Skip to main content
SpringerLink
Log in

Honeybees (Apis mellifera) as a biological barrier for contamination of honey by environmental toxic metals

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The aim of the study was to investigate the transfer of toxic metals from honeybee workers (Apis mellifera L.) to bee honey in relation to the ecological state of the environment. The materials of the study consisted of samples of honeybee bodies and varietal honeys taken from the same apiary located in three areas: R1—urbanized (16), R2—ecologically clean (16) and R3—industrialized (15) of south-eastern Poland. The contents of 14 elements in all tested samples, including toxic metals (Cd, Pb, Hg, Al, Ni, Tl) as well as bioelements (K, Mg, Ca, Mn, Fe, Zn, Cu, Se), were analysed by the ICP-OES method with prior microwave mineralization. The concentrations of the majority of the studied elements, excluding aluminum and lead, were significantly higher in bee bodies than in honey samples (P < 0.05). The pollution of bee bodies by toxic metals was dependent on the environmental cleanliness, and the most pollution was observed in the industrialized area. The bee body was the most effective barrier for Cd and Tl transfer to the honey, while the level of Ni was similar in both tested materials. The Al concentration was significantly higher in honey than bee bodies (14.81 ± 24.69 and 6.51 ± 5.83 mg kg−1, respectively), which suggests the possibility of secondary contamination of honey. The greatest sensitivity to heavy metal pollution was observed in honeydew honey compared to nectar honeys (P < 0.05). It was proved for the first time that bees work as biofilters for toxic metals and prevent honey contamination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aghamirlou, H. M., Khadem, M., Rahmani, A., Sadeghian, M., Mahvi, A. H., Akbarzadeh, A., & Nazmara, S. (2015). Heavy metals determination in honey samples using inductively coupled plasma-optical emission spectrometry. Journal of Environmental Health Science and Engineering, 13(1), 39–47. https://doi.org/10.1186/s40201-015-0189-8

    Article  Google Scholar 

  • Al Naggar, Y. A., Naiem, E. A., Seif, A. I., & Mona, M. H. (2013). Honey bees and their products as a bio-indicator of environmental pollution with heavy metals. Mellifera, 13, 10–20.

    Google Scholar 

  • Bogdanov, S. (2006). Contaminants of bee products. Apidologie, 37(1), 1–18. https://doi.org/10.1051/apido:2005043

    Article  CAS  Google Scholar 

  • Bogdanov, S., Ryll, G., & Roth, H. (2003). Pesticide residues in honey and beeswax produced in Switzerland. Apidologie, 34, 484–485.

    Google Scholar 

  • Cempel, M., & Nikel, G. (2006). Nickel: a review of its sources and environmental toxicology. Polish Journal of Environmental Studies, 15, 375–382.

    CAS  Google Scholar 

  • Conti, M. E., & Botrè, F. (2001). Honeybees and their products as potential bioindicators of heavy metals contamination. Environmental Monitoring and Assessment, 69(3), 267–282. https://doi.org/10.1023/A:1010719107006

    Article  CAS  Google Scholar 

  • De Castro, C. S. P., Arruda, A. F., Da Cunha, L. R., SouzaDe, J. R., Braga, J. W. W., & Dórea, J. G. (2010). Toxic metals (Pb and Cd) and their respective antagonists (Ca and Zn) in infant formulas and milk marketed in Brasilia, Brazil. International Journal of Environmental Research and Public Health, 7(11), 4062–4077. https://doi.org/10.3390/ijerph7114062

    Article  Google Scholar 

  • Devillers, J. (2002). The ecological importance of honey bees and their relevance to ecotoxicology. In J. Devillers and M.-H. Pham-Delegue (Eds.), Honey bees: estimating the environmental impact of chemicals (pp. 1–11). CRC Press 2002. DOI: https://doi.org/10.1201/9780203218655.ch11

  • Dżugan, M., Zaguła, G., Wesołowska, M., Sowa, P., & Puchalski, C. (2017). Levels of toxic and essential metals in varietal honeys from Podkarpacie. Journal of Elementology, 22(3), 1039–1048. https://doi.org/10.5601/jelem.2016.21.4.1298

    Google Scholar 

  • Fakhimzadeh, K. (2000). Honey, pollen and bees as indicator of metal pollution. Acta Universitatis Carolinae Environmentalica, 14, 13–20.

