Bee Stressors from an Immunological Perspective and Strategies to Improve Bee Health
Abstract
:1. Introduction
2. Honeybee Immunity
3. Main Causes of Honeybee Colony Losses
3.1. Varroa Mite
3.2. Nosema spp.
3.3. Viral Pathogens
3.4. Pesticides
3.5. Malnutrition
3.6. Other Causes
4. Interaction between Different Stressors Affects the Bees Immunocompetence
4.1. Interaction between Pesticides and Pathogens
4.2. Interaction between Pesticides and Poor Nutrition
4.3. Interaction between Pathogens and Poor Nutrition
4.4. Interaction between Parasites and Pathogens
First Stressor | Second Stressor | Model | Results | References |
---|---|---|---|---|
Varroa destructor | Neonicotinoid insecticides | Honeybees | Reduction in survival of long-lived winter honeybees | [115] |
Deformed wing virus (DWV) | White-eye honeybees pupae | Higher virus replication | [116] | |
Poor nutrition | Freshly emerged honeybee workers | Reduction in body weight Reduction in abdominal protein level Increased head to abdomen protein ratio | [117] | |
Nosema ceranae | Insecticide fipronil | Emerging honeybees | Decreased survival | [118] |
DWV | Newly emerged honeybee workers | Higher virus replication in infected bees in a dose- and nutrition-dependent manner | [119] | |
Neurotoxic insecticides | Emerging honeybees | Increased mortality of immunity-related genes Strong alteration of midgut immunity | [104] | |
Thiacloprid | Freshly emerged honeybee workers | Higher Nosema replication | [105] | |
Microsporidia Nosema | Neonicotinoid (imidacloprid) | Young Africanized honeybees | Higher mortality rate Higher pathogen load | [120] |
Thiamethoxam | N. ceranae | Larvae and adult honeybees | Gene expression patterns change with time in each treatment | [121] |
Chronic bee paralysis virus (CBPV) | Nine-day-old bees | Higher viral titers Increased mortality | [122] | |
CBPV | Emerging honeybees | High pesticides increased mortality without an increase in viral titers Low pesticide has no effect on mortality, however, increases in viral titers | [123] | |
Imidacloprid | N. ceranae | Honeybee queens | Decreased metabolic and detoxification functions Increased mortality Reduced lifespan | [103] |
N. ceranae | Honeybees | Higher Nosema infection load Increased mortality of honey bee colonies | [101] | |
Thiacloprid | Microsporidian N. ceranae and BQCV | Larval and adult honeybees | Elevation of viral load Increased individual mortality | [124] |
Clothianidin | Nosema spp. | Emerging honeybees | No any synergistic effect | [125] |
Fipronil and Thiacloprid | N. ceranae | Emerging honeybees | Higher Nosema infection Higher mortality | [126] |
Poor nutrition | Israeli acute paralysis virus (IAPV). | Honeybees | Elevation of bee mortality | [113] |
First Stressor | Second Stressor | Model | Results | References |
---|---|---|---|---|
Varroa destructor | Clothianidin | Honeybees | Reduced weight and number Up-regulated differentially expressed genes (DEGs) associated with metabolism | [127] |
Deformed wing virus (DWV) | Africanized honeybees | Inhibition of immunity Reduction in lifespan | [128] | |
Neonicotinoid insecticide imidacloprid | Honeybees | Reduce homing success of foragers High V. destructor load | [129] | |
Poor nutrition | Freshly emerged honeybee workers | Death of bee about 40% Ageing enhancement | [117] | |
Viruses (Acute-Kashmir-Israeli and DWV, acaricide) | Honeybees | Higher virus replication immune-suppression | [130] | |
DWV | Honeybees | Down-regulation of a member of the NF-Κβ Increase in bees mortality | [41] | |
Nosema | Herbicide glyphosate and the fungicide difenoconazole | Emerging honeybees | Induces strong physiological disturbances Reduced honeybees longevity | [131] |
Nosema apis | Neonicotinoid pesticide Thiamethoxam | Honeybee workers | Increase in mortality Reduction in immunocompetence | [132] |
V. destructor, Nosema spp. | Imidacloprid | Honeybees | Reduced the flight performance by ~24% No effect on colony size | [133] |
Acaricides | N. ceranae | Newly emerged honeybees | Reduction in ethyl oleate as primer pheromone | [134] |
Parasites | Pesticides | Honeybees | Increased mortality | [135] |
