ArticlePDF Available

Biomonitoring of heavy metals (Cd, Hg, and Pb) and metalloid (As) with the Portuguese common buzzard (Buteo buteo)


Abstract and Figures

The accumulation of heavy metals in the environment may have a wide range of health effects on animals and humans. Thus, in this study, the concentrations of arsenic (As), cadmium (Cd), lead (Pb), and mercury (Hg) in the blood and tissues (liver and kidney) of Portuguese common buzzards (Buteo buteo) were determined by inductively coupled plasma-mass spectrometer (ICP-MS) in order to monitor environmental pollution to these elements. In general, Hg and As were the elements which appeared in the highest and lowest concentrations, respectively. A highest percentage of non-detected concentration was found for blood Cd (94.6 %) but, in turn, it was the only metal that was detected in all kidney samples. The kidney was the analyzed sample which showed the highest concentrations of each element evaluated. Statistically, significant differences among blood, liver, and kidney samples were observed for As and Cd (P < 0.05). Cd concentrations in kidney and liver varied significantly with age: Adults showed higher hepatic and renal Cd concentrations than juveniles. Blood Pb concentration seems to show an association with the hunting season. Although raptors are at the top of the food chain and are thus potentially exposed to any biomagnification processes that may occur in a food web, the individuals evaluated in this study generally had low levels of heavy metals in blood and tissues. However, chronic exposure to these metals was verified. The results presented here lend weight to arguments in favor of continuous biomonitoring of metals and metalloids, since heavy metals may accumulate to levels that will pose a risk to both human health and the environment.
Content may be subject to copyright.
Biomonitoring of heavy metals (Cd, Hg, and Pb) and metalloid
(As) with the Portuguese common buzzard (Buteo buteo)
Manuela Carneiro &Bruno Colaço &Ricardo Brandão &
Carla Ferreira &Nuno Santos &Vanessa Soeiro &Aura Colaço &
Maria João Pires &Paula A. Oliveira &Santiago Lavín
Received: 21 November 2013 /Accepted: 30 June 2014
#Springer International Publishing Switzerland 2014
Abstract The accumulation of heavy metals in the
environment may have a wide range of health effects
on animals and humans. Thus, in this study, the concen-
trations of arsenic (As), cadmium (Cd), lead (Pb), and
mercury (Hg) in the blood and tissues (liver and kidney)
of Portuguese common buzzards (Buteo buteo)were
determined by inductively coupled plasma-mass spec-
trometer (ICP-MS) in order to monitor environmental
pollution to these elements. In general, Hg and As were
the elements which appeared in the highest and lowest
concentrations, respectively. A highest percentage of
non-detected concentration was found for blood Cd
(94.6 %) but, in turn, it was the only metal that was
detected in all kidney samples. The kidney was the
analyzed sample which showed the highest concentra-
tions of each element evaluated. Statistically, significant
differences among blood, liver, and kidney samples
were observed for As and Cd (P<0.05). Cd concentra-
tions in kidney and liver varied significantly with age:
Adults showed higher hepatic and renal Cd concentra-
tions than juveniles. Blood Pb concentration seems to
show an association with the hunting season. Although
raptors are at the top of the food chain and are thus
potentially exposed to any biomagnification processes
Environ Monit Assess
DOI 10.1007/s10661-014-3906-3
M. Carneiro :A. Colaço
Animal and Veterinary Research Centre (CECAV), University
of Trás-os-Montes and Alto Douro, 5000-801 Vila Real,
B. Colaço
Department of Zootechnics, ECAV, University of
Trás-os-Montes e Alto Douro, Quinta dos Prados,
5000-801 Vila Real, Portugal
B. Colaço :M. J. Pires :P. A . O l i v e i r a
Centre for the Research and Technology of
Agro-Environmental and Biological Sciences, University of
Trás-os-Montes e Alto Douro, Quinta dos Prados,
5000-801 Vila Real, Portugal
R. Brandão
Ecology, Monitoring and Recovery Center of Wild Animals
(CERVAS), 6290-909 Gouveia, Portugal
C. Ferreira
Research and Recovery Center of Wild Animals of the Ria
Formosa Natural Park (RIAS), 8700 Olhão, Portugal
N. Santos
Wildlife Rehabilitation Center of the Peneda-Gerês National
Park, 4704-538 Braga, Portugal
V. S o e i ro
Wildlife Rehabilitation Center of the Gaia Biological Park,
4430-757 Avintes, Portugal
A. Colaço :M. J. Pires :P. A. Oliveira (*)
Department of Veterinary Sciences, ECAV, University of
Trás-os-Montes e Alto Douro, Quinta dos Prados,
5000-801 Vila Real, Portugal
S. Lavín
Servei dEcopatologia de Fauna Salvatge (SEFaS),
Department of Medicine and Animal Surgery, Autonomous
University of Barcelona, 08193 Bellaterra, Spain
that may occur in a food web, the individuals evaluated
in this study generally had low levels of heavy
metals in blood and tissues. However, chronic
exposure to these metals was verified. The results
presented here lend weight to arguments in favor
of continuous biomonitoring of metals and metal-
loids, since heavy metals may accumulate to levels
that will pose a risk to both human health and the
Keywords Buteo buteo .Common buzzard .Heavy
metals .Metalloid .Raptors .Portugal
Trace elements are present in the environment through
the geological cycle and various anthropogenic activi-
ties, with the latter the most relevant (Licata et al. 2010;
Naccari et al. 2009). These elements can easily enter the
food chain, and at high doses they can be acutely lethal,
while at lower doses they may have a wide range of
health effectssuch as mutagenicity, carcinogenici-
ty, teratogenicity, inmunosuppression, poor body
condition, and impaired reproduction in humans and
animals (Florea and Busselberg 2006; Scheuhammer
1987). All of which make them a serious threat to the
stability of ecosystems and living organisms (Battaglia
et al. 2005; López-Alonso et al. 2007; Naccari et al.
Levels of trace elements and their effects on organ-
isms are influenced by numerous factors related to hab-
itat, physiology, and life history (Peakall and Burger
2003). Exposure to nonessential elements generally is
below levels thought to be acutely toxic (Henny et al.
1995; Stout and Trust 2002; Wayland et al. 2001b).
Although acute toxicity is unlikely to occur, chronic
exposure to nonessential elements may interact with
other environmental stressors namely parasitic infec-
tions or other pathogens and this could compromise
birds survival and reproduction (Wayland et al.
2008). It should be appreciated that potentially sub-
lethal effects caused by chronic exposure to envi-
ronmental contaminants are largely unknown in wild
birds (Shlosberg et al. 2011).
Biomonitoring of trace elements in the environment
has enabled the identification of many sources of pol-
lutants. Typically, the bioavailability of environmental
pollutants is assessed by measuring chemical residues in
tissues or fluids taken from animals living in specific
habitats (López-Alonso et al. 2007). The direct measure-
ment of contaminants in blood and internal tissues is the
best indicator of the degree and type of exposure to them
(García-Fernández et al. 1997), presenting blood the
advantage of being easily accessible, sampling can be
relatively harmless, and it is in contact with all tissues
where chemicals are deposited and stored (Esteban and
Castano 2009). Some species have biological habits that
increase the likelihood of exposure to contaminants and
can produce relevant information that would be missed
if only the areas water or soil were analyzed (Battaglia
et al. 2005). However, assessing an ecosystemshealth
adequately by means of biomonitoring requires the
selection of species that are representative. Territorial
birds of prey, ones that are non-migratory and have
long life spans, are likely to reflect chemical contam-
ination within their extended home ranges (Pérez-
López et al. 2008). These localised, upper-trophic
level species are also believed to be especially vul-
nerable to metals and play a very important role as
environmental-contamination indicators (Stout and
Trust 2002; Wayland et al. 1999).
The common buzzard (Buteo buteo), a diurnal bird of
prey belonging to the order Accipitriformes and to the
family Accipitridae, was the sentinel species selected for
this study for several reasons: it is abundant within
Portuguese territory and the Portuguese population of
these birds is essentially resident, though in autumn and
winter a comparatively small number of common buz-
zards from northern Europe do reach the Iberian Penin-
sula. What is more, these birds are very territorial, are
present in different habitats (forests, agricultural zones,
mountain regions, and sub-urban areas), they feed on a
wide range of prey, and are very opportunistic hunters
(Catry et al. 2010).
The present study was carried out in order to evaluate
the degree and type of exposure to trace elements that
the Portuguese common buzzards may be exposed and
to monitor environmental pollution. For this purpose,
we determine the arsenic (As), cadmium (Cd), lead (Pb),
and mercury (Hg) concentrations in whole blood,
liver, and kidney samples taken from common buz-
zards from different areas of Portugal. Also, differ-
ences between their areas of origin and the influence
of age and gender on toxic-metal concentrations
were studied. The influence of the season the sam-
ples were taken in, on blood-metal concentrations,
was also investigated.
Environ Monit Assess
Material and methods
Sample collection
All samples collected from common buzzards came
from five Portuguese wildlife rehabilitation centers
(Centro de Ecologia,Recuperação e Vigilância de
Animais Selvagens (CERVAS); Centro de Recuperação
de Animais Selvagens do Parque Nacional da Peneda
do Gerês;Centro de Recuperação de Animais Selvagens
do Parque Biológico de Gaia;Centro de Recuperação e
Investigação de Animais Selvagens da Ria Formosa
(RIAS); and Centro de Estudos e Recuperação de
Animais Selvagens de Castelo Branco (CERAS)) be-
tween November 2007 and January 2012.
