Journal of Vector Ecology

354

December 2010

Estimating reaction norms for predictive population parameters, age specific

mortality, and mean longevity in temperature-dependent cohorts of Culex
quinquefasciatus Say (Diptera: Culicidae)
Filiz Gunay, Bulent Alten, and Ergi Deniz Ozsoy
Hacettepe University, Science Faculty, Department of Biology, Evolutionary and Ecological Genetics Laboratory,
06800 Beytepe, Ankara, Turkey
Received 11 March 2010; Accepted 18 July 2010
ABSTRACT: Culex quinquefasciatus plays a major role in the transmission of important parasites and viruses throughout
the world. Because temperature is an important limiting factor on growth and longevity of all mosquito species, estimating
the reaction norms provides very important basic information for understanding both plasticity and individual variations of
the population. In the present study, Cx. quinquefasciatus were maintained at five different constant temperatures (15, 20,
23, 27, and 30C) for two subsequent generations. Reproductive population parameters in blood-fed mated females and
longevities of virgin and blood-fed mated adults reared at different temperatures were compared for the two generations.
Longevity increased as temperature decreased within a range of 15 to 30C for the unmated adults, and 15 to 27C for
the mated and blood-fed adults. Generation times were as long as 124.07 and 106.76 days for two subsequent generations
reared at 15C, and the highest intrinsic rate of increase (rm) values were estimated at 0.22 and 0.18, respectively, from the
cohorts reared at 27C. For survival rates, reproductive rates (R0), and rm values, 30C was found to be a critical temperature
for this species. These cohorts produced the smallest amount of eggs (R0= 5.06), rm values decreasing across generations
(from 0.11 to 0.06), and the survival rates from egg to adult were found to be insufficient (16.1 and 10.8%). Additionally,
the rate of exponential increase with age and age specific mortalities (b) were calculated for the virgin cohorts. Age specific
mortality rates increased as temperature decreased. The increase in mortality rates started to accelerate at 27C and was more
pronounced at 30C, for both females and males. We estimated the coefficients of variation for the b values in which females
have smaller coefficients than those of the males at all temperatures. Journal of Vector Ecology 35 (2): 354-362. 2010.
Keyword Index: Culex quinquefasciatus, temperature, variation, life table traits, longevity, age specific mortality.

INTRODUCTION
Life-history theory in evolutionary biology (Roff
1992, Stearns 1982) is a theory of fitness. The information
regarding life history traits of organisms, from experiments
carried out under laboratory conditions, could provide us
with sound predictions of the expressions of their genetic
potential, and thus could establish baselines for subsequent
field studies. A fitness framework enables generalizations
to be made not only for the species under study, but also
for other species that could have been subjected to similar
selective pressures (Nylin and Gotthard 1998).
The reaction norm is used to quantitatively model the
dependence of fitness-related characters on environmental
parameters such as ambient temperature and nutrition
(Stearns 1982). Therefore, it defines phenotypic plasticity.
As a generally accepted guideline, increased temperature
results in higher growth rates, shorter development times
and longevity, and smaller adult size in insects and other
ectotherms (Sibly and Atkinson 1994, Li and Jackson 1996,
Worthen 1996). Estimating the reaction norms in response
to these components, such as temperature variations
effecting distribution area of a given population, provides
important basic information for understanding both
plasticity and individual variations of the population.

The mosquito, Cx. quinquefasciatus Say 1823, plays

a major role in the transmission of bancroftian filariasis,
Chikungunya, West Nile, and St. Louis encephalitis worldwide. The species is widely distributed in the tropical and
subtropical areas of the world from the Nearctic region to the
end of the Palearctic region. It occurs in all climatic zones,
and altitude does not appear to limit its distribution (Bhat
1975). Although waste water is a major larval habitat, this
species can develop in virtually any type of aquatic habitat
in the human environment. Females of Cx. quinquefasciatus
generally feed indoors or outdoors on human blood.
Because of these characteristics, Cx. quinquefasciatus is
a good model organism to study predictive life traits in
relation to reaction norms.
The effects of temperature on the development of Cx.
quinquefasciatus have been reported previously (Shelton
1973, Suleman and Reisen 1979, Rayah and Groun 1983,
Service 1986, Rueda et al. 1990, Mogi 1992). In this study,
the effects of constant temperatures on life table traits of Cx.
quinquefasciatus were determined. Longevity comparisons
were also designed to reveal the reaction norms of the
adults with respect to the different constant temperatures
at which they developed. For this reason, as well as the life
table mortality outcomes, virgin adult cages were prepared
to exclude effects of mating and blood feeding on mortality.

