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Average number of reproductive cycles performed by Varroa jacobsoni in honey bee (Apis mellifera) colonies

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Abstract

Due to the low fecundity of Varroa jacobsoni, it: is presently not possible to explain satisfactorily the observed rapid build up of mite populations in Apis mellifera colonies. The number of reproductive cycles, i.e. the number of times a mite enters brood cells to reproduce, has been suggested to be the key to this problem. Despite several studies on this aspect, large discrepancies in the published data remain. This paper describes a new experimental method for studying this aspect of the mites' biology in order to resolve this question. Colonies containing only worker bee brood were manipulated so they had discrete brood cycles. Colonies were kept in a mite-free area and infested with a known number of mites at the start of the study. To estimate the average number of reproductive cycles performed, the observed growth in the mite populations was compared with the theoretical growth of mite populations which performed different numbers of reproductive cycles, but with conditions otherwise similar to those observed in the study colonies. The level of mite drop was used as an indicator of the mite population. The average potential number of reproductive cycles required to explain the observed mite population growth was between two and three.
Journal of Apicultural Research 36(3/4): 113–123 (1997) ©1997 IBRA
SUMMARY
Due to the low fecundity of Varroa jacobsoni, it
is presently not possible to explain satisfactorily
the observed rapid build up of mite populations
in Apis mellifera colonies. The number of repro-
ductive cycles, i.e. the number of times a mite
enters brood cells to reproduce, has been sug-
gested to be the key to this problem. Despite
several studies on this aspect, large discrepan-
cies in the published data remain. This paper
describes a new experimental method for
studying this aspect of the mites’ biology in
order to resolve this question. Colonies con-
taining only worker bee brood were manipulat-
ed so they had discrete brood cycles. Colonies
were kept in a mite-free area and infested with
a known number of mites at the start of the
study. To estimate the average number of
reproductive cycles performed, the observed
growth in the mite populations was compared
with the theoretical growth of mite populations
which performed different numbers of repro-
ductive cycles, but with conditions otherwise
similar to those observed in the study colonies.
The level of mite drop was used as an indicator
of the mite population. The average potential
number of reproductive cycles required to
explain the observed mite population growth
was between two and three.
Keywords: Varroa jacobsoni, honey bees, Apis
mellifera, reproductive cycles, mite drop, mite
populations
Average number
of reproductive
cycles performed
by Varroa
jacobsoni in
honey bee (Apis
mellifera)
colonies
S J MARTIN; D KEMP
National Bee Unit, Central Science Laboratory,
Sand Hutton, York, YO4 1LZ, UK
(Received 27 May 1997,
accepted subject to revision 16 September 1997,
accepted for publication 17 October 1997)
MATERIALS AND METHODS
The study was carried out in 1995 using six study
colonies and repeated in 1996 using 15 study colonies.
All the A. mellifera colonies used in this study were
chemically untreated, varroa free and kept in 11-frame
Standard Smith hives fitted with removable bottom
(varroa) floors. All debris samples were carefully
inspected for fallen mites before passing the samples
through sieves using boiling water to ensure that they
all had been collected. In the study colonies all drone
cells were destroyed immediately prior to, and
throughout, the study. The entrance was placed above
the queen excluder in the study colonies to prevent
adult drones entering the brood nest. Numbers of
adult bees and sealed brood were estimated by the
comb coverage method (Jeffree, 1951) and validated by
taking digital photographs of selected combs.
Study colonies
The study colonies were of a similar size with respect
to adult worker bee and sealed brood populations (fig.
1) prior to being placed on the study site on 25 May
1995 or 17 May 1996. The site consisted of a series of
small clearings in a young (2–3 m high) pine tree plan-
tation. One study hive was placed in each clearing. No
mites had been reported within a 50 km radius of the
site in 1995. By the end of the study (October 1996)
very low numbers (1–2 mites per hive) were being
reported in nearby apiaries. The hive debris, number
of adult bees and sealed brood were monitored regu-
larly throughout the study.
The level of mite drop was used as an indicator of the
mite population. Any colonies in which mite drop,
recorded during each brood emergence period, failed
to increase in the subsequent brood emergence period
or reached an unusually high level during the no-brood
emergence period, were excluded from the study.
