نوع مقاله : مروری
نویسنده
بخش تحقیقات علوم دامی، مرکز تحقیقات و آموزش کشاورزی و منابع طبیعی کردستان، سازمان تحقیقات، آموزش و ترویج کشاورزی، سنندج، ایران
چکیده
رفتار بهداشتی زنبورعسل به عنوان یک ویژگی بالقوه مرتبط با مقاومت در برابر آفات و بیماریهای زنبورعسل به ویژه کنهواروآ در نظر گرفته شده و بروز آن در زنبورهای کارگر به مصونیت اجتماعی کلنیهای زنبورعسل کمک میکند. توانایی زنبورهای کارگر در تشخیص و حذف نوزادان مرده یا غیر طبیعی از انتقال و انتشار بیماریهای نوزادان به داخل کلنیها جلوگیری میکند. در طول پنج دهه گذشته، این رفتار به طور گسترده مورد مطالعه قرار گرفته و در چندین برنامه تحقیقاتی مورد اصلاح و بهبود قرار گرفته است. تا دهه 1990، هیچ دیدگاه جدیدی در مورد کارآمدی این رفتار در برابر بیمارهای لوک آمریکایی و لارو گچی وجود نداشته است. در دو دهه اخیر، مطالعات وسیعی در مورد تأثیر بروز رفتار بهداشتی زنبورها در برابر کنهواروآ صورت گرفته که این موضوع بحث در مورد کارایی رفتار بهداشتی زنبورها را در برابر این آفت دامن میزند. برنامههای اصلاح نژادی روی رفتار بهداشتی زنبورها نشان دادهاند که انتخاب برای یک صفت خاص ممکن است بر سایر صفات نیز تأثیر بگذارد. بنابراین، در این بررسی مزایا و معایب بروز رفتار بهداشتی زنبورها در کلنی، تأثیر آن روی سایر صفات مهم اقتصادی و نتایج مطالعات قبلی در مورد این رفتار را از اواخر دهه 1990 تاکنون مورد بررسی و بحث قرار خواهیم داد. به طور کلی، به نظر میرسد مزایای بروز رفتار بهداشتی زنبورها برای کلنیها و پرورش دهندگان زنبورعسل تا حدود زیادی بیشتر از هزینههای آن است.
کلیدواژهها
موضوعات
Al Toufailia, H.M., Amiri, E., Scandian, L., Kryger, P. and Ratnieks, F.L.W. (2014). Towards integrated control of varroa: Effect of variation in hygienic behaviour among honey bee colonies on mite population increase and deformed wing virus incidence. Journal of Apicultural Research. 53: 555–562. doi:10.3896/ibra.1.53.5.10
Asnaashari, M., Ayarani-Najaran, Z., Shahrampour, D. and Rahimi, A. (2025). Quality Assessment of Native Iranian Cedar and Citrus Honeys: Bioactive Components, Antioxidant Activity, and Estrogenic Properties in MCF-7 Cells. Journal of Food Quality. 2025 (1): 4928391, 13. https://doi.org/10.1155/jfq/4928391
Bigio, G., Al Toufailia, H.M. and Ratnieks, F.L.W. (2014). Honey bee hygienic behaviour does not incur a cost via removal of healthy brood. Journal of Evolutionary Biology. 27: 226–230. doi:10.1111/jeb.12288
Boecking, O., Bienefeld, K. and Drescher, W. (2000). Heritability of the Varroa-specific hygienic behaviour in honey bees (Hymenoptera: Apidae). Journal of Animal Breeding and Genetics. 117: 417–424. doi:10.1046/j.1439- 0388.2000.00271.x
Boecking, O. (1999). Sealing up and non-removal of diseased and Varroa jacobsoni infested drone brood cells is part of the hygienic behaviour in Apis cerana. Journal of Apicultural Research. 38: 159–168. doi:10.1080/00218839.1999.11101006
Boecking, O. and Drescher, W. (1991). Response of Apis mellifera L colonies infested with Varroa jacobsoni Oud. Apidologie. 22: 237–241. doi:10.1051/apido:19910308
Boecking, O. and Drescher, W. (1992). The removal response of Apis mellifera L. colonies to brood in wax and plastic cells after artificial and natural infestation with Varroa jacobsoni Oud. and to freeze-killed brood. Experimental and Applied Acarology. 16: 321–329. doi:10.1007/bf01218574
