____________________________________________________

MARINA MESOPOTAMICA 23(2):363-376 2008

CONCENTRATIONS OF COPPER, CADMIUM,
COBALT, MANGANESE, NICKEL, AND LEAD IN THE
MUSCLES OF FRESHWATER FISHES, Crassius crassius,
Aspius vorax and Barbus luteus COLLETED FROM AL-
HAMMAR MARSH (SOUTH OF IRAQ).

Hamid T. Al-Saad1; Jabbar K. Abdul-Hassn2; Maha K.Zukhair3

Ibraheim A. Abd4
1
Marine Scie center, Basrah Univ., Iraq 2 fisheries and marine resources dept.,
Agri. Coll. 3Biology Dep., Coll. of Science, Basrah Univ., Iraq
4
Minster of Environment, Baghdad-Iraq

ABSTRACT
To assess the significance of metals in fishes from Al-
Hammer marsh (South of Iraq), preliminary data is presented on
concentrations of Cu, Cd, Co, Mn, Ni and Pb in tissues of three
fresh water fishes (Crassius crassius, Aspius vorax and Barbus
luteus) collected in 2006-2007 seasonally period. Copper range
from Below detection limit (BDL) in B. luteus tissues for all
sampling seasons to 4.12 (µg/g. dw) in the muscles, for Cd, Co
and Ni were range between BDL to 24.49 Cd, 4.86 (µg/g. dw) in
all tissues and 88.85 Ni (µg/g. dw) in the A. vorax and B. luteus
muscles respectively. Metal concentrations seemed to be
increased through hot periods (Summer and Spring) compared
with cold periods (Autumn and Winter), During data analyses,
C. crassius tend to accumulate more concentration of all study
metals than A. vorax and B. luteus.

INTRODUCTION
Trace metals are generally released in aquatic environments in different
ways and accumulation of these metals is dependent on the concentration of
the metal, the type of aquatic animals and the exposure period
(Canli et al., 1998). Levels of heavy metals in fish have been widely
reported (Romeo et al., 1999, Edwards et al., 2001, Gaspic et al., 2002,
Satarug et al., 2003, Kuçuksezgin et al., 2006).
Cadmium has not been found to occur naturally in its pure state and its
concentration seems to be directly proportional to zinc and lead
concentrations. Use of Cadmium in agriculture and industry has been
identified as a major source of wide dispersion into the environment and
food.
 364 Al-Saad H.T. et al.
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The major route of exposure to Cd for the non-smoking general
population is via food; the contribution from other pathways to total uptake
is small (Goyer, 1991). and many chemical elements that are present in
aquatic food are essential for human life at low concentrations, but can be
toxic at high concentrations while Others such as mercury, cadmium and
lead have no known essential function in life and are toxic even at low
concentrations when ingested over a long period (Williams and Moore,
2003). Therefore, many consumers regard any presence of these elements
in fish as a hazard to health (Oehlenschlager, 2005).
To understanding the relationship in fish between environmental
exposure and the resulting concentration of contaminants in fish tissues is
necessary, but often lacking, basis for effective use of fish as indicators of
chronic environmental contamination (Goyer, 1991). When fish are used as
pollution indicators, the underlying objective is protection of the organisms
themselves, which requires an understanding the relationships between
tissue residues, impacts on the animals and ultimately on populations and
community assemblages (Canli and Atli, 2005).
Few studies have been undertaken to assess the concentration of
elements in concerned different species of fish collected from Arabian Gulf,
Shatt al Arab river and South Iraqi marshes. Due to the fact that fish are
considered an essential part of the diet in the region (Abaychi and Al-Saad
1988; Al-Saad et al., 1994; Mustafa et al., 1995; Al-Saad et al., 1996, Al-
Saad et al., 1997).
Therefore, an investigation was usual assumption is that contaminant
concentrations are positively correlated with contaminant exposure. Their
components may alter quantitatively and qualitatively the natural
biochemical cycle (Grimanis et al., 1978). Fish which live in polluted
waters may accumulate toxic trace elements via their food chains or via
water column thus possibly endangering human health. In the Arabian Gulf
region, recently vast industrial, agricultural, economic and social
developments have taken place, in addition to an increase in population.
This may enhance the magnitude of environmental pollution year by year.
Fish species usually accumulate small quantities from heavy metals, but
predatory fishes sometimes accumulate greater quantities than the rest of
aquatic organisms (Canli and Atli, 2005). Hallebach (1985) demonstrates
the fact that the heavy metals first of all penetrate through the mucous
membrane of the branchia, from where they spread after some days and
accumulate in the kidneys and the liver.
Over the last few decades, there has been growing interest in
determining heavy metal levels in the marine environment and attention
was drawn to the measurement of contamination levels in public food
supplies, particularly fish (Dietz et al., 1996; AMAP, 1997).
Trace metals in fishes from Al-Hammar Marsh 365
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The contamination of freshwater with heavy metals has become a matter of
great concern, not only because of the threat to public water supplies, but
also their damage caused to the aquatic life (Canli et al., 1998).
Contamination with heavy metals may have devastating effects on the
ecological balance of the aquatic environment and the diversity of aquatic
organisms becomes limited with the extent of contamination (Suziki et al.,
1988).
This study aimed to determine the natural occurrence of some metals in
selected kinds of fresh water fishes collected from Al-Hammer marsh
(southern Iraq).

