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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Larvicidal activity of <italic>Syzygium aromaticum</italic>
(L.) Merr and
<italic>Citrus sinensis</italic>
(L.) Osbeck essential oils and their antagonistic
effects with temephos in resistant populations of <italic>Aedes aegypti</italic>
</title>
<author><name sortKey="Araujo, Adriana Faraco De Oliveira" sort="Araujo, Adriana Faraco De Oliveira" uniqKey="Araujo A" first="Adriana Faraco De Oliveira" last="Araujo">Adriana Faraco De Oliveira Araujo</name>
<affiliation><nlm:aff id="aff1">Universidade Estadual Paulista, Faculdade de Ciências e Letras, Departamento de Ciências Biológicas, Assis, SP, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Ribeiro Paes, Joao Tadeu" sort="Ribeiro Paes, Joao Tadeu" uniqKey="Ribeiro Paes J" first="João Tadeu" last="Ribeiro-Paes">João Tadeu Ribeiro-Paes</name>
<affiliation><nlm:aff id="aff1">Universidade Estadual Paulista, Faculdade de Ciências e Letras, Departamento de Ciências Biológicas, Assis, SP, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="De Deus, Juliana Telles" sort="De Deus, Juliana Telles" uniqKey="De Deus J" first="Juliana Telles" last="De Deus">Juliana Telles De Deus</name>
<affiliation><nlm:aff id="aff2">Superintendência de Controle de Endemias, Marília, SP, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cavalcanti, S Crates Cabral De Holanda" sort="Cavalcanti, S Crates Cabral De Holanda" uniqKey="Cavalcanti S" first="S Crates Cabral De Holanda" last="Cavalcanti">S Crates Cabral De Holanda Cavalcanti</name>
<affiliation><nlm:aff id="aff3">Universidade Federal de Sergipe, Departamento de Farmácia, São Cristóvão, SE, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Nunes, Rogeria De Souza" sort="Nunes, Rogeria De Souza" uniqKey="Nunes R" first="Rogéria De Souza" last="Nunes">Rogéria De Souza Nunes</name>
<affiliation><nlm:aff id="aff3">Universidade Federal de Sergipe, Departamento de Farmácia, São Cristóvão, SE, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Alves, Pericles Barreto" sort="Alves, Pericles Barreto" uniqKey="Alves P" first="Péricles Barreto" last="Alves">Péricles Barreto Alves</name>
<affiliation><nlm:aff id="aff4">Universidade Federal de Sergipe, Departamento de Química, São Cristóvão, SE, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Macoris, Maria De Lourdes Da Graca" sort="Macoris, Maria De Lourdes Da Graca" uniqKey="Macoris M" first="Maria De Lourdes Da Graça" last="Macoris">Maria De Lourdes Da Graça Macoris</name>
<affiliation><nlm:aff id="aff2">Superintendência de Controle de Endemias, Marília, SP, Brasil</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">27384083</idno>
<idno type="pmc">4957496</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4957496</idno>
<idno type="RBID">PMC:4957496</idno>
<idno type="doi">10.1590/0074-02760160075</idno>
<date when="2016">2016</date>
<idno type="wicri:Area/Pmc/Corpus">000359</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Larvicidal activity of <italic>Syzygium aromaticum</italic>
(L.) Merr and
<italic>Citrus sinensis</italic>
(L.) Osbeck essential oils and their antagonistic
effects with temephos in resistant populations of <italic>Aedes aegypti</italic>
</title>
<author><name sortKey="Araujo, Adriana Faraco De Oliveira" sort="Araujo, Adriana Faraco De Oliveira" uniqKey="Araujo A" first="Adriana Faraco De Oliveira" last="Araujo">Adriana Faraco De Oliveira Araujo</name>
<affiliation><nlm:aff id="aff1">Universidade Estadual Paulista, Faculdade de Ciências e Letras, Departamento de Ciências Biológicas, Assis, SP, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Ribeiro Paes, Joao Tadeu" sort="Ribeiro Paes, Joao Tadeu" uniqKey="Ribeiro Paes J" first="João Tadeu" last="Ribeiro-Paes">João Tadeu Ribeiro-Paes</name>
<affiliation><nlm:aff id="aff1">Universidade Estadual Paulista, Faculdade de Ciências e Letras, Departamento de Ciências Biológicas, Assis, SP, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="De Deus, Juliana Telles" sort="De Deus, Juliana Telles" uniqKey="De Deus J" first="Juliana Telles" last="De Deus">Juliana Telles De Deus</name>
<affiliation><nlm:aff id="aff2">Superintendência de Controle de Endemias, Marília, SP, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cavalcanti, S Crates Cabral De Holanda" sort="Cavalcanti, S Crates Cabral De Holanda" uniqKey="Cavalcanti S" first="S Crates Cabral De Holanda" last="Cavalcanti">S Crates Cabral De Holanda Cavalcanti</name>
<affiliation><nlm:aff id="aff3">Universidade Federal de Sergipe, Departamento de Farmácia, São Cristóvão, SE, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Nunes, Rogeria De Souza" sort="Nunes, Rogeria De Souza" uniqKey="Nunes R" first="Rogéria De Souza" last="Nunes">Rogéria De Souza Nunes</name>
<affiliation><nlm:aff id="aff3">Universidade Federal de Sergipe, Departamento de Farmácia, São Cristóvão, SE, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Alves, Pericles Barreto" sort="Alves, Pericles Barreto" uniqKey="Alves P" first="Péricles Barreto" last="Alves">Péricles Barreto Alves</name>
<affiliation><nlm:aff id="aff4">Universidade Federal de Sergipe, Departamento de Química, São Cristóvão, SE, Brasil</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Macoris, Maria De Lourdes Da Graca" sort="Macoris, Maria De Lourdes Da Graca" uniqKey="Macoris M" first="Maria De Lourdes Da Graça" last="Macoris">Maria De Lourdes Da Graça Macoris</name>
<affiliation><nlm:aff id="aff2">Superintendência de Controle de Endemias, Marília, SP, Brasil</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Memórias do Instituto Oswaldo Cruz</title>
<idno type="ISSN">0074-0276</idno>
<idno type="eISSN">1678-8060</idno>
<imprint><date when="2016">2016</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Environmentally friendly botanical larvicides are commonly considered as an
alternative to synthetic larvicides against <italic>Aedes aegypti</italic>
Linn. In
addition, mosquito resistance to currently used larvicides has motivated research to
find new compounds acting via different mechanisms of action, with the goal of
controlling the spread of mosquitos. Essential oils have been widely studied for this
purpose. This work aims to evaluate the larvicidal potential of <italic>Syzygium
aromaticum</italic>
and <italic>Citrus sinensis</italic>
essential oils, either
alone or in combination with temephos, on <italic>Ae. aegypti</italic>
populations
having different levels of organophosphate resistance. The 50% lethal concentration
(LC50) of the essential oils alone and in combination with temephos and the influence
of essential oils on vector oviposition were evaluated. The results revealed that
essential oils exhibited similar larvicidal activity in resistant populations and
susceptible populations. However, <italic>S. aromaticum</italic>
and <italic>C.
sinensis</italic>
essential oils in combination with temephos did not decrease
resistance profiles. The presence of the evaluated essential oils in oviposition
sites significantly decreased the number of eggs compared to sites with tap water.
