Melissa A. Y. Oddie*
Bjørn Dahle- Norges Birøkterlag, Kløfta, Norway
Pollinator declines across the globe are centrally driven by a synergistic interaction between intensive land use, pesticides, and climate change. Competition between managed and wild pollinators has been a growing topic of research, however the ensuing social conflict builds antagonism between beekeepers and conservationists, two parties that have an interest in protecting natural diversity for pollinators. The threats perpetuating this potential for competition are as real for managed bees as wild species and uniting both groups, wherever possible, can create long lasting and meaningful change in current agricultural practices. This review examines the most recent literature on pollinator competition and the common threats that drive it. It also delves into the social elements of beekeeping and examines the potential for beekeepers to contribute to the protection of natural habitats. Beekeepers have a genuine interest to preserve natural space and with their charismatic species, dutiful observations, and innovative techniques, they can be valuable assets in filling knowledge gaps and generating public interest. Pollinator strategies in the future should include beekeepers as key stakeholders if their impacts are to be improved.
1 Introduction
Insect pollination is a vital service to both natural ecosystems and humans. At least 30% of the most nutritionally valuable crop yields produced for human consumption require insect pollinators (Klein et al., 2007; Eilers et al., 2011; Garibaldi et al., 2013; Rollin and Garibaldi, 2019). The dependence of human crops on pollination is increasing over time (Aizen et al., 2009) and plant-pollinator networks build a crucial base for the effectiveness of this ecosystem service (Kremen et al., 2004; Dainese et al., 2019). Managed pollinators, mostly managed honeybees (Apis mellifera), are tightly linked to this service in many human-mediated landscapes, now both in their native and non-native ranges (Rollin and Garibaldi, 2019). It has been well documented that pollinators are in global decline and in nearly all cases, the central driver is the intensification of land management (Kevan and Viana, 2003; Potts et al., 2010a; Burkle et al., 2013; Durant and Otto, 2019; Seibold et al., 2019; Dicks et al., 2021).
With increasingly limited natural resources, conflict between managed and wild pollinators becomes inevitable. Recently, there has been a research focus on identifying and assessing the potential for competition between wild pollinators managed bees (Mallinger et al., 2017; Wojcik et al., 2018). Likely this has come, at least partially, as a pushback against the misguided concept that honeybee conservation is a functional equivalent to species-level biodiversity conservation (Wilson et al., 2017; Geldmann and González-Varo, 2018). In their non-native ranges, managed species like honeybees kept at high densities, or large populations of escaped, feral bees can have severe impacts on local wildlife.
Though the risks of competition are evident, the social implications of this divisive stance splits two parties with a vested interest in protecting the same thing, namely, healthy environments for pollinators. The beekeeping industry has grown increasingly vulnerable in many areas due to its reliance on private and public land permissions. Shifting land use and conservation policy has created a more exclusionary environment which beekeepers must now navigate (Durant, 2019). As a result, many beekeepers have turned from small scale wild honey operations to large scale industrial honey or pollination services, that perpetuate unsustainable farming practices and make little room for wild space (Maderson, 2023b). Often, beekeeping cannot break away from agricultural landscapes, which are more exposed to threats that contribute to both pollinator decline and competition, making their presence and their plight more visible (Seibold et al., 2019).
This review explores the most current research on the underlying causes of competition and outlines the commonality between the threats that face both wild pollinators and kept honeybees in the Anthropocene. It also investigates the social elements that define the relationship between these threats and stakeholders and explores the role beekeepers have played as well as their future potential in insect conservation. The data presented here details the essential practicality of pooling the efforts of both beekeepers and conservation groups to improve conditions collectively for all pollinators in human-mediated landscapes.
2 Competition: when does it happen and why?
When species experience niche overlap, there is potential for competition. Exploitative competition decreases the fitness of at least one competitor group due to reduced access to a finite resource (Elton, 1946; Schoener, 1983; Abrams, 2022). The common belief is that a highly social, generalist pollinator like the honeybee, in high enough densities, can reduce the available nectar or pollen for wild pollinator species. This may often remove specialized resources for an already declining group of insects (Thomson, 2004; Cane and Tepedino, 2017; Wojcik et al., 2018; Rasmussen et al., 2021), or shift plant-pollinator interactions to affect the habitat as a whole (Valido et al., 2019). Honeybees also have the potential to spread pests and disease, and their large, tight-knit colony lifestyles creates opportunity for zoonotic shifts, which could lead to massive outbreaks in wild pollinator communities (Otterstatter and Thomson, 2008; Fürst et al., 2014; Goulson and Hughes, 2015; Mallinger et al., 2017). By human hands, honeybees have been moved to many places where they are not native. High domestic hive densities like those in the Americas (Geslin et al., 2017), as well as released, feral populations like those in Australasia (Prendergast, 2023; Pyke et al., 2023), have the potential to magnify the above-stated issues because of the sheer number of colonies present where they have never been before. Due to the increasing disappearance of key habitats, the ever-shifting use of harmful chemicals, climate change and invasive species, the effect of managed pollinators certainly has the potential to become damaging to local pollinator communities under the right circumstances (Brown and Paxton, 2009; Goulson et al., 2015; Brown et al., 2016; Baldock, 2020; Herrera, 2020; MacInnis et al., 2023).
Much of the current research on pollinator competition extrapolates potential risk from field observations but provides very little direct experimental evidence: The studies actively testing for impacts of honeybee-wild pollinator competition on fitness are surprisingly few, and relegated to handful of species, mostly bumblebees. Two recent reviews (Mallinger et al., 2017; Wojcik et al., 2018) investigated the number of papers on pollinator competition and pathogen spillover. In the field of competition, the first review examined 81 papers and found 19 that met their criteria for “direct impacts” on fitness, presenting experimental evidence and not only observational fluctuations in species abundance and richness based on proximity to honeybee hives or hive density. Of those 19, 10 found evidence of exploitative competition and 9 found no direct evidence. The second review found 38 out of 72 papers reporting negative effects of honeybees on wild pollinator foraging. Of the 27 papers investigating viral transmission, only 2 documented active transmission of viruses from honeybees to wild bees. An updated review (Iwasaki and Hogendoorn, 2022) found that the body of literature is increasing rapidly, growing by 47% since Mallinger et al. (2017), and the reporting of negative effects of competition has increased by about 13%, indicating a disproportionately slow growth of negative findings to the overall growth of the literature body. In short, there is little evidence that shows that the presence of honeybees has direct, negative impact on wild pollinator fitness, and likely, competition does not create easily measurable impacts in every instance of shared land.
Even with moderate rates of positive evidence, competition is inarguably a risk, and every case of honeybee presence must be considered as having the potential to impact wild pollinators negatively. There is much to be said for the precautionary principle in cases where honeybee competition with wild pollinators seems likely (Pyke, 1999). However, shifts in social perspective and the corresponding calls for policy change have been highly focused on mitigating the effects by restricting beekeeper access to often much-needed resources as a blanket strategy in all cases (Durant, 2019; Matsuzawa and Kohsaka, 2021). Efforts to mitigate the effects of competition may be more successful overall, if the focus was less on the damage from honeybees and more on the conditions under which that damage could occur. The largest underlying threats facing wild pollinators are very much the same threats facing honeybees. In this light, a growing body of research is being produced outlining the tight-knit similarities between the needs, problems, and solutions for all pollinators. Acknowledging beekeepers as fundamental stakeholders in the health of the natural environment plays well on two stages: scientifically beekeepers can offer much in their constant monitoring of a species that lives and thrives on natural biodiversity, and socially, beekeepers, their bees and their industry are charismatic bannermen for campaigns to involve the public in environmental challenges. If meaningful change is to occur for pollinators, all active players must be unified.
3 Common threats (and solutions)
3.1 Habitat loss
Habitat destruction is the most significant cause of biodiversity decline (Caro et al., 2022). Recent maps indicate an area of untouched “wild” land at just 25% across the globe (Allan et al., 2017). Additionally, species made vulnerable by the removal of needed habitat are much more susceptible to other threats like climate change and invasive species (Ganuza et al., 2022). Habitat loss is driven by the changing of land from a natural state to a state that provides food and other resources for human use (Tilman et al., 2017). Agricultural landscapes have historically been interlaced with natural and semi-natural habitats that were suitable for a large diversity of pollinators, but with the rapid increase in human population and general wealth, land is being handed to urbanization, farming practices are becoming more intense and this removes practical habitats that house many species (Shi et al., 2021). It is well-known that wild pollinators can only thrive if a suitable diversity of flowering plants is present in their environment. The issue lies in the area of land that is needed to maintain these natural landscapes. Stakeholders often see a loss of opportunity in natural landscapes, where they could instead be managed as more cropland (Kleijn et al., 2015; Montoya et al., 2020), and if pollinators are required, they can be purchased and fed with supplements (Noordyke and Ellis, 2021). The demand of pollination in today’s landscapes in many areas however, is rising faster than the increase in honeybee colonies (Potts et al., 2010b). Wild pollinators can augment the performance of managed bees and sometimes surpass it (Garibaldi et al., 2013; Monasterolo et al., 2022), and there is now clear evidence that restoring natural diversity in intensely-managed landscapes may be required for honeybees as well. Natural and semi-natural habitats can improve nutritional intake and provide diverse resources during times of food scarcity in predominantly monofloral environments.
