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Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation

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Abstract

A population of European honey bees (Apis mellifera) surviving Varroa destructor mite infestation in Sweden for over 10years without treatment, demonstrate that a balanced host–parasite relationship may evolve over time. Colony-level adaptive traits linked to Varroa tolerance were investigated in this population to identify possible characteristics that may be responsible for colony survival in spite of mite infestations. Brood removal rate, adult grooming rate, and the mite distribution between brood and adults were not significantly different in the untreated population compared with treated control colonies. However, colony size and the reproductive success of the mite were significantly reduced in surviving colonies compared with control colonies. Our data suggest that colony-level adaptive traits may limit mite population growth by reducing mite reproduction opportunities and also by suppressing the mite reproductive success. Keywords Varroa destructor – Apis mellifera –natural selection–tolerance–host–parasite interaction
Characteristics of honey bee colonies (Apis mellifera)
in Sweden surviving Varroa destructor infestation
Barbara LOCKE,Ingemar FRIES
Department of Ecology, Swedish University of Agricultural Sciences, P.O. Box 7044, 750 07 Uppsala, Sweden
Received 7 June 2010 Revised 7 October 2010 Accepted 13 October 2010
Abstract A population of European honey bees (Apis mellifera) surviving Varroa destructor mite infestation
in Sweden for over 10 years without treatment, demonstrate that a balanced hostparasite relationship may
evolve over time. Colony-level adaptive traits linked to Varroa tolerance were investigated in this population to
identify possible characteristics that may be responsible for colony survival in spite of mite infestations. Brood
removal rate, adult grooming rate, and the mite distribution between brood and adults were not significantly
different in the untreated population compared with treated control colonies. However, colony size and the
reproductive success of the mite were significantly reduced in surviving colonies compared with control
colonies. Our data suggest that colony-level adaptive traits may limit mite population growth by reducing mite
reproduction opportunities and also by suppressing the mite reproductive success.
Varroa destructor /Apis mellifera / natural selection / tolerance / hostparasite interaction
1. INTRODUCTION
Hostparasite interactions in social insects
are intricate with two different levels in which
social insects can defend themselves against
parasites: (1) by innate individual-level im-
mune responses and (2) by adaptive colony-
level defence mechanisms. At the individual
level, the immune system of the European
honey bee, Apis mellifera,isnotwell-
developed compared with other insects (Evans
et al.2006), and rather, they rely heavily on
colony-level adaptive mechanisms for defence.
The parasitic Varroa destructor mite has be-
come a major threat to apiculture with European
races of A. mellifera throughout most of the
world in contrast to the African honey bee race
A.mellifera scutellata and the Africanized bees
in South America (Rosenkranz et al.2010).
By feeding on the hemolymph of adult bees
(during their phoretic phase) and developing
bees (during their reproductive phase), the mite
vectors naturally occurring otherwise latent
viruses which can develop into severe overt
infections and potentially lead to colony
mortality (Allen and Ball 1996; Nordström et
al.1999; Martin 2001; Sumpter and Martin
2004).
Mite control methods, which are used in
apiculture to limit the mite population and
avoid colony losses, can be problematic for
several reasons. Chemical residues can build
up in hive products (Bogdanov et al.1998;
Wa l l n e r 1999); mites can develop resistance to
effective acaricides (Sammataro et al.2005);
some methods cause damage to bees (Imdorf et
al.1990,1999; Charrièr and Imdorf 2002), but
most importantly, they remove the selective
pressures on the mites and the host that may
otherwise produce a stable hostparasite rela-
tionship through co-adaptive evolution (Fries
and Camazine 2001).
Corresponding author: B. Locke,
barbara.locke@ekol.slu.se
Manuscript editor: David Tarpy
Apidologie (2011) 42:533542 Original article
*INRA, DIB-AGIB and Springer Science+Business Media B.V., 2011
DOI: 10.1007/s13592-011-0029-5
A stable hostparasite relationship is seen
between the mite and its natural host, the Asian
honey bee, Apis cerana. In this system, through a
long evolutionary process, the Asian honey bee
has adapted unique colony-level defence mech-
anisms, such as preventing mite reproduction in
worker brood and entombing mites in drone
brood, thereby limiting the mite population
growth to a tolerable level where colony mortal-
ity rarely occurs (reviewed in Rath 1999). The
Africanized honey bees in South America,
descendants of A.mellifera scutellata, also exhibit
tolerance to V. destructor and a variety of defence
mechanisms, such as behavioural traits (Corrêa-
Marques and De Jong 1998; Boecking and
Spivak 1999; reviewed in Rosenkranz 1999)
and reduced mite reproductive ability (Medina et
al.2002; Martin and Medina 2004; Mondragon
et al.2006)have been reported to explain their
survival without mite control treatments. In
addition, in the African bee race A.mellifera
scutellata, the bees and/or the mites haveadapted
to a stable hostparasite relationship within 5
6 years from exposure (Allsopp et al.1997;
Allsopp 2006). These African and Africanized
hybrid bees may have different genetic or envi-
ronmental advantages for Va r r o a tolerance com-
pared with the European races of A. mellifera,but
their tolerance mechanisms are still unclear.
Breeding programmes, with efforts to produce
mite-tolerant strains of European honey bee races,
have had some success most notably with bees
expressing the Varroa-sensitive hygiene trait
(Harbo and Harris 2005; Ibrahim and Spivak
2006) and bees of the Russian-hybrid stock
(Rinderer et al.2001), yet mite population moni-
toring and mite control treatments are still required
for the survival of these bees (Tarpy et al. 2007).
