© The Authors, 2023, Published by the Universidad del Zulia*Corresponding author: avalverde@unheval.edu.pe
Keywords:
Biological control
Beauveria
Metarhizium
Bacillus
Acaropathogens
Eciency of entomopathogenic bacteria and fungi on Oligonychus yothersi in vitro and on
Persea americana Mill. plants
Eciencia de bacterias y hongos entomopatógenos sobre Oligonychus yothersi in vitro y en plantas
de Persea americana Mill.
Eciência de bactérias e fungos entomopatogênicos em Oligonychus yothersi in vitro e em plantas
Persea americana Mill.
Laura Carmen Barrionuevo Torres
4
Javier Romero Chavez
2
Rev. Fac. Agron. (LUZ). 2023, 40(4): e234033
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v40.n4.02
Crop Production
Associate editor: Dra. Lilia Urdaneta
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
Abstract
In the germplasm bank of 22 varieties of avocado (Persea americana
Mill.) belonging to the Fruit Horticultural Institute Investigation, Hermilio
Valdizan National University (UNHEVAL)-Peru, it is common to observe a
high population of the species Oligonychus yothersi, a phytophagous mite
harmful to the crop. Controls with commercial acaricides are restricted in
place, due to the presence of beehives installed in adjacent plots. The objective
of this study was to evaluate the eect of four commercial formulations
containing strains of Metarhizium anisopliae and Beauveria bassiana and
the toxins of Bacillus subtilis, Bacillus thuringiensis var. kurstaki (Btk) for
the control of O. yothersi. The entomopathogenic products were evaluated in
the eld applying a randomized complete block design with ve treatments
and three replicates. In the laboratory, 500 adult mites were selected, placing
100 mites per Petri dish with three repetitions per treatment. It was found that
the formulation Bacillus thuringiensis var. kurstaki under eld conditions
reduced the population incidence of mites by up to 98.07 % in 49 days. In
the laboratory, the B. subtilis and M. anisopliae formulations caused 100 %
mortality six days after application proving to be ecient control alternatives.
Jhimy Andy Parco Quinchori
1
Agustina Valverde-Rodriguez
2*
Antonio Cornejo y Maldonado
3
Henry Briceño Yen
2
1
National
Institute
of
Agrarian
Innovation
(INIA),
Junín,
Peru.
2
Faculty
of
Agrarian
Sciences,
HermilioValdizán
National
University, Peru.
3
Fruit Horticultural Institute Investigation, HermilioValdizan
National University.
4
Faculty
of
Educational
Sciences
Biology
and
Chemistry,
HermilioValdizán National University, Peru.
Received: 11-07-2023
Accepted: 15-09-2023
Published: 03-11-2023
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2023, 40(4): e234033. October-December. ISSN 2477-9407.2-7 |
Resumen
En el Banco de germoplasma de 22 variedades del palto (Persea
americana Mill.) perteneciente al Centro de Investigación Frutícola
Olerícola, Universidad Nacional Hermilio Valdizan (UNHEVAL)-
Perú, es frecuente observar una población alta de la especie
Oligonychus yothersi, ácaro tófago perjudicial al cultivo. Los
controles con acaricidas comerciales son restringidos en el lugar,
por la presencia de las colmenas de abejas instaladas en las parcelas
adyacentes. El objetivo de este estudio fue evaluar el efecto de cuatro
formulaciones comerciales que contienen cepas de Metarhizium
anisopliae y Beauveria bassiana y las toxinas de Bacillus subtilis,
Bacillus thuringiensis var. kurstaki (Btk) para el control de O.
yothersi. Los productos entomopatógenos fueron evaluados en
campo aplicando un diseño de bloques completos al azar con cinco
tratamientos y tres replicas. En el laboratorio se seleccionaron
500 ácaros adultos, colocando 100 ácaros por placa Petri con tres
repeticiones por tratamiento. Se encontró que el formulado Bacillus
thuringiensis var. kurstaki en condiciones de campo redujo hasta
un 98,07 % la incidencia poblacional de los ácaros en 49 días. En
laboratorio, los formulados de B. subtilis y M. anisopliae provocaron
el 100 % de mortalidad a los seis días pos-aplicación resultando ser
alternativas ecientes de control.
