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Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate


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An isolated honey bee population (N = 150) was established on the southern tip of Gotland, an island in the Baltic sea. After infestation with 36 to 89 Varroa destructor mites per colony, they were unmanaged and allowed to swarm. For over six years colonies were monitored for swarming, winter losses, infestation rate in the fall, and bee population size in the spring. Winter mortality rate decreased from 76% and 57% in the third and fourth years, to 13% and 19% in the fifth and sixth years. Swarming rates increased from zero the third field season to 57.1% and 36.4% in the last two years. The mite infestation on adult bees decreased during the last two years, from 0.47% in the third year to 0.19% and 0.22% respectively. Our data suggest that a host-parasite co-adaptation has occurred ensuring survival of both the host and the parasite. The mechanisms behind this co-adaptation require further study.
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Apidologie 37 (2006) 1
INRA/DIB-AGIB/EDP Sciences, 2006
DOI: 10.1051/apido:2006031 Original article
Survival of mite infested (Varroa destructor)honeybee
(Apis mellifera) colonies in a Nordic climate
Ingemar Fa, Anton Ib, Peter Rc
aDepartment of Entomology, Swedish University of Agricultural Sciences, Box 7044, 750 07 Uppsala, Sweden
bSwiss Apicultural Institute, FAM, Liebefeld, 3003 Bern, Switzerland
cState Institute of Apiculture, University of Hohenheim, 70593 Stuttgart, Germany
Received 7 November 2005 – accepted 23 December 2005
Abstract An isolated honey bee population (N =150) was established on the southern tip of Gotland,
an island in the Baltic sea. After infestation with 36 to 89 Varroa destructor mites per colony, they were
unmanaged and allowed to swarm. For over six years colonies were monitored for swarming, winter losses,
infestation rate in the fall, and bee population size in the spring. Winter mortality rate decreased from 76%
and 57% in the third and fourth years, to 13% and 19% in the fifth and six years. Swarming rates increased
from zero the third field season to 57.1% and 36.4% in the last two years. The mite infestation on adult bees
decreased during the last two years, from 0.47% in the third year to 0.19% and 0.22% respectively. Our data
suggest that a host-parasite co-adaptation has occurred ensuring survival of both the host and the parasite.
The mechanisms behind this co-adaptation require further study.
Varroa destructor /Apis mellifera /host-parasite interaction /survival /adaption
Varroa destructor Anderson and Trueman
mites have become a major plague for world
beekeeping of European bees (Apis mellif-
era L.), although the impact from mite in-
festations varies greatly between continents
(Rosenkranz, 1999). The original host of the
mite V. destructor, the Asian honey bee Apis
cerana Fabr., is not damaged to any apprecia-
ble degree by the infestations mainly because
mite reproduction occurs only in drone brood,
and mites become increasingly entrapped in
dying drone brood when the mite population
increases (Rath and Drescher, 1990). Groom-
ing of mites is also more eective in A. cerana,
compared to A. mellifera (Peng et al., 1987),
but the impact from this behaviour on mite
tolerance probably has been over emphasized
(Fries et al., 1996).
Corresponding author: I. Fries,
It is well documented that Africanized
honey bees (Apis mellifera adansoni imported
into Brazil) also survive and coexist with V. d e -
structor in South America (Rosenkranz, 1999)
and similar host-parasite adaptations have also
been reported from North Africa (Boecking
and Ritter, 1993). In Europe, however, it is
generally accepted that the mite population
must be controlled to avoid colony collapse
(Fries et al., 1994). Nevertheless, although
data demonstrate that in a Nordic climate
colonies infested by V. destructor are dam-
aged and are likely to die over winter only
three years post infestation (Korpela et al.,
1993), there are frequent anecdotal reports in
beekeeping journals of mite infested colonies
surviving extended periods without mite con-
trol. Although such claims are often dicult to
verify, a documented case of European honey
bees surviving mite infestation without treat-
ment is found on an island 345 km othe
coast of Brazil (de Jong and Soares, 1997).
Italian bees infested with V. destructor were
2 I. Fries et al.
introduced in 1984 onto this island and this bee
population later increased in size without mite
control (de Jong and Soares, 1997). Recently,
the return of feral bee populations has been re-
ported from France (Le Conte, 2004) and the
USA (Seeley, 2004), indicating long-term sur-
vival of non-treated mite infested honey bee
colonies in Europe as well as in the US. In
France there are also reports of mite tolerant
bees developing based on bee material brought
into Europe from Tunesia (Kefuss et al., 2004).
It remains unknown if this development oc-
curs because of increased mite tolerance in the
host, reduced virulence in the parasite (with
the virus infections vectored), or both.
Epidemiological considerations predict that
honey bees and V. destructor may develop
a benign host-parasite relationship, but this
depends on beekeepers maintaining selection
pressure on both the bees and mites imposed
by the infestations. This means that beekeepers
should not constantly remove mites from the
system through mite control methods (Fries
and Camazine, 2001). Host-parasite adapta-
tions have probably occurred where mites and
bees coexist, although these processes have
not been documented. On the other hand, the
introduction of an exotic parasite, V. destruc-
tor, into a new host system, A. mellifera, could
potentially lead to local eradication of the
honey bee species. The invasion of an exotic
species into an ecosystem is currently viewed
as one of the most important sources of biodi-
versity loss and may lead to host eradication
(Deredec and Courchamp, 2003).
We have studied the survival rate for over
six years in a population of V. destructor in-
fested honey bee colonies in an isolated area
to determine if all colonies would perish, and
their parasites along with them.
