Abstract
Social immunity, which describes how individual behaviors of group members effectively reduce disease and parasite transmission at the colony level, is an emerging field in social insect biology. An understudied, but significant behavioral disease resistance mechanism in honey bees is their collection and use of plant resins. Honey bees harvest resins with antimicrobial properties from various plant species and bring them back to the colony where they are then mixed with varying amounts of wax and utilized as propolis. Propolis is an apicultural term for the resins when used by bees within a hive. While numerous studies have investigated the chemical components of propolis that could be used to treat human diseases, there is a lack of information on the importance of propolis in regards to bee health. This review serves to provide a compilation of recent research concerning the behavior of bees in relation to resins and propolis, focusing more on the bees themselves and the potential evolutionary benefits of resin collection. Future research goals are also established in order to create a new focus within the literature on the natural history of resin use among the social insects and role that propolis plays in disease resistance.
Zusammenfassung
Die „soziale Immunität“ als neues Forschungsfeld bei sozialen Insekten beschreibt, wie das individuelle Verhalten von Mitgliedern einer Gruppe wirkungsvoll die Verbreitung von Krankheiten und Parasiten auf der Ebene des Sozialstaates verhindern kann. Ein bisher zwar wenig untersuchtes aber wichtiges Verhaltensmerkmal zur Krankheitsabwehr bei Honigbienen ist die Verwendung von Pflanzenharzen. Honigbienen sammeln Harze mit antimikrobiellen Eigenschaften von verschiedenen Pflanzen, mischen diese dann im Bienenvolk mit unterschiedlichen Mengen von Wachs und benutzen dies als Propolis (Abb. 1–4). Propolis ist demnach der bienenkundliche Begriff für Harze, die im Bienenstock verwendet werden. Während es zahlreiche Untersuchungen zur Verwendung bestimmter Bestandteile des Propolis zur Krankheitsbekämpfung beim Menschen gibt, sind kaum Informationen über die Bedeutung von Propolis für die Bienengesundheit vorhanden.
Dieses Review ist eine Zusammenstellung neuerer Forschungsergebnisse zum Verhalten der Bienen in Bezug auf Harze und Propolis mit dem Schwerpunkt auf die möglichen evolutiven Vorteile des Harzsammelns für die Honigbienen. Die Verwendung von Harzen durch Bienenvölker (Apis mellifera) ist weit verbreitet. Während es erhebliche Unterschiede zwischen einzelnen Völkern bzgl. der Menge an gesammelten Harzen und Propolis gibt, scheinen alle — und dabei insbesondere die wildlebenden — Bienenvölker das Propolis zur Auskleidung des gesamten Stockinneren zu benutzen. Es wird angenommen, dass Propolis dazu beiträgt, die Homöostase innerhalb des Bienenstockes aufrecht zu erhalten. Konkret könnte das Propolis dabei das mikrobielle Wachstum an den Beutenwänden reduzieren, unkontrollierten Luftzug ins Beuteninnere verhindern und zusätzlich mechanische Barrieren gegenüber Eindringlingen bilden. Einige Forschungsprojekte zeigen eindeutig, dass Propolis im Bienenstock direkt gegenüber Krankheitserregern (z.B. Amerikanische Faulbrut) und Parasiten (z.B. Kleiner Beutenkäfer, Varroa destructor) wirkt. Daneben scheint es aber auch eine subtilere Wirkung über die Unterstützung des individuellen Immunsystems zu geben. Die weiteren Forschungen sollten sich auf das bessere Verständnis der Verwendung von Harzen durch Honigbienen und andere soziale Insekten konzentrieren. Dafür gibt es eine Vielzahl an Forschungsfeldern, von den pharmazeutischen Möglichkeiten des Propolis für die menschliche Gesundheit über die Mechanismen der Sammelstrategie von Propolis auf den Ebenen der Einzelbienen und des Bienenvolkes bis hin zu einer möglichen Anwendung von Propolis als Bekämpfung von Bienenkrankheiten. Schließlich ermöglichen Informationen zur Verwendung von Harzen und deren Aufnahme in den Bienenstock spannende Forschungsansätze zum Einfluss der Umwelt auf Krankheitsresistenz und soziale Immunität.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alfonsus E.C. (1933) Some sources of propolis, Glean. Bee Cult. 61, 92–93.
