 g) analyzed by Su et al. [14].

Also, litchi fruit contains higher content of bound tannins (37.37 mg CE/100 g) than that obtained for the fresh fruits in the present study. These results demonstrate that tannins content of all fruits was higher than that found in B. sapida (0.372 mg CE/100 g) by Oyeleke et al. [31] during their study. These can be due to the ripeness at the time of harvest, and environmental factors such as soil type, sun exposure, rainfall, and storage conditions could be among those factors which may affect the polyphenol content in bound and free fraction of plants other than species [6]. However, the quantification of free and bound polyphenol content in wild edible fruits of the present study may provide systematic estimation of biological activities, including beneficial health effects and industrial purposes [12]. According to Li et al. [32], these wild fruits could be used as a good bioactive elements as the functional food in order to manage various diseases or use in pharmaceutical and cosmetic industries.

3.1.4. Total Anthocyanin Content of Wild Edible Fruits

Found in most plant species, anthocyanin content of fruits ranged from 8.65 (X. america) to 98.95 μg C-3G E/100 g (P. reticulatum) among fresh fruits, while it ranged between 14. (Z. mauritiana) and 168.10 μg C3G E/100 g (D. mespiliformis) among the dry fruits (Table 2). These significant difference variations among fruits were linked with the genetic factors of the species. When compared to the work of Prvulović et al. [33], D. mespiliformis has higher total anthocyanin content than P. avium, which values ranged between 0.35 and 0.69 mg C-3G E of total anthocyanin content. Fact, the fruits with high anthocyanins content may be responsible for some biological activities including the prevention or lowering the risk of cardiovascular disease, diabetes, arthritis, and cancer [34]. These fruits can be a potential ingredient for new functional food products.

3.2. Antioxidant Activities of Phenolic (Free and Bound) Content of Wild Edible Fruits

Antioxidant potentials of wild fruits were evaluated by DPPH, ABTS, and FRAP methods for both bound and free fractions of phenolics. Antioxidant potentials exhibited by free and bound polyphenols of the fruits evaluated by DPPH, ABTS, and FRAP methods varied significantly (p < 0.01) among the species and edible forms of fruits (Table 3). The variations of the results of antioxidant capacities evaluated by the same methods were reported by many researchers [35, 36]. These variations in antioxidant activity may be due to the different modes of action of the in vitro assays used. Free polyphenols of D. microcarpum (120.94 mg TE/100 g) and P. biglobosa (784.54 mg TE/100 g) showed higher and lower DPPH radical scavenging activity for the dry fruits, respectively. However, V. diversifolia (40.86 mg TE/100 g) and H. barteri (82.71 mg TE/100 g) had the lowest and the highest values of DPPH radical scavenging among the fresh fruits. The results were in agreement with Pérez-Balladares et al. [37], who found in their study high variation of DPPH radical scavenging activity among fruits, while the bound polyphenols of dry fruits exhibited DPPH radical scavenging activity ranging between 58.88 (D. msepiliformis) and 559.35 mg TE/100 g (Z. mauritiana).

Table 3

Antioxidant activities of polyphenolic (free and bound) compounds (mg TE/100 g EP) of twenty-eight wild edible fruits.

