Abstract

Urban geochemistry is an emerging field in which key scientific and societal challenges, including rapid urbanization and population growth, compel investigation of readily accessible biomonitors to determine the source, transport and fate of heavy metal pollutants in cities. Lead isotopic analyses of honey have recently proven its efficacy as a biomonitor for Pb source apportionment applications. We collected honey directly from hives in six geographical sectors in Vancouver, British Columbia (Canada) to investigate the presence of potential pollutants from varying zoning districts: urban, industrial, residential and agricultural. Systematic variations in trace element concentrations and Pb isotopic compositions of the honeys reflect proximity to anthropogenic land-use activities such as shipping ports and heavy traffic. Honey sampled from downtown hives, near the Port of Vancouver, shows elevated trace element concentrations compared with suburban and rural honey, and distinctly higher 208Pb/206Pb (that is, less radiogenic) compared with local environmental proxies (for example, oysters, Fraser River sediment and volcanic rocks), indicating possible input from Asian anthropogenic sources. This study presents the first Pb isotope data for North American honey, and supports the combined use of trace elements and Pb isotopic compositions in honey as a geochemical biomonitor.

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References

  1. 1.

    United Nations, Department of Economic and Social Affairs, Population Division World Urbanization Prospects: The 2014 Revision (ST/ESA/SER.A/366) (2015). .

  2. 2.

    United Nations, Department of Economic and Social Affairs, Population Division World Population Prospects: The 2017 Revision, Key Findings and Advance Tables. Working Paper No. ESA/P/WP/248 (2017). .

  3. 3.

    Landrigan, P. J. et al. The Lancet Commission on pollution and health. Lancet 391, 462–512 (2017).

  4. 4.

    Chambers, L. G. et al. Developing the scientific framework for urban geochemistry. Appl. Geochem. 67, 1–20 (2016).

  5. 5.

    Holt, E. A. & Miller, S. W. Bioindicators: using organisms to measure environmental impacts. Nat. Educ. Knowl. 3, 8 (2010).

  6. 6.

    Watmough, S. A. Monitoring historical changes in soil and atmospheric trace metal levels by dendrochemical analysis. Environ. Pollut. 106, 391–403 (1999).

  7. 7.

    Novak, M. et al. Radial distribution of lead and lead isotopes in stem wood of Norway spruce: a reliable archive of pollution trends in Central Europe. Geochim. Cosmochim. Acta 74, 4207–4218 (2010).

  8. 8.

    Bollhöfer, A. & Rosman, K. J. R. Isotopic source signatures for atmospheric lead: the Northern Hemisphere. Geochim. Cosmochim. Acta 65, 1727–1740 (2001).

  9. 9.

    Simonetti, A., Clement, G. & Carignan, J. Tracing sources of atmospheric pollution in Western Canada using the Pb isotopic composition and heavy metal abundances of epiphytic lichens. Atmos. Environ. 37, 2853–2865 (2003).

  10. 10.

    Conti, M. E. & Tudino, M. B. Lichens as biomonitors of heavy-metal pollution. Compr. Anal. Chem. 73, 117–145 (2016).

  11. 11.

    Shiel, A. E., Weis, D. & Orians, K. J. Tracing cadmium, zinc and lead sources in bivalves from the coasts of western Canada and the USA using isotopes. Geochim. Cosmochim. Acta 76, 175–190 (2012).

  12. 12.

    Shiel, A. E., Weis, D., Cossa, D. & Orians, K. J. Determining provenance of marine metal pollution in French bivalves using Cd, Zn and Pb isotopes. Geochim. Cosmochim. Acta 121, 155–167 (2013).

  13. 13.

    Ruttner, F. Biogeography and Taxonomy of Honey Bees (Springer, 1988).

  14. 14.

    Bromenshenk, J. J., Carlson, S. R., Simpson, J. C. & Thomas, J. Pollution monitoring of Puget Sound with honey bees. Science 227, 632–634 (1985).

  15. 15.

