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Citizen Science contributes significantly to the conservation of biodiversity, but its application to honey bee research has remained minimal. Even though certain European honey bee (Apis mellifera) populations are known to naturally survive Varroa destructor infestations, it is unclear how widespread or common such populations are. Such colonies are highly valuable for investigating the mechanisms enabling colony survival, as well as for tracking the conservation status of free-living honey bees. Here, we use targeted Citizen Science to identify potentially new cases of managed or free-living A. mellifera populations that survive V. destructor without mite control strategies. In 2018, a survey containing 20 questions was developed, translated into 13 languages, and promoted at beekeeping conferences and online. After three years, 305 reports were collected from 28 countries: 241 from managed colonies and 64 from free-living colonies. The collected data suggest that there could be twice as many naturally surviving colonies worldwide than are currently known. Further, online and personal promotion seem to be key for successful recruitment of participants. Although the survivor status of these colonies still needs to be confirmed, the volume of reports and responses already illustrate how effectively Citizen Science can contribute to bee research by massively increasing generated data, broadening opportunities for comparative research, and fostering collaboration between scientists, beekeepers, and citizens. The success of this survey spurred the development of a more advanced Citizen Science platform, Honey Bee Watch, that will enable a more accurate reporting, confirmation, and monitoring of surviving colonies, and strengthen the ties between science, stakeholders, and citizens to foster the protection of both free-living and managed honey bees.
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Insects 2021, 12, 536. https://doi.org/10.3390/insects12060536 www.mdpi.com/journal/insects
Article
Using Citizen Science to Scout Honey Bee Colonies that
Naturally Survive Varroa destructor Infestations
Arrigo Moro 1,*, Alexis Beaurepaire 1, Raffaele Dall’Olio 2, Steve Rogenstein 3, Tjeerd Blacquière 4, Bjørn Dahle 5,6,
Joachim R. de Miranda 7, Vincent Dietemann 8,9, Barbara Locke 7, Rosa María Licón Luna 10, Yves Le Conte 11 and
Peter Neumann 1
1 Institute of Bee Health, Vetsuisse Faculty, University of Bern, 3003 Bern, Switzerland;
alexis.beaurepaire@vetsuisse.unibe.ch (A.B.); peter.neumann@vetsuisse.unibe.ch (P.N.)
2 BeeSources, 40132 Bologna, Italy; raffaele.dallolio@gmail.com
3 The Ambeessadors, 10439 Berlin, Germany; ambeessadors@gmail.com
4 Wageningen Plant Research, Wageningen University & Research, 6708 PB 1 Wageningen & Blacqbee, 141
RK 18 Aalsmeer, The Netherlands; blacqbee@blacqbee.nl
5 Norwegian Beekeepers Association, NO-2040 Kløfta, Norway; bjorn.dahle@norbi.no
6 Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sci-
ences, 1433 Ås, Norway
7 Department of Ecology, Swedish University of Agricultural Sciences, 750 07 Uppsala, Sweden;
joachim.de.miranda@slu.se (J.R.d.M.); barbara.locke@slu.se (B.L.)
8 Swiss Bee Research Center, Agroscope, 3003 Bern, Switzerland; vincent.dietemann@agroscope.admin.ch
9 Department of Ecology and Evolution, Biophore, UNIL-Sorge, University of Lausanne, 1015 Lausanne,
Switzerland
10 Wild Bees Project, 01170 Crozet, France; romaliconluna@live.com
11 UR 406 Abeilles et Environnement, INRAE, 84914 Avignon, France; yves.le-conte@inrae.fr
* Correspondence: arrigo.moro@vetsuisse.unibe.ch
Simple Summary: Citizen Science is a valuable resource that can substantially contribute to the
conservation of biodiversity. However, its use in honey bee research has remained minimal. The
Survivors Task Force of the COLOSS association created and promoted an online surveying tool
with the aim of identifying potential cases of Western honey bee, Apis mellifera, populations that are
surviving infestations with ectoparasitic mites Varroa destructor without control measures by bee-
keepers. The reports suggest that there could be twice as many naturally surviving colonies world-
wide than are currently known. The survey also shows that citizens can be readily engaged through
social media, personal networks, and promotional campaigns to gather valuable and previously
inaccessible data. These reports of surviving honey bee colonies will now be validated through the
new initiative Honey Bee Watch, a global and multi-year Citizen Science project founded to connect
citizens, beekeepers, and scientists. This will enable to increase scientific knowledge, mitigate honey
bee colony losses, and develop education and conservation campaigns.