Antúnez K., Harriet J., Gende L., Maggi M., Eguaras M., Zunino P. (2008) Efficacy of natural propolis extract in the control of American Foulbrood, Vet. Microbiol. 131, 324–331.
Armbruster W.S. (1984) The role of resin in angiosperm pollination: ecological and chemical considerations, Am. J. Bot. 71, 1149–1160.
Bankova V.S., de Castro S.L., Marcucci M.C. (2000) Propolis: recent advances in chemistry and plant origin, Apidologie 31, 3–15.
Bankova V., Dyulgerov A., Popov S., Evstatieva L., Kuleva L., Pureb O., Zamjansan Z. (1992) Propolis produced in Bulgaria and Mongolia: phenolic composition and plant origin, Apidologie 23, 79–85.
Bankova V., Popova M., Trusheva B. (2006) Plant sources of propolis: an update from a chemist’s point of view, Nat. Prod. Commun. 1, 1023–1028.
Bankova V., Trusheva B., Popova M. (2008) New developments in propolis chemical diversity studies (since 2000), in: Oršolić N., Bašić I. (Eds.), Scientific evidence of the use of propolis in ethnomedicine.
Banskota A.H., Tezuka Y., Kadota S. (2001) Recent progress in pharmacological research of propolis, Phytother. Res. 15, 561–571.
Barth O.M. (2004) Melissopalynology in Brazil: A review of pollen analysis of honeys, propolis and pollen loads of bees, Sci. Agric. (Piracicaba, Brazil) 61, 342–350.
Bastos E.M.A.F., Simone M., Jorge D.M., Soares A.E.S., Spivak M. (2008) In vitro study of the antimicrobial activity of Brazilian and Minnesota, USA propolis against Paenibacillus larvae, J. Invertebr. Pathol. 97, 273–281.
Betts A. (1921) Propolising, Bee World 2, 131–132.
Bogdanov S. (2006) Contaminants of bee products, Apidologie 37, 1–18.
Bogdanov S., Kolchenmann V., Imdorf A. (1998) Acaricide residues in some bee products, J. Apic. Res. 37, 57–67.
Butler C.G. (1949) The Honeybee: An introduction to her sense-physiology and behaviour, Oxford University Press, London.
Castella G., Chapuisat M., Moret Y., Christe P. (2008a) The presence of conifer resin decreases the use of the immune system in wood ants, Ecol. Entomol. 33, 408–412.
Castella G., Chapuisat M., Christe P. (2008b) Prophylaxis with resin in wood ants, Anim. Behav. 75, 1591–1596.
Chaillou L.L., Nazareno M.A. (2009) Chemical variability in propolis from Santiago del Estero, Argentina, related to the arboreal environment as the sources of resins, J. Sci. Food Agric. 89, 978–983.
Chapuisat M., Oppliger A., Magliano P., Christe P. (2007) Wood ants use resin to protect themselves against pathogens, Proc. R. Soc. B. 274, 2013–2017.
Chen F., Chen L., Wang Q., Zhou J., Xue X., Zhao J. (2009) Determination of organochlorine pesticides in propolis by gas chromatography-electron capture detection using double column series solid-phase extraction, Anal. Bioanal. Chem. 393, 1073–9.
Christe P., Oppliger A., Bancalà F., Castella G., Chapuisat M. (2003) Evidence for collective medication in ants, Ecol. Let. 6, 19–22.
Clayton D.H., Wolfe N.D. (1993) The adaptive significance of self-medication, Trends Ecol. Evol. 8, 60–63.
Cox-Foster D.L., Conlan S., Holmes E.C., Palacios G., Evans J.D., Moran N.A., Quan P.-L., Briese T., Hornig M., Geiser D.M., Martinson V., vanEngelsdorp D., Kalkstein A.L., Drysdale A., Hui J., Zhai J., Cui L., Hutchison S.K., Simons J.F., Egholm M., Pettis J.S., Lipkin W.I. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder, Science 318, 283–287.
Crane E. (1990) Bees and beekeeping, Cornell Univ. Press, Ithaca, N.Y.
Cremer S., Sixt M. (2009) Analogies in the evolution of individual and social immunity, Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 129–142.
Cremer S., Armitage S., Schmid-Hempel P. (2007) Social immunity, Curr. Biol. 17, R693-R702.
