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Reznik, 2012, published in Entomologicheskoe Obozrenie, 2012, Vol. 91, No. 4, pp. 681–690. 405. Effects of Cold Shock on Host Egg Parasitization by Females.
ISSN 0013-8738, Entomological Review, 2013, Vol. 93, No. 4, pp. 405–411. © Pleiades Publishing, Inc., 2013. Original Russian Text © N.D. Voinovich, N.P. Vaghina, S.Ya. Reznik, 2012, published in Entomologicheskoe Obozrenie, 2012, Vol. 91, No. 4, pp. 681–690.

Effects of Cold Shock on Host Egg Parasitization by Females of Trichogramma buesi Voegele (Hymenoptera, Trichogrammatidae) N. D. Voinovich, N. P. Vaghina, and S. Ya. Reznik Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia Received May 13, 2012

Abstract—The effects of cold shock (4°C for 18–24 h) on survival of Trichogramma buesi females, their fecundity, and the inclination to parasitize grain moth eggs were studied under laboratory conditions. Cold shock did not result in any significant change in the survival rate, whereas the fraction of females that parasitized grain moth eggs and the fecundity of these females slightly decreased. However, females which had already started oviposition before cold shock infested grain moth eggs much more frequently. In most insect species studied, cold shock results in a sharp decrease or even disruption of the effect of experience on the subsequent behavior. Thus, the results of this study suggest that “the effect of acquired experience” (a tendency to continue infestation of the particular host species) in Trichogramma females is based not on learning or not only on learning but on some other, possibly hormonal mechanisms. DOI: 10.1134/S0013873813040015

The activity of insects, as well as of other ectothermic organisms, depends considerably on the ambient temperature. The lower optimum limit for most insect species is about 15°C; their activity decreases abruptly at lower temperatures, whereas a prolonged exposure to near-zero or below-zero temperatures is usually lethal for insects unless they have been prepared for wintering (Chernyshev, 1996). Our previous research (Reznik et al., 1998, 2001a, 2001b, 2011) has shown that when females of some species of Trichogramma Westw. (Hymenoptera, Trichogrammatidae) are offered eggs of the grain moth Sitotroga cerealella Oliv. (Lepidoptera, Gelechiidae), the onset of parasitization may be delayed by up to 10 days. The rate of induction of parasitization (the value inversely proportional to the duration of the delay) increases linearly with the temperature within the thermal optimum zone. Moreover, the females which have infested grain moth eggs at a high temperature tend to continue infestation even at relatively low temperatures (Reznik and Vaghina, 2006a; Reznik et al., 2009, 2010, 2011). Special experiments have also shown that heat shock (a short-term action of sublethal high temperatures) reduces the fraction of females that can start parasitization, whereas the females which have already started infesting the host usually continue to do so after heat shock (Reznik and Vaghina, 2006b). This stable trend towards continued

parasitization may be based on a number of mechanisms, including learning (Reznik, 1993; Turlings et al., 1993; Bjorksten and Hoffmann, 1998; Reznik et al., 2003). The study of factors reducing the stability of a particular response is one of the ways to determine the mechanisms underlying it. For example, experiments with different species of insects have shown that cold shock usually negatively affects long-term memory (Perisse et al., 2007; Emden et al., 2008; Lizé et al., 2010). The study of the effects of cold shock (a short-term action of a sublethal low temperature) on induction and continuation of infestation of eggs of a particular host species is also important from the viewpoint of biological control. Trichogramma wasps are widely used for control of various lepidopteran agricultural and forest pests, the thermolability of their activity representing a considerable obstacle to their efficient use in the temperate climate (Pak and Heiningen, 1985; Smith, 1996; Sorokina, 2001, 2008; Heimpel and Casas, 2008; Pizzol et al., 2010). On the other hand, the non-diapausing stages of Trichogramma wasps: the larvae, pupae, and even adults, can be stored for relatively short periods at low positive temperatures (Shlyakhtich et al., 1989; Jalali, 1992; Boivin, 1994; Kumar et al., 2005; Yilmaz et al., 2007; Özder, 2008; Colinet and Boivin, 2011).