These observations indicated that either few mites had
entered cells or unusual amounts of sealed brood were
being killed by chalkbrood, both of which invalidate the
use of the matrix model to estimate the average num-
ber of reproductive cycles. Equivalent colonies, e.g. per-
centage of mites invading cells, must be used in com-
parisons with the matrix model otherwise the number
of reproductive cycles will appear to be depressed.
Support colonies
Eight (1995) and 16 (1996) additional uninfested
colonies provided open (uncapped) brood used to sup-
plement the study colonies. Five (1995) and 11 (1996)
Number of reproductive cycles by varroa in honey bee colonies 115
INTRODUCTION
The parasitic honey bee mite, Varroa jacobsoni, only
reproduces within the sealed brood phase of honey
bee development. Therefore, V. jacobsoni reproduction
occurs in discrete reproductive cycles which start just
after the host cell is sealed and ends when the bee
emerges 12 days (workers) or 15 days (drones) later.
Detailed studies (Martin, 1994; Boot et al., 1995; Donzé
et al., 1996) have found that in worker cells an average
of 1.0–1.1adult female offspring are produced by each
mite during a reproductive cycle. Limited field data have
suggested that mites undergo very few reproductive
cycles (table 1) and so current models of mite popula-
tion growth (Fries et al., 1994) rely very heavily on the
mites reproducing in drone cells (Martin, 1995a); at
least twice as many adult female offspring can be pro-
duced in drone cells than in worker cells (Martin,
1995b). However, laboratory studies involving the arti-
ficial transfer of mites between cells (Tzortzi, 1982; Rui-
jter, 1987) have shown that up to eight reproductive
cycles can be achieved by a single mite during which
time up to 30 eggs were laid.
Varroa mites can live for 2.5–3.5 months during the
summer (Ruijter, 1987; Calatayud & Verdú, 1994:
Boecking, personal communication) and are capable of
laying 18–30 eggs (Akimov & Yastrebtsov, 1984; Alberti
& Hanel, 1986; Ruijter, 1987) under natural conditions.
Field studies have shown that mite populations proba-
bly can increase 100-fold during one summer (Liebig et
al., 1984; Fries et al., 1991), may double their number
every 20 days (Klepsch, personal communication; Fries
et al., 1994) and, where continuous breeding is possible,
a conservative yearly 300-fold increase was reported
(Kraus & Page, 1995). These observations suggest that
the average number of reproductive cycles should be
significantly larger than has been reported in most of
the earlier studies (table 1). This view is supported by
recent studies where a high percentage of mites which,
if artificially transferred, lay eggs for at least a second
time (78%, Ifantidis, 1982; 77%, Martin & Cook, 1996;
70%, Creasey, personal communication) or even a third
time (51%, Ifantidis, 1982; 40%, Wendel & Rosenkranz,
1990; 26%, Creasey, personal communication). Rath
(1991) also suggested the mites utilize drone brood for
two to three reproductive cycles in its natural host A.
cerana.
It is important to resolve these differences between the
field and laboratory data, since small changes in the
number of reproductive cycles greatly influence the
growth of the mite population (Fries et al., 1994) and
subsequently the accuracy of any predictive varroa pop-
ulation models.
The primary aim of this study was to estimate, using a
new technique, the average potential number of repro-
ductive cycles a population of mites must perform to
account for their observed growth in drone-free honey
bee colonies, under field non-limiting (plentiful healthy
brood) conditions.
114 Martin; Kemp
FIG. 1. Estimated mean number of sealed brood and bees in the study colonies. Error bars
indicate ± 1standard deviation.
TABLE 11. Number of times a mite invades and/or reproduces within a cell. All studies except
Ruijter (11987) were carried out in the field.
% of mites reproducing in Initial % lost Mean no. of Author
or (entering) cells for the nth time. sample reproductive cycles
112 3 4 5 6 7 size or (cell entries)
? ? 4.10.88 Wendel and
Rosenkranz, 1990
(92) (8) 155 92 (1.08) Schulz, 1984
78.9 5.8 4.8 1.9 ? ? 1.22 Mikityuk, 1979
78 18 4 ? ? 1.26 Grobov, 1977
(30.3) (21.5) (13.8) 475 47 (1.75) Fries and
Rosenkranz,
1996*
64 29 7 15174 1.43 Ducker, pers.
