# Avenues towards reconciling wild and managed bee proponents

Alexis L Beaurepaire, Katja Hogendoorn, David Kleijn, Gard W Otis, Simon G Potts, Theresa L Singer, Samuel Boff, Christian Pirk, Josef Settele, Robert J Paxton, et al.

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Alexis L Beaurepaire, Katja Hogendoorn, David Kleijn, Gard W Otis, Simon G Potts, et al. Av- enues towards reconciling wild and managed bee proponents. Trends in Ecology & Evolution, 2024, 10.1016/j.tree.2024.11.009 . hal-04829945

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# Trends in Ecology & Evolution

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## Science & Society

### Avenues towards reconciling wild and managed bee proponents

Alexis L. Beaurepaire ¹,²,*,
Katja Hogendoorn³, David Kleijn⁴,
Gard W. Otis²,⁵, Simon G. Potts⁶,
Theresa L. Singer⁷, Samuel Boff⁸,
Christian Pirk⁹,
Josef Settele¹⁰,¹¹,¹²,
Robert J. Paxton¹³, Nigel E. Raine⁵,
Simone Tosi¹⁴, Neal Williams¹⁵,
Alexandra-Maria Klein¹⁶,¹⁷,
Yves Le Conte¹⁸,
Joshua W. Campbell¹⁹,
Geoffrey R. Williams²⁰,
Lorenzo Marini²¹,
Axel Brockmann²²,
Fabio Sgolastra²³, Natalie Boyle²⁴,
Markus Neuditschko²⁵,
Lars Straub²,²⁶,²⁷,
Peter Neumann²,
Jean-Daniel Charrière¹,
Matthias Albrecht²⁸, and
Vincent Dietemann¹,²⁹

Bees are crucial for food security and biodiversity. However, managed bees are increasingly considered drivers of wild bee declines, leading to stakeholder conflicts and restrictive policies. We propose avenues to reconcile wild and managed bee proponents and point out knowledge gaps that hinder the development of evidence-based policies.

### Negative impacts of managed bees: a growing concern based on circumstantial scientific evidence

Integrating biodiversity conservation with food security for a growing world

population represents a major challenge. Three quarters of the world's crops are dependent on pollinators, and their cropped area is expanding. Consequently, reliance on pollinators, especially managed and wild bees, is increasing [1]. Among Earth's 20 000+ wild bee species, many are declining, threatening biodiversity and leading to pollination deficits [2,3]. To mitigate pollination deficits, 19 bee species can currently be managed and transported where and when required to promote crop pollination [4].

Establishing and maintaining high densities of managed bees raises concerns about their impacts on wild bee populations [5]. In recent decades, a growing number of studies have investigated whether competition for floral and nesting resources with managed bees and pathogen transmission negatively impact wild bees [5,6], often fueling conflicts among beekeepers, farmers, conservationists, and scientists [7]. Despite more than 200 scientific papers addressing managed bee-wild bee interactions, and 66% concluding that there are potential risks to wild bees, evidence remains circumstantial, contextual, and does not include long-term and population-level assessments [5]. Insufficient knowledge of the circumstances in which interactions amongst bees become detrimental can lead to inaccurate risk assessments and potentially to ecological or economic harm. Nevertheless, due to increasing pressure from stakeholders, and despite the low degree of confidence in available data, policy-makers have begun to ban managed bees from conservation areas or cities [8], a trend that is likely to increase. Ensuring contextually optimal trade-offs between conservation and socioeconomic priorities is key for bee policies (Box 1) and necessitates rapid and coordinated action to facilitate the co-creation of solutions by stakeholders. Here, we propose research avenues to generate the knowledge required to assess the risks

associated with bee management and to develop effective policies. Furthermore, we highlight challenges and list currently actionable levers to mitigate conflicts.

