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Mating flights of the queen honeybee (Apis mellifera) in a subtropical climate
Camp. Biochem. Physiol. Vol. 81A, No. 2, pp.
0300-9629/85 $3.00 + 0.00 0 1985Pergamon Press Ltd
2299241,1985
Printed in Great Britain
MATING FLIGHTS OF THE QUEEN HONEYBEE (APIS MELLIFERA) IN A SUBTROPICAL CLIMATE YAACOV LENSKY and MICHAL DEMTER The Triwaks Bee Research Center, Hebrew University of Jerusalem, Faculty of Agriculture, 76100 Rehovot, Israel (Received 16 July 1984) Abstract-l.
Mating behaviour of queens and drones and mating success were studied throughout the year. 2. Worker bees directed virgin queens to leave the hive and take mating flight. 3. Cloudiness above 7 octavas and wind velocity above 3.9m/sec. delayed queen and drone flights. 4. Duration of queen tlights was reduced at 15-20°C and wind velocity of 2.63.9m/sec. 5. The peak of flight activity hours of queens and drones overlapped throughout the year. 6. CO,-treatment of queens resulted in a delay of mating flight and in an enhancement of egg-laying. 7. The queens successfully mated throughout one year. 8. Colonies headed by 2-lo-month old queens yielded similar honey crops.
INTRODUCXION
Honeybee queens and drones mate during fights which generally occur on warm and sunny days. Drones fly to established drone congregation sites (Ruttner, 1966) and are attracted to these sites by pheromones of unknown chemical nature which are secreted by the drone’s mandibular gland (Lensky et al., 1984). At the present time it is not clear who is attracted to whom first, drones or queens. It is known that drones are attracted to queens at distances greater than 50 m by a pheromone produced in the queen’s manidbular gland, E-9-oxodec-2-enoic acid. At distances of up to 3Ocm drones are attracted to queen pheromones (chemical identity not known) from Renner’s glands, which apparently trigger copulation (Butler, 1971; Renner and Vierling, 1977). The queen mates with several drones during her mating flights. Workers are attracted to the 4-6-day old queen due to the secretion of queen pheromones from the mandibular glands (Pain, 1961). Workers participate passively in the queen’s mating llight, by restricting the queen’s movements specifically in the direction of the hive entrace, and by emitting Nasanov gland’s scent inside and outside the hive (Fletcher and Tribe, 1977; Hammann, 1958; Ruttner, 1956). This worker behavior continues until the queen begins oviposition (Hammann, 1958). The queen leaves for her first mating flight generally when 5-6 days old (Alber et al., 1955; Fletcher and Tribe, 1977), while drones’ mating flights occur 7-9 days after emergence (Drescher, 1969; Kurennoi, 1954; Oertel, 1956). Queens fly an average of 2-5 flights (Alber et al., 1955; Fletcher and Tribe, 1977; Ruttner, 1956), and drones 25 ilights (Whiterell, 1972). There are two types of drone and queen flights: short orientation Bights, lasting l-10 min, and longer mating flights, lasting 5-27 min (queen) (Fletcher and Tribe, 1977; Soczek, 1958; Woyke, 1975), or an average of 33 min (drones) (Drescher, 1969; Whith-
erell, 1972). Although honeybee mating has been extensively studied, the timing of queen and drone flights has not been examined simultaneously. All that is known is that queens and drones leave the hive during the afternoon hours, the greatest activity being between the hours of 14.00-16.00 (Bol’shakova, 1978; Ruttner, 1956; Soczek, 1958; Taber, 1964; Woyke, 1975). Taber (1964) suggests that climate does not influence mating behavior. In contrast, most researchers believe that climate does influence mating behavior, with mating occurring above 20°C and during times when wind speed is less than 4-5 m/set on clear, cloudless days (Alber et al., 1955; Bol’shakova, 1978; Drescher, 1969; Fletcher and Tribe, 1977; Oertel, 1956; Ruttner, 1955; Soczek, 1958; Taber, 1964). Investigators have not pinpointed the climatic factors associated with mating. Research on the conditions and, factors that influence honeybee mating behavior has both applied and theoretical value. Queen rearing and mating in Israel takes place during March-April and in September. It is generally accepted that during other months, successful mating is not possible, however no scientific studies prior to the present research have been undertaken in Israel to verify this contention. Queen replacement in the commercial apiary is an important aspect of successful beekeeping. Because of the queen’s high egg-laying rate it is important to requeen annually in order to maintain high adult population levels and to prevent swarming (Barkan, 1981; Lensky and Seifert, 1975; Lensky and Slabezki, 1981). The time of requeening depends on the supply of commercially reared queens, which is mostly in the spring and to a lesser extent in September. Because of the rapid population growth in the spring and pressures of colony work associated with swarm control and honey production it is hard for the beekeeper to requeen during the spring. In addition there is a loss of queens throughout the year for various reasons. Year-round availability of queens may solve these above-mentioned problems. 229
CBPA 8 1/Z-B
230
YAACOV LENSKY and MICHAL DEMIER Table I. Percentage of &gin queens accepted in mating nuclei Date of introduction of queen cells
Date of emergence of queens
No. mating nuclei
Accepted queens (%)
1980 6 June 17 July 14 September 5 October 15 November
1 June 19 July 18 September 6 October 15 November
I 12 15 17 15
86 92 87 59 87
1981 19 January 18 February 15 May
20 January 19 February 17 May
17 11 14
53 64 86
The goals of this study were to: (1) study the behavior of the workers and queen from queen emergence to the onset of oviposition in glass-walled observation hives and in mating colonies; (2) determine whether there exists an overlapping of the hours during which queens and drones fly throughout the year; (3) quantify the number and duration of queen flights throughout the year; (4) describe the climatic conditions associated with successful mating, and; (5) determine the times of the year during which queens can be reared and mated in Israel, based on the analysis of mating success and queen quality by measurement of honey yields. MATERIALS
APllD METHODS
Queen rearing Queen honeybees (Apis mellifera L. var. ligustica) were reared each month from Italian stock brought from the U.S. Cell builders were either queenless or queenright with the queen confined to the lower super. Cell builders were fed in August and January with a 60% sugar solution for 2-5 days before receiving the grafted larvae. In July, August, September, November and February cell builders were fed a 40-60x sugar solution throughout the queen rearing process, until the day on which cells were sealed.
colonies and the proportion in Table 1. Observations period
of accepted
queens is indicated
of queen and worker behavior during the mating
Two glass-walled observation hives were used. Queens cells were introduced on October 9, 1980 and queens began oviposition on October 30, 1980. Observation began upon queen emergence on October 11, 1980, and lasted until October 30, 1980, when queens began oviposition. The behavior of workers towards the queens was examined throughout the observations every several hours. Continuous observation of worker and queen behavior were made between 12.30-15.30 hr (local time) every day. Observations
of queen mating jights
Drone traps were installed at the entrance of the mating hives in order to examine the parameters associated with mating. The trap blocked the entrance of the hive, preventing the exit of the queen. The mating success of queens held in mating colonies that were fitted with drone traps relative to queens held in control colonies was examined by comparing the percentage of successfully mating queens and the number of days between queen emergence and the onset of oviposition (Table 2). Since the presence of the drone trap did not delay egg-laying activities, they were used in subsequent experiments. They were removed after the queen went out on a mating flight. Observations were conducted at the Triwaks Bee Research Center, Rehovot, during June-July, September-November, 1980; January-February and May 1981.
Drone rearing Because there are few drones in colonies during the fall and winter under natural conditions, we introduced 2 frames with a drone foundation in each of 5 colonies on June 24, 1980. In follow-up observation, however, we found that only 4 frames had eggs. There was a positive correlation between the number of combs with eggs and the length of time they had been in the hive. From February to April 1981, SO-100% of the combs had drone brood. Thus, in order to rear drones, frames with a drone brood foundation must be installed in hives in the spring. A4ating hives Observations of seasonal mating patterns were made on mating hives (50 x 25 x 24cm), each holding 4 frames: 2 brood, 1 honey, and 1 pollen. The number of mating
Observation
of drone mating jights
Observations were made of 5 colonies whose populations covered at least 10 frames. Drone traps were installed at hive entrances and observations were made 5 days per month, overlapping the days on which queens were observed. Examinations
of the onset of oviposition
On the day after the queen stopped making long mating flights the presence of eggs was ascertained. Daily examinations were continued until eggs were seen in all mating colonies or until 14 days had elapsed since the queen stopped making mating flights. Fourteen days after the appearance of eggs the brood was checked to determine whether the eggs had been fertilized.
Table 2. Onset of egg-laying in queens maintained in hives blocked by a queen trap and in hives with free entrances (June&&ember. 1980) Mating nucleus Restricted entrances Free entrances
No. nuclei 34 17
Laying queens (%) 41 67
No. days from emergence to egg-laying 9.00 * 0.05 9.14 * 0.09
231
Honeybee mating flights Carbon dioxide anesthetization of virgin queens
Queen cells reared from larvae grafted on 29 February
a
Hive no.
~
Hive no. 2
1980 were removed from the cell-builders 10 days after grafting and placed in an incubator (32°C 60% R.H.). Upon emergence they were anesthetized with carbon dioxide for thirty seconds and introduced into mating colonies. They were then observed from 10 October to 13 October 1980. Imtroduction of queens mated in mat&g colonies into fill-sized colonies To check the quality of queens mated at various times of the year, a random sample of these queens was transferred to each of 3-4 frame colonies. Population growth and egg laying rates were checked at random from queen introduction to 10 February, 1981. From 10 February 1981 to 15 April 1981, examinations were made every two weeks; supers were added and frames of brood raised according to need. Honey yields were established on 21 April 1981. Equipment for the measurement of climatic conditions A record of climatic conditions on each day of observation was made every half hour. The following equipment was usedz (1) ~e~ometer-l~lOO°C (Phoenikia, Israel) (2) anemometer~Casella, London) (3) sol~meter~ipp and Zonen, Delft, Holland).
cl R”,;“,:;g,d”f workers
Worker behavior, as related to the leaving of the queens on a mating flight, was investigated in observation and mating hives. hives (October
1980)
Queen cells were introduced into two glass-walled hive colonies on 8 October 1980. Worker and queen behavior was observed for 20 days after the emergence of the queen, or until the onset of oviposition. Young queens walked around and fed themselves, and were not attended to by workers for the first three days. Beginning on day 4, workers did feed and antennatethe queen (Fig. 1). From day 5 to the beginning of the queens’ oviposition (7 and 12 days after queen emergence, respectively) distinct worker behavior was observed daily between the
Activity
of
Queens
Running
of
Workers
Running
of
Queens
Queen’s
vibratory
Exposure
Mating Removal
of
and
Observation made in front of entrance to mating hives (June 198~May 1981)
Intensive worker flight activity preceeded the queen’s exit by 50-60min. Some workers stood on the drone trap and exposed their Nasanov glands. Queens leaving the mating hive were caught in the drone trap, from which they moved to the second super of the colony, accompanied by workers. Intense
Workers
dance
scent
gland
mating
sign
a
by
workers
t
A’
’
-
flight of
Pzzz--=-+
D B
z/z
z:
Of
hours of 12.30-16.30. During this time some workers ran to and from the entrance repeatedly (Figs 2-10). Prior to exiting for a mating flight, the queen would participate in this running 15-30 min after it began. The queen interrupted this running every 5-lOmin, exposed the intersegmental membranes of her tergites and groomed her abdomen with her hind legs (i.e. vibratory dance). Part of the workers tried to direct the queen away from the hive entrance, while others stood near the entrance exposing their Nasanov gland during the 10 min prior to the queen’s exit. Workers removed the drone’s penis from the newlymated queen (Fig. 2).