MATERIALS AND METHODS

Fish samples were collected from Al-Hammer marsh area (southern
Iraq) from location as shown in fig. (1) during the period 2006-2007 by
"Gill nets". Metals analysis was performed on the 63 um fraction of the fish
muscles, which has been separated by sieving after drying and grinding.
The determination of metals in fish samples was done according to the
following procedure described by Sturgeon et al., (1982). Concentrated of
hydrochloric acid (HCl) and nitric acid (HNO3) 1:1 was added to each
sample and evaporated to near dryness on the hotplate at 80ºC, then mixture
of concentrated percloric acid HClO4 and HF (1:1) was added. After
heating to near dryness, 20ml of 0.5 HCl were added and cooled for 10
mins. The extraction was decanted into 25 ml plastic volumetric flask.
Finally the volume of samples were stored for analysis using a Pye-Unicam
Atomic Absorption.

RESULTS AND DISCUSSION

The mean concentrations of six metals studied (Copper, Cadmium,
Cobelt, Manganise, Nickel and lead) in three fresh water fish muscles
(C. crassius, A. vorax and Barbus luteus) have been illustrated in Figs.
(2, 3, 4, 5). The values of metals showed relative variation among different
fish species during different seasons, a substantial variability was noted for
some metals such as nickel, Cadmium and lead in some study species
(A. vorax and B. luteus).
Gaspic et al., (2002) mentioned that the distribution patterns of the
studied metals exhibited similar trend, since their concentrations increased
during hot periods (Spring and summer seasons. Figs. 4, 5), compared with
those in cold periods (Autumn And winter seasons) Figs.(2, 3). Fish tissues
from A.vorax were detected in all samples for study metals at Autumn
season (Fig. 2), but in the same time some metals are below the limits of
detection in each cases such as Cd, Co, Ni, at Autumn, winter, spring and
summer respectively, while it is true for muscle in case of lead.
 366 Al-Saad H.T. et al.
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Fig. (1) showed collection station through Al-Hammer marsh (southern

Iraqi marshes)

