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Apidologie 38 (2007) 19–29 19
c
INRA/DIB-AGIB/EDP Sciences, 2007
DOI: 10.1051/apido:2006055 Original article
Honey bees of the Arnot Forest: a population of feral
colonies persisting with Varroa destructor
in the northeastern United States*
Thomas D. S
Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853, USA
Received 21 January 2006 – Revised 23 April 2006 – Accepted 23 April 2006
Abstract – Feral colonies of European honey bees living in the Arnot Forest, a 1651-ha research preserve
in New York State, were studied over a three-year period, 2002 to 2005. This population of colonies was
previously censused in 1978. A census in 2002 revealed as many colonies as before, even though Varro a
destructor was introduced to North America in the intervening years. Most colonies located in fall 2002
were still alive in fall 2005. The Arnot Forest colonies proved to be infested with V. destructor,buttheir
mite populations did not surge to high levels in late summer. To see if Arnot Forest bees can suppress the
reproduction rate of mites, colonies of Arnot Forest bees and New World Carniolan bees were inoculated
with mites from an apiary and the growth patterns of their mite populations were compared. No difference
was found between the two colony types. Evidently, the stable bee-mite relationship in the Arnot Forest
reflects adaptations for parasite (mite) avirulence, not host (bee) resistance.
Apis mellifera /Varroa destructor /host-parasite relationship /tolerance /avirulence
1. INTRODUCTION
The mite Varroa destructor is a new para-
site of European honey bees living in North
America, having been introduced to these bees
only in the mid 1980s (Wenner and Bushing,
1996; Sanford, 2001). It is also a virulent par-
asite. As a rule, if a colony of European honey
bees does not receive mite control treatments,
the mite population will grow from just a few
mites to severalthousand mites in three to four
years, ultimately killing the colony (Ritter,
1988; Korpela, et al., 1992; Wenner and Thorp,
2002). It seems that there is little opportunity
for the evolution of a stable host-parasite re-
lationship in areas where the population of
colonies consists primarily of colonies man-
Corresponding author: T.D. Seeley,
tds5@cornell.edu
* Manuscript editor: M. Spivak
This article was published online on November 29th
2006 in a wrong version. The version published
here is the correct one.
aged by beekeepers. This is partly because
beekeepers control mite populations to avoid
loss of colonies, thereby preventing selection
for V. destructor-tolerant bees, and partly be-
cause beekeepers manage their bees in ways
(e.g. crowding colonies into apiaries, trans-
ferring combs of bees and brood between
colonies, and preventing swarming) that pro-
mote the horizontal transmission of the mites
between colonies. Virulence theory suggests
that horizontal transmission, defined as infec-
tious transfer among unrelated hosts, promotes
the evolution of virulent parasites by favoring
those that strongly (and thus harmfully) repro-
duce in current hosts before moving on to new
hosts (Ewald, 1983; Bull, 1994).
One might expect, however, the evolution
of a balanced host-parasite relationship in ar-
eas with little or no beekeeping, hence where
the population of colonies is mostly feral
(Mobus and de Bruyn, 1993). Here there will
be little or no control of the mites, allowing
selection for V. destructor-tolerant bees, and
Article published by EDP Sciences and available at http://www.edpsciences.org/apidoor http://dx.doi.org/10.1051/apido:2006055
20 T.D. Seeley
there will mainly vertical transmission of the
mites between colonies. Virulence theory sug-
gests that vertical transmission, in which para-
sites are passed from host parent to offspring,
promotes the evolution of avirulent parasites
because the reproduction of the parasites is
linked to that of their hosts. There are strong
indications that a balanced host-parasite rela-
tionship, in which both bees and mites survive,
has evolved in isolated populations living un-
der feral or feral-like conditions in several
locations (Tunisia: Ritter et al., 1990; Aus-
tria: Ruttner, 1991; Büchler, 1994; Brazil: de
Jong and Soares, 1997, United States: Wenner
and Thorp, 2002; Sweden: Fries et al., 2006).
