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Vol. 41, no.

1 Journal of Vector Ecology 1

Effects of temperature on the life cycle, expansion, and dispersion of Aedes aegypti
(Diptera: Culicidae) in three cities in Paraiba, Brazil
Rafael A. Marinho1*, Eduardo B. Beserra1, Maria A. Bezerra-Gusmão¹, Valbia de S. Porto1, Ricardo A. Olinda2,
and Carlos A. C. dos Santos3

Entomology Laboratory, Nucleus for Systematic and Bioecology of Insects, Department of Biology, Universidade Estadual da Paraíba,
¹

Campina Grande, Paraiba, Brazil, rafa_paraibano@hotmail.com


2
Department of Statistics, Universidade Estadual da Paraíba, Campina Grande, Paraiba, Brazil
3
Unity of Atmospheric Sciences, Center of Technology and Natural Resources, Federal University of Campina Grande, Paraíba, Brazil

Received 9 April 2015; Accepted 27 September 2015

ABSTRACT: The mosquito Aedes aegypti is the primary vector of dengue and is common throughout tropical and subtropical regions. Its
distribution is modulated by environmental factors, such as temperature. This study aimed to evaluate the influence of temperature on the
life cycle and expansion of Ae. aegypti populations in the cities of Campina Grande, João Pessoa, and Patos. Samples of Ae. aegypti were
collected in the three cities and raised in the laboratory. We assessed the life cycles of the three Ae. aegypti populations under six constant
temperatures (16, 22, 28, 33, 36, and 39° C), selected on the basis of historical temperature tendencies of each city. We also used existing
climate data to calculate projected temperature increases for all three areas. Our results suggest that Campina Grande, João Pessoa, and
Patos will experience, respectively, maximum temperature increases of 0.030° C/year, 0.069° C/year, and 0.061° C/year, and minimum
temperature increases of 0.019° C/year, -0.047° C/year, and -0.086° C/year. These projected increases will result in temperatures favorable
to the Ae. aegypti life cycle, causing rapid population growth. Therefore, Ae. aegypti populations are likely to expand in the mesoregions
represented by these cities. Journal of Vector Ecology 41 (1): 1-10. 2016.

Keyword Index: Aedes aegypti, vector biological cycle, intra-population variation, development, temperature tendency.

INTRODUCTION that regulate aspects of mosquito ecobiology in natural and urban


ecosystems that favor the transmission of dengue.
The mosquito Aedes aegypti is the primary vector of dengue Based on current understanding of the close relationship
fever and an extremely synanthropic insect due to its anthropophilic between climate and the life cycle of Ae. aegypti, a projected
nature and specific reproductive needs (Lambrechts and Failloux temperature elevation of 2° C by the end of the 21st century will
2012). It is abundant in neotropical regions, where environmental likely broaden the distribution of dengue worldwide (Donalísio
factors (e.g., rainfall, temperature, and relative humidity) favor its and Glasser 2002). Furthermore, each of the last three decades has
life cycle (Eisen et al. 2014). The global distribution of Ae. aegypti been successively warmer than any decade since 1850. In tropical
is strongly influenced by climatic factors, with temperatures of regions of South America where Ae. aegypti are particularly
10° C or lower limiting larval development and adult survival prevalent both maximum and minimum temperatures have risen
(Slosek 1986, Hopp and Foley 2001). Optimal temperatures for in recent decades, corresponding to the worldwide trend.
development, longevity, and fecundity are between 22° C and 32° Based on these previous findings, we hypothesized that the
C (Beserra et al. 2009). With higher temperatures in the favorable rise in temperature will favor vector dispersal and geographical
survival range of Ae. aegypti, egg-laying time decreases, causing an expansion. In this study we aimed to (1) estimate increasing
increase in egg number (Costa et al. 2010). Moreover, the extrinsic temperature trends over the next 18 years (until 2032) for the
incubation period of the dengue virus is reduced, resulting in cities of Campina Grande, João Pessoa, and Patos; (2) evaluate
higher rates of viral transmission (Focks et al. 2000, Hopp and the effects of temperature on the Ae. aegypti life cycle; and (3)
Foley 2001). According to estimates by Bhatt et al. (2013), 390 investigate whether estimates of temperature increase in the three
million dengue virus infections occur annually, including close to cities will favor Ae. aegypti dispersion and expansion.
100 million cases of dengue disease.
Vector-borne diseases, such as dengue, may be particularly MATERIALS AND METHODS
sensitive to both periodic fluctuations and sustained changes
in global and local climates because the vectors themselves Study site
are temperature- and moisture-dependent (Thai and Anders The assessment was conducted for 12 months (January, 2012
2011). As the effect of temperature on Ae. aegypti life cycles are to February, 2013) and samples of Ae. aegypti populations were
substantially established (Bar-Zeev 1958, Keirans and Fay 1968, collected from Campina Grande (Bodocongó neighborhood -
Rueda et al. 1990, Kamimura et al. 2002, Mohammed and Chadee 07°13′14.92″S, 035°55′1.32″W), João Pessoa (Castelo Branco -
2011, Richardson et al. 2011), recent studies (Williams et al. 2014, 07°08′11″S, 034°51′9.33″W), and Patos (Jatobá - 07°02′40′′S,
Campbell et al. 2015) focus on the investigation of the interaction 037°16′16′′W). These cities were selected because they are
between life cycle and global climate changes and future scenarios located in different mesoregions (Agreste, Mata, and Sertão da
2 Journal of Vector Ecology June 2016