Fruits		DPPH		ABTS		FRAP
		Free fraction	Bound fraction	Free fraction	Bound fraction	Free fraction	Bound fraction
Dry	Zma	172.68 ± 0.10g	559.35 ± 0.54a	261.39 ± 0.44ij	344.40 ± 0.54a	233.58 ± 0.26h	425.53 ± 0.10d
	Pbi	784.54 ± 0.55a	239.43 ± 0.22c	379.09 ± 0.82e	286.61 ± 0.44b	225.77 ± 0.23h	322.43 ± 0.13fg
	Dmi	120.94 ± 0.22j	73.64 ± 0.58p	700.32 ± 0.82b	263.45 ± 0.30c	132.88 ± 0.26l	313.41 ± 0.21g
	Bae	34.56 ± 0.56u	245.78 ± 0.78e	167.34 ± 0.87m	89.03 ± 0.45i	172.12 ± 0.76jk	193.60 ± 0.12m
	Pre	78.56 ± 0.23m	64.67 ± 0.09q	325.98 ± 0.45f	36.04 ± 0.56t	387.65 ± 0.73d	332.76 ± 0.02f
	Ada	128.65 ± 0.69i	76.43 ± 0.39o	146.77 ± 0.36o	53.72 ± 0.67r	98.63 ± 0.37o	196.64 ± 0.56m
	Zsp	254.98 ± 0.45e	98.45 ± 0.84k	45.67 ± 0.56a	167.82 ± 0.63f	345.07 ± 0.13e	132.75 ± 0.63o
	The	156.67 ± 0.78f	128.53 ± 0.34i	66.43 ± 0.72u	48.21 ± 0.16s	452.64 ± 0.52b	276.87 ± 0.46i
	Dme	405.76 ± 0.42d	158.88 ± 0.07g	265.97 ± 0.28h	86.22 ± 0.10j	313.62 ± 0.25f	52.99 ± 0.07q
	Tam	740.45 ± 0.15b	58.49 ± 0.21r	463.10 ± 0.40d	105.26 ± 0.01h	537.70 ± 0.43a	653.12 ± 0.08a
Fresh	Vdi	40.86 ± 0.01t	58.24 ± 0.09b	96.06 ± 0.20st	74.71 ± 0.15m	276.31 ± 0.04g	451.09 ± 0.05c
	Vpa	49.39 ± 0.10s	80.90 ± 0.17mn	103.06 ± 0.18q	62.67 ± 0.06o	174.05 ± 0.31jk	223.86 ± 0.10kl
	Hba	62.71 ± 0.08q	76.07 ± 0.00n	67.34 ± 0.05u	21.86 ± 0.01v	79.41 ± 0.03p	113.37 ± 0.01p
	Ase	48.04 ± 0.13bc	92.90 ± 0.20l	107.45 ± 0.27q	103.08 ± 0.15h	350.43 ± 0.21e	468.89 ± 0.16c
	Xam	68.56 ± 0.10p	56.36 ± 0.15r	63.65 ± 0.10v	59.93 ± 0.17p	185.66 ± 0.04j	237.06 ± 0.03k
	Pre	53.75 ± 0.46r	83.48 ± 0.27m	187.67 ± 0.35l	209.30 ± 0.31d	349.15 ± 0.37e	143.73 ± 0.45o
	Afl	87.23 ± 0.16fg	96.48 ± 0.67kl	167.43 ± 0.23m	89.48 ± 0.44i	129.75 ± 0.02l	327.45 ± 0.65f
	Vdo	77.37 ± 0.27no	92.35 ± 0.45l	987.23 ± 0.19a	84.07 ± 0.11k	69.36 ± 0.38pq	256.46 ± 0.18j
	Fid	138.03 ± 0.47h	73.72 ± 0.17p	543.36 ± 0.82c	30.75 ± 0.25u	103.32 ± 0.12o	17.36 ± 0.82r
	Csi	76.34 ± 0.69o	143.46 ± 0.45h	92.34 ± 0.11t	78.30 ± 0.17l	34.06 ± 0.01r	514.93 ± 0.52b
	Vgr	84.56 ± 0.26l	203.38 ± 0.23f	314.50 ± 0.35g	102.60 ± 0.42h	128.97 ± 0.15lm	177.23 ± 0.30n
	Boe	97.45 ± 0.62k	133.83 ± 0.34i	245.48 ± 0.62k	68.62 ± 0.12n	112.18 ± 0.32n	223.42 ± 0.76kl
	Dme	634.03 ± 0.47c	279.45 ± 0.22d	243.87 ± 0.72k	169.50 ± 0.31e	95.18 ± 0.16o	179.43 ± 0.34n
	Hmo	52.65 ± 0.12rs	35.46 ± 0.34m	152.87 ± 0.56n	119.54 ± 0.43g	43.87 ± 0.52r	67.34 ± 0.52q
	The	66.27 ± 0.36p	76.42 ± 0.42o	65.67 ± 0.83uv	78.39 ± 0.09l	206.04 ± 0.42i	182.36 ± 0.10mn
	Zsp	52.02 ± 0.47c	73.63 ± 0.74p	98.35 ± 0.62r	89.50 ± 0.13i	121.89 ± 0.34m	293.03 ± 0.45gh
	Zma	78.37 ± 0.49mn	98.72 ± 0.98k	256.87 ± 0.54j	115.79 ± 0.23gh	70.46 ± 0.17pq	376.35 ± 0.17e
	Ced	227.48 ± 0.23i	378.81 ± 0.37b	123.78 ± 0.52p	118.12 ± 0.14g	413.90 ± 0.04c	169.45 ± 0.23n

