Effects of Plant Age and Insect Densities on Parasitism by Cotesia vestalis (Haliday)

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1 Middle-East Journal of Scientific Research 24 (5): , 2016 ISSN IDOSI Publications, 2016 DOI: /idosi.mejsr Effects of Plant Age and Insect Densities on Parasitism by Cotesia vestalis (Haliday) S. Amalina, Y. Mohd Hanifah, M.N. Mohamad Roff and A.B. Idris 1 School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Bangi, Selangor, Malaysia 2 Plant and Soil Science Research Centre, Malaysian Agricultural Research and Development Institute (MARDI), PO Box 12301, Kuala Lumpur, Malaysia Abstract: Cruciferous crops are important vegetables in Malaysia. One of the limiting factors to successful production of these vegetables is the infestation of insect pest, the diamondback moth (DBM), Plutella xylostella (L.) (Lepidoptera: Plutellidae). In controlling the pest, the effectiveness of its natural enemies could be influenced by various factors. In this study, we investigated the effects of plant age infested with different density of DBM larvae on parasitism by Cotesia vestalis (Haliday) (Hymenoptera: Braconidae), one of its important natural enemy. The experiment was conducted under glasshouse conditions by using three ages (4, 8 and 12-week-old plants) of cabbage plants, Brassica oleracea L. var. capitata cv. K-K Cross. Three different levels of DBM larvae densities (10, 20 and 30 larvae per plant) were tested separately with different exposure durations (1 h, 3 h and 6 h). The experiments were arranged using completely randomized design (CRD) with five replicates. There was a significant difference (P < 0.05) in mean percentage parasitism of DBM larvae by C. vestalis among different ages of cabbage plants and exposure durations of C. vestalis to its host larvae. However, host densities had no significant effect (P > 0.05) on percentage parasitism of DBM larvae. It showed that percentage parasitism was negatively and significantly correlated (P < 0.05) with plant age, while no significant relationship (P > 0.05) was found between the percentage parasitism and exposure durations. Results showed that DBM larvae feeding on 4-week-old cabbages were most parasitized at all levels of host densities. Results of this study indicate that parasitism by C. vestalis was influenced by age of plants fed by its DBM host. Young cabbage plants seemed to be more attractive to the foraging C. vestalis and influenced its choice to parasitize more DBM larvae on these plants. Thus, the use of biopesticides should be considered when integrating biological control agents such as C. vestalis in controlling DBM during young age of cabbage. Key words: Plutella xylostella Cotesia vestalis Parasitism Plant age Host density INTRODUCTION reproduction potential, the disruption and lack of natural enemies and its ability to become resistant to a wide range Cabbage is a popular cruciferous crop around the of insecticide products including Bacillus thuringiensis world. One of the major insect pests of this crop in many (Bt) [5,6,7]. Hence, the integrated pest management (IPM) parts of the world including in Malaysia is diamondback has been developed as an alternative approach to control moth (DBM), Plutella xylostella (L.) (Lepidoptera: the DBM. This includes the manipulation of its Plutellidae) [1,2]. The DBM larvae feed all above ground parasitoids as biological control agents [8]. parts of cabbage plants, which reducing yield quality and Plants play significant roles in mediating some quantity [3,4]. There are several reasons why this species interactions between herbivores and their natural enemies, still remains as one of the most destructive insect pest of which include influencing the effectiveness of the crucifers worldwide. Among the reasons are its high herbivores natural enemies [9]. Infochemicals derived Corresponding Author: S. Amalina, School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Bangi, Selangor, Malaysia. 1839

