Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-23T00:05:41.415Z Has data issue: false hasContentIssue false

The effects of crude propolis, its volatiles and ethanolic extracts on the ecto-parasitic mite, Varroa destructor and health of the African savannah honey bee, Apis mellifera scutellata

Published online by Cambridge University Press:  17 February 2021

Beatrice T. Nganso*
Affiliation:
International Centre of Insect Physiology and Ecology, P. O. Box 30772-00100, Nairobi, Kenya
Baldwyn Torto
Affiliation:
International Centre of Insect Physiology and Ecology, P. O. Box 30772-00100, Nairobi, Kenya
*
Author for correspondence: Beatrice T. Nganso, E-mail: [email protected]

Abstract

Propolis is a hive product composed of biologically active plant resins, and has been shown to enhance individual honey bee (Apis mellifera L.) health. Propolis has also been demonstrated to mitigate, in part, the negative effects caused by the ecto-parasitic mite Varroa destructor and its associated viruses on the health of managed European honey bee colonies. However, its effect on the health status of African honey bees remains largely unknown. Here, we found that the African savannah honey bees, A. m. scutellata in Kenya, deposited approximately two and half-fold more propolis in their colonies during periods of increased than reduced worker brood rearing. This finding suggested that A. m. scutellata may use high quantities of propolis prophylactically to protect their young brood; yet, we observed no significant correlation between the quantity of propolis and the amount of worker brood or mite-infestation level on adult workers. Furthermore, whereas propolis volatiles or propolis placed in direct contact with the mites had no effect on mite survival under laboratory conditions, the ethanolic extract of propolis significantly reduced mite survival when compared with untreated control. These results suggest the presence of mite deterrent compounds in the ethanolic extract of the African honey bee propolis.

