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Journal of the Saudi Society of Agricultural Sciences (2016) xxx, xxx–xxx

King Saud University

Journal of the Saudi Society of Agricultural Sciences


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FULL LENGTH ARTICLE

Rheological behavior of high altitude Indian honey


varieties as affected by temperature
Gulzar Ahmad Nayik a,*, B.N. Dar b, Vikas Nanda a

a
Department of Food Engineering and Technology, Sant Longowal Institute of Engineering and Technology, Longowal
148106, Punjab, India
b
Department of Food Technology, Islamic University of Science and Technology, Awantipora, J&K 192122, India

Received 28 May 2016; revised 26 June 2016; accepted 11 July 2016

KEYWORDS Abstract The rheological properties of high altitude India honeys were analyzed in honeydew
Honey; (pine) and nectar honey (multifloral and acacia) varieties at a wide range of temperatures (0, 5,
Loss modulus; 10, 20, and 30 °C). All the honey samples were significantly dominated by loss modulus (G00 ) which
Storage modulus; displayed their viscous nature. Irrespective of geographical origin and temperature, all the honey
Viscosity; varieties showed a Newtonian behavior. The viscosity of all honey varieties showed a strong depen-
Arrhenius model dence on temperature, and Arrhenius model was examined to describe this.
Ó 2016 The Authors. Production and hosting by Elsevier B.V. on behalf of King Saud University. This is
an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction acids, organic acids, some macro- and microelements and


polyphenols (Nayik and Nanda, 2016a). The polyphenols
According to Codex Alimentarius (2001), honey is the natural (phenolic acids and flavonoid compounds) are primarily
sweet substance produced by honeybees from the nectar of responsible for antioxidant activity of honey (Nayik and
plants or from secretions of living parts of plants or excretions Nanda, 2015a; Nayik and Nanda, 2016b; Suhag et al., 2016;
of plant sucking insects on the living parts of plants, which the Nayik et al., 2016b). Viscosity is one of the most important
bees collect, transform by combining with specific substances and significant characteristics of honey which affects its quality
of their own, deposit, dehydrate, store and leave in the honey- as well as the design of processing equipment (Anupama et al.,
comb to ripen and mature. Honey is considered as oldest 2003). The viscosity of honey depends on several factors, espe-
sweetening substance mainly dominated by 70% of sugars pri- cially on temperature, moisture content and chemical constitu-
marily glucose and fructose (Nayik et al., 2014; Smanalieva tion (Yanniotis et al., 2006; Kang and Yoo, 2008). The
and Senge, 2009; Nayik et al., 2016a). It is rich source of amino viscosity is considered as an important parameter in all stages
of honey production, starting from the extraction of honey
* Corresponding author. Fax: +91 1672 280057. from combs to straining, pumping, processing and packing
E-mail address: gulzarnaik@gmail.com (G.A. Nayik). as well. The presence of sugars, acids, proteins and colloids
Peer review under responsibility of King Saud University. makes the honey a material with changing molecular structure.
Studies on rheological behaviors of honey are important for
applications related to handling, storage, processing, pumping,
transport, quality control, and sensory analysis of foods. The
Production and hosting by Elsevier effect of temperature on rheological properties also needs to

http://dx.doi.org/10.1016/j.jssas.2016.07.003
1658-077X Ó 2016 The Authors. Production and hosting by Elsevier B.V. on behalf of King Saud University.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Nayik, G.A. et al., Rheological behavior of high altitude Indian honey varieties as affected by temperature. Journal of the Saudi
Society of Agricultural Sciences (2016), http://dx.doi.org/10.1016/j.jssas.2016.07.003
2 G.A. Nayik et al.

