lead levels in eurasian otters decline with time and reveal interactions between sources, prevailing...

Published: February 04, 2011

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

ARTICLE

pubs.acs.org/est

Lead Levels in Eurasian Otters Decline with Time and RevealInteractions between Sources, Prevailing Weather, And StreamChemistryElizabeth 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 spatiallyand temporally due to a complex range of interacting environmentalvariables, but such complexities are typically disregarded in studiesof temporal change. Here, we use linear modeling to explore spatialand temporal variation in bone Pb levels measured in samples takenfrom 329 Eurasian otters (Lutra lutra) found dead in southwestEngland. Between 1992 and 2004 Pb levels in otters fell by 73%,following UK legislative control of Pb emissions implemented sincethe mid 1980s. Spatial variation in bone Pb was positively correlatedwith modeled Pb emissions and stream sediment Pb, which inter-acted negatively with wind-speed and sediment Ca, respectively.Opportunistic collection of samples from wildlife mortalities pro-vided a valuable opportunity for monitoring environmental con-tamination, interpretation of which was aided by spatially explicitanalysis of environmental variables.

1. INTRODUCTION

Lead is commonly present in the natural environment, butlevels are significantly increased by anthropogenic activities(such as mining, smelting, coal combustion, and wasteincineration).1 Tetra ethyl lead (TEL), introduced as an additiveto petrol in the 1920s, rapidly became a significant diffusecontributor to global Pb emissions, peaking in the 1970s.2

Exhaust emissions and other human activities result in increasedPb contamination of water, soils and air, and are linked toelevated levels in a wide range of mammals.1

For most mammals the principal route of exposure to Pb is byingestion, with accumulation primarily in bone.3 Manifestationsof Pb poisoning include neuro-behavioral effects, immunosup-pression, anemia, impaired renal function and reduced gesta-tional age and growth, with young animals being particularlysusceptible.1 Risks to human health have prompted legislationaimed at reducing Pb exposure. In the UK, the level of Pbpermitted 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 fallingconcentrations in biotic and abiotic indicators (e.g., vegetation,4

road dusts,7 and sediments8). It is not clear, however, howtemporal change in emissions is reflected within aquatic foodchains.

Uptake of Pb by biota is likely to vary spatially and temporallydue to a range of interacting factors; Pb emissions vary with traffic

intensity and distance from roads;9 Pb weathering varies withsubstrate and climate; dispersal of atmospheric Pb is mediated byclimate,10 and bioavailability can be influenced by chemical andphysical characteristics of water bodies and their sediments.11 Sexrelated differences in contaminationmay arise if differentiation indiet affects exposure, or if maternal transfer acts as an eliminationroute.12 Age related differences occur where the degree ofcontamination reflects duration of exposure,13 but this may beconfounded by higher absorption of Pb by immature than adultmammals.14 The interaction of spatially and individually hetero-geneous variables is poorly understood.

Water courses are frequently a sink for pollutants, includingheavy metals.15 Because biota integrate contaminants over time,biotic monitoring can allow detection of intermittent as well aschronic exposure, and permits measurement where contaminantlevels in water, for example, are below detection limits. TheEurasian otter (Lutra lutra) is a nonmigratory semiaquatic(primarily piscivorous) predator, with a relatively restrictedlinear range along watercourses (up to 40 or 20 km, for malesand females, respectively).16 The species is therefore a suitablecandidate for biotic monitoring of pollutants in their local

Received: October 13, 2010Accepted: January 17, 2011Revised: January 10, 2011

1912 dx.doi.org/10.1021/es1034602 |Environ. Sci. Technol. 2011, 45, 1911–1916

Environmental Science & Technology ARTICLE

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 thecurrent Biodiversity Action Plan.20

The population of Eurasian otters in western Europe declinedsubstantially during the 1960s-1970s, and although no in-depthstudies were carried out during this period to determine thecause, it was suspected that environmental pollutants wereresponsible.21 In England, relict populations persisted in the south-west and, from 1988 onward, otters found dead were collected forpost mortem examination22 and samples retained for toxicolo-gical research. During the following two decades otter popula-tions in England made a strong recovery23 and this, together withescalating road traffic, resulted in increasing numbers of ottersbeing examined, providing a substantial archive of samples foranalysis.

Here, we aim to investigate whether Pb contamination inotters has changed following legislative control of Pb emissions.Further to this we assess whether variation in otter Pb levelsreflects spatial variation in emissions, pH, aspects of prevailingweather or stream sediment geochemistry, or individual variationin age, sex, or size.

