Honeybees and their products as bioindicators for heavy metal pollution in Malta
Abstract
In this study, honeybees, propolis, air, soil and plant samples were gathered from two contrasting sites Ħal Luqa (industrial area) and L-Imġarr (agricultural area) in mainland Malta. Superficial heavy metals were extracted from the samples and tested using microwave plasma-atomic emission spectrometry in order to determine the concentrations of Ag, As, Cd, Cr, Cu, Pb, Sn, Zn, Ni and Hg. The honeybee and propolis samples were digested using nitric acid and hydrogen peroxide and then ashed using a muffle furnace in order to prepare mineral solutions. Simultaneously the air samplers, soil and plant samples were washed using de-ionised water in order to extract the heavy metals settling on sample surfaces. Different methods of filtration were used in order to extract the metals from the surfaces of the samples. The most abundant metals in honeybees and propolis, and on plant and soil samples, were Sn and As (p<0.0001). In air samples0, the most abundant metal was Pb followed by Sn (p<0.05). These findings indicate that the honeybee and its propolis are good indicators for Sn and As contamination.
Downloads
Download data is not yet available.
References
Abrol, D. (2010). Pollination Biology. Springer Science+Business Media B.V. The Netherlands. doi: 10.1007/978-94-007-1942-2
Air Quality, E. (2019). Existing Legislation - Air Quality - Environment -European Commission. Recovered from http://ec.europa.eu/environment/air/quality/legislation/existing_leg.htm
Attard, E (2004). Status of Medicinal and Aromatic Plants in Malta in Baricevic, D., Bernath, J., Maggioni, L. and Lipman E. Report of a Working Group on Medicinal and Aromatic Plants, First Meeting, 12-14 September 2002, Gozd Martuljek, Slovenia, International Plant Genetic Resources Institute, Rome, Italy, 85-87.
Attard, E., & Bugeja Douglas, A. (2017). Physicochemical Characterization of Maltese Honey. Honey Analysis, Prof. Dr. Vagner Arnaut (Ed.), InTech Recovered from: https://www.intechopen.com/books/ honey-analysis/physicochemical-characterization-of-maltese-honey
Badiou-Bénéteau, A., Benneveau, A., Géret, F., Delatte, H., Becker, N., Brunet, J., Reynaud, B., & Belzunces, L. P. (2013). Honeybee biomarkers as promising tools to monitor environmental quality. Environment International, 60, 31-41. doi: 10.1016/j.envint.2013.07.002
Balestra, V., Celli, G., & Porrini, C. (1992). Bees, honey, larvae and pollen in biomonitoring of atmospheric pollution. Aerobiologia, 8(1), 122-126. doi: 10.1007/bf02291339
Baranowska, I., Srogi, K., Włochowicz, A., & Szczepanik, K. (2002). Determination of Heavy Metal Contents in Samples of Medicinal Herbs. Polish Journal of Environmental Studies, 11(5), 467-471. Recovered from http://www.pjoes.com/pdf/11.5/467-471.pdf
Bertholf, L., & Pilson, J. (1941). Studies on Toxicity to Honeybees of Acid Lead Arsenate, Calcium Arsenate, Phenothiazine, and Cryolite. Journal of Economic Entomology, 34(1), 24-33. doi: 10.1093/jee/34.1.24
Bonvehí, J. S., & Bermejo, F. O. (2013). Element content of propolis collected from different areas of South Spain. Environmental Monitoring and Assessment, 185(7), 6035-6047.
Borsuk, G., Paleolog, J., Olszewski, K., & Strachecka, A. (2013). Laboratory assessment of the effect of nanosilver on longevity, sugar syrup ingestion, and infection of honeybees with Nosema spp. Medycyna Weterynaryjna, 69(12), 730-732. Recovered from http://www.medycynawet.edu.pl
Bromenshenk, J., Henderson, C., Wick, C., Stanford, M., Zulich, A., Jabbour, R. E., Deshpande, S. V., McCubbin, P. E., Seccomb, R. A., Welch, P. M. & Williams, T., (2010). Iridovirus and Microsporidian Linked to Honey Bee Colony Decline. PLOS ONE. doi: 10.1371/journal.pone.0013181
Brown, S., & Welton, W. (2008). Heavy metal pollution Nova Science Pub Inc; UK.