be analyzed since the honey experiences a wide range of tem- After this, the frequency sweep test was employed over the
peratures during processing and storage (Rao, 1999). range of 0.63–63 rad/s at 3% strain in order to determine the
In the literature, most honey varieties have showed Newto- rheological data. A Rheoplus data analysis software (32
nian behavior irrespective of their geographical origin (Al- V3.40.) was used to obtain the experimental data and to calcu-
Malah et al., 2001; Junzheng and Changying, 1998; Mossel late storage modulus (G0 ) and loss modulus (G00 ). Shear stress/
et al., 2000; Nayik and Nanda, 2015b) but few authors have shear rate were evaluated in order to measure the viscosity.
reported non-Newtonian behavior of honey as in case of Results were obtained as an average of two measurements.
heather, manuka and buckwheat honeys (thixotropic), and
eucalyptus honeys (dilatant) which may be due to presence 3. Results and discussion
of high-molecular compounds such as proteins or polysaccha-
rides (dextran) (Smanalieva and Senge, 2009; Witczak et al., 3.1. Pollen analysis
2011; Yanniotis et al., 2006).
In past few decades, the rheological properties of honey
The pollen spectra of honey samples studied have been briefly
from different countries have been briefly analyzed: Australia
described and the percentages are related to pollen of nectar
(Mossel et al., 2000), China (Chen et al., 2009), Korea (Kang
producing plants. Acacia honey contained 54–60% pollen of
and Yoo, 2008), Greece (Yanniotis et al., 2006), India
R. pseudoacacia sp. The honeydew element/pollen grain
(Kumar and Mandal, 2009; Nayik et al., 2015; Saxena et al.,
(HDE/P) ratio was in a range of 2.79–3.01 in pine honeydew
2014), Spain (Gomez-Diaz et al., 2009), Jordan (Abu-Jdayil
(P. wallichiana), which was in good agreement with
et al., 2002), and Poland (Witczak et al., 2011).
Louveaux et al. (1978). The microscopic analysis revealed
Although we have studied the rheology of few varieties of
some fungal spores in pine honeydew which is in good agree-
honey from fruit sources belonging to Kashmir valley of India
ment with those found in Greek pine honeys. Multifloral
(Nayik et al., 2015), still few varieties from non-fruit sources
honey contained 2–5% pollens of Plectranthus rugosus, and
are yet to be studied. Thus, the main aim of the study was to
other pollens found were from Prunus sp., Brassica sp., Thyme
determine rheological behavior of three high altitude Indian
sp. and Ailanthus sp.
honey varieties from Kashmir valley (Altitude: 1850 m ASL)
of India as a function of temperature.
3.2. Rheological measurement
2. Material and methods
Frequency sweep test was carried out to determine the rheo-
logical parameters (G0 and G00 ) and their dependence on angu-
2.1. Honey sample collection and pollen analysis
lar frequency. The loss modulus (G00 ) magnitude was much
greater than storage modulus (G0 ) which displayed that all
Three different raw and fresh honey varieties (n = 24) of aca- three honey varieties showed more viscous behavior than elas-
cia honey (Robinia pseudoacacia), pine honeydew (Pinus wal- tic i.e. G00  G0 . Similar rheological behavior for different
lichiana) and multifloral honey samples were collected types of honey has been obtained by different authors around
directly from beekeepers from September 2012 to May 2014 the world (Gomez-Diaz et al., 2009; Juszczak and Fortuna,
from different areas (Pulwama, Budgam and Srinagar) of 2006; Kumar and Mandal, 2009; Yanniotis et al., 2006; Yoo,
Kashmir valley. All the honey samples were packed and stored 2004).
at 4 °C prior to analysis. The origins of each honey sample With increase in angular frequency, both G0 and G00
were confirmed by melissopalynology. Honey samples were increased which is in agreement with Yoo (2004). Fig. 1a–c
classified according to their botanical origin using the method shows the loss modulus (G00 ) as a function of angular frequency
described by Von der Ohe et al. (2004). The following terms (x) for three honey varieties at different temperatures (0–
were used for frequency classes: predominant pollen (>45% 30 °C). The values for the viscous component i.e. G00 varied
of pollen grains counted), secondary pollen (16–45%), impor- between 0.19 Pa at 30 °C in acacia honey and 1085.49 Pa at
tant minor pollen (3–15%) and minor pollen (<3%). 0 °C in multifloral honey while elastic component ranged
Presence of the air bubbles and sugar crystals in honey can between 0.01 Pa at 30 °C in acacia honey and 15.3 Pa at 0 °C
influence the rheological properties of honey (Abu-Jdayil et al., in multifloral honey. The reason behind the differences in G00
2002); thus, the honey samples were heated to 50 °C for 1 h in and G0 between three honey varieties could be due to variations
a water bath to dissolve crystals, and then kept in 30 °C to in pollen spectra, sugar composition and moisture content
remove air bubbles. (Lazaridou et al., 2004). Doublier and Cuvelier (1996) con-
cluded that G0 is less important than G00 due to its low value.
2.2. Rheological measurement Thus in our present study, the effect of temperature on
dynamic rheological properties on honeys was characterized
A Modular Compact Rheometer (MCR-102, M/s. Anton by G00 values only. To describe the variation in the rheological
Paar, Austria), equipped with parallel plate system (50 mm properties of all honey varieties, the data obtained for both
diameter) at a gap of 0.5 mm at different temperatures (0, 5, parameters (G00 and G0 ) at different temperatures (0–30 °C)
10, 20, and 30 °C) was used to study the dynamic rheological were fitted to the well-known power law as suggested by Rao
characteristics of honey samples. A strain sweep test was per- and Cooley (1992) (Eqs. (1) and (2)):
formed in the range of 0.01% and 50% in order to establish % 00

strain since viscoelastic material is independent of strain up to G00 ¼ k00 ðxÞn ð1Þ
0 0 n0
a critical strain level. In this case, the critical strain obtained G ¼ k ðxÞ ð2Þ
was at 3%.

