Richard F. Shore

Ecotoxicology of wild mammals

List of Contributors. Series Foreword. Editorsa Preface. Abbreviations. Environmental Contaminants (D. Hoffman, et al.). Mammal Classification and Characteristics (G. Amori & R. Nowak). Marsupialia and Monotremata (R. Bolton--Grob, et al.). Insectivora (W.--C. Ma & S. Talmage). Chiroptera (D. Clark & R. Shore). Rodentia and Lagomorpha (S. Sheffield, et al.). Carnivora (C. Mason & C. Wren). Pinnipedia (P. Ross & G.Troisi). Cetacea and Sirenia (T. Oa Shea & A. Aguilar). Perissodactyla and Artiodactyla (A. Fr?slie, et al.). Biomarkers for Contaminant Exposure and Effects in Mammals (D. Peakall & K. McBee). Extrapolation of Laboratory Tests to Field Populations (D. Forsyth). Assessing Hazard and Risk of Chemical Exposures to Wild Mammals: Food--chain Analysis and its Role in Ecological Risk Assessment (G. Linder & G. Joermann). Putting the Impacts of Environmental Contamination into Perspective (A. Fairbrother). Summation (R. Ringer). Index.

Diorthosubstituted Polychlorinated Biphenyls in Caudate Nucleus in Parkinson's Disease

As it had previously been demonstrated that there were reduced brain dopamine concentrations in monkeys who had been given polychlorinated biphenyls (PCBs) chronically, we hypothesized that organochlorine compounds in general, and PCBs in particular, might be important in the pathogenesis of Parkinsons disease (PD). In a study of caudate nucleus obtained post mortem from patients with Parkinsons disease and from controls, there were significantly higher concentrations of the organochlorine insecticide dieldrin and the PCB congener 153 in the PD tissue. DDE, PCB congener 180, and total PCBs (matched with a commercial preparation) also tended to be higher in Parkinsons disease tissue. We think that this is important preliminary evidence that diorthosubstituted PCBs may contribute to the pathogenesis of Parkinsons disease, and a greater presence of organochlorine insecticides in the PD tissue suggests that this may be in part the explanation for the association between PD and rural living.

Arsenic, cadmium, lead, copper and zinc in cattle from Galicia, NW Spain

Knowledge of trace and toxic metal concentrations in livestock is important for assessing the effects of pollutants on domestic animals and contaminant intakes by humans. Metal levels in cattle have been measured in various countries but not in Spain. In this study, the (wet wt.) concentrations of three toxic elements (arsenic, cadmium, lead) and two trace elements (copper, zinc) were quantified in the liver (Li), kidney (Ki), muscle (M) and blood (Bl) of calves (males and females between 6 and 10 months old) and cows (2-16 years old) from Galicia, NW Spain. For the toxic elements, geometric mean concentrations of arsenic in calves (sexes combined) and cows were 10.8 and 10.2 microg/kg (Li), 11.3 and 15.2 microg/kg (Ki), 3.75 and 4.25 microg/kg (M), 3.23 and 2.92 microg/l (Bl). The corresponding cadmium concentrations were 7.78 and 83.3 microg/kg (Li), 54.3 and 388 microg/kg (Ki), 0.839 and 0.944 microg/kg (M), 0.373 and 0.449 microg/l (Bl). Geometric mean concentrations of lead in calves and cows were similarly low and were 33.0 and 47.5 microg/kg (Li), 38.9 and 58.3 microg/kg (Ki), 6.37 and 12.5 microg/kg (M), 5.47 and 12.2 microg/l (Bl). Sex had almost no effect on the amount of toxic metal accumulated except that kidney cadmium concentrations were significantly higher in females than males. Age did influence accumulation; cadmium and lead (but not arsenic) concentrations in most tissues were significantly greater in cows than female calves. For the trace elements, geometric mean copper levels in calf and cow tissues were 49.9 and 36.6 mg/kg (Li), 4.27 and 3.63 mg/kg (Ki), 0.649 and 1.68 mg/kg (M) and 0.878 and 0.890 mg/l (Bl). The corresponding zinc concentrations were 46.3 and 52.5 mg/kg (Li), 14.2 and 20.7 mg/kg (Ki), 47.3 and 52.5 mg/kg (M) and 2.80 and 2.22 mg/l (Bl). Female calves had significantly higher levels than males of muscle zinc and blood copper and zinc. Female calves accumulated more copper but less zinc in the liver and kidneys compared with cows; this may have been associated with the chronic, low-level cadmium accumulation observed in cows. Overall, the levels of arsenic, cadmium, lead and zinc in cattle in Galicia do not constitute a risk for animal health. However, up to 20% of cattle in some regions in Galicia had levels of copper in the liver that exceeded 150 mg/kg wet wt. These animals may be at risk from copper poisoning.

