South African Journal of Botany 115 (2018) 170–178

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South African Journal of Botany

journal homepage: www.elsevier.com/locate/sajb

Cropping system contributes largely to fruit composition and sensory

properties of pomegranate (Punica granatum L. var. Gabsi)
F. Boussaa a,⁎, F. Zaouay a, F. Hernandez b, L. Noguera-Artiaga c, Ά. Carbonell-Barrachina c,
P. Melgarejo b, M. Mars a
a
Research Unit on Agrobiodiversity (UR13AGR05), Higher Agronomic Institute, Chott-Mariem, IRESA-University of Sousse, Tunisia
b
Department of Plant Production and Microbiology, University Miguel Hernandez, E-03312 Orihuela, Alicante, Spain
c
Department of Agricultural Food Technology, Food Quality and Safety Group, University Miguel Hernandez, E-03312 Orihuela, Alicante, Spain

a r t i c l e i n f o a b s t r a c t

Article history: The oasis, where pomegranate is grown simultaneously with several crops, is considered as an ecosystem with
Received 19 July 2017 particular properties. No research has been made to investigate the relationship between pomegranate fruit
Received in revised form 30 December 2017 quality and oasis environment. A comparison between full shade oasis (pomegranate trees were intercropped
Accepted 26 January 2018
with date palm trees and other fruit species), partial shade oasis (pomegranate trees grown under date palm
Available online xxxx
trees) and regular orchards with full sun conditions has been investigated in terms of fruit quality. The
Edited by OM Grace full shade oasis microclimate was more favourable to obtain pomegranate arils with an attractive red colour
and high total anthocyanin content. Pomegranates under these conditions contained total volatile content
Keywords: (79–144 μg L−1) which was about 2 times higher than that in full sun exposed fruits (47–64 μg L−1). Particularly,
Oasis hexanal and limonene were the most abundant compounds characterizing the aroma profile of fruits cultivated
Organic acids under full shade oasis, and their arils were the most appreciated in terms of colour, odour and taste by Tunisian
Sugars consumers. However, fruits from partial shade oasis provided the sweetest juices with high concentrations of
Sensory appreciation glucose (59.8–63.3 g L−1) and fructose (108–111 g L−1). Titratable acidity and total organic acids content
Volatile compounds
were also higher in fruits grown under Zarat 3 characterized by partial shade conditions. PCA analysis was
used to identify which physicochemical and sensory attributes were more closely linked to oasis conditions.
Red colour intensity, monoterpenes, hexanal, citric and quinic acids were useful to discriminate full shade
oasis. These compounds seem to contribute to the typical organoleptic properties of oasis pomegranate fruits.
© 2017 SAAB. Published by Elsevier B.V. All rights reserved.

1. Introduction system. The pomegranate species is considered a major component of

Pomegranate (Punica granatum L.) belongs to the Lythraceae family
and has been a culturally important plant in northern Africa since
ancient times. This fruit tree can be grown in a wide range of climates
from temperate to desert conditions. In recent years, pomegranate has
gained popularity due to its multi-functionality and nutritional value
in human diet (Calin-Sanchez et al., 2011).
Tunisia is one of the main producers of pomegranate in the
Mediterranean countries with a total production of 83,000 tons in
2016. Gabès oasis being a major pomegranate producing area in terms
of acreage and production as it gives 40% of total production (G.I.Fruits,
2016). Considered as an ≪Outstanding Universal Value ≫, Gabès oasis
is one of the last of its kind in the world (UNESCO, 2010; Verner,
2013). The area is considered unique because of its rich wildlife and
fauna, breath-taking landscape and its complex traditional irrigation
⁎ Corresponding author at: Research Unit on Agrobiodiversity, Higher Agronomic
Institute, Chott-Mariem, BP.47, 4042, Tunisia.
E-mail address: faten.boussaa@laposte.net (F. Boussaa).
this oasis and Gabsi is the dominant variety.
The oasis is an intercropping system which was one of the most ef-
fective human adaptation strategies in an environment challenged by
pronounced temperature variations and low precipitation (Cheneval,
2016). Typically, the oasis is based on the date palm grove, essential
element for creating its microclimate that allows the cultivation of
other fruit trees (pomegranate, fig, citrus, etc.), forage crops and vegeta-
bles forming the lower storey (Sellami and Sifaoui, 1998). In arid
regions, because of high temperature and drought, the oasis effect, is de-
fined as “the vegetation cooling effect” due to extensive evapotranspira-
tion in oasis compared with the surroundings (Hao et al., 2016).
According to Riou (1990), three elements are modified in the presence
of the oasis; water content in the upper soil layers is higher, the dynamic
roughness (or the friction force of the wind) increases by the presence
of trees and several levels of vegetation and the vertical distribution
of the radiant energy is dispersed in the oasis according to plant
strata. These findings were later confirmed by Potchter et al. (2008).
Light partitioning between intercrop components is a main determi-
nant of their transpiration and photosynthetic capacity, hence water

