Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-18T10:22:49.730Z Has data issue: false hasContentIssue false
  • English
  • Français

A descriptive study of the prevalence of parasites and pathogens in Chinese black honeybees

Published online by Cambridge University Press:  17 July 2015

WENJUN PENG ,
JILIAN LI ,
YAZHOU ZHAO ,
YANPING CHEN  and
ZHIJIANG ZENG
WENJUN PENG
Affiliation:
Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Science, Xiangshan, Beijing 100093, China
JILIAN LI
Affiliation:
Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Science, Xiangshan, Beijing 100093, China
YAZHOU ZHAO
Affiliation:
Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Science, Xiangshan, Beijing 100093, China
YANPING CHEN
Affiliation:
USDA-ARS Bee Research Laboratory, Beltsville, MD 20705, USA
ZHIJIANG ZENG*
Affiliation:
Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China
*
* Corresponding author. Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The Chinese black honey bee is a distinct honey bee subspecies distributed in the Xinjiang, Heilongjiang and Jilin Provinces of China. We conducted a study to investigate the genetic origin and the parasite/pathogen profile on Chinese black honeybees. The phylogenetic analysis indicated that Chinese black honeybees were two distinct groups: one group of bees formed a distinct clade that was most similar to Apis mellifera mellifera and the other group was a hybrid of the subspecies, Apis mellifera carnica, Apis mellifera anatolica and Apis mellifera caucasica. This suggests that the beekeeping practices might have promoted gene flow between different subspecies. Screening for pathogens and parasites showed that Varroa destructor and viruses were detected at low prevalence in Chinese black honeybees, compared with Italian bees. Further, a population of pure breeding black honeybees, A. m. mellifera, displayed a high degree of resistance to Varroa. No Varroa mites or Deformed wing virus could be detected in any examined bee colonies. This finding suggests that a population of pure breeding Chinese black honeybees possess some natural resistance to Varroa and indicated the need or importance for the conservation of the black honeybees in China.