Collected animals were either found dead or brought
to the centers alive but injured or debilitated due to
several potential reasons. These reasons were as fol-
lows: collision with a vehicle (n=18), collision with
power lines (n=17), lead shot (n=22), fall from nest
(n=14), malnutrition (n=3), and injury of unknown
origin (n=51). The following data were registered for
each bird: date of arrival at the center, area of origin,
reason for being brought in, gender (male, female, or
unknown), and age (juvenile, adult, or unknown). The
birdsorigin was divided into two different Portuguese
regions: littoral (urban and industrial areas) and up-
country (rural and natural areas).
From a total of 125 common buzzards, blood (n=93),
liver (n=56), and kidney (n=36) samples were collect-
ed. The number of samples collected across different
years, seasons, regions, and for different gender and age
classes were listed in Table 1. Blood samples were
collected via the brachial vein at the moment of arrival
to the rehabilitation center and immediately transferred
into collection tubes without the use of an anticoagulant.
Liver and kidney samples were collected from animals
that were found dead, died of natural causes, or were
sacrificed when their state of health indicated a potential
recovery was unlikely. Liver and kidney samples were
placed individually in plastic bags. In this study, only
samples from animals that died in the rehabilitation
center within the first month after admission were in-
cluded. All samples were stored at 20ºC until analysis.
Analytical procedure
Sample analysis was performed in the laboratories of the
Scientific-Technical Services of the University of
Barcelona (SCT-UB), Spain. Liver and kidney sub-
samples [250350 mg wet weight (w.w.)] were digested
in Teflon reactors with 3 ml of 65 % concentrated nitric
acid (HNO
) and 2 ml of 30 % hydrogen peroxide
) at 90ºC in an oven and left overnight. According
to the volume of blood contained in the tubes, different
amounts of HNO
and H
were used until the diges-
tion of blood samples was complete. After digestion,
each liver and kidney sample was brought up to a
volume of 40 ml with milli-Q water and according to
the blood volume to be analyzed, blood samples were
brought up to a volume of 20, 30, or 40 ml with milli-Q
water. All samples were transferred to the measuring
vessel and then analyzed for As, Cd, Hg, and Pb in an
inductively coupled plasma-mass spectrometer (ICP-
MS) (Perkin Elmer Model Elan 6000, Perkin Elmer,
Waltham, USA). All material used in the digestion
process was thoroughly acid-rinsed. A second set of
identical liver and kidney samples (12 g) was oven-
dried at 60ºC until reaching a constant weight in order to
calculate the percentage of humidity in each sample,
which enabled the transformation of wet-weight results
into dry-weight (d.w.) values (Ribeiro et al. 2009).
Tabl e 1 Data relating to common buzzards (Buteo buteo)ofthis
Year 2007 5 0 0
2008 8 6 0
2009 24 19 5
2010 33 24 24
2011 22 7 7
2012 1 0 0
Season Spring 15 11 6
Autumn 34 17 15
Winter 17 13 8
Origin Littoral 47 28 24
Up-country 46 28 12
Age Adult 30 19 16
Juvenile 44 24 9
Male 35 26 19
Environ Monit Assess
An analytical quality-control program was applied
throughout the study, according to López-Alonso et al.
(2007). Blank absorbance values were monitored
throughout the survey and were subtracted from the
readings before the results were calculated. The limits
of detection (LOD) in the acid digest (set at three times
the standard deviation of the reagent blanks) were in all
cases <0.5 μg/l, and the limits of quantification (LOQ),
expressed as a concentration in the blood and tissue,
were calculated on the basis of the mean sample weight
and volume analyzed. Analytical recoveries were deter-
mined from the certified standard reference materials
(Whole-blood Seronorm, Trace Element, Whole Blood
2 ref. 201605, and Whole Blood 3 ref. 102405 from
SERO AS, Norway and Bovine Liver-1577b from Na-
tional Institute of Standards and Technology, Gaithers-
burg, USA) analyzed together with the samples. The
range of recovery rates (in view of the concentrations in
the reference material) ranged between 93.67 % for
hepatic Pb and 138.43 % for blood As.
Data analysis
Statistical analyses were performed with IBM SPSS
Statistics for Windows, V.19.0.
A statistical significance level of P<0.05 was used
for null hypothesis rejection.
Each sample below the LOQ was assigned a value of
one-half the LOQ and included in the data set for statis-
tical treatment, a technique which minimizes nominal
type I error rates (Clarke 1998).
Normal-distribution assumption was checked
using the KolmogorovSmirnov test. When normal
distribution assumption was violated, the data sets
were log-transformed before analysis and checked
with the KolmogorovSmirnov test. However, most
of the variables did not follow normal distribution
even after transformation, so a non-parametric ap-
proach to the data analysis was necessary. The
MannWhitney Utest was used to test the statistical
significance for area of origin, age, and gender in
the blood and tissues concentrations. Birds with
unknown age and gender were not included in the
statistical analysis when testing the significance for
these variables. Comparisons across the different
seasons in terms of blood concentrations and differences
between metal concentrations in the blood, liver, and
kidney samples were tested using the KruskalWallis test
followed by the Dunns post-hoc test. A non-parametric
Spearman`s test was applied to test the correlation be-
tween blood and tissues and between tissue concentra-
tions for each analyzed metal.
Heavy metals and metalloid concentrations found in the
blood, liver, and kidney of common buzzards are listed
in Table 2.
Concerning As concentrations, blood As was not
detected in 30.1 % of total samples, in the liver and
kidney samples it was not detected in 37.5 % and
19.4 %, respectively (Table 2). Mean As concentrations
were significantly statistically different between ani-
malsblood, liver, and kidney (P<0.01): the lowest
mean concentration was found in blood (0.014±
0.014 μg/g w.w) and the highest in the kidney (0.041±
0.026 μg/g w.w.) (Table 2and Fig. 1). As concentrations
in kidney samples varied significantly with age and
gender: Adults showed higher (P<0.05) renal-As con-
centrations than juveniles and females showed renal-As
concentrations that were nearly twice as high as average
concentrations in males (P<0.05). No significant influ-
ence from any factor was detected in blood- and hepatic-
As concentrations (Table 3).
When considering Cd results, this was not detected in
94.6 % of total blood samples, and for that reason, the
influence of age, gender, origin, and season on concen-
trations of this metal in blood was not studied. In con-
trast, Cd was detected in 96.4 % of liver samples and in
all the kidney samples (Table 2). Mean Cd concentra-
tions were significantly (nearly four times) higher
(P<0.05) in the kidney (0.373±0.381 μg/g w.w.) than
in the liver (0.089±0.097 μg/g w.w.) (Fig. 1). Cd con-
centrations in tissues varied significantly with age:
Adults showed higher hepatic- (twice as high, P<0.01)
and renal- (three times as high, P<0.05) Cd concentra-
tions than juveniles. No significant influence of origin
and gender in hepatic and renal levels were detected for
Cd accumulation (Table 3).
In this study, Pb was detected in most of the samples:
97.8 % (blood), 87.5 % (liver), and 94.4 % (kidney)
(Table 2). Mean Pb concentrations were very similar
between blood (0.142±0.628 μg/g w.w.) and liver
(0.152± 0.194 μg/g w.w.). In the kidney, the highest
mean Pb concentration (0.245±0.364 μg/g w.w.) was
found, but this difference was not statistically significant
(Fig. 1). Blood Pb was significantly affected by age
Environ Monit Assess
(P<0.01), adults had higher concentrations than juve-
niles, and by season (P<0.01), blood samples collected
in autumn had higher Pb concentrations than those
collected in spring and summer. Hepatic and renal Pb
concentrations were not significantly affected by age,
gender, and origin (Table 3).
Turning to Hg results, this metal was also detected in
most of the samples: 88.2 % (blood), 94.6 % (liver), and
97.2 % (kidney) (Table 2). Blood Hg concentrations
were significantly lower than hepatic and renal Hg
(P<0.001). Hg accumulation was mainly in the kidney,
although there is no significant difference between he-
patic and renal concentrations (Fig. 1). Blood Hg con-
centrations were significantly higher (P<0.01) in adults
than in juveniles. The season the samples were taken in
also had significant effects on blood Hg concentrations
(P<0.001): Higher levels were found in autumn and
winter than in spring and summer, but significant dif-
ferences were only verified between autumn and spring
and autumn and summer. Hepatic and renal Hg was not
significantly affected by any of the variation factors
considered in this study (Table 3).
The existence of a statistical relationship between
metal concentrations in blood and in the different tissues
was studied by means of simple correlation coefficients
(Table 4). The relationship between Cd contents in
blood and tissues was not studied, since it was barely
detected in blood. The highest correlation was ob-
served between hepatic and renal Hg concentrations
(R=0.946, P<0.001).