https://doi.org/10.1016/j.sajb.2018.01.016
0254-6299/© 2017 SAAB. Published by Elsevier B.V. All rights reserved.
 F. Boussaa et al. / South African Journal of Botany 115 (2018) 170–178
consumption and biomass production (Sellami and Sifaoui, 2008).
Moreover, dense foliage and multiple layers of canopy can partially
or totally obstruct incoming radiation, resulting in cooler tempera-
tures at the shaded side (Middel et al., 2014). Studies showed that
summer air temperature of oasis can be cooler 2–7 °C while relative
humidity measurements in oasis was up to 6% than their surroundings
in desert environments (Saaroni et al., 2004).
Few studies related to the effects of environmental factors on pome-
granate fruit quality have been carried out (Mirdehghan and Rahemi,
2007; Schwartz et al., 2009), and even less have focused on the effect
of climate on sensory and nutritional traits, whereas it is necessary to
take these factors into account to improve final pomegranate quality.
Hence, this study was undertaken to investigate the impact of oasis
cropping system on physicochemical and sensory properties of pome-
granate fruit, cv. Gabsi, compared with those grown in new regular
orchards under full sun exposure.
2. Materials and methods
2.1. Plant material
The study was carried out in Gabès ‘South-East of Tunisia’. This
region is characterized by an arid climate with mild winter and hot
summer on the coast. The sampling was done from different trees of
commercial “Gabsi” variety. Punica granatum var. “Gabsi” is a local
pomegranate variety which takes its denomination from its geographic
origin (Gabès). Generally, “Gabsi” is a mid-early maturing variety pro-
ducing mature fruits from approximately mid-September in southern
Tunisia. This variety bears big-sized fruits with relatively large calyx
and spreading outward sepals. When fully mature, ‘Gabsi’ fruits are red-
dish with yellowish blush. They contain many moderately soft seeds
enclosed in a red juicy edible pulp which is sweet and slightly acid
(Mars and Gaaliche, 1993; Mars and Marrakchi, 1999). Fruit samples
were obtained at the commercial harvest date from eight orchards
located at four localities: Zarat (33° 40′ 00″ N, 10° 21′ 0″ E), Kettana
(33° 46′ 00″ N, 10° 12′ 00″ E) and Zerkine (33° 45′ 00″ N, 10° 17′ 00″ E)
in Southern Gabès, whereas Ouedhref (33° 59′ 00″ N, 95° 58′ 00″ E) in
Northern Gabès. In three orchards (Kettana 1, Kettana 2 and Ouedhref),
pomegranate trees were cultivated in an oasis system. Several fruit
species such as olive trees, grapes and citrus were planted, under date
palms, in combination with pomegranate trees. In such intercropping
system (oasis conditions), pomegranate fruits were grown in full-
shade conditions. The orchards of Zarat 1, Zarat 2 and Zarat 3 were
cultivated also in oasis system. However, pomegranate trees were
intercropped only with date palm trees. These conditions make fruits
in partial shade. In Zerkine 1 and Zerkine 2, pomegranate trees were
grown in full sunlight conditions since trees were planted without
intercropping.
2.2. Sampling and sample processing
From each orchard, ripe fruits from 5 different sites of each canopy of
5 trees were harvested at the beginning of October at early morning
during the coolest time (medium temperature and moderate humidity)
and immediately transported to the laboratory. Fruits were manually
peeled and juice was obtained from fleshly arils using a domestic
blender and filtered through a cloth tissue. Juice was stored at −20 °C
for further analysis.
2.3. Physicochemical analysis
Titratable acidity (TA), pH, total soluble solids (TSS) and maturity
index (MI) were evaluated as quality indexes. Juice pH was measured
using a pH-meter (Jenway). The TA was determined by acid–base
potentiometry (0.1 mol L−1 NaOH up to pH 8.1), expressed as g L−1.
The TSS content was recorded using a refractometer (Atago) at 20 °C
171
with values being expressed as °Brix. Aril colour of each fruit placed in
a colourless glass petri dish, was measured in CIEL*a*b* coordinates
(L*, a*, b*) using a Minolta Chroma Meter CR-400 (Minolta Corp,
Osaka, Japan) after calibration with white tile background. All analyses
were repeated twenty times and results were expressed as means ± SE
(standard error).
2.4. Total anthocyanin content
Total anthocyanin content (TAC) was determined according to the
pH differential method (Cheng and Breen, 1991). Briefly, 0.4 mL of
pomegranate juice was diluted in 3.6 mL of two different buffers: potas-
sium chloride (0.025 M, pH 1.0) and sodium acetate (0.4 M, pH 4.5). The
absorbance (A) of two dilutions was measured at 510 and 700 nm,
where A = (A510 nm − A700 nm)pH 1.0 − (A510 nm − A700 nm)pH 4.5. The
content of total anthocyanins (mg cyanidin-3-glucoside/L) was calcu-
lated as: TAC = (A × MW × DF × 1000) / (Ɛ × l), with an extinction
coefficient (Ɛ) of 26,900 L mol−1 cm−1 and molecular weight (MW)
of 449.2 g mol−1.
2.5. Analysis of organic acids and sugars
Organic acids and sugars were quantified according to Carbonell-
Barrachina et al. (2012). Briefly, 1 mL of centrifuged juice (10,000 ×g
for 20 min) was passed through a 0.45 μm Millipore filter and then
injected into a Hewlett-Packard Series 1100 (Wilmington, Del, USA)
high-performance liquid chromatography (HPLC). Organic acids were
isolated and were measured using a diode array detector (DAD) set-
up at 210 nm. For sugar analyses, the detection was conducted using a
refractive index detector (RID). Sugars and organic acids were deter-
mined in triplicate and results were expressed as g L−1.
2.6. Volatile compounds
2.6.1. Extraction procedure
Volatile compounds were extracted from pomegranate juices using
headspace solid phase micro-extraction (HS-SPME) as described by
Calin-Sanchez et al. (2011). After several preliminary tests to optimize
the extraction system, 15 mL of juice was hermetically placed into a
50 mL vial with a polypropylene cap and a polytétrafluoroéthylène
(PTFE)/silicone septum. 1 μL of the internal standard (benzyl acetate)
was added together with NaCl and the vial was equilibrated for
15 min at 40 °C in the water bath. Then a 50/30 μm Divinylbenzene/
Carboxen/Polydimethylsiloxane (DVB/CAR/PDMS) fibre was exposed
to the sample headspace for 50 min at 40 °C.
2.6.2. Chromatographic analysis
Isolation and identification of the volatile compounds were per-
formed using a Shimadzu GC-17A gas chromatograph coupled with a
Shimadzu QP-5050A mass spectrometer (Shimadzu Corporation, Kyoto,
Japan). The GC/MS system was equipped with a TRACSIL Meta.X5 column
(95% dimethylpolysiloxane/5% diphenylpolysiloxane, 60 m × 0.25 mm,
0.25 μm film thickness; Teknokroma S. Coop. C. Ltd., Barcelona, Spain).
The volatile studies were conducted in triplicate. The concentration
of each compound is expressed as % of the total arbitrary area units.
2.7. Descriptive sensory evaluation
Eight highly trained panellists, (aged 23 to 51 years; 50% females)
from the research group “Food Quality and Safety” of the Miguel
Hernández University (UMH, Orihuela, Alicante, Spain) participated
in the study. The panel was selected and trained following the ISO
standard 8586 (2012), and it is specialized in descriptive sensory
evaluation of fruits and vegetables, including pomegranate products
(e.g. Szychowski et al., 2015). For the current study, no orientation
session was needed, because of the high expertise of the panel on
172 F. Boussaa et al. / South African Journal of Botany 115 (2018) 170–178

