Lead Poisoning of Seabirds: Environmental Risks from Leaded Paint

Jun 21, 2003 - Midway Atoll hosts a decommissioned military base and was designated a National Wildlife Refuge in 1988. A 1994 study showed that 85% o...
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Environ. Sci. Technol. 2003, 37, 3256-3260

Lead Poisoning of Seabirds: Environmental Risks from Leaded Paint at a Decommissioned Military Base M Y R A E . F I N K E L S T E I N , * ,†,‡ ROBERTO H. GWIAZDA,‡ AND DONALD R. SMITH‡ Department of Ocean Sciences and Department of Environmental Toxicology, 1156 High Street, University of California, Santa Cruz, California 95064

The sources and risk factors for lead exposure to humans are relatively well recognized, yet much less is known about lead exposure risks and effects to wildlife. Here we utilized lead isotopic fingerprinting to investigate sources of elevated lead exposure to Laysan albatross (Phoebastria immutabilis) chicks in the Midway Island National Wildlife Refuge, which was established on the site of a decommissioned military base that previously had undergone lead remediation. Whole blood from chicks as well as soil and paint chips from the chicks’ nests were collected from birds nesting close to (100 m, reference site) buildings and analyzed for lead levels and isotopic compositions using magnetic sector ICP-MS. Blood lead levels of chicks from the building site had a geometric mean of 190 µg/dL (average ) 320 ( 310 SD, range ) 6.8-1400, n ) 21) as compared to 4.5 µg/ dL (average ) 6.0 ( 4.2 SD, range ) 1.2-13, n ) 15) in chicks from the reference site. Nest soil lead levels from both sites were similar and relatively low (0.05-11 µg/g) unless visibly contaminated with paint chips (building site). Isotopic analyses confirmed that leaded paint was the source of lead poisoning in these chicks and showed that the pathway of exposure was via direct ingestion of paint chips and not through contaminated soil. This study found continued risk to wildlife and possibly humans from lead hazards in a wildlife refuge established on a decommissioned military base. In addition, this study demonstrates the utility of lead isotopes to identify environmental lead hazards and exposure pathways to wildlife.

Introduction Human lead poisoning from environmental sources such as lead-based paints and contaminated dusts and soils remains a significant public health problem in the United States and elsewhere (1-3). The sources of exposure are less understood for wildlife, except with respect to spent lead shot, a wellrecognized pathway of exposure that has impacted wild birds throughout the last century (4-7). Sources of elevated lead exposure can be difficult to identify for wildlife given that * Corresponding author phone: (831)459-4571; fax: (831)459-3524; e-mail: [email protected]. † Department of Ocean Sciences. ‡ Department of Environmental Toxicology. 3256

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specific feeding behavior (e.g., location, prey) in most situations is unknown and because anthropogenic lead is ubiquitous in the environment, often providing multiple possible sources of exposure. Midway Atoll hosts a decommissioned military base and was designated a National Wildlife Refuge in 1988. A 1994 study showed that 85% of the 253 building structures on Midway contained lead-based paint (8). This potential environmental lead hazard appears to represent a significant health threat to wildlife on Midway based on several reports of increased morbidity (e.g., “droopwing” peripheral neuropathy) and mortality of Laysan albatross (Phoebastria immutabilis) chicks nesting in the vicinity of buildings (912). In fact, Work et al. (10) found that lead poisoning was a leading cause of mortality in chicks collected on Midway over the study years 1993-1995 (∼12% of 127 chicks collected), second only to enteritis. Work and Smith (9) attributed ingestion of lead-based paint chips from deteriorating buildings as the probable source of elevated lead levels in Laysan albatross chicks, substantiating a previous suggestion by Sileo and Fefer (11). These observations are alarming since Midway hosts the largest known breeding population of Laysan albatross, accounting for ∼50% of the world’s population (13). The above studies provided compelling evidence of lead hazards to Laysan albatross on Midway. However, they were unable to clearly demonstrate the specific sources and pathways of exposure, due primarily to limitations in lead concentration measurements as a method to distinguish sources of lead exposure. Furthermore, while lead hazards on Midway have undergone some degree of on-site remediation during 1994-1997 (8), it remains unclear whether those efforts were successful in reducing lead exposures to Laysan albatross chicks. These questions can be addressed with the use of lead isotope fingerprinting techniques. Lead isotope ratios have been used to determine the biogeochemical cycles of lead in the environment (14-16) as well as to investigate the sources and pathways of lead exposure to humans (17-21) and to a lesser extent wildlife (7, 22-25). The use of lead isotope ratios as a tracer methodology for evaluating lead exposure is based upon differences in the relative amounts of the four naturally occurring isotopes of lead: 204Pb, 206Pb, 207Pb, and 208Pb. The natural relative abundances of these isotopes vary between different geologic sources of lead, and these isotopic differences persist when the lead is mined and incorporated into industrial materials, such as lead-based paints. Typically, industrial leads contain a mixture of leads from different geologic sources as well as substantial amounts of recycled lead (22, 26-28). Here we investigated the persistent presence of lead hazards on Sand Island, Midway Atoll, using lead isotopes to identify sources and pathways of lead exposure to Laysan albatross chicks.

