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Prevalence of common honey bee pathogens at selected apiaries in Kenya, 2013/2014

Published online by Cambridge University Press:  17 October 2017

Juliette R. Ongus*
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772-00100, Nairobi, Kenya
Ayuka T. Fombong
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772-00100, Nairobi, Kenya
Janet Irungu
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772-00100, Nairobi, Kenya
Daniel Masiga
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772-00100, Nairobi, Kenya
Suresh Raina
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), PO Box 30772-00100, Nairobi, Kenya
*
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Abstract

The present study was part of a larger surveillance effort to identify the determinants of African honey bee health, and, particularly, to detect honey bee pathogens across Kenya, where 160 colonies were examined from 32 apiaries (five colonies/apiary). From each colony, 20 individual foragers, nurse bees, worker pupae, and drone pupae were sampled separately. These were organized as 30 foragers, 32 nurse bees, 28 worker pupae, and 10 drone pupae pools. Nucleic acid was extracted from the pooled homogenates and tested using a panel of 18 different (RT-)PCR methods targeted at detecting Paenibacillus larvae, Melissococcus plutonius, Ascophaera apis, Aspergillus spp., Nosema ceranae, N. apis, Deformed wing virus (DWV), Varroa destructor virus 1 (VDV 1), Acute bee paralysis virus (ABPV), Sacbrood virus (SBV), Israeli acute paralysis virus (IAPV), Black queen cell virus (BQCV), Chronic bee paralysis virus (CBPV), and Kashmir bee virus. All amplified bands were sequenced and compared to the GenBank database. VDV 1 was the most abundant virus at 50% prevalence in the 100 bee pools. It was closely followed by DWV at 44%. The others were BQCV (36%), SBV (14%), IAPV (9%), ABPV (8%), and N. ceranae (5%). The pathogens co-existed within apiaries. VDV 1 was present in 66% of the apiaries, DWV in 69%, BQCV in 69%, SBV in 28%, IAPV in 22%, ABPV in 19%, and N. ceranae in 13%. The study concludes that these pathogens should be incorporated in honey bee disease surveillance activities in the region.

Type
Research Paper
Copyright
Copyright © icipe 2017 

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References

Bakonyi, T., Farkas, R., Szendroi, A., Dobos-Kovacs, M. and Rusvai, M. (2002) Detection of acute bee paralysis virus by RT-PCR in honey bee and Varroa destructor field samples: Rapid screening of representative Hungarian apiaries. Apidologie 33, 6374. doi: 10.1051/apido: 2001004.CrossRefGoogle Scholar
Berg, J. M., Tymoczko, J. L. and Stryer, L. (2002) Biochemistry. 5th Revised edition. W.H. Freeman, New York, 128–131.Google Scholar
Biesmeijer, J. C., Roberts, S. P., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A. P., Potts, S. G., Kleukers, R., Thomas, C. D., Settele, J. and Kunin, W. E. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351354. doi: 10.1126/science.1127863.Google ScholarPubMed
Blanchard, P., Olivier, V., Iscache, A. L., Celle, O., Schurr, F., Lallemand, P. and Ribière, M. (2008) Improvement of RT-PCR detection of chronic bee paralysis virus (CBPV) required by the description of genomic variability in French CBPV isolates. Journal of Invertebrate Pathology 97, 182185.Google Scholar
Blanchard, P., Ribière, M., Celle, O., Lallemand, P., Schurr, F., Olivier, V., Iscache, A. L. and Faucon, J. P. (2007) Evaluation of a real-time two-step RT-PCR assay for quantitation of Chronic bee paralysis virus (CBPV) genome in experimentally-infected bee tissues and in life stages of a symptomatic colony. Journal of Virological Methods 141, 713.CrossRefGoogle ScholarPubMed
