Abstract

Crucifers comprise a major group of vegetable crops in the Changjiang River Valley, China. The control of insect pests on crucifer vegetable crops has largely relied on the heavy use of chemical insecticides in the last 30 years, resulting in serious consequences of insecticide resistance, increased costs of control and insecticide residues hazardous to human health. A group of Chinese and Australian scientists have undertaken a joint venture to develop practical and sustainable IPM strategies for crucifer vegetable crops in this region. The work consists of three overlapping and ongoing phases: problem definition, research and development, and implementation. Natural enemies were surveyed and evaluated. Biological and selective insecticides were screened through bioassays and field tests. Damage relationships by various insect pests were assessed by artificial defoliation and natural infestation of plants. It was found that cabbages could endure some defoliation without reduction of head weight, but that the level of compensation varied with the growth stages being attacked. Plants at the pre-heading or mid-late heading stages could endure substantial damage while plants at transplant or cupping to early heading stage were sensitive to damage. These findings on various components interrelated to IPM were used to develop management strategies at the crop system level, which were tested in the field. Field IPM trials across several seasons and localities showed that the new strategy could offer effective control of all insect pests. Compared with conventional methods, IPM practices could usually reduce insecticide input by as much as 30–70%, with little risk of crop loss. Implementation activities included grower involvement in field trials, field days and participatory workshops as well as frequent dissemination of fact sheets. Evidence shows that a substantial improvement in farmers’ knowledge, attitude and approaches towards IPM has been achieved in the project areas. The future challenges to and opportunities for improving crucifer IPM in China are discussed.

Keywords

crucifer vegetables, action thresholds, natural enemies, biological insecticides, integrated pest management

Introduction

Crucifers constitute one major group of vegetables in China. The area under vegetable cultivation has increased about 5-fold in the last 20 years, reaching over 14 million ha in 2000, based on single crops. The proportion of crucifers usually accounts for 40–55% of all vegetable crops, depending on the region. In Zhejiang province, the proportion of crucifer vegetables has been decreasing in recent years due to an increase in other crops, but remains over 40%.

In the Changjiang River Valley, crucifer vegetables are mostly grown by small landholders (<0.5 ha) around urban centres, in highlands, and in specialised production areas. The crop systems are complex and erratic, revolving as they often do around intercropping (growing more than one crop on a small piece of land at the same time) throughout the year. A complex of insect pests attacks crucifer vegetable crops. As an example, Figure 1 shows the major insect pests that the crucifer growers usually have to deal with through the seasons in a year in Hangzhou, Zhejiang.

In the last 30 years, the control of insect pests on crucifer vegetable crops in China has largely relied on heavy use of chemical insecticides. This has had serious consequences of insecticide resistance, increase of control costs, and most importantly pesticide residues hazardous to human health. Here we report a joint effort by farmers, extension officers and researchers that has helped to improve the situation in some localities. We then discuss briefly the challenges to and opportunities for improving integrated pest management (IPM) in crucifer vegetable crops in the Changjiang River Valley, China.

Figure 1. Occurrence of insect pests that may cause serious damage to crucifer vegetable crops during various periods of the year in Hangzhou, China.

A joint venture in improving crucifer IPM

This project was started in 1995 to build on existing studies to develop sound, sustainable crucifer IPM strategies that significantly reduce pesticide hazards, and are acceptable to the growers in the east range of the Changjiang River Valley. It has involved five institutes in China, working in close collaboration with two institutes from Australia (Liu et al. 1996). The working strategy consists of three overlapping and ongoing phases: problem definition, research and development, and implementation. Structured problem definition workshops, involving all groups of stakeholders and in particular farmers and extension workers, were organised at the start of the project to promote information flow, determine priority issues, address priority needs and propose action plans (Liu et al. 1996, Norton & Mumford 1993). Work has since been concentrating on the following five, interacting components: (1) survey and evaluation of natural beneficial insects, (2) rational application of insecticides, in particular promoting use of biological insecticides, (3) development of action thresholds, (4) development of management strategies, through season-long in-field IPM trials and (5) IPM implementation activities.

Survey and evaluation of parasitoids

Regular sampling in both farmers’ fields and unsprayed fields in Hangzhou showed that a range of parasitoids attack each of the major pests. For example, the diamondback moth (DBM), Plutella xylostella is attacked by at least eight species of parasitoid, of which Cotesia plutellae, Oomyzus sokolowskii and Diadromus collaris were the major larval, larval-pupal and pupal parasitoids respectively (Liu et al. 2000). Pieris rapae is attacked by the following 7 species of parasitoids: Trichogramma chilonis in the egg stage, Cotesia glomeratus and Hyposoter ebeninus in the larval stage, and Pteromalus puparum, Brachymeria lasus, Pimpla disparis and Iseropus kuwanae in the pupal stage. Of the 7 species, C. glomeratus and P. puparum were most abundant.

