-
Medical and Veterinary Entomology (2011), doi:
10.1111/j.1365-2915.2010.00939.x
Variations in life tables of geographically isolatedstrains of
the mosquito Culex quinquefasciatus
D. S. S U M A N1, S. N. T I K A R1, M. J. M E N D K I1, D. S U K
U M A R A N1,O. P. A G R A W A L2, B. D. P A R A S H A R1 and S. P
R A K A S H11Division of Entomology, Defence Research and
Development Establishment, Gwalior, India and 2School of Studies in
Zoology,Jiwaji University, Gwalior, India
Abstract. Variations in the life tables and other biological
attributes of four strains ofCulex quinquefasciatus Say (Diptera:
Culicidae) from geographically isolated regionsof India that had
been reared to the fifth generation in the laboratory were
assessedunder a standardized rearing regime under constant
laboratory conditions. Two strainsfrom arid habitats [Jodhpur (JD)
and Bikaner (BKN)], one from a semi-arid inlandhabitat [Bathinda
(BTH)], one from a semi-arid coastal habitat [Jamnagar (JMN)] anda
standard laboratory strain (LAB) were compared. Horizontal
life-table parameterswere measured for each strain. Egg mortality
ranged from 4.4% (JD and BTH) to19.5% (BKN). The lowest rate of
adult emergence and highest female : male ratiowere found in BKN,
and the highest rate of adult emergence and lowest female :
maleratio were recorded in BTH. The egg-hatching period was longest
in BTH and shortestin LAB. The duration from oviposition to adult
emergence was longest in JD andshortest in LAB. Females lived
longer than males in all strains. The net reproductiverates (R0) of
all field-derived strains (122.9162.2) differed significantly
betweenstrains and were significantly greater than that of LAB
(107.6). Similarly, both theintrinsic rate of increase (rm ) and
finite rate of increase () were found to be lowerin LAB than in the
field strains, but the mean generation time (T ) and doubling
time(DT ) were longest in LAB. For several life-table attributes,
JD and BTH clusteredtogether and were more similar to JMN than to
BKN and LAB. The results indicatethat BTH, BKN and JD can be
characterized as r-strategists, more so than JMN.Overall fecundity
increased with age. Differences in annual temperature ranges
andmean annual rainfall between locations were positively
correlated (r = 0.460.97)with egg production, female life
expectancy, R0, rm , and T . The results suggest thatstrains of Cx.
quinquefasciatus from different geographical areas with
contrastinghabitats vary in their survival and reproductive
strategies accordingly.
Key words. Culex quinquefasciatus, ecological variation, life
reproductive strategies,life-table attributes, strain
development.
Introduction
Culex quinquefasciatus Say is the most common domesticspecies of
mosquito in the tropics. It is the principal vector ofBancroftian
filariasis (World Health Organization, 2006) and
Correspondence: Dr B. D. Parashar, Scientist F, Division of
Entomology, Defence Research and Development Establishment,
Gwalior, MadhyaPradesh 474002, India. Tel.: +91 751 223 1862; Fax:
+91 751 234 1148; E-mail: [email protected]
breeds in diverse aquatic habitats, ranging from polluted
tofresh water (Sirivanakaran, 1976).
The survival and fecundity of different mosquito species
areaffected by factors such as nutrition (Day et al., 1994;
Costeroet al., 1998), resistance to organophosphate insecticides
(Jinfu
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society 1
-
2 D. S. Suman et al.
et al., 1998), temperature (Maharaj, 2003) and infection
bymicrobial pathogens (Mahmood et al., 2004). Mosquitoesoccurring
in distinct locations normally adapt to local con-ditions. Over
time, ecological isolation and adaptation to localconditions may
lead to the development of geographically iso-lated strains that
differ in various biological traits, such asfecundity and
survivorship, which gives rise to variation in arange of population
parameters (Reisen et al., 1979).
Distinctive life-table attributes have been found in strainsof
Cx. quinquefasciatus from Bangkok (Thailand), the south-eastern
U.S.A. (Vero Beach, FL), the southwestern U.S.A.(Houston, TX)
(Walter & Hacker, 1974) and the NorthwestFrontier in Pakistan
(Suleman & Reisen, 1979). Recently,Suman et al. (2009) reported
significant variations in morpho-metrics and morphology among eggs
from the four strains ofCx. quinquefasciatus investigated in the
present study, sourcedfrom arid, semi-arid and coastal regions of
India. We hypoth-esized that these mosquito strains will differ in
their life-tableand biological traits because they appear to be
adapted to their
respective local environments. To test this notion, we
assessedlife-table and other biological attributes under
standardized lab-oratory environments in four strains of Cx.
quinquefasciatusfrom a range of distinct isolated habitats in India
and a standardlaboratory strain, and correlated the attributes with
ecologicalvariables.
Materials and methods
Mosquito collection, rearing and experimentation
Culex quinquefasciatus larvae were collected from
militarycantonments in Jodhpur and Bikaner on the western plain of
anarid zone in the Thar Desert, an air force station in Jamnagaron
the west coastal plain of a semi-arid zone close to the Ara-bian
Sea coast, and Bathinda on a northern plain of the
uppernorthwestern region of a semi-arid zone (Fig. 1). The
annualrange of temperature (winter minimumsummer maximum)
km
Fig. 1. Locations of collections of Culex quinquefasciatus in
India. BTH, Bathinda; BKN, Bikaner; JD, Jodhpur; JMN, Jamnagar;
GWL, laboratoryat Gwalior.
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
Culex quinquefasciatus life tables 3
was intermediate in Jodhpur and Bikaner (245 C), mildestin
Jamnagar (936 C) and most extreme in Bathinda(247 C). Annual
rainfall ranged from 10 years. This is situated ina semi-arid
region that receives 5001000 mm of rainfall peryear. Annual
temperature ranges between 2 C and 48 C. Thevegetation of this
region is tropical deciduous and thorny.
Larvae were brought to the Defence Research and Devel-opment
Establishment, Gwalior and maintained in standardlaboratory
conditions at 27 1 C, 75 5% relative humid-ity (RH) and light :
dark (LD) 12 : 12 h. Larvae were kept ata density of 100 larvae per
bowl, in enamel bowls contain-ing 2 L of dechlorinated water and
were fed regular amountsof dried yeast on alternate days. After
pupation, they weretransferred to cages (75 65 65 cm) to provide up
to 50male and 50 female adults per cage after emergence.
