J Pest Sci (2013) 86:361–386
DOI 10.1007/s10340-013-0503-0
REVIEW
A review of the major biological approaches to control
the worldwide pest Tetranychus urticae (Acari: Tetranychidae)
with special reference to natural pesticides
Biological approaches to control Tetranychus urticae
Sabrine Attia • Kaouthar Lebdi Grissa •
Georges Lognay • Ellyn Bitume • Thierry Hance •
Anne Catherine Mailleux
Received: 25 January 2013 / Accepted: 22 April 2013 / Published online: 5 May 2013
Ó European Union 2013
Abstract The two-spotted spider mite, Tetranychus ur-
ticae Koch, is a phytophagous pest that can cause signifi-
cant yield losses in many agricultural crops, including
fruits, cotton, vegetables, and ornamentals. To date, 3877
host species have been reported around the world in both
outdoor crops and greenhouses. In this paper, we present
the common methods to control this pest including chem-
ical and biological practices. While synthetic acaricides
have been widely used to manage T. urticae, in recent
years, interest in pesticides derived from plants has
increased considerably as a result of environmental con-
cerns and pest population resistance to conventional pes-
ticides. Some botanical pesticides can be easily produced,
are relatively efficient against pests, and with few excep-
tions, their mammalian toxicity and persistence in the
environment is low. Thus, the use of plant extracts appears
to be a promising alternative strategy for pest management.
The present paper reviews studies on the biocidal activities
of plant extracts, including essential oils, against T. urticae,
Communicated by M. Traugott.
S. Attia (&)  E. Bitume  T. Hance  A. C. Mailleux
Earth and Life Institute, Biodiversity Research Centre,
Université Catholique de Louvain, 4-5, Place Croix du sud,
1348 Louvain, Belgium
e-mail: sabine_bio5@yahoo.fr
K. L. Grissa
Laboratoire d’Entomologie-acarologie, Institut National
Agronomique de Tunisie, 1082 Cité Mahrajène, Tunis, Tunisia
G. Lognay
Gembloux Agro-Bio Tech, Unité de Chimie Analytique,
Université de Liège, Passage des Déportés, 2, 5030 Gembloux,
Belgium
a plant-feeding mite found worldwide and a serious agri-
cultural and home garden pest.
Keywords Tetranychus urticae  Pest management 
Essential oil  Plant extract
Introduction
The two-spotted spider mite Tetranychus urticae Koch
(Acari: Tetranychidae) is a ubiquitous species, present
worldwide on a wide variety of plants (Helle and Sabelis
1985). It is a phytophagous pest that can cause significant
yield losses in many agricultural crops, including fruits,
cotton, vegetables, and ornamentals (Stumpf et al. 2001; Van
Leeuwen et al. 2007). To date, 3,877 host species have been
reported around the world in both outdoor crops and green-
houses (Migeon and Dorkeld 2007). From the larval stage
through to adulthood, mites preferentially feed on the lower
surface of the leaf (Jhonson and Lyon 1991). The host plant
can be affected in different ways, including a decrease in
photosynthesis or an injection of phytotoxic substances
when feeding (Jhonson and Lyon 1991). Moreover, the
accumulation of faeces, webbing, and/or defoliation can
affect the plant’s appearance as well as its commercial value
(Jhonson and Lyon 1991). The combination of these factors
can decrease the economic interests of producers and cus-
tomers and can lead to severe economic loss. Yield losses can
approach 15 % for strawberries in the USA, 14 % for corn in
France, and 14–44 % for cotton plants (Powell and Lindquist
1997). Common methods to control this pest include cul-
tural, chemical, and biological practices (Powell and Lind-
quist 1997; Bethke et al. 2001).
Synthetic acaricides have been widely used to manage T.
urticae (Sundaram and Sloane 1995; Van Leeuwen et al. 2006).
123
362
Currently, the cost of their use to counter spider mite
damage exceeds USD $1 billion per year in the European
Union (Press release 2011). Due to the excessive use of
pesticides and the associated problems of resistance and
environmental pollution, there is an increasing demand for
sustainable, environmentally friendly control methods. In
addition, control methods based on the use of synthetic
acaricides sometimes fail to keep the number of spider
mites below economic threshold levels (Tirello et al. 2012).
It is therefore crucial to find new, selective pesticides
compatible with the use of natural enemies that can mini-
mise negative effects on the environment, including both
fauna and flora (Steiner et al. 2011).
Biological control of spider mites has been achieved in
glasshouses as an alternative method to chemical control
(Osborne et al. 1985; Kropczynska et al. 1999). Among
the current alternative strategies aimed at decreasing pest
populations, pesticides based on plant extracts are cur-
rently one of the most promising methods. Derived from
plant extracts, allelochemicals, i.e. compounds important
in plant–insect interactions, are being more frequently
considered for use as an alternative or complementary
approach to synthetic insecticide treatments (Heuskin
2011). These allelochemicals are chemical mediators used
in interspecies communication between plants and herbi-
vores (Regnault-Roger 1997). Indeed, some plants have
evolved broad spectrum chemical and physical defences
against diverse groups of insects (Ryan and Byrne 1988).
In this context, the use of some plant extracts can present a
realistic alternative to synthetic acaricides because of their
efficiency against pests. For example, when used as pes-
ticides, plant extracts can affect pest behaviour, including
repelling the pest or prohibiting feeding activity, and pest
physiology, including molting and respiratory inhibition,
growth and fecundity reduction, and also cuticle disruption
(Saxena 1989; Isman 2000; Enan 2001; Gokce et al.
2011). Moreover, exposure to varying mixtures of bio-
synthetically different compounds found in plant extracts
can delay the evolution of resistance (Isman 2000). Plants
extracts are also an environmentally interesting tool
because of their biodegradability and minimal side-effects
on non-target organisms as well as on the environment
(Hay and Watermen 1993; Isman 2000, 2001, 2004;
Chiasson et al. 2001; Basta and Spooner-Hart 2002; Fla-
mini 2003, 2006; Rasikari et al. 2005; Tewary et al. 2005;
Pontes et al. 2007, 2010; Cavalcanti et al. 2010; Attia
et al. 2011b, 2012a, b). However, it is important to note
that the plant extracts that are most efficient against pests
are often the most phytotoxic (Isman 2000). The combi-
nation of the risks associated with conventional pesticides
and the efficiency of natural pest extracts provide the basis
for the recent interest in bioactive acaricidal compounds
from plants.
123
J Pest Sci (2013) 86:361–386
Among these plant extracts, the use of essential oils and
of distillates are currently proposed as two alternative
means of controlling agricultural pests, notably because
they contain a rich array of bioactive chemicals. To date,
several reports have dealt with the use of essential oils and
other extracts from plants to control phytophagous and
parasitic mites (Choi et al. 2004; Floris et al. 2004;
Çalmasur et al. 2006; Pontes et al. 2007; Cavalcanti et al.
2010; Han et al. 2010; Neves et al. 2011). Plant compounds
that can be used as pesticides are produced in 17,500
species of higher plants, the majority of which are aro-
matic, belonging mostly to a few families, including the
Myrtaceae, Lauraceae, Lamiaceae, and Asteraceae (Re-
gnault-Roger et al. 2012). Many plants have been tested for
the control of spider mites and many of them seem to have
some acaricidal properties.
This paper reviews presents the damage caused by the
pest and common methods to control this pest including
chemical, cultural, and biological practices.
Damage caused by T. urticae
Tetranychus urticae feeding causes greying or yellowing of
the leaves and necrotic spots occur in advanced stages of leaf
damage. Mite damage to the open flower causes a browning
and withering of the petals that resembles spray burn. In
addition, small chlorotic spots can be formed at feeding sites
as the mesophyll tissue collapses due to the destruction of
18–22 cells per minute. Continued feeding causes a spotted-
bleached effect and the leaves then turn yellow, grey, or
bronze. In the case of a severe infestation of trees, damage
can be identified by defoliation during the summer or autumn
(Jeppson et al. 1975; Helle and Sabelis 1985).
Control of T. urticae
Chemical control
The synthetic acaricides used in the control of T. urticae
are characterised by a large variety of chemical structures
and modes of action found among the many types of
compounds that are toxic to phytophagous mites. The
modes of action of acaricides and the identification of their
target sites were reviewed by Knowles (1997) and De-
keyser (2005). Here, we present an overview of acaricides
listed according to their group, their database of chemical
molecules (subchem), their primary site of action, and the
emergence of resistance based on Van Leeuwen et al.
(2009) and the Insecticide Resistance Action Committee
(IRAC 2008) (Table 1). Although the number of com-
pounds available for the control of mites looks impressive,
J Pest Sci (2013) 86:361–386 363

Table 1 A list of chemicals acaricides used in the field, including their group, their mode of action, their subchem (database of chemical
molecules) and their resistance against spider mites (IRAC 2008; Van Leeuwen et al. 2009)
Type of insecticides Mode of action Acaricides (Pubchem) (R = resistance evidence in T. urticae)

Carbamates Acetylcholinesterase inhibitors Aldicarb (9570071) R. Bendiocarb (2314). Carbaryl (63252). Carbofuran (2566).
Fenobucarb (19588). Formetanate (31099) R. Methiocarb (16248) R. Oxamyl
(5366286). Propoxur(4944) R
Organophosphates Azinphos-ethyl (17531) R. Azinphos-methyl (2268) R. Chlorfenvinfos (5377784).
Chlorpyrifos (2730) R. Chlorpyro-methyl (2730). Coumaphos (2871) R. Demeton-S-
methyl (13526) R. Diazinon (3017) R. Dichlorvos (3039) R. Dimethoate (3082) R.
Disulfoton (3118) R. Ethion (3286). Fention (3346). Heptenophos (62773).
Malathion (4004) R. Mecarbam (17434). Methamidophos (4096). Mevinphos
(5355863). Monocrotophos (5371562) R. Omethoate (14210). Parathion (13844817).
R. Parathion-ethyl (991) R. Phorate (4790). Phosalone (4793) R. Phosmet (12901).
Phoxim (9570290). Pirimiphos-ethyl (31957). Prophenophos (?) R. Quinalphos
(26124). Sulfotep (19395) R. Tetrachlorvinphos (5284462). Triazophos (32184) R.
Trichlorfon (5853). Vamodothion (560193) R
Cyclodiene GABA-gated chloride channel Endosulfan (21117730) R. Dicofol (8268) R
organochlorines antagonists
Pyrethroids Synaptic agonists Acrinathrin (6436606) R. Bifenthrin (10938769) R. Cyhalothrin (5281873) R.
Cypermethrin (2912) R. fenpropathrin (47326) R. fenvalerate (3347) R. flucythrinate
(50980) R. Flumethrin (91702) R. tau-fluvalinate (91768) R. Halfenprox (10140464).
R. Lubrocytrhinate (16722122). Permethrin (40326) R
Organotin miticides Azocyclotin (91634) R. Cyhexatin (6327054) R. Fenbutatin oxide (16683004) R
Benzoylureas Chitin synthesis inhibitors Flucyloxuron (6537963). Flufenoxuron (91766)
METI-acaricides Mitochondrial complex I Fenazaquin (86356) R. Fenpyroximate (9576412) R. Pyrimidifen (6451139) R.
electron transport inhibitors Pyridaben (91754) R. Tebufenpyrad (86354) R
Spirocyclic Inhibitors of acetyl coenzyme A Spirodiclofen (177863) R. Spiromesifen (9907412)
compounds carboxylase
Organochlorine Unknown or uncertain mode of Dicofol (8268) R. Tetradifon (8305) R
action
Hydrazine carbazate Unknown or uncertain mode of Bifenazate (176879) R
action
Macrocyclic Chloride channel activators Abamectin (6435890) R. Milbemectin (87692394) R
lactones
N-substituted Uncoupler of oxidative Chlorfenapyr (91778) R
halogenated phosphorylation
pyrrole
Other chemicals Inhibitors of mitochondrial ATP Diafenthiuron (3034380)
synthase
Octopamine antagonist Amitraz (36324) R
Mitochondrial electron transport Acequinocyl (93315) R. Fluacrypyrim (9954185) R
inhibitors
Mite growth inhibitors Clofentezine (73670) R. Hexythiazox (13218777) R. Etoxazole (153974) R

in practice the number of acaricides that are registered for
use in particular crops can be rather limited (Van Leeuwen
et al. 2009). For example, in Belgium, only 12 compounds
are registered specifically for spider mite control (Fytoweb
2008).
Advantages of synthetic acaricides
Since World War Two, insecticides and acaricides have
played a central role in the protection of field and greenhouse
crops. However, most of the acaricides (organochlorine) of
the first and second generation are not currently used and/or
are prohibited (Marcic 2012). A pesticide may have both
direct and indirect effects on T. urticae. Some may kill
immediately, while other pesticides take longer to induce
mortality. Others may affect general fitness, by inhibiting
movement, reducing searching abilityk or lowering ovipo-
sition rates. Overall, acaricides may be repellent or harmful
(Steiner et al. 2011). Synthetic pesticides generally result in a
decrease in the number of pests when compared to natural
extracts from plants (Isman 2000; Katsvanga and Chigwaza,
2004). Their utilisation can be easy and fast (Bajwa and
Schaefers 1998), and many are not cost prohibitive (Berger
1994). Moreover, they show greatly increased stability while

