October 23, 2008 20:4 WSPC/129-JBS 00269

Journal of Biological Systems, Vol. 16, No. 4 (2008) 565–577

c World Scientific Publishing Company

ASSESSING THE SUITABILITY OF STERILE INSECT

TECHNIQUE APPLIED TO AEDES AEGYPTI

CLAUDIA PIO FERREIRA

IBB — Departamento de Bioestatı́stica — UNESP
Caixa Postal 510, CEP: 18618-000, Botucatu, SP, Brasil
pio@ibb.unesp.br

HYUN MO YANG
IMECC — Departamento de Matemática Aplicada
Caixa Postal 6065, CEP: 13083-859, Campinas, SP, Brasil
hyunyang@ime.unicamp.br

LOURDES ESTEVA
Departamento de Matemáticas, Faculdad de Ciencias
UNAM 04510, Mexico, D.F., Mexico
lesteva@lya.fceincias.unam.mx

Received 29 September 2007

Revised 31 July 2008

The efficacy of biological control of Aedes aegypti mosquitoes using Sterile Insect Tech-
nique (SIT) is analyzed. This approach has shown to be very efficient on agricultural
plagues and has become an alternative control strategy to the usual technique of insec-
ticide application, which promotes resistance against chemical controls and is harmful
to other species that live in the same mosquito habitat. By using a discrete cellular
automata approach we have shown that in the case of Aedes aegypti, the spatially het-
erogeneous distribution of oviposition containers and the mosquito behavior, especially
with respect to mating, make the application of STI difficult or impracticable.

Keywords: Cellular Automata; Biological Control; Aedes aegypti; STI Technique.

1. Introduction
The use of genetic control of pest insects population initiated in the 1930s–59s
with the works of Knipling, Bushland, Muller, and Serebrovsky.1–4 Since then, the
developed techniques have been based on the introduction of genetic mutations
in the native population during mating. In general, it aims at suppressing or dis-
placing the native population in favor of one species that is resistant to the agent
causing the disease.
The Sterile Insect Technique (SIT) is based on the release of a large number
of sterile males over the area affected by plague. These sterile males compete with
the native ones to mate with wild females, which mate with them and produce
nonviable eggs. This technique is species-specific, environmentally non-polluting

565
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566 Ferreira et al.

and consists in three stages: mass rearing, sexual sterilization usually with gamma
radiation and release of the sterile males over the target area.
In general, the viability of the biological control depends on several factors,
such as: complete sterilization of the insects; massive creation in laboratory must
be easy and relatively cheap; elimination of the females during the production
process; sterile males have to compete successfully with the native ones for the
females; mating number of females must also be small; the radiated insects should
not cause damage or transmit pathogenic agents to man, animals or plants and
dispersion in the field must be easy.
Moreover, since the cost of the technique is proportional to the size of wild
populations, it should be combined with the usual techniques of insect control,
or used at the time of the year when the pest population is at its lowest. Also,
the choice of the target area size is an important factor due to the possibility of
recolonization from adjacent infested untreated areas. Therefore, it is essential to
know the biology, ecology and behavior of the target species.5
In 1955 the eradication of the screwworm fly, the second most important plague
caused by arthropods, was carried out for the first time on the Caribbean island of
Curacao.6 The entire island was treated weekly with about 800 sterile flies/mile2
and eradication was reached after seven weeks. Since then, this technique has been
studied and applied in the control of insect pests, mainly agricultural. Because
vector control is one of the few proved ways to reduce transmission of many vector-
borne diseases, there is an increasing effort to use this technique on mosquito
populations.7
In particular, mathematical models can be a useful tool to create and test dif-
ferent scenarios concerning biological problems. Different, continuous or discrete
approaches can be done and the choice between them depends on the specific prob-
lem. For example, there has recently been a growing interest in spatial issues in
ecology, such as how locality of competition and the range of dispersal play a role
in ecosystem dynamics. These models are usually investigated via simulation or
else they are simplified by essentially throwing away the whole detailed spatial
structure, resulting in the so-called metapopulations or mean-field models. How-
ever, when the local interactions are important for the dynamics of the process, the
cellular automata models (CA) are a very useful and simple tool.
In summary, a CA is a mathematical model with discrete time, space and vari-
ables, composed of lots of identical, simple components arrangement on a lattice.
These components interacted with each other and change states according to local
rules that specify how the automaton develops in time. The emergence of a com-
plex behavior from simple local rules is a characteristic of the CA models.8 First
introduced by John von Neumann in the early 1950s to act as simple models of bio-
logical self-reproductions, CA has been used for model plant growth, propagation
of infection disease, social dynamics, forest fires and also as a discrete version of
partial differential equations in one or more variables.9
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Suitability of Sterile Insect Technique Applied to A. aegypti 567

