Dioxin exposure in contaminated sawmill area: the use of molar teeth and bone of bank vole (Clethrionomys glareolus) and field vole (Microtus agrestis) as biomarkers

Developmental disorders of teeth are among the most sensitive targets of polychlorinated dibenzo-p-dioxin and -furan (PCDD/F) exposure. In rats, 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) reduces dose-dependently the size of molars, most severely the third lower molars. Dioxins also have effects on developing bone, including altered bone mineral density as well as reduced bending breaking force and stiffness. The aim of this study was to evaluate the use of the third lower molar and long bones as biomarkers of PCDD/F exposure in two wild vole species, the bank vole (Clethrionomys glareolus) and the field vole (Microtus agrestis) collected from a PCDD/F contaminated former sawmill area. Survey of soil and biota of the sawmill area indicated a PCDD/F contamination with a congener profile characteristic for the chlorophenol wood preservative Ky-5. The PCDD/F concentration in the bank vole was notably higher than in the field vole. The third molar of the bank vole was significantly smaller in dioxin-exposed animals compared to control group, while there was no difference between these two groups in the field vole. No significant alterations were observed in bone density and strength in either species except for reduced bending strength of the femur neck in bank vole males exposed to dioxins. Even though the bone changes are among the sensitive endpoints of dioxin-exposure, high variability due to age, size and gender limits their use as biomarkers of wildlife exposure. In conclusion, the size of molar teeth seems to be a sensitive and robust biomarker for PCDD/F exposure in wild bank vole populations and thus worth of further studies.     

The heavy metal content of the teeth of the bank vole (Clethrionomys glareolus) as an exposure marker of environmental pollution in Poland

This investigation is based on the premise that heavy metals are sequestered by the mineral phase of teeth, hydroxyapatite, during their formation. Once formed these tissues are not subject to significant turnover and it is suggested, therefore, that they provide a permanent and cumulative record of heavy metal exposure during the development of the teeth. The teeth of the bank vole (Clethrionomys glareolus) were analysed by inductively coupled plasma mass spectrometry to monitor the animals' exposure to lead, cadmium, zinc, copper and strontium. Animals were trapped in clean and polluted areas in Poland in and around Krakow in 1996 and in Olkusz and Legnica in 1996 and 1997. The control area in 1996 was Bieszcady National Park and in 1997 Borecka Forest. The results showed that there were statistically different concentrations of heavy metals in the teeth of animals from different sites. The high levels of pollution from industrial emissions were related to higher concentrations of heavy metals in the teeth. Unexpectedly high levels of heavy metals in the teeth of animals from Bieszczady National Park, thought to be environmentally clean, suggested cross-border pollution from Slovakia and the Ukraine. It was concluded that the teeth of small mammals, such as the bank vole, are a sensitive and reliable marker of environmental pollution by heavy metals.     

Fluoride in the prey of barn owls (Tyto alba)

Bone fluoride in short-tailed voles (Microtus agrestis) and common shrews (Sorex araneus), the prey of barn owls (Tyto alba), was studied on Anglesey, North Wales. The average fluoride content of M. agrestis skulls obtained from a location 0.9 km from an aluminium reduction plant was significantly greater than that of skulls from another location 22 km from the source of industrial fluoride pollution. At both locations, mean fluoride levels of skulls extracted from owl pellets and those of voles trapped mechanically were broadly similar but important differences existed. Near the aluminium reduction plant, owls caught voles and shrews with a much wider range of fluoride levels than occurred at a single trapping site. However, there was no evidence for selection of heavily fluoridated prey. Within 1 km of the aluminium reduction plant, six trapping sites yielded S. araneus with a fourfold difference between the highest and lowest mean bone fluoride level.     

