Apidologie

, Volume 41, Issue 3, pp 295–311 | Cite as

Propolis and bee health: the natural history and significance of resin use by honey bees

Open Access
Review Article

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.

Apis mellifera social immunity antimicrobial defense ecological immunity 

Propolis et santé de l’abeille : l’histoire naturelle et la signification de l’utilisation de résine végétale chez les abeilles

Apis mellifera immunité sociale défense antimicrobienne immunité écologique 

Propolis und Bienengesundheit: Die Naturgeschichte und die Bedeutung des Gebrauchs von Pflanzenharzen durch Bienen

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.

Apis mellifera Soziale Immunität antimikrobielle Abwehr ökologische Immunität 

References

  1. Alfonsus E.C. (1933) Some sources of propolis, Glean. Bee Cult. 61, 92–93.Google Scholar
  2. 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.PubMedGoogle Scholar
  3. Armbruster W.S. (1984) The role of resin in angiosperm pollination: ecological and chemical considerations, Am. J. Bot. 71, 1149–1160.Google Scholar
  4. Bankova V.S., de Castro S.L., Marcucci M.C. (2000) Propolis: recent advances in chemistry and plant origin, Apidologie 31, 3–15.Google Scholar
  5. 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.Google Scholar
  6. 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.Google Scholar
  7. 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.Google Scholar
  8. Banskota A.H., Tezuka Y., Kadota S. (2001) Recent progress in pharmacological research of propolis, Phytother. Res. 15, 561–571.PubMedGoogle Scholar
  9. 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.Google Scholar
  10. 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.PubMedGoogle Scholar
  11. Betts A. (1921) Propolising, Bee World 2, 131–132.Google Scholar
  12. Bogdanov S. (2006) Contaminants of bee products, Apidologie 37, 1–18.Google Scholar
  13. Bogdanov S., Kolchenmann V., Imdorf A. (1998) Acaricide residues in some bee products, J. Apic. Res. 37, 57–67.Google Scholar
  14. Butler C.G. (1949) The Honeybee: An introduction to her sense-physiology and behaviour, Oxford University Press, London.Google Scholar
  15. 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.Google Scholar
  16. Castella G., Chapuisat M., Christe P. (2008b) Prophylaxis with resin in wood ants, Anim. Behav. 75, 1591–1596.Google Scholar
  17. 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.Google Scholar
  18. 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.PubMedGoogle Scholar
  19. 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.PubMedGoogle Scholar
  20. Christe P., Oppliger A., Bancalà F., Castella G., Chapuisat M. (2003) Evidence for collective medication in ants, Ecol. Let. 6, 19–22.Google Scholar
  21. Clayton D.H., Wolfe N.D. (1993) The adaptive significance of self-medication, Trends Ecol. Evol. 8, 60–63.PubMedGoogle Scholar
  22. 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.PubMedGoogle Scholar
  23. Crane E. (1990) Bees and beekeeping, Cornell Univ. Press, Ithaca, N.Y.Google Scholar
  24. 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.PubMedGoogle Scholar
  25. Cremer S., Armitage S., Schmid-Hempel P. (2007) Social immunity, Curr. Biol. 17, R693-R702.PubMedGoogle Scholar
  26. Currie C.R., Stuart A.E. (2001) Weeding and grooming of pathogens in agriculture by ants, Proc. R. Soc. Lond. B 268, 1033–1039.Google Scholar
  27. 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.Google Scholar
  28. 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.Google Scholar
  29. 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.Google Scholar
  30. 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.Google Scholar
  31. 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.Google Scholar
  32. Evans J.D. (2003) Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae, J. Invertebr. Pathol. 83, 46–50.PubMedGoogle Scholar
  33. Evans J.D., Pettis J.S. (2005) Colony-level impacts of immune responsiveness in honey bees, Apis mellifera, Evolution 59, 2270–2274.PubMedGoogle Scholar
  34. Evans J.D., Spivak M. (2010) Socialized Medicine: Individual and communal disease barriers in honey bees, J. Invertebr. Pathol., 103, S62-S72.PubMedGoogle Scholar
  35. 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.PubMedGoogle Scholar
  36. 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.PubMedGoogle Scholar
