Peruvian Journal of Agronomy 3(3): 126–133 (2019) Received for publication: 01 September 2019

ISSN: 2616–4477 (Versión electrónica) Accepted for publication: 20 September 2019

DOI: http://dx.doi.org/10.21704/pja.v3i3.1206
http://revistas.lamolina.edu.pe/index.php/jpagronomy/index
© Universidad Nacional Agraria La Molina, Lima - Perú

Peruvian Botanical Biopesticides for Sustainable Development and Protection of the

Environment
Biopesticidas botánicos de origen peruano para el desarrollo sostenible y la protección del ambiente

Bracho-Pérez, J. (1); Tacza-Valverde, I. (1); Vásquez-Castro, J. (2)*

*Corresponding author: [email protected]

Abstract

Daphnia magna is proposed as a bioindicator to establish the minimum concentration capable of controlling pests
before performing toxicity tests. This study uses the proposed pest control extracts of two Peruvian species, Clibadium
peruvianum Poepp. (seeds) and Petiveria alliacea L. (leaves). The toxicological effects of the plant extracts were
evaluated with D. magna, using five neonates over a period of 24–48 h. A lack of mobility or the absence of heart rhythm
for 15 s under a stereomicroscope was considered to indicate mortality. Organic extracts were discarded due to their
higher toxicity when compared with the aqueous extracts of C. peruvianum and P. alliacea, which had LC50 = 460.74
mg/L and LC50 = 711.18 mg L−1 at a concentration of 10 mg L−1, respectively. Using this Daphnia-safe concentration,
toxicity tests were performed on the third instar larvae of Musca domestica (housefly). Higher activity was observed
with an aqueous extract of seeds of C. peruvianum and a leaf aqueous extract of P. alliacea, showing 58.33% and 56.7%
mortality against M. domestica, respectively. Both extracts induced abnormal changes in the development of the housefly,
causing deformation, burns, and dehydration of tissues in the larvae. It is evident that using D. magna as a preliminary
toxicological test allows the determination of concentrations that are safer to use while maintaining the activity of the
extracts as a botanical biopesticide, thus posing the lowest risk to the environment, ecosystems, their species, and human
health.

Key words: Botanical biopesticides, Clibadium peruvianum, Daphnia magna, housefly, Musca domestica, Petiveria
alliacea.

Resumen

Se propuso el uso de Daphnia magna como bioindicador para establecer la concentración mínima capaz de controlar
las plagas antes de realizar pruebas de toxicidad. Este estudio consistió en el uso de dos especies peruanas, Clibadium
peruvianum Poepp (semillas) y Petiveria alliacea L. (hojas). Los efectos toxicológicos de los extractos de plantas se
evaluaron con D. magna, utilizando cinco neonatos en un período de 24–48 h. La falta de movilidad o ausencia de
ritmo cardíaco durante 15 s bajo microscopio estereoscópico se utilizó como un indicador de mortalidad. Los extractos
orgánicos se descartaron debido a su mayor toxicidad en comparación con los extractos acuosos de C. peruvianum y
P. alliacea, que tenían CL50 = 460.74 mg L−1 y CL50 = 711.18 mg L−1 a 10 mg L−1 de concentración, respectivamente.
Usando esta concentración segura, se realizaron pruebas de toxicidad en larvas de Musca domestica de tercer estadio. Se
observó una mayor actividad con extracto acuoso de semilla de C. peruvianum 58,33% y extracto acuoso de hoja de P.
alliacea 56,7% de mortalidad contra M. domestica. Ambos extractos indujeron cambios anormales en el desarrollo de la
mosca común, causando deformación, quemaduras y deshidratación de los tejidos de las larvas. Es evidente que el uso de
D. magna como prueba toxicológica preliminar permite el uso de concentraciones más seguras, manteniendo la actividad
de los extractos como un bioplaguicida botánico y presentando el menor riesgo para el medio ambiente, los ecosistemas,
sus especies y la atención de la salud humana.

Palabras clave: Bioplaguicida botánico, Clibadium peruvianum, Daphnia magna, mosca común, Musca domestica,
Petiveria alliacea.
Introduction rear in the laboratory, and has advantages such as short
life cycle and high susceptibility to pesticides and other
One of the organisms most used in toxicological studies environmental pollutants, it has become a worldwide
with pesticides is the crustacean Daphnia magna Straus reference species for this type of study (Mansour et al.,
(Cladocera: Daphniidae). Because D. magna is easy to 2015; Qi et al., 2018).