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Journal of Vector Ecology

Maximum likelihood estimations of the rate of increase

in age specific mortality (b parameter of the Gompertz
function) were calculated in virgin Cx. quinquefasciatus
cohorts. Variation in age specific mortality in response to
temperature was defined in terms of a reaction norm after
one generation of rearing.

355

Table 1. Life table attributes used in this study and their

rationale.
Age specific
survivorship

lx= yx/yo

MATERIALS AND METHODS

Maintenance of the colony in the laboratory
The lab colony used in this study was previously reared
in France (ISEM) but originated in California in the 1980s.
Egg rafts from the colony were transferred to the Ecological
Research Laboratory at Hacettepe University (ESRL) in
Ankara, Turkey, in 2005. The rearing and feeding of adults
and larvae followed the methods of Kasap and Kasap
(1983) with a temperature 271C, 605 RH%, and 14:10
h (L:D) photoperiod. Individuals used in the experiments
were obtained from the same generation (F30) to avoid the
effects of genetic differences between generations.
Maintenance of cohorts in the climate chambers
Age-specific (horizontal) life tables were constructed
to determine whether temperature affects the basic
demography of Cx. quinquefasciatus adults. Three replicates
of 750 1st instar larvae were transferred into standard
polyethylene cups (27x16x17 cm) that contained 1 liter of
distilled water. The cups were placed in five climate chambers
programmed at five different temperatures (15, 20, 23,
27, and 30C) and exposed to a 14:10 (L:D) photoperiod
with a constant relative humidity of 60%. The larvae were
fed each day with 0.04 g sinking Tetramin, which was
spread evenly over the water surface. Pupal development
and the number of pupae present were checked daily. All
pupae were transferred to glass vials before eclosion. For
the virgin adults, female (100 individuals) and male (100
individuals) cages were prepared separately, with each
chamber containing 30% sucrose solution, for the estimation
of the rate of exponential increase in mortality with age (the
b parameter of the Gompertz function). In this experiment,
females were not blood-fed. In another experiment, 100
females and 100 males were placed together in 20x20x20
cm cloth cages containing plastic cups with distilled water
as oviposition sites. Females fed on quail blood every four
days for 2 h. Experiments were replicated three times for
each temperature regime. This procedure was followed for
two subsequent generations.
Life tables and statistical data analyses
Horizontal life table parameters were calculated from
daily records of mortality and fecundity of each cohort
of Cx. quinquefasciatus. Life table attributes of adult
mosquitoes, the calculation procedures, formulae used, and
their rationale in the present study were according to Belen
and Alten (2005) and summarized in Table 1.
Homogeneity of the data was tested with the Shapiro
Wilk test and the predictive population parameters were
compared using the non-parametric Kruskall-Wallis test.

Net reproductive
rate per cohort

Age of mean
cohort
reproduction

Intrinsic rate of
increase

lxmx

xlx mx /R0

lxmxe-rmx

yx = the number of
females or males
on each day, x.

m is the mean
number of female
progeny produced
by females of age
x. The value of mx
was calculated by
mx=Exs where Ex is
the mean number
of eggs produced
per female per
age x, and s=the
proportion of the
offspring (eggs)
that were females.

starting at x=1,
the day of adult
emergence.
l, m, w are as
above, e is the
base of natural
logarithms, x is the
age interval, lxmx
is the product of
the survivorship of
each cohort female
by its fecundity at
an age x.

Age specific mortality parameters from the Gompertz

function (Gompertz 1825), i.e., the baseline mortality
rate (a) and the rate of exponential increase in mortality
with age (b), were estimated with the virgins, per sex per
treated temperature, by the method of Pletcher (1999). A
likelihood X2 ratio test with 1 degree-of-freedom (only
b was constrained) was performed to assess statistical
significance.
RESULTS
The survival rates of the immature stages from egg
to adult are shown in Table 2. The highest survival rates
were from the cohorts at 23C and the lowest rates were
seen at the highest temperature condition (30C) for both
generations.
Separate adult life tables were constructed for each of
the cohorts reared under different temperature regimes
for two subsequent generations, and predictive population
parameters (R0, Tc, rm) were also calculated. The results are
compared in Table 3 for the first and second generations.
While the net reproductive rate, R0 was lowest at the
highest temperature for two subsequent generations, the
highest value was calculated from the cohort reared at 23C
while it decreased at the second generation. As a specific
observation, at this temperature males lived longer than
expected, which could mean the death caused by mating
was lower. R0 value was found to be slightly higher (52.31)
at 15C than at 27C (50.22), which is the laboratory