  37. Fearnley J. (2001) Bee propolis: natural healing from the hive, Souvenir Press, London.Google Scholar
  38. Frazier M., Mullin C., Frazier J., Ashcraft S. (2008) What have pesticides got to do with it? Am. Bee J. 148, 521–523.Google Scholar
  39. Garedew A., Lamprecht I., Schmolz E., Schricker B. (2002) The varroacidal action of propolis: a laboratory assay, Apidologie 33, 41–50.Google Scholar
  40. 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.Google Scholar
  41. 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.Google Scholar
  42. 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.PubMedGoogle Scholar
  43. Ghisalberti E.L. (1979) Propolis: a review, Bee World 60, 59–84.Google Scholar
  44. 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.Google Scholar
  45. 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.PubMedGoogle Scholar
  46. 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.Google Scholar
  47. 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.Google Scholar
  48. 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.PubMedGoogle Scholar
  49. Haydak M.H. (1953) Propolis, Report Iowa State Apiarist, pp. 74–87.Google Scholar
  50. Hoyt M. (1965) The World of Bees, Coward McCann, Inc., New York.Google Scholar
  51. Huber F. (1814) New Observations Upon Bees, Translated by C.P. Dadant, 1926, American Bee Journal, Hamilton, IL.Google Scholar
  52. 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.PubMedGoogle Scholar
  53. Johnson B.R. (2008) Global information sampling in the honeybee, Naturwissenschaften 95, 523–530.PubMedGoogle Scholar
  54. 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.Google Scholar
  55. Johnson R.M., Ellis M.D., Mullin C.A., Frazier M. (2010) Pesticides and bee toxicity—USA, Apidologie 41, 312–331.Google Scholar
  56. 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.PubMedGoogle Scholar
  57. Jones R.J. (1980) Gallery construction by Nasutitermes costalis: polyethism and the behavior of individuals, Insectes Soc. 27, 5–28.Google Scholar
  58. 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.PubMedGoogle Scholar
  59. 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.Google Scholar
  60. Lee S.H., Bardunias P., Yang R.L. (2008) Behavioral response of termites to tunnel surface irregularity, Behav. Process 78, 397–400.Google Scholar
  61. 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.Google Scholar
  62. Lindenfelser L.A. (1967) Antimicrobial activity of propolis, Am. Bee J. 107, 90–92, 130–131.Google Scholar
  63. Lindenfelser L.A. (1968) In vivo activity of propolis against Bacillus larvae, J. Invertebr. Pathol. 12, 129–131.Google Scholar
  64. Lokvam J., Braddock J.F. (1999) Anti-bacterial function in the sexually dimorphic pollinator rewards of Clusia grandiflora (Clusiaceae), Oecologia 119, 534–540.Google Scholar
  65. Lozano G.A. (1998) Parasitic stress and self-medication in wild animals, Adv. Study Behav. 27, 291–317.Google Scholar
  66. 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.Google Scholar
  67. 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.Google Scholar
  68. 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.Google Scholar
  69. Messer A.C. (1985) Fresh dipterocarp resins gathered by Megechild bees inhibit growth of pollenassociated fungi, Biotropica 17, 175–176.Google Scholar
  70. Meyer W. (1956) Propolis bees and their activities, Bee World 37, 25–36.Google Scholar
  71. Milum V.G. (1955) Honey bee communication, Am. Bee J. 95, 97–104.Google Scholar
  72. Mlagan V., Sulimanovic D. 1982. Action of propolis solutions on Bacillus larvae, Apiacta 17, 16–20.Google Scholar
  73. Moret Y., Schmid-Hempel P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers, Science 290, 1166–1168.PubMedGoogle Scholar
  74. 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.Google Scholar
  75. 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.Google Scholar
  76. Nakamura J., Seeley T.D. (2006) The functional organization of resin work in honey bee colonies, Behav. Ecol. Sociobiol. 60, 339–349.Google Scholar
  77. 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.PubMedGoogle Scholar
  78. 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.PubMedGoogle Scholar
  79. 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.Google Scholar
  80. Page R.E. Jr., Fondrk M.K. (2004) Levels of behavioral organization and the evolution of division of labor, Naturwissenschaften 89, 91–106.Google Scholar