123
364
retaining the favourable properties of high insect and low
mammalian toxicity (Ruscoe 1977). Currently, acaricides
are introduced provided that they are safer or ‘‘greener’’
pesticides and that they respond to some eco-toxicological
criteria imposed by the environmental protection agency
(Marcic 2012).
Disadvantages of synthetic acaricides
Resistance The control of T. urticae populations depends
largely on the application of a few conventional acaricides,
such as organotin compounds, mitochondrial electron
transport inhibitor-acaricides (fenazaquin, fenpyroximate,
pyridaben, chlorpyrifos, and tebufenpyrad), and pyre-
throids. However, this mite is able to develop resistance to
these synthetic compounds because of its short life cycle,
abundant progeny, and arrhenotokous reproductive ability
(Ay and Yorulmaz 2010). The repeated use can lead to the
development of resistance and can disrupt the natural
biological control systems of the spider mite (Van Leeu-
wen et al. 2007, 2010; Ay and Yorulmaz 2010: Kumral
et al. 2010). Because of its resistance to a large number of
pesticides, the two-spotted spider mite is considered the
‘‘most resistant species’’ in many areas worldwide (Whalon
et al. 2008).
Expensive compounds Commercial growers use synthetic
pesticides (Jeppson et al. 1975; Rodriguez 1979; Rizzieri
et al. 1998), while small-scale growers with limited access
to financial resources find their cost to be prohibitive. In
1994, a survey in Zimbabwe showed that the number of
peasant farmers who used natural pesticides increased from
20 % before 1989 to 80 % (Katsvanga and Chigwaza
2004), and in Botswana, the cost of 1 l of a common
pesticide is approximately USD $80 (Berger 1994). In
addition, the commercialisation licences are costly.
Effect on non-target organisms and environment These
chemicals also have undesirable effects on non-target
organisms and can be hazardous to the environment (Choi
et al. 2004; Van Leeuwen et al. 2007, 2010). They usually
have a high knock-down effect on pests, however, concern
regarding the long-term consequences of using synthetic
pesticides has arisen for several ecological reasons. These
reasons include the destruction of predators and parasitoids
that control pests (Helle and Sabelis 1985), mortality of
pollinators, and pesticide residues (Georghiou 1986; Clegg
and Mackean 1994). Pesticides may have direct or indirect
environmental effects. The direct effects include persis-
tence and environmental impact, due to their bio-accumu-
lation and persistence in soils. When applied to agricultural
lands by aerial spraying, these compounds can pollute
aquatic systems through soil erosion and water run-off. In
123
J Pest Sci (2013) 86:361–386
addition, ingestion of contaminated seeds or food could be
harmful for animal life. Equally concerning are the indirect
effects, such as changes in the physiology and biology of
living organisms, modification of fecundity and behaviour
(Mansour et al. 1986; Kunz and Kemp 1994), and the
considerable effects of pesticides on the natural enemies of
spider mites (Van de Vrie et al. 1972). In fact, the absence
of control by natural enemies due to their death by pesti-
cides can cause a considerable increase in T. urticae pop-
ulations (Helle and Sabelis 1985). This is evidenced by
several studies demonstrating increases in spider mite
populations associated with the application of pesticides
(Van de Vrie et al. 1972; Jeppson et al. 1975; Helle and
Sabelis 1985).
Phytotoxicity Some acaricides, such as morestan and bi-
napacryl, which are effective against resistant strains, are
phytotoxic when applied under greenhouses conditions
(Jeppson et al. 1975).
Cultural control techniques
It has long been known that high humidity levels reduce the
reproductive potential of tetranychids whose optimal
environment is provided by hot and dry air (Sabelis 1986;
Nihoul 1993; Duso et al. 2004). A report in 1969 demon-
strated that host plant nutrition may have a positive effect
on the reduction of the mite population by varying the
fertiliser regime applied to the crops (Markkula and Ti-
ittanen 1969). Furthermore, large quantities of nitrogen or a
deficiency of potassium can increase the amount of soluble
nitrogen available in the plant so that sharp increases in the
populations of T. urticae follow such fertiliser regimes
(Sabelis 1986). However, the plant response to such
extreme feeding regimes is not economically viable, so
variations in host nutrition have not been used for pest
control (Helle and Sabelis 1985).
Biological control
Phytoseiulus persimilis (Athias-Henriot)
Biological control of spider mites using predators is com-
monly practiced, most often using Phytoseiidae (Ferrero
et al. 2011). Phytoseiulus persimilis (Acari: Phytoseiidae)
is a specialist predator that feeds exclusively on Tetrany-
chus species and whose survival depends on the presence
and quality of its prey. This mite is very voracious, with
adults able to eat 34 eggs or 4.8 females and 10 juveniles of
T. urticae per day (McMurtry and Croft 1997).
Phytoseiulus persimilis can colonise 10 plants in 24 h,
with only the ground and the connections between
the plants influencing the movements of this predator
J Pest Sci (2013) 86:361–386
(Helle and Sabelis 1985). However, there are some failures
in the biological control of T. urticae by this predatory
mite. P. persimilis is sensitive not only to the quality and
quantity of prey but also to environmental conditions, such
as temperature and relative humidity. A relative humidity
of 90 % is necessary for all eggs to hatch, with the per-
centage of hatching approaching 0 at 50 % relative
humidity. Temperatures between 30 and 35 °C result in
optimal development in Tunisia (Sabelis 1986). In tomato
crops, P. persimilis is hampered by molecules released by
the glandular trichomes, such as triacylglycerols and some
sesquiterpenes, and its effectiveness in this culture is not
satisfactory (Kennedy 2003). Finally, the successful control
of T. urticae with P. persimilis depends largely on main-
taining the correct balance between predators and prey
(Helle and Sabelis 1985).
Neoseiulus californicus (McGregor)
The use of other predators has also been investigated,
including N. californicus (Acari: Phytoseiidae). This
polyphagous predator feeds on the two-spotted spider mite
along with other mite species (Castiglioni et al. 2002). It
can survive for a few days without eating any prey by
feeding solely on a diet of pollen. In addition, its life cycle
is not hampered by low relative humidity, but it is less
voracious than P. persimilis and suffers from a low birth
rate. However, augmentative or inoculative use is strongly
considered, and this mite is currently marketed by several
firms (Rondon et al. 2005).
Feltiella acarisuga (Vallot)
Another commercially marketed and interesting predator is
F. acarisuga (Diptera: Cecidomyiidae), which is widely
used in greenhouses. Cecidomyid females lay their eggs
within spider mite colonies, and the predaceous larvae eat
eggs, nymphs, and adults. F. acarisuga can be released in
combination with the predaceous mite, P. persimilis, but F.
acarisuga is more mobile in the adult stage than P. per-
similis and eats at least five times more spider mites once it
is established. However, P. persimilis is known to eat
midge eggs if prey is limited, so they should not be
released where F. acarisuga is already established
(Gillespie et al. 1998).
Stethorus punctillum (Weise)
The stethorus Stethorus punctillum (Coleoptera: Coccinel-
idae) ladybeetle has been reported to be efficient in seeking
out spider mite colonies both indoors and outdoors. Each
female beetle is capable of laying about 100 eggs in
her lifetime. Both the larvae and adult beetles feed on
365
all stages of the spider mites and their eggs (Rott and
Ponsonby 2000).
Bacteria and fungi
Many previous studies have underlined the moderate effect
of Bacillus thuringiensis (Bacillales: Bacillaceae) against
T. urticae and its predators (Macintosh et al. 1990; Chap-
man and Hoy 1991). Recently, Aksoy et al. (2008) proved
that the Biotype B of Pseudomonas putida had strong
efficacy in causing the mortality of two-spotted spider
mites. In addition, Aksoy and Mennan (2004) demonstrated
the effects of a fluorescent Pseudomonas sp. isolate against
nematodes. However, none of the fluorescent Pseudomonas
have been used as a biocontrol agent of mites to date,
although an infection that caused disease in T. urticae was
identified as Pseudomonas aeruginosa (Poinar and Poinar
1998). The use of this bacterium is an example of the
increasing interest in direct pathogens of mites, and is
supported by the large number of reviews on this subject
(Mc Coy 1996; Poinar and Poinar 1998; Chandler et al.
2000; Van der Geest et al. 2000). Indeed, the susceptibility
of mites to fungal infections could rapidly lead to efficient
management of spider mites by some entomopathogenic
fungi (Maniania et al. 2008). In such a case, Neozygites
spp. could be used either via inundative release or by
augmentative release. According to Moino et al. (1998), the
application of Beauveria bassiana Balsamo (Hypocreales:
Clavicipitaceae) and Paecilomyces fumosoroseus Apopka
(Deuteromycotina: Hyphomycetes) on T. urticae results in
high rates of mortality. In addition, these fungi could be
used with P. persimilis and N. californicus as well as garlic
extracts as part of an integrated pest management strategy.
However, the susceptibility of mites to entomopathogenic
fungi varies between different isolates of the fungus (Braga
et al. 2009).
Scolothrips longicornis Priesner
Several species of predatory thrips of the genus Scolothrips
(Thysanoptera: Thripidae) have been investigated for their
potential to contribute to the control of spider mites, spe-
cifically S. longicornis (Pakayari et al. 2011). The results of
Pakayari et al. (2009) suggest that S. longicornis seems to
be a good candidate for controlling T. urticae from late
spring to early fall in greenhouses in the Mediterranean
region where the temperature is frequently above 25 °C.
Ecochemical control: an alternative strategy
Chemical mediators, especially allelochemicals, are used in
interspecies communication. These non-nutritional mole-
cules, produced by one organism, can modify the
123
366
behaviour or the biology of an organism from another
species. Consequently, plant allelochemicals exert a wide
range of influence on insects: they can be repellent (Oji-
melukwe and Adler 1999; Ndungu et al. 1995; Huang et al.
2002), deterrent, or antifeedant (Chiam et al. 1999; Ta-
pondjou et al. 2005), and they also seem to be important
agents of interspecific communication, as they favour
pollination by attracting insects. They also play a part in
the defence of plants against herbivores, microorganisms,
and fungi (Regnault-Roger 1997). In addition, they may
increase oviposition or, conversely, decrease reproduction
by ovicidal and larvicidal effects (Regnault-Roger and
Hamraoui 1994a, b; Kim 2003; Obeng-Ofori and Amiteye
2005; Mansour et al. 1986). Most of these molecules are
classified as secondary plant metabolites and have chemi-
cal structures that identify them as alkaloids, polypheno-
lics, terpenes, isoprenoids, cyanogenic glycosides (Strebler
1989), or tannins (Chiasson and Beloin 2007).
The use of these allelochemcials as an alternative strategy
based on the identification of plant insecticidal molecules, is
not recent, as humans have traditionally used plants in order
to protect crops (Golob and Webly 1989). In the nineteenth
century, several active molecules were extracted from
plants: nicotine extracted from tobacco, rotenone from
Derris elliptica (Fabaceae), and pyrethrum from Chrysan-
themum (Compositeae); all of which were chemically
unstable (Philogène et al. 2002). Over the last 15 years,
research has been devoted to find other insecticidal mole-
cules extracted from plants (Arnason et al. 1989).
The essential oils
Among the molecules extracted from plants, essential oils
are obtained by hydrodistillation, steam distillation, dry
distillation, or mechanical cold pressing of aromatic plants
(Bakkali et al. 2008). They have long been used as fragrances
and flavourings in the perfume and food industries, respec-
tively, and more recently for aromatherapy and herbal
medicines (Isman 2001). Plant essential oils are produced
commercially from several botanical sources, particularly
those belonging to the mint family (Lamiaceae). They can be
synthesised by all plant organs, such as buds, flowers, leaves,
stems, twigs, seeds, fruits, roots, wood, or bark, and are, for
some species, stored in secretory cells, cavities, canals,
epidermic cells, or glandular trichomes (Isman 2001).
Plants use essential oils to prevent water loss due to
excessive evaporation (Regnault-Roger 1997). The oils can
also play a major role in pollination by attracting insects.
Repellence is another property of essential oils, as some
contain numerous secondary metabolites that can deter
attacks from insects and general herbivores (Isman 2000).
Thus, the essential oils may serve as a defence for plants
against many pests, including insects (Philogène et al.
123
J Pest Sci (2013) 86:361–386
2002), fungi (Mishra and Dubey 1994; Katooli et al. 2011),
nematodes (Chitwood 2002; Collange 2011), and other
pests (Regnault-Roger and Hamraoui 1994b; Kim 2003;
Miresmailli and Isman 2006).
Contact acaricidal activity of plant extracts have been
well demonstrated against several species of mites (Isman
2000, 2001; Miresmailli and Isman 2006; Gokce et al.
