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Comparison of Oviposition on Host Larvae and Rubber Tubes byExorista japonicaTownsend (Diptera: Tachinidae)
Biological Control 14, 7–10 (1999) Article ID bcon.1998.0669, available online at http://www.idealibrary.com on
Comparison of Oviposition on Host Larvae and Rubber Tubes by Exorista japonica Townsend (Diptera: Tachinidae) Chiharu Tanaka, Yooichi Kainoh,1 and Hiroshi Honda Institute of Agriculture and Forestry, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan Received January 12, 1998; accepted October 12, 1998
litura Fabricius), and the cabbage armyworm (Mamestra brassicae L.) in Japan (Oku and Kobayashi, 1974). E. japonica females lay 474.1 ⫾ 131.4 eggs on the host cuticle throughout their lives (Nakamura, 1994). Fecundity of E. japonica rises rapidly a few days after the preoviposition period (2 days), then culminates between days 5 and 7 and falls rapidly afterwards. In previous work, we found that E. japonica approached and oviposited on black rubber tubes, suggesting that physical factors are important in host selection of E. japonica (Tanaka et al., 1999). In this experiment, the frequency of oviposition of E. japonica on model hosts made of black rubber tubes was compared to that on actual hosts. The effect of an oviposition experience on subsequent oviposition on such host models was also examined.
Oviposition responses of Exorista japonica Townsend to host models compared to host larvae, Mythimna separata Walker (Lepidoptera: Noctuidae), were investigated. Total number of examinations of a host model with forelegs during 10 min and the number of eggs laid on a host or host model during 24 h were observed daily for 40 days. Semi-cylindrical black rubber tubes (4.0 ⴛ 1.0 ⴛ 0.5 cm) were provided as host models. The pattern of daily oviposition on host models was similar to that on hosts; oviposition peaked on the 6th to 7th days after adult emergence. However, flies oviposited very few eggs on host models compared to hosts. Previous oviposition experience on M. separata did not affect the acceptance of host models or the number of eggs laid on host models. At first, the pattern of daily examination of a host model was related to the oviposition pattern, while afterwards, it varied independently.
MATERIALS AND METHODS
r 1999 Academic Press
Key Words: Exorista japonica; Tachinidae; parasitoid; host selection; tarsal examination; black rubber tube; Mythimna separata; Noctuidae.
Host and Parasitoid Larvae of the common armyworm, M. separata, were obtained from a stock culture and reared on an artificial diet according to Kanda (1991). The E. japonica culture was established with larvae and pupae provided by Dr. Nakamura, the Japan International Research Center for Agricultural Sciences, Tsukuba, Ibaraki, in September 1996 and maintained after the method of Nakamura (1994). Adult parasitoids were reared in a plastic container (16 ⫻ 28 ⫻ 17 cm) and provided with sugar in a glass petri dish (4.5 cm in diameter, 1.5 cm in depth) and water-soaked dental wick. Five last-instar larvae each of M. separata were placed in clear plastic cups (9 cm in diameter, 3.5 cm in depth). After flies deposited 1 to 3 eggs, M. separata larvae were removed from the rearing cages. After parasitoid pupation, E. japonica puparia were placed in a plastic cup and held until adult parasitoid emergence.
INTRODUCTION
Development of artificial hosts has been investigated for establishment of mass rearing systems for natural enemies. Rearing of Trichogramma on artificial host media is a good example of a successful case. Some Trichogramma can be now reared on artificial diet within plastic host egg-cards. Alternative rearing systems will lead to reduction in the size of rearing facilities and the cost of the product, as well as to changes in the strategy for implementation in the field (Smith, 1996). The tachinid fly Exorista japonica Townsend is a parasitoid of lepidopterous larvae, particularly noctuid larvae such as the common armyworm (Mythimna separata Walker), the common cutworm (Spodoptera
Host Model Black rubber tubes (1.0 cm in diameter, 4.0 cm long) were cut in half in a longitudinal direction, and the semicylindrical tubes were used in the experiment.
1
To whom correspondence should be addressed. E-mail: [email protected]. 7
1049-9644/99 $30.00 Copyright r 1999 by Academic Press All rights of reproduction in any form reserved.