Therefore, the evaluated essential oils are suitable for use in mosquito resistance
management, whereas their combinations with temephos are not recommended.
Additionally, repellency should be considered during formulation development to avoid
mosquito deterrence.</p>
</div>
</front>
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</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Mem Inst Oswaldo Cruz</journal-id>
<journal-id journal-id-type="iso-abbrev">Mem. Inst. Oswaldo Cruz</journal-id>
<journal-id journal-id-type="publisher-id">mioc</journal-id>
<journal-title-group><journal-title>Memórias do Instituto Oswaldo Cruz</journal-title>
</journal-title-group>
<issn pub-type="ppub">0074-0276</issn>
<issn pub-type="epub">1678-8060</issn>
<publisher><publisher-name>Instituto Oswaldo Cruz, Ministério da Saúde</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27384083</article-id>
<article-id pub-id-type="pmc">4957496</article-id>
<article-id pub-id-type="publisher-id" specific-use="previous-pid">S0074-02762016005001405</article-id>
<article-id pub-id-type="doi">10.1590/0074-02760160075</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Larvicidal activity of <italic>Syzygium aromaticum</italic>
(L.) Merr and
<italic>Citrus sinensis</italic>
(L.) Osbeck essential oils and their antagonistic
effects with temephos in resistant populations of <italic>Aedes aegypti</italic>
</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Araujo</surname>
<given-names>Adriana Faraco de Oliveira</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="c01"><sup>+</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ribeiro-Paes</surname>
<given-names>João Tadeu</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>de Deus</surname>
<given-names>Juliana Telles</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cavalcanti</surname>
<given-names>Sócrates Cabral de Holanda</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nunes</surname>
<given-names>Rogéria de Souza</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Alves</surname>
<given-names>Péricles Barreto</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Macoris</surname>
<given-names>Maria de Lourdes da Graça</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
Universidade Estadual Paulista, Faculdade de Ciências e Letras, Departamento de Ciências Biológicas, Assis, SP, Brasil</aff>
<aff id="aff2"><label>2</label>
Superintendência de Controle de Endemias, Marília, SP, Brasil</aff>
<aff id="aff3"><label>3</label>
Universidade Federal de Sergipe, Departamento de Farmácia, São Cristóvão, SE, Brasil</aff>
<aff id="aff4"><label>4</label>
Universidade Federal de Sergipe, Departamento de Química, São Cristóvão, SE, Brasil</aff>
<author-notes><corresp id="c01"><label>+</label>
Corresponding author: <email>adrifaracofb@yahoo.com.br</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>04</day>
<month>7</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="ppub"><month>7</month>
<year>2016</year>
</pub-date>
<volume>111</volume>
<issue>7</issue>
<fpage>443</fpage>
<lpage>449</lpage>
<history><date date-type="received"><day>26</day>
<month>2</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>24</day>
<month>5</month>
<year>2016</year>
</date>
</history>
<permissions><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p> This is an Open Access article distributed under the terms of the
Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is
properly cited. </license-p>
</license>
</permissions>
<abstract><p>Environmentally friendly botanical larvicides are commonly considered as an
alternative to synthetic larvicides against <italic>Aedes aegypti</italic>
Linn. In
addition, mosquito resistance to currently used larvicides has motivated research to
find new compounds acting via different mechanisms of action, with the goal of
controlling the spread of mosquitos. Essential oils have been widely studied for this
purpose. This work aims to evaluate the larvicidal potential of <italic>Syzygium
aromaticum</italic>
and <italic>Citrus sinensis</italic>
essential oils, either
alone or in combination with temephos, on <italic>Ae. aegypti</italic>
populations
having different levels of organophosphate resistance. The 50% lethal concentration
(LC50) of the essential oils alone and in combination with temephos and the influence
of essential oils on vector oviposition were evaluated. The results revealed that
essential oils exhibited similar larvicidal activity in resistant populations and
susceptible populations. However, <italic>S. aromaticum</italic>
and <italic>C.
sinensis</italic>
essential oils in combination with temephos did not decrease
resistance profiles. The presence of the evaluated essential oils in oviposition
sites significantly decreased the number of eggs compared to sites with tap water.
Therefore, the evaluated essential oils are suitable for use in mosquito resistance
management, whereas their combinations with temephos are not recommended.
Additionally, repellency should be considered during formulation development to avoid
mosquito deterrence.</p>
</abstract>
<kwd-group><kwd>Syzygium aromaticum</kwd>
<kwd>Citrus sinensis</kwd>
<kwd>Aedes aegypti</kwd>
<kwd>vector control</kwd>
<kwd>larvicide</kwd>
<kwd>dengue</kwd>
</kwd-group>
<counts><fig-count count="2"></fig-count>
<table-count count="5"></table-count>
<equation-count count="2"></equation-count>
<ref-count count="29"></ref-count>
<page-count count="7"></page-count>
</counts>
</article-meta>
</front>
<body><p>Dengue is currently considered to be one of the most important arboviroses, accounting for
substantial morbidity and mortality worldwide. This virus represents a serious public
threat, especially in tropical countries, where the warm temperature and environmental
conditions favour the development and proliferation of its disease vector, <italic>Aedes
aegypti</italic>
Linn. (<xref rid="B26" ref-type="bibr">Sharp et al. 2014</xref>
).
Furthermore, there is currently no vaccine available that acts against the different virus
serotypes. As a result, prevention efforts are restricted to focusing exclusively on
mosquito control, and the interventions available for prevention and control actions in
combatting the vector are therefore limited (<xref rid="B3" ref-type="bibr">Bisset et al.
2011</xref>
, <xref rid="B9" ref-type="bibr">Coelho 2012</xref>
). Control strategies
frequently focus on the use of chemical larvicides and insecticides, which are mainly
organophosphates, such as temephos, and pyrethroids. Such control actions are integrated
with environmental management. However, the frequent use of such products has selected for
mosquito populations that are resistant to these chemicals (<xref rid="B25" ref-type="bibr">Pocquet et al. 2014</xref>
). In addition, the environmental impacts of pesticides have
been widely studied, as they are responsible for non-target toxicity and water stream
contamination (<xref rid="B21" ref-type="bibr">Muhammetoglu et al. 2010</xref>
).</p>
<p>Resistance is commonly related to the activity of enzymes present in the mosquito
biochemical routes of insecticide metabolism. Resistance data from São Paulo state reports
that the major pathway for the detoxification of temephos, the larvicide that has been
widely used in Brazil for over 30 years, is performed by esterases (<xref rid="B19" ref-type="bibr">Melo-Santos et al. 2010</xref>
). Given the characteristics of <italic>Ae.
aegypti</italic>
populations that are resistant to temephos and other larvicides, the
demand for alternative plant-based products with a different mode of action than that which
conferred organophosphate resistance is necessary.</p>
<p>In recent years, numerous investigations have been conducted in the search for active
compounds from natural sources, with an emphasis on medicinal and aromatic plant essential
oils. These oils are widely known for their larvicidal properties, as well as antiviral,
fungicidal, antiparasitic and cosmetic properties (<xref rid="B24" ref-type="bibr">Palazzolo et al. 2013</xref>
, <xref rid="B20" ref-type="bibr">Mittal et al.
