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Temperature effect on apple biospeckle activity

evaluated with different indices

Article in Postharvest Biology and Technology · October 2013

Impact Factor: 2.22 · DOI: 10.1016/j.postharvbio.2011.12.017

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 Postharvest Biology and Technology 67 (2012) 118–123

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Postharvest Biology and Technology

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

Temperature effect on apple biospeckle activity evaluated with different indices

Andrzej Kurenda ∗ , Anna Adamiak, Artur Zdunek
Department of Microstructure and Mechanics of Biomaterials, Institute of Agrophysics PAS Doświadczalna 4, 20-290 Lublin 27, Poland

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

Article history: The physical explanation of the biospeckle phenomenon is well known; however, there is lack of biolog-
Received 7 December 2010 ically related interpretation, which limits a possible application of the method as a new, nondestructive
Accepted 31 December 2011 technique for evaluation of fruit quality. Physically, biospeckles are the result of scattering of coherent
light on moving particles inside living tissue. Almost all biological processes are temperature-dependent;
Keywords: therefore, the aim of this study was to investigate a temperature effect on biospeckle activity in apples
Biospeckle
and determine the extent to which this activity results from biological processes in the tissues of the
Apple
fruit. Apples of ‘Idared’ cultivar were cooled in a storage room from high room temperature 29 ◦ C down
Temperature
to 2 ◦ C, which resulted in apple surface temperatures in the range 29–4 ◦ C. To evaluate the biospeckle
activity, three methods of image analysis were used: correlation coefficient, speckle contrast, and the
moment of inertia. The results showed that biospeckle activity measured by each method decreases with
temperature decreases. However, the correlation coefficient was found as the most robust indicator of
biospeckle activity and Q10 factor indicates a mostly biological basis for this phenomenon.
© 2012 Elsevier B.V. All rights reserved.

1. Introduction pattern consists of two components: static, from nonmoving ele-

Fruits and vegetables are biologically variable and highly per-
ishable (Johnston et al., 2002; Bobelyn et al., 2010). Hence, there
is a need to evaluate their quality at different stages pre- and
post-harvest in order to provide best quality product to con-
sumers. Recently, a few interesting optical techniques and devices
have been developed for nondestructive evaluation of fruits and
vegetables: Vis/NIR spectrophotometry (Zude-Sasse et al., 2002;
Zude et al., 2011; Mireei et al., 2010; Rutkowski et al., 2008),
time-resolved reflectance spectroscopy (Zerbini et al., 2003),
hyperspectral backscattering imaging (Qin and Lu, 2006; Peng and
Lu, 2008) or laser-induced light backscattering (Qing et al., 2006;
Baranyai and Zude, 2009). Nicolaï et al. (2007) have reviewed most
of the above techniques, using the term NIR spectroscopy, and
have shown their feasibility and areas where more research is still
needed.
Biospeckle is another optical technique, although less known,
that has been developing for the last fifteen years for evaluation
of properties of biological materials (Xu et al., 1995; Zhao et al.,
1997). The physics of biospeckle is well developed. Laser speckle is
an interference pattern of backscattered light observed, for exam-
ple by a CCD camera, at a some distance from the illuminated object.
If the sample does not show activity, the speckle pattern is stable
in time. However, in the case of biological samples, the speckle
∗ Corresponding author. Tel.: +48 81 743 8558; fax: +48 81 744 5067.
E-mail address: a.kurenda@ipan.lublin.pl (A. Kurenda).
ments of an object, and variable in time, from moving particles
within a material. This variable-in-time speckle pattern is charac-
teristic for biological tissues and has been called a biospeckle (Zhao
et al., 1997; Xu et al., 1995).
So far, attempts to apply the biospeckle method in a biological
study have included measurements of blood flow in blood vessels
(Briers and Fercher, 1982), viability of seeds (Braga et al., 2003;
Sendra et al., 2005), activity of parasites in living tissues (Pomarico
et al., 2004; Braga et al., 2005), analysis of maturation and bruis-
ing of fruits and vegetables (Xu et al., 1995; Pajuelo et al., 2003;
Rabelo et al., 2005), and, monitoring of apple shelf life (Zdunek
et al., 2007, 2008). In many publications on the biological applica-
tions, one can find a statement that biospeckle activity corresponds
to activity of biological samples; however, exactly what kind of
activity is not specified anywhere or is only suspected. Braga et al.
(2009) has summarized that processes related to movement of
the scattering centers in the tissue such as cytoplasmic stream-
ing, organelle movement, cell growth and division during fruit
maturation, and biochemical reactions are responsible for certain
biospeckle activity. Brownian motions should be considered as the
source of biospeckle activity, too (Zhao et al., 1997).
In the case of living organisms, whose operation is based on
enzymes, the rate of biological processes strongly depends on tem-
perature (apart from a few temperature-compensated ones). An
example of that temperature-dependent process is the cytoplasmic
streaming in Nitella obtusa and Elodea canadensis cells (Shimmen
and Yoshida, 1993; Vorob’ev et al., 2004) that is suspected to
be a biospeckle source. Therefore, in this study, we decided to