(22) (49) (18) (11) (2.18) comm.*
39 4118 2 117 66 1.83 Creasey, pers.
(26) (37) (31) (4) (2) (2.19) comm.*
37 12 11 11 10 17 2 3.04 Ruijter, 1987*
number of times a mite could breed and allowed the
mites a maximum phoretic period of six days between
brood cycles.
On the same day that the queen was caged, frames of
open brood from the uninfested support colonies were
added to the study colonies to compensate for the eggs
destroyed during the queen isolation period and to
increase the amount of brood available for the mites to
invade. After a worker egg is laid it takes about eight
days before the cell containing the developing bee is
sealed. Therefore, the brood age laid by the queen in
the study colonies (1–8 days) matched the brood age
(1–8 days) of any open brood transferred from the sup-
port colonies; any older brood would already be sealed
and so inaccessible to the mites.
Study colony collection
Every 10 days after the queens were caged, three study
colonies were collected (1in 1995 and 2 in 1996) (fig.
2). At this time no open bee brood existed so all the
mites were either in the sealed brood or on the bees.
In the morning, all study colonies had the number of
sealed brood and bees estimated before releasing the
queens from the queen cages. The colony to be collect-
ed had all frames containing sealed brood cleared of
their adult bees and placed into a new hive which
contained two frames of honey (food source). Then
uninfested nurse bees (c. 5000) from a nearby support
colony were placed into the hive to thermoregulate the
sealed brood and the temperature was monitored by
probes placed between the frames and attached to a
Grant Squirrel datalogger. The top of each hive was fit-
ted with a mesh screen which was covered with a
board with a 4 ×1cm gap on one side for ventilation.
The now sealed colony containing the infested sealed
brood and uninfested bees was transported to the lab-
oratory where the natural mite drop was monitored
until all the sealed brood had emerged. The colony,
which now contained all the live mites which had invad-
ed cells and their mature offspring, was then killed by
carbon dioxide and freezing.
The study colonies from which sealed brood had been
removed were sealed after dark on the same day. All
the bees, and any mites which had not invaded cells,
were then killed by carbon dioxide and freezing.
Collection of mites
Once all the bees had been killed they were collected
from the hives and weighed. The total number of bees
was estimated by counting and weighing subsamples (c.
100–300) of bees. Groups of about 300 bees were
placed in a 1.7 mm mesh sieve and washed using a high
pressure jet of water. Any adult female mites present
were trapped in a lower 0.71mm mesh sieve. Each
sample was washed until two consecutive washes pro-
duced no further mites. Each comb was checked for
mites by careful visual inspection followed by sharp
knocks on to a hard white surface to dislodge any mites
adhering to the combs.
Number of viable female offspring
produced each reproductive cycle
Previous studies (Martin, 1994, 1995c) using similar
stocks of bees and mites kept under similar field con-
ditions (i.e. plentiful brood) and time of year (May–July)
as those in this study were used to determine the aver-
age number of adult female offspring produced by each
mite during one reproductive cycle. The values deter-
mined from those studies were 1.1(n= 1344 mother
mites) (Martin, 1994), 1.0 (n= 1596 mother mites) and
1.1(n= 2930 mother mites) (Martin, 1995c) which are
similar to the values determined by Boot et al., 1993
(1.0) and Donzé et al., 1996 (1.1). So, a value of 1.1
viable female offspring is used in this study, although this
may be an overestimate (see discussion).
RESULTS
Throughout the study the amount of sealed brood (c.
15 000) and adult bees (c. 32 500) in the study colonies
was maintained (fig. 1) at a fairly constant level, despite
the colony manipulations. The study colony size did not
differ significantly between 1995 and 1996. Caging the
queen did not adversely affect her egg-laying activities.
In 1995 a very warm and sunny summer ensured a
plentiful supply of nectar and pollen was available for
brood rearing. However, in 1996, six colonies had to
be excluded from the study. This was due to periods
of poor weather combined with the artificially high lev-
els of brood in the colonies, resulting in these colonies
initially suffering from a fungal infection known as chalk-
brood (Ascosphaera apis). This resulted in high mite
drops during periods when no brood was emerging
suggesting elevated levels of sealed brood removal by
the bees in these colonies. Brood removal normally
occurs at a level of 2.8% in similar colonies (Martin,
1994). In addition, the final three colonies (7 bee cycles)
failed to produce sufficient brood numbers in Septem-
ber due to lack of forage. This resulted in only 23–31%
of the mites invading cells and since this is well below
the normal 85% for that year, were excluded.