Methods Study Area. This study was conducted on Sand Island, Midway Atoll (28°13′ N latitude, 177°22′ W longitude), located approximately 1800 km northwest of Honolulu. Two study sites were utilized: a “reference” site with no known source of lead contamination and a “building” site containing multiple building structures. The reference site was composed of a plot (∼700 m2) within an open grass field, located >100 m from the nearest buildings, with no evidence or history of modern building structures. The building site was composed of a 5-m perimeter zone surrounding building structures located on the eastern side of the island. All of the buildings 10.1021/es026272e CCC: $25.00

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in the building site were used for housing and recreation. The buildings were constructed with exterior wood siding and exhibited various degrees of deteriorating paint, from minor flaking to extreme deterioration, where the ground around the building structures contained visible paint chips. Four building complexes were sampled: two were currently occupied and two were unoccupied. All samples were collected in May of 2000 and 2001. Sample Collection. Whole blood from Laysan albatross chicks, nest soil, and paint chips were collected for analyses. Because Laysan albatross are synchronistic breeders (13), all chicks were of similar ages (∼3.5-4.5 months old) when sampled. Laysan albatross hatch one chick per year, and their nests consist of a depression in the sand/dirt/grass with a rim (twigs, leaves, sand, etc. dragged up from the depression) of variable height (13). Fifteen blood and matching nest soil samples were collected from chicks from the reference site. Blood samples were collected from 21 chicks from the building site, including 14 that exhibited droopwing. Matching nest soil samples were collected from 10 of these chicks (3 droopwing and 7 normal), while paint chips were collected specifically from nests of 7 of the remaining chicks (all droopwing). In addition, whole blood was collected opportunistically from 10 Laysan albatross adults in several locations on the island, excluding the reference and building sites. All birds were released immediately following sampling. All chicks and adults were hand-caught, and 3 (chicks) or 6 mL (adults) of blood was collected from the cutaneous ular vein with a 21-g Vacutainer winged collection kit attached to a pre-heparinized syringe. Blood was then transferred to low-lead heparinized Vacutainers (Fisher Scientific, Pittsburgh, PA) and frozen at -20 °C until analysis. A composite nest soil sample composed of five subsamples (∼5 g each) taken to a depth of 1-2 in. was collected from the nest cup using a clean stainless steel trowel and stored double-bagged in individual plastic bags. The trowel was wiped clean between samplings to prevent cross contamination. Blanks to account for potential contamination of blood samples were collected by drawing 3-6 mL of ultrapure quartz distilled Milli-Q water (stored in acid-cleaned Teflon vials) through the blood collection apparatus and dispensing it into Vacutainers. Lead Concentration and Stable Isotope Analysis. All sample processing was conducted under trace metal clean HEPA-filtered air (Class 100) laboratory conditions using clean techniques (29). Laboratory water was high purity grade (Milli-Q system, 18 MΩ‚cm2), and acids were subboiling quartz double-distilled. Laboratoryware was acid-cleaned following procedures detailed elsewhere (30). Blood aliquots (0.5-1 mL) were transferred to Teflon vials, weighed, evaporated to dryness, and digested overnight with 2 mL of subboiling concentrated HNO3 in closed vials. The concentrated acid was evaporated to dryness, and samples were reconstituted in 1 N HNO3 for analyses. Soil and paint samples were oven-dried and pulverized to homogeneity with a mortar and pestle. An aliquot of soil (2 g) or paint (0.1-0.2 g) was transferred into 30-mL polyethylene bottles and leached with 15 (for soils) or 5 mL (for paints) of 0.5 N HCl at room temperature for 24 h on a shaker table. The leachate was centrifuged at 1400g for 10 min, and the supernatant was diluted in 1 N HNO3. This weak acid leaching was performed in order to approximate the biologically available fraction of ingested soil or paint lead. In addition, separate aliquots of paint samples were digested overnight in 2 mL of subboiling concentrated HNO3 to produce a near total measure of paint lead levels that is more consistent with the analysis and identification of lead-containing paints used in human risk assessment. All samples were screened for their approximate lead concentration using a Perkin-Elmer Optima 4300 optical

