Nikita Aseem Grover Preeti Kalia Reshma Sinha Pratibha Garg


Apiculture has become a profitable profession due to the high economic importance of honey and various beehive products. Honeybees are tiny social insects that perform a crucial function in the agricultural field and are necessary for good yields. Honeybees are the biological indicators of environmental health. Unforeseen rapid decrease in honeybee numbers characterized by the departure of honeybees from the colonies and accompanied by the total absence of any dead bees in the hive surrounding and inside it suggests a condition called Colony Collapse Disorder (CCD). Pesticides, pathogens, and other ecological stresses such as nutritional deficiency may add to bee extinction or CCD. Besides this, the exposure to low-level radiofrequency and microwave radiations from mobile phones also have profound undesirable effects on honeybees. Research has shown changes in biology and behaviour which includes some undesirable changes in the biomolecules concentration in honeybees because of radiation exposure. Extremely low-frequency electromagnetic field (ELF- EMF ) also affects honeybee`s immune system and navigation activities. The radiation induces emotional disturbance and genetic disorders in brood which attributes to a decline in the breeding efficiency of bees. The present review is an attempt to compile the causes of CCD and discuss the management practices to be followed by the beekeepers to avoid the devastating loss to them and the planet Earth.




Colony collapse disorder, Electromagnetic radiation, Honeybee, Pathogens, Pesticides

Abdelaal, A.A.A. (2015). Biological and chemical activities of honey bee colonies exposed to electromagnetic radiation of cell phone towers. J. Plant Prot. & Pathol. 6(9), 1231-1238. 10.21608/jppp.2015.74936.
Alaux, C., Ducloz, F., Crauser, D. & Le Conte, Y. (2010). Diet effects on Honeybee immunocompetence. Biol. Lett. 6(4), 562-565, https://doi.org/10.1098/rsbl.2009.0986.
Ansari, M. J., Al-Ghamdi, A., Nuru, A., Ahmed, A. M., Ayaad, T. H., Al-Qarni, A., Alattal, Y. & Al-Waili, N. (2017). Survey and molecular detection of Melissococcus plutonius, the causative agent of European Foulbrood in honeybees in Saudi Arabia. Saudi Journal of Biological Sciences,  24(6), 1327–1335. https://doi.org/10.1016/j.sjbs.2016.10.012
Arias, M. C. & Sheppard, W. S. (2005). Phylogenetic relationships of honeybees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol. Phylogenet. Evol. 37(1), 25-35. 10.1016/j.ympev.2005.02.017.
Bailey, L. (1985). Acarapis woodi: A modern appraisal. Bee World, 66(3): 99-104.
Barrionuevo, A. (2007). Bees vanish; Scientists race for reasons. New York Times 24:1. https://www.nytimes.com/2007/04/24/science/24bees.html.
Berthoud, H., Imdorf, A., Haueter, M., Radloff, S. & Neumann, P. (2010). Virus infections and winter losses of honey bee colonies (Apis mellifera). J. Apic. Res. 49(1), 60-65. https://doi.org/10.3896/IBRA.
Branchiccela, B., Castelli, L., Corona, M., Díaz-Cetti, S., Invernizzi, C., Martínez de la Escalera, G., Mendoza, Y., Santos, E., Silva, C., Zunino, P. & Antúnez, K. (2019). Impact of nutritional stress on the honeybee colony health. Scientific Reports, 9(1), 10156. https://doi.org/10.1038/s41598-019-46453-9.
Brockmann, A. & Robinson, G. E. (2007). Central projections of sensory systems involved in honey bee dance language communication. Brain Behav. Evol. 70(2), 125-136. 10.1159/000102974.
Broeckx, B. J., De Smet, L., Blacquière, T., Maebe, K., Khalenkow, M., Van Poucke, M. & de Graaf, D. C. (2019) Honey bee predisposition of resistance to ubiquitous mite infestations. Sci. Rep. 9(1), 1-11. 10.1038/s41598-019-44254-8.
Bullamore, G. W. (1922). Nosema apis and Acarapis (Tarsonemus) woodi in relation to Isle of Wight Bee Disease. Cambridge, At the University press, [1922]. https://doi.org/10.5962/bhl.title.57091.
Cammaerts, M. C. (2017). Is electromagnetism one of the causes of the CCD? A work plan for testing this hypothesis. J. Behav. 2(1), 1006. https://www.jscimedcentral.com/Behavior/behavior-2-1006.php.