In 1999 we established a genetically diverse
honey bee population of 150 honey bee colonies in
8 apiaries with variable distances between apiaries
(500 m to 2 km). The apiaries (N5801’–N5804’,
E1809’–E1815’, only a few meters above sea
level) were located on “Sudret”, which is the south-
ern tip of the island Gotland in the Baltic sea, iso-
lated from the main island through a narrow land
bridge. In July of the same year, these mite free
colonies were infested with 36 to 89 V. destructor
by adding 400 cm3of bees (number of mites cal-
culated from three separate sub-samples), collected
from mite infested colonies. No mite treatments
were performed at all and the colonies were allowed
to swarm at will. The only management of experi-
mental colonies throughout the six year monitoring
period consisted of data sampling and of feeding
of sugar solution for winter in cases where honey
stores were deemed insucient for winter survival.
The hives used were Swedish standard hives with a
frame size of 366 ×222 mm. Throughout the exper-
iment each colony has had access to two boxes with
a total of 20 combs. The background and the origin
of the bees and the impact from swarming on mite
population dynamics have been described in some
detail (Fries et al., 2003).
2.1. Data collection and analysis
Inspections of all colonies were done 4 times
each year during the summers of 2000–2005 to reg-
ister if colonies had swarmed or not. When colonies
had emerged queen cells and a break in brood pro-
duction, they were registered as swarming colonies.
Swarms were collected on site upon inspection or
from swarm boxes put up in the experimental area.
In one colony with mature queen cells in 2003,
an artificial swarm was produced to avoid losing
this swarm. In 2004 and in 2005 four artificial
swarms each year were made the same way follow-
ing swarm preparations in individual colonies. In
2004, one natural secondary swarm was also cap-
tured. Swarms collected or produced were placed in
separate apiaries each year but returned to the api-
ary where they originated the following year.
Late October 2000–2005, when colonies have
no sealed brood in the study region, samples of
approximately 100 cm3of bees were taken from
all colonies to measure mite infestation levels.
Colonies that were wintered each year were re-
garded as surviving the winter if they had a queen
and enough bees (i.e. more than 1000 bees) to ex-
pand in June the following year.
During the first inspection (late April or early
May) each year, the size of the bee population in
each colony was investigated from 2001 through
2005 by examining the combs and estimating the
number of bees on each comb (Imdorf et al., 1987).
Throughout the experiment, no attempt was made
to strengthen any colony by adding bees, or to re-
place failing queens. Thus, a few colonies were lost
Survival of mite infested honey bee colonies 3
Figure 1. Mortality rate of honey bee colonies over
six winters without control of Varroa destructor.
N=number of colonies in late October each year.
Bars with dierent letters above are significantly
dierent between years (P<0.05, chi-square).
during the breeding season not due to colony col-
lapse, but to queens becoming drone layers. This
explains why some colonies disappeared from the
experiment for reasons other than winter mortality.
The proportion of colonies that died each winter
and the swarming rate of colonies each field sea-
son were compared between years using chi-square
statistics. The mite load of colonies in late fall was
compared using a Kruskall-Wallis test for mite in-
festation rate, with year as grouping variable. The
data for each year were also analyzed by correlat-
ing first the mite infestation in the fall with the bee
population size in the spring (between years, over
winter) and second the bee population in the spring
with the mite population in the fall (within year,
over summer). The influence of the mite infestation
level on bee population size in the spring and the
influence of the bee population size in the spring on
the mite infestation level in the fall were also an-
alyzed (ANOVA) where the influence of year was
added to the respective models.
3.1. Winter mortality, swarming
and mite infestation rate
Figure 1 shows the mortality rates of win-
tered colonies each year of the experiment.
The mortality rate during winter decreased af-
ter the third year of the experiment when more
than 80% of the wintered colonies died. The
Figure 2. Swarming rate of honey bee colonies for
six years without V. destructor control. N =number
of colonies in late May each year. Bars with dier-
ent letters above are significantly dierent between
years (P<0.05, chi-square).
mortality rates during the two last years of
the experiment were not significantly dier-
ent from the first winter with low mite infesta-
tion levels (P>0.05, chi-square), whereas the
mortality rates the last two winters were sig-
nificantly lower compared to the two preced-
ing years (P<0.05, chi-square). The swarm-
ing rate of colonies throughout the experi-
ment showed the opposite trend compared to
the mortality rate (Fig. 2). During the third
year, no colony showed any swarming ten-
dency, whereas the swarming frequency in-
creased significantly in the last years of the
experiment (Fig. 2) (P<0.05, chi-square).
The mite infestation levels on adult bees in
the fall in broodless colonies are graphed in
Figure 3. The average infestation levels were
significantly reduced by about 50% during the
sixth and seventh fall recordings from high in-
festation rates of 40 or more mites per 100 bees
during the second to the fourth fall of the ex-
periment (P<0.05, Kruskall –Wallis).
Table I lists the number of colonies and
swarms that survived throughout the experi-
ment. The survival of swarms did not seem to
be better compared to the “mother” colonies
(here called “original colony”), which re-
mained in the apiary with the new queen. This
finding is congruent with earlier evaluations
from the same experiment (Fries et al., 2003).
4 I. Fries et al.
Table I. Number of wintered and surviving original colonies and swarms respectively and total number or
colonies in the experiment.