2011), including T. urticae (Roh et al. 2011; Attia et al.
2011a, b, c, d). Indeed, to develop sustainable pest control
in Tunisian citrus orchards, Attia et al. (2011d) evaluated
the effects of 31 plant extracts obtained from Tunisia and
two synthetic acaricides (spirodiclofen and Fenbutatin
oxyde) against T. urticae. Field experiments showed that
the extracts of seven plant species (Haplophyllum tuber-
culatum, Deverra scoparia, Mentha pulegium, Chrysan-
themum coronarium, Hertia cheirifolia, Citrus aurantium,
and Santolina africana) were effective in reducing the
population of T. urticae from 0.3 to 0.53 mites per leaf, and
this reduction was maintained for more than 21 days after
treatment compared with the untreated control (3.7 mites
per leaf). The extracts also showed comparable efficiency
with classical acaricides (0.5 mites per leaf for spirodi-
clofen and 0.53 mites per leaf for Fenbutatin oxyde). The
evaluation of the potential of biologically active plant
volatiles against T. urticae might provide a new approach
to the development of natural acaricides to be used both in
biological and integrated pest management strategies for
controlling two-spotted spider mites in Tunisian citrus
orchards (Attia et al. 2011d).
Advantages of essential oils
Most essential oil constituents degrade quickly in the
environment or are rapidly lost from plant foliage through
volatilisation, which minimises residual contact. They have
short residual activities due to temperature and UV light
degradation (Miresmailli and Isman 2006). In contrast to
some synthetic insecticides, no bio-accumulation or bio-
magnification has been reported to date (Regnault-Roger
et al. 2012), and, with a few exceptions, their mammalian
toxicity is low and environmental persistence is short
(Regnault-Roger et al. 2012).
Essential oils can be applied to both field and green-
house crops in the same manner as current synthetic aca-
ricides. Today essential oils represent a market estimated at
US $700 Million, indicating that a diversified use of
essential oils in the pest management sector could be of
economic benefit (Regnault-Roger 1997).
Disadvantages of essential oils
Expensive compounds The classical preparation method
used for essential oils is based on the Clevenger steam
J Pest Sci (2013) 86:361–386
distillation system, which requires large containers because
of the low (generally \1 %) yield and is costly because of
the high temperatures needed for distillation (Regnault-
Roger et al. 2012). The availability and cost of the natural
source should be considered, both from an economical and
ethical perspective. Currently, at required application rates,
essential oils can only be used for high-value crops or
domestic markets (Regnault-Roger et al. 2012).
Variable composition Genetic differences in plants of the
same species that are otherwise indistinguishable (chemo-
types) can result in widely different essential oil contents.
Therefore, the qualitative and quantitative composition of
extracts and essential oils can vary more than the compo-
sition of synthetic chemicals. In fact, these results, and
those reported earlier, indicate that the acaricidal activity of
the essential oils varies depending on the plant origin of the
essential oil (Tunç et al. 2000; Chiasson et al. 2001; Choi
et al. 2004)
Effect on non-target organisms and environment The
effects of essential oils depend on the target species and
trophic level. For example, under laboratory conditions, a
rosemary-oil-based insecticide/acaricide was significantly
less efficient in the control of predatory mites (P. persim-
ilis) than of their spider mite prey (T. urticae), whereas the
parasitoid Encarsia formosa was more susceptible than its
whitefly hosts (Isman and Machial 2006). Another example
involves the use of essential oils from citronella and basil,
which were shown to be efficient to control the bruchid C.
maculatus, as well as its parasitoid Dinarmus basalis, thus
compromising the biocontrol (Huignard et al. 2008). The
use of these oils was also thought to influence predator
behaviour and the foraging activity of honeybees and other
pollinators (Isman and Machial 2006).
Human health concerns The mammalian toxicity of
essential oils is low and they have been relatively well-
studied, both experimentally and clinically, as a result of
their use as medicinal products (Regnault-Roger et al.
2012). However, their use must be controlled, as some
essential oils may cause irritation of the skin, eyes, and
mucous membranes when applied in concentrated forms. A
good example of this is pulegone, which is considerably
toxic to rats at higher doses (LD50 = 150 mg/kg) (Isman
and Machial 2006). The source of pulegone, pennyroyal
oil, has been implicated in both human and animal poi-
sonings (Anderson et al. 1996). The constituent of the
liqueur absinthe, a-thujone, is also very toxic to rats at high
doses (LD50 = 45 mg/kg) (Höld et al. 2000). Dermal
toxicity was observed with some essential oils, or at least
with the monoterpenes included therein (Regnault-Roger
et al. 2012). Essential oil compounds can easily pass
367
through the blood–brain barrier of the nervous system, and,
as a result, there are numerous examples of neurotoxicity.
Although chronic neurotoxicity of essential oils is poorly
documented, some examples of adverse effects from long-
term animal and human use have been mentioned in the
literature (Regnault-Roger et al. 2012).
Phytotoxic Some phytotoxic effects have been described
for Cymbopogon citratus (Poaceae) or Origanum vulgare
hirtum (Labiales: Labiateae). Both of these oils inhibited the
growth of crops such as wheat (Triticum aestivum L.) and
tomatoes (Lycopersicon esculentum Mill.) (Regnault-Roger
et al. 2012). Environmental conditions, such as temperature,
humidity, and light, can also influence phytotoxicity. Indeed,
high temperatures can increase degradation and volatilisa-
tion of essential oils but may also result in increased phyto-
toxicity for some products. Therefore, future research could
involve testing the phytotoxicity and evaluating the residues
on various vegetables, herbaceous plants, and foliar plant
material, such as fruits in citrus orchards, with regard to plant
extracts and especially essential oils.
Resistance To date, no study has been done on the effect
of these extracts on the resistance of pests. It is necessary to
study the effect of these extracts on the resistance of T.
urticae males that develop from unfertilised eggs. Resis-
tance in males is of major concern because males are
haploid, with an enhanced ability to develop and transfer
resistance to future generations.
Volatility The high volatility of essential oils is an
advantage from an environmental point of view but can be
a disadvantage from an IPM perspective. Indeed, the
absence of persistence can be major problem in any control
strategy as it demands that treatments be repeated several
times (Bruce et al. 2005). The possible negative effects
from repeated spraying of diluted extracts must be inves-
tigated in mammals before implementation on a large scale
in integrated pest and disease management programmes.
Many essential oils have short residual activities due to
temperature and UV light degradation (Miresmailli and
Isman 2006), necessitating repeated applications and pos-
sibly resulting in increased phytotoxicity (Cloyd et al.
2009). Phytotoxicity is not necessarily caused by the active
ingredient, but can be caused by solvents such as TweenÒ
20, impurities in spray water, or by the use of greater
concentrations than those listed on the label.
Unknown mode of action Little is known about the exact
active site of plant extracts and essential oils with regard to
the metabolism of the two-spotted spider mite. In fact, the
observed mortality of T. urticae may be attributed to
123
368
several activities including acetylcholinesterase activity,
P450 cytochrome monooxygenase inhibition (Houghton
et al. 2006), c-Aminobutyric acid (GABA) receptor regu-
lation, and sodium channel alterations (Riveiro et al. 2010).
Some essential oils have been demonstrated to be neuro-
toxic by either inhalation or direct application to the cuticle
in arthropods (Isman 2000; Isman and Machial 2006).
Because of the great number of elements that can con-
stitute essential oils, natural plant extracts might have more
than one specific cellular target (Carson et al. 2002). For
example, James and Xu (2012) suggested that some bo-
tanicals, such as Azadiractin and the aqueous extract of
Artemisia annua L. (Asterales: Asteraceae), can influence
hemocyte number, differentiation, and phagocytosis in
addition to their insecticidal activity.
Ecochemical control of T. urticae including
the essential oils
Sulphur compounds Sulphur-containing amino acids and
their derivatives are found in cruciferous plants and in
Allium, and are known to be toxic to mites (Catar 1954;
Boyd and Alverson 2000; Dabrowski and Seredynska
2007; Hincapié Ll et al. 2008). Moreover, numerous
studies have demonstrated that extracts and preparations
containing these compounds have repellent effects against
T. urticae (Boyd and Alverson 2000; Chiasson et al. 2004;
Philogène et al. 2002).
Plant extracts, such as garlic (Allium sativum Linn.), may
represent a viable alternative. The effect and repellent action
of garlic was tested against Acanthoscelides obtectus Say
(Coleoptera: Bruchidae) (Regnault-Roger and Hamraoui
1993), Tribolium castaneum (Coleoptera: Tenebrionidae)
and Sitophilus zeamais (Coleoptera: Curculionidae) (Ho
et al. 1996; Chiam et al. 1999; Huang et al. 2000), Cydia
pomonella L. (Landolt et al. 1999), Lipaphis erysimi Kal-
tenbach and Dysdercus cingulatus (Hemiptera: Pyrrhocori-
dae) (Bandyopadhyay et al. 2001; Banerjee et al. 2004),
Meloidogyne incognita (Thylinchida: Heteroderidae)
(Chitwood 2002), Reticulitermes santonensis (Isoptera:
Heterotermitidae), Reticulitermes grassei (Isoptera: Ter-
mitidae) (Auger et al. 2004) and Attagenus unicolor japo-
nicus (Coleoprera: Dermestidae) (Han et al. 2006). They
have all been shown to reduce the number of eggs laid as well
as the amount of feeding damage done by certain insects.
Together, these results suggest that garlic may be useful for
controlling T. urticae populations in the field (Singh et al.
2001). Contact acaricidal activity of A. sativum has been well
demonstrated against T. urticae in field conditions (Attia
et al. 2011b). In fact, experiments have shown that the extract
A. sativum was effective and the population of T. urticae was
reduced to 1.7 mites per leaf for more than 21 days after
treatment compared with the untreated control at 3.7 mites
123
J Pest Sci (2013) 86:361–386
per leaf (Attia et al. 2011d). Another future research direc-
tion might be to test the phytotoxicity of various vegetables,
herbaceous plants, and foliar plant material against A. sati-
vum (Cloyd et al. 2009). More importantly, possible toxic
effects of spraying diluted garlic extract (with repeated
applications) must be investigated in mammals before
implementation on a large scale in integrated pest and dis-
ease management programmes.
Pyrethrum The pyrethrum daisy, Tanacetum cinera-
riaefolium (Asterales: Asteraceae) is mainly grown in
Kenya and Australia. Small quantities are also grown in
Tanzania and Ecuador (B. Chung, personal communica-
tion). Pyrethrins obtained from dried flowers are shown to
exert a neurotoxic effect by blocking voltage-gated sodium
channels in nerve axons. The extreme lability of pyrethrins
in the presence of UV and sunlight has led to the devel-
opment of synthetic derivatives (pyrethroids) that are more
stable in sunlight (Isman 2006).
Rotenone Rotenone is an isoflavonoid that is naturally
present in the roots or rhizomes of tropical legumes of the
genus Derris, Lonchocarpus, and Tephrosia, which acts as
a mitochondrial poison. When ingested orally, it blocks the
electron transport chain and prevents energy production
(Hollingworth et al. 1994). It significantly reduces hatching
rates of T. urticae eggs, but is can also affect the mortality
and fecundity of P. persimilis adults (Duso et al. 2008).
This pesticide has two drawbacks: it is persistent on foods
after treatment and is dangerous for non-target organisms
(CEC 2008).
Neem extracts Neem oil obtained from seeds of the Indian
Neem tree Azadirachta indica contains several azadirachtin
analogs, but many lines of evidence point to azadirachtin as
the most important active substance (Isman and Machial
2006). As a pesticide, azadirachtin is an insect growth reg-
ulator and an antifeedant agent. Currently, there is no com-
mercial synthesis of azadirachtin derivatives. Different
studies attempting to evaluate the effects of neem extracts on
T. urticae show controversial results (Duso et al. 2008).
Other essential oils used against T. urticae Several lab-
oratory studies have previously described the acaricidal
activity of essential oils (Table 2). Among the more active
essential oils are those from thyme, garlic, rosemary, and
mint, but more empirical testing on rarer plant species and
a wider array of pest species will undoubtedly reveal par-
ticularly valuable biological activities (Shaaya and Ko-
styukovsky 2006; Isman and Machial 2006).
Most papers document the immediate effects, such as
acute toxicity or repellence, of essential oils on the basis of
 Table 2 List of studies in which plant essential oils have been screened for bioactivity against T. urticae, investigating fumigant and contact toxicity
Family Plant species Reference Type of test Tested treat Efficiency LD50

