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The ectoparasitic mite Varroa destructor is a key threat for European honeybee subspecies (Apis mellifera) globally. However, some A. mellifera populations are known to survive mite infestations by means of natural selection (naturally surviving), likely due to reduced mite reproductive success. The effect of small brood cell size on mite reproductive success has not been investigated in these surviving populations and we have little knowledge of its relationship with mite-surviving traits. Here we tested the impact of smaller worker brood cell size on mite reproductive success in susceptible and naturally surviving colonies in Norway. The data show that mite reproductive success was significantly reduced in smaller cells in susceptible colonies (higher rates of non-reproduction, delayed reproduction, and male absence), but not in the surviving colonies. The results support the claim that smaller cell size can have an impact on V. destructor reproductive success, but this seems not to work in tandem with mite-surviving mechanisms favored by natural selection.
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Cell size and Varroa destructor mite infestations in
susceptible and naturally-surviving honeybee (Apis
mellifera ) colonies
Melissa A. Y. ODDIE
1
,Peter NEUMANN
2,3
,Bjørn DAHLE
4,5
1
Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
2
Institute of Bee Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland
3
Agroscope, Swiss Bee Research Center, Bern, Switzerland
4
Department of Animal and Aquacultural Sciences, Norwegian University of Life sciences, Ås, Norway
5
Norwegian Beekeepers Association, Kløfta, Norway
Received 24 November 2017 Revised 31 May 2018 Accepted 4 October 2018
Abstract The ectoparasitic mite Varroa destructor is a key threat for European honeybee subspecies (Apis
mellifer a ) globally. However, some A. mellifera populations are known to survive mite infestations by means of
natural selection (naturally surviving), likely due to reduced mite reproductive success. The effect of small brood cell
size on mite reproductive success has not been investigated in these surviving populations and we have little
knowledgeof its relationship with mite-surviving traits. Here we tested the impact of smaller worker brood cell size
on mite reproductive success in susceptible and naturally surviving colonies in Norway. The data show that mite
reproductive success was significantly reduced in smaller cells in susceptible colonies (higher rates of non-
reproduction, delayed reproduction, and male absence), but not in the surviving colonies. The results support the
claim that smaller cell size can have an impact on V. destructor reproductive success, but this seems not to work in
tandem with mite-surviving mechanisms favored by natural selection.
Apis mellifera / cell size / honeybee / Varroa destructor
1. INTRODUCTION
There is consensus that the ectoparasitic mite
Varroa destructor is at present the most impactful
global influence on the health of managed honey-
bees (Apis mellifera )ofEuropeanorigin(Dahle
2010; Genersch et al. 2010; Neumann and Carreck
2010; Rosenkranz et al. 2010; VanEngelsdorp et al.
2011). This invasive Asian mite carries out its entire
reproductive cycle within the capped brood cells of
the honeybee host, exposing both adults and juve-
niles to infestations (Rosenkranz et al. 2010). Since
its invasion, this mite has become a potent vector for
a number of viruses and altered the virulence of
some pathogens to the point where they have be-
come a lethal problem (Martin 2001;Chenetal.
2006;Dainatetal.2012). Generally, colonies of
European honeybee subspecies have no effective
defense against the mite and parasite populations
generally increase at an exponential rate until colo-
nies collapse under viral pressure within 2 to 3 years
(Sammataro et al. 2000; Rosenkranz et al. 2010;
Dainat et al. 2012).
At present, beekeepers use a range of acaricides,
which can often result in the development of resis-
tance in the mite, contamination of bee products,
and undesired side effects on the bees themselves
(reviewed by Rosenkranz et al. (2010). Regular mite
treatments also prevent adaptation to the selection
pressure of this novel parasite (Neumann and
Blacquière 2017). Indeed, over the past 17 years,
several distinct, untreated populations of European
Corresponding author: M. Oddie,
melissa.oddie@slu.se
Manuscript editor: Yves Le Conte
Apidologie Original article
*The Author(s), 2018
DOI: 10.1007/s13592-018-0610-2
honeybee subspecies have been documented to sur-
vive V. destructor infestations due to natural selec-
tion (Fries et al. 2006,LeConteetal.2007, Seeley
2007, Locke et al. 2012; Mikheyev et al. 2015;
Oddie et al. 2017,reviewedbyLocke2016). The
means by which they achieve this is likely their
ability to reduce V. destructor reproductive success
by approximately 30% (Locke 2016; Oddie et al.