Afteremergence, adults were provided with 10% sugar solution
adlibitum dispensed through a cotton wick in a Petri dish anda
chick was provided as a source of blood twice a week.These colonies
were maintained for up to four generations(approximately 2
months).Chicks were maintained in accor-dance with approved
guidelines of the Committee for the Pur-pose of Control and
Supervision of Experiments on Animals(CPCSEA), India.
Although laboratory rearing imposes a certain degree ofselection
pressure on aspects of mosquito biology, all colonieswere exposed
to standardized environmental conditions thatwere favourable to
mosquito survival; hence, we assume thatestimates of life-table
parameters derived from data collectedfrom the colonized wild
strains represent a maximum expres-sion of their life-table
parameters and are likely to reflect truedifferences between
geographically isolated strains. Similarassumptions were made by
Reisen et al. (1979) to comparethe life-table strategies of
geographically distinct strains ofCulex tritaeniorhynchus after
colonization in standard labo-ratory conditions for many
generations (range: 63236).
To assess the adult parameters, 50 pairs of male and
femalemosquitoes of the same age from the F5 generation
werereleased in each of three rearing cages for each strain
[i.e.four experimental strains from Jodhpur (JD), Bikaner
(BKN),Bathinda (BTH) and Jamnagar (JMN), respectively, plus
thelaboratory strain (LAB)]. Adults were provided with 10%
sugarsolution and a chick for blood feeding ad libitum
throughoutthe experiment. A glass Petri dish (140 mm in
diameter)containing 400 mL water was provided for oviposition.
Dailyobservations of egg rafts laid and the mortality or survival
ofadult male and female mosquitoes were recorded until the deathof
all mosquitoes. The numbers of egg rafts laid were counted,after
which the numbers of eggs per raft were counted under
a microscope (Lieca MZ12; Leica Microsystems, Wetzlar,Germany).
For each strain, the three largest egg rafts wereselected and
placed individually into three bowls, eachcontaining 2 L of
dechlorinated water. Subsequently, variousdevelopmental parameters
of immature stages were recordedfor each strain. Hatching rates
were calculated by comparingthe number of eggs per egg raft with
the number of larvaeproduced 12 h later. This was carried out by
observing thelarvae against a contrasting background and removing
themby pipette to a new bowl. Egg rafts with unhatched eggswere
transferred to separate bowls for further hatching andcounted at
24-h intervals until hatching of larvae was complete;numbers of
late-hatching larvae were added to the initial count.
Statistical analysis of life-table and other biological
attributes
Data analysis was based on mean values for the three repli-cated
cohorts of 50 females for each strain. Data were anal-ysed for mean
pre-oviposition days (mean number of daysfrom first exposure to
blood host to the appearance of thefirst egg raft), oviposition
days (mean number of days ofegg laying) and post-oviposition days
(mean number of daysfrom the last egg raft laid to the death of the
last female),mean number of eggs produced per cohort of 50
females,mean number of eggs per female lifespan [mean numberof
eggs/female/oviposition (i.e. number of eggs/number offemales alive
on each oviposition day) for all oviposition daysuntil all females
were dead number of oviposition days]and eggs/female/day
(eggs/female lifespan/number of ovipo-sition days). Various
attributes of a horizontal life table wereestimated, including life
expectancy at emergence (ex ), netreproductive rate (R0), intrinsic
rate of increase (rm ), finiterate of increase () and mean
generation time (T ) as per themethod of Howe (1953), Andrewartha
& Birch (1954) andSlobodkin (1962). Population doubling time
(DT ) was alsocalculated (Yurttas & Alten, 2006). The equations
used forthese calculations were as follows:
1 age-specific survivorship: lx = yx/y0, where yx = thenumber of
males or females alive on each day, x;
2 life expectancy at emergence: ex = Tx/lx , where Tx =wx=1 Lx
and Lx = (lx + lx+1 )/2, where w = the day on
which the last individual died;3 net reproductive rate: R0 =
wx=1 lxmx , where mx =
mean number of eggs/2 (i.e. assuming a 1 : 1 sex ratiofor
progeny, the mean number of eggs is divided by 2 togive the number
of female eggs;
4 mean generation time: T =WX=1 xlxmx/R0;5 intrinsic rate of
increase: rm = log e R0/T , where log e
is the natural logarithm;6 finite rate of increase: = anti-log
erm , and7 doubling time: DT = (loge2)/rm.
Percentages of apparent mortality of each life stage
(percent-age of dead individuals out of the total number of
individualsthat entered that stage) and actual mortality
(percentage ofdead individuals in a particular stage out of the
total num-ber of individuals at the beginning of that generation)
for each
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
4 D. S. Suman et al.
developmental stage (i.e. eggs, larvae, pupae and adults)
werecalculated (Southwood, 1978). The sex ratio (female :
male)(Maharaj, 2003), egg-hatching period and periods from
egglaying to development of larvae, pupae and adults were
alsocalculated.
In order to compare findings among all the strains, all
thebiological and life-table parameters of these strains were
sub-jected to analysis of variance (anova) to obtain the
leastsignificant difference (LSD) at P < 0.05. Regression
analy-sis was conducted to reveal the relationship between
fecundity(Y-function; i.e. eggs/female, egg rafts/female and
eggs/eggraft) and age of female mosquitoes (X-function). The range
ofannual temperature (difference between minimum winter andmaximum
summer temperatures) and the mean annual rain-fall for the study
areas were correlated with various life-tableattributes. Cluster
analysis with the nearest neighbour methodand the squared Euclidean
distance metric method (Krebs,1989) (statgraphics Plus 5.0;
StatPoint Technologies, Inc.,Warrenton, VA, U.S.A.) was used to
assess degrees of similar-ity among different strains according to
14 important life-tableand biological attributes of immature and
adult stages, includ-ing actual mortality (percentages) of eggs,
larvae and pupae,rate of adult emergence, female : male ratio,
total egg produc-tion by cohort, eggs laid per female per day, life
expectanciesof males and females, R0, rm , , T and DT. For the
analysisof r-strategy, the ex of females, and the rm , and DT of
allstrains including LAB, were considered.
Results
Mortality in different stages of immature Cx.
quinquefasciatus
The actual and apparent percentages of egg mortality(Table 1)
were highest in BKN (19.5%) and lowest in JDand BTH (4.4%). On
these parameters, JD and BTH differedsignificantly from LAB, BKN
and JMN. The LAB straindiffered significantly from BKN, but not
from JMN.
