Saudi Journal of Biological Sciences xxx (xxxx) xxx

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Saudi Journal of Biological Sciences

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Original article

Health risk assessment by toxic metals in little egrets (Egretta garzetta)

and food chain contaminations
Madiha Rani a, Rizwan Ullah a, Mona S Alwahibi b, Mohamed S. Elshikh b,⇑,
Mohamed Ragab AbdelGawwad d,⇑, Adeel Mahmood c
a
Department of Zoology, Mirpur University of Science and Technology (MUST), Mirpur 10250 AJK, Pakistan
b
Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
c
Department of Environmental Sciences, GC Women University, Sialkot 51310, Pakistan
d
Genetics and Bioengineering, Faculty of Engineering and Natural Sciences, International University of Sarajevo, 71210 Sarajevo, Bosnia and Herzegovina

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

Article history: This study analysed heavy metals from little egret (Egretta garzetta). Egret’s Eggs, egg shells, food (fish and
Received 14 July 2021 insects), blood, meat samples (thigh, liver, and chest), water, soil and sediments samples were collected
Revised 19 August 2021 from the two selected sites of the study area. Samples were analysed on flame atomic absorption spec-
Accepted 31 August 2021
trometer after acid digestion. Detected metals were found almost inline of concentrations when com-
Available online xxxx
pared with the both sites. Among detected metals Mn was found higher in concentration (mg/g) i.e.
18.509 followed by Zn i.e. 9.383, Ni, Cu, Pb and Cd. Sediment exhibited higher levels (mg/g) of metals
Keyword:
(25.061) followed by the meat (19.044) egrets food (18.825), excreta (16.26), blood serums (4.577), eggs
Heavy metals
Biomonitoring
(3.626) and water samples (2.432).The level of metals in sediments of the study are showed environmen-
Little egret tal concerns. Health risks were also investigated that were compared to guidelines of WHO and FAO
Flame Atomic Absorption threshold limits. It was found a marginal health risk to life through detected metals. This study revealed
Spectrophotometer that little egret are good bio-indicator for the screening and investigation of contaminates presence in the
Food web contaminations environment.
Ó 2021 Published 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 include nickel, arsenic, and zinc. These metalloids even in a smaller
quantity can cause toxicity to living organisms. Heavy metals can
Egretta garzetta is a bird of size ranged from 55 to 65 cm in generate from point sources and non-point sources of pollution
length with the measurement of 88 to 106 cm from tip to tip with including mining areas, foundries, smelters, and other industrial
weight ranged from 350 to 550 g. During breeding season two activities which ultimately contaminate the environment. Due to
elongated nape plumes appeared on the breast and back of the bird prolonged stay of such metals in environment they are placed to
while bill and eyes turned red or blue (Hancock et al., 2010). type of inorganic toxicants. Due to anthropogenic activities heavy
In certain aquatic ecosystems egrets are considered excellent metals incorporate directly from geological cycle and contribute
source of food being provided to the not only to the invertebrates as an environmental toxicity. Certain heavy metals such as Cam-
but the higher organisms. bium (Cd), Copper (Cu), Zinc (Zn), Lead (Pb) and Cobalt (Co) are
Heavy metals are present in environment due to natural and absorbed in living organism from bottom line of ecosystem and
anthropogenic activities which are composed of metalloids those cause toxicity (Dauwe et al., 2005). Such heavy metals become part
of the proteins and lipid contents in the living organism and cause
⇑ Corresponding author at: Department of Botany and Microbiology, College of
negative impacts during cellular metabolic activities (Koivula and
Science, King Saud University, Riyadh 11451, Saudi Arabia. Eeva., 2010). In the newly hatched baby birds Cd cause disease like
E-mail addresses: melshikh@ksu.edu.sa (M.S. Elshikh), mragab@ius.edu.ba cancer and in male baby bird destruction of testicular (Burger and
(M.R. AbdelGawwad). Gochfeld, 2009).
Peer review under responsibility of King Saud University. Certain investigations on this bird showing that for the assess-
ment of heavy metals different body part of the bird can be used
such as feathers, liver, blood (Malik and zeb., 2009). Eggs (Burger
an Gochfeld., 2000a, 2000b) and its shell (Ayes., 2007) can also
Production and hosting by Elsevier be used for the investigation of different metals in this bird, partic-

