Translate this page into:
Bioefficacy of essential oils emulsion and predatory mite, Euseius scutalis (Athias-Henriot) (Acari: Phytoseiidae) for the management of citrus brown mite, Eutetranychus orientalis (Klein) (Acari: Tetranychidae)
⁎Corresponding author. azema1@yahoo.com (Abdel-Azeem S. Abdel-Baki)
-
Received: ,
Accepted: ,
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.
Peer review under responsibility of King Saud University.
Abstract
The citrus brown mite, Eutetranychus orientalis (Klein), is a significant pest that is widely distributed in different agricultural systems. It causes significant damage to field crops and fruit trees. The most common method of control is the use of chemical acaricides. However, the extensive use of such chemicals developed resistance in addition to environmental and health hazards. Plant-derived acaricides might therefore be an environmentally friendly alternative to synthetic ones in order to increase agricultural production efficiency and to protect consumer health. Following this prospective, the present study was aimed to evaluate the toxic effects of anise (Pimpinella anisum), rosemary (Rosmarinus officinalis), eucalyptus (Eucalyptus globulus), clove (Eugenia caryophyllus), and garlic (Allium sativum) essential oils (EO) against the eggs and adult’s females of E. orentalis under laboratory conditions. Additionally, Euseius scutalis, a predator mite, was investigated as a bioagent to control E. orientalis under field conditions. GC-MS was used to assess the chemical components of the tested EOs. The results showed that anethole; 9, 12-Octadecadienoic acid (Z, Z); camphor; octatriacontyl pentafluoropropiona; and eugenol, were the major components for anise, rosemary eucalyptus, garlic, and cloves, respectively. Comparably, anise has been shown to be the most effective EO against E. orentalis eggs and adults as it exhibited a high level of efficiency and required the lowest concentration to reach the LC50. Additionally, the three Euseius scutalis release rates significantly reduced the Eutetranychus orientalis population. Ten individuals /seedlings in particular induced the highest reduction (84.95%). Based on our findings, we suggest using Euseius scutalis release and anise essential oil as alternative strategies to control of E. orentalis.
Keywords
Eutetranychus orientalis
Euseius scutalis
Essential oils
Bioagent
Management
1 Introduction
The citrus brown mite, Eutetranychus orientalis (Klein), is the most significant phytophagous species in fields and greenhouses. It is found in tropical regions and threatens a variety of economically important horticultural and ornamental plants (Kamali et al., 2004). In developing countries, chemical control is remaining the most utilized tactic in pest management (Aktar et al., 2009). However, unlimited use of these chemicals against pests has massive effect on the environment, populations of natural enemies, soil and human health (Kumar et al., 2010). In addition, it leads to disrupt the biotic balance, increasing secondary pest outbreaks, pest resistance and resurgence. In order to avoid the downsides of synthetic pesticides, research has been conducted in recent years to identify eco-friendly, economical, and effective alternative approaches, including the use of plants derived pesticides derived, microorganisms, and natural enemies (Miresmailli and Isman, 2006). In this context, numerous studies have been conducted on the use of essential oils and their active ingredients as sustainable methods for the management of phytophagous mites, (Miresmailli and Isman, 2006; Han et al., 2010; Elhalawany and Dewidar, 2017), however Eutetranychus orientalis was the subject of few of these studies (Elhalawany et al., 2019). Many essential oils from rosemary, garlic, eucalyptus jojoba were proven to have insecticidal properties and generally much safe to the environment and humans (Afify et al., 2012; Hussein et al., 2013). Also, there were many experiments on the use of biocontrol agents such as phytoseiid mite against many tetranychide mite infesting different crops (El-Ghobashy, 2012; Ebrahim, 2016). Euseius scutalis (Athias-Henriot) is considered one of the most pollen-feeding phytoseiid mite species. It is widely distributed in cultivated and uncultivated plants (including citrus crops). It feeds and survives on plant tissues without causing economic damage (Adar et al., 2012). In addition, it showed a large scale of environmental tolerances (temperature and humidity). Several previous studies have shown that E. scutalis can develop and reproduce feeding on both T. urticae and E. orientalis (Stathakis et al., 2021). Hence, it could be considered as one of the most suitable and effective bio-control agent for integrated pest management programs against plant feeding mites. The present work was therefore aimed on one hand to evaluate the chemical composition and the effect of some plant essential oils on the eggs and adult females of pest mite E. orientalis, and on other hand control of E. orientalis on citrus seedling by releasing of predatory mite E. scutalis.