Colony behavior during the mating period
in glass-walled
The onset egg-laying
Fig. 1. Behaviour of worker bees towards queens from 4th day after emergence till the onset of egg-laying. Two colonies in observation hives were used (Rehovot, October 1980).
RESULTS
Observations
Of mating flights
Days
1
I
I
Pig. 2. Behaviour of worker bees and a queen bee before and after mating flights, as observed in two observations hives (Rehovot, October 1980).
YAACOVLENSKYand MICHALDEMTER
232
01 II-16 J”“e
I
I
I
24-2s JULY
17-M NO”.
21-25
Sept.
I 23-30 Jan
I
1
23 Feb 5 March.
0
20-26
May 1981
1980
Fig. 3. Seasonal effect on queens’ first mating flight and on the total number of mating flights (Rehovot, 198&1981).
worker flight activity declined after the queen was released from the drone trap and flew off. Two to five minutes prior to the return of the queen, workers crowded the entrance of the hive and released Nasanov pheromone. When the queen alighted at the hive entrance she was accompanied by workers, and if she returned with a penis in her vagina, they tried to remove it. The workers at the hive entrance entered the colony within 5 min of the queen’s entrance. The influence of season on queen matingflights: timing and number The date of the first mating flight was considered to be the first date on which the queen was found in the trap or second super (via the trap). To establish the number of flights, traps were returned to the hive entrances after the queen returned from her flight. Results were calculated as follows: (1) Mean date of first mating flight = X7 day of first flight n n = number of queens.
F= Total 0 = Total
no. of flights no. of Queens
(2) Mean number of flights per queen = C< all frights n f = number of flights, n = number of queens. From the results in Fig. 3 one sees that in the months of June-November 1980 and May 1981 queens took their first mating flight 5-6 days after emergence and flew an average of 2-3 flights. During January and February 1981 queens took their first flight 8-9 days after emergence, and flew an average of 11-13 flights. Duration of mating Jlight Duration of mating flight was calculated from the time the queen was released from the entrance trap and took off on a flight to the time she alighted on the hive entrance. The number of observations of duration of mating flights does not correspond to the number of mating flight, because some returns were not seen. These observations indicate the two types of queen flights exist: short and long. Queens returned
qShort Long
flights fUghts
(l-5 mini 05 min)
z E
12
1980
1981
Fig. 4. Seasonal effect on the duration of queens’ short and long flights (Rehovot, 1980-1981).
233
Honeybee mating flights
23
Feb-
5 March Hz5
/ 1981
17-24 Nov. 1980 H=lO
d
24-29 July
1980
“=B
II-16
June
1980
H = No.
Hr
of
hives
of flight
Fig. 5. Seasonal effect on the frequency and the hours of queens’ mating flights (Rehovot, 1980-1981).
from long flights mated, as evidenced by the usual appearance of the penis in the queen’s vagina. The results in Fig. 4 show that:
(1) During all months queens took at least one long flight; (2) During all months queens took more long flights than short flights, except in February; (3) Short flights were l-5 min in duration, whereas long flights were l&15 min in duration.
In the winter and spring the peak occurred between 13.00-14.30 hr, and in the summer and fall this period was between 14.00-15.30 hr. (3) The total number of flights made by a queen varied with the month. During February the total number of queen flights was much larger than in other months. Climatic conditions also influenced the lota number Of flights’ The average time at which mating flights began was determined in the following way:
Time of day at which mating took place
zc;2
-
Results are summarized in Fig. 5. They show that: (1) Queens fly for 2-3 hr every month. In winter and early spring, queen flights occurred 1.5 hr earlier than flights in spring and summer. (2) In each month there was a period of peak queen flight activity, during which 50% of the queens flew.
F-II 16-Q=
I*_
I ‘,I-16 June
I 21-25 sap-t. 1980
rfrSE
X = mean time (hr) at which each queen began her mating flight, n = number of queens. The mean time at which mating flights began is indicated in Fig. 6. In January flights occurred ear-
5
I 24-25 J”lY
n
I 17-24 NW.
F = Total
no. of flights
0
Queens
= No. of
I 23-30 Jon.
I 23 Feb.5 March 198 I
I 20 -26 MOY
Fig. 6. Mean (2 SE) queens’ mating %ght hours throughout the year (Rehovot, 1980-1981).
YAACOV LENSKY
234
Table 3. Position of the sun during Date
20-26 Mav
15.39f0.13 14.41 ir 0.12 14.30 * 0.08 13.37 * 0.09
11.06 9.51 9.02 7.24
20.55 19.59 20.51 20.58
48.82 49.05 48.67 57.89
13.00 +_0.10
6.22
19.52
53.01
196.31
13.24 + 0.07 14.30 + 0.01
7.13 9.50
19.47 19.55
43.21 36.04
206.57 260.62
(1) Number of hours from sunrise to the time at which queens took flights. (2) Number of hours from sunset to the time at which queens took flights. (3) The angle of zenith based on the following formula (List, 1966): COST cos* sin6 sin4
= angle of zenith, = declination of sun, = meridean, = angle of hour.
(4) Sun azimuth was calculated according to the following formula (List, 1966) cos 6 sin * sin CI= sin z CI= sun azimuth. The results in Table 3 show that: (1) Throughout after sunset.
Fig.
flights
Angle of zenith
Position of the sun during the time at which mating flights occurred Does the position of the sun influence the time at which mating flights occur? To answer this question the following calculations were made:
z 6 4 4
queens’ take off for their mating Hours from sunset
Bight (hr)
liest in the day, (13.00 +_0.09 hr) and in June latest (15.39 f 0.15 hr).
cos z =cos6
MICHAL DEMTER
Hours from sunrise
Mating
1980 11-16 June 2&29 July 21-25 September 17-24 November 1981 23-30 January 23 February-5 March
and
the year queens fly 20.19 + 0.12 hr
7. Mean drones’ flight hour throughout on five beehives
during
Azimuth
of sun
266.01 259.07 237.41 211.22
(2) The angle of zenith during flight periods was between 36.04-57.89”. (3) The sun azimuth during ilight periods was between 196.31-266.01”. The timing of drone flights The purpose of these observations was to determine if drones engage in mating flights at the same times as queens during the entire year. Traps were installed on 5 colonies chosen at random. Drone and queen flights were observed on the same days. The number of drones trapped in the second story was determined daily at half-hour intervals, after which time they were released. At the end of each day’s observations, all the traps were removed except for one, which was kept to check for early drone flights the following day. Calculations of drone tlight activity were made according to the general average of 5 days of observation which were picked at random from all the observations of each month. The results in Fig. 7 show that: (1) Drones take fight 24 hr daily. In the winter and spring the timing of their flights is earlier (10.30-l 1.30 hr), than in the summer and fall (11.30-12.30 hr). (2) The peak period of activity, during which more than 50% of the drones flew, occurred between 12.00-13.30 hr in the winter and spring, and 13.30-15.00 hr during summer and fall. Throughout
the year. Each point represents five consecutive days (Rehovot,
a mean of observations 1980-1981).
made
235
Honeybee mating flights 6 0
Drones
tza Queens
127 12 t
1981
1980
Fig. 8. Overlapping of flight hours peaks of queens and drones throughout the year. Above the bars; the number of individuals exiting from a beehive during the peak hours; beneath the bars; the total number of individuals that took flights (Rehovot, 1980-1981).
the year drone ilights were not observed
from sunrise to 10.00 hr although worker flight was evident. (3) The number of drones taking flights varied with the month. In September the minimum number of
Climatic jligh ts
drones took flights, and in May-June the maximum number was attained (70 drones per colony). Peak flight periods for drones and queens (the period during which more than 50% of the individuals took Bights) are presented in Fig. 8. These results indicate that there is at least a 30min overlap in the two periods of the year. Drone flight periods began and ended about 30 min before queen flight periods began and ended.
than 3.9 mjsec (Fig. 9a: days 7 and 8 post-emergence; Fig. 9b: day 5 post-emergence). Flights also did not take place on rainy days (Fig. 9b: days 6-7 postemergence). From Fig. 9a we see that on day 4 post-emergence only drone flight occurred, because queens do not take their first flight until they are 5 days old.
Injuence
of climatic conditions on queen and drone
frights
The influence of climatic factors such as temperature, cloudiness, wind speed and global radiation on queen and drone flight was examined from June 1980-May 1981. Table 4 indicates that the climatic conditions that existed during the four seasons of the study period did not influence queen and drone flight activity. To summarize: Queen and drone flights took place without disturbance at temperatures ranging from 2635”C, wind speed not higher than 2.6 mjsec and cloudiness lower than 2 octavas. On the other hand, in November 1980, and February and May 1981 the prevailing climatic conditions did inhibit queen and drone flight or increased the number of short queen flights (Figs. 9a,b and lOa,b).
Table 4. Weather Date 11-16 June 24-29 July 21-25 September 8-13 October *CO, anaesthetized.
Mating 15.39 14.41 14.30 14.33
conditions
flight (hr) kO.13 * 0.12 * 0.08 f 0.03
during
Temp (“C) 26-31 29-35 29-33 21-32
conditions
that
delayed
queen and drone
Queen and drone flight did not occur at cloudiness levels above 7 octavas and at wind speeds greater
Climatic conditions that increased the number of short queen Jights Queens that flew during the period 23 February-5 March 1981, took about twice as many short flights on days 9-13 post-emergence as they did on days 14-15, presumably due to the low temperatures that were recorded on the later days (15-18°C; Fig. 10a). A similar rise in the number of short flights occurred during 21-25 May 1981 with a 3-fold increase in short flights evident on days 5-8 post-emergence vs day 9. This increase due to strong winds, 2.6-2.88 mjsec was probably due to the fact that queens take short orientation flights on their first day out of the hive.