Abstract: Citizen Science contributes significantly to the conservation of biodiversity, but its appli-
cation to honey bee research has remained minimal. Even though certain European honey bee (Apis
mellifera) populations are known to naturally survive Varroa destructor infestations, it is unclear how
widespread or common such populations are. Such colonies are highly valuable for investigating
the mechanisms enabling colony survival, as well as for tracking the conservation status of free-
living honey bees. Here, we use targeted Citizen Science to identify potentially new cases of man-
aged or free-living A. mellifera populations that survive V. destructor without mite control strategies.
In 2018, a survey containing 20 questions was developed, translated into 13 languages, and pro-
moted at beekeeping conferences and online. After three years, 305 reports were collected from 28
countries: 241 from managed colonies and 64 from free-living colonies. The collected data suggest
that there could be twice as many naturally surviving colonies worldwide than are currently known.
Further, online and personal promotion seem to be key for successful recruitment of participants.
Although the survivor status of these colonies still needs to be confirmed, the volume of reports and
responses already illustrate how effectively Citizen Science can contribute to bee research by
Citation:
Moro, A.; Beaurepaire, A.;
Dall’Olio, R.; Rogenstein, S.;
Blacquière, T.; Dahle, B.;
de Miranda, J.R.; Dietemann, V.;
Locke, B.; Licón Luna, R.M.; et al.
Using Citizen Sci
ence to Scout
Honey Bee Colonies
that Naturally
Survive
Varroa destructor
Infestations.
Insects 2021, 12, 536.
https://doi.org/10.3390/insects
12060536
Academic Editor
s:
Cristina Castracani and
Alessandro Campanaro
Received: 21 May 2021
Accepted:
6 June 2021
Published:
9 June 2021
Publisher’s Note:
MDPI stays neu-
tral with regard to jurisdictional
claims in published maps and institu-
tional affiliations.
C
opyright: © 2021 by the authors. Li-
censee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and con-
ditions of the Creative Commons At-
tribution (CC BY) license (http:
//crea-
tivecommons.org/licenses/by/4.0/).
Insects 2021, 12, 536 2 of 12
massively increasing generated data, broadening opportunities for comparative research, and fos-
tering collaboration between scientists, beekeepers, and citizens. The success of this survey spurred
the development of a more advanced Citizen Science platform, Honey Bee Watch, that will enable
a more accurate reporting, confirmation, and monitoring of surviving colonies, and strengthen the
ties between science, stakeholders, and citizens to foster the protection of both free-living and man-
aged honey bees.
Keywords: citizen science; COLOSS; honey bee; honey bee watch; monitoring; natural selection;
Varroa destructor
1. Introduction
Citizen Science is an effective tool for engaging the general public in research pro-
jects. It is most commonly used in media-friendly subjects such as ecology and conserva-
tion [14]. By definition, this discipline relies on the active involvement of the public in
the provision of data and the co-creation of scientific knowledge [5,6]. For scientists, this
offers many opportunities, such as real-time access to large-scale data and direct contact
with both citizens and practitioners [7]. Citizen Science simultaneously offers citizens the
opportunity to partake in research questions that interest them, while also providing the
possibility of advancing their education [8], with multiple benefits to all actors involved
[9,10]. As such, the use of Citizen Science for facing the multiple challenges affecting
global biodiversity has been widely increasing, even in bee research [11]. However, de-
spite the need to mitigate the current global health crisis affecting Western honey bees, A.
mellifera [12,13], Citizen Science almost exclusively focused on the quantification of winter
losses of managed colonies [11] and has not yet been capitalized for finding possible so-
lutions to this problem.
Severe losses of managed colonies of Western honey bees have in fact been thor-
oughly monitored in the last decades [14] and the ectoparasitic mite Varroa destructor has
been widely recognized as one of the major drivers of these losses. Generally, infestations
with this parasite lead to the death of a colony within two years unless appropriate control
measures are taken [15]. Beekeepers worldwide therefore rely on mite control measures
(primarily regular acaricide treatments), in order to keep their stocks alive [16]. However,
these acaricides vary in efficacy, are prone to resistance development by the mites and
contaminate hive products and can thus only be used outside the foraging season [17]. As
it stands, chemical treatments therefore do not represent a long-term solution to V. destruc-
tor [17]. Non-chemical alternative treatments have also been developed [18], but are cur-
rently not widely used and represent an increased work load for the beekeepers. The dis-
covery of naturally V. destructor-surviving populations [19,20] led to the realization that
the Western honey bee possesses certain traits enabling their survival without the need
for mite control [21], similar to what is observed in the original host Apis cerana [22]. This
encouraged scientists and beekeepers to search for or establish A. mellifera populations
capable of surviving V. destructor infestation without mite control [20] in order to identify
traits that are most amenable to natural or artificial selection [19,21,23]. Unfortunately,
identifying or establishing such populations takes much time and effort, leading to a re-
search that focuses on only a few populations [19]. However, considering a more diverse
group of V. destructor-surviving A. mellifera populations that undoubtedly exist [24] would
provide increased opportunities to investigate known survival mechanisms and discover
novel ones. Moreover, a diversity of naturally surviving populations could represent an
important asset for the re-establishment of A. mellifera in the wild.