Tabl e 2 Arsenic (As), cadmium (Cd), lead (Pb), and mercury (Hg) concentrations in the blood, liver, and kidney of common buzzards from
Portugal analyzed in the present study
Blood (n=93) Liver (n=56) Kidney (n=36)
μg/dl μg/g w.w. μg/g d.w. μg/g w.w. μ/g d.w. μg/g w.w
Mean±S.D 1.489± 1.457 0.014± 0.014 0.104± 0.136 0.029± 0.039 0.180± 0.133 0.041± 0.026
Median 1.391 0.013 0.074 0.022 0.149 0.036
Maximum 8.508 0.082 0.978 0.281 0.588 0.112
n<LOQ/% 28/30.1 % 21/37.5 % 7/19.4 %
Mean±S.D 0.201± 0.567 0.002± 0.005 0.322± 0.361 0.089± 0.097 1.553± 1.706 0.373± 0.381
Median 0.102 0.001 0.184 0.050 0.865 0.216
Minimum ND ND ND ND 0.033 0.009
Maximum 4.447 0.043 1.801 0.450 8.344 1.697
n<LOQ/% 88/94.6 % 2/3.6 % 0
Mean±S.D 14.711±65.156 0.142± 0.628 0.541± 0.687 0.152± 0.194 0.945± 1.356 0.24 0.364
Median 5.864 0.056 0.284 0.079 0.443 0.102
Maximum 631.473 6.089 3.468 0.949 5.331 1.386
n<LOQ/% 2/2.2 % 7/12.5 % 2/5.6 %
Mean±S.D 20.940± 26.728 0.202± 0.258 1.387± 1.242 0.389± 0.346 2.086± 1.689 0.50 0.310
Median 12.603 0.121 1.168 0.319 1.850 0.448
Maximum 164.895 1.590 5.314 1.479 5.945 1.482
n<LOQ/% 11/11.8 % 3/5.4 % 1/2.8 %
S.D. standard deviation, nnumber of samples, LOQ limit of quantification, ND non-detected
Environ Monit Assess
Previous data on the concentrations of nonessential
elements in the blood and tissues of common buzzard
are scarce. In fact, this study reports the first data on the
concentrations of trace elements (As, Cd, Hg, and Pb) in
blood and tissues of raptors residing in Portugal.
The common buzzards, being birds of prey, are at the
top of the food chain and consequently are potentially
exposed to any biomagnification processes that may
occur in a food web (Gochfeld and Burger 1987). In
the common buzzard, concentrations of toxic elements
reported in the literature were usually determined in the
liver and kidney (Battaglia et al. 2005; Castro et al.
2011; Naccari et al. 2009; Pérez-López et al. 2008).
Concentrations of heavy metals in the liver and kidney
can be considered suggestive of chronic exposure to
metals while concentrations in blood reflect recent
exposure and thus can be used as a real-time mon-
itor for all stages of the birdslife-cycles. Better
understanding of the relationship between heavy-metal
concentrations in tissues and blood would enable the
researchers to assess whether high concentrations in
blood warrant concern regarding their toxic effects,
without having to use lethal sampling techniques
(Burger and Gochfeld 1997;Castroetal.2011;
Naccari et al. 2009; Wayland et al. 2001a).
There have been a few studies on the transfer of As
through terrestrial food chains to predatory birds and on
the presence of such metalloid in the raptor tissues, but it
is known that vertebrate top predators experiencing
higher As burdens (Erry et al. 1999; Lebedeva 1997;
Lucia et al. 2012b). In fact, published data on arsenic
levels in common buzzards is sparse (Naccari et al.
2009; Pérez-López et al. 2008), and this study reports
the first data on blood As concentrations in this species,
so it is difficult to compare our results with other studies.
However, other species of birds sampled in natural areas
(Burger and Gochfeld 1997) and near potential sources
of metals (Baos et al. 2006a,b; Blanco et al. 2003)
showed similar and higher blood As concentrations,
respectively. With respect to As concentrations in the
liver and kidney, our results are much lower than those
observed for the common buzzard in Galicia, Spain
(Pérez-López et al. 2008) and in Sicily, Italy (Naccari
et al. 2009) where the exposure to As was considered of
no toxicological concern. However, we obtained similar
or slightly lower concentrations than those obtained by
Erry et al. (1999)inkestrels(Falco tinnunculus)from
Britain, which have similar feeding habits to common
buzzards. Erry et al. (1999) also measured hepatic and
renal As concentrations in barn owls (Tyto alba)that
despite having similar feeding habits with kestrels and
common buzzards, presented lower As concentrations
Fig. 1 Bar chart showing the
toxic metal concentrations
(expressed as arithmetic means,
μg/g wet weight) in the blood,
liver, and kidney in the 125
common buzzards considered in
this study. *P<0.05, **P<0.01,
Environ Monit Assess
than those obtained in these two species. Taking into
account this previous information, the study of common
buzzards in Portugal showed a low level of exposure to
this metalloid. However, the significantly higher As
levels found in kidney samples of adult birds suggest
that As is being bioconcentrated over time. This mean
that common buzzards face chronic exposure to this
metalloid (Eisler 1998). Despite the As burdens detected
in common buzzards were not likely to have been asso-
ciated with adverse health effects (this element could not
be considered as a threat for the survival of the studied
birds), it could be involved in sublethal effects (Lucia
et al. 2012a,b).
Cd has been described as one of the most dangerous
trace elements from environmental and toxicological
standpoints, both for humans and animals, not only for
its high toxicity but also for its persistence (Battaglia
et al. 2005; García-Fernández et al. 1996;Licataetal.
2010). Cd distribution and bioaccumulation patterns
observed in our study are consistent with the previous
studies in the common buzzard (Battaglia et al. 2005;
Castro et al. 2011; García-Fernández et al. 1996;Jager
et al. 1996; Naccari et al. 2009). The kidney was the
organ with the highest concentration. In contrast, Cd in
Tabl e 3 Heavy metals in adults and juveniles birds, females and male birds, from littoral and up-country birds and in blood samples
collected in the different seasons expressed as mean value (M.V.) ±standard deviation (S.D.) μg/dl in blood and μg/gd.w.intissues
Sample As Cd Pb Hg
M.V±S.D. M.V ±S.D. M.V. ±S.D. M.V.±S.D.
Blood (μg/dl) Age Adult 1.578± 1.178 9.865± 8.302
Juvenile 1.451±1.647 5.704±7.534
Gender Female 1.69 1.188 5.64 8.000 14.688± 14.085
Male 1.662±1.734 6.291±5.692 22.642± 26.565
Origin Littoral 1.389±1.088 20.852 ± 91.300 27.605 ±34.075
Up-country 1.593±1.769 8.436±8.860 14.131±13.409
Season Spring 2.267±2.220 5.413±6.493
Summer 1.297±1.249 6.310±9.278
Autumn 1.438±1.271 9.608± 7.353
Winter 1.205± 1.265 9.89 8.560 29.429±38.931
Liver (μg/g d.w.) Age Adult 0.104± 0.055 0.46 0.454
0.443±0.433 1.481±1.330
Juvenile 0.118± 0.192 0.209± 0.278
0.441±0.618 1.130±1.132
Gender Female 0.096± 0.048 0.199± 0.196 0.323± 0.348 1.364±1.341
Male 0.083±0.058 0.342±0.405 0.508± 0.555 1.415±1.385
Origin Littoral 0.077±0.044 0.273±0.359 0.484± 0.519 1.618±1.489
Up-country 0.132± 0.184 0.37 0.364 0.59 0.829 1.155±0.903
Kidney (μg/g d.w.) Age Adult 0.217± 0.139
0.828±1.326 1.895±1.725
Juvenile 0.139± 0.068
0.822±1.558 1.816±1.331
Gender Female 0.245± 0.106
2.056±1.793 0.706±0.762 2.407± 1.705
Male 0.166±0.131
1.496±1.990 0.892±1.533 1.745± 1.720
Origin Littoral 0.150±0.092 1.620±1.972 0.874± 1.207 2.455±1.871
Up-country 0.241± 0.179 1.42 1.048 1.08 1.665 1.348±0.928
(Z=2.940, P<0.003),
(Z=3.164, P<0.002),
(H=11.639, P<0.008),
(H=24.190, P<0.001),
(Z=2.641, P<0.008),
(Z=2.040, P<0.043),
(Z=1.981, P<0.048),
(Z=2.447, P<0.013)
Tabl e 4 Correlations coefficients (R) between blood and tissues
and between tissues for each element in common buzzard
As R=0.572** R=0.530* R=0.886***
Cd −− R=0.831***
Pb R=0.859*** R=0.875*** R=0.811***
Hg R=0.857*** R=0.832*** R=0.946***
Environ Monit Assess
the blood was not detected in 94.6 % of blood samples,
which reflect its low concentrations in blood and/or may
be associated with the detection limit of our analytical
method. In the blood samples where Cd was detected,
the mean concentration was higher than that obtained by
García-Fernández et al. (1996) in samples of whole
blood from wild birds. Comparison of the Cd concen-
trations in tissues obtained in this study with those
obtained in other recent studies with the same species
reveals that our results differ depending on the geo-
graphical area: similar with the results obtained in Italy
by Alleva et al. (2006), Battaglia et al. (2005), and
Naccari et al. (2009), lower than those observed in
Galicia, Spain by Pérez-López et al. (2008) and Castro
et al. (2011), and higher than the results obtained by
García-Fernández et al. (1995) in Murcia, Spain. Ac-
cording to Scheuhammer (1987), the hepatic and renal-
Cd concentrations obtained in our study are indicative of
a prolonged exposure to low and background amounts
of this metal.