Boecking, O. and Spivak, M. (1999). Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie. 30: 141–158. doi:10.1051/apido:19990205
Boot, W.J., Tan, N.Q., Dien, P.C., Huan, L., Dung, N. and Long, L.T. (1997). Reproductive success of Varroa jacobsoni in brood of its original host, Apis cerana, in comparison to that of its new host, A. mellifera (Hymenoptera: Apidae). Bulletin of Entomological Research. 87: 119–126. doi:10.1017/ S0007485300027255
Buchler, R., Andonov, S., Bienefeld, K., Costa, C., Hatjina, F., Kezic, N., … Wilde, J. (2013). Standard methods for rearing and selection of Apis mellifera queens. In V. Dietemann, J.D. Ellis & P. Neumann (Eds.), The COLOSS BEEBOOK, Volume I: Standard methods for Apis mellifera pest and pathogen research. Journal of Apicultural Research. 52(1): doi:10.3896/IBRA.1.52.1.07
Cremer, S., Armitage, S.A.O. and Schmid-Hempel, P. (2007). Social immunity. Current Biology. 17: R693–R702. doi: 10.1016/j.cub.2007.06.008
Cunard, S.J. and Breed, M.D. (1998). Post-stinging behavior of worker honey bees (Hymenoptera: Apidae). Annals of the Entomological Society of America. 91: 754–757. doi:10.1093/aesa/91.5.754
Danka, R.G., Harris, J.W. and Dodds, G.E. (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
Danka, R.G., Harris, J.W., Villa, J.D. and Dodds, G.E. (2013). Varying congruence of hygienic responses to Varroa destructor and freeze-killed brood among different types of honey bees. Apidologie. 44: 447–457. doi:10.1007/s13592- 013-0195-8
De Guzman, L.I., Rinderer, T.E. and Frake, A.M. (2008). Comparative reproduction of Varroa destructor in different types of Russian and Italian honey bee combs. Experimental and Applied Acarology. 44: 227–238. doi:10.1007/s10493-008- 9142-1
De Guzman, L.I., Rinderer, T.E., Frake, A.M. and Kirrane, M.J. (2015). Brood removal influences fall of Varroa destructor in honey bee colonies. Journal of Apicultural Research. 54: 216– 225. doi:10.1080/00218839.2015.1117294
Dietemann, V., Nazzi, F., Martin, S.J., Anderson, D., Locke, B., Delaplane, K.S., … Ellis, J.D. (2013). Standard methods for varroa research. In V. Dietemann, J.D. Ellis & P. Neumann (Eds.), The COLOSS BEEBOOK, Volume II: Standard methods for Apis mellifera pest and pathogen research. Journal of Apicultural Research.52(1): doi:10.3896/IBRA.1.52.1.09
Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H., … Hultmark, D. (2006). Immune pathways and defense mechanisms in honey bees Apis mellifera. Insect Molecular Biology. 15: 645–656. doi:10.1111/j.1365-2583.2006. 00682.x
Flores, J.M., Ruiz, J.A., Ruz, J.M., Puerta, F. and Bustos, M. (2001). Hygienic behaviour of Apis mellifera iberica against brood cells artificially infested with varroa. Journal of Apicultural Research. 40: 29–34. doi:10.1080/00218839.2001.11101046
Forsgren, E. (2010). European foulbrood in honey bees. Journal of Invertebrate Pathology.103(Suppl.), S5–S9. doi:10.1016/ j.jip.2009.06.016
Fries, I., Camazine, S. and Sneyd, J. (1994). Population dynamics of Varroa jacobsoni: A model and a review. Bee World. 75. 5–28. doi:10.1080/0005772X.1994.11099190