    Jones, K. C. Honey as an indicator of heavy metal contamination. Water Air Soil Pollut. 33, 179–189 (1987).

  16. 16.

    Eckert, J. E. The flight range of the honeybee. J. Agric. Res. 47, 257–285 (1933).

  17. 17.

    Kalbande, D., Dhadse, S., Chaudhari, P. & Wate, S. Biomonitoring of heavy metals by pollen in urban environment. Environ. Monit. Assess. 138, 233–238 (2008).

  18. 18.

    Curie, C. et al. Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann. Bot. 103, 1–11 (2009).

  19. 19.

    Tong, S., Morse, R., Bache, C. & Lisk, D. Elemental analysis of honey as an indicator of pollution. Arch. Environ. Health 30, 329–332 (1975).

  20. 20.

    Celli, G. & Maccagnani, B. Honey bees as bioindicators of environmental pollution. Bull. Insectol. 56, 137–139 (2003).

  21. 21.

    Girolami, V. et al. Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication. J. Appl. Entomol. 136, 17–26 (2012).

  22. 22.

    Negri, I., Mavris, C., Di Prisco, G., Caprio, E. & Pellecchia, M. Honey bees (Apis mellifera, L.) as active samplers of airborne particulate matter. PLoS ONE 10, e0132491 (2015).

  23. 23.

    Solayman, M. et al. Physicochemical properties, minerals, trace elements, and heavy metals in honey of different origins: a comprehensive review. Compr. Rev. Food Sci. Food Saf. 15, 219–233 (2016).

  24. 24.

    Saunier, J. B., Losfeld, G., Freydier, R. & Grison, C. Trace elements biomonitoring in a historical mining district (Les Malines, France). Chemosphere 93, 2016–2023 (2013).

  25. 25.

    Silici, S., Uluozlu, O. D., Tuzen, M. & Soylak, M. Honeybees and honey as monitors for heavy metal contamination near thermal power plants in Mugla, Turkey. Toxicol. Ind. Health 32, 507–516 (2016).

  26. 26.

    Losfeld, G., Saunier, J. B. & Grison, C. Minor and trace-elements in apiary products from a historical mining district (Les Malines, France). Food Chem. 146, 455–459 (2014).

  27. 27.

    Álvarez-Ayuso, E. & Abad-Valle, P. Trace element levels in an area impacted by old mining operations and their relationship with beehive products. Sci. Total Environ. 599–600, 671–678 (2017).

  28. 28.

    Giglio, A. et al. Apis mellifera ligustica, Spinola 1806 as bioindicator for detecting environmental contamination: a preliminary study of heavy metal pollution in Trieste, Italy. Environ. Sci. Pollut. Res. 24, 659–665 (2017).

  29. 29.

    Zhou, X., Taylor, M. P., Davies, P. J. & Prasad, S. Identifying sources of environmental contamination in European honey bees (Apis mellifera) using trace elements and lead isotopic compositions. Environ. Sci. Technol. 52, 991–1001 (2018).

  30. 30.

    Di, N., Hladun, K. R., Zhang, K., Liu, T.-X. & Trumble, J. T. Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere 152, 530–538 (2016).

  31. 31.

    Dong, S. et al. Isotopic signatures suggest important contributions from recycled gasoline, road dust and non-exhaust traffic sources for copper, zinc and lead in PM10 in London, United Kingdom. Atmos. Environ. 165, 88–98 (2017).

  32. 32.

    Lambert, O. et al. Bees, honey and pollen as sentinels for lead environmental contamination. Environ. Pollut. 170, 254–259 (2012).

  33. 33.

    Mihaly Cozmuta, A., Bretan, L., Mihaly Cozmuta, L., Nicula, C. & Peter, A. Lead traceability along soil–melliferous flora–bee family–apiary products chain. J. Environ. Monit. 14, 1622–1630 (2012).

  34. 34.

    Zarić, N. M., Ilijević, K., Stanisavljević, L. & Gržetić, I. Use of honeybees (Apis mellifera L.) as bioindicators for assessment and source appointment of metal pollution. Environ. Sci. Pollut. Res. 24, 25828–25838 (2017).