The rank order of the various strains by percentage of
actualmortality in the larval stages was JMN < JD < LAB <
BTH< BKN (Table 1). Statistically significant differences in
per-centages of both apparent and actual mortality were
observedamong LAB, BKN and JMN. However, LAB did not
showsignificant differences from JD and BTH for either
parameter.Differences between JMN and BTH were significant for
thepercentage of actual mortality, but not for the percentage
ofapparent mortality.
The highest percentages for actual and apparent pupal mor-tality
were recorded in JD and the lowest in BTH (Table 1).Both of these
strains differed significantly from the otherstrains in this
respect.
The rank order of the various strains for adult emergencewas BKN
< LAB < JD < JMN < BTH; rates ranged from42.0% to 74.0%
(Table 1). The female : male ratio was >1.0in all strains except
BTH (Table 1).
Developmental period for different stagesof Cx.
quinquefasciatus
Only LAB and BTH differed significantly from one anotheron
length of egg-hatching period. The minimum and maximumperiods from
egg laying to the development of pupae occurredin BKN and JD,
respectively. The minimum and maximumperiods from egg laying to
adult emergence occurred in LABand JD, respectively (Table 1).
Survival of adult mosquitoes
Overall, females lived longer than males (Figs 2 and 3,Table 2).
Life expectancies at emergence (ex ) of males dif-fered
significantly among all strains, except between JMN andJD, and BTH
and LAB. In females, ex differed significantlyamong all strains,
except between BKN and LAB.
Table 1. Mortality rates and other developmental parameters in
immature Culex quinquefasciatus of four strains from different
geographical areasand a strain raised under laboratory
conditions.
ParametersLAB strain,mean SE
JD strain,mean SE
BKN strain,mean SE
JMN strain,mean SE
BTH strain,Mean SE LSD
Eggs hatching, % 86.7 1.21a 95.6 0.55b 80.5 2.40a 85.9 8.50a
95.6 2.10b 7.50Mortality ratesEggs % actual and apparent 13.3 1.21a
4.4 0.55b 19.5 2.37c 18.1 3.90ac 4.4 2.10b 5.28Larvae % actual 14.5
0.60a 13.0 1.13a 32.3 2.89b 6.6 1.02c 17.2 3.05a 4.39
% apparent 16.7 0.71a 13.6 1.25ac 40.1 4.23b 8.1 1.65c 15.2
6.94ac 8.08Pupae % actual 7.7 0.43a 14.8 0.59b 6.3 0.88a 7.0 1.18a
4.4 0.48ac 1.83
% apparent 10.6 0.49a 17.9 1.68b 13.1 2.16a 9.4 2.04a 5.0 1.62c
3.93Developmental parametersEgg-hatching period, days 1.5 0.22a 1.8
0.51ab 1.7 0.1ab 2.0 0.36ab 2.4 0.58b 0.87Eggpupa period, days 10.0
0.71ab 11.8 0.51b 8.8 1.50a 9.5 1.52ab 9.3 0.51ab 2.55Eggadult
period, days 11.6 0.22a 14.8 0.51b 11.7 0.58a 12.0 0.36a 12.2 0.36a
0.97% adult emergence 64.5 1.05a 67.7 1.57ac 42.0 4.46b 68.3 5.88a
74.0 5.56c 9.33Sex ratio (female : male) 1.1 0.05a 1.0 0.04ac 1.2
0.06b 1.1 0.06a 1.0 0.03c 0.12Mean values within rows indicated by
same letter do not differ significantly.LAB, laboratory; JD,
Jodhpur; BKN, Bikaner; JMN, Jamnagar; BTH, Bathinda; SE, standard
error; LSD, least significant difference.
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
Culex quinquefasciatus life tables 5
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
1 5 9 13 17 21 25 29 33 37 41 45 49 53 57 61Days
lx
Lab JD BKN JMN BTH
Fig. 2. Survival of males in the LAB, JD, BKN, JMN and BTH
strainsof Culex quinquefasciatus.
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
1 5 9 13 17 21 25 29 33 37 41 45 49 53 57 61Days
lx
Lab JD BKN JMN BTH
Fig. 3. Survival of females in the LAB, JD, BKN, JMN and
BTHstrains of Culex quinquefasciatus.
Oviposition schedule
Only JD differed significantly from the rest of the strains
inoviposition days. No significant differences were recorded
forpre- and post-oviposition days in any strain (Table 2).
Fecundity
The rank order of the various strains for egg productionby
cohort of 50 females was LAB < BKN < BTH < JD< JMN,
with significant differences among strains (Table 2).The highest
and lowest numbers of egg rafts were produced byJMN and LAB,
respectively. Significant differences in egg raftproduction were
observed among all strains, except betweenBTH and LAB. The number
of eggs per egg raft was highestin BTH (n = 207.5) and lowest in
JMN (n = 161.1), withsignificant differences among all field
strains, but not betweenLAB and BKN or JMN. The largest (mean 317.3
eggs/raft) andthe smallest (mean 73.0 eggs/raft) were recorded in
BKN. Nosignificant differences were recorded among all field
strains forlargest and smallest egg rafts, except for BTH for the
smallestegg rafts. The number of eggs/female lifespan was greatest
inBTH (812.3 eggs) and least in LAB (512.4 eggs), and
variedsignificantly among strains. Eggs/female/day ranged from
20.5(LAB) to 30.8 (BTH), showing some significant
differencesbetween strains.
Effect of ageing on fecundity
Regression slopes indicate that the mean number of egg raftsper
female (Table 3, Fig. 4) and the mean number of eggs perfemale
(Table 4, Fig. 5) increased significantly with increasingage of
females in all strains except JD. Reductions in the meannumber of
eggs per raft with increasing age of females werevariable across
the strains (Table 5, Fig. 6).
Adult life-table attributes
All strains differed significantly from one another in thenet
reproductive rate (R0) (Fig. 7), with the maximum occur-ring in JMN
(162.2) and the minimum in LAB (107.6). Theintrinsic (rm ) and
finite () rates of increase were least inLAB and greatest in BTH,
with significant differences between
Table 2. Comparison of biological attributes in Culex
quinquefasciatus of four strains from different geographical areas
and a strain raised underlaboratory conditions.