There have been reports on populations of
European honey bee races surviving mite
infestation for long periods without mite control
treatment (De Jong and Soares 1997; Kefuss et
al.2004; Fries et al.2006; Le Conte et al. 2007;
Seeley 2007), however little has been described
concerning their tolerance mechanisms or colony
characteristics. In an attempt to consider both the
host and the parasite in co-adaptation processes,
Fries and Bommarco (2007) demonstrated that
mite tolerance in one of these surviving popula-
tions is a product of adapted traits of the bees and
not of the mites. This could be the case for other
surviving populations in Europe because of the
low genetic variation in European mites, due to
their clonal origin (Solignac et al.2005). These
surviving populations may hold an answer to the
selective process of achieving a stable relation-
ship between A. mellifera and V. destructor and
give insight into colony-level adaptations of mite
infestation.
The objective of this study was to unravel the
mechanisms responsible for the increased mite
tolerance in a population of surviving European
honey bee colonies in Sweden on the island of
Gotland in the Baltic Sea. This population was
established as part of a natural selection experi-
ment called the Bond-Projectand has survived
since 1999 without mite control or beekeeping
management and with exposure to severe mite
infestation selection pressure. For a more detailed
explanation on the background of these surviving
honey bee colonies, refer to Fries et al. (2003;
2006) and Fries and Bommarco (2007).
This study was an exploratory investigation
of colony-level characteristics that have been
linked to, or suggested to be important for, mite
tolerance in European races of honey bees.
These characteristics include: (1) hygienic be-
haviour, the ability of honey bees to detect and
remove mite-infested brood (Spivak 1996;
Spivak and Reuter 2001); (2) grooming of adult
bees, a behaviour resulting in capturing and
damaging of adult mites (Moosbeckhofer 1992;
Moretto et al. 1995); (3) colony size and
temporal dynamics, a characteristic known to
greatly influence the mite population given the
importance of brood amounts for mite repro-
duction (Fries et al.1994; Calis et al.1999); (4)
brood attractivity, measured by the distribution
ratio of mites on adult bees (phoretic mites) and
in the brood (reproducing mites), can influence
the proportion of reproducing mites in the
colony and therefore the growth rate (Boot et
al.1993) and (5) suppression of mite reproduc-
tive ability and success, an important parameter
able to greatly affect the mite population (Fries
et al.1994; Rosenkranz and Engels 1994).
534 B. Locke and I. Fries
2. MATERIALS AND METHODS
The study was conducted from June through
September in 2008 and 2009. The population of
surviving honey bee colonies (N=14) was studied in
a single apiary on the southern part of the island
Gotland, Sweden, with the mite-susceptible control
colonies (N=12) in an apiary approximately 20 km
away. A second apiary was established in Uppsala,
Sweden, in 2009, with colonies headed with queens
produced and mated within the population of the
surviving colonies on Gotland (N=7) and with a
control group (N=7) in the same apiary.
The control apiary on Gotland was effectively
treated for mites in the autumn of 2007 and therefore
had only a few mites during the 2008 season. The
control colonies were not treated in 2008 so the mite
population was able to increase during 2009. Every
measurement was compared with control colonies at
the same time except for grooming behaviour in 2008
since no mites were available in the control colonies
to examine. The surviving colonies were sometimes
weak or did not have brood due to supersedure and
therefore the actual number of colonies examined
varied for different traits at each visit.
2.1. Hygienic behaviour
On Gotland in 2008, hygienic behaviour was
tested in surviving and control colonies in June, July
and August, and again in July 2009, both in Uppsala
and on Gotland. One hundred pupae in each colony
were marked and pin-killed (Palacio et al.2000)
while 100 cells in the same brood area were marked
without pin-killing, for control. The proportion of
removed killed pupae was recorded at 12 and 24 h
after pinning to determine hygienic behaviour
expressed as the brood removal rate. Every test was
conducted on the surviving colonies and control
colonies on the same day and approximately at the
same time of the day.
2.2. Grooming behaviour
Grooming behaviour was tested in surviving
colonies in June, July and August of 2008 on Gotland
and in surviving and control colonies in August 2009
in Uppsala. Bottom-board metal slide-in trays were
used to collect colony debris and remained under the
colony for 7 days before examination. The proportion
of damaged mites in colony debris was recorded in
surviving colonies and in control colonies to deter-
mine the adult bee grooming rate or grooming
behaviour (Bienefeld et al.1999).
2.3. Colony size and temporal dynamics
Colony size was measured in surviving and
control colonies on Gotland in June, July and August
of 2008, July, August and September of 2009 and in
August of 2009 in Uppsala. Population estimates of
the adult bees, worker brood and drone brood were
made using the Liebefeld Estimation Method (Imdorf
et al.1987) to determine colony size and analysed
over time to determine temporal dynamics of colony
size.
2.4. Brood attractivity and Varroa mite
infestation and distribution
Samples for determining mite infestation rates
were taken on the same dates as colony size
measurement. The phoretic Va r r o a mite infestation
rates were determined by washing samples of
around 200 bees in each sample with soapy water
to dislodge the mites to count them as a sample
proportion (De Jong et al. 1982; Fries et al. 1991a).
Adult bees were collected from the brood chamber
of the hive.The Va r r o a infestation rates in worker
brood were calculated as the proportion of infested
cells in a sample. This was measured when cells
were opened for examination of mite reproduction
or otherwise by opening 100 randomly selected
pupal cells in the field (Fries et al.1991b). The
number of mites on adults in the colony was
calculated by multiplying the infestation rates of
adults by the number of adult bees in the colony.
Using colony brood estimations, the same procedure
was done to calculate the number of mites in brood.