Table 1
Variation of CIEL*a*b* colour coordinates of pomegranate arils according to orchard microclimate.

L* a* b* C* H

Zarat 1 35.00 ± 1.59a 10.75 ± 0.70bcd 11.44 ± 0.49b 16.00 ± 0.54b 47.43 ± 2.50bc
Zarat 2 31.73 ± 2.23ab 10.76 ± 0.66bcd 12.71 ± 0.66ab 16.95 ± 0.62ab 49.84 ± 2.40b
Zarat 3 36.10 ± 2.10a 11.07 ± 1.05bcd 12.99 ± 0.53ab 17.50 ± 0.80ab 50.91 ± 2.80b
Kettana1 29.23 ± 1.63b 12.46 ± 0.95ab 9.70 ± 0.42c 16.06 ± 0.80b 39.18 ± 2.20d
Kettana 2 29.13 ± 1.70b 14.03 ± 1.01a 11.52 ± 0.52b 18.47 ± 0.85a 40.40 ± 2.50cd
Ouedhref 34.67 ± 2.17ab 11.95 ± 0.93abc 11.98 ± 0.69b 17.20 ± 0.90ab 45.94 ± 2.40bcd
Zerkine 1 34.47 ± 1.20ab 9.58 ± 0.63cd 11.37 ± 0.43b 15.20 ± 0.50b 49.72 ± 2.10b
Zerkine 2 35.85 ± 1.38a 8.46 ± 0.77d 14.36 ± 0.68a 17.00 ± 0.70ab 59.61 ± 2.40a

Mean square
Inter-orchards 170.64 61.92 39.72 21.54 868.77
Intra-orchards 67.09 15.41 6.6 11.13 128.01
Significance ⁎ ⁎⁎ ⁎⁎ NS ⁎

Values are means ± standard error of twenty replications. Means followed by the different letter within a same column indicate significant differences according to Duncan test.
Significance of F ratio: NS, not significant (P N 0.05).
⁎ P b 0.05.
⁎⁎ P b 0.01.

pomegranates. The following attributes were chosen on the basis of the Low temperature enhanced anthocyanin synthesis and thus amelio-
lexicon by Vázquez-Araújo et al. (2014): (appearance) colour; (basic rated red colour of pomegranate arils (Schwartz et al., 2009). Aril
tastes and chemical feelings) sourness, sweetness, and astringency. The lightness (L*) values increased with high sun exposure of fruits.
panel used a numerical scale for quantifying the intensity of the pome- Similarly, yellow-blue coordinate (b*) values were higher for Zerkine
granate products attributes where 0 represents none and 10 extremely 2 with full sun conditions (14.40) than that recorded for the fruits
strong with 0.5 increments. Samples (~10 g of arils from 5 fruits) were from Kettana 1 oasis (9.70). As regards to the chroma value (C*), no
served monadically in a randomized order and coded using 3 digit significant variation was noted between orchard microclimates. Never-
numbers. Unsalted crackers and distillate water were provided to theless, significant differences existed in the hue angle (H), ranging
panellists to clean their palates between samples. from 39.20° (Kettana 1) to 59.60° (Zerkine 2).
Significant differences in physicochemical parameters were re-
2.8. Affective sensory evaluation corded in response to microclimate conditions (Table 2). The fruits of
Zerkine 2 characterized by full sun exposure presented the highest pH
A group of 100 panellists (aged between 20 and 55 years) who had value, while the lowest value was recorded for fruits from the full
no previous experience in evaluation of pomegranate, but were fre- shade oasis of Ouedhref. A considerable variation in titratable acidity
quent consumers of pomegranates (2–3 times consumption per week was also recorded. The fruits harvested from Kettana 1 characterized
during the pomegranate season) and consisting of the staff and students by full shade and those from Zarat 3 grown under partial shade showed
of High Agronomic Institute of Chott-Mariem (Tunisia), participated the highest titratable acidity levels. Total soluble solids content varied
in taste panels. Consumers were asked to describe their overall satisfac- greatly depending on microclimate conditions and ranged from 14.74
tion degree but also that for the main sensory attributes under evalua- to 17.42 °Brix (Table 2). The fruits of Zarat 3 with partial shade condi-
tion. The scale used for this affective test was a 9-point hedonic scale tions registered the highest total soluble solids content, while the full
(1 = dislike extremely, 5 = neither like nor dislike, 9 = like extremely). sun exposed fruits for Zerkine 2 showed the lowest content (Table 2).
Samples (~10 g of arils from 5 fruits) were served monadically in a ran- Previous studies (Dussi et al., 2005; Jifon and Syvertsen, 2001) reported
domized order and coded using 3 digit numbers. Unsalted crackers and also that high shading conditions reduced TSS content. Poudel et al.
spring water were provided to panellists to clean their palates between (2009) stated that 25 °C was the optimum temperature to obtain the
samples. highest TSS accumulation in grapes, with a tendency for lower values
at 20 and 30 °C.
2.9. Statistical analysis Maturity index (TSS/TA) is one of the important indicators of the
taste and flavour of pomegranate fruit. In fact, it seems that shading
Statistical analyses were performed using one-way analysis of
variance ANOVA, and the significant difference between means was Table 2
determined by Duncan's multiple range test using SPSS 20 software. Change of physicochemical parameters (pH; TA: titratable acidity; TSS: total soluble solid;
Significance was defined at P b 0.05.Data were analysed also to deter- MI: maturity index) in pomegranates cultivated under different microclimates.
mine correlations between instrumental and sensory analysis using TSS (°Brix) TA (g L−1) MI pH
Pearson correlation. Principal component analysis (PCA) was carried cd
Kettana 1 15.61 ± 0.09 2.50 ± 0.01a 62.40 ± 0.94f 3.97 ± 0.01de
out using XLSTAT 2016. The scores were maximized to discriminate Kettana 2 15.37 ± 0.07de 2.00 ± 0.01c 75.50 ± 1.12e 4.05 ± 0.01c
the group of samples according to orchard microclimates. Ouedhref 15.20 ± 0.13e 2.00 ± 0.01c 76.77 ± 2.04de 3.91 ± 0.05f
Zarat 1 15.96 ± 0.14b 1.80 ± 0.01d 88.81 ± 1.66a 4.15 ± 0.02b
3. Results and discussion Zarat 2 15.46 ± 0.06de 1.80 ± 0.01d 84.61 ± 1.67b 4.13 ± 0.02b
Zarat 3 17.42 ± 0.16a 2.40 ± 0.01a 74.18 ± 0.87e 3.95 ± 0.01ef
Zerkine 1 15.90 ± 0.13bc 2.00 ± 0.01c 81.30 ± 1.04bc 4.02 ± 0.01cd
3.1. Physicochemical properties Zerkine 2 14.74 ± 0.12f 1.90 ± 0.01d 79.85 ± 1.54cd 4.27 ± 0.02a

