Biological Control 68 (2014) 73–91

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Biological Control

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Tea: Biological control of and mite pests in China ⇑ Gong-Yin Ye a, , Qiang Xiao b, Mao Chen c, Xue-xin Chen a, Zhi-jun Yuan b, David W. Stanley d, Cui Hu a a Key Laboratory of Agricultural Entomology of Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China b Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou 310008, China c Department of Entomology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456, USA d USDA/Agricultural Research Service, Biological Control of Research Laboratory, 1503 S. Providence Road, Columbia, MO 65203, USA highlights graphical abstract

 More than 1100 species of natural enemies recorded in China have been summarized.  Biological characteristics of some dominant natural enemies have been well reviewed.  Various biocontrol measures combined with other IPM approaches have been reviewed.  The future researches and policy implementation of tea pests are suggested. article info abstract

Article history: Tea is one of the most economically important crops in China. To secure its production and quality, bio- Available online 3 July 2013 logical control measures within the context of integrated management (IPM) has been widely pop- ularized in China. IMP programs also provide better control of pests on tea with less chemical Keywords: insecticide usage and minimal impact on the environment. More than 1100 species of natural enemies Tea ecosystem including about 80 species of viruses, 40 species of fungi, 240 species of and 600 species of Biological control predators, as well as several species of bacteria have been recorded in tea ecosystems in China. Biological Natural enemies and ecological characteristics of some dominant natural enemies have been well documented. Several viral, bacterial, and fungal insecticides have been commercially utilized at large scale in China. Progress in biological control methods in conjunction with other pest control approaches for tea insect pest man- agement is reviewed in this article. Knowledge gaps and future directions for tea pest management are also discussed. Ó 2013 Elsevier Inc. All rights reserved.

1. Introduction cultivation doubled from 1.37 million ha to over 3.01 million ha in the nearly 50 years from 1961 to 2009. In that time, total tea Tea, (L.) Kuntze, is the most popular and lowest production increased fourfold from 0.98 to 3.95 million metric cost beverage in the world, second only to water. It would be very tons. China, where tea has been used as a beverage and a medicine difficult to overestimate the economic impact of tea at the global or since at least 2700 BCE, is the origin of tea and the largest tea pro- Chinese national level. Tea is a globally important monoculture ducing country. China produces non-fermented tea (Green tea), crop cultivated in large- and small-scale plantations between lati- semi-fermented tea (Oolong tea) and various fermented teas (Black tudes 41° N and 16° S including 46 countries across Asia, Africa, La- teas). tin America, and Oceania (Hazzrika et al., 2009). Global tea Gobal cultivation of tea has rapidly grown in the last 50 years. In the China of 1950 tea was grown on 169,400 ha with annual yield of 62,200 metric tons. By 2010 Chinese tea production increased to al- ⇑ Corresponding author. Fax: +86 571 8795124. most two million ha with an annual yield of about 1.5 million metric E-mail address: [email protected] (G.-Y. Ye).

1049-9644/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.biocontrol.2013.06.013 74 G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 tons (a 24-fold increase) in 2010 (ITC, 2011). As an emerging trend, Various pest control techniques have been practiced in China, organic tea (formally defined based on cultivation practices and including mechanical, cultural, biological and chemical control. Be- independently certified by third-party certifiers) has been growing tween the 1950s and 1980s, chemical pesticides were commonly since the end of 1980s. The planted area and yield increased to applied. Overuse of pesticides, however, led to resurgence of pri- 30,000 ha and about 25,000 metric tons by 2009 (CTIYC, 2011). mary pests, secondary pest outbreaks, and environmental pollu- Tea is produced in vast areas of China with north–south distribution tion, including undesirable residues on brewed tea. Integrated between 37° N and 18° S and east–west distribution between 122° E pest management (IPM) has been popularized to ameliorate the and 97° W, totaling more than 20 provinces across tropical, subtrop- environmental pollution and health-hazard issues associated with ical and temperate regions. overuse of synthetic pesticides. The key techniques include There are four major tea-growing regions in China. One is the improving the influence of natural enemies on pest populations Jiangnan region: it lies the south of the middle and lower reaches via vegetation management (conservation biological control) and of the Changjiang (Yangtze) River, and is the most prolific of China’s releasing biological control agents (classical and/or augmentation tea-growing areas. Most of its output is the green variety, with biological control), utilizing cultural control and rationally apply- some black tea. Another is the Jiangbei region, a large area north ing safer chemical insecticides with low toxicity and low residues of the Yangtze, where the average temperature is 2–3 °C lower than (Chen and Chen, 1999). Biological control measures are widely ac- in the Jiangnan region. Green tea is the principal variety, along with cepted in China to produce safer (contaminant-free) or organic tea. compressed tea for the minority areas in the northwest. The south- The broad use of biological control is the positive outcome of west region embraces Sichuan, Yunnan, Guizhou and Tibet, produc- three decades of extensive investigations. These include surveying ing black, green and compressed teas such as Pu’er tea. The Lingnan, and identifying local natural enemies (including pathogens, para- also known as the south China, region covers all southern provinces sitoids and predators) in tea ecosystems, understanding the biol- of China, namely, Guangdong, Guangxi, Hainan, Fujian and Taiwan. ogy and ecological importance of natural enemies, and The Lingnam region produces mainly Oolong tea. developing strategies on rearing and releasing natural enemies in Given the very large areas of tea monocultures, a large number tea plantations. In this paper, we review advances on biological of tea pests is not surprising. Globally, 1034 arthropod species are control of tea pests and discuss future research needs. associated with tea, of which about 3% are common pests through- out the world (Chen and Chen, 1989). In China, 808 species of in- 2. Survey and classification of natural enemies sect and mite pests, belonging to 109 families from 13 orders of 2 classes were recorded in tea, of which only 6 species damage Natural enemy diversity in tea ecosystems plays a prominent tea products during storage (Zhang and Han, 1999). Among the role in biological control of tea pests. Since the 1960s, many inves- 808 pest species, most are hemipterans and lepidopterans (Table 1). tigators surveyed and identified natural enemies throughout the There are about 700 shoot and leaf feeders, 50 stem and root feed- tea producing regions of China (Xia, 1965; Tsai et al., 1978; Hu ers, and less than 10 flower and fruit feeders (Zhang and Han, et al., 1979). To date, more than 1100 species of natural enemies 1999). Aside from the common pest species, regionally specific (including vertebrate predators such as birds) of tea pests have pests require special attention (Supplemental Table 1)(Zhang been recorded (Zhang and Tan, 2004). and Han, 1999; Zhang and Tan, 2004). Among these pests, only six insect species and two mite species are serious pests (Supple- mental Table 1). This small number of pest species often account 2.1. Entomopathogens for 10–20% yield loss and in some catastrophic cases, even total crop losses (Chen and Chen, 1999). Entomopathogens include viruses, bacteria and fungi. These microbes cause epizootics in natural pest populations and carry

Table 1 List of pest, and predator orders and their family and species number in tea gardens recorded in China.

Class/order Family number Species number Species proportion (%) Pests Parasitoids Predators Pests Parasitoids Predators Pests Parasitoids Predators Insecta Collembola 1 – – 1 – – 0.12 – – Odonata – – 6 – – 24 – – 3.31 Blattodea 2 – – 3 – – 0.37 – – Isoptera 2 – – 9 – – 1.11 – – Orthoptera 5 – 2 48 – 11 5.94 – 1.52 Mantodea – – 1 – – 9 – – 1.24 Dermaptera – – 3 – – 10 – – 1.38 Embiodea 1 – – 1 – – 0.12 – – Corrodentia 2 – – 4 – – 0.50 – – Thysanoptera 2 – 1 22 – 1 2.72 – 0.14 Hemipteraa 38 – 8 284 – 66 35.15 – 9.09 Neuroptera – – 7 – – 26 – – 3.58 Coleoptera 14 – 7 135 – 176 16.71 – 24.24 Strepsiptera – 1 – – 1 – – 0.37 – Diptera 4 1 4 7 29 38 0.87 10.70 5.23 29 – – 273 – – 33.79 – – 4 24 6 4 241 29 0.50 88.93 3.99 Arachnida Acarina 5 – 7 17 – 41 2.10 – 5.65 Araneida – – 26 – – 295 – – 40.63 Total 109 26 78 808 271 726 100 100 100

