Volume 5, Issue 4, April 2015, Pages 287–291
Document heading
Toxicity of Mexican native plant extracts against larvae of Aedes aegypti (Diptera: Culicidae)
- Open Access funded by Hainan Medical University
- Under a Creative Commons license
Open Access
ABSTRACT
Objective
To evaluate five indigenous Mexican plants [Hippocratea excelsa, Hippocratea celastroides, Argemone mexicana (A. mexicana), Tagetes lucida, and Pseudosmodingium perniciosum (P. perniciosum)] toxicity against the fourth instar larvae of the dengue primary vector, Aedes aegypti (A. aegypti).
Methods
Each
plant part was treated successively with hexane, ethyl acetate,
acetone, and methanol to extract potential active components of the
plants against the dengue vector.
Results
There was a range of toxicity at 24 or 48 h post-exposure for the different plant parts and organic solvent used (LC50 values ranged between 20 and 890 μg/mL). Extracts from seeds of A. mexicana (hexane washing with methanol and acetone) and stem-bark of P. perniciosum (hexane) showed highest toxicity to Ae. aegypti larvae at 48 h post-exposure (LC50
values were 80, 50, and 20 μg/mL, respectively), thus making them
potential candidates as biolarvicides. Efforts are on-going to
characterize the bioactive components of the extracts, through
chromatography, for their use as biological tools for the control of the
primary dengue vector.
Conclusions
A. mexicana and P. perniciosum are good candidates to combat the dengue vector, Ae. aegypti, as they were highly toxic to the larvae.
KEYWORDS
- Aedes aegypti;
- Dengue;
- Larvicidal activity;
- Plant organic extracts
1. Introduction
Dengue is a viral disease transmitted by Aedes mosquitoes and constitutes a serious public health threat worldwide[ 1, 2, 3, 4 and 5]. The control of the dengue primary vector, Aedes aegypti (Ae. aegypti),
stems mostly on chemical insecticides. The wide spread of insecticide
resistance has reduced the ability of insecticides to control mosquito
vectors[ 2, 6, 7 and 8].
Thus, the search for new control strategies that can tackle insecticide
resistance or reduce the use of such chemicals in insect vectors are
desperately needed. Plants usually produce compounds which protect them
from insects, and these compounds have detrimental effect on the
development of the insects[ 9 and 10]. These observations have therefore encouraged studies to evaluate Mexican native plants against the dengue primary vector.
One
of the effective methods to control insect vectors is the prevention of
mosquito breeding through the use of easily biodegradable insecticides.
Much of the research against Ae. aegypti mosquitoes have focused on by-products of plants already utilized for economic gain or on already recognized medicinal plants[ 11, 12, 13 and 14].
The use of botanical insecticides has been intensified over the past
decades due to their bioactive compounds, which leave no residues in the
environment; hence, it's suitable for integrated vector management
programs (IVMP). Traditionally, IVMP have been based on two components:
chemical control (temephos as larvicide and organophosphates and
pyrethroids as adulticides applied by ultra-low volume space spraying)
and community contribution to remove the water in artificial containers
that serve as breeding sites for the mosquitoes. However, dengue is
associated to the lowest socio-economical strata of the endemic
(developing) countries worldwide where the community lacks a culture of
participation[ 15 and 16].
In Mexico, dengue fever has increased significantly in recent years and there are reports of resistance of Ae. aegypti to chemical insecticides[ 17, 18 and 19].
Nowadays, the application of chemical insecticides is still a major
tool that Mexican Health Secretariat has been using against the dengue
primary vector. In Mexico, there are several reports on the use of
promising biological agents to control Ae. aegypti[ 11 and 17]. However, most of the natural enemies of the Aedes
mosquitoes incriminated in suburban and urban transmission areas are at
experimental level. In addition, many reports have been published on
the toxicity of botanical larvicides against Ae. aegypti[ 11, 12, 20 and 21].
