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Assessing the impacts of urban beehives on wild bees using individual, community, and population-level metrics

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Sarah MacKell
Sarah MacKell
Sarah MacKell
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Hadil Elsayed
Hadil Elsayed
Hadil Elsayed
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Sheila Colla
Sheila Colla
Sheila Colla
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Abstract and Figures

Several species of wild bees are in decline globally and the presence of managed honey bees is one of many proposed stressors on wild bee populations. However, there is limited knowledge of the impacts of honey bee hives on wild bees, especially in urban landscapes. We performed a field study to assess the associations between honey bees and wild bees within the Greater Toronto Area in Ontario, Canada. We measured relative abundance of honey bees, wild bee metrics (abundance, community composition, functional diversity, and body size), and floral resources (floral density and richness); we also calculated impervious surface at 500 m and 1 km for each of our sites. Our main findings were that increasing honey bee abundance was correlated with decreases in wild bee species richness and functional diversity, as well as two wild bee species’ abundances and one wild bee species body size, out of many assessed. This research adds to the growing body of literature aiming to evaluate whether honey bees are a stressor on wild bees in urban landscapes, which will be valuable for informing conservation management practices and future research.
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Urban Ecosystems (2023) 26:1209–1223
https://doi.org/10.1007/s11252-023-01374-4
loss and fragmentation (e.g., increased urbanization), lack
of suitable forage, diseases and pests, and even the increase
in non-native pollinators (Potts et al. 2010; Winfree 2010;
Thomson 2016). Honey bees, which are non-native to North
America, are often the focus of conservation initiatives,
including in urban areas (Colla and MacIvor 2017). How-
ever, there is evidence that: the introduction of non-native
honey bees may negatively impact wild bee species (Thom-
son 2004; Lindström et al. 2016; Cane and Tepedino 2017),
honey bee hive reductions are not a good proxy for native
bee declines (Wood et al. 2020), and that honey bees are not
at-risk of extinction (IUCN 2020).
There are two main hypotheses for how the presence
of managed honey bees might harm native bees: pathogen
spillover and oral resource competition. Pathogen spill-
over from domesticated hosts has been documented in a
variety of taxonomic groups and can lead to drastic declines
among the exposed wild species, for example the Ethio-
pian wolf, red squirrels in the UK, and orange-bellied par-
rots (Haydon et al. 2002; Rushton et al. 2006; Randall et al.
2006; Woodroe et al. 2012; Peters et al. 2014). Pathogen
spillover from managed bees to wild bees is a relatively new
eld of research and has mainly been documented in bum-
ble bees (Colla et al. 2006; Cameron et al. 2011) and honey
Introduction
Bees are among the most ecient pollinators for many crops
and wildowers (Fontaine et al. 2006; Winfree et al. 2008)
and pollination services are estimated to increase annual
global crop production by USD $235–577 billion (Laut-
enbach et al. 2012). Alarmingly, many bee species abun-
dances are in steep decline globally, including in Canada
(Colla and Packer 2008; Potts et al. 2010). There are numer-
ous proposed reasons as to why some native bee species
are declining, including climate change, pesticides, habitat
Sarah MacKell
sarahmackell14@gmail.com
Hadil Elsayed
hadil.lomomba@gmail.com
Sheila Colla
collasheila@gmail.com
1 Department of Biology, York University, York University,
4700 Keele Street, M3J 1P3 Toronto, ON, Canada
2 Faculty of Environmental and Urban Change, York
University, 4700 Keele Street, M3J 1P3 Toronto, ON,
Canada
Abstract
Several species of wild bees are in decline globally and the presence of managed honey bees is one of many proposed
stressors on wild bee populations. However, there is limited knowledge of the impacts of honey bee hives on wild bees,
especially in urban landscapes. We performed a eld study to assess the associations between honey bees and wild bees
within the Greater Toronto Area in Ontario, Canada. We measured relative abundance of honey bees, wild bee metrics
(abundance, community composition, functional diversity, and body size), and oral resources (oral density and rich-
ness); we also calculated impervious surface at 500 m and 1 km for each of our sites. Our main ndings were that increas-
ing honey bee abundance was correlated with decreases in wild bee species richness and functional diversity, as well as
two wild bee species’ abundances and one wild bee species body size, out of many assessed. This research adds to the
growing body of literature aiming to evaluate whether honey bees are a stressor on wild bees in urban landscapes, which
will be valuable for informing conservation management practices and future research.
Keywords Urban ecology · Apis mellifera · Wild bees · Competition · Canada · Honey bees
Accepted: 14 May 2023 / Published online: 22 May 2023
© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2023
Assessing the impacts of urban beehives on wild bees using
individual, community, and population-level metrics
SarahMacKell1· HadilElsayed1· SheilaColla2
1 3
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Since 2017, the concept of MIMS has been largely acknowledged in the literature (e.g., Geldmann and González-Varo, 2018;Ghisbain et al., 2021;Iwasaki and Hogendoorn, 2022). In parallel, concerns around the massive introduction of managed pollinators in natural (e.g., Henry and Rodet, 2018;Page and Williams, 2022;2023;Ropars et al., 2022), urbanized habitats (e.g., MacInnis et al., 2023;Mackell et al., 2023;Ropars et al., 2019) and oceanic islands (e.g., Lázaro et al., 2021;Valido et al., 2019;Zakardjian et al., 2020) have grown considerably, particularly when A. mellifera and B. terrestris are involved (e.g., Thomson and Page, 2020;Wojcik et al., 2018;Zakardjian et al., 2022). Over the past six years, research about competitive interactions between honey bees and wild bees has increased by 47% with 148 articles published in 2017 (Mallinger et al., 2017) and 216 articles published in 2022 (Iwasaki and Hogendoorn, 2022). ...
... Over the past six years, research about competitive interactions between honey bees and wild bees has increased by 47% with 148 articles published in 2017 (Mallinger et al., 2017) and 216 articles published in 2022 (Iwasaki and Hogendoorn, 2022). Since this latter review, the quantity of evidence of negative impacts of managed bees on wild pollinators did continue to increase (e.g., MacInnis et al., 2023;Mackell et al., 2023;Mouillard-Lample et al., 2023;Page and Williams, 2022;2023;Prendergast and Ollerton, 2022;Prendergast and Ollerton, 2021;Ropars et al., 2022). Thus, this scientific mobilization has brought about new concerns regarding the impacts of MIMS in less explored plant-pollinator systems, such as the trade of wild bee cocoons for bee hotels , the increased demand for ornamental plants in cities (Erickson et al., 2020;Cecala and Rankin, 2021;Garbuzov et al., 2017;Zaninotto et al., 2023a) and the setup of pollinatorfriendly schemes in agricultural landscapes (Wood et al. 2015;Seitz et al., 2020;Schatz et al., 2021;see Albrecht et al. 2021 for a review). ...
... In the past six years, the establishment of honey bee colonies and their impacts on wild pollinators have received increasing attention in the literature, either in natural areas Henry and Rodet, 2018;Ropars et al., 2020;Weaver et al., 2022), agricultural environments (Magrach et al., 2017;Weekers et al., 2022; see also Weissmann et al., 2021), or cities (Casanelles-Abella et al., 2023;MacInnis et al., 2023;MacKell et al., 2023;McCune et al., 2020;Renner et al., 2021;Ropars et al., 2019) and archipelagos (Ing and Mogren, 2020;Lázaro et al., 2021;Valido et al., 2019). Field studies carried out in such environments commonly illustrate the negative effects of excessive honey bee colony densities on wild pollinators (i.e., 66% of the studies in 2022; Iwasaki and Hogendoorn, 2022), implying several impacts: ...
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View
... The risk of competition was highlighted by the finding that the high honey bee density in Montreal was negatively impacting wild bee species richness [40]. Similar findings have been documented from elsewhere in Canada and Europe [41,42]. Beyond municipal boundaries, most provinces track the location and number of honey bee hives by using a registry system, where such registries have the potential to track the density of bee hives and competition risk to native pollinators. ...
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Simple Summary Natural ecosystems support a rich variety of native bees, many of which are important economically. Honey bees, which are not native to North America, and domesticated bumble bees spread pathogens (diseases and parasites) and outcompete native bees for nectar and pollen. We aimed to reduce these threats by finding Canadian provincial legislation that could direct legislation in Yukon Territory, where native pollinator communities are still healthy and essential for pollinating agricultural crops. We classified the legislative requirements as follows: tracking numbers and locations of honey bee hives (registry); controlling the spread of pathogens (inspections, quarantines, and cleaning); controlling the competition with native pollinators (limiting shared use of space); and applying regulations to all domesticated bee species. There is little Canadian legislation controlling the interactions of honey bees and native pollinators; the competition problem is poorly addressed. We recommend controls on the numbers, locations, and timing of honey bee hives on public lands in the form of permitted “foraging leases” (for domestic insect livestock), similar to “grazing leases” (for domestic mammalian livestock). We detail changes to Yukon legislation (Animal Health, Animal Protection and Control, Wildlife, and Public Lands Acts) to deal with pathogen spread and competition. Protecting native pollinators will conserve the successful pollination of flowers producing foods and medicines for people.
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... Yet, several studies document reduced wild bee abundance and diversity in the presence of artificially high honeybee abundance (e.g. Prendergast & Ollerton, 2022;MacInnis et al., 2023;MacKell et al., 2023), even in regions where honeybee keeping has a long history (e.g., Ropars et al., 2019). Honeybees can negatively impact wild bees through competition for resources (e.g. ...
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Wild bee populations are threatened by habitat fragmentation and land-use change, but few development plans consider resource competition. However, managed honeybees (Apis mellifera) are often introduced to residential areas by hobbyist beekeepers, placing potential competitive pressure on wild bees. We sampled bee-plant interactions from natural reserves across the peri-urban landscape of Fort Collins, Colorado (U.S.A.) and modeled pollination networks and bee foraging breadth in response to road and natural area density, reserve size, and background honeybee abundance. Four key findings emerged: (1) honeybees dominated pollination networks, representing 26% of recorded bee-plant interactions. High frequencies of honeybees reduced network modu-larity, but reserve size, natural area density, and seasonality did not predict network structure. (2) Honeybee frequency increased with road density and declined as natural area cover increased, indicating that higher residential densities drive honeybee pressure. (3) Patterns of floral visitation by honeybees and wild bees indicate substantial niche overlap, and foraging breadths of Megachilidae (leafcutter bees) and Colletidae (plasterer bees) declined as honeybee frequency increased. (4) Noxious weed species (e.g., Convulvulus arvense and Carduus nutans) had high rates of visitation by wild bees and were identified as both pollination network 'hubs' and 'connectors'. We conclude that honeybee presence alters topology of bee-plant networks, and prioritizing creation of natural area reserves to maximize density of non-impervious cover may indirectly reduce competition with honeybees. Conservation practitioners can offset honeybee effects by favoring floral species that support wild bee foraging and are not visited by honeybees, especially in regions where honeybees are not native.
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... Previous research examining the interactions between native bees and honey bees has indicated negative or neutral interactions through competition for floral resources and changes in the availability and quality of floral rewards of native plants (Mu et al. 2014, Mallinger et al. 2017, Iwasaki and Hogendoorn 2022, Page and Williams 2023a, 2023b. The fewer studies analyzing honey bees' impact on entire native bee community composition often exhibit negative effects where honey bees suppress native bee richness and abundance (Angelella et al. 2021, Garibaldi et al. 2021, MacInnis et al. 2023, MacKell et al. 2023. However, these studies are often conducted in agricultural or urban land-use settings where honey bees have been naturalized or the native environment and ecology have already been disturbed by humans. ...
Low-density migratory beekeeping induces intermediate disturbance effects on native bee communities in Tibetan Plateau alpine meadows
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Ecological disturbance can promote or reduce community biodiversity depending on its severity. Beekeeping activities represent a type of ecological disturbance when large numbers of honey bees are introduced to a landscape and interact with the local plant and pollinator community. In this study, we characterized the effect of immediate and long-term low-density migratory beekeeping on the diversity and abundance of native bees in the Qinghai-Tibet Plateau (China). We found that the presence of apiaries and the number of honey bees reduced native bee abundances in the local bee community, likely through displacement from floral resources. However, in locations where apiaries were previously kept for decades but are not currently present, native bee abundances recovered, and phylogenetic diversity increased; yet community relative abundances and dominant species were distinct from those that had never been stocked. Our results suggest that the presence of a transient, intermediate number of migratory honey bee colonies (60–100 colonies spaced ≥15 km from each other) may represent an intermediate ecological disturbance and not permanently reduce native bee abundances past a critical threshold that may lead to local extirpation. Yet, our study demonstrates the potential for even intermediate-scale low-density beekeeping to alter native bee communities in the long-term.
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... Several publications have evaluated the influence of honey bee on wild bee communities (e.g., Steffan-dewenter and Tscharntke 2000; Cane and Tepedino 2017;Angelella et al. 2021;Prendergast et al. 2021;Weekers et al. 2022;Macinnis et al. 2023;Mackell et al. 2023). However, these studies show contrasting responses depending on the study context (e.g., the availability of floral resources, the heterogeneity of the landscape and the honey bee density). ...
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... Recent studies have shown that the introduction of honey bee colonies into protected areas could deplete floral resources with detrimental effects on populations of wild pollinators (e.g., Magrach et al., 2017;Henry and Rodet, 2018;Valido et al., 2019;Ropars et al., 2020bRopars et al., , 2022Williams, 2023a, 2023b;MacInnis et al., 2023;Prendergast and Ollerton, 2022;Weaver et al., 2022;Casanelles-Abella et al., 2023;MacKell et al., 2023;Mouillard-Lample et al., 2023;Sponsler et al., 2024). In particular, studies suggest potential causal links between this exploitative competition and the fitness of wild pollinators (e.g., Cane and Tepedino, 2017;Fig. ...
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Due to the increasing pressures on bees, many beekeepers currently wish to move their managed livestock of Apis mellifera into little disturbed ecosystems such as protected natural areas. This may, however, exert detrimental competitive effects upon local wild pollinators. While it appears critical for land managers to get an adequate knowledge of this issue for effective wildlife conservation schemes, the frequency of this competition is not clear to date. Based on a systematic literature review of 96 studies, we assessed the frequency of exploitative competition between honey bees and wild pollinators. We found that 78% of the studies highlighted exploitative competition from honey bees to wild pollinators. Importantly, these studies have mostly explored competition with wild bees, while only 18% of them considered other pollinator taxa such as ants, beetles, bugs, butterflies, flies, moths, and wasps. The integration of non-bee pollinators into scientific studies and conservation plans is urgently required as they are critical for the pollination of many wild plants and crops. Interestingly, we found that a majority (88%) of these studies considering also non-bee pollinators report evidence of competition. Thus, neglecting non-bee pollinators could imply an underestimation of competition risks from honey bees. More inclusive work is needed to estimate the risks of competition in its entirety, but also to apprehend the context-dependency of competition so as to properly inform wildlife conservation schemes.
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... Recent studies have shown that the introduction of honey bee colonies into protected areas could deplete floral resources with detrimental effects on populations of wild pollinators (e.g., Magrach et al., 2017;Henry and Rodet, 2018;Valido et al., 2019;Ropars et al., 2020bRopars et al., , 2022Williams, 2023a, 2023b;MacInnis et al., 2023;Prendergast and Ollerton, 2022;Weaver et al., 2022;Casanelles-Abella et al., 2023;MacKell et al., 2023;Mouillard-Lample et al., 2023;Sponsler et al., 2024). In particular, studies suggest potential causal links between this exploitative competition and the fitness of wild pollinators (e.g., Cane and Tepedino, 2017;Fig. ...
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Numerous animal species can survive in human-modified habitats, but often display behavioral, morphological, physiological or genetic plasticity compared to non-urban conspecifics. One group of organisms with a large urban presence are bees. Bee species have high diversity and abundance in cities, which has been empirically supported in numerous studies assessing community composition. Recent reviews of these articles reveal global patterns of high bee richness in cities, and the impact of urban landscape characteristics on bee populations. However, more specific information about how bees are able to be successful in cities, as have been studied in birds and mammals, has not been prioritized in any review thus far. These topics, though uncommon in much of the current published literature, are important for understanding how urban pollinating bees survive. Therefore, the goal of this paper is to review urban bee literature, focusing on topics that have yet to be examined in entirety, but are crucial for the plasticity observed, including foraging, nesting, competition, physiological adaptations, morphological shifts, genetics and gene flow. Additionally, we provide predictions and propose possible experimental directions based upon what is currently known about urban animal populations and bee life history. These predictions aim to inspire future multidisciplinary research to holistically evaluate urban bee populations. Expanding the knowledge base from primarily community composition studies to intricate assessments of behavior, genetics, and other important traits will aid in the creation of more targeted conservation policies, land development, and improve the capacity for pollination services in cities.
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Chapter
  • Jan 2021
A review of current capture and collection techniques for bees is presented. Information regarding primary collection techniques (i.e. netting, malaise traps, bowl traps, trap nests, visual surveys) along with issues of variability, bias, and the impacts of observers along with taxonomic impediments are discussed. Notable is the lack of standardization in any of these approaches along with a similar sparsity of statistical evaluation of the methodologies themselves. Practitioners deploy these and several lesser-known techniques, in a great many ways. We are at the beginning of a learning curve on how to develop accurate and precise research and monitoring tools for bee populations, and it is clear that there is much to learn.
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