Alliaceae Allium cepa Attia et al. (2012a) Contact M (larvae) ?

Allium sativum Boyd and Alverson (2000)
Dabrowski and Seredynska (2007)
Hincapié Ll et al. (2008)
M (adult) ?
Fumigant R ??? 50 g/l air
Contact M ? 8.11 mg g-1 air (24 h)
R ??? 5.41 mg g-1 air (48 h)
Fumigation M ??? 2.82 mg g-1 air (72 h)
J Pest Sci (2013) 86:361–386

Attia et al. (2012a) Contact M (larvae) ??

M (adult) ?
Anacardiaceae Pistacia lentiscus Attia et al. (2012a) Contact M (larvae) –
M (adult) –
Cotinus coggyra Attia et al. (2012a) Contact M (larvae) ?
M (adult) ?
Annonaceae Cananga adorata Choi et al. (2004) Fumigation M –
Roh et al. (2011) Contact M –
F –
Apiaceae Coriandrum sativum Choi et al. (2004) Fumigation M ???
Carum carvi Choi et al. (2004) Fumigation M ???
Deverra scoparia Attia et al. (2012a) Contact M (larvae) –
M (adult) –
Daucus carota Attia et al. (2012a) Contact M (larvae) ?
M (adult) ?
Asteraceae Artemisia absinthum Choi et al. (2004) Fumigation M ???
Tagetes glandulifera Choi et al. (2004) Fumigation M –
Anthemis nobilis Choi et al. (2004) Fumigation M ???
Chrysanthemum coronarium Attia et al. (2012a) Contact M (larvae) ???
M (adult) ???
Hertia cheirifolia Attia et al. (2012a) Contact M (larvae) ???
M (adult) ???
Santolina africana Attia et al. (2012a) Contact M (larvae) ??
M (adult) ??
Brassicaceae Sinapsis alba Dabrowski and Seredynska (2007) Contact M –
R ???
369

123
 Table 2 continued
370

Family Plant species Reference Type of test Tested treat Efficiency LD50

123
Burseraceae Boswellia carterii Choi et al. (2004) Fumigation M –
Protium bahianum Pontes et al. (2007) Fumigation M ???
F ???
R ?
Protium bahianum Pontes et al. (2010) Fumigation M ??? 3.5 ll/l air (leaf oil)
R ??? 9.1 ll/l air (fruit oil)
Boswellia carterii Roh et al. (2011) Contact M –
F –
Commiphora myrrha Roh et al. (2011) Contact M –
F –
Capparaceae Capparis aegyptia Hussein et al. (2006) M ???
F ???
R ???
Chenopodiaceae Chenopodium ambrosioides Chiasson et al. (2004) Contact M ???
Oviposition ???
Kochia scoparia Shi et al. (2006) Contact M ??
Cupressaceae Cedrus atlantica Choi et al. (2004) Fumigation M –
Cupressus sempervirens Choi et al. (2004) Fumigation M –
Roh et al. (2011) Contact M –
F –
Juneperus communis Choi et al. (2004) Fumigation M –
Roh et al. (2011) Contact M ?
F –
Juniperus pjoenicea Attia et al. (2012a) Contact M (larvae) ?
M (adult) ?
Juneperus oxycedrus Choi et al. (2004) Fumigation M –
Euphorbiaceae Euphorbia Kansui Dang et al. (2010) Contact M ?
Fabaceae Acacia cyanophylla Attia et al. (2012a) Contact M (larvae) ?
M (adult) –
Sophora secundiflora Attia et al. (2012a) Contact M (larvae) ?
M (adult) ?
Geraniaceae Pelargonium graveolens Choi et al. (2004) Fumigation M ???
Pelargonium roseum Roh et al. (2011) Contact M –
F –
Pelargonium graveolens Attia et al. (2012a) Contact M (larvae) ??
M (adult) ??
Globulariaceae Globularia alypum Attia et al. (2012a) Contact M (larvae) ??
M (adult) ??
J Pest Sci (2013) 86:361–386
 Table 2 continued
Family Plant species Reference Type of test Tested treat Efficiency LD50

Gramineae Vetiveria zizaniodes Choi et al. (2004) Fumigation M –

Cymbopogon martini Choi et al. (2004) Fumigation M ???
Cymbopogon nardus Choi et al. (2004) Fumigation M –
Cymbopogon citratus Choi et al. (2004) Fumigation M ???
Juglandaceae Juglans regia Wang et al. (2009) Fumigation M ???
Lamiaceae Origanum vulgare Choi et al. (2004) Fumigation M ???
J Pest Sci (2013) 86:361–386

Pogostemon cablin Choi et al. (2004) Fumigation M –

Roh et al. (2011) Contact M –
F –
Ocimum basilicum Roh et al. (2011) Contact M –
F –
Origanum majorana Choi et al. (2004) Fumigation M ???
Roh et al. (2011) Contact M –
F –
Lavadula agustifolia Mansour et al. (1986) Contact M ?
R ?
F ???
Lavandula officinalis Choi et al. (2004) Fumigation M ???
Attia et al. (2012a) Contact M (larvae) –
M (adult) –
Lavandula vera Roh et al. (2011) Contact M –
F –
Lavadula angustifolia 9 L. Latifolia Mansour et al. (1986) Contact M ??
R ?
F ???
Ocimum basilicum Mansour et al. (1986) Contact M ?
R ?
F ???
Aslan et al. (2004) Fumigation M ?
Choi et al. (2004) Fumigation M ???
Majorana hortensis Mansour et al. (1986) Contact M ?
R –
F ??
Salvia sclarea Mansour et al. (1986) Contact M –
R ?
F ??
Choi et al. (2004) Fumigation M ???
Roh et al. (2011) Contact M –
F –
371

123
 Table 2 continued
372

Family Plant species Reference Type of test Tested treat Efficiency LD50

123
Salvia dominica Mansour et al. (1986)
Salvia fruticosa Mansour et al. (1986)
Salvia officinalis Mansour et al. (1986)
Choi et al. (2004)
Attia et al. (2012a)
Rosmarinus officinalis Choi et al. (2004)
Mansour et al. (1986)
Miresmailli and Isman (2006)
Roh et al. (2011)
Attia et al. (2012a)
Mentha piperita Choi et al. (2004)
Mansour et al. (1986)
Roh et al. (2011)
Mentha spicata Choi et al. (2004)
Mansour et al. (1986)
Omar et al. (2009)
Mentha pulegium Choi et al. (2004)
Attia et al. (2012a)
Contact M ?
R –
F ??
Contact M ?
R ?
F ???
Contact M ?
R –
F ??
Fumigation M ???
Contact M (larvae) ?
M (adult) ?
Fumigation M –
Contact M ?
R ?
F ???
Contact M ???
Contact M –
F –
Contact M (larvae) ??
M (adult) ?
Fumigation M ???
Contact M ?
R ?
F ???
Contact M –
F –
Fumigation M ???
Contact M ??
R ?
F ??
Contact M ???
R ??
Fumigation M ???
Contact M (larvae) ???
M (adult) ???
J Pest Sci (2013) 86:361–386
 Table 2 continued
Family Plant species Reference Type of test Tested treat Efficiency LD50

Micromeria fruticosa Mansour et al. (1986) Contact M –

R ?
F ??
Çalmasur et al. (2006) Fumigation M ???
Melissa officinalis Mansour et al. (1986) Contact M ??
R ?
J Pest Sci (2013) 86:361–386

F ???
Hyssopus officinalis Mansour et al. (1986) Contact M –
R –
F ?
Artemisia absinthum Chiasson et al. (2001) Contact M ??
Seriphidium herba-album Attia et al. (2012a) Contact M (larvae) ?
M (adult) –
Artemisia judaica El-Sharabasy (2010) Contact M ???
R ???
Tanacetum vulgare Chiasson et al. (2001) Contact M ???
Satureja hortensis Aslan et al. 2004 Fumigation M ???
Thymus vulgaris Choi et al. (2004) Fumigation M ???
Aslan et al. (2004) Fumigation M ?
Roh et al. (2011) Contact M ?
F –
Thymbra capitata Attia et al. (2011d) Contact M (larvae) ?
M (adult) ?
Nepeta racimosa Çalmasur et al. 2006 Fumigation M ???
Origanum vulgare Çalmasur et al. (2006) Fumigation M ???
Hyssopus officinale Roh et al. (2011) Contact M –
F –
Lauraceae Aniba rosaeodora Choi et al. (2004) Fumigation M –
Cinamomum zelandicum Roh et al. (2011) Contact M –
F –
Laurus nobilis Attia et al. (2012a) Contact M (larvae) ?
M (adult) –
373

123
 Table 2 continued
374

Family Plant species Reference Type of test Tested treat Efficiency LD50

123
Meliaceae Azadirachta indica Dabrowski and Seredynska (2007) Contact M ??
R ???
Martı́nez-Villar et al. (2005) Contact M ???
F ???
Knapp and Kashenge (2003) Fertility –
Offspring development –
M ??
R ?
Brito et al. (2006) Oviposition ???
M ???
F ?
R ???
Melia azedarach Attia et al. (2012a) Contact M (larvae) ??
M (adult) ??
Myrtaceae Eugenia caryophyllata Choi et al. (2004) Fumigation M ???
Eucalyptus citriodora Choi et al. (2004) Fumigation M ???
Eucalyptus globulus Choi et al. (2004) Fumigation M ???
Roh et al. (2011) Contact M –
F –
Eucalyptys ghomphocephala Attia et al. (2012a) Contact M (larvae) ?
M (adult) –
Melaleuca leucadendron Roh et al. (2011) Contact M –
F –
Zyzygium aromaticum Roh et al. (2011) Contact M ?
F –
Melaleuca viridiflora Roh et al. (2011) Contact M –
F –
Melaleuca alternifolia Choi et al. (2004) Fumigation M –
Roh et al. (2011) Contact M –
F –
Myrtus communis Choi et al. (2004) Fumigation M –
Attia et al. (2012a) Contact M (larvae) ???
M (adult) –
Pimenta racemosa Choi et al. (2004) Fumigation M ???
Pimenta officinalis Choi et al. (2004) Fumigation M –
Myristicaceae Myristica fragrans Choi et al. (2004) Fumigation M –
Papaveraceae Papaver rhoeas Attia et al. (2012a) Contact M (larvae) –
M (adult) –
J Pest Sci (2013) 86:361–386
 Table 2 continued
Family Plant species Reference Type of test Tested treat Efficiency LD50

Phytolaccaceae Petiveria alliacea Neves et al. (2011) Fumigation M ??? Flower oil (0.16 ll/l air)
Root oil (0.12 ll/l air)
Pinaceae Abies alba Choi et al. (2004) Fumigation M –
Pinus silvestris Roh et al. (2011) Contact M –
F –
Cedrus atlantica Roh et al. (2011) Contact M –
J Pest Sci (2013) 86:361–386

F –
Piperaceae Piper nigrum Choi et al. (2004) Fumigation M –
Roh et al. (2011)
Piper caldensis De Araujo et al. (2010) Fumigation M ??? 1.36 ll/l air
Poaceae Cymbopogon winterianus Roh et al. (2011) Contact M –
F –
Cymbopogon citratus Roh et al. (2011) Contact M –
F –
Punicaceae Punica granatum Abo-Moch et al. (2010) Fumigation M ??
R ?
F ???
Rutaceae Citrus reticulata Choi et al. (2004) Fumigation M –
Citrus aurantifolia Choi et al. (2004) Fumigation M –
Citrus cinensis var. pêra De Araujo et al. (2010) Fumigation M ? 4.63 ll/l air
R ? 2.22 ll/l air
Citrus cinensis var. mimo Fumigation M ??
R ???
Citrus sinensi Choi et al. (2004) Contact M ???
Roh et al. (2011) M ?
F –
Citrus aurantium Choi et al. (2004) Fumigation M ??? 1.63 ll/l air
De Araujo et al. (2010) Fumigation M ???
R ??
Roh et al. (2011) Contact M –
F –
Attia et al. (2012a) Contact M (larvae) ?
M (adult) ?
Citrus limonum Choi et al. (2004) Fumigation M –
Roh et al. (2011) Contact M –
F –
Citrus bergamia Roh et al. (2011) Contact M –
F –
Choi et al. (2004) Fumigation M ???
375

123
 Table 2 continued
Family Plant species
123
Citrus paradisi
Haplophyllum tuberculatum
Ruta chalepensis
Solanaceae Capsicum chinese
Capsicum frutescens
Capsicum baccatum
Capsicum annuum
Capsicum pubescens
Lycopersicon hirsutum
Lycopersicon glabratum
Lycopersicon pennellii
Lycopersicon pimpinellifolium
Datura stramonium
Santalum austrocaledonicum
Santalaceae Santalum album
Urticaceae Urtica dioica
Urtica pilulifera
Verbenaceae Lippia sidoides
Lantana camara
376
Reference Type of test Tested treat Efficiency LD50
Choi et al. (2004) Fumigation M –
Roh et al. (2011) Contact M –
F –
Attia et al. (2012a) Contact M (larvae) ???
M (adult) ???
Attia et al. (2012a) Contact M (larvae) ?
M (adult) ?
Antonious et al. (2006) Fumigation M ?
R ?
M ?
R ?
M ??
R ???
M ??
R ???
M ?
R ?
Antonious and Snyder (2006) Contact M ???
R ???
M –
R –
M –
R –
M –
R –
Kumral et al. (2009) Contact M ???
R ??
Roh et al. (2011) Contact M ??
F ?
Choi et al. (2004) Fumigation M –
Dabrowski and Seredynska (2007) Contact M ??
R ???
Attia et al. (2012a) Contact M (larvae) –
M (adult) –
Cavalcanti et al. (2010) Fumigation M ??? 0.01 ll/l air
Attia et al. (2012a) Contact M (larvae) –
M (adult) –
J Pest Sci (2013) 86:361–386
J Pest Sci (2013) 86:361–386 377

assays persisting less than 48 h (Table 3). For example,

Miresmailli and Isman (2006) described the acaricidal
activity of Rosmarinus officinalis L. (Labiales: Labiatae)
essential oil and blends of its major components against T.
urticae on two host plants. T. urticae is susceptible to the
LD50

composition of the essential oils therein evaluated

(Table 3).
Mansour et al. (1986) pointed out that besides the tox-
icity, the residues of essential oils from some Labiatae
Efficiency

species are repellent, and strongly reduce the fecundity of

???

T. urticae females. Some essential oils are highly selective

–
–
–
–
–

and specifically affect the pest populations without affect-

ing their predators (Miresmailli and Isman 2006). In Chi-
asson et al. (2004), the effect of Chenopodium
ambrosioides oil (Caryohyllales: Chenopodiaceae) was
assessed on both T. urticae and the predator Panonychus
Tested treat

citri. Other studies highlighted the fact that the essential

M (larvae)
M (adult)

oils of Satureja hortensis L., and Thymus vulgaris L. were

F fecundity, M mortality, R repellency, ? toxic, ?? slightly toxic, ??? highly toxic, - not toxic, DL50 dose which kills 50 % of individuals

effective as fumigants against Bemisia tabaci (Homoptera:

M
M
M
F

Aleyrodidae) and T. urticae (Aslan et al. 2004).

Attia et al. (2011a, b, 2012b) investigated the acaricidal
effects of four plant extracts collected from Tunisia on the
Type of test

Fumigation
Fumigation

spider mite: Deverra scoparia, Santolina africana, Hertia

Contact

Contact

cheirifolia, and Allium sativum. Compared to synthetic

acaricides, the efficacy of these four extracts against the
two-spotted spider mite is significantly higher with lower
LC50 values, and greater decreases in fecundity.