2 Materials and methods
2.1 1. Preparation of essential oils emulsion
Essential oils of anise (Pimpinella anisum), rosemary (Rosmarinus officinalis), eucalyptus (Eucalyptus globulus), clove (Eugenia caryophyllus), and garlic (Allium sativum) were obtained from El- Gabry medical herbs pharmacy in Giza, Egypt. To prepare different concentrations of essential oil emulsions; two drops of 0.05 % Tween-80 as an emulsifier agent were added to the oils and the known volume was completed with distal water then the mixture was stirred for 30 min. Tween-80 (0.05 %) with distal water was used as a control treatment (Koschier et al., 2002).
2.2 Chemical composition
The essential oils chemical constituents were analyzed using GC–MS/FID (Gas chromatography coupled to mass spectrometry/flame ionization detector) at the laboratory of environmental and food pollutant analysis, Faculty of Agriculture Fayoum University Egypt as recommended by Adams (1995). The identification of the compounds was based on the comparison of their relative retention indexes and mass spectra with those provided in mass spectra library NIST (2007), literature and instrument’s databases (Adams Book 07, Nist 98, Xcalibur).
2.3 Source of E. orentalis prey mites
The citrus brown mites, E. orientalis were collected from leaves of castor bean (Ricinus communis). The adult females of E. orientalis were transferred to castor bean disks, which were placed on moistened cotton pads resting on sponge layer in the foam dish (15 × 20 cm). The colonies were maintained at room temperature. The leaves were examined and replaced with fresh ones when becoming yellow and crowding of mites. In addition, water was added to prevent the mites from escaping.
2.4 Adult spraying test
Four concentrations (1 %, 2 %, 3 % and 4 %) of each essential oil were used in five replicates per concentration to calculate the LC50 and LC90 according to the method proposed by Mailloux and Morrison (1962). Briefly, discs of mulberry leaves (3 cm in diameter) were placed in a foam dish (15 × 20 cm) which was lined with a layer of sponge and cotton pads soaked in water. Ten adult females of mites were transferred to each disc (10 adult female/leaf discs) in five replicates per treatment and repeated in each concentration. 50 adult females in five replicates (10 adult females per leaf disc) were act as control treatment. Each disc of mulberry leaves was sprayed by a glass atomizer in each concentration for each essential oil while the control was sprayed by distal water with two drops of 0.05 % of Tween-80. At 24, 48, and 72 h post treatments, the dead and live adult female mites were counted using a binocular microscope and a fine camel hairbrush. The mean mortality rate, LC50 and LC90 were calculated according to Abbott's formula (1925).
2.5 Egg hatchability test
Leaf discs of mulberry were used as substrate. For each treatment, five leaf discs were used, and the female mites were transferred to each disc and given 24 h to lay eggs before being removed. Subsequently, five replicates leaf discs, 20 eggs per each replicate were used (100 eggs in five replicate)/ per each concentration (4 %, 3 %, 2 %, and 1 %). Eggs were sprayed by a glass atomizer in each concentration for each essential oil emulsion while, the control was sprayed by distal water with two drops of 0.05 % of Tween-80. Eggs were maintained under laboratory conditions for seven days till hatching. The numbers of hatched and non-hatched eggs were recorded. Corrected mortality was calculated using Abbott's formula (1925) whereas, LC50, LC90 and slope values were estimated according to Finney (1971).
2.6 Euseius scutalis (A-H) releasing
This experiment was carried out under the field condition to estimate the effect of the predatory mite Euseius scutalis against E. orientalis at Fayoum Governorate on mandarin seedlings (with age of two years old) with three levels of release (3, 5 and 10 predators/ seedling) from May to October 2021. In brief, forty–mandarin seedlings infested with the mite pest Eutetranychus orientalis were prepared and divided into four groups of 10 seedlings each as three levels of release and control. Make mass rearing of predatory mite Euseius scutalis using bean plant phaseolus vulgaris as a host of pry and predator to obtain a lot of numbers of this mite to use in releasing. The leaf of bean plant with the predatory mite was collected and packed in plastic bags and transferred to the field experiment of seedlings and then distributed on the seedlings with three levels 3, 5 and 10 individuals of predators per seedling. The next samples were collected every 10 days after release the predators and the numbers of motile stage prey and predators were recorded till the end of the experiment. The percent of reduction was calculated the using the equation of Henderson and Tilton (1955) as following:
One-way analysis of variance (ANOVA) and the Least Significant Difference (LSD) have been utilized to analyze the data using SAS Program version 9.1 (SAS Institute, 2003). The data were subjected to probit analysis (Finney 1971) to determine lethal concentration of essential oil needed to kill 50 % and 90 % of Eutetranychus orientalis (LC50 and LC90), slope, and toxicity index values using Ldp line software ( http://www.ehabsoft.com/ldpline/ ). The reduction percent of E orientalis was calculated according to the equation proposed by Henderson and Tilton (1955) to select the suitable level of release, which could be recommended. In full test F, P and LSD values were used for comparing the means of reduction (α ≤ 0.05).