Palabras clave: control biológico, Beauveria, Metarhizium, Bacillus,
acaropatógenos.
Resumo
No Banco de Germoplasma de 22 variedades de abacate
(Persea Americana Mill.) pertencenteao Centro de Pesquisa de
Frutas Olerícola da Universidade Nacional Hermilio Valdizan
(UNHEVAL)-Peru, é comum observar uma elevada população da
espécie Oligonychus yothersi, um ácaro tófago prejudicial para a
colheita. Os controles com acaricidas comerciaissãorestritosdevido à
presença de colméias instaladas em parcelas adjacentes. O objetivo
desteestudofoi avaliar o efeito de quatro formulações comerciais
contendo cepas de Metarhizium anisopliae e Beauveria bassiana e
as toxinas de Bacillus subtilis, Bacillus thuringiensis var. kurstaki
(Btk) no controle de O. yothersi. Os produtos entomopatogênicos
foram avaliados em campo utilizando delineamento em blocos
casualizados com cinco tratamentos e três repetições. Em laboratório
foram selecionados 500 ácaros adultos, colocando 100 ácaros por
placa de Petri com três repetições por tratamento. Vericou-se que
a formulação Bacillus thuringiensis var. kurstaki em condições de
campo reduziu a incidênciapopulacional de ácaros em até 98,07 % em
49 dias. Em laboratório, as formulações de B. subtilis e M. anisopliae
causaram 100 % de mortalidade seis diasapós a aplicação mostrando-
se alternativas de controle ecientes.
Palavras-chave: controle biológico, Beauveria, Metarhizium,
Bacillus, acaropatógenos.
Introduction
In Peru, the species Oligonychus yothersi (McGregor) (Acari:
Tetranychidae) plays a limiting role in the agro-export processes of
Persea americana Miller, commonly known as avocado. In recent
years, the country has led the boom in avocado exports, entering 34
international markets (Chávez, 2019), so it is necessary to guarantee
compliance with phytosanitary standards as Peru’s commitment to
the international market.
The pest O. yothersi has been reported as a polyphagous and
severe species in several countries of the world (Pinto et al., 2012;
Ceballos et al., 2022), plant damage is expressed in the reduction
of photosynthetic activity, the consequence of which is excessive
defoliation of the plant when attacks are severe (Rioja et al., 2018;
Rioja et al., 2019). Among the most susceptible varieties of Persea
americana are Hass and Fuerte, with a direct consequence on fruit
quality and yield (Ceballos et al., 2022). This is the foliar pest with
the highest incidence during the autumn and summer season (Yang
et al., 2015; Bayu et al., 2017; Rioja et al., 2019) whose symptoms
are tanning and leaf fall, because the mite pierces the leaf with its
chelicerae in the form of a stylet and sucks the cellular contents (Rioja
et al., 2018; Chiaradia et al., 2021).
The traditional control of O. yothersi and other pests in the
cultivation of P. americana is based on chemical compounds such as
abamectins, spirodiclofen and sulfur, harmful to human health, and the
environment (Fathipour and Maleknia, 2016; Díaz and Aguilar, 2018;
Ramírez, 2018; Borges et al., 2021; Tosi et al., 2022), in addition to
causing resistance and resurgence of mites (Fathipour and Maleknia,
2016). In recent decades, a wide range of microbial pesticides have
been developed (Köhlet al., 2019) as a resilient strategy in agricultural
systems, a challenge of sustainable healthy food production (Balog et
al., 2017; Borges et al., 2021).
Among them are entomopathogenic microorganisms with
pathogenic capacity towards insects (Solter et al., 2012; Solórzano-
Acosta et al., 2021), capable of causing natural epizootics in
populations of mites or other arthropods, in addition to persisting in
the absence of their hosts in natural habitats (Meyling and Eilenberg,
2007; Zemek et al., 2018; Konopická et al., 2022).
