Behavioral Responses of Apis mellifera Adult Workers to Odors from Healthy Brood and Diseased Brood

HongXia Zhao, Qin Liang, JiangHong Lee, XueFeng Zhang, WenZhong Huang, HuaSheng Cheng, YueXiong Luo

Abstract


Studies of adult workers’ responses to infected brood were undertaken to isolate discrete volatile compounds that elicited honeybee hygienic behavior. Using a freeze-killed brood assay, we determined that in healthy colonies adult workers recognized and emptied infected cells with a 95% clearance rate. SPME-GC-MS results emptied >95% infected cells indicated differences in the composition and relative content of volatile compounds released by healthy and diseased brood. Additionally, we determined that the main volatile compound released from the pathogen Ascosphaera apis was phenethyl alcohol. The Y-tube olfactometer indicated that 10- to 20-day-old workers of healthy colonies, but only 15-day-old workers of diseased colonies, were significantly sensitive to differences in characteristic volatile compounds. This information could facilitate honey bee selection based on mechanisms that contribute to chalkbrood disease tolerance.


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References


Aronstein KA, Murray KD. (2010). Chalkbrood disease in honey bees. Journal of Invertebrate Pathology, 103: 20-29.

Arathi HS, Burns I, Spivak M. (2000). Ethology of hygienic behavior in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioral repertoire of hygienic bees. Ethology, 106: 365-379.

Aupinel P, Medrzycki P, Fortini D, Michaud B, Tasei JN, Odoux JF. (2007). A new larval in vitro rearing method to test effects of pesticides on honey bee brood. Redia, 90, 91-94.

Aupinel P, Fortini D, Dufour H, Tasei, JN, Michaud B, Odoux JF, Pham-Delegue MH. (2005). Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bulletin of Insectology, 58: 107-111.

Aumeier P, Rosenkranz P, Francke W. (2002). Cuticular volatiles, attractivity of worker larvaeand invasion of brood cells by Varroa mites. A comparison of Africanized and European honeybees. Chemoecology, 12: 65-75.

Boecking O, Spivak M. (1999). Behavioral defenses of honey bees against Varroa jacobsoni Oud Apidologie, 30: 141-158.

Ben-Shahar Y, Leung HT, Pak WL. (2002). Division of labor in honey bee colonies is influenced by cGMP-dependent changes in phototaxis. Journal of Experimental Biology, 206: 2507-2515.

Ben-Shahar Y. (2005). The foraging gene, behavioral plasticity, and honey bee division of labor. Journal of Comparative Physiology, 191: 987-994.

Evans GW. (2004). The Environment of Childhood Poverty. American Psychologist, 59: 77-92.

Francesco N, Giorgio D, Mauro D. (2004). A semiochemical from brood cells infested by Varroa destructor triggers hygienic behaviour in Apis mellifera. Apidologie, 35: 65-70.

Gramacho KP, Spivak M. (2003). Differences in olfactory sensitivity and behavioral responses among honey bees bred for hygienic behavior. Behavioral Ecology and Sociobiology, 54: 472-479

Gregorc A, Ellis JD. (2011). Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides[J]. Pesticide Biochemistry and Physiology, 99: 200-207.

Gilley DC, DeGrandi H, offman G, Hooper J. (2006). Volatile compounds emitted by live European honey bee(Apis mellifera L.) queens[J]. Journal Insect Physiology, 52: 520-527.

Invernizzi C, Corbella E. (1999). Edad de las obreras que realizan comportamiento higiénico y otros comportamientos en lasabejas Apis mellifera. Revista de Etología, 2: 78-87.

Johnson BR. (2008a). Global information sampling in the honey bee. Naturwissenschaften, 95: 523-530.

Johnson BR. (2003). Organization of work in the honeybee: a compromise between division of labour and behavioural flexibility. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270: 147-152.

Kraus B. (1994). Factors influencing host choice of the honey bee parasite Varroa jacobsoni Oud. Experimental and Applied Acarology, 18: 435-443.

Kraus B. (1993). Preferences of Varroa jacobsoni for honey bees (Apis mellifera L.) of different ages. Journal of Apicultural Research, 32: 57-64.

Kraus B. (1990). Effects of honey-bee alarm pheromone compounds on the behaviour of Varroa jacobsoni. Apidologie, 21: 127-134.

