Skip to main content
Log in

Essential and Potentially Toxic Elements from Brazilian Geopropolis Produced by the Stingless Bee Melipona quadrifasciata anthidioides Using ICP OES

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Melipona quadrifasciata anthidioides is a species of stingless bee popularly known in Brazil as “mandaçaia”. Products derived from bees for food and therapeutic uses, have stimulated the evaluation of the chemical composition of geopropolis. Concentrations of 24 essential and potentially toxic elements were determined in geopropolis samples, using a sequential optical emission spectrometer with inductively coupled plasma (ICP OES) after microwave-assisted acid digestion. Principal component analysis (PCA) and Hierarchical cluster analysis (HCA) were used to carry out an exploratory analysis of the samples. The following elements were quantified (in mg Kg−1): Al (320,414.40–36,911.1), As (<LoQ-4.37), Ba (38.36–211.11), Ca (672.38–94,527), Co (<LoQ-14.12), Cr (17.41–38.07), Cu (10.63–28.73), Fe (21,973.96–11,536.47), K (1974.38–9198.91), Mg (1961.17–7481.79), Mn (50.51–310.51), Na (154.55–340.46), Ni (2.28–21.74), P (16.59–51.07), Pb (3.45–8.55), Sb (<LoQ-1.64), Se (<LoQ-1.01), Sn (4.92–16.14), Sr (9.21–36.29), V (28.77–78.73) and Zn (24.34–50.31). Cd and Mo were found to be below the limit of detection (LoD) and quantification (LoQ) values of ICP OES in all investigated samples. Geopropolis can be a potential source of macro- and microelements for colonies and products derived from these bees for human consumption, contributing to their geographical origin and quality control, besides being an indicator of environmental monitoring.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Silva MD, Ramalho M, Monteiro D (2014) Communities of social bees (Apidae: Meliponini) in trap-nests: the spatial dynamics of reproduction in an area of Atlantic forest. Neotrop Entomol 43(4):307–313

    CAS  PubMed  Google Scholar 

  2. Kerr WE, Carvalho GA, Silva AC, Assis MGP (2001) Little-mentioned aspects of Amazonian biodiversity. Parc Estrat 6(12):20–41

    Google Scholar 

  3. Belsky J, Joshi NK (2019) Impact of biotic and abiotic stressors on managed and feral bees. Insects 10(233):1–42

    Google Scholar 

  4. Barth OM, Luz CFP (2003) Palynological analysis of Brazilian geopropolis sediments. Grana 42(2):121–127

    Google Scholar 

  5. Dutra RP, Bezerra JL, Silva MCP, Batista MCA, Patrício FJB, Nascimento FRF, Ribeiro MNS, Guerra RNM (2019) Antileishmanial activity and chemical composition from Brazilian geopropolis produced by stingless bee Melipona fasciculate. Rev Bras Farmacogn 29(3):287–293

    CAS  Google Scholar 

  6. Araújo MJAM, Búfalo MC, Conti BJ, Fernandes A Jr, Trusheva B, Bankova V, Sforcin JM (2015) The chemical composition and pharmacological activities of geopropolis produced by Melipona fasciculata smith in Northeast Brazil. J Mol Pathophysiol 4(1):12–20

    Google Scholar 

  7. Sanches MA, Pereira AMS, Serrão JE (2017) Pharmacological actions of extracts of propolis of stingless bees (Meliponini). J Apic Res 56(1):50–57

    Google Scholar 

  8. IOM (2006) Dietary reference intakes: the essential guide to nutrient requirements. Institute of Medicine of the National Academies. https://www.nal.usda.gov/sites/default/files/fnic_uploads/DRIEssentialGuideNutReq.pdf.