FIGURE 1. Lead concentrations and isotopic ratios of composite soil samples collected from nests within the reference (open circle) and building (filled circle) sites on Sand Island, Midway Atoll. Soil lead concentrations or isotopic compositions were not measurably different between the two sites (p ) 0.11, Mann-Whitney U; n ) 15 for reference and n ) 10 for building sites). emission spectrophotometer (OES). These values were used to prepare diluted samples of ∼50 ng/mL lead for analyses of lead concentrations and isotopic compositions with a Finnigan MAT-Element 1 double-focusing magnetic sector inductively coupled plasma mass spectrometer (ThermoQuest, San Jose, CA) using methods described elsewhere (17, 31). Measured masses were 206Pb, 207Pb, 208Pb, and 209Bi. Bismuth-209 (209Bi) was added to the samples as an internal standard before injection into the instrument. External standardization for lead isotopes was via the National Institute of Standards and Technology (NIST) Standard Reference Material (SRM) 981 isotopic standard. NIST SRM 955 (lead in blood) was used to validate accuracy of the blood lead measurements. Replicate measurement (intra-sample analysis, n ) 3-4) precisions of the 207Pb/206Pb ratio of blood and soil samples were 0.07% and 0.09% (2 relative standard deviations (RSD)), respectively. Inter-sample analysis precision of 207Pb/206Pb ratios of the standard reference material lead in bovine blood NIST 955b was 0.20% (2 RSD, n ) 5 different days). Statistics. Data were analyzed using analysis of variance (ANOVA), linear regression, or nonparametric tests (MannWhitney U, Spearman rank correlation) when appropriate. For significant ANOVA effects, differences among means were determined using the Tukey pairwise-comparison test. Significance was reported if p < 0.05. All statistical tests were performed using SYSTAT (SPSS Inc., 10th ed., 2000).

