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Heavy metal contamination in little owl (Athene noctua) and common buzzard (Buteo buteo) from northern Italy
ARTICLE IN PRESS
Ecotoxicology and Environmental Safety 60 (2005) 61–66
Heavy metal contamination in little owl (Athene noctua) and common buzzard (Buteo buteo) from northern Italy Alessandra Battaglia,a,* Sergio Ghidini,a Giorgio Campanini,a and Roberto Spaggiarib a
Dipartimento di Produzioni Animali, Biotecnologie Veterinarie, Qualita` e Sicurezza degli Alimenti, Facolta` di Medicina Veterinaria, Universita` di Parma,43100 Parma, Italy b Agenzia Regionale Prevenzione e Ambiente, Sezione Provinciale di Reggio Emilia, Italy Received 14 July 2003
Abstract In this study, two raptor species, the common buzzard (Buteo buteo) and the little owl (Athene noctua), were investigated for lead and cadmium concentrations, using liver, kidneys, pectoral muscle, sternum bone, and feathers. All the collected birds died at the Centro Recupero Rapaci of Lega Italiana Protezione Uccelli in Sala Baganza (Parma, Italy). They arrived alive at the Centro between November 1998 and November 1999 but died or were put to death as a consequence of injuries or other ailments. The results of the investigation do not show an excessive exposure to cadmium, whereas some interesting data have emerged in the case of lead. The concentration of the latter in the liver and in the bone of two little owls seem to suggest the possibility of chronic exposure. The high values found in one common buzzard, on the other hand, suggest an acute exposure and, probably, a case of lead shot ingestion. r 2004 Elsevier Inc. All rights reserved. Keywords: Lead; Cadmium; Little owl; Common buzzard; Shot; Sentinel species
1. Introduction The impact of heavy metals on the environment can be a serious threat for the stability of ecosystems. The spread of hunting bullets and fishing weights represents a problem of growing relevance. The use of lead shot, indeed, increases anthropogenic input of this metal into the environment and causes a very specific pollution problem, resulting in considerable avian mortality (Pain and Amiard-Triquet, 1993). Primary lead toxicosis is prevalent among waterbirds which ingest lead shot by mistaking it for grit or seeds. Secondary lead toxicosis occurs in birds of prey or other scavengers by eating animals wounded by gunfire or impaired by primary toxicosis. Furthermore, a sufficient amount of evidence is now available to conclude that the whole metallic lead in shot and sinkers is transformed into particulate and molecular Pb species, becoming dispersed in the environment to some degree (Scheuhammer and Norris, 1996). Lead oxides, carbonates, and other compounds *Corresponding author. Fax: +39-0521-032752. E-mail address: [email protected] (A. Battaglia). 0147-6513/$ - see front matter r 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ecoenv.2003.12.019
are produced by weathering of the pellets when metallic lead of spent shot or sinkers is exposed to air or water (Sever, 1993). Lead breaks down more quickly where the soil and water are acidic and full of oxygen. Lead attached to soil particles can be moved to new places by erosion. This process can result in local lead concentrations in soils and waters far in excess of normal concentrations (Scheuhammer and Norris, 1996). Cadmium has been described as one of the most dangerous trace elements in food and in the environment, not only for its high toxicity but also for its persistence. Atmospheric cadmium deposited on the earth’s crust can be absorbed or retained by soil particles and become part of biological structures. Dissolved cadmium is readily absorbed by plants and leaches rapidly into the subsoil, contaminating deep and surface waters (Cabrera et al., 1998). The transfer of cadmium from soils to the edible portions of agricultural crops is significantly greater than that of other elements (Cabrera et al., 1998). The use of sentinel species can provide interesting data to monitor the quality of the environment. Some species have biological habits that increase the
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likelihood of exposure to contaminants and, in that way, can produce relevant information that would be missed if only water or soil were analyzed. Animals at the top of the food pyramid can yield information over a large area around each sampling site, not only on bioavailability of contaminants but also on how, where, and when they are transferred within the food web (Jager et al., 1996). This research aimed at this kind of information by measuring the amounts of lead and cadmium in tissues of two raptor species: common buzzards and little owls. Common buzzards are suitable for biomonitoring for several reasons: they catch a wide range of prey, are mainly sedentary in Italy (the migrant flows of northern European birds occur in autumn and in spring), and, moreover, birds found dead can provide a sufficiently large sample. Similar to buzzards, the little owls, in Italy, are resident, they feed on a wide range of prey, and individuals found dead can provide a sufficiently large sample for analysis.
Table 1 Age, sex, and weight data of little owls
2. Materials and methods
adopted for individual identification throughout the study. The 38 little owls comprised 15 adults (9 females and 6 males) and 23 juveniles (11 females and 11 males; the sex of 1 juvenile could not be established). The 18 buzzards comprised 5 adults (4 females and 1 male), 12 juveniles (5 females and 7 males), and 1 individual of unknown age (see Tables 1 and 2). Most of the birds came from the provinces of Parma and Reggio Emilia, but some birds came also from nearby provinces (Piacenza, Modena, Mantova, Cremona, Lodi, Brescia, Alessandria, Novara, Torino, Vercelli, Pavia). Almost all little owls were collected during the summer, whereas the majority of the buzzards gathered during the winter. All carcasses were stored at 20 C. The following samples were taken from each corpse: liver, kidneys, pectoral muscle, and sternum bone. The feathers from the back were sampled also. The preparation of the dead birds and samples was carried out taking care to avoid contamination and losses as much as possible: sterile scalpels and surgical tools cleaned or substituted for each bird were used together with rubber latex gloves. The working surface was also cleaned after each operation. The samples were handled in a way to avoid any contact with external surfaces, placed individually in plastic bags, and stored at 20 C.