Insect parasitoids are active in the fields despite heavy use of chemical insecticides in the crop systems over the years. For example, parasitoids usually achieved 10–60% parasitism of DBM larvae and pupae during June to early July and September-November each year when DBM was most abundant (Liu et al. 2000). The biology of the major DBM parasitoids has been studied to provide information essential for understanding and evaluation of these beneficial insects (Wang et al. 1999; Liu et al. 2001, 2002; Shi et al. 2002; Wang & Liu 2002). Liu et al. (2003) showed that DBM resistance to an insecticide not only confers some protection to an endo-larval parasitoid, but also helps selection of resistance genes in the latter. This new information may help to gain more understanding of parasitoid survival in the field. The impact of natural enemies on the survival of DBM in the field has been investigated under different management strategies (see below).

Evaluation of biological and selective insecticides

Biological and chemical insecticides were bio-assayed in the laboratory and tested in the field. A number of Bt and NPV products were shown to have high efficacy in killing the target pests without side effects on the beneficial insects (Liu & Zhang 1997, Shi & Liu 1998). Other insecticides showing desirable selectivity include: abamectin, avermectin, spinosad and fipronil against DBM and P. rapae, chlorfluazuron and chlorfenapyr against S. litura and S. exigua, and imidacloprid against aphids (Liu & Zalucki 2001, Guo et al. 2003).

Development of action thresholds

Laboratory and greenhouse trials by artificial defoliation demonstrated that the common cabbage (cv. Jingfeng No. 1) can endure some defoliation without reduction of head weight at harvest. There was substantial evidence of over-compensation for defoliation at the pre-heading stage. However, the plants were sensitive to defoliation at the cupping stage (Table 1). Results of trial by insect defoliation in the field seemed to agree with the findings of artificial defoliation (Figure 2). These data were used to develop action thresholds for practical application (Table 2). Of particular value was the characterisation of crop growth stages sensitive to insect damage. Thus, farmers and extension officers were asked to monitor the insect pests more carefully at both the seedling and cupping stages.

Table 1. Head weight of cabbage at harvest after artificial defoliation of middle and outer leaves at various growth stages

Growth	Head	Proportion of defoliation
Stage	Measurements	1/8	1/4	1/2	Control
Pre-heading	Head weight (kg)a	1.01 ± 0.26 a	0.84 ± 0.22 b	0.82 ± 0.16 b	0.92 ± 0.18 ab
	Increase (%)b	9.78	-8.70	-10.86
Cupping	Head weight (kg)	0.88 ± 0.28 ab	0.81 ± 0.24 b	0.82 ± 0.20 b	0.92 ± 0.18 a
	Increase (%)	-4.34	-11.96	-10.86
Heading	Head weight (kg)	0.95 ± 0.25 a	0.91 ± 0.23 a	0.86 ± 0.23 a	0.92 ± 0.18 a
	Increase (%)	3.26	-0.84	-5.53

^a Mean ± S.D. head weight per plant (n = 45 to 50) , and means in the same row followed by the same letter do not differ significantly (P>0.05, Fisher LSD test).

^b Percent increase of head weight in comparison with that of the control, i.e. zero defoliation.

Table 2. Action thresholds (mean number of insects/plant) used in IPM treatment

Pests	Cabbage growth stages
	Transplants	Pre-heading	Cupping to early heading	Heading to mature
Lepidopteraa	0.5	1.0	1.0	4.0
Aphids	5	500	500	2000

^a Numbers of lepidopterous larvae were converted to “standard” insects by the following formula:

1 standard insect = 1 Pieris rapae = 1 Spodoptera exigua = 0.5 S. litura = 5 Plutella xylostella.

IPM field trials

Based on the findings of studies of various components and information from literature, management strategies were formulated and tested in the field to develop practical IPM guidelines and protocols. The major components in the IPM strategy included use of action thresholds in decision-making and strategic use of biological and selective insecticides (Tables 2 and 3). Field IPM trials with common cabbage were conducted in Hangzhou from 1996 to 2000 and, in 2000, trials were conducted at five sites at Zhejiang and Shanghai. The results showed that biological and selective insecticides could offer effective control of all the insect pests. The activities by natural enemies were evidently promoted (Table 4). Compared with conventional practice, IPM practice could usually reduce insecticide input by as much as 30–70%, with little risk of crop loss (Table 4, Zhang et al. 1999).

Figure 2. Relationship between defoliation at the cupping stage and reduction of head weight at harvest in common cabbage (cv Jingfeng No.1). Each data point represents the mean value of 50 plants.

Table 3. Summary of designs of field IPM trials

Treatment	Description	Application of insecticides
IPM	Use of action thresholds, apply biological and selective insecticides	Spray Bt for control of DBM and Pieris rapae, spray NPV and chlorfluazuron for control of Spodoptera spp. and spray imidacloprid for control of aphids
Farmer	Simulation of typical practice by farmers, or recording of farmer’s practice	Calendar sprays with mixtures of hard chemical insecticides such as chlorpyrifos, fenvalerate, methomyl, fipronil, and methamidophos

Table 4. Examples of IPM trial results in Hangzhou in autumn 1998 and autumn 2000

