A survey of insect parasitoids of Plutella xylostella and the seasonal abundance of the major parasitoids in Hangzhou, China

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1 A survey of insect parasitoids of Plutella xylostella and the seasonal abundance of the major parasitoids in Hangzhou, China Liu Shu-sheng 1, Wang Xin-geng 1, Guo Shi-jian 2, He Jun-hua 1 and Song Hui-ming 2 1 Department of Plant Protection, Zhejiang Agricultural University, Hangzhou 329; 2 Institute of Plant Protection, Zhejiang Academy of Agricultural Sciences, Hangzhou 34, China Abstract We conducted an investigation of insect parasitoids of the diamondback moth, Plutella xylostella, in crucifer vegetable crops in the suburbs of Hangzhou in four periods from 1989 to The following six species of primary parasitoids were recorded: Trichogramma sp., Cotesia plutellae, Oomyzus sokolowskii, Diadromus collaris, Itoplectis naranyae, Brachymeria excarinata. Also recorded were seven species of hyperparasitoids of C. plutellae. Rates of parasitization of eggs were usually very low or none. However, rates of parasitization of larvae and pupae usually were substantial and showed two peaks each year, around June-July and September November, respectively. During the peaks the rates of parasitization were usually in the range of 6% and reached over 8% on a few occasions. C. plutellae, O. sokolowskii and D. collaris were the major larval, larval-pupal and pupal parasitoids, respectively. In the field, C. plutellae was active throughout the year. O. sokolowskii was active from May to October, entered into a quiescent state at the pupal stage in October November to overwinter and would not emerge until April May next year. D. collaris usually was recorded only from May to July. It was noted that rates of parasitization of the diamondback moth in radish and mustard fields were usually higher than those in common cabbage and Chinese cabbage fields in the same locality. It was also noted that there were negative correlation of the rates of parasitization between the two major larval parasitoids, C. plutellae and O. sokolowskii, indicating that there may be competitive relationship for host larvae between the two parasitoids. Key words: Plutella xylostella, insect parasitoids, rates of parasitization Introduction The diamondback moth (DBM), Plutella xylostella (L.) (Lepidoptera: Yponomeutidae), was a minor pest of crucifer vegetable crops in China before the 196 s. Its pest status increased rapidly since early sixties when chemical insecticides started to be widely applied in vegetable crops. In the last twenty years, this insect has been the most important insect pest of crucifer vegetable crops, especially in the Changjiang River Valley and Southern China (Shi and Liu, 1995). It has developed resistance to all groups of insecticides, including insect growth regulators and Bacillus thuringiensis Berliner (Bt) (Chao et al., 1991; Tang et al., 1992). Development and implementation of integrated pest management (IPM) systems are now considered to be the only solution to combat this highly resistant insect pest (Liu et al., 1995). In the past twenty years, development and implementation of biological control-based IPM has made remarkable achievement in the management of DBM in many parts of the world, such as in Southeast Asia and USA (Talekar and Shelton, 1993; Ooi, 1992; Biever, 1994). In these IPM systems, introduction and augmentation of insect parasitoids have played a key role. On the mainland of China, preliminary surveys of insect parasitoids of DBM have been conducted in Hubei (Lu, 1983), Guangzhou (Chen et al., 1987), Beijing (Wu et al., 1987) and Hangzhou (Ke and Fang, 1982). A total of 16 species have been recorded, but the majority of them have not been identified to the species. Little is known about the impact of insect parasitoids on the populations of DBM. As part of an effort to help develop biological control-based IPM of DBM in the Changjiang River Valley, we conducted a survey of insect parasitoids of DBM in Hangzhou suburbs and observed the seasonal changes of rates of parasitization. We also investigated the patterns of seasonal abundance of the major parasitoids. Materials and Methods Two types of sampling, i.e., irregular sampling in sprayed plots and regular sampling in unsprayed plots, were carried out in the suburbs