Bol. Inst. Pesca, São Paulo, 44(vol. esp.): 93 - 98, 2017
Doi: 10.20950/1678-2305.2017.93.98
EFFICIENCY OF BRAZILIAN NATIVE ORNAMENTAL FISHES AS MOSQUITO
LARVAE PREDATORS
Marcel Câmara MIRALDO
1
,
2
and Iracy Lea PECORA
1
ABSTRACT
Fish are an alternative in mosquito biological control. Some species are proven to be effective in
many countries, but are Brazilian native. Brazilian species may be larvivorous but this lacks
information. Therefore, the widely used exotic species, Poecilia reticulata and Betta splendens, were
compared with the Brazilian species Hyphessobrycon eques and Pterophyllum scalare for their
efficiency as Aedes aegypti mosquito larvae feeders. Fifty mosquito larvae were offered to the fishes
(n = 20) and after five minutes the remaining larvae were counted. Betta splendens ingested the
largest larvae amount but when this value was divided by fish weights, P. reticulata was the species
with the highest intake per gram. Brazilian native species did not differ from B. splendens in the
ingestion per weight rate. Thus, it is concluded that the most efficient larvivorous fish was P.
reticulata, but the Brazilian species showed a larvivorous potential, with fewer impacts on
biodiversity.
Keywords: Aedes aegypti; angelfish; jewel tetra; larvivorous fish; mosquito control
EFICIÊNCIA DE PEIXES NATIVOS BRASILEIROS COMO PREDADORES DE LARVAS DE
MOSQUITOS
RESUMO
Peixes são uma alternativa no controle biológico de mosquitos. Algumas espécies são
comprovadamente eficientes em muitos países, porém não são nativas brasileiras. Espécies
brasileiras podem ser larvófagas, porém carência de informações. Portanto, foram comparadas
as espécies exóticas geralmente utilizadas, Poecilia reticulata e Betta splendens, com as espécies
brasileiras, Hyphessobrycon eques e Pterophyllum scalare, por sua eficiência como predadoras de
larvas do mosquito Aedes aegypti. Foram oferecidas 50 larvas do mosquito para os peixes (n = 20) e,
após cinco minutos, as larvas restantes foram contabilizadas. Betta splendens ingeriu a maior
quantidade de larvas, mas quando esse valor foi dividido pelo peso dos peixes, P. reticulata foi a
espécie com maior ingestão por grama. As espécies nativas não diferiram de B. splendens na taxa de
ingestão por peso. Conclui-se que o peixe mais eficiente foi P. reticulata, mas as espécies brasileiras
apresentaram potencial como larvófagas, com menores impactos na biodiversidade.
Palavras-chave: Aedes aegypti; acará-bandeira; mato-grosso; peixes larvófagos; controle de
mosquitos
Scientific Note/Nota Científica: Recebida em 11/11/2016 Aprovada em 10/03/2017
1
São Paulo State University, Biosciences Institute, Coastal Campus of São Vicente. São Vicente SP Brazil;
2
Sustainable Aquaculture Laboratory. Praça Infante Dom Henrique s/n - Parque Bitaru - CEP: 11330-900 São Vicente
SP Brazil. e-mail: mcmiraldo@gmail.com (corresponding author)
94 MIRALDO and PECORA
Bol. Inst. Pesca, São Paulo, 44(vol. esp.): 93 - 98, 2017
INTRODUCTION
An efficient and responsible method to
control Aedes aegypti is needed. The mosquito
transmits zika, chikungunya and dengue, and its
distribution is alarmingly increasing throughout
the urbanized areas in the world (BHATT et al.,
2013; MESSINA et al., 2015; AI et al., 2016;
NDEFFO-MBAH et al., 2016). This is happening
as a consequence of the increase of suitable places
for laying their eggs (BENTLEY and DAY, 1989),
its rapid growth and higher population densities
(EISENSTEIN, 2016). The chemical control,
despite being efficient (VAN DEN BERG et al.,
2012), is a weapon against the environment,
because it pollutes the air and the water while
suppressing non-target species and causing
diseases in humans (HEMINGWAY and
RANSON, 2000). This requires the search for
alternative and efficient control means which has
fewer impacts on the environment.