ParametersLAB strain,mean SE
JD strain,mean SE
BKN strain,mean SE
JMN strain,mean SE
BTH strain,mean SE LSD
Pre-oviposition, days 7.0 1.00a 6.3 0.58a 6.7 0.58a 8.0 1.73a
7.3 0.58a 2.47Oviposition, days 25.3 0.58a 21.0 1.00b 25.7 1.15a
24.7 2.08a 26.3 0.58a 2.67Post-oviposition, days 7.3 0.58a 6.7
1.15a 4.7 0.58a 4.0 2.65a 5.3 0.58a 3.42Total egg raft production
by cohort 63.4 2.08a 80.0 1.00b 74.3 3.51c 100.7 2.89d 65.3 0.58a
5.45Largest egg raft 276.3 35.80a 308.0 20.07ab 317.3 19.14b 287.7
2.31ab 310.3 8.08b 32.52Smallest egg raft 83.7 3.51a 74.7 0.58ab
73.0 5.20b 77.0 1.73ab 95.3 5.77c 9.82Eggs per egg raft 169.1
2.99ab 186.3 3.49c 170.2 5.16a 161.1 2.64b 207.5 0.92d 8.03Total
egg production/cohort 10 763 196a 14 903 320b 12 639 213c 16 218
196d 13 560 129e 533Eggs/female/day 20.5 0.26a 28.2 0.77b 20.5
1.91a 27.9 2.13b 30.8 0.50c 2.38Eggs/female lifespan 512.4 6.64a
573.9 1.67b 552.4 12.80c 684.3 3.67d 812.3 4.66e 17.39Life
expectancy (ex ) (at emergence), days 21.2 0.15a 19.2 0.21b 18.2
0.38c 19.8 1.02b 21.3 0.40a 0.97Life expectancy (ex ) (at
emergence), days 27.4 0.16a 30.8 0.28b 28.0 0.40a 36.9 0.70c 25.2
0.60d 0.81Mean values within rows indicated by same letter do not
differ significantly.LAB, laboratory; JD, Jodhpur; BKN, Bikaner;
JMN, Jamnagar; BTH, Bathinda; SE, standard error; LSD, least
significant difference.
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
6 D. S. Suman et al.
Table 3. Regression analysis for number of egg rafts/female (Y)
as a function of age (X) of females in Culex quinquefasciatus of
four strainsfrom different geographical areas and a strain raised
under laboratory conditions.
Strain Source of variation Mean square Regression equation d.f.
F-ratio P -value
LAB Regression 0.0424 Y = 0.0140 + 0.0026X 1 12.67
0.0011Residual 0.00335 34
JD Regression 0.00848 Y = 0.0665 + 0.0011X 1 2.39 0.1327Residual
0.00354 29
BKN Regression 0.07664 Y = 0.0002 + 0.0038X 1 12.58
0.0012Residual 0.00609 34
JMN Regression 0.13987 Y = 0.00588 + 0.004X 1 22.33
0.0001Residual 0.00626 31
BTH Regression 0.20294 Y = 0.06088 + 0.0072X 1 21.79
0.0001Residual 0.00931 31
LAB, laboratory; JD, Jodhpur; BKN, Bikaner; JMN, Jamnagar; BTH,
Bathinda.
(E)
Bathinda strain BTH
Egg
rafts
/fem
ale
0 10 20 30 40 500
0.1
0.2
0.3
0.4
0.5
0.6Y = -0.061 + 0.0072X
(C)
Bikaner strain BKN
Egg
raft/
fem
ale
0 10 20 30 40 500
0.1
0.2
0.3
0.4Y = 0.002 + 0.0038X
(D)
Jamnagar strain JMN
Egg
rafts
/fem
ale
0 20 40 60 800
0.1
0.2
0.3
0.4
0.5Y = -0.0059 + 0.004X
(A)
Laboratory strain LAB
Age of female, Days
Egg
rafts
/fem
ale
0 10 20 30 40 50 600
0.05
0.1
0.15
0.2
0.25Y = 0.0140 + 0.0026X
(B)
Jodhpur strain JD
Age of female, Days
Age of female, Days
Age of female, Days
Age of female, Days
Egg
raft/
fem
ale
0 10 20 30 40 50 600
0.04
0.08
0.12
0.16
0.2
0.24 Y= 0.0666 + 0.0011X
Fig. 4. Regression line between egg rafts per female and age of
female (days) in Culex quinquefasciatus in (A) LAB, (B) JD, (C)
BKN, (D) JMNand (E) BTH strains.
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
Culex quinquefasciatus life tables 7
Table 4. Regression analysis for number of eggs/female (Y) as a
function of age (X) of females in Culex quinquefasciatus of four
strains fromdifferent geographical areas and a strain raised under
laboratory conditions.
Strain Source of variation Mean square Regression equation d.f.
F-ratio P -value
LAB Regression 594.577 Y = 5.7396 + 0.3168X 1 5.15 0.029Residual
115.374 33
JD Regression 142.008 Y = 13.8519 + 0.1612X 1 1.07
0.3107Residual 133.205 28
BKN Regression 840.04 Y = 4.6648 + 0.4075X 1 6.06 0.019Residual
138.514 34
JMN Regression 2328.9 Y = 2.5433 + 0.5467X 1 14.51
0.0006Residual 160.481 31
BTH Regression 7102.28 Y = 9.720 + 1.3603X 1 15.65
0.0004Residual 453.736 31
LAB, laboratory; JD, Jodhpur; BKN, Bikaner; JMN, Jamnagar; BTH,
Bathinda.
(E)
Bathinda strain BTH
Age of female, Days
Egg/
fem
ale
0 10 20 30 40 500
30
60
90
120
150Y = -9.720 + 0.1.360X
(C)
Bikaner strain BKN
Age of female, Days
Eggs
/fem
ale
0 10 20 30 40 500
10
20
30
40
50
60Y = 4.6648 + 0.4075X
(D)
Jamnagar strain JMN
Age of female, Days
Eggs
/fem
ale
0 20 40 60 800
20
40
60
80Y = 2.5433 + 0.5467X
(A)
Laboratory strain LAB
Age of female, Days
Eggs
/fem
ale
0 10 20 30 40 50 600
10
20
30
40
50Y= 5.7396 + 0.3168X
(B)
Jodhpur strain JD
Age of female, Days
Eggs
/fem
ale
0 10 20 30 40 50 600
10
20
30
40
50Y = 13.851 + 0.1612X
Fig. 5. Regression line between eggs per female and age of
female (days) in Culex quinquefasciatus in (A) LAB, (B) JD, (C)
BKN, (D) JMN and(E) BTH strains.