The total number of mites on adults and in brood
was added together to produce the total number of
mites in the colony. The mite distribution was then
determined as proportions of mites on either adult
bees or in brood of the total mite population within
the colony. The mite distributions were used to
determine the effect of brood attractivity.
Swedish honey bee colonies surviving V. destructor infestation 535
2.5. Suppression of mite reproductive
success
Mite reproductive parameters were recorded in
surviving colonies in August 2008 on Gotland with
control colonies in Uppsala recorded in July 2008. In
2009, records were made both in surviving and
control colonies on Gotland in July and in Uppsala
in August. Sealed worker brood cells containing
pupae older than approximately 190 h (brown eyes
and yellow body stage, according to Martin 1994)
were carefully opened and pupae removed in the
laboratory. The developmental stage of each pupa
was recorded based on the appearance description
given by Martin (1994). Complete mite families from
single-mother mite-infested cells were removed using
a fine brush and examined under a stereo microscope.
Within each pupal cell, the following information
was collected:
1. Whether the mother mite reproduced,
2. The total number of offspring per mother mite,
3. Whether an alive male was present or absent,
4. The number of dead mite progeny, and
5. The developmental stage of each individual mite
offspring.
The collected information was then used to
determine the reproductive success measured as the
ability of the mother mite to produce at least one
viable mated female offspring at the time the
developing bee hatches from the cell. The informa-
tion collected was further used to explain fecundity
and which parameter that was most often responsible
for any reproductive failure. Such failure could
depend on infertility, absence of male offspring, high
proportion of mite offspring mortality, or delayed
egg-laying by the mother mite.
The yellow thorax stage of the pupae is the longest
stage ranging from approximately 190240 h, and the
male mite does not become adult until about 210 h
(Martin 1994). Therefore, any yellow thorax-stage
recording where no adult male mite was observed
was recorded as uncertain since immature male mites
are difficult to distinguish from early developing
female mite offspring. A total of 22 cells in the
control population and 24 cells in the surviving
population were considered uncertain and were
therefore not included in the analysis. For each
colony examined, the proportions of the different
reproductive parameters were used in the statistical
analysis. In the surviving population, a total of 614
cells were examined in 23 colonies, and a total of 592
cells were examined in the 21 control colonies with
observations between ten and 35 cells per colony.
2.6. Statistical analysis
All statistical analyses were performed in SAS 9.1
for Windows.
We used linear repeated-measures mixed-effects
models (SAS proc Mixed) to independently test the
effects that surviving colonies compared with control
colonies (treatment groups) had on brood removal
rate (hygienic behaviour), adult grooming rate
(grooming behaviour), colony size, mite infestation,
mite distribution (brood attractivity) and the propor-
tion of successfully reproducing mites (along with the
various parameters measured to determine mite
reproductive success). The covariance structure for
the repeated factor was selected based on the
Aikaikes information criteria (Littell et al.1996).
In order to test for all possible effects, we started
by analysing full models including all possible
explanatory variables such as treatment, mite infesta-
tion, colony, date and location. Non-significant
variables (P>0.05) were sequentially excluded from
the model starting with the higher order of inter-
actions while factors that were significant or part of
significant interactions were kept in the model
(Crawley 2002). The assumption of normality and
equal variance were verified by analysis of residuals
(Littell et al.1996). The Satterthwaite method was
used to approximate denominator degrees of freedom
in all models (Littell et al.1996). Correlation analysis
was used to compare the variation in colony size due
to mite infestation rates.
3. RESULTS
3.1. Hygienic behaviour
Brood removal rates at 12 and 24 h did not
differ significantly (P>0.05) at 12 h between
control colonies, 0.15 ± 0.02 (xSE,n=34)
and surviving colonies, 0.20±0.04 (xSE,n=
34), or at 24 h between control colonies, 0.49±
536 B. Locke and I. Fries
0.05 (xSE,n=34) and surviving colonies,
0.46±0.05 (xSE,n=34). No other variables
included in the model had any significant effect
on the hygienic behaviour (P>0.05).
3.2. Grooming behaviour
The adult bee grooming rate in 2008 was
only measured on mites from the surviving
colonies, 0.31±0.02 (xSE,n=1174), since
no mites were found in the control group that
year. In the Uppsala apiary in 2009, the
proportion of damaged mites in surviving
colonies, 0.36±0.04 (xSE,n=135) was not
significantly different (P>0.05) than in the
control colonies, 0.46±0.04 (xSE,n=109).
No other variables included in the model had
any significant effect on the grooming behav-
iour (P>0.05).
3.3. Colony size and temporal dynamics
Colony size measurements were significantly
reduced in the surviving colonies compared
with control colonies (adult bees, F
1, 56.7
=
28.94, P<0.0001, Figure 1a; worker brood,
F
1, 42.7
=7.81, P=0.0078 Figure 1b and drone
brood, F
1, 21.5
=10.35, P=0.0040, Figure 1c).
Date also had a significant effect on colony size
(adult bees, F
4, 64.7
=6.23, P=0.0003; worker
brood, F
4, 78.6
=8.65, P<0.0001 and drone
brood, F
4, 83.7
=7.91, P<0.0001), however the
two populations showed significantly different
temporal dynamics between adult bees and
drone brood production but not for worker
brood production (adult bees, F
4, 68.9
=3.72,
P=0.0085; drone brood, F
4, 84.4
=3.11, P=
0.0193; Figure 1). In 2008, the mite infestation
rates in the surviving colonies on adult bees for
June, 0.02±0.004 (xSE,n=12); July, 0.05 ±
0.03 (xSE,n=6) and August, 0.07± 0.03
(xSE,n=12) did not correlate significantly
with the number of adult bees in the colonies
(R=0.23; n=30; P>0.05). The mite infesta-
tion rates in the worker brood of the surviving
colonies in June 0.09±0.03 (xSE,n=12);
July, 0.09 ± 0.03 (xSE,n=6) and August,
0.17±0.04 (xSE,n=12) of 2008, also did
not correlate with the number of worker brood
production (R=0.33; n=30; P>0.05). There-
fore, the reduced colony size in the surviving
population was not an effect of mite infestation.