2017). A number of mechanisms have been put
forward as contributors to such reduced mite repro-
ductive success (Rinderer et al. 2001; Salvy et al.
2001;Harrisetal.2010; Locke et al. 2014;Oddie
et al. 2018). Among these, the reduction of cell size
has been proposed as an effective solution that
beekeepers can employ. It is hypothesized that a
smaller cell size limits the number of foundresses
that can invade a cell and makes it difficult for mites
to move within, a necessary action throughout the
reproductive process. It may also increase instances
of entrapment, where the mite is pinned between the
brood cell wall and the silk cocoon spun by the
pupating larvae, effectively immobilizing and ulti-
mately killing the foundress, preventing reproduc-
tion entirely. As a natural trait, a smaller cell size has
been found in the surviving African and Africanized
A. mellifera populations; however, as a mechanical
method of controlling V. destructor managed by
European beekeepers, evidence has been mixed,
with studies supporting (De Jong and Morse 1988;
De Ruijter and Calis 1988; Message and Gonçalves
1995; Piccirillo and De Jong 2003;Maggietal.
2010) and refuting the effect (Ellis et al. 2009;
Taylor et al. 2008; Berry et al. 2009). Aside from
this ambiguity, interactions with other surviving
mechanisms have not yet been thoroughly investi-
gated: Small cell size can increase honeybee respon-
siveness to certain hygienic tests, such as the exam-
ple provided by Olszewski et al. (2014); bees on
small cell size tended to remove pin-killed brood
faster than bees on a larger cell size Though known
surviving African/ized populations have a smaller
cell size, the role small cell size plays in populations
of naturally-surviving European honeybees is cur-
rently not known. Interestingly, colonies of the re-
cently documented Norwegian surviving population
(Oddie et al. 2017) were selected for resistance
while on a comb foundation cell size of 4.93 mm,
smaller than the conventional size of 5.3 mm. This
population did not display higher levels of grooming
or mite-targeted brood removal, but the observed
reduction in reproductive success was evidently due
to a brood care behavior termed Bcell recapping^in
which cells during pupal development (and mite
reproduction) were opened, exposing them to
changes in temperature and humidity (Oddie et al.
2018). Our study is aimed at comparing the impact
of small cell size between naturally-surviving hon-
eybees and their susceptible counterparts. We intend
to analyze mite reproductive success in a depth not
commonly used by previous studies on cell size.
Given that small cell size may play a significant role
in reducing mite reproduction, we expect that ma-
nipulating the cell size will yield effects on mite
reproductive success in both surviving and suscep-
tible colonies and may act synergistically with the
adult-mediated trait present in surviving colonies.
2. METHODS
The experiments were conducted in the Oslo
region of Norway. In order to track the interaction
of cell size and the surviving phenotype in the
surviving population, 10 local susceptible
queenright A. mellifera colonies from a donor
apiary were chosen for their high V. destructor mite
infestation rates (~ 1050% brood infestation), this
was done to ensure sufficient mites were available
to conduct the study as the surviving population
yielded consistently low mite numbers and brood
infestation rates over several years. Two brood
frames from each donor colony were distributed
among the colonies in two separate apiaries ~
50 km apart. The first receiver apiary contained
only local V. d e s t r u c t o r susceptible stock, reared
on a standard large brood cell size (wax foundation
size 5.3 mm). Grooming and mite-targeted brood
removal were not found at any significant level
(Oddie et al. 2017). The second receiver apiary
contained bees of a local surviving stock (Oddie
et al. 2017). These bees were reared on the small
cell size used in this study (wax foundation size
4.93 mm) and they too did not display high levels
of the aforementioned adult bee behaviors. Five
colonies in each receiver apiary were chosen ran-
domly to take one frame of each of the two foun-
dation base sizes. Prior to the swap, each donor
colony was provided with one frame of large cell
comb (5.3 mm) and one frame of small cell comb
M. A. Y. Oddie et al.
(4.93 mm). Small cell size frames were built out by
the bees that had been reared on the small comb
size to obtain an accurate Bactual^cell size. This
was done because bees reared on larger cells build
out small comb much less accurately (Taylor et al.