The fungi Metarhizium brunneum, Metarhizium avoviride,
Lecanicillium lecanii, and Beauveria bassiana have been proven
eective against the dierent stages of development of the red spider
mite (Tetranychus urticae) with adult mortality success greater than 80
% (Dogan et al., 2017). The fungi, Akanthomyces lecanii, Beauveria
bassiana, Metarhizium anisopliae, and Aschersonia aleyrodis, after
nine days of exposure to red mites (Panonychus citri) caused more
than 70 % mortality (Qasim et al., 2021). Hussein et al. (2020) found
that the mortality percentage of the mite Oligonychus afrasiaticus
(McGregor) varied between 73.3 % and 92 %, after seven days of
treatment with B. bassiana, Metarhizium acridum, Lecanicillium
muscarium and Isaria fumosorosea. Among bacteria, Bacillus
thuringiensis Berliner has been shown to be eective against some
mite pests (Erban et al., 2009; Alahyane et al., 2019; Sánchez-Yáñez
et al., 2022) against pest insects of the orders coleoptera, diptera,
hymenoptera, homoptera, orthoptera, and others (Fang et al., 2009;
Ferreira-Agüero et al., 2020; Sánchez- Yáñez et al., 2022). These
ndings allow us to infer that the pathogenic or endotoxic eects of
entomopathogens would prove to be eective against the red spider
of the avocado O. yothersi. The present study evaluated the eect
of the entomopathogens Metarhizium anisopliae, Beauveria bassiana
and the toxins of Bacillus subtilis, Bacillus thuringiensis var. kurstaki
in the control of O. yothersi in avocado crops.
Materials and methods
The study was developed between November 2019 and February
2020 in the plots of the Hass variety, belonging to the germplasm
bank of 22 varieties of the avocado in the Fruit Horticultural Institute
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3-7 |
Investigation- UNHEVAL, district of Pillco Marca, Huánuco
region, Peru (09° 57′ 03” S, 76° 14′ 79” W), located above 1947
masl, with minimum temperatures of 14.8 °C and a maximum of
26.1°C and relative humidity of 77 % to 81.63 % (National Service
of Meteorology and Hydrology of Peru [Senamhi], 2020) during the
study period and in the laboratory of agricultural phytopathology,
Faculty of Agrarian Sciences- UNHEVAL.
Table 1. Characteristics of the treatments under study.
N° Treatments Microorganism
Concentration and
dosage
1
Bacillus thuringiensis
var. kurstaki
Bacterium
2.5.10
9
CFU.mL, 2
mL.L
-1
2
Bacillus subtilis
Bacterium
2.5.10
9
CFU.mL, 2
mL.L
-1
3
Metarhizium anisopliae
Fungus 1.0.10
10
conidia, 2 g.L
-1
4
Beauveria bassiana
Fungus 1.5.10
10
conidia, 2 g.L-
1
5 Absolute control No application
Methodology in the eld
The experimental design was a randomized complete block
design, with ve treatments and three replicates, because the upper
margin of the experimental area borders with the Coea arabica plots
and on the right margin with the irrigation distribution points and
Pinus sp. trees, that fulll the function of windbreak curtains. The
total population of the plants was 180 of the Hass variety (hybrid
cross of the Guatemalan and Mexican breeds), of uniform size with
2.82 m of height on average, of ve years, established in a frame of
four meters between plants, eight meters between lines as recorded in
gure 1. In avocado plants highly infested with the mite O. yothersi, to
determine the initial infestation, a count of mites per leaf was carried
out before the application of the products, for which two leaves were
identied at random from the lower third, two leaves from the middle
third and one leaf from the upper third of each plant.
