Chemical Characterization and Bioactivity of Tetragonisca angustula Pot-Pollen from Mérida, Venezuela

  • Patricia VitEmail author
  • Bertha Santiago
  • María Peña-Vera
  • Elizabeth Pérez-Pérez


Norms for commercial and nutritional standards of pollen collected by stingless bees and used in human nutrition are currently lacking. Six samples of Tetragonisca angustula fresh pot-pollen from two locations in Mérida were characterized for macronutrients (moisture, ash, protein, fat, carbohydrates). The flavonoid, polyphenol, and protein contents were studied in ethanolic extracts of pot-pollen, as well as the antioxidant activity measured by three methods. Percentages of 23.34–24.69 g water, 2.06–2.13 g ash, 22.43–22.97 g protein, 4.42–4.58 g fat, and 45.98–46.68 g carbohydrates characterized 100 g of pot-pollen from Tetragonisca angustula. Polyphenol concentrations of 1.053.1–2.627.4 mg gallic acid equivalents, flavonoid contents of 104.6–676.4 mg quercetin equivalents, and protein concentrations of 118.9–811.4 mg per 100 g pot-pollen occurred in ethanolic extracts. The antioxidant activity of the ethanolic extract varied in each method. The hydroxyl radical inhibition percentage was 30.0–60.1% inhibition, the antioxidant activity was 0.74–1.12 mM uric acid equivalent, and the total antioxidant activity was 401.8–500.4 μmoles Trolox equivalents each per 100 g pot-pollen. Positive correlations between antioxidant activity and total polyphenol content (0.802–0.921) were found. This nutritional, biochemical, and bioactive assessment of Tetragonisca angustula pot-pollen can help to establish their norms and methodological examination.



Project FA-592-16-08-B and CVI-FA-04-97 from Consejo de Desarrollo Científico, Humanístico, Tecnológico y de las Artes at Universidad de Los Andes, Mérida, Venezuela. The Secretariat of the Universidad de Los Andes and Schullo Products from Ecuador supported the participation in the Congress APICENS, Okinawa, Japan, in 2016 with some of the results in this chapter. To comments of reviewers and Dr. DW Roubik for valued English editing.