https://doi.org/10.1016/j.sjbs.2021.08.106
1319-562X/Ó 2021 Published 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 as: M. Rani, R. Ullah, Mona S Alwahibi et al., Health risk assessment by toxic metals in little egrets (Egretta garzetta) and food chain
contaminations, Saudi Journal of Biological Sciences, https://doi.org/10.1016/j.sjbs.2021.08.106
M. Rani, R. Ullah, Mona S Alwahibi et al. Saudi Journal of Biological Sciences xxx (xxxx) xxx

ularly the female bird is considered a mean of excretion of these added to the soil samples which were heated again till dryness. For
toxic heavy metals (Lam et al., 2005). The concentration of Cd in filtration Whatman filter paper was used, to raise the volume up to
tissues of aquatic birds is reported higher when compared with 25 ml the distilled water and remaining solution was added.
other metals.
The massive traffic, industries and burning of fossil fuels are 2.3.3. Water
adding Pb and Cd in the environment locally and globally. These Water sample 250 ml was filtered through Whattmann filter
metals do not have any positive or known use for living biota par- paper. Filter paper was digested in HCl and HNO3 (1:5). The mix-
ticularly the fauna (Kenntner et al., 2003). In the trace metals ture was heated until transparent solution obtained. Solution
shows Cd is considered the utmost toxic metal while Pb is lethal was again filtered after cooling by using Whattmann filter paper.
to birds (Battaglia et al., 2003). In birds’ physique state is also influ-
enced by Zinc (Kim et al., 2009). After soaking up these metals can 2.3.4. Filtration
flow around bird’s physique and later it assembles in eggs and Distilled water was used to add in all samples when the diges-
excrete (Burger, 2002). tion was completed; all samples filtered through filter papers and
The Pollution problem of heavy metals has increased in in filtrates were collected in round bottom flask of capacity (50 ml)
recent decade in the South Asia (Hordoy et al.,1992 In states like and kept at 4°c till further analysis.
Costa Rica and Florida certain studies have been conducted which
showed ecotoxicology effects in the nesting birds. (Burger
2.4. Laboratory analysis
et al.,1993). Regular and long-term research is needed to unveil
the problem of accumulation of heavy metals in the aquatic as well
Flame Atomic Absorption Spectrophotometer (FAAS) was used
as terrestrial organisms. It is mandatory to understand that how
for the deduction of heavy metals. The results were obtained sub-
these toxic contaminants bioaccumulate and bio-transform in dif-
sequently while placing the standard dilutions in FAAS.
ferent species of birds.