Year Parameter Original Swarms Swarms Swarms Swarms Swarms Total, no of
colonies 2000 2001 2003 2004 2005 colonies
1999 Wintered 150 - ----150
2000 Survived 142 - ---- 142
2000 Wintered 130 16 ----146
2001 Survived 92 12 ----104
2001 Wintered 91 12 17 - - - 120
2002 Survived 21 8 0 - - - 29
2002 Wintered 17 4 0 - - - 21
2003 Survived 9 0 0 - - - 9
2003 Wintered 8 0 0 1 - - 8
2004 Survived 6 0 0 1 - - 7
2004 Wintered 6 0 0 1 4 - 11
2005 Survived 5 0 0 1 3 - 9
2005 Wintered 5 0 0134 13
Figure 3. Average infestation rate of adult bees in
brood-less colonies in late October each year. N =
number of colonies in late October sampled each
year. Bars with dierent letters above are signifi-
cantly dierent between years (P<0.05, Kruskall-
3.2. Mite infestation in the fall vs. bee
population the following spring
There was a significant negative correlation
between the mite infestation rate in the fall and
the size of the bee population in the spring for
each winter even when colonies that died over
winter were removed from the data set (Tab.
II). When data from all the years were com-
bined this negative relationship remained (–
0.31, P<0.001). An analysis of variance (data
not shown), with bee population size in the
spring as the dependent variable and mite in-
Table II. Correlation coecients between mite in-
festations in the fall and bee population size in
the spring (log10) the following year in surviving
colonies. Values are given for each year separately
and for the combined data set.
Winter Correlation coecient N P-value
1999/2000 –0.20 15 0.49
2000/2001 –0.42 121 <0.001
2001/2002 –0.12 36 0.50
2002/2003 –0.33 11 0.33
2003/2004 –0.46 7 0.32
2004/2005 –0.77 9 0.013
1999–2005 –0.33 199 <0.001
festation rate during fall (not including the first
winter when mite levels were low (Fig. 1)) and
year as independent variables, demonstrated
that both parameters had a significant influ-
ence (P<0.0001) on the variation in bee pop-
ulation size in the spring.
3.3. Bee population in the spring vs. mite
infestation the same fall
For the two years with the largest numberof
observations (2001 and 2002) and for the fifth
year there was a significant positive correlation
between the bee population size in the spring
and the mite infestation rate during the same
fall, (Tab. III). When data from all the years
were combined there was a significant positive
Survival of mite infested honey bee colonies 5
Table III. Correlation coecients between bee
population size in the spring (log10) and mite in-
festations in the fall the fall of the same year. Val-
ues are given for each year separately and for the
combined data set.
Summer Correlation coecient N P-value
2000 0.44 14 0.12
2001 0.27 103 0.006
2002 0.54 21 0.01
2003 –0.18 7 0.71
2004 0.87 7 0.008
2005 –0.08 9 0.84
2000–2005 0.27 161 0.0004
correlation (0.27, P<0.001). An analysis of
variance (data not shown), with the fall mite
infestation rate as the dependent variable and
the bee population size in the spring and year
as independent variables, demonstrated only a
tendency (P=0.12) of a direct influence from
the bee population size on the variation in fall
mite infestation rates.
This is the first experimental data from Eu-
rope with continuous monitoring where it is
demonstrated that honey bee colonies infested
by V. destructor may survive for over 6 years
even if mite control is not practiced. The pre-
sented data suggest that some form of adapta-
tion has occurred in the system, ensuring the
survival of both the host and the parasite. The
fact that (i) the proportion of colonies that died
over winter decreased significantly (Fig. 1),
(ii) the swarming incidence increased (Fig. 2),
and (iii) the mite infestation rate of adult
bees in the fall decreased significantly (Fig. 3)
strongly supports the hypothesis that the sys-
tem will develop a host-parasite relationship
where both parties will survive even if mite
control is not practiced. This is what could be
predicted from an evolutionary epidemiolog-
ical perspective (Fries and Camazine, 2001)
provided the host population does not perish.
Whether this persistent relationship is depen-
dent on the bees becoming mite tolerant, the
mites (and vectored virus infections) becom-
ing less virulent, or both, remain to be investi-
Our experiment demonstrated that most
colonies were likely to succumb within the
first three years if left untreated, which was ex-
pected from previous experience. During this
phase of selection a fluctuating population size
of the honey bee colonies, induced by the mite
parasitism, may have supported the survival of
some colonies even without changes in host
resistance or parasite virulence. Such a pat-
tern became clear when the interactions be-
tween the host and the parasite were consid-
ered. First it was obvious that there was a sig-
nificant negative correlation between the mite
infestation rate in the fall and the number of
bees in the following spring (except for the
first year when no eect was expected because
the mite population was still low). This obser-
vation was supported by the results from an
analysis of variance where both the influence
from winter and mite infestation level in the
fall had a significant impact on the spring pop-
ulation size of the bees. This means that the
mite infestation level in the fall was decisive
for how well the colonies survived the win-
ter, something previously demonstrated in an
earlier phase of this experiment (Fries et al.,
2003). Likewise, the bee population size in the
spring seemed to influence the mite infestation
rate in the fall (Tab. III) with a positive corre-
lation for most part of the data set. An analysis
of variance, however, demonstrated no signifi-
cant tendency (P=0.12) of a direct influence
from the bee population size on the variation
in fall mite infestation rates.
