Impact Assessment of Apanteles plutellae on Diamond back Moth Using an Insecticide-check
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1 19 Impact Assessment of Apanteles plutellae on Diamond back Moth Using an Insecticide-check Guan-Soon Lim, A. Sivapragasam¹, and M. Ruwaida² Pest Science Unit, Central Research Laboratories Division, MARDI, Serdang, Selangor, Malaysia. Crop Protection Unit, Cocoa and Coconut Division, MARDI, Malaysia. ²MARDI Research Station, Tanah Rata, Cameron Highlands, Pahang, Malaysia. Abstract Field surveys of parasitoids of diamondback moth, Plutella xylostella (L), have indicated that Apanteles plutellae Kurdj may have a suppressing effect on the population of this insect. How important the parasitoid really is and to what extent it is beneficial is, however, not exactly known. This was, therefore, evaluated using an insecticide-check method whereby four treatments, each having different selective effects, were compared, viz: Dipel (Bacillus thuringiensis Berl, selectively toxic to diamondback moth but not the parasitoid); Sevithion (carbaryl + malathion, which is toxic to the parasitoid but not to DBM); cartap (highly toxic to both host and parasitoid); and an untreated control. Cartap and Dipel treatments had significantly higher yields than either the Sevithion treatment or the control. Sevithion treatment had less yield than the control. Both the control and Dipel treatment had significantly higher A. plutellae parasitism. The parasitism rate was least in the cartap treatment while Sevithion had a moderate level of parasitism. Based on these results and on the number of parasitoid cocoons collected from the crop, there was distinct evidence of differential survival and abundance of the parasitoid as well as the diamondback moth adults between different treatments. In caparison with cartap treatment, the diamondback moth adult ratios were 1.9, 8.0 and 47.9 for Dipel, control, and Sevithion respectively. Correspondingly, the parasitoid: host ratios were 3.22, 0.64 and These findings, in particular the high adult ratio (47.9) and the extremely low parasitoid:host ratio (0.05) for Sevithion, showed that A. plutellae is important and can contribute substantially to the suppression of diamondback moth. That this is so, and that resurgence was not due to hormoligosis or altered physiology of the host plant by Sevithion, was further confirmed in follow-up laboratory investigations. Introduction In the Cameron Highlands, control of the diamondback moth (DBM) Plutella xylostella (L) (Lepidoptera: Yponomeutidae) by conventional chemical insecticides has so far been the only practice. This unilateral approach and over-reliance on chemicals have resulted in development of insecticide resistance, pesticide poisoning of the farmers, the presence of insecticidal residues in marketable produce, and hazards to beneficial organisms (Henderson 1957, Balasubramaniam 1974, Sudderuddin and Kok 1978, Ooi 1979, Lim 1982). For the foreseeable future, insecticides will continue to remain a powerful and essential tool in DBM management. However, it is necessary that their use be minimized so as to prevent the present trend from reaching a disaster phase (Smith 1969). A prime strategy is to build a broader ecological base that would make
2 196 Lim, Sivapragasam, and Ruwaida possible the integration of various pest management techniques. Largely because biological control is a natural ecological phenomenon and can potentially provide a relatively harmonious, economical and permanent solution, the consideration of DBM s natural enemies has in recent years been given priority. In consequence, initial surveys in 1973 revealed the presence of a primary endo-larval parasitoid, Apanteles plutellae Kurdj (Hymenoptera: Braconidae) (Lim and Ko 1975). From extensive surveys, A. plutellae has been found to be widespread and fairly abundant (Lim 1982). There are indications that it may have a suppressing effect on the population of DBM. However, how important the parasitoid really is and to what extent it is beneficial is not exactly known. There is a need to evaluate this so that priorities may be assessed in attempts to exploit its beneficial role. This seems all the more important since other parasitoid species were observed to be rare (Ooi and Kelderman 1977, Ooi 1979). In this assessment, the importance