0925-5214/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.postharvbio.2011.12.017
 A. Kurenda et al. / Postharvest Biology and Technology 67 (2012) 118–123
investigate the relation of the biospeckle activity with temperature.
The main objective of this experiment is to determine the extent
to which the activity coefficients, currently used in measuring, are
most useful for practical application, and whether biospeckle activ-
ity corresponds to the physical or biological phenomena. We have
chosen apples, which were stored at temperatures used in post-
harvest technology, as a model object.
The rate of processes based on enzymatic reactions is deter-
mined by the temperature coefficient Q10 , which describes a
process activity gradient with temperature rise of 10 ◦ C (Hegarty,
1973; Xiao, 2000). When the process is independent of the tem-
perature, the value of Q10 is 1. When the process depends on
temperature, Q10 > 1. The value of Q10 for diffusion is approxi-
mately 1, for a typical chemical reaction 2, and for some metabolic
reactions, even 3 (Kotov et al., 2007). Brownian motion veloc-
ity depends on the temperature in a linear way and its Q10 ratio
is about 1.1 (Jia et al., 2007). Since temperature in the range of
5–29 ◦ C is studied in this paper, the temperature compensation
phenomenon should be taken into account. Temperature compen-
sation is a phenomenon observed in many living organisms and
maintains a constant living activity in lower temperature com-
pared to the optimal temperature (Ruoff et al., 2007). It is assumed
that the mechanism of temperature compensation involves con-
junction of many temperature-dependent metabolic reactions in a
temperature-independent system based on feedbacks (Rajan and
Abbott, 2007).
2. Materials and methods
The device for biospeckle measurements was similar to that
which was previously used by Zdunek et al. (2008) (Fig. 1). The sys-
tem consists of a low power He–Ne laser (1 mW,  = 632.8 nm, LLR
811, Optel, Opole, Poland), with a microscope objective PZO Poland
10/0.24, 160/- (as a beam expander) to illuminate the sample, and
a CCD camera (Monochrome FireWire Astronomy Camera DMK
21AF04.AS, The Imaging Source Europe GmbH, Bremen, Germany)
with a 25 mm objective with a 20 mm extension ring, as a detector
of scattered light. The distance from camera to object was 37 mm
and laser to object was 180 mm. The illumination angle was  ≈ 30◦ .
Biospeckle activity was recorded as uncompressed movies (AVI, 8
bits, RGB24 codec) lasting 4 s with 15 frames per second (fps) rate.
The image resolution was 320 × 240 pixels, which corresponded
to an observation area of 7.5 mm2 . In the observations with con-
stant temperatures, movies were recorded for 95 min with lag of
5 min. In the observations with decreasing temperature, 4 s movies
were registered at the moments when the sample temperature
decreased by 1 ◦ C. The image exposure time of the CCD camera
was 1/250 s. Gain and brightness of the CCD camera was found
experimentally so as to avoid overexposures of pixels on the image
histogram. The image acquisition settings were kept unchanged
during the experiment.
The experiment was carried out in a temperature range that
suits both, the conditions in the orchard as well as those in which
fruit can be stored and sold. Measurements were planned in three
temperature regimes: 24 ◦ C (room conditions), 2.5 ◦ C (cold storage
room, normal atmosphere), and gradually free-falling temperature
from 29 ◦ C (warmer than the usual room temperature) to 2.5 ◦ C
(cold storage room, normal atmosphere). In the latter regime, typi-
cally the fruit did not reach the lower target temperature. Storage at
constant temperatures 2.5 ◦ C and 24 ◦ C was aimed at checking the
stability of the measuring system and checking possible existence
of natural oscillations of biological activity. The lowest temperature
achieved by the fruit was about 4–5 ◦ C. When the samples reached
the lowest temperature, they were kept for another 24 h to check if
the temperature still decreased. 35 apples (Malus domestica Borkh
119
var. ‘Idared’) purchased at the local market were used for the exper-
iment. The apples were not selected according to size or maturity
stage, and no other treatments were performed. The fruit were con-
ditioned for 24 h at the starting temperature for each temperature
regime prior to measurements. The regime with gradual reduc-
tion of the temperature was performed on 15 apples, whereas the
regimes with constant temperature involved 10 randomly selected
apples. After preconditioning, a standard resistance temperature
sensor, Pt 1000, was mounted approximately 1 mm under the apple
skin on the opposite side of the fruit than the point of illumination.
The temperature of the apples was measured with accuracy of 0.3 ◦ C
by a digital ohmmeter using a temperature calibration chart. The
temperature in the cold storage room was also monitored.
2.1. Indices of biospeckle activity
Three indices characterizing the biospeckle activity were calcu-
lated from the biospeckle movies:
(1) Cross-correlation coefficient Ck , where k = 0, 1, 2, . . . and
 = 1/15 s was calculated as the correlation coefficient of the
data matrix of the first frame (k = 0) with the data matrices of the
following frames (at k) from the analyzed biospeckle movie.
In this study, C4 was analyzed only as the correlation coeffi-
cient between the first frame k = 0 and the frame at k = 4 s,
because after this time, this parameter stabilized at a value
corresponding to the biospeckle activity, as in Zdunek et al.,
2008. Correlation coefficient Ck was determined by means of
“corrcoef” function available in the Matlab® R2010a (The Math-
Works, Inc., Massachusetts, U.S.A.)
(2) Speckle contrast (SC) along time defined as the ratio of the stan-
dard deviation  t of the intensity
 I to the temporal mean value
of the intensities in each pixel I on the speckle pattern was
t
also used for describing biospeckle fluctuations.

