Physicochemical characterization, antioxidant and antifungal activity of three stingless bee pollen aggregate (Apidae: Meliponini) from Soconusco, Chiapas

Víctor Albores-Flores, Erick Saavedra-Camacho, José Alfonso López-García, Julieta Grajales-Conesa, Liliana Carolina Córdova-Albores

Abstract


Plants-bees interaction can generate bee-hive products with different physicochemical, bioactive and antimicrobial composition. Therefore, in this study we determined the physicochemical composition of pollen aggregates collected from 12 stingless bee-hives established in Chiapas, Mexico, from three different municipalities: Tapachula, Mazatán and Cacahoatán, and with three different species: Melipona beecheii, Scaptotrigona mexicana and Tetragonisca angustula. We also evaluated the effect of pollen aggregate extracts on Colletotrichum gloeosporioides growth. Our results showed differences in the physicochemical composition based on bee species. Pollen from M. beecheii registered the highest phenol content, flavonoids, and free acidity. These results, and the obtained from the antioxidant capacity (Trolox), glucose and pH, were associated with in vitro C. gloesporioides growth. The fungus radial growth rate during the nine-day study was 0.013-0.009 mm h-1 with pollen extracts, which was equivalent to 44% lower value than chlorothalonil. The antifungal activity of pollen extracts depends on bee species; for M. beecheii we registered 65 and 37%, for T. angustula 57 and 16%, and for S. mexicana 60 and 30%, which were higher than the chlorothalonil fungicide.


Keywords


Interaction; inhibition; hive products; pollen aggregate; stingless bees

Full Text:

PDF

References


Albores-Flores V, Marín SIM, López-García JA, Sánchez GA y Grajales-Conesa J. 2018. Propiedad antifúngica de mieles sobre el desarrollo in vitro de Colletotrichum gloeosporioides. Revista Mexicana de Fitopatología 36(3): 423–431. http://doi.org/10.18781/R.MEX.FIT.1805-3

Ayala R, González VH and Engel MS. 2013. Mexican stingless bees (Hymenoptera:Apidae): diversity, distribution, and indigenous Knowledge. In: Vit P, Pedro SR and Roubik D (eds.). Honey-Pot: A legacy of stingless bees. New York: Springer. 366p. http://doi.org/10.1007/978-1-4614-4960-7_9

AOAC (Association of Official Analytical Chemists). 2003. Methods of analysis. Washington, D.C. AOAC. https://www.scirp.org/(S(lz5mqp453edsnp55rrgjct55))/reference/ReferencesPapers.aspx?ReferenceID=1994521

Basim E, Basim H and Özcan M. 2006. Antibacterial activities of Turkish pollen and propolis extracts against plant bacterial pathogens. Journal of Food Engineering 77(4): 992–996. http://dx.doi.org/10.1016/j.jfoodeng.2005.08.027

Beltrán CMC y García JDJ. 2006. Colletotrichum gloeosporioides fitopatógeno asociado a la nutrición humana. Investigaciones Andinas 8(13): 73-80. https://www.redalyc.org/articulo.oa?id=239017515006

Bertrams J, Müller M, Kunz N, Kammerer D and Stintzing FC. 2013. Phenolic compounds as marker compounds for botanical origin determination of German propolis samples based on TLC and TLC-MS. Journal of Applied Botany and Food Quality 86(1):143-153. http://dx.doi.org/10.5073/JABFQ.2013.086.020

Bogdanov S. 2004. Quality and standards of pollen and beeswax. Apiacta 38: 334–341. http://www.researchgate.net/publication/229041189_Quality_and_standards_of_pollen_and_beeswax

Bogdanov S. 2002. Harmonized Methods of the International Honey Commission. International Honey Commission. http://www.researchgate.net/publication/285841406_Harmonised_methods_of_the_International_Honey_Commission

Borkraâ L and Sulaiman S. 2010. Rediscovering the antibiotics of the hive. Recent patents on anti-effective drug discovery 4(3):2006-2013. http://dx.doi.org/10.2174/157489109789318505

Cabrera C and Montenegro G. 2013. Pathogen control using a natural Chilean bee pollen extract of known botanical origin. Ciencia e Investigación Agraria 40(1): 223-230. http://dx.doi.org/10.4067/S0718-16202013000100020.

Carpes S, Begnini R, de Alencar S and Masson M. 2007. Study of preparations of bee pollen extracts, antioxidant and antibacterial activity. Ciência e Agrotecnologia 31(6): 1818-1825. http://www.scielo.br/pdf/cagro/v31n6/a32v31n6.pdf

Chacini C, Blanco M, Sanchez S y Acevedo I. 2013. Evaluación a nivel de laboratorio del efecto de 7 extractos vegetales para el control de Colletotrichum sp. agente causal de la antracnosis en el cultivo de tomate de árbol. Innovaciencia 1(1): 30-35. https://doi.org/10.15649/2346075X.214

Da Silva PM, Gauche C, Gonzaga LV, Costa ACO and Fett R. 2016. Honey: Chemical composition, stability and authenticity. Food Chemistry 196: 309–323. http://dx.doi.org/10.1016/j.foodchem.2015.09.051

