You're using an outdated browser. Please upgrade to a modern browser for the best experience.
Effect of Stressors on Honeybee Immunity: History
View Latest Version
Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor: Hesham El-Seedi ,
, Aida Abd El-Wahed , Aamer Saeed , Nour F. Attia , Zhiming Guo , Syed Ghulam Musharra , Alfi Khatib , Sultan M. Alsharif , Yahya Al Naggar , Shaden Khalifa , Kai Wang

Honeybees are the most prevalent insect pollinator species; they pollinate a wide range of crops. Colony collapse disorder (CCD), which is caused by a variety of biotic and abiotic factors, incurs high economic/ecological loss. Various ecological stressors are microbial infections, exposure to pesticides, loss of habitat, and improper beekeeping practices that are claimed to cause these declines. Honeybees have an innate immune system, which includes physical barriers and cellular and humeral responses to defend against pathogens and parasites. Exposure to various stressors may affect this system and the health of individual bees and colonies.

  • honeybees
  • immunity
  • ecological stressors
  • sustainable beekeeping

1. Introduction

The European honeybees (Apis mellifera L.) is considered one of the most important agricultural pollinators worldwide. They play a key role in food productivity by pollinating various plants [1][2]. One-third of a person’s diet comes from insect-pollinated plants, and honeybees are responsible for the pollination of over 80% of flowering plants. Without honeybees pollination, crop yields would decrease by >90% [3]. Therefore, there is major international concern related to bee colony loss [4][5].
Colony collapse disorder (CCD), which first emerged in the US in 2006, caused huge colony losses and posed challenges for crop pollination, which is the major service of the apicultural industry in North America [6]. The observed losses between 1961 and 2007 recorded in Europe and North America were 26.5% and 49.5%, respectively. Honeybee colonies have increased, primarily in Asia (426%), Africa (130%), South America (86%), and Oceania (39%) [7]. The following factors have been implicated in honeybee losses in different parts of the world: honeybee diseases, parasites, in-hive chemical substances, agrochemicals, genetically modified (GM) plants, modified land-use, changed and alteration in the cultural practices, beekeeping practices, as well as the climate change [8][9][10][11][12][13].

2. Honeybee Immunity

The widespread agreement on the multifactorial origins of colony collapse and its frequent correlation with high pathogen and parasite loads indicate that the immune system is the most targeted, and its activity can be altered by a variety of stressors [14]. Bees have an innate immune system, which includes physical barriers, cellular, and humoral responses to defend against pathogens and parasites. The physical barrier includes an exoskeleton cuticle and the peritrophic membranes lining the digestive tract to prevent the entry of pathogenic organisms into the body cavity [15]. The recognition of pathogen-associated molecular patterns by recognition receptors triggers the innate immune system [16]. As a result, hemocytes that represent the primary mediators of cellular immunity will be activated, including phagocytosis, nodule formation, encapsulation, as well as the initiation of phenol-oxidase that regulates coagulation or melanization, or the synthesis of antimicrobial peptides (AMP), such as abaecin, apidaecin, hymenoptaecin, and defensin [17]. The immune system of honeybees possesses orthologues for the major members of immune pathways comprising the following: Toll (transmembrane signal transduction pathway), immune deficiency (Imd), Jun-N-terminal kinase, and JAK/STAT (Janus kinase/signal transducers and activators of transcription). RNA interference (RNAi), known as RNA silencing, is an important antiviral defense mechanism in insects, including honeybees. The efficacy of RNAi-mediated treatment against honeybee viruses and the fact that honeybee viruses encode for putative virus-encoded suppressors of RNAi shows that RNAi is an important honeybee antiviral defense mechanism [9][18]. In addition, several studies implicate the involvement of innate immune pathways (Jak-STAT, Toll, and Imd) and non-sequence-specific dsRNA-mediated antiviral defense as part of the immune responses in honeybee [19].
Bees are creatures that exhibit social immunity to prevent parasite infection from spreading among colony members. Honeybee workers use hygienic practices to remove diseased brood [20]. Furthermore, social fever develops when bees cooperate to raise the temperature within the colony to resist the heat-sensitive fungal disease Ascosphaera apis, known as chalkbrood disease [21]. Grooming, which is the physical removal of parasitic mites from the bodies of adult bees by individual workers or their nest-mates, is one of the most important defense modes against the ectoparasitic mite Varroa destructor [22]. Other mechanisms of social immunity such as propolis collection is used for nest constriction. It helps in declining investment in the immune response of 7-day-old bees and enriches the health and productivity of the colony [23]. Previous study showed that a propolis envelope reduced the clinical symptoms of American foulbrood (AFB) two months after the challenge, compared with those of colonies without a propolis envelope. Additionally, it protected the brood from pathogenic infection [24]. Glucose oxidase (GOX) is an antiseptic enzyme found in nectar and larval diet, and an additive to prolong the products’ shelf life. In the hypopharyngeal glands, GOX is a catalytic enzyme that catalyzes the conversion of β- d- glucose to gluconic acid and hydrogen peroxide (H2O2) [25] and provides the social immunity. H2O2 functions as an antiseptic, preventing pathogen growth in honeybee larval diet [26].

