BAL ARILARINDA SOSYAL VE BİREYSEL BAĞIŞIKLIK

Yıl 2020, Cilt: 20 Sayı: 2, 232 - 256, 09.11.2020

Ayşe Ebru Borum

https://doi.org/10.31467/uluaricilik.790629

Öz

Bal arıları, doğal ekosistem ve tarımsal alanda tozlaşmada oldukça önemli rol oynarlar. Patojenler (Parazit,mantar, virüs ve bakteriler), ekosistem değişikliği ya da kayıpları, zirai kimyasal kullanımı gibi birçok biyotik ve abiyotik stres faktörü tek başına ya da birlikte arı kolonisinin, sağlık ve yaşamını olumsuz olarak etkilemektedir. Tüm bu faktörler arıların bağışıklık sistemini etkileyerek savunma mekanizmalarını değiştirir.
Bal arıları kendilerini infeksiyöz ve paraziter etkenlere karşı korumak için fiziksel bariyerler, genelleşmiş hücresel ve humoral immun yanıttan oluşan doğal bir immun sisteme sahiptir.
Patojenler, akarisitler, fungisitler, herbisitler ve diğer böcek ilaçları arı bağışıklık sistemini ve dolayısıyla arı sağlığını etkiler. Arı bağışıklık sisteminin savunma mekanizmaları sinyal yollarını, patojen tanıma reseptörlerini ve doğal bağışıklık sistemi efektörlerini içerir. Bal arısı kolonilerindeki, salgın infeksiyon riski, bireysel ve sosyal bağışıklık ile azaltılır. Her iki bağışıklık türü birlikte çeşitli düzeylerde hastalıklardan korur, oluşan paraziter ya da diğer infeksiyöz hastalıklara karşı immun yanıt oluşmasında önemli rol oynarlar.

Anahtar Kelimeler

Bal Arısı, Patojen, Bireysel Bağışıkılık, Sosyal Bağışıklık

Social Immunity and Individual Immunity in Honey Bees

Öz

Honey bees play an important role in pollination in the natural ecosystem and agricultural field. Many biotic and abiotic stress factors such as pathogens (parasites, fungi, viruses and bacteria), ecosystem changes or losses, use of agricultural chemicals, alone or in combination, adversely affect the health and life of the bee colony. All these factors affect the immune system of the bees and change their defense mechanisms.
Honey bees have a natural immune system consisting of physical barriers, generalized cellular and humoral immune response to protect themselves against infectious and parasitic agents.
Pathogens, acaricides, fungicides, herbicides and other pesticides affect the bee immune system and hence bee health. Defense mechanisms of the bee immune system include signaling pathways, pathogen recognition receptors and innate immune system effectors. The risk of epidemic infection in honey bee colonies is reduced by individual and social immunity. Both types of immunity protect from diseases at various levels and play an important role in the formation of immune response against parasitic or other infectious diseases.

Anahtar Kelimeler

Honey Bees, Pathogens, Individual Immunity, Social Immunity

Kaynakça

• Agaisse, H., Perrimon, N. 2004. The roles of JAK/STAT signaling in Drosophila immune responses.Immunol Rev. 198:72-82., doi:10.1111/j.0105-2896.2004.0133.x.
• Alaux, C., Robinson, GE.2007. Alarm pheromone induces immediate-early gene expression and slow behavioral response in honey bees. J Chem Ecol. 33(7):1346-1350., doi:10.1007/s10886-007-9301-6.
• Anderson, KE., Sheehan, TH., Mott, BM., Maes, P., Snyder, L., Schwan, MR., Walton, A., Jones, BM., Corby-Harris, V. 2013. Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One. 8(12):e83125., doi:10.1371/journal.pone.0083125.
• Annoscia, D., Brown, SP., Di Prisco, G., et al. 2019. Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model. Proceedings. Biological Sciences 286(1901):20190331., doi: 10.1098/rspb.2019.0331.
• Antunez, 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 (3-4): 324–331., doi: 10.1016/j.vetmic.2008.04.011.
• Arathi, HS., Burns, I., Spivak, M. 2000. Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): Behavioural repertoire of hygienic bees. Ethology. 106(4): 365-379., doi.: 10.1046/j.1439-0310.2000.00556.x.
• Arathi, HS., Ho, G., Spivak, M. 2006. Inefficient task partitioning among nonhygienic honeybees, Apis mellifera L., and implications for disease transmission. Anim Behav. 72, 431–438., doi: 10.1016/j.anbehav.2006.01.018.
• Arechavaleta-Velasco, M., Guzman-Novoa, E. 2001. Relative effect of four characteristics that restrain the population growth of the mite Varroa destructor in honey bee (Apis mellifera) colonies. Apidologie. 32: 157–174., doi: 10.1051/apido:2001121.
• Aumeier, P., Rosenkranz, P., Goncalves, L.S., 2000. A comparison of the hygienic response of Africanized and European (Apis mellifera carnica) honey bees to Varroa-infested brood in tropical Brazil. Gen Mol Biol. 23 (4): 787–791., doi: 10.1590/S1415-47572000000400013.
• Bailey, L. 1999. The quest for a super-bee. Bee World. 80: 55–60. doi:10.1080/0005772X.1999.11099427.
• Baracchi, D., Fadda, A., Turillazzi, S. 2012. Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J Insect Physiol. 58(12):1589-1596., doi:10.1016/j.jinsphys.2012.09.014.