Dmi: Detarium microcarpum; Pbi: Parkia biglobosa; Zma: Ziziphus mauritiana; Bae: Balanites eagyptiaca; Dme: Diospyrus mespiliformis; Tam: Tamarindus indica; Ada: Adansonia digitata; Zsp: Ziziphus spina-christi; Pre: Phoenix reclinatum; Hts: Hyphaene thebaica; Vdi: Vitex diversifolia; Vpa: Vitellaria paradoxa; Hba: Haematostaphis barteri; Ase: Annona senegalensis; Xam: Ximenia americana; Csi: Cordia sinensis; Ced: Carissa edulis; Fid: Ficus dicranostyla; Ale: Afrostyrax lepidophyllus; Hmo: Hexabolus monopetalus; Boe: Borassus aethiopium. Values are the means ± SE with four replicates per specie, and results were expressed in milligram equivalent trolox per 100 grams edible portion (mgET/100 g EP). In the same column, values followed by different superscript letters are significantly different (p < 0.01).

Also, DPPH radical scavenging activity of bound polyphenols from fresh fruits was ranged from 12.07 (H. barteri) to 302.90 mg TE/100 g (A. senegalensis) (Table 3). The highest DPPH radical scavenging activity was shown by Detarium microcarpum (120.94 mg TE/100 g) and Diospyrus mespiliformis (58.88 mg TE/100 g) conferring by free and bound polyphenol amount, for the dry fruits, respectively. Among fresh fruits, H. barteri (12.07 mg TE/100 g) and V. diversifolia (40.86 mg TE/100 g) showed the highest DPPH radical scavenging activity by their bound and free polyphenols, respectively. Yang et al. [12] reported that antioxidant activities of fruit species could greatly vary according to the distribution of their polyphenol form. For both fractions, bound polyphenol content of most fruits such as D. mespiliformis, T. indica, and H. barteri showed the strongest DPPH radical scavenging activity compared to their free fraction (Table 3). This finding is in agreement with Arruda et al. [26], who found that the bound polyphenols of A. crassiflora fruit showed higher antioxidant activity than free polyphenols. Similarly, Laya and Koubala [13] were found that bound polyphenols of cassava leaves showed higher DPPH radical scavenging activity than free polyphenol fraction. The highest DPPH radical savenging may linked to flavonoid content in fruits known as free radical scavengers preventing oxidative cell damage and having strong anticancer activity [38].

Furthermore, result of ABTS radical scavenging activity indicated that the free and bound polyphenols of dry fruits were stronger in Z. mauritiana (261.39 mg TE/100 g) and D. mespiliformis (86.22 mg TE/100 g), respectively (Table 3). However, X. americana (63.65 mg TE/100 g) and H. barteri (21.86 mg TE/100 g) among the fresh fruits showed the highest activity for free and bound polyphenols, respectively. Thus, ABTS radical scavenger was offered stronger activity with bound polyphenolic compounds in the dry and fresh fruits than its free fraction. Fact, phenolic acids are known as strong antioxidant compounds and can scavenge almost all oxidant molecules such as free radicals via their hydroxyl groups [10]. This may be justified by their higher content than their free amounts. Moreover, based on FRAP assays, free and bound polyphenols of T. indica (537.70 mg TE/g) and Z. mauritiana (425.53 mg TE/100 g) had a stronger antioxidant activities among the dry fruits, respectively.