Çelik, A., Kartal, A., Akdoğan, A., & Kaska, Y. (2005). Determining the heavy metal pollution in Denizli (Turkey) by using Robinio pseudo-acacia L. Environment International, 31(1), 105-112. doi: 10.1016/j.envint.2004.07.004
Charlesworth, S., Everett, M., McCarthy, R., Ordóñez, A., & de Miguel, E. (2003). A comparative study of heavy metal concentration and distribution in deposited street dusts in a large and a small urban area: Birmingham and Coventry, West Midlands, UK. Environment International, 29(5), 563-573. doi: 10.1016/s0160-4120(03)00015-1
Clemens, S., Palmgren, M., & Krämer, U. (2002). A long way ahead: understanding and engineering plant metal accumulation. Trends in Plant Science, 7(7), 309-315. doi: 10.1016/s1360-1385(02)02295-1
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. doi: 10.1023/a:1010719107006
De la Rúa, P., Jaffé, R., Dall'Olio, R., Muñoz, I., & Serrano, J. (2009). Biodiversity, conservation and current threats to European honeybees. Apidologie, 40(3), 263-284. doi: 10.1051/apido/2009027
Devillers, J., & Pham-Delègue, M. (2002). Honey bees: Estimating the Environmental Impact of Chemicals. Taylor & Francis. London, UK.
Di, N., Hladun, K., Zhang, K., Liu, T., & Trumble, J. (2016). Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere, 152, 530-538. doi: 10.1016/j.chemosphere.2016.03.033
Directive 2001/81/EC of the European Parliament and of the Council of 23 October 2001 on national emission ceilings for certain atmospheric pollutants. Official Journal of the European Communities. L. 309. 22-30.
Directive 2004/107/EC of the European Parliament and of the Council of 15 December 2004 relating to arsenic, cadmium, mercury, nickel and polycyclic aromatic hydrocarbons in ambient air. Official Journal of the European Communities. L. 23. 3-16.
Directive 2008/50/EC of the European Parliament and of the Council of 21 May 2008 on ambient air quality and cleaner air for Europe. Official Journal of the European Communities. L. 152. 1-44.
Dospatliev, L., Kostadinov, K., Mihaylova, G., & Katrandzhiev, N. (2012). Determination of Heavy Metals (Pb, Zn, Cd and Ni) in Eggplant. Trakia Journal of Sciences, 10(2), 31-35.
ERA (2019). Subsidiary Legislation 549.59 Ambient Air Quality Regulations Recovered from https://eracms.gov.mt/en/Pages/S-L-549-59-Ambient-Air-Quality-Regulations.aspx.
Ferreira, B. L., Gonzaga, L. V., Vitali, L., Micke, G. A., Maltez, H. F., Ressureição, C., Oliveira Costa, A. C., & Fett. R (2019). Southern-Brazilian Geopropolis: A potential source of polyphenolic compounds and assessment of mineral composition. Food Research International, 108683. doi: 10.1016/j.foodres.2019.108683
Finger, D., Kelte Filho, I., Torres, Y. R., & Quináia, S. P. (2014). Propolis as an indicator of environmental contamination by metals. Bulletin of Environmental Contamination and Toxicology, 92(3), 259-264.
Formicki, G., Gren, A., Stawarz, R., Zysk, B., & Gal, 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.
Fowler, D., Skiba, U., Nemitz, E., Choubedar, F., Branford, D., Donovan, R., & Rowland, P. (2004). Measuring Aerosol and Heavy Metal Deposition on Urban Woodland and Grass Using Inventories of 210Pb and Metal Concentrations in Soil. Water, Air, & Soil Pollution: Focus, 4(2/3), 483-499. doi: 10.1023/b:wafo.0000028373.02470.ba
Gagné, F. (2012). A new research journal to understand the interactions of xenobiotics with living organisms. Journal of Xenobiotics, 2(1), 8. doi: 10.4081/xeno.2012.e8
Golomb, D., Ryan, D., Eby, N., Underhill, J., & Zemba, S. (1997). Atmospheric deposition of toxics onto Massachusetts Bay—I. Metals. Atmospheric Environment, 31(9), 1349-1359. doi: 10.1016/S1352-2310(96)00276-2
González-Martín, M., Escuredo, O., Revilla, I., Vivar-Quintana, A., Coello, M., Riocerezo, C., & Moncada, G. (2015). Determination of the Mineral Composition and Toxic Element Contents of Propolis by Near Infrared Spectroscopy. Sensors, 15(11), 27854-27868. doi: 10.3390/s151127854
Gutiérrez, M., Molero, R., Gaju, M., Van der Steen, J., Porrini, C., & Ruiz, J. (2015). Assessment of heavy metal pollution in Córdoba (Spain) by biomonitoring foraging honeybee. Environmental Monitoring and Assessment, 187(10). doi: 10.1007/s10661-015-4877-8
Handika, R. A., Purwaningrum, S. I., & Lestari, R. A. (2019). Analisis Risiko Non Karsinogenik Pajanan PM10 di Kawasan Komersial, Kota Jambi. Jurnal Serambi Engineering, 4(2). doi: 10.32672/jse.v4i2.1329
Kampouroglou, E., & Economou-Eliopoulos, M. (2013). Natural contamination by As and heavy metals in soil, their bio-accumulation and potential sources: the case of a travertine limestone quarry, Greece. Open Geosciences, 5(1). doi: 10.2478/s13533-012-0122-y
Krmar, M., Radnović, D., & Frontasyeva, M. V. (2012). Moss Biomonitoring Technique Used to Study Spatial and Temporal Atmospheric Deposition of Heavy Metals and Airborne Radionuclides in Serbia. Essays of Fundamental and Applied Environmental Topics/Ed. DT Mihailovic. Nova Publ. Inc, 159Ä192.
