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Botanicals Against Tetranychus urticae Koch Under Laboratory Conditions: A Survey of Alternatives for Controlling Pest Mites

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Tetranychus urticae Koch is a phytophagous mite capable of altering the physiological processes of plants, causing damages estimated at USD$ 4500 per hectare, corresponding to approximately 30% of the total cost of pesticides used in some important crops. Several tools are used in the management of this pest, with chemical control being the most frequently exploited. Nevertheless, the use of chemically synthesized acaricides brings a number of disadvantages, such as the development of resistance by the pest, hormolygosis, incompatibility with natural predators, phytotoxicity, environmental pollution, and risks to human health. In that sense, the continuous search for botanical pesticides arises as a complementary alternative in the control of T. urticae Koch. Although a lot of information is unknown about its mechanisms of action and composition, there are multiple experiments in lab conditions that have been performed to determine the toxic effects of botanicals on this mite. Among the most studied botanical families for this purpose are plants from the Lamiaceae, the Asteraceae, the Myrtaceae, and the Apiaceae taxons. These are particularly abundant and exhibit several results at different levels; therefore, many of them can be considered as promising elements to be included into integrated pest management for controlling T. urticae.
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plants
Review
Botanicals Against Tetranychus urticae Koch Under
Laboratory Conditions: A Survey of Alternatives for
Controlling Pest Mites
Ricardo A. Rincón1,2, Daniel Rodríguez 1, * and Ericsson Coy-Barrera 2, *
1Biological Control Laboratory, Universidad Militar Nueva Granada, Cajicá250247, Colombia
2Bioorganic Chemistry Laboratory, Universidad Militar Nueva Granada, Cajicá250247, Colombia
*Correspondence: daniel.rodriguez@unimilitar.edu.co (D.R.); ericsson.coy@unimilitar.edu.co (E.C.-B.);
Tel.: +57-6500000 (ext. 3269) (D.R.); +57-6500000 (ext. 3270) (E.C.-B.)
Received: 1 July 2019; Accepted: 3 August 2019; Published: 7 August 2019


Abstract:
Tetranychus urticae Koch is a phytophagous mite capable of altering the physiological
processes of plants, causing damages estimated at USD$ 4500 per hectare, corresponding to
approximately 30% of the total cost of pesticides used in some important crops. Several tools
are used in the management of this pest, with chemical control being the most frequently exploited.
Nevertheless, the use of chemically synthesized acaricides brings a number of disadvantages, such as
the development of resistance by the pest, hormolygosis, incompatibility with natural predators,
phytotoxicity, environmental pollution, and risks to human health. In that sense, the continuous
search for botanical pesticides arises as a complementary alternative in the control of T. urticae Koch.
Although a lot of information is unknown about its mechanisms of action and composition, there are
multiple experiments in lab conditions that have been performed to determine the toxic eects of
botanicals on this mite. Among the most studied botanical families for this purpose are plants
from the Lamiaceae, the Asteraceae, the Myrtaceae, and the Apiaceae taxons. These are particularly
abundant and exhibit several results at dierent levels; therefore, many of them can be considered as
promising elements to be included into integrated pest management for controlling T. urticae.
Keywords:
Tetranychus urticae; resistance; botanical pesticides; acaricide; integrated pest management
1. Introduction
One of the most important pests in commercial crops worldwide is the polyphagous, two-spotted
spider mite, Tetranychus urticae Koch. This mite is able to alter the physiological processes of plants,
reducing the area of photosynthetic activity and causing the abscission of leaves in severe infestations [
1
].
The cost of damages caused by this pest in crops such as beans, citrus, cotton, avocado, apples, pears,
plums, and many other horticultural and ornamental crops are estimated at over USD$ 4500 per
hectare. Such costs correspond to 30% of the total cost of pesticides in crops of ornamental flowers.
This constitutes a spending of almost 62% of the global market value on T. urticae Koch control based
on data of 2008 [
2
]. The main tools used to control this pest are chemically synthesized acaricides.
However, this mite is known to generate a resistance to these chemicals in a short period of time [
3
].
In addition, when the T. urticae Koch is exposed to sublethal pesticide levels, this mite has the ability to
increase its reproduction rate, thus its populations increase in a shorter time [
4
]. Furthermore, many of
the active ingredients in pesticide formulations are incompatible with the T. urticae Koch’s natural
predators; consequently, when they are applied to crops, they suppress populations of predators that
can contribute to the decrease of phytophagous mites [5].
Courtesy of the above-mentioned issues—together with problems related to environmental
contamination, the risk for human and animal health, and phytotoxicity—it is necessary to complement
Plants 2019,8, 272; doi:10.3390/plants8080272 www.mdpi.com/journal/plants
Plants 2019,8, 272 2 of 51
the control of T. urticae Koch with tools other than chemically-synthesized acaricides, such as biological
control and the use of botanical pesticides (plant extracts), a growing alternative for the control of this
pest. From the perspective of locating new options for the control of two-spotted spider mites, the use
of botanical pesticides represents a useful tool with minimal detrimental eects on the environment,
a low residuality, a slight induction of resistance due to its complex matrix, and with fewer harmful
eects on human health when compared to those of the chemically-synthesized acaricides. Therefore,
in the present review, a survey is presented based on some characteristics of T. urticae Koch behavior
in the presence of toxic substances. In addition, this review builds upon other studies in order to
determine the biological activity of some botanical pesticides on the phytophagous mite T. urticae Koch
under laboratory conditions.
2. Characteristics of T. urticae
The T. urticae Koch is the most abundant and the most widely distributed species of the genus
Tetranychus. This genus presents a confusing taxonomy due to partial reproductive incompatibilities
that have been found in some populations. It is known that, in certain cases, these incompatibilities are
caused by species of bacteria from the genus Wolbachia [6].
The individuals of the T. urticae Koch are characterized by having two spots on their back (dorsal
idiosome), green or brown coloration, and white or yellow colored legs [
4
]. They present sexual
dimorphism, as males are smaller than females [
4
]. An important feature of this species is that it is
is able to form a web on the plants in which it grows [
4
]. These mites feed initially on the leaves
of the lower part of the plants, but they can later colonize the rest of them as the population grows.
The damage they cause is observed in the form of chlorotic spots and, in some cases, the tanning of
leaves and defoliation [4].
2.1. The Biology of T. urticae Koch
The life cycle of the family Tetranychidae includes the stages of egg, larva, protonymph,
deutonymph, and adult [
7
], between each of which a quiescent state usually occurs. Their eggs are
round, white, or translucent, and the duration of their cycle depends on the temperature, the relative
humidity, and the host plant in which they develop. Under temperature conditions between 25 and
30
C, the T. urticae Koch can complete its cycle between three and five days [
8
,
9
]. The eggs are
approximately 0.13 mm in diameter. The larvae are spherical or oval in shape, generally greenish
yellow with three pairs of legs, and their size is approximately 0.16 mm in length. The protonymphs
have an oval shape and a pale green color. They are distinguished from larvae by having four pairs
of legs, and their length is approximately 0.2 mm. In the case of deutonymphs, they reach a length
of approximately 0.3 mm and have a yellow or light brown color. At this stage, two dark brown
spots usually appear on the dorsal level. On the other hand, adults have a globular or oval shape
and range from pale green to reddish yellow in color; adults present two red or dark brown spots
on the idiosome. Males are smaller than females, with lengths of 0.4 and 0.5 mm, respectively [
7
,
10
].
This species is arrhenotokous [
8
], which increases the probability that a female will mate with her
ospring. According to some authors, its high genetic variability allows it to adapt quickly and
decreases its probability of expressing deleterious mutations [9].
2.2. Characteristics of Resistance of T. urticae Koch to Acaricides
The T. urticae Koch is a widespread polyphagous pest that attacks more than 1100 dierent
plant species [
9
,
11
], making it one of the main phytosanitary problems for many crops. This trait is
owing (among other reasons) to its capacity for quickly generating resistance to synthetic acaricidal
products [12]—from two to four years of new active ingredients [9]—even after a few applications of
the active ingredient [11].
This resistance capacity to pesticides of the T. urticae Koch has encouraged some researchers to
carry out several studies regarding their genetic characteristics in response to the pressure generated
Plants 2019,8, 272 3 of 51
by the use of acaricides. Such is the case of Grbi´c et al. (2011) [
9
], who carried out a deep analysis of
the T. urticae Koch genome. They found that more than 10% of their genome comprises transposable
elements (9.09 Mb). In the same study, they also observed the presence of several families of genes
involved in digestion, detoxification, and transport of xenobiotic compounds with a unique composition.
Eighty-six genes encode for cytochromes P450, a group of 32 genes encode for glutathione S-transferases
(GST) (12 of these are believed to be unique to vertebrates), and 39 genes encode for drug-resistant
proteins of the ABC transporters type (ATP-binding cassette). This repertoire of transporter proteins
greatly exceeds the number presented by crustaceans, insects, vertebrates, and nematodes.
All these detoxifying enzymes are closely related to the resistance of T. urticae Koch, but this is not
the only mechanism used by these mites to counteract the eect of xenobiotics. A set of mutations in
the action points of pesticides is another way they are able to mitigate the eect of these compounds.
Demaeght et al. (2014) [
13
] reported a resistance case for this species when there was a mutation in
quitin synthase 1, which is the target enzyme of etoxazole. Additionally, because of its similarity to the
mechanism of action of hexythiazox and clofentezine, this mutation can cause a cross-resistance to these
products. Table 1shows an example of the eects of 10 dierent acaricides on four dierent populations
of T. urticae Koch in the state of Pernambuco (Brazil) [
14
]. This information demonstrates the ability
of this pest to counteract the eects of dierent active ingredients, showing variable responses to the
same compounds in dierent regions.
Table 1.
The resistance of dierent populations of T. urticae Koch—from the state of Pernambuco
(Brazil)—to 10 dierent acaricides. Adapted from Ferreira et al. [14].
Acaricide Population NLC50 (mg/L) * LC95 (mg/L) * RR50
Diafenthiuron
Petrolina II 426 6.6 70 1
Piracicaba 484 10.7 105 1.6
Brejão 340 4053 93,708 619
Bonito 401 7732 133,440 1180
Milbemectin
Piracicaba 484 0.6 8.3 1
Petrolina II 455 5.4 101 9.9
Bonito 373 357 3726 650
Brejão 380 384 2386 700
Fenpyroximate
Piracicaba 315 22 341 1
Petrolina II 469 87 1929 4
Bonito 378 3246 10,014 200
Brejão 387 4343 16.234 150
Clorfenapyr
Piracicaba 424 1.3 9.3 1
Petrolina II 481 2.8 20.1 2.2
Brejão 477 735 4157 570
Bonito 524 4652 94.598 3600
Spirodiclofen
Piracicaba 401 16.4 1590 1
Petrolina II 547 37.5 370.870 2.3
Bonito 538 6401 127.750 390
Brejão 414 6586 56.390 400
Fenbutatin
oxide
Piracicaba 465 0.83 436 1
Petrolina II 538 1.72 1093 2.1
Bonito 477 293 52.892 350
Brejão 459 1705 197.990 2048
Propargite
Piracicaba 472 6.5 28 1
Petrolina II 397 15 66 2.3
Bonito 395 291 990 45
Brejão 391 622 4410 96
Plants 2019,8, 272 4 of 51
Table 1. Cont.
Acaricide Population NLC50 (mg/L) * LC95 (mg/L) * RR50
Hexythiazox
Piracicaba 416 2938 64.871 1
Petrolina II 404 4370 100.510 1.5
Brejão 440 12,700 605.400 4.3
Bonito 415 1384 381.630 4.7
Spiromesifen
Piracicaba 418 373 18.404 1
Petrolina II 487 487 17.752 1
Brejão 467 1388 42.781 3.7
Bonito 470 3201 90.424 8.6
Abamectin
Petrolina II 613 0.0011 0.033 1
Piracicaba 714 0.0084 0.066 8
Petrolina I 676 0.036 0.205 34.4
Gravatá787 0.041 1.66 39.3
Goiânia 584 1.79 27.9 1716
Brejão 610 118 3000 113.532
Bonito 693 326 3397 295.270
* LC
50
: the mortality-causing concentration of 50% of the test population. LC
95
: the mortality-causing concentration
of 95% of the test population. N
: the number of mites used in the trial. RR
50
: the resistance proportion between the
resistant population and the susceptible one at LC50.
Function of Detoxifying Enzymes
Cytochrome P450 has been extensively investigated, as it is the most important group of detoxifying
proteins in arthropods [
15
]. This enzyme group has been linked to cases of resistance in the common
fly, Musca domestica L., with resistance to those furanocoumarins produced by a host plant in Papilio
polyxenes Fabricius [
15
], and in cases of resistance to abamectins in T. urticae Koch [
16
]. One of
the characteristics of this group of proteins in arthropods is their inducibility over time, which is
proportional to the consumption of certain toxic compounds from the plants that serve them as
food. Such is the case of the Spodoptera frugiperda Smith. In this species, it was demonstrated that,
when consuming a diet containing indole-3-carbinol, in time and with the increase in the concentration
of this compound, there was an increase in the production of P450 enzymes [15].
Another group of proteins that is important in the response to xenobiotics is the
Glutathione-S-Transferases (GST) family. Among these proteins, two enzymes belonging to the
delta class—tuGSTd10 and tuGSTd14—and one of the mu class—tuGSTm09—are present in T. urticae
Koch. They are strongly associated with mite resistance to the active ingredient abamectin [
17
].
Similarly, Pavlidi et al. (2017) [
18
], through molecular docking analysis and implementation of
HPLC-MS, deduced that the active ingredient cyflumetofen and its de-esterified metabolite could be
transformed by the enzyme TuGSTd05 in the same mite species.
On the other hand, Merzendorfer (2014) [
19
] and Dermauw and Van Leeuwen (2014) [
20
]
mentioned the presence of 104 genes belonging to subfamilies of ABC genes in T. urticae Koch.