2008). Queens were caged on built frames for a
period of 48 h. Brood was left in the donor colonies
for 9 days until just after the capping phase
(Dietemann et al. 2012) and then transferred to
the receiver apiaries. Frames were kept in receiver
colonies for a period of 10 days, allowing enough
time for honeybee brood to develop and juvenile
mite stages to mature to a point where mite repro-
ductioncouldbeproperlymeasured(Martin1995;
Dietemann et al. 2012). Frames were then removed
andstoredat20 °C until cells could be dissected.
Brood cells were opened in a horizontal line begin-
ning in the middle of the brood patch and skipping
three rows progressively above and below each
previously examined line to ensure even sampling
across the patch. Bee brood was aged according to
Martin (1995) and measured in stage instead of
exact age because the exact age of brood could
not be guaranteed. Mite stages were identified
using the ontogenetic developmental chart by Mar-
tin (1995) and recorded for each cell. Multiple
foundress events were included in the analysis of
viable female offspring because our interest lay in
the overall reproductive success of the mite popu-
lation on each frame rather than success of the
individual. Moreover, the number of foundresses
also had the potential to interact with cell size. For
the binary measures of reproductive success (i.e.,
delayed reproduction, non-reproduction, and male
presence), only cells containing a single foundress
were included, as multiple foundresses in a cell
make these parameters impossible to determine
accurately. Using the brood and mite stage, we
were able to determine the average number of
viable female offspring produced per foundress
and whether each foundress in a single-infested cell
was displaying delayed mite reproduction (retarded
production of viable female offspring), non-
reproduction (failure to produce viable female off-
spring), and infertility (no offspring). Male mite
presence was recorded as well as the number of
foundresses in each cell. The measure of viable
female mite offspring was defined as the number
of female offspring that had the potential to emerge
successfully given an appropriate stage of the
brood and was in a cell that also contained a male
(Corrêa-Marques et al. 2003; Locke et al. 2012).
Taylor et al. (2008) found that the actual cell size
drawn from foundation can show variation from
the foundation size. Therefore, the actual cell size
was measured: using calipers to take the length of
10 cells and obtain an average cell size of those 10;
this measurement was repeated on each frame five
times. Foundation size and actual cell size were
both considered in this study.
2.1. Statistical analyses
Cell size was compared between treatment
groups by performing a MannWhitney Utest
on the average cell sizes of each colony. This test
was also used to look at whether the foundation
size affected the final comb cell size. R statistical
analysis software (R Core Team 2008) and the
LME4 package (Bates et al. 2015)wereusedto
perform general linear models and mixed-effects
models to test the effect of actual cell size and
foundation base size on the average number of
viable female offspring per foundress. Models
were fitted by maximum likelihood (Laplace ap-
proximation). Foundation size, actual cell size,
brood stage, and foundress number for each cell
were added as fixed effects; foundress number
and brood stage are both known to influence mite
reproductive success and offspring estimates
(Fuchs and Langenbach 1989; Martin 1995).
The donor colony that housed each frame prior
to the experiment was set as a random effect to
account for between-colony variance. The data
from both apiaries (surviving and susceptible)
were analyzed together and then split and ana-
lyzed separately to examine possible interacting
effects between colony type and actual cell/
foundation base size. Similar models were created
for the variables of non-reproduction, delayed
reproduction, male presence, and infestation rates.
Models were adjusted to account for the binomial
nature of the data using the logit function. Mini-
mum adequate models were isolated by removing
non-significant terms and reducing models to in-
clude only parameters that significantly affected
variation in the response variable. Dispersion
Cell size effect on mite-surviving bees
parameters were monitored for all models and
found to be within a reasonable range.
