Conservation biological control and IPM practices in Brassica vegetable crops in China

This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution

and sharing with colleagues.

Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third party

websites are prohibited.

In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further information

regarding Elsevier’s archiving and manuscript policies areencouraged to visit:

http://www.elsevier.com/authorsrights

Author's personal copy

Conservation biological control and IPM practices in Brassica vegetablecrops in China

Yin-Quan Liu a,⇑, Zu-Hua Shi a, Myron P. Zalucki b, Shu-Sheng Liu a

a Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, Chinab School of Biological Sciences, The University of Queensland, Brisbane 4072, Australia

h i g h l i g h t s

� Natural enemies of insect pests inbrassica vegetable crops arenumerous in China.� Major parasitoids have great potential

to suppress pest populations.� The role of natural enemies can be

promoted by the use of selectiveinsecticides.� The strategy of conservation

biological control can reduceinsecticide input.� Several successful brassica IPM

practices have enhanced conservationbiological control.

g r a p h i c a l a b s t r a c t

a r t i c l e i n f o

Article history:Available online 2 July 2013

Keywords:BrassicaBiological controlNatural enemiesCrop systemAction thresholdsConservation

a b s t r a c t

Brassicas are major vegetable crops in China but the systems for growing the crops are complex. During the last30 years, the area of vegetable crops has increased steadily, however, the control of insect pests on brassica veg-etables has largely relied on the heavy use of chemical insecticides, resulting in high levels of resistance, insec-ticide residues hazardous to human health and other serious consequences. Nevertheless, efforts to developpractical and sustainable integrated pest management (IPM) strategies for brassica vegetables have been imple-mented. Here we first review the work on surveys of natural enemies of insect pests in brassicas and describethe biology and ecology of a few important parasitoids. We then introduce the progress of conservation biolog-ical control by reviewing studies on evaluation of natural enemies and selective insecticides, the work on thedevelopment of action thresholds and some successful examples of IPM field trials at the cropping system level.The successful examples of IPM practices in brassicas show the great potential of conservation biologicalcontrolto reduce chemical pesticide input and improve vegetable production in the future.

� 2013 Elsevier Inc. All rights reserved.

1. Introduction

During the last 30 years, the area of vegetable cropping in Chinahas increased about 5.5-fold, reaching close to 18 million hectares

when calculated on an individual crop basis in 2008 (Fig. 1).Brassicas constitute the major group of vegetable crops in China.Depending on the region, the proportion of brassica accounts for30–45% of all vegetable crops. In 2008, the area of commoncabbage, Brassica oleracea var. capitata, Chinese cabbage, Brassicacampestris var. pekinensis, and pakchoi cabbage, Brassica campestrisvar. chinensis, the three main brassica crops in China was about

1049-9644/$ - see front matter � 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.biocontrol.2013.06.008

⇑ Corresponding author. Address: Institute of Insect Sciences, Zhejiang University,866 Yuhangtang Road, Hangzhou 310058, China.

E-mail address: [email protected] (Y.-Q. Liu).

Biological Control 68 (2014) 37–46

Contents lists available at SciVerse ScienceDirect

Biological Control

journal homepage: www.elsevier .com/locate /ybcon

Author's personal copy

4 million hectares, with products totaling about 150 million tons(China Agriculture Yearbook Editorial Committee, 2009).

Most brassica crops are grown by family-based small landhold-ers (<0.5 ha) around cities and in highlands, and some are grown inspecialized production areas. The crop systems are complex revol-ving around intercropping throughout the year. Different farmershave different habits of crop management, thus the ability in,and the level of crop management vary depending on the regionand the knowledge of the producers. An example is the vegetablecropping system in the Changjiang river valley as described byLiu and Yan (1998).

A complex of insect pests attacks brassica vegetable crops. Forexample, in the Changjiang river valley, the major pest species in-clude the diamondback moth (DBM), Plutella xylostella L. (Lepidop-tera: Plutellidae), the cabbage white butterfly, Pieris rapae L.(Lepidoptera: Pieridae), the cluster caterpillars, Spodoptera lituraFabricius (Lepidoptera: Noctuidae), the beet armyworm, Spodop-tera exigua Hübner (Lepidoptera: Noctuidae), the green peachaphid, Myzus persicae Sulzer (Hemiptera: Aphididae), and the tur-nip aphid Lipaphis erysimi Kaltenbach (Hemiptera: Aphididae) (Liet al., 2012; Liu and Yan, 1998; Zalucki et al., 2012). Other insectpests such as Mamestra brassicae L. (Lepidoptera: Noctuidae), Brev-icoryne brassicae L. (Hemiptera: Aphididae) and Phyllotreta striolataFabricius (Coleoptera: Chrysomelidae) may also cause seriousdamage occasionally in different regions (Liu et al., 1995). Since1990s, two invasive cryptic species of the whitefly Bemisia tabaciGennadius (Hemiptera: Aleyrodidae) complex have become com-mon pests in brassicas (De Barro et al., 2011; Zhang and Luo, 2001).

Although the negative effects of chemical pesticides, such asside effects on natural enemies, had been mentioned as early asthe 1950s (Han, 1956), the control of insect pests on brassica veg-etable crops has relied heavily on the use of chemical insecticidessince the 1970s. The regular overuse and misuse of chemical insec-ticides have had serious consequences of insecticide resistance, in-crease of pest control costs and insecticide residues hazardous tohuman health (Li et al., 2012; Liu et al., 2004a; Liu and Yan,1998). Due to increasing awareness on environmental protection

and food safety, biological control and integrated pest manage-ment (IPM) have received much attention since 1980s. Here wedocument the progress of conservation biological control andIPM practices in brassica vegetables in China.

2. Surveys and classification of natural enemies

The earliest study on natural enemies of brassica insect pests inChina was on two pupal parasitoids of P. rapae in the 1930s (Jin,1936). However, because of historical reasons, little research onbiological control in brassica crops was done until late 1970s,and research in this area has increased greatly since the 1980s,with most work focusing on surveys of natural enemies of the maininsect pests in brassica crops (Zhang and Liu, 1993).

There are many natural enemies of insect pests in brassica veg-etables (Table 1). Most surveys of natural enemies focus on parasit-oids and predatory arthropods, relatively few on pathogens,although pathogens as biological agents have been widely used.The main pathogens used to control pests include the well knownbacteria, Bacillus thuringiensis (Bt), nuclear polyhedrosis virus(NPV) and granulosis virus (GV) for lepidopterous pests, andentomopathogenic fungi of lepidopterous pests and aphids. Majorarthropod natural enemies of brassica pests are parasitic wasps,predatory beetles and spiders (Table 1). The insect pests sharemany of the natural enemy species, particularly generalist preda-tors. The relatively low number of predatory natural enemies ofS. exigua was likely an artifact of recording.

Depending on the region, the dominant natural enemies of insectpests in brassica vegetables vary (Table 2). For example, Cotesiaglomeratus (L.) is the dominant parasitoid of P. rapae in Shanghaiand Zhejiang, in the lower reaches of the Changjiang River (He et al.,1983; Hu, 1983). However, this wasp was found to exhibit very lowrates of parasitism of P. rapae in Shanxi, North-west of China whereanother parasitoid, C. rubecula Marshall dominates (Song et al., 1992).

3. Biological and ecological studies of major natural enemies

Studies on the biology and ecology have been conducted onmany of the species listed in Table 2. We review briefly the dataof the six species of parasitoids that have been studied in greatdetail.

3.1. Cotesia vestalis (Haliday) (Hymenoptera: Braconidae)

Cotesia vestalis, also well known as Cotesia (formerly Apanteles)plutellae, is a major solitary larval endoparasitoid of DBM (Ke andFang, 1982). It can parasitize larvae of all four instars of DBM,but prefers 2nd and 3rd instars. Superparasitism, host nutritionalstatus after parasitism, and the level of resistance to insecticidehad obvious effects on the biology of the parasitoid (Bai et al.,2005; Li et al., 2002, 2001). The parasitoid appears to regulate host

Year

Are

a (m

illio

n ha

)

Fig. 1. The annual area of vegetable crops in China.

Table 1Numbers of species of recorded natural enemies of major insect pests in brassica vegetable crops in China up to 2011.

Insectpests

Parasitic naturalenemies

Predatory naturalenemies

Pathogens Total Refs.

DBM 21 75 5 101 Huangfu et al. (2010), Li (1987), Liu (2001), Lv (1983), Wang et al. (1998), Wu et al.(1987), Wu and You (2002)

P. rapae 22 56 26 104 He et al. (1983), Hu (1983), Li (1987), Song et al. (1992), Wu et al. (1987), Zhao et al.(2005a, 1986)

S. litura 51 38 10 99 Chai et al. (2009), He et al. (2002a), Luo et al. (2004), Xie et al. (1999), Yang (1982)S. exigua 37 2 8 47 He et al. (2002b), Liu et al. (1990), Luo et al. (2004), Su (1997), Xu et al. (2001)Aphids 6 67 30 103 Liu et al. (1990), Lu et al. (1986), Wu et al. (1987), Yang (1982), Zhou et al. (2004)

38 Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46

Author's personal copy

growth and metabolic efficiency (Huang et al., 2008; Shi et al.,2002).

Plant volatiles influence host selection by C. vestalis. The para-sitoid parasitizes more host larvae on Chinese cabbage than oncommon cabbage. Volatiles from Chinese cabbage were moreattractive to C. vestalis than those from common cabbage (Liuand Jiang, 2003). However, an experience of searching coupledwith an oviposition in a host larva on a leaf of the common cabbagesignificantly increases the preference for parasitizing host larvaeon this plant (Liu and Jiang, 2003).

In Hangzhou, C. vestalis could complete up to 15 generations peryear at room temperature, and the parasitoid could overwinter atthe pre-pupal stage (Ke and Fang, 1982). A study on diapause indi-cated that photoperiod experienced during both the current andprevious generations as well as temperature of the current gener-ation all had significant effects on diapause incidence of the para-sitoid (Ahmed et al., 2007).

