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Abstract

Observation on predation activities of guppies (Poecilia reticulata) on the larvae of three species of mosquito, namely Aedes albopictus, Aedes aegypti, and Culex quinquefasciatus was carried out under laboratory conditions. Male and female guppies were used as predators for predation experiments on the 4th instars of mosquito larvae. The daily feeding rates comparing male and female guppies on mosquito larvae were different; the female guppies consumed more mosquito larvae than male guppies did. The daily feeding rates of female guppies were 121.3 for Ae. aegypti, 105.6 for Ae. albopictus, and 72.3 for Cx. quinquefasciatus. The daily feeding rates of male guppies were 98.6 for Ae. aegypti, 73.6 for Ae. albopictus, and 47.6 for Cx. quinquefasciatus. In terms of prey preference, there was greater preference towards mosquito larvae of Ae. aegypti, followed by Ae. albopictus, and the least preferred was Cx. quinquefasciatus. Male and female guppies consumed more mosquito larvae during lights on (day time) compared with lights off (night time). The water volume, prey species, number of fish predators available, prey densities, and prey's sex also influenced the predation activities.
Guppies As predAtors of Mosquito LArvAe
Vol 45 No. 2 March 2014 299
Correspondence: SNR Saleeza, Institute of Bio-
logical Sciences, Faculty of Science, University
Malaya, 50603 Kuala Lumpur, Malaysia.
E-mail: saleeza84@siswa.um.edu.my
GUPPIES AS PREDATORS OF COMMON MOSQUITO
LARVAE IN MALAYSIA
SNR Saleeza1, Y Norma-Rashid1,21
1Institute of Biological Sciences, Faculty of Science, University Malaya, Kuala Lumpur,
Malaysia; 2Department of Organismic and Evolutionary Biology, Harvard University,
Cambridge, MA, USA
Abstract. Observation on predation activities of guppies (Poecilia reticulata) on
the larvae of three species of mosquito, namely Aedes albopictus, Aedes aegypti,
and Culex quinquefasciatus was carried out under laboratory conditions. Male and
female guppies were used as predators for predation experiments on the 4th instars
of mosquito larvae. The daily feeding rates comparing male and female guppies
on mosquito larvae were different; the female guppies consumed more mosquito
larvae than male guppies did. The daily feeding rates of female guppies were
121.3 for Ae. aegypti, 105.6 for Ae. albopictus, and 72.3 for Cx. quinquefasciatus. The
daily feeding rates of male guppies were 98.6 for Ae. aegypti, 73.6 for Ae. albopictus,
and 47.6 for Cx. quinquefasciatus. In terms of prey preference, there was greater
preference towards mosquito larvae of Ae. aegypti, followed by Ae. albopictus, and
the least preferred was Cx. quinquefasciatus. Male and female guppies consumed
more mosquito larvae during lights on (day time) compared with lights off (night


Keywords: Ae. aegypti, Ae. albopictus, Culex quinquefasciatus, guppy, predation
activities, Malaysia
sphaericus (WHO, 1986). Biological control
of mosquitoes was very popular during
the early part of the 20th century, but this
type of control has been replaced with the
insecticidal control due to easy availabi-
lity of chemicals such as organochlorines
and organophosphates. However, because
of problems with insecticide resistance
and greater awareness of environmental
contamination, there has been renewed
interest in biological methods (Service,
2000).
Among the popular biocontrol agents
against mosquito populations are the
  Gam-
 and G. holbrooki. This species,
however, is ineffective for the control of
INTRODUCTION
Natural predators are used in bio-
logical control. This type of control is an
environmentally friendly preventative
method to control, among others, popu-
lations of pest organisms (Becker, 2006).
Several organisms have proved to be ef-
fective predators against mosquito larvae,