This number is higher than that of other dierent species such as Homo sapiens L., Apis mellifera L.,
Drosophila melanogaster Meigen, Anopheles gambiae Giles, Bombyx mori L., Tribolium castaneum Herbst,
Pediculus humanus L., Daphnia pulex Leydig, Caenorhabditis elegans Maupas, and Saccharomyces cerevisiae
Meyen ex EC Hansen, demonstrating its importance within this species. This group of genes has also
been related to the development of elytra and wings in some insects and to the transport of certain
drugs of hydrophobic origin. The type of transport of compounds of these proteins has been elucidated
through models constructed by crystallography, for which it is known that they act as proteins of
import, export, or as flipases [19].
2.3. Relationship Between Resistance and the Host Plant
The dierent mechanisms of resistance presented by the T. urticae Koch suggest that these
adaptations may not be due exclusively to the pressure generated from the use of pesticides.
Plants 2019,8, 272 5 of 51
This question was asked by Dermauw et al. (2012) [
21
], who made an interesting finding when
studying the transcriptome of resistant and susceptible strains of the T. urticae Koch in the presence of
dierent host plants.
In that study, they demonstrated that a susceptible strain of this phytophagous mite was capable
of expressing diverse deactivated genes when it was relocated from a bean to a tomato as its host
plant [
21
]. In addition, the number of expressed genes that are related to the generation of resistance
increased considerably, going from 13 genes—expressed after two hours from host plant change—
to 1206 genes after five generations. On the other hand, they compared the transcriptome of two
resistant strains and that of the susceptible strain developed in the tomato. They also found that both
mite strains shared the expression of a significant number of genes related to resistance (Figure 1).
This seems to indicate that there is a strong relationship between the resistance mechanisms developed
by the T. urticae Koch and its host plants. These mechanisms may be similar to those developed by this
species to face exposure to dierent pesticides.
Figure 1.
A graphical representation of the study performed by Dermauw et al. (2012) [
21
]. (
a
) represents
the transcriptional changes in the susceptible London strain of the T. urticae Koch when changing host
plant. (
b
) represents the number of genes expressed in two resistant strains and the susceptible London
strain of T. urticae Koch after 5 generations from the relocation to another host plant. The scheme was
constructed by R.A. Rincón for this review from the data published by Dermauw et al. (2012) [21].
Evidence of the resistance capacity of this phytophagous mite is shown in Table 2. A list of
important pest arthropod species is shown, reporting the number of active ingredients to which they
developed resistance until the year 2012 [
22
,
23
]. The list is led by the T. urticae Koch, a species that
showed a reported resistance to 93 active ingredients until that moment.
Owing to the large number of reports of resistance existing for the T. urticae Koch, some studies have
provided important information and promising aspects in terms of understanding the resistance with
promising results. Such is the case of the research conducted by Demaeght et al. (2013) [
24
] concerning
cross-resistance. They studied two T. urticae Koch strains that were resistant to Spirodiclofen—an active
ingredient belonging to group 23 of the IRAC (i.e., inhibitors of acetyl CoA carboxylase). Although
strains appeared to be strongly resistant to this ingredient, they had a very low cross-resistance to
spirotetramat and spirodiclofenenol. This information could serve as a base for the understanding of
some routes of resistance-generation in this phytophagous mite, because they demonstrated that the
spirodiclofen detoxification route aects—at least partially—all of the tetranic and the tetronic acid
derivatives in the T. urticae Koch.
In the same study, Demaeght et al. (2013) discarded resistance to spirodiclofen by active site
mutations after aligning the sequences of active sites from target proteins with BlastP [
24
]. However,
Plants 2019,8, 272 6 of 51
when microarrays were made to express the genome of the studied strains and subsequently compared,
they found similarities in several genes expressed among the spirodiclofen resistant strains, which were
identified as P450 family proteins, carboxylesterases, glutathione S-transferases, transport proteins,
lipocalins, and several proteins without homology in the available databases. This fact demonstrated
that this detoxifying route is strongly related to the response of the T. urticae Koch to this ingredient.
On the other hand, Kwon et al. (2012) [
25
] detected a fitness decrease of T. urticae Koch strains that
demonstrated Monocrotophos resistance. Although the presence of more than one mutation increased
the resistance up to 1165-fold, these modifications in genes significantly decreased the catalytic capacity
of acetyl cholinesterase, thus gene overexpression seems to be necessary in order to compensate for
deficiency acquired by resistance-conferring mutations to the acaricide.
Table 2.
A list of pest arthropods based on the reported number of active ingredients resistance and
the number of reported cases per species—adapted from Van Leeuwen et al. (2010, 2012) [
22
,
23
].
The information for the species Plutella xylostella L., Myzus persicae Sulzer, Leptinotarsa decemlineata Say,
Blatella germanica L., and Panonychus ulmi Koch correspond to the cases reported up to 2010.
Species Taxonomy Kind of Pest Number of Active
Ingredients
Cases of
Resistance
Tetranychus urticae Koch Acari: Tetranychidae Crop 93 389
Plutella xylostella L. Lepidoptera: Plutellidae Crop 81 437
Myzus persicae Sulzer Hemiptera: Aphididae Crop 73 320
Leptinotarsa decemlineata Say Coleoptera: Chrysomelidae Crop 51 188
Musca domestica L. Diptera: Muscidae Urban 53 266
Blatella germanica L. Blattodea: Blatellidae Urban 43 213
Rhipicephalus microplus
Canestrini Acari: Ixodidae Cattle 43 158
Helicoverpa armigera Hubner Lepidoptera: Noctuidae Crop 43 639
Bemisia tabaci Gennadius Hemiptera: Aleyrodidae Crop 45 428
Panonychus ulmi Koch Acari: Tetranychidae Crop 42 181
Varroa destructor
Anderson y trueman Acari: Varroidae Bees parasite 2 10
Ixodes scapularis Say Acari: Ixodidae Cattle 0 0
Culex pipiens L. Diptera: Culicidae Disease vector 36 161
Culex quinquefasciatus Say Diptera: Culicidae Disease vector 32 256
Tribolium castaneum Herbst Coleoptera: Tenebrionidae Stored-grain pest 32 113
Aedes egypti egypti L. Diptera: Culicidae Disease vector 24 267
Spodoptera frugiperda Smith Lepidoptera: Noctuidae Crop 16 25
Pediculus humanus L. Phthiraptera: Pediculidae Disease vector 9 59
Anopheles gambiae Giles Diptera: Culicidae Disease vector 3 39
Manduca sexta L. Lepidoptera: Sphingidae Crop 3 4
Rhodnius prolixus Stal Hemiptera: Reduviidae Disease vector 3 3
Anopheles darlingi Root Diptera: Culicidae Disease vector 1 2
Linepithema humile Mayr Hymenoptera: Formicidae Urban 2 2
3. Control Strategies for T. urticae Koch
In agricultural crops, the main pest control method used is the spraying of solutions based on
chemically synthetic products such as insecticides and acaricides [
26
]. Although this method has
been eective in some cases for T. urticae Koch control, it has also demonstrated serious limitations
and disadvantages, especially due to T. urticae Koch’s high reproductive potential. This peculiarity
encourages farmers to use acaricides in larger volumes and doses, causing high levels of toxic waste in
fruits, the development of resistant populations, the intoxication of mammals, and the destruction of
beneficial organisms [23,27,28].
Another strategy used for T. urticae Koch management is biological control. Among the predators
of this pest are some mites of the family Phytoseiidae. Within this family, two predators stand
out—the Neoseiulus californicus McGregor and the Phytoseiulus persimilis Athias-Henriot. These mites
are characterized by consuming a large number of prey at adequate conditions and having high
reproductive rates and a capacity for rapid development [
4
]. Other natural predators that are less
Plants 2019,8, 272 7 of 51
commonly used for the control of this mite are the beetle Stethorus punctillum Weise (Coccinellidae)
and the Conwentzia psociformis Curtis (Neuroptera: Coniopterygidae)—which are found naturally
in Spain [
29
]—purely to mention some of the predators of this phytophagous species. Additionally,
the fungus Neozygites floridana Weiser and Muma has also exhibited significant control over the T. urticae
Koch, but some diculties in cultivation have hampered its use [
30
]. However, other fungi such as
the Lecanicillium lecanii Zimmermann and the Beauveria bassiana Bals.-Criv., as well as the bacterium
Bacillus thuringiensis Berliner, have been commercially used for the management of the two-spotted
spider mite with positive eects.
3.1. Other Methods for T. urticae Koch Control
As complementary strategies, these mites are controlled in some crops through the application of
water washings and the manual massaging of the aected leaves using water and soap in order to
remove the mites from the plant, kill them mechanically, and break their webs. Within the strategies
used for controlling the T. urticae Koch, biopesticides based on plant extracts or phytochemicals
are considered to be another alternative to chemically-synthesized acaricides [
31
,
32
], which have
also emerged as a complement to traditional management. This has allowed the development of
commercial products with formulations based on substances of natural origin, such as CinnAcar
®
,
Biodie
®
and PHC Neem
®
, which are produced from compounds and mixtures isolated from plant
extracts. As an example for this case, they have demonstrated compatibility with the natural
predator Tamarixia radiata Waterston (Hymenoptera: Eulophidae)—parasitoid of the Diaphorina citri
Kuwayama (Hemiptera: Psyllidae)—thus these formulations may constitute excellent alternatives to
be included into integrated management programs (IPM) of the so-called “Asian citrus psyllid” [
33
].
Therefore, the fact that these botanical pesticides are compatible with natural predators becomes
an advantage in the control of pests and constitutes an additional tool that can be used in integrated
pest management strategies.
An essential prerequisite for success when using extracts as a control strategy for pests is their
compatibility with other management strategies. Within the context of the IPM, a relevant issue is the
evaluation of how this type of product can aect biological control agents. In the particular case of
the T. urticae Koch, a question arises about how phytoseiid mites that have been successfully used as
a control strategy could be aected—a topic that has been explored by dierent researchers. Among
the botanical pesticides, probably the most used are the neem derivatives, a trend that is also present
in the case of the T. urticae Koch. A moderate reduction in female survival and fecundity in response
to Azadirachtin use on P. persimils Athias-Henriot was reported by Duso et al. (2008) [
34
], although
a positive shift in favor of the predator in terms of the predator–prey interaction can be inferred,
since azadirachtin was more toxic to the T. urticae Koch. A moderate eect was also reported by Spollen
and Isman (1996) [
35
], who found a maximum mortality of 14% in P. persimils Athias-Henriot adults
sprayed with neem extract. Although variables such as egg eclosion, the mean number of eggs laid per
female, and dierences in preference between treated or untreated leaves were not found, the authors
concluded that neem-derived insecticides could be eective and safe. Neem pesticides have exhibited
few negative impacts on the phitoseids N. californicus McGregor [
36
], Euseius alatus De Leon [
37
],
and Phytoseiulus macropilis Banks [
36
,
37
]. On the other hand, the negative eects of NeemAzal-T/S
in terms of its potential impact on populations of the predator Metaseiulus occidentalis Nesbitt were
reported by Yanar (2019) [
38
], who recommended the use of low concentrations of this product in cases
where the M. occidentalis is a relevant component of IPM. Regarding another plant species used to
obtain botanicals, crude extracts of Artemisia judaica L. exhibited acaricidal bioactivity against T. urticae
Koch in terms of LC
50
, while its negative impacts upon P. persimils Athias-Henriot were clearly lower,
suggesting that such extracts are compatible with the predaceous mite [
39
]. Similarly, a promising
toxic eect of the Melissa ocinalis L. on T. urticae Koch has been reported, along with an LC
50
for
the N. californicus McGregor, which is comparatively extremely lower. Undertaking compatibility
evaluations between extracts and natural predators is essential, since there is no reason to generalize
Plants 2019,8, 272 8 of 51
slight or innocuous eects of these products on said beneficial organisms. Commercial formulations
and application rates similar to those used by farmers are needed in order to obtain results with more
predictive value in respect of those expected in the field. Sublethal eects will also be a subject of
relevant research in the future, because, although many of the evaluations that demonstrate little or
no eect on the natural predators have been carried out in adults, the sublethal eects could raise
compatibility issues that are not evident when restricting evaluations to adult individuals [40].
3.2. The Use of Plant Extracts for the Control of T. urticae Koch in The Field
There are many studies regarding the use of plant extracts for the control of the T. urticae Koch.
Although many of these trials have delivered successful results, others have not demonstrated the level
of expected control over this mite species. For that reason, a greater understanding of the mechanisms
of action presented by molecules that demonstrate biological activity on these mites and the way in
which these molecules interact is highly required. In addition, the toxic eects of such molecules are
generated in many cases by the presence of several toxic compounds contained in the same extract,
which act in a synergistic manner. An understanding of these factors will help to foster a broader
understanding of the use of this tool in the control of the two-spotted spider mite. Further studies
must take into account the results of the studies developed thus far, which have delivered promising
results, not just in terms of the toxic eects demonstrated on these mites, but also in terms of sublethal
eects such as low fecundity and repellency.
3.2.1. Methods for the Evaluation of Extracts under Laboratory Conditions
The methods of testing the eects of extracts are very much the same as those used thus far for
evaluations of chemical compounds. An important prerequisite for making appropriate evaluations is
having a susceptible population of individuals. Generally, this population can be obtained by rearing
individuals that have not been exposed to any type of chemical substance with a possible acaricidal
eect for a considerable number of generations [
5
,
41
43
]. Additionally, the origin and the type of the
selected plant material must be clearly defined in order to ensure the repeatability of results. Hence,
correct taxonomic classification, location, season of the year, time of day, phenological stage, and organs
to be collected and processed in order to obtain the extracts aect the particular composition of the
tested botanical and influence the acaricidal activity [
5
,
44
46
]. Finally, the type of preparation and the
extracting protocol are also crucial steps for obtaining a standardized mixture of plant-based compounds,
which would be the source of eective botanical-based acaricidal or repellent agents. Thus, solid–liquid
(S–L) extractions—i.e., the selected plant material directly enters into contact with the extracting
solvent during a defined period through a continuous (maceration) or discontinuous (percolation or
Soxhlet) procedure—are the most commonly used method for obtaining dierent types of extracts,
depending on the polarity of the extracting solvent. In order of polarity, water, water/ethanol mixture
(hydroalcoholic), ethanol/methanol, chloroform, ethyl acetate, and hexane are the most commonly
used solvents for extractions. Other types of preparations are essential oil (usually obtained by steam
distillation) or low-polar/volatile extracts (aorded by hydrodistillation, supercritical fluid extraction,
microwave or ultrasound-assisted hydrodistillation, among others) [
47
]. The physicochemical nature
of these naturally occurring compounds, which are present in the preparation (extract or essential oil),
is the critical prerequisite information required to identify the extracting procedure. The purification or
the isolation of the active principles requires several steps, usually using preparative techniques such as
column chromatography under a bioguided fractionation strategy—although the isolated compounds
might be separately assessed after a conventional purification protocol. In any case, these eorts could
aect upon acaricidal rather than repellent activities to facilitate mite control, but this choice depends
of the aims of use. Essential oils often exhibit repellent activity in comparison to extracts, owing to
their volatile nature.