2 from damaged food plant of the herbivores, together with No insecticides were applied to the plants. Three ages of the chemical cues originating from the herbivore plants were used in this study; 4, 8 and 12-week-old themselves are well-known signals that help parasitoids plants. The three ages of cabbage plants correspond to to successful locate their hosts [10-14]. Previous studies the developmental stages of second, fourth and sixth showed that parasitism of DBM larvae by parasitoids may cabbage plants as described by Andaloro et al. [37]. differ among different species [11,15], varieties [16], cultivars [17] and plant age of DBM host plants [18-20]. Insects: Cotesia vestalis and its host, DBM larvae were Regarding plant age, younger plants showed to contain originally collected from brassica vegetable farms in Kuala higher content of plant secondary metabolites, which play Lumpur. No specific permits were required for the field an important role in attracting parasitoids [21,22]. sampling and permission was granted by the landowners. Therefore, parasitism by parasitoids should be influenced Both colonies were raised on Brassica campestris L. in by ontogenetic changes in the food plant of their hosts. mesh cages (45 cm 45 cm 45 cm) under laboratory Cotesia vestalis (Haliday) (Hymenoptera: conditions in MARDI at 25 ± 2 C, 63 ± 5% RH and a Braconidae) is a solitary larval endoparasitoid of DBM photoperiod of 12:12 (L:D) h. The parasitoids were reared [23]. In Malaysia, it was discovered in the 1970s [24] and by using DBM larvae as hosts. Adult insects of the species is considered one of the major biological C. vestalis and DBM were provided with cotton wool control agents in IPM programme for DBM [2]. soaked with 10% (v:v) honey solution. The insects had This specialist parasitoid of DBM uses volatile chemicals been reared over several generations before the produced by wounds made by DBM larvae to locate experiments were conducted. For the experimental host-infested plants [12,25,26]. On the plants, females may purpose, cocoons of C. vestalis were collected from the exploit the cues originating from their host to successfully stock culture and placed in mesh cage (35 cm 20 cm 20 locate the hosts for parasitization [27,28]. Both field and cm) for adult emergence and mating. These adults were laboratory studies showed that parasitism by C. vestalis maintained without any contact with plant material or host produced inconsistent pattern of parasitism against the larvae and therefore they are referred to as naive density of DBM. Although density-dependent parasitism parasitoids. Only two to five-day-old mated naive females has been more commonly reported [18,29-33], were used in the tests [38] and they were acclimatized negative correlations and no correlation between the under the glasshouse conditions for 1-2 h before the tests percentage of parasitism and host density were also well started [26]. documented [11,20,28,31,34]. Therefore, the objective of this work was to study the effects of cabbage plants of Parasitism by Cotesia vestalis: The experiment was different ages infested with different densities of DBM larvae on parasitism by C. vestalis. The results of this study are expected to provide valuable information for effective control of DBM particularly when integrating biological control agents in IPM program for DBM. MATERIALS AND METHODS Plants: Cabbage plants (Brassica oleracea L. var. capitata cv. K-K Cross) were planted using hydroponic method under glasshouse conditions at temperature 29 ± 4 C, 78 ± 5% relative humidity (RH) and a photoperiod of 12:12 (L:D) h in Malaysian Agricultural Research and Development Institute (MARDI), Serdang, Selangor. Cabbage seed were individually sown on pieces of wet sponge (2.5 cm 2.5 cm) as growing medium [35]. After two weeks, the seedlings were individually transferred to net pots and placed on non-circulating hydroponic containers [36]. The hydroponic solution was added accordingly throughout the plant growth. conducted in screen cages (1.5 m 2.4 m 1.5 m) under glasshouse conditions at 29 ± 4 C and 78 ± 5% RH. Three ages of cabbage plants were arranged in a completely randomized design (CRD) with 5 replicates. Before the experiment, the cabbage plants were infested with second instar DBM larvae for 24 h at three different host densities (10, 20 and 30 larvae). For each level of host density, 15 randomly selected naive females of C. vestalis were released into the experimental cage and parasitism was assessed within three different exposure durations (1 h, 3 h and 6 h). All females were only used once. The experiment was carried out between 0830 and 1500 hrs. All DBM larvae were collected and dissected under stereoscopic microscope (Olympus SZ40, Japan) to determine parasitism [39]. Statistical Analysis: Data were transformed using arcsine square root transformation to satisfy the assumption of equal variance and normal distribution for the analysis of variance (ANOVA) model [40]. The effect of plant age, 1840