In this study, five indigenous Mexican plants [Hippocratea excelsa (H. excelsa), Hippocratea celastroides (H. celastroides), Argemone mexicana (A. mexicana), Tagetes lucida (T. lucida), and Pseudosmodingium perniciosum (P. perniciosum)] were evaluated for its toxicity against the fourth larval instar of the dengue primary vector, Ae. aegypti.
All these plants are easily available and have medicinal values.
However, there is not known information on their larvicidal potentials
against Ae. aegypti, except for the seed of A. mexicana which had been signaled as chemosterilant agent against Ae. aegypti[ 13 and 22].
The accessibility to indigenous plant material will enhance their use
among the affected population as they have been proved to be efficient
against the disease vector mosquitoes. In addition, the plants can be
grown by rural or semi-urban communities which will provide sustainable
and relatively cheap mosquito control.
2. Materials and methods
2.1. Plants
Selected fresh plant specimens of H. excelsa Kunth (Hippocrateaceae) and H. celastroides
Kunth (Hippocrateaceae) were collected in March 2009 from the community
of Iguala (18°24 N, 99°32.15′ W) in the state of Guerrero. A. mexicana
(Papaveraceae) was collected in May 2008 from the community of San
Felipe Ixtacuixtla (19°19′ N, 98°22 W) in the state of Tlaxcala, and T. lucida
Cav. (Compositae) was collected between June and July 2009 from the
communities of Calpulalpan (19°33 N, 98°35 W) and Nanacamilpa (19°28 N,
98°30 W) in the State of Tlaxcala. P. perniciosum
(Anacardiaceae) was collected in September 2009 from the communities of
Buenavista de Cuéllar (18°29′ N, 99°27 W) in the state of Guerrero.
Voucher specimens of each taxonomically identified plant were deposited
at the Herbario Nacional de México in the Instituto de Biología of the
Universidad Nacional Autónoma de México.
2.2. Organic extracts
Selected
parts of the plants: roots, stems, leaves, flowers, seeds, and
stem-bark, freshly collected were dried and each portion (≤ 500 g)
grinded through two consecutive maceration processes (each one for three
days). The solvents used to extract bioactive compounds from plants
were hexane, ethyl acetate, acetone, and methanol. Plants crude extracts
were also concentrated and stored at −4 °C until tested. Stock
solutions (500 μg/mL) of each extract containing 1% dimethylsulphoxide
(Aldrich, Milwuakee, WI, USA) were prepared. Three serial dilutions 250,
125, and 50 μg/mL in distilled water were then prepared from the stock
solution.
Preliminary
phytochemical screening of plants with better activity was carried out
to identify chemical groups of substances such as alkaloids, flavonoids,
coumarins, saponins, tanins, cardiotonics glycosides, and sterols
and/or terpenes[23].
2.3. Mosquitoes
Ae. aegypti
eggs were collected from the state of Guerrero, Mexico by the personnel
of the Mexican Health Secretariate. Briefly, pieces of filter paper
with the eggs attached were submerged into 500 mL of dechlorinated water
for 30 to 60 min to allow the eggs to hatch into larvae. The larvae
were reared under insectary conditions at (27 ± 2) °C, 70% ± 10%
relative humidity and 14 h-10 h light-dark photoperiod. They were daily
fed ad libitum with fish food until pupation. The pupae were
collected and placed inside cages, where adults were fed with a 10%
sucrose-honey solution. Three day old female mosquitoes were placed in
metal cages with a surgical stockinet sleeve and fed with rabbit blood
for 2 h every four days as previously described[ 24 and 25]. The gravid mosquitoes laid their eggs and subsequent generations (F1 and F2) were obtained.