There is also evidence that in these popula-
tions the bees have evolved resistance mech-
anisms (Boecking and Ritter, 1993) and/or
the mites have evolved reduced reproduction
(Milani et al., 1999). However, the extent to
which these stable host-parasite relationships
reflect adaptations for host resistance or para-
site avirulence, or both, remains uncertain.
This paper reports a three-year study (fall
2002 to fall 2005) of a feral population of
honey bee colonies living in the Arnot Forest, a
research preserve near Ithaca, New York State.
This population was previously censused in
1978, prior to the introduction of V. destructor
to North America (Visscher and Seeley, 1982).
The current study had four goals: (1) to deter-
mine whether feral colonies remain abundant
in the Arnot Forest; (2) to determine if the
colonies in this population are infested with
V. destructor; (3) to determine if the colonies
in this population are long-lived despite be-
ing infested with V. destructor;and(4)ifthey
are long-lived with V. destructor,thentode-
termine how they have achieved a stable host-
parasite relationship.
2. MATERIALS AND METHODS
2.1. Study site
The feral bee population of interest lives in the
Arnot Forest (42◦17’N, 76◦39’W, altitude 585 m),
a 1651-ha research preserve owned by Cornell
University, outside the town of Cayuta, Schuyler
County, New York State, USA. Most of this pre-
serve is forested, with forest types ranging from
young old-field successional forest to mature hard-
wood forest, with the latter predominant (see Fig. 1
in Odell et al., 1980). Most of the surrounding land
is also mature hardwood forest, as it consists largely
of protected forests owned by New York State (see
Fig. 1 in Visscher and Seeley, 1982). When the
study began in the fall of 2002, there were no known
hives of bees within 3 km of the boundary of the
Arnot Forest, but in the summer of 2004 one bee-
keeper established a small apiary with eight hives
along Cayuta Creek, 1 km from the forest’s south-
ern boundary.
2.2. Locating feral colonies in trees
During the fall of 2002, I located all the feral bee
colonies within the western two-thirds of the Arnot
Forest. Using a modification of beelining tech-
niques (Edgell, 1949; Visscher and Seeley, 1989), I
captured foraging bees, fed them scented 2.5-mol/L
sucrose syrup from a piece of old comb, and then re-
leased them to fly home. Usually some bees would
eventually return to the feeding station, recruiting
nestmates as well. Once bees were well oriented to
the feeding station, they would leave in a beeline
homeward, and I would record the vanishing bear-
ings for these bees; these bearings indicated the ap-
proximate direction of the bee’s nest in a tree (“bee
tree”). The distance to the nest could be estimated
from the minimum round-trip times of individually
marked bees.
To census the colonies, I systematically initiated
beelines from feeding stations (Fig. 2, 1–12) located
in open areas spaced throughout the western half of
the forest, generally <1 km apart. At a single feed-
ing station, I often initiated beelines from multiple
colonies. Once the beelines were established, for-
agers at the feeder were again trapped, and carried
along one of the beelines to another clearing. Here
the bees were released, and their vanishing bear-
ings again noted. By repeating such moves, the tree
that the colony inhabited could be located. The cen-
sus appears to have been exhaustive for the western
two-thirds of the Arnot Forest (time limitations pre-
vented censusing the entire forest). Bees from all
eight colonies (Fig. 2, A–H) were captured at 3.0 ±
0.4 locations in the forest, and this redundancy reas-
sured me that there were not colonies in the western
half of the forest whose members I did not capture.
All colonies were inspected for life each year
with inspections made around May 1, June 15, and
October 1. Bees flying around a nest entrance do
Feral bees persisting with Var roa 21
Figure 1. One of five bait hives installed in trees in the Arnot Forest to attract swarms and so provide feral
colonies living in movable-frame hives. Installation shown is typical: hive mounted some 4 m offthe ground
and with entrance opening reduced to 16 cm2and oriented to south.
not by themselves indicate a living colony within –
they could be robber bees or scout bees, plunder-
ing or inspecting the nest of a dead colony – so
I used the criterion of the presence of pollen for-
agers as my indicator of a live colony. The nests
of colonies that had died were kept in the inspec-
tion program to provide data on the occurrence of
nest reoccupation. The May 1 inspection preceded
the swarming season for the Ithaca area (Fell et al.,
1977), so all colonies alive at that time were as-
sumed to have survived the winter. The mid-June
inspection served to check for late spring mortality
among colonies that survived winter. The October 1
inspection provided data on nest reoccupation and
colony survivorship for the preceding summer. A
prior study of the demography of feral colonies in
central New York State (Seeley, 1978) found that
98% of colony mortality occurred during winter, so
it is highly likely that each bee tree colony that was
found alive in May and June and again in October
was alive all summer (i.e., did not die out and then
get reoccupied).