2.1. Collection of samples In the time period of 1 year, between November 1998 and November 1999, we collected 38 little owls (Athene noctua) and 18 common buzzards (Buteo buteo), hereafter called buzzard. All raptors came from Centro Recupero Rapaci of Lega Italiana Protezione Uccelli in Sala Baganza (Parma, Italy). The birds had been brought to the Centro alive but injured or debilitated for various reasons. The birds died naturally later or were euthanized soon after admission with Tanax (Intervet Italia s.r.l.) by the veterinary of the Centro when their health state did not indicate potential recovery. The main cause of death, for both species, was classified as different kinds of trauma. Frequently the birds were injured by collision with a vehicle or with power lines or by lead shot. The last kind of trauma concerned essentially the buzzards: 5 of 18 buzzards were shot according to the notes of admission in the Centro. In general, the main causes of admission in the Centro were fractures and luxations due to traumas. A choice was made to use for the study only those birds that had not been held at the Centro more than 1 month. The average period of stay in the Centro of the chosen birds, however, was about 1 week. The diet provided during this period was composed only of dead chicks coming from chicken farms. The following data were gathered for each bird: sex, age, weight, cause of death, area of origin, date of arrival, and date of death. The file number given to each bird at the time of admission to the Centro has been
Age/sex
Adult/female Adult/male Juvenile/female Juvenile/male
No.
9 6 11 11
Weight (g) Min.
Max.
Median
Mean
113 125 91 66
174 183 172 148
154 164.5 136 97
148.2 155.8 135.2 100.5
Table 2 Age, sex, and weight data of buzzards Age/sex
Adult/female Adult/male Juvenile/female Juvenile/male
No.
4 1 5 7
Weight (g) Min.
Max.
Median
Mean
579 582 605 420
800 582 860 986
769 582 640 559
729.3 582 683 676.1
2.2. Preparation and analysis of the samples Samples were thawed and dried in air for 24 h at 105 C. The dried material was joined together in a mortar with the exception of the feathers, which were digested as such. About 0.25 g were weighed directly in
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the digestion tubes and digested in a microwave oven (Milestone MEGA 1200), with 3 mL of HNO3 and 0.5 mL of H2O2. Lead content was determined with a Perkin–Elmer 2100 atomic absorption spectrophotometer, equipped with a graphite furnace atomizer. The detection limit was 0.20 mg/kg dry weight. Cadmium analysis was carried out with a Perkin–Elmer Analyst 600 graphite furnace atomic absorption spectrophotometer, equipped with Zeeman background correction. The detection limit was 0.003 mg/kg dry weight. Each analysis was carried out in duplicate. 2.3. Statistical analysis A nonparametric approach to the analysis of the data was necessary, because of skewness of the distributions of heavy metals concentrations. The difference between adults and juveniles was tested using Mann–Whitney U test and the correlation among tissue concentrations with Kendall’s t partial correlation coefficient. Significance was considered at 0.05 probability level. For mathematical reasons, a value of half the detection limit was given to data points below the detection limit.
3. Results Lead and cadmium concentrations are presented in Tables 3 and 4 expressed as mg/kg dry weight (dw). The analyses were performed on dry tissues because dry weight values are more reliable and consistent than wet weight values (Adrian and Stevens, 1979). Due to the skewness of the distribution the results are expressed as median with minimum and maximum values also presented; the maximum values are expressed as mean7standard deviation. Median lead contents of little owls ranged from a minimum of 0.1 mg/kg dw in the muscle to 2 mg/kg dw Table 3 Lead and cadmium concentrations (mg/kg dw) in little owls Median
Min.
Max.
Lead Liver Kidney Bone Muscle Feather
0.35 0.50 0.88 0.10 2.00
o0.20 o0.20 o0.20 o0.20 o0.20
11.970.87 2.9570.42 17.970.23 0.7270.01 19.170.18
Cadmium Liver Kidney Bone Muscle Feather
0.050 0.040 0.010 o0.003 0.050
o0.003 o0.003 o0.003 o0.003 0.017
2.62070.040 7.48070.230 0.13070.002 0.42070.020 0.69070.010
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Table 4 Lead and cadmium concentrations (mg/kg dw) in common buzzards Median
Min.
Max.