LeConte Y, Hefetz A. (2008). Primer pheromones in social hymenoptera. Annual Review of Entomology, 53: 523-542.

Maisonnasse A, Lenoir JC, Beslay D, Crauser D, LeConte Y. (2010). E-β-ocimene, a Volatile Brood Pheromone Involved in Social Regulation in the Honey Bee Colony (Apis mellifera). PLoS ONE, 5(10): e13531. doi: 10.1371/ journal. pone. 0013531.

Maisonnasse A, Lenoir JC, Costagliola G, Beslay D, Choteau F. (2009). A scientific note on E-β-ocimene, a new volatile primer pheromone that inhibits worker ovary development in honey bees. Apidologie, 40: 562-564.

Masterman R, Ross R, Mesch KA, Spivak M. (2001). Olfactory and behavioral response thresholds to odors ofdiseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). Journal of Comparative Physiology A, 187: 441-452.

Martin C, Salvy M, Provost E, et al. (2001). Variations in chemical mimicry by the ectoparasitic mite Varroa jacobsoni to the developmental stage of the host honeybee Apis mellifera. Insect Biochemistry and Molecular Biology, 31: 365-379.

Masterman R, Smith BH, Spivak M. (1999). Brood odordiscrimination abilities in hygienic honey bees (Apis mellifera L.) using proboscis extension reflex conditioning. Insect Behavior, 13: 87-101.

Nazzi F, Milani N, Della VG, Nimis M. (2001). Semiochemicals from larval food affect the locomotory behaviour of Varroa destructor. Apidologie, 32: 149- 155.

Nazzi F, Della G. (2004). A semiochemical from brood cells infested by Varroa destructor triggers hygienic behaviour in Apis mellifera. Apidologie, 35: 65-70.

Nazzi F, Milani N, Della V. (2002). (Z)-8-Heptadecene from infested cells reduces the reproduction of Varroa destructor under laboratory conditions. Journal of Chemical Ecology, 28, 2181-2190.

Palacio MA, Rodriguez E, Spivak M. et al. (2010). Hygienic behaviors of honey bees in response to brood experimentally pinkilled or infected with Ascosphaera apis. Apidologie, 41: 602-612.

Reynald FJ, De Giusti MR, Alippi AM. (2004). Inhibition of the growth of Ascosphaera apis by Bacillus and Paenibacillus strains isolated from honey. Revista Argentina de Microbiologia, 36: 52-55.

Rothenbuhler WC. (1964). Behavior genetics of nest cleaning in honey bees. Responses of four inbred lines to disease-killed brood. Animal Behavior, 12: 578-583.

Spivak M, Masterman R, Ross R, Mesce KA. (2003). Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. Neurobiology, 55: 341-354.

Spivak M, Boecking O. (2001). Honey bee resistance to Varroa mites. In: Webster, T., Delaplane, K. (Eds.), Mites of the Honey Bee. Dadant & Sons, Hamilton, Illinois, 205-227.

Spivak M, Downey DL. (1998). Field assays for hygienic behavior in disease resistance in honey bees (Apidae: Hymenoptera). Journal of Economic Entomology, 91: 64-70.

Spivak M, Reuter GS. (1998a). Honey bee hygienic behavior. American Bee Journal, 138: 283-286.

Spivak M, Reuter GS. (1998b). Performance of hygienic honey bee colonies in a commercial apiary. Apidologie, 29, 285-302.

Swanson JA, Torto B, Kells SA, et al. (2009). Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. Journal of Chemical Ecology, 35: 1108-1116.

Vandenberg JD, Shimanuki H. (1987). Technique for rearing worker honeybees in the laboratory. Apiculture Research, 26: 90-97.

Wallner K. (1999). Varroacides and their residues in bee products. Apidologie, 30: 235-248.

Whitfield CW, Ben-Shahar Y, Brillet C, et al. (1987). The Biology of the Honey Bee, vol. viii. Harvard University Press, Cambridge, Mass. 281.

Wilson-Rich N, Spivak M, Fefferman NH, Starks PT. (2009). Genetic, individual, and group facilitation of disease resistance in insect societies. Annual Review of Entomology, 54: 405-423.




DOI: http://dx.doi.org/10.13102/sociobiology.v62i4.392

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