2.3. Establishing feral colonies in hives
and monitoring mite levels
To accurately measure the mite levels in feral
colonies in the Arnot Forest, I needed to have
feral colonies living in movable-frame hives. To ac-
quire such colonies, during the summer of 2003 I
mounted a hive in a tree in each of five locations
(near sites 1, 2, 5, 7, and 10 in Fig. 2) and waited
for swarms to occupy them. Each hive consisted
22 T.D. Seeley
Figure 2. Map of the Arnot Forest. Shown are the locations of the bee trees (8) and of the feeding stations
(12) used to establish beelines that led to the bee trees. Feeding stations are numbered in order of use. The
lines radiating from each feeding station depict vanishing bearings of bees leaving the station. Note that
most of these lines occur in clusters which point toward identified bee trees; the clusters that do not are
marked with question marks. Grey areas denote forested land and white areas denote cleared land.
Feral bees persisting with Var roa 23
of a single, deep Langstroth hive body filled with
eight frames of old worker comb and two frames
of old drone comb (placed in the #2 and #9 posi-
tions in the hive). Thus each hive contained a typical
amount of worker comb and drone comb and had
the drone comb positioned in its typical location, to-
ward the edge of the nest (Seeley and Morse, 1976).
I placed a Dadant Varroa Screen (Dadant and Sons,
Inc., Hamilton, Illinois, USA) between the bottom
board and hive body of each hive, so that I could
later place a sticky board for catching mites inside
each hive without disturbing the colony. As shown
in Figure 1, the entrance of each hive consisted of
an opening that was 2 cm high ×8 cm wide, faced
south, and was located 3.9–4.6 m offthe ground.
Hives configured in this manner match the nest-site
preferences of European honey bees (Seeley and
Morse, 1978) and are highly attractive to swarms
(Morse and Seeley, 1979). These bait hives were set
up in early May, 2003, hence before the start of the
swarm season.
Each hive was inspected at the start of each
month to see if it had been occupied by a swarm.
Once a hive was occupied, I began making monthly
readings of the mite population in the resident
colony by counting the mites caught on a sticky
board placed on the hive’s bottom board (Webster,
2001). At the start of each month, I inserted a sticky
board (Varroa Mite Trap, Phero Tech, Inc., Delta,
British Columbia, Canada) into each hive, left it
there for 48 hours, and then removed it and counted
the number of mites that had fallen onto and be-
come trapped on the sticky board. No acaricide was
applied.
2.4. Comparing Arnot Forest and New
World Carniolan bees for
V. destructor resistance
I wished to see if colonies of Arnot Forest bees
were resistant to V. destructor mites, i.e., were able
to inhibit the growth of their mite populations. To
do so, in the summer of 2005, I set up in the vicin-
ity of the Liddell Field Station of Cornell Univer-
sity in Ithaca, NY, six pairs of matched colonies
in which one colony was headed by an Arnot For-
est (AF) queen and one was headed by a New
World Carniolan (NWC) queen. I inoculated each
colony with the same number of mites from the
same source, and then made a monthly reading of
the mite population in each colony. I reasoned that
if bees in AF colonies can inhibit the growth of mite
populations, then the colony mite counts of the AF
bees should be lower than those of the NWC bees.
