Interspecific competition between Diadegma semiclausum and Oomyzus sokolowskii, parasitoids of diamondback moth, Plutella xylostella
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1 Interspecific competition between Diadegma semiclausum and Oomyzus sokolowskii, parasitoids of diamondback moth, Plutella xylostella Zu-hua Shi, Qin-bao Li, Xin Li and Shu-sheng Liu Institute of Applied Entomology, Zhejiang University, Hangzhou 3129, China Corresponding author: Abstract Interspecific competition between Diadegma semiclausum (Hellén) (Hymenoptera: Ichneumonidae) and Oomyzus sokolowskii (Kurdjumov) (Hymenoptera: Eulophidae) was investigated at 25 C in the laboratory, by exposing III instar larvae of diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae) to either species alone or exposing the host larvae already exposed to one species to the other. Both D. semiclausum and could lay eggs into the host larvae that had previously been parasitised by the other species, leading to occurrence of multiparasitised hosts. When host larvae were exposed first to D. semiclausum and then to, and the time intervals between the two exposures were shorter than one day, ensuing parasitoid adults from the multiparasitised host larvae were nearly always. When host larvae that were first exposed to and then exposed to either immediately or 3-4 days later, immature stages of both parasitoids were found inside the host larvae by dissection. However, at 6-7 days after parasitism by, only one larva of remained in each host, suggesting that physically removed the immatures through feeding. When host larvae were first exposed to and then exposed to D. semiclausum, the percentage of adult emergence increased as the time intervals between the two exposures increased. When host larvae exposed to three days previously were exposed to, no could survive to adulthood. Introduction Interspecific competition is one of the most predominant interspecific interactions and can influence the size and structure as well as the stability of communities (Mackauer 199). Interspecific competition between parasitoids can be of great importance in the application of biological control (van Alebeek et al. 1993) because it could reduce the potential of parasitoids against target pests (Leveque et al. 1993) and sometimes lead to failure of an introduction of a natural enemy (Pijls et al. 1995). Diamondback moth (DBM), Plutella xylostella (L.) (Lepidoptera: Plutellidae), is a major pest of crucifer crops worldwide and has developed high resistance to almost all types of insecticides (Talekar & Shelton 1993, Noda et al. 2). Oomyzus sokolowskii (Kurdjumov) (Hymenoptera: Eulophidae) and Diadegma semiclausum (Hellén) (Hymenoptera: Ichneumonidae) are two major parasitoids of DBM (Ooi 1988, Wang et al. 1999). They have been introduced into many countries or regions to enhance biological control of DBM (Ooi 1988, Yang et al. 1993, Talekar & Hu 1996, Noda et al. 2). Because both parasitoids oviposit into DBM larvae, they may compete for hosts. But, as yet, no information is available on their competition. In this study, we observed the oviposition of these species into host larvae already parasitised by the other and determined the development of the two parasitoids in multiparasitised hosts. Materials and methods Insects and plants All insect stock cultures were maintained in temperature-controlled rooms at 25±2 C, 6-8% RH with a photoperiod of 14:1 (L:D). DBM was originally collected from a cabbage field in a suburb of Hangzhou, China in June The stock culture of DBM was reared on potted plants of cabbage, Brassica oleracea var capitata, using the method described by Wang et al. (1999). The stock culture of was established from parasitised DBM pupae collected from a cabbage field in a suburb of Hangzhou in July 2. The culture was maintained using DBM as hosts reared on cabbage plants and had been reared for 5-6 generations prior to the experiments. The stock culture of was started from 1 cocoons of the parasitoid from a stock culture at the Institute of Plant Protection, the Academy of Agricultural Sciences of Yunnan Province, China. The Proceedings of the 4th International Workshop, Nov. 21, Melbourne, Australia 243