• Baracchi, D., Cini, A. 2014. A socio-spatial combined approach confirms a highly compartmentalised structure in honeybees. Ethology. 120: 1167–1176., doi: 10.1111/eth.12290.
• Barnett JR. 2004. Langenheim, J.H. Plant resins: chemistry, evolution, ecology and ethnobotany. Ann Bot. 93(6):784-785., doi:10.1093/aob/mch103.
• Barribeau, SM., Sadd, BM., du Plessis, L., Brown, MJ., Buechel, SD., Cappelle, K., Carolan, JC., Christiaens, O., Colgan, TJ., Erler, S., et al. 2015. A depauperate immune repertoire precedes evolution of sociality in bees. Genome Biol., 16: 83–103., doi: 10.1186/s13059-015-0628-y.
• Blum, MS., Novak, AF., Taber, S. 3rd. 1959. 10-Hydroxy-delta 2-decenoic acid, an antibiotic found in royal jelly. Science 130(3373):452-453., doi:10.1126/science.130.3373.452.
• Boecking, O., Drescher, W. 1991. Response of Apis mellifera L. colonies infested with Varroa jacobsoni Oud. Apidologie. 22 (3): 237–241., doi: 10.1051/apido:19910308.
• Boecking, O., Spivak, M., 1999. Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie. 30: 141–158., doi: 10.1051/apido:19990205.
• Boncristiani, H., Underwood, R., Schwarz, R., Evans, JD., Pettis, J., vanEngelsdorp, D. 2012. Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J Insect Physiol. 58(5): 613–620., doi:10.1016/j.jinsphys.2011.12.011.
• Borba, RS. 2015. Constitutive and therapeutic benefits of plant resins and a propolis envelope to honey bee, Apis mellifera L., immunity and health. (3734812 Ph.D.), University of Minnesota, Ann Arbor.
• Brodschneider, R., Crailsheim, K. 2010. Nutrition and health in honey bees. Apidologie. 41 (3):278-294., doi:10.1051/apido/2010012.
• Brown, GD., Gordon, S. 2003. Fungal beta-glucans and mammalian immunity. Immunity 19(3):311-315., doi:10.1016/s1074-7613(03)00233-4.
• Burritt, NL., Foss, NJ., Neeno-Eckwall, EC., Church, JO., Hilger, AM., Hildebrand, JA., Warshauer, DM., Perna, NT., Burritt, JB. 2016. Sepsis and Hemocyte Loss in Honey Bees (Apis mellifera) Infected with Serratia marcescens Strain Sicaria. PloS one, 11(12): e0167752., doi: 10.1371/journal.pone.0167752.
• Brutscher, LM., Daughenbaugh, KF., Flenniken, ML. 2015. Antiviral defense mechanisms in honey bees. Curr Opin Insect Sci.10:71–82., doi: 10.1016/j.cois.2015.04.016.
• Chan, QWT., Melathopoulos, AP., Pernal, SF., Foster, L.J. 2009. The innate and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genom. 10: 387., doi:10.1186/1471-2164-10-387.
• Christe, P., Oppliger, A., Bancalà, F., Castella, G. and Chapuisat, M. 2003. Evidence for collective medication in ants. Ecol Lett. 6: 19-22., doi:10.1046/j.1461-0248.2003.00395.x.
• Cornman, RS., Chen, YP., Schatz, MC., Street, C., Zhao, Y., Desany, B., Egholm, M., Hutchison, S., Pettis, JS., Lipkin, WI., Evans, JD. 2009. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS pathog. 5(6): e1000466., doi:10.1371/journal.ppat.1000466.
• Corby-Harris, V., Maes, P., Anderson, KE. 2014. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS One. 9(4):e95056., doi:10.1371/journal.pone.0095056.
• Crailsheim, K., Riessberger-Gallé, U. 2001. Honey bee age-dependent resistance against American foulbrood. Apidologie 32: 91-104., doi:10.1051/apido:2001114.
• Cremer, S., Armitage, SA., Schmid-Hempel, P. 2007. Social immunity. Curr Biol. 2007;17(16): R693-R702., doi:10.1016/j.cub.2007.06.008.
• Cremer, S., Sixt, M. 2009. Analogies in the evolution of individual and social immunity. Philos Trans R Soc Lond B Biol Sci. 364(1513):129-142., doi:10.1098/rstb.2008.0166.
• Danka, RG., Villa, J.D., 1998. Evidence of autogrooming as a mechanism of honey bee resistance to tracheal mite infestation. J Apic Res. 37: 39–46., doi: 10.1080/00218839.1998.11100953.
• Danka, RG., Villa, D., 2000. Inheritance of resistance to Acarapis woodi (Acari: Tarsonemidae) in first-generation crosses of honey bees (Hymenoptera: Apidae). J Econ Entomol. 93: 1602–1605., doi: 10.1603/0022-0493-93.6.1602.
• Danka, RG., Harris, JW., Dodds, GE. 2016. Selection of VSH-derived “Pol-line” honey bees and evaluation of their Varroa-resistance characteristics. Apidologie. 47, 483–490., doi: 10.1007/s13592-015-0413-7.
• de Graaf, D., Dauwe, R., Walravens, K., Jacobs, F. 2002. Flow cytometric analysis of lectin-stained haemocytesof the honeybee ( Apis mellifera ). Apidologie. 33: 571-579., doi: 10.1051/apido:2002041.