3.2. Oomyzus sokolowskii Kurdjumov (Hymenoptera: Eulophidae)

The eulophid parasitoid Oomyzus sokolowskii is a gregarious lar-val–pupal parasitoid of DBM. It is also a parasitoid of C. vestalis andthus a facultative hyperparasitoid of DBM (Liu and Wang, 1999; Liu

et al., 2000a). The parasitoid parasitizes all larval and pupal stagesbut exhibits a strong preference for larvae over prepupae or pupae,and does not show a preference among the larval instars. Thedevelopmental time, number and sex ratio of offspring per hostpupa, and successful parasitism do not differ significantly amongparasitoids reared from host larvae of different instars, indicatingsimilar host suitability between larvae of different instars (Liuand Wang, 1999; Wang et al., 1999).

In Hangzhou, O. sokolowskii is active in the field from April toOctober, and starts to over-winter as matured larvae or prepupaeinside the host in middle to late October (Liu et al., 2000b).

3.3. Diadromus collaris (Gravenhorst) (Hymenoptera: Ichneumonidae)

Diadromus collaris is a solitary pupal endoparasitoid of DBM.The performance of D. collaris is affected by host age. Female adultsprefer host pupae that are in the first half of their pupal develop-ment. Survival from larva to adult, and size and parasitizing capac-ity of the resultant female adults decrease dramatically as hostpupal age increases. When eggs are laid into host pupae that arein the last quarter of their development, all parasitoids die beforeadult emergence (Wang and Liu, 2002).

Table 2The dominant arthropod natural enemies of insect pests in brassica vegetable crops and their known distributions in China. Parasitoids based on many records and predatorsbased on field observation (1) and/or lab feeding (2).

Natural enemy Target pests Location of surveya Refs.

ParasitoidsEgg parasitoidsTrichogramma confusum P. xylostella Guangdong (Shenzhen) He and Pang (2000)Trichogramma confusum S. litura Jiangxi Yang (1982)Trichogramma evanescens P. rapae Shanxi Song et al. (1992)Larval parasitoidsCotesia vestalis P. xylostella Zhejiang (Hangzhou, Wenzhou,

Ningbo), Fujian (Fuzhou), Hubei,Henan (Zhengzhou), Guangxi(Nanning)

Huangfu et al. (2010), Liu et al.(2000a), Lv (1983), Tang et al. (2007),Wang et al. (2003), Wu and You(2002), Xu et al. (2003)

Diadegma semiclausum P. xylostella Yunnan, Henan (Zhengzhou) Chen et al. (2003), Tang et al. (2007)Cotesia glomeratus P. rapae Shanghai, Zhejiang (Hangzhou) He et al. (1983), Hu (1983)Cotesia rubcula P. rapae Shanxi Song et al. (1992)Snellenius manilae, Microplitis sp, Meteorus pulchricornis S. litura Zhejiang (Ningbo) Chai et al. (2009)Campeletis chlorideae S. litura Zhejiang (Ningbo), Jiangxi Chai et al. (2009), Yang (1982)

Larval–pupal parasitoidOomyzus sokolowskii P. xylostella Zhejiang (Hangzhou, Wenzhou,

Ningbo), Fujian (Fuzhou), JiangxiHuangfu et al. (2010), Liu et al.(2000a), Wu and You (2002), Xu et al.(2003), Yang (1982)

Pupal parasitoidsDiadromus collarsis P. xylostella Zhejiang (Hangzhou) Liu et al. (2000a)Pteromalus glomeratus P. rapae Shanghai, Zhejiang (Hangzhou),

JiangxiHe et al. (1983), Hu (1983), Yang(1982)

Metapius rufusr S. litura Jiangxi Yang (1982)Nymph and adult parasitoidsDiaeretiella rapae Aphids Qinghai (Xining), Zhejiang

(Hangzhou), Guangdong (Shenzhen),Jiangxi

Li (1997), Liu et al. (1990), Yang(1982), Zhou et al. (2004)

Aphidius gifuensis M. persicae, L.erysimi

Jiangsu (Yangzhou), Beijing, Zhejiang(Hangzhou), Guangdong (Shenzhen),

Liu et al. (1990), Lu et al. (1986), Shiet al. (1992), Zhou et al. (2004)

PredatorsErigonidium graminicolum P. xylostella Fujian (Fuzhou), Hubei (Huangzhou) Lv (1983) (1,2), Wu et al. (2003)(1,2)Lycosa pseudoannulata P. xylostella Hubei (Huangzhou) Lv (1983) (1,2)Lycosa pseudoannulata P. xylostella Fujian (Fuzhou) Wu et al. (2003) (2)Coccinella septempunctata L., Harmonia axyridis (Pallas), Propylaea

japonica (Thungberg)P. xylostella Hubei (Huangzhou) Lv (1983) (1,2)

Theridion octomaculatum P. xylostella Hubei (Huangzhou), Fujian (Fuzhou) Lv (1983) (1), Wu and You (2002) (1)Oedothorax insecticeps Boes. Et Str. P. xylostella Fujian (Fuzhou) Wu et al. (2003) (1,2)Sitticus sinensis Schenkel, Theridion(um) octomaculatum P. rapae Anhui (Hefei) Zhao et al. (2005a) (1,2)Menochilus sexmaculata, Episyrphus balteatus M. persicae, L.

erysimiGuangdong (Shenzhen) Zhou et al. (2004) (1)

a Names of provinces and the localities within the province are shown in parentheses.

Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46 39

Author's personal copy

Experiments were performed in Hangzhou to compare repro-ductive compatibility and variation of two geographic populationsof D. collaris, one from Hangzhou, Zhejiang and the other fromLishan, Taiwan. The results indicated complete reproductive com-patibility between the two populations (Liu et al., 2002). The pop-ulation from Hangzhou achieves higher rates of survival at hightemperatures, probably as a result of long-term adaptation to localclimates, and has higher proportions of female progeny at sometemperatures (Liu et al., 2002). A population of this parasitoidintroduced from Malaysia shows similar development time andhost age preference as the Hangzhou population (Zhang et al.,1998).

3.4. Diadegma semiclausum (Hellen) (Hymenoptera: Ichneumonidae)

Diadegma semiclausum is another important larval endoparasi-toid of DBM, particularly in areas with mild temperatures (Liuet al., 2004b; Wang et al., 2004). In the late 1990s D. semiclausumwas introduced to Yunnan province of southwest China, and estab-lished successfully (Chen et al., 2003). However, subsequently thenatural, wide distribution of this species in northern China wasdocumented (Liu et al., 2004b).

Host age has significant effects on the biological characteristicsof D. semiclausum. Individuals initiated parasitism in the 4th instarhost larvae have shorter developmental time and produce more fe-male progeny than those initiated in 2nd and 3rd instar host larvae(Cai et al., 2006; Yuan and Li, 2008). Moreover, females with lessintraspecific competition and at relatively low temperatures pro-duce more female progeny (Yuan and Li, 2008).

3.5. Cotesia glomeratus (L.) (Hymenoptera: Braconidae)

Cotesia glomeratus is a gregarious larval endoparasitoid of P. ra-pae (Yang et al., 1982). This parasitoid prefers to parasitize 2nd and3rd instar larvae. Parasitized host larvae consume the sameamount of leaves in the first three instars as that of unparasitizedlarvae; however, food consumption of parasitized larvae in the 4thinstar decreases sharply compared to unparasitized larvae. Provi-sion of honey solution to the adult wasps can substantially increasetheir longevity (Wang et al., 2005; Yang et al., 1982).

The parasitoid over-winters as mature larvae in cocoons. Thereare 11 generations a year at room temperature in Shanghai, how-ever, only 4 generations a year are reported in the field in Chang-sha, Hunan province (He et al., 1986; Wang et al., 2005).

3.6. Pteromalus puparum L. (Hymenoptera: Pteromalidae)

Pteromalus puparum is a gregarious pupal parasitoid of P. rapae.Usually one to two eclosion holes are found in one P. rapae pupa,sometime 3–4 holes can be seen. Both males and females can matewith different individuals many times (Xiao, 1984; Yin and Wang,1997). The parasitoid prefers to parasitize prepupae and early stagepupae of P. rapae. Number of offspring per host pupa varies from 21to 60 (Yin, 1992).

This parasitoid over-winters as mature larvae inside the pupaeof P. rapae. At room temperature the parasitoid passes 13 genera-tions in Xinyang, Henan province and Hangzhou, Zhejiang prov-ince, and 11 generations in Guiyang, Guizhou province (Hu,1984; Xiao, 1984; Yin and Wang, 1997).

4. Conservation biological control in the development andimplementation of IPM

As seen above, research on insect pests in brassica vegetableshas long been a main field of vegetable entomology in China. In a

bibliography of insects associated with vegetable crops in China,compiled by Zhang and Liu (1993), about 50% of publications dealtwith insects on crucifers (mainly brassicas). As the authors pointedout, the high proportion of publications related to insects in cruci-fers reflected both the significance of crucifer vegetables and theimportant effects of insect pests. However, based on this bibliogra-phy, there was little literature at that time on brassica IPM at thecropping system level, although an extensive literature existedon particular species. This situation has been improved recentlywith some long-term, quantitative field studies of brassica IPM atthe cropping system levels having been reported. We first intro-duce the research on evaluation of arthropod natural enemiesand selective insecticides, and then introduce the development ofaction thresholds and IPM field trials.

