Skip to main content

Advertisement

Log in

A comparison of the antioxidant activities and biomonitoring of heavy metals by pollen in the urban environments

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

Abstract

Pollen is one of the most valuable nutrients due to its content and antioxidant activity. In this study, its botanic origin, total phenol content (TPC), total flavonoid content (TFC), the hydrogen peroxide scavenging activity (HPSA) (in terms of SC50), ferric reducing antioxidant power capacity (FRAP), 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity (in terms of SC50), metal-chelating activity (MCA) (%), and heavy metal content were examined to determine the quality of pollen that has been collected from seven different cities of Turkey. According to the melissopalynological analysis, the botanic origin of samples is six uni-flora and one multiflora. The TPC, TFC, HPSA, FRAP, DPPH, and MCA were found between 1360.70–2981.34 mg GAE/100 g, 74.23–111.74 mg CAE/100 g, 25.56–30.28 μg/mL, 71.92–73.86%, 52.26–53.27 μg/mL, and 43.97–65.21%, respectively. When obtained results compared to the standards (Butylated Hydroxy Anisole (BHA), Butylated Hydroxy Toluene (BHT) and α-Tocopherol (TOC)), pollen samples showed the effective antioxidant properties with respect to HPSA, FRAP, and DPPH radical scavenging activity. In addition, it was observed that honey samples were being contaminated with most of the metals to some extent (Al, Cr, Mn, Fe, Ni, Cu, Zn, B, As, Te, U), while some heavy metals (Co, Cd, V, Ga, and Ag) were never determined in all samples. However, Pb was determined only in sample 2 and sample 4, Mo in sample 1 and sample 2. According to meteorological parameters, samples 3, 4, and 5 were distinguished from the other samples. Finally, the data indicate that pollen could be affected by environmental pollutions.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Alaşalvar, C., Güder, A., Gökçe, H., Kaştaş, Ç. A., & Çelik, R. Ç. (2017). Theoretical, spectroscopic and antioxidant activity studies on (E)-2-[(2-fluorophenylimino)methyl]-4-hydroxyphenol and (E)-2-[(3-fluorophenylimino)methyl]-4-hydroxyphenol compounds. Journal of Molecular Structure, 1133, 37–48.

    Article  CAS  Google Scholar 

  • Almeida-Muradian, L. B., Pamplona, L. C., Coimbra, S., & Barth, O. M. (2005). Chemical composition and botanical evaluation of dried bee pollen pellets. Journal of Food Composition and Analysis, 18(1), 105–111.

    Article  CAS  Google Scholar 

  • Altunatmaz, S. S., Tarhan, D., Aksu, F., Barutçu, U. B., & Or, M. E. (2017). Mineral element and heavy metal (cadmium, lead and arsenic) levels of bee pollen in Turkey. Food Science and Technology, 37(1), 136–141.

    Article  Google Scholar 

  • Arslan, S., & Arıkan, A. (2013). Accumulation of heavy metals in bee products effect of distance from highway. Turkish Journal of Agriculture - Food Science and Technology, 1(2), 90–93.

    Article  Google Scholar 

  • Blois, M. S. (1958). Antioxidant determinations by the use of a stable free radical. Nature, 181, 1199–1200.

    Article  CAS  Google Scholar 

  • Bogdanov, S. (2006). Contaminants of bee products. Apidologie, 37(1), 1–18.

    Article  CAS  Google Scholar 

  • Carpes, S. T., Begnini, R., De Alencar, S. M., & Masson, M. L. (2007). Study of preparations of bee pollen extracts, antioxidant and antibacterial activity. Ciência e Agrotecnologia. Lavras, 31(6), 1818–1825.

    CAS  Google Scholar 

  • Çelemli, Ö. G., & Sorkun, K. (2012). The plant choices of honey bees to collect propolis in Tekirdag-Turkey. Hacettepe Journal of Biology and Chemistry, 40(1), 45–51.

    Google Scholar 

  • Chung, Y. C., Chang, C. T., Chao, W. W., Lin, C. F., & Chou, S. T. (2002). Antioxidative activity and safety of the 50% ethanolic extract from red bean fermented by Bacillus subtilis IMR–NK1. Journal of Agricultural and Food Chemistry, 50(8), 2454–2458.

    Article  CAS  Google Scholar 

  • Conti, M. E., & Botre, F. (2001). Honeybees and their products as potential bioindicators of heavy metals contamination. Environmental Monitoring and Assessment, 69(3), 267–282.

    Article  CAS  Google Scholar 

  • Cosmulescu, S., Trandafir, I., & Nour, V. (2015). Chemical composition and antioxidant activity of walnut pollen samples. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 43(2), 361–365.

    Article  CAS  Google Scholar 

  • Diaz-Losada, E., Ricciardelli-D’Albore, G., & Saa-Otero, M. P. (1998). The possible use of honeybee pollen loads in characterizing vegetation. Grana, 37(3), 155–163.