Currie C.R., Stuart A.E. (2001) Weeding and grooming of pathogens in agriculture by ants, Proc. R. Soc. Lond. B 268, 1033–1039.
da Silva J.F.M., de Souza M.C., Matta S.R., de Andrade M.R., Vidal F.V.N. (2006). Correlation analysis between phenolic levels of Brazilian propolis extracts and their antimicrobial and antioxidant activities, Food Chem. 99, 431–435.
dos Santos C.G., Megiolaro F.L., Serrão J.E., Blochtein B. (2009) Morphology of the head salivary and intramandibular glands of the stingless bee Plebeia emerina (Hymenoptera: Meliponini) workers associated with propolis, Morphol. Histol. Fine Struct. 102, 137–143.
Downing H.A., Jeanne R.L. (1990) The regulation of complex behaviour in the paper wasp, Polistes fuscatus (Insecta, Hymenoptera, Vespidae), Anim. Behav. 39, 105–124.
Erber J., Pribbenow B. (2001) Antennal movements in the honeybee: How complex tasks are solved by a simple neuronal system, in: Cruse H. et al. (Eds.), Prerational intelligence: adaptive behavior and intelligent systems without symbols and logic, vol 1. Kluwer Academic, Netherlands.
Erber J., Pribbenow B., Grandy K., Kierzek S. (1997) Tactile motor learning in the antennal system of the honeybee (Apis mellifera L.), J. Comp. Physiol. A. 181, 355–365.
Evans J.D. (2003) Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae, J. Invertebr. Pathol. 83, 46–50.
Evans J.D., Pettis J.S. (2005) Colony-level impacts of immune responsiveness in honey bees, Apis mellifera, Evolution 59, 2270–2274.
Evans J.D., Spivak M. (2010) Socialized Medicine: Individual and communal disease barriers in honey bees, J. Invertebr. Pathol., 103, S62-S72.
Evans J.D., Aronstein K., Chen Y.P., Hetru C., Imler J.-L., Jiang H., Kanost M., Thompson G.J., Zou Z., Hultmark D. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645–656.
Farnesi A.P., Aquino-Ferreira R., De Jong D., Bastos J.K., Soares A.E.E. (2009) Effects of stingless bee and honey bee propolis on four species of bacteria, Genet. Mol. Res. 8, 635–640.
Fearnley J. (2001) Bee propolis: natural healing from the hive, Souvenir Press, London.
Frazier M., Mullin C., Frazier J., Ashcraft S. (2008) What have pesticides got to do with it? Am. Bee J. 148, 521–523.
Garedew A., Lamprecht I., Schmolz E., Schricker B. (2002) The varroacidal action of propolis: a laboratory assay, Apidologie 33, 41–50.
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, 171–180.
Garedew A., Schmolz E., Lamprecht I. (2004) Effect of the bee glue (propolis) on the calorimetrically measured metabolic rate and metamorphosis of the greater wax moth Galleria mellonella, Thermochim. Acta 413, 63–72.
Gekker G., Hu S., Spivak M., Lokensgard J.R., Peterson P.K. (2005) Anti-HIV-1 activity of propolis in CD4+ lymphocyte and microglial cell cultures, J. Ethnopharmacol. 102, 158–163.
Ghisalberti E.L. (1979) Propolis: a review, Bee World 60, 59–84.
Gonçalves-Alvim S.D.J. (2002) Resin-collecting bees (Apidae) on Clusia palmicida (Clusiaceae) in a riparian forest in Brazil, J. Trop. Ecol. 17, 149–153.
Greco M.K., Hoffmann D., Dollin A., Duncan M., Spooner-Hart R., Neumann, P. (2009) The alternative Pharaoh approach: stingless bees mummify beetle parasites alive, Naturwissenschaften 97, 319–323.
Greenaway W., Scaysbrook T., Whatley F.R. (1987) The analysis of bud exudate of Populus x euramericana, and of propolis, by gas chromatographymass spectrometry, Proc. R. Soc. London B 232, 249–272.
Greenaway W., Scaysbrook T., Whatley F.R. (1990) The composition and plant origins of propolis: a report of work at oxford, Bee World 71, 107–118.
Hart A.G., Bot A.N.M., Brown M.J.F. (2002) A colony-level response to disease control in a leaf-cutting ant, Naturwissenschaften 89, 275–277.
Haydak M.H. (1953) Propolis, Report Iowa State Apiarist, pp. 74–87.
Hoyt M. (1965) The World of Bees, Coward McCann, Inc., New York.
