Lead Levels in Eurasian Otters Decline with Time and Reveal

Feb 4, 2011 - Wildlife Veterinary Investigation Centre, Jollys Bottom Farm, Chacewater, Truro, TR4 8PB, U.K.. bS Supporting Information. ABSTRACT: The...
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Lead Levels in Eurasian Otters Decline with Time and Reveal Interactions between Sources, Prevailing Weather, And Stream Chemistry Elizabeth A Chadwick,†,* Victor R Simpson,‡ Abigail E L Nicholls,† and Frederick M Slater† † ‡

Cardiff University School of Biosciences, Museum Avenue, Cardiff, CF10 3AX, U.K. Wildlife Veterinary Investigation Centre, Jollys Bottom Farm, Chacewater, Truro, TR4 8PB, U.K.

bS Supporting Information ABSTRACT: The uptake of contaminants by biota varies spatially and temporally due to a complex range of interacting environmental variables, but such complexities are typically disregarded in studies of temporal change. Here, we use linear modeling to explore spatial and temporal variation in bone Pb levels measured in samples taken from 329 Eurasian otters (Lutra lutra) found dead in southwest England. Between 1992 and 2004 Pb levels in otters fell by 73%, following UK legislative control of Pb emissions implemented since the mid 1980s. Spatial variation in bone Pb was positively correlated with modeled Pb emissions and stream sediment Pb, which interacted negatively with wind-speed and sediment Ca, respectively. Opportunistic collection of samples from wildlife mortalities provided a valuable opportunity for monitoring environmental contamination, interpretation of which was aided by spatially explicit analysis of environmental variables.

1. INTRODUCTION Lead is commonly present in the natural environment, but levels are significantly increased by anthropogenic activities (such as mining, smelting, coal combustion, and waste incineration).1 Tetra ethyl lead (TEL), introduced as an additive to petrol in the 1920s, rapidly became a significant diffuse contributor to global Pb emissions, peaking in the 1970s.2 Exhaust emissions and other human activities result in increased Pb contamination of water, soils and air, and are linked to elevated levels in a wide range of mammals.1 For most mammals the principal route of exposure to Pb is by ingestion, with accumulation primarily in bone.3 Manifestations of Pb poisoning include neuro-behavioral effects, immunosuppression, anemia, impaired renal function and reduced gestational age and growth, with young animals being particularly susceptible.1 Risks to human health have prompted legislation aimed at reducing Pb exposure. In the UK, the level of Pb permitted in petrol was reduced from 0.4 to 0.15 g l-1 in 19864 and leaded petrol was removed from the market in 2000.5 Subsequent monitoring indicates falling emissions,6 and falling concentrations in biotic and abiotic indicators (e.g., vegetation,4 road dusts,7 and sediments8). It is not clear, however, how temporal change in emissions is reflected within aquatic food chains. Uptake of Pb by biota is likely to vary spatially and temporally due to a range of interacting factors; Pb emissions vary with traffic r 2011 American Chemical Society

intensity and distance from roads;9 Pb weathering varies with substrate and climate; dispersal of atmospheric Pb is mediated by climate,10 and bioavailability can be influenced by chemical and physical characteristics of water bodies and their sediments.11 Sex related differences in contamination may arise if differentiation in diet affects exposure, or if maternal transfer acts as an elimination route.12 Age related differences occur where the degree of contamination reflects duration of exposure,13 but this may be confounded by higher absorption of Pb by immature than adult mammals.14 The interaction of spatially and individually heterogeneous variables is poorly understood. Water courses are frequently a sink for pollutants, including heavy metals.15 Because biota integrate contaminants over time, biotic monitoring can allow detection of intermittent as well as chronic exposure, and permits measurement where contaminant levels in water, for example, are below detection limits. The Eurasian otter (Lutra lutra) is a nonmigratory semiaquatic (primarily piscivorous) predator, with a relatively restricted linear range along watercourses (up to 40 or 20 km, for males and females, respectively).16 The species is therefore a suitable candidate for biotic monitoring of pollutants in their local Received: October 13, 2010 Accepted: January 17, 2011 Revised: January 10, 2011 Published: February 04, 2011 1911

dx.doi.org/10.1021/es1034602 | Environ. Sci. Technol. 2011, 45, 1911–1916

Environmental Science & Technology environment (as previously demonstrated, i.e., refs 15,17-19). In addition, because the otter is a European Protected Species, monitoring it for pollutants is a conservation priority under the current Biodiversity Action Plan.20 The population of Eurasian otters in western Europe declined substantially during the 1960s-1970s, and although no in-depth studies were carried out during this period to determine the cause, it was suspected that environmental pollutants were responsible.21 In England, relict populations persisted in the southwest and, from 1988 onward, otters found dead were collected for post mortem examination22 and samples retained for toxicological research. During the following two decades otter populations in England made a strong recovery23 and this, together with escalating road traffic, resulted in increasing numbers of otters being examined, providing a substantial archive of samples for analysis. Here, we aim to investigate whether Pb contamination in otters has changed following legislative control of Pb emissions. Further to this we assess whether variation in otter Pb levels reflects spatial variation in emissions, pH, aspects of prevailing weather or stream sediment geochemistry, or individual variation in age, sex, or size.

