Main Article Content



POPs, PCDD/PCDFs, honeybees, bio-indicators, environment, health


Polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/PCDFs) are well-known persistent organic pollutants (POPs) with highly toxic potential. These compounds are released in the environment as a complex mixture of various congeners which shown significant physico-chemical differences, as well as different environmental fates. PCDD/PCDF mixtures change spatially and temporally in the environment and biota, complicating the risk assessment and regulatory control for human and animal exposure. Considering the well-known role of honeybees as bioindicators for pesticides, heavy metals and other chemicals, the present study has been developed to assess the use of honeybees and honeybee products in biomonitoring projects about PCDD/PCDFs.  Three Dadant-Blatt type beehives, located since March 2017 in the headquarter of Ducati Motor Holding S.p.A. (Borgo Panigale, Bologna, Italy) have been used as monitoring stations. Honeybees, honey and beeswax have been sampled and analyzed for PCDD/PCDFs detection in June and in September of the same year. Among the analyzed matrices, beeswax has shown the highest WHO-TEQ values, probably due to its lipidic nature capable of accumulating fat-soluble, non-volatile, persistent organic pollutants. Hexaclorodibenzo-p-dioxin (HxCDD), usually measured in vegetables and fruits, has been detected only in honey samples. Maximum levels of PCDD/PCDFs are settled by Commission Regulation (EC) No 1259/2011 of 2 December 2011, but only on animal-derived products. Considering the role of dietary-model adopted by the consumers on toxic substances dietary intake and associated exposure risks, limits on botanical derived products are needed. But more controls about bee-products are advisable also in order to reduce the exposure risk for bees and for protecting biodiversity.

Abstract 54 | pdf Downloads 41


Balayiannis G. and Balayiannis P. 2008. Bee honey as an environmental bioindicator of pesticides occurrence in six agricultural areas of Greece. Arch. Environ. Contam. Toxicol. 55:461-470.

Birnbauma L.S., Staskalb D.F. and DilibertoaJ.J. 2003. Health effects of polybrominated dibenzo-p-dioxins (PBDDs) and dibenzofurans (PBDFs). Environ. Int. 29(6):855-860.

Bocio A. and Domingo J.L. 2005. Daily intake of polychlorinated dibenzo-p-dioxins/polychlorinated dibenzofurans (PCDD/PCDFs) in foodstuffs consumed in Tarragona, Spain: a review of recent studies (2001-2003) on human PCDD/PCDF exposure through the diet. Environ. Res. 97:1-9.

Bogdanov S. 2006. Contaminants of bee products. Apidologie. 37, 1-18.

Bordajandi L.R., Gómez G., Abad E., Rivera J., Fernandez-Bastón M., Blasco J. and Gonzalez M.J. 2004. Survey of Persistent Organochlorine Contaminants (PCBs, PCDD/Fs, and PAHs), Heavy Metals (Cu, Cd, Zn, Pb, and Hg), and Arsenic in Food Samples From Huelva (Spain): Levels and Health Implication. J. Agric. Food Chem. 52:992-1001.

Bromenshenk J.J., Carlson S.R., Simpson J.C. and Thomas J.M. 1985. Pollution monitoring of Puget Sound with honeybees. Science. 227:532-634.

Celli G. and Maccagnani B. 2003. Honeybees as bioindicators of environmental pollution. Bull. Insectol. 56:137-139.

Chauzat M.P., Martel A.C., Cougoule N., Porta P., Lachaize J., Zeggane S., Aubert M., Carpentier P. and Faucon J.P. 2011. An Assessment of Honeybee Colony Matrices, Apis mellifera (Hymenoptera: Apidae) to Monitor Pesticides Presence in Continental France. Environ. Tox. 30(1):103-111.

Cohen M.D., Draxler R.R. and Artz R. 2002. Modeling the atmospheric transport and deposition of PCDD/F to the Great Lakes. Environ. Sci. Technol. 36:4831-4845

Commission Regulation (EC) No. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. 2006, Official Journal, L-364:5-24.

Commission Regulation (EU) No 589/2014 of 2 June 2014 laying down methods of sampling and analysis for the control of levels of dioxins, dioxin-like PCBs and non-dioxin-like PCBs in certain foodstuffs and repealing Regulation (EU) No 252/2012.2014, Official Journal, L-164:18-42.

Commission Regulation (EU) No. 1259/2011 of 2 December 2011 emending Regulation (EC) No 1881/2006 as regards maximum levels for dioxins, dioxin-like PCBs and non dioxin-like PCBs in foodstuffs. 2011, Official Journal, L-320:18-23.

Conti M.E. and Botrè F. 2001. Honeybees and Their Products as Potential Bioindicators of Heavy Metals Contamination. Environ. Monit. Asses. 69:267-282.

Crane E. 1984. Bee, honey and pollen as indicators of metals in the environment. Bee World. 65(1):47-49.