SC =  t (1)
I
t
The moment of inertia (IM) which is based on the creation of the
secondary image called the Time of the History Speckle Pattern
(THSP). This display is formed by comparing, side by side, chosen
rows extracted from registered frames. In our case, the line number
120 (the middle row in frame) was chosen for THSP formation. From
THSP image, co-occurrence matrix COM is created:
 
COM = Nij (2)
where the entries are the N number of occurrences of a certain
intensity value i, that is followed by an intensity value j in the THSP.
As a result of the normalization process of the co-occurrence matrix
(Eq. (2)) a new, modified matrix is obtained, in which the sum of
the components in each row equals 1.
Nij
Mij =  (3)
Nij
j
Finally, the IM is calculated according to Eq. (4) (Arizaga et al.,
1999):

IM = M ij (i − j)
2
(4)
ij
In summary, an increase in biospeckle activity corresponds to an
increase in IM and a decrease in C4 and SC. C4 and SC can change in
the range from 0 to 1.
120 A. Kurenda et al. / Postharvest Biology and Technology 67 (2012) 118–123

Fig. 1. Scheme of experimental setup for biospeckle activity measurements.

Table 1
Mean values of biospeckle activity indices with their percentage error expressed as standard deviation/mean value at constant temperatures of storage.

Parameter C4 in 4 ◦ C C4 in 24 ◦ C IM in 4 ◦ C IM in 24 ◦ C SC in 4 ◦ C SC in 24 ◦ C

Mean value 0.741 0.484 96629 214700 0.538 0.425

SD/mean (%) 0.41 1.80 10.71 7.07 3.15 2.23

C4 – correlation coefficient; IM – inertia moment; SC – speckle contrast; SD – standard deviation.

The temperature coefficient, Q10 , was calculated according to
the equation:
 K 10/(T1 −T2 )
1 perature decreased exponentially (Fig. 2). The fruit reached the
Q10 =
K2
where K1 and K2 are rate constants of a biological process at tem-
peratures T1 and T2 , respectively. Q10 was determined for all indices
of biospeckle activity (Xiao, 2000).
2.2. Statistical analysis
The experiment was performed on 10 or 15 apples that were
treated as replicates. Mean values with standard deviations and
other statistics were calculated with STASTICA® 8.0 (StatSoft, Inc.
1984–2008). One-way ANOVA was used for checking the temper-
ature effect on the biospeckle activity indices. Significance of the
effect was determined at p < 0.05. Post hoc analysis was performed
using corrected variance ω2 .
was obtained for SC (SD/mean < 3.5%), while the largest one for IM
(SD/mean < 11%).
When the apples were cooled in the storage room, their tem-
(5)
minimum temperature of ∼4–5 ◦ C after about 5 h. Fig. 2 also
presents the mean values of all biospeckle activity indices during
cooling of the apples. In terms of the mean values, the indices show
a tendency to decrease the biospeckle activity with the time of cool-
ing, which is visible as an increase in C4 and SC and a decrease in IM.
However, ANOVA on the raw data shows that the effect is signifi-
cant only in the case of C4 value, which is additionally confirmed
by the highest values of corrected variance (48%) (Table 2).
The relationship between temperature and biospeckle activity
determined by C4 is shown in Fig. 3. The C4 value decreases along
with the temperature increase, which means that biospeckle activ-
ity increases with temperature. The relation seems to be non-linear,
especially at temperatures higher than 20 ◦ C. On the other hand, at
low temperatures (close to 0 ◦ C) C4 is expected to reach a value

Table 2
3. Results ANOVA of the temperature effect on indices of biospeckle activity of apples.

Statistics Indices of biospeckle activity

Table 1 shows the mean values of biospeckle activity indices
with their percentage error expressed as a ratio of standard devi- C4 IM SC

ation to the mean value at constant temperatures 4 ◦ C and 24 ◦ C. F-value 13.49 1.02 0.43
The most stable parameter determining the biospeckle activity was Level of significance p <0.000 0.439 0.992
Corrected variance ω2 48% 0.1% 6%
C4 , which was particularly evident at 4 ◦ C (SD/mean < 0.5% at 4 ◦ C
and <2% at 24 ◦ C). Larger data scattering at constant temperatures C4 – correlation coefficient; IM – inertia moment; SC – speckle contrast.
 A. Kurenda et al. / Postharvest Biology and Technology 67 (2012) 118–123 121

Fig. 2. Changes of apple surface temperature and indices of biospeckle activity during cooling of the apples from 29 ◦ C to 5 ◦ C.