Distribution of trace element pollutants in a contaminated ecosystem established on metalliferous fluorspar tailings. 3: fluoride

High total soil fluoride (10 000 microg g(-1)) in the metalliferous fluorspar tailings was reflected by elevated concentrations in standing live vegetation (300-1000 microg g(-1)); plant roots (c. 6000 microg g(-1)); plant litter (c. 4000 microg g(-1)); total body concentrations of invertebrates (400-4000 microg g(-1)) and the small mammals Microtus agrestis (120-360 microg g(-1)) and Sorex araneus (140-250 microg g(-1)). Seasonal changes in the standing live vegetation and the availability of soil fluoride to plants are discussed. Seasonal changes in total body concentrations of the small mammals were related to the age structure of the populations as well as dietary levels. In the small mammals, the concentration ratios were < 0.5 at the tailings dam and > 1.1 at the control site, indicating that both species were able to regulate fluoride accumulation at the higher levels of intake. Soft tissue concentrations were, as expected, very low compared to the hard tissues but, still, were generally significantly higher at the tailings dam compared to the control site. Evidence of dental fluorosis was found in Microtus agrestis, but not Sorex araneus.     

Distribution of trace element pollutants in a contaminated grassland ecosystem established on metalliferous fluorspar tailings. 2: Zinc

Concentrations of zinc in vegetation, invertebrates and small mammals in a grassland ecosystem derived from a mine waste vegetation scheme indicated the high concentration of zinc in the original tailings. However, the considerable differences in soil and vegetation zinc concentrations between the tailings and an uncontaminated site were not reflected in the invertebrate and small mammal communities. Invertebrate zinc levels and total body concentrations in Microtus agrestis L. (field vole) and Sorex araneus L. (common shrew) suggested a notable buffering of zinc absorption and tissue accumulation in the presence of substantially elevated dietary zinc. In the small mammals the skeleton appeared to function as the major storage site for zinc, possibly contributing to homeostasis in the soft tissues.     

Risk assessment of metals and organic pollutants for herbivorous and carnivorous small mammal food chains in a polluted floodplain (Biesbosch, The Netherlands)

A risk assessment was made for a carnivorous and a herbivorous food chain in a heavily polluted natural estuary (Biesbosch), by determining the most critical pollutants and the food chain most at risk. Exposure of food chains to metals, polycyclic aromatic hydrocarbons (PAHs), and polychlorinated biphenyls (PCBs) was assessed by analyzing dietary concentrations, internal concentrations, and biomarkers of exposure. Common shrew (Sorex araneus) and bank vole (Clethrionomys glareolus) were selected as representative small mammal species for the carnivorous and herbivorous food chain, respectively, and earthworms (Lumbricus rubellus) and snails (Cepaea nemoralis) as representative prey species for the carnivorous food chain. Metals contributed most to the total risk for small mammals and earthworms. PCBs, but not PAHs, contributed to the overall risk for S. araneus at regularly flooded locations. The carnivorous food chain appeared most at risk given the higher exposure levels and bioaccumulating potency found for contaminants in S. araneus.     

Effects of airborne fluoride emissions near an aluminium works in Wales: part 2--saxicolous lichens growing on rocks and walls

Effects of fluoride (F(-)) emissions on previously unpolluted assemblages of saxicolous lichens, near an aluminium reduction works, are described. Lichens contained a mean 16 microg F(-) g(-1) dry weight in 1970 before emissions commenced. Subsequently, where annually monitored Ramalina contained >100microg g(-1) severe damage occurred, including loss of attachment to the rocky substratum. At sites within 1 km of the works well-exposed to emissions, fruticose (shrubby) lichens were eliminated, but in more sheltered locations 18% cover had survived by 1983. Some foliose (leaf-like) lichens tolerated >200 microg g(-1), while crustose (crust-like) species were least affected, 32% and 70% surviving, respectively. Concentrations of fluoride, and associated injury, decreased with increasing distance from the works. Fruticose and sensitive foliose species sustained 40-75% losses of cover up to 4 km NE, downwind of the works, where fluoride averaged 50-100 microg g(-1), but <40% losses were recorded in fruticose species up to 9 km, where concentrations averaged 35-50 microg. Saxicolous lichens were damaged less than corticolous species previously reported and, following decreased emissions, were also regrowing in sheltered and more distant locations by 1985.     

