Environmental Pollution(SeriesA) 22 (1980) 207-217

METAL C O N T A M I N A T I O N OF FERAL PIGEONS

COLUMBA LIVIA FROM THE L O N D O N AREA: PART I - -
TISSUE A C C U M U L A T I O N OF LEAD, C A D M I U M A N D
ZINC

M. HUTTON*& G. T. GOODMAN'["

Department of" Applied Biology, Chelsea College, University of London, Great Britain

ABSTRACT

This study investigated the variation of lead and cadmium contamination in urban-
dwellingferal pigeons. Tissue lead concentrations in three populationsfrom London
inct~eased progressively with proximit)' to the city centre, where markedll' elevated
values were recorded and where females contained higher bone levels than males. No
organolead was detected in an)' of the tissues examined. The cadmium content of"
central London birds was also greater than in the suburban sample, but birds from the
outer urban site, Heathrow Airport, also contained elevated cadmium; aircraft were
considered as a possible source of this contamination. The differences in tissue metal
content between populations corrc,sponded to the levels encountered in the intestine
contents; b)' feeding at ground level the .speciek is probably ingesting /hod
contaminated with roadside dust.
Lead and cadmium toxicity in this species was discussed in relation to the possible
antagonist&' role of :int'.
The ability of an urban-dwelling organism tO accumulate elevated lead
concentrations draws attention to the potential hazard of children ingesting street
dust fi'om such areas. It is suggested that theferal pigeon ma)' be used both to monitor
urban lead contamination and as a model for chronic lead toxicity.

INTRODUCTION

The use of alkyl lead compounds as anti-knock agents in petrol is a major source of
lead in the urban environment (NAS, 1972). High traffic densities in urban areas
have been associated with increasing lead concentrations in urban aerosols and
* Present address: Monitoring and Assessment Research Centre, Chelsea College, University of London,
London, Great Britain.
"t"Present address: Beijer Institute, The Royal Swedish Academy of Sciences, Fack S-104-05 Stockholm,
Sweden.
207
Era,iron. Polhtt. Ser. A. 0143-1471/80/0022-0207/$02"25 ~' Applied Science Publishers Ltd, England, 1980
Printed in Great Britain
208 M. HUTTON, G. T. GOODMAN

roadside dusts with proximity to the centre of a city (NAS, 1972; Duggan &
Williams, 1977). Similarly, elevated cadmium levels in air and dust of urban areas
(Friberg et al., 1974) may be associated with motor vehicles, as cadmium is present
in tyres (Lagerwerff & Specht, 1970). The significance of this contamination to
urban-dwelling humans is a matter of continuing concern, and attention has
recently been paid to the risks from ingesting lead-rich street dusts, especially by
children (Duggan & Williams, 1977). There is, however, little information with
regard to the biological availability of lead from this source. Furthermore, although
most of the alkyl lead in petrol is decomposed during combustion, small amounts
of these toxic compounds have been detected in particulates from urban areas
(Harrison & Laxen, 1977),
The present study examined the levels of lead, cadmium and zinc in tissues of three
feral pigeon, Columba livia, populations, residing at differing distances from the
centre of London. In urban areas this species is sedentary, forming discrete flocks
which remain faithful to specific feeding and roosting areas (Murton et al., 1972).
For this reason, a relatively small sample of birds is expected to reflect any variation
in metal exposure at the local level. The possible hazard of residual organolead
contamination in the urban environment was evaluated by attempting to detect
these compounds in selected pigeon tissues. Finally, the dietary intake of metals was
assessed in two London populations and related to the tissue levels encountered in
these birds.

MATERIALS AND METHODS

Sample collection
Pigeons were sampled at Chelsea, London SW10, Mortlake, London SWI4 and
Heathrow Airport, Middlesex. These were located, respectively, 4 km, 8 km and
18 km from the centre of London and represented a central, a suburban and an outer
urban location. Control birds were obtained from rural Cambridgeshire at a site
removed from metal contamination. Urban pigeons were caught using a wire mesh
trap, placed on a suitable flat roof and pre-baited for between one and two weeks.
In the laboratory, blood samples were collected in heparinised tubes by
puncturing the alar vein in the region of the carpal joint, after first removing feathers
in the area and thoroughly cleaning the skin. Birds were then killed by cervical
dislocation and the liver, kidneys, brain and tibiotarsus were excised, precautions
being taken to prevent metal contamination. The gizzard and intestine contents of
pigeons from Chelsea and Heathrow were also retained for metal analysis.