Mean square
Pomegranate aril colour is one of main criteria for consumer
Inter-orchards 13.25 0.01 1321.83 0.30
acceptability. Significant variations of aril colorimetric coordinates Intra-orchards 0.28 0.00 42.55 0.011
were registered depending on orchard microclimate (Table 1). Fruits Significance ** ** ** **
grown outside the oasis (under full sun exposure) presented the less Values are means ± standard error of twenty replications. Means followed by the different
red-coloured arils (a* = 8.50), while fruits harvested from the full letter within a same column indicate significant differences according to Duncan test.
shade oasis of Kettana 2 gave the most red-coloured arils (a* = 14). Significance of F ratio: **P b 0.01.
 F. Boussaa et al. / South African Journal of Botany 115 (2018) 170–178 173

Fig. 1. Total anthocyanin content in different pomegranate juice samples. Means with different letters indicate significant differences at P ≤ 0.01 according to Duncan range test.

environment delays the ripening. Fruits harvested in oasis of Kettana 1
under full shade environment showed the lowest maturity index
(62.4), while the highest value was recorded in fruits grown under par-
tial shade conditions of Zarat 1 (88.81). These results are consistent with
those reported by Jackson and Lombard (1993).
3.2. Total anthocyanin content
Anthocyanins are water-soluble pigments responsible for blue, pur-
ple and red colours of many fruits (Goulas et al., 2012). Environmental
conditions, including sunlight exposure, UV radiation and tempera-
ture are important factors affecting anthocyanin biosynthesis in fruits
(Wang, 2006). Microclimate conditions of different orchards had a
significant effect on total anthocyanin content in pomegranate juices.
The total anthocyanin level was significantly higher in juices from the
full shade oasis of Kettana and Ouedhref, than those from Zarat and
Zerkine grown under partial or full sun exposure (Fig. 1). Similarly,
Schwartz et al. (2009) reported that high temperatures reduced the
total anthocyanin content in pomegranate arils.
3.3. Organic acids
The composition and concentration of organic acids are important
factors that determine consumer perceptions of both sweetness and
sourness in pomegranate fruits (Holland et al., 2009). In the current
study, predominant organic acids detected in pomegranate juices
were quinic and malic acids followed by citric acid (Table 3). However,
organic acid types and contents depend on environmental conditions
(Schwartz et al., 2009). Total organic acids concentration varied from
14 to 16.5 g L− 1 in response to microclimate conditions (Table 3).
The highest malic acid content (52 % of total content) was found in fruits
from Zerkine 1 and Zerkine 2 characterized by full sun exposure, while
those grown in the full shade oasis of Ouedhref, showed the lowest
content (39 % of total content). This is mainly due to oasis cooling effect
in which dense trees provide a cooling effect up to 3 °C by reduction
of sun radiation, increased ambient air humidity and moderate wind
velocity (Tukiran et al., 2016). Wang and Camp (2000) showed that
malic acid in strawberry and bilberry increased as temperature in-
creased. Sunlight is also an important factor to increase malate ions in
fruits (Hummell and Ferree, 1998). The effect of oasis microclimate is
more pronounced for quinic acid. Pomegranate fruits grown under par-
tial and full shade conditions accumulated the highest content (48–56 %
of total content). This result agreed with that of Marsh et al. (1999) who
affirmed that raising air temperatures in the tree canopy decreased
quinate levels. As for quinic acid, pomegranate fruits from oasis showed
the highest citric acid contents. These differences could be attributed to
the high temperatures and respiration rates of exposed fruits (Martinoia
and Rentsch, 1994).
3.4. Sugars
Sugars, contributing to the sweetness of fruits, are important compo-
nents determining the sensory properties and influencing preference of
fruits. Total sugar content ranged from 131 g L−1 to 174 g L−1 (Table 3).
Fructose (84.3–111 g L−1) and glucose (46.7–63.3 g L−1) were the main
sugars in studied juice samples. Table 3 shows significant variation of
glucose and fructose contents depending on microclimate conditions.
Glucose and fructose amounts were higher in fruits from Zerkine 1
and Zerkine 2 exposed to full sun than those of the full shade oases
of Kettana and Ouedhref. However, the fruits from partial shade