Domingo J.L., Schuhmacher M., Granero S. and Llobei J.M. 1999. PCDDs and PCDFs in food samples from Catalonia, Spain. An assessment of dietary intake. Chemosphere. 38:3517-3528.

EU-SCOOP European Commission, Scientific Co-operation on Questions Relating to Food. Assessment of dietary intake of dioxins and related PCBs by the population of EU Member States. Task 3.2.5, Brussels, Belgium, June 2000.

Focant J.-F., Eppe G., Pirard C., Massart A.-C., André J.-E. and De Pau E. 2002. Levels and congener distribution of PCDDs, PCDFs and non-ortho PCBs in Belgian foodstuff. Assessment of dietary intake. Chemosph. 48:167-179.

Franco M.A., Chessa M., Sferlazzo G., Giaccio M., Di Giacomo F. and Prota R. 1997. Bee pollen as an indicator of environmental pollution by haevy metals. Riv. Merceol. 36:67-78.

Franco M.A., Chessa M., Sferlazzo G., Giaccio M., Di Giacomo F., Prota R. and Manca G. 1998. Beeswax as an indicator of environmental pollution by haevy metals. Riv. Merceol. 37(1):3-11.

Hutzinger O., Choudhry G.G., Chittim B.G. and Johnston L.E. 1985. Formation of polychlorinated dibenzofurans and dioxins during combustion, electrical equipment fires and PCB incineration. Environ. Health Perspect. 60:3-9.

Johnson R.M., Ellis M.D., Mullin C.A. and Frazier M. 2010. Pesticides and honey bee toxicity -USA. Apidologie. 41:312-331.

Karl H., Ruoff U. and Blüthgen A. 2002. Levels of dioxins in fish and fishery products on the German market. Chemosph. 49:765-773.

Kirkham M.B. and Core J. C. 1977. Pollen as indicator of radionuclide pollution. J. Nucl. Agric. Biol. 3:71-74.

Leita L., Muhlbachova G., Cesco S., Barbattini R. and Mondini C. 1996. Investigation on the use of honeybees and honeybee products to assess haevy metals contamination. Environ. Monit. Assess. 43:1-9.

Lohmann R. and Jones C.K. 1998. Dioxins and furans in air and deposition: A review of levels, behaviour and processes. Sci. Total Environ. 219:53-81.

Meneses M., Schuhmacher M. and Domingo J.L. 2004. Health risk assessment of emissions of dioxins and furans from a municipal waste incinerator: comparison with other emission sources. Environ. Int. 30:481-489.

Mullin C.A., Frazier M., Frazier J.L., Ashcraft S., Simonds R., Van Engelsdorp D. and Pettis J.S. 2010. High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health. PLoS ONE. 5:e9754.

Özkök A., Sorkun K., Çakirogullari G.Ç., Yagli H., G., Aslan I., Bektas B. and Kiliç D. 2017. Dioxin analysis in pine honey from Turkey. Acta Biol. Szeged. 61(1):69-75.

Özkök A., Çakirogullari Sorkun K. G.Ç., Yagli H.,G., Aslan I., Bektas B. and Kiliç D. 2018. Dioxin Analysis of Bee Pollen Pellets Collected by Apis mellifera L. in Rural Area of Turkey. J. Api. Sci. 62(1):79-88.

Perugini M., Tulini S.M.R., Zezza D., Fenucci S., Conte A. and Amorena M. 2018. Occurrence of agrochemical residues in beeswax samples collected in Italy during 2013-2015. Sci. Total Environ. 625:470-476.

Porrini C., Caprio E., Tesoriero D. and Di Prisco G. 2014. Using honey bee as bioindicator of chemicals in Campanian agroecosystems (South Italy). Bull Insectol. 7(1):137-146.

Raes H., Cornelis R. and Rzeznik U. 1992. Distribution, accumulation and depuration of administered lead in adult honeybees. Sci. Total Environ. 113:269-279.

Ravoet J., Reybroeck W. and De Graaf D.C., 2015. Pesticides for Apicultural and/or Agricultural Application Found in Belgian Honey Bee Wax Combs. Environ. Contam. Tox. 94:543-548.

Schecter A., Päpke O., Harris T.R., Tung K.C., Musumba A., Olson J. and Birnbaum L. Polybrominated Diphenyl Ether (PBDE) Levels in an Expanded Market Basket Survey of U.S. Food and Estimated PBDE Dietary Intake by Age and Sex. Environ. Health Perspect. 114:1515-1520.

Schrenk D., Lipp H.P., Wiesmuller T., Hagenmaier H. and Bock K.W. 1991. Assessment of biological activities of mixtures of polychlorinated dibenzo-p-dioxins: Comparison between defined mixtures and their constituents. Arch. Toxicol. 65:114-118.