Paraíba, respectively) that vary in thermal characteristics (Figure microscope. The study species (Ae. aegypti) was differentiated from
1). Population samples of Ae. aegypti were obtained from eggs the sympatric Ae. albopictus based on morphological characters
collected in oviposition traps that were installed in 50 residences, of the eighth abdominal segment, following the identification
one per block, for each city. key presented by Consoli and Lourenço de Oliveira (1994). We
Based on the Köppen-Geiger climatic classification, the three successfully identified 30% of the larvae in each container.
cities are characterized as follows: (1) Campina Grande has a
moderate tropical climate, with a spring/summer dry season and Calculation of temperature tendencies
an autumn/winter wet season. Maximum summer and winter To set appropriate temperatures in the laboratory, we
temperatures are 30 and 18° C, respectively. Minimum summer calculated temperature tendencies for each study region using
and winter temperatures are 20 and 15° C, respectively. The historical (1975 to 2011) annual temperature data, which were
annual relative humidity is between 75–82%. (2) João Pessoa has obtained from the National Institute of Meteorology. RClimdex
a hot and humid intertropical climate, with an average annual software 1.9.0, based on the R statistical package, was used for index
temperature of 26.1º C. Maximum temperatures (around 30.5° C) calculation. RClimdex calculates all 27 indexes recommended
occur in February and minimum temperatures (around 20.5° C) by Climate Change Initiative/Climate and Ocean: Variability,
occur in August. The annual relative humidity is approximately Predictability, and Change (CCI/CLIVAR) Expert Team for
89%. (3) Patos has a hot semi-arid climate, with the hottest month Climate Change Detection Monitoring and Indexes (ETCCDMI)
being December (average minimum and maximum temperatures (Orlowsky and Seneviratne 2012). The program is able to adjust
of 20.4 and 32.7° C, respectively) and the coldest month being July for errors in the database by replacing all faulty data with -99.9,
(average minimum and maximum temperatures of 17.1 and 28.1° an internal format recognized by R. These errors include negative
C, respectively). The annual relative humidity is between 40% and daily precipitation values and maximum daily temperatures lower
60%. than the minimum daily temperatures.
Upon obtaining annual temperature tendencies, we multiplied
Aedes aegypti maintenance in the laboratory the values by 10 to obtain decadal tendencies. Starting from 2012,
Rearing and bioassays were carried out at the Entomology we projected mean maximum and minimum temperatures for two
Laboratory of the Center of Systematic and Insect Bioecology decades, until 2032. Based on the decadal ones, we were able to
of Paraíba State University. Rearing was conducted in linearly calibrate the temperatures of the three cities. Temperatures
environmentally controlled rooms, with the temperature set to between the estimated minimum temperature (16° C) and the
26 ± 2° C, photoperiod to 12:12 hours light-dark, and relative maximum temperature (39° C) were calibrated at differences of 6,
humidity to 70%, the latter being verified using a thermo- 5, and 3° C, resulting in constant temperature ranges of 16, 22, 28,
hygrometer dry bulb and wet. Rearing procedures followed those 33, 36, and 39° C. These temperatures were used to evaluate the
described by Beserra et al. (2009). cycle life and thermal requirements for Ae. aegypti development.
We attempted to minimize interference between different Although the effects of constant temperatures on Ae. aegypti are
Aedes species in our study area with the following procedure. Eggs well established (Delatte et al. 2009, Richardson et al. 2011), we
from each block were submerged in separate containers filled chose not to alter the selected temperatures to better compare our
with water and allowed to hatch. Upon reaching the 4th instar, results with previous studies.
larvae were fixed on a slide for species identification under the

Figure 1. Map of Paraíba, Brazil, showing the


three cities (João Pessoa, Patos, and Campina
Grande) sampled in this study.
Vol. 41, no. 1 Journal of Vector Ecology 3