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
8 D. S. Suman et al.
Table 5. Regression analysis for number of eggs/egg raft (Y) as
a function of age (X) of females in Culex quinquefasciatus of four
strains fromdifferent geographical areas and a strain raised under
laboratory conditions.
Strain Source of variation Mean square Regression equation d.f.
F-ratio P -value
LAB Regression 4427.62 Y = 145.155 0.8647X 1 1.27 0.268Residual
3488.81 33
JD Regression 189.155 Y = 126.537 0.1788X 1 0.08 0.780Residual
2397.94 29
BKN Regression 20 985.8 Y = 173.792 2.0369X 1 7.79 0.008Residual
2694.96 34
JMN Regression 3614.83 Y = 141.675 0.6811X 1 1.56 0.2217Residual
2323.96 31
BTH Regression 1824.54 Y = 187.838 0.6894X 1 0.36 0.5540Residual
5097.64 31
LAB, laboratory; JD, Jodhpur; BKN, Bikaner; JMN, Jamnagar; BTH,
Bathinda.
(E)
Bathinda strain BTH
0 10 20 30 40 500
50
100
150
200
250
300Y = 187.83-0.6864X
Eggs
/egg
raft
(C) (D)
Jamnagar strain JMN
0 20 40 60 800
40
80
120
160
200
240Y = 141.675-0.6811X
Eggs
/egg
raft
Bikaner strain BKN
0 10 20 30 40 500
50
100
150
200
250
300Y =173.792-2.0369X
Eggs
/egg
raft
(B)
Jodhpur strain JD
Age of female, Days0 10 20 30 40 50 60
0
40
80
120
160
200
240Y=126.537-0.1788X
Eggs
/egg
raft
(A)
Laboratory strain LAB
Age of female, Days
Age of female, DaysAge of female, Days
Age of female, Days
0 10 20 30 40 50 600
40
80
120
160
200
240Y = 145.155-0.8647X
Eggs
/egg
raft
Fig. 6. Regression line between eggs per egg raft and age of
female (days) in Culex quinquefasciatus in (A) LAB, (B) JD, (C)
BKN, (D) JMNand (E) BTH strains.
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
Culex quinquefasciatus life tables 9
020406080
100120140160180
1 6 11 16 21 26 31 36 41 46 51 56 61Days
Net
repr
oduc
tion
rate
Lab JD BKN JMN BTH
Fig. 7. Cumulative net reproductive rate (R0) in Culex
quinquefascia-tus in the LAB, JD, BKN, JMN and BTH strains.
JD and BKN and between BTH and JMN, but no
significantdifferences between JD and BTH or between BKN and
JMN.The mean generation time (T ) was longest in LAB and shortestin
BTH. The LAB strain differed significantly from JD andBTH for T ,
but not from BKN and JMN. The longest doublingtime (DT ) was
observed in LAB, followed by JMN, BKN, JDand BTH, but the
differences between strains was not alwayssignificant (Table
6).
Cluster analysis
Analysis of all Cx. quinquefasciatus strains indicated
twoclusters, consisting of BKN and LAB, and JD, BTH andJMN,
respectively (Fig. 8). The distance between the clus-ters was
22.20. Cluster analysis also indicated a closerrelationship between
JD and BTH than between JMNand BKN.
Correlation analysis between environmental factorsand life-table
attributes
Table 7 indicates that annual temperature ranges in the
fourfield locations were strongly correlated with egg
production,female life expectancy, R0, rm , and T (0.770.97).
Meanannual rainfall also correlated strongly with egg
production,
Table 6. Comparison of adult life-table attributes in Culex
quinquefasciatus of four strains from different geographical areas
and a strain raisedunder laboratory conditions.
ParametersLAB strain,mean SE
JD strain,mean SE
BKN strain,mean SE
JMN strain,mean SE
BTH strain,mean SE LSD
R0 107.6 1.96a 147.4 2.83b 122.9 7.89c 162.2 1.96d 135.6 1.29e
8.76rm 0.15 0.00a 0.20 0.00b 0.17 0.00c 0.16 0.01ac 0.21 0.02b 0.02
1.16 0.00a 1.23 0.00b 1.18 0.00a 1.17 0.01a 1.24 0.02b 0.02T 31.6
0.80a 24.5 0.38b 28.8 0.70a 31.4 2.08a 22.9 1.67b 2.94DT 4.7 0.11a
3.4 0.05b 4.1 0.05c 4.3 0.28c 3.2 0.24b 0.24Mean values within rows
indicated by same letter do not differ significantly.LAB,
laboratory; JD, Jodhpur; BKN, Bikaner; JMN, Jamnagar; BTH,
Bathinda; SE, standard error; LSD, least significant difference;
R0, netreproductive rate; rm , intrinsic rate of increase; , finite
rate of increase; T , mean generation time; DT, doubling time.
female life expectancy and R0 (0.850.91), but relativelyweakly
with rm , and T (0.460.59).
Comparison of r-strategy among the different strains
Among the different field strains, JMN had the longestfemale
survival period, DT and the lowest rm and incomparison with BTH,
BKN and JD, indicating that JMNwas superior in r-strategy. LAB
appeared to be a weakerr-strategist than all the field strains
because it required thelongest DT and had the least rm and .
Discussion
The life-table parameters and other biological attributes infive
strains of Cx. quinquefasciatus originating from
differentgeographical areas varied with ecological conditions.
Apparent and actual mortality in eggs was found to rangefrom
4.4% (JD and BTH) to 19.5% (BKN); values in the othertwo strains
were relatively close to that in BKN. Rates of actualmortality of
larval stages ranged from 6.6% (JMN) to 32.3%(BKN), with values for
the other strains falling between theseextremes. The cumulative
effect of mortalities of eggs, larvaeand pupae resulted in lower
rates of adult emergence, rangingfrom 42.0% (BKN) to 74.0% (BTH);
values for the otherstrains fell within 10% of that for BTH. The
high mortality inBKN may be associated with its habitat, which is
very proneto drought and is almost completely characterized by
desertconditions. By contrast, JMN has a significantly higher rate
ofadult emergence than BKN despite a non-significant differencein
egg hatching because the conditions in which it lives providebetter
support for larval and pupal development. In otherstudies, rates of
adult emergence were low for four strains ofAnopheles sacharovi
Favr (Diptera: Culicidae) (11.414.6%)(Yurttas & Alten, 2006),
but exceeded 50% from first instarsof field-collected Anopheles
gambiae Giles s.s. from BurkinaFaso (Lehmann et al., 2006). These
studies revealed thatvariations in immature mosquito developmental
rates dependon habitat conditions.