Gallai, N., Salles, J.-M., Settele, J. and Vaissie`re, B.E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics. 68: 810–821. doi: 10.1016/j.ecolecon.2008.06.014
Garcia, R.C., Oliveira, N.T.E.d., Camargo, S.C., Pires, B.G., Oliveira, C.A.L.d., Teixeira, R.d.A. and Pickler, M.A. (2013). Honey and propolis production, hygiene and defense behaviors of two generations of Africanized honey bees. Scientia Agricola. 70: 74–81. doi:10.1590/S0103-90162013000200003
Genersch, E., Ashiralieva, A. and Fries, I. (2005). Strain-and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, a bacterial pathogen causing American foulbrood disease in honey bees. Applied and Environmental Microbiology. 71: 7551–7555. doi:10.1128/AEM.71.11.7551- 7555.2005
Gilliam, M., Taber, S., Lorenz, B.J. and Prest, D.B. (1988). Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis. Journal of Invertebrate Pathology. 52: 314–325. doi:10.1016/0022-2011(88)90141-3
Gilliam, M., Taber, S. and Richardson, G.V. (1983). Hygienic behavior of honey bees in relation to chalkbrood disease. Apidologie. 14: 29–39. doi:10.1051/apido:19830103
Guarna, M.M., Melathopoulos, A.P., Huxter, E., Iovinella, I., Parker, R., Stoynov, N., … Foster, L.J. (2015). A search for protein biomarkers links olfactory signal transduction to social immunity. BMC Genomics. 16: 63. doi:10.1186/ s12864-014-1193-6
Guzman-Novoa, E., Hunt, G.J., Page, R.E. and Fondrk, M.K. (2002). Genetic correlations among honey bee (Hymenoptera: Apidae) behavioral characteristics and wing length. Annals of the Entomological Society of America. 95: 402–406. doi:10.1603/0013-8746(2002)095[0402: GCAHBH]2.0.CO;2
Hansen, H. and Brødsgaard, C.J. (1999). American foulbrood: A review of its biology, diagnosis and control. Bee World. 80: 5–23. doi:10.1080/0005772X.1999.11099415
Harris, J.W. (2007). Bees with Varroa Sensitive Hygiene preferentially remove mite infested pupae aged ≤ five days post capping. Journal of Apicultural Research. 46: 134–139. doi:10.1080/00218839.2007.11101383
Harbo, J.R. and Harris, J.W. (2009). Responses to Varroa by honey bees with different levels of Varroa sensitive hygiene. Journal of Apicultural Research. 48: 156-161.doi:10.3896/ibra.1.48.3.02
Harbo, J.R. and Harris, J.W. (2005). Suppressed mite reproduction explained by the behaviour of adult bees. Journal of Apicultural Research. 44: 21–23. doi:10.1080/ 00218839.2005.11101141
Harbo, J.R. Hoopingarner, R.A. (1997). Honey bees (Hymenoptera: Apidae) in the United States that express resistance to Varroa jacobsoni (Mesostigmata: Varroidae). Journal of Economic Entomology. 90: 893–898. doi:10.1093/jee/90.4.893
Harpur, B.A., Chernyshova, A., Soltani, A., Tsvetkov, N., Mahjoorighasrodashti, M., Xu, Z. and Zayed, A. (2014). No genetic tradeoffs between hygienic behaviour and individual innate immunity in the honey bee, Apis mellifera. PLoS ONE. 9: e104214. doi: 10.1371/journal.pone.0104214
Harris, J.W., Danka, R.G. and Villa, J.D. (2009). Hygienic activity toward varroa mites in capped brood is not dependent on mite reproductive status. American Journal of Bee. 149: 587–588.
