Tetranychus urticae (two-spotted spider mite)

T. urticae is a highly polyphagous, cosmopolitan species, which is readily spread on the wind. Under optimum conditions, it reaches a high population density, and its presence can cause a reduction in crop yield.

Tetranychus urticae is part of a group of very similar species in the genus Tetranychus. At one time, a species complex included about 60 synonyms, each described from different hosts or from different parts of the world, the best known of which were Tetranychus telarius L., Tetranychus bimaculatus Harvey and Tetranychus altheae von Hanstein. The taxonomy of the genus Tetranychus is still problematical, but may be elucidated using molecular techniques.The list of other names used excludes Tetranychus cinnabarinus, which may be the same species (see Similarities to Other Pests and datasheet for Tetranychus cinnabarinus). Additional synonyms are provided in Bolland et al. (1998). T. urticae is also known as the red spider mite.

EggsThe egg is 0.13 mm in diameter, globular and translucent.LarvaThe larva is pale green and has six legs.Nymphal stagesThere are two nymphal instars, protonymph and deutonymph, with a quiescent interval between them and another between the deutonymph and adult. The nymphs are pale green with darker markings and have eight legs.AdultsThe adult female is 0.6 mm long, pale green or greenish-yellow with two darker patches on the body, which is oval with quite long hairs on the dorsal side. Overwintering females are orange-red in colour. The male has a smaller, narrower, more pointed body than the female.

T. urticae occurs in most parts of the world. It has been recorded from most countries in Europe, Asia, Africa, Australasia, the Pacific and Caribbean islands, North, Central and South America.Other reference sources are given in Bolland et al. (1998).

T. urticae disperses by active walking or by passive transport in the wind and on plants, tools and people (Zhang, 2003). Phoretic dispersal of T. urticae mediated by winged insects is thought to be rare in the wild (Yano, 2004).

T. urticae has a very wide host range. It includes many crops grown in glasshouses such as tomatoes, cucumbers and peppers and flowers such as chrysanthemums and orchids. It is also a problem on protected and unprotected strawberries. In some areas it is a problem on field-grown fruit crops such as apples, pears and on grapevines. Other important crops that are infested include cotton, soyabeans and other legumes. This mite can also live on many non-crop hosts, which can provide a source of infestation. A more exhaustive list of hosts is given by Bolland et al. (1998).

Feeding by T. urticae causes pale spots to appear on leaves. As infestations become more severe, leaves appear bronzed or silvery, become brittle, and may fall prematurely. Plants can be killed quite rapidly by this mite.The mites spin webbing, which can cover all the surfaces of the plant.

Several species of Tetranychus look similar to T. urticae, and have similar biology. Some of the morphological differences between Tetranychus species were described by Boudreaux and Dosse (1963). However, it is difficult to separate some of these species and, more recently, new biochemical and molecular techniques have been used to try and distinguish between them. Enohara and Amano (1996) studied six species of Tetranychus common in Japan, which are difficult to separate: T. urticae, T. kanzawai, T. phaselus, T. ludeni, T. viennensis and T. piercis. They found that esterase patterns showed species specific characteristics and that the morphological characters of the adult females could also be used to distinguish between species. Goka and Takafuji (1997) used polyacrylamide gel electrophoresis to study the differences between two enzymes among seven species of Tetranychus and concluded that these enzymes could be useful markers for classification. Navajas et al. (1997) used nucleotide sequence variation and morphological characters to study the evolutionary relationships among nine tetranychid mite species.The relationship/conspecificity with Tetranychus cinnabarinus is still problematical: molecular techniques seem to show them as conspecifics, for example, Gotoh and Tokioka (1996). More recently, Zhang and Jacobson (2000) reported on the use of adult female morphological characters to differentiate between T. urticae and T. cinnabarinus. They stated that T. cinnabarinus could be readily separated from T. urticae by variation in the number of setae on tibia I in females.