3 Results
3.1 Chemical components of essential oils
The percentages of identified components and their retention time (R.T.) were given in Table 1. The major constituents of the oil are anethole (26.175 %); 9, 12-Octadecadienoic acid (Z, Z) (30.03 %); octatriacontyl pentafluoropropiona (11.522 %), camphor (14.262 %); and eugenol (32.823 %) in anise, rosemary, garlic, eucalyptus and cloves, respectively.
Anise
Rosemary
Eucaluptus
R.T.
Name of compound
%
R.T.
Name of compound
%
RT
Name of compound
%
6.829
α-Pinene
0.011
6.836
α-Pinene
1.041
9.145
d-Limonene
0.002
7.866
β-Pinene
0.028
7.192
Camphene
2. 324
10.659
l-Fenchone
2.008
9.043
p-Cymene
0.042
7.872
β-Pinene
0.137
10.952
Terpin diacetate
2.010
12.224
Citronellal
0.519
9.049
p-Cymene
1.103
11.079
camphene
0.040
12.536
l-Menthone
0.122
9.150
d-Limonene
1.103
12.122
Camphor
14.262
12.345
Isopulegol
0.390
9.219
Camphor
14.595
12.281
l-Menthone
0.050
13.352
Estragole
0.408
12.05
Eucalyptol
12.497
12.377
Isoborneol
0.008
15.036
4-methoxy- Benzaldehyde,
7.413
12.60
propan-2-ol
0.260
17.034
Eugenol
0.019
15.666
Anethole
26.175
13.18
α-Terpineol
1.397
24.916
2-propyl tetradecyl ester
0.050
17.740
2-Propanone
2.939
15.40
Bornyl acetate
1.063
31.774
Ethanol
4.761
19.686
1,5-dimethyl-4-hexenyl
1.086
17.40
Eugenol
2.210
32.538
Tetrapentacontane
2.278
20.208
β -Bisabolene
0.339
21.78
Caryophyllene oxide
0.456
33.028
Eicosane
7.140
20.539
trans-calamenene
0.202
31.40
9,12-Octadecadienoic acid(Z,Z)
30.03034wq
33.218
1,8- Cineole
3.701
21.805
2(1H)-Pyridinone
7.201
31.90
9-Eicosyne
7.205
33.333
Octadecane
1.256
23.122
alpha.-ethyl-4-methoxy
2.310
36.241
1-palmitate
2.005
33.568
Docosane
5.076
23.593
2-Butanone
1.269
38.411
9,17-Octadecadienal
1.231
33.766
Menthol
1.525
24.229
4-Methoxyphenyl
2.491
38.567
3-hydroxypropyl ester
21.099
34.332
Octatriacontyl pentafluoropropiona
4.261
32.798
4-Hexanoylresorcinol
1.337
38.826
2,3-hydroxypropyl ester
6.273
34.701
1-Chloroeicosane
1. 542
33.327
2-Heptanone
1.239
39.063
2-Chloroethyl linoleate
8.467
34.917
Tetracosane
2.311
35.509
Benzamide
5.353
41.266
2-Butanone
0.368
35.280
Heneicosane
9.813
35.763
Acetamide
2.275
35.598
1-Eicosene
3. 811
35.865
4,4′-Dimethoxychalcone
5.079
39.231
3-oxo-1-butenyl
0.241
36.590
3-Methyl-5-nitrosotropone
4.015
36.940
Ethanone
9.658
37.920
1-Propanone
3. 750
Garlic
Clove
9.056
o-Cymene
0.006
16.073
2,4-Decadienal
3.127
9.151
d-Limonene
0.005
17.091
Eugenol
32.823
12.071
Camphor
0.010
34.268
Pentadecane
1.017
12.555
cis- l-Menthone
0.005
34.357
Octadecane
1.078
12.866
Terpinen-4-ol
0.002
34.618
Tetracosane
1.439
17.046
Eugenol
0.013
34.694
Eicosane
6.028
20.577
p-Menth-8(10)-en-9-ol
0.031
34.840
Heneicosane
11.329
23.415
1-Hydroxypyrene
0.242
35.203
Tricosane
3.619
24.585
2-propyl tridecyl ester
1.007
36.148
Pentacosane
2.671
25.768
Hexadecane
1.871
36.291
Tetracosane
1.017
27.359
1-Decanol
2.134
36.478
Hexacosane
1.450
30.381
1-Eicosene
2.431
40.108
Squalene
0.366
31.876
Ethanol
2.961
40.673
Acetophenone
11.160
32.519
Octadecane
1.988
40.997
3-Methyl-5-nitrosotropone
1.967
32.805
Tetrapentacontane
0.616
41.456
Benzothiophene-3-carbohydrazide
9.917
33.536
Docosane
1.658