1
Universidad Nacional Tecnológica de Lima Sur. Facultad de Ingeniería y Gestión. Campus - Sector 3 Grupo 1A 03 - Cercado (Av. Central y Av.
Bolívar) - Villa El Salvador, Lima 42, Perú
2
Universidad Nacional Agraria La Molina (UNALM), Departamento de Entomología, Facultad de Agronomía, Av. La Molina s/n, Lima 12, Perú
 Bracho-Pérez, J.; Tacza-Valverde, I.; Vásquez-Castro, J.
Peruvian Journal of Agronomy 3(3): 126–133 (2019)

The housefly, Musca domestica L. (Diptera: Muscidae), Kim, & Musah, 2002; Williams, Rosner, Levy, & Barton,
is considered a vector of viruses, bacteria, and protozoa 2007; Luz et al., 2016).
that cause many diseases in humans and other mammals
and has become an important public health concern (Urzúa However, some studies have shown that this plant also
et al., 2010a; Sripongpun, 2008). Management of M. possesses great potential in controlling pests and that it is
domestica has been carried out through the application not necessary to depredate (uproot or destroy the plants)
and extensive use of synthetic insecticides, which in turn it for this purpose, since an effective preparation does not
have caused serious environmental problems, such as the require the use of the plant’s roots. In this sense, several
development of pest resistance, ecological damage, and studies of leaf and stem extracts have demonstrated
irreversible damage to human health (Vásquez, de Baptista, their ability to control pests, such as via acaricidal and
Trevizan, & Gadanha, 2008; Ahmed, Zain, & Irfanullah, insecticidal action against larvae and adults of the cattle
2004; Nivsarkar, Cherian, & Padh, 2001; Kristensen & tick Rhipicephalus (Boophilus) and whitefly (Bemisia
Jespersen, 2003; Taşkin, Kence, & Göçmen, 2004; Khalaf, tabaci Genn.), respectively (Rosado et al., 2010; Cruz,
Hussein, & Shoukry, 2009). Gamboa, Borges, & Ruiz, 2013).

A vast number of studies conducted worldwide have This study aimed to evaluate the toxicological effects
focused on the insect-control uses of insect growth regulators of hexane, ethanol, and aqueous extracts of C. peruvianum
(IGRs) and plant secondary metabolites (Céspedes, Salazar, and P. alliacea on D. magna in order to determine the
Martínez, & Aranda, 2005; Torres et al., 2003; Magalhães extract with the lowest mortality risk and then to carry out
et al., 2010; Pohlit, Rezende, Lopes, Lopes, & Neto, 2011; toxicity tests on the third instar larvae of M. domestica.
Urzúa et al., 2010b). Plant-derived compounds that are
rich sources of bioactive chemicals provide promising
alternatives to the current use of chemical pesticides for Materials and Methods
insect control (Khalaf et al., 2009). The Asteraceae family
constitutes an important source of secondary metabolites, Material
such as monoterpenes, sesquiterpenes, sesquiterpene
Two Peruvian species, C. peruvianum Poepp. (seeds)
lactones, diterpenes, triterpenes, flavonoids, coumarins,
and P. alliacea L. (leaves), were collected from both
polyacetylenes, and benzofurans (Raal et al., 2011;
Tingo María City, Rupa-Rupa District, situated in the
Alvarenga, Ferreira, Emerenciano & Cabrol-Bass, 2001;
Huánuco department (09°24´ S, 75°58´ W), and Castillo
Ferreira, Brant, Alvarenga, & Emerenciano, 2005).
district, Leoncio Prado Province, located in the Huánuco
The Asteraceae family is widely distributed in Perú, department (09°16´ S, 76°00´ W), in August 2016. The
where there are almost 250 genera and 1590 species Weberbauer Herbarium, Universidad Nacional Agraria La
(Beltrán et al., 2006). One species of this family, Clibadium Molina, then confirmed the identification of both plants
peruvianum Poepp. ex DC. (Asterales: Asteraceae), is when voucher specimens were deposited there.
known as “huaca” in the rainforest of Perú. Rainforest
The plants were dried in an oven at 40 °C for 48 h
natives have long used leaves from C. peruvianum as
and pulverized, and then 10 g of each dried plant material
a fishing aid (Arriagada, 1995; Arriagada, 2003; Pérez,
part was extracted with ethanol, hexane, or distilled water
Muñoz, Noyola, & García, 2006; Bohm & Stuessy, 1981;
using an ultrasound bath at 48 °C for 2 h. The extracts were
Bohm & Stuessy, 1985; Czerson, Bohlmann, Stuessy, &
filtered, and the organic extracts were dried on a rotary
Fischer, 1979). The use of piscicidal extracts in fishing
evaporator under reduced pressure at 38 °C and dissolved
is considered favorable because these extracts are not
in propylene glycol and distilled water.
persistent chemicals. Furthermore, they may represent a
good pest control alternative that avoids the use of synthetic Preparation of extracts
and non-biodegradable products. For instance, rotenone is
a piscicide that is also currently used as a botanical control Dry ground seeds (3 × 10 g) and leaves (3 × 10 g) were
in agriculture (Harada, 1996; Gabriel & Okey, 2009). extracted with 100 mL of 96% ethanol, hexane, or distilled
water by ultrasonication at 48 °C for 2 h and then filtered.
Petiveria alliacea L. (Phytolaccaceae) is a perennial The organic extracts were dried on a rotary evaporator
herbaceous plant native to the Amazon rainforest and under reduced pressure at 38 °C and dissolved in propylene
widely distributed in other areas, including tropical and glycol.
Central America, Africa, Sri Lanka, and the southeastern
United States. It is known as “mucura.” Preparations Test organism
of this plant have been widely used in the traditional
medicine of South and Central America to treat many Experiments were conducted with strains of D. magna.
disorders. Reports indicate that it has anti-inflammatory, Cultures of D. magna were maintained at a temperature
antimicrobial, anticancer, and stimulant effects, among of 20 °C ± 2 °C in water at pH 7.14, with conductivity of
others. Most studies of this plant have focused on its roots 10 µS cm−1, alkalinity of 93.5 mg CaCO3 L−1, and total
and on medical–pharmacological applications (Kubec, hardness of 45.6 mg CaCO3 L−1. The D. magna were fed