8
TANAKA, KAINOH, AND HONDA
Bioassays Ten mated females were kept in a cage (16 ⫻ 28 ⫻ 17 cm) and exposed every day to a black rubber tube (n ⫽ 5). In a second test, a larva of the common armyworm was exposed to 10 mated female flies until they started to oviposit, and then a black rubber tube was provided in place of the larva (n ⫽ 3). In a third test, a host in a clear plastic cup (9 cm in diameter, 3.5 cm in depth) was exposed to 10 mated females every day (n ⫽ 3). One-day-old females were allowed to mate with males older than 2 days. Hosts and host models were exposed to the flies for 9 h from 09:00 to 18:00 and were changed every day. All experiments continued for 40 days after adult parasitoid at which date the last female fly in the experiment died. The number of eggs on a host or host model during 24 h was counted and, further, the number of ‘examinations’ of the host model by females for 10 min was also observed. Observations of examinations were carried out at random in the afternoon. Examinations consisted of a parasitoid facing and touching the host with their front tarsi. The definition of examination behavior in this experiment followed that of Nakamura (1997). All experiments and insect rearing were conducted at 25°C, 60% RH, and with a photoregime of 16L-8D (light on: 5:00, light off: 21:00). Statistical Analysis The number of eggs deposited at the peak of oviposition on host models was compared to that on a host using a t test. The total lifetime number of eggs deposited on a host model by naive females and by experienced females and on a host was analyzed with Tukey–Kramer tests.
FIG. 1. Oviposition response to rubber tubes with survival rate of naive E. japonica females. Vertical bars indicate S. E. (n ⫽ 5).
The total lifetime number of eggs (⫾S.E.) laid on a host model by females which experienced oviposition on a host was 5.57 ⫾ 1.81 (n ⫽ 3), which was greater than that laid by naive females (2.46 ⫾ 0.479 [⫾S. E.], n ⫽ 5) (Table 1). However, there was no significant difference between these two values. The total number of eggs (⫾S.E.) on a live host was 195 ⫾ 14.8, which was highly significant compared to that on a host model by naive females and experienced females (Table 1). In young flies, the largest number of examinations of a host model by experienced females occurred on the 5th day and for naive females, on the 7th day (Figs. 4 and 5). The frequency of host model examinations was not always related to oviposition. In older flies the number of examinations increased again from the 25th
RESULTS
The number of eggs laid per female each day rose rapidly from the 4th to the 7th day, even in tests in which oviposition occurred only on host models (Figs. 1, 2, and 3). Each oviposition curve fell rapidly afterwards; however, females continued to oviposit till their death. At the peak of oviposition (day 7) on host models the number of eggs laid by naive females (0.183 ⫾ 0.075 [⫾S.E.], n ⫽ 5, day 7) was significantly lower than on a host (9.91 ⫾ 0.586 [⫾S.E.], n ⫽ 3, day 7) (P ⬍ 0.01 by t test). The maximum number of eggs (⫾S.E.) laid on host models by experienced females was 0.657 ⫾ 0.575 (n ⫽ 3, day 14). This also was significantly smaller than the number laid on a host (7.82 ⫾ 0.353 [⫾S.E.], n ⫽ 3, day 14) (P ⬍ 0.01 by t test), while there was no significant difference in the maximum number of eggs laid on host models by naive females (day 7) and experienced females (day 14) (P ⬎ 0.05 by t test).
FIG. 2. Oviposition response to rubber tubes with survival rate of E. japonica females that had experienced oviposition to armyworm, M. separata, for 2 days. Vertical bars indicate S. E. (n ⫽ 3).
OVIPOSITION ON HOST MODELS BY E. japonica
FIG. 3. Oviposition response to armyworm, M. separata, with survival rate of E. japonica females. Vertical bars indicate S.E. (n ⫽ 3).
to the 40th day, but females rarely oviposited on host models during this period. Almost all females in which daily exposure to a host occurred died by the 40th day after the beginning of the experiment (Fig. 3). Females exposed to a host model lived longer, with more than 30% of females in each experiment surviving to the 40th day (Figs. 1 and 2). DISCUSSION
The total number of eggs laid on a host model was extremely small compared to that on a host, indicating that important factors were missing from host models for stimulating female flies to oviposit (Figs. 1, 2, and 3). For example, chemicals derived from hosts or plants on which hosts are feeding may also play an important role in host acceptance. Adults of the tachinid fly Compsilura concinnata (Meigen) were less attracted to freeze-dried gypsy moth larvae Lymantria dispar (L.) extracted with hexane than nonextracted ones, suggesting that a host integumentary chemical has a role in host recognition (Weseloh, 1980). Although we have demonstrated the importance of physical factors in host
9
FIG. 4. Examination of rubber tubes by naive E. japonica females. Vertical bars indicate S. E. (n ⫽ 5).