In addition, the free (350.43 mg TE/100 g) and bound polyphenols (268.89 mg TE/g) of A. senegalensis showed the highest activity among the fresh fruits (Table 3). Compared to previous findings reported by Imeh and Khokhar [25] on apple cultivars (1.83 to 2.89 mg TE/100 g) and Kiwi (1.57 mg TE/100 g) FRAP values, their values were lower than those found in all fruits investigated in the present study. This variation in total antioxidant among fruits species was reported by Pérez-Balladares et al. [39] on various fruits. Also, the bound polyphenols of Z. mauritiana, P. biglobosa, and D. microcarpum among dry fruits have the highest ability to reduce ferric ions than their free forms. Except H. barteri, the free polyphenols of the other fresh fruits showed higher antioxidant capacity than their bound forms, suggesting that these fruits may be very important for consumers because of the longer effect of bound phenols in human body. Fact, the bound phenolics are releasing in the slower manner in the intestine and their bioactivity is higher than free phenolics. These species of wild edible fruits can be utilized for harnessing the polyphenols and antioxidant compounds and should be promoted as a source of natural antioxidant for other formulations [36]. The present results suggest that the wild fruits are a source of phenolics which could prevent oxidative DNA damage.

3.3. Mineral Content of Wild Edible Fruits

Minerals are important vital elements for healthy growth and development and disease prevention found in small amounts in foods. However, these substances varied in respect with the plant foods and species. The present fruits contained high amounts of P and K and relatively quantities of Ca, Mg, and Na with significant (p < 0.01) difference among fruits and species for macrominerals (expressed in mg/100 g in edible portion) (Table 4). The contents of Na of all fruits range from 2.01 to 54.01 in Xam and Tam, respectively. For Ca contents, the values varied between 9.74 and 57.06 in Ase and Bae fruits, respectively. The contents of K are higher compared to other macroelements that varied also significantly among fruits and species with the values ranged from 48.56 to 301.34 in Xam and Tam. Regarding the P content, the values varied between 40.32 and 118.05 in Zsp and Xam, respectively. The variations of macroelements among fruits and species found in the present study were also reported by Hegazy et al. [40] when they evaluated the minerals composition of some wild edible fruits in the three study species from Middle East of Egypt. In comparison with the fruits form, microelements (expressed in mg/100 g edible portion) such as Mn, Cu, and Se are higher in fresh than dry fruits (Table 4). However, the contents of Mn ranged from 0.45 to 4.56 in Hba and Ale, respectively, while Fe contents ranged from 0.99 to 2.77 in Ada and Zma, respectively. Fruits Dmi (0.13) and Boe (1.13) had the highest and the lowest values of Cu in fruits, respectively. The present study showed that Cu is in low amount among microelements compared to others (Table 4).

Table 4

Mineral content in seventeen wild fruits (values are expressed in mg/100 g in edible portion).