Application of treatments
Water analysis was necessary to determine the pH and carbonate
content, and with the results obtained, the water was neutralized to
a pH range of 5.5 since the latter inuences the germination of the
fungus, delaying the values lower than 5.5 and higher than 7 (Velez et
al., 1997; Padmavathi et al., 2003; National Agrarian Health Service
[SENASA], 2014). The sequence for the dosage of the formulations
(SENASA, 2014) was as follows:
a) In 5 L of water, 5 mL of pH corrector was added and 30 minutes
later, 40 g of the biological product was added and then stirred until a
homogeneous mixture was obtained, in the case of entomopathogenic
fungi, 20 mL of agricultural oil was also added and then the mixture
was left to stand for six hours.
b) In a 20 L backpack sprayer, 15 liters of neutral pH water was
incorporated, and this was completed with the 5 L of the previously
prepared mixture.
The applications were made in the afternoon (4:00 pm), with
a frequency of every 7 days during the rst three weeks, and then
extended to every 15 days, adding a total of 14 applications in the
tree, for the entire trial.
Nine trees were sampled per treatment, the sample unit being 10
leaves per tree, divided into four leaves of the lower third, four of the
middle third, and two of the upper third. The number of mites per leaf
was quantied every 7 days, making observations at 7, 14, 21, 35, 49,
and up to 63 days.
Eciency estimates were made using the formula of Henderson
and Tilton (1955).
% Corrected ecacy percentage = [1-(Ca/Ta) * (Td/Cd)] *100
Where:
Ta = Infestation in treated plot before treatment.
Ca = Infestation in control plot before applying the treatment.
Td = Infestation in treated plot after application of treatment.
Cd = Infestation in control plot after applying the treatment.
Data on the number of mites per leaf were subjected to an analysis
of variance and Fisher LSD mean comparison test (α= 0.05) using the
Info Statstatistical program (Di Rienzo et al., 2013).
Laboratory methodology
Five hundred adult mites were selected without being
discriminated by sex, which were distributed in 15 units of Petri
dishes (90 x 100 mm), each dish with 100 mites and being occupied
three dishes for each treatment. Clean and disinfected leaves were
Figure 1. Sketch of the experimental eld and distribution of
treatments. Coee plots (Coea arabica). Block I, block
II, block III.
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placed inside each unit. The preparation of the entomopathogen
(SENASA, 2014) was as follows:
a) 250 mL distilled water was available.
b) They were transformed into milligrams or milliliters according
to the doses used in the eld.
c) The product was dosed in a 60 mL graduated cylinder where
0.06 mL of water corrector and 0.06 mL of agricultural oil (only for
the entomopathogenic fungi M. anisopliae and B. bassiana) and 0.12
g of the biological product were mixed.
d) It was necessary to use a 60 mL Hammer atomizer to pour the
distilled water and mix the biological product plus 0.06 mL of water
corrector and 0.06 mL of agricultural oil (only for M. anisopliae and
B. bassiana) to nally homogenize the mixture.
e) Ecacy observations were made daily for a period of 7 days,
with the response variable being the number of mites killed per dish
per day.
f) Eciency estimates were made using the Abbott formula
(1925).
% Corrected ecacy percentage = [ 1-(Ta/Co)] *100
Where:
Ta = Population in treated plot after treatment.
Co = Population in control plot after treatment.
Results and discussion
Eciency of entomopathogens in reducing populations of
Oligonychus yothersi under eld conditions
The eectiveness of entomopathogens is shown in table 2. At
seven days of pre-application counting, populations ranged from 144
to 177 mites per leaf on average (p>0.05). After the rst intervention,
populations were signicantly reduced to averages between 1.14
mites per leaf with the entomopathogenic fungus M. anisopliae and
8.64 mites per leaf with B. subtilis and in contrast to the control
treatment populations that reached averages of up to 146.5 mites per
leaf (p<0.05) in the rst fourteen days after application. In subsequent
evaluations the number of individuals was low and constant over time
with a maximum of 4.08 mites per leaf at 63 days, this being the last
evaluation; however, in the control treatment, the mite/leaf averages
oscillated over time.