3. Main Causes of Honeybee Colony Losses

3.1. Varroa Mite

The ectoparasitic mite V. destructor is considered one of the most important factors behind the recent high annual loss of honeybee colonies. The mite directly damages bees by feeding primarily on honeybee fat body tissue and not hemolymph [27][28].
The physical damage caused by the mite has been reported to suppress the bees’ immune response [29]. Varroa parasitism has inhibited the expression of genes encoding immunity (hymenoptaecin and defensin), longevity, and stem cell proliferation in honeybees [30].
The mite is unlikely to cause the collapse of hives; however, it acts as a vector for a cocktail of viral disease agents, which are among the probable causes for CCD, including the deformed wing virus (DWV), kashmir bee virus, sacbrood virus (SBV), acute bee paralysis virus, and Israeli acute paralysis virus (IAPV) [31][32][33][34].

3.2. Nosema spp.

Nosemosis is a disease that affects honeybees and is caused by intracellular parasites (Nosema apis and Nosema ceranae) that infect the adults’ midgut epithelial cells [35]. N. ceranae infection is highly pathogenic for honeybee colonies, significantly reducing the colony size, brood rearing, and honey production, and increasing winter mortality. In persistent infections, the pathogen can impact colony performance by reducing a colony’s ability to regulate hive temperature or by killing the entire colony [36]. For the European honeybee, N. ceranae reduced homing and orientation skills, and altered the metabolism of forager bees [37].

3.3. Viral Pathogens

For honeybees worldwide, over 24 viruses have been discovered, some of which can have major health repercussions [38]. A highly prevalent and relatively virulent virus transmitted by V. destructor which impacts the health of honeybee colonies worldwide is DWV [10]. DWV-induced honeybee loss, coupled with a long-term decline in beekeeping, has become a serious threat to the adequate provision of pollination services, which threatens food security and ecosystem stability [39].

3.4. Pesticides

The exposure of honeybees to pesticides compromises their immune responses, navigation ability, learning, and memory [40]. Pesticides in sub-lethal quantities can be harmful to honeybees, as it may not kill bees but reduce their performance and survival during foraging. Bees exposed to pesticides had high vulnerability to infections and hence became means to spread diseases to other parts of the colony or other colonies via the shared use of flowers [8].

3.5. Malnutrition

Food resources are collected in large quantities by bee colonies to prepare for scarcity and are stored as honey and bee bread. This is because nutrition deficiency and deterioration can affect development and bee lifespan and increase the likelihood of infestation by a parasite, virus, or disease, resulting in honeybee mortality [41][42]. Bees fed only on water and sugar (low protein diet) exhibited higher mortality and viral load rates, compared with bees fed on higher pollen diets. These results showed that poor nutrition can suppress immunity and that a different host’s nutrition can alter specific components of the immune system [43]. Supplementary nutrition such as homemade sugar syrups can cause undesirable effects on bee health due to the presence of toxic compounds, such as hydroxylmethylfurfural (HMF). In addition, the preparation conditions of these sugar syrups such as temperature or addition of an acidifying substance resulted in a higher amount of HMF and bee mortality [44].

3.6. Other Causes

Heavy metal pollution originates from various sources. Heavy metals may be ingested by honeybees through water sources and by foraging for nectar and pollen from plants that have already stored heavy metals [45]. Cd, Pb, As, Hg, Ni, and Cr are particularly harmful to living beings due to their high toxicity. Furthermore, elements such as Cu, Fe, Se, Zn, Mn, and Co, which are required for a range of biochemical and physiological processes, can be hazardous to bee colonies [46].
Urbanization is one of the biggest challenges to wild plants and pollinators, including bees [47]. Heavy metals such as Pb and Cd are found in high concentrations in urban areas. In urban areas, bees were more susceptible to disease transmission, particularly the black queen cell virus (BQCV) and fungal pathogen N. ceranae. This effect did not appear to be mediated by immunity, as determined by immune-gene expression, which was not affected by urbanization [48]. Moreover, there was no evidence of immunocompetence differences between managed and feral bees [49].
Nanoparticles (NPs), which are used in a variety of industrial applications, negatively impact human and animal health, including honeybees. CdO or PbO NPs produced histological and cellular abnormalities in honeybee workers’ midgut epithelial cells [50]. When exposed to CdO or PbO NPs, separately or in combination, acetylcholinesterase (AChE) activity and the expression of a variety of stress-related detoxifying enzymes were inhibited. Furthermore, the rate of feeding and survival reduced [51].
The rapid expansion of the telecommunications industry has resulted in a massive increase in the number of mobile phones and the rapid deployment of cell towers across the globe. According to certain studies, honeybees do not rely on the electromagnetic field (EMF) to navigate, and many apiaries that are experiencing losses are in rural areas where cell phone service is absent. The World Health Organization confirmed the same data; however, some researchers revealed that there was standard evidence that the EMF could cause damage in honeybees [52][53]. It was associated with increased bees activity, increased inside temperature, increased queen loss, abnormal real cell production, weight loss, and reduced operculated brood [54]. Chronic radiofrequency EMF exposure significantly reduced the hatching of honeybee queens [55].