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. doi: 10.1007/bf00399566
Lepp, N. W. (Ed.). (2012). Effect of heavy metal pollution on plants: metals in the environment (Vol. 2). Springer Science & Business Media. London.
Maas, S., Scheifler, R., Benslama, M., Crini, N., Lucot, E., Brahmia, Z., Benyacoub, S. & Giraudoux, P. (2010). Spatial distribution of heavy metal concentrations in urban, suburban and agricultural soils in a Mediterranean city of Algeria. Environmental Pollution, 158(6), 2294-2301. doi: 10.1016/j.envpol.2010.02.001
Maître, A., Collot-Fertey, D., Anzivino, L. M. M. H. M., Marques, M., Hours, M., & Stoklov, M. (2003). Municipal waste incinerators: air and biological monitoring of workers for exposure to particles, metals, and organic compounds. Occupational and Environmental Medicine, 60(8), 563-569. doi: 10.1136/oem.60.8.563
Maragou, N., Pavlidis, G., Karasali, H., & Hatjina, F. (2017). Determination of Arsenic in Honey, Propolis, Pollen and Honey Bees by Microwave Digestion and Hydride Generation Flame Atomic Absorption. Analytical Letters, 50(11), 1831-1838. doi: 10.1080/00032719.2016.1244542
Markle, S. (2013). The case of the vanishing honeybees (1st ed.). Millbrook Press. Minneapolis. USA.
Matin, G., Kargar, N., & Buyukisik, H. B. (2016). Bio-monitoring of cadmium, lead, arsenic and mercury in industrial districts of Izmir, Turkey by using honey bees, propolis and pine tree leaves. Ecological Engineering, 90, 331-335. doi: 10.1016/j.ecoleng.2016.01.035.
Nikolić, T. V., Kojić, D., Orčić, S., Batinić, D., Vukašinović, E., Blagojević, D. P., & Purać, J. (2016). The impact of sublethal concentrations of Cu, Pb and Cd on honey bee redox status, superoxide dismutase and catalase in laboratory conditions. Chemosphere, 164, 98-105. doi: 10.1016/j.chemosphere.2016.08.077.
Onder, S., & Dursun, S. (2006). Air borne heavy metal pollution of Cedrus libani (A. Rich.) in the city centre of Konya (Turkey). Atmospheric Environment, 40(6), 1122-1133. doi: 10.1016/j.atmosenv.2005.11.006
Ordonez, A., Loredo, J., De Miguel, E., & Charlesworth, S. (2003). Distribution of Heavy Metals in the Street Dusts and Soils of an Industrial City in Northern Spain. Archives of Environmental Contamination and Toxicology, 44(2), 160-170. doi: 10.1007/s00244-002-2005-6
Peris, M., Micó, C., Recatalá, L., Sánchez, R., & Sánchez, J. (2007). Heavy metal contents in horticultural crops of a representative area of the European Mediterranean region. Science of the Total Environment, 378(1-2), 42-48. doi: 10.1016/j.scitotenv.2007.01.030
Perugini, M., Manera, M., Grotta, L., Abete, M., Tarasco, R., & Amorena, M. (2010). Heavy Metal (Hg, Cr, Cd, and Pb) Contamination in Urban Areas and Wildlife Reserves: Honeybees as Bioindicators. Biological Trace Element Research, 140(2), 170-176. doi: 10.1007/s12011-010-8688-z
Popescu, I. V., Frontasyeva, M., Stihi, C., Cimpoca, G. V., Radulescu, C., Gheboianu, A., Oros, C., Vlaicu, G., Petre, C., Bancuta, I., & Dulama, I. D. (2010). Nuclear and nuclear related analytical methods applied in environmental research. Romanian Journal of Physics. 55(7-8), 821-829.