High Cd (at winter) and Pb (at summer) levels in fish muscles indicate
that may be contamination has occurred as pointed by (Parsons, 1999). It is
clear from the obtained results that nickel showed it's highest values in
C.crassius tissues during all seasons, but fig. (2) showed that copper,
Cadmium, Cobalt and nickel concentrations are below the limits of
detection in many cases, the data was summarized the statistical analyses
for present results (using Spss statistical program.).
Few data about metal concentrations in Al-Hammer marsh have been
reported dealing with general biota especially fish tissues, Al-Khafaji
(2005) has been determined the concentrations of six study metals in some
C. luteus tissues (Gill, liver, mules and kidney) these concentrations were:
0.0-6.1 (as µg/g dw) in the tissues which is agree with present results.
While metal concentrations in eleven aquatic plants from Al-Hammer
marsh were: Cd:0.0 -5.23/Mn;1.20-3.10/Ni:0.86-10.53/ Pb: 0.09-0.86 µg/g
dw (Al-Saad et al., 1994). Mustafa et al. (1995) were determined the
seasonal variations of some metals in aquatic vascular plants of Al-Hammer
marsh, the results were: Cd:nd-1.74/Mn:1.20-4.00/Ni:0.0 -6.73/Pb:0.08-
2.84.
Trace metals in fishes from Al-Hammar Marsh 367
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Fig. (2): Concentration of metals in the tissues of (C. crassius, A. vorax and
B. luteus) collected during autumn season

Fig. (3): Showed concentration of metals in the tissues of (C. crassius, A.

vorax and B. luteus) collected during winter season
 368 Al-Saad H.T. et al.
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Fig. (4): Showed concentration of metals in the tissues of (C. crassius,