Plants 2019,8, 272 9 of 51
3.2.2. Bioassays
The purpose of bioassays is to determine the eect of a given agent on the physiology of
an organism, which, in the context of acari research, is generally associated with determining the
toxicity of a chemical compound—or resistance to it—either in the field or in laboratory conditions [
48
].
Repeatability of results, practical facilities, and conditions as similar as possible to those under which
the acaricide will be used are desirable [
49
]. In the case of mites, a small size and fast movement
are aspects conditioning the bioassay design. The main aspects of some common bioassays used for
the evaluation of botanicals on T. urticae Koch adults (generally females) and their advantages and
disadvantages are described below.
Slide Dip Methods
An initial method was described by Voss (1961) [
50
] as part of an acaricide screening procedure.
Double-sided Scotch
®
tape is adhered on one of its sides to a microscope slide. It is important to avoid
bubbles or empty spaces between the tape and the glass, because deposits of the substance under
evaluation could be formed, which could aect the test results [
51
]. After this, the mites must be axed
to the other side of the tape by the dorsal part of the hysterosoma. A fine brush is usually used to
transfer individuals to the tape. The slides are then dipped into the solution containing the toxicant for
5s[
48
,
51
] and, after this, are placed on a paper towel. It is important to remove any excess of liquid with
filter paper. After this, the slides are placed on trays covered with slightly moistened disposable towels,
which must then be taken into controlled conditions. The mortality criterion in the dierent methods is
usually an absence of movement when the individual is gently prodded with a fine brush. High control
mortalities due to desiccation and an absence of food are common in this method for times of evaluation
greater than 24 h, limiting the accuracy of the response parameters. Furthermore, individuals are
exposed to toxicants in an artificial substrate, and in some cases, problems distinguishing alive and
dead mites arise [
48
]. Despite such problems, this method has been used repeatedly to determine
the eect of botanicals on adults of the T. urticae Koch, in some cases considering evaluation times
of 24 h [
52
], but in other cases employing higher evaluation times [
41
,
52
57
]. An advantage of this
method is that the results obtained are highly reproducible. It can also be modified by employing
a spray tower to supply the toxicant, which allows for a better coverage [58].
Petri Dish Methods
The main variant is the Petri Dish Residue-Potter Tower Method (PDR-PT), in which the bottom
and the top inner surfaces of a Petri dish are sprayed with the toxicant using a Potter Tower and
allowed to dry for around 30 min at room temperature. After this, the individuals are transferred to
the dishes using a fine brush. For this method, high mortalities after 48 h have been reported, thus it is
advisable to restrict the evaluation time to shorter periods, such as 24 h [
59
]. The petri dish methods
have been used in some cases for the evaluation of botanicals against T. urticae Koch [3,60].
Leaf Disc Methods
For this kind of bioassay, leaf discs of variable diameter (approximately 20 mm) are cut from leaves
of several plant species, such as beans [
1
,
43
,
46
], peaches [
48
], or roses [
3
], and placed upside down in
a Petri dish containing moistened cotton wool when bean or rose leaf discs are used or a semi-solid
agar pad in the case of peach leaf discs. A variable number of adults (between five and 20) must be
transferred to each leaf disc using a fine brush. The experimental assembly is maintained without
disturbance for at least one hour before the spraying of the toxicant is performed. This spraying can be
performed using an airbrush, provided the required distance—as well as the number of drops/cm
2
and
the pressure—may be adequately standardized [
61
], which corresponds to the basic Leaf Disc Direct
Method (LDD). This method can be improved employing the Potter spray tower, derivating in the
so-called “Leaf Disc Direct-Potter Tower Method” (LDD-PT) [
48
]. This device was developed by C.
Plants 2019,8, 272 10 of 51
Potter from the Rothamsted Experimental Station [
62
], and it is recognized as a reference standard
for making chemical sprays under laboratory conditions, since it enables the achievement of an even
deposition of spray in the target area. The LDD and the LDD-PT methods can also be used to evaluate
the eect of a residual film of the toxicant on adults placed on a sprayed surface (such as a leaf disc in
this instance). In this case, the procedures are named “Leaf Disc Residue Method” (LDR) and “Leaf Disc
Residue-Potter Tower Method” (DR-PTM) [
48
]. Both a direct spray and the residual film are intended
to evaluate the toxic eects generated by contact between the individual mites and the test substance.
After the spray, Petri dishes are kept uncovered for around 30 min, which allows for the drying of the
leaf disc surface. They are then covered and placed under controlled conditions. Generally, mites that
cannot walk a distance equivalent to their body length are considered dead. Since the leaf disc method
implies the presence of the natural substrate of spider mites, it can be considered to have a greater
similarity with field conditions than the slide dip or the petri dish methods. However, one drawback
is the escape of individuals. This problem intensifies when the toxicant requires a prolonged time
to act or when it should be ingested in the feeding process. The fate of individuals that escape is
uncertain, thus the most advisable procedure is to discard them in the analysis; to consider them as
part of the mortality rate would not be justifiable [
48
]. An alternative approach is the development of
methods that do not allow for the escape of individuals, as proposed by Bostanian et al. [
63
]. In their
setup, a large leaf disc (50 mm in diameter) is placed upside down and tightly fitted to the bottom
of a plastic Petri dish of the same diameter, thus it occupies the whole dish. The base of each petri
dish contains thinly moistened cotton wool (1.5 mm in thickness) to prevent desiccation. A circular
window of 28 mm is cut in the top of the Petri dish to facilitate air circulation and avoid condensation.
For bioassays involving tetranychyds, they recommend covering the window with a 40
µ
m polyester
mesh screen to avoid run-o. The edges of the Petri dish bottoms are wrapped with masking tape
to ensure a strong grip on the top, preventing the escape of individuals. A small hole in the lower
half of the Petri dish allows the petiole to protrude outwards, where it must be covered with a wet
cloth. This method enables observations for a period as long as nine days, which makes it suitable for
slow- and fast-acting reduced-risk toxicants. A dierent variant of the leaf disc method is the Leaf
Disc-Residue Dipping Method (LDR-D), in which the leaf discs are dipped into the solution containing
the toxicant [
64
]. Although estimations of lethal concentrations obtained by this method are less precise
when compared to the LDD-PT, this fact could be explained by an uneven distribution of residues on
the leaf surface. The leaf disc methods have been widely used in several trials of botanicals against
T. urticae Koch [5,40,5462].
Leaf Absorption Method
In this method, the leaf is placed in some kind of recipient containing the toxicant solution in
order to allow the absorption by the leaf for an adequate period (usually around 72 h). The leaf is then
located in a Petri dish containing agaropectin to prevent desiccation, and the mites are transferred onto
the leaf, where they are allowed to feed by 24 h, and mortality is then evaluated. The design of the
experimental unit should consider alternatives to prevent the escape of mites, as discussed in the leaf
disc method [42,63].
Whole Plant Direct Method
The purpose of this kind of bioassay is to evaluate the direct eect of toxicants under conditions
as similar as possible to those of the field. Young bean plants with 2–3 leaves can be used, and the
apical part of the plant must be removed to prevent the appearance of new leaves, which have not
received the treatment. Adult females are then placed in the plants long enough before performing the
application in order to allow oviposition. Alternatively, a specific number of immature stages and
adults can be placed in the plants. The spray of the toxicant is made using an atomizer, considering
an application volume similar to the required under crop conditions. The number of eggs, nymphs,
Plants 2019,8, 272 11 of 51
and adults is recorded at predefined evaluation times, usually between 5 and 10 days [
65
,
66
]. This
method has been also used to evaluate repellency [67].
Filter Paper Difussion Methods (Fumigant Bioassays)
This kind of assay is designed to evaluate the fumigant action of toxictants, thus it is essential to
avoid any direct contact between individuals and the toxicant. The setup is similar to that employed in
the leaf disc method, but the bottoms of the Petri dishes are covered using a tight-fitting lid with a fine
wire sieve. The toxicant is applied to filter papers, which should be allowed to dry before being placed
over the wire sieve [
68
]. In some cases, the paper is attached to the downside of the lid with a small
quantity of solid glue that should not aect individuals [42].
3.3. Studies Carried Out for the Control of T. urticae Koch from Plant Extracts Grouped by Plant Families
The investigations carried out, which focused on the eects of biopesticides on T. urticae Koch,
have led to the identification of a large number of plant extracts with acaricidal, repellent, and deterrent
properties. Below are descriptions of some species—grouped by plant families—whose plant extracts
have been used in laboratory studies that have exhibited their biological activity on the two-spotted
spider mite (the information is summarized and complemented in Table A1 in the Appendix A).
3.3.1. Family Amaranthaceae
This family has aroused interest in dierent areas such as traditional and alternative medicine,
given the properties that have been identified in some of the species that comprise it. Such is
the case of Achyranthes aspera L., whose secondary metabolites have antinociceptic activity [
69
],
or Chenopodium ambrosioides Mosyakin et Clemants, which has toxic eects that have been studied in
some human parasites [70].
Due to these toxic eects, Hiremath et al. (1995) [
71
] evaluated the acaricidal eect of the extract
of this plant. They compared the activity of the methanolic extracts obtained from 21 dierent species
of African plants against T. urticae Koch adults using the leaf immersion method. Among the most
active extracts, the whole plant of Celosia trigyna Linn. exhibited the highest biological activity, causing
mortality rates between 40% and 60% of evaluated mites.
Chiasson et al. (2004) [
41
] also evaluated the acaricidal eects of a species of this family.
They studied the eect of an emulsifiable concentrate—obtained from Chenopodium ambrosioides
Mosyakin et Clemants essential oil—on adults and eggs of the T. urticae Koch and the Panonychus
ulmi Koch and compared it with the eect obtained from the use of commercially available products.
The products were applied with an airbrush on females that were placed on microscope slides with
glue. In the case of eggs, the application was made on the eggs previously laid by females on leaf discs
located within Petri dishes. Thus, a dose of 0.5% produced a mortality of 94.7% in females, which was
higher than that obtained from the Neem extract (22.1%). Otherwise, hatching was diminished on days
five and nine after application. This hatching eect was lower in treatments with Neem, Abamectin,
and insecticide soap. A lower eect was observed for an ethanolic extract from seeds of Chenopodium
quinoa Willd. on adult females and nymphs of this mite, exhibiting an LD50 of 1.24% w/v [72].
Two years later, Shi et al. (2006) [
52
] evaluated the eect of Kochia scoparia (L.) Schrad extract
on T. urticae Koch, T. cinnabarinus Boisdu-Val, and T. viennensis Zacher using three dierent solvents
for extracting the compounds contained in the plant material: methanol, chloroform, and petroleum
ether. The mortality trials were carried out using three dierent methodologies: (1) the slide dip
method measuring mortality after 24 h of immersion, (2) the LDD-PT, and (3) the leaf absorption
method. Using these methodologies, the highest mortality of the T. urticae Koch was obtained with the
chloroform-soluble extract, which exhibited a 78.86% average mortality and an LC
50
of 0.88 using the
dipping method, in which mites were glued to an adhesive tape.
Plants 2019,8, 272 12 of 51
3.3.2. Family Amaryllidaceae
This family is studied widely due to its potential uses in the control of human diseases [
73
] as well
as its antitumor [
74
] and insecticides properties [
75
]. Abbassy et al. (1998) [
76
] determined the LC
50
of
the alkaloidal extract, the ethanolic extract, and the essential oil of the bulb of the ornamental plant
Pancratium maritimum L. (Amaryllidaceae) on the T. urticae Koch, whose values were 0.2%, 0.36%, and
1.5%, respectively.
The insecticidal properties demonstrated by various studies led Attia et al. (2011) [
77
] to expose
adult T. urticae Koch females to dierent concentrations of garlic extract (Allium sativum L.).
These concentrations ranged between 0.46 and 14.4 mg/L using the Potter Tower application. After the
bioassays, they determined the LD
50
and the LD
90
, whose values were 7.49 and 13.5 mg/L, respectively.
On the other hand, they concluded that fecundity was reduced by using the concentrations of 0.36
and 0.74 mg/L. Geng et al. (2014) [
78
] measured the toxicity by the contact and the repellency of the
garlic extract at 20, 10, 5, 2.5, and 1.25 g/L. From these tests, they found that treatment with 20 g/L
caused a 76.5% mortality rate on mites at 48 h after its application. Additionally, with the obtained
data, they calculated the regression equation of toxicity as Y =1.3 x +3.9. They were also able to
determine the LD
50
value, which corresponded to 7.2 g/L. Furthermore, the repellencies were found to
be 95.6% and 65.2% at extract concentrations of 10 g/L and 20 g/L, respectively.
3.3.3. Family Annonaceae
Within this group of plants, the presence of several important secondary metabolites involved in
the communication of arthropods and plants’ defenses against the attack of pests has been identified [
79
].
However, Ohsawa et al. (1991) [
80
] obtained negative results when using Annona glabra L. seed extract
on T. urticae Koch eggs. During their experiment, they dissolved 10 mg of the extract in acetone (1 mL)
and applied 0.5 mL of the solution to a bean leaf where the eggs were laid. After this, they noticed that
the extract demonstrated no impact on mortality rates, deterrence in feeding, or mite growth.
Pontes et al. (2007) [
44
] also demonstrated the acaricidal activity of the essential oils of this
family of plants, but in this case, they used the species Xilopia ser
í
cea A.St.-Hil., which was evaluated
on T. urticae Koch. Using gas chromatography–mass spectrometry (GC–MS), they identified the
compounds present in both leaves and fruits, finding mostly monoterpenes and sesquiterpenes.