Data from the temperature probes indicated that the
bees introduced to the study sealed brood thermoreg-
ulated normally as soon as they were placed into the
hive, and continued to do so despite being confined in
the hive and transported to the laboratory.
Initial rejection rate of mites recovered
in hive debris
In 1995, during the first three days after introduction,
only 18 (3.6%) of the 498 introduced mites were found
in the debris of the six study colonies. Over the next
seven days a total of only six mites were found in the
debris. In 1996, during the first three days after intro-
duction, a total of 96 (7.5%) of the 1275 introduced
mites were found in the debris. However, over the next
Number of reproductive cycles by varroa in honey bee colonies 117
of these colonies were kept on the study site in a group
at least 4 m away from the nearest study colony. These
colonies were also used to supply uninfested adult bees
needed to thermoregulate the sealed brood removed
from the study colonies and monitor any local mite
dispersal from the study hives. The remainder of the
support colonies were kept at another varroa-free site.
Throughout the study all support colonies had the
floor debris monitored for the presence of mites. At
the end of the study 15 October 1995 or 12 October
1996 all support colonies were treated with Bayvarol
(flumethrin) strips to test for the presence or absence
of mites.
Mite introduction
During 1and 2 June 1995, around 700 phoretic mites
(females) of unknown age and reproductive history (i.e.
previous number of reproductive cycles performed)
were collected individually using a fine paint brush from
adult drones (mainly) and worker bees from a heavily
infested colony. The 300 mites collected on day 2 and
the survivors kept on drone larvae from day 1were
moved to the study site immediately and transferred to
the study colonies. A total of 498 mites was trans-
ferred: 85 to each of five colonies and 73 to one colony.
On 24 May 1996, around 1500 mites were collected by
applying industrial talc to four heavily infested colonies.
The fallen mites were washed in tepid water and placed
in storage dishes within 20 min of applying the talc.
Later that same day a total of 1275 mites was trans-
ferred: 85 to each of the 15 study colonies.
All mites were individually placed, using a fine brush, on
to nurse bees occupying frames from the study
colonies which contained open brood. Only mites that
were able to move unaided from the brush on to the
bee were used and a maximum of 30 mites was placed
on bees on any one frame.
The floor debris was collected daily over the following
three days to estimate the mite rejection rate.
Study colony manipulation
To ensure that the study colonies had discrete bee
brood cycles the presence and absence of worker bee
brood was manipulated. To achieve this, on the first day
of the study (2 June 1995; 24 May 1996) the queen was
confined to a single frame of empty worker comb using
a queen cage. This cage allows only workers free pas-
sage to and from the isolated frame. The comb in the
cage was replaced at 3–4 day intervals, so the queen
continued to lay eggs normally when released after the
10-day isolation period. All eggs laid during the caged
period were removed from the hive and either
destroyed by chilling or placed into the support
colonies. During the next 8-day period the queen was
allowed to lay freely in the colony before being isolated
again for another 10-day period. This alternating 10 : 8
day cycle was continued throughout the period of the
study (fig. 2). This design controlled the maximum
116 Martin; Kemp
FIG. 2. Manipulation of the study colonies during the study. This shows the periods when the
queen was caged or free and the number of bee breeding cycles, hence the maximum number
of times (reproductive cycles) a mite could breed. E = bees eggs laid; 1= cells sealing and mites
invading; A = bees and mites emerging; Su = supplement brood from support colonies added to
study colonies; R = indicates collection of one colony (1995) or two colonies (1996).
the percentage of mites which invade cells was estimat-
ed by:
[1– (b/[a + b])] ×100
The estimated percentage of mites invading cells for all
study colonies in the brood cycle just prior to being
collected in 1995 was 90% ± 5 (n= 6) and 85% ± 8 (n
= 12) for 1996.
