PCA and LDA Assessment of the Heavy Metal Contamination in Honey Bees, Bee Pollen and Honey Produced in Urban Areas of Türkiye

Year 2023, Volume: 15 Issue: 2, 49 - 59, 28.12.2023

Fatma İlhan , Hüseyin Bayır , Ali Aygün

Abstract

Heavy metals are of great importance in terms of environmental pollution. Environmental pollution affects not only humans but also plants and animals. Living organisms with varying sensitivity to various pollutants can be used to assess environmental pollution. Honey bees have been used as bioindicators for this purpose because they operate in very large areas in their region. The aim of this study is to investigate heavy metal pollution in honey bees and bee products in 4 different urban regions of Konya using principal component analysis (PCA) and linear discriminant analysis. In this study, when the heavy metal contents of honey bees, bee pollen, and honey samples are compared, it is seen that bees are exposed to more heavy metal contamination. Honey bees don`t reflect these amounts in the honey, and the heavy metal content in honey remains in much smaller amounts. When principal component analysis (PCA) is applied to these samples, the heavy metal variation of bees and bee pollen can be explained by three components, while the variation of the heavy metal contents of honey can be explained by four components. Linear discriminant analysis was performed to distinguish the geographic locations of the samples. According to the results of the LDA analysis for heavy metal content, the bees can be assigned to 80% and the pollen and honey to 100% of their correct geographical origin.

Keywords

Principal component analysis, Linear discriminant analysis, Heavy metal pollution, Bioindicator

Ethical Statement

Not applicable.

Supporting Institution

Selçuk University provided funding for this project (Project Number: BAP-18101008).