### Challenges towards effective conflict resolution

Measuring long-term and population-level effects of managed and wild bee interactions

Enhancing our knowledge about the effects of managed bees on wild bees requires an assessment of conservation-relevant parameters that is currently lacking. These parameters include population size and genetic diversity, which are crucial to the long-term sustainability of populations but are extremely resource-intensive or impossible to assess using classical methods based on counting bees. By comparison, genetic methods require relatively small sample sizes, provide information on genetic diversity, population demography [10], and on pathogen prevalence, loads, and transmission. The possibility of collecting bee environmental (e)DNA also provides another potential noninvasive method to assess these. The recent development of genomic tools to analyze historic samples also allows screening of museum specimens to reveal fluctuations in genetic diversity and demography over time. Such data can link variation in bee management intensity or other stressors to wild bee population sizes over time, contributing to the assessment of their respective effects and to possible mitigation measures. The need for molecular approaches is highlighted as a goal of the CBD COP15 Global Biodiversity Framework: 'Genetic diversity within populations of wild and domesticated species is maintained, safeguarding their adaptive potential'.

### Assessing the impact of pathogens

While pathogen transmission between managed and wild bees is increasingly considered a threat, which pathogens compromise wild bees, to what extent,
Box 1. The importance of contextualization in bee policies

Ecological contexts include interactions among biologically diverse bee species and their impacts on eco-
systems. Socioeconomic aspects include pollination demand, beekeeping profitability, food security
needs, and livelihood goals. A crucial aspect for contextualizing bee-oriented policies is the interplay be-
tween land-cover types and the endemism of managed species. In many regions of the world, crop polli-
nation relies on non-native managed bees. In agricultural landscapes, where pollination is mainly a
necessary economic service, the introduction of managed non-native bees to fill pollination deficits can
be acceptable. However, in urban, semi-natural, and natural habitats, where pollination is mainly an eco-
logical service, negative interactions with native bees can be less acceptable, as arguments about eco-
nomic losses are irrelevant. Developing management techniques for local populations of native bee
species could be a viable alternative to introducing non-native bees [4]. In the native ranges of managed
bee species, policy-making is more complex than in the non-native range [9]. Although they are naturally
occurring, their management can lead to unnaturally high densities, with potential negative consequences
for wild conspecifics or other pollinators. Whether it is desirable, or indeed possible, to regulate native man-
aged bee densities according to local carrying capacities and pollination requirements should be further
considered.

and in which contexts they are impacted,
remain unclear, especially for interspecific
transmission (e.g., [6]). Identifying these
contexts is crucial to accurately determine
the risks associated with bee manage-
ment. Molecular detection and phylogeny
to assess transmission patterns combined
with experimental work to test the impact
of pathogens will guide the development
of policies to regulate the localization and
densities of managed bees at levels ap-
propriate to ensure the conservation of
wild bee populations.

Before such data become available,
pre-emptive measures known to reduce
pathogen loads in managed bees (e.g.,
therapeutic treatments), and thus potential
transmission to wild bees, should be imple-
mented more consistently [11] or better
enforced [2]. Identifying the obstacles to
implementation and enforcement of good
practices through socioeconomic studies
is required. In parallel, maintaining or re-
storing diverse communities of plants and
pollinators in ecosystems can reduce the
risks associated with pathogen transmis-
sion through partitioning of foraging niches
[12].

Quantifying ecosystem carrying capacities
to mitigate competition

The intensity of competition between
organisms is modulated by resource avail-
ability and quality. Ecosystem carrying

capacities, resource niche overlaps, and
their temporal dynamics will, therefore,
influence how bee species interact.
Increasing carrying capacities to reduce
competition can be achieved through
measures such as floral enhancements
(e.g., flower strips, hedgerows) promoted
by the European Union (EU) Common
Agricultural Policy or the US Farm Bill
(e.g., programs of the Natural Resources
Conservation Service of the US Depart-
ment of Agriculture) [13]. Pollinator-friendly
enhancements of agricultural landscapes
can also decrease natural and human-
driven displacement of managed bees,
thereby decreasing the spatial range of
potential impacts.

Despite our ability to increase resources
locally, tools are lacking to estimate
ecosystem carrying capacities to match
resource availability with local wild and
managed bee community requirements.
Where increasing floral resources is
impractical, knowing the carrying capacity
of ecosystems is imperative for making
informed adjustments to managed bee
densities [14]. Deterministic models incor-
porating resource availability – as well as
spatiotemporal resource requirements
and use by local pollinator assemblages –
are promising tools to estimate the
degree of competition and the effective-
ness of mitigation measures. However,
multidisciplinary projects are required

to generate the pertinent data to optimize
such models.

