journal article·2022-11-16Open access

Effects of Varroa destructor on Hemolymph Sugars and Secondary Infections in Honeybees (Apis mellifera)

Antoine Cournoyer, Laurence Plamondon, Liza Bau-Gaudreault, Annie Deschamps, Pascal Dubreuil, Marie-Odile Benoit-Biancamano

Applied Sciences· Volume 12· Issue 22

Abstract

The European honeybee contributes to the agriculture by its pollination; however, the overwintering loss rate over the last decades is worrisome. Varroa destructor is considered one of the most important causes of bee colony declines. This project aims to correlate the infestation by varroa to the hemolymph sugar concentrations and bacterial and viral coinfections. Six highly infested and six control hives were compared over time. Pooled hemolymph samples from honeybees were collected for sugar concentration measurements using a previously validated portable glucometer. The hemolymph samples were submitted for bacteriology. Multiplex RT-PCR analysis was performed on honeybees for six viruses: DWV-A, DWV-B, BQCV, ABPV, KBV, and IAPV. There was also no predominance of pathogenic bacteria. In September, sugar concentrations in hemolymph were significantly lower in highly infested hives than in control hives. Infested hives showed markedly higher viral loads except for ABPV. DWV-A and BQCV viral loads from highly infested hives were significantly higher in September compared to July. A continued and severe exposure to varroa leads to increased viral charges and decreased sugar concentrations, suggesting alterations in immunity, metabolism, and reserve mobilization. These parameters contribute to the weakening and mortality of the colonies.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Insect and Pesticide Research · Plant and animal studies · Insect and Arachnid Ecology and Behavior

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Groupe de Recherche sur les Maladies Infectieuses en Production Animale (GREMIP), Faculté de Médecine Vétérinaire, Saint-Hyacinthe, QC J2S 2M2, Canada

Centre de Diagnostic Vétérinaire de l’Université de Montréal, Département de Pathologie et Microbiologie, Faculté de Médecine Vétérinaire, Saint-Hyacinthe, QC J2S 2M2, Canada

Département de Biologie, Université Laval, Québec, QC G1V 0A6, Canada

Charles River Laboratories, Senneville, Québec, QC H9X 1C1, Canada

Funding

Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (MAPAQ)

References (87)