A. vorax and B. luteus) collected during spring season

Fig. (5): Showed concentration of metals in the tissues of (C. crassius,

A. vorax and B. luteus) collected during Summer season
Trace metals in fishes from Al-Hammar Marsh 369
-------------------------------------------------------------------------------------------------------------
The distribution patterns of metals in the water, sediment and biota
increased in the hot seasons (spring and summer) and may be attributed to
the release of metals from sediments to the overlying water under the effect
of both high temperature and fermentation process resulted from
decomposition of organic matter (Elewa et al., 2001). Moreover, these
increase in water coincided with the decrease in the same metal's values in
the sediments and biota. In addition, the values of metals showed an
obvious decrease in the water during cold period (winter and autumn) with
a correspondent increase in the sediments due to precipitation of heavy
metals from water column to the sediments under high pH values and the
adsorption of heavy metals onto organic matter and their settlement
downward (Goher, 2002).
Because most trace metals tend to accumulate in the different body
organs, these metals are dangerous for fish and in turn they lead to serious
problems in both man and animals (Marzouk, 1994). Fishes may absorb
dissolved elements and trace metals from its feeding diets and surrounding
water leading to their accumulation in various tissues in significant amounts
and exhibit eliciting toxicological effects at target criteria (McCarthy and
Shugart, 1990; Parsons, 1999).
In present study, which are varied mainly due to the different fish
habitat and the influence of the surrounding ecosystem. Table (1) showed
these differences in the ranges and data statistical analyses. These results
are agreed with that reported by Abaychi and Al-Saad (1988), FAO (1996)
Zyadah (1997) and Abdel-Baky et al. (1998).
Few local studies have been done on Arabian Gulf and Shatt Al Arab
River, which were concerned determination of metals in water, sediments,
and different biota especially fishes as economically source in the region.
Many studies have been done using many species from fishes as bio-
indicator for pollution monitoring because most of fish tissues can
accumulate heavy metals from aquatic environment (Abdul-Hassan and
Kareem, 1989; Abdul-Hassan et al., 1989; Ali and Fishar, 2005; Canli and
Atli, 2005; Ashraf, 2006; Dalman et al., 2006), due to this reason a few
studies have been reported dealing with different fish species collected
from area closed to the present study area.
Many studies have been done using many fish species as a bio-indicator
for pollution monitoring because most of fish tissues can accumulate heavy
metals from aquatic environment (Abdul-Hassan and Kareem, 1989;
Abdul-Hassan et al., 1989, Ali and Fishar, 2005: Canli and Atli, 2005;
Ashraf, 2006; Dalman et al., 2006). Abaychi and Al-Saad (1988) were
determined metal concentrations in some fish species collected from Shatt
Al-Arab river (six fresh water species),
 370 Al-Saad H.T. et al.
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Table (1): means and statistical analyses of metal concentrations (as
µg/g dw) in the tissues of C. crissius, A. vorax and B. luteus
through study seasons.
Autumn Winter
Metal Species Range Sig. Metal Species Range Sig.
C. crassius 3.91-4.45 S.c C. crassius 4.01-4.22 S.c
Cu A. vorax 6.06-6.31 S.c Cu A. vorax 4.11-4.13 S.c
B. luteus 1.34-2.11 S.c B. luteus 2.01-2.09 S.c
C. crassius Nd 0 C. crassius 19.56-19.66 S.b
Cd A. vorax 4.80-5.03 S.c Cd A. vorax 14.68-14.71 S.c
B. luteus Nd 0 B. luteus 14.37-14.90 S.c
C. crassius 4.79-4.97 S.a C. crassius Nd 0
Co A. vorax 4.71-4.99 S.c Co A. vorax 4.71-5.02 S.b
B. luteus Nd 0 B. luteus Nd 0
C. crassius 7.81-8.17 S.a C. crassius 3.89-4.05 S.b
Mn A. vorax 7.58-8.13 S.a Mn A. vorax Nd 0
B. luteus 3.91-4.09 S B. luteus 3.90-4.06 S.b
C. crassius 88.77-88.90 S.c C. crassius 59.12-59.33 S.c
Ni A. vorax 29.42-29.81 S.c Ni A. vorax Nd 0
B. luteus 29.42-29.79 S.c B. luteus Nd 0
C. crassius 4.10-5.09 S.a C. crassius 4.10-5.30 S.b
Pb A. vorax 6.21-6.30 S.b Pb A. vorax 5.91-6.50 S.b
B. luteus 6.56-7.23 B. luteus 8.91-9.40 S.b
Spring Summer
Metal Species Range Sig. Metal Species Range Sig.
C. crassius 4.10-4.15 S.c C. crassius 4.07-4.21 S.a
Cu A. vorax 2.00-2.13 S.c Cu A. vorax 1.99-2.10 S.a
B. luteus Nd S.c B. luteus 1.99-2.11 S.a
C. crassius Nd 0 C. crassius 9.59-10.00 S.a
Cd A. vorax Nd S.c Cd A. vorax 24.48-24.50 S
B. luteus Nd 0 B. luteus Nd 0
C. crassius Nd S.a C. crassius Nd 0
Co A. vorax Nd S.c Co A. vorax Nd 0
B. luteus Nd 0 B. luteus 4.55-5.10 S.a
C. crassius 3.88-4.16 S.a C. crassius 3.92-4.07 S.b
Mn A. vorax 7.77-8.15 S.a Mn A. vorax 3.96-3.99 S.b
B. luteus 3.90-4.10 S B. luteus 3.70-4.15 S.b
C. crassius 29.51-29.67 S.c C. crassius 27.31-29.82 S.c
Ni A. vorax 29.49-29.71 S.c Ni A. vorax Nd 0
B. luteus Nd S.c B. luteus 29.52-29.74 S.c
C. crassius 5.91-6.30 S.a C. crassius 6.23-6.81 S.c
Pb A. vorax 3.98-4.13 S.b Pb A. vorax 7.20-7.99 S.b
B. luteus 4.50-4.88 Sig. B. luteus 9.10-9.67 S.b
S= Significant, a=P<0.001, b=P>0.01, C=P>0.005
Trace metals in fishes from Al-Hammar Marsh 371
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the concentration range for Cd was 0.00-0.02, for Co=0.20-0.80, for
Cu=3.9-10.3, for Mn=1.2-7.3, for Ni=0.0=4.3, and for Pb=0.16-0.82 (as
µg/g dw). While concentration ranges of these metals in fourteen marine
fish species were collected from Arabian Gulf, the ranges were for Cd= 0.1-
0.28, for Co=0.4-1.5, for Cu=3.1-16.4, for Mn=0.0-6.9, for Ni= 0.0-6.8 and
for Pb=0.02-0.50 (as µg/g dw).
The ranges of Cd=0.50,0.03, for Cu=37,1.57, for Mn= 7.9, 1.79, for
Ni= 39.3, 2.27 and for Pb=5.9,0.06 as as µg/g dw in the tissues of shrimps
and Liza subviridus fish respectively (Al-Saad and Al-Imarah, in press)
which are agree with present study.
Trace metals enter the aquatic environment of southern Iraq from both
natural and anthropogenic sources (Abaychi and Al-Saad, 1988). Natural
sources include storm dust fall, erosion or crusted weathering and dead and
decomposition of the biota in the water, whereas the anthropogenic sources
include sewage wastes, industrial effluent, automobile effluent, petroleum
and fertilizer industry effluent .The accumulation of these metals in the fish
muscles depend on the concentration of these metals, exposure time,
physiological conditions of theses organism and environmental factors
(Al-Saad et al., 1996). These different in concentration may related also to
the food habitat of these fish which played the dominant role. There are few
data available on the concentrations of trace metals in different tissues of
fish from Shatt Al-Arab and its estuary and other area of the Arabian Gulf
which could used together with values from world wide and heavily
polluted site for comparative purpose. All the concentrations of trace metals
obtained in these fish in the present study are much lower than those
reported at heavily polluted site (Table 2).
 372 Al-Saad H.T. et al.
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Table (2): Trace metal concentrations in muscle of fish (µg/g

