Honey from Stingless Bee as Indicator of Contamination with Metals

Andreia Santos do Nascimento, Emerson Dechechi Chambó, Daiane de Jesus Oliveira, Brunelle Ramos Andrade, Josemario Santana Bonsucesso, Carlos Alfredo Lopes de Carvalho

Abstract


Melipona scutellaris (Apidae, Meliponini) is one of the main species of stingless bees used in beekeeping in the Northeast of Brazil. We examined the honey from M. scutellaris as an indicator to evaluate the levels of metals at sampling sites subject to a broad spectrum of environmental pollutants. The collections were carried out in the urban-industrial area of Salvador, Bahia and the metropolitan region. Samples (n= 58) were submitted to the nitroperchloric digestion procedure. We used the inductively coupled plasma optical emission spectrometry technique (ICP OES) to determine the concentration of metals (Cd, Co, Cr, Cu, Fe, Mn, Mo, Ni, Pb and Zn) in the samples. The studied metals were detected among the samples, which presented tolerable levels according to current Brazilian legislation and recommendations from the World Health Organization (WHO), except for Cr, which presented mean values higher than the threshold for all sampling sites. The detection of the analyzed metals indicates that the honey of M. scutellaris is a useful tool to evaluate the presence of environmental contaminants; therefore, it can be considered a good indicator of environmental contamination for monitoring a particular region and preventing issues due to the release of metals into the environment.

Keywords


Meliponini, Melipona scutellaris, bioindicators, environmental pollution, ICP OES

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References


Aghamirlou, H.M., Khadem, M., Rahmani, A., Sadeghian, M., Mahvi, A.H., Akbarzadeh, A. & Nazmara, S. (2015). Heavy metals determination in honey samples using inductively coupledplasma-optical emission spectrometry. Journal of Environmental Health Science & Engineering, 39: 2-8. doi: 10.1186/s40201-015-0189-8

Atsdr (Agency for Toxic Substances and Disease Registry). (2012a). Toxicological profi le for Chromium. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service. 592p

Atsdr (Agency for Toxic Substances and Disease Registry). (2012b). Toxicological profi le for Manganese. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service. 10p

Atsdr (Agency for Toxic Substances and Disease Registry). (2017).Toxicological profi le for Molybidenium. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service. 276p

Barbosa, A.P., Viana, V.J., Araujo, A.C.P.S. & Lima, D.A. (2017). Evaluation of phytoremediation potentials of some plants species of Serra da Tiririca, Rio de Janeiro, Brazil. International Journal of Plant & Soil Science, 15: 1-9. doi: 10.9734/IJPSS/2017/32075

Barth, O.M. (1989). O pólem no mel brasileiro. Rio de Janeiro: Luxor, 152 p

Bastías, J.M., Jambon, P., Muñoz, O., Manquián, N., Bahamonde, P. & Neira, M. (2013). Honey as a bioindicator of arsenic contamination due to volcanic and mining activities in Chile. Chilean Journal of Agricultural Research, 73: 147-153. doi: 10.4067/S0718-58392013000200010

Batista, B.L., Silva, L.R.S., Rocha, B.A., Rodrigues, J.L., Berretta-Silva, A.A., Bonates, T.O., Gomes, V.S.D., Barbosa, R.M. & Barbosa, F. (2012). Multi-element determination in Brazilian honey samples by inductively coupled plasma mass spectrometry and estimation of geographic origin with data mining techniques. Food Research International, 49: 209-215. doi: 10.1016/j.foodres.2012.07.015

Bogdanov, S. (2006). Contaminants of bee products. Apidologie,37: 1-18. doi: 10.1051/apido:2005043

Bogdanov, S., Haldimann, M., Luginbuh, W. & Gallmann, P. (2007). Minerals in honey: environmental, geographical and botanical aspects. Bee World, 46: 269-275. doi: 10.1080/00218839.2007.11101407

Bonsucesso, J.S., Gloaguen, T.V., Nascimento, A.S.,Carvalho, C.A.L. & Dias, F.S. (2018). Metals in geopropolis from beehive of Melipona scutellaris in urban environments. Science of the Total Environment, 634: 687- 694. doi: 10.1016/j.scitotenv.2018.04.022

Brasil, Ministério da Saúde. (1965). Decreto nº55.871, de 26 de março de 1965. Modifi ca o Decreto nº50.040, de 24 de janeiro de 1961, referente as normas reguladoras do emprego de aditivos para alimentos. http://www.planalto.gov.br/ccivil_03/decreto/1950-1969/anexo/AN55871-65.PDF.

