June, 2004
Journal of Vector Ecology
11
Food as a limiting factor for Aedes aegypti in water-storage containers
Jazzmin Arrivillaga1 and Roberto Barrera2
Universidad de Carabobo, Laboratorio de Entomología Medica, BIOMED, Las Delicias,
Maracay, Aragua, Venezuela
2
Laboratorio de Biología de Vectores, Instituto de Zoología Tropical, Facultad de Ciencias,
Universidad Central de Venezuela, Apdo. 47058, Caracas 1041-A, Venezuela
2
Corresponding author
1
Received 24 March 2003; Accepted 5 May 2003
ABSTRACT: An understanding of the ecological factors that regulate natural populations of Aedes aegypti mosquitoes
can improve control and reduce the incidence of dengue (DF) and dengue hemorrhagic fever (DHF) in tropical
areas. We investigated whether immature Ae. aegypti in water-storage containers from an urban area were under
food limitation. We used starvation resistance (number of days alive without food) as an indicator of the feeding
history in third-instar Ae. aegypti larvae. Resistance to starvation and other measures of immature success, such as
development time, survival, and adult mass, were investigated across a wide range of feeding conditions in the
laboratory. Resistance to starvation of third-instar larvae and body mass of adults emerging from pupae collected in
water-storage containers in an urban area were compared with the laboratory results. If resistance to starvation and
adult mass of field-collected Ae. aegypti corresponded with the lower levels of feeding in the laboratory, then food
limitation could be inferred in field-collected larvae. Results showed that resistance to starvation was well correlated
with previous feeding levels and with the other measures of immature success. Both resistance to starvation and
adult body mass of field-collected specimens corresponded with the lower levels of feeding in the laboratory.
Therefore, it was concluded that food limitation or competition is likely to be a regulatory factor in water-storage
containers in the urban area. It is recommended that any control measure applied to immature Ae. aegypti in waterstorage containers should eliminate all or most of the individuals, otherwise unintended, undesirable results might
occur, such as the production of more and larger adults. Journal of Vector Ecology 29 (1): 11-20. 2004.
Keyword Index: Aedes aegypti, ecology, dengue, mosquito control, competition.
INTRODUCTION
It is important to understand the ecological factors
that regulate pre-adult populations of Aedes aegypti in
the numerous containers present in urban areas, where
dengue fever and dengue hemorrhagic fever are
increasingly important public health problems (Gubler
1997, Gubler and Clark 1995, Pinheiro and Chuit 1998).
Such an understanding allows selection of appropriate
control methods. For example, Gilpin and McClelland
(1979), in their system analysis of Ae. aegypti,
recommended source reduction and the introduction of
interspecific competitors for larval food, since “densityindependent mortality on adults or eggs could be worse
than useless.” If food limitation and/or intraspecific
competition were the main factors of immature mortality
in Ae. aegypti, any imposed reduction of less than 100
percent within a breeding place would produce larger
adults, with a greater vectorial capacity. Agudelo-Silva
and Spielman (1984) provided a laboratory
demonstration of such effects in Ae. aegypti. Source
reduction, however, is difficult to accomplish with waterstorage containers because they usually result from
inadequate or non-existent water supply services (Barrera
et al. 1993, Barrera et al. 1995). Also, control techniques
used in these habitats are limited by the need to preserve
the quality of the drinking water.
A variable that has proven useful to indirectly
explore the importance of ecological factors in the
aquatic habitats of mosquitoes is the capacity of larvae
to withstand starvation. Such a trait significantly varies
with different species and their aquatic habitats. In
Current address: Centers for Disease Control and Prevention (CDC), Dengue Branch, 1324 Calle Cañada, San
Juan, Puerto Rico 00920-3860
2
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Journal of Vector Ecology
general, container-inhabiting mosquitoes have a
significantly greater capacity to withstand starvation than
mosquitoes in ground-water habitats, perhaps as a result
of the prevailing selective factors within each group of
aquatic habitats (Barrera and Medialdea 1996). The
ability to prolong development could be an adaptive
response of immature mosquitoes in container habitats
where food limitation due to pulsed food input (e.g., leaf
litter) and/or crowding may be common (Frank and Curtis
1977). Such ability lacks adaptive significance in aquatic
habitats where desiccation (e.g., in ground pools) or
predation (e.g., in lagoons) are the main regulatory
factors.
