Abstract
In recent years, honeybees and bee products such as pollen and honey have been used as bioindicators for monitoring environmental pollution. Unfortunately, there are few studies about polychlorinated biphenyl (PCB) concentrations in honeybees and bee products from Turkey. Honeybee and pollen samples were taken between May and September 2017, and honey samples were taken between July and September 2017 at urban and semi-urban areas in Bursa (Turkey). PCB concentrations measured by gas chromatography-microelectron capture detector (GC-μECD) were found to be 135.46 ± 6.53, 81.47 ± 23.52, and 106.35 ± 21.60 ng g−1 dry weight (dw) for honeybee, pollen, and honey samples in the urban area, respectively; and 126.35 ± 26.54, 67.57 ± 27.34, and 118.88 ± 55.28 ng g−1 dw for honeybee, pollen, and honey samples in the semi-urban area, respectively. Pearson correlation was made between meteorological parameters and pollutant concentrations. According to the correlation results, a significant relationship was found between the pollen and honey results and the total cloudiness and temperature in the semi-urban area. The coefficient of divergence (COD) and Pearson correlation coefficient (PCC) methods were applied to determine the similarities and differences between the pollutant concentrations and sources of the two areas and the temporal variation. According to these two methods, PCB concentrations and emission sources in honeybee and pollen samples in urban and semi-urban areas were generally different in May and June, and similar in August and September.
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Abella V, Pérez T, Scotece M, Conde J, Pirozzi C, Pino J, Lago F, González-Gay MÁ, Mera A, Gómez R, Gualillo O (2016) Pollutants make rheumatic diseases worse: facts on polychlorinated biphenyls (PCBs) exposure and rheumatic diseases. Life Sci 157:140–144. https://doi.org/10.1016/j.lfs.2016.06.010
Al-Waili N, Salom K, Al-Ghamdi A, Ansari MJ (2012, 2012) Antibiotic, pesticide, and microbial contaminants of honey: human health hazards. Sci World J. https://doi.org/10.1100/2012/930849
Amores-Arrocha A, Roldán A, Jiménez-Cantizano A, Caro I, Palacios V (2018) Evaluation of the use of multiflora bee pollen on the volatile compounds and sensorial profile of Palomino fino and Riesling white young wines. Food Res Int 105:197–209. https://doi.org/10.1016/j.foodres.2017.11.013
Ares AM, Valverde S, Bernal JL, Nozal MJ, Bernal J (2018) Extraction and determination of bioactive compounds from bee pollen. J Pharm Biomed Anal 147:110–124. https://doi.org/10.1016/j.jpba.2017.08.009
Badolato M, Carullo G, Cione E, Aiello F, Caroleo MC (2017) From the hive: honey, a novel weapon against cancer. Eur J Med Chem 142:290–299. https://doi.org/10.1016/j.ejmech.2017.07.064
Bahrami Asl F, Leili M, Vaziri Y, Salahshour Arian S, Cristaldi A, Oliveri Conti G, Ferrante M (2018) Health impacts quantification of ambient air pollutants using AirQ model approach in Hamadan, Iran. Environ Res 161:114–121. https://doi.org/10.1016/j.envres.2017.10.050
Bano S, Pervez S, Chow JC, Matawle JL, Watson JG, Sahu RK, Srivastava A, Tiwari S, Pervez YF, Deb MK (2018) Coarse particle (PM10–2.5) source profiles for emissions from domestic cooking and industrial process in Central India. Sci Total Environ 627:1137–1145. https://doi.org/10.1016/j.scitotenv.2018.01.289
Barbas B, de la Torre A, Sanz P, Navarro I, Artíñano B, Martínez MA (2018) Gas/particle partitioning and particle size distribution of PCDD/Fs and PCBs in urban ambient air. Sci Total Environ 624:170–179. https://doi.org/10.1016/j.scitotenv.2017.12.114
Benuszak J, Laurent M, Chauzat MP (2017) The exposure of honey bees (Apis mellifera; Hymenoptera: Apidae) to pesticides: room for improvement in research. Sci Total Environ 587–588:423–438. https://doi.org/10.1016/j.scitotenv.2017.02.062
Bogdanov S (2006) Contaminants of bee product. Apidologie 37:1–18. https://doi.org/10.1051/apido
Bromenshenk et al (1991) Le rappor t à l’eau et à la terre dans la construction de territoires multisitués : le cas palestinien. Espac Geogr 22:359–369. https://doi.org/10.1051/apido
