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Lead levels of feral pigeons (Columba livia) from Madrid (Spain)
Environmental Pollution 54 (1988) 89-96
Lead Levels of. Feral Pigeons (Columba Madrid (Spain)
livia) from
M. T. Antonio Garcia, E. Martinez-Conde & I. Corpas Vazquez Dpto Biologia Animal II (Fisiologia Animal), Facultad de Ciencias Bioi6gicas, Universidad Complutensede Madrid, 28040 Madrid, Spain (Received 14 October 1987; revised version received28 January 1988; accepted 17 February 1988)
A BSTRA CT Tissue lead data are presented for populations of feral pigeons (Columba livia) from three locations in Madrid (Spain). The lead present in the lungs and digestive tract of pigeons increased progressively with traffic density and in parallel with atmospheric and ground lead values. The contribution of the respiratory route of Pb intake to the pigeons was about three times greater than the digestive route. The highest Pb values were found in bones. It is suggested that the pigeons gave a greatly magnified picture of lead pollution in cities than indicated by atmospheric lead concentrations.
INTRODUCTION With increasing concern about lead contamination of the urban environment, particularly that due to derivatives of alkyl lead compounds used as anti-knock agents in petrol (Caplun, 1985), attention has been drawn to the biological consequences of exposure to lead-contaminated aerosols and dusts to free-living vertebrates and especially to human health. Several surveys have been made in urban areas in an attempt to find plant and animal species that reflect ambient metal concentrations, and so can serve as sensitive biological indicators of lead contamination (Ohi et aL, 1974, 1980; Jenkins, 1975). Moreover, studies of lead accumulation in the feral pigeon, Columba livia, suggest that the use of this species as an indicator organism would facilitate the periodic monitoring of chronic lead exposure conditions 89
90
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez
in the urban environment that cannot readily be achieved through laboratory investigations (Hutt0n, 1980; Hutton & Goodman, 1980). The advantages of pigeons as bioindicators are related to their biological and ecological properties: pigeons have a higher metabolic rate (0.98 ml 0 2 g- 1 h- 1) than man (0-265 ml 02 g- 1 h- 1) and a greater ventilation volume ( 3 5 0 m l a i r m i n - l k g -1) than man ( 1 0 0 m l a i r m i n - l k g - l ) . The pigeon's habit of taking up small stones coated with lead particles into the gizzard, and the limited mobility of pigeons in the city, means that pigeons can demonstrate the severity of pollution at a given place more clearly than man. In this study we analysed lead pollution in the city of Madrid (Spain) using three pigeon populations from areas with low, medium and high traffic densities, respectively. Atmospheric and ground lead levels at the sites where the pigeons lived were measured. We have also analysed the lead concentration in lungs and digestive tracts of the pigeons, to identify the route of lead intake to the animal, and the lead levels in bones, because these are known to concentrate this metal.
MATERIALS A N D METHODS The pigeons were caught in Madrid city, in the three different areas of traffic density; low density areas (those with below 100 000 vehicles per day (v/d), intermediate (100000-200000 v/d) and high density zones (above 200 000 v/d) were covered. At the same time, control birds were obtained from a rural area without vehicular traffic, where lead concentrations were practically nil. In each of the urban areas the lead present in the ground was analysed, following the method of Archer & Barrat (1976), and atmospheric lead levels were measured, following the method of Simmonds et al. (1983). Samples of the pigeons'bones were calcinated at 450°C over 16 h and, as with lungs and digestive tracts, they were submitted to wet digestion, using a mixture of nitric and perchloric acids (4:1 v/v). All these assays were duplicated. After appropriate dilution, digests were analysed for lead by atomic absorption spectrophotometry. Background correction for non-atomic absorption was carried out with a hydrogen continuum lamp. Calibration curves were prepared from standards of a similar acid strength to the sample digest. The data fitted a normal distribution of data, and so the results are presented as mean _+standard deviation, and the significance of the difference between the groups was tested by Student's t. Portions of pigeons' lungs were fixed in 10% formalin and embedded in paraffin wax. Potassium dichromate and sodium rodozionate techniques were used to examine the appearance and frequency of lead particles within the lung tissue.
