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Metal contamination of feral pigeons Columba livia from the London area: Part 1—tissue accumulation of lead, cadmium and zinc
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 urbandwellingferal 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
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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 wetdigested 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 freezedried, 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 diand 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
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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) Blood Liver Kidney
Brain Chelsea
12.0 + 1.00 ° (20) 6.33 _+ 1.12 b (13) 3.34 __ 0.29' (15) nd
Mortlake Heathrow Controls
I01.1 ___ 13.2 ~ (I 7) 45.2 __ 10.3 ~ (7) 16.2 _+ 5.50 c (10) 19.0 __ 2,60 c ( I 0)
21.6 ___ 1.9.5" (53) 10.1 __ 2.36 b (15) 6.11 _+ 1.09 c (15) 2.01 _+ 0 . 2 ~ (10)
321.4 + 45.3 ° (64) 48-7 __ 17.5 b (15) 9.87 __ 2.60 ~ (15) 4-34 +_ 1.26; d (7)
Bone 669"2 + 45-5 ° (41) 281-8 __. 73.7 b (15) 107-9 + 27.5 ~ (15) 5.73 +_ 1.05 ~ (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 Females Chelsea Mortlake Heathrow
Metal in bone (#g/g dry weight) Lead Zinc Males Females
868-2 + 99.6 (12) 349.6 + 118.4 (7) 134.4 + 44.9 (8)
566.9 __ 41.8* (29) 224.4 _+ 53.6 (8) 77.6 _+ 28-5 (7)
218.7 __ 10.4 (12) 144.2 + 13.1 (7) 186.3 _+ 32.9 (8)
Males 188.9 __ 5.04* (29) 160.7 _ 14.9 (8) 143.5 _+ 13.4 (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.
211
METAL ACCUMULATION IN PIGEONS TABLE 3 TISSUE CADMIUMCONCENTRATIONSOF FERAL PIGEONS FROM URBAN AND CONTROL AREAS (Mean _ standard error; sample size in parentheses)
Site Chelsea Mortlake Heathrow Controls
Cadmium in tissue (ltg/g dry weight) Brain Liver Kidney 0-19 + 0.02* (20) 0-14 + 0.02* (13) 0.47 4- 0.03 b
2.45 4- 0.28" (43) 0.40 4- 0-07 b (15) 9-48 4- 3'15"
12-3 + 2-05* (41) 1"52 + 0'31 b (15) 50.7 _+ 22.7*
(15)
(15)
(15)
nd
0.54 4- 0-05 (5)
1-75 (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 Brain Chelsea
Zinc in tissue (ltg/g dry weight) Lioer Kidney
Mortlake
53.9 4- 2.72* (20) 53.4 4- 5.47*
(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) Controls
N
146-5 4- 8 . 3 ~ (36) ,~b 78-8 ~ o.~o
(15) 203.9 + 31.9""
(10)
168.8 4- 5.87~ (44) 101.8 4- 12-8 b
Bone 197-7 4- 5'08* (41) 153-0 4- 9-9 b
(15)
(15)
190.5 + 18.9"
157.7 4. 5.8 b
(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
Chelsea (10) Heathrow ( l l )
Lead Gizzard
Intestine
5.60 _ 1'61 8.84 4- i.84
22.2 4- 7.01 2.09 ± 0.58
Cadmium Gizzard Intestine 0.31 4- 0.07 0'52 4. 0"08
0.82 4- 0.10 2"19 4. 0"75
Zinc Gizzard 44"4 4- 8.5 39"2 4. 8.2
Intestine 171.2 4- 13.8 180-9 ± 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 urbandwelling 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
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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 coaccumulates 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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HARRISON, R. M., PERRY, R. & WELLINGS, R. A. (1975). Lead and cadmium in precipitation: Their contribution to pollution. J. Air Pollut. Control Ass., 25, 627-30. HURWITZ, S. & BAR, A. (1965). Absorption of calcium and phosphorous along the gastrointestinal tract of the laying fowl as influenced by dietary calcium and eggshell formation. Y. Nutr., 86, 433-8. HUTTON, M. (I 979). An experimental survey of the impact of heavy metals on selected species of birds from contaminated environments. PhD thesis, University of London. LAGERWERFF, J. V. & SPECHT, A. W. (1970). Contamination of roadside soil and vegetation with cadmium, nickel, lead and zinc. Environ. Sci.