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Bulletin of Entomological Research (2003) 93, 375–381 DOI 10.1079/BER2003259
Effect of temperature on the development
of the aquatic stages of Anopheles gambiae
sensu stricto (Diptera: Culicidae)
M.N. Bayoh and S.W. Lindsay*
School of Biological and Biomedical Sciences, University of Durham,
Science Laboratories, Durham, DH1 3LE, UK
Abstract
Global warming may affect the future pattern of many arthropod-borne
diseases, yet the relationship between temperature and development has been
poorly described for many key vectors. Here the development of the aquatic stages
of Africa‘s principal malaria vector, Anopheles gambiae s.s. Giles, is described at
different temperatures. Development time from egg to adult was measured under
laboratory conditions at constant temperatures between 10 and 40°C. Rate of
development from one immature stage to the next increased at higher
temperatures to a peak around 28°C and then declined. Adult development rate
was greatest between 28 and 32°C, although adult emergence was highest between
22 and 26°C. No adults emerged below 18°C or above 34°C. Non-linear models
were used to describe the relationship between developmental rate and
temperature, which could be used for developing process-based models of malaria
transmission. The utility of these findings is demonstrated by showing that a map
where the climate is suitable for the development of aquatic stages of A. gambiae
s.s. corresponded closely with the best map of malaria risk currently available for
Africa.
Introduction
Estimating the potential impact of climate change on
malaria transmission has generated a great deal of interest
due, in part, to the concern that this debilitating disease may
emerge or re-emerge in many parts of the world (Bradley,
1993; Sutherst et al., 1995; Lindsay & Birley, 1996; Martens,
1998; Craig et al., 1999; Rogers & Randolph, 2000; Kovats et
al., 2001). There is a consensus amongst these scientists that
changes in the weather can affect malaria transmission, but
it is uncertain whether any changes in recent malaria
patterns are related to long-term changes in climate. With
the availability of detailed environmental data sets and
increased computing power, modelling climate change and
malaria transmission has never been easier. However, some
of the basic insect data on which process-based models are
constructed, such as vector survival and human-biting rate,
are lacking or poorly derived, raising concerns about the
accuracy of future scenarios.
The rate at which new individuals are produced is one
of the key factors that determine the growth rate of insect
populations. This rate is critically dependent on the
growth characteristics of immature stages, which is
governed by temperature, where food is not limiting
(Lassiter et al., 1995). The influence of temperature on
these stages has been studied in a number of different
species of mosquitoes (Diptera: Culicidae), including
Anopheles quadrimaculatus Say (Huffaker, 1944), Aedes
aegypti Linnaeus (Bar-Zeev, 1958; Tun-Lin et al., 2000),
Culex and Anopheles species (Shelton, 1973), Toxorhynchites
brevipaplis Theobald (Trips, 1972) and Wyeomyia smithii
Coquillett (Bradshaw, 1980), but not in detail in
*Author for correspondence
Fax: +44 (0)191 374 1179
E-mail: S.W.Lindsay@durham.ac.uk
anophelines (Bradshaw, 1980). In general, within the limits
of a lower development threshold and an upper lethal
temperature, the aquatic stages of mosquitoes develop
faster as temperature increases (Brust, 1967; Hagstrum &
Workman; 1971; Lyimo & Takken, 1993). The shortening of
aquatic life is important since it will increase adult
turnover, with consequences for increased vector biting
rates and disease transmission (Garett-Jones, 1964).
Importantly, the production of adult mosquitoes is not
directly proportional to the rate of development of the
aquatic stages since at temperatures that result in the fastest
rate of development, fewer adults are produced. Similarly, at
low temperatures, few adults may be produced in the field,
due to the drying up of breeding habitat, or a reduction in
numbers from predation or disease pathogens (Speight et al.,
1999), although evidence for this is rare.
Various temperature driven development models have
been used to predict the time of insect development. Where
temperatures fluctuate during the day, hourly rates can be
accumulated and converted to daily rates and then
converted to development times. A common approach is to
use the linear portion of the development rate versus
temperature curve to calculate development time, by
summing the number of thermal units (degree-hours or
degree-days) contributed at each temperature (Baskerville
& Emin, 1969; Abrami, 1972; Sevacherian et al., 1977). This
method is convenient as it requires minimal data for
formulation, it is simple to calculate and is often accurate
(Eckenrode & Chapman, 1972; Ali Niazee, 1976). However,
it is valid only over intermediate temperatures and the
threshold temperatures below or above which development
ceases are often determined by extrapolation. As a result,
the number of degree-days required for complete
development is often too low at temperatures near the
lower threshold and too high at temperatures near or above
the optimum (Howe, 1967). Several other models involving
the use of exponential equations, second and third degree
polynomials, logistic equations, modified sigmoid
equations have been developed and used with varying
degrees of success (Wagner et al., 1984).