• DeGrandi-Hoffman, G., Chen, Y. 2015. Nutrition, immunity and viral infections in honey bees. Curr Opin Insect Sci. 10:170–176., doi: 10.1016/j.cois.2015.05.007.
• de Roode, JC., Lefèvre, T. 2012. Behavioral Immunity in Insects. Insects. 3(3):789-820., doi:10.3390/insects3030789.
• Dolezal, AG., Toth, AL. 2018. Feedbacks between nutrition and disease in honey bee health. Curr Opin Insect Sci. 26:114-119., doi: 10.1016/j.cois.2018.02.006.
• Drescher, N., Wallace, HM., Katouli, M., Massaro, CF., Leonhardt, SD. 2014. Diversity matters: how bees benefit from different resin sources. Oecologia. 76(4):943-953., doi:10.1007/s00442-014-3070-z.
• Drescher, N., Klein, AM., Neumann, P., Yañez, O., Leonhardt, SD. 2017. Inside Honeybee Hives: Impact of Natural Propolis on the Ectoparasitic Mite Varroa destructor and Viruses. Insects. 8(1):15., doi:10.3390/insects8010015
• Dubovskiy, I., Kryukova, N., Glupov, V., Ratcliffe, N. 2016. Encapsulation and nodulation in insects. Invert Surviv J. 13(1): 229-246., doi:10.25431/1824-307X/isj.v13i1.229-246.
• Eckholm, BJ., Anderson, KE., Weiss, M., DeGrandi- Hoffman, G. 2011. Intracolonial genetic diversity in honeybee (Apis mellifera) colonies increases pollen foraging efficiency. Behav Ecol Sociobiol. 65: 1037–1044., doi: 10.1007/s00265-010-1108-8.
• Ekengren, S., Hultmark, D. 2001. A family of Turandot-related genes in the humoral stress response of Drosophila. Biochem Biophys Res Commun. 284(4):998-1003., doi:10.1006/bbrc.2001.5067.
• Ekengren, S., Tryselius, Y., Dushay, M. S., Liu, G., Steiner, H., Hultmark, D. 2001. A humoral stress response in Drosophila. Curr Biol. 11(18):1479., doi:10.1016/s0960-9822(01)00452-3.
• Eleftherianos, I., Felföldi, G., ffrench-Constant, RH., Reynolds, SE. 2009. Induced nitric oxide synthesis in the gut of Manduca sexta protects against oral infection by the bacterial pathogen Photorhabdus luminescens. Insect Mol Biol. 18(4):507-516., doi:10.1111/j.1365-2583.2009.00899.x.
• Ellis, JD., Hepburn, R., Delaplane, KS., Elzen, PJ. 2003. A scientific note on small hive beetle (Aethina tumida) oviposition and behaviour during European (Apis mellifera) honey bee clustering and absconding events. J Apic. Res. 42: 47–48., doi:10.1080/00218839.2003.11101089.
• Esch, H. 1960. Über die Körpertemperaturen und den Wärmehaushalt von Apis mellifica. Z. Vergl. Physiol. 43: 305–335., doi: 10.1007/BF00298066.
• Evans, JD., Armstrong, TN., 2005. Inhibition of the American foulbrood bacterium, Paenibacillus larvae, by bacteria isolated from honey bees. J Apic. Res. 44: 168–171., doi: 10.1080/00218839.2005.11101173.
• Evans, JD. 2006. Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease. J Invertebr Pathol. 93(2): 135–139., doi:10.1016/j.jip.2006.04.004
• Evans, JD., Armstrong, TN. 2006. Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecology 6 (4): 1-9., doi:10.1186/1472-6785-6-4.
• 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 (5): 645–656., doi: 10.1111/j.1365-2583.2006.00682.x.
• Evans, JD., Spivak, M. 2010. Socialized medicine: Individual and communal disease barriers in honey bees. J Invertebr Pathol. 103 (Supplement): S62–S72., doi: 10.1016/j.jip.2009.06.019.
• Evison, SE., Fazio, G., Chappell, P., Foley, K., Jensen, AB., Hughes, WO. 2013. Host-parasite genotypic interactions in the honey bee: the dynamics of diversity. Ecol Evol. 3(7):2214-2222., doi:10.1002/ece3.599.
• Gábor, E., Cinege, G., Csordás, G., Török, T., Folkl-Medzihradszky, K., Darula, Z., Ando, I., Kurucz, E. 2017. Hemolectin expression reveals functional heterogeneity in honey bee (Apis mellifera) hemocytes. Dev Comp Immunol. 76:403-411., doi: 10.1016/j.dci.2017.07.013.
• Galbraith, DA., Yang, X., Niño, EL., Yi S, Grozinger, C. 2015. Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). PLoS Pathog. 11(3): e1004713., doi:10.1371/journal.ppat.1004713.
• Genç, M., Genç, F. 2019. Stress Factors on Honey Bees (Apis mellifera L.) and The Components of Their Defense System Against Diseases, Parasites, and Pests. Mellifera 19 (1): 7-20.
• Ghisalberti, EL. 1979. Propolis: A Review. Bee World. 60(2): 59-84., doi:10.1080/0005772X.1979.11097738.
• Gillespie, JP., Kanost, MR., Trenczek, T. 1997. Biological mediators of insect immunity. Annu Rev Entomol. 42:611-643., doi:10.1146/annurev.ento.42.1.611.
