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

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 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.

Full text

Apidologie 37 (2006) 1
c
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
1. INTRODUCTION
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 effective 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,
ingemar.fries@entom.slu.se
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 difficult to
verify, a documented case of European honey
bees surviving mite infestation without treat-
ment is found on an island 345 km offthe
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.
2. MATERIALS AND METHODS
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 (N58◦01’–N58◦04’,
E18◦09’–E18◦15’, 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 insufficient 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 different letters above are significantly
different 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. RESULTS
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 differ-
ent letters above are significantly different between
years (P<0.05, chi-square).
mortality rates during the two last years of
the experiment were not significantly differ-
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 different letters above are signifi-
cantly different between years (P<0.05, Kruskall-
Wallis).
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 coefficients 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 coefficient 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 coefficients 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 coefficient 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.
4. DISCUSSION
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-
gated.
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 effect 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 sufficiently 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 different 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 difficult 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 efforts.
Further experiments must confirm whether se-
lection experiments as described here can be
used as a basis for further honey bee breeding
programs.
ACKNOWLEDGEMENTS
The dedicated efforts 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
suffisamment 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
REFERENCES
Boecking O., Ritter W. (1993) Grooming and removal
behaviour of Apis mellifera intermissa in Tunesia
against Varroa jacobsoni, J. Apic. Res. 32, 127–
134.
Deredec A., Courchamp F. (2003) Extinction thresh-
olds in host-parasite dynamics, Ann. Zool. Fenn.
40, 115–130.
de Jong D., Soares A.E.E. (1997) An isolated pop-
ulation of Italian bees that has survived Va rr oa
jacobsoni infestation without treatment for over
12 years, Am. Bee J. 137, 742–745.
Fries I., Camazine S. (2001) Implications of horizontal
and vertical pathogen transmission for honey bee
epidemiology, Apidologie 32, 199–214.
Fries I., Perez-Escala S. (2001) Mortality of var-
roa mites (Varroa destructor) in honey bee (Apis
mellifera) colonies during winter, Apidologie 32,
223–229.
Fries I., Camazine S., Sneyd J. (1994) Population dy-
namics of Varroa jacobsoni: a model and a review,
Bee World 75, 5–28.
Fries I., Wei H., Shi W., Chen S.J. (1996) Grooming
behavior and damaged mites (Varroa jacobsoni)in
Apis cerana cerana and Apis mellifera ligustica,
Apidologie 27, 3–11.
Fries I., Hansen H., Imdorf A., Rosenkranz P. (2003)
Swarming in honey bees (Apis mellifera)and
Varr oa mite (Varroa destructor) population devel-
opment in Sweden, Apidologie 34, 1–9.
Imdorf A., Bühlmann G., Gerig L., Kilchenmann V.,
Wille H. (1987) Überprüfung der Schätzmethode
zur Ermittlung der Brutfläche und der Anzahl
Arbeiterinnen in freifliegenden Bienenvölkern,
Apidologie 18, 137–146.
Kefuss J., Vanpoucke J., Ducos de Lahitte J., Ritter W.
(2004) Varr oa tolerance in France of intermissa
bees from Tunesia and their naturally mated de-
scendants: 1993–2004, Am. Bee J. 144, 563–568.
Korpela S., Aarhus A., Fries I., Hansen H. (1993)
Varroa jacobsoni Oud. in cold climates: popula-
tion growth, winter mortality and influence on sur-
vival of honey bee colonies, J. Apic. Res. 31, 157–
164.
Le Conte Y. (2004) Honey bees surviving Varroa de-
structor infestations in France, in: Experts’ meet-
ing on apiculture Var ro a control, Brussels 24
October 2003, European Commission, Brussels,
pp. 82–84.
Peng Y.S., Fang Y., Xu S., Ge L. (1987) The resistance
mechanism of the Asian honey bee Apis cerana
Fabr. to an ectoparasitic mite, Varroa jacobsoni
Oudemans, J. Invertebr. Pathol. 49, 54–60.
Rath W., Drescher W. (1990) Response of Apis cer-
ana Fabr. towards brood infested with Va r r o a j a -
cobsoni Oud. and infestation rate of colonies in
Thailand, Apidologie 21, 311–321.
Rosenkranz P. (1999) Honey bee (Apis mellifera L.)
tolerance to Varroa jacobsoni Oud. in South
America. Apidologie 30, 159–172.
Seeley T. (2004) Forest bees and Va rr oa mites, Bee
Culture 132, 22–23.