(accessed date: 2 December, 2016)

Brasil, Ministério da Saúde, Secretaria de Vigilância Sanitária. (1998). Portaria nº685, de 27 de agosto de 1998. Aprova o Regulamento Técnico: Princípios Gerais para o Estabelecimento de Níveis Máximos de Contaminantes Químicos em Alimentos” e seu anexo: “Limites máximos de tolerâncias para contaminantes inorgânicos. http://bvsms.saude.gov.br/bvs/saudelegis/anvisa/1998/prt0685_27_08_1998_rep.html. (accessed date: 6 December, 2016)

Brasil, Ministério da Agricultura, Pecuária e Abastecimento. (2009). Instrução Normativa Nº 14, de 25 de maio de 2009. Programas de Controle de Resíduos e Contaminantes em Carnes, Leite, Mel, Ovos e Pescado. http://www.agricultura.gov.br/animal/qualidade-dos-alimentos/residuos-econtaminantes. (accessed date: 8 November, 2016)

Burghardt, W., Morel, J. L. & Zhang, G.L. (2015). Development of the soil research about urban, industrial, traffi c, mining andmilitary areas (SUITMA), Soil Science and Plant Nutrition, 61: 3-21. doi: 10.1080/00380768.2015.1046136

Camargo, R.C.R., Oliveira, K.L. & Berto, M.I. (2017). Stingless bee honey: technical regulation proposal. Brazilian Journal of Food Technology, 20: 2-6. doi: 10.1590/1981-6723.15716

Davies, N.A., Hodson, M.E. & Black, S. (2003). Is the OECD acute worm toxicity test environmentally relevant? The effect of mineral form on calculated lead toxicity. Environmental Pollution, 121: 49-54. doi: 10.1016/S0269-7491(02)00206-3

Di, N., Hladun, K.R., Zhang, K., Liu, T.X. & Trumble, J.T. (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

Erdtman, G. (1960). The acetolysis method. A revised description. Svensk Botanisk Tidskrift, 54: 561-564

Hladun, K.R., Parker, D.R. & Trumble, J.T. (2015). Cadmium, copper, and lead accumulation and bioconcentration in the vegetative and reproductive organs of Raphanus sativus: implications for plant performance and pollination. Journal of Chemical Ecology, 41: 386-395. doi: 10.1007/s10886-015-0569-7

Jones, G.D. & Bryant Jr., V.M. (2004). The use of ETOH for the dilution of honey. Grana, 43: 174-182. doi: 10.1080/00173130410019497

Louveaux, J., Maurizio, A. & Vorwohl, G. (1978). Methods of Melissopalynology. Bee World, 59: 139 -157. doi:10.1080/0005772X.1978.11097714

Malavolta, E., Vitti, G.C. & Oliveira, S.A. (1989). Avaliação do estado nutricional das plantas: princípios e aplicações. Piracicaba: Potafos, 319 p

Malavolta, E. (1994). Fertilizantes e seu impacto ambiental: micronutrientes e metais pesados, mitos, mistifi cações e fatos. São Paulo: ProduQuímica, 153 p

Matin, G., Kargar, N. & Buyukisik, H.B. (2016). Biomonitoring 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

Mercosur. (2011). GMC/RES. nº 012/2011. Regulamento técnico Mercosul sobre limites máximos de contaminantes inorgânicos em alimentos. LXXXIV GMC (Grupo Mercado Comum). http://www.puntofocal.gov.ar/doc/r_gmc_12-11.pdf. (accessed date: 2 March, 2017)

Morgano, M.A., Teixeira Martins, M.C., Rabonato, L.C., Milani, R.F., Yotsuyanagi, K. & Rodriguez-Amaya, D.B. (2010). Inorganic contaminants in bee pollen from southeastern Brazil. Journal of Agricultural and Food Chemistry, 58, 6876-6883. doi: 10.1021/jf100433p

Naccari, C., Macaluso, A., Giangrosso, G., Naccari, F. & Ferrantelli, V. (2014). Risk assessment of heavy metals and pesticides in honey from Sicily (Italy). Journal of Food Research, 3: 107-117. doi: 10.5539/jfr.v3n2p107

Nascimento, A.S., Marchini, L.C., Carvalho, C.A.L., Araújo, D.F.D., Silveira, T.A. & Olinda, R.A. (2015). Determining the levels of trace elements Cd, Cu, Pb and Zn in honey of stingless bee (Hymenoptera: Apidae) using voltammetry. Food and Nutrition Sciences, 6: 591-596. doi: 10.4236/fns.2015.67062

Oroian, M., Prisacaru, A., Hretcanu, E.C., Stroe, S.G., Leahu, A. & Buculei, A. (2016) Heavy Metals profi le in honey as a potential indicator of botanical and geographical origin. International Journal of Food Properties, 19:1825-1836. doi: 10.1080/10942912.2015.1107578

Perugini, M., Manera, M., Grotta, L., Abete, M.C., Tarasco, R. & Amorena, M. (2011). Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: honeybees as bioindicators. Biological Trace Element Research, 140:170-176. doi: 10.1007/s12011-010-8688-z

Pisani, A., Protano, G. & Riccobono, F. (2008). Minor and trace elements in different honey types produced in Siena County (Italy). Food Chemistry, 107: 1553-1560. doi: 10.1016/j.foodchem.2007.09.029

Pohl, P., Sergiel, I., Stecka, H. & Jamroz, P. (2012). Different aspects of the elemental analysis of honey by fl ame atomic absorption and emission spectrometry: a review. Food Analytical Methods, 5: 737-751. doi: 10.1007/s12161-011-9309-y

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: 63-70

Punt, W., Hoen, P.P., Blackmore, S., Nilsson, S. & LE Thomas, A. (2007). Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology, 143: 1-81. doi: 10.1016/j.revpalbo.2006.06.008

R Development Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/

Reynaud, A.C. (2014). Requerimiento de micronutrientes y oligoelementos. Revista Peruana de Ginecología y Obstetricia, 60: 161-170.