Canciani, M., Arnellos, A. & Moreno, A. (2019). Revising the Superorganism: An Organizational Approach to Complex Eusociality. Frontiers in Psychology, 10, 2653. https://doi.org/10.3389/fpsyg.2019.02653.
Chandler, D., Sunderland, K. D., Ball, B. V. & Davidson, G. (2001). Prospective biological control agents of Varroa destructor n. sp., an important pest of the European Honey bee, Apis mellifera. Biocontrol Sci. Technol. 11(4), 429-448. https://doi.org/10.1080/09583150120067472.
Colin, T., Meikle, W. G., Wu, X. & Barron, A. B. (2019). Traces of a Neonicotinoid Induce Precocious Foraging and Reduce Foraging Performance in Honey Bees. Environmental Science & Technology, 53 (14), 8252-8261. DOI: 10.1021/acs.est.9b02452.
Cornman, R. S., Tarpy, D. R., Chen, Y., Jeffreys, L., Lopez, D., Pettis, J. S., Dennis vanEngelsdorp, D. & Evans, J. D. (2012). Pathogen webs in collapsing honey bee colonies. e43562. https://doi.org/10.1371/journal.pone.0043562.
Cox-Foster, D. & vanEngelsdorp, D. (2009) Saving the Honey bee. Sci. Am. 300(4), 40-47. 10.1038/scientificamerican0409-40.
Critchlow, B. P. (1904). Gleanings in bee culture. Bee Cult. 32, 692.
Cucurachi, S., Tamis, W. L., Vijver, M. G., Peijnenburg, W. J., Bolte, J. F. & de Snoo, G. R. (2013). A review of the ecological effects of radiofrequency electromagnetic fields (RF-EMF). Environ. Int. 51, 116-140. 10.1016/j.envint.2012.10.009.
Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. & Neumann, P. (2012). Predictive markers of honey bee colony collapse. PLoS One, 7(2), e32151. 10.1371/journal.pone.0032151.
Decourtye, A., Devillers, J., Aupinel, P., Brun, F., Bagnis, C., Fourrier, J. & Gauthier, M. (2011). Honey bee tracking with microchips: a new methodology to measure the effects of pesticides. Ecotoxicology, 20(2), 429-437. 10.1007/s10646-011-0594-4.
Desneux, N., Decourtye, A. & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81-106. 10.1146/annurev.ento.52.110405.091440.
De la Rúa, P. Jaffé, R., Dall'Olio, R., Muñoz, I. & Serrano, J. (2009). Biodiversity, conservation and current threats to European Honey bees. Apidologie, 40(3), 263-284.
de Miranda, J. R., Cordoni, G. & Budge, G. (2010). The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J Invertebr. Pathol. 103,30-47
Di Prisco, G., Pennacchio, F., Caprio, E., Boncristiani Jr, H. F., Evans, J. D. & Chen, Y. (2011). Varroa destructor is an effective vector of Israeli acute paralysis virus in the Honey bee, Apis mellifera. J. Gen. Virol. 92(1), 151-155. 10.1099/vir.0.023853-0.
Djukic, M., Brzuszkiewicz, E., Fünfhaus, A., Voss, J., Gollnow, K., Poppinga, L., Heiko, L., Garcia-Gonzalez, E., Genersch, E. & Daniel, R. (2014). How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae. PLoS One, 9(3), e90914. 10.1371/journal.pone.0090914.
El Halabi, N., Achkar, R. & Haidar, G. A. (2013). The effect of cell phone radiations on the life cycle of honeybees," Eurocon 2013, pp. 529-536, doi: 10.1109/EUROCON.2013.6625032.
El Halabi, N., Achkar, R. & Haidar, G. A. (2014). "The effect of cell phone antennas' radiations on the life cycle of honeybees," MELECON 2014 - 2014 17th IEEE Mediterranean Electrotechnical Conference, pp. 408-414, doi: 10.1109/MELCON.2014.6820569.
Ellis, J. (2007). Colony collapse disorder (CCD) in honey bees. EDIS, 2007(15). file:///C:/Users/sinha/Downloads/cmcgillicuddy-in720%20(1).pdf.
Ellis, J. (2016).  Colony Collapse Disorder (CCD) in Honey Bees (ENY-150), UF/IFAS Entomology and Nematology Department.
Favre, D. (2017). Disturbing Honey bees’ behavior with electromagnetic waves: a methodology. J. Behav. 2, 1010. https://www.jscimedcentral.com/Behavior/behavior-2-1010.php.