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September - December 2019

with the algal species Pseudokirchneriella subcapitata through a one-way analysis of variance (ANOVA), with
according to ISO 6341 (2012), OECD 202 (2004), and a significance level of p = 0.05 after transformation of the
USEPA 2021.0 (2002) methods. data to square root of the arcsine to ensure a homogeneity
of variances, using IBM SPSS Statistics (Zar, 1996).
Acute ecotoxicity

A reference test with sodium chloride (NaCl) was also

conducted to test the sensitivity of D. magna (24-h old). Results and Discussion
The static toxicity test was performed in plastic vessels
containing 4 mL of test medium. For each concentration, Acute ecotoxicity
five neonates were exposed to five test concentrations of Clibadium peruvianum Poepp. (huaca)
dried extracts per liter from 1% (1000 mg L−1) to 0.01 mg
L−1 (10 mg L−1), without feeding during the test, for 24 and The seeds of C. peruvianum were selected as the organ
48 h. For each concentration, three replicates were used. of interest for this plant, based on the study of Pérez et al.
Plastic vessels were incubated in darkness at 20°C ± 2°C. (2012), which demonstrated that the alcoholic extract of
The immobilization of treated organisms or the absence of its seeds had higher insecticidal activity compared with the
heart rhythm for 15 s under a stereomicroscope was used other organs of the plant.
to indicate mortality.
Studies of ecotoxicity using D. magna have
Low environmental risk decision demonstrated that at 48 h of exposure, the lethal average
concentration reached its highest value (LC50 = 460.74
Taking into account the results obtained from the acute mg L−1) for a concentration of 10 mg L−1 (0.01%),
ecotoxicity test, the vegetable extracts and respective demonstrating that the aqueous extract of the seed
concentrations that exhibited toxicity against D. magna possesses a minor toxic effect, unlike the more powerful
were discarded. The remaining extracts were used to effects of the alcoholic extracts (LC50 = 164.36 mg L−1)
carry out the control bioassays for the selected pest, M. and hexanic extracts (LC50 = 371.47 mg L−1). As a result,
domestica. the aqueous extract of the C. peruvianum became the
Residual contact toxicity only extract considered for further studies of biopesticide
activity and development of future formulations for pest
Bioassays were performed in order to demonstrate the control (Table 1).
insecticidal activity of each extract against M. domestica.
For this purpose, each of the selected extracts from both Petiveria alliacea L. (mucura)
plant types was mixed with an increasing amount of The acute toxicity results of the extracts drawn from the
distilled water to obtain four solutions with dilutions leaves of the mucura plant demonstrated that the aqueous
ranging from 100% (undiluted) to 10% (100, 80, 50, and extract also exhibited the highest lethal concentration (LC50
10). An aliquot of 1 mL of each extract was applied to = 711.18 mg L−1) compared with those of the alcoholic
each of four petri dishes. In each petri dish, the applied extract (LC50 = 255.50 mg L−1) and hexanic extract (LC50
liquid was spread over the entire treatment area to form a = 65.36 mg L−1); the hexanic extract showed mortality in a
thin film, which was evaporated under the Environmental concentration range of 10-100 mg L−1, equivalent to 0.1%-
Chemistry Laboratory conditions (25 °C ± 2 °C and 65% ± 0.01% (Table 2).
2% relative humidity [RH]) for 10 min. Once the treatment
area was dry, 40 third instar larvae of M. domestica were The results obtained indicate that the aqueous extract
placed in each petri dish, and the dishes were covered and of the P. alliacea has the lowest acute toxicity, even lower
sealed with Parafilm. The same process was performed than the aqueous extract of C. peruvianum. However,
with distilled water as a control. Four replicates per both aqueous extracts must be considered since they both
treatment were used in the experiment. For evaluation, generate the lowest toxic effect to M. daphnia, which is the
the adults that emerged after 15 days were counted (Pérez, selected bioindicator.
Bracho, & Vásquez, 2012).
This implies that the other extracts should no longer be
Data analysis considered in order to reduce future environmental toxicity
risks, and 10 mg L−1 (0.01%) of dried extract per liter was
Taking into account the data related to acute ecotoxicity, the most appropriate concentration for the development of
the LC50 (concentration lethal to 50% of the population) biopesticide activity studies.
was determined by applying the probit analysis as part of
an appropriate statistical program (IBM SPSS Statistics Insecticidal activity
22). Student’s t-test was used to examine the hypothesis
of possible differences between the mean results from the The results of the insecticidal activity reveal that both the
two treatments. The efficacy of treatments (percentage aqueous extracts prepared caused mortality higher than
of mortality at different concentrations) was evaluated 50%, specifically, 58.33% for C. peruvianum (huaca) and

