A Review of Crop Protection Methods against the Twospotted Spider Mite— Tetranychus urticae Koch (Acari: Tetranychidae)—With Special Reference to Alternative Methods

: Tetranychus urticae is one of the most important pests of many species of economically important crops, cultivated both under cover and in open ground. Feeding T. urticae reduces the size and quality of the yield. Nowadays, in connection with the popularization of organic farming and the green order policy, non-chemical methods that provide an effective reduction in the harmfulness of this spider mite are sought. The aim of the study is to present the current state of knowledge on methods of reducing the undesirable effects of T. urticae feeding. The paper discusses the main directions of searching for biopesticides against T. urticae and provides a list of natural components on which commercially available products are based. The aspect of using the natural properties of plants, micro-and macro-organisms is presented. The paper also deals with the issue of the spread of spider mites in connection with the observed climate changes.


Introduction
The twospotted spider mite-Tetranychus urticae Koch, 1836-is a member of the family Tetranychidae, which includes about 4000 species [1,2].It has been found in all climate zones in Europe, Asia, and North and South America [3][4][5].T. urticae was originally described based on European specimens.It is regarded as a native species of the temperate climate zone but is also found in subtropical regions.It occurs throughout the United States in greenhouses, where it winters outside its natural range of distribution.Tuttle and Baker [6] reported that this species colonizes deciduous fruit trees in the northern regions of the US and Europe.The host range of T. urticae covers about 1275 plant species from 70 genera representing several dozen botanical families [7], either wild or cultivated, including vegetables, ornamental plants, crops, fruit trees and shrubs [2].
The control of T. urticae relies mainly on the use of synthetic acaricides, which is not always effective as this species has a high ability to develop resistant populations [2,8,9], and many acaricides have a non-selective effect on predatory mites [10].The misuse of chemical products for the control of spider mites can cause contamination of the natural environment and food, especially fruit and vegetables meant to be consumed when freshly harvested [11,12].Acaricides belong to several main groups of chemical compounds: organophosphates, pyrethroids, carbazinates, quinolines, carbamates, tetrazines, diphenyl oxazolines, quinazolines, phenoxypyrazoles, thiazolidines, macrocyclic lactones, pyridazones, and pyrazole derivatives [13][14][15].Recently, many studies have been carried out on replacing synthetic acaricides with new, safer agents, due to the risk of developing tolerance, toxicity and harmfulness to the natural environment associated with their overuse [16][17][18][19][20][21].
This review presents examples of currently used methods to control mites, including chemical and other measures.We aimed to present promising studies by various authors on the use of natural substances, biological strategies relying on bacterial and fungal microorganisms, as well as macro-organisms, including predatory mites and insects.