Life cycle of Ae. aegypti and developmental thermal 2). We attribute the lack of significance to the short-time series
requirements used in the analysis (only 18 years of data), but we do not consider
For each of the 50 population samples per city, life cycles the amount of data available to have compromised the methods
were assessed through the first generation (F1), considering the six applied in this study.
different temperatures (see previous section), 12-h photoperiod, Based on existing data, maximum temperatures in João
and 70% relative humidity. Evaluation of the incubation period Pessoa tended to increase at approximately 0.069° C/year, while
was performed from the first five ovipositions of each repetition, minimum temperatures tended to decrease at -0.047° C/year.
which were immersed in 500 ml disposable cups filled with Projected maximum and minimum temperatures for 2032 were
distilled water. Water temperatures ranged from 15.0 to 15.7° C, 32.8° C and 18.8° C, respectively. Maximum and minimum
21.0 to 21.7° C, 27.2 to 27.5° C, 32.0 to 32.8° C, 34.9 to 35.5° C, and temperatures in Campina Grande tended to increase at rates
38.1 to 38.7° C for the temperatures conditions of 16, 22, 28, 33, of 0.030° C/year and 0.019° C/year, respectively, resulting in
36, and 39° C, respectively. To assess the length of the larval stage, projected 2032 temperatures of 33.7 °C (maximum) 16.6 °C
20 larvae/cup were used per repetition. Assessments were made (minimum). Patos exhibited an increasing trend of 0.061 °C/year
daily; for each temperature, we recorded the egg development for maximum temperature and a decreasing trend of -0.0869°
periods and mortality, larval and pupal stages, larval emergence, C/year for minimum temperature. Projected 2032 temperatures
and adult longevity and fecundity. in Patos were calculated to be 39.1 °C (maximum) and 16.8°
C (minimum). The minimum (16° C) and maximum (39° C)
Statistical analysis projected temperatures were used as the reference for determining
The experiment was completely randomized in a factorial 3 the six temperatures used in our rearing experiments.
× 6 design (18 treatments). Independent variables consisted of
six temperatures (16, 22, 28, 33, 36, and 39° C), three populations Ae. aegypti aquatic life cycle at six constant temperatures
(Campina Grande, João Pessoa, and Patos), and five replications. We found no significant interaction between population
Group differences and any significant interactions between origin and temperature on egg viability (p > 0.05), showing that
independent variables were examined using ANOVA. Dependent independently of vector collection point and temperature, egg
biological variables were checked for homogeneity of variance viability did not differ between population samples. Observed
using the Box-Cox test (Box and Cox 1964) and the Hartley test viabilities were generally high: the greatest percentage of viable
(Hartley 1950). Subsequently, treatment averages were compared eggs (85.2%) was in João Pessoa, while the greatest percentages
using Tukey’s test. All analyses were performed in SAS/STAT of viable larvae 87.7% and pupae (92.6%) were in Patos (Table 1).
(2003). Significance was set at p < 0.05. Temperature affected every stage of the Ae. aegypti life cycle
Linear regression equations y1 = ai + bit were estimated similarly in all three populations: the length of developmental
between the inverse of development time (1/D response variable, stages was inversely proportional to the temperature increase.
yt in days) and studied temperatures (dependent variable, t in However, the egg stage and the overall life cycle (egg to adult) of the
°C). The base temperature (Tb) was estimated as the relationship populations differed significantly in the intensity of their response
between the intercept and the linear coefficient of the equation to temperature (Tables 2 and 3). No embryonic development or
(Tb = -ai/bi) when development time = 0 (0 = ai + bit). The survival of the larval stages occurred at 39° C (water temperature
thermal constant (K), which is expressed as degrees/day (GD), 37.8 to 38.5° C), and so this temperature was excluded from
was calculated as the inverse of the linear coefficient (K = 1/bi) statistical analysis.
(Santana et al. 2010). There was a significant interaction between population origin
In order to estimate the annual number of generations, we and temperature on the Ae. aegypti embryonic development
used biological data from the temperature setting that resulted in period (Campina Grande p = 0.0490; Patos p = 0.0366), except in
the shortest life cycle. The likely generation number (NG) of insects João Pessoa, which ranged from 10.4 days at 16° C to 2.59 days at
in the field was estimated based on their thermal requirements 36° C. In general, Ae. aegypti from João Pessoa had the shortest
and on the typical temperatures in their area of origin (obtained embryonic development (5.03 days), whereas mosquitoes from
from INMET). Specifically, we used the following equation: NG Patos (5.92 days) and Campina Grande (5.86 days) did not differ
= T(tc-tb)/K, where T is the time considered in a year, tc is the significantly from each other (Table 2). No significant differences
average monthly temperatures of the study areas, K is the thermal were found in the duration of larval and pupal stages among
constant, and tb is the base temperature. population samples at any temperature. However, the length of
the full life cycle (egg to adult) differed significantly among the
RESULTS populations at temperatures between 16° C and 22° C (Campina
Grande p = 0.0100, João Pessoa p = 0.0047, Patos p = 0.0082) ;
Maximum and minimum temperature tendencies specifically, the Campina Grande population required more
Due to missing temperature data in some years, we selected days to develop. In general, Ae. aegypti from João Pessoa had the
only the period from 1994 to 2011 (18 years) for analysis (Figure shortest development period of 18.3 days (Table 3).
2). We found no significant linear increases in the maximum
and minimum temperature tendencies of our study regions (p > Adult longevity and number of eggs per Ae. aegypti female
0.05). However, we noted that only Campina Grande exhibited a Longevity and female fecundity (measured by egg number)
trend of increasing minimum temperature, while the minimum were significantly affected by the interaction between population
temperatures for the other two cities tended to decrease (Figure and temperature. The temperature extremes of 16 and 36° C were
4 Journal of Vector Ecology June 2016