a Here, Hemipteran pests include 219 species of 28 families belonging to the previous Homptera and 65 species of 10 families belonging to the previous Hemiperar. G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 75 maximum regulatory power. They have been explored as potential species (Xia, 1965). Investigations of parasitic insects in tea planta- biocontrol agents since the end of the 1970s. To date, about 80 spe- tions focused on the ecosystem level to identify key insect pests cies of viruses, more than fungal 40 species and several bacterial and their natural enemies (Hu et al., 1979, 1993a; Zhang, 1989a; species have been reported. Additionally, a microsporidium (Nose- Liu and Xu, 1990; Song et al., 1992, 1996; Chen et al., 1999; Huang ma sp.) was isolated from the tung oil tree geometrid, Buzura sup- et al., 1999, 2000; Xiao et al., 1992a, 1999; Ai et al., 2000a,b; Wang pressaria Guenee (Ding et al., 1994), and an unidentified nematode et al., 2001a,b; Han and Dai, 2009; Wang et al., 2010a; Mei et al., species belonging to Mermithidae was found in larvae of 2011). To date, 241 species of parasitic belonging to 24 fam- obliqua Prout (Hu et al., 1979). ilies of Hymenoptera, and 29 species of parasitic tachinid flies have been identified as primary parasitoids associated with tea insect 2.1.1. Viruses pests (Table 1)(Zhang and Tan, 2004). Among these parasitic The exploration of insect virus associated with tea insect pests wasps, species of Ichneumonidae, Braconidae, Aphelinidae, Ency- has received more attention since the end of the 1970s. Insect-spe- rtidae, Chalcididae and Eulophidae ranked as the top five groups, cific viruses can be highly effective natural controls of caterpillar accounting for 27%, 19%, 14%, 7%, 3% and 3% of the total, respec- pests and they are promising candidate biocontrol agents (Tsai tively (Supplemental Fig. 1A), and parasitoid species of several et al., 1978). To date, 82 species of viruses associated with tea in- key tea insect pests are summarized in Supplemental Table 4.In sects have been discovered, and listed by virus type in Supplemen- addition, several species of hyperparasitioids were also discovered tal Table 2 (Zheng et al., 1985; Hong, 1998; Zhang and Tan, 2004). (Hu et al., 1993a; Song et al., 1996; Xiao et al., 1999). Beyond these, an E. obliqua picorna-like virus was isolated from Among 29 species of parasitic flies (Shi, 1982; Hu et al., 1979; larval geometrid cadavers, and characterized at the molecular level Zhang, 1989a; Chen et al., 1993; Xiao et al., 1999; Wang et al., (Wang et al., 2004). 2001a; Zhang and Tan, 2004; Wang et al., 2010a), most were par- asitoids of lepidopteran tea pests. Eight species attack larval or pu- 2.1.2. Bacteria pal stages of a single pest species, E. pseudoconspersa Strand (Chen Almost all entomopathogenic bacteria isolated from tea insect et al., 1999). Drino inconspicua Meign was the only species parasit- cadavers or tea ecosystems are Bacillus thuringiensis Berliner (Bt). izing larvae of E. obliqua Prout (Hu et al., 1979). Five species, Bel- Wu and Tang (1981) identified a strain from larval cadavers of B. pharipa tibialis (Chao), Chaetexorista atripalpis Shima, Carcelia supressaria Guenee which was subsequently named B. thuringiensis rasella Baranov, C. transbaicalica Richter, Exorista rossica Mesnil, var. finitimus strain CW-1. Three Bt strains (strain 111, 119 and were recorded in Guizhou province (Wang et al., 2010a). A few spe- 109) were isolated from lepidopteran pest cadavers, of which cies of Strepsiptera were found. Hong (1989) recorded Halictopha- strain 111 and 119 caused up to 74% mortality of Euproctis pseudo- gus bipunctatus Yang as a parasitoid of E. vitis Göthe. conspersa strand larvae (Tan and Lu, 1985). Recently, 54 Bt strains were isolated from the pyhlloplane of 25 plant species in China. 2.3. Predators Among these, 10 strains were effective against E. obliqua Prout (Zhang et al., 2005). Serratia marcescens Bizic is pathogenic against In tea ecosystems, predators of tea insect and mite pests include two species of scales, Paralepidosaphes tubulorum (Ferris) and and entomophagous vertebrates (bats, birds, amphibi- Chrysomphalus ficus L. (Wang et al., 2010a). ans, reptiles and rodents) (Zhang 1986; Dai, 1995a,b; Jiang et al., 2008; Tang et al., 2008). More than 600 species of predatory 2.1.3. Fungi arthropods, 42 bird species, six amphibian species, two reptile spe- Entomopathogenic fungi can act as parasites of insects and cies, three rodent species and one bat species were summarized by either kill or seriously disable them. They are widespread in tea Zhang and Tan (2004). Among 54 species including 24 bird species, ecosystems and, under some environmental conditions, can pro- 9 amphibian species, 11 reptile species and 10 mammalian species, duce extensive epizootics in pest populations. The survey, isolation 11 species were evaluated as prominent pest predators in Anhui and identification of entomopathogenic fungi associated with tea province, as showed in Supplemental Table 5 (Tang et al., 2008). insects have received considerable attention since the end of the 1970s (Liang, 1979). So far, about 40 species of entomopathogenic fungi have been documented (Liang, 1981a,b; Li et al., 1989; Ye and 2.3.1. Predatory insects Wang, 1990; Chen et al., 1990a, 1994; Han, 2000; Han and Li, 2001; Surveys show that predatory insects include coccinalids, cara- Tang et al., 2003; Zhang and Tan, 2004; Qin et al., 2008; Wang bids, chrysopids, syrphids and hemipterans (Zhang and Peng, et al., 2010b)(Supplemental Table 3). These fungi belong to four 1984; Xiao et al., 1992b,c, 1999; Dai, 1995a, 1996a; Han et al., Phyla, Zygomycotina, Ascomycotina, Basidiomycotina and Deu- 1996; Chen et al., 1999; Wang et al., 2001a, 2010a; Dai et al., teromycotina. Within these recorded fungi, Aegerita webberi Fawc- 2010, 2011; Mei et al., 2011). For example, 84 species of coccinelids ett, Beauveria bassiana (Balsamo) Vuillemi, and Paecilomyces from tea plantations in Guizhou province were identified as preda- fumosorosens (Wize) have most promise as biological control tors of aphids, scales and mites (Dai, 1996a; Wang et al., 2010a). agents of tea pests (Tang, 2001; Feng et al., 2004a,b). For example, Within these species, seven species of Scymninae that attack tea epizootics in the 1990s due to A. webberi Fawcett, usually resulted mites are listed in Table 2. Six and 11 species of syrphids were re- in more than 90% mortality of tea black spiny whitefly (A. spiniferus ported by Dai (1995a) and Wang et al. (2010a), respectively. Xiao Quaint.) population (Chen et al., 1994; Han and Li, 2001). Between et al. (1992b) reported 27 coccinellid species within seven subfam- 1988 and 1994, B. bassiana (Balsamo) Vuillemi naturally resulted ilies in Hunan province. Dai et al. (2010) recorded 41 species of 1.0–21.2% control of larval and pupal Myllocerinus auroliineatus predatory carabids in three Carabid subfamilies, along with their Voss (Wu et al., 1996). prey and distribution in eastern Guizou province. Similarly, 20 spe- cies in the subfamilies Caraninae and Harpalinae were registered in 2.2. Parasitoids tea gardens of Hunan province (Xiao et al., 1992c). A list of 390 species of predatory insect belonging to 45 families Surveys of parasitoids from tea insect pests started in the 1960s. within ten orders (Table 1), with their distributions and predatory For example, parasitoid species of tea scales and their natural par- targets (of some species) was consolidated by Zhang and Tan asitism rates were investigated between 1962 and 1964 in Meitan (2004). The number of predatory species for each family is showed (Guizhou Province). This work led to identification of 14 parasitoid in Supplemental Fig. 1B. Within all families, Coccinellidae, Carabi- 76 G.-Y. Ye et al. / Biological Control 68 (2014) 73–91

Table 2 She and Tao, 1996; Hu and Yu, 2000; Chen et al., 2004; Zhang Predatory insect species attacking mites as well as common spider and syrphid fly and Sun, 2004; Zeng et al., 2008; Dai and Han, 2009). Agricultural species occurred in Chinese tea gardens. practices also influence populations of beneficials. Han (2005) re- Groups Species Reference ported 14 species of eight families in tea systems treated with Mite specialists in Stethorus punctillum Dai (1996a), Wang 10–15 pesticide sprays, 16 species of eight families in plantations subfamily Scymninae Weise et al. (2010a) treated seven or eight spray times and 29 species of 12 families S. aptus Kapur found in an organic tea garden.Among 295 spider species belong- S. longisphonulus Pang ing to 26 families (Table 1), representatives of three families, Ara- S. cantonensis Pang S. siphonulus Kapur neidae, Salticidae and Theridiidae are dominant, accounting for S. chengi Sasaji 23%, 13% and 9% of the total (Zhang and Tan, 2004)(Supplemen- Scymnus babi Sasaji tal Fig. 1C). Common spider species Hylyphantes Chen et al. (2004) graminicolum 2.3.3. Predatory mites (Sundevall) Coleosoma Predatory mites, usually characterized by their orange-red col- octomaculatum (Böse. & ored, pear shaped bodies and long front legs are important control Str.) agents of pest mites in tea ecosystems. A few of species survey has Misumenops tricuspidatus been conducted (Table 3)(Liang, 1985a,b; Jiang et al., 1992; Zhao (Thomisidae) and Hou, 1993; Zhu et al., 2010), however, predatory mites in tea Clubiona reichlini Schenkel gardens need more study. In Guangdong province, Amblyseius eha- Oxyopes sertatus L. Koch rai Amitai et Swirski was the dominant species (Zhu et al., 2010). In Phintella bifurcilinea Anhui province, Zhao and Hou (1993) found that four species, (Böse. & Str.) including Anystis baccarum (L.), Amblyseius nicholsi Ehara, Amblyse- Common syrphid fly Betasyrphus serarius Zhang (1989b) ius sp., Allothrombinus sp., consume A. theae Watt. Among these species (Wiedemann) predators, A. baccarum (L.) was the dominant species, accounting Episyrphus balteatus (de Geer) for 28% of of the natural enemies of A. theae Watt. Zhang and Tan Syrphus corollae Fabricius (2004) listed 41 predatory mite species belonging to 7 families (Ta- Sphaerophoris menthastri ble 1) recorded in China and their distribution. Among these spe- L. cies, the phytoseiid mites were the largest group, accounting 60% Paragus guadifasciatus of the total (Supplemental Fig. 1D). Meigen

3. Biological and ecological studies on some key parasitoids and predators dae, Reduviidae, Syrphidae and Cicindelidae ranked the top five, The biological, ecological and, in some species, molecular char- constituting 22%, 16%, 9%, 6% and 3% of the total, respectively. acteristics of several NPVs and GVs isolated from important tea in- sect pests, including Ectropis obliqua NPV (Chen, 1989; Hu et al., 2.3.2. Spiders 1994; Ma et al., 2007), Buzura suppressaria NPV (Hu et al., 1995, Among predatory arthropods, spiders usually outnumbered 1999), Euproctis pesudoconspersa NPV (Leng et al., 2006; Tang the other groups, accounting for more than 65% of predatory et al., 2009), are well documented. Similarly, biological character- arthropods and as high as 98% in some regions. Spiders are istics of several fungal species isolated from the spiny black white- widely distributed Chinese tea ecosystems (Chen, 1992; Chen fly, A. spiniferus Quaint., have been also defined (Han and Li, 2001; and Zhao, 1993; Xu et al., 1995; Dai, 1996b, 1997, 1999; She Tang, 2001; Tang et al., 2003). Here we summarize biological and and Tao, 1996; Chen et al., 2010a, 2004; Hu and Yu, 2000; Zhang ecological studies of some key parasitoids and predators. and Sun, 2004; Zeng et al., 2008; Dai and Han, 2009; Wang et al., 2010a; Mei et al., 2011). Among these studies, Chen et al. (2000a) 3.1. Parasitoids reported 290 spider species representing 27 families were discov- ered during the years spanning 1983–1999. There are six com- 3.1.1. Braconids mon species occurred for each tea-grown region (Chen et al., Although 48 species of braconids reportedly attack tea pests 2004)(Table 2) although spider species varied over sampling (Supplemental Fig. 1A), little is known about their biology. Two times and locations, as shown in Table 3 (Chen and Zhao, 1993; species of Apanteles are the dominant larval parasitoids of the tea

Table 3 Spider and predatory mite species number recorded in tea gardens of several provinces in China.