In this work, a cellular automata model to analyze the biological control

efforts used on the mosquito Aedes aegypti was developed. This approach captures
essential features of mosquito Aedes, such as spatial heterogeneity, spreading and
colonization.10 The main objective of this paper is to compare the efficiency of bio-
logical control when we consider two situations: homogeneous and heterogeneous
distributions of mosquito populations associated with the spatial distribution of
oviposition containers. Also, the control efficacy related to the time interval of the
SIT technique application as well as the proportion between irradiated and wild
males have been analyzed.
This paper is organized as follows: Sec. 2 presents the cellular automata model
used to describe the population dynamics of native and irradiated mosquitoes;
Sec. 3 shows the results related to biological control efficiency in a homogeneous and
heterogeneous spatial distribution of mosquito population; finally, Sec. 4 presents
the conclusion.

2. The Cellular Automata Model

The major difficulty associated with the mosquito Aedes control is associated with
the oviposition containers. The doctrine of container homogeneity related to size
and spatial distribution results in non-prioritized mosquito controls and a basic
lack of understanding of the causes of the problem.11 In general, the wild male
mosquito emerges before the female and the meeting between them, which results
in fertile female mosquito, takes place in the neighborhood of the containers. This
mosquito behavior as well as the spatial distribution of oviposition containers are
easily reproduced using the cellular automata approach. Also, colonization, per-
sistence and distribution of the mosquito population in controlled regions can be
reproduced using this formalism.10
To model the space localization of the containers together with the mosquitoes
behavior, we developed a stochastic two-dimensional (L × L) cellular automata.
With each site we associated a five-state automaton that represents the non-fertile
female (not mating yet), fertile female (can produce viable eggs), wild male, ste-
rile male and empty state. The empty sites represent females that had mated with
sterile males and cannot produce viable eggs, therefore do not contribute to the
overall dynamics.12 One time step corresponds to the parallel update of the entire
lattice and will correspond to one day. Between time steps, diffusion is imple-
mented using Margolus neighborhood.8 Briefly, the Margolus neighborhood is a
cell-interconnection scheme constructed following the steps described below:

1. The array of cells is partitioned into a collection of finite, disjoint and uniformly
arranged pieces called blocks.
2. A block rule is given that looks at the contents of a block and updates the whole
block (rather than a single cell as in a ordinary CA). The same rule is applied
October 23, 2008 20:4 WSPC/129-JBS 00269

568 Ferreira et al.

to every block. Blocks do not overlap and no information is exchanged between

adjacent blocks.
3. The partition is changed from one step to the next, so as to have some overlap
between blocks used at one step and those used at the next one.

Therefore, the temporal evolution of mosquito populations is given by the fol-

lowing local rules applied in a Moore neighborhood, which comprises the eight cells
surrounding a central cell on a two-dimensional square lattice:

1. Sites occupied by non-fertile female (I) can become empty with probability µI +
γ1 β1 , because of mortality or mating with sterile males; or can become occupied
by fertile females with probability γ2 β2 , where γ1 and γ2 are the numbers of,
respectively, sterile and wild males in the neighborhood; β1 and β2 are meeting
probabilities;
2. Sites occupied by female mosquitoes (F), wild (M) or sterile males (R) can
become empty with probability µ (mortality);
3. Empty sites (V) can become occupied with probability γ by new mosquitoes that
emerge from the oviposition containers (aquatic emergence rate). The proportion
between female and male emergence is given by the parameter r. Emergence
occurs in the neighborhood of the oviposition containers, defined by the ratio D
with a center in the position of the oviposition container;
4. Mosquito oviposition occurs inside oviposition containers and is proportional to
Cγ3 φ, where C, γ3 and φ are, respectively, the carrying capacity of the container,
the number of fertile females in the oviposition neighborhood and the oviposition
rate; and
5. There are N oviposition containers distributed on the lattice, and in each of
them a fraction of the aquatic population dies with probability µA times the
number of aquatic individuals.

The transition rules among the automaton states defined above were constructed
based on the compartmental model described in Esteva.12 To compare the control
efficacy in homogeneous and heterogeneous spatial distribution of mosquito popu-
lations, all results are obtained using the two distinct lattices shown in Fig. 1.