NMR spectroscopy based metabonomic studies on the comparative biochemistry of the kidney and urine of the bank vole (Clethrionomys glareolus), wood mouse (Apodemus sylvaticus), white toothed shrew (Crocidura suaveolens) and the laboratory rat

The metabolic profiles of three wild mammals that vary in their trophic strategies, the herbivorous bank vole (Clethrionomys glareolus), the granivorous wood mouse (Apodemus sylvaticus), and the insectivorous white-toothed shrew (Crocidura suaveolens), were compared with that of a widely used strain of laboratory rat (Sprague Dawley). In conjunction with NMR spectroscopic investigations into the urine and blood plasma composition for these mammals, high resolution magic angle spinning (HRMAS) 1H-nuclear magnetic resonance (NMR) spectroscopy was applied to investigate the composition of intact kidney samples. Adaptation to natural diet affects both renal metabolism and urinary profiles, and while these techniques have been used to study the metabolism of the laboratory rat little is known about wild small mammals. The species were readily separated by their urinary profiles using either crude metabolite ratios or statistical pattern recognition. Bank vole urine contained higher concentrations of aromatic amino acids compared with the other small mammals, while the laboratory rats produced relatively more hippurate. HRMAS 1H-NMR demonstrated striking differences in both lipid concentration and composition between the wild mammals and Sprague Dawley rats. Bank voles contained high concentrations of the aromatic amino acids phenylalanine, tyrosine and tryptophan in all tissue and biofluids studied. This study demonstrates the analytical power of combined NMR techniques for the study of inter-species metabolism and further demonstrates that metabolic data acquired on laboratory animals cannot be extended to wild species.

Second generation anticoagulant rodenticides in predatory birds: Probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada.

Second-generation anticoagulant rodenticides (SGARs) are widely used to control rodent pests but exposure and poisonings occur in non-target species, such as birds of prey. Liver residues are often analysed to detect exposure in birds found dead but their use to assess toxicity of SGARs is problematic. We analysed published data on hepatic rodenticide residues and associated symptoms of anticoagulant poisoning from 270 birds of prey using logistic regression to estimate the probability of toxicosis associated with different liver SGAR residues. We also evaluated exposure to SGARs on a national level in Canada by analysing 196 livers from great horned owls (Bubo virginianus) and red-tailed hawks (Buteo jamaicensis) found dead at locations across the country. Analysis of a broader sample of raptor species from Quebec also helped define the taxonomic breadth of contamination. Calculated probability curves suggest significant species differences in sensitivity to SGARs and significant likelihood of toxicosis below previously suggested concentrations of concern (<0.1mg/kg). Analysis of birds from Quebec showed that a broad range of raptor species are exposed to SGARs, indicating that generalised terrestrial food chains could be contaminated in the vicinity of the sampled areas. Of the two species for which we had samples from across Canada, great horned owls are exposed to SGARs to a greater extent than red-tailed hawks and the liver residue levels were also higher. Using our probability estimates of effect, we estimate that a minimum of 11% of the sampled great horned owl population is at risk of being directly killed by SGARs. This is the first time the potential mortality impact of SGARs on a raptor population has been estimated.

