Accumulation of Lead,Zinc, and Cadmium in a Wild Population of <Emphasis Type="Italic">Clethrionomys glareolus</Emphasis> from an Abandoned Lead Mine

Lead, zinc, and cadmium were determined in a range of tissues from wild populations of bank voles (Clethrionomys glareolus) trapped on an abandoned metalliferous mine site and a reference site. Estimated dietary intakes indicated that animals were exposed to elevated levels of all three metals at the mine site, and this was generally reflected in metal residues in body tissues. Lead concentrations were significantly higher in all tissues of animals from the mine compared to the reference site, while Cd was higher only in the kidney. There was evidence of age-accumulation (using total body weight as an index of age) of Cd in both the liver and kidney of mine site animals but no evidence of such accumulation of lead in bone. In contrast to Cd and Pb, Zn was lower in the tissues of mine site animals compared to the reference site. Based on critical tissue concentrations, the ecotoxicological risk to a wild population of bank voles (Clethrionomys glareolus), associated with total substrate levels of 1 μg g⁻¹ dry weight Cd and 700 μg g⁻¹ dry weight Zn at this mine site is negligible, but that associated with 4000 μg g⁻¹ dry weight Pb may be considered significant. Received: 28 January 2002/Accepted: 29 July 2002     

Differential Susceptibility to Cadmium-Induced Liver and Kidney Injury in Wild and Laboratory-Bred Bank Voles Myodes glareolus

The objective of the study was to compare the sensitivity of wild and laboratory-bred bank voles to cadmium (Cd)-induced histopathological changes in the liver and kidneys. For 4 weeks, the male bank voles—both wild and laboratory-bred—were provided with diet containing Cd in quantities <0.1 (control), 30, and 60 μg/g dry weight. At the end of exposure period, histopathology and analyses of Cd, metallothionein (MT), glutathione (GSH), zinc (Zn), copper (Cu), iron (Fe), and lipid peroxidation—all considered to be critical factors during the development of Cd toxicity in the liver and kidneys—were carried out. Histopathological changes (focal hepatocyte swelling, vacuolation and inflammation [leukocyte infiltration] in the liver, and focal proximal tubule degeneration [including epithelial cell swelling] in the kidneys) occurred only in the wild bank voles fed a diet containing 60 μg Cd/g. There were no differences in concentrations of Cd, MT, GSH, Zn, and Cu in liver and kidney between the respective groups of wild and laboratory-bred animals. However, a decrease of hepatic Fe and lipid peroxidation was observed in the wild voles exhibiting histopathological changes. These data indicate the following: (1) wild bank voles are more susceptible to Cd-induced liver and kidney injury than those bred and raised in the laboratory; (2) the difference in sensitivity may be associated with a distinct decrease of hepatic Fe in response to Cd exposure between the two groups of bank voles; and (3) dietary Cd may produce histopathological changes indirectly through decreasing the hepatic Fe and Fe-dependent oxidative processes. These results also suggest that histopathology in the liver and kidney of wild bank voles living in a contaminated environment may occur at relatively low levels of tissue Cd.     

Histopathological changes in the liver, kidneys, and testes of bank voles environmentally exposed to heavy metal emissions from the steelworks and zinc smelter in Poland

Bank voles were trapped in the neighborhood of the Sendzimir steelworks in Krakow and the ZGH Boleslaw zinc smelter in Bukowno. The Borecka forest in the north of Poland served as a control area. Lead, cadmium, zinc, and iron concentrations were analyzed in the liver, kidneys, testes, and femur bones of the bank voles. Typically, high levels of lead and cadmium were found in the bones and kidneys, respectively. In the femurs of the rodents from Bukowno, 109.26 microg g(-1) dry weight of lead was detected. The kidneys of these animals had accumulated 32.98 microg g(-1) cadmium. Concentrations of zinc and iron in the tissues were at physiological levels. No damage was found in the tissues of the bank voles from the Borecka forest or in the testes of animals from other areas. Histopathological changes in the kidneys of the rodents from Krakow as well as changes to the liver and kidneys of the animals from Bukowno were demonstrated.     