3. Results and Discussion

Oviposition containers and the wild population are distributed on the lattice at
the beginning of the simulation (in our examples 20% of the lattice is occupied
by native female and male mosquitoes distributed randomly). All simulations were
performed taking into account a square toroidal lattice with a linear dimension
L = 250. Meanwhile, the oviposition containers were always distributed inside a
square region smaller that the previous one (L
= 190), in such a way that the
same results are obtained for an open square lattice.10
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Suitability of Sterile Insect Technique Applied to A. aegypti 569

(a) (b)

Fig. 1. Two different spatial distributions of oviposition containers used in simulations: (a) homo-
geneous and (b) heterogeneous. In the both cases, the number of recipients is N = 324 and the
lattice linear size L = 250.

Initially, the simulation is carried on until the native population becomes sta-
tionery, which is defined as in Caswell and Etter,13 i.e., when the last-squares
regression line through the values of mosquito population for the last 100 time
steps had a slope of less than 0.001, the simulation was considered close enough to
equilibrium and then the suppression process is started by distributing randomly
the sterile male mosquitoes in the empty sites of the lattice during a time interval,
∆, in a proportion of  sterile mosquitoes for each native male mosquito. The results
are shown for D = 15, C = 30 and 2 diffusion steps. The other parameters are:
φ = 0.1, µA = 0.015 (66 days), µI = 0.03 (33 days), µ = 0.04 (25 days), γ = 0.1
(10 days). Mean values were obtained from 50 simulations.
We assume that r = 0.5 and β1 = β2 = 0.1077, therefore, the maximum prob-
ability of oviposition is 9 × 0.1077 ∼ 1 if all cells in a Moore neighborhood of the
oviposition containers are occupied, and that sterile and wild males are equally fit.
For a detailed analysis of the parameters space see Ferreira.10
We remark that for this set of parameters the basic offspring of natural
mosquitoes (average number of viable female descendants that an adult female
mosquito produces during its fertile period10 ) is bigger than one, and therefore
the continuous model given in Esteva12 establishes the persistence of the mosquito
population, regardless of the carrying capacity (related to the number and size of
the containers) as long as it is different from zero.
Figure 2 shows the number of non-fertile female population (I) in the steady
state when we consider random and uniform distributions of the oviposition con-
tainers. We notice that for 110 < N < 250, persistence of mosquitoes is obtained
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570 Ferreira et al.

3000

2000

1000

0
0 100 200 300 400 500
N

Fig. 2. Steady state of the non-fertile female population, I, as a function of the number of
oviposition containers, N, without biological control. The different curves are related to uniform
(•) and random (◦) distribution of oviposition containers.

only for the random distribution of the containers; for 250 < N < 350 persistence
is obtained for uniform and random distribution, but the number of mosquitoes
is much smaller for the uniform distribution. Finally, for N > 350 the results
obtained with the two distributions are practically the same. Therefore, for the
cellular automata model, there exists a critical point depending on the environ-
mental carrying capacity, N × C, where N is the number of containers and C, the
size of each container, below which population becomes extinct. This critical point
depends on the spatial distribution of the containers (Fig. 1), mosquito diffusion
speed, and the size of the neighborhood containers. Then, for a fixed C, there is
a threshold number Nc such that if N < Nc the mosquito population becomes
extinct. For a uniform distribution we obtained Nc ≈ 250, whereas for a random
distribution we obtained Nc ≈ 110. Therefore, a random distribution facilitates dis-
persion and colonization of mosquitoes, since the threshold number of containers for
persistence, Nc is smaller than the one for uniform distribution. Furthermore, for
Nc large the cellular automata model reproduces the qualitative behavior obtained
by the continuous model.12
In order to understand why a random distribution of oviposition containers pro-
motes mosquito persistence, in Fig. 3 we display the average distance, Φ, and the
minimum distance, η, between successive oviposition containers. We can see that
Φ is almost the same for both distributions, but for all values of N the random
distribution generates, on average, space distributions with a lower minimum dis-
tance between the containers, facilitating colonization and persistence of mosquito
populations.
In fact, the threshold obtained for both spatial distributions of oviposition con-
tainers (Fig. 2) are related to the percolation properties. For N > Nc we have a
cluster of female mosquitoes extending from one side of the lattice to the other,
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Suitability of Sterile Insect Technique Applied to A. aegypti 571

40 110

Φ
100

90
η
20 0 110 220 330 440 550
N

0
0 110 220 330 440 550
N

Fig. 3. Distance average, Φ, and the minor distance, η, between oviposition containers as a
function of the number of oviposition containers, N. The different curves are related to uniform
(•) and random (◦) distribution of oviposition containers.

