Pollen storage by stingless bees as an environmental marker for metal contamination: spatial and temporal distribution of metal elements

Authors

  • Nathalia De Oliveira Nascimento Universidade Federal de Ouro Preto
  • Herminio Arias Nalini Junior Universidade Federal de Ouro Preto
  • Fernanda Ataide Universidade Federal de Ouro Preto
  • Adriana Tropia Abreu Universidade Federal de Ouro Preto
  • Yasmine Antonini Universidade Federal de Ouro Preto http://orcid.org/0000-0002-5582-8193

DOI:

https://doi.org/10.13102/sociobiology.v65i2.2078

Keywords:

Bee, Pollen, suspended particulate material, mining activities, Iron Quadrangle.

Abstract

Since the middle of the 20th century, human activities have led to overall ecosystem contamination and to major modifications in landscape structure and composition. Mining activities represent a major source of environmental contamination by metal residues. The objective of our study was to evaluate the presence of heavy metals and other elements on stingless bee pollen, and compare them to samples of Suspended Particulate Material (SPM) in five points a Mineral Province, in Brazil. More than 50 elements were identified by ICP-OES and ICP-MS, after microwave digestion. Overall, we found a strong relation among elements present on pollen and SPM. Samples from the four areas exhibited higher levels of minerals compared to the reference site. Mineral levels varied widely within the two seasonal periods. Some elements, like Pb, Cd, As, Cu, Zn, and Fe were found at levels considered potentially toxic to human health. Pollen stored by stingless bees was a successful bioindicator, and demonstrated the value of quantitative ecological information for detecting air pollution.

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Author Biographies

Nathalia De Oliveira Nascimento, Universidade Federal de Ouro Preto

Laboratorio de Biodiversidade - DEBIO- ICEB

Herminio Arias Nalini Junior, Universidade Federal de Ouro Preto

Laboratório de Geoquímica Ambiental - Departamento de Geologia - UFOP

Fernanda Ataide, Universidade Federal de Ouro Preto

Laboratório de Geoquímica Ambiental - Departamento de Geologia - UFOP

Adriana Tropia Abreu, Universidade Federal de Ouro Preto

Laboratório de Geoquímica Ambiental - Departamento de Geologia - UFOP

Yasmine Antonini, Universidade Federal de Ouro Preto

Laboratorio de Biodiversidade - DEBIO- ICEB

References

ANVISA - Agência Nacional de Vigilância Sanitária; Brazilian Ministry of Health. (1998). Portaria N. 27, 13 de Janeiro de 1998: Informação Nutricional Complementar, Brasília, DF, Brasil.

Azevedo, U.R., Machado, M.M.M., Castro, P.T.A., Renger, F.E., Trevisol, A. & Beato, D.A.C. (2012). Geoparque Quadrilátero Ferrífero (MG) – proposta. In: Schobbenhaus, C. & Silva, C.R. (org). Geoparques do Brasil.CPRM – Serviço Geológico do Brasil.

Azimi, S., Ludwig, A., Théev Venot, D.R. & Colin, J.L. (2003). Trace metal determination in total atmospheric deposition in rural and urban areas. The Science of the Total Environment, 308: 247-256.

Baêta, H.E. (2012). Contribuição da deposição úmida (chuva e neblina) nas relações hídricas e nutricionais de fisionomias de campos ferruginosos na Serra da Brígida, ouro preto, MG. Dissertação (Mestrado) – Instituto de Ciências Exatas e Biológicas, Universidade Federal de Ouro Preto, Minas Gerais

Bilandžić, N., OkicÅL, M., Sedak, M., KolanovicÅL, B.S., Varenina, I., Koncˇurat, A.& Rudan, N.(2011). Determination of trace elements in Croatian floral honey originating from different regions. Food Chemistry, 128: 1160-1164. doi: 10. 1016/j.foodchem.2011.04.023

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

Bratu, I. & Beorgescu, C. (2005). Chemical contamination of bee honey – identifying sensor of the environment pollution. Journal of Central European Agriculture. 6: 95-98.

Caroli, S., Forte, G., Iamiceli, A.L. & Galoppi, B. (1999). Determination of essential and potentially toxic trace elements in honey by inductively coupled plasma-based techniques Talanta, 50: 327-336.

Carvalho-Filho, A., Curi, N. & Shinzato, E. (2010). Relações solo‑paisagem no Quadrilátero Ferrífero em Minas Gerais. Pesquisa Agropecuária Brasileira, 45: 903-916.