European A. mellifera populations have been considered almost extinct in the wild as
a consequence of the spread of V. destructor [25]. However, recent evidence suggests that
free-living honey bee colonies can survive in the wild in a self-sustainable manner [26
30]. Despite these few occurrences, there remains a large gap of knowledge on the current
Insects 2021, 12, 536 3 of 12
abundance, distribution, and diversity of free-living A. mellifera populations. As their
identification is most efficiently achieved with large-scale coordinated efforts, it appears
high time to mobilize Citizen Scientists for a large-scale survey on this topic.
Beekeepers represent the major stakeholders upon which honey bee health ulti-
mately depends [31,32]. Their participation in bee health research is therefore both desir-
able and mutually beneficial. Furthermore, the recent development of online surveying
platforms makes it much easier to involve stakeholders such as beekeepers as well as the
general public in participatory research [33]. As the level of contribution among users of
such platforms is often uneven [7], the use of multiple communication channels, including
social media and newsletters, can foster wider and more representative engagement by
citizens [34]. Here, we present the outcome of an online survey organized by the members
of “Survivors”, a Task Force within the COLOSS (Prevention of honey bee COlony
LOSSes; www.coloss.org, accessed on 7 June 2021) association, aimed at both beekeepers
and the general public, for mapping and identifying new cases of A. mellifera colonies that,
either in the wild or in managed apiaries, survive V. destructor infestation without the need
for mite control.
2. Materials and Methods
In March 2018, during a COLOSS Survivors Task Force workshop in Bern, Switzer-
land, an online survey was created (Figure 1) and later translated into 13 languages: Chi-
nese, Dutch, English, French, German, Italian, Norwegian, Russian, Serbian, Slovenian,
Spanish, Swedish, and Ukrainian. The survey was developed using the Google® Form
platform, activated and made accessible from the Survivors Task Force webpage
(https://coloss.org/taskforces/survivors/, accessed on 7 June 2021). The survey was simul-
taneously disseminated through local national beekeeping networks of the COLOSS Sur-
vivors Task Force members through a variety of channels. The initiative was further pro-
moted during a beekeeping conference in the Netherlands in 2018, followed by a passive
online campaign using social networks.
The survey started with an introductory question asking the responder for possible
cases of surviving A. mellifera populations (Figure 1). As the survey aimed at identifying
surviving honey bee populations, rather than individual colonies, a stipulation was in-
cluded to only submit reports of a minimum of five surviving colonies from managed
beekeeping operations. This requirement was not imposed for free-living survivors,
which inevitably are well-dispersed individual colonies, wherever they are found (Figure
1). Depending on the answer to the introductory question, the user was directed to one of
three sections (Figure 1). The first section concerned managed surviving colonies and con-
tained seven questions. These questions aimed at collecting data regarding the general
location of each case (i.e., region and city name), the number of years these colonies was
known to survive without mite control, the number of colonies in the surviving group at
the date of the report, and finally the proportion of colonies that needed to be replaced
annually to maintain the population size, as a measure of the population’s ability to sur-
vive V. destructor unaided. The second section concerned possible cases of free-living sur-
vivors and contained a single question about the general location of the colony, together
with an open-text field to provide other relevant information. The third section combined
questions from Sections 1 and 2, for users reporting cases of both managed and free-living
surviving colonies. At the end of the survey, the user was given the possibility to submit
a personal contact, for future case validation and collaborative research (Figure 1). The
respondents personal data were treated confidentially, in compliance with the General
Data Protection Regulations (GDPR) of the European Union [35].
Insects 2021, 12, 536 4 of 12
Figure 1. Flow diagram of the online survey on honey bee, Apis mellifera, colonies surviving infesta-
tions with Varroa destructor without acaricidal treatments. The first question directed respondents
to one of three sections, depending on whether they intended to report cases of managed A. mellifera
colonies surviving without conventional treatment against V. destructor (left), free-living surviving
A. mellifera colonies (middle), or both (right).
In January 2021, the reports were compiled and screened to remove duplicate reports
and cases already known to science. The compiled data set was analyzed statistically with
respect to a range of factors relevant to the aims of the project, using R software [36]. For
potentially stable surviving populations of managed survivors, the reports were ranked
in three classes: gold, silver”, and bronze, according to the reported survival time,
the number of colonies in the group, and the annual proportion of colony replacement.
For all classes, the minimum requirement for inclusion was an annual replacement rate of
less than 50%. Cases reporting more than 30 colonies surviving for more than 10 years
were considered as the goldstandard. Next, groups surviving more than 10 years but
Insects 2021, 12, 536 5 of 12
involving fewer than 30 colonies, were considered silver class. Last, groups of more than
30 colonies surviving for a period between five and ten years, were considered as bronze
class. All reports falling outside these criteria were included into a fourth class.