Life Cycle
T. urticae feeds mainly on the underside of the leaf [22].After colonizing a new site, spider mites produce a silk web, which protects them against the negative effects of abiotic and biotic environmental factors and indicates the presence of the pest [23,24].The silk web is also used by T. urticae for migration and is the carrier of a pheromone substrate [25][26][27].Some plant species have leaves structures called leaf domatia, which are very eagerly colonized due to the microclimate promoting the development of spider mites [28].
Apart from the occurrence of webs, the presence of spider mites is evidenced by chlorotic discolouration on the leaves caused by feeding.Physical damage to leaf tissues disturbs the structure of the photosynthetic apparatus and photosynthesis, carbon dioxide assimilation, sugar metabolism and transpiration of the colonized leaves [29][30][31][32][33]. Significantly increased guaiacol peroxidase (GPX) activity and low level of catalase (CAT) activity were measured in Ocimun basilicum L. 'Purpurascens' (Lamiaceae) leaves infested by mites [34].It is a species characterised by haplodiploid arrhenotoky, in which males develop from unfertilized eggs and are haploid, whereas females develop from fertilized eggs and are diploid [35].The life cycle consists of the egg, larvae, quiescent larva (protochrysalis), protonymph, quiescent protonymph (deutochrysalis), deutonymph, quiescent deutonymph (teleiochrysalis), and sexually mature individuals: males and females.Males guard quiescent deutonymph females before they reach maturity, or juvenile females, and then fertilize them [35].Regev and Cone [36][37][38] identified farnesol, nerolidol, geraniol, and citronellol as the components of sex pheromones in quiescent deutonymph females.Females mate only once, while males mate multiple times [39], preferring unrelated females [40].The length of the life cycle and the development of the population depends on the temperature, the type of host plant on which it develops, and plant health [41,42].The dynamics of its population also depend on the light intensity at the site of plant growth.Exposure to light intensity from 50 to 450 µmol m −2 •s −1 increases its fertility and decreases its mortality [43].Under optimal conditions, their life cycle is shorter than 10 days, and one female can deposit more than 100 eggs [44,45].During the growing season of the host plant, the population of T. urticae may increase by many times.Its growth population, apart from environmental conditions, is also influenced by the type of social interactions between females and males, modifying female fertility [46].
T. urticae only moves relatively short distances on its own.It mainly migrates by wind-drift dispersal [47].When food availability is low, silk balls, i.e., aggregates formed mainly by sexually immature females, can be observed on apical parts of plants.Silk balls are dispersed to new sites where females establish new colonies [48,49].Females can go into the state of diapause.During this period, they do not feed or deposit eggs.Differences with respect to diapause have been observed between populations from different geographic regions [50,51].Diapausing females are more tolerant to lower temperatures [52].They are characterized by a different metabolism of amino acids, sugars and proteins compared to summer females [53,54] and a different expression of genes determining digestion and detoxification, cryoprotection, carotenoid synthesis and the organization of the cytoskeleton [55].A difference in the termination of the diapause in females collected at different times of winter has been observed [56].Diapause in T. urticae females is associated with the reorganization of their metabolism and physiology in short-day regions, low ambient temperatures and limited food availability.Diapause in females is a strategy enabling survival in these unfavourable conditions.

Harmfulness
About 10% host plants infested by T. urticae are crops [57], including economically important crops in different regions of the world [58][59][60][61].The intensive feeding of mites combined with a rapid increase in population size have a negative effect on the physiology of the whole plant, as well as the yield size and quality [58,62].Muluken et al. [63] observed the complete destruction of potato plants in fields.Nyoike and Liburd [64] reported 50 to 80% loss in strawberry yield, while Jayasinghe and Mallik [65] reported up to 50% loss in tomato yield.This high loss in yield has been explained by pest invasion in the early stages of plant development, which was observed in Cucumis sativus L. (Cucurcitaceae) [66], cotton [67], tomato [65], and potato [68].Spider mites are also harmful to sugar beet Beta vulgaris L. (Chenopodiaceae) grown in Poland [69].For several years, large populations of this pest have been observed in plantations in central Poland, especially in Wielkopolskie, Kujawsko-Pomorskie, Łódzkie, Lubelskie, and parts of Mazowieckie provinces.It is a region with a large acreage of sugar beet crops, as well as agrometeorological conditions favourable for the development of the pest during the growing season (dry springs, high summer temperatures 25-30 • C and low precipitation 0−200 mm) [70].
Symptoms of damage caused by mites are initially observed on field margins, and with time they appear in patches all over the field.T. urticae causes premature yellowing and drying of the leaves.The feeding of mites that suck out the parenchymal tissue is visible on both sides of the leaf of sugar beet plants.As a result of intense pest feeding, small, bright spots in a mosaic pattern develop on the upper side of the leaf.The underside of the leaves is covered by a silk web with different developmental stages of the spider mite.The symptoms of early pest feeding are very often underestimated and mistaken for symptoms caused by viruses, nematodes or drought.The increase in twospotted spider mite population and further feeding cause leaf malformation and a web occurs on the plant apex.Plants wilt, turn brown and eventually die back.In the climate of Poland, T. urticae might produce from 4 to 6 generations during one growing season.When temperatures are favourable (25-30 • C), which often happens in late spring and summer, a single generation might develop in just 8 days [69].The decrease in the root yield caused by intensive feeding of twospotted mite on sugar beet may be from 20 to 50%, and the sugar content in the roots may be reduced by up to 2% [69,71,72].