2. MATERIALS AND METHODS

2.1. Otter Collection and Post Mortem Examination. Ot-ters found dead in southwest England between 1990 and 2004were 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 sizeand developmental features, otters were categorized as adult,subadult, immature or cub.25 Length and weight were used toderive condition, using Kruuk et al’s26 body condition index. Thefifth 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, ashedin a muffle furnace at 450 �C and then ground to powder using aglass pestle and mortar. A 200 mg subsample was digested in 2mL of hot HNO3, made up to 5 mL with deionized water.27

2.3. Analytical Procedure. Samples were analyzed usinginductively coupled plasma mass spectrometry (ICP-MS).At high matrix concentrations calcium build-up on instru-

ment cones is known to cause signal reduction.28 Preliminaryanalyses showed this to be the case, necessitating further dilu-tion. 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. Uptakeand wash-out times between samples were 25 and 90 s,respectively. Four replicates were performed per sample(percentage relative standard deviation averaged 0.98%); meanvalues are used in all further analyses. Data were automaticallycorrected using an internal standard of 0.5 mL of thallium(thallium is commonly used as an internal standard for Pb; bothshow the same response to the hydroxyapatite matrix28). Driftcorrection was further refined by repeat analysis of a certifiedreference material (rock standard ENDV) every 15th sample;batch corrections were made using percentage recovery. Asecond certified standard (JB1a) was analyzed at the end ofeach sample run (expected Pb value 7200 ug/kg, measuredvalues across five sample runs averaged ((st dev) 7179( 230.4ug/kg). The limit of detection was 0.1ug/kg; measured Pb levelsexceeded this in all cases.

2.4. Source of Other Data Used in Analyses. Atmosphericlead emissions were quantified using UK National AtmosphericEmissions Inventory data.6 Emissions are estimated based onmodeling both point (e.g., industrial emissions) and dispersed(e.g., road traffic) sources.29 Spatial variation in emissions wasmapped using NAEI data (kg) for each 1 � 1 km grid square(data hereafter referred to as “local emissions”). Only 2003 datawere available at this resolution and are used here as an index ofspatial variation for 1992-2004. Temporal variation in emissionswas 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 averagescalculated from monthly sampling in 2003 (chosen for consis-tency with NAEI data). A subsample of data from 300 locationswas used to test the correlation between pH recorded in 2003and in years 1992-2002 and 2004. Correlations were highlysignificant (p < 0.001) with a correlation coefficient (r) between0.807 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 byImperial College London.30 Each sample location is described byeasting and northing (to nearest 100 m). Sampling density washigh but variable between areas; 0.42-0.47 samples/km2 inCornwall, Devon, and Somerset, and 0.20-0.35 samples/km2 inAvon, Dorset, Hampshire, and Wiltshire. Detection limits were0.2% (Ca) and 5 mg/kg (Pb).Spatial variations in rainfall and wind-speed were quantified

using Meteorological Office gridded data sets.31 Data used wereaverages for 1961-2000, at a resolution of one value per 5� 5 kmsquare, for rainfall (total annual precipitation, mm) and wind-speed (annual mean, knots).32

2.5. Spatial Data Extraction Using ArcMap. Raster layersfor pH, rainfall and wind-speed were created using inversedistance weighted interpolation (ArcMap version 9.1, ESRI).All spatial factors were mapped, as point (NAEI data, stream Pband Ca) or raster (pH, rainfall, wind-speed) layers (FiguresS1-6, and Table S1, Supporting Information (SI)). Each otterlocation 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 mappedlayer. Within each area, the mean value was calculated for everyvariable (e.g., mean annual rainfall within areas 2.5, 5, 10, and 20km radius from each otter location). Five data sets werecompiled, with the same set of variables but differing spatialresolution: (i) at the point where carcass was found, and (ii-v)averaged over 2.5, 5, 10, and 20 km radius from the carcasslocation. Preliminary analyses showed all data sets to be highlycorrelated and the best model fit was found using a 20 km radius;results at other radii are not presented here. At radii >20 kmcircular areas show considerable overlap and exceed otters’ likelyrange, so were not considered independent or biologicallymeaningful.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 bonePb levels were examined using a GLM. Data distributions forseveral independent variables were skewed but were normalized



after transformation. All variables in the initial model, whichincluded potential Pb sources, year, aspects of otter biology, andenvironmental variables, and all relevant interactions betweenthese variables (up to second order) are listed in Table 1. Themodel was simplified using standard stepwise deletion.Modeling Annual Median Otter Bone Pb Using Annual Pb

Emissions. A linear model was used to predict annual medianotter bone Pb levels between 1992 and 2004, from nationalannual emissions totals. The model was weighted using the totalnumber of otter Pb measurements for each year. The resultingmodel was used to back forecast potential levels of otter bone Pbin previous years for which emissions were recorded but otterbone samples were not available.