Ferrari, T. E. (2014). Magnets, magnetic field fluctuations and geomagnetic disturbances impair the homing ability of honey bees (Apis mellifera). J. Apic. Res. 53(4), 452-465. https://doi.org/10.3896/IBRA.
Fievet, J., Tentcheva, D., Gauthier, L. et al. (2006). Localization of deformed wing virus infection in queen and drone Apis mellifera L.  Virol. J . 3, 16 https://doi.org/10.1186/1743-422X-3-16.
Flores, J. M., Gil-Lebrero, S., Gámiz, V., Rodríguez, M. I., Ortiz, M. A. & Quiles, F. J. (2019). Effect of the climate change on honey bee colonies in a temperate Mediterranean zone assessed through remote hive weight monitoring system in conjunction with exhaustive colonies assessment. Sci. Total Environ. 653, 1111-1119. 10.1016/j.scitotenv.2018.11.004.
Gajger, I. T., Sakac, M., & Gregorc, A. (2017). Impact of thiamethoxam on honey ˇ bee queen (Apis mellifera carnica) reproductive morphology and physiology. Bull. Environ. Contam. Toxicol. 99, 297–302. doi: 10.1007/s00128-017-2144-0.
Genersch, E. (2010). American Foulbrood in Honey bees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol. 103, S10-S19. https://doi.org/10.1016/j.jip.2009.06.015.
Genersch, E. & Aubert, M. (2010). Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Veterinary research, 41(6), 54.
Genersch, E., Ashiralieva, A. & 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. Appl. Environ. Microbiol. 71(11), 7551-7555. 10.1128/AEM.71.11.7551-7555.2005.
Gong, Y. & Diao, Q. (2017). Current knowledge of detoxification mechanisms of xenobiotic in honey bees. Ecotoxicol. Lond. Engl. 26, 1–12. doi: 10.1007/s10646- 016-1742-7.
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229), 1255957. 10.1126/science.1255957.
Grabensteiner, E., Ritter, W., Carter, M. J., Davison, S., Pechhacker, H., Kolodziejek, J., Boecking, O., Derakhshifar, I., Moosbeckhofer, R., Licek, E. & Nowotny, N. (2001). Sacbrood Virus of the honeybee (Apis mellifera): rapid identification and phylogenetic analysis using reverse transcription-PCR. Clin. Diagn. Lab. Immun. 8, 93-104.
Haddad, N. (2011). Honey bee viruses, diseases and hive management in the Middle East and their relation to the colony collapse disorder and bee losses. Bee Science, 11(1), 17-24. https://dergipark.org.tr/en/pub/uluaricilik/issue/52025/162346.
Haddad, N. J., Noureddine, A., Al-Shagour, B., Loucif-Ayad, W., ElNiweiri, M. A. A., Anaswah, E., Hammour, W. A., El-Obeid, D., Imad, A., Shebl, M. A., Almaleky, A. S., Nasher, A., Walid, N., Bergigui, M. F., Yañez, O. & de Miranda, J. R. (2017). Distribution and variability of deformed wing virus of honeybees (Apis mellifera) in the Middle East and North Africa. Insect Science, 24(1), 103-113. http://dx.doi.org/10.1111/1744-7917.12277.
Hamzelou, J. (2007). Where have all the bees gone? The Lancet, 370(9588), 639. https://doi.org/10.1016/S0140-6736(07)61319-1.
Harries-Jones, P. (2009). Honey bees, communicative order, and the collapse of ecosystems. Biosemiotics, 2(2), 193-204. 10.1007/s12304-009-9044-6.
Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P., Aptel, J., Tchamitchian, S. & Decourtye, A. (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336(6079), 348-350. 10.1126/science.1215039.
Higes, M., Martín-Hernández, R., Garrido-Bailón, E., Botías, C. & Meana, A. (2009). The presence of Nosema ceranae (Microsporidia) in North African honey bees (Apis mellifera intermissa). J. Apic. Res. 48(3), 217-219. https://doi.org/10.3896/IBRA.
Higes, M., Martín‐Hernández, R., Martínez‐Salvador, A., Garrido‐Bailón, E., González‐Porto, A. V., Meana, A., Bernal, J. L., Nozal, M. J. D. & Bernal, J. (2010). A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ. Microbiol. Rep. 2(2), 243-250. 10.1111/j.1758-2229.2009.00099.x.
Highfield, A. C., El Nagar, A., Mackinder, L. C., Noël, L. M., Hall, M. J., Martin, S. J., & Schroeder, D. C. (2009). Deformed wing virus implicated in overwintering honeybee colony losses. Applied and environmental microbiology, 75(22), 7212–7220. https://doi.org/10.1128/AEM.02227-09.