    Google Scholar 

  • Formicki, G., Greń, A., Stawarz, R., Zyśk, B., & Gał, A. (2013). Metal content in honey, propolis, wax, and bee pollen and implications for metal pollution monitoring. Polish Journal of Environmental Studies, 22(1), 99–106.

    CAS  Google Scholar 

  • Garzone, V., D’Alessandro, C., Mininni, R., Addante, R. & Terzano, R. (2002). Bees as bioindicators of environmental metal pollution nearby a large industrial site in Apulia Region. In J. Devillers and M.-H. Pham-Delegue (Eds.), Honey Bees: Estimating the Environmental Impact of Chemicals (pp. 186–247). CRC Press 2002. DOI: https://doi.org/10.1201/9780203218655.ch11

  • Girotti, S., Maiolini, E., Bolelli, L., Ghini, S., Ferri, E., Barile, N. & Medvedeva, S. (2008). Analytical techniques and bioindicators in environmental control: honeybees, mussels, bioluminescent bacteria: rapid immunoassays for pesticide detection. In: Simeonov L. and Sargsyan V. (Eds.), Soil Chemical Pollution, Risk Assessment, Remediation and Security (pp. 327–347). Springer Science+Business Media B.V. 2008.

  • Gliga, O. (2016). The content of heavy metals in the bees body depending on location area of hives. Scientific Papers-Animal Science Series: Lucrări Ştiinţifice - Seria Zootehnie, 65, 169–175.

    Google Scholar 

  • Gutiérrez, M., Molero, R., Gaju, M., van der Steen, J., Porrini, C., & Ruiz, J. A. (2015). Assessment of heavy metal pollution in Córdoba (Spain) by biomonitoring foraging honeybee. Environmental Monitoring and Assessment, 187(10), 651. https://doi.org/10.1007/s10661-015-4877-8

    Article  Google Scholar 

  • Kacaniova, M., Knazovicka, V., Melich, M., Fikselova, M., Massanyi, P., Stawarz, R., Hascik, P., Pechociak, T., Kuczkowska, A., & Putała, A. (2009). Environmental concentration of selected elements and relation to physicochemical parameters in honey. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 44(4), 414–422. https://doi.org/10.1080/10934520802659802

    Article  CAS  Google Scholar 

  • Komarnicki, G. J. K. (2005). Lead and cadmium in indoor air and the urban environment. Environmental Pollution, 136(1), 47–61. https://doi.org/10.1016/j.envpol.2004.12.006

    Article  CAS  Google Scholar 

  • Kotaś, J., & Stasicka, Z. (2000). Chromium occurrence in the environment and methods of its speciation. Environmental Pollution, 107(3), 263–283. https://doi.org/10.1016/S0269-7491(99)00168-2

    Article  Google Scholar 

  • Leita, L., Muhlbachova, G., Cesco, S., Barbattini, R., & Mondini, C. (1996). Investigation of the use of honey bees and honey bee products to assess heavy metals contamination. Environmental Monitoring and Assessment, 43(1), 1–9. https://doi.org/10.1007/BF00399566

    Article  CAS  Google Scholar 

  • Linden, A., Olsson, M., Bensryd, I., Lundh, T., Skerfving, S., & Oskarssona, A. (2003). Monitoring of cadmium in the chain from soil via crops and feed to pig blood and kidney. Ecotoxicology and Environmental Safety, 55(2), 213–222. https://doi.org/10.1016/S0147-6513(02)00079-9

    Article  CAS  Google Scholar 

  • Madejczyk, M., & Baralkiewicz, D. (2008). Characterization of Polish rape and honeydew honey according to their mineral contents using ICP-MS and F-AAS/AES. Analytica Chimica Acta, 617(1-2), 11–17. https://doi.org/10.1016/j.aca.2008.01.038

    Article  CAS  Google Scholar 

  • Naggar, Y. A., Naiem, S. A., Seif, A. I., & Mona, M. H. (2013). Honey bees and their products as a bio-indicator of environmental pollution with heavy metals. Mellifera, 13-26, 10–20.

    Google Scholar 

  • Porrini, C., Sabatini, A. G., Girotti, S., Ghini, S., Medrzycki, P., Grillenzoni, F., Bortolotti, L., Gattavecchia, E., & Celli, G. (2003). Honeybees and bee products as monitors of the environmental contamination. Apiacta, 38, 63–70.

