Molecular Examination of Pathogens in the Red Dwarf Honeybee, Apis Florea, in Southwest Saudi Arabia
DOI:
https://doi.org/10.53555/jaz.v45i6.4985Keywords:
Apis florea, honeybee viruses, Nosema spp, Melissococcus plutonius, Saudi ArabiaAbstract
Apis florea is a wild honeybee native to Asia that is currently spreading throughout the countries of the Middle East and East Africa, including Saudi Arabia. The spread of these honeybees raises questions regarding their pathogens, pests, and the diseases they may harbor. This is the first study of the prevalence of A. florea pathogens in Saudi Arabia. Samples from three different locations were diagnosed to identify six honeybee viruses: acute bee paralysis virus (ABPV), chronic bee paralysis virus (CBPV), black queen cell virus (BQCV), deformed wing virus type A (DWV-A), deformed wing virus type B (DWV-B), and sacbrood virus (SBV); two microsporidian gut parasites, Nosema apis and Nosema ceranae; one fungi, Ascosphaera apis; two bacterial pathogens, Paenibacillus larvae and Melissococcus plutonius; and the ectoparasites Euvarroa sinhai and Varroa destructor. In this study, ABPV, CBPV, BQCV, DWV-A, N. apis, N. ceranae, and M. plutonius were detected in A. florea, while DWV-B, SBV, A. apis, P. larvae, E. sinhai, and V. destructor were absent. The findings of this study represent the initial contribution to understanding the presence of pathogens in the A. florea honeybee in Saudi Arabia. However, further research is necessary to develop sustainable strategies for the beekeeping industry and awareness of pathogens that cause diseases in the country.
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References
1- Rader R, Bartomeus I, Garibaldi LA, Garratte MPD et al. 2016. Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Science of the USA 113: 146–151.
2- Lord, W. G., & Nagi, S. K. (1987). Apis Florea Discovered in Africa. Bee World, 68(1), 39–40.
3- Hepburn, H. R., & Radloff, S. E. (2011). Honeybees of Asia. Springer Science & Business Media.
4- Saraithong, P., Li, Y., Saenphet, K., Chen, Z. and Chantawannakul, P. (2015). Bacterial community structure in Apis florea larvae analyzed by denaturing gradient gel electrophoresis and 16S rRNA gene sequencing. Insect Science, 22(5), pp. 606-618.
5- Özkan Koca, A., Moradi, M.G., Deliklitas, Ö, Uçan, A. and Kandemir, I. (2018). Discrimination of dwarf honey bee (Apis florea, Fabricius 1876) populations in Iran using elliptic Fourier wing cell shape analysis. Journal of Apicultural Research, 57(2), pp. 195-202.
6- Moritz, R., Haddad, N., Bataieneh, A., Shalmon, B. and Hefetz, A. (2010). Invasion of the dwarf honeybee Apis florea into the near East. Biological Invasions, 12(5), pp. 1093-1099.
7- Bezabih, G., Adgaba, N., Hepburn, H.R. and Pirk, C.W.W. (2014). The territorial invasion of Apis florea in Africa. African Entomology, 22(4), pp. 888-890.
8- Al-Kahtani, S. N., & Taha, E. A. (2014). Morphometric studies on dwarf honey bee Apis florea F. workers in Saudi Arabia. Journal of Apicultural Science, 58(1), 127–134.
9- Steiner, W.E. (2017). A scientific note on the arrival of the dwarf honeybee, Apis florea (Hymenoptera: Apidae), in Djibouti. Apidologie, 48(5), pp. 657-659.
10- Shebl, M.A. (2017). Discovery of Apis florea Colonies in Northeastern Egypt. African Entomology, 25(1), pp. 248-249.
11- Nanork, P., Paar, J., Chapman, N.C., Wongsiri, S. and Oldroyd, B.P. (2005). Asian honeybees parasitize the future dead. Nature, 437(7060), pp. 829.
12- Tian, J.-X.; Tsai,W.-S.; Sung, I.-H. A Novel Variant of Deformed Wing Virus (DWV) from the Invasive Honeybee Apis florea (Apidae, Hymenoptera) and Its Ectoparasite Euvarroa sinhai (Acarina, Mesostigmata) in Taiwan. Insects 2023, 14, 103.
13- El-Niweiri, M. a. A., Moritz, R. F. A., & Lattorff, H. M. G. (2019). The Invasion of the Dwarf Honeybee, Apis florea, along the River Nile in Sudan. Insects, 10(11), 405.
14- Alghamdi, A. and Nuru, A. (2013). Beekeeping in the Kingdom of Saudi Arabia Past and Present Practices. Bee World, 90(2), pp. 26-29.
15- Hroobi, A. (2020). Deformed wing virus in managed and wild honeybees in Saudi Arabia and Australia: Discovery, Detection, and Characterization [PHD Dissertation]. University of Abrdeen. [PhD Dissertation]. University of Abredeen.