Carletto, J., Gauthier, A., Regnault, J., Blanchard, P., Schurr, F. and Ribière-Chabert, M. (2010) Detection of main honey bee pathogens by multiplex PCR. EuroReference, No. 4, ER04-10R02. http://www.anses.fr/euroreference/numero4/PN60I0.htm.Google Scholar
Costopoulou, C. I., Lambrou, M. A. and Harizanis, P. C. (2000) A framework for electronic trading of hive products. Bee World 81, 172181. doi: 10.1080/0005772X.2000.11099491.Google Scholar
Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., Quan, P.-L., Briese, T., Hornig, M., Geiser, D. M., Martinson, V., vanEngelsdorp, D., Kalkstein, A. L., Drysdale, A., Hui, J., Zhai, J., Cui, L., Hutchison, S. K., Simons, J. F., Egholm, M., Pettis, J. S. and Lipkin, W. I. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283286. doi: 10.1126/science.1146498.Google Scholar
Dietemann, V., Ellis, J. D. and Neumann, P. (Eds) (2013) The COLOSS BEEBOOK, Volume II: Standard Methods for Apis mellifera Pest and Pathogen Research. International Bee Research Association, Cardiff, UK. 356 pp.Google Scholar
Djordjevic, S. P., Noone, K., Smith, L. and Hornitzky, M. A. Z. (1998) Development of a hemi-nested PCR assay for the specific detection of Melissococcus pluton . Journal of Apicultural Research 37, 165174.Google Scholar
Dobbelaere, W., de Graaf, D., Peeters, J. E. and Jacobs, F. J. (2001) Development of a fast and reliable diagnostic method for American foulbrood disease (Paenibacillus larvae subsp. larvae) using a 16S rRNA gene based PCR. Apidologie 32, 363370.Google Scholar
Fitzpatrick, Ú., Murray, T. E., Paxton, R. J., Breen, J., Cotton, D., Santorum, V. and Brown, M. J. F. (2007) Rarity and decline in bumblebees – A test of causes and correlates in the Irish fauna. Biological Conservation 136, 185194.Google Scholar
Forsgren, E. and Fries, I. (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary Parasitology 170, 212217. doi: 10.1016/j.vetpar.2010.02.010.Google Scholar
Frazier, M., Caron, D. and vanEngelsdorp, D. (2011) A Field Guide to Honey Bees and Their Maladies. The Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC): Delaware, Maryland, New Jersey, Pennsylvania, West Virginia, Virginia, and the USDA cooperating. 85 pp. Available at: http://www.nj.gov/agriculture/divisions/pi/pdf/fieldguidetohoneybees.pdf.Google Scholar
Fries, I., Chauzat, M.-P., Chen, Y.-P., Doublet, V., Genersch, E., Gisder, S., Higes, M., McMahon, D. P., Martiń-Hernańdez, R., Natsopoulou, M., Paxton, R. J., Tanner, G., Webster, T. C. and Williams, G. R. (2013) Standard methods for Nosema research. Journal of Apicultural Research 52 (1), 128.Google Scholar
Gallai, N., Salles, J.-M., Settele, J. and Vaissière, B. E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68, 810821.Google Scholar
Garrido-Bailón, E., Higes, M., Martínez-Salvador, A., Antúnez, K., Botías, C., Meana, A., Prieto, L. and 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, 731739.Google Scholar
Glass, N. L. and Donaldson, G. C. (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61, 13231330.Google Scholar
Govan, V. A., Brözel, V., Allsopp, M. H. and Davison, S. (1998) A PCR detection method for rapid identification of Melissococcus pluton in honeybee larvae. Applied and Environmental Microbiology 64, 19831985.Google Scholar
Grabensteiner, E., Ritter, W., Carter, M. J., Davison, S., Pechhacker, H., Kolodziejek, J., Boecking, O., Derakhshifar, I., Moosbeckhofer, R., Licek, E. and Nowotny, N. (2001) Sacbrood virus of the honeybee (Apis mellifera): rapid identification and phylogenetic analysis using reverse transcription-PCR. Clinical and Vaccine Immunology 8, 93104.Google ScholarPubMed