    Google Scholar 

  • Reszel, R., Reszel, H., Pęcak J. & Hadam, B. (2003). The content of sulfur and heavy metals in soils of agricultural land and plants of protected areas of the Podkarpackie Voivodship. In: J. A. Tomaszek (Ed.), Postęp w inżynierii środowiska, Oficyna Wydawnicza Politechniki Rzeszowskiej, Rzeszów 2003, pp. 435–445. (in Polish).

  • Roman, A. (2010). Levels of copper, selenium, lead, and cadmium in forager bees. Polish Journal of Environmental Studies, 19(3), 663–669.

    CAS  Google Scholar 

  • Roman, A., Madras-Majewska, B., & Popiela-Pleban, E. (2011). Comparative study of selected toxic elements in propolis and honey. Journal of Apicultural Science, 55(2), 97–106.

    Google Scholar 

  • Ruschioni, S., Riolo, P., Minuz, R. L., Stefano, M., Cannella, M., Porrini, C., & Isidoro, N. (2013). Biomonitoring with honeybees of heavy metals and pesticides in nature reserves of the Marche Region (Italy). Biological Trace Element Research Journal, 154(2), 226–233. https://doi.org/10.1007/s12011-013-9732-6

    Article  CAS  Google Scholar 

  • Tanakaa, M., Yamaguchia, Y., Haradaa, Y., Tsuchiyaa, K., & Takakub, Y. (2017). As, Cd and Hg in the organs of Todarodes pacificus, Sepia longipes and Sepia madokai in the East China Sea. Ecotoxicology and Environmental Safety, 145, 103–110. https://doi.org/10.1016/j.ecoenv.2017.06.054

    Article  Google Scholar 

  • Wajdzik, M., Halecki, W., Kalarus, K., Gąsiorek, M., & Pająk, M. (2017). Relationship between heavy metal accumulation and morphometric parameters in European hare (Lepus europaeus) inhabiting various types of landscapes in southern Poland. Ecotoxicology and Environmental Safety, 145, 16–23. https://doi.org/10.1016/j.ecoenv.2017.06.070

    Article  CAS  Google Scholar 

  • Wesołowska, M., Miąsik, B., Sowa, P., Zaguła, G., & Dżugan, M. (2017). The possibility of secondary contamination of honey during storage in aluminium cans. In M. Dżugan, A. Pasternakiewicz, & M. Wesołowska (Eds.), Environmental influence on the food quality and human health (Vol. 2016, pp. 136–144). Rzeszów: Wydawnictwo Uniwersytetu Rzeszowskiego ISBN 978-83-7996-409-3.

    Google Scholar 

  • Zhelyazkova, I. (2012). Honeybees—bioindicators for environmental quality. Bulgarian Journal of Agricultural Science, 18(3), 435–442.

    Google Scholar 

Download references

Funding

This work was supported financially by the Marshal’s Department of Podkarpackie Voivodeship, project No RPPK.01.03.00-18-040/13, funded by UE.

Author information

Authors and Affiliations

  1. Department of Chemistry and Food Toxicology, University of Rzeszow, Ćwiklińskiej 1a St., 35-601, Rzeszów, Poland

    Małgorzata Dżugan & Monika Wesołowska

  2. Faculty of Biotechnology and Food Sciences, Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 949 76, Nitra, Slovakia

    Monika Wesołowska

  3. Department of Bioenergy Technology and Food Analysis, University of Rzeszów, Zelwerowicza 4 St., 35-601, Rzeszów, Poland

    Grzegorz Zaguła, Maria Czernicka & Czesław Puchalski

  4. Department of Agriculture, The Jan Grodek State Vocational Academy in Sanok, Mickiewicza 21 St., 38-500, Sanok, Poland

    Mateusz Kaczmarski

Authors
  1. Małgorzata Dżugan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika Wesołowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Grzegorz Zaguła
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mateusz Kaczmarski
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Czernicka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Czesław Puchalski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Małgorzata Dżugan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dżugan, M., Wesołowska, M., Zaguła, G. et al. Honeybees (Apis mellifera) as a biological barrier for contamination of honey by environmental toxic metals. Environ Monit Assess 190, 101 (2018). https://doi.org/10.1007/s10661-018-6474-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-018-6474-0

Keywords

Search

Navigation