Chauzat, M.P., Martel, A.C., Cougoule, N., Porta, P., Lachaize, J., Zeggane, S., et al. (2011). An assessment of honeybee colony matrices, Apis melifera (Hymenoptera: Apidae) to monitor pesticide presence in continental France. Environmental Toxicology and Chemistry, 30: 103-111. doi: 10.1002/etc.361

Costa, R.V.F., Matschullat, J., Garcia, M.L., Nalini-Junior, H.A. & Mendonça, F.P.C. (2015). Iron Quadrangle stream sediments, Brazil: geochemical maps and reference values. Environ Earth Science, 74: 4407-4417.

CPRM. Serviço geológico do Brasil. (2014). Secretaria de geologia, mineração e transformação mineral – Ministério de Minas e Energia. Brasil.

D’Ambrosio, M. & Marchesini, A. (1982). Heavy metal contamination of honey. Atti Societá Italiana Scienze Naturali, 123: 342-348.

FAO (1998). World reference base for soil resources. World Soil Resources Report 84, FAO/ISRIC/ISSS, Rome.

Figueiredo, B.R., Gabriod, T. & Schwenkd, M. (2000). Human and environmental contamination in the Iron Quadrangle, Brazil. Applied Geochemistry, 15: 181-190.

Formick, 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 Environmental Study, 22: 99-106.

Freedman, B. & Hutchinson, T. (1981). Source of metal and contamination of terrestrial environments. Pp35-94. In. Leep, N. W. Leep (ed). Effect of heavy metal pollution on plants. Applied Science Publishers, London, 35-94.

Gajek, O., Gdanski, M. & Gajewska, R. (1987). Metallic impurities in imported canned fruit and vegetables and bee honey. Roczniki Panstwowego Zakladu Higieny, 38:14-20.

Hewett, P. & Ganser, G.H. (2007). A Comparison of Several Methods for Analyzing Censored Data. The Annals of Occupational Hygiene, 51: 611-632.

Lambert, O., Puyo, M.P.S., Thorin, C., Larhantec, M. & Pouliquen, F.D.H. (2012). Bees, honey and pollen as sentinels for lead environmental contamination. Environmental Pollution, 170: 254-259. doi: 10.1016/j.envpol.2012.07.012

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 Assessment, 43: 1-9.

Magalhães, M. (2007). Mel e pólen de Apis mellifera como bioindicador de poluição ambiental por metais pesados. Dissertação de Mestrado. Universidade Federal de Ouro Preto, MG, Brazil, pp.66.

Matei, N., Birghila, S., Dobrinas, S. & Capota, P. (2004). Determination of C Vitamin and some Essential Trace Elements (Ni, Mn, Fe, Cr) in Bee Products. Acta Chimica Slovenica, 51: 169-175.

Matina, G., Kargarb, N. & Buyukisika, 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

McGeoch, M.A. (2007). Insects andbioindication: Theory and progress. In: Stewart, A.J.A., New, T.R., & Lewis, O.T. (Eds), Insect conservation biology: Proceedings of the Royal Entomological Society, CABI, Wallingford, Oxfordshire, pp. 144-174.

Meneses, I., Renger, F.E. & Deschamps, E. (2011). History and socioeconomy of Iron Quadrangle. In: Deschamps, E., Matschullat, J. (eds). Arsenic: natural and anthropogenic. Arsenic in the environment, pp 73–80, CRC Press London.

Mermet, J.M. & Poussel, E. (1995). ICP Emission Spectrometers: 1995 Analytical Figures of Merit. Applied Spectroscopy, 49: 12A-18A.

Messias, M.C.T.B., Leite, M.G.P., Meira Neto, J.A.A., Kozovits, A.R. & Tavares, R. (2013). Soil-Vegetation Relationship in Quartzitic and Ferruginous Brazilian Rocky Outcrops. Folia Geobotanica, 48: 509-521. doi: 10.1007/s12224-013-9154-4

Miller, J.N. & Miller, J.C. (2005). Statistics and Chemometrics for Analytical Chemistry, Pearson Education, Harlow.

Minussi, L.C. & Alves-Dos-Santos, I. (2007). Abelhas nativas versus Apis mellifera, Linnaeus, espécie exótica (Hymenoptera: Apidae). Bioscience Journal, 23: 58-62.