Natural mite drop
During the study different numbers of mites dropped
during the periods when brood was emerging or not
emerging (fig. 3). The ratio between the mite drop dur-
ing ‘no brood emergence’ and ‘brood emergence’ peri-
ods was fairly constant 1: 12 ± 2 (n= 5, first hive
excluded due to very few mites) in 1995 but lower and
more variable 1: 7 ± 5 (n= 6) in 1996.
The daily death rate of adult female mites during peri-
ods when brood was emerging was 0.069 ± 0.015
mites per day in 1995 and 0.054 ± 0.026 mites per day
in 1996. When no brood was emerging, i.e. mortality
during phoretic period, the daily death rates were
0.0045 ± 0.0017 mites per day in 1995 and 0.0076 ±
0.0052 mites per day in 1996.
Half of the mites (51% ± 13, 1995; 49% ± 12, 1996)
found in the debris during the times of brood emer-
gence were pale (not fully tanned) while pale mites dur-
ing periods of no brood emergence were much less
common (12% ± 14, 1995; 24% ± 16, 1996). Irrespec-
tive of the size of the mite population the number of
the adult female mites in the debris represented 30%
±6 (1995) or 29% ± 9 (1996) of the total mite popu-
lation which emerged from worker cells. Of the mites
in the debris that were sampled daily during brood
emergence in the laboratory, around half (54%, 1995;
40%, 1996) were still alive although these mites would
die within 24 h (personal observation). These live mites
in the debris represented 19% ± 6% (1995) and 15% ±
8% (1996) of the total live mite population that
emerged from the cells.
Mite buildup
Despite the colony manipulations and only being able
to reproduce in worker brood, all 21mite populations
increased in size with 12 mite populations showing a
continuous increase throughout the study period (table
2A). Even the colonies which were excluded from the
detailed study because of irregular mite drop or lack of
brood, still showed considerable increases in mite num-
bers (table 2B), despite being unable to reproduce in
drone brood.
The data from the study colonies were compared with
a theoretical matrix model (Martin, unpublished) of
mite population growth, to estimate the number of
reproductive cycles necessary to obtain the observed
increase in mite levels.
In the model the following assumptions were made,
being based on the data obtained from this and earlier
studies:
Since the number of previous reproductive cycles
performed by the initial group of mites was
unknown, the model uses a reproductive age (num-
ber of times the mite has already reproduced)
distribution similar to that generated by a theoretical
population arising from a single mother, which is
skewed towards younger mites (table 3). This should
be more realistic than assuming all mites to be of the
same reproductive age.
86% of the mother mites enter cells to breed during
each brood cycle and the remaining 14% survive to
breed during the next bee generation.
Each mite produces an average of 1.1viable female
offspring during each reproductive cycle.
16% of the adult female offspring produced during
each reproductive cycle die trapped in the varroa
floor and so fail to reproduce during the next cycle.
There is no export or import of mites.
There is no removal of mites from brood cells or
bees (grooming).
Figure 4 shows how the number of reproductive cycles
performed by the mites affects its population build up
using the above assumptions. The observed increases
in mite population in the study colonies suggest that the
mean number of reproductive cycles required to
explain both the live (fig. 4a) and cumulative total (dead
+ live) (fig. 4b) mite population build up, lies between
two and three.
DISCUSSION
The following observations suggest that the results
from this study, despite the colony manipulations, may
be representative of natural colonies.
The daily emergence pattern, indicated by the daily
mite drop, monitored in the laboratory, was similar
to that found in other studies (Wendel &
Rosenkranz, 1990; Boot et al., 1993).
The percentage of mites falling on to the bottom
board during one mite reproductive cycle (12 days),
was similar in this study (29%–30%) to the 29%
observed by Boot et al. (1995).
The mean phoretic mite death rate in this study
(0.006 ± 0.003) compares well with the results of
other studies (0.006, Fries et al., 1994; 0.006, Boot
et al., 1995).
The intrinsic rate of increase (r) in this study (0.0243
± 0.0089) is similar to that found in previous studies
(0.027, Calatayud & Verdú, 1993; 0.021, Kraus &
Page, 1995).
Number of reproductive cycles by varroa in honey bee colonies 119
seven days another 93 mites were recovered from the
debris. The nine colonies with the symptoms of chalk-
brood (mummified larvae) accounted for 80 (86%) of
these mites, while only 13 mites were recovered from
the six colonies which showed no signs of the disease.