Sample analysis
With the exception of blood, tissue samples were freeze-dried and then wet-
digested using a concentrated nitric/perchloric acid mixture (4:1 v/v), the normal
 METAL ACCUMULATION IN PIGEONS 209

precautions to avoid explosive digestion being taken. After appropriate dilution,

digestions were analysed for lead, cadmium and zinc by flame atomic absorption
spectrophotometry. Background correction for non-atomic absorption was carried
out with a hydrogen continuum lamp. Calibration curves were prepared from
standards of similar acid strength to sample digests.
Blood-lead levels were determined with an ESA 2014 Anodic Stripping
Voltammeter (Matson et al., 1965). Replicate 200 t~1 blood samples were digested
in pyrex cells with 400 ~L1of a concentrated nitric/perchloric acid mixture (1 : 1).
After cooling, 5 ml of double distilled water were added to the digest and the cells
were placed on the module assembly. Plating and stripping steps were then
performed in the manner recommended by the makers. Standard lead solutionswere
used to calibrate the module. The sensitivity of the method employed was estimated
at 3/~g/100ml for a 200/A sample of blood.
A qualitative technique for the detection of organolead compounds was used,
based on a method devised by Potter (1976). Only the presence of di- and trialkyl
lead was investigated, as tetraethyl lead is unstable in animal tissues (Cremer, 1965).
Liver, kidney and brain samples were initially homogenised with double distilled
water then excess lead nitrate added; this has the effect of releasing organic lead from
complexing sites. The homogenate was then filtered and 2 M sodium hydroxide
added to pH 8, precipitating inorganic lead. The filtrate from this step was freeze-
dried, dissolved in acetone and spotted on to 'alumina' thin layer chromatography
plates, together with samples ofdi- and trialkyl lead salts. Plates were eluted with 5 ~o
acetic acid in benzene and then sprayed with 0.1 ~ dithizone. Dialkyl lead salts
produced a salmon-red spot nearest the origin, while nearer to the solvent front,
trialkyl salts gave a yellow spot. This method allowed the detection of 1 #g of both di-
and trialkyl lead.
Tissue metal values from different locations exhibited skewed distributions but
logarithmic transformation sufficiently normalised the data. Bartlett's Fro,Xtest was
used to evaluate the equality of group variance of the transformed data before
proceeding with one-way analysis of variance. Individual means were then
compared by the method of least significant difference.

RESULTS

Tissue lead
Concentrations of tissue lead conformed to the order Chelsea > Mortlake >
Heathrow > Controls, with the exception of blood, where differences between
Heathrow and control birds showed no statistical difference (Table 1).
These results show a trend of increasing tissue lead content with proximity to the
centre of London, where levels were markedly elevated. At Chelsea, the highest lead
concentration in the kidney was 1448/~g/g and in bone 1703/ag/g. Highest mean
210 M. HUTTON, G. T. GOODMAN

values were found in the bone, followed by the kidney, then liver and, finally, brain,
corresponding tO the distribution patterns recorded in humans (Barry & Mossman,
1970) and roadside-dwelling small mammals (Mierau & Favara, 1975).
Lead concentrations in bone tissue of female pigeons from Chelsea were
significantly (p < 0.01) higher than in males from this central London location
(Table 2). Although female pigeons from the other London sites also contained
higher bone lead concentrations than males, the difference was not statistically
significant.
Neither di- nor trialkyl lead compounds were detected in any tissues analysed for
organolead. These were: five kidneys with lead values up to 1068/~g/g, five livers with
a maximum of 46.5/~g/g and four brains with up to 22.8~g/g.
TABLE 1
TISSUE LEAD CONCENTRATIONS OF FERAL PIGEONS FROM URBAN AND CONTROL AREAS
(Mean + standard error; sample size in parentheses)

Site Lead in tissue (l~g/g dry weight: blood l~g/lOOml)

