Appl. Entomol. Zool. 38 (2): 215–223 (2003)

Development of a tachinid parasitoid, Gymnosoma rotundatum (Diptera: Tachinidae) on Plautia crossota stali (Heteroptera: Pentatomidae),† and its effects on host reproduction‡

Morio HIGAKI* Laboratory of Entomology, Department of Plant Protection, National Institute of Fruit Tree Science; Tsukuba, Ibaraki 305–8605, Japan (Received 4 March 2002; Accepted 16 January 2003)

Abstract The developmental biology of a tachinid parasitoid (Gymnosoma rotundatum) and the effects of its parasitism on re- production of the host, the brown-winged green bug (Plautia crossota stali), were studied. The tachinid females laid eggs on the abdominal tergum of the hosts and larvae penetrated into and developed in their body cavities. A single mature larva exited from each of the hosts and pupariated. Even in cases when the fly deposited two eggs onto a host, only one maggot survived to maturity. The hosts died within a day after the maggot emerged. The percentage of larvae emerging from hosts, larval duration, and puparial weight were not affected by the number (one or two) of parasitoid eggs per host. The duration of the larval stage was longer and puparia were bigger in parasitoids that emerged from fe- male hosts than those that emerged from male hosts; G. rotundatum was so variable in body size that larger individu- als tended to emerge from larger hosts. Though parasitoids did develop even in unfed hosts, such puparia were much smaller in size than puparia developed in fed hosts. The reproductive abilities of the parasitized bugs gradually re- duced as the tachinid maggots matured. In parasitized female bugs, ovaries gradually shrank with a suppression of oviposition. Both the number of laid eggs and the percentage of viable eggs decreased rapidly after the 8th day of par- asitization. In parasitized male bugs, the fertility rates decreased rapidly after the 8th day of parasitization.

Key words: Tachinidae; Gymnosoma rotundatum; Pentatomidae; Plautia crossota stali; parasitism

A tachinid parasitoid, Gymnosoma rotundatum INTRODUCTION parasitizes the live adults of the brown-winged Parasitoids are mainly comprised of hy- green bug, Plautia crossota stali, a serious fruit menopteran and dipteran insects. Some species tree pest in Japan (Yamada and Miyahara, 1979). among them kill or paralyze the hosts at parasitiza- The impact of the tachinid on P. c. stali populations tion (idiobionts), and other species develop in the has been evaluated and the fly has been recognized body cavities of live host insects that continue to to be a prominent biological control agent (Yamada feed and develop (koinobionts). On the latter hosts, and Miyahara, 1979; Oda, 1980). However, there is parasitism causes various harmful effects such as little known about the basic biology of G. rotunda- the inhibition of development and the atrophy of tum and its influence upon its host. Thus, to clarify the reproductive organs (Clausen, 1940). the traits of the tachinid fly as a natural enemy, the Tachinid flies are exclusively endoparasitic development of G. rotundatum on P. c. stali and species that develop in the cavities of live hosts. the reproductive ability of parasitized hosts were They have a vast host range that spreads over many studied. taxonomic groups of insects, including the phy- tophagous species (Belshaw, 1994). Accordingly, MATERIALS AND METHODS tachinids are considered as potentially important biological control agents as are the hymenopteran Stock culture. The stock culture of G. rotunda- parasitoids (Greathead, 1986; Grenier, 1988). tum used for the present study originated from

* To whom correspondence should be addressed at: E-mail: [email protected] † The scientific name, Plautia crossota stali is used for this species in the present paper according to its use by Tomokuni et al. (1993), although Plautia stali has been commonly used. ‡ Contribution No. 1288 of the National Institute of Fruit Tree Science.