Evaluating the impacts on a broader
diversity of wild bee species

Most research on the impacts of bee
competition and pathogen transmission
has focused on a restricted number of
model species that are easy to manage
or to find in the wild (e.g., buff-tailed bum-
ble bees Bombus terrestris, European or-
chard bees Osmia cornuta; [5]). The
resulting narrow range of life-history traits
considered in those studies limits our abil-
ity to provide broad predictions for diverse
native pollinator communities. Developing
methods to study other wild bee species
will decrease reliance on these few um-
brella species. Moreover, the effects of in-
terspecific competition or pathogen
spillover on wild bees are frequently tested
using managed populations of these spe-
cies. A concern with these tests is that a
managed population can be genetically
and/or phenotypically different to local
wild conspecifics, and thus does not rep-
resent the natural situation. Studying wild
populations of bees is more challenging
but can be facilitated by genetic ap-
proaches, for example, using eDNA to
quantify effective population sizes and
monitor pathogens [10].

Fostering the co-creation of policies

Due to differing values, motivations, un-
derstandings, and expectations, different
stakeholder groups (e.g., farmers, bee-
keepers, conservationists) have diverse
and sometimes contradictory views on
the management of pollinators, and on
their contributions to livelihoods and
wider society. Recognizing these views
during a co-creation process, and placing
them within the current knowledge base on
interactions between bees, is key to the de-
velopment of evidence-based policies that
consider local ecological and socioeconomic
contexts and decrease conflicts [9]
(Figure 1). The simultaneous consideration
of a multitude of factors is an essential but
<figure><img src="image_4.png" /></figure>

<figure><img src="image_5.png" /></figure>

Trends in Ecology & Evolution

<caption>Figure 1. Guidelines towards inclusive bee policy-making. Inclusive policy-making to better integrate food security and conservation needs can be developed by taking into account both available and missing knowledge in a co-creation process considering socioeconomic factors. Figure created with Biorender.com.</caption>

challenging task that requires an inclusive approach [7,9]. To enable this, key wild and managed bee proponents should be provided opportunities to co-create policies through stakeholder consultations and multi-actor knowledge synthesis [e.g., The Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES)] during which win-win solutions can be elaborated to federate both parties towards a common goal. In addition to national policies, a variety of incentives driven by local or national stakeholders (such as beekeeper associations, wild bee conservation societies, and grower groups) have great potential to foster such co-creation and reduce trade-offs resulting from conflicting goals.

## Unity for managed and wild bees

In the context of pollinator declines and increasing reliance on managed bees for crop pollination, actual and perceived negative interactions between managed and wild bees will inevitably lead to escalating conflicts. Habitat loss and climate change that alter floral resource diversity and availability will likely exacerbate these issues. Evidence-based policies to integrate conservation and food security requirements are, therefore, urgently needed. To develop such policies and move beyond precautionary principles, we suggest that more emphasis be placed on identifying the general contexts in which managed bees impact wild bees and the importance of these impacts

in relation to other bee stressors. A recent global expert assessment ranked pollinator management and associated pathogens lower than land cover, land configuration, land management, pesticide use, and climate change as drivers of pollinator declines in terms of importance and confidence level [15]. Obtaining greater confidence in the risks posed by managed bees to wild bees and other pollinators will allow effective allocation of resources towards policy-making and implementation. International scientific collaborations and interdisciplinary initiatives involving all stakeholders are key to co-create effective and context-relevant policies to reconcile food security and conservation of wild bees.
Acknowledgments

This work was supported by the Natural Sciences and
Engineering Research Council Discovery grant (2021-
04210) and the Rebanks Family Chair in Pollinator
Conservation by the Weston Family Foundation (N.E.R.),
the European Union's Horizon Europe Framework
Programme project No. 101082101 (A.M.K., S.G.P.),
the National Research foundation of South Africa, grant
number SRUG2204062235 (C.W.W.P.), The Alabama
Agricultural Experiment Station, USDA ARS Cooperative
Agreement 58-6066-3-029, and the USDA NIFA Multi-
state Hatch Project NC1173 (G.R.W.).

Declaration of interests

The authors have no interests to declare.