Please cite this article in press as: Nayik, G.A. et al., Rheological behavior of high altitude Indian honey varieties as affected by temperature. Journal of the Saudi
Society of Agricultural Sciences (2016), http://dx.doi.org/10.1016/j.jssas.2016.07.003
Rheological behavior of Indian honey varieties 3

Figure 1 Loss modulus (G00 ) as a function of angular frequency (x) for (a) multifloral honey, (b) pine honeydew honey, (c) acacia honey
at various temperatures from 0 °C to 30 °C.

Table 1 Consistency coefficient (k) and flow behavior index (n) of storage modulus (G0 ) and loss modulus (G00 ) versus angular
frequency (x) of different honey varieties.
Honey Temperature (°C) G0 G00
0 0
n k R 2
n00 k00 R2
Multifloral 0 0.28 4.97 0.97 1.00 17.30 0.99
5 0.47 1.83 0.98 1.00 14.85 0.99
10 0.30 2.92 0.98 1.01 4.29 0.99
20 0.52 1.62 0.97 1.00 3.95 0.99
30 0.32 1.92 0.94 1.00 1.04 0.99
Pine honeydew 0 0.63 0.45 0.96 1.00 12.94 0.99
5 0.56 0.51 0.95 1.00 7.26 0.99
10 0.88 0.05 0.99 1.00 3.26 0.99
20 1.17 0.02 0.99 1.00 1.96 0.99
30 0.77 0.06 0.99 1.00 0.79 0.99
Acacia 0 0.62 0.23 0.96 1.00 9.39 0.99
5 0.69 0.07 0.88 1.00 4.70 0.99
10 0.86 0.03 0.98 1.00 2.31 0.99
20 0.68 0.05 0.97 1.00 1.39 0.99
30 0.18 0.02 0.85 1.00 0.28 0.99
n = Flow behavior index.
k = Consistency coefficient.

where k0 and k00 are elastic and viscous consistency coefficients cients, flow behavior index and the coefficient of regression
and n0 and n00 represent elastic and viscous flow behavior (R2) for Eqs. (1) and (2) are presented in Table 1. The rheolog-
indexes, respectively. The magnitudes of consistency coeffi- ical data obtained from Eqs. (1) and (2) showed that all honey

Please cite this article in press as: Nayik, G.A. et al., Rheological behavior of high altitude Indian honey varieties as affected by temperature. Journal of the Saudi
Society of Agricultural Sciences (2016), http://dx.doi.org/10.1016/j.jssas.2016.07.003
4 G.A. Nayik et al.

20
Pa Table 2 Viscosity of different honeys as a function of
18
17
temperature.
16
15 Honey Temperature (°C) Viscosity (Pa s)
14
13 Multifloral 0 17.27
12 5 14.82
11
τ 10
10 9.77
9 20 3.93
8 30 1.01
7
6
5
Pine honeydew 0 12.90
4 5 7.26
3
2
10 3.23
1 20 1.95
0 30 0.78
0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 1/s 2
Acacia 0 9.36
5 4.70
10 2.29
Figure 2 Flow curves of honey at 20 °C (AH: Acacia honey; 20 1.37
MFH: multifloral honey; PH: pine honey). 30 0.27

varieties displayed a liquid like behavior because the magni-


tudes of consistency coefficient k00 (0.28–17.30) were much to 1 (Table 1) indicated Newtonian behavior of all honey vari-
greater than those of k0 (0.02–4.97). Similar results for k00 eties. The Newtonian behavior was also shown by flow curves
and k0 were found in Spanish honeys (Oroian et al., 2013), of honey varieties at 20 °C where the shear stress linearly varies
Korean honeys (Yoo, 2004) and Indian honeys (Nayik et al., with the shear rate and passes through the origin (Fig. 2). The
2015). The values of viscous flow behavior index (n00 ) equal viscosity was not influenced by frequency exhibiting a

Figure 3 Viscosity as a function of angular frequency of different unifloral honeys: (a) multifloral honey, (b) pine honeydew honey, (c)
acacia honey at different temperatures (0–30 °C).