Success of mating throughout the year Colonies were examined daily for the presence of eggs beginning 14 days following the last day of
queen flight. The mating success of queens is presented in Table 5. These results show that there
queen and drone mating Wind velocity 0.4-1.0 1.17-1.82 1.19-2.59 1.23-2.41
(m/set)
flights
(Rehovot, Cloudiness (octavas) l&l o-2 o-o.5 o-1
1980) Global radiation (cal/cn?) 56-14 45-58 45-58 20-53
236
YAACOV LENSKY and MICHAL DEMTER
Days
from
emergence
(Queens)
(4
01
I 4
i 6
I
_
11
*
Doys from
11 10
1’ 12
emergence
14
(Queens)
(b) Fig. 9. The effect of cloudiness and wind velocity on the tlight activity of queens and drones. (a) 13.30hr, 17-23 November 1980. (b) 13.30hr, 23 February-3 March 1981. (Rehovot). was lOO’%mating success during all months except September (70%). Despite these results, there were less mated queens reported than there were mating hives. These losses occurred during:
days old, and were than introduced into mating hives. Observations of queen flights were made throughout the mating period until the onset of oviposition. The results in Fig. 12 indicate that:
(1) September 1980 and January and February 1981-65% queen loss after mating; (2) 3uly and November 1980 and May 1981-51% queen loss; (3) June 1980-39’~ queen loss.
(1) Anaesthetized queens took their first flight 7 days after emergence, while untreated queens took their first flight on day 5. Thus, carbon dioxide anaesthetization caused a delay of 2 days in the timing of the first mating flight. (2) Anaesthetized queens flew 44min later than their expected time in October (14.4 +_0.07 hr, vs 14.03 hr, see Fig. 6). (3) Anaesthetized queens took their first flight earlier than queens usually do in September and November.
The timing of the onset of oviposition among mated queens throughout the year is summarized in Fig. 11. From these results we see that during May, June, July and September oviposition began 9-11 days after emergence, while in November, January, and February oviposition began 14.5-19 days after emergence. Two to six days elapsed between the last mating flight and the onset of oviposition. The effect of carbon dioxide anaesthetization of virgin queens on the timing of mating flights and oviposition The purpose of this experiment was to investigate the possibility of shortening the mating period by administering carbon dioxide anaesthetization to virgin queens. Queens were treated for 30 set when l-3
The quality of queens mated throughout the year The following factors were evaluated as a measure of queen quality: egg-laying rate, colony population growth, and honey yields. After it had been determined that the queen had mated and had begun to oviposit she was transferred from the mating hive to a full sized colony. Beginning two weeks after queen’s introduction, (10 February-l 5 April 198 1) colonies
Honeybee mating flights -3
*O
(A)
Days from emergence to oviposition ~~TI;y;~$no$ flight 4
Q = No. of laying Queens 75
-2-
5
‘:: 2
i
_, .g
50
8
25-0
Days
-A4
fromemergence
(a) 3
-25
: 0
(A)
1980
23 Ft!b5 MO rch 1981
20-a May
Fig. 11. The onset of oviposition by queens mated during different seasons (Rehovot, 1980-1981).
-J22
Fig. 10. The effect of wind velocity and temperature on the frequency of queens’ short flights. (a) 13.30hr, 23 February-5 March 1981; (b) 14.30hr, 21-25 May 1981 (Rehovot).
headed by the recently mated queens were evaluated as follows: density of adult colony population, number of brood frames, and honey yields after the citrus honey Aow (ending on 21 April 1981). The percent survival of introduced queens throughout the year is presented in Table 6. From the results, it is apparent that the percentage of queen acceptance was relatively low during the months of September, November and January. Rejected queens were apparently balled by the colony’s workers. Queens that mated in November and Jan-
uary survived until April 1981; they disappeared as a result of frequent inspections. The results of egglaying rate, population growth and honey yields are presented in Fig. 13. All queens, regardless of the month of their mating, showed a 3-fold increase in egg laying rate and colony population from February to April. At harvest time, all colonies contained a similar number of brood frames and bees. Furthermore, honey yields were similar (41.31 5 1.42 kg/colony) among all colonies, regardless of the month the queens mated. It is important to emphasize that queens that mated in November and December were held in queen banks and introduced to colonies on 10 February 1981; these queens headed coionies that were just as productive as those headed by queens mated during the rest of the year.
DISCUSSION
Queen and worker behavior during the mating period
Observation of glass-walled and mating hives revealed the role played by workers in directing the queen to leave the hive for a mating flight. The interaction between queen and workers is illustrated in Fig. 1. Queen and worker behavior prior to queen
Table 5. Acceptanceof queens in nuclei and their mating SUCCESS throughout the year
Month
Acceptance in nuclei No. accepted q”&%lS No. cofonies
1980 June July September November 1981 January February Mav
*yeLaying queens =
Mating flights No. leaving No. returning queens queens
No. iaying queens ._-_____-
Oviposition after flights No. laying queens *Fertilized ___ No. colonies queens (%I
I 12 15 15
6 11 13 13
5 8 11 10
5 6 7 7
5 6 5 7
100 100 71.43 100
0.71 0.50 0.33 0.47
17 11 14
9 I 12
6 5 I
6 4 7
6 4 I
100 100 100
0.35 0.36 0.50
No. laying queens x 100. No. queens returned from mating flights
YAACOV LENSKY a
September
0
October
m
November
(CO,
0 = No. of Queens
from
Days from
Fig. 12. The effect of CO,-anaesthesy of virgin queens on their mating flights and on the onset of oviposition. September-November, Controls (Rehovot, 1980). mating has been observed by Hammann (1958), Ruttner (1956), and Triasko (1951), but the chronological order of these behavioral events was not specified. Our results indicate that workers begin directing the queen toward the hive entrance about 60 min prior to the queen’s exit and release Nasonov scent at the hive entrance for 10-15 min afterwards (Fig. 2). Also, the above mentioned investigators did not point out the pheromonal connection between queen and workers: The queen exposes the intersegmental membranes beside her Renner glands while participating in the “worker run” during the 45 min prior to queen flight (Fig. 2). The observation of mating hives completes the behavioural picture begun with the observation of the glass-walled hives, revealing the many worker flights and the workers’ accompaniment of the queen at the hive entrance. This behavior has not been previously described. Time of day at which matingflights occured throughout the year
Our observations revealed that throughout the year, there is an overlap of queen and drone daily mating fight periods during the afternoon. Mating flights were not observed in the morning hours (Figs 5,7 and 8). These findings suggest that queen matings can occur throughout the year in Israel. Even though drones stopped flying 30min earlier than queens during the months of June, September, November, January and February (Fig. 8), they were still in the
and
MICHAL DEMTER
air when queen flights took place. Drone mating flights average 33 min in duration (Drescher, 1969: Whitherell, 1972; Woyke, 1975), while queen mating flights last from 10-15 min (Fig. 4). This overlapping of queen and drone mating flights, as well as the timing of these flights throughout the year has also not been previously reported. From other studies it appears that in various climates and at various latitudes, queens and drones take mating tights between 12.00-17.00 hr, with maximum frequency between 14.00-16.00 hr (Alber et al., 1955; Bol’shakova, 1978; Drescher, 1969; Koeniger and Wijayagunesekera, 1976; Soczek, 1958; Taber, 1964; Whitherell, 1972; Woyke, 1975). Most queens fly at a defined hour which changes by 15-45 min every month (Fig. 6). This variation suggested that meteorological conditions may influence queen flight, via the workers. Our results indicate that queens fly 20.19 + 0.12 hr after sunset (Table 5). Taber (1964) found that as day length increases, drone flight is delayed. It is known that field bees orient to food sources according to the sun. Frisch (1967) and Lindauer (1960) explain that this orientation is due to the zenith position. Renner (1960) suggests that honeybee orientation is based on the sun azimuth position. Our calculations indicate that queen fight occurs when the zenith angle is 35-60” and when the azimuth angle is between 200-270” (Table 5). Gary (1971) suggested that queens released at distances of up to 1600 m were able to orient and return to their mating hive during the morning hours, even though they generally fly in the afternoon. The findings of Taber (1964), Gary (1971) and our results together suggest that the time of day at which queen flight occurs depends on day length, while fight orientation is based on sun zenith and/or sun azimuth angle. Influence of climatic conditions on mating flights of queens and drones throughout the year
Climatic conditions do affect queen and drone mating flights. During rainy days, days in which cloud cover was greater that 7 octavas, and/or days in which wind speed measured greater than 3.9 m/set, queen and drone flights did not take place. On the other hand, no effect of climate on the time of day at which mating flights occur was found, in contrast to Ruttner’s proposition (1956) that queen flight occurred during the time of day of maximum temperature, and to Taber’s supposition (1964) that during cold days drones fly earlier in the day. Mating tights took place throughout the year at temperatures ranging from 15°C (February) to 35°C (July). Temperature did not affect mating flight activ-
Table 6. Survival of mated queens Mating flight (month) 1980 JUXK! July September October November 1981 January
No. queens introduced into colonies
Introduction of mated queens (date)
No. queens remaining till 15 April 1981
Survival (“/,)
4 5 3 2 6
20.6 14.8 1.10 1.11 10.2
4 5 1 2 5
100 100 33 100 83
3
10.2
2
66
239
Honeybee mating flights
March
April
Fig. 13. The effect of queens’ mating date on developing and adult worker bee population and on honey yields of a bee colony. ity, in contrast to the results of Bol’shakova (1978), Oertel (1956), and Ruttner (1956), who maintained that mating flights do not occur at temperatures less than 19°C. Our research indicates that low temperatures (between 15-20°C) influence the length of queen flights. Temperatures of 15-20°C and wind speeds between 2.6-2.88 mjsec resulted in an increase in the number of short queen flights, during which mating does not occur (Fig. 10). The increase in number of short queen flights may be due to the fact that queens must mate with about 10 drones in order to fill the spermatheca (Triasko, 1956; Woyke, 1964). At lower temperatures and greater wind speeds there are less chances of mating (Alber et al., 1955). Reports of the number of queen flights (Fletcher and Tribe, 1977; Konopacka, 1968; Kurennoi, 1954; Woyke, 1975) and on their duration (Alber et al., 1955; Shoemaker, 1947; Triasko, 1951) indicate great variation, probably because the studies were conducted under different climatic conditions, not specified by the investigators. From our results it is apparent that as the number of days increased during which poor weather conditions inhibited mating flights both mating and the onset of oviposition were increasingly delayed (see Fig. 11; Taber, 1974). To summarize, during the months of November 1980, and February and May 1981 (Figs 9 and lo), the climatic conditions inhibited mating, however, they did not prevent or reduce the incidence of mating nor lower queen quality, as compared with matings at other times of the year. This conclusion is in contrast to Laidlaw and Eckert (1962) and Ruttner (1955). Influence of carbon dioxide queen mating period
anaesthetization
on the
Carbon dioxide anaesthetized queens took their first mating flight 2 days later than control queens, but oviposition began 2 days earlier. Anaesthetized queens took mating flights 44min later in the day than the other queens (Fig. 12). In constrast to our results, Skowronek (1976) reports that carbon
dioxide anaesthetization causes queens to delay their mating flights by one week. This delay may be caused by a decreased release of 9-oxo-trans-2-decenoic acid from the mandibular glands of anaesthetized queens (Pain et al., 1967). This pheromonal release causes workers to be attracted to the queen (Vierling and Renner, 1977), since the workers are in closer contact with the queen, she leaves on her mating flight at a younger age (Hammann, 1958; Harbo, 1971; Medugorac and Lindauer, 1967). Carbon dioxide anaesthetization of workers also results in a decrease in the production of mandibular gland compounds, apparently because carbon dioxide treatments affect corpora allata activity (Skowronek, 1976). According to Medugorac and Lindauer (1967), carbon dioxide anaesthetization influences the worker’s biological clock, which may also explain the delay in queen mating flights (Fig. 12). Carbon dioxide anaesthetization enhances oviposition among artificially inseminated queens (Mackensen, 1947). We also observed that carbon dioxide treated queens began to oviposit at a younger age (a smaller interval between the last mating flight and oviposition). Carbon dioxide anaesthetization of field bees results in a decrease in longevity, but does not affect their sense of orientation (Ebadi et al., (1980). Treated queens flew mating flights, mated, returned to their colony and began to oviposit, confirming these results (Fig. 12). Quality of queens mated throughout
the year
During most of the year 100% of the queens successfully mated, but the number of laying queens was different from the number of queens that emerged in the mating hives (Table 5). Some queens were lost due to drifting, which is a problem in mating yards due to the fact that hives are often placed close together with entrances oriented in the same direction (Laidlaw, 1979). Greater queen losses occurred in September and December (Table 5) caused by the Oriental Hornet (Vespa orientals).