4. Interaction between Different Stressors Affects the Bees Immunocompetence

4.1. Interaction between Pesticides and Pathogens

Many factors including pesticides, diseases, and malnutrition lead to bees’ decline in different regions worldwide. These threats are frequently interconnected, and it is unlikely that colony losses are caused by single stressors (Figure 1) [56].
/media/item_content/202205/629423ec1878fvetsci-09-00199-g001.png
Figure 1. The impact on honeybees’ health when exposed to interaction between environmental and ecological stressors.
Interactions between pesticides and pathogens may play a role in increased honeybee colony losses, including CCD and other pollinator reductions worldwide [57]. CLO inhibits NF-κB immune signaling in insects at sub-lethal dosages, and CLO and imidacloprid compromise honeybees antiviral defenses regulated by transcription factors [58]. Although other studies estimated that increased pesticides may not always result in increased viral loads [10], exposure to neonicotinoid pesticide imidacloprid, in the presence of the gut parasite N. ceranae, increased the levels of enzymes such as catalase (CAT) and glutathione-S-transferase in the heads of bees. These enzymes are involved in pesticide and parasite resistance to xenobiotics and oxidative stress. Furthermore, stressors affected midgut enzymes, i.e., carboxylesterase alpha (CaE) and carboxylesterase para (CaE p), which are engaged in metabolic and detoxifying processes [57][59][60][61]. In honeybees, the interactions between thiacloprid and N. ceranae caused Nosema to increase, regardless of the thiacloprid dosage [61].

4.2. Interaction between Pesticides and Poor Nutrition

The combination of low diet and chemical exposure affects bee survival synergistically (−50%). The interaction reduced food consumption (−48%), hemolymph levels of glucose (−60%), and trehalose (−27%) [62]. Researchers have indicated that various insecticides indirectly influence honeybees’ health via diet by suppressing immunity-related genes and negatively altering NFB immunological signaling. It can significantly impair the honeybees’ immune system, reducing the bees antiviral defense regulated by this transcription factor. This may cause direct death or become easy prey to predators [58][63][64]. Bees survival was reduced as a result of the interaction of restricted nectar and nectar availability with neonicotinoid exposures, such as CLO and TMX [62].

4.3. Interaction between Pathogens and Poor Nutrition

Nutritional deficiencies increased pathogen load and reduced adult longevity and survival [65]. Diseases altered foraging behavior by reducing foraging abilities or altering floral preferences. In addition, pollination services were impaired when bee populations were reduced or feeding habits were altered [66]. The interaction between poor nutrition and pathogenic infection increased the rate of colony mortality and reduced the ability of bees to fight other stressors [67]. Disease infection (viral, fungal, and bacterial pathogens), reduced bee nutrition (caloric needs, dietary requirements, nutrient storage, gut physiology, and microbiota), and made bees more susceptible to diseases and vice versa [68].

4.4. Interaction between Parasites and Pathogens

The interactions between the DWV and ectoparasitic mite, V. destructor, resulted in DWV replication and increased Varroa reproductive output [69]. V. destructor can vector IAPV in honeybees and are capable of IAPV replication. The density of Varroa mites and the duration of exposure to the mites were positively related to the copy number of IAPV in bees. Furthermore, the mite–virus association may reduce the host immunity, promoting high levels of virus replication. Varroa mites provide a plausible route for IAPV transmission in the field and may significantly contribute to the honeybee diseases associated with CCD [27][70].