selection of E. japonica (Tanaka et al., 1999), we need to investigate other factors that elicit oviposition, such as chemical stimuli in future studies. There was no difference in the daily oviposition on host models by naive females versus experienced females (Figs. 1 and 2). Nor were any differences in total number of eggs laid by naive females versus experienced females observed (Table 1). Learning gained through the experience of oviposition to their hosts did not change the acceptance of host models as hosts. In general, learning is an important source of behavioral variability in foraging natural enemies (Vet and Dicke, 1992). Some dipterous parasitoids exhibit associative learning as well as Hymenoptera. Drino bohemica Mesn. which were conditioned to respond to moving trays containing hosts in rearing cages would respond
TABLE 1 Total Number of Eggs Oviposited on Host Models and M. separata Larvae by E. japonica Females for 40 Days Model or host
Female
n
No. eggs (mean ⫾ S.E.)*
Black rubber tube Black rubber tube Host larva
naive experienced —
5 3 3
2.46 ⫾ 0.827A 5.57 ⫾ 3.14A 195 ⫾ 14.8B
* Means within a column followed by the same letters are not significantly different according to Tukey–Kramer test (P ⬍ 0.01).
FIG. 5. Examination of rubber tubes by E. japonica females that had experienced oviposition to armyworm, M. separata, for 2 days. Vertical bars indicate S.E. (n ⫽ 3).
10
TANAKA, KAINOH, AND HONDA
to tray movement even when trays were empty (Monteith, 1963). If E. japonica females have an ability to learn to associate physical or chemical stimuli with their host, the low acceptance rate of host models in this experiment could be improved. The peak of examination frequency by experienced females occurred 2 days earlier than that by naive females (Figs. 4 and 5). These results indicated that the urge to oviposit in experienced females increased with conditioning. Concerning the longevity of E. japonica, the effect of daily oviposition on the longevity of E. japonica females was examined by Nakamura (1994). E. japonica females to which hosts were provided at 4–5 day intervals lived 20 days longer than females that were provided hosts every day. Because the total number of eggs on a host model for 40 days was much smaller than that on a host (Table 1), the longevity of females to which a host model was provided might become longer. Finally, we should improve artificial oviposition substrates to establish effective mass rearing systems of E. japonica. ACKNOWLEDGMENTS We are deeply indebted to Dr. D. Taylor, College of Agrobiological Resources, University of Tsukuba, for critically reading the manuscript.
REFERENCES Kanda, K. 1991. Rearing method of armyworm. In ‘‘Rearing Method of Insects’’ (K. Yushima, S. Kamano, and Y. Tamaki, Eds.), pp. 206–209. Japan Plant Protection Association, Tokyo. [in Japanese]. Monteith, L. G. 1963. Habituation and associative learning in Drino bohemica Mesn. Can. Entomol. 95, 418–426. Nakamura, S. 1994. Parasitization and life history parameters of Exorista japonica (Diptera: Tachinidae) using the common armyworm, Pseudaletia separata (Lepidoptera: Noctuidae) as a host. Appl. Entomol. Zool. 29, 133–140. Nakamura, S. 1997. Ovipositional behavior of the parasitoid fly, Exorista japonica (Diptera: Tachinidae), in the laboratory: Diel periodicity and egg distribution on a host. Appl. Entomol. Zool. 32, 189–195. Oku, T., and Kobayashi, T. 1974. Some dynamic aspects of field populations of the cabbage armyworm, Mamestra brassicae Linne, in Tohoku district. 4. Mortality factors of the later larval and pupal stages. Bull. Tohoku Natl. Agric. Exp. Stn. 47, 165–179. [in Japanese with an English summary]. Smith, S. M. 1996. Biological control with Trichogramma: Advances, successes, and potential of their use. Annu. Rev. Entomol. 41, 375–406. Tanaka, C., Kainoh, Y., and Honda, H. 1999. Physical factors in host selection of the parasitoid fly, Exorista japonica Townsend (Diptera: Tachinidae). Appl. Entomol. Zool. (in press). Vet, L. E. M., and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37, 141–172. Weseloh, R. M. 1980. Host recognition behavior of the tachinid parasitoid, Compsilura concinnata. Ann. Entomol. Soc. Am. 73, 593–601.