Despite the enormous medical importance of Anopheles
gambiae Giles, the chief vector of malaria in Africa, the
relationship between temperature and their development is
poorly understood. One of the few published references is
the work of Jepson and others from Mauritius (Jepson et al.,
1947). This work describes development at mean
temperatures between 23 and 32°C at 11, markedly different,
natural-breeding sites. There were also large daily
differences in temperature between sites, varying from 4 to
12°C. This is important since developmental rates of
organisms depend both on the mean temperature and the
frequency and magnitude of any fluctuations around the
mean (Cossins & Bowler, 1987; Liu; 1990). Lyimo and
colleagues (Lyimo et al., 1992) investigated the effect of
temperature on A. gambiae development rate, but also at a
narrow temperature range (24–30°C). The aim of the present
study was to produce a mathematical expression for the
relationship between A. gambiae s.s. development rates over
a wider temperature range (10–40°C) in order to quantify
adult production at these temperatures. Maximum and
minimum thresholds for adult emergence were used to
produce a distribution map for mosquito suitability based
on climate and this was compared with the distribution of
malaria across Africa.
Materials and methods
Insect cultures
Stocks of the 16CSS strain of A. gambiae s.s., originally
from Lagos, were maintained at 26°C (± 1°C), 80% relative
humidity (± 10%) and a 12:12 h light and dark regime.
Immature stages were reared at constant temperatures
ranging from 10 to 40°C (± 1°C), with 2°C increments, under
a 12:12h light and dark regime in programmable growth
chambers (LMS cooled incubators, S.H. Scientific, UK).
Water temperature was monitored using data loggers (Tiny
Talk II, Gemini, UK, with ± 0.5°C accuracy).
Egg development
Approximately 200 adult female mosquitoes were fed on
defibrinated horse blood (Oxoid, UK) in order to produce
eggs. Sixty eggs, less than one day old, were added to 1 l of
48-h-old tap water in plastic bowls, 15 cm × 10 cm × 8 cm, in
volume. Bowls were lined with No. 1 Whatman filter paper
to prevent eggs adhering to the sides of the plastic bowl and
drying out. Each bowl was housed in an environmental
chamber at a constant temperature. Hatched larvae were
counted and removed daily until no further instars were
seen. This procedure was repeated four times for each set
temperature (five in total).
Larva and pupa development
Thirty, 2-day-old larvae from each egg tray were
dispensed into larval bowls containing 1 l of tap water and
100 ml of rearing medium. Larval bowls were the same as
the egg bowls, but without filter paper. Rearing medium
was produced by placing five whole grass plants (Festuca
spp.) with soil attached to the roots in 4 l of tap water for
48 h. Bacteria produced from the grass served as starting
food for the first instar larvae. Feeding with solid food
commenced 24 h after the hatched larvae were placed in the
rearing medium. About 10 mg of tropical fish food
(Tetramin
®
, Germany), ground into a fine powder, was
provided for each larval bowl daily. Dead larvae or pupae
were removed each day and the rearing medium replaced
every two days to prevent scum formation and the
accumulation of metabolites toxic to the insects. Larvae were
counted daily and categorized according to instar stages
(WHO, 1975).
Statistical analysis
Development time was recorded as the duration of
development of 50% of individuals for the immature stages,
and as mean emergence times for adults, in days. The rate of
development was described as the sum of the inverse of the
development times for each individual expressed as an
average. The Jonckheere-Terpstra and the Kruskal-Wallis
non-parametric tests in SPSS (Version 10.0 for Windows,
SPSS Inc., Chicago) statistical package were used,
respectively, to compare between group (temperature
regimes) and within group differences in mean development
times, while Chi-square statistics was used to compare the
number of adults produced. For between-group
comparisons, the null hypothesis that the distribution of
development times does not differ among the temperature
levels was tested against the alternative that as the
376 M.N. Bayoh and S.W. Lindsay
temperature increases, the magnitude of the response
increases. Because the alternative hypothesis is ordered, the
Jonckheere-Terpstra is more appropriate than the Kruskal-
Wallis test. The software TableCurve
®
2D version 4.0 for
Windows was used to fit curves to the data for overall
development rate and temperature and for rates of the instar
stages and temperature. SigmaPlot 2001 software was used
to produce three-dimensional surfaces describing adult
emergence times and the number of adults emerging at the
different temperatures.