Brain Blood Liver Kidney Bone

Chelsea 12.0 + 1.00 ° I01.1 ___ 13.2 ~ 21.6 ___ 1.9.5" 321.4 + 45.3 ° 669"2 + 45-5 °
(20) (I 7) (53) (64) (41)
Mortlake 6.33 _+ 1.12 b 45.2 __ 10.3 ~ 10.1 __ 2.36 b 48-7 __ 17.5 b 281-8 __. 73.7 b
(13) (7) (15) (15) (15)
Heathrow 3.34 __ 0.29' 16.2 _+ 5.50 c 6.11 _+ 1.09 c 9.87 __ 2.60 ~ 107-9 + 27.5 ~
(15) (10) (15) (15) (15)
Controls nd 19.0 __ 2,60 c 2.01 _+ 0 . 2 ~ 4-34 +_ 1.26; d 5.73 +_ 1.05 ~
( I 0) (10) (7) (7)

nd, not determined.

Dissimilar superscripts denote statistical differences at p < 0'05 within vertical columns.

TABLE 2
BONE LEAD AND ZINC CONCENTRATIONS IN FERAL PIGEONS FROM THREE LONDON SITES,
SUBDIVIDED ACCORDING TO SEX
(Mean + standard error; sample size in parentheses)

Site Metal in bone (#g/g dry weight)

Lead Zinc
Females Males Females Males

Chelsea 868-2 + 99.6 566.9 __ 41.8* 218.7 __ 10.4 188.9 __ 5.04*

(12) (29) (12) (29)
Mortlake 349.6 + 118.4 224.4 _+ 53.6 144.2 + 13.1 160.7 _ 14.9
(7) (8) (7) (8)
Heathrow 134.4 + 44.9 77.6 _+ 28-5 186.3 _+ 32.9 143.5 _+ 13.4
(8) (7) (8) (7)

* denotes statistical significance of sex difference at p < 0-01, as shown by Student's t test.

Tissue cadmium
The distribution of cadmium between kidney, liver and brain of London pigeons is
summarised in Table 3. Brain cadmium was not measured in controls and levels in
the other tissues of this group were excluded from statistical analysis because of
small sample sizes.
 METAL ACCUMULATION IN PIGEONS 211

TABLE 3
TISSUE CADMIUMCONCENTRATIONSOF FERAL PIGEONS FROM URBAN AND
CONTROL AREAS
(Mean _ standard error; sample size in parentheses)

Site Cadmium in tissue (ltg/g dry weight)

Brain Liver Kidney

Chelsea 0-19 + 0.02* 2.45 4- 0.28" 12-3 + 2-05*

(20) (43) (41)
Mortlake 0-14 + 0.02* 0.40 4- 0-07 b 1"52 + 0'31 b
(13) (15) (15)
Heathrow 0.47 4- 0.03 b 9-48 4- 3'15" 50.7 _+ 22.7*
(15) (15) (15)
Controls nd 0.54 4- 0-05 1-75
(5) (2)

nd, not determined.

Dissimilar superscripts denote statistical differences at p < 0.001 within
vertical columns.

Brain cadmium concentrations were similar at Chelsea and Mortlake but both
were significantly (p < 0.001) lower than those at Heathrow. Kidney and liver
cadmium levels at Mortlake were also lower (p < 0.001) than at both Chelsea and
Heathrow; values at the latter sites were statistically similar.
The higher renal and hepatic cadmium concentrations at Chelsea compared with
suburban Mortlake indicates that, as with lead, there is also an increased cadmium
exposure at central London. In contrast to the lead results, however, cadmium
concentrations in the brain were uniformly low at both locations and thus did not
reflect the differential body burdens of the metal at these sites.
The most noticeable difference between the results of lead and cadmium analyses
was the elevated cadmium status of birds from the outer urban location, Heathrow.
Indeed, despite the limited uptake of cadmium by cerebral tissue, the mean brain
value at this location was over three times that at Mortlake. Some birds from
Heathrow contained very high cadmium residues, maximum renal and hepatic
values were, respectively, 302-4 and 34.2/~g/g. However, although the mean liver and
kidney cadmium concentrations at Heathrow were more than three times those at
Chelsea, the differences were not statistically significant. This was because of the
great variability in tissue levels at Heathrow, with six birds from this site containing
kidneY[Ca_d.miumconcentration of less than 2 lag/g.
Highest cadmium levels were found in kidney, followed by liver and, lastly, brain;
a similar distribution pattern is present in humans (Friberg et al., 1974) and seabirds
(Hutton, 1979). In contrast to lead, the cadmium content did not vary significantly
between tissues at any of the London sites when subdivided according to sex.

