Definition and Identification of Honey Bee Welfare Practices Within the Five Domains Framework for Sustainable Beekeeping

Featured Application

The main applications of this article include integrating Honey Bee Welfare Practices (HBWPs) into beekeeper training programs, developing sustainability policies and standards, creating technological monitoring tools, conducting welfare audits, fostering environmental partnerships, and supporting ongoing research, promoting a sustainable impact aligned with the One Welfare framework.

Abstract

This paper aims to define and identify the Honey Bee Welfare Practices (HBWPs) that beekeepers should adopt within a modern framework for sustainable apiculture. Once identified, HBWPs were categorized according to the Five Domains Model used in other animal species. Drawing on findings of the European BPRACTICES Horizon 2020 project, we identified, for the first time, 243 HBWPs: while all practices were considered impacting the mental state domain, 38 were assigned to nutrition/hydration, 90 to environment, 220 to health, and 50 to behavior. The proposed HBWPs aim to fill existing gaps by introducing a new approach that more fully respects honey bee behavior and helps prevent unnecessary suffering for each bee and the whole beehive at the same time. Future efforts should focus on maximizing welfare benefits within the One Welfare framework, moving beyond the previously considered One Health perspective. This welfare-oriented focus benefits honey bees, supports beekeepers, and promotes environmental sustainability, aligning with the principles of One Welfare.

1. Introduction

The welfare of honey bees (Apis mellifera) has received significant attention due to their crucial roles in agroecosystems, such as pollination, serving as bioindicators, producing hive products, and their use in Api tourism and apitherapy [1,2,3,4,5,6,7,8]. Food production is heavily reliant on bees, as more than 80% of plants are pollinated by honeybees, and some plants cannot reproduce without their pollination. Additionally, the well-being of bees is directly linked to improved honey production, highlighting the importance of maintaining their health [1,2,3,4,5,6,7,8].

Bee welfare is an important topic for both the ecosystem and the economy, as bees are essential for pollinating many cultivated and wild plants. Bee welfare refers to maintaining optimal conditions for their health and survival requiring sustainable beekeeping management practices [9]. In fact, sustainable beekeeping refers to the implementation of bee-friendly practices aimed at addressing the various threats to honeybee health, including pests, predators, chemicals, inadequate management practices, climate change, and other stressors. This involves a holistic approach that extends beyond the apiary, considering the surrounding environment and all relevant stakeholders. This approach prioritizes the long-term health and well-being of bee colonies, ensuring their resilience and productivity while promoting ecological balance and sustainability in beekeeping practices [10].

Several factors affect bee welfare, mainly nutritional stress, loss of habitat, climatic changes, improper use of PPPs (phytosanitary products), diseases and wrong management.

In terms of nutrition, bees require a diverse diet to maintain optimal health. However, this is increasingly threatened by habitat loss. Urbanization, deforestation, and intensive agricultural practices contribute to the loss of natural habitats, limiting bees’ access to essential food and water sources and shelter [10]. Monoculture practices and insufficient floral diversity can lead to malnutrition, weakening honey bee resilience to diseases and environmental stressors [11]. Climate change, characterized by shifts in temperature patterns and irregular precipitation, disrupts the availability of forage and affects bees’ ability to pollinate and survive seasonal transitions, thereby disturbing their life cycles [12,13]. The improper use of certain PPPs, particularly neonicotinoids, has been shown to negatively affect bees by disrupting their nervous systems, impairing navigation and reproduction, and increasing mortality rates [14,15]. Bee colonies are also highly susceptible to parasites, such as the Varroa destructor mite, and pathogens, including Nosema and various viruses, which together contribute to significant colony declines and collapse [16]. Finally, effective hive management, which includes the control of diseases and parasites as well as providing supplemental feeding during critical periods, is crucial to maintaining the health and productivity of bee colonies [14,15]. As challenges facing bee populations continue to grow, it is crucial to adopt comprehensive approaches to ensure their health and welfare, guiding beekeepers in their activities through the application of Good Beekeeping Practices (GBPs) and Biosecurity Measures in Beekeeping (BMBs).

Rivera Gomis et al. described GBPs as “all the integrative activities that beekeepers apply in on-apiary production to ensure optimal health for humans, honey bees, and the environment” [17,18]. Additionally, Pietropaoli et al. defined BMBs as “all operational activities to reduce the risk of introduction and/or spread of specific honey bee disease agents” [18]. This definition follows valuable models, such as the traditional One Health approach; however, a shift toward more holistic and modern frameworks, such as One Welfare, that describes the interconnection between animal welfare, human well-being and their physical and social environment as important elements to consider in the elaboration and implementation of policies and activities related to each of these aspects, became necessary [19,20,21]. In this approach, a balanced compromise between honey bees, humans, and environmental well-being is recognized as fundamental [7,19,20].

Although there is no consensus within the scientific community on insect consciousness [13], the precautionary principle assumes that all animals, including honey bees, are sentient and capable of experiencing suffering and emotions [21]. This view has recently been reinforced by the New York Declaration of Consciousness, which acknowledges the realistic possibility of honey bee consciousness and emotional capacities [22] and the need to grant honey bee welfare in beekeeping. The concept of Honey Bee Welfare (HBW) was first defined by Garrido and Nanetti in 2019. They described the welfare of managed honey bees as maintaining “the most natural condition possible”, while considering all potential threats to honey bees. Although this definition is valuable, it lacks a positive application of welfare principles for bee life improvements and does not consider the individual experiences of bees or the precautionary principle. We amplified the honey bee welfare concept and defined reared honey bee welfare as “a balanced and dynamic state, as natural as possible, in which the beehive superorganism and each individual bee have the freedom to express their roles and preferences, meet their fundamental needs, and adapt positively to external stressors without experiencing unnecessary suffering”.

This definition aligns with current welfare models used for other livestock species, particularly the Five Domains Model [23].

In major livestock species, animal welfare science has significantly improved our understanding of animal welfare. Welfare is assessed by utilizing multiple indicators to measure various aspects of well-being [23]. In particular, the Five Domains Model for animal welfare is currently used across different animal sectors. The model emphasizes the significance of both negative and positive emotions and offers a structured and comprehensive approach to evaluating and improving welfare [24]. The Five Domains Model evaluates the animal’s well-being across five key areas: nutrition, environment, health, behavior, and mental state [25]. The latter illustrates the impact of the first four domains on the animal. For instance, the scarcity of food, which affects the nutrition domain, is reflected in the mental domain as a state of ‘hunger’, representing the animal’s subjective experience (or feeling) of the event [23,24,26]. In fact, this model considers both, physical and emotional state, and their interconnections [25,27,28,29,30,31]. Although the Five Domains Model has not yet been applied to beekeeping, it can offer a structure to facilitate the implementation of targeted welfare practices in this field [25]. Considerations of honey bee mental state are supported by the recognition of their sentience and by the recent New York Declaration [22]. Honey bee mental state can be assessed by observing the colony’s response to stimuli, treating the superorganism as an individual entity, just as one would consider a single bee.

In this paper, we established the first definition of HBWPs and applied the Five Domains Model to categorize practices that support not only honey bee survival and productivity but also their overall welfare, along with benefits for humans and the environment, thereby promoting a more sustainable, welfare-oriented approach to modern beekeeping.

2. Materials and Methods

In the present study, after defining and listing the HBWPs, we categorized them according to the existing literature about relevant topics for honey bee Welfare, such as the Five Domains Model, sustainable beekeeping practices, and scientifically validated approaches. To list the practices, we referred to the One Health approach, used to identify the 140 GBPs [32] and the 84 [18] already validated through the European BPRACTICES Horizon 2020 project (https://www.izslt.it/bpractices/, accessed on 16 July 2024) in collaboration with European beekeepers, international federation of beekeepers association of APIMONDIA, and research Institutes. Additionally, we included previously unlisted practices to ensure comprehensive coverage of all aspects of honey bee welfare. These practices were identified through a detailed review of scientific literature and consultations with experts, with a particular focus on addressing honey bee behavior and minimizing suffering. The inclusion process also considered practices that could complement the existing validated ones to provide a holistic approach to honey bee welfare.

Regarding the headings of the practices, we adhered to those already established. The 140 Good Beekeeping Practices (GBPs) were organized into six categories [17]: general apiary management (including transportation, hygiene, bee health, apiary management, wintering, human health, and colony management), veterinary medicines, disease management, hygiene, animal feeding and watering, and record keeping [17]. In contrast, BMBs were organized under five headings corresponding to the main honey bee diseases in Europe [18]: Varroosis; American Foulbrood, European Foulbrood, Nosemosis and Aethinosis. Finally, we categorized the HBWPs according to the domains nutrition/hydration (N), environment (E), health (H), behavior (B), and mental domain (M) as usually performed for the other animal species. We also used bold characters to indicate the domain we considered to be most significantly affected compared to the others.

3. Results

Keeping in mind our functional approach of HBW [33], we defined HBWPs as “all those operational activities that aim to implement positively best living conditions for honey bees, pursuing optimal welfare for humans, animals and the environment”.

A total of 243 practices (see Annex) were classified as HBWPs, expanding on those previously identified in GBPs and BMBs within the BPRACTICES project. In addition, 28 new practices, primarily focused on preventing unnecessary suffering and addressing honey bee behaviors (Table 1), were introduced to ensure comprehensive coverage of honey bee welfare, as they had not been covered in the BPRACTICES project. Each practice was evaluated to confirm its alignment with the HBWP definition and to determine its corresponding domain (see Appendix A Table A1).

Table 1. New Honey Bee Welfare Practices identified.

Honey Bee Welfare Practices	Honey Bee Welfare Domain
1. Ensure that honey bees are housed under optimal physiological conditions, including temperature and humidity control	E/B/M
2. Locate the hive in a biodiverse area with a variety of melliferous and nectareous plants, as well as bushes that provide natural foraging and swarming opportunities for honey bees	E/B/N/H/M
3. Locate the hive avoiding light pollution, and excessive vibrations	E/H/N/M
4. Locate the hives avoiding excessive chemical pollution PPPs	E/H/N/M
5. Maintain appropriate distances between different apiaries	H/E/N/B/M
6. Ensure proper hive density per area	H/E/B/M
7. Prefer to place apiaries at a lower height than the foraging area, allowing foragers carrying nectar and pollen to return to their hive without fatigue	E/M
8. During transport, ensure that bees are exposed to minimal mechanical stress by scheduling stopovers to allow rest and recover	H/E/M
9. Prioritize gentle beekeeping practices during inspections preventing unnecessary suffering during inspections (e.g., by avoiding abrupt or sudden movements; using well-fitted latex gloves; lifting or moving combs/frames carefully; avoiding bee crushing, e.g., when closing the hive top, using the smoker properly)	H/B/M
10. Avoid rearranging the order of combs unless necessary	B/E/H/M
11. Avoid moving hives unless necessary	E/B/N/M
12. Do not open the hive at night or when it is rainy or windy	B/H/E/M
13. Breed your own autochthonous, locally adapted queens	E/H/B/M
14. Be cautious when handling the queen (e.g., avoiding damaging her or displacing her outside the hive)	H/B/M
15. Confine the queen in a way that allows her to move freely and lay eggs	B/H/M
16. Do not replace the queen	H/B/M
17. Explore alternative methods for identifying the queen without marking her with metal disks or painting her thorax	H/B/M
18. Do not perform artificial insemination	B/H/M
19. Do not perform genetic selection	B/H/M
20. Adopt effective techniques to control honey bee predators (such as wasps, bee-eaters, ants, rats, and bears)	H/E/B/M
21. Administer varroacide treatments using active ingredients that prioritize bee welfare, such as those with lower toxicity for honey bees	H/M
22. Do not perform drone brood removal	H/B/M
23. Monitor honey bee behaviors, including flight activity, noise levels, aggression, calmness, and other emotional states	B/H/M
24. If bees show signs of agitation, restlessness, or aggression, wait until they have calmed down before continuing with inspections	B/H/M
25. Respect the natural bee space between combs and remove any abnormal comb constructions	B/E/M
26. Encourage the natural construction of wax combs in the spring	B/E/M
27. Communicate with other stakeholders (e.g., beekeepers, farmers, advisors, veterinarians) in the area to coordinate actions for managing foraging resources	E/N/H/M
28. Attend personal training on One Welfare, with a focus on Honey Bee Welfare	B/E/H/N/M

N = nutrition; E = environment (inside and/or outside the hive); H = health; B = behavior; M = mental state. In bold is the main domain affected.

We adapted to honey bees the Five Domains, identifying challenges and opportunities concerning their welfare. The results are shown in Table 2.

Table 2. A description of the Five Domains Model, adapted to managed honey bees (Harvey et al. [13], modified).

DOMAIN 1                Nutrition/hydration Challenges: restricted feed, food and water intake; low feed, food and water quality. Opportunities: Sufficient and good quality of food, feed and water, varied and preferred shapes, colours, smells.		DOMAIN 5 Mental state NEGATIVE Thirst, hunger, breathlessness, general (thermal, physical, etc.) discomfort, sickness, exhaustion, frustration, loneliness, isolation, lack of control or security, anxiety, fear, and pain. POSITIVE Rewarding engagement in exploration and foraging; general comfort (thermal, physical, etc.); calmness and liveliness.	HONEY BEE WELFARE STATUS
	➝
DOMAIN 2                Environment Challenges: Internal or external discomfort (housing): extreme heat or cold, lack of shade, extreme humidity, lack of internal space within the hive, challenging flying and foraging areas (e.g., physical obstacles, excessive distance from the hive, monoculture/non-melliferous plants, presence of competitors), or predatory threats (bears, birds, wasps, hornets, etc.); poor quality of air/soil/water; anthropogenic pollution (pesticides, electromagnetic fields). Opportunities: Internal or external comfort (housing): thermal comfort, adequate humidity, presence of shade, adequate space within the hive, variable underfoot substrate and terrain. Good location, orientation, and disposition. Painting hives in colors and shapes. Adequate ventilation during transport and when stationary; correct wintering.	➝
DOMAIN 3                   Health Challenges: Acute or chronic injury, poor health, poor fitness (e.g., queen quality, drone/queen fertility, productivity), and weakness (e.g., flight activity, colony). Opportunities: injury and disease-free, robust good health, good physical fitness.	➝
DOMAIN 4                   Behavior Challenges: Limited positive interactions and behavior (e.g., restriction of natural foraging and flights, wax building, defending, fanning, egg laying, mating); lack of enrichment. Opportunities: Ability to express natural behaviors (e.g., foraging, swarming, flying, building wax, defending, ventilating, laying eggs, mating) and to interact within a balanced social structure.	➝

After a detailed analysis of the 243 identified HBWPs, all practices were considered relevant to the mental state domain (M), 42 were assigned to the nutrition/hydration domain (N), 94 to the environment domain (E), 217 to the health domain (H), and 50 to the behavior domain (B) (Table 3). During the allocation, each HBWP could be assigned to more than one domain (Table 3).

Table 3. Honey Bee Welfare practices (HBWPs), an overview of the domain distribution.

Honey Bee Welfare Category	Number of Honey Bee Welfare Practices Idetified
Nutrition/Hydration (N)	40
Environment (E)	90
Health (H)	220
Behavior (B)	50
Mental state (M)	243

4. Discussion

The Five Domains Model, originally developed for vertebrates [34], has been adapted in the present work to the managed honey bees (Table 2).

Honey Bee (Apis mellifera) Welfare (HBW) includes the adoption of proper practices, named Honey Bee Welfare Practices (HBWPs), by the beekeeper. Starting from GBPs and BMBs already identified by in the EU project BPRACTICES, under the One Health approach [1,17,32,35,36,37,38,39,40], the proposed model evaluates both classic and emerging threats to honey bees, considering their belonging to the different welfare domains and their effects on small and large scales during stationary and migratory beekeeping practices.

The adoption of the Five Domains Model for honey bee welfare introduces a novel framework that extends beyond traditional beekeeping practices. This offers a more holistic perspective by addressing both the physiological and psychological needs of honey bees, while emphasizing not only the single bee, but even the superorganism response as the primary focus to which beekeeping practices should be adapted. Through the application of the One Welfare framework and the Five Domains Model, HBWPs encompassed all aspects of managed bee life. This includes the health of the bees (by monitoring their health, preventing diseases, and ensuring responsible use of medications) along with their emotional well-being, which acknowledges the importance of honey bees’ mental states for optimal welfare (by minimizing negative emotions consequential to negative conditions of living and favoring positive emotions, such as contempt or calmness, with environmental enrichments). Environmental impact is also thoroughly considered, considering factors such as pollution, location, exposition, available space, food and water resources and stores (based on colony size), predators, and interactions with other animals and humans.

This approach encompasses previously underexplored aspects such as the bees’ mental state, their sufferance and their natural behaviors, acknowledging their importance in promoting not only the well-being of the colonies but also the sustainability of apiculture. Compared to those already considered by the B-PRACTICES project within the One-Health approach, the newly introduced welfare practices (28 in total) place special emphasis on honey bee physiology, behavior, and suffering. These practices aim to better recognize what is rewarding for honey bees, with the key objectives including alignment with the natural behaviors of Apis mellifera, promotion of gentle beekeeping, a reduction in unnecessary stress and suffering, and provision of environmental enrichment to enhance adaptability and choice.

For example, we discouraged the use of invasive techniques, such as queen artificial insemination and queen marking, as these practices strongly conflict with the bees’ natural behavioral expression and cause unnecessary suffering. In addition, by promoting the use of locally adapted bee populations and non-invasive management practices, we aim to preserve the genetic integrity and natural behavior of pure honeybee subspecies or races, ensuring their resilience and sustainability over time Moreover, when managing brood interruption, different beekeeping techniques can be compared, such as using trapped comb versus queen caging. Both techniques are effective in protecting bee health. However, in considering their impact on honey bee welfare, the method that allows the queen more freedom to exhibit her natural behavior should be favored. Similarly, additional behavioral considerations should be considered when evaluating practices such as drone brood removal, which is not permitted for bee welfare but is considered a good biosecurity measure against Varroa destructor. The use of local bee populations, which is requested for bee welfare to ensure autochthony, should also be prioritized as best as possible considering factors such as productivity, costs for the beekeeper, the difficulty to avoid hybrids, and honey production. In terms of environmental enrichment, we recommended the introduction of beehives in highly biodiverse areas with great numbers of melliferous and nectareous plants or selecting diverse foraging regions avoiding monocultures, areas with conventional agriculture density, or polluted environments in general, and we considered a balanced and rational use of supplementary feeding to be extremely important, advising its use only when necessary.

Additionally, we highlighted the need to prevent unnecessary bee mortality through more gentle management practices, such as using latex gloves to improve the beekeeper’s tactile sensitivity and avoid accidental bee crushing, applying bee culling with CO2 before hive destruction, and recognizing bee mental states by avoiding hive inspections when bees are extremely aggressive or irritable.

Furthermore, adopting this model and pursuing a positive welfare state could improve resilience to emerging threats, such as climate change, habitat loss, and pesticide exposure, which are increasingly affecting honey bee populations worldwide.

The integration of these additional practices into beekeeping management also has the potential to foster greater public awareness and support for honey bee conservation efforts.

Future research should aim on developing valid, reliable, and feasible indicators for assessing the effectiveness of these practices, enabling the evaluation of welfare conditions once they are implemented in the field. Such indicators could provide valuable data to further refine the HBWPs and help bridge any gaps between scientific recommendations and practical application in diverse environmental and cultural contexts. Continuous monitoring and feedback loops between researchers and practitioners will be essential to adapt these practices dynamically as new challenges arise.

Further validation, harmonization and scoring of HBWPs across different geographic contexts and types of beekeeping will require expert knowledge elicitation [41,42,43,44,45,46,47,48]. To ensure this process is multidisciplinary, and produces transparent and unbiased measures [26], it should involve not only beekeepers, apiculture experts, and beekeepers’ associations but also specialists from related fields of welfare science, such as veterinarians, biologists, ecologists, ethologists, and legislators.

Now that HBWPs for managed Apis mellifera are established, valuable tools can be developed to further enhance beekeeping management. These tools could include the creation of specific manuals, guidelines, and practical instructions for beekeepers and policymakers, as well as the development and the improvement of dedicated checklists for audits, official inspections, and self-assessment tools [6,7,42,48,49,50] All of these resources can be revised and refined based on the HBWPs already identified with the present paper.

Finally, to encourage adherence to these practices and promote compliance among beekeepers, dedicated labelling and marks, such as complementary or integrated organic production labels, can be introduced to certify good will, proper management and boost farmers’ income [51,52,53,54,55]. To encourage adherence to these practices and promote compliance among beekeepers, specific marks and labels, such as certification programs, could be introduced. Such certification would not only offer specific incentives for farmers [3,13,53,56,57,58], but also enhance consumer trust in the sustainability and welfare standards of beekeeping practices [51,53,54,55]. There are already established quality certification programs in animal husbandry that ensure animal welfare, and in Italy, the Classy Farm [46] integrated system is applying a similar approach to beekeeping, ensuring the welfare of honeybees within the broader framework of sustainable farming practices [45].

As consumers become more informed about the welfare standards behind hive products, their demand for ethically produced honey and other by-products is likely to increase, which could drive market preferences toward more sustainable beekeeping practices. In turn, this could incentive more beekeepers to adopt HBWPs, thereby creating a positive feedback loop that benefits both the bees, beekeepers, consumers, and the broader ecosystem services they support.

This approach to including welfare considerations in beekeeping represents a transformative step toward sustainable and modern apiculture. The new Honey Bee Welfare Practices prompt to intervene on long-term effects that proper beekeeping management have on ecosystems and biodiversity. Following a positive approach, they seek to minimize environmental impact and enrich bee life, offering opportunities for positive experiences while still reducing and controlling negative stressors. Moreover, they allow bees to choose their optimal conditions.

The holistic perspective framing these practices advocates for gentle beekeeping and recognizes the interconnectedness of humans, animals, and their environments to achieve optimal welfare conditions. As we highlighted with the HBWPs list, beekeepers can be guided to carry out these practices through specific training programs, peer discussions among beekeepers, collaboration with scientific authorities, and input from veterinary professionals.

Performing the above-mentioned new practices together with the previous one already identified, will empower both bees and beekeepers to make informed decisions regarding welfare options. This approach emphasizes that improving animal welfare directly benefits human welfare, and vice versa, and underscores the need for coordinated actions between veterinary and other services. Moreover, welfare considerations for honey bees highlight environmental protection as a fundamental step in safeguarding the well-being of both humans and animals [30]. An important challenge moving forward will be the development of practical strategies for implementing these practices on a large scale. This will require collaboration between researchers, practitioners, and policymakers to ensure that these practices are effectively integrated into beekeeping management and adapted to different regional contexts such as professional, and hobbyist beekeeping, organic beekeeping, propolis production, queen breeding, transport, and bee protection efforts. To achieve this, future research should involve the collaboration of beekeepers, ecologists, veterinarians, and policymakers, ensuring that HBWPs are validated, harmonized, and scored according to regional variations in beekeeping practices and environmental conditions.

HBWPs should be evaluated across diverse beekeeping contexts, engaging a wide range of stakeholders, and developing tools such as manuals and guidelines to support their effective implementation.

By evolving beyond a sole focus on production and adopting a multidisciplinary and comprehensive strategy, beekeeping practices can now aim for more resilient hives and thriving colonies. This shift aligns with the One Welfare concept, as it benefits not only the honey bees but also supports beekeepers and promotes environmental sustainability toward a modern concept of apiculture [1,8,23,25,27,29,30,31].

In conclusion, the HBWP approach offers a comprehensive framework for improving honey bee welfare by integrating scientifically validated practices into daily beekeeping operations. The adoption of HBWPs is particularly important for beekeepers, veterinarians, policymakers, and researchers, as it provides clear and actionable guidance for managing apiaries in ways that prioritize honey bee health, behavior, and overall well-being. Furthermore, the development of tools such as checklists, guidelines, and manuals can facilitate the assessment and implementation of these practices, enabling stakeholders to align farm management strategies with the HBWPs. This approach not only enhances the sustainability of apiculture but also strengthens its role in supporting broader environmental and societal goals.