genus Toxorhynchites, dragonflies and
-
tode, Bacillus thuringiensis H-14, and B.
southeAst AsiAn J trop Med pubLic heALth
300 Vol 45 No. 2 March 2014
mosquitoes in what is termed as “contain-
er habitats”, that is, mosquito breeding
places such as phytotelmata, tree holes,
bamboo nodes, and discarded containers
(Kumar and Hwang, 2006). Another com-

the South African guppy, Poecilia reticulata,
which can tolerate waters of high tem-
peratures or that are organically polluted.
Carps, Cyprinus carpio, found in Chinese
Aedes aegypti.
Clarias fuscus in Myanmar,
Oreochromis, Tilapia species in Africa, and
Aplocheilus species in Europe and Asia are
placed in water storage tanks to control
Ae. aegypti (Service, 2000). Additionally,
guppies of the Poecilia reticulata species are
used to control dengue vector, Ae. aegypti,
in domestic water storage containers in
rural areas of Cambodia (Seng et al, 2008).

agents has been proved effective towards
malaria mosquito larvae (Howard et al,
2007; Kweka et al, 2011). P. reticulata also
shows preference for other prey besides
mosquito larvae (Manna et al, 2008).In this

P. reticulata was investigated using mos-
quito larvae of Ae. aegypti, Ae. albopictus,
and Cx. quinquefasciatus as prey.
MATERIALS AND METHODS
The guppies, P. reticulata, used as
predators in the experiments were col-
lected in the drains of Putrajaya and Kuala

for their wet weights and lengths before
and after the experiment. Before the start

acclimatized to laboratory conditions
and were placed in plastic aquaria for
a period of one week prior to the actual


as a diet for maintenance. Guppies were
starved for 24 hours before introduction
to the experimental aquaria, as this period
would increase the motivation to feed
(Bhattacharjee, 2009).
The experimental aquaria contained
-
mentation. For this experiment, the daily
feeding rates of guppies for three species
of mosquito larvae were recorded. The
P. reticulata was exposed to 100 4th instar
larvae for each species of Ae. aegypti, Ae.
albopictus, and Cx. quinquefasciatus. Three
aquaria were arranged for each mosquito
species, and three replicates of experi-
ments were completed on separate days.
-

and the daily feeding rate was recorded
repeatedly at 3-hour interval.

were not used in subsequent experiments.
At each 3-hour interval, the water from
experimental aquaria was sieved and
transferred to a white tray to count the
number of mosquito larvae consumed

carried out within 24 hours from 5:00 AM
until 5:00 pM for ‘lights on’ and from 5:00
pM until 5:00 AM for ‘lights off’. Using
this experimental procedure, the active
 
P. reticulata could be obtained.
The second experimental setup was
to assess the relationship of feeding rate
with different water volumes together
with the number of predator and prey
densities. This procedure was done in
three replicates for each species the ex-
perimental protocols used are: 1) Aquaria

liter of water volume and 100 4th instar of


Guppies As predAtors of Mosquito LArvAe
Vol 45 No. 2 March 2014 301
volume and 100 4th instar of mosquito

two fish with 1 liter of water volume
and 100 4th instar of mosquito larvae; 4)


4th instar of mosquito larvae; 5) Aquaria

liter of water volume and 100 4th instar of


volume and 100 4th instar of mosquito lar-


4th instar of mosquito larvae; 8) Aquaria

liter of water volume and 200 4th instar of
mosquito larvae.
The data of daily consumption rate
of both male and female guppies were
analyzed using one-way ANOVA (SPSS®;
IBM, Armonk, NY), and the relationships
between consumption rate and variation
of water volume, prey species, number of
-
lyzed using multiple regression.
RESULTS
Exposing 100 4th instar mosquito lar-
vae of every species to a single predator
species assessed the daily feeding rate.
The number of larvae remaining was re-
corded at every 3-hour interval, and the
experiment was carried out over 24 hours.
The overall feeding rates of female