2 institute at Yunnan introduced from Taiwan in The culture was maintained using DBM as hosts reared on cabbage plants and had been reared for 4-7 generations prior to experiments. All parasitoids of both species used in experiments were randomly chosen, mated adult females, at 1-2 days post-emergence. They were provided with 1% honey solution as food. Host larvae used in experiments were in early III instar. To obtain larvae parasitised by, we exposed DBM larvae individually to a female parasitoid in a test tube, and observed each of them to be attacked once. With this method, 2-3 attacked larvae could be obtained in half an hour. However, it was not possible to obtain the parasitised larvae by with this method because this parasitoid attacked only a few DBM larvae per female per day (Wang et al. 1999). Therefore, we obtained parasitised larvae by exposing 3 host larvae to 2 wasps for 24 h. Oomyzus sokolowskii parasitism of larvae already parasitised by Diadegma semiclausum Thirty larvae attacked by in early III instar and 3 healthy host larvae of the corresponding age were exposed either h (immediately after), 48 h, 72 h or 96 h later to 1 female wasps of O. sokolowskii for 24 h. At the end of exposure, 1-15 larvae in each of the replicates were dissected and the numbers of host larvae containing eggs or larvae of the two parasitoid species were recorded. The remaining15-2 larvae were reared until emergence of parasitoids. The numbers of hosts that produced parasitoid adults of either species were recorded. All dead DBM larvae and the pupae that did not produce either moth or parasitoid were dissected to determine whether they had been parasitised by either of the two species. In a separate test, 3 host larvae attacked by were exposed either h, 72 h or 96 h later to 1 female adults for 24 h. After the exposure, the host larvae were sampled and dissected at 24 h intervals, and the numbers of host larvae containing eggs or larvae of the two parasitoid species were recorded. Diadegma semiclausum parasitism of host larvae already parasitised by Oomyzus sokolowskii The experiment design was similar to that described above, but DBM larvae were exposed first to 2 female wasps of Oomyzus sokolowskii for 24 h, then to two females for 6 h either h, 24 h, 48 h or 72 h later, and series sample dissections at 24 h intervals were made. Results Oomyzus sokolowskii parasitism of larvae already parasitised by Diadegma semiclausum Oomyzus sokolowskii oviposited in the host larvae that had previously been parasitised by, leading to the occurrence of multiparasitised hosts. Oviposition was not deterred by the presence of eggs or larvae of in the host larvae (Table 1). Those multiparasitised host larvae had lower survival, and almost all of them failed to produce wasps of except when oviposition of occurred 48 h after parasitism by (Table 2). As the parasitised host larvae continued to develop, the percentage of host larvae with decreased while that with remained unchanged. In all three treatments, no individuals were found in the multiparasitised larvae on the 6-7 th day after parasitism by (Figure 1 and Figure 2). Diadegma semiclausum parasitism of larvae already parasitised by Oomyzus sokolowskii Although attacks by on DBM larvae were hasty, almost all attacks (ca. 95%) resulted in parasitism (Table 1). No significant differences were found in percentage of parasitism by between the host larvae previously exposed to and the healthy ones. However, in both treatments and controls, percentage of parasitism by decreased with the increase of larval age (Table 3). When oviposition by occurred after that by, the percentage of hosts that produced wasps of decreased with increase of the intervals between the two oviposition events. When the interval reached 72 h, no adults of were produced (Table 2). 244 Proceedings of the 4th International Workshop, Nov. 21, Melbourne, Australia
3 When host larvae were exposed immediately to after the exposure to, the percentage of hosts with remained high, while that with decreased as the parasitised host larvae developed (Figure 3). However, when the hosts were attacked by after had developed for 48 h or 72 h, the percentage of hosts with remained virtually unchanged as that with (Figure 4). with parasitoid eggs or larvae Days after oviposition by Figure 1. Percentage of Plutella xylostella host larvae with parasitoid eggs or larvae when the host larvae were first attacked by Diadegma semiclausum and then immediately exposed to Oomyzus sokolowskii. with parasitoid eggs or larvae Days after Oviposition by Figure 2. Percentage of Plutella xylostella host larvae with parasitoid eggs or larvae when the host larvae were first attacked by Diadegma semiclausum and then exposed to Oomyzus sokolowskii 72 h later. Table 1. Percentage parasitism by Oomyzus sokolowskii of Plutella xylostella larvae that were already parasitised by Diadegma semiclausum -96 h previously % parasitism of hosts Time in h a exposed to both parasitoids by only % parasitism of host exposed to 95. ±2.4 (1) b 71. ± ±7.3 (5) ±3.7 (5) 52. ± ±5.6 (5) ±1.8 (5) 53. ± ±4.9 (5) ±1.5 (5) 52.3 ± ±5.7 (5) a Time in hours between exposure to Diadegma semiclausum and exposure to Oomyzus sokolowskii. b Mean ±standard error; data in parentheses are the number of replicates. Proceedings of the 4th International Workshop, Nov. 21, Melbourne, Australia 245