whereas for N < Nc no such cluster exists. However, determining critical behavior
from steady-state simulations is often very difficult due to large fluctuations, crit-
ical slowing down, finite-size effects and difficulties in exactly locating the critical
point. Therefore, these phase transitions will be studied in a future paper using
time-dependent simulations.14
Figure 4 shows the time evolution of the mosquito population [fertile female
(F), wild male (M) and sterile male (R)] for a uniform distribution of N = 326
oviposition containers. The release of the sterile mosquitoes occurs at t ≈ 1000

3000
F, M, R

1500

0
0 2500 5000 7500 10000
time

Fig. 4. Time evolution of fertile female, F (hatch line), wild males, M (dot line), and sterile
males, R (continuous line), for a uniform distribution of oviposition containers.
October 23, 2008 20:4 WSPC/129-JBS 00269

572 Ferreira et al.

during a period of time ∆ = 20 days, and it is proportional to the number of

native mosquitoes  = I/M = 7. The native population is reduced during the time
interval ∆, and then increases when control application is discontinued. The native
population after the SIT control is smaller than the population at the beginning of
the control, and its final size depends on the  value. This fact is associated with
a local extinction of the population in regions of the lattice that were colonized
before control, (bear in mind that the initial mosquito population was distributed
randomly on the lattice, and new colonizations started from oviposition contain-
ers). In general, the number of positive containers which have immature forms of
mosquito is lower than the number of containers distributed on the lattice. For a
random distribution of containers, the recovery dynamics after control is faster and
therefore local extinction is less probable (results not shown).
To measure the efficiency of the SIT technique, we define J, the accumulated

T
index control parameter, as J = (1 − Ac /A0 ) × 100, where A• = 0 F (t)dt is
the the accumulated number of female mosquitoes with (Ac ) and without (A0 )
controlling mechanisms applied on the mosquito population. Observe that Ac −
A0 measures the accumulated reduction in the number of female mosquitoes by
controlling mechanism in the range from 0 to T, therefore, J is the percentage of
reduction of female mosquitoes over the interval [0, T ].15 A similar index was used
to measure vaccine efficacy on malaria control programs.16
Figure 5 shows control efficacy measurement as a function of the time interval
when sterile mosquitoes are released, ∆, for a uniform distribution of N = 326
oviposition containers. The proportion of sterile and wild male mosquito is fixed in
 = 7. According to the above definition of J, note that it is not allowed to reach
the value of 100%, even when female mosquitoes are eliminated. For instance, when

100

80

60
J
40

20

0
0 10 20 30 40
∆

Fig. 5. Control efficacy, J, measures as a function of sterile mosquito time release, ∆, for a
uniform distribution of oviposition containers. The proportion of sterile and wild male mosquito
is fixed on  = 7.
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Suitability of Sterile Insect Technique Applied to A. aegypti 573

100

80

60
J

40

20

0
0 5 10 15
ε

Fig. 6. Control efficacy, J, measures as a function of the proportion of sterile and wild male
mosquito, , for a uniform distribution of oviposition containers. Sterile mosquito time release is
fixed on ∆ = 20.

the release of sterile mosquitoes occurs during a period of time larger than 40 days,
or ∆ ≥ 40, the mosquito population is extinguished, but the control index assumes
J ≈ 74%. The corresponding elimination index for a random containers distribution
is attained when ∆ ≥ 400, but mosquito extinction is not observed.
Figure 6 shows control efficacy measurement as a function of the proportion
between sterile and wild male mosquitoes, , for a uniform distribution of oviposi-
tion containers. The period of time that sterile mosquitoes are released is fixed in
∆ = 20, and all other parameters have the values defined previously. At  = 15 the
mosquito population is extinguished. Notwithstanding that, for a random distribu-
tion of oviposition containers and  = 30, the efficacy observed was below 5%, and
mosquito extinction is never observed.
Comparing Figs. 5 and 6 with respect to tangent slopes in each point, we notice
that for SIT control, increasing the ratio between wild and native males was more
effective than increasing the time for releasing sterile mosquitoes. Furthermore, the
two graphs increase monotonically until they reach a constant value near 80%,
which represents mosquito extinction.
In order to increase control efficacy for a random distribution of oviposition
containers, J was measured for a set of parameters above the critical value of the
carrying capacity given by N = 300. Also, the proportion of sterile and wild males
and the time for releasing sterile males were changed for these new simulations. In
this case, mosquito control is easier to obtain than for the previous one described
above. Figure 7 shows control measures efficacy as a function of sterile mosquito
time release, ∆, for a random distribution of oviposition containers. The proportion
between sterile and wild male mosquitoes is fixed on  = 7. At ∆ = 200, the index
J is almost 74%, but extinction is not observed yet.
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574 Ferreira et al.