  1. Aličić D, Šubarić D, Jašić M, Pašalic H, Ačkar D. 2014. Antioxidant properties of pollen. Food in Health and Disease: Scientific-Professional Journal of Nutrition and Dietetics 3: 6-12.Google Scholar
  2. Almaraz-Abarca N, Campos MG, Avila-Reyes JA, Naranjo-Jimenez N, Herrera Corral J, Gonzalez-Valdez LS. 2004. Variability of antioxidant activity among honeybee-collected pollen of different botanical origin. Interciencia 29: 574-578.Google Scholar
  3. AOAC. 1999. Official Methods of Analysis. 15th ed. Association of Official Analytical Chemists; Arlington, VA, USA. 1093 pp.Google Scholar
  4. Bárbara MS, Machado CS, Sodré Gda S, Dias LG, Estevinho LM, de Carvalho CA. 2015. Microbiological assessment, nutritional characterization and phenolic compounds of bee pollen from Melipona mandacaia Smith, 1983. Molecules 20: 12525-12544.CrossRefPubMedGoogle Scholar
  5. Barrientos L, Herrera CL, Montenegro G, Ortega X, Veloz J, Alvear M, Cuevas A, Saavedra N, Salazar LA. 2013. Chemical and botanical characterization of Chilean propolis and biological activity on cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus. Brazilian Journal of Microbiology 44: 577-585.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Camargo JMF, Pedro SRM. 2013. Meliponini Lepeletier, 1836. In Moure JS, Urban D, Melo GAR, orgs. Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical Region. On-line version. Available at: Accessed the 25.01.2017.
  7. Campos MG, Webby RF, Markham KR, Mitchell KA, Cunha AP. 2003. Age-Induced Diminution of free radical scavening capacity in bee pollens and the contribution of Consistent flavonoids. Journal of Agricultural and Food Chemistry 51: 742-745.CrossRefPubMedGoogle Scholar
  8. Carpes ST, Mourao GB, Alencar SM, Masson ML. 2009. Chemical composition and free radical scavenging activity of Apis mellifera bee pollen from Southern Brazil. Brazilian Journal of Food Technology 12: 220-229.CrossRefGoogle Scholar
  9. Carvalho CAL and Marchini LC. 1999. Tipos polínicos coletados por Nannotrigona testaceicornis e Tetragonisca angustula (Hymenoptera, Apidae, Meliponinae). Sciencia Agricola 56: 717-722.CrossRefGoogle Scholar
  10. Cortopassi-Laurino M, Ramalho M. 1988. Pollen harvest by Africanized Apis mellifera and Trigona spinipes in São Paulo. Botanical and ecological views. Apidologie 19: 1-24.CrossRefGoogle Scholar
  11. Estevinho LM, Rodrigues S, Pereira AP, Feás X. 2012. Portuguese bee pollen: palynological study, nutritional and microbiological evaluation. International Journal of Food Science and Technology 47: 429-435.CrossRefGoogle Scholar
  12. Feás X, Vázquez-Tato MP, Estevinho L, Seijas JA, Iglesias A. 2012. Organic bee pollen: botanical origin, nutritional value, bioactive compounds, antioxidant activity and microbiological quality. Molecules 17: 8359-8377.CrossRefPubMedGoogle Scholar
  13. Graikou K, Kapeta S, Aligiannis N, Sotiroudis G, Chondrogianni N, Gonos E, Chinou I. 2011. Chemical analysis of Greek pollen - Antioxidant, antimicrobial and proteasome activation properties Chemistry Central Journal 5: 33-42.Google Scholar
  14. Halliwell B, Gutteridge J, Aruoma O. 1987. The deoxyribose method:a simple test-tube assay for determination of rate constants for reactions of hydroxyl radicals. Analytical Biochemistry 165: 215–219.CrossRefPubMedGoogle Scholar
  15. Human H, Nicolson SW. 2006. Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry 67: 1486-1492.CrossRefPubMedGoogle Scholar
  16. Koracevic D, Koracevic G, Djordjevic V, Andrejevic S, Cosic V. 2001. Method for measurement of antioxidant activity in human fluids. Journal of Clinical Patholology 54: 356–361.CrossRefGoogle Scholar
  17. Kustiawan PM, Puthong S, Arung ET, Chanchao C. 2014. In vitro cytotoxicity of Indonesian stingless bee products against human cancer cell lines. Asian Pacific Journal of Tropical Biomedicine 4: 549-556.CrossRefPubMedPubMedCentralGoogle Scholar
  18. LeBlanc B, Davis O, Boue S, DeLucca A, Deeby T. 2009. Antioxidant activity of Sonoran Desert bee pollen. Food Chemistry 115: 1299-1305.CrossRefGoogle Scholar
  19. Leja M, Mareczek A, Wyzgolik G, Klepacz-Baniak J, Czenonska K. 2007. Antioxidative properties of bee pollen in selected plant species. Food Chemistry 100: 237-240.CrossRefGoogle Scholar
  20. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193: 265-275.PubMedPubMedCentralGoogle Scholar
  21. Marghitas L, Stanciu O, Dezmirean D, Bobis O, Popescu O, Bogdanov S, Campos M. 2009. In vitro antioxidant capacity of honeybee-collected pollen of selected floral origin harvested from Romania. Food Chemistry 115: 878-883.CrossRefGoogle Scholar
  22. Nogueira C, Iglesias A, Feás X, Estevinho LM. 2012. Commercial bee pollen with different geographical origins: a comprehensive approach. International Journal of Molecular Sciences 13: 11173–11187.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Novais JS, Absy ML. 2013. Palynological examination of the pollen pots of native stingless bees from the Lower Amazon region in Pará, Brazil. Palynology 37: 218–230.CrossRefGoogle Scholar
  24. Novais JS, Garcez ACA, Absy ML, Santos FAR. 2015. Comparative pollen spectra of Tetragonisca angustula (Apidae, Meliponini) from the Lower Amazon (N Brazil) and caatinga (NE Brazil). Apidologie 46: 417-431.CrossRefGoogle Scholar
  25. Nurdianah HF, Ahmad Firdaus AH, Eshaifol Azam O, Wan Adnan WO. 2016. Antioxidant activity of bee pollen ethanolic extracts from Malaysian stingless bee measured using DPPH-HPLC assay. International Food Research Journal 23: 403-405.Google Scholar