of Hangzhou, where a vegetable cropping system typical for the Changjiang River Valley has existed for many years. For the irregular sampling in sprayed plots, sampling was done 1 2 times every month. In each time of sampling, samples were taken from one or more plots of different crops. These plots were not chosen at random. They were chosen on the basis of (1) no spray of chemical insecticides in the past days and (2) relative high number of DBM. Irregular sampling was conducted for four periods of time from 1989 to 1996: September December 1989, June July 199, June November 1994, and May 1995 April For the Status of DBM and other pests of crucifers and their biocontrol 61

2 sampling in unsprayed plots, sampling was made at intervals of 5 days from transplanting to harvest. Regular sampling was conducted in three plots in September October 1989, June July 199, and May 1995 January 1996, respectively. The following sampling methods were used for both types of sampling. On each sampling date, depending on the density of DBM, to 5 plants were chosen at random on each plot of crop (the size of one plot varied in the range of.3.7 ha). All larvae (with exception of first instar larvae), prepupae, pupae and parasitoid pupae were removed from each plant and taken back to the laboratory. Thirty to 5 DBM eggs were also taken from the plants. In the laboratory, DBM eggs were kept in groups of 5 in glass vials. DBM larvae were retained singly on fresh cabbage leaves in glass vials. DBM prepupae and pupae, and parasitoid pupae were kept singly in glass vials. All the vials were kept at room temperatures except in July August when they were kept at 25 C in a temperature-controlled room because of the high ambient temperature. DBM eggs were kept until eclosion or parasitoid emergence. DBM larvae, prepupae and pupae, and parasitoid pupae were reared until emergence of parasitoid adults or emergence of DBM moths. Dead individuals were dissected to see whether there were parasitoid larvae or eggs inside. Results During the four periods of this study, 83 samples in all were taken from common cabbage, Pak-choi, cauliflower, radish and mustard. A total of 45 eggs, 55 larvae and 56 pupae of DBM were sampled and reared in the laboratory. Species of parasitoids Six primary parasitoids were recorded (Table 1). Of the 6 species, Oomyzus sokolowskii is the only aggregate parasitoid, all the rest 5 species are solitary parasitoids. Cotesia plutellae and O. sokolowskii were most abundant, and Diadromus collaris was also abundant at times (see below). These three species can be regarded as the major species. It was noted that O. sokolowskii is also a major hyperparasitoid. Seven species of parasitoids of Cotesia plutellae, i.e., hyperparasitoids of DBM, were recorded as follows: Eurytoma verticillata (Fabricius) (Hymenoptera: Eurytomidae), O. sokolowskii, Ceraphron manilae (Ashmead) (Hymenoptera: Ceraphronidae), Trichomalopsis apanteloctenus (Crawford), T. shirakii (Crawford), Trichomalopsis sp.1 and Trichomalopsis sp. 2 (Hymenoptera: Pteromalidae). Of the seven species, E. verticillata and the 4 species of Trichomalopsis are solitary parasitoids, while O. sokolowskii and C. manilae are aggregate parasitoids. Rates of parasitization of DBM eggs Rates of parasitization of DBM eggs were low throughout the study periods, usually in the range of 5%. However, in one plot of radish sampled during September October, rates of parasitization were substantial, reaching 62.9% at its peak. Rates of parasitization of DBM larvae Rates of parasitization varied greatly with time. There were also a lot of variations between plots of the same crop and between plots of different crops at the same time of the year. These variations were not unexpected, especially in view of the wide variations of spray of chemical insecticides in different plots by different farmers. Nevertheless, the data of Table 2 show that parasitization of larvae was substantial on many occasions despite of the heavy input of chemical insecticides into the crop system. The rates of parasitization were in general highest during June July and September November each year, when DBM population was most abundant. During these two peak periods, rates of parasitization were usually in the range of 6%. It can be seen from Table 2 that the parasitization was mainly done by two