215 216 M. HIGAKI about 20 adults collected from Ushiku City, Ibaraki hosts were checked daily and puparial weight was Prefecture (36.0°N), in early September 1998. measured by an electric balance the day after pu- Adult flies were reared in a netted stainless steel pariation. The period from oviposition to larval cage (30ϫ30ϫ30 cm), and kept at 22.5°C and a emergence was noted, and subsequently treated as photoperiod of 16L–8D. Sugar cubes were given as the larval duration in this study, as the period of the food, and water-soaked cotton wool was given as egg stage was difficult to determine without impos- the water supply. P. c. stali adults that were reared ing stress on the hosts. On the day of eclosion, in the laboratory according to the method de- adult flies were weighed by an electric balance and scribed by Moriya et al. (1985) were provided as their head width was measured under a binocular hosts. They were randomized from large culture. microscope. Exposure to parasitization was carried out by plac- Effects of hosts’ nutritional condition on ta- ing adult bugs to be parasitized into cages which chinid larval development and puparial weight. housed male and female flies. Thirty bugs para- Female adult bugs on which one parasitoid egg was sitized by G. rotundatum were reared in a plastic deposited on the 14th day of adult stage were di- container (9 cm highϫ15 cm in diameter). On the vided into three groups; the 1st and the 2nd groups top of the container, a hole (6 cm in diameter) cov- were allowed to feed every day and every five days, ered with nylon gauze served for ventilation. For respectively, and the 3rd group was kept without the hosts, raw peanuts served as food and water- food. Water was supplied to all three groups. The soaked cotton wool served as the water supply. G. parasitized female bugs were paired with mature rotundatum individuals that emerged from the intact males and reared in petri dishes (2 cm hosts and soon pupariated were kept on layers of highϫ9 cm in diameter). Parasitoid emergence moist tissue paper in a plastic cup (4 cm highϫ from the host and the number of eggs laid by para- 5 cm in diameter) until they emerged as adults. sitized bugs were checked every day. Puparia were This procedure was conducted for maintaining weighed by an electric balance one day after pu- successive generations of G. rotundatum. Fol- pariation. lowing experiments were conducted at 22.5°C and Effects of parasitization on host fecundity and a photoperiod of 16L–8D except when otherwise fertility. To elucidate the effects of parasitization indicated. on host fecundity, female bugs were exposed to Fecundity and longevity of parasitoid flies. A parasitization on either the 4th or the 14th day of male and a female of G. rotundatum were paired in adult stage. Female bugs are immature on day 4 a plastic container (9 cm highϫ15 cm in diameter) and mature on day 14 because pre-oviposition pe- on the day of their emergence and were kept at riod is about 11–12 days (Moriya, 1995). These fe- 21–22°C and a photoperiod of 16L–8D. Other rear- male bugs on which female flies laid one or two ing conditions were the same as those described in eggs were paired with unparasitized matured males the stock culture. Five stink bug adults were pro- in petri dishes (2 cm highϫ9 cm in diameter). vided as hosts into each container. On the next day, Other experiments in the present study showed that they were removed and five new adult stink bugs even if the flies deposited two eggs onto a single were introduced. The number of eggs laid on the host, only one maggot could survive to maturity. bugs was checked daily. This procedure was re- Therefore, the female bugs with one or two para- peated until the flies died. site eggs were pooled in this experiment. The num- Effects of host sex, host body size, and the ber of eggs laid by the female bugs was examined number of parasitoid eggs per host on tachinid daily. The percentage of fertilized eggs was also larval development and puparial weight. Both examined because the eye spots of the embryos be- sexes of the 10-day-old adult bugs of various body came visible through the egg shell by the 5th day sizes were exposed to parasitization in the cages after oviposition at 22.5°C. which housed male and female flies. Of these, the In addition, ovary size and egg size were exam- hosts on which one or two parasitoid eggs were de- ined. Pairs of ovaries were extracted by dissection posited were individually weighed by an electric under a binocular microscope and ovaries were in- balance and reared in a petri dish (2 cm highϫ9cm dividually weighed by an electric balance after hav- in diameter). Parasitoid larvae emerging from the ing been dried at 80°C for about one day. P. c. stali Parasitization of a Stink Bug by a Tachinid 217 lays cylindrical eggs as a batch of about 14 eggs; performed with Stat View-J version 5.0 (SAS Insti- three to five of these eggs were selected randomly tute Inc., 1998). from the egg batches laid by parasitized and intact females in order to measure egg diameters under a RESULTS binocular microscope. In males, adult bugs were exposed to parasitiza- Fecundity and longevity of parasitoid flies tion on the 11th day of the adult stage when male Adults of G. rotundatum mated readily in a plas- bugs already mature and often show mating behav- tic container and a netted stainless steel cage. Flies ior. These males were reared individually in a petri were often observed to mate on the day of emer- dish. An unparasitized virgin female was intro- gence. Most female flies began to lay eggs on the duced into each petri dish for two days, and then day after adult emergence. Eggs were laid on the was replaced with another virgin female. Removed abdominal tergum of the host. Although the females were reared individually in petri dishes to longevity of adult parasitoids varied considerably, examine their fecundity and the percentage of fer- males tended to survive longer than females; mean tilized eggs. This procedure was repeated until the (ϮSE) longevity was 20.1 (Ϯ2.5) days and 15.8 male bug died. (Ϯ2.0) days in males and females with oviposition, Data analysis. All statistical analyses were respectively (Fig. 1). Females oviposited almost