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Peruvian Journal of Agronomy 3(3): 126–133 (2019)

Table 1. Toxic effect of Clibadium peruvianum Poepp. (huaca) extracts in terms of mortality of Daphnia magna during 24 and 48 h
of exposure.
Number of 24 h 48 h
Concentration individuals
Extract (mg L−1)1 of D. magna Mortality (%) Casualties Mortality (%)
Casualties
10 15 0 0.00 1 6.67
100 15 1 6.67 3 20.00
500 15 7 46.67 9 60.00
Aqueous
Clibadium peruvianum Poepp. (huaca)

1000 15 8 53.33 10 66.67

10000 15 15 100.00 15 100.00
2
LC50 674.93 460.74
10 15 3 20.00 4 26.67
100 15 5 33.33 7 46.67
500 15 11 73.33 14 93.33
Ethanolic
1000 15 14 93.33 15 100.00
10000 15 15 100.00 15 100.00
LC50 295.84 164.35
10 15 2 13.33 5 33.33
100 15 4 26.67 8 53.33
500 15 6 40.00 10 66.67
Hexanic
1000 15 9 60.00 13 86.67
10000 15 15 100.00 15 100.00
LC50 942.24 371.47
mg L−1 = mg of dry aqueous extract per liter, 2LC50 is the concentration of C. peruvianum extracts that kill 50% of the test population of Daphnia
1

magna within a designated period.

Table 2. Toxic effect of Petiveria alliacea L. (mucura) extracts in terms of mortality of Daphnia magna during 24 and 48 h of
exposure.
Number of 24 h 48 h
Concentration individuals
Extract (mg L−1)1 of D. magna Mortality (%) Casualties Mortality (%)
Casualties
10 15 0 0.00 0 0.00
100 15 0 0.00 0 0.00
500 15 0 0.00 5 33.33
Aqueous
1000 15 8 53.33 10 66.67
10000 15 15 100.00 15 100.00
Petiveria alliacea L. (mucura)

LC50
2
973.45 711.18
10 15 0 0.00 1 6.67
100 15 0 0.00 4 26.67
Ethanolic 500 15 9 60.00 10 66.67
1000 15 14 93.33 15 100.00
10000 15 15 100.00 15 100.00
LC50 446.09 255.50
10 15 3 20.00 5 33.33
100 15 9 60.00 11 73.33
500 15 13 86.67 13 86.67
Hexanic
1000 15 15 100.00 15 100.00
10000 15 15 100.00 15 100.00
LC50 104.78 65.35
mg L = mg of dry aqueous extract per liter, LC50 is the concentration of P. alliacea extracts that kills 50% of the test population of  Daphnia
1 −1 2

magna within a designated period.