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This communication is devoted to the effect of cold shock on the survival rates of females of Trichogramma buesi Voegele, their fecundity, and tendency to parasitize grain moth eggs. MATERIALS AND METHODS Experiments were performed using a laboratory culture of T. buesi which had been maintained for many generations on grain moth eggs under constant conditions, at the photoperiod L : D = 18 : 6 and the temperature 20°C. At the beginning of each experiment, the freshly emerged adults of T. buesi were allowed to mate for 2–4 h, after which the females were placed in separate small tubes (8 × 45 mm). They were fed on 50% solution of honey which was applied as a narrow strip on the tube wall. According to the experiment design (see below), some females were offered 50–60 grain moth eggs glued onto numbered cardboard sheets. At the beginning of the first experiment, all the females were kept at a temperature of 25°C that facilitated the onset of parasitization (Reznik and Vaghina, 2006a; Reznik et al., 2009, 2010, 2011), for 4 h after placement in tubes. Grain moth eggs were offered to half of the females (Table 1, variants I–IV). After this first (high-temperature) exposure, cardboard sheets with host eggs were replaced with empty numbered sheets. Then, all the females (those which had been offered host eggs and those which had simply spent 4 h at a high temperature) were randomly divided into two groups: the first group (experimental variants: I, II, and V) was subjected to cold shock (24 h in the dark at 4 ± 1°C), whereas the second group (control variants: III, IV, and VI) spent 24 h in the dark at 20°C. The experimental females were divided into variants I and II post factum, depending on whether or not they infested the host eggs during the first (hightemperature) exposure; the control females were divided into variants III and IV in the same way. At the end of the first experiment, immediately after cold shock (experiment) or after an equal period in the dark at 20°C (control), all the females were offered grain moth eggs for 48 h at 15°C (the second, lowtemperature exposure). The first experiment was carried out in 8 replicates, each using 100 experimental and 100 control females from one generation of the laboratory strain. The second experiment followed the same general design; however, the experimental females were trans-

ferred into the cold shock conditions (and the control ones, into the dark) not after 4-hour high-temperature exposure but according to the following scheme. All the females which were offered host eggs for infestation (Table 2, variants I–IV) were constantly monitored; when a female started infesting the first host, it was immediately transferred into the cold conditions or into the dark (variants I and III). Simultaneously, one of the females kept without hosts was transferred into the same regime (variants V and VI). When the number of females in the high-temperature regime decreased to about one-half of the initial value (which usually happened within 4–6 h), all the remaining females were simultaneously transferred into the corresponding regimes (variants II and IV). Twenty-four hours after the first female was transferred into the cold shock conditions, all the females were offered grain moth eggs for 48 h at 15°C (the second exposure). The second experiment was carried out in 10 replicates, also using different generations of the laboratory strain (100 experimental and 100 control females for each replicate). Thus, in the first experiment, the duration of exposure at 25°C and at 4°C was the same for all the experimental females (4 h and 24 h, respectively), whereas the time interval between the onset of infestation and the beginning of cold shock varied from several minutes to 4 h. On the contrary, in the second experiment the time interval between the onset of infestation and the beginning of cold shock was relatively constant, not exceeding several minutes, whereas the time of exposure at a high temperature varied from several minutes to 6 h, and the cold shock duration varied from 18 to 24 h. In both experiments, after the first and second exposure the sheets with grain moth eggs were removed from the tubes and transferred into the optimum conditions for preimaginal development of T. buesi (photoperiod L : D = 18 : 6, temperature 25°C). On completion of larval development, the number of darkened (parasitized) grain moth eggs was determined on each sheet. At the parasitoid-to-host ratio used in our experiments, females of T. buesi usually lay only one egg into each host egg; therefore, the number of eggs laid by a particular female was taken to be equal to the number of hosts parasitized. As a result, the fraction of ovipositing females (those which have laid at least one egg) was calculated for each variant in each replicate of both experiments, and the fecundity (the number of eggs) was determined for each female. In addition, the ENTOMOLOGICAL REVIEW Vol. 93 No. 4 2013

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Table 1. Effects of cold shock on parasitization of grain moth eggs by females of Trichogramma buesi (the first experiment) Conditions and results of the experiment