Dispersal of mites
Bayvarol treatment of the support colonies on the
study site at the end of 1995 revealed four mites in one
colony while the remainder were clear. Similar treat-
ment in 1996 showed a total of 36 mites; one hive had
10 mites while the other 10 hives had from zero to six
mites each. These findings suggest low levels of local
mite dispersal from the study colonies.
Number of mites invading cells during
the first cycle
The number of mites which were thought to have
invaded cells was estimated for the three study
colonies which were collected after the bees had
completed one brood cycle. This was calculated by two
methods. The first involved subtracting the number of
mites remaining on the bees and those recovered from
the debris from the number of mites introduced. The
second estimate was obtained by dividing the total
number of adult female mites emerged from sealed
brood by 2.1(1mother + 1.1offspring). However,
there was a large difference between the two methods
suggesting that either mothers produced very few off-
spring, 0.18 rather than 1.1, or over one-third of the
mites that were introduced were lost outside the hive.
Percentage of the mite population
invading cells
For all colonies the number of mites invading cells in
the brood cycle prior to colony collection was estimat-
ed by dividing the number of adult female mites
emerged from the sealed brood (alive and dead mites)
by 2.1(1mother + 1.1offspring) (a). Using this and the
number of mites which remained on the adult bees (b),
118 Martin; Kemp
FIG. 3. Natural mite drop during periods in the presence or absence of brood emerging during
the study period.
Number of reproductive cycles by varroa in honey bee colonies 121
The initial high acceptance rate of mites is probably due
to individually placing the mites on to the nurse bees.
The resulting high proportion of mites invading brood
cells during each bee generation is due to the large
numbers, (around 1900 cells per day) available for the
mites to invade, in relation to the number of bees. Our
measurements of the percentage of mite population
invading cells (85–90%), compare well with the predic-
tions derived from the equation of Boot et al. (1994).
This supports their finding that there is a strong rela-
tionship between the brood : bee ratio and probability
of mite invasion.
The death of any mites after cell emergence, and prior
to breeding in another cell, will lower the overall repro-
ductive success of the mite population. In this study,
16–19% of the adult female mites emerging from the
worker cells fell to the floor and were still alive, and so
would have been considered viable in any calculation of
mite reproductive success, since in all studies the
reproductive capacity is calculated at or just prior to
bee emergence. This means that the average value of
1.1adult female offspring produced per mother mite
is an overestimate. If this value is lowered in the matrix
model both the estimated percentage of mites entering
cells and average potential number of reproductive
cycles increases.
It is not clear why the rate of mite population growth
in the three colonies which were assessed after one
bee brood cycle was low (table 2A). It is possible that
the reproductive success of the mites was greatly
reduced by the transfer of the mites or, more likely, that
mites were lost outside the hive. Using the mite-drop
data collected from all the other hives during the emer-
gence of the sealed brood from the first cycle it is pos-
sible to estimate the mite population after one brood
cycle in these colonies. This shows that overall the mite
population increased by only 8%. Even the colony
which showed the greatest increase of 69%, is still short
of the 110% (1.1offspring) expected. Fries and
Rosenkranz (1996) showed that the reproductive suc-
cess of varroa is not influenced by previous brood
cycles. If the rates of mite reproduction during the first
cycle are normal then the mite loss which occurred
outside the hive must have been around 39%. Lodesani
et al., (1996) found that 14% of the natural mite drop
was recovered in dead bee traps (Gary trap) placed
outside the hive, suggesting that at least this number of
mites die outside the hive. However, since the model
used in this study has no allowance for the export of
mites; any export or drop in reproductive success
which occurred in the field will mean that the number
of reproductive cycles needed to account for the
observed mite build up will have to be increased.
120 Martin; Kemp
FIG. 4. Theoretical increase of mite populations whose females undergo 1– 4 reproductive
cycles (lines) compared with the observed increase (squares) of both live (A) and cumulative
total (live + dead) (B) of mites in the study colonies.
TABLE 2. Number of mites recovered from each colony after they had the opportunity to
reproduce one to seven times. The mite populations which showed continuous growth (A) or
for various reasons showed irregular growth (B) and so were excluded from the detailed final
analysis. The start number of mites is the number initially introduced minus the number
found in the debris within 10 days of the introduction.