4.1. Evaluation of arthropod natural enemies

4.1.1. Natural enemies of DBMThe selection of effective species and strains of Trichogramma

and Trichogrammatoidea showed that Trichogramma confusum Vig-giani (=T. chilonis Ishii), T. pretiosum Riley, and Trichogrammatoideabactrae Nagaraja were suitable candidates for control of DBM inChina (Guo et al., 1999; He et al., 2001). The rate of parasitizationby the local T. confusum could reach 30–35% in Shenzhen, Guang-dong province (He and Pang, 2000; Zhang and Pang, 1995). In com-parison with T. confusum, the introduced T. pretiosum had a highercompetitive capacity and could parasitize DBM eggs of a wider agerange in laboratory tests (He et al., 2005). Recently, another Tricho-gramma species, T. ostriniae Pang et Chen, was found dominant inparasitism of DBM eggs in crucifer-corn fields, where this parasit-oid had a higher parasitism rate than T. confusum (Chen et al.,2006).

Despite the wide distribution of T. confusum, the parasitism ofDBM eggs was very low in some areas, such as Hangzhou suburb(Liu et al., 2000a). However, high overall rates of parasitism ofDBM in Hangzhou suburb could be attained because of the roleof larval and pupal parasitoids, such as C. vestalis, O. sokolowskiiand D. collaris. In the field, the rates of parasitism were usually10–60% during peaks and reached 80% on a few occasions (Keand Fang, 1982; Liu et al., 2000a). The natural parasitism rate ofthe introduced parasitoid, D. semiclausum, could reach 75% in thefield in Yunnan province (Chen et al., 2003). Investigation in otherregions including Fuzhou, Wenzhou and Ningbo, Huanggang andZhengzhou indicated that the natural parasitism rate varied from10% to 70%, and was mainly caused by C. vestalis and O. sokolowskii(Huangfu et al., 2010; Lv, 1983; Tang et al., 2007; Wu and You,2002; Xu et al., 2003).

Because the main parasitoids of DBM, C. vestalis, D. semiclausum,O. sokolowskii and D. collaris are sympatric species, interactions andcompetition are inevitable and have been extensively investigated.

4.1.1.1. Cotesia vestalis vs. Oomyzus sokolowskii. Competition exper-iments reveal that C. vestalis is a stronger competitor than O. soko-lowskii and both physical attack and physiological suppressionwere involved in the competition between the two endoparasitoids(Bai et al., 2011; Li et al., 2004; Shi et al., 2003b). Usually O. soko-lowskii prefers to parasitize unparasitized DBM larvae, however, O.sokolowskii can oviposit into old larvae of C. vestalis and completetheir development (Li et al., 2004). Despite the competition, the to-tal parasitism of DBM larvae was higher when both parasitoidswere present than when either of them alone (Shi et al., 2003b).

4.1.1.2. Diadegma semiclausum vs. Oomyzus sokolowskii. Multipleparasitism and competition for food resource occur between D.semiclausum and O. sokolowskii. Depending on the order and time

40 Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46

Author's personal copy

lag of oviposition by the two parasitoids, the outcome of interspe-cific competition varies (Shi et al., 2003a).

4.1.1.3. Cotesia vestalis vs. Diadegma semiclausum. Cotesia vestalislarva has an obvious advantage over D. semiclausum in interspecificcompetition; however, the adult females of D. semiclausum aremore effective at detecting and parasitizing the hosts. The totalparasitism by the two parasitoids is similar to, or higher than thatby one of the parasitoids alone (Shi et al., 2004b; Wang and Keller,2002).

4.1.1.4. Diadromus collaris vs. Oomyzus sokolowskii. Females of D.collaris can discriminate pupae already parasitized by O. sokolow-skii. Although they insert their ovipositor into the host pupae al-ready parasitized by O. sokolowskii at a similar frequency as intounparasitized host pupae, they do not lay eggs inside the parasi-tised hosts (Liu et al., 2001). The combined rate of parasitism bythe two parasitoids is higher than that by one of the parasitoidsalone (Shi et al., 2001).

Most predatory natural enemies of DBM are spiders, ladybirdbeetles and carabid beetles, and at least 75 species have been re-corded in China (Table 1; Liu, 2001; Lv, 1983). However, relativelyfewer studies have been conducted on these predators comparedto parasitic natural enemies of DBM. One possible reason is thatcompared to study on parasitism it is more difficult to collect directevidence of predation and show its effects on pest population (Fur-long and Zalucki, 2010). To date, most work on predatory naturalenemies of DBM has been on their functional response in the lab-oratory and factors influencing potential field predation (Li et al.,2008; Liu, 2001; Lv, 1983; Wu et al., 2003).

4.1.2. Natural enemies of P. rapaeThe parasitism of P. rapae eggs in most parts of China is low, but

in Shanxi province 33–46% parasitism was recorded in summer,mainly by Trichogramma evanescens Westwood (Hu, 1983; Songet al., 1992; Zhao et al., 1986). From 1978 to 1982, a large scalefield survey on parasitoids of P. rapae was carried out; C. glomeratusand P. puparum in East China, C. rubecula and P. puparum in NorthChina, C. rubecula and Phryxe vulgaris Fallen in Northeast China,and P. puparum in South China were found as the main species oflarval and pupal parasitoids of P. rapae, based on field parasitismrates (He et al., 1983; Hu, 1983; Zhao et al., 1986). However, thevariation of parasitization percentage was large at different periodsand places, ranging from 0% to 86% for larvae and 0% to 97% for pu-pae respectively. Circumstantial evidence suggests that in manycases frequent use of chemical pesticides may have reduced para-sitoid populations and consequently parasitism of P. rapae in thefield (He et al., 1983, 1986; Hu, 1983; Lin et al., 1998; Song et al.,1992; Wang et al., 2005; Xiao, 1984; Yin and Wang, 1997; Zhaoet al., 1986).

Few studies focus on the predatory natural enemies of P. rapae.Several species of spiders and a beetle, Paederus fuscipes Curtis,show high rates of predation on eggs of P. rapae in the laboratory(Zhang et al., 2006; Zhao et al., 2005a).

4.1.3. Natural enemies of Spodoptera sppSpodoptera litura and S. exigua are polyphagous pests. They have

become more harmful in brassica and other vegetable crops sincelate 1980s and the high resistance to insecticides is one of theimportant reasons (Lin et al., 2007; Luo et al., 2000; Zhou andHuang, 2002).

Major parasitoids of S. litura and S. exigua have been investi-gated and their potential efficacy of pest control assessed in severalplaces. In Guangzhou, a braconid, Microplitis sp., is the dominantparasitoid of S. litura and the average rate of parasitism was 14%in 1979, with the highest rate of parasitism at 48% in November

(Xu and Yang, 1983). In Ningbo, larvae of S. litura were parasitizedmainly by another braconid, Snellenius manilae (Ashmead), thehigher rate of parasitism in September varied from 17% to 32% inbrassica vegetables (Chai et al., 2009).

The braconid Microplitis tuberculiter Wesmael can parasitize theyoung larvae of S. exigua and the highest level of parasitism rangedfrom 20% to 30% in Hebei province (Qu et al., 2004). In a field of aShanghai suburb, the highest rate of parasitism of S. exigua was 48%by another braconid species, Microplitis pallidipes Szepligeti (Zenget al., 2005). In Guangzhou, the rate of parasitism in S. exigua larvaeby S. manilae reached approximately 30% (Sun and Huang, 2010).Laboratory experiments showed that the 2nd instar larvae of S.litura and S. exigua were the best hosts for S. manilae as measuredby fecundity and adult longevity of the parasitoid (Qiu and Tang,2010).

The braconid Meteorus pulchricornis (Wesmael) is also animportant endoparasitoid of S. litura and S. exigua, however, fieldsurveys of this species are mainly from soybean fields (Chaiet al., 2009; Liu and Li, 2006).

Predators were shown to have a strong influence on abundanceof S. litura (Jiang et al., 1999). However, complex interactions occuramong predators. For example, the predatory bug Cantheconideafurcellate Wolff, and two spider species, Erigone graminicolum(Sundvall) and Pirata subpiraticus Boes. et Str. are three sympatricpredators of S. litura in Shenzhen. It was shown in the laboratorythat P. subpiraticus would kill E. graminicolum and C. furcellatewhen coexisting, while E. graminicolum and C. furcellate could pro-mote each other and increase the predation rate (Jiang and Liang,2001).

4.1.4. Natural enemies of aphidsAphidius gifuensis Ashmead and Diaeretiella rapae M’Intosh are

two major endoparasitoids of aphids on brassica. Both of themare distributed widely in China, although A. gifuensis has betteradaptability to low temperature than D. rapae (Zhang, 1992). Aphi-dius gifuensis can parasitise M. persicae and L. erysimi, while D. ra-pae can parasitize all three species of aphids on brassica butprefers M. persicae and L. erysimi (Lu et al., 1992). Both parasitoidscan attack nymphs and adults. When 1st or 2nd instar nymphs areparasitized, no progeny can be produced by aphids; aphids at-tacked at later stages can produce progeny and the intrinsic rateof increase achieved by an aphid cohort increases rapidly as theage of the initial parasitization increases (Liu, 1990; Lu et al.,1992). In the field, rates of parasitism of aphids on brassica cropsare generally low but can reach over 30% during peaks (Li, 1997;Liu et al., 1990; Lu et al., 1986).

Predators of aphids on brassica crops are many. To date, atleast 15 species of predators have been tested for their predatoryfunctional responses to aphids in the laboratory. The predatorstested include: E. graminicolum, Pardosa astrigera Koch, Menochilussexmaculatus (Fabricius), Coccinella septempunctata L., Harmoniaaxyridis (Pallas), Propylaea japonica (Thungberg), Stenus sp., Paede-rus fuscipes Curtis, Stenus cicindela Sharp, Calathus halenisis Schall.,Epistrophe balteata De Geer, Metasyrphus corollae Fabricius, Scaevapyrastri (L.), Sphaerophoria memthastri L., and Aphidoletes aph-idimyza Rondani. Nearly all the functional responses belonged toHolling type II. Among the predators, the average numbers ofpreys eaten are high for ladybird beetles and syrphid flies, andlow for spiders and staphylinids. However, the spiders are stillimportant predators in brassica fields because of their large num-ber. Some of the ladybird beetles such as C. septempunctata and H.axyridis have been well studied and their mass rearing and utili-zation has been improved greatly (Sun and Wan, 2000; Wanget al., 2007).

Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46 41

Author's personal copy

4.2. Evaluation of biological and selective insecticides

Laboratory and field evaluation of many biological and chemicalinsecticides have been conducted against the main insect pests andtheir natural enemies. A number of Bt and NPV products such as S.litura NPV (SlNPV) and S. exigua multicapsid NPV (SeMNPV) wereshown to have high efficacy in killing the target pests without di-rect side effects on the beneficials (Luo et al., 2005; Shi et al.,2004a; Wang et al., 2010, 2009; Wu and Jiang, 2004). Other insec-ticides showing selectivity include: abamectin, avermectin, spino-sad, chlorfluazuron and chlorfenapyr against lepidopterous pests,and abamectin, acetamiprid, and imidacloprid against aphids(Guo et al., 2003; Li and Liu, 2005; Wang and Shen, 2002; Yinet al., 2005).

Host resistance to insecticides provides survival opportunityfor parasitoids developing inside the host, although the insecti-cide could reach the parasitoid larvae through penetration ofcuticle and/or feeding of host hemolymph by the parasitoid lar-vae (Li et al., 2006). Host resistance favors selection of resistancein the parasitoid and parasitoid resistance to insecticide could bepromoted by integrating resistance of hosts. For example, labora-tory selection of insecticide resistance in the parasitoid C. vestalisdemonstrated that selection with more resistant host larvae ofDBM could accelerate development of resistance to the insecti-cide fenvalerate and spinosad respectively (Liu et al., 2003,2007).

4.3. Development of action thresholds

Damage relationships by various insect pests have been as-sessed by artificial defoliation and natural infestation of plants.Field trials have demonstrated that common cabbage and cauli-flower could endure some defoliation without reduction of headweight at harvest, but the level of compensation varied withthe growth stage being attacked (Chen et al., 2002; Zhao et al.,2005b; Zhu et al., 1994). There was evidence of over-compensa-tion for defoliation at the pre-heading stage of common cabbage.However, the plants were more sensitive to defoliation at thecupping stage. For example, 12.5% defoliation of common cabbage(cultivar Jing-Feng No.1) at the pre-heading, cupping and headingstages respectively resulted in mean head weights at harvest 9.8%heavier, 4.3% lighter and 3.3% heavier than undamaged controls(Chen et al., 2002; Liu et al., 2004a). These data were invaluablein developing action thresholds for practical application (Liuet al., 2004a). Of particular value was the characterization of cropgrowth stages sensitive to insect damage. The sensitivity of com-mon cabbage to aphids at different growth stage was also testedin field trials. These trials verified that the seedling and cuppingstage were more sensitive to aphid damage (Chen et al., 2000;Zhang et al., 1999). Thus, farmers and extension officers wereasked to monitor insect pests more closely at both the seedlingand cupping stages.

Studies on action thresholds before 1990s were mostly based onone species and thereafter composite and dynamic action thresh-olds were established and used to manage lepidopterous pest com-plex on brassica crops (Zhou et al., 1996; Zhu et al., 1994). Furtherefforts were made to make the action thresholds more practicaland easier to apply by farmers and extension officers based on sev-eral field trials (Liu et al., 2004a; Zhang et al., 1999). This simplecomposite and dynamic action threshold was then used to reducepesticide application and promote activities of natural enemies(Lin et al., 2002; Yu et al., 2002). The same principle has been ap-plied to IPM trials in the Democratic People’s Republic of Korea(Furlong et al., 2008; Hamilton et al., 2009), Australia (Furlonget al., 2004) and the South Pacific (MJ Furlong, pers comm).

4.4. IPM field trials

As mentioned above, a great deal of research effort has focusedon individual species, and some aspects of the major pests andtheir natural enemies have been well studied. These studies pro-vide important information for the development of brassica IPM.However, much more work was needed for the development ofimplementation of practical brassica IPM at the crop system level.This has been explored in several regions in China with some pro-gress and success.

Since the 1980s, the use of selective insecticides, strategic rota-tion of different groups of insecticides, yellow sticky traps for alateaphids in seedling stage, and cultivation of early season cultivarshave been implemented for the control of insect pests on brassicasin the suburbs of Beijing (Wu, 1997). Evaluation of this IPM systemshowed that it resulted in effective control of the insect pests andsome reduction of insecticide input (Zhang et al., 1996; Zhu et al.,1992).

Field trials of IPM in brassica crops were conducted in southernChina in 1990s with a focus on promotion of cultural and biologicalcontrol methods. Using a population life-system approach, fieldevaluation of various ecological measures showed that each factorsuch as Bt, Plutella xylostella GV (PxGV), T. confusum, and sex pher-omone traps could have good control on DBM, but the use of singlefactors could not suppress the DBM population below the eco-nomic threshold (Liang and Pang, 1996; Xian et al., 1997). Ecolog-ical measures, developed through the integration of several factors,were effective in suppressing DBM populations and increasing thespecies diversity and population abundance of natural enemies(Table 3; Zhong et al., 2005, 2002). Meanwhile, the pesticides inputwas reduced by 44–51% and the product yield increased by 4–7%(Zhong et al., 2005).

Brassica IPM practice in the Changjiang river valley was largelypromoted by a joint project between China and Australia. Theobjective of the joint project was to develop and implement sound,sustainable brassica IPM strategies that significantly reduce pesti-cide hazards, and were acceptable to growers in the Changjiangriver valley, China and Queensland, Australia (Liu et al., 2004a;Liu and Yan, 1998). From the beginning of the project in 1995, allgroups of stakeholders and particularly farmers and extension staffwere involved in problem definition, setting priority needs and ac-tion plans. The strategy, to have farmers and extension staff in-volved from the beginning, proved successful in both improvingfarmers’ attitudes towards IPM and the implementation of IPMmethods in both China and Australia (Liu and Qiu, 2001; Liu andYan, 1998; Zalucki, 2007).

Using findings of the China–Australia joint project and informa-tion from literature, management strategies were formulated andtested in the field to evaluate the effects of different control meth-ods on populations of pests and natural enemies and to developpractical IPM guidelines. The major components in the IPM strat-egy included use of action thresholds in decision-making and stra-tegic use of biological and selective insecticides (Liu et al., 2005,2004a; Zhang et al., 1999). A field trial with a crop of approxi-mately one hectare was divided into an IPM plot and a conven-tional strategy plot, then regular sampling was conductedthroughout the whole season and pest control action was takenaccording to the guidelines developed. At the end of each trial, cropyield and quality, input of insecticides and the parasitism rates ofkey insect pests and abundance of natural enemies in differentplots were compared (Table 4; Liu et al., 2005, 2004a). Field IPMtrials with common cabbage were conducted in Hangzhou from1996 to 2000 and, in 2000, trials were conducted at five sites inZhejiang and Shanghai (Lin et al., 2002; Liu et al., 2004a; Yuet al., 2002; Zhang et al., 1999). In 2001 and 2002, field IPM trialswith cauliflower, broccoli or Chinese cabbage were conducted at

42 Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46

Author's personal copy

three sites in Zhejiang and Shanghai (Liu et al., 2005). The resultsfrom all the field trials showed that biological and selective insec-ticides could offer effective control of all the insect pests and thatthe activities of natural enemies were promoted. Compared withconventional practice, IPM practice could reduce insecticide inputby 20–70%, with no risk of crop loss (Liu et al., 2005, 2004a). More-over, the abundance of ground dwelling predators in field trialswith IPM strategy is significantly higher than that in conventionaltreatment (Table 4). The strategy to perform field trials in severallocations the same year and run several crop seasons in the samesite helped to test the validity of the new IPM guidelines, althoughthe apparent effects of natural enemies usually occurred later in acrop season probably because of the small field plots (Liu et al.,2005). Similar and very dramatic results were observed in Australiawhere the experiments were conducted on farms of 30–50 hect-ares each (Furlong et al., 2004).

4.5. Implementation

Implementation activities included grower involvement in fieldtrials, field days and participatory workshops, frequent dissemina-tion of fact sheets, as well as short training courses for extensionofficers and growers (Liu et al., 2004a). There was substantialimprovement in farmers’ knowledge, attitude and approaches to-wards IPM (Liu and Qiu, 2001). For example, an independent eval-uation on the joint project between China and Australia indicatedthat growers in the project areas had more frequent contact withextension officers than growers in the non-project areas; by2001, 36% of the growers in the project areas conducted regularsampling of insect pests and usually tried to use biological or selec-tive insecticides, compared with only about 20% in the non-projectareas (Liu and Qiu, 2001). An extensive survey by the agriculturaldepartments in Zhejiang and Shanghai in late 2002 showed thatin 10 major, project-associated production areas, which involvedsome 50,000 farming families and produced some 2 million tonsof brassica vegetables in a year, input of chemical insecticideswas reduced by 30–60% in a period of five years. Incidence of

pesticide residues exceeding the legally allowed level on brassicavegetables from August to October (the season when insecticideswere mostly applied) was reduced steadily from 20–40% in themid 1990s to 0–10% (0% in the central project areas) in 2002 (Liuet al., 2005).

5. Conclusion and discussion

A successful IPM program usually requires some conditionssuch as a relatively simple ecosystem, strong research and exten-sion capacity, and stable markets (Morse and Buhler, 1997). Inthe complicated vegetable ecosystems in China, it is hard to devel-op and implement a brassica IPM program in all locations and sea-sons. Although brassica IPM practice has achieved considerableprogress in several regions in China, serious challenges remainfor the development and implementation of IPM (Li et al., 2012;Liu et al., 2004a; Liu and Yan, 1998).

