Parasitology Research

, Volume 117, Issue 11, pp 3527–3535 | Cite as

The effects of raw propolis on Varroa-infested honey bee (Apis mellifera) workers

  • Michelina Pusceddu
  • Ignazio FlorisEmail author
  • Alessandra Mura
  • Panagiotis Theodorou
  • Giorgia Cirotto
  • Giovanna Piluzza
  • Simonetta Bullitta
  • Alberto Angioni
  • Alberto Satta
Original Paper


Self-medication plays a major role in the behavioral defense against pathogens and parasites that animals have developed during evolution. The conditions defining this adaptive behavior are: (1) contact with the substance in question must be deliberate; (2) the substance must be detrimental to one or more parasites; (3) the detrimental effect on parasites must lead to increased host fitness. Recent studies have shown that A. mellifera colonies are able to increase resin foraging rates when infested by V. destructor, whereas further investigations are needed for evidence of parasite and host fitness. In order to understand whether Varroa-infested colonies could benefit from increasing levels of resin, we carried out laboratory bioassays to investigate the effects of propolis on the fitness of infested workers. The longevity and energetic stress of adult bees kept in experimental cages and artificially infested with the mite were thus monitored over time. At the same time, in vitro experiments were performed to study the contact effects of crude propolis on Varroa mites. Our results clearly demonstrate the positive effects of raw propolis on the lifespan of Varroa-infested adult bees. A low narcoleptic effect (19–22%) of raw propolis on phoretic mites after 5 h was also observed. In terms of energetic stress, we found no differences between Varroa-free and Varroa-infested bees in terms of the daily sucrose solution demand. Our findings seem to confirm the hypothesis that resin collection and propolis use in the hive represent an example of self-medication behavior in social insects.


Self-medication Energetic stress Bee longevity Narcoleptic power Polyphenols 



The authors acknowledge the Regione Autonoma della Sardegna for the financial support of Alessandra Mura’s PhD scholarship, P.O.R. Sardegna F.S.E. 2014/2020 Asse III- Istruzione e formazione–Obiettivo tematico 10 “Investire nell’istruzione e nella formazione professionale per le competenze e l’apprendimento permanente”.

The authors are also grateful to Angela Milia and Gavino Tutedde for the technical support provided in the laboratory experiments.


This study was financially supported by the Italian Ministry of Education, University and Research (MIUR; 2012RCEZWH), “Social immunity in honeybee: behavioral, chemical and microbiological aspects.”

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

436_2018_6050_MOESM1_ESM.docx (277 kb)
ESM 1 (DOCX 277 kb)