Available Methods for the Control of T. urticae 2.1. Chemical Control of T. urticae
Currently, the most popular method for the control of spider mites relies on the use of synthetic acaricides.Treatments should be performed based on systematic monitoring.According to regulations on integrated pest management, plants should be sprayed when threshold values of economic injury are exceeded and when the pest population cannot be reduced by growing arachnid-tolerant plants or using biological methods.If several treatments are necessary, they should be performed with products from different chemical groups, representing different modes of action.Phytophagous mites from the Tetranychidae family are a very specific group of crop pests.Their presence on crops often goes unnoticed until the damage caused by feeding causes significant economic losses.In practice, acaricides should be used when a greater number of mites is observed, and a silk web occurs on different plant organs.Moreover, these pests may produce up to several generations during the growing season and very quickly develop resistance to the active ingredients contained in synthetic acaricides.Table 1 presents selected products for the control of spider mites from among 14 chemical groups (15 active substances) available on the world market of plant protection chemicals.The presented acaricides are diverse in their mechanism of action.They affect the nervous system-neurotoxins (5)-inhibit the growth of mites or disturb their development (8), and inhibit lipid metabolism (2).Many years of observations on the chemical control of spider mites revealed the presence of pest resistance.For example, since the 1970s, T. urticae has dominated in cotton grown in Australia, where resistance to acaricides used at that time was very quickly noted.Tolerance of T. urticae was also observed in cotton and bean plantations treated with insecticidal organophosphates [80].
The resistance of T. urticae to pyridaben, a substance from the pyridazinone class, was also investigated [16,17,81,82].Pyridaben is a mitochondrial electron transport complex I inhibitor.The H110R mutation in the PSST subunit has been reported as a major factor in pyridaben resistance in the two-spotted spider mite, T. urticae.However, backcross experiments revealed that the mutant PSST alone conferred only moderate resistance.In contrast, inhibition of cytochrome P450 (CYP) significantly reduces resistance levels in many highly resistant strains.It was reported previously that maternal factors contributed to the inheritance of pyridaben resistance in the egg stage, but the underlying mechanisms have not been explained.Itoh et al. [82] studied the combined effects of the PSST H110R mutation and candidate CYPs, as resistance factors on pyridaben resistance in T. urticae.Their study (2021) revealed that the maternal effects of inheritance of resistance in the egg stage were associated with CYP activity.Analysis of differential gene expression by RNA-seq identified CYP392A3 as a candidate causal factor for the high resistance level.The researchers concluded that the high pyridaben resistance levels are due to a synergistic or cumulative effect of the combination of mutant PSST and associated CYPs, including CYP392A3, but other yet to be discovered factors might also be involved [82].
Currently, T. urticae is defined as the major crop that is pest-resistant to most of the selective acaricides approved for its control, i.e., organophosphates, abamectin, clofentezine, hexythiazox, bifenthrin and chlorphenapil [16,17,83].The control of spider mites is very difficult because, due to the emergence of several generations per year, the rapid development of resistance to chemical products has been observed in this species.In the practice of plant protection, various biological agents are increasingly used, including acarophages, biotechnological agents, or other methods based on natural substances [19,84,85].