The percentages of eciency for the population incidence of
O. yothersi caused by each entomopathogenic product are shown
in gure 2, where it is observed that the treatment M. anisopliae,
during the rst 14 days of the trial reduced up to 99.31 %, followed
by the entomopathogen B. thuringiensis var. kurstaki with an ecacy
of 97.12 %, leaving with lower percentages the B. subtilis and B.
bassiana.
Table 2. Incidence of the mite Oligonychus yothersi in avocado crop before and after the application of entomopathogens during the
2019-2020 season.
Treatments
Recount
Pre-application
Live mites per leaf in days (ddi) ± Standard Error
14 ddi 21 ddi 35 ddi 49 ddi 63 ddi
Bacillus subtilis (2 mL.L
-1
)
151.67±10.34 a 8.64±2.64 a 9.28±4.08 a 5.22±3.93 a 7.19±1.85 a 4.08±3.96 a
Bt var kurstaki (2 mL.L
-1
)
177.00±10.34 a 5.38±2.64 a 3.67±4.08 a 3.64±3.93 a 3.31±1.85 a 2.98±3.96 a
Metarhizium anisopliae (2 g.L
-1
)
147.33±10.34 a 1.14±2.64 a 3.17±4.08 a 2.14±3.93 a 3.11±1.85 a 2.08±3.96 a
Beauveria bassiana (2 g.L
-1
)
144.00±10.34 a 5.28±2.64 a 5.17±4.08 a 5.56±3.93 a 6.25±1.85 a 2.58±3.96 a
Control 150.67±10.34 a 146.5±2.64 b 119.53±4.08 b 104.83±3.93 b 131.64±1.85 b 128.42±3.96 b
Coecient of variance (%) 11.63 13.68 25.02 28.08 10.55 22.2
Note: ddi: days after application, dierent letters in the same column represent signicant dierences, Fisher LSD test (p < 0.05), independent statistical analysis for each
time comparing treatments.
Figure 2. Eciency (%) in the reduction of mites per leaf in days
(ddi) in the avocado crops of the CIFO-UNHEVAL
germplasm bank, 2019-2020 season.
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Similar behavior is demonstrated at 21, 35, 49, and 63 ddi, after
inoculation, with the percentages of population reduction higher than
90 % and less than 98.07 %, the latter with Bacillus thuringiensis
var. kurstaki. Research by Deka et al. (2022) recorded the eciency
of M. anisopliae up to 68.2 % in reducing the population incidence
of Oligonychus coeae at 14 ddi, although the percentages of
eectiveness are lower compared to the present study, and according
to the reports of Tahmina et al. (2020), native entomopathogenic
isolates have higher eciency than commercial acaricides based
on entomopathogens, in the present study it is demonstrated that
entomopathogens were ecient possibly favored by environmental
conditions that helped dispersion, viability, and incidence (Meyling
and Eilenberg, 2006; Meyling and Eilenberg, 2007). Cuatlayotl-
Cottier et al. (2022) evaluated B. thuringiensis spores as a biological
insecticide on Tetranychus urticae, observing between 60 % and 90
% mortality under eld conditions and up to 50 % and 80 % under
laboratory conditions. Veloorvalappil et al. (2018) demonstrated that
the entomopathogen Bacillus thuringiensis var. kurstaki was ecient
in controlling the red mite Eutetranychus orientalis.
Eciency of entomopathogens in the mortality of Oligonychus
yothersi under laboratory conditions
The evaluations showed that the entomopathogen M. anisopliae
(1.10
10
conidia) was the most ecient at the laboratory level,
achieving a reduction at a rate of 100; 5.3; 3.7; 0.7; 0,7; 0.7 and 0.00
respectively, during six assessment days, as shown in table 3. Similar
behavior was recorded for the treatment B. subtilis, of the 100 mites
treated on the rst day, all were eliminated (death) until the sixth day
of evaluation.
With B. bassiana and B. thuringiensis var. kurstaki reductions
were close to zero mites per dish, however, no signicant dierences
have been shown between entomopathogenic treatments (p>0.05).