and effect of the parasitoid were evaluated by the insecticide-check method. This compares host development and survival in both the presence and the absence of the parasitoid, the latter situation being effected through the selective use of chemical insecticides. Materials and Methods The insecticide check method adopted in the present studies compared three chemical treatments (Dipel, cartap, Sevithion) and an untreated control. Dipel, (Bacillus thuringiensis Berl was selectively toxic to DBM but not to the parasitoid (Lim 1982). In the case of Sevithion (carbaryl + malathion) the reverse situation was true, while cartap was highly toxic to both the host and parasitoid. Except for Dipel, which was applied at 2.5 g/4.5 I, both cartap and Sevithion were sprayed at 0.1% AI. A total of eight sprays were made beginning two weeks after transplanting and at weekly intervals thereafter. The field design was randomized complete block with three replications. For each treatment, the plot size was 14.3 m x 12.2 m consisting of 23 beds including two outer guard rows. The beds were spaced 0.6 m apart with each bed having 27 plants including two guard row plants at the end. A 0.5 m planting distance was used resulting in a total of 525 plants/plot. Cabbage (cv Constanta F1 Danish) was planted while fertilizer practices closely followed those of the farmers. Damage was assessed weekly on 10 random plants/replicate. For assessment of injury by the pest, the following damage index (Seaman et al 1963, Williams 1966) was employed: Damage index (%)= (No x 5) + (N1 x 20) + (N2 x 60) + (N3 x 100) where, of plants with score 0 (damage 5% and less), =number of plants with score 1 (5 to 20% damage), of plants with score 2 (20 to 60% damage), N3=number of plants with score 3 (60 to 100% damage), and No+ I +2+3 = total number of plants (Figure 1). Following such scoring under normal field conditions, a 10% damage index would correspond approximately to yield loss of 20%, which is unacceptable, while a 20% damage index may result in about 50% yield reduction. The populations of the larvae and pupae of DBM and cocoons of A. plutellae were also recorded weekly from 10 plants/replicate. For the assessment of host larval survival, 20 larvae/collection/replicate were randomly obtained over a total of nine samplings spread throughout the cropping period.
3 Assessment of A. plutellae for DBM Control 197 Figure 1. Damage scores of feeding injuries by DBM on cabbages. A = Score 0, damage 5% or less; B=Score 1, damage between 6 and 20%, C=Score 2, damage between 20 and 60%, D=Score 3, damage between 61 and 100% The larvae collected were maintained in breeding jars until adult host or parasitoid emergence. Survival of the parasitoid cocoons was also similarly examined. This examination was based on 15 cocoons/collection/replicate, and was repeated over nine samplings. A study was conducted into Sevithion-induced DBM resurgence, using one-month old potted cabbage plants. One group was sprayed with 0.1% AI Sevithion for four consecutive weeks while another, acting as a control was treated only with water. Following the treatment, each plant was enclosed in a net cage (51 cm x 51 cm x 51 cm). For the determination of oviposition rate, three newly emerged and mated DBM females were released into the cage 10 days after the last spray treatment. Every 24 hours for the next five days, the plant was replaced by another which was similarly treated. All eggs deposited on each plant were counted. Throughout the study, a water and 30% honey mixture was provided as food to the adult insects. The experiment was replicated five times. In the determination of developmental period, 20 freshly-laid (deposited within the first 24 h) eggs from each replicate were isolated. These were transferred to breeding jars, and on hatching were individually reared to the adult stage. The length of each developmental stage was recorded, while the sex of the emerging adults determined. Studies on fecundity and longevity of the first generation adults were made by isolating 10 freshly emerged females from each replicate of the treatment group, as well as from control. These were provided daily with a 30% honey-water solution fed through a wick as well as fresh Brassica rapa leaves of similar size for oviposition. All eggs deposited daily were recorded until the females died.