Experimental variants I

II

Hosts offered during the first exposure Cold shock Mortality before the second exposure, % 1 Hosts infested during the first exposure Fraction of ovipositing females during the second exposure, % 1 Fecundity of ovipositing females during the second exposure, eggs per female 2

III

IV

Yes

Yes

Yes

Yes

No 5.6 a (n = 375)

Yes

No

Yes

No

46.0 b (n = 261)

3.2 a (n = 93)

62.0 c (n = 242)

1.1 a (n = 92) 19

21.3 ± 3.2 b 13.4 ± 5.3 b 19–25 1–28 (n = 3) (n = 148)

VI No No

No

5.7 a (n = 356)

9.7 ± 5.4 a 1–31 (n = 119)

V

(n = 1)

Yes 2.7 a (n = 378) –

No 5.1 a (n = 367) –

1.9 a (n = 370)

3.4 a (n = 348)

25.9±11.2bc 31.4 ± 7.6 c 4–39 20–44 (n = 7) (n = 11)

1

Notes: Percentage calculated for the aggregate data of 8 replicates; the values which were found to be significantly different (p < 0.05) by pairwise comparison using the Mantel-Haenszel χ2 test are marked with different letters (a, b, c, d). 2 Mean, standard deviation, and minimum and maximum values determined for the aggregate data of 8 replicates; the values which were found to be significantly different (p < 0.05) by Tukey's test are marked with different letters (a, b, c, d). n is the sample size.

fraction of females which died before the second exposure was calculated; these individuals were not taken into account when determining the fraction of ovipositing females and their mean fecundity. The occasional females which died during the first exposure or escaped before the end of the second exposure were not taken into account. The fraction of ovipositing females and other biological parameters of Trichogramma wasps are known to vary considerably even in the consecutive generations of the laboratory strains (Reznik et al., 1996). Therefore, the fractions of females that survived and infested the host in different variants of the experiment were compared pairwise by the Mantel-Haenszel χ2 test, using the generation (the replicate of the experiment) as the stratifying variable. The significance of differences in fecundity was assessed by ANOVA, and the variants were compared by Tukey's test. The values given in the text and tables represent aggregate data for all the replicates of each experiment. The results were statistically processed using the SYSTAT software. RESULTS AND DISCUSSION Mortality In the first experiment, 4.1% of females died after cold shock (4°C for 24 h) in all the corresponding ENTOMOLOGICAL REVIEW Vol. 93 No. 4 2013

variants (Table 1, variants I, II, and V). This figure was even slightly (non-significantly) smaller than that in the control (5.4%; variants III, IV, and VI). The previous contact with the host did not affect the mortality rate, either (Table 1). In the second experiment, the mortality of females by the beginning of the second exposure was somewhat lower but the difference between the experimental (2.8%) and the control variants (1.7%) was also non-significant (Table 2). The Fraction of Ovipositing Females First of all, it should be noted that in both experiments, the females which had acquired the experience of parasitizing grain moth eggs during the first exposure, infested eggs of this host considerably more frequently during the second exposure. As can be seen from Table 1, in the first experiment, about half of the females which infested grain moth eggs at 25°C (variants I and III) continued to do so at 15°C, despite the 24-h gap between the two batches of host eggs; however, this “infestation stability” was reduced by cold shock, the difference being significant at p < 0.001 as determined by the Mantel-Haenszel χ2 test. Among the females which ignored grain moth eggs (variants II and IV) and those which were not offered any host (variants V and VI) during the first exposure, only occasional individuals started to infest the hosts at 15°C; the effect of cold shock proved to be nonsignificant in our material.