Lead levels of feral pigeons (C. livia) from Madrid (Spain)
91
RESULTS The urban pigeons, regardless of area, showed much higher levels of lead in their lungs than the rural ones, this difference being statistically significant (p < 0-002, Student's t-test). As Table 1 shows, not only the atmospheric lead levels but also lead concentration in the lungs increased when the traffic density was higher, so that the lead levels in the lungs of the pigeons from the area of highest traffic density were about twenty times greater than those of the rural area. Moreover, a positive correlation was found between atmospheric lead levels and the concentration of Pb in the pigeon's lungs (r = 0"52; p < 0"002). Histological examination of lung tissue from the pigeons showed the presence of lead particles in the parabronchus and alveolar sacks. Their diameter was always less than 1/zm, being principally between 0.30 and 0.75 pm. Several accumulations of these particles were observed in the lungs that might have been damaging to lung function. Likewise, their abundance was related to the lead concentration found in the pigeon's lungs, being maximum in those birds from areas of high traffic density (Fig. 1) and nil in those from rural areas (Fig. 2). The lead levels in the digestive tracts, as well as those in the ground where pigeons feed, are shown in Table 2. Again the urban birds gave much higher levels than the rural ones (p < 0.002), this difference being in proportion to vehicle density. Nevertheless, the lead intake via the digestive tract in urban pigeons is approximately three times less than via the respiratory route, while rural pigeons show almost the same lead levels in the digestive tract and lungs (Fig 3). Lead levels found in the pigeons' bones are shown in Fig. 4. Without TABLE 1 Atmospheric Lead Concentrations and Lung Lead Levels of Feral Pigeons from Urban and Control Areas (mean + standard deviation; L: low, M: medium and H: high traffic density)
.4rea
n
Rural Urban (L) Urban (M) Urban (H)
6 25 15 36
A tmospheric lead Lung lead levels (/zg m - 3) (Itg per g dry weight) -0.71 0.86 1-44
0-58 ___0-20 7-04 + 1"85" 7"71 + 0"91" 11.21 _ 2.32*
*Significantly different from controls at p < 0 . 0 0 2 Student's t-test.
using
92
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez
Fig. 1.
Fig. 2.
Lead levels of feral pigeons (C. livia) from Madrid (Spain)
93
TABLE 2 Ground Lead Concentration and Digestive Tract Lead Levels of Feral Pigeons from Urban and Control Areas (mean + standard deviation; sample size in parentheses; L: low, M: medium and H: high traffic density)
Area
Ground lead Organicmatter Digestive tract lead (ltg per g dry weight) (%) (l~gper g dry weight)
Rural
--
--
0.71 + 0-28
80-46 + 19.53 (23) 62.59 _+ 15.85 (18) 177"74 + 30.09 (27)
2-18
1.81 +0-50* (25) 2-57 _+0.41" (15) 4-52 + 1-56" (36)
(6) Urban (L) Urban (M) Urban (H)
4.06 4"69
* Significantly different from controls at p < if002 using Student's t-test.
exception, females showed higher concentrations than males, but these differences were statistically significant (p<0.002) only in rural birds (Table 3). DISCUSSION The present results show that lead levels in air and ground increase with traffic density. This gradient is also apparent in the tissues of the urban X
d.w.
1110Pb in lungs
9-
Pb in digestive tube
X
8-
,I
X
765-
X l
4-
~:,.
3-
Vf"
2-
':':..~."i*7..'-
1N
L RURAL
URBAN AREAS
Fig. 3.
94
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez TABLE 3 Bone Lead Concentration in Feral Pigeons from Urban and Control Areas Subdivided According to Sex (mean_ standard deviation; sample size in parentheses; L: low, M: medium and H: high traffic density) A rea
Bone lead levels (#g per g dry weight)
Rural Urban (L) Urban (M) Urban (H)
Males
Females
9.19 _+ 1-46 (3) 53.53 _ 43.22* (13) 144.19 -I-44.01" (9) 231.92 _+72.58* (16)
15.04 ___1.09 (3) 75.75 __+37.89* (12) 148.19 _ 37.63* (6) 302"83 _+62.39* (20)
* Significantly different from controls at p<0.002 using Student's t-test.
280--
240--
200--
o~ LU
160--
f13 120-e-., LLI ...a
809
40--
L
M
Kq.~AL
URBAN AREAS
Fig. 4.
