Printer Friendly

Parasitism of Plutella xylostella (Lepidoptera: Plutellidae) in southern Pakistan.

The diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), was a secondary pest of crucifer crops that has become a primary pest due to widespread application of insecticides that has reduced populations of natural enemies and caused widespread insecticide resistance in the host (Talekar & Shelton 1993). Now it is regarded as the most destructive insect of crucifers, occurring wherever crucifer crops are grown (Talekar & Shelton 1993; Shelton 2004). Plutella xylostella is one of the few insect species that have developed resistance to all major classes of insecticides, including recently introduced anthranilic diamides (Talekar & Shelton 1993; Shelton et al. 1993; Zhao et al. 2006; Wang & Wu 2012). Plutella xylostella ranks second for resistance to the highest number of insecticides with 95 active ingredients (APRD 2017). Two decades ago, the annual cost of controlling P. xylostella on a worldwide basis was estimated to be US$1 billion (Talekar & Shelton 1993). With monetary inflation and the increased production of crucifer vegetable and oil seed crops over the last 2 decades, the global management cost for P. xylostella is now estimated to be US$4 to 5 billion annually (Furlong et al. 2013).

Insecticide use to control P. xylostella by farmers in Asia and Africa generally is characterized by its overuse, with little regard to recommended integrated pest management (IPM) practices, and is seen as both increasingly expensive and unreliable (Grzywacz et al. 2010). A common problem with resource-poor farmers is their illiteracy and lack of understanding about how natural enemies work (Grzywacz et al. 2010). In Asia, another constraint to IPM programs is the availability of cheap, illegally imported insecticides (Sivapragasam 2004; Grzywacz et al. 2010). Failure of insecticides to provide adequate control has made P. xylostella the single most important constraint to commercial production of crucifer vegetables (Talekar & Shelton 1993). Outbreaks of P. xylostella in Southeast Asia can cause crop losses > 90% (Verkerk & Wright 1996). Production of crucifer vegetables in developing countries, including Pakistan, primarily is by smallholder farmers with intensive use of land, labor, and pesticides. The common method of insect management available to smallholder farmers in Pakistan is the frequent use of insecticides. Even with spraying every other d with cocktails of very toxic insecticides, farmers often are unable to save their crucifer crops, and resort to planting non-crucifer crops to avoid complete economic loss of the land (Abro et al. 1994).

More than 135 species of parasitoids attacking P. xylostella have been reported from various parts of the world (Delvare 2004), but only about 60 species appear to be important for biological control (Talekar & Shelton 1993). About a dozen species frequently are recovered in field studies (Furlong et al. 2013). Among larval parasitoids, the major ones, in order of decreasing importance, belong to the genera Diadegma, Cotesia, Apanteles, and Microplitis; among pupal parasitoids those in the genera Diadromus and Oomyzus appear to be most abundant (Lim 1986; Waterhouse 1992). Cotesia plutellae Kurdj (Hymenoptera: Braconidae) is native to Europe (Lloyd 1940) but has been reported from many countries (Sarfraz et al. 2005; Furlong et al. 2013). Similarly, Oomyzus sokolowskii Kurdj (Hymenoptera: Eulophidae), a gregarious larval-pupal primary parasitoid (Mushtaque 1990; Alam 1992; Fitton & Walker 1992), also has been recorded from many countries (Talekar & Shelton 1993; Sarfraz et al. 2005; Furlong et al. 2013).

No detailed research has been carried out on P. xylostella in this part of Pakistan, except for a few studies (Abro et al. 1994; Syed et al. 2012; Abro et al. 2013; Shah et al. 2013). Fundamental to all IPM programs should be the conservation of natural enemies (Furlong et al. 2013). As an alternative to reliance on broad-spectrum insecticides, natural enemies may provide an important component for an IPM program of this serious pest of crucifers in Pakistan. This study was undertaken to identify indigenous parasitoids attacking P. xylostella larvae and pupae in southern Pakistan.

Materials and Methods


Studies were performed in farmer fields in the Tando Allahyar District (25.4666[degrees]N, 68.7166[degrees]E) of Sindh located 200 km northeast of Karachi in southern Pakistan. The farmers are smallholders with 0.4 to 0.5 ha of cauliflower, Brassica oleracea var. botrytis (Brassicales: Brassicaceae). There were 2 experiments conducted on cauliflower plantings of 0.5 ha each during 2007. The summer cauliflower crop (cv 'Desi') was transplanted on 26 Jul 2007 and the winter crop (cv 'Snowdrift White Mountain') was transplanted on 14 Dec 2007. Both plantings of cauliflower used standard planting, fertilizer, and weeding practices. During 2008 and 2009, 2 additional plantings were made (cv 'Snowdrift White Mountain') with transplanting on 3 Dec 2008 in 0.5 ha and 6 Dec 2008 in 0.4 ha fields, respectively. Standard planting and fertilizer practices were used, and weeding was done by hand. In all plantings, farmers applied different insecticides to their crucifer vegetable crops, usually once a wk, with high doses of mixtures of chemical insecticides including organophosphates, pyrethroids, and insect growth regulators (Abro et al. 2013) for the management of different insect pests, including P. xylostella.