A
Year of study No. of completed Start no. Total live Total mites Total adult
bee cycles of mites mites recovered recovered female mites
or maximum no. attached to bees in debris produced
of times mites
could reproduce
1995 157 58 12 70
1996 173 70 27 97
1996 17154 28 82
1995 2 74 124 54 178
1996 2 71104 110 214
1996 2 71109 92 201
1995 3 81195 175 370
1995 4 83 456 365 821
1996 4 80 321313 634
1995 5 80 438 404 842
1995 6 80 1525 776 2301
1996 6 77 1072 566 1638
B
Year of study No. of completed Start no. Total live Total mites Total adult
bee cycles of mites mites recovered recovered female mites
or maximum no. attached to bees in debris produced
of times mites
could reproduce
1996 3 69 93 117 210
1996 3 80 103 112 215
1996 4 62 183 249 432
1996 5 68 164 199 363
1996 5 67 300 179 479
1996 6 68 529 367 896
1996 7 67 395 305 700
1996 7 77 562 486 1048
1996 7 76 740 399 1139
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tion and population growth.] Dissertation, Aristotle University of
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JEFFREE, E P (1951) A photographic presentation of estimated numbers
of honeybees (Apis mellifera) on combs in 14 ×8 inch frames. Bee
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Number of reproductive cycles by varroa in honey bee colonies 123
The model of Fries et al. (1994) used a value of 1.4 for
the average number of reproduction cycles, which
meant that the mite population growth must occur
mainly in the drone cells. The present field study has
shown that rapid mite population growth can occur in
drone-free colonies. Thus, the previous value for the
average number of reproductive cycles must be
increased.
The present study suggests that the average number of
mite reproductive cycles in field populations lies
between two and three. This range is more realistic
than previous studies, since it is based on several
colonies, has been replicated and is supported by
recent independent field data (table 1).
Variations in some of the values, e.g. percentage of
mites entering cells, affects the predicted number of
reproductive cycles. However, most changes resulted
in increasing the value since most of the assumptions
underestimate the final number of mite reproductive
cycles, e.g. no export from the hive or removal of mites
from cells.
It is unlikely that a reliable single definitive value for the
mean number of reproductive cycles can be calculated,
since this factor is ultimately determined by variables
such as mite lifespan, brood availability, mating efficiency
and infertility which are still poorly understood. How-
ever, this study has shown that despite these variables
most mites will perform on average two to three
reproductive cycles given non-limiting conditions. This
provides for the first time a satisfactory explanation for
the observed rapid buildup of mite populations despite
their low fecundity during each reproductive cycle.
ACKNOWLEDGEMENTS
I am grateful to J Perrett for help in the laboratory and to D Ducker and
P Creasey of Exeter University for allowing me to use data from their
undergraduate theses. Also many thanks to the Trustees of the Chatsworth
Settlement for their invaluable assistance during this study. This work was
funded by the Horticulture and Potatoes Division of the Ministry of Agri-
culture, Fisheries and Food and the British Beekeepers Association.
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122 Martin; Kemp
TABLE 3. Theoretical distribution of mites having completed (0 to 4) reproductive cycles.
This is based on the reproductive age distribution arising from a single mite after it and its
offspring have passed through six bee generations.
Maximum no. of % of mites having completed n reproductive cycles
mite reproductive cycles n = 0 n = 1n = 2 n = 3 n = 4
1cycle 50 50
2 cycles 50 3119
3 cycles 50 27 158
4 cycles 50 26 147 3
... The observed positive association between mid-summer sealed brood cells and mite infestation level was not surprising as this has also been observed by others [76][77][78][79]. Varroa mites have a non-reproductive phase on adult bees for movement between hosts and/or feeding [80], and a reproductive phase inside drone or worker brood cells [81]. ...
... Varroa mites have a non-reproductive phase on adult bees for movement between hosts and/or feeding [80], and a reproductive phase inside drone or worker brood cells [81]. When brood is not scarce, there is a positive relationship between brood cells and mite infestation in the brood [76][77][78][79]. We also found that the mid-summer sealed brood population has a positive correlation with honey production, as observed during both experimental years, and in previous studies [76,82,83]. ...