Resistance to starvation, as measured by the length
of time a third-instar larva survives without food reflects
the energy-reserve accumulation, mainly lipids, that the
larva had been able to store (Wigglesworth 1942).
Present work showed that resistance to starvation was
correlated with food and with other measures of immature
success, such as adult body mass, immature survival,
and development time. Also, we used resistance to
starvation to indirectly determine whether immature Ae.
aegypti in water-storage containers were under food
limitation. Here, we investigated metal drums because
they are commonly used to store water in tropical urban
areas (Barrera et al. 1993, Barrera et al. 1995).
June, 2004
used as the larval food, and it was added daily depending
on the number of larvae alive, so that the amount of food
offered per larva per day was kept constant throughout
the immature development. This procedure was
replicated four times. Immatures were observed daily to
record their numbers and instars. Emerged adults were
counted, separated by sex, and weighed 6-24 h after
emergence using an electronic micro-balance (Cahn C3; sensitivity 1 ¼ g).
In the second experiment, 40 first-instar larvae were
reared in 200 ml plastic containers until the third-instar
under each of 12 feeding conditions, representing 4 low,
4 medium, and 4 high feeding conditions (0.01, 0.05,
0.075, 0.1, 0.3, 0.4, 0.6, 0.7, 0.9, 1.0, 1.4, 1.6 mg/larva/
d). This procedure was also replicated four times. Each
third-instar larva was transferred to a 5 ml vial with
aerated tap water to observe the length of time the larva
survived without food. Each larva was transferred to a
fresh vial every 48 h to avoid accumulation of bacteria
and waste.
Aedes aegypti larvae used in these experiments
originated from an F1 colony initiated with larvae and
pupae collected from metal drums in Piritu (10º 05’N;
65º 05’W), a town in the eastern state of Anzoategui,
Venezuela, where we were conducting a baseline study
on the ecology of the vector (Barrera et al. 1993). The
colony was kept at 27 ± 1ºC, 80-90% RH, and 12 h
photoperiod in the laboratory.
Data analyses
One-way ANOVA was used to test the null
hypothesis that mean mortality, development time,
survival, or resistance to starvation did not change with
feeding level (á = 0.05). Correlation coefficients
(Pearson; two-sided:á =0.05) were used to explore the
relationships between variables of development and
resistance to starvation. Regression analyses were
employed to describe the relationship between dependent
variables and feeding levels. To normalize the data,
variables expressed as counts were transformed using
the square root function, percentages were transformed
using the arcsine function, and continuous variables were
transformed using the log10 function before performing
statistical analysis. Where shown in figures, means were
accompanied with 95% confidence intervals.
Responses to liver powder in the laboratory
To understand the relationships between resistance
to starvation and other responses of larval development,
two experiments were performed. In the first one, we
reared first-instar Ae. aegypti under a wide range of
feeding conditions and observed their immature
development time, survival, and mass of emerging adults.
In the second experiment, we reared first-instar larvae
under similar conditions until they reached the third
instar, then starved them to determine their survival time.
In the first experiment, 40 first-instar larvae were added
to plastic containers with 200 ml of aerated tap-water,
and one of 17 feeding levels (0.01, 0.025, 0.05, 0.075,
0.1, 0.2, 0.3, 0.4, 0.5, 0.6, 0.7, 0.8, 0.9, 1.0, 1.2, 1.4, 1.6
mg/larva/d) until adult emergence. Liver powder was
Responses of Ae. aegypti in metal drums in the
laboratory
We evaluated the responses of immature Ae. aegypti
reared at low density with natural food in metal drums
in the laboratory. If the quality of food in metal drums
was comparable with that of liver powder, similar
responses to those of high feeding levels with liver
powder should be observed. We also investigated
whether the volume of water in metal drums affected the
immature responses at low larval density. Each metal
drum was seeded with 40 first-instar larvae from the
colony, with one of three levels of water (low = 51 l;
medium 101 l; high 203 l), and a two l mixture of natural
food. This procedure was replicated three times. The
mixture of natural food was prepared from 180 g of
MATERIALS AND METHODS
June, 2004
Journal of Vector Ecology
13
Table 1. Results of One-way Analyses of Variance (ANOVA) of response variables to varying feeding levels of
Aedes aegypti from Puerto Piritu, Venezuela.