When comparing their acaricidal activity, they concluded that the essential oils of the leaves exhibited
a greater toxicity than those obtained from the fruits.
3.3.4. Family Apiaceae
Plants of this family are widely used within the diet of dierent human communities [
81
], although
their nature is so varied that many species have been used as pesticides and repellents [
82
]. For example,
Choi et al. (2004) [
42
] tested the essential oils of 53 plants to determine their acaricidal potential on
T. urticae Koch eggs and adults. Among these oils, the highest toxicity was exhibited by species of the
family Apiaceae—i.e., Carum carvi L.—since a 100% mortality rate of adult mites was obtained. To carry
out this study, the researchers conducted bioassays by diusion on filter paper, avoiding any direct
contact between the oil and the mites. The tests were developed in a plastic container (4.5
×
9.5 cm) at
a concentration of 14 ×103µL/mL air.
Tsolakis and Ragusa (2007) [
83
] studied the eect of a mixture of essential oils from the C. carvi L.
with potassium salts of fatty acids on the T. urticae Koch and one of its predators, Phytoseiulus persimilis
Athias-Henriot. This combination proved to be very selective, since it generated a mortality rate of
83.4% in T. urticae Koch females compared to a 24% mortality rate in P. persimilis Athias-Henriot females.
Besides, the product also caused a decrease in the intrinsic growth rate of the phytophagous mite
while having no eect on the growth rate of the predator. Approximately four years later, this same
essential oil was tested by Han et al. (2010) [
68
] on the same species of mite. In this case, by using
Plants 2019,8, 272 13 of 51
mortality bioassays by vapor phase to evaluate fumigant eect (see section of Myrtaceae Family),
they established an LD50 of 22.4 µg/cm3air.
Among works carried out with plants of this family, Attia et al. (2011) [
43
] showed that the Deverra
scoparia Coss. & Durieu essential oil has an acaricidal eect and decreases the fecundity of the T. urticae
Koch. In the same study, they isolated the components of the oil and tested them individually on
the pest, obtaining the highest toxicities with the compounds
α
-pinene,
3
-carene, and terpinen-4-ol.
Amizadeh et al. (2013) [
84
] also decided to evaluate the eect on two species of this family of the
inhalation of essential oils. For this purpose, they carried out tests to determine the fumigant activity of
Heracleum persicum Desf. Ex. Fisch. essential oils and Foeniculum vulgare Mill. seeds on adult females and
eggs of the T. urticae Koch. The LD
50
s were 3.15
µ
L/L and 1.53
µ
L/L for females and eggs treated with
Heracleum persicum Desf. Ex. Fisch. essential oil, respectively, and 5.75
µ
L/L and 1.17
µ
L/L for females
and eggs treated with Foeniculum vulgare Mill. essential oil, respectively. Other essential oils obtained
from Apiaceae plants having acaricidal activity on T. urticae Koch were Cuminum cyminum L. (seeds)
and Ferula gumosa Boiss (leaves), showing LD50 values of 3.74 and 6.52 µL/L air, respectively [85,86].
On the other hand, Pavela (2015) [
65
] tested acaricidal and ovicidal eects of the methanolic
extract of Ammi visnaga (L.) Lamarck seeds on T. urticae Koch. The ecacy in terms of adult mortality
rates increased over time, with LD
50
s (after 72 h from the time of application) estimated at 17, 10,
and 98
µ
g/cm
2
for the extract and its two major compounds, khellin and visnagin (furanochromenes),
respectively. Moreover, the extract and the two isolated furanochromenes inhibited the development
of eggs and caused their mortality, with LD
50
s of 13.3, 0.5, and 1.8
µ
g/cm
2
for the extract, the visnagin,
and the khellin, respectively. The application of the extract to leaves infested with T. urticae Koch
achieved a reduction of the number of individuals in all stages of development. The concentration
of 10 mg/mL showed the highest ecacy, which was 98.5% on the tenth day since the application.
The terpenes isofuranodiene and germacrone, isolated from Smyrnium olusatrum L. inflorescences,
also exhibited toxicity on this mite (LD50s=1.9 and 42.7 µg/mL, respectively) [87].
3.3.5. Family Asteraceae
There have been numerous studies carried out with species from this group to evaluate their
acaricidal activity. First, Chiasson et al. (2001) [
45
] evaluated the essential oils of two plant species
known as potential pesticides—Artemisia absinthium L. and Tanacetum vulgare L.—to determine their
acaricidal activity against the T. urticae Koch. The oils were obtained via a microwave-assisted process
(MAP), distillation in water (DW), and by direct distillation with steam (DDS), and their relative
toxicities were tested by direct contact. All oils were tested at 1%, 2%, 4%, and 8% as emulsions
prepared in water with 9% denatured ethanol and 0.32% Alkamul EL-620 as emulsifier, and mite
mortality was evaluated after 48 h.
The three oils of A. absinthium L. were toxic to the T. urticae Koch; however, there were dierences
in their levels of toxicity. For example, the oil extracted by MAP and DW methods caused 52.7% and
51.1% mortality in the mites, respectively, while the oil obtained by DDS produced a mortality rate
of 83.2%. Consequently, the LC
50
of the oil extracted by DDS was lower (0.043 mg/cm
2
) than those
obtained by MAP (0.134 mg/cm
2
) and by DW (0.130 mg/cm
2
). The extracts of T. vulgare L. obtained
by DW and DDS exhibited greater acaricidal activity than the extract prepared by the MAP method.
At a concentration of 4%, oils delivered mortality rates of 60.4%, 75.6%, and 16.7%, respectively.
The chemical analysis of the extracts of T. vulgare L. indicated that the compound p-thujone is the
major compound in the oil (>87.6%) and probably contributes significantly to its acaricidal activity.
Additionally, the acetone extract from leaves of Artemisia judaica L. exhibited an LD
50
of 0.56
µ
g/mL
against adult females [39].
Trials that have shown acaricidal activity within this family have also identified important
compounds in essential oils that may play a role in the toxic activity against the T. urticae Koch. One of
these cases was developed by Attia et al. (2012) [
46
], who identified the terpinen-4-ol compound in
the Santolina africana Jord. & Fourr. essential oil. This compound was the most abundant component
Plants 2019,8, 272 14 of 51
(54.96%) within the study. They evaluated the acaricidal activity of the S. africana Jord. & Fourr. and
the Hertia cheirifolia (L.) Kuntze essential oils, with positive impacts upon the mortality rates of the
T. urticae Koch and important eects in the reduction of oviposited eggs.
In another study, this same group of researchers tested the eect of the Chrysanthemum coronarium L.
essential oil on the T. urticae Koch and produced mortality rates of 88% and 93% on larvae and adult
females, respectively [
88
]. In the same year, another paper was published by Afify et al. (2012) [
89
],
who tested the acaricidal activity of Chamomilla recutita L. extract on the T. urticae Koch. The LD
50
values
obtained for adults and eggs in this study were 0.65% and 1.17%, respectively. In this study, the authors
identified the main compounds of C. recutita L. by means of gas chromatography–mass spectrometry.
The most predominant compounds were
α
-bisabolol oxide (35.25%) and trans-
β
-farnesene (7.75%).
The essential oil from the aerial part of Achillea mellifolium L. showed LD
50
values of 1.208% v/vand
1.801
µ
L/L air when evaluated through leaf dipping and fumigation, respectively. The GC–MS chemical
profile of this oil was mainly composed of piperitone (12.8%) and p-cymene (10.6%) [64].
However, not all studies using species from this plant family obtained satisfactory results in terms
of the T. urticae Koch. For example, extracts obtained from Artemisia absinthium L.—known insecticides
and acaricides used throughout the world to control aphids—demonstrated weak activity upon the
T. urticae Koch, as reported by Aslan et al. (2005) [
90
]. Similarly, Derbalah et al. (2013) [
91
] found that
the extract of castor leaves (Artemisia cinae O. Berg & C.F. Schmidt ex.Plajakov) exhibited low toxicity
against the T. urticae Koch, with an LD
50
of 1326.53 ppm. Similarly, Pavela et al. (2016) [
92
] studied the
eect of the methanolic extract taken from leaves of the Tithonia diversifolia Hemsl. on T. urticae Koch
and its ethyl acetate fraction in order to measure acute and chronic toxicity as well as its inhibitory
eects on oviposition. In acute toxicity trials, mortality did not exceed 50%, even for the highest dose
evaluated (150
µ
g/cm
3
). On the other hand, in the chronic toxicity tests on the fifth day after application,
the LD
50
of the methanolic extract was 41.3
µ
g/cm
3
, and the LD
90
was 98.7
µ
g/cm
3
. However, the two
extracts caused inhibition in the oviposition of mites.
3.3.6. Family Boraginaceae
A low polar extract from roots of Onosma visianii Clem. demonstrated significant chronic
toxicity and oviposition inhibition on T. urticae Koch adult females (LD
50
=2.6
µ
g/mL). Eleven
naphthoquinone-type related compounds were isolated and structurally elucidated [
93
]. Although all
isolated derivatives exhibited eects against this mite, isobutylshikonin and isovalerylshikonin were
found to be the most active isolated compounds (LD50s=2.69 and 1.06 µg/mL, respectively).
3.3.7. Family Burseraceae
Several species belonging to this family exhibit anti-inflammatory properties [
94
]. They are
considered to be anticarcinogenic agents with antimalarial, antidiarrheal, and antifever properties and
uses as insecticides [
95
], antimicrobials, and antioxidants [
96
] (among others) for disease treatment [
95
].
However, some studies have pursued applications in agriculture, specifically for the management
of important pests. In that respect, Pontes et al. (2007) [
97
] studied the acaricidal and the repellent
eects of the Protium bahianum Daly plant resin oil on the T. urticae Koch by fumigant tests. For this,
they kept mites in leaf discs of Canavalia ensiformis (L.) DC. inside 9 cm Petri dishes as test chambers.
Each chamber had a strip stuck on the inner side that was saturated with dierent amounts and
concentrations of the oil (5, 10, 15, 20, and 25
µ
L, corresponding to 2, 4, 6, 8, and 10
µ
L/L of air,
respectively). They evaluated the fresh resin oil and the old resin oil separately. Results showed that
the fumigant eect of the oil in both cases increased with concentration and exposure times and had
mortality rates of 79.6% and 59.0% after 72 h for the old and the new resin oils, respectively. Regarding
the deterrent eect of oviposition, the fresh resin oil presented an increased activity, with only 14 eggs
oviposited at 72 h at a concentration of 10
µ
L/L of air. In repellency tests, only fresh resin oil showed
positive eect against mites.
Plants 2019,8, 272 15 of 51
3.3.8. Family Cannabaceae
Although this family of plants is recognized for its various pharmaceutical uses, little has been
studied about its eects as an insecticidal and an acaricidal agent. Among the studies that have been
performed, Yanar et al. (2011) [
60
] used the extract obtained from the flower buds of Humulus lupulus L.
on T. urticae Koch adults at 5% (adhesive tape method) and at 50% (residual film method). Using the
adhesive tape methodology (in which 1 mL of solution was applied to the tape left for 4 to 5 h to dry,
and 20 adult females were then placed on it), the mortality rate after 24 h was 67.84%
±
2.52%. On the
other hand, with the residual film methodology (in which the extract was applied to a 90 mm Petri
dish, distributed homogeneously, and left for 2 to 4 h to dry before the addition of 20 T. urticae Koch
adult females), the mortality observed after 24 h was 56.37%
±
0.99%. The acaricidal eect against this
mite of an essential oil from panicles of hemp (Cannabis sativa L.) was also evaluated, exhibiting 83.28%
of mortality on adult females at 0.10% [98].
3.3.9. Family Caryophyllaceae
The acaricidal eect of an aqueous extract from roots of Saponaria ocinalis was evaluated against all
developmental stages of T. urticae Koch [
66
]. The lowest sensitivity was found for adults (LD
50
=0.31%
w/v), while eggs revealed the highest sensitivity (LC
50
=1.18% w/v). Oviposition was also inhibited by
this extract (LC50 =0.91% w/v).
3.3.10. Family Combretaceae
There are several plant species of this group on which acaricidal activity studies of the T. urticae
Koch have been carried out—the majority of them successfully. An example of this is the study
performed by Hiremath et al. (1995) [
71
], who compared the activity of the methanolic extracts
obtained from 21 dierent species of African plants against adults of the T. urticae Koch using the leaf
immersion method. Among the results found, the Combretum micronthum G. Don. and the Piloitigma
vetilicolin whole plant extracts demonstrated eects on the rates of T. urticae Koch mortality of between
40% and 60%.
3.3.11. Family Convolvulaceae
There are few studies on the T. urticae Koch that involve this plant family, with plants of the genera
Convolvulus and Ipomaea being the most used. Chermenskaya et al. (2010) [
99
] studied the eect of
the species Convolvulus krauseanus Regel. and Schmalh. on three species of pest arthropods, among
which was the T. urticae Koch. From this study, which gathered the eect of extracts from 123 plant
species, they concluded that the C. Kraseanus Regel. and Schmalh. roots extract was one of the two that
showed the highest miticidal eect [together with the Ailanthus altissima (Mill.) Swingle leaf extract,
Simarubaceae], causing a mortality rate of 95.6% after seven days from the application (using the
immersion method).
3.3.12. Family Cupressaceae
Essential oils from two plants of this family were evaluated against adult females of T. urticae
Koch in the same study [
55
]. Oil from leaves of Cupressus macrocarpa Hartw. ex Gordon had an LD
50
of 5.69
µ
L/L air, whereas Thuja orientalis L. leaves resulted in an LD
50
of 7.51
µ
L/L air. The main
compounds in these essential oils were β-citronellol (35.92%) and α-pinene (35.49%), respectively.
3.3.13. Family Euphorbiaceae
The species of this family have not been well studied in terms of their pesticide properties. One of
the works carried out in this area was that of Dang et al. (2010) [
100
], who investigated the eect of
the dried root extract of Euphorbia kansui S.L. Liou ex S.B. Ho on the T. urticae Koch, as well as that
of two of its compounds separately: 3-O-(2,3-dimethylbutanoyl)-13-ododecanoilingenol (compound
Plants 2019,8, 272 16 of 51
1) and 3-O-(2
0
E, 4
0
Z-decadienoyl)-ingenol (compound 2). Concerning the extract, they found that it
generated mortality rates of 27% and 55% at concentrations of 3 and 5 g/L, respectively. When testing
the two compounds obtained by fractionation and evaluating them on mites, they determined that
compound 1 caused mortality rates of 45% and 59% when applied at 500 and 1000 mg/L, respectively.