Show source-provided references
1. The honey bee (Apis mellifera L., 1758) and the seasonal adaptation of productions. Highlights on summer to winter transition and back to summer metabolic activity. A review10.1016/j.livsci.2020.104011 ↗
2. Kane, T., and Faux, C. (2021). Physiology of the Honey Bee—Principles for the Beekeeper and Veterinarian. Honey Bee Medicine for the Veterinary Practitioner, John Wiley & Sons Inc.10.1002/9781119583417 ↗
3. Timing of production of winter bees in honey bee (Apis mellifera) colonies10.1007/PL00001764 ↗
4. Winston, M.L. (1987). The Biology of the Honey Bee, Harvard University Press.
5. Kane, T., and Faux, C. (2021). The Superorganism and Herd Health for the Honey Bee. Honey Bee Medicine for the Veterinary Practitioner, John Wiley & Sons Inc.10.1002/9781119583417 ↗
6. Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone, protein and vitellogenin in worker honey bees10.1016/0022-1910(82)90023-3 ↗
7. Overwintering honey bees: Biology and management10.1016/j.cois.2015.05.014 ↗
8. Fluri, P., and Bogdanov, S. (1986, January 18–22). Age dependence of fat body protein in summer and winter bees. Proceedings of the 10th International Congress of IUSSI, München, Germany.
9. Differences in drone and worker physiology in honeybees (Apis mellifera)10.1051/apido:2005015 ↗
10. Thermoregulation in Bees
11. Honey bee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018–2019, and the effects of a new queen on the risk of colony winter loss10.1080/00218839.2020.1797272 ↗
12. Ferland, J., Kempers, M., Kozak, P., Lafrenière, R., Maund, C., Menzies, C., Mesher, C., Muirhead, S., Pernal, S., and Sproule, J. (2022). Canadian Association of Professional Apiculturists Statement on Honey Bee Wintering Losses in Canada (2022), Canadian Association of Professional Apiculturists National Survey Committee and Provincial Apiarists.
13. Ferland, J., Kempers, M., Kennedy, K., Kozak, P., Lafrenière, R., Maund, C., Menzies, C., Muirhead, S., Nasr, M., and Pernal, S. (2019). Canadian Association of Professional Apiculturists Statement on Honey Bee Wintering Losses in Canada (2019), Canadian Association of Professional Apiculturists National Survey Committee and Provincial Apiarists.
14. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering?10.1603/0022-0493(2004)097[0741:APIWHB]2.0.CO;2 ↗
15. Kane, T., and Faux, C. (2021). The Parasitic Mite Varroa destructor. Honey Bee Medicine for the Veterinary Practitioner, John Wiley & Sons Inc.10.1002/9781119583417 ↗
16. Varroa destructor: How does it harm Apis mellifera honey bees and what can be done about it?10.1042/ETLS20190125 ↗
17. Mondet, F., de Miranda, J.R., Kretzschmar, A., Le Conte, Y., and Mercer, A.R. (2014). On the front line: Quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathog., 10.10.1371/journal.ppat.1004323 ↗
18. Vidal-Naquet, N., Lewbart, G., and Vallat, B. (2015). Honeybee Veterinary Medicine: Apis Mellifera, 5M Publishing. [1st ed.].
19. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph10.1073/pnas.1818371116 ↗
20. Insect fat body: Energy, metabolism, and regulation10.1146/annurev-ento-112408-085356 ↗
21. Fat Body Biology in the Last Decade10.1146/annurev-ento-011118-112007 ↗
22. Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers10.1016/j.jinsphys.2010.05.016 ↗
23. General stress responses in the honey bee10.3390/insects3041271 ↗
24. Quantitative variation in the core bacterial community associated with honey bees from Varroa-infested colonies10.1080/00218839.2019.1589669 ↗
25. Varroa destructor induces changes in the expression of immunity-related genes during the development of Apis mellifera worker and drone broods10.1515/ap-2017-0094 ↗
26. Varroa destructor parasitism reduces hemocyte concentrations and prophenol oxidase gene expression in bees from two populations10.1007/s00436-018-5796-8 ↗
27. Pathogenicity of Serratia marcescens Strains in Honey Bees10.1128/mBio.01649-18 ↗
28. Burritt, N.L., Foss, N.J., Neeno-Eckwall, E.C., Church, J.O., Hilger, A.M., Hildebrand, J.A., Warshauer, D.M., Perna, N.T., and Burritt, J.B. (2016). Sepsis and Hemocyte Loss in Honey Bees (Apis mellifera) Infected with Serratia marcescens Strain Sicaria. PLoS ONE, 11.10.1371/journal.pone.0167752 ↗
29. Borsuk, G., Ptaszynska, A.A., Olszewski, K., Domaciuk, M., Krutmuang, P., and Paleolog, J. (2017). A New Method for Quick and Easy Hemolymph Collection from Apidae Adults. PLoS ONE, 12.10.1371/journal.pone.0170487 ↗
30. The phenylthiourea is a competitive inhibitor of the enzymatic oxidation of DOPA by phenoloxidase10.3109/14756366.2011.576010 ↗
31. Analytical validation of a portable human Accu-Chek glucometer in honeybee hemolymph10.1177/10406387221117233 ↗
32. Timing acaricide treatments to prevent Varroa destructor (Acari: Varroidae) from causing economic damage to honey bee colonies10.4039/n05-024 ↗
33. Effect of activity on the haemolymph sugar titres in honey bees10.1080/00218839.1997.11100928 ↗
34. The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels10.1046/j.1570-7458.2001.00905.x ↗
35. Heatley, J.J., and Russell, K.E. (2020). Terrestrial Invertebrates. Exotic Animal Laboratory Diagnosis, John Wiley & Sons, Inc.10.1002/9781119108610 ↗
36. Gas chromatography—Mass spectrometry as a preferred method for quantification of insect hemolymph sugars10.1016/j.jinsphys.2020.104115 ↗
37. Corby-Harris, V., Maes, P., and Anderson, K.E. (2014). The Bacterial Communities Associated with Honey Bee (Apis mellifera) Foragers. PLoS ONE, 9.10.1371/journal.pone.0095056 ↗
38. Gut microbiota structure differs between honeybees in winter and summer10.1038/s41396-019-0568-8 ↗
39. Gut microbial communities of social bees10.1038/nrmicro.2016.43 ↗
40. Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner10.1038/s41598-019-47447-3 ↗
