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1 December 2012 Host Plants Alter the Reproductive Behavior of Pierisbrassicae (Lepidoptera: Pieridae) and its Solitary Larval Endo-Parasitoid, Hyposoter ebeninus (Hymenoptera: Ichneumonidae) in a Cruciferous Ecosystem
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The behavior of most destructive pest of cabbage, Pieris brassicae and that of its potential parasitoid, Hyposoter ebeninus, were studied under the influence of 4 common Brassica host plantspecies, cabbage, broccoli, cauliflower and knol-kohl. These host plant species were found to have considerable influence on egg distribution and leaf surface preference for oviposition and pupation. The number of egg masses was highest on knol-khol; however, the number of eggs per mass was highest on cabbage. Similarly, larval incidence was also highest on cabbage throughout the season, indicating that cabbage is the most preferred host. Natural parasitism on P. brassicae larvae by Hyposoter ebeninus was higher on knol-khol and cabbage. The weight of the third instar parasitized caterpillars was the highest on cabbage, suggesting that cabbage is the most favorable of these 4 hosts of P. brassicae for mass rearing of H. ebeninus. The development time of H. ebeninus was also shortest for cabbagereared larvae. Also the cocoon weight of the parasitoid was significantly higher when its host larvae were reared on cabbage. Overall from this study it can be concluded that, of the host plants evaluated, cabbage was preferred for oviposition by P. brassicae and its parasitoid. In addition, cabbage was found to be the best host plant for producing excellent quality H. ebeninus parasitoids.

Cole crops are a major component of vegetables in human diets. The greater cabbage white butterfly, Pieris brassicae (L.) (Lepidoptera: Pieridae) is one of the most serious pests of cabbage (Brassica oleracea var. capitata L.), cauliflower (Brassica oleracea var. botrytis L.) and many crucifers found along temperate, tropical and subtropical regions of the eastern hemishere (Jainlabdeen & Prasad 2004; Lal & Ram 2004; Younas et al. 2004). The young caterpillars feed gregariously on leaves, defoliating the plants and making insecticidal applications necessary for the cultivation of cole crops. Protective measures using different chemicals can cause undesirable side effects to human health, as the cole crops are being used as fresh vegetables in human diet. These chemicals are costly and cause hazardous health related issues in animals including humans (Bam 2008; Dasgupta et al. 2007). Moreover, uncontrolled use of synthetic chemicals cause severe damage to on-farm biodiversity as well.

Consequently, biological control is now, emerging as an important component of pest management (Balevski et al. 2007). Biological control of cruciferous pests, including cabbage butterflies, has traditionally relied on microbial pesticides, predators and parasitoids (Harcourt 1966; Biever & Wilkinson 1978; Peters & Coaker 1993; Van Driesche et al. 2003). Many workers have recommended the use of parasitoids for the management of P. brassicae (Harvey 2004; Patriche 2006; Bhat & Bhagat 2009).

Among the parasitoids attacking this pest, Cotesia glomerata (L.) (Hymenoptera: Braconidae) and Hyposoter ebeninus (Gravenhorst) (Hymenoptera: Ichneumonidae) are the 2 most important endo-larval parasitoids, with both being widely distributed across the world (Lozan et al., 2008; Harvey et al. 2010). Unlike C. glomerata, H. ebeninus (Supplementary Fig. 1) develops inside second and third instar larvae of Pieris spp. as a solitary endoparasite with the distinctive habit of forming a cocoon within the shrunken larval body (Supplementary Fig. 2) (Moiseeva 1976; Gauld 1988). Besides the generally recognized excellence of C. glomerata as a natural enemy, excellent bio-control potential of H. ebeninus has been reported from different parts of the world (Thakur & Deka 1997; Bhat & Bhagat 2009; Harvey et al. 2010; Razmi et al. 2011). Although, C. glomerata has been extensively studied around the world, H. ebeninus, is often ignored. Surprisingly, even basic biological studies on this species were not available until recent report of Harvey et al. (2010).

Fig. 1.

Distribution of eggs by Pieris brassicae influenced by different host plants (mean ± SEM). Different small letter over each bar indicate significant differences among treatments (Tukey's HSD, P ≤ 0.05).


In terms of fitness of the pest, selection of a good oviposition site is critical (Janz 2002). Ovipositional preferences of Pieris spp. are affected by several factors, including thickness of the plant's wax layer, physiological age and its biochemical composition (Bernays & Chapman 1994; Schoonhoven 1972; Schoonhoven et al. 1998), plant size (Reudler et al. 2008) and color (Radcliffe & Chapman 1966). Similarly, different host plants have considerable effects on host preference of P. brassicae; thus the latter's pattern and incidence of laying of eggs also varies on different hosts, even when these are grown together at same place under same physical conditions (Lytan & Firake 2012).