Fig. 1. Egg production and longevity of G. rotundatum adults. nϭ17 for each sex.

Table 1. Effects of host sex and the number of parasitoid eggs per host (1 egg and 2 eggs/host) on larval development and puparial weight of G. rotundatum

P. c. stali G. rotundatum

No. of larvae emerging Fresh weight of puparium No. of hosts parasitized Larval duration in daysa from host in mga Host sex 1 egg/host 2 eggs/host 1 egg/host 2 eggs/host 1 egg/host 2 eggs/host 1 egg/host 2 eggs/host

Male 50 50 27 26 15.22Ϯ0.22 15.65Ϯ0.28 35.66Ϯ0.74 34.51Ϯ0.86 Female 50 50 30 31 16.73Ϯ0.30 16.84Ϯ0.45 42.34Ϯ1.07 41.39Ϯ1.22 p (ANOVA) Ͻ0.001 0.038 Ͻ0.001 Ͻ0.001

a MeanϮSE. Two-way ANOVA with two factors of the host sex and the number of parasitoid eggs was conducted first and showed that only the host sex was responsible for significant differences in larval duration (host sex: pϽ0.001, the number of parasitoid eggs: pϭ0.428, the interaction of the two factors: pϭ0.630) and in fresh weight of puparium (host sex: pϽ0.001, the number of parasitoid eggs: pϭ0.305, the interaction of the two factors: pϭ0.925). Then, one-way ANOVA was performed by regarding the host sex as the main factor, so that significant differences were observed in all columns. 218 M. HIGAKI 0.79 (24) 0.70 (23) 0.001 c,g,h Ϯ Ϯ Ͻ 0.255). 0.020). 0.271). 0.031). ϭ ϭ ϭ p p ϭ p p 0.70 (24) 32.03 0.60 (22) 24.71 Body weight in mg Body weight 0.001 1.312, 5.592, 1.225, Ϯ Ϯ 4.796, Ͻ ϭ ϭ ϭ ϭ F F F F 1, 1, 1, 1, Adult ϭ ϭ ϭ ϭ he concerned coulmns.

Fig. 2. The relationship between host size and parasitoid G. rotundatum G. 0.02 (24) 29.35 0.03 (23) 25.40

0.001 size. The fresh weight of the puparium is plotted against the b,f,h Ϯ Ϯ Ͻ

)] of fresh weight of the host. ***: Significant at 0.1% level. n SE ( Ϯ daily during their lifetime (14.9 [Ϯ2.0] days), and the total number (ϮSE) of eggs laid by a single fe- Head width in mm 0.03 (24) 2.98 0.02 (23) 2.79 0.001 male was 98.1 (Ϯ13.2). Ϯ Ϯ Ͻ Effects of host sex, host body size, and the num- 0.017, the interaction of the two factors: df 0.017, the interaction of two factors: df 0.151, the interaction of two 0.265, the interaction of the two factors: df 0.265, the interaction of two

