Pathogen-associated self-medication behavior in the honeybee Apis mellifera

Behavioral Ecology and Sociobiology

Volumn 68, Issue 11, 2014, Pages 1777-1784

  Gherman, Bogdan I ^a   Denner, Andreas ^a   Bobiş, Otilia ^a   Dezmirean, Daniel S ^a   Mărghitaş, Liviu A ^a   Schlüns, Helge ^a,d   Moritz, Robin F A ^a,b,c   Erler, Silvio ^a,b  

^a UNIVERSITY OF AGRICULTURAL SCIENCES AND VETERINARY MEDICINE   (Romania)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c UNIVERSITY OF PRETORIA   (South Africa)

^d UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Antimicrobial activity; Honey; Honeybee; Nosema ceranae; Social immunity; Therapeutic self medication

Indexed keywords

EID: 84939885384     PISSN: 03405443     EISSN: 14320762     Source Type: Journal    
DOI: 10.1007/s00265-014-1786-8     Document Type: Article

References (60)

1. Adams CJ, Boult CH, Deadman BJ, Farr JM, Grainger MN, Manley-Harris M, Snow MJ (2008) Isolation by HPLC and characterisation of the bioactive fraction of New Zealand manuka (Leptospermum scoparium) honey. Carbohydr Res 343:651–659. doi:10.1016/j.carres.2007.12.011
2. Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562–565. doi:10.1098/rsbl.2009.0986
3. Altaye SZ, Pirk CW, Crewe RM, Nicolson SW (2010) Convergence of carbohydrate-biased intake targets in caged worker honeybees fed different protein sources. J Exp Biol 213:3311–3318. doi:10.1242/jeb.046953
4. Beetsma J (1979) The process of queen-worker differentiation in the honeybee. Bee World 60:24–39
5. Blum MS, Novak AF, Taber S 3rd (1959) 10-Hydroxy-delta 2-decenoic acid, an antibiotic found in royal jelly. Science 130:452–453. doi:10.1126/science.130.3373.452
6. Camazine S (1991) Self-organizing pattern formation on the combs of honey bee colonies. Behav Ecol Sociobiol 28:61–76. doi:10.1007/BF00172140
7. Camazine S, Sneyd J, Jenkins MJ, Murray JD (1990) A mathematical model of self-organized pattern formation on the combs of honeybee colonies. J Theor Biol 147:553–571. doi:10.1016/S0022-5193(05)80264-4
8. Carson MC (1993) Simultaneous determination of multiple tetracycline residues in milk using metal chelate affinity chromatography. J AOAC Int 76:329–34
9. Castella G, Chapuisat M, Moret Y, Christe P (2008) The presence of conifer resin decreases the use of the immune system in wood ants. Ecol Entomol 33:408–412. doi:10.1111/j.1365-2311.2007.00983.x
10. 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. doi:10.1098/rspb.2007.0531
11. Christe P, Oppliger A, Bancalà F, Castella G, Chapuisat M (2003) Evidence for collective medication in ants. Ecol Lett 6:19–22. doi:10.1046/j.1461-0248.2003.00395.x
12. Clayton DH, Wolfe ND (1993) The adaptive significance of self-medication. Trends Ecol Evol 8:60–63. doi:10.1016/0169-5347(93)90160-Q
13. Crailsheim K (1998) Trophallactic interactions in the adult honeybee (Apis mellifera L.). Apidologie 29:97–112. doi:10.1051/apido:19980106
14. de Roode JC, Lefèvre T (2012) Behavioral immunity in insects. Insects 3:789–820. doi:10.3390/insects3030789
15. Dezmirean GI, Mărghitaş LA, Bobiş O, Dezmirean DS, Bonta V, Erler S (2012) Botanical origin causes changes in nutritional profile and antioxidant activity of fermented products obtained from honey. J Agric Food Chem 60:8028–8035. doi:10.1021/jf3022282
16. Dustmann JH (1979) Antibacterial effect of honey. Apiacta 1:1–4
17. Efem SE, Udoh KT, Iwara CI (1992) The antimicrobial spectrum of honey and its clinical significance. Infection 20:227–229. doi:10.1007/BF02033065
18. Evans JD, Schwarz RS (2011) Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 19:614–620. doi:10.1016/j.tim.2011.09.003
19. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15:645–656. doi:10.1111/j.1365-2583.2006.00682.x
20. Fries I, Feng F, da Silva A, Slemenda SB, Pieniazek NJ (1996) Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol 32:356–365. doi:10.1016/S0932-4739(96)80059-9
21. Fouks B, Lattorff HMG (2011) Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). PLoS One 6:e26328. doi:10.1371/journal.pone.0026328
22. Frost EH, Shutler D, Hillier NK (2012) The proboscis extension reflex to evaluate learning and memory in honeybees (Apis mellifera): some caveats. Naturwissenschaften 99:677–686. doi:10.1007/s00114-012-0955-8
23. Fujiwara S, Imai J, Fujiwara M, Yaeshima T, Kawashima T, Kobayashi K (1990) A potent antibacterial protein in royal jelly. purification and determination of the primary structure of royalisin. J Biol Chem 265:11333–11337
24. Galizia G, Eisenhardt D, Giurfa M (2011) Honeybee neurobiology and behavior: a tribute to Randolf Menzel. Springer, Berlin
25. Gilliam M, Taber S, Lorenz BJ, Prest DB (1988) Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis. J Invertebr Pathol 52:314–325. doi:10.1016/0022-2011(88)90141-3
26. Hart BL (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav R 14:273–294. doi:10.1016/S0149-7634(05)80038-7
27. Hart BL (2005) The evolution of herbal medicine: behavioural perspectives. Anim Behav 70:975-989. doi:10.1016/j.anbehav.2005.03.005