Comparison of Oviposition on Host Larvae and Rubber Tubes by Exorista japonica Townsend (Diptera: Tachinidae) Chiharu Tanaka, Yooichi Kainoh,1 and Hiroshi Honda Institute of Agriculture and Forestry, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan Received January 12, 1998; accepted October 12, 1998
litura Fabricius), and the cabbage armyworm (Mamestra brassicae L.) in Japan (Oku and Kobayashi, 1974). E. japonica females lay 474.1 ⫾ 131.4 eggs on the host cuticle throughout their lives (Nakamura, 1994). Fecundity of E. japonica rises rapidly a few days after the preoviposition period (2 days), then culminates between days 5 and 7 and falls rapidly afterwards. In previous work, we found that E. japonica approached and oviposited on black rubber tubes, suggesting that physical factors are important in host selection of E. japonica (Tanaka et al., 1999). In this experiment, the frequency of oviposition of E. japonica on model hosts made of black rubber tubes was compared to that on actual hosts. The effect of an oviposition experience on subsequent oviposition on such host models was also examined.
Oviposition responses of Exorista japonica Townsend to host models compared to host larvae, Mythimna separata Walker (Lepidoptera: Noctuidae), were investigated. Total number of examinations of a host model with forelegs during 10 min and the number of eggs laid on a host or host model during 24 h were observed daily for 40 days. Semi-cylindrical black rubber tubes (4.0 ⴛ 1.0 ⴛ 0.5 cm) were provided as host models. The pattern of daily oviposition on host models was similar to that on hosts; oviposition peaked on the 6th to 7th days after adult emergence. However, flies oviposited very few eggs on host models compared to hosts. Previous oviposition experience on M. separata did not affect the acceptance of host models or the number of eggs laid on host models. At first, the pattern of daily examination of a host model was related to the oviposition pattern, while afterwards, it varied independently.
MATERIALS AND METHODS
r 1999 Academic Press
Key Words: Exorista japonica; Tachinidae; parasitoid; host selection; tarsal examination; black rubber tube; Mythimna separata; Noctuidae.
Host and Parasitoid Larvae of the common armyworm, M. separata, were obtained from a stock culture and reared on an artificial diet according to Kanda (1991). The E. japonica culture was established with larvae and pupae provided by Dr. Nakamura, the Japan International Research Center for Agricultural Sciences, Tsukuba, Ibaraki, in September 1996 and maintained after the method of Nakamura (1994). Adult parasitoids were reared in a plastic container (16 ⫻ 28 ⫻ 17 cm) and provided with sugar in a glass petri dish (4.5 cm in diameter, 1.5 cm in depth) and water-soaked dental wick. Five last-instar larvae each of M. separata were placed in clear plastic cups (9 cm in diameter, 3.5 cm in depth). After flies deposited 1 to 3 eggs, M. separata larvae were removed from the rearing cages. After parasitoid pupation, E. japonica puparia were placed in a plastic cup and held until adult parasitoid emergence.
INTRODUCTION
Development of artificial hosts has been investigated for establishment of mass rearing systems for natural enemies. Rearing of Trichogramma on artificial host media is a good example of a successful case. Some Trichogramma can be now reared on artificial diet within plastic host egg-cards. Alternative rearing systems will lead to reduction in the size of rearing facilities and the cost of the product, as well as to changes in the strategy for implementation in the field (Smith, 1996). The tachinid fly Exorista japonica Townsend is a parasitoid of lepidopterous larvae, particularly noctuid larvae such as the common armyworm (Mythimna separata Walker), the common cutworm (Spodoptera
Host Model Black rubber tubes (1.0 cm in diameter, 4.0 cm long) were cut in half in a longitudinal direction, and the semicylindrical tubes were used in the experiment.
1
To whom correspondence should be addressed. E-mail: [email protected]. 7
1049-9644/99 $30.00 Copyright r 1999 by Academic Press All rights of reproduction in any form reserved.