100

80

60
J

40

20

0
0 50 100 150 200
∆

Fig. 7. Control efficacy, J, measures as a function of sterile mosquito time release, ∆, for a
random distribution of oviposition containers. The proportion of sterile and wild male mosquitoes
is fixed on  = 7.

100

80

60
J

40

20

0
0 5 10 15 20 25
ε

Fig. 8. Control efficacy, J, measures as a function of the proportion of sterile and wild male
mosquito, , for a random distribution of oviposition containers. The sterile mosquito time release
is fixed on ∆ = 100.

Figure 8 shows control efficacy measurement as a function of the proportion

of sterile and wild male mosquitoes, , for a random distribution of oviposition
containers (N = 300). The sterile mosquito time release is fixed on ∆ = 100. At
 = 25 the index J is almost 62%, but extinction has not been observed yet.
The continuous compartmental model described in Esteva12 shows that in the
absence of sterile insects the condition for the existence of natural insects is R > 1,
where the parameter R is the basic offspring number. However, when sterile insects
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Suitability of Sterile Insect Technique Applied to A. aegypti 575

are released, the threshold values are situated at R = R∗ (> 1), indicating that one of
the conditions for the existence of natural insects is furnished by increasing R. This
is due to the decrease in mating fertilized females with sterile male insects, resulting
in diminishing net production of offspring. This value depends on the parameter S
that measures the number of mated but not fertilized female insects in comparison
with the fertilized ones, which depends on the proportion of sterile insects that are
sprayed in adequate places and on the lost fitness associated with the sterilization
process. If S is sufficiently high, the next generation of wild insects will be smaller
than the present one since a proportion of eggs will not hatch. Therefore, if sterile
male insects are sprayed for a long period of time, natural insect populations will
be driven to zero. In particular, the trivial solution (mosquito extinction) is always
stable and if R > 1 and S > S c the non-trivial equilibrium coexist with the trivial
one. In the region of coexistence, numerical simulations indicate that SIT would
have a low chance of success.
The results shown in Figs. 5, 6, 7 and 8 for the cellular automata model agree
with those provided by the continuous compartmental model.12 The two mod-
els show that control efficacy is reduced by the non-homogeneous distribution of
breeding sites but control efficacy is overestimated by continuous compartmental
modeling. In this case, the increase of S can be offset by increasing the number
of sterile or applying alternative controls (like larvacide and insecticide) together
with SIT to decrease the number of viable female mosquitoes. For the automata
cellular model, extinction is not observed for a spatially heterogeneous distribution
of mosquitoes, even in the best situation.

4. Conclusion
The automata cellular model proposed here was able to reproduce aspects of Aedes
mosquito behavior, such as spatial heterogeneity, infestation and persistence. As
in other CA models, such a success shows the importance of local interactions for
the mosquito population dynamics. The efficacy of SIT control was measured for
two distributions of oviposition containers: homogeneous and heterogeneous, which
reproduce different spatial distributions of mosquitoes. The results show that even
in the best situation, when sterile males have the same fitness as the wild mosquito
and the number of mosquito is not large, spatially heterogeneous distribution of
mosquitoes makes the use of SIT technique difficult or impracticable. In fact, this
result is correlated with the observation that non-homogeneous spatial distribution
on breeding sites facilitates colonization and persistence of Aedes aegypti. This result
is not accessed by the compartmental model described in Esteva.12
The model proposed here predicts that for a spatially uniform distribution
of breeding sites, and consequently quasi-homogeneous distribution of female
mosquitoes, the SIT technique is suitable to eliminate wild mosquito populations.
This result can be borrowed to explain the success in controlling agricultural plagues
or screwworm fly by SIT technique: reproduction does not depend on the spatial
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576 Ferreira et al.

distribution of breeding sites and, naturally, the target area is also well delimited.
This technique is also suitable for other mosquitoes which have dispersion, sex-
ual behavior and adult habitat preferences different from aedes mosquito, such as
Anopheles, the malaria vector.
Furthermore, as cited before, the threshold obtained for the two spatial distri-
bution of oviposition containers (Fig. 2) are related to the percolation properties.
Therefore, a great amount of interesting theoretical work can be done, such as
cluster analysis and determination of the transition universality class.17

Acknowledgments
The work of C.P.F. is supported by Fundação de Amparo a Pesquisa do Estado de
São Paulo (FAPESP), Project No. 05/51671-6 (fellowship awarded by FAPESP).
H.M.Y. is support in part by Conselho Nacional de Desenvolvimento Cientı́fico e
Tecnológico (CNPq) and FAPESP, Project No. 04/07075-7. The third author of this
paper, Lourdes Esteva was supported by grant IN108607-03 of PAPIIT UNAM.

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