41.839
6H-Purin-6-one
1.011
34.122
Octatriacontyl pentafluoropropiona
11.522
42.055
Silane
0.289
34.901
Eicosane
9.751
35.261
Heneicosane
8.575
39.523
Triacontyl acetate
0.621
3.2 Efficacy of essential oils emulsion against Eutetranychus orientalis Klein
3.2.1 Adult spraying test
The acaricidal activities of the five EOs against adult females of E. orientalis after 72 hrs are presented in Table 2. All treatments induced significant effects on E. orientalis when compared to the control. The anise EO showed the highest significant mortality (77.7 %) at a concentration of 4 % (P ≤ 0.05) as the other four EO induced mortality below 70 % at the same concentration. Also, LC50 of anise attained at a concentration of 1.27 % which comparably lowers than the concentrations required to the LC50 the other four EO and this evidenced that the strongest acaricidal activity was for the anise EO (Table 4 and Fig. 1). Data are means ± standard error means (SEM). Superscript of the same letter in cells of the same column is non-significant. Superscript of different letters in cells of the same column is significant (P ≤ 0.05).
Conc
Anise
rosemary
Garlic
Eucalyptus
Cloves
Mortality (mean ± SEM)
4 %
77.7 ± 1.2a
68.88 ± 2.31a
66.65 ± 1.15a
66.66 ± 1.73a
64.44 ± 2.56a
3 %
73.33 ± 1.73b
60.00 ± 1.2b
53.33 ± 2.5b
57.77 ± 2.31b
55.55 ± 2.89b
2 %
68.8 ± 1.2c
44.44 ± 2.31c
51.11 ± 0.64b
55.55 ± 1.15b
42.22 ± 1.28c
1 %
40.00 ± 1.15d
35.55 ± 0.58d
33.33 ± 1.34c
33.33 ± 1.2c
33.33 ± 1.35d
Control(0.05 % of Tween-80)
9.33 ± 0.67e
9.33 ± 0.67e
9.33 ± 0.67d
9.33 ± 0.67d
9.33 ± 0.67e
F value
562.68
290.45
181.52
234.91
121.28
P value
<0.001
<0.001
<0.001
<0.001
<0.001
Ldp-lines of toxicity effect of anise, rosemary, eucalyptus, clove and garlic essential oil on eggs adult females and of Eutetranychus orientalis.
3.2.2 Egg hatchability test
As shown in Table 3, all the tested EO showed pronounced ovicidial activity in comparison with the control. The rosemary EO showed maximum inhibition of the egg hatchability (93.33 %) followed by the anise EO (84 %) while the lowest inhibition of egg hatchability was induced by eucalyptus and garlic showed (73.33 %). LC50 attained at a concentration of 0.593 %, and 0.597 % for rosemary and anise, respectively. The slopes for rosemary, anise, cloves, eucalyptus and garlic are 1.67, 1.16, 0.99, 0.91 and 0.99, respectively. Thus, it is shown that rosemary essential oil became more effective with increase in the concentrations (Table 5 and Fig. 1). Data are means ± standard error means (SEM). Superscript of the same letter in cells of the same column is non-significant. Superscript of different letters in cells of the same column is significant (P ≤ 0.05). LC50: Lethal concentration of essential oil required to kill 50% of Eutetranychus orientalis. LC90: Lethal concentration of essential oil required to kill 90% of Eutetranychus orientalis. Index compared with anise. Index compared with Egg anise. LC50: Lethal concentration of essential oil required to kill 50% of Eutetranychus orientalis. LC90: Lethal concentration of essential oil required to kill 90% of Eutetranychus orientalis.