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) 663-669.
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.z
Sabin, L. D., Lim, J. H., Stolzenbach, K. D., & Schiff, K. C. (2006). Atmospheric dry deposition of trace metals in the coastal region of Los Angeles, California, USA. Environmental Toxicology and Chemistry: An International Journal, 25(9), 2334-2341. doi: 10.1897/05-300R.1
Sakata, M., & Marumoto, K. (2004). Dry deposition fluxes and deposition velocities of trace metals in the Tokyo metropolitan area measured with a water surface sampler. Environmental Science & Technology, 38(7), 2190-2197. doi: 10.1021/es030467k
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(9), 3977-3988. doi. 10.1007/s11356-012-0921-1
Schembri, P. J. (1997). The Maltese Islands: climate, vegetation and landscape. GeoJournal, 41(2), 1-11. doi: 10.1023/a:1006828706452
Schreuder, M. D., Brewer, C. A., & Heine, C. (2001). Modelled influences of non-exchanging trichomes on leaf boundary layers and gas exchange. Journal of Theoretical Biology, 210(1), 23-32.
Sheppard, W., Arias, M., Grech, A., & Meixner, M. (1997). Apis mellifera ruttneri, a new honey bee subspecies from Malta. Apidologie, 28(5), 287-293. doi: 10.1051/apido:19970505
Sultana, J. & Falzon, V. (2002). Wildlife of the Maltese Islands (1st ed.). BirdLife Malta. Floriana, Malta.
Suryanarayanan, S., & Kleinman, D. (2016). Vanishing bees: Science, Politics, and Honeybee Health (Nature, Society, and Culture) (1st ed.). Rutgers University Press. New Jersey, USA.
Swaileh, K., & Abdulkhaliq, A. (2013). Analysis of aflatoxins, caffeine, nicotine and heavy metals in Palestinian multifloral honey from different geographic regions. Journal of the Science of Food and Agriculture, 93(9), 2116-2120. doi: 10.1002/jsfa.6014
Tautz, J., Sandeman, D., & Heilmann, H. (2008). The buzz about bees: Biology of a Superorganism (1st ed.). Springer. Berlin, Germany.
Tchounwou, P., Yedjou, C., Patlolla, A., & Sutton, D. (2012). Heavy Metal Toxicity and the Environment. Experientia Supplementum, 133-164. doi: 10.1007/978-3-7643-8340-46
Van der Steen, J. (2016). Beehold: the colony of the honeybee (Apis mellifera L) as a bio-sampler for pollutants and plant pathogens (Ph.D. thesis) Wageningen University. Netherlands.
Van der Steen, J., Cornelissen, B., Blacquière, T., Pijnenburg, J., & Severijnen, M. (2016). Think regionally, act locally: metals in honeybee workers in the Netherlands (surveillance study 2008). Environmental Monitoring and Assessment, 188(8). doi: 10.1007/s10661-016-5451-8
Van der Steen, J., de Kraker, J., & Grotenhuis, J. T. C. (2015). Assessment of the potential of honeybees (Apis mellifera L.) in biomonitoring of air pollution by cadmium, lead and vanadium. Journal of Environmental Protection, 6(2), 96-102. doi: 10.4236/jep.2015.62011.
Van der Steen, J., de Kraker, J., & Grotenhuis, T. (2011). Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.). Environmental Monitoring and Assessment, 184(7), 4119-4126. doi: 10.1007/s10661-011-2248-7
Vernet, J. (1992). Impact of heavy metals on the environment (Volume 2). Elsevier. Amsterdam, The Netherlands.
Wunderground.com (2017) Weather History for Luqa, Mauritania Weather Underground. Recovered from https://www.wunderground.com/history/
Wilson-Rich, N., Allin, K., Carreck, N., & Quigley, A. (2014). The Bee: A Natural History (1st ed.). Princeton University Press. New Jersey, USA.