2014</xref>
). The vast Brazilian biodiversity and the insecticidal potential of several
unexplored species may provide alternative novel chemical agents to control culicids,
especially <italic>Ae. aegypti</italic>
(<xref rid="B5" ref-type="bibr">Brandão et al.
2013</xref>
, <xref rid="B23" ref-type="bibr">Novaes et al. 2013</xref>
). The use of
plants-based chemicals as an alternative for vector control is based on their usually low
toxicity to animals and aquatic ecosystems, in addition to their biodegradability and
environmental safety. In contrast, synthetic insecticides, which can cause resistance, are
toxic and pollutants (<xref rid="B10" ref-type="bibr">Corrêa & Salgado
2011</xref>
).</p>
<p>Several studies have demonstrated the activity of <italic>Syzygium aromaticum</italic>
(L.)
Merr. & Perry and <italic>Citrus sinensis</italic>
(L.) Osbeck essential oils, as well
as their major components, against <italic>Ae. aegypti</italic>
larvae (<xref rid="B7" ref-type="bibr">Cavalcanti et al. 2004</xref>
, <xref rid="B11" ref-type="bibr">Costa et al. 2005</xref>
, <xref rid="B2" ref-type="bibr">Barbosa et al. 2012</xref>
,
<xref rid="B22" ref-type="bibr">Murugan et al. 2012</xref>
, <xref rid="B28" ref-type="bibr">Warikoo et al. 2012</xref>
, <xref rid="B12" ref-type="bibr">Fayemiwo et al.
2014)</xref>
. In this context, we aimed to further evaluate the larvicidal activity of
<italic>S. aromaticum</italic>
and <italic>C. sinensis</italic>
essential oils on
insecticide-resistant <italic>Ae. aegypti</italic>
populations, as well as to assess the
combined effects of these essential oils and temephos. Furthermore, the oviposition
behaviour of females in the presence of these larvicidal agents was evaluated because
repellence is detrimental to larvicidal action.</p>
<sec sec-type="materials|methods"><title>MATERIALS AND METHODS</title>
<p><italic>Chemicals and essential oil extraction</italic>
- Temephos (97.5%) and Tween 80
were purchased from Sigma-Aldrich Chemical Co. (St. Louis, MO, USA). Sodium sulphate was
purchased from Synth (Brazil). The <italic>C. sinensis</italic>
fruits and dry clove
buds (Maratá<sup>TM</sup>
, Itaporanga D’Ajuda, SE, Brazil) used in this study were
acquired from a local market in Aracaju city, Sergipe state, Brazil, in a single lot.
<italic>C. sinensis</italic>
peels were dried in a circulating air oven at 40ºC for
three days. The dry materials were separately ground and submitted to hydrodistillation
for 3 h in a Clevenger-type apparatus to yield yellowish oils. The essential oils
obtained were separated from the aqueous phase, followed by the addition of sodium
sulphate (Na<sub>2</sub>
SO<sub>4</sub>
) to remove water residue, and were then filtered
and kept in a freezer until further analysis and activity evaluation.</p>
<p><italic>Analytical conditions</italic>
- The essential oils obtained by
hydrodistillation were analysed by gas chromatography-mass spectrometry (GC-MS) using a
Shimadzu QP5050A (Shimadzu Europe, North Rhine-Westphalia, Germany) gas chromatograph
equipped with a DB-5 MS fused silica column (30 m x 0.25 mm; film thickness 0.25 μm),
under the following conditions: helium as the carrier gas at 1.0 mL/min; injector split
at 250ºC (split ratio 1/20); detector at 280ºC; column temperature programme of 80ºC for
1.5 min, increase of 4ºC per min to 180ºC, then 10ºC per min to 300ºC, ending with a 10
min isothermal at 300ºC. The mass spectra were taken at 70 eV with a scanning speed of
0.85 scan/s from 40 to 550 Da. Peak identification was made on the basis of comparison
of their retention indices relative to an <italic>n</italic>
-alkane homologous series
obtained by co-injecting the oil sample with a linear hydrocarbon mixture.</p>
<p>Quantitative analysis of the chemical constituents was performed by flame ionization gas
chromatography (FID) using a Shimadzu GC-17A (Shimadzu Corporation, Kyoto, Japan)
instrument under the following operational conditions: a capillary ZB-5MS column (5%
phenyl-arylene-95%-dimethylpolysiloxane) fused silica capillary column (30 m x 0.25 mm
i.d. x 0.25 μm film thickness) from Phenomenex (Torrance, CA, USA), under the same
conditions reported for the GC-MS. Quantification of each constituent was estimated by
area normalisation (%). The compound concentrations were calculated from the GC peak
areas and arranged in the order of GC elution.</p>
<p><italic>Stock solutions</italic>
- Mixtures of <italic>C. sinensis</italic>
or
<italic>S. aromaticum</italic>
essential oils and temephos at ratios of 54:1 and
100:1, respectively, were prepared based on previous LC<sub>50</sub>
data for both
essential oils and temephos separately. Thus, a 1 L solution containing 55 mg of
<italic>C. sinensis</italic>
/temephos or 101 mg of <italic>S.
aromaticum/</italic>
temephos would contain a concentration approximately equivalent to
the LC<sub>50</sub>
of the essential oil and 1 ppm of temephos.</p>
<p>A 20,000 ppm stock solution was prepared using each essential oil or its mixture with
temephos (20 mg/mL), Tween 80 (5 mL), and deionized water (1 mL). The stock solution was
used to make 150 mL water solutions ranging from 0.1 to 220 ppm. Temephos was also
separately used to monitor <italic>Ae. aegypti</italic>
susceptibility.</p>
<p><italic>Mosquitoes</italic>
- The Rockefeller strain of <italic>Ae. aegypti</italic>
was
maintained under laboratory conditions at a controlled temperature of 25ºC ± 2ºC and a
relative humidity of 70 ± 10%. Insecticide-resistant populations were collected from the
following counties: Marília, Araçatuba and Santos, São Paulo state, Brazil. Resistant
populations were maintained under the same conditions as the Rockefeller strain but in
separate rooms. Populations were selected based on previously evaluate levels of
insecticide-detoxificant enzymes (α- and β-esterases and glutathione-S-transferase).