Results Lead Concentrations in Nest Soil, Paint, and Blood. No difference was detected in lead concentrations between nest soil collected from the building (n ) 10) or reference sites (n ) 15) (p ) 0.11, Mann-Whitney U, Figure 1). The geometric mean of nest soil lead concentrations from the reference site was 1.6 µg/g (average ) 3.0 ( 3.4 SD, range ) 0.05-11 µg/g, n ) 15), while the geometric mean of nest soil concentrations from the building site was 1.1 µg/g (average ) 7.1 ( 20 SD, range ) 0.3-64 µg/g, n ) 10). Paint chip samples processed using the 0.5 N hydrochloric acid leach procedure had a geometric mean of 29 000 µg/g (average ) 35 000 ( 19 000 SD, range ) 5500-56 000, n ) 7). Typically, this weak acid leach yielded lead concentrations that were ∼75% of the sample lead levels extracted using the concentrated nitric acid digestion procedure (geometric mean ) 35 000 µg/g, average ) 47 000 ( 31 000 SD, range ) 5800-88 000, n ) 7). All paint samples analyzed yielded lead levels >5000 µg/g VOL. 37, NO. 15, 2003 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 2. Blood lead concentrations of Laysan albatross chicks from the reference and building sites on Sand Island and adult Laysan albatross from multiple sites on the island. The box plot shows the median (horizontal line within the box), 25th and 75th percentiles (lower and upper margin of the box), and 10th and 90th percentiles (lower and upper hash marks) as well as outliers. Blood lead concentrations between groups were significantly different from each other (one-way ANOVA, F3,42 ) 130 on log-transformed data, p < 0.001; Tukey, p < 0.001 for all comparisons). and thus can be classified as lead-based paint according to the U.S. Environmental Protection Agency (32). The geometric mean blood lead level in chicks from the reference site was 4.5 µg/dL (average ) 6.0 ( 4.2 SD, range ) 1.2-13, n ) 15, Figure 2). In contrast, the geometric mean blood lead level of building site non-droopwing chicks was 48 µg/dL (average ) 85 ( 77 SD, range ) 6.8-200, n ) 7), while the blood lead level in droopwing chicks was 370 µg/ dL (average ) 440 ( 310 SD, range ) 120-1400, n ) 14) (Figure 2). Blood lead levels in adult Laysan albatross collected from various sites within the colony had a geometric mean of 0.85 µg/dL (average ) 1.0 ( 0.95 SD, range ) 0.41-3.7, n ) 10). Lead levels in all four of these groups (reference site, building site non-droopwing, building site droopwing, and adults) were significantly different from each other (oneway ANOVA, F3,42 ) 130 on log-transformed data, p < 0.001; Tukey post-hoc, p < 0.001 for all comparisons, Figure 2). Lead Isotope Ratios in Nest Soil, Paint, and Blood. No significant difference was found between the lead isotopic compositions of nest soils collected from the building (n ) 10) and reference (n ) 15) sites (Figure 1, p ) 0.11, MannWhitney U). Moreover, there was no significant correlation (p > 0.05, Spearman rank) between soil lead isotopic composition and lead concentration for the reference (r ) 0.487, n ) 15) or building (r ) -0.11, n ) 10) sites. Soil lead isotopic compositions differed widely among samples within each site: reference site 207Pb/206Pb ratios ranged from 0.828 to 0.869, while building site 207Pb/206Pb ratios ranged from 0.840 to 0.897 (Figure 1). No relationship (linear regression) was found between isotopic compositions of lead in chick blood and lead in nest soil (with no visible paint chips) from the building site (r 2 ) 0.363, p ) 0.152, n ) 6) or reference site (r 2 ) 0.224, p ) 0.074, n ) 15) (Figure 3a), substantiating that soil was not the source of lead contamination to the chicks. However, blood lead isotopic compositions of droopwing chicks from the building site were significantly related to the lead isotopic compositions of paint chips collected from the chick’s nest (r 2 ) 0.853, p ) 0.003, n ) 7; Figure 3b), indicating that paint chips were responsible for the lead poisoning in these chicks. As with soil lead isotopic compositions noted above, the lead isotopic compositions of lead in blood and paint chips also 3258

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FIGURE 3. 207Pb/206Pb ratios of nest soil or leached paint vs the 207Pb/206Pb ratio of blood from chicks for each nest-chick pair collected from the reference and building sites. (a) No significant relationship was found between blood and nest soil (no visible paint chips) 207Pb/206Pb ratios of chicks from the building site (filled circle, solid regression line; r 2 ) 0.363 linear regression, p ) 0.152, n ) 6) or in chicks from the reference site (open circle, dashed regression line; r 2 ) 0.224, p ) 0.074, n ) 15). (b) The 207Pb/206Pb ratios in blood of droopwing chicks from the building site were significantly related to ratios in paint collected from their nests (r 2 ) 0.853, p ) 0.003, n ) 7). differed widely between samples (207Pb/206Pb ) 0.838-0.908 for chicks and 207Pb/206Pb ) 0.824-0.887 for paint). Finally, it is noteworthy that the lead isotopic compositions of paint samples processed using a 0.5 N hydrochloric acid weak leach and strong nitric acid digestion were measurably different. Moreover, the 207Pb/206Pb ratios of the leached paint explained a greater amount of the variability of 207Pb/206Pb ratios of the matching chick’s blood than did the ratios of the concentrated HNO3 digested sample of the same paint (linear regression, weak leach r 2 ) 0.852, p ) 0.003 vs concentrated HNO3 r 2 ) 0.701, p ) 0.019).