Xian, Y., Wang, M., & Chen, W. (2015). Quantitative assessment on soil enzyme activities of heavy metal contaminated soils with various soil properties. Chemosphere, 139, 604-608. doi: 10.1016/j.chemosphere.2014.12.060
Zhelyazkova, I., Atanasova, S., Barakova, V., & Mihaylova, G. (2010). Content of heavy metals and metalloids in bees and bee products from areas with different degree of anthropogenic impact. Agricultural Science and Technology, 3(1), 136 - 142.
Air Quality, E. (2019). Existing Legislation - Air Quality - Environment -European Commission. Recovered from http://ec.europa.eu/environment/air/quality/legislation/existing_leg.htm
Attard, E (2004). Status of Medicinal and Aromatic Plants in Malta in Baricevic, D., Bernath, J., Maggioni, L. and Lipman E. Report of a Working Group on Medicinal and Aromatic Plants, First Meeting, 12-14 September 2002, Gozd Martuljek, Slovenia, International Plant Genetic Resources Institute, Rome, Italy, 85-87.
Attard, E., & Bugeja Douglas, A. (2017). Physicochemical Characterization of Maltese Honey. Honey Analysis, Prof. Dr. Vagner Arnaut (Ed.), InTech Recovered from: https://www.intechopen.com/books/ honey-analysis/physicochemical-characterization-of-maltese-honey
Badiou-Bénéteau, A., Benneveau, A., Géret, F., Delatte, H., Becker, N., Brunet, J., Reynaud, B., & Belzunces, L. P. (2013). Honeybee biomarkers as promising tools to monitor environmental quality. Environment International, 60, 31-41. doi: 10.1016/j.envint.2013.07.002
Balestra, V., Celli, G., & Porrini, C. (1992). Bees, honey, larvae and pollen in biomonitoring of atmospheric pollution. Aerobiologia, 8(1), 122-126. doi: 10.1007/bf02291339
Baranowska, I., Srogi, K., Włochowicz, A., & Szczepanik, K. (2002). Determination of Heavy Metal Contents in Samples of Medicinal Herbs. Polish Journal of Environmental Studies, 11(5), 467-471. Recovered from http://www.pjoes.com/pdf/11.5/467-471.pdf
Bertholf, L., & Pilson, J. (1941). Studies on Toxicity to Honeybees of Acid Lead Arsenate, Calcium Arsenate, Phenothiazine, and Cryolite. Journal of Economic Entomology, 34(1), 24-33. doi: 10.1093/jee/34.1.24
Bonvehí, J. S., & Bermejo, F. O. (2013). Element content of propolis collected from different areas of South Spain. Environmental Monitoring and Assessment, 185(7), 6035-6047.
Borsuk, G., Paleolog, J., Olszewski, K., & Strachecka, A. (2013). Laboratory assessment of the effect of nanosilver on longevity, sugar syrup ingestion, and infection of honeybees with Nosema spp. Medycyna Weterynaryjna, 69(12), 730-732. Recovered from http://www.medycynawet.edu.pl
Bromenshenk, J., Henderson, C., Wick, C., Stanford, M., Zulich, A., Jabbour, R. E., Deshpande, S. V., McCubbin, P. E., Seccomb, R. A., Welch, P. M. & Williams, T., (2010). Iridovirus and Microsporidian Linked to Honey Bee Colony Decline. PLOS ONE. doi: 10.1371/journal.pone.0013181
Brown, S., & Welton, W. (2008). Heavy metal pollution Nova Science Pub Inc; UK.
Çelik, A., Kartal, A., Akdoğan, A., & Kaska, Y. (2005). Determining the heavy metal pollution in Denizli (Turkey) by using Robinio pseudo-acacia L. Environment International, 31(1), 105-112. doi: 10.1016/j.envint.2004.07.004
Charlesworth, S., Everett, M., McCarthy, R., Ordóñez, A., & de Miguel, E. (2003). A comparative study of heavy metal concentration and distribution in deposited street dusts in a large and a small urban area: Birmingham and Coventry, West Midlands, UK. Environment International, 29(5), 563-573. doi: 10.1016/s0160-4120(03)00015-1
Clemens, S., Palmgren, M., & Krämer, U. (2002). A long way ahead: understanding and engineering plant metal accumulation. Trends in Plant Science, 7(7), 309-315. doi: 10.1016/s1360-1385(02)02295-1
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. doi: 10.1023/a:1010719107006
De la Rúa, P., Jaffé, R., Dall'Olio, R., Muñoz, I., & Serrano, J. (2009). Biodiversity, conservation and current threats to European honeybees. Apidologie, 40(3), 263-284. doi: 10.1051/apido/2009027
Devillers, J., & Pham-Delègue, M. (2002). Honey bees: Estimating the Environmental Impact of Chemicals. Taylor & Francis. London, UK.