240
YAACOV LENSKY and MICHAL DEMTER
The small number of drones in colonies during September 1980 resulted in the low incidence of acceptance of queens mated during this time. Most queens disappeared within three weeks of their introduction to full-sized colonies, probably because they were balled by workers (Table 6). Ruttner (1955) maintains that queens that mate in areas with few drones, receive only small amounts of sperm, and are killed by workers. It should be emphasized that queens mated at all other times of the year were accepted by colonies and survived for many months. It is possible that most of their deaths were due to our the hives during frequent inspections of February-April, 1981 (Table 6). The quality of queens mated at various times of the year did not differ greatly and honey yields were similar among colonies headed by queens mated throughout the year (41.31 + 1.42 kg/colony; queens ranged in age from 2-10 months). All queens increased their rate of egg-laying during February 1981, and by the end of March 1981 (20 days before the honey harvest), all colonies were similar in population size and brood area, which would explain the uniformity of honey yields. This finding refutes the general opinion held by beekeepers that queens younger than 7 months are not as productive as queens that are older. Bodenheimer and Ben-Nerya (1937) indicated that in Israel, both the rate of queen egg-laying and colony population density increase between January-April or May, depending on the region. To summarize, our results indicate that queens mate successfully throughout the year. In September one must overcome the natural lack of drones by recruiting them from a mating yard. Acknowledgements-We thank Mrs Martha Levinsohn for her excellent assistance. This work was supported in part by the Triwaks Fund. Mrs Michal Demter was the recipient of Leon Americus, D. Ben-Gurion, Israeli Beekeepers Association and Beniamin and Gavriel Triwaks Fellowships. We * are also grateful to Mr Gene Robinson for helpful chticism of the manuscript. REFERENCES Alber M., Jordan R., Ruttner F. and Ruttner H. (1955) Von der Paarung der Honigbiene. Z. Bienenforsch. 3, l-28. Barkan A. (1981) The effect of expanding the space on building of swarming queen cups and cells in honeybee (Apis mellifera L.) colonies. M.Sc. Thesis, 39 pp. Hebrew University of Jerusalem. Bodenheimer F. S. and Ben-Nerya A. (1937) One-year studies on the biology of the honey-bee in Palestine. Ann. appl. Biol. 24, 385403. Bol’shakova M. D. (1978). The flight of honeybee drones Apis mellifera (Hymenoptera, Apidae) to the queen in relation to various ecological factors. Entomol. Rev. 56, 53-56. Butler C. G. (1971) The mating behaviour of the honeybee (Apis me&era L.). J. Entomol. 46, 1-11. Drescher W. (1969) Die Flugaktivitlt von Drohnen der Rasse (Apis mellfira carnica L.) und (A. m. ligustica L.) in Abhlngigkeit von Lebensalter und Witterung. Z. Bienenforsch. 9, 39&409. Ebadi R., Garv N. E. and Lorenzen K. (1980) Effect of carbon dioxide and low temperature narcosis on honey bee (Aois mellifera L.). Environ. Entomol. 9, 144-147. Fletcher ‘D. J. C. “and Tribe G. D. (1977) Natural emergency queen rearing by Apis mellifera adansonii-II. In African Bees: Taxonomy, Biology and Economic Use (Edited by
Fletcher D. J. C.), pp. 132-140. Apimondia, Pretoria, South-Africa. Frisch Von K. (1967) The Dance Language and Orientation of Bees, pp. 331-465. Harvard University Press, Cambridge, Mass. Gary N. E. (1971) Observation of flight-experienced queen honey-bees following extra-apiary release. J. Apic. Res. 10, 3-9. Hammann E. (1958) Which takes the initiative in the virgin queen’s flight, the queen or the worker. Bee Wld. 39, 57-62. Koeniger N. and Wijayagunasekera H. N. P. (1976) Time of drone flight in the three asiatic honeybee species (Apis cerana, Apisjorea, Apis dorsata). J. Apic. Res. 15,67-71. Konopacka Z. (1968) Loty matek trutni pszczoly miodnej (Apis mellifera L.) Pszczel. Zesz. Nauk. 12, I-30. Kurennoi N. M. (1954) Flight activity and sexual maturity of drones. Pchelovodstvo, 31, 24-28. In Russian. Laidlaw H. H. (1979) Mating of the queen. In Queen Rearing, pp. 171-175. Dadant and Sons, Hamilton, Illinois. Laidlaw H. H. and Eckert J. E. (1962) Mating of the queen. In Queen Rearing, pp. 24-25. University California Press, Berkeley, Los Angeles. Lensky Y., Gassier P., Nutkin M., Delorme-Joulie M. and Levinson M. (1984) Pheromonal activity and fine structure of the mandibular glands of the honeybee drones. J. Insect Physiol. (In Press). Lensky Y. and Seifert H. (1975) Factors affecting swarming of bee colonies. Hassadeh 55, 632-636 (In Hebrew). Lensky Y. and Slabezki Y. (1981) The inhibiting effect of the queen bee (Apis mellifera L.) foot-print pheromone on the construction of swarming queen cups. J. Insect Physiol. 27, 313-323. Lindauer M. (1960) Time-compensated sun orientation in bees. Cold Spring Harbor Symp. Quant. Biol. 25, 371-377. List J. R. (1966) Smithsonian Meteorological Tables, p. 479. Smithsonian Inst. Washington, DC. Mackensen 0. (1947) Effect of carbon dioxide on initial oviposition of artificially inseminated and virgin queen bees. J. Econ. Entomol. 40, 344349. Medugorac I. and Lindauer M. (1967) Das Zeitgedachtnis der Bienen unter dem Einfluss von Narkose und sozialen Zeitgebem. 2. Vergl. Physiol.. 55, 450474.
Oertel E. (1956) Observation
on the flight of drone honey bees. Ann. Ent. Sot. Am. 49, 497-500. Pain J. (1961) Sur la pheromone des reines d’abeilles et ses effects physiologiques. Ann. Abeille 4, 73152, Pain J., Barbier M. and Roger B. (1967) Dosages individuels des acides Cito-9-&&m-2 oique et hydroxy-10-dec&re-2 oique dans les tetes des reines et des ouvrieres d’abeilles. Ann Abeille 10, 45-52. Renner M. (1960) The contribution of the honeybee to the study of time-sense and astronomical orientation. Cold Spring Harbor Symp. Quant. Biol. 25, 361-367. Renner M. and Vierling 6. (1977) Die Rolle des Taschendrtisenpheromons beim Hocheitsflug der Bienenkonigen. Behavioral Ecol. Sociobiol. 2, 329-338. Ruttner F. (1955) Einfache und mehrfache Paarung der KBnigin, erwiesen aus der Nachkommenschaft. Bienenvater 76, 5-10, 50-56, 1233127, I-59-164, 198-202. Ruttner F. (1956) The mating of the honeybee. Bee WZd. 37, 3-15. Ruttner F. (1966) The life and flight activity of drones. Bee Wld. 47, 93-100. Shoemaker H. H. (1947) Multiple mating in the queen honeybee. Am. Bee. J. 87, 19. Skowronek W. (1976) Biologia unasieniania sie matek pszczelich usypianych dwutlenkiem wegla. Pszczel. Zeszy. Nauk. 20, 99-115. Soczek Z. (1958) Wplyw neiktorych czynnikow na loty i kopulacje matek poszczelich. Pszczel. Zesz. Nauk. 2, 109-120.
Honeybee Taber S. (1964) Factors influencing the circadian flight rhythm of drone honey bees. Ann. Ent. Sot. Am. 57,
169-115. Taber S. (1974) Rearing and mating of queen and drone honey bees in winter. Am. Bee. J. 14, 18-19. Triasko V. V. (1951) Signs indicating the mating of queens. Pchelovodstvo 28, 2531 (In Russian). Triasko V. V. (1956) Repeated and multiple mating of queens. Pchelovodstvo 33, 43-50. (In Russian). Vierling G. and Renner M. (1977) Die Bedeutung des
mating
241
thghts
Sekretes der Tergittaschendtisen der Bienenkiinigin. Behavioral
fur
die Attraktivitlt
Ecol.
Sociobiol.
2,
185-200. Whitherell P. C. of normal and 65-75. Woyke J. (1964) honeybees. J. Woyke J. (1975)
(1972) Flight activity and natural mortality mutant drone honeybees. J. Apic. Res. 11, Causes of repeated
mating
flights by queen
Apic. Res. 3, 17-23. Natural
and instrumental
insemination
of
Apis cerana indica in India. J. Apic. Res. 14, 153-159.