41. Kane, T., and Faux, C. (2021). Epidemiology and Biosecurity. Honey Bee Medicine for the Veterinary Practitioner, John Wiley & Sons Inc.10.1002/9781119583417 ↗
42. Bee Viruses: Ecology, Pathogenicity, and Impacts10.1146/annurev-ento-011118-111942 ↗
43. Francis, R.M., Nielsen, S.L., and Kryger, P. (2013). Varroa-virus interaction in collapsing honey bee colonies. PLoS ONE, 8.10.1371/journal.pone.0057540 ↗
44. The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex10.1016/j.jip.2009.06.014 ↗
45. Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera) colonies infested with Varroa destructor10.1051/apido:2007021 ↗
46. Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique10.1051/apido:2007026 ↗
47. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France10.1128/AEM.70.12.7185-7191.2004 ↗
48. Ribière, M., Ball, B., and Aubert, M. (2008). Natural history and geographical distribution of honey bee viruses. Virology and the Honey Bee, European Communities.
49. Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge10.1017/S0031182006000710 ↗
50. Dead or alive: Deformed wing virus and Varroa destructor reduce the life span of winter honeybees10.1128/AEM.06537-11 ↗
51. The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies10.1051/apido/2010014 ↗
52. Kane, T., and Faux, C. (2021). Honey Bee Viral Diseases. Honey Bee Medicine for the Veterinary Practitioner, John Wiley & Sons Inc.10.1002/9781119583417 ↗
53. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera10.1099/vir.0.023853-0 ↗
54. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite10.1099/vir.0.80824-0 ↗
55. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees10.1016/j.virol.2005.07.012 ↗
56. Wiegers, F. (1988). Transmission of honeybee viruses by Varroa jacobsoni Oud. European Research on Varroatosis Control, CRC Press.
57. Prevalence and transmission of honeybee viruses10.1128/AEM.72.1.606-611.2006 ↗
58. Immunolocalization of deformed wing virus particles within the mite Varroa destructor10.1099/vir.0.83223-0 ↗
59. Tehel, A., Quynh, V., Bigot, D., Gogol-Döring, A., Koch, P., Jenkins, C., Doublet, V., Theodorou, P., and Paxton, R. (2019). The two prevalent genotypes of an emerging infectious disease, Deformed wing virus, cause equally low pupal mortality and equally high wing deformities in host honey bees. Viruses, 11.10.3390/v11020114 ↗
60. Elevated virulence of an emerging viral genotype as a driver of honeybee loss10.1098/rspb.2016.0811 ↗
61. Association of viruses with two protozoal pathogens of the honey bee10.1111/j.1744-7348.1983.tb02735.x ↗
62. Two viruses from adult honey bees (Apis mellifera Linnaeus)10.1016/0042-6822(63)90200-9 ↗
63. Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: Evidence for diversity due to intra- and inter-species recombination10.1099/vir.0.83284-0 ↗
64. Kane, T., and Faux, C. (2021). Wild Bees: Diversity, Ecology, and Stressors of Non-Apis Bees. Honey Bee Medicine for the Veterinary Practitioner, John Wiley & Sons Inc.10.1002/9781119583417 ↗
65. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud10.1006/jipa.1998.4807 ↗
66. Viral communities in the parasite Varroa destructor and in colonies of their honey bee host (Apis mellifera) in New Zealand10.1038/s41598-022-12888-w ↗
67. Nazzi, F., and Pennacchio, F. (2018). Honey Bee Antiviral Immune Barriers as Affected by Multiple Stress Factors: A Novel Paradigm to Interpret Colony Health Decline and Collapse. Viruses, 10.10.3390/v10040159 ↗
68. Does pollen diversity influence honey bee colony health?10.5424/sjar/2019173-13991 ↗
69. Ryabov, E.V., Wood, G.R., Fannon, J.M., Moore, J.D., Bull, J.C., Chandler, D., Mead, A., Burroughs, N., and Evans, D.J. (2014). A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathog., 10.10.1371/journal.ppat.1004230 ↗
70. Global honey bee viral landscape altered by a parasitic mite10.1126/science.1220941 ↗
71. RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor)10.1099/vir.0.81401-0 ↗
72. Deformed wing virus: Replication and viral load in mites (Varroa destructor)10.1099/vir.0.005579-0 ↗
73. Epidemiology of a major honey bee pathogen, deformed wing virus: Potential worldwide replacement of genotype A by genotype B10.1016/j.ijppaw.2022.04.013 ↗
74. High Load of Deformed Wing Virus and Varroa destructor Infestation Are Related to Weakness of Honey Bee Colonies in Southern Spain10.3389/fmicb.2019.01331 ↗
75. Development of a real-time RT-PCR assay with TaqMan probe for specific detection of acute bee paralysis virus10.1016/j.jviromet.2012.05.010 ↗
76. Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control10.1128/AEM.06094-11 ↗
77. A sting in the spit: Widespread cross-infection of multiple RNA viruses across wild and managed bees10.1111/1365-2656.12345 ↗
78. A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary10.1016/j.jip.2005.11.001 ↗
79. First detection of Kashmir bee virus in the UK using real-time PCR10.1051/apido:2006072 ↗
80. Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.)10.1128/AEM.71.1.436-441.2005 ↗
81. In-depth proteomic analysis of Varroa destructor: Detection of DWV-complex, ABPV, VdMLV and honeybee proteins in the mite10.1038/srep13907 ↗
82. Distribution of deformed wing virus within honey bee (Apis mellifera) brood cells infested with the ectoparasitic mite Varroa destructor10.1023/A:1025853731214 ↗
83. Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra’s model10.1098/rspb.2019.0331 ↗
84. Direct Evidence for Infection of Varroa destructor Mites with the Bee-Pathogenic Deformed Wing Virus Variant B—But Not Variant A—Via Fluorescence-in situ-Hybridization Analysis10.1128/JVI.01786-20 ↗
85. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor10.1099/vir.0.80470-0 ↗
86. Association of Varroa jacobsoni with virus diseases of honey bees
87. Honey bee colony losses and associated viruses10.1016/j.cois.2015.01.015 ↗