Di, N., Hladun, K., Zhang, K., Liu, T., & Trumble, J. (2016). Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere, 152, 530-538. doi: 10.1016/j.chemosphere.2016.03.033
Directive 2001/81/EC of the European Parliament and of the Council of 23 October 2001 on national emission ceilings for certain atmospheric pollutants. Official Journal of the European Communities. L. 309. 22-30.
Directive 2004/107/EC of the European Parliament and of the Council of 15 December 2004 relating to arsenic, cadmium, mercury, nickel and polycyclic aromatic hydrocarbons in ambient air. Official Journal of the European Communities. L. 23. 3-16.
Directive 2008/50/EC of the European Parliament and of the Council of 21 May 2008 on ambient air quality and cleaner air for Europe. Official Journal of the European Communities. L. 152. 1-44.
Dospatliev, L., Kostadinov, K., Mihaylova, G., & Katrandzhiev, N. (2012). Determination of Heavy Metals (Pb, Zn, Cd and Ni) in Eggplant. Trakia Journal of Sciences, 10(2), 31-35.
ERA (2019). Subsidiary Legislation 549.59 Ambient Air Quality Regulations Recovered from https://eracms.gov.mt/en/Pages/S-L-549-59-Ambient-Air-Quality-Regulations.aspx.
Ferreira, B. L., Gonzaga, L. V., Vitali, L., Micke, G. A., Maltez, H. F., Ressureição, C., Oliveira Costa, A. C., & Fett. R (2019). Southern-Brazilian Geopropolis: A potential source of polyphenolic compounds and assessment of mineral composition. Food Research International, 108683. doi: 10.1016/j.foodres.2019.108683
Finger, D., Kelte Filho, I., Torres, Y. R., & Quináia, S. P. (2014). Propolis as an indicator of environmental contamination by metals. Bulletin of Environmental Contamination and Toxicology, 92(3), 259-264.
Formicki, G., Gren, A., Stawarz, R., Zysk, B., & Gal, 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.
Fowler, D., Skiba, U., Nemitz, E., Choubedar, F., Branford, D., Donovan, R., & Rowland, P. (2004). Measuring Aerosol and Heavy Metal Deposition on Urban Woodland and Grass Using Inventories of 210Pb and Metal Concentrations in Soil. Water, Air, & Soil Pollution: Focus, 4(2/3), 483-499. doi: 10.1023/b:wafo.0000028373.02470.ba
Gagné, F. (2012). A new research journal to understand the interactions of xenobiotics with living organisms. Journal of Xenobiotics, 2(1), 8. doi: 10.4081/xeno.2012.e8
Golomb, D., Ryan, D., Eby, N., Underhill, J., & Zemba, S. (1997). Atmospheric deposition of toxics onto Massachusetts Bay—I. Metals. Atmospheric Environment, 31(9), 1349-1359. doi: 10.1016/S1352-2310(96)00276-2
González-Martín, M., Escuredo, O., Revilla, I., Vivar-Quintana, A., Coello, M., Riocerezo, C., & Moncada, G. (2015). Determination of the Mineral Composition and Toxic Element Contents of Propolis by Near Infrared Spectroscopy. Sensors, 15(11), 27854-27868. doi: 10.3390/s151127854
Gutiérrez, M., Molero, R., Gaju, M., Van der Steen, J., Porrini, C., & Ruiz, J. (2015). Assessment of heavy metal pollution in Córdoba (Spain) by biomonitoring foraging honeybee. Environmental Monitoring and Assessment, 187(10). doi: 10.1007/s10661-015-4877-8
Handika, R. A., Purwaningrum, S. I., & Lestari, R. A. (2019). Analisis Risiko Non Karsinogenik Pajanan PM10 di Kawasan Komersial, Kota Jambi. Jurnal Serambi Engineering, 4(2). doi: 10.32672/jse.v4i2.1329
Kampouroglou, E., & Economou-Eliopoulos, M. (2013). Natural contamination by As and heavy metals in soil, their bio-accumulation and potential sources: the case of a travertine limestone quarry, Greece. Open Geosciences, 5(1). doi: 10.2478/s13533-012-0122-y
Krmar, M., Radnović, D., & Frontasyeva, M. V. (2012). Moss Biomonitoring Technique Used to Study Spatial and Temporal Atmospheric Deposition of Heavy Metals and Airborne Radionuclides in Serbia. Essays of Fundamental and Applied Environmental Topics/Ed. DT Mihailovic. Nova Publ. Inc, 159Ä192.