3. RESULTS

3.1. Otters Sampled. Rib-bones were analyzed from 329otters (Mapped, Figure S7, SI). Most (81%) died in road trafficaccidents; other significant causes of death were bite wounds andsepsis (10%). The male: female sex ratio was 3:2 (n = 200 males,129 females); 71% (235) were adult, 14% (46) subadult, 11%(35) immature, and 4% (14) cubs.Where both length and weightwere recorded, condition averaged 0.990 ( 0.148 (n = 160,males) and 1.017 ( 0.181 (n = 107, females).3.2. Measured Pb Levels. Lead levels in otter bone varied

between 11.8 ug/kg and 7852 ug/kg. The distribution of valueswas highly skewed (Figure S8, SI), with a median of 84.4 andmean ((standard deviation) of 205.1 ((568.9). 1990 data areomitted from further analysis due to a small n of 2. Annualmedians dropped by 73% from 154 ug/kg in 1992, to 41 ug/kg in2004 (Table S2, SI).3.3. Modeling Individual Otter Bone Pb Using Individual,

Spatial and Temporal Variables. Year had a significant andstrongly negative predicted effect on otter bone Pb levels(Table 1). The interaction between wind and local emissions

was predicted to have a significant effect on otter bone Pb(Table 1). Local emissions are predicted to increase bone Pb, butthis effect diminishes with increasing wind-speed (Figure 1). Theinteraction between stream Pb and stream Ca was also predictedto have a significant effect on bone Pb (Table 1). Stream Pb ispredicted to increase bone Pb, but this effect diminishes withincreasing stream Ca (Figure 2). Neither rainfall, pH, age, sex,length, or weight (nor their interactions) explained any signifi-cant variation in bone Pb levels.3.4. Modeling Annual Median Otter Bone Pb Using An-

nual Pb Emissions. Annual emissions data (Figure 3a) explain70.76% of the variability in median annual otter bone Pb levels(Ln[BonePb] = 4.80864 þ 0.31723 Ln[Emissions], F1,11 =26.63, p< 0.001). Using this model to back forecast otter bone Pblevels suggests median levels up to 250 ug/kg in 1973, some fivetimes higher than 2004 levels (Figure 3b).

4. DISCUSSION

Temporal Change. The 73% decline in Pb measured in otterbone between 1992 and 2004 coincides with a reduction in Pbemissions, following legislative controls imposed since 1986. Nomajor change in otter diet was noted by the examining pathol-ogist during this period. Falling Pb levels in abiotic samples (e.g.,street dust) have been recorded in several European countries(e.g., 7,34) and reductions in Pb in biotic samples have beenrecorded in organisms including cetaceans,35 sphagnum moss,36

herbage (mixed grass-clover ley),4 and humans.37 Here wedescribe for the first time declining Pb in a semiaquatic mammal.

Table 1. Independent Variables Included in GeneralizedLinear Model As Predictors of Otter Bone Pb, and theSignificance (p) of Terms Remaining in the Model FollowingStandardised Stepwise Deletiona

estimate std. error t value p

Temporal Variation (Date of Otter Death)

year -0.114 0.013 -8.749 <0.001

month (c) ns

Otter Biology (Variables Recorded during Post Mortem Examination)

Otter Weight; Otter Length;

Otter Age Class (c); Otter Sex (c)

all ns

Spatial Variation in Environmental Variables

local Pb emissions 3.284 1.474 2.228 0.027

wind -6.742 2.709 -2.489 0.013

sedCa 1.478 0.349 4.241 <0.001

sedPb 0.625 0.117 5.356 <0.001

stream pH; rain both ns

Interaction Terms

local Pb emissions: wind -1.370 0.637 -2.15 0.032

sedCa: sedPb -0.491 0.096 -5.097 <0.001

year: local Pb emissions; year: sedPb; otter weight: length; otter age:

sex; local Pb emissions: rain; pH: sedCa; pH: sedPb

all ns

aCategorical predictors are marked (c), non-significant terms ns. SedCaand SedPb are stream sediment Ca and Pb, respectively.

