Eggs Sampling As an Effective Tool for Identifying the Incidence of Viruses in Honey Bees Involved in Artificial Queen Rearing

Overview

Journal Sci Rep

Specialty Science

Date 2024 Apr 26

PMID 38671077

Authors

Caio E C Domingues

Laura Simenc

Ivan Toplak

Dirk C de Graaf

Lina De Smet

Wim Verbeke

Luc Peelman

Leticia S Ansaloni

Ales Gregorc

Affiliations

Soon will be listed here.

Abstract

The Carniolan honey bee (Apis mellifera carnica) plays an essential role in crop pollination, environment diversity, and the production of honey bee products. However, the health of individual honey bees and their colonies is under pressure due to multiple stressors, including viruses as a significant threat to bees. Monitoring various virus infections could be a crucial selection tool during queen rearing. In the present study, samples from all developmental stages (eggs, larvae, pupae, and queens) were screened for the incidence of seven viruses during queen rearing in Slovenia. The screening of a total of 108 samples from five queen breeders was performed by the RT-qPCR assays. The results showed that the highest incidence was observed for black queen cell virus (BQCV), Lake Sinai virus 3 (LSV3), deformed wing virus B (DWV-B), and sacbrood virus (SBV). The highest viral load was detected in queens (6.07 log copies/queen) and larvae (5.50 log copies/larva) for BQCV, followed by SBV in larvae (5.47 log copies/larva). When comparing all the honey bee developmental stages, the eggs exhibited general screening for virus incidence and load in queen mother colonies. The results suggest that analyzing eggs is a good indicator of resilience to virus infection during queen development.

Citing Articles

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Ansaloni L, Kristl J, Domingues C, Gregorc A Insects. 2025; 16(1).

PMID: 39859678 PMC: 11766133. DOI: 10.3390/insects16010097.

References

Klein S, Cabirol A, Devaud J, Barron A, Lihoreau M . Why Bees Are So Vulnerable to Environmental Stressors. Trends Ecol Evol. 2017; 32(4):268-278. DOI: 10.1016/j.tree.2016.12.009. View

Gonzalez-Varo J, Biesmeijer J, Bommarco R, Potts S, Schweiger O, Smith H . Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol. 2013; 28(9):524-30. DOI: 10.1016/j.tree.2013.05.008. View

Chen Y, Pettis J, Collins A, Feldlaufer M . Prevalence and transmission of honeybee viruses. Appl Environ Microbiol. 2006; 72(1):606-11. PMC: 1352288. DOI: 10.1128/AEM.72.1.606-611.2006. View

Beaurepaire A, Piot N, Doublet V, Antunez K, Campbell E, Chantawannakul P . Diversity and Global Distribution of Viruses of the Western Honey Bee, . Insects. 2020; 11(4). PMC: 7240362. DOI: 10.3390/insects11040239. View

Chen Y, Pettis J, Feldlaufer M . Detection of multiple viruses in queens of the honey bee Apis mellifera L. J Invertebr Pathol. 2005; 90(2):118-21. DOI: 10.1016/j.jip.2005.08.005. View

McMenamin A, Genersch E . Honey bee colony losses and associated viruses. Curr Opin Insect Sci. 2020; 8:121-129. DOI: 10.1016/j.cois.2015.01.015. View

Chen Y, Siede R . Honey bee viruses. Adv Virus Res. 2007; 70:33-80. DOI: 10.1016/S0065-3527(07)70002-7. View

Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T, Nomoto A . Novel insect picorna-like virus identified in the brains of aggressive worker honeybees. J Virol. 2004; 78(3):1093-100. PMC: 321398. DOI: 10.1128/jvi.78.3.1093-1100.2004. View

de Miranda J, Drebot M, Tyler S, Shen M, Cameron C, Stoltz D . Complete nucleotide sequence of Kashmir bee virus and comparison with acute bee paralysis virus. J Gen Virol. 2004; 85(Pt 8):2263-2270. DOI: 10.1099/vir.0.79990-0. View

10.

Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O . 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. 2007; 88(Pt 12):3428-3438. DOI: 10.1099/vir.0.83284-0. View

11.

Blanchard P, Schurr F, Olivier V, Celle O, Antunez K, Bakonyi T . Phylogenetic analysis of the RNA-dependent RNA polymerase (RdRp) and a predicted structural protein (pSP) of the Chronic bee paralysis virus (CBPV) isolated from various geographic regions. Virus Res. 2009; 144(1-2):334-8. DOI: 10.1016/j.virusres.2009.04.025. View

12.

Simenc L, Kuhar U, Jamnikar-Ciglenecki U, Toplak I . First Complete Genome of Lake Sinai Virus Lineage 3 and Genetic Diversity of Lake Sinai Virus Strains From Honey Bees and Bumble Bees. J Econ Entomol. 2020; 113(3):1055-1061. DOI: 10.1093/jee/toaa049. View

13.

Brutscher L, McMenamin A, Flenniken M . The Buzz about Honey Bee Viruses. PLoS Pathog. 2016; 12(8):e1005757. PMC: 4990335. DOI: 10.1371/journal.ppat.1005757. View

14.

Simenc L, Knific T, Toplak I . The Comparison of Honeybee Viral Loads for Six Honeybee Viruses (ABPV, BQCV, CBPV, DWV, LSV3 and SBV) in Healthy and Clinically Affected Honeybees with TaqMan Quantitative Real-Time RT-PCR Assays. Viruses. 2021; 13(7). PMC: 8310196. DOI: 10.3390/v13071340. View

15.

Grabensteiner E, Ritter W, Carter M, Davison S, Pechhacker H, Kolodziejek J . Sacbrood virus of the honeybee (Apis mellifera): rapid identification and phylogenetic analysis using reverse transcription-PCR. Clin Diagn Lab Immunol. 2001; 8(1):93-104. PMC: 96016. DOI: 10.1128/CDLI.8.1.93-104.2001. View

16.

Ribiere M, Olivier V, Blanchard P . Chronic bee paralysis: a disease and a virus like no other?. J Invertebr Pathol. 2009; 103 Suppl 1:S120-31. DOI: 10.1016/j.jip.2009.06.013. View

17.

Budge G, Simcock N, Holder P, Shirley M, Brown M, Van Weymers P . Chronic bee paralysis as a serious emerging threat to honey bees. Nat Commun. 2020; 11(1):2164. PMC: 7195492. DOI: 10.1038/s41467-020-15919-0. View

18.

Porrini C, Mutinelli F, Bortolotti L, Granato A, Laurenson L, Roberts K . The Status of Honey Bee Health in Italy: Results from the Nationwide Bee Monitoring Network. PLoS One. 2016; 11(5):e0155411. PMC: 4868308. DOI: 10.1371/journal.pone.0155411. View

19.

Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F, Colin M . Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol. 2004; 70(12):7185-91. PMC: 535170. DOI: 10.1128/AEM.70.12.7185-7191.2004. View

21.

Amiri E, Strand M, Tarpy D, Rueppell O . Honey Bee Queens and Virus Infections. Viruses. 2020; 12(3). PMC: 7150968. DOI: 10.3390/v12030322. View