  35. 35.

    Van Der Steen, J. J. M., De Kraker, J. & Grotenhuis, T. Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.). Environ. Monit. Assess. 184, 4119–4126 (2012).

  36. 36.

    Van der Steen, J. J. M., Cornelissen, B., Blacquière, T., Pijnenburg, J. E. M. L. & Severijnen, M. Think regionally, act locally: metals in honeybee workers in the Netherlands (surveillance study 2008). Environ. Monit. Assess. 188, 463 (2016).

  37. 37.

    Komárek, M., Ettler, V., Chrastný, V. & Mihaljevič, M. Lead isotopes in environmental sciences: a review. Environ. Int. 34, 562–577 (2008).

  38. 38.

    Preciado, H. F., Li, L. Y. & Weis, D. Investigation of past and present multi-metal input along two highways of British Columbia, Canada, using lead isotopic signatures. Water Air Soil Pollut. 184, 127–139 (2007).

  39. 39.

    Smith, K. E., Shafer, M. M., Weiss, D., Anderson, H. A. & Gorski, P. R. High-precision (MC-ICPMS) isotope ratio analysis reveals contrasting sources of elevated blood lead levels of an adult with retained bullet fragments, and of his child, in Milwaukee, Wisconsin. Biol. Trace Elem. Res. 177, 33–42 (2017).

  40. 40.

    Zhou, X., Taylor, M. P. & Davies, P. J. Tracing natural and industrial contamination and lead isotopic compositions in an Australian native bee species. Environ. Pollut. 242, 54–62 (2018).

  41. 41.

    Zarić, N. M. et al. Honeybees as sentinels of lead pollution: spatio-temporal variations and source appointment using stable isotopes and Kohonen self-organizing maps. Sci. Total Environ. 642, 56–62 (2018).

  42. 42.

    Leita, L., Muhlbachova, G., Cesco, S., Barbattini, R. & Mondini, C. Investigation of the use of honey bees and honey bee products to assess heavy metals contamination. Environ. Monit. Assess. 43, 1–9 (1996).

  43. 43.

    Fodor, P. & Molnar, E. Honey as an environmental indicator: effect of sample preparation on trace element determination by ICP-AES. Mikrochim. Acta 112, 113–118 (1993).

  44. 44.

    Perna, A., Intaglietta, I., Simonetti, A. & Gambacorta, E. Metals in honeys from different areas of Southern Italy. Bull. Environ. Contam. Toxicol. 92, 253–258 (2014).

  45. 45.

    Conti, M. E. & Botrè, F. Honeybees and their products as potential bioindicators of heavy metals contamination. Environ. Monit. Assess. 69, 267–282 (2001).

  46. 46.

    Birge, W. & Price, D. Analysis of Metals and Polychlorinated Biphenyl (PCB) Residues in Honeybees, Honey and Pollen Samples Collected from the Paducah Gaseous Diffusion Plant and Other Areas (2001); https://www.uky.edu/Research/Superfund/images/pdf/22%20PCB%20Metals%20in%20bees%20honey%20pollen%20030901%20Report.pdf.

  47. 47.

    Alvarez-Suarez, J. M. et al. Radical-scavenging activity, protective effect against lipid peroxidation and mineral contents of monofloral Cuban honeys. Plant Food Hum. Nutr. 67, 31–38 (2012).

  48. 48.

    Mondragón-Cortez, P., Ulloa, J. A., Rosas-Ulloa, P., Rodríguez-Rodríguez, R. & Resendiz Vázquezc, J. A. Physicochemical characterization of honey from the West region of México. CYTA J. Food 11, 7–13 (2013).

  49. 49.

    Gunawardana, C., Egodawatta, P. & Goonetilleke, A. Adsorption and mobility of metals in build-up on road surfaces. Chemosphere 119, 1391–1398 (2015).

  50. 50.