2.4. Bioassays
This study encompassed bioassays to test larvicidal activity expressed as LC50 in μg/mL against the F2Ae. aegypti larvae. To comply with the World Health Organization requirements[ 26],
twenty fourth-instar larvae were placed in glass beakers containing 100
mL of the stock solution (500 μg/mL) for preliminary screening. Plant
extracts which produced over 50% larval mortality during the initial
testing were serially diluted to 250, 125, and 50 μg/mL in distilled
water. The LC50 for Ae. aegypti larvae was
determined in five treatments (including 14 plant parts and four organic
solvents) plus two controls dimethylsulphoxide and deionized water
(1:100) and 100 mL of distilled water alone. A total of 1 344 larvae per
treatment were used, encompassing four replicates of 24 each in a glass
beaker containing 100 mL of each plant´s part extract in solvent. Dead
larvae in treatments were recorded 24 and 48 h post-exposure and removed
daily. Larvae were considered dead if they did not respond to physical
stimulus (with a wooden stick). No food was provided to the larvae
during the bioassay.
2.5. Statistical analysis
Probit analyses were conducted on Ae. aegypti
mortality data collected after 24 h and 48 h post-exposure to organic
extracts from parts of five plant species using the software IBM-SPSS
Statistics V.19 to determine the LC50[ 27]. A P-value of 0.05 or less was considered statistically significant.
3. Results
Bioassays using five species of plants were conducted to determine larvicidal activity against the fourth instar Ae. aegypti larvae. Six plant parts and four organic solvents, making a total of 24 combinations, were used to determine LC50. Actual bioassay values of these plant extracts against Ae. aegypti larvae were indicated in Table 1. The LC50 actual values of the seeds of A. mexicana
using acetone and hexane as solvents were 60 and 100 μg/mL after 24 h
post-exposure and 50 and 80 μg/mL after 48 h, respectively. The hexanoic
extract from stem-bark of P. perniciosum increased 5-fold of their efficiency (P < 0.05) against Ae. aegypti from 24 to 48 h post-exposure. The LC50 actual value fell from 110 μg/mL to 20 μg/mL, the lowest LC50 seen after 48 h post-exposure. Table 2
summarizes relative toxicity of all bioassays performed using four
solvents to extract the compounds in aforementioned parts of the plants.
When using methanol as solvent, no larvicidal activity was observed
from the extracts. The highest larvicidal activity was recorded within
24 h post-exposure when hexane and acetone were used as extracting
solvents for the seeds of A. mexicana. Similarly, a relatively high activity, but only at 48 h post-exposure, was recorded in roots extract using ethyl acetate. P. perniciosum,
also showed high larvicidal activity within 24 h post-exposure when the
compounds were extracted from stem-bark using hexane. Relative lower
larvicidal activities were observed in the extracts of the other three
plants (T. lucida, H. excelsa, and H. celastroides).
- Table 1. The LC50 for Ae. aegypti larvae at 24 and 48 h post-exposure to organic extracts from parts of five Mexican plant species.
Plant species Plant part Organic solvent LC50 expressed in μg/mL
24 h 48 h T. lucida Flower Hexane 250 (220-270) 230 (170-300) Ethyl acetate 180 (160-200) 180 (160-210) Acetone 570 (490-740) 430 (380-470) Leaf Hexane 260 (130-310) 250 (180-290) Ethyl acetate 190 (160-210) 170 (150-190) Stem Hexane 210 (80-250) 210 (120-240) Ethyl acetate 180 (120-220) 130 (110-160) A. mexicana Seed Hexane* 100 (100-150) 80 (80-130) Ethyl acetate 340 (290-410) 230 (90-290) Acetone 60 (40-70) 50 (30-60) Flower Ethyl acetate 390 (250-490) 330 (200-590) Leaf Hexane 400 (220-610) 430 (230-660) Ethyl acetate 640 (520-890) 560 (460-860) Acetone 300 (300-390) 250 (120-340) Stem Ethyl acetate 340 (90-390) 230 (190-270) Root 270 (240-310) 150 (100-190) Acetone 230 (160-290) 210 (120-320) Methanol 580 (430-730) 530 (450-680) H. excelsa Stem Hexane 610 (510-990) 490 (430-610) H. celastroides Leaf Ethyl acetate 840 (580-930) 500 (380-680) Stem Acetone 740 (520-940) 600 (470-890) P. perniciosum Leaf Hexane 890 (550-990) 190 (140-240) Stem-bark 110 (110-130) 20 (10-30) Ethyl acetate 580 (430-730) 200 (110-340) - The LC50 was estimated by probit analysis. LC50 value represents point estimate and LC50 values in parentheses represent the standard deviation surrounding point estimate.