Tritrophic interactions (host plant-herbivoreparasitoid) play a crucial role in biological control of insect pests in every crop ecosystem. Many reports have suggested that female parasitoids usually detect their host by some important inherent cues (Fatouros et al. 2005), probably derived from the host plant in combination with herbivore (Geervliet et al. 1996). Parasitism by endoparasitoids can also induce physiological alterations in the herbivore (Gu et al. 2003), and the herbivore species consumes more food due to enhanced digestibility (Parker & Pinnell 1973; Sato et al. 1986; Schopf & Steinberger 1997; Nakamatsu et al. 2001) and grow faster than unparasitized larvae (Coleman et al. 1999). The characteristics of the host's growth, however, depend on the parasitoid species and the nature of the parasitism. In general, the herbivore eats more when parasitized by a gregarious species than by a solitary one.

Fig. 2.

Effect of different host plants on quantity of eggs per mass laid by Pieris brassicae (mean ± SEM). Different small letter over each bar indicate significant differences among treatments (Tukey's HSD, P ≤ 0.05).


The cabbage butterfly, P. brassicae, is one of the most widely studied insects. Although, extensive work has been done on several ecological aspects of this species (Ansari et al. 2012; Rather & Azaim 2009; Metspalu et al. 2003; David & Gardiner 1961); some important behavioral aspects have been overlooked or underestimated. Mass rearing and utilization of high quality bio-control agents may also be essential in successful biocontrol programs. Moreover, different host plants of the herbivore have considerable effect on the behavior of their natural enemies, especially koinobiont species. Accordingly, the host plant has significant influence on field parasitism, and growth and development of the parasitoid. A few studies on Cotesia have revealed improved biological parameters, when parasitoids developed inside herbivores reared on a highly favorable host plant (Hasan et al. 2011). Unlike Cotesia, the parasitoid H. ebeninus comparatively prefer early instar larvae for oviposition and develop into full grown pupae in third instar P. brassicae caterpillars. Therefore, weights of second and third instar parasitized larvae and cocoon parameters of H. ebeninus may vary on different host plants. There is a direct relationship between weight of the parasitoid and fecundity (Takagi 1985); hence a higher quality host plant of P. brassicae may produce a more efficient parasitoid for use in biocontrol programs.

Additionally, tritrophic communication also results in significant changes in the behavior of both the herbivore and its natural enemies. Globally, most of the bio-control attempts against crop pests have been unsuccessful, and such lack of success is frequently the result of too little knowledge of parasitoid biology and behavior, especially as related to bio-control potential (Beirne 1963; Peter 1993; Louda et al. 1997; Myers 2000; Hokkanen 2002). Therefore, the main objective of this study was to ascertain host plant-mediated effects on behavioral and biological aspects of the herbivore, P. brassicae and on its potential para- sitoid, H. ebeninus. In this study attempts were also undertaken to determine the level of quality of host plant of the P. brassicae for mass rearing of H. ebeninus, so that highly efficient parasitoid could be produced.


All experiments were carried out at an experimental field of the Division of Crop Improvement (Entomology), ICAR Research Complex for the NEH Region, Umiam, India during 2010–11. These experimental fields were situated at N 25° 41′ 01.91′ E91° 54′ 46.24′.

About 1-month old seedlings of 4 cruciferous crops, i.e., broccoli (Brassica oleracea L. var. italica Plenck; Capparales: Brassicaceae) (‘Pushpa’), cabbage (Brassica oleracea L. var. capitata L., ‘Wonder ball’), cauliflower (Brassica oleracea L. var. botrytis L., ‘Him Kiran’) and knol-khol (Brassica oleracea L. var. gongylodes L., ‘Sultan's knolkhol’ and ‘Early White Vienna’) were transplanted in the experimental field of the Entomology unit at Umiam. Experimental plot size was 3 × 3 m and each plot was separated the next by 1 m on all sides. All the necessary horticultural practices (i.e., irrigation, weeding and other intercultural operations) were followed for healthy growth of the crop. Butterflies were allowed to lay eggs on different host plants, and observations on number of eggs masses per plant and number of eggs per mass were taken at weekly intervals during the peak infestation period (Feb–Mar 2011). Similarly, leaf surface preference for oviposition and pupation was also studied by noting the site of egg laying and pupation (abaxial/adaxial surface) and the percent oviposition/pupation on the lower leaf (abaxial) surface was calculated. Observations on number of larvae per plant were also taken at weekly intervals during the peak infestation period of P. brassicae.

Natural larval parasitism by H. ebeninus was studied on the 4 above mentioned host plants of P. brassicae under field conditions. Observations were taken at weekly intervals during peak season of larval parasitism (Azad 1994; Lytan 2012; Firake, unpublished). The weight (g) of second and third instar parasitized caterpillars, developmental period (days), and adult emergence of H. ebeninus were recorded. Similarly, various cocoon parameters of H ebeninus, i.e., weight (g), length (mm) and diam (mm) were also noted. Larval parasitism throughout the season was considered for calculation of per cent parasitism. Parasitized caterpillars and parasitoid cocoon were weighed on digital electronic balance (Mettler Toledo® AB analytical balance, Model AB104-S). Diam of thorax (greatest width of cocoon) was measured with the help of ‘Vernier Caliper’ (Mitutoyo, Japan).