4 198 Lim, Sivapragasam, and Ruwaida As distinct from the above study, which attempted to explore possible effects of Sevithion indirectly through treatment of the host plants, a parallel and separate experiment was also conducted to determine the effect via direct treatment of the insect. The overall procedure was in general similar to that of the previous study, except that instead of the plants 2nd-instar larvae of DBM were exposed to the insecticide. Only those surviving the treatment and completing the life cycle were considered. For the control, larvae were sprayed with water only. Field assessment Results Results of the field trial of the insecticide-check method (Table 1) showed that the cartap and Dipel treatments gave significantly higher yields than either Sevithion treatment or the untreated control. Between cartap and Dipel, although the former gave a slightly higher yield, the difference was not significant. In the Sevithion treatment the yield was significantly less than in the control, suggesting that insecticidal applications need not necessarily increase crop yields. Our study showed that in some cases insecticidal applications not only involved additional cost, but failed to provide protection of the crop from DBM. Table 1. DBM damage and cabbage yield as affected by various insecticidal treatments in the Cameron Highlands Treatment Head formation Mean damage index (%) to heads Mean weight Yield/plot Mean No % Marketable Nonmarketable' Total (kg) (kg)ª Dipel a Cartap a Sevithion c Control b LSD (0.05) ns 48.2 ªMeans in vertical column followed by the same letter are not significantly different at 5% level by Duncan's multiple range test The yield differences for the various treatments were apparently related largely to successful head formation as well as individual head weight. For the latter, although no significant difference existed among the different treatments the ranking in magnitude of the mean head weight closely paralleled that of the overall crop yields, thus the cartap treatment had the highest, followed by Dipel, the control, and Sevithion (Table 1). In terms of head formation, the Dipel treatment had the highest number of heads formed per unit area. Although the head weight was less than that for cartap the higher number of head formed apparently compensated to some extent in raising the overall yield in the Dipel treatment (Table 1). In the Sevithion treatment and the control, significantly fewer heads were formed, thus depressing further the overall yields. Assessment of damage by DBM clearly showed that the damage inflicted was higher on non-marketable heads, suggesting that reduced crop yields are both closely associated with and dependent on the extent of DBM infestations. Within both categories of marketable and non-marketable heads, much lower damage occurred in the cartap and Dipel treatments. This trend was observed in assessments throughout the cropping period (Figure 2) as well as at harvest (Table 1). Also, in both cartap and Dipel treatments, the number of plants showing high damage scores was distinctly lower.
5 Assessment of A. plutellae for DBM Control Days after transplanting Figure 2. I Development of DBM, its parasitoid (Apanteles plutellae Kurdj), and crop damage as influenced by insecticidal treatments, D = Dipel, P = cartap, S = Sevithion, and C = untreated control Cartap and Dipel treatments had much lower levels of DBM infestation while Sevithion and the control exhibited extremely high damage (Table 2). Of the larvae that escaped A. plutellae parasitism, the numbers entering the pupal stage were highest in the control, followed by Sevithion, cartap and Dipel treatments. This trend was also noted for the rate of adult emergence from the surviving pupae. From these results and the relative abundance of the larvae in the field (Table 2), it is evident that a much higher number of larvae reached the adult stage in the Sevithion treatment and the control than in the cartap or Dipel treatments. These were respectively 47.9 and 8.0 times that of cartap. With Dipel, the number was nearly double that of cartap, although very much less than that of the Sevithion and the control. In general, pupal population in the field showed a similar trend to that of the larvae. This was clearly evident from the population development observed in the periodic samplings as well as from the overall total (Figure 2). Both the control and Dipel treatments had significantly higher levels of parasitoid attack. The parasitism rate was least in the cartap treatment, while the Sevithion treatment resulted in a moderate level of parasitism (Table 3). Higher numbers of parasitoid cocoons could be collected from the untreated control and the cabbage sprayed with Dipel; the number from the Dipel treatment was approximately six times higher than that from the cartap treatment (Figure 3). Such differential survival and abundance of the parasitoid among the different treatments not only strongly indicates the adverse effects of both cartap and Sevithion, but also the selectivity of Dipel for the parasitoid. These differential effects were also clearly reflected in the rate of parasitoid emergence from field-collected cocoons, for which rates of 69.4%, 67.2%, 55.6% and 45.6% were recorded for the control, Dipel, Sevithion, and cartap treatments, respectively. This order of parasitoid emergence was also observed for cocoons which developed from fieldcollected host larvae (Table 3). From these figures, and from the relative abundance of parasitoid cocoons in the field, it was concluded that a very much higher number of adult parasitoids occurred and survived in the fields sprayed with Dipel and in the