Table 3
Organic acids and sugars variation (g L−1) in pomegranate juices from different microclimates.

Organic acids (g L−1) Sugars (g L−1)

Citric acid Malic acid Quinic acid Total Fructose Glucose Total

Kettana 1 0.68 ± 0.07a 6.97 ± 0.01abcd 7.29 ± 0.06ab 14.94 ± 0.04 87.00 ± 0.02e 47.80 ± 0.01f 135 ± 0.02
Kettana 2 0.57 ± 0.06abc 6.84 ± 0.03bcd 7.89 ± 0.02ab 15.30 ± 0.03 84.30 ± 0.01f 46.70 ± 0.01g 131 ± 0.01
Ouedhref 0.60 ± 0.01abc 6.06 ± 0.01d 8.56 ± 0.05a 15.22 ± 0.07 85.20 ± 0.06f 46.90 ± 0.03g 132 ± 0.05
Zarat 1 0.47 ± 0.01c 6.75 ± 0.02cd 7.46 ± 0.09ab 14.68 ± 0.06 108 ± 0.05b 59.80 ± 0.03c 168 ± 0.04
Zarat 2 0.60 ± 0.01abc 6.40 ± 0.03cd 7.07 ± 0.05b 14.07 ± 0.03 111 ± 0.05a 60.60 ± 0.02b 171 ± 0.03
Zarat 3 0.64 ± 0.01ab 7.43 ± 0.03abc 8.33 ± 0.01a 16.40 ± 0.02 111 ± 0.01a 63.30 ± 0.01a 174 ± 0.01
Zerkine 1 0.51 ± 0.01bc 8.23 ± 0.01a 7.00 ± 0.05b 15.74 ± 0.01 100 ± 0.01c 55.50 ± 0.01d 156 ± 0.01
Zerkine 2 0.51 ± 0.01bc 8.12 ± 0.01ab 7.01 ± 0.09b 15.64 ± 0.03 98.30 ± 0.03d 54.40 ± 0.02e 153 ± 0.02

Mean square
Inter-orchards 0.017 1.77 3.09 81.37 32.18
Intra-orchards 0.005 0.55 1.02 8.35 3.2
Significance * * * ** **

Values are means ± standard error of three replications. Means followed by the different letter within a same column indicate significant differences according to Duncan test.
Significance of F ratio: *P b 0.05; **P b 0.01.
174 F. Boussaa et al. / South African Journal of Botany 115 (2018) 170–178

Table 4 partial shade conditions compared with that registered in full sun ex-
Identification and characteristics of volatile compounds in different pomegranate juice posed ones.
samples.

Retention indexes 3.5. Volatile compounds

Compound RT (min) Literature Experimental Descriptor
Fruits produce a range of volatile compounds that make up their
Hexanal 7.35 804 802 Fatty, green, grassy,
powerful characteristic aroma and contribute to their flavour (El Hadi et al.,
1-Hexanol 8.70 888 881 Mint, grass 2013). Aromatic compounds identified in pomegranate juice samples
α-Pinene 10.48 933 940 Sharp, pine were low in number and concentration. The total concentrations of
Sabinene 11.66 973 980 volatile compounds in the headspace of pomegranate juices obtained
β-Pinene 11.95 981 990 Woody, pine
Decane 12.21 1000 999
from only fleshly arils ranged from 47 μg L−1 to 144 μg L− 1
p-Cymene 13.48 1027 1032 Weak, citrus odour (Table 5). A total of 15 compounds were isolated, identified and
Limonene 13.64 1029 1036 Mild, citrus, sweet, orange, quantified using the HS-SPME technique (Tables 4, 5). These com-
lemon pounds can be grouped into six chemical families: (a) monoterpenes:
γ-Terpinene 14.70 1059 1063 Berry, lemon, vegetable,
limonene, α-pinene, β-pinene, p-cymene, γ–terpinene, sabinene and
woody, pepper
Linalool 16.28 1098 1104 Lemon, orange, citrus, floral α-bergamotene; (b) aldehydes: hexanal, nonanal; (c) alcohols:
Nonanal 16.45 1103 1108 Floral, citrus, orange, rose, 1-hexanol; (d) monoterpenoids: α-terpineol, linalool, dihydrocarveol;
fatty (e) esters: linalyl acetate; (f) hydrocarbons: decane. Monoterpenes,
α-Terpineol 20.88 1200 1207 Fragrant, floral, lilac aldehydes and alcohols represented the predominant groups in the
Dihydrocarveol 20.98 1206 1209
Linalyl acetate 22.83 1248 1249 Floral, fruity, pear, sweet
headspace of pomegranate juices. These results are consistent with
α-Bergamotene 31.67 1446 1442 Citrus those of Melgarejo et al. (2011) and Calin-Sanchez et al. (2011). In
general, the most abundant compounds in the investigated samples
were limonene (sensory descriptors: mild, citrus, sweet, orange, lemon),
hexanal (fatty, green, grassy, powerful), 1-hexanol (mint, grass) and
oasis of Zarat contained the highest glucose and fructose levels. decane (Tables 4–5).
These results are in agreement with previous studies showing that Nevertheless, environment affected the accumulation of volatile
shading conditions reduced the total sugar concentration and delayed compounds in fruits that may contribute to their flavour variation
ripening (Krumbein and Schwarz, 2013). However, high temperature (Styger et al., 2011). The concentration and the relative percentages of
beyond an optimum may inhibited photosynthesis and thus induced a volatile components varied greatly following orchard microclimates.
reduction in sugar accumulation (Greer and Weston, 2010). This can In general, the total concentrations of volatile compounds were greater
explain the high content of glucose and fructose in fruits grown under in fruits from full shade oasis (79–144 μg L−1) than those from full sun