Type
Research Article
Copyright
Copyright © The Author(s) 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, DL and Trueman, JW (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology 24, 165189.CrossRefGoogle ScholarPubMed
Anjum, SI, Ullah, A, Khan, KA, Attaullah, M, Khan, H, Ali, H, Bashir, MA, Tahir, M, Ansari, MJ, Ghramh, HA and Adgaba, N (2019) Composition and functional properties of propolis (bee glue): a review. Saudi Journal of Biological Sciences 26, 16951703.CrossRefGoogle ScholarPubMed
Annoscia, D, Del Piccolo, F, Covre, F and Nazzi, F (2015) Mite infestation during development alters the in-hive behavior of adult honeybees. Apidologie 46, 306314.CrossRefGoogle Scholar
Bankova, V, Bertelli, D, Borba, R, Conti, BJ, da Silva Cunha, IB, Danert, C, Eberlin, MN, Falcão, SI, Isla, MI, Moreno, MIN and Papotti, G (2016) Standard methods for Apis mellifera propolis research. Journal of Apicultural Research 58, 149.CrossRefGoogle Scholar
Banskota, AH, Tezuka, Y and Kadota, S (2001) Recent progress in pharmacological research of propolis. Phytotherapy Research 15, 561571.CrossRefGoogle ScholarPubMed
Bastos, EM, Simone, M, Jorge, DM, Soares, AE and Spivak, M (2008) In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. Journal of Invertebrate Pathology 97, 273281.CrossRefGoogle ScholarPubMed
Borba, RS, Klyczek, KK, Mogen, KL and Spivak, M (2015) Seasonal benefits of a natural propolis envelope to honey bee immunity and colony health. Journal of Experimental Biology 218, 36893699.Google ScholarPubMed
Dalgaard, P (2008) Introductory Statistics with R, 2nd edition. New York: Springer Verlag.CrossRefGoogle Scholar
Damiani, N, Maggi, MD, Gende, LB, Faverin, C, Eguaras, MJ and Marcangeli, JA (2010) Evaluation of the toxicity of a propolis extract on Varroa destructor (Acari: Varroidae) and Apis mellifera (Hymenoptera: Apidae). Journal of Apicultural Research 49, 257264.CrossRefGoogle Scholar
Drescher, N, Klein, AM, Neumann, P, Yañez, O and Leonhardt, SD (2017) Inside honeybee hives: impact of natural propolis on the ecto-parasitic mite Varroa destructor and viruses. Insects 8, 15.CrossRefGoogle Scholar
Falcão, SI, Vale, N, Gomes, P, Domingues, MR, Freire, C, Cardoso, SM and Vilas-Boas, M (2013) Phenolic profiling of Portuguese propolis by LC–MS spectrometry: uncommon propolis rich in flavonoid glycosides. Phytochemical Analysis 24, 309318.CrossRefGoogle Scholar
Francis, RM, Nielsen, SL and Kryger, P (2013) Varroa-virus interaction in collapsing honey bee colonies. PLoS ONE 8, e57540.CrossRefGoogle ScholarPubMed
Garedew, A, Lamprecht, I, Schmolz, E and Schricker, B (2002) The varroacidal action of propolis: a laboratory assay. Apidologie 33, 4150.CrossRefGoogle Scholar
Garedew, A, Schmolz, E and Lamprecht, I (2003) Microcalorimetric and respirometric investigation of the effect of temperature on the anti Varroa action of the natural bee product-propolis. Thermochimica Acta 399, 171180.CrossRefGoogle Scholar
Gray, A, Brodschneider, R, Adjlane, N, Ballis, A, Brusbardis, V, Charrière, JD, Chlebo, R, Coffey, MF, Cornelissen, B, Amaro da Costa, C and Csáki, T (2019) Loss rates of honey bee colonies during winter 2017/18 in 36 countries participating in the COLOSS survey, including effects of forage sources. Journal of Apicultural Research 58, 479485.CrossRefGoogle Scholar
Hepburn, HR and Radloff, SE (1988) Honey Bees of Africa. Berlin, Heidelberg, New York: Springer Verlag.Google Scholar
Huang, S, Zhang, CP, Wang, K, Li, GQ and Hu, FL (2014) Recent advances in the chemical composition of propolis. Molecules 19, 1961019632.CrossRefGoogle ScholarPubMed
Kulhanek, K, Steinhauer, N, Rennich, K, Caron, DM, Sagili, RR, Pettis, JS, Ellis, JD, Wilson, ME, Wilkes, JT, Tarpy, DR and Rose, R (2017) A national survey of managed honey bee 2015–2016 annual colony losses in the USA. Journal of Apicultural Research 56, 328340.CrossRefGoogle Scholar
Lee, KV, Steinhauer, N, Rennich, K, Wilson, ME, Tarpy, DR, Caron, DM, Rose, R, Delaplane, KS, Baylis, K, Lengerich, EJ and Pettis, J (2015) A national survey of managed honey bee 2013–2014 annual colony losses in the USA. Apidologie 46, 292305.CrossRefGoogle Scholar
Lin, Z, Qin, Y, Page, P, Wang, S, Li, L, Wen, Z, Hu, F, Neumann, P, Zheng, H and Dietemann, V (2018) Reproduction of parasitic mites Varroa destructor in original and new honeybee hosts. Ecology and Evolution 8, 21352145.CrossRefGoogle ScholarPubMed
Locke, B (2012) Host-Parasite Adaptations and Interactions Between Honeybees, Varroa Mites and Viruses (Doctoral thesis). Swedish University of Agricultural Sciences, Uppsala.Google Scholar