dry weight) from Iraqi and NW Arabian Gulf in
comparison with word wide average concentration
and polluted site

location Cd Co Cr Fe Mn Ni Pb V Zn Source
Abaychi
Shatt and
0.10 0.60 4.50 60.5 7.30 - 0.46 1.00 13.0
Al-Arab Douabul
(1988)
Abaychi
Arabian and
0.05 1.20 0.80 55.2 6.90 4.80 0.50 4.60 10.7
Gulf Douabul
(1988)
Khor Al- Al-Edanee
0.90 - - 51.5 1.70 6.00 3.90 5.40 16.3
Zubair et al. (1991)
Fowler
Kuwait 0.35 0.04 0.14 12.5 0.52 - 0.27 0.07 20.0
et al.,(1993)
Shatt
Al-Saad
Al-Arab ND 0.30 ND 43.9 1.40 4.16 0.33 1.73 2.93
et al.,(1997)
estuary
Shatt Al-Khafaji
ND 0.11 - - 0.09 0.36 0.05 0.22 5.70
Al-Arab (2005)
Fowler
Kuwait 0.35 0.04 0.14 12.5 0.52 - 0.27 0.07 20.0
et al.,(1993)
Al-Hamme 0- 0- 195- 3.75- 48- 4.1- Present
- - -
marsh 24.49 4.86 411 5.00 88.85 9.67 work
World Bryan
0.10 0.20 0.10 50.0 10.0 1.00 3.00 1.00 80.0
wide (1978)
Dallinger
Polluted and
0.92 - 8.90 - 3.90 7.80 20.1 - 517.8
region Kautzky
(1985)
Trace metals in fishes from Al-Hammar Marsh 373
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‫ﺘﺭﻜﻴﺯ ﻋﻨﺎﺼﺭ ﺍﻟﻨﺤﺎﺱ‪ ،‬ﻜﺎﺩﻤﻴﻭﻡ‪ ،‬ﻜﻭﺒﻠﺕ‪ ،‬ﻤﻨﻐﻨﻴﺯ‪ ،‬ﻨﻴﻜل ﻭﺍﻟﺭﺼﺎﺹ ﻓﻲ‬

