Tolerance of two honey bee races to various temperature and relative humidity gradients

Abstract

There are various factors that can have an effect on honey bee colonies. Temperature and relative humidity, in particularly, have special importance for honey bee colonies. Relatively few studies have been conducted on the effects of temperature and relative humidity on honey bee races. Here, the effects of different levels of temperature and relative humidity on survival, tolerance and body water loss were investigated on two races, one adapted to harsh conditions (Yemeni honey bees) and the other adapted to normal conditions (Carniolan honey bees). Results showed that temperature had higher effect than relative humidity on workers survival and Yemeni honey bees were
more tolerant to elevated temperature than Carniolan honey bees. Moreover, rates of body water loss for the two races were high under elevated temperature and low humidity conditions. In general, the response of the two races in the studied treatments was somewhat similar. However, under extreme conditions at elevated temperature or low humidity, Yemeni honey bees showed higher tolerance than
Carniolan honey bees.

Full text

Tolerance of two honey bee races to various temperature
and relative humidity gradients
Hossam F. Abou-Shaara*, Ahmad A. Al-Ghamdi, Abdelsalam A. Mohamed
Baqshan`s Chair for Bee Research, Plant Protection Department, College of Food and Agricultural Sciences, King Saud University,
P.O. Box. 2460, Riyadh 11451, Saudi Arabia
*Corresponding author, E-mail: entomology_20802000@yahoo.com
Abstract
ere are various factors that can have an effect on honey bee colonies. Temperature and relative humidity, in particularly, have special
importance for honey bee colonies. Relatively few studies have been conducted on the effects of temperature and relative humidity on
honey bee races. Here, the effects of different levels of temperature and relative humidity on survival, tolerance and body water loss were
investigated on two races, one adapted to harsh conditions (Yemeni honey bees) and the other adapted to normal conditions (Carniolan
honey bees). Results showed that temperature had higher effect than relative humidity on workers survival and Yemeni honey bees were
more tolerant to elevated temperature than Carniolan honey bees. Moreover, rates of body water loss for the two races were high under
elevated temperature and low humidity conditions. In general, the response of the two races in the studied treatments was somewhat
similar. However, under extreme conditions at elevated temperature or low humidity, Yemeni honey bees showed higher tolerance than
Carniolan honey bees.
Key words: Apis mellifera carnica, Apis mellifera jemenitica, honey bees, humidity, temperature, tolerance, survival.
Abbreviations: RH, relative humidity.
Environmental and Experimental Biology (2012) 10: 133–138 Original Paper
Introduction
e importance of temperature and relative humidity for
honey bees is well known, and all activities of honey bee
colonies are under the control of these factors. Temperature,
in particularly, is very important for internal as well as
external activities of honey bee colonies. Maintaining
a suitable range of temperature from 33 to 36 °C inside
colonies is very important for honey bees (Petz et al. 2004).
Deviation from this range can affect the developmental
period of honey bee immature stages, emergence rate (Tautz
et al. 2003), colour of emerged bees (DeGrandi-Hoffman
et al. 1993), wing morphology (Ken et al. 2005), learning
ability (Tautz et al. 2003), adult brain (Groh et al. 2004)
and disease prevalence. Also, ambient temperature has a
great effect on foraging activity, as high temperature has a
negative effect on bee foraging (Cooper, Schaffer 1985; Al-
Qarni 2006; Blazyte-Cereskiene et al. 2010). Moreover, very
low temperature below 10 °C can prevent flight activity
(Joshi, Joshi 2010).
On the other side, relative humidity has a particular
importance within the colony where high humidity is
mostly required for brood development (Human et al.
2006). Effect of humidity on egg hatching rate has been
previously identified (Doull 1976) and a relative humidity
about 75% within colonies could be considered as suitable
for immature stages (Ellis et al. 2008). In the case of external
activities, no clear direct impact of relative humidity on
honey bees has been reported, including foraging activity
(Joshi, Joshi 2010). Under low levels of relative humidity,
within colonies, honey bee workers try to increase humidity
by various means including nectar water evaporation
and water collection (e.g. Human et al. 2006). Caged bees
exposed to high temperature have been noticed to increase
water uptake (Free, Spencer-Booth 1958). erefore, the
integration between temperature and relative humidity is
very important for honey bee activity.