A minority of seropositive wild bank voles (Clethrionomys glareolus) show evidence of current Puumala virus infection.

Bank voles (Clethrionomys glareolus) serve as the reservoir for Puumala (PUU) virus, the aetiologic agent of nephropathia epidemica. The animals are believed to be persistently infected and the occurrence of serum antibodies is usually taken as an evidence of active infection. We found serum antibodies to PUU virus in 42 of 299 wild bank voles captured in a PUU virus endemic area. PUU virus RNA was demonstrated in lung specimens of 11 of these 42 animals and in 2 of them antigen was also found. Thus in the lungs of 31 of 42 seropositive animals neither PUU virus RNA nor antigen was detected. In 2 of 257 seronegative animals, lung specimens showed presence of PUU virus antigen and RNA. Isolation of PUU virus from lung tissue was successful in all 4 antigen-positive bank voles but in none of 16 tested antigen-negative animals. In conclusion, only a minority of bank voles with serum antibodies to PUU virus showed evidence of current infection.     

Joint effects of dietary cadmium and polychlorinated biphenyls on metallothionein induction, lipid peroxidation and histopathology in the kidneys and liver of bank voles

Free-living bank voles have been shown to be more sensitive to cadmium (Cd) toxicity than the rodents exposed to Cd under laboratory conditions. The present study was designed to find out whether polychlorinated biphenyls (PCBs), common environmental co-contaminants, increase susceptibility to Cd toxicity through inhibition of metallothionein (MT) synthesis-a low molecular weight protein that is considered to be a primary intracellular component of the protective mechanism. For 12 weeks, the male bank voles were provided with diets containing Cd (0.05 microg/g (control) and 10 microg/g dry wt) and PCBs (0, 10 and 50 microg/g dry wt) alone or in combination under long (16 h) and short (8 h) photoperiods. At the end of exposure period, histological examinations and analyses of MT, Cd, Fe and lipid peroxidation in the kidneys and liver were carried out. Dietary PCBs did not affect Cd inducibility of renal MT, but decreased it significantly in the liver; however, no signs of Cd toxicity (measured by histopathology) occurred in both organs. On the contrary, PCBs at the highest dose increased significantly lipid peroxidation in the kidneys and liver (4-fold) only in the bank voles raised under a long photoperiod; the PCB-induced hepatic lipid peroxidation was accompanied by extensive histopathological changes including hepatocyte enlargement, necrosis and steatosis. Co-treatment with dietary Cd significantly suppressed the increase in lipid peroxidation and apparently reduced hepatic damage. These data indicate that (1) dietary PCBs do not enhance Cd toxicity in the kidneys and liver of bank voles and (2) dietary Cd suppresses PCB-induced hepatotoxicity that appears to be photoperiod-dependent.     

Effect of soil pollution with metallic lead pellets on lead bioaccumulation and organ/body weight alterations in small mammals

Using small mammals as bioindicators, the bioavailable status and ecotoxicity of lead was investigated in an acidic sandy soil environment polluted with metallic lead pellets from shotgun ammunition. Average concentrations of lead in kidney, liver and bone tissue of wood mice (Apodemus sylvaticus), bank voles (Clethrionomys glareolus), and shrews (Sorex araneus) were strongly elevated, compared to tissue levels of conspecifics collected from an adjacent unpolluted area. All shrews and some bank voles collected from the shooting range exceeded the critical renal Pb concentration of 25 g/g dry weight, considered diagnostic of lead intoxication in mammals. The geometric mean renal Pb concentration in shrews was 270 g/g dry weight, with an upper range of more than 1,000 g/g. The population of shrews and bank voles from the shooting range also showed a significantly increased average relative kidney weight (kidneyto-body weight ratio), which is indicative of lead poisoning. The results suggest that metallic lead pellets deposited in an acidic sandy soil are transformed to a chemical form of lead, probably Pb²⁺, which is toxic to organisms and which can readily enter the terrestrial food chain.     