5. Strategies to Enhance Honeybee Immunity

5.1. Fortified Nutrients

Currently, honeybees face numerous threats that hinder their survival. Special attention should be paid to beekeepers, bee supplements, and nutrition to limit the risk of viruses, other diseases, and agrochemicals. Beekeepers should support colonies with suitable supplementary feeding during dearth periods [71]. In addition, the diversity of nutrition that comes from different natural plant sources can improve honeybee immunity, antiviral, and antimicrobial properties [68]. A diet with pollen from different plants or high-quality single pollen organs can enhance honeybees’ immunity and survival as shown in Figure 2.
/media/item_content/202205/62942410223e2vetsci-09-00199-g002.png
Figure 2. Factors that can improve honeybees immunity against different stressors.

5.2. Natural Products as Alternative Sources

Essential oils such as thymol, linalool, and camphor, as well as cocktails of thymol, eucalyptol, menthol, and others, have been confirmed to be particularly efficient in suppressing Varroa mites. These types of essential oils were discovered to lower mortality rates among bees in diseased colonies [72]. Although natural products therapy has fewer side effects than chemical therapy, the efficacy of these substances varies depending on the climate and colony condition [73].

Recently, Chinese herbal medicine has demonstrated a unique antiviral effect for both human and animal life. Honeybees are at risk from SBV and Chinese sacbrood virus (CSBV). Infected larvae will not develop into pupae and will eventually die, and there is currently no effective cure for the virus [19]. Radix isatidis, a Chinese herbal remedy, was primarily utilized to treat human influenza viruses. It has recently been proved to effectively regulate CSBV by suppressing its replication, increasing immunological response, and extending the lifespan of CSBV infection larvae, thereby lowering death rates and preventing CCD [74]. DWV and Lake Sinai virus are two RNA viruses with positive strands that kill honeybees. Bees fed with polypore mushroom extracts exhibited a strong ability to diminish both virus larvae. Modified porphyrins, which are mostly produced by living organisms, can reduce spore burdens in bees and increase the survival likelihood of bees infected with RNA viruses [75].

5.3. Nanomaterials as Novel Alternative Approaches

Nanotechnology is one of the most active areas in research that has proven to be extremely versatile and has sparked a revolution in medical treatments, fast diagnoses, cellular regeneration, and medication delivery [76][77]. It has been employed to discover novel therapies for honeybee diseases, as current antibiotics do not entirely eradicate the infection. Antibiotic use over time results in an accumulation of antibiotics in honey, which can be hazardous to human health [78].

5.4. Organizations and Initiatives Directed to Saving the Bees

Organizations and initiatives are directed to save the bees in response to honeybee colony losses. Working groups such as COLOSS, a COST initiative funded by the EU Science Foundation, have been formed to address the global loss of managed honeybee colonies. By offering strategies to reduce the risk of this problem, COLOSS is playing an important role in identifying and mitigating colony losses [79]. One of these strategies was adequate nutrition that was a key factor for honeybees’ growth and colony development.

6. Conclusions

Honeybees are important pollinators for humans and ecosystems. Unfortunately, CCD, a serious threat to the beekeeping industry, has recently been reported worldwide. It is caused by a variety of stressors that affect the immune system of bees, such as pathogens, insecticides, and inadequate diets. Scholars and governments have universally agreed that there is no single cause is to be blamed and that the causes are interconnected. However, further research is required to understand the mechanisms behind the interactions among different stressors and to discover more important genes and signaling pathways involved in honeybee stress responses. First, beekeepers must consider these aspects by planting floral-rich vegetation around the apiary and using proper dietary supplements. Second, experts could agree on a scientific plan for the treatment and management of the related diseases and pests, including the development of new nanotechnology-based remedies. Finally, organizations and stakeholders should pay attention to training to improve the efficiency of breeders and recent graduates in apiary management.

