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      Monitoring of Pb Exposure in Waterfowl Ten Years after a Mine Spill through the Use of Noninvasive Sampling

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          Abstract

          Lead exposure in waterfowl was studied using noninvasive fecal sampling in the Guadalquivir Marshes in Spain, an area affected by the 1998 Aznalcóllar mine disaster. Feces of greylag geese ( Anser anser, n = 191) and purple gallinule ( Porphyrio porphyrio, n = 91) were collected from three different impacted sites (Entremuros, Caracoles and Cerro de los Ánsares) during the winters of 2004 to 2008. Lead and aluminium (an indicator of sediment ingestion) and Pb isotope signatures (to discriminate between sources of Pb exposure) were analyzed in freeze-dried, acid digested samples. The concentrations of fecal porphyrins and biliverdin were determined as noninvasive biomarkers to study Pb exposure effects. Results showed a decrease in Pb exposure over time in wintering greylag geese. In contrast, for purple gallinule resident in the Entremuros a clear trend was not evident. For both species, sediment ingestion appeared to be the main source of exposure to Pb. In the Entremuros, some samples from purple gallinule were detected with higher Pb levels than expected for simple soil ingestion, and these had Pb isotopic profiles compatible with mining sludge or Pb shot. Whilst fecal Pb isotopic profiles were effective in differentiating between samples from sites with different levels and sources of pollution, the combined use of element ratios (such as Pb/Al) and other non-traditional stable isotope signatures may also prove worthwhile. Overall, the fecal Pb levels detected were below those described in feces for waterfowl from other uncontaminated areas(<10 µg/g d.w.). Despite this, for both species fecal Pb levels were positively correlated with porphyrin excretion, and for purple gallinule, with the coproporphyrin III/I ratio, suggesting some subtle effects on heme synthesis in birds. Ten years after the mine spill, Pb contamination in birds by this pollution source was still detectable and subtlethal effects may persist.

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          Most cited references33

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          Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants.

          Iron plaque on aquatic plant roots are ubiquitous and sequester metals in wetland soils; however, the mechanisms of metal sequestration are unresolved. Thus, characterizing the Fe plaque and associated metals will aid in understanding and predicting metal cycling in wetland ecosystems. Accordingly, microscopic and spectroscopic techniques were utilized to identify the spatial distributions, associations, and chemical environments of Fe, Mn, Pb, and Zn on the roots of a common, indigenous wetland plant (Phalaris arundinacea). Iron forms a continuous precipitate on the root surface, which is composed dominantly of ferrihydrite (ca. 63%) with lesser amounts of goethite (32%) and minor levels of siderite (5%). Although Pb is juxtaposed with Fe on the root surface, it is complexed to organic functional groups, consistent with those of bacterial biofilms. In contrast, Mn and Zn exist as discrete, isolated mixed-metal carbonate (rhodochrosite/hydrozincite) nodules on the root surface. Accordingly, the soil-root interface appears to be a complex biochemical environment, containing both reduced and oxidized mineral species, as well as bacterial-induced organic-metal complexes. As such, hydrated iron oxides, bacterial biofilms, and metal carbonates will influence the availability and mobility of metals within the rhizosphere of aquatic plants.
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            Biomarkers of lead exposure.