  9. Lavinas FC, Macedo EHBC, Sá GBL, Amaral ACF, Silva JRA, Azevedo MMB, Vieira BA, Domingos TFS, Vermelho AB, Carneiro CS, Rodrigues IA (2019) Brazilian stingless bee propolis and geopropolis: promising sources of biologically active compounds. Rev Bras Farmacogn 29(3):389–399

    CAS  Google Scholar 

  10. Brazil MAPA (2001) Normative Instruction No. 03 of January 19, 2001: Approves the technical regulations on identity and quality of Apitoxin, beeswax, Royal Jelly, lyophilized Royal Jelly, bee pollen, Propolis and Propolis Extract. Ministry of Agriculture, Livestock and Supply. http://extranet.agricultura.gov.br/sislegis-consulta/consultarLegislacao.do?operacao=visualizar&id=1798.

  11. Spirić D, Ćirić J, Đorđević V, Nikolić D, Janković S, Nikolić A, Petrović Z, Katanić N, Teodorović V (2019) Toxic and essential element concentrations in different honey types. Int J Environ An Ch 99(5):474–485

    Google Scholar 

  12. Ćirić J, Spirić D, Baltić T, Lazić IB, Trbović D, Parunović N, Petronijević R (2020) Đorđević V (2020) honey bees and their products as indicators of environmental element deposition. Biol Trace Elem Res. https://doi.org/10.1007/s12011-020-02321-6

  13. Bonsucesso JS, Gloaguen TV, Nascimento AS, Carvalho CAL, Dias FS (2018) Metals in geopropolis from beehive of Melipona scutellaris in urban environments. Sci Total Environ 634:687–694

    CAS  PubMed  Google Scholar 

  14. Ferreira BL, Gonzaga LV, Vitali L, Micke GA, Maltez HF, Ressureição C, Costa ACO, Fett R (2019) Southern-Brazilian geopropolis: a potential source of polyphenolic compounds and assessment of mineral composition. Food Res Int 126:108683

    CAS  PubMed  Google Scholar 

  15. Ferreira BL, Gonzaga LV, Vitali L, Micke GA, Baggio D, Costa ACO, Fett R (2020) Dataset about southern-Brazilian geopropolis: physical and chemical perspectives. Data Brief 29:105–109

    Google Scholar 

  16. Silici S, Uluozlu OD, Tuzen M, Soylak M (2016) Honeybee and honey as monitors for heavy metal contamination near the thermal power plants in Mugla, Turkey. Toxicol Ind Health 32(3):507–516

    CAS  PubMed  Google Scholar 

  17. Ćirić J, Đorđević V, Trbović D, Baltić T, Lazić IB, Matović K, Janković S, Parunović N (2020) Risk assessment of toxic elements in acacia honey. Meat Technology 61(1):70–74

    Google Scholar 

  18. Vojtíšek M, Patková J, Knotková J, Kašparová L, Hornychová M, Frantík E, Formánek J, Svandová E (2008) Metals – impact and implications. Interdiscip Toxicol 1(2):198–199

    PubMed  PubMed Central  Google Scholar 

  19. Santos Júnior AF, Matos RA, Andrade EMJ, dos Santos WNL, Magalhães HIF, Costa FN, Korn MGA (2017) Multielement determination of macro and micro contents in medicinal plants and Phytomedicines from Brazil by ICP OES. J Braz Chem Soc 28(2):376–384

    Google Scholar 

  20. Oliveira SS, Alves CN, Boa Morte ES, Santos Júnior AF, Araujo RGO, Santos DCMB (2019) Determination of essential and potentially toxic elements and their estimation of bioaccessibility in honeys. Microchem J 151:104221

    CAS  Google Scholar 

  21. Migdał P, Roman A, Popiela-Pleban E, Kowalska-Góralska M, Opaliński S (2018) The impact of selected pesticides on honey bees. Pol J Environ Stud 27(2):787–792

    Google Scholar 

  22. Sant'ana RS, Carvalho CAL, Oda-Souza M, Souza BA, Dias FS (2020) Characterization of honey of stingless bees from the Brazilian semi-arid region. Food Chem 327:127041