This entry is adapted from the peer-reviewed paper 10.3390/vetsci9050199

References

  1. Stein, K.; Coulibaly, D.; Stenchly, K.; Goetze, D.; Porembski, S.; Lindner, A.; Konaté, S.; Linsenmair, E.K. Bee pollination increases yield quantity and quality of cash crops in Burkina Faso, West Africa. Sci. Rep. 2017, 7, 17691–17700.
  2. Khalifa, S.A.M.; Elshafiey, E.H.; Shetaia, A.A.; El-Wahed, A.A.A.; Algethami, A.F.; Musharraf, S.G.; Alajmi, M.F.; Zhao, C.; Masry, S.H.D.; Abdel-Daim, M.M.; et al. Overview of bee pollination and its economic value for crop production. Insects 2021, 12, 688.
  3. Klein, A.M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 2007, 274, 303–313.
  4. Hristov, P.; Neov, B.; Shumkova, R.; Palova, N. Significance of apoidea as main pollinators. Ecological and economic impact and implications for human nutrition. Diversity 2020, 12, 280.
  5. Dicks, L.V.; Breeze, T.D.; Ngo, H.T.; Senapathi, D.; An, J.; Aizen, M.A.; Basu, P.; Buchori, D.; Galetto, L.; Garibaldi, L.A.; et al. A global-scale expert assessment of drivers and risks associated with pollinator decline. Nat. Ecol. Evol. 2021, 5, 1453–1461.
  6. VanEngelsdorp, D.; Traynor, K.S.; Andree, M.; Lichtenberg, E.M.; Chen, Y.; Saegerman, C.; Cox-Foster, D.L. Colony collapse disorder (CCD) and bee age impact honey bee pathophysiology. PLoS ONE 2017, 12, e0179535.
  7. van Engelsdorp, D.; Meixner, M.D. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 2010, 103, S80–S95.
  8. Al Naggar, Y.; Baer, B. Consequences of a short time exposure to a sublethal dose of Flupyradifurone (Sivanto) pesticide early in life on survival and immunity in the honeybee (Apis mellifera). Sci. Rep. 2019, 9, 19753–19762.
  9. Al Naggar, Y.; Paxton, R.J. Mode of transmission determines the virulence of black queen cell virus in adult honey bees, posing a future threat to bees and apiculture. Viruses 2020, 12, 535.
  10. Al Naggar, Y.; Paxton, R.J. The novel insecticides flupyradifurone and sulfoxaflor do not act synergistically with viral pathogens in reducing honey bee (Apis mellifera) survival but sulfoxaflor modulates host immunocompetence. Microb. Biotechnol. 2021, 14, 227–240.
  11. Jacques, A.; Laurent, M.; Consortium, E.; Ribière-Chabert, M.; Saussac, M.; Bougeard, S.; Budge, G.E.; Hendrikx, P.; Chauzat, M.-P. A pan-European epidemiological study reveals honey bee colony survival depends on beekeeper education and disease control. PLoS ONE 2017, 12, e0172591.
  12. Mullapudi, E.; Přidal, A.; Pálková, L.; de Miranda, J.R.; Plevka, P. Virion structure of Israeli acute bee paralysis virus. J. Virol. 2016, 90, 8150–8159.
  13. van Engelsdorp, D.; Evans, J.D.; Saegerman, C.; Mullin, C.; Haubruge, E.; Nguyen, B.K.; Frazier, M.; Frazier, J.; Cox-Foster, D.; Chen, Y.; et al. Colony collapse disorder: A descriptive study. PLoS ONE 2009, 4, e6481.
  14. Nazzi, F.; Annoscia, D.; Caprio, E.; Di Prisco, G.; Pennacchio, F. Honeybee immunity and colony losses. Entomologia 2014, 2, 80–87.
  15. Antúnez, K.; Martín-Hernández, R.; Prieto, L.; Meana, A.; Zunino, P.; Higes, M. Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol. 2009, 11, 2284–2290.
  16. Fallon, J.P.; Troy, N.; Kavanagh, K. Pre-exposure of Galleria mellonella larvae to different doses of Aspergillus fumigatus conidia causes differential activation of cellular and humoral immune responses. Virulence 2011, 2, 413–421.
  17. DeGrandi-Hoffman, G.; Chen, Y. Nutrition, immunity and viral infections in honey bees. Curr. Opin. Insect Sci. 2015, 10, 170–176.
  18. Karlikow, M.; Goic, B.; Saleh, M.-C. RNAi and antiviral defense in Drosophila: Setting up a systemic immune response. Dev. Comp. Immunol. 2014, 42, 85–92.
  19. Brutscher, L.M.; Flenniken, M.L. RNAi and antiviral defense in the honey bee. J. Immunol. Res. 2015, 2015, 941897.
  20. Vung, N.N.; Choi, Y.S.; Kim, I. High resistance to Sacbrood virus disease in Apis cerana (Hymenoptera: Apidae) colonies selected for superior brood viability and hygienic behavior. Apidologie 2020, 51, 61–74.