56.70% for P. alliacea (mucura). This indicates that huaca the means of the two determinations is not confirmed.
has a greater tendency to maintain a higher insecticidal The level of significance (p) of this test is lower than that
effect (Table 3). of Levene’s statistic, F = 0.05, for huaca compared with
mucura, obtaining p = 0.262 and p = 0.167, respectively.
However, the means of observed mortality are not This means that the equality of the means was rejected.
homogeneous. By applying Student’s t-test, it can be Therefore, the means obtained must be transformed by
determined that the hypothesis of the difference between applying the square root of the arccosine and then by

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September - December 2019

Table 3. Mortality percentages for the third instar larvae of related to the effect of inhibiting the fly growth process by
Musca domestica exposed to aqueous extracts of C. peruvianum substances known as IGRs, a consideration that has been
(huaca) and P. alliacea (mucura).
supported by other authors (Khalaf et al., 2009; Youssef,
Mortality (%) 1997; Wang, Li, & Lei, 2005).
Concentration
(mg L−1) C. peruvianum P. alliacea extract On the other hand, because the insecticidal activity
extract
considered in this study was found in extracts of the seeds
10.00 58.33 ± 0.10 56.70 ± 0.10
and leaves, it is not necessary to kill the plants to obtain
8.00 43.33 ± 0.10 35.00 ± 0.10 the needed raw material for these insecticides. The plants
6.00 20.00 ± 0.10 25.00 ± 0.10 can continue to grow, thus preserving the species. It is
4.00 16.66 ± 0.10 11.00 ± 0.10 very remarkable that the dilution chosen for the aqueous
2.00 10.00 ± 0.10 3.33 ± 0.10 extract of C. peruvianum showed a pattern of biological
activity similar to previous studies on this species, but
at a much lower concentration. Both aqueous extracts
caused deformations in the larvae, but to a lower extent.
It is evident that using a bioindicator, such as D. magna,
as part of the preliminary toxicological tests allows the
choosing of the safest concentrations of a biopesticide
while maintaining biological activity.

Finally, emphasis should be placed on the importance

of continuing the chemical composition studies to
establish the relationship between chemical composition
and biological activity. This will enable the design of
increasingly environment-friendly formulations of pest
control, capable of protecting pest ecosystems, the species
that inhabit them, and human health.

Conclusions
Figure 1. Mortality curve for Musca domestica larvae, where
Mortality(T) indicates the percentage of mortality transformed
according to Zar (1996), using the data presented in Table 3 Daphnia magna can be used as a bioindicator to determine
versus concentration of C. peruvianum (huaca) and P. alliacea the minimum concentration capable of controlling pests
(mucura) extracts. before performing toxicity tests on pest species.
ANOVA, obtaining a graphical description of results in
Toxicological evaluation with D. magna demonstrated
both toxicity studies on the housefly, as presented in Figure
that alcoholic and hexanic extracts of C. peruvianum and
1 (Zar, 1996).
P. alliacea are more toxic to D. magna than the aqueous
Toxicity results allow the inference that although the extract, evidencing the greater environmental impact of
extract of huaca leaves has, in general, greater toxicity, the organic extracts.
behaviors of both extracts are similar, causing mortality
The aqueous extracts of C. peruvianum and P. alliacea
higher than 50% to the third instar larvae of M. domestica
are environment-friendly, as measured by their relatively
at a concentration of 10 mg L−1 of dried extract. Both
low toxicity to D. magna, and the appropriate extract that
extracts induced abnormal changes in the development of
should be used for the control of M. domestica.
the housefly, causing deformation, burns, and dehydration
of tissues in the larvae, similar to the results of the study of Finally, the toxicity tests carried out on Musca
Pérez et al. (2012). domestica demonstrated that both aqueous extracts of
C. peruvianum and P. alliacea on D. magna have great
The morphological aberrations obtained are similar to
potential for insect pest control.
those described on Synthesiomyia nudiseta Wulp larvae
(Khalaf et al., 2009; Khalil, Assae, Abo El Mahasen, &
Mahmoud, 2010) and on M. domestica (Elkattan, Ahmed,
Elbermaway, & Abdel-Gawad, 2011), causing a 24-h References
delay in the development of the larvae treated with an
Ahmed, S., Abdin, Z., & Irfan, M. (2004). Evaluation of
extract of seeds in comparison to other treatments. The
some pyrethroids for the control of house fly, Musca
effect of delay during the transformation from larvae to
domestica L. International Journal of Agriculture
pupae was also described by other authors (Elkattan et al.,
and Biology, 6(5), 806–809.
2011; Ande, 2001; Assar & Abo-Shaeshae, 2004). This
unusual extension of the larval growth period could be Alvarenga, S. A., Ferreira, M. J., Emerenciano, V. P., &