Groups Province Family number Species number Reference Spiders Anhui 22 118 Chen and Zhao (1993) Zhejiang 14 116 Chen et al. (2004) Jiangxi 17 82 Hu and Yu (2000) Fujian 13 45 Zeng et al. (2008) Hunan 14 51 Zhang and Sun (2004) Yunan 14 114 She and Tao (1996) Guizhou 26 204 Dai and Han (2009) Predatory mites Hunan 1 17 Jiang et al. (1992)a Guangdong (three locations) 6 17 Liang (1985a,b) Guangdong (Yingde) 6 13 Zhu et al. (2010)

a Only one family, Phytoseiidae was surveyed. G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 77 geometrid, E. obiqua Prout (Hu et al., 1979, 1993a). One is Apanteles 3.1.2. Aphelinids sp. 1 with pale-yellow cocoons, and the other is Apanteles sp. 2, Thirty-five aphelined species attack tea scales, aphids or white- which produces white woolen cocoons. Apanteles sp. 1, is a mono- flies. As just seen for A. conspersae, however, studies on their bio- parasitoid, overwinters as prepupae within its cocoon on tea logical characteristics are quite limited with the exception of bushes, and pupates in March and early April. Adults emerge from surveys on their rate in tea gardens. Tian (1987) re- late March to early May. Apanteles sp. 1 is multivoltine, with about ported that Aphytis chrysomphali (Mercet), a parasitoid of Chrys- 11–12 generations per year in Zhejiang province, of which the par- omphalus ficus Ashmead, is multi-voltine with 6–7 generations asitism rate can reache as high as 98% in tea garden. This braconid per year in Guizhou province, with an average natural parasitism preferred to parasitize the 1st and 2nd instars with average para- rate of 13%. A. chrysomphali overwinter as mature larvae within fe- sitism of approximately 23 host larvae per female. It usually repro- male scales, and the adults emerge late April with peak emergence duces by amphigony, and occasionally with arrhenotoky. The in early May. High summer temperatures are unsuitable for para- female proportion of the population was 53–67%. Electroantenno- sitoid survival, leading to in-host mortality up to 67% (Tian, 1987). gram (EAG) and behavioral responses of this bracoind to tea shoot Aphidius sp. is a dominant parasitoid of the tea aphid, T. aurantii volatiles were studied by Huang et al. (2009). Methyl salicylate, (Boyer), with two population peaks, the first in May and the second E-2-hexenal and an equivalent mixture of E-2-hexenal, Z-3-hex- in October. Its parasitism rates ranged between 10% and 15% (Han en-1-ol and linalool paraffin solution elicited EAG and behavioral and Cui, 2003). The location and the selectivity of this parasitoid to responses. The methyl salicylate solution and, separately, the blend tea aphid damaged and normal tea shoots, various parts of the of methyl salicylate plus E-2-hexenal, prepared with hexane (as shoots, extracts of the shoots, tea aphid honeydew and several solvent) and loaded onto lures, generated intense attraction in kinds of non-host plant materials were investigated by Han and tea gardens of several provinces. Chen (1999). The authors showed that only aphid-damaged tea Apanteles sp. 2, also is a monoparasitoid that overwinters as shoots and honeydew attracted the parasitoid and the parasitoid prepupae within its cocoons on tea bushes. Its highest parasitism preferred to honeydew over other potential attractants. Han and rate was 45% in tea gardens (Hu et al., 1993a). The overwintering Chen (2002a,b,c) later reported that in wind tunnel experiments, cocoons are mostly distributed in the upper (87%) and middle volatiles from aphid-tea shoot complexes and benzaldehyde influ- (13%) parts of tea plants. Most of them (97%) were located on the enced three parameters, EAG responses, upwind flight and behav- dorsal leaf surface and the remaining 3% on the shoot. Under var- ioral arrestin this parasitoid. These two chemicals led to much iable ambient temperatures, the life cycle is about 12–14 days, stronger effects than other infochemicals. about 8–9 days from egg to cocoon and about 4–5 days to adult emergence. The adults lived about 1 to 2 days. This braconid pre- 3.1.3. Mymarids ferred to attack younger host larvae with average parasitism of Two species of Mymaridae, Stethynium empoasca Subba Rao and 12–13 host larvae per female (Hong and Yin, 1978). The optimal Schizophragma parvulas Ogloblin, parasitize eggs of E. vitis (Göthe), temperature for development and reproduction is between 23 at parasitism rates of 40 to 65% (Mao et al., 2008). The two mymar- and 28 °C. Similarly, Ye et al. (1994a) found that no adults emerged ids can reproduce by both patterns of amphigony and arrhenotoky. as reared at 14 or 34 °C. The initial developmental threshold tem- Their adults mostly emerge before 8:00 am. Females and males can perature and effective accumulative temperature were defined as mate immediately after emergence. For S. parvulas, mating usually 10 ± 3 °C and 250 ± 46 degree-days. It may have 11–13 generations lasted 10–20 s. S. empoasca mated a little longer, up to 2 min. The per year in Hangzhou, Zhejiang province. Apanteles sp. 2 operates reproductive capacity (36.8 mature oocytes/female) in S. parvulas in a tri-trophic pattern. Xu et al. (1998) reported that the larval oral was about one third higher than S. empoasca Subba Rao (22 mature secretions of tea geometrids induce damaged tea shoots to release oocytes/female) (Li and Lin, 2008). volatiles. These volatile compounds apparently attract this braco- In tea gardens of Fujian province, the population size of S. nid and possibly other parasitoids because the parasitic efficiency empoasca during June and July occurred in higher numbers than of this was increased by synomone release. They also showed other months, while S. parvulas populations were high between that b-D-glucosidase associated with the herbivore’s saliva may October and November (Mao et al., 2008). Population sizes are promote release of the synomone. Tea plant volatiles attractive influenced by regional environments. For example, the populations to this braconid were isolated and identified by Xu et al. (1999a). of these two parasitoids peaked in September in Zhejiang province Bioassay results showed that inexperienced female wasps had (Han et al., 2009). Annual seasons influenced the sex ratio (% fe- stronger preferences for volatiles emitted from mechanically dam- males) of the mymarids in the field: the proportions of females in- aged tea shoots (MDS) treated with regurgitate from host larvae, creased from 46% to 72% between January and December, and was for larval damaged shoots (LDS) and for the plant host feeding the highest (72%) in May (Li and Lin, 2008). complex compared to controls. Gui et al. (2004) reported that tea volatile organic compounds (VOC) induced by exogenous methyl 3.1.4. Scelionids jasmonatge (MJA) spraying or MJA exposure led to increased Telenomus euproctidis Wilcox is an egg parasitoid of E. pesudo- attractiveness of adult female parasitoids to the plants.MJA treat- conspersa Strand. The parasitism rate was mostly between 15% ments also increased the parasitism rate in field experiments . and 20%, but was highter for overwintered host eggs (45%) (Ai Apanteles conspersae Fiske parasitizes larvae of the tea tussock et al., 2000a,b). In Hunan province, it overwintered as the first , E. pseudoconspersa Strand. Among tussock moth parasitoids, instar, and the adults emerged in early April of the next year. The this one has the highest natural parasitism rate of about 20%. adults were distributed in an aggregated distribution pattern Although detailed studies are mostly limited to surveys of its par- (Wang, 1981, 1984). In the field, the female percentage of the sce- asitism rate in tea gardens (Xiao et al., 1999; Ai et al., 2000a,b), re- lionid was about 70% and 84% in the overwintering and the first sults of some ecological research have been reported. The generation. Environmental temperatures influenced length of their parasitoid primarily attacks larvae of the 2nd and 3rd generation life cycles, which took 21–22 days (at 21 °C), 17–18 (at 23.3 °C), and of the tea tussock moth. Its temporal and spatial niche breadth val- 10–12 days (at 30.1–30.9 °C). The average fecundity for females ues are 0.5683 and 0.5982, lower than those of its hosts at 0.8062 provided with a 20% honey solution was 32–46 eggs/female, and and 0.7234 (Ai and Zhao, 1999; Ai et al., 2000a,b). as seen for the life cycle, was influenced by temperature (Wang 78 G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 and Wang, 1987). This parasitoid can reproduce by both patterns of tea pests will depend on generation of still more fundamental amphigony and arrhenotoky. Within an oviposition period of knowledge of the parasitoids. 10 days, 80–90% eggs were laid within the initial five days. T. euproctidis prefers to deposit eggs into newly laid host eggs and also 3.2. Predatory insects can parasitize host eggs within embryonic stages. Usually the par- asitoid laid a single egg into a host egg, but this was influenced 3.2.1. Hemipterous predators by availability of host eggs. Females deposited 2–6 eggs/host egg Hemipterous predators are players in the population ecology of when host eggs were lacking. The parasitized eggs parasitized, in numerous tea pests, particularly lepidopteran pests in tea planta- which the parasitoid developed into the 1st larval stage, can be tions. The biological characteristics of the pentatomid, Cantheconi- stored at 9 °C for one month. Eggs of five lymantrid species, includ- dea concinna Walker and the mirid, Stethoconus japonicus ing Porthesia similis (Fueszly), P. kurosawai Inoue, E. varians (Walk- Schumacher has been descdribed. er), E. bipunctapex (Hopson) and E. dissimlis Wileman can be used as For C. concinna Walker, its annual life cycle and biological char- factitious hosts. Functional response of T. euproctidis was observed acteristics have been reported by Wu et al. (1983). This bug has by Ou et al. (1998), who reported that the functional response five nymphal stages. The 1st instar nymphs are not predacious curves of this scelionid at all five tested temperatures (18, 22, 26, and require plant saps to meet their growth to the 2nd instar. 28, and 32 °C) could be described by Holling’s type II equations, in The developmental durations lasted 7–26 days for eggs, 2–9 days which handling time is the limiting factor at high host densities. for 1st instars, 3–10 days for 2nd instars, 3–10 days for 3rd instars, The process of parasitism by this parasitoid was recorded by Ou 3–9 days for 4th instars and 4.5–25 days for 5th instars, depending et al. (1996a), which were divided into antennae drumming on different generations. In general, the adults began to mate about (14 s), assuming the probing posture (3 s), ovipositor probing 4 days after emergence and to lay eggs within 3–4 days after mat- (4 s), drilling (53 s), oviposition (50 s) and external marking (7 s). ing. Adults mated 3–5 times and oviposited 4–7 times. They laid They also found an obligate oviposition stimulant in the superna- 300–500 eggs per female, in masses of 40–90 and up to 100 eggs tant of host egg homogenates (Ou et al., 1996b). Ou (1997) later re- per mass (Wu et al., 1983). Xie (1987) reported that the bug is mul- ported that an egg-recognition kairomone acts in parasitization. tivoltine, with four or five overlapping generations in a year. For The kairomone from host egg masses could be extracted with polar adults overwintering in Guangzhou province, the overwintered fe- solvents such as distilled water, 70% methanol or ethanol, but not males started to lay eggs between late March and early April. The with n-hexane or acetone. Water- or methanol-extracts promoted bug attacks at least 18 species of lepidopteran tea pests, preferring the antennal movement and ovipositor probing, with the response eucleids. The annual lifecycle, prey range, herbivorous and gregar- rate up to 80%. The kairomone was stable in room temperature, but ious habits, cannibalistic and predation behavior and the control- not to boiling, as part of its activity is lost after boiling at 100 °C for ling efficacy of this bug were investigated by Zeng et al. (2004). one hour. Through use of the kairomone, the parasitic rate was in- There were more than five overlapping generations per year with creased. The scelionid had been induced to oviposit and success- the adults overwintering in eastern locations of Fujian province. fully develop in non-host eggs such as Porthesia similis Fuessly The adults became active in early May, and all developmental and Spodoptera exigua (Hübner). Thus, the use of this kairomone stages were active between June and October. The populations can help broaden the host range for T. euproctidis and possibly other peaked between July and August, and disappeared in early Novem- parasitoids and may increase the number of factitious hosts avail- ber. The 1st–3rd instar nymphs lived gregariously and then be- able for mass rearing and field releasing. came scattered. Later instars were cannibalistic if there was a prey shortage. Predator density led to mutual interference, espe- 3.1.5. Platygasterids cially in 5th instar. At a predator: prey ratio of 1:10, early nymphs Two species of platygasterids parasitize the spiny black white- consumed about one third of larval E. obliqua Prout. In addition, the fly, A. spiniferus Quaint., namely, Amitus hesperidum Silvestri and prey consumption for this bug to different tea pests was also mea- A. longicornis Föster. Zhu (1996) reported some biological charac- sured (Wu et al., 1983; Xie, 1987; Zeng et al., 2004), as showed in teristic of A. longicornis, a parasitoid of the 1st and 2nd instar Supplemental Table 6. nymphs of the spiny black whitefly (with about 45% parasitization S. japonicus Schumacher, is an enemy of Stephanitis (Norba) rate) in tea gardens of Hunan province. His results showed the par- chinensis Drak. It produces three generations annually with eggs asitoid had five and four generations in the laboratory and field, overwintering within leaf tissues. Among its biological characteris- respectively, per year. In tea gardens, parasitoid emergence peaked tics, adults deposited on average of 108, 60 and 121 eggs in the 1st, in late May, early July, mid-August, and late September, coordi- 2nd and 3rd generation, respectively. S. chinensis was effectively nated with the hatching peak of their hosts. The adults can mate suppressed by this bug the predator: prey range of 1:24–52.0 (ITS- within the first day after emergence. The females mated once, MTPSP, 1979). but the males did several times. The female adults lived five or six days. After mating, the females laid eggs into 1st instar nymphs 3.2.2. Coccinellids between 9:00 am and 4:00 pm and could lay up to 61 eggs per fe- Predatory ladybird are natural enemies of scales, aphids male in two days. and whiteflies. There are about 23 common ladybug species in Chi- Zhu and Chen (1994) suggested that the functional response of na, of which Chilocorus kuwanae Silvestri, Coccinella septempunctata this parasitoid to its hosts at seven various temperatures between L., Leis (Harmonia) axyridis (Pallas), and Propylaea japonica (Thun- 22 and 38 °C be described by Holling’s type II equation, and the berg), are the most dominant species, all accounting for a great suitable temperature range for parasitism be between 24.7 and share of total ladybug populations. Their populations peaked from 35.5 °C with the optimal temperature of 30 °C. Interference para- mid-April to late May, July and from late August to mid-September sitism among the parasitoids was described by Hassell & Varley’s (Han et al., 1996). Because of their value in biological control pro- model. Li et al. (1993) reported that a searching kairomone existed grams, some species have been studied in considerable detail. In in the host honeydew, which elicited strong host-seeking activity the following paragraphs, we treat several species. and increasedparasitization by 10–12% in tea gardens. C. kuwanae Silvestri is a polyphagous predator attacking 27 Research into the biology of parasitoids has yielded a great deal scale species from five families in tea and other crop systems of detailed information. Nonetheless, as seen in the relatively brief (Xia et al., 1985). In Guizhou province, C. kuwanae has four gener- descriptions just above, continued advances in biological control of ations annually. The overwintered adults deposit eggs from early G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 79