Project Number

Project Number: BAP-18101008

References

• Adgaba, N., Al-Ghamdi, A. A., Getachew, A., Tadesse, Y., Belay, A., Ansari, M. J., Radloff, S. E., & Sharma, D. (2017). Characterization of honeys by their botanical and geographical origins based on physico-chemical properties and chemo-metrics analysis. Journal of Food Measurement and Characterization, 11, 1106-1117.
• Ahmida, N. H., Elagori, M., Agha, A., Elwerfali, S., & Ahmida, M. H. (2012). Physicochemical, heavy metals and phenolic compounds analysis of Libyan honey samples collected from Benghazi during 2009-2010. Food and Nutrition Sciences, 4(1), 33-40. https://doi.org/https://doi.org/10.4236/fns.2013.4100 6
• Al Naggar, Y., Khalil, M. S., & Ghorab, M. A. (2018). Environmental pollution by heavy metals in the aquatic ecosystems of Egypt. Open Access Journal of Toxicology, 3, 555603.
• Alimentarius, C. (2015). General standard for contaminants and toxins in food and feed (Codex STAN 193-1995). In International Food Standards (Vol. 193).
• Ares, A. M., Martín, M. T., Tapia, J. A., González-Porto, A. V., Higes, M., Martín-Hernández, R., & Bernal, J. (2022a). Differentiation of bee pollen samples according to the betaines and other quaternary ammonium related compounds content by using a canonical discriminant analysis. Food Research International, 160, 111698.
• Ares, A. M., Redondo, M., Tapia, J., González-Porto, A. V., Higes, M., Martín-Hernández, R., & Bernal, J. (2020). Differentiation of bee pollen samples according to their intact-glucosinolate content using canonical discriminant analysis. Lwt, 129, 109559.
• Ares, A. M., Tapia, J. A., González-Porto, A. V., Higes, M., Martín-Hernández, R., & Bernal, J. (2022b). Glucosinolates as markers of the origin and harvesting period for discrimination of bee pollen by UPLC-MS/MS. Foods, 11(10), 1446.
• Bassbasi, M., De Luca, M., Ioele, G., Oussama, A., & Ragno, G. (2014). Prediction of the geographical origin of butters by partial least square discriminant analysis (PLS-DA) applied to infrared spectroscopy (FTIR) data. Journal of Food Composition and Analysis, 33(2), 210-215.
• Bayir, H., & Aygun, A. (2022). Heavy metal in honey bees, honey, and pollen produced in rural and urban areas of Konya province in Türkiye. Environmental Science and Pollution Research, 29(49), 74569-74578. https://doi.org/https://doi.org/10.1007/s11356-02221017-z
• Bazeyad, A. Y., Al-Sarar, A. S., Rushdi, A. I., Hassanin, A. S., & Abobakr, Y. (2019). Levels of heavy metals in a multifloral Saudi honey. Environmental Science and Pollution Research, 26, 3946-3953. https://doi.org/https://doi.org/10.1007/s11356-0183909-7
• Boussaid, A., Chouaibi, M., Rezig, L., Hellal, R., Donsì, F., Ferrari, G., & Hamdi, S. (2018). Physicochemical and bioactive properties of six honey samples from various floral origins from Tunisia. Arabian journal of chemistry, 11(2), 265-274. https://doi.org/https://doi.org/10.1016/j.arabjc.2014.0 8.011
• Caravaca, F., Carrizosa, J., Urrutia, B., Baena, F., Jordana, J., Amills, M., Badaoui, B., Sánchez, A., Angiolillo, A., & Serradilla, J. (2009). Effect of αS1-casein (CSN1S1) and κcasein (CSN3) genotypes on milk composition in Murciano-Granadina goats. Journal of Dairy Science, 92(6), 2960-2964.
• Celli, G., & Maccagnani, B. (2003). Honey bees as bioindicators of environmental pollution. Bulletin of Insectology, 56(1), 137-139.
• Choi, G.-H., & Lee, K.-H. (2012). Effect of ozone treatment for sanitation of egg. Korean Journal for Food Science of Animal Resources, 32(2), 198-203.
• Ćirić, J., Spirić, D., Baltić, T., Lazić, I. B., Trbović, D., Parunović, N., Petronijević, R., & Đorđević, V. (2021). Honey bees and their products as indicators of environmental element deposition. Biological Trace Element Research, 199(6), 2312-2319. https://doi.org/https://doi.org/10.1007/s12011-02002321-6.
• Conti, M. E., Astolfi, M. L., Finoia, M. G., Massimi, L., & Canepari, S. (2022). Biomonitoring of element contamination in bees and beehive products in the Rome province (Italy). Environmental Science and Pollution Research, 29(24), 36057-36074. https://doi.org/https://doi.org/10.1007/s11356-02118072-3.
• 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/https://doi.org/10.1023/A:1010719107 006
• Di Fiore, C., Nuzzo, A., Torino, V., De Cristofaro, A., Notardonato, I., Passarella, S., Di Giorgi, S., & Avino, P. (2022). Honeybees as bioindicators of heavy metal pollution in urban and rural areas in the South of Italy. Atmosphere, 13(4), 624. https://doi.org/https://doi.org/10.3390/atmos1304062 4
• El-Haskoury, R., Kriaa, W., Lyoussi, B., & Makni, M. (2018). Ceratonia siliqua honeys from Morocco: Physicochemical properties, mineral contents, and antioxidant activities. Journal of Food and Drug Analysis, 26(1), 67-73. https://doi.org/https://doi.org/10.1016/j.jfda.2016.11. 016