Roubik, D.W. & Moreno, J.E.P. (1991). Pollen and Spores of Barro Colorado Island. St. Louis: Monographs in Systematic Botany, 268 p

Ru, Q.M., Feng, Q. & He, J.Z. (2013). Risk assessment of heavy metals in honey consumed in Zhejiang province, southeastern China. Food Chemistry Toxicology, 53: 256-62. doi: 10.1016/j.fct.2012.12.015

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: 3977-3988. doi: 10.1007/s11356-012-0921-1

Silici, S., Uluozlu, O.D., Tuzen, M. & Soylak, M. (2008). Assessment of trace element levels in Rhododendron honeys of Black Sea Region, Turkey. Journal Hazardous Materials, 156: 612-8. doi: 10.1016/j.jhazmat.2007.12.065

Silici, S., Uluozlu, O.D., Tuzen, M. & Soylak, M. (2016). Honeybee and honey as monitors for heavy metal contamination near the thermal power plants in Mugla, Turkey. Toxicology and Industrial Health, 32: 507-516. doi: 10.1177/0748233713503393

Silva, L.T., Pinho, J.L. & Nurusman, H. (2014). Traffi c air pollution monitoring based on an air-water pollutants deposition device. International Journal of Environmental Science and Technology, 11: 2307-2318. doi: 10.1007/s13762-014-0625-9

Silveira, T.A., Araujo, D.F.D., Marchini, L.C., Moreti, A.C.C.C. & Olinda, R.A. (2013). Detection of metals by differential pulse anodic stripping voltammetry (DPASV) in pollen collected from a fragment of the atlantic forest in Piracicaba/SP. Ecotoxicology and Environmental Contamination, 8: 31-36. doi: 10.5132/eec.2013.02.005

Souza, L.A., Piotto, F.A., Nogueirol, R.C. & Azevedo, R.A. (2013). Use of non-hyperaccumulator plant species for the phytoextraction of heavy metals using chelating agents. Scientia Agricola, 70: 290-295. doi: 10.1590/S0103-90162013000400010

Stecka, H., Jedryczko, D., Welna, M. & Pohl, P. (2014). Determination of traces of copper and zinc in honeys by the solid phase extraction pre-concentration followed by the fl ame atomic absorption spectrometry detection. Environmental Monitoring and Assessment, 186: 6145-6155 doi: 10.1007/

s10661-014-3845-z

Steen, J.J.M. van der, Cornelissen, B., Blacquière, T., Pijnenburg, J. E.M.L. & Severijnen, M. (2016). Think regionally, act locally: metals in honeybee workers in the Netherlands (surveillance study 2008). Environmental Monitoring and Assessment, 188: 463. doi: 10.1007/s10661-016-5451-8

Vasconcellos, M.C., Pagliuso, D. & Sotomaior, V.S. (2012). Fitorremediação: Uma proposta de descontaminação do solo. Estudos de Biologia: Ambiente e Diversidade, 83: 261-267. doi: 10.7213/estud.biol.7338

Villas-Bôas, J. (2012). Manual tecnológico: Mel de abelhas sem ferrão. Brasília: ISPN, 96 p

WHO (World Health Organization). (1982). Toxicological evaluation of certain food additives. FAO/WHO Expert Committee on Food Additives. WHO Food Additives Series,

Geneva: World Health Organization.

WHO (World Health Organization). (1983). Toxicological evaluation of certain food additives and food contaminants. FAO/WHO Expert Committee on Food Additives. WHO Food Additives Series, 18. Geneva: World Health Organization.

WHO (World Health Organization). (1993). Evaluation of certain food additives and contaminants. WHO Technical Report Series, 837. Geneva: World Health Organization.

Zarić, N.M., Ilijević, K., Stanisavljević, L. & Gržetić, I. (2016). Metal concentrations around thermal power plants, rural and urban areas using honeybees (Apis mellifera L.) as bioindicators. International Journal of Environmental Science and Technology, 13: 413-422. doi: 10.1007/s13762-015-0895-x

Zhelyazkova, I. (2012). Honeybees – bioindicators for environmental quality. Bulgarian Journal of Agricultural Science, 18: 435-442




DOI: http://dx.doi.org/10.13102/sociobiology.v65i4.3394

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