Table 5
Variation of volatile compounds concentrations (μg L−1) in Tunisian pomegranate juices according to microclimate conditions.

Compounds Significance Kettana 1 Kettana 2 Ouedhref Zarat 1 Zarat 2 Zarat 3 Zerkine 1 Zerkine 2

Monoterpenes
Limonene ** 6.28g 25.28b 36.47a 21.40c 13.99d 9.76e 3.63h 6.43f
α-Pinene ** 0.41b 0.41b 0.66a 0.41b 0.29c 0.11d 0.13d 0.06e
β-Pinene ** 1.13d 1.27c 3.25a 1.81b 1.05f 0.77f 0.43h 0.71g
Sabinene ** 0.22e 0.37c 0.77b 0.93a 0.34c 0.29d 0.20e 0.11f
p-Cymene ** 0.44d 0.83c 2.04b 2.54 a 0.47d 0.24f 0.22f 0.38e
γ-Terpinene ** 0.61e 0.94d 8.82a 1.75b 0.61e 0.58e 0.31f 1.52c
α-Bergamotene ** 0.04c 0.01d 0.25a 0.09b 0.24a 0.08b 0.01d 0.01d
Total 9.12 29.11 52.86 28.92 17.00 11.83 4.93 9.13
Percentage (%) 10.02 36.84 36.71 26.29 29.31 17.15 10.49 14.27

Monoterpenoids
α-Terpineol ** 2.97g 2.76h 4.76b 8.01a 4.59c 4.49d 3.45f 3.65e
Linalool ** 0.23e 0.12f 0.52b 1.00a 0.30d 0.34c 0.22e 0.15f
Dihydrocarveol ** 4.94g 4.08h 8.47b 11.12a 7.95d 8.41c 5.81f 7.62e
Total 8.14 6.96 13.75 20.13 12.84 13.24 9.47 11.41
Percentage (%) 8.94 8.81 9.55 18.30 22.14 19.18 20.16 17.83

Aldehydes
Hexanal ** 39.04a 11.85b 8.37d 8.44c 2.22h 7.45e 4.5f 3.69g
Nonanal ** 6.72g 6.06h 9.64c 10.76b 7.17e 14.63a 9.33d 6.93f
Total 45.75 17.92 18.01 19.20 9.39 22.07 13.83 10.62
Percentage (%) 50.28 22.69 12.51 17.46 16.20 31.99 29.42 16.59

Alcohols
1-Hexanol ** 19.20c 13.51e 40.50a 17.47d 7.92h 11.30g 11.42f 22b
Percentage (%) 21.10 17.10 28.12 15.89 13.65 16.37 24.30 34.38

Esters
Linalyl acetate ** 0.08cd 0.10bc 0.7a 0.06d 0.10bc 0.13b 0.05d 0.05d
Percentage (%) 0.09 0.13 0.48 0.06 0.17 0.19 0.11 0.08

Hydrocarbons
Decane ** 8.69g 11.01c 18.37b 24.12a 10.73d 10.58e 7.44h 10.45f
Percentage (%) 9.55 13.94 12.76 21.93 18.51 15.33 15.84 16.33
General total 91 79 144 110 58 69 47 64

Values are means ± standard error of three replications. Means followed by the different letter within a same row indicate significant differences according to Duncan test. Significance of
F ratio: **P b 0.01.
 F. Boussaa et al. / South African Journal of Botany 115 (2018) 170–178 175

Table 6
Intensity of the key sensory attributes analysed by descriptive sensory analysis (trained panel) and consumers' scores on their satisfaction degree for the key sensory attributes and their
overall liking.

Descriptive sensory analysis Affective sensory analysis

Aril colour Sourness Sweetness Astringency Aril colour Aroma Taste Overall liking
b a a a d c c
Zarat 1 4.3 ± 0.3 2.7 ± 0.9 5.4 ± 0.5 1.4 ± 0.3 3.4 ± 0.2 3.8 ± 0.2 4.3 ± 0.2 4.2 ± 0.2bc
Zarat 2 5.5 ± 0.3ab 3.0 ± 1.1a 5.4 ± 0.5a 1.5 ± 0.3a 4.5 ± 0.2c 4.1 ± 0.2bc 4.6 ± 0.2bc 4.6 ± 0.2bc
Zarat 3 4.3 ± 0.2b 3.3 ± 1.1a 5.9 ± 0.4a 1.5 ± 0.3a 3.3 ± 0.2d 4.2 ± 0.2bc 4.5 ± 0.2bc 4.5 ± 0.2bc
Zerkine 1 3.9 ± 0.4b 3.6 ± 1.2a 5.5 ± 0.3a 1.7 ± 0.2a 3.3 ± 0.2d 3.9 ± 0.2c 4.3 ± 0.2c 4.1 ± 0.2bc
Zerkine 2 3.3 ± 0.5b 3.9 ± 1.3a 5.3 ± 0.2a 1.4 ± 0.3a 2.4 ± 0.2e 3.8 ± 0.2c 4.1 ± 0.3c 4.1 ± 0.2bc
Kettana 1 6.4 ± 0.2a 3.5 ± 1.3a 5.7 ± 0.2a 1.4 ± 0.3a 6.3 ± 0.1a 5.3 ± 0.2a 5.5 ± 0.2a 5.9 ± 0.2a
Kettana 2 6.3 ± 0.5a 3.3 ± 1.1a 5.5 ± 0.3a 1.4 ± 0.3a 5.3 ± 0.2b 4.2 ± 0.2bc 4.5 ± 0.3bc 4.8 ± 0.2b
Ouedhref 6.0 ± 0.4a 2.5 ± 0.9a 5.6 ± 0.5a 1.4 ± 0.2a 5.2 ± 0.2b 4.7 ± 0.3ab 5.2 ± 0.3ab 5.4 ± 0.2a
Significance ** NS NS NS ** ** ** **