2.5. Statistical analysis

2. Methodology
Basic descriptive statistics, Hierarchical agglomerative cluster
2.1. Study area analysis (HACA) are the statistical analysis of data. For the identifi-
cation of sources of heavy metal contamination of egret species
This study was conducted in Mirpur which is a district of the feeding habitats, Ward’s linkage method and Pearson distance
state of Azad Jammu and Kashmir (AJK), Pakistan 33°8‘ 350 ’ North, matrix was used in cluster analysis.
73° 44‘ 510 ’ East. It is adjoining area of northern Districts Jhelum
and Rawalpindi of Punjab Province of Pakistan. Its elevation from
3. Results
sea level is 459 m and possess a mega water body namely Mangle
Dam which holds about 100sq Km area.
All samples associated with little egret have shown that there
are seven heavy metals namely Mn, Zn, Ni, Cu, Cd, Pb and Co metals
2.2. Sampling were present with different concentrations. Three metals Pb, Co
and Cd are toxic non-essential whenever present in any sample.
Samples were collected from two colonies of little egret from The rest of metals like Mn, Zn, Ni and Cu are essential elements
Jabbi area of District Mirpur AJK, two colonies were selected which and useful in metabolic activity of the bird but these essential
along Jabbi stream and were just opposite to each other. Prelimi- heavy metals become toxic or lethal for human and birds when
nary survey was conducted in March 2015 to finalize the sampling found beyond the permissible limits.
procedure, but sapling was done during the mints of April-June Two sites were selected for sample collection from the study
2015. The collected samples were comprises of eggs, egg shells, area. The samples used for the detection of metals were; egg con-
liver, blood, chest, thigh, excreta, water, soil and food of egrets like tent, egg shell, food samples (fish, insect), meat samples (liver,
(insects, fish) chest and thigh), blood sample, excreta sample, water samples, soil
sediments. The concentrations of metals were different in samples
2.3. Digestion from two sites and the concentration of heavy metals in site one is
given in the Fig. 2.
2.3.1. Eggs and egg shells
In the beginning with help of spatula eggs were broken down
and white of eggs and Yellow of eggs were transferred to the respec-
tive label bottles, which were centrifuged at 2200 rpm for one min-
ute. Then 1 ml of white of egg and yellow of eggs was transferred to
a glass flask having volume 200 ml and Nitric Acid (HNO3) 5 ml was
added, and flask stirred for 2 min. After this Perchloric acid (HCLO4)
1 ml was added to flask and again stirred for 2 min.
Egg samples were heated in order to dry the added acid the
temperature of hot plat was gradually increased (50°c-250°c.) until
the acids are completely dried out. A white colour material was
obtained. The rest of the samples were also treated with the same
method for digestion.

2.3.2. Sediments
Sediment samples 1 gm were taken in a tube, added Aquaregia
(HCL, HNO3) in 3:1 ratio 15 ml and left for overnight simply. After
this samples were heated at 150°c and then added 5 ml HCLO4 was Fig. 1. Map of the study Area (source: pakimage.com).

2
M. Rani, R. Ullah, Mona S Alwahibi et al. Saudi Journal of Biological Sciences xxx (xxxx) xxx

Conc. of Heavy Metals In Diff. Samples

Conc.

Fig. 2. Graphical presentation of heavy metals in different samples at site 1.