Thus, the data confirm that heavy mite in-
festation levels in the fall led to poor win-
tering survival. Those colonies that neverthe-
less did survive with small number of bees
also had small absolute numbers of mites be-
cause mites and bees had similar death rates
in over-wintering colonies (Fries and Perez-
Escala, 2001). Some of these colonies may
then grow to be suciently strong by the next
winter, but at that point would have lower
mite infestation levels compared to the previ-
ous fall. Thus, some colonies in the experi-
ment may have survived part of the time be-
cause of this dynamic host-parasite interac-
tion. This is an important observation, because
it puts anecdotal observations by beekeepers
of surviving colonies in a dierent perspective.
6 I. Fries et al.
Survival of individual colonies, also for ex-
tended periods, does not necessarily mean that
such bees have developed specific traits for tol-
erance to V. destructor. For the colonies in our
experiment that were still alive after over six
years without mite treatment it is dicult to
know if survival depended on random events
or on specific traits. But although the number
of colonies that have survived in the present
experiment is limited, the significant increase
in colony survival and swarming rates and the
decrease in mite infestation rates clearly indi-
cated that the reported development was not
driven primarily by fluctuating dynamics in
mite and bee population sizes. The only pos-
sible conclusion that explains the experimental
outcome is an adaptive processon behalf of the
bees, the mites, or both. The course of V. d e -
structor infestation over the years shows simi-
larities to the development observed in a trop-
ical island of Brazil where mite infested Eu-
ropean bee colonies were left untreated since
1984: after an increase in the infestation levels
of the adult bees during the first years the in-
festation decreased continuously leading to an
obviously balanced relationship between host
and parasite till today (de Jong and Soares,
1997; de Jong 2005, pers. comm.). Unfortu-
nately, also in this case, the critical factors for
this stable situation are unknown.
Our results allow us to conclude that the
problems facing the apicultural industry with
mite infestations probably is linked to the api-
cultural system, where beekeepers remove the
selective pressure induced from the parasitism
by removing mites through control eorts.
Further experiments must confirm whether se-
lection experiments as described here can be
used as a basis for further honey bee breeding
The dedicated eorts from beekeeper Åke Ly-
berg in supplying infrastructure and ground sup-
port is highly appreciated. The study had finan-
cial support from the National Board of Agriculture
through the European Commission supported “Na-
tional programme for support of beekeeping and
sale of honey”, from the “Gesellschaft der Freunde
der Landesanstalt für Bienenkunde an der Univer-
sität Hohenheim e.V.”, and from the Swiss Beekeep-
ers Association. All highly appreciated.
Résumé Survie de colonies d’abeilles (Apis mel-
lifera) infestées d’acariens (Varroa destructor)en
climat nordique. Une population d’abeilles do-
mestiques (Apis mellifera) isolée et génétiquement
diverse de 150 colonies a été installée dans huit ru-
chers afin d’étudier si les acariens Varroa destruc-
tor pouvaient éradiquer la population hôte. Après
avoir ajouté la même année entre 36 et 89 acariens
par colonie, on n’est plus intervenu sur les colonies
et on les a laissé essaimer à leur guise. Durant six
ans on a noté les essaimages, le taux d’infestation
par les acariens à l’automne et la taille de la po-
pulation d’abeilles au printemps. Dans la mesure
du possible, les essaims ont été capturés et utilisés
pour regonfler les colonies. Nos données montrent
qu’une certaine forme d’adaptation a dû avoir lieu
dans le système, permettant la survie à la fois de
l’hôte et du parasite. Le fait que (i) la proportion de
colonies mourant durant l’hiver ait diminué signifi-
cativement (Fig. 1), (ii) que l’incidence de l’essai-
mage se soit accru après plusieurs années (Fig. 2),
et (iii) que les taux d’infestation des abeilles adultes
à l’automne aient diminué (Fig. 3) corrobore forte-
ment l’hypothèse selon laquelle le système se déve-
loppe en une relation hôte-parasite où les deux par-
ties survivent. Du point de vue de l’épidémiologie
évolutive, ceci correspond à la prédiction (Fries et
Camazine, 2001) à condition que la population hôte
ne meure pas. Il reste à étudier si ce développement
repose sur la tolérance des abeilles aux acariens, sur
la moindre virulence des acariens (et des infections
virales qu’ils véhiculent) ou sur les deux.
Les données récoltées suggèrent que les fortes in-
festations par V. destructor à l’automne peuvent être
la cause de mauvais résultats d’hivernage et que
les colonies qui néanmoins survivent avec un pe-
tit nombre d’abeilles puissent parfois se développer
susamment et passer l’hiver suivant, mais avec
des taux d’infestation moindres (Tabs. II, III). Cer-
taines colonies de l’expérimentation ont pu ainsi
survivre un temps en raison de cette interaction
dynamique hôte-parasite. Cela n’explique pourtant
pas les variations de taux dans la mortalité hiver-
nale, les taux d’essaimage, ni les taux d’infestation.
Les résultats suggèrent que le problème sur le long
terme de l’apiculture avec les infestations par V. d e s -
tructor est lié au système apicole, dans lequel les
apiculteurs suppriment la pression de sélection in-
duite par le parasitisme en éliminant les acariens par
des traitements.