GeneticsImportant economic species of Tetranychidae tend to have a chromosome number of n = 3 (Hussey and Huffaker, 1976). See Overmeer and Harrison (1969) and Mitchell (1972) for reports on genetic variation with respect to factors controlling the sex ratio of T. urticae. Refer to Hussey and Huffaker (1976), and references therein, for further information on the genetics of spider mites.Physiology and phenologyT. urticae has an overwintering or diapause form of the adult female that is initiated by short photoperiod, decreased temperature and unfavourable food supply. The overwintering females stop feeding and egg laying and leave their host plants to hibernate in cracks and crevices in protected places, such as the soil or glasshouse structures. They resume activity in the spring when they lay eggs on leaves. These mites also produce copious amounts of webbing.Reproductive biologyThe development of the mite is rapid, particularly at high temperatures. At 30-32°C, which is the optimum temperature for development, the egg stage lasts 3-5 days, the larval/nymphal stages 4-5 days, and with a pre-oviposition period of 1-2 days, the total life cycle takes only 8-12 days. Each female can lay an average of 90-110 eggs during a lifetime of about 30 days, therefore numbers of mites can increase very rapidly during the summer, or under glass or plastic.There is much additional information available on cytology and sex determination, mating behaviour, sex ratio, genetics, etc. Much of this information is reviewed in the chapters by various authors in the volumes on spider mites edited by Helle and Sabelis (1995a, b).

At each separate locality there is a complex of local predators, hence lists of natural enemies are long and of limited value in other locations. The most effective natural enemies of T. urticae are predatory mites from the family Phytoseiidae. These mites, belonging to a number of genera, such as Amblyseius, Euseius, Neoseiulus and Phytoseius, have been shown to regulate populations of T. urticae on a range of crops. Phytoseiulus persimilis successfully controls the mite in greenhouses. It is also sometimes useful outdoors and has been released into the field; usually augmentative releases are required to maintain control.Species of Stethorus, a group of small ladybird beetles (Coccinellidae), are also important predators of spider mites. Other useful predators include anthocorids (mainly Orius spp.), larvae of chrysopids, thrips (e.g. Scolothrips spp.), staphylinids (e.g. Oligota spp.), and larvae of cecidomyiid midges, in particular Feltiella acarisuga (=Therodiplosis persicae).Epidemics of fungal disease sometimes occur, particularly in warm, humid conditions. These epidemics are usually caused by Neozygites spp.

During feeding the mites penetrate the plant foliage/leaves with their mouth stylets and suck out the cell contents. On strawberry, low populations of T. urticae mainly damage the spongy mesophyll tissue but higher densities increase the area of damage and injury to the palisade parenchyma occurs (Sances et al., 1979; Kielkiewicz and Van de Vrie, 1983). The function of the stomatal apparatus is also affected, so that the stomata remain closed.

The result of this damage to leaf tissue is reduced chlorophyll content and reduced photosynthesis, carbon dioxide assimilation and transpiration. Such effects have been shown for cotton (Bondana et al., 1995), tomato (Nihoul et al., 1992), apple and peach (Mobley and Marini, 1990), and strawberry (Sances et al., 1982).

Crop yields are diminished as essential plant processes are affected. This has been demonstrated on maize (Archer and Bynum, 1993), strawberry (Oatman et al., 1982), pear (McNab and Jerie, 1993), cotton (Wilson, 1993), soyabean (Singh, 1988; Suekane et al., 2012) and grapevine (Hluchy and Pospisil, 1992), among others.

The mites feed directly on tomato fruit, causing gold fleck (discolouration of the fruit), which could have a negative impact on the marketability of the fruit (Meck et al., 2012).

Nyoike and Liburd (2013) studied the impact of the mites on the marketable yield of field grown strawberries in Florida and reported that yield reduction in strawberry was detected when plants had 80 mites per leaf in the 2008/2009 growing season, and 50 mites per leaf in the 2009/2010 growing season. Results like this can be used to determine the timing of control programmes, ensuring maximum yields are attained.

The timing of mite infestation has also been shown to have an impact. For example, Gore et al. (2013) reported that early infestations of T. urticae on cotton in mid-southern USA caused the highest impact on yield (compared with later infestations).

Severely infested plants can be recognized by speckling and bronzing of the leaves and the presence of webbing. However, it is important to detect infestations before they reach this stage by examining the leaves, with a hand lens or under a microscope, to reveal the mites. Some sampling schemes have been developed that use the presence or absence of mites on a sample of leaves, to reduce the time spent counting (Raworth, 1986; Butcher et al., 1987).