0.170, the interaction of the two factors: df 0.170, the interaction of two ber of parasitoid eggs per host on tachinid lar- ϭ ϭ ϭ p p ϭ p

p val development and puparial weight

a,e Parasitized hosts died without exception within a 5.930, 2.095, 1.261, 0.10 (25) 2.98 0.14 (23) 2.85 1.910, ϭ ϭ ϭ day after the maggot emerged. The maggots pu- Ϯ Ϯ ϭ F F F F

1, 1, pariated within a day after emergence from the 1, 1, ϭ ϭ ϭ

ϭ hosts. Table 1 shows the effects of host sex and the number of eggs per host on larval development and puparial weight of the parasitoid fly. Even if the flies deposited two eggs onto a single host, only 0.12 (24) 12.36 0.13 (25) 12.44 Ϯ Ϯ Puparial duration in days one maggot could survive to maturity. Percentage of larvae emerging from hosts was not affected by either the host sex or the number of parasitoid eggs 0.001, parasitoid sex: df 0.001, parasitoid sex: df 0.001, parasitoid sex: 0.001, parasitoid sex: df 0.001, parasitoid sex: 0.119, parasitoid sex: df 0.119, parasitoid sex: Ͻ Ͻ Ͻ per host. On the other hand, the larval duration and p p ϭ p p purparial weight of the flies were affected by the

a,d,h host sex but not by the number of parasitoid eggs 0.38 (25) 12.46 0.29 (23) 12.00 17.792, 64.473, 2.483, 36.624, Ϯ Ϯ ϭ ϭ ϭ per host. The larval period of parasitoid tended to ϭ F F F F be longer in female hosts than in male hosts. Mean Table 2. traits [mean on developmental and parasitoid sex of host sex Effects 1, 1, 1, 1, ϭ ϭ ϭ ϭ puparial weights from female hosts were about 20% larger than those from male hosts. Larval and puparial durations and adult body 0.20 (24) 17.20 0.26 (25) 15.65 Male Female Male Femalesize of both Male sexes in G. Female rotundatum Maleare shown Female in Ϯ Ϯ Larval duration in days Larval Table 2. Two-way ANOVA with two factors of the host sex and the parasitoid sex showed that the host sex was responsible for differences in larval dura- tion and adult body size of parasitoids, and that the variance associated with the parasitoid sex was ex- Flies that failed to emerge as adults were excluded. as adults were Flies that failed to emerge df (host sex: ANOVA Two-way df (host sex: ANOVA Two-way observed in t were so that the significant differences as the main factor, the host sex regarding performed by was ANOVA One-way Flies that died in larval or puparial stage were excluded. or puparial stage were Flies that died in larval excluded. were after adult emergence Flies that died within a day df (host sex: ANOVA Two-way Two-way ANOVA (host sex: df (host sex: ANOVA Two-way (ANOVA) 0.009 0.002 a b c d e f g h Host sex P. c. staliP. rotundatum G. Female 16.17 Malep 15.28 tremely small. Neither the host sex nor the para- Parasitization of a Stink Bug by a Tachinid 219

sitoid sex had meaningful effects on the parasitoid

a,f puparial durations. Sex ratios were about 1 : 1 in parasitic flies that emerged from both sexes of the 2.07 ( 9) a 1.50 (19) a 1.66 (16) b hosts. G. rotundatum was highly variable as regards Ϯ Ϯ Ϯ adult body size: the largest fly was 39% larger in head width than the smallest fly. The relationship between host size and para- sitoid size is shown in Fig. 2. The correlation was significant at 0.1% level in both sexes of host; 1.24 (20) a 44.16 1.42 (15) a 41.98 1.20 (17) b 27.23 Ϯ Ϯ Ϯ larger parasitoids tended to emerge from larger

Fresh weight of puparium in mg weight Fresh hosts. l condition was responsible for difference responsible l condition was

fferences for any of the factors (hosts’ nutri- for any fferences Effects of hosts’ nutritional conditions on ta- G. rotundatum G. at the 5% level by Scheffé’s test. Scheffé’s by at the 5% level rent at the 5% level. chinid larval development and puparial weight a,e 0.37 ( 9) 41.33 0.58 (16) 27.42 0.29 (19) 42.49 Percentage of larvae emerging from female bugs Ϯ Ϯ Ϯ and adult emergence, and the means of larval dura- tion were not significantly different among the three nutritional conditions of the hosts (Table 3). On the other hand, mean puparial weight was sig- nificantly smaller in the unfed treatment. Most of 0.26 (20) 17.33 0.27 (17) 16.63 0.35 (15) 16.32 0.522). The hosts’ nutritional condition was regarded as the main factor, regarded 0.522). The hosts’ nutritional condition was