Reduced survival and body size in the terrestrial isopod Porcellio scaber from a metal-polluted environment

Terrestrial isopods (woodlice) may show trade-offs in life history parameters when exposed to toxins. We have shown previously [Jones and Hopkin (1996) Functional Ecology 10, 741-750] that woodlice which survive to reproduce in sites heavily polluted with metals from an industrial smelting works do not alter their reproductive allocation. This study investigates whether there are differences in the survival and body size of Porcellio scaber from these same populations. Specimens were collected from eight sites at different distances from the Avonmouth smelter, UK. The sites represented a gradient of concentrations of Zn, Cd, Pb and Cu in the woodlice, from background levels to a grossly contaminated sites close to the smelter. In laboratory trials, the number of days survived by starved males showed a significant decline with increased concentrations of Zn in those animals. The maximum size of both sexes declined significantly from the least to the most polluted sites. The most polluted sites had significantly fewer large animals. The cost of detoxifying assimilated metals appears to be reduced energy reserves and smaller body size.     

Ecophysiological responses of Empetrum nigrum to heavy metal pollution

Chlorophyll, organic (citric and malic acids) and abscisic acid (ABA) contents and stem water potential were measured to indicate possible physiological effects of heavy metal deposition on Empetrum nigrum L. (crowberry). The leaves and stems of E. nigrum were collected at distances of 0.5 and 8 km from the Cu-Ni smelter at Harjavalta, south-west Finland. All the investigated parameters were clearly affected by heavy metal emissions. Chlorophyll contents in the leaves and organic acid contents in the leaves and stems were lower close to the emission source. Generally found increase in organic acid contents with increasing Ni concentrations was not found, which might be due to the lower production of organic acids measured by decreased photosynthesis near the smelter. In contrast, ABA contents in stems and leaves in general, were higher in plants growing 0.5 km from the pollution source. Close to the smelter the stem water potential of E. nigrum was less negative during the day but more negative during the night. These results suggest that smelter emissions have a negative effect on the ecophysiology of E. nigrum even though it is considered to be a tolerant species to heavy metals.     

Atmospheric deposition of fluoride in the lower Tamar Valley,Tasmania

Soluble fluoride (F⁻), measured using an ion-selective electrode, was monitored during 1982–1983 in monthly bulk (wet and dry) atmospheric deposition samples collected at 17 locations in the lower Tamar Valley, Tasmania, where an aluminium (Al) smelter is located. Glass samplers (funnel-bottle type) were used, with duplications by plastic samplers at five locations later. The spatial and temporal variations in F⁻ deposition in relation to wind flow and rainfall are discussed, and its impact on the environment is highlighted. The mean deposition rates of F⁻, as measured from September 1982 to August 1983, ranged from about 90 μg m⁻² day⁻¹ at the intended ‘background’ location to 12,568 μg m⁻²day⁻¹ at a location about 1 km east-southeast from the smelter. The depositional fluxes of F⁻ and insoluble Al (another elemental tracer of the smelter) are significantly correlated (P < 0.001). They were much higher within 3 km of the smelter, where vegetation damage by fluoride contamination was most evident. However, air emissions from the smelter could travel at least 10 km up the valley. Wet deposition was the predominant removal process for F⁻ during autumn and winter, while dry deposition appeared to be more significant in summer. The plastic samplers collected about 8 and 17% more F⁻ and Al, respectively, but with higher standard deviations. Thus the variations observed could be largely due to sampling fluctuations.     