Additional voluntary information added to reports on free-living colonies were ana-
lyzed qualitatively.
3. Results
In total, 305 reports were collected from 28 countries (Figure 2; Table 1), comprising
64 reports on free-living colonies and 241 on managed colonies. The majority of users pro-
vided a contact for future case confirmation (N = 216, 86%). Most of the reports were from
the United Kingdom (N = 86, 28%), The Netherlands (N = 77, 25%), and the USA (N = 68,
22%).
Figure 2. Global reach of the COLOSS Survivors Task Force online survey on possible cases of honey
bee, Apis mellifera, colonies that, in an apiary or free-living, are surviving Varroa destructor mite in-
festations in the absence of chemical treatments. Regions indicated by respondents are highlighted
with different colors, depending on the type of surviving colonies (managed, only free-living, or
both). The majority of reports were submitted from UK, The Netherlands, and USA.
Overall, only a few reports were submitted on possible cases of free-living colonies
(N = 64, 20%, Table 1). Respondents consistently provided the general locations in which
these colonies were located (Table 1), and a large proportion also provided voluntary ad-
ditional information on each case (N = 48, 75%). From this information, a count of the
reports that mentioned the type of nests in which the free-living colonies resided (N = 35,
72%) or whether the respondent monitored these nests (N = 20, 41%) could be extracted
purposefully (Table 2).
Insects 2021, 12, 536 6 of 12
Table 1. Number of reports, divided per category, collected by the COLOSS Survivors Task Force survey on putative cases
of untreated A. mellifera colonies surviving V. destructor infestation. The country in which these colonies were reported to
occur is specified.
Category of Answer
Number of Answers
Countries
Managed survivors 241
Bangladesh (1), Belgium (12), Canada
(3), Colombia (1), Egypt (2), Finland
(2), France (1), Germany (1), India (3),
Iran (1), Ireland (1), Israel (1), Italy (16),
Kenya (1), Lithuania (3), Netherlands
(62), Poland (1), Portugal (4), Romania
(1), Saudi Arabia (1), Serbia (1), Spain
(1), Switzerland (3), Thailand (1), Tur-
key (1), UK (63), USA (53)
Free-living survivors 64
Austria (1), Belgium (1), France (1), Ire-
land (2), Italy (1), Kenya (1), Nether-
lands (15), Portugal (2), Serbia (1),
Spain (1), UK (23), USA (15)
Total
305
Table 2. Counts and proportions of users who did or did not submit case-specific information on
free-living colonies to the COLOSS Survivors Task Force survey. In total, 64 reports on free-living
colonies were submitted. The counts and proportions of instances in which the type of nests was
mentioned are also given, together with those in which the user reported to be voluntarily monitor-
ing the colonies.
Types of Response
Number of Answers
Percentage
Reported information
48
75%
No reported information
16
25%
Described nest type
35
54%
Voluntary monitoring
20
31%
When reporting about managed surviving colonies (Total N = 241), almost all re-
spondents (N = 224, 93%) indicated the number of colonies composing the group. Among
these, 195 (87%) described groups of five to 30 colonies, 44 (22%) of which untreated and
surviving for less than three years, 70 (36%) for a period between three and five years, 51
(26%) for a period between five and 10 years, and 30 (15%) for more than 10 years (Figure
3). Few respondents described managed groups consisting of more than 30 colonies (N =
29), of which 6 (20%) were untreated and surviving for less than five years, 11 (37%) for a
period between five and 10 years, and 12 (41%) for more than 10 years (Figure 3).
Insects 2021, 12, 536 7 of 12
Figure 3. Time span over which the reported managed honey bee, Apis mellifera, colonies were not
subjected to treatments against Varroa destructor. The number of answers from the COLOSS survey
is shown (dark gray = surviving populations with >30 colonies, N = 29; light gray = groups between
five and 30 colonies, N = 195).
Respondents reporting of managed surviving colonies also indicated the proportion
of colonies that needed to be replaced annually in order to maintain the stock (Figure 4).
Among these, the majority (N = 160, 80%) reported replacing less than one-quarter of the
colonies per year (Figure 4), while the remaining respondents reported replacing between
one-quarter and one-half of the colonies in their stock (N = 32, 16%, Figure 4) per year.
Another eight (4%) reports indicated an annual replacement rate of more than one-half.
Because these high rates suggest that these colonies did not develop a stable relationship
with V. destructor, these eight reports were not considered as potential survivors and were
excluded.
Interestingly, 44 reports (18%) collected on managed, untreated groups could be clas-
sified as potentially stable populations of survivors as nine gold, 25 silver, and 10 bronze
cases were found (Figure 5).