3.1.1 Nutrition and stressor resistance
A large body of literature illustrates the link between poor nutritional intake and honeybee susceptibility to other external stressors (Naug, 2009). Poor nutrition can lead to higher instances of disease (DeGrandi-Hoffman and Chen, 2015; Branchiccela et al., 2019; Dolezal et al., 2019) and a greater susceptibility to environmental toxins (Tosi et al., 2017). Numerous studies now link the loss of natural and semi-natural habitats to poor nutritional health in honeybees: A US study found a strong correlation between the decrease in rangeland (grazed natural grasslands) and honeybee colony losses. States with the highest areas of natural land cover had a higher honey production per hive. This tells us that lands with more diverse resources improved overall colony survival, likely by providing a higher diversity and volume of pollen and nectar (Naug, 2009). Similar patterns were found recently in Canada (Richardson et al., 2023), and more diverse pollen collection, a key for good nutrition, was also linked to natural landscapes in Great Britain (Woodcock et al., 2022), France (Odoux et al., 2012) and Papua New Guinea (Cannizzaro et al., 2022). A wide variety of pollen can even work synergistically to improve honeybee health (Donkersley et al., 2017). Looking at the impacts on individual bees, a higher natural diversity can reduce microbial imbalances (Gorrochategui-Ortega et al., 2022) and improve the production of vitellogenin (Alaux et al., 2017), a protein that has been linked to better toxin processing (Barascou et al., 2021) and is crucial for winter survival in temperate climates (Amdam et al., 2005).
Access to a variety of different pollens plays a large role in many aspects of honeybee health (Di Pasquale et al., 2016), and not all roles are entirely understood, therefore replicating the needed diversity artificially through food substitutes may not serve as a good long term strategy.
In addition to maintaining preexisting diversity, restoring natural diversity in agricultural landscapes can increase the volume of food available: An experiment performed by Zhang et al. (2023) examining prairie strips in an agricultural landscape found that honeybees collected 50% more pollen and colonies were 24% larger at the end of season monitoring. Many of the resources in the strips were left uncollected, meaning there was the potential capacity to provide food for other species. This study offers direct evidence that replacing some natural diversity in highly managed agricultural landscapes can work to reduce nutritional stress in honeybees and possibly reduce competition with wild pollinators.
3.1.2 Temporal availability
Floral diversity in natural habitats can increase the availability of resources like pollen and nectar on a temporal scale too (Mallinger et al., 2016). A study in Western France examining the composition of collected pollen over time revealed that honeybees collected up to 40% of their pollen from weed species growing between the desired crop flowerings (Requier et al., 2015). Honeybees do not often use a high level of diversity at any given point in a season, but the types of resources collected in diverse environments changes significantly over time (Jones et al., 2022). Temporal shifts in floral availability are just as present in tropical climates as temperate (Souza et al., 2018), so consideration of temporal diversity in landscape management planning is as important as area coverage. Limiting this availability exposes honeybee colonies to greater risk of malnutrition or starvation and could increase competition at key points in a season.
3.1.3 Strategies for maximizing floral diversity in agricultural landscapes
There are many strategies being implemented to improve conditions for pollinators, including diverse cropping (planting more than one crop in an area: Martínez-Núñez et al., 2022), flower strips (narrow lengths of planted flowers in or around cropland: Scheper et al., 2015) and lower crop seed densities (Sidemo-Holm et al., 2021). However, it is natural floral diversity that stands out as the most effective resource for wild pollinator and honeybee health:
Studies have shown that though flower strips and semi-natural habitats provide similar resources, the pollinator diversity supported by semi-natural habitats is often superior (Morandin et al., 2007; Hevia et al., 2021; Hadrava et al., 2022). This means that natural and semi-natural habitats provide better resources for rare species. Choosing seed mixtures can be a complex affair when considering the effects they must have, and often, natural mixtures provide the best nutrition for pollinating species (Haaland et al., 2011). A combination then, of natural, semi-natural and floral strip habitats might offer the best spread of strategies to accommodate a variety of landscape assemblages.
Though the benefit of natural diversity in farming landscapes is generally accepted, there is a large gap in knowledge from an economic and social perspective on the direct benefits of these strategies to the farmers who produce crops (Uyttenbroeck et al., 2016). It is not known if these strategies produce enough incentive alone to employ them in all cases, and in many cases, subsidies are required to encourage their use. The fastest solution may currently involve interested stakeholders like beekeepers and conservation groups working together to make natural diversity a requirement in landscape planning and not only an option, as it often is (Durant, 2019; Pe’er et al., 2022).
3.2 Agrochemicals
Agrochemicals are essentially all chemicals used in agriculture, from fertilizers to pesticides that target a number of taxa and can have severe detrimental effects. Most current agrochemical application practices for the globalized agricultural sector are unsustainable (Weltin et al., 2018). Often these chemicals affect species and areas outside the intended and cause toxin buildup in the environment. This endangers organisms on all trophic levels and can eventually damage ecosystem services, food production and subsequently human health (Singh et al., 2018). The effects of many agrochemicals on pollinators are no different. Depending on the method and timing of application, these chemicals have the capacity to cause mass deaths and serious sublethal conditions for honeybees and wild pollinators alike (Woodcock et al., 2017; Holder et al., 2018; Fikadu, 2020).
Honeybees are often chosen as a model organism for assessing the toxicity levels of pesticides, however honeybees, due to their eusocial, large colony-nesting strategies are often more resistant to the effects, and not the best proxies for assessing the threats to wild pollinators (Franklin and Raine, 2019). Even other eusocial bees, like neotropical stingless bees, can suffer stronger effects than those measured in managed honeybees. Two studies found a much more profound effect of a combination of pesticides and fungicides on one species of stingless bee (Partamona helleri) than the tested A. mellifera (Tomé et al., 2017; Almeida et al., 2021). So, if a chemical is found to affect honeybees in a serous way, it may well affect many wild pollinator species more profoundly.
Methods of assessing the toxicity of agrochemicals often fall very short of the entire system of effect they can have on species in the field. Until recently, focus for assessment had generally been on the LD50: the concentration of the chemical that caused a 50% mortality rate in tested subjects (Trevan and Dale, 1927). This would be realistic if there were no other stressors posing challenges to pollinator health, but pesticides can affect learning and memory in foraging (Henry et al., 2012), reduce reproductive success (Sandrock et al., 2014; Woodcock et al., 2017), alter parasite loads (Evans et al., 2018; Schwartz et al., 2021), lower immunity (Pettis et al., 2013; Sánchez-Bayo et al., 2016), and cause changes to food webs and species assemblages in the ecosystems that pollinators require to sustain themselves (Tooker and Pearsons, 2021). In short, with all other challenges, both natural and man-made, pesticide effects can become synergistic with other threats to make “sublethal” effects very lethal indeed (Goulson et al., 2015; Siviter et al., 2021a).
3.2.1 Lack of knowledge in policymaking
Methods for successfully predicting pesticide exposure and the (not so) sub-lethal effects are still under development (Barmaz et al., 2010; Siviter et al., 2021b). Currently, many regulatory bodies are relying on the published results of independent studies and the hope that large-scale decision-makers will take the data into account when reworking policies. As of yet, there have been very few steps taken to include any species other than honeybees in most assessments (Siviter et al., 2021b).
Current EFSA guidelines for the risk assessment of plant protection products (PPPs) only have clear sublethal effect thresholds for honeybees, thresholds for wild pollinators remain ‘undefined’, due to insufficient data (Authority (EFSA) et al., 2023). Today, studies on the agrochemical effects on honeybees still dominate the literature at about 80% (Vanbergen, 2021; Dirilgen et al., 2023), and the majority of studies on other insects are focused on bumblebees, mason bees and leaf-cutter bees (Dirilgen et al., 2023). There are large gaps in the knowledge on the synergistic effects of pesticides and by this, policy makers may excuse non-committal opinions in favor of continued, intense agricultural production.
3.2.2 Strategies for minimizing the effects of agrochemicals on non-target systems
The growing global human population is increasing the demand on our agricultural systems (Noel et al., 2016), and land users often see the call for a reduction of agrochemicals as a threat to their productivity (Young et al., 2022; Argüelles and March, 2023). However, food production cannot persist outside the framework of stable ecosystems (Dudley and Alexander, 2017; Kopittke et al., 2019), and some reduction in the intensity of management to make way for that healthy framework may be necessary for the production to continue indefinitely.
Interestingly, pollinators themselves, both domestic and wild may provide an incentive to reduce the use of chemical pest control. One study found that by reducing pesticide use in oilseed rape fields, the subsequent increase in pollinator abundance raised crop yield to the point where it negated the cost of product loss from pest species, and cut production costs by reducing the volume of the purchased pest control chemicals (Catarino et al., 2019). Similar evidence was found when measuring wild pollinator abundance in watermelon fields in relation to a reduction in pesticide applications (Pecenka et al., 2021), increasing yield via improved pollination services beyond the crop loss from pests.
Knowing the unsustainability of current agrochemical applications in most countries and given the evidence that providing for pollinators can nullify the crop loss from pest species, governments must put a high value on farmers, crops and pollinators (both domestic and wild) and work to consider strategies beneficial to all groups.
Beekeepers have a stake in making the landscape more hospitable for pollinators, and beyond the use of their bees, their power of advocacy can be a formidable tool. As an example of policy change regarding agrochemicals in Europe, the three neonicotinoids Clothianidin, Thiamethoxam and Imidacloprid, which were where three of the most widely used pesticides at the time, were banned for outdoor use (EC, 2013), partly as a result of lobbying by beekeepers (Demortain, 2021). Beekeepers have a very keen awareness of how their bees fair in the environments they navigate, and honeybee potential as an ecological monitor, through the attentive beekeepers, may be a strong resource to provide some missing data for policymakers (Cunningham et al., 2022), keeping in mind the effects of these chemicals are likely more severe for any pollinator that is not a honeybee (Thompson and Pamminger, 2019).
Honeybees are often used as indicator species to measure the effects of agrochemicals like pesticides, however they are often not good representatives for the other insect species present in the systems. The increasing pressure on food production systems is pressing for a higher-level of chemical inputs, but this in turn, decreases the stability of the land processes required to grow food successfully. Now we are discovering that there may be alternatives to more intensive land management and using natural solutions, like reducing pesticides to encourage pollinators may prove just as profitable. Accounting for a trade-off between crop productivity and ecological sustainability, involving indirect stakeholders like beekeepers, and pushing for more research to close knowledge gaps should bring us closer to building an agricultural system that can coexist with natural diversity and continue safely into the future.