All the experiments were carried out in a Randomized Block Design (RBD) and each treatment was replicated 3 times. The complete experiment was repeated 3 times each in a different field. Differences between treatments were analyzed using ANOVA at a significance level of 0.05 and Tukey's HSD (Tukey's Honestly Significant Difference) test was used to find out the significant differences between mean values. Statistical software SPSS 13.0 for windows (SPSS, Inc., 2004) was used for overall statistical analysis.


Behavioral Response of Pieris brassicae to the Different Host Plants

Host plants of the P. brassicae significantly influenced its reproductive behavior. Numbers of egg masses of P. brassicae (L.) were significantly higher (F = 11.54, df = 11, P = 0.03) on knol-khol than other host plants (Fig. 1). Interestingly, the number of eggs per mass was also variable on different host plants, there being significantly more eggs per mass (F = 57.67, df = 11, P < 0.001) on cabbage followed by on cauliflower and knol-khol; while lowest on broccoli (Fig. 2).

Mean larval infestation was also highest (F = 13.44, df = 11, P = 0.002) on cabbage followed by cauliflower and knol-khol, and the least on broccoli (Fig. 3). Similarly, leaf surface preferences for oviposition and pupation were found to vary on different host plants (Fig. 4). Furthermore, preference for oviposition (Supplementary Fig. 3) and pupation on abaxial surface of leaves was significantly higher on cabbage (F = 31.20, df = 11, P = 0.000 and F = 6.56, df = 11, P = 0.002, respectively) followed by broccoli, knol-khol and cauliflower.

Effect of Different Host Plants of Pieris brassicae on Biological Parameters of Larval Parasitoid, Hyposoter ebeninus

Under field conditions, significantly higher larval parasitism was observed in knol-khol (F = 4.57, df = 11, P = 0.017) followed by cabbage and cauliflower and broccoli (Table 1). Effect of larvae reared on different hosts plants and subsequent parasitoid emergence from them was found to be non-significant (F = 1.08, df = 11, P = 0.39). However, it was higher on cabbage than on other crops.

Fig. 3.

Leaf surface preference for oviposition and pupation of Pieris brassicae influenced by different host plants (mean ± SEM). Different small letter over each bar with different arena indicate significant differences among treatments (Tukey's HSD, P ≤ 0.05).


Fig. 4.

Incidence of Pieris brassicae (mean ± SEM) on variable host plants over a season. Different small letter over each bar indicate significant differences among treatments (Tukey's HSD, P ≤ 0.05).


Effect of different hosts on the weight of the second instar parasitized caterpillar (SIPC) was also found to be non-significant (F = 0.97, df = 11, P = 0.43). Though, it was comparatively higher on cabbage than other crops. In contrast, the weight of the third instar parasitized caterpillar (TIPC) was significantly higher (F = 4.57, df = 11, P = 0.017) on cabbage followed in decreasing by cauliflower, broccoli and knol-khol (Table 1).

No significant differences in length and diameter of H. ebeninus cocoons (F = 0.645, df = 11, P = 0.59 and F = 2.16, df = 11, P = 1.33, respectively) were found, when parasitized caterpillars were reared on different host plants (Table 2). However, cocoon weight of the parasitoid was significantly higher (F = 12.34, df = 11, P = 0.00) on cabbage as well as on knol-khol fed larvae than the other host crops. Significant difference was also observed in developmental period of H. ebeninus (F = 3.52, df = 11, P = 0.03), when parasitized larvae reared on variable host plants. Development period was found to be lower on cabbage followed by cauliflower and broccoli; while it was extended on knol-khol (Table 1).


Several factors affect egg laying behavior of the female insect and her choice has considerable influence on the life history of her progeny. In the present study, P. brassicae laid significantly more eggs on the knol-khol plant followed in descending order by cauliflower, cabbage and broccoli. This behavior might be attributed to the host plant phenology and tenderness of leaves as found in knol-khol and cauliflower. However, the number of eggs per mass was found to be higher on cabbage, followed in descending order by cauliflower, knol-khol and broccoli. This behavior suggests that, although number of egg masses was few on cabbage the butterfly preferred to lay more eggs per mass on it. Therefore, the egg laying preference of P. brassicae may depend on the host size, stage and phenology. There are several factors that affect the oviposition behavior of butterflies. The thickness of wax layer, physiological age (Bernays & Chapman 1994), size (Reudler et al. 2008), color (Radcliffe & Chapman 1966) and biochemical composition (Schoonhoven et al. 1998) of the plant are among the most significant factors during selection of oviposition site by butterfly.




Some Pieris species tend to lay eggs in large masses when locating large-sized hosts with abundant leaves and such display of egg laying preference associated with host size has also been found for P. brassicae (Stamp 1980; Le Masurier 1994). Many reports also suggested that Pieris butterfly's flight and egg laying patterns are influenced by factors such as plant size, phenology, species, humidity content, nutrients, leaf color and plant chemistry (Jones 1977; Latheef & Irwin 1979; Myers 1985; Andow et al. 1986; Hern et al. 1996; Hooks & Johnson 2001). In several cases, insect egg laying behavior depended on various factors which included minimizing parasitic and predatory risk, selecting the most nutritious host, avoiding intra-specific competition for food and maximizing egg laying (Myers 1985; Ohsaki & Sato 1999). For that, the insect internally weighs the various stimuli and inhibitors perceived through visual, chemical, and mechanical signals (Thompson & Pellmyr 1991; Hern et al. 1996).