3 host density and exposure on parasitism of DBM larvae There was a significant negative correlation between by C. vestalis was analysed by ANOVA using the percentage parasitism by C. vestalis and plant age of 2 General Linear Model (GLM) and followed by Tukey's test cabbage (F(1,25) = 40.14, r = 0.616, P < 0.000). Overall, when the analysis was significant (P < 0.05). Regression the DBM larvae fed on 4-week-old plants were more analysis was also performed on these transformed data to parasitized than the larvae on older plants (Table 2). determine the relationship of the significant treatments. In contrast, 12-week-old plants had the least incidence of One-way ANOVA was used to analyse percentage parasitism by C. vestalis. It seemed that the DBM-infested parasitism by C. vestalis on different ages of cabbage young plants were more attractive to the foraging among different host densities and exposure durations. C. vestalis and influenced its preference to parasitized Means were separated by Tukey s test at 5% level of more DBM larvae on these plants. The differential significance. Although all analyses were operated on parasitism of larvae by C. vestalis on different transformed data, actual means were presented in table. plant age in this study could have been caused by the All statistical analyses were run on Minitab Version 16 herbivore-induced volatiles released by DBM-infested [41]. cabbage plants of different ages. These plant volatiles can be utilised by parasitoids as chemical cues in their host RESULTS AND DISCUSSION searching [42-44]. Plant ontogeny has been shown to affect plant The effects of different ages of cabbage plants on the responses. Young plants are more inducible [21] and percentage parasitism of DBM larvae by C. vestalis effective in emitting volatile organic compounds (VOCs) infested with different levels of host densities and as they are metabolically more active than older plants exposure durations are shown in Table 1. The results [45]. Moreover, many secondary metabolites that are revealed that plant age and exposure durations had assumed to be involved in induced plant defence are significant (P < 0.05) influence on the mean parasitism of synthesized in specific tissues, which are active especially DBM larvae by C. vestalis. However, parasitism by this during early growth of plants [46,47]. Hence, the higher parasitoid was not significantly affected (P > 0.05) by its parasitism of DBM larvae on young cabbage in this host density. The results also showed no significant study might also be due to higher attractiveness of interaction effect (P > 0.05) in influencing the mean C. vestalis to these young plants that contain higher percentage parasitism of DBM larvae. content of glucosinolates and more active myrosinase Table 1: Results of ANOVA for parasitism of DBM larvae by C. vestalis as affected by plant age, host density within different exposure durations Source df Adj SS F-value P-value Plant age Host density Exposure Plant age Host density Plant age Exposure Host density Exposure Plant age Host density Exposure Error Table 2: Mean percentage of parasitism by C. vestalis on different plant ages of cabbage within three different exposure durations Mean ± SE % parasitism of larvae per plant Host density Exposure (hour) (larvae per plant) 4-week-old 8-week-old 12-week-old ± 3.7a 8.0 ± 3.7ab 2.0 ± 2.0b ± 2.6a 7.0 ± 2.6a 4.0 ± 1.9a ± 2.3a 4.0 ± 1.2b 2.7 ± 1.2b ± 3.7a 12.0 ± 3.7ab 6.0 ± 2.5b ± 4.2a 17.0 ± 2.6ab 7.0 ± 2.0b ± 2.2a 12.7 ± 1.9ab 6.7 ± 1.1b ± 5.5a 18.0 ± 3.7ab 8.0 ± 2.0b ± 3.3a 20.0 ± 3.5a 8.0 ± 1.2b ± 3.1a 20.7 ± 2.9a 8.7 ± 1.7b Means in each row followed by the same letter are not significantly different (P > 0.05) as determined by Tukey s test. 1841

4 activity [22,48]. This is because glucosinolates and their In another field experiment by Talekar [19], the parasitism associates have significant roles in producing of DBM larvae by Oomyzus sokolowksii Kurdjumov allelochemicals that can attract parasitoids of herbivores (Hymenoptera: Eulophidae) was also not affected by [49]. host-plant age. Here we suggest that these trends of The observed parasitism pattern showed by parasitism could be due to various complex combinations C. vestalis responding to DBM-infested cabbage of of abiotic factors that may influence the parasitoid different ages in this study was also probably due to behaviour under field conditions [53,54]. differential feeding damage caused by the