Additionally, the levels of multi-function oxidase enzyme activity in the Marília
population were considered normal, while the Araçatuba and Santos populations presented
altered activity (<xref rid="B16" ref-type="bibr">Macoris et al. 2003</xref>
).</p>
<p><italic>Larvicidal assay</italic>
- Assays were conducted at the Applied Entomology
Laboratory (SUCEN, Marília, São Paulo, Brazil) under a controlled environment and were
performed according to the procedure recommended by the World Health Organization (<xref rid="B29" ref-type="bibr">WHO 2005</xref>
). Concentration ranges were determined
using a previously generated concentration-response curve for 20 third-instar larvae.
Eight different concentrations and four replicates were used for each essential oil
mixture and the control. Twenty late third-instar larvae were exposed to 150 mL
solutions of larvicide in disposable cups. A mortality count was conducted 24 h after
treatment. Each experiment was repeated three times in different days, in such a way
that 240 larvae were exposed to each larvicide concentration or controls. The controls
were prepared with Tween 80 and water at the highest concentration used in each
experiment. The organophosphate temephos, a standard insecticide for larvae control, was
used as a positive control. In all cases where mortality of between 5-20% occurred in
the control experiment, the data were corrected using Abbott’s formula (% deaths =
[1-(test/control)] x 100) (<xref rid="B1" ref-type="bibr">Abbott 1925</xref>
). Any
experiment with over 20% mortality in controls was discarded.</p>
<p><italic>Oviposition behaviour</italic>
- To evaluate whether the presence of essential
oils in oviposition sites influence the oviposition behaviour of females, two rearing
cages, one for each essential oil, were set with field-collected (Marília, São Paulo,
Brazil), newly emerged <italic>Ae. aegypti</italic>
(100 females and 50 males). The
mosquitoes were fed with 10% honey in cotton pads. After a three-day long copulation
period, the cotton pads were removed. On the fourth day, blood was offered via an
artificial membrane blood-feeding apparatus. Honey and blood feeding were then offered
every other day until the end of the experiment, which extended for 33 days.</p>
<p>Three days after blood feeding, two sites for oviposition were placed in each rearing
cage to monitor possible oviposition preferences. One site consisted of a disposable cup
containing tap water, and a second cup contained essential oil. The cups were lined with
filter paper as a substrate for oviposition and were covered with black cups to control
the availability of light. The essential oil concentrations of <italic>C.
sinensis</italic>
and <italic>S. aromaticum</italic>
were 81.44 and 860 ppm,
respectively, approximately four times the LC<sub>99</sub>
for the Rockefeller strain,
an arbitrary criterion for the use of larvicides in the field (<xref rid="B29" ref-type="bibr">WHO 2005</xref>
).</p>
<p>Blood feeding was offered three times a week (Mondays, Wednesdays and Fridays). At these
times, the paper filters were removed and allowed to dry, and the larvicidal solutions
were replaced. To prevent possible effects of local brightness, which can interfere with
the choice of oviposition site, the cups were also repositioned during this procedure.
After 24 h, the number of eggs was quantified.</p>
<p><italic>Statistical analysis</italic>
- Probit analysis was conducted on the mortality
data collected after 24 h of exposure to different concentrations of the testing
solutions to establish lethal concentrations (LC<sub>50</sub>
, LC<sub>95</sub>
, and
LC<sub>99</sub>
) and 95% confidence intervals (CI) for the respective essential oils
or mixtures using the Polo-PC software suite (<xref rid="B14" ref-type="bibr">LeOra
Software 1987</xref>
). The activity of the essential oils or mixtures were considered
to be significantly different when their 95% CIs failed to overlap. The lethal
concentrations were used to calculate the resistance ratio (RR) using Equation 1.</p>
<disp-formula id="e1"><graphic xlink:href="0074-0276-mioc-0074-02760160075-e1.jpg" position="float" orientation="portrait"></graphic>
</disp-formula>
<p>The concentration-response graphics were created using Graph Pad Prism software version
6.0.</p>
<p>The oviposition index (OI, Equation 2) was used to evaluate the oviposition response of
females to different sites of oviposition (<xref rid="B17" ref-type="bibr">Marques et
al. 2013</xref>
). The OI varies between -1 and +1. Substances attracting or
stimulating egg deposition result in a positive OI, while substances repelling or
inhibiting egg deposition result in a negative OI.</p>
<disp-formula id="e2"><graphic xlink:href="0074-0276-mioc-0074-02760160075-e2.jpg" position="float" orientation="portrait"></graphic>
</disp-formula>
<p>Where OI is the oviposition index, Nt is the average number of eggs in the test solution
and Nc is the average number of eggs in the control solution.</p>
<p>Student’s t-test was used to compare the number of oviposited eggs in each oviposition
site. Graphs showing the total number of eggs in each oviposition site and the total
number of eggs over the course of the experiment were created using Graph Pad Prism
software version 6.0.</p>
</sec>
<sec><title>RESULTS AND DISCUSSION</title>
<p>The essential oils of <italic>C. sinensis</italic>
and <italic>S. aromaticum</italic>
were obtained at 9.1-19.0% yield, respectively. Four compounds were identified in the
essential oil of <italic>C. sinensis</italic>
, representing 99% of the essential oil,
while five compounds were identified in the essential oil of <italic>S.