    Article  Google Scholar 

  • Dinis, T. C. P., Maderia, V. M. C., & Almeida, L. M. (1994). Action of phenolic derivates (acetoaminophen, salycilate, and 5-aminosalycilate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Archives of Biochemistry and Biophysics, 315(1), 161–169.

    Article  CAS  Google Scholar 

  • Dinkov, D., & Stratev, D. (2016). The content of two toxic heavy metals in Bulgarian bee pollen. International Food Research Journal, 23(3), 1343–1345.

    CAS  Google Scholar 

  • Erik, S. & Doğan, C. (2002) Allerjen Bitkiler, Editör: Metin Önerci, 2002. Allerjik Rinosinüzitler, Rekmay Ltd., Ankara, 257–338.

  • Fadzilah, N. H., Jaapar, M. F., Jajuli, R., & Omar, W. A. W. (2017). Total phenolic content, total flavonoid and antioxidant activity of ethanolic bee pollen extracts from three species of Malaysian stingless bee. Journal of Apicultural Research, 56(2), 130–135.

    Article  Google Scholar 

  • Feás, X., Tato, M. P. V., Estevinho, L., Seijas, J. A., & Iglesias, A. (2012). Organic bee pollen: botanical origin, nutritional value, bioactive compounds, antioxidant activity and microbiological quality. Molecules, 17(7), 8359–8377.

    Article  CAS  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 

  • Freire, K. R. L., Lins, A. C. S., Dórea, M. C., Santos, F. A. R., Camara, C. A., & Silva, T. M. S. (2012). Palynological origin, phenolic content, and antioxidant properties of honeybee-collected pollen from Bahia, Brazil. Molecules, 17(2), 1652–1664.

    Article  CAS  Google Scholar 

  • Gabriele, M., Parri, E., Felicioli, A., Sagona, S., Pozzo, L., Biondi, C., Domenici, V., & Pucci, L. (2015). Phytochemical composition and antioxidant activity of Tuscan bee pollen of different botanic origins. Italian Journal of Food Science, 27(2), 248–259.

    CAS  Google Scholar 

  • Gergen, I., Gogoaşǎ, I., Drǎgan, S., Moigrdean, D. & Hǎrmǎnescu, M. (2006). Heavy metal status in fruits and vegetables from a non-polluted area of Romania (Banat country), metal elements in environment, medicine and biology, Gârban Z., Drǎgan P. (Eds. Symp. Series), Tome VII, Publishing House Eurobit, Timişoara, 2006, 149–165.

  • Graikou, K., Kapeta, S., Aligiannis, N., Sotiroudis, G., Chondrogianni, N., Gonos, E., & Chinou, I. (2011). Chemical analysis of Greek pollen—antioxidant antimicrobial and proteasome activation properties. Chemistry Central Journal, 5(33), 1–9.

    Google Scholar 

  • Güder, A., & Korkmaz, H. (2012). Evaluation of in-vitro antioxidant properties of hydroalcoholic solution extracts Urtica dioica L., Malva neglecta Wallr and their mixture. Iranian Journal of Pharmaceutical Research, 11(3), 913–923.

    Google Scholar 

  • Güder, A., Korkmaz, H., Gökce, H., Alpaslan, Y. B., & Alpaslan, G. (2014). Isolation, characterization, spectroscopic properties and quantum chemical computations of an important phytoalexin resveratrol as antioxidant component from Vitis labrusca L. and their chemical compositions. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 133, 378–395.

    Article  CAS  Google Scholar 

  • Harmanescu, M., Bordean, D., & Gergen, I. (2007). Heavy metals contents of bee’s pollen from different locations of Romania. Lucrǎri Ştiintifice Medicinǎ Veterinarǎ, XL, 253–260.

    Google Scholar 

  • Ismail, A. H. M., Owayss, A. A., Mohanny, K. M., & Salem, R. A. (2013). Evaluation of pollen collected by honey bee, Apis mellifera L. colonies at Fayoum governorate, Egypt. Part 1: Botanical origin. Journal of the Saudi Society of Agricultural Sciences, 12(2), 129–135.

    Article  Google Scholar 

  • Kalbande, D. M., Dhadse, S. N., Chaudhari, P. R., & Wate, S. R. (2008). Biomonitoring of heavy metals by pollen in urban environment. Environmental Monitoring and Assessment, 138(1–3), 233–238.

    Article  CAS  Google Scholar 

  • Kaştaş, Ç. A., Kaştaş, G., Güder, A., Gür, M., Muğlu, H., & Büyükgüngör, O. (2017). Investigation of two o-hydroxy Schiff bases in terms of prototropy and radical scavenging activity. Journal of Molecular Structure, 1130, 623–632.

    Article  CAS  Google Scholar 

  • Kızılpınar, T. İ., Güder, A., & Gençay Çelemli, Ö. (2016). Botanic origin, various physicochemical and antioxidant properties of honey samples from Giresun, Turkey. Hacettepe Journal of Biology and Chemistry, 44(3), 209–215.