larvae on This study showed that host density had no different plant age. Cotesia vestalis was previously significant influence (P > 0.05) on the mean percentage reported to give stronger response to plants with parasitism by C. vestalis. The occurrence of density extensive feeding damaged by DBM larvae [13]. independence parasitism by C. vestalis was also reported Feeding activity by larvae on younger plants is expected by Wang and Keller [28]. Although they noticed that the to cause more tissue damage than older plants. Although time spent by C. vestalis on infested plants increased with larvae on older plants might favour feeding on young increasing host densities and the females focused their leaves of these plants, these leaves may be ten times searching on the plants with the highest host densities, tougher and fibrous than the leaves from young plants the rate of parasitism was independent of host density. [50]. Hence, young plants may suffer more damage than Similar parasitism pattern was also observed in a study older plants. As a result, this could be the cause of by Liu and Jiang [11]. They found that the preference attraction of female parasitoids to the infested young of C. vestalis for parasitizing more DBM larvae on cabbages than the older ones, which later led to their B. campestris than on B. oleracea was independent of oviposition choice. host density. However, there were studies that showed The higher number of parasitized larvae on infested parasitism by C. vestalis responds in both density young cabbage plants could also be explained by the dependence [18,29-33,55,56] and inversely density differential physical structure of cabbage plants that dependence [19,20,31,34]. related to plant age. It is observed that younger cabbage Alam [29] reported that this specialist of DBM plant is generally smaller and has less number of leaves displayed a highly density-dependent mortality when than older plants. Cloyd and Sadof [51] found these responding to the increasing in diamondback moth are among the characteristics of plant structure populations. Several other field experiments by Velasco that gave the negative impact on Leptomastix dactylopii [33], Chelliah and Srinivasan [55], Cobblah et al. [30] and (Hymenoptera: Encyrtidae) attack on its host, Sow et al. [18] also revealed that the parasitism of DBM citrus mealybug (Homoptera: Pseudococcidae). Moreover, populations by C. vestalis acted in a density dependent plant physical characteristics were also reported to manner. Under laboratory conditions, Lim [31] found affect the searching efficiency of the female parasitoids, that the action of C. vestalis was density dependent. where simple plant structure may increase probability of Similarly, Soyelu [32] noticed the likely occurrence of encountering hosts compared to complex plant structure density-dependent parasitism by C. vestalis in a [52]. laboratory experiment regarding the dietary protein Contrary to our results, a field study by Talekar and on host-parasitoid population dynamics. Indeed, Yang [20] showed that the plant age had no significant the occurrence of inversely density dependence influence on parasitism of DBM larvae by C. vestalis, parasitism by C. vestalis was all detected under field although they observed the parasitism by this parasitoid conditions, where the parasitism decreased with was high soon after cabbage transplanting and later increasing DBM densities [19,20,31,34]. declined as the plant aged. Interestingly, Sow et al. [18] The lack of observed density dependent parasitism in showed significant relationship between the age of our study could probably due to long handling times by cabbage and the total parasitism by natural enemies of C. vestalis when exploiting high host densities [57,58], DBM, but found no relationship between the age of which caused decreasing in the parasitoid efficiency cabbage and parasitism of DBM larvae by C. vestalis. [59,60]. Moreover, this parasitoid may probably spend In the same study, they explained that a significant low much time on the heavy feeding damaged produced by numbers of immature stages of DBM larvae on mature high number of DBM larvae. This was also observed in cabbage plants was probably due to less attraction Cotesia rubecula Marshall (Hymenoptera: Braconidae) of old cabbages to the ovipositing female parasitoids. which attack the cabbage butterfly Pieris rapae (L.) 1842