aromaticum</italic>
, representing 100% of the essential oil. Their retention indices
and composition percentages, listed in the order of elution in the ZB-5MS column, are
given in <xref ref-type="table" rid="t1">Table I</xref>
.</p>
<p><table-wrap id="t1" orientation="portrait" position="float"><label>TABLE I</label>
<caption><title>Essential oil compositions of <italic>Citrus sinensis</italic>
and
<italic>Syzygium aromaticum</italic>
</title>
</caption>
<table frame="hsides" rules="groups"><colgroup width="25%" span="1"><col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
</colgroup>
<thead><tr><th align="left" style="font-weight:normal" rowspan="1" colspan="1">RI</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Compound</th>
<th style="font-weight:normal" rowspan="1" colspan="1"><italic>C. sinensis</italic>
(% FID)</th>
<th style="font-weight:normal" rowspan="1" colspan="1"><italic>S. aromaticum</italic>
(% FID)</th>
</tr>
</thead>
<tbody><tr><td rowspan="1" colspan="1">998</td>
<td align="center" rowspan="1" colspan="1">Mircene</td>
<td align="center" rowspan="1" colspan="1">1.27</td>
<td align="center" rowspan="1" colspan="1">-</td>
</tr>
<tr><td rowspan="1" colspan="1">1003</td>
<td align="center" rowspan="1" colspan="1"><italic>n</italic>
-Octanol</td>
<td align="center" rowspan="1" colspan="1">1.09</td>
<td align="center" rowspan="1" colspan="1">-</td>
</tr>
<tr><td rowspan="1" colspan="1">1028</td>
<td align="center" rowspan="1" colspan="1">Limonene</td>
<td align="center" rowspan="1" colspan="1">91.88</td>
<td align="center" rowspan="1" colspan="1">-</td>
</tr>
<tr><td rowspan="1" colspan="1">1099</td>
<td align="center" rowspan="1" colspan="1">Linalool</td>
<td align="center" rowspan="1" colspan="1">4.76</td>
<td align="center" rowspan="1" colspan="1">-</td>
</tr>
<tr><td rowspan="1" colspan="1">1354</td>
<td align="center" rowspan="1" colspan="1">Eugenol</td>
<td align="center" rowspan="1" colspan="1">-</td>
<td align="center" rowspan="1" colspan="1">65.99</td>
</tr>
<tr><td rowspan="1" colspan="1">1421</td>
<td align="center" rowspan="1" colspan="1">b-Caryophyllene</td>
<td align="center" rowspan="1" colspan="1">-</td>
<td align="center" rowspan="1" colspan="1">28.32</td>
</tr>
<tr><td rowspan="1" colspan="1">1455</td>
<td align="center" rowspan="1" colspan="1">α-humulene</td>
<td align="center" rowspan="1" colspan="1">-</td>
<td align="center" rowspan="1" colspan="1">2.34</td>
</tr>
<tr><td rowspan="1" colspan="1">1522</td>
<td align="center" rowspan="1" colspan="1">Eugenol acetate</td>
<td align="center" rowspan="1" colspan="1">-</td>
<td align="center" rowspan="1" colspan="1">3.35</td>
</tr>
<tr><td colspan="4" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Total</td>
<td rowspan="1" colspan="1"></td>
<td align="center" rowspan="1" colspan="1">99.00</td>
<td align="center" rowspan="1" colspan="1">100.00</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="TFN1"><p>FID: flame ionization gas chromatography; RI: relative retention index
calculated against <italic>n</italic>
-alkanes, applying the Van den Dool
equation; %: compound percentage.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</p>
<p>The major component of <italic>C. sinensis</italic>
was identified as limonene,
accounting for 91.88% of the essential oil, and for <italic>S. aromaticum</italic>
, the
main component was eugenol, accounting for 65.99% of the essential oil.</p>
<p>The <italic>Ae. aegypti</italic>
larvae susceptibility assays demonstrated that
<italic>S. aromaticum</italic>
and <italic>C. sinensis</italic>
essential oils have
larvicidal effects in all tested populations. Because no mortality above 20% in the
control groups was observed, the use of Tween 80 as a surfactant had no effect on
mortality; therefore, none of the assays were invalidated. Lethal concentrations and
their respective CIs are presented in <xref ref-type="table" rid="t2">Table
II</xref>
.</p>
<p><table-wrap id="t2" orientation="portrait" position="float"><label>TABLE II</label>
<caption><title>Lethal concentrations (LC<sub>50</sub>
, LC<sub>95</sub>
, and
LC<sub>99</sub>
) and confidence intervals (CI) of essential oils and their
combinations with temephos in <italic>Aedes aegypti</italic>
field-collected in
Araçatuba, Marília and Santos and the Rockefeller strain</title>
</caption>
<table frame="hsides" rules="groups"><colgroup width="20%" span="1"><col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
</colgroup>
<thead><tr><th align="left" style="font-weight:normal" rowspan="1" colspan="1">Larvicide</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Strain</th>
<th style="font-weight:normal" rowspan="1" colspan="1">LC<sub>50</sub>
(95%
CI) ppm</th>
<th style="font-weight:normal" rowspan="1" colspan="1">LC<sub>95</sub>
(95%
CI) ppm</th>
<th style="font-weight:normal" rowspan="1" colspan="1">LC<sub>99</sub>
(95%
CI) ppm</th>
</tr>
</thead>
<tbody><tr><td rowspan="4" colspan="1"><italic>Citrus sinensis</italic>
</td>
<td align="center" rowspan="1" colspan="1">Rockefeller</td>
<td align="center" rowspan="1" colspan="1">11.92 (11.7 to 12.2)</td>
<td align="center" rowspan="1" colspan="1">17.40 (16.4 to 18.9)</td>
<td align="center" rowspan="1" colspan="1">20.36 (18.8 to 22.7)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">15.06 (14.7 to 15.5)</td>
<td align="center" rowspan="1" colspan="1">27.59 (26.3 to 29.1)</td>
<td align="center" rowspan="1" colspan="1">35.45(33.3 to 38.1)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">13.70 (13.4 to 14.0)</td>
<td align="center" rowspan="1" colspan="1">21.08 (20.4 to 21.9)</td>
<td align="center" rowspan="1" colspan="1">25.20 (24.1 to 26.6)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">16.30 (15.5 to 17.1)</td>
<td align="center" rowspan="1" colspan="1">34.18 (31.5 to 37.7)</td>
<td align="center" rowspan="1" colspan="1">46.40 (41.7 to 53)</td>
</tr>
<tr><td rowspan="4" colspan="1"><italic>Syzygium aromaticum</italic>
</td>
<td align="center" rowspan="1" colspan="1">Rockefeller</td>
<td align="center" rowspan="1" colspan="1">93.56 (90.1 to 97.0)</td>
<td align="center" rowspan="1" colspan="1">167.85 (157.2 to 182.1)</td>
<td align="center" rowspan="1" colspan="1">213.83 (195.6 to 239.0)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">92.97 (90.0 to 95.8)</td>
<td align="center" rowspan="1" colspan="1">163.40 (156.2 to 172.0)</td>
<td align="center" rowspan="1" colspan="1">206.40 (194.4 to 221.4)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">106.90 (103.9 to 109.8)</td>
<td align="center" rowspan="1" colspan="1">174.20 (167.7 to 181.9)</td>
<td align="center" rowspan="1" colspan="1">213.20 (202.6 to 226.3)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">95.00 (92.2 to 97.8)</td>
<td align="center" rowspan="1" colspan="1">155.50 (148.3 to 164.4)</td>
<td align="center" rowspan="1" colspan="1">190.70 (179.1 to 205.6)</td>
</tr>
<tr><td rowspan="4" colspan="1"><italic>C. sinensis</italic>
+ temephos</td>
<td align="center" rowspan="1" colspan="1">Rockefeller</td>