In the Changjiang river valley, field trials were mostly con-ducted for a single season on a rather small scale, using plots with-in the same field, although extensive effort was made to repeat thesame trials in different locations and years (Lin et al., 2002; Liuet al., 2004a,b; Yu et al., 2002; Zhang et al., 1999). In such circum-stances movement of natural enemies between treatments canconfound results and the effectiveness of the natural enemy com-plex at the agro-ecosystem or landscape level cannot be fully ad-dressed. Besides, to make an IPM package acceptable, themethods should be as simple as possible, particularly the use ofmonitoring and action thresholds. This inevitably will requirewell-designed field trials across several seasons to achieve a prac-tical and reliable IPM practice.

For the implementation of IPM, several technical, financial, edu-cational, marketing/social and organizational obstacles are listedby Wearing (1988). Liu and Yan (1998) discussed these obstaclesin China in detail. These obstacles still remain today. For example,there is a high ratio of chemical sales personnel, distributors andadvisers to IPM extension workers in China and the voice of chem-ical-oriented advice is usually stronger than IPM-oriented advice

Table 3Examples of diversity and abundance of natural enemies in field trials treated with different pest control strategiesa (IPM or Conventional (Con)) in Dongguan, China, April–December 1998b.

Major groups of natural enemies Brassica campestris cv. 49dCaixin

Brassica juncea Brassica campestris cv. 80dCaixin

IPM Con IPM Con IPM Con

Predatory insects (Carabidae, Coccinellidae, Straphylinidae, Miridae, Formicidae, etc.) 17 (24) c 10 (20) 21 (71) 13 (56) 14 (48) 10 (20)Parasitoids (Braconidae, Oomyzus, etc.) 4 (9) 2 (5) 9 (54) 4 (38) 3 (6) 2 (5)Spiders (E. graminicola, Araneidae, Theridiidae, etc.) 10 (63) 6 (9) 9 (209) 8 (26) 7 (58) 6 (9)Total 31 (96) 18 (34) 39 (334) 25 (120) 24 (112) 18 (34)

a In the IPM treatment, ecological measures of biological and selective insecticides (Bt, avermectin etc.), T. confusum, and sex pheromone traps of DBM were used; while inthe conventional treatment, calendar sprays of broad-spectrum chemical insecticides was carried out.

b Data in this table were based on the report of Zhong et al. (2002) and were reorganized. Data were collected using a range of sampling methods including counting onplants, light trapping and insect net sweeping depending on the groups of natural enemies.

c Number of species of natural enemies and the number of individuals are shown in parentheses.

Table 4Examples of abundance of ground dwelling predators shown by pitfall trapping in field trials treated with different pest control strategies a (IPM or Conventional (Con)) inHangzhou, China, in autumn 2000 and autumn 2001.

Major presumed ground dwelling predators 2000 (cabbage)b 2001 (broccoli)b

IPM Con IPM Con

Spiders (Lycosidae, E. graminicola, etc.) 6.7a 3.0b 13.7a 5.7bColeoptera (Carabidae, Straphylinidae, etc.) 22.0a 3.0b 15.0a 3.7b

a In the IPM treatment, action thresholds was used, and biological and selective insecticides were applied; while in the conventional treatment, typical practice by farmerswas simulated, or farmer’s practice (basically calendar sprays with mixtures of broad-spectrum chemical insecticides) was recorded.

b Figures are means of three replicates, and figures in the same row of the same year followed by different letters differ significantly (p < 0.05, Student-t test).

Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46 43

Author's personal copy

(Liu and Yan, 1998). Another obstacle is the lack of trained farmers.In the past 20 years, a large number of young farmers have movedto cities for temporary jobs, and only the less-trained elderly andwomen are left home for farming.

Challenges present opportunities to change. The abuse of pesti-cides has resulted in serious food safety problem since the mid1980s and become a threat to human health. Consumer aversionto pesticide residues and increasing demands for food safety hasbeen major forces driving implementation of IPM in vegetablesin China. Monitoring of pesticide residue has increased in bothdomestic vegetable supplies and international trade. Meanwhile,as the standard for living improves, many consumers are preparedto pay a slightly higher price for ‘green and clean’ vegetables(Wang, 1992). The ‘organic vegetables’, on which input of chemicalproducts are forbidden, has become a growing market from thenew century in China, particularly for well-paid ‘white collar’ con-sumers (Du et al., 2010; Yu, 2003). This will certainly provideopportunities for biological control of insect pests on brassicacrops. Accordingly, besides the removal of chemical pesticides,the effects of providing supplementary resources such as nectarsubsidies and habitat manipulation should be investigated to en-hance the efficiency of natural enemies. The reviews on the life his-tory traits of the major natural enemies in this article indicate asubstantial scope for enhancing conservational biological controlin the years to come.

Opportunities also come from the increase of support for re-search and extension, development of better organized farming,and policy and legislation support in China (Liu and Yan, 1998).Since the mid 2000s, the financial support for research and exten-sion has increased steadily in agriculture, and some major projectson biological control have been initiated recently. Policies relatingto land use in the new century have been changing gradually. Theleasing of land is encouraged for better farming, which certainlywill favor IPM implementation as large farms may make morecommitments to practice IPM.

In general, the successful examples of current IPM practices inbrassicas show a great potential for conservation biological controlto reduce chemical pesticide input. Further ecological measuressuch as habitat manipulation and landscape management shouldbe integrated to promote conservation biological control, and ulti-mately to implement better IPM strategies and improve vegetableproduction.

Acknowledgments

This paper was financially supported by China Agriculture Re-search System (CARS-25-B-08) and the National Natural ScienceFoundation of China (31021003). We thank the Australian Centrefor International Agriculture Research for support to China-Austra-lia joint Brassica IPM projects from 1995 to 2006 (ACIAR CS/1992/013; ACIAR CS2/1998/089; ACIAR Hort/2002/016). We also thanktwo anonymous referees for their helpful comments andsuggestions.

References

Ahmed, U.A.M., Shi, Z.H., Guo, Y.L., Zou, X.F., Hao, Z.P., Pang, S.T., 2007. Maternalphotoperiod effect on and geographic variation of diapause incidence in Cotesiaplutellae (Hymenoptera: Braconidae) from China. Appl. Entomol. Zool. 42, 383–389.

Bai, S.F., Chen, X.X., Cheng, J.A., Fu, W.J., He, J.H., 2005. Effects of host age at the timeof ovipositiion, superparasitism and host starvation after parasitism on thegrowth of Cotesia plutellae larvae and their teratocytes. Acta Entomol. Sinica 48,331–336.

Bai, S.F., Li, X., Chen, X.X., Cheng, J.A., He, J.H., 2011. Interspecific competitionbetween two endoparasitoids Cotesia vestalis (Hymenoptera: Braconidae) andOomyzus sokolowskii (Hymenoptera: Eulophidae). Arch. Insect Biochem. Physiol.76, 156–167.

Cai, X., Hao, Z.P., Shi, Z.H., Chen, X.X., 2006. The effect of host age on biologicalcharacteristics of Diadegma semiclausum. Chin. J. Biol. Control 22, 92–95.

Chai, W.G., Chai, H.F., Huangfu, W.G., Gao, M.Q., Wu, Q., Sun, M.M., Chen, J.H., Chen,R.X., Chen, X.X., 2009. Hymenopteran parasitoids of the common cutwormSpodoptera litura Fabricius larvae in Ningbo, China. Entomol. J. East China 18,30–34.

Chen, Y.N., Chen, C., Ma, J., 2000. Study on the action threshold in cabbage pestoptimal management of aphids. Plant Prot. 26, 10–13.

Chen, Y.N., Ma, J., Yuan, Z.M., Chen, C., Jiang, J.X., Xiao, X.P., 2002. Study on theinfluence of artificial defoliation on the yield of common cabbage and the actionthresholds for main leaf-mass consuming insect. J. Hunan Agric. Univ. (Nat. Sci.)28, 308–313.

Chen, Z.Q., Miao, S., Yang, C.X., Luo, K.J., Chen, A.D., Mu, W.D., 2003. Introduction of alarval parasitoid Diadegma semiclausum Hellen and evaluation of its potency ofcontrolling Plutella xylostella L. Plant Prot. 29, 22–24.

Chen, K.W., Huang, S.S., He, Y.R., 2006. Natural protection and augment ofTrichogramma population for controlling Plutella xylostella. J. South ChinaAgric. Univ. 27, 35–38.

China Agriculture Yearbook Editorial Committee, 2009. China Agriculture Yearbook.China Agriculture Press, Beijing.

De Barro, P.J., Liu, S.S., Boykin, L.M., Dinsdale, A.B., 2011. Bemisia tabaci: a statementof species status. Annu. Rev. Entomol. 56, 1–19.

Du, Y.C., Hu, H., Liu, F.Q., Chen, J.F., Wang, Q.L., Zhuang, Y., 2010. The current statusof organic vegetables in United States of America and its elicitation. ChinaVegetables 2010 (19), 9–11.

Furlong, M.J., Zalucki, M.P., 2010. Exploiting predators for pest management: theneed for sound ecological assessment. Entomol. Exp. Appl. 135, 225–236.

Furlong, M.J., Shi, Z.H., Liu, Y.Q., Guo, S.J., Lu, Y.B., Liu, S.S., Zalucki, M.P., 2004.Experimental analysis of the influence of pest management practice on theefficacy of an endemic arthropod natural enemy complex of the diamondbackmoth. J. Econ. Entomol. 97, 1814–1827.

Furlong, M.J., Kim, H.J., Pak, W.S., Jo, K.C., Ri, C.I., Zalucki, M.P., 2008. Integration ofendemic natural enemies and Bacillus thuringiensis to manage insect pests ofBrassica crops in North Korea. Agric. Ecosyst. Environ. 125, 223–238.