Iqbal, J. & Mueller, U. (2007). Virus infection causes specific learning deficits in honeybee foragers. Pr. Roy. Soc. B. 274, 1517-21.
John, C. A., Brendan, D. A., Andrew, P. P., Graham, T. J. & Gregor, R. (2020). Understanding the Effects of Sublethal Pesticide Exposure on Honey Bees: A Role for Probiotics as Mediators of Environmental Stress. Frontiers in Ecology and Evolution, 8.  https://doi.org/10.3389/fevo.2020.00022.
Johnson, R. (2011). Honey Bee Colony Collapse Disorder. DIANE Publishing. https://books.google.com/books?hl=en&lr=&id=SxaJTt3KgoEC&oi=fnd&pg=PA1&dq=Johnson,+R.+(2010).+Honey+bee+colony+collapse+disorder.&ots=aZ99MIQbGk&sig=9IyemjGE3OR562vPqhgIjVShRCs
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. Nat. Acad. Sci. 106(35), 14790-14795. https://doi.org/10.1073/pnas.0906970106.
Jones, A. K., Raymond-Delpech, V., Thany, S. H., Gauthier, M. & Sattelle, D. B. (2006). The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Res. 16(11), 1422-1430. 10.1101/gr.4549206.
Khezri, M. & Moharami, M. (2017). The Incidence of Acarapis woodi and Varroa destructor in Kurdistan Apiaries, Iran. Advances in Animal and Veterinary Sciences, 5. 10.11648/j.avs.20170506.11
Korolev, V (2022). Impact on next generation 5G cellular communications on honey bees. IOP Conf. Ser.: Earth Environ. Sci. 979 012013, 1-5. doi:10.1088/1755-1315/979/1/012013.
Koziorowska, A., Depciuch, J., Białek, J., Woś, I., Kozioł, K., Sadło, S. & Piechowicz, B. (2020). Electromagnetic field of extremely low frequency has an impact on selected chemical components of the Honey bee. Pol. J. Vet. Sci. 23(4), 537-544. 10.24425/pjvs.2020.134703.
Kumar, N. R., Rana, N. & Kalia, P. (2013). Biochemical changes in haemolymph of Apis mellifera L. drone under the influence of cell phone radiations. J. Appl. Nat. Sci. 5(1), 139-141. https://doi.org/10.31018/jans.v5i1.296.
Kumar, S. S. (2018). Colony collapse disorder (CCD) in honey Bees caused by EMF radiation. Bioinformation, 14(9), 521-524. 10.6026/97320630014521.
Le Conte, Y., Ellis, M. & Ritter, W. (2010). Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie, 41(3), 353-363. 10.1051/apido/2010017.
Le Goff, G. & Hilliou, F. (2017). Resistance evolution in Drosophila: the case of CYP6G1. Pest Manag. Sci. 73, 493–499. doi: 10.1002/ps.4470.
Leat, N., Ball, B., Govan, V. & Davison, S. (2000). Analysis of the complete genome sequence of black queen-cell virus, a picorna-like virus of honeybees. J. Gen. Virol. 81,2111-9.
Liang, C. H., Chuang, C. L., Jiang, J. A. & Yang, E. C. (2016). Magnetic sensing through the abdomen of the honey bee. Sci. Rep. 6(1), 1-7. https://doi.org/10.1038/srep23657.
López-Uribe, M. & Underwood, R. (2019). Honey Bee Diseases: American Foulbrood. https://extension.psu.edu/honey-bee-diseases-american-foulbrood.
Lu, C., Hung, Y. T. & Cheng, Q. (2020). A review of sub-lethal neonicotinoid insecticides exposure and effects on pollinators. Curr. Pollution Rep. 6(2), 137-151. https://doi.org/10.1007/s40726-020-00142-8.
Lupi, D., Mesiano, M. P., Adani, A., Benocci, R., Giacchini, R., Parenti, P., Zambon, G., Lavazza, A., Boniotti, M. A., Bassi, S., Colombo, M. & Tremolada, P. (2021). Combined Effects of Pesticides and Electromagnetic-Fields on Honey bees: Multi-Stress Exposure. Insects, 12(8), 716. 10.3390/insects12080716.
Maori, E., Lavi, S., Mozes-Koch, R., Gantman, Y., Peretz, Y., Edelbaum, O., Tanne, E. & Sela, I. (2007). Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra and inter-species recombination. J. Gen. Virol . 88, 3428-3.