Values are means ± standard error. Means followed by the different letter within a same column indicate significant differences according to Duncan test.
Significance of F ratio: NS: not significant; **P b 0.01.

exposed trees (47–64 μg L−1) (Table 5). Similar results were reported
by Jia et al. (2005) who showed that an increase in temperature caused
by sun exposure has contributed to the degradation of aroma com-
pounds. Generally, the full shade conditions of the oasis were favourable
to accumulate hexanal in pomegranate fruits. Limonene also showed
high concentrations in fruits grown under full shade oasis except
those of Kettana 1. However, monoterpenoids ranged from 17.8
to 22% of total volatiles in pomegranate fruits obtained from partial
shade and full sun exposure. These percentages were higher as
compared with those recorded in fruits grown under full shade oasis
(8–9 %) (Table 5). Previous studies affirmed that hexanal, limonene
and 1-hexanol concentrations were greater in the shaded berries
than in the sun-exposed ones (Scafidi et al., 2013). Nevertheless, ele-
vated temperatures impaired the expression of 1-deoxy-D-xylulose-5-
phosphate synthase transcripts required for isopentenylpyrophosphate
(IPP) synthesis, the universal precursor for the biosynthesis of terpenes
(Rohdich et al., 2002). Belancic et al. (1997) also affirmed that moderate
sun exposure enhances the accumulation of terpenols in fruits, while
too high temperatures can have inverse effects.
3.6. Descriptive and affective sensory evaluation
Sensory perception plays an important role in food preference.
Actually, several circumstantial factors such as habits, beliefs, attitudes
and values influence consumer choices (Palojoki and Tuomi-Gröhn,
2001). Geck et al. (2017) reported also that the perception of gustatory
and olfactory sensations is highly subjective, depending on genetic,
physiological, environmental, and especially cultural variables. In fact,
Cardinal et al. (2015) proved that food-science-related consumers
(FSRC) checked fruit-flavoured powdered beverages differently to the
other two consumer segments, women and children. This is why the
consumer panel not only consisted of students but also staff. The staff
group contained also cleaning people, gardeners, concierges, etc., and
represented 42% of the total consumer panel. In any case, further studies
involving no-food-related consumers and international consumers are
needed to completely support the findings that will be discussed in
this section.
In the current study, descriptive sensory analysis revealed differ-
ences between oasis and regular orchard with full sun exposure in the
aril colour intensity (Table 6).On the other hand, consumers showed
significant differences in their overall liking and in their satisfaction
degree for all studied sensory attributes. Arils from fruits cultivated
under full shade oasis system, particularly from Kettana 1, were charac-
terized by high intensity of the red colour (trained panel) which made
them well appreciated by the consumer panel. Although the descriptive
panel was not able to find differences in the intensity of the individual
sensory attributes under study (sourness, sweetness, and astringency)
as affected by the microclimates, the consumers scored better their
satisfaction degrees for both aroma and taste. However, it is possible
that these differences in the aroma and taste could be influenced
by the colour of the arils. In a similar way, the overall liking was also
higher in the pomegranates grown under full shade oasis (Kettana 1
and Ouedhref), as compared with those samples grown under full sun
(Zerkine 1 and Zerkine 2). In general, Zerkine microclimate conditions
had a negative effect on the aril colour (less red colour intensity was
reached), which was linked to a lower overall satisfaction degree and
also for the colour, aroma, and taste degrees. These results suggested
that environmental conditions influenced pomegranate fruit appearance
(colour intensity) and the final perception by consumers (overall,
appearance, and flavour).

Table 7
Correlation between instrumental and sensory analysis of pomegranate quality.

Aril colour SD Aroma SD Taste SD Overall liking Aril colour int. Sourness int. Sweetness int. Astringency int.

TSS −0.20 −0.02 −0.04 −0.15 0.16 0.09 0.28 −0.73

TA 0.45 0.77 0.66 0.65 0.69 0.72 0.34 −0.25
MI −0.59 −0.85 −0.74 −0.78 −0.70 −0.75 −0.24 −0.09
L*aril −0.88 −0.57 −0.49 −0.61 −0.80 −0.12 −0.26 −0.01
a*aril 0.91 0.61 0.57 0.67 0.93 −0.07 0.52 −0.22
b*aril −0.68 −0.68 −0.64 −0.61 −0.71 −0.05 −0.85 0.58
Anthocyanin content 0.87 0.62 0.59 0.67 0.85 −0.10 0.61 −0.08
Citric acid 0.54 0.79 0.75 0.76 0.65 0.64 −0.07 0.06
Fructose −0.22 −0.22 −0.24 −0.33 0.11 −0.21 0.50 −0.78
Glucose −0.29 −0.38 −0.37 −0.47 −0.02 −0.42 0.37 −0.71
Hexanal 0.65 0.86 0.76 0.79 0.71 0.66 0.48 −0.18
Aril colour SD 1 0.77 0.74 0.83 0.92 0.05 0.43 −0.05
Aroma SD 0.77 1 0.98 0.98 0.77 0.49 0.42 −0.10
Taste SD 0.74 0.98 1 0.98 0.71 0.36 0.40 −0.13
Overall liking 0.83 0.98 0.98 1 0.78 0.39 0.35 0.00
Aril colour int. 0.92 0.77 0.71 0.78 1 0.19 0.53 −0.27