Imidacloprid | CBPV | Adult honeybee workers | Higher virus load and mortality in case of higher doses Lower dosages had no influence on virus titer | [106] |
Clothianidin | Varroa | Honeybees | No elevation of immune gene expression | [74] |
DWV | Honeybees | Decreased immunocompetence expression Higher replication of the DWV | [102] | |
Pathogens (RNA viruses, DNA virus, Nosema SP, and beneficial bacteria) | Bumblebees | No increase in viral titers Impairs reproduction of queens and males | [136] | |
Pathogens | Honeybees | No adverse effect on honey bee colonies No increase in pathogens titers | [137] | |
Infection with parasites and diseases | Honeybees | No increase in titers of several viruses No impact on success of colony or honey yield | [138] | |
RoundupVR | Nosema microsporidia | Emerged and adult honeybees | Reduced survival rate and increased food consumption of the bees | [139] |
Thiamethoxam | N. ceranae | Apis mellifera carnica | Epithelium degeneration Higher mortality | [140] |
N. ceranae | Larvae and adult honeybees | Highest mortality rate Decreased immunocompetence expression | [121] | |
DWV | Newly emerged bees | The chance of not returning to the hive after the first flight was raised Decreased survival | [141] | |
Chronic bee paralysis virus (CBPV) | Emerging honeybees | High pesticides increased mortality without an increase in viral titers Low pesticide has no effect on mortality but increases in viral titers | [123] | |
CBPV | Adult honeybee workers | Higher viral titers Increased mortality | [122] | |
Neonicotinoid insecticides | V. destructor | Newly emerged bees | Decreased immunocompetence expression | [142] |
Insecticide Flupyradifurone (FPF, Sivanto®) | Nutritional stress | Foraging honeybees | Reduced bee survival and food consumption | [110] |
Pesticides (fipronil, thiamethoxam and boscalid) | N. ceranae | Newly emerged honeybees | Gut microbiota dysbiosis | [143] |
Neonicotinoid pesticides | Nutritional stress | Honeybees | Reduction in bee survival Reduction in food consumption | [107] |
Pesticides (dimethoate, clothianidin and fluvalinate) | American foulbrood (AFB) | Honeybees | Higher mortality Reduction in hemocyte counts | [144] |
Poor nutrition | Virus infection | Honeybees | Elevation of bee mortality | [113] |
Thiamethoxam | Bumblebees micro-colonies | Slower growth Reduced reproductive efforts | [145] | |
Thiamethoxam | Apis mellifera ligustica | Negative impact on hypopharyngeal gland development | [146] |
5. Strategies to Enhance Honeybee Immunity
5.1. Fortified Nutrients
5.2. Natural Products as Alternative Sources
5.3. Nanomaterials as Novel Alternative Approaches
5.4. Organizations and Initiatives Directed to Saving the Bees
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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El-Seedi, H.R.; Ahmed, H.R.; El-Wahed, A.A.A.; Saeed, A.; Algethami, A.F.; Attia, N.F.; Guo, Z.; Musharraf, S.G.; Khatib, A.; Alsharif, S.M.; et al. Bee Stressors from an Immunological Perspective and Strategies to Improve Bee Health. Vet. Sci. 2022, 9, 199. https://doi.org/10.3390/vetsci9050199
El-Seedi HR, Ahmed HR, El-Wahed AAA, Saeed A, Algethami AF, Attia NF, Guo Z, Musharraf SG, Khatib A, Alsharif SM, et al. Bee Stressors from an Immunological Perspective and Strategies to Improve Bee Health. Veterinary Sciences. 2022; 9(5):199. https://doi.org/10.3390/vetsci9050199
Chicago/Turabian StyleEl-Seedi, Hesham R., Hanan R. Ahmed, Aida A. Abd El-Wahed, Aamer Saeed, Ahmed F. Algethami, Nour F. Attia, Zhiming Guo, Syed G. Musharraf, Alfi Khatib, Sultan M. Alsharif, and et al. 2022. "Bee Stressors from an Immunological Perspective and Strategies to Improve Bee Health" Veterinary Sciences 9, no. 5: 199. https://doi.org/10.3390/vetsci9050199
APA StyleEl-Seedi, H. R., Ahmed, H. R., El-Wahed, A. A. A., Saeed, A., Algethami, A. F., Attia, N. F., Guo, Z., Musharraf, S. G., Khatib, A., Alsharif, S. M., Naggar, Y. A., Khalifa, S. A. M., & Wang, K. (2022). Bee Stressors from an Immunological Perspective and Strategies to Improve Bee Health. Veterinary Sciences, 9(5), 199. https://doi.org/10.3390/vetsci9050199