8
TANAKA, KAINOH, AND HONDA
Bioassays Ten mated females were kept in a cage (16 ⫻ 28 ⫻ 17 cm) and exposed every day to a black rubber tube (n ⫽ 5). In a second test, a larva of the common armyworm was exposed to 10 mated female flies until they started to oviposit, and then a black rubber tube was provided in place of the larva (n ⫽ 3). In a third test, a host in a clear plastic cup (9 cm in diameter, 3.5 cm in depth) was exposed to 10 mated females every day (n ⫽ 3). One-day-old females were allowed to mate with males older than 2 days. Hosts and host models were exposed to the flies for 9 h from 09:00 to 18:00 and were changed every day. All experiments continued for 40 days after adult parasitoid at which date the last female fly in the experiment died. The number of eggs on a host or host model during 24 h was counted and, further, the number of ‘examinations’ of the host model by females for 10 min was also observed. Observations of examinations were carried out at random in the afternoon. Examinations consisted of a parasitoid facing and touching the host with their front tarsi. The definition of examination behavior in this experiment followed that of Nakamura (1997). All experiments and insect rearing were conducted at 25°C, 60% RH, and with a photoregime of 16L-8D (light on: 5:00, light off: 21:00). Statistical Analysis The number of eggs deposited at the peak of oviposition on host models was compared to that on a host using a t test. The total lifetime number of eggs deposited on a host model by naive females and by experienced females and on a host was analyzed with Tukey–Kramer tests.
FIG. 1. Oviposition response to rubber tubes with survival rate of naive E. japonica females. Vertical bars indicate S. E. (n ⫽ 5).
The total lifetime number of eggs (⫾S.E.) laid on a host model by females which experienced oviposition on a host was 5.57 ⫾ 1.81 (n ⫽ 3), which was greater than that laid by naive females (2.46 ⫾ 0.479 [⫾S. E.], n ⫽ 5) (Table 1). However, there was no significant difference between these two values. The total number of eggs (⫾S.E.) on a live host was 195 ⫾ 14.8, which was highly significant compared to that on a host model by naive females and experienced females (Table 1). In young flies, the largest number of examinations of a host model by experienced females occurred on the 5th day and for naive females, on the 7th day (Figs. 4 and 5). The frequency of host model examinations was not always related to oviposition. In older flies the number of examinations increased again from the 25th
RESULTS
The number of eggs laid per female each day rose rapidly from the 4th to the 7th day, even in tests in which oviposition occurred only on host models (Figs. 1, 2, and 3). Each oviposition curve fell rapidly afterwards; however, females continued to oviposit till their death. At the peak of oviposition (day 7) on host models the number of eggs laid by naive females (0.183 ⫾ 0.075 [⫾S.E.], n ⫽ 5, day 7) was significantly lower than on a host (9.91 ⫾ 0.586 [⫾S.E.], n ⫽ 3, day 7) (P ⬍ 0.01 by t test). The maximum number of eggs (⫾S.E.) laid on host models by experienced females was 0.657 ⫾ 0.575 (n ⫽ 3, day 14). This also was significantly smaller than the number laid on a host (7.82 ⫾ 0.353 [⫾S.E.], n ⫽ 3, day 14) (P ⬍ 0.01 by t test), while there was no significant difference in the maximum number of eggs laid on host models by naive females (day 7) and experienced females (day 14) (P ⬎ 0.05 by t test).
FIG. 2. Oviposition response to rubber tubes with survival rate of E. japonica females that had experienced oviposition to armyworm, M. separata, for 2 days. Vertical bars indicate S. E. (n ⫽ 3).
OVIPOSITION ON HOST MODELS BY E. japonica
FIG. 3. Oviposition response to armyworm, M. separata, with survival rate of E. japonica females. Vertical bars indicate S.E. (n ⫽ 3).
to the 40th day, but females rarely oviposited on host models during this period. Almost all females in which daily exposure to a host occurred died by the 40th day after the beginning of the experiment (Fig. 3). Females exposed to a host model lived longer, with more than 30% of females in each experiment surviving to the 40th day (Figs. 1 and 2). DISCUSSION
The total number of eggs laid on a host model was extremely small compared to that on a host, indicating that important factors were missing from host models for stimulating female flies to oviposit (Figs. 1, 2, and 3). For example, chemicals derived from hosts or plants on which hosts are feeding may also play an important role in host acceptance. Adults of the tachinid fly Compsilura concinnata (Meigen) were less attracted to freeze-dried gypsy moth larvae Lymantria dispar (L.) extracted with hexane than nonextracted ones, suggesting that a host integumentary chemical has a role in host recognition (Weseloh, 1980). Although we have demonstrated the importance of physical factors in host
9
FIG. 4. Examination of rubber tubes by naive E. japonica females. Vertical bars indicate S. E. (n ⫽ 5).