Huber F. (1814) New Observations Upon Bees, Translated by C.P. Dadant, 1926, American Bee Journal, Hamilton, IL.
Hunt G.J., Amdam G.V., Schlipalius D., Emore C., Sardesai N., Williams C.E., Rueppell O., Guzmán-Novoa E., Arechavaleta-Velasco M., Chandra S., Fondrk M.K., Beye M., Page R.E. Jr. (2007) Behavioral genomics of honeybee foraging and nest defense, Naturwissenschaften 94, 247–267.
Johnson B.R. (2008) Global information sampling in the honeybee, Naturwissenschaften 95, 523–530.
Johnson K.S., Eischen F.A., Giannasi D.E. (1994) Chemical composition of North American bee propolis and biological activity towards larvae of the greater wax moth (Lepidoptera: Pyralidae), J. Chem. Ecol. 20, 1783–1792.
Johnson R.M., Ellis M.D., Mullin C.A., Frazier M. (2010) Pesticides and bee toxicity—USA, Apidologie 41, 312–331.
Johnson R.M., Evans J.D., Robinson G.E., Berenbaum M.R. (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera), Proc. Natl. Acad. Sci. 106, 14790–14795.
Jones R.J. (1980) Gallery construction by Nasutitermes costalis: polyethism and the behavior of individuals, Insectes Soc. 27, 5–28.
Kujumgiev A., Tsvetkova I., Serkedjieva Yu., Bankova V., Christov R., Popov S. (1999) Antibacterial, antifungal and antiviral activity of propolis of different geographic origin, J. Ethnopharmacol. 64, 235–240.
Kumazawa S., Nakamura J., Murase M., Miyagawa M., Ahn M.-R., Fukumoto S. (2008) Plant origin of Okinawan propolis: honeybee behavior observation and phytochemical analysis, Naturwissenchaften 95, 781–786.
Lee S.H., Bardunias P., Yang R.L. (2008) Behavioral response of termites to tunnel surface irregularity, Behav. Process 78, 397–400.
Lehmberg L., Dwlrschak K., Blüthgen N. (2008) Defensive behavior and chemical deterrence against ants in the stingless bee genus Trigona (Apidae, Meliponini), J. Apic. Res. 47, 17–21.
Lindenfelser L.A. (1967) Antimicrobial activity of propolis, Am. Bee J. 107, 90–92, 130–131.
Lindenfelser L.A. (1968) In vivo activity of propolis against Bacillus larvae, J. Invertebr. Pathol. 12, 129–131.
Lokvam J., Braddock J.F. (1999) Anti-bacterial function in the sexually dimorphic pollinator rewards of Clusia grandiflora (Clusiaceae), Oecologia 119, 534–540.
Lozano G.A. (1998) Parasitic stress and self-medication in wild animals, Adv. Study Behav. 27, 291–317.
Manrique A.J., Soares A.E.E. (2002) Start of africanized honey bee selection program for increased propolis production and its effect on honey production, Interciencia 27, 312–316.
Markham K.R., Mitchell K.A., Wilkins A.L., Daldy J.A., Lu Y. (1996) HPLC and GC-MS identification of the major organic constituents in New Zealand propolis, Phytochemistry 42, 205–211.
Messer A.C. (1983) Chalicodoma pluto: the world’s largest bee rediscovered living communally in termite nests (Hymenoptera: Megachilidae), J. Kans. Entomol. Soc. 57, 165–168.
Messer A.C. (1985) Fresh dipterocarp resins gathered by Megechild bees inhibit growth of pollenassociated fungi, Biotropica 17, 175–176.
Meyer W. (1956) Propolis bees and their activities, Bee World 37, 25–36.
Milum V.G. (1955) Honey bee communication, Am. Bee J. 95, 97–104.
Mlagan V., Sulimanovic D. 1982. Action of propolis solutions on Bacillus larvae, Apiacta 17, 16–20.
Moret Y., Schmid-Hempel P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers, Science 290, 1166–1168.
Moritz R.F.A., de Miranda J., Fries I., Le Conte Y., Neumann P., Paxton R.J. (2010) Research strategies to improve honeybee health in Europe, Apidologie 41, 227–242.
Nagy E., Papay V., Litkei G., Dinya Z. (1986) Investigation of the chemical constituents, particularly the flavonoid components, of propolis and Populi gemma by the GC/MS method, Stud. Org. Chem. (Amsterdam) 23, 223–232.