Serological evidence for the reservoir hosts of cowpox virus in British wildlife.

The reservoir host of cowpox virus in Western Europe is not known, but epidemiological evidence from human and feline infections indicates that the virus is probably endemic in small wild rodents. Therefore, serum and tissue samples were collected from a variety of wild British mammals and some birds, and tested for evidence of Orthopoxvirus infection. Antibody reacting with cowpox virus was detected in 9/44 (20%) bank voles (Clethrionomys glareolus), 8/24 (33%) field voles (Microtus agrestis), 17/86 (20%) wood mice (Apodemus sylvaticus) and 1/44 house mice (Mus musculus), but in no other animal species tested. Although virus was not isolated from any animal, this serological survey, together with other evidence, suggests that bank and field voles and wood mice are the main reservoir hosts of cowpox virus in Great Britain.     

Toxicity and bioaccumulation of lead and cadmium in marine protozoan communities

The behavior of lead and cadmium in a protozoan community was studied in order to obtain new data regarding the toxicity and bioaccumulation of these heavy metals. For this purpose, microcosms with different concentrations of the pollutants (without metals, 500 microg Cd and Pb x L(-1) 1,000 microg Cd and Pb x L(-1)) were used. Protozoans bioaccumulated 7.03-207.00 microg Pb x g(-1) dry weight (dw) and 0.05-332.75 microg Cd x g(-1) dw, representing an accumulation capacity of up to 161.45 microg Pb x g(-1) dw and 310.75 microg Cd x g(-1) dw more than that of the bacteria. The addition of both metals caused a significant reduction in the density of protozoans. These data were compared with those obtained previously in treatments that used these metals separately.     

Reservoir animals for nephropathia epidemica in Norway: indications of a major role for the bank vole (C. glareolus) in comparison with the woodmouse (A. sylvaticus)

Small rodents were collected live in two different locations within a nephropathia epidemica (NE) endemic area, and tested for both antiviral serum antibodies and viral antigens in lung sections. In one location, only Apodemus sylvaticus (woodmice) were found in the traps, in the other, both A. sylvaticus and Clethrionomys glareolus (bank voles) were collected. Among the woodmice from the former location the prevalence of NE virus markers was significantly lower than for either woodmice or bank voles from the other location, and no NE antigen-positive animals was found. The woodmice co-existing with bank voles had a lower prevalence of NE antigen and antibodies than the bank voles, and fewer woodmice had both antibodies and antigen. The results emphasize the important role of bank voles as a major NE virus reservoir and probable source of human infections.     

Genetic similarity of Puumala viruses found in Finland and western Siberia and of the mitochondrial DNA of their rodent hosts suggests a common evolutionary origin

A total of 678 small mammals representing eight species were trapped in western Siberia in 1999-2000 and assayed for the presence of hantaviruses. Eighteen animals, all Clethrionomys species, were antigen positive by enzyme-linked immunosorbent assay (ELISA). Small and medium genome segments were recovered by RT-PCR from six samples from Clethrionomys glareolus and three from Clethrionomys rufocanus. Sequence comparison and phylogenetic analysis revealed that these hantaviruses were Puumala virus and were similar to hantavirus strains from Finland. To confirm these data, partial nucleotide sequences of the rodent hosts' cytochrome b genes were obtained, as well as several sequences from genes from rodents trapped at different localities of European Russia and western Siberia. The cytochrome b sequences of Siberian bank voles were similar to sequences of C. glareolus, trapped in Finland. These data suggest that the Puumala hantaviruses, as well as their rodent hosts, share a common evolutionary history. We propose that these rodents and viruses may be descendents of a population of bank voles that expanded northward from southern refugia during one of the interglacial periods.     