‫ﺃﻨﺴﺠﺔ ﺍﺴﻤﺎﻙ ﺍﻟﻤﻴﺎﻩ ﺍﻟﻌﺫﺒﺔ )ﻜﺭﺍﺴﻴﻥ‪ ،‬ﺸﻠﻙ ﻭﺍﻟﺤﻤﺭﻱ( ﺠﻤﻌﺕ ﻤﻥ ﻫﻭﺭ‬
‫ﺍﻟﺤﻤﺎﺭ )ﺠﻨﻭﺏ ﺍﻟﻌﺭﺍﻕ(‬

‫‪،3‬‬
‫‪4‬‬
‫ﺇﺒﺭﺍﻫﻴﻡ ﻤﻬﺩﻱ ﻋﺒﺩ‬ ‫ﺤﺎﻤﺩ ﻁﺎﻟﺏ ﺍﻟﺴﻌﺩ‪ ،1‬ﺠﺒﺎﺭ ﺨﻁﺎﺭ ﻋﺒﺩﺍﻟﺤﺴﻥ‪ ،2‬ﻭﻤﻬﺎ ﺨﻠﻑ ﺯﻏﻴﺭ‬
‫‪ -2‬ﻗﺴﻡ ﺍﻷﺴﻤﺎﻙ ﻭﺍﻟﺜﺭﻭﺓ ﺍﻟﺒﺤﺭﻴﺔ‪ ،‬ﻜﻠﻴﺔ ﺍﻟﺯﺭﺍﻋﺔ‪،‬‬ ‫‪ -1‬ﻤﺭﻜﺯ ﻋﻠﻭﻡ ﺍﻟﺒﺤﺎﺭ‪ ،‬ﺠﺎﻤﻌﺔ ﺍﻟﺒﺼﺭﺓ‬
‫‪ -4‬ﻭﺯﺍﺭﺓ ﺍﻟﺒﻴﺌﺔ‪ ،‬ﺒﻐﺩﺍﺩ‬ ‫‪ -3‬ﻗﺴﻡ ﻋﻠﻭﻡ ﺍﻟﺤﻴﺎﺓ‪ ،‬ﻜﻠﻴﺔ ﺍﻟﻌﻠﻭﻡ‪ ،‬ﺠﺎﻤﻌﺔ ﺍﻟﺒﺼﺭﺓ‪،‬‬