In our study, preference of lower leaf surface for oviposition as well as pupation was significantly higher in cabbage as compared to other cole crops. This behavior might be attributed to host phenology and also to avoid the risk of parasitism and predation of the early instar larvae. Earlier findings (Kobayashi 1965; Tagawa et al. 2008) revealed that, P. rapae crucivora eggs were generally found on the lower or abaxial surface of leaves in cabbage under field conditions. The strong bias towards the lower surface preference might be due to the egg-laying posture of females, which generally land on the leaf margins from above and bend their abdomens to lay eggs (Kobayashi 1963; Tagawa et al. 2008). Besides this, oviposition and pupation on the lower surface could avoid the increased risk of parasitism and predation on upper surface (Tagawa et al. 2008). In general, it is easier for the parasitoids to locate their host on the exposed leaf surface (Zago et al. 2010); so chances of parasitization of Pieris larvae are higher on upper leaf surface (Supplementary Fig. 4). Moreover, the phenology of the cabbage plant is completely different from the other 3 crops and especially cauliflower. The lower surface of the newly formed cabbage leaf is slightly concave (Supplementary Fig. 5), which is analogous to that of the upper leaf surface of cauliflower (Supplementary Fig. 6). Therefore, it is easier for the female butterfly to sit on such a concave leaf surface to lay eggs (Supplementary Fig. 7). As a result, maximum egg masses might be observed on lower leaf surface of cabbage.




Natural parasitism of P. brassicae by the larval parasitoid, H. ebeninus was highest on knol-khol followed by cabbage and it was comparatively less on cauliflower and broccoli. Tritrophic interaction has a noteworthy role in the biological control of crop pests. Host plants invite natural enemies to reduce herbivore pressure and in several cases the female parasitoid depends on smell of a host plant in combination with the herbivore for this purpose (Geervlietet al. 1996). The female can also detect its host on different plants, such as red and white cabbage, brussels sprouts (Brassica oleracea L. var. gemmifera Zenker) and nasturtium (Nasturtium sp.; Capparales: Brassicaceae); but the parasitoid seems to have a preference for host larvae in particular crop (Kaushal & Vats 1983; Geervliet et al. 1996). Therefore, the chemical composition of knol-khol might be different than other host plants, and it may be responsible for the attraction of parasitoids. Besides, the shapes of knol-khol and cabbage are also responsible for retaining the excreta and larval frass of P. brassicae on nearby leaves, which is most favorable for female parasitoids to locate their host larvae.

In the present findings, the weight of the second instar parasitized caterpillars was not affected by the different host plants. However, the weight of the third instar parasitized caterpillars was higher on cabbage followed by cauliflower and lower still on knol-khol. This effect on weight of the third instar parasitized caterpillars might be attributed to host plant phenology, because in the initial growth phase, the weight of the caterpillar is usually greater on the most suitable or preferred host plant, i.e., cabbage as observed by Talaei (2009). Furthermore, the plant population on which the caterpillars were reared differentially affects herbivore performance. The successful development of a parasitoid requires that the resources available in its hosts should satisfy their minimal nutritional requirements.. Therefore, host nutrition can have profound effects on the ability of a parasitoid to develop optimally (Hawkins 1994; Abrahamson & Weis 1997). Parasitoid host relations can be altered by the food plants of their respective hosts in 2 ways. Plants may affect the host selection activities of parasitoids (Mueller 1983) or the nutritional quality of the host's food can influence parasitoid growth and survival (House & Barlow 1961; DeMoras & Escher 1990).

There is a positive correlation between host plant suitability of the herbivore and its parasitoids. For instance, vigorous herbivores feed more and therefore produce more body mass on which the parasitoids can feed (Karowe & Schoonhoven 1992; Mueller 1983). Body size of the wasp is affected by the plant species on which its host caterpillar feeds (Price 1986; Guillot & Vinson 1973; Zohdy & Zohdy 1976; Beckage & Riddiford 1983; Mackauer 1986; Slansky 1986), where development of the wasps is synchronized with the host. Plant species may also change herbivore suitability and parasitoid development time (Pierce & Holloway 1912).

Changes in the food-plant may change the host's value for parasitoids (Shapiro 1956; Smith 1957; Cheng 1970; Greenblatt & Barbosa 1981; Karowe & Schoonhoven 1992), but few attempts have been made to measure and compare host quality in relation to the plant on which it feeds (Karowe & Schoonhoven 1992). The butterfly, P. brassicae (L.), developed faster and attained greater pupal mass when reared on black mustard, Brassica nigra L. than on Sinapis arvensis. Therefore, differences in host plant quality affect the herbivores and also its parasitoids showing that parasitoid performance is affected by herbivore diet (Gols et al. 2008a, 2008b).

