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Avian Urine: Its Potential as a Non-Invasive Biomonitor of Environmental Metal Exposure in Birds

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Abstract

Current non-invasive biomonitoring techniques to measure heavy metal exposure in free ranging birds using eggs, feathers and guano are problematic because essential metals copper (Cu) and zinc (Zn) deposited in eggs and feathers are under physiological control, feathers accumulate metals from surface contamination and guano may contain faecal metals of mixed bioavailability. This paper reports a new technique of measuring lead (Pb), Cu and Zn in avian urate spheres (AUS), the solid component of avian urine. These metal levels in AUS (theoretically representing the level of metal taken into the bloodstream, i.e. bioavailable to birds) were compared with levels in eggs (yolk and shell), feathers and whole guano from chickens (Gallus gallus domesticus) exposed to a heavy metal-contaminated soil (an allotment soil containing Pb 555 mg kg−1 dry mass (dm), Cu 273 mg kg−1 dm and Zn 827 mg kg−1 dm). The median metal levels (n = 2) in AUS from chickens exposed to this contaminated soil were Pb 208 μg g−1 uric acid, Cu 66 μg g−1 uric acid and Zn: 526 μg g−1 uric acid. Lead concentrations in egg yolk and shell samples (n = 3) were below the limit of detection (<2 mg kg−1), while Cu and Zn were only consistently detected in the yolk, with median values of 3 and 70 mg kg−1 (dm), respectively, restricting the usefulness of eggs as a biomonitor. Feathers (n = 4) had median Pb, Cu and Zn levels respectively of 15, 10 and 140 mg kg−1 (dm), while whole guano samples (n = 6) were 140, 70 and 230 mg kg−1 (dm). Control samples were collected from another chicken flock; however, because they had no access to soil and their diet was significantly higher in Cu and Zn, no meaningful comparison was possible. Six months after site remediation, by top soil replacement, the exposed chickens had median Pb, Cu and Zn levels respectively in whole guano (n = 6) of 30, 20 and 103 mg kg−1 (dm) and in AUS (n = 4) of 147, 16 and 85 μg g−1 uric acid. We suggest the persistent high Pb level in AUS was a consequence of bone mobilised for egg production, releasing chronically sequestered Pb deposits into the bloodstream. In contrast, AUS levels of Cu and Zn (metals under homeostatic control and sparingly stored) had declined, reflecting the lower current exposure. However because pre- and post-remediation samples were measured using different methods carried out at different laboratories, such comparisons should be guarded. The present study showed that metals can be measured in AUS, but no assessment could be made of availability or uptake to the birds because tissue and blood samples were not concomitantly analysed. A major short coming of the study was the inappropriate control group, having no access to uncontaminated soil and being fed a different diet to the exposed birds. Furthermore guano and urine analysis should have been carried out on samples from individual birds, so biological (rather than just technical) variation of metal levels could have been determined. Future studies into using AUS for biomonitoring environmental heavy metals must resolve such experimental design issues.

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References

  • Ademuyiwa, O., Arowolo, T., Ojo, D. A., Odukoya, O. O., Yusuf, A. A., & Akinhanmi, T. F. (2002). Lead levels in blood and urine of some residents of Abeokuta, Nigeria. Trace Elements and Electrolytes, 19(2), 63–69.

    CAS  Google Scholar 

  • Adeola, O., & Rogler, J. C. (1994). Comparative extraction methods for spectrophotometric analysis of uric acid in avian excreta. Archives of Animal Nutrition-Archiv Fur Tierernahrung, 47(1), 1–10.

    CAS  Google Scholar 

  • Al-Asheh, S., Banat, F., & Al-Rousan, D. (2003). Beneficial reuse of chicken feathers in removal of heavy metals from wastewater. Journal of Cleaner Production, 11(3), 321–326.

    Article  Google Scholar 

  • Bal, W., Christodoulou, J., Sadler, P. J., & Tucker, A. (1998). Multi-metal binding site of serum albumin. Journal of Inorganic Biochemistry, 70(1), 33–39.

    Article  CAS  Google Scholar 

  • Beyer, W. N., Connor, E. E., & Gerould, S. (1994). Estimates of soil ingestion by wildlife. Journal of Wildlife Management, 58(2), 375–382.