28. Herbert EW Jr (1992) Honey bee nutrition. In: The hive and the honey bee (edt. Graham, JM). Published by Dadant & Sons, pp.197–233.
29. Higes M, García-Palencia P, Martín-Hernández R, Meana A (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (microsporidia). J Invertebr Pathol 94:211–217. doi:10.1016/j.jip.2006.11.001
30. Higes M, Martín-Hernández R, Meana A (2010) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41:375–392. doi:10.1051/apido/2010019
31. Huang Q, Kryger P, Le Conte Y, Moritz RFA (2012) Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. J Invertebr Pathol 109:297–302. doi:10.1016/j.jip.2012.01.004
32. Keeling PJ, Fast NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol 56:93–116. doi:10.1146/annurev.micro.56.012302.160854
33. Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton RJ (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96:1–10. doi:10.1016/j.jip.2007.02.014
34. König B (1985) Plant sources of propolis. Bee World 66:136–139
35. König B, Dustmann JH (1986) Propolis und Viren: der gegenwärtige forschungsstand. Apidologie 17:334–336
36. Kwakman PH, te Velde AA, de Boer L, Speijer D, Vandenbroucke-Grauls CM, Zaat SA (2010) How honey kills bacteria. FASEB J 24:2576–2582. doi:10.1096/fj.09-150789
37. Lefèvre T, Chiang A, Kelavkar M, Li H, Li J, de Castillejo CL, Oliver L, Potini Y, Hunter MD, de Roode JC (2012) Behavioural resistance against a protozoan parasite in the monarch butterfly. J Anim Ecol 81:70–79. doi:10.1111/j.1365-2656.2011.01901.x
38. Lozano GA (1998) Parasitic stress and self-medication in wild animals. Adv Stud Behav 27:291–317. doi:10.1016/S0065-3454(08)60367-8
39. Malone LA, Gatehouse HS, Tregidga EL (2001) Effects of time, temperature, and honey on Nosema apis (Microsporidia: Nosematidae), a parasite of the honeybee, Apis mellifera (Hymenoptera: Apidae). J Invertebr Pathol 77:258–268. doi:10.1006/jipa.2001.5028
40. Manson JS, Otterstatter MC, Thomson JD (2010) Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162:81–89. doi:10.1007/s00442-009-1431-9
41. McArt SH, Koch H, Irwin RE, Adler LS (2014) Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecol Lett 17:624–636. doi:10.1111/ele.12257
42. Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13:758–768. doi:10.1038/nrn3357
43. Menzel R, Müller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379–404. doi:10.1146/annurev.ne.19.030196.002115
44. Nicolson SW, de Veer L, Köhler A, Pirk CWW (2013) Honeybees prefer warmer nectar and less viscous nectar, regardless of sugar concentration. Proc R Soc B 280:20131597. doi:10.1098/rspb.2013.1597
45. Oelschlaegel S, Pieper L, Staufenbiel R, Gruner M, Zeippert L, Pieper B, Koelling-Speer I, Speer K (2012) Floral markers of cornflower (Centaurea cyanus) honey and its peroxide antibacterial activity for an alternative treatment of digital dermatitis. J Agric Food Chem 60:11811–11820. doi:10.1021/jf303699t
46. Parker BJ, Barribeau SM, Laughton AM, de Roode JC, Gerardo NM (2011) Non-immunological defense in an evolutionary framework. Trends Ecol Evol 26:242–248. doi:10.1016/j.tree.2011.02.005
47. Pirk CWW, Human H, Crewe RM, vanEngelsdorp D (2014) A survey of managed honey bee colony losses in the Republic of South Africa—2009 to 2011. J Apicult Res 53:35–42. doi:10.3896/IBRA.1.53.1.03
48. Ratcliffe NA, Mello CB, Garcia ES, Butt TM, Azambuja P (2011) Insect natural products and processes: new treatments for human disease. Insect Biochem Mol Biol 41:747–769. doi:10.1016/j.ibmb.2011.05.007
49. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton
50. Seeley TD (1997) Honey bee colonies are group-level adaptive units. Am Nat 150(Suppl 1):S22–S41. doi:10.1086/286048
51. Seeley TD (2010) Honeybee democracy. Princeton University Press, Princeton
52. Seeley TD, Morse RA (1976) The nest of the honey bee (Apis mellifera L.). Insect Soc 23:495–512. doi:10.1007/BF02223477
53. Simone M, Evans JD, Spivak M (2009) Resin collection and social immunity in honey bees. Evolution 63:3016–3022. doi:10.1111/j.1558-5646.2009.00772.x
54. Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41:295–311. doi:10.1051/apido/2010016
55. Simone-Finstrom MD, Spivak M (2012) Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS One 7:e34601. doi:10.1371/journal.pone.0034601
56. Strassmann J (2001) The rarity of multiple mating by females in the social hymenoptera. Insect Soc 48:01–13. doi:10.1007/PL00001737
57. Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J, Pérez-Alvarez JA (2008) Functional properties of honey, propolis, and royal jelly. J Food Sci 73:R117–124. doi:10.1111/j.1750-3841.2008.00966.x
58. Walker P, Crane E (1987) Constituents of propolis. Apidologie 18:327–334. doi:10.1051/apido:19870404
59. White JW Jr, Subers MH, Schepartz AI (1963) The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system. Biochim Biophys Acta 73:57–70. doi:10.1016/0926-6569(63)90108-1
60. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT (2009) Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 54:405–423. doi:10.1146/annurev.ento.53.103106.093301