Male Female Male Female the parasitized female bugs laid their eggs for Ϯ Ϯ Ϯ ϭ p about one week, and mating behavior was observed in some parasitized females. Host females that fed freely laid significantly more eggs than those that d 0.724).

ϭ were restrictively fed and those that were unfed. p

Effects of parasitization on host fecundity and

emerged (%) emerged fertility Percentages of female bugs that could oviposit were 93% and 100% when the bugs were para- c,d sitized on the 4th and the 14th day of the adult stage, respectively. However, ovaries of parasitized hosts (%)

0.571, the interaction of the two factors: 0.571, the interaction of two bugs gradually shrank after the 6th day of parasiti- ϭ

p zation (Fig. 3), and oviducts coincidentally came to be devoid of eggs. On the other hand, intact fe- males retained mature ovaries for at least two a,b 0.064, the interaction of the two factors: 0.064, the interaction of two weeks. The loss of functional ovaries was reflected ϭ p 2.47 (40) a 40 (66.7) 34 (56.7) 16.07 1.24 (36) b 36 (60.0) 29 (48.3) 16.65 1.78 (39) b 39 (48.8) 33 (41.3) 15.82 as a suppression of oviposition. Percentage of Ϯ Ϯ Ϯ ovipositing host females decreased rapidly prior to their death, with the result that the mean number of 0.001, parasitoid sex: 0.001, parasitoid sex:

Ͻ laid eggs decreased (Fig. 4A, B). The percentage of p Table 3. traits of and developmental nutritional levels of the parasitized hosts different Fecundity fertilized eggs decreased rapidly (Fig. 4C, D). Clutch size and egg volume decreased (Figs. 5 and 0.079, parasitoid sex: 0.079, parasitoid sex: P. c. staliP. 6), and percentage rotundatum G. of malformed eggs increased ϭ p (data not shown). As a result, female bugs para- ).

n sitized on the 4th and the 14th day of adult stage produced 8.6 and 34.8 viable eggs after parasitiza- SE (

Ϯ tion, respectively (Table 4). The number of viable Hosts’ No. of No. of No. of larvae No. of duration in days Larval condition parasitized hosts by

nutritional hosts laid eggs from emerging adults that eggs produced by unparasitized females was 170.9 The hosts from which parasitoid larvae emerged were examined. Means followed by the same letters are not significantly different the same letters are not significantly by Means followed examined. were emerged parasitoid larvae The hosts from which using chi-square test. in the same column at 5% level no significant differences There were Mean emerged. parasitoid larvae The numeral is equal to the number of hosts from which tional condition: Two-way ANOVA with two factors of the hosts’ nutritional condition and the parasitoid sex shows that there are no significant di shows factors of the hosts’ nutritional condition and parasitoid sex with two ANOVA Two-way and the means were compared by Scheffé’s test. Means followed by the same letters in the same column are not significantly diffe the same letters in column are not significantly by test. Means followed Scheffé’s compared by and the means were Two-way ANOVA with two factors of the hosts’ nutritional condition and the parasitoid sex shows that only the hosts’ nutritiona that only shows factors of the hosts’ nutritional condition and parasitoid sex with two ANOVA Two-way (hosts’ nutritional condition: a b c d e f Fed every 5 days every Fed 60 21.61 Fed every day every Fed 60 36.75 Unfed 80 18.23 for the lifetime of the insect, and 135.6 after the 220 M. HIGAKI

Fig. 3. Changes in ovary size of unparasitized and parasitized female bugs. The parasitized female bugs were prepared by ex- posing female bugs to parasitization on the 14th day of adult stage. Days after parasitization are shown on the right of each figure. Means are indicated by arrows.