The six AF queens were produced from one of
the Arnot Forest colonies that had moved into a bait
hive in 2003 (colony 2 in Tab. I). This colony was
removed from the forest in mid-October 2004, in
preparation for rearing queens from it in the sum-
mer of 2005. The colony swarmed in mid June
2005, just before larvae were to be grafted from
it for queen rearing. Fortunately, it contained nu-
merous queen cells, so I was able to divide it
to create six small colonies, each containing at
least two capped queen cells. These “mating nucs”
were moved back to the Arnot Forest, so that each
colony’s virgin queen would be apt to mate with
drones from feral colonies there. By the end of
June, all six colonies contained a mated and laying
AF queen. Meanwhile, I had obtained six naturally-
mated NWC queens that were sisters (Strachan Api-
aries, Yuba City, California, USA) and had installed
each one in a small colony, the same size as the mat-
ing nucs housing the AF queens, so that the NWC
queens would be laying at the start of the experi-
ment. All the queens were given paint marks to en-
sure that any supersedure queens could be identi-
fied.
On 1 July 2005, I established the six pairs of ex-
perimental colonies. Within each pair, both colonies
were created by taking one frame of bees and brood,
one frame of bees and food (pollen and honey), and
one frame of honey from one of the strong “stock”
colonies in the apiary at the Liddell Field Station
and placing these three frames in a hive with seven
more frames of empty, drawn comb. None of the ten
frames contained drone comb. Thus, both colonies
in each pair started out with approximately the same
number of bees from the same source and with ap-
proximately the same number of mites from the
same source. (Note: the bees and mites for each
pair of colonies came from a different stock colony;
these six different stock colonies were unrelated.)
The exact number of mites that each colony re-
ceived is unknown. Both colonies in each pair were
then moved together to one of six locations in the
vicinity of the Liddell Field Station; these locations
were some 50 km from the Arnot Forest and were
at least 5 km from each other. At each location, the
colonies were placed at least 10 m apart to mini-
mize drifting of bees and were given a caged queen,
either one of the AF queens or one of the NWC
queens. An inspection of the colonies on 5 July
revealed that the queen in each had been released
from her cage and had begun laying eggs.
24 T.D. Seeley
Two weeks later, on 15 July, I started a series
of monthly assays of the mite populations in each
hive, using the 48-hour mite drop method described
above. Each of the hives used in this experiment
was equipped with a Dadant Varroa Screen between
hive body and bottom board so that I could insert
and remove a sticky board without disturbing the
colony. These colonies received no treatments with
acaricides. Mite assays were made on 15–17 July,
12–14 August, 16–18 September, and 16–18 Octo-
ber. After each of these mite assays, each colony
was inspected for queen turnover; the final round
of inspections in mid-October 2005 revealed that
each colony still had its original AF or NWC queen.
Also, near the end of August, by which time virtu-
ally all the adult bees and certainly all the immature
bees in each hive were the offspring of the AF or
NWC queen, each colony was examined to deter-
mine the number of frames covered by adult bees
and the number of frames filled with brood.
3. RESULTS
3.1. Feral colonies still exist in the Arnot
Forest
Between 20 August and 30 September
2002, I bee hunted in the Arnot Forest for
117 hours spread over 27 days, during which
time I started beelines from 12 feeding sta-
tions in clearings spread over about two-thirds
of the forest (Fig. 2). This work revealed eight
colonies living in trees. It should be noted that
only four of the 29 beelines pointed out of the
Arnot Forest: just those pointing west into the
adjacent Cliffside State Forest, from feeding
stations 3, 5, and 9. This indicates that few, if
any, managedcolonies in hives were living just
outside the boundary of the Arnot Forest.
3.2. The Arnot Forest colonies are
infested with V. destructor
Three of the five bait hives set up in the
Arnot Forest were occupied in the summer of
2003, sometime between 30 June and 31 July.
It is likely that the swarms occupying these
bait hives came from feral colonies living in
trees because each of the three occupied bait
hives (located near sites 2, 5, and 7 in Fig. 2)
Table I. Monthly assays of mite populations in feral
colonies living in hives in the Arnot Forest. Each
assay is the number of mites that dropped onto a
sticky board over a 48-h period at the start of the
month indicated.
Date Colony 1 Colony 2 Colony 3
August 2003 30 14 21
September 2003 16 21 39
October 2003 36 3 22
May 2004 2 2 1
June 2004 3 11 2
July 2004 2 10 4
August 2004 3 5 7
September 2004 16 15 13
October 2004 42 40 22
was surrounded by forest for more than 2 km,
and prior work has shown that most (86%)
swarms travel less than 2 km to reach a new
home site (see Fig. 1 in Seeley and Morse,
1977).