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. doi: 10.1007/bf00399566
Lepp, N. W. (Ed.). (2012). Effect of heavy metal pollution on plants: metals in the environment (Vol. 2). Springer Science & Business Media. London.
Maas, S., Scheifler, R., Benslama, M., Crini, N., Lucot, E., Brahmia, Z., Benyacoub, S. & Giraudoux, P. (2010). Spatial distribution of heavy metal concentrations in urban, suburban and agricultural soils in a Mediterranean city of Algeria. Environmental Pollution, 158(6), 2294-2301. doi: 10.1016/j.envpol.2010.02.001
Maître, A., Collot-Fertey, D., Anzivino, L. M. M. H. M., Marques, M., Hours, M., & Stoklov, M. (2003). Municipal waste incinerators: air and biological monitoring of workers for exposure to particles, metals, and organic compounds. Occupational and Environmental Medicine, 60(8), 563-569. doi: 10.1136/oem.60.8.563
Maragou, N., Pavlidis, G., Karasali, H., & Hatjina, F. (2017). Determination of Arsenic in Honey, Propolis, Pollen and Honey Bees by Microwave Digestion and Hydride Generation Flame Atomic Absorption. Analytical Letters, 50(11), 1831-1838. doi: 10.1080/00032719.2016.1244542
Markle, S. (2013). The case of the vanishing honeybees (1st ed.). Millbrook Press. Minneapolis. USA.
Matin, G., Kargar, N., & Buyukisik, H. B. (2016). Bio-monitoring of cadmium, lead, arsenic and mercury in industrial districts of Izmir, Turkey by using honey bees, propolis and pine tree leaves. Ecological Engineering, 90, 331-335. doi: 10.1016/j.ecoleng.2016.01.035.
Nikolić, T. V., Kojić, D., Orčić, S., Batinić, D., Vukašinović, E., Blagojević, D. P., & Purać, J. (2016). The impact of sublethal concentrations of Cu, Pb and Cd on honey bee redox status, superoxide dismutase and catalase in laboratory conditions. Chemosphere, 164, 98-105. doi: 10.1016/j.chemosphere.2016.08.077.
Onder, S., & Dursun, S. (2006). Air borne heavy metal pollution of Cedrus libani (A. Rich.) in the city centre of Konya (Turkey). Atmospheric Environment, 40(6), 1122-1133. doi: 10.1016/j.atmosenv.2005.11.006
Ordonez, A., Loredo, J., De Miguel, E., & Charlesworth, S. (2003). Distribution of Heavy Metals in the Street Dusts and Soils of an Industrial City in Northern Spain. Archives of Environmental Contamination and Toxicology, 44(2), 160-170. doi: 10.1007/s00244-002-2005-6
Peris, M., Micó, C., Recatalá, L., Sánchez, R., & Sánchez, J. (2007). Heavy metal contents in horticultural crops of a representative area of the European Mediterranean region. Science of the Total Environment, 378(1-2), 42-48. doi: 10.1016/j.scitotenv.2007.01.030
Perugini, M., Manera, M., Grotta, L., Abete, M., Tarasco, R., & Amorena, M. (2010). Heavy Metal (Hg, Cr, Cd, and Pb) Contamination in Urban Areas and Wildlife Reserves: Honeybees as Bioindicators. Biological Trace Element Research, 140(2), 170-176. doi: 10.1007/s12011-010-8688-z
Popescu, I. V., Frontasyeva, M., Stihi, C., Cimpoca, G. V., Radulescu, C., Gheboianu, A., Oros, C., Vlaicu, G., Petre, C., Bancuta, I., & Dulama, I. D. (2010). Nuclear and nuclear related analytical methods applied in environmental research. Romanian Journal of Physics. 55(7-8), 821-829.
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) 663-669.