Figure 2. Trends of maximum and minimum temperatures for Campina Grande (a), João Pessoa (b), and Patos (c), based on the INMET
historical data series.
Vol. 41, no. 1 Journal of Vector Ecology 5
Table 1. Average viability (% ± SD) of egg, larval, and pupal stages across five temperatures, in Aedes aegypti (Linnaeus, 1762) populations
from the cities of Campina Grande, João Pessoa, and Patos (Paraíba, Brazil). Insects were reared in a 12:12 h light:dark photoperiod.
Viability (%)
Population
Eggns Larvans Pupans
Campina Grande 81.8 ± 14.57 78.2 ± 1.97 91.2 ± 1.79
João Pessoa 85.2 ± 14.38 80.0 ± 5.74 91.0 ± 2.37
Patos 82.59 ± 6.23 87.7 ± 4.59 92.6 ± 0.71
Overall mean 83.2 81.9 91.6
CV 7.09 11.5 7.79
ns
Not significant (ANOVA; p ≤ 0.05).

Table 2. Embryonic developmental duration (days) of Aedes aegypti from Campina Grande, João Pessoa, and Patos. Insects were reared
in a 12:12 h light:dark photoperiod under five temperatures. Data are presented as means ± SD. Original means are listed; data were log-
transformed for statistical analysis. Means followed by the same lowercase letters in the rows and the same capital letters in the columns
are not significantly different (Tukey’s test; p < 0.05).
Embryonic development (days)
16°C 22°C 28°C 33°C 36°C Overall mean
Campina Grande 13.4 ± 0.47aA 7.68 ± 0.59 bA 3.35 ± 0.62 cA 2.70 ± 0.41 cB 3.66 ± 0.59 cA 5.86 ± 3.95 A

João Pessoa 10.4 ± 0.59 aB 5.16 ± 0.30 bB 3.15 ± 0.40 cA 2.61 ± 0.64 cB 3.48 ± 0.32 cA 5.03 ± 301 B

Patos 11.5 ± 0.66 aB 7.92 ± 0.65 bA 3.32 ± 0.48 cdA 4.23 ± 0.43 cA 2.59 ± 0.36 dA 5.92 ± 3.46 A
CV = 9.32%