3.3 Climate change
Climate change is likely one of the most daunting yet seemingly vague threats facing the world. It is difficult to attribute real time events to a force that cannot be seen or measured except over long periods of time, however recent data have now illuminated the effects quite clearly.
Climate change is impacting global temperatures (Hansen et al., 2006; Seneviratne et al., 2006; Sun et al., 2014) and this is causing more frequent and more violent extreme weather events like droughts, floods, wildfires and storms (National Academies of Sciences, Engineering, and Medicine, 2016; Stott, 2016). The effects of these events and increasing temperatures pose problems for most life on earth, and makes current human problems, like taxing an already stressed food production system, harder (Brás et al., 2021).
3.3.1 The varying effects of climate change on pollinators
The effects of climate change on honeybees (both managed and feral) and on other wild and native bees will likely be similar. Extreme weather, for example, can limit forage, and in areas where habitat quality is already reduced (intensely managed landscapes) this could have serious impacts for food collection and nesting habitat (Goulson et al., 2015). Changing weather and temperature patterns can alter local assemblages and shift home ranges, hinder flowering phenology, and make way for invasive species (Parmesan, 2007; Schweiger et al., 2010; Duchenne et al., 2020). Wildlife, and to an extent honeybees, recover from extreme events by being recolonized from surrounding populations that were not affected (Macarthur and Wilson, 1967; Venturini et al., 2017), but reducing habitat patch size and increasing distance between those patches affects recolonization potential (Parmesan et al., 2000). This means there must be suitable habitat within reachable distance with which to support populations that will recolonize after a drastic disturbance (Vasiliev and Greenwood, 2021) created by climate change. Recolonization might be less problematic for domestic pollinators, that can be repopulated by human means, but decreasing the amount of suitable environment makes even honeybees weaker and more susceptible to other threats (Naug, 2009; Potts et al., 2010b). Data on the direct impacts of climate change on pollinators are scant (Decourtye et al., 2019). Many papers detailing potential effects rely on laboratory studies or theoretical modelling which, though insightful, is not a substitute for tangible evidence (Forrest, 2017; Giannini et al., 2017; Hannah et al., 2017).
Despite this lack of concrete knowledge, there are strategies providing necessary data. The effects of climate change, though difficult to predict, are very measurable in their impacts.
3.3.2 Strategies for mitigating the effects of climate change for pollinators
Because it is so hard to measure, and studies that capture discernible effects must be long term and include many samples, there simply is not a large amount of conclusive field data detailing climate change effects on pollinators. The problem then, is one of time and work force. Beekeepers often make excellent watch dogs for the effects of extreme weather. For example, professional beekeepers in Italy retained good records and offered insight into the changes of nectar amount and type in tandem with the weather from year to year (Vercelli et al., 2021). These data might be useful as a proxy for floral abundances of significant resources for pollinators in the environment and could be valuable data to inform policy makers on climate change mitigation strategies. The fact is, much of a beekeeper’s data is empirical, they are highly motivated, and with a small amount of training, many can provide high quality data for long term monitoring projects (Maderson and Wynne-Jones, 2016; Gratzer and Brodschneider, 2021).
To directly mitigate the impacts of climate change, restoring natural habitat can be a viable option. A recent global study concluded that insect biodiversity benefitted directly from more natural habitat in the area, reducing the synergistic impact of climate change and landscape degradation, though the amount of natural habitat needed was great (Outhwaite et al., 2022). A less intense strategy for agriculture could permit a large amount of natural diversity to persist interlaced with needed cropland, and indeed, multiple studies have found that smaller, more diverse crop spaces increase biodiversity and landscape connectivity with minimal losses to productivity by area (Dudley and Alexander, 2017; Tscharntke et al., 2021).
On a local scale, native plants can be more drought resistant than monoculture crops, and a high enough diversity makes sure there are more floral resources that can tolerate varying conditions. Honeybees in Iowa, when given access to natural resources during times of drought switched from their main source of pollen at the time (clover, Trifolium spp), which was much less abundant, to a small variety of natural prairie species and the amount of pollen collected was statistically comparable to other years (Zhang et al., 2022), effectively mitigating a climate-induced forage dearth.
To bring it together: Direct measures to mitigate the effects of climate change, apart from reducing greenhouse gases, lie most prominently in doing what we can to restore natural habitat and reduce the intensity of management in affected landscapes, while also protecting the natural diversity that remains. More data on the effects of climate change would help drive decisions, and beekeepers might offer the efficient and long-term information collection that could help obtain it. Beekeepers have a keen understanding of the importance of natural diversity, and they can provide a force for conservation that is both insightful and passionate. Ultimately, beekeepers have much to offer in the battle for biodiversity.
4 Beekeepers in conservation
Beekeepers have a vested interest in protecting resources for their bees, and this ultimately includes resources for wild pollinators as well. There has recently been significant dialogue on whether or not honeybees fall under the category of “pollinators that need conserving” (Geldmann and González-Varo, 2018; Kleijn et al., 2018; Saunders et al., 2018; Alaux et al., 2019). Arguably, they are managed in most cases, their survival is aided, their numbers bolstered beyond natural limits, or, they are non-native to where they occur. In addition, many projects promoting beekeeping have been pedaled as efforts to increase biodiversity, but this claim is false (Colla and MacIvor, 2017). Outside of wild honeybee colonies in their natural ranges, the conservation of honeybees does very little to aid other species directly.
In terms of practical solutions for habitat loss, the discourse on whether honeybees should be the targets of conservation is irrelevant. Resources required by honeybees and wild pollinators overlap enough that the commonality can be exploited, as ultimately it is not the species that should be the focus in many cases, but the habitats they need to live.
Negatively targeting beekeepers in the effort to preserve wild pollinators alienates an industry that has the most to gain by aligning with them. The repercussions of being restricted from forage for the sake of conservation may be effective in some cases, and short term, but the longstanding, widespread consequences might be that beekeepers seek a sustainable profit in other areas, like industrial scale commercial pollination, and end up supporting a practice even more hostile to the preservation of natural space (Maderson, 2023b). The effects of competition, even those highlighted in the vying for policy attention, can be effectively mitigated in many cases if efforts are combined by these two passionate sides to preserve natural ecosystems in our changing landscapes. Resources must be considered common between both parties and equally protected by both. Wild pollinator conservation groups and the beekeeping industry have unique resources to lend to this cause, and they complement each other in ways that could be synergistic in solving the common problems outlined at length in previous sections.
4.1 Lessons from developing countries: value creation for intact natural habitat
Compared to the West, the story of pollinator conservation in Africa and Southeast Asia includes beekeeping, it being adopted to generate a sustainable income for those who would otherwise depend on trades that are damaging to natural landscapes (Kassa Degu and Regasa Megerssa, 2020; Harianja et al., 2023). Many countries like Ethiopia, Kenya, Tanzania Uganda, India, Indonesia, and Nepal have created conservation programs that center around managing honey-producing bees. The strategy is to generate value in intact natural landscapes and restore disturbed habitats by promoting an industry that can harvest resources with minimal impact on ecosystem function (Wagner et al., 2019; Bareke et al., 2022). As a result, the people who practice beekeeping have gained economic benefits (Kadigi et al., 2021) and are more aware of factors affecting the health of their forests and surrounding land. Some projects have found that beekeepers are active drivers in restoring and protecting local diversity (Sialuk, 2014). Though restricted resources and difficulties in developing appropriate training programs hinder success, observers are optimistic about the potential of this strategy to eventually safeguard natural space (Wagner et al., 2019; Ghode, 2022).
The circumstances surrounding rural communities in developing countries obviously differ from many issues present in places like Europe and North America, however working to create economic value in intact natural landscapes offers an additional level of protection and a new cohort of people ready to defend them. Beekeeping raises conservation awareness wherever it has been measured, and beekeepers have a lot to give in the push for better pollinator conservation (Maderson and Wynne-Jones, 2016).
4.2 Beekeeper drive and public motivation
Applying a monetary value to natural diversity is a solid conservation strategy, but beekeepers’ understanding of its real value goes beyond money. A study done in Massachusetts found that beekeepers are more aware of conservation issues than the general public, and more willing to engage actively in pollinator conservation beyond their own bees (DiDonato and Gareau, 2022). Another study found that some beekeepers can be more willing to work for and pay for the conservation of wild pollinators (Penn et al., 2019). These findings are understandable when considering the day-to-day of a beekeeper and their livestock. Beekeepers, especially commercial beekeepers, live the threats to biodiversity every day, because they are often the same threats that affect their own livelihoods. This would not apply to all beekeepers, however, the awareness and incentives are present enough as to consider the beekeeping community as a valuable resource in the endeavor of preserving natural landscapes.
One of the most common reasons given by people starting a hobby beekeeping business is to aid in conserving natural diversity (Duarte Alonso et al., 2021). Beekeeping is used to raise environmental awareness, promote local identity (regional honey) and reignite an interest in traditional and low-impact farming practices (Kohsaka et al., 2017; Cho and Lee, 2018). Though there are apparent misunderstandings of the real impact of honeybees on natural diversity, the willingness to be part of the solution is irrefutably present (Lorenz and Stark, 2015; Duarte Alonso et al., 2021). So, hobby beekeepers want to help, and potentially focusing on environmental education for this particular group of stakeholders may be an easy method to engage them in impactful solutions.
Another possible way beekeepers might influence changes in agricultural strategies is by indirect contact, engaging with crop-based farmers that rely on pollination services for productivity. Studies investigating farmer perception on pollinator declines and supporting management strategies found that knowledge of the threats and the willingness to enact change was related to on-farm experiences and age (Bloom et al., 2021) rather than their use of managed pollinators, and was also linked to their level of knowledge on the subject (Osterman et al., 2021). Still, no studies were found on the perception of crop farmers on the topic of pollinator conservation and their level of engagement with beekeepers, so the possibility exists that beekeepers may well be able to interact as intermediaries between farmers and wild pollinator conservation strategies, providing education to crop farmers by simple interaction.