	Macrominerals (mg/100 g)					Microminerals
	Na	Ca	Mg	K	P	Mn	Fe	Cu	Se	Zn
Zma	48.34 ± 0.01a	36.24 ± 0.01c	9.21 ± 0.04f	158.12 ± 0.05c	78.02 ± 0.01d	3.01 ± 0.01c	2.77 ± 0.02a	0.25 ± 0.01g	0.93 ± 0.01c	5.01 ± 0.01d
Pbi	30.65 ± 0.05b	24.65 ± 0.02e	57.41 ± 0.01b	96.02 ± 0.15e	54.36 ± 0.03f	2.15 ± 0.02d	1.45 ± 0.01de	0.58 ± 0.02e	0.23 ± 0.00i	7.10 ± 0.03c
Dmi	5.22 ± 0.01f	15.04 ± 0.04f	32.25 ± 0.04c	74.21 ± 0.24g	42.89 ± 0.05g	0.96 ± 0.06g	1.63 ± 0.01d	0.13 ± 0.01h	0.32 ± 0.01i	3.13 ± 0.04e
Bae	18.21 ± 0.00d	57.06 ± 0.01a	68.26 ± 0.00a	116.01 ± 0.01d	102.58 ± 0.01b	1.45 ± 0.05e	2.85 ± 0.10a	0.86 ± 0.05c	0.59 ± 0.03g	6.30 ± 0.01b
Pre	25.14 ± 0.12c	32.01 ± 0.02c	16.45 ± 0.01e	59.25 ± 0.06h	69.01 ± 0.02de	2.50 ± 0.03d	1.25 ± 0.15e	0.45 ± 0.01f	0.51 ± 0.03g	0.98 ± 0.02i
Ada	35.24 ± 0.01b	45.15 ± 0.06b	21.05 ± 0.01e	126.21 ± 0.04d	89.34 ± 0.01c	1.32 ± 0.01e	0.99 ± 0.00f	0.26 ± 0.00g	0.78 ± 0.02d	10.26 ± 0.01a
Zsp	31.01 ± 0.05b	28.35 ± 0.01cd	5.24 ± 0.02g	204.09 ± 0.35b	118.05 ± 0.03a	2.78 ± 0.02d	2.02 ± 0.11b	0.69 ± 0.01d	0.82 ± 0.00cd	1.88 ± 0.03g
Dme	9.54 ± 0.14e	52.02 ± 0.03a	11.04 ± 0.04f	102.01 ± 0.08e	95.21 ± 0.12b	3.28 ± 0.20b	1.87 ± 0.00c	1.04 ± 0.00bc	0.45 ± 0.01h	0.68 ± 0.00j
Tam	54.01 ± 0.25a	25.24 ± 0.01d	28.67 ± 0.03d	301.34 ± 0.01a	107.35 ± 0.06b	1.14 ± 0.15e	2.54 ± 0.03a	0.53 ± 0.02e	0.42 ± 0.02h	4.36 ± 0.03e
Vdi	3.28 ± 0.05f	14.25 ± 0.04f	20.09 ± 0.07e	88.32 ± 0.06f	59.29 ± 0.04ef	0.89 ± 0.05h	1.02 ± 0.01f	0.44 ± 0.01f	0.65 ± 0.01f	1.30 ± 0.01h
Vpa	11.94 ± 0.01e	43.05 ± 0.01b	35.02 ± 0.05c	124.95 ± 0.02d	65.09 ± 0.05e	4.36 ± 0.36a	2.09 ± 0.01b	0.61 ± 0.03de	1.06 ± 0.02b	3.01 ± 0.02e
Hba	18.02 ± 0.25d	34.09 ± 0.11c	4.57 ± 0.01g	90.18 ± 0.01ef	77.68 ± 0.01d	0.45 ± 0.03i	1.52 ± 0.02d	0.70 ± 0.01d	0.89 ± 0.01b	9.32 ± 0.01b
Ase	22.35 ± 0.00cd	9.74 ± 0.08g	15.06 ± 0.13ef	68.29 ± 0.02gh	88.14 ± 0.03c	1.22 ± 0.01e	2.04 ± 0.01bc	0.91 ± 0.03c	0.76 ± 0.02ef	1.65 ± 0.00g
Xam	2.01 ± 0.08g	26.08 ± 0.02de	6.25 ± 0.07g	48.56 ± 0.04i	40.32 ± 0.02g	2.01 ± 0.03d	1.98 ± 0.02c	2.01 ± 0.03a	1.15 ± 0.01a	2.69 ± 0.01f
Ale	12.58 ± 0.02e	33.07 ± 0.06c	19.56 ± 0.08e	63.32 ± 0.02h	57.25 ± 0.01f	4.56 ± 0.04a	2.14 ± 0.00b	0.79 ± 0.01cd	0.98 ± 0.08b	3.99 ± 0.02e
Boe	15.23 ± 0.03de	27.32 ± 0.05d	56.09 ± 0.04b	67.02 ± 0.03gh	96.21 ± 0.00b	2.56 ± 0.00d	1.34 ± 0.10de	1.13 ± 0.01b	1.28 ± 0.01a	2.32 ± 0.01f
Hmo	8.65 ± 0.25ef	21.39 ± 0.01e	17.05 ± 0.05e	101.05 ± 0.06e	72.37 ± 0.03d	3.65 ± 0.02b	1.90 ± 0.04c	0.40 ± 0.03f	0.79 ± 0.02cd	1.82 ± 0.01g