-
- *
- : Washed with ethanol.
- Table 2. Relative toxicity of fourth instar Ae. aegypti larvae to organic extracts from parts of five Mexican plant species.
Plant species Plant part Solvent
Hexane
Ethyl acetate
Acetone
Methanol
24 h 4 00 h 24 h 48 h 24 h 4 00 h 24 h 4 00 h T. lucida Flower + ++ ++ ++ + + − − Leaf + ++ ++ ++ − − − − Stem ++ ++ + ++ − − − − A. mexicana Seed +++ +++ + ++ +++ +++ − − Flower − − + + + + − − Leaf + + + + + ++ − − Stem Root − − ++ +++ ++ ++ + + H. excelsa Stem Leaf + + − − − − − − H. celastroides Leaf − − + + − − − − Stem − − − − + + − − P. perniciosum Leaf − − + ++ − − − − Stem bark +++ +++ + ++ − − − − - +++: LC50 < 150 μg/mL; ++: LC50 between 150-250 μg/mL; +: LC50 > 250 μg/mL;-: No activity detected.
In general, there was no association between the larvicidal activity against Ae. aegypti
and the polarity of the solvent used in the extract given that a
preliminary phytochemical analysis performed with the extracts with the
highest activity ( Table 3)
showed differences in the content of chemical compounds. The presence
of alkaloids was overwhelming in the hexanic and ethyl acetate extracts
of seeds of A. mexicana; however, the cetonic extract did not
reveal its presence. Other important components found were sterols
and/or terpenoids and tanins that were identified in all extracts of A. mexicana. Meanwhile, in the hexanic extract from stem-bark of P. perniciosum, the most abundant chemical groups were cumarins, tannins, sterols/terpenoids, and flavonoids.
- Table 3. Preliminary phytochemical analysis performed with the extracts showing the highest larvicidal activity against Ae. aegypti.
Compounds A. mexicana (seeds)
P. perniciosum (stem-bark)
Hexane Ethyl acetate Acetone Hexane Ethyl acetate Acetone Alkaloids + − − − − − Cumarinas − − − + + + Tanins + + + + + + Sterols/terpens + + + + + + Flavonoids − − − + − − Glycosides cardoitonics + + + + + + Sterols + + + + + + Saponins − − − − − − - -: Not detected; +: Detected.
4. Discussion
Hundreds of plant species have been tested for their toxicities against mosquitoes with a recent review published by Rehman[21 and 28].
Plant extracts have not yet been used to control dengue vectors in the
field, and are not currently under consideration for inclusion into
IVMP, but many laboratory trials have been conducted with a view to
identify promising candidates.
As
expected, there was a variation in the toxicity against the larvae of
the mosquitoes because the compounds extracted using different solvents
and from different parts of plants tested[29]. In the present study, seeds of A. mexicana and stem-bark of P. perniciosum using acetone and hexane as solvents showed excellent larvicidal properties (LC50 ranged from 60 μg/mL-110 μg/mL) within the first 24 h post-exposure. A range of LC50 values between 30.47 μg/mL and 13.58 μg/mL has been observed by Sakthivadivel when using petroleum ether extract from seeds of A. mexicana at 24 h[ 13 and 19]. Similarly, low LC50 values (LC50 ranged from 20 μg/mL-50 μg/mL) were observed in our study when using hexane as solvent in both seeds of A. mexicana and stem-bark of P. perniciosum, respectively at 48 h post-exposure.
It
can be pointed out that there was no association between the larvicidal
activity and the polarity of the solvent used in the extraction.