    Google Scholar 

  23. Tannus CA, Dias FS, Santana FB, Santos DCMB, Magalhães HIF, Dias FS, Santos Júnior AF (2020) Multielement determination in medicinal plants and herbal medicines containing Cynara scolymus L., Harpagophytum procumbens D.C., and Maytenus ilifolia (Mart.) ex Reiss from Brazil using ICP OES. Biol trace Elem res (2020). https://doi.org/10.1007/s12011-020-02334-1

  24. Korn MGA, Guida MAB, Barbosa JTP, Torres EA, Fernandes AP, Santos JCC, Dantas KGF, Nóbrega JA (2013) Evaluation of sample preparation procedures for trace element determination in brazilian propolis by inductively coupled plasma optical emission spectrometry and their discrimination according to geographic region. Food Anal Methods 6(3):872–880

    Google Scholar 

  25. Tuzen M, Soylak M (2005) Trace heavy metal levels in microwave digested honey samples from middle Anatolia, Turkey. J Food Drug Anal 13(4):343–347

    CAS  Google Scholar 

  26. Trevizan LC, Nóbrega JA (2007) Inductively coupled plasma optical emission spectrometry with axially viewed configuration: an overview of applications. J Braz Chem Soc 18(4):678–690

    CAS  Google Scholar 

  27. Novaes CG, Bezerra MA, da Silva EGP, dos Santos AMP, Romão ILS, Santos Neto JH (2016) A review of multivariate designs applied to the optimization of methods based on inductively coupled plasma optical emission spectrometry (ICP OES). Microchem J 128:331–346

    CAS  Google Scholar 

  28. Gouveia ST, Silva FV, Costa LM, Nogueira ARA, Nóbrega JA (2001) Determination of residual carbon by inductively-coupled plasma optical emission spectrometry with axial and radial view configurations. Anal Chim Acta 445:269–275

    CAS  Google Scholar 

  29. ICH (2005) Validation of analytical procedures: text and methodology Q2 (R1). International Conference on Harmonisation. https://www.gmp-compliance.org/guidemgr/files/Q2(R1).pdf.

  30. Canale A, Cosci F, Canovai R, Giannotti P, Benelli G (2014) Foreign matter contaminating ethanolic extract of propolis: a filth-test survey comparing products from small beekeeping farms and industrial producers. Food Addit Contam Part A 31(12):2022–2025

    CAS  Google Scholar 

  31. Krewski D, Yokel RA, Nieboer E, Borchelt D, Cohen J, Harry J, Kacew S, Lindsay J, Mahfouz AM, Rondeau V (2007) Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide. J Toxicol Environ Health B Crit Rev 10(1):1–269

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Exley C (2013) Human exposure to aluminium. Environ Sci: Processes Impacts 15(10):1807–1816

    CAS  Google Scholar 

  33. Finger D, Filho IK, Torres YR, Quináia SP (2014) Propolis as an indicator of environmental contamination by metals. Bull Environ Contam Toxicol 92(3):259–264

    CAS  PubMed  Google Scholar 

  34. Bonvehí JS, Bermejo FJO (2013) Element content of propolis collected from different areas of South Spain. Environ Monit Assess 185(7):6035–6047

    PubMed  Google Scholar 

  35. Abbaspour N, Hurrell R, Kelishadi R (2014) Review on iron and its importance for human health. J Res Med Sci 19(2):164–174

    PubMed  PubMed Central  Google Scholar 

  36. Cvek J, Medić-Šarić M, Vitali D, Vedrina-Dragojević I, Šmit Z, Tomić S (2008) The content of essential and toxic elements in Croatian propolis samples and their tinctures. J Apicult Res 47(1):35–45

    CAS  Google Scholar 

  37. Moe SM (2008) Disorders involving calcium, phosphorus, and magnesium. Prim Care 35(2):215–2vi

    PubMed  PubMed Central  Google Scholar 

  38. Schwalfenber GK, Genuis SJ (2017) The importance of magnesium in clinical healthcare. Scientifica (Cairo) 2017:4179326