The mean concentration of heavy metals in egg content sample respectively. The concentration of heavy metals in food samples
collected from little egret of site 1 was in order, (Fish and Insects) at site 2 was different from the previous one with
Zn > Pb > Ni > Cu > Co > Mn > Cd with the mean concentration the following order, Zn > Mn > Ni > Pb > Cu > Co > Cd with the mean
of 2.8418, 0.6407, 0.6325, 0.4641, 0. 4485, 0.4285 and 0.715 concentration of 7.2166, 6.7769, 2.0984, 1.8035, 1.7529, 1.0204
respectively. The concentration of heavy metals in egg shell sam- and 0.3637 respectively. Whereas the mean concentration of heavy
ples of site 1 collected from little egret was little bit different from metals in Meat samples (Liver, Chest and Thigh) at site 2 was in the
the concentration of heavy metals in egg content by following the following order, Zn > Ni > Co > Cu > Mn > Pb > Cd with the mean
order, Zn > Pb > Co > Mn > Cu > Ni > Cd with the mean concentra- concentration of 5.2003, 2.9812, 2.7309, 2.6373, 2.5355. 2.3489
tion of 1.7825, 0.7042, 0.5447, 0.5051, 0.3198, 0.712 and 0.0748 and 2.335respectively. The order of heavy metals in blood samples
respectively. The concentration of heavy metals in food samples was Zn > Cd > Mn > Ni > Co > Pb > Cu with the mean concentration
(Fish and Insects) was different from the previous one with the fol- of 1.1308, 1.186, 1.0569, 0.8267, 0.6987, 0.4372, and 0.3433
lowing order, Zn > Mn > Ni > Cu > Pb > Co > Cd with the mean con- respectively. The concentration of heavy metals in the excreta
centration of 6.8106, 4.1908, 1.7033, 1.4761, 1.1925, 1.1231 and samples of site 2 was similar to some extent with the following
0.1518 respectively. Whereas the mean concentration of heavy order, Mn > Zn > Cu > Ni > Pb > Cd > Co with the mean concentra-
metals in Meat samples (Liver, Chest and Thigh) was in the follow- tion of 6.3071, 1.4035, 1.2439, 1.1571, 0.7956, 0.6096 and 0.805
ing order, Zn > Cu > Mn > Co > Ni > Pb > Cd with the mean concen- respectively. The mean concentration of heavy metals in the water
tration of 5.8229, 2.782, 2.1581, 1.980, 1.7988, 1.6982 and 1.3136 samples was in the following order Ni > Mn > Co > Pb > Cu > Cd > Zn
respectively. The order of heavy metals in blood samples was with the mean concentration of 0.5974, 0.4408, 0.4242, 0.3748,
Ni > Zn > Co > Mn > Cu > PB > Cd with the mean concentration 0.2269, 0.0692, and 0.476 respectively whereas the mean concen-
of 0.8875, 0.8247, 0.7865, 0.3469, 0.3185, 0.322 and 0.0768 respec- tration of heavy metals in soil sediments was in the following order
tively. The concentration of heavy metals in the excreta samples of Mn > Ni > Zn > Cu > Pb > Co > Cd with the mean concentration of
site 1 was similar to some extent with the following order, 10.6005, 3.8185, 1.6163 1.1961, 1.17, 0.9522, and 0.5998
Mn > Zn > Cu > Cd > Ni > Pb > Cd and Co with the mean concentra- respectively.
tion of 12.1389, 2.7158, 1.5172, 1.2583, 1.0839, 0.8195 and 0.6823
respectively. The mean concentration of heavy metals in the water
3.1. Statistical analysis in hierarchical dendrogram of metals
samples was in the following order Ni > Pb > Mn > Co > Cu > Zn > Cd
with the mean concentration of 0.9323, 0.6353, 0.6325, 0.5797,
Basic descriptive statistics, Hierarchical agglomerative cluster
0.3475, 0.1432 and 0.087 respectively whereas the mean concen-
analysis (HACA) for analysis of data. Ward’s linkage method and
tration of heavy metals in soil sediments was in the following order
Pearson distance matrix was used in cluster analysis (SI Figs. 1-8).
Mn > Ni > Zn > Cu > Pb > Co > Cd with the mean concentration of
22.1174, 2.5486, 2.832, 1.2071, 0.9842, 0.8593 and 0.0784
respectively. 4. Discussion
The concentrations of metals were different in samples from
two sites and the concentration of heavy metals in site one is given Results showed that there was slight difference among the two
in the Fig. 3. The mean concentration of heavy metals in egg con- colonies of little egrets the heavy metals like Co, Cu, Cd, Ni, Zn, and
tent sample collected from little egret of site 2 was in order, Pb. This non-significant variation can be associated to various for-
Zn > Ni > Pb > Co > Mn > Cu > Cd with the mean concentration aging environment. The accumulation of heavy metals in birds
of 1.7045, 0.4487, 0.4452, 0.3545, 0.3052, 0.2751, and 0.0488 depends upon pattern of diets being taken, body size, condition
respectively. The concentration of heavy metals in egg shell sam- of body of bird etc. (Kojadinovic et al., 2007). Another reason for
ples of site 2 collected from little egret was little bit different from concentrations variations is egg laying time of the bird, metabolic
the concentration of heavy metals in egg content by following the differences, mechanisms of detoxification of an enzyme etc.
order, Zn > Ni > Pb > Mn > Cu > Co > Cd with the mean concentra- From both colonies of Jattali headworks Head the mean concen-
tion of 1.135, 0.5219, 0.4359, 0.3676, 0.3187, 0.357 and 0.0657 tration was calculated 0.682 ± 0.956. This concentration was com-
3
M. Rani, R. Ullah, Mona S Alwahibi et al. Saudi Journal of Biological Sciences xxx (xxxx) xxx

Conc. of Heavy Metals In Diff. Samples

Conc.