Conc
Anise
rosemary
Garlic
Eucalyptus
Cloves
Un-hatched egg (Mean ± SEM)
4 %
84.00 ± 2.31a
93.33 ± 1.73a
73.33 ± 1.73a
73.33 ± 2.89a
77.33 ± 2.08a
3 %
77.33 ± 1.73a,b
88.00 ± 2.89a
65.33 ± 2.08b
70.66 ± 2.08a
70.66 ± 2.89a
2 %
74.66 ± 2.89b
77.33 ± 4.04b
62.66 ± 2.88b
65.33 ± 2.88a
68.00 ± 4.04a
1 %
60.00 ± 2.89c
66.66 ± 1.73c
49.33 ± 1.15c
53.33 ± 1.73b
54.66 ± 2.31b
Control (0.05 % of tween 80)
25.00 ± 2.88d
25.00 ± 2.88d
25.00 ± 2.88d
25.00 ± 2.88c
25.00 ± 2.88c
F value
83.5
77.04
68.04
62.85
36.2
P value
<0.001
<0.001
<0.001
<0.001
<0.001
Essential oil
LC50
Lower limit%
Upper limit%
Toxicity index
Slope
LC90
Anise
1.27
0.72
1.67
100
1.70
7.19
Rosemary
1.91
1.36
2.88
99.33
1.36
8.03
Cloves
2.33
1.62
3.50
79.49
1.32
21.55
Eucalyptus
2.06
1.20
2.63
75.83
1.36
16.79
Garlic
2.06
1.38
2.86
57.62
1.38
17.38
Essential oils
LC50
Lower limit%
Upper limit%
toxicity index
slope
LC90
Anise
0.593
0.156
0.954
100
1.16
7.537
Rosemary
0.597
0.276
0.864
99.33
1.67
3. 476
Coves
0.746
0.173
1.174
79. 49
0.99
14.563
Eucalyptus
0.782
0.143
1.247
75.83
0.91
20.049
Garlic
1.029
0.362
1.478
57.62
0.99
20.131
3.3 Euseius scutalis (Athias-Henriot) releasing
On the control seedlings leaves, the average number of E. orientalis varied throughout time. At the beginning of the trial, means were 100 individuals/20 leaves, and they peaked between July 30 and September 28 with 330 mites/20 leaves during the 2021 season. (Fig. 2). On May 31 (at the beginning of the experiment), the means for 3, 5, and 10 levels of release were 90, 65, and 100, respectively. On October 8, the means for the three levels decline to their lowest densities of 13, 7, and 11. The mean numbers of E. orientalis in the treated seedlings changed throughout time. At all inspection dates, their numbers were always lower than that of the control. Each treatment was statistically different from the control.Mean number of Eutetranychus orientalis after 3, 5 and 10 release of Euseius scutalis on seedling of mandarin in season 2021.
The maximum reduction in pest mites was observed for the first, second, and third levels of release on September 28 with percent of 94.27 %, 96.27, and 98.48 %, respectively, and this associated with highest numbers of E. scutalis (15, 17, and 25 predators per 20 leaves)/330 individuals in the released and unreleased one, respectively (Fig. 2).
In all assessments, the highest mean percentage of reduction (84.95 %) in Eutetranychus orientalis was attained at a release rate of 10 predatory/seedlings meanwhile, the lowest one (76.10 %) was occurred at a release rate of 3 predators/ seedling. This decrease did not differ significantly between the release rate of 3 and 5 seedlings/predators (Table 6). Euseius scutalis was observed on mandarin seedlings where it was released but not in the control one after the release. In the 3, 5 and 10 release rates, the mean number of predators was significantly different (p ≤ 0.001) (Table 7). Superscript of the same letter is non-significant. Superscript of different letters is significant (P ≤ 0.05). Superscript of the same letter is non-significant. Superscript of different letters is significant (P ≤ 0.05).
Sampling date
Reduction % of E. orientalis/ 20 leaves after release of E. scutalis
3 predators/ mandarin seeding
5 predators/ mandarin seeding
10 predators/ mandarin seeding
10-Jun
45.67
47
49.46
20-Jun
58.03
59.44
60
30-Jun
65.27
66.66
73.75
10-Jul
74.07
74.35
85.66
20-Jul
63.88
64.1
88.75
30-Jul
76.43
77.15
93.93
09-Aug
78.9
83.77
91.98
19-Aug
75.69
82.69
93.12
29-Aug
82.87
84.61
85.83
08-Sep
92.87
93.58
95.83
18-Sep
88.17
88.21
92.76
28-Sep
94.27
96.27
98.48
08-Oct
93.12
94.06
94.76
Mean
76.10a
77.84a
84.95b
F-value
15.38
P-value
0.0001
L.S.D at 0.05
3.48
Sampling date
Number of E. scutalis / 20 leaves
3 predators/ mandarin seeding
5 predators/ mandarin seeding
10 predators/ mandarin seeding
Mean Temp.
Mean RH.