Guo, M.F., Zhu, D.F., Li, L.Y., 1999. Selection of Trichogramma species for controllingthe diamondback moth, Plutella xylostella (L.). Entomol. Sinica 6, 187–192.

Guo, S.J., Lin, W.C., Zhang, J.M., Xu, X.G., Liu, S.S., 2003. Selective and persistenttoxicity of insecticide mixtures to the diamondback moth, Plutella xylostella andits parasite, Oomyzus sokolowskii. Acta Agriculturae Zhejiangensis 15,231–236.

Hamilton, A.J., Waters, E.K., Kim, H.J., Pak, W.S., Furlong, M.J., 2009. Validation offixed sample size plans for monitoring lepidopteran pests of Brassica oleraceacrops in North Korea. J. Econ. Entomol. 102, 1336–1343.

Han, X.L., 1956. On integration of chemical control and biological control. Entomol.Knowledge 2, 57–60.

He, Y.R., Pang, X.F., 2000. Species and parasitism of Trichogramma on thediamondback moth, Plutella xylostella in Shenzhen, China. Nat. EnemiesInsects 22, 1–5.

He, J.L., Wang, B.S., Li, X.M., 1983. A survey of parasites of the cabbage whitebutterfly, Pieris rapae L. and their biological characters in Shanghai. J. ShanghaiAgric. College 1, 5–10, 20.

He, J.L., Wang, B.S., Li, X.M., Zhang, Z.L., Zhu, L.L., 1986. A preliminary study on thebionomics of Apanteles glomeratus (L.). J. Shanghai Agric. College 4, 309–318.

He, Y.R., Lv, L.H., Pang, X.F., 2001. Selection of effetive species of Trichogramma eggparasitoids of diamondback moth: I. Laboratory evaluation on the parasitizatingcapacity of several Trichogramma and Trichogrammatoidea species. Chin. J. Biol.Control 17, 6–9.

He, J.H., Liu, Y.Q., Shi, Z.H., 2002a. List of hymenopterous parasitid of Spodopteralitura Fabricius from China. Nat. Enemies Insects 24, 128–137.

He, J.H., Shi, Z.H., Liu, Y.Q., 2002b. List of hymenopterous parasitoids of Spodopteraexigua (Hubner) from China. J. Zhejiang Univ.-Agric. Life Sci. 28, 473–479.

He, Y.R., Lv, L.H., Chen, K.W., 2005. Parasitizing ability and interspecific competitionof Trichogramma confusum Viggiani and T. pretiosum Riley on the eggs of Plutellaxylostella (L.) in the laboratory. Acta Ecologica Sinica 25, 837–841.

Hu, C., 1983. A survey on the parasites of the small white butterfly, Artogeia rapae(L.) in China. Acta Entomol. Sinica 26, 287–294.

Hu, C., 1984. Life history and occurrence of Pteromalus puparum L. in Hangzhou.Acta Entomol. Sinica 27, 302–307.

Huang, F., Cao, T.T., Shi, M., Chen, Y.F., Chen, X.X., 2008. Parasitism-induced effectson host growth and metabolic efficiency in Plutella xylostella larvae parasitizedby Cotesia vestalis or Diadegma semiclausum. Insect Sci. 15, 237–243.

Huangfu, W.G., Gao, M.Q., Wu, Q., Wei, S.J., Chai, W.G., Chen, R.X., Chen, X.X., 2010.Hymenopteran parasitoids from larvae and pupae of the diamondback moth,Plutella xylostella in Ningbo, China. Chin. J. Biol. Control 26, 254–259.

Jiang, J.X., Liang, G.W., 2001. Effect of multiple predator species on commoncutworm. Chin. J. Biol. Control 17, 133–137.

Jiang, J.X., Liang, G.W., Pang, X.F., 1999. Effectiveness of natural enemies onSpodoptera litura. Chin. J. Appl. Ecol. 10, 461–463.

Jin, M.X., 1936. Two pupal parasite wasps of Pieris rapae. Insects Plant Pathog. 4,592–600.

Ke, L.D., Fang, J.L., 1982. Studies on the biology of the braconid wasp, Apantelesplutellae Kurdjumov. Acta Phytophylacica Sinica 9, 27–34.

Li, H.K., 1987. Survey on the pathogens of major vegetable pests. Nat. EnemiesInsects 9, 194–198.

Li, N., 1997. Preliminary studies on the aphidius of rape aphid in Xining area. J.Qinghai Uinv. 15, 14–17.

44 Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46

Author's personal copy

Li, Z.M., Liu, Y.Q., 2005. Comparative toxicity of several insecticides to Cotesiaplutellae. Chin. J. Pesticides 44, 374–376.

Li, Y.X., Liu, Y.Q., Liu, S.S., 2001. Effect of superparasitism on bionomics of Cotesiaplutellae. Chin. J. Biol. Control 17, 151–154.

Li, Y.X., Liu, S.S., Liu, Y.Q., 2002. Effects of host insecticide resistance on thebiological characteristics of Cotesia plutellae. Acta Entomol. Sinica 45, 459–464.

Li, Q.B., Shi, Z.H., Liu, S.S., 2004. Ability of host discrimination and interspecificcompetition of Oomyzus sokolowskii (Kurdjumov). J. Zhejiang Univ.-Agric. LifeSci. 30, 164–168.

Li, Z.M., Wang, W.L., Wu, H.M., Liu, S.S., Liu, Y.Q., Tang, Z.H., 2006. Detection andanalysis of spinosad residue in the body fluid of Cotesia plutella larvae withHPLC. Acta Entomol. Sinica 49, 137–141.

Li, L.R., Xue, R.F., Wang, X.J., Zeng, F.R., 2008. Predation of Nesidiocoris tenuis toTrialeurodes vaporariorum and Plutella xylostella. J. Agric. Univ. Hebei 31, 84–87.

Li, Z.Y., Zalucki, M.P., Bao, H.L., Chen, H.Y., Hu, Z.D., Zhang, D.Y., Lin, Q.S., Yin, F.,Wang, M., Feng, X., 2012. Population dynamics and ‘‘outbreakes’’ ofdiamondback moth (Lepidoptera: Plutellae) in Guangdong province, China:climate or failure of management? J. Econ. Entomol. 105, 739–752.

Liang, G.W., Pang, X.F., 1996. Strategy and tactics of ecological control of Plutellaxylostella population. In: Zhang, Z.L., Piao, Y.F., Wu, J.W. (Eds.), Proceedings ofthe National Symposium on IPM in China. China Agricultural Science andTechnology Press, Beijing, p. 720.

Lin, W.C., Guo, S.J., Song, H.M., 1998. Population fluctuation of Apanteles glomeratusand toxicity of insecticides. Nat. Enemies Insects 20, 150–155.

Lin, W.C., Guo, S.J., Zhang, J.M., Liu, S.S., 2002. Effects of different control practices onlepidopterous insect pests and beneficials in autumn cabbage. Acta AgriculturaeZhejiangensis 14, 150–154.

Lin, Z.F., Luo, L.Z., Pan, X.L., 2007. Insecticide abuse is an important cause of beetarmyworm outbreak. Chin. Bull. Entomol. 44, 327–332.

Liu, S.S., 1990. The relationship between the age and at parasitization and parasiteimpact in Myzus persicae. Acta Ecologica Sinica 33, 430–436.

Liu, H.T., 2001. Studies on predation function systems of the dominant predatorynatural enemies for diamondback moth and mechanism of enhancing theirfucntions., Master thesis. Department of Plant Protection, Yangzhou University,Yangzhou, pp. 42.

Liu, S.S., Jiang, L.H., 2003. Differential parasitism of Plutella xylostella (Lepidoptera:Plutellidae) larvae by the parasitoid Cotesia plutellae (Hymenoptera:Braconidae) on two host plant species. Bull. Entomol. Res. 93, 65–72.

Liu, Y.H., Li, B.P., 2006. Host-stage selection for Spodoptera exigua larvae and theeffect on developmental parameters of solitary endoparasitoid in Meteoruspulchricornis (Hymenoptera: Braconidae). J. Nanjing Agric. Univ. 29, 66–70.

Liu, Y.G., Qiu, G.J., 2001. Socioeconomic study on farmer’s adoption of IPM strategiesin brassica vegetable crops in China. Study report submitted to ACIAR, Centrefor Integrated Agriculture Development. China Agricultural University, Beijing.

Liu, S.S., Wang, X.G., 1999. Host stage preference and suitability of Oomyzussokolowskii, a major larval – pupal parasitoid of Plutella xylostella. Chin. J. Biol.Control 15, 1–4.

Liu, S.S., Yan, S., 1998. Brassica IPM in Asia: successes, challenges, and opportunities.In: Zalucki, M.P., Drew, R.A.I., White, G.G. (Eds.), Pest management – FutureChallenges, Proceedings of the Sixth Australasian Applied EntomologicalResearch Conference. Univ Queensland, Dept Hosp Tourism Prop ManagementLawes, Brisbane, Australia, pp. 85–97.

Liu, S.S., Xu, Z.H., Li, Z.Q., 1990. A preliminary investigation of the parasites of aphidson cruciferous vegetables in Hangzhou. Chin. J. Biol. Control 6, 5–8.

Liu, S.S., Cao, R.B., Zhu, G.N., 1995. Handbook of Control of Insect Pests, Diseases, andWeeds in Vegetables. China Agriculture Press, Beijing.

Liu, S.S., Wang, X.G., Guo, S.J., He, J.H., Shi, Z.H., 2000a. Seasonal abundance of theparasitoid complex associated with the diamondback moth, Plutella xylostella(Lepidoptera: Plutellidae) in Hangzhou, China. Bull. Entomol. Res. 90, 221–231.

Liu, S.S., Wang, X.G., Shi, Z.H., Guo, S.J., 2000b. Biology of Oomyzus sokolowskii andeffect of temperature on its population parameters. Acta Entomol. Sinica 43,159–167.