Fig. 3. Graphical presentation of heavy metals in different samples at site 1.

pared with common Eider Glaucous-winged Gull (0.30 mg/g) from study was calculate (3.189 ± 0.917) higher than (202.57 ± 1.65 m
Alaska (Burger and Goch Feld 2007). The concentration of Cd in g/g) faeces of vulture bird investigated by Bravo et al., (2005).
present study (0.980 ± 0.544) was calculated below the uncertain The variation among different bird species is due to differences
threshold effect stage. The Cd concentration (1.163 ± 0.707 mg/g) in bioavailability and diet (Adendorff. 1993).
in prey sample of little egret when compared with Black tailed god- During current investigation the concentration (0.648 ± 0.372)
wit (4.27, 3.07 mg/g) found lower (Roodbergen et al., 2008.) Similar of Cd found lower than the concentration found in fecal samples
Cd results were also compared with Black crowned night and Grey of vulture bird from Venezuala state (13.93 ± 1.18 ppm) by
heron (174 and 172 mg/g) from Pyeongtaek, China (Kim and koo., (Bravo et al., 2005). Although Cd is considered the most hazardous
2008) and results of this study were also found lower. heavy metal present in both environment and food with longer
In present study the Pb concentration in the contents of eggs of lit- persistence (Lee et al., 1994). The heavy metal Mn have a vital role
tle egrets was calculated (1.633 ± 0.315) while Bostan et al., (2007) with birds excretion its exposure to avian embryos has teratogenic
reported higher concentrations Pb (6.74 mg/g) and (73.50 mg/g) in impacts (Hashmi et al., 2013). Bravo et al., (2005) calculated the
Cattle egret respectively. A similar study was conducted from highest concentration of Ni (15.19 ± 1.33 mg/g), while in current
Alaska Burger and Goch Feld (2007) and they also reported higher study the concentration of Ni was (1.205 ± 0.373), Higher concen-
concentration of Pb. The Pb concentration in liver of little egret Pb tration can damage the respiratory system, deoxyribonucleic acid
(0.606 ± 0.141) was recoded lower as compared to (<10 mg/g wet (DNA) of the bird (Vanwyk et al., 2001).
weight) Muhammad Shahbaz et al., (2013) With in the same study are two little egret species from two dif-
In current study the mean concentration of Pb in soil samples ferent sites showed non-significant difference among the assessed
were calculated (2.135 ± 0.403) which was much lower (9.60 – metals like Mn, Co, Cd, Cu, Pb, Ni and Zn. Samples like egg contents,
29.40 mg/g) calculated by Shahbaz et al., (2013). egg shell, meat, Food, excreta, blood, water and sediments also
Similarly, the Mean concentration of Ni was calculated (2.093 have slight variations among the concentrations levels may be
± 0.811) in present study was higher than (0.50 – 0.76 mg/g dry because of foraged in different habitats before their breeding.
weight) reported by Shahbaz et al., (2013). In prey samples The Heavy metals are being incorporated in the food chain through
Ni concentration was calculated (2.251 ± 0.42) that was found pollutions caused by anthropogenic and some natural activities
higher (1.77 mg/g) when compared with a study conducted by and most effected arears of world are from developing countries
(Rood Bergen et al., 2008) for Black tailed godwit. Boston et al., like Pakistan, India, Bangladesh and Nepal (Karn and Harada.,
(2007) also conducted a study on cattel egert from Pakistan and 2001).
found higher concentration of Ni (24.80 mg/g).
In case of Co the results of current study showed higher concen-
tration of Co(1.639 ± 0.351) than a study conducted by Shahbaz 5. Conclusion and recommendations
et al., (2013) and calculated (3.79 mg/g) concentration of Co. The
concentration of Mn in egg contents of little egret was calculated The results of current study depicted that all samples from
(1.022 ± 0.255), which was lower than a separate study (0.51–3.5 study area associated with little egrets were contaminated with
5 mg/g) conducted by Shahbaz et al., (2013). heavy metals. There was no significant difference among the heavy
Zn concentration in a balance state contributes for metabolism metals concentrations of both sites (birds colonies) of study area.
but its exertive or beyond the limit concentration become toxic for From the studied metals the maximum concentration Mn was cal-
the birds. The mean concentration of Zn was calculated (4.928 ± 0. culated and the order of accumulation of heavy metals on the basis
418) in recent study, this concentration is much lower when com- of concentration in the study area was sediments > meat
pared with the study conducted by Shahbaz et al., (2013) on Islam samples > food > excreta > blood > egg
headwork and Trimu headwork’s Heronries of little egrets (52.35 – content > eggshell > water samples. The higher concentration in
58.21 mg/g. In current study the concentration of Cu in the egg con- of sediments study area is might be due to anthropogenic activities
tent was found higher (1.019 ± 0.334) when compared with a study which are of environmental concern. The bird little egret is consid-
conducted by Braune and Nobel (2009). They suggest that in most ered largely scattered species and elevated on food chain. This
of the living organisms heavy metal concentration usually lesser study shoes that such birds can be a wonderful tool for examining
(1 ppm-2.00 mg/g). The concentration of Zn in faeces in present the environmental toxicants. It is also concluded that this bio can
4
M. Rani, R. Ullah, Mona S Alwahibi et al. Saudi Journal of Biological Sciences xxx (xxxx) xxx