Following the bait hive occupations in the
summer of 2003, and throughout the sum-
mer of 2004, I took monthly readings of the
mite population in each colony by counting
the mites that fell onto a sticky board over
48 h. All three colonies were infested with
V. destructor mites, evidently from the times
they moved into the hives (Tab. I). We also
see that the population of mites in each colony
was rather stable during the summer of 2003,
dropped markedly over the winter of 2003–
2004, and increased only slowly and gradually
over the summer of 2004.
There are no data for 2005 because one of
the colonies (colony 2) was removed from the
forest in mid-October 2004 to provide larvae
for future queen rearing, and the other two
colonies were destroyed by black bears (Ursus
americanus) sometime between the last check
of the colonies in 2004 (in mid-October) and
the first check in 2005 (in mid-April).
All three feral colonies in hives were in-
spected internally toward the end of the sum-
mer in 2003 (on 4 September) and again in
2004 (on 29 August). Both years, the inspec-
tions revealed that all three colonies were
strong and healthy with adult bees cover-
ing all ten frames, brood in three to six
Feral bees persisting with Var roa 25
Table II. Fates of the feral colonies living in trees in the Arnot Forest. Each bee tree was inspected at least
three times a year, around 1 May, 15 June, and 1 October.
Date Colonies alive Notes
Oct 2002 8 8 colonies found by bee lining
May 2003 6 2 colonies died over winter
June 2003 6 0 colonies died in late spring
Oct 2003 6 2 empty bee trees were not reoccupied
May 2004 5 1 colony died over winter (tree toppled)
June 2004 5 0 colonies died in late spring
Oct 2004 6 1 empty bee tree reoccupied
May 2005 6 0 colonies died over winter
June 2005 6 0 colonies died in late spring
Oct 2005 7 1 empty bee tree reoccupied
frames (including frames with drone comb),
and honey filling several frames.
3.3. The Arnot Forest colonies are
persisting with V. destructor
Table II summarizes the information about
the fates of the feral colonies living in trees
over the three-year period of fall 2002 to fall
2005. We see that five of the eight colonies
found in the fall of 2002 were still alive in the
fall of 2005. Regarding the three colonies that
died during the three-year period, two perished
in the winter of 2002–2003 (cause of deaths
is unknown) and one perished in the winter
of 2003–2004 (a gale in early October 2003
toppled the tree housing the colony). The two
intact but empty bee trees were eventually re-
occupied by swarms, one in 2004 and one in
2005. Thus this population of feral colonies
remained essentially stable over three years,
with a net loss of just one colony due to the
natural destruction of a nesting site.
3.4. The Arnot Forest bees are not
inhibiting V. destructor population
growth
There are no signs that colonies of Arnot
Forest bees, relative to those of New World
Carniolan bees, are better at limiting the pop-
ulationgrowthofV. destructor mites. As is
shown in Figure 3, the monthly mite-drop
counts indicate that both colonies in each
Figure 3. Results of the monthly assays of the mite
populations in six pairs (A–F) of colonies, with
each pair containing one Arnot Forest colony and
one New World Carniolan colony. Changes in the
mite population of each colony were monitored by
counting the mites that dropped onto a sticky board
over 48 h. Sampling dates: mid-month in July (J),
August (A), September (S), and October (O).
pair were initially infested with similar lev-
els of mites and that their mite populations in-
creased markedly over the summer (except in
the NWC colony in pair B). Furthermore, we
26 T.D. Seeley
Table III. Strength comparisons of the colonies
headed by Arnot Forest (AF) or New World
Carniolan (NWC) queens. Measurements were
made on 26 August 2005. P-values are based on
paired-comparison ttests of significance of the dif-
ferences between treatment means.