<td align="center" rowspan="1" colspan="1">0.33 (0.29 to 0.35)</td>
<td align="center" rowspan="1" colspan="1">0.57 (0.53 to 0.65)</td>
<td align="center" rowspan="1" colspan="1">0.73 (0.64 to 0.88)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">1.65 (1.48 to 1.81)</td>
<td align="center" rowspan="1" colspan="1">5.13 (4.61 to 5.83)</td>
<td align="center" rowspan="1" colspan="1">8.21 (7.08 to 9.86)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">1.78 (1.61 to 1.95)</td>
<td align="center" rowspan="1" colspan="1">5.48 (4.39 to 7.80)</td>
<td align="center" rowspan="1" colspan="1">8.75 (6.43 to 14.33)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">1.88 (1.65 to 2.09)</td>
<td align="center" rowspan="1" colspan="1">5.35 (4.62 to 6.56)</td>
<td align="center" rowspan="1" colspan="1">8.25 (6.70 to 11.14)</td>
</tr>
<tr><td rowspan="4" colspan="1"><italic>S. aromaticum</italic>
+ temephos</td>
<td align="center" rowspan="1" colspan="1">Rockefeller</td>
<td align="center" rowspan="1" colspan="1">0.72 (0.69 to 0.75)</td>
<td align="center" rowspan="1" colspan="1">1.00 (0.94 to 1.08)</td>
<td align="center" rowspan="1" colspan="1">1.14 (1.06 to 1.26)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">1.66 (1.5 to 1.8)</td>
<td align="center" rowspan="1" colspan="1">4.39 (3.8 to 5.4)</td>
<td align="center" rowspan="1" colspan="1">6.60 (5.36 to 8.81)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">1.87 (1.41 to 2.21)</td>
<td align="center" rowspan="1" colspan="1">5.20 (4.21 to 7.74)</td>
<td align="center" rowspan="1" colspan="1">7.94 (10.98 to 24.13)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">1.96 (1.75 to 2.14)</td>
<td align="center" rowspan="1" colspan="1">3.96 (3.53 to 4.65)</td>
<td align="center" rowspan="1" colspan="1">5.30 (4.54 to 6.66)</td>
</tr>
<tr><td rowspan="4" colspan="1">Temephos</td>
<td align="center" rowspan="1" colspan="1">Rockefeller</td>
<td align="center" rowspan="1" colspan="1">0.0035 (0.0034 to 0.0036)</td>
<td align="center" rowspan="1" colspan="1">0.0052 (0.0050 to 0.0054)</td>
<td align="center" rowspan="1" colspan="1">0.0061 (0.0058 to 0.0065)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">0.0130 (0.012 to 0.013)</td>
<td align="center" rowspan="1" colspan="1">0.0240 (0.023 to 0.026)</td>
<td align="center" rowspan="1" colspan="1">0.0310 (0.028 to 0.034)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">0.0088 (0.0083 to 0.0092)</td>
<td align="center" rowspan="1" colspan="1">0.0180 (0.017 to 0.019)</td>
<td align="center" rowspan="1" colspan="1">0.02400 (0.022 to 0.027)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">0.0120 (0.011 to 0.012)</td>
<td align="center" rowspan="1" colspan="1">0.0200 (0.0191 to 0.022)</td>
<td align="center" rowspan="1" colspan="1">0.0260 (0.024 to 0.028)</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="TFN2"><p>95% CI: ninety-five percent probability confidence interval.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</p>
<p><italic>C. sinensis</italic>
evaluated as a larvicide exhibited significantly different
LC<sub>95</sub>
s in different <italic>Ae. aegypti</italic>
populations because no
overlap in 95% confidence intervals was observed for any population. In contrast, the
LC<sub>95</sub>
for <italic>S. aromaticum</italic>
exhibited no significant
differences between the field-collected populations and the Rockefeller strain, and
within the field-collected populations, only the LC<sub>95</sub>
s for the Santos and
Marília populations were significantly different. The average CI ranges for <italic>C.
sinensis</italic>
and <italic>S. aromaticum</italic>
were 3.25 and 17.75,
respectively, demonstrating a greater variability of the latter because it had verified
activity over a larger range of concentrations.</p>
<p>The combinations of essential oils and temephos evaluated in the field-collected
populations of <italic>Ae. aegypti</italic>
had a significantly different
LC<sub>95</sub>
compared to that of the Rockefeller strain, exhibiting a resistance
profile close to that of temephos alone.</p>
<p><xref rid="B8" ref-type="bibr">Chaieb et al. (2007)</xref>
and <xref rid="B27" ref-type="bibr">Simas et al. (2004)</xref>
found that LC<sub>50</sub>
= 44.5 ppm for
eugenol, the major compound in <italic>S. aromaticum</italic>
essential oil, in
<italic>Ae. aegypti</italic>
populations. The larvicidal activity of <italic>S.
aromaticum</italic>
essential oil has been previously reported by several authors.
<xref rid="B11" ref-type="bibr">Costa et al. (2005)</xref>
found that LC<sub>50</sub>
= 21.4 ppm , while <xref rid="B12" ref-type="bibr">Fayemiwo et al. (2014)</xref>
found
LC<sub>50</sub>
= 92.56 and <xref rid="B2" ref-type="bibr">Barbosa et al.
(2012)</xref>
obtained values of 62.3 and 77.0 ppm for field-collected and
Rockefeller larvae, respectively. The differences in the LC<sub>50</sub>
values observed
in the present and previous studies can be explained as a result the use of different
populations, methodologies, and the composition of the essential oils tested.</p>
<p>The pH of the deionized water was not altered by the addition of essential oils or
mixtures, even at the highest concentration used in the study, eliminating the
possibility of larvae mortality caused by increased acidity.</p>
<p>According to Mazzari and Georghiou (<xref rid="B18" ref-type="bibr">Mazzarri &
Georghiou 1995</xref>
), a mosquito strain is considered susceptible when its
resistance ratio is less than five, moderately resistant when the resistance ratio is
between five and ten, and highly resistant when the resistance ratio is greater than
ten. Accordingly, the results of this study show that the resistance levels to the
essential oils alone are low and the field-collected strains are susceptible to the
composition of the essential oils. However, the resistance ratio for temephos and the
essential oil/temephos combinations is considered moderate (<xref ref-type="table" rid="t3">Table III</xref>
). The <italic>C. sinensis</italic>
/temephos combinations
exhibited resistance ratios close to ten. Therefore, within the evaluated products, the
<italic>C. sinensis</italic>
/temephos mixture is less suitable for use as a larvicide
to control this vector.</p>
<p><table-wrap id="t3" orientation="portrait" position="float"><label>TABLE III</label>
<caption><title>Resistance ratios to the larvicidal compositions for resistant
strains</title>
</caption>
<table frame="hsides" rules="groups"><colgroup width="20%" span="1"><col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
</colgroup>
<thead><tr><th align="left" style="font-weight:normal" rowspan="1" colspan="1">Larvicide</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Strain</th>
<th style="font-weight:normal" rowspan="1" colspan="1">RR LC<sub>50</sub>
</th>
<th style="font-weight:normal" rowspan="1" colspan="1">RR LC<sub>95</sub>
</th>
<th style="font-weight:normal" rowspan="1" colspan="1">RR LC<sub>99</sub>
</th>
</tr>
</thead>