0300-9629/85 $3.00 + 0.00 0 1985Pergamon Press Ltd
2299241,1985
Printed in Great Britain
MATING FLIGHTS OF THE QUEEN HONEYBEE (APIS MELLIFERA) IN A SUBTROPICAL CLIMATE YAACOV LENSKY and MICHAL DEMTER The Triwaks Bee Research Center, Hebrew University of Jerusalem, Faculty of Agriculture, 76100 Rehovot, Israel (Received 16 July 1984) Abstract-l.
Mating behaviour of queens and drones and mating success were studied throughout the year. 2. Worker bees directed virgin queens to leave the hive and take mating flight. 3. Cloudiness above 7 octavas and wind velocity above 3.9m/sec. delayed queen and drone flights. 4. Duration of queen tlights was reduced at 15-20°C and wind velocity of 2.63.9m/sec. 5. The peak of flight activity hours of queens and drones overlapped throughout the year. 6. CO,-treatment of queens resulted in a delay of mating flight and in an enhancement of egg-laying. 7. The queens successfully mated throughout one year. 8. Colonies headed by 2-lo-month old queens yielded similar honey crops.
INTRODUCXION
Honeybee queens and drones mate during fights which generally occur on warm and sunny days. Drones fly to established drone congregation sites (Ruttner, 1966) and are attracted to these sites by pheromones of unknown chemical nature which are secreted by the drone’s mandibular gland (Lensky et al., 1984). At the present time it is not clear who is attracted to whom first, drones or queens. It is known that drones are attracted to queens at distances greater than 50 m by a pheromone produced in the queen’s manidbular gland, E-9-oxodec-2-enoic acid. At distances of up to 3Ocm drones are attracted to queen pheromones (chemical identity not known) from Renner’s glands, which apparently trigger copulation (Butler, 1971; Renner and Vierling, 1977). The queen mates with several drones during her mating flights. Workers are attracted to the 4-6-day old queen due to the secretion of queen pheromones from the mandibular glands (Pain, 1961). Workers participate passively in the queen’s mating llight, by restricting the queen’s movements specifically in the direction of the hive entrace, and by emitting Nasanov gland’s scent inside and outside the hive (Fletcher and Tribe, 1977; Hammann, 1958; Ruttner, 1956). This worker behavior continues until the queen begins oviposition (Hammann, 1958). The queen leaves for her first mating flight generally when 5-6 days old (Alber et al., 1955; Fletcher and Tribe, 1977), while drones’ mating flights occur 7-9 days after emergence (Drescher, 1969; Kurennoi, 1954; Oertel, 1956). Queens fly an average of 2-5 flights (Alber et al., 1955; Fletcher and Tribe, 1977; Ruttner, 1956), and drones 25 ilights (Whiterell, 1972). There are two types of drone and queen flights: short orientation Bights, lasting l-10 min, and longer mating flights, lasting 5-27 min (queen) (Fletcher and Tribe, 1977; Soczek, 1958; Woyke, 1975), or an average of 33 min (drones) (Drescher, 1969; Whith-
erell, 1972). Although honeybee mating has been extensively studied, the timing of queen and drone flights has not been examined simultaneously. All that is known is that queens and drones leave the hive during the afternoon hours, the greatest activity being between the hours of 14.00-16.00 (Bol’shakova, 1978; Ruttner, 1956; Soczek, 1958; Taber, 1964; Woyke, 1975). Taber (1964) suggests that climate does not influence mating behavior. In contrast, most researchers believe that climate does influence mating behavior, with mating occurring above 20°C and during times when wind speed is less than 4-5 m/set on clear, cloudless days (Alber et al., 1955; Bol’shakova, 1978; Drescher, 1969; Fletcher and Tribe, 1977; Oertel, 1956; Ruttner, 1955; Soczek, 1958; Taber, 1964). Investigators have not pinpointed the climatic factors associated with mating. Research on the conditions and, factors that influence honeybee mating behavior has both applied and theoretical value. Queen rearing and mating in Israel takes place during March-April and in September. It is generally accepted that during other months, successful mating is not possible, however no scientific studies prior to the present research have been undertaken in Israel to verify this contention. Queen replacement in the commercial apiary is an important aspect of successful beekeeping. Because of the queen’s high egg-laying rate it is important to requeen annually in order to maintain high adult population levels and to prevent swarming (Barkan, 1981; Lensky and Seifert, 1975; Lensky and Slabezki, 1981). The time of requeening depends on the supply of commercially reared queens, which is mostly in the spring and to a lesser extent in September. Because of the rapid population growth in the spring and pressures of colony work associated with swarm control and honey production it is hard for the beekeeper to requeen during the spring. In addition there is a loss of queens throughout the year for various reasons. Year-round availability of queens may solve these above-mentioned problems. 229
CBPA 8 1/Z-B
230
YAACOV LENSKY and MICHAL DEMIER Table I. Percentage of &gin queens accepted in mating nuclei Date of introduction of queen cells
Date of emergence of queens
No. mating nuclei
Accepted queens (%)
1980 6 June 17 July 14 September 5 October 15 November
1 June 19 July 18 September 6 October 15 November
I 12 15 17 15
86 92 87 59 87
1981 19 January 18 February 15 May
20 January 19 February 17 May
17 11 14
53 64 86
The goals of this study were to: (1) study the behavior of the workers and queen from queen emergence to the onset of oviposition in glass-walled observation hives and in mating colonies; (2) determine whether there exists an overlapping of the hours during which queens and drones fly throughout the year; (3) quantify the number and duration of queen flights throughout the year; (4) describe the climatic conditions associated with successful mating, and; (5) determine the times of the year during which queens can be reared and mated in Israel, based on the analysis of mating success and queen quality by measurement of honey yields. MATERIALS
APllD METHODS
Queen rearing Queen honeybees (Apis mellifera L. var. ligustica) were reared each month from Italian stock brought from the U.S. Cell builders were either queenless or queenright with the queen confined to the lower super. Cell builders were fed in August and January with a 60% sugar solution for 2-5 days before receiving the grafted larvae. In July, August, September, November and February cell builders were fed a 40-60x sugar solution throughout the queen rearing process, until the day on which cells were sealed.
colonies and the proportion in Table 1. Observations period
of accepted
queens is indicated
of queen and worker behavior during the mating
Two glass-walled observation hives were used. Queens cells were introduced on October 9, 1980 and queens began oviposition on October 30, 1980. Observation began upon queen emergence on October 11, 1980, and lasted until October 30, 1980, when queens began oviposition. The behavior of workers towards the queens was examined throughout the observations every several hours. Continuous observation of worker and queen behavior were made between 12.30-15.30 hr (local time) every day. Observations
of queen mating jights
Drone traps were installed at the entrance of the mating hives in order to examine the parameters associated with mating. The trap blocked the entrance of the hive, preventing the exit of the queen. The mating success of queens held in mating colonies that were fitted with drone traps relative to queens held in control colonies was examined by comparing the percentage of successfully mating queens and the number of days between queen emergence and the onset of oviposition (Table 2). Since the presence of the drone trap did not delay egg-laying activities, they were used in subsequent experiments. They were removed after the queen went out on a mating flight. Observations were conducted at the Triwaks Bee Research Center, Rehovot, during June-July, September-November, 1980; January-February and May 1981.
Drone rearing Because there are few drones in colonies during the fall and winter under natural conditions, we introduced 2 frames with a drone foundation in each of 5 colonies on June 24, 1980. In follow-up observation, however, we found that only 4 frames had eggs. There was a positive correlation between the number of combs with eggs and the length of time they had been in the hive. From February to April 1981, SO-100% of the combs had drone brood. Thus, in order to rear drones, frames with a drone brood foundation must be installed in hives in the spring. A4ating hives Observations of seasonal mating patterns were made on mating hives (50 x 25 x 24cm), each holding 4 frames: 2 brood, 1 honey, and 1 pollen. The number of mating
Observation
of drone mating jights
Observations were made of 5 colonies whose populations covered at least 10 frames. Drone traps were installed at hive entrances and observations were made 5 days per month, overlapping the days on which queens were observed. Examinations
of the onset of oviposition
On the day after the queen stopped making long mating flights the presence of eggs was ascertained. Daily examinations were continued until eggs were seen in all mating colonies or until 14 days had elapsed since the queen stopped making mating flights. Fourteen days after the appearance of eggs the brood was checked to determine whether the eggs had been fertilized.
Table 2. Onset of egg-laying in queens maintained in hives blocked by a queen trap and in hives with free entrances (June&&ember. 1980) Mating nucleus Restricted entrances Free entrances
No. nuclei 34 17
Laying queens (%) 41 67
No. days from emergence to egg-laying 9.00 * 0.05 9.14 * 0.09
231
Honeybee mating flights Carbon dioxide anesthetization of virgin queens
Queen cells reared from larvae grafted on 29 February
a
Hive no.
~
Hive no. 2
1980 were removed from the cell-builders 10 days after grafting and placed in an incubator (32°C 60% R.H.). Upon emergence they were anesthetized with carbon dioxide for thirty seconds and introduced into mating colonies. They were then observed from 10 October to 13 October 1980. Imtroduction of queens mated in mat&g colonies into fill-sized colonies To check the quality of queens mated at various times of the year, a random sample of these queens was transferred to each of 3-4 frame colonies. Population growth and egg laying rates were checked at random from queen introduction to 10 February, 1981. From 10 February 1981 to 15 April 1981, examinations were made every two weeks; supers were added and frames of brood raised according to need. Honey yields were established on 21 April 1981. Equipment for the measurement of climatic conditions A record of climatic conditions on each day of observation was made every half hour. The following equipment was usedz (1) ~e~ometer-l~lOO°C (Phoenikia, Israel) (2) anemometer~Casella, London) (3) sol~meter~ipp and Zonen, Delft, Holland).
cl R”,;“,:;g,d”f workers
Worker behavior, as related to the leaving of the queens on a mating flight, was investigated in observation and mating hives. hives (October
1980)
Queen cells were introduced into two glass-walled hive colonies on 8 October 1980. Worker and queen behavior was observed for 20 days after the emergence of the queen, or until the onset of oviposition. Young queens walked around and fed themselves, and were not attended to by workers for the first three days. Beginning on day 4, workers did feed and antennatethe queen (Fig. 1). From day 5 to the beginning of the queens’ oviposition (7 and 12 days after queen emergence, respectively) distinct worker behavior was observed daily between the
Activity
of
Queens
Running
of
Workers
Running
of
Queens
Queen’s
vibratory
Exposure
Mating Removal
of
and
Observation made in front of entrance to mating hives (June 198~May 1981)
Intensive worker flight activity preceeded the queen’s exit by 50-60min. Some workers stood on the drone trap and exposed their Nasanov glands. Queens leaving the mating hive were caught in the drone trap, from which they moved to the second super of the colony, accompanied by workers. Intense
Workers
dance
scent
gland
mating
sign
a
by
workers
t
A’
’
-
flight of
Pzzz--=-+
D B
z/z
z:
Of
hours of 12.30-16.30. During this time some workers ran to and from the entrance repeatedly (Figs 2-10). Prior to exiting for a mating flight, the queen would participate in this running 15-30 min after it began. The queen interrupted this running every 5-lOmin, exposed the intersegmental membranes of her tergites and groomed her abdomen with her hind legs (i.e. vibratory dance). Part of the workers tried to direct the queen away from the hive entrance, while others stood near the entrance exposing their Nasanov gland during the 10 min prior to the queen’s exit. Workers removed the drone’s penis from the newlymated queen (Fig. 2).