March to early April. The larval stage required about twice as much shoots (TADTS) and benzaldehyde, also emitted from TADTS, elic- time to pupation in spring (21 days), compared to summer ited strong EAG responses and strong upwind flight and behavioral (10 days). The pupal duration was about 10 days. The adults lived arrest in wind tunnel experiments. As mentioned just above, the for an average of 25 days. A 3rd–4th instar larva and adult con- honeydew secreted by tea aphids also strongly attracted this lady- sumed 19 and 34 scale insects, Temnaspidiotus destructor (Signo- bug. Recent studies using grey correlation analysis, ecological ret), respectively. A 3rd or 4th instar larva, as well as adult, niche analysis and spatial pattern of aggregation intensity index potentially consume up to 4120 scales in a year. In tea gardens, this analysis indicated that this ladybug was the important natural en- ladybug provides 90% control of T. destructor (Signoret). In some emy for tea aphid, and two species of whiteflies including A. spi- cases, T. destructor is parasitized by two parasitoids, Homalotylus niferus Quanit. and Pealius akebiae Kuwana in tea gardens (Dang haoninius Dalman and Tetraslychus sp. with the highest parasitism et al., 2010; Zhou et al., 2010), and also for the whitefly, Dia- rate of 66.7% (Xia, 1964). Similarly, Zhao (1980) reported that the leurodes citri Ashmead in low-altitude tea gardens (Bi et al., 2011). ladybug goes through four generations/year in Zhejiang province. P. japonica (Thunberg) is called the Japanese ladybird. It is lar- The fecundity averaged more than 80 eggs per female, and reached gely aphidophagous, but also preyed on whiteflies in tea and other up to 190 eggs. The predation of this ladybug on the scale, L. japon- crop systems. There aere several varieties, including P. japonica ab. ica (Cockerell) was as high as 280 scales per day, and possibly more lineate Kurisaki, P. japonica ab. faliciae Mulsant and P. japonica ab. than 3000 scales within its lifecycle. Yang et al. (1996) demon- dionea Mulsant (Qi et al., 2008). Behavioral responses to volatiles À1 strated that the innate capacity for increase (rm; 0.0606 day ) from tea plants were measured by Qi et al. (2008), who demon- and corresponding finite rate of increase (k; 1.0625 dayÀ1), mean strated the ladybug was attracted to the volatiles from tea plants. length of a generation (T; 82 days) and net reproductive rate Benzaldehyde and methyl salicylate had more attractive effects (95.6) of this ladybug, measured at 25 °C with Unaspis yanomensis than other components. The attractive processes include the influ- (Kuwana) as the prey. They also indicated that optimum tempera- ence of thresholds, however, and high dosages depressed the nor- ture range for this ladybug was 25 to 30 °C. The daily predation on mal attractiveness. Dang et al. (2010) indicated this ladybug is a U. yanomensis (Kuwana) was about 43 scales/female and 22 scales/ natural enemy for tea aphids, ranked before Mantis religiosa L. male (Yang et al., 1997). and L. axyridis (Pallas), and also is a predator of the citrus whitefly, C. septempunctata L. is another polyphagous predator that preys Dialeurodes citri Ashmead (Zhou et al., 2010). onnumerous species of aphid in tea and other crop systems. Sev- eral biological characteristics, including predation functional re- 3.2.3. Carabids sponses, artificial rearing and diets, natural enemies, and Predatory carabids are natural enemies of tea pests such as insecticide susceptibility have been documented (Cheng et al., hemipteran, lepidopteran and coleoperan pests. Some species of 2006). It had four or five generations annually, overwinters as these predators were recorded by several authors (Zhang, 1989b; adults, and becomes active in mid- or late-February of the next Xiao et al., 1992b; Chen et al., 2007a; Dai et al., 2010). Long and year as environmental temperatures increase up to 10 °C. One Liu (1986) reported Parena rufotestacea Jedlicka had two overlap- adult or 3rd instar larva on average consumes 50–100 aphids/day ping generations per year and overwintered as adults in Hunan (Gao et al., 2009). The functional responses of 1st–4th instar larvae province. The adults began to lay eggs in mid-May of the following and female adult to tea aphids could well fit Holling’s type II equa- year, the larvae were active between late-May and mid-June, and tion and the maximum prey consumption per day were 24.8 (1st the adults emerged in mid-July. Females began to lay eggs 30 days instar), 83.3 (2nd instar), 212.8 (3rd instar), 434.8 (4th instar) after mating. For the overwintered females, each female on average and 384.6 (adult females) aphids per individual (Ju, 2009). Olfac- laid 57 and 214 eggs in the 1st ovipostion period in May and June, tometer bioassay and electrophysiological analysis showed C. sep- and the 2nd oviposition period in August. The larvae and adults tempunctata L. responded to volatiles from tea aphids, to n-hexane consumed 33.2 (larvae) and 959 (adults) larvae of E. pseudocon- or to ether rinses of tea aphid cuticles.In more direct analyses, it re- spersa Strand. As seen in many insects, the larvae of this sponds to synomones released by aphid-damaged tea shoots and are cannibalistic during prey shortage (Long and Liu, 1986). Zhou to the tea shoot-aphid complex (Han, 2001; Han and Chen, and Lin (1987) indicated that this beetle consumes 12 species of 2000a, 2002a,b,c). The honeydew secreted by tea aphids also tea pests belonging to 5 families, preferring larvae of Lymantridae, strongly attracted this ladybug. Geometridae and Eucleidae. The larvae consumed 30 larvae of E. L. axyridis (Pallas) is also known as the multicolored Asian lady- pseudoconspersa Strand (all instars), with an average of 7 for each bird beetle. It is a generalist predator attacking numerous species instar of its prey and an average of 2.5 larvae/day. The 4th instar of aphid, scales and mites in a variety of crop sytems, including larvae account for 38% of total predation amount with an average tea. It expresses one to eight generations annually from northeast of approximately 11 preys per larva. There were three generations to east China and overwinters as adults. Research progress in sev- at least in the middle and northern parts of Hunan province, with eral biological and ecological parameters, including variations in different prey consumption rates for each of two prey species elytra color polymorphism, life history, fecundity, appetite, preda- (Zhang and Sun, 2009), as showed in Supplemental Table 7. tion, overwintering, dormancy, preservation, artificial rearing and field dynamics were reviewed by (Wang and Shen, 2002). Gao 3.2.4. Chrysopids et al. (2009) reported that the eggs or larvae of the 1st generation Chrysopids (lacewings) are predators of aphids, scales, leafhop- occurred in early- and mid-April and the adults emerged between pers, whiteflies and small moth larvae in tea and other crop sys- mid- and late May. In general, the adults lived about 35 days in the tems, of which Chrysopa pallens Rambur (C. septempunctata non-overwintering generation, which became shorter as the envi- Wsemale) and C. sinica Tjeder (Chrysoperla sinica (Tjeder)) are the ronmental temperatures increased in the summer. Adults depos- most prevalent taxa in tea gardens. ited 300–500 eggs/female. The 4th instar larvae individually C. pallens Rambur is a voracious predator. In a preliminary consumed 100–200 tea aphids per day (Gao et al. 2009). The adult study, Yin (1980) reported that one C. pallens larva or adult gener- behavioral responses to kairomone from tea aphids and damaged ally consumed 600–1000 aphids throughout their life. Female are tea shoots were determined. Han and Chen (2000b, 2002a,b,c) rather fecund, depositing on average 512–1000 eggs. In the south- showed that this ladybug had a preference for tea aphids, tea ern locations of Anhui province, five generations occurred annu- aphids plus aphid-damaged tea shoots and aphid-damaged tea ally, and its population in tea plants peaked during early and late shoots. The air entrainment extracts of tea aphid-damaged tea July (Gao et al., 2009). Liu et al. (2007) measured the selective 80 G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 predation of 2nd instar larvae on egg and 1st instar larvae of the S. enthastri larvae daily consumed 55–70 aphids/larva. The volatiles geometrid, E. oblique Prout. The results showed the lacewing had from tea aphids and their honeydew as well as tea aphid-damaged positive preference for the geometrid eggs. The volatiles from tea tea shoots, and specific compounds, including aldehydes, methyl aphids and aphid-damaged tea shoots strongly attracted this lace- salicylate, geraniol, n-octanol and (E)-2-hexen-1-ol strongly attract wing, and besides aldehydes and methyl salicylate, geraniol, n-oct- S. menthastri L. (Han and Zhou, 2004, 2007). anol and (E)-2-hexen-1-ol were attractive to this lacewing (Han and Chen, 2002c; Han and Zhou, 2004). Tea aphid honeydew is a 3.3. Predatory spiders contact kairomone for this lacewing (Han and Zhou, 2007). In addi- tion, C. pallens is the main natural enemy of the whitefly, Pealius 3.3.1. Agelena labyrinthica (Clerck) akebiae Kuwana (Dang et al., 2010). A. labyrinthica is a dominant spider in control of various tea Reportedly, C. sinica Tjeder produces six generations annually in pests such as E. vitis (Göthe) (tea green leafhopper) and E. obqulia tea gardens (Gao et al., 2009). One larva consumed 400–500 tea Prout (tea geometrid). Its population commonly occurred in early aphids before pupation. Liu et al. (2007) reported this lacewing May, early June and mid-August with a peak in early May, and had positive preference for the eggs, compared to 1st instar larvae daily consumed an average of 3.4 tea geometrid larvae of in the of E. obliqua. C. sinica responded to volatiles from tea aphids, hex- 1st–2nd instar (Hou and Zhao, 1988). The predatory functional ane or ether rinses of tea aphid cuticles, and to synomones released responses of this spider to the green leafhopper, E. vitis (Göthe) by aphid-damaged tea shoots. Tea shoot-aphid complex the vola- were studied in laboratory by Zhao et al. (2001a), who showed that tiles from the tea shoot-aphid complex and benzaldehyde elicited the functional responses of male and female spiders belonged to more arresting behavior from C. sinica than other infochemicals Holling’s II type. Greed leafhopper predation by female spiders (Han, 2001; Han and Chen, 2002a,b,c). Similarly, tea aphid honey- was greater than male spiders, and their predatory upper limits dew is a contact kairomone for this lacewing (Han and Zhou, 2007). were 295 adults for females and 120 for males. The authors inferred that the spiders have potential as biological control agents 3.2.5. Syrphids for the leafhoppers. Syrphid flies, also known as hover flies for their ability to hover in flight, are common predators of aphids and other soft bodied in- 3.3.2. Evarcha albaria L. Koch sects. Five species occurred commonly in tea plantations and effec- This is one of the predatory enemies of tea green leafhopper, E. tively controlled tea aphid populations in the spring and autumn, vitis (Göthe). Gao et al. (2004) reported the functional responses as listed in Table 2 (Zhang, 1989b). Their populations decline in of both female and male spiders to leafhopper adults and nymphs late spring and early summer because of high temperature, short- belonged to Holling’s II type. The control competence (a/Th) of the age of flower nectar and attack by their own natural enemies spider on the prey was in the order of female spiders on including spiders, carabids and parasitoids, of which the common nymphs > male spiders on nymphs > female spiders on adults > - species included Diplazon laetatorius (Fabricius) and Pachycrepoide- male spiders on adults. There was significant variation among us sp., with parasitism rates of 27–35% and 18–26%, respectively spider individuals. Isolation and identification of volatiles within (Dai, 1995a). the tea plant-green leafhopper-spider system were investigated B. serarius (Wiedemann) populations peaked between April and by Zhao et al. (2002). The attractive rate of the spider toward May, consistent with the occurrence of tea aphids in Hangzhou, the volatiles from normal tea shoots and mechanically damaged Zhejiang province (Yin, 1979). The developmental periods of larvae tea shoots was weaker compared to tea shoots damaged by tea (9–10 days) and pupae (10–12 days) as well as the life span of green leafhoppers. Among the tested components from various adults (2–3 days) in early to mid-May were recorded (Yin, 1979) volatiles of damaged tea shoots, the 2,6-dimethyl-3,7-octadiene- A single 3rd instar larva daily consumed 100–200 tea aphids. Some 2,6-diol and indole were specific compounds formed after the biological characteristics were observed by Dai (1995a). It occurrs damage by tea green leafhopper, and these two compounds are in six or seven overlapping generations/year, and overwinters as a the active compounds responsible for attraction to the spider. In complex of eggs, mature larvae, pupae and adults in Guizhou prov- separate work, Hou and Zhao (1982) observed that a single fe- ince. The population peaked twice in early of May and June and in male spider daily consumed an average of 1.7 larvae of E. obliqua September and mid-October. The populations began overwintering in 2nd–3rd instar. in late October. At 20–22 °C, the average duration of eggs, larvae, pupae as well as the lifespan of adults were 4, 8, 11 and 15 days, 3.3.3. Erigonidum graminicolum Sundevall respectively. However, durations for eggs, larvae and pupae be- This spider is active from April to December and populations came longer as environmental temperatures decreased below peaked in early June and mid-September in Anhui province and 15 °C or increased above 26 °C. The longevity of adults declined it accounts for 22% of total number of spiders in tea gardens. and the fecundity and egg hatching rate also decreased when envi- An adult female daily consumed an average of 3.3 E. obliqua Prout ronmental temperatures were outside the 15–26 °C range. Dai larvae in 1st–2nd instar (Hou and Zhao, 1982, 1988). Guo (1987) (1993) reported a preliminary study on rearing this fly. It showed indicated that the predatory functional responses to 1st–2nd in- that the larval survival rate and adult emergence rate were 77– star nymphs and to 3rd–5th instar nymphs of E. vitis (Göthe) 80% and 90–92% when provided with one of three species, T. aur- could be described by Holling’s I and II types, respectively, and antii (Boyer), Myzus persioae (Suszer) or Macrosiphoniella sanborni the spider preferred nymphs of the leafhopper over 2nd instar (Gilltte). These parameters were reduced to 40% and 58% when larvae of Homona coffearia Nietner. The predatory functional and fed on Myzephis rosarum (Kaltenbach). Maize pollen was the best interference responses of this spider to the leafhopper at various diet for the fly adults, which laid an average of 894.6 eggs/female temperatures from 22 to 28 °C were observed by Xie (1995). The with the average longevity of 15 days for females and 14 days for results revealed that the functional response matched Holling’s II males. type, and the interference response could be described by the The biological characteristics of E. balteatus (de Geer) (Yin and model of Wett. Environmental temperature influenced the search- Zhou, 1980; Gao et al., 2009) and S. menthastri L. (Zhang 1989b) re- ing efficiency of the spider. Xie (1996) reported that the preda- main under-investigated. E. balteatus larval populaitons peaked in tory ability of this spider was stronger compared to two other May, and individually consumed an average of 110–120 tea spider species, Clubiona japonicola Boes. et Str. and C. maculate aphids/day and a total of 1400–1500 tea aphids during its lifetime. Roewer through comparisons of predatory functional responses G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 81 of these three spiders to tea green leafhopper. Similarly, Lin et al. Other researches led to identification of other spiders as effec- (2007) studied the predatory functional responses of this spider tive biological control agents. Guo (1989) studied predation of to tea aphids. The functional responses again belonged to Hol- Oxyopes sertatus (L. Koch) on Homona sp. Work on three other spi- ling’s II type. Intraspecific interference also influences predation der species, Clubiona japonicola Boes. et Str. (Wang and Zhang, in this system. The predation rate also decreased with increasing 1993), Chrysilla versicolor (C. L. Koch) (Xie, 1993) and Silerella vitta- gof predator density. Mutual interference of prey and predator ta (Karsch) (She et al., 1996)toE. vitis (Göthe) were also conducted, densities could reduce the searching efficiency of this spider, showing these spiders alo act in controlling tea pests. but had no effect on total predation. A single female consumed 48 wingless and 67 winged tea aphids/day and a male adult con- 3.4. Predatory mites sumed 39 wingless and 55 winged aphids/day. Both predatory functional and intraspecific interference responses of the female Several predacious mite species were studied as potential bio- adults to female adults of the whitefly (A. spiniferus Quaint.) were logical control agents for control of small-sized tea pests. observed by Zhao et al. (1995), who reported that the functional response also could be described by Holling’s II type, and the con- 3.4.1. Neoseiulus (Amblyseius) cucumeris (Oudemans) trol ability on the whitefly was approximately 67 whitefly adults/ N. cucumeris (Oudemans) was first introduced into China to day. control greenhouse thrips in the 1980s and later for tea pests in tea orchards (Li and Fu, 2006). Global research progress in its clas- 3.3.4. Xysticus ephippiatus Simon sification, distribution, biological characteristics, mass rearing and The predation of penultimate-instar X. ephippiatus on 3-day-old application were summarized by Li and Fu (2006). Here, we review larvae of the tea geometrid, E. obliqua was determined at different some studies in China. Ji et al. (2001) reported the laboratory pop- temperatures by Wang et al. (2010c). The results showed that all ulation life table and predation of this mite on tea pink mites, A. the functional responses could be described with Holling’s type II theae Watt. The intrinsic rate of natural increase (rm: 0.19), net equation. At constant temperature, the predation capacity of this reproductive rate (R0: 21.8), time for population to double (t: spider was enhanced with an increase in prey density. The maxi- 3.6), mean generation time (T: 16.2) and the finite rate of increase mal predation of female spiders was 68 larvae/day at 25 or 30 °C, (k: 1.2). One female adult laid an average of 39 eggs with daily ovi- and for males at 30 °C 67 larvae/day. When the temperature and position rate of 2.2 eggs. In the whole lifecycle, each female and the density of the prey were same, the predation was not different male mite consumed 1978 and 979 tea pink mites. Similar studies between female and male spiders, but temperature influenced pre- by Li et al. (2003a) with P. latus (Banks) as prey at three environ- dation. Hou and Zhao (1982) reported that female spiders on aver- mental temperatures, 23, 25, 28 and 30 °C. 25 °C was the optimum age consumed 1.3 larvae of 1st and 2nd instar tea geometrid per temperature for the development and reproduction of N. cucumeris. day. Li et al. (2003b) reported that the lower and upper temperature thresholds for development of N. cucumeris from eggs to adults were 