6 200 Lim, Sivapragasam, and Ruwaida
7 Assessment of A. plutellae for DBM Control Insecticide treatment Figure 3. Total DBM and Apanteles plutellae count and crop damage as influenced by insecticidal treatments, D = Dipel, P = cartap, S = Sevithion, C = untreated control untreated control. These numbers were respectively 7.8 and 6.7 times higher than those recorded for cartap-treated fields (Table 3). The figure for the Sevithion treatment was only about 3.2 times high. Sevithion effects on development and reproduction in DBM Indirect exposure through the host plant Sevithion had no significant effect on DBM oviposition. Nevertheless, the number of eggs laid by the moths reared on treated plants was higher in several cases when compared to the control. Several other parameters were unaffected; these included the developmental period, the sex ratio, as well as the longevity and fecundity of the first generation females. The mean fecundities of the control and Sevithion-exposed females were 304 ± 17.6 eggs and 254 ± 21.3 eggs respectively, and their mean longevities 13.8 ± 1.0 days and 14.0 ± 1.4 days. Both differences were statistically non-significant. Direct exposure to sub-lethal dose There were no statistical differences between fecundity of the Sevithion-exposed and unexposed DBM females in both first and second generations. For the first generation the mean fecundities were 96.8 ± 11.6 eggs and 97.7 ± 17.3 eggs/female for treated and control respectively, while for the second generation the number of eggs was 48.0± 17.3 and 54.7 ± 7.8/female respectively. Although the mean fecundity was much lower in the first generation, comparisons made for first and second generations in treated adults showed no statistically significant difference. For the controls the difference was, however, significant. Studies on mean longevity also revealed little difference between the treated females and those in the control. For first generation females, mean longevity was 21.0± 1.2 days for the treated and 14.1 ± 1.3 days for the control. For second generation, longevity was 14.3± 1.1 days in the treated and 15.0± 1.2 days in the control. Similarly, there was little difference in the mean longevity of males in both first and second generation. 0 Discussion Previous field observation as well as experimental studies have pointed to A. plutellae as one of the more important parasitoids of DBM. In general, a somewhat
8 202 Lim, Sivapragasam, and Ruwaida similar conclusion was also obtained and confirmed by findings from the present chemical exclusion studies, wherein a much poorer crop yield resulted from higher infestations of DBM due to the selective destruction of A. plutellae by Sevithion. Because of Sevithion s selective toxicity to the parasitoid, a shift to an extremely small parasitoidhost ratio (0.05) resulted, leading to a rapid upsurge of DBM (Table 3). On the other hand, the ratio greatly increased to 3.22 in favor of the parasitoid when Dipel was applied. In the case of the cartap treatment there was hardly any significant change in the parasitoid:host ratio of 0.77 from that of untreated control (0.64). These findings clearly revealed that in a host-parasitoid system, the ratio of their respective numbers may be altered in various ways by the use of different insecticides, and depending on direction and degree these changes can either be favorable to the parasitoid or pose a greater hazard to it. Such findings evidently suggest that the correct choice of chemical to be used could be crucial for any effective pest management of DBM, and that the choice should be made very carefully. In the field trial, the accelerated increase in DBM population in the Sevithion treatment may well also be due to an altered plant physiology. This could result from improved nutrition as in the case of phytophagous mites (Chaboussou 1965). Alternatively, it may be due to hormoligosis (Locher 1958, Luckey 1968, Dittrich et al 1974), wherein Luckey (1968) conceptualized that subharmful quantities of any stressing agent will be stimulatory to an organism by providing it (with) increased sensitivity to respond to changes in its environment and increased efficiency to develop new or better systems to fit a suboptimum environment. In the present studies, no significant differences were observed for all the parameters considered (developmental period, fecundity, adult longevity and sex ratio), showing conclusively that neither hormoligosis nor an improved nutritional basis via an altered physiology of the host plant were responsible for the observed effects. With these factors ruled out, it thus follows that the resurgence of DBM following Sevithion treatment could only logically be attributed to the selective removal of A. plutellae. The vast increase in DBM population following the Sevithion treatment furnishes proof of the parasitoid s controlling power and potential. However, the control-exerted remained only partial. This is suggested by the fairly high infestations in the untreated control, where the parasitoid s activity was undisturbed, as well as by the results of the Dipel and cartap treatments where these chemicals assisted as supplementary measures to provide effective control. From investigations into the adverse effects of Sevithion on A. plutellae, it was noted that these