Experimental exposure of naive bank voles (Clethrionomys glareolus) to the Chornobyl, Ukraine, environment: a test of radioresistance

Previous studies have demonstrated no difference in micronucleus (MN) frequencies between wild rodents chronically exposed to the environmental radiation contamination of the Chornobyl (Ukraine) exclusion zone and those inhabiting reference populations. The aim of the present study was to test the hypothesis that a population of bank voles (Clethrionomys glareolus) has developed radioresistance as a result of 14 years of chronic, low-dose radiation exposure. Naive voles were placed in environmental enclosures in the Red Forest region of the exclusion zone for 30 d. Blood samples were obtained at regular intervals, and the MN assay was used to assess chromosomal damage. Additionally, radionuclide uptake was monitored throughout the study, and dose was documented for each individual as well as for their offspring. Total dose for the voles experimentally exposed in this environment averaged 1.09 Gy (36.20 mGy d(-1)) for the 30-d study period. Our results indicate that exposure to radiation levels well above regulatory statutes did not result in an increased MN frequency. Furthermore, our results do not support the hypothesis that voles chronically exposed to these radiation levels have developed a genetic basis for radioresistance that is unique from that present in naive populations. The use of C. glareolus as a sentinel species for environmental studies of radiation contamination and the question of whether the MN assay is an appropriate endpoint for studies of low-dose, chronic radiation exposure are also discussed.     

Zinc and lead poisoning in wild birds in the tri-state mining district (Oklahoma, Kansas, and Missouri)

The Tri-State Mining District (Oklahoma, Kansas, and Missouri) is contaminated with Pb, Cd, and Zn from mining, milling and smelting. Metals have been dispersed heterogeneously throughout the District in the form of milled mine waste ("chat"), as flotation tailings and from smelters as aerial deposition or slag. This study was conducted to determine if the habitat has been contaminated to the extent that the assessment populations of wild birds are exposed to toxic concentrations of metals. American robins (Turdus migratorius), northern cardinals (Cardinalis cardinalis), and waterfowl had increased Pb tissue concentrations (p < 0.05) compared with Pb tissue concentrations from reference birds, and the exposure of songbirds to Pb was comparable with that of birds observed at other sites severely contaminated with Pb. Mean activities of the Pb-sensitive enzyme delta-aminolevulinic acid dehydratase (ALAD) were decreased by >50% in red blood cells in these birds (p < 0.05). Several birds had tissue concentrations of Pb that have been associated with impaired biological functions and external signs of poisoning. Cadmium was increased in kidneys of songbirds (p < 0.05), but no proximal tubule cell necrosis associated with Cd poisoning was observed. Zinc concentrations in liver and kidney of waterfowl were significantly higher (p < 0.05) than reference values. The increased environmental concentrations of Zn associated with mining in the District accounted for the pancreatitis previously observed in five waterfowl from the District. The District is the first site at which free-flying wild birds have been found to be suffering severe effects of Zn poisoning.     

Telescopium telescopium as potential biomonitors of Cu, Zn, and Pb for the tropical intertidal area

The distributions of Cu, Zn, and Pb concentrations in the selected soft tissues (foot, cephalic tentacle, mantle, muscle, gill, digestive caecum, and remaining soft tissues) and shells of the mud-flat snail Telescopium telescopium were determined in snails from eight geographical sites in the south-western intertidal area of Peninsular Malaysia. Generally, the digestive caecum compared with other selected soft tissues, accumulated higher concentration of Zn (214.35+/-14.56 microg/g dry weight), indicating that the digestive caecum has higher affinity for the essential Zn to bind to metallothionein. The shell demonstrated higher concentrations of Pb (41.23+/-1.20 microg/g dry weight) when compared to the selected soft tissues except gill from Kuala Sg. Ayam (95.76+/-5.32 microg/g dry weight). The use of different soft tissues also can solve the problem of defecation to reduce error in interpreting the bioavailability of heavy metals in the intertidal area.     