Starting 15 d after transplanting, 50 cauliflower plants were collected randomly every wk and searched for third to fourth instars and pupae off! xylostella. Insect samples were placed in a cooler and then returned to the laboratory where they were reared individually in 7 x 2.7 cm plastic cups. Larvae were provided insecticide-free cauliflower leaves as food, and the leaves were changed daily. Development of larvae and pupae was monitored daily until a P. xylostella adult parasitoid emerged or the larva died. The percent parasitism was calculated by dividing the number of emerged parasitoids by the total number of parasitoids, and P. xylostella adults recovered after rearing. The larvae that were unaccounted for after rearing, due to disease or other causes, were not included in the denominator (Russell 1987; Rowell et al. 2005). There were 12 weekly collections beginning 15 d after transplanting and ending at crop harvest. The 12 collections were divided into 2 sets (6 early and 6 late season) and each set was averaged to obtain means for that period.

The parasitoids collected were identified by the International Commonwealth Institute of Biological Control, Rawalpindi, Pakistan. The weekly average temperature was obtained from the meteorological department of Sindh Agriculture University to study the effect of temperature on pupal parasitism by determining the correlation between these 2 variables. Correlation also was carried out between pupal weight and number of parasitoids emerging from a single pupa. The percent parasitism means of summer and winter 2007 crops were compared using a paired t-test. All data were analyzed using 2-way analyses of variance (ANOVA) for a randomized complete block design. Treatment means were separated by least significant differences (LSD) and were reported as means [+ or -] SE (Zar 2010) on a computer employing statistical software (STATISTIX[R] VERSION-8.1, Analytical Software, Inc., Tallahassee, Florida, USA).


An experiment was conducted using weekly field collection of P. xylostella pupae parasitized by O. sokolowskii from Oct 2009 to Apr 2010. During each collection, 50 pupae were weighed individually on a Mettler AE 100 electronic balance (Mettler-Toledo, Columbus, Ohio, USA) and each pupa was placed into a labeled glass vial (3x2 cm) and observed daily until emergence of an adult P. xylostella or parasitoid, or death of the pupa. On emergence, parasitoids from each pupa were counted and recorded. The average weight of a P. xylostella pupa was calculated for those pupae that were parasitized at each collection date. Similarly, the number of parasitoids emerging from each pupa [= parasitoid load) was recorded. The number of parasitoids per pupa was grouped into parasitoid load classes (i.e.,1-5, 5-10) as shown in Figure 1. The average number of pupae parasitized per wk also was calculated.



Six species (3 larval and 3 pupal) of parasitoids were collected and 4 of these were identified to species level, the remaining 2 were identified to genus (Table 1). During the summer and winter seasons, C. plutellae was the most dominant larval parasitoid (Table 2). The parasitism rate of C. plutellae fluctuated between 2.3 and 52.2%. Early season larval parasitism of P. xylostella by C. plutellae from the 2007 summer crop averaged 8.2 (SE [+ or -] 1.4), and individual collections ranged from 2.7 to 12.3% (data not shown in Table 2). The late season parasitism averaged 11.0 (SE [+ or -] 0.8), and individual collections ranged from 8.2 and 13.7% (data not shown in Table 2). Although more parasitism by C. plutellae occurred in winter than in the summer crop, the difference was not significant. Plutella xylostella larval parasitism during the early winter crop of 2008 was lower than the late season but the difference was not significant. The percent parasitism recorded on winter-sown crops for 3 yr indicated a significant difference for collection dates within a season and for different seasons (F = 3.0; df = 11, 22; P < 0.05 for dates; F= 22.46; df = 2, 22; P < 0.01 for seasons). The parasitism rate of the larval parasitoid Cotesia sp. was low and remained in the range of 0.3 to 3.2%. The larval parasitoid Diadegma sp. was not present in the summer crop and its rate of parasitism remained < 0.5% (Table 2).