males for all 3 species of mosquitoes test-
ed. Both female and male guppies showed
greater preference for Ae. aegypti larvae,
followed by Ae. albopictus, and the least
preferred was Cx. quinquefasciatus (Fig 1).
It was observed that the female guppies
were more aggressive than male guppies
as they consumed more mosquito larvae
species. Both male and female guppies
spent most of their time at surface water
and were active in searching mosquito
larvae, but the female guppies were more
aggressive than male guppies. When the
mosquito larvae were released in the
aquaria, the first attack of guppy was
very fast.
The feeding rate between lights on
and lights off also varied between male
and female guppies, but both were active
during lights on. As shown in Fig 2, both
predators were active during lights on
as they consumed more mosquito larvae
during this time. The presence of light

can easily search and attack the prey. Some
studies indicate that when the water is tur-

because their vision is not clear (Robertis
et al, 2003; Turesson and Brönmark, 2007;
Jacobsen et al, 2014)
In this study, 100 and 200 4th instars of
mosquito larvae were used in the preda-
tion experiment. When 100 4th instars of
mosquito larvae were exposed to the gup-
pies, they consumed all mosquitoes, and
when 200 4th instars of mosquito larvae
were exposed to the guppies, more than
100 4th instars were consumed. Larvae
consumption increased, as there was an
increase in prey densities, until satiation
level was reached (Table 1).
From the regression equation, it was
observed that the feeding rate of male
guppies increased when water volume
was increased, and the number of preda-
tors was increased. Conversely, the feed-
ing rate of female guppies increased when
water volume and mosquito larvae densi-
ties were increased. All the three factors

male and female guppies.
southeAst AsiAn J trop Med pubLic heALth
302 Vol 45 No. 2 March 2014
Sex of Mosquito Water Fish (n) Mosquito Mean ± SE
guppies species volume densities
Male Ae. albopictus 1 1 100 49.67 ± 1.202
1 2 100 100.00 ± 0.000
1 1 200 53.00 ± 2.887
2 1 100 37.33 ± 1.453
Female Ae. albopictus 1 1 100 87.00 ± 7.572
1 2 100 100.00 ± 0.000
1 1 200 102.00 ± 10.599
2 1 100 73.00 ± 5.686
Male Ae. aegypti 1 1 100 77.00 ± 9.815
1 2 100 100.00 ± 0.000
1 1 200 101.00 ± 2.082
2 1 100 60.00 ± 4.726
Female Ae. aegypti 1 1 100 100.00 ± 0.000
1 2 100 100.00 ± 0.000
1 1 200 123.00 ± 4.619
2 1 100 85.00 ± 2.887
Male Cx. quinquefasciatus 1 1 100 46.00 ± 5.196
1 2 100 100.00 ± 0.000
1 1 200 50.00 ± 8.544
2 1 100 34.00 ± 6.083
Female Cx. quinquefasciatus 1 1 100 77.00 ± 6.928
1 2 100 85.00 ± 4.041
1 1 200 94.00 ± 6.351
2 1 100 65.00 ± 4.041
Table 1
Feeding rate of male and female guppies in 24 hours (mean ± SE of 3 experiments)
on larvae of Ae. albopictus, Ae. aegypti, and Cx. quinquefasciatus with the variations in

Sex of guppies Equations for larval feeding rate R-value
Male guppy Y = 44.55 – 19.0 X1 + 37.22 X2 0.77
Female guppy Y = 93.83 + 17.16 X1 + 14.83 X2 0.67
Table 2

larvae by guppies.
Y, feeding rate of larvae; X1, water volume; X2, number of predator; R, multiple correlation coef-