In contrast, compound 2 showed no acaricidal activity during the study.
On the other hand, in 2015, Numa et al. (2015) [
61
] published a study in which they tested the
susceptibility of T. urticae Koch females to the Cnidoscolus aconitifolius (Mill) I.M. Johnst. leaf extract
using the leaf immersion methodology merged with direct application using an airbrush. In this
study, they determined that a dose of 2000
µ
g/mL was the only one that did not show dierences in
the positive control (based on chlorfenapyr as the active ingredient). This dose could be the most
appropriate for an extract formulation based of this plant during its potential use in the control of pests
in agricultural crops, taking into account the fact that it caused a 92% rate of mortality of mite females
in the trials.
3.3.14. Family Fabaceae
This family is well known as an aspect of human diets throughout the world. Several studies
have been carried out to evaluate the eects of their plant extracts on arthropods with very varied
results. These include the study performed by Hiremath et al. (1995) [
71
], who compared the activity of
methanolic extracts obtained from 21 dierent species of African plants against adults of the T. urticae
Koch using the leaf immersion method. The most active extracts were those obtained from the leaves,
the fruits, and the whole plant of Prosopis chinensis (Molina) Stuntz, which caused mortality rates
between 61% and 80% for the leaf extract and higher than 80% in the case of the extracts obtained from
the fruits and the whole plant. The plant oil of Millettia pinnata L. showed an LD
50
of 0.004% on adult
females after four days of testing [101].
3.3.15. Family Gramineae (Poaceae)
Although this family is made up of nearly 10,000 plant species, studies involving the eect of its
plant extracts on the T. urticae Koch have focused on only some of the 55 species that make up the
Cymbopogon genus [
102
]. In one of these cases, Choi et al. (2004) [
42
] included the oil from Cymbopogon
nardus (L) Rendle within the 53 essential oils that they evaluated on the T. urticae Koch. This oil
showed a positive result, causing a mortality rate greater than 90% on adults of this phytophagous
mite. In a study of another species of genus Cymbopogon, Han et al. (2010) [
68
] examined the eect
of Citronella Java oil on the T. urticae Koch, evaluating its fumigant eect. To do this, they took
disc-shaped bean leaves and placed them on moistened cotton contained in Petri dishes together with
T. urticae Koch adult mites. On each Petri dish, a mesh cover was placed and placed over this was filter
paper moistened with the essential oil. Under these conditions, the LD50 found was 22.5 µg/cm3.
3.3.16. Family Lamiaceae
The eects of plant extracts and essential oils from the species that make up this family have
been the most studied on the phytophagous mite T. urticae Koch. Among the studies reported in
the literature are, for instance, those from the species Rosmarinus ocinalis L. and Salvia ocinalis L.
The essential oils of these plants demonstrated eective control over populations of the T. urticae Koch
and a decrease in the number of oviposited eggs when concentrations increased [
53
]. In a similar way,
Choi et al. (2004) [
42
] performed trials using the S. ocinalis L. essential oil on the same species of mite,
obtaining an adult mortality rate of 82%. In the same study, they included another species from the
family Lamiaceae—Mentha spicata L.—from which they obtained the essential oil that was evaluated
on the T. urticae Koch. As a result, the mortality rate of these arthropods in the adult stage was 81%.
On the other hand, Rasikari et al. (2005) [
103
] carried out a screening of the leaf extracts of
67 species of plants belonging to the Lamiaceae family. They were evaluated on the T. urticae Koch,
which were applied by direct contact with the Potter Tower to bean leaves kept in Petri dishes with
Plants 2019,8, 272 17 of 51
cotton. From the extracts tested, 14 had a moderate to acute toxic eect on mites. From these, extracts
obtained from the plants Clerodendrum traceyi F. Muell., Premna serratifolia L., Ceratanthus longicornis
(F.Muell.) G. Taylor, Plectranthus habrophyllus P.I. Forst, and Plectranthus sp. Hann caused a 100%
mortality rate, whereas the extracts of Gmelina leichardtii F.Muell. & Benth, Premna acuminata R. Br.,
Viticipremna queenslandica Munir, Plectranthus diversus S.T. Blake, Plectranthus glabriflorus P.I. Forst, and
Plectranthus suaveolens S.T. Blake caused mortality rates that were between 90% and 99%.
In 2006, a study performed by Miresmailli et al. (2006) [
104
] was published. In that investigation,
they tested the eect of the R. ocinalis L. essential oil on the T. urticae Koch. For that, they took two
dierent populations of mites, one from bean plants and another from tomato plants. For the tests,
they used five dierent concentrations (2.5, 5, 10, 20, 40, and 80 mL/L) of the essential oil diluted in
methanol and water (70:30 v/v). In order to evaluate the mortality rates of mites, they took 3 mm
disc leaves within Petri dishes, to which they applied 20
µ
L of the treatment solution. Once dried
at room temperature, they placed five adult females on the leaves and kept them at a temperature
of 26
±
2
C, a relative humidity (RH) between 55% and 60%, and a photoperiod of 16:8 (light:dark).
From these assays, they determined that the LC
50
for the females maintained on bean plants was 10
mL/L, while for the females kept on tomato plants, it was 13 mL/L. Moreover, with a concentration of
20 mL/L, a mortality of 100% of females produced in bean plants was obtained, whereas a 40 mL/L
concentration was necessary before females on the tomato plants reached total mortality (100%).
Additionally, Miresmailli et al. [
104
] identified the components of R. ocinalis L. essential oil using
GC–MS by column chromatography and tested them individually on the T. urticae Koch. In the case of
mites reared on bean plants, two compounds revealed a significant toxicity—1,8-cineol and
α
-pinene
(with 88%
±
4.8% and 32%
±
4.8% mortality, respectively)—whereas for mites raised on tomato plants,
the same two compounds were those that revealed a significant toxicity. The resulting values were
80% ±6.2% and 72% ±4.8% for 1,8-cineol and α-pinene, respectively.
In a similar study, Çalma¸sur et al. (2006) [
105
] tested the eect of the vapors of three essential oils
from Micromeria fruticosa L., Nepeta racemosa L., and Origanum vulgare L. on nymphs and adults of the
T. urticae Koch and adults of the Bemisia tabaci Gennadius, finding the highest mortality rates (96.7%,
95%, and 95%, respectively, for T. urticae Koch, and 100% for B.tabaci Gennadius) when using doses
of 2
µ
L/L of air at 12 h of exposure. Han et al. (2010) [
68
] also studied several essential oils obtained
from species of this family. To do this, they evaluated its fumigant eects on the T. urticae Koch and,
as a result, obtained LD
50
s of 22.7, 22.8, 23.7, 38.8, 39.5, and 63.7
µ
g/cm
3
for Thymus vulgaris L., Mentha L.
piperita,Mentha pulegium L., Mentha spicata L., Ocimum basilicum L., and Salvia ocinalis L., respectively.
In 2012, Afify et al. (2012) [
89
] tested the acaricidal activity of Majorana hortensis Moench extract
on the T. urticae Koch. The LD
50
values obtained for adults and eggs in the trial were 1.84% and 6.26%,
respectively. In the study, they identified the main compounds of M. hortensis Moench by means of
gas chromatography–mass spectrometry as terpinen-4-ol (23.86%), p-cymene (23.40%), and sabinene
(10.90%)—the main compounds for this species. In the same year, Attia et al. (2012) [
88
] tested the
eect of the essential oil of Mentha pulegium L. on the T. urticae Koch, obtaining a mortality rate of 91%
in larvae and adult females. The same essential oil was evaluated by Choi et al. (2004) [
42
] on the same
mite species, in which a mortality rate higher than 90% was obtained. Within the same experiment,
they analyzed the eect of the essential oil of the Mentha piperita L., in which the mortality rate also
exceeded 90%. On the other hand, Amizadeh et al. (2013) [
84
] studied the fumigant eect of the
essential oil obtained from leaves of the Satureja sahendica Bornm. on eggs and adult females. The LD
50
obtained for females was 0.98 µL/L, while it was of 0.54 µL/L for eggs.
3.3.17. Family Meliaceae
The insecticidal properties of plants belonging to the family Meliaceae have been studied
extensively [
106
]. For this reason, Ismail (1997) [
107
] evaluated the relative toxicity of the extracts of
Melia azedarach L. and some synthetic acaricides against recently hatched larvae of the T. urticae Koch
and third-instar larvae of the predatory beetle, Stethorus gilvifrons Mulsant. The methanolic extract
Plants 2019,8, 272 18 of 51
of the plant was the most eective among the tested products, followed by the extracts of acetone
and petroleum ether. The toxicity of the plant material obtained was less active against the predator
compared to the eect it had on the two-spotted spider mite, in which a decrease in fecundity was
also observed. The study of the joint action of the products also revealed a strong synergy in the
bromopropylate mixture with the methanolic extract of the M. azedarach L. Interestingly, this mixture
demonstrated no eect on the predator.
In a similar way, Brito et al. (2006) [
37
] tested the toxicity of dierent commercial products
based on one of the plants with the highest pesticide potential, the Neem (Azadirachta indica A. Juss.).
It was tested not only on the T. urticae Koch but also on its predators, Euseius alatus DeLeon and
Phytoseiulus macropilis Banks. In this study, they found that the formulation of the product Neemseto
(1%) was the one that obtained the best result on the T. urticae Koch by topical contact. In the same
way, they tested the product at dierent concentrations (0.25%, 0.5%, and 1.0%) and found that the
product had a repellent eect on T. urticae Koch and E. alatus DeLeon; however, it did not aect the
P. macropilis Banks. Additionally, the Neemseto exhibited an important reduction in T. urticae Koch
fecundity, but on the predatory mites, a significant decrease was only observed when mites were
exposed to the highest concentrations. This shows that this product can be a promising option for the
management of the two-spotted spider mites within integrated pest management schemes given its
relative compatibility with predatory mites.
3.3.18. Family Myrtaceae
T. urticae Koch toxicity studies involving these plants have had varying results. First, Choi et al.
(2004) [
42
] determined that the Eucalyptus citriodora Hook’s essential oil is capable of causing a mortality
rate of more than 90% on T. urticae Koch adults. This essential oil was also tested by Han et al.
(2010) [
68
] on the same mite species using the vapor-phase mortality bioassay; they found similar
fumigant activity results to those obtained previously [
42
]. The test performed consisted of placing
3 cm diameter bean leaf discs on wet cotton inside Petri dishes, each with 20 adult mite individuals [
68
].
On each Petri dish, they installed a mesh cover on which a filter paper moistened with the essential oil
at the evaluated concentrations was placed (after drying for two minutes). From these experiments,
they estimated an LD50 of 19.3 µg/cm3.
On the other hand, they also wanted to evaluate the fumigant eect of Syzygium aromaticum
(L.) Merr. & L.M. Perry essential oil. Within the study, they found an LD
50
value of 23.6
µ
g/cm
3
on
T. urticae Koch adults. In 2011, Afify et al. [
108
] tested the activity of six extracts of Syzygium cumini (L.)
Skeels at three dierent concentrations (75, 150, and 300
µ
g/mL) on the T. urticae Koch. The highest
mortality rates were obtained with the ethanolic extract (98.5%), followed by the hexane extract (94%)
and the ether-ethyl acetate extract (90%). The LD
50
values obtained were 85, 101, 102, and 98
µ
g/mL,
respectively. The same group of researchers in 2012 conducted a study to measure the acaricidal
activity of Eucalyptus sp. on the same mite [
89
]. The LD
50
values obtained for adults and eggs in the
assay were 2.18 and 7.33 µg/mL, respectively.
In 2013, Amizadeh et al. [
84
] also tested the fumigant eect of some essential oils of this family,
including those obtained from leaves and fruits of the Eucalyptus microtheca F. Muell. on both eggs
and adult females of the T. urticae Koch. For the tests, mites were placed on bean leaf discs laid in
plastic containers in which an oil-impregnated filter paper was held without coming into direct contact
with leaf discs or mites. The LD
50
s on the adult females were 1.52
µ
L/L and 5.7
µ
L/L for the extracts
of leaves and fruits, respectively, while for eggs, they were 0.56
µ
L/L and 2.36
µ
L/L for leaf and fruit
extracts, respectively.
3.3.19. Piperaceae Family
There have been few studies carried out concerning the eects of extracts of species of the
Piperaceae family on the T. urticae Koch—particularly considering the fact that they have focused
on very few species of the genus Piper, which has more than 1000 species [
109
]. One of those
Plants 2019,8, 272 19 of 51
studies was developed by Ara
ú
jo et al. (2012) [
110
], who reported acaricidal and repellent activity
of the essential oils obtained from Piper aduncum L. leaves and its components separately on the
T. urticae Koch. The repellent activity was attributed to the components (E)-nerolidol,
α
-humulene,
and
β
-caryophyllene, while the toxicity was attributed to
β
-caryophyllene. The extracts and their
components exhibited a better performance in fumigation than in contact.
3.3.20. Family Ranunculaceae
In general terms, the toxicity studies of extracts of these plants used on the T. urticae Koch have not
been very satisfactory. A case demonstrating this is the study conducted by Derbalah et al. (2013) [
91
],
which found that the black cumin seeds (Nigella sativum L.) extract showed a low toxic eect on the
T. urticae Koch, with an LD
50
of 708.57 ppm. However, some species of this family—such as Aconitum
soongaricum Stapf and Clematis orientalis L.—have shown toxic eects on the T. urticae Koch with
mortality rates ranging between 50% and 80% of mites [99].