Ultimately, be it commercial beekeeper, hobby beekeeper or non-beekeeper, there is a great deal of human love for the honeybee both in and outside of beekeeping circles; they have been consistent and valuable partners for millennia (Prendergast et al., 2021). We have many reasons to look on honeybees favorably. They are pollinating allies that make us food, provide sweet treats, and draw us in with their complex social behavior that is easily related to our own societies: Honeybees work together, they care for their young and they dance.
When looking at media representation, honeybees receive much more attention than wild pollinators (Smith and Saunders, 2016; van Vierssen Trip et al., 2020). This has been seen by conservationists as part of the problem as honeybees are the least threatened pollinator globally (Iwasaki and Hogendoorn, 2021), but it can also be seen as part of the solution.
A flagship species is defined as a charismatic species that draws the attention and sympathy of the public to raise awareness and action for a specific cause (Jepson and Barua, 2015). In many countries it is part of our cultural upbringing to be aware of honeybees and what they do. The awareness of the plight of the pollinators is growing around the world (Hall and Martins, 2020), and within that, our practical and emotional connections to the honeybee creates a drive that galvanizes many people to take action (Schönfelder and Bogner, 2017). A fantastic example of this was presented during the debate which ended in a Europe-wide ban of the three damaging neonicotinoid pesticides. The public cry “Save the bees” is still well-known to this day (Demortain, 2021). There is a pitfall to be avoided here however, and strategies must be careful to use honeybees to draw attention but build the focus of conservation around needed habitats and not the honeybees themselves (Basset and Lamarre, 2019). If properly harnessed with structured outreach and education (elements that honeybees already contribute to), our collective love for honeybees could be one of the central public drivers to sway policy in favor of more sustainable practices and protect natural habitats for all pollinators.
4.3 For science: practical contributions of beekeepers and their bees
Both beekeepers and their bees have a large potential to contribute practically to conservation projects. Honeybees may not be the most sensitive bioindicators, nesting in large numbers and using a suite of effective eusocial behaviors to reduce stressors at the individual level (Franklin and Raine, 2019), however they are abundant, easily managed, respond predictably to their environment, their data can be standardized across large areas, and they come with their own passionate people who are already collecting their data (Quigley et al., 2019; Cunningham et al., 2022). Honeybees will not be able to provide all data needed for informed decision-making on pollinator conservation, but in situations where large amounts of similar data are needed on a multi-regional scale, they may be one of the best options for scientists to use.
This is an example of how beekeepers can contribute to scientific knowledge. Scientific knowledge is one of the most reliable types of knowledge, using strict, repeatable methods and numerical quantification to form conclusions. However, it is expensive, time-consuming, and very limited due to restricted funding. If practical solutions are to be found for issues like the growing decline of insect pollinators, other types of knowledge must be included and taken seriously, knowledges like the practical and experiential knowledges of people who keep bees for a living. Oftentimes issue is taken with incorporating the knowledge of laymen because it is not considered as well-collected or based in concrete scientific understanding and therefore, is not as valuable (Maderson, 2023b, 2023a). However traditional and lay knowledges have the benefit of direct, long term experience with the systems under study, a different lens that can add much-needed insight to solving on-the-ground problems (Maderson and Wynne-Jones, 2016).
A hard truth is that scientists often do not obtain sufficient funding to complete the tasks that would supply all the information needed for solid policymaking. Citizen science is defined as a collection of volunteers that participate in data collection for scientific studies (Cohn, 2008). It requires an interest in the subject and a consistent time commitment from the participants. Today we have an extensive list of tools to train and employ large numbers of dedicated volunteers in science monitoring projects. The fact that almost everyone on the planet now carries a smartphone, effectively a small computer, has made the idea of citizen science all the more practical. Combine these tools with the expertise, passion, and keen observational skills of a beekeeper, and you are likely to get data that rival the fastidious detail found in the scientific community.
Several studies have now been published using the data collected by beekeepers on their honeybees: some to assess pollen availability and the use of forage plants by honeybees over the active season (Brodschneider et al., 2019), others to examine the field levels of pesticides (Woodcock et al., 2022) or heavy metals (Shaw et al., 2023). These studies identified seasonal declines in pollen diversity, successfully linked foliar insecticides to an increase in disease, and monitored levels of several heavy metals present in an environment.
In addition to participating in data collection, beekeepers have been shown to contribute to the design of novel data collection tools. They optimized methods to align with their capabilities, identified pitfalls and streamlined the collection plans when set to the task of improving technologies (Phillips et al., 2013). Beekeepers are natural innovators and are often willing to lend their expertise to improving projects when invited.
Citizen science offers an address to the problem of resources for scientific studies, and involving beekeepers in science is, in itself, a form of outreach and education. One of the central issues around pollinator declines is a lack of understanding of the core elements of the issue, both by the public and some beekeepers. Involving these key stakeholders in scientific solutions and data collection can provide the education missing in many of the stakeholder groups that have been historically excluded from direct scientific findings (Vohland et al., 2021).
In the end too, creating strategies around people is usually the most long-lasting form of conservation, as it creates value for the communities using these systems, includes them as stakeholders in solutions and ensures that effects can be intergenerational, building local culture around sustainable principles and allowing an internalization of core practices.
5 Conclusion
In the end, honeybees do not contribute directly to improving the environment for wild pollinators, and in some cases, can be detrimental, but this does not mean that beekeepers are, by default, antagonists to conservation. Managed honeybees, like wild pollinators, stand to lose a considerable amount of stability with the reduction of natural and semi-natural habitats, and without sufficient natural diversity in the landscape, competition between the two species groups is inevitable. Competition dynamics have the potential to cause both great harm to natural systems and threaten to restrict the land beekeepers depend on for their livelihoods. The effects of land use intensification can combine with other threats like climate change and competition to exacerbate conditions and magnify problems, and it is only in the direct mitigation of these larger threats that broadscale solutions can be found. The literature body is growing however, knowledge is still lacking in key areas and this allows policymakers to sidestep meaningful action.
Beekeepers have a good deal to offer in needed data collection and the development of strategies to mitigate habitat loss. For example, they are the bannermen that generate public interest for pollinators, and the honeybees they keep are charismatic flagships. Beekeepers are present on the ground for many direct changes and can offer pinpointed local information as well as largescale, long-term data that can aid in policymaking. With precise education, training and guidance, beekeepers can harness their interest and passion and the weight of their industry to afford better protections for natural lands and push for more sustainable agriculture.
It would be a powerful combination to arm beekeepers with the factual knowledge of conservation and channel their endeavors into a collective effort to protect all pollinators. The beekeeping industry is one that closely aligns with the goals of sustainable agriculture due to their livestock’s dependency on natural diversity for good health. Honeybees and beekeepers, in the context of human-mediated landscapes could be said to have a symbiotic relationship with wild pollinator groups in the context of their mutual need for wild space and the drive of the domestic bee industry to create a sustainable future for itself. A collaborative, unified effort between beekeepers and wild pollinator advocates will provide a louder voice when pushing for policy improvements regarding the preservation of natural habitats. Both groups standing together may serve as a needed example on how our agricultural systems in their entirety could benefit from taking the needs of the natural environment into account.
There must be a push to understand the underlying causes of competition, and education for both beekeepers and other farmers will be needed to deepen knowledge and understanding of the issues surrounding it. Like the Three Musketeers, beekeepers and wild pollinator conservationists must rally together and unite their efforts. Involving beekeepers in decision-making, acknowledging them as key stakeholders and keepers of valuable knowledge, and promoting their potential to be part of the solution is the only way to create long-lasting and self-perpetuating change directly in the environments that must be conserved, both for wild pollinators and for our bees.
Author contributions
MO: Conceptualization, Data curation, Funding acquisition, Project administration, Resources, Validation, Visualization, Writing – original draft, Writing – review & editing. BD: Writing – review & editing.
Funding
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. Funding provided to Melissa Oddie by The Research Council of Norway. 331662 -IPNAERINGSLIV21 Innovation Project for the Industrial Sector.