close to 1 due to sample freezing and loss of particle movement.
Therefore, the data could be modeled with a non-linear function
of the third-order. In Fig. 3, the function of best fit to mean values
of 15 replicates at each temperature is presented with appropriate
statistics.
The Q10 temperature coefficient calculated throughout the tem-
perature range for the three methods was 1.4 for the C4 , 1.1 for SC
and 1.2 for the IM. An additional procedure was to calculate Q10 in
the tested range in every 1 ◦ C. The results of these calculations are
shown in Table 3. Small changes of the Q10 in the case of SC and IM
and high volatility for the C4 are observed.
4. Discussion
It is believed that the biospeckle activity is the result of light
scattering by moving particles or organelles in cells. In the case of
harvested fruit, phenomena such as cell growth or division may
not play a significant role in generating movement in the cells,
because the anabolic processes are limited by stoppage of the influx
of water and nutrients. However, an important role can be played
by phenomena associated with the distribution of the accumulated
substances, transport of metabolites through the inner cell mem-
brane and within the cytoplasm, organelle movement, cytoskeletal
reconstruction and cell wall degradation. All these processes take
place as a result of two types of active transport. The movement of
the cytoplasm and the movement of macromolecular substances
and organelles are associated with the cytoskeletal and actin motor
proteins. In the case of transport through cell membranes, agents
that allow movement of substances are ion pumps and channels, as
well as the elements involved in the process of exocytosis. Since the
basis of these processes is obtaining energy from ATP hydrolysis,
which is a biochemical process, temperature dependence should
be present.
The results of this experiment revealed a decrease in biospeckle
activity when the biological sample is cooled within a typical post-
harvest temperature range. The determination coefficient of 0.96
for raw data of C4 vs. temperature shows potential of the biospeckle
method in practical application. However, it also shows the need
for measurements at constant temperature or for considering tem-
perature correction. Although all the methods for assessing the
biospeckle dynamics show a tendency to change with temperature,
speckle contrast and moment of inertia seem to be not feasible for
biospeckle activity evaluation. Data scattering among apples at a
certain temperature was too high in the case of these two indices.
Among the indices we evaluated for biospeckle activity, the corre-
lation coefficient is the best because measurement data processed
with this method have the lowest dispersion value and the highest
sensitivity to temperature.
Table 3
Q10 temperature coefficients in 10◦ temperature ranges and throughout the tem-
perature range from 5 to 29 ◦ C for the three indices of biospeckle activity.

Q10 for temperature range (◦ C) C4 SC IM

5–15 1.159 1.035 1.303

6–16 1.153 1.064 1.332
7–17 1.179 1.029 1.251
8–18 1.162 1.085 1.392
9–19 1.167 1.035 1.142
10–20 1.175 1.047 1.207
11–21 1.192 1.052 1.209
12–22 1.223 1.025 1.147
13–23 1.207 1.094 1.222
14–24 1.295 1.056 1.034
15–25 1.335 1.020 1.113
16–26 1.309 1.073 1.246
17–27 1.633 1.203 1.041
18–28 1.489 1.017 1.011
19–29 1.860 1.216 1.183
4–29 1.41 1.108 1.201

Q10 – temperature coefficient; C4 – correlation coefficient; IM – inertia moment; SC