Journal of Vector Ecology

356

December 2010

Table 2. Survival rates of the immature stages from egg to adult for two subsequent generations of Cx. quinquefasciatus at five
different constant temperatures.
15C
17.60
14.01

Survival rates % (from egg to adult) F0

Survival rates % (from egg to adult) F1

optimum for the first generation, but it decreased to

37.23 for the second generation at the lowest temperature
(15C). In spite of these differences, for both generations
there was no discrepancy between the temperatures and
R0 values statistically (p=0.1377, p=0.0581). At the lowest
temperature, the generation time, Tc, was found to be
almost three months (106.76 days) for the first, and four
months (124.07 days), for the second generation. Tc showed
a negative correlation with the temperature, except at 30C
for both generations and at 23C for the second generation,
in which the females produced fewer eggs than expected.
There was a significant difference between temperatures
and Tc values for the first (p=0.0102) and second (p=0.0193)
generations. For generation times, the greatest significant
difference was between 15 and 27C (p=0.0101, p=0.0127,
respectively) for both generations among all cohorts.
Although the R0 values were greater at 15C than at
30C in the first generation, rm, the intrinsic rate of increase
gave the opposite outcome. Another important point was
that the rm value decreased in the course of one generation
at 30C. The highest value was calculated from the cohorts
at 27C, and the differences between the cohorts for both
generations are statistically significant (p=0.0159; p=0.0164,
respectively).
Interaction between longevity and temperature
variation is shown in Table 5 and Figure 1 for mated (life
table experiments) and unmated females and males of
the second generation. For mated sexes, longevity was
significantly affected by temperature and by sex, but there
were no significant differences between replicates (Table 4).
While the longevity of Cx. quinquefasciatus was
normally higher at lower temperatures, the mean
longevity of both female and male adults was clearly low
at extremely high temperatures (Table 5). Although there
were no significant differences between the replicates,
differences were obtained between females and males of
the temperature-dependent cohorts (Table 5, Figure 1). The

20C
40.38
35.42

23C
47.64
40.70

27C
30.61
39.99

30C
16.07
10.75

males demonstrated a significantly shorter longevity than

females at all temperatures (p<0.001). In general, longevity
patterns of both sexes approximated Slobodkins (1961)
Type II curve with little increase in mortality during early
age intervals in all the cohorts. According to lx data, the
greatest longevity of females and males was at 15C, for 103.5
days and 47.9 days, respectively. While longevity decreased
from 15 to 27C, it showed an unexpected increase at 30C
(Table 5). These results show that longevity, in general, is
linearly correlated with increasing temperature, with the
mentioned exception. The longevity of males reared at 23C
was slightly longer than that of males at 20C. Results were
similar with respect to the mean development time of the
larvae and pupae that lived longer at 30 than 27C for two
subsequent generations (data not shown).
Longevity of unmated individuals was also negatively
correlated with temperature (p<0.01), and the unmated
females in all cohorts had a longer lifespan compared to
males. All virgin cohorts, except adults aged at the highest
temperature condition (30 C), lived longer than the bloodfed and mated cohorts (Table 5 and Figure 1A). These results
suggest that 30C is a critical temperature for this species.
Table 6 and Figure 2 show the values of the rate
of increase in age specific mortality with age, b, and its
coefficients of variation determined for each temperature
used in the study by sex. The rate of exponential increase
in mortality (b) for unmated females and males was
significantly correlated with temperature (p<0.05, p<0.01,
respectively). According to the likelihood ratio test results
of females, there was no significant difference in age specific
mortality rates (X2=4.8128, p=0.0282) between 27 and
30C, but the other temperature comparisons were highly
significant. In contrast, the differences between all the male
b values were highly significant (X2=31.2487, p=0.001). Most
of the female to male comparisons in terms of temperature
variation gave highly significant figures (15, 20, 27,
and 30C; X2>10.8342, p<0.001; 27C X2=3.8778, p<0.05,

Table 3. Comparison of life table predictive parameters of Cx. quinquefasciatus cohorts maintained at five constant
temperatures for two subsequent generations.