Mapping
An environmental database for Africa, the spatial charac-
terization tool (SCT) (Corbett & O‘Brien, 1997), operating
within a geographical information system (GIS, arc/info
Version 7.2; ESRI, Redlands, California), was used to
generate mosquito suitability maps for Africa using data
produced from this study.
Results
There were no significant differences, at the 5% level, in
adult emergence times and number of adults of A. gambiae
produced at the different replicates within each temperature
regime, thus all five replicates were combined for further
analysis. Mean emergence times as well as proportions
developing into adults differed between temperature
regimes (Jonckheere-Terpstra Test Statistic = 22104.5 and Chi
square test statistic = 94.4 respectively, P < 0.001 in both
cases). The mean duration from egg to adult and the
percentage of adults produced at the various constant
temperatures are shown in table 1. Less than 50% of pupae
developed into adults at 30 and 32°C, with most deaths
(> 80%) occurring at pupation. The proportion of larvae
becoming adults was similar between 20 and 28°C (χ
2
= 2.81,
ns).
Overall, the rate of development increased at higher
temperatures for each immature stage. However, as the life
stages advanced, the lower temperature threshold for
development increased while the upper temperature
Temperature and larval development of A. gambiae 377
0
5
10
15
20
25
10 16 22 28 34
Temperature (°C)
Development time (days)
0
5
10
15
20
25
10 16 22 28 34 40
Temperature (°C)
Development time (days)
Fig. 1. Development times of the aquatic stages of Anopheles
gambiae s.s. at different temperatures.
●
, Egg; –, first instar;
,
second instar;
, third instar; , fourth instar;
●
, pupa.
Fig. 2. Development times of the aquatic stages of Anopheles
gambiae s.s. at different temperatures based on the equation D =
a+b/(1+(t/c)
d
).
●
, Egg; –, first instar;
, second instar;
, third
instar; , fourth instar;
●
, pupa.
Table 1. Development time of Anopheles gambiae s.s. and proportion of adults
produced at different constant temperatures.
Temperature
Time to adult (days) No. adults produced
(°C) Mean (± 95% CI) H P % χ
2
P
16 None – – None – –
18 23.3 (22.2–23.5) 1.427 0.839 42.0 1.841 0.765
20 20.4 (19.5–20.2) 7.139 0.129 70.0 8.476 0.076
22 17.5 (16.7–17.6) 4.571 0.334 76.0 1.175 0.882
24 13.5 (13.6–14.3) 3.592 0.464 78.7 2.424 0.658
26 11.5 (11.2–11.9) 5.817 0.213 72.7 0.128 0.998
28 9.8 (9.4–10.0) 4.858 0.302 66.0 7.010 0.135
30 10.0 (9.8–10.5) 5.918 0.205 27.3 1.073 0.899
32 10.2 (10.0–10.4) 2.274 0.685 34.7 4.538 0.338
34 None – – None – –
Overall – 22104.5 <0.001 94.418 <0.001
H = Kruskal-Wallis Test Statistics, n = 5 for each temperature; for overall time to adult
data Jonckheere-Terpstra Test Statistic reported n = 8 for all temperatures; CI =
confidence interval.
threshold decreased (fig. 1). Adults emerged only between
16 and 34°C. There was no development of first instar larvae
at 10, 12 and 40
o
C. Larval development at 14 and 38°C
ceased at the second instar stage with immediate death at
38°C but prolonged life at 14°C. Similarly, development at 16
and 34° ceased at the fourth stage with prolonged duration
of life at 16°C.
Smooth curves were fitted along data points for
development times of each stage across the temperatures
(fig. 2) and all fitted the expression
D = a + b/(1 + (t/c)
d
)
where D = development time, t = temperature, and a, b, c
and d are coefficients for the fit which differ for each
immature stage and are presented in table 2.
Optimal temperatures for adult development ranged
from 28 to 32°C and for adult production from 22 to 26°C.
The peaks for development and adult production relative to
temperature were out of phase (fig. 3).
The relationship between overall development rate (R)
and temperature (t) is best described by the non-linear
expression
R = a + bt + ce
t
+ de-
t
where a = 0.050, b = 0.005, c = 2.139E-16, d = 281357.656
(goodness of fit, r
2
= 0.99 and F = 243.2).