Chiesa LM, Labella GF, Giorgi A, Panseri S, Pavlovic R, Bonacci S, Arioli F (2016) The occurrence of pesticides and persistent organic pollutants in Italian organic honeys from different productive areas in relation to potential environmental pollution. Chemosphere 154:482–490. https://doi.org/10.1016/j.chemosphere.2016.04.004
Chuang H-C, Sun J, Ni H, Tian J, Lui KH, Han Y, Cao J, Huang R-J, Shen Z, Ho K-F (2019) Characterization of the chemical components and bioreactivity of fine particulate matter produced during crop-residue burning in China. Environ Pollut 245:226–234. https://doi.org/10.1016/j.envpol.2018.10.119
Cindoruk SS, Esen F, Tasdemir Y (2007) Concentration and gas/particle partitioning of polychlorinated biphenyls (PCBs) at an industrial site at Bursa, Turkey. Atmos Res 85:338–350. https://doi.org/10.1016/j.atmosres.2007.02.004
Da Silva PM, Gauche C, Gonzaga LV, Costa ACO, Fett R (2016) Honey: chemical composition, stability and authenticity. Food Chem 196:309–323. https://doi.org/10.1016/j.foodchem.2015.09.051
David A, Botías C, Abdul-Sada A, Nicholls E, Rotheray EL, Hill EM, Goulson D (2016) Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ Int 88:169–178. https://doi.org/10.1016/j.envint.2015.12.011
de Oliveira RC, Queiroz SC d N, da Luz CFP, Porto RS, Rath S (2016) Bee pollen as a bioindicator of environmental pesticide contamination. Chemosphere 163:525–534. https://doi.org/10.1016/j.chemosphere.2016.08.022
Di Bella G, Lo Turco V, Potortì AG, Bua GD, Fede MR, Dugo G (2015) Geographical discrimination of Italian honey by multi-element analysis with a chemometric approach. J Food Compos Anal 44:25–35. https://doi.org/10.1016/j.jfca.2015.05.003
Drummond J, Williamson SM, Fitchett AE, Wright GA, Judge SJ (2017) Spontaneous honeybee behaviour is altered by persistent organic pollutants. Ecotoxicology 26:141–150. https://doi.org/10.1007/s10646-016-1749-0
Erdogrul O (2007) Levels of selected pesticides in honey samples from Kahramanmaraş, Turkey. Food Control 18:866–871. https://doi.org/10.1016/j.foodcont.2006.05.001
Esen F, Kayikci G (2018) Polycyclic aromatic hydrocarbons in indoor and outdoor air in Turkey: estimations of sources and exposure, environ. Forensics 19(1):39–49. https://doi.org/10.1080/15275922.2017.1408162
Esen F, Tasdemir Y, Vardar N (2008) Atmospheric concentrations of PAHs, their possible sources and gas-to-particle partitioning at a residential site of Bursa, Turkey. Atmos Res 88:243–255. https://doi.org/10.1016/j.atmosres.2007.11.022
Esen F, Tasdemir Y, Cindoruk SS (2010) Dry deposition, concentration and gas/particle partitioning of atmospheric carbazole. Atmos Res 95:379–385. https://doi.org/10.1016/j.atmosres.2009.10.010
Günindi M, Tasdemir Y (2010) Atmospheric polychlorinated biphenyl (pcb) inputs to a coastal city near the marmara sea. Mar Pollut Bull 60:2242–2250. https://doi.org/10.1016/j.marpolbul.2010.08.012
Hakme E, Lozano A, Gómez-Ramos MM, Hernando MD, Fernández-Alba AR (2017) Non-target evaluation of contaminants in honey bees and pollen samples by gas chromatography time-of-flight mass spectrometry. Chemosphere 184:1310–1319. https://doi.org/10.1016/j.chemosphere.2017.06.089
Harrad S, Mao H (2004) Atmospheric PCBs and organochlorine pesticides in Birmingham, UK: concentrations, sources, temporal and seasonal trends. Atmos Environ 38:1437–1445. https://doi.org/10.1016/j.atmosenv.2003.12.002
Hogarh JN, Seike N, Kobara Y, Masunaga S (2013) Seasonal variation of atmospheric polychlorinated biphenyls and polychlorinated naphthalenes in Japan. Atmos Environ 80:275–280. https://doi.org/10.1016/j.atmosenv.2013.07.076
Huang RJ, Zhang Y, Bozzetti C, Ho KF, Cao JJ, Han Y, Daellenbach KR, Slowik JG, Platt SM, Canonaco F, Zotter P, Wolf R, Pieber SM, Bruns EA, Crippa M, Ciarelli G, Piazzalunga A, Schwikowski M, Abbaszade G, Schnelle-Kreis J, Zimmermann R, An Z, Szidat S, Baltensperger U, El Haddad I, Prévôt ASH (2014) High secondary aerosol contribution to particulate pollution during haze events in China. Nature 514:218–222. https://doi.org/10.1038/nature13774