Discussion The isotopic agreement between lead in blood and paint chips clearly shows that lead-containing paints from decommissioned military buildings on Midway serve as a significant source of lead poisoning to Laysan albatross. Moreover, the disagreement between blood and soil lead isotopic compositions shows that the route of exposure to lead poisoned birds is through direct ingestion of lead paint chips and not from lead-contaminated soil. These results are significant for several reasons. First, they demonstrate the continued presence of an environmental and wildlife health problem

on Midway despite efforts to scrape lead-based paint from buildings and repaint with lead-free oil-based paint (8). Second, they demonstrate a unique pathway of lead exposure to wildlife (direct exposure to leaded paint), while excluding a soil/dust lead exposure pathway, which is the predominant pathway of exposure to lead poisoned children in the United States (33, 34). Third, these results on Midway are likely representative of a much larger problem underlying the closure of U.S. military bases elsewhere and their conversion to designated wildlife habitat. Exposure/Poisoning. Laysan albatross chicks from the building site appear to be exposed to lead-based paint by picking at and ingesting deteriorating paint directly from buildings or by ingesting paint chips that have fallen in/ around their nests through weathering of the buildings. Chicks were observed playing with and ingesting paint chips on several occasions, and past studies have documented paint chips in the proventriculus of lead-poisoned chicks on Midway (9, 11, 12). Adult Laysan albatross at the building site were never observed to eat or move paint chips around, which is supported by their low blood lead values observed here (geometric mean of 0.85 µg/dL) and in previous studies (9, 11). Laysan albatross chicks at the reference site had significantly higher blood lead concentrations than adults from the colony (Figure 2). The source of lead exposure to these chicks is unknown. A food source is doubtful since a large proportion of the chick’s diet is oil derived from the adult’s food (13), and adults have very low blood lead concentrations. Midway has had multiple uses over the past century and was the center of a major battle during World War II. Therefore, low to moderate level lead exposure from ingestion of various unidentified lead-containing debris is a possibility for many chicks, including those at the reference site. We identified 26 droopwing chicks with lead poisoning surrounding three buildings with deteriorated lead-based paint. Since there may be as many as 215 buildings on Midway with lead-based paint (8), the number of droopwing lead poisoned chicks in a given year could be substantial. Perhaps more important, the total number of birds suffering detrimental effects from lead exposure on Midway is certainly larger than the number of dead or droopwing chicks on the basis of the geometric mean blood lead level of 48 µg/dL in nondroopwing chicks at the building site. Lead exposure effects to Laysan chicks in the absence of droopwing is substantiated by a study in red-tailed hawks that showed lead-induced immune dysfunction without clinical signs of toxicity (35) as well as a study in an avian model (chickens) that demonstrated significant effects of low-level lead exposure on the developing immune system (36). Lead-induced neurological effects have also been observed in avian species. Dey et al. (37) illustrated that developmental exposure to lead disrupted the expression of synaptic neural cell adhesion molecules in young herring gull hatchlings. These avian studies are consistent with studies in mammals, including humans, showing significant impairment of immune, neurological and renal function at low to moderate lead exposures (e.g., blood lead levels e 30 µg/dL) that otherwise may not produce overt symptoms of toxicity (38-41). Thus, the elevated blood lead levels observed in albatross chicks at the building site are sufficiently high to indicate immunological and neurological toxic effects in the absence of overt signs of dysfunction (e.g., droopwing syndrome), which could decrease their fitness and survival. Isotopes. Lead isotopic fingerprinting has been used successfully in a variety of lead exposure studies. Some of these studies have evaluated the relative contributions of potential lead sources to exposed individuals (17, 20) or changes in lead exposure sources over time to wildlife and humans (7, 22, 42, 43). Scheuhammer and Templeton (7)