3.4. Brood attractivity and Varroa mite
infestation and distribution
Date significantly affected the number of
mites within the colonies (F
1, 57.2
=13.54, P<
0.0001). In 2008, no mites were recorded in the
control colonies, although by July 2009, the
average mite infestation rates in adults, 0.05±
0.01 (xSE,n=13) and in brood 0.12±0.03
(xSE,n=13) were similar to those of the
surviving colonies (adult, 0.07±0.02; brood,
0.13±0.03; xSE,n=11). The mite population
growth rate measured on adult bees over time
from July to September 2009 was significantly
faster in the control colonies compared with
surviving colonies (F
4, 60.9
=5.59, P=0.0007,
Figure 2). During the summer of 2009, the adult
bee mite infestation rates were significantly
correlated with the number of adult bees in the
control colonies (R=0.62; n=30; P>0.001),
and mortality occurred in all these colonies by
the following winter. In contrast to 2008, there
was a correlation between the adult bee mite
infestation rates and the number of adult bees in
the surviving population in 2009 (R=0.45; n=
37; 0.001<P<0.01). However the surviving
population survived the winter.
The distribution of mites between adult bees
and brood did not show any significant differ-
ence (P>0.05) between the surviving colonies
and control colonies.
3.5. Suppression of mite reproductive
success
A highly significant difference was observed
in the average proportions of successfully
reproducing Varroa mites between the surviving
colonies 0.48±0.02 (xSE,n=23) and the
control colonies 0.78±0.02 (xSE,n=21,
F
1, 41.4
=75.78, P<0.0001, Figure 3). Individu-
Swedish honey bee colonies surviving V. destructor infestation 537
ally, each parameter investigated for determining
the proportion of mites successfully reproducing
was significantly different between the surviv-
ing population and the control population
(Table I). The fecundity of the mother mites,
excluding mites that did not reproduce, was also
significantly different between the two popula-
tions (Table I).
4. DISCUSSION
Our results clearly demonstrate a significant
reduction in the reproductive success of Va r r o a
mites (measured as the ability to produce at least
one viable offspring) in a European population of
A. mellifera colonies where no mite control was
practiced for more than 10 years. The surviving
colonies had on average almost twice the
proportion of infertile mites, more than twice
the proportion of dead progeny, significantly
reduced fecundity and an overall reproductive
success rate of less than 50% compared with
over 75% in control colonies. Delayed egg-
laying by the mother mites was proportionally
the most frequent cause of reproductive failure
with dead progeny as the second most common
cause. Reduced fecundity, along with the reduced
ability to produce viable female offspring clearly,
is important to explain the lower mite infestation
rates in the surviving population.
Although differences were small, mite infertil-
ity was significantly different between the surviv-
ing and control populations in this study. This
result contrasts the observations by Rosenkranz et
al. (2009) who were unable to show a difference
Figure 1. Mean colony size estimations on the number of aadult bees, bworker pupae and cdrone brood, with
standard error bars, in 2008, for surviving honey bee colonies (solid line) through June (n= 12), July (n=6) and
August (n=12), and for control colonies (dotted line) through June (n=10), July (n=4) and August (n=4) on
Gotland.
Figure 2. Regression lines on
the mean mite infestation rates
(number of mites per 200
adult bees) with standard error
bars, in 2009, of surviving
colonies (solid line;y=0.15x
0.12) through July (n=13),
August (n=11) and September
(n=13), and for control
colonies (dotted line;
y=0.51x0.45) through July
(n=11), August (n=11) and
September (n=8) on Gotland.
538 B. Locke and I. Fries
in mite infertility between different European
honey bee races, surviving honey bees from
Gotland or bees selected for Va r r o a -sensitive
hygienic behaviour. However, Rosenkranz et al.
(2009) were able to find different cuticular
compounds on the bees in their study which
could possible reduce (Millani et al. 2004), or
stimulate (Garrido and Rosenkranz 2003;2004),
V. destructor reproduction in different ways
including the fertility, fecundity, egg-laying initi-
ation and possibly even mite progeny mortality
all together, thereby limiting the reproductive
success of the mite. This hypothesis needs
further investigation with detailed observations
on mite reproduction in relation to the cuticular
compounds described.
Based on the results of this study, neither
hygienic behaviour nor grooming behaviour can
be considered characteristics responsible for the
mite tolerance observed in this surviving honey
bee population in Sweden. Therefore, selection
for these traits was probably not as important as
traits related to mite reproduction for their survival
with Va r r o a mites. This is an important observa-
tion considering the attention mite-resistant
breeding programmes put towards these behav-
ioural traits (Büchler et al.2010; Rinderer et al.
2010). Furthermore, expressions of these behav-
ioural traits are difficult to properly determine.
The type of damage recorded for grooming
behaviour included mutilated legs and dorsal
shields as well as dimples in the dorsal shields.
The latter has recently been shown to also result
from birth defects (Davis 2009), and therefore
the actual damages caused by bees may have
been overestimated in this study. Bees can also
damage already-dead mites (Rosenkranz et al.