Nakamura J., Seeley T.D. (2006) The functional organization of resin work in honey bee colonies, Behav. Ecol. Sociobiol. 60, 339–349.
Neumann P., Pirk C.W.W., Hepburn H.R., Solbrig A.J., Ratnieks F.L.W., Elzen P.J., Baxter J.R. (2001) Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.), Naturwissenschaften 88, 214–216.
Nyeko P., Edwards-Jones G., Day R.K. (2002) Honeybee, Apis mellifera (Hymenoptera: Apidae), leaf damage on Alnus species in Uganda: a blessing or curse in agroforestry? Bull. Entomol. Res. 92, 405–412.
Page R.E. Jr., Fondrk M.K. (1995) The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding, Behav. Ecol. Sociobiol. 36, 135–144.
Page R.E. Jr., Fondrk M.K. (2004) Levels of behavioral organization and the evolution of division of labor, Naturwissenschaften 89, 91–106.
Page R.E. Jr., Robinson G.E., Fondrk M.K., Nasr M.E. (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.), Behav. Ecol. Sociobiol. 36, 387–396.
Park Y.K., Paredes-Guzman J.F., Aguiar C.L., Alencar S.M., Fujiwara F.Y. (2004) Chemical constituents in Baccharis dracunculifolia as the main botanical origin of southeastern Brazilian propolis, J. Agric. Food Chem. 52, 1100–1103.
Patricio E.F.L.R.A., Cruz-Lopez L., Maile R., Tentschert J., Jones G.R., Morgan E.D. (2002) The propolis of stingless bees: terpenes from the tibia of three Frieseomelitta species, J. Insect Physiol. 48, 249–254.
Peev C., Vlase L., Dehelean C., Soica C., Feflea S., Alexa E. (2009) HPLC comparative analysis of polyphenolic content of propolis and black poplar foliar bud extracts, Proc. Actual Tasks Agric. Eng. 37, 395–404.
Pereira A.S., Bicalho B., de Aquino Neto F.R. (2003) Comparison of propolis from Apis mellifera and Tetragonisca angustula, Apidologie 34, 291–298.
Popova M.P., Bankova V.S., Bogdanov S., Tsvetkova I., Naydenski C., Marcazzan G.L., Sabatini A.G. (2007) Chemical characteristics of poplar type propolis of different geographic origin, Apidologie 38, 306–311.
Popravko S.A., Sokolov M.V. (1980) Plant sources of propolis, Pchelovodstvo 2, 28–29.
Ranger S., O’Donnell S. (1999) Genotypic effects on forager behavior in the neotropical stingless bee Partamona bilineata (Hymenoptera: Meliponidae), Naturwissenschaften 86, 187–190.
Ratnieks F.L.W., Anderson C. (1999) Task partitioning in insect societies, Insectes Soc. 46, 95–108.
Ribbands C.R. 1953. The Behaviour and Social Life of Honeybees, Bee Research Association, Ltd., London.
Rosengaus R.B., Maxmen A.B., Coates L.E., Traniello J.F.A. (1998) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoperta: Temopsidae), Behav. Ecol. Sociobiol. 44, 125–134.
Rothenbuhler W.C. (1964) Behaviour genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood, Am. Zool. 4, 111–123.
Roubik D.W. (1989) Ecology and natural history of tropical bees, Cambridge University Press, Cambridge, MA.
Roubik D.W. (2006) Stingless bee nesting biology, Apidologie 37, 124–143.
Salatino A., Teixeira E.W., Negri G., Message D. (2005) Origin and chemical variation of Brazilian propolis, eCAM 2, 33–38.
Samšiňáková A., Kálalová S., Haragsim O. (1977) Effects of some antimycotics and disinfectants on the Ascosphaera apis Maassen fungus in vitro, Z. Angew. Entomol. 84, 225–232.
Santana dos Santos T.F.S., Aquino A., Dórea H.S., Navickiene S. (2008) MSPD procedure for determining buprofezin, tetradifon, vinclozolin, and bifenthrin residues in propolis by gas chromatography-mass spectrometry, Anal. Bioanal. Chem. 390, 1425–1430.
Schmid-Hempel P. (1998) Parasites in social insects, Princeton University Press, Princeton, New Jersey.
Schmid-Hempel P., Ebert D. (2003) On the evolutionary ecology of specific immune defence, Trends Ecol. Evol. 18, 27–32.