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Fifteen honeybee colonies (Apis mellifera L.) infested with the ectoparasiteVarroa jacobsoni Oud. were monitored for the number of mites falling to the bottom of the hive. Mites in the debris were counted periodically on the plastic sheet on which they were collected. Two months later, colonies were treated with an acaricide to determine mite population. A high positive correlation was found between the number of mites collected in the hive debris over different periods and the final population size. Based on this correlation, it was possible to use hive debris counts to predict the degree of infestation. Furthermore, counting fallen mites over a period of two months, followed by an acaricide treatment, might be a useful method of estimating the rate of growth ofV. jacobsoni in honeybee colonies.
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The female genital tract ofVarroa jacobsoni is composed of a sperm-access system comprising paired solenostomes located between coxa III and IV, paired tubules, paired rami, an unpaired sperm duct, and an unpaired spermatheca. Another part of the female genital system is confined to egg development and oviposition. It is composed of an ovary (s.str.), in which oocytes mature, and a lyrate organ functioning as a nutrimentary structure. Both compartments, regarded as parts of the gonad, are connected by a region named the camera spermatis. This part is also in continuity with the oviduct I, which is provided with a muscular layer and numerous nerve endings. The following cuticle-lined oviduct II leads to the genital orifice through which the eggs are deposited. The fine structure of all these parts is described. Attention is drawn especially to the peculiar spermatheca which contains the “inner cells” which are thought to connect by way of free cells with a specialized region of the camera spermatis, thus establishing a “cellular bridge” through which penetration of capacitated spermatozoa into the ovary s.str. may occur. Lyrate organ and oocytes are connected via intercellular bridges/nutritive cords and are thus comparable to the telotrophic ovarioles of certain insects. The male genital system, composed of unpaired testis, paired vasa deferentia, unpaired accessory gland and ductus ejaculatorius, is described ultrastructurally. Spermiogenesis occurs in cysts and spermatozoa belong to the “ribbon type”. The vasa deferentia are provided with a muscular layer. For the first time receptors are detected in the proximal part or the ductus ejaculatorius. The accessory gland produces a proteinaceous secretion. Spermatozoa were observed in the female rami and spermatheca. Only in the latter were elongated, capacitated spermatozoa seen.
Article
Reproduction of Varroa jacobsoni Oudemans (Acari: Varroidae) and the number of Varroa mites that were found dead on the bottom board of the hive, were studied in relation to the period the mites spent on adult honey bees, Apis mellifera L. (Hymenoptera: Apidae), prior to invasion into brood cells. The maximum period on adult bees was 23 days. To introduce mites, combs with emerging worker brood, heavily infested with mites, were placed into a colony and removed the next day. At the beginning of the first day following emergence from brood cells, 18% of the mites introduced into the colony was found on the bottom of the hive. Part of these mites may already have died inside the capped brood cells, and then fallen down after cleaning of cells by the bees. At the second and third day following emergence, respectively 4% and 2% of the mites on adult bees at the previous day was recovered on the bottom, whereas from the fourth day on only 0.6% of the mites on adult bees was recovered on the bottom per day. After invasion into brood cells, 8–12% of the mites did not produce any offspring. Of the mites that did reproduce, the total number of offspring was 4.0–4.4 per mite during one reproductive cycle, part of which may reach maturity resulting in 1.2–1.3 viable daughters, and 8–10% of the mites produced only male offspring. Reproduction was independent of the period the mites had spent on adult bees prior to invasion into brood cells.
Article
The development of an infestation by five to eight introduced adult females ofVarroa jacobsoni Oud. in 35 honey-bee (Apis mellifera L.) colonies was monitored for 16 months with no outside source of infestation. Calculations on the size of the mite populations were based on collection of debris, samples of bees and brood, and estimates of number of bees and broodcells during the summer. In the winter, only dead bees and debris were collected. Samples were taken at 3-week intervals. Data indicated that the mite population probably could increase more than 100 times within one summer, and more than ten times between years, in a climate with a brood-rearing period of less than five months. A large variation in mite population increase existed between colonies. The winter mortality of mites that die with the host or drop from the winter cluster has a large influence on the population dynamics of the mite. Data also indicated that the simple method of counting mites in hive debris is a useful parameter for monitoring the population development ofVarroa in colonies with hatching brood.