• Fechner, D. C., Moresi, A. L., Díaz, J. D. R., Pellerano, R. G., & Vazquez, F. A. (2016). Multivariate classification of honeys from Corrientes (Argentina) according to geographical origin based on physicochemical properties. Food Bioscience, 15, 49-54.
• Fernández-Torres, R., Perez-Bernal, J. L., Bello-Lopez, M. A., Callejon-Mochon, M., Jimenez-Sanchez, J. C., & Guiraúm-Pérez, A. (2005). Mineral content and botanical origin of Spanish honeys. Talanta, 65(3), 686-691.
• 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).
• Fredes, C., & Montenegro, G. (2006). Heavy metals and other trace element contents in Chilean honey. Ciencia e Investigacion. Agraria, 33(1), 50-58.
• Goretti, E., Pallottini, M., Rossi, R., La Porta, G., Gardi, T., Cenci Goga, B. T., Elia, A. C., Galletti, M., Moroni, B., Petroselli, C., Selvaggi, R., & Cappelletti, D. (2020). Heavy metal bioaccumulation in honey bee matrix, an indicator to assess the contamination level in terrestrial environments. Environmental Pollution, 256, 113388. https://doi.org/https://doi.org/10.1016/j.envpol.2019. 113388
• Guler, A., & Bek, Y. (2002). Forewing angles of honey bee (Apis mellifera) samples from different regions of Türkiye. Journal of Apicultural Research, 41(1-2), 43-49.
• Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B. B., & Beeregowda, K. N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary toxicology, 7(2), 60. https://doi.org/https://doi.org/10.2478/intox-20140009
• Jöbstl, D., Bandoniene, D., Meisel, T., & Chatzistathis, S. (2010). Identification of the geographical origin of pumpkin seed oil by the use of rare earth elements and discriminant analysis. Food Chemistry, 123(4), 1303-1309.
• Kacar, B., & İnal, A. (2008). Bitki analizleri (Vol. 2). Nobel Akademik.
• Karabagias, I. K., Badeka, A., Kontakos, S., Karabournioti, S., & Kontominas, M. G. (2014). Characterisation and classification of Greek pine honeys according to their geographical origin based on volatiles, physicochemical parameters and chemometrics. Food Chemistry, 146, 548-557.
• Kaškonienė, V., Ruočkuvienė, G., Kaškonas, P., Akuneca, I., & Maruška, A. (2015). Chemometric analysis of bee pollen based on volatile and phenolic compound compositions and antioxidant properties. Food Analytical Methods, 8, 1150-1163.
• Keil, D. E., Berger-Ritchie, J., & McMillin, G. A. (2011). Testing for toxic elements: a focus on arsenic, cadmium, lead, and mercury. Laboratory Medicine, 42(12), 735-742. https://doi.org/https://doi.org/10.1309/LMYKGU05BEP E7IAW
• Leblebici, Z., & Aksoy, A. (2008). Determination of heavy metals in honey samples from Central Anatolia using plasma optical emission spectrofotometry (ICP-OES). Polish Journal of Environmental Studies, 17(4), 549-555.
• Li, Y., Yu, Z.-M., & Song, X. X. (2006). Application of principal component analysis (PCA) for the estimation of source of heavy metal contamination in marine sediments. Huan Jing ke Xue= Huanjing Kexue, 27(1), 137-141.
• Lilek, N., Kandolf Borovšak, A., Bertoncelj, J., Vogel Mikuš, K., & Nečemer, M. (2022). Use of EDXRF elemental fingerprinting for discrimination of botanical and geographical origin of Slovenian bee pollen. X‐Ray Spectrometry, 51(3), 186-197.
• Manu Kumar, H., Ananda, A., & Vishwanathan, D. (2013). Study of Physicochemical parameters and Antioxidant in Honey collected from different locations of India. International Journal of Pharmacy & Life Sciences, 4(12), 3159-3165.
• Meixner, M. D., Leta, M. A., Koeniger, N., & Fuchs, S. (2011). The honey bees of Ethiopia represent a new subspecies of Apis mellifera-Apis mellifera simensis n. ssp. Apidologie, 42, 425-437.
• Mohammed, A. S., Kapri, A., & Goel, R. (2011). Heavy metal pollution: source, impact, and remedies. In Mohammad Saghir Khan, Almas Zaidi, Reeta Goel, & J. Musarrat (Eds.), Biomanagement of metal-contaminated soils (pp. 1-28). Springer Dordrecht. https://doi.org/https://doi.org/10.1007/978-94-0071914-9
• Nozal, M. J., Bernal, J. L., Toribio, L., Alamo, M., Diego, J. C., & Tapia, J. (2005). The use of carbohydrate profiles and chemometrics in the characterization of natural honeys of identical geographical origin. Journal of agricultural and food chemistry, 53(8), 3095-3100.
• Oroian, M., & Ropciuc, S. (2017). Honey authentication based on physicochemical parameters and phenolic compounds. Computers and Electronics in Agriculture, 138, 148-156.
• Ozbakir, G., & Firatli, C. (2013). Morphometric classification of honeybee populations (Apis mellifera L.) along the southeast border of Türkiye. Bulgarian Journal Agricultural Science, 19, 1396-1400.
• Ozdamar, K. (2004). Paket programlar ile istatistiksel veri analizi 2 (çok değişkenli analizler). 7. İstanbul: Kaan Kitabevi.