used lead isotopes to determine if lead shot ammunition pellets were the source of lead exposure to wild birds. However, the wide range in isotopic compositions of the pellets analyzed made interpretation of their findings difficult. A more recent study by Meharg et al. (25) successfully used lead isotopes to establish that white storks (Ciconia ciconia) were exposed to contaminated acid mining sludge 1 yr after a spill because the sludge had a different lead isotopic signature than reference sediments in the area. In general, we have found that lead isotope fingerprinting is most informative in studies that take a “case study”-type approach, in which all likely potential sources of exposure are identified for each case (44). In addition, when evaluating lead exposure sources, consideration should be given to differences measured in lead isotope ratios between samples prepared using weak acid leach versus strong acid digestion methods. A weak acid leach preparation method may provide a more relevant measure of the fraction of lead that is biologically assimilated following ingestion, based on the assumption that weak acid leaches (e.g., 0.5 N HCl) more closely approximate the acid conditions of the digestive tract than do strong acid digestions. Military bases, especially ones with a complex history such as Midway, are a composite of multiple possible sources of lead. Midway is a coral atoll, although its surface has been supplemented with more than 9000 t of soil shipped in from Honolulu and Guam in the early 1900s (8). This imported soil in combination with the varied military activities that have occurred on Midway may explain the large range in soil lead isotopic ratios observed within the reference and building sites (Figure 1). For example, this range in soil 207Pb/206Pb compositions (0.828-0.897) is comparable to the range of lead isotopic compositions for gasoline additives used across the United States (0.82-0.88) (45). Midway contains over 250 building structures, some dating back to 1903. On the basis of the limited sampling of this study, there are significant differences in the isotopic compositions of paints used on these buildings (e.g., 207Pb/ 206Pb ratios ranging from 0.824 to 0.887). The differences in paint isotopic ratios are not surprising since the sources of lead used in the production of paint pigments varied over time and between different paint pigment manufacturers (46). Because of the wide range of paint lead isotopic ratios on Midway, using a case study approach to match the isotopic composition of paint chips collected from a chick’s nest with the isotopic composition of lead in its blood was essential to identify paint as the source of lead exposure. Management Recommendations. Lead-based paint remediation on Midway should be conducted according to the U.S. Department of Housing and Urban Development Guidelines for the Evaluation and Control of Lead-Based Paint Hazards in Housing (47). Since Midway is subject to extreme weathering processes, proper containment of deteriorating lead-based paint may prove challenging. Known lead hazards must either be suitably contained or removed from the island because of the clear health risk to both wildlife and human occupants. Furthermore, extreme caution should be used when removing lead-based paint from buildings; Work and Smith (9) observed that routine maintenance of a building on Midway without proper containment of paint chips resulted in large numbers of droopwing chicks. In conclusion, this study found that Laysan albatross chicks on Sand Island, Midway Atoll, continue to be exposed to substantially elevated levels of lead from the ingestion of lead-based paint. The existence of this problem is in direct contradiction to the designation of Midway as a U.S. National Wildlife Refuge. This study also demonstrates that lead isotopic fingerprinting can be an effective tool to determine the source and risk of lead exposure to wildlife. However, a case study approach is necessary to ensure that all possible VOL. 37, NO. 15, 2003 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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sources of lead are considered. The isotopic fingerprinting method is especially useful in situations with a complex history of lead contamination, such as decommissioned military bases.

Acknowledgments We are grateful for the assistance of Bradford S. Keitt, Donald Croll, Bernie Tershy, Brook Gamble, Wayne Sentman, Jen Schramm, Molly Church, Thierry Work, Doug Woolard, Rob Franks, and the U.S. Fish and Wildlife Service, in particular Nancy Hoffman and Lee Ann Woodward. We also thank the three anonymous reviewers for their valuable comments on this manuscript. This research was funded by the U.S. Environmental Protection Agency (EPA STAR Graduate Fellowship), the University of California Toxic Substance and Research Program, and the Switzer Environmental Fellowship Program.

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Received for review October 24, 2002. Revised manuscript received May 8, 2003. Accepted May 9, 2003. ES026272E