3.3.21. Family Rutaceae
In 2005, Tewary et al. [
111
] tested two concentrations (5000 and 10,000 ppm) of the Zanthoxylum
armatum DC. leaf extract on the arthropods H. armigera Hübner, P. xylostella L., T. urticae Koch,
and A. craccivora Koch, with mortality rates of 46% at 10,000 ppm in the H. armigera Hübner, 42% at
10,000 ppm in the P. xylostella L., 36% and 39% at 5000 and 10,000 ppm, respectively, in the T. urticae
Koch, and 30% and 65% at 5000 and 10,000 ppm, respectively, in the A. craccivora Koch. On the other
hand, Attia et al. (2012) [
88
] also included plants of the Rutaceae family, since they proved the eect
caused by the essential oil of Haplophyllum tuberculatum (Forssk.) A. Juss. on the T. urticae Koch,
obtaining a mortality of 93%.
Da Camara et al. (2015) [
67
] demonstrated that essential oils obtained from the epicarp of
pear orange fruits (Citrus sinensis Osbeck var. Pera) and the lime orange (Citrus aurantium L.) had
repellent eects against the T. urticae Koch, with very similar repellency results to those obtained with
eugenol. Using mass spectrometry, 27 compounds were idenitified both in C. sinensis Osbeck and in
C. aurantium L., which corresponded to 98.1% and 98.9% of the total constituents of the two extracts,
respectively. This demonstrated that the major compound in the two essential oils was d-limonene.
Within this study, the authors determined that all the identified compounds were responsible for
the repellency.
3.3.22. Family Santalaceae
Within this family, Roh et al. (2011) [
112
] studied the eect of Santalum L. sp. essential oil on
the T. urticae Koch using the leaf immersion method. Through this methodology, they found that the
mortality rate of mites was 87.2%
±
2.9%. Additionally, they noticed an oviposition decrease of 89.3%
on leaves treated with oil. Subsequently, they evaluated a mixture of
α
and
β
–Sandalool—the two
main compounds of Santalum L. sp.—on the T. urticae Koch and obtained a mortality of 85.5%
±
2.9%
and a decrease of 94.7% in fecundity.
3.3.23. Family Scrophulariaceae
The toxic eects of Scrophulariaceae plants on the T. urticae Koch have been less studied
than plant species of other groups. Within the investigations carried out in this regard,
Khambay et al. (1999) [
113
] studied the eect of two compounds of Calceolaria andina Benth extract
with recognized insecticidal activity—2-(1,1-dimethylprop-2-enyl)-3-hydroxy-1,4-naphthoquinone
(compound
1
) and 2-acetoxy-3-(1,1-dimethylprop-2-enyl)-1,4-naphthoquinone (compound
2
)—on 29
pest species, including the T. urticae Koch. The LD
50
s for this species were 80 ppm and 30 ppm for
each compound, respectively. The two cases were evaluated using the micro-immersion method.
Additionally, they performed the same test on individuals from a population that showed resistance
Plants 2019,8, 272 20 of 51
to chlorpyrifos and bifenthrin using the same compounds of C. andina Benth extract, thus obtaining
LD50s of 44 ppm and 33 ppm for compounds 1and 2, respectively.
3.3.24. Family Simarubaceae
The toxicity of plant extracts from species of this family on the tetraniquid mite T. urticae Koch
have not been well studied. Among the studies accomplished, Latif et al. (2000) [
114
] tested the
extract from Quassia sp. aerial parts on this mite at a concentration of 10,000 ppm, finding acaricidal
activity. Subsequently, they identified the quassinoid Chaparinone compound and tested it separately,
obtaining an LC
50
of 47 ppm. Chermenskaya et al. (2010) [
99
] evaluated extracts from 123 dierent
plant species on the T. urticae Koch, Frankliniella occidentalis Pergande and Shizaphis graminum Rondani,
using the leaf immersion method. Within these extracts, one that demonstrated a high acaricidal eect
was obtained from the Ailanthus altissima (Mill.) Swingle leaves, which caused a mortality rate of 97.4%
after 7 days of evaluation.
3.3.25. Family Solanaceae
Although most studies involving plant extracts tested on the T. urticae Koch have focused on
assessing the eects on mortality and fecundity, those involving the Solanaceae family have been mostly
dedicated to determining the repellent eects of certain extracts. Such is the case of the study conducted
by Snyder et al. (1993) [
115
]. They isolated dihydrofarnesoic acid as one of the phytoconstituents
in trichomes of Lycopersicon hirsutum Dunal, and its repellent eect on the phytophagous mite was
then evaluated. For this purpose, 10
µ
L of the extract was applied to a filter paper separated by
1.5 cm from another similar filter, which was impregnated with 10
µ
L of hexane. Once the solvent
was evaporated, a strip of filter paper was positioned to connect the two filter papers, and a mite was
placed in the middle of the paper bridge to evaluate its displacement preference. This process was
performed with approximately 40 adult females. According to the obtained results, they concluded that
dihydrofarnesoic acid exhibited a repellent activity against the T. urticae Koch. Similarly, Antonious et al.
(2006) [
116
] also evaluated toxic and repellent eect of the fruit extracts of Capsicum chinense Jacq.,
Capsicum frutescens L., Capsicum baccatum L., Capsicum annuum L., and Capsicum pubescens Ru
í
z & Pav.
In their results, they determined that the highest mortality rate (45%) occurred when using the extract
of the C. annuum L., while the extracts of the fruits of the C. baccatum L. and C. annuum L. caused
repellence on mites.
Extracts of leaves and seeds of the Datura stramonium L. were used by Kumral et al. (2009) [
5
]
to evaluate their acaricidal, repelling, and deterrent eects on oviposition over T. urticae Koch adults at
167.25 mg/L and 145.75 mg/L (for leaves and seeds, respectively). For these tests, they used a Potter
Tower in order to place the mites on leaf discs contained in Petri dishes. These concentrations caused
98% and 25% of the mortality, respectively, for the two concentrations after 48 h of application. Through
a simple logistic regression analysis, they determined that an increase in the leaf extract dose caused
a significant increase in mite mortality, while the eect of increasing the dose of the seed extract was
not significant. Based on Probit analysis, they estimated that the lethal dose (LD
50
) with the leaf extract
was 70.59 mg/L. According to the Pearson X
2
test, they concluded that mites showed a strong tendency
to flee from areas treated with leaf and seed extracts to untreated areas.
3.3.26. Verbenaceae Family
In this family, a highlighted study was conducted by Cavalcanti et al. (2010) [
117
], in which they
carried out a characterization of the essential oils of the Lippia sidoides Cham. (Verbenaceae) by GC–MS
and tested their acaricidal activity on T. urticae Koch females. They concluded that the compounds
thymol and carvacrol—as well as the essential oil of L. sidoides Cham.—showed a promising miticidal
activity against this mite.
Plants 2019,8, 272 21 of 51
3.4. Additional Studies with Isolated Compounds Obtained after Plant Extract Fractionation
As with essential oils and plant extracts, a considerable number of their isolated constituents have
also been tested on the T. urticae Koch. For example, Lee et al. (1997) [
118
] studied the insecticidal
and the acaricidal eects of several monoterpenes and their possible phytotoxicity in maize plants
that served as hosts of the Diabrotica virgifera virgifera LeConte, T. urticae Koch, and Musca domestica L.
Twenty-nine compounds belonging to dierent chemical classes were tested against the T. urticae Koch
by means of the leaf immersion method.
These tests used: the alcohols carveol, carvomentenol, citronellol, geraniol, 10-hydroxygeranol,
isopulegol, linalool, menthol, perilyl alcohol, aterpineol, and verbenol; the phenols carvacrol,
eugenol, and thymol; the ketones (
)-carvone, (+)-carvone, (+)-fenchone, menthone, pulegone,
tuyone, and verbenone; the aldehydes citral and citronellal; citronelic acid; ether 1,8-cineol; and the
hydrocarbons limonene, α-terpinene, and y-terpinene.
All compounds were tested in water with Triton X-100 as a wetting agent at 10,000 and 1000 ppm,
and the activity was evaluated 24, 48, and 72 h after the treatment. The toxicity varied depending on
the concentrations and the exposure times. All of the monoterpenes tested—except for 1,8-cineole,
10-hydroxygeraniol, aterpineol, verbenol, and verbenone—caused a 100% mortality rate at the
highest concentration after 24 h. However, carvacrol was the most eective compound in the lowest
concentrations, followed by citronellol.
On the other hand, geraniol produced a 100% rate of mortality, while its 10-hydroxy geraniol
analogue exhibited a 0% mortality rate. During the trial, a longer exposure time increased acaricidal
eects. Alternately, the most eective monoterpenoids (carvacrol, carvomenthenol, carvone, citronellol,
eugenol, geraniol, perilyl alcohol, 4-terpineol, thymol) were evaluated separately in more detailed
tests. From these compounds, carvomentenol and 4-terpineol demonstrated greater acaricidal activity
(LC50s=59 and 96 ppm, respectively).
In another study, Mart
í
nez et al. (2005) [
119
] examined the eect of azadirachtin at 64 and
128 ppm on dierent biological parameters of the T. urticae Koch, such as longevity, fecundity, fertility,
and ospring development. The tests were performed on bean leaf discs in Petri dishes using the
Potter Tower. The results found that this compound aected mortality and fecundity but exhibited
no eects on fertility and ospring development. In a later analysis of life table, they determined
that, with the application of azadirachtin at 80 ppm, the adult survival rate was reduced to 50%.
Duso et al. (2008) [
34
] also tested the toxicity of Azadirachtin on the T. urticae Koch. In that case,
the micro-immersion bioassay methodology was implemented using a concentration of 4.5 g of active
ingredient/L on T. urticae Koch females. For those conditions, the mortality rate obtained was 86.49%.
Similarly, Han et al. (2011) [
120
] tested some constituent compounds of the Eucalyptus citriodora
Hook extract and other plants on resistant and susceptible acaricidal T. urticae Koch females. Among
them, those that showed the highest toxicity were menthol (LD
50
of 12.9
µ
g/cm
3
) and citronellium
acetate (LD
50
of 16.8
µ
g/cm
3
), evaluated on females susceptible to acaricides. Other compounds such
as
β
-citronellol, citral, geranyl acetate, and eugenol also demonstrated a high toxic activity, with LD
50
s
between 21.7
µ
g/cm
3
and 24.6
µ
g/cm
3
. When comparing the mortality results obtained for both
susceptible and acaricide-resistant mites, the researchers estimated that they were very similar to each
other and therefore evidenced that the mechanisms of action of the components of the essential oil and
of the synthetic acaricides are dierent and do not present processes that promote cross-resistance.
One year later, Akhtar et al. (2012) [
121
] studied the eect of eight quinones on the T. urticae
Koch—Myzus persicae Sulzer, Myzocallis walshii Monell, and Illinoia liriodendri Monell—using the leaf
immersion method. The compound plumbagine was the one that exhibited the greatest activity on
the mite, with an LC
50
of 0.001%. Marˇci´c and Me
đ
o (2014) [
122
] also performed experiments with
secondary metabolites from plants. In their study, they tested a combination of oximatrin and psoralen
(0.2% and 0.4%, respectively) on the T. urticae Koch and measured acute toxicity and repellency.
The applications were made on bean leaves with a Potter Tower, and the subsequently calculated
LD
50
s were 55.49, 52.68, 6.88, 13.03, and 8.8
µ
L/L for eggs, females that had not oviposited, larvae,
Plants 2019,8, 272 22 of 51
protonymphs, and deutonymphs, respectively. Additionally, they noticed that, in preferential tests
on the leaves, the mites tended to be located in the middle of the untreated leaf, at which point the
oviposition was greater.
The same authors also tested compounds from the Neem extract (azadirachtin-A) on females of
the two-spotted spider mite [
123
]. For this case, they introduced bean leaf discs inside Petri dishes
with moistened cotton and made applications of the product using a Potter Tower in the middle of the
leaf. They concluded that females preferred to be located in the middle of the leaf not treated with the
product and, in the same way, they observed that oviposition was higher in females that were located
in the untreated areas.
4. Conclusions
In conclusion, 458 records of plant species from 67 plant families (listed in this survey) have
repellent or acaricidal eects against the T. urticae Koch under laboratory conditions. The ecacy is
available at dierent levels depending on species, extractions (extract or essential oils), plant parts
used, and concentrations of test extract/essential oil. Among the most studied botanical families
for this purpose are plants from Lamiaceae, Asteraceae, Myrtaceae, and Apiaceae taxons. Extracts
from species including Celosia Trygina L., Cassia mimosoides L., Clome viscosa L., Boscia senagalensis
(Pers.) Lam. Ex. Poir., Cobretum micranthum G. Don, Ipomaea asarifolia (Desr.) Roem. and Schult.,
Cnidoscolus aconitifolius (Mill) I.M. Johnst., Azadirachta indica A. Juss., Syzygium cumini (L.) Skeels,
Papaver rhoeas L., Plantago major L., Ailanthus altissima (Mill.) Swingle, and Capsicum annuum L. exhibited
better acaricidal properties with ecacies between 90% and 100% at a concentration range between
0.2% and 1%—comparable to some commercial acaricides. LD
50
values can be found below 20
µ
g/mL or
5
µ
L/L air. Thus, botanical-based preparations can be a good source of eective acaricidal preparations
either as extracts or as essential oils. Although the information herein presented only concerns a basic
screening of the acaricidal ecacy of botanicals at laboratory (
in vitro
) levels, several plants could
be considered for future research on field evaluations or as sources of acaricide compounds. In this
sense, several compounds such as azadirachtin, 10-hydroxygeraniol, terpineols, verbenol, verbenone,
carvacrol, plumbagine, linalool, and citral, among others, have been isolated as bioactive acaricidal
compounds. In future studies, attention may be focused on acaricidal activity rather than on repellent
properties to facilitate two-spotted mite control. However, formulations and application rates similar
to those used by farmers must be assessed in order to achieve more predictive results in further field
experiments. Sublethal eects must also be relevant in future research, since those eects could produce
other subsequent problems or benefits in the control of mites. Finally, more compatibility studies
and phytotoxicity as well as extract stability, extraction standardization, and field formulations are
required to ensure good results on integrated pest management programs for T. urticae Koch control
using eective botanicals.