Lead Liver Kidney Bone Muscle Feather
0.95 0.75 1.87 o0.20 1.48
o0.20 o0.20 0.28 o0.20 o0.20
47.773.82 10.870.94 42.072.83 19.470.63 8.8770.96
Cadmium Liver Kidney Bone Muscle Feather
0.010 0.620 0.010 o0.003 0.060
0.01770.001 0.02370.001 o0.003 o0.003 0.018
2.02070.040 12.1270.590 0.06070.001 0.42070.010 0.37070.004
in the feathers. Seven little owls had lead concentrations in the liver between 6 and 20 mg/kg dw. Two of them, with liver lead contents of 9.3270.68 and 11.7570.85 mg/kg dw, had high lead concentrations in the bone (17.9170.23 and 12.1570.15 mg/kg dw, respectively). Two other little owls had lead concentrations in the bone (6.3270.16 and 9.0570.29 mg/kg dw) that suggest high environmental contamination. Lead concentrations in the kidneys were lower than 3 mg/kg dw in all cases and only two little owls with 2.5670.02 and 2.9570.42 mg/kg dw were close to 3 mg/ kg dw. Muscle lead content never exceeded 1 mg/kg dw. The highest lead values in the feathers were 18.2870.13 and 19.0670.18 mg/kg dw. Median values of lead content in buzzards ranged from 0.2 mg/kg dw in muscle to 1.87 mg/kg dw in bone and, with the exception of feathers, median values were higher than those of little owls. The same pattern applies to maximum values. Two buzzards had lead concentrations in the liver of 7.2870.53 and 6.2170.45 mg/kg dw. Two other buzzards had liver lead concentrations 420 mg/kg dw. One of them had 47.7073.82 mg/kg dw lead in the liver, 6.6070.57 mg/ kg dw in the kidneys, and 4272.83 mg/kg dw in the bone. The same bird had the highest value in the feathers (8.8770.96 mg/kg dw) among the buzzards. A second buzzard, with 7.5970.16 mg/kg dw lead in the feathers, ranked very close to the previous one. The second buzzard with liver lead concentration 420 mg/kg dw (20.4571.49 mg/kg dw) had 10.757 0.94 mg/kg dw lead in the kidneys and 16.1070.87 mg/ kg dw lead in the bone. This bird, however, had been shot and the presence of lead fragments remains a possibility. The work plan of the present study did not include X-ray radiography nor digestive tract examination but relied only on the notes of admission to the Centro. The same doubt remains for two other shot animals; one had high lead concentrations in the muscle
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(19.3970.63 mg/kg dw) and in the bone (27.6670.76 mg/ kg dw) and the other had high lead concentration only in the muscle (11.2270.14 mg/kg dw). Cadmium contents of little owls ranged from a median value close to the detection limit for the muscle to 0.05 mg/kg dw in liver and feathers. Liver cadmium concentrations of little owls never exceeded 3 mg/kg dw. Just one bird got close to such a value with 2.6270.04 mg/kg dw. Cadmium concentrations in the kidneys were lower than 8 mg/kg dw. The highest value observed in one little owl was 7.4870.23 mg/kg dw. Lead content of muscles, feathers, and bones was lower than 1 mg/kg dw in all cases. Median cadmium values in buzzards were lowest in muscle, as in little owls, and highest in kidneys. Two birds had cadmium concentrations in kidneys over 8 mg/ kg dw: one with 8.6270.42 mg/kg dw and one with 12.1270.59 mg/kg dw. Cadmium in the liver showed a maximum value of 2.02 mg/kg dw and in muscles, bones, and feathers it never exceeded 0.5 mg/kg dw. No significant difference was observed in metal content of adult and juvenile buzzards, whereas highly significant differences in cadmium content of liver, kidneys, and muscle were observed in adult and juvenile little owls (Table 5). The existence of a statistical relationship between metal contents in different tissues was studied by means of simple correlation coefficients. In little owls (Table 6) a highly significant r value was observed for liver versus kidney cadmium content. The same applies for buzzards (Table 7) but in this species r was highly significant also
Table 5 Significant differences between adult and juvenile little owls Metal
Tissue
P
Lead
Bone
0.015
Cadmium
Liver Kidney Muscle Bone
0.0001 0.0001 0.0001 0.012
Po0:05: Po0:01:
Table 6 Significant correlations between tissues in little owls Metal
Tissues
P
Lead
Bone and liver Bone and feathers
0.017 0.019
Cadmium
Kidney and liver Kidney and feathers
0.0001 0.014
Po0:05: Po0:01:
Table 7 Significant correlations between tissues in buzzards Metal
Tissues
P
Lead
Liver and kidney
0.004
Cadmium
Liver and kidney Liver and feathers Kidney and feathers
0.0001 0.049 0.005
Po0:05: Po0:01:
for lead content of liver versus kidneys and for cadmium content of kidneys versus feathers.
4. Discussion Shot are the only widespread source of lead likely to result in lead poisoning in raptors as they can be carried in the flesh of dead or injured prey. Acute lead poisoning can ensue in the case of ingestion of a large number of shot (10 or more) and birds usually die within a few days. More commonly, birds die of chronic lead poisoning following ingestion of a smaller number of shot (Scheuhammer and Norris, 1996). Ingested shot dissolve in the acid environment of the avian stomach and are absorbed into the bloodstream through the wall of the digestive system. Lead shot that become embedded in tissues of birds that are not killed, instead, are not solubilized except when they penetrate into the lumen of the gizzard or proventriculus (Kendall et al., 1996). Liver and kidney concentrations are primarily considered indexes of a recent exposure, whereas bone contents reflect chronic exposure. The significant difference between adult and juvenile little owls observed for lead content in the bone shows the tendency of this tissue to hoard the metal in the long term. Feathers can play the role both of storing and of eliminating metals. Metal levels in feathers reflect blood levels during the short period of feather growth, when the feather is connected with blood vessels and metals are incorporated in the keratin structure (Dauwe et al., 2000). This is not the only factor to take into account, though. Indeed, feathers can also measure external contamination. The toxicological consequences of lead shot ingestion are dependent, however, on different variables (e.g., condition of the animal, gender, age, diet, and climate). Previous studies revealed that liver lead concentrations found in raptors not diagnosed as having died of lead poisoning were generally o2 mg/kg dw and often o1 mg/kg dw. Such values represent a normal exposure to background levels and are not sufficient to severely impair normal biological functioning. Concentrations