Guppies As predAtors of Mosquito LArvAe
Vol 45 No. 2 March 2014 303
Number of mosquito larvae
consumed by guppies
Mosquito species
Female guppies
Male guppies
Cx. quinquefasciatus
Ae.albopictus Ae.aegypti
70
60
50
40
30
20
10
0
0
10
20
30
40
50
60
70
80
90
Light on Light off Light on Light off
Female Male
Number of mosquito larvae
consumed by guppies
Guppies
Cx. quinquefasciatus
Ae.albopictus
Ae.aegypti
Fig 1–Number of mosquito larvae consumed by
female and male guppies (P. reticulata) on Ae.
albopictus, Ae. aegypti, and Cx. quinquefasciatus
larvae.
Fig 2–Feeding rate of female and male guppies (P.
reticulata) on Ae. albopictus, Ae. aegypti, and Cx.
quinquefasciatus larvae in 24 hours during light
on and light off.
DISCUSSION
In this study, guppies were used as
predators against three common mosquito
larvae in Malaysia. Saleeza et al (2011)
reported that the three common mosquito
larvae, Ae. albopictus, Ae. aegypti, and Cx.
quinquefasciatus, are commonly found in
residential areas in both urban and sub-
The number of prey consumed var-
ies with the difference in body size. This
means that prey consumption increases
with body size (Manna et al, 2008). This
 -
alcanti et al (2007) who report that the ef-

and sex. Cavalcanti et al 

urban areas. A number of studies
have indicated that guppies of the
P. reticulata species are good pred-
ators, as they can control mosquito
larvae population (Manna et al,
2008; Seng et al, 2008; Anogwih
and Makanjuola, 2010; Ghosh et
al, 2011). However, guppies do not
choose Cx. quinquefasciatus when
other available foods are present
in polluted water or drain water,
such as plankton (Dua et al, 2007).
P. reticulata is a more effective
predator against Ae. albopictus
-
cies such as Puntius bimaculatus
and Rasbora caverii. A study in Sri
Lanka suggested that, in compari-
son to Toxorhynchites larvae, which

consumed more mosquito larvae
(Wijesinghe et al, 2009).
In this study, it was observed
that female guppies (P. reticulata)
ate mosquito larvae more than
male guppies did. This result
et
al (2008): female guppies ate more
than male guppies, with 122.9
and 74 Ae. aegypti larvae per day,
respectively. This is due to the
larger size of the female guppies.
Therefore, female guppies can
consume more mosquito larvae
than male guppies can.
southeAst AsiAn J trop Med pubLic heALth
304 Vol 45 No. 2 March 2014
Ae. aegypti larvae and found that the
       
and female guppies are more capable
to eradicate Ae. aegypti larvae than male
guppies are.
According to Neng et al (1987), the
 Clarias fuscus de-
pends on the body weight of the predator.


Anyaele and Obembe (2010), the adult

higher biocontrol potential compared to

feeding rate, the daily feeding rate of the
guppies on mosquito larvae species was
different between sexes. However, the
prey preferences of both sexes of guppy
were the same, as they preferred Ae. ae-
gypti > Ae. albopictus > Cx. quinquefasciatus
larvae, and they tried to avoid the pupa
stage of mosquito development.
Most frequently, male and female
guppies were at the water surface actively
searching and attacking mosquito larvae;
however, they totally avoided mosquito
pupae. This behavior has also been ob-
served by Anogwih and Makanjuola
(2010). Moreover, in this study, it was ob-
served that male and female guppies were
more active and consumed more mosquito
larvae during lights on period. Anyaele
  
eat more under lights on compared with

on their visual ability to search for prey.
However, according to Ghosh et al (2011),
this difference in eating behavior during
daytime and nighttime had no practical