Harris, J.W., Danka, R.G. and Villa, J.D. (2010). Honey bees (Hymenoptera: Apidae) with the trait of varroa sensitive hygiene remove brood with all reproductive stages of varroa mites (Mesostigmata: Varroidae). Annals of the Entomological Society of America. 103: 146–152. doi:10.1603/ an09138
Holloway, B., Tarver, M.R. and Rinderer, T.E. (2013). Fine mapping identifies significantly associating markers for resistance to the honey bee brood fungal disease, Chalkbrood. Journal of Apicultural Research. 52: 134–140. doi:10.3896/ ibra.1.52.3.04
Ibrahim, A., Reuter, G.S. and Spivak, M. (2007). Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor. Apidologie. 38: 67–76. doi:10.1051/ apido:2006065
Ibrahim, A. and Spivak, M. (2006). The relationship between hygienic behavior and suppression of mite reproduction as honey bee (Apis mellifera) mechanisms of resistance to Varroa destructor. Apidologie. 37: 31–40. doi:10.1051/ apido:2005052
Invernizzi, C., Rivas, F. and Bettucci, L. (2011). Resistance to chalkbrood disease in Apis mellifera L. (Hymenoptera: Apidae) colonies with different hygienic behavior. Neotropical Entomology. 40: 28–34. doi:10.1590/S1519 566X2011000100004
Kirrane, M.J., de Guzman, L.I., Holloway, B., Frake, A.M., Rinderer, T.E., & Whelan, P.M. (2015). Phenotypic and genetic analyses of the varroa sensitive hygienic trait in Russian honey bee (Hymenoptera: Apidae) colonies. PLOS ONE. 10: e0116672. doi: 10.1371/journal.pone.0116672
Kefuss, J., Taber III, S., Vanpoucke, J. and Rey, F. (1996). A practical method to test for disease resistance in honey bees. American Bee Journal. 136: 31–32. doi:10.1603/EC11035
Kirrane, M.J., De Guzman, L.I., Rinderer, T.E., Frake, A.M., Wagnitz, J. and Whelan, P.M. (2011). Asynchronous development of honey bee host and Varroa destructor (Mesostigmata: Varroidae) influences reproductive potential of mites. Journal of Economic Entomology. 104: 1146–1152. doi:10.1603/EC11035
Muli, E., Patch, H., Frazier, M., Frazier, J., Torto, B., Baumgarten, T., … Grozinger, C. (2014). Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in East Africa. PLoS ONE. 9: e94459. doi: 10.1371/journal. pone.0094459
Newton, D. and Ostasiewski, N. (1986). A simplified bioassay for behavioral resistance to American Foulbrood in honey bees (Apis mellifera L.). American Bee Journal. 126: 278–281.
Nicodemo, D., De Jong, D., Couto, R. and Malheiros, E. (2013). Honey bee lines selected for high propolis production also have superior hygienic behavior and increased honey and pollen stores. Genetics and Molecular Research. 12: 6931– 6938. doi: 10.4238/2013.December.19.12
Omar, M.O., Moustafa, A.M., Ansari, M.J., Anwar, A.M., Fahmy, B.F., Al-Ghamdi, A. and Nuru, A. (2014). Antagonistic effect of gut bacteria in the hybrid Carniolan honey bee, Apis mellifera carnica, against Ascosphaera apis, the causal organism of chalkbrood disease. Journal of Apicultural Science. 58: 17–27. doi:10.2478/jas-2014-0002
Oxley, P.R., Spivak, M. and Oldroyd, B.P. (2010). Six quantitative trait loci influence task thresholds for hygienic behaviour in honey bees (Apis mellifera). Molecular Ecology. 19:1452– 1461. doi:10.1111/j.1365-294X.2010. 04569.x
Palacio, M.A., Rodriguez, E., Goncalves, L., Bedascarrasbure, E. and Spivak, M. (2010). Hygienic behaviors of honey bees in response to brood experimentally pin-killed or infected with Ascosphaera apis. Apidologie. 41: 602–612. doi:10.1051/ apido/2010022
Panasiuk, B., Skowronek, W. and Bien´kowsk, M. (2008). Influence of genotype and method of brood killing on brood removal rate in honey bee. Journal of Apicultural Science. 52: 55–65.
Pinto, F.d.A., Puker, A. and Barreto, L. (2012). The ectoparasite mite Varroa destructor Anderson and Trueman in southeastern Brazil apiaries: Effects of the hygienic behavior of Africanized honey bees on infestation rates. Arquivo Brasileiro de Medicina Veterina´ria e Zootecnia. 64: 1194–1199. doi:10.1590/S0102-09352012000500017
Rath, W. (1992). The key to varroa: The drones of Apis cerana and their cell cap. American Bee Journal.