  26. Pascoal A, Rodrigues, S, Teixeira A, Feás X, Estevinho LM. 2014. Biological activities of commercial bee pollens: antimicrobial, antimutagenic, antioxidant and anti-inflammatory. Food and Chemical Toxicology 63: 233-239.CrossRefPubMedGoogle Scholar
  27. Pedro SRM, Camargo JMF. 2013. Stingless bees from Venezuela. pp. 73-86. In: Vit P, Pedro SRM, Roubik D, eds. Pot-Honey: A legacy of stingless bees. Springer. New York, USA. 654 pp.CrossRefGoogle Scholar
  28. Pereira AS, Bicalho B, Aquino Neto FR. 2003. Comparison of propolis from Apis mellifera and Tetragonisca angustula. Apidologie 34: 291-298.CrossRefGoogle Scholar
  29. Pérez-Pérez EM, Suárez E, Peña-Vera MJ, González AC, Vit P. 2013. Antioxidant activity and microorganisms in nest products of Tetragonisca angustula Latreille, 1811 from Mérida, Venezuela. pp. 1-8. In: Vit P & Roubik DW, eds. Stingless bees process honey and pollen in cerumen pots. Facultad de Farmacia y Bioanálisis, Universidad de Los Andes; Mérida, Venezuela. Available at: Accessed the 25.01.2017.
  30. Pietta PG. 2000. Flavonoids as antioxidants. Journal of Natural Products 63: 1035-1042.CrossRefPubMedGoogle Scholar
  31. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. 1999. Antioxidant activity in improved ABTS radical cation decolorization assay. Free Radical in Biology and Medicine 26: 1231-1237.CrossRefGoogle Scholar
  32. Rebelo KS, Ferreira AG, Carvalho-Zilse GA. 2016. Physicochemical characteristics of pollen collected by Amazonian stingless bees. Ciência Rural 46: 927-932.CrossRefGoogle Scholar
  33. Rivero Oramas R. 1972. Abejas criollas sin aguijón. Colección Científica. Monte Avila Editores; Caracas, Venezuela. 110 pp.Google Scholar
  34. Roubik DW, Moreno Patiño JE. 2013. How to be a beebotanist using pollen spectra pp. 73–86. In: Vit P, Pedro SRM, Roubik D, Pot-Honey: A legacy of stingless bees. Springer, New York, USA. 654.Google Scholar
  35. Saral Ö, Yildiz O, Aliyazicioğlu R, Yuluğ E, Canpolat S, Öztürk F, Kolayli S. 2016. Apitherapy products enhance the recovery of CCL4-induced hepatic damages in rats. Turkey Journal of Medical Science 36: 192-202.Google Scholar
  36. Sardar AA, Akhan ZU, Perveen A, Farid S, Khan I. 2014. In vitro antioxidant potential and free radical scavenging activity of various extracts of pollen of Typha domigensis Pers. PakistanGoogle Scholar
  37. Sawaya ACFH, Cunha IBS, Marcucci MC, de Oliveira Rodrigues RF, Eberlin MN. 2006. Brazilian propolis of Tetragonisca angustula and Apis mellifera. Apidologie 37: 398-407.CrossRefGoogle Scholar
  38. Sharaf S, Higazy A, Hebeish A. 2013. Propolis induced antibacterial activity and other technical properties of cotton textiles. International Journal of Biological Macromolecules 59: 408-416.CrossRefPubMedGoogle Scholar
  39. Singleton VL, Orthofer R, Lamuela-Raventos RM. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology 299: 152–178.CrossRefGoogle Scholar
  40. Slaa EJ, Chaves LAS, Malagodi-Braga KS, Hofstde FE. 2006. Stingless bees in applied pollination: practice and perspectives. Apidologie 37: 293-315.CrossRefGoogle Scholar
  41. Sommeijer MJ, de Rooy GA, Punt W, de Bruijn LLM. 1983. A comparative study of foraging behavior and pollen resouces of various stingless bees (Hym., Meliponinae) and honeybees (Hym., Apinae) in Trinidad, West Indies. Apidologie 14: 205-224.CrossRefGoogle Scholar
  42. Souza B, Roubik D, Barth O, Heard T, Enríquez E, Carvalho C, Marchini L, Villas-Bôas J, Locatelli J, Persano Oddo L, Almeida-Muradian L, Bogdanov S, Vit P. 2006. Composition of stingless bee honey: Setting quality standards. Interciencia 31: 867-875.Google Scholar
  43. Ulusoy E, Kolayli S. 2014. Phenolic composition and antioxidant properties of Anzer bee pollen. Journal of Food Biochemistry 38: 73–82.CrossRefGoogle Scholar
  44. Velez-Ruiz RI, Gonzalez VH, Engel MS. 2013. Observations on the urban ecology of the Neotropical stingless bee Tetragonisca angustula (Hymenoptera: Apidae: Meliponini). Journal of Melittology. 15:1-8.CrossRefGoogle Scholar
  45. Vit P. 1994. Las abejas criollas sin aguijón. Vida Apícola 63: 34-41.Google Scholar
  46. Vit P. 2009. Origen botánico y propiedades medicinales del polen apícola. Revista Médica de la Extensión Portuguesa ULA 3: 27-34.Google Scholar
  47. Vit P, Santiago B, Pedro SRM, Peña-Vera M, Pérez-Pérez E. 2016. Chemical and bioactive characterization of pot-pollen produced by Melipona and Scaptotrigona stingless bees from Paria Grande, Amazonas State, Venezuela. Emirates Journal of Food and Agriculture 28: 78-84.CrossRefGoogle Scholar
  48. Vossler FG, Fagúndez GA, Bettler BC. 2014. Variability of Food Stores of Tetragonisca fiebrigi (Schwarz) (Hymenoptera: Apidae: Meliponini) from the Argentine Chaco Based on Pollen Analysis. Sociobiology 61: 449-460.Google Scholar
  49. Woisky RG, Salatino A. 1998. Analysis of propolis: some parameters and procedures for chemical quality control. Journal of Apicultural Research 37: 99-105.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Patricia Vit
    • 1
    • 2
    Email author
  • Bertha Santiago
    • 1
  • María Peña-Vera
    • 3
  • Elizabeth Pérez-Pérez
    • 3
  1. 1.Apitherapy and Bioactivity, Food Science Department, Faculty of Pharmacy and BioanalysisUniversidad de Los AndesMéridaVenezuela
  2. 2.Cancer Research Group, Discipline of Biomedical Science, Cumberland Campus C42The University of SydneyLidcombeAustralia
  3. 3.Laboratory of Biotechnological and Molecular Analysis, Faculty of Pharmacy and BioanalysisUniversidad de Los AndesMéridaVenezuela

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