  21. Goblirsch, M.; Warner, J.F.; Sommerfeldt, B.A.; Spivak, M. Social fever or general immune response? Revisiting an example of social immunity in honey bees. Insects 2020, 11, 528.
  22. Cini, A.; Bordoni, A.; Cappa, F.; Petrocelli, I.; Pitzalis, M.; Iovinella, I.; Dani, F.R.; Turillazzi, S.; Cervo, R. Increased immunocompetence and network centrality of allogroomer workers suggest a link between individual and social immunity in honeybees. Sci. Rep. 2020, 10, 8928–8939.
  23. Simone, M.; Evans, J.D.; Spivak, M. Resin collection and social immunity in honey bees. Evol. Int. J. Org. Evol. 2009, 63, 3016–3022.
  24. Borba, R.S.; Spivak, M. Propolis envelope in Apis mellifera colonies supports honey bees against the pathogen, Paenibacillus larvae. Sci. Rep. 2017, 7, 11429–11440.
  25. Bucekova, M.; Valachova, I.; Kohutova, L.; Prochazka, E.; Klaudiny, J.; Majtan, J. Honeybee glucose oxidase—its expression in honeybee workers and comparative analyses of its content and H2O2-mediated antibacterial activity in natural honeys. Naturwissenschaften 2014, 101, 661–670.
  26. Brudzynski, K. Effect of hydrogen peroxide on antibacterial activities of Canadian honeys. Can. J. Microbiol. 2006, 52, 1228–1237.
  27. Gebremedhn, H.; Amssalu, B.; De Smet, L.; De Graaf, D.C. Factors restraining the population growth of Varroa destructor in Ethiopian honey bees (Apis mellifera simensis). PLoS ONE 2019, 14, e0223236.
  28. Ramsey, S.D.; Ochoa, R.; Bauchan, G.; Gulbronson, C.; Mowery, J.D.; Cohen, A.; Lim, D.; Joklik, J.; Cicero, J.M.; Ellis, J.D.; et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc. Natl. Acad. Sci. USA 2019, 116, 1792–1801.
  29. Richards, E.H.; Jones, B.; Bowman, A. Salivary secretions from the honeybee mite, Varroa destructor: Effects on insect haemocytes and preliminary biochemical characterization. Parasitology 2011, 138, 602–608.
  30. Koleoglu, G.; Goodwin, P.H.; Reyes-Quintana, M.; Guzman-Novoa, E. Effect of Varroa destructor, counding and Varroa homogenate on gene expression in brood and adult honey bees. PLoS ONE 2017, 12, e0169669.
  31. Nazzi, F.; Brown, S.P.; Annoscia, D.; Del Piccolo, F.; Di Prisco, G.; Varricchio, P.; Della Vedova, G.; Cattonaro, F.; Caprio, E.; Pennacchio, F. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog. 2012, 8, e1002735.
  32. Kielmanowicz, M.G.; Inberg, A.; Lerner, I.M.; Golani, Y.; Brown, N.; Turner, C.L.; Hayes, G.J.R.; Ballam, J.M. Prospective large-scale field study generates predictive model identifying major contributors to colony losses. PLoS Pathog. 2015, 11, e1004816.
  33. Di Prisco, G.; Pennacchio, F.; Caprio, E.; Boncristiani, H.F.; Evans, J.D.; Chen, Y. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J. Gen. Virol. 2011, 92, 151–155.
  34. Dainat, B.; Evans, J.D.; Chen, Y.P.; Gauthier, L.; Neumann, P. Predictive markers of honey bee colony collapse. PLoS ONE 2012, 7, e32151.
  35. Gisder, S.; Schüler, V.; Horchler, L.L.; Groth, D.; Genersch, E. Long-term temporal trends of Nosema spp. infection prevalence in Northeast Germany: Continuous spread of Nosema ceranae, an emerging pathogen of honey bees (Apis mellifera), but no general replacement of Nosema apis. Front. Cell. Infect. Microbiol. 2017, 7, 301–314.
  36. Higes, M.; Martín-Hernández, R.; Botías, C.; Bailón, E.G.; González-Porto, A.V.; Barrios, L.; Del Nozal, M.J.; Bernal, J.L.; Jiménez, J.J.; Palencia, P.G.; et al. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 2008, 10, 2659–2669.
  37. Dosselli, R.; Grassl, J.; Carson, A.; Simmons, L.W.; Baer, B. Flight behaviour of honey bee (Apis mellifera) workers is altered by initial infections of the fungal parasite Nosema apis. Sci. Rep. 2016, 6, 36649–36659.
  38. Grozinger, C.M.; Flenniken, M.L. Bee viruses: Ecology, pathogenicity, and impacts. Annu. Rev. Entomol. 2019, 64, 205–226.
  39. Škubnik, K.; Nováček, J.; Füzik, T.; Přidal, A.; Paxton, R.J.; Plevka, P. Structure of deformed wing virus, a major honey bee pathogen. Proc. Natl. Acad. Sci. USA 2017, 114, 3210–3215.
  40. Mao, W.; Schuler, M.A.; Berenbaum, M.R. Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. Proc. Natl. Acad. Sci. USA 2013, 110, 8842–8846.
  41. Alaux, C.; Kemper, N.; Kretzschmar, A.; Le Conte, Y. Brain, physiological and behavioral modulation induced by immune stimulation in honeybees (Apis mellifera): A potential mediator of social immunity? Brain Behav. Immun. 2012, 26, 1057–1060.
  42. Brodschneider, R.; Crailsheim, K. Nutrition and health in honey bees. Apidologie 2010, 41, 278–294.
  43. Cotter, S.C.; Simpson, S.J.; Raubenheimer, D.; Wilson, K. Macronutrient balance mediates trade-offs between immune function and life history traits. Funct. Ecol. 2011, 25, 186–198.
  44. Frizzera, D.; Del Fabbro, S.; Ortis, G.; Zanni, V.; Bortolomeazzi, R.; Nazzi, F.; Annoscia, D. Possible side effects of sugar supplementary nutrition on honey bee health. Apidologie 2020, 51, 594–608.
  45. Aldgini, H.M.M.; Al-Abbadi, A.A.; Abu-Nameh, E.S.M.; Alghazeer, R.O. Determination of metals as bio indicators in some selected bee pollen samples from Jordan. Saudi J. Biol. Sci. 2019, 26, 1418–1422.
  46. Nikolić, T.V.; Kojić, D.; Orčić, S.; Batinić, D.; Vukašinović, E.; Blagojević, D.P.; Purać, J. The impact of sublethal concentrations of Cu, Pb and Cd on honey bee redox status, superoxide dismutase and catalase in laboratory conditions. Chemosphere 2016, 164, 98–105.
  47. Fisogni, A.; Hautekèete, N.; Piquot, Y.; Brun, M.; Vanappelghem, C.; Michez, D.; Massol, F. Urbanization drives an early spring for plants but not for pollinators. Oikos 2020, 129, 1681–1691.
  48. Sadowska, M.; Gogolewska, H.; Pawelec, N.; Sentkowska, A.; Krasnodębska-Ostręga, B. Comparison of the contents of selected elements and pesticides in honey bees with regard to their habitat. Environ. Sci. Pollut. Res. 2019, 26, 371–380.
  49. Appler, R.H.; Frank, S.D.; Tarpy, D.R. Within-colony variation in the immunocompetency of managed and feral honey bees (Apis mellifera L.) in different urban landscapes. Insects 2015, 6, 912–925.
  50. Dabour, K.; Al Naggar, Y.; Masry, S.; Naiem, E.; Giesy, J.P. Cellular alterations in midgut cells of honey bee workers (Apis millefera L.) exposed to sublethal concentrations of CdO or PbO nanoparticles or their binary mixture. Sci. Total Environ. 2019, 651, 1356–1367.
  51. AL Naggar, Y.; Dabour, K.; Masry, S.; Sadek, A.; Naiem, E.; Giesy, J.P. Sublethal effects of chronic exposure to CdO or PbO nanoparticles or their binary mixture on the honey bee (Apis millefera L.). Environ. Sci. Pollut. Res. 2020, 27, 19004–19015.
  52. Sharma, V.P.; Kumar, N.R. Changes in honeybee behaviour and biology under the influence of cellphone radiations. Curr. Sci. 2010, 98, 1376–1378.
  53. Santhosh Kumar, S. Colony collapse disorder (CCD) in honey bees caused by EMF radiation. Bioinformation 2018, 14, 521–524.
  54. Lupi, D.; Tremolada, P.; Colombo, M.; Giacchini, R.; Benocci, R.; Parenti, P.; Parolini, M.; Zambon, G.; Vighi, M. Effects of pesticides and electromagnetic fields on honeybees: A field study using biomarkers. Int. J. Environ. Res. 2020, 14, 107–122.
  55. Odemer, R.; Odemer, F. Effects of radiofrequency electromagnetic radiation (RF-EMF) on honey bee queen development and mating success. Sci. Total Environ. 2019, 661, 553–562.
  56. O’Neal, S.T.; Anderson, T.D.; Wu-Smart, J.Y. Interactions between pesticides and pathogen susceptibility in honey bees. Curr. Opin. Insect Sci. 2018, 26, 57–62.
  57. Pettis, J.S.; Vanengelsdorp, D.; Johnson, J.; Dively, G. Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 2012, 99, 153–158.
  58. Di, G.; Cavaliere, V.; Annoscia, D.; Varricchio, P.; Caprio, E.; Nazzi, F. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc. Natl. Acad. Sci. USA 2013, 110, 18466–18471.
  59. Dussaubat, C.; Maisonnasse, A.; Crauser, D.; Tchamitchian, S.; Bonnet, M.; Cousin, M.; Kretzschmar, A.; Brunet, J.-L.; Le Conte, Y. Combined neonicotinoid pesticide and parasite stress alter honeybee queens’ physiology and survival. Sci. Rep. 2016, 6, 31430–31436.