<tbody><tr><td rowspan="3" colspan="1"><italic>Citrus sinensis</italic>
</td>
<td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">1.3</td>
<td align="center" rowspan="1" colspan="1">1.6</td>
<td align="center" rowspan="1" colspan="1">1.7</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">1.1</td>
<td align="center" rowspan="1" colspan="1">1.2</td>
<td align="center" rowspan="1" colspan="1">1.2</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">1.4</td>
<td align="center" rowspan="1" colspan="1">2.0</td>
<td align="center" rowspan="1" colspan="1">2.3</td>
</tr>
<tr><td rowspan="3" colspan="1"><italic>Syzygium aromaticum</italic>
</td>
<td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">1.0</td>
<td align="center" rowspan="1" colspan="1">1.0</td>
<td align="center" rowspan="1" colspan="1">1.0</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">1.1</td>
<td align="center" rowspan="1" colspan="1">1.0</td>
<td align="center" rowspan="1" colspan="1">1.0</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">1.0</td>
<td align="center" rowspan="1" colspan="1">0.9</td>
<td align="center" rowspan="1" colspan="1">0.9</td>
</tr>
<tr><td rowspan="3" colspan="1">Temephos</td>
<td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">3.7</td>
<td align="center" rowspan="1" colspan="1">4.6</td>
<td align="center" rowspan="1" colspan="1">5.1</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">2.5</td>
<td align="center" rowspan="1" colspan="1">3.5</td>
<td align="center" rowspan="1" colspan="1">3.9</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">3.4</td>
<td align="center" rowspan="1" colspan="1">3.8</td>
<td align="center" rowspan="1" colspan="1">4.3</td>
</tr>
<tr><td rowspan="3" colspan="1"><italic>C. sinensis</italic>
+ temephos</td>
<td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">5.0</td>
<td align="center" rowspan="1" colspan="1">9.0</td>
<td align="center" rowspan="1" colspan="1">11.2</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">5.4</td>
<td align="center" rowspan="1" colspan="1">9.6</td>
<td align="center" rowspan="1" colspan="1">12.0</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">5.7</td>
<td align="center" rowspan="1" colspan="1">9.4</td>
<td align="center" rowspan="1" colspan="1">11.3</td>
</tr>
<tr><td rowspan="3" colspan="1"><italic>S. aromaticum</italic>
+ temephos</td>
<td align="center" rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">2.3</td>
<td align="center" rowspan="1" colspan="1">4.4</td>
<td align="center" rowspan="1" colspan="1">5.8</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">2.6</td>
<td align="center" rowspan="1" colspan="1">5.2</td>
<td align="center" rowspan="1" colspan="1">7.0</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">2.7</td>
<td align="center" rowspan="1" colspan="1">4.0</td>
<td align="center" rowspan="1" colspan="1">4.6</td>
</tr>
</tbody>
</table>
</table-wrap>
</p>
<p>The Brazilian <italic>Ae. aegypti</italic>
insecticide resistance monitoring network
(MoReNAa) suggests a substitution of the larvicide when the resistance ratio is equal to
or higher than three (Secretaria de Vigilância em Saúde 2006, unpublished data).
Therefore, <italic>C. sinensis</italic>
and <italic>S. aromaticum</italic>
essential
oils are potential candidates for use as auxiliary larvicides to control <italic>Ae.
aegypti</italic>
strains that are resistant to temephos, while their combinations
with temephos are not recommended for use as larvicides.</p>
<p>Concentration-response plots were generated based on the methodology proposed by <xref rid="B4" ref-type="bibr">Bliss (1935)</xref>
and <xref rid="B13" ref-type="bibr">Fisher (1935)</xref>
, which allows for the comparison between different populations
and tested products by transforming the sigmoid concentration-response curves to lines
by converting the concentration to a logarithmic scale and the percent mortality to a
probit scale, which ranges from two-eight. The lines are illustrated in <xref ref-type="fig" rid="f01">Fig. 1</xref>
.</p>
<p><fig id="f01" orientation="portrait" position="float"><label>Fig. 1</label>
<caption><title>: dose-response curves created using bioassay data after exposure to the
essential oils of <italic>Citrus sinensis</italic>
(A) and <italic>Syzygium
aromaticum</italic>
(B), temephos combinations (C-D) and temephos alone
(E).</title>
</caption>
<graphic xlink:href="0074-0276-mioc-0074-02760160075-gf01"></graphic>
</fig>
</p>
<p>The concentration required by <italic>S. aromaticum</italic>
to act as a larvicide is
approximately 10 times higher than that of <italic>C. sinensis</italic>
(<xref ref-type="fig" rid="f01">Fig. 1</xref>
, plots 1A-B). However, the mortality response
obtained by the former essential oil in all populations is more homogeneous than that of
<italic>C. sinensis</italic>
. Furthermore, the concentration needed for temephos
alone to act as a larvicide is lower than that of the essential oil/temephos
combinations (<xref ref-type="fig" rid="f01">Fig. 1</xref>
, plots 1C-E).</p>
<p>According to the concept proposed by Brindley and Selim (<xref rid="B6" ref-type="bibr">Brindley & Selim 1984</xref>
), synergists are substances that, although used in
sublethal concentrations, confer a higher mortality than that of each single agent. The
concentration of temephos to achieve the LC<sub>50</sub>
in the temephos/essential oil
mixtures was higher than that of temephos alone for all tested populations. Therefore,
the essential oils in combination with temephos exerted an antagonistic effect (<xref ref-type="table" rid="t4">Table IV</xref>
).</p>
<p>The results of the oviposition behaviour assay demonstrated that gravid females
oviposited in all available sites. However, the number of eggs in each site was
significantly different (p < 0.05). The number of eggs at oviposition sites
containing essential oils was significantly lower than the sites containing tap water,
as described in <xref ref-type="table" rid="t5">Table V</xref>
and illustrated in <xref ref-type="fig" rid="f02">Fig. 2</xref>
.</p>
<p><table-wrap id="t4" orientation="portrait" position="float"><label>TABLE IV</label>
<caption><title>Concentration of temephos at LC<sub>50</sub>
for the essential oil/temephos
combinations and temephos alone</title>
</caption>
<table frame="hsides" rules="groups"><colgroup width="25%" span="1"><col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
</colgroup>
<thead><tr><th align="left" style="font-weight:normal" rowspan="1" colspan="1">Strain</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Concentration of
temephos<sup>1</sup>
</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Concentration of
temephos<sup>2</sup>
</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Concentration of
temephos<sup>3</sup>
</th>
</tr>
</thead>
<tbody><tr><td rowspan="1" colspan="1">Rockefeller</td>
<td align="center" rowspan="1" colspan="1">0.004</td>
<td align="center" rowspan="1" colspan="1">0.006</td>
<td align="center" rowspan="1" colspan="1">0.007</td>