Variation in mitochondrial DNA control region haplotypes in populations of the bank vole, Clethrionomys glareolus, living in the Chernobyl environment, Ukraine

Bank vole, Clethrionomys glareolus, specimens have been annually sampled from the radioactive Chernobyl, Ukraine, environment and nonradioactive reference sites since 1997. Exposed voles continually exhibit increased mitochondrial DNA haplotype (h) and nucleotide diversity (ND), observed in the hypervariable control region (1997-1999). Increased maternal mutation rates, source-sink relationships, or both are proposed as hypotheses for these differences. Samples from additional years (2000 and 2001) have been incorporated into this temporal study. To evaluate the hypothesis that an increased mutation rate is associated with increased h, DNA sequences were examined in a phylogenetic context for novel substitutions not observed in haplotypes from bank voles from outside Ukraine or in other species of Clethrionomys. Such novel substitutions might result from in situ mutation events and, if largely restricted to samples from radioactive environments, support an increased maternal mutation rate in these areas. The only unique substitution meeting this criterion was found in an uncontaminated reference site. All other substitutions are found in other haplotypes of the bank vole or in other species. Increased maternal mutation rates do not appear to explain trends in h and ND observed in northern Ukraine. Studies examining ecological dynamics will clarify the reasons behind, and significance of, increased levels of h in contaminated areas.     

Metal and metallothionein concentrations in Scoter (Melanitta spp.) from the Pacific northwest of Canada, 1989-1994

Eighty-six surf ( Melanitta perspicillata) and nine white winged (M. fusca) scoters were collected from 1989-1994 at 11 locations in British Columbia and the Yukon. Their kidney and liver tissues were analyzed for cadmium (Cd), copper (Cu), zinc (Zn), and metallothionein (MT) concentrations. Individual kidney Cd values ranged from 2.4 microg/g dry weight (DW) in birds from northern Vancouver Island to 390.2 microg/g (DW) in birds from the Queen Charlotte Islands, which is in the range of values potentially associated with kidney damage. Birds from the Queen Charlotte Islands also had high kidney Zn concentrations, which were significantly higher than values in birds from Naniamo and Westham Island on the south coast of BC. Cd values were significantly (p < 0.001) correlated with both Zn and MT concentrations in kidney tissue (r = 0.66 and 0.62, respectively). Male surf scoters had significantly higher kidney Cd and Zn levels than females, with mean Cd values of 47.3 and 19.7 microg/g DW (p < 0.002) for males and females, respectively. Mean Zn values were 120.8 and 108.0 microg/g DW (p < 0.05) for males and females, respectively. However, no sex differences were observed for either Cu or MT concentrations in kidney tissue. Individual MT values ranged from 2.7 to 416.8 microg/g wet weight (WW). Individual kidney Cu values ranged from 15.1 to 48.4 microg/g DW for both sexes. Kidney and liver Cd concentrations were significantly correlated (r = 0.90, p < 0.05) with kidney levels almost always higher than liver values. Although Cd accumulation by the Skidegate scoters was high, comparable tissue Cd values have been documented in other seabirds collected from the same general area, indicating elevated Cd concentrations in marine food chains around the Queen Charlotte Islands (Haida Gwaii) region of the Pacific coast.     

Reservoir animals for nephropathia epidemica in Norway: indications of a major role for the bank vole (C. glareolus) in comparison with the woodmouse (A. sylvaticus).

Small rodents were collected live in two different locations within a nephropathia epidemica (NE) endemic area, and tested for both antiviral serum antibodies and viral antigens in lung sections. In one location, only Apodemus sylvaticus (woodmice) were found in the traps, in the other, both A. sylvaticus and Clethrionomys glareolus (bank voles) were collected. Among the woodmice from the former location the prevalence of NE virus markers was significantly lower than for either woodmice or bank voles from the other location, and no NE antigen-positive animals was found. The woodmice co-existing with bank voles had a lower prevalence of NE antigen and antibodies than the bank voles, and fewer woodmice had both antibodies and antigen. The results emphasize the important role of bank voles as a major NE virus reservoir and probable source of human infections.     

