Effect of Propolis Oral Intake on Physiological Condition of Young Worker Honey Bees, Apis Mellifera L.

Natalia Damiani 1 , 2 , Martín P. Porrini 1 , 2 , Juan P. Lancia 3 , 4 , Estefanía Álvarez 1 , Paula M. Garrido 1 , 2 , Enzo Domínguez 1 , Liesel B. Gende 1 , 2  and Martín J. Eguaras 1 , 2
  • 1 Centro de Investigación en Abejas Sociales. Facultad de Ciencias Exactas y Naturales. Universidad Nacional de Mar del Plata. Funes 3350 (7600) Mar del Plata. , Buenos Aires, Argentina
  • 2 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), , Buenos Aires, Argentina
  • 3 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), , Buenos Aires, Argentina
  • 4 Laboratorio de Invertebrados, Instituto de Investigaciones Marinas y Costeras (IIMyC), Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata. Funes 3250 Casilla de Correo 1260, , Mar del Plata, Argentina


Honey bees collect resin from various plant species and transform it into propolis that is incorporated into the nest. The role of resins in the bee health field is poorly understood. The aim was to evaluate the effects of forced consumption of propolis on the physiological condition and short-term survival of Apis mellifera worker bees. It was tested if the number of circulating hemocytes in hemolymph, the abdominal fat bodies and the hypopharyngeal glands development were affected by the feeding with propolis extracts in laboratory conditions during the warm and the cold seasons. Propolis added to sugar candy was consumed by workers for fourteen days without affecting the bee survival. The number of circulating hemocytes in hemolymph remained constant despite the differential diet during the experiment. However, the development of fat bodies and hypopharyngeal glands was altered by propolis ingestion. The abdominal fat body development in winter bees diminished after fourteen days of propolis consumption, while it increased in summer bees. The hypopharyngeal gland development decreased for the assayed period in workers from both seasons. Our results encourage us to continue exploring this research field and learn how long-term forced ingestion of a plant-derived compound, a non-nutritive substance, can modify physiological bee parameters. A broader understanding of the multiple roles of propolis in the health of the honey bee colonies could be obtained by studying the ways in which it is processed and metabolized and the effect that generates in another physiological responses.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Amaral, I., Moreira Neto, J., Pereira, G., Franco, M., Beletti, M., Kerr, W., Bonetti, A., Ueira-Vieira, C. (2010). Circulating hemocytes from larvae of Melipona scutellaris (Hymenoptera, Apidae, Meliponini): cell types and their role in phagocytosis. Micron, 41(2), 123-129. DOI: 10.1016/j.micron.2009.10.003

  • Amdam, G., & Omholt, S. (2002). The regulatory anatomyof honeybee lifespan. Journal of Theoretical Biology, 216, 209-228. DOI: 10.1006/jtbi.2002.2545

  • Amdam, G., & Page, R. (2005). Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect. Ageing Research Reviews, 4(3), 398-408. DOI: 10.1016/j.arr.2005.03.007

  • Amdam, G., & Seehuu, S. (2006). Order, disorder, death: Lessons from a superorganism. Advances in Cancer Research, 95, 31-60. DOI: 10.1016/S0065-230X(06)95002-7

  • Amdam, G., Rueppell, O., Fondrk, M., Page, R., Nelson, C. (2009). The nurse’s load: Early-life exposure to brood-rearing affects behavior and lifespan in honey bees (Apis mellifera). Experimental Gerontology, 44, 467-471. DOI: 10.1016/j.exger.2009.02.013

  • Antúnez, K., Harriet, J., Gende, L., Maggi, M., Eguaras, M., Zunino, P. (2008). Efficacy of natural propolis extract in the control of American Foulbrood. Veterinary Microbiology, 131, 324-331. DOI: 10.1016/j.vetmic.2008.04.011

  • Babendreier, D., Kalberer, N., Romeis, J., Fluri, P., Mulligan, E., Bigler, F. (2005). Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees. Apidologie, 6(4), 585-594. DOI: 10.1051/apido:2005049

  • Bankova, V., De Castro, S., & Marcucci, M. (2000). Propolis: recent advances in chemistry and plant origin. Apidologie, 31, 3-15. DOI: 10.1051/apido:2000102

  • Bastos, E., Simone, M., Macedo, D., Soares, A., Spivak, M. (2008). In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. Journal of Invertebrate Pathology, 97, 273-281. DOI: 10.1016/j.jip.2007.10.007

  • Bogdanov, S. (2015). Propolis: Composition, Health, Medicine: A Review. Bee Product Science, 1-40.