Acknowledgments
The authors would like to thank Professor Graham Pyke for his thorough review of the manuscript.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Abrams P. A. (2022). Competition Theory in Ecology (Oxford, United Kingdom: Oxford University Press). doi: 10.1093/oso/9780192895523.001.0001
Aizen M. A., Garibaldi L. A., Cunningham S. A., Klein A. M. (2009). How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 103, 1579–1588. doi: 10.1093/aob/mcp076
Alaux C., Allier F., Decourtye A., Odoux J.-F., Tamic T., Chabirand M., et al. (2017). A ‘Landscape physiology’ approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats. Sci. Rep. 7, 40568. doi: 10.1038/srep40568
Alaux C., Le Conte Y., Decourtye A. (2019). Pitting wild bees against managed honey bees in their native range, a losing strategy for the conservation of honey bee biodiversity. Front. Ecol. Evol. 7. doi: 10.3389/fevo.2019.00060
Allan J. R., Venter O., Watson J. E. M. (2017). Temporally inter-comparable maps of terrestrial wilderness and the Last of the Wild. Sci. Data 4, 170187. doi: 10.1038/sdata.2017.187
Almeida C. H. S., Haddi K., Toledo P. F. S., Rezende S. M., Santana W. C., Guedes R. N. C., et al. (2021). Sublethal agrochemical exposures can alter honey bees’ and Neotropical stingless bees’ color preferences, respiration rates, and locomotory responses. Sci. Total Environ. 779, 146432. doi: 10.1016/j.scitotenv.2021.146432
Amdam G. V., Norberg K., Omholt S. W., Kryger P., Lourenço A. P., Bitondi M. M. G., et al. (2005). Higher vitellogenin concentrations in honey bee workers may be an adaptation to life in temperate climates. Insect Soc 52, 316–319. doi: 10.1007/s00040-005-0812-2
Argüelles L., March H. (2023). A relational approach to pesticide use: Farmers, herbicides, nutsedge, and the weedy path to pesticide use reduction objectives. J. Rural Stud. 101, 103046. doi: 10.1016/j.jrurstud.2023.103046
Authority (EFSA), E. F. S, Adriaanse P., Arce A., Focks A., Ingels B., Jölli D., et al. (2023). Revised guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 21, e07989. doi: 10.2903/j.efsa.2023.7989
Baldock K. C. (2020). Opportunities and threats for pollinator conservation in global towns and cities. Curr. Opin. Insect Sci. 38, 63–71. doi: 10.1016/j.cois.2020.01.006
Barascou L., Sene D., Barraud A., Michez D., Lefebvre V., Medrzycki P., et al. (2021). Pollen nutrition fosters honeybee tolerance to pesticides. R. Soc. Open Sci. 8, 210818. doi: 10.1098/rsos.210818
Bareke T., Gemeda M., Kumsa T., Addi A., Endale W. (2022). Beekeeping as an incentive to catchment rehabilitation. Int. J. Environ. Stud. 79, 613–623. doi: 10.1080/00207233.2021.1940533
Barmaz S., Potts S. G., Vighi M. (2010). A novel method for assessing risks to pollinators from plant protection products using honeybees as a model species. Ecotoxicology 19, 1347–1359. doi: 10.1007/s10646-010-0521-0
Basset Y., Lamarre G. P. A. (2019). Toward a world that values insects. Science 364, 1230–1231. doi: 10.1126/science.aaw7071
Bloom E. H., Bauer D. M., Kaminski A., Kaplan I., Szendrei Z. (2021). Socioecological factors and farmer perceptions impacting pesticide use and pollinator conservation on cucurbit farms. Front. Sustain. Food Syst. 5. doi: 10.3389/fsufs.2021.672981
Branchiccela B., Castelli L., Corona M., Díaz-Cetti S., Invernizzi C., Martínez de la Escalera G., et al. (2019). Impact of nutritional stress on the honeybee colony health. Sci. Rep. 9, 10156. doi: 10.1038/s41598-019-46453-9
Brás T. A., Seixas J., Carvalhais N., Jägermeyr J. (2021). Severity of drought and heatwave crop losses tripled over the last five decades in Europe. Environ. Res. Lett. 16, 065012. doi: 10.1088/1748-9326/abf004
Brodschneider R., Gratzer K., Kalcher-Sommersguter E., Heigl H., Auer W., Moosbeckhofer R., et al. (2019). A citizen science supported study on seasonal diversity and monoflorality of pollen collected by honey bees in Austria. Sci. Rep. 9, 16633. doi: 10.1038/s41598-019-53016-5
Brown M. J. F., Dicks L. V., Paxton R. J., Baldock K. C. R., Barron A. B., Chauzat M.-P., et al. (2016). A horizon scan of future threats and opportunities for pollinators and pollination. PeerJ 4, e2249. doi: 10.7717/peerj.2249
Brown M. J. F., Paxton R. J. (2009). The conservation of bees: a global perspective. Apidologie 40, 410–416. doi: 10.1051/apido/2009019
Burkle L. A., Marlin J. C., Knight T. M. (2013). Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339, 1611–1615. doi: 10.1126/science.1232728
Cane J. H., Tepedino V. J. (2017). Gauging the effect of honey bee pollen collection on native bee communities. Conserv. Lett. 10, 205–210. doi: 10.1111/conl.12263
Cannizzaro C., Keller A., Wilson R. S., Elliott B., Newis R., Ovah R., et al. (2022). Forest landscapes increase diversity of honeybee diets in the tropics. For. Ecol. Manage. 504, 119869. doi: 10.1016/j.foreco.2021.119869
Caro T., Rowe Z., Berger J., Wholey P., Dobson A. (2022). An inconvenient misconception: Climate change is not the principal driver of biodiversity loss. Conserv. Lett. 15, e12868. doi: 10.1111/conl.12868
Catarino R., Bretagnolle V., Perrot T., Vialloux F., Gaba S. (2019). Bee pollination outperforms pesticides for oilseed crop production and profitability. Proc. R. Soc. B: Biol. Sci. 286, 20191550. doi: 10.1098/rspb.2019.1550
Cho Y., Lee D. (2018). ‘Love honey, hate honey bees’: reviving biophilia of elementary school students through environmental education program. Environ. Educ. Res. 24, 445–460. doi: 10.1080/13504622.2017.1279277
Cohn J. P. (2008). Citizen science: can volunteers do real research? BioScience 58, 192–197. doi: 10.1641/B580303
Colla S. R., MacIvor J. S. (2017). Questioning public perception, conservation policy, and recovery actions for honeybees in North America. Conserv. Biol. 31, 1202–1204. doi: 10.1111/cobi.12839
Cunningham M. M., Tran L., McKee C. G., Ortega Polo R., Newman T., Lansing L., et al. (2022). Honey bees as biomonitors of environmental contaminants, pathogens, and climate change. Ecol. Indic. 134, 108457. doi: 10.1016/j.ecolind.2021.108457
Dainese M., Martin E. A., Aizen M. A., Albrecht M., Bartomeus I., Bommarco R., et al. (2019). A global synthesis reveals biodiversity-mediated benefits for crop production. Sci. Adv. 5, eaax0121. doi: 10.1126/sciadv.aax0121
Decourtye A., Alaux C., Le Conte Y., Henry M. (2019). Toward the protection of bees and pollination under global change: present and future perspectives in a challenging applied science. Curr. Opin. Insect Sci. 35, 123–131. doi: 10.1016/j.cois.2019.07.008
DeGrandi-Hoffman G., Chen Y. (2015). Nutrition, immunity and viral infections in honey bees. Curr. Opin. Insect Sci. 10, 170–176. doi: 10.1016/j.cois.2015.05.007
Demortain D. (2021). The science behind the ban: the outstanding impact of ecotoxicological research on the regulation of neonicotinoids. Curr. Opin. Insect Sci. 46, 78–82. doi: 10.1016/j.cois.2021.02.017
Dicks L. V., Breeze T. D., Ngo H. T., Senapathi D., An J., Aizen M. A., et al. (2021). A global-scale expert assessment of drivers and risks associated with pollinator decline. Nat. Ecol. Evol. 5, 1453–1461. doi: 10.1038/s41559-021-01534-9
DiDonato S., Gareau B. J. (2022). Be(e)coming pollinators: Beekeeping and perceptions of environmentalism in Massachusetts. PloS One 17, e0263281. doi: 10.1371/journal.pone.0263281
Di Pasquale G., Alaux C., Conte Y. L., Odoux J.-F., Pioz M., Vaissière B. E., et al. (2016). Variations in the availability of pollen resources affect honey bee health. PloS One 11, e0162818. doi: 10.1371/journal.pone.0162818
Dirilgen T., Herbertsson L., O’Reilly A. D., Mahon N., Stanley D. A. (2023). Moving past neonicotinoids and honeybees: A systematic review of existing research on other insecticides and bees. Environ. Res. 235, 116612. doi: 10.1016/j.envres.2023.116612
Dolezal A. G., Carrillo-Tripp J., Judd T. M., Allen Miller W., Bonning B. C., Toth A. L. (2019). Interacting stressors matter: diet quality and virus infection in honeybee health. R. Soc. Open Sci. 6, 181803. doi: 10.1098/rsos.181803
Donkersley P., Rhodes G., Pickup R. W., Jones K. C., Power E. F., Wright G. A., et al. (2017). Nutritional composition of honey bee food stores vary with floral composition. Oecologia 185, 749–761. doi: 10.1007/s00442-017-3968-3
Duarte Alonso A., Kok S. K., O’Shea M. (2021). Perceived contributory leisure in the context of hobby beekeeping: a multi-country comparison. Leisure Stud. 40, 243–260. doi: 10.1080/02614367.2020.1810303
Duchenne F., Thébault E., Michez D., Elias M., Drake M., Persson M., et al. (2020). Phenological shifts alter the seasonal structure of pollinator assemblages in Europe. Nat. Ecol. Evol. 4, 115–121. doi: 10.1038/s41559-019-1062-4
Dudley N., Alexander S. (2017). Agriculture and biodiversity: a review. Biodiversity 18, 45–49. doi: 10.1080/14888386.2017.1351892
Durant J. L. (2019). Where have all the flowers gone? Honey bee declines and exclusions from floral resources. J. Rural Stud. 65, 161–171. doi: 10.1016/j.jrurstud.2018.10.007
Durant J. L., Otto C. R. V. (2019). Feeling the sting? Addressing land-use changes can mitigate bee declines. Land Use Policy 87, 104005. doi: 10.1016/j.landusepol.2019.05.024
EC. (2013). Commission Implementing Regulation (EU) No 485/2013 of 24 May 2013 amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substances. Official Journal of the European Union 139, 1226.