Resistance to synthetic and natural pesticides

Attia et al. (2012a)
Choi et al. (2004)
Choi et al. (2004)
Roh et al. (2011)

Previous studies reported that successive treatments with

chemical products and the extended persistence of pesti-
Reference

cides could lead to the development of resistance. For

example, acrinathrin is a chemical product used to control
T. urticae and was commercialised by Bayer Crop Science
in 1991 (Pinochet 1991). This product affects the nervous
system of mites by blocking the nerve signal and pro-
longing the opening of sodium ion channels, therefore
resulting in a moderate environmental persistence, corre-
sponding to a DT50 of 52 days (Dekeyser 2005). A spray
Elettaria cardamomum

bioassay of this chemical product showed that a strain of T.

Perganum harmala
Zingiber officinale

urticae could develop resistance towards Acrinathrin after

20 generations (Kim et al. 2006). Other cases of resistance
Plant species

to acaricides are due to mutations in the mitochondrial

cytochrome b protein of T. urticae, which is a mitoc-
hondrially encoded protein in the respiratory pathway (Van
Nieuwenhuyse et al. 2009; Van Leeuwen et al. 2008). In
Table 2 continued

fact, like insects, spider mites can develop resistance

Zygophyllaceae

through enhanced metabolic detoxification of acaricides

Zingiberaceae

and also through mutations in the target site (Knowles

Family

1997). It was demonstrated that cross-resistance to Ace-

quinocylÒ in two bifenazate-resistant strains was

123
378 J Pest Sci (2013) 86:361–386

Table 3 Toxicity of some essential oil constituents to T. urticae investigating fumigant and contact toxicity
Essential oil Compound Reference Type of test Tested Efficiency LD50
treat

Santalum Santalol Roh et al. (2011) Contact M ???

austrocaledonicum F –
Lippia sidoides Thymol Cavalcanti et al. (2010) Fumigation M ??? 0.001 ll/l air
p-Cymene ? 3.020 ll/l air
b-Caryophyllene ?? 0.08 ll/l air
Carvacrol ?? 0.036 ll/l air
Citrus sinensis var. pêra Limonene De Araujo et al. (2010) Fumigation R ?? 0.004 ll/l air
Citrus sinensis var. mimo a-Pinene
Citrus aurantium Myrcene
Linalool
Eugenol
Euphorbia kansui 3-O-(2,3-Dimethylbutanoyl-13- Dang et al. (2010) Contact M ???
O-dodecanoyeingenol
3-O-(20 E,40 Z-Decadienoyl)- –
Ingenol
Eugenol ?
Rosmarinus officinalis Camphene Miresmailli and Isman (2006) Residue contact M –
1,8-Cineole ???
b-Pinene ?
Camphor –
p-cymene –
Borneol –
D-Limonene –
a-Terpineol –
Bornyl acetate –
a-Pinene ???
Anethole Erler and Tunç (2005) Fumigation M ???
F ???
Carvacrol M ???
F ???
1,8-Cineole M ???
F ???
p-Cymene M ???
F ???
Menthol M ???
F ???
c-Terpinene M ???
F ???
Terpinen-4-ol M ???
F ???
Thymol M ???
F ???
Carvomenthenol Lee et al. (1997) Fumigation M ???
Terpinen-4-ol ???

F fecundity, M mortality, R repellency, ? toxic, ?? slightly toxic, ??? highly toxic, - not toxic, DL50 dose which kills 50 % of individuals

maternally inherited and caused by the combination of two
specific mutations in the cytochrome b Qo pocket (Van
Nieuwenhuyse et al. 2009).
To avoid resistance development to essential oils or
plant extracts, essential oils should be used alternatively or
in combination with other extracts or biological products.
In fact, the acaricidal activity of plant essential oils is often
enhanced by the presence of several chemical compounds,
and they exhibit more than one mode of action. However,
essential oils can act synergistically or, at the very least, by
diffusing selection in insect herbivores or mites, thereby
inhibiting the development of resistance (Feng and Isman