Fig. 4. Longevity and fecundity of parasitized female bugs. The parasitized female bugs were prepared by exposing female bugs to parasitization on the 4th day (A and C) or 14th day (B and D) of the adult stage. Parasitization of a Stink Bug by a Tachinid 221

Fig. 5. Changes in batch size of unparasitized and parasitized female bugs. The parasitized female bugs were prepared by exposing female bugs to parasitization on the 14th day of the adult stage. Days after parasitization are shown on the left of each figure.

14th day of the adult stage. In males, the survival rates were high until the 14th day after parasitization, but the number of in- dividuals that were able to fertilize eggs decreased rapidly after the 8th day of parasitization (Fig. 7).

DISCUSSION Tachinid parasitoids often affect the reproductive abilities of pentatomid bugs (Beard, 1940; Clausen, 1940; Shahjahan, 1968; Harris and Todd, 1982). When adult females of Nezara viridula were para- sitized by Trichopoda pennipes, fecundity was not reduced relative to that of unparasitized females. Fig. 6. Changes in egg size of unparasitized and para- However, the lifetime fecundity of unparasitized sitized female bugs. The parasitized female bugs were pre- females was much higher than that of parasitized pared by exposing female bugs to parasitization on the 18th females due to the difference in longevity (Shahja- day of the adult stage. Open and closed circles indicate mean han, 1968; Harris and Todd, 1982). On the other diameters of eggs laid by unparasitized and parasitized female bugs, respectively. Vertical bars indicate standard deviations. hand, Nysius ericeae females parasitized by The sample size is shown in parentheses. ***: Significant dif- Hyalomya aldrichi can only rarely lay eggs ference at 0.1% level between eggs laid by parasitized and in- (Clausen, 1940). Thus, the effect of tachinid para- tact bugs (ANOVA). sitism upon pentatomid bugs varies from species to 222 M. HIGAKI

Table 4. Effects of parasitization on longevity and fecundity of the host

Host age at parasitization N Longevity in daysa No. of eggs laida No. of fertilized eggsa

Day 4 30 22.63Ϯ0.44 14.40Ϯ1.39 8.63Ϯ1.23 (18.63Ϯ0.44)b Day 14 35 31.71Ϯ0.34 45.26Ϯ2.59c 34.80Ϯ3.20c (17.71Ϯ0.36)b Control 40 42.45Ϯ3.31 212.45Ϯ21.73 170.93Ϯ18.32 (166.48Ϯ20.20)c (135.60Ϯ16.74)c

a MeanϮSE. b Longevity after parasitization. c The number of eggs laid after the 14th day of the adult stage.