Biological control by fishes is not a new
proposal, however it was forgotten during time
even though its efficiency has been proven in
other opportunities in several places (WU et al.,
1987; FLETCHER et al., 1993; NAM et al., 2000;
LARDEUX et al., 2002; MARTÍNEZ-IBARRA et al.,
2002). For the success of the mosquito control, the
fishes used must be larvivorous, which are
defined as small fish capable to easily move
between thick weeds to reach the suitable places
where mosquitoes lay their eggs (JOB, 1940).
Other characteristics are defined, such as
toleration to rough handling and transportation,
short and prolific life cycle, surface carnivorous
feeding habits with preference for mosquito
larvae and non-impactant for the local fish
community (CHANDRA et al., 2008).
Some ornamental fish species are used as
larvivorous species (CHAPMAN, 1974; KUMAR
and HWANG, 2006; CHANDRA et al., 2008).
Despite their efficiency, in Brazil they are not
native species, and this is considered a misguided
strategy because it negatively affects native
populations (AZEVEDO-SANTOS et al., 2016).
Thus, the main objective was to evaluate the
efficiency of Brazilian native ornamental fishes as
predators of A. aegypti larvae, comparing with two
of the most used species for mosquito control.
MATERIAL AND METHODS
Animals and stock conditions
The species tested were guppy (Poecilia
reticulata), betta (Betta splendens), jewel tetra
(Hyphessobrycon eques) and angelfish (Pterophyllum
scalare). All the species, except for the guppies,
were obtained in a commercial establishment. In
pilot surveys conducted in a coastal city of the
State of São Paulo, in Brazil, was verified that the
wild guppies had a larger size than the fish bred
in captivity, which is why the wild animals were
chosen for this study. They were collected in a
water channel of São Vicente, São Paulo, Brazil,
using baited traps to avoid physical injury to
the animals. The A. aegypti larvae were achieved
through partnership with the São Vicente
Regional Service of the Endemies Control
Superintendence (SUCEN SR-2). The larvae were
born in laboratory conditions from an A. aegypti
population with no contact with the natural
environment. The adults laid their eggs in traps
placed inside the cages, and these eggs were
hatched until the larvae reached the IV instar.
The animals were stocked in three 45 L tanks
(one for each species) with controlled temperature
(25.0 ± 1.0 ºC), pH (6.8 ± 0.3) and dissolved oxygen
(>5.00 mg L
-1
) and fed ad libitum with commercial
feed. The bettas, due to their aggressiveness with
conspecifics (JOHNSON and JOHNSON, 1973),
were stocked in individual 6 L aquaria under the
same conditions as the others. All animals
remained at least two weeks in stock conditions
prior to the tests to exclude effects of capture or
transport. The larvae were collected and
immediately used in tests.
This study was approved by the UNESP
IB/CLP Animal Use Ethics Committee (CEUA-
UNESP/CLP) under the protocol number
24/2016.
Experimental design and procedures
Were used 20 fish of each species, randomly
chosen from the stock populations, weighed
them and placed individually in 6 L aquaria
without visual contact with the outside, totaling
20 samples per species. The temperature was
maintained constant at 25.0 ± 1.0 °C. The
acclimation period occurred during 24 hours in
which individuals were not fed, so that when
Efficiency of Brazilian native ornamental fishes as mosquito 95
Bol. Inst. Pesca, São Paulo, 44(vol. esp.): 93 - 98, 2017
testing started, the animals were in fasting
conditions.
The test consisted in offering the animals, at
once, 50 stage IV larvae of A. aegypti and, five
minutes later, the fish were removed from the
aquaria and all the remaining larvae were
accounted. This period was chosen based on a
pilot experiment in which the predation occurred
mostly during the first five minutes after the food
presentation.
Statistical analysis
After testing normality with Shapiro-Wilk test
and homoscedasticity with Levene’s test and
having both confirmed, the amount of ingested
larvae by each fish species was compared using
analysis of variance (ANOVA), followed by
Tukey’s HSD, as well as the number of ingested
larvae per gram of fish. Statistical differences
were set at p<0.05.
RESULTS AND DISCUSSION
Siamese fighting fish ate more larvae (29.50 ±
11.24; number of larvae ± standard deviation)
than all other species (Figure 1; p<0.05). Angelfish
ingested 13.84 ± 13.02 larvae; guppies ate 5.78 ±
4.63 larvae and jewel tetras consumed 2.39 ± 3.18
larvae.