123
J Pest Sci (2013) 86:361–386
1995) and the behaviour (Akthar and Isman 2004) in those
insect herbivores (Isman and Akhtar 2007).
Commercialisation of pesticides based on essential oils?
Essential oil-based pesticides will not be a panacea against
all pests, but there should be a substantial market. Until
now, products based on essential oils have not been
accepted by growers for crop protection (Isman 2000).
There are at least three barriers to the commercialisation of
new products based on essential oils (Isman 2000, 2006).
The first barrier is the scarcity of the natural resource or
the availability of the plant material on a sustainable basis
(Isman 2000). In our previous studies, the yield of essential
oil varied greatly. The maximum yields were obtained with
H. cheirifolia (0.7 %), S. africana (0.6 %), and D. scoparia
(0.5 %) (Attia et al. 2011a, 2012b). However, these plants
are endemic to the North of Africa, and are not available all
year round. For the treatment of 10 ha of citrus orchards,
about 550 kg of plants from the three species must be
collected in order to generate the necessary yield. In terms
of specific constraints, the long-term efficiency of these
plant extracts falls short when compared to synthetic pes-
ticides, as they are not persistent. In fact, essential oils
present low persistence, requiring a higher application rate
and frequent reapplications when used in the field (Koul
et al. 2008). Therefore, huge quantities may ultimately be
needed.
Conversely, other species of plants, such as the garlic
extract of A. sativum, are abundant and available all year
round from the food industry. However, Attia et al. (2011b)
showed that garlic extract did not yield essential oil, so
they tested the effects of the distillate. Distillates are
widely available and are especially interesting as their
production is not expensive in comparison with essential
oils when extracted by farmers. Moreover, their extraction
is easier and does not require large quantity of biomass, in
contrast to essential oils. Garlic is easy to grow and can be
grown year-round in mild climates. In addition, garlic
plants can be grown close together, leaving enough room
for the bulbs to mature, and are easily grown in containers
of sufficient depth. This plant is, therefore, still a potential
tool for the control of T. urticae. However, the use of garlic
via spray applications may affect the odour of the flowers
or the fruits. Further studies need to be addressed in order
to confirm this hypothesis.
The cost of essential oils may also be a critical factor for
their implementation, which depends on the availability of
the plant and its yield per hectare (Cavalcanti et al. 2010).
Some essential oils can be used as insecticides and acari-
cides in the field on crops (Isman 2000). Alternatively, it
may be possible to cultivate plants on a commercial scale.
379
Further cultivation for use in the pest control industry
should, therefore, be achievable both here and throughout
other parts of the world.
The second barrier is the standardisation and refinement
of pesticide products based on the quantification of active
ingredients, i.e. the protection of technology, regulatory
approval, and increasing quality control (Isman 2000). In
fact, standardisation could open the door for new users,
drive an increase in market size, trigger new technology
refinements, reduce costs, and set the stage for the next
level of standardisation.
The composition of a plant extract depends on the
material of biological origin, season, climate conditions,
and manufacturing process, and may also depend on further
processing. Geographic locations and agricultural factors
also influence oil production (Noudjou et al. 2007; Nasra-
badi et al. 2009). Indeed, the formation of essential oils in
plants, as well as the yield and composition of the oil
produced, depend on many factors, such as genetic dif-
ferences in plants of the same species that are otherwise
indistinguishable (chemotypes) that can result in widely
different essential oil contents (Nasrabadi et al. 2009). For
example, a report from Assareh et al. (2007) indicated that
1,8-cineole (41.9 %), a-pinene (13.7 %), and aromadend-
rene (3.7 %) were the main constituents of the oil of leaves
from Eucalyptus loxophleba Benth from Iran. More
recently, Nasrabadi and Batooli (2011) showed that the
major components of E. loxophleba essential oil were 1,8-
cineole (39.4 %), methyl amyl acetate (19.8 %), and aro-
madendrene (10.0 %). These differences might have been
derived both from harvest time and local, climatic, and
seasonal factors, or the fact that these samples may belong
to a different chemotype (Nasrabadi and Batooli 2011).
The composition of oils obtained from plants growing in
different localities in the south east of Tunisia is known to
vary considerably (Ben Haj et al. 2007), but no information
appears to be available on North African species.
The third barrier is difficulty in obtaining government
approval and the legal registration of new pesticides.
Normally, this process requires the costly toxicological
evaluation of candidate products (Isman 2000). Many plant
extracts, such as garlic, Lavandula officinalis, Mentha
pulegium, and other aromatic plant oils, have other, more
significant, non-pesticidal uses, such as food additives,
food flavourings, and components of cosmetics, soaps,
perfumes, and other products.
The European Community Regulation on chemicals and
their safe use (REACH) deals with the Registration,
Evaluation, Authorisation, and Restriction of Chemical
substances in Europe. The aim of REACH is to improve the
protection of human health and the environment through
enhanced identification of the intrinsic properties of
chemical substances. It aims to better the innovation and
123
380
competitiveness of the European chemical industry
(REACH 2012). It deals with transmitting safety informa-
tion on classified substances and mixtures, including
information obtained from the Chemical Safety Report,
directly to the immediate user. It sets out the criteria for the
identification of persistent, bio-accumulative and toxic
(PBT) substances (REACH 2012). For these reasons, fur-
ther experiments are required in order to verify the effects
of each substance on humans, specifically farmers.
As the essential oils and their purified components have
a long history of global utilisation by the food and fra-
grance industries, as well as in the field of aromatherapy,
several of the oils and components are already present in
the market.
In the European Union, the procedure for the re-evalu-
ation of plant protection products ended in 2008 (Regnault-
Roger et al. 2012). This procedure allowed for the inclu-
sion of active substances that were not found to have
harmful effects on human health, animals, ground water, or
any unacceptable effects on the environment. For example,
since 2009, orange oil has been allowed in France for the
control of whitefly on field pumpkins and for the control of
greenhouse whitefly on tomatoes (OJEU 2009). In Bel-
gium, it is possible to buy many sprays containing essential
oils that aim to kill mites and insects. Additional products,
such as EcoVETTM for veterinary use, are also under
development (Isman 2000). Another product produced in
Italy, Apilife VARTM, is based on thymol and cineole
(Koul et al. 2008).
American companies have also developed essential oil-
based pesticides, such as CinnamiteTM (Mycotech, Butte,
MT), and ValeroTM, which are miticides or fungicides.
Both products are based on cinnamon oil, with cinnamal-
dehyde (Isman 2000). RequiemTM, developed by Codena,
was registered in the United States in 2008, and it was the
first botanical to be registered since 2005 for use against a
wide range of pests including aphids, whitefly, thrips, and
mites (Chiasson et al. 2008). EcoSMART Technologies
produces products containing different mixtures of essen-
tial oil compounds, such as eugenol and 2-phenethyl pro-
pionate, in order to control domestic pests (Isman 2000).
This American company has 20 product formulations that
are exempt from EPA registration under the rules defined
in the 1996 Food Quality Protection Act. Under these rules,
EcoSMART’s EPA-exempt products can make unique,
explicit safety claims not allowed with traditional pesti-
cides. These safety claims enable EcoSMART to clearly
distinguish its products from conventional, synthetic
products.
The fact that these products are now considered safe
from a legal point of view is an opportunity for the com-
mercialisation of these types of products. But it is critical
that essential oils be tested against lab animals before being
123
J Pest Sci (2013) 86:361–386
considered safe for the environment and non-target
organisms, including human beings, as with any pesticide.
Conclusion
Many plant essential oils and their components have a
broad spectrum of activity against mites, many other pests.
As such, they have considerable potential as crop protec-
tants and for pest management in other situations. It is
important to note, however, that the essential oils that are
most efficient against pests are often the most phytotoxic
(Isman 2000). This latter issue requires serious attention
when manufacturing products for agricultural and land-
scape use. In order to produce these essential oils on an
industrial scale, future experiments and developments are
still needed.
First, future research should be directed toward the
improvement of processing and extraction methods in
order to obtain high grade extracts while simultaneously
preserving or improving the biological properties. It is also
possible to select chemotypes that produce greater yields of
essential oils and then purify the molecules in order to
obtain blends that can kill mites. Second, more testing on
the phytotoxicity of plant extracts and essential oils, and
the evaluation of the residues on various vegetables, her-
baceous plants, and foliar plant material, is also necessary.
In the case of unavailable plant material, the essential oil
components and/or their blends should be used.
Third, further studies are necessary to elucidate the
mode of action of essential oils on mites, specifically T.
urticae. This kind of study should involve understanding
how the targeted pests’ systems normally function (Enan
2001). Although the octopaminergic nervous system is
considered to be the site of action of essential oils against
the American cockroach (Enan 2005a, b), this may not be
the case for the two-spotted spider mite. Therefore, the
other potential properties of plants that are toxic for pests
must be studied before being used in an integrated program
of pest control.
Fourth, future work should study the advantages and
drawbacks of plant extracts from an economical point of
view, and to compare them with chemical applications
effects, taking into account environmental pollution and
the potential apparition of resistance in pest population.
Finally, other studies are necessary to determine the
toxicity and the repellence of these extract residues on
predatory mites and on non-target arthropods. These stud-
ies would also elucidate the feasibility of the use of these
extracts on other economically serious pests in citrus
orchards where pest management depends on chemical
applications. It will also be necessary to study the effect of
these extracts on the resistance potential of pests. Such
J Pest Sci (2013) 86:361–386
measures might be integrated in agriculture to protect the
environment, as well as the fauna and flora. In fact, bees
and other pollinators provide crucial services, and other
beneficial insects including predators and parasitoids pro-
vide valuable pest management services to agriculture.
Indeed, this information might guide the selection and use
of appropriate varieties of such plants in traditional control
strategies.
A diversified use of plant extracts in the pest manage-
ment sector could have both economic and ecological
benefits. To develop more effective and safer pesticides, as
well as application techniques in the future, it is compul-
sory to promote basic research by coordination among
academic resources and in governmental and industrial
agencies with a sense of responsibility from all concerned.
We expect that pesticides based on essential oils will find
their greatest commercial application in worldwide urban
pest control. In agriculture, these pesticides will be most
useful for protected crops, such as in greenhouses where
few alternative pesticides are available. As conventional
yet hazardous pesticides are removed from the marketplace
and the cost of developing new chemical products contin-
ues to rise, it is likely that pesticides based on plant
essential oils will gain further acceptance. The changing of
consumer preference towards the use of natural products,
the existence of niche markets where the quality is more
important than the price, the potential to extend pesticides
based on essential oils through biotechnology, and, the
production of plant extracts in developing countries are all
opportunities for the increase in use of plant extracts and
essential oils. The efficiency of these changes requires
productive collaboration between different groups, such as
agronomists, entomologists, chemists with experience in
pest behaviours and technology, and, finally, the crop
producers.
Acknowledgments The authors are very grateful to Georges Van
Impe and Thomas Van Leeuwen for useful discussions about Tetr-
anychus urticae. They are also indebted to Wallonies-Bruxelles
International (WBI). This is publication BRC 270 of the Biodiversity
research centre at UCL.
References
Abo-Moch F, Saadi I, Holland D, Mansoura F (2010) The potential of
pomegranate peel and heartwood extracts as a source of new
bioacaricides to control the carmine spider mite Tetranychus
cinnabarinus. Israel J Plant Sci 58:13–17
Aksoy HM, Mennan S (2004) Biological control of Heterodera
cruciferae (Tylenchida: Heteroderidae) Franklin 1945 with
fluorescent Pseudomonas spp. J Phytopathol 152:514–518
Aksoy HM, Ozman-Sullivan SK, Ocal H, Celik N, Sullivan GT
(2008) The effects of Pseudomonas putida biotype B on
Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol
46:223–230
381
Akthar Y, Isman MB (2004) Feeding responses of specialist
herbivores to plant extracts and pure allelochemicals: effects of
prolonged exposure. Entomol Exp Appl 111:201–208
Anderson IB, Mullen WH, Meeker JE, Khojasteh-Bakht SC, Oishi S,
Nelson SD et al (1996) Pennyroyal toxicity: measurement of
toxic metabolite levels in two cases and review of the literature.
Ann Intern Med 124:726–734
Antonious GF, Snyder JC (2006) Natural products: repellency and
toxicity of wild tomato leaf extracts to the two-spotted spider
mite, Tetranychus urticae Koch. J Environ Sci Heal B 41:43–55
Antonious G, Meyer J, Snyder J (2006) Toxicity and repellency of hot
pepper extracts to spider mite, Tetranychus urticae Koch.
J Environ Sci Heal B 41:1383–1391
Arnason JT, Philogene BJR, Morand P (1989) Insecticides of plant
origin. ACS Symposium Series, London
Aslan I, Ozbek H, Calmasur O, Sahin F (2004) Toxicity of essential
oil vapours to two greenhouse pests, Tetranychus urticae Koch
and Bemisia tabaci Genn. Ind Crops Prod 19:167–173
Assareh MH, Jaimand K, Rezaee MB (2007) Chemical composition
of the essential oils of six Eucalyptus species (Myrtaceae) from
South West of Iran. J Essent Oil Research 19:8–10
Attia S, Grissa KL, Lognay G, Heuskin S, Mailleux AC, Hance T
(2011a) Chemical composition and acaricidal properties of
Deverra scoparia essential oil (Araliales: Apiaceae) and blends