Dötterl S and Vereecken N. 2010. The chemical ecology and evolution of bee-flower interactions: a review and perspectives. Canadian Journal of Zoology 88(7): 668-697. http://dx.doi.org/10.1139/Z10-031

Duran N, Muz M, Culha G, Duran G and Ozer B. 2011. GC-MS analysis and antileishmanial activities of two Turkish propolis types. Parasitology Research 108(1):95-105. http://dx.doi.org/10.1007/s00436-010-2039-z

Espinoza-Toledo C, Vázquez-Ovando A, Torres de los Santos R, López García A, Albores-Flores V and Grajales-Conesa J. 2018. Stingless bee honeys from Soconusco, Chiapas: a complementary approach. Revista de Biología Tropical 66(4): 1536-1546. http:77dx.dor.org/10.15517/RBT.V66I4.32181

Grajales-Conesa J, Ibarias TC, Ruíz TJ y Sánchez D. 2018. Mieles de abejas sin aguijón en el tratamiento de úlceras de pie diabético. Salud Pública de México 60:102-104. http://doi.org/10.21149/8604

Huerta G, Holguin F, Benítez C y Toledo J. 2009. Epidemiología de la antracnosis (Colletotrichum gloeosporioides (Penz) Penz and Sacc) en mango (Mangifera indica L.) CV. Ataulfo en el Soconusco, Chiapas, México. Revista Mexicana de Fitopatología 27: 93-105. http://www.scielo.org.mx/pdf/rmfi/v27n2/v27n2a2.pdf

Kacaniova M, Vukovi? N, Chlebo R, Haš?ík P, Rovná K, Cubon J and Pasternakiewicz A. 2012. The antimicrobial activity of honey, bee pollen loads and beeswax from Slovakia. Archives of Biological Sciences 64(3): 927–934. http://doi.org/10.2298/ABS1203927K

Komosinska VK, Olczyk P, Ka?mierczak J, Mencner L and Olczyk K. 2015. Bee pollen: chemical composition and therapeutic application. Evidence-Based Complementary and Alternative Medicine 2015: 1–6. http://dx.doi.org/10.1155/2015/297425

Li Y, Skouroumounis GK, Elsey GM and Taylor DK. 2011. Microwave-assistance provides very rapid and efficient extraction of grape seed polyphenols. Food Chemistry 129(2):570-6. http://doi.org/10.1016/j.foodchem.2011.04.068.

M?rg?oan R, M?rghita? L, Dezmirean D, Mihai CM and Bobi? O. 2010. Bee collected pollen – general aspects and chemical composition. Bull UASVM Animal Science and Biotecnologies 67(1-2): 254-259. file:///C:/Users/RMF/Downloads/5305-19198-1-PB.pdf

M?rghita? LA, Stanciu OG, Dezmirean DS, Bobi? O, Popescu O, Bogdanov S and Campos MG. 2009. In vitro antioxidant capacity of honeybee-collected pollen of selected floral origin harvested from Romania. Food Chemistry 115(3): 878-83. http://doi.org/10.1016/j.foodchem.2009.01.014.

Molan P and Betts N. 2004. Clinical usage of honey as a wound dressing: an update. Journal of Wound Care 13: 353-356. https://doi.org/10.12968/jowc.2004.13.9.26708

Muñoz CW, Chavez RW, Pabón LC, Rendón FMR, Patricia CM y Otálvaro AAM. 2015. Extracción de compuestos fenólicos con actividad antioxidante a partir de Champa (Campomanesia lineatifolia) Revista CENIC Ciencias Químicas 46: 38–46. http://www.redalyc.org/pdf/1816/181643224027.pdf

Okwu DE and Nnamdi FU. 2008. Evaluation of the chemical composition of Dacryodes edulis and Raphia hookeri Mann and wendl exudates used in herbal madicine in South Eastern Nigeria. African Journal of Traditional, Complementary and Alternative Medicines 5(2): 194-200. http://doi.org/10.4314/ajtcam.v5i2.31273

Overveld FWPC, Haenen GRMM, Rhemrev J, Vermeiden JPW and Bast A. 2000. Tyrosine as important contributor to the antioxidant capacity of seminal plasma. Chemico-Biological Interactions 127(2): 151 – 161. http://doi.org/10.1016/S0009-2797(00)00179-4

Pascoal A, Rodriges S, Teixeira A, Feás X and Estevinho L. 2014. Biological activities of commercial bee pollens: antimicrobial, antimutagenic, antioxidant y antiinflamatorio. Food and Chemical Toxicology 63: 633-639. http://dx.doi.org/10.1016/j.fct.2013.11.010

Paulino-Zunini M, Rojas C, De Paula S, Elingold I, Alvareda ME, Casanova MB, Iribarne RF, Aguilera MS and Dubin M. 2010. Phenolic contents and antioxidant activity in central-southern Uruguayan propolis extracts. Journal of the Chilean Chemical Society 55(1):141-146. http://dx.doi.org/10.4067/S0717-97072010000100033