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.z
Sabin, L. D., Lim, J. H., Stolzenbach, K. D., & Schiff, K. C. (2006). Atmospheric dry deposition of trace metals in the coastal region of Los Angeles, California, USA. Environmental Toxicology and Chemistry: An International Journal, 25(9), 2334-2341. doi: 10.1897/05-300R.1
Sakata, M., & Marumoto, K. (2004). Dry deposition fluxes and deposition velocities of trace metals in the Tokyo metropolitan area measured with a water surface sampler. Environmental Science & Technology, 38(7), 2190-2197. doi: 10.1021/es030467k
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(9), 3977-3988. doi. 10.1007/s11356-012-0921-1
Schembri, P. J. (1997). The Maltese Islands: climate, vegetation and landscape. GeoJournal, 41(2), 1-11. doi: 10.1023/a:1006828706452
Schreuder, M. D., Brewer, C. A., & Heine, C. (2001). Modelled influences of non-exchanging trichomes on leaf boundary layers and gas exchange. Journal of Theoretical Biology, 210(1), 23-32.
Sheppard, W., Arias, M., Grech, A., & Meixner, M. (1997). Apis mellifera ruttneri, a new honey bee subspecies from Malta. Apidologie, 28(5), 287-293. doi: 10.1051/apido:19970505
Sultana, J. & Falzon, V. (2002). Wildlife of the Maltese Islands (1st ed.). BirdLife Malta. Floriana, Malta.
Suryanarayanan, S., & Kleinman, D. (2016). Vanishing bees: Science, Politics, and Honeybee Health (Nature, Society, and Culture) (1st ed.). Rutgers University Press. New Jersey, USA.
Swaileh, K., & Abdulkhaliq, A. (2013). Analysis of aflatoxins, caffeine, nicotine and heavy metals in Palestinian multifloral honey from different geographic regions. Journal of the Science of Food and Agriculture, 93(9), 2116-2120. doi: 10.1002/jsfa.6014
Tautz, J., Sandeman, D., & Heilmann, H. (2008). The buzz about bees: Biology of a Superorganism (1st ed.). Springer. Berlin, Germany.
Tchounwou, P., Yedjou, C., Patlolla, A., & Sutton, D. (2012). Heavy Metal Toxicity and the Environment. Experientia Supplementum, 133-164. doi: 10.1007/978-3-7643-8340-46
Van der Steen, J. (2016). Beehold: the colony of the honeybee (Apis mellifera L) as a bio-sampler for pollutants and plant pathogens (Ph.D. thesis) Wageningen University. Netherlands.
Van der Steen, J., Cornelissen, B., Blacquière, T., Pijnenburg, J., & Severijnen, M. (2016). Think regionally, act locally: metals in honeybee workers in the Netherlands (surveillance study 2008). Environmental Monitoring and Assessment, 188(8). doi: 10.1007/s10661-016-5451-8
Van der Steen, J., de Kraker, J., & Grotenhuis, J. T. C. (2015). Assessment of the potential of honeybees (Apis mellifera L.) in biomonitoring of air pollution by cadmium, lead and vanadium. Journal of Environmental Protection, 6(2), 96-102. doi: 10.4236/jep.2015.62011.
Van der Steen, J., de Kraker, J., & Grotenhuis, T. (2011). Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.). Environmental Monitoring and Assessment, 184(7), 4119-4126. doi: 10.1007/s10661-011-2248-7
Vernet, J. (1992). Impact of heavy metals on the environment (Volume 2). Elsevier. Amsterdam, The Netherlands.
Wunderground.com (2017) Weather History for Luqa, Mauritania Weather Underground. Recovered from https://www.wunderground.com/history/
Wilson-Rich, N., Allin, K., Carreck, N., & Quigley, A. (2014). The Bee: A Natural History (1st ed.). Princeton University Press. New Jersey, USA.
Xian, Y., Wang, M., & Chen, W. (2015). Quantitative assessment on soil enzyme activities of heavy metal contaminated soils with various soil properties. Chemosphere, 139, 604-608. doi: 10.1016/j.chemosphere.2014.12.060
Zhelyazkova, I., Atanasova, S., Barakova, V., & Mihaylova, G. (2010). Content of heavy metals and metalloids in bees and bee products from areas with different degree of anthropogenic impact. Agricultural Science and Technology, 3(1), 136 - 142.
Published
2020-01-20
How to Cite
BORG, Daniel; ATTARD, Everaldo.
Honeybees and their products as bioindicators for heavy metal pollution in Malta.
Acta Brasiliensis, [S.l.], v. 4, n. 1, p. 60-69, jan. 2020.
ISSN 2526-4338.
Available at: <http://revistas.ufcg.edu.br/actabra/index.php/actabra/article/view/282>. Date accessed: 19 dec. 2024.
doi: https://doi.org/10.22571/2526-4338282.
Section
Environmental Chemistry