Colony behavior during the mating period
in glass-walled
The onset egg-laying
Fig. 1. Behaviour of worker bees towards queens from 4th day after emergence till the onset of egg-laying. Two colonies in observation hives were used (Rehovot, October 1980).
RESULTS
Observations
Of mating flights
Days
1
I
I
Pig. 2. Behaviour of worker bees and a queen bee before and after mating flights, as observed in two observations hives (Rehovot, October 1980).
YAACOVLENSKYand MICHALDEMTER
232
01 II-16 J”“e
I
I
I
24-2s JULY
17-M NO”.
21-25
Sept.
I 23-30 Jan
I
1
23 Feb 5 March.
0
20-26
May 1981
1980
Fig. 3. Seasonal effect on queens’ first mating flight and on the total number of mating flights (Rehovot, 198&1981).
worker flight activity declined after the queen was released from the drone trap and flew off. Two to five minutes prior to the return of the queen, workers crowded the entrance of the hive and released Nasanov pheromone. When the queen alighted at the hive entrance she was accompanied by workers, and if she returned with a penis in her vagina, they tried to remove it. The workers at the hive entrance entered the colony within 5 min of the queen’s entrance. The influence of season on queen matingflights: timing and number The date of the first mating flight was considered to be the first date on which the queen was found in the trap or second super (via the trap). To establish the number of flights, traps were returned to the hive entrances after the queen returned from her flight. Results were calculated as follows: (1) Mean date of first mating flight = X7 day of first flight n n = number of queens.
F= Total 0 = Total
no. of flights no. of Queens
(2) Mean number of flights per queen = C< all frights n f = number of flights, n = number of queens. From the results in Fig. 3 one sees that in the months of June-November 1980 and May 1981 queens took their first mating flight 5-6 days after emergence and flew an average of 2-3 flights. During January and February 1981 queens took their first flight 8-9 days after emergence, and flew an average of 11-13 flights. Duration of mating Jlight Duration of mating flight was calculated from the time the queen was released from the entrance trap and took off on a flight to the time she alighted on the hive entrance. The number of observations of duration of mating flights does not correspond to the number of mating flight, because some returns were not seen. These observations indicate the two types of queen flights exist: short and long. Queens returned
qShort Long
flights fUghts
(l-5 mini 05 min)
z E
12
1980
1981
Fig. 4. Seasonal effect on the duration of queens’ short and long flights (Rehovot, 1980-1981).
233
Honeybee mating flights
23
Feb-
5 March Hz5
/ 1981
17-24 Nov. 1980 H=lO
d
24-29 July
1980
“=B
II-16
June
1980
H = No.
Hr
of
hives
of flight
Fig. 5. Seasonal effect on the frequency and the hours of queens’ mating flights (Rehovot, 1980-1981).
from long flights mated, as evidenced by the usual appearance of the penis in the queen’s vagina. The results in Fig. 4 show that:
(1) During all months queens took at least one long flight; (2) During all months queens took more long flights than short flights, except in February; (3) Short flights were l-5 min in duration, whereas long flights were l&15 min in duration.
In the winter and spring the peak occurred between 13.00-14.30 hr, and in the summer and fall this period was between 14.00-15.30 hr. (3) The total number of flights made by a queen varied with the month. During February the total number of queen flights was much larger than in other months. Climatic conditions also influenced the lota number Of flights’ The average time at which mating flights began was determined in the following way:
Time of day at which mating took place
zc;2
-
Results are summarized in Fig. 5. They show that: (1) Queens fly for 2-3 hr every month. In winter and early spring, queen flights occurred 1.5 hr earlier than flights in spring and summer. (2) In each month there was a period of peak queen flight activity, during which 50% of the queens flew.
F-II 16-Q=
I*_
I ‘,I-16 June
I 21-25 sap-t. 1980
rfrSE
X = mean time (hr) at which each queen began her mating flight, n = number of queens. The mean time at which mating flights began is indicated in Fig. 6. In January flights occurred ear-
5
I 24-25 J”lY
n
I 17-24 NW.
F = Total
no. of flights
0
Queens
= No. of
I 23-30 Jon.
I 23 Feb.5 March 198 I
I 20 -26 MOY
Fig. 6. Mean (2 SE) queens’ mating %ght hours throughout the year (Rehovot, 1980-1981).
YAACOV LENSKY
234
Table 3. Position of the sun during Date
20-26 Mav
15.39f0.13 14.41 ir 0.12 14.30 * 0.08 13.37 * 0.09
11.06 9.51 9.02 7.24
20.55 19.59 20.51 20.58
48.82 49.05 48.67 57.89
13.00 +_0.10
6.22
19.52
53.01
196.31
13.24 + 0.07 14.30 + 0.01
7.13 9.50
19.47 19.55
43.21 36.04
206.57 260.62
(1) Number of hours from sunrise to the time at which queens took flights. (2) Number of hours from sunset to the time at which queens took flights. (3) The angle of zenith based on the following formula (List, 1966): COST cos* sin6 sin4
= angle of zenith, = declination of sun, = meridean, = angle of hour.
(4) Sun azimuth was calculated according to the following formula (List, 1966) cos 6 sin * sin CI= sin z CI= sun azimuth. The results in Table 3 show that: (1) Throughout after sunset.
Fig.
flights
Angle of zenith
Position of the sun during the time at which mating flights occurred Does the position of the sun influence the time at which mating flights occur? To answer this question the following calculations were made:
z 6 4 4
queens’ take off for their mating Hours from sunset
Bight (hr)
liest in the day, (13.00 +_0.09 hr) and in June latest (15.39 f 0.15 hr).
cos z =cos6
MICHAL DEMTER
Hours from sunrise
Mating
1980 11-16 June 2&29 July 21-25 September 17-24 November 1981 23-30 January 23 February-5 March
and
the year queens fly 20.19 + 0.12 hr
7. Mean drones’ flight hour throughout on five beehives
during
Azimuth
of sun
266.01 259.07 237.41 211.22
(2) The angle of zenith during flight periods was between 36.04-57.89”. (3) The sun azimuth during ilight periods was between 196.31-266.01”. The timing of drone flights The purpose of these observations was to determine if drones engage in mating flights at the same times as queens during the entire year. Traps were installed on 5 colonies chosen at random. Drone and queen flights were observed on the same days. The number of drones trapped in the second story was determined daily at half-hour intervals, after which time they were released. At the end of each day’s observations, all the traps were removed except for one, which was kept to check for early drone flights the following day. Calculations of drone tlight activity were made according to the general average of 5 days of observation which were picked at random from all the observations of each month. The results in Fig. 7 show that: (1) Drones take fight 24 hr daily. In the winter and spring the timing of their flights is earlier (10.30-l 1.30 hr), than in the summer and fall (11.30-12.30 hr). (2) The peak period of activity, during which more than 50% of the drones flew, occurred between 12.00-13.30 hr in the winter and spring, and 13.30-15.00 hr during summer and fall. Throughout
the year. Each point represents five consecutive days (Rehovot,
a mean of observations 1980-1981).
made
235
Honeybee mating flights 6 0
Drones
tza Queens
127 12 t
1981
1980
Fig. 8. Overlapping of flight hours peaks of queens and drones throughout the year. Above the bars; the number of individuals exiting from a beehive during the peak hours; beneath the bars; the total number of individuals that took flights (Rehovot, 1980-1981).
the year drone ilights were not observed
from sunrise to 10.00 hr although worker flight was evident. (3) The number of drones taking flights varied with the month. In September the minimum number of
Climatic jligh ts
drones took flights, and in May-June the maximum number was attained (70 drones per colony). Peak flight periods for drones and queens (the period during which more than 50% of the individuals took Bights) are presented in Fig. 8. These results indicate that there is at least a 30min overlap in the two periods of the year. Drone flight periods began and ended about 30 min before queen flight periods began and ended.
than 3.9 mjsec (Fig. 9a: days 7 and 8 post-emergence; Fig. 9b: day 5 post-emergence). Flights also did not take place on rainy days (Fig. 9b: days 6-7 postemergence). From Fig. 9a we see that on day 4 post-emergence only drone flight occurred, because queens do not take their first flight until they are 5 days old.
Injuence
of climatic conditions on queen and drone
frights
The influence of climatic factors such as temperature, cloudiness, wind speed and global radiation on queen and drone flight was examined from June 1980-May 1981. Table 4 indicates that the climatic conditions that existed during the four seasons of the study period did not influence queen and drone flight activity. To summarize: Queen and drone flights took place without disturbance at temperatures ranging from 2635”C, wind speed not higher than 2.6 mjsec and cloudiness lower than 2 octavas. On the other hand, in November 1980, and February and May 1981 the prevailing climatic conditions did inhibit queen and drone flight or increased the number of short queen flights (Figs. 9a,b and lOa,b).
Table 4. Weather Date 11-16 June 24-29 July 21-25 September 8-13 October *CO, anaesthetized.
Mating 15.39 14.41 14.30 14.33
conditions
flight (hr) kO.13 * 0.12 * 0.08 f 0.03
during
Temp (“C) 26-31 29-35 29-33 21-32
conditions
that
delayed
queen and drone
Queen and drone flight did not occur at cloudiness levels above 7 octavas and at wind speeds greater
Climatic conditions that increased the number of short queen Jights Queens that flew during the period 23 February-5 March 1981, took about twice as many short flights on days 9-13 post-emergence as they did on days 14-15, presumably due to the low temperatures that were recorded on the later days (15-18°C; Fig. 10a). A similar rise in the number of short flights occurred during 21-25 May 1981 with a 3-fold increase in short flights evident on days 5-8 post-emergence vs day 9. This increase due to strong winds, 2.6-2.88 mjsec was probably due to the fact that queens take short orientation flights on their first day out of the hive.