    Clarke, L. W., Jenerette, G. D. & Bain, D. J. Urban legacies and soil management affect the concentration and speciation of trace metals in Los Angeles community garden soils. Environ. Pollut. 197, 1–12 (2015).

  51. 51.

    Mcbride, M. B. et al. Concentrations of lead, cadmium and barium in urban garden-grown vegetables: the impact of soil variables. Environ. Pollut. 194, 254–261 (2014).

  52. 52.

    Mitchell, R. G. et al. Lead (Pb) and other metals in New York City community garden soils: factors influencing contaminant distributions. Environ. Pollut. 187, 162–169 (2014).

  53. 53.

    Zacháry, D., Jordan, G., Völgyesi, P., Bartha, A. & Szabó, C. Urban geochemical mapping for spatial risk assessment of multisource potentially toxic elements—a case study in the city of Ajka, Hungary. J. Geochem. Explor. 158, 186–200 (2015).

  54. 54.

    Trujillo-González, J. M., Torres-Mora, M. A., Keesstra, S., Brevik, E. C. & Jiménez-Ballesta, R. Heavy metal accumulation related to population density in road dust samples taken from urban sites under different land uses. Sci. Total Environ. 553, 636–642 (2016).

  55. 55.

    Rouillon, M., Harvey, P. J., Kristensen, L. J., George, S. G. & Taylor, M. P. VegeSafe: a community science program measuring soil-metal contamination, evaluating risk and providing advice for safe gardening. Environ. Pollut. 222, 557–566 (2017).

  56. 56.

    Muschack, W. Pollution of street run-off by traffic and local conditions. Sci. Total Environ. 93, 419–431 (1990).

  57. 57.

    Mangani, G., Berloni, A., Bellucci, F., Tatàno, F. & Maione, M. Evaluation of the pollutant content in road runoff first flush waters. Water Air Soil Pollut. 160, 213–228 (2005).

  58. 58.

    Huber, M., Welker, A. & Helmreich, B. Critical review of heavy metal pollution of traffic area runoff: occurrence, influencing factors, and partitioning. Sci. Total Environ. 541, 895–919 (2015).

  59. 59.

    Wang, Q. et al. Probing the severe haze pollution in three typical regions of China: characteristics, sources and regional impacts. Atmos. Environ. 120, 76–88 (2015).

  60. 60.

    Zhao, M. et al. Characteristics and ship traffic source identification of air pollutants in China’s largest port. Atmos. Environ. 64, 277–286 (2013).

  61. 61.

    La Pera, L. et al. Statistical study of the influence of fungicide treatments (mancozeb, zoxamide and copper oxychloride) on heavy metal concentrations in Sicilian red wine. Food Addit. Contam. 25, 302–313 (2008).

  62. 62.

    Rocha, G. H. O. et al. Exposure to heavy metals due to pesticide use by vineyard farmers. Int. Arch. Occup. Environ. Health 88, 875–880 (2015).

  63. 63.

    Chen, T. B., Wong, J. W. C., Zhou, H. Y. & Wong, M. H. Assessment of trace metal distribution and contamination in surface soils of Hong Kong. Environ. Pollut. 96, 61–68 (1997).

  64. 64.

    Szolnoki, Z., Farsang, A. & Puskás, I. Cumulative impacts of human activities on urban garden soils: origin and accumulation of metals. Environ. Pollut. 177, 106–115 (2013).

  65. 65.

    Pohl, P., Stecka, H., Greda, K. & Jamroz, P. Bioaccessibility of Ca, Cu, Fe, Mg, Mn and Zn from commercial bee honeys. Food Chem. 134, 392–396 (2012).

  66. 66.

    Carrington, C. D. & Bolger, P. M. An assessment of the hazards of lead in food. Regul. Toxicol. Pharmacol. 16, 265–272 (1992).

  67. 67.

    Goldhaber, S. B. Trace element risk assessment: essentiality vs. toxicity. Regul. Toxicol. Pharmacol. 38, 232–242 (2003).

  68. 68.