3. RESULTS
The average cell size measured on the combs of
the donor colonies did not differ significantly
between surviving and susceptible receiver colo-
nies (MannWhitney U=9.00, n
1
=10 n
2
=9,
p> 0.05, two-tailed, surviving mean = 5.29 ±
0.23, susceptible mean = 5.20 ± 0.22). Average
cell size on frames given to surviving colonies
was between 4.92 and 5.53 mm and average cell
size provided to susceptible colonies was between
4.93 and 5.50 mm. Cell sizes on the large foun-
dation were overall significantly larger than those
built on the small foundation (MannWhitney
U=7.00, n
1
=10 n
2
=9, p< 0.05, two-tailed,
mean for large = 5.44 ± 0.06, mean for small=
5.09 ± 0.20). When foundation size was analyzed,
there was no significant difference in the average
number of viable female offspring per foundress
between the large and small cell bases (Table I,
χ
2
= 0.69, p= 0.405, mean viableoffspring count
for large foundation = 1.09 ± 0.34, mean viable
offspring count for small foundation = 1.10 ±
0.15). However, when actual cell size was inves-
tigated, it was found that there was a significant
interacting effect between cell size and whether
the colony was from the surviving or susceptible
group (Table I,n=832, χ
2
=5.48, p=0.019).
When colony groups were analyzed separately, it
was found that in susceptible colonies, small cell
size correlated significantly with a reduced num-
ber of viable female offspring in cells (n=410,
χ
2
= 4.86, p= 0.028, Figure 1). No significant
effect was found in the surviving colonies (n=
422, χ
2
=0.64,p= 0.423, Figure 1). In suscepti-
ble colonies, frames with a smaller average cell
size had higher rates of mite non-reproduction
(Figure 2a, Table II,n= 301, χ
2
= 6.32, p=
0.012), and delayed reproduction (Figure 2b,
Table II,n= 301, χ
2
= 5.30, p= 0.021). Male
mite presence was also lower on frames with a
smaller cell size (Figure 2c, Table II,n= 301,
χ
2
= 6.61, p= 0.010). Cell size did not yield a
significant impact on the levels of infertility
(Table II,χ
2
= 0.59, p= 0.441). None of the bi-
nomial parameters were found to be significantly
affected by actual cell size in surviving colonies
Table I. Mixed-effects model outputs outlining the effect of foundation size and actual cell size on the viable female
offspring count per cell. Models fitted by maximum likelihood. Minimum adequate models were isolated by
excluding non-significant terms.
Model nIndependent variable Dependent variable df χ
2
pvalue
M1 832 Number of viable female
offspring per foundress
Brood stage 5 17.96 0.003**
Foundress number 1 0.59 0.441
Colony type int.
foundation size
10.00 0.998
Foundation size 1 0.69 0.405
Colony type 1 8.75 0.003 **
M2 832 Number of viable female
offspring per foundress
Brood stage 5 0.69 0.003 **
Foundress number 1 0.63 0.430
Colony type int. cell size 1 5.48 0.019 *
M3 (survivor only) 422 Number of viable female
offspring per foundress
Brood stage 5 9.28 0.099
Foundress number 1 0.02 0.891
Cell size 1 0.64 0.423
M4 (susceptible only) 410 Number of viable female
offspring per foundress
Brood stage 22.47 <0.001**
Foundress number 1.47 0.226
Cell size 4.86 0.028 *
Note: italic terms with an *denote statistical significance
M. A. Y. Oddie et al.
(Table II). Finally, infestation rates were slightly
lower on frames with a smaller average cell size in
susceptible receiver colonies (Figure 2d, n=
1898, χ
2
= 260.13, p< 0.001) but no significant
pattern could be found in surviving receiver colo-
nies (Figure 2d, n=1529,χ
2
=1.98,p=0.160).
4. DISCUSSION
Our data support the conclusion that smaller
worker brood cell size can significantly contribute
to the overall reduced reproductive success of
V. destructor mites in susceptible colonies and
may contribute to lower infestation rates; however,
this effect was not significant in surviving colonies
known to possess cell recapping as a mite-
surviving trait (Oddie et al. 2018). The effect of
cell size may be masked by these traits in surviving
colonies, or else it is not present. Regardless, a
small cell size does not appear to work in tandem
with mite resistance traits favored by natural selec-
tion in the surviving Norwegian population.