2. MATERIALS AND METHODS 2.1. Otter Collection and Post Mortem Examination. Otters found dead in southwest England between 1990 and 2004 were examined following a standard post mortem protocol.24 This included recording date of death, National Grid Reference, sex, weight and body length (nose to tail tip). According to size and developmental features, otters were categorized as adult, subadult, immature or cub.25 Length and weight were used to derive condition, using Kruuk et al’s26 body condition index. The fifth left rib was retained at -20 °C pending Pb analysis. 2.2. Sample preparation. Ribs were soaked in water at 70 °C for 24 h; adhering soft tissue was removed, samples dried, ashed in a muffle furnace at 450 °C and then ground to powder using a glass pestle and mortar. A 200 mg subsample was digested in 2 mL of hot HNO3, made up to 5 mL with deionized water.27 2.3. Analytical Procedure. Samples were analyzed using inductively coupled plasma mass spectrometry (ICP-MS). At high matrix concentrations calcium build-up on instrument cones is known to cause signal reduction.28 Preliminary analyses showed this to be the case, necessitating further dilution. A 1 mL subsample was added to 3 mL of 2% HNO3. Diluted solutions were analyzed on a Thermo X7 (X series) ICP-MS system coupled to a Cetac AS500 autosampler. Uptake and wash-out times between samples were 25 and 90 s, respectively. Four replicates were performed per sample (percentage relative standard deviation averaged 0.98%); mean values are used in all further analyses. Data were automatically corrected using an internal standard of 0.5 mL of thallium (thallium is commonly used as an internal standard for Pb; both show the same response to the hydroxyapatite matrix28). Drift correction was further refined by repeat analysis of a certified reference material (rock standard ENDV) every 15th sample; batch corrections were made using percentage recovery. A second certified standard (JB1a) was analyzed at the end of each sample run (expected Pb value 7200 ug/kg, measured values across five sample runs averaged ((st dev) 7179 ( 230.4 ug/kg). The limit of detection was 0.1ug/kg; measured Pb levels exceeded this in all cases.

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2.4. Source of Other Data Used in Analyses. Atmospheric lead emissions were quantified using UK National Atmospheric Emissions Inventory data.6 Emissions are estimated based on modeling both point (e.g., industrial emissions) and dispersed (e.g., road traffic) sources.29 Spatial variation in emissions was mapped using NAEI data (kg) for each 1  1 km grid square (data hereafter referred to as “local emissions”). Only 2003 data were available at this resolution and are used here as an index of spatial variation for 1992-2004. Temporal variation in emissions was quantified using NAEI national annual emissions totals, available from 1970 (tonnes per year). Spatial variation in pH was quantified using Environment Agency Stream Sampling Programme data—annual averages calculated from monthly sampling in 2003 (chosen for consistency with NAEI data). A subsample of data from 300 locations was used to test the correlation between pH recorded in 2003 and in years 1992-2002 and 2004. Correlations were highly significant (p < 0.001) with a correlation coefficient (r) between 0.807 and 0.903. Sampling density varied between 0.05 samples/ km2 (Wiltshire) and 0.12 samples/km2 (Cornwall). Spatial variation in stream sediment geochemistry was quantified using calcium (Ca, %), and lead (Pb, mg/kg) data supplied by Imperial College London.30 Each sample location is described by easting and northing (to nearest 100 m). Sampling density was high but variable between areas; 0.42-0.47 samples/km2 in Cornwall, Devon, and Somerset, and 0.20-0.35 samples/km2 in Avon, Dorset, Hampshire, and Wiltshire. Detection limits were 0.2% (Ca) and 5 mg/kg (Pb). Spatial variations in rainfall and wind-speed were quantified using Meteorological Office gridded data sets.31 Data used were averages for 1961-2000, at a resolution of one value per 5  5 km square, for rainfall (total annual precipitation, mm) and windspeed (annual mean, knots).32 2.5. Spatial Data Extraction Using ArcMap. Raster layers for pH, rainfall and wind-speed were created using inverse distance weighted interpolation (ArcMap version 9.1, ESRI). All spatial factors were mapped, as point (NAEI data, stream Pb and Ca) or raster (pH, rainfall, wind-speed) layers (Figures S1-6, and Table S1, Supporting Information (SI)). Each otter location was used as the center of four circular areas, of 2.5, 5, 10, and 20 km radius; these were used to sample from each mapped layer. Within each area, the mean value was calculated for every variable (e.g., mean annual rainfall within areas 2.5, 5, 10, and 20 km radius from each otter location). Five data sets were compiled, with the same set of variables but differing spatial resolution: (i) at the point where carcass was found, and (ii-v) averaged over 2.5, 5, 10, and 20 km radius from the carcass location. Preliminary analyses showed all data sets to be highly correlated and the best model fit was found using a 20 km radius; results at other radii are not presented here. At radii >20 km circular areas show considerable overlap and exceed otters’ likely range, so were not considered independent or biologically meaningful. 2.6. Statistical Methods. All analyses were conducted in the R statistical package33 using Generalized Linear Models (GLM). Dependent variables in both models (individual otter bone Pb, annual median otter bone Pb) were natural log transformed (ln[x]) following examination of residuals from initial models. Modeling Individual Otter Bone Pb Using Individual, Spatial and Temporal Variables. Possible influencing factors on bone Pb levels were examined using a GLM. Data distributions for several independent variables were skewed but were normalized 1912

dx.doi.org/10.1021/es1034602 |Environ. Sci. Technol. 2011, 45, 1911–1916

Environmental Science & Technology

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Table 1. Independent Variables Included in Generalized Linear Model As Predictors of Otter Bone Pb, and the Significance (p) of Terms Remaining in the Model Following Standardised Stepwise Deletiona estimate

std. error

t value

p

Temporal Variation (Date of Otter Death) -0.114

year

0.013

-8.749