parasitoids, i.e., C. plutellae and O. sokolowskii. It was also observed that C. plutellae was parasitized by a number of secondary parasitoids, and the rates of parasitization reached over 2% on many occasions. Simple comparison between crops indicates that on the whole the rates of parasitization in radish and mustard were higher than those in cabbage, Pak-choi and cauliflower. Because the sprays of chemical insecticides and the number of DBM larvae in different plots of crops were not recorded, it is not possible to speculate any particular reasons for the differences. Field and laboratory observation on C. plutellae showed that this parasitoid was active throughout the year, although it had very low numbers and developed slowly in winter months. Figure 1 shows the results from an unsprayed plot of common cabbage in autumn to winter DBM larvae increased rapidly initially to 25 per plant, then decreased to 15 per plant and maintained at that level to the end of the crop. Parasitoids of larvae were active throughout the crop period. Following the peak of DBM larvae, there was an apparent increase in rates of parasitization to nearly 5%. Decrease of parasitism during the late part of the crop was accompanied by low temperatures apparently unfavorable to the parasitoids during that time of the year. Detailed examinations of the rates of parasitization by each of the larval parasitoids indicate likely negative correlation of rates of parasitization between the two major larval parasitoids, C. plutellae and O. sokolowskii. Higher rates of parasitization of one species were usually accompanied by lower rates of the other species (Table 2). The phenomenon was also demonstrated by the data from unsprayed plots (Figure 2). Rates of parasitization of DBM pupae The data in Table 3 and Figure 1 show that the patterns of parasitization of pupae, including seasonal variations and variations between plots and crops, were similar to those of larvae described above. Highest 62 Proceedings: The Management of Diamondback Moth and Other Crucifer Pests

3 Table 1. Hymenopterous parasitoids of diamondback moth recorded from Hangzhou, China Species Stages of DBM attacked Relative importance a Ichneumomonidae Diadromus collaris (Gravenhorst) b Pupa ++ Itoplectis naranyae (Ashmead) b Pupa + Braconidae Cotesia plutellae Kurdjumov Larva +++ Eulophidae Oomyzus sokolowskii Kurdjumov Larva-pupa +++ Chalcididae Brachymeria excarinata Gahan b Pupa + Trichogrammatidae Trichogramma sp. egg + a +++ abundant and most important, ++ frequently seen and important, + occasionally seen b New records from China Table 2. Rates of parasitization of diamondback moth larvae in sprayed plots in Hangzhou, China Date Crop No. of Total no. % parasitized % parasitized by major species % of C. (yr./ samples of larvae in each plutellae month) sampled sample C. plutellae O. sokolowskii parasitized a Cauliflower , , 13.8 Cabbage 1 13 Cauliflower , 5., , 46.7, 15.6 Radish , 44.7, , 4.7, Cauliflower 2 72, 33.3, 7.4, 25.9, Cauliflower Cabbage Pak-choi Pak-choi Pak-choi Pak-choi 2 39, 7.7, 7.7 Cabbage 2 28., 46.3, 3.6., Cabbage 2 33, 11.6, Cabbage Cabbage Mustard , , Radish , , , Pak-choi , 2. 8 Radish Mustard Pak-choi , , 58.9, 2. 8 Cabbage Cabbage Cabbage Cabbage Cabbage Cabbage Cabbage Cauliflower Cauliflower a % of C. plutellae parasitized by secondary parasitoids. rates of parasitization also occurred in June-July and October November each year when DBM was most abundant. The rates during these peak periods were usually in the range of 6%, but reached 8 9% on several occasions. The parasitization was done mainly by two species, O. sokolowskii and D. collaris. O. sokolowskii was observed in the field from April to December each year, but D. collaris was observed only from May to July. We observed the distribution and sex ratio of the adults of O. sokolowskii coming out from 556 parasitized pupae of DBM. The average number of parasitoids per DBM pupa was 7.8±3.3, ranging from 1 to 23. Females accounted for 85.1% of total number of parasitoid adults. Of the 556 parasitized pupae, 18.4% produced only females, with an average of 6.3 individuals per pupa. These figures compare favorably with those reported by Ooi (1988). Observations were made on the overwintering of O. sokolowskii. Immature individuals collected before early October developed normally to adult emergence. From mid October onwards, an increasing proportion of individuals remained at the prepupal stage and would not develop to adult emergence until April May Status of DBM and other pests of crucifers and their biocontrol 63