Success of mating throughout the year Colonies were examined daily for the presence of eggs beginning 14 days following the last day of
queen flight. The mating success of queens is presented in Table 5. These results show that there
queen and drone mating Wind velocity 0.4-1.0 1.17-1.82 1.19-2.59 1.23-2.41
(m/set)
flights
(Rehovot, Cloudiness (octavas) l&l o-2 o-o.5 o-1
1980) Global radiation (cal/cn?) 56-14 45-58 45-58 20-53
236
YAACOV LENSKY and MICHAL DEMTER
Days
from
emergence
(Queens)
(4
01
I 4
i 6
I
_
11
*
Doys from
11 10
1’ 12
emergence
14
(Queens)
(b) Fig. 9. The effect of cloudiness and wind velocity on the tlight activity of queens and drones. (a) 13.30hr, 17-23 November 1980. (b) 13.30hr, 23 February-3 March 1981. (Rehovot). was lOO’%mating success during all months except September (70%). Despite these results, there were less mated queens reported than there were mating hives. These losses occurred during:
days old, and were than introduced into mating hives. Observations of queen flights were made throughout the mating period until the onset of oviposition. The results in Fig. 12 indicate that:
(1) September 1980 and January and February 1981-65% queen loss after mating; (2) 3uly and November 1980 and May 1981-51% queen loss; (3) June 1980-39’~ queen loss.
(1) Anaesthetized queens took their first flight 7 days after emergence, while untreated queens took their first flight on day 5. Thus, carbon dioxide anaesthetization caused a delay of 2 days in the timing of the first mating flight. (2) Anaesthetized queens flew 44min later than their expected time in October (14.4 +_0.07 hr, vs 14.03 hr, see Fig. 6). (3) Anaesthetized queens took their first flight earlier than queens usually do in September and November.
The timing of the onset of oviposition among mated queens throughout the year is summarized in Fig. 11. From these results we see that during May, June, July and September oviposition began 9-11 days after emergence, while in November, January, and February oviposition began 14.5-19 days after emergence. Two to six days elapsed between the last mating flight and the onset of oviposition. The effect of carbon dioxide anaesthetization of virgin queens on the timing of mating flights and oviposition The purpose of this experiment was to investigate the possibility of shortening the mating period by administering carbon dioxide anaesthetization to virgin queens. Queens were treated for 30 set when l-3
The quality of queens mated throughout the year The following factors were evaluated as a measure of queen quality: egg-laying rate, colony population growth, and honey yields. After it had been determined that the queen had mated and had begun to oviposit she was transferred from the mating hive to a full sized colony. Beginning two weeks after queen’s introduction, (10 February-l 5 April 198 1) colonies
Honeybee mating flights -3
*O
(A)
Days from emergence to oviposition ~~TI;y;~$no$ flight 4
Q = No. of laying Queens 75
-2-
5
‘:: 2
i
_, .g
50
8
25-0
Days
-A4
fromemergence
(a) 3
-25
: 0
(A)
1980
23 Ft!b5 MO rch 1981
20-a May
Fig. 11. The onset of oviposition by queens mated during different seasons (Rehovot, 1980-1981).
-J22
Fig. 10. The effect of wind velocity and temperature on the frequency of queens’ short flights. (a) 13.30hr, 23 February-5 March 1981; (b) 14.30hr, 21-25 May 1981 (Rehovot).
headed by the recently mated queens were evaluated as follows: density of adult colony population, number of brood frames, and honey yields after the citrus honey Aow (ending on 21 April 1981). The percent survival of introduced queens throughout the year is presented in Table 6. From the results, it is apparent that the percentage of queen acceptance was relatively low during the months of September, November and January. Rejected queens were apparently balled by the colony’s workers. Queens that mated in November and Jan-
uary survived until April 1981; they disappeared as a result of frequent inspections. The results of egglaying rate, population growth and honey yields are presented in Fig. 13. All queens, regardless of the month of their mating, showed a 3-fold increase in egg laying rate and colony population from February to April. At harvest time, all colonies contained a similar number of brood frames and bees. Furthermore, honey yields were similar (41.31 5 1.42 kg/colony) among all colonies, regardless of the month the queens mated. It is important to emphasize that queens that mated in November and December were held in queen banks and introduced to colonies on 10 February 1981; these queens headed coionies that were just as productive as those headed by queens mated during the rest of the year.
DISCUSSION
Queen and worker behavior during the mating period
Observation of glass-walled and mating hives revealed the role played by workers in directing the queen to leave the hive for a mating flight. The interaction between queen and workers is illustrated in Fig. 1. Queen and worker behavior prior to queen
Table 5. Acceptanceof queens in nuclei and their mating SUCCESS throughout the year
Month
Acceptance in nuclei No. accepted q”&%lS No. cofonies
1980 June July September November 1981 January February Mav
*yeLaying queens =
Mating flights No. leaving No. returning queens queens
No. iaying queens ._-_____-
Oviposition after flights No. laying queens *Fertilized ___ No. colonies queens (%I
I 12 15 15
6 11 13 13
5 8 11 10
5 6 7 7
5 6 5 7
100 100 71.43 100
0.71 0.50 0.33 0.47
17 11 14
9 I 12
6 5 I
6 4 7
6 4 I
100 100 100
0.35 0.36 0.50
No. laying queens x 100. No. queens returned from mating flights
YAACOV LENSKY a
September
0
October
m
November
(CO,
0 = No. of Queens
from
Days from
Fig. 12. The effect of CO,-anaesthesy of virgin queens on their mating flights and on the onset of oviposition. September-November, Controls (Rehovot, 1980). mating has been observed by Hammann (1958), Ruttner (1956), and Triasko (1951), but the chronological order of these behavioral events was not specified. Our results indicate that workers begin directing the queen toward the hive entrance about 60 min prior to the queen’s exit and release Nasonov scent at the hive entrance for 10-15 min afterwards (Fig. 2). Also, the above mentioned investigators did not point out the pheromonal connection between queen and workers: The queen exposes the intersegmental membranes beside her Renner glands while participating in the “worker run” during the 45 min prior to queen flight (Fig. 2). The observation of mating hives completes the behavioural picture begun with the observation of the glass-walled hives, revealing the many worker flights and the workers’ accompaniment of the queen at the hive entrance. This behavior has not been previously described. Time of day at which matingflights occured throughout the year
Our observations revealed that throughout the year, there is an overlap of queen and drone daily mating fight periods during the afternoon. Mating flights were not observed in the morning hours (Figs 5,7 and 8). These findings suggest that queen matings can occur throughout the year in Israel. Even though drones stopped flying 30min earlier than queens during the months of June, September, November, January and February (Fig. 8), they were still in the
and
MICHAL DEMTER
air when queen flights took place. Drone mating flights average 33 min in duration (Drescher, 1969: Whitherell, 1972; Woyke, 1975), while queen mating flights last from 10-15 min (Fig. 4). This overlapping of queen and drone mating flights, as well as the timing of these flights throughout the year has also not been previously reported. From other studies it appears that in various climates and at various latitudes, queens and drones take mating tights between 12.00-17.00 hr, with maximum frequency between 14.00-16.00 hr (Alber et al., 1955; Bol’shakova, 1978; Drescher, 1969; Koeniger and Wijayagunesekera, 1976; Soczek, 1958; Taber, 1964; Whitherell, 1972; Woyke, 1975). Most queens fly at a defined hour which changes by 15-45 min every month (Fig. 6). This variation suggested that meteorological conditions may influence queen flight, via the workers. Our results indicate that queens fly 20.19 + 0.12 hr after sunset (Table 5). Taber (1964) found that as day length increases, drone flight is delayed. It is known that field bees orient to food sources according to the sun. Frisch (1967) and Lindauer (1960) explain that this orientation is due to the zenith position. Renner (1960) suggests that honeybee orientation is based on the sun azimuth position. Our calculations indicate that queen fight occurs when the zenith angle is 35-60” and when the azimuth angle is between 200-270” (Table 5). Gary (1971) suggested that queens released at distances of up to 1600 m were able to orient and return to their mating hive during the morning hours, even though they generally fly in the afternoon. The findings of Taber (1964), Gary (1971) and our results together suggest that the time of day at which queen flight occurs depends on day length, while fight orientation is based on sun zenith and/or sun azimuth angle. Influence of climatic conditions on mating flights of queens and drones throughout the year
Climatic conditions do affect queen and drone mating flights. During rainy days, days in which cloud cover was greater that 7 octavas, and/or days in which wind speed measured greater than 3.9 m/set, queen and drone flights did not take place. On the other hand, no effect of climate on the time of day at which mating flights occur was found, in contrast to Ruttner’s proposition (1956) that queen flight occurred during the time of day of maximum temperature, and to Taber’s supposition (1964) that during cold days drones fly earlier in the day. Mating tights took place throughout the year at temperatures ranging from 15°C (February) to 35°C (July). Temperature did not affect mating flight activ-
Table 6. Survival of mated queens Mating flight (month) 1980 JUXK! July September October November 1981 January
No. queens introduced into colonies
Introduction of mated queens (date)
No. queens remaining till 15 April 1981
Survival (“/,)
4 5 3 2 6
20.6 14.8 1.10 1.11 10.2
4 5 1 2 5
100 100 33 100 83
3
10.2
2
66
239
Honeybee mating flights
March
April
Fig. 13. The effect of queens’ mating date on developing and adult worker bee population and on honey yields of a bee colony. ity, in contrast to the results of Bol’shakova (1978), Oertel (1956), and Ruttner (1956), who maintained that mating flights do not occur at temperatures less than 19°C. Our research indicates that low temperatures (between 15-20°C) influence the length of queen flights. Temperatures of 15-20°C and wind speeds between 2.6-2.88 mjsec resulted in an increase in the number of short queen flights, during which mating does not occur (Fig. 10). The increase in number of short queen flights may be due to the fact that queens must mate with about 10 drones in order to fill the spermatheca (Triasko, 1956; Woyke, 1964). At lower temperatures and greater wind speeds there are less chances of mating (Alber et al., 1955). Reports of the number of queen flights (Fletcher and Tribe, 1977; Konopacka, 1968; Kurennoi, 1954; Woyke, 1975) and on their duration (Alber et al., 1955; Shoemaker, 1947; Triasko, 1951) indicate great variation, probably because the studies were conducted under different climatic conditions, not specified by the investigators. From our results it is apparent that as the number of days increased during which poor weather conditions inhibited mating flights both mating and the onset of oviposition were increasingly delayed (see Fig. 11; Taber, 1974). To summarize, during the months of November 1980, and February and May 1981 (Figs 9 and lo), the climatic conditions inhibited mating, however, they did not prevent or reduce the incidence of mating nor lower queen quality, as compared with matings at other times of the year. This conclusion is in contrast to Laidlaw and Eckert (1962) and Ruttner (1955). Influence of carbon dioxide queen mating period
anaesthetization
on the
Carbon dioxide anaesthetized queens took their first mating flight 2 days later than control queens, but oviposition began 2 days earlier. Anaesthetized queens took mating flights 44min later in the day than the other queens (Fig. 12). In constrast to our results, Skowronek (1976) reports that carbon
dioxide anaesthetization causes queens to delay their mating flights by one week. This delay may be caused by a decreased release of 9-oxo-trans-2-decenoic acid from the mandibular glands of anaesthetized queens (Pain et al., 1967). This pheromonal release causes workers to be attracted to the queen (Vierling and Renner, 1977), since the workers are in closer contact with the queen, she leaves on her mating flight at a younger age (Hammann, 1958; Harbo, 1971; Medugorac and Lindauer, 1967). Carbon dioxide anaesthetization of workers also results in a decrease in the production of mandibular gland compounds, apparently because carbon dioxide treatments affect corpora allata activity (Skowronek, 1976). According to Medugorac and Lindauer (1967), carbon dioxide anaesthetization influences the worker’s biological clock, which may also explain the delay in queen mating flights (Fig. 12). Carbon dioxide anaesthetization enhances oviposition among artificially inseminated queens (Mackensen, 1947). We also observed that carbon dioxide treated queens began to oviposit at a younger age (a smaller interval between the last mating flight and oviposition). Carbon dioxide anaesthetization of field bees results in a decrease in longevity, but does not affect their sense of orientation (Ebadi et al., (1980). Treated queens flew mating flights, mated, returned to their colony and began to oviposit, confirming these results (Fig. 12). Quality of queens mated throughout
the year
During most of the year 100% of the queens successfully mated, but the number of laying queens was different from the number of queens that emerged in the mating hives (Table 5). Some queens were lost due to drifting, which is a problem in mating yards due to the fact that hives are often placed close together with entrances oriented in the same direction (Laidlaw, 1979). Greater queen losses occurred in September and December (Table 5) caused by the Oriental Hornet (Vespa orientals).