10-Jun
3
6
5
33.51
30.67
20-Jun
4
10
10
31.43
34.34
30-Jun
7
11
13
34.18
45.47
10-Jul
7
12
15
32.89
51.37
20-Jul
5
9
11
36.01
26.99
30-Jul
6
11
12
32.62
44.57
09-Aug
7
15
17
33.35
49.69
19-Aug
4
9
14
32.39
49.16
29-Aug
11
7
10
33.74
47.15
08-Sep
15
15
22
34.29
40.97
18-Sep
10
12
17
27.61
49.86
28-Sep
12
17
25
27.35
55.13
08-Oct
9
10
12
27.33
51.58
Mean
7.69a
11.07b
14.07c
F-value
26.97
P-value
0.0001
L.S.D at 0.05
1.97
4 Discussion
Using conventional chemical acaricides is the most common method to control the citrus brown mite, E. orientalis (Afify et al., 2012). However, the indiscriminate use of such chemicals induced great problems to the environment in addition to development of resistance to many acaricides (Heikal et al., 2019). To avoid these problems, alternative methods for the control of E. orientalis are being evaluated, including the use of essential oils that proved to be promising agents for the control of agricultural pests (Heikal et al., 2019). Following this perspective, in the present study anise, rosemary, garlic, eucalyptus and cloves oils were tested for their acaricidal effects against E. orientalis. Analysis of these oils revealed that the major constituents were anethole in anise, 9,12-octadecadienoic acid (Z,Z) in rosemary, octatriacontyl pentafluoropropiona in garlic, camphor in eucalyptus and eugenol in cloves similar to these reported by Kuś and Jerković, (2021) and Elazab et al. (2022).
In the present study, anise EO showed the most significant acaricidal efficacy with a mortality rate reaching 77.7 % after 72 h while the cloves EO showed the lowest efficacy. This may be attributed to the presence of anethole as major oils constituents. Anethole was proven to have direct effect on the nervous system due to its inhibitory activity against the AChE enzyme by binding with the active site of AChE by the hydrophobic interactions (El-Sayed et al., 2022). In agreement with our result, Vinicius et al. 2018 found that anise was the most promising extract against T. urticae with a mortality rate above 75 %. Also, El-Sayed et al. (2022) confirmed the acaricide activity of anise against T. urticae. In addition, anethole phenylpropanoid; the most important component of anise, was very efficient in controlling Aedes aegypti and Culex pipiens (Knio et al., 2008). The obtained LC50 for anise also reflects its high acaricidal activity against E. orientalis.
Regarding egg hatchability, the highest mean number of unhatched eggs was associated with rosemary (93.3 %), followed by anise (84 %), while eucalyptus and garlic showed the lowest mean number (73.33 %). Similarly, Menaceur et al. (2016) found significant reduction in the hatchability of Callosobruchus maculatus eggs after the treatment with rosemary EO. The difference in the amount of phenolic metabolites these oils contained may account for the variability in their impact on the eggs' capacity to hatch.
In this study, fatty acids and their esters were the main components of rosemary EO based on GC/MS analysis. Several studies have been conducted to correlate insecticidal activity with the chemical structure of fatty acids and their esters. According to Chen and Dai (2015), 9-octadecenoic acid, ethyl ester, a structurally-similar compound, shows the potential to be developed as new natural acaricide for controlling carmine spider mites (Tetranychus cinnabarinus). Also, Jiang et al. (2018) identified 9, 12-octadecadienoic acid (20.9 %), as a major constituent in the extract of Robinia pseudacacia and it exhibited strong insecticidal activities against cotton aphid and cabbage aphid. In addition, 9, 12-octadecadienoic acid was the major fatty acid in the Jatropha curcas oil that exhibited anti-oviposition and ovicidal effects on cowpea bruchid, Callosobrochus maculatus (Adebowale and Adedire, 2006). Furthermore, Satyan et al. (2009) found that the treatment with fatty acid mixtures can inhibit the growth of Helicoverpa armigera larvae. The acaricidal effects of these fatty acids were attributed to their interfering with the nematode cuticle or hypodermis via a detergent/solubilization effect or through their direct interaction with the lipophilic regions of target plasma membranes (Davis et al., 1997).
Our results proved the impact of the predatory mite, E. scutalis in the management of the citrus brown mite, E. orientalis using three rates of release during 5 months as its release induced a significant reduction in the number of E. orientalis during the full growing season. Similarly, Metwally et al. (2010) found that the release of E. scutalis reduced the percent of T. urticae on apple seedling. Also, Heikal et al. 2019 found that the numbers of E. orientalis on the navel orange trees were affected by releasing of E. scutalis as a biological control agent.