  1. Alaux C, Allier F, Decourtye A, Odoux JF, Tamic T, Chabirand M, Henry M (2017) A “landscape physiology” approach for assessing bee healt highlights the benefits of floral landscape enrichment and semi-natural habitats. Sci Rep 7:40568. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amdam GV, Omholt SW (2002) The regulatory anatomy of honeybee lifespan. J Theor Biol 216(2):209–228CrossRefGoogle Scholar
  3. Ball BV, Allen MF (1988) The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Ann Appl Biol 113(2):237–244CrossRefGoogle Scholar
  4. Bartoń K (2018) MuMIn: Multi-Model Inference. R package version 1.40.4.
  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. CrossRefGoogle Scholar
  6. Borba RS (2015) Constitutive and therapeutic benefits of plant resins and a propolis envelope to honey bee, Apis mellifera L., immunity and health. Ph.D. thesis, University of Minnesota, Ann Arbor, MA, USAGoogle Scholar
  7. Borba RS, Spivak M (2017) Propolis envelope in Apis mellifera colonies supports honey bees against the pathogen, Paenibacillus larvae. Sci Rep 7:11429. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Borba RS, Klyczek KK, Mogen KL, Spivak M (2015) Seasonal benefits of a natural propolis envelope to honey bee immunity and colony health. J Exp Biol 218(22):3689–3699CrossRefGoogle Scholar
  9. Clayton DH, Wolfe ND (1993) The adaptive significance of self-medication. Trends Ecol Evol 8(2):60–63CrossRefGoogle Scholar
  10. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318(5848):283–287CrossRefGoogle Scholar
  11. Cremer S, Armitage SA, Schmid-Hempel P (2007) Social immunity. Curr Biol 17(16):R693–R702CrossRefGoogle Scholar
  12. Cremer S, Pull CD, Fürst MA (2018) Social immunity: emergence and evolution of colony-level disease protection. Annu Rev Entomol 63:105–123CrossRefGoogle Scholar
  13. da Silva JFM, de Souza MC, Matta SR, de Andrade MR, Vidal FVN (2006) Correlation analysis between phenolic levels of Brazilian propolis extracts and their antimicrobial and antioxidant activities. Food Chem 99(3):431–435CrossRefGoogle Scholar
  14. Damiani N, Fernández NJ, Maldonado LM, Álvarez AR, Eguaras MJ, Marcangeli JA (2010) Bioactivity of propolis from different geographical origins on Varroa destructor (Acari: Varroidae). Parasitol Res 107(1):31–37CrossRefGoogle Scholar
  15. de Roode JC, Lefèvre T, Hunter MD (2013) Self-medication in animals. Science 340(6129):150–151CrossRefGoogle Scholar
  16. Drescher N, Klein AM, Neumann P, Yañez O, Leonhardt SD (2017) Inside honeybee hives: impact of natural propolis on the ectoparasitic mite Varroa destructor and viruses. Insects 8(1):15CrossRefGoogle Scholar
  17. Erler S, Moritz RF (2016) Pharmacophagy and pharmacophory: mechanisms of self-medication and disease prevention in the honeybee colony (Apis mellifera). Apidologie 47(3):389–411CrossRefGoogle Scholar
  18. Evans JD, Pettis JS (2005) Colony-level impacts of immune responsiveness in honey bees, Apis mellifera. Evolution 59(10):2270–2274CrossRefGoogle Scholar
  19. Garcia RC, Oliveira NTED, Camargo SC, Pires BG, Oliveira CALD, Teixeira RDA, Pickler MA (2013) Honey and propolis production, hygiene and defense behaviors of two generations of Africanized honey bees. Sci Agric 70(2):74–81CrossRefGoogle Scholar
  20. Garedew A, Lamprecht I, Schmolz E, Schricker B (2002) The varroacidal action of propolis: a laboratory assay. Apidologie 33(1):41–50CrossRefGoogle Scholar
  21. Garedew A, Schmolz E, Lamprecht I (2003) Microcalorimetric and respirometric investigation of the effect of temperature on the antiVarroa action of the natural bee product-propolis. Thermochim Acta 399(1–2):171–180CrossRefGoogle Scholar
  22. Higes M, Meana A, Bartolomé C, Botías C, Martín-Hernández R (2013) Nosema ceranae (microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 5(1):17–29CrossRefGoogle Scholar
  23. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363CrossRefGoogle Scholar
  24. Lozano GA (1998) Parasitic stress and self-medication in wild animals, in advances in the study behavior. In: Møller AP, Milinski M, Slater PJB (eds) Stress and behavior, vol 27. Academic, Cambridge, pp 291–317CrossRefGoogle Scholar
  25. Macedo PA, Wu J, Ellis MD (2002) Using inert dusts to detect and assess varroa infestations in honey bee colonies. J Apic Res 41(1–2):3–7CrossRefGoogle Scholar
  26. Manrique AJ, Soares EEA (2002) Início de um programa de seleção de abelhas africanizadas para a melhoria na produção de própolis e seu efeito na produção de mel. Interciencia 27(6):312–316Google Scholar
  27. Marcucci MC (1995) Propolis: chemical composition, biological properties and therapeutic activity. Apidologie 26(2):83–99CrossRefGoogle Scholar
  28. Martin SJ (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J Appl Ecol 38(5):1082–1093CrossRefGoogle Scholar
  29. Martín-Hernández R, Botías C, Barrios L, Martínez-Salvador A, Meana A, Mayack C, Higes M (2011) Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitol Res 109(3):605–612CrossRefGoogle Scholar
  30. Mattila HR, Harris JL, Otis GW (2001) Timing of production of winter bees in honey bee (Apis mellifera) colonies. Insect Soc 48:88–93CrossRefGoogle Scholar
  31. Mayack C, Naug D (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100(3):185–188CrossRefGoogle Scholar
  32. Mazzei M, Carrozza ML, Luisi E, Forzan M, Giusti M, Sagona S, Tolari F, Felicioli A (2014) Infectivity of DWV associated to flower pollen: experimental evidence of a horizontal transmission route. PLoS One 9(11):e113448CrossRefGoogle Scholar