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between 6 and 20 mg/kg dw are signs of exposure levels higher than background exposure and external signs of poisoning may be present. Higher concentrations are associated with acute exposure and are immediately life threatening. Liver lead concentrations 420 mg/kg dw almost certainly result from shot ingestion and have been reported in species most likely to be exposed to this source of lead (Pain et al., 1994). Jager et al. (1996) reported that 10 mg/kg dw lead in kidneys correspond to environmental pollution. Scheuhammer (1987) suggested that lead levels above 5 mg/kg dw in bones correspond to a high level of environmental contamination. The first buzzard mentioned in the previous section with 47.7073.82 mg/kg dw lead in the liver, 6.6070.57 mg/kg dw in the kidneys, and 4272.83 mg/ kg dw in the bone is probably a case of acute exposure. The bird was not shot but when it was admitted to the Centro Recupero Rapaci it was undernourished and suffered from paresis of the legs and strong contraction of the talons interpreted as nerve damage consequent to tetanus. Common buzzards catch a wide range of prey: their diet includes small mammals, birds, amphibians, reptiles, and insects. Little owls also feed on a wide range of prey, particularly small mammals and invertebrates, e.g., earthworms (Lumbricidae), and sometimes reptiles, amphibians, and small birds. Buzzards act often as scavengers and, in this way, are more likely than little owls to be exposed to lead shot in small game species. This could explain the correlation between concentrations of lead in liver and kidney in buzzards since such tissues are the first targets of the metal and, as mentioned above, are index of recent exposure. In the little owls of our study, instead, the correlations with the tissues index of a chronic exposure (bone and feathers) was significant. It is more difficult to determine the origin of lead exposure when liver concentration is lower than the values expected from acute exposure. Concentrations between 6 and 20 mg/kg dw could result from shot having been in the stomach for only a short time (before regurgitation) or from the remnant of a larger exposure which had taken place in previous weeks or months (Pain et al., 1994). The two little owls with liver lead contents of 9.3270.68 and 11.7570.85 mg/kg dw and bone lead concentrations of 17.9170.23 and 12.1570.15 mg/kg dw, respectively, had probably been exposed for a long time to lead pollution. Cadmium concentrations in birds are generally reported to be highest in kidneys, lower in liver, and very low in muscle (Nicholson, 1981; Thompson, 1990). A few reports show muscle cadmium concentrations in adult birds to be around 0.2% to 5% of kidney concentrations (e.g., Osborn et al., 1979; Cheney et al., 1981; Leonzio et al., 1986; Nielsen and Dietz, 1989). The
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present study has confirmed the very low cadmium content of muscle as, indeed, all samples were below 0.5 mg/kg dw, both for little owls and for buzzards. Cadmium content of feathers cannot be clearly ascribed to either the share deposited in growing feathers from the blood or to that on feather surfaces of atmospheric or aqueous origin (Hahn, 1991; Furness, 1996). The significant correlations observed in this research between liver and feathers and between kidney and feathers in buzzards and between kidney and feathers in little owls, however, support the hypothesis that cadmium accumulated from the diet could be excreted through the feathers. Kidneys and liver could be used to assess cadmium exposure of birds of prey, a working hypothesis substantiated by the significant correlations between liver and kidney cadmium content in both species. Liver cadmium content of healthy adult birds in wild populations is usually between one half and one tenth of the concentration in the kidney of the same bird (Lee et al., 1987; Thompson, 1990; Lock et al., 1992). Although cadmium concentrations are usually higher in kidneys, Scheuhammer (1987) advocated the use also of the liver in monitoring biological exposure to cadmium, since it accumulates about one half of the cadmium total body burden and since its cadmium content is extremely stable, probably because the liver is generally resistant to the toxic effects of cadmium (Furness, 1996). Concentrations of cadmium in the kidney, instead, can fall considerably after cadmiuminduced tubular disfunctions (White et al., 1978; Goyer et al., 1984) consequent to high exposure. Scheuhammer (1987) suggested that cadmium levels above 3 mg/kg dw in liver and above 8 mg/kg dw in kidneys might indicate an increased environmental exposure. Only two buzzards exceeded the threshold of 8 mg/kg dw cadmium in kidneys, but in general exposure did not appear to be abnormal. Biological half-life of cadmium is very long and, indeed, cadmium concentrations increase with age in both species (Table 5). Many studies have shown that cadmium concentrations are higher in adults than in juveniles or immatures, often 10 times and sometimes as much as 100 times higher in adults than in chicks (Hulse et al., 1980; Stoneburner et al., 1980; Cheney et al., 1981; Maedgen et al., 1982; Stock et al., 1989; Lock et al., 1992; Furness, 1996). Therefore, the significant differences of cadmium content observed in adults and juveniles in all tissues, except the feathers, did not come as a surprise.
5. Conclusions This analysis of lead and cadmium concentrations allows the conclusion that there is not a condition of
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abnormal exposure to cadmium, but some interesting cases suggest a condition of chronic exposure for two little owls and a clear acute exposure of one buzzard for lead. The spreading in the environment of shot and fishing weights expose many birds to lead. As Locke and Friend (1992) asserted, lead poisoning has been documented in a sufficiently wide variety of birds to consider all birds as being susceptible to intoxication after ingesting and retaining lead shot. On that basis it is reasonable to consider the case of the buzzard one of lead shot ingestion. The biological habits of the buzzards and the little owls make these species useful sentinels. They could act as local monitors of contamination levels and provide effective support for classical monitoring.
Acknowledgments Special thanks are due to Centro Recupero Rapaci of LIPU in Sala Baganza for the kind collaboration, to Messori Roberto of Agenzia Regionale Prevenzione e Ambiente, Sezione Provinciale di Reggio Emilia, Italy for technical assistance, to Chizzolini Roberto of Dipartimento di Produzioni Animali, Biotecnologie Veterinarie, Qualita` e Sicurezza degli Alimenti (Universita` di Parma, Italy) and Csermely Davide of Dipartimento di Biologia Evolutiva e Funzionale (Universita` di Parma, Italy) for the kind support, and to Consorzio Spinner (Servizi e incentivi per la ricerca e l’innovazione) for the financial support that gave the opportunity of completing this research.