Varroa destructor /Apis mellifera /interaction
hôte-parasite /survie /adaptation
Zusammenfassung Das Überleben milbeninfi-
zierter (Varroa destructor) Honigbienenvölker in
einem nordischen Klima. Um zu untersuchen, ob
Survival of mite infested honey bee colonies 7
Varroamilben (Varroa destructor) eine Wirtspopu-
lation ausrotten können, wurde eine isolierte und
genetisch diverse Bienenpopulation aus 150 Bie-
nenvölkern auf 8 Bienenständen eingerichtet. Nach
Zufügung von 36 bis 89 Milben pro Volk im Juli
des gleichen Jahres konnten die unbewirtschafteten
Völker nach Belieben Schwärmen und wurden über
einen Zeitraum von 6 Jahren auf Schwarmhäufig-
keit, Milbenbefallsrate im Herbst und Bienenpopu-
lation im Frühjahr untersucht. Soweit möglich, wur-
den die Schwärme eingefangen und zur Ergänzung
der Population genutzt. Die vorgelegten Daten zei-
gen, dass in dem System eine Form von Anpassung
aufgetreten sein muss, die das Überleben von Wir-
ten und Parasiten ermöglichte. Die Tatsache, dass
(i) der Anteil über Winter gestorbener Völker si-
gnifikant abnahm (Abb. 1), (ii) nach mehreren Jah-
ren die Schwarmtätigkeit wieder zunahm (Abb. 2)
und (iii) die Milbenbefallsrate der adulten Bienen
im Herbst abnahm (Abb. 3), ist eine starke Unter-
stützung für die Hypothese, dass sich das System in
Richtung einer Wirt-Parasit-Beziehung entwickelt,
bei der beide Partner überleben. Aus einer evolu-
tionären epidemiologischen Perspektive entspricht
dies der Vorhersage (Fries und Camazine, 2001)
unter der Vorraussetzung, dass die Wirtspopulation
nicht zuvor zu Grunde geht. Ob diese Entwicklung
darauf beruht, dass die Bienen milbentolerant wur-
den, die Milben (zusammen mit den übertragenen
Viren) weniger virulent wurden oder beides, muss
noch geklärt werden.
Die gesammelten Daten legen weiterhin nahe, dass
ein hoher Milbenbefall im Herbst zu schlechten
Überwinterungsergebnissen führt. Völker, die trotz
geringer Bienenanzahlen dennoch überleben, wur-
den häufig über die Saison genügend stark um den
nächsten Winter zu überleben, wobei sie dann einen
geringeren Milbenbefall aufwiesen. Es ist daher
möglich, dass einige der Völker in dem Experiment
über einen Teil der Versuchszeit auf Grund dieser
Dynamik in der Wirt-Parasit-Beziehung überlebt
haben. Dies erklärt allerdings nicht die Änderung
in der Wintermortalität, der Häufigkeit des Schwär-
mens oder der Milbenbefallsrate. Die Ergebnisse le-
gen weiterhin nahe, dass das langjährige Problem
der Bienenhaltung mit dem Milbenbefall vermut-
lich mit der Methode der Bienenhaltung zusammen-
hängt, bei der die Imker den von den Parasiten aus-
geübten Selektionsdruck beseitigen, indem sie die
Milben durch Behandlungsmaß-nahmen entfernen.
Varroa destructor /Apis mellifera /Wirt-Parasit-
Beziehung /Überleben /Anpassung
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... Also of interest is the slower increase in DWV titre development for the MR colonies between April and August. The final panel shows the development of the phoretic varroa infestation rate on adult bees from October 2014 to April 2016, which is consistent with how these rates develop in similar experiments with colonies from this varroa-surviving population 8,10,[14][15][16] . The data for the other four time-points during 2015 was unfortunately lost. ...
... The MR colonies also reared less brood, particularly drone brood, had higher incidence of chalkbrood and were more inclined to supercede at all times during the season. These are all traits associated with small colonies that, coincidentally or not, also slow varroa population development, and are known features of these MR colonies 8,10,12,15 . In other words, many of the beneficial varroa-surviving features of the MR colonies, including possible metagenomic ones, may simply be an indirect consequence of their smaller size, similar to varroa-surviving Africanized bees 4,8,11,12 . ...
... Colony establishment and origin. The varroa-surviving honeybee population investigated in these studies originated in 1999 on the island of Gotland, Sweden, as a part of selection experiment on honeybee survival with Varroa destructor mites 8,10 . The original population was constituted to have as broad a genetic basis as possible, which was achieved by collecting 120 colonies from throughout mainland Sweden with a wide diversity of locally adapted, pure-bred and mixed-race genetic backgrounds 10 Monitoring, bee marking and sample collection. ...
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There is increasing evidence that honeybees (Apis mellifera L.) can adapt naturally to survive Varroa destructor, the primary cause of colony mortality world-wide. Most of the adaptive traits of naturally varroa-surviving honeybees concern varroa reproduction. Here we investigate whether factors in the honeybee metagenome also contribute to this survival. The quantitative and qualitative composition of the bacterial and viral metagenome fluctuated greatly during the active season, but with little overall difference between varroa-surviving and varroa-susceptible colonies. The main exceptions were Bartonella apis and sacbrood virus, particularly during early spring and autumn. Bombella apis was also strongly associated with early and late season, though equally for all colonies. All three affect colony protein management and metabolism. Lake Sinai virus was more abundant in varroa-surviving colonies during the summer. Lake Sinai virus and deformed wing virus also showed a tendency towards seasonal genetic change, but without any distinction between varroa-surviving and varroa-susceptible colonies. Whether the changes in these taxa contribute to survival or reflect demographic differences between the colonies (or both) remains unclear.
... High V. destructor loads preceding summer collapse 22,50 or wintering [21][22][23] were identified as the main risk factors for honey bee colony losses throughout the season. But it is the high infestation rates in autumn that cause more common winter colony deaths and are of serious concern in bee management. ...