Keywords

Chinese black honeybeeVarroavirusesresistanceconservation
Type
Research Article
Information
Parasitology , Volume 142 , Issue 11 , September 2015 , pp. 1364 - 1374
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altschul, S. F., Gish, W. and Miller, W. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Anderson, D. and Trueman, J. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology 24, 165–189.CrossRefGoogle ScholarPubMed
Arechavaleta-Velasco, M. E., Alcala-Escamilla, K., Robles-Rios, C., Tsuruda, J. M. and Hunt, G. J. (2012). Fine-scale linkage mapping reveals a small set of candidate genes influencing honey bee grooming behavior in response to Varroa mites. PLoS ONE 7, e47269.CrossRefGoogle ScholarPubMed
Becher, M. A., Osborne, J. L., Thorbek, P., Kennedy, P. J. and Grimm, V. (2013). Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models. Journal of Applied Ecology 50, 868–880.CrossRefGoogle ScholarPubMed
Bowen-Walker, P., Martin, S. and Gunn, A. (1999). The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. Journal of Invertebrate Pathology 73, 101–106.CrossRefGoogle ScholarPubMed
Branco, M. R., Kidd, N. A. C. and Pickard, R. S. (2006). A comparative evaluation of sampling methods for Varroa destructor (Acari: Varroidae) population estimation. Apidologie 37, 452–461.CrossRefGoogle Scholar
Carreck, N. L., Ball, B. V. and Martin, S. J. (2010). Honey bee colony collapse and changes in viral prevalence associated with Varroa destructor . Journal of Apicultural Research 49, 93–94.CrossRefGoogle Scholar
Chen, Y. P., Higgins, J. A. and Feldlaufer, M. F. (2004). Quantitative analysis of Deformed wing virus infection in the honey bee, Apis mellifera L. by real-time RT–PCR. Applied and Environmental Microbiology 71, 436–441.CrossRefGoogle Scholar
Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G. and Evans, J. D. (2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287.CrossRefGoogle ScholarPubMed
DeJong, D., DeJong, P. H. and Goncalves, L. S. (1982). Weight loss and other damage to developing worker honey bees from infestation with Varroa jacobsoni . Journal of Apicultural Research 21, 165–167.CrossRefGoogle Scholar
de Miranda, J. R., Chen, Y. P., Ribière, M. and Gauthier, L. (2011). Varroa and viruses. In Varroa – Still a Problem in the 21st Century (ed. Carreck, N. L.), pp. 11–31. International Bee Research Association, Cardiff, UK.Google Scholar
Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., Delaplane, K. S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P. and Ellis, J. D. (2013). Standard methods for Varroa research. Journal of Apicultural Research 52, doi: 10.3896/IBRA.3891.3852.3891.3809.CrossRefGoogle Scholar
Di Prisco, G., Pennacchio, F., Caprio, E., Boncristiani, H. F. and Evans, J. D. (2011). Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera . Journal of General Virology 92, 151–155.CrossRefGoogle ScholarPubMed
Evans, J. D., Schwarz, R. S., Chen, Y. P., Budge, G., Cornman, R. S., De la Rua, P., de Miranda, J. R., et al. (2013). Standard methods for molecular research in Apis mellifera . Journal of Apicultural Research 52. doi: 10.3896/IBRA.1.52.4.11.CrossRefGoogle Scholar
Gallai, N., Salles, J. M., Settele, J., Vaissière, B. E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68, 810–821.CrossRefGoogle Scholar
Garnery, L., Solignac, M., Celebrano, G. and Cornuet, J. M. (1993). A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structure of Apis mellifera L. Experientia 49, 1016–1021.CrossRefGoogle Scholar
Genersch, E. (2010). Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology 87, 87–97.CrossRefGoogle ScholarPubMed
Guzmán-Novoa, E. E. L., Calvete, Y., Mcgowan, J., Kelly, P. G. and Correa-Benítez, A. (2009). Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apodologie 41, 443–450.CrossRefGoogle Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Series No. 41, pp. 95–98.Google Scholar
Harbo, J. and Harris, J. (1999). Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). Journal of Economic Entomology 92, 261–265.CrossRefGoogle Scholar
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 and Bee World 48, 156–161.CrossRefGoogle Scholar
Higes, M., Martin-Hernandez, R., Botias, C., Bailon, E. G. and Gonzalez-Porto, A. V. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology 10, 2659–2669.CrossRefGoogle ScholarPubMed
Human, H., Archer, C. R., du Rand, E. E., Pirk, C. W. W. and Nicolson, S. W. (2014). Resistance of developing honeybee larvae during chronic exposure to dietary nicotine. Journal of Insect Physiology 69, 245–250.CrossRefGoogle ScholarPubMed
Klee, J., Besana, A. M., Genersch, E., Gisder, S. and Nanetti, A. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera . Journal of Invertebrate Pathology 96, 1–10.CrossRefGoogle ScholarPubMed