Pellati F, Orlandini G, Pinetti D and Benvenuti S. 2011. HPLC-DAD and HPLC-ESI-MS/MS methods for metabolite profiling of propolis extracts. Journal of Pharmaceutical and Biomedical Analysis 55(5): 934-48. http://doi.org/10.1016/j.jpba.2011.03.024

Pietarinen SP, Willfor SM, Vikstrom FA and Holmbom BR. 2006. Aspen knots, a rich source of flavonids. Journal of Wood Chemistry and Technology 26(3): 245 – 258. http://doi.org/10.1080/02773810601023487

Rao PV, Krishnan KT, Salleh N and Gan SH. 2016. Biological and therapeutic effects of honey produced by honey bees and stingless bees: a comparative review. Revista Brasileira de Farmacognosia 26: 657-664. http://dx.doi.org/10.1016/j.bjp.2016.01.012.

Restrepo SDC, Narváez CCE and Restrepo SPL. 2009. Extracción de compuestos con actividad antioxidante de frutos de guayaba cultivada en Vélez Santander, Colombia. Química Nova 32: 1517-1522. http://www.scielo.br/pdf/qn/v32n6/30.pdf

Rodríguez-Maturino A R, Troncoso-Rojas R, Sánchez-Estrada A, González-Mendoza D, Ruíz-Sánchez E, Zamora-Bustillos R, Cece na-Duran, C, Grimaldo-Juarez O, Avilez-Marin M. 2015. Efecto antifúngico de extractos fenólicos y de carotenoides de chiltepín (Capsicum annum var. glabriusculum) en Alternaria alternata y Fusarium oxysporum. Revista Argentina de microbiología 47(1): 72-77. https://doi.org/10.1016/j.ram.2014.12.005

Rojas YPM. 2015. Valoración in vitro del potencial antimicrobiano de extractos etanólicos de polen de Apis mellifera y de Tetragonisca angustula, en busca de posibles usos terapéuticos. Tesis magister. Universidad Nacional de Colombia 83 p. http://bdigital.unal.edu.co/51696/1/yurleypaolamonserraterojas.2015.pdf

Ruíz-Montañez G, Ragazo SJ, Calderón SM, Velázquez de la CG, Ramírez de LJ and Navarro OA. 2014. Evaluation of extraction methods for preparative scale obtention of mangiferin and lupeol from mango peles (Mangifera indica L.). Food Chemistry 159: 267-272. http://doi.org/10.1016/j.foodchem.2014.03.009

Saavedra CKI, Rojas IC y Delgado PGE. 2013. Características polínicas y composición química del polen apícola colectado de Cayaltí (Lambayeque-Perú). Revista Chilena de Nutrición 40: 71-78. http://dx.doi.org/10.4067/S0717-75182013000100011.

Schaich K, Tian X and Xie J. 2015. Hurdles and pitfalls in measuring antioxidant efficacy: A critical evaluation of ABTS, DPPH, and ORAC assays. Journal of Functional Foods 14: 111-25. http://doi.org/10.1016/j.jff.2015.01.043

Soto GM y Rosales CM. 2016. Efecto del solvente y de la relación masa / solvente, sobre la extracción de compuestos fenólicos y la capacidad antioxidante de extractos de corteza de Pinus durangensis y Quercus sideroxyla. Maderas, Ciencia y Tecnología 18(4): 701 – 714. http://dx.doi.org/10.4067/S0718-221X2016005000061

Trinidad-Ángel E, Ascencio VFJ, Ulloa JA, Ramírez RJC, Ragazzo SJA, Calderon SM y Bautista RPU. 2017. Identificación y caracterización de Colletotrichum spp. Causante de antracnosis en aguacate Nayarit, México. Revista Mexicana de Ciencias Agrícolas 19: 3953-3964. http://www.scielo.org.mx/pdf/remexca/v8nspe19/2007-0934-remexca-8-spe19-3953-en.pdf

Vit P, Gutiérrez MG, Titera D, Bednar M y Rodríguez-Malaver AJ. 2008. Mieles checas categorizadas según su actividad antioxidante. Acta Bioquímica Clínica Latinoamericana 42(2): 237-244. http://www.redalyc.org/pdf/535/53542209.pdf

Vit P. 2008 Review: valorization honey of stingless bees (Meliponini). Brazilian Journal of Pharmaceutical Science 50: 20-28.

Vit P, Santiago B, Silva P, Ruíz J, Maza F, Peña M and 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(2): 78-84. http://doi.org/10.9755/ejfa.2015-05-245

Villanueva-Gutiérrez R, Roubik D and Porter-Bolland L. 2015. Bee-Plant interactions: Competition and phenology of flowers visited by bees. In: Islebe G, Calmé S, León-Cortés J, Schmook B. (eds). Biodiversity and conservation of the Yucatán Península. Springer, Cham. https://doi.org/10.1007/978-3-319-06529-8_6

Zainol M, Mohd K and Mohd Y. 2013. Antibacterial activity of selected Malaysian honey. BMC complementary and alternative Medicine 13(129): 1-10. http://doi.org/10.1186/1472-6882-13-129.




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.2009-4

Refbacks

  • There are currently no refbacks.