Fig. 3. Changes of correlation coefficient C4 in relation to apple surface temperature. – speckle contrast.
122 A. Kurenda et al. / Postharvest Biology and Technology 67 (2012) 118–123
Additional information about the usefulness of the methods for
determining the biospeckle activity is provided by the change of
Q10 with increasing temperature. Although this parameter is used
to compare the temperature dependence between different bio-
logical parameters in our case, we decided to use it to compare
the performance of various methods for estimating activity. By
calculating the Q10 for the 10 ◦ C change in activity, we obtained
a description of the activity provided by the individual methods
in the temperature ranges examined. This has confirmed that the
best method among those evaluated for determining the biological
activity using biospeckle phenomenon is calculation of C4 , since
the biological activity calculated with this method is most simi-
lar in nature to the initial part of a sigmoid curve, which should
closely reflect the biological activity of the appropriate tissue in the
temperature range considered in this research (Ruoff et al., 2007).
The SC method with factor Q10 of 1.1 for the range 4–29 ◦ C prob-
ably does not indicate a normal level of biological activity due to
slight changes in temperature coefficient even at the highest tem-
perature range of 19–29 ◦ C. In our opinion, the worst parameter of
biospeckle activity is IM, which has the highest dispersion, both in
constant temperatures (Table 1) and during the lowering of fruit
temperature and also showed the highest Q10 factor for the lowest
temperatures, which is obviously the wrong result. The explana-
tion for this phenomenon may be the experiment made by Nobre
et al. (2009), demonstrating that the method of IM in low frequen-
cies cannot document statistically significant changes in activity,
but on the other hand the specific sensitivity of this method on
certain parameters in recorded movies can also result in excessive
scattering of the results.
It should be taken into account that even for C4 biospeckle activ-
ity does not fall below 0.3 in the lowest temperature and the Q10
coefficient has a value similar to that specified for the Brownian
motion. In practice there may, therefore, occur a situation where
the activity at temperatures below 10 ◦ C will be the result of the
Brownian motion and not the biological activity of tested fruit.
Another reason for the C4 ratio may remain at a relatively high
level, despite the fruit temperature about 4 ◦ C, may be exothermic
biochemical reactions that occur inside the fruit tissue. During the
experiment we noticed that the minimum value of temperature
under the apple skin was slightly higher than the target tempera-
ture in the storage room (2.5 ◦ C), i.e. the apples reached ∼4–5 ◦ C.
Longer cooling (up to 24 h at 2.5 ◦ C) did not cause any further tem-
perature decrease. Exothermic reactions in the tissues of apples as
well as high concentrations of solutes in the cytoplasm may cause
certain biospeckle activity to be registered even slightly below 0 ◦ C.
Biochemical reactions that cause higher temperatures inside the
fruit than the ambient temperature may also partly explain the
low corrected variance for C4 . Of course, low ω2 for SC and IM
at respectively 6% and 0.1%, are caused mainly by the large dis-
persion of biospeckle activity counted for this methods, but in the
case of C4 , corrected variance at 48% may be underestimated. The