Pupal parasitism was lower than larval parasitism. The larval-pupal parasitoid O. sokolowskii was one of the other dominant parasitoids of P. xylostella occurring during the summer and winter seasons. Its parasitism range was 2.1 to 6.7%. The percent parasitism recorded on winter-sown crops for 3 yr was not significantly different for seasons [F = 0.00; df = 2, 105; P = 1.000). Diadromus collaris Gravenhorst, a pupal parasitoid of P. xylostella, was rare and found only in the winter crop during Jan when temperatures were low. Its parasitism range was 0.3 to 0.5%. Brachymeria excarinata Gahan, a pupal parasitoid of P. xylostella and a hyperparasitoid on C. plutellae, also was rare and not found in the summer season crop. In the winter crop, its parasitism was only 0.2% (Table 2).


A total of 1,150 P. xylostella pupae were collected from Oct 2009 to Apr 2010. From these, 182 were parasitized by O. sokolowskii and data were recorded for 167 parasitized pupae. The overall average parasitoid load per pupa was 8.4 [+ or -] 0.3 of O. sokolowskii adults. However, the parasitoid load varied enormously (Fig. 1). The majority (51.5%) of P. xylostella pupae had a parasitoid load in the 6-10 class intervals (average 7.9 [+ or -] 1.3). The maximum number of O. sokolowskii recorded per P. xylostella pupa was 21.0. There was a significant negative correlation between temperature and number of O. sokolowskii adults emerged (r = -0.538; df = 18; P[+ or -]0.02) (Fig. 2) and a significant positive correlation [r = 0.626; df = 18; P [+ or -]0.01) between P xylostella pupal weight and the number of O. sokolowskii adults emerged per pupa (Fig. 3).


The results indicated that larval parasitism could be an important mortality factor of P xylostella in southern Pakistan, even in commercial fields that are treated routinely with broad-spectrum insecticides. With the use of softer insecticides, one would expect parasitism rates to increase. The rate of larval parasitism of P xylostella was higher in the winter-spring crop compared with the summer crop. The highest larval parasitism of 65.2% was recorded 85 d after transplanting the winter crop, in the last wk of Feb. In a previous report from southern Pakistan, Mushtaque and Mohyuddin (1987) recorded 57.2% parasitism of P xylostella larvae by C. plutellae during the month of Jan. In Australia, Goodwin (1979) also reported high parasitoid activity during spring and summer, although extremely high temperatures during summer reduced the number of both the host and its parasitoids. In China, Liu et al. (2000a) demonstrated that C. plutellae was active throughout the yr but was less abundant and developed slowly during winter months. In the present studies, parasitism by C. plutellae ranged between 1.9 to 48.8% during different periods, which might be due to host density, because it has been reported that a density-dependent relationship exists between C. plutellae and its host (Nagarketti & Jayanth 1982) and C. plutellae are responsive numerically to increasing populations of P xylostella (Ooi 1992; Rowell et al. 1992). Cotesia plutellae thrive in environments that have not been sprayed with insecticides (Alam 1992), but also has been reported to be a dominant parasitoid of P xylostella in China, India, Thailand, and other countries, where it has been collected from fields sprayed with insecticides (Liu et al. 1997; Liu et al. 2000a; Krishnamoorthy 2004; Rowell et al. 2005; Sarfraz et al.2005).

The other Cotesia sp. was found parasitizing larvae of P xylostella during the season when temperatures were comparatively low. Additional studies are needed to confirm its identity and evaluate its effectiveness. Diadegma sp. also was observed during Dec and Jan only, when temperatures were low and its rate of parasitism was < 2%. Diadegma semiclausum Hellen is an important European species parasitizing P xylostella, and has been introduced in many tropical and subtropical Asian countries, but it has become established only in cooler areas where temperatures rarely exceed 28 [degrees]C (Talekar & Hu 1996; Rowell et al. 2005).

The parasitism of P xylostella by O. sokolowskii was greater during the winter-spring crop than the summer crop. This could be due to high temperatures during the summer season compared with the winter-spring crop. Mushtaque (1990) reported low parasitism of P xylostella by O. sokolowskii during Jul and Aug on cauliflower at Sahiwal, Pakistan. Oomyzus sokolowskii is an effective parasitoid found in many countries of the world (Talekar & Hu 1996; Wang et al. 1999; Silva-Torres et al. 2009). Because C plutellae and O. sokolowskii share similar ecological niches and co-exist in many countries (Talekar & Hu 1996), and both attack P. xylostella larvae with a slight overlap in their host stage preference (Talekar & Hu 1996), it is possible that both parasitoids may compete for host larvae in the field (Wang et al. 1999). Talekar & Hu (1996) reported that when P. xylostella larvae parasitized by C. plutellae were offered to O. sokolowskii, it readily parasitized the larvae and developed to the adult stage only if the C. plutellae parasitism was < 24 h old. Liu et al. (2000b) observed negative correlation in rates of parasitism of P. xylostella larvae by C. plutellae and O. sokolowskii, suggesting potential competition. Similar interactions also have been recorded by Shi et al. (2004) for D. semiclausum and O. sokolowskii.