Korpela, S., Aarhus, A., Fries, I. and Hansen, H. (1992). Varroa jacobsoni Oud. in cold climates: population growth, winter mortality and influence on the survival of honey bee colonies. Journal of Apicultural Research 31, 157–164.CrossRefGoogle Scholar
Kovac, H. and Crailsheim, K. (1988). Lifespan of Apis mellifera carnica Pollm. infested by Varroa jacobsoni Oud. in relation to season and extent of infestation. Journal of Apicultural Research 27, 230–238.CrossRefGoogle Scholar
Li, J., Qin, H., Wu, J., Sadd, B. M., Wang, X., Peng, W. J., Wu, J. and Chen, Y. P. (2012). The prevalence of parasites and pathogens in Asian honeybees Apis cerana in China. PLoS ONE 7, e47955.Google ScholarPubMed
Martin, S. J., Highfield, A. C., Brettell, L., Villalobos, E. M. and Budge, G. E. (2012). Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306.CrossRefGoogle ScholarPubMed
Oxley, P. R., Spivak, M. and Oldroyd, B. P. (2010). Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Molecular Ecology 19, 1452–1461.CrossRefGoogle ScholarPubMed
Peng, W. J., Luo, J. H., An, J. D., Huang, J. X. and Guo, J. (2009). Analysis of genetic relationships of Northeastern Black Bee (Apis mellifera ssp.) in China. Scientia Agricultura Sinica 42, 1494–1502.Google Scholar
Peng, W. J., Luo, J. H., Chun, L. C., Dong, L. X. and Zhen, M. Y. (2012). Genetic relationships of the Raohe black bee (Apis mellifera ssp.) inferred from microsatellite markers. Chinese Journal of Applied Entomology 49, 1160–1166.Google Scholar
Pirk, C. W. W., Human, H., Crewe, R. M. and vanEngelsdorp, D. (2014). A survey of managed honey bee colony losses in the Republic of South Africa-2009 to 2011. Journal of Apicultural Research 53, 35–42.CrossRefGoogle Scholar
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P. and Schweiger, O. (2010). Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25, 345–353.CrossRefGoogle ScholarPubMed
Rosenkranz, P., Aumeier, P. and Ziegelmann, B. (2010). Biology and control of Varroa destructor . Journal of Invertebrate Pathology 103, S96–S119.CrossRefGoogle ScholarPubMed
Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biological Evolution 4, 406–425.Google Scholar
Shen, M., Yang, X., Cox-Foster, D. and Cui, L. (2005). The role of Varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 342, 141–149.CrossRefGoogle Scholar
Smith, K. M., Loh, E. H., Rostal, M. K., Zambrana-Torrelio, C. M. and Mendiola, L. (2013). Pathogens, pests, and economics: drivers of honey bee colony declines and losses. Ecohealth 10, 434–445.CrossRefGoogle ScholarPubMed
Spivak, M. (1996). Honey bee hygienic behavior and defense against Varroa jacobsoni . Apidologie 27, 245–260.CrossRefGoogle Scholar
Tamura, K., Nei, M. and Kumar, S. (2004). Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America 101, 11030–11035.CrossRefGoogle ScholarPubMed
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biological Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle Scholar
Van Engelsdorp, D. and Meixner, M. D. (2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology 103(Suppl. 1), S80–S95.CrossRefGoogle Scholar
Van Engelsdorp, D., Underwood, R., Caron, D. and Hayes, J. Jr. (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, 599–603.Google Scholar
Van Engelsdorp, D., Hayes, J., Underwood, R., Pettis, J. and Gay, N. (2008). A survey of honey bee colony losses in the, U. S., Fall 2007 to Spring 2008. PLoS ONE 3, 12.Google Scholar
Van Engelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C. and Haubruge, E. (2009). Colony collapse disorder: a descriptive study. PLoS ONE 4, e6481.CrossRefGoogle Scholar
Van Engelsdorp, D., Hayes, J., Underwood, R. and Pettis, J. (2010). A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. Journal of Apicultural Research 49, 14.Google Scholar
Van Engelsdorp, D., Hayes, J., Underwood, R. M., Caron, D. and Pettis, J. S. (2011). A survey of honey bee colony losses in the United States, fall 2009 to spring 2010. Journal of Apicultural Research 50, 1–10.CrossRefGoogle Scholar
Van Engelsdorp, D., Caron, D., Hayes, J., Underwood, R., Henson, K. R. M., Spleen, A., Andree, M., Snyder, R., Lee, K., Roccasecca, K., Wilson, M., Wilkes, J., Lengerich, E. and Pettis, J. (2012). A national survey of managed honey bee 2010–11 winter colony losses in the USA: results from the Bee Informed Partnership. Journal of Apicultural Research 51, 115–124.CrossRefGoogle Scholar
Weinberg, K. P.aM, G. (1985). The influence of the mite Varroa jacobsoni Oud. on the protein concentration and hemolymph volume of the blood of the worker bees and drones of the honey bee, Apis mellifera . Apidologie 16, 421–436.CrossRefGoogle Scholar
Yang, X. and Cox-Foster, D. L. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences of the United States of America 102, 7470–7475.CrossRefGoogle ScholarPubMed