F0

F1

15C

20C

23C

27C

30C

Ro

52.31

69.26

71.15

50.22

13.41

rm

0.06

0.13

0.17

0.22

0.11

Tc

124.07

63.69

49.64

34.69

44.90

Ro

37.24

58.86

35.48

58.43

5.06

rm

0.07

0.13

0.11

0.18

0.06

Tc

106.76

61.02

64.30

44.90

52.45

* Significant differences identified by the Kruskall-Wallis Test at the 0.05 level.

Journal of Vector Ecology

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357

Table 4. General linear model for the effects of temperature, replicate and sex on longevity from life table experiments with
mated + blood-fed adults of Cx. quinquefasciatus.
Replicate
Sex
Temperature
Rep x Sex
Temp x Sex
Temp x Rep x Sex
Error

MS
899.0
527,975.0
180,278.8
267.9
43,726.3
2,078.0
680.5

d.f.
2
1
4
2
4
7
2472

F
1.3
775.9
264.9
0.4
64.3
3.1

P
0.267
<0.001
<0.001
0.675
<0.001
0.003

Table 5. Weighted Square means of longevity (days, mean SE) of Cx. quinquefasciatus across temperatures, sexes, and
virginity. Data were pooled across the replicates that did not differ significantly from each other.
Temperature C
15
20
23
27
30

Unmated
female
156.186.39
75.873.31
55.262.18
34.291.06
14.910.62

Mated and blood

fed female
103.53.65
72.362.66
46.011.77
28.590.79
32.040.73

respectively) except that of 23C which was not significant

(X2= 0.1986, p= 0.6558). In contrast to the general trend of
females that showed lower age specific mortality rates than
males presented above, an opposite pattern was found for
the adults at 27C. Mean longevity of the females and males
at this temperature were very similar, unlike those from the
other temperature regimes.
Figure 2 also shows the coefficient of variation (CV) of
the b between the temperatures for each sex. Females had
less variability than males at all temperature conditions. At
27C, the optimum temperature of the laboratory colony,
Table 6. Rate of exponential increase in age specific
mortalities (b values x10-2 ) and coefficients of variation
(CV) at five different constant temperatures in Cx.
quinquefasciatus.
n

b (x 10-2)

(LCI, UCI)*

CV

Females
15C
100
1.468
(0.346- 6.231)
0.410
20C
100
2.790
(2.262- 3.440)
0.436
23C
100
4.915
(3.592- 6.727)
0.396
27C
100
11.538
(9.672- 13.765)
0.286
30C
100
14.561
(11.902- 17.815)
0.419
Males
15C
100
2.080
(0.515- 8.400)
0.421
20C
100
3.100
(2.448- 3.926)
0.451
23C
100
4.957
(4.136- 5.940)
0.425
27C
100
9.030
(7.684- 10.661)
0.357
30C
100
24.372
(19.629- 30.260)
0.451
*LCI: Lower Confidence Interval; UCI: Upper Confidence
Interval

Unmated
male
108.374.56
45.152.04
42.121.79
29.870.98
9.340.42

Mated and
blood fed male
47.92.56
24.71.23
26.71.06
13.80.53
19.80.51

both females (0.286) and males (0.357) had smaller

variation coefficients than those of the other temperature
regimes.
DISCUSSION
Although there have been many studies on the effects
of temperature variation on the pre-adult and adult stages
of mosquitoes, few have collected data in the appropriate
form and in sufficient detail to provide a distribution of
values required for calculations in mathematical models or
estimates for temperature-dependent development (Gomez
et al. 1977, Suleman and Reisen 1979, Mogi 1992, Su and
Mulla 2001). Our results showed Cx. quinquefasciatus is a
good model organism to study the predictive life traits in
relation to reaction norms of the temperature variation
affecting populations.
All of the temperature regimes we used affected reproductive parameters. Even though the main colony was
reared at 27C, the optimum temperature on the basis of
fecundity was 23C for the first, and 20C for the second,
generations. Nevertheless, there was no significant difference between the cohorts for R0 values for both generations
(p=0.1377, p=0.0581, respectively). As for the rm, the optimum temperature was 27C for the two consecutive generations. It is well known that one of the most valuable applications of the intrinsic rate of increase concept is in the
delineation of the livable environment of a species (Vargas
et al. 2000). Similar to the rm values calculated from different populations around the world (Walter and Hacker 1974,
Gomez et al. 1977, Suleman and Reisen 1979), rm values in
our study were also found to be positive under a wide range
of temperature regimes (15, 20, 23, 27, and 30C), so