Frames of adult bees Frames of brood
Colony pair AF NWC AF NWC
A 7753.5
B 5443.5
C 7654.5
D 5.5 3.5 4.5 3
E 5745
F 6644
Mean 5.92 5.58 4.42 3.92
SD 0.92 1.50 0.49 0.74
P>0.58 >0.26
see that each month the mite-drop counts were
similar for the two types of colonies. Paired-
comparison ttests of significance of the dif-
ference between the mean mite-drop counts
for AF and NWC colonies confirmed a lack
of difference in each month: July: t5=1.37,
P>0.23; August: t5=0.62, P>0.57;
September: t5=0.58, P>0.59; October:
t5=0.92, P>0.41). As is shown in Table
III, measurements taken at the end of August,
by which time virtually all the bees in each ex-
perimental colony were the offspring of its AF
or NWC queen, indicate that both colonies in
all six pairs were queenright. These measure-
ments also reveal that all the colonies, though
still quite small, having been established with
just two frames of bees on 1 July, were well
stocked with bees and brood. The two types
of colonies were similar in strength (frames of
bees, Student’s ttest: t5=0.60, P>0.58;
frames of brood, Student’s ttest: t5=1.29,
P>0.26).
4. DISCUSSION
It is generally believed, probably correctly,
that the introduction of Varroa destructor in
the mid-1980s has all but wiped out the
feral populations of European honey bees in
North America (Sanford, 2001; Wenner and
Bushing, 1996). Nevertheless, it is now clear
that a feral population of these bees, infested
with V. destructor, persists in the Arnot For-
est in New York State. Indeed, there as many,
if not more, feral colonies living in this for-
est now as when they were censused 24 years
earlier in 1978, hence long before the arrival
of V. destructor (Visscher and Seeley, 1982).
In the previous survey covering the entire
Arnot Forest, nine feral colonies were found,
whereas in the present survey covering only
the western two-thirds of the forest, eight feral
colonies were found. It should be noted that
both the 1978 and the 2002 census were made
by the same person (the author) in the same
season (mid-August to late September) and in
the same way (by bee lining), so it is meaning-
ful to compare their results.
The population of European honey bees
surviving in the Arnot Forest is probably not
unique. Anecdotal reports suggest that feral
populations of European honey bees also exist
in other areas of North America where there
are few colonies kept by beekeepers (Wenner
and Thorp, 2002). Certainly the cases of Eu-
ropean honey bees surviving mite infestations
without acaricide treatments on isolated is-
lands in Brazil (De Jong and Soares, 1997) and
Sweden (Fries et al. in press) shows that Euro-
pean honey bees have the potential to develop
a stable host-parasite relationship with V. d e -
structor.
What is particularly intriguing about the
colonies living in the Arnot Forest is that many
of them (five out of the original eight colonies
living in trees) have survived for more than
three years even though V. destructor proba-
bly infests every colony living in this forest
(all three swarms that occupied the bait hives
came infested with the mites). The long-term
survival of these colonies begs the question:
how are they surviving with V. destructor?
There are several possible answers. One
is that these bees have evolved mechanisms
of resistance to the mites, such as groom-
ing of phoretic mites offadult bees, hygienic
behavior that removes worker brood infested
with mites, or inhibition of mite reproduc-
tion on worker brood (reviewed by Boecking
and Spivak, 1999; Rosenkranz, 1999). The
hypothesis that bees have evolved resistance
mechanisms was tested by setting up pairs
of colonies headed by Arnot Forest (AF) and
Feral bees persisting with Var roa 27
New World Carniolan (NWC) queens, seed-
ing both colonies in each pair with mites from
the same source colony, and comparing the
growth patterns of the mite populations in the
paired colonies. If the AF bees have evolved
resistance, then the AF colonies in this ex-
periment should have had slower mite pop-
ulation growth than the NWC colonies. This
prediction was not supported. The mite popu-
lations grew as briskly in the AF colonies as
in the NWC colonies. (Note: the mite drop
counts shown in Fig. 3 are low not because
the mites were reproducing slowly in the AF
and NWC colonies, but because these colonies
were small, each with only about 6 frames
of bees; see Tab. III.) It looks, therefore,
rather doubtful that the Arnot Forest bees have
evolved mechanisms of resistance to V. d e -
structor mites.