Pb is a highly toxic heavy metal that acts as a non-
specific poison, affecting all body systems (Hernández
and Margalida 2009). Blood-Pb concentrations obtained
in this study were slightly higher than those obtained by
García-Fernández et al. (1995) and García-Fernández
et al. (1997) in common buzzards from south-eastern
Spain. According to Franson (1996), 90.3 % of the
common buzzards analyzed in our study had blood-Pb
concentrations compatible with an absence of abnormal
Pb exposure, 8.6 % had Pb levels indicative of subclin-
ical exposure, and only 1.1 % had a potentially lethal
blood-Pb concentration. Taking hepatic-Pb concentra-
tions into consideration, several researchers determined
higher concentrations in the same species than those we
quantified (Alleva et al. 2006; Battaglia et al. 2005;
Jager et al. 1996; Licata et al. 2010; Naccari et al.
2009; Pain et al. 1995; Pérez-López et al. 2008). In
contrast, García-Fernández et al. (1995) and García-
Fernández et al. (1997) quantified lower hepatic- and
renal-Pb concentrations. According to the ranges
established by Pain et al. (1995), none of the studied
animals exceeded the calculated dry weight threshold
for massive exposure and most of them had very low
hepatic and renal Pb concentrations of <2 μg/g, with
many <1 μg/g d.w., indicating a safe environmental
exposure. These results suggest that common buzzards
in Portugal are exposed to relatively low levels of Pb.
However, some studies provide evidence that low-level
Pb exposure, although not causing the clinical
symptoms of classical Pb poisoning, may nevertheless
have subtle detrimental effects on normal behavior and
cognitive function (Burger and Gochfeld 2000;
Scheuhammer 1987), while Pb poisoning has been rec-
ognized as one of the most significant causes of mortal-
ity in raptors (Pain et al. 2005).
There are very few studies on Hg concentrations in
birds of prey and, as far as we know, this is the first
report on Hg blood concentrations in the common buz-
zard and, in Portugal, the first in raptors. Tartu et al.
(2013) and Goutte et al. (2014) evaluated the effect of
Hg in seabirds predators, and they conclude that Hg
exposure could affect the ability of modulate their re-
productive effort. As threshold-effects levels for Hg
have yet to be established for bird blood, it is unclear
whether Hg levels were high enough to pose a risk to
any of these birds. Considering the hepatic and renal Hg
concentrations, other authors have quantified higher Hg
concentrations in the common buzzard (Alleva et al.
2006;Castroetal.2011). Hg concentrations observed
in our birds suggested that a source of Hg does exist.
According to the previous information and to
Scheuhammer (1987), the common buzzards studied
are chronically exposed to normal background levels.
It is perhaps because Portugal is a small country (with
a maximum extension in length of 561 and 218 Km in
width) that we did not observe significant differences
between areas of origin in the concentrations of various
elements analyzed.
Age was the only factor explaining Cd accumulation
in both the liver and kidney, as observed in other studies
with wild birds (García-Fernández et al. 1996;Naccari
et al. 2009; Ribeiro et al. 2009). With continued expo-
sure, even at low levels, this nonessential element is
accumulated throughout the life span of birds, due to
its extremely long biological half-life once bound to
metallothionein in tissues and its slow elimination from
these tissues (Scheuhammer 1987;Furness1996). Age
also had an influence on blood Pb and Hg concentra-
tions, but this influence was not verified in hepatic and
renal concentrations. Differences in blood Hg levels
between age classes seem to be related with prey-size
selection and stage of juvenile feather moult (Evers et al.
2005). Knowing that blood Hg is strongly influenced by
dietary uptake, these age-related differences could be
due to adults and young eat different foods or eat dif-
ferent proportions of the same foods (Burger and
Gochfeld 1997). Apart from the dietary intake, the Hg
concentration in blood reflects physiological influences,
Environ Monit Assess
such as mobilization and storage in feathers and eggs
(Dauwe et al. 2000,2003; Honda et al. 1986). The
amount of Hg eliminated into eggs is usually small
compared to the amount transferred into feathers during
the moult (Furness 1993). Feather moult and growth is
the main Hg excretion pathway (Braune and Gaskin
1987; Honda et al. 1985; Monteiro and Furness 2001).
The ability to rapidly transfer blood Hg into growing
feathers partly accounts for the significant difference in
blood Hg levels between adults and juveniles prior to
fledging (Evers et al. 2005). Although the Pb excretion
into growing feathers occurs to a lesser extent compared
with Hg (Dmowski 1999; Furness 1993), the differences
between adults and juveniles in blood Pb concentrations
could also be related to the stage of juvenile feather
moult and growth. Once blood Pb concentrations reflect
immediate dietary intake (Furness 1993), the differences
for blood Pb concentrations between adults and juve-
niles could also be explained by the considerations of
feeding behavior (Burger and Gochfeld 1997).
Only Pb- and Hg-blood concentrations were influ-
enced by season. Pb poisoning in raptors is likely to be
more significant in autumn and winter, since the propor-
tion of carrion taken by certain species may be higher in
these seasons. In addition, since waterfowl and other
game species are generally hunted during autumn and
winter, killed, crippled, and poisoned individuals pro-
vide a readily available Pb-contaminated food source
(Pain and Amiard-Triquet 1993). Common buzzards
often act as scavengers and, in this way, are more likely
to be exposed to the lead shot prevalent in small game
species (Battaglia et al. 2005). This fact could help to
understand the generally higher blood Pb concentration
quantified in autumn and winter. In the case of Hg,
possible explanations for the significant differences
found between the different seasons are migration, diet
(Eisler 1987), and moult. It is during the moulting that
Hg is incorporated in the keratin structure of the
feathers, thus reducing the Hg levels in blood (Braune
and Gaskin 1987; Honda et al. 1986; Monteiro and
Furness 2001).
Regarding correlations, we found that Pb- and Hg-
blood concentrations were statistically related to their
corresponding concentrations in the liver or kidney
which suggests that blood concentrations of these metals
may be a useful indicator of the degree of recent expo-
sure. García-Fernández et al. (1996) showed that blood-
Cd concentration may also be a useful indicator of the
degree of exposure to this metal. In this study, due to the
large number of samples in which it was not detected, it
was not possible to show whether blood could be a
useful indicator of the degree of exposure to Cd. Kidney
samples could be used to assess chronic exposure to As,
Cd, Pb, and Hg, a working hypothesis substantiated by
the significant correlations between liver and kidney
concentrations of these trace elements.
In general, Hg was the element studied present in the
highest concentrations in the three types of samples, and
the kidney was the sample with the highest concentra-
tions of each element. If possible, in future studies, it
would be important to exclude birds that had migrated
from northern Europe and to measure Hg concentrations
in feathers, in order to further examine the causes of the
higher blood-Hg concentrations in winter and autumn.
The generally higher blood-Pb concentrations quanti-
fied in autumn and winter are possibly due to birds
higher consumption of individuals crippled and poi-
soned through the hunting of small game species, which
indicates that future measures regarding hunting practices
are necessary in order to avoid high Pb exposure and/or
Pb poisoning in wild birds. Although raptors are at the top
of the food chain, and thus potentially exposed to any
biomagnification processes that may occur in a food web,
the individuals studied in this study generally had low
levels of heavy metals in blood and tissues, compared
with other authors. However, there are unknown sources
of exposure to the trace elements studied, so further
studies are needed to determine their origin.
Acknowledgments This study was supported by the fellowship
SFRH/BD/62115/2009 provided by the Fundação para a Ciência
e Tecnologia. The authors wish to thank all personnel at the Serveis
Científics i Tècnics of the University of Barcelona, Spain and
especially all personnel from the Servei dEcopatologia de Fauna
Salvatge of the Autonomous University of Barcelona, Spain.
Alleva, E., Francia, N., Pandolfi, M., De Marinis, A. M., Chiarotti,
F., & Santucci, D. (2006). Organochlorine and heavy-metal
contaminants in wild mammals and birds of Urbino-Pesaro
Province, Italy: an analytic overview for potential
bioindicators. Archives of Environmental Contamination
and Toxicology, 51,123134.
Environ Monit Assess
Baos, R., Jovani, R., Forero, M. G., Tella, J. L., Gómez, G.,
Jiménez, B., González, M. J., & Hiraldo, F. (2006a).
Relationships between T-cell-mediated immune response
and Pb, Zn, Cu, Cd, and As concentrations in blood of
nestling white storks (Ciconia ciconia) and black kites
(Milvus migrans) from Doñana (southwestern Spain) after
the Aznalcóllar toxic spill. Environmental Toxicology and
Chemistry, 25(4), 11531159.
Baos, R., Jovani, R., Pastor, N., Tella, J. L., Jiménez, B., Gómez, G.,
genotoxic effects of heavy metals and arsenic in wild nestling
white storks (Ciconia ciconia)andblackkites(Milvus
migrans) from southwestern Spain after a mining accident.
Environmental Toxicology and Chemistry, 25(10), 27942803.
Battaglia, A., Ghidini, S., Campanini, G., & Spaggiari, R. (2005).
Heavy metal contamination in little owl (Athene noctua)and
common buzzard (Buteo buteo) from northern Italy.
Ecotoxicology and Environmental Safety, 60,6166.