Available Methods for the Control of T. urticae
Due to the policy aiming to reduce the use of synthetic pesticides, the purpose of which is to protect the natural environment and its biodiversity, researchers are looking for new, effective methods to limit the harmfulness of T. urticae.In this area of interest, studies are carried out on the development of biopesticides based on natural substances and the bionomy of host plants, on the effects of microorganisms, their metabolites, and beneficial organisms.
Secondary plant metabolites have been investigated in many experimental studies aimed at identifying effective and safe agents protecting against spider mites.Plant extracts may have a potential for the control of mites due to the content of secondary metabolites, such as terpenoids, alkaloids, flavonoids and polyacetylenes [120,121].Moreover, plant extracts often contain mixtures of active substances which may delay or prevent the development of resistance [122].In addition, when selecting potential pesticidal plant extracts, several properties need to be considered, including the efficiency of their low concentrations in mite control, and non-toxicity to other animals, so that they can be used safely in sustainable agriculture [123].Extracts obtained from aboveground and underground parts of plants have a lethal effect on spider mites, change the conductivity in the nervous system by influencing sodium channel transport [124], and have a deterrent/repellent effect and inhibit the egg-laying process [125][126][127][128][129][130][131][132].
So far, studies on the efficiency of T. urticae control have been carried out for more than 100 plant species from different botanical families, among which the largest number of plants studied represented Asteracae [133,134].Yanar et al. [135] reported that the foliar application of alcoholic leaf extract from X. strumarium L. (Asteraceae) and Anthemis vulgaris L. (Asteraceae) caused 79.85 ± 0.83 and 76.63 ± 2.08% mortality in female two-spotted mites, respectively.Among natural pesticides, French marigold Tagetes patula Linn.(Asteracae) is considered an excellent species because it produces thiophenes and many polyacetylene compounds with a strong biocidal effect [136].Antibacterial, antifungal, insecticidal and nematocidal activities of this plant species have been demonstrated in many studies [137][138][139][140][141][142][143], in addition to the effective control of ticks [87].An experiment carried out by Ismail et al. [72] revealed that the marigold extract had toxic, ovicidal and repellent effects on T. urticae, and caused a 30−50% reduction in the number of deposited eggs.The deterrent and toxic properties of Abrus precatorius (Fabaceae) seed extracts were reported by Amer et al. [144].The essential oils obtained from Tanacetum vulgare L. (Asteraceae) and Artemisia absinthium L. (Asteraceae) strongly increased the mortality of T. urticae [145].Extracts from Matricaria recutita L. (Asteraceae), Achillea millefolium L. (Asteraceae), Taraxacum officinale L. (Asteraceae), and Salvia officinalis L. (Lamiaceae) strongly decreased the fertility, viability and feeding intensity of T. urticae [146,147].Surface deposits on Taxus baccata L. (Taxaceae) needles removed by dipping in water had a detrimental effect on the total fecundity and oviposition period of T. urticae [148].Many experimental studies have demonstrated that fragrances of phylogenetically distant plants are most effective in repelling certain pests on host plants [17,20,[95][96][97].When selecting potentially pesticidal plant extracts, several properties should be considered, including the efficiency of low concentrations in controlling mites, and lack of toxicity to other animals, ensuring safe use in sustainable agriculture [17].One aspect of introducing and using plant extracts is their persistence and efficiency.The persistence and efficiency of a biopesticide can be improved by using new formulations, e.g., chitosan nanocapsules loaded with oil extracted from A. millefolium.In a study by Ahmadi et al. [149], this procedure significantly prolonged the acaricidal effect of the oil by controlling its release depending on the pH of the environment.

Micro-and Macro-Organisms for the Control of T. urticae Bacteria
The use of bacteria for the control of T. urticae is one of the research areas to develop an effective method for the control of the two-spotted spider mite.Many studies have demonstrated that Pseudomonas aeruginosa (Schroeter) caused a 100% mortality of adult females T. urticae after 72 h at a concentration of 10 7 cfu mL −1 by spraying application.Treatment with Bacillus subtilis (Ehrenberg) resulted in approximately 80% mortality, and Lysinibacillus spaericus (Meyer and Neide) slightly more than 95% [156].Golec et al. [157] reported that products based on Chromobacterium subtsugae Martin et al., strain PRAA4-1 (Grandevo DF2) and heat-killed Burkholderia spp.92 strain A396 (91 Venerate EP) limited the growth of a T. urtice population after a single treatment during a single pest generation.Grandevo DF2 caused 50% mortality in nymphs and reduced the fertility of females that survived the application of this product.Treatments with Streptomyces avermitilis (Burg et al.) and B. thuringiensis Berliner 1915 caused 90-100% mortality in females and 91-99% mortality in nymphs, respectively [158].The pathogenicity of the bacteria is based on adhesion, which can increase the penetration of proteases, chitinase, lipase and hydrolase across the epidermis and natural openings in the T. urticae body, leading to the rapid death of the pest.In addition, the deterrent effect of Pseudomonas strains could be explained by the production of secondary metabolites, including volatiles, which prevent T. urticae colonizing leaves [159].
One method to reduce the harmfulness of T. urticae relies on the use of fungal fermentation products: milabamectin and abamectin.These compounds are produced by soil fungi from the actinomycetes group: Streptomyces hygroscopicus subsp.aureolacrimosus (Jensen) and Streptomyces avermitilis (ex Burg).Abamectin is commercially available in products for the control of T. urticae in a wide range of vegetables, fruit shrubs and ornamental plants (Table 1).In recent years, resistance to this substance has been observed among T. urticae populations in many regions of the world [75,[163][164][165][166].Among European populations, resistance to milabamectin and cross-resistance to both substances was observed [167].
One vital aspect of using bacteria and fungi to control T. urticae is their potential impact on beneficial predatory mites.Studies have demonstrated a significant role of timing when using microbial products.Despite their high efficiency, Bacillus thuringiensis Berliner and Streptomyces avermitilis (ex Burg), as well as fungus Lecanicillium lecanii had a negative effect on Phytoseiulus persimilis Athias-Henriot when products were applied on the same day.The release of predatory mites one day after treatment of plants with L. lecanii and 7 days after treatment of plants with B. thuringiensis or S. avermitilis had no negative effect on the survival of the introduced predators.These findings confirm the potential suitability of entomopathogenic fungi and bacteria in combination with predatory mites in T. urticae biocontrol [158].