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Table 2. Effects of cold shock on parasitization of grain moth eggs by females of Trichogramma buesi (the second experiment) Conditions and results of the experiment Hosts offered during the first exposure Cold shock Mortality before the second exposure, % 1 Hosts infested during the first exposure Fraction of ovipositing females during the second exposure, % 1 Fecundity of ovipositing females during the second exposure, eggs per female 2

Experimental variants I

II

III

IV

Yes

V

Yes

Yes

Yes

VI No

No

Yes

No

Yes

No

Yes 2.3 a (n = 486) –

20.2 c (n = 198)

2.4 a (n = 253)

30.1 d (n = 219)

3.7 a (n = 248)

4.0 a (n = 478)

8.0 b (n = 477)

26.5 ± 8.9 a 8–46 (n = 40)

30.0 ± 7.4 a 19–38 (n = 6)

25.8 ± 9.4 a 1–44 (n = 66)

23.2 ± 8.9 a 3–35 (n = 9)

23.8±11.0 a 4–44 (n = 20)

29.5 ± 7.5 a 9–42 (n = 32)

3.4 a (n = 466)

No 1.7 a (n = 474)

No 1.7 a (n = 484) –

Notes: 1 Percentage calculated for the aggregate data of 10 replicates; the values which were found to be significantly different (p < 0.05) by pairwise comparison using the Mantel-Haenszel χ2 test are marked with different letters (a, b, c, d). 2 Mean, standard deviation, and minimum and maximum values determined for the aggregate data of 10 replicates; the values which were found to be significantly different (p < 0.05) by Tukey's test are marked with different letters (a, b, c, d). n is the sample size.

Similar results were also obtained in the second experiment (Table 2): the females which had started parasitizing grain moth eggs during the first exposure (variants I and III), infested the host during the second exposure much more frequently than the females which had not started oviposition (variants II and IV) or had not been offered any host during the first exposure (variants V and VI). In this case, the effect of acquired experience was also reduced by cold shock. Moreover, a twofold decrease in the fraction of females which had no previous contact with grain moth eggs but started to infest them during the second exposure (variants V and VI), caused by cold shock, also proved to be significant (p = 0.013). It should be noted that variants V and VI in the first experiment revealed a comparable degree of difference; however, it was statistically non-significant (p = 0.246), probably due to insufficient sample size. As mentioned above, the tendency to continue infestation of a particular host species once it has started was demonstrated earlier for several species of the genus Trichogramma (Reznik et al., 1997, 2001, 2010, 2011). The effect of previous experience on behavior associated with host seeking, host selection, and infestation is quite common among insect parasitoids (Reznik, 1993; Turlings et al., 1993; Fellowes et al., 2007; Heimpel and Casas, 2008; Hilker and McNeil, 2008).

However, such drastic behavioral differences during the second exposure between the individuals which did and did not infest grain moth eggs during the first exposure, may have resulted not only from the “acquired experience” effect but also from individual variation. It is possible that the females which for some reasons had a greater initial inclination to infesting grain moth eggs were more likely to acquire the experience of parasitization. However, the differences between females with and without such experience cannot be accounted for by the intrastrain variation alone, because the individuals which had not been offered any hosts during the first exposure (variants V and VI), showed the same (Table 1) or almost the same (Table 2) frequency of oviposition during the second exposure as the females which had rejected the hosts (variants II and IV). In addition, processing of the total data for all the females (those which did and did not infest hosts during the first exposure) has shown that in the first experiment, 45.2% of the females which had been in contact with grain moth eggs for 4 h at 25°C infested these eggs at 15°C, whereas only 3.4% of the females which had spent the same time at the same temperature without contact with the host started parasitization at 15°C; the difference is significant at p < 0.001. These parameters were somewhat reduced by cold shock (34.7% and 1.9% with and without contact during the ENTOMOLOGICAL REVIEW Vol. 93 No. 4 2013