Figure 4. Annual colony replacement rate in groups of managed honey bee, Apis mellifera, colonies
not treated against parasitic mites Varroa destructor. The number of answers from the COLOSS Sur-
vivors Task Force survey is shown (dark gray = groups with >30 colonies, N = 26; light gray = groups
between five and 30 colonies, N = 174).
0
20
40
60
<3 years 3 to 5 years 5 to 10 years >10 years
Reported time without conventional treatments
Number of answers
Insects 2021, 12, 536 8 of 12
Figure 5. Counts of reports on potentially self-sustaining managed A. mellifera populations surviv-
ing Varroa destructor based on group composition, proportion of annual colony replacement, and
untreated period as collected by the COLOSS Survivors Task Force survey. The reports are divided
by classes (gold, silver, and bronze) and regions. Dark gray = cases for which a replacement rate
between 25 and 50% was reported; light gray = cases for which a replacement rate lower than 25%
was reported. Gold class (N = 9) was defined by managed groups of colonies composed of more
than 30 colonies with an annual replacement rate below 50% and untreated for more than 10 years.
Silver class (N = 25) were managed groups of colonies composed of a number between five and 30
colonies with an annual replacement rate below 50% and untreated for more than 10 years. Bronze
class (N = 10) were managed groups of colonies composed of more than 30 colonies with an annual
replacement rate below 50% and untreated for a period between five and 10 years. Only cases pre-
viously unknown to scientific literature have been included.
4. Discussion
By providing access to previously unreported cases of untreated A. mellifera colonies
potentially surviving V. destructor infestations without treatments, this survey will help
improve our understanding of the mechanisms underlying survival of colonies. The out-
put of this survey further illustrates the potential of Citizen Science to provide valuable
and large-scale data for solving the major health problems that Western honey bees are
currently facing worldwide.
Despite a low investment in online and personal communications to promote the
survey, its outreach was substantial. Notably, it engaged responders from continents not
included in previous COLOSS surveys [14]. Interestingly, the majority of reports were
collected from three countries: United Kingdom, the Netherlands, and the USA (Table 1).
This pattern seems to largely stem from the way by which the survey was promoted. Most
answers were submitted after the authors personally promoted the survey during a con-
ference held in the Netherlands in 2018, at which attendees were mostly local or from the
UK and USA. Following this event, a modest social media campaign was launched to fur-
ther promote the survey within the conference attendee’s networks. Moreover, in the
same period, the link to the survey was also spread to Dutch beekeepers through an online
newsletter. As has been the case for other citizen science initiatives [6], the recruitment of
participants through personal engagement and the use of online and social media plat-
forms appeared to have been crucial for the successful dissemination of this initiative.
The survey of the COLOSS Survivors Task Force lists among the few scientific initi-
atives aimed at mapping free-living and surviving A. mellifera colonies on an international
scale [30]. In the northern hemisphere, free-living colonies are considered to be very rare
[25,37] and are notoriously difficult to spot in the field [28]. As a consequence, few reports
Insects 2021, 12, 536 9 of 12
(i.e., 20% of the total answers, Table 1) were collected on such cases in comparison to man-
aged colonies. The data collected on free-living colonies provided only an indication of
their locations (Table 1). A comparative analysis of the data derived from these cases was
not possible given that the majority of information collected consisted of anecdotal re-
ports. Most likely, this was due to the lack of precise instructions given to users when
submitting information on such colonies (Figure 1). Yet, more than one-third of the re-
sponses collected suggested that responders were voluntarily monitoring the free-living
colonies known to them (Table 2). This considerable level of public engagement is prom-
ising and suggests that there are good perspectives for successfully implementing a more
advanced version of this Citizen Science tool capable of obtaining more detailed data on
free-living honey bee colonies. This is the goal of a follow-up initiative developed by a
core team of members within the COLOSS Survivors Task Force. The team launched
Honey Bee Watch (www.honeybeewatch.com, accessed on 7 June 2021), which aims at
pursuing this study in greater depth, over a much longer timeframe, and with a much
wider scope that includes all Apis species so to provide more data over their distribution
and conservation status [38,39].