Table 3. Duration (days) of larval and pupal stages, as well as full development (egg to adult emergence) in Aedes aegypti populations
from Campina Grande, João Pessoa, and Patos. Insects were reared in a 12:12 h light:dark photoperiod under five temperatures. Means
followed by the same lowercase letters in the rows and the same capital letters in the columns are not significantly different (Tukey’s test;
p <0.05).
Temperature
Population 16° C 22° C 28° C 33° C 36° C Overall Mean
(15.0–15.7°C) 2
(21.0–21.7°C) (27.2–27.5°C) (32.0–32.8°C) (34.9–35.5°C)
Larval stage
Campina Grande 20.51 ± 1.45 aA 13.40 ± 0.54 bA 6.16 ± 0.63 cdA 6.70 ± 0.37 cA 5.17 ± 0.79 dA 10.39 ± 6.0 A
João Pessoa 19.86 ± 0.70 aA 12.49 ± 0.49 bA 7.20 ± 0.46 cA 6.12 ± 0.72 cdA 5.26 ± 0.35 dA 10.19 ± 5.58 A
Patos 20.19 ± 1.01 aA 12.12 ± 0.49 bA 7.25 ± 0.30 cA 7.12 ± 0.38 cA 5.43 ± 0.97 dA 10.42 ± 5.51 A
CV = 6.90%
Pupal stage
Campina Grande 6.97 ± 1.53 aA 3.68 ± 0.70 bA 2.08 ± 0.48 cA 2.51 ± 0.33 bcA 1.29 ± 0.30 dA 3.30 ± 2.16 A
João Pessoa 5.95 ± 0.74 aA
3.25 ± 0.50 bA
2.16 ± 0.69 bcA
2.69 ± 0.27 bA
1.50 ± 0.39 cA
3.11 ± 1.64 A
Patos 7.06 ± 1.61 aA 3.38 ± 0.91 bA 2.51 ± 0.34 bcA 1.88 ± 0.16 cA 1.30 ± 0.18 cA 3.22 ± 2.21 A
CV = 23.31%
Full development (egg to adult)
Campina Grande 41.42 ± 2.56 aA 24.76 ± 1.06 bA 11.59 ± 0.57 cA 11.92 ± 0.43 cA 10.13 ± 1.29 dA 19.96 ± 12.2 A
João Pessoa 36.28 ± 1.63 aB
20.91 ± 0.54 bB
12.52 ± 0.49 cA
11.43 ± 0.64 cdA
10.67 ± 1.40 dA
18.36 ± 9.93 B
Patos 38.82 ± 1.46a AB 23.42 ± 1.46 bAB 13.08 ± 0.60 cA 13.24 ± 0.46 cA 9.33 ± 0.90 dA 19.58 ± 10.9 A
CV = 6.51%
6 Journal of Vector Ecology June 2016

Table 4. Longevity (days) of adults and number of eggs/female in Aedes aegypti populations from Campina Grande, João Pessoa, and
Patos at five temperatures and with a 12:12 h light:dark photoperiod. Means followed by the same lowercase letters in the rows and
the same capital letters in the columns are not significantly different (Tukey’s test; p < 0.05). Original means are listed; data were log-
transformed for statistical analysis.
Temperature
Population
16°C 22°C 28°C 33°C 36°C Overall mean
Longevity of males
Campina Grande 10.89 ± 3.83 bA 29.26 ± 2.03 aAB 21.94 ± 3.32 abB 14.75 ± 5.11 bB 8.32 ± 1.50 bA 17.04 ± 8.40 B
João Pessoa 15.37 ± 2.64 cA
35.55 ± 3.41 aA
32.06 ± 2.26 aA
23.18 ± 3.38 bA
8.72 ± 1.43 cA
22.98 ± 10.5 A
Patos 10.86 ± 1.38 bA 27.59 ± 4.16 aB 31.05 ± 3.92 aA 23.54 ± 1.19 aA 10.53 ± 2.13 bA 20.71 ± 9.1 A
CV = 14.88%
Longevity of females
Campina Grande 12.93 ± 2.44 bcA
25.44 ± 4.13 aB
23.30 ± 2.16 aB 15.05 ± 3.33 bB 7.10 ± 1.45 cA 16.76 ± 7.39 C
João Pessoa 14.76 ± 2.74 cA 34.71 ± 1.88 aA 30.08 ± 3.95 aA 22.16 ± 1.98 bA 10.53 ± 1.68 cA 22.45 ± 9.56 A
Patos 10.22 ± 2.73 bA
26.56 ± 1.56 aB
27.45 ± 2.05 aAB
22.64 ± 2.11 aA
9.49 ± 3.77 cA
19.27 ± 8.38 B
CV = 13.72%
Number of eggs/female
Campina Grande 3.50 ± 1.44 dA
79.22 ± 11.2 aB
64.42 ± 8.65 abB 40.4 ± 11.7 bA 16.12 ± 8.83 cA 40.73 ± 30.1 C
João Pessoa 2.75 ± 1.51 dA 161.5 ± 7.34 bA 262.3 ± 19.7 aA 51.3 ± 10.5 cA 30.57 ± 14.1 cA 101.6 ± 99.8 A
Patos 1.46 ± 0.70 dA
126 ± 23.3 aAB
181.3 ± 43.1 aA
52.92 ± 10.8 bA
22.27 ± 8.73 cA
76.79 ± 71.53 B
CV = 21.50%

Table 5. Results of regression analyses on the development time of Aedes aegypti populations from Campina Grande, João Pessoa, and
Patos. Insects were raised in a 12:12 light:dark photoperiod. Base temperatures (tb), thermal constants (K), intercepts (a), and slopes (b)
are shown.