‫ﺍﻟﻤﺴﺘﺨﻠﺹ‪:‬‬
‫ﻟﻐﺭﺽ ﺍﻟﺘﻤﻬﻴﺩ ﺇﻟﻰ ﻤﻌﺭﻓﺔ ﻤﻌﻨﻭﻴﺔ ﻟﺘﺭﻜﻴﺯ ﺍﻟﻌﻨﺎﺼﺭ ﻓﻲ ﺃﻨﺴﺠﺔ ﺒﻌـﺽ‬
‫ﺍﺴﻤﺎﻙ ﻫﻭﺭ ﺍﻟﺤﻤﺎﺭ‪ ،‬ﻋﺭﻀﺕ ﺍﻟﺒﻴﺎﻨﺎﺕ ﺍﻟﺘﻤﻬﻴﺩﻴﺔ ﻟﺘﺭﻜﻴﺯ ﺍﻟﻨﺤﺎﺱ‪ ،‬ﺍﻟﻜﺎﺩﻤﻴﻭﻡ‪،‬‬
‫ﺍﻟﻜﻭﺒﻠﺕ‪ ،‬ﺍﻟﻤﻨﻐﻨﻴﺯ‪ ،‬ﺍﻟﻨﻴﻜل ﻭﺍﻟﺭﺼﺎﺹ ﻓﻲ ﺜﻼﺙ ﺍﺴﻤﺎﻙ ﻤﻴﺎﻩ ﻋﺫﺒﺔ )ﺍﻟﻜﺭﺍﺴﻴﻥ‪،‬‬
‫ﺍﻟﺸﻠﻙ ﻭﺍﻟﺤﻤﺭﻱ( ﺠﻤﻌﺕ ﺒﻔﺘﺭﺓ ﻤﻭﺴﻤﻴﺔ ﺨﻼل‪ .2007-200 6‬ﻤﺩﻯ ﺍﻟﻨﺤﺎﺱ‬
‫ﻜﺎﻥ ﺒﻴﻥ ﻋﺩﻡ ﺘﺤﺴﺱ ﺠﻬﺎﺯ ﺍﻻﻤﺘﺼﺎﺹ ﻓﻲ ﺃﻨﺴﺠﺔ ﺍﺴـﻤﺎﻙ ﺍﻟﺤﻤـﺭﻱ ﻟﻜـل‬
‫ﻋﻴﻨﺎﺕ ﺍﻟﻤﻭﺴﻡ ﺍﻟﻰ ‪ 4.12‬ﻤﺎﻴﻜﺭﻭﻏﺭﺍﻡ‪/‬ﻏﺭﺍﻡ )ﻭﺯﻥ ﺠـﺎﻑ( ﻓـﻲ ﺍﻷﻨـﻭﺍﻉ‬
‫ﺍﻟﻤﺩﺭﻭﺴﺔ‪،‬ﻋﻨﺎﺼﺭ ﺍﻟﻜﺎﺩﻤﻴﻭﻡ‪ ،‬ﻜﻭﺒﻠﺕ ﻭﺍﻟﻨﻴﻜل ﻜﺎﻨﺕ ﺘﺤﺕ ﺘﺤـﺴﺱ ﺍﻟﺠﻬـﺎﺯ‬
‫ﺃﻴﻀﺎ ﻓﻲ ﻜل ﺍﻷﻨﺴﺠﺔ ﺍﻟﻰ ‪ 24.49‬ﻜﺎﺩﻤﻴﻭﻡ‪ 4.86 ،‬ﻓﻲ ﺠﻤﻴﻊ ﺍﻷﻨﺴﺠﺔ ﺍﻟـﻰ‬
‫‪ 88.85‬ﻤﺎﻴﻜﺭﻭﻏﺭﺍﻡ ‪/‬ﻏﺭﺍﻡ ﻨﻴﻜل ﻓﻲ ﺃﻨﺴﺠﺔ ﺍﺴﻤﺎﻙ ﺍﻟﺸﻠﻙ ﻭﺍﻟﺤﻤﺭﻱ ﻋﻠـﻰ‬
‫ﺍﻟﺘﻭﺍﻟﻲ‪ .‬ﺘﺭﺍﻜﻴﺯ ﺍﻟﻌﻨﺎﺼﺭ ﺒﺩﺃﺕ ﺒﺎﻟﺯﻴﺎﺩﺓ ﻓﻲ ﺍﻟﻔﺘﺭﺍﺕ ﺍﻟﺤﺎﺭﺓ )ﺼﻴﻑ ﻭﺭﺒﻴـﻊ(‬
‫ﻤﻘﺎﺭﻨﺔ ﺒﺎﻟﻔﺘﺭﺍﺕ ﺍﻟﺒﺎﺭﺩﺓ )ﺨﺭﻴﻑ ﻭﺸﺘﺎﺀ(‪ ،‬ﻤﻥ ﺨﻼل ﺘﺤﻠﻴل ﺍﻟﺒﻴﺎﻨﺎﺕ ﺍﺘﻀﺢ ﺃﻥ‬
‫ﺃﻨﺴﺠﺔ ﺍﺴﻤﺎﻙ ﺍﻟﻜﺭﺍﺴﻴﻥ ﺘﻤﻴل ﻟﺘﺭﺍﻜﻡ ﺍﻟﻌﻨﺎﺼﺭ ﺍﻟﻤﺩﺭﻭﺴـﺔ ﻤﻘﺎﺭﻨـﺔ ﺒﺄﻨـﺴﺠﺔ‬
‫ﺍﺴﻤﺎﻙ ﺍﻟﺸﻠﻙ ﻭﺍﻟﺤﻤﺭﻱ‪.‬‬