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Heavy metal contamination in little owl (Athene noctua) and common buzzard (Buteo buteo) from northern Italy Alessandra Battaglia,a,* Sergio Ghidini,a Giorgio Campanini,a and Roberto Spaggiarib a
Dipartimento di Produzioni Animali, Biotecnologie Veterinarie, Qualita` e Sicurezza degli Alimenti, Facolta` di Medicina Veterinaria, Universita` di Parma,43100 Parma, Italy b Agenzia Regionale Prevenzione e Ambiente, Sezione Provinciale di Reggio Emilia, Italy Received 14 July 2003
Abstract In this study, two raptor species, the common buzzard (Buteo buteo) and the little owl (Athene noctua), were investigated for lead and cadmium concentrations, using liver, kidneys, pectoral muscle, sternum bone, and feathers. All the collected birds died at the Centro Recupero Rapaci of Lega Italiana Protezione Uccelli in Sala Baganza (Parma, Italy). They arrived alive at the Centro between November 1998 and November 1999 but died or were put to death as a consequence of injuries or other ailments. The results of the investigation do not show an excessive exposure to cadmium, whereas some interesting data have emerged in the case of lead. The concentration of the latter in the liver and in the bone of two little owls seem to suggest the possibility of chronic exposure. The high values found in one common buzzard, on the other hand, suggest an acute exposure and, probably, a case of lead shot ingestion. r 2004 Elsevier Inc. All rights reserved. Keywords: Lead; Cadmium; Little owl; Common buzzard; Shot; Sentinel species
1. Introduction The impact of heavy metals on the environment can be a serious threat for the stability of ecosystems. The spread of hunting bullets and fishing weights represents a problem of growing relevance. The use of lead shot, indeed, increases anthropogenic input of this metal into the environment and causes a very specific pollution problem, resulting in considerable avian mortality (Pain and Amiard-Triquet, 1993). Primary lead toxicosis is prevalent among waterbirds which ingest lead shot by mistaking it for grit or seeds. Secondary lead toxicosis occurs in birds of prey or other scavengers by eating animals wounded by gunfire or impaired by primary toxicosis. Furthermore, a sufficient amount of evidence is now available to conclude that the whole metallic lead in shot and sinkers is transformed into particulate and molecular Pb species, becoming dispersed in the environment to some degree (Scheuhammer and Norris, 1996). Lead oxides, carbonates, and other compounds *Corresponding author. Fax: +39-0521-032752. E-mail address: [email protected] (A. Battaglia). 0147-6513/$ - see front matter r 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ecoenv.2003.12.019
are produced by weathering of the pellets when metallic lead of spent shot or sinkers is exposed to air or water (Sever, 1993). Lead breaks down more quickly where the soil and water are acidic and full of oxygen. Lead attached to soil particles can be moved to new places by erosion. This process can result in local lead concentrations in soils and waters far in excess of normal concentrations (Scheuhammer and Norris, 1996). Cadmium has been described as one of the most dangerous trace elements in food and in the environment, not only for its high toxicity but also for its persistence. Atmospheric cadmium deposited on the earth’s crust can be absorbed or retained by soil particles and become part of biological structures. Dissolved cadmium is readily absorbed by plants and leaches rapidly into the subsoil, contaminating deep and surface waters (Cabrera et al., 1998). The transfer of cadmium from soils to the edible portions of agricultural crops is significantly greater than that of other elements (Cabrera et al., 1998). The use of sentinel species can provide interesting data to monitor the quality of the environment. Some species have biological habits that increase the
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likelihood of exposure to contaminants and, in that way, can produce relevant information that would be missed if only water or soil were analyzed. Animals at the top of the food pyramid can yield information over a large area around each sampling site, not only on bioavailability of contaminants but also on how, where, and when they are transferred within the food web (Jager et al., 1996). This research aimed at this kind of information by measuring the amounts of lead and cadmium in tissues of two raptor species: common buzzards and little owls. Common buzzards are suitable for biomonitoring for several reasons: they catch a wide range of prey, are mainly sedentary in Italy (the migrant flows of northern European birds occur in autumn and in spring), and, moreover, birds found dead can provide a sufficiently large sample. Similar to buzzards, the little owls, in Italy, are resident, they feed on a wide range of prey, and individuals found dead can provide a sufficiently large sample for analysis.
Table 1 Age, sex, and weight data of little owls
2. Materials and methods
adopted for individual identification throughout the study. The 38 little owls comprised 15 adults (9 females and 6 males) and 23 juveniles (11 females and 11 males; the sex of 1 juvenile could not be established). The 18 buzzards comprised 5 adults (4 females and 1 male), 12 juveniles (5 females and 7 males), and 1 individual of unknown age (see Tables 1 and 2). Most of the birds came from the provinces of Parma and Reggio Emilia, but some birds came also from nearby provinces (Piacenza, Modena, Mantova, Cremona, Lodi, Brescia, Alessandria, Novara, Torino, Vercelli, Pavia). Almost all little owls were collected during the summer, whereas the majority of the buzzards gathered during the winter. All carcasses were stored at 20 C. The following samples were taken from each corpse: liver, kidneys, pectoral muscle, and sternum bone. The feathers from the back were sampled also. The preparation of the dead birds and samples was carried out taking care to avoid contamination and losses as much as possible: sterile scalpels and surgical tools cleaned or substituted for each bird were used together with rubber latex gloves. The working surface was also cleaned after each operation. The samples were handled in a way to avoid any contact with external surfaces, placed individually in plastic bags, and stored at 20 C.