Spatial and temporal analysis of second-generation anticoagulant rodenticide residues in polecats (Mustela putorius) from throughout their range in Britain, 1992–1999

Polecats (Mustela putorius) in Britain are currently expanding their range eastwards from Wales to reoccupy central and eastern areas of England. Second-generation anticoagulant rodenticides (SGARs), to which polecats are exposed by eating contaminated prey, are used more extensively in these central and eastern regions, leading to fears of increased exposure, and possible resultant mortality. We measured bromadiolone, difenacoum, flocoumafen and brodifacoum concentrations in the livers of 50 polecats from areas that included newly recolonised habitats and found that at least one SGAR was detected in the livers of 13 out of 37 (35.1%) male and 5 out of 13 (38.5%) female polecats. Difenacoum and bromadiolone were detected most frequently. We then combined these data with measurements on another 50 individuals from earlier studies to create a dataset for 100 polecats collected throughout the 1990s from across the whole of their current range. Using this dataset, we determined if there was any evidence that contamination in polecats had increased during the 1990s and whether animals from England were more contaminated than those from Wales, as might be expected given regional differences in the patterns of SGAR use. Overall, 31 of the 100 polecats analysed to date contained SGAR residues. The incidence was a little higher (40%) in animals that died between January and June and this probably better reflects the overall proportion of animals that are sub-lethally exposed. There was no statistically significant change during the 1990s in the proportion of polecats exposed to SGARs nor any evidence that greater use of SGARs in England resulted in more contamination of polecats. Contrary to expectation, the proportion of animals that contained difenacoum was marginally higher in Wales than elsewhere.

The ecotoxicological significance of cadmium intake and residues in terrestrial small mammals

Little is known about the ecotoxicological hazard of cadmium to wild small mammals. This paper reviewed laboratory and field studies to determine: (i) intake and residue lowest-observable-adverse-effect-levels (LOAELs) for the ecologically important parameters of reproduction and development; (ii) whether these LOAELs are exceeded by wild small mammals on contaminated habitats and what adverse effects result; and (iii) which species may be at most risk from cadmium. The intake LOAEL in laboratory rodents was 3.5-7.5 mg kg-1 body wt day-1 and the residue LOAEL, based on cellular damage in the kidney, was a renal cadmium concentration of 105 mg kg-1 dry wt. On contaminated habitats, these LOAELs are exceeded by common shrews Sorex araneus but not by wild rodents. However, there is little evidence of adverse cadmium-mediated effects in common shrews and this species may be tolerant to cadmium exposure. Large cadmium concentrations in body organs may simply reflect an ability to store cadmium in a nontoxic, metallothionein-bound state. In contrast, studies suggest that microtine voles may be sensitive to cadmium and, despite their relatively low cadmium intake and accumulated residues, may suffer adverse effects. The need to establish dose-residue-effect relationships for intakes and residues which are appropriate for wild species and also based on ecologically important parameters is discussed.

Country-specific effects of neonicotinoid pesticides on honey bees and wild bees

Damage confirmed Early studies of the impacts of neonicotinoid insecticides on insect pollinators indicated considerable harm. However, lingering criticism was that the studies did not represent field-realistic levels of the chemicals or prevailing environmental conditions. Two studies, conducted on different crops and on two continents, now substantiate that neonicotinoids diminish bee health (see the Perspective by Kerr). Tsvetkov et al. find that bees near corn crops are exposed to neonicotinoids for 3 to 4 months via nontarget pollen, resulting in decreased survival and immune responses, especially when coexposed to a commonly used agrochemical fungicide. Woodcock et al., in a multicounty experiment on rapeseed in Europe, find that neonicotinoid exposure from several nontarget sources reduces overwintering success and colony reproduction in both honeybees and wild bees. These field results confirm that neonicotinoids negatively affect pollinator health under realistic agricultural conditions. Science, this issue p. 1395, p. 1393; see also p. 1331 Bee health is affected by neonicotinoids under field-realistic conditions across crops conditions. Neonicotinoid seed dressings have caused concern world-wide. We use large field experiments to assess the effects of neonicotinoid-treated crops on three bee species across three countries (Hungary, Germany, and the United Kingdom). Winter-sown oilseed rape was grown commercially with either seed coatings containing neonicotinoids (clothianidin or thiamethoxam) or no seed treatment (control). For honey bees, we found both negative (Hungary and United Kingdom) and positive (Germany) effects during crop flowering. In Hungary, negative effects on honey bees (associated with clothianidin) persisted over winter and resulted in smaller colonies in the following spring (24% declines). In wild bees (Bombus terrestris and Osmia bicornis), reproduction was negatively correlated with neonicotinoid residues. These findings point to neonicotinoids causing a reduced capacity of bee species to establish new populations in the year following exposure.