Tb (°C) K (GD) a ± SEM b ± SEM R²


Population
Egg stage
Campina Grande 9.92 74.6 -0.13286 ± 0.11663 0.01339 ± 0.00417 0.77
João Pessoa 4.32 90.9 -0.04758 ± 0.13102 0.01099 ± 0.00469 0.64
Patos 10.35 73.3 -0.14111±0.10571 0.01363 ± 0.00378 0.81
Larval stage
Campina Grande 9.41 139.8 -0.06734 ± 0.03843 0.00715 ± 0.00137 0.90
João Pessoa 9.45 140.8 -0.06713 ± 0.01274 0.00710 ± 0.00045 0.98
Patos 8.31 156.9 -0.05298 ± 0.02273 0.00637 ± 0.00081 0.95
Pupal stage
Campina Grande 11.1 38.2 -0.29193 ± 0.21694 0.02612 ± 0.00776 0.79
João Pessoa 7.31 49.8 -0.14683 ± 0.17590 0.02006 ± 0.00629 0.77
Patos 11.9 35.4 -0.33578 ± 0.12554 0.02824 ± 0.00449 0.92
Full development (egg to adult)
Campina Grande 9.57 261.0 -0.03667 ± 0.01830 0.00383 ± 0.00065 0.91
João Pessoa 7.30 290.6 -0.02513 ± 0.01259 0.00344 ± 0.00045 0.95
Patos 9.65 264.5 -0.03648 ± 0.01688 0.00378 ± 0.00060 0.92
Vol. 41, no. 1 Journal of Vector Ecology 7

Table 6. Number of annual generations estimated for laboratory and field populations of Aedes aegypti in Campina Grande, João Pessoa,
and Patos.

Laboratory Annual Generations Field


Population
Annual
16º C 22º C 28º C 33º C 36º C Average o C
Generations
Campina Grande 9.0 17.3 25.7 32.7 37.0 23.6 23.6
João Pessoa 10.9 18.4 26.0 32.2 36.0 24.7 24.7
Patos 8.7 17.0 25.3 32.2 36.3 28.0 28.0

highly unfavorable to adult longevity in all populations. In Patos, For the larval stage, the Campina Grande population exhibited
temperatures between 22 and 33° C were favorable to both male the fastest development (b = 0.00715) compared with the other
and female longevity, with no significant difference between them. two populations (b = 0.00637 for Patos and b = 0.00710 for João
However, in Campina Grande and João Pessoa, male and female Pessoa. When examining the full life cycle (egg to adult), the
longevity were significantly reduced at 33° C (Campina Grande Campina Grande population exhibited faster development (b =
pfemale < 0.0001; pmale < 0.0001)/( João Pessoa pfemale < 0.0001; pmale < 0.00383), followed by the João Pessoa population (b = 0.00378).
0.0001) compared with 22 and 28° C, respectively. In general, João Based on the thermal requirements for Ae. aegypti
Pessoa males and females were longer-lived than mosquitoes from development and laboratory temperatures, we found that the
the other two cities (Table 4). number of annual generations varies between 8.7 (at 16° C) to 37
The temperature extremes of 16 and 36° C decreased the (at 36 °C). On the basis of these results and data on the typical
number of eggs per female considerably, with 16° C resulting climate in each region, we observed that the number of insect
in the lowest fecundity, between 1.46 eggs/Patos female and generations is higher in Patos (28.0) than in Campina Grande
3.5 eggs/Campina Grande female. The largest number of eggs/ (23.6) or João Pessoa (24.7) (Table 6). Therefore, increase in the
female (average = 262.3) was observed at 28° C in João Pessoa. Ae. aegypti population in Patos is likely to be faster than that in
Considering the overall average of all populations across all the other two cities.
temperatures, the females of João Pessoa exhibited high fecundity
(101.6 eggs/female). DISCUSSION