Author Contributions:
Conceptualization, R.A.R., D.R., E.C.-B.; methodology, R.A.R.; validation, R.A.R.; formal
analysis, R.A.R., D.R., E.C.-B.; investigation, R.A.R.; resources D.R., E.C.-B.; data curation, R.A.R., D.R., E.C.-B.;
writing—original draft preparation, R.A.R.; writing—review and editing, D.R., E.C.-B.; supervision, D.R., E.C.-B.;
project administration, E.C.-B.; funding acquisition D.R., E.C.-B.
Funding:
This research was funded by the Vicerrectoria de Investigaciones at UMNG, grant number
INV-CIAS-1788-validity 2016.
Acknowledgments:
Authors thank Universidad Militar Nueva Granada (UMNG) for the financial support
through the project INV-CIAS-1788.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
publish the results.
Plants 2019,8, 272 23 of 51
Appendix A
Table A1. Compilation of reported studies using plant extracts and essential oils against T. urticae Koch under laboratory conditions.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Amaranthaceae
Amaranthus viridis L. Whole plant extract 5000 ppm G Adults Mortality between 40 and 60% - [108]
Amaranthaceae
Amaranthus viridis L. Whole plant extract 2500 ppm G Adults Mortality between 40 and 60% - [108]
Amaranthaceae
Blepharis linariifolia Pers. Whole plant extract 5000 ppm G Adults Mortality between 61 and 80% - [108]
Amaranthaceae
Blepharis linariifolia Pers. Whole plant extract 2500 ppm G Adults Mortality between 61 and 80% - [108]
Amaranthaceae
Blepharis sp. Whole plant extract 5000 ppm G Adults More than 80% of mortality - [108]
Amaranthaceae
Blepharis sp. Whole plant extract 2500 ppm G Adults Mortality between 61 and 80% - [108]
Amaranthaceae
Celosia Trygina L. Whole plant extract 5000 ppm G Adults More than 80% of mortality - [108]
Amaranthaceae
Celosia Trygina L. Whole plant extract 2500 ppm G Adults More than 80% of mortality - [108]
Amaranthaceae
Chenopodium ambrosioides
Mosyakin et Clemants
Emulsifiable
Concentrate 0.50% A,C Adults and eggs 94.7% of mortality - [41]
Amaranthaceae
Chenopodium quinoa Willd. Seeds extract 6–9% w/v
[1.24% w/v (LD
50
)]
E,F Adult females
and nymphs
Mortalities ranged
from 30% to 99% - [89]
Amaranthaceae
Kochia scoparia (L.) Schrad. -
98.13%
(chloroform
extraction)
A,E,H Adult females 92.58% of mortality - [52]
Amaryllidaceae
Allium cepa L. Essential oil - D Larvae and
adults.
Mortalities of 65% (larvae) and
67% (adults) - [88]
Amaryllidaceae
Allium cepa L. Peel fruit extract 1% G Adult females Mortality between 0 and 20% - [99]
Amaryllidaceae
Allium galanthum
Kar. & Kir. Whole plant extract 1% G Adult females Mortality between 20 and 50% - [99]
Amaryllidaceae
Allium obliquum L. Whole plant extract 1% G Adult females Mortality between 50 and 80% - [99]
Amaryllidaceae
Allium sativum L. - 7.2 g/L A,G Adult females LD50 - [78]
Amaryllidaceae
Allium sativum L. Bulb extract 7.49 and
13.5 mg/LE,F Adult females LD50 and LD90 (respectively) - [77]
Amaryllidaceae
Allium sativum L. Essential oil - D Larvae and adults Mortalities of 86% (larvae) and
61% (adults) - [88]
Amaryllidaceae
Pancratium maritimum L.
Alkaloidal ethanolic
extract and bulb
essential oil
0.2%. 0.36% and
1.5%
respectively
- LD50 - [76]
Amaryllidaceae
Ungernia severtzovii Regel Root extract 1% G Adult females Mortality between 20 and 50% - [99]
Anacardiaceae
Cotinus coggygria Scop. Essential oil - D Larvae and adults Mortalities of 58% (larvae) and
58% (adults) - [88]
Anacardiaceae
Cotinus coggygria Scop. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Anacardiaceae
Pistacia lentiscus L. Essential oil - D Larvae and adults Mortalities of 22% (larvae) and
23% (adults) - [88]
Annonaceae Annona glabra L. Seed extract 1000 ppm D,G Eggs No eects - [80]
Plants 2019,8, 272 24 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Annonaceae Cananga odorata (Lam.)
Hook.F. & Thomson Essential oil 0.1% G Adult females 24.2% of mortality - [112]
Annonaceae Xilopia sericea A.St.-Hill. Leaves and fruits
essential oils 4.08 µL/L C Adult females LD50
α-pinene (0.41% leaves,
17.18% fruits),
β
-pinene
(45.59% fruits), cubenol
(57.43% leaves),
myrcene (9.13% fruits),
between others
[44]
Apiaceae Ammi visnaga Seed extract 17 µg/cm2D,I Eggs LD50 Kheline and visnagine [65]
Apiaceae Carum carvi L. Essential oil
19
×
10
3µ
L/mL
of air. J Adults 100% of mortality - [42]
Apiaceae Carum carvi L. Essential oil 22.4 µg/cm3C,J Adults LD50 - [68]
Apiaceae Carum carvi L.
Essential oils mixed
with Fatty acid
potassium salts
570 ppm of
essential oil and
2478 ppm of
potassium salts
E Adults 83.4% of mortality - [83]
Apiaceae Conium maculatum L. Flowers and
leaves extract 10–50% A,B Adult females Mortalities of 95.18% and
81.11%, respectively - [60]
Apiaceae Coriandrum sativum L. Essential oil
19
×
10
3µ
L/mL
of air J Adults 92% of mortality - [42]
Apiaceae Cuminum cyminum L. Essential oil
from seeds 3.74 µL/L air C,J Adult females LD50
α-pinene (29.1%),
limonene (22%),
1,8-cineole (17.9%)
[85]
Apiaceae Daucus carota L. Essential oil - D Larvae and adults Mortalities of 5% (larvae) and
3% (adults) - [88]
Apiaceae Deverra scoparia
Coss. & Durieu Essential oil 1.79 and
3.2 mg/LE Young females LD50 and LD90, respectively α-pinene, 3-carene
and terpinen-4-ol [43]
Apiaceae Deverra scoparia
Coss. & Durieu Essential oil - D larvae and adults Mortalities of 98% (larvae) and
97% (adults) - [88]
Apiaceae Ferula gumosa Boiss. Essential oil 6.98 and
6.52 µL/L air C,J Eggs and adults,
respectively LD50
β-pinene (50.1%),
α-pinene (14.9%),
δ-3-carene (6.7%)
[86]
Apiaceae Foeniculum vulgare Mill. Seed essential
oil vapors
5.75 µL/L
(females),
1.17 µL/L (eggs)
J Eggs and adults LD50 - [84]
Apiaceae Foeniculum vulgare Mill. Essential oil 1.17% E Adults LD50 - [83]
Apiaceae Heracleum persicum
Desf. Ex. Fisch.
Fruit essential
oils vapors
3.15
µ
L/L (females)-
1.53 µL/L (eggs) J Eggs and adults LD50 - [84]
Plants 2019,8, 272 25 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Apiaceae Heracleum persicum
Desf. Ex. Fisch. Essential oil 1.53% E Adults LD50 - [83]
Apiaceae Smyrnium olusatrum L.
Inflorescence extract
1.9 and
42.7 µg/mL,
respectively for
isolated
compounds
D Adult females LD50 (chronic toxicity after 5
days)
Isolation of
isofuranodiene and
germacrone, separately
evaluated
[87]
Apocynaceae Vinca erecta
Regel & Schmalh Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Apocynaceae Vinca minor L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Araceae Arum korolkovii Regel Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asclepiadaceae
Calotropis gigantea
W.T. Aiton Leaf extract 5000 ppm G Adults Mortality between 61 and 80% - [71]
Asclepiadaceae
Calotropis gigantea
W.T. Aiton Leaf extract 2500 ppm G Adults Mortality between 40 and 60% - [71]
Asteraceae Achillea mellifolium L. Essential oil from
aerial part
1.208% v/v(leaf
dipping) and
1.801 µL/L air
(fumigation)
G,J Adult females LD50 Piperitone (12.8%),
p-cymene (10.6%) [64]
Asteraceae Achillea millefolium L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Acroptilon repens (L.) DC. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Ajania fastigiata
(C. Winkler) Poljakov Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Anaphalis rosea-alba Krasch. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Anthemis nobilis L. Essential oil
19
×
10
3µ
L/mL
of air J Adults 69% of mortality - [42]
Asteraceae Anthemis vulgaris L. Flower extract 7–50% A,B Adult females Mortalities of 92.37% and
92.34%, respectively - [60]
Asteraceae Anthemis vulgaris L. Leaf extract 13–50% A,B Adult females Mortalities of 82.33% and
76.63%, respectively - [60]
Asteraceae Artemisia absinthium L. Essential oil
19
×
10
3µ
L/mL
of air J Adults 97% of mortality - [42]
Asteraceae Artemisia absinthium L. Essential oil 0.043 mg/cm2A - LD50 - [45]
Asteraceae Artemisia absinthium L. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Artemisia aschurbajewii
C. Winkl. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Artemisia cinae O. Berg &
C.F. Schmidt ex. Pljakov Leaf extract 1326.53 ppm A,B Adult females LD50 - [60]
Plants 2019,8, 272 26 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Asteraceae Artemisia compacta
Fisch. Ex. Besser Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Artemisia dracunculus L. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Artemisia judaica L. Leaves (acetone
extract) 0.56 µg/mL C,G Adult females LD50 - [39]
Asteraceae Artemisia panciflora Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Artemisia vulgaris L. Leaf extract 15-50% A,B Adult females Mortalities of 54.13% and
75.12%, respectively - [60]
Asteraceae Artemisia vulgaris L. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Calendula ocinalis L. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Chamomilla recutita L. Essential oil 0.65–1.17% C Adults ggs LD50
α-basabolol oxide
(35.25%), Trans
β-farersene (7.76%)
[89]
Asteraceae
Chrisanthemum coronarium L.
Essential oil - D Larvae and adults Mortalities of 88% (larvae) and
93% (adults) - [88]
Asteraceae
Handelia trichopylla Heimerl
Aerial part extract 1% G Adult females Mortality between 0 and 20%. - [99]
Asteraceae
Hertia cheirifolia (L.) Kuntze
Essential oil 3.43 mg/L E Adult females LD50 and side-eect over
fecundity [46]
Asteraceae
Hertia cheirifolia (L.) Kuntze
Essential oil - D Larvae and adults Mortalities of 81% (larvae) and
89% (adults) - [88]
Asteraceae Hieracium dschirgalanicum
E. Nikit. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Inula helenium L. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Jurinea capussi Franch. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae
Lamyropappus schakaptaricus
Knorr & Tamamsch. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Matricaria chamomilla L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Matricaria matricarioides
(Less.) Porter Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Matricaria recutita L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Pseudoglossanthis litwinowii
(Tzvel.) R. Kam. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Pyrethrum alatavicum
O. & B. Fedtsch. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae
Pyrethrum
branchanthemoides
R. Kam. & Lazkov
Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Pyrethrum
cinerariifolium Trev. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Plants 2019,8, 272 27 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Asteraceae Pyrethrum sovetkinae
Kovalevsk Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Pyrethrum sussamyrense
Lazkov Root extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Santolina africana
Jord. & Fourr. Essential oil 2.35 mg/L E Adult females LD50 and side-eect over
fecundity Terpinen-4-ol (54.96%) [46]
Asteraceae Santolina africana
Jord. & Fourr. Essential oil - D Larvae and adults Mortalities of 77% (larvae) and
68% (adults) - [88]
Asteraceae Senecio saposhnikovii
Krasch et. Schipcz. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Seriphidium herba-album
(Asso) Sojak Essential oil - D Larvae and adults Mortalities of 54% (larvae) and
37% (adults) - [88]
Asteraceae Tagetes minuta L. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Tanacetopsis ferganensis
Kovalevsk Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Tanacetopsis setacea
Kovalevsk Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Tanacetopsis submarginata
Kovalevsk Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Tanacetum boreale
Fisch. Ex. DC. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Asteraceae Tanacetum pseudoachillea
C. Winkl. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Asteraceae Tanacetum vulgare L. Essential oil 4% A - 75.6% of mortality - [45]
Asteraceae Thitonia diversifolia Hemsl. Methanolic extract 150 µg/cm3D Adult females Mortality less than 50% - [92]
Asteraceae Tripleurospermum inodorum
Sch. Bip. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Asteraceae Xanthium strumarium L. Fruit extract 9-50% A,B Adult females Mortalities of 68.24% and
85.88%, respectively - [60]
Asteraceae Xanthium strumarium L. Leaf extract 11-50% A,B Adult females Mortalities of 52.48% and
79.85%, respectively - [60]
Berveridaceae Berberis iliensis Popov Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Bignonianceae
Jacaranda obtusifolia Bonpl. Leaf extract 0.06% C,G Adult females Mortality of 64.4% [124]
Boraginaceae Echium vulgare L. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Boraginaceae Onosma visianii Clem. Root extract 2.6 µg/mL D Adult females LD50 (chronic toxicity after
5 days)
Shikonin derivatives
(naphthoquinones),
i.e., isobutylshikonin
and isovalerylshikonin
[93]
Plants 2019,8, 272 28 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Brassicaceae Armoracia rusticana G.