• Pascoal, A., Chambó, É. D., & Estevinho, L. M. (2022). Botanical origin, physicochemical characterization, and antioxidant activity of bee pollen samples from the northeast of Portugal. Journal of Apicultural Research, 111.
• Pisani, A., Protano, G., & Riccobono, F. (2008). Minor and trace elements in different honey types produced in Siena County (Italy). Food Chemistry, 107(4), 1553-1560. https://doi.org/https://doi.org/10.1016/j.foodchem.20 07.09.029
• Porrini, C., Sabatini, A. G., Girotti, S., Ghini, S., Medrzycki, P., Grillenzoni, F., Bortolotti, L., Gattavecchia, E., & Celli, G.(2003). Honey bees and bee products as monitors of the environmental contamination. Apiacta, 38(1), 63-70.
• Roman, A. (2010). Levels of copper, selenium, lead, and cadmium in forager bees. Polish Journal of Environmental Studies, 19(3).
• Sari, M. F., Gurkan Ayyildiz, E., & Esen, F. (2020). Determination of polychlorinated biphenyls in honeybee, pollen, and honey samples from urban and semi-urban areas in Türkiye. Environmental Science and Pollution Research, 27, 4414-4422. https://doi.org/https://doi.org/10.1007/s11356-01907013-w
• Satta, A., Verdinelli, M., Ruiu, L., Buffa, F., Salis, S., Sassu, A., & Floris, I. (2012). Combination of beehive matrices analysis and ant biodiversity to study heavy metal pollution impact in a post-mining area (Sardinia, Italy). Environmental Science and Pollution Research, 19, 39773988. https://doi.org/https://doi.org/10.1007/s11356012-0921-1.
• Sattler, J. A. G., de Melo, I. L. P., Granato, D., Araújo, E., de Freitas, A. D. S., Barth, O. M., Sattler, A., & de AlmeidaMuradian, L. B. (2015). Impact of origin on bioactive compounds and nutritional composition of bee pollen from Southern Brazil: A screening study. Food Research International, 77, 82-91.
• Serrano, S., Villarejo, M., Espejo, R., & Jodral, M. (2004). Chemical and physical parameters of Andalusian honey: classification of Citrus and Eucalyptus honeys by discriminant analysis. Food Chemistry, 87(4), 619-625.
• Silici, S., Uluozlu, O. D., Tuzen, M., & Soylak, M. (2016). Honeybees and honey as monitors for heavy metal contamination near thermal power plants in Mugla, Türkiye. Toxicology and industrial health, 32(3), 507-516.
• Sıralı, R., Şengül, T., & Yıldız, İ. (2003). Investigations on some morphological characteristics of the honey bees (Apis mellifera L.) of the Harran Plain-Türkiye. Uludağ Arıcılık Dergisi, 3(4), 30-36.
• Stanimirova, I., Üstün, B., Cajka, T., Riddelova, K., Hajslova, J., Buydens, L., & Walczak, B. (2010). Tracing the geographical origin of honeys based on volatile compounds profiles assessment using pattern recognition techniques. Food Chemistry, 118(1), 171176
• Stella, O. (2019). Discriminant analysis: An analysis of its predictship function. Journal of Education and Practice, 10(5), 50-57.
• Strange, J. P., Garnery, L., & Sheppard, W. S. (2008). Morphological and molecular characterization of the Landes honey bee (Apis mellifera L.) ecotype for genetic conservation. Journal of Insect Conservation, 12, 527537.
• Taha, E.K. A., Al-Jabr, A. M., & Al-Kahtani, S. N. (2017). Honey Bees, Bee-collected pollen and honey as monitors of environmental pollution at an industrial cement area in Saudi Arabia. Journal of the Kansas Entomological Society, 90(1), 1-10. https://doi.org/https://doi.org/10.2317/151230.1
• USDA. (2004). Soil Survey Laboratory Methods Manual. In (4 ed.). Washington, DC: U. S. Department of Agriculture.
• Yang, J. S., Hu, X. J., Li, X. X., Li, H. Y., & Wang, Y. (2013). Application of principal component analysis (PCA) for the estimation of source of heavy metal contamination in sediments of Xihe River, Shenyang City. Advanced Materials Research, 610, 948-951.
• Yayinie, M., & Atlabachew, M. (2022). Multi-element analysis of honey from Amhara Region-Ethiopia for quality, bioindicator of environmental pollution, and geographical origin discrimination. Biological Trace Element Research, 200(12), 5283-5297.
• Zarić, N. M., Ilijević, K., Stanisavljević, L., & Gržetić, I. (2017). Use of honeybees (Apis mellifera L.) as bioindicators for assessment and source appointment of metal pollution. Environmental Science and Pollution Research, 24, 25828-25838. https://doi.org/https://doi.org/10.1007/s11356-0170196-7.
• Zhelyazkova, I. (2012). Honeybees–bioindicators for environmental quality. Bulgarian Journal of Agricultural Science, 18(3), 435-442.
• Zhiyuan, W., Dengfeng, W., Huiping, Z., & Zhiping, Q. (2011). Assessment of soil heavy metal pollution with principal component analysis and geoaccumulation index. Procedia Environmental Sciences, 10, 1946-1952. https://doi.org/https://doi.org/10.1016/j.proenv.2011. 09.305