    Mullen, E. K. & Weis, D. Sr–Nd–Hf–Pb isotope and trace element evidence for the origin of alkalic basalts in the Garibaldi Belt, northern Cascade arc. Geochem. Geophys. Geosyst. 14, 3126–3155 (2013).

  69. 69.

    Carpentier, M., Weis, D. & Chauvel, C. Fractionation of Sr and Hf isotopes by mineral sorting in Cascadia Basin terrigenous sediments. Chem. Geol. 382, 67–82 (2014).

  70. 70.

    Sturges, W. & Barrie, L. Lead 206/207 isotope ratios in the atmosphere of North America as tracers of US and Canadian emissions. Nature 329, 144–146 (1987).

  71. 71.

    Laidlaw, M. A. S. & Filippelli, G. M. Resuspension of urban soils as a persistent source of lead poisoning in children: a review and new directions. Appl. Geochem. 23, 2021–2039 (2008).

  72. 72.

    Kurkjian, R. & Russell Flegal, A. Isotopic evidence of the persistent dominance of blood lead concentrations by previous gasoline lead emissions in Yerevan, Armenia. Environ. Res. 93, 308–315 (2003).

  73. 73.

    Snauffer, A., Menard, O., Kieffer, B., Francois, R. & Weis, D. In EOS Trans. Am. Geophys. Union Fall Meeting (2010).

  74. 74.

    Godwin, C. I. & Sinclair, A. J. Average lead isotope growth curves for shale-hosted zinc–lead deposits, Canadian cordillera. Econ. Geol. 77, 675–690 (1982).

  75. 75.

    Cheng, H. & Hu, Y. Lead (Pb) isotopic fingerprinting and its applications in lead pollution studies in China: a review. Environ. Pollut. 158, 1134–1146 (2010).

  76. 76.

    Sangster, D. F., Outridge, P. M. & Davis, W. J. Stable lead isotope characteristics of lead ore deposits of environmental significance. Environ. Rev. 8, 115–147 (2000).

  77. 77.

    Port of Vancouver Statistics Overview (Vancouver Fraser Port Authority, 2017).

  78. 78.

    Davis, B. & Birch, G. Comparison of heavy metal loads in stormwater runoff from major and minor urban roads using pollutant yield rating curves. Environ. Pollut. 158, 2541–2545 (2010).

  79. 79.

    Kaushal, S. S., McDowell, W. H. & Wollheim, W. M. Tracking evolution of urban biogeochemical cycles: past, present, and future. Biogeochemistry 121, 1–21 (2014).

  80. 80.

    Klein, A.-M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313 (2007).

  81. 81.

    Leonhardt, S. D., Gallai, N., Garibaldi, L. A., Kuhlmann, M. & Klein, A.-M. Economic gain, stability of pollination and bee diversity decrease from southern to northern Europe. Basic Appl. Ecol. 14, 461–471 (2013).

  82. 82.

    Makinson, J. C., Threlfall, C. G. & Latty, T. Bee-friendly community gardens: impact of environmental variables on the richness and abundance of exotic and native bees. Urban Ecosyst. 20, 463–476 (2017).

  83. 83.

    Tommasi, D., Miro, A., Higo, H. A. & Winston, M. L. Bee diversity and abundance in an urban setting. Can. Entomol. 136, 851–869 (2004).

  84. 84.

    2011 Census of Agriculture: British Columbia Highlights (British Columbia Ministry of Agriculture, 2011).

  85. 85.

    Metro Vancouver Regional Growth Strategy 2015 (Metro Vancouver, 2015).

  86. 86.

    Weis, D. et al. High-precision isotopic characterization of USGS reference materials by TIMS and MC-ICP-MS. Geochem. Geophys. Geosyst. 7, Q08006 (2006).

  87. 87.

    Fourny, A., Weis, D. & Scoates, J. S. Comprehensive Pb–Sr–Nd–Hf isotopic, trace element, and mineralogical characterization of mafic to ultramafic rock reference materials. Geochem. Geophys. Geosyst. 17, 739–773 (2016).