& Technol., 4, 583-6. LEFEBVRE,E. A. (1964). The use of D 2 0 la for measuring energy metabolism in Columba livia at rest and in flight. Auk, 81,403-16. MATSON, W. R., ROE, D. K. & CARRITT,D. E. (1965). Composite graphite-mercury electrode for anodic stripping voltammetry, Analyt. Chem., 37, 1594-5. MIERAU, G. W. & FAVARA,B. E. (1975). Lead poisoning in roadside populations of deer mice. Environ. Pollut., 8, 55-64. Mouw, D. R., KALITIS, K., Anver, M., SCHWARTZ, J., CONSTAN, A., HARTUNG, R., COHEN, B. & RINGLER, D. (1975). Lead: Possible toxicity in urban versus rural rats. Arch. environ. Hlth, 30, 276-80. Mouw, D. R., WAGNER, J. G., KALITIS, K., VANDER, A. J. & MAJOR, G. H. (1978). The effect of parathyroid hormone on the renal accumulation of lead. Environ. Res., 15, 20-7. MURTON, R. K., THEARLE,R. J. P. & THOMPSON,J. (1972). Ecological studies of the feral pigeon Columba livia var. 1. Population, breeding biology and methods of control. J. appl. Ecol., 9, 835-74. NAS COMMIYrEEON BIOLOGICALEFFECTSOF ATMOSPHERICPOLLUTANTS,DIVISIONOF MEDICALSCIENCES, NATIONAL RESEARCH COUNCIL. (1972). Lead: Airborne lead in perspective. Washington, DC, National Academy of Sciences. NIELSEN, T., JENSEN, K. A. & GRANDJEAN, P. (1978). Organic lead in normal human brains. Nature, Lend., 274, 602-3. OJANEN, M., HAARAKANGAS,H. & HYVARINEN,H. (1975). Seasonal changes in bone mineral content and alkaline phosphatase activity in the house sparrow (Passer domesticus L). Camp. Biochem. Physiol., 50A, 581-5. PARIZEK, J. (1957). The destructive effect of cadmium ion on the testicular tissue and its prevention by zinc. Y. Endocrinol., 15, 55-63. POTTER,H. R. (1976). The nature and concentration of organometallics in natural waters. PhD thesis, University of ARRan, Birmingham. SCHROEDER, H. A., NASON, A. P., T1PTON, 1. H. & BALASSA,J. J. (1967). Essential trace elements in man: Zinc, relation to environmental cadmium. Y. Chron. Dis., 20, 179-210. SIMglSS, K. (1975). Calcium and avian reproduction. Syrup. Zeal. Sac. Lend., No. 35, 307-37. STONARD,M. D. & WEBB, M. (1976). Influence of dietary cadmium on the distribution of the essential metals copper, zinc and iron in tissues of the rat. Chem-Biol, Interactions, 15, 349-63. VALLEE,B. L. & ULMER, D. D. (1972). Biochemical effects of mercury, cadmium and lead. A. Rev. Biochem., 41, 91-128. WILLS, M. R., WORTSMAN,J., PAK, C. Y. C. & BARTTER,F. C. (1970). The role of parathyroid hormone in the gastro-intestinal absorption of calcium. Clin. Sci., 39, 89-94.
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 urbandwellingferal 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
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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 wetdigested 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 freezedried, 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 diand 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) Blood Liver Kidney
Brain Chelsea
12.0 + 1.00 ° (20) 6.33 _+ 1.12 b (13) 3.34 __ 0.29' (15) nd
Mortlake Heathrow Controls
I01.1 ___ 13.2 ~ (I 7) 45.2 __ 10.3 ~ (7) 16.2 _+ 5.50 c (10) 19.0 __ 2,60 c ( I 0)
21.6 ___ 1.9.5" (53) 10.1 __ 2.36 b (15) 6.11 _+ 1.09 c (15) 2.01 _+ 0 . 2 ~ (10)
321.4 + 45.3 ° (64) 48-7 __ 17.5 b (15) 9.87 __ 2.60 ~ (15) 4-34 +_ 1.26; d (7)
Bone 669"2 + 45-5 ° (41) 281-8 __. 73.7 b (15) 107-9 + 27.5 ~ (15) 5.73 +_ 1.05 ~ (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 Females Chelsea Mortlake Heathrow
Metal in bone (#g/g dry weight) Lead Zinc Males Females
868-2 + 99.6 (12) 349.6 + 118.4 (7) 134.4 + 44.9 (8)
566.9 __ 41.8* (29) 224.4 _+ 53.6 (8) 77.6 _+ 28-5 (7)
218.7 __ 10.4 (12) 144.2 + 13.1 (7) 186.3 _+ 32.9 (8)
Males 188.9 __ 5.04* (29) 160.7 _ 14.9 (8) 143.5 _+ 13.4 (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.