130
 Bracho-Pérez, J.; Tacza-Valverde, I.; Vásquez-Castro, J.
Peruvian Journal of Agronomy 3(3): 126–133 (2019)

Cabrol-Bass, D. (2001). Chemosystematic studies 18(2), 257–260. https://doi.org/10.1016/0031-

of natural compounds isolated from Asteraceae: 9422(79)80065-5
characterization of tribes by principal component
analysis. Chemometrics and Intelligent Laboratory Elkattan, N. A., Ahmed, K. S., Elbermaway, S. M., &
Systems, 56, 27–37. https://doi.org/10.1016/S0169- Abdel-Gawad, R. M. (2011). Effect of some
7439(01)00103-4 botanical materials on certain biological aspects
of the housefly, Musca domestica L. The Egyptian
Ande, A. T. (2001). Biological activities of some plant Journal of Hospital Medicine. 42, 33–48.
materials against the housefly-Musca domestica.
Journal of the Nigerian Society for Experimental Ferreira, M. J., Brant, A. J., Alvarenga, S. A., &
Biology, 1, 293–296. Emerenciano, V. P. (2005). Neural networks
in chemosystematic studies of Asteraceae: A
Arriagada, J. (1995). Notes on Economics plants. Economic classification based on a dichotomic approach.
Botany, 49, 328–332. Chemistry & Biodiversity. 2, 633–644. https://doi.
org/10.1002/cbdv.200590040
Arriagada, J. (2003). Revision of the genus Clibadium
(Asteraceae, Heliantheae). Brittonia, 55(3), 245– Gabriel, U., & Okey, I. (2009). Effect of aqueous leaf
301. https://doi.org/10.1663/0007-196X(2003)055 extracts of Lepidagathis alopecuroides on the
[0245:ROTGCA]2.0.CO;2 behaviours and mortality of hybrid Catfish
(Heterobranchus bidorsalis X Clarias gariepinus)
Assar, A. A., & Abo-Shaeshae, A. A. (2004). Effect of two Fingerlings. Research Journal of Applied Science,
insect growth regulators, methoxyfenozide and Engineering and Technology, 1(3), 116–120.
pyriproxyfen on the housefly, Musca domestica
vicina (Diptera: Muscidae). Journal of the Egyptian- Harada, J. (1992). Allelopathy and fish toxicity of aquatic
German Society of Zoology, 44,19–42. weeds. International Symposium on Biological
Control and Integrated Management of Paddy
Beltrán, H., Granda, A., León, B., Sagastegui, A., Sánchez, and Aquatic Weeds in Asia, 305. 19–25 October.
I., & Zapata, M. (2006). Asteraceae endémicas del Tsukuba, Japan.
Perú. Revista Peruana de Biología, 13(2), 64–164.
https//doi.org: 10.15381/rpb.v13i2.1807. ISO International Organization for Standardization.
(2012). Water quality. Determination of the
Bohm, B. A., & Stuessy, T. F. (1981). Flavonol inhibition of the mobility of Daphnia magna
derivatives of the genus Clibadium (Compositae). Straus (Cladocera, Crustacea). Acute toxicity test
Phytochemistry, 20(5), 1053–1055. https://doi. (ISO 6341). Retrieved from https://www.iso.org/
org/10.1016/0031-9422(81)83025-7 standard/54614.html
Bohm, B. A., & Stuessy, T. F. (1985). Further studies Khalaf, A. A., Hussein, K. T., & Shoukry, K. K. (2009).
of flavonols of Clibadium (Compositae). Biocidal activity of two botanical volatile oils
Phytochemistry, 24(9), 2134–2136. https://doi. against the larvae of Synthesiomyia nudiseta (Wulp)
org/10.1016/S0031-9422(00)83144-1 (Diptera: Muscidae). Egyptian Academic Journal of
Céspedes, C. L., Salazar, J. R., Martínez, M., & Aranda, Biological Sciences, 2, 89–101.
E. (2005). Insect growth regulatory effects of Khalil, M. S., Assae, A. A., Abo El Mahasen, M. M., &
some extracts and sterols from Myrtillocactus Mahmoud, S. H. (2010). Morphological effects of
geometrizans (Cactaceae) against Spodoptera some insect growth regulators on Musca domestica
frugiperda and Tenebrio molitor. Phytochemistry, (Diptera, Muscidae). Egyptian Academic Journal
66(20), 2481–2493. https://doi.org/10.1016/j. of Biological Sciences, 2, 29–36. https://doi.
phytochem.2005.07.010 org/10.21608/EAJBSF.2010.17445
Cruz, E. A., Gamboa, A. M., Borges, A. R., & Ruiz, S. Kristensen, M., & Jespersen, J. B. (2003). Larvicide
E. (2013). Insecticidal effect of plant extracts resistance in Musca domestica (Diptera: Muscidae)
on immature whitefly Bemisia tabaci Genn. population in Denmark and establishment of
(Hemiptera: Aleyroideae). Electronic Journal of resistant laboratory strains. Journal of Economic
Biotechnology, 16(1), 1–9. DOI: 10.2225/vol16- Entomology, 96, 1300–1306. https://doi.
issue1-fulltext-6 Retrieved from http://www. org/10.1093/jee/96.4.1300
ejbiotechnology.info/index.php/ejbiotechnology/
article/view/v16n1-6 Kubec, R., Kim, S., & Musah, R. A. (2002). S-Substituted
cysteine derivatives and thiosulfinate formation
Czerson, H., Bohlmann, F., Stuessy, F., & Fischer, H. in Petiveria alliacea-part II. Phytochemistry
(1979). Sesquiterpenoid and acetylenic constituents 61(6), 675–680. https://doi.org/10.1016/S0031-
of seven Clibadium species. Phytochemistry, 9422(02)00328-X