be used as useful bioindicator for the assessment of organic and Burger, J., Gochfeld, M., 2007. Metals and radionuclides in birds and eggs from
Amchitka and Kiska Islands in the Bering Sea/Pacific Ocean ecosystem. Environ.
inorganic pollutants. Further comprehensive investigations and
Monit. Assess. 127 (1-3), 105–117.
research should be performed to explain the destiny and ecotoxi- Braune, B.M., Noble, D.G., 2009. Environmental contaminants in Canadian
cological after-effects of heavy metals in avian species. Such inves- shorebirds. Environ. Monit. Assess. 148 (1-4), 185–204.
tigation can portray the actual understandings of heavy metals and Bravo, A., Colina, M., Azuero, S., Salas, R., 2005. Heavy metal levels in plasma and
fecal material samples of the Black vulture (Coragyps atratus). Revista Científica
other pollutants, which could enable investigators to comprehend 15, 319–325.
that how toxic contaminants move across the food chain. The tem- Bostan, N., Ashraf, M., Mumtaz, A.S., Ahmad, I., 2007. Diagnosis of heavy metal
poral and continuous monitoring is also required for in the study contamination in agro-ecology of Gujranwala, Pakistan using cattle egret
(Bubulcus Ibis) as bio indicator. Ecotoxicology 16 (2), 247–251.
area. Dauwe, T., Janssens, E., Bervoets, L., Blust, R., Eens, M., 2005. Heavy-metal
concentrations in female laying great tits (Parus major) and their clutches.
Declaration of Competing Interest Arch. Environ. Contam. Toxicol. 49 (2), 249–256.
Hashmi, M.Z., Malik, R.N., Shahbaz, M., 2013. Heavy metals in eggshells of cattle
egret (Bubulcus ibis) and little egret (Egretta garzetta) from the Punjab
The authors declare that they have no known competing finan- province, Pakistan. Ecotoxicol. Environ. Saf. 89, 158–165.
cial interests or personal relationships that could have appeared Hordoy, G.E. The Urban Child in the Third World: Urbanization Trends and Some
Principle Issues. Innocent Occasional Papers, the Urban Child Series, (4) (1992).
to influence the work reported in this paper. Hancock, J., Kushlan, J.A., 2010. The herons handbook. A&C Black.
Koivula, M.J., Eeva, T., 2010. Metal-related oxidative stress in birds. Environ. Pollut.
Acknowledgement 158 (7), 2359–2370.
Kenntner, N., Krone, O., Altenkamp, R., Tataruch, F., 2003. Environmental
contaminants in liver and kidney of free-ranging northern goshawks
The authors extend their appreciation to the Researchers sup- (Accipiter gentilis) from three regions of Germany. Arch. Environ. Contam.
porting project number (RSP-2021/173), King Saud University, Toxicol. 45 (1), 128–135.
Riyadh, Saudi Arabia. Kim, J., Lee, H.-S., Koo, T.-H., 2009. Heavy metal concentrations in three shorebird
species from Okgu Mudflat, Gunsan. Korea. Ecotoxicology 18 (1), 61–68.
Kojadinovic, J., Le Corre, M., Cosson, R.P., Bustamante, P., 2007. Trace elements in
Appendix A three marine Birds breeding On Reunion Island (western Indian Ocean): Part 1—