The percentage of eggs hatching has been reported tobe 82.1% in
Culex pipiens fatigans (synonymous withCx. quinquefasciatus; Gomez
et al., 1977) and 79.6% in
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
10 D. S. Suman et al.
0
4
8
12
16
20
24D
ista
nce
Lab JD
BKN
JMN
BTH
Fig. 8. Dendrogram of the four field strains (JD, BKN, JMN
andBTH) and a laboratory strain (LAB) of Culex
quinquefasciatusshowing similarities in various life-table
attributes. The distancecoefficient is measured using a squared
Euclidean method.
Table 7. Correlation analysis of various life-table and
biologicalattributes for the JD, BKN, JMN and BTH strains of
Culexquinquefasciatus for temperature range and mean annual
rainfall.
Correlation coefficient (r )Attributes Temperature range Mean
annual rainfall
Egg production/cohort 0.79 0.90Female life expectancy 0.97
0.86R0 0.76 0.91rm 0.82 0.51 0.77 0.46T 0.87 0.59
R0, net reproductive rate; rm , intrinsic rate of increase; ,
finite rate ofincrease; T , mean generation time.
Cx. quinquefasciatus (Suleman & Reisen, 1979), which
areclose to the values reported in the present study (Table
1).Variations in percentages of eggs hatching have also
beenrecorded in Cx. tritaeniorhynchus, for which higher
ratesemerged in Indian subcontinental strains (93.0%) than ina
Japanese strain (78.8%) (Reisen et al., 1979).
However,significantly lower egg-hatching rates were recorded in
fourstrains of An. sacharovi from southeastern Anatolia,
Turkey,leading to high overall real mortality rates
(85.488.6%;Yurttas & Alten, 2006). The eggs of strains
collectedin the present study from the most arid environments(BKN,
JD) required a shorter hatching period than thoseof semi-arid
strains (JMN, BTH), which suggests that shorthatching times may be
a positive factor for survival in aridconditions.
In the present study, the mean development time from eggto adult
was found to vary little, with four of the strainsshowing a range
of
-
Culex quinquefasciatus life tables 11
Numbers of eggs/raft varied significantly among strains ofCx.
quinquefasciatus (Table 2), ranging from 161.1 (JMN) to207.5 (BTH),
whereas the mean number of rafts/cohort wasnearly opposite, ranging
from 65.3 (BTH) to 100.7 (JMN). Thisis not surprising because high
numbers of eggs/raft probablyreflect the production of relatively
few rafts/female and viceversa. The construction of large egg rafts
may consume morereproductive energy and time than the construction
of smalleregg rafts and thus females that laid small egg rafts
wereable to produce more eggs over their lifetime.
Significantdifferences in mean numbers of eggs/raft were observed
amongall four field-collected strains, but values in BKN and JMNdid
not differ significantly from that in LAB. Variations inthe mean
number of eggs/raft among different strains of Culexmosquitoes have
been reported previously (Walter & Hacker,1974; Reisen et al.,
1979, 1984).
Interestingly, the strains from areas with the greatestrange of
annual temperatures (Bathinda, Bikaner and Jodh-pur) face tougher
conditions for survival in nature and thesemosquitoes typically had
a shorter female life expectancy(25.230.8 days), laid eggs on most
days (21.026.3 days) andconstructed larger egg rafts (170.2207.5
eggs/raft), indicatingthat these strains invest the most energy in
rapid reproduction.By contrast, the Jamnagar strain, which comes
from the areawith the smallest range of annual temperatures and
hence moreoptimal conditions for mosquitoes, had the longest female
lifeexpectancy (mean: 36.9 days), but a shorter oviposition
period(mean: 24.7 days) and laid fewer eggs/raft (mean: 161.1).
Fox& Czesak (2000) reviewed the evolutionary ecology of
progenysize and concluded that more hostile environmental
conditionsmay favour the production of a greater number of
offspringin order to increase the probability that some will
survive toadulthood. Thus, individuals from unfavourable
environmentsare inherently committed to put maximum effort into the
pro-duction of more offspring to ensure that an adequate
numbersurvive to reproduce in their turn.
In the present investigation, the mean number of eggrafts/female
(Fig. 4, Table 3) and the mean number ofeggs/female (Fig. 5, Table
4) increased with female age. Themean number of eggs/raft, however,
decreased with femaleage (Fig. 6, Table 5). These observations
indicate that cumu-lative fecundity increased as a function of
female age asa result of an increase in the frequency of the
depositionof progressively smaller rafts. Similarly, Walter &
Hacker(1974) found the number of eggs/raft to decrease with
increas-ing age in a range of geographically distinct strains ofCx.
quinquefasciatus. Suleman & Reisen (1979) recorded sim-ilar
observations in Cx. quinquefasciatus and Reisen et al.(1984) did so
in Cx. tarsalis.
Species with relatively high net reproductive rates (R0) tendto
have a competitive advantage over sympatric species thatoccupy
similar ecological niches. Gubler (1970) observed thecompetitive
displacement of Aedes polynesiensis Marks byAedes albopictus
(Skuse) (Diptera: Culicidae), and showedthat the latter species was
superior in female survival and netreproductive rate. In the
present investigations, the R0 values inall wild strains
(122.9162.2) were significantly greater than inLAB (107.6) and
differed significantly amongst one amother,which suggests that
varying degrees of fitness of the wild
strains may have been imposed by different levels of
selectionpressure on the reproductive rate for each strain.
Similarly,significant differences in R0 for Cx. quinquefasciatus
havebeen reported in strains from Bangkok (8.1), Vero Beach
(24.3)and Houston (37.7) (Walter & Hacker, 1974), from
Caracas,Venezuela (80.7) (Gomez et al., 1977) and from
Peshawar,Pakistan (58.6) (Suleman & Reisen, 1979); however
thesevalues are all lower than those found in the present
study.Reisen et al. (1979) observed variations inR0 in nine
strainsof Cx. tritaeniorhynchus, with the highest values reported
instrains from Karachi (98.5) and Taipei (84.9), and the
lowestreported in three strains from Japan (14.431.2). The
presentand referenced data show a consistent trend for
mosquitopopulations in colder climates to have lowerR0 values
thanpopulations in warmer climates. Yurttas & Alten (2006)
alsofound significant differences in R0 (range: 3.212.8)
amongdifferent strains of An. sacharovi, which are again, lower
thanthose in the present study.