Rath, W. (1999). Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie. 30: 97–110. doi:10.1051/apido:19990202
Rahimi, A., Bahmani, H.R. & Mahdavi, V. (2025). Acaricidal and insecticidal activity of plant extracts of Ferola pseudalliacea, Smyrnopsis aucheri, Satureja sahendica and Prangos ferulacea for the control of Varroa mite in honey bee colonies. Research on Animal Production. 16 (1):167-179. https://doi.org/0.61186/rap.16.1.167
Rahimi, A. & Parichehreh, S. (2024a). Evaluation and introduction of a new plant-based formulation to control Varroa mite (Varroa destructor) in honey bee colonies (Apis mellifera). Journal of Entomological Society of Iran. 44(4): 417-428. https://doi.org/ 10.61186/jesi.44.4.5
Rahimi, A., Parichehreh, S.H. (2024b). Evaluation of the Uncapping & Removing hygienic behaviors of Iranian honey bee colonies (Apis mellifera meda) against Varroa mite (Varroa destructor) in Kermanshah province. Research Journal of Livestock Science. 44:3-16. https://doi.org/10.22092/asj.2023.363059.2330
Rahimi, A., Mirmoayedi, A., Kahriz, D., Zarei, L. and Jamali, S. (2023). Genetic characterization of Iranian honey bees, Apis mellifera meda Skorikow, 1929, based on microsatellite DNA polymorphism. Biochemical Genetics. 61 (2): 1-25. https://doi: 10.1007/s10528-023-10368-y
Rahimi, A., Mirmoayedi, A., Kahriz, D., Zarei, L. & Jamali, S. (2022). Molecular genetic diversity and population structure of Iranian honey bee (Apis mellifera meda) populations: Implications for breeding and conservation. Journal of Plant diseases and protection. 129: 1-12. doi:10.1007/s41348-022-00657-w
Ramsey, S.D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J.D., Mowery, A., Lim, D., Joklik, J., Cicero, J.M., Ellis, J.D., Hawthorne, D. and VanEngelsdorp, D. (2021). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, the Nederland, 29 Jun 2019. 116(5): 1792-1801. https://doi: 10.1073/pnas.1818371116.
Rinderer, T.E., Harris, J.W., Hunt, G.J. and de Guzman, L.I. (2010). Breeding for resistance to Varroa destructor in North America. Apidologie. 41: 409–424.
Rothenbuhler, W.C. (1964). Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease- killed brood. Animal Behaviour. 12: 578–583. doi:10.1016/0003-3472(64)90082-X
Schoning, C., Gisder, S., Geiselhardt, S., Kretschmann, I., Bienefeld, K., Hilker, M. and Genersch, E. (2012). Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera. Journal of Experimental Biology. 215: 264–271. doi:10.1242/jeb.062562
Seltzer, R., Kamer, Y., Kahanov, P., Splitt, A., Bieńkowska, M., Hefetz, A. and Soroker, V. (2022). Breeding for hygienic behavior in honey bees (Apis mellifera): a strong paternal effect. Journal of Apicultural Research. 62(3): 419–428. https://doi.org/10.1080/00218839.2022.2140927
Spivak, M. and Danka, R. G. (2021). Perspectives on hygienic behavior in Apis mellifera and other social insects. Apidologie. 52(1): 1–16. https://doi.org/10.1007/s13592- 020-00784-z
Spivak, M. (1996). Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie. 27: 245–260. doi:10.1051/apido:19960407
Spivak, M. and Gilliam, M. (1998a). Hygienic behavior of honey bees and its application for control of brood diseases and varroa. Part II. Studies on hygienic behaviour since the Rothenbuhler era. Bee World. 79: 169–186. doi:10.1080/ 0005772X.1998.11099408
Spivak, M. and Gilliam, M. (1998b). Hygienic behavior of honey bees and its application for control of brood diseases and varroa. Part I. Hygienic behavior and resistance to American foulbrood. Bee World. 79: 124–134. doi:10.1080/ 0005772x.1998.11099394