12.77 and 33.50. All functional responses for 1st and 2nd in- 3.3.5. Misumenops tricusipdatus Fabricus star nymphs and female adults on female adults of P. latus (Banks) The predatory functional response of penultimate-instar M. tric- matched the Holling’s II type.The predation by the mated female usipdatus to tea green leafhoppers was studied by Pan and Zhao adults was the most efficient, followed by the deutonymphs (Li (1995). Their results indicated as the following: each penulti- et al., 2001, 2003c). mate-instar spider consumed 18 nymphs and 17 adults per day, the functional response and mutual interference among individual 3.4.2. Anystis baccarum (L.) spiders could be stimulated by Holling’s equation and Hassell & A. baccarum (L.) is also known as the whirligig mite. It is a pred- Varley’s equation, respectively, and the temperature influenced ator on phytophagous mites, leafhoppers, aphids and scales in tea the functional response. and orchard gardens (Zeng et al., 2007). Populations are active The speed of predation of this spider was not influenced by prey from April to July, October to November, and they peaked in June body size, but impacted by temperature, starvation and gender. and within October to November in tea gardens (Zhao and Hou, The optimal temperature for predation was 25 °C and the preda- 1993). There were 2–3 generations/year and one generation took tion speed slowed at 34 or 14 °C. Under starvation for three or four 99.5 days on average at 21 °C. No diapause was found in winter, days, the speed of predation increased. Male spiders were faster fe- although the mites aestivated in summer as the temperature in- males. The co-ocurrance of spiders, for example female and male, creased above 28 °C(Wu, 1994). Effects the whirligig mite on tea female and female, male and male, also had some effects on the red spider mite, Oligonychus coffeae (Nietner) were studied by Liao predation rate. When two male spiders coexisted, they both slo- et al. (2010). The simulated equation on the effects of predation on wed their predatory speeds. When two female spiders co-ocurred, tea red spider mites corresponded to the Holling’s II type there was no impact on either one. When one male spider and one model.Predation was affected by prey stage, temperature and female spider were together, males decreased their predatory rate predator density. The adults tended to prey on the larva and while females did not (Xiong et al., 2004). nymphs and the highest predation amounted to 49 and 38 per day. At the same prey density, predation increased with the tem- 3.3.6. Hylyphantes graminicola (Sundevall) perature ranging from 15 to 30 °C, however it decreased at 35 °C. A function response for predation of this spider to tea geome- At 30 °C, predation was the highest, which closely matches the trid, E. obliqua was studied with the design of positive rotation temperature for the red spider mite reproduction peak in autumn. combination by Chang et al. (2006). Their work defined the effects The average predation number and rate of A. baccarum decreased of prey and predator densities and interferences within species on with the increase of its density. In a separate study, the functional functional responses. These parameters influenced predation when response of this predatory mite to tea green leafhopper, E. vitis densities of prey or predator were changed. The largest effector (Göthe) also fit Holling’s type II curve (Zeng et al., 2007). was the density of the predators. Liu et al. (2007) reported that this Amblyseius deleoni Muma et Denmark is also a predatory mite of had no evident selectivity to 1st instar larvae of tea geometrid and various tea phytophagous mites, whiteflies, thrips and scale as well the adults of tea green leafhopper, and their selective efficiency did as pollen of some plant species. It preferred P. latus (Banks). Its bio- not transfer with the increase of prey densities. logological characteristics and rearing method using pollens from 82 G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 various plant species have been preliminarily studied by Wang of tea geometrids (Ye et al., 1994b). The viral virulence to tea geo- (1985). Its population peaked in spring and autumn and decreased metrids was synergized with the 02–85 strain of Bt (Xu et al., 2006). in summer due to high temperature. For its survival, development EpNPV has been applied for the control of E. pseudoconspersa and reproduction, the suitable and optimal temperatures were 11– Strand by large scale field application with concentrations of 3– 25 °C, and 18–22 °C, respectively, with the suitable relatively 6 Â 107 PIB/ml led to more than 80% caterpillar mortality (Sun humidity of 75–95%. Above 28 °C, the reproduction was inhibited, et al., 1988, 1996). Yin and Xiao (2004) improved the spraying and the mortality increased, up to 100% up to 30 °C. One female techniques for this virus, and they obtained 100% control of E. adult laid 11–46 eggs with a daily number of 1–2 eggs. The longev- pseudoconspersa Strand by spraying 7.5–1.5 Â 1011 PIB/ha in the ity of adults averaged 34 days, and up to between four and five field. When EpNPV (1 Â 107 PIB/ml) and Bt (2000 IU/ll) were months in the overwintering generation. A single female adult dai- mixed and used as foliar spray at 750–1500 ml/ha, 98% control ly preyed on 8.7 eggs, 9 larvae, 7 nymphs and 6.7 adults of P. latus efficacy was obtained within one month, which led to 98.8% mor- (Banks). tality at the next generation (Xiao et al., 2004). The EoNPV-Bt mixed preparation enhanced the lethal rate of the pest by 1.8 times compared to EpNPV alone.The mixed treatment led to 4. Biological control in the development and implementation of 86% mortality of Inagoides fasciata (Moore) (Leng et al., 2007). A IPM lateral spray method directed toward the lower part of tea bushes at 1.5 Â 105 PIB/ml was recommended to enhance the control Biological control of tea insect pests in China was practiced as effectiveness. This method obtained over 90% control of the pest early as the 1960s. As reviewed here, extensive efforts were fo- (Yao et al., 1987). cused on natural enemy surveys, identifying potential biological Mass production and application techniques of AbGV against control agents, understanding their biology and their ecological Andraca bipuncta Walker were investigated (Ding et al., 1996, services within tea ecosystems. We stress the point, however, that 1999). The control effect of AbGV suspension sprayed at 600 ml/ biological control is not the only tool applied to the management of ha was 80–91% and control was increased to 86–97% when mixed tea pests. Biological control has been used within the context of with the lower dose of the chemical insecticide bisultap. Within 1– integrated pest management (IPM), especially in the past two dec- 3 years after AbGV spray, 47–62% of the caterpillars were still in- ades. Other IPM tools, such as host plant resistance, insect habitat fected by the virus in tea gardens (Ding et al., 1999). Use of the protection, cultural control and selective insecticides, are also used purified AbGV suspension was encouraged to protect natural ene- to protect natural enemies in tea ecosystems and to improve tea mies although the control effect of the virus was improved by sev- quality and quantities by achievingbetter and greener control of in- eral chemical insecticides (Zhang et al., 1995). AoGV was also sect pests. utilized to control the smaller tea tortrix, Adoxphyes orana F. & R. (Du et al., 1984). The results showed that 87–93% control was ob- 4.1. Release and utilization of natural enemies tained by spraying 187.5–375 mg/ha AoGV suspension (one in- fected larva was equivalent to 0.5 mg of AoGV suspension), and 4.1.1. Viruses the viral infection efficacy was maintained at least 16 generations Since the end of 1970s, several insect viruses, such as Buzura over more than three years after spraying. suppressaria NPV (BsNPV), Ectropis obliqua NPV (EoNPV), Euproctis pesudoconspersa NPV (EpNPV), Andraca bipuncta GV (AbGV) and 4.1.2. Bacteria Adoxphyes orana GV (AoGV) have been used as large-scale biocon- Although commercial formulations of Bt have been popularly trol agents in tea plantations. Of these useful viruses, EoNPV and applied in vegetable and fruit crops as well as forest ecosystems, EpNPV formulations are currently registered as biological agents they were only tested at small scale in tea ecosystems because of in China. BsNPV has been applied in more than 20 farms in seven their low to moderate toxicities towards tea lepidopteran pests. provinces, and resulted in 97% and 93% mortality of the 1st and Several studies on the effectiveness of Bt formulations to some 2nd generation of B. suppressaria Guenee at 10 days after spraying lepidopteran species including B. suppressaria Guenee and of polyhedral suspensions at the concentration of 3 Â 1012 PIB/ha D. baibarana Mats., E. pseudoconspersa Strand and E. obliqua Prout (Peng et al., 1998). The spray treatments contributed to possible in small-scale field trials have been reported (Chen et al., 1990b; infection of the next generation as well (Peng et al., 1986). The pro- Liu, 1994; Zhu et al., 1999; Zheng, 2001). The tested Bt prepara- tocols for production of this viral insecticide involve infecting B. tions often resulted about 90% caterpillar mortality. Against suppressaria larvae reared on an artificial diet with BsNPV inocu- E. obliqua Prout, however, Bt led to about 50% control in some cases lum propagated in insect cell cultures (Xie et al., 1992). (Xu et al., 1999b; Zheng, 2001). Bt formulations were recom- Several studies reported on mass production of EoNPV. Protocols mended for mixing with some chemical insecticides or tea insect include suitable rearing conditions combined with viral infection viruses. Several Bt strains with high toxicity to tea pests have also concentrations and host stage, as well as temperature, using Den- been selected and investigated (Xu et al., 2004). It remains to select dranthema morifolium Ramat leaves instead of tea leaves for rearing effective strains of Bt against lepidopterous pests so as to improve E. oblique larvae (Wu and Hu, 1987; Ye et al., 1992; Hu et al., 1993b). the application status of Bt in tea cultivation. For the control of the tea geometrid in the 1st and 5th generations (also the 2nd generation in some years when the temperature falls 4.1.3. Fungi below 28 °C), the viral suspension could be sprayed alone at con- Entomopathogenic fungi perform better in the ecosystems with centrations between 1.09 and 2.25 Â 1011 PIB/ha, and resulted in more than 80% relative humidity, yet application of fungi on tea 96–100% pest mortality. For control during the 3rd and 4th gener- crops has not reached it potential. Here we treat three fungal spe- ations (2nd generation in some years, when temperatures rise over cies that have been use in China, including B. bassiana (Balsamo) 28 °C), the viral suspension (concentrations between 2.25 and Vuillemin, A. webberi Fawcett and P. fumosorosens Wize. 4.50 Â 1011 PIB/ha) are integrated with fenvalarate at the concen- Strain 871 of B. bassiana has been used for control of the tea tration of its LC25 to obtain 78–100% control of the pest (Hu et al., weevil, Myllocerus aurolineatus Voss. (Wu and Sun, 1994; Wu 1997). Use of microbial control agents is increasing. Application et al., 1995). Sprays of conidial suspensions (100–200 million con- and utilization of EoNPV preparations were also reported (Yin idia/ml at 15–30 kg/ha) at the peak stage of pupation resulted in et al., 2000, 2003). Spraying this virus, produced sustained control 65% mortality of larvae and pupae in soil and more than 80% adult G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 83 mortality. Sprays of 7.5–15 kg/ha conidial suspensions at 1– Entomopathogenic nematodes have been investigated for pest 2 Â 108 conidia/ml led to more than 80% control of the weevil. This control in tea. For example, Steinernema carpocapsae (Weiser) efficiency lasted one and two years in tea gardens. In a 2000 ha (strain AII) produced the highest efficacy (83%) to control larvae field trial, the average control effectiveness of 81% (ranging from of the tea brown beetle, Basilepta melanopus Lefevre in organic 68% to 96%) was obtained (Wu et al., 2002). This fungus was also tea gardens (Liao et al., 2007). formulated for mixed application with some synthetic pyrethroids and organophosphorus insecticides in soil, which controlled over- 4.2. Implementation of IPM for tea insect pest control wintering weevils during October–December (Sun et al., 1993). B. bassiana strain Ef465-3 was used to control the tea leafhopper, E. 4.2.1. Host plant resistance flavescent Fabricius by spraying conidial suspension at 8 Â 106 - Host plant resistance is a fundamental component of IPM, conidia/ml, yielding over 85% mortality (Wang and Tan, 1989). which can protect crops by making them less suitable for the pest To control ttea green leafhopper, E. vitis (Göthe), B. bassiana strain or by making them tolerant to pest damage. Substantial morpho- Be2 (108 conidia/ml suspension) produced high toxicity (80%) to metric and genetic variability exists among tea cultivars, to which nymphs and adults (Cai, 2005). An oil-based emulsifiable B. bassi- pests react differentially. Such diversity has facilitated host plant ana formulation (strain SG8702) containing imidacloprid 10% WP resistance selection and development. Most studies on insect resis- at a rate as low as 615% of its recommended rate was incorporated tance concern differences in tea cultivars to pests, particularly to into the system, resulting in the maximal efficacy of 83% (Pu and smaller insect and mite pests with piercing/sucking mouthparts. Feng, 2004; Feng et al., 2004a,b). Zhu (1992) reported that tea varieties with the character of late A. webberi Fawcett is a prominent biocontrol agent of the black sprouting were resistant to tea green leafhopper, E. vitis (Göthe) spiny whitefly, A. spiniferus Quaint. in tea ecosystems. Sprays of and those with leaves curled downward and long distances be- this fungus suspension (at the concentration of 1.46 Â 107 and tween buds were susceptible. He concluded that the thicknesses 2.92 Â 108 conidia/ml) yielded more than 70% control of whiteflies of palisade tissue and thick horny cells were key factors for the in large-scale tea gardens, and also contributed to persistent effec- resistance to the leafhoppers. Similar studies were also reported tiveness for more than two years (Chen et al., 1994, 1997). Another by other investigators (Zeng and Wang, 2001; Hu et al., 2003; fungus Paecilomyces fumosoroseus Apopka (strain Pfr116) has been Zou et al., 2006). The correlation between leaf structure or bio- applied for the control of tea green leafhopper. Spray of oil-based chemical components in new tea shoots and their resistance to emulsifiable formulation at 2 Â 107 conidia/ml mixed with imida- the black spiny whitefly (A. spiniferus Quaint.) were also investi- cloprid 10% WP at a rate 3% of its recommended rate resulted in gated (Wang et al., 2006a, 2009; Chen et al., 2007b). The fecundity 71% control of the leafhopper (Pu and Feng, 2004). of the whitefly was positively correlated with stoma density and thickness of spongy tea tissue. The whitefly fecundity was also 4.1.4. Parasitoids and predators negativele correlated with thickness of palisade tissue, and some By comparison with entomopathogens just described, little biochemical compositions (phenylalanine, soluble proteins, ala- attention has been paid to release parasitoids and predators for nine and methionin) in new shoots. Studies of another biological controlling tea pests except some small scale field trials. Hu et al. parameter, the generational survival rate, revealed a positive corre- (1980) reported that the larval parasitism rate of the tea geometrid lation with stoma density, and a markedly negative correlation increased to about 90% after releasing a braconid (Apanteles sp. 1) with thickness of subepidermis and the palisade tissue cuticular in a tea garden. Zhang et al. (1980) released three batches of Tricho- layer on subepidermis. With respect to the biochemical make up gramma dendrolimi Matsumura at the rates of 3 Â 105,6Â 105 and of new shoots, survival was negatively correlated with 3 Â 106 adults/ha, to control the smaller tea tortrix with an average phenylalanine. parasitism rate of 83.3% to the pest eggs. Similarly, releasing T. Similar studies of resistance to mite pest such as A. theae Watt ostriniae (Peng & Chen) led to an average parasitism rate of 64%. (Chen et al., 1996, 2000b; Xu et al., 1996; Yao et al., 2008), P. latus As to predatory insects and spiders, their protections in tea garden (Banks) (Liu et al., 1994a,b,c, 1996, 1999) and Oligonychus coffeae remain troublesome. (Nietner) (Zeng et al., 1995) were also reported. Recently, the resis- Predatory mites are biocontrol agents for the control of tea mite tance to tea pests of 105 accessions of tea germplasms collected pests. Two predatory mites, N. cucumeris Oudemans and Cheyletus from Yunnan province were identified and evaluated by field test- fortis Oudemans were used to control two important phytopha- ing, indicating that three and two accessions, respectively showed gous mites, A. theae Watt and P. latus (Banks) by releasing of pred- high resistant to E. vitis and O. coffeae (Nietner) (Wang et al., atory mites with 150,000 individuals/ha (Su et al., 2001). This 2011a). treatment produced better control than chemical treatments. For A. theae Watt, the control efficacies by N. cucumeris were 94% and 4.2.2. Cultural control 64% by 10 and 30 days after mite release, respectively. Chemical Tea cultivation and management through cultural practices, treatments led to 63% and 48% mortailities. As for the control effect such as picking, pruning, fertilization, and insect habitat manage- on P. latus (Banks), control by N. cucumeris was similar to chemical ment by intercropping other plants can increase the growth poten- controls, all generating about 98% efficiency. Similarly, Zhu et al. tial of tea while also increasing its resistance to pests and diseases. (2010) showed that 23.8–81.3% control of Brevipalpus obovatus Picking and pruning tea shoots (main harvested tissues) are effec- Donnadieu was obtained 10–50 days after releasing 54 predatory tive means of pest control because tea shoots are nutrient-rich and mites per square meter. They also suggested that the release of prone to infestation by insect pests such as tea aphids, tea leafhop- the predatory mite by hanging a sachet with 300 mites per tea can- pers, tea miners and mites. Shoot picking reduces an insect food opy is enough to control B. obovatus Donnadieu. source, disturbs insect living conditions and greatly reduce num- Utilization of spiders in biological control programs is best bers of eggs and larvae on tea. Du et al. (2003) reported that the accomplished by conservation control strategies based on mini- populations of tea green leafhopper, E. vitis (Göthe) were reduced mizing use of chemical insecticides because we have no suitable by 15% to 28% through shoot pruning. At the same time, the com- techniques mass produce spiders. For example, the population of plex spider populations were increased by more than 25%. the green leafhopper was effectively suppressed by spiders at ra- Mechanical picking reduced the populations of tea green leafhop- tios of spiders: leafhoppers was between 1: 5.6 and 1: 7.6 (Lei per by an average of 56% had less impact on spider populations et al., 1992). by an average of 17% (Zhang and Wang, 1993a). 84 G.-Y. Ye et al. / Biological Control 68 (2014) 73–91