    Google Scholar 

  39. Strazzullo P, Leclercq C (2014) Sodium. Adv Nutr 5(2):188–190

    PubMed  PubMed Central  Google Scholar 

  40. Souza EA, Zaluski R, Veiga N, Orsi RO (2016) Effects of seasonal variations and collection methods on the mineral composition of propolis from Apis mellifera Linnaeus beehives. Braz J Biol 76(2):396–401

    CAS  PubMed  Google Scholar 

  41. Perugini M, Manera M, Grotta L, Abete MC, Tarasco R, Amorena M (2011) Heavy metal (hg, Cr, cd, and Pb) contamination in urban areas and wildlife reserves: honeybees as bioindicators. Biol Trace Elem Res 140(2):170–176

    CAS  PubMed  Google Scholar 

  42. Bogdanov S (2006) Contaminants of bee products. Apidologie 37(1):1–18

    CAS  Google Scholar 

  43. Souza MLP, Andreoli CV, Amaral MB, Domaszak SC (1996) Preliminary survey of heavy metals in some soils in Paraná. Rev Sanare 5(5):68–75

    Google Scholar 

  44. Moreira RCA, Boaventura GR (2003) Regional geochemical reference for the interpretation of the concentrations of chemical elements in the sediments of the Lago Paranoá-DF basin. Quím Nova 26(6):812–820

    CAS  Google Scholar 

  45. Carvalho SRL, Vilas-Boas GS, Fadigas FS (2010) Estimate of the concentration of heavy metals in soils of tables of Bahia's Reconcavo. Cad Geoc 7(1):1–11

    Google Scholar 

  46. Paustenbach DJ, Tvermoes BE, Unice KM, Finley BL, Kerger BD (2013) A review of the health hazards posed by cobalt. Crit Rev Toxicol 43(4):316–362

    CAS  PubMed  Google Scholar 

  47. Hamilton EI (2000) Environmental variables in a holistic evaluation of land contaminated by historic mine wastes: a study of multi-element mine wastes in West Devon, England using arsenic as an element of potential concern to human health. Sci Total Environ 249(1–3):171–221

    CAS  PubMed  Google Scholar 

  48. Zaborowska M, Kucharski J, Wyszkowska J (2016) Biological activity of soil contaminated with cobalt, tin, and molybdenum. Environ Monit Assess 188(7):398

    PubMed  PubMed Central  Google Scholar 

  49. Pyrzyńska K (2007) Determination of molybdenum in environmental samples. Anal Chim Acta 590(1):40–48

    PubMed  Google Scholar 

  50. Mendel R, Bittner F (2006) Cell biology of molybdenum. Biochim Biophys Acta 1763(7):621–635

    CAS  PubMed  Google Scholar 

  51. Nielsen FH (2012) History of zinc in agriculture. Adv Nutr 3(6):783–789

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Brazil MS (2005) Resolution of Collegiate Board No. 269 of September 22, 2005: Technical regulation on daily ingestion recommended (DIR) protein, vitamins and minerals. Ministry of Health. http://portal.anvisa.gov.br/documents/33916/394219/RDC_269_2005.pdf/2e95553c-a482-45c3-bdd1-f96162d607b3.

  53. Roohani N, Hurrell R, Kelishadi R, Schulin R (2013) Zinc and its importance for human health: an integrative review. J Res Med Sci 18(2):144–157

    PubMed  PubMed Central  Google Scholar 

  54. Cantarelli MA, Camiña JM, Pettenati EM, Marchevsky EJ, Pellerano RG (2011) Trace mineral content of Argentinean raw propolis by neutron activation analysis (NAA): assessment of geographical provenance by chemometrics. Food Sci Technol 44(1):256–260

    CAS  Google Scholar 

  55. Rayman MP (2000) The importance of selenium to human health. Lancet 356(9225):233–241

    CAS  PubMed  Google Scholar 

  56. Ramkissoon C, Degryse F, Silva RC, Baird R, Young SD, Bailey EH, McLaughlin MJ (2019) Improving the efficacy of selenium fertilizers for wheat biofortification. Sci Rep 9:19520