Insects
A study investigating the effects of naturally occurring insects in an organic strawberry crop demonstrated that Anthocoris nemorum (Linnaeus) may play a role in reducing T. urticae populations.Molecular analysis of the intestinal contents of these insects revealed the presence of T. urticae DNA [169].The larval forms of the predatory thrips Scolothrips longicornis Priesner eat the eggs of T. urticae.Consumption increases as the temperature rises to 30 • C, and decreases at higher temperatures.T. urticae eggs are also consumed by female thrips most intensively before oviposition [170,171].Laboratory studies revealed that a minute anthocorid, Orius albidipennis (Reuter), eats on average 7 females of T. urticae [172].Investigation shown that ants have limiting effect on twospotted spider mite.In study under glasshouse conditions Miyagi et al. [173] and Osborne et al. [174] demonstrated that Tapinoma melanocephalum (Fabricius) is a significant predator of T. urticae.
The above-mentioned groups of micro-and macro-organisms have been used to develop commercially available biocontrol products.Products based on the activity of micro-and macro-organisms are presented in Table 3.

Table 3.
Micro-and macro-organisms used in plant protection products for treatment T. urticae worldwide.

The Effect of Climate Change and the Expansion and Development of Spider Mites in the Future
The climate change observed for several decades will certainly affect the role of spider mites as crop pests.According to the current climate change scenario, T. urticae shortens its life cycle in dry and hot conditions, produces more generations per year, and broadens its host range [175].Climate change models predict that the frequency, intensity and duration of heat waves will increase over the next two decades.Warming may promote the spread of not only T. urticae in the regions where the species is present, but also create conditions for the development of spider mites that so far are normally found in areas of warmer climate, e.g., the tropical species Tetranychus evansi Baker & Pritchard, 1960 [176,177].Unfavourable winter temperatures do not rule out the possibility of this pest's survival on crops under cover.Currently, T. evansi has the status of an invasive species.Heat waves might have a profound impact on the efficiency of biological agents for the control of the spider mite [178].High temperatures might influence the biology of the biocontrol agent, ranging from postponing oviposition to manipulating offspring quantity via egg number and quality via egg size.Such species-specific responses of biocontrol agents to heat stress may also affect their success in controlling spider mites.
Apart from the temperature, wind plays an important role in the dispersal of spider mites.Findings by Narimanov et al. [179] confirmed that strong electrical fields in the air elicit pre-dispersal behaviour, and in combination with a light wind facilitate the dispersal of mobile forms and propagation of spiders to other areas where crops are grown.In their experimental study, the researchers emphasized that the employed strong electrical fields played a rather supplementary role in spiders' dispersal, with wind remaining the most influential factor.
Current climate change is expected to improve the occurrence and spread of T. urticae in many cultivated plant species.Currently, the role of modern plant protection is to provide effective methods to control pests and to deliver solutions that minimize negative effects on the natural environment.Biological control methods are in line with the European Green Deal strategy, and they rely on the use of microorganisms, including entomopathogenic fungi, predators, or natural plant extracts and secondary metabolites, which create a natural barrier to the increased pressure of twospotted spider mites.Biological control treatments as an alternative to new chemicals used to control mites depend on a number of biotic and abiotic factors.Detailed ecological studies are required to investigate the interactions between the environment and its individual components, and to explain the bionomy of spider mites.

Table 1 .
Synthetic acaricides that have been used for controlling T. urticae worldwide.

Table 2 .
Plant protection products formulated on natural extracts from plants used for treatment T. urticae worldwide.