1997), and the actual level of bee damages to
vital mites is difficult to estimate from debris
observations.
Figure 3. Mean proportions of mother mites producing viable mated female offspring in surviving (n=23) and
control colonies (n=21) with standard error bars.
Table I. Means with standard errors, Fvalues and Pvalues for the differences in the proportions of infertile
mites, dead progeny, absence of male progeny, delayed egg-laying and the average fecundity of mother mites,
between surviving (n=23) and control colonies (n= 21).
Infertility Dead progeny Absence of male
progeny
Delayed egg-
laying
Fecundity
Surviving colonies
xSE 0.08±0.01 0.16 ± 0.03 0.07 ± 0.01 0.20±0.02 3.74±0.09
Control colonies
xSE 0.04±0.01 0.07 ± 0.01 0.03 ± 0.01 0.05±0.01 4.26±0.08
Fvalues F
(1,41.6)
=5.34 F
(1,41.9)
=8.77 F
(1,41.7)
=7.21 F
(1,41)
=27.85 F
(1,40.2)
=19.99
Pvalues P=0.0259 P= 0.0050 P= 0.0104 P< 0.0001 P< 0.0001
Swedish honey bee colonies surviving V. destructor infestation 539
The amounts of adult bees, worker brood and
drone brood were significantly lower in the
surviving colonies compared with the control
colonies. Since mites reproduce in the brood cells
with preference for drone brood (Fuchs 1990), the
reduced amounts of brood availability, in partic-
ular drone brood, in the surviving population
consequently limits the reproductive opportuni-
ties for the mites. Hence, reduced colony size
may be an adaptive characteristic of the surviv-
ing colonies to limit the mite population growth
rate. In addition, it was clear that the smaller
colony size of the surviving population was not a
symptom of mite infestation since no statistically
significant effects were observed on colony size
from the mite infestation rates. Inbred honey bee
colonies can also result in reduced colony size
and since an inbreeding potential exists in the
surviving colonies from Gotland due to their
isolation, the level of inbreeding in this popula-
tion should be investigated.
The control colonies were not treated in the
fall of 2008 and by July 2009 the average mite
infestation rate between the surviving and
control colonies were nearly the same. However,
by late September, the mite population in the
surviving colonies was significantly lower com-
pared with the control colonies. This is congruent
with earlier reports on this surviving population
by Fries and Bommarco (2007) who showed mite
infestation rates 82% lower in surviving colonies
compared with the control colonies in the fall.
Our results, however, could not confirm their
hypothesis that brood attractivity could possibly
play a role in the mite tolerance of this
population. Although mite population growth
rate was higher in control colonies, surviving
colonies still had high rates of mite infestation
and showed clinical symptoms of viral infec-
tions. Another potential survival mechanism
in this population that should be investigated
is a possible heightened individual immune
response to the viral infections vectored by
Va r r o a mites.
In conclusion, this study presents colony-
level characteristics in a population of surviv-
ing honey bee colonies that limit the mite
population growth by either suppressing mite
reproductive success or limiting mite repro-
ductive opportunities by reduced brood pro-
duction. Although the exact mechanisms
behind these traits are not yet identified, the
information collected from this investigation
is a step forward towards understanding the
adaptive processes of mite tolerance in honey
bee colonies. The only documented sustainable
tolerance to V. destructor mite in European honey
bees are of colonies that have not been selected
by humans but that have been exposed to natural
selection pressures. Our current direction is to
compare our data with other Va r r o a mite-tolerant
European honey bee populations to gain a deeper
understanding of the hostparasite interactions in
such stable relationships.
ACKNOWLEDGMENTS
Åke Lyberg is thanked for providing excellent
field sites and beekeeping support. Financial support
was provided by the Montagu Foundation Switzer-
land, within the SAVE project, the EU-funded 7th
Framework project BEE DOC, Grant Agreement
244956, and Jordbruksverket for beekeeping and
maintaining the original population of bees.
Caractéristiques des colonies dabeilles (Apis
mellifera) en Suède survivant à une infestation de
Varroa destructor.
Varroa destructor / Apis mellifera / sélection naturelle /
intéraction hôte-parasite / adaptation
Eigenschaften von Bienenvölkern (Apis mellifera)
in Schweden, die Varroa destructor Infektionen
überleben.
Varroa destructor /Apis mellifera /Natürliche
Selektion / Toleranz / Wirt-Parasit Wechselwirkung
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... The study of the features of V. underwoodi will make it possible to develop methods for combating the new parasite in advance (Guzman and Rinderer, 1999;Kolar and Lodge, 2001;Woolhouse et al., 2005). One such method is the selection of A. mellifera bee colonies based on hygienic behavior against the V. destructor mite, which will probably also work against the V. underwoodi mite (Mondragón et al., 2005;Allsopp, 2006;Locke and Fries, 2011;Çakmak and Fuchs, 2013;Locke, 2016;Conlon et al., 2018;McMullan, 2018;Alphen and Fernhout, 2020). In the present work, a detailed characterization of V. underwoodi mites in the population of Apis cerana ussuriensis in Primorsky Krai is given based on the analysis of morphometry and polymorphism of the COX1 gene mtDNA; all available knowledge about the V. underwoodi mite is systematized, and possible threats of V. underwoodi to other g. ...