H
Lead levels of feral pigeons (C. iivia)from Madrid (Spain)
95
pigeons. Several considerations emerge from these data. First, the amount of lead present in the lungs and digestive tract of the studied pigeons reflects perfectly the levels of contamination of air and ground in different areas of Madrid. This fact is very important, because the lead levels present in different tissues of urban pigeons give a clear idea of the risks to human inhabitants of the city. Secondly, the way of life of these birds results in lead capture via both ingestion and inhalation. According to our observations, the contribution via the respiratory tract to the intake of Pb is approximately three times greater than via the gastrointestinal tract. This is not surprising, since the percentage of lead absorbed by respiration is about 50%, while, by the digestive route, it is only 10% (Rabinowitz et al., 1976). Most of the Pb particles present in the urban atmosphere are less than 1 #m in diameter (Vie le Sage et al., 1982) and this size produces a high absorption rate for this metal. This observation agrees with our laboratory data, where the lead particles in urban pigeons' lungs are between 0.30 and 0.75 #m in diameter. The highest amount of Pb within a pigeon's body is found in bones. This is biologically important, since the bone can hold a large amount of lead for many years, but part of this can return to the blood in a similar amount of time to that for which the metal would remain in other tissues, 100-200 days (Marcus, 1985). For this reason many authors believe that the Pb found in bone is a very good indicator of the total amount of such metal in the body. In our study female pigeons showed higher lead levels in bone than males, as was found in previous studies (Jenkins, 1975; Johnson et al., 1982), and this may be associated with an increased retention of lead during the changes in calcium metabolism connected with eggshell production. In conclusion, we can say that, at the traffic densities found in Madrid, lead levels found in the atmosphere and ground are reflected in the lead levels in different tissues of urban pigeons. Our results therefore indicate the urban pigeons are good biological indicators of environmental lead pollution in cities.
REFERENCES Archer, A. & Barrat, B. S. (1976). Lead levels in Birmingham dust. Sci. Total Environ., 6, 275-86. Caplun, E., Petit, D. & Piccioto, E. (1984). Le plomb dans l'essence. La Recherche, 152(15), 270-80. Hutton, M. (1980). Metal contamination of feral pigeons, Columba livia, from the London area. Part2: Biological effects of lead exposure. Environ. Pollut. (Ser. A), 22, 281-93. Hutton, M. & Goodman, G. T. (1980). Metal contamination of feral pigeons,
96
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez
Columba iivia, from the London area. Part 1: Tissue accumulation of lead, cadmium and zinc. Environ. Pollut. (Set. A), 22, 207-17. Jenkins, C. (1975). Use of the feral pigeon (Columba livia) to monitor atmospheric lead pollution. C.R. Acad. Sci., 281(D), 1187-9. Johnson, M. S., Pluck, H., Hutton, M. & Moore, G. (1982). Accumulation and renal effects of lead in urban populations of feral pigeons, Columba livia. Arch. Environ. Cont. ToxicoL, ll, 761-7. Marcus, A. H. (1985). Multicompartment kinetic models for lead. 1: Bone diffusion models for long-term retention. Environ. Res., 36, 441-58. Ohi, G., Seki, H., Akiyama, K. & Yagyu, H. (1974). The pigeon, a sensor of lead pollution. Bull. of Environ. Contam. & ToxicoL, 12(1), 92-8. Ohi, G., Seki, H., Minowa, K., Osawa, M., Mizoguchi, I. & Sugimori, F. (1981).Lead pollution in Tokyo: The pigeon reflects its amelioration. Environ. Res., 26, 125-9. Rabinowitz, M. B., Wetherhill, G. W. & Kopple, J. D. (1976). Kinetic analysis of lead metabolism in healthy humans. J. Clin. Invest., 58, 260-70. Simmonds, P. R., Tan, S. Y. & Fergusson, J. E. (1983). Heavy metal pollution at an intersection involving a busy urban road in Christchurch, New Zealand. New Zealand Journal of Science, 26, 229-42. Vie le Sage, R., Elichegaray, C., Darzi, M. & Dutot, A. (1982). La chimie du plomb et du brome particulaire en atmosphere urbaine I y II. Chemosphere, 11(3), 319-24.