Please cite this article in press as: Nayik, G.A. et al., Rheological behavior of high altitude Indian honey varieties as affected by temperature. Journal of the Saudi
Society of Agricultural Sciences (2016), http://dx.doi.org/10.1016/j.jssas.2016.07.003
Rheological behavior of Indian honey varieties 5

Figure 6 Arrhenius model fit for different types of honey


Figure 4 Effect of temperature on viscosity of different honey
varieties.
varieties.

2015a), Chinese Rape honey (Junzheng and Changying,


1998), Greece pine and cotton honeys (Yanniotis et al.,
2006). The diverse difference exhibited among different honey
viscosities from different countries could be due to the depen-
dency of viscosity on moisture content, sugars and protein
contents, which change with the geographical and floral origins
of each honey. The viscosity decreases with increase in temper-
ature (Fig. 4) due to less molecular friction and reduced hydro-
dynamic forces (Mossel et al., 2000; Patil and Muskan, 2009).
The descending order of loss modulus (G00 ) for all studied sam-
ples is shown in Fig. 5: multifloral honey, pine honeydew and
acacia honey.

3.3. Effect of temperature on honey viscosity

The viscosity–temperature relationship is best described by


using the Arrhenius equation:
l ¼ lo exp½Ea =RT
Figure 5 Representation of loss modulus (G00 ) at 20 °C in
dynamic oscillatory procedure for all honeys. where l is viscosity (Pa s), lo is constant, Ea is activation
energy (kJ/mol), R is gas constant (8.314 kJ/mol/K) and T is
absolute temperature in Kelvin. The constant pre-
exponential factor (lo) and activation energies (Ea) were esti-
Table 3 Effect of temperature on honey viscosity.
mated from the intercept and slope of straight lines obtained
Honey Ea [kJ/mol] go [mPa s] R2 by the least square regression. The values of activation energy
Multifloral 65.75 5.93  1011 0.99 of the analyzed honey varieties ranged from 62.10 kJ/mol in
Pine honeydew 62.10 1.49  1012 0.99 pine honeydew to 75.87 kJ/mol in acacia honey (Table 3). Sim-
Acacia 75.87 2.74  1014 0.99 ilar values for activation energy were found by Lazaridou et al.
(2004) in Greek honeys and Juszczak and Fortuna (2006) in
Polish honeys.
The activation energy values reported in our study were
Newtonian behavior as shown in Fig. 3a–c. The Newtonian considerably lower than those reported by Sopade et al.
behavior of different honeys from different parts of world (2002) in Australian honeys which could be probably due to
has been observed by many authors (Oroian et al., 2014; the fact that the authors performed their rheological measure-
Gomez-Diaz et al., 2009; Saxena et al., 2014). The lowest vis- ments at lower temperatures (below 8 °C). The activation
cosity value was 0.27 Pa s at 30 °C observed in acacia honey energy reflects the sensitivity of the viscosity to the tempera-
while highest was 17.27 Pa s at 0 °C in multifloral honey ture change. Higher the values of activation energy, more is
(Table 2). Our results for viscosity were in agreement with the viscosity sensitiveness to temperature change Lazaridou
the values reported in Indian honey (Nayik and Nanda, et al. (2004). Table 3 shows that acacia honey was the most

Please cite this article in press as: Nayik, G.A. et al., Rheological behavior of high altitude Indian honey varieties as affected by temperature. Journal of the Saudi
Society of Agricultural Sciences (2016), http://dx.doi.org/10.1016/j.jssas.2016.07.003
6 G.A. Nayik et al.

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highest material constant (lo) displayed the highest viscosity Nayik, G.A., Suhag, Y., Majid, I., Nanda, V., 2016a. Discrimination
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Acknowledgments Nayik, G.A., Nanda, V., 2016a. Effect of thermal treatment and pH on
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The first author is thankful to local beekeepers of Kashmir val-
Nayik, G.A., Nanda, V., 2016b. Application of response surface
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Grant Commission, New Delhi, for financial support in the pH on antioxidant activity of cherry honey. Pol. J. Food Nutr. Sci.
form of MANF-2013–14. (4) http://dx.doi.org/10.1515/pjfns-2015-0055.
Nayik, G.A., Dar, B.N., Nanda, V., 2016b. Optimization of the
process parameters to establish the quality attributes of DPPH
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Society of Agricultural Sciences (2016), http://dx.doi.org/10.1016/j.jssas.2016.07.003
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Please cite this article in press as: Nayik, G.A. et al., Rheological behavior of high altitude Indian honey varieties as affected by temperature. Journal of the Saudi
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