Table 3. Number of live mites per Petri dish after the application of entomopathogenic formulations in the laboratory-UHEVAL.
Treatments
Live mites per plate and day (ddi) ± Standard Error
1 ddi 2 ddi 3 ddi 4 ddi 5 ddi 6 ddi
Bacillus subtilis (2 mL.L
-1
)
9.7±2.0 a 8.0±1.9 a 6.0±1.71 a 5.7±1.9 a 2.3±1.8 a 0.0±0.9 a
Bt var. kurstaki (2 mL.L
-1
)
3.7±2.0 a 3.7±1.9 a 3.3±1.71 a 2.7±1.9 a 2.0±1.8 a 1.0±0.9 a
Metarhizium anisopliae (2 g.L
-1
)
5.3±2.0 a 3.7±1.9 a 0.7±1.71 a 0.7±1.9 a 0.7±1.8 a 0.0±0.9 a
Beauveria bassiana (2 g.L
-1
)
10.3±2.0 a 8.0±1.9 a 6.3±1.71 a 5.7±1.9 a 4.7±1.8 a 0.7±0.9 a
Control (no application) 98.3± b 96.7±1.9 b 96.7±1.71 b 91.3±1.9 b 84.0±1.8 b 77.0±0.9 b
Coecient of variance (%) 14.0 13.72 13.1 15.6 16.5 10.1
Note: ddi: days after application, dierent letters in the same column show signicant dierences, LSD Fisher test (p < 0.05), independent statistical analysis for each time
comparing treatments.
Except for the control treatment where it was observed that, of
the 100 mites per dish, 77 mites survived on average up to six days
of evaluation.
The percentages of eciency of entomopathogens in laboratory
conditions are shown in table 4, registering for M. anisopliae and
B. subtilis 100 % eciency on the sixth day after inoculation of the
formulations. Followed by B. bassiana and Bacillus thuringiensis
var. kurstaki obtaining 98.70 % eciency in the mortality of mites of
the species O. yothersi. Slightly higher survival rates were reported
by Huanes-Carranza and Wilson-Krugg (2016) with B. bassiana and
M. anisopliae on adults and nymphs of Oligonychus sp. Meanwhile,
Deka et al. (2022) reported that M. anisopliae was eective against
O. coeae causing a mortality of 78 % four days after application.
Mamun et al. (2014) veried the eciency of several entomopathogens
against mites of the species O. coeae under laboratory conditions,
obtaining 81.83 and 97.24 % mortality with the entomopathogens M.
anisopliae and B. bassiana respectively.
Conclusions
The eect of the entomopathogens Metarhizium anisopliae,
Beauveria bassiana and the toxins of Bacilluss ubtilis, Bacillus
thuringiensis var. kurstaki, in the control of O. yothersi in avocado
crops has been proven, the most promising being M. anisopliae and
B. thuringiensis var. kurstaki with high percentages of eectiveness
in a short period of time. It is advisable to determine the persistence
over time of a single application and verify the eciency of the two
entomopathogens that oered the best results.
Table 4. Eectiveness of entomopathogens in reducing mites by dish under laboratory conditions.
Treatments
Eciency (%)
1 ddi 2 ddi 3 ddi 4 ddi 5 ddi 6 ddi
Bacillus subtilis (2 mL.L
-1
)
89.80 91.75 93.81 93.41 97.62 100.00
Bacillus thuringiensis var. kurstaki (2 mL.L
-1
)
95.92 95.88 96.91 96.70 97.62 98.70
Metarhizium anisopliae (2 g.L
-1
)
94.90 95.88 98.97 98.90 98.81 100.00
Beauveria bassiana (2 g.L
-1
)
89.80 91.75 93.81 93.41 94.05 98.70
Control ...... ...... ...... ...... ...... ......
Note: ddi: days after inoculation, % eectiveness: calculated according to Abbott’s formula (Abbott, 1925), independent statistical analysis for each time comparing
treatments.
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Parco et al. Rev. Fac. Agron. (LUZ). 2023 40(4): e234033
6-7 |
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