In terms of prey preference among
the three species of mosquito larvae, both
sexes of guppy prefer Ae. aegypti larvae
compared with the other two species of

the selectivity of prey by predator are as
follows: how the prey escapes from the
predator (guppy), ability of the predator,
prey attraction, and posture of mosquito
larvae. Deacon (2010) states that the fac-

are vegetation, feeding behavior of differ-
ent mosquito genera, ability to escape, dis-
tinct morphology, posture in the water for
mosquito larvae, and color of the larvae.
In this study, both sexes of guppy
preferred Ae. aegypti larvae compared
with Ae. albopictus and Cx. quinquefasciatus
larvae. As suggested by Kesavaraju et al

by the behavior of prey species and de-
velopment stage of prey. This means that
different predator attacks different stage
of mosquito larvae. However, in this
study, the 3rd and 4th instar larvae used as
the trial experiment showed that guppy
preferred late-stage larvae compared with
early-stage larvae. The black color of the
Ae. aegypti larvae could be the factor that
attracted the guppy to attack and consume
them, unlike the Cx. quinquefasciatus lar-
vae that are pale in color.
Otherwise, Rajasekharan and Chow-
daiah (1972) suggest that the preference
of Gambusia for Ae. aegypti larvae could
be attributed to the larvae’s small size,
their vertical position in water, and their
tendency to clump in groups; these factors
facilitate their capture. Kar and Aditya
(2003) state that planaria prefer and con-
sume Anopheles larvae more than they do
Culex larvae. It is likely due to the behavior
of the prey and the predator, as the larval
posture of Anopheles larvae is parallel to the
water surface. This posture helps planaria
to attack the larvae more easily.
Additionally, Kar and Aditya (2003)
state that Culex larvae are more active
Guppies As predAtors of Mosquito LArvAe
Vol 45 No. 2 March 2014 305
and move faster than Anopheles larvae
and Culex 
attacked. This suggests a reason that both
sexes of guppy observed in this study

Cx. quinquefasciatus compared with the
other two species. Anyaele and Obembe

Anopheles compared with Culex. It is most
likely because Culex has the ability to es-
cape faster than Anopheles.
As reported by Culler and Lamp
(2009), the preference towards certain
type of prey is not only due to the ease to
capture they prey, but it also depends on
-
tor. For example, although ostracods are
easy to capture, they lack the nutritional
composition needed by predators for their
growth, and so predators do not prefer to
eat the ostracods (Culler and Lamp, 2009).
Anogwih and Makanjuola (2010) also
found that guppies prefer alternative prey,
that is, Chironomus larvae, which are the
most preferred prey, only then followed
by mosquito larvae and worm larvae.
Manna et al (2008) also indicated that
guppies prefer alternative preys such
 
preys are present, but nonetheless guppies
still consume mosquito larvae. Manna et al
(2008) also mentioned that guppies have a
wide range of dietary choices. Both stud-
ies, Anogwih and Makanjuola (2010) and
Manna et al (2008), showed that the guppy
prefers alternative prey than mosquito
larvae when both are present together;
however, in both experiment, it was ob-
served that the guppy also consumed the

Aphyosemion gularis prefers mosquito
larvae than non-mosquito macroinverte-
brates, such as chironomid larvae (Any-
aele and Obembe, 2011).
 

and Knight (2012), and these factors are
categorized into two, namely, ecological
factors and behavioral factors. The eco-
logical factors include suitable breeding
sites or habitat for predator and prey,
prey preference by predators, and devel-
opmental stage of both prey and predator.
The behavioral factors are, for example,
the feeding habits of their predator and
preference for alternative prey.
The effective way to use biocontrol
agents depends on the suitability of the
breeding site for predators to eradicate the
mosquito population and species prefer-
ence for mosquito larvae. For example, a
study in French Polynesia found that cov-
ered sites are preferred by Aedes spp and
are suitable for Mesocyclops aspericornis

light. Therefore, the most effective way
to control Aedes spp in covered sites is by
using M. aspericornis.
-
-
tation to its new environment (Lardeux,
1992). According to Kweka et al (2011),
besides habitat type, predator species

found that   is the most
effective predator than other predators

belostomatidae, and tadpoles in consum-
ing Anopheles gambiae larvae. Other factors
that influence predation activities are
number of predators, prey densities, water
volume, and respective sizes of predator
and prey (Aditya et al, 2007; Chandra et al,
2008), aquatic vegetation (Savino and
Stein, 1989; Shaalan et al, 2007), body size of
predator, behavior of predator, and mech-
anism of prey capture (Tranchida et al,
2009; Ohba and Takagi, 2010).
southeAst AsiAn J trop Med pubLic heALth
306 Vol 45 No. 2 March 2014
In this study, when two fish were
exposed to prey, the number of prey
consumed was more than when only one
-
quito larvae were consumed by these two

two male guppies were released in the
aquaria, but this was not observed when
two female guppies were released. It was
likely due to competition when the two