Liu, S.S., Wang, X.G., Shi, Z.H., Gebremeskel, F.B., 2001. The biology of Diadromuscollaris (Hymenoptera: Ichneumonidae), a pupal parasitoid of Plutella xylostella(Lepidoptera: Plutellidae), and its interactions with Oomyzus sokolowskii(Hymenoptera: Eulophidae). Bull. Entomol. Res. 91, 461–469.

Liu, S.S., Gebremeskel, F.B., Shi, Z.H., 2002. Reproductive compatibility and variationin survival and sex ratio between two geographic populations of Diadromuscollaris, a pupal parasitoid of the diamondback moth, Plutella xylostella.Biocontrol 47, 625–643.

Liu, S.S., Li, Y.X., Tang, Z.H., 2003. Host resistance to an insecticide favors selection ofresistance in the parasitoid, Cotesia plutellae (Hymenoptera: Braconidae). Biol.Control 28, 137–143.

Liu, S.S., Shi, Z.H., Guo, S.J., Chen, Y.N., Zhang, G.M., Lu, L.F., Wang, D.S., Deuter, P.,Zalucki, M.P., 2004a. Improvement of crucifer IPM in the Changjiang Rivervalley, China: From research to practice. In: Endersby, N.M., Ridland, P.M. (Eds.),Management of Diamondback Moth and Other Crucifer Pests: Proceedings ofthe Fourth International Workshop, Melbourne, pp. 61–66.

Liu, S.S., Zhou, H.W., Liu, Y.Q., He, J.H., 2004b. An investigation of geographicdistribution of Diadegma semiclausum, a major parasitoid of the diamondbackmoth, Plutella xylostella, in China. Acta Phytophylacica Sinica 31, 13–20.

Liu, S.S., Shi, Z.H., Furlong, M.J., Zalucki, M.P., 2005. Conservation and enhancementof biological control helps to improve sustainable production of brassicavegetables in China and Australia. In: Hoddle, M.S. (Ed.), Second InternationalSymposium on Biological Control of Arthropods. USDA Forest ServicePublication FHTET-2005-08, Davos, Switzerland, pp. 270–282.

Liu, S.S., Li, Z.M., Liu, Y.Q., Feng, M.G., Tang, Z.H., 2007. Promoting selection ofresistance to spinosad in the parasitoid Cotesia plutellae by integratingresistance of hosts to the insecticide into the selection process. Biol. Control41, 246–255.

Lu, Z.Q., Lin, G.L., Chen, L.F., Zhu, Z.L., Zhu, S.D., 1986. Studies on natural enemies ofaphids on vegetable crops and their control effects. Nat. Enemies Insects 8, 63–71.

Lu, H., Shi, B.C., Zhang, Z.L., 1992. Effects and selections of Aphidius gifuensis andDiaeretiella rapae on host aphids. In: Zhu, G.R., Zhang, Z.L., Shen, C.Y. (Eds.),Advance in IPM on Main Vegetables. Chinese Agricultural Science TechnologyPress, Beijing, pp. 251–254.

Luo, L.Z., Cao, Y.Z., Jiang, X.F., 2000. Characteristics of occurence and tendency ofbeet armyworm, Spodoptera exigua. Plant Prot. 26, 37–39.

Luo, K.J., Gu, D.X., Zhang, G.R., Chen, Z.Q., 2004. Parasitoids of four Noctuidae pestsin cruciferous vegetable. Chin. J. Biol. Control 20, 211–214.

Luo, K.J., Zhang, G.R., Gu, D.X., Pang, Y., 2005. Effect of Spodoptera exigua multicapsidnucleopolyhedrovirus on Trichogramma confusum: comparison of populationparameters and PCR detection. Acta Entomol. Sinica 48, 57–60.

Lv, Y.X., 1983. A survey of natural enemies of larvae of Plutella xylostella. Nat.Enemies Insects 5, 188–189.

Morse, S., Buhler, W., 1997. IPM in developing countries: the danger of an ideal.Integr. Pest Manage. Rev. 2, 175–185.

Qiu, B., Tang, Y.L., 2010. Effect of Host Stadium on the fecundity and life-span ofSnellenius manilae (Ashmead). J. ChangJiang Vegetables 18, 16–18.

Qu, Z.G., Wang, J.Y., Zhu, L.Y., 2004. Study on developmental durations, accumulatedtemperature and developmental zero of Microplitis tuberculifer Wesmael. ActaAgriculturae Boriali-Sinica 19, 100–101.

Shi, B.C., Lu, H., Niu, Y.Z., Zhang, Z.L., 1992. Studies on the parasite wasps of aphidson vegetable cruciferae in Beijing area. In: Zhu, G.R., Zhang, Z.L., Shen, C.Y.(Eds.), Advance in IPM on Main Vegetables. Chinese Agricultural ScienceTechnology Press, Beijing, pp. 246–250.

Shi, Z.H., Gebremeskel, F.B., Liu, S.S., 2001. Interspecific competition betweenDiadromus collaris and Oomyzus sokolowskii, two major parasitoids of Plutellaxylostella. Chin. J. Biol. Control 17, 112–115.

Shi, Z.H., Liu, S.S., Li, Y.X., 2002. Cotesia plutellae parasitizing Plutella xylostella: host-age dependent parasitism and its effect on host development and foodconsumption. Biocontrol 47, 499–511.

Shi, Z.H., Li, Q.B., Li, X., Liu, S.S., 2003a. Interspecific competition between twoparasitoids Diadegma semiclausum and Oomyzus sokolowskii in Plutella xylostella.Chin. J. Biol. Control 19, 97–102.

Shi, Z.H., Rageh, M.A., Liu, S.S., 2003b. Effects of host age and temperature oninterspecific competition between Cotesia plutellae (Kurdjmov) and Oomyzussokolowskii (Kurdjmov). J. Zhejiang Univ.-Agric. Life Sci. 29, 24–28.

Shi, Z.H., Guo, S.J., Lin, W.C., Liu, S.S., 2004a. Evaluation of selective toxicity of fivepesticides against Plutella xylostelia (Lep.: Plutellidae) and their side-effectsagainst Cotesia plutellae (Hym.: Braconidae) and Oomyzus sokolowskii (Hym.:Eulophidae). Pest Manage. Sci. 60, 1213–1219.

Shi, Z.H., Li, Q.B., Li, X., Liu, S.S., 2004b. Interspecific competition between Diadegmasemiclausum (Hymenoptera: Ichneumonidae) and Cotesia plutellae(Hymenoptera: Braconidae) in parasitizing Plutella xylostella larvae. ActaEntomol. Sinica 47, 342–348.

Song, J.X., Huo, S.T., Yang, Y., 1992. A survey on the parasites of the cabbage whitebutterfly, Pieris rapae L. and their utilization potentialtity in Shanxi. ActaAgriculturae Boreali-occidentalis Sinica 1, 18–22.

Su, J.Y., 1997. Natural enemies and biological control of Laphygma exigua Hubner.Nat. Enemies Insects 19 (180–187), 151.

Sun, J.S., Huang, S.S., 2010. Evaluation of potential control ability of Snelleniusmanilae (Ashmead) against Spodoptera exigua (Hubner). Acta Ecologica Sinica30, 1494–1499.

Sun, Y., Wan, F.H., 2000. Quality control in mass rearing procedure of Coccinellaseptempunctata L. (Col.: Coccinellidae). Chin. J. Biol. Control 16, 8–11.

Tang, L.Q., Li, X., Sun, S.J., 2007. Investigation on species population dynamics andcontrol efficacy of parasitoids of diamondback moth in the suburb ofZhengzhou. J. Henan Agric. Univ. 41, 167–170.

Wang, L.L., 1992. Improvement of marketing system of ‘green and clean’ vegetables.China Vegetables 1992 (2), 27–29.

Wang, X.G., Keller, M.A., 2002. A comparison of the host-searching efficiency of twolarval parasitoids of Plutella xylostella. Ecol. Entomol. 27, 105–114.

Wang, X.G., Liu, S.S., 2002. Effects of host age on the performance of Diadromuscollaris, a pupal parasitoid of Plutella xylostella. Biocontrol 47, 293–307.

Wang, X.Y., Shen, Z.R., 2002. Selective toxicity of four insecticides on green peachaphid (Homoptera: aphididae) and predator multicolored asian ladybird(Coleoptera: Coccinellidae) and the coordination evaluation of biological &chemical control to isect pest. Chin. J. Pesticide Sci. 4, 34–38.

Wang, X.G., Liu, S.S., He, J.H., Guo, S.J., 1998. Investigations on parasitoids ofdiamondback moth in the suburb areas of Hangzhou. Acta PhytophylacicaSinica 25, 20–26.

Wang, X.G., Liu, S.S., Guo, S.J., Lin, W.C., 1999. Effects of host stages and temperatureon population parameters of Oomyzus sokolowskii, a larval–pupal parasitoid ofPlutella xylostella. Biocontrol 44, 391–402.

Wang, W.G., Zhang, Y.Q., Hou, M.Z., Chen, Y.N., Zeng, H.G., 2003. Analysis ofcommunity structure of pest enemy of crucifer vegetables in Nanning. J.Guangxi Agric. Biol. Sci. 22, 266–270.

Wang, X.G., Duff, J., Keller, M.A., Zalucki, M.P., Liu, S.S., Bailey, P., 2004. Role ofDiadegma semiclausum (Hymenoptera: Ichneumonidae) in controlling Plutellaxylostella (Lepidoptera: Plutellidae): cage exclusion experiments and directobservation. Biocontrol Sci. Tech. 14, 571–586.

Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46 45

Author's personal copy

Wang, C.P., You, L.S., Xiao, F., Xiao, S.H., 2005. Bionomic of Cotesia glomerata as aparasitoid of Pieris rapae. Hunan Agric. Sci. 2005 (3), 51–53.