131
 Peruvian Botanical Biopesticides for Sustainable Development and Protection of the Environment

September - December 2019

Luz, D. A., Pinheiro, A. M., Silva, M. L., Monteiro, M. of essential oils in some Asteraceae species.
C., Prediger, R. D., Ferraz Maia, C. S., & Fontes- Proceedings of the Estonian Academy of Sciences,
Júnior, E. A. (2016). Ethnobotany, phytochemistry 60, 55–63.
and neuropharmacological effects of Petiveria
alliacea L. (Phytolaccaceae): A review. Journal Rosado, A. J., Aguilar, C. A., Rodríguez, V. R., Borges,
of Ethnopharmacology. 185, 182–201. https://doi. A. R., García, V. Z., & Méndez, G. M. (2010).
org/10.1016/j.jep.2016.02.053 Acaricidal activity of extracts from Petiveria
alliacea (Phytolaccaceae) against the cattle tick,
Magalhães, L. A., Lima, M., Marques, M. O., Facanali, Rhipicephalus (Boophilus) microplus (Acari:
R., Pinto, A. C., & Tadei, W. P. (2010). Chemical Ixodidae). Veterinary Parasitology, 168(3–4), 299–
composition and larvicidal activity against Aedes 303.
aegypti larvae of essential oils from four Guarea
species. Molecules, 15, 5734–5741. https://doi. Sripongpun, G. (2008). Contact toxicity of the crude
org/10.3390/molecules15085734 extract of Chinese star anise fruits to house fly
larvae and their development. Songklanakarin
Mansour, S. A., Abdel-Hamid, A. A., Ibrahim, A. W., Journal of Science and Technology, 30(5), 667–
Mahmoud, N. H., & Moselhy, W. A. (2015). 672. Retrieved from http://rdo.psu.ac.th/sjst/journ
Toxicity of some pesticides, heavy metals and their al/30-5/0125-3395-30-5-667-672.pdf
mixtures to Vibrio fischeri bacteria and Daphnia
magna: Comparative Study. Journal of Biology and Taşkin, V., Kence, M., & Göçmen, B. (2004).
Life Science, 6, 221–240. http://dx.doi.org/10.5296/ Determination of malathion and diazinon resistance
jbls.v6i2.8174 by sequencing the MdαE7 gene from Guatemala,
Colombia, Manhattan, and Thailand housefly
Nivsarkar, M., Cherian, B., & Padh, H. (2001). Alpha- (Musca domestica L.) Strains. Russian Journal of
terthienyl: A plant-derived new generation Genetics, 40, 377–380.
insecticide. Current Science, 81, 667–672.
Torres, P., Ávila, J. G., Romo de Vivar, A., García, A. M.,
OECD (2004). Test No. 202: Daphnia sp. Acute Marín, J. C., Aranda, E., Céspedes, C. L. (2003).
Immobilisation Test, OECD Guidelines for the Antioxidant and insect growth regulatory activities
Testing of Chemicals, Section 2, OECD Publishing, of stilbenes and extracts from Yucca periculosa.
Paris. https://doi.org/10.1787/9789264069947-en Phytochemistry, 64(2), 463–473. https://doi.
org/10.1016/S0031-9422(03)00348-0
Pérez, G., Bracho, J. C., & Vásquez, J. A. (2012). Efeito
inseticida de Clibadium peruvianum sobre Musca Urzúa, A., Santander, R., Echeverría, J., Cabezas, N.,
domestica, e a sua composição química. XXIV Palacios, S. M., & Rossi, Y. (2010a). Insecticide