2.1. Collection of samples In the time period of 1 year, between November 1998 and November 1999, we collected 38 little owls (Athene noctua) and 18 common buzzards (Buteo buteo), hereafter called buzzard. All raptors came from Centro Recupero Rapaci of Lega Italiana Protezione Uccelli in Sala Baganza (Parma, Italy). The birds had been brought to the Centro alive but injured or debilitated for various reasons. The birds died naturally later or were euthanized soon after admission with Tanax (Intervet Italia s.r.l.) by the veterinary of the Centro when their health state did not indicate potential recovery. The main cause of death, for both species, was classified as different kinds of trauma. Frequently the birds were injured by collision with a vehicle or with power lines or by lead shot. The last kind of trauma concerned essentially the buzzards: 5 of 18 buzzards were shot according to the notes of admission in the Centro. In general, the main causes of admission in the Centro were fractures and luxations due to traumas. A choice was made to use for the study only those birds that had not been held at the Centro more than 1 month. The average period of stay in the Centro of the chosen birds, however, was about 1 week. The diet provided during this period was composed only of dead chicks coming from chicken farms. The following data were gathered for each bird: sex, age, weight, cause of death, area of origin, date of arrival, and date of death. The file number given to each bird at the time of admission to the Centro has been
Age/sex
Adult/female Adult/male Juvenile/female Juvenile/male
No.
9 6 11 11
Weight (g) Min.
Max.
Median
Mean
113 125 91 66
174 183 172 148
154 164.5 136 97
148.2 155.8 135.2 100.5
Table 2 Age, sex, and weight data of buzzards Age/sex
Adult/female Adult/male Juvenile/female Juvenile/male
No.
4 1 5 7
Weight (g) Min.
Max.
Median
Mean
579 582 605 420
800 582 860 986
769 582 640 559
729.3 582 683 676.1
2.2. Preparation and analysis of the samples Samples were thawed and dried in air for 24 h at 105 C. The dried material was joined together in a mortar with the exception of the feathers, which were digested as such. About 0.25 g were weighed directly in
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the digestion tubes and digested in a microwave oven (Milestone MEGA 1200), with 3 mL of HNO3 and 0.5 mL of H2O2. Lead content was determined with a Perkin–Elmer 2100 atomic absorption spectrophotometer, equipped with a graphite furnace atomizer. The detection limit was 0.20 mg/kg dry weight. Cadmium analysis was carried out with a Perkin–Elmer Analyst 600 graphite furnace atomic absorption spectrophotometer, equipped with Zeeman background correction. The detection limit was 0.003 mg/kg dry weight. Each analysis was carried out in duplicate. 2.3. Statistical analysis A nonparametric approach to the analysis of the data was necessary, because of skewness of the distributions of heavy metals concentrations. The difference between adults and juveniles was tested using Mann–Whitney U test and the correlation among tissue concentrations with Kendall’s t partial correlation coefficient. Significance was considered at 0.05 probability level. For mathematical reasons, a value of half the detection limit was given to data points below the detection limit.
3. Results Lead and cadmium concentrations are presented in Tables 3 and 4 expressed as mg/kg dry weight (dw). The analyses were performed on dry tissues because dry weight values are more reliable and consistent than wet weight values (Adrian and Stevens, 1979). Due to the skewness of the distribution the results are expressed as median with minimum and maximum values also presented; the maximum values are expressed as mean7standard deviation. Median lead contents of little owls ranged from a minimum of 0.1 mg/kg dw in the muscle to 2 mg/kg dw Table 3 Lead and cadmium concentrations (mg/kg dw) in little owls Median
Min.
Max.
Lead Liver Kidney Bone Muscle Feather
0.35 0.50 0.88 0.10 2.00
o0.20 o0.20 o0.20 o0.20 o0.20
11.970.87 2.9570.42 17.970.23 0.7270.01 19.170.18
Cadmium Liver Kidney Bone Muscle Feather
0.050 0.040 0.010 o0.003 0.050
o0.003 o0.003 o0.003 o0.003 0.017
2.62070.040 7.48070.230 0.13070.002 0.42070.020 0.69070.010
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Table 4 Lead and cadmium concentrations (mg/kg dw) in common buzzards Median
Min.
Max.