Not all honey bee races respond in the same way to
thermal stress or even relative humidity levels. Hence,
the success of honey bee races to occupy specific regions
is the overall result of an adapted response to ecological
stresses. Here, two honey bee races were studied (Yemeni
honey bees, Apis mellifera jemenitica, bees adapted to harsh
conditions of Saudi Arabia, and Carniolan honey bees, Apis
mellifera carnica, bees adapted to normal conditions) to
investigate the impacts of various temperature and relative
humidity levels on survival, tolerance and body water loss
for these two races as well as to identify differences in their
tolerance ability.
Materials and methods
Material
e research was performed at the Bee Research Unit
133

H.F. Abou-Shaara, A.A. Al-Ghamdi, A.A. Mohamed
laboratory, King Saud University, Saudi Arabia. e
influence of temperature and relative humidity was
investigated on forager bees (age above 21 days) of two
honey bee races, Yemeni (Apis mellifera jemenitica Ruttner)
and Carniolan (Apis mellifera carnica Pollmann) honey
bees. e following experiments were conducted under
controlled conditions of temperatures and relative humidity
(RH) in Memeret incubators, Germany. ese incubators
allowed control of temperature and relative humidity, and
have an internal glass door to allow treatment inspection
without interrupting adjusted levels of temperature and
relative humidity.
Workers survival
ree cages with dimensions 16 × 16 × 7cm and with one
glass side and one wire mesh side (Fig. 1) per race were
used per treatment. Fiy workers per each cage per race
with a total of 300 workers for the two races were used per
treatment. Caged bees were provided with 5 mL water, 5
mL 50% sugar syrup, and a 20 g pollen patty. Temperature
levels of 35 °C, 40 °C and 45 °C at 75% constant RH, and
RH levels of 15, 30, 50 and 75% at constant temperature of
35 °C were tested. ese levels of temperature and relative
humidity were selected to coincide with the existing harsh
conditions, elevated temperature and low humidity, of Saudi
Arabia. e cages were subjected to one of the treatments
and daily inspection was made of the number of dead
workers. Worker survival per each cage was calculated as
the number of days at which all bees had died. Subsequently,
the survival mean per treatment was calculated by dividing
the total number of days at which 100% death was occurred
in three cages by three (the number of cages per each
treatment).
Temperature tolerance
To assess heat tolerance for the two races, the method
of Atmowidjojo et al. (1997) was adopted with some
modifications. A total of 300 bees per each race were
used in this experiment (50 bees per cage and six cages
per race). e caged bees were equilibrated to room
temperature before the incubator-programme started.
e incubator was adjusted to a constant humidity (50%),
while temperature was programmed to start at 30 °C and
increase to 70 °C during 80 min. Aer the incubator heating
program was started, the number of intolerant bees were
recorded at each 0.5 °C step. e dorsal turning reflex was
used to assess temperature tolerance. Bees unable to right
themselves immediately were classed as intolerant to the
given temperature. e temperature at which bees started
to be intolerant and the percentage of intolerant bees per
each temperature were recorded.
Body water loss
Rates of body water loss were estimated gravimetrically.
ree plastic containers with an upper cover of aluminum
foil with 100 pores were used per race per treatment. Ten
bees were placed in each container (total of thirty bees per
race per treatment) and were weighed by using GR 200
balance (A & D Company Limited, Japan) to the nearest
0.01 mg (W1). e experimental groups were maintained
in incubators at 35 °C, 40 °C or 45 °C. Combinations of the
temperatures and 10, 25 and 50% RH treatments for 2 h
were employed, aer which the bees were reweighed (W2).
Rates of water loss were calculated as (W1) – (W2). To
identify the water loss rate per bee, each weight was divided
by 10 and the final results were expressed as mg per hour
(mg h–1).
Fig. 1. Cages used for bee survival studies in the present experiments.
134

Statistical analysis
A completely randomized design was used for all the
above-mentioned experiments. e obtained data were
statistically analysed using analysis of variance (ANOVA)
and means were compared by using the Least Significant
Difference test (LSD0.05) with the SAS 9.1.3 programme
(SAS Institute 2004).
Results
Effect of temperature on worker survival
Honey bee races showed distinctive response to different
temperature gradients (Table 1). At 35 °C, relatively long
survival was found for Carniolan and Yemeni honey
bees, while at 40 °C Yemeni honey bees survived longer
than Carniolan honey bees by about 2.66 days. At 45 °C
all workers of Carniolan and Yemeni honey bees had died
within 24 h. Significant (P < 0.05) and a strong negative
correlation (r = –0.91) was found between survival and
temperature.