Biological Control

T. urticae has been the subject of some of the most successful examples of biological control. The predator used most often has been the phytoseiid mite Phytoseiulus persimilis. This species was first used in glasshouses, on various crops, in the 1960s (for example, Hussey et al., 1965), and since then has been used successfully on a wide variety of crops in a range of protected and unprotected environments. Several biological control companies package this predator for distribution on to plants by growers. Suitable release rates and timings vary with the crop. In areas where the mite has been established, augmentative releases are required to maintain control.

However, P. persimilis is active only under a limited range of conditions (Gorski and Eajfer, 2003), and so other species of phytoseiid mite have also been used against T. urticae. For example, Amblyseius idaeus and Phytoseiulus macropilis have been used on strawberry and cucumber in Brazil (Watanabe et al., 1994). Metwally et al. (2005) investigated life table and prey consumption of the predatory mite Neoseiulus cynodactylon, and concluded that T. urticae was a profitable prey species of this phytoseiid as a facultative predator.

Predators from other insect families have also shown promise as biocontrol agents against T. urticae. For example, the chrysopid Mallada basalis has been used on strawberry in Taiwan (Tzeng and Kao, 1996). Yanagita et al. (2014) reported that the predatory thrip Scolothrips takahashii could be used as an effective control agent against T. urticae in integrated pest management programmes for strawberry plug plants. Other potential predatory biocontrol agents include Orius minutus (Fathi, 2013), Coccinellla septempunctata (Sirvi and Singh, 2014), Stethorus gilvifrons (Ahmad et al., 2010) and Stethorus punctillum (Gorski and Eajfer, 2003).

Neoseiulus californicus has shown promise as an agent in conservation biological control of T. urticae; the natural control of the mite in strawberries was used as the basis for developing an integrated management plan, using acaricide only when necessary (Greco et al., 2011).

Shivaprakash et al. (2004) reported on the natural occurrence of the entomopathogenic fungus Beauveria bassiana on T. urticae in an okra plot grown without the use of chemicals in Bangalore, Karnataka, India. Laboratory tests using entomopathogens against T. urticae have also been carried out (e.g. Simova and Draganova, 2003; Chandler et al., 2005).

Host-Plant Resistance

Research to find sources of resistance to T. urticae has been carried out on a variety of crops, including Impatiens (Al-Abbasi and Weigle, 1982), soyabean (Mohammad and Rodriguez, 1985), Pelargonium (Chang et al., 1972), cucumber (de Ponti, 1980), Vigna angularis (Aguilar et al., 1996), strawberry (Shanks and Moore, 1995; Easterbrook and Simpson, 1998; Olbricht et al., 2014), watermelon (Lopez et al., 2005; El-Saiedy et al., 2011), maize (Mead et al., 2010), tomato (e.g. Saeidi and Mallik, 2012) and citrus (Agut et al., 2014). Several studies have found differences in susceptibility to the mite between different cultivars or selections. However, the resistance may be polygenic in most cases (Easterbrook and Simpson, 1998), and so is difficult to exploit by plant breeders. Even partial resistance is potentially useful in IPM programmes, however, as it slows the rate of population increase of the spider mite, and so makes it easier for predators to gain control.

Mechanisms of host-plant resistance to T. urticae have been attributed to flavonoid pathways in citrus (Agut et al., 2014), leaf trichomes on Fragaria (Olbricht et al., 2014) (shown to entrap mites on tomato [Saeidi and Mallik, 2012]), increased peroxidase and polyphenol oxidase activity in melon (Shoorooei et al., 2013), antibiosis and antixenosis in bean (Kamelmanesh et al., 2010), phytochemical compounds in watermelon, where El-Saiedy et al. (2011) reported a negative relationship between mite infestation and tannins, and nitrogen and protein content in maize leaves (Mead et al., 2010).

Chemical Control

T. urticae is very difficult to control with acaricides because most populations developed resistance to chemical groups after a few years of use (Cranham and Helle, 1985). In some cases, cross-resistance to other chemical groups has also developed. For example, resistance to the ovicide clofentezine developed quite rapidly, and cross-resistance to hexythiazox also occurred (Thwaite, 1991). Al-Jboory et al. (2004) reported that a bromopropylate-resistant strain (R) of T. urticae showed strong positive cross-resistance towards dicofol and a mixture of dicofol and tetradifon, moderate positive cross-resistance towards amitraz, and low negative cross-resistance towards chlorpyrifos. No cross-resistance was observed towards abamectin and dinobuton.