  88. 88.

    Shiel, A. E., Weis, D. & Orians, K. J. Evaluation of zinc, cadmium and lead isotope fractionation during smelting and refining. Sci. Total Environ. 408, 2357–2368 (2010).

  89. 89.

    Dixon, W. J. Analysis of extreme values. Ann. Math. Stat. 21, 488–506 (1950).

  90. 90.

    Dixon, W. J. Processing data for outliers. Biometrics 9, 74–89 (1953).

  91. 91.

    Fisher, R. A. Statistical Methods for Research Workers (Oliver and Boyd, 1954).

  92. 92.

    Driscoll, W. C. Robustness of the ANOVA and Tukey–Kramer statistical tests. Comput. Ind. Eng. 31, 265–268 (1996).

  93. 93.

    Anderson, K. A. & Smith, B. W. Use of chemical profiling to differentiate geographic growing origin of raw pistachios. J. Agric. Food Chem. 53, 410–418 (2005).

  94. 94.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).

  95. 95.

    Vancouver Historical Wind Direction (Environment Canada, accessed May 2018); https://weather.gc.ca/.

  96. 96.

    Zheng, J. et al. Characteristics of lead isotope ratios and elemental concentrations in PM10 fraction of airborne particulate matter in Shanghai after the phase-out of leaded gasoline. Atmos. Environ. 38, 1191–1200 (2004).

  97. 97.

    Mukai, H. et al. Regional characteristics of sulfur and lead isotope ratios in the atmosphere at several Chinese urban sites. Environ. Sci. Technol. 35, 1064–1071 (2001).

  98. 98.

    Mukai, H. et al. Characterization of sources of lead in the urban air of Asia using ratios of stable lead isotopes. Environ. Sci. Technol. 27, 1347–1356 (1993).

  99. 99.

    Wang, W. et al. Effectiveness of leaded petrol phase-out in Tianjin, China based on the aerosol lead concentration and isotope abundance ratio. Sci. Total Environ. 364, 175–187 (2006).

  100. 100.

    Hu, X. et al. Lead contamination and transfer in urban environmental compartments analyzed by lead levels and isotopic compositions. Environ. Pollut. 187, 42–48 (2014).

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Acknowledgements

Funding for this project was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant and Peter Wall Institute for Advanced Studies Solutions Award, both awarded to D.W. Additional support awarded to K.E.S. was provided by the Natural Sciences and Engineering Research Council of Canada’s Multidisciplinary Applied Geochemistry Network and via the University of British Columbia’s International Doctoral Fellowship. The authors thank J. Common, co-founder and chief beekeeper of Hives for Humanity of Vancouver, her team of apiary experts and her network of community volunteers, who provided honey samples, access to hives for direct sampling, and indispensable education and guidance for PCIGR scientists. The authors also thank the apiarists B. Finlay, E. Mitchell and A. Garr/K. Grecia for providing honey from Galiano Island, Bowen Island and the Vancouver Convention Centre rooftop, respectively.

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  1. Pacific Centre for Isotopic and Geochemical Research, Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia, Canada

    • Kate E. Smith
    • , Dominique Weis
    • , Marghaleray Amini
    • , Alyssa E. Shiel
    • , Vivian W.-M. Lai
    •  & Kathy Gordon
  2. College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, OR, USA

    • Alyssa E. Shiel

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Contributions

D.W. conceived the study and, along with V.W.-M.L., K.G. and M.A., developed the sample preparation and analytical methods for the first two years. K.E.S. managed the project, performed systematic field work across the GVRD, perfected the analytical techniques and analysed the data. K.E.S. and D.W. wrote the manuscript. A.E.S. performed the tree ring analyses. All authors commented on and provided edits to the manuscript.

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The authors declare no competing interests.

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Correspondence to Kate E. Smith.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–2, Supplementary Method Notes, Supplementary Discussion, Supplementary References 1–31

  2. Supplementary Tables

    Supplementary tables and figures containing chemical analysis results and statistical analyses

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