Figure 1. Number of Aedes aegypti larvae ingested
by Brazilian native (jewel tetra Hyphessobrycon
eques and angelfish Pterophyllum scalare) and
non-native (Guppy Poecilia reticulata and Betta
Betta splendens) ornamental fish species. Different
letters indicate statistical differences between
species (p<0.05).
However, when the values are considered
proportionally to the fish weights, the most
efficient species in larvae ingestion was the guppy
(Figure 2; p<0.05), ingesting 2.05 ± 1.10 larvae per
gram. The other species did not show statistical
differences; betta ingested 1.94 ± 0.53 larvae per
gram; angelfish, 1.25 ± 0.86; and jewel tetra, 0.85 ±
0.95 larvae per gram.
Figure 2. Amount of Aedes aegypti larvae ingested
by the weights of Brazilian native (jewel tetra
Hyphessobrycon eques and angelfish Pterophyllum
scalare) and non-native (Guppy Poecilia reticulata
and Betta Betta splendens) ornamental fish species
(N g
-1
). Different letters indicate statistical differences
(p<0.05).
The Brazilian native ornamental fish species
are suited to be used in mosquito control programs.
Both H. eques and P. scalare were efficient, and
their use would not cause great damages to local
fish populations. Even though they do not
consume the highest amounts (Figure 1), the
proportions of larvae ingested by their weights
are similar of B. splendens (Figure 2). In this case,
the native species have an advantage over the
Siamese fighting fish, because they group in
shoals (CARVALHO and DEL-CLARO, 2004;
MEZ-LAPLAZA and GERLAI, 2011) while
B. splendens tends to be aggressive with other
fishes (BRADDOCK and BRADDOCK, 1955;
JOHNSON and JOHNSON, 1973). Consequently,
a large group can eat a higher amount of larvae
compared with a single individual.
The species with the greatest efficiency to
capture mosquito larvae is P. reticulata because it
showed the highest larvae ingestion relatively to
96 MIRALDO and PECORA
Bol. Inst. Pesca, São Paulo, 44(vol. esp.): 93 - 98, 2017
the body weight and also groups in shoals
(SEGHERS, 1974). The guppy is less effective than
the most widely used species for mosquito
control, Gambusia affinis (CHANDRA et al., 2008;
SARWAR, 2015), but the latter does not breed
well in tropical environments (SARWAR, 2015).
Nevertheless, individual guppies are able to
consume up to 102 larvae per day, and females
are more efficient than males (SENG et al., 2008).
The use of non-native species to control another
invasive species such as A. aegypti is not
recommended by the World Health Organization
(WORLD HEALTH ORGANIZATION, 2003). This
is considered to be a threat to native biodiversity
by reducing or negatively affecting local
populations (AZEVEDO-SANTOS et al., 2016),
even when they are efficient mosquito larvae
predators (EL-SABAAWI et al., 2016). In some
places native fishes are already proven to be more
effective than introduced species , as in Australia
(RUSSELL et al., 2001; LAWRENCE et al., 2016),
India (RAO et al., 2015), Iran (SHAHI et al., 2015)
and Mexico (MARTÍNEZ-IBARRA et al., 2002).
Therefore, although the use of non-native
fishes in mosquito control programs in Brazil is
succeeded (LIMA et al., 2010), the use of jewel
tetra and angelfish as mosquito larvae controllers
should and must be encouraged, since they can be
effective mosquito larvae predators and are
Brazilian native species. Another alternative to
reduce the number of introduced fishes into the
environment is the integrated use of different
methods along with the fishes (ARAÚJO et al.,
2015; SARWAR, 2015; CAIXETA et al., 2016). Some
chemicals already used for controlling A. aegypti
in low and environmentally safe concentrations
tend to reduce the mosquito infestation, such as
pyriproxyfen (CAIXETA et al., 2016) and spinosad
(PEREIRA et al., 2016). Moreover, reduced doses
of silver nanoparticles synthesized with Sonneratia
alba extracts can boost the larvae predation by P.
reticulata (MURUGAN et al., 2017). Future studies
are needed to assess the Brazilian native species
sensitivity to chemical larvicides and support
their use in integrated programs.
ACKNOWLEDGEMENTS
Authors thank Lumi Peixes and SUCEN for
the fish and larvae used in this work. Also Dr.
Alessandra Pereira Majer for statistical advising.
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