Presence of a parasitic nematode (Eustrongylidies sp.) in brown trout (Salmo trutta) from a heavy metal contaminated aquatic ecosystem

The Flat Nickel mine at Evje in southern Norway was mined intensively between 1914 and 1945 with little regard for any potential environmental effect. Much of the ore extracted was smelted at a site adjacent to the river Otra south of Evje. Recent studies have revealed heavy metal pollution in the land surrounding the smelter and in water draining from the mine, leading to concern for the aquatic ecosystem in the river Otra. Brown trout were sampled from an uncontaminated lake nine kilometres upstream from the smelter, from the base of the Oddebekken (a tributary draining the mine water into the Otra), from sites immediately upstream and down stream of the smelter and from a site four kilometres down stream from the smelter. Fish from sites adjacent to the smelter and the base of the Oddebekken were smaller than those from the lake and down stream site. Fish from sites adjacent to the smelter and the base of the Oddebekken were more likely to be infected with parasitic nematode Eustrongylidies. At the population but not the individual level the presence of encapsulated parasitic larvae correlated with the concentrations of two metals, Ni and Cu, in fish.     

Polychlorinated biphenyls in small mammals from contaminated landfill sites

PCBs in small mammals living in a contaminated landfill site varied in both concentration and congener composition, reflecting both the feeding strategy of each species and the chlorination of the congeners. Body concentrations of SigmaPCB on a 1:1:1 Arochlor (1242:1254:1260) basis gave a rank order of Sorex araneus > Apodemus sylvaticus > Microtus agrestis. Comparisons with data for other PCB-contaminated sites suggest that the SigmaPCB values in S. araneus from the landfill site may be of sufficient magnitude to inhibit reproductive capability and to cause other major organ dysfunction. There were also inter-specific differences in the whole body concentrations of the individually quantified congeners. For S. araneus, the rank order of concentrations of the selected ICES 7 marker PCB congeners was: No. 153>138>180>118>28>101>52. In M. agrestis the rank order was: No. 28>118>153>138>180, 52>101. The congener order for A. sylvaticus differed from both S. araneus and M. agrestis, but was more similar to the latter, being: No. 153>138>118>180>28>52, 101. The contribution of the different congeners to SigmaPCB in the mammals reflects the degree of chlorination of different congeners but varies with feeding strategy of the species. In the insectivorous S. araneus, heavily chlorinated congeners (Nos 153, 138 and 180) are most abundant, whereas the herbivore, M. agrestis showed congeners Nos 28 and 118 to be present in the highest amounts, whilst the equivalent pattern for the more omnivorous A. sylvaticus was intermediate between S. araneus and M. agrestis. The high concentrations of PCBs in S. araneus relative to the other species, suggests that it may serve as a useful biomarker of terrestrial environmental pollution by organochlorines.     

Predicting cadmium, lead and fluoride levels in small mammals from soil residues and by species-species extrapolation

The effects of heavy metals on wild mammals are often assessed by analysing residues in body organs. This paper reviews published studies to determine whether cadmium (Cd), lead (Pb) and fluoride (F) residues in small mammals can be predicted directly from residues in soil or, when this is not possible, from residues in other species. It was found that residues in soil could be used to predict Cd and Pb concentrations in small mammals. There were significant (P < 0.05) relationships between Cd residues in soil and in the liver and kidneys of wood mice Apodemus sylvaticus and common shrews Sorex araneus; similar relationships occurred in field voles Microtus agrestis (0.05 < P < 0.10). There were also significant relationships between Pb residues in soil and body organs for wood mice and field voles. Insufficient data were available to relate either Pb levels in soil to those in shrews or F levels in soil to residues in any species. However, both Cd and F residues in any one of the three small mammal species examined could be predicted from the corresponding residues in the other species, there being significant relationships between species for residues in the liver and kidneys (Cd) or bone (F). Too few data were available to determine species-species relationships for Pb.     

Understorey vegetation along a heavy-metal pollution gradient in SW Finland

Understorey vegetation of Scots pine forests was studied along a 8-km transect running SE from a Cu-Ni smelter at Harjavalta, SW Finland. Long-term accumulation of heavy metals and sulphur in the forest ecosystem has drastically changed plant communities. Vegetation was almost absent up to a distance of 0.5 km from the smelter. The total coverage and the number of plant species increased with increasing distance from the smelter. Ordination by global non-metric multidimensional scaling (GNMDS) indicated that the floristic composition was differentiated in response to the pollution level. The main compositional gradient of GNMDS was correlated with the heavy metal concentrations in the organic soil layer and with the size of the overstorey trees. Vascular plants were more pollution-resistant than ground lichens, whereas mosses were the most sensitive plant group. In addition to heavy metals, nutrient imbalances and the considerably reduced water-holding capacity of the surface soil also restrict plant recolonisation on the degraded sites.     