	1998		2000
Assessments a	IPM	Farmer	IPM	Farmer
Mean head weight (kg)	1.23 a	1.11 a	1.18 a	1.02 a
% marketable heads	94.4 a	88.0 b	95.6 a	91.1 a
% heads without insect damage	52.5 a	16.7 b	76.7 b	96.7 a
Number of sprays	7 (8)	8(23)	3(5)	5(8)
Cost of insecticide application per ha (RMB)	2,700	3,780	680	1,025
% parasitism of DBM larvae	19.4 a	2.0 b	35.2 a	7.1 b
% parasitism of DBM pupae	32.6 a	1.3 b	18.8 a	13.0 a

^a Figures in the same row of the same year followed by the same letter do not differ (P>0.05, Student-t test).
^b In the IPM treatment, usually one insecticide and only rarely a mixture of 2 insecticides was used per spray, while in the Farmer treatment, usually a mixture of 2–3 insecticides was used per spray. Figure in brackets indicates the relative amount of insecticide input calculated on the basis of one insecticide in one spray at the recommended rates.

Implementation

Implementation activities included grower involvement in field trials, field days and participatory workshops, frequent dissemination of fact sheets, as well as short training courses for extension officers and growers (Liu et al. 1996, Liu & Zalucki 2001). An independent project evaluation in the project areas showed substantial improvement in farmers’ knowledge, attitude and approaches towards IPM. For example, 36% of the growers in the project areas do regular monitoring of insect pests on their crops and try to choose biological or selective insecticides for spray, compared with about 20% in the non-project areas. Growers in the project areas were found to have much more frequent contacts with extension officers than the non-project areas (Liu & Qiu 2001).

Future challenges

Morse and Buhler (1997) analysed the conditions for successful IPM, which include relatively simple agro-ecosystems, strong research and extension capacity, and stable markets, among others. These authors rightly point out that it is much more difficult to develop and adopt IPM in developing countries than in developed countries. Because of the complicated nature of crucifer vegetable ecosystems in the Changjiang River Valley, the development and implementation of crucifer IPM in this region indeed presents serious challenges to all the stakeholders involved.

Research and development

For IPM methods to be widely acceptable, they must be simplified as much as possible, particularly the use of monitoring and action thresholds. With the erratic vegetable cropping systems in the Changjiang River Valley, development of practical and reliable IPM methods for any crop will certainly take well-designed field trials across several seasons.

Implementation

Wearing (1988) lists the obstacles to IPM implementation under five interrelated headings: technical, financial, educational, marketing/social and organisational. These apply to crucifer IPM in the Changjiang River Valley. Liu and Yan (1998) discussed these obstacles in some detail. For example, in regard to the organisational obstacles, they pointed out that the co-ordination among organisations, disciplines and personnel will remain a serious problem. IPM can only be implemented effectively on an area-wide scale (Morse & Buhler 1997). This calls for close co-operation of many farmers in an area, which is difficult to achieve. Lack of trained extension workers will continue to be a major obstacle. In China, many of the state-employed extension workers have been directly involved in marketing chemical pesticides since the late 1980s. Consequently, their advice to farmers is no longer IPM-oriented but biased towards increasing pesticide inputs. This unfortunate situation has been seen to be a major reason for the rapid increase of pesticide application in recent years in China. It seems unlikely that this organisational problem will be overcome quickly.

Future opportunities

Major opportunities for promotion of IPM in crucifer vegetable will come from: (1) consumers' demand of food safety, (2) development of better organised farming, (3) increased support for research and extension, and (4) policy and legislation support (Liu & Yan 1998).

Consumer aversion to pesticide residues and increasing demands for food safety have been major forces driving implementation of IPM in vegetables in many Asian countries. In China, serious poisoning of humans by insecticide residue on crucifer vegetables has frequently been reported since the mid 1980s. These poisoning events initiated the demand by consumers for reducing chemical pesticide use on vegetables. Cosmetic standards of vegetables have become less stringent (Liu et al. 1996). Monitoring of pesticide residue has increased in both domestic vegetable supplies and international trade. There is some evidence that many consumers are prepared to pay a slightly higher price for “green and clean” vegetables. As the life style of consumers improves, their demand for eliminating pesticide residue on vegetables will become stronger and provide increasing opportunities for biological methods of pest control.

In China, IPM has been formally promoted as the national plant protection policy since 1975. However, effective policy support and legislation are still under development. National and local policies and legislative measures that ensure reduction of chemical insecticides, and increased food safety and environment protection are essential for successful implementation of IPM on crops, including crucifer vegetables. There is much to be done in this area.

Concluding remarks

Our work in the last several years proves that improvement of crucifer IPM can be achieved through a participatory approach involving growers, extension agents, and researchers. However, the control of insect pests on crucifer vegetable crops in the Changjiang River Valley as a whole still relies heavily on chemical insecticides. While obstacles to vegetable IPM are many, consumer aversion to pesticide residues, changes in the cropping system, increased support for research and extension, and a more favourable policy and legislation environment will act together to provide opportunities to achieve area-wide implementation of crucifer IPM in the years to come.

Acknowledgements

This work has been supported by the Australian Centre for International Agricultural Research, and the Department of Science and Technology, Zhejiang Province, China. About 20 scientists from China and 10 scientists from Australia contributed substantially to the achievements and many others participated in activities at various stages. Their names are not listed here because of space restrictions.

References