The pupal parasitoid D. collaris was observed only during the month of Jan when temperatures were cooler in Southern Sindh, Pakistan, and its parasitism was < 1.0%. This pupal parasitoid has been introduced in many countries where it has shown some effectiveness in controlling P. xylostella in cooler highland crucifer vegetable production (Talekar & Hu 1996; Rowell et al. 2005). Brachymeria excarinata was recorded only twice during Mar from pupae of P. xylostella. Recently this parasitoid was recorded from Rawalpindi and Islamabad, Punjab, Pakistan, as a hyperparasitoid of Cotesia plutellae (Khaliq et al. 2016).

Oomyzus sokolowskii is a larval-pupal gregarious parasitoid naturally found parasitizing P. xlostella worldwide (Silva-Torres et al. 2009). This study indicated that on average, 8.4 parasitoids emerged from a single host pupa. Uematsu and Yamashita (2000) collected P. xylostella pupae from cabbage fields, and reported the average number of parasitoids emerging from a single host changed seasonally from 8.6 to 10.9 during autumn-winter and spring-summer cabbage crops, respectively. Under laboratory studies, Ooi (1988) recorded an average of 8.6 O. sokolowskii adults emerging from a single host. In the laboratory, Wang et al. (1999) parasitized different larval instars of P. xylostella and found the average number of O. sokolowskii emerging per host varied from 7.6 to 9.5. Liu et al. (2000b) found 7.8 [+ or -] 3.3 O. sokolowskii per P. xylostella pupa. In the laboratory, Silva-Torres et al. (2009) observed that progeny per host depended on the number of ovipositions per host by female O. sokolowskii. The number of progeny per host ranged from < 10 per 1 oviposition to > 20 per host per 3 ovipositions.

Resource availability is assumed higher in larger hosts based on the amount of food available inside the host for a developing parasitoid [Hardy et al. 1992; Zaviezo & Mills 2000). Greater resource availability is expected to promote parasitoid survival and produce offspring with larger body size, increased longevity, and higher fecundity rates than parasitoids emerging from low quality hosts (King 2000; Silva-Torres et al. 2009). There was a significant positive relationship between host pupal weight and number of O. sokolowskii parasitoids emerging per host pupa (Fig. 2). Nakamura and Noda (2002) also reported that number of progeny of O. sokolowskii per host increased significantly with host size. The study by Li et al. (2017) also suggested that O. sokolowskii females might optimize their clutch size in response to P. xylostella larval body size, and their sex allocation in response to clutch size. On the other hand, Silva-Torres et al. (2009) found no effect of host size on number of progeny per host in O. sokolowskii.

The present study found a negative relationship between the temperature and number of parasitoids emerging per host pupa. Working on parasitism of P. xylostella by O. sokolowskii, Talekar and Hu (1996) found that increasing temperatures from 10 to 35 [degrees]C significantly increased the parasitism of P. xylostella by O. sokolowskii. Wang et al. (1999) observed that the favorable temperature range for development, survival and reproduction of O. sokolowskii was 20 to 30 [degrees]C and observed that adult longevity of O. sokolowskii was significantly reduced when temperature increased from 20 to 30 [degrees]C. Furthermore, emergence was sharply reduced above 32.5 [degrees]C and parasitoids failed to emerge at 15 [degrees]C. Under laboratory experiments, Liu et al. (2000b) showed that the most favorable temperature for development, survival and reproduction of O. sokolowskii ranged from 20 to 30 [degrees]C, and temperatures below 20 [degrees]C or above 30 [degrees]C were unfavorable for its survival. The studies of Talekar & Hu (1996), Wang et al. (1999), and Liu et al. (2000b) were conducted under laboratory conditions, whereas our studies were conducted under field conditions where weather conditions vary enormously, and this could explain the differences.

This study indicated that C. plutellae and O. sokolowskii are important larval and pupal parasitoids and could play an important role in IPM of P. xylostella in Pakistan if they are conserved and, if possible, increased. This could be accomplished by habitat manipulation, diversifying the landscape, and providing plants that can offer nectar and other resources to natural enemies (Juric et al. 2017). Studies conducted by Johanowicz and Mitchell (2000) showed that sweet alyssum, Lobularia maritima (L.) Desv. (Brassicales: Brassicaceae), planted in cabbage fields increased adult parasitoid longevity and improved biological control of lepidopteran pests in Florida. Under field conditions, Lavandera et al. (2005) observed that the percentage of D. semiclausum that parasitized P. xylostella larvae in a treatment that included flowering plants was more than twice that in a non-flower treatment. Winkler et al. (2010) found significantly more D. semiclausum adults within a field of Brussels sprout fields bordered by dill, Anethum graveolens L. (Apiales: Apiaceae), as compared to the control. Application of softer, less toxic insecticides to natural enemies should be encouraged, instead of the older insecticides including organophosphates and carbamates that are widely used in Pakistan (Abro et al. 2013). These measures also should help reduce the risk to farmers, the environment, and the pesticide residue problem on crucifer vegetables in developing countries (Grzywacz et al. 2010), including Pakistan.