5 (Lepidoptera: Pieridae), where the heavy feeding damage ACKNOWLEDGEMENTS by its host may reduce the C. rubecula searching efficiency because the wasp waste much time examining This study was funded by UKM grant No the feeding damage [61]. SF0896 and ST The authors thank Pest and This study revealed that the exposure durations of Disease Management Programme, Horticulture Research C. vestalis to DBM larvae feeding on cabbage plants had Centre, Malaysian Agricultural Research and significant effect (P < 0.05) on its parasitism. It showed Development Institute (MARDI), Serdang, Selangor, that the relationship between parasitism and exposure Malaysia for technical assistance and facilities. The first durations was statistically significant (F(1,25) = 10.50, author is supported by Ministry of Education Malaysia 2 r = 0.296, P = 0.003), where the parasitism by this doctoral scholarship. parasitoid increased with longer periods of exposure to its host larvae. In all exposure durations, the mean REFERENCES percentage parasitism on 4-week-old cabbage plants was the highest, followed by 8 and 12-week-old plants 1. Furlong, M.J., D.J. Wright and L.M. Dosdall, (Table 2). However, there were little variations in this Diamondback moth ecology and management: parasitism pattern with increasing host densities, where it problems, progress and prospects. Annual Review of was more noticeable on plants infested with 30 larvae. Entomology, 58: At this host density, the mean percentage parasitism was 2. Sivapragasam, A., W.H. Loke and M.N. Mohamad significantly greater on the 4-week-old than on older Roff, Brassica IPM adoption: progress and plants after 1 h of exposure. This pattern gradually constrains in South-east Asia. In the Proceedings of changed when the exposure duration of C. vestalis to the the Sixth International Workshop on the larvae was increased to 3 h and 6 h. It seemed that the Management of Diamondback Moth and Other preference for oviposition on 4-week-old plants was Crucifer Pests, pp: impermanent as the percentage parasitism on other older 3. Mahr, S.E., D.L. Mahr and J.A. Wyman, plants gradually increased over time. This result may Biological control of insect pest of cabbage and other depict the initial innate preference of this parasitoid crucifers. North Central Regional Publication, 471: 54. towards the infested young plant. Our result here was 4. Talekar, N.S., Biological control of diamondback somehow similar to those reported by Karimzadeh et al. moth in Taiwan-a review. Plant Protection Bulletin, [62]. They found that this parasitoid preferentially 38: chose to parasitize DBM larvae kept on susceptible 5. Idris, A.B. and E.J. Grafius, Field studies on the plant (young Chinese plant) rather than the larvae on effect of pesticides on the diamondback moth, partially resistant plant (intermediate or old common Plutella xylostella (L.) (Lepidoptera: Plutellidae) and cabbage) during the first 24 h of exposure. However, parasitism by Diadegma insulare (Cresson) this trend in parasitism changed and was not (Hymenoptera: Ichneumonidae). Journal of Economic detected when the exposure period was increased to Entomology, 86(4): h. In view of this, although C. vestalis initially 6. Sarfraz, M. and A.B. Keddie, Conserving the favours to parasitize DBM larvae feeding on young efficacy of insecticides against Plutella xylostella plants, this preference may not be permanent and seems (L.) (Lep., Plutellidae). Journal of Applied to fade over time. Entomology, 129: Tabashnik, B.E., N.L. Cushing, N. Finson and CONCLUSION M.W. Johnson, Field development of resistance to Bacillus thuringiensis in diamondback moth The parasitism of DBM larvae by its specialist (Lepidoptera: Plutellidae). Journal of Economic parasitoid, C. vestalis was influenced by plant age, Entomology, 83: where young infested cabbage plants were the most 8. Sarfraz, M., A.B. Keddie and L.M. Dosdall, preferred for parasitism. However, parasitism by Biological control of the diamondback moth, C. vestalis was not affected by DBM host density. Plutella xylostella: a review. Biocontrol Science and Thus, the use of biopesticides should be promoted when Technology, 15(8): integrating biological control agents such as parasitoid in 9. Cortesero, A.M., J.O. Stapel and W.J. Lewis, controlling the pest especially during young age of plants Understanding and manipulating plant attributes to as this may reduce the negative impact to the parasitoid enhance biological control. Biological Control, population. 17(1):

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