Dmi: Detarium microcarpum; Pbi: Parkia biglobosa; Zma: Ziziphus mauritiana; Bae: Balanites eagyptiaca; Dme: Diospyrus mespiliformis; Tam: Tamarindus indica; Ada: Adansonia digitata; Zsp: Ziziphus spina-christi; Pre: Phoenix reclinatum; Vdi: Vitex diversifolia; Vpa: Vitellaria paradoxa; Hba: Haematostaphis barteri; Ase: Annona senegalensis; Xam: Ximenia americana; Ale: Afrostyrax lepidophyllus; Hmo: Hexabolus monopetalus; Boe: Borassus aethiopium. Values are the means ± SE with three replicates. In the same column, values followed by different superscript letters are significantly different (p < 0.01).

Zn contents found at higher amount among fruits varied between 0.68 and 10.26 in Dme and Ada, respectively. These significant variations of microelements among fruits and species were similar with the results obtained by Sibiya et al. [41] in their study of mineral composition of selected indigenous wild southern African fruits. Our fruits are rich in microelements (Fe, Zn and Cu) compared to the contents (0.00-0.27 mg/100 g) found in four fruit jams reported by Naeem et al. [42]. This result could be due to specie, variety, location, soil, and climatic conditions. In fact, Paunović et al. [43] found that minerals in black mulberry fruit varied significantly among 3 locations. Se is an essential mineral that have high antioxidant activity found with high amount in Boe which can be considered a source of Se which will be benefit for fruit consumers.

3.4. Correlation between Phenolic Compounds and Antioxidant Activities

The antioxidant activities evaluated in the present study are highly and positively correlated with total polyphenols, flavonoids and tannins content (Table 5). Various findings reported relationships between polyphenols content and antioxidant activity of fruits [24, 44]. Similarly, and Surveswaran et al. [45] reported significant and positive linear correlations between total antioxidant capacities and phenolic contents.

Table 5

Pearson's correlation between polyphenolic compounds and antioxidant properties of twenty-eight wild edible fruits.

	PPi	FLi	TTi	ABTSi	DPPHi	FRAPi	PPs	FLs	TTs	ABTSs	DPPHs	FRAPs	TA
PPi	1	.540∗∗	.375∗∗	.690∗	.154	.747∗∗	-.149	.150	.379∗∗	.287∗∗	-.111	-.147	-.087
FLi		1	.507∗∗	-.277∗∗	.694∗∗	.767∗∗	-.250∗∗	-.236∗	.027	-.280∗∗	-.175	-.290∗∗	-.180
TTi			1	-.157	-.104	.603∗∗	-.106	-.055	-.044	-.370∗∗	-.433∗∗	-.449∗∗	-.261∗∗
ABTSi				1	.906∗∗	-.140	.452∗∗	.868∗∗	.128	.788∗∗	.386∗∗	.544∗∗	.025
DPPHi					1	-.148	.493∗∗	.729∗∗	.003	.670∗∗	.269∗∗	.459∗∗	.106
FRAPi						1	-.237∗	-.068	.279∗∗	-.111	-.257∗∗	-.350∗∗	.016
PPs							1	.378∗∗	-.042	.889∗∗	.784∗∗	.664∗∗	.147
FLs								1	.296∗∗	.720∗∗	.534∗∗	.620∗∗	.584∗
TTs									1	.408∗∗	.527∗∗	.382∗∗	.339∗∗
ABTSs										1	.641∗∗	.690∗∗	.464∗∗
DPPHs											1	.908∗∗	.383∗∗
FRAPs												1	.279∗∗
AT													1

∗∗Correlation is significant at the 0.01 level. ∗Correlation is significant at the 0.05 level. PPi: bound polyphenols; FLi: bound flavonoids; TTi: bound tannins; ABTSi: ABTS activity of the bound phenolic compounds; DPPHi: DPPH activity of the bound phenolic compounds; FRAPi: FRAP activity of the bound phenolic compounds; PPs: free polyphenols; FLs: free flavonoids; TTs: free tannins; ABTSs: ABTS activity of the free phenolic compounds; DPPHs: DPPH activity of the free phenolic compounds; FRAPs: FRAP of the free phenolic compounds; TA: total anthocyanins.