  • Burdock, G. (1998). Review of the biological properties and toxicity of bee propolis (Propolis). Food and Chemical Toxicology, 36(4), 347-363. DOI: 10.1016/S0278-6915(97)00145-2

  • Cremer, S., & Sixt, M. (2009). Analogies in the evolution of individual and social immunity. Philosophical Transactions of the Royal Society B, 364, 129-142. DOI: 10.1098/rstb.2008.0166

  • Damiani, N., Fernández, N., Maldonado, L., Álvarez, A., Eguaras, M., Marcangeli, J. (2010). Bioactivity of propolis from different geographical origins on Varroa destructor (Acari: Varroidae). Parasitology Research, 107(1), 31-37. DOI: 10.1007/s00436-010-1829-7

  • de Moraes, R., & Bowen, I. (2000). Modes of cell death in the hypopharyngeal gland of the honey bee (Apis mellifera L). Cell Biology International, 24(10), 737-743. DOI: 10.1006/cbir.2000.0534

  • Deseyn, J., & Billen, J. (2005). Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae). Apidologie 36(1), 49-57. DOI: 10.1051/apido: 2004068

  • Drescher, W., & Schneider, P. (1987). The effect of the Varroa mite upon the fat body of worker bees and their tolerance of pesticides. In Africanized honey bees and bee mites. (pp. 452-456).England: Ellis Horwood ltd. Chichester.

  • Ebert, T., Kevan, P., Bishop, B., Kevan, S., Downer, R. (2007). Oral toxicity of essential oils and organic acids fed to honey bees (Apis mellifera). Journal of Apicultural Research and Bee World, 46(4), 220-224. DOI: 10.3896/IBRA.

  • Erler, S., & Moritz, R. (2016). Pharmacophagy and pharmacophory: mechanisms of self-medication and disease prevention in the honeybee colony (Apis mellifera). Apidologie, 47(3), 389-411. DOI: 10.1007/s13592-015-0400-z

  • Fluri, P., & Bogdanov, S. (1987). Age dependence of fat body protein in summer and winter bees (Apis mellifera). In Chemistry and biology of social insects. (pp. 170-171). Munchen: Verlag J. Peperny.

  • Fluri, P., Lüscher, M., Wille, H., & Gerig, L. (1982). Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone and vitellogenin in worker honeybees. Journal of Insect Physiology, 28(1), 61-68. DOI: 10.1016/0022-1910(82)90023-3

  • Gillespie, J., Kanost, M., & Trenczek, T. (1997). Biological mediators of insect immunity. Annual Review of Entomology, 42, 611-43. DOI: 10.1146/annurev.ento.42.1.611

  • Gupta, P., & Chandel, R. (1995). Effects of Diflubenzuron and Penfluron on workers of Apis cerana-indica F. and Apis mellifera L. Apidologie, 26, 3-10. DOI: 10.1051/apido:19950101

  • Hrassnigg, N., & Crailsheim, K. (1998). Adaptation of hypopharyngeal gland development to the brood status of honeybee (Apis mellifera L.) colonies. Journal of Insect Physiology, 44(10), 929-939. DOI: 10.1016/S0022-1910(98)00058-4

  • James, R., & Xu, J. (2012). Mechanisms by which pesticides affect insect immunity. Journal of Invertebrate Pathology, 109(2), 175-82. DOI: 10.1016/j.jip.2011.12.005

  • Johnson, R., Mao, W., Pollock, H., Niu, G., Schuler, M., Berenbaum, M. (2012). Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLoS One, 7(2), e31051. DOI: 10.1371/journal.pone.0031051

  • Jones, J. (1962). Current concepts concerning insect hemocytes. Integrative and Comparative Biology, 2(2), 209-246. DOI: 10.1093/icb/2.2.209

  • Keeley, L. (1985). Biochemistry and physiology of the insect fat body. In Comprehensive insect physiology, biochemistry and pharmacology. (pp. 211-228). New York: Pergamon.