In the current study, differences in rm (0.150.21), (1.161.24)
and DT (3.234.67) were observed amongthe various strains of Cx.
quinquefasciatus and some ofthese differences were significant.
Similarly, Walter &Hacker (1974) found significant differences
in rm betweena Cx. quinquefasciatus strain from Bangkok and two
otherstrains (Vero Beach and Houston), although the latter
twostrains did not differ significantly in rm from each other.The
rm values in LAB, BKN and JMN are closest to thatin the Caracas
strain of Cx. p. fatigans (Gomez et al., 1977),but much higher than
the value in the Peshawar strain ofCx. quinquefasciatus (Suleman
& Reisen, 1979). Reisen et al.(1979) reported greater
differences in rm among various strainsof Cx. tritaeniorhynchus
from the Indo-Pakistani subcontinent(0.160.19) and Taiwan (0.18)
than among Japanese strains(0.080.12). This appears to reflect a
greater need on the partof the Japanese strains for a longer mean
generation period(28.229.8 days) than the Indo-Pakistani (22.224.1
days) andTaiwanese (24.0 days) strains. A comparison of these
dataindicates that warmer climates have a positive effect on rm
,increasing inherent capacity for reproduction.
In the present study, the mean generation time (T ) rangedfrom
22.9 days to 31.6 days among the various strains ofCx.
quinquefasciatus. Higher values for T (39.6 days and44.7 days) were
recorded by Gomez et al. (1977) and Suleman& Reisen (1979) and
lower values by Walter & Hacker (1974)in the Bangkok (32.1),
Vero Beach (26.8) and Houston (28.5)strains of Cx.
quinquefasciatus.
The cluster analysis of various life-table and
biologicalattributes of the four wild strains of Cx.
quinquefasciatusrevealed that JD was biologically closer to BTH
than to BKNand JMN, which may reflect cumulative differences in
theirrespective ecologies.
Although Bathinda (BTH) and Jamnagar (JMN) are 1000km apart,
they both lie in the same semi-arid zone. Averageannual rainfall is
greater in Jamnagar than in Bathinda and RHis also greater for most
of the year in Jamnagar as a resultof its coastal location. The
range of annual temperatures isnarrower for Jamnagar than Bathinda.
Accordingly, we mightexpect that environmental conditions in
Jamnagar would favoursurvival and reproductive potential and would
support a shorter
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
12 D. S. Suman et al.
egg-hatching period (1.96 days), longer female life
expectancy(36.9 days), a higher net reproductive rate (162.2) and a
longermean generation time (31.4 days) than conditions in BTH(2.42
days, 25.2 days, 135.6 days and 22.9 days, respectively).
Jodhpur and Bikaner both lie in arid zones. Although Jodh-pur
has relatively higher rainfall than Bikaner, these siteswould be
expected to be less favourable than Jamnagar andBathinda for
mosquito survival and reproduction. The positivecorrelations
between rainfall and various life-table parame-ters for the wild
strains indicate that environmental factorsdo indeed have an
important evolutionary effect on mosquitolife strategies that can
be detected even after several gen-erations of colonization. The
JD, BKN and BTH strains ofCx. quinquefasciatus have relatively low
DT as a result ofhigher rm and , which perhaps reflects adaptations
to moreextreme environmental conditions than occur in
Jamnagar,whereas the JMN strain had lower rm and values and
higherDT, despite high R0 and T values. By contrast, the LAB
strainhad a relatively high DT value as a result of having the
low-est R0, rm and in comparison with the four wild
strains.Crovello & Hacker (1972) also reported variation in the
repro-ductive potential of 13 strains of Aedes aegypti L. from a
rangeof habitats and found forest strains to show the lowest
repro-ductive potential as a result of more homogeneous levels
ofenvironmental stress than found in urban and semi-urban
areas,where there is a greater degree of fluctuation in
environmentalconditions. The evolution of an r-strategy has been
describedfor Cx. quinquefasciatus by Rabinovich (1974) and
supportedby Gomez et al. (1977) and Suleman & Reisen (1979).
Reisenet al. (1979) also showed that strains of Cx.
tritaeniorhynchusfrom Taiwan and the Indo-Pakistan subcontinent
were morer-selected as a result of the more variable ecological
sys-tems in which they live compared with Japanese strains,
whichoriginated from more stable, cooler and more humid
maritimeclimates. These strains of Cx. tritaeniorhynchus were
lesser r-strategists than domestic species, such as Cx.
quinquefasciatusand Ae. aegypti (Schlosser & Buffington, 1977).
Analysis ofthe various parameters in the present study indicates
that,among the wild strains, BTH, BKN and JD are more
efficientr-strategists as they face more difficult environmental
con-ditions than does JMN, which exists in more
homogeneousenvironmental conditions. Interestingly, Suman et al.
(2009)showed the JMN strain to differ from the JD, BKN and
BTHstrains of this mosquito for various egg-related attributes.
Fur-thermore, higher R0, rm and values and lower T and DTvalues
were observed in the wild strains than in LAB, which isconsistent
with the hypothesis that harsher environmental con-ditions select
for high r-strategists in the field. Strains with highr-strategies
may be more difficult to control because, when apopulation is
diminished, it is able to re-establish more quicklythan a less able
r-strategist.
The results of this study extend our knowledge of the impactof
the environment on a wide range of life history traits in
localpopulations of disease vectors. The study also provides
detailedinformation which is valuable for increasing the accuracy
ofthe population dynamic models that are an essential componentof
the decision-making tools used to plan and monitor vectorcontrol
programmes (World Health Organization, 2004).
Acknowledgements
We thank Dr R Vijayaraghavan, Director, Defence Researchand
Development Establishment, Gwalior, for his support andinterest in
this work.
References
Andrewartha, H.G. & Birch, L.C. (1954) The Distribution and
Abun-dance of Animals. University of Chicago Press, Chicago,
IL.
Bancroft, T.L. (1899) On the metamorphosis of the young formof
Filaria bancrofti Cobb. Journal and Proceedings of the RoyalSociety
of New South Wales, 82, 6265.