</tr>
<tr><td rowspan="1" colspan="1">Araçatuba</td>
<td align="center" rowspan="1" colspan="1">0.013</td>
<td align="center" rowspan="1" colspan="1">1.620</td>
<td align="center" rowspan="1" colspan="1">0.016</td>
</tr>
<tr><td rowspan="1" colspan="1">Marília</td>
<td align="center" rowspan="1" colspan="1">0.009</td>
<td align="center" rowspan="1" colspan="1">1.748</td>
<td align="center" rowspan="1" colspan="1">0.019</td>
</tr>
<tr><td rowspan="1" colspan="1">Santos</td>
<td align="center" rowspan="1" colspan="1">0.012</td>
<td align="center" rowspan="1" colspan="1">1.846</td>
<td align="center" rowspan="1" colspan="1">0.019</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="TFN3"><p><sup>1</sup>
alone; <sup>2</sup>
in combination with <italic>Citrus
sinensis</italic>
; <sup>3</sup>
in combination with <italic>Syzygium
aromaticum</italic>
.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</p>
<p><table-wrap id="t5" orientation="portrait" position="float"><label>TABLE V</label>
<caption><title>Oviposition response of female <italic>Aedes aegypti</italic>
in
oviposition sites containing water, <italic>Citrus sinensis</italic>
, and
<italic>Syzygium aromaticum</italic>
essential oils</title>
</caption>
<table frame="hsides" rules="groups"><colgroup width="20%" span="1"><col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
<col span="1"></col>
</colgroup>
<thead><tr><th align="left" style="font-weight:normal" rowspan="1" colspan="1"></th>
<th style="font-weight:normal" rowspan="1" colspan="1"><italic>S. aromaticum</italic>
</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Water</th>
<th style="font-weight:normal" rowspan="1" colspan="1"><italic>C. sinensis</italic>
</th>
<th style="font-weight:normal" rowspan="1" colspan="1">Water</th>
</tr>
</thead>
<tbody><tr><td rowspan="1" colspan="1">Total number of eggs <italic>per</italic>
oviposition site</td>
<td align="center" rowspan="1" colspan="1">515</td>
<td align="center" rowspan="1" colspan="1">14536</td>
<td align="center" rowspan="1" colspan="1">5050</td>
<td align="center" rowspan="1" colspan="1">7592</td>
</tr>
<tr><td rowspan="1" colspan="1">Average number of eggs every 48 h</td>
<td align="center" rowspan="1" colspan="1">34</td>
<td align="center" rowspan="1" colspan="1">969</td>
<td align="center" rowspan="1" colspan="1">337</td>
<td align="center" rowspan="1" colspan="1">506</td>
</tr>
<tr><td rowspan="1" colspan="1">Standard deviation</td>
<td align="center" rowspan="1" colspan="1">40.98</td>
<td align="center" rowspan="1" colspan="1">521.49</td>
<td align="center" rowspan="1" colspan="1">220.61</td>
<td align="center" rowspan="1" colspan="1">295,35</td>
</tr>
<tr><td rowspan="1" colspan="1">Student’s t-test</td>
<td align="center" rowspan="1" colspan="1">0.000002</td>
<td align="center" rowspan="1" colspan="1">-</td>
<td align="center" rowspan="1" colspan="1">0.0006</td>
<td align="center" rowspan="1" colspan="1">-</td>
</tr>
<tr><td rowspan="1" colspan="1">Oviposition Index</td>
<td align="center" rowspan="1" colspan="1">-0.93</td>
<td align="center" rowspan="1" colspan="1">-</td>
<td align="center" rowspan="1" colspan="1">-0.2</td>
<td align="center" rowspan="1" colspan="1">-</td>
</tr>
</tbody>
</table>
</table-wrap>
</p>
<p><fig id="f02" orientation="portrait" position="float"><label>Fig. 2</label>
<caption><title>: total number of eggs laid in paired oviposition sites, with and without
the presence of each essential oil.</title>
</caption>
<graphic xlink:href="0074-0276-mioc-0074-02760160075-gf02"></graphic>
</fig>
</p>
<p><xref rid="B17" ref-type="bibr">Marques et al. (2013)</xref>
reported the oviposition
index (OI), ranging from -1 to +1, to evaluate oviposition-attractant or -repellent
substances. A positive OI means that the substance has an attractant activity, while a
negative value means the substance has a repellent activity. <italic>C.
sinensis</italic>
and <italic>S. aromaticum</italic>
exhibited OIs of -0.2 and -0.93,
respectively. Although <italic>C. sinensis</italic>
exhibited a low repellency profile,
the essential oils evaluated here exhibit negative OIs and therefore have repellent
effects on <italic>Ae. aegypti</italic>
oviposition. According to <xref rid="B15" ref-type="bibr">Machado and Fernandes Jr (2011)</xref>
, essential oils are natural,
volatile and complex compounds, characterised by a strong odour, which influence the
ovipositional behaviour of the gravid female. Repellence is an aggravating influence for
larvicides because the vector avoids oviposition in treated containers, favouring
non-treated water sources for oviposition. These results should be considered in the
development of new formulations because essential oil volatility increases repellency,
and therefore low volatile formulations will decrease repellency.</p>
<p><italic>C. sinensis</italic>
and <italic>S. aromaticum</italic>
exhibit similar
larvicidal activities in <italic>Ae. aegypti</italic>
populations with different
susceptibility profiles to the organophosphate temephos. Therefore, the evaluated
essential oils have the potential to be used in mosquito control as an alternative to
overcome <italic>Ae. aegypti</italic>
resistance.</p>
<p>The mechanism of action of the essential oil of <italic>S. aromaticum</italic>
is most
likely different from that of temephos because no significant difference was observed
between the larvicidal activity for this essential oil in susceptible Rockefeller and
resistant strains. In contrast, <italic>C. sinensis</italic>
essential oil exhibited
significantly different larvicidal activities between the evaluated populations, which
indicates either cross-resistance to previously used larvicides or close contact to this
essential oil, as São Paulo state is the main citrus producer in Brazil.</p>
<p>The combination of the evaluated essential oils and temephos did not display increased
toxicity; therefore, no synergistic effect was observed. Additionally, resistance was
found to essential oil/temephos combinations, and therefore the combined use of the
evaluated essential oils and temephos is not recommended.</p>
<p>The essential oils evaluated here exhibit repellent effects on the oviposition behaviour
of <italic>Ae. aegypti</italic>
females. Therefore, volatility should be considered
during the development of larvicides formulations containing these products, with the
goal of reducing volatility and consequently reducing repellency.</p>
<p>The results suggest that the <italic>S. aromaticum</italic>
and <italic>C.
sinensis</italic>
essential oils represent an alternative as low-toxicity natural
larvicides and a promising approach for <italic>Ae. aegypti</italic>
control, especially
in strains showing resistance to currently employed larvicides, such as
organophosphates.</p>
</sec>
</body>
<back><fn-group><fn fn-type="financial-disclosure" id="fn1"><p>Financial support: FAPITEC-SE, CNPq (550116-2010-9-Rede Dengue).</p>
</fn>
</fn-group>
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