References Cited

Abro GH, Joyo AL, Syed TS. 1994. Ecology of diamondback moth, Plutella xylostella (L.) in Pakistan 1. Host plant preference. Pakistan Journal of Zoology 26: 35-38.

Abro GH, Syed TS, Kalhoro AN, Sheikh GH, Awan MS, Jessar RD, Shelton AM. 2013. Insecticides for control of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae) in Pakistan and factors that affect their toxicity. Crop Protection 52: 91-96.

Alam MM. 1992. Diamondback moth and its natural enemies in Jamaica and some other Caribbean Islands, pp. 223-244 In Talekar NS [ed.], Diamondback Moth and Other Crucifer Pests. Proceedings of the Second International Workshop. Asian Vegetable Research and Development Center, Shanhua, Taiwan.

APRD. Arthropod Pesticide Resistance Database. (last accessed 25 Nov 2017).

Delvare G. 2004. The taxonomic status and role of hymenoptera in the biological control of DBM, Plutella xylostella (L) (Lepidptera: Plutellidae), pp. 17-49 In Kirk AA, Bordat D [eds.], Improving Biocontrol of Plutella xylostella. Proceedings of the International Symposium, 21-24 Oct 2002, Montpellier, France. Fitton M, Walker A. 1992. Hymenopterous parasitoids associated with diamondback moth: the taxonomic dilemma, pp. 225-232 In Talekar NS [ed.] Diamondback Moth and Other Crucifer Pests. Proceedings of the Second International Workshop. Asian Vegetable Research and Development Center, Shanhua, Taiwan.

Furlong MJ, Wright DJ, Dosdall LM. 2013. Diamondback moth ecology and management: problems, progress, and prospects. Annual Review of Entomology 58: 517-541.

Goodwin S. 1979. Changes in number in the parasitoid complex associated with the diamondback moth, Plutella xylostella (L.) (Lepidoptera) in Victoria. Australian Journal of Zoology 27: 981-989.

Grzywacz D, Rossbach A, Rauf A, Russell DA, Srinivasan R, Shelton AM. 2010. Current control methods for diamondback moth and other Brassica insect pests and the prospects for improved management with lepidopteran-resistant Bt vegetable brassicas in Asia and Africa. Crop Protection 29: 68-79.

Hardy JCW, Griffiths NT, Godfray HCJ. 1992. Clutch size in a parasitoid wasp: a manipulation experiment. Journal of Animal Ecology 61: 121-129.

Johanowicz DL, Mitchell ER. 2000. Effects of sweet alyssum flowers on the longevity of the parasitoid wasps Cotesia marginiventris (Hymenoptera: Braconidae) and Diadegma insulare (Hymenoptera: Ichneumonidae). Florida Entomologist 83: 41-47.

Juric I, Salzburger W, Balmer O. 2017. Spread and global population structure of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) and its larval parasitoids Diadegma semiclausum and Diadegma fenestrale (Hymenoptera: Ichneumonidae) based on mtDNA. Bulletin of Entomological Research 107: 155-164.

Khaliq S, Aziz MA, Bodlah I, Ata-ul-Mohsin, Ahmad M. 2016. First record of Brachymeria excarinata Gahan, 1925 (Hymenoptera: Chalcididae) as hyperparasitoid of Cotesia plutellae (Hymenoptera: Braconidae) from Pakistan. Journal of Entomology and Zoology Studies 4: 718-721.

King BH. 2000. Sex ratio and oviposition responses to host age and the fitness consequences to mother and offspring in the parasitoid wasp Spalangia endius. Behavioral Ecology and Sociobiology 48: 316-320.

Krishnamoorthy A. 2004. Biological control of diamondback moth, Plutella xylostella (L): an Indian scenario with reference to past and future strategies, pp. 204-211 In Kirk AA, Bordat D, [eds.], Improving Biocontrol of Plutella xylostella. Proceedings of the International Symposium, 21-24 October 2002, Montpellier, France.

Lavandera B, Wratten SD, Shishehbor P, Worner S. 2005. Enhancing the effectiveness of the parasitoid Diadegma semiclausum (Helen): movement after use of nectar in the field. Biological Control 34: 152-158.