Lead Levels of. Feral Pigeons (Columba Madrid (Spain)
livia) from
M. T. Antonio Garcia, E. Martinez-Conde & I. Corpas Vazquez Dpto Biologia Animal II (Fisiologia Animal), Facultad de Ciencias Bioi6gicas, Universidad Complutensede Madrid, 28040 Madrid, Spain (Received 14 October 1987; revised version received28 January 1988; accepted 17 February 1988)
A BSTRA CT Tissue lead data are presented for populations of feral pigeons (Columba livia) from three locations in Madrid (Spain). The lead present in the lungs and digestive tract of pigeons increased progressively with traffic density and in parallel with atmospheric and ground lead values. The contribution of the respiratory route of Pb intake to the pigeons was about three times greater than the digestive route. The highest Pb values were found in bones. It is suggested that the pigeons gave a greatly magnified picture of lead pollution in cities than indicated by atmospheric lead concentrations.
INTRODUCTION With increasing concern about lead contamination of the urban environment, particularly that due to derivatives of alkyl lead compounds used as anti-knock agents in petrol (Caplun, 1985), attention has been drawn to the biological consequences of exposure to lead-contaminated aerosols and dusts to free-living vertebrates and especially to human health. Several surveys have been made in urban areas in an attempt to find plant and animal species that reflect ambient metal concentrations, and so can serve as sensitive biological indicators of lead contamination (Ohi et aL, 1974, 1980; Jenkins, 1975). Moreover, studies of lead accumulation in the feral pigeon, Columba livia, suggest that the use of this species as an indicator organism would facilitate the periodic monitoring of chronic lead exposure conditions 89
90
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez
in the urban environment that cannot readily be achieved through laboratory investigations (Hutt0n, 1980; Hutton & Goodman, 1980). The advantages of pigeons as bioindicators are related to their biological and ecological properties: pigeons have a higher metabolic rate (0.98 ml 0 2 g- 1 h- 1) than man (0-265 ml 02 g- 1 h- 1) and a greater ventilation volume ( 3 5 0 m l a i r m i n - l k g -1) than man ( 1 0 0 m l a i r m i n - l k g - l ) . The pigeon's habit of taking up small stones coated with lead particles into the gizzard, and the limited mobility of pigeons in the city, means that pigeons can demonstrate the severity of pollution at a given place more clearly than man. In this study we analysed lead pollution in the city of Madrid (Spain) using three pigeon populations from areas with low, medium and high traffic densities, respectively. Atmospheric and ground lead levels at the sites where the pigeons lived were measured. We have also analysed the lead concentration in lungs and digestive tracts of the pigeons, to identify the route of lead intake to the animal, and the lead levels in bones, because these are known to concentrate this metal.
MATERIALS A N D METHODS The pigeons were caught in Madrid city, in the three different areas of traffic density; low density areas (those with below 100 000 vehicles per day (v/d), intermediate (100000-200000 v/d) and high density zones (above 200 000 v/d) were covered. At the same time, control birds were obtained from a rural area without vehicular traffic, where lead concentrations were practically nil. In each of the urban areas the lead present in the ground was analysed, following the method of Archer & Barrat (1976), and atmospheric lead levels were measured, following the method of Simmonds et al. (1983). Samples of the pigeons'bones were calcinated at 450°C over 16 h and, as with lungs and digestive tracts, they were submitted to wet digestion, using a mixture of nitric and perchloric acids (4:1 v/v). All these assays were duplicated. After appropriate dilution, digests were analysed for lead by atomic absorption spectrophotometry. Background correction for non-atomic absorption was carried out with a hydrogen continuum lamp. Calibration curves were prepared from standards of a similar acid strength to the sample digest. The data fitted a normal distribution of data, and so the results are presented as mean _+standard deviation, and the significance of the difference between the groups was tested by Student's t. Portions of pigeons' lungs were fixed in 10% formalin and embedded in paraffin wax. Potassium dichromate and sodium rodozionate techniques were used to examine the appearance and frequency of lead particles within the lung tissue.