Tissue zinc
In contrast to lead and cadmium, brain zinc levels were similar at all London
locations, while values in other tissues showed more limited concentration ranges
(Table 4). These differences reflect the essential nature of zinc, with homeostatic
212 M. HUTTON, G. T. GOODMAN

TABLE 4
TISSUE ZINC CONCENTRATIONSOF FERAL PIGEONS FROM URBAN AND CONTROL AREAS
(Mean 4. standard error; sample size in parentheses)

Site Zinc in tissue (ltg/g dry weight)

Brain Lioer Kidney Bone

Chelsea 53.9 4- 2.72* 146-5 4- 8 . 3 ~ 168.8 4- 5.87~ 197-7 4- 5'08*

(20) (36) ,~b (44) (41)
Mortlake 53.4 4- 5.47* 78-8 ~ o.~o 101.8 4- 12-8 b 153-0 4- 9-9 b
(13) (15) (15) (15)
Heathrow 61.1 4- 1.71" 238-6 4- 36"2 c 183.0 4- 28-8* 166-3 4- 18.9 b
(15) (15) (15) (15)
Controls N 203.9 + 31.9"" 190.5 + 18.9" 157.7 4. 5.8 b
(10) (7) (7)
nd, not determined.
Dissimilar superscripts denote statistical differences at p < 0"01 within vertical columns.

mechanisms maintaining tissue levels (Fisher, 1975). Nevertheless, mean liver and
kidney zinc values in London birds corresponded to the cadmium status of these
populations, with highest concentrations of both metals at Heathrow, followed by
Chelsea and, lastly, Mortlake. Controls did not, however, conform to this pattern
and although cadmium levels were low in this group, liver and kidney zinc values
were similar to those at Chelsea.
Bone zinc concentrations at Mortlake, Heathrow and in control birds were
statistically similar and were all lower (p < 0-001) than at Chelsea. Unlike soft
tissues, zinc in bone corresponded to the lead status of the study populations, with
the highest values of both metals at Chelsea. There was also a significant correlation
between lead and zinc in bone, at both Chelsea (r39 = 0.484; p < 0.01) and
Mortlake (r13 = 0.626; p < 0-05). Additionally, as Table 2 shows, only female
pigeons from Chelsea contained greater concentrations of zinc in bone as well as
lead compared with males.

Metals in gut contents

Levels of both lead and cadmium in gizzard contents were similar at Chelsea and
Heathrow (Table 5). There was also no difference between zinc values in either the
gizzard or intestine contents of the two populations.
Lead concentrations in the intestine contents of birds from Chelsea were ten times
greater than those at Heathrow, while the mean bone lead value was six times higher
TABLE 5
METALCONCENTRATIONS(/~g/g dry weight) OF FERALPIGEONGIZZARDAND INTESTINECONTENTSFROMTWO
LONDON SITES
(Mean 4. standard error; sample size in parentheses)

Site Lead Cadmium Zinc

Gizzard Intestine Gizzard Intestine Gizzard Intestine

Chelsea (10) 5.60 _ 1'61 22.2 4- 7.01 0.31 4- 0.07 0.82 4- 0.10 44"4 4- 8.5 171.2 4- 13.8
Heathrow ( l l ) 8.84 4- i.84 2.09 ± 0.58 0'52 4. 0"08 2"19 4. 0"75 39"2 4. 8.2 180-9 ± 34-4
 METAL ACCUMULATION IN PIGEONS 213

at this central London site. Although cadmium concentrations in the intestine

contents were generally much lower than lead, the mean value at Heathrow was three
times that of Chelsea. This corresponded to the fourfold higher renal cadmium value
in birds from the outer London location. Additionally, in Heathrow birds there was
a significant correlation ( r 9 ----0.76; p < 0.01) between the concentration of
cadmium in the intestine contents and that in the kidney.