... Interannual deviances from the long-term mean mite abundance identified in this study were synchronized across-colonies and were potentially associated with common environmental drivers or horizontal spread of mites [51][52][53] . Besides the climatic impacts, interannual changes in mite infestation may result from fluctuating dynamics in bee and mite survival 21,23 . We may expect that heavy autumn mite infestation rates reduced the number of bees that survived winter. ...
... Regrowth of mite populations follows the rehabilitation of bee colonies. However, the autumn numbers of mites would be smaller than in the previous year, as suggested by Ref. 23 , unless the weak colonies were merged. ...
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Varroa destructor is the main pest of the honey bee Apis mellifera, causing colony losses. We investigated the effect of temperature on the autumn abundance of V. destructor in bee colonies over 1991–2020 in Central Europe. We tested the hypothesis that temperature can affect autumn mite populations with different time-lags modulating the bee abundance and brood availability. We showed that raised spring (March–May) and autumn (October) temperatures reinforce autumn V. destructor infestation in the bee colonies. The critical temperature signals embrace periods of bee activity, i.e., just after the first cleansing flights and just before the last observed bee flights, but no direct effects of phenological changes on V. destructor abundance were found. These effects were potentially associated with increased bee reproduction in the specific periods of the year and not with the extended period of activity or accelerated spring onset. We found significant effects of autumn bee abundance, autumn capped brood abundance, and the number of colonies merged on autumn mite infestation. We also observed differences in V. destructor abundance between bees derived from different subspecies. We indicated that climatic effects, through influence on the bee abundance and brood availability, are one of the main drivers regulating V. destructor abundance.
... There is a widely accepted view that unmanaged (wild/feral) honey bee populations were completely eradicated in Europe since the 1980s, following the introduction and spread of Varroa and the associated spillover of various pathogens [26,27]. However, several studies reported that both feral and managed colonies can survive for an extended period despite of Varroa infestation, and without receiving any treatments, triggering wide scientific and public attention [28][29][30][31][32][33][34][35][36][37]. ...
... Available chemical treatments against Varroa mite do not provide a long-term solution (due to the development of resistance to pesticides), while some are even harmful to bees [65,66]. Moreover, any kind of treatment may inhibit natural selection pressures preventing coevolution between parasite and host, thus being counterproductive [33,43,67,68]. In uncontrolled/wild settings natural selection will lead toward disease-resistant bees and less virulent forms of pathogens [69,70]. ...
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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.
... From infestation in 1952 and1987 to the early 2000s, wild and feral honeybees were believed to have been cleared out by V. destructor in Europe and North America, respectively (Jaffé et al., 2010;Kraus and Page, 1995;Moritz et al., 2007). However, in the mid-2000 s, some wild and feral colonies were reported to survive interactions with V. destructor in France (Le Conte et al., 2007), Sweden (Fries et al., 2006), and the USA (Seeley, 2007). This increases concerns regarding the availability and stability of future honeybee pollination services (Potts et al., 2010). ...
Evidence of a decline in wild pollinators is increasing across global and local habitats. However, with regional variation, the number of managed pollinators has increased globally. Whether these managed pollinators can sufficiently meet the agricultural pollination demand given wild pollinator declines remains unclear. Data on 49 honeybee-pollinated crops cultivated worldwide and stocked honeybee colonies were analysed to assess the pollination demand and pollination service capacity between 1989 and 2019. We found a rapidly increasing demand for honeybee pollination but a decreasing pollination service capacity of honeybee colonies. Globally, the demand for honeybee pollination rose approximately 2.3 times higher than the stocked number of honeybee colonies in 2019, growing 1.78% annually, almost 2 times faster than honeybee colonies (0.95%). On average, the pollination service capacity, growth rates of demands for honeybee colony stocks and honeybee pollination, and diversity of honeybee-pollinated crops varied regionally. Nevertheless, fluctuation of the honeybee-pollination demand increased with increased fluctuation of crop diversification. Oil crops accounted for over 70% of the world's honeybee-pollination demand in 2019, with soybean and rapeseed accounting for 39% and 16%, respectively. This was the case in less diversified countries, where a few crops dominated the demand for honeybee pollination, including American countries such as Argentina, Brazil, and the USA, compared to more diversified countries such as China, India, and Japan in Asia. Our study shows that managed pollinators are far too insufficient to adequately supply the agricultural pollination demand worldwide. This emphasises the importance of ongoing calls for protecting pollinators and the integrated management of honeybees and wild pollinator assemblages for a sustainable food-secure future world.
... This was until the arrival of taufluvalinate (Apistan®) and its ease of use (1989). Indeed, without annual treatment, most colonies collapse within three years or less (around 80% colony loss) (Fries et al., 2006). However, in 1995, the first case of tau-fluvalinate resistance was reported under laboratory conditions (Milani, 1995). ...