The potential cases of survivors managed by beekeepers collected in the survey may
substantially contribute to the number of previously known cases of untreated popula-
tions of Western honey bees surviving V. destructor infestation. Current scientific literature
indicates that approximately 20 untreated and surviving populations are managed by bee-
keepers/breeders or are part of scientific projects [20,4051]. The answers collected from
this survey reported twice as many cases, the majority of which in regions with no previ-
ously reported cases (Figure 5). The data also suggest that some of these honey bee colo-
nies may have reached a stable equilibrium with V. destructor, as the majority of respond-
ents reported an annual colony replacement rate <25% (Figure 5). This indicates adapta-
tions of both the honey bee host to the selection pressure imposed by the parasite [23,43]
and the local mites to its host [52]. Yet, despite the promising data obtained, these poten-
tial novel cases need to be confirmed via thorough investigation and long-term monitor-
ing before they can be considered as surviving mite infestations. With each respondents
approval, and after funding has been secured, phenotypic and molecular tests will be per-
formed by the Honey Bee Watch study on gold, silver, and bronze cases. Inspired by the
level of citizens’ engagement that the present initiative generated, Honey Bee Watch will
initiate a more strategically focused communication campaign to continue collecting data
on untreated and free-living honey bee colonies.
5. Conclusions
Given the relevant contributions that Citizen Science initiatives have demonstrated
in multiple conservation and ecological studies [2], using this tool to investigate the extent
of A. mellifera populations surviving V. destructor without treatments appears both mean-
ingful and fruitful. Through the COLOSS Survivors Task Force survey, beekeepers, and
citizens, incentivized by social media and promotional campaigns, were motivated to sub-
mit data on and monitor untreated and free-living colonies. In the process, they have be-
come a valuable reporting resource on potentially self-sustainable and V. destructor sur-
viving A. mellifera populations. As the initiative reported here has ended, the results gath-
ered are calling for case validation and the development of a more advanced citizen sci-
ence platform. To fulfil such aims, COLOSS Survivors Task Force members initiated
Honey Bee Watch (www.honeybeewatch.com, accessed on 7 June 2021), aimed at expand-
ing data collection on untreated, surviving, and free-living honey bee colonies. Overall,
this initiative, together with the results obtained from the scientific validation of the cases
presented here, may ultimately demonstrate how bridging the gap between scientists,
practitioners, and citizens can help discover solutions to promote large-scale conservation
of biodiversity.
Insects 2021, 12, 536 10 of 12
Author Contributions: Conceptualization, A.M., P.N., A.B., R.D., S.R., T.B., B.D., J.R.d.M., V.D., B.L.,
R.M.L.L., and Y.L.C.; methodology, A.M., P.N., A.B., R.D., S.R., T.B., B.D., J.R.d.M., V.D., B.L.,
R.M.L.L., and Y.L.C.; software, A.M.; formal analysis, A.M.; data curation, A.M.; writingoriginal
draft preparation, A.M.; writingreview and editing, A.M., P.N., A.B., R.D., S.R., T.B., B.D.,
J.R.d.M., V.D., B.L., R.M.L.L., and Y.L.C.; funding acquisition, P.N. All authors have read and agreed
to the published version of the manuscript.
Funding: This research was funded by the UniBe international 2021 program of the University of
Bern (A.M., P.N.) and by the Vinetum Foundation (P.N.) Financial support was provided to
COLOSS by the Ricola Foundation Nature & Culture and Véto-pharma.
Institutional Review Board Statement: Not applicable.
Data Availability Statement: Data used in the submitted manuscript can be available after reason-
able request to the corresponding author. Personal data of survey respondents will not be provided
as it would violate privacy laws.
Acknowledgments: The authors thank all the responders that submitted reports to the survey and
contributed to its dissemination. We also thank Melissa Oddie and Robin F.A. Moritz from the
COLOSS Survivors Task Force for the fruitful discussions and their input in composing the first
draft of the survey and Jonathan Powell of the National Beekeeping Trust for disseminating and
promoting our initiative.
Conflicts of Interest: The authors declare no conflicts of interest.
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... However, it is not clear whether the parasite inevitably causes naïve wild-living honeybees to go entirely extinct because, on the population level, frequent reproduction by established colonies might level out colony losses [28][29][30]. There is a growing number of reports from Europe documenting the occurrence of honeybee colonies nesting wild in various types of cavities and habitats [7,14,17,[31][32][33][34][35][36], but we currently lack detailed studies of their population dynamics. ...
... While 'bee-lining', the tracing of honeybees from artificial feeding sites to their homes, can be used as an unbiased search method [44], finding actual nests (and not only their approximate locations) is very time-consuming [7,32,44,45]. Hence, the most used method is asking the public for help [17,26,31,34,46,47]. The downside of citizen science is that the reported colonies are typically scattered over a large area, so that researchers further rely on many volunteers to collect data on survival rates, potentially compromising data quality. ...
... In recent years, several studies have reported on the occurrence of wild-living honeybee colonies in Europe [7,14,17,31,32,[34][35][36]. In the few cases where colony densities were estimated, the numbers were comparable to those reported here (rural avenues in Poland [14]: 0.1 km −2 ; Hainich National Park, Germany [7]: 0.13 km −2 ; agricultural landscape in northwest Spain [36]: 0.17-0.22 ...