Statistically, there were significant differences between the three releasing rates. The rate of 10 predatory mites /seedling was the most appropriate one with an average reduction of 84.95 %. There was no significant difference between the rates of 3 and 5 predatory mites/seedling. This study did not record any kind of damage to the seedling, but concerned the impact of different release rates of Euseius scutalis on populations of E. orientalis infesting mandarin seedlings only. Similarly to EL-Halawany et al. (1993), the release of Euseius scutalis caused a high percent reduction (89.5 %) in Brevipalpus californicus on the Baladi orange tree. Also, El-Ghobashy (2012) evaluated the efficacy of the predatory mite, Euseius scutalis against citrus brown mite, Eutetranychus orientalis on the citrus trees and they found an 82.88 % reduction in prey population density.
At all release rates, there was a reduction in the density of E. orientalis after release. The lowest reduction rate of the E. orientalis was at the density of 3 predatory mites /seedling. Thus, the higher release rates (higher densities of predators) resulted in greater reductions of the E. orientalis.
In conclusion, the results obtained in the present study indicated that Euseius scutalis is an important factor for the population reduction of E. orientalis on mandarin seedlings under field conditions. This predatory mite could therefore be suitable as a biological control agent for this pest with the release rate of 10 predators per seedling as it introduced the highest percent of reduction in the mite pest.
Further studies in the combination of predatory mites and essential oil active ingredient will represent a more efficient biological control strategy for E. orientalis.
CRediT authorship contribution statement
Mariam Mohamed Ibrahim Ata: Methodology, Investigation. Gamal Zidan El-Shahawy: Supervision, Methodology. Magdy Hussein Fawzy: Supervision. Abdel-Azeem S. Abdel-Baki: Supervision, Methodology. Saleh Al-Quraishyd: Project administration, Funding acquisition. Ahmed O. Hassan: Supervision, Methodology. Heba Abdel-Tawab: Methodology, Investigation.
Acknowledgements
This work was supported by Researcher supporting Project (RSP 2021/3), King Saud University
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
References
- A method of computing the effectiveness of an insecticide. J. Econ. Entomol.. 1925;18:265-267.
- [CrossRef] [Google Scholar]
- Identification of Essential Oil Components by Gas Chromatography / Mass Spectroscopy. Illinois: Allured Publishing Corporation; 1995.
- Plant-feeding and non-plant feeding phytoseiids: differences in behavior and cheliceral morphology. Experi. Appli. Acarol.. 2012;58:341-357.
- [Google Scholar]
- Chemical composition and insecticidal properties of the underutilized Jatropha curcas seed oil. Afr. J. Biotechnol.. 2006;5(10):901-906.
- [Google Scholar]
- Control of Tetranychus urticae Koch by extracts of three essential oils of chamomile, marjoram and Eucalyptus. Asian Pac J Trop Biomed.. 2012;2(1):24-30.
- [CrossRef] [Google Scholar]
- Impact of pesticides use in agriculture: 259 their benefits and hazards. Interdiscip. Toxicol.. 2009;2(1):1-12.
- [CrossRef] [Google Scholar]
- Acaricidal activity of compounds from Cinnamomum camphora (L.) Presl against the carmine spider mite, Tetranychus cinnabarinus. Pest Manag. Sci.. 2015;71(11):1561-1571.
- [CrossRef] [Google Scholar]
- Nematicidal activity of fatty acid esters on soybean cyst and root-knot nematodes. J. Nematol.. 1997;29(4s):677-684. PMID: 19274268 PMCID: PMC2619835
- [Google Scholar]
- Releasing of the Predatory Mite, Neoseiulus californicus (McGregor) for controlling the citrus red mite, Panonychus citri (McGregor) ACARINES.. 2016;10:53-58.
- [CrossRef] [Google Scholar]
- Effect of dietary rosemary and ginger essential oils on the growth performance, feed utilization, meat nutritive value, blood biochemicals, and redox status of growing rabbits. Animals.. 2022;12:375.
- [CrossRef] [Google Scholar]
- feasibility of using the predatory mite Euseius scutalis (Athias-Henriot) in controlling Eutetranychs orientalis (Klein) on citrus trees. J. Plant Port. Path., Mansoura Univ. Egypt.. 2012;3(12):13331-111336.
- [Google Scholar]
- Evaluating the efficiency of different levels of Euseius scutalis (Athias – Henriot) released for the control of Brevipalpus californicus Banks on Baladi orange tree. Menoufia J. Agric. Res. Egypt. 1993;18(2):2697-2707.
- [Google Scholar]
- Laboratory Bioassay for the Efficacy of Coriander and Rosemary Extracted Essential Oils on the Citrus Brown Mite, Eutetranychus orientalis (Actinidida: Tetranychidae) ACARINES. 2019;13:15-20.