• Gilliam, M. 1997. Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett. 155:1–10., doi: 10.1111/j.1574-6968.1997.tb12678.x.
• González‐Santoyo, I., Córdoba‐Aguilar, A. 2012. Phenoloxidase: a key component of the insect immune system. Entomol Exp et Appl. 142: 1-16., doi:10.1111/j.1570-7458.2011.01187.x.
• Graveley, BR., Kaur, A., Gunning, D., Zipursky, SL., Rowen, L., Clemens, JC. 2004. The organization and evolution of the dipteran and hymenopteran Down syndrome cell adhesion molecule (Dscam) genes. RNA (New York, N.Y.) 10(10): 1499–1506., doi:10.1261/rna.7105504.
• Gupta, L., Molina-Cruz, A., Kumar, S., Rodrigues, J., Dixit, R., Zamora, R. E., Barillas-Mury, C. 2009. The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe. 5(5):498-507., doi:10.1016/j.chom.2009.04.003.
• Guzman-Novoa, E. 2011. Integration biotechnologies. Genetic basis of disease resistance in the honey bee (Apis mellifera). In: Murray M-Y editor. Comprehensive biotechnology, Second ed. Elsevier (4):763-767.
• Haine, ER., Moret, Y., Siva-Jothy MT., Rolff, J. 2008. Antimicrobial defense and persistent infection in insects. Science.;322(5905):1257-1259., doi:10.1126/science.1165265.
• Hamilton, C., Lejeune, BT., Rosengaus, RB. 2011. Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus. Biol Lett. 7(1):89-92., doi:10.1098/rsbl.2010.0466.
• Harbo, JR., Harris, JW. 2001. Resistance to Varroa destructor (Mesostigmata: Varroidae) when mite-resistant queen honey bees (Hymenoptera: Apidae) were free-mated with unselected drones. J Econ Entomol. ,94 (6): 1319–1323.
• Harbo, JR., Harris, JW. 2005. Suppressed mite reproduction explained by the behaviour of adult bees. J. Apic. Res., 44 (1): 21–23., doi: 10.1080/00218839.2005.11101141.
• Haydak, M., 1945. The language of the honeybee. American Bee Journal. 85: 316–317.
• Hernández López, J., Schuehly, W., Crailsheim, K., Riessberger-Gallé, U. 2014. Trans-generational immune priming in honeybees. Proceedings. Biological sciences, 281(1785):20140454., doi:10.1098/rspb.2014.0454.
• Hoffmann, JA. 2003. The immune response of Drosophila. Nature 426(6962):33-38., doi:10.1038/nature02021.
• Hultmark, D. 2003. Drosophila immunity: paths and patterns. Curr Opin Immunol. 15(1):12–19., doi:10.1016/s0952-7915(02)00005-5.
• Jander, R., 1976. Grooming and pollen manipulation in bees (Apoidea): the natüre and evolution of movements involving the foreleg. Physiological Entomology. 1: 179–194., doi: 10.1111/j.1365-3032.1976.tb00960.x.
• Johnson, BR. 2010. Division of labor in honeybees: form, function, and proximate mechanisms. Behav Ecol Sociobiol. 64: 305–316., doi: 10.1007/s00265-009-0874-7.
• Jones, JC., Myerscough, MR., Graham, S., Oldroyd, B. P.2004. Honey bee nest thermoregulation: diversity promotes stability. Science. 305(5682):402-404., doi:10.1126/science.1096340.
• Kingsolver, MB., Huang, Z., Hardy, RW. 2013. Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol. 425(24):4921-4936., doi:10.1016/j.jmb.2013.10.006.
• Koch, H., Schmid-Hempel, P. 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci U S A.108(48):19288-19292., doi:10.1073/pnas.1110474108.
• Koch, H., Brown, MJF., Stevenson, PC. 2017. The role of disease in bee foraging ecology. Curr Opin Insect Sci. 21: 60-67., doi:10.1016/j.cois.2017.05.008
• Koleoglu, G., Goodwin, P.H., Reyes-Quintana, M., Hamudizzaman, MM., Guzman-Novoa, E. 2018. Varroa destructor parasitism reduces hemocyte concentrations and prophenol oxidase gene expression in bees from two populations. Parasitol Res 117: 1175–1183., doi:10.1007/s00436-018-5796-8.
• Konrad, M., Vyleta, ML., Theis, FJ., Stock, M., Tragust, S., Klatt, M., Drescher, V., Marr, C., Ugelvig, LV., Cremer, S. 2012. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biol. 10(4): e1001300., doi:10.1371/journal.pbio.1001300.
• Korayem, AM., Fabbri, M., Takahashi, K., Scherfer, C., Lindgren, M., Schmidt, O., Ueda, R., Dushay, MS., Theopold, U. 2004. A Drosophila salivary gland mucin is also expressed in immune tissues: evidence for a function in coagulation and the entrapment of bacteria. Insect Biochem Mol Biol. 34(12):1297-1304., doi 10.1016/j.ibmb.2004.09.001.
• Korayem, AM., Khodairy, MM., Abdel-Aal, AAA., El-Sonbaty, AA. 2012. The protective strategy of antioxidant enzymes against hydrogen peroxide in honey bee, Apis mellifera during two different seasons. J. Biol. Earth Sci. 2: B93–B109.