4 % Parasitized Larvae Pupae Mean number/plant Larvae Pupae 9/ / 23 11/ / /2 Date (Month/day) Figure 1. Changes of mean numbers of diamondback moth larvae and pupae, and percentages of diamondback moth larvae and pupae parasitized by insect parasitoids in an unsprayed plot of common cabbage in autumn to winter 1995 in Hangzhou, China of the coming year (Table 4). Table 4 also shows that the individuals parasitizing host larvae entered into a state of overwintering earlier than those parasitizing pupae collected on the same day. Because O. sokolowskii is a larval-pupal parasitoid, a proportion of individuals collected from host pupae probably started their parasitization earlier when the hosts were at the larval stage, and the parasitoids had already developed to the pupal stage at the time of collection. These parasitoid pupae would keep on normal development to adult emergence. Discussion In the suburbs of Hangzhou, DBM is attacked by at least six primary parasitoids, of which C. plutellae, O. sokolowskii and D. collaris are the three major species. In this study, investigations of parasitization of DBM were conducted in both sprayed and unsprayed plots of crucifers. However, strictly speaking, the terms sprayed and unsprayed are not precise for what they describe. For the feasibility of sampling, the sprayed plots chosen for sampling in general received less chemical insecticides than average and also had higher density of DBM. Meanwhile, the occurrence and development of insect populations in unsprayed plots were undoubtedly affected by the heavy sprays in surrounding plots % Parasitization /9/12 /21 11/15 9/6/12 7/13 7/2 4 C. plutellae 3 O. sokolowskii 2 95/9/ / 23 11/ /12 28 Date (year/month/day) Figure 2. Changes of percentages of diamondback moth larvae parasitized by Cotesia plutellae and Oomyzus sokolowskii in a plot of cauliflower in 1989, in a plot of Pak-choi in 199, and in a plot of common cabbage in 1995, in Hangzhou, China 64 Proceedings: The Management of Diamondback Moth and Other Crucifer Pests

5 Table 3. Rates of parasitization of diamondback moth pupae in sprayed plots in Hangzhou, China Date Crop No. of Total no. % parasitized % parasitized by major species (yr. samples of pupae in each sample month) taken sampled O. sokolowskii D. collaris Cauliflower , , Cabbage 1 12 Pak-choi 1 Radish Cauliflower Cabbage Cauliflower , , Pak-choi Cabbage Pak-choi , , Pak-choi Pak-choi Pak-choi Cabbage Cabbage , , Cabbage , , Cabbage Cabbage Mustard , , Radish Pak-choi Pak-choi 2 58, Cabbage Mustard Cabbage Cabbage Cabbage Cabbage Cabbage Cabbage Cabbage Cabbage Table 4. Dates of adult emergence of O. sokolowskii collected from parasitized diamondback moth larvae or pupae in late autumn and early winter from the field in Hangzhou, China Dates of Individuals parasitizing host larvae Individuals parasitizing host larvae collection from the % emergence % emergence % emergence % emergence field (yr./ during Oct.-Nov. during April-May during Oct.-Nov. during April-May month/date) of the same year of the coming year of the same year of the coming year 89/9/2 /1... / / / / /7 12/ //5.. 12/2.. 12/28.. because of the small sizes of unsprayed plots. Nevertheless, the data collected in this study suggest strongly that insect parasitoids are active in the fields despite of the heavy spray of chemical insecticides in the crop systems over the years, and they can kill a substantial proportion of DBM population especially during periods when the pest is relatively abundant. Further, detailed investigations of DBM-parasitoids interactions, both in the laboratory and in the field, are warranted for quantifying the impact of parasitoids on DBM. The negative correlation in rates of parasitization of DBM larvae between C. plutellae and O. sokolowskii observed in this study suggests some sort of competition between the two parasitoids, which also warrants further investigation. In many parts of the world, Diadegma semiclausum Hellen (Hymenoptera: Ichneumonidae) Status of DBM and other pests of crucifers and their biocontrol 65