In the present study, taken apart each fraction of polyphenol content, it is observed that bound polyphenol content shows a significant and positive relationship with ABTS (r = 0.690, p < 0.01) and FRAP (r = 0.747, p < 0.01). Also, significant and positive relationships between antioxidant activities and bound polyphenol content in these fruits were similar with other studies on some exotic fruits [23, 38]. However, no association is shown by bound forms of polyphenolic compounds performed through the DPPH assay.

In fact, according to the mechanisms, based on the types of the induced compound antioxidant activities, ABTS radical scavenging is conferred by both lipophilic and hydrophilic compounds, while DPPH radical capturing is induced by hydrophilic compound [46]. These results suggest that lipophilic bound polyphenolic compounds were the major contributors to the antioxidant activity of the fruits evaluated by the two radical scavenging methods. However, free polyphenol content shows higher significant correlative values with ABTS (r = 0.889; p < 0.01) and DPPH (r = 0.784; p < 0.01), while these show average relationships with FRAP (r = 0.664; p < 0.01). Moreover, free polyphenol content shows stronger correlation with ABTS (r = 0.889; p < 0.01) and DPPH (r = 0.784; p < 0.01) than the bound forms; however, the contrary is shown with FRAP value. High correlation observed in the present study is not in agreement with Imeh and Khokhar [25], who found a weak correlation (r = 0.518) between total polyphenols and total antioxidant activity of 16 fruits.

According to the type of polyphenolic compounds and to the DPPH scavenging activity, the present results show that most of the free polyphenolic compounds of fruits may be hydrophilic than that in the bound forms. Flavonoids, another antioxidant compounds found in large amounts in plants, show a significant and positive correlation between its two fraction (bound and free) contents (Table 5). Bound flavonoid content is significantly and positively associated with DPPH (r = 0.694, p < 0.01) and FRAP (r = 0.767, p < 0.01). The positive association is shown between free fraction content of flavonoids with ABTS (r = 0.720, p < 0.01), DPPH (r = 0.534, p < 0.01), and FRAP (r = 0.620, p < 0.01). Additionally, bound flavonoids show higher associative values than their free forms performed with the three methods (Table 5). Throughout the result, free and bound flavonoid content contributes to the DPPH radical scavenging capacity and FRAP, while bound forms contribute more than its free forms to ABTS radical scavenging activity.

The present findings are in accordance with the reports of those who found that flavonoids were the main contributors to antioxidant activities from A. crassiflora [26] and grape fruits [46] due to the presence of double bonds in their C-rings, which increase their nucleophilic power. Moreover, tannin content with its bound fraction content shows only a significant and positive relationship with FRAP (r = 0.603, p < 0.01). The free polyphenol fraction is lowly and positively related to ABTS (r = 0.408, p < 0.01), DPPH (r = 0.527, p < 0.01), and FRAP (r = 0.382, p < 0.01) antioxidant properties. The results also revealed that free tannin content contributes to ABTS and DPPH radical scavenging activities, while bound ones mostly confer FRAP activity (Table 5). The different antioxidant capacity assays evaluated in the present study show a positive relationship between one form to another which vary significantly according to the antioxidant assays (Table 5). Concerning to the contribution of the two forms of polyphenol content evaluated in this work, the results lead to know that bound polyphenol content contributes to the antioxidant activities of the free forms performed by the ABTS method (r = 0.287, p < 0.01). Additionally, free polyphenol content contributes to the bound polyphenol antioxidant activities through ABTS (r = 0.452, p < 0.01) and DPPH (r = 0.493, p < 0.01). However, free fractions of flavonoids show strong contribution to the antioxidant properties of bounds performed with ABTS (r = 0.868, p < 0.01) and DPPH (r = 0.729, p < 0.01). Moreover, free tannin content contributes to the bound forms with the FRAP assay (r = 0.279, p < 0.01).

