Appl. Entomol. Zool. 40 (4): 679–686 (2005) http://odokon.ac.affrc.go.jp/
Helicoverpa armigera as an alternative host of the larval parasitoid Microplitis croceipes (Hymenoptera: Braconidae)
Le Khac HOANG1 and Keiji TAKASU2,* 1 Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University; Fukuoka 812–8581, Japan 2 Faculty of Agriculture, Kyushu University; Fukuoka 812–8581, Japan (Received 26 April 2005; Accepted 4 August 2005)
Abstract Microplitis croceipes is a solitary larval parasitoid of Helicoverpa/Heliothis species in North America. Laboratory ex- periments were conducted to determine suitability of the non-natural host, a Japanese strain of Helicoverpa armigera for parasitism by M. croceipes. Females oviposited in the third instar of H. armigera. When the parasitized hosts were reared with artificial diet at 15–30°C with 16L:8D, 67–92% of them produced parasitoid pupae. However, only 9% at 13°C and 53% at 33°C produced parasitoid pupae, and none of those parasitoid pupae developed to adults at these temperatures. Mean time taken from oviposition to adult emergence varied from 14.8 d at 30°C to 53.2 d at 15°C for males and from 15.5 d at 30°C to 60.7 d at 15°C for females. The proportions of females in the emerged adults were 0.45–0.56. Mean lengths of forewings varied from 4.4 mm at 30°C to 4.9 mm at 15°C for males and from 4.3 mm at 30°C to 4.7 mm at 15°C for females. H. armigera was as suitable for parasitism by M. croceipes as H. zea and H. virescens, natural hosts of this parasitoid. The optimal temperature range for development of M. croceipes was 20–28°C.
Key words: Microplitis croceipes; Helicoverpa armigera; parasitism; host suitability; temperature
parasitoid is capable of parasitizing the non-natural INTRODUCTION host Helicoverpa armigera that is a serious pest of Koinobiont endoparasitoids should be relatively horticultural and ornamental crops worldwide in- specialized to one or a few closely related hosts be- cluding Japan and other Asian countries (Blumberg cause of an intimate biochemical and physiological et al., 1997; Herman and Davidson, 2000). Al- connection with their hosts (Godfray, 1994; though H. armigera was used for experiments as an Quicke, 1997). One of such parasitoids is Micropli- alternative host of M. croceipes (Blumberg et al., tis croceipes (Cresson). Microplitis croceipes is a 1997), suitability of this alternative host for para- solitary endoparasitoid of Helicoverpa/Heliothis sitism by M. croceipes has not been qualitatively species, including Helicoverpa zea (Boddie), H. evaluated. subflexa (Guene), and Heliothis virescens (F.). All In addition to a biological control agent of Heli- of these hosts feed on a wide range of crops such coverpa/Heliothis spp., M. croceipes is an impor- as cotton, soybean and corn in United State and tant insect for laboratory research. Host selection Canada (Lewis and Brazzel, 1968; King et al., behavior of this species has been intensively stud- 1985; Fitt, 1989). ied (Lewis and Martin, 1990). The behavioral This parasitoid is considered to be an effective mechanisms by which this parasitoid forages for biological control agent of these pests in North hosts or food were partially elucidated (Jones et al., America and possibly against other Helicoverpa/ 1971; Drost et al., 1988). A number of studies Heliothis species (Lewis and Burton, 1970; King demonstrated significance of learning on host and and Coleman, 1989; Knipling and Stadelbacher, food foraging (Lewis and Tumlinson, 1988; Lewis 1983). Previous studies have indicated that this and Takasu, 1990; Takasu and Lewis, 2003). Fur-
*To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2005.679
679 680 L. K. HOANG and K. TAKASU ther, recent studies have shown the possibility of Table1. Composition of artificial diet for H. armigera use of its learning ability for odor detection (Olson et al., 2003). Due to the information together with Ingredient Amount well-known biology and already developed mass RC4a 75.0 g rearing methods, M. croceipes has been often used Wheat germb 75.0 g for studies on foraging and learning (Lewis and Dried yeastc 15.0 g Martin, 1990; Quicke, 1997). Ascorbic acid 4.0 g We have started studying life history and learn- Methyl p-hydroxybenzoate 2.0 g Sorbic acid 2.0 g ing behavior of M. croceipes at the laboratory of Agar 9.0 g Bioresource and Management, Kyushu University, Propionic acid 1.5 ml Japan. To maintain a laboratory colony of M. cro- Distilled water 500.0 ml ceipes in Japan, we needed to use an insect native a to Japan as the alternative host because its natural Pellet food for rabbits and marmots, Oriental Yeast Co. hosts do not exist in Japan. Thus, we conducted Ltd., Tokyo, Japan. b HY-GY B, Nisshin Seifun Co., Tokyo, Japan. laboratory experiments to determine suitability of a c Dried yeast Ebios, Asahi Food & Health Co. Ltd., Tokyo, Japanese strain of H. armigera for parasitism by M. Japan. croceipes. In the present study, we first observed whether M. croceipes normally oviposited in H. emergence, adults were placed in a plastic con- armigera larvae. Then, we examined suitability of tainer (30 cm 30 cm 30 cm) with 30% honey so- the hosts for parasitism by M. croceipes at different lution for 2 to 4 d and then the females were used rearing temperatures, including developmental for experiments or rearing. time and survival of immature stages, and size and Oviposition behavior. Individual M. croceipes sex ratio of adults emerged from the hosts. females were first allowed to antennate frass of H. armigera larvae for 10 s to stimulate their oviposi- tion behavior. Thereafter, an unparasitized H. MATERIALS AND METHODS armigera larva was placed on a Petri dish (9 cm in Insects. Helicoverpa armigera were obtained diameter), and then a M. croceipes female being from a stock culture maintained at the laboratory held in a glass vial (in diameter and in length) was of Bioresource and Management, Kyushu Univer- allowed to walk from the vial onto the Petri dish sity. The laboratory colony was originated from a and to attack the host larva. After an oviposition in colony of Sankei Chemical Co. Ltd., Kagoshima a host, M. croceipes females often needed resting city, Japan. Adults were kept with water in a plastic or preening for a few minutes before the next cage (20 cm 40 cm 20 cm). As oviposition sub- oviposition. Therefore, after an oviposition