    Article  Google Scholar 

  • Kocaer, F. O., & Başkaya, H. S. (2003). Remediation technologies for metal-contaminated soil. Uludağ University Journal of the Faculty of Engineering, 8(1), 121–131.

    Google Scholar 

  • Louveaux, J., Maurizio, A., & Vorwohl, G. (1978). Methods of Melissopalynology. Bee World, 59, 139–157.

    Article  Google Scholar 

  • Madras-Majewska, B., & Jasinski, Z. (2003). Lead content of bees, brood and bee products from different regions of Poland. Journal of Apicultural Science, 47(2), 47–55.

    Google Scholar 

  • Madras-Majewska B., Jasinski Z., Zarski T. & Zarska H. (2002). The content of mercury in honeybee body and bee products originating from different region of Poland, 5th Int. Conf. On the black bee Apis mellifera mellifera, Wierzba, Poland, 2–6 September 2002, pp. 101–102.

  • Ojuederie, O. B., & Babalola, O. O. (2017). Microbial and plant-asisted bioremediation of heavy metal polluted environments: a review. International Journal of Environmental Research and Public Health, 14(12), 1–26.

    Article  Google Scholar 

  • Rebiai, A., & Lanez, T. (2012). Chemical composition and antioxidant activity of Apis mellifera bee pollen from Northwest Algeria. Journal of Fundamental and Applied Science, 4(2), 155–163.

    Article  Google Scholar 

  • Roman, A., Popiela-Pleban, E., Migdat, P., & Kruszynski, W. (2016). As, Cr, Cd, and bee product from a polish industrialized region. Open Chemistry, 14(1), 33–36.

    Article  CAS  Google Scholar 

  • Ruch, R. J., Cheng, S. J., & Klaunig, J. E. (1989). Prevention of cytotoxicity and inhibition of intracellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis, 10(6), 1003–1008.

    Article  CAS  Google Scholar 

  • Sabo, M., Potočnjak, M., Banjari, I., & Petrović, D. (2011). Pollen analysis of honeys from Varaždin County. Croatia. Turkish Journal of Botany, 35(5), 581–587.

    Google Scholar 

  • Serra Bonvehí, J. (1988). Plant origin of honeybee-collected pollen produced in Spain. Anales de la Asociación de Palinólogos de Lengua Española, 4, 73–78.

    Google Scholar 

  • Silva, T. M. S., Camara, C. A., Lins, A. C. S., Agra, M. d. F., Silva, E. M. S., Reis, I. T., & Freitas, B. M. (2009). Chemical composition, botanical evaluation and screening of radical scavenging activity of collected pollen by the stingless bees Melipona rufiventris (Uruçu-amarela). Anais Da Academia Brasileira de Ciencias, 81(2), 173–178.

    Article  CAS  Google Scholar 

  • Slinkard, K., & Singleton, V. L. (1977). Total phenol analyses: automation and comparison with manual methods. American Journal of Enology and Viticulture, 28, 49–55.

    CAS  Google Scholar 

  • Sorkun, K. (2000). Türkiye’nin nektarlı bitkileri ve polenleri. Ankara: Türkiye Kalkınma Vakfı yayını.

    Google Scholar 

  • Sorkun, K. (2008). Türkiye’nin nektarlı bitkileri polenleri ve balları (p. 352). Ankara: Palme Yayınları.

    Google Scholar 

  • Stojko, A. R., Stojko, J., Gorecka, A. K., Gorecki, M., Sobczak, A., Stojko, R., & Buszman, E. (2015). Polyphenol content and antioxidant activity of bee pollen extracts from Poland. Journal of Apicultural Research, 54(5), 482–490.

    Article  Google Scholar 

  • Temel, E., Alaşalvar, C., Gökçe, H., Güder, A., Albayrak, Ç., Alpaslan, Y. B., Alpaslan, G., & Dilek, N. (2015). DFT calculations, spectroscopy and antioxidant activity studies on (E)-2-nitro-4-[(phenylimino)methyl]phenol. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 136(B), 534–546.

    Article  CAS  Google Scholar 

  • Ulusoy, E., & Kolaylı, S. (2014). Phenolic composition and antioxidant properties of anzer bee pollen. Journal of Food Biochemistry, 38(1), 73–82.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Giresun University for providing the opportunity to research. The authors are grateful to Feyza Çolakoğlu from the University of Sidney for their kind help with the English language. The authors wish to extend our thanks to the English-editing-service of Turkey.

Funding

This work was financed by a scholarship of the Giresun University for support of Scientific/Technological Research (FEN-BAP-A-140316-80).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fulya Aydın Temel.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Temizer, İ.K., Güder, A., Temel, F.A. et al. A comparison of the antioxidant activities and biomonitoring of heavy metals by pollen in the urban environments. Environ Monit Assess 190, 462 (2018). https://doi.org/10.1007/s10661-018-6829-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-018-6829-6

Keywords