Variable
Degrees of freedom
Error
Mean squares
Effect
Error
F
P-level
Effect
Development time
(square root)
50
16
0.005
0.689
129.69
< 0.001
Immature survival
(arcsine)
50
16
0.045
0.228
5.04
< 0.001
Female mass
(log10)
50
16
0.0007
0.033
43.33
< 0.001
Male mass
(log10)
50
16
0.0008
0.012
14.10
< 0.001
Resistance to starvation
(square root)
33
11
0.047
3.657
77.71
< 0.001
22
Development time (days)
20
18
16
14
12
10
8
6
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Food level (mg/larva/day)
Figure 1. Development time (first-instar to adult emergence) of Aedes aegypti reared under 17 levels of feeding
(mg of food/larva/d) in the laboratory.
14
Journal of Vector Ecology
June, 2004
Immature survival (%)
100
80
60
40
20
1
2
3
4
5
6
7
8
9 10 11 12 13 14 15 16 17
Feeding level
100
90
Pupal mortality (%)
80
70
60
50
40
30
20
10
0
1
2
3
4
5
6
7
8
9 10 11 12 13 14 15 16 17
Feeding level
Figure 2. Mean immature survival and pupal mortality of Aedes aegypti reared under 17 levels of feeding (mg of
food/larva/d) in the laboratory.
June, 2004
Journal of Vector Ecology
15
Table 2. Correlations between mean resistance to starvation (square-root transformed) in third-instar larvae of
Aedes aegypti (maximum number of days alive without food), feeding level, and variables of
immature success. Each correlation was significant at á < 0.05 (N = 44).
Variable
Feeding level (mg/larva/day)
Development time (square root)
Pupal mortality (arcsine)
Immature survival (arcsine)
Female adult mass (log10)
Male adult mass (log10)
organic material collected from the bottom and inner
walls of nine metal drums in the field, then passed through
a sieve (to exclude Ae. aegypti eggs) and suspended in
18 l of aerated tap water. Metal drums used in the
experiments were covered with an inner layer of cement
and allowed to hold water for several weeks before
performing the experiments. This simulates the way metal
drums are used in urban areas. Metal drums with different
levels of water and two l of food were prepared and set
for one week prior to seeding them with 40 first-instar
larvae. When in third instar, 10 larvae were taken from
each drum and transferred to individual vials to observe
resistance to starvation, whereas the rest of the larvae
were allowed to develop to adults. A one-way ANOVA
was used to explore the hypothesis that water level does
not affect immature responses (immature survival,
development time, adult body mass, resistance to
starvation). The regression equations calculated before
were used to extrapolate to equivalent responses with
liver powder.
Immature Ae. aegypti collected from metal drums in
the field
We observed resistance to starvation in third-instar
larvae and body mass of emerged adults from pupae
collected in metal drums in the urban area. Third-instar
larvae were collected in the field on three occasions
(March, May, August 1992), whereas pupae were
collected on six field trips to the study area (November
1991, January, March, May, August, October 1992) to
detect any temporal changes in immature responses. A
one-way ANOVA was used to compare resistance to
starvation or adult body mass across sampling events.
The regression equations calculated before were used to
extrapolate to equivalent responses with liver powder.
Pearson’s correlation coefficient (r)
0.94
- 0.93
- 0.69
0.38
0.94
0.87
RESULTS
Responses to liver powder in the laboratory
Development time (days from first-instar to adult)
Immature development significantly varied (Table
1) with the amount of food, from 8.5 d at the highest
feeding level to 18.5 d at the lowest feeding conditions.
Development time decreased with food levels as
described by the following equation (R2 = 0.93; N = 67):
Development time = 10.28 – 4.48 x [log10 (food level)]
(Figure 1).