Wang, S., Zhang, R.Z., Zhang, F., 2007. Research progress on biology and ecology ofHarmonia axyridis Pallas (Coleoptera: Coccinellidae). Chin. J. Appl. Ecol. 18,2117–2126.

Wang, J.P., Guo, H.F., Fang, J.C., Zhong, W.F., Liu, B.S., 2009. Interaction of Meteoruspulchriconis with Spodoptera litura neuclopolyhedrovirus and impact ofchlorfluazuron on parasitoid. Jiangsu J. Agric. Sci. 25, 1268–1272.

Wang, D.S., Lv, L.H., He, Y.R., Qin, S.S., Pan, F., 2010. Effect of conventionalinsecticides on Trichogrammatoidea bactrae. Chin. Bull. Entomol. 47, 379–383.

Wearing, C.H., 1988. Evaluating the IPM implementation process. Annu. Rev.Entomol. 33, 17–38.

Wu, J.W., 1997. Introduction of cruciferous vegetable IPM in China. ChinaVegetables 16, 55–57.

Wu, G., Jiang, S.R., 2004. Susceptibility to insecticides and enzymetic characteristicsin the parasitoid Apanteles plutellae Kurdj. (Hymenoptera: Braconidae) and itshost Plutella xylostella (L.). Acta Entomol. Sinica 47, 25–32.

Wu, M.X., You, M.S., 2002. Investigations on natural enemines of diamondbackmoth in the suburbs of Fuzhou. Entomol. J. East China 11, 25–28.

Wu, J.W., Wang, J.R., Wang, J., Shi, B.C., Wang, W., Wang, B.Z., Dong, Z.H., Wei, D.Z.,Huang, Q.F., 1987. A checklist of naural enemy on vegetable pests in Beijing.Acta Agriculturae Boriali-Sinica 2, 75–96.

Wu, M.X., Huang, J.M., You, M.S., 2003. Preliminary study on the main predators–spiders of the diamondbck moth. Wuyi Sci. J. 19, 48–52.

Xian, J.D., Zhang, M.L., Pang, X.F., 1997. Simulation of the complementary effect ofthe biological agents on diamond back moth. J. South China Agric. Univ. 18, 1–5.

Xiao, S.L., 1984. Preliminary study on biological characteristcs of Pteromaluspuparum and protection. Guizhou Agric. Sci. 1984 (2), 33–36.

Xie, J.J., He, M.Y., Xu, Z.F., 1999. Natural enemies and biological control of Spodopteralitura Fabricius. Nat. Enemies Insects 21, 82–92.

Xu, J.L., Yang, G.Q., 1983. Observation of biological characteristics of Microplitis sp.Nat. Enemies Insects 5, 12–13.

Xu, Z.F., Qiu, X.H., Song, L.Q., Ren, S.X., 2001. Survey of the natural enemies ofSpodoptera exigua (Hubner). Nat. Enemies Insects 23, 95–96.

Xu, F.C., Yu, Y.J., Chen, X.Y., Wu, Y.H., 2003. Investigation on parasitoids of crucifervegetable pests in the suburb ares of Wenzhou. Acta Agriculturae Zhejiangensis15, 353–356.

Yang, Z.Q., 1982. Preliminary investigation on major natural enemies of vegetablepests in Jiangxi province. Jiangxi Plant Prot. 5, 10–14.

Yang, L.M., Lu, Z.Q., Lv, Z.L., Yin, Z.S., 1982. The development of Apanteles glomeratusin Pieris rapae and host larvae reaction. Nat. Enemies Insects 4, 9–12.

Yin, R.G., 1992. Several addtional observation on Pteromalus puparum in parasitizingPieris rapae. Nat. Enemies Insects 14, 19–20.

Yin, J., Wang, J.C., 1997. Preliminary study on the occurrence regularity ofPteromalus puparum. J. Henan Agric. Sci. 26, 15–16.

Yin, K.S., Wu, W.W., He, C.X., Luo, Y.J., 2005. Toxicity of 5 insecticides on Brevicorynebrassicae and Diaeretiella rapae. Plant Prot. 31, 84–85.

Yu, F.M., 2003. The current status of organic vegetables in Shanghai and the strategyfor development. J. ChangJiang Vegetables 2003 (6), 7–8.

Yu, Y.J., Lv, L.F., Xu, F.C., Wu, Y.H., Yu, C.H., 2002. Study on different control practicesof lepidopterous insect pests in autumn cabbage. Plant Prot. 28, 23–26.

Yuan, J.Q., Li, X., 2008. Studies on the influencing factors of sex ration of Diadegmasemiclausum Hellen. J. Henan Agric. Univ. 42, 334–336.

Zalucki, M.P., 2007. Improvement of integrated pest management of brassicavegetable crops in China and Australia (CS2/1998/089). In: Gordon, J., Davis, J.(Eds.), Adoption of ACIAR Project Outputs: Studies of Projects Completed in2002–2003. ACIAR, Canberra, pp. 31–34.

Zalucki, M.P., Shabbir, A., Silva, R., Adamson, D., Liu, S.S., Furlong, M.J., 2012.Estimating the economic cost of one of the world’s major insect pests, Plutellaxylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J. Econ.Entomol. 105, 1115–1129.

Zeng, A.P., Wang, K.W., Jiang, J.X., Ji, X.Y., You, L.S., 2005. On the bionomics ofMicroplitis pallidipes. J. Hunan Agric. Univ. (Nat. Sci.) 31, 502–505.

Zhang, Z.L., 1992. Studies on effect of temperature on two species of parasitoids,Aphidius gifuensis and Diaeretiella rapae on Myzus persicae. In: Zhu, G.R., Zhang,Z.L., Shen, C.Y. (Eds.), Advance in IPM on Main Vegetables. Chinese AgriculturalScience Technology Press, Beijing, pp. 255–258.

Zhang, G.M., Liu, S.S., 1993. A Bibliography of Insects Associated with VegetableCrops in China. China Agricultural Science and Technology Press, Beijing.

Zhang, Z.L., Luo, C., 2001. Current status and control methods of Bemisia tabaci inChina. Plant Prot. 27, 25–30.

Zhang, M.L., Pang, X.F., 1995. Studies of the effectiveness of Trichogramma ondiamondback moth. Ecol. Sci. 14, 84–87.

Zhang, Z.L., Zhu, G.R., Wu, J.W., 1996. Twenty years of the integrated control ofvegetable diseases and insect pests. In: Zhang, Z.L., Piao, Y.F., Wu, J.W. (Eds.),Proceedings of the National Symposium on IPM in China. China AgriculturalScience and Technology Press, Beijing, pp. 43–46.

Zhang, M.L., Han, S.C., Li, L.Y., Zeng, B.K., Lu, L.M., Guo, M.F., 1998. The characteristicsof biology and ecology of Diadromus collaris, a pupal parasitoid of diamondbackmoth. Nat. Enemies Insects 20, 2–8.

Zhang, G.M., Liu, Y.Q., Shi, Z.H., Liu, S.S., Shen, J.H., 1999. Development of practicalIPM systems in autumn cabbage crops. In: China National AgriculturalTechnology Extension and Service Centre (Ed.), Recent Developments inResearch of Sustainable Management of Pests in Agricultural Crops.Agriculture Press, Beijing, China, pp. 379–386.

Zhang, J.M., Zhang, C.Q., Wang, H., Zhu, X.Y., 2006. Predation of Paederus fuscipes(Coleoptera: Staphylinidae) on Pieris rapae eggs. J. Yangtze Univ. (Nat. Sci. Ed.) 3,113–117.

Zhao, H.Y., Wan, L.M., Zhang, W.L., Pei, J.D., 1986. A survey of the natural enemyresource of Pieris rapae in Tong-Hua, Ji Lin. Chin. J. Biol. Control 2, 42.

Zhao, H.F., Shen, Y., Lei, L.B., 2005a. Predatory functional response of spiders to Pierisrapae. Anhui Agric. Sci. Bull. 11, 65–66.

Zhao, S.R., Yuan, Y.D., Yu, W.J., Zhang, H.T., Wang, D.S., 2005b. Studies on theinfluence of diamondback moth on the yield of autumn cauliflower and theeconomic thresholds. Acta Agriculturae Shanghai 21, 45–48.

Zhong, P.S., Tian, M.Y., Zeng, L., 2002. Effects of ecological measures for controllingPlutella xylostella (L.) on arthropod community. Wuyi Sci. J. 18, 99–103.

Zhong, P.S., Liang, G.W., Zeng, L., 2005. Studies on effects of ecological measuresagainst diamondback moth (DBM), Plutella xylostella (L.). Acta AgriculturaeUniversitatis Jiangxiensis 27, 417–421.

Zhou, X.M., Huang, B.Q., 2002. Insecticide resistance of the common cutworm(Spodoptera litura) and its contrl strategies. Entomol. Knowledge 39, 98–102.

Zhou, A.N., Ma, X.L., Ma, C.Z., 1996. Composite and dynamic economic threshold forlepidopterous pest complex of cabbage in Shanghai suburb. Acta Entomol.Sinica 39, 149–157.

Zhou, Q., Liang, G.W., Zeng, L., 2004. Population dynamics of aphids and theirnatural enemies on crucifer vegetables in Shenzhen suburbs. Chin. J. Biol.Control 20, 70–71.

Zhu, G.R., Zhang, Z.L., Shen, C.Y., 1992. Advance in IPM on Main Vegetables. ChinaAgricultural Science and Technology Press, Beijing.

Zhu, S.D., Lu, Z.Q., Chen, L.F., 1994. Injury equivalence system of leaf-massconsuming insect pests on cabbage and the multiple-species economicthreshold. J. Jiangsu Agric. College 15, 23–28.

46 Y.-Q. Liu et al. / Biological Control 68 (2014) 37–46