Lead Liver Kidney Bone Muscle Feather
0.95 0.75 1.87 o0.20 1.48
o0.20 o0.20 0.28 o0.20 o0.20
47.773.82 10.870.94 42.072.83 19.470.63 8.8770.96
Cadmium Liver Kidney Bone Muscle Feather
0.010 0.620 0.010 o0.003 0.060
0.01770.001 0.02370.001 o0.003 o0.003 0.018
2.02070.040 12.1270.590 0.06070.001 0.42070.010 0.37070.004
in the feathers. Seven little owls had lead concentrations in the liver between 6 and 20 mg/kg dw. Two of them, with liver lead contents of 9.3270.68 and 11.7570.85 mg/kg dw, had high lead concentrations in the bone (17.9170.23 and 12.1570.15 mg/kg dw, respectively). Two other little owls had lead concentrations in the bone (6.3270.16 and 9.0570.29 mg/kg dw) that suggest high environmental contamination. Lead concentrations in the kidneys were lower than 3 mg/kg dw in all cases and only two little owls with 2.5670.02 and 2.9570.42 mg/kg dw were close to 3 mg/ kg dw. Muscle lead content never exceeded 1 mg/kg dw. The highest lead values in the feathers were 18.2870.13 and 19.0670.18 mg/kg dw. Median values of lead content in buzzards ranged from 0.2 mg/kg dw in muscle to 1.87 mg/kg dw in bone and, with the exception of feathers, median values were higher than those of little owls. The same pattern applies to maximum values. Two buzzards had lead concentrations in the liver of 7.2870.53 and 6.2170.45 mg/kg dw. Two other buzzards had liver lead concentrations 420 mg/kg dw. One of them had 47.7073.82 mg/kg dw lead in the liver, 6.6070.57 mg/ kg dw in the kidneys, and 4272.83 mg/kg dw in the bone. The same bird had the highest value in the feathers (8.8770.96 mg/kg dw) among the buzzards. A second buzzard, with 7.5970.16 mg/kg dw lead in the feathers, ranked very close to the previous one. The second buzzard with liver lead concentration 420 mg/kg dw (20.4571.49 mg/kg dw) had 10.757 0.94 mg/kg dw lead in the kidneys and 16.1070.87 mg/ kg dw lead in the bone. This bird, however, had been shot and the presence of lead fragments remains a possibility. The work plan of the present study did not include X-ray radiography nor digestive tract examination but relied only on the notes of admission to the Centro. The same doubt remains for two other shot animals; one had high lead concentrations in the muscle
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(19.3970.63 mg/kg dw) and in the bone (27.6670.76 mg/ kg dw) and the other had high lead concentration only in the muscle (11.2270.14 mg/kg dw). Cadmium contents of little owls ranged from a median value close to the detection limit for the muscle to 0.05 mg/kg dw in liver and feathers. Liver cadmium concentrations of little owls never exceeded 3 mg/kg dw. Just one bird got close to such a value with 2.6270.04 mg/kg dw. Cadmium concentrations in the kidneys were lower than 8 mg/kg dw. The highest value observed in one little owl was 7.4870.23 mg/kg dw. Lead content of muscles, feathers, and bones was lower than 1 mg/kg dw in all cases. Median cadmium values in buzzards were lowest in muscle, as in little owls, and highest in kidneys. Two birds had cadmium concentrations in kidneys over 8 mg/ kg dw: one with 8.6270.42 mg/kg dw and one with 12.1270.59 mg/kg dw. Cadmium in the liver showed a maximum value of 2.02 mg/kg dw and in muscles, bones, and feathers it never exceeded 0.5 mg/kg dw. No significant difference was observed in metal content of adult and juvenile buzzards, whereas highly significant differences in cadmium content of liver, kidneys, and muscle were observed in adult and juvenile little owls (Table 5). The existence of a statistical relationship between metal contents in different tissues was studied by means of simple correlation coefficients. In little owls (Table 6) a highly significant r value was observed for liver versus kidney cadmium content. The same applies for buzzards (Table 7) but in this species r was highly significant also
Table 5 Significant differences between adult and juvenile little owls Metal
Tissue
P
Lead
Bone
0.015
Cadmium
Liver Kidney Muscle Bone
0.0001 0.0001 0.0001 0.012
Po0:05: Po0:01:
Table 6 Significant correlations between tissues in little owls Metal
Tissues
P
Lead
Bone and liver Bone and feathers
0.017 0.019
Cadmium
Kidney and liver Kidney and feathers
0.0001 0.014
Po0:05: Po0:01:
Table 7 Significant correlations between tissues in buzzards Metal
Tissues
P
Lead
Liver and kidney
0.004
Cadmium
Liver and kidney Liver and feathers Kidney and feathers
0.0001 0.049 0.005
Po0:05: Po0:01:
for lead content of liver versus kidneys and for cadmium content of kidneys versus feathers.
4. Discussion Shot are the only widespread source of lead likely to result in lead poisoning in raptors as they can be carried in the flesh of dead or injured prey. Acute lead poisoning can ensue in the case of ingestion of a large number of shot (10 or more) and birds usually die within a few days. More commonly, birds die of chronic lead poisoning following ingestion of a smaller number of shot (Scheuhammer and Norris, 1996). Ingested shot dissolve in the acid environment of the avian stomach and are absorbed into the bloodstream through the wall of the digestive system. Lead shot that become embedded in tissues of birds that are not killed, instead, are not solubilized except when they penetrate into the lumen of the gizzard or proventriculus (Kendall et al., 1996). Liver and kidney concentrations are primarily considered indexes of a recent exposure, whereas bone contents reflect chronic exposure. The significant difference between adult and juvenile little owls observed for lead content in the bone shows the tendency of this tissue to hoard the metal in the long term. Feathers can play the role both of storing and of eliminating metals. Metal levels in feathers reflect blood levels during the short period of feather growth, when the feather is connected with blood vessels and metals are incorporated in the keratin structure (Dauwe et al., 2000). This is not the only factor to take into account, though. Indeed, feathers can also measure external contamination. The toxicological consequences of lead shot ingestion are dependent, however, on different variables (e.g., condition of the animal, gender, age, diet, and climate). Previous studies revealed that liver lead concentrations found in raptors not diagnosed as having died of lead poisoning were generally o2 mg/kg dw and often o1 mg/kg dw. Such values represent a normal exposure to background levels and are not sufficient to severely impair normal biological functioning. Concentrations