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Treviño S, Díaz A, Sánchez-Lara E, Sanchez-Gaytan BL, Perez-Aguilar JM, González-Vergara E (2019) Vanadium in biological action: chemical, pharmacological aspects, and metabolic implications in diabetes mellitus. Biol Trace Elem Res 188(1):68–98

    PubMed  Google Scholar 

  58. Barceloux DG, Barceloux D (1999) Vanadium. J Toxicol Clin Toxicol 37(2):265–278

    CAS  PubMed  Google Scholar 

  59. Genuis SJ, Bouchard TP (2012) Combination of micronutrients for bone (COMB) study: bone density after micronutrient intervention. J Environ Public Health 2012:354151

    PubMed  PubMed Central  Google Scholar 

  60. D’Amore JJ, Al-Abed SR, Scheckel KG, Ryan JA (2005) Methods for speciation of metals in soils: a review. J Environ Qual 34(5):1707–1745

    PubMed  Google Scholar 

  61. Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol 2011:402647

    Google Scholar 

  62. Echevarria G, Massoura ST, Sterckeman T, Becquer T, Schwartz C, Morel JL (2006) Assessment and control of the bioavailability of nickel in soils. Environ Toxicol Chem 25(3):643–651

    CAS  PubMed  Google Scholar 

  63. Lewińska K, Karczewska A (2019) Antimony in soils of SW Poland – an overview of potentially enriched sites. Environ Monit Assess 191(2):70

    PubMed  PubMed Central  Google Scholar 

  64. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metals toxicity and the environment. EXS 101:133–164

    PubMed  PubMed Central  Google Scholar 

  65. Popov BB, Hristova VK, Presilski S, Shariati MA, Najman S (2017) Assessment of heavy metals in propolis and soil from the pelagonia region, republic of Macedonia, Maced. J Chem Chem Eng 36(1):23–33

    CAS  Google Scholar 

  66. Franchin M, Cunha MG, Denny C, Napimoga MH, Cunha TM, Koo H, Alencar SM, Ikegaki M, Rosalen PL (2012) Geopropolis from Melipona scutellaris decreases the mechanical inflammatory hypernociception by inhibiting the production of IL and TNF. J Ethnopharmacol 143(2):709–715

    CAS  PubMed  Google Scholar 

  67. Roman A, Madras-Majewska B, Popiela-Pleban E (2011) Comparative study of selected toxic elements in propolis and honey. J Apic Sci 55(2):97–106

    Google Scholar 

  68. Santos Júnior AF, Brandão GC, Santos Júnior MC, Santos FAR, Magalhães HIF, Korn MGA (2020) Multi-element composition, physicochemical and pollen attributes of honeys from the Paraguaçu River (Bahia, Brazil) by inductively coupled plasma-optical emission spectrometry (ICP OES). An Acad Bras Cienc 92(3):e20181196

    PubMed  Google Scholar 

  69. Hodel KVS, Machado BAS, Santos NR, Costa RG, Menezes-Filho JA, Umsza-Guez MA (2020) Metal content of nutritional and toxic value in different types of brazilian propolis. Sci World J 2020:4395496

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to the following Brazilian agencies: Bahia State Research Support Foundation (FAPESB), Brazilian National Council for Scientific and Technological Development (CNPq) and “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES)”, and Research Group: Biopharmaceutics and Drugs.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aníbal de Freitas Santos Júnior.

Ethics declarations

Conflict of Interest

The authors declare that have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Cruz Ferreira, R., de Souza Dias, F., de Aragão Tannus, C. et al. Essential and Potentially Toxic Elements from Brazilian Geopropolis Produced by the Stingless Bee Melipona quadrifasciata anthidioides Using ICP OES. Biol Trace Elem Res 199, 3527–3539 (2021). https://doi.org/10.1007/s12011-020-02455-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-020-02455-7

Keywords

Navigation