Li X, Zhu L, Meng L, Li B. 2017. Brood size and sex ratio in response to host quality and wasp traits in the gregarious parasitoid Oomyzus sokolowskii (Hymenoptera: Eulophidae). PeerJournal 5: e2919

Lim GS. 1986. Biological control of diamondback moth, pp. 159-172 In Talekar NS, Griggs TD [eds.] Diamondback Moth Management. Proceedings of the First International Workshop. Asian Vegetable Research and Development Center, Shanhua, Taiwan.

Liu S, Wang X, Guo S, He J, Song H. 1997. A survey of the parasitoids of Plutella xylostella and the seasonal abundance of the major parasitoids in Hangzhou, China, pp. 54-60 In Sivapragasam A, Loke WH, Hussan AK, Lim GS [eds.], The Management of Diamondback Moth and Other Crucifer Pests. Proceedings of the Third International Workshop, 29 Oct-10 Nov 1996, Kuala Lumpur, Malaysia.

Liu SS, Wang XG, Guo SJ, He JH, Shi ZH. 2000a. Seasonal abundance of the parasitoid complex associated with the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) in Hangzhou, China. Bulletin of Entomological Research 90: 221-231.

Liu SS, Wang X, Shi Z, Guo S, Liu SS, Wang X, Shi Z, Guo SJ. 2000b. Biology of Oomyzus sokolowskii and effect of temperature on its population parameters. Acta Entomology Sinica 43: 159-167.

Lloyd DC. 1940. Host selection by Hymenopterous parasites of the moth Plutella maculipennis. Proceedings of the Royal Society London B: Biological Science 128: 451-484.

Mushtaque M, Mohyuddin AI. 1987. Apanteles plutellae Kurdj. (Braconidae: Hymenoptera) an effective parasite of diamondback moth in Pakistan. Pakistan Journal of Zoology 19: 341-348.

Mushtaque M. 1990. Some studies on Tetrastichus sokolowskii Kurd. (Eulophidae: Hymenoptera) a parasitoid of diamondback moth in Pakistan. Pakistan Journal of Zoology 22: 37-43.

Nagarkatti S, Jayanth KP. 1982. Population dynamics of major insect pests of cabbage and their natural enemies in Bangalore district (India), pp. 325-347 In Heong KL, Lee BS, Lim TM, Teoh CH, Ibrahim Y [eds.], Proceedings of the International Conference on Plant Protection in the Tropics. 1-4 Mar 1982, Malaysian Plant Protection Society, Kuala Lumpur, Malaysia.

Nakamura A, Noda T. 2002. Effects of host age and size on clutch size and sex ratio of Oomyzus sokolowskii (Hymenoptera: Eulphidae), a larval-pupal parasitoid of Plutella xylostella (Lepidoptera: Yponomeutidae). Applied Entomology and Zoology 37: 319-322.

Ooi PAC. 1988. Laboratory studies of Tetrastichus sokolowskii. Entomophaga 33: 145-152.

Ooi PAC. 1992. Role of parasitoids in managing diamondback moth in the Cameron Highlands, Malaysia, pp. 255-262 In Talekar NS [ed.], Diamondback Moth and Other Cruciferous Pests. Proceedings of the Second International Workshop. Asian Vegetable Research and Development Center, Shanhua, Taiwan.

Rowell B, Jeerakan A, Wimol S. 1992. Crucifer seed crop pests, parasites and the potential for IPM in northern Thailand, pp. 551-563 In Talekar NS [ed.], Diamondback Moth and Other Cruciferous Pests. Proceedings of the Second International Workshop. Asian Vegetable Research and Development Center, Shanhua, Taiwan.

Rowell B, Bunsong N, Satthaporn K, Phithamma S, Doungsa-Ard C. 2005. Hymenopteran parasitoids of diamondback moth (Lepidoptera: Ypeunomutidae) in Northern Thailand. Journal of Economic Entomology 98: 449-456.

Russell DA. 1987. A simple method for improving estimates of percentage parasitism by insect parasitoids from field sampling of hosts. New Zealand Entomologist 10: 38-40.

Sarfraz M, Keddie AB, Dosdall LM. 2005. Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Science and Technology 15: 763-789.

Shah R, Shakeel A, Poswal A. 2013. Population dynamics of insect pests, parasitoids and predators in cabbage and cauliflower agro-ecosystems. Journal of Entomological Research 37: 129-137.

Shelton AM, Robertson JL, Tang JD, Eigenbrode SD, Preisler HK, Wilsey WT, Cooley RJ. 1993. Resistance of diamondback moth to Bacillus thurigiensis in the field. Journal of Economic Entomology 86: 697-705.