Survival to immature development
Mean immature survival significantly changed
among treatments (Table 1). Survival was low (27 - 40%)
at feeding levels below 0.1 mg of food per larva/d (Figure
2), increased (63 - 75%) at feeding levels between 0.1
and 0.8 mg, reached the highest values (86 - 88%)
between 0.9 and 1.0 mg, and decreased (50 - 68%) at
greater than 1.0 mg feeding levels. Pupal mortality
decreased with increased food, and it was lowest (0 –
2.5%) at feeding levels above 0.5 mg of food (Figure 2).
Pupal mortality was higher at feeding conditions below
0.1 mg, following the same tendency observed for total
survival under those conditions.
Adult body mass
The mean mass of emerging females and males
significantly changed with feeding levels (Table 1). Adult
mass gradually increased with the amount of food
supplied (Figure 3). Mean female mass varied between
0.554 mg at 0.01 mg of food/larva/d and 2.338 mg at
1.6 mg of food (range 0.109 - 2.950 mg), whereas male
mass changed between 0.387 and 1.203 mg (range 0.106
- 1.990 mg), respectively. A linear regression between
female mass and food levels was significant (R2 = 0.86;
N = 67; F = 407; P < 0.01), resulting in the following
equation: Female mass = 0.739 + 0.925 x food level.
16
Journal of Vector Ecology
June, 2004
Female adult mass (mg)
3.0
2.4
1.8
1.2
0.6
0.0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8
1.4
1.6
1.8
Food level (mg/larva/day)
Male adult mass (mg)
3.0
2.4
1.8
1.2
0.6
0.0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
Food level (mg/larva/day)
Figure 3. Mean adult mass (mg) of Aedes aegypti females and males reared under 17 levels of feeding (mg of
food/larva/d) in the laboratory.
Resistance to starvation (days)
June, 2004
Journal of Vector Ecology
17
50
40
30
20
10
0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8
Food (mg/larva/day)
Figure 4. Mean resistance to starvation (days alive without food) in third-instar larvae of Aedes aegypti reared
under 12 levels of feeding (mg of food/larva/d) in the laboratory.
The regression analysis between male body mass and
food level was also significant (R2 = 0.73; N = 67; F=
175; P < 0.01), resulting in the equation: Male mass =
0.510 + 0.416 x food level. The ratio male : female
emergence in the experiments was 1.02 : 1.
Resistance to starvation
The mean maximum number of days that third-instar
larvae survived without food significantly changed with
feeding conditions (Table 1). Mean resistance to
starvation (RS) gradually increased with feeding level
(Figure 4), from 12 to 46.75 d (range 2 - 47 d). Mean RS
could be fitted to a power equation (R2 = 0.88; N = 45):
Resistance to starvation = 37.06 x (food)0.279.
Relationships between variables
Mean resistance to starvation was positively and
significantly correlated with feeding level, immature
survival, and adult mass, and negatively correlated with
pupal mortality and development time (Table 2). The
highest correlations were observed with feeding level,
development time, and female body mass.
Responses of Ae. aegypti in metal drums in the
laboratory
Development time
Immature development time did not change with the
level of water in metal drums (ANOVA df = 2, 6; F =
0.5; P >0.05), varying from 11.6 to 12.6 d. The
development time corresponded to 0.3-0.5 mg of liver
powder/larva/d.
Immature survival
Survival of larvae did not significantly change with
water level (ANOVA df = 2, 6; F = 0.4; P > 0.05), varying
between 94 and 97%.
Adult body mass
Mean adult body mass of females emerging from
metal drums in the laboratory did not significantly change
with water volume (ANOVA df = 2, 72; F = 0.4; P >
0.05). Mean female mass varied between 1.998 and 2.152
mg. These values of female adult mass corresponded to
those attained with 1.4 - 1.5 mg of liver powder/larva/d.
Mean adult body mass of males did not change with water
level (ANOVA df = 2, 79; F = 1.64; P > 0.05), and varied
from 1.023 to 1.108 mg. These values corresponded with
1.2 - 1.4 mg of liver powder/larva/d.
Resistance to starvation
This variable did not change with the water level in
metal drums in the laboratory (ANOVA df = 2, 86; F =
0.2; P > 0.05). Mean resistance to starvation was around
20 d under all conditions studied. This value
18
Journal of Vector Ecology
corresponded to 0.11 mg of liver powder/larva/d.