Intercropping non-tea plants and regulating tea garden man- through the year in the covered fields, while pesticides were used agement patterns are effective means of pest control and natural 5–7 times to control tea pests in the uncovered fields. enemy protection by enhancing biodiversity (Tan et al., 1998; Deng and Tan, 2002; Jiang et al., 2003; Han et al., 2007; Ye et al., 2010; 4.2.4. Sex pheromone and its application Wang et al., 2010d; Chen et al., 2011a). For example, Jiang et al. For pest monitoring and control, studies of sex pheromones (2003) reported that the populations of the mite, P. latus (Banks) from several species of tea pests have been conducted. The sex were reduced by intercropping non-tea plants in tea garden. Mite pheromone of the tea geometrid (E. obliqua Prout), includes seven control efficiency varied with the kinds of trees interplanted with bioactive components, all of which were synthesized (Yin et al., tea bushes as follows: cedar > pear > peach > plum. Ye et al. 1990, 1993; Liu et al., 1994d). The mixture of (z, z, z)-3, 6, 9-docos- (2010) reported that leafhopper populations and the usage times atriene, (z, z, z)-3, 6, 9-tetracosatriene and (z, z)-9, 12-oetadecadi- of insecticides were reduced because of the increase of spider pop- en-1-al (ratio 1:1:1) was attractive to male , trapping about ulations by intercropping citrus, waxberry or snake gourd plants. 27% of them (Yin et al., 1993). Similarly, Chen et al. (2011a) managed mite pests by intercropping The sex pheromone of tea tussock moth (E. pseudoconspersa with a species of grass, i.e. Paspalum notatum Flugge or Cassia Strand) was quite effective in trapping the pest (Zhao et al., rotundifolia Pers., which significantly increased diversity of preda- 1998; Ge et al., 2002, 2003; Wang et al., 2006b). The numbers of tory mites. gravid females, eggs and larvae were decreased by 93% 85% and A measure of mulching rice straw in the ground resulted in the 815%, respectively, by mass traps charged with the sex pheromone, effective control of leafhoppers and aphids by protecting and 10, 14-dimethylpentadecyl isobutyrate (Ge et al., 2002). increasing populations of natural enemies, especially spiders (Zhang and Wang, 1993b; Xiao et al., 2006). Appropriate fertiliza- 4.2.5. Forecasting and control action threshold of tea pests tion was also important for conversation of natural enemies, sug- The monitoring and forecasting of tea pests is a crucial aspect of gesting the annual suitable usage of nitrogenous fertilizer controlling tea pests in a time-sensitive manner. Seasonal abun- (760.01 kg/ha) in Wuyi tea garden of Fujian (Chen, 2008). dance and numerical predictions of tea green leafhopper were investigated for setting up empirical prediction equations (Zhu, 4.2.3. Physical control 1986, 1991, 1992, 1993). The first population peak was closely cor- Various types of light traps, emergence traps, colored sticky related with the number of days in which mean daily temperature traps and pheromone traps have been used for pest monitoring was 0 °C or below from the beginning of December to the end of and control. Black-light traps, frequency-vibrated lamps with the the next March, and the second peak was correlated with the ratio wave length of 320–400 nm, were applied in a tea garden (Qi of rainfall to mean ambient temperature in July and with the rain- et al., 2005; Wen et al., 2009; Zeng et al., 2010; Wang et al., fall amount in August. Numbers of the 1st peak were positively 2011b). In general, the lamps are set up between 50 and 60 cm correlated with leafhopper density after overwintering and at the above tea canopies, about 120–155 m apart. The control efficacy 1st generation, while negatively correlated with rainy days in of tea pests, especially lepidopteran pests, was usually between March and April. Analogous forecasting techniques for three spe- 50% and 80%, covering 2.7–4.0 ha tea gardens by one lamp. Under cies were set up. These are the late hatching stage of 1st generation this system, the ratio of natural enemies (mainly including syrphid and the adult peak stage of the overwintering generation of A. spi- flies, coccinellids, chrysopids, carabids and parasitoids) to pests is niferus Quaint. (Zhu, 2000), the late hatching stage of 1st genera- 1:114–132. Zeng et al. (2010) also indicated that light emitting tion of L. japonica (Cockerell) (Zhu, 1990) and the 1st beginning diode (LED) lamps are more promising for controlling tea pests. population peak of A. theae Watt (Lu and Lou, 1995; Xu and Zheng, The lepidopteran insects, coleoptera pests and natural enemies 1998). Similarly, the forecasting methods of occurrence time and were preferably trapped by violet LED lamps with wave lengths amount for E. obliqua Prout, D. baibarana Mats. and Myllocerinus of 385–390 nm over blue ones with wave length of 450 nm. Blue aurolineatus Voss were also developed by Zhu (2002). LED lamps were more efficient in traping hemipteran, dipteran, The control action thresholds of tea pests are necessary for homopteran and ephemeropteran pest and red LED lamps with making control decisions and designing pest management pro- wave length of 660 nm were not effective traps. Overall, LED lamps grams to reduce pesticide usage. Up to date, the control action were safer to natural enemies than frequency-vibrated lamps. thresholds of nine tea pests have been determined in China Colored sticky traps have been used for controlling several in- (Table 4). sect pests. Wang et al. (1991) found that the lemon-yellow papers more effectively attracted neonate larvae of E. obliqua Prout than 4.2.6. Rational use of insecticides yellowish brown and yellow-green papers, or tea branches. Zhao To enhance natural enemies in tea ecosystems, it is necessary to et al. (2001b) showed that the false-eye green leafhopper, E. vitis select pesticides that are safer for the valued natural enemies, but (Göthe) had a preference for yellow green and pale green. In the effective against pests. It is necessary, also, to use chemical pesti- field applications, Xiang et al. (2007) proposed that bud green cides appropriately, and to prohibit all synthetic pesticides in or- and jasmine yellow sticky plates effectively trap leafhoppers and ganic tea gardens. Surveys of the pest and natural enemy whiteflies, respectively. Han et al. (2008) documented effective complex under two different management systems in tea: organic trapping of the moth E. pseudoconspersa Strand using bud green vs conventional practices are instructive. Pest populations were and jasmine yellow sticky traps. Trapping efficacy was markedly lower but natural enemy populations were higher in organic tea increased by combining these colors with the sex pheromone trap. gardens, compared with conventional ones (Du et al., 2004; Han, Lin et al. (2009) also suggested that the jasmine yellow and bud 2005; Han et al., 2006, 2007). Another survey found leafhopper green sticky plates can be used to monitor and control the leafhop- populations were reduced by 37% and spider populations were in- per and the whitefly in tea gardens after comparing the effectives creased by 34% when annual insecticide spraying was reduced of 10 types of color sticky traps. Green sticky traps containing info- from 6 to 7/year to 1 to 2 times/year and applied with the insect chemicals were attractive to the parasitoid Apanteles sp. for control growth regulator, buprofezin (Zhang and Wang, 1994). of tea geometrids (Han et al., 2005). To reduce adverse effects of pesticides, safety evaluations with Covering tea gardens with gauze net can protect tea plants from respect to natural enemies have been carried out. Zhu (1988) doc- pest damages. Zhu et al. (2001) indicated that both species and umented that deltamethrin, with 7% lethality spiders 10–13 days numbers of tea pests were reduced and pesticides were not used after spraying, was safer than fenvalerate and dimethoate with G.-Y. Ye et al. / Biological Control 68 (2014) 73–91 85