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first exposure, respectively) but the difference remained highly significant (p < 0.001). The data of the second experiment reveal the same trend: without cold shock, 16.1% of the females which had been in contact with grain moth eggs at 25°C infested these eggs at 15°C, whereas the females which had not been offered any host started infestation in only 8% of the cases (p < 0.001). As in the first experiment, cold shock decreased the probability of parasitization (to 11.1 and 4.0% of the females which had and had not previously contacted the host, respectively) but the difference remained highly significant (p < 0.001). Thus, judging by the above data, the tendency of T. buesi females to continue infestation once it has started could be also observed after cold shock; the fraction of females which continued parasitization of grain moth eggs was slightly reduced by cold shock, but the difference between individuals which had and had not acquired the experience of infestation was still considerable. The effect of acquired experience was more pronounced in the females which had infested several hosts (Table 1) than in those which had only started parasitization, both with and without cold shock (Table 2); a similar result was obtained in our earlier research (Reznik et al., 2010). Moreover, a cold shock related decrease in the incidence of oviposition was observed both in the females that had the experience of parasitization and in those which were offered eggs of this host for the first time. As mentioned above, in most insects for which this phenomenon was specially studied, cold shock abruptly reduced or even eliminated the effect of acquired experience on the subsequent behavior (Perisse et al., 2007; Lizé et al., 2010). For example, females of Aphidius colemani Viereck (Hymenoptera, Braconidae) preferred to infest aphids Myzus persicae (Sulzer) (Hemiptera, Aphididae) feeding on the previously “memorized” plant; however, this memory was almost completely “erased” by cooling to 5°C for 24 h (Emden et al., 2008). In our experiments with T. buesi, the fraction of females which continued infestation of grain moth eggs was also slightly reduced; however, since this effect was also observed in the females that had no experience of infestation, it must have been the result of direct negative influence of sublethal low temperatures. Thus, our research has confirmed the conclusions made in the previous publications: namely, that the tendency of Trichogramma females to ENTOMOLOGICAL REVIEW Vol. 93 No. 4 2013

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continue infestation of a particular host species once it has started is based not on learning (or not only on learning) but on some other, probably hormonal, mechanisms. The Fecundity of Ovipositing Females In the first experiment, the mean number of hosts infested during the second exposure was noticeably smaller in the females which had the experience of parasitization (Table 1). The observed decline in fecundity can evidently be explained by the fact that freshly emerged females of T. buesi, as well as those of other Trichogramma species, contain 20–30 mature eggs ready for oviposition (Zaslavsky and Mai, 1982; Fleury and Boulétreau, 1993; Hegazi and Khafagi, 2001; Reznik et al., 2001, 2009, 2011). During the first exposure, the infesting females (variants I and III) laid on average 32.2 ± 7.3 eggs and thus totally depleted the “pro-ovigenic component” of their fecundity; therefore, during the second exposure they became able to infest hosts only when the new eggs reached maturity. The females which were not offered any hosts during the first exposure (Table 1, variants V and VI), preserved their initial stock of eggs which ensured their high fecundity during the second exposure. The females which had not infested the hosts during the first exposure (variants II and IV), very rarely started oviposition during the second exposure; their mean fecundity could not be reliably estimated but it was undoubtedly higher than that of the females which had participated in infestation (variants I and III). It can also be seen from Table 1 that cold shock (other conditions being equal) reduced the fecundity both in the females which had infested hosts during the first exposure (variants I and III) and in those which had not been offered any hosts (variants V and VI), even though in the last case the difference was statistically non-significant. According to the design of the second experiment, the females were only just allowed to start infestation during the first exposure, so that their initial “stock” of eggs remained almost intact. Therefore, the fecundity of females infesting grain moth eggs during the second exposure practically did not depend on whether they had infested any hosts during the first exposure. The effect of cold shock on fecundity during the second exposure was also generally non-significant (Table 2), but separate processing of data for the females which had not been offered any host during the first exposure revealed a significant difference (p = 0.028) in fecun-