Gaertn., B. Mey. & Scherb. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Brassicaceae
Barbarea vulgaris W.T. Aiton
Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Brassicaceae Capsella bursa-pastoris L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Brassicaceae Cardaria repens Schrenk Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Brassicaceae Lepidium latifolium L. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Burseraceae Boswellia carterii Birdw. Essential oil 0.1% G Adult females 24.8% of mortality - [112]
Burseraceae Commiphora myrrha
(Nees) Engl. Essential oil 0.1% G Adult females 22.8% of mortality - [112]
Burseraceae Protium bahianum Daly Fresh and old resin
essential oils - J Adult females Mortalities of 79.6% (fresh
resin) and 59% (old resin) - [97]
Caesalpiniaceae
Cassia mimosoides L. Leaf extract 5000 ppm G Adults More than 80% of mortality - [71]
Caesalpiniaceae
Cassia mimosoides L. Leaf extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Caesalpiniaceae
Cassia occidentalis L. Whole plant extract 5000 ppm G Adults Mortality between 61 and 80% - [71]
Caesalpiniaceae
Cassia occidentalis L. Whole plant extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Caesalpiniaceae
Cassia tora L. Whole plant extract 5000 ppm G Adults More than 80% of mortality - [71]
Caesalpiniaceae
Cassia tora L. Whole plant extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Campanulaceae
Codonopsis clematidea
Schrenk Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Cannabaceae Cannabis sativa L. Essential oil from
panicles 0.10% G Adult females 83.28% of mortality
β-myrcene (18.5%),
trans-caryophyllene
(35.6%)
[98]
Cannabaceae Cannabis sativa L. Aerial part and root
extracts 1% G Adult females Mortality between 50 and 80% - [99]
Cannabaceae Humulus lupulus L. Flower extract 5-50% A,B Adult females Mortalities of 56.37% and
67.84%, respectively - [60]
Cappandaceae
Clome viscosa L. Whole plant extract 5000 ppm G Adults More than 80% of mortality - [71]
Cappandaceae
Clome viscosa L. Whole plant extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Capparidaceae
Boscia senagalensis (Pers.)
Lam. Ex. Poir. Leaf extract 5000 ppm G Adults More than 80% of mortality - [71]
Capparidaceae
Boscia senagalensis (Pers.)
Lam. Ex. Poir. Leaf extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Caprifoliaceae Sambucus nigra L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Caryophyllaceae
Saponaria ocinalis L. Root extract
0.31% (eggs),
1.18% (adulst),
0.91%
(oviposition) w/v
IEggs, adults and
oviposition LD50 - [66]
Plants 2019,8, 272 29 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Caryophyllaceae
Silene sussamyrica Lazkov Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Chenopodiaceae
Anabasis aphylla L. Seed and bark
extracts 1% G Adult females Mortality between 50 and 80% - [99]
Chenopodiaceae
Anthochlamis tianschanica
Iljin Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Chenopodiaceae
Chenopodium álbum (L.)
Mosc. Ex. Moq.
Flower and leaf
extracts 8–50%. A,B Adult females Mortalities of 96.99% and
91.15%, respectively - [60]
Combretaceae Cobretum micranthum
G. Don Whole plant extract 5000 ppm G Adults More than 80% of mortality - [71]
Combretaceae Cobretum micranthum
G. Don Whole plant extract 2500 ppm G Adults More than 80% of mortality - [71]
Combretaceae Combretum glutinosum
Perr. Ex. DC. Leaf extract 5000 ppm G Adults More than 80% of mortality - [71]
Combretaceae Combretum glutinosum
Perr. Ex. DC. Leaf extract 2500 ppm G Adults More than 80% of mortality - [71]
Combretaceae Combretum glutinosum
Perr. Ex. DC. Stem extract 5000 ppm G Adults Mortality between 61 and 80% - [71]
Combretaceae Combretum glutinosum
Perr. Ex. DC. Stem extract 2500 ppm G Adults Mortality between 40 and 60% - [71]
Combretaceae Guiera senegalensis
J.F. Gmel. Leaf extract 5000 ppm G Adults More than 80% of mortality - [71]
Combretaceae Guiera senegalensis
J.F. Gmel. Leaf extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Combretaceae Guiera senegalensis
J.F. Gmel. Stem extract 5000 ppm G Adults Mortality between 61 and 80% - [71]
Combretaceae Guiera senegalensis
J.F. Gmel. Stem extract 2500 ppm G Adults Mortality between 40 and 60% - [71]
Combretaceae Piloitigma vetilicolin Whole plant extract 5000 ppm G Adults More than 80% of mortality - [71]
Combretaceae Piloitigma vetilicolin Whole plant extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Convolvulaceae
Convolvulus arvensis L. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Convolvulaceae
Convolvulus krauseanus
Regel. & Schmalh Root extract 1% G Adult females
Mortality between 80 and 100%
- [99]
Convolvulaceae
Ipomaea asarifolia (Desr.)
Roem. & Schult. Whole plant extract 5000 ppm G Adults More than 80% of mortality - [71]
Convolvulaceae
Ipomaea asarifolia (Desr.)
Roem. & Schult. Whole plant extract 2500 ppm G Adults Mortality between 40 and 60% - [71]
Convolvulaceae
Ipomaea sp. L. Whole plant extract 5000 ppm G Adults More than 80% of mortality - [71]
Convolvulaceae
Ipomaea sp. L. Whole plant extract 2500 ppm G Adults Mortality between 61 and 80% - [71]
Plants 2019,8, 272 30 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Cupressaceae Cupressus macrocarpa
Hartw. ex Gordon Leaf extract 5.69 µL/L air A Adult females LD50 β-citronellol (35.92%) [55]
Cupressaceae Cupressus sempervirens L. Essential oil 0.1%. G Adult females 28.9% of mortality - [112]
Cupressaceae Juniperus communis L. Essential oil 0.1%. G Adult females 42.6% of mortality - [112]
Cupressaceae Juniperus phoenicea L. Essential oil - D Larvae and adults Mortalities of 60% (larvae) and
56% (adults) - [88]
Cupressaceae Thuja orientalis L. Leaf extract 7.51 µL/L air A Adult females LD50 α-pinene (35.49%) [55]
Elaeagnaceae Elaeagnus angustifolia L. Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Equisetaceae Equisetum arvense L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Euforbiaceae Jatropha curcas L. Leaf extract 0.06% C,G Adult females Mortality of 63.3% - [124]
Euphorbiaceae
Chrozophora oblongifolia
(Delile) Spreng. Whole plant extract 312.72 and
206.91 ppm GAdult females
and larvae LD50
7-O-β-D-[2”,6”-bis(4-
hydroxy-E-cinnamoyl)]
glucopyranoside,
apigenin
7-O-ß-D-glucopyranoside
isolated from butanol
fration
[125]
Euphorbiaceae
Cnidoscolus aconitifolius
(Mill) I.M. Johnst. Leaf extract 2000 µg/mL C,G Adult females 92% of mortality - [61]
Euphorbiaceae
Euphorbia ferganensis
B. Fedtsch. Root extract 1% G Adult females Mortality between 0 and 20% - [99]
Euphorbiaceae
Euphorbia kansui
S.L. Liou S.B. Ho Root extract 3-5 g/L C Adult females Mortalities of 27% and 55%,
respectively
3-O-(2,3-
dimethylbutanoyl)-13-
dodecanoylingenol y
3-O-(20E,40Z-
decadienoyl)-ingenol
[100]
Fabaceae Acacia cyanophylla Lindl. Essential oil - D Larvae and adults Mortalities of 58% (larvae) and
26% (adults) - [88]
Fabaceae Amnopiptanthus nanus
(M. pop) Cheng Pod extract 1% G Adult females Mortality between 50 and 80% - [99]
Fabaceae Bowdichia virgilioides Kunth Leaf extract 0.06% w/v C,G Adult females Mortality of 64.4% [126]
Fabaceae Gleditschia spp. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Fabaceae Glycirrhisa uralensis L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Fabaceae Hedysarum cephalotes
Franchet Whole plant extract 1% G Adult females Mortality between 20 and 50% - [99]
Fabaceae
Hedysarum
daraut-kurganicum
Sultanova
Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Fabaceae Hymenaea courbaril L. Leaf extract 0.06% w/v C,G Adult females Mortality of 59.4% [126]
Plants 2019,8, 272 31 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Fabaceae Medicago minima L. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Fabaceae Melilotus ocinalis L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Fabaceae Millettia pinnata L. Laef oil 0.004% C Adult females LD50 (after 4 days) - [101]
Fabaceae Oxytropis rosea Bunge Aerial part extract 1% G Adult females Mortality between 20 and 50% - [99]
Fabaceae Sophora korolkovii Koehne. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Fabaceae
Sophora secundiflora (Ortega)
Lag. Ex. DC. Essential oil - D Larvae and adults Mortalities of 68% (larvae) and
61% (adults) - [88]
Fabaceae Vicia cracca L. Aerial part extract 1% G Adult females Mortality between 0 and 20% - [99]
Geraniaceae Pelargonium graveolens
L’Her Leaf extract 12.27 µL/L air A Adult females LD50 terpinen-4-ol (20.29%) [55]
Geraniaceae Pelargonium graveolens
L’Hér. Essential oil
19
×
10
3µ
L/mL
of air. K Adults 100% of mortality - [42]
Geraniaceae Pelargonium graveolens
L’Hér. Essential oil - D Larvae and adults Mortalities of 78% (larvae) and
70% (adults) - [88]
Geraniaceae Pelargonium roseum Willd Essential oil 0.1%. G Adult females 30% of mortality - [112]
Gramineae Chrysopogon zizanioides (L.) Essential oil 18.82 µg/mL J Adult females LD50 - [127]
Gramineae Cymbopogon citratus
(DC.) Stapf Essential oil
19
×
10
3µ
L/mL
of air. J Adults 100% of mortality - [42]
Gramineae Cymbopogon citratus
(DC.) Stapf Essential oil 0.1%. G Adult females 17.8% of mortality - [112]
Gramineae Cymbopogon flexuosus (Nees
ex Steud.) W. Watson Essential oil 17.23 µg/mL J Adult females LD50 - [127]
Gramineae
Cymbopogon Martini (Roxb.)
W. Watson Essential oil
19
×
10
3µ
L/mL
of air J Adults 67% of mortality - [42]
Gramineae Cymbopogon nardus
(L) Rendle Essential oil
19
×
10
3µ
L/mL
of air J Adults 99% of mortality - [42]
Gramineae Cymbopogon nardus
(L) Rendle Essential oil 22.5 µg/cm3C,J Adults LD50 - [68]
Gramineae Cymbopogon winterianus
Jowitt ex. Bor Essential oil 0.1% G Adult females 27.6% of mortality - [112]
Gramineae Lolium perenne L. Leaf and flower
methanolic extracts 6-50% A,B Adult females Mortalities of 91.43% and
93.5%, respectively - [60]
Guttiferae Hypericum perforatum L. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Iridaceae Iris sogdiana Regel. Leaf extract 1% G Adult females Mortality between 0 and 20% - [99]
Juglandecaea Juglans regia L. Leaf extract 12% v/w C,G
Adult females and
nymphs Mortality between 83 and 90% - [128]
Lamiaceae Acinos thymoides (L.)
Moench Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Plants 2019,8, 272 32 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Lamiaceae Ajuga australis R.Br. Leaf extract 1% C - Mortality between 20 and 49% - [103]
Lamiaceae Callicarpa pedunculata R.Br. Leaf extract 1% C - Mortality between 20 and 49% - [103]
Lamiaceae Ceratanthus longicornis
(F.Muell.) G. Taylor Leaf extract 1% C - 100% of mortality - [103]
Lamiaceae Clerodendrum floribundum
R.Br. Leaf extract 1% C - Mortality between 50 and 89% - [103]
Lamiaceae Clerodendrum inerme
(L.) Gaertn. Leaf extract 1% C - Mortality between 50 and 89% - [103]
Lamiaceae Clerodendrum tomentosum
(Vent.) R.Br. Leaf extract 1% C - Mortality between 50 and 89% - [103]
Lamiaceae Clerodendrum traceyi
F. Muell. Leaf extract 1% C - 100% of mortality - [103]
Lamiaceae Faradaya albertissii F. Muell. Leaf extract 1% C - Less than 20% of mortality - [103]
Lamiaceae Faradaya splendida F. Muell. Leaf extract 1% C - Mortality between 50 and 89% - [103]
Lamiaceae
Glossocarya calcicola Domin.
Leaf extract 1% C - Less than 20% of mortality - [103]
Lamiaceae Glossocarya
hemiderma Benth. Leaf extract 1% C - Mortality between 20 and 49% - [103]
Lamiaceae Gmelina leichardtii
(F.Muell.) Benth Leaf extract 1% C - Mortality between 90 and 99% - [103]
Lamiaceae Hemiandra australis
B.J. Conn. Leaf extract 1% C - Mortality between 20 and 49% - [103]
Lamiaceae Hemiandra leiantha Benth. Leaf extract 1% C - Less than 20% of mortality - [103]
Lamiaceae Hemiandra pungens R.Br. Leaf extract 1% C - Mortality between 20 and 49% - [103]
Lamiaceae Hemigenia humilis Benth. Leaf extract 1% C - Mortality between 20 and 49% - [103]
Lamiaceae Hemigenia sericea Benth. Leaf extract 1% C - Less than 20% of mortality - [103]
Lamiaceae Hemigenia
westringioides Benth. Leaf extract 1% C - Less than 20% of mortality - [103]
Lamiaceae Hyssopus ocinalis L. Aerial part extract 1% G Adult females Less than 20% of mortality - [99]
Lamiaceae Hyssopus ocinalis L. Essential oil 0.1%. G Adult females 28.1% of mortality - [112]
Lamiaceae Lachnostachys eriobotrya
(F. Muell.) Druce Leaf extract 1% C - Less than 20% of mortality - [103]
Lamiaceae Lavandula angustifolia Mill. Leaf extract 4.93 µL/L J Adult females LD50 1,8-cineole, camphor,
β-pinene [129]
Lamiaceae Lavandula latifolia Medik.
Essential oil from
twigs with leaves
andflowers
0.20–0.25% v/vA,C Adult females
Mortality between 95 and 100%
linalool (37.8%),
1,8-cineole (24.9%),
camphor (18.7%)
[56]
Lamiaceae Lavandula ocinalis Chaix Essential oil
19
×
10
3µ
L/mL
of air J Adults 97% of mortality - [42]
Plants 2019,8, 272 33 of 51
Table A1. Cont.
Family Plant Species Source Concentration BioassayaT. urticae
Koch Stage Eect on T. urticae Koch Identified Compounds Ref.
Lamiaceae Lavandula ocinalis Chaix Essential oil - D Larvae and adults Mortalities of 38% (larvae) and
41% (adults) - [88]
Lamiaceae Lavandula vera DC. Essential oil 0.1% G Adult females 26.1% of mortality - [112]
Lamiaceae Leonorus turkestanicus V.
Krecz. & Kupr. Aerial part extract 1% G Adult females Mortality between 50 and 80% - [99]
Lamiaceae Lycopus australis R. Br