Nganso, BT, Fombong, AT, Yusuf, AA, Pirk, CW, Stuhl, C and Torto, B (2017) Hygienic and grooming behaviors in African and European honeybees – new damage categories in Varroa destructor. PLoS ONE 12, e0179329.CrossRefGoogle ScholarPubMed
Nganso, BT, Fombong, AT, Yusuf, AA, Pirk, CW, Stuhl, C and Torto, B (2018) Low fertility, fecundity and numbers of mated female offspring explain the lower reproductive success of the parasitic mite Varroa destructor in African honeybees. Parasitology 145, 16331639.CrossRefGoogle ScholarPubMed
Nganso, BT, Mani, K, Altman, Y, Rafaeli, A and Soroker, V (2020) How crucial is the functional pit organ for the Varroa mite? Insects 11, 395.CrossRefGoogle ScholarPubMed
Nicodemo, D, De Jong, D, Couto, RHN and Malheiros, B (2013) Honey bee lines selected for high propolis production also have superior hygienic behavior and increased honey and pollen stores. Genetics and Molecular Research 12, 69316938.CrossRefGoogle ScholarPubMed
Nicodemo, D, Malheiros, EB, De Jong, D and Couto, RHN (2014) Increased brood viability and longer lifespan of honeybees selected for propolis production. Apidologie 45, 269275.CrossRefGoogle Scholar
Piepho, HP (2004) An algorithm for a letter-based representation of all-pairwise comparisons. Journal of Computational and Graphical Statistics 13, 456466.CrossRefGoogle Scholar
Plettner, E, Eliash, N, Singh, NK, Pinnelli, GR and Soroker, V (2017) The chemical ecology of host-parasite interaction as a target of Varroa destructor control agents. Apidologie 48, 7892.CrossRefGoogle Scholar
Popova, M, Reyes, M, Le Conte, Y and Bankova, V (2014) Propolis chemical composition and honeybee resistance against Varroa destructor. Natural Product Research 28, 788794.CrossRefGoogle ScholarPubMed
Potts, SG, Imperatriz-Fonseca, V, Ngo, HT, Aizen, MA, Biesmeijer, JC, Breeze, TD, Dicks, LV, Garibaldi, LA, Hill, R, Settele, J and Vanbergen, AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540, 220229.CrossRefGoogle ScholarPubMed
Pujirahayu, N, Ritonga, H and Uslinawaty, Z (2014) Properties and flavonoids content in propolis of some extraction method of raw propolis. International Journal of Pharmacy and Pharmaceutical Sciences 6, 338340.Google Scholar
Pusceddu, M, Floris, I, Mura, A, Theodorou, P, Cirotto, G, Piluzza, G, Bullitta, S, Angioni, A and Satta, A (2018) The effects of raw propolis on Varroa-infested honey bee (Apis mellifera) workers. Parasitology Research 117, 35273535.CrossRefGoogle ScholarPubMed
Ramsey, SD, Ochoa, R, Bauchan, G, Gulbronson, C, Mowery, JD, Cohen, A, Lim, D, Joklik, J, Cicero, JM, Ellis, JD and Hawthorne, D (2019) Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences 116, 17921801.CrossRefGoogle Scholar
R Development Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Roberts, JM, Anderson, DL and Tay, WT (2015) Multiple host shifts by the emerging honey bee parasite, Varroa jacobsoni. Molecular Ecology 24, 23792391.CrossRefGoogle Scholar
Rosenkranz, P, Aumeier, P and Ziegelmann, B (2010) Biology and control of Varroa destructor. Journal of Invertebrate Pathology 103, S96S119.CrossRefGoogle ScholarPubMed
Scrucca, L (2018) Dispmod: modelling dispersion in GLM. R package version 1.2. Retrieved from https://CRAN.R-project.org/package=dispmodGoogle Scholar
Simone-Finstrom, M and Spivak, M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41, 295311.CrossRefGoogle Scholar
Simone-Finstrom, MD and Spivak, M (2012) Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS ONE 7, e34601.CrossRefGoogle ScholarPubMed
Simone-Finstrom, M, Borba, RS, Wilson, M and Spivak, M (2017) Propolis counteracts some threats to honey bee health. Insects 8, 46.CrossRefGoogle ScholarPubMed
Simone, M, Evans, JD and Spivak, M (2009) Resin collection and social immunity in honey bees. Evolution: International Journal of Organic Evolution 63, 30163022.CrossRefGoogle ScholarPubMed
Therneau, TM (2020) A Package for Survival Analysis in R. R package version 3.2.7. Retrieved from https://CRAN.R-project.org/package=survival.Google Scholar
Wilson, MB, Spivak, M, Hegeman, AD, Rendahl, A and Cohen, JD (2013) Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees. PLoS ONE 8, e77512.CrossRefGoogle ScholarPubMed
Wilson, MB, Brinkman, D, Spivak, M, Gardner, G and Cohen, JD (2015) Regional variation in composition and antimicrobial activity of US propolis against Paenibacillus larvae and Ascosphaera apis. Journal of Invertebrate Pathology 124, 4450.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Nganso and Torto supplementary material

Figure S1

Download Nganso and Torto supplementary material(Image)
Image 5.7 MB