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dity between variants V and VI. Earlier research by different authors has also shown that adult Trichogramma wasps are negatively affected even by a relatively short-term storage at low, and especially at nearzero temperatures (Jalali, 1992; Boivin, 1994; Yilmaz et al., 2007; Özder, 2008). CONCLUSIONS (1) The effect of cold shock (4°C for 18–24 h) on females of Trichogramma buesi was negative but relatively weak: changes in their mortality were nonsignificant; the fraction of females infesting grain moth eggs and their fecundity slightly decreased. (2) The females which had already started parasitization of grain moth eggs infested this host more frequently than those which had no experience of parasitization, even after cold shock. (3) In most insect species specially studied in this respect, cold shock strongly reduced or even eliminated the effect of learning on subsequent behavior; therefore, the results obtained in this research indicate that the effect of “acquired experience” (the tendency to continue parasitization of a particular host species once it has started) in Trichogramma females is based not on learning but on some other, possibly hormonal, mechanisms. ACKNOWLEDGMENTS The authors are sincerely grateful to T.Ya. Umarova (ZIN RAS) for her help with maintaining the insect cultures and carrying out the experiments. Part of the work was financially supported by the Russian Academy of Sciences research program “Biological Resources of Russia: Their dynamics under the Conditions of Global Climatic and Anthropogenic Influence” and the state contract no. 2-2.20 “Unique Collections of the Zoological Institute.” REFERENCES 1. Bjorksten, T.A. and Hoffmann, A.A., “Separating the Effects of Experience, Size, Egg Load, and Genotype on Host Response in Trichogramma (Hymenoptera: Trichogrammatidae),” J. Ins. Behav. 11 (1), 129–148 (1998). 2. Boivin, G., “Overwintering Strategies of Egg Parasitoids,” in Biological Control with Egg Parasitoids (CABI, Wallingford, 1994), pp. 219–244. 3. Chernyshev, V.B., Ecology of Insects (Moscow State Univ., Moscow, 1996) [in Russian].

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EFFECTS OF COLD SHOCK ON HOST EGG PARASITIZATION 17. Pizzol, J., Pintureau, B., Khoualdia, O., and Desneux, N., “Temperature-Dependent Differences in Biological Traits between Two Strains of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae),” J. Pest Sci. 83 (4), 447–452 (2010). 18. Reznik, S.Ya., “Learning in the Trophic Specialization of Insects,” Trudy Zool. Inst. Ross. Akad. Nauk 193, 5–72 (1993). 19. Reznik, S.Ya. and Vaghina, N.P., “Temperature Effects on Induction of Parasitization by Females of Trichogramma principium (Hymenoptera, Trichogrammatidae),” Zool. Zh. 85 (1), 48–53 (2006a) [Entomol. Rev. 86 (2), 133–138 (2006)]. 20. Reznik, S.Ya. and Vaghina, N.P., “Heat Shock Influences on Parasitization of the Angoumois Grain Moth Sitotroga cerealella Oliv. (Lepidoptera, Gelechiidae) Eggs by the Egg Parasitoid Trichogramma principium Sug. et Sor. (Hymenoptera, Trichogrammatidae) Females,” Entomol. Obozr. 85 (4), 721–726 (2006b) [Entomol. Rev. 86 (8), 861–865 (2006)]. 21. Reznik, S.Ya., Voinovich, N.D., and Umarova, T.Ya., “An Experimental Study of the Fraction of Ovipositing Females and Their Fecundity in Consecutive Generations of Trichogramma (Hymenoptera, Trichogrammatidae),” Zool. Zh. 75 (3), 375–382 (1996). 22. Reznik, S.Ya., Umarova, T.Ya., and Voinovich, N.D., “The Influence of Previous Host Age on Current Host Acceptance in Trichogramma,” Entomol. Exp. Appl. 82 (2), 153–157 (1997). 23. Reznik, S.Ya., Voinovich, N.D., and Umarova, T.Ya., “Egg Retention in the Presence of a Host in Trichogramma Females,” J. Appl. Entomol. 122 (9–10), 555–559 (1998). 24. Reznik, S.Ya., Voinovich, N.D., and Umarova, T.Ya., “Comparative Behavioral Analysis of Ovipositing Females and Females with Egg Retention in Trichogramma principium Sug. et Sor. (Hymenoptera, Trichogrammatidae),” Entomol. Obozr. 80 (3), 545–555 (2001a) [Entomol. Rev. 81 (8), 895–903 (2001)]. 25. Reznik, S.Ya., Voinovich, N.D., and Umarova, T.Ya., “Long-Term Egg Retention and Parasitization in Trichogramma principium (Hymenoptera, Trichogrammatidae),” J. Appl. Entomol. 125 (4), 169–175 (2001b). 26. Reznik, S.Ya., Umarova, T.Ya., and Voinovich, N.D., “Egg Retention in Trichogramma (Hymenoptera: Chalcidoidea: Trichogrammatidae): Learning or Diapause?” Acta Soc. Zool. Bohem. 67 (1), 25–33 (2003).

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