Lead levels of feral pigeons (C. livia) from Madrid (Spain)
91
RESULTS The urban pigeons, regardless of area, showed much higher levels of lead in their lungs than the rural ones, this difference being statistically significant (p < 0-002, Student's t-test). As Table 1 shows, not only the atmospheric lead levels but also lead concentration in the lungs increased when the traffic density was higher, so that the lead levels in the lungs of the pigeons from the area of highest traffic density were about twenty times greater than those of the rural area. Moreover, a positive correlation was found between atmospheric lead levels and the concentration of Pb in the pigeon's lungs (r = 0"52; p < 0"002). Histological examination of lung tissue from the pigeons showed the presence of lead particles in the parabronchus and alveolar sacks. Their diameter was always less than 1/zm, being principally between 0.30 and 0.75 pm. Several accumulations of these particles were observed in the lungs that might have been damaging to lung function. Likewise, their abundance was related to the lead concentration found in the pigeon's lungs, being maximum in those birds from areas of high traffic density (Fig. 1) and nil in those from rural areas (Fig. 2). The lead levels in the digestive tracts, as well as those in the ground where pigeons feed, are shown in Table 2. Again the urban birds gave much higher levels than the rural ones (p < 0.002), this difference being in proportion to vehicle density. Nevertheless, the lead intake via the digestive tract in urban pigeons is approximately three times less than via the respiratory route, while rural pigeons show almost the same lead levels in the digestive tract and lungs (Fig 3). Lead levels found in the pigeons' bones are shown in Fig. 4. Without TABLE 1 Atmospheric Lead Concentrations and Lung Lead Levels of Feral Pigeons from Urban and Control Areas (mean + standard deviation; L: low, M: medium and H: high traffic density)
.4rea
n
Rural Urban (L) Urban (M) Urban (H)
6 25 15 36
A tmospheric lead Lung lead levels (/zg m - 3) (Itg per g dry weight) -0.71 0.86 1-44
0-58 ___0-20 7-04 + 1"85" 7"71 + 0"91" 11.21 _ 2.32*
*Significantly different from controls at p < 0 . 0 0 2 Student's t-test.
using
92
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez
Fig. 1.
Fig. 2.
Lead levels of feral pigeons (C. livia) from Madrid (Spain)
93
TABLE 2 Ground Lead Concentration and Digestive Tract Lead Levels of Feral Pigeons from Urban and Control Areas (mean + standard deviation; sample size in parentheses; L: low, M: medium and H: high traffic density)
Area
Ground lead Organicmatter Digestive tract lead (ltg per g dry weight) (%) (l~gper g dry weight)
Rural
--
--
0.71 + 0-28
80-46 + 19.53 (23) 62.59 _+ 15.85 (18) 177"74 + 30.09 (27)
2-18
1.81 +0-50* (25) 2-57 _+0.41" (15) 4-52 + 1-56" (36)
(6) Urban (L) Urban (M) Urban (H)
4.06 4"69
* Significantly different from controls at p < if002 using Student's t-test.
exception, females showed higher concentrations than males, but these differences were statistically significant (p<0.002) only in rural birds (Table 3). DISCUSSION The present results show that lead levels in air and ground increase with traffic density. This gradient is also apparent in the tissues of the urban X
d.w.
1110Pb in lungs
9-
Pb in digestive tube
X
8-
,I
X
765-
X l
4-
~:,.
3-
Vf"
2-
':':..~."i*7..'-
1N
L RURAL
URBAN AREAS
Fig. 3.
94
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez TABLE 3 Bone Lead Concentration in Feral Pigeons from Urban and Control Areas Subdivided According to Sex (mean_ standard deviation; sample size in parentheses; L: low, M: medium and H: high traffic density) A rea
Bone lead levels (#g per g dry weight)
Rural Urban (L) Urban (M) Urban (H)
Males
Females
9.19 _+ 1-46 (3) 53.53 _ 43.22* (13) 144.19 -I-44.01" (9) 231.92 _+72.58* (16)
15.04 ___1.09 (3) 75.75 __+37.89* (12) 148.19 _ 37.63* (6) 302"83 _+62.39* (20)
* Significantly different from controls at p<0.002 using Student's t-test.
280--
240--
200--
o~ LU
160--
f13 120-e-., LLI ...a
809
40--
L
M
Kq.~AL
URBAN AREAS
Fig. 4.