Figure 1. Model predictions of otter bone Pb showing interactionbetween wind-speed and Local Pb emissions.

Figure 2. Model predictions of otter bone Pb showing interactionbetween stream sediment Pb and Ca. (SedCa = stream sedimentcalcium).



Our findings contrast with a study of bats collected in the samearea, which showed no measurable decline in Pb in kidneysamples taken between 1988 and 2003.38 Renal Pb reflects recentexposure whereas bone Pb reflects cumulative exposure; bonemay therefore be a better indicator of long-term trends becauseshort-term variability in exposure is smoothed. Differences mayalso reflect more gradual purging of residual Pb in terrestrial thanaquatic systems.There is a continued decrease in otter bone Pb from 2000 to

2004 despite very little change in Pb emissions over this period. Atime-lag in response may reflect time taken for Pb to pass alongthe aquatic food chain, and/or the period of accumulation inotters (>70% of otters analyzed were adults, and researchsuggests that UK otters killed on roads are up to eight yearsold, but typically 1-3 years old39). A direct relationship betweenemissions and predator Pb levels is not expected, due to sourcesother than atmospheric deposition of Pb (e.g., geological weath-ering, leaching from land-fill sites, shot-gun ammunition andsewage).15,40,41 Future analyses may reveal whether declinescontinue in bone Pb, or level out as do emissions.Differences between Individuals. Sex and age influence Pb

accumulation in some mammals,12 but neither were significantfactors in our model. Length and weight are potential proxies forage (offering greater discrimination than categorical age-classes),but also showed no effect. Previous analyses of otters (NorthAmerican river otter Lontra canandensis,42 and Californian seaotters Enhydra lutris 43) also show no correlation betweenanimal age and Pb concentration, perhaps because variation indiet between individuals obscures accumulation with age. Thelack of significant difference in accumulation between malesand females suggests that sexual divergence in feeding niche(reported in some studies, (e.g., ref 44) does not result indifferential uptake.Spatial Variation in Associated Environmental Variables.

Heavy metals entering aquatic systems tend to become asso-ciated with particulate matter and accumulate in sediment.45

Accumulation may be a function of residence time of standingwater and particle size of sediments,46 while factors such aschemical form, water chemistry, and the relative distribution of

metals between soluble and particulate fractions further impacton metal deposition and bioavailability.45-48 Data describingmany of these variables were unavailable, but spatial variability instream sediment Pb and Ca, and stream pH, were included in ourmodel. Sediment Pb levels were a highly significant predictor ofbone Pb, as might be expected through their influence at the baseof the aquatic food chain. Although there is limited evidence thatPb biomagnifies, levels of various heavy metals (including Pb) insediments are significantly correlated with concentrations mea-sured in aquatic macroinvertebrates,49 and eels Anguilla anguilla(a highly favored otter prey item), are known to accumulate highconcentrations of Pb due to their bottom living, carnivorousnature, and longevity.50 Sediment Pb levels represent spatialvariability not only in Pb emissions, but also in other sources ofPb, including fishing weights and shotgun pellets, both known tobe important causes of wildlife poisoning.51 Although notattempted here, stable isotope analyses could be effectively usedto discriminate different Pb sources (e.g., ref 35), allowing theinfluence of environmental variables on different routes ofexposure to be modeled separately.The positive correlation between stream sediment Pb and

bone Pb diminishes with increasing stream Ca. This can beexplained by the impact of Ca on bioavailability: low dietary Ca isimplicated in higher uptake (and toxicity) of Pb in birds andmammals.14 Although pH was not a significant explanatoryvariable in our full model, when sediment Ca was removed fromthe model pH showed a similar interaction with sediment Pb(data not presented), such that as pH increased, sediment Pb hada reduced correlation with bone Pb. Acidification of waters bothincreases the abundance of biologically available forms of Pb, andresults in lower availability of Ca,47 so it is likely that pH andsediment Ca have a complementary impact on Pb uptake.Spatial trends in Pb emissions from traffic have been described

by a number of authors, with higher Pb levels recorded in areas ofdense road networks.7,9,52 An estimated 22-58% of Pb emittedby vehicle exhausts is deposited on roadside verges.46 Initialdeposition is influenced by wind and rainfall (rain increasesdeposition while wind disperses emission), and once deposited,Pb may be further mobilized as wind-blown dust or by surfacerunoff. Our model showed that local emissions were a significantpredictor of bone Pb, except in areas of high wind-speed. It seemslikely that as wind-speed increases, Pb emissions are less likely tobe deposited locally, thereby reducing likelihood of uptake bylocal biota. Rainfall was not a significant factor in our model,perhaps because, as an intermittent event, its influence is tootemporally variable to have a measurable impact.Using a circular area of influence around each carcass