Values in bold font mean that correlations were significant at P ≤ 0.01 according to Pearson correlation. SD and int. mean satisfaction degree and intensity, respectively.
176 F. Boussaa et al. / South African Journal of Botany 115 (2018) 170–178

3.7. Correlation between instrumental and sensory analysis
The correlation was conducted to determine the relationship be-
tween instrumental and sensory analyses (Table 7). The TSS/TA ratio,
often used as a measure of sweetness, was not useful in measuring
this descriptor, but was a reasonable predictor of the sourness. Overall
quality, as well as sensory evaluation of aroma and taste was correlated
positively with citric acid, and negatively with (TSS/TA) ratio. The
sweetness/sourness balance could be crucial in affecting flavour quality
and determining consumer preference. TSS, glucose and fructose were
showed as very good predictors of astringency disappearance that
were highly and negatively correlated with this descriptor. Based on
the correlation coefficient with hexanal, it can be stated that aldehydes
contribute essentially to the aroma and overall appreciation of pome-
granate quality. In addition, aril colour positively impacted quality
scores of products in terms of aroma, taste and overall quality. These
results indicated that aril colour and sourness were evaluated in an
unequivocal way by the panel and were the main attributes for deter-
mining overall quality of samples.
3.8. Principal component analysis
Principal component analysis was carried out on the basis of selected
descriptive and affective sensory plus instrumental parameters. Within
the first two principal components, 59.01 % of the total variance can be
explained (Fig. 2A). The first PC, representing 30.59% gathered posi-
tively 3 classes of volatiles (monoterpenes, alcohols and esters), total
anthocyanin content, a* colour coordinate, quinic acid and sweetness
intensity. Malic acid and pH depicted negative loadings to PC1. PC2
which accounted for 28.42 %, had high positive loadings for TSS/TA
ratio, L*, b* and monoterpenoids and negative loadings for titratable
acidity, citric acid, overall liking, intensities of sourness and aril red

Fig. 2. (A) Plot of contribution of chemical and sensory properties investigated into the first and second principal components. (B) Plot of the first and second principal components
resulting from a PCA of pomegranate orchards based on fruit chemical and sensory properties.
 F. Boussaa et al. / South African Journal of Botany 115 (2018) 170–178
colour and hexanal (Fig. 2A).In the score plot of the principle compo-
nents, the eight orchards could be separated according to their cultiva-
tion system. Kettana 1, Kettana 2 and Ouedhref maintained under full
shade oasis, were separated from full sun exposed orchards and partial
shade oasis (Zerkine 1, Zerkine 2, Zarat 1, Zarat 2, Zarat 3). Compounds
that have the greater role in the definition of the first component were
quite abundant in Ouedhref pomegranates, whose position in the bi-
factors plot was in the positive range of PC1. Many of these compounds
contribute to the typical organoleptic properties of full shade oasis
pomegranate fruits. However, Zarat 1 had large positive scores on
the PC2 axis. Accordingly, volatile compounds, particularly
monoterpenoids could be one of the criteria influencing negatively
consumer's preference. Considering also the third axis, PC3, the ex-
plained variation increased to 76 %, and the biplot representation
using PC1 and PC3 helped to find some more interesting differences be-
tween microclimates (Fig. 2B). Interestingly, such analysis highlighted
the metabolites (glucose and fructose) that mainly participated to the
definition of PC3 were mostly present in Zarat 3 samples.
4. Conclusion
A significant variation in pomegranate fruit composition was noted
following the variation of orchard microclimate. Principal component
analysis allowed the distinction of localities on the basis of pomegranate
fruit organoleptic properties. The oases containing several species were
separated from those with two species and monovarietal orchards.
The fruits from full shade oases of Kettana 1, Kettana 2 and Ouedhref
showed an attractive red colour of arils and a reduction in total sugar
concentrations. Hexanal and limonene was showed to be responsible
for a typical aroma profile of fruits grown under full shade oasis system.
Pomegranate arils from such system were found to be the most appre-
ciated by consumers in terms of colour, aroma and taste. However,
full sun conditions of trees grown outside the oasis had a negative effect
on titratable acidity and the satisfaction degree of consumers for
sensory attributes such as aril colour, aroma, taste and overall quality,
but they improved the synthesis of malic acid. The special oasis ecosys-
tem should be safeguarded as a heritage of global importance and con-
sidered to improve sensory traits related to taste perception. These
results extended earlier studies suggesting that environment condi-
tioned pomegranate fruit quality. Further studies will be required to
grasp the complex factors underlying quality in pomegranate in or
outside oasis. Typical oasis pomegranate properties could be used for
its labelling as geographical indication (GI) or protected designation of
origin (PDO).
Acknowledgments
We would like to extend special acknowledgments to farmers from
Gabès who provided us the fresh pomegranate samples. We also grate-
fully acknowledge the support and collaboration of Mr. Boubaker El Arbi
(Regional Commissary for Agricultural Development, CRDA of Gabès)
and Mrs. Mahassen Gmati (Ministry of Agriculture, Hydraulic Resources
and Fishery, Tunisia).
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