Table 4 The control action thresholds of tea pests determined in China.

Species Control action threshold Reference Insect pests Aleurocanthus spiniferus 6 Individuals per leaf Chen et al. Quaintance (1997) Dasychira bailaranan (1) Overwintering generation: 43,500 and 34,500 larvae/ha for tea garden with the annual made tea output of 2250 and Zhu and Shang Matsumura 1500 Kg/ha, respectively(2) 1st Generation: 67,500 and 55,500 larvae/ha for tea garden with the annual made tea output (1992) of 2250 and 1500 Kg/ha, respectively Ectropis obliqua Prout 67,500 larvae/ha Lu and Lou (1989) Empoasca vitis (Göthe) 5.6 and 12 Individuals per 100 tea leaves for summer and autumn tea production season Zhu (1983) Euproctis pseudoconspera (1) For the annual made tea output of 2250 Kg/ha: 91,400, 32,700 and 163,900 larvae/ha for the 1st, 2nd and 3rd Ai and Zhao Strand generation, respectively(2) For the annual made tea output of 1500 Kg/ha: 73,100, 256,600 and 148,600 larvae ha for the (1997) 1st, 2nd and 3rd generation, respectively Myllocerinus aurolineatus 82,500, 123,000 and 165,000 adults/ha for tea fresh yield of 750, 1500 and 2250 Kg/ha, respectively Zhu and Shang Voss (1990) Mite pests Acaphylla theae Watt An average of 20 mites per leaf Zhang and Tan Brevipalpus obovatus An average of 10–15 mites per leaf (2004) Donnadieu Polyphagotarsonemus An average of more than 10 mites per leaf latus (Banks)