Background Varroa destructor is a parasite of honeybees. It causes biological damage leading to the colony collapse in the absence of treatment. In recent years, acaricide resistance has emerged in Varroa mites, leading to a decrease in treatment efficacy. We modelled the action of Apivar® (amitraz) treatment, using three input parameters: treatment duration, treatment period, and daily mortality due to the treatment. The output parameters were cumulative mite mortality during treatment, the residual number of Varroa mites, and treatment efficacy, expressed as a percentage. Results The model was validated by monitoring efficacy in the field, in 36 treated hives. According to the model, treatment in the absence of brood is optimal. For a long period without egg laying during the winter, an initial infestation of 100 mites and a start date for treatment of August 7th, a minimal treatment efficacy of 98.8% is required for stabilisation of the mite population for year to year. More effective treatment is associated lower cumulative numbers of dead Varroa mites over the entire treatment period. Thus, the total number of dead mites observed during the monitoring of field efficacy provides information about more than just the initial level of colony infestation. The proportion of resistant mites can be modelized by a decrease of daily mortality rate influencing treatment efficacy. Management of the initial Varroa mite infestation of the colony by the beekeeper can compensate for the decrease in treatment efficacy for resistance thresholds of up to 40% of resistant mites. Conclusion Treatment efficacy depends on several parameters, including initial level of infestation, treatment period and the presence of acaricide resistance. Amitraz resistance may lead to treatment failure, even if the beekeeper is able to keep initial infestation rates low. This article is protected by copyright. All rights reserved.
... Adequate control of Varroa mites is of crucial importance in modern bee keeping practice as noncontrolled varroosis inevitably leads to the colony loss in a couple of years (Fries et al., 2006;Rosenkranz et al., 2010). Varroa problem persists mostly because of insufficient efficiency of available acaricides, both synthetic (Beaurepaire et al., 2017;Gonz alez-Cabrera et al., 2013, 2016Kamler et al., 2016;Kanga et al., 2010;Loucif-Ayad et al., 2010;Maggi et al., 2010;Stara et al., 2019) and naturalbased ones (Conti et al., 2020;Floris et al., 2004;Pietropaoli & Formato, 2018, 2019Underwood & Currie, 2005;Vandervalk et al., 2014). ...
In a cage experiment, lithium chloride (LiCl) and lithium citrate hydrate (Li-cit) were tested for varroacidal efficacy and impact on bees. Treatment with Li-cit (4, 7.5, 10, and 25 mM) resulted in 100% varroacidal efficacy and 100% bee survival. Due to better results in the cage experiment, Li-cit was further tested in field experiments on full-sized free-flying colonies treated three times in 6-day intervals. All the concentrations of Li-cit in the field experiment (5, 10, 15, 20, and 25 mM) expressed high varroacidal efficacy: 93.2–95.5%, significantly (p < 0.01) greater than in the negative and positive (amitraz-treated) controls. Lithium residues in honey from brood chambers were much higher nine months after the last treatment (169.3–1756.0 μg/kg) than seven days post-treatment (19.2–27.8 μg/kg). In honey from honey chambers (eligible for human consumption), the average lithium residues were 26.9 μg/kg and 33.7 μg/kg seven days after the last treatment. In wax combs taken from the brood chamber nine months post-treatment, lithium residues ranged from 410 μg/kg to 2314 µg/kg, without significant differences from the negative control. Lithium residues in wax matrices seven days after the last treatment were in a narrow range of 234.3–300 µg/kg, in wax combs and cappings being significantly lower than in commercial wax foundations. For the first time, Li-cit proved to be effective against Varroa destructor under field conditions.
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Bees are the major pollinators in natural ecosystems and in the agricultural production of several crops used for human consumption. However, they are exposed to multiple stressors that are causing a serious decline in their population. We highlight a major one among them, the Varroa destructor mite (Varroa) that causes severe impacts on the health of honey bee colonies, transmitting a variety of viruses that can affect the survival ability of individual bees and entire colonies. Diagnosis and mite control methods have been intensively studied in recent decades, with many studies in different areas of knowledge having been conducted. This overview summarizes these studies with a focus on colony defense systems, biological characteristics of the parasite Varroa, diagnostic methods used to establish the infestation level of colonies, and currently used control methods.
Conference Paper
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Results of Livestock Research Activities Completed During 2020
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The ectoparasite Varroa destructor Anderson and Trueman is the most important parasites of the western honey bee, Apis mellifera L . The most widely currently used treatment uses formic acid (FA), but the understanding of its effects on V . destructor is limited. In order to understand the mechanism of action of FA, its effect on Varroa mites was investigated using proteomic analysis by liquid chromatography-mass spectrometry/mass spectrometry (LC-MS/MS). V . destructor was collected from honey bee colonies with natural mite infestation before and 24 h after the initiation of FA treatment and subjected to proteome analysis. A total of 2637 proteins were identified. Quantitative analysis of differentially expressed candidate proteins (fold change ≥ 1.5; p ≤ 0.05) revealed 205 differentially expressed proteins: 91 were induced and 114 repressed in the FA-treated group compared to the untreated control group. Impaired protein synthesis accompanied by increased protein and amino acid degradation suggest an imbalance in proteostasis. Signs of oxidative stress included significant dysregulation of candidate proteins of mitochondrial cellular respiration, increased endocytosis, and induction of heat shock proteins. Furthermore, an increased concentration of several candidate proteins associated with detoxification was observed. These results suggest dysregulated cellular respiration triggered by FA treatment as well as an increase in cellular defense mechanisms, including induced heat shock proteins and detoxification enzymes.