Factors influencing their Bioaccumulation. Arch. Environ. Contamination
Toxicol. 52 (3), 418–443.
https://doi.org/10.1016/j.sjbs.2021.08.106 Kim, J., Koo, T.-H., 2008. Heavy metal concentrations in feathers of Korean
shorebirds. Arch. Environ. Contam. Toxicol. 55 (1), 122–128.
KARN, S.K., Harada, H., 2001. Surface water pollution in three urban territories of
Nepal, India, and Bangladesh. Environ. Manage. 28 (4), 483–496.
Lam, J.C., Tanabe, S., Lam, M.H., Lam, P.K., 2005. Risk to breeding success of water
References birds by contaminants in Hong Kong: evidence from trace elements in eggs.
Environ. Pollut. 135 (3), 481–490.
Ayasß, Z., 2007. Trace element residues in eggshells of grey heron (Ardea cinerea) and Lee, J., Grace, N.D., Rounce, J.R. Cadmium accumulation in liver and kidney of sheep
black-crowned night heron (Nycticorax Nycticorax) from Nallihan Bird grazing Ryegrass/white clover pastures. In: proceeding- NEW ZEALAND society
Paradise, Ankara Turkey. Ecotoxicology 16 (4), 347–352. of animal production, Vol. 54, pp. 31-31, (1994).
Adendorff, R., 1993. Code switching amongst Zulu-speaking teachers and their Malik, R.N., Zeb, N., 2009. Assessment of environmental contamination using
pupils: its functions and implications for teacher education. Language feathers of Bubulcus ibis L., as a bio monitor of heavy metal pollution, Pakistan.
Education 7 (3), 141–162. Ecotoxicology 18 (5), 522–536.
Burger, J., Gochfeld, M., 2000a. Metal levels in feathers of 12 species of seabirds from Muhammad Shahbaz a, Muhammad Zaffar Hashmi b, Riffat Naseem Malik a, Azra
Midway Atoll in the Northern Pacific Ocean. Sci. Total Environ. 257 (1), 37–52. Yasmin Environmental Biology and Ecotoxicology Laboratory, Department of
Burger, J., 2002. Food chain differences affect heavy metals in bird eggs in Barnegat Environmental Sciences, Faculty of Biological Sciences, Quaid-i-Azam
Bay, New Jersey. Environ. Res. 90 (1), 33–39. University, Islamabad, Pakistan the Mall, Rawalpindi, Pakistan (2013).
Burger, J., 1993. Metals in avian feathers: Bio indicators of environmental pollution. Roodbergen, M., Klok, C., van der Hout, A., 2008. Transfer of heavy metals in the food
Rev. Environ. Toxicol. 5, 203–311. chain earthworm Black-tailed godwit (Limosa limosa): comparison of a
Burger, J., Gochfeld, M., 2000b. Metal levels in feathers of 12 species of seabirds polluted and a reference site in The Netherlands. Sci. Total Environ. 406 (3),
from Midway Atoll in the Northern Pacific Ocean. Sci. Total Environ. 257 (1), 407–412.
37–52. Van Wyk, E., Van der Bank, F.H., Verdoorn, G.H., Hofmann, D., 2001. Selected mineral
Bhatt, C.J., Arora, J., Shah, M.S., 2003. Role of color Doppler in pregnancy induced and heavy metal Concentrations in blood and tissues of vultures in different
hypertension (a study of 100 cases). Indian J. Radiol. Imaging 13 (4), 417. regions of South Africa. South African J. Animal Sci. 31 (2), 57–64.