A second possible explanation for the long-
term survival of the V. destructor infested
but untreated Arnot Forest colonies is that
the mites have evolved avirulence, that is, re-
duced reproduction. Avirulence is predicted
to evolve in parasites which undergo verti-
cal (parent to offspring) rather than horizon-
tal (infectious spread) transmission (Ewald,
1983; Bull, 1994). This is because the vertical
transmission of parasites favors ones that leave
the host healthy enough to produce offspring.
Vertical transmission of V. destructor mites
will occur when an infested honey bee colony
swarms and so creates an offspring colony also
infested with the mites. Horizontal transmis-
sion, however, will occur when infested work-
ers drift into uninfested colonies or when un-
infested workers rob a weak colony containing
mites and then bring them home. In the Arnot
Forest, where the colonies are living in forest
trees separated by hundreds, if not thousands,
of meters (see Fig. 2), drifting of bees between
colonies is most unlikely and robbing may also
be exceedingly rare. If so, then we can ex-
pect avirulence to have evolved in the V. d e -
structor mites in the Arnot Forest, especially if
the bees/mites living there are largely isolated
from bees/mites in colonies being managed
by beekeepers, which is probably the case. At
present, however, there is no direct evidence
of reduced reproduction by the V. destructor
mites in the Arnot Forest, though this hypoth-
esis is indirectly supported by the curious ab-
sence of explosive growth in the mite popula-
tions in the Arnot Forest colonies in late sum-
mer (see Tab. I).
Still a third possible cause of the longevity
of the Arnot Forest colonies could be related
to frequent swarming, which is typical of feral
colonies in this locality (Seeley, 1978). When
a colony swarms, approximately half the adult
bees leave and along with them go a sub-
stantial portion of the adult mites, probably
15–20%, given the distribution of adult mites
between adult worker bees and sealed brood
cells (Fuchs, 1985; Martin et al., 1998). More-
over, after a colony swarms, there will be no
brood produced in the colony for two to three
weeks, during which time there will be no
mite reproduction. Nevertheless, when Fries et
al. (2003) compared the mite populations of
swarming and non-swarmingcolonies in Swe-
den, they found that swarming did not prevent
mite populations from growing to detrimental
levels. All 150 of the colonies in the Swedish
study were given a small number (36–89) of
mites in July 1999, and within three years 129
of the colonies were dead, mostly due to the
mites, regardlessof whether they did or did not
swarm in the summers of 2000 and 2001. It
seems unlikely, therefore, that swarming alone
could explain why many of the Arnot Forest
colonies have survived for 3+years without
treatments to control V. destructor.
The logical next step in the study of the
honey bees of the Arnot Forest is to test rigor-
ously the hypothesis that the basis for this sta-
ble host-parasite relationship is the evolution
of avirulence in the mites. There is evidence
that mite avirulence evolved in an isolated, ex-
perimental population of European honey bees
in Austria (Büchler, 1994; Milani et al., 1999),
and it will be interesting to see if the same has
happened in the northeastern United States. If
so, then this will reinforce the idea that Euro-
pean honey bees and V. destructor mites can
evolve a host-parasite relationship that is sta-
ble.
ACKNOWLEDGEMENTS
This research was supported by the U.S. Depart-
ment of Agriculture (Hatch grant NYC-191407).
28 T.D. Seeley
I am grateful to Dr. Peter Smallidge, Director of
the Arnot Forest, for his interest and support of this
study, and to Dr. Heather Mattila for giving helpful
suggestions for improving this paper.
Les abeilles de la forêt d’Arnot : une population
de colonies sauvages dans le nord-est des États-
Unis qui se maintiennent avec Varroa destructor.
Apis mellifera /Varroa destructor /relation hôte-
parasite /tolérance /avirulence
Zusammenfassung –Honigbienen im Arnot Fo-
rest: eine Population von mit Varroa destruc-
tor fortdauernden wilden Bienenvölkern in den
nordöstlichen USA. Über den Zeitraum von drei
Jahren (Herbst 2002 – Frühjahr 2005) wurde eine
wildlebende Population von europäischen Honig-
bienen im Arnot Forest, einem 1.651 ha großen For-
schungsreservat im Staat New York, untersucht. Die
Untersuchung verfolgte 4 Ziele: (1) festzustellen,
ob wildlebende Honigbienenvölker im Arnot Forest
häufig vorkommen, (2) festzustellen, ob die Bienen-
völker dieser Population mit V. destructor befallen
sind, (3) festzustellen, ob die Völker dieser Popula-
tion trotz eines Befalls mit V. destructor langfristig
überleben und (4) festzustellen, wie diese Bienen-
völker ein stabiles Parasit-Wirt-Verhältnis erreicht
haben.