Later, control often relied on acaricides from a group that act as inhibitors of mitochondrial respiration in the mite (METIs), such as pyridaben, fenpyroximate, fenazaquin and tebufenpyrad. However, resistance was detected in a relatively short space of time, leading to decreased susceptibility to all the compounds in this group (Bylemans and Meurrens, 1997). This illustrates the importance of anti-resistance strategies, involving restricted acaricide use and rotation of acaricides from different chemical groups, such as that proposed for fruit crops by the Insecticide Resistance Action Committee (IRAC) (Wege and Leonard, 1994).

Increased resistance to acaricides has led to research into alternative sources for control, such as fatty acid derivatives (Silva-Flores et al., 2005), sugar esters (Puterka et al., 2003), plant extracts, including essential oils (e.g. Kawka and Tomczyk, 2002; Mateeva et al., 2003; Aslan et al., 2004, 2005; Hou et al., 2004; Kawka, 2004), such as Elettaria cardamomum (Fatemikia et al., 2014), and botanical insecticides derived from the neem tree (Azadirachta indica) (Pavela, 2003). Of various plant extracts tested for acaricidal activity against T. urticae in Plovdiv, Bulgaria, Mateeva et al. (2003) reported that thornapple (Datura stramonium), wormwood (Artemisia absinthium) and basil (Ocimum basilicum) were toxic to the active stages of this pest. It was stated that extracts of these species could be used to control T. urticae on rose in urban areas. Saber (2004) reported that ethanol extracts of sand wormwood (Artemisia monosperma) were least effective against females of T. urticae compared to petroleum ether, chloroform or ethyl acetate. The acaricidal activity of Australian Lamiaceae extracts has also been tested against T. urticae with varying results (Rasikari et al., 2005). Extracts from the subfamilies Ajugoideae, Scutellarioideae, Chloanthoideae, Viticoideae and Nepetoideae showed acaricidal activity, and 14 species of Plectranthus showed moderate to high contact toxicity against T. urticae. Methanol extracts of Cinnamomum species (family Lauraceae) are potential acaricides (Reddy et al., 2014).

Commercially available Bionatrol (specified emulsion nano-particle soyabean oil) was shown to reduce populations of T. urticae, aphids (Aphis gossypii) and whiteflies (Trialeurodes vaporariorum) on greenhouse-grown English cucumber (Cucumis subsp. kasa) by 88-95% (Lee et al., 2005).

Integrated Pest Management

Management of T. urticae forms an integral part of IPM programmes for many crops. It is important that pesticides used for other pests and diseases are chosen so that they cause minimal disruption to naturally occurring predators or biocontrol agents such as Phytoseiulus persimilis. Also, control agents applied against the same pest must also be chosen carefully so that they do not disrupt each other. Thus, even though P. persimilis and B. bassiana have been shown to be effective in controlling T. urticae, when applied together, an increase in handling time by P. persimilis was reported, leading to a decrease in the rate of feeding by the predatory mite (Seiedy et al., 2012).

It may sometimes be necessary to use a selective acaricide to reduce spider mite numbers and maintain a suitable pest/predator ratio. For example, a selective acaricide may be needed to reduce a large overwintered population of T. urticae in the spring, before a release of P. persimilis later in the year (Easterbrook, 1992).

IPM programmes should minimize the use of acaricides, to delay the onset of resistance and prolong their effective life, but even programmes that do not heavily rely on pesticide use need to be cautious when employing different control strategies. For example, hot-water treatment on strawberry discs has been shown to control T. urticae (Gotoh et al., 2013); however, it was suggested by the authors that the natural enemy, Neoseiulus californicus would have to be replaced following treatment due to its sensitivity to hot water.

Supplements, such as fertilizers, used in the growing environment must also work synergistically in an IPM programme and several authors have investigated the effect of fertilizer application on pests, such as T. urticae. For example, Zhang and Xiang (2007) reported an increase in the number of T. urticae (and Aphis gossypii) with an increase in organic fertilizer application; however, cucumber yield also increased. In contrast, other studies have shown that application of nitrogen or phosphorous fertilizers had no effect on numbers or activity of T. urticae (e.g. Shabalta et al., 1992, on soyabeans).