A significant difference (P < 0.05) was found between
survival of Yemeni and Carniolan honey bees 40 °C while no
significant differences were found for the other treatments
(LSD0.05 values were 6.54, 2.62 and 0 for treatments 35 °C,
40 °C and 45 °C, respectively).
Effect of relative humidity on worker survival
At a fixed temperature of 35 °C, humidity had effect on
worker survival (Table 1). e best survival for the two
races was at relative humidity of 75% followed by 50%,
30%, and then 15%. Mean values of worker survival were
higher for Carniolan honey bees than Yemeni honey bees
at all humidity treatments except at 15% where Yemeni
honey bees had higher survival than Carniolan honey
bees. In general, no large differences in survival were found
between Yemeni and Carniolan honey bees at all humidity
treatments, as difference in survival between the two races
was only 1, 0.66, 0.34 and 1 days for treatments of 15, 30, 50
and 75%, respectively. Significant (P < 0.05) and moderate
positive correlation (r = 0.79) was found between survival
and humidity.
No significant differences (P > 0.05) were found
between mean survival of Yemeni and Carniolan honey
bees at all humidity treatments (LSD0.05 values were 5.70,
4.43, 5.23 and 6.54 for treatments 15, 30, 50 and 75% RH,
respectively).
Effect of temperature and relative humidity on worker
survival
Results of temperature and relative humidity treatments are
shown in Table 1. Temperature seemed to have higher effect
on worker survival than humidity, as a noticeable reduction
in workers survival was found with elevated temperature.
On the other hand, no major difference in workers survival
was observed between humidity treatments, especially
between 30 and 50% as well as between 50 and 75%. e
highest reduction in worker survival was observed at
temperatures 40 and 45 °C, as well as at relative humidity
15%. However, the reduction rate of survival in the case of
temperature was higher than that of humidity.
No significant differences (P > 0.05) were detected
between survival at 40 and 45 °C in the case of Carniolan
honey bees, while significant differences (P < 0.05) were
found between survival in all heat treatments for Yemeni
honey bees. Also, no significant differences were found
between survival at humidity treatments 15 and 30% as well
as 30 and 50% in the case of Carniolan honey bees, while
no significant differences were found between survival
among humidity treatments 75, 50 and 30% as well as 50,
30 and 15%. In general, significant differences were found
between the overall mean survival on heat treatments while
no significant differences were detected between the overall
mean of some humidity treatments (30 and 50% as well as
30 and 15%).
It was clear that temperature had higher effect on worker
survival than humidity. Yemeni honey bees showed higher
survival under elevated temperature and very low humidity
conditions than Carniolan honey bees while Carniolan
Tolerance of honey bee races to temperature and relative humidity
135
Table 1. Mean survival (days) for two honey bee races at different temperature and relative humidity gradients. Means followed with the
same letter in the same column within each treatment category are not significantly different (P > 0.05)
Type of treatment Temperature (°C) / Survival mean (days) ± SE Overall mean ± SD
humidity (%) Carniolan honey bees Yemeni honey bees
Heat treatments 35 / 75 13.67 ± 1.45 a 12.67 ± 1.85 a 13.16 ± 2.64 a
40 / 75 2.67 ± 0.67 b 5.33 ± 0.67 b 4.00 ± 1.78 b
45 / 75 1.00 ± 0.00 b 1.00 ± 0.00 c 1.00 ± 0.00 c
Humidity treatments 35 / 15 5.33 ±1.20 c 6.33 ± 1.67 b 5.83 ± 2.32 c
35 / 30 8.33 ± 0.66 bc 7.67 ± 1.45 ab 8.00 ± 1.79 bc
35 / 50 9.67 ± 0.67 b 9.33 ± 1.76 ab 9.50 ± 2.07 b
35 / 75 13.67 ± 1.45 a 12.67 ± 1.85 a 13.16 ± 2.64 a
LSD0.05 (temperature) 3.19 3.94 2.26
LSD0.05 (humidity) 3.44 5.51 2.68

honey bees had higher survival than Yemeni honey bees
under suitable conditions, especially at temperature 35°C
and humidity above 30%.
Temperature tolerance
Aer exposing honey bee workers to various temperatures
from 30 to 70 °C, Carniolan honey bee workers began to be
intolerant at 57.5 °C while Yemeni honey bee workers began
to be intolerant at 61 °C (Fig. 2). All Carniolan honey bee
workers had died at 66 °C, while all Yemeni honey workers
had died at 68 °C. e majority of intolerant Carniolan
honey bees were observed at 62.5 and 66 °C while for
Yemeni honey bees the majority occurred at 64 to 68 °C.