Factors determining amounts of fluoride in woodlice Oniscus asellus and Porcellio scaber, litter and soil near an aluminium reduction plant

Amounts of fluoride were measured in whole woodlice Oniscus asellus and Porcellio scaber, together with associated soil and litter, from 17 sites near an aluminium reduction plant at Holyhead, Anglesey, in North Wales. There was a strong positive correlation between amounts of fluoride in woodlice, soil and litter in all comparisons (P<0.02). Highest and lowest fluoride concentrations in woodlice differed by a factor of >50. Where both woodlice species occurred together at the more polluted sites, fluoride levels in Oniscus asellus were generally twice as high as those found in Porcellio scaber. At any given site, amounts of environmental fluoride were determined partly by distance and direction from the pot-rooms of the plant (a function of prevailing winds), modified by the presence of trees which acted as collectors for gaseous and particulate fluoride.     

Effects of heavy metal exposure on the condition and health of adult great tits (Parus major)

We examined the possible effects of heavy metal exposure on the quality and health of adult great tits (Parus major) at four study sites along a pollution gradient near a non-ferrous smelter in Belgium. Tarsus length, wing length, body mass and condition of great tits were compared with respect to study site, age (first-year and older great tits), sex and season (birds caught in winter and during breeding). Tarsus length did not differ significantly among study sites. The wing length of great tits was larger at the study site furthest from the smelter, especially for older great tits. The length of the outermost tail feathers, however, did not differ significantly among study sites. We found no signs of loss of body mass or condition towards the pollution source. The body mass and condition was lowest for female great tits at the site furthest from the smelter, especially during winter. Haematocrit values did not differ significantly among sites. Overall, we found no clear significant effects of heavy metal pollution on morphological measurements and health parameters of great tits.     

Patterns of insect communities along a stress gradient following decommissioning of a Cu-Ni smelter

The diversity, estimated richness and abundance of terrestrial insect communities were examined along a stress gradient of past pollution in the region of Sudbury, Ontario, Canada. This gradient represents the natural recovery and lingering effects of a decommissioned copper-nickel smelting complex. Ant genera and sixteen higher taxonomic groups (family and order) had the highest abundance at the sites with intermediate stress. Eight families increased in abundance with distance from the decommissioned source of pollution and eleven families decreased reflecting a complex response of diversity to pollution. Carabid beetles show an increase in diversity further from the smelter; however, examination of the species composition reveals a distinct carabid community closest to the smelter, emphasizing the unique habitat created by severe pollution. Although almost forty years since decomissioning of the smelter complex, the terrestrial insect community in the vicinity remains significantly impacted suggesting slow recovery.     

Status of industrial fluoride pollution and its diverse adverse health effects in man and domestic animals in India

Hydrofluorosis in humans and domestic animals is a worldwide health problem and caused by a prolonged period of fluoride exposure through drinking of fluoride contaminated water. But in recent years, due to rapid industrialization in India, diverse serious health problems among industrial workers and residents and domestic animals living in the industrial areas due to fluoride pollution are on the rise. A number of coal-burning and industrial activities such as power-generating stations, welding operations and the manufacturing or production of steel, iron, aluminum, zinc, phosphorus, chemical fertilizers, bricks, glass, plastic, cement, and hydrofluoric acid are generally discharging fluoride in both gaseous and particulate/dust forms into surrounding environments which create a industrial fluoride pollution and are an important cause of occupational exposure to fluoride in several countries including India. An industrial emitted fluoride contaminates not only surrounding soil, air, and water but also vegetation, crops and many other biotic communities on which man and animals are generally dependants for food. Long- time of inhalation or ingestion of industrial fluoride also causes serious health problems in the forms of industrial and neighborhood fluorosis. In India, whatever research works conducted so far on the chronic industrial fluoride intoxication or poisoning (industrial and neighborhood fluorosis) in man and various species of domestic animals due to a prolonged period of industrial fluoride exposure or pollution (contamination) are critically reviewed in the present communication. Simultaneously, we are also focused the various bio-indicators and bio-markers for chronic industrial fluoride intoxication or pollution.     