Migdał, P., Murawska, A., Strachecka, A., Bieńkowski, P. & Roman, A. (2021). Honey bee proteolytic system and behavior parameters under the influence of an electric field at 50 hz and variable intensities for a long exposure time. Animals, 11(3), 863. 10.3390/ani11030863.
Mockel, N., Gisder, S. & Genersch, E. (2011). Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. Journal of General Virology, 92(2), 370–377. https://doi.org/10.1099/vir.0.025940-0
Nagaraja, N. & Rajagopal, D. (2019). Honey Bees: diseases, parasites, pests, predators and their management. MJP publisher.
Naug, D. (2009). Nutritional stress due to habitat loss may explain recent honey bee colony collapses. Biol. Conservation. 142(10), 2369-2372. https://doi.org/10.1016/j.biocon.2009.04.007.
Nicolson, S. W. (2009). Water homeostasis in bees, with the emphasis on sociality. J. Exp. Biol. 212(3), 429-434. https://doi.org/10.1242/jeb.022343.
Odemer, R. & Odemer, F. (2019). Effects of radiofrequency electromagnetic radiation (RF-EMF) on honey bee queen development and mating success. Sci. Total Environ. 661, 553-562. 10.1016/j.scitotenv.2019.01.154.
Oldroyd, B. P. (2007). What's killing American honey bees?. PLoS Biology, 5(6), e168. 10.1371/journal.pbio.0050168.
Price, R. I. & Gruter, C. (2015). Why, when and where did honey bee dance communication evolve? Front Ecol. Evol. 3, 125. https://doi.org/10.3389/fevo.2015.00125
Ragsdale, N. N., Hackett, K. & Kaplan, K. (2007). Vanishing honey bees-colony collapse disorder. Outlooks on Pest Management, 18(6), 280.
Roy, D., Debnath, P., Mondal, D. & Sarkar, P. (2018). Colony collapse disorder of honey bee: A neoteric ruction in global apiculture. Curr. Appl. Sci. Technol. 26(3), 1-12. 10.9734/CJAST/2018/38218.
Sammataro, D. (2006). An easy dissection technique for finding the tracheal mite, Acarapis woodi (Rennie)(Acari: Tarsonemidae), in honey bees, with video link. Int. J. Acarology. 32(4), 339-343. https://doi.org/10.1080/01647950608684479
Sharma, V. P. & Kumar, N. R. (2010). Changes in Honey bee behaviour and biology under the influence of cellphone radiations. Current Science, 98(10), 1376-1378. https://www.emf-portal.org/en/article/18302.
Shepherd, S., Hollands, G., Godley, V. C., Sharkh, S. M., Jackson, C. W. & Newland, P. L. (2019). Increased aggression and reduced aversive learning in honeybees exposed to extremely low frequency electromagnetic fields. Plos One, 14(10), e0223614. https://doi.org/10.1371/journal.pone.0223614.
Shepherd, S., Lima, M. A. P., Oliveira, E. E., Sharkh, S. M., Jackson, C. W. & Newland, P. L. (2018). Extremely low frequency electromagnetic fields impair the cognitive and motor abilities of honey bees. Sci. Rep. 8(1), 1-9. https://doi.org/10.1038/s41598-018-26185-y.
Shutler, D., Head, K., Burgher-MacLellan, K. L., Colwell, M. J., Levitt, A. L., Ostiguy, N. & Williams, G. R. (2014). Honey Bee Apis mellifera Parasites in the Absence of Nosema ceranae Fungi and Varroa destructor Mites. PloS One, 9(6), e98599.
Somerville, D. C. (2001). Nutritional value of bee collected pollen. Rural Ind. Res. Dev, Corp. 1–166 .
Somerville, D. C. & Nicol, H. I. Crude protein and amino acid composition of honey bee-collected pollen pellets from south-east Australia and a note on laboratory disparity. Aust. J. Exp. Agric. 46, 141–149 (2006).
Stanimirovic, Z., Glavinic, U., Ristanić, M., Aleksic, N., Jovanovic, N., Vejnović, B. & Stevanovic, J. (2019). Looking for the causes of and solutions to the issue of honey bee colony losses. Acta Veterinaria, 69. 1-31. 10.2478/acve-2019-0001.