240
YAACOV LENSKY and MICHAL DEMTER
The small number of drones in colonies during September 1980 resulted in the low incidence of acceptance of queens mated during this time. Most queens disappeared within three weeks of their introduction to full-sized colonies, probably because they were balled by workers (Table 6). Ruttner (1955) maintains that queens that mate in areas with few drones, receive only small amounts of sperm, and are killed by workers. It should be emphasized that queens mated at all other times of the year were accepted by colonies and survived for many months. It is possible that most of their deaths were due to our the hives during frequent inspections of February-April, 1981 (Table 6). The quality of queens mated at various times of the year did not differ greatly and honey yields were similar among colonies headed by queens mated throughout the year (41.31 + 1.42 kg/colony; queens ranged in age from 2-10 months). All queens increased their rate of egg-laying during February 1981, and by the end of March 1981 (20 days before the honey harvest), all colonies were similar in population size and brood area, which would explain the uniformity of honey yields. This finding refutes the general opinion held by beekeepers that queens younger than 7 months are not as productive as queens that are older. Bodenheimer and Ben-Nerya (1937) indicated that in Israel, both the rate of queen egg-laying and colony population density increase between January-April or May, depending on the region. To summarize, our results indicate that queens mate successfully throughout the year. In September one must overcome the natural lack of drones by recruiting them from a mating yard. Acknowledgements-We thank Mrs Martha Levinsohn for her excellent assistance. This work was supported in part by the Triwaks Fund. Mrs Michal Demter was the recipient of Leon Americus, D. Ben-Gurion, Israeli Beekeepers Association and Beniamin and Gavriel Triwaks Fellowships. We * are also grateful to Mr Gene Robinson for helpful chticism of the manuscript. REFERENCES Alber M., Jordan R., Ruttner F. and Ruttner H. (1955) Von der Paarung der Honigbiene. Z. Bienenforsch. 3, l-28. Barkan A. (1981) The effect of expanding the space on building of swarming queen cups and cells in honeybee (Apis mellifera L.) colonies. M.Sc. Thesis, 39 pp. Hebrew University of Jerusalem. Bodenheimer F. S. and Ben-Nerya A. (1937) One-year studies on the biology of the honey-bee in Palestine. Ann. appl. Biol. 24, 385403. Bol’shakova M. D. (1978). The flight of honeybee drones Apis mellifera (Hymenoptera, Apidae) to the queen in relation to various ecological factors. Entomol. Rev. 56, 53-56. Butler C. G. (1971) The mating behaviour of the honeybee (Apis me&era L.). J. Entomol. 46, 1-11. Drescher W. (1969) Die Flugaktivitlt von Drohnen der Rasse (Apis mellfira carnica L.) und (A. m. ligustica L.) in Abhlngigkeit von Lebensalter und Witterung. Z. Bienenforsch. 9, 39&409. Ebadi R., Garv N. E. and Lorenzen K. (1980) Effect of carbon dioxide and low temperature narcosis on honey bee (Aois mellifera L.). Environ. Entomol. 9, 144-147. Fletcher ‘D. J. C. “and Tribe G. D. (1977) Natural emergency queen rearing by Apis mellifera adansonii-II. In African Bees: Taxonomy, Biology and Economic Use (Edited by
Fletcher D. J. C.), pp. 132-140. Apimondia, Pretoria, South-Africa. Frisch Von K. (1967) The Dance Language and Orientation of Bees, pp. 331-465. Harvard University Press, Cambridge, Mass. Gary N. E. (1971) Observation of flight-experienced queen honey-bees following extra-apiary release. J. Apic. Res. 10, 3-9. Hammann E. (1958) Which takes the initiative in the virgin queen’s flight, the queen or the worker. Bee Wld. 39, 57-62. Koeniger N. and Wijayagunasekera H. N. P. (1976) Time of drone flight in the three asiatic honeybee species (Apis cerana, Apisjorea, Apis dorsata). J. Apic. Res. 15,67-71. Konopacka Z. (1968) Loty matek trutni pszczoly miodnej (Apis mellifera L.) Pszczel. Zesz. Nauk. 12, I-30. Kurennoi N. M. (1954) Flight activity and sexual maturity of drones. Pchelovodstvo, 31, 24-28. In Russian. Laidlaw H. H. (1979) Mating of the queen. In Queen Rearing, pp. 171-175. Dadant and Sons, Hamilton, Illinois. Laidlaw H. H. and Eckert J. E. (1962) Mating of the queen. In Queen Rearing, pp. 24-25. University California Press, Berkeley, Los Angeles. Lensky Y., Gassier P., Nutkin M., Delorme-Joulie M. and Levinson M. (1984) Pheromonal activity and fine structure of the mandibular glands of the honeybee drones. J. Insect Physiol. (In Press). Lensky Y. and Seifert H. (1975) Factors affecting swarming of bee colonies. Hassadeh 55, 632-636 (In Hebrew). Lensky Y. and Slabezki Y. (1981) The inhibiting effect of the queen bee (Apis mellifera L.) foot-print pheromone on the construction of swarming queen cups. J. Insect Physiol. 27, 313-323. Lindauer M. (1960) Time-compensated sun orientation in bees. Cold Spring Harbor Symp. Quant. Biol. 25, 371-377. List J. R. (1966) Smithsonian Meteorological Tables, p. 479. Smithsonian Inst. Washington, DC. Mackensen 0. (1947) Effect of carbon dioxide on initial oviposition of artificially inseminated and virgin queen bees. J. Econ. Entomol. 40, 344349. Medugorac I. and Lindauer M. (1967) Das Zeitgedachtnis der Bienen unter dem Einfluss von Narkose und sozialen Zeitgebem. 2. Vergl. Physiol.. 55, 450474.
Oertel E. (1956) Observation
on the flight of drone honey bees. Ann. Ent. Sot. Am. 49, 497-500. Pain J. (1961) Sur la pheromone des reines d’abeilles et ses effects physiologiques. Ann. Abeille 4, 73152, Pain J., Barbier M. and Roger B. (1967) Dosages individuels des acides Cito-9-&&m-2 oique et hydroxy-10-dec&re-2 oique dans les tetes des reines et des ouvrieres d’abeilles. Ann Abeille 10, 45-52. Renner M. (1960) The contribution of the honeybee to the study of time-sense and astronomical orientation. Cold Spring Harbor Symp. Quant. Biol. 25, 361-367. Renner M. and Vierling 6. (1977) Die Rolle des Taschendrtisenpheromons beim Hocheitsflug der Bienenkonigen. Behavioral Ecol. Sociobiol. 2, 329-338. Ruttner F. (1955) Einfache und mehrfache Paarung der KBnigin, erwiesen aus der Nachkommenschaft. Bienenvater 76, 5-10, 50-56, 1233127, I-59-164, 198-202. Ruttner F. (1956) The mating of the honeybee. Bee WZd. 37, 3-15. Ruttner F. (1966) The life and flight activity of drones. Bee Wld. 47, 93-100. Shoemaker H. H. (1947) Multiple mating in the queen honeybee. Am. Bee. J. 87, 19. Skowronek W. (1976) Biologia unasieniania sie matek pszczelich usypianych dwutlenkiem wegla. Pszczel. Zeszy. Nauk. 20, 99-115. Soczek Z. (1958) Wplyw neiktorych czynnikow na loty i kopulacje matek poszczelich. Pszczel. Zesz. Nauk. 2, 109-120.
Honeybee Taber S. (1964) Factors influencing the circadian flight rhythm of drone honey bees. Ann. Ent. Sot. Am. 57,
169-115. Taber S. (1974) Rearing and mating of queen and drone honey bees in winter. Am. Bee. J. 14, 18-19. Triasko V. V. (1951) Signs indicating the mating of queens. Pchelovodstvo 28, 2531 (In Russian). Triasko V. V. (1956) Repeated and multiple mating of queens. Pchelovodstvo 33, 43-50. (In Russian). Vierling G. and Renner M. (1977) Die Bedeutung des
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241
thghts
Sekretes der Tergittaschendtisen der Bienenkiinigin. Behavioral
fur
die Attraktivitlt
Ecol.
Sociobiol.
2,
185-200. Whitherell P. C. of normal and 65-75. Woyke J. (1964) honeybees. J. Woyke J. (1975)
(1972) Flight activity and natural mortality mutant drone honeybees. J. Apic. Res. 11, Causes of repeated
mating
flights by queen
Apic. Res. 3, 17-23. Natural
and instrumental
insemination
of
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