In general, Yemeni honey bees had higher ability to tolerate
temperature than Carniolan honey bees.
Body water loss
Table 2 shows body water loss for the studied races under
different levels of temperature and relative humidity. e
highest body water loss was found when honey bee workers
were exposed to 10% RH and temperatures of 40 and 45
°C, as well as 25% RH and 45 °C, while the least loss was
obtained when honey bee workers were exposed to 50%
RH and temperature 45, 40 and 35 °C. In general, Carniolan
honey bee workers lost more body water than Yemeni
honey bees, especially at high temperatures 40 and 45 °C
and low humidity 10 and 25%.
Significant differences, in general, were found in
water loss between all temperature and relative humidity
treatments except between temperature treatments of 35
and 40 °C at all humidity treatments for Carniolan honey
bees, also between treatments of 35 and 40 °C at 10% RH
as well as 35 and 40 °C at 25% RH for Yemeni honey bees.
Moreover, significant differences were found between
Carniolan and Yemeni honey bees for all treatments (P <
0.05), except at 50% RH and 35 °C.
Discussion
Effect of temperature and relative humidity on workers
survival
High temperature had negative effect on worker survival
for the two races. is result is in accordance with Remolina
et al. (2007) who exposed honey bee workers to 42 °C till
death and found the range of life span mean was from 31
to 91 h (about 1.29 to 3.79 days). Also, Mardan and Kevan
(2002) found that adult workers of giant honey bees, Apis
dorsata, exposed to 38 and 45 °C had died within 5 days and
48 h, respectively which supports the idea that temperature
has negative effect on worker survival.
e highest mean worker survival was at temperature
treatment of 35 °C, observed by Clinch and Faulke (2012)
who found that the least mortality rates of honey bee
workers were at temperature treatment of 35 °C. Yemeni
honey bees showed higher survival at temperature 40 °C
than Carniolan honey bees. However, no differences were
found between survival of the two races at 35 and 45 °C.
us, Yemeni honey bees can be used for beekeeping
purposes at regions with higher ambient temperature than
Carniolan honey bees.
Higher relative humidity treatments was associated
with increasing worker survival. However, the effect of
humidity was not high and no differences in survival mean
were detected between the two races. Moreover, Carniolan
honey bees had higher survival than Yemeni honey bees for
all treatments except at 15% RH, which indicated the high
performance of both Carniolan than Yemeni honey bees
under normal conditions, while under stress conditions
Yemeni honey bees seemed to have better response than
Carniolan honey bees.
Generally, high humidity is better for enhancing
survival. Unfortunately, there are not many studies that
have considered effect of humidity on honey bee workers.
However, the effect of humidity seemed to be rather low, in
accordance with the findings of Joshi and Joshi (2010) who
investigated honey bee flight activity.
Temperature tolerance
Presently, the bees adapted to harsh conditions (Yemeni
honey bees) had higher tolerance ability than the adapted
bees to normal conditions (Carniolan honey bees). is
result is in agreement with the findings of Atmowidjojo et
al. (1997), who observed that tolerance of the feral honey
bees, more adapted bees to harsh conditions, as higher than
domestic honey bees of the Arizona region. In general,
Yemeni and Carniolan honey bees were less tolerant to
very high temperature, which is supported by the study
of Mardan and Kevan (2002) who found that temperature
from 26 to 36 °C did not affect survivorship of workers
Fig. 2. Mortality of Yemeni and Carniolan honey bees with
elevated temperature.
H.F. Abou-Shaara, A.A. Al-Ghamdi, A.A. Mohamed
136

of giant honey bees, A. dorsata, survivorship while at 45
°C workers had died within 48 h. us, honey bees have
less tolerance ability to endure high temperatures for a
long time. e ability of honey bee races to survive under
high temperatures before death can be explained by the
presence of heat shock proteins which have been identified
previously in honey bee larvae (Chacon-Almeida et al.
2000) and adults (Severson et al. 1990). Also, the differences
between Yemeni and Carniolan honey bees in their thermal
tolerance could be attributed to differences in their body
size as Yemeni honey bees are smaller than Carniolan
honey bees (Abou-Shaara, Al-Ghamdi 2012).
In the present study, the maximum tolerance for
honey bee workers was found at 57.5 and 61 °C while the
maximum tolerance was found at 49.1 °C by Kafer et al.
(2012) study and at 42.8 and 50.7 °C by Atmowidjojo et al.