The contribution of one form of polyphenolic compounds to another in the antioxidant capacities of the wild fruits found in the present study is in agreement with Arruda et al. [26], who observed that antioxidant activity of polyphenol compounds is affected by intermolecular interactions, which can be either synergistic or antagonistic, depending on the conditions and compounds under study. Once more, as reported by Arruda et al. [26], the contribution of phenolic content to antioxidant activity in a food will therefore depend on its concentration and chemical features, matrix composition, and medium conditions. The present study suggests clearly that the wild fruits can offer greater potential sources of natural antioxidants since no previous study had directly examined the contributions of bound and free polyphenols in the antioxidant capacity.

3.5. Principal Component Analysis (PCA)

To further discover the contribution of each fruit according its phenolic contents in the antioxidant potentials, PCA showed clearly the separation between bound and free polyphenol content (Figure 3). Figure 3(a) shows that the polyphenolic compounds and antioxidant activities quantified in the fruits were reduced into two main components (F1 and F2) by the principal component analysis. F1 and F2 explain 60.17% of total data variance, with F1 alone accounting for 39.51% of the observed variations. The variables which mainly contributed positively (F loading >0.50) to F1 are bound flavonoids, bound polyphenols, insoluble forms of antioxidants conferred by FRAP. However, F2 accounts for 20.66% of the observed variations were free flavonoids, ABTS, and DPPH which contribute positively (F loading > 0.75). Therefore, the main fruits species which have contributed mostly to the antioxidant capacities with their polyphenol content are divided into two groups according to F1 and F2 components (Figure 3(b)). However, A. lepilidofilus, H. monopetalus,and the two forms of Z. spina-christi and P. reticulatum are the most contributors to the F1 component, while, P. biglobosa, T. indica, B. aegyptiaca, D. microcarpum, and the two edible forms of Z. mauritiana for F2.

Figure 3

Principal component analysis (PCA) means showing the relationship among total polyphenols (free and bound), total flavonoids (free and bound), total tannins (free and bound), and antioxidant activities. (a) Correlation between variables and factors and (b) biplot of fruit distribution according to their polyphenolic contents and antioxidant activities. PPi: bound polyphenols; FLi: bound flavonoids; TTi: bound tannins; ABTSi: ABTS activity of the bound phenolic compounds; DPPHi: DPPH activity of the bound phenolic compounds; FRAPi: FRAP activity of the bound phenolic compounds; PPs: free polyphenols; FLs: free flavonoids; TTs: free tannins; ABTSs: ABTS activity of the free phenolic compounds; DPPHs: DPPH activity of the free phenolic compounds; FRAPs: FRAP of the free phenolic compounds; TA: total anthocyanins. Blue color indicates different samples.

4. Conclusions

The aims of the present study is to investigate for the first time the polyphenol compound (bound and free) content and their antioxidant activities of the most consumed wild edible fruits native of the Far North Region of Cameroon. Polyphenolic compounds and antioxidant activities of these fruits were quantified for their free and bound fractions. Except P. reticulatum and A. digitata, other dry fruits contain higher amounts of bound polyphenols than their free forms content. Bound polyphenolic compounds of P. reticulatum show strong ABTS radical scavenging activity, while DPPH radical scavenging activity and FRAP values were both recorded in T. indica among dry fruits. However, the highest DPPH, ABTS, and FRAP activities among fresh fruits were shown by V. diversifolia, X. americana, and C. edulis, respectively, for free polyphenol content. Bound polyphenols of H. monopetalus, H. barteri, and C. sinensis showed the highest DPPH and ABTS radical scavenging activity and FRAP values. Furthermore, significant and highly positive correlation among antioxidant activities and phenolic content is established. The present study revealed that the wild edible fruits are rich in free and bound phenolic compounds as sources of antioxidants with high antioxidant activities. The mineral content analysis indicates that wild fruits are rich in valuable macro- and trace elements. Also, correlation between phenolic compounds and antioxidant capacities showed that phenolics may be responsible of the biological activities when fruits are consumed. Thus, consumption of these wild fruits can offer benefits for consumer's health through the supply of natural bioactive compounds which are associated to the prevention of diseases. However, biological activities (antidiabetic and antiobesity) of phenolics of these fruits will be investigated in the future.