Seasonal variability in cadmium, lead, copper, zinc and iron concentrations in the three major fish species, Oreochromis niloticus, Lates niloticus and Rastrineobola argentea in Winam Gulf, Lake Victoria: impact of wash-off into the lake

Trace metals Cadmium (Cd), Lead (Pb), Copper (Cu), Zinc (Zn) and Iron (Fe) were analyzed in edible portions of three main finfish species namely Lates niloticus, Oreochromis niloticus and Rastrineobola argentea sampled from various beaches of Winam Gulf, Lake Victoria, Kenya, in order to determine any seasonal and site variations and the results showed significantly (p < 0.05) higher mean concentrations of Cd, Cu, Zn and Fe during the wet season compared to the dry season for all the three species indicating the impact of wash-off into the lake during the rainy periods. The overall mean concentrations of the heavy metals (in μg/g dry weight) in all combined samples ranged from 0.17–0.40 (Cd), 0.47–2.53 (Pb), 2.13–8.74 (Cu), 28.9–409.3 (Zn) and 31.4–208.1 (Fe), respectively. It was found that consumption of Rastrineobola argentea can be a significant source of heavy metals especially Zn, to humans, compared with Lates niloticus and Oreochromis niloticus, if only the muscle parts of the latter two are consumed.     

Uptake of lead, cadmium, and other metals in the liver and kidneys of cattle near a lead-zinc mine in Kabwe, Zambia

Concentrations of lead, cadmium, and other metals in the liver and kidneys of cattle near a lead-zinc mine in Kabwe (Zambia), which is ranked among the 10 worst polluted places on earth, were compared with other Zambian towns. Metal concentrations were measured in the liver and kidneys of 51 cattle from Kabwe and other Zambian towns. The maximum metal concentrations, expressed in mg/kg and dry weight, in the liver or kidneys were 398.4 (Cu), 252.6 (Zn), 77.81 (Cr), 19.37 (Cd), 7.57 (Ni), 1.8 (Pb), 1.04 (Co), 0.112 (Hg), and 0.05 (As). Concentrations of Pb and Cd in Kabwe cattle were higher than levels in other Zambian towns. The mean concentration of Cd exceeded benchmark values in offal destined for human consumption. Levels of Ni and Cr may also pose public health concerns. Concentrations of Pb and Cr, Pb and Cu, Cd and Zn, Cd and Hg, Zn and Cu, Cu and Co, as well as Co and Ni were positively correlated. The present study also highlighted the dangers of exposure of animals and humans to a mixture of toxic metals.     

Excretion of vancomycin-resistant enterococci by wild mammals

A survey of fecal samples found enterococcal excretion in 82% of 388 bank voles (Clethrionomys glareolus), 92% of 131 woodmice (Apodemus sylvaticus), and 75% of 165 badgers (Meles meles). Vancomycin-resistant enterococci, all Enterococcus faecium of vanA genotype, were excreted by 4.6% of the woodmice and 1.2% of the badgers, but by none of the bank voles.     

Photoperiod affects hepatic and renal cadmium accumulation, metallothionein induction, and cadmium toxicity in the wild bank vole (Clethrionomys glareolus)

The objective of this study was to examine the toxic effects of dietary cadmium (Cd) on bank voles, being the F1 offspring of a wild-caught population. For 6 weeks, the rodents were provided with diets containing 0.05 (control), 40, 80, and 120 microg Cd/g dry wt of diet under moderate (12 h) and long (16 h) photoperiods. Histological examinations and analyses of metallothionein (MT), Cd, Cd bound and not bound to MT, iron and lipid peroxidation in the liver and kidneys were carried out. Histopathological changes occurred in the liver (infiltrations of leukocytes) and kidneys (hemorrhage, glomerular injury, tubular cell degeneration) of bank voles fed the highest dose of dietary Cd only under the moderate photoperiod. The same voles also exhibited the highest values of hepatic and renal Cd, Cd not bound to MT, and renal lipid peroxidation. It seems that under the long photoperiod the liver and kidneys of bank voles were protected against Cd-induced injury through decreasing Cd accumulation and increasing synthesis of MT.