... mites. There are currently nine V. destructor mite-resistant A. mellifera honey bee populations in the world, which have been developed through targeted breeding: 1) the North County Dublin honey bee population in Ireland; 2) the population of the honey bee subspecies A. m. scutellata in Brazil and South Africa; 3) the population of honey bees in Toulouse in France; 4) the population of honey bees on the island of Fernando de Noronha in Brazil; 5) the coastal population of honey bees in the Primorsky Krai of Russia; 6) the population of honey bees in Gotland, Sweden; 7) the honey bee population of Avignon in France; 8) Arnot Forest Ithaca honey bee population in New York State, USA; and 9) the honey bee population on Marmara Island in Turkey (Mondragón et al., 2005;Allsopp, 2006;Locke and Fries, 2011;Çakmak and Fuchs, 2013;Locke, 2016;Conlon et al., 2018;McMullan, 2018;Alphen , Fernhout, 2020). Selection of honey bee colonies based on hygienic behavior for resistance to the V. destructor mite will make it possible to use less acaricides and prevent disturbances in the intestinal microbiome, which provides the protective function of the body and plays an important role in the immunity and adaptation of bees to environmental conditions (Çakmak and Fuchs, 2013). ...
Article
Species of the genus Varroa are ectoparasitic mites of the Apis honey bees. Unlike the well-known species of mites V. destructor and V. jacobsoni, V. underwoodi is still poorly studied. According to foreign publications, the currently recognized distribution of V. underwoodi in the A. cerana population includes Nepal, South Korea, Japan, Malaysia, India, Indonesia, Papua New Guinea, Vietnam, and China. Recently it has been detected in Russia (Primorsky krai) on A. cerana ussuriensis honey bees. Since V. destructor and V. jacobsoni have the ability to easily switch to other bee species, there is a possibility that later V. underwoodi may also extensively switch from the Asian honey bees A. cerana to the European honey bees A. mellifera. The first case of V. underwoodi parasitizing in A. mellifera colonies was recorded in Papua New Guinea. The parasitic mite V. underwoodi requires careful study, since it is a new potential parasite of the honey bees A. mellifera, which can also bring new species and strains of viruses and bacteria, change the composition of the gut microbiome, and disrupt the protective and adaptive mechanisms of the bees. This article presents the data of morphometry and polymorphism of the COX1 gene mtDNA. Varroa underwoodi was compared with the other mite species V. destructor and V. jacobsoni. The mean genetic divergence and p-distance between V. underwoodi and other Varroa species were 9% and 0.09, respectively, which is consistent with the level of species differences in insects. The nucleotide sequences of the COX1 gene mtDNA of V. underwoodi from Primorsky krai of Russia LC532104 and from the Jilin province of China MH205176 turned out to be identical and were assigned to the China 1 MH205176 haplotype. It is assumed that there is continuous migration between the A. cerana populations of Russia and China, which led to the spread of V. underwoodi in the natural population of A. cerana ussuriensis in the Primorsky krai of Russia, and the mite is currently distributed up to 45.06° N. Thus, the northern border of the V. underwoodi range is located on the territory of the Russian Far East and, probably, coincides with the range of A. cerana ussuriensis. It is likely that the selection of A. mellifera bee colonies for hygienic behavior against the V. destructor mite may also be effective against V. underwoodi and will prevent the possible transition of V. underwoodi from Asian A. cerana to European A. mellifera.
... Andrews (2019) describes 'natural beekeepers' in the US who do not treat for Varroa, and 'not-so-natural' beekeepers, who seek to improve the genetic fitness of honeybees through selective breeding. Research supporting these approaches maintains that Varroa treatment reduces opportunity for honeybees to evolve adaptive strategies through natural selection, thus reducing their genetic fitness over the long-term (Conte et al. 2007;Locke and Fries 2011). ...
... Whether honeybees adapt to Varroa if left untreated, and indeed whether they can survive long term outside managed colonies in the UK, are both issues subject to scientific debate (Conte et al. 2007;Locke and Fries, 2011;Thompson et al. 2014;Loftus et al. 2016;Seeley, 2017). There were strong opinions on this among beekeepers; the black bee farmers believe that pressures of Varroa and disease, lack of forage or suitable cavities and intensive agricultural practices mean honeybees cannot survive long term outside managed colonies, which is a key motivation for breeding bees with better survival capabilities. ...
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Beekeepers are central to pollinator health. For policymakers and beekeeping organisations to develop widely accepted strategies to sustain honeybee populations alongside wild pollinators, a structured understanding of beekeeper motivations is essential. UK beekeepers are increasing in number, with diverse management styles despite calls for coordinated practice to manage honeybee health. Our Q methodology study in Cornwall, UK, indicated five beekeeping perspectives; conventional hobbyists, natural beekeepers, black bee farmers, new-conventional hobbyists and pragmatic bee farmers. Motivations can be shared across perspectives but trade-offs (notably between economic, social responsibility and ideological motivations) result in differing practices, some of which counter ‘official’ UK advice and may have implications for pollinator health and competition. Honeybee conservation emerged as a key motivator behind non-conventional practices, but wild pollinator conservation was not prioritised by most beekeepers in practice. Q methodology has the potential to facilitate non-hierarchical collaboration and conceptualisation of sustainable beekeeping, moving towards co-production of knowledge to influence policy.
... Kolar, Lodge, 2001;Woolhouse et al., 2005). Одним из таких методов является селекция семей пчел A. mellifera по гигиеническому поведению против клеща V. destructor, которая, вероятно, будет также работать и против клеща V. underwoodi (Mondragón et al., 2005;Allsopp, 2006;Locke, Fries, 2011;Çakmak, Fuchs, 2013;Locke, 2016;Conlon et al., 2018;McMullan, 2018;Alphen, Fernhout, 2020). В настоящей работе дана детальная характеристика клещей V. underwoodi в популяции A. cerana ussuriensis в Приморском крае на основе анализа морфометрии и полиморфизма гена COX1 мтДНК, систематизированы все имеющиеся знания о клеще V. underwoodi, проведена оценке возможных угроз V. underwoodi для других видов пчел р. ...