4 Table 2. Successful parasitism of Plutella xylostella and adult emergence of Diadegma semiclausum and Oomyzus sokolowskii in relation to oviposition sequence and interval Host exposure sequence to parasitoids a % of host survival to prepupa Number (%) hosts that produced adults of D--O (96.3) 2 ( 3.7) D-48-O (6.) 2 (4.) D-72-O (85.7) 1 (14.3) D-96-O (96.8) 1 ( 3.2) O--D (96.3) 3 ( 3.7) O-24-D (75.) 6 (25.) O-48-D (13.3) 13 (86.7) O-72-D 35.2 (.) 1 (1) a D=Diadegma semiclausum, O=Oomyzus sokolowskii,, 24, 48, 72, 96 are hours between exposures to two parasitoids, thus D--O and D-48-O stand for host exposures to or 48 h after exposure to respectively. Table 3. Percentage parasitism by Diadegma semiclausum of Plutella xylostella larvae that were already exposed to Oomyzus sokolowskii -72 h previously % parasitism of hosts Time in h a exposed to both parasitoids by only % parasitism of host exposed to 84. ±7.8 (5) b 97.3 ± ±3.3 (5) b ±2.2 (5) 68.9 ± ±5.4 (5) ±3. (5) 57.8 ± ±8.5 (5) ±5.6 (5) 51.7 ± ±8.1 (5) a Time in hours between exposure to Oomyzus sokolowskii and exposure to Diadegma semiclausum. b Mean ±standard error; data in parentheses are the number of replicates with parasitoid eggs or larvae Days after exposure to Figure 3. Percentage of Plutella xylostella hosts with parasitoid eggs or larvae when the host larvae were first exposed to Oomyzus sokolowskii and then exposed to Diadegma semiclausum immediately. 246 Proceedings of the 4th International Workshop, Nov. 21, Melbourne, Australia
5 with parasitoid eggs or larvae Days after oviposition by Figure 4. Percentages of Plutella xylostella hosts with parasitoid eggs or larvae when the host larvae were first exposed to Oomyzus sokolowskii and then exposed to Diadegma semiclausum 48 h later. Discussion Many parasitoids can discriminate between hosts parasitised by conspecific females and those from nonparasitised hosts, but interspecific host discrimination has been rarely reported, particularly for larval parasitoids. As larval parasitoids usually incur strong physical defence from hosts that they attack (Brodeur et al. 1996), host larvae may be too active to be held by parasitoids for sufficient duration to judge whether they had been parasitised. The results obtained in this study demonstrated that both parasitoid species could parasitise host larvae previously parasitised by the other species, no matter whether the first parasitoid was in the egg or the larval stage. Both parasitoid species showed little discrimination and seemed to take the strategy to deposit all their eggs into hosts as soon as possible, to increase their fitness. Yang et al. (1994) reported that only one parasitoid could survive to adult in one superparasitised larva. Eggs of began to hatch 1-2 days after oviposition at 25 C (Yang et al. 1993). Dissections showed that newly hatched larvae were swimming in the host haemocoele, suggesting that the early larval stage lived on the materials in the haemolymph. In all treatments where ovipositions by were followed by, and where ovipositions by were immediately followed by, the proportion of hosts with O. sokolowskii reduced sharply after had developed for 4-5 days. It could be inferred that D. semiclausum killed and swallowed the immatures during its late larval stages. On the contrary, when ovipositions by were followed by with 2 or 3 days delay, the proportions of hosts with did not change as the host developed. After the host had pupated, they remained suitable for the pupation of, but became unfavourable to larval development and survival of. Therefore, hosts from such treatments produced more than. Endoparasitoids require sufficient nutrients from their hosts to develop to maturity. One DBM larvae usually support the complete development of 8-1 (Ooi 1988, Wang et al. 1999), or one D. semiclausum (Yang et al. 1994). Over use of host material by both parasitoids may be responsible to the low survival rates of multiparasitised host larvae. Although multiparasitism by the two species reduces their fitness, it may not necessarily reduce their effectiveness against DBM because their differential requirements for temperature (Yang et al. 1993, Wang et al. 1999) and possibly other environmental factors may result in niche separation between the two species. However, as has a wide range of hosts and is a facultative hyperparasitoid as well as a primary parasitoid, caution must be taken when introduction of this parasitoid into new areas is considered. Acknowledgements This study was supported jointly by the National Natural Science Foundation of China (Project no ) and the Australian Centre for International Agricultural Research (Project no. ACIAR CS2/1998/89). Proceedings of the 4th International Workshop, Nov. 21, Melbourne, Australia 247
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