• Kurata, S. 2014. Peptidoglycan recognition proteins in Drosophila immunity. Dev Comp Immunol.42(1):36-41., doi:10.1016/j.dci.2013.06.006.
• Lamattina, L., Eguaras, M. 2019. Towards Precision Nutrition: A Novel Concept Linking Phytochemicals, Immune Response and Honey Bee Health Insects, 10 (11): 401., doi: 10.3390/insects10110401.
• Lapidge, KL., Oldroyd, B.P., Spivak, M. 2002. Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Naturwissenschaften. 89: 565–568., doi:10.1007/s00114-002-0371-6.
• Larsen, A., Reynaldi, JF., Guzmán-Novoa, E. 2019. Fundaments of the honey bee (Apis mellifera) immune system. Review. Rev Mex Cienc Pecu 10(3):705-728., doi: 10.22319/rmcp.v10i3.4785.
• Laughton, AM., Boots, M., Siva-Jothy, MT. 2011. The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge. J Insect Physiol. 57(7):1023-1032., doi: 10.1016/j.jinsphys.2011.04.020.
• Lee, GM., McGee, PA., Oldroyd, BP. 2013. Variable virulence among isolates of Ascosphaera apis: testing the parasite-pathogen hypothesis for the evolution of polyandry in social insects. Naturwissenschaften. 100(3):229-234., doi:10.1007/s00114-013-1016-7.
• Lemaitre, B., Hoffmann, J. 2007. The host defense of Drosophila melanogaster. Annu Rev Immunol. 25:697-743., doi:10.1146/annurev.immunol.25.022106.141615.
• Li, G., Zhao, H., Liu, Z., Wang, H., Xu, B., Guo, X. 2018. The Wisdom of Honeybee Defenses Against Environmental Stresses. Front Microbiol. 9 (722): 1-15., doi: 10.3389/fmicb.2018.00722.
• Lihoreau, M., Buhl, J., Charleston, MA., Sword, GA., Raubenheimer, D., Simpson, SJ. 2015. Nutritional ecology beyond the individual: A conceptual framework for integrating nutrition and social interactions. Ecol. Lett. 18 (3): 273–286., doi:10.1111/ele.12406.
• Lindenfelser, LA. 1968. In vivo activity of propolis against Bacillus larvae. J Invertebr Pathol. 12 (1):129–131., doi: 10.1016/0022-2011(68)90252-8.
• Lourenco, AP., Karina, R., Guidugli-Lazzarini, FCP., Freitas, M., Bitondi, MG., Zilá, LP. et al. 2013. Bacterial infection activates the immune system response and dysregulates microRNA expression in honey bees. Ins Bioch Molec Biol 43(5):474-82., doi: 10.1016/j.ibmb.2013.03.001.
• Marmaras, VJ., Lampropoulou, M. 2009. Regulators and signalling in insect haemocyte immunity. Cell Signal. 21(2):186-195., doi:10.1016/j.cellsig.2008.08.014.
• Martin, S., Medina, LM. 2004. Africanized honeybees have unique tolerance to Varroa mites. Trends Parasitol. 20: 112–114., doi: 10.1016/j.pt.2004.01.001.
• Mattila, HR., Seeley, TD. 2007. Genetic diversity in honey bee colonies enhances productivity and fitness. Science. 317(5836):362-364., doi:10.1126/science.1143046.
• Mattila, HR., Rios, D., Walker-Sperlin, VE., Roeselers, G., Newton, ILG. 2012. Characterization of the Active Microbiotas Associated with Honey Bees Reveals Healthier and Broader Communities when Colonies are Genetically Diverse. PLoS ONE 7(3): e32962., doi: 10.1371/journal.pone.0032962
• Mirabito, D., Rosengaus, RB. 2016. A double-edged sword? The cost of proctodeal trophallaxis in termites. Insect Soc. 63: 135–141., doi: 10.1007/s00040-015-0448-9.
• Milium, V. 1955. Grooming dance and associated activities of the honeybee colony.Illionois Academy of Science Transcation. 40: 97–104.
• Mondet, F., Kim, S., de Miranda, J., Beslay, D., Conte, YL., Mercer, AR. 2016. Specific Cues Associated With Honey Bee Social Defence against Varroa destructor Infested Brood. Sci Rep. 6: 25444. doi: 10.1038/srep25444.
• Moreau, SJM. 2013. “It stings a bit but it cleans well:” Venoms of hymenoptera and their antimicrobial potential. J Insect Physiol. 59(2): 186–204., doi: 10.1016/j.jinsphys.2012.10.005.
• Murphy, K., Travers, P., Walport, M. 2017. Janeway`s Inmunobiology. 9th ed. London and New York: Garland Science Ed.942 pg.
• Nappi, AJ., Christensen, BM. 2005. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol.35(5):443-459., doi:10.1016/j.ibmb.2005.01.014.
• Negri, P., Villalobos, E., Szawarski, N., Damiani, N., Gende, L., Garrido, M., Maggi, M., Quintana, S., Schmid, MR., Brockmann, A., Pirk, CWW., Stanley, DW., Tautz, J. 2008. Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J Insect Physiol. 54 (2): 439–444., doi: 10.1016/j.jinsphys.2007.11.002.
• Negri, P., Maggi, M., Massazza, D., Correa-Aragunde, N., Eguaras, MJ., Lamattina, L. 2012. Nitric oxide stimulates melanin production during immune response in Apis mellifera. Biocell 36:68., doi: 10.1007/s13592-013-0207-8ff. ffhal-01201327f.