Predicting Ecotoxicological Impacts of Environmental Contaminants on Terrestrial Small Mammals

This review examines whether the effects of environmental contaminants on wild small mammals can be predicted from the results of single-species, laboratory toxicity studies. Heavy metals, organochlorines, chlorinated aromatic hydrocarbons, and OP/carbamate pesticides were identified as the groups of xenobiotics for which there are toxicity data for terrestrial small mammals and that, on the basis of persistence, acute toxicity, and bio-accumulation potential, present the greatest hazard to wild mammals. Laboratory-generated toxicity data, which used lethality and reproduction as measurable endpoints, were reviewed and intake and residue LOAELs estimated for representative chemicals (lead, endrin, PCBs) from the heavy metal, organochlorine, and chlorinated aromatic hydrocarbon substance groups; the OPs and carbamates were reviewed as a whole. Intakes and residues of these compounds in wild small mammals were compared with laboratory-defined LOAELs and the likelihood of effects predicted. The accuracy of these predictions was examined and the efficacy of extrapolating toxicity data from laboratory to wild species assessed. Qualitative extrapolation from laboratory to wild species was good for all the chemicals considered, laboratory tests correctly identifying the types of effects chemicals had on a wide range of wild mammals. In contrast, the quantitative extrapolation of dose-response data was either poor or largely unvalidated. This is because interspecies variation in sensitivity to xenobiotics and the effects on toxicity of differences in exposure pattern between laboratory and wild species are largely unquantified. Based upon the limited evidence available, errors in the direct extrapolation of dose-response data from laboratory to field may be as large as three orders of magnitude. Direct extrapolation of residue-response data from laboratory to wild mammals is good both for the effects of heavy metals on specific organs and for residues and acetylcholinesterase inhibition associated with pesticide-induced mortality. The use of organ residues or biomarkers to predict the severity of sublethal effects on reproductive output may be possible, although large residues or biomarker responses are not necessarily indicative of the severity of wider physiological effect. Appropriate residues/biomarkers may differ for various xenobiotics and even between species for the same xenobiotic. Further research is required to identify suitable markers that can be correlated with the occurrence and magnitude of ecologically important effects. Xenobiotics likely to have a direct effect on population dynamics are those that are persistent and adversely affect survival and reproduction. At present, this weak correlation is the only one that can be made between single-species laboratory tests and population effects.(ABSTRACT TRUNCATED AT 400 WORDS)

Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus)

Studies on exposure of non-targets to anticoagulant rodenticides have largely focussed on predatory birds and mammals; insectivores have rarely been studied. We investigated the exposure of 120 European hedgehogs (Erinaceus europaeus) from throughout Britain to first- and second-generation anticoagulant rodenticides (FGARs and SGARs) using high performance liquid chromatography coupled with fluorescence detection (HPLC) and liquid-chromatography mass spectrometry (LCMS). The proportion of hedgehogs with liver SGAR concentrations detected by HPLC was 3-13% per compound, 23% overall. LCMS identified much higher prevalence for difenacoum and bromadiolone, mainly because of greater ability to detect low-level contamination. The overall proportion of hedgehogs with LCMS-detected residues was 57.5% (SGARs alone) and 66.7% (FGARs and SGARs combined); 27 (22.5%) hedgehogs contained >1 rodenticide. Exposure of insectivores and predators to anticoagulant rodenticides appears to be similar. The greater sensitivity of LCMS suggests that hitherto exposure of non-targets is likely to have been under-estimated using HPLC techniques.