  81. 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.Google Scholar
  82. 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.PubMedGoogle Scholar
  83. 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.PubMedGoogle Scholar
  84. 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.Google Scholar
  85. Pereira A.S., Bicalho B., de Aquino Neto F.R. (2003) Comparison of propolis from Apis mellifera and Tetragonisca angustula, Apidologie 34, 291–298.Google Scholar
  86. 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.Google Scholar
  87. Popravko S.A., Sokolov M.V. (1980) Plant sources of propolis, Pchelovodstvo 2, 28–29.Google Scholar
  88. Ranger S., O’Donnell S. (1999) Genotypic effects on forager behavior in the neotropical stingless bee Partamona bilineata (Hymenoptera: Meliponidae), Naturwissenschaften 86, 187–190.Google Scholar
  89. Ratnieks F.L.W., Anderson C. (1999) Task partitioning in insect societies, Insectes Soc. 46, 95–108.Google Scholar
  90. Ribbands C.R. 1953. The Behaviour and Social Life of Honeybees, Bee Research Association, Ltd., London.Google Scholar
  91. 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.Google Scholar
  92. 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.PubMedGoogle Scholar
  93. Roubik D.W. (1989) Ecology and natural history of tropical bees, Cambridge University Press, Cambridge, MA.Google Scholar
  94. Roubik D.W. (2006) Stingless bee nesting biology, Apidologie 37, 124–143.Google Scholar
  95. Salatino A., Teixeira E.W., Negri G., Message D. (2005) Origin and chemical variation of Brazilian propolis, eCAM 2, 33–38.PubMedGoogle Scholar
  96. 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.Google Scholar
  97. 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.Google Scholar
  98. Schmid-Hempel P. (1998) Parasites in social insects, Princeton University Press, Princeton, New Jersey.Google Scholar
  99. Schmid-Hempel P., Ebert D. (2003) On the evolutionary ecology of specific immune defence, Trends Ecol. Evol. 18, 27–32.Google Scholar
  100. Seeley T.D., Morse R.A. (1976) The nest of the honeybee (Apis mellifera L.), Insectes Soc. 23, 495–512.Google Scholar
  101. Seeley T.D., Seeley R.H., Akratanakul P. (1982) Colony defense strategies of the honeybees in Thailand, Ecol. Monogr. 52, 43–63.Google Scholar
  102. 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.Google Scholar
  103. 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.Google Scholar
  104. Sforcin J.M. (2007) Propolis and immune system: a review, J. Ethnopharmacol. 113, 1–14.PubMedGoogle Scholar
  105. 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.PubMedGoogle Scholar
  106. 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.PubMedGoogle Scholar
  107. 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.Google Scholar
  108. 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.PubMedGoogle Scholar
  109. Simone M., Evans J., Spivak M. (2009). Resin collection and social immunity in honey bees, Evolution 63, 3016–3022.PubMedGoogle Scholar
  110. Spivak M. (1996) Honey bee hygienic behavior and defense against Varroa jacobsoni, Apidologie 27, 245–260.Google Scholar
  111. Starks P.T., Blackie C.A., Seeley T.D. (2000) Fever in honeybee colonies, Naturwissenschaften 87, 229–231.PubMedGoogle Scholar
  112. Tautz J. (2008) The buzz about bees: biology of a superorganism, Springer, Heidelberg, Germany.Google Scholar
  113. 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.PubMedGoogle Scholar
  114. 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.PubMedGoogle Scholar
  115. 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.Google Scholar
  116. Visscher P. (1980) Adaptations of honey bees (Apis mellifera) to problems of nest hygiene, Sociobiology 5, 249–260.Google Scholar
  117. 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.Google Scholar
  118. von Frisch K. (1993) The dance language and orientation of bees, Harvard Univ. Press, Cambridge, MA.Google Scholar
  119. Wallner K. (1999) Varroacides and their residues in bee products, Apidologie 30, 235–248.Google Scholar
  120. 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.PubMedGoogle Scholar
  121. 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.Google Scholar

Copyright information

© Springer S+B Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Ecology, Evolution and BehaviorUniversity of MinnesotaSt. PaulUSA
  2. 2.Department of EntomologyUniversity of MinnesotaSt. PaulUSA

Personalised recommendations