Blanco, G., Frías, O., Jiménez, B., & Gómez, G. (2003). Factors
influencing variability and potential uptake routes of heavy
metals in black kites exposed to emissions from a solid-waste
incinerator. Environmental Toxicology and Chemistry,
22(11), 27112718.
Braune, B. M., & Gaskin, D. E. (1987). Mercury levels in
Bonapartes gulls (Larus philadelphia)duringautumnmolt
in the Quoddy Region, New Brunswick, Canada. Archives of
Environmental Contamination and Toxicology, 16,539549.
Burger, J., & Gochfeld, M. (1997).Age differences in metals in the
blood of herring (Larus argentatus) and Franklins(Larus
pipixcan) gulls. Archives of Environmental Contamination
and Toxicology, 33,436440.
Burger, J., & Gochfeld, M. (2000). Effects of lead on birds
(Laridae): a review of laboratory and field studies. Journal
of Toxicology and Environmental Health. Part B, Critical
Reviews, 3(2), 5978.
Castro, I., Aboal, J. R., Fernández, J. A., & Carballeira, A. (2011).
Use of raptors for biomonitoring of heavy metals: Gender,
age and tissue selection. Bulletin of Environmental
Contamination and Toxicology, 86,347351.
Catry, P., Costa, H., Elias, G., & Matias, R. (2010). Aves de
Portugal, Ornitologia do território continental. Lisboa:
Assírio & Alvim.
Clarke, J. U. (1998). Evaluation of censored data methods to allow
statistical comparisons among very small samples with below
detection limits observations. Environmental Science and
Technology, 32(1), 177183.
Dauwe, T., Bervoets, L., Blust, R., Pinxten,R., & Eens, M. (2000).
Can excrement and feathers of nestling songbirds be used as
biomonitors for heavy metal pollution? Archives of
Environmental Contamination and Toxicology, 39(4), 541
Dauwe, T., Bervoets, L., Pinxten, R., Blust, R., & Eens, M. (2003).
Variation of heavy metals within and among feathers of birds
of prey: Effects of molt and external contamination.
Environmental Pollution, 124(3), 429436.
Dmowski, K. (1999). Birds as bioindicators of heavy metal pollu-
tion: Review and examples concerning European species.
Acta Ornithologica, 341,125.
Eisler, R. (1987). Mercury hazards to fish, wildlife, and inverte-
brates: a synoptic review. U.S. Fish and Wildlife Service
Biological Report, 85(1.10), 32.
Eisler, R. (1998). Arsenic hazards to fish, wildlife, and inverte-
brates: a synoptic review. U.S. Fish and Wildlife Service
Biological Report, 85(1.12), 2.
Erry, B. V., Macnair, M. R., Meharg, A. A., Shore, R. F., &
Newton, I. (1999). Arsenic residues in predatory birds from
an area of Britain with naturally and anthropogenically
elevated arsenic levels. Environmental Pollution,
106(1), 9195.
Esteban, M., & Castano, A. (2009). Non-invasive matrices in
human biomonitoring: a review. Environment International,
35(2), 438449.
Evers, D. C., Burgess, N. M., Champoux, L., Hoskins, B., Major,
A., Goodale, W. M., Taylor, R. J., Poppenga, R., & Daigle, T.
(2005). Patterns and interpretation of mercury exposure in
freshwater avian communities in northeastern north America.
Ecotoxicology, 14(12), 193221.
Florea, A. M., & Busselberg, D. (2006). Occurrence, use and
potential toxic effects of metals and metal compounds.
Biometals, 19(4), 419427.
Franson, J. C. (1996). Interpretation of tissue lead residues in birds
other than waterfowl. In W. N. Beyer, G. H. Heinz, & A. W.
Redmon-Norwood (Eds.), Environmental contaminants in
wildlife: Interpreting tissue concentrations (1st ed., pp.
265279). Boca Raton: Lewis.
Furness, R. W. (1993). Birds as monitors of pollutants. In R. W.
Furness&J.J.D.Greenwood(Eds.),Birds as monitors of
environmental change (pp. 86143). London: Chapman and
Furness, R. W. (1996). Cadmium in birds. In W. N. Beyer, G. H.
Heinz, & A. W. Redmon-Norwood (Eds.), Environmental
contaminants in wildlife: Interpreting tissue concentrations
(1st ed., pp. 389404). Boca Raton: Lewis.
García-Fernández, A. J., Sanchez-Garcia, J. A., Jimenez-
Montalban, P., & Luna, A. (1995). Lead and cadmium in
wild birds in southeastern Spain. Environmental Toxicology
and Chemistry, 14, 20492058.
García-Fernández, A. J., Sanchez-Garcia, J. A., Gomez-Zapata,
blood and tissues of wild birds. Archives of Environmental
Contamination and Toxicology, 30,252258.
(1997). Environmental exposure and distribution of
lead in four species of raptors in Southeastern Spain.
Archives of Environmental Contamination and Toxicology,
Gochfeld, M., & Burger, J. (1987). Heavy metal concentrations in
the liver of three duck species: Influence of species and sex.
Environmental Pollution, 45,115.
H., & Chastel, O. (2014). Demographic responses to mercury
exposure in two closely related Antarctic top predators.
Ecology, 95(14), 10751086.
Henny, C. J., Rudis, D. D., Roffe, T. J., & Robinson-Wilson, E.
(1995). Contaminants and sea ducks in Alaska and the cir-
cumpolar region. Environmental Health Perspectives,
103(4), 4149.
Hernández, M., & Margalida, A. (2009). Assessing the risk of lead
exposure for the conservation of the endangered Pyrenean
bearded vulture (Gypaetus barbatus) population.
Environmental Research, 109,837842.
Environ Monit Assess
Honda, K., Min, B. Y., & Tatsukawa, R. (1985). Heavy metal
distribution in organs and tissues of the eastern great white
egret Egretta alba modesta. Bulletin of Environmental
Contamination and Toxicology, 35(6), 781789.
Honda, K., Nasu, T., & Tatsukawa, R. (1986). Seasonal changes in
mercury accumulation in the black-eared kite, Milvus
migrans lineatus. Environmental Pollution, 42,325334.
Jager, L. P., Rijnierse, F. V. J., Esselink, H., & Baars, A. J. (1996).
Biomonitoring with the Buzzard Buteo buteo in the
Netherlands: Heavy metals and sources of variation.
Journal of Ornithology, 137,295318.
Lebedeva, N. V. (1997). Accumulation of heavy metals by birds in
the southwest of Russia. Russian Journal of Ecology, 28(1),
Licata, P., Naccari, F., Lo Turco, V., Rando, R., Di Bella, G., &
Dugo, G. (2010). Levels of Cd (II), Mn (II), Pb (II), Cu (II),
and Zn (II) in Common Buzzard (Buteo buteo)fromSicily
(Italy) by Derivative Stripping Potentiometry. International
Journal of Ecology,1-7.
López-Alonso, M., Miranda, M., García-Partida, P., Cantero, F.,
Hernández, J., & Benedito, J. L. (2007). Use of dogs as
indicators of metal exposure in rural and urban habitats in
NW Spain. Science of the Total Environment, 372,668675.
Lucia, M., Bocher, P., Cosson, R. P., Churlaud, C., & Bustamante,
P. (2012a). Evidence of species-specific detoxification pro-
cesses for trace elements in shorebirds. Ecotoxicology, 21(8),
Lucia, M., Bocher, P., Cosson, R. P., Churlaud, C., Robin, F., &
Bustamante, P. (2012b). Insight on trace element detoxifica-
tion in the Black-tailed Godwit (Limosa limosa) through
genetic, enzymatic and metallothionein analyses. Science of
the Total Environment, 423,7383.
Monteiro, L. R., & Furness, R. W. (2001). Kinetics, dosere-
sponse, and excretion of methylmercury in free-living adult
Corys shearwaters. Environmental Science and Technology,
35(4), 739746.
Naccari, C., Cristani, M., Cimino, F., Arcoraci, T., & Trombetta,
D. (2009). Common buzzards (Buteo buteo) bio-indicators of
heavy metals pollution in Sicily (Italy). Environment
International, 35,594598.
Pain, D. J., & Amiard-Triquet, C. (1993). Lead poisoning of
raptors in France and elsewhere. Ecotoxicology and
Environmental Safety, 25,183192.
Pain, D. J., Sears, J., & Newton, I. (1995). Lead concentrations in
birds of prey in Britain. Environmental Pollution, 87,173180.
Pain, D. J., Meharg, A. A., Ferrer, M., Taggart, M., & Penteriani,
V. (2005). Lead concentrations in bones and feathers of the
globally threatened Spanish imperial eagle. Biological
Conservation, 121,603610.
Peakall, D., & Burger, J. (2003). Methodologies for assessing
exposure to metals: Speciation, bioavailability of metals,
and ecological host factors. Ecotoxicology and
Environmental Safety, 56(1), 110121.
Pérez-López, M., Hermoso de Mendoza, M., López Beceiro, A., &
Soler Rodriguez, F. (2008). Heavy metal (Cd, Pb, Zn) and
metalloid (As) content in raptor species from Galicia
(NW Spain). Ecotoxicology and Environmental Safety,
Ribeiro, A. R., Eira, C., Torres, J., Mendes, P., Miquel, J., Soares,
A. M., & Vingada, J. (2009). Toxic element concentrations in
the Razorbill Alca torda (Charadriiformes, Alcidae) in
Portugal. Archives of Environmental Contamination and
Toxicology, 56,588595.