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between 6 and 20 mg/kg dw are signs of exposure levels higher than background exposure and external signs of poisoning may be present. Higher concentrations are associated with acute exposure and are immediately life threatening. Liver lead concentrations 420 mg/kg dw almost certainly result from shot ingestion and have been reported in species most likely to be exposed to this source of lead (Pain et al., 1994). Jager et al. (1996) reported that 10 mg/kg dw lead in kidneys correspond to environmental pollution. Scheuhammer (1987) suggested that lead levels above 5 mg/kg dw in bones correspond to a high level of environmental contamination. The first buzzard mentioned in the previous section with 47.7073.82 mg/kg dw lead in the liver, 6.6070.57 mg/kg dw in the kidneys, and 4272.83 mg/ kg dw in the bone is probably a case of acute exposure. The bird was not shot but when it was admitted to the Centro Recupero Rapaci it was undernourished and suffered from paresis of the legs and strong contraction of the talons interpreted as nerve damage consequent to tetanus. Common buzzards catch a wide range of prey: their diet includes small mammals, birds, amphibians, reptiles, and insects. Little owls also feed on a wide range of prey, particularly small mammals and invertebrates, e.g., earthworms (Lumbricidae), and sometimes reptiles, amphibians, and small birds. Buzzards act often as scavengers and, in this way, are more likely than little owls to be exposed to lead shot in small game species. This could explain the correlation between concentrations of lead in liver and kidney in buzzards since such tissues are the first targets of the metal and, as mentioned above, are index of recent exposure. In the little owls of our study, instead, the correlations with the tissues index of a chronic exposure (bone and feathers) was significant. It is more difficult to determine the origin of lead exposure when liver concentration is lower than the values expected from acute exposure. Concentrations between 6 and 20 mg/kg dw could result from shot having been in the stomach for only a short time (before regurgitation) or from the remnant of a larger exposure which had taken place in previous weeks or months (Pain et al., 1994). The two little owls with liver lead contents of 9.3270.68 and 11.7570.85 mg/kg dw and bone lead concentrations of 17.9170.23 and 12.1570.15 mg/kg dw, respectively, had probably been exposed for a long time to lead pollution. Cadmium concentrations in birds are generally reported to be highest in kidneys, lower in liver, and very low in muscle (Nicholson, 1981; Thompson, 1990). A few reports show muscle cadmium concentrations in adult birds to be around 0.2% to 5% of kidney concentrations (e.g., Osborn et al., 1979; Cheney et al., 1981; Leonzio et al., 1986; Nielsen and Dietz, 1989). The
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present study has confirmed the very low cadmium content of muscle as, indeed, all samples were below 0.5 mg/kg dw, both for little owls and for buzzards. Cadmium content of feathers cannot be clearly ascribed to either the share deposited in growing feathers from the blood or to that on feather surfaces of atmospheric or aqueous origin (Hahn, 1991; Furness, 1996). The significant correlations observed in this research between liver and feathers and between kidney and feathers in buzzards and between kidney and feathers in little owls, however, support the hypothesis that cadmium accumulated from the diet could be excreted through the feathers. Kidneys and liver could be used to assess cadmium exposure of birds of prey, a working hypothesis substantiated by the significant correlations between liver and kidney cadmium content in both species. Liver cadmium content of healthy adult birds in wild populations is usually between one half and one tenth of the concentration in the kidney of the same bird (Lee et al., 1987; Thompson, 1990; Lock et al., 1992). Although cadmium concentrations are usually higher in kidneys, Scheuhammer (1987) advocated the use also of the liver in monitoring biological exposure to cadmium, since it accumulates about one half of the cadmium total body burden and since its cadmium content is extremely stable, probably because the liver is generally resistant to the toxic effects of cadmium (Furness, 1996). Concentrations of cadmium in the kidney, instead, can fall considerably after cadmiuminduced tubular disfunctions (White et al., 1978; Goyer et al., 1984) consequent to high exposure. Scheuhammer (1987) suggested that cadmium levels above 3 mg/kg dw in liver and above 8 mg/kg dw in kidneys might indicate an increased environmental exposure. Only two buzzards exceeded the threshold of 8 mg/kg dw cadmium in kidneys, but in general exposure did not appear to be abnormal. Biological half-life of cadmium is very long and, indeed, cadmium concentrations increase with age in both species (Table 5). Many studies have shown that cadmium concentrations are higher in adults than in juveniles or immatures, often 10 times and sometimes as much as 100 times higher in adults than in chicks (Hulse et al., 1980; Stoneburner et al., 1980; Cheney et al., 1981; Maedgen et al., 1982; Stock et al., 1989; Lock et al., 1992; Furness, 1996). Therefore, the significant differences of cadmium content observed in adults and juveniles in all tissues, except the feathers, did not come as a surprise.
5. Conclusions This analysis of lead and cadmium concentrations allows the conclusion that there is not a condition of
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abnormal exposure to cadmium, but some interesting cases suggest a condition of chronic exposure for two little owls and a clear acute exposure of one buzzard for lead. The spreading in the environment of shot and fishing weights expose many birds to lead. As Locke and Friend (1992) asserted, lead poisoning has been documented in a sufficiently wide variety of birds to consider all birds as being susceptible to intoxication after ingesting and retaining lead shot. On that basis it is reasonable to consider the case of the buzzard one of lead shot ingestion. The biological habits of the buzzards and the little owls make these species useful sentinels. They could act as local monitors of contamination levels and provide effective support for classical monitoring.
Acknowledgments Special thanks are due to Centro Recupero Rapaci of LIPU in Sala Baganza for the kind collaboration, to Messori Roberto of Agenzia Regionale Prevenzione e Ambiente, Sezione Provinciale di Reggio Emilia, Italy for technical assistance, to Chizzolini Roberto of Dipartimento di Produzioni Animali, Biotecnologie Veterinarie, Qualita` e Sicurezza degli Alimenti (Universita` di Parma, Italy) and Csermely Davide of Dipartimento di Biologia Evolutiva e Funzionale (Universita` di Parma, Italy) for the kind support, and to Consorzio Spinner (Servizi e incentivi per la ricerca e l’innovazione) for the financial support that gave the opportunity of completing this research.
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