Cell size differences were comparable between
surviving and susceptible test colonies and there
was an observable distinction between large and
small cell size foundation; however, foundation
size did not yield significant differences in mite
fecundity among surviving or susceptible bees.
This is likely due to the fact that some frames built
up from small cell foundation actually yielded
larger average cell sizes, as was also found by
Taylor et al. (2008). The comb-builders in some
colonies likely follow the foundation base more
accurately than others, making actual cell size a
much more reliable measure than foundation base.
When actual cell size was examined in depth, it
was found that susceptible colonies did benefit
from the small cell size: Cells of smaller average
diameter showed slightly lower mite infestation
rates as well as a significant increase in delayed
reproduction, non-reproduction, and male off-
spring absence, all factors contributing to a lower
mite reproductive success. No effect was found on
mite infertility; however, the rates of infertility
were very low in general within this study. In
contrast, there was no significant effect of cell size
in surviving colonies for any measured parameter;
therefore, a smaller cell size does not appear to
work together with other mechanisms reducing
mite reproduction used by naturally-surviving
populations (Locke et al. 2012;Oddieetal.
2017). The observation that the infestation rate
was affected in the susceptible receiver colonies,
but not in the surviving ones, may point to an
effect put upon infested cells by the surviving
phenotype, though at this point, it can only be
speculated as to how this has occurred. If the
adult-mediated trait does remove infested cells, it
is possiblethe process is not affected by the size of
the cell. The results for susceptible colonies at
least align with those found in several previous
studies: Message and Gonçalves (1995)uncov-
ered a difference in V. destructor infestation rate
and number offemale mite deutonymphs between
0
0.5
1
1.5
2
2.5
3
4.8 4.9 5 5.1 5.2 5.3 5.4 5.5 5.6
Cell size [mm]
offspring per foundress
Average number of viable female
Figure 1 The average number of viable female Varroa destructor mite offspring in each host worker brood cell in
relation to the average actual cell diameter per frame in honeybee (Apis mellifera ) colonies naturally surviving
V. destructor infestations (gray) and in susceptible ones (black). No significant correlation could be found in
surviving colonies (n=410, χ
2
=0.64, p= 0.423). However, in susceptible colonies, there was a significant
positive correlation (n= 422, χ
2
=4.86, p= 0.028).
Cell size effect on mite-surviving bees
cells of 4.54.6 mm and those of 4.95.1 mm.
Maggi et al. (2010) and Piccirillo and De Jong
(2003) found differences in the rate of mite infes-
tation between large and small cell sizes. Size
ranges in both studies were comparable to the
sizes used in this study. Maggi et al. (2010) also
investigated mite reproductive rate, but found no
significant effect while our dataset uncovered a
small but significant reduction. A study in New
Zealand (Taylor et al. 2008) did not find a signif-
icant influence of cell size on mite reproductive
success but found an increase in infestation rate on
smaller cell sizes. Berry et al. (2009) found similar
results, overall mite populations were higher in
colonies reared on the smaller cell size when they
compared entire colonies given small or large
comb sizes (4.9 ± 0.08 and 5.3 ± 0.04 respective-
ly). These varying results provide evidence that
there are parameters that have yet to be considered
regarding V. destructor mite population dynamics
in relation to the size of brood cells. It is possible
that the different methods and environments of
each study are contributing to the mixed results.