Spivak, M. and Reuter, G.S. (1998). Performance of hygienic honey bee colonies in a commercial apiary. Apidologie. 29: 291–302. doi:10.1051/apido:19980308
Spivak, M. and Gilliam, M. (1993). Facultative expression of hygienic behaviour of honey bees in relation to disease resistance. Journal of Apicultural Research. 32: 147–157. doi:10.1080/00218839.1993.11101300
Spivak, M. and Reuter, G.S. (2001a). Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie. 32: 555–565. doi: 10.1051/apido:2001103
Spivak, M. and Reuter, G.S. (2001b). Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. Journal of Economic Entomology. 94: 326–331. doi:10.1603/0022-0493-94.2.326
Snyder, P., Martin, J., Herman, J.J., Franklin, s., Wagoner, K.M., Soroker, V. and Rueppell, O. (2024). The impact of honey bee (Apis mellifera) group size on hygienic behavior performance. Behavioral Ecology and Sociobiology. 78: 52. https://doi.org/10.1007/s00265-024-03471-6
Swanson, J.A.I., Torto, B., Kells, S.A., Mesce, K.A., Tumlinson, J.H. and Spivak, M. (2009). Odorants that induce hygienic behavior in honey bees: Identification of Volatile Compounds in Chalkbrood-Infected Honey bee Larvae. Journal of Chemical Ecology. 35: 1108–1116. doi:10.1007/s10886-009-9683-8.
Taheri Imam Kandi, R., Ghafari, M., Rahimi, A. and Hashemi, A. (2024). A Study of Hygienic and Grooming Behaviors in the Iranian Honeybee (Apis mellifera meda) Colonies Against Varroa destructor. Sociobiology. 71(2): e10302. https://doi: 10.13102/sociobiology. v71i2.10302
Tsuruda, J.M., Harris, J.W., Bourgeois, L., Danka, R.G. and Hunt, G.J. (2012). High-resolution linkage analyses to identify genes that influence varroa sensitive hygiene behavior in honey bees. PLoS ONE. 7: e48276. doi:10.1371/journal. pone.0048276
Uzunov, A., Costa, C., Panasiuk, B., Meixner, M., Kryger, P., Hatjina, F., … Le Conte, Y. (2014). Swarming, defensive and hygienic behaviour in honey bee colonies of different genetic origin in a pan-European experiment. Journal of Apicultural Research. 53: 248–260. doi:10.3896/IBRA.1.53.2.06
Villa, J.D., Danka, R.G. and Harris, J.W. (2009). Simplified methods of evaluating colonies for levels of Varroa Sensitive Hygiene (VSH). Journal of Apicultural Research. 48: 162–167. doi:10.3896/IBRA.1.48.3.03
Wallberg, A., Gle´min, S. and Webster, M.T. (2015). Extreme recombination frequencies shape genome variation and evolution in the honey bee, Apis mellifera. PLOS Genetics. 11: e1005189. doi: 10.1371/journal.pgen.1005189
Wedenig, M., Riessberger-Galle´, U. and Crailsheim, K. (2003). A substance in honey bee larvae inhibits the growth of Paenibacillus larvae larvae. Apidologie. 34: 43–51. doi:10.1051/ apido:2002043
Wilson-Rich, N., Spivak, M., Fefferman, N.H. and Starks, P.T. (2009). Genetic, individual, and group facilitation of disease resistance in insect societies. Annual Review of Entomology. 54: 405–423. doi: 10.1146/annurev.ento.53.103106.093301
Wielewski, P., De Alencar Arnaut De Toledo, V., Martins, E.N., Costa-Maia, F.M., Faquinello, P., Lino-Lourenc¸o, D.A., Sereia, M.J. (2012). Relationship between hygienic behavior and Varroa destructor mites in colonies producing honey or royal jelly. Sociobiology. 59: 251–274.
Windig, J.J., Calus, M.P.L., Beerda, B. and Veerkamp, R.F. (2006). Genetic correlations between milk production and health and fertility depending on herd environment. Journal of Dairy Science. 89: 1765–1775. doi:10.3168/jds. S0022-0302 (06)72245-7
)