H
Lead levels of feral pigeons (C. iivia)from Madrid (Spain)
95
pigeons. Several considerations emerge from these data. First, the amount of lead present in the lungs and digestive tract of the studied pigeons reflects perfectly the levels of contamination of air and ground in different areas of Madrid. This fact is very important, because the lead levels present in different tissues of urban pigeons give a clear idea of the risks to human inhabitants of the city. Secondly, the way of life of these birds results in lead capture via both ingestion and inhalation. According to our observations, the contribution via the respiratory tract to the intake of Pb is approximately three times greater than via the gastrointestinal tract. This is not surprising, since the percentage of lead absorbed by respiration is about 50%, while, by the digestive route, it is only 10% (Rabinowitz et al., 1976). Most of the Pb particles present in the urban atmosphere are less than 1 #m in diameter (Vie le Sage et al., 1982) and this size produces a high absorption rate for this metal. This observation agrees with our laboratory data, where the lead particles in urban pigeons' lungs are between 0.30 and 0.75 #m in diameter. The highest amount of Pb within a pigeon's body is found in bones. This is biologically important, since the bone can hold a large amount of lead for many years, but part of this can return to the blood in a similar amount of time to that for which the metal would remain in other tissues, 100-200 days (Marcus, 1985). For this reason many authors believe that the Pb found in bone is a very good indicator of the total amount of such metal in the body. In our study female pigeons showed higher lead levels in bone than males, as was found in previous studies (Jenkins, 1975; Johnson et al., 1982), and this may be associated with an increased retention of lead during the changes in calcium metabolism connected with eggshell production. In conclusion, we can say that, at the traffic densities found in Madrid, lead levels found in the atmosphere and ground are reflected in the lead levels in different tissues of urban pigeons. Our results therefore indicate the urban pigeons are good biological indicators of environmental lead pollution in cities.
REFERENCES Archer, A. & Barrat, B. S. (1976). Lead levels in Birmingham dust. Sci. Total Environ., 6, 275-86. Caplun, E., Petit, D. & Piccioto, E. (1984). Le plomb dans l'essence. La Recherche, 152(15), 270-80. Hutton, M. (1980). Metal contamination of feral pigeons, Columba livia, from the London area. Part2: Biological effects of lead exposure. Environ. Pollut. (Ser. A), 22, 281-93. Hutton, M. & Goodman, G. T. (1980). Metal contamination of feral pigeons,
96
M. T. Antonio Garcia, E. Martinez-Conde, L Corpas Vazquez
Columba iivia, from the London area. Part 1: Tissue accumulation of lead, cadmium and zinc. Environ. Pollut. (Set. A), 22, 207-17. Jenkins, C. (1975). Use of the feral pigeon (Columba livia) to monitor atmospheric lead pollution. C.R. Acad. Sci., 281(D), 1187-9. Johnson, M. S., Pluck, H., Hutton, M. & Moore, G. (1982). Accumulation and renal effects of lead in urban populations of feral pigeons, Columba livia. Arch. Environ. Cont. ToxicoL, ll, 761-7. Marcus, A. H. (1985). Multicompartment kinetic models for lead. 1: Bone diffusion models for long-term retention. Environ. Res., 36, 441-58. Ohi, G., Seki, H., Akiyama, K. & Yagyu, H. (1974). The pigeon, a sensor of lead pollution. Bull. of Environ. Contam. & ToxicoL, 12(1), 92-8. Ohi, G., Seki, H., Minowa, K., Osawa, M., Mizoguchi, I. & Sugimori, F. (1981).Lead pollution in Tokyo: The pigeon reflects its amelioration. Environ. Res., 26, 125-9. Rabinowitz, M. B., Wetherhill, G. W. & Kopple, J. D. (1976). Kinetic analysis of lead metabolism in healthy humans. J. Clin. Invest., 58, 260-70. Simmonds, P. R., Tan, S. Y. & Fergusson, J. E. (1983). Heavy metal pollution at an intersection involving a busy urban road in Christchurch, New Zealand. New Zealand Journal of Science, 26, 229-42. Vie le Sage, R., Elichegaray, C., Darzi, M. & Dutot, A. (1982). La chimie du plomb et du brome particulaire en atmosphere urbaine I y II. Chemosphere, 11(3), 319-24.