Scheuhammer, A. M. (1987). The chronic toxicity of aluminium,
cadmium, mercury, and lead in birds: a review.
Environmental Pollution, 46,263295.
Shlosberg, A., Rumbeiha, W. K., Lublin, A., & Kannan, K. (2011).
A database of avian blood spot examinations for exposure of
wild birds to environmental toxicants: the DABSE biomon-
itoring project. Journal of Environmental Monitoring, 13(6),
Stout, J. H., & Trust, K. A. (2002). Elemental and organochlorine
residues in bald eagles from Adak Island, Alaska. Journal of
Wildlife Diseases, 38(3), 511517.
Tartu, S., Goutte, A., Bustamante, P., Angelier, F., Moe, B.,
Clement-Chastel, C., Bech, C., Gabrielsen, G. W., Bustnes,
J. O., & Chastel, O. (2013). To breed or not to breed:
Endocrine response to mercury contamination by an Arctic
seabird. Biology Letters, 9,14.
Wayland, M., Neugebauer, E., & Bollinger, T. (1999).
Concentrations of lead in liver, kidney, and bone of bald and
golden eagles. Archives of Environmental Contamination and
Toxicology, 37(2), 267272.
Wayland, M., García-Fernández, A. J., Neugebauer, E., &
Gilchrist, H. G. (2001a). Concentrations of cadmium, mer-
cury and selenium in blood, liver and kidney of common
eider ducks from the Canadian arctic. Environmental
Monitoring and Assessment, 71,255267.
Wayland, M., Gilchrist, H. G., Dickson, D. L., Bollinger, T.,
James, C., Carreno, R. A., & Keating, J. (2001b). Trace
elements in king eiders and common eiders in the Canadian
arctic. Archives of Environmental Contamination and
Toxicology, 41(4), 491500.
Wayland, M., Drake, K. L., Alisauskas, R. T., Kellett, D. K.,
Traylor, J., Swoboda, C., & Mehl, K. (2008). Survival rates
and blood metal concentrations in t wo species of free-ra nging
North American sea ducks. Environmental Toxicology and
Chemistry, 27(3), 698704.
Environ Monit Assess
... Compared with the golden eagle, less is known about lead exposure in the common buzzard and we did not find any published studies that reported lead isotope signatures in this species. However, opportunistic scavenging has been presumed to be the cause of lead contamination in buzzards (Battaglia et al., 2005;Carneiro et al., 2014). Furthermore, three studies on common buzzards have reported elevated liver and kidney lead levels that were of similar magnitude to those found in (obligate scavenging) vultures (Pain and Amiard-Triquet, 1993;Naccari et al., 2009;Castro et al., 2011). ...
... When evaluating blood lead concentrations, we found seasonal trends in risk of lead poisoning with blood lead levels higher during the hunting than the non-hunting season. Previous studies have already reported such an association (e.g., Berny et al., 2015;Carneiro et al., 2014;Gangoso et al., 2009;Mateo et al., 1999). However, our review provides the first systematic evaluation and evidence of this trend using data from 10 species. ...
Full-text available
Lead contamination is a widely recognised conservation problem for raptors worldwide. There are a number of studies in individual raptor species but those data have not been systematically evaluated to understand raptor-wide lead exposure and effects at a pan-European scale. To critically assess the extent of this problem, we performed a systematic review compiling all published data on lead in raptors (1983–2019) and, through a meta-analysis, determined if there was evidence for differences in exposure across feeding traits, geographical regions, between hunting and non-hunting periods, and changes over time. We also reviewed the impact of lead on raptors and the likely main source of exposure. We examined 114 studies that were unevenly distributed in terms of time of publication and the countries in which studies were performed. Peer-reviewed articles reported data for 39 raptor species but very few species were widely monitored across Europe. Obligate (vultures) and facultative scavengers (golden eagle, common buzzard and white-tailed sea eagle) accumulated the highest lead concentrations in tissues and generally were the species most at risk of lead poisoning. We found no evidence of a spatial or decadal trend in lead residues, but we demonstrated that high lead blood levels relate to hunting season. Exposure at levels associated with both subclinical and lethal effects is common and lead from rifle bullets and shot is often the likely source of exposure. Overall, our review illustrates the high incidence and ubiquity of lead contamination in raptors in Europe. However, we did not find studies that related exposure to quantitative impacts on European raptor populations nor detailed studies on the impact of mitigation measures. Such information is urgently needed and requires a more harmonised approach to quantifying lead contamination and effects in raptors across Europe.
... The non-essential trace elements As, Cr, Cd, and Pb cause health problems to organisms, even at low concentrations (Rahman et al., 2013), whereas the essential trace elements Cu, Ni, Fe, Co, and Zn are important for physiological processes, but can cause toxic effects at high concentrations (Ahmed et al., 2016;Jeong et al., 2021a). Biomonitoring research is important because it provides useful information to evaluate the degree of pollution in ecosystems, determine the fate of contaminants and biogeochemical cycles of trace metals, and identify metal pollution sources through forensic investigations (George et al., 2012;Carneiro et al., 2014;Keke et al., 2020;Mehana et al., 2020). Marine organisms, such as fish, bivalve mollusks, aquatic plants, and crustaceans, are an important food resource and are used as monitoring organisms for metal contamination in many countries (El-Moselhy et al., 2013;Mazzei et al., 2013;Luo et al., 2014;Rajeshkumar and Li, 2018;Gopi et al., 2020). ...
Thirteen trace metals and Zn isotopic signatures were investigated in mussels and oysters collected from the coast of South Korea to evaluate their bioavailability in bivalve mollusks. The average Cu, Zn, and Cd concentrations were 2.6-17.7 times higher in oysters than mussels, and high biota sediment accumulation factors (>30) were observed for these metals in oysters. Except for Pb in mussels, most metals had no correlation with total sediment concentrations. In oysters, Fe, V, Cu, Zn, Sn, and Pb concentrations were significantly correlated with sediments. The average values of δ66ZnIRMM3702 in mussels, oyster, and sediments were +0.09‰, +0.12‰, and -0.06‰, respectively. Soft tissues of mussels and oysters with high Zn concentrations tended to contain lighter Zn isotopes. The results indicate that oysters are a better biomonitoring organism for metal contamination than mussels and can be used in the monitoring and management of coastal environments and ecosystems.
... Metal biomonitoring allows the identification of the bioavailability of environmental pollutants from the measurement of chemical residues in tissues or fluids of animals from a specific habitat [10,11]. Specifically, raptors are an ideal tool to study the environmental quality of the ecosystem through biomonitoring because they are located at the top of the trophic chain, have a wide geographical distribution and they are highly sensitive to changes in the environment [16,56]. ...
Full-text available
The monitoring of trace elements and toxic metals in apical predators of the trophic chain provides data on the degree of contamination in ecosystems. The common kestrel is one of the most interesting raptors in this respect in the Canary Islands; therefore, the study of the levels of trace elements and toxic metals in this species is of much scientific value. The content of trace elements and toxic metals (B, Ba, Co, Cr, Cu, Fe, Mn, Mo, Li, Zn, Ni, Sr, V, Al, Cd, Pb) was determined in the liver, muscle, and feathers of 200 specimens of common kestrel carcasses (Falco tinnunculus canariensis) from Tenerife. Cr (0.82 ± 2.62 mg/kg), Cu (11.82 ± 7.77 mg/kg), and Zn (198.47 ± 520.80 mg/kg) are the trace elements that stand out in the feather samples; this may be due to their affinity for the pigments that give them their coloring. Li was noteworthy in the liver samples (8.470 ± 5.702 mg/kg). Pb stood out in the feathers (4.353 ± 20.645 mg/kg) > muscle (0.148 ± 0.095 mg/kg) > liver (0.187 ± 0.133 mg/kg). The presence of metals in feathers correlates with recent exposure and reflects environmental contamination. When using raptor feathers as indicators of metal contamination, it is important to know what the levels of each metal signify. The analysis of the different tissues and organs of raptors, such as the common kestrel, provides valuable information on the degree of environmental contamination of the ecosystem in which it lives. Gender was not an influencing factor in this study.
... Coal combustion, including emissions from coal-burning stoves is another important cadmium source, especially in Eastern Europe (Seshadri et al., 2010;Pacyna et al., 2010). Some studies indicated that cadmium levels in buzzards recorded Northern Italy, (Battaglia et al., 2005), Portugal (Carneiro et al., 2014) and Spain (Castro et al. 2011) were lower than in East Poland (Kitowski et al., 2016). Other low levels of liver cadmium concentrations were recorded in goshawks in Germany (Kenntner et al., 2003) and buzzards in Spain (Castro et al., 2011). ...