  33. Mihai CM, Mărghitaş LA, Dezmirean DS, Chirilă F, Moritz RF, Schlüns H (2012) Interactions among flavonoids of propolis affect antibacterial activity against the honeybee pathogen Paenibacillus larvae. J Invertebr Pathol 110(1):68–72CrossRefGoogle Scholar
  34. Milani N (1995) The resistance of Varroa jacobsoni oud to pyrethroids: a laboratory assay. Apidologie 26(5):415–429CrossRefGoogle Scholar
  35. Nakamura J, Seeley TD (2006) The functional organization of resin work in honey bee colonies. Behav Ecol Sociobiol 60:339–349CrossRefGoogle Scholar
  36. Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G et al (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8(6):e1002735CrossRefGoogle Scholar
  37. Neumann P, Carreck NL (2010) Honey bee colony losses. J Apic Res 49(1):1–6CrossRefGoogle Scholar
  38. Nicodemo D, De Jong D, Couto RHN, Malheiros B (2013) Honey bee lines selected for high propolis production also have superior hygienic behavior and increased honey and pollen stores. Genet Mol Res 12:6931–6938CrossRefGoogle Scholar
  39. Nicodemo D, Malheiros EB, De Jong D (2014) Increased brood viability and longer lifespan of honeybees selected for propolis production. Apidologie 45(2):269–275CrossRefGoogle Scholar
  40. Padilha AH, Sattler A, Cobuci JA, McManus CM (2013) Genetic parameters for five traits in Africanized honeybees using Bayesian inference. Genet Mol Biol 36(2):207–213CrossRefGoogle Scholar
  41. Pappas N, Thrasyvoulou A (1988) Searching for an accurate method to evaluate the degree of Varroa infestation in honeybee colonies. European research on varroatosis control, Commission of the European Communities, Rotterdam, pp 85–92Google Scholar
  42. Pellati F, Orlandini G, Pinetti D, Benvenuti S (2011) HPLC-DAD and HPLC-ESI-MS/MS methods for metabolite profiling of propolis extracts. J Pharm Biomed Anal 55(5):934–948CrossRefGoogle Scholar
  43. Popova M, Reyes M, Le Conte Y, Bankova V (2014) Propolis chemical composition and honeybee resistance against Varroa destructor. Nat Prod Res 28(11):788–794CrossRefGoogle Scholar
  44. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353CrossRefGoogle Scholar
  45. Pusceddu M, Piluzza G, Theodorou P, Buffa F, Ruiu L, Bullitta S, Floris I, Satta A (2017) Resin foraging dynamics in Varroa destructor infested hives. A case of medication of kin? Insect Sci.
  46. R Core Team (2017) R: a language and environment for statistical computing. Available from
  47. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119CrossRefGoogle Scholar
  48. Simone M, Evans JD, Spivak M (2009) Resin collection and social immunity in honey bees. Evolution 63(11):3016–3022CrossRefGoogle Scholar
  49. Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41(3):295–311CrossRefGoogle Scholar
  50. Simone-Finstrom MD, Spivak M (2012) Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS One 7(3):e34601CrossRefGoogle Scholar
  51. Simone-Finstrom M, Borba RS, Wilson M, Spivak M (2017) Propolis counteracts some threats to honey bee health. Insects 8(2):46CrossRefGoogle Scholar
  52. Singer MS, Mace KC, Bernays EA (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS One 4(3):e4796CrossRefGoogle Scholar
  53. Siripatrawan U, Vitchayakitti W, Sanguandeekul R (2013) Antioxidant and antimicrobial properties of Thai propolis extracted using ethanol aqueous solution. Int J Food Sci Technol 48(1):22–27CrossRefGoogle Scholar
  54. Smart M, Pettis J, Rice N, Browning Z, Spivak M (2016) Linking measures of Colony and individual honey bee health to survival among apiaries exposed to varying agricultural land use. PLoS One 11(3):e0152685CrossRefGoogle Scholar
  55. Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F, Colin ME, Bergoin M (2004) Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol 70(12):7185–7191CrossRefGoogle Scholar
  56. Therneau TM (2015) coxme: mixed effects cox models. R package version 2.2–5.
  57. Therneau TM, Grambsch PM (2000) Modeling survival data extending the cox model. Springer, New York ISBN 0-387-98784-3CrossRefGoogle Scholar
  58. Williams GR, Alaux C, Costa C, Csáki T, Doublet V, Eisenhardt D, Fries I, Kuhn R, McMahon DP, Medrzycki P, Murray TE, Natsopoulou ME, Neumann P, Oliver R, Paxton RJ, Pernal SF, Shutler D, Tanner G, van der Steen JJM, Brodschneider R (2013) Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J Apic Res 52(1):1–36CrossRefGoogle Scholar
  59. Yue C, Genersch E (2005) RT-PCR analysis of deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol 86(12):3419–3424CrossRefGoogle Scholar
  60. Yue C, Schröder M, Gisder S, Genersch E (2007) Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol 88(8):2329–2336CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Michelina Pusceddu
    • 1
  • Ignazio Floris
    • 1
    Email author
  • Alessandra Mura
    • 1
  • Panagiotis Theodorou
    • 2
  • Giorgia Cirotto
    • 3
  • Giovanna Piluzza
    • 4
  • Simonetta Bullitta
    • 4
  • Alberto Angioni
    • 5
  • Alberto Satta
    • 1
  1. 1.Dipartimento di Agraria, Sezione di Patologia vegetale ed EntomologiaUniversità di SassariSassariItaly
  2. 2.General Zoology, Institute of BiologyMartin Luther University Halle-WittenbergHalle (Saale)Germany
  3. 3.Dipartimento di Scienze Agrarie e Forestali (DAFNE)Università della Tuscia-ViterboViterboItaly
  4. 4.Istituto per il Sistema Produzione Animale in Ambiente Mediterraneo (ISPAAM uos Sassari) Consiglio Nazionale delle Ricerche (CNR)SassariItaly
  5. 5.Dipartimento di Scienze della Vita e dell’AmbienteUniversità degli Studi di CagliariCagliariItaly

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