DISCUSSION

The results of this study indicate that the lead content of feral pigeon populations
increases with proximity to the centre of London. Such a gradient was found not
only in the 'concentrator' organs, bone and kidney, but also in the brain, a tissue
usually considered to possess a low affinity for the metal. Average tissue
concentrations in birds from outer London were relatively low and generally about
half those in suburban pigeons. Brain, liver, blood and bone lead levels at the central
location, Chelsea, were, in turn, twice those at Mortlake while the kidney value was
six times higher. Indeed, the tissue concentrations in these birds are some of the
highest recorded in a free-living vertebrate, being much greater than in either
roadside populations of small mammals (Mierau & Favara, 1975), or in urban-
dwelling rats Rattus norvegicus (Mouw et al., 1975). When compared with humans,
blood lead levels in birds from outer London and in controls from Cambridgeshire
fall within the range reported for rural populations (Goldwater & Hoover, 1967). In
contrast, values in both suburban and central London pigeons were far in excess of
those quoted for human urban dwellers and those from the latter site were greater
than levels in occupationally exposed workers (Cooper et al., 1972).
The feral pigeon's habit of feeding at ground level, on pavements and in the
gutters of roads, offers an explanation for the very high lead content of birds from
central London. Food items taken from such locations are expected to be
contaminated with the lead-rich dusts of urban areas (Duggan & Williams, 1977).
Certainly, relatively high lead concentrations were present in the intestinal contents
of central London samples and, although the importance of dietary lead uptake was
not quantified, levels in the intestinal contents also reflected the degree of
contamination in two of the London populations. Small stones, taken up for
digestive purposes in the gizzard, could be an important source of contamination,
butany metal-rich dust adhering to these stones may already have been absorbed in
the digestive process. Additionally, the contribution from respiratory lead uptake
may be of greater significance than it is in humans (Chamberlain et al., 1978), since
avian species consume relatively more oxygen than humans, especially during flight
(Altman & Dittmer, 1974; LeFebvre, 1964).
The tissue lead gradient observed in urban pigeon populations is presumably
associated with an increasing degree of lead exposure with proximity to the centre of
London. A similar gradient has been reported for lead in both city air (NAS, 1972)
and in London street dusts (Duggan & Williams, 1977). However, another study
214 M. HUTTON, G. T. GOODMAN

detected no increase in dust lead levels with proximity to a city centre (Day et al.,
1975). Although there is no evidence to support the suggestion, it is possible that
there are actually increased quantities of street dusts in areas nearer the city centre.
If this is so, then the ingestion of more lead by central London pigeons may occur
because their food is contaminated with greater amounts of lead-rich dust rather
than dust with a higher lead concentration.
Despite the feral pigeon's intimate association with the primary source of urban
lead contamination, no organolead was detected in the three tissues examined.
Apparently, these compounds are too unstable, or ambient levels are too low, to
allow accumulation in this species. Nevertheless, it has recently been claimed that
trialkyl lead is present in the brain tissue of urban-dwelling humans (Nielsen et al.,
1978), albeit at very low concentrations and below the detection limit of the method
employed in the present study.
Female pigeons from central London contained greater bone lead concentrations
than males; a similar finding was reported in mallard dosed with lead shot (Finley et
al., 1976). This sex difference is probably associated with the increased calcium
requirement during eggshell formation, as Finley et al. also noted a positive
correlation between the bone lead levels of female mallard and number of eggs laid.
The intestinal absorption of calcium is related to parathyroid hormone action (Wills
et al., 1970); in avian species there is a marked increase in absorption during eggshell
formation (Hurwitz & Bar, 1965). Conceivably, intestinal lead absorption in female
pigeons is also greater at this time, as treatment of lead-dosed rats with parathyroid
hormone also increased uptake of this metal (Mouw et al., 1978). The medullary
bone, a labile structure located within skeletal bone, also acts as a source of calcium
that is rapidly mobilised during eggshell formation (Simkiss, 1975). Enhanced lead
retention by structural bone in female pigeons may thus result from a competitive
effect between lead and calcium at the time of increased calcium mobilisation during
medullary bone formation and destruction.
Evidence arising primarily from central London pigeons indicates that zinc co-
accumulates with lead in the bone tissue of urban pigeons. This apparent association
is not thought to be related to any differences in dietary zinc intake, as zinc levels of
the gut contents were similar in the two London populations examined. At present it
is not known whether this co-accumulation reflects an interaction of toxicological
significance. Zinc has been shown to antagonise lead toxicity by reducing tissue lead
accumulation and by reactivating lead-inhibited ALA-D, an enzyme involved in
haem synthesis (El-gazzar et al., 1978; Hutton, 1979). A competitive interaction
between the two metals in bone may also arise during egg formation, as bone
calcium mobilisation at this time is closely related to alkaline phosphatase activity
(Ojanen et al., 1975). This is a zinc metallo-enzyme (Fisher, 1975), known to be
inhibited in lead poisoning (Vallee & Ulmer, 1972). A fortuitous co-accumulation
cannot be ruled out, however, and increased zinc retention, as well as lead, may
simply result from active bone metabolism during egg formation. The marked
 METAL ACCUMULATION IN PIGEONS 2 !5