effects, although substantial, could not exterminate completely the parasitoid population. Thus the total extent of host increase was not fully expressed in the chemical exclusion studies because the parasitoid was not completely eliminated, and so may have continued to produce some effect in limiting DBM. In this instance A. plutellae was probably responsible for the observed lower host level. What population level the host might achieve in the complete absence of the parasitoid remains unknown. The effectiveness of A. plutellae was clearly discernible even though the insecticidalcheck treatment was carried through only one crop season. Although quite evident, the resurgence effect was not as spectacular as in other parallel studies, such as in the biological control exerted by the parasitoid Aphytis rnaculicornis (Masi) on the infestation of olive scale insect (Parlatoria oleae Colvee). In that case, the infestation occurring under conditions of undisturbed parasitoid activity, when compared with the exploded infestations characteristic of DDT-caused suppression of natural enemy activity, had ratios of initial to final densities of 100-fold and 1000-fold (DeBach and Huffaker 1971). Similar studies involved the purple scale insect Lepidosaphes beckii (Newm) which is parasitized by Aphytis lepidosaphes Compere. Here the selective check-insecticide, endrin, gave an increase in host population over a three-year period from an initial density of 174 to one of 20,615 (DeBach and Huffaker 1971). Such an impressive difference
9 Assessment of A. plutellae for DBM Control 203 is probably also obtainable with Sevithion should the period of exposure be greatly extended. That this may be so is strongly suggested by the experience of DeBach and Huffaker (1971) who noted that the biological control potential from established enemies cannot be accurately evaluated in study plots which have not gone without major chemical pesticide treatments for significant periods. It is recognized that the insecticide-check method employed in the present study may have shortcomings. Nevertheless, the findings clearly demonstrate that the parasitoid can contribute significantly to the control of DBM. This is now firmly established, and should convince critics and sceptics who still have doubts about the beneficial role of the parasitoid. Although A. plutellae has a definite role in the management of DBM, it is important to recognize that its full impact is often affected by several factors, both physical and biological. Among the latter are the parasitoid s behavior (foraging, migration tendency for example), its hyperparasitoids (Lim 1982), the diseases of the host, and the presence of other competitive parasitoids. All these factors merit serious and full consideration in determining the contributory potential of A. plutellae, and for its successful exploitation in the control of DBM. Acknowledgement The senior author would like to acknowledge the kind encouragement and invaluable advice provided by his adviser, Professor M. J. Way during the course of these studies which were carried out as part of a Ph. D. thesis submitted by him to the University of London, U.K. in Literature Cited Balasubramaniam, A Pesticide pollution. Bull. Public Health Soc. 8: Chaboussou, F The multiplication of tetranychids by trophic means as a result of pesticide treatments. Relationship with the phenomenon of acquired resistance. (In Italian with English summary). Boll. Zool. Agric. Bachicolt. SIIv. 7: DeBach, P. and C. B. Huffaker Experimental techniques for evaluation of the effectiveness of natural enemies. pp In C. B. Huffaker (ed) Biological Control. Plenum Press, New York and London. Dittrich, V., P. Streibert, and P. A. Bathe An old case reopened: mite stimulation by insecticide residues. Envin. Entomol. 3: Henderson, M Insecticidal control of the diamondback moth (Plutella maculipennis Curt.) on cabbage at Cameron Highlands. Malay. Agric. J. 40: Lim, G. S The biology and effects of parasites on the diamondback moth, Plutella xylostella (L.). Ph.D. thesis, University of London, London, U.K. 317 pp. Lim, G. S. and W. W. Ko Apanteles plutellae Kurdj, a newly recorded parasite of Plutella xylostella (L) in Malaysia. MARDI Res. Bull. 3: Locher, F. J Der Einfluss von Dichlordiphenyl-trichlormethylmethan (DDT) auf einige Tetranychiden (Acari, Tetranychidae). (In German with English summary). Z. Angew. Zool. 45: Luckey, T. D Insecticide hormoligosis. J. Econ. Entomol. 61:7-12. Ooi, P. A. C An ecological study of the diamondback moth in Cameron Highlands and its possible biological control with introduced parasites. M. Sc. thesis, University of Malaya, Kuala Lumpur, Malaysia. 151 pp. Ooi, P. A. C. and W. Kelderman A parasite of the diamondback moth in Cameron Highlands, Malaysia, Malay. Agric. J. 51: Seaman, W. L., J. C. Walker, and R. H. Larson A new race of Plasmodiophora brassicae affecting Badger Shipper cabbage. Phytopathol. 53:
10 204 Lim, Sivapragasam, and Ruwaida Smith, R. F The new and the old in pest control. Proc. Acad. Nazion. dei Lincei, Rome 366: Sudderuddin, K. I. and P. F. Kok Insecticide resistance in Plutella xylostella collected from the Cameron Highlands of Malaysia. FAO Plant Prot. Bull. 26: van den Bosch, R. and P. S. Messenger Biological Control. Intext Press, Inc., New York. 180 pp. Williams, P. H A system for the determination of races of Plasmodiophora brussicae that infect cabbage and rutabaga. Phytopathol. 56:
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