Human H, Nicolson SW (2006) Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry 67:1486–1492. https://doi.org/10.1016/j.phytochem.2006.05.023
Jankovic S, Djinovic-Stojanovic J, Stefanovic S, Radicevic T, Curcic M, Nikolic D, Spiric D (2015) ScienceDirect non-dioxin like polychlorinated biphenyls in mackerel (Scomber scombrus) available on the Serbian market. Procedia Food Sci 5:113–116. https://doi.org/10.1016/j.profoo.2015.09.031
Kargar N, Matin G, Matin AA, Buyukisik HB (2017) Biomonitoring, status and source risk assessment of polycyclic aromatic hydrocarbons (PAHs) using honeybees, pine tree leaves, and propolis. Chemosphere 186:140–150. https://doi.org/10.1016/j.chemosphere.2017.07.127
Kasper ML, Reeson AF, MacKay DA, Austin AD (2008) Environmental factors influencing daily foraging activity of Vespula germanica (Hymenoptera, Vespidae) in Mediterranean Australia. Insect Soc 55:288–295. https://doi.org/10.1007/s00040-008-1004-7
Kim KS, Masunaga S (2005) Behavior and source characteristic of PCBS in urban ambient air of Yokohama, Japan. Environ Pollut 138:290–298. https://doi.org/10.1016/j.envpol.2005.03.011
Lambert O, Veyrand B, Durand S, Marchand P, Le Bizec B, Piroux M, Puyo S, Thorin C, Delbac F, Pouliquen H (2012) Polycyclic aromatic hydrocarbons: bees, honey and pollen as sentinels for environmental chemical contaminants. Chemosphere 86:98–104. https://doi.org/10.1016/j.chemosphere.2011.09.025
Li H, Wang D, Cui L, Gao Y, Huo J, Wang X, Zhang Z, Tan Y, Huang Y, Cao J, Chow JC, Lee S c, Fu Q (2019) Characteristics of atmospheric PM2.5 composition during the implementation of stringent pollution control measures in shanghai for the 2016 G20 summit. Sci Total Environ 648:1121–1129. https://doi.org/10.1016/j.scitotenv.2018.08.219
Liu Y, Yan C, Ding X, Wang X, Fu Q, Zhao Q, Zhang Y, Duan Y, Qiu X, Zheng M (2017) Sources and spatial distribution of particulate polycyclic aromatic hydrocarbons in Shanghai, China. Sci Total Environ 584–585:307–317. https://doi.org/10.1016/j.scitotenv.2016.12.134
Lo Turco V, Di Bella G, Potortì AG, Tropea A, Casale EK, Fede MR, Dugo G (2016) Determination of plasticisers and BPA in Sicilian and Calabrian nectar honeys by selected ion monitoring GC/MS. Food Addit Contam - Part A Chem Anal Control Expo Risk Assess 33:1693–1699. https://doi.org/10.1080/19440049.2016.1239030
Lorga G, Balaceanu Raicu C, Stefan S (2015) Annual air pollution level of major primary pollutants in Greater Area of Bucharest. Atmos Pollut Res 6:824–834. https://doi.org/10.5094/APR.2015.091
Moret S, Purcaro G, Conte LS (2010) Polycyclic aromatic hydrocarbons (PAHs) levels in propolis and propolis-based dietary supplements from the Italian market. Food Chem 122:333–338. https://doi.org/10.1016/j.foodchem.2010.02.041
Nisbet C, Guler A, Yarim GF, Cenesiz S, Ardali Y (2013) Relationship between environmental and flora change with mineral content of honey bee products. Turkish J Biochem 38:494–498. https://doi.org/10.5505/tjb.2013.07269
Odabasi M, Ozgunerge Falay E, Tuna G, Altiok H, Kara M, Dumanoglu Y, Bayram A, Tolunay D, Elbir T (2015) Biomonitoring the spatial and historical variations of persistent organic pollutants (POPs) in an industrial region. Environ Sci Technol 49:2105–2114. https://doi.org/10.1021/es506316t
Orecchio S (2011) Polycyclic aromatic hydrocarbons (PAHs) in indoor emission from decorative candles. Atmos Environ 45:1888–1895. https://doi.org/10.1016/j.atmosenv.2010.12.024
Ozgunerge Falay E, Tuna G, Altiok H, Kara M, Dumanoglu Y, Bayram A, Tolunay D, Elbir T, Odabasi M (2013) Spatial variation of polycyclic aromatic hydrocarbons (PAHs) in air , soil and tree components in Iskenderun Industrial Region, Turkey. Int J Chem Environ Biol Sci 1:263–267
Putschögl FM, Gaum PM, Schettgen T, Kraus T, Gube M, Lang J (2015) Effects of occupational exposure to polychlorinated biphenyls on urinary metabolites of neurotransmitters: a cross-sectional and longitudinal perspective. Int J Hyg Environ Health 218:452–460. https://doi.org/10.1016/j.ijheh.2015.03.009