Developmental thermal requirements and estimation of Ae. Climate tendencies and potential effects on vector expansion
aegypti annual generation number Climate tendencies estimated for the regions of Campina
The development speed of Ae. aegypti responded significantly Grande, João Pessoa, and Patos are similar to patterns described
to an increase in temperature. The estimated values for Tb and (K) in the 5th IPCC-AR5 report, which found a progressive
in Campina Grande, João Pessoa, and Patos populations varied temperature increase over the past 100 years, caused primarily
between immature development stages (egg, larval, pupal) and the by anthropogenic activity but also by climate variability. Other
full life cycle. states in the northeastern region of Brazil are also experiencing
In the João Pessoa sample, we observed the lowest Tb for a trend of increasing temperature. For example, cities such as
viable egg (4.32° C) and pupal (7.31° C) stages, as well as for Teresina, Piaui, and Sao Luís, Maranhão are projected to have an
the full egg to adult cycle (7.30° C), whereas the lowest Tb for a average increase of approximately 0.014° C per year, causing a rise
viable larval stage occurred in the Patos sample (8.31° C). These in temperature of 0.62° C by 2050 and 1.34° C by 2100 (Santos
data suggest that the João Pessoa and Patos populations have et al. 2010). Collectively, our results combined with previous data
higher tolerances to reduced environment temperature (Table 5). suggest that neotropical regions will tend to grow hotter over the
However, we also note that Patos mosquitoes exhibited the highest years. On a worldwide scale, the IPCC affirms this trend of warmer
Tb (11.9° C) across all stages and populations. climates and predicts that 2016–2035 will experience an increase
Respectively, K values obtained from egg, larval, and pupal of 0.3 to 0.7° C in global mean surface temperature, relative to
stages were as follows: 74.6, 139.8, and 38.2 GD for Campina 1986–2005.
Grande; 90.9, 140.8, and 49.8 GD for João Pessoa; 73.3, 156.9, and Our projected temperature increases for Campina Grande
35.4 for Patos. As the thermal constant is the sum of favorable (33.7° C) and João Pessoa (32.6° C) by 2032 were similar to the
temperatures for mosquito development, 261.0 GD (Campina 30.4 to 34.8° C projections of the IPCC (2013). Because these
Grande), 290.6 GD (João Pessoa), and 264.5 GD (Patos) were temperature conditions are favorable to Ae. aegypti development
required to complete the full Ae. aegypti life cycle in each of the (Tables 1–6), future climatic changes will likely encourage the
three cities. spread and expansion of Ae. aegypti. Patos is a notable exception,
The slope of the regression equations for each life stage however, because the city’s estimated 2032 temperature of 39.1
represents developmental speed, where a steeper slope indicates °C is too hot for Ae. aegypti. Overall, as regional climates shift to
a higher development speed. The Patos population exhibited the become warmer, the resultant changes in Ae. aegypti populations
steepest slopes in egg (b = 0.01363) and pupal (b = 0.02824) stages. (Vargas et al. 2010) should also influence the distribution of
8 Journal of Vector Ecology June 2016