Journal of Vector Ecology

358

December 2010

Figure 1. Box and Whisker plots of longevity (+1 SE) for mated + blood-fed and virgin adults of Cx. quinquefasciatus
(a), survival curves of mated and blood-fed females and males (b), virgin females and males (c) at five different constant
temperature (15C, 20C, 23C, 27C and 30C). Data were pooled across replicates (fm: female, m: male).

Vol. 35, no. 2

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359

Figure 2. Exponential increase curves in age specific mortalities (b values x 10-2) and coefficients of variation (CV) at five
different constant temperatures in Cx. quinquefasciatus.
we can conclude that Cx. quinquefasciatus may increase its
population size under all these temperature conditions but
with some differences. This is one explanation for why the
species has the ability to disperse widely in nature.
Minimal and maximal temperature thresholds for
embryonic development of Cx. quinquefasciatus are 13 and
39C, respectively. The hatching rate varies directly with
temperature, up to 32C, after which eclosion rates drop
gradually (Rayah and Groun 1983). We found that at 15C,
this species could complete its life cycle with a positive rm
and a very long generation time (124.07 days) (Table 3).
Suleman and Reisen (1979) have shown that this species
could overwinter in Pakistan, in a gonoactive state, with
females emerging during late autumn, persisting through
the cold winter months and into early spring. Overwintering
strategies of this nature coupled with a high degree of human
and bird feeding seemed to indicate that this species could
provide an overwintering mechanism for West Nile Virus
and perhaps for other disease agents (Suleman and Reisen
1979). Regarding the variety of the viruses transmitted by
this species (Jozan et al. 2003, Kilpatrick et al. 2007, Peterson
et al. 2008), our results suggest that Cx. quinquefasciatus
can overwinter in cooler areas than Pakistan (Lanciotti et
al. 1999, Epstein 2000, Githeko et al. 2000, Kilpatrick et al.
2004, Hayes et al. 2005).
According to McCann et al. (2009), better larval
conditions result in females capable of greater reproductive
output. In the present study, the most suitable condition in
terms of survival rates for the immature stages was found
to be 23C (Table 2). In the second generation at 23C, we
observed unexpected results. We were expecting to find a
greater R0 value at 23C, and indeed obtained it for the first
generation (Table 3), but in contrast, the R0 value was found
to be lower, and the Tc was longer, for the second generation
at the same temperature regime. One of the factors that can

affect the observed decrease in R0 and rm is the production

of offspring at an older age (Futuyma 1998). Since we
detected a delay at the second generation, this factor may
be responsible for the decrease in these parameters and
consequently in the increase of mean longevity of the
adults, eventually in Tc. Similar results were found at 30C
temperature regime for both generations. These unexpected
values of R0 and rm may also be the result of high mortality
among the cohort females that lived a maximum of 51
days and started to reproduce at the age of 21, while the
females that lived at the optimum temperature laid eggs on
the seventh day of emergence (not shown). Even though at
the coldest temperature rm values were found to be smaller
than those of the hottest for both generations, rm increased
with temperature increases for both generations, but it
was significantly decreased at 30C (Table 3). Changes in
the rm matters strongly for understanding the fitness and
permanency of the cohorts (Tatar 2001, Simsek et al. 2005).
These findings suggest that extremely warm temperatures
could be more detrimental, and possibly more limiting, than
cold temperatures for this species. For life span, the specific
patterns were mostly as expected and thus in agreement
with the general notion of pronounced differences between
different rearing temperatures (Tatar 2001). Like many of
the previous studies, the pattern of increasing life span of
cohorts at low temperatures was evident in both mated
and unmated cohorts as shown previously (Su and Mulla
2001, Norry and Loeschcke 2002, Gilles et al. 2005, Kasap
and Alten 2006, Aytekin et al. 2009, Karl and Fisher 2009).
This frequent pattern is related to increasing metabolic
rates with increasing temperatures in ectotherms, with
higher metabolic rates in turn being correlated with shorter
life spans (Karl and Fisher 2009). Life table experiments
at the highest temperature (30C) for mated and bloodfed adults (Table 5) yielded a higher corresponding adult