50–59% lethality, and a acaricide, propargite, had no toxicity to spi- (Göthe) (Huang and Wang, 2009; Zhou et al., 2011). The mixture ders. Yin and Hong (1989) reported that synthetic pyrethroids of botanical insecticides and mineral oil increased the effectiveness were safer than organophosphorus insecticides to pupae in coc- to tea pests (Liu, 2010). He showed that both mixtures, made by cons of Apanteles sp., and diflubenzuron was the safest with mixing 0.3% azadirachtin emulsion (diluted 500 times) and 0.3% 19.5% mortality among all tested insecticides. The wettable power matrine agent (diluted 500 times) with mineral oil diluted 300 of Verticillum lecanii (Zimm.) had no toxicity to the predatory mites times, respectively, were more effective to E. vitis (Göthe) and P. la- (Chen et al., 2001). The mixture of Bt (600 g/ha) and 10% imidaclo- tus (Banks) than mixtures of either of these two botanicals and prid WP (120 g/ha) was safer to spiders (Jiang et al., 2001). The Bt mineral oil alone. and EpNPV formulations were safe to two dominant parasitoids of Crystal lime sulphure (45%) is used to control scales and mites E. pseudoconspera Strand, namely, T. euproctidis Wilicox and A. con- during the overwintering season of tea production (Zhou et al., spersae Fiske. In contrast, chemical insecticides including cyhaoth- 2011). Insect growth regulators (IGRs) mimic insect hormones, rin, deltamelthrin, dichlorvos and isocarbophos, of which such as juvenile hormone and ecdysone, and thus interfere with dichlorvos was the most toxic, exerted adverse effects on these normal growth and development. They also have been used against two parasitoids at different levels (Ai et al., 2000a,b). Recently, some tea pests. For example, some ecdysone agonists such as dif- Chen et al. (2011b) indicated that several compounds, including lubenzuron, teflufenoxuron and buprofezin controlled E. vitis three insecticides, 25% thiamthoxam WG, 0.5% matrine and nico- (Göthe) (Zhang et al., 1992). However, many other groups of IGRs tine AS, 0.3% azadirachtin emulsion, and six other fungicides had may show promise in laboratory trials, but their efficacy and eco- little mortality on nymphs and eggs the predatory mite, N. cucume- nomics are yet to be evaluated against tea pests (Hazzrika et al., ris (Oudemans). 2009). Botanicals and their use in tea pest management have attracted growing attention in China. Some plant extracts possess significant antifeedant or toxic effects on selected tea pests (Wang et al., 2002; 5. Conclusions Chen et al., 2007c, 2009; Zhou et al., 2007). In laboratory studies, bishkatali (Polygonum hydropiper L.) extract (in95% ethanol) ex- Tea plantations serve as permanent habitats for 808 species of erted 52% mortality and 90% antifeedant effect on E. obliqua 3rd in- tea insect pests and more than 1100 species of natural enemies star larvae (Chen et al., 2007c). Extracts of the plume poppy of these pests. These include entomopathogens, nematodes, para- (Macleaya cordata (Willd.) R. Br.), prepared with 95% ethanol, also sitoids and predators, all of which were surveyed and identified showed high toxicity to larvae of E. obliqua Prout and E. pseudocon- nationally in the past five decades. Several dominant species of spersa Strand (Zhou et al., 2007). Similarly, 0.5% matrine agent was parasitoids, predators and a few pathogens suppress populations markedly toxic to E. obliqua Prout and E. vitis (Göthe) but not to Ira- of these pests under natural conditions. Great progress has been goides fasciata Moore. 0.5% veratridine solvent was also toxic to made in recent years toward better understanding of the biological these three lepidopteran species (Chen et al., 2009). The neem-seed and ecological characteristics of dominant natural enemies, and natural product 1.2% azadirachtin emulsion showed high but de- tritrophic interactions among tea plants, herbivores and parasit- layed action against E. obliqua Prout and significant effects on D. oids or predators. Aspects of biocontrol practices, such as protec- baibarana Mats. and A. theae Watt. In the field, Wang et al. tion and release of parasitoids and predators and dissemination (2002) managed three tea pests by applying 1.2% matrine agent of several specific entomopathogenic bioinsecticides such as EoN- in large scale. They obtained more than 95% control of E. obliqua PV and EpNPV have been implemented into modern tea pest man- Prout on the 3rd day after spraying (diluted 1000 times), and about agement systems. These advances were made in conjunction with 80% and 70% control to M. aurolineatus Voss and E. vitis (Göthe) host plant resistance, cultural practices, physical control methods, after spraying (diluted 500 times). use of selective insecticides and pest monitoring and forecasting Mineral oil is also recommended to control of tea pests. 99% techniques. To meet the increasing demands for contaminant-free mineral oil (Enspray) diluted 100–150 times resulted more than and safer tea and tea products, innovative studies on biocontrol 95% control of A. theae Watt, but unsatisfactory control to E. vitis techniques and other pest management tactics are sorely needed. 86 G.-Y. Ye et al. / Biological Control 68 (2014) 73–91

This is particularly important for obtaining formal organic certifi- The technology to genetically engineer tea cultivars with im- cation at the international level. proved economic traits, such as increased resistance to tea pests has been applied to other crop plants, particularly cotton. How- ever, wide-spread consumer resistance to genetically modified 6. An agenda for research and policy implementation crops makes research in this area a very risky commercial enter- prise. We do not recommend investments in genetic modifications About one third of the world’s tea is grown in China and Chinese in the current global marketplace. The situation may change in fu- tea exports exceed 300,000 tons. Tea is a high-value element of the ture and our recommendation will be re-visited. Chinese economy and investments into improving tea crop protec- Tea is extremely valuable for human consumption not only as tion will generate returns in terms of fiscal profitability, in terms of an everyday drink but also as a therapeutic aid in many illnesses. social benefits and in terms of China’s place in world-wide agricul- Protecting tea crops from insect and other arthropod pests with ture. In this final section, we set forth an agenda designed to move safer and greener control tactics has been and will continue to be tea pest control in China to the level of a global model. Our agenda challenging. Nonetheless, in view of the tremendous progress in re- identifies the most effectual research directions, it is understood search and implementation of conservation biological control that research in and of itself does not lead to the most profitable within the context of IPM through the last fifty years, we predict changes in agriculture. For that reason, we go beyond research acti- accelerating improvements over the next five decades. vates to address advisable policy directions. Microbial control of tea pests is now the most effective time-of- Acknowledgments need biological control tool available. While effective, substantial investments in research can yield even more substantial improve- This work was supported by grants from China National Science ments. First, it is essential to promote basic research on viral, bac- Fund for Innovative Research Groups of Biological Control (Grant terial and fungal pathogens and improve the efficacy and no. 31021003), and China National Science Fund for Distinguished sustainability of these biological control agents. Several insect Young Scholars (Grant no. 31025021). Mention of trade names or viruses can be improved via genetic engineering to enhance their commercial products in this article is solely for the purpose of pro- toxicity against tea pests, generate wider host ranges and express viding specific information and does not imply recommendation or faster rates of kill (Hu et al., 1993b, 1999; Leng et al., 2006; Ma endorsement by the U.S. Department of Agriculture. All programs et al., 2007; Tang et al., 2009). Mass production systems for insect and services of the U.S. Department of Agriculture are offered on viruses require improvement. Most viral species must be grown in a nondiscriminatory basis without regard to race, color, national insect hosts, which requires intense research into artificial diets origin, religion, sex, age, marital status, or handicap. and rearing systems to mass produce insect hosts for commer- cial-level viral production. Strains of Bt with much higher toxicity Appendix A. 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