Responses of Ae. aegypti in metal drums from the field
Adult body mass
Mean mass of female adults that emerged from
pupae collected in the field significantly varied among
months (ANOVA df = 5, 113; F = 6.3; P < 0.01). Mean
values changed from 0.74 in January 1992 to 0.94 in
March 1992. Those values corresponded to 30 - 40% of
the maximum mean body mass of females reared under
the highest liver-powder regime (1.6 mg). Mean mass of
adult females collected in the field was similar to those
obtained from low feeding conditions using liver powder
(Figure 3). Using the regression equation calculated
before, the mean mass of females from the field
corresponded with feeding levels of 0.001 - 0.2 mg of
liver powder/larvae/d.
Mean mass of male adults from the field significantly
varied among months (ANOVA df = 5, 114; F = 5.1; P <
0.01). Mean values changed from 0.47 in May 1992 to
0.67 in October 1992 (range 0.22 - 1.00 mg). Those
values corresponded to 40 - 56% of the maximum mean
body mass of males reared under the highest feeding
levels with liver powder. Mean mass of adult males
collected in the field was similar to those obtained from
low to intermediate feeding conditions using liver powder
(Figure 3). Using the regression equation calculated
before, the mass of males from the field corresponded
with feeding levels comparable to - 0.09 and 0.38 mg of
liver powder/larvae/d. More females than males were
collected from metal drums in the field, with a male :
female ratio of 0.86 : 1.
Resistance to starvation
Third-instar larvae collected in metal drums showed
significant differences in mean RS among sampled
months (ANOVA df = 2, 901; F = 85.3; P < 0.01). Mean
RS values were similar in March and May (14.3-14.7
d), and lower in October (10.9 d; range 2-47 d).
Comparatively, values observed in field-collected larvae
were 23 - 31% of the mean maximum RS values under
the highest feeding conditions in the laboratory. Also,
field values corresponded with the lower levels of feeding
in the laboratory experiments with liver powder (Figure
4). Using the regression equation described before, the
equivalent feeding levels with liver powder of wild larvae
were from 0.01 to 0.04 mg.
DISCUSSION
The results showed a wide phenotypic variation in
immature development, adult mass, and resistance to
starvation of Ae. aegypti reared with liver powder in the
June, 2004
laboratory. The range of food used in the laboratory
experiments covered a wide range of possible feeding
conditions in the field. The lower larval survival observed
in the experiments at the highest feeding levels (Figure
2) can usually be observed when Ae. aegypti is reared
with excess food in the laboratory (unpublished data).
Adults emerging under these conditions had the largest
body mass (Figure 3), and third-instar larvae showed
the greatest resistance to starvation (Figure 4). On the
other hand, the lowest larval and pupal survival were
observed at feeding levels under 0.1 mg of liver powder,
probably as a result of insufficient energy to complete
development, and this is well illustrated by the smallest
adult body mass and the lowest resistance to starvation
observed in third-instar larvae.
The results also showed that resistance to starvation
in third-instar larvae of Ae. aegypti is a variable affected
by food availability, much in the same way that
development time, survival, and adult mass have
traditionally been shown to respond to such a factor. We
used third-instar larvae of Ae. aegypti instead of fourthinstar larvae because the latter tend to pupate in the
absence of food; a process that is possible only if enough
energy has been accumulated in prior larval stages. The
number of days larvae can survive without food is a
function of accumulated reserves, mainly lipids
(Wigglesworth 1942, Gilpin and McClelland 1979),
which are probably the result of the history of food
availability. Present results indicated that resistance to
starvation was negatively correlated with pupal mortality
(Table 2), particularly at the lowest feeding levels. Thus,
under conditions of food limitation, resistance to
starvation can partially be used as a predictor of immature
success, as early as in the third-instar of Ae. aegypti reared
under laboratory conditions.