of its major constituents against Tetranychus urticae (Acari:
Tetranychidae). J Econ Entomol 104:1220–1228
Attia S, Grissa KL, Mailleux AC, Lognay G, Heuskin S, Mayoufi S,
Hance T (2011b) Effective concentrations of garlic distillate
(Allium sativum) for the control of Tetranychus urticae (Tetr-
anychidae). J Appl Entomol. doi:10.1111/j.1439-0418.2011.
01640.x
Attia S, Grisssa LK, Ghrabi GZ, Mailleux AC, Lognay G, Le Goff G,
Hance T (2011c) Contrôle de Tetranychus urticae par les extraits
de plantes en vergers d’agrumes. Faunistic Entomol 63:229–235
Attia S, Grisssa LK, Ghrabi-Gammar Z, Lognay G, Mailleux A-C,
Hance T (2011d) Assessment of the acaricidal activity of several
plant extracts on the phytophagous mite Tetranychus urticae
(Tetranychidae) in Tunisian citrus orchards. SRBE 147:71–79
Attia S, Grisssa LK, Ghrabi GZ, Mailleux A-C, Lognay G, Hance T
(2012a) Acaricidal activity of 31 essential oils extracted from
plants collected in Tunisia. J Essent Oil Res 24:279–288
Attia S, Grissa KL, Lognay G, Heuskin S, Mailleux AC, Hance T
(2012b) Acaricidal activities of Santolina africana and Hertia
cheirifolia against Tetranychus urticae (Acari: Tetranychidae).
Pest Manag Sci. doi:10.1002/ps.3269
Auger J, Arnault I, Diwo-Allain S, Ravier M, Molia F, Pettiti M
(2004) Insecticidal and fungicidal potential of Allium substances
as biofumigants. Agroindustria 3:5–8
Ay R, Yorulmaz S (2010) Inheritance and detoxification enzyme
levels in Tetranychus urticae Koch (Acari: Tetranychidae) strain
selected with chlorpyrifos. J Pest Sci 83:85–93
Bajwa W, Schaefers G (1998) Indigenous crop protection practices in
sub-saharan East Africa. http//www.ippc.orst.educ/ipmafrica/
elements/ncpp. Accessed 23 June 2010
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological
effects of essential oils—a review. Food Chem Toxicol
46:446–475
Bandyopadhyay S, Roy A, Das S (2001) Binding of garlic (Allium
sativum) leaf lectin to the gut receptors of homopteran pests is
correlated to its insecticidal activity. Plant Sci 161:1025–1033
Banerjee S, Hess D, Majumder P, Roy D, Das S (2004) The
interactions of Allium sativum leaf agglutinin with a chaperonin
group of unique receptor protein isolated from a bacterial
endosymbiont of the mustard aphid. J Biol Chem 279:
23782–23789
123
382
Basta A, Spooner-Hart RN (2002) Efficacy of an extract of Dorrigo
pepper against two-spotted mite and greenhouse thrips. In: Spray
oils beyond 2000, Australia. University of Western, Sydney,
pp 471–476
Ben Haj JI, Ghrabi GZ, Zouaghi M (2007) Valorisation de la
biodiversité en plantes médicinales et étude ethnobotanique de la
flore du sud-ouest du kef. Ethnopharmacologia 39:36–43
Berger A (1994) Using natural pesticides: current and future
perspectives. A report for the plant protection. Improvement
programme in Botswana, Zambia and Tanzania
Bethke A, Siapno O, Redak R (2001) The latest miticides. Green-
house Product News 14:54–56
Boyd DW, Alverson DR (2000) Repellency effects of garlic extracts
on the two-spotted spider mite, Tetranychus urticae Koch.
J Entomol Sci 35:86–90
Braga RB, Araujo JV, Silva AR, Araujo JM, Carvalho RO, Tavela
AO, Campos AK, Carvalho GR (2009) Biological control of
horse cyathostomin (Nematoda: Cyathostominae) using the
nematophagous fungus Duddingtonia flagrans in tropical south-
eastern Brazil. Vet Parasitol 163:335–340
Brito HM, Gondim Júnior MGC, Oliveira JV, Câmara CAG (2006)
Toxicidade de formulaçoes de nim (Azadirachta indica A. Juss.)
ao ácaro-rajado ea Euseius alatus De Leone Phytoseiulus
macropilis (Banks) (Acari: Phytoseiidae); Toxicity of neem
(Azadirachta indica A. Juss) formulations for twospotted spider
mite and Euseius alatus De Leon and Phytoseiulus macropilis
(Banks) (Acari: Phytoseiidae). Neotrop Entomol 35:500–505
Bruce TJ, Birkett MA, Blande J, Hooper AM, Martin JL, Khambay B
(2005) Response of economically important aphids to compo-
nents of Hemizygia petiolata essential oil. Pest Manag Sci
61:1115–1121
Çalmaşur Ö, Aslan İ, Şahin F (2006) Insecticidal and acaricidal effect
of three Lamiaceae plant essential oils against Tetranychus
urticae Koch and Bemisia tabaci Genn. Ind Crop Prod
23:140–146
Carson CF, Mee BJ, Riley TV (2002) Mechanism of action of
Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus
determined by time-Kill, lysis, leakage and salt tolerance assays
and electron microscopy. Antimicrob Agents Chemother 46:
1914–1920
Castiglioni E, Vendramin JD, Tamai MA (2002) Evaluación del
efecto tóxico de extractos acuosos y derivados de meliáceas
sobre Tetrancychus urticae (Koch) (Acari, Tetrancychidae).
Agrociencia 6:75–82
Catar G (1954) Effect of plant extracts on Ixodes ricinus. Bratislava
Med J 34:1004
Cavalcanti SCH, Niculau Edos S, Blank AF, Câmara CAG, Araújo
IN, Alves PB (2010) Composition and acaricidal activity of
Lippia sidoides essential oil against two-spotted spider mite
(Tetranychus urticae Koch). Bioresour Technol 101:829–832
CEC (2008) Commission decision of 10 April 2008, concerning the
non-inclusion of rotenone, extract from equisetum and chinin-
hydrochlorid in Annex I to Council Directive 91/414/EEC and
the withdrawal of authorisations for plant protection products
containing these substances. Official Journal of the European
Union, pp 30–32
Chandler D, Davidson G, Pell JK, Ball BV, Shaw K, Sunderland KD
(2000) Fungal biocontrol of Acari. Biocontrol Sci Technol
3157:357–385
Chapman MH, Hoy MA (1991) Relative toxicity of Bacillus
thuringiensis var. tenebrionis to the two-spotted spider mite
(Tetranychus urticae Koch) and its predator Metaseiulus occi-
dentalis (Nesbitt) (Acari, Tetranychidae and Phytoseiidae).
J Appl Entomol 111:147–154
Chiam WY, Huang Y, Chen SX, Shuit HH (1999) Toxic and
antifeedant effects of allyl disulphide on Tribolium castaneum
123
J Pest Sci (2013) 86:361–386
(Coleoptera: Tenebrionidae) and Sitophilus zeamais (Coleoptera:
Curculionidae). J Econ Entomol 92:239–245
Chiasson H, Beloin N (2007) Les huiles essentielles, des biopesticides
«Nouveau genre». Ann Soc Entomol Que 14:3–6
Chiasson H, Bélanger A, Bostanian N, Vincent C, Poliquin A (2001)
Acaricidal properties of Artemisia absinthium and Tanacetum
vulgare (Asteraceae) essential oils obtained by three methods of
extraction. J Econ Entomol 94:167–171
Chiasson H, Bostanian NJ, Vincent C (2004) Acaricidal properties of
a Chenopodium-based botanical. J Econ Entomol 97:1373–
1377
Chiasson H, Delisle U, Bostanian NJ, Vincent C (2008) Recherche,
développement et commercialisation de FACIN, un biopesticide
d’origine végétale. Etude d’un cas de réussite en Amérique du
Nord 98:451–463
Chitwood DJ (2002) Phytochemical based strategies for nematode
control. Annu Rev Phytopathol 40:221–249
Choi W-I, Lee S-G, Park H-M, Ahn Y-J (2004) Toxicity of plant
essential oils to Tetranychus urticae (Acari: Tetranychidae) and
Phytoseiulus persimilis (Acari: Phytoseiidae). J Econ Entomol
97:553–558
Clegg CJ, Mackean DG (1994) Advanced biology: principles and
applications. John Murray, London
Cloyd RA, Galle CL, Keith SR, Kalscheur NA, Kemp KE
(2009) Effect of commercially available plant-derived essential
oil products on arthropod pests. J Econ Entomol 102:1567–
1579
Collange B (2011) Root-knot nematode (Meloidogyne) management
in vegetable crop production: the challenge of an agronomic
system analysis. Crop Prot 30:1251–1262
Dabrowski TZ, Seredynska US (2007) Characterisation of the two-
spotted spider mite (Tetranychus urticae Koch, Acari: Tetrany-
chidae) response to aqueous extracts from selected plant species.
J Plant Prot Res 47:113–124
Dang QL, Choi YH, Choi GJ, Jang KS, Park MS, Park N-J et al
(2010) Pesticidal activity of ingenane diterpenes isolated from
Euphorbia kansui against Nilaparvata lugens and Tetranychus
urticae. J Asia Pacific Entomol 13:51–54
De Araujo MJC, De Oliveira WH, Born FDS, Ribeiro NDC, De
Moraes MM, Neves RCS, et al (2010) Actividade Fumigante Do
Oleo Essential de Folhas de Piper caldensis C. DC. Sobre
Tetranychus urticae Koch (Acari: Tetranychidae). XI JEPEX
Dekeyser MA (2005) Acaricide mode of action. Pest Manag Sci
61:103–110
Duso C, Chiarini F, Conte L, Bonora V, Monta LD, Otto S (2004)
Fogging can control Tetranychus urticae on greenhouse cucum-
bers. J Pest Sci 77:105–111
Duso C, Malagnini V, Pozzebon A, Castagnoli M, Liguori M, Simoni
S (2008) Comparative toxicity of botanical and reduced-risk
insecticides to Mediterranean populations of Tetranychus urticae
and Phytoseiulus persimilis (Acari Tetranychidae, Phytoseiidae).
Biol Control 47:16–21
El-Sharabasy HM (2010) Acaricidal activities of Artemisia judaica L.
extracts against Tetranychus urticae Koch and its predator
Phytoseiulus persimilis Athias Henriot (Tetranychidae: Phyto-
seiidae). J Biopest 3:514–519
Enan E (2001) Insecticidal activity of essential oils: octopaminergic
sites of action. Comp Biochem Physiol C: Toxicol Pharmacol
130:325–337
Enan E (2005a) Molecular and pharmacological analysis of an
octopamine receptor from American cockroach and fruit fly in
response to plant essential oils. Arch Insect Biochem Physiol
59:161–171
Enan E (2005b) Molecular response of Drosophila melanogaster
tyramine receptor cascade to plant essential oils. Insect Biochem
Mol Biol 35:309–321
J Pest Sci (2013) 86:361–386
Erler F, Tunç T (2005) Monoterpenoids as fumigants against
greenhouse pests: toxic, development and reproduction-inhibit-
ing effects. J Plant Dis Protect 112:181–192
Feng R, Isman MB (1995) Selection for resistance to azadirachtin in
the green peach aphid, Myzus persicae. Experientia 51:831–833
Ferrero M, Calvo FJ, Atuahiva T, Tixier M-S, Kreiter S (2011)
Biological control of Tetranychus evansi Baker & Pritchard and
Tetranychus urticae Koch by Phytoseiulus longipes Evans in
tomato greenhouses in Spain [Acari: Tetranychidae, Phytoseii-
dae]. Biol Control 58:30–35
Flamini G (2003) Acaricides of natural origin, personal experiences
and review of the literature (1990–2001). Stud Nat Prod Chem
28:381–451
Flamini G (2006) Acaricides of natural origin. Part 2. Review of the
literature (2002–2006). Nat Prod Commun 1:1151–1158
Floris I, Satta A, Cabras P, Garau VL, Angioni A (2004) Comparison
between two thymol formulations in the control of Varroa
destructor: effectiveness, persistence, and residues. J Econ
Entomol 97:187–191
Fytoweb (2008) http://www.fytoweb.fgov.be/
Georghiou GP (1986) The magnitude of the resistance problem. In:
Pesticide resistance: strategies and tactics for management.
National Academy Press, Washington, DC, pp 11–44
Gillespie DR, Roitberg B, Basalyga E, Johnstone M, Opit G, Rodgers
J, Sawyer N (1998) Biology and application of Feltiella
acarisuga (Vallot) (Diptera: Cecidomyiidae) for biological
control of two-spotted spider mites on greenhouse vegetable
crops. Pacific Agri-Food Research Centre (Agassiz) Technical
Report 145 Agriculture and Agri-Food Canada
Gokce A, Isaacs R, Whalon ME (2011) Ovicidal, larvicidal and anti-
ovipositional activities of Bifora radians and other plant extracts
on the grape berry moth Paralobesia viteana (Clemens). J Pest
Sci 84:487–493
Golob P, Webly DJ (1989) The use of plants and minerals as traditional
protectants of stored products. Trop Prod Inst 138:1–32
Han MK, Kim SI, Ahn YJ (2006) Insecticidal and antifeedant activities
of medicinal plant extracts against Attagenus unicolor japonicus
(Coleoptera: Dermestidae). J Stored Prod Res 42:15–22
Han J, Choi B-R, Lee S-G, Kim SI, Ahn Y-J (2010) Toxicity of plant
essential oils to acaricide-susceptible and -resistant Tetranychus
urticae (Acari: Tetranychidae) and Neoseiulus californicus
(Acari: Phytoseiidae). J Econ Entomol 103:1293–1298
Hay RKM, Watermen PG (1993) Volatile oil crops. Wiley, New York
Helle H, Sabelis MW (1985) Spider mites: their biology, natural
enemies and control. Elsevier, Amsterdam
Heuskin S (2011) Contribution to the study of semiochemical slow-
release formulations as biological control devices. PhD thesis.
Université de Liège, Gembloux, Agrobiotech, Belgium
Hincapié Ll CA, López PGE, Torres ChR (2008) Comparison and
characterisation of garlic (Allium sativum L.) bulbs extracts and
their effect on mortality and repellency of Tetranychus urticae
Koch (Acari: Tetranychidae). Chil J Agric Res 68:317–327
Ho SH, Koh L, Ma Y, Huang Y, Sim KY (1996) The oil of garlic,
Allium sativum L. (Amaryllidaceae), as a potential grain
protectant against Tribolium castaneum (Herbst) and Sitophilus
zeamais Motsch. Postharvest Biol Technol 9:41–48
Höld KM, Sirisoma NS, Ikeda T, Narahashi T, Casida JE (2000) a-
Thujone (the active component of absinthe): c-aminobutyric acid
type a receptor modulation and metabolic detoxification. Proc
Natl Acad Sci USA 97:3826–3831
Hollingworth RM, Ahammadsahib KI, Gadelhak G, McLaughlin JL
(1994) New inhibitors of complex I of the mitochondrial electron
transport chain with activity as pesticides. Biochem Soc Trans
22:230–233
Houghton PJ, Jayne M, Ren Y (2006) Acetylcholinesterase inhibitors
from plants and fungi. Nat Prod Rep 23:181–199
383
Huang Y, Chen SX, Ho SH (2000) Bioactivities of methyl allyl
disulphide and diallyl trisulfide from essential oils of garlic to
two species of stored-product pests, Sitophilus zeamais (Cole-
optera: Curculionidae) and Tribolium castaneum (Coleoptera:
Tenebrionidae). J Econ Entomol 93:537–543
Huang Y, Ho SH, Lee HC, Yap YL (2002) Insecticidal properties of
eugenol, isoeugenol and methyleugenol and their effects on
nutrition of Sitophilus zeamais Motsch. (Coleoptera: Curculion-
idae) and Tribolium castaneum (Herbst) (Coleoptera: Tenebri-
onidae). J Stored Prod Res 38:403–412
Huignard J, Lapied B, Dugravot S, Magnin-Robert M, Ketoh GK
(2008) Modes d’action neurotoxiques des derives soufres et de
certaines huiles essentielles et risques lies a leur utilisation. In:
Philogène B et al (eds) Biopesctides d’origine végétale. Lavoi-
sier, Paris, pp 219–231
Hussein H, Abou-Elelia M, Amer SAA, Momen FM (2006)
Repellency and toxicity of extracts from Capparis aegyptia L.
to Tetranychus urticae Koch. (Acari: Tetranychidae). Acta
Phytopathol Hung 41:331–340
IRAC (2008) Mode of Action Classification. http://www.
irac-online.org
Isman MB (2000) Plant essential oils for pest and disease manage-
ment. Crop Prot 19:603–608
Isman MB (2001) Pesticides based on plant essential oils for
management of plant pests and diseases. In: symposium on
development of natural pesticides from forest resources. Repub-
lic of Korea, Seoul, pp 1–9
Isman MB (2004) Plant essential oils as green pesticides for pest and
disease management. ACS Symp Ser 887:41–51
Isman MB (2006) The role of botanical insecticides, deterrents and
repellents in modern agriculture and an increasingly regulated
world. Annl Rev Entomol 51:45–66
Isman MB, Akhtar Y (2007) Plant natural products as a source for
developing environmentally acceptable insecticides. In: Ishaaya
I, Nauen R, Horowitz AR (eds) Insecticides design using
advanced technologies. Springer, Berlin, pp 235–248
Isman MB, Machial CM (2006) Pesticides based on plant essential
oils: from traditional practice to commercialisation. In: Rai M,
Carpinella MC (eds) Naturally occurring bioactive compounds.
Elsevier, New York, pp 29–44
James RR, Xu J (2012) Mechanisms by which pesticides affect insect
immunity. J Invertebr Pathol 109:175–182
Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to
economic plants. University of California, London
Jhonson WT, Lyon HH (1991) Insects that feed on trees and shrubs.
Cornell University, Ithaca
Katooli N, Maghsodlo R, Razavi SE (2011) Evaluation of eucalyptus
essential oil against some plant pathogenic fungi. J Plant Breed
Crop Sci 3:41–43
Katsvanga CAT, Chigwaza S (2004) Effectiveness of natural herbs,