Full-text available
Large carnivores such as pumas are often killed in conflicts with humans because they prey on domestic livestock. Habitat loss, partly driven by the increasing use of traditional pasture systems, makes livestock vulneracle to puma attacks. The aim of this study was describe the conflict between local farmers and pumas in a mosais of Protected Areas in southern Brazil. We hypothesized that the farmer's preception, knowledge and attitudes towards the conflict with pumas is affected by socioeconomic variables, such as age, educaton, monthly income and farming experience. Forty-five face-to-face interviews with local farmers were performed in 2011, using a structured questionnaire with 16 open and 26 closed questions focusing on the perception farmers. Our results show that the majority of the local population considered the conflict with pumas a serious problem and thought that attacks by pumas on domestic herds shoud be controlled with the involvement of government authorities. Financial losses caused about pumas attacks on farms did not inflence the attitudes of farmers, and knowledge abou pumas was more inluenced by social variables such as age and educational level. Meetings with the local Rural Consulting Council revelated that conflict with pumas still remains in the region. In this context, a long-term educational program with local farmers is highly recommended, focused on engaging the community in the discussion about possible mitigations tools. Conservation wildlife depends on the ability to provaide decision makers with academic and traditional knowledge which could be build bridges between the commnunity and Environmental Agencies.
... Coal combustion, including emissions from coal-burning stoves is another important cadmium source, especially in Eastern Europe (Seshadri et al., 2010;Pacyna et al., 2010). Some studies indicated that cadmium levels in buzzards recorded Northern Italy, (Battaglia et al., 2005), Portugal (Carneiro et al., 2014) and Spain (Castro et al. 2011) were lower than in East Poland (Kitowski et al., 2016). Other low levels of liver cadmium concentrations were recorded in goshawks in Germany (Kenntner et al., 2003) and buzzards in Spain (Castro et al., 2011). ...
INTRODUCTION This book is edited by two environmental scientists with interests in GIS and remote sensing applications, forest, and habitat change, and large animal ecology. It examines the cutting-edge issues related to animal and habitat ecology research and management, with case studies across Asia, the Americas, Africa, and Europe. The topics are based on research and reviews of specific and general topics covering the habitats as well as the species of importance in selected case studies, and the overall general scenarios. The chapters of the book are written by leading academic and field experts, who discuss their skills and research findings. The field covered is vast, so selectivity enters, based on concurrent and relevant subjects, such as field research techniques, nature-society relations, and chemistry in conservation biology and policy. The chapters focus on cases as varied as vultures, storks, waterbirds, pumas or cougars, and elephants, and research techniques such as genetics and GIS. Technological developments, such as GIS and remote sensing, and some genetic methods have altered the nature of ecological research. These include the utility of GIS, and the related techniques of remote sensing, which allow more precise and accurate measurements and consequently more informed and reliable results. Species distribution modeling enables evaluations of habitat suitability and the impacts of habitat alteration and the requirements for the improvement of animal conservation. Integrated research, including the interfacial studies of social and natural sciences, is increasingly important in ecological research, as disciplinary boundaries break down and hybrid disciplines emerge. Simultaneously, chemical and genetic studies are increasing in importance, with applications in the interfaces of the ecological, social, and medical sciences. The topics covered in this book may contribute to the scientific understanding of different, relevant topics on research methods on ecology and conservation biology. This is especially the case, considering the wide selection of research topics in widely varying contexts. Strands may emerge from these selected topics that may inform further research and development in varied areas. These research findings may be replicable in the different contexts to contribute to the objectives of ecological sustainability. The results and conclusions presented, and the strategies recommended in different chapters will help the policymakers and decision implementers, scientists, resource managers, research scholars, and other stakeholders to attain effective and sustainable animal conservation and habitat
... The presence of blood in the droppings, which is not actually blood but the breakdown product of blood, bird just may not 'look' well, sitting quietly with fluffed feathers. Birds shows weakness and depression, loss of control and coordination of its body movements, constant thirst regurgitation of water, frequent runny green droppings, seizures, muscle tremors and finally death [15]. Wild birds can be poisoned by the lead pellets found in the wetlands, ingestion of lead fishing weights and contaminated prey animals. ...
Full-text available
Lead (Pb) is a heavy metal that is found to be present naturally in the earth crust but nowadays it is spreader widely in our environment due to the man-made activities such as mining, fossil fuel burning etc. Lead is also becoming a part of our life as it presents in most of the products of our daily basis equipment like power supply batteries. Due to these interactions and widespread presence of the Pb in our life, there is an increase in its amount in the environment that has toxic effect on all the living creatures and cause Lead Poisoning. It's a slow process of accumulation of this heavy metals in our food chain, water resources and body initiate over month or years. Even a minute level exceeds than the 5 µg/d causes severe health problems, deformities and death. Although there are various major steps has been taken to overcome the effect of metal toxicity but still many cases are reported. Lead poisoning is an issue whose impact is seen in different living organisms such as humans, animals, plants, microorganisms in our ecosystem .
... In regards to As, concentrations reached in nestlings may be of special concern in the mining area. For comparison, blood As levels in other raptor species were compiled in Fig. 2. In general, nestling Eagle owls showed higher As levels than those reported in Northern goshawk and Common buzzard (Buteo buteo) from Spain, Norway and Portugal (Carneiro et al., 2014;Dolan et al., 2017), and were similar to those found in Black kites from Spain and Portugal (Blanco et al., 2003;Carneiro et al., 2018) (Fig. 2). Black kites sampled in Doñana (Spain) in 1999 after the Aznalc ollar mine spill showed remarkably higher As levels (125 ng/ml) than those found in nestling Eagle owls, which was related to the toxic spill and the foraging habits of the species in that sampling site (marine fish were found as prey remains in the nests) (Baos et al., 2006). ...
Some metals and metalloids (e.g. Pb, Hg, Cd and As) are well-known for their bioaccumulation capacity and their toxic effects on birds, but concerns on other minor elements and rare earth elements (ME and REE) are growing due to their intensive use in modern technology and potential toxicity. Vitamins and carotenoids play essential roles in nestling growth and proper development, and are known to be affected by the metals classically considered as toxic. However, we are unaware of any attempts to evaluate the exposure to 50 elements and related effects in plasma vitamins and carotenoids in raptor species. The main goals of this study are: (i) to assess the exposure to 50 elements (i.e. classic toxic elements, trace elements, REE and ME) in nestling Eagle owls (Bubo bubo) inhabiting three differently polluted environments (mining, industrial and control areas) in southeastern Spain, and (ii) to evaluate how element exposure affects plasma vitamin and carotenoid levels, hematocrit and body measurements (mass and wing length) of the individuals. Our results show that local contamination in the mining area contributes to increased blood concentrations of Pb, As and Tl in nestlings, while diet differences between control and mining/industrial areas may account for the different levels of Mn, Zn, and Sr in blood, and lutein in plasma. Plasma tocopherol levels were increased in the mining-impacted environment, which may be a mechanism of protection to prevent toxic element-related oxidative stress. Plasma α-tocopherol was enhanced by 20% at blood Pb concentrations ≥8 ng/ml, and nestlings exhibited up to 56% increase in α-tocopherol levels when blood Pb concentrations reached 170 ng/ml. Tocopherol seems to be a sensitive biomarker when exposed to certain toxic elements (e.g. Pb, As, Tl).
... Birds have been recognized since the 1960s as potential bioindicators of environmental pollution (18). With the aim of measuring environmental pollution from metals and their effects on living organisms, researchers have used different materials taken from birds, such as blood, lungs, liver, musculature, and the gizzard (19,20,21,22,23). Fairly reliable results for the measurement of environmental contamination with metals have been obtained using avian feathers (24,25,26,27). ...
Full-text available
The aim of this study was to assess the presence of metals in three regions of Kosovo using chicken (Gallus gallus domesticus) breast feathers collected from the industrial regions of Mitrovica and Obiliq and the non-industrial region of Dragash. This study was carried out from September to November 2016, and feathers were collected from 90 individual domestic chickens housed as free range. The concentrations of metals in the chicken feathers were determined with atomic absorption spectrometry (AAS). The range of average measured concentrations of metals (μg g-1) in examined regions were: Zn 109-131, Mn 6.17-31.30, Cu 22.1-27.2, Cr 5.09-19.0, Ni 12.3-15.8, Pb <0.0945-15.5, Cd 11.1-12.3 and As <0.099-7.44. The highest average levels of metals were determined in regions (μg g-1): Dragash: Zn 131, Cu 27.2, Mn 31.3, Cr 19.0, Ni 15.8; Mitrovica As 7.44, Cd 12.3, Pb 15.5. High statistically significant differences (p<0.001) were found between the three regions for Pb, As, Mn, and Cr content. There were no significant differences (p>0.05) between the Mitrovica and Obiliq regions in terms of Zn content, Mitrovica and Dragash in terms of Cu or between the Obiliq and Dragash regions in terms of Cd content. These results should concern the environmental agencies in Kosovo and encourage them to take concrete steps by periodically checking these pollutants in these two industrial regions. Based on our results, we recommend that programmes for monitoring environmental pollution from metals could use chicken feathers as an important and valuable test material.