Changing parameters within a colony such as cell
size may change the behavior of the bees to the
point where they create unmeasured differences
between themselves and a control population. To
give an example of this, the study performed by
Piccirillo and De Jong (2003)onlyusedbees
accustomed to a small cell size for their trials
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
4.8 5 5.2 5.4 5.6
non fo noitroporP -reproducing
cells
Cell size [mm]
0
0.05
0.1
0.15
0.2
0.25
0.3
0.35
0.4
4.8 5 5.2 5.4 5.6
htiw sllec fo noitroporP
noitcudorper deyaled
Cell size [mm]
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
4.8 5 5.2 5.4 5.6
htiwsllecfonoitroporP
male absent
Cell size [mm]
0
0.1
0.2
0.3
0.4
0.5
0.6
4.8 4.9 5 5.1 5.2 5.3 5.4 5.5 5.6
sllecdetsefnIfonoitroporP
Cell size [mm]
ac
bd
Figure 2 a The proportion of infested honeybee (Apis mellifera ) worker brood cells in which Varroa destructor
foundresses failed to produce viable female offspring relative to the average cell diameter on the frames in surviving
(gray) and susceptible colonies (black). A significant negative correlation was observed in susceptible colonies (n=
301, χ
2
=6.32, p=0.012). bThe proportion of infested honeybee (Apis mellifera ) worker brood cells that
displayed a delay in Varroa destructor reproduction and average cell diameter on frames in surviving (gray) and
susceptible colonies (black). A significant negative correlation was observed in susceptible colonies (n= 301, χ
2
=
5.30, p=0.021). cThe proportion of infested honeybee (Apis mellifera ) worker brood cells without Varroa
destructor males and average cell diameter on frames in surviving (gray) and susceptible colonies (black). A
significant negative correlation was observed in susceptible colonies (n= 301, χ
2
=6.61, p= 0.010). dThe
proportion of Varroa destructor infested honeybee (Apis mellifera ) worker brood in relation to the average diameter
of the cells on frames in surviving (gray) and susceptible (black) receiver colonies. A significant positive correlation
was found in susceptible colonies (n= 1898, χ
2
= 260.13, p<0.001).
M. A. Y. Oddie et al.
and found higher infestation rates on the larger
cell size comb. Taylor et al. (2008) used bees
accustomed to the large cell size and found higher
infestation rates on smaller comb, and both studies
provided their bees with pre-built comb from an-
other source for at least one of the treatment
groups. Ellis et al. (2009) used bees accustomed
to each cell size; they were kept on for the exper-
iment and found no significant differences in
overall mite population. It should then be said that
the cell size on which the bees werereared as well
as the origin of the comb used should be taken into
consideration when analyzing highly variable pa-
rameters such as overall colony mite infestation
rate and V. destructor foundress fecundity. Our
studyalsointroducedframesbuiltoutbyother
colonies, yet only two frames were given and kept
within the colonies, and only for a single brood
cycle; this may not have introduced enough
change to elicit a response from the bees.
Our study delved into V. destructor mite re-
productive parameters in depth, investigating
not only viable offspring number, but also pro-
portion of delayed reproduction, non-
reproduction, infertility, and male presence, all
valuable parameters when considering mite re-
productive success (Locke et al. 2012). The fact
that we found significant patterns in all of these,
save infertility, indicates that cell size does not
affect just one parameter largely, but may have
small, combined effects in each differing param-
eter that create an additive difference. Olszewski
et al. (2014) found that rearing mite-susceptible
bees on foundation size of 4.93 mm (compared
to 5.56 mm) increased hygienic behavior per-
formed, though this study could find no signif-
icant link to this elevated behavior and the
number of immature mites found on the bottom
boards.Olszewskietal.(2014) did suggest that
small cell size could synergize with hygienic
behavior in some populations but not in others
depending on the level of hygienic behavior and
the bees' adaptability to a smaller cell size.
Within-colony variation in our study was large,
making it difficult to isolate strong effects, but
even between only 10 colonies, a distinct pattern
was observed. This study, however, was not
long term and could not take into account the
Tab le II . General linear model and mixed-effects model outputs describing the effect of actual cell size on binomial
reproductive parameters of Varroa destructor . Models fitted by REML. Minimum adequate models were isolated by
excluding non-significant terms.