Adult body mass and resistance to starvation of Ae.
aegypti collected from metal drums in the field
corresponded with the lowest levels of feeding with liver
powder in the laboratory. Those responses did vary
among months, but they were equivalent to low feeding
levels in the laboratory. One explanation for such a
finding is that immature Ae. aegypti in metal drums in
the study area were under food limitation or competing
for food. Our observations in metal drums in the study
area showed that only half of the metal drums in the study
area were producing pupae. Also, the presence of aquatic
predators (e.g., Odonata larvae, Toxorhynchites sp.) and
desiccation were rare events in metal drums in this study
area (unpublished data). Previous work with urban
immature Ae. aegypti populations pointed out the
importance of intra-specific competition and/or food
limitation, particularly in water-storage containers
(Southwood et al. 1972, Subra and Mouchet 1984).
June, 2004
Journal of Vector Ecology
An alternative explanation is that liver powder may
be a better food than that found in metal drums; although
several authors have indicated that natural food for
immature mosquitoes (e.g., bacteria, algae, protozoa,
fungi, etc.) has high protein content (Clements 1963,
Bursell 1970). The mass of adults reared in metal drums
with natural food and low density in the laboratory
corresponded to the equivalent of high feeding levels
with liver powder. However, development time was
longer and resistance to starvation was lower than that
observed at high feeding levels with liver powder. This
result may indicate that Ae. aegypti larvae in metal drums,
even at low density, could not store or derive as many
reserves to resist starvation as those observed when
reared with liver powder. It is conceivable that the small
volume of water used in the experiments with liver
powder (200 ml) could have contributed to a larger
storage of reserves because not much energy had to be
expended to obtain food, particularly in third-instar
larvae, as compared with the large volume of metal
drums. On the other hand, we did not observe significant
differences in immature responses of Ae. aegypti reared
at low density and three water volumes in metal drums
that would reveal an effect of volume on energy storage
or body size. These results differed from a previous study
(Timmermann and Briegel 1993) where the authors
reported significant effects of water volume and/or
container depth on parameters of immature Ae. aegypti
from a laboratory colony.
It may still be possible that the type of food or the
process of gathering food in natural or artificial
containers influences how Ae. aegypti larvae allocate
energy for growth, storage, and maintenance. It has been
observed that in the prolonged absence of food,
mosquitoes (Barrera 1996) and other insects (Richards
1969, Stockhoff 1991) rapidly reduce their respiration
rate, therefore resistance to starvation should be directly
related to accumulated energy. Our experiments showed
that resistance to starvation allowed third-instar larvae
reared with liver powder to survive for a long as 47 d,
whereas with natural food some larvae could only survive
for up to 24 d. Given that the maximum body mass of
adults attained under both types of food was comparable,
it was evident that less energy could be allocated for
reserves by third-instars. It would have to be determined
whether a further, improved reserve accumulation takes
place during the fourth instar, when the larvae have a
better capacity to move around and gather food.
In conclusion, resistance to starvation in later instars
is a variable that depends on the previous feeding history
of Ae. aegypti larvae and is well correlated with other
measures of immature success, but is one that can be
observed as early as the third larval instar. Given the
19
difficulty in assessing the quantity of food available in
the aquatic habitats of mosquitoes, we wonder whether
resistance to starvation or more properly, the content of
lipids in third-instar larvae, could serve as an indicator
for potential mosquito adult productivity in aquatic
habitats. For mosquito control, any incomplete reduction
in the density of Ae. aegypti larvae in water-storage
containers would most likely produce more and larger
females, which may be better vectors. We recommend
using control measures that eliminate all or most of the
Aedes aegypti in a given container, otherwise unintended,
undesirable results might occur, such as the production
of more and larger adults (Agudelo-Silva and Spielman
1984). We also recommend that studies assessing the
impact of any control agent on Ae. aegypti and other
container mosquitoes (e.g., Ae. albopictus), particularly
predators and parasites, not just examine numbers killed,
but include estimates of the quality of any surviving
mosquitoes (body mass, longevity, fecundity, etc.).
Acknowledgments
We thank Dr. Juan C. Navarro for his advice and
support, and Giovannina Vele, Jorge Avila, Jonathan
Liria, Javier Ingunza, and Wilmer Mendez for their
collaboration with fieldwork. We appreciate the thorough
revision of the manuscript made by Dr. Gary G. Clark.
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