Tantillo, G., Bottaro, M., Di Pinto, A., Martella, v., Di Pinto, P. & Terio, V. (2015). Virus infections of honeybees Apis mellifera. Italian Journal of Food Safety, 4,5364 doi:10.4081/ijfs.2015.5364
Taye, R. R., Deka, M. K., Borkataki, S., Panda, S. & Gogoi, J. (2017). Effect of electromagnetic radiation of cell phone tower on foraging behaviour of Asiatic honey bee, Apis cerana F. (Hymenoptera: Apidae). Journal of Entomology and Zoology Studies, 5(3), 1527-1529.
Taye, R. R., Deka, M. K., Borkataki, S., Panda, S. & Gogoi, J. (2018). Effect of electromagnetic radiation of cell phone tower on development of Asiatic Honey Bee, Apis cerana F. (Hymenoptera: Apidae). Int. J. Curr. Microbiol. Appl. Sci. 7, 4334-4339. https://doi.org/10.20546/ijcmas.2018.708.454.
Traynor, K. S., Mondet, F., de Miranda, J. R., Techer, M., Kowallik, V., Oddie, M. A. Y., Chantuwannakul, P. & McAfee, A. (2020). Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends in Parasitol. 36(7), 592-606. https://doi.org/10.1016/j.pt.2020.04.004
Vanbergen, A. J. (2013). Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Environ. 11(5), 251-259. https://doi.org/10.1890/120126 .
vanEngelsdorp, D., Cox-Foster, D., Frazier, M., Ostiguy, N. & Hayes, J. (2006). "Colony Collapse Disorder Preliminary Report". Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC)–CCD Working Group. 2006. pp. 22. http://www.beekeeping.com/articles/us/ccd.pdf
vanEngelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B. K., Frazier, M., Frazier, J., Cox-Foster, D., Chen, Y., Underwood, R., Tarpy, D. R. & Pettis, J. S. (2009). Colony collapse disorder: A descriptive study. PloS One, 4(8), e6481. https://doi.org/10.1371/journal.pone.0006481
vanEngelsdorp, D., Traynor, K. S., Andree, M., Lichtenberg, E. M., Chen, Y., Saegerman, C. & Cox-Foster, D. L. (2017). Colony Collapse Disorder (CCD) and bee age impact honey bee pathophysiology. PLoS One, 12(7) e0179535. https://doi.org/10.1371/journal.pone.0179535
Wang, Z. L., Liu, T. T., Huang, Z. Y., Wu, X. B., Yan, W. Y. & Zeng, Z. J. (2012). Transcriptome analysis of the Asian honey bee Apis cerana cerana. PloS One, 7(10), e47954. https://doi.org/10.1371/journal.pone.0047954
Wild, B., Dormagen, D. M., Zachariae, A., Smith, M. L., Traynor, K. S., Brockmann. D., Couzin, I. D. & Landgraf, T. (2021). Social networks predict the life and death of honey bees. Nat. Commun. 12(1), 1-12. https://www.nature.com/articles/s41467-021-21212-5
Wilson-Rich, N., Dres, S. T. & Starks, P. T. (2008). The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). J. Insect Physiol. 54(10-11), 1392-9. doi: 10.1016/j.jinsphys.20 08.07.016. Epub 2008 Aug 7. PMID: 18761014.
Wyszkowska, J., Grodzicki, P. & Szczygieł, M. (2019). Electromagnetic fields and colony collapse disorder of the Honey bee. Przegląd Elektrotechniczny, 95(1), 137-40. 10.15199/48.2019.01.35
Zhang, E. & Nieh, J. C. (2015). The neonicotinoid imidacloprid impairs honey bee aversive learning of simulated predation. J. Exp. Biol. 218(20), 3199-3205. 10.1242/jeb.127472.
Ziska, L. H., Pettis, J. S., Edwards, J., Hancock, J. E., Tomecek, M. B., Clark, A., Dukes, J. S., Loladze, I. & Polley, H. W. (2016). Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees. Proc. Royal Soc. B P ROY SOC B-BIOL SCI, 283(1828), 20160414. https://doi.org/10.1098/rspb.2016.0414
Zubrzak, B., Bieńkowski, P., Cała, P., Płaskota, P., Rudno-Rudziński, K. & Nowakowski, P. (2018). Thermal and acoustic changes in bee colony due to exposure to microwave electromagnetic field– preliminary research. Przegląd Elektrotechniczny, 1(12), 264-26710.15199/4 8.2018.12.60 .
Research Articles

How to Cite

Colony collapse disorder: A peril to apiculture. (2022). Journal of Applied and Natural Science, 14(3), 729-739. https://doi.org/10.31018/jans.v14i3.3502