Morgano, M.A., Martins, M.C.T., Rabonato, L.C., Milani, R.F., Yotsuyanagi, K. & Rodriguez-Amaya, D.B. (2012). A Comprehensive Investigation of the Mineral Composition of Brazilian Bee Pollen: Geographic and Seasonal Variations and Contribution to Human Diet. Journal of Brazilian Chemical Society, 23: 727-736.

Nogueira-Neto, P. (1997).Vida e criação de abelhas indígenas sem ferrão. São Paulo: Nogueirapis, pp.445

Oliveira, F.A., Abreu, A.T., Oliveira Nascimento, N.O., Froes-Silva, R.E., Antonini, Y., Nalini-Júnior, H.A. Jr. & Lena, J.C.(2017). Evaluation of matrix effect on the determination of rare earth elements and As, Bi, Cd, Pb, Se and In in honey and pollen of native Brazilian bees (Tetragonisca angustula - Jataí) by Q-ICP-MS. Talanta, 162C: 488-494. doi: 10.1016/j.talanta.2016.10.058

Pereira, J.C., Guimarães-Silva, A. K., Nalini-Júnior, H.A., Pacheco-Silva E. & Lena, J.C. (2007). Distribuição, fracionamento e mobilidade de elementos traço em sedimentos superficiais. Química Nova, 30: 1249-1255.

Perugini, M., Manera, M., Grotta, L., Abete, M.C., Tarasco, R. & Amorena, M. (2011). Heavy metals (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

Pohl, P. (2009). Determination of metal content in honey by atomic absorption and emission spectrometries. Trends in Analytical Chemistry. 28: 117-128.

R language and environment for statistical computing (2010). RFoundation for statistical computing. Vienna, Austria.

Rapini, A., Ribeiro, P.L., Lambert, S. & Pirani, J.R. (2008). A flora dos campos rupestres da Cadeia do Espinhaço. Mega-diversidade, 4: 15-23.

Ribeiro, S.P., Londe, V., Bueno, A.P., Barbosa, J.S., Corrêa, T.L., Soeltl, T., Maia, M., Pinto V.D., Dueli, G.F. Sousa, H.C.D., Kozovits, A. R. & Nalini Jr, H.A. (2016). Plant defense against leaf herbivory based on metal accumulation: examples from a tropical high altitude ecosystem. Plant Species Biology, 32: 147-155. doi: 10.1111/1442-1984.12136

Schaefer, C.E., Cândido, H.G., Corrêa, G.R., Nunes, J.A & Arruda, D.M. (2016). Soils Associated with Rupestrian Grasslands. In: Fernandes, G. W. (Ed.), Ecology and Conservation of Mountaintop grasslands in Brazil (pp. 55-69). Springer International Publishing. doi: 10.1007/978-3-319-29808-5.

Silveira, F.A.O., Negreiros, D., Barbosa, N.P.U., Buisson, E., Carmo, F.F., Carstensen, D.W., Conceição, A.A., Cornelissen, T.G., Echternacht ,L., Fernandes, G.W., Garcia, Q.S., Guerra, T.J., Jacobi, C.M., Lemos-Filho, J.P., Le Stradic, S., Morellato, L.P.C., Neves, F.S., Oliveira, R.S., Schaefer, C.E., Viana, P.L. & Lambers, L. (2016). Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant and Soil, 403: 129-152. doi: 10.1007/s11104-015-2637-8

USDA. (1998). Keys to soil taxonomy. United States Department of Agriculture, New York.

Valim, E.A.R. (2012). Ciclagem de nutrientes no sistema atmosfera-solo-planta em formação campestre e florestal sobre canga em Minas Gerais. Dissertação (Mestrado) - Instituto de Ciências Exatas e Biológicas, Universidade Federal de Ouro Preto, Minas Gerais

Vinas, P., Pardo-Martinez, M. & Hernandez-Cordoba, M. (2000). Rapid determination of selenium, lead, and cadmium in baby food samples using electrothermal atomic absorption spectrometry and slurry atomization. Analytica Chimica Acta, 412: 121-130.

Wayne, L. (1983). Bee miners join British Columbia God Hunt. American Bee Journal, 3: 635-637.

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Published

2018-07-09

How to Cite

Nascimento, N. D. O., Nalini Junior, H. A., Ataide, F., Abreu, A. T., & Antonini, Y. (2018). Pollen storage by stingless bees as an environmental marker for metal contamination: spatial and temporal distribution of metal elements. Sociobiology, 65(2), 259–270. https://doi.org/10.13102/sociobiology.v65i2.2078

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Section

Research Article - Bees

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