Graystock, P., Blane, E. J., McFrederick, Q. S., Goulson, D. and Hughes, W. O. H. (2015) Do managed bees drive parasite spread and emergence in wild bees? International Journal for Parasitology: Parasites and Wildlife 5, 6475. https://doi.org/10.1016/j.ijppaw.2015.10.001.Google Scholar
James, R. R. and Skinner, J. S. (2005) PCR diagnostic methods for Ascosphaera infections in bees. Journal of Invertebrate Pathology 90, 98103.Google Scholar
Kasina, J. M., Mburu, J., Kraemer, M. and Holm-Mueller, K. (2009) Economic benefit of crop pollination by bees: A case of Kakamega small-holder farming in western Kenya. Journal of Economic Entomology 102, 467473.Google Scholar
Klatt, B. K., Holzschuh, A., Westphal, C., Clough, Y., Smit, I., Pawelzik, E. and Tscharntke, T. (2014) Bee pollination improves crop quality, shelf life and commercial value. Proceedings of the Royal Society B 281, 20132440. https://doi.org/10.1098/rspb.2013.2440.Google Scholar
Klein, A.-M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. and Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B 274, 303313. doi:10.1098/rspb.2006.3721.Google Scholar
Kluser, S. and Peduzzi, P. (2007) Global Pollinator Decline: A Literature Review. UNEP/GRID-Europe, Geneva, Switzerland, 10 pp. Available at: http://www.grid.unep.ch/products/3_Reports/Global_pollinator_decline_literature_review_2007.pdf.Google Scholar
Kremen, C. and Ricketts, T. (2000) Global perspectives on pollination disruptions. Conservation Biology 14, 12261228.Google Scholar
Lauro, F. M., Favaretto, M., Covolo, L., Rassu, M. and Bertoloni, G. (2003) Rapid detection of Paenibacillus larvae from honey and hive samples with a novel nested PCR protocol. International Journal of Food Microbiology 81, 195201.CrossRefGoogle ScholarPubMed
Lefever, S., Pattyn, F., Hellemans, J. and Vandesompele, J. (2013) Single-nucleotide polymorphisms and other mismatches reduce performance of quantitative PCR assays. Clinical Chemistry 59, 14701480.Google Scholar
Macharia, P. (2004) Gateway to Land and Water Information. Kenya National Report. Kenya Soil Survey. Ministry of Agriculture of the Government of Kenya. Available at: http://www.apipnm.org/swlwpnr/reports/y_sf/z_ke/ke.htm#menu Google Scholar
Martín-Hernández, R., Meana, A., Prieto, L., Martinez-Salvador, A., Garrido-Bailón, E. and Higes, M. (2007) Outcome of colonization of Apis mellifera by Nosema ceranae . Applied and Environmental Microbiology 73, 63316338.Google Scholar
Mckee, B. A., Djordjevic, S. P., Goodman, R. D. and Hornitzky, M. A. (2003) The detection of Melissococcus pluton in honey bees (Apis mellifera) and their products using a hemi-nested PCR. Apidologie 34, 1927.Google Scholar
Mokili, J. L., Rohwer, F. and Dutilh, B. E. (2012) Metagenomics and future perspectives in virus discovery. Current Opinion in Virology 2, 6377.Google Scholar
Muli, E., Patch, H., Frazier, M., Frazier, J., Torto, B., Baumgarten, T., Kilonzo, J., Kimani, J. N., Mumoki, F., Masiga, D., Tumlinson, J. and 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 (4), e94459.Google Scholar
Mumoki, F. N., Fombong, A., Muli, E., Muigai, A. W. T. and Masiga, D. (2014) An inventory of documented diseases of African honeybees. African Entomology 22, 473487.Google Scholar
OIE [World Organisation for Animal Health] (2008) OIE Terrestrial Manual, 2008. World Organisation for Animal Health, Paris, France, 387 pp.Google Scholar
OIE [World Organisation for Animal Health] (2012) Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. 7th edn. Volumes 1 and 2, World Organisation for Animal Health (OIE), Paris, France, 1404 pp.Google Scholar