Shelton AM. 2004. Management of the diamondback moth: deja vu all over again?, pp. 3-8 In Endersby NM, Ridland PM [eds.], The Management of Diamondback Moth and Other Crucifer Pests. Proceedings of the Fourth International Workshop, 26-29Nov 2001. Melbourne, Australia.

Shi Z, Li Q, Li X, Liu SS. 2004. Interspecific competition between Diadegma semiclausum and Oomyzus sokolowskii, parasitoids of diamondback moth, Plutella xylostella, pp. 243-248 In Endersby NM, Ridland PM [eds], The Management of Diamondback Moth and Other Crucifer Pests. Proceedings of the Fourth International Workshop, 22-26 Nov 2001. Melbourne, Australia.

Silva-Torres CSA, Ramos-Filho IT, Torres JB, Barros R. 2009. Superparasitism and host size effects in Oomyzus sokolowskii, a parasitoid of diamondback moth. Entomologia Experimentalis et Applicata 133: 65-73.

Sivapragasam A. 2004. Brassica IPM adoption: progress and constraints in South East Asia, pp. 11-18 In Sivapragasam A, Loke WH, Kadir AH, Lim GS [eds.], The Management of Diamondback Moth and Other Crucifer Pests. Proceedings of the Third International Workshop, 29 Oct-1 Nov 1996. Kuala Lumpur, Malaysia.

Syed TS, Abro GH, Awan MS, Sattar M. 2012. The role of natural enemies to control diamondback moth, Plutella xylostella (L.) population in various seasons. Pakistan Journal of Zoology 44: 1479-1485.

Talekar NS, Shelton AM. 1993. Biology, ecology and management of the diamondback moth. Annual Review of Entomology 38: 275-301.

Talekar NS, Hu WJ. 1996. Characteristics of parasitism of Plutella xylostella (Lepidoptera: Plutellidae) by Oomyzus sokolowskii (Hymenoptera: Eulophidae). Entomophaga 41: 45-52.

Uematsu H, Yamashita T. 2000. Number and sex ratio of adult wasps, Oomyzus sokolowskii (Hymenoptera: Eulophidae), emerging from diamondback moth pupae collected in cabbage fields. Japan Journal of Applied Entomology and Zoology 44: 197-200.

Verkerk RHJ, Wright DJ. 1996. Multitrophic interactions and management of the diamondback moth: a review. Bulletin of Entomological Research 86: 205-216.

Wang X, Liu SS, Guo S, Lin W. 1999. Effects of host stages and temperature on population parameters of Omyzus sokolowskii, a larval-pupal parasitoid of Plutella xylostella. BioControl 44: 391-402.

Wang XG, Wu YD. 2012. High levels of resistance to chlorantraniliprole evolved in field population of Plutella xylostella. Journal of Economic Entomology 105: 1019-1023.

Waterhouse DF. 1992. Biological control of diamondback moth in the Pacific, pp. 231-234 In Talekar NS [ed.] Diamondback Moth and Other Crucifer Pests. Proceedings of the Second International Workshop. Asian Vegetable Research and Development Center, Shanhua, Taiwan.

Winkler K, Wackers FL, Termorshuizen AJ, van Lenteren JC. 2010. Assessing risks and benefits of floral supplements in conservation biological control. Bio-Control 55: 719-727.

Zar JH. 2010. Biostatistical Analysis. Prentice- Hall, New York, USA.

Zaviezo T, Mills N. 2000. Factors influencing the evolution in clutch size in a gregarious insect parasitoid. Journal of Animal Ecology 61: 1047-1057.

Zhao JZ, Collins HL, Li YX, Mau RFL, Thompson GD, Hertlein M, Andaloro JT, Boykin R, Shelton AM. 2006. Monitoring diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad, indoxacarb and emamectin benzoate. Journal of Economic Entomology 99: 176-181.

T. S. Syed (1), G. H. Abro (1,2), M. A. Shaikh (1), B. Mal (1), and A. M. Shelton (2,*)

(1) Sindh Agriculture University, Department of Entomology, Tandojam, Pakistan; Emails: (T. S. S.); (M. A. S.); (B. M.)

(2) Cornell University/NYSAES, Department of Entomology, Geneva, NY 14456, USA; Emails: (G. H. A.); (A. M. S.)

(*) Corresponding author; Email:

Caption: Fig. 1. Frequency distribution of number of Oomyzus sokolowskii adults emerging from a single Plutella xylostella pupa.

Caption: Fig. 2. Relationship between average temperature and average number of Oomyzus sokolowskii adults emerged per Plutella xylostella pupa.