Overall from this study it can be concluded that different host plants have significantly different effects on the ovipositional preference of an herbivore and on the behavior of its parasitoids. The female butterfly discriminates the leaf surface for oviposition/pupation and her preference depends on host plant phenology. Her preference may also express an avoidance of increased risk of predation/parasitism and intra specific competition. Host plants also invite natural enemies to reduce herbivore pressure; consequently natural field parasitism varies per host plant species. In addition, cabbage is found to be the best host plant of P. brassicae for producing excellent quality H. ebeninus parasitoids.


The authors are highly thankful to the Director, ICAR Research Complex for NEH Region, Umiam, Meghalaya for providing necessary laboratory facilities and funding for this research work.


  1. W. G. Abrahamson , and A. E. Weis 1997. Evolutionary ecology across three trophic levels. Princeton University Press, Princeton, NJ, USA. Google Scholar

  2. D. A. Andow , H. C. Nicholson, A. G, Wien , and H. R. Will-son 1986. Insect populations on cabbage grown with living mulches. Environ. Entomol. 15: 293–299. Google Scholar

  3. M. S Ansari , F Hasan , and N. Ahmad 2012. Influence of various host plants on the consumption and utilization of food by Pieris brassicae (Linn.). Bull. Entomol. Res., 102:231–237 Google Scholar

  4. N. Balevski , H. Draganov , M. Velichkova-Kojuharova , and S. Draganova 2007. Beneficial organisms (entomopathogens and entomophagous) on pests in the biocoenoses of cabbage in Bulgaria. J. Plant Sci. 44 (3): 230–235. Google Scholar

  5. E. Bauer , T. Trenczek , and S. Dorn 1998. Instar-dependent hemocyte changes in Pieris brassicae after parasitization by Cotesia glomerata. Entomol. Exp. Appl. 88: 49–58. Google Scholar

  6. N. E. Beckage , and L. M. Riddiford 1983. Growth and development of the endoparasitic wasp Apanteles congregatus dependence on host nutritional status and parasite load. Physiol. Entomol. 8: 231–241. Google Scholar

  7. B. P. Beirne 1963. Ecology in biological control. Mem. Entomol. Soc. Canada. 95: 7–10. Google Scholar

  8. E. Bernays , and R. F. Chapman 1994. Host-Plant Selection by Phytophagous Insects. Chapman and Hall, New York. 312 pp. Google Scholar

  9. M. D. Bhat , and R. C. Andbhagat 2009. Natural parasitism of Pieris rapae (L.) and Pontia daplidice (Lepidoptera: Pieridae) on Cruciferous Crops in Kashmir Valley: American Eurasian J. Agric. & Environ. Sci. 5(4): 590–591. Google Scholar

  10. K. D. Biever , and J. D. Wilkinson 1978. A stress-induced granulosis virus of Pieris rapae. Environ. Entomol. 7: 572–573. Google Scholar

  11. L. Cheng 1970. Timing of attack by Lyphadubia Fall. (Diptera: Tachinidae) on the winter moth, Operophthera brumata (Lepidoptera: Geometridae) as a factor affecting parasite success. J. Anim. Ecol. 39: 313–320. Google Scholar

  12. R. A. Coleman , A. M. Barker , and M. Fenner 1999. Parasitism of the Herbivore Pieris brassicae (L.) (Lepidoptera: Pieridae) by Cotesia glomerata L. (Hymenoptera: Braconidae) does not benefit the hostplant by reduction of herbivory. J. Appl. Entomol. 123: 171–177. Google Scholar

  13. S Dasgupta , C Meisner , and H. Mainul 2007, A pinch or a pint? Evidence of pesticide overuse in Bangladesh, J. Agri. Econ, 58: 91–114 Google Scholar

  14. W. A. L David , and B. O. C. Gardiner 1961. The mating behaviour of Pieris brassicae (L.) in a laboratory culture. Bull. Entomol. Res., 52: 263–280 Google Scholar

  15. C. M. Demoras , and M. C. Escher 1990. Interactions in Entomology: Plant-Parasitoid interaction in tritrophic system. J. Entomol. Sci. 34(1): 31–39. Google Scholar

  16. N. E. Fatouros , J. J. A. Van Loon , and K. A. Hordijk 2005. Herbivore-induced plant volatiles mediate inflight host discrimination by parasitoids. J. Chem. Ecol. 31: 2033–2047. Google Scholar

  17. B. O. C. Gardiner 1978. Instar number and pupal coloration in Palestinian Pieris brassicae nepalensis. Doubleday. J. Hill Res. 2: 45–55. Google Scholar

  18. I. D. Gauld 1988. Evolutionary patterns of host utilization by ichneumonoid parasitoids (Hymenoptera: Ichneumonoidea and Braconidae). Biol. J. Linn. Soc. 57: 137–162. Google Scholar

  19. J. B. F. Geervliet , J. Brodeur , and L. E. M. Vet 1996. The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomol. Exp. Appl. 81: 125–132. Google Scholar

  20. R. Gols , R. Wagenaar , T. Bukovinszky , N. Van Dam , and M. Dicke 2008a. Genetic variation in the defense chemistry of wild cabbage affects native herbivores and their endoparasitoids. Ecol. 89: 1616–26. Google Scholar

  21. R. Gols , L. M. A. Witjes , J. J. A. Van Loon , M. A. Posthumus , M. Dicke , and J. A. Harvey 2008b. The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid. Entomol. Exp. Appl. 128: 99–108. Google Scholar

  22. J. A. Greenblatt , and P. Barbosa 1981. Effects of host's diet on two pupal parasitoids of the gypsy moth: Brachymeria intermedia (Nees) and Coccygo mimusturionellae (L.). J. Appl. Ecol. 18: 1–10. Google Scholar

  23. H. Gu , Q. Wang , and S. Dorn 2003. Superparasitism in Cotesia glomerata: Response of hosts and consequences for parasitoids. Ecol. Entomol. 28: 422–431. Google Scholar

  24. F. S. Guillot , and S. B. Vinson 1973. Effect of parasitism by Cardichiles nigriceps on food consumption and utilization by Heliothis virescens. J. Insect Physiol. 19: 2073–2082. Google Scholar

  25. D. G. Harcourt 1966. Major factors in the survival of the immature stages of Pieris rapae (L.). Canadian Entomol. 98: 653–662. Google Scholar

  26. J. A. Harvey 2004. Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness. Ecol. Entomol. 25: 267–278. Google Scholar

  27. J. A. Harvey , E. H. Poelman , and R. Gols 2010. Development and host utilization in Hyposoter ebeninus (Hymenoptera: Ichneumonidae), a solitary endoparasitoid of Pieris rapae and P. brassicae caterpillars (Lepidoptera: Pieridae). Biol. Control 53: 312–318. Google Scholar

  28. F. Hasan , M. S. Ansari , and N. Ahmad 2011. Foraging of Host-Habitat and Superparasitism in Cotesia glomerata: A gregarious parasitoid of Pieris brassicae. J. Insect Behav. 24: 363–369. Google Scholar

  29. B. A. Hawkins 1994. Pattern and Process in Host—parasitoid Interactions. Cambridge University Press, Cambridge. Google Scholar

  30. A Hern , G. Edwards , and R. McKinlay 1996. A review of the pre-oviposition behaviour of the small cabbage white butterfly, Pieris rapae (Lepidoptera: Pieridae). Ann. Appl. Biol. 128: 349–371. Google Scholar

  31. H. Hokkanen 2002. Biological Control: Successes and Failures, pp. 81–84 In D. Pimentai [ed.], Encyclopedia of Pest Management, CRC Press. doi:  10.1201/NOE0824706326.ch33  Google Scholar

  32. C. Hooks , and M. W. Johnson 2001. Broccoli growth parameters and level of head infestations in simple and mixed plantings: impact of increased flora diversification. Ann. Appl. Biol. 138: 269–280. Google Scholar

  33. J. L. House , and J. S. Barlow 1961. Effects of different diets of a host Agria afinia (Fall.) (Diptera: Sarcophagidae), on the development of a parasitoid Aphareta pallipes (Say) (Hymenoptera: Braconidae). Canadian Entomol. 93: 1041–1044. Google Scholar

  34. S Jainulabdeen , and S. K. Prasad 2004. Severe infection of cabbage butterfly, Pieris brassicae (L.) on six species of Brassica and effect of abiotic factor on its population dynamics. J. Entomol. Res. 28:193–197 Google Scholar

  35. N. Janz 2002. Evolutionary ecology of oviposition strategies, pp. 349–376 In M. Hilker and T. Meiners [eds.], Chemoecology of insect eggs and egg deposition. Blackwell, Berlin. Google Scholar

  36. R. E. Jones 1977. Movements, patterns and egg distribution in cabbage butterflies. J. Animal Ecol. 46: 195–212. Google Scholar

  37. D. N. Karowe , and L. M. Schoonhoven 1992. Interactions among three trophic levels: the influence of host plant on performance of Pieris brassicae and its parasitoid, Cotesia glomerata. Entomol. Exp. Appl. 62(3): 241–251. Google Scholar

  38. B. R. Kaushal , and L. K. Vats 1983. Energy budget of Pieris brassicae (L.) larvae fed on four host plant species. Agri. Ecosyst. Environ. 10: 385–398. Google Scholar

  39. S. Kobayashi 1963. The distribution of Pieris rapae crucivora on cabbage leaves. Japanese J. Ecol. 13: 226–230. (In Japanese with English summary.) Google Scholar

  40. S. Kobayashi 1965. Influence of adult density upon the oviposition site in the cabbage butterfly, Pieris rapae crucivora. Japan J. Ecol. 15: 35–38. (In Japanese with English summary.) Google Scholar

  41. M. N. Lal , and B. Ram 2004. Cabbage butterfly, Pieris brassicae L. An upcoming menance for Brassicae oilseed crop in northern India. Cruciferae Newsl. 25: 83–86 Google Scholar

  42. M. A. Latheef , and R. D. Irwin 1979. The effect of companionate planting on lepidopteran pests of cabbage. Canadian Entomol. 111: 863–864. Google Scholar

  43. A. D. Le Masurier 1990. Host discrimination by Cotesia (= Apanteles) glomerata parasitizing Pieris brassicae.Entomol. Exp. Appl. 54: 65–72. Google Scholar

  44. A. D. Le Masurier 1994.Costs and benefits of egg clustering in Pieris brassicae. J. Animal Ecol. 63: 677–685. Google Scholar

  45. Z Liu , D. Li , P. Gong , and K. Wu 2004. Life table studies of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on different host plants. Environ. Entomol. 33: 1570–1576. Google Scholar

  46. S Louda , D Kendall , J Connor , and D. Simberloff 1997. Ecological effects of an insect introduced for the biological control of weeds. Science 277: 1088– 1090. Google Scholar

  47. A. I. Lozan , M. T. Monaghan , K. Spitzer , J. Jaros , M. Zurovcova , and V. Broz 2008. DNA-based confirmation that the parasitic wasp Cotesia glomerata (Braconidae, Hymenoptera) is a new threat to endemic butterflies of the Canary Islands. Conserv. Genet. 9: 1431–1437 Google Scholar

  48. D. Lytan , and D. M. Firake 2012. Effects of different host plants and rearing atmosphere on life cycle of large white cabbage butterfly, Pieris brassicae (Linnaeus). Arch. Phytopath. Plant Prot. 45: 1819–1825. Google Scholar

  49. M. MacKauer 1986. Growth and developmental interactions in some aphids and their hymenopterous parasites. J. Insect Physiol. 32: 275–280. Google Scholar

  50. L Metspalu , K Hiiesaar , and K. Jogar 2003. Plant influencing behavior of large white cabbage butterfly, Pieris brassicae (L.). Agro. Res. 1: 211–220 Google Scholar

  51. T. S. Moiseeva 1976. The protective reaction of insects. Zashchita Rastenii. 8: 21–22. Google Scholar

  52. T. F. Mueller 1983. The effect of plants on the host relations of a specialist parasitoid of Heliothis larvae. Entomol. Exp. Appl. 34: 78–84. Google Scholar

  53. J. Myers 1985. Effect of physiological condition of the host plant on the ovipositional choice of cabbage white butterfly, Pieris rapae. J. Animal Ecol. 54: 193–204. Google Scholar

  54. J. H. Myers 2000. What can we learn from biological control failures?, pp. 151–154 In N. R. Spencer [ed.], Proc. X Intl. Symp. on Biological Control of Weeds , 4–14 July 1999, Montana State University, Bozeman, MT, USA. Google Scholar

  55. Y. Nakamatsu , Y. Gyotoku , and T. Tanaka 2001. The endoparasitoid Cotesia kariyai (Ck) regulates the growth and metabolic efficiency of Pseudaletia separata larvae by venom and Ck polydnavirus. J. Insect Physiol. 47: 573–584. Google Scholar

  56. N. Ohsaki , and Y. Sato 1999. The role of parasitoids in evolution of habitat and larval food plant preference by three Pieris butterflies. Res. Pop. Ecol. 41: 107–119. Google Scholar

  57. F. D. Parker , and R. E. Pinnell 1973. Effect on food consumption of the imported cabbage worm when parasitized by two species of Apanteles. Environ. Entomol. 2: 216–219. Google Scholar

  58. G. Patriche 2006. Parasitoid assemblages of the defoliator Noctuidae spp. in cabbage crops; Studiisi. Comunicari, complexul. Muzeal de StinteleNaturii “Ion Borcea”, vol. 21: 495–501. Bacaus, Romania. Google Scholar

  59. S. Peter 1993. Why do natural enemies fail in classical biological control programs? Amer. Entomol. 31: 31–37. Google Scholar

  60. S. E. O. Peters , and T. H. Coaker 1993. The enhancement of Pieris brassicae (L.) (Lepidoptera: Pieridae) granulosis virus infection by microbial and synthetic insecticides. Z. Angew. Entomol. 116: 72–79. Google Scholar

  61. W. D. Pierce , and T. E. Holloway 1912. Notes on the biology of Chelonus texanus. J. Econ. Entomol. 5: 425–428. Google Scholar

  62. P. W. Price 1986. Ecological aspects of host plant resistance and biological control: interactions among three trophic levels, pp. 11–30 In D. J. Boethel and R. D. Eikenbary [eds.], Interactions of plant resistance and parasitoids and predators of insects. John Wiley and Sons, New York. Google Scholar

  63. E. B. Radcliffe , and R. K. Chapman 1966. Varietal resistance to insect attack in various cruciferous crops. J. Econ. Entomol. 59: 120–125. Google Scholar

  64. M. H. Rahman 1970. Effect of parasitism on food consumption of Pieris rapae larvae. J. Econ. Entomol. 63: 820–821. Google Scholar