reason for this, may be the different character changes of tem-
perature and changes in biospeckle activity of fruit. The relatively
high biospeckle activity due to metabolic reactions, especially at
temperatures below 10 ◦ C, can cause decreases in the value of the
corrected variance which, paradoxically, may also indicate a sig-
nificant share of biological processes in the creation of biospeckle
activity. This phenomenon may be, in fact, a form of temperature
compensation (decrease in the rate of biological processes is slower
than the decrease in temperature) but the low biological activ-
ity measured by Q10 at low temperatures (1.15 for the 5–15 ◦ C
range) compared to high temperatures (1.86 for the 19–29 ◦ C range)
demonstrates lack of temperature compensation for the apple tis-
sue in the form described in the literature.
Taking into account the practical application of the biospeckle
method to assess the biological activity of fruit, it is important
that the same recordings were analyzed in all three methods of
biospeckle activity assessment, while only the C4 method showed
statistically significant dependence on temperature. In conclusion,
it is the method of C4 that can be used to yield a new, commercial
technique to assess the quality of fruit.
Admittedly, the current state of development of the biospeckle
method allows only for laboratory use, e.g. evaluation of biological
activity in plant and animal tissues, but the rapid development of
statistical methods for evaluation of activity of this phenomenon,
may allow application in fruit and vegetable sorting lines.
Currently, in literature reports, we can find information indi-
cating the possible application of this technique in evaluation of
the quality of apples during shelf-life (Zdunek et al., 2008) and
starch content (Zdunek and Cybulska, 2011), but potentially, the
measurement of other quality parameters will be possible.
Opportunity to evaluate the above parameters can be used
as a supplement to existing fruit sorting lines based on the NIR
technique, which allows for example to sort the fruit in terms of
sugar content or acidity, but not starch content. Favorable factor
in comparison to other non-destructive techniques is also price of
measuring set, which is relatively low due to the use of only the
laser, camera and computer (Fig. 1).
To enable practical use of a biospeckle technique, our future
research will include creating new and improving existing meth-
ods of determining biospeckle activity. In addition, another goal
of further study should be determination whether the biological
activity resulting from the biospeckle activity is proper in compar-
ison to the real biological process such as cytoplasmic streaming,
and not only to the theoretical data, as in the case of this work.
5. Conclusions
This work revealed that among the methods we examined, the
best method for evaluation of biospeckle activity on apples is the C4
coefficient. Other parameters, such as IM and SC, have dispersion
of measured values too large for their use.
The character of decline in biospeckle activity with decreas-
ing temperatures as measured by the coefficient of Q10 and the
existence of relatively high metabolic activity of the fruit in a low
ambient temperature indicates that the phenomenon arises mainly
due to biochemical metabolic processes, while physical phenom-
ena such as Brownian motion or diffusion may be important mainly
at low temperatures (below 10 ◦ C).
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