Eilers E. J., Kremen C., Greenleaf S. S., Garber A. K., Klein A.-M. (2011). Contribution of pollinator-mediated crops to nutrients in the human food supply. PloS One 6, e21363. doi: 10.1371/journal.pone.0021363
Elton C. (1946). Competition and the structure of ecological communities. J. Anim. Ecol. 15, 54–68. doi: 10.2307/1625
Evans A. N., Llanos J. E. M., Kunin W. E., Evison S. E. F. (2018). Indirect effects of agricultural pesticide use on parasite prevalence in wild pollinators. Agriculture Ecosyst. Environ. 258, 40–48. doi: 10.1016/j.agee.2018.02.002
Fikadu Z. (2020). Pesticides use, practice and its effect on honeybee in Ethiopia: a review. Int. J. Trop. Insect Sci. 40, 473–481. doi: 10.1007/s42690-020-00114-x
Forrest J. R. K. (2017). ““Insect Pollinators and Climate Change,”,” in Global Climate Change and Terrestrial Invertebrates (Malden MA, United States: John Wiley & Sons, Ltd), 69–91. doi: 10.1002/9781119070894.ch5
Franklin E. L., Raine N. E. (2019). Moving beyond honeybee-centric pesticide risk assessments to protect all pollinators. Nat. Ecol. Evol. 3, 1373–1375. doi: 10.1038/s41559-019-0987-y
Fürst M. A., McMahon D. P., Osborne J. L., Paxton R. J., Brown M. J. F. (2014). Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366. doi: 10.1038/nature12977
Ganuza C., Redlich S., Uhler J., Tobisch C., Rojas-Botero S., Peters M. K., et al. (2022). Interactive effects of climate and land use on pollinator diversity differ among taxa and scales. Sci. Adv. 8, eabm9359. doi: 10.1126/sciadv.abm9359
Garibaldi L. A., Steffan-Dewenter I., Winfree R., Aizen M. A., Bommarco R., Cunningham S. A., et al. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611. doi: 10.1126/science.1230200
Geldmann J., González-Varo J. P. (2018). Conserving honey bees does not help wildlife. Science 359, 392–393. doi: 10.1126/science.aar2269
Geslin B., Gauzens B., Baude M., Dajoz I., Fontaine C., Henry M., et al. (2017). ““Chapter Four - Massively Introduced Managed Species and Their Consequences for Plant–Pollinator Interactions,”,” in Advances in Ecological Research Networks of Invasion: Empirical Evidence and Case Studies. Eds. Bohan D. A., Dumbrell A. J., Massol F. (Cambridge MA, United States: Academic Press), 147–199. doi: 10.1016/bs.aecr.2016.10.007
Ghode N. (2022). Constraints and future prospects for beekeeping in tribal forest region of Chhattisgarh. Pharma Innovation J. SP-11, 240–245.
Giannini T. C., Costa W. F., Cordeiro G. D., Imperatriz-Fonseca V. L., Saraiva A. M., Biesmeijer J., et al. (2017). Projected climate change threatens pollinators and crop production in Brazil. PloS One 12, e0182274. doi: 10.1371/journal.pone.0182274
Gorrochategui-Ortega J., Muñoz-Colmenero M., Kovačić M., Filipi J., Puškadija Z., Kezić N., et al. (2022). A short exposure to a semi-natural habitat alleviates the honey bee hive microbial imbalance caused by agricultural stress. Sci. Rep. 12, 18832. doi: 10.1038/s41598-022-23287-6
Goulson D., Hughes W. O. H. (2015). Mitigating the anthropogenic spread of bee parasites to protect wild pollinators. Biol. Conserv. 191, 10–19. doi: 10.1016/j.biocon.2015.06.023
Goulson D., Nicholls E., Botías C., Rotheray E. L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957. doi: 10.1126/science.1255957
Gratzer K., Brodschneider R. (2021). How and why beekeepers participate in the INSIGNIA citizen science honey bee environmental monitoring project. Environ. Sci. pollut. Res. 28, 37995–38006. doi: 10.1007/s11356-021-13379-7
Haaland C., Naisbit R. E., Bersier L.-F. (2011). Sown wildflower strips for insect conservation: a review. Insect Conserv. Diversity 4, 60–80. doi: 10.1111/icad.2011.4.issue-1
Hadrava J., Talašová A., Straka J., Benda D., Kazda J., Klečka J. (2022). A comparison of wild bee communities in sown flower strips and semi-natural habitats: A pollination network approach. Insect Conserv. Diversity 15, 312–324. doi: 10.1111/icad.12565
Hall D. M., Martins D. J. (2020). Human dimensions of insect pollinator conservation. Curr. Opin. Insect Sci. 38, 107–114. doi: 10.1016/j.cois.2020.04.001
Hannah L., Steele M., Fung E., Imbach P., Flint L., Flint A. (2017). Climate change influences on pollinator, forest, and farm interactions across a climate gradient. Climatic Change 141, 63–75. doi: 10.1007/s10584-016-1868-x
Hansen J., Sato M., Ruedy R., Lo K., Lea D. W., Medina-Elizade M. (2006). Global temperature change. Proc. Natl. Acad. Sci. 103, 14288–14293. doi: 10.1073/pnas.0606291103
Harianja A. H., Adalina Y., Pasaribu G., Winarni I., Maharani R., Fernandes A., et al. (2023). Potential of beekeeping to support the livelihood, economy, society, and environment of Indonesia. Forests 14, 321. doi: 10.3390/f14020321
Henry M., Béguin M., Requier F., Rollin O., Odoux J.-F., Aupinel P., et al. (2012). A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350. doi: 10.1126/science.1215039
Herrera C. M. (2020). Gradual replacement of wild bees by honeybees in flowers of the Mediterranean Basin over the last 50 years. Proc. Biol. Sci. 287, 20192657. doi: 10.1098/rspb.2019.2657
Hevia V., Carmona C. P., Azcárate F. M., Heredia R., González J. A. (2021). Role of floral strips and semi-natural habitats as enhancers of wild bee functional diversity in intensive agricultural landscapes. Agriculture Ecosyst. Environ. 319, 107544. doi: 10.1016/j.agee.2021.107544
Holder P. J., Jones A., Tyler C. R., Cresswell J. E. (2018). Fipronil pesticide as a suspect in historical mass mortalities of honey bees. Proc. Natl. Acad. Sci. 115, 13033–13038. doi: 10.1073/pnas.1804934115
Iwasaki J. M., Hogendoorn K. (2021). How protection of honey bees can help and hinder bee conservation. Curr. Opin. Insect Sci. 46, 112–118. doi: 10.1016/j.cois.2021.05.005
Iwasaki J. M., Hogendoorn K. (2022). Mounting evidence that managed and introduced bees have negative impacts on wild bees: an updated review. Curr. Res. Insect Sci. 2, 100043. doi: 10.1016/j.cris.2022.100043
Jepson P., Barua M. (2015). A theory of flagship species action. Conserv. Soc. 13, 95–104. doi: 10.4103/0972-4923.161228
Jones L., Lowe A., Ford C. R., Christie L., Creer S., de Vere N. (2022). Temporal patterns of honeybee foraging in a diverse floral landscape revealed using pollen DNA metabarcoding of honey. Integr. Comp. Biol. 62, 199–210. doi: 10.1093/icb/icac029
Kadigi W. R., Ngaga Y. M., Kadigi R. M. J. (2021) Economic viability of smallholder agroforestry and beekeeping projects in Uluguru Mountains, Tanzania: A cost benefit analysis. Available online at: http://www.suaire.sua.ac.tz/handle/123456789/4369 (Accessed September 19, 2023).
Kassa Degu T., Regasa Megerssa G. (2020). Role of beekeeping in the community forest conservation: evidence from Ethiopia. Bee World 97, 98–104. doi: 10.1080/0005772X.2020.1825308
Kevan P. G., Viana B. F. (2003). The global decline of pollination services. Biodiversity 4, 3–8. doi: 10.1080/14888386.2003.9712703
Kleijn D., Biesmeijer K., Dupont Y. L., Nielsen A., Potts S. G., Settele J. (2018). Bee conservation: Inclusive solutions. Science 360, 389–390. doi: 10.1126/science.aat2054
Kleijn D., Winfree R., Bartomeus I., Carvalheiro L. G., Henry M., Isaacs R., et al. (2015). Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat. Commun. 6, 7414. doi: 10.1038/ncomms8414
Klein A.-M., Vaissière B. E., Cane J. H., Steffan-Dewenter I., Cunningham S. A., Kremen C., et al. (2007). Importance of pollinators in changing landscapes for world crops. Proc. R. Soc B 274, 303–313. doi: 10.1098/rspb.2006.3721
Kohsaka R., Park M. S., Uchiyama Y. (2017). Beekeeping and honey production in Japan and South Korea: past and present. J. Ethnic Foods 4, 72–79. doi: 10.1016/j.jef.2017.05.002
Kopittke P. M., Menzies N. W., Wang P., McKenna B. A., Lombi E. (2019). Soil and the intensification of agriculture for global food security. Environ. Int. 132, 105078. doi: 10.1016/j.envint.2019.105078
Kremen C., Williams N. M., Bugg R. L., Fay J. P., Thorp R. W. (2004). The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecol. Lett. 7, 1109–1119. doi: 10.1111/j.1461-0248.2004.00662.x
Lorenz S., Stark K. (2015). Saving the honeybees in Berlin? A case study of the urban beekeeping boom. Environ. Sociol. 1, 116–126. doi: 10.1080/23251042.2015.1008383
Macarthur R. H., Wilson E. O. (1967) The Theory of Island Biogeography. REV-Revised (Princeton University Press). Available online at: https://www.jstor.org/stable/j.ctt19cc1t2 (Accessed September 14, 2023).