Anogwih and Makanjuola (2010) reported
low foraging behavior of guppies when a
-

to mosquito larvae, competition between

their foraging behavior.
In terms of feeding rate in this study,
female guppies had their feeding rate
increased when the prey densities were in-

of Anyaele and Obembe (2010). They re-
ported that larval consumption increased
when the densities of prey increase until
satiation level is reached, that is, when the

of Pseudomugil signifer Kner and Gambu-
sia holbrooki Girard consume more larvae
at the lowest densities compared to the
highest densities. However, both species
reached a level of satiation when they are
exposed to high densities of larvae and
late instars of mosquito larvae (Willems
et al, 2005).
-
tion activities and feeding rate. When 2
liters of water was used in the experiment,
the predation activities and feeding rate
decreased. Fish spent more time forag-
ing and searching for mosquito larvae.
The feeding rate decreased when water
volume of water was increased, and the
feeding rate increased when the number
of predators and the densities of preys
were increased (Chandra et al, 2008; Man-
dal et al, 2008). As discussed by Jacob et al
(1983), environmental factors such as tem-
 

but salinities do not affect the predation
activities. The predation activities increase
when the temperature is increased and
the feeding rate under lighting is higher
than in dark condition. In addition, Marti
et al (2006) suggested that different prey
attack strategies and handling time of

feeding rate.
ACKNOWLEDGEMENTS
We would like to thank the Institute
of Medical Research for supplying the
mosquito larvae that we used in the
experimentation, the Putrajaya Health

the Putrajaya areas, and the Institute of
Biological Science, University Malaya
   
This project was funded by IPPP grant
PS209/2009C and PV065/2011B.
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Muhamat, Hadisusanto S, Umniyati SR, Soesilohadi RCH. 2021. Dynamics of Toxorhynchites splendens population in the Larval phase at a rubber plantation in Banjarbaru, South Kalimantan, Indonesia. Biodiversitas 22: 4915-4922. This study aims to describe a water-filled rubber sap bowl as a habitat for larval Toxorhynchites splendens. The research used a quota drive count method, taking the first 10 rubber sap bowls found in the study area: (i) with larval Tx. splendens, (ii) with other mosquito larvae, (iii) with water but without mosquito larvae, and (iv) without water. The number of larval Tx. splendens was calculated based on the developmental phase and other mosquito larvae present in each bowl. Environmental factors, such as temperature and humidity, rainfall, wind velocity, and duration of irradiation were the additional data. The results of this study showed that the average frequency of On average, over 20% of bowls contained larval Tx. splendens, and the percentage increased in high rainfall. During low rainfall in August and September, Tx. splendens used water-filled rubber sap bowls as breeding places. This study concludes that Tx. splendens can make use of water-filled rubber sap bowls as places for breeding. Each rubber sap bowl contained one or more individuals of instar larvae 2, and the number decreased as the developmental phase continued because of the limited volume of water in the bowl, cannibalism, and the number of other mosquito larvae as prey.
... Despite this, Gambusia spp. together with other Poeciliid fishes (e.g., Poecilia reticulata) are still used as mosquito control agents in some parts of the world (Jayapriya & Shoba, 2014;Saleeza et al., 2014;Verma et al., 2016). From a conservation perspective it is, therefore, essential to identify regions where the-deliberate or accidental-introduction results in a high probability of establishment due to suitable (current and future) climatic conditions. ...
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