Oldroyd, B. P. (2007). What's killing American honey bees. PLOS Biology 5, 1195.Google Scholar
Ongus, J. R. (2006) Varroa destructor virus 1: A new picorna-like virus in Varroa mites as well as honeybees. PhD thesis, Wageningen University, Wageningen, The Netherlands. 126 pp.Google Scholar
Pirk, C. W. W., Strauss, U., Yusuf, A. A. Démares, F. and Human, H. (2016) Honeybee health in Africa―a review. Apidologie 47, 276300.Google Scholar
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O. and Kunin, W. E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25, 345353. https://doi.org/10.1016/j.tree.2010.01.007.CrossRefGoogle ScholarPubMed
Richards, A. J. (2001) Does low biodiversity resulting from modern agricultural practice affect crop pollination and yield?. Annals of Botany 88, 165172.Google Scholar
Rodríguez, M., Vargas, M., Antúnez, K., Gerding, M., Castro, F. O. and Zapata, N. (2014) Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Chilean Journal of Agricultural Research 74, 170177.Google Scholar
Ryba, S., Titera, D., Schodelbauerova-Traxmandlova, I. and Kindlmann, P. (2012) Prevalence of honeybee viruses in the Czech Republic and coinfections with other honeybee diseases. Biologia 67, 590595.Google Scholar
Sguazza, G. H., Reynaldi, F. J., Galosi, C. M. and Pecoraro, M. R. (2013) Simultaneous detection of bee viruses by multiplex PCR. Journal of Virological Methods 194, 102106.Google Scholar
Shimanuki, H. and Knox, D. A. (2000) Diagnosis of Honey Bee Diseases. United States Department of Agriculture, Agricultural Research Service. Agriculture Handbook Number 690. Available at: https://www.ars.usda.gov/is/np/honeybeediseases/honeybeediseases.pdf.Google Scholar
Sipos, R., Székely, A. J., Palatinszky, M., Révész, S., Márialigeti, K. and Nikolausz, M. (2007) Effect of primer mismatch, annealing temperature and PCR cycle number on 16S rRNA gene-targeting bacterial community analysis. FEMS Microbiology Ecology 60, 341350.Google Scholar
Sombroek, W. G., Braun, H. M. H. and Van der Pouw, B. J. A. (1982) Explanatory soil map and agro-climatic zone map of Kenya, 1980. Scale 1:1,000,000. Kenya Soil Survey, Nairobi. 56 pp.Google Scholar
Steffan-Dewenter, I., Potts, S. G. and Packer, L. (2005) Pollinator diversity and crop pollination services are at risk. TRENDS in Ecology and Evolution 20, 651652.Google Scholar
Stevanovic, J., Stanimirovic, Z., Genersch, E., Kovacevic, S. R., Ljubenkovic, J., Radakovic, M. and Aleksic, N. (2011) Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie 42, 4958.Google Scholar
Strauss, U., Human, H., Gauthier, L., Crewe, R. M., Dietemann, V. and Pirk, C. W. W. (2013) Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata). Journal of Invertebrate Pathology 114, 4552.Google Scholar
Van Engelsdorp, D., Underwood, R., Caron, D. and Hayes, J. (2007) An estimate of managed colony losses in the winter of 2006–2007: A report commissioned by the apiary inspectors of America. American Bee Journal 147, 599603.Google Scholar
Westerkamp, C. and Gottsberger, G. (2002) The costly crop pollination crisis, pp. 5156. In Pollinating Bees: The Conservation Link Between Agriculture and Nature (edited by Kevan, P. G. and Imperatriz-Fonseca, V. L.). Ministry of Environment, Brasilia.Google Scholar
White, T. J., Bruns, T., Lee, S. and Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , pp. 315322. In PCR Protocols: A Guide to Methods and Applications (edited by Innis, M. A., Gelfand, D. H., Sninsky, J. J. and White, T. J.). Academic Press Inc., San Diego, USA.Google Scholar
Withgott, J. (1999) Pollination migrates to top of conservation agenda. BioScience 49, 857862.Google Scholar