360

Journal of Vector Ecology

longevity. Likewise, Rueda et al. (1990) found the same

decrease in lifespan in both Cx. quinquefasciatus and Aedes
aegypti from 15 to 27C, but an increase at 30 and 34C.
Interestingly, this trend was not determined in unmated
cohorts in our study. On the other hand, Shelton (1973)
showed that in the immature stages of Cx. quinquefasciatus,
longevity increased while the temperature decreased in the
range from 20 to 26C, but at 32C, longevity increased.
Because even the immature stages show this response to
the highest temperature, it might be expected that unmated
adults would show the same reaction. We estimate that
this could have occurred with the effect of mating as a
specific trend. Perhaps there was a trade-off between the
rise of temperature and the decrease of longevity in which,
after some specific temperature is reached, some buffering
physiology of the organism may be overturning the negative
relationship between the temperature increase and the
longevity. It is thus possible that some overall metabolic and
genome expression changes could be linked to the mating
status of aging flies at higher temperatures, as mating
accelerates aging in general.
The longevity of a vector population is an extremely
important facet of its vectorial potential. Longevity patterns
in Cx. quinquefasciatus varied between sexes, with females
living longer than males, as are found in many other
animals (Smith and Warner 1989, Nuzhdin et al. 1997).
Males generally appear to sacrifice viability for enhanced
sexual performance, whereas females may benefit by
investing more in immunity and longevity (Rolf 2002).
As a rule, large animals tend to live longer than small
animals (Lindstedt and Calder 1976, Speakman 2005),
which may also have an impact on the pattern found in Cx.
quinquefasciatus, as adult females are larger than males at
all constant temperatures (data not shown). Sex differences
were affected by temperature. While males and females
showed similar life spans at the higher temperature, females
lived much longer than males at the lower temperatures.
This suggests that females may have an enhanced heat
tolerance compared to males, which has already been
shown in Drosophila (Sorensen et al. 2001, Jensen et al.
2007). Mating and blood feeding have important effects on
adult survival (Yuval 2006), and that it is shown once again
in this study. In what may be somewhat aberrant results at
30C, virgin adults did not live as long as those that were
mated and blood fed, suggesting that temperature stress
combined with blood deprivation and the inability to find
mates caused an enhanced death rate.
We have excluded the effects of mating and blood
feeding and examined the longevity of the virgin
individuals to observe the reaction norm in response to
temperature variation. Using the Gompertz function, we
estimated a, initial mortality rate, and b, exponential rate of
increase with age (Pletcher 1999). In general, total vectorial
capacity is more sensitive to changes in b than a, which
is understandable because b is exponentially, whereas a
is multiplicatively, related to overall mortality. As overall
mortality increases, the potential for mosquito populations
to transmit pathogens declines (Styer et al. 2007).

December 2010

Supporting our findings, Cx. quinquefasciatus adults have

more vectorial importance at relatively low temperatures
(15 and 20C). Tests indicated that with increasing
temperature, the exponential rate of increase in mortality
increased as we expected. Females at higher temperatures
(27 and 30C) showed considerably higher b values than
at lower temperatures. The reaction norm is a basic tool
of evolutionary analysis that quantifies the relationship
between environmental parameters and functional
characters, including reproduction and longevity (Phelan
and Rose 2006). In our study, the reaction norm relating
the exponential rate of increase in age specific mortality to
ambient temperature was fairly steep (Figure 2), especially
for males at 30C. In addition, except at the middle
temperature of 23C, there was a significant difference on
b values at every constant temperature for adults. Variation
coefficients of the b parameter suggest that the population
is strongly adapted to 27C and females give more stable
reactions than males.
Temperature may also affect the vectorial capacity and
changes in the population densities of species (Olejnicek
and Gelbic 2000). We conclude that temperature is a crucial
factor in the evolution and ecology of Cx. quinquefasciatus.
As climate changes could cause some unexpected effects on
the dispersal of disease (Epstein 2000), our results show that
this species is also a good candidate in this respect across its
distribution range.
Acknowledgments
We thank Dr. Utku Perktas and Murat Ylmaz for
their help and support. This study is part of an MSc thesis
submitted to Hacettepe University.
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