Caption: Fig. 3. Relationship between average Plutella xylostella pupal weight and average number of Oomyzus sokolowskii adults emerged per pupa.
Table 1. Hymenopteran parasitoids of Plutella xylostella collected at
Tando Allahyar, Southern Sindh, Pakistan, 2007-2010.

Species                       Family

Cotesia plutellae Kurdj       Braconidae
Cotesia sp.                   Braconidae
Diadegma sp.                  Ichneumonidae
OomyZus sokolowskii Kurdj     Eulophidae
Diadromus collaris Grav.      Ichneumonidae
Brachymeria excarinata Gahan  Chalcididae

Species                       Type

Cotesia plutellae Kurdj       Solitary larval endoparasitoid
Cotesia sp.                   Solitary larval endoparasitoid
Diadegma sp.                  Solitary larval endoparasitoid
OomyZus sokolowskii Kurdj     Gregarious larval-pupal endoparasitoid
Diadromus collaris Grav.      Solitary pupal endoparasitoid
Brachymeria excarinata Gahan  Solitary pupal parasitoid

Table 2. Percent larval and pupal parasitism of Plutellaxylostella
collected at Tando Allahyra, Southern Sindh, Pakistan, 2007-2010.

                      Summer 2007                  Winter 2007
parasitoids     Larval            Pupal            Larval

C. plutellae     8.2 [+ or -]1.4                   18.2 [+ or -]3.5
Cotesia sp.      0                                  3.2 [+ or -]1.0
Diadegam sp.     0                                  0.4 [+ or -]0.2
O. sokolowskii                    2.1 [+ or -]0.4
D. collaris                       0
B. excarinata                     0
C. plutellae    11.0 [+ or -]0.8                   52.2 [+ or -]5.4
Cotesia sp.      0                                  2.4 [+ or -]0.5
Diadegma sp.     0                                  0.4 [+ or -]0.6
O. sokolowskii                    3.2 [+ or -]0.4
D. collaris                       0
B. excarinata                     0
Overall mean     9.6 [+ or -]0.8  2.7[+ or -]0.3   12.8 [+ or -] 8.3a

                Winter 2007                Winter 2008
parasitoids     Pupal            Larval             Pupal

C. plutellae                     4.7 [+ or -]0.5
Cotesia sp.                      2.1 [+ or -]0.4
Diadegam sp.                     0.3 [+ or -]0.0
O. sokolowskii  2.2 [+ or -]0.2                     2.1 [+ or -]0.2
D. collaris     0.3 [+ or -]0.0                     0.4 [+ or -]0.1
B. excarinata   0                                   0
C. plutellae                     31.5 [+ or -]6.4
Cotesia sp.                       2.6 [+ or -]0.5
Diadegma sp.                      0.4 [+ or -]0.1
O. sokolowskii  6.2 [+ or -]0.5                     5.6 [+ or -]0.4
D. collaris     0.5 [+ or -]0.1                     0.3 [+ or -]0.2
B. excarinata   0.2 [+ or -]0.2                     0
Overall mean    1.6 [+ or -]0.6   6.9[+ or -]4.9ab  1.4 [+ or -]0.9

                Winter 2009
parasitoids     Larval             Pupal

C. plutellae    2.3 [+ or -]0.2
Cotesia sp.     0.3 [+ or -]0.1
Diadegam sp.    0
O. sokolowskii                     3.1 [+ or -]0.6
D. collaris                        0.4 [+ or -]0.2
B. excarinata                      0.2 [+ or -]0.0
C. plutellae    3.1 [+ or -]0.4
Cotesia sp.     0.7 [+ or -]0.2
Diadegma sp.    0
O. sokolowskii                     6.7 [+ or -]0.6
D. collaris                        0.4 [+ or -]0.2
B. excarinata                      0.2 [+ or -]0.1
Overall mean    1.1 [+ or -] 0.5b  1.8 [+ or -]1.1

Means [+ or -] SE followed by different letters are significantly (P <
0.05) different from each other by LSD.

Please Note: Illustration(s) are not available due to copyright restrictions.
COPYRIGHT 2018 Florida Entomological Society
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2018 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Syed, T.S.; Abro, G.H.; Shaikh, M.A.; Mal, B.; Shelton, A.M.
Publication:Florida Entomologist
Article Type:Report
Geographic Code:9PAKI
Date:Jun 1, 2018
Previous Article:Population abundance, phenology, spatial distribution and a binominal sampling plan for Heliothrips haemorrhoidalis (Thysanoptera: Thripidae) in...
Next Article:Taxonomy of Calophya (Hemiptera: Calophyidae) species associated with Schinus terebinthifolia (Anacardiaceae).

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters |