1 Introduction

Honey bee colonies are essential for the pollination of many crops, contributing significantly to global food production and biodiversity. However, bee colonies face numerous challenges, including malnutrition, diseases, and environmental stressors, which can lead to colony decline and losses (DeGrandi-Hoffman et al., 2015; Topal et al., 2022; Li, 2024). Ensuring the health and sustainability of bee colonies is critical for both ecological balance and agricultural productivity.

Nutrition plays a pivotal role in the health and productivity of honey bee colonies. Adequate nutrition, primarily derived from pollen and nectar, is necessary for the development of brood, maintenance of adult bee populations, and overall colony strength (Tawfik et al., 2020; Hoover et al., 2022). During periods of natural forage scarcity, such as winter or early spring, supplemental feeding becomes crucial. Studies have shown that different types of supplemental diets can significantly impact colony parameters, including brood area, population density, and honey yield (Rousseau and Giovenazzo, 2016; Ahmad et al., 2021; Vijayakumari et al., 2022). Proper nutrition also enhances bees' resilience to diseases and parasites, contributing to better colony survival rates (Mortensen et al., 2018; Al-Ghamdi et al., 2021).

Bee feed optimization involves the strategic use of supplemental diets to enhance colony health and performance. Various studies have explored the effects of different protein and carbohydrate supplements on bee colonies. For instance, feeding colonies with protein-rich diets, such as pollen substitutes, has been shown to improve brood rearing and adult bee populations. Additionally, the inclusion of specific additives, like vitamins and plant extracts, can further boost colony health by enhancing bees’ immune responses and reducing parasite loads (Tawfik et al., 2020; Al-Ghamdi et al., 2021). The optimization of bee feed not only supports colony growth during dearth periods but also prepares colonies for critical pollination tasks (Rousseau and Giovenazzo, 2016; Hoover et al., 2022).

This study attempts to explore the impact of optimized bee feed on colony health, discusses effective supplemental feeding strategies that enhance colony performance and resilience, and provides an overview of best practices for bee nutrition management, with the aim of offering valuable insights for beekeepers and researchers, contributing to the sustainability of honey bee populations.

2 Bee Nutrition Requirements

2.1 Macronutrients in bee diets

Carbohydrates are a primary energy source for honey bees, especially during the winter months when natural forage is scarce. In managed colonies, beekeepers often replace harvested honey with artificial feeds such as sucrose syrup, high-fructose corn syrup, or invert syrup. Studies have shown that bees fed on natural honey exhibit better survival rates and larger fat bodies compared to those fed on artificial carbohydrate sources, indicating the superior nutritional quality of honey (Quinlan et al., 2023). The choice of carbohydrate source can significantly impact colony strength and individual bee health, with natural honey being the most beneficial.

Proteins are crucial for the growth and development of bee larvae and the maintenance of adult bees. Pollen is the primary source of protein for bees, and its quality can affect colony performance. For instance, colonies fed with high-protein pollen sources such as Papaver somniferum showed better wintering ability and longer in-vitro longevity compared to those fed with lower protein sources (Topal et al., 2022). Additionally, supplemental protein feeds in the form of patties have been shown to support colony growth and increase brood rearing, especially during periods of pollen scarcity (Mortensen et al., 2018; Hoover et al., 2022).

Lipids play a vital role in maintaining cell membrane integrity and hormonal balance in bees. They are primarily obtained frompollen and are essential for the development of hypopharyngeal glands in nurse bees. Studies have demonstrated that bees regulate their intake of lipids to maintain an optimal balance with proteins, which is crucial for their health and behavior (Stabler et al., 2020). Diets with balanced fatty acid ratios have been shown to improve olfactory learning and cognitive functions in young worker bees, which are essential for brood care and colony hygiene (Bennett et al., 2022).

2.2 Micronutrients and their impact on bee health

Vitamins are essential micronutrients that support various physiological functions in bees. For example, Vitamin C supplementation in pollen substitute diets has been shown to improve pollen load, worker-sealed brood area, and overall colony strength (Ahmad et al., 2021). The inclusion of vitamins in supplemental diets can enhance the nutritional quality of the feed and support better colony health.Minerals, though required in smaller quantities, are vital for bee health. They play roles in enzyme function, nerve transmission, and overall metabolic processes. The specific impact of different minerals on bee health is less studied, but their presence in natural pollen sources suggests their importance in a balanced diet.

2.3 Water as an essential component of bee health

Water is a critical component of bee health, necessary for digestion, thermoregulation, and brood rearing. Bees collect water from natural sources, and its availability can influence colony activities. Ensuring that bees have access to clean water is essential for maintaining colony health and supporting various physiological functions. Optimizing bee feed by ensuring a balanced intake of macronutrients, micronutrients, and water is crucial for maintaining colony health and productivity. Carbohydrates, proteins, and lipids each play distinct roles in supporting the energy needs, growth, and development of bees. Additionally, vitamins and minerals, though required in smaller amounts, are essential for various physiological functions. Proper supplementation, especially during periods of natural forage scarcity, can significantly enhance colony performance and resilience.

3 Bee Feed Optimization Techniques

3.1 Artificial diets: components and formulation

Artificial diets play a crucial role in maintaining the health and productivity of honey bee colonies, especially during periods when natural forage is scarce. These diets typically include a combination of proteins, carbohydrates, vitamins, and minerals. For instance, a study demonstrated that a diet consisting of soybean flour, Brewer’s yeast, powdered sugar, skimmed milk, date palm pollen, and sugar syrup supplemented with Vitamin C significantly improved colony parameters such as pollen load, worker-sealed brood area, population strength, and honey yield (Ahmad et al., 2021). Another study highlighted the importance of including all essential amino acids in protein feeds, noting that deficiencies in lysine and arginine could impact colony growth (Hoover et al., 2022).

3.2 Seasonal feeding strategies

Winter feeding is critical for colony survival and health during the cold months when natural food sources are unavailable. Research has shown that colonies fed with artificial diet cakes and sucrose syrup supplemented with Vitamin C for extended periods (up to 18 weeks) exhibited marked improvements in colony growth parameters and antioxidant systems, which are essential for reducing oxidative stress during overwintering (Tawfik et al., 2020). Additionally, the type of carbohydrate used for winter feeding can influence colony health. Colonies fed with honey or sucrose syrup showed better survival rates and larger adult populations compared to those fed with high-fructose corn syrup (Quinlan et al., 2023).

During the summer, when colonies are actively foraging and pollinating, supplemental feeding can enhance colony strength and productivity. A study on the effects of spring protein feeds found that colonies supplemented with protein in advance of the summer pollination season had increased brood rearing and adult bee populations, which are crucial for effective pollination (Hoover et al., 2022). Moreover, feeding colonies with sucrose syrup and protein supplements in early spring was shown to improve drone reproductive quality, which is vital for queen fecundation (Rousseau and Giovenazzo, 2016).

3.3 Nutritional supplementation

Protein supplements are essential for the development and maintenance of healthy bee colonies. Various studies have demonstrated the benefits of different protein sources. For example, feeding colonies with pollen sources of different protein content significantly affected colony performance, wintering ability, and in-vitro longevity, with Papaver somniferum pollen showing the best results (Topal et al., 2022). Another study found that protein feeding modulates both individual and social immunity, with mixed pollen diets leading to higher vitellogenin levels and better stress protein profiles in bees (Sarioğlu-Bozkurt et al., 2022).

Carbohydrate supplements are equally important, especially during periods when natural nectar is scarce. Research comparing different carbohydrate sources for overwintering found that while sucrose and invert syrups are commonly used, there were no significant differences in colony condition or honey production between the two, although invert syrups were more expensive (Přidal et al., 2023). Another study highlighted that colonies fed with honey or sucrose syrup had better nutritional states and gene expression profiles compared to those fed with high-fructose corn syrup (Quinlan et al., 2023).

3.4 Environmental and floral diversity impacts on nutrition

The availability and diversity of floral resources significantly impact the nutritional status and health of bee colonies. A comprehensive review emphasized the importance of a well-balanced diet rich in proteins and carbohydrates, which can be achieved through diverse floral sources or well-formulated artificial diets (Lata et al., 2023). The study noted that proper hydration and the use of electrolyte solutions are crucial for supporting honeybee thermoregulation, digestion, and overall colony maintenance. The presence of diverse pollen sources, such as Cistus creticus and mixed pollen, was shown to positively affect the health and longevity of honey bees (Figure 1) (Branchiccela et al., 2019; Topal et al., 2022; Sarioğlu-Bozkurt et al., 2022).

Figure 1 Experimental design (Adopted from Branchiccela et al., 2019)

Optimizing bee feed through artificial diets, seasonal feeding strategies, and nutritional supplementation is essential for maintaining healthy and productive colonies. The choice of diet components, timing of feeding, and the diversity of nutritional sources all play critical roles in enhancing colony health and resilience. By understanding and implementing these techniques, beekeepers can significantly improve the sustainability and productivity of their apiaries.

Branchiccela et al. (2019) presents a timeline-based experimental setup examining the seasonal activity and strength of honeybee colonies. It highlights the Eucalyptus grandis bloom period during autumn (March to May), where two groups of colonies (Group M and Group P, each with 31 colonies) were fed polyfloral pollen pie every 15 days. Six sampling events were conducted from March to September (autumn to spring) to assess colony strength. After the autumn season, the colonies were relocated from Rivera to Colonia to adapt to winter conditions, as depicted by the truck icon. The schematic integrates temporal, geographical, and methodological elements, showcasing the seasonal influence on colony dynamics.

4 Evaluating the Effects of Optimized Feed on Colony Health

4.1 Physiological indicators of bee health

Optimized feeding regimens have been shown to significantly enhance the immune system function of honey bees. For instance, colonies supplemented with a diet containing soybean flour, Brewer’s yeast, powdered sugar, skimmed milk, date palm pollen, and Vitamin C exhibited improved colony development and health parameters compared to control groups (Ahmad et al., 2021). Additionally, the antioxidant system in bees, including activities of superoxide dismutase (SOD) and catalase (CAT) enzymes, was markedly improved with prolonged supplemental feeding, suggesting a reduction in oxidative stress (Tawfik et al., 2020). This indicates that optimized feeding can bolster the bees’ immune defenses, potentially reducing susceptibility to diseases.

The longevity and lifespan of worker bees are critical indicators of colony health. Studies have demonstrated that feeding bees with high-protein pollen sources, such as Papaver somniferum pollen, significantly increased their in-vitro longevity, with bees in this group living up to 23 days (Topal et al., 2022). Furthermore, the presence of essential amino acids in supplemental feeds has been linked to improved longevity and overall health of the bees (Hoover et al., 2022; Sarioğlu-Bozkurt et al., 2022). These findings underscore the importance of nutrient-rich diets in extending the lifespan of worker bees, thereby enhancing colony stability.

4.2 Brood production and development

Brood rearing rates are a direct measure of a colony’s reproductive success. Colonies provided with supplemental diets, particularly those rich in protein, showed significantly higher brood rearing rates. For example, colonies fed with a diet containing a mix of soybean flour, Brewer’s yeast, and other nutrients had a larger worker-sealed brood area compared to those on a sugar syrup diet (Ahmad et al., 2021). Similarly, colonies supplemented with various protein feeds in spring exhibited increased brood rearing, which is crucial for maintaining colony strength during pollination periods (Hoover et al., 2022).

The developmental health and survival of brood are enhanced by optimized feeding. Colonies fed with high-protein pollen sources demonstrated better wintering ability and higher survival rates of brood (Topal et al., 2022). Additionally, the quality of the brood, as indicated by parameters such as queen emergence weight and spermathecae diameter, was improved with supplemental feeding (Cengiz et al., 2019). These improvements in brood health and survival are essential for sustaining robust and productive colonies.

4.3 Colony productivity and honey yield

Optimized feeding has a profound impact on colony productivity and honey yield. Studies have shown that colonies receiving supplemental diets, particularly those rich in protein and essential nutrients, produced significantly more honey compared to control groups (Ahmad et al., 2021; Vijayakumari et al., 2022). The increased availability of nutrients supports higher foraging activity and better overall colony health, leading to enhanced honey production. This is particularly important during periods of pollen dearth, where natural forage is limited.

4.4 Resilience to environmental stressors

The resilience of honey bee colonies to environmental stressors is greatly influenced by their nutritional status. Colonies that received supplemental feeding exhibited better resilience to stressors such as malnutrition and oxidative stress. For instance, bees fed with a combination of sugar syrup and protein supplements showed improved antioxidant enzyme activities, which help mitigate the effects of environmental stress (Tawfik et al., 2020). Additionally, the presence of essential fatty acids and amino acids in the diet was linked to better stress protein (HSP 70) responses, further enhancing the bees’ ability to cope with adverse conditions (Sarioğlu-Bozkurt et al., 2022). These findings highlight the critical role of optimized feeding in enhancing the resilience and overall health of honey bee colonies.

5 Case Study: Impact of High-Protein Diet on Colony Health and Productivity

5.1 Study design and methodology

The study aimed to evaluate the impact of a high-protein diet on the health and productivity of honey bee colonies. Various protein supplements were tested, including commercially available protein feeds and natural pollen sources. The experimental setup involved multiple colonies divided into treatment and control groups. The treatment groups received different protein supplements, while the control groups were either unsupplemented or provided with sugar syrup. Key parameters measured included colony growth, brood rearing, adult bee population, and overall colony health indicators such as pathogen load and stress protein levels (Figure 2) (Ahmad et al., 2021; Hoover et al., 2022; Kim et al., 2024).

Figure 2 Schematic overview of experiment design (Adopted from Kim et al., 2024) Image caption: (A) Field experiment: Fifteen colonies were used for field experiments. (B) Cage experiment: Twelve cages were used for cage experiments. The diets were provided during the timeframe indicated by the empty egg-shaped circles (Adopted from Kim et al., 2024)

5.2 Comparison of colonies with and without high-protein diet

Colonies supplemented with high-protein diets showed significant differences compared to those without such supplementation. Colonies receiving protein feeds demonstrated higher brood rearing efficiency, increased adult bee populations, and improved overall colony strength. For instance, colonies fed with a diet containing 23% crude protein exhibited larger mandibular glands and higher secretory cell heights, indicating better nutritional status (Camilli et al., 2021). Additionally, colonies provided with natural forage had lower pathogen loads and higher overwinter survival rates compared to those fed protein supplements (DeGrandi-Hoffman et al., 2015). In contrast, unsupplemented colonies or those given only sugar syrup showed reduced brood rearing and lower adult bee populations (Blagov and Kolchaeva, 2022).

5.3 Results and observations

The results indicated that high-protein diets positively influenced colony health and productivity. Colonies fed with protein supplements had higher vitellogenin (Vg) levels, which are crucial for overwintering success and overall colony health (Sarioğlu-Bozkurt et al., 2022). The study also observed that colonies receiving mixed pollen or specific high-protein pollen sources like Papaver somniferum had better wintering ability and longer in-vitro longevity (Topal et al., 2022). Furthermore, colonies supplemented with protein feeds showed enhanced drone reproductive quality, with increased drone weight and semen viability (Rousseau and Giovenazzo, 2016). However, it was noted that the type and quality of protein feed significantly affected the outcomes, with some feeds being more effective than others (Mortensen et al., 2018).

5.4 Implications of findings for feed optimization

The findings underscore the importance of optimizing protein feed for honey bee colonies to enhance their health and productivity. High-protein diets, particularly those with balanced amino acid profiles and additional biologically active substances, can significantly improve colony strength and resilience against environmental stresses and pathogens (Tawfik et al., 2020). Beekeepers should consider incorporating high-quality protein supplements, especially during periods of pollen dearth, to support colony growth and sustainability. The study also highlights the potential benefits of natural forage over artificial supplements, suggesting that providing access to diverse and high-protein pollen sources could be a more effective strategy for maintaining colony health.

6 Challenges and Limitations in Bee Feed Optimization

6.1 Cost and accessibility of feed resources

One of the primary challenges in bee feed optimization is the cost and accessibility of high-quality feed resources. Beekeepers often need to supplement natural forage with commercial pollen and nectar substitutes to maintain colony health, especially during periods of nutritional stress or habitat depletion (Mortensen et al., 2018; Branchiccela et al., 2019). However, the cost of these supplements can be prohibitive, and their availability may be limited, particularly in remote or economically disadvantaged areas. Additionally, the variability in the nutritional content of commercially available feeds can affect their efficacy, making it difficult for beekeepers to choose the best option for their colonies (Hoover et al., 2022).

6.2 Variability in environmental and floral conditions

Environmental and floral conditions play a significant role in the success of bee feed optimization. The availability and quality of natural forage can vary widely depending on the season, weather, and landscape composition (Vaudo et al., 2015; Abi-Akar et al., 2020). For instance, colonies placed in areas with limited floral diversity or during off-peak flowering periods may suffer from nutritional stress, even with supplemental feeding (Branchiccela et al., 2019; Requier et al., 2019). This variability makes it challenging to standardize feeding practices and ensure consistent colony health across different environments.

6.3 Impact of pesticides and pollutants on bee nutrition

Pesticides and pollutants present another significant limitation to bee feed optimization. Exposure to these chemicals can negatively impact bee health by reducing the nutritional quality of available forage and directly affecting bee physiology. Pesticides can alter the composition of royal jelly, a critical nutrient for developing queens, and reduce the overall nutritional value of pollen and nectar (Milone et al., 2021). Additionally, the interaction between pesticides and pathogens can exacerbate health issues, making it more difficult to maintain healthy colonies even with optimized feeding practices (O’Neal et al., 2018).

6.4 Ethical considerations in artificial feeding

Ethical considerations also arise in the context of artificial feeding. While supplemental feeding can help maintain colony health during periods of nutritional stress, it may also lead to unintended consequences, such as dependency on artificial feeds or disruption of natural foraging behaviors (Hoover et al., 2022; Topal et al., 2022). There is also the concern that artificial feeding may mask underlying environmental issues, such as habitat loss and pesticide exposure, rather than addressing the root causes of bee population declines (Jovanović et al., 2021). Beekeepers and researchers must balance the immediate benefits of supplemental feeding with the long-term sustainability of bee populations and ecosystems.

Optimizing bee feed to enhance colony health involves navigating several challenges and limitations, including the cost and accessibility of feed resources, variability in environmental and floral conditions, the impact of pesticides and pollutants, and ethical considerations in artificial feeding. Addressing these challenges requires a multifaceted approach that includes improving the quality and availability of supplemental feeds, mitigating environmental stressors, and promoting sustainable beekeeping practices. By understanding and addressing these limitations, we can better support the health and resilience of bee colonies.

7 Future Directions and Recommendations

7.1 Innovations in feed formulation

The optimization of bee feed formulations is crucial for enhancing colony health and productivity. Future research should focus on developing feeds that closely mimic the nutritional profile of natural pollen, ensuring that all essential amino acids, vitamins, and minerals are present in optimal proportions. Studies have shown that current commercial feeds often lack sufficient levels of certain amino acids like lysine and arginine, which are vital for bee growth and development (Ahmad et al., 2021; Hoover et al., 2022). Additionally, incorporating plant extracts such as cinnamon and chamomile into sugar feeds has shown promise in improving colony health and controlling parasites like Varroa mites (Al-Ghamdi et al., 2021). Therefore, further exploration into the synergistic effects of various natural additives could lead to more effective and holistic feed solutions.

7.2 Integrating feed optimization with environmental conservation

The health of bee colonies is intrinsically linked to the availability of natural forage. Therefore, feed optimization should be integrated with broader environmental conservation efforts. This includes promoting the planting of diverse, bee-friendly flora to ensure a steady supply of natural pollen and nectar throughout the year. Studies have indicated that the availability of external forage sources significantly impacts the effectiveness of supplemental feeds (Hoover et al., 2022; Topal et al., 2022). Moreover, landscape composition and environmental conditions play a critical role in the overwintering success of bee colonies (Abi-Akar et al., 2020). By aligning feed optimization strategies with environmental conservation, we can create a more sustainable ecosystem that supports both managed and wild bee populations.

7.3 Collaboration between beekeepers, scientists, and policy makers

Effective feed optimization and colony health management require a collaborative approach involving beekeepers, scientists, and policymakers. Beekeepers’ practical insights and experiences are invaluable for identifying the most pressing challenges and testing new feed formulations in real-world conditions (Sperandio et al., 2019; Steinhauer et al., 2021). Scientists can contribute by conducting rigorous research to understand the nutritional needs of bees and the impacts of various feed components on colony health (Paiva et al., 2016; Mortensen et al., 2018). Policymakers can support these efforts by funding research initiatives, promoting best practices, and implementing regulations that protect bee habitats and ensure the availability of high-quality feed ingredients. By fostering a collaborative environment, we can develop comprehensive strategies that enhance bee health and ensure the sustainability of apiculture and agriculture as a whole.

8 Concluding Remarks

The research on bee feed optimization has demonstrated significant impacts on colony health and performance. Various studies have shown that supplemental diets can enhance colony strength, brood area, and honey yield. For instance, a study found that a diet consisting of soybean flour, Brewer’s yeast, powdered sugar, skimmed milk, date palm pollen, and sugar syrup significantly improved pollen load, worker-sealed brood area, population strength, and honey yield compared to other diets and a control group. Another study highlighted the benefits of feeding colonies with P. somniferum pollen, which resulted in better colony performance, wintering ability, and in-vitro longevity. Additionally, the use of commercially available protein feeds in spring was shown to increase colony populations in preparation for summer pollination. The inclusion of plant extracts like cinnamon in sugar feeding also demonstrated potential in controlling Varroa mites and enhancing colony development.

Optimized feed plays a crucial role in sustainable beekeeping by ensuring that colonies receive adequate nutrition, especially during periods of pollen dearth. Studies have shown that supplemental feeding with protein and sugar syrups can significantly improve colony health and productivity. For example, feeding colonies with sucrose syrup and protein supplements in early spring was found to enhance drone reproductive quality, which is vital for the fecundation of early-bred queens. Similarly, the use of sugar syrup with glucose was effective in increasing sealed brood area, honey store area, pollen store area, and adult bee population in Asiatic hive bees. Moreover, plant-based supplements containing B-complex vitamins were shown to improve colony strength and reduce pathogen loads, thereby preventing nutritive stress and enhancing the bees’ ability to combat pathogens. However, it is also important to note that natural forage can provide better outcomes in terms of pathogen loads and overwinter survival compared to protein supplements.

The future potential of bee feed optimization lies in the continued exploration and refinement of supplemental diets to meet the nutritional needs of honey bee colonies. Further research is needed to understand the long-term impacts of various feed types on colony health and productivity. Additionally, the development of cost-effective and nutritionally balanced supplements will be crucial for widespread adoption among beekeepers. The integration of natural forage with supplemental feeding strategies could offer a balanced approach to maintaining colony health and sustainability. As the beekeeping industry faces challenges such as climate change and habitat loss, optimized feeding practices will be essential in supporting the resilience and productivity of honey bee colonies.

Acknowledgments

We are grateful to Dr. Zhang for critically reading the manuscript and providing valuable feedback that improved the clarity of the text. We express our heartfelt gratitude to the two anonymous reviewers for their valuable comments on the manuscript.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

References

Abi-Akar F., Schmolke A., Roy C., Galic N., and Hinarejos S., 2020, simulating honey bee large‐scale colony feeding studies using the BEEHAVE model-part II: analysis of overwintering outcomes, Environmental Toxicology and Chemistry, 39(11): 2286-2297.

https://doi.org/10.1002/etc.4844

Ahmad S., Khan K.A., Khan S.A., Ghramh H.A., and Gul A., 2021, Comparative assessment of various supplementary diets on commercial honey bee (Apis mellifera) health and colony performance, PLoS One, 16(10): e0258430.

https://doi.org/10.1371/journal.pone.0258430

Al-Ghamdi AA.., Abou-Shaara, H.F., and Ansari M.J., 2021, Effects of sugar feeding supplemented with three plant extracts on some parameters of honey bee colonies, Saudi Journal of Biological Sciences, 28(4): 2076-2082.

https://doi.org/10.1016/j.sjbs.2021.02.050

Bennett M.M., Welchert A.C., Carroll M., Shafir S., Smith B.H., and Corby-Harris V., 2022, Unbalanced fatty acid diets impair discrimination ability of honey bee workers to damaged and healthy brood odors, The Journal of Experimental Biology, 225(7): jeb244103. 

https://doi.org/10.1242/jeb.244103

Blagov D.A., and Kolchaeva I.N., 2022, The use of protein and other biologically active substances in feeding honey bees, The Agrarian Scientific Journal, 2022: 54-57. 

https://doi.org/10.28983/asj.y2022i12pp54-57

Branchiccela B., Castelli L., Corona M., Díaz-Cetti S., Invernizzi C., Escalera G., Mendoza Y., Santos E., Silva C., Zunino P., and Antúnez K., 2019, Impact of nutritional stress on the honeybee colony health, Scientific Reports, 9(1): 10156.

https://doi.org/10.1038/s41598-019-46453-9

Camilli M.P., Barros D.C., Justulin L.A., Tse M.L., and Orsi R.D.O., 2021, Protein feed stimulates the development of mandibular glands of honey bees (Apis mellifera), Journal of Apicultural Research, 60(1): 165-171.

https://doi.org/10.1080/00218839.2020.1778922

Cengiz M., Yazici K., and Arslan S., 2019, The effect of the supplemental feeding of queen rearing colonies on the reproductive characteristics of queen bees (Apis mellifera L.) reared from egg and different old of larvae, Kafkas Universitesi Veteriner Fakultesi Dergisi, 25: 849-855.

DeGrandi-Hoffman G., Chen Y., Rivera R., Carroll M., Chambers M., Hidalgo G., and Jong E.W., 2015, Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements, Apidologie, 47: 186-196.

https://doi.org/10.1007/s13592-015-0386-6

Hoover S.E., Ovinge L.P., and Kearns J.D., 2022, Consumption of supplemental spring protein feeds by western honey bee (hymenoptera: apidae) colonies: effects on colony growth and pollination potential, Journal of Economic Entomology, 115(2): 417-429.

https://doi.org/10.1093/jee/toac006

Jovanović N.M., Glavinić U., Delić B., Vejnović B., Aleksic N., Mladjan V., and Stanimirović Z., 2021, Plant-based supplement containing B-complex vitamins can improve bee health and increase colony performance, Preventive Veterinary Medicine, 190: 105322.

https://doi.org/10.1016/j.prevetmed.2021.105322

Kim H., Frunze O., Lee J.H., and Kwon H.W., 2024, Enhancing honey bee health: evaluating pollen substitute diets in field and cage experiments, Insects, 15(5): 361.

Lata P., Prasad S., and Gupta G., 2023, Artificial diet alternatives or supplements for healthy honey beekeeping, Current Journal of Applied Science and Technology, 42(46): 91-100. 

https://doi.org/10.9734/cjast/2023/v42i464298

Li J., 2024, Threats to honeybee populations: pathogens, pesticides, and environmental changes, Molecular Pathogens, 15(3): 129-141.

https://doi.org/10.5376/mp.2024.15.0013

Milone J.P., Chakrabarti P., Sagili R.R., and Tarpy D.R., 2021, Colony-level pesticide exposure affects honey bee (Apis mellifera L.) royal jelly production and nutritional composition, Chemosphere, 263: 128183.

https://doi.org/10.1016/j.chemosphere.2020.128183

Mortensen A., Jack C., Bustamante T., Schmehl D., and Ellis J., 2018, Effects of supplemental pollen feeding on honey bee (hymenoptera: apidae) colony strength and Nosema spp. Infection, Journal of Economic Entomology, 112(1): 60-66. 

https://doi.org/10.1093/jee/toy341

O’Neal S., Anderson T.D., and Wu-Smart J.Y., 2018, Interactions between pesticides and pathogen susceptibility in honey bees, Current Opinion in Insect Science, 26: 57-62. 

https://doi.org/10.1016/j.cois.2018.01.006

Paiva J.P.L.M., Paiva H.M., Esposito E., and Morais M.M., 2016, On the effects of artificial feeding on bee colony dynamics: a mathematical model, PLoS One, 11(11): e0167054.

https://doi.org/10.1371/journal.pone.0167054

Přidal A., Musila J., and Svoboda J., 2023, Condition and honey productivity of honeybee colonies depending on type of supplemental feed for overwintering, Animals: an Open Access Journal from MDPI, 13(3): 323.

https://doi.org/10.3390/ani13030323

Quinlan G., Döke M.A., Ortiz-Alvarado Y., Rodriguez-Gomez N., Koru Y.B., and Underwood R., 2023, Carbohydrate nutrition associated with health of overwintering honey bees, Journal of Insect Science, 23(6): 16.

https://doi.org/10.1093/jisesa/iead084

Requier F., Jowanowitsch K.K., Kallnik K., and Steffan‐Dewenter I., 2019, Limitation of complementary resources affects colony growth, foraging behavior, and reproduction in bumble bees, Ecology, 101(3): e02946.

https://doi.org/10.1002/ecy.2946

Rousseau A., and Giovenazzo P., 2016, Optimizing drone fertility with spring nutritional supplements to honey bee (hymenoptera: apidae) colonies, Journal of Economic Entomology, 109: 1009-1014.

https://doi.org/10.1093/jee/tow056

Sarioğlu-Bozkurt A., Topal E., Güneş N., Üçeş E., Cornea-Cipcigan M., Coşkun İ., Cuibus L., and Mărgăoan R., 2022, Changes in vitellogenin (Vg) and stress protein (HSP 70) in honey bee (Apis mellifera anatoliaca) groups under different diets linked with physico-chemical, antioxidant and fatty and amino acid profiles, Insects, 13(11): 985.

https://doi.org/10.3390/insects13110985

Sperandio G., Simonetto A., Carnesecchi E., Costa C., Hatjina F., Tosi S., and Gilioli G., 2019, Beekeeping and honey bee colony health: A review and conceptualization of beekeeping management practices implemented in Europe, Science of The Total Environment, 696: 133795. 

https://doi.org/10.1016/J.SCITOTENV.2019.133795

Stabler D., Al-Esawy M., Chennells J.A., Perri G., Robinson A., and Wright G.A., 2020, Regulation of dietary intake of protein and lipid by nurse-age adult worker honeybees, The Journal of Experimental Biology, 224(3): jeb230615. 

https://doi.org/10.1242/jeb.230615

Steinhauer N., vanEngelsdorp D., and Saegerman C., 2021, Prioritizing changes in management practices associated with reduced winter honey bee colony losses for US beekeepers, The Science of the Total Environment, 753: 141629.

https://doi.org/10.1016/j.scitotenv.2020.141629

Tawfik A., Ahmed Z.H., Abdel-Rahman M.F., and Moustafa A.M., 2020, Influence of winter feeding on colony development and the antioxidant system of the honey bee, Apis mellifera, Journal of Apicultural Research, 59(5): 752-763.

https://doi.org/10.1080/00218839.2020.1752456

Topal E., Mărgăoan R., Bay V., Takma Ç., Yücel B., Oskay D., Düz G., Acar S., and Kösoğlu M., 2022, The effect of supplementary feeding with different pollens in autumn on colony development under natural environment and in vitro lifespan of honey bees, Insects, 13(7): 588.

https://doi.org/10.3390/insects13070588

Vaudo A.D., Tooker J.F., Grozinger C.M., and Patch H.M., 2015, Bee nutrition and floral resource restoration, Current Opinion in Insect Science, 10: 133-141.

https://doi.org/10.1016/j.cois.2015.05.008

Vijayakumari N., Saravanan P. A., Chitra N., and Rajendran L., 2022, Effect of supplementary sugar feeding on colony growth of Asiatic hive bee, Apis cerana indica F., Journal of Applied and Natural Science, 14(SI): 220. 

https://doi.org/10.31018/jans.v14isi.3612