... Для борьбы с распространением V. destructor и предотвращения потенциального перехода V. underwoodi возможно применять селекции пчел по гигиеническому поведению, устойчивых к паразитированию клещами Varroa spp. Сейчас в мире существует девять устойчивых к клещу V. destructor популяций медоносной пчелы A. mellifera, которые были получены путем целенаправленной селекции: 1) популяция медоносных пчел северного графства Дублин в Ирландии; 2) популяция медоносных пчел подвида A. m. scutellata в Бразилии и Южной Африке; 3) популяция медоносных пчел в Тулузе во Франции; 4) популяция медоносных пчел на острове Фернандо де Норонья в Бразилии; 5) приморская популяция медоносных пчел в Приморском крае России; 6) популяция медоносных пчел Готланд в Швеции; 7) популяция медоносных пчел Авиньон во Франции; 8) популяция медоносных пчел Арнотского леса в Итаке в штате Нью-Йорк США; 9) популяция медоносных пчел на острове Мармара в Турции (Mondragón et al., 2005;Allsopp, 2006;Locke, Fries, 2011;Çakmak, Fuchs, 2013;Locke, 2016;Conlon et al., 2018;McMullan, 2018;Alphen, Fernhout, 2020). Селекция семей медоносных пчел по гигиеническому поведению на устойчивость к клещу V. destructor позволит использовать меньше акарицидов и предотвратить нарушения микробиома кишечника, обеспечивающего защитную функцию организма и играющего важную роль в иммунитете и адаптации пчел к условиям окружающей среды (Çakmak, Fuchs, 2013). ...
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Ильясов, Р.А., Такахаши, Д.И., Ли, М.Л., Прощалыкин, М.Ю., Лелей, А.С., Квон, Х.В., Даниленко, В.Н., Николенко, А.Г., 2022. Характеристика клещей Varroa underwoodi (Acari Varroidae) в популяции Apis cerana ussuriensis (Hymenoptera: Apidae) в Приморском крае, Россия. Журнал Общей Биологии. 83 (1), 38-50. doi: 10.31857/S0044459622010055. (SCI, WoS, Scopus). IF = 1,028. Ilyasov, R.A., Takahashi, J.I., Lee, M.L., Proshchalykin, M.Y., Lelej, A.S., Kwon, H.W., Danilenko, V.N., Nikolenko, A.G., 2022. Characteristics of Varroa underwoodi mites (Acari: Varroidae) in the population of Apis cerana ussuriensis (Hymenoptera: Apidae) in the Primorsky Krai of Russia. Biology Bulletin Reviews (Zhurnal obshchei biologii). 83 (1), 38-50. doi: 10.31857/S0044459622010055. (SCI, WoS, Scopus). IF = 1,028. ISSN 0044-4596 Abstract. Species of the genus Varroa are ectoparasitic mites of the Apis honey bees. Unlike the well-known species ofmites V. destructor and V. jacobsoni, V. underwoodi is still poorly studied. According to foreign publications, thecurrently recognized distribution of V. underwoodi in the A. cerana population includes Nepal, South Korea,Japan, Malaysia, India, Indonesia, Papua New Guinea, Vietnam, and China. Recently it was discovered inthe Russia (Primorsky Krai) on the honey bees A. cerana ussuriensis. Since V. destructor and V. jacobsoni havethe ability to easily switch to other bee species, there is a possibility that later V. underwoodi may also extensively switch from Asian honey bees A. cerana to European honey bees A. mellifera. The first case of V. underwoodi parasitizing in A. mellifera colonies was recorded in Papua New Guinea. The parasitic mite V. underwoodi requires careful study, since it is a new potential parasite of honey bees A. mellifera, which can also bringnew species and strains of viruses and bacteria, change the composition of the gut microbiome, and disruptthe protective and adaptive mechanisms of the bees. The article presents the data on morphometry and polymorphism of the gene COX1 of mtDNA. Varroa underwoodi was compared with other mite species V. destructor and V. jacobsoni. The mean genetic divergence and p-distance between V. underwoodi and other Varroaspecies were 9% and 0.09, respectively, which are consistent with the level of species differences in insects.The nucleotide sequences of the gene COX1 of mtDNA of V. underwoodi from Primorsky Krai of RussiaLC532104 and from the Jilin province of China MH205176 turned out to be identical and were assigned tothe China 1 MH205176 haplotype. It is assumed that there is continuous migration between the A. ceranapopulations of Russia and China, which led to the spread of V. underwoodi in the natural population of A. cerana ussuriensis in the Primorsky Krai of Russia, and the mite is currently distributed up to 45.06°N. Thus, thenorthern border of the V. underwoodi range is located on the territory of Russian Far East and, probably, coincides with the range of A. cerana ussuriensis. It is likely that the selection of A. mellifera bee colonies for hygienic behavior against the V. destructor mite may also be effective against V. underwoodi and will prevent thepossible transition of V. underwoodi from Asian A. cerana to European A. mellifera. Аннотация. Виды рода Varroa являются эктопаразитическими клещами медоносных пчел рода Apis. В отличие от хорошо известных видов клещей V. destructor и V. jacobsoni, V. underwoodi остается мало изученным. Современный ареал V. underwoodi в популяции A. cerana включает Непал, Южную Корею, Японию, Малайзию, Индию, Индонезию, Папуа-Новую Гвинею, Вьетнам и Китай. Недавно он был найден в России (Приморский край) на A. cerana ussuriensis. Поскольку V. destructor и V. jacobsoni обладают способностью легко переходить на другие виды медоносных пчел, есть большая вероятность того,что V. underwoodi может в дальнейшем перейти в массовом порядке с A. cerana на A. mellifera. Первый случай паразитирования V. underwoodi в семьях пчел A. mellifera зафиксирован в Папуа-Новой Гвинее. Varroa underwoodi требует тщательного изучения, поскольку является новым потенциальным паразитом A. mellifera и способен принести с собой новые виды и штаммы вирусов и бактерий, изменить состав микробиома кишечника пчел, нарушить защитные и адаптивные механизмы их организма. В статье