Density patterns of gall mites (Acarina:Eriophyidae) in a polluted area

Trends in the densities of six species of gall mites on European aspen (Populus tremula) and on two birch species (Betula pubescens and B. pendula) were compared in an air pollution gradient from the Harjavalta copper-nickel smelter, SW Finland. The densities of gall mites on both birch species decreased towards the smelter and were negatively correlated with the levels of copper and nickel in the birch leaves. In contrast, the densities of aspen mites correlated neither with distance from the pollution source nor with the content of heavy metals in aspen leaves. Both birch and aspen trees tended to produce smaller leaves near the smelter, but a significant correlation between gall mite densities and site-specific leaf areas was only found for one species of mite.     

Impact of a smelter closedown on metal contents of wheat cultivated in the neighbourhood

BACKGROUND: The contamination of soils by heavy metals engenders important environmental and sanitary problems in Northern France where a smelter has been located for more than one hundred of years. It has been one of the most important Pb production sites in Europe until its closedown in March 2003. Ore smelting process generated considerable atmospheric emissions of dust. Despite an active environmental strategy, these emissions were still significant in 2002 with up to 17 tonnes of Pb, 32 tonnes of Zn and 1 tonne of Cd. Over the years, the generated deposits have led to an important contamination of the surrounding soils. Previous studies have shown pollutant transfers to plants, which can induce a risk for human and animal health. The objective of this study was to evaluate the consequences of the smelter closedown on the Cd and Pb contents of wheat (grain and straw) cultivated in the area. METHODS: Paired topsoil and vegetable samples were taken at harvest time at various distances to the smelter. The sample sites were chosen in order to represent a large range of soil metal contamination. Sampling was realised on several wheat harvests between 1997 and 2003. 25 samples were collected before the smelter closedown and 15 after. All ears of about 1 m long of two rows were manually picked and threshed in the lab. Similarly, straw was harvested at the same time. Total metal contents in soil and wheat samples were quantified. RESULTS: A negative correlation between metal concentrations in soil and the distance to the smelter was shown. The wheat grain and straw showed significant Cd and Pb contents. The straw had higher metal contents than the grain. During the smelter activity, the grain contents were up to 0.8 mg kg(-1) DM of Cd and 8 mg kg(-1) DM of Pb. For the straw, maximum contents were 5 mg kg(-1) DM of Cd and 114 mg kg(-1) DM of Pb. After the smelter closedown, we observed a very large decrease of Pb in the grain (82%) and in the straw (91%). A smaller decrease was observed for Cd in grain. Despite this improvement, 80% of the studied samples remained non-acceptable for human consumption, according to the European legislation values, due to a high Cd content. DISCUSSION: Results highlighted a difference in metal accumulation in the plant organs as well as a difference in metal uptake. The approach pointed out the importance of atmospheric fallout in the wheat contamination pathways for Pb. The smelter closedown has lead to a decrease of the Pb content in wheat. It is interesting to relate this finding with the lead blood levels in children living close to the smelter. CONCLUSIONS: Those results have confirmed the importance of dust fallout in the plant contamination pathways. Before the closedown, Pb measured in the plant was principally originating from the smelter dust emissions. It raised the question of the sanitary risks for humans and animals living in the surrounding a of the smelter. RECOMMENDATIONS AND PERSPECTIVES: In the literature, very few articles take the dust deposit as contamination pathways for crops into consideration. However, in highly contaminated sites, this pathway can be very important. Thus, it would be worthy studying the uptake of metal contaminants by plants through the foliar system.