16- Bhattacharyya, M., Chakraborty, S.K., Acharya, S.K., 2019. Proboscis extension reflex in Apis florea (Hymenoptera: Apidae) in response to temperature. J. Entomol. Sci. 54 (3), 238–249.
17- (Cavigli, I., Daughenbaugh, K. F., Martin, M., Lerch, M. D., Banner, K., Garcia, E., Brutscher, L. M., & Flenniken, M. L. (2015). Pathogen prevalence and abundance in honey bee colonies involved in almond pollination. Apidologie, 47(2), 251–266.
18- Matthijs, S., De Waele, V., Vandenberge, V., Verhoeven, B., Evers, J., Brunain, M., Saegerman, C., De Winter, P.J.J., Roels, S., de Graaf, D.C. and De Regge, N. 2020. Nationwide Screening for Bee Viruses and Parasites in Belgian Honey Bees. Viruses. 12(8): 890. doi:10.3390/v12080890.
19- Ngor, L., Palmer-Young, E.C., Nevarez, R.B., Russell, K.A., Leger, L., Giacomini, S.J., Pinilla-Gallego, M.S., Irwin, R.E. and McFrederick, Q.S. 2020. Cross-infectivity of honey and bumble bee-associated parasites across three bee families. Parasitology. 147(12): 1290-1304.
20- Vanengelsdorp, D.; Meixner, M.D. A Historical Review of Managed Honey Bee Populations in Europe and the United States and the Factors That May Affect Them. J. Invertebr. Pathol. 2010, 103, S80–S95.
21- Gisder, S.; Genersch, E. Special Issue: Honey Bee Viruses. Viruses 2015, 7, 5603–5608.
22- Higes, M.; Martín-Hernández, R.; Botías, C.; Bailón, E.G.; González-Porto, A.V.; Barrios, L.; del Nozal, M.J.; Bernal, J.L.; Jiménez, J.J.; Palencia, P.G.; et al. How Natural Infection by Nosema ceranae Causes Honeybee Colony Collapse. Environ. Microbiol. 2008, 10, 2659–2669.
23- Gómez-moracho, T.; Heeb, P.; Lihoreau, M. Effects of parasites and pathogens on bee cognition. Ecol. Entomol. 2017, 42, 51–64.
24- Seeley, T.D.; Smith, M.L. Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie 2015, 46, 716–727.
25- Chahal, B.S.; Brar, H.S.; Gatoria, G.S.; Jhajj, H.S. Aggressive behavior of Apis florea towards Apis mellifera in hive robbing and in foraging. J. Apic. Res. 1986, 25, 134–138.
26- El-Niweiri, M.A.A.; El-Sarrag, M.S.A.; Satti, A.A. Detection, distribution and incidences of insect pests and predators of honeybees (Apis mellifera L.) in Sudan. Albuhuth 2005, 9, 104–122.
27- Koeniger, N., Koeniger, G. and Delfinado-Baker, M. (1983). Observations on mites of the Asian honeybee species (Apis cerana, Apis dorsata, Apis florea). Apidologie, 14(3), pp. 197-204.
28- Goulson, D. Eects of introduced bees on native ecosystems. Annu. Rev. Ecol. Evol. Syst. 2003, 34, 1–26.
29- Runckel, C., Flenniken, M.L., Engel, J.C., Ruby, J.G., Ganem, D., Andino, R., DeRisi, J.L. (2011) Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE 6 , e20656. doi:10.1371/journal.pone.0020656.
30- Teixeira, É. W., Chen, Y., Message, D., Pettis, J., & Evans, J. D. (2008). Virus infections in Brazilian honey bees. Journal of Invertebrate Pathology, 99(1), 117–119.
31- Ribière, M., Triboulot, C., Mathieu, L., Aurieres, C., Faucon, J-P., & Pépin, M. (2002). Molecular diagnosis of chronic bee paralysis virus infection. Apidologie, 33, 339-351
32- Benjeddou, M., Leat, N., Allsopp, M., & Davison, S. (2001). Detection of acute bee paralysis virus and black queen cell virus from honey bees by reverse transcriptase PCR. Applied and Environmental Microbiology, 67(5), 2384-2387
33- Bradford, E. L., Christie, C. R., Campbell, E. M., & Bowman, A. S. (2017). A real-time PCR method for quantification of the total and major variant strains of the deformed wing virus. PLoS ONE, 12(12), e0190017
34- Moore, J. D., Jironkin, A., Chandler, D., Burroughs, N. J., Evans, D. J., & Ryabov, E. V. (2011). Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. Journal of General Virology, 92, 156-161
35- Wang, M., Bi, J., Wang, L., Zhou, D., Ma, X., Li, W., Zhao, W., Yin, G., Liu, J., & He, S. (2016). Prevalence of Four Common Bee RNA Viruses in Eastern Bee Populations in Yunnan Province, China. J Veterinar Sci Technol, 7(1)
36- Chen, Y., Evans, J. D., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T., Litkowski, A., & Pettis, J. S. (2009). Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. Journal of Invertebrate Pathology, 101(3), 204–209.