• Negri, P., Maggi, M., Correa-Aragunde, N., Brasesco, C., Eguaras, M., Lamattina, L. 2013. Nitric oxide participates at the first steps of Apis mellifera cellular immune activation in response to non-self recognition. Apidologie. 44 (5): 575-585., doi:10.1007/s13592-013-0207-8.Negri, P., Quintana, S., Maggi, M., Szawarski, N., Lamattina, L., Eguaras, M. 2014. Apis mellifera hemocytes generate increased amounts of nitric oxide in response to wounding/encapsulation. Apidologie. 45: 610-617., doi:10.1007/s13592-014-0279-0.
• Negri, P., Maggi, M., Ramirez, L., Szawarski A., Feudis, LD., Lamattina, L., Eguaras M. 2016. Cellular immunity in Apis mellifera: studying hemocytes brings light about bees skills to confront threats. Apidologie 47: 379–388., doi: 10.1007/s13592-015-0418-2.
• Negri, P., Ramirez, L., Quintana, S., Szawarski, N., Maggi, M., Le Conte, Y., Lamattina, L., Eguaras, M. 2017. Dietary Supplementation of Honey Bee Larvae with Arginine and Abscisic Acid Enhances Nitric Oxide and Granulocyte Immune Responses after Trauma. Insects 8(3): 85. doi: 10.3390/insects8030085.
• Negri, P., Villalobos, E., Szawarski, N., Damiani, N., Gende, L., Garrido, M., Maggi, M., Quintana, S., Lamattina, L., Eguaras, M. 2019. Towards Precision Nutrition: A Novel Concept Linking Phytochemicals, Immune Response and Honey Bee Health. Insects 10(11): 401. doi: 10.3390/insects10110401.
• Nouvian, M., Reinhard, J., & Giurfa, M. (2016). The defensive response of the honeybee Apis mellifera. J Exp Biol. 219(Pt 22):3505-3517., doi:10.1242/jeb.143016.
• Olofsson, TC., Vásquez, A. 2008. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Curr Microbiol. 57(4):356-363., doi:10.1007/s00284-008-9202-0.
• Otti, O., Tragust, S., Feldhaar, H. 2014. Unifying external and internal immune defences. Trends Ecol Evol. 29(11):625-634., doi:10.1016/j.tree.2014.09.002.
• Panziera, D., van Langevelde, F., Blacquière, T. 2017. Varroa sensitive hygiene contributes to naturally selected varroa resistance in honey bees. J. Apic. Res. 56 (5): 635–642., doi: 10.1080/00218839.2017.1351860.
• Parker, JS., Mizuguchi, K., Gay, NJ. 2001. A family of proteins related to Spätzle, the toll receptor ligand, are encoded in the Drosophila genome. Proteins 45(1): 71–80., doi:10.1002/prot.1125.
• Pettis, JS., Pankiw, T. 1998. Grooming behavior by Apis mellifera L. in the presence of Acarapis woodi (Rennie) (Acari:Tarsonemidae). Apidologie. 29: 241–253., doi: ffhal00891491f.
• Popova, M., Reyes, M., Le Conte, Y., Bankova, V. 2014. Propolis chemical composition and honeybee resistance against Varroa destructor. Nat Prod Res. 28(11):788-794., doi: 10.1080/14786419.2014.881366.
• Powell, JE., Martinson, VG., Urban-Mead, K., Moran, NA. 2014. Routes of Acquisition of the Gut Microbiota of the Honey Bee Apis mellifera. Appl Environ Microbiol. 80(23):7378-7387., doi:10.1128/AEM.01861-14.
• Reynaldi, FJ., De Giusti, MR., Alippi, AM. 2004. Inhibition of the growth of Ascosphaera apis by Bacillus and Paenibacillus strains isolated from honey. Rev Argent Microbiol. 36(1):52-55.
• Richard, F., Aubert, A. & Grozinger, C. 2008. Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol. 6: 50., doi: 10.1186/1741-7007-6-50.
• Richard, F., Holt, HL., Grozinger, CM. 2012. Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics 13: 558., doi: 10.1186/1471-2164-13-558.
• Rittschof, C., Coombs, C., Frazier, M., Grozinger, MC., Robinson, GE. 2015. Early-life experience affects honey bee aggression and resilience to immune challenge. Sci Rep. 5: 15572., doi: 10.1038/srep15572.
• Rivero, A. 2006. Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol. 22(5): 219–225., doi: 1016/j.pt.2006.02.014.
• Rosenkranz, P., Fries, I., Boecking, O., Sturmer, M., 1997. Damaged Varroa mites in the debris of honey bee (Apis mellifera L) colonies with and without hatching brood. Apidologie. 28: 427–437., doi: 10.1051/apido:19970609.
• Rothenbuhler, WC. 1964. Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood. Anim Behav. 12(4): 578-583., doi:10.1016/0003-3472(64)90082-X.
• Royet, J., Reichhart, JM., Hoffmann, JA. 2005. Sensing and signaling during infection in Drosophila. Curr Opin Immunol. 17(1): 1–17., doi: 10.1016/j.coi.2004.12.002.
• Rueppell, O., Hayworth, MK., Ross, N. P. 2010. Altruistic self-removal of health-compromised honey bee workers from their hive. J Evol Biol. 23(7):1538-1546., doi:10.1111/j.1420-9101.2010.02022.x.