представлены данные морфометрии V. underwoodi и полиморфизма его гена COX1мтДНК. Проведено сравнение V. underwoodi с другими видами клещей V. destructor и V. jacobsoni. Средняя генетическая дивергенция и p-дистанция между V. underwoodi и другими видами Varroa составляли 9% и 0.09 соответственно, что согласуется со средним уровнем видовых различий у насекомых. Нуклеотидные последовательности гена COX1 мтДНК V. underwoodi из Приморского края (Россия) LC532104 и провинции Цзилинь (Китай) MH205176 оказались идентичными и отнесены кгаплотипу China 1 MH205176. Предполагается, что между популяциями A. cerana России и Китая происходит непрерывный обмен, который привел к появлению V. underwoodi в природной популяции A. cerana ussuriensis в Приморском крае. Современная северная граница ареала V. underwoodi проходит по территории Дальнего Востока России и, вероятно, совпадает с таковой A. cerana ussuriensis (45.06° с.ш.). Вероятно, селекция семей пчел A. mellifera по гигиеническому поведению против клещей V. destructor может оказаться эффективной также против V. underwoodi и позволит предотвратить возможный переход V. underwoodi с азиатских пчел A. cerana на европейских пчел A. mellifera.
... they last 1-3 years. Recently however, there are reports of longer survival of free-living colonies (De Jong & Soares 1997;Fries et al., 2006;Le Conte et al., 2007, 2020Locke et al., 2012;Locke & Fries 2011;Seeley 2007Seeley , 2017Seeley et al., 2015). Apparently, far from beekeeping management practices, also in Europe western honey bees are being able to create a host-parasite equilibrium (Blacquière & Panziera 2018;Kohl et al., 2022;McMullan 2018). ...
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The Survivors Task Force (Dall’Olio et al., 2022) of the international research association COLOSS that gathers scientists, researchers, students, veterinarians and agriculture specialists focused on improving the well-being of honey bees, organized a Belgrade city walk tour to visit and observe some of the free-living colonies around the city (Figure 3). The walk was organized as a social event of the IX European Congress of Apidology (Eurbee 9), which was held in September 2022 in Belgrade, free of charge and open to all conference participants and accompanying people. The tour was locally organized and guided by Serbian researchers that studied free-living colonies in detail (JBD and SD) and Survivors Task Force members. Registration for the walk was obligatory, and since the interest was high, two walks were realized on two separate days (Figures 4 and 5).
... These natural hives were heavier but less populated than the non-natural beehives. Reduced colony sizes have been associated with Varroa-surviving colonies 31 . Worker guts from the natural environment displayed bacterial profiles associated with good health, and were enriched in Acetobacteraceae and the gut core members Snodgrasella, Lactobacillus and Commensalibacter (involved in nutrient acquisition and immune responses). ...
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... In the USA, V. destructor-resistant colonies have been selected; their main characteristic is the ability that bees have to detect and clean cells with pupa parasitized by the mite, naming this characteristic VSH (Varroa Sensitive Hygiene) [20,26,27]. Grooming behavior, by which parasitized bees can dislodge mites by themselves (autogrooming) or receiving help from other bees (allogrooming) [28], has been reported as an effective resistance mechanism against V. destructor [24,[29][30][31], although other studies have not found an association between this behavior and the prevalence of the mite [32][33][34]. Both the grooming and hygienic behavior are expressed in a very efficient way in the Asian honey bees Apis cerana, the natural host of V. destructor, and would be keys to control the parasite's population [35][36][37]. ...
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In the past few years there has been an increasing interest for the study of honey bee populations that are naturally resistant to the ectoparasitic mite Varroa destructor, aiming to identify the mechanisms that allow the bees to limit the reproduction of the mite. In eastern Uruguay there are still bees resistant to mites that survive without acaricides. In order to determine if the differential resistance to V. destructor was maintained in other environments, a reciprocal transplant experiment was performed between the mite-resistant bee colonies and the mite-susceptible bee colonies from the east and the west of the country, respectively, infesting bees with local mites. In both regions, the mite-resistant colonies expressed a higher hygienic behavior and presented a higher phoretic mites/reproductive mites and mites in drone cells/mites in worker cells ratio than the mite-susceptible colonies. All the mite-susceptible colonies died during fall–winter, while a considerable number of mite-resistant colonies survived until spring, especially in the east of the country. This study shows that the bees in the east of the country maintain in good measure the resistance to V. destructor in other regions and leaves open the possibility that the mites of the two populations have biases in the reproductive behavior.
... Feral or wild honey bee colonies live in a nonmanaged environment and are under natural selection. In this environment, Varroa destructor mites persist, and the bees are equipped with greater immunocompetence (Seeley 2007, Locke and Fries 2011, López-Uribe et al. 2017. Previous reports showed that colonies living in traditional trmka hives, similar to feral colonies, were free of several major bee pathogens and viruses (Taric et al. 2019). ...
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