Full-text available
In nature, certain animals share a common living environment with humans, thus these animals have become biomonitors of health effects related to various environmental exposures. As one of the most toxic environmental chemicals, lead (Pb) can cause detriment health effects to animals, plants, and even humans through different exposure pathways such as atmosphere, soil, food, water, and dust, etc. Sentinel animals played an “indicative” role in the researches of environmental pollution monitoring and human health. In order to comprehend the usage of sentinel animals in the indication of environmental Pb pollution and human Pb exposure completely, a combination of traditional review and visualization analysis based on CiteSpace literature was used to review earlier researches in this study. In the first instance, present researches on exposure sources and exposure pathways of Pb were summarized briefly, and then the studies using sentinel animals to monitor environmental heavy metal pollution and human health were combed. Finally, visualization software CiteSpace 5.8.R3 was used to explore and analyze the hotspots and frontiers of lead exposure and sentinel animals researches at home and abroad. The results showed that certain mammals were good indicators for human lead exposure. Sentinel animals had been widely used to monitor the ecological environment and human lead exposure. Among them, the blood lead levels of small mammals, particularly for domestic dogs and cats, had a significant correlation with the blood lead levels of human living in the same environment. It indicated that certain biological indicators in animals can be used as surrogates to monitor human body exposure to heavy metals. This study also explored the challenges and perspectives that may be faced in sentinel animal research, in order to provide a certain theoretical basis and train of thought guidance for future research.
Full-text available
Lead poisoning, mainly through incidental ingestion of lead ammunition in carcasses, is a threat to scavenging and predatory bird species worldwide. In Australia, shooting for animal control is widespread, and a range of native scavenging species are susceptible to lead exposure. However, the prevalence of lead exposure in Australia's scavenging and predatory birds is largely unknown. We evaluated the degree to which the Tasmanian wedge-tailed eagle (Aquila audax fleayi), an endangered Australian raptor and facultative scavenger, showed evidence of lead exposure. We detected lead in 100% of femur and liver tissues of 109 eagle carcasses opportunistically collected throughout Tasmania between 1996 and 2018. Concentrations were elevated in 10% of 106 liver (> 6 mg/kg dw) and 4% of 108 femur (> 10 mg/kg dw) samples. We also detected lead in 96% of blood samples taken from 24 live nestlings, with 8% at elevated concentrations (> 10 μg/dL). Of the liver samples with elevated lead, 73% had lead207/206 isotope ratios within the published range of lead-based bullets available in Tasmania. These first comprehensive data on lead exposure of an Australian raptor are comparable to those for raptor studies elsewhere that identify lead-based ammunition exposure as a conservation threat. Our findings highlight the importance of further research and efforts to address lead contamination throughout the Tasmanian ecosystem and in other Australian regions. This article is protected by copyright. All rights reserved.
Full-text available
The following species of sedentary birds with widespread and common occurrence are the most convenient as bioindicators: Magpie Pica pica, Feral Pigeon Columba livia f. domestica, House Sparrow Passer domesticus or Tree Sparrow Passer montanus, Blackbird Turdus merula, Goshawk Accipiter gentilis (feathers) and nestlings of various species. The non-destructive method of feather analysis is suitable mainly for assessment of Pb, Cd, As, Sb, Ge, Tl, and Hg. It cannot be applied for Mn, Ni, Sr, Rb, Mo and Fe that are cumulated in feathers at similar levels in polluted and unpolluted areas. Hg, Zn, Cu, Cr, As and Se have stronger affinity to keratin than others. The method requires strict standardisation, particularly in the way samples are to be collected and prepared for mineralisation. None of feather cleaning procedures removes all contaminants from vane surfaces. With respect to many elements, analysing 'concentration in feathers' is a measurement of external deposition therefore metal levels found in feathers correspond more strongly to the data on immission than to the element pool available in food. Mercury is an exception here. In cases of toxic elements as Pb, Cd or Tl it is possible to predict their concentrations in internal tissues on the basis of feather analysis.
Full-text available
Accumulation of heavy metals (chromium, lead, arsenic, nickel, copper, and manganese) in the bones, food, and feces of 24 bird species in the southwest of Russia, the Rostovskaya oblast and Kalmykia, was studied. Differences in the lead accumulation in the bones of terrestrial and aquatic birds, as well as in the arsenic accumulation in the bones of birds belonging to different trophic levels, were demonstrated. An inverse linear relation between the lead concentration in bird bones and the body mass was found. Heavy metal content in the food (earthworms) and excrement of rooks from suburban and urban colonies are discussed. Worms and rook excrement from urban habitats are more polluted with heavy metals.
Birds as Monitors of Environmental Change looks at how bird populations are affected by pollutants, water quality, and other physical changes and how this scientific knowledge can help in predicting the effects of pollutants and other physical changes in the environment.
Several authors of books on the monitoring of pollution have advocated the use of animals as monitors in terrestrial and aquatic environments (e.g. Phillips, 1980; Schubert, 1985). Such studies tend to emphasize the use of sedentary invertebrate animals as biomonitors. By comparison, birds suffer from several apparent drawbacks. They are mobile, so pollutants will be picked up from a wide, often ill-defined, area; they are long-lived, so pollutant burdens may be integrated in some complex way over time; and they have more complex physiology, and so may regulate pollutant levels better then invertebrates. Furthermore, birds tend to be more difficult to sample, and killing birds may be unacceptable for conservation or ethical reasons. However, some of these characteristics may at times be positively advantegeous. Integrating pollutant levels over greater areas or timescales or over food webs, may be useful, provided that species are chosen carefully. Less sampling may be necessary if birds can reflect pollutant levels in the whole ecosystem or over a broad area. In addition, since they are high in food chains, birds may reflect pollutant hazards to humans better than do most invertebrates. It is also significant that birds are extremely popular animals with the general public, so pollutant hazards to them are likely to receive greater attention than threats to invertebrates.
Concentrations of heavy metals and selenium were measured in the blood of adult and young herring (Larus argentatus) and Franklin's (Larus pipixcan) gulls collected during the same breeding season in colonies in the New York Bight and in northwestern Minnesota, respectively. Concentrations were expected to be higher in young herring gulls collected in an urban, industrialized area, compared to young Franklin's gulls collected in a relatively pristine prairie marsh. Exposure is similar for the fledgling and adult gulls because by the time the blood of young gulls is drawn both adults and young have been eating foods from the surrounding region for two months; leading to the prediction that metal levels should be similar in adults and young. However, young Franklin's gulls had significantly higher levels of arsenic, cadmium, and manganese than adults; adults had significantly higher levels of mercury and selenium. Young herring gulls had significantly higher concentrations of arsenic and selenium, but lower levels of lead than adult herring gulls. Interspecific comparisons indicated that young Franklin's gulls had significantly higher levels of cadmium than young herring gulls, and adult Franklin's gulls had higher levels of selenium and chromium than adult herring gulls, but for all other comparisons herring gulls had higher levels of metals in their blood. Young herring gulls chicks had higher arsenic, manganese, and selenium levels and lower cadmium and lead levels in 1993 than in 1994. Overall, the levels in the two species were usually within an order of magnitude.
This study investigated sub-lethal effects and detoxification processes activated in free-ranging Red Knots (RKs) (Calidris canutus) from the Pertuis Charentais on the Atlantic coast of France, and compared the results with previous data obtained on another shorebird species, the Black-tailed Godwit (Limosa limosa). The concentrations of 13 trace elements (Ag, As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, Zn) were assessed in the liver, kidneys, muscle and feathers. Stable isotope analyses of carbon and nitrogen were carried out to determine whether differences in diet explained variations in elemental uptake. The mRNA expression of relevant genes (cytochrome c oxidase 1, acetyl-CoA carboxylase, Cu/Zn and Mn superoxide dismutase, catalase, metallothionein, malic enzyme), antioxidant enzyme activities (catalase, glutathione peroxidase (GPx), superoxide dismutase), and metallothionein (MT) levels were investigated to shed light on trace element detoxification and toxic effects. Although Red Knots were characterized by elevated As and Se concentrations which were potentially toxic, most elements were usually below toxicity threshold levels. The results strongly suggested a dietary specialization of Red Knots, with individuals feeding on higher trophic status prey experiencing higher As, Hg and Se burdens. Red Knots and Godwits also showed discrepancies in elemental accumulation and detoxification processes. Higher As and Se concentrations in Red Knots enhanced catalase gene expression and enzyme activity, while Godwits had higher Ag, Cu, Fe and Zn levels and showed higher MT production and GPx activity. The results strongly suggest that detoxification pathways are essentially trace element- and species-specific.
Although toxic chemicals constitute a major threat for wildlife, their effects have been mainly assessed at the individual level and under laboratory conditions. Predicting population-level responses to pollutants in natural conditions is a major and ultimate task in ecological and ecotoxicological research. The present study aims to estimate the effect of mercury (Hg) levels on future apparent survival rates and breeding performances. We used a long-term data set (;10 years) and recently developed methodological tools on two closely related Antarctic top predators, the South Polar Skua Catharacta maccormicki from Ade´ lie Land and the Brown Skua C. lonnbergi from the Kerguelen Archipelago. Adult survival rates and breeding probabilities were not affected by Hg levels, but breeding success in the following year decreased with increasing Hg levels. Although South Polar Skuas exhibited much lower Hg levels than Brown Skuas, they suffered from higher Hg-induced breeding failure. This species difference could be attributed to an interaction between Hg and other environmental perturbations, including climate change and a complex cocktail of pollutants. By including Hg-dependent demographic parameters in population models, we showed a weak population decline in response to increasing Hg levels. This demographic decline was more pronounced in South Polar Skuas than in Brown Skuas. Hence, Hg exposure differently affects closely related species. The wide range of environmental perturbations in Antarctic regions could exacerbate the demographic responses to Hg levels. In that respect, we urge future population modeling to take into account the coupled effects of climate change and anthropogenic pollution to estimate population projections.