• Ryabov, EV., Wood, GR., Fannon, JM., Moore, JD., Bull, JC., Chandler, D., Mead, A., Burroughs, N., Evans, DJ. 2014. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS pathogens 10(6): e1004230., doi: 10.1371/journal.ppat.1004230.
• Salmela, H., Amdam, G. V., Freitak, D. 2015. Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin. PLoS pathogens 11(7): e1005015., doi: 10.1371/journal.ppat.1005015.
• Schmid, MR., Brockmann, A., Pirk, CW., Stanley, DW., Tautz, J. 2008. Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J Insect Physiol.54(2):439-444., doi:10.1016/j.jinsphys.2007.11.002.
• Salvy, M., Martin, C., Bagnères, AG., Provost, E., Roux, M., Le Conte, Y., Clément, JL. 2001. Modifications of the cuticular hydrocarbon profile of Apis mellifera worker bees in the presence of the ectoparasitic mite Varroa jacobsoni in brood cells. Parasitology. 122(Pt 2):145-159., doi:10.1017/s0031182001007181.
• Schoning, C., Gisder, S., Geiselhardt, S., Kretschmann, I., Bienefeld, K., Hilker, M., Genersch, E. 2012. Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera. J Exp Biol. 215: 264–271. doi: 10.1242/jeb.062562.
• Seeley, TD., Morse, RA. 1976. The nest of the honey bee (Apis mellifera L.). Ins. Soc. 23: 495–512., doi: 10.1007/BF02223477.
• Seeley, TD., Visscher, PK., 1985. Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecol Entomol. 10: 81–88., doi: 10.1111/j.1365-2311.1985.tb00537.x.
• Silici, S. 2011. Bal Arısı Biyolojisi ve Yetiştiriciliği. Efil Yayınevi, 240s.
• Simone-Finstrom MD., Evans, JD., Spivak, M. 2009. Resin collection and social immunity in honey bees. Evolution. 63(11):3016-3022., doi:10.1111/j.1558-5646.2009.00772.x.
• Simone-Finstrom, MD., Spivak, M. 2010. Propolis and bee health: The natural history and significance of resin use by honey bees. Apidologie. 41 (3): 295–311., doi: 10.1051/apido/2010016.
• Simone-Finstrom, M., Foo, B., Tarpy, DR., Starks, PT. 2014. Impact of Food Availability, Pathogen Exposure, and Genetic Diversity on Thermoregulation in Honey Bees (Apis mellifera). J Insect Behav. 27: 527–539., doi: 10.1007/s10905-014-9447-3.
• Simone-Finstrom, MD. 2017. Social Immunity and the Superorganism: Behavioral Defenses Protecting Honey Bee Colonies from Pathogens and Parasites, Bee World. 94(1):21-29., doi: 10.1080/0005772X.2017.1307800.
• Spivak, M., Reuter, GS. 1998. Performance of hygienic honey bee colonies in a commercial apiary. Apidologie. 29 (3): 291–302., doi: 10.1051/apido:19980308.
• Spivak, M., Goblirsch, M., Simone-Finstrom, M. 2019. Social-medication in bees: the line between individual and social regulation. Curr Opin Insect Sci. 33:49–55., doi: 10.1016/j.cois.2019.02.009.
• Stabentheiner, A., Kovac, H., Brodschneider, R. 2010. Honeybee colony thermoregulation--regulatory mechanisms and contribution of individuals in dependence on age, location and thermal stress. PLoS One. 5(1):e8967., doi:10.1371/journal.pone.0008967.
• Starks, PT., Blackie, CA., Seeley, TD. 2000. Fever in honeybee colonies. Naturwissenschaften. 87(5):229-231., doi:10.1007/s001140050709.
• Steinmann, N., Corona, M., Neumann, P., Dainat, B. 2015. Overwintering Is Associated with Reduced Expression of Immune Genes and Higher Susceptibility to Virus Infection in Honey Bees. PloS one, 10(6): e0129956., doi: 10.1371/journal.pone.0129956.
• Stokes, BA., Yadavi, S., Shoka, lU., Smith, LC., Eleftherianos, I. 2015. Bacterial and fungal pattern recognition receptors in homologous innate signaling pathways of insects and mammals. Front Microbiol 6:19., doi:10.3389/fmicb.2015.00019.
• Strand, MR. 2008. The insect cellular immune response. Insect Science 15: 1-14., doi:10.1111/j.1744-7917.2008.00183.x.
• Stow, A., Briscoe, D., Gillings, M., Holley, M., Smith, S., Leys, R., Silberbauer, T., Turnbull, C., Beattie, A. 2007. Antimicrobial defences increase with sociality in bees. Biol Lett.3(4):422-424. doi:10.1098/rsbl.2007.0178.
• Swanson, J. A., Torto, B., Kells, S. A., Mesce, K. A., Tumlinson, J. H., Spivak, M. 2009. Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. J Chem Ecol. 35(9):1108-1116., doi:10.1007/s10886-009-9683-8.
• Tarpy, DR. 2003. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc Biol Sci. 270(1510):99-103., doi:10.1098/rspb.2002.2199.
• Tarpy, DR., Nielsen, R., Nielsen, DI. 2004. A scientific note on the revised estimates of effective paternity frequency in Apis. Insect. Soc. 51: 203–204., doi:10.1007/s00040-004-0734-4.