(1997). us, the present results differ from those in other
studies. ese differences in maximum tolerance can be
attributed to study conditions and honey bee race used:
Kafer et al. (2012) investigated Carniolan honey bees and
a temperature range from 25 to 53 °C at an increasing rate
of 0.25 °C per minute. Atmowidjojo et al. (1997) used a
temperature range from 30 to 60 °C at an increasing rate
of 0.5 °C per minute for domestic and feral honey bees
of the Arizona region. In the present study a temperature
range from 30 to 70 °C at an increasing rate of 0.5 °C per
minute and RH 50% were tested on Carniolan and Yemeni
honey bees. No data about relative humidity were provided
in the Kafer et al. (2012) and Atmowidjojo et al. (1997)
investigations.
Body water loss
As compared with Yemeni honey bees, Carniolan honey
bees lost more body water under the studied treatments.
is result is in accordance with Al-Qarni (2006), who
found that mean weight loss was higher for Carniolan
honey bees than Yemeni honey bees, aer subjecting the
bees to air temperature during season for two hours in
conditions of the Riyadh region, Saudi Arabia. Also, rates
of body water loss increased with elevated temperature
and with low humidity. is is in accordance with Roberts
and Harrison (1999), who observed that water vapour loss
increased at air temperature values above 33 °C.
Moreover, Atmowidjojo et al. (1997) recorded the
highest rate of body water loss at 35 °C and 0% relative
humidity while the least mean body water loss was at 25 °C
/ 75% RH and at 30 °C / 100% RH. Additionally, in a study
by Heinrich (1980) honey bees at ambient temperature of
15 °C to 25 °C were found to maintain head temperature
above the ambient temperature by about 7 °C while at
ambient temperature of 46 °C mean of head temperature
was about 43 °C, which implies that honey bees under high
temperature decrease their body temperature mainly by
body water loss or other means.
Tolerance of honey bee races to temperature and relative humidity
137
Table 2. Mean ± SE of body water loss (mg h–1) of honey bee workers under different levels of temperature and relative humidity
Race Relative humidity / temperature LSD0.05
10% 25% 50%
35 °C 40 °C 45 °C 35 °C 40 °C 45 °C 35 °C 40 °C 45 °C
Carniolan 2.67 ± 0.16 b 3.50 ± 0.28 b 7.16 ± 0.33 a 1.33 ± 0.17 b 2.33 ± 0.16 b 6.00 ± 0.50 a 1.00 ± 0.28 b 1.83 ± 0.16 b 3.17 ± 0.33 a RH 10% (0.94)
RH 25% (1.10)
RH 50% (0.94)
Yemeni 1.33 ± 0.17 b 1.67 ± 0.16 b 4.17 ± 0.17 a 0.67 ± 0.16 b 1.17 ± 0.16 b 3.17 ± 0.17 a 0.50 ± 0.00 c 1.00 ± 0.00 b 1.67 ± 0.16 a RH 10% (0.58)
RH 25% (0.58)
RH 50% (0.33)
LSD0.05 0.65 0.92 1.03 0.65 0.65 1.46 0.80* 0.46 1.03

Exp. Biol. 114: 1–15.
DeGrandi-Hoffman G., Spivak M., Martin J. 1993. e influence
of temperature on cuticular color of honeybee (Apis mellifera
L) queens. Apidologie 24: 101–108.
Doull K.M. 1976. e effects of different humidities on the
hatching of the eggs of honeybees. Apidologie 7: 61–66.
Ellis M.B., Nicolson S.W., Crewe R.M., Dietemann V. 2008.
Hygropreference and brood care in the honeybee (Apis
mellifera). J. Insect Physiol. 54: 1516–1521.
Free J.B., Spencer-Booth Y. 1958. Observations on the temperature
regulation and food consumption of honeybees (Apis
mellifera). J. Exp. Biol. 35: 930–937.
Groh C., Tautz J., Rossler W. 2004. Synaptic organization in the
adult honey bee brain is influenced by brood-temperature
control during pupal development. Proc. Natl. Acad. Sci. USA
101: 4268–4273.
Heinrich B. 1980. Mechanisms of body-temperature regulation in
honeybees Apis mellifera, I. regulation of head temperature. J.
Exp. Biol. 85: 61–73.
Human H., Nicolson S.W., Dietemann V. 2006. Do honeybees,
Apis mellifera scutellata, regulate humidity in their nest?
Naturwissenschaen 93: 397–401.
Joshi N.C., Joshi P.C. 2010. Foraging behaviour of Apis spp. on
apple flowers in a subtropical environment. NY Sci. J. 3: 71–76.