increases in bone zinc levels of female house sparrows Passer domesticus during
medullary bone formation and egg laying (Ojanen et al., 1975), together with the
experimental evidence of bone lead accumulation in mallard (Finley et al., 1976),
support this suggestion.
The cadmium content of Chelsea pigeons was greater than in suburban samples,
indicating that there is a moderate degree of cadmium contamination in central
London. Further, cadmium exposure in suburban areas is apparently minimal, as
tissue concentrations in birds from Mortlake were similar to those of rural controls.
The elevated cadmium levels in several birds from Heathrow do, however, suggest
the presence of an appreciable degree of cadmium contamination at this site. In
accord with this possibility, Harrison et al. (1975) found that rainwater collected at
Heathrow Airport contained six times more cadmium than samples from central
London. The source of this apparent contamination is not clear at present, but
aircraft may be implicated, as the metal is used in their engines and bodywork. It is
conceivable that cadmium is released as a result of wear on the aircraft or it may
originate from the severe tyre erosion which occurs during landing and takeoff.
Whatever the source of cadmium at Heathrow, levels of the metal in food, like
tissue values, indicate that the degree of exposure at this site is greater than in central
London. Further evidence for a close association between the cadmium status of
pigeons and dietary intake of the metal was also noted at Heathrow, where there was
a correlation between cadmium concentrations in the kidney and intestine contents.
The restricted uptake of cadmium by brain tissue may be associated with the
selective retention of cadmium in the kidney as, in this species, a large proportion of
renal cadmium, but no lead, is bound to a protein with many of the properties of
metallothionein (Hutton, 1979). Chelation of cadmium to metallothionein probably
prevents cadmium-induced toxicity by removal from biological turnover; this would
also explain the metal's localised tissue distribution.
The apparent association between zinc and cadmium in the kidney and liver of
urban pigeons is thought to be a reflection of the interaction which is known to occur
between these two metals (Friberg et al., 1974). The co-accumulation of tissue
cadmium and zinc has also been reported in horses, humans (Friberg et al., 1974),
seabirds (Hutton, 1979) and cadmium-dosed rats (Stonard & Webb, 1976). Zinc
administration has been shown to antagonise a number of toxic effects of cadmium,
including testicular necrosis and tumour formation (Parizek, 1957, Gunn et al.,
1963), and cadmium-induced toxic effects have been linked to an increase in the
cadmium-to-zinc ratio in the kidney (Schroeder et al., 1967). The protective effect of
zinc is thought to be partly related to the induction of an enhanced synthesis of
metallothionein, to which both metals bind, and partly based on a competition for
various ligand sites in target tissues. It is suggested that in view of the importance of
zinc in determining the toxicity of cadmium, the relationship between these two
metals be examined when assessing the significance of cadmium contamination in an
environmentally exposed organism.
216 M. HUTTON, G. T. GOODMAN

CONCLUSIONS

This study has shown that feral pigeons from an urban environment can accumulate
elevated lead concentrations. It is concluded that this finding illustrates the
propensity for bioaccumulation of petrol-derived lead and this draws attention to
the potential hazard of children ingesting dust in urban areas. The ability of feral
pigeons to accumulate high metal concentrations is considered to be a desirable
characteristic in an indicator organism and this would facilitate periodic monitoring
of lead contamination in the urban environment. Similarly, the presence of a
moderate but biologically available cadmium contamination in urban areas can be
monitored by using this species. Finally, examination of the biological impact of
lead exposure upon urban pigeons is expected to be of more relevance in assessing
the implications of low level chronic lead contamination than certain laboratory
studies in which high doses are administered over short time periods.

ACKNOWLEDGEMENT

We wish to acknowledge the financial support provided by the Natural

Environment Research Council.

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