    Article  Google Scholar 

  • Beyer, W. N., Spann, J. W., Sileo, L., & Franson, J. C. (1988). Lead poisoning in six captive avian species. Archives of Environmental Contamination and Toxicology, 17, 121–130.

    Google Scholar 

  • Braun, E. J., & Pacelli, M. M. (1991). The packaging of uric acid in avian urine. The FASEB Journal, A1408.

  • Burger, J., & Gochfeld, M. (1993). Lead and cadmium accumulation in eggs and fledgling seabirds in the New-York bight. Environmental Toxicology and Chemistry, 12(2), 261–267.

    Article  CAS  Google Scholar 

  • Burger, J., Nisbet, I. C. T., & Gochfeld, M. (1992). Metal Levels In regrown feathers—assessment of contamination on the wintering and breeding grounds in the same individuals. Journal of Toxicology and Environmental Health, 37(3), 363–374.

    Article  CAS  Google Scholar 

  • Casotti, G., & Braun, E. J. (1997). Ionic composition of urate-containing spheres in the urine of domestic fowl. Comparative Biochemistry and Physiology, Part A 118(3), 585–588.

    Google Scholar 

  • Casotti, G., & Braun, E. J. (2004). Protein location and elemental composition of urine spheres in different avian species. Journal of Experimental Zoology Part A-Comparative Experimental Biology, 301A(7), 579–587.

    Article  CAS  Google Scholar 

  • CDC (2009). Fourth national report on human exposure to environmental chemicals. Atlanta, GA: Centers for Disease Control and Prevention. Available: http://www.cdc.gov/exposurereport/. Accessed 10 April 2012.

  • Clark, H. F., Brabander, D. J., & Erdil, R. M. (2006). Sources, sinks, and exposure pathways of lead in urban garden soil. Journal of Environmental Quality, 35(6), 2066–2074.

    Article  CAS  Google Scholar 

  • Dacke, G. C. (2000). In G. C. Whittow (Ed.), Sturkie’s avian physiology (5th ed., Vol. Chapter 18, pp. 472–485). London: Academic.

    Google Scholar 

  • Dauwe, T., Bervoets, L., Pinxten, R., Blust, R., & Eens, M. (2003). Variation of heavy metals within and among feathers of birds of prey: effects of moult and external contamination. Environmental Pollution, 124(3), 429–436.

    Article  CAS  Google Scholar 

  • Dauwe, T., Janssens, E., Bervoets, L., Blust, R., & Eens, M. (2005). Heavy-metal concentrations in female laying great tits (Parus major) and their clutches. Archives of Environmental Contamination and Toxicology, 49(2), 249–256.

    Article  CAS  Google Scholar 

  • Davies, K. J. A., Sevanian, A., Muakkassahkelly, S. F., & Hochstein, P. (1986). Uric-acid iron-ion complexes—a new aspect of the antioxidant functions of uric-acid. Biochemical Journal, 235(3), 747–754.

    CAS  Google Scholar 

  • DEFRA (2000). Statutory guidance. UK DETR circular 2/2000.

  • Drees, L. R., & Manu, A. (1996). Bird urate contamination of atmospheric dust traps. Catena, 27(3–4), 287–294.

    Article  CAS  Google Scholar 

  • Eisler, R. (2000). Handbook of chemical risk assessment. Vol 1 Metals (pp. 264–273). Boca Raton: Lewis, CRC.

    Book  Google Scholar 

  • EPA publication number 600491010 (1991). Methods for the determination of metals in environmental samples. Office of Research and Development, Washington DC 20460. Available at http://www.epa.gov/nscep/index.html. Accessed 10 April 2012.

  • Fitzner, R. E., Gray, R. H., & Hinds, W. T. (1995). Heavy-metal concentrations in great blue heron fecal castings in Washington State—a technique for monitoring regional and global trends in environmental contaminants. Bulletin of Environmental Contamination and Toxicology, 55(3), 398–403.

    Article  CAS  Google Scholar 

  • Flores, R., & Martins, A. F. (1997). Distribution of trace elements in egg samples collected near coal power plants. Journal of Environmental Quality, 26(3), 744–748.