211
METAL ACCUMULATION IN PIGEONS TABLE 3 TISSUE CADMIUMCONCENTRATIONSOF FERAL PIGEONS FROM URBAN AND CONTROL AREAS (Mean _ standard error; sample size in parentheses)
Site Chelsea Mortlake Heathrow Controls
Cadmium in tissue (ltg/g dry weight) Brain Liver Kidney 0-19 + 0.02* (20) 0-14 + 0.02* (13) 0.47 4- 0.03 b
2.45 4- 0.28" (43) 0.40 4- 0-07 b (15) 9-48 4- 3'15"
12-3 + 2-05* (41) 1"52 + 0'31 b (15) 50.7 _+ 22.7*
(15)
(15)
(15)
nd
0.54 4- 0-05 (5)
1-75 (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 Brain Chelsea
Zinc in tissue (ltg/g dry weight) Lioer Kidney
Mortlake
53.9 4- 2.72* (20) 53.4 4- 5.47*
(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) Controls
N
146-5 4- 8 . 3 ~ (36) ,~b 78-8 ~ o.~o
(15) 203.9 + 31.9""
(10)
168.8 4- 5.87~ (44) 101.8 4- 12-8 b
Bone 197-7 4- 5'08* (41) 153-0 4- 9-9 b
(15)
(15)
190.5 + 18.9"
157.7 4. 5.8 b
(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
Chelsea (10) Heathrow ( l l )
Lead Gizzard
Intestine
5.60 _ 1'61 8.84 4- i.84
22.2 4- 7.01 2.09 ± 0.58
Cadmium Gizzard Intestine 0.31 4- 0.07 0'52 4. 0"08
0.82 4- 0.10 2"19 4. 0"75
Zinc Gizzard 44"4 4- 8.5 39"2 4. 8.2
Intestine 171.2 4- 13.8 180-9 ± 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 urbandwelling 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 coaccumulates 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.
REFERENCES ALTMAN, P. L. & DITTMER, D. S. (Eds) (1974). Biology data bbok, 2nd edn. Bethesda, Maryland. BARRY, P. S. 1. & MOSSMAN,D. B. (1970). Lead concentrations in human tissues. Br. J. ind. Med., 27, 339-51. CHAMBERLAIN,A. C., HEARD, M. J., LITTLE, P., NEWTON, D., WELLS, A. C. & WIFFEN, R. D. (1978). Investigations into lead from motor exhaust. AERE Report, R-9198. COOPER, W. C., TABERSHAW, I. R. & NELSON, K. W. (1973).iLaboratory studies of workers in lead smelting and refining. Proc. int. Symp. Environ. Hlth )lspects of Lead, Amsterdam, 2-6 October 1973,' 517-30. CREMER,J. E. (1965). Toxicology and biochemistry of alkyl lead compounds. Occup. Hlth Rev., 17, 14-19. DAY, J. P., HART, M. & ROBINSON, M. S. (1975)_Lead in urban Street dust. Nature, Lond., 253, 343-5. DUGGAN, M. J. & WILLIAm, S. (1977). Lead in dust in city streets. Sci. Total Environ., 7, 91-7. EL-GAZZAR,R. M., FINELLI,V. N., BOIANO,J. & PETERING,H. G. (1978). Influence of dietary zinc on lead toxicity in rats. Toxicol. Lett., I, 22%34. FINLEY, M. T., DIETER, M. P. & LOCKE, L. N. (1976). Lead in tissues of mallard ducks dosed with two types of lead shot. Bull. environ. Contain. & Toxicol., 16, 261-9. FISHER, G. L. (1975). Function and homeostasis of copper and zinc in mammals. Sci. Total Environ., 4, 373-412. FRIBERG, L., PISCATOR,M., NORDBERG,G. &!KJELLSTR6M,T. (1974). Cadmium in the environment, 2nd edn. Cleveland, Ohio, CRC Press. GOLDWATER,L. J. & HOOVER,A. W. (1967). An international study of normal levels of lead in blood and urine. Arch. environ. Hlth, 15, 60-3. GUNN, S. A., GOULD, T. C. & ANDERSON,W. A. D. (1963). The selective injurious response of testicular and epididymal blood vessels to cadmium and its prevention by zinc. Am. J. Path., 42, 685-94. HARRISON, R. M. & LAXEN, D. P. H. (1977). Organolead compounds adsorbed upon atmospheric particulates: A minor component of urban air. Atmos. Environ., 11,201-3.
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