  65. A. H. Rather , and M. N. Azim 2009. Feeding response in Pieris brassicae larvae to host/non-host plants. World J. Agric. Sci. 5: 143–145 Google Scholar

  66. M. Razmi , Y. Karimpour , M. H. Safaralizadeh , and S. A. Safavi 2011. Parasitoid complex of cabbage large white butterfly Pieris brassicae (L.) (Lepidoptera: Pieridae) in Urmia with new records from Iran. J. Plant Prot. Res. 51: 248–251. Google Scholar

  67. J. H. T. Reudler , A. Biere , J. A. Harvey , and S. Van Nouhuys 2008. Oviposition cues for a specialist butterfly-plant chemistry and size. J. Chem. Ecol. 34: 1202–1212. Google Scholar

  68. Y. Sato , J. Tagawa , and T. Hidaka 1986. Effects of the gregarious parasitoids Apanteles rufricus and A. kariyai on host growth and development. J. Insect Physiol. 32: 281–286. Google Scholar

  69. L. M. Schoonhoven 1972. Secondary plant substances and insects. Phytochem. 5: 197–224. Google Scholar

  70. L. M. Schoonhoven , T. Jermy , and J. J. A. Van Loon 1998. Insect-plant biology from physiology to evolution. Chapman & Hall. London Google Scholar

  71. A. Schopf , and P. Steinberger 1997 The influence of the endoparasitic wasp, Glyptapanteles liparidis (Hymenoptera: Braconidae) on the growth, food consumption, and food utilization of its host larvae, Lymantria dispar (Lepidoptera: Lymantridae). European J. Entomol. 93: 555–568 Google Scholar

  72. V. A. Shapiro 1956. The influence of the nutritional regimes of the host on the growth of certain parasites. Zhurnal Obshcher Biol. 17: 218–227. Google Scholar

  73. F. Slansky 1978. Utilization of energy and nitrogen by larvae of the imported cabbage worm, Pieris rapae as affected by parasitism by Apanteles glomeratus. Environ. Entomol. 17: 179–185. Google Scholar

  74. F. Slansky 1986. Nutritional ecology of endoparasitic insects and their hosts: An overview. J. Insect Physiol. 32: 255–261. Google Scholar

  75. J. M. Smith 1957. Effects of the food of California red scale, Aonidiella aurantii (Mask.), on the reproduction of its hymenopterous parasites. Canadian Entomol. 89: 219–230. Google Scholar

  76. SPSS INC. 2004. SPSS for Windows, Release 13.0. SPSS, Inc., Chicago, Illinois, USA. Google Scholar

  77. N. Stamp 1980. Egg deposition patterns in butterflies: why do some species cluster their eggs rather than deposit them singly? American Nat. 115: 367–380. Google Scholar

  78. J. Tagawa , J. A. Matsushita , and T. Watanabe 2008. Leaf surface preference in the cabbage worm, Pieris rapae crucivora, and parasitism by the gregarious parasitoid Cotesia glomerata. Entomol. Exp. Appl. 129: 37–43. Google Scholar

  79. M. Takagi , 1985. The reproductive strategy of the gregarious parasitoid, Pteromalus puparum (Hymenoptera: Pteromalidae). Oecol. 68:1–6. Google Scholar

  80. R. Talaei 2009. Influences of plant species on life history traits of Cotesia rubecula (Hymenoptera: Braconidae) and its host Pieris rapae (Lepidotera: Pieridae). Biol. Control 51: 72–75. Google Scholar

  81. N. S. A. Thakur , and T. C. Deka 1997. Ecological studies on the cabbage butterfly, Pieris brassicae in North Eastern India. Pest Mgt. Hort. Ecosyst. 3(3): 13–15. Google Scholar

  82. J. N. Thompson , and O. Pellmyr 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Annu. Rev. Entomol. 36: 65–89. Google Scholar

  83. R. G. Van Driesche , C. Nunn , N. Kreke , B. Goldstein , and J. Benson 2003. Laboratory and field host preferences of introduced Cotesia spp. parasitoids (Hymenoptera: Braconidae) between native and invasive Pieris butterflies. Biol. Control. 28: 214–221. Google Scholar

  84. H. B Zago , R. Barros , J. B. Torres , and D. Pratissoli 2010. Distribuição de ovos de Plutella xylostella (L.) (Lepidoptera: Plutellidae) e o parasitismo por Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Neotrop. Entomol. 39: 241– 247. Google Scholar

  85. N. Zohdy , and M. Zohdy 1976. On the effect of the food of Myzus persicae Sulz on the hymenopteran parasite Aphelinus asychis Walker. Oecol. 26: 185–191. Google Scholar

D. M. Firake, Damitre Lytan, G. T. Behere, and N. S. Azad Thakur "Host Plants Alter the Reproductive Behavior of Pierisbrassicae (Lepidoptera: Pieridae) and its Solitary Larval Endo-Parasitoid, Hyposoter ebeninus (Hymenoptera: Ichneumonidae) in a Cruciferous Ecosystem," Florida Entomologist 95(4), (1 December 2012).
Published: 1 December 2012

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