MacInnis G., Normandin E., Ziter C. D. (2023). Decline in wild bee species richness associated with honey bee (Apis mellifera L.) abundance in an urban ecosystem. PeerJ 11, e14699. doi: 10.7717/peerj.14699
Maderson S. (2023a). Co-producing agricultural policy with beekeepers: Obstacles and opportunities. Land Use Policy 128, 106603. doi: 10.1016/j.landusepol.2023.106603
Maderson S. (2023b). There’s More Than One Way To Know A Bee: Beekeepers’ environmental knowledge, and its potential role in governing for sustainability. Geoforum 139, 103690. doi: 10.1016/j.geoforum.2023.103690
Maderson S., Wynne-Jones S. (2016). Beekeepers’ knowledges and participation in pollinator conservation policy. J. Rural Stud. 45, 88–98. doi: 10.1016/j.jrurstud.2016.02.015
Mallinger R. E., Gaines-Day H. R., Gratton C. (2017). Do managed bees have negative effects on wild bees?: A systematic review of the literature. PloS One 12, e0189268. doi: 10.1371/journal.pone.0189268
Mallinger R. E., Gibbs J., Gratton C. (2016). Diverse landscapes have a higher abundance and species richness of spring wild bees by providing complementary floral resources over bees’ foraging periods. Landscape Ecol. 31, 1523–1535. doi: 10.1007/s10980-015-0332-z
Martínez-Núñez C., Kleijn D., Ganuza C., Heupink D., Raemakers I., Vertommen W., et al. (2022). Temporal and spatial heterogeneity of semi-natural habitat, but not crop diversity, is correlated with landscape pollinator richness. J. Appl. Ecol. 59, 1258–1267. doi: 10.1111/1365-2664.14137
Matsuzawa T., Kohsaka R. (2021). Status and trends of urban beekeeping regulations: A global review. Earth 2, 933–942. doi: 10.3390/earth2040054
Monasterolo M., Chacoff N. P., Segura Á.D., Benavidez A., Schliserman P. (2022). Native pollinators increase fruit set while honeybees decrease the quality of mandarins in family farms. Basic Appl. Ecol. 64, 79–88. doi: 10.1016/j.baae.2022.07.008
Montoya D., Gaba S., de Mazancourt C., Bretagnolle V., Loreau M. (2020). Reconciling biodiversity conservation, food production and farmers’ demand in agricultural landscapes. Ecol. Model. 416, 108889. doi: 10.1016/j.ecolmodel.2019.108889
Morandin L. A., Winston M. L., Abbott V. A., Franklin M. T. (2007). Can pastureland increase wild bee abundance in agriculturally intense areas? Basic Appl. Ecol. 8, 117–124. doi: 10.1016/j.baae.2006.06.003
National Academies of Sciences, Engineering, and Medicine (2016) Attribution of Extreme Weather Events in the Context of Climate Change (Washington D.C: National Academies Press). Available online at: https://books.google.com/books/about/Attribution_of_Extreme_Weather_Events_in.html?id=WWEpDQAAQBAJ (Accessed September 14, 2023).
Naug D. (2009). Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol. Conserv. 142, 2369–2372. doi: 10.1016/j.biocon.2009.04.007
Noel S., Mikulcak F., Etter H., Stewart N. (2016) Economics of Land Degradation Initiative: Report for policy and decision makers_ Reaping economic and environmental benefits from sustainable land management. ELD Initiative and Deutsche Gesellschaft für Internationale Zusammenarbeit (GIZ) GmbH. Available online at: https://repo.mel.cgiar.org/handle/20.500.11766/4881 (Accessed September 21, 2023).
Noordyke E. R., Ellis J. D. (2021)Reviewing the efficacy of pollen substitutes as a management tool for improving the health and productivity of western honey bee (Apis mellifera) colonies (Accessed September 8, 2023). doi: 10.3389/fsufs.2021.772897
Odoux J.-F., Feuillet D., Aupinel P., Loublier Y., Tasei J.-N., Mateescu C. (2012). Territorial biodiversity and consequences on physico-chemical characteristics of pollen collected by honey bee colonies. Apidologie 43, 561–575. doi: 10.1007/s13592-012-0125-1
Osterman J., Landaverde-González P., Garratt M. P. D., Gee M., Mandelik Y., Langowska A., et al. (2021). On-farm experiences shape farmer knowledge, perceptions of pollinators, and management practices. Global Ecol. Conserv. 32, e01949. doi: 10.1016/j.gecco.2021.e01949
Otterstatter M. C., Thomson J. D. (2008). Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PloS One 3, e2771. doi: 10.1371/journal.pone.0002771
Outhwaite C. L., McCann P., Newbold T. (2022). Agriculture and climate change are reshaping insect biodiversity worldwide. Nature 605, 97–102. doi: 10.1038/s41586-022-04644-x
Parmesan C. (2007). Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Global Change Biol. 13, 1860–1872. doi: 10.1111/j.1365-2486.2007.01404.x
Parmesan C., Root T. L., Willig M. R. (2000). Impacts of extreme weather and climate on terrestrial biota. Bull. Am. Meteorological Soc. 81, 443–450. doi: 10.1175/1520-0477(2000)081<0443:IOEWAC>2.3.CO;2
Pecenka J. R., Ingwell L. L., Foster R. E., Krupke C. H., Kaplan I. (2021). IPM reduces insecticide applications by 95% while maintaining or enhancing crop yields through wild pollinator conservation. Proc. Natl. Acad. Sci. 118, e2108429118. doi: 10.1073/pnas.2108429118
Pe’er G., Finn J. A., Díaz M., Birkenstock M., Lakner S., Röder N., et al. (2022). How can the European Common Agricultural Policy help halt biodiversity loss? Recommendations by over 300 experts. Conserv. Lett. 15, e12901. doi: 10.1111/conl.12901
Penn J., Hu W., Penn H. J. (2019). Support for Solitary Bee Conservation among the Public versus Beekeepers. Am. J. Agric. Economics 101, 1386–1400. doi: 10.1093/ajae/aaz050
Pettis J. S., Lichtenberg E. M., Andree M., Stitzinger J., Rose R., vanEngelsdorp D. (2013). Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen nosema ceranae. PloS One 8, e70182. doi: 10.1371/journal.pone.0070182
Phillips R., Ford Y., Sadler K., Silve S., Baurley S. (2013). “Open Design: Non-professional User-Designers Creating Products for Citizen Science: A Case Study of Beekeepers,” in Design, User Experience, and Usability. Web, Mobile, and Product Design. Ed. Marcus A. (Springer, Berlin, Heidelberg), 424–431. doi: 10.1007/978-3-642-39253-5_47
Potts S. G., Biesmeijer J. C., Kremen C., Neumann P., Schweiger O., Kunin W. E. (2010a). Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353. doi: 10.1016/j.tree.2010.01.007
Potts S. G., Roberts S. P. M., Dean R., Marris G., Brown M. A., Jones R., et al. (2010b). Declines of managed honey bees and beekeepers in Europe. J. Apicultural Res. 49, 15–22. doi: 10.3896/IBRA.1.49.1.02
Prendergast K. S. (2023). Native flora receive more visits than exotics from bees, especially native bees, in an urbanised biodiversity hotspot. Pac. Conserv. Biol. 30 (1). doi: 10.1071/PC22033
Prendergast K. S., Garcia J. E., Howard S. R., Ren Z.-X., McFarlane S. J., Dyer A. G. (2021). Bee representations in human art and culture through the ages. Art Percept. 10, 1–62. doi: 10.1163/22134913-bja10031
Pyke G. (1999). The introduced Honeybee Apis mellifera and the Precautionary Principle: reducing the conflict. Australian Zoologist 31, 181186. doi: 10.7882/AZ.1999.018
Pyke G. H., Prendergast K. S., Ren Z.-X. (2023). Pollination crisis Down-Under: Has Australasia dodged the bullet? Ecol. Evol. 13, e10639. doi: 10.1002/ece3.10639
Quigley T. P., Amdam G. V., Harwood G. H. (2019). Honey bees as bioindicators of changing global agricultural landscapes. Curr. Opin. Insect Sci. 35, 132–137. doi: 10.1016/j.cois.2019.08.012
Rasmussen C., Dupont Y. L., Madsen H. B., Bogusch P., Goulson D., Herbertsson L., et al. (2021). Evaluating competition for forage plants between honey bees and wild bees in Denmark. PloS One 16, e0250056. doi: 10.1371/journal.pone.0250056
Requier F., Odoux J.-F., Tamic T., Moreau N., Henry M., Decourtye A., et al. (2015). Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol. Appl. 25, 881–890. doi: 10.1890/14-1011.1
Richardson R. T., Conflitti I. M., Labuschagne R. S., Hoover S. E., Currie R. W., Giovenazzo P., et al. (2023). Land use changes associated with declining honey bee health across temperate North America. Environ. Res. Lett. 18, 064042. doi: 10.1088/1748-9326/acd867
Rollin O., Garibaldi L. A. (2019). Impacts of honeybee density on crop yield: A meta-analysis. J. Appl. Ecol. 56, 1152–1163. doi: 10.1111/1365-2664.13355
Sánchez-Bayo F., Goulson D., Pennacchio F., Nazzi F., Goka K., Desneux N. (2016). Are bee diseases linked to pesticides? — A brief review. Environ. Int. 89–90, 7–11. doi: 10.1016/j.envint.2016.01.009
Sandrock C., Tanadini L. G., Pettis J. S., Biesmeijer J. C., Potts S. G., Neumann P. (2014). Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agric. For. Entomol. 16, 119–128. doi: 10.1111/afe.12041
Saunders M. E., Smith T. J., Rader R. (2018). Bee conservation: Key role of managed bees. Science 360, 389–389. doi: 10.1126/science.aat1535
Scheper J., Bommarco R., Holzschuh A., Potts S. G., Riedinger V., Roberts S. P. M., et al. (2015). Local and landscape-level floral resources explain effects of wildflower strips on wild bees across four European countries. J. Appl. Ecol. 52, 1165–1175. doi: 10.1111/1365-2664.12479
Schoener T. W. (1983). Field experiments on interspecific competition. Am. Nat. 122, 240–285. doi: 10.1086/284133
Schönfelder M. L., Bogner F. X. (2017). Individual perception of bees: Between perceived danger and willingness to protect. PloS One 12, e0180168. doi: 10.1371/journal.pone.0180168
Schwartz K. R., Minor H., Magro C., McConnell J., Capani J., Griffin J., et al. (2021). The neonicotinoid imidacloprid alone alters the cognitive behavior in Apis mellifera L. and the combined exposure of imidacloprid and Varroa destructor mites synergistically contributes to trial attrition. J. Apicultural Res. 60, 431–438. doi: 10.1080/00218839.2020.1866233
Schweiger O., Biesmeijer J. C., Bommarco R., Hickler T., Hulme P. E., Klotz S., et al. (2010). Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol. Rev. 85, 777–795. doi: 10.1111/j.1469-185X.2010.00125.x
Seibold S., Gossner M. M., Simons N. K., Blüthgen N., Müller J., Ambarlı D., et al. (2019). Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674. doi: 10.1038/s41586-019-1684-3
Seneviratne S. I., Lüthi D., Litschi M., Schär C. (2006). Land–atmosphere coupling and climate change in Europe. Nature 443, 205–209. doi: 10.1038/nature05095
Shaw J., Cunningham C., Harper S., Ragazzon-Smith A., Lythgoe P. R., Walker T. R. (2023). Biomonitoring of honey metal(loid) pollution in Northwest England by citizen scientists. Environ. Adv. 13, 100406. doi: 10.1016/j.envadv.2023.100406
Shi X., Xiao H., Luo S., Hodgson J. A., Bianchi F. J. J. A., He H., et al. (2021). Can landscape level semi-natural habitat compensate for pollinator biodiversity loss due to farmland consolidation? Agriculture Ecosyst. Environ. 319, 107519. doi: 10.1016/j.agee.2021.107519
Sialuk S. C. (2014) Determinants of beekeeping in enhancing environmental conservation in arid and semi arid lands in Kenya: a case of Lomut ward, west Pokot county. Available online at: http://erepository.uonbi.ac.ke/handle/11295/76292 (Accessed September 20, 2023).