Belen, A. & Alten, B. (2006) Variation in the life-table
characteristicsamong populations of Phlebotomus papatasi at
different altitudes.Journal of Vector Ecology, 31, 3544.
Chandra, G., Chatterjee, S.N., Banerjee, B.D. & Majumdar, G.
(1997)Effect of seasonal variations on the development of
Wuchererialarvae in Culex quinquefasciatus. Basic and Applied
Biomedicine,5, 2124.
Costero, A., Edman, J.D., Clark, G.G. & Scott, T.W. (1998)
Life tablestudy of Aedes aegypti (Diptera: Culicidae) in Puerto
Rico fedonly human blood plus sugar. Journal of Medical Entomology,
35,809813.
Crovello, T. & Hacker, C. (1972) Evolutionary strategies in
life tablecharacteristics among feral and urban strains of Aedes
aegypti.Evolution, 26, 185196.
Day, J.F., Edman, J.D. & Scott, T.W. (1994) Reproductive
fitness andsurvivorship of Aedes aegypti (Diptera: Culicidae)
maintained onblood, with field observations from Thailand. Journal
of MedicalEntomology, 3, 611617.
Fox, C.W. & Czesak, M.E. (2000) Evolutionary ecology of
progenysize in arthropods. Annual Review of Entomology, 45,
341369.
Gomez, C., Rabinovich, J.E. & Machado-Allison, C.E. (1977)
Popu-lation analysis of Culex pipiens fatigans Weid. (Diptera:
Culicidae)under laboratory conditions. Journal of Medical
Entomology, 13,453463.
Gubler, D.J. (1970) Comparison of reproductive potentials of
Aedes(Stegomyia) albopictus Skuse and Aedes (Stegomyia)
polynesiensisMarks. Mosquito News, 30, 201209.
Howe, R.W. (1953) The rapid determination of the intrinsic rate
ofincrease of an insect population. Annals of Applied Biology,
40,134151.
Jinfu, W., Shaohong, L., Rui, C. & Lingling, W. (1998)
Relativefitness of three organophosphate-resistant strains of Culex
pipienspallens (Diptera: Culicidae). Journal of Medical Entomology,
35,716719.
Krebs, C.J. (1989) Ecological Methodology. Harper Collins
Publishers,New York, NY.
Lehmann, T., Dalton, R., Kim, E.H., Dahl, E., Diabate, A.,
Dabire, R.& Dujardin, J.P. (2006) Genetic contribution to
variation in larvaldevelopment time, adult size, and longevity of
starved adults ofAnopheles gambiae. Infection, Genetics and
Evolution, 35, 410416.
Maharaj, R. (2003) Life table characteristics of Anopheles
arabiensis(Diptera: Culicidae) under simulated seasonal conditions.
Journal ofMedical Entomology, 40, 737742.
Mahmood, F., Reisen, W.K., Chiles, R.E. & Fang, Y. (2004)
Westernequine encephalomyelitis virus infection affects the life
tablecharacteristics of Culex tarsalis (Diptera: Culicidae).
Journal ofMedical Entomology, 41, 982986.
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x
-
Culex quinquefasciatus life tables 13Manson-Bahr, P.E.C. &
Bell, D.R. (2003) Mansons Tropical Disease.
ELBS Publishers, London.Rabinovich, J.E. (1974) Demographic
strategies in animal populations:
a regression analysis. Tropical Ecological Systems,
EcologicalStudies, Vol. 11 (ed. by F. B. Golley & E. Medina),
pp. 1940.Springer-Verlag, New York, NY.
Reisen, W.K. & Milby, M.M. (1987) Studies on autogeny in
Culextarsalis : 3. Life table attributes on autogenous and
anautogenousstrains under laboratory conditions. Journal of the
AmericanMosquito Control Association, 3, 619625.
Reisen, W.K., Siddiqui, T.F., Aslam, Y. & Malik, G.M. (1979)
Geo-graphic variation among the life table characteristics of Culex
tri-taeniorhynchus from Asia. Annals of the Entomological Society
ofAmerica, 72, 700709.
Reisen, W.K., Milby, M.M. & Bock, M.E. (1984) Effects of
immaturestress on selected events in the life history of Culex
tarsalis.Mosquito News, 44, 385395.
Schlosser, I.J. & Buffington, J.D. (1977) The energetics of
r - and k -selection in two African strains of Aedes aegypti.
Annals of theEntomological Society of America, 70, 196202.
Sirivanakaran, S. (1976) Medical entomology studies III. A
revisionof the subgenus Culex in the Oriental region (Diptera:
Culicidae).Contributions of the American Entomological Institute,
12, 1272.
Slobodkin, L.B. (1962) Growth and Regulation of Animal
Populations.Holt, Rinehart & Winston, New York, NY.
Southwood, T.R.E. (1978) Ecological Methods, with Particular
Refer-ences to the Study of Insect Populations, 2nd edn. John Wiley
&Sons, New York, NY.
Suleman, M. & Reisen, W.K. (1979) Culex quinquefasciatus
Say:life table characteristics of adults reared from wild-caught
pupaefrom North West Frontier Province, Pakistan. Mosquito News,
39,756762.
Suman, D.S., Shrivastava, A.R., Parashar, B.D., Pant, S.C.,
Agrawal,O.P. & Prakash, S. (2009) Variation in morphology and
morphomet-rics of eggs of Culex quinquefasciatus mosquitoes from
ecologicalregions of India. Journal of Vector Ecology, 34,
191199.
Walter, M.N. & Hacker, C.S. (1974) Variation in the life
tablecharacteristics among three geographic strains of Culex
pipiensquinquefasciatus. Journal of Medical Entomology, 11,
541550.
World Health Organization (2004) Global Strategic Frameworkfor
Integrated Vector Management, WHO/CDS/CPE/PVC/2004.10.WHO,
Geneva.
World Health Organization (2006) Global programme to
eliminatelymphatic filariasis. Weekly Epidemiological Record, 81,
22232.
Yurttas, H. & Alten, B. (2006) Geographic differentiation of
lifetable attributes among Anopheles sacharovi (Diptera:
Culicidae)populations in Turkey. Journal of Vector Ecology, 31,
275284.
Accepted 1 November 2010
2011 The AuthorsMedical and Veterinary Entomology 2011 The Royal
Entomological Society, Medical and Veterinary Entomology, doi:
10.1111/j.1365-2915.2010.00939.x