            Biomarkers of exposure, effect, and susceptibility are reviewed in relation to lead exposure. Of the biomarkers of lead exposure, blood lead (Pb-B), mainly red cell lead, is a representative of soft tissue lead, and most widely used as measures of body burden and absorbed (internal) doses of lead. Urine lead (Pb-U) as well as plasma lead (Pb-P) increases exponentially with increasing Pb-B under a steady-state situation and is a reflection of recent exposure. The amount of lead in plasma and urine (MPb-P and MPb-U) after administration of a chelating agent (e.g. CaEDTA) can be useful for biomarkers of internal exposure of lead, reflecting the mobilizable pool of lead which consists of mainly blood and soft tissue lead with only a small fraction derived from bones. The critical effects in bone marrow arise mainly from the interaction of lead with some enzymatic process responsible for heme synthesis. The effects can be used for the biomarkers of effects. They are the inhibition of delta-aminolevulinic acid dehydratase (ALAD) and the variation in some metabolite concentrations (e.g. delta-aminolevulinic acid in urine (ALA-U), blood (ALA-B) or plasma (ALA-P), coproporphyrin in urine (CP), zinc protoporphyrin (ZP) in blood). The activities of pyrimidine nucleotidase (P5'N) and nicotinamide adenine dinucleotide synthetase (NADS) in blood are also decreased in lead exposure, and nucleotide contents in blood is altered in lead exposure. These effects of lead on human can be also useful biomarkers of effect. The differences in levels of heme precursors between two types of ALAD genotypes might be attributable to those in the affinity of different ALAD isozymes to lead. ALAD1 homozygotes have higher levels of ZP and ALA in comparison with ALAD2 carriers at the high lead exposure, suggesting that ALAD1 homozygotes might be more susceptible for disturbance in heme biosynthesis by lead than ALAD2 carriers.
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              Effects of lead exposure on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field.

              Medina lagoon in Andalusia has one of the highest densities of spent lead (Pb) shot in Europe. Blood samples from waterbirds were collected in 2006-2008 to measure Pb concentration (PbB), δ-aminolevulinic acid dehydratase (ALAD), oxidative stress biomarkers and plasma biochemistry. PbB above background levels (>20 μg/dl) was observed in 19% (n=59) of mallards (Anas platyrhynchos) and in all common pochards (Aythya ferina) (n=4), but common coots (Fulica atra) (n=37) and moorhens (Gallinula chloropus) (n=12) were all 6 μg/dl. In mallards, an inhibition of glutathione peroxidase (GPx) and an increased level of oxidized glutathione (oxGSH) in red blood cells (RBC) were associated with PbB levels >20 μg/dl. In coots, PbB levels were negatively related to vitamin A and carotenoid levels in plasma, and total glutathione in RBCs; and positively related with higher superoxide dismutase and GPx activities and % oxGSH in RBCs. Overall, the results indicate that previously assumed background levels of PbB for birds need to be revised. Copyright © 2011 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                20 February 2013
                : 8
                : 2
                : e57295
                Affiliations
                [1 ]Instituto de Investigación en Recursos Cinegéticos – IREC (CSIC-UCLM-JCCM), Ciudad Real, Spain
                [2 ]Department of Wetland Ecology, Estación Biológica de Doñana – EBD (CSIC), Sevilla, Spain
                [3 ]Environmental Research Institute (ERI), University of the Highlands and Islands, Thurso, Scotland
                [4 ]Department of Analytical Chemistry and Food Technology, Faculty of Environmental Sciences and Biochemistry, University of Castilla-La Mancha, Toledo, Spain
                University of Lethbridge, Canada
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MMH AJG RM. Performed the experiments: MMH HL AJG RCMD. Analyzed the data: MMH MAT RM. Wrote the paper: MMH MAT AJG RM.

                Article
                PONE-D-12-29184
                10.1371/journal.pone.0057295
                3577725
                23437364
                13d7f6ad-1315-4b7a-b21f-0b330a370187
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 September 2012
                : 20 January 2013
                Page count
                Pages: 8
                Funding
                M. Martinez-Haro was supported by a project funded by the Consejería, de Medio Ambiente, Junta de Andalucía, under a CSIC contract. This study was also funded by MICINN (under CGL2007-62797). Currently, M. Martinez-Haro is supported by a postdoctoral grant (Ref: SFRH/BPD/73890/2010) funded by the Portuguese Foundation for Science and Technology (FCT), the European Social Fund and POPH programme. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Conservation Science
                Environmental Protection
                Earth Sciences
                Marine and Aquatic Sciences
                Water Quality
                Heavy Metals
                Veterinary Science
                Animal Types
                Wildlife
                Veterinary Toxicology

                Uncategorized
                Uncategorized

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