6 has made remarkable contribution to the control of DBM (Talekar and Shelton, 1993). This parasitoid seems to be absent from Hangzhou and has not been recorded from the Changjiang River Valley. The high temperatures in summer in the Changjiang River Valley are probably unfavorable to the survival of this parasitoid, because rates of parasitism by this parasitoid were reduced to very low levels at temperatures above 25 C (Talekar et al., 1992). However, in southern Queensland, Australia, where the weather is also characterized by hot summer, D. semiclausum survives well and seems to be an important natural enemy of DBM (John Hargreaves, personal communication). Thus, the introduction of D. semiclausum into the Changjiang River Valley may be considered. Acknowledgements This study forms part of an Australian-China cooperative project Improvement of Integrated Pest Management of Brassica Vegetable Crops in China and Australia (PN 9213), funded by the Australian Centre for International Agricultural Research. We also thank the Science and Technology Council of Zhejiang Province for support of the work conducted from 1989 to References Chao Chien-Zhou, Zhu Guo-Ren and Wu Shi-Chang (1991). Development of insecticide resistance and its management in Plutella xylostella. World Agriculture, 9: 3 32 (in Chinese) Chen Long-Ling, Kuang Ming-Zheng, Zhen Zhi-Dong, Cao Yi and Xu Wan-Weng. (1987). A survey of natural enemies of insect pests of vegetable crops in the suburbs of Guangzhou. In: Integrated Control of Insect Pests and Diseases in Vegetable Crops (ed. Fan Hui-Zhong et al.), pp , Guangzhou Science-Technology Press (in Chinese) Chien Ching-Chin and Chin Shui-Chen. (1985). The hyperparasitoids of Apanteles plutellae, a larval parasitoid of diamondback moth in Taiwan. Journal of Agricultural Research China, 34: (in Chinese, English, summary) Biever, K. D., Hostetter, D. L. and Kern, J. R. (1994). Evolution and implementation of a biological control- IPM system for crucifers: 24 year case history. American Entomologist, 4: 3 8 Liu Shu-Sheng, Brough, E. J., and Norton, G. A. (1995). ACIAR Workshop Report: Integrated Pest Management in Brassica Vegetable Crops. Cooperative Research Centre for Tropical Pest Management, Brisbane, Australia, 69 pp. Hargreaves, J. (1996). Personal communication. DPI Redlands Research Station, Cleveland, Qld 4163, Australia Ke Li-Dao and Fang Ju-Lian. (1982). Studies on the biology of the braconid wasp, Apanteles plutellae Kurdjumov. Acta Phytophylacica Sinica, 9: (in Chinese, English summary) Lu, Yan-Xiong. (1983). A preliminary survey of natural enemies of larvae of Plutella xylostella. Natural Enemies of Insects, 5: (in Chinese) Ooi, P. A. C. (1988). Laboratory studies of Tetrastichus sokolowskii. Entomophaga, 33: Ooi, P. A. C. (1992). Role of parasitoids in managing diamondback moth in the Cameron Highlands, Malaysia. In: Diamondback Moth and Other Crucifer Pests: Proceedings of the Second International Workshop (ed. N. S. Talekar), pp , Asian Vegetable Research and Development Centre, Tainan, Taiwan Shi Zu-Hua and Liu Shu-Sheng. (1995). A review of research and management of diamondback moth in China. In: ACIAR Workshop Report: Integrated Pest Management in Brassica Vegetable Crops (Liu Shu-sheng, E. J. Brough and G.A. Norton), Cooperative Research Centre for Tropical Pest Management, Brisbane, Australia Talekar, N. S. and Shelton, A. M. (1993). Biology, ecology, and management of the diamondback moth. Annual Review of Entomology, 38: Talekar, N. S., Yang, J. C. and Lee, S.T. (1992). Introduction of Diadegma semiclausum to control diamondback moth in Taiwan. In: Diamondback Moth and Other Crucifer Pests: Proceedings of the Second International Workshop (ed. N. S. Talekar), pp , Asian Vegetable Research and Development Centre, Tainan, Taiwan. Tang Zhen-Hua, Zhou Cheng-Li, Wu Shi-Chang, Zheng Hui- Zhong, Sheng Hui-Liang and GuYan-Zhen. (1992). Insecticide resistance and the effects of synergists in the diamondback moth from Shanghai. Acta phytophylacica Sinica, 19(2): (in Chinese, English summary). Wu Ju-Wen, Wang Jin-Rui, Wang Jun, Shi Ba-Dai, Wang Wei, Wang Bao-Zho, Dong Zhen-Hoa, Wei De-Zhong and Huang Qin-Feng A list of natural enemies of insect pests of vegetable crops in Beijing. Acta Agricultural Boriali-Sinica, 2: (in Chinese, English summary) 66 Proceedings: The Management of Diamondback Moth and Other Crucifer Pests