• Tarpy, DR., Seeley, TD. 2006. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften. 93(4):195-199., doi:10.1007/s00114-006-0091-4.
• Tarpy, DR., Vanengelsdorp, D., Pettis, JS. 2013. Genetic diversity affects colony survivorship in commercial honey bee colonies. Naturwissenschaften.100(8):723-728., doi:10.1007/s00114-013-1065-y.
• Traniello, JF., Rosengaus, RB., Savoie, K. 2002. The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc Natl Acad Sci U S A. 99(10): 6838-6842., doi:10.1073/pnas.102176599.
• Tragust, S., Mitteregger, B., Barone, V., Konrad, M., Ugelvig, LV., Cremer, S. 2013. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Curr Biol. 23(1):76-82. doi:10.1016/j.cub.2012.11.034.
• Unger, P., Guzman-Novoa, E. 2010. Maternal effects on the hygienic behavior of Russian x Ontario hybrid honeybees (Apis mellifera L.). J Heredity. 10(1):91-96., doi:10.1093/jhered/esp092.
• Valanne, S., Wang, JH., Rämet, M. 2011. The Drosophila Toll signaling pathway. J Immunol. (Baltimore, Md: 1950) 186(2): 649–656., doi: 10.4049/jimmunol.1002302.
• Van Steenkiste, D. 1988. De hemocyten van dehonigbij (Apis mellifera L). Typologie, bloedbeeldencellulaireverdedigingsreacties [doctoral thesis]. Gent, Belgium, Rijksuniversiteit.
• Vaudo, AD., Patch, HM., Mortensen, DA., Tooker, JF., Grozinger, CM. 2016. Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proc Natl Acad Sci U S A. 113(28): E4035-E4042., doi:10.1073/pnas.1606101113.
• Visscher, P.1983. The honey bee way of death: Necrophoric behaviour in Apis mellifera colonies. Animal Behaviour. 31: 1070-1076.
• Vojvodic, S., Jensen, AB., Markussen, B., Eilenberg, J., Boomsma, JJ. 2011. Genetic variation in virulence among chalkbrood strains infecting honeybees. PLoS One. 6(9):e25035.,doi:10.1371/journal.pone.0025035.
• Walderdorff, L., Laval-Gilly, P., Bonnefoy, A., Falla-Angel, J. 2018. Imidacloprid intensifies its impact on honeybee and bumblebee cellular immune response when challenged with LPS (lippopolysacharide) of Escherichia coli. J Insect Physiol. 108: 17–24., doi: 10.1016/j.jinsphys.2018.05.002.
• Wang, L., Weber, AN., Atilano, ML., Filipe, SR., Gay, NJ., Ligoxygakis, P. 2006. Sensing of Gram-positive bacteria in Drosophila: GNBP1 is needed to process and present peptidoglycan to PGRP-SA. The EMBO journal 25(20): 5005–5014., doi: 10.1038/sj.emboj.7601363.
• Ward, K., Danka, R., Ward, R. 2008. Comparative performance of two mite-resistant stocks of honey bees (Hymenoptera: Apidae) in Alabama beekeeping operations. J Econ Entomol. 101(3):654-659., doi:10.1603/0022-0493(2008)101[654:cpotms]2.0.co;2.
• Weirich, G., Collins, A., Williams, V. 2002. Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie Springer Verlag 33(1): 3-14., doi: ff10.1051/apido:2001001ff. ffhal-00891910f.
• Werner, T., Borge-Renberg, K., Mellroth, P., Steiner, H., Hultmark, D. 2003. Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysaccharide and peptidoglycan. J Biol Chem. 278(29):26319-26322., doi:10.1074/jbc.C300184200.
• Wilson-Rich, N., Dres, ST., Starks, PT., 2008. The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). J Insect Physiol. 54 (10-11): 392–1399. doi: 10.1016/j.jinsphys.2008.07.016.
• Wilson-Rich, N., Spivak, M., Fefferman, NH., Starks, P. T. 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
• Winston, ML., Taylor, OR., Otis, GW. 1983. Some differences between temperate European and tropical African and South American honey bees. Bee World. 64: 12–21., doi: 10.1080/0005772X.1983.11097902.
• Xu, P., Shi, M., Chen, XX. 2009. Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. PloS one, 4(1): e4239., doi: 10.1371/journal.pone.0004239.
• Yi, HY., Chowdhury, M., Huang, YD., Yu, X Q. 2014. Insect antimicrobial peptides and their applications. Appl Microbiol Biotechnol. 98(13): 5807–5822., doi: 10.1007/s00253-014-5792-6.
• Zakaria, M. 2007. The Cellular Immunity Responses In The Haemolymph of Honey Bee Workers Infected By American Foulbrood Disease (AFB). Res. J. Appl. Sci. 3: 56-63.
• Zono, M., Okada, I., Sasaki, M. 2005. Heat production by balling in the Japanese honeybee, Apis cerana japonica as a defensive behavior against the hornet, Vespa simillima xanthoptera (Hymenoptera: Vespidae). Experientia. 43: 1031-1034., doi: 10.1007/BF01952231.
• Zhukovskaya, M., Yanagawa, A., Forschler, B. T. 2013. Grooming Behavior as a Mechanism of Insect Disease Defense. Insects. 4(4):609-630., doi:10.3390/insects4040609