Honey as a biomonitor for a changing world

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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Fig. 1: Map of the GVRD, featuring locations of the beehives sampled for this study.
Fig. 2: Bivariate concentration plots of selected trace element concentrations versus Pb concentration for honey from the GVRD sampled in 2014–2017.
Fig. 3: Effect of radial distance from the Port of Vancouver on Pb and Cu concentrations and V/Ni ratios in honey.
Fig. 4: Lead isotopic compositions of all honey digests from this study.
Fig. 5: Lead isotopic composition of all analysed honey and tree rings from this study compared with local geological samples and anthropogenic sources.

Data availability

The data that support the findings of this study are available in the Supplementary Information files and from the corresponding author upon request.

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).

    Article  Google Scholar 

  4. 4.

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

    CAS  Article  Google Scholar 

  5. 5.

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

    Google Scholar 

  6. 6.

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

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  8. 8.

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

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  10. 10.

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

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  15. 15.

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

    CAS  Article  Google Scholar 

  16. 16.

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

    Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  20. 20.

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

    Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  32. 32.

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

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  37. 37.

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

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  49. 49.

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

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  56. 56.

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

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  66. 66.

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

    CAS  Article  Google Scholar 

  67. 67.

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

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  80. 80.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  89. 89.

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

    Article  Google Scholar 

  90. 90.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

  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).

    CAS  Article  Google Scholar 

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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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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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Correspondence to Kate E. Smith.

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

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Smith, K.E., Weis, D., Amini, M. et al. Honey as a biomonitor for a changing world. Nat Sustain 2, 223–232 (2019). https://doi.org/10.1038/s41893-019-0243-0

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