dengue (Campbell et al. 2015). and likely to reduce longevity. Our longevity results are similar
to a previous study showing reduced longevity with increasing
Effect of temperature on the Ae. aegypti life cycle temperatures and significantly higher mortality for females than
Most of the temperatures selected for this study allowed Ae. for males (Beserra et al. 2009). However, studies in Ae. albopictus
aegypti populations to fully develop without causing deleterious found that females tended to live longer than males (Löwenberg
effects. The sole exception was 39° C, which suppressed and Navarro-Silva 2004, Delatte et al. 2009).
embryonic development and led to larval death within hours of
hatching. The negative effect of the 39° C condition is consistent Thermal requirements and number of annual generations
with the influence of temperature on culicid vector development The Campina Grande, João Pessoa, and Patos populations
(Mohammed and Chadee 2011, Zequi and Lopes 2012) and differed in thermal requirements at all stages of the life cycle. The
suggests that 39° C approaches the lethal temperature (Mourya et João Pessoa population possessed the lowest base temperatures
al. 2004, Aghdam et al. 2009, Couret et al. 2014) for Ae. aegypti. required for successful development, reflecting their ability to
According to Eisen et al. (2014), the relationship between water tolerate gradual temperature reduction to the threshold at which
temperature and development rate is similar for eggs, larvae, and development ceases. In general, variation in Tb and K values may
pupae. At temperatures favorable to the life cycle, insects not indicate adaptability to adverse environmental conditions that
only complete their development but do so more quickly, which require an immediate response to temperature changes. The rapid
may enhance vector competence for arboviruses (Muturi et al. proportional development between instars following rising water
2012). Above the optimal temperature, development rates remain temperatures is an example of such an immediate response.
relatively stable and may decrease slightly until temperatures reach Tb and K values of all developmental stages were generally
an upper limit, at which point development drops dramatically. within previously reported ranges (Beserra et al. 2006), regardless
This upper limit occurs at ∼38 to 42° C (Eisen et al. 2014), of population origin. One exception was our K value for the pupal
corroborating our findings. Despite the lack of full life cycle data stage, which was higher at 35 GD than the range of 19.6–32.1
at 39° C, the fact that some larvae still hatched indicates a possible GD reported by Beserra et al. (2006). Beserra et al. (2009) have
physiological adaptive response to high water temperatures (37.9 also found tb and K within the ranges above. However, a later
to 38.5° C under the 39° C condition). study by Beserra et al. (2009) reported observed Tb and K that
According to Beserra et al. (2009), development time and were generally lower than those reported in this study, indicating
temperature are inversely related, and the optimum growth considerable variation in these values. A very low value of Tb for
range is between 22 and 32° C. Insects that develop within this Ae. aegypti was probably caused by physiological differences of
optimum range experience improvements in other intrinsic each stage when exposed to stressful environmental conditions.
characteristics, such as starvation resistance (Padmanabha et One major caveat in our study is the use of constant
al. 2011). Temperature-influenced variation in development temperatures in the laboratory. Some authors (Carrington et al.
and related characteristics have been reported in Ae. aegypti 2013a) have suggested that such conditions may not accurately
populations originating from several cities in the Agreste and reflect the variable environmental conditions in the field. For
Sertão da Paraíba mesoregions, with each population differing in example, estimates of degree/days will differ under constant
ways that reflected eco-climatic adaptations to their home regions versus fluctuating temperatures. Carrington et al. (2013b) also
(Beserra et al. 2006). noted that in their Thailand Ae. aegypti population, they were
The mean viability of egg, larval, and pupal stages for all unable to find a significant difference in developmental stages
population samples was high (above 80%), corroborating previous based on K values calculated with constant temperature, while
reports (Beserra et al. 2006, Tejerina et al. 2009). However, we differences emerged under fluctuating temperatures. While we
should note that due to differences in experimental conditions acknowledge this issue, we were able to obtain significant results
such as variation in feed, insect density, amount of water, insect using constant temperatures, suggesting that the importance of
strain, and equipment, comparisons across multiple studies may using natural temperature variation may depend on the specific
not always be reliable and should be considered with caution Ae. aegypti population.
when the objective is to define the best ecological parameters of Our study strongly suggests that future thermal conditions
the vector (Walsh et al. 2011). of the three examined cities will result in Ae. aegypti population
The temperature extremes of 16 and 36° C considerably growth, as well as increases in dispersion and expansion.
decreased adult longevity and female fecundity, similar to the Specifically, the optimal temperature (22 to 36° C) for Ae.
findings of Costa et al. (2010). Twice as many female Ae. aegypti aegypti development falls within both the current and projected
survived when subjected to 25 vs 35° C, resulting in 40% more temperature ranges for Campina Grande (max. = 33.7° C and
eggs produced. According to Carrington (2013a) that evaluated min. = 16.6° C), João Pessoa (max. = 32.8° C and min. = 18.8° C),
temperature fluctuations (DTR) in an Ae. aegypti population of and Patos (max. = 39.1° C and min. = 16.8° C). These favorable
Thailand, females from the 35° C constant treatment were the only temperatures resulted in a larger number of generations per
ones to successfully take a blood meal. The mean number of eggs year, most notably in Patos, and increased development speed in
laid was 25.5 eggs/female. At 35° C, with small fluctuations, no Campina Grande and João Pessoa. Both factors contributed to an
females were interested in feeding on human blood. At 16° C the Ae. aegypti population spike by shortening the time required for
authors reported that the reproduction had failed. Males tended to completing a full life cycle and reproducing.
live longer than females at most temperatures. This pattern may be To conclude, our results showed that local populations of
due to the intensity of oviposition, which is energetically expensive Ae. aegypti were able to complete the cycle of life in extreme
Vol. 41, no. 1 Journal of Vector Ecology 9

temperatures. Projected thermal increases in the neotropics are Costa, E.A.P.A., E.M.M. Santos, J.C. Correia, and C.M.R.
likely to enhance Ae. aegypti persistence of the vector in the area, Albuquerque. 2010. Impact of small variations in temperature
dispersal, and expansion. The spread of a major vector will have and humidity on the reproductive activity and survival of
obvious consequences for disease transmission. The ecological Aedes aegypti (Diptera, Culicidae). Rev. Bras. Entomol. 54:
data of this study can be used to refine Ae. aegypti monitoring 488-493.
strategies and improve existing preventive or control measures. Couret, J., E. Dotson, and M.Q. Benedict. 2014. Temperature, larval
diet, and density effects on development rate and survival of
Aedes aegypti (Diptera: Culicidae). PLoS ONE 9(2): e87468.
Acknowledgments
Delatte, H., G. Gimonneau, A.Triboire, and E.D. Fontenille.
2009. Influence of temperature on immature development,
Thanks to the Municipal Health Department of Campina
survival, longevity, fecundity, and gonotrophic cycles of Aedes
Grande, João Pessoa, and Patos, and to Paraíba State University
albopictus, vector of chikungunya and dengue in the Indian
for supporting this research.
Ocean. J. Med. Entomol. 46: 33-41.
Donalísio, M.R. and C.M Glasser. 2002. Vigilância entomológica
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