    Article  CAS  Google Scholar 

  • Fossi, M. C. (1994). Nondestructive biomarkers in ecotoxicology. Environmental Health Perspectives, 102, 49–54.

    Article  Google Scholar 

  • Franson, J. C., & Custer, T. W. (1982). Toxicity of dietary lead in young cockerels. Veterinary and Human Toxicology, 24, 421–423.

    CAS  Google Scholar 

  • Furness, R. W. (1993). Birds as monitors of pollutants. In R. W. Furness & J. J. D. Greenwood (Eds.), Birds as monitors of environmental change (pp. 86–143). London: Chapman & Hall.

    Google Scholar 

  • Gomez, G., Baos, R., Gomara, B., Jimenez, B., Benito, V., Montoro, R., Hiraldo, F., & Gonzalez, M. J. (2004). Influence of a mine tailing accident near Donana National Park (Spain) on heavy metals and arsenic accumulation in 14 species of waterfowl (1998 to 2000). Archives of Environmental Contamination and Toxicology, 47(4), 521–529.

    Article  CAS  Google Scholar 

  • Grand, J. B., Franson, J. C., Flint, P. L., & Petersen, M. R. (2002). Concentrations of trace elements in eggs and blood of spectacled and common eiders on the Yukon-Kuskokwim Delta, Alaska, USA. Environmental Toxicology and Chemistry, 21(8), 1673–1678.

    CAS  Google Scholar 

  • Hartley, C.P., Vizard, K., & Air, V. (2004). Branxton A and Branxton B allotment sites. Desk top study and site investigation. Newcastle City Council. Public Health and Environmental Protection. Civic Centre, Newcastle upon Tyne, NE1 8PB, UK.

  • Hogstad, O., Nygard, T., Gatzschmann, P., Lierhagen, S., & Thingstad, P. G. (2003). Bird skins in museum collections: are they suitable as indicators of environmental metal load after conservation procedures? Environmental Monitoring and Assessment, 87(1), 47–56.

    Article  CAS  Google Scholar 

  • Hollamby, S., Afema-Azikuru, J., Waigo, S., Cameron, K., Gandolf, A. R., Norris, A., & Sikarskie, J. G. (2006). Suggested guidelines for use of avian species as biomonitors. Environmental Monitoring and Assessment, 118(1–3), 13–20.

    Article  CAS  Google Scholar 

  • Hu, H., Rabinowitz, M., & Smith, D. (1998). Bone lead as a biological marker in epidemiologic studies of chronic toxicity: conceptual paradigms. Environmental Health Perspectives, 106(1), 1–8.

    Article  CAS  Google Scholar 

  • Jaspers, V., Dauwe, T., Pinxten, R., Bervoets, L., Blust, R., & Eens, M. (2004). The importance of exogenous contamination on heavy metal levels in bird feathers. A field experiment with free-living great tits, Parus major. Journal of Environmental Monitoring, 6(4), 356–360.

    Article  Google Scholar 

  • Jaspers, V. L. B., Rodriguez, F. S., Boertmann, D., Sonne, C., Dietz, R., Rasmussen, L. M., Eens, M., & Covaci, A. (2011). Body feathers as a potential new biomonitoring tool in raptors: a study on organohalogenated contaminants in different feather types and preen oil of West Greenland white-tailed eagles (Haliaeetus albicilla). Environment International, 37, 1349–1356.

    Article  CAS  Google Scholar 

  • JFWEC (1999) Joint FAO/WHO Expert Committee on food additives, Report TRS 896-JECFA 53/81, Monograph FAS 44-JECFA 53/273.

  • Kannan, K., & Falandysz, J. (1997). Butyltin residues in sediment, fish, fish-eating birds, harbour porpoise and human tissues from the Polish coast of the Baltic Sea. Marine Pollution Bulletin, 34, 203–207.

    Article  CAS  Google Scholar 

  • King, A. S., & McLelland, J. (1975). Outlines of avian anatomy (pp. 25–26). London: Bailliere Tindall.