  • Knecht, D., & Kaatz, H. (1990). Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie, 21, 457-467. DOI: 10.1051/apido:19900507

  • König, B. (1988). The honeybee as pharmacophorus insect. Entomologia Generalis, 14(2), 145-148. DOI: 10.1127/entom.gen/14/1988/145

  • Lavine M., & Strand, M. (2002). Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32(10), 1295-1309. DOI: 10.1016/S0965-1748(02)00092-9

  • Mao, W., Schuler, M., & Berenbaum, M. (2013). Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. In Proceedings of the National Academy of Sciences of the United States of America (pp. 8842-8846). USA.

  • Mao, W., Schuler, M., & Berenbaum, M. (2015). A dietary phytochemical alters caste-associated gene expression in honey bees. Science Advances, 1(7), e1500795. DOI: 10.1126/sciadv.1500795

  • Marcucci, M. (1995). Propolis: chemical composition, biological properties and therapeutic activity. Apidologie, 26(2), 83-99. DOI: 10.1051/apido:19950202

  • Marmaras, V., & Lampropoulou, M. (2009). Regulatorsand signalling in insect haemocyte immunity. Cell Signal, 21(2), 186-195. DOI: 10.1016/j.cellsig.2008.08.014

  • Maurizio, V. (1954). Pollenernährung und Lebensvorgänge bei der Honigbiene (Apis mellifica L.). Landwirtschaftliches Jahrbuch der Schweiz, 68(2), 115-182.

  • McMullan, J., & Brown, M. (2006). The influence of small-cell brood combs on the morphometry of honeybees (Apis mellifera). Apidologie, 37(6), 665-672. DOI: 10.1051/apido:2006041

  • Mead, G., Ratcliffe, N., & Renwrantz, L. (1986). The separation of insect haemocyte types on Percoll gradients; methodology and problems. Journal of Insect Physiology, 32(2), 167-177. DOI: 10.1016/0022-1910(86)90137-X

  • Mihai, C., Mărghitaş, L., Dezmirean, D., Chirilă, F., Moritz, R., Schlüns, H. (2012). Interactions among flavonoids of propolis affect antibacterial activity against the honeybee pathogen Paenibacillus larvae. Journal of Invertebrate Pathology, 110(1), 68-72. DOI: 10.1016/j.jip.2012.02.009

  • Simone, M., Evans, J., & Spivak M. (2009). Resin collection and social immunity in honey bees. Evolution, 63(11), 3016-3022. DOI: 10.1111/j.1558-5646.2009.00772.x

  • Simone-Finstrom, M., & Spivak, M. (2010). Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie, 41(3), 295-311. DOI: 10.1051/apido/2010016

  • Szymaś, B., & Jędruszuk, A. (2003). The influence of different diets on haemocytes of adult worker honey bees, Apis mellifera. Apidologie, 34(2), 97-102. DOI: 10.1051/apido:2003012

  • Wilson, M., Brinkman, D., Spivak, M., Gardner, G., Cohen, J. (2015). Regional variation in composition and antimicrobial activity of US propolis against Paenibacillus larvae and Ascosphaera apis. Journal of Invertebrate Pathology, 124, 44-50. DOI: 10.1016/j.jip.2014.10.005

  • Wilson-Rich, N., Dres, S., & Starks, P. (2008). The ontogeny of immunity: Development of innate immune strength in the honey bee (Apis mellifera). Journal of Insect Physiology, 54(10-11), 1392-1399. DOI: 10.1016/j.jinsphys.2008.07.016

  • Wilson-Rich, N., Spivak, M., Fefferman, N., & Starks, P. (2009). Genetic, individual, and group facilitation of disease resistance in insect societies. Annual Review of Entomology, 54, 405-423. DOI: 10.1146/annurev.ento.53.103106.093301


Journal + Issues