Congresso Brasileiro de Entomología, 16. Curitiba- properties of the essential oils from Haplopappus
Paraná, 2012. Brasil. foliosus and Bahia ambrosoides against the
housefly, Musca domestica L. Journal of the
Pérez, M. C., Muñoz, V. A., Noyola, A., & García, F. Chilean Chemical Society, 55, 392–395. http://
(2006). Essential oil and phototoxic compounds dx.doi.org/10.4067/S0717-97072010000300026
in Clibadium surinamense L. and Montanoa
grandiflora D.C. (Asteraceae). Phyton, Urzúa, A., Santander, R., Echeverría, J., Villalobos, C.,
International Journal of Experimental Botany, 75, Palacios, S. M., & Rossi, Y. (2010b). Insecticidal
145–150. properties of Peumus boldus Mol. essential oil on
the house fly, Musca domestica. Latin American
Pohlit, A. M., Rezende, A. R., Lopes, E. L., Lopes, N.
and Caribbean Bulletin of Medicinal and Aromatic
P., & Neto, V. F. (2011). Plant extracts, isolated
Plants, 9, 465–469.
phytochemicals, and plant-derived agents, which
are lethal to arthropod vectors of Human tropical USEPA. (2002). Method 2021.0: Daphnia pulex and D.
diseases: a review. Planta Medica, 77, 618–630. magna Acute Toxicity Tests with Effluents and
https://doi.org/10.1055/s-0030-1270949 Receiving Waters in: Methods for measuring the
acute toxicity of effluents and receiving waters to
Qi, S., Wang, D., Zhu, L., Teng, M., Wang, C., Xue, X.,
freshwater and marine organisms. Fifth ed., EPA
& Wu, L. (2018). Neonicotinoid insecticides
Volume 821-R-02-012.
imidacloprid, guadipyr, and cycloxaprid induce
acute oxidative stress in Daphnia magna.
Ecotoxicology Environmental Safety, 148, 352– Vásquez, J. A., de Baptista, G. C., Trevizan, L. R.,
358. https://doi.org/10.1016/j.ecoenv.2017.10.042 & Gadanha, C. D. (2008). Fenitrothion and
esfenvalerate stability during corn and wheat sample
Raal, A., Kaur, H., Orav, A., Arak, E., Kailas, T., & processing. Scientia Agricola, 65, 157–160. http://
Muurisepp, M. (2011). Content and composition dx.doi.org/10.1590/S0103-90162008000200008

132 b
 Bracho-Pérez, J.; Tacza-Valverde, I.; Vásquez-Castro, J.
Peruvian Journal of Agronomy 3(3): 126–133 (2019)

Williams, L. A., Rosner, H., Levy, H. G., & Barton, E. N.

(2007). A critical review of the therapeutic potential
of dibenzyl trisulphide isolated from Petiveria
alliacea L. (guinea hen weed, anamu). West Indian
medical Journal, 56(1), 17–21.

Wang, J., Li, Y., & Lei, CL. (2005). The repellency and
fumigant activity of Artemisia vulgaris essential
oil to Musca Domestica Vicina. Chinese Bulletin of
Entomology, 42(1), 51–53.

Youssef, N. S. (1997). Toxic and synergistic properties

of several volatile oils against larvae of the house
fly, Musca domestica vicina maquart (Diptera:
Muscidae). Journal of the Egyptian-German
Society of Zoology, 22, 131–149.

Zar, J. H. 1996. Biostatistical analysis. Prentice-Hall. Inc.

Upper Saddle River. New Jersey, USA.

133