nIndependent variable Dependent variable df χ
2
pvalue
Susceptible 301 Male presence Cell size 1 6.61 0.010 *
Brood stage 5 6.60 0.253
Delayed reproduction Cell size 5.30 0.021 *
Brood stage 6.48 0.263
Non-reproductive Cell size 6.32 0.012 *
Brood stage 4.01 0.549
Infertile Cell size 0.59 0.441
Brood stage 16.63 0.005 **
Surviving 298 Male presence Cell size 0.49 0.484
Brood stage 4.11 0.534
Delayed reproduction Cell size 0.63 0.426
Brood stage 6.92 0.226
Non-reproductive Cell size 0.01 0.928
Brood stage 3.34 0.559
Infertile Cell size 0.08 0.775
Brood stage 6.85 0.233
Note: italic terms with an *denote statistical significance
Cell size effect on mite-surviving bees
effect of small cell size on the overall population
dynamics of V. destructor in the test colonies, so
the ability of small cell size to help control
V. destructor cannot be reported here. To find
more robust evidence that small cell size affects
mite populations in a practical way, colonies
would need to be bred and reared on small cell
size and compared year-round with those bees
from the same genetic background reared on
large cells. Measuring cell diameter for each
dissected cell individually instead of taking an
average on a frame may also allow for a higher
resolution of the collected information. Overall,
there are many factors to consider when exam-
ining the effect of small cell size on
V. destructor mite population dynamics. Our
study finds evidence that at least in the Nordic
ranges of domestic beekeeping, a smaller cell
size seems to help reduce the reproductive suc-
cess of V. destructor , but this effect does not
seem entirely relevant for bees already known
to survive the parasite by means of natural se-
lection. Indeed, A. mellifera populations in tem-
perate European regions naturally display a larg-
er brood cell size compared to African subspe-
cies. This confers an advantage on the African
honeybees in terms of flight abilities solely on
the grounds of morphometric dimensions due to
a better engine to aircraft mass ratio (Hepburn
et al. 1999). Nevertheless, natural selection has
favored larger cell sizes in the temperate re-
gions. This suggests that surviving colder tem-
peratures may be involved. In colder climates,
many species adhere to Bergmannsrule
(Bergmann 1847), displaying a trend of larger
body sizes at higher latitudes (Cushman et al.
1993; Olson et al. 2009), as this is a better
adaptation to tolerate low temperatures. Small
cell size and its potential to reduce the sizes of
worker bees (McMullan and Brown 2006)may
then prove a detriment in the long run to popu-
lations in higher latitudes, and though it may
produce an effect on V. d e s t r u c t o r , the overall
reduction in competitive ability may render the
effect negligible regarding colony survival.
Small cell size, though potentially useful in
aiding the management of parasites, may not
be the key factor in achieving treatment-free,
mite-surviving bees in temperate climates.
ACKNOWLEDGMENTS
Wearegratefultothelocalbeekeepersthatletus
carry out these experiments in their apiaries.
AUTHOR CONTRIBUTIONS
P.N., B.D. & M.O. conceived and designed ex-
periments; M.O. collected data; and performed
analysis; P.N. & M.O. wrote the paper, all authors
revised it. All authors approved the final
manuscript.Funding information
Financial support was granted to P.N. by the
Ricola FoundationNature and Culture and the
Vinetum foundation. Financial support was
granted to B.D. by the Norwegian Research
Council, grant no. 234193.
OPEN ACCESS
This article is distributed under the terms of the
Creative Commons Attribution 4.0 International Li-
cense (http://creativecommons.org/licenses/by/4.0/),
which permits unrestricted use, distribution, and repro-
duction in any medium, provided you give appropriate
credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if
changes were made.
Taille des cellules et infestation par les acariens Va r roa
destructor chez les colonies d'abeilles ( Apis mellifera )
sensibles et naturellement survivantes
Apis mellifera / taille de la cellule / abeille mellifère /
Varroa destructor
Brutzellgrösse und Befall durch Varroa destructor
Milben in anfälligen und natürlich überlebenden
Apis mellifera / Zellgrösse / Honigbiene / Varroa
destructor
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... The authors concluded, however, that whilst reduced mite reproductive success seemed to be a key factor in survival, neither grooming or VSH appeared to be important to explain the differences in survival. More recent investigations have shown that a shorter postcapping period may also contribute to natural colony survival of this population [61], while it is not the case for cell size [62]. Moreover, recapping behavior has been shown to be an important factor in the survival of this bee population [63]. ...
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