A linear degree-day model was obtained by substituting
for temperature in the equation suggested by Craig and
others (Craig et al., 1999) and overlaid with predicted rates
from this study (fig. 4). There was a close resemblance
between the two models over the projected linear area
depicted by our model, except at temperature extremes.
The relationship between temperature, adult emergence
times and number of larvae surviving to adults was displayed
on a 3D surface (fig. 5). The period of adult emergence was
narrow for all temperatures while the number of adults
emerging peaked at the moderate temperatures.
378 M.N. Bayoh and S.W. Lindsay
Stages a b c d r
2
Fit SE F-value
Egg 48.549 970.200 12.096 4.839 0.98 16.623 135.876
First instar 131.322 988.156 14.134 5.425 0.97 28.816 114.707
Second instar 210.666 7430.194 9.402 4.658 0.97 35.324 82.633
Third instar 317.494 56199.178 7.038 5.174 0.98 43.781 96.438
Fourth instar 390.236 662.094 20.742 8.946 0.99 17.054 278.261
Pupa 410.863 991.391 19.759 6.827 0.99 22.046 234.515
Table 2. Coefficients of the curve fit D = a + b/(1 + (t/c)
d
), which describes the
relationship between temperature and the stage specific development times of
Anopheles gambiae s.s. immature stages.
0
0.02
0.04
0.06
0.08
0.10
0.12
16 20 24 28 32
Temperature (°C)
Development rate (days
–1
)
0
20
40
60
80
100
Adults (%)
0
0.04
0.08
0.12
0.16
0.20
12 18 24 30 36 42
Temperature °C
Development rate (days
–1
)
Temperature (°C)
Time (days)
No. adults
40
30
20
10
0
5
10
15
20
25
30
18
20
22
24
26
28
30
Fig. 3. Development rate of Anopheles gambiae s.s. ( ) and
percentage developing to adults (
●
) at different tempera-
tures.
Fig. 4. Comparison of a linear degree-day model (
) of
relationship between temperature and development rate of
Anopheles gambiae mosquitoes (Craig et al., 1999) with the non-
linear model produced from this study (
●
).
Fig. 5. A three-dimensional view of the influence of temperature
on adult Anopheles gambiae s.s. emergence times and numbers
produced.
The climate suitability map for A. gambiae s.s. was based
on areas in Africa where the mean temperature ranged from
a minimum of 15°C to a maximum of 35°C and rainfall was
higher than 350 mm during the wettest five months of the
year. Since the sensitivity of the growth chambers was ±1°C,
the temperature range for larval development was adjusted
to include this factor. Thus 15°C was used as the lower limit
and 35°C for the upper limit, rather than the 16 and 34°C
thresholds determined directly from the present
experiments. The rainfall criteria employed were based on
suggestions for stable malaria made by Craig and others,
that 80 mm rain for five months was sufficient but 60 mm
rain for five months was not (Craig et al., 1999). It was
assumed that the amount of rainfall needed for malaria fell
between these two values and took the average value of
350 mm was taken for the five wettest months of the year.
The map generated by the temperature requirements for A.
gambiae s.s. larval development where rainfall is not limiting,
approximately highlighted the areas known for stable
malaria and was very similar to the MARA/ARMA malaria
distribution map (fig. 6).
Discussion
The development of the aquatic stages of A. gambiae s.s.
increases with temperature between a lower and upper
threshold. The overall relationship between development
rate and temperature is non-linear and is made up of three
parts. Firstly, there is a non-linear increase in development
rate from zero development at a low temperature threshold,
in this case 16°C. Secondly, there is a temperature where the
rate begins to increase proportionally with temperature,
between 22 and 28°C. Finally, after the optimum
temperature is approached there is a rapid non-linear
decline to no development at an upper lethal temperature, in
this instance, 34°C. This trend has also been reported for
other insects (Logan et al., 1976; Briere & Pracros, 1998;
Petavy et al., 2001). The difference between the widely used
linear model of development versus time and the
polynomials used in this study was apparent when the
curves were superimposed. There is no upper bound for
development in the linear model but in the non-linear
polynomials upper and lower limits were imposed,
reflecting better the relationship between temperature and
development in which such continuous extreme
temperatures would not naturally support life.