However, our preliminary phytochemical analysis of the most toxic
extracts (A. mexicana seeds and P. perniciosum stem-bark) against Ae. aegypti larvae suggests that the bioactive compounds (alkaloids in A. mexicana and coumarins and flavonoids in P. perniciosum) present in these two plants are promising candidates for the control of Ae. aegypti
larvae. Although further evidence is needed, the results of
phytochemical analysis showed that the metabolites varied based on the
solvent used for the extraction. The toxic effect of P. perniciosum
stem-bark can be attributed to the presence of coumarins. Previous
authors have demonstrated high toxicity of this compound against the
larvae of Ae. aegypti[ 30 and 31]. In addition, flavonoids have also been recognized to have activity as natural insecticide against Ae. aegypti[ 31, 32 and 33]. Moreover, the major metabolites reported for seeds of A. mexicana are berberine and protopine, both toxic alkaloids[ 31 and 34].
It
would be gratifying to determine the effect of the plant extracts on
non-target organisms. These could be done on native aquatic fauna and
other biological control of natural enemies or mammals that have access
to the water into which the botanical larvicides are to be placed. Such
studies of the effect of A. mexicana seeds and P. perniciosum stem-bark extracts on non-target organisms are currently underway.
In conclusion, two of five species of plants here studied, A. mexicana and P. perniciosum, may be good candidates to be employed in control programs against the dengue vector, Ae. aegypti,
as they are highly toxic to the larvae and are abundant as weeds in the
Mexican territory and accessible to most inhabitants in the endemic
areas[ 35 and 36].
Conflict of interest statement
We declare that we have no conflict of interest.
Comments
Background
Dengue fever is an important emerging infectious viral disease transmitted by Aedes
mosquitoes. The control of this disease relies on the use of chemical
insecticides to reduce human-mosquito contact. However, these mosquito
vectors are developing resistance to major insecticides used for their
control.
Research frontiers
This study showed that A. mexicana and P. perniciosum, had toxic effect on Aedes
mosquitoes larvae and may therefore be employed in control programs
against these dengue vectors. Due to the availability of these plants in
Mexico, their use by the programme to control mosquito larvae may be
easy and sustainable.
Related reports
Similar studies in Mexico and elsewhere also demonstrated high toxicity of A. mexicana and P. perniciosum against the larvae of Ae. aegypti. However, such studies were conducted in different settings although they used almost similar experimental designs.
Innovations and breakthroughs
A. mexicana and P. perniciosum
are known to be toxic against mosquitoes larvae, however, this study
demonstrated the toxicity from different parts of the plant using
several solvents.
Applications
These
plants can be used in the control of mosquito vectors in cheap and
sustainable manner. Their availability in Mexico, makes the use by
mosquito control programme to be easy. They may further be used to
manage insecticide resistance.
Peer review
This is a well written paper which presents valuable information that A. mexicana and P. perniciosum, have toxic effect on Aedes
mosquitoes larvae and they may be employed in control programs against
these dengue vectors. Their toxicity against the larvae of the
mosquitoes varied according to the solvent used.
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- PEER REVIEW
- Peer reviewer
- Dr Bilali Kabula, Senior Research Scientist, National Institute for Medical Research (NIMR), Tanzania.
- Tel:
+255 783021213 - E-mail: bika72@yahoo.com
- Comments
- This is a well written paper which presents valuable information that A. mexicana and P. perniciosum, have toxic effect on Aedes mosquitoes larvae and they may be employed in control programs against these dengue vectors. Their toxicity against the larvae of the mosquitoes varied according to the solvent used.
- Details on Page 290
- Available online 13 Mar 2015
- Corresponding
author: Rosario Ruiz-Guerrero, Instituto Politécnico Nacional- CIITEC,
Cerrada de Cecati S/N. Col. Santa Catarina Azcapotzalco, D. F., CP
02250, México. Tel: + 52 55 5729 6000 Ext. 68325
Copyright © 2015 Hainan Medical University. Production and hosting by Elsevier (Singapore) Pte Ltd.