    Google Scholar 

  • Kunkle, W. E., Carr, L. E., Carter, T. A., & Bossard, E. H. (1981). Effect of flock and floor type on the levels of nutrients and heavy-metals in broiler litter. Poultry Science, 60(6), 1160–1164.

    Google Scholar 

  • Mazliah, J., Barron, S., Bental, E., & Reznik, I. (1989). The effect of chronic lead-intoxication in mature chickens. Avian Diseases, 33(3), 566–570.

    Article  CAS  Google Scholar 

  • McGrath, S. P., & Loveland, P. (1992). The soil geochemical atlas of England and Wales. London: Blackie Academic and Professional.

    Google Scholar 

  • McNabb, R. A., & McNabb, F. M. A. (1980). Physiological chemistry of uric acid: solubility, colloid and ion binding properties. Comparative Biochemistry and Physiology, Part A 67, 27–34.

    Google Scholar 

  • Meharg, A. A., & French, M. C. (1995). Heavy-metals as markers for assessing environmental pollution from chemical warehouse and plastics fires. Chemosphere, 30(10), 1987–1994.

    Article  CAS  Google Scholar 

  • Mercier, G., Duchesne, J., & Blackburn, D. (2001). Prediction of metal removal efficiency from contaminated soils by physical methods. Journal of Environmental Engineering-Asce, 127(4), 348–358.

    Article  CAS  Google Scholar 

  • Mikulski, C. M., Holman, M. E., Tener, G., Dobson, T., Eang, S., Welsh, W., Nujoma, Y., & Karayannis, N. M. (1994). Urate complexes of dipositive first row transition-metal ions. Transition Metal Chemistry, 19(5), 491–493.

    Article  CAS  Google Scholar 

  • Mohanna, C., & Nys, Y. (1998). Influence of age, sex and cross on body concentrations of trace elements (zinc, iron, copper and manganese) in chickens. British Poultry Science, 39(4), 536–543.

    Article  CAS  Google Scholar 

  • Nam, D. H., Lee, D. P., & Koo, T. H. (2004). Monitoring for lead pollution using feathers of feral pigeons (Columba livia) from Korea. Environmental Monitoring and Assessment, 95(1–3), 13–22.

    Article  CAS  Google Scholar 

  • Nicholson, F. A., Chambers, B. J., Williams, J. R., & Unwin, R. J. (1999). Heavy metal contents of livestock feeds and animal manures in England and Wales. Bioresource Technology, 70(1), 23–31.

    Article  CAS  Google Scholar 

  • Pain, D. J., Bavoux, C., & Burneleau, G. (1997). Seasonal blood lead concentrations in marsh harriers Circus aeruginosus from Charente-Maritime, France: relationship with the hunting season. Biological Conservation, 81(1–2), 1–7.

    Article  Google Scholar 

  • Peakall, D., & Burger, J. (2003). Methodologies for assessing exposure to metals: speciation, bioavailability of metals, and ecological host factors. Ecotoxicology and Environmental Safety, 56(1), 110–121.

    Article  CAS  Google Scholar 

  • Pless-Mulloli, T., Air, V., Vizard, C., Singleton, I., Rimmer, D., & Hartley, P. (2004). The legacy of allotment gardens in industrial urban settings. Epidemiology, 15(4), S208–S209.

    Article  Google Scholar 

  • Rieuwerts, J. S., Farago, M. E., Cikrt, M., & Bencko, V. (2000). Differences in lead bioavailability between a smelting and a mining area. Water Air and Soil Pollution, 122(1–2), 203–229.

    Article  CAS  Google Scholar 

  • Rimmer, D. L., Vizard, C. G., Pless-Mulloli, T., Singleton, I., Air, V. S., & Keatinge, Z. A. F. (2006). Metal contamination of urban soils in the vicinity of a municipal waste incinerator: one source among many. Science of the Total Environment, 356(1–3), 207–216.

    Article  CAS  Google Scholar 

  • Ruby, M. V. (2004). Bioavailability of soil-borne chemicals: abiotic assessment tools. Human and Ecological Risk Assessment, 10, 647–656.