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Annual losses of honey bee colonies are high in the United States, with losses often attributed to the effects of the ectoparasitic mite, Varroa destructor, and its associated viruses (e.g., Deformed Wing Virus, DWV). In the spring, beekeepers rely on package bees to replace lost colonies. However, these packages often come with high levels of mites and are treated with miticides upon installation. Oxalic acid (OA) is a popular miticide used in spring, but little is known about its long-term efficacy for mite control. On the other hand, natural behavior that helps with mite control is swarming, which results in a break in the production of brood in a colony. In this study, we investigated the effect of spring OA sublimation and summer swarming on colony health and productivity. We found that OA sublimation is an effective method to increase mite drop from the colony in the first three days after treatment. However, mite populations recovered quickly leading to high mite levels in the fall for colonies that did not swarm during the summer. OA applications had a marginally significant negative effect on honey yield. Mid-season swarming was correlated with lower levels of Varroa mites suggesting that implementing a brood break in the middle of the summer could play an important role in reducing mite populations for colonies originating from packages. However, the combination of OA applications to packages in the spring and summer brood break had a significant effect on reducing mite levels for colonies entering the winter. We conclude that treating packages with OA in the spring in combination with summer mite treatments are powerful tools for beekeepers to keep colonies with lower pest loads entering the winter.
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In 1993 at Le Born near Toulouse, France 12 Apis mellifera intermissa queens from Tunisian colonies that had been naturally selected for tolerance to varroosis were tested against 12 unselected Apis mellifera carnica queens. We wished to determine if the tolerance of the intermissa queens was genetic in origin or simply due to specific local conditions in Tunisia. Queens were placed in 2 kg swarms of varroa infested bees and allowed to develop without any treatments. Nine colonies from each group over wintered. After exposure to heavy varroa infestations one carnica and seven intermissa queens were still surviving in August 1994. From 1995 to 2004 the surviving experimental colonies hybridized with the local population of bees. The majority of these hybrids were tolerant to Varroa destructor indicating a genetic control of the tolerance.
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The change in infestation levels of the mite Varroa destructorAnderson and Trueman on adult bees during periods with little or no brood rearing (late October/early November to early Febru- ary) was investigated in 10 colonies for two consecutive years in a Swedish climate (N57°06'E18°16'). The results do not support the hypothesis that mites become concentrated on the remaining bees as bees die off from the winter cluster. When the number of all mites recovered from dead bees or from debris was used to calculate mites per dead bee, the level of infestation per bee was not signif- icantly different between samples of live bee and dead bees. For modelling purposes, we presently find no reason to differentiate the mortality rates of bees and mites during periods when there is no or limited amounts of brood in the colonies, although the connection between bee mortality and mite mortality may not be as direct as previously assumed.
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In this paper, we review the main thresholds that can infl uence the population dynamics of host–parasite relationships. We start by considering the thresholds that have infl u-enced the conceptualisation of theoretical epidemiology. The most common threshold involving parasites is the host population invasion threshold, but persistence and infec-tion thresholds are also important. We recap how the existence of the invasion thresh-old is linked to the nature of the transmission term in theoretical studies. We examine some of the main thresholds that can affect host population dynamics including the Allee effect and then relate these to parasite thresholds, as a way to assess the dynamic consequences of the interplay between host and parasite thresholds on the fi nal out-come of the system. We propose that overlooking the existence of parasite and host thresholds can have important detrimental consequences in major domains of applied ecology, including in epidemiology, conservation biology and biological control.
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Field techniques for sampling and measuring the standing crop and secretion rate of nectar are described, in order to clarify some discrepancies and omissions in existing reviews of nectar measuring techniques. Slender microcapillary tubes (a fresh one for each sample) are recommended for withdrawing nectar, and a hand held sucrose refractometer, capable of operating with very small fluid volumes, is used for measuring concentration. Potential errors due to the presence of solutes other than sucrose, or to temperatures other than the calibration temperature, are discussed. I consider how measurements of secretion rate are affected by reabsorption and by the nature of the bags used to exclude nectarivores.
Twenty colonies of Italian bees, infested with Varroa jacobsoni were introduced to the Island of Fernando de Noronha, located near the equator off the coast of Brazil, in 1984. These colonies initiated a population that is isolated and protected from genetic contamination by 345 km of ocean. During the 13 years since that time, the colony numbers have increased to about 50 colonies in hives, and an undetermined number of wild colonies on the 26 square kilometers of this archipelago. This group of colonies is unique, as it is maintained without any type of treatment, and yet there is no evidence of significant damage or colony mortality due to the varroa infestations. The mean infestation rates of the adult bees in the colonies, found to be about 26 mites per hundred bees in 1991, decreased to 19 in 1993, and 14 in 1996.
The removal and grooming behaviour of Apis mellifera intermissa against Varroa jacobsoni was investigated in Tunisia. Workers in 15 test colonies detected and removed up to 75% of artificially infested brood and removed up to 97%-99% of freeze-killed brood in each of two trials. Likewise, A. m. intermissa actively groomed off V. jacobsoni, as shown by a great number of injured mites dropping from naturally infested colonies. Both grooming and removal activities of A. m. intermissa provide evidence for active mechanisms of resistance against V. jacobsoni.
A behavioral and physiological resistance mechanism of the Asian honey bee (Apis cerana) to an ectoparasitic mite, Varroa jacobsoni, which causes severe damage to the European honey bee (Apis mellifera) in the beekeeping industry worldwide, is reported here for the first time. Parasitism by the mite induced Asian worker bees to perform a series of cleaning behaviors that effectively removed the mites from the bodies of the adult host bees. The mites were subsequently killed and removed from the bee hives in a few seconds to a few minutes. The grooming behavior consists of self-cleaning, grooming dance, nestmate cleaning, and group cleaning. Worker bees can also rapidly and effectively remove the mites from the brood. The European bee showed cleaning behavior at low frequency and generally failed to remove the mites from both the adult bees and the brood.