Kafer H., Kovac H., Stabentheiner A. 2012. Upper thermal limits of
honeybee (Apis mellifera) and yellowjacket (Vespula vulgaris)
foragers. Mitt. Dtsch. Ges. Allg. Angew. Ent. 18: 267–270.
Ken T., Bock F., Fuchs S., Streit S., Brockmann A., Tautz J. 2005.
Effects of brood temperature on honey bee Apis mellifera wing
morphology. Acta Zool. Sin. 51: 768–771.
Mardan M., Kevan P.G. 2002. Critical temperatures for survival of
brood and adult workers of the giant honeybee, Apis dorsata
(Hymenoptera: Apidae). Apidologie 33: 295–301.
Petz M., Stabentheiner A., Crailsheim K. 2004. Respiration of
individual honeybee larvae in relation to age and ambient
temperature. J. Compar. Physiol. B 174: 511–518.
Remolina S.C., Hafez D.M., Robinson G.E., Hughes K.A. 2007.
Senescence in the worker honey bee Apis mellifera. J. Insect
Physiol. 53: 1027–1033.
Roberts S.P., Harrison J. 1999. Mechanisms of thermal stability
during flight in the honeybee Apis mellifera. J. Exp. Biol. 202:
1523–1533.
SAS institute 2004. e SAS System Version 9.1.3. SAS Institute,
Cary, NC.
Severson D.W., Erickson E.H.Jr, Williamson J.L., Aiken J.M. 1990.
Heat stress induced enhancement of heat shock protein gene
activity in the honey bee (Apis mellifera). Experientia 46: 737–
739.
Tautz J., Maier S., Groh C., Rossler W., Brockmann A. 2003.
Behavioral performance in adult honey bees is influenced by
the temperature experienced during their pupal development.
Proc. Natl. Acad. Sci. USA 100: 7343–7347.
Conclusions
Temperature and relative humidity had high effect on
honey bee adults. Elevated temperature had negative effect
on worker survival while relative humidity had positive
effect on worker survival. Differences between the studied
races in their heat tolerance ability were observed and the
most adapted bees to harsh conditions, Yemeni honey bees,
showed higher tolerance than Carniolan honey bees. Also,
rates of body water loss of the two races increased with
temperature and lower humidity. In general, Yemeni honey
bees showed less body water loss than Carniolan honey
bees. It is reasonable to believe that Carniolan honey bees
have higher performance than Yemeni honey bees under
normal conditions while under harsh conditions, elevated
temperature and low humidity, Yemeni honey bees are
more suitable than Carniolan honey bees.
Acknowledgements
anks are given to the Bee Research Unit, Plant Protection
Department, College of Food and Agricultural Sciences, King
Saud University for providing the necessary materials for the
research.
References
Abou-Shaara H.F., Al-Ghamdi A.A. 2012. Studies on wings
symmetry and honey bee races discrimination by using
standard and geometric morphometrics. Biotechnol. Animal
Husb. 28: 575–584.
Al-Qarni A.S. 2006. Tolerance of summer temperature in
imported and indigenous honeybee Apis mellifera L. races in
central Saudi Arabia. Saudi J. Biol. Sci. 13: 123–127.
Atmowidjojo A.H., Wheeler D.E., Erickson E.H., Cohen A.C.
1997. Temperature tolerance and water balance in feral and
domestic honey bees, Apis mellifera L. Compar. Biochem.
Physiol. 118A: 1399–1403.
Blazyte-Cereskiene L., Vaitkeviciene G., Venskutonyte S., Buda
V. 2010. Honey bee foraging in spring oilseed rape crops
under high ambient temperature conditions. Zemdirbyste-
Agriculture 97: 61–70.
Chacon-Almeida V.M.L., Simoes Z.L.P., Bitondi M.M.G. 2000.
Induction of heat shock proteins in the larval fat body of Apis
mellifera L. bees. Apidologie 31: 487–501.
Clinch P.G., Faulke J. 2012. Effect of population density and
storage temperature on the longevity of caged worker honey
bees. New Zealand J. Exp. Agric. 5: 67–69.
Cooper P.D., Schaffer W.M. 1985. Temperature regulation of
honey bees (Apis mellifera) foraging in the Sonoran desert. J.
Received 22 October 2012; received in revised form 17 November 2012; accepted 19 November 2012
H.F. Abou-Shaara, A.A. Al-Ghamdi, A.A. Mohamed
138