Serra-Bonvehí J. and Orantes-Bermejo J. 2010. Acaricides and their residues in Spanish commercial beeswax. Pest Manag. Sci. 66:1230-1235.

Simanainen U., Tuomisto J.T., Tuomisto J. and Viluksela M. 2002. Structure-activity relationships and dose responses of polychlorinated dibenzo-p-dioxins for short-term effects in 2,3,7,8-tetrachloro dibenzo-pdioxin-resistant and -sensitive rat strains.Toxicol. Appl. Pharmacol. 181:38-47.

Stöcker G. 1980. In Schubert, R., Schuh J. (Eds): Methodische and Theoretische Grundlagen der Bioindikation (Bioindikation 1). Martin-Luther-Universität; Halle (Saale), GDR, pp. 10-21.

Sweetman A.J., Alcock R.E., Wittsiepe J. and Jones K.C. 2000. Human exposure to PCDD/Fs in the UK: the development of a modelling approach to give historical and future perspective. Environ. Int. 26:37-47.

Tonelli D., Gattavecchia E., Ghini S., Porrini C., Celli G. and Mercuri A.M. 1990. Honey Bees and Their Products as Indicators of Environmental Radioactive Pollution. J Radioanal Nucl Ch. 141(2):427-436.

Tong S.S.C., Morse R.A., Bache C.A. and Lisk D.J. 1975. Elemental analysis of honey as an indicator of pollution. Arch. Environ. Health. 30:329-332.

Traag W.A., Kan C.A., Van der Weg G., Onstenk and C. Hoogenbooma L.A.P., 2006. Residues of dioxins (PCDD/Fs) and PCBs in eggs, fat and livers of laying hens following consumption of contaminated feed. Chem. 65(9):1518-1525.

Tulloch A.P.1980. Beeswax -composition and analysis. Bee World. 61:47-62.

Van den Berg M., Birnbauml L., Bosveld A.T.C., Brunstrdm B., Cook P., Feely M., GiesyJ.P., Hanberg A., Hasegawa R., Kennedy S.W., Kubiak T., Larsen J.C., van Leeuwen FX.R., Liem A.K.D., Nolt C., Peterson R.E., Poellinger L., Safe S., Schrenk D., Tillitt D., Tysklind M., Younes M., Warn F. and Zacharewsk T. 1998. Toxic Equivalency Factors (TEFs) for PCBs, PCDDs, PCDFs for Humans and Wildlife. Environ. Health Perspect. 106:775-791.

Van den Berg M., Birnbauml L., Denison M., De Vito M., Farland W., Feelev M., Fiedler H., Hakansson H., Hanberg A., Haws L., Rose M., Safe S., Schrenk D., Tohyama C., Tritscher A., Tuomisto J., Tysklind M., Walker N. and Peterson R.E. 2006. The 2005 World Health Organization Reevaluation of Human and Mammalian Toxic Equivalency Factors for Dioxins and Dioxin-Like Compounds. Toxicol. Sci. 93(2):223-241.

Van den Berg M., De Jongh J., Poiger H. and Olson J. R. 1994. The toxicokinetics and metabolism of polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) and their relevance for toxicity. Crit. Rev. Toxicol. 24:1-74.

Van den Berg M., Denison M., Birnbauml L., De Vito M., Fiedler H., Falandysz J., Rose M., Schrenk D., Safe S., Tohyama C., Tritscher A., Tysklind M. and Peterson R.E. 2013. Polybrominated Dibenzo-p-Dioxins, Dibenzofurans, and Biphenyls: inclusion in the Toxicity equivalency Factor Concept for Dioxin-Like Compounds. Toxicol. Sci. 133(2):197-208.

Wallwork-Barber M.K., Ferenbaugh R.W. and Glandney E.S. 1982. The use of honeybees as monitors of environmental pollution. Am. Bee J. 122:770-772.

Wegiel M., Chrzaszcz R., Maslanka and A. Grochowalski A. 2018. Seasonal variations of PCDD/Fs congeners in air, soil and eggs from a Polish small-scale farm. Chemosphere. 199:89-97.

Wu J.Y., Anelli C.M. and Sheppard W.S., 2011. Sublethal effects of pesticides residues in brood comb on worker honey bee (Apis mellifera) development and longevity. Plos One. 6:e14720.

Wu J.Y., Smart M.D., Anelli C.M. and Sheppard W.S. 2012. Honey bee (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J. Invertebr. Pathol. 109:326-329.

Zhelyazkova I. 2012. Honeybees -bioindicators for environmental quality. Bulg. J. Agric. Sci. 18:435-442.

Zheng G.J., Leung A.O.W., Jiao L.P. and Wong M.H. 2008. Polychlorinated dibenzo-p-dioxins and dibenzofurans pollution in China: Sources, environmental levels and potential human health impacts. Environ. Int. 34:1050-1061.