Despite the fact that the duration of larval development
reduced with increased temperature, care must be taken
when incorporating these relationships in malaria
transmission models. As shown by this work, the
proportion of larvae that develop into adults reduced at
higher temperatures. Holometabolous insects, such as
mosquitoes, must attain a certain critical mass during larval
development before they can pupate (Clements, 1992). The
potential attainable mass decreases with increasing
temperature (Chambers & Klowden, 1990) and at higher
temperatures, when development occurs quickly, many
individuals may not accumulate sufficient mass for
eclosion. At these high temperatures, most fourth instar
larvae died during pupation or pupae failed to emerge into
adults. The physiological explanation for why few adults
emerged is unclear. One possibility could be that when
developing at a rapid rate, the organism may be unable to
keep up with the accompanying nutrient intake,
metabolism or accumulation (Korochkina et al., 1997)
required for the complex physiological process in the
change from fourth instar to pupa (Lassiter et al., 1995), and
as a result fails to develop. In field situations, such
physiological activities may well occur when temperatures
drop later in the day and the adults emerge in the early
evening (Shute, 1956). Inhibition of further development
also occurred at low temperatures, probably because of the
low metabolic rate experienced and the inability of the
aquatic stages to accumulate the required mass for
moulting. When Jalil (1971) placed the four different larval
stages of Aedes triseriatus Say at 6–8°C, he observed that
although they were all active, moulting did not take place.
However, they did moult and complete their development
when returned to 25°C. This indicates that cold
temperatures act as an inhibitor by which larvae are held
back at a moulting barrier. However, larvae exposed to 38°C
did not complete development when they were transferred
Temperature and larval development of A. gambiae 379
Fig. 6. Distribution map for malaria in Africa generated by (a) the temperature restrictions shown by this
study and (b) the MARA/ARMA Project.
to 25°C, implying a possible cumulative injurious effect at
the high temperature which prevents further development.
A cautionary note should also be made to emphasize that
the data reported here refers to just one strain of A. gambiae,
and we cannot exclude the possibility that the impact of
temperature on development may vary between
populations. Such intraspecific variation has been recorded
for some insect species (e.g. Trimble & Lund, 1983; Stacey &
Fellowes, 2002), but not all (Tauber et al., 1987; Mogi, 1992;
Royer et al., 2001).
The present work suggests that development rate-
temperature models alone are not sufficient for estimating
adult production. For instance, though development rates at
30 and 32°C were high, the actual numbers of adults
produced at these temperatures were very low compared to
lower temperatures. Thus, the adult production rate should
be expressed in terms of not only time to adult but also
numbers surviving to adulthood.
The map generated using the temperature ranges for
larval development, and assuming rainfall is not limiting,
compared favourably with maps published using more
sophisticated techniques. This zone map of suitable larval
breeding sites was remarkably similar to the areas in the
MARA/ARMA map depicting stable malaria. The southern
limits coincided with areas of greater than 50% stability
including north-eastern Namibia, northern and eastern
Zimbabwe, Lesotho and northern South Africa including the
east coast. Also, in the distribution maps produced by
Lindsay and others (Lindsay et al., 1998), all regions with a
probability of A. gambiae s.s. greater than 10% fell within the
areas depicted by the larval map. This is evidence that
climate is a first order determinant of the distribution and
abundance of species.
The development of processed-based models for
predicting the future spread or retreat of mosquito vectors
requires not only an understanding of the temperature
dependence of the development and survival of the aquatic
stages, but also an appreciation of how climate affects adult
mosquito survival and reproduction. Such mathematical
models could be developed for measuring future changes in
the distribution of this vector in Africa and identify areas of
the world that could support this vector if it were
accidentally introduced.
Acknowledgements
M.N. Bayoh was supported for this work by a
Commonwealth Scholarship. The authors thank Professor
Ken Bowler and two anonymous referees for their helpful
suggestions and we are also grateful to Ms Barbara Sawyers
and Professor Chris Curtis for providing us with the 16C
strain of Anopheles gambiae sensu stricto.
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(Accepted 12 June 2003)
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Temperature and larval development of A. gambiae 381
Readership
Zoology, parasitology, animal behaviour and ecology.
Description
Parasites have evolved numerous complex and fascinating ways of interacting with their hosts. The
subject attracts the interest of numerous biologists from the perspective of ecology and behavioural
biology, as well as from those concerned with more applied aspects of parasitology. However, until
now there has been no recent book to synthesize this field.
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The Behavioural
Ecology of Parasites
Edited by E E Lewis, Virginia Polytechnic Institute and
State University, J F Campbell, US Department of
Agriculture, Kansas, and M V K Sukhdeo, Rutgers
University, New Jersey, USA
ISBN 0 85199 615 9
August 2002 384 pages
Hardback £65.00 (US$120.00)
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