Seeley T.D., Morse R.A. (1976) The nest of the honeybee (Apis mellifera L.), Insectes Soc. 23, 495–512.
Seeley T.D., Seeley R.H., Akratanakul P. (1982) Colony defense strategies of the honeybees in Thailand, Ecol. Monogr. 52, 43–63.
Seeley T.D., Kühnholz S., Weidenmüller A. (1996) The honeybee’s tremble dance stimulates additional bees to function as nectar receivers, Behav. Ecol. Sociobiol. 39, 419–427.
Seidel V., Peyfoon E., Watson D.G., Fearnley J. (2008) Comparative study of the antibacterial activity of propolis from different geographical and climatic zones, Phytotherapy Res. 22, 1256–1263.
Sforcin J.M. (2007) Propolis and immune system: a review, J. Ethnopharmacol. 113, 1–14.
Sforcin J.M., Fernandes A. Jr., Lopes C.A.M., Bankova V., Funari S.R.C. (2000) Seasonal effect on Brazilian propolis antibacterial activity, J. Ethnopharmacol. 73, 243–249.
Silici S., Kutluca S. (2005) Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region, J. Ethnopharmacol. 99, 69–73.
Silici S., Ünlü M., Vardar-Ünlü G. (2007) Antibacterial activity and phytochemical evidence for the plant origin of Turkish propolis from different regions, World J. Microbiol. Biotechnol. 23, 1797–1803.
Silva B.B., Rosalen P.L., Cury J.A., Ikegaki M., Souza V.C., Esteves A., Alencar S.M. (2008) Chemical composition and botanical origin of red propolis, a new type of Brazilian propolis, eCAM 5, 313–316.
Simone M., Evans J., Spivak M. (2009). Resin collection and social immunity in honey bees, Evolution 63, 3016–3022.
Spivak M. (1996) Honey bee hygienic behavior and defense against Varroa jacobsoni, Apidologie 27, 245–260.
Starks P.T., Blackie C.A., Seeley T.D. (2000) Fever in honeybee colonies, Naturwissenschaften 87, 229–231.
Tautz J. (2008) The buzz about bees: biology of a superorganism, Springer, Heidelberg, Germany.
Teixeira E.W., Negri G., Renata M.S.A.M., Message D., Salatino A. (2005) Plant origin of green propolis: bee behavior, plant anatomy and chemistry, eCAM 2, 85–92.
vanEngelsdorp D., Evans J.D., Donovall L., Mullin C., Frazier M., Frazier J., Tarpy D.R., Hayes J. Jr., Pettis J.S. (2009) “Entombed pollen”: a new condition in honey bee colonies associated with increased risk of colony mortality, J. Invertebr. Pathol. 101, 147–149.
Vardar-Ünlü G., Silici S., Ünlü M. (2008) Composition and in vitro antimicrobial activity of Populus buds and poplar-type propolis, World J. Microbiol. Biotechnol. 24, 1011–1017.
Visscher P. (1980) Adaptations of honey bees (Apis mellifera) to problems of nest hygiene, Sociobiology 5, 249–260.
Viuda-Martos M., Ruiz-Navajas Y., Fernández-López J., Pérez-Álvarez J.A. (2008) Functional properties of honey, propolis, and royal jelly, J. Food Sci. 73, 117–124.
von Frisch K. (1993) The dance language and orientation of bees, Harvard Univ. Press, Cambridge, MA.
Wallner K. (1999) Varroacides and their residues in bee products, Apidologie 30, 235–248.
Wilson-Rich N., Spivak M., Fefferman N.H., Starks P.T. (2009) Genetic, individual, and group facilitation of disease resistance in insect societies, Annu. Rev. Entomol. 54, 405–423.
Zhou J., Xue X., Li Y., Zhang J., Chen F., Wu L., Chen L., Zhao J. (2009) Multiresidue determination of tetracycline antibiotics in propolis by using HPLC-UV detection with ultrasonic-assisted extraction and two-step solid phase extraction, Food Chem. 115, 1074–1080.
Author information
Authors and Affiliations
Corresponding author
Additional information
Manuscript editor: Yves Le Conte
Rights and permissions
Open Access This is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License ( https://creativecommons.org/licenses/by-nc/2.0 ), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
About this article
Cite this article
Simone-Finstrom, M., Spivak, M. Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41, 295–311 (2010). https://doi.org/10.1051/apido/2010016
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1051/apido/2010016