  60. Aufauvre, J.; Misme-Aucouturier, B.; Viguès, B.; Texier, C.; Delbac, F.; Blot, N. Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS ONE 2014, 9, e91686.
  61. Retschnig, G.; Neumann, P.; Williams, G.R. Thiacloprid-Nosema ceranae interactions in honey bees: Host survivorship but not parasite reproduction is dependent on pesticide dose. J. Invertebr. Pathol. 2014, 118, 18–19.
  62. Tosi, S.; Nieh, J.C.; Sgolastra, F.; Cabbri, R.; Medrzycki, P. Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proc. R. Soc. B Biol. Sci. 2017, 284, 20171711–20171719.
  63. Sánchez-bayo, F.; Goulson, D.; Pennacchio, F.; Nazzi, F.; Goka, K.; Desneux, N. Are bee diseases linked to pesticides ?—A brief review. Environ. Int. 2016, 89–90, 7–11.
  64. Wu-Smart, J.; Spivak, M. Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development. Sci. Rep. 2016, 6, 32108–32119.
  65. Foley, K.; Fazio, G.; Jensen, A.B.; Hughes, W.O.H. Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae. J. Invertebr. Pathol. 2012, 111, 68–73.
  66. Koch, H.; Brown, M.J.; Stevenson, P.C. The role of disease in bee foraging ecology. Curr. Opin. Insect Sci. 2017, 21, 60–67.
  67. Dolezal, A.G.; Carrillo-Tripp, J.; Judd, T.M.; Allen Miller, W.; Bonning, B.C.; Toth, A.L. Interacting stressors matter: Diet quality and virus infection in honeybee health. R. Soc. Open Sci. 2019, 6, 181803–181813.
  68. Dolezal, A.G.; Toth, A.L. Feedbacks between nutrition and disease in honey bee health. Curr. Opin. Insect Sci. 2018, 26, 114–119.
  69. Zhao, Y.; Heerman, M.; Peng, W.; Evans, J.D.; Rose, R.; DeGrandi-Hoffman, G.; Simone-Finstrom, M.; Li, J.; Li, Z.; Cook, S.C. The dynamics of deformed wing virus concentration and host defensive gene expression after Varroa mite parasitism in honey bees, Apis mellifera. Insects 2019, 10, 16.
  70. Hou, C.; Rivkin, H.; Slabezki, Y.; Chejanovsky, N. Dynamics of the presence of israeli acute paralysis virus in honey bee colonies with colony collapse disorder. Viruses 2014, 6, 2012–2027.
  71. Sperandio, G.; Simonetto, A.; Carnesecchi, E.; Costa, C.; Hatjina, F.; Tosi, S.; Gilioli, G. Beekeeping and honey bee colony health: A review and conceptualization of beekeeping management practices implemented in Europe. Sci. Total Environ. 2019, 696, 133795–133806.
  72. Adamczyk, S.; Lázaro, R.; Pérez-Arquillué, C.; Conchello, P.; Herrera, A. Evaluation of residues of essential oil components in honey after different anti-Varroa treatments. J. Agric. Food Chem. 2005, 53, 10085–10090.
  73. Rosenkranz, P.; Aumeier, P.; Ziegelmann, B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 2010, 103, S96–S119.
  74. Sun, L.; Zhang, X.; Xu, S.; Hou, C.; Xu, J.; Zhao, D.; Chen, Y. Antiviral activities of a medicinal plant extract against sacbrood virus in honeybees. Virol. J. 2021, 18, 83–92.
  75. Tauber, J.P.; Collins, W.R.; Schwarz, R.S.; Chen, Y.; Grubbs, K.; Huang, Q.; Lopez, D.; Peterson, R.; Evans, J.D. Natural product medicines for honey bees: Perspective and protocols. Insects 2019, 10, 356.
  76. Hasan, S. A review on nanoparticles: Their synthesis and types. Res. J. Recent Sci 2015, 2277, 2502–2504.
  77. Sousa, F.; Ferreira, D.; Reis, S.; Costa, P. Current insights on antifungal therapy: Novel nanotechnology approaches for drug delivery systems and new drugs from natural sources. Pharmaceuticals 2020, 13, 248.
  78. Culha, M.; Kalay, Ş.; Sevim, E.; Pinarbaş, M.; Baş, Y.; Akpinar, R.; Karaoğlu, Ş.A. Biocidal properties of maltose reduced silver nanoparticles against American foulbrood diseases pathogens. Biometals 2017, 30, 893–902.
  79. Potts, S.G.; Roberts, S.P.M.; Dean, R.; Marris, G.; Brown, M.A.; Jones, R.; Neumann, P.; Settele, J. Declines of managed honey bees and beekeepers in Europe. J. Apic. Res. 2010, 49, 15–22.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
This entry is offline, you can click here to edit this entry!
Academic Video Service
Feedback