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European honeybee populations are considered to consist only of managed colonies, but recent censuses have revealed that wild/feral colonies still occur in various countries. To gauge the ecological and evolutionary relevance of wild-living honeybees, information is needed on their population demography. We monitored feral honeybee colonies in German forests for up to 4 years through regular inspections of woodpecker cavity trees and microsatellite genotyping. Each summer, about 10% of the trees were occupied, corresponding to average densities of 0.23 feral colonies km−2 (an estimated 5% of the regional honeybee populations). Populations decreased moderately until autumn but dropped massively during winter, so that their densities were only about 0.02 colonies km−2 in early spring. During the reproductive (swarming) season, in May and June, populations recovered, with new swarms preferring nest sites that had been occupied in the previous year. The annual survival rate and the estimated lifespan of feral colonies (n = 112) were 10.6% and 0.6 years, respectively. We conclude that managed forests in Germany do not harbour self-sustaining feral honeybee populations, but they are recolonized every year by swarms escaping from apiaries.
... Despite the devastating impact of Varroa mites on honey bee health, some populations have been able to mitigate the effects of mite infestation in the absence of management or treatment Moro et al. 2021;Oddie et al. 2021). Le Conte and Mondet examined Varroa resistant honey bee colonies in France to understand the underlying mechanisms by which some bee populations persist. ...
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Global pollinator declines threaten food production and natural ecosystems. The drivers of declines are complicated and driven by numerous factors such as pesticide use, loss of habitat, rising pathogens due to commercial bee keeping and climate change. Halting and reversing pollinator declines will require a multidisciplinary approach and international cooperation. Here, we summarize 20 presentations given in the symposium ‘Protecting pollinators and our food supply: Understanding and managing threats to pollinator health’ at the 19th Congress of the International Union for the Study of Social Insects in San Diego, 2022. We then synthesize the key findings and discuss future research areas such as better understanding the impact of anthropogenic stressors on wild bees.
... (large parts of Europe). Finally, this activity for the first time introduced citizen science to the broad bee science community, with the CSI meme living on in the Varroa Task Force Soroker et al., 2022) and the involvement of beekeepers, a central point in COLOSS, in other recent large scale citizen science projects (Dall'Olio et al., 2022;Moro et al., 2021). ...
... Successful cohabitation with Varroa is well known in closely related Asian species (Apis cerana), which co-evolved with this parasite [23]. Understanding the mechanisms behind these interactions might provide clues for improving the health status and fitness of managed A. mellifera colonies and securing perspectives for sustainable beekeeping [41][42][43][44]. In that respect, various studies focused on genetic differences between feral and managed colonies [31], or on more efficient hygienic and grooming behaviors [35,45] that might have evolved in colonies left untreated against parasites. ...
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It is assumed that wild honey bees have become largely extinct across Europe since the 1980s, following the introduction of exotic ectoparasitic mite (Varroa) and the associated spillover of various pathogens. However, several recent studies reported on unmanaged colonies that survived the Varroa mite infestation. Herewith, we present another case of unmanaged, free-living population of honey bees in SE Europe, a rare case of feral bees inhabiting a large and highly populated urban area: Belgrade, the capital of Serbia. We compiled a massive data-set derived from opportunistic citizen science (>1300 records) during the 2011–2017 period and investigated whether these honey bee colonies and the high incidence of swarms could be a result of a stable, self-sustaining feral population (i.e., not of regular inflow of swarms escaping from local managed apiaries), and discussed various explanations for its existence. We also present the possibilities and challenges associated with the detection and effective monitoring of feral/wild honey bees in urban settings, and the role of citizen science in such endeavors. Our results will underpin ongoing initiatives to better understand and support naturally selected resistance mechanisms against the Varroa mite, which should contribute to alleviating current threats and risks to global apiculture and food production security.
... Citizen science is becoming increasingly applied in ecological studies and also in bee research (Koffler et al., 2021;Miller-Rushing et al., 2012;Moro et al., 2021). The involvement of interested citizens has many advantages. ...
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Pollen metabarcoding is emerging as a powerful tool for ecological research and offers unprecedented scale in citizen science projects for environmental monitoring via honey bees. Biases in metabarcoding can be introduced at any stage of sample processing and preservation is at the forefront of the pipeline. While in metabarcoding studies pollen has been preserved at − 20 °C (FRZ), this is not the best method for citizen scientists. Herein, we compared this method with ethanol (EtOH), silica gel (SG) and room temperature (RT) for preservation of pollen collected from hives in Austria and Denmark. After ~ 4 months of storage, DNAs were extracted with a food kit, and their quality and concentration measured. Most DNA extracts exhibited 260/280 absorbance ratios close to the optimal 1.8, with RT samples from Austria performing slightly worse than FRZ and SG samples (P < 0.027). Statistical differences were also detected for DNA concentration, with EtOH samples producing lower yields than RT and FRZ samples in both countries and SG in Austria (P < 0.042). Yet, qualitative and quantitative assessments of floral composition obtained using high-throughput sequencing with the ITS2 barcode gave non-significant effects of preservation methods on richness, relative abundance and Shannon diversity, in both countries. While freezing and ethanol are commonly employed for archiving tissue for molecular applications, desiccation is cheaper and easier to use regarding both storage and transportation. Since SG is less dependent on ambient humidity and less prone to contamination than RT, we recommend SG for preserving pollen for metabarcoding. SG is straightforward for laymen to use and hence robust for widespread application in citizen science studies.