- [CrossRef] [Google Scholar]
- Efficiency of Some Plant Essential Oils Against the Two-Spotted Spider Mite, Tetranychus urticae Koch and the Two Predatory Mites Phytoseiulus persimilis(A.-H.), and Neoseiulus californicus (McGregor) Egypt. Acad. J. Biolog. Sci.. 2017;10(7):135-147.
- [CrossRef] [Google Scholar]
- Acaricidal and Antioxidant Activities of Anise Oil (Pimpinella anisum) and the Oil’s Effect on Protease and Acetylcholinesterase in the Two-Spotted Spider Mite (Tetranychus urticae Koch) Agriculture. 2022;12:224-237.
- [CrossRef] [Google Scholar]
- Probit Analysis (3rd ed.). London: Cambridge Univ. Press; 1971.
- Toxicity of plant essential oils to acaricide-susceptible and -resistant Tetranychus urticae (Acari: Tetranychidae) and Neoseiulus californicus (Acari: Phytoseiidae) J. Econ. Entomol.. 2010;103:1293-1298.
- [CrossRef] [Google Scholar]
- Safe Control Methods of Eutetranychus orientalis (Klein) Infested Navel Orange Trees at Menoufia Governorate. Egypt. African Entomol.. 2019;27(2):468-476.
- [CrossRef] [Google Scholar]
- Tests with acaricides against the brown wheat mite. J. Econ. Entomol.. 1955;48 157 –161
- [CrossRef] [Google Scholar]
- Repellent, antifeedent and toxic effects of three essential oils on the two Spotted Spider Mite, Tetranychus urticae Koch (Acari: Tetranychidae) Acta Phytopathol. Entomol. Hung.. 2013;48(1):177-186.
- [CrossRef] [Google Scholar]
- Chemical composition of an insecticidal extract from Robinia pseudacacia L. seeds and its efficacy against aphids in oilseed rape. Crop Protection.. 2018;104:1-6.
- [CrossRef] [Google Scholar]
- A Catalog of Mites and Ticks (Acari) of Iran. Islamic Azad Univ. Sci. Publ. Center, Tehran. 2004
- [CrossRef] [Google Scholar]
- Larvicidal activity of essential oils extracted from commonly used herbs in Lebanon against the seaside mosquito, Ochlerotatus Caspius. Bioresour. Technol.. 2008;99:763-768.
- [CrossRef] [Google Scholar]
- Influence of plant volatiles on feeding damage caused by the onion Thrips tabaci. Crop Prot.. 2002;21(5):419-425.
- [CrossRef] [Google Scholar]
- Management of two spotted spider mite Tetranychus urticae Koch a serious pest of brinjal, by integrating biorational methods of pest control. J. Biopestic.. 2010;3(1):361-368.
- [Google Scholar]
- Application of the dehydration homogeneous liquid–liquid extraction (DHLLE) sample preparation method for fingerprinting of honey volatiles. Molecules. 2021;26:2277.
- [CrossRef] [Google Scholar]
- The effect of acaricides on developmental stages of the two-spotted spider mite Tetranychus telarius. J. Econ. Entomol.. 1962;55:479-483.
- [Google Scholar]
- Biological control of Tetranychus urticae Koch using the phytoseiid mite, Euseius scutalis (A-H) on apple seedlings. Egypt J. Agric. Res.. 2010;88(3):693-700.
- [Google Scholar]
- Efficiency and persistence of rosemary oil as an acaricide against two spotted spider mite (Acari: Tetranychidae) on greenhouse tomato. J. Econ. Entomol.. 2006;99(6):2015-2023.
- [CrossRef] [Google Scholar]
- SAS Institute. 2010. SAS Statistics and Graphics Guide, Release 9.1. SAS Institute, Cary, North Carolina, 275l3, USA.
- Growth inhibitory activity of fatty acid methyl esters in the whole seed oil of Madagascar periwinkle (Apocyanaceae) against Helicoverpa armigera (Lepidoptera: Noctuidae) J. Econo. Entomol.. 2009;102(3):1197-1202.
- [CrossRef] [Google Scholar]
- Predation by Euseius scutalis (Acari: Phytoseiidae) on Tetranychus urticae and Eutetranychus orientalis (Acari: Tetranychidae): effect of prey density and developmental stage. Systematic and Applied Acarology. 2021;26(10):1940-1951.
- [Google Scholar]
- Plant extracts with potential to control of two-spotted spider mite. Arq. Inst. Biol.. 2018;85:1-8.
- [CrossRef] [Google Scholar]