ready mature eggs in ovarioles appear to be laid in- dependent of parasitization. Once the endoparasite gets into the host body, its development must depend on the nutrients in the host. The nutritional condition of P. c. stali affected the body size of G. rotundatum, though it did not affected the percentage of maggots that matured (Table 3). G. rotundatum individuals that emerged from restrictively fed bugs were similar in body size to those that emerged from bugs fed freely, and were significantly larger than those from unfed hosts (Table 3). Thus, when the hosts were fed re- strictively, nutrients taken by the host were mostly used for the development of parasitoid larvae, and therefore the egg production of those hosts was re- duced. In contrast to the study of parasitized female Fig. 7. Longevity (A) and fertility (B) of unparasitized bugs, the reproductive ability of parasitized male and parasitized male bugs. The parasitized male bugs were prepared by exposing male bugs to parasitization on the 11th bugs has been poorly studied. Beard (1940) re- day of the adult stage. ported that the testes of Anasa tristis males were degenerated by parasitization with T. pennipes, but species. that their reproductive activity was not reduced. The present study showed that adults of P. c . However, the reproductive ability of these males stali parasitized by G. rotundatum lost their repro- was not studied over the duration of a lifetime. The ductive abilities prior to death: the number of laid present study demonstrated that parasitized P. c . eggs, clutch size, egg size and the percentage of vi- stali males retained their reproductive ability for able eggs began to decrease approximately one approximately one week, and this ability was re- week after parasitization (Figs. 4, 5, and 6). It was duced thereafter (Fig. 7). The cause of this reduc- also clarified by dissection that the ovaries of para- tion is not clear. Testis and mating behavior of par- sitized females shrank after six days of parasitiza- asitized male bugs should be examined in detail. tion (Fig. 3). When mature female bugs were para- Thus, the present study showed that parasitiza- sitized, they were able to lay egg masses normally tion by G. rotundatum causes considerable reduc- several times. On the other hand, when young fe- tion in reproductive ability of P. c. stali. These re- male bugs were parasitized, they laid considerably sults suggest that this fly potentially has the ability fewer eggs (Table 4). These findings suggest that to control the density of P. c. stali populations. To parasitization inhibits egg production by hamper- quantify the impact of G. rotundatum on P. c. stali ing egg development in ovarioles. In contrast, al- populations, seasonal abundance of this fly and Parasitization of a Stink Bug by a Tachinid 223 percentage of parasitism in the field should be esti- tion of the southern green stink bug, Nezara viridula, as mated. affected by parasitization by Trichopoda pennipes. En- tomol. Exp. Appl. 31: 409–412. ACKNOWLEDGEMENTS Moriya, S. (1995) Ecological studies on the brown-winged green stink bug, Plautia stali Scott, with special reference I am deeply obliged to Ishizue Adachi (National Institute of to its occurrence and adult movement. Bull Okinawa Fruit Tree Science: NIFTS) for critically reading an early draft Agric. Exp. Sta. Suppl. 5: 1–135 (in Japanese). of this manuscript. I also thank Hidenari Kishimoto, Yasuki Moriya, S., M. Shiga and M. Mabuchi (1985) A method for Kitashima, and Hisako Okano (NIFTS) for their collaboration successive rearing of the brown-winged green bug, Plau- in the rearing of the insects used in this study. tia stali Scott (Heteroptera: Pentatomidae). Bull. Fruit REFERENCES Tree Res. Stn. A12: 133–143 (in Japanese with English summary). Beard, R. L. (1940) Parasitic castration of Anasa tristis DeG. Oda, M. (1980) Life cycle and migration of Plautia stali. by Trichopoda pennipes Fab., and its effect on reproduc- Plant Protect. 34: 309–314 (in Japanese). tion. J. Econ. Entomol. 33: 269–272. SAS Institute Inc. (1998) Stat View User’s Manual, Version Belshaw, R. (1994) Life history characteristics of Tachinidae 5. SAS Institute Inc., Cary, NC. (Diptera) and their effect on polyphagy. In Parasitoid Shahjahan, M. (1968) Superparasitization of the southern Community Ecology (B. A. Hawkins and W. Sheehan green stink bug by the tachinid parasite Trichopoda pen- eds.). Oxford University Press, New York, pp. 145–162. nipes and its effect on the host and parasite survival. J. Clausen, C. P. (1940) Entomophagous Insects. Hafner, Econ. Entomol. 61: 1088–1091. New York, 688 pp. Tomokuni, M., T. Yasunaga, M. Takai, I. Yamashita, M. Kawa- Greathead, D. J. (1986) Parasitoids in classical biological mura and T. Kawasawa (1993) A Field Guide to Japa- control. In Insect Parasitoids (J. K. Waage and D. J. nese Bugs—Terrestrial Heteropterans—. Zenkoku Greathead eds.). Academic Press, London, pp. 289– Noson Kyoiku Kyokai, Tokyo. 380 pp. (in Japanese). 318. Yamada, K. and M. Miyahara (1979) Studies on the ecology Grenier, S. (1988) Applied biological control with tachinid and control of some stink bugs infesting fruit. II. Gymno- flies (Diptera, Tachinidae): a review. Anz. soma rotundatum as a natural enemy to the brown- Schadlingskde., Pflanzenschutz, Umweltschutz 61: 49–56. winged green bug. Bull. Fukuoka Hort. Exp. St. 17: 54– Harris, V. E. and J. W. Todd (1982) Longevity and reproduc- 62 (in Japanese with English summary).