Rissato SR, Galhiane MS, de Almeida MV, Gerenutti M, Apon BM (2007) Multiresidue determination of pesticides in honey samples by gas chromatography-mass spectrometry and application in environmental contamination. Food Chem 101:1719–1726. https://doi.org/10.1016/j.foodchem.2005.10.034
Roszko MŁ, Kamińska M, Szymczyk K, Jȩdrzejczak R (2016) Levels of selected persistent organic pollutants (PCB, PBDE) and pesticides in honey bee pollen sampled in Poland. PLoS One 11:1–22. https://doi.org/10.1371/journal.pone.0167487
Saitta M, Di Bella G, Fede MR, Lo Turco V, Potortì AG, Rando R, Russo MT, Dugo G (2017) Gas chromatography-tandem mass spectrometry multi-residual analysis of contaminants in Italian honey samples. Food Addit Contam - Part A Chem Anal Control Expo Risk Assess 34:800–808. https://doi.org/10.1080/19440049.2017.1292054
Sanchez-Bayo F, Goka K (2016) Impacts of pesticides on honey bees. Beekeeping and Bee Conservation-Advances in Research, Chapter 4. https://doi.org/10.5772/62487
Shaban YA, El Sayed MA, El Maradny AA, Al Farawati RK, Al Zobidi MI, Khan SUM (2016, 2016) Laboratory and pilot-plant scale photocatalytic degradation of polychlorinated biphenyls in seawater using CM-n-TiO2 nanoparticles. Int J Photoenergy. https://doi.org/10.1155/2016/8471960
Sun J, Shen Z, Zhang L, Lei Y, Gong X, Zhang Q, Zhang T, Xu H, Cui S, Wang Q, Cao J, Tao J, Zhang N, Zhang R (2019) Chemical source profiles of urban fugitive dust PM2.5samples from 21 cities across China. Sci Total Environ 649:1045–1053. https://doi.org/10.1016/j.scitotenv.2018.08.374
Switanek M, Crailsheim K, Truhetz H, Brodschneider R (2017) Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate. Sci Total Environ 579:1581–1587. https://doi.org/10.1016/j.scitotenv.2016.11.178
Tasdemir Y, Esen F (2007) Urban air PAHs: concentrations, temporal changes and gas/particle partitioning at a traffic site in Turkey. Atmos Res 84:1–12. https://doi.org/10.1016/j.atmosres.2006.04.003
Tasdemir Y, Odabasi M, Holsen TM (2005) Measurement of the vapor phase deposition of polychlorinated bipheyls (PCBs) using a water surface sampler. Atmos Environ 39:885–897. https://doi.org/10.1016/j.atmosenv.2004.10.032
Tavera Busso I, Tames F, Silva JA, Ramos S, Homem V, Ratola N, Carreras H (2018) Biomonitoring levels and trends of PAHs and synthetic musks associated with land use in urban environments. Sci Total Environ 618:93–100. https://doi.org/10.1016/j.scitotenv.2017.10.295
Yadav V, Turner J (2014) Gauging intraurban variability of ambient particulate matter arsenic and other air toxic metals from a network of monitoring sites. Atmos Environ 89:318–328. https://doi.org/10.1016/j.atmosenv.2014.02.030
Zani C, Ceretti E, Covolo L, Donato F (2017) Do polychlorinated biphenyls cause cancer? A systematic review and meta-analysis of epidemiological studies on risk of cutaneous melanoma and non-Hodgkin lymphoma. Chemosphere 183:97–106. https://doi.org/10.1016/j.chemosphere.2017.05.053
Ziegler S, Schettgen T, Beier F, Wilop S, Quinete N, Esser A, Masouleh BK, Ferreira MSV, Vankann L, Uciechowski P, Rink L, Kraus T, Brümmendorf TH, Ziegler P (2017) Accelerated telomere shortening in peripheral blood lymphocytes after occupational polychlorinated biphenyls exposure. Arch Toxicol 91:289–300. https://doi.org/10.1007/s00204-016-1725-8
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We would like to thank Dr. M. Ertan GUNES for his help during the sampling section.
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This study was supported by The Scientific and Technological Research Council of Turkey (TUBITAK Project No: 116Y208).
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Sari, M.F., Gurkan Ayyildiz, E. & Esen, F. Determination of polychlorinated biphenyls in honeybee, pollen, and honey samples from urban and semi-urban areas in Turkey. Environ Sci Pollut Res 27, 4414–4422 (2020). https://doi.org/10.1007/s11356-019-07013-w
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DOI: https://doi.org/10.1007/s11356-019-07013-w