    Article  CAS  Google Scholar 

  • Scheifler, R., Coeurdassier, M., Morilhat, C., Bernard, N., Faivre, B., Flicoteaux, P., Giraudoux, P., Noel, M., Piotte, P., Rieffel, D., de Vaufleurs, A., & Badot, P. M. (2006). Lead concentrations in feathers and blood of common blackbirds (Turdus merula) and in earthworms inhabiting unpolluted and moderately polluted urban areas. Science of the Total Environment, 371(1–3), 197–205.

    Article  CAS  Google Scholar 

  • Scheuhammer, A. M., & Norris, S. L. (1996). The ecotoxicology of lead shot and lead fishing mass. Ecotoxicology, 5(5), 279–295.

    Article  CAS  Google Scholar 

  • Scheuhammer, A. M., Rogers, C. A., & Bond, D. (1999). Elevated lead exposure in American woodcock (Scolopax minor) in eastern Canada. Archives of Environmental Contamination and Toxicology, 36(3), 334–340.

    Article  CAS  Google Scholar 

  • Skrivan, M., Skrivanova, V., & Marounek, M. (2006). Effect of various copper supplements to feed of laying hens on Cu content in eggs, liver, excreta, soil, and herbage. Archives of Environmental Contamination and Toxicology, 50(2), 280–283.

    Article  CAS  Google Scholar 

  • Stephens, R. D., Petreas, M. X., & Hayward, D. G. (1995). Biotransfer and bioaccumulation of dioxins and furans from soil: chickens as a model for foraging animals. Science of the Total Environment, 175(3), 253–273.

    Article  CAS  Google Scholar 

  • Swaileh, K. M., & Sansur, R. (2006). Monitoring urban heavy metal pollution using the house sparrow (Passer domesticus). Journal of Environmental Monitoring, 8(1), 209–213.

    Article  CAS  Google Scholar 

  • Taylor, M. G., & Simkiss, K. (1989). Structural and analytical studies on metal ion-containing granules. In S. Mann, J. Webb, & R. J. P. Williams (Eds.), Biomineralisation: chemical and biochemical perspectives (pp. 427–460). Weinheim: VCH.

    Google Scholar 

  • Trampel, D. W., Imerman, P. M., Carson, T. L., Kinker, J. A., & Ensley, S. M. (2003). Lead contamination of chicken eggs and tissues from a small farm flock. Journal of Veterinary Diagnostic Investigation, 15(5), 418–422.

    Article  Google Scholar 

  • Van Handel, E. (1975). Direct determination of uric-acid in fecal material. Biochemical Medicine, 12(1), 92–93.

    Article  Google Scholar 

  • Vesk, P. A., & Byrne, M. (1999). Metal levels in tissue granules of the freshwater bivalve Hyridella depressa unionida for biomonitoring: the importance of cryopreparation. The Science of the Total Environment, 225, 219–229.

    Article  CAS  Google Scholar 

  • Walker, C. H., Hopkins, S. P., Sibly, R. M., & Peakall, D. B. (2001). Principles of ecotoxicology (2nd ed., pp. 3–6). New York: Taylor and Francis.

    Google Scholar 

  • Walsh, P. M. (1990). Use of seabirds as monitors of heavy metals in the marine environment. In R. W. Furness & P. S. Rainbow (Eds.), Heavy metals in the marine environment (pp. 183–204). Boca Raton: CRC.

    Google Scholar 

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Acknowledgments

We are grateful for the assistance of P. Hartley of Newcastle City Council in the collection of samples from the two allotments and the generous cooperation of the allotment gardeners. We thank Dave Dunbar for metal analysis and Grant Staines for SEM imaging and laboratory assistance from Fiona McLachlan, all from Newcastle University, UK.

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  1. School of Biology, Newcastle University, Ridley Building, Newcastle upon Tyne, NE1 7RU, UK

    J. B. Clapp, R. M. Bevan & I. Singleton

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  1. J. B. Clapp
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Clapp, J.B., Bevan, R.M. & Singleton, I. Avian Urine: Its Potential as a Non-Invasive Biomonitor of Environmental Metal Exposure in Birds. Water Air Soil Pollut 223, 3923–3938 (2012). https://doi.org/10.1007/s11270-012-1161-1

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