Sidemo-Holm W., Carrié R., Ekroos J., Lindström S. A. M., Smith H. G. (2021). Reduced crop density increases floral resources to pollinators without affecting crop yield in organic and conventional fields. J. Appl. Ecol. 58, 1421–1430. doi: 10.1111/1365-2664.13887
Singh N. S., Sharma R., Parween T., Patanjali P. K. (2018). ““Pesticide Contamination and Human Health Risk Factor,”,” in Modern Age Environmental Problems and their Remediation. Eds. Oves M., Zain Khan M., Ismail I. M. I. (Springer International Publishing, Cham), 49–68. doi: 10.1007/978-3-319-64501-8_3
Siviter H., Bailes E. J., Martin C. D., Oliver T. R., Koricheva J., Leadbeater E., et al. (2021a). Agrochemicals interact synergistically to increase bee mortality. Nature 596, 389–392. doi: 10.1038/s41586-021-03787-7
Siviter H., Richman S. K., Muth F. (2021b). Field-realistic neonicotinoid exposure has sub-lethal effects on non-Apis bees: A meta-analysis. Ecol. Lett. 24, 2586–2597. doi: 10.1111/ele.13873
Smith T. J., Saunders M. E. (2016). Honey bees: the queens of mass media, despite minority rule among insect pollinators. Insect Conserv. Diversity 9, 384–390. doi: 10.1111/icad.12178
Souza C. S., Maruyama P. K., Aoki C., Sigrist M. R., Raizer J., Gross C. L., et al. (2018). Temporal variation in plant–pollinator networks from seasonal tropical environments: Higher specialization when resources are scarce. J. Ecol. 106, 2409–2420. doi: 10.1111/1365-2745.12978
Stott P. (2016). How climate change affects extreme weather events. Science 352, 1517–1518. doi: 10.1126/science.aaf7271
Sun Y., Zhang X., Zwiers F. W., Song L., Wan H., Hu T., et al. (2014). Rapid increase in the risk of extreme summer heat in Eastern China. Nat. Clim Change 4, 1082–1085. doi: 10.1038/nclimate2410
Thompson H. M., Pamminger T. (2019). Are honeybees suitable surrogates for use in pesticide risk assessment for non-Apis bees? Pest Manage. Sci. 75, 2549–2557. doi: 10.1002/ps.5494
Thomson D. (2004). Competitive interactions between the invasive european honey bee and native bumble bees. Ecology 85, 458–470. doi: 10.1890/02-0626
Tilman D., Clark M., Williams D. R., Kimmel K., Polasky S., Packer C. (2017). Future threats to biodiversity and pathways to their prevention. Nature 546, 73–81. doi: 10.1038/nature22900
Tomé H. V. V., Ramos G. S., Araújo M. F., Santana W. C., Santos G. R., Guedes R. N. C., et al. (2017). Agrochemical synergism imposes higher risk to Neotropical bees than to honeybees. R. Soc. Open Sci. 4, 160866. doi: 10.1098/rsos.160866
Tooker J. F., Pearsons K. A. (2021). Newer characters, same story: neonicotinoid insecticides disrupt food webs through direct and indirect effects. Curr. Opin. Insect Sci. 46, 50–56. doi: 10.1016/j.cois.2021.02.013
Tosi S., Nieh J. C., Sgolastra F., Cabbri R., Medrzycki P. (2017). Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proc. R. Soc. B: Biol. Sci. 284, 20171711. doi: 10.1098/rspb.2017.1711
Trevan J. W., Dale H. H. (1927). The error of determination of toxicity. Proc. R. Soc. London Ser. B Containing Papers Biol. Character 101, 483–514. doi: 10.1098/rspb.1927.0030
Tscharntke T., Grass I., Wanger T. C., Westphal C., Batáry P. (2021). Beyond organic farming – harnessing biodiversity-friendly landscapes. Trends Ecol. Evol. 36, 919–930. doi: 10.1016/j.tree.2021.06.010
Uyttenbroeck R., Hatt S., Paul A., Boeraeve F., Piqueray J., Francis F., et al. (2016). Pros and cons of flowers strips for farmers. A review. Biotechnologie Agronomie Société Environnement 20, 225–235. doi: 10.25518/1780-4507
Valido A., Rodríguez-Rodríguez M. C., Jordano P. (2019). Honeybees disrupt the structure and functionality of plant-pollinator networks. Sci. Rep. 9, 4711. doi: 10.1038/s41598-019-41271-5
Vanbergen A. J. (2021). A cocktail of pesticides, parasites and hunger leaves bees down and out. Nature 596, 351–352. doi: 10.1038/d41586-021-02079-4
van Vierssen Trip N., MacPhail V. J., Colla S. R., Olivastri B. (2020). Examining the public’s awareness of bee (Hymenoptera: Apoidae: Anthophila) conservation in Canada. Conserv. Sci. Pract. 2, e293. doi: 10.1111/csp2.293
Vasiliev D., Greenwood S. (2021). The role of climate change in pollinator decline across the Northern Hemisphere is underestimated. Sci. Total Environ. 775, 145788. doi: 10.1016/j.scitotenv.2021.145788
Venturini E. M., Drummond F. A., Hoshide A. K., Dibble A. C., Stack L. B. (2017). Pollination reservoirs for wild bee habitat enhancement in cropping systems: a review. Agroecol. Sustain. Food Syst. 41, 101–142. doi: 10.1080/21683565.2016.1258377
Vercelli M., Novelli S., Ferrazzi P., Lentini G., Ferracini C. (2021). A qualitative analysis of beekeepers’ Perceptions and farm management adaptations to the impact of climate change on honey bees. Insects 12, 228. doi: 10.3390/insects12030228
Vohland K., Land-Zandstra A., Ceccaroni L., Lemmens R., Perelló J., Ponti M., et al. (Eds.) (2021). The Science of Citizen Science (Springer Nature). doi: 10.1007/978-3-030-58278-4
Wagner K., Meilby H., Cross P. (2019). Sticky business - Why do beekeepers keep bees and what makes them successful in Tanzania? J. Rural Stud. 66, 52–66. doi: 10.1016/j.jrurstud.2019.01.022
Weltin M., Zasada I., Piorr A., Debolini M., Geniaux G., Moreno Perez O., et al. (2018). Conceptualising fields of action for sustainable intensification – A systematic literature review and application to regional case studies. Agriculture Ecosyst. Environ. 257, 68–80. doi: 10.1016/j.agee.2018.01.023
Wilson J. S., Forister M. L., Carril O. M. (2017). Interest exceeds understanding in public support of bee conservation. Front. Ecol. Environ. 15, 460–466. doi: 10.1002/fee.1531
Wojcik V. A., Morandin L. A., Davies Adams L., Rourke K. E. (2018). Floral resource competition between honey bees and wild bees: is there clear evidence and can we guide management and conservation? Environ. Entomol. 47, 822–833. doi: 10.1093/ee/nvy077
Woodcock B. A., Bullock J. M., Shore R. F., Heard M. S., Pereira M. G., Redhead J., et al. (2017). Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395. doi: 10.1126/science.aaa1190
Woodcock B. A., Oliver A. E., Newbold L. K., Soon Gweon H., Read D. S., Sayed U., et al. (2022). Citizen science monitoring reveals links between honeybee health, pesticide exposure and seasonal availability of floral resources. Sci. Rep. 12, 14331. doi: 10.1038/s41598-022-18672-0
Young J. C., Calla S., Lécuyer L., Skrimizea E. (2022). Understanding the social enablers and disablers of pesticide reduction and agricultural transformation. J. Rural Stud. 95, 67–76. doi: 10.1016/j.jrurstud.2022.07.023
Zhang G., Murray C. J., St. Clair A. L., Cass R. P., Dolezal A. G., Schulte L. A., et al. (2023). Native vegetation embedded in landscapes dominated by corn and soybean improves honey bee health and productivity. J. Appl. Ecol. 60, 1032–1043. doi: 10.1111/1365-2664.14397
Keywords: beekeepers, competition, conservation, honeybees, sustainability, wild pollinators
Citation: Oddie MAY and Dahle B (2024) One for all and all for one: a review on the commonality of risk to honeybees and wild pollinators and the benefits of beekeepers in conservation. Front. Bee Sci. 2:1305679. doi: 10.3389/frbee.2024.1305679
Received: 02 October 2023; Accepted: 04 March 2024;
Published: 14 March 2024.
Edited by:
Peter Kevan, University of Guelph, CanadaCopyright © 2024 Oddie and Dahle. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Melissa A. Y. Oddie, melissa.oddie@norbi.no