37- James, R., & Skinner, J. (2005b). PCR diagnostic methods for Ascosphaera infections in bees. Journal of Invertebrate Pathology, 90(2), 98–103.
38- Garrido‐Bailón, E., Higes, M., Martínez‐Salvador, A., Antúnez, K., Botías, C., Meana, A., Prieto, L., & Martín‐Hernández, R. (2013). The prevalence of the honeybee brood pathogens Ascosphaera apis, Paenibacillus larvae and Melissococcus plutonius in Spanish apiaries determined with a new multiplex PCR assay. Microbial Biotechnology, 6(6), 731–739.
39- Govan, V. A., Brözel, V., Allsopp, M. H., & Davison, S. (1998). A PCR Detection Method for Rapid Identification of Melissococcus pluton in Honeybee Larvae. Applied and Environmental Microbiology, 64(5), 1983–1985.
40- Dietemann, V., Ellis, J. D., & Neumann, P. (Eds.). (2013). The COLOSS BEEBOOK Volume II: Standard methods for Apis mellifera pest and pathogen research. Journal of Apicultural Research
41- Potts, S., Biesmeijer, J., Kremen, C., Neumann, P., Schweiger, O., and Kunin, W. (2010). Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353.
42- Ganeshprasad, D. N., Lone, J. K., Jani, K., Shouche, Y. S., Khan, K. A., Sayed, S., Shukry, M., Dar, S. A., Mushtaq, M., & Sneharani, A. H. (2022). Gut Bacterial Flora of Open Nested Honeybee, Apis florea. Frontiers in Ecology and Evolution, 10.
43- Shwetha, B. V., Bhat, N. S., & Neethu, T. (2020). Utilization of Apis florea in Crop Pollination. In CRC Press eBooks (pp. 107–123).
44- Deutsch, K. R., Graham, J. R., Boncristiani, H. F., Bustamante, T., Mortensen, A. N., Schmehl, D. R., Wedde, A. E., Lopez, D. L., Evans, J. D., & Ellis, J. D. (2023). Widespread distribution of honey bee-associated pathogens in native bees and wasps: Trends in pathogen prevalence and co-occurrence. Journal of Invertebrate Pathology, 200, 107973.
45- Sébastien, A., Lester, P. J., Hall, R. J., Wang, J., Moore, N. E., & Gruber, M. a. M. (2015). Invasive ants carry novel viruses in their new range and form reservoirs for a honeybee pathogen. Biology Letters, 11(9), 20150610.
46- Campbell, E. M., McIntosh, C. H., & Bowman, A. S. (2016). A Toolbox for Quantitative Gene Expression in Varroa destructor: RNA Degradation in Field Samples and Systematic Analysis of Reference Gene Stability. PLoS ONE, 11(5), e0155640.
47- Gajger, I. T., Šimenc, L., & Toplak, I. (2021). The First Detection and Genetic Characterization of Four Different Honeybee Viruses in Wild Bumblebees from Croatia. Pathogens, 10(7), 808.
48- Zhang, X., He, S. Y., Evans, J. D., Pettis, J. S., Yin, G. F., & Chen, Y. P. (2012). New evidence that deformed wing virus and black queen cell virus are multi-host pathogens. Journal of Invertebrate Pathology, 109(1), 156–159.
49- Lin, Z., Zhao, L., Cao, L., Xu, H., Miao, C., Jie, H., Zhang, Z., Liu, Y., Zhang, N., Gao, F., Wang, Z., Chen, G., & Ji, T. (2021). A Survey of Common Pathogens of Apis spp. in Wild Non-Cave Honeybees in Southwest China. Journal of Wildlife Diseases, 57(4).
50- Han, B., & Weiss, L. M. (2017). Microsporidia: obligate intracellular pathogens within the fungal kingdom. In ASM Press eBooks (pp. 97–113).
51- Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., Puerta, F., Ruz, J. M., Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I., & Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96(1), 1–10.
52- Chaimanee, V., Warrit, N., & Chantawannakul, P. (2010). Infections of Nosema ceranae in four different honeybee species. Journal of Invertebrate Pathology, 105(2), 207–210.
53- Suwannapong, G., Maksong, S., Seanbualuang, P., & Benbow, M. E. (2010). Experimental infection of red dwarf honeybee, Apis florea, with Nosema ceranae. Journal of Asia-Pacific Entomology, 13(4), 361–364.
54- 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.
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