Die Anzahl der wildlebenden Bienenvölker war im
Jahr 2002 ähnlich hoch wie bei einer Zählung im
Jahr 1978, lange bevor V. destructor eingeschleppt
wurde (Visscher and Seeley, 1982). Die Untersu-
chung wurde im westlichen Teil des Gebietes von
derselben Person, während derselben Jahreszeit und
mit denselben Methoden wie 1972 durchgeführt.
Acht Bienenvölker wurden in Bienenbäumen ent-
deckt (Abb. 2). Diese acht Völker wurden von Ok-
tober 2002 bis Oktober 2005 regelmäßig inspiziert.
Die meisten Völker (fünf von acht) waren nach die-
sen drei Jahren noch am Leben (Tab. II).
Die wildlebenden Völker im Arnot Forest waren
mit V. destructor befallen. Fünf Schwarmkisten
(Abb. 1) wurden im Sommer 2003 aufgestellt, um
den Milbenbefall in wildlebenden Völkern zu er-
mitteln. In drei dieser Kästen nisteten sich Schwär-
me ein. Bei diesen Völkern wurden über zwei Som-
mer die Milbenpopulationen monatlich anhand der
Anzahl abgefallener Milben in den Bodeneinlagen
(„sticky boards“) überprüft. Alle drei Völker waren
mit Milben befallen, blieben aber bei schwachem
bis mittlerem Milbenbefall vital.
Um zu überprüfen, ob die Bienenvölker des Ar-
not Forest den Anstieg ihrer Milbenpopulation kon-
trollieren können, wurden zwei vergleichbare Grup-
pen von Bienenvölkern paarweise aufgestellt. Je-
des Paar bestand aus einem Volk mit einer Kö-
nigin aus der Arnot Forest-Population und einem
Volk mit einer Carnica-Königin. Beide Völker wur-
den jeweils mit einer ähnlichen Anzahl an Var-
roamilben infiziert, die aus demselben Bienenvolk
stammten. Die Milbenpopulation wurde in der Fol-
ge monatlich durch Auszählen des Milbenfalls in
die Bodeneinlagen bestimmt. In allen Monaten wa-
ren die durchschnittlichen Milbenzahlen in den bei-
den Gruppen von Bienenvölkern gleich (Abb. 3).
Das heißt, die Milbenpopulation wuchs in den Ar-
not Forest-Völkern genauso rasch an wie in den
Carnica-Völkern.
Für das Überleben der Bienenvölker im Arnot Fo-
rest scheint demnach eher die Evolution einer gerin-
geren Virulenz bei den V. destructor-Milben (gerin-
gere Reproduktion) als die Entwicklung einer Re-
sistenz bei den Bienen (Mechanismen der Milben-
abwehr) verantwortlich zu sein. Allgemein sollte
bei Parasiten eine Evolution in Richtung geringe-
rer Virulenz dann von Vorteil sein, wenn sie sich
eher vertikal (Eltern zu Nachkommen) als horizon-
tal (infektiöse Verbreitung innerhalb der Populati-
on) ausbreiten. Im Arnot Forest, in dem die Bienen-
völker in Bäumen leben, die mehrere hundert Meter
voneinander entfernt stehen, dürfte die Verbreitung
von V. destructor eher vertikal (durch Schwärme)
als horizontal (Verflug und Räuberei) erfolgen. Ei-
ne weitere Untersuchung der Bienenvölker im Ar-
not Forest wird die Hypothese testen, dass die of-
fensichtlich stabile Beziehung dieser Bienen mit V.
destructor die Folge der Evolution einer geringeren
Virulenz der Milben ist.
Apis mellifera /Varroa destructor /Parasit-Wirt
Verhältnis /Toleranz /Avi r u l enz
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