location to collate environmental data may not accuratelyreflect the area over which otters accumulate their Pb burden,but without individual-specific information regarding range,the approach used was considered a suitable approximation.Otters’ spatial range (10 s of kilometres) and the potentialinaccuracy implicit in using circular buffer zones to sampleenvironmental data reduce the spatial resolution with whichcontaminant modeling can be carried out, but despite this, ouranalyses successfully use spatial variation in the measuredenvironmental variables to describe biologically relevant inter-actions between sources of contamination (emissions, sedi-ment Pb), and factors influencing dispersal and bioavailability(wind, sediment Ca). While other studies compare temporaltrends between regions (e.g., ref 3), to our knowledge no studyhas modeled the interactions between spatially variable envir-

Figure 3. (a) National annual Pb emissions totals (years when relevantlegislation was implemented are indicated). (b) Otter bone Pb (median)as measured ([) and back forecast (]). Error bars indicate upper andlower quartiles of measured data distribution; dashed lines show upperand lower 95% confidence intervals of modeled data.



onmental data and temporal variation in biotic Pb levels. Ourresults demonstrate that inclusion of relevant environmentaldata at a landscape scale enhances interpretation of contami-nant data.Levels of Contamination, And Implications for Health. In

the current study, annual mean bone Pb levels varied between 65( 17ug/kg and 446 ( 273 ug/kg (in 2004 and 1992, respec-tively, excluding 1990). Bone Pb levels measured in L. canadensisin north America (means of 730-3850 ug/kg in Ontario, usingfemur53 and 1410-5310 ug/kg in Virginia, bone type notspecified42) were considerably higher than in L. lutra in thecurrent study. Our linear regression model used median values,but where these are replaced with annual means for comparison(model not presented), back fore-casts for the 1980s (whensamples were collected for the above studies of L. canadensis)suggest levels of 400-1000 ug/kg, still much lower than in northAmerican L. canadensis. No similar studies report bone Pb levelsin L. lutra, and it is unclear whether differences are due to regionalor species specific variation, or differences in methodology (e.g.,bone type).Unlike synthetic contaminants, metals occur naturally in the

environment so their presence at low levels may be considered“normal’”. Organolead forms (primarily tetraethyl- and tetra-methyl-Pb) are, however, almost exclusively of industrialorigin.14 Anthropogenic inputs have substantially altered Pbavailability in the environment, to the extent that Pb levels inhuman skeletal remains are 500-1000 times greater in recenthistory than in preindustrial times.54 How significant this is inrelation to health is difficult to ascertain. Most studies of Pbcontamination in otters (e.g., refs 15,17-19,55,56) consider thatlevels detected are not likely to be detrimental to their health, andin our study otters with high (>95th percentile) Pb levels were ofnormal body condition. Subclinical effects (such as reproductiveimpairment, lowered birth weight, hyperactivity or impairedneuro-behavioral development14) are not, however, measurablein post mortem studies such as this, and although subclinicaleffects may be minor at an individual level, impacts may besignificant in population terms.57

This study shows that environmental Pb contamination offreshwater aquatic systems was substantially reduced between1992 and 2004. Pb levels measured in otter bone show not onlyclear temporal change, but also interactions between environ-mental variables affecting sources, dispersal, and bioavailability.

’ASSOCIATED CONTENT

bS Supporting Information. Maps of otter sample sites andenvironmental variables; descriptive statistics for environmentalvariables, and data distribution and descriptive statistics formeasured otter Pb levels. This material is available free of chargevia the Internet at http://pubs.acs.org.

’AUTHOR INFORMATION

Corresponding Author*Phone:þ44(0)29 20 874046; faxþ44(0)29 20 874116. E-mail:[email protected].

’ACKNOWLEDGMENT

Analysis was funded by the UK Environment Agency (EA).We would like to thank the EA for supply of pH data, and

Imperial College London for stream geochemistry data. Wegratefully acknowledge Iain MacDonald for analytical support,Ian Vaughan and Joanne Lello for statistical advice, and RichardShore and four anonymous reviewers for helpful comments onearlier drafts.

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lead levels in eurasian otters decline with time and reveal interactions between sources, prevailing...

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