... The involvement of citizen scientists is common in ecological research [44][45][46]. Beekeepers, as a group of citizens with special knowledge and equipment, have been employed in several scientific investigations on bees [47][48][49][50]. ...
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Most Varroa induced colony losses occur during the autumn or winter season as a consequence of an elevated Varroa infestation level and an insufficient health status of the adult bees. Even with an initial low Varroa infestation in early spring, critical mite and virus infection levels can be reached before winter if colonies continuously rear brood throughout the whole season. To overcome this challenge, beekeepers can artificially interrupt brood production by suitable management procedures, depending on their type of beekeeping operation. To assess their efficacy, associated workload, and impact on colony development, different methods for brood interruption (queen caging with the combination of oxalic acid treatment, total brood removal, trapping comb technique) were tested during two seasons in 11 locations on 370 colonies in 10 European countries. A protocol was developed to standardize the methods’ application across different environmental conditions. The efficacy of queen caging depended on the mode of oxalic acid application and ranged from 48.16% to 89.57% mite removal. The highest efficacies were achieved with trickling a 4.2% solution (89.57%) and with the sublimation of 2 g of oxalic acid (average of 88.25%) in the broodless period. The efficacy of the purely biotechnical, chemical-free trapping comb and brood removal methods did not differ significantly from the queen caging groups. We conclude that a proper application of one of the described brood interruption methods can significantly contribute to an efficient Varroa control and to the production of honey bee products meeting the highest quality and food-safety standards.
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The parasitic mite, Varroa destructor, has shaken the beekeeping and pollination industries since its spread from its native host, the Asian honey bee (Apis cerana), to the naïve European honey bee (Apis mellifera) used commercially for pollination and honey production around the globe. Varroa is the greatest threat to honey bee health. Worrying observations include increasing acaricide resistance in the varroa population and sinking economic treatment thresholds, suggesting that the mites or their vectored viruses are becoming more virulent. Highly infested weak colonies facilitate mite dispersal and disease transmission to stronger and healthier colonies. Here, we review recent developments in the biology, pathology, and management of varroa, and integrate older knowledge that is less well known.
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The ectoparasitic mite Varroa destructor is the most significant pathological threat to the western honey bee, Apis mellifera, leading to the death of most colonies if left untreated. An alternative approach to chemical treatments is to selectively enhance heritable honey bee traits of resistance or tolerance to the mite through breeding programs, or select for naturally surviving untreated colonies. We conducted a literature review of all studies documenting traits of A. mellifera populations either selectively bred or naturally selected for resistance and tolerance to mite parasitism. This allowed us to conduct an analysis of the diversity, distribution and importance of the traits in different honey bee populations that can survive V. destructor globally. In a second analysis, we investigated the genetic bases of these different phenotypes by comparing ’omics studies (genomics, transcriptomics, and proteomics) of A. mellifera resistance and tolerance to the parasite. Altogether, this review provides a detailed overview of the current state of the research projects and breeding efforts against the most devastating parasite of A. mellifera. By highlighting the most promising traits of Varroa-surviving bees and our current knowledge on their genetic bases, this work will help direct future research efforts and selection programs to control this pest. Additionally, by comparing the diverse populations of honey bees that exhibit those traits, this review highlights the consequences of anthropogenic and natural selection in the interactions between hosts and parasites.
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Citizen science is a powerful tool for connecting members of the public with research and for obtaining large amounts of data. However, it is far less commonly implemented in developing countries than in developed countries. We conducted a large-scale citizen-science program monitoring honey bee (Apis mellifera) colony losses in Argentina to examine how a national consortium composed of local coordinators and two different recruitment strategies influenced volunteer participation. These strategies consisted of online questionnaires and face-to-face interviews with beekeepers to record bee health issues. We found that use of both recruitment strategies was necessary because they reached different volunteer profiles and different locations, and therefore influenced the survey’s results. Furthermore, public participation increased when the number of local coordinators was higher, regardless of recruitment strategy. These findings could also apply to other developing countries, where lack of internet access for some potential volunteers, logistical constraints such as long distances, and poor infrastructure hamper implementing large-scale citizen-science programs.