Fever tea (Lippia javanica) and Mexican marigold (Tagetes
minuta) as substitutes to synthetic pesticides in controlling aphid
species (Brevicoryne brassica) on cabbage (Brassica capitata).
Trop Subtrop Agroecosyst 4:101–106
Kennedy GG (2003) Tomato, pests, parasitoids, and predators:
tritrophic interactions involving the genus Lycopersicon. Annu
Rev Entomol 48:51–72
Kim S (2003) Contact and fumigant activities of aromatic plant
extracts and essential oils against Lasioderma serricorne (Cole-
optera: Anobiidae). J Stored Prod Res 39:11–19
Kim YJ, Park HM, Cho JR, Ahn YJ (2006) Multiple resistance
and biochemical mechanisms of pyridaben resistance in Tetr-
anychus urticae (Acari: Tetranychidae). J Econ Entomol
99:954–980
Knapp M, Kashenge SS (2003) Effects of different neem formulations
on the two-spotted spider mite, Tetranychus urticae Koch, on
123
384
tomato (Lycopersicon Esculentum Mill.). Int J Trop Insect Sci
23:1–7
Knowles CO (1997) Mechanisms of resistance to acaricides. In: Sjut
V (ed) Molecular mechanisms of resistance to agrochemicals.
Springer, Berlin, pp 57–77
Koul O, Walia S, Dhaliwal GS (2008) Essential oils as green
pesticides: potential and constraints. Biopest Int 4:63–84
Kropczynska A, Pilko A, Witul A, Asshleb AM (1999) Control of
two-spotted spider mite with Amblyseius californicus on cotton.
IOBC/WPRS Bull 22:133–136
Kumral NA, Cobanoglu S, Yalcin C (2009) Acaricidal, repellent and
oviposition deterrent activities of Datura stramonium L. against
adult Tetranychus urticae (Koch). J Pest Sci 21:23–30
Kumral NA, Çobanoğlu S, Yalcin C (2010) Acaricidal, repellent and
oviposition deterrent activities of Datura stramonium L. against
adult Tetranychus urticae (Koch). J Pest Sci 83:173–180
Kunz SE, Kemp DH (1994) Insecticides and acaricides: resistance
and environmental impact. Rev Off Int Epizoot 13:1249–1286
Landolt PJ, Hofstetter RW, Biddick LL (1999) Plant essential oils as
arrestants and repellents for neonate larvae of the codling moth
(Lepidoptera: Tortricidae). Environ Entomol 28:954–960
Lee S, Tsao R, Peterson C, Coats JR (1997) Insecticidal activity of
monoterpenoids to Western Corn Rootworm (Coleoptera:
Chrysomelidae), Twospotted Spider Mite (Acari: Tetranychi-
dae), and House Fly (Diptera: Muscidae). J Econ Entomol
90:883–982
MacIntosh SC, Stone TB, Sims SR, Hunst PL, Greenplate JT,
Marrone PG (1990) Specificity and efficacy of purified Bacillus
thuringiensis proteins against agronomically important insects.
J Invertebr Pathol 56:258–266
Mansour F, Ravid U, Putievsky E (1986) Studies of the effects of
essential oils isolated from 14 species of Labiatae on the carmine
spider mite Tetranychus cinnabarinus. Phytoparasitica 14:
137–142
Maniania NK, Bugeme DM, Wekesa VW, Delalibera IJ, Knapp M
(2008) Role of entomopathogenic fungi in the control of
Tetranychus evansi and Tetranychus urticae (Acari: Tetranychi-
dae), pests of horticultural crops. Exp Appl Acarol 46:259–274
Marcic D (2012) Acaricides in modern management of plant-feeding
mites. J Pest Sci 85:395–408
Markkula M, Tiittanen K (1969) Effect of fertilisers on the
reproduction of Tetranychus telarius (L.), Myzus persicae (lz)
and Acyrthosiphon pisum Harris. Ann Agric Fenn 8:9–14
Martı́nez-Villar E, Sáenz-De-Cabezón FJ, Moreno-Grijalba F, Marco
V, Pérez-Moreno I (2005) Effects of azadirachtin on the two-
spotted spider mite, Tetranychus urticae (Acari: Tetranychidae).
Exp Appl Acarol 35:215–222
Mc Coy CW (1996) Pathogens of eriophyoid mites. In: Lindquist EE,
Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology,
natural enemies and control. Elsevier, Amsterdam, pp 481–490
McMurtry JA, Croft BA (1997) Life-styles of Phytoseiid mites and
their roles in biological control. Annu Rev Entomol 42:291–321
Migeon A, Dorkeld F (2007) Spider Mites Web: a comprehensive
database for the Tetranychidae. http://www.montpellier.inra.fr/
CBGP/spmweb. Accessed 3 February 2011
Miresmailli S, Isman MB (2006) Efficacy and persistence of rosemary
oil as an acaricide against two-spotted spider mite (Acari:
Tetranychidae) on greenhouse tomato. J Econ Entomol
99:2015–2023
Mishra AK, Dubey NK (1994) Evaluation of some essential oils for
their toxicity against fungi causing deterioration of stored food
commodities. Appl Environ Microbiol 60:1101–1105
Moino A, Alves SB, Pereira RM (1998) Efficacy of Beauveria
bassiana (Balsamo) Vuillemin isolates for control of stored-
grain pests. J Appl Entomol 122:301–305
123
J Pest Sci (2013) 86:361–386
Nasrabadi MR, Batooli H (2011) Chemical composition of essential
oils of two cultivated Eucalyptus species from central Iran.
J Plant Breed Crop Sci 3:379–381
Nasrabadi RM, Gholivand MB, Batooli H (2009) Chemical compo-
sition of the essential oil from leaves and flowering aerial parts
of Haplophyllum Robustum Bge. (Rutaceae). Digest J Nanoma-
ter Biostruct 4:819–822
Ndungu M, Lwande W, Hassanali A, Moreka L, Chhabra SC (1995)
Cleome monophylla essential oil and its constituents as tick
(Rhipicephalus appendiculatus) and maize weevil (Sitophilus
zeamais) repellents. Entomol Exp Appl 76:217–222
Neves IIDA, Da Camara CAG, De Oliviera JCS, De Almeida AV
(2011) Acaricidal activity and essential oil composition of
Petiveria alliacea L. from Pernambuco (Northeast Brazil).
J Essent Oil Res 23:23–26
Nihoul P (1993) Controlling glasshouse climate influences the
interaction between tomato glandular trichome, spider mite and
predatory mite. Crop Prot 12:443–447
Noudjou F, Kouninki H, Ngamo LST, Maponmestsem PM, Ngas-
soum M, Hance T, Haubruge E, Malaisse F, Marlier M, Lognay
G (2007) Effect of site location and collecting period on the
chemical composition of Hyptis spicigera Lam. an insecticidal
essential oil from North-Cameroon. J Essent Oil Res 19:597–601
Obeng-Ofori D, Amiteye S (2005) Efficacy of mixing vegetable oils
with pirimiphos-methyl against the maize weevil, Sitophilus
zeamais Motschulsky in stored maize. J Stored Prod Res
41:57–66
OJEU (2009) Official Jouranl of Union Commission Decision of 8
June 2009 recognising in principle the completeness of the
dossier submitted for detailed examination in view of the
possible inclusion of orange oil in Annex I to Council Directive
91/414/EEC (notified under document number C-4232)
52:145–147
Ojimelukwe PC, Adler C (1999) Potential of zimtaldehyde, 4-ally-
lanisol, linalool, terpineol and other phytochemicals for the
control of the confused flour beetle (Tribolium confusum J. d. V.)
(Col., Tenebrionidae). Anz Schädlingskde 72:81–86
Omar AN, El Sayed IAZ, Romeh AA (2009) Chemical constituents
and biocidal activity of the essential oil of Mentha Spicata L.
grown in Zagazig region. J Agric Biol Sci 6:1089–1097
Osborne LS, Ehler LE, Nechols JR (1985) Biological control of the
two-spotted spider mite in greenhouses. Fl Agric Exp Stn Bull
853:40
Pakayari H, Fathipour Y, Rezapanah M, Kamali K (2009) Temper-
ature-dependent functional response of Scolothrips longicornis
Priesner (Thysanoptera: Thripidae) preying on Tetranychus
urticae Koch (Acari: Tetranychidae). J Asia-Pacific Entomol
12:23–26
Pakayari H, Fathipour Y, Enkegaard A (2011) Estimating develop-
ment and temperature thresholds of Scolothrips longicornis
(Thysanoptera: Thripidae) on eggs of two-spotted spider mite
using linear and nonlinear models. J Pest Sci 84:153–163
Philogène BJR, Regnault-Roger C, Vincent C (2002) Produits
phytosanitaires insecticides d’origine végétale: promesses d’hier
et d’aujourd’hui. In: (2ème édition) Produits insecticides phy-
tosanitaires d’origine végétale. Lavoisier, Paris, pp 1–17
Pinochet G (1991) Acrinathrin: an acaricide for vineyards and
orchards. Phytoma 428:54–57
Poinar G, Poinar R (1998) Parasites and pathogenes of mites. Annu
Rev Entomol 43:449–469
Pontes WJT, de Oliveira JCS, da Camara CAG, Lopes A, Junior M,
de Oliveira JV et al (2007) Composition and acaricidal activity
of the resin’s essential oil of Protium bahianum Daly against the
two-spotted spider mite (Tetranychus urticae). J Essent Oil Res
19:379–389
J Pest Sci (2013) 86:361–386
Pontes W, Silva J, Da Camara C, Gondim-Junior M, Olivera J,
Schwartz M (2010) Chemical composition and acaricidal
activity of the essential oils from fruits and leaves of Protium
bahianum Daly. J Essent Oil Res 22:279–282
Powell C, Lindquist R (1997) Spider mites (Acari-Tetranychidae).
Ball Publishing, Batavia
Press Release (2011) Spider Mites Secrets Revealed. Tiny pest’s
genome opens door to novel approaches to crop protection and
silk production. http://www.igc.gulbenkian.pt/media/article/87
Rasikari HL, Leach DN, Waterman PG, Spooner-Hart RN, Basta AH,
Banbury LK et al (2005) Acaricidal and cytotoxic activities of
extracts from selected genera of Australian Lamiaceae. J Econ
Entomol 98:1259–1266
REACH (2012) European Comiission environment. http://ec.europa.eu/
environment/chemicals/reach/reviews_en.htm
Regnault-Roger C (1997) The potential of botanical essential oils for
insect pest control. IPM Rev 2:25–34
Regnault-Roger C, Hamraoui A (1993) Efficiency of plants from the
South of France used as traditional protectants of Phaseolus
vulgaris L. against its bruchid Acanthoscelides obtectus (Say).
J Stored Prod Res 29:259–264
Regnault-Roger C, Hamraoui A (1994a) Inhibition of reproduction of
Acanthoscelides obtectus Say (Coleoptera), a kidney bean
(Phaseolus vulgaris) bruchid, by aromatic essential oils. Crop
Prot 13:624–628
Regnault-Roger C, Hamraoui A (1994b) Comparison of the insecti-
cidal effects of water extracted and intact aromatic plants on
Acanthoscelides obtectus, a bruchid beetle pest of kidney beans.
Chemoecology 1:1–5
Regnault-Roger C, Vincent C, Arnasson JT (2012) Essential oils in
insect control: low-risk products in a high-stakes world. Annu
Rev Entomol 57:405–425
Riveiro A, Vézilier J, Weill M, Read AF, Gandon S (2010).
Insecticide control of vector-borne diseases: when is insecticide
resistance a problem? PLoS Pathogen 6. doi:10.1371/journal.
ppat.1001000
Rizzieri DA, Dennehy TJ, Glover TJ (1998) Genetic analysis of
dicofol resistance in two populations of the two-spotted spider
mite (Acari: Tetranychidae) from New York apple orchards.
J Econ Entomol 81:1271–1276
Rodriguez JG (1979) Recent advances in acarology, vol I. London,
New York
Roh HS, Lim EG, Kim J, Park CG (2011) Acaricidal and oviposition
deterring effects of santalol identified in sandalwood oil against
the two-spotted spider mite, Tetranychus urticae Koch (Acari:
Tetranychidae). J Pest Sci 84:495–501
Rondon SI, Price JF, Liburd OE, Francis R, Cantliffe DJ (2005)
Neoseiulus californicus McGregor: a predatory mite species for
controlling two-spotted spider mites in strawberries. University
of Florida, IFAS, Cooperative Extension Service, Gainesville,
FL. EDIS HS245
Rott AS, Ponsonby DJ (2000) Improving the control of Tetranychus
urticae on edible glasshouse crops using a specialist coccinellid
(Stethorus punctillum Weise) and a generalist mite (Amblyseius
californicus McGregor) as biocontrol agents. Biocontrol Sci
Technol 10:87–498
Ruscoe CNE (1977) The new NRDC pyrethroids as agricultural
insecticides. Pest Sci 8:236–242
Ryan MF, Byrne O (1988) Plant–insect coevolution and inhibition of
acethylcholinesterase. J Chem Ecol 14:1965–1975
Sabelis MW (1986) The functional response of predatory mites to the
density of two-spotted spider mites. In: Metz JAJ, Diekmann O
(eds) Dynamics of structured populations. Springer, Berlin
Saxena P (1989) Role of demographic data in monitoring status of
women and recent fertility transition. In: Bose A, Desai PB (eds)
Population planning in India. B.R. Publishing Corporation, Delhi
385
Shaaya E, Kostyukovsky M (2006) Essential oils: potency against
stored product insects and mode of action. Stewart Posthar Rev
2:1–6
Shi GL, Zhao LL, Liu SQ, Cao H, Clarke SR, Sun JH (2006)
Acaricidal activities of extracts of Kochia scoparia against
Tetranychus urticae, Tetranychus cinnabarinus, and Tetranychus
viennensis (Acari: Tetranychidae). J Econ Entomol 99:858–863
Singh UP, Prithiviraj B, Sarma BK, Singh M, Ray AB (2001) Role of
garlic (Allium sativum L.) in human and plant diseases. Indian J
Exp Biol 39:310–322
Steiner MY, Spohr LJ, Goodwin S (2011) Impact of two formulations
of the acaricide bifenazate on the spider mite predator Phyto-
seiulus persimilis Athias-Henriot (Acari: Phytoseiidae). Aust J
Entomol 50:99–105
Strebler G (1989) Les Médiateurs chimiques: leur incidence sur la
bioécologie des animaux. Lavoisier, Paris
Stumpf N, Zebitz CPW, Kraus W, Moores GD, Nauen R (2001)
Resistance to organophosphates and biochemical genotyping of
Acetylcholinesterases in Tetranychus urticae (Acari: Tetrany-
chidae). Pest Biochem Physiol 69:131–142
Sundaram KMS, Sloane L (1995) Effects of pure and formulated
azadirachtin, a neem-based biopesticide, on the phytophagous
spider mite, Tetranychus urticae Koch. J Environ Sci Health Part
B 30:801–814
Tapondjou AL, Adler C, Fontem DA, Bouda H, Reichmuth C (2005)
Bioactivities of cymol and essential oils of Cupressus semper-
virens and Eucalyptus saligna against Sitophilus zeamais
Motschulsky and Tribolium confusum du Val. J Stored Prod
Res 41:91–102
Tewary DK, Bhardwaj A, Shanker A (2005) Pesticidal activities in
five medicinal plants collected from mid hills of western
Himalayas. Ind Crop Prod 22:241–247
Tirello P, Pozzebon A, Cassanelli S, Van Leeuwen T, Duso C (2012)
Resistance to acaricides in Italian strains of Tetranychus urticae:
toxicological and enzymatic assays. Exp Appl Acarol 57:53–64
Tunç İ, Berger BM, Erler F, Dağlı F (2000) Ovicidal activity of
essential oils from five plants against two stored-product insects.
J Stored Prod Res 36:161–168
Van de Vrie M, McMurtry JA, Huffaker C (1972) Ecology of
Tetranychid mites and their natural enemies: a review. III.
Biology, ecology, and pest status, and host-plant relations of
tetranychids. Hilgardia 41:343–432
Van der Geest LP, Elliot SL, Breeuwer JA, Beerling EA (2000)
Diseases of mites. Exp Appl Acarol 24:497–560
Van Leeuwen T, Van Pottelberge S, Tirry L (2006) Biochemical
analysis of a chlorfenapyr-selected resistant strain of Tetrany-
chus urticae Koch. Pest Manag Sci 62:425–433
Van Leeuwen T, Van Pottelberge S, Nauen R, Tirry L (2007)
Organophosphate insecticides and acaricides antagonise bife-
nazate toxicity through esterase inhibition in Tetranychus
urticae. Pest Manag Sci 63:1172–1177
Van Leeuwen T, Vanholme B, Van Pottelberge S, Van Nie-
euwenhuyze P, Nauen R, Tirry L, Denholm I (2008) Mitochon-
drial heteoplasmy and the evolution of insecticide resistance:
non-Mendelian inheritance in action. PNAS 105:5980–5985
Van Leeuwen T, Vontas T, Tsagkarakou A (2009) Mechanisms of
acaricide resistance in the two-spotted spider mite Tetranychus
urticae. In: Ishaaya I, Horowitz AR (eds) Biorational control of
arthropod pests. Springer, Dordrecht, pp 347–393
Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L
(2010) Acaricide resistance mechanisms in the two-spotted
spider mite Tetranychus urticae and other important Acari: a
review. Insect Biochem Mol Biol 40:563–572
Van Nieuwenhuyse P, Van Leeuwen T, Khajehali J, Vanholme B,
Tirry L (2009) Mutations in the mitochondrial cytochrome b of
Tetranychus urticae Koch (Acari: Tetranychidae) confer cross-
123
386 J Pest Sci (2013) 86:361–386

resistance between bifenazate and acequinocyl. Pest Manag Sci
65:404–412
Wang YN, Wang HX, Shen ZJ, Zhao LL, Clarke SR, Sun JH et al
(2009) Methyl palmitate, an acaricidal compound occurring in
green walnut husks. J Econ Entomol 102:196–202
Whalon AE, Mota-Sanchez RM, Hollingworth, RM, Duynslager L
(2008) Arthropods Resistant to Pesticides Database (ARPD).
http://www.pesticideresistance.org. Accessed 18 December 2011

123