selection of E. japonica (Tanaka et al., 1999), we need to investigate other factors that elicit oviposition, such as chemical stimuli in future studies. There was no difference in the daily oviposition on host models by naive females versus experienced females (Figs. 1 and 2). Nor were any differences in total number of eggs laid by naive females versus experienced females observed (Table 1). Learning gained through the experience of oviposition to their hosts did not change the acceptance of host models as hosts. In general, learning is an important source of behavioral variability in foraging natural enemies (Vet and Dicke, 1992). Some dipterous parasitoids exhibit associative learning as well as Hymenoptera. Drino bohemica Mesn. which were conditioned to respond to moving trays containing hosts in rearing cages would respond
TABLE 1 Total Number of Eggs Oviposited on Host Models and M. separata Larvae by E. japonica Females for 40 Days Model or host
Female
n
No. eggs (mean ⫾ S.E.)*
Black rubber tube Black rubber tube Host larva
naive experienced —
5 3 3
2.46 ⫾ 0.827A 5.57 ⫾ 3.14A 195 ⫾ 14.8B
* Means within a column followed by the same letters are not significantly different according to Tukey–Kramer test (P ⬍ 0.01).
FIG. 5. Examination of rubber tubes by E. japonica females that had experienced oviposition to armyworm, M. separata, for 2 days. Vertical bars indicate S.E. (n ⫽ 3).
10
TANAKA, KAINOH, AND HONDA
to tray movement even when trays were empty (Monteith, 1963). If E. japonica females have an ability to learn to associate physical or chemical stimuli with their host, the low acceptance rate of host models in this experiment could be improved. The peak of examination frequency by experienced females occurred 2 days earlier than that by naive females (Figs. 4 and 5). These results indicated that the urge to oviposit in experienced females increased with conditioning. Concerning the longevity of E. japonica, the effect of daily oviposition on the longevity of E. japonica females was examined by Nakamura (1994). E. japonica females to which hosts were provided at 4–5 day intervals lived 20 days longer than females that were provided hosts every day. Because the total number of eggs on a host model for 40 days was much smaller than that on a host (Table 1), the longevity of females to which a host model was provided might become longer. Finally, we should improve artificial oviposition substrates to establish effective mass rearing systems of E. japonica. ACKNOWLEDGMENTS We are deeply indebted to Dr. D. Taylor, College of Agrobiological Resources, University of Tsukuba, for critically reading the manuscript.
REFERENCES Kanda, K. 1991. Rearing method of armyworm. In ‘‘Rearing Method of Insects’’ (K. Yushima, S. Kamano, and Y. Tamaki, Eds.), pp. 206–209. Japan Plant Protection Association, Tokyo. [in Japanese]. Monteith, L. G. 1963. Habituation and associative learning in Drino bohemica Mesn. Can. Entomol. 95, 418–426. Nakamura, S. 1994. Parasitization and life history parameters of Exorista japonica (Diptera: Tachinidae) using the common armyworm, Pseudaletia separata (Lepidoptera: Noctuidae) as a host. Appl. Entomol. Zool. 29, 133–140. Nakamura, S. 1997. Ovipositional behavior of the parasitoid fly, Exorista japonica (Diptera: Tachinidae), in the laboratory: Diel periodicity and egg distribution on a host. Appl. Entomol. Zool. 32, 189–195. Oku, T., and Kobayashi, T. 1974. Some dynamic aspects of field populations of the cabbage armyworm, Mamestra brassicae Linne, in Tohoku district. 4. Mortality factors of the later larval and pupal stages. Bull. Tohoku Natl. Agric. Exp. Stn. 47, 165–179. [in Japanese with an English summary]. Smith, S. M. 1996. Biological control with Trichogramma: Advances, successes, and potential of their use. Annu. Rev. Entomol. 41, 375–406. Tanaka, C., Kainoh, Y., and Honda, H. 1999. Physical factors in host selection of the parasitoid fly, Exorista japonica Townsend (Diptera: Tachinidae). Appl. Entomol. Zool. (in press). Vet, L. E. M., and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37, 141–172. Weseloh, R. M. 1980. Host recognition behavior of the tachinid parasitoid, Compsilura concinnata. Ann. Entomol. Soc. Am. 73, 593–601.