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<footnote n="1">¹Swiss Bee Research Centre, Agroscope, Berne 3003, Switzerland</footnote>

<footnote n="2">²Institute of Bee Health, Vetsuisse Faculty, University of Bern,
Liebefeld, 3097, Switzerland</footnote>

<footnote n="3">³School of Agriculture, Food, and Wine, University of Adelaide,
Adelaide, SA 5064, Australia</footnote>

<footnote n="4">⁴Plant Ecology and Nature Conservation Group, Wageningen
University, Wageningen, 6708, The Netherlands</footnote>

<footnote n="5">⁵School of Environmental Sciences, University of Guelph,
Guelph, ON N1G 2W1, Canada</footnote>

<footnote n="6">⁶Centre for Agri-Environmental Research, School of Agriculture,
Policy, and Development, University of Reading, Reading,
RG6 6UR, UK</footnote>

<footnote n="7">⁷Retired USDA ARS Pollinating Insects Research Unit,
Utah State University, Logan, UT 84322, USA</footnote>

<footnote n="8">⁸Institute of Botany, Ulm University, Ulm, 89081, Germany</footnote>

<footnote n="9">⁹Social Insects Research Group, Department of Zoology and
Entomology, University of Pretoria, Pretoria, 0002, South Africa</footnote>

<footnote n="10">¹⁰Department of Conservation Biology and Social-Ecological Systems, Helmholtz-Centre for Environmental Research - UFZ, Halle (Saale), 06120, Germany</footnote>

<footnote n="11">¹¹German Centre for Integrative Biodiversity Research (iDiv)
Halle-Jena-Leipzig, Leipzig, 04103, Germany</footnote>

<footnote n="12">¹²Institute of Biological Sciences, College of Arts and Sciences,
University of the Philippines Los Baños, Los Baños, 4031,
Philippines</footnote>

<footnote n="13">¹³Institute for Biology, Martin Luther University Halle-Wittenberg,
Halle (Saale), 06120, Germany</footnote>

<footnote n="14">¹⁴Department of Agricultural, Forest, and Food Sciences,
University of Turin, Torino, 10124, Italy</footnote>

<footnote n="15">¹⁵Department of Entomology and Nematology, University of California Davis, Davis, CA 95616, USA</footnote>

<footnote n="16">¹⁶Nature Conservation and Landscape Ecology, University of
Freiburg, Freiburg, 79085, Germany</footnote>

<footnote n="17">¹⁷Centre of Environmental and Climate Science,
Lund University, Lund, SE-223 62, Sweden</footnote>

<footnote n="18">¹⁸INRAE, UR 406 Abeilles et Environnement, Avignon, 84914,
France</footnote>

<footnote n="19">¹⁹US Department of Agriculture, Agricultural Research Service,
Sidney, MT 59270, USA</footnote>

<footnote n="20">²⁰Department of Entomology and Plant Pathology,
Auburn University, Auburn, AL 36849, USA</footnote>

<footnote n="21">²¹DAFNAE, University of Padova, Padova, 35020, Italy</footnote>

<footnote n="22">²²National Centre for Biological Sciences, Tata Institute of
Fundamental Research, Bengaluru, 560097, India</footnote>

<footnote n="23">²³Dipartimento di Scienze e Tecnologie Agro-alimentari,
Alma Mater Studiorum Università di Bologna, Bologna, 40127, Italy</footnote>

<footnote n="24">²⁴Department of Entomology, Center for Pollinator Research,
Penn State University, University Park, PA 16802, USA</footnote>

<footnote n="25">²⁵Animal GenoPhenomics, Agroscope, Posieux, 1725,
Switzerland</footnote>

<footnote n="26">²⁶Centre for Ecology Evolution and Behaviour, Department of
Biological Sciences, Royal Holloway University of London
Egham, Egham, TW20 0EX, UK</footnote>

<footnote n="27">²⁷Faculty of Science, Energy, and Environment, King Mongkut's
University of Technology North Bangkok, Rayong, 10800,
Thailand</footnote>

<footnote n="28">²⁸Agroecology and Environment, Agroscope, Zurich, 8046,
Switzerland</footnote>

<footnote n="29">²⁹Department Ecology and Evolution, University of Lausanne,
Lausanne, 1015, Switzerland</footnote>

<footnote>*Correspondence:
alexis.beaurepaire@agroscope.admin.ch (A.L. Beaurepaire).</footnote>

<footnote>https://doi.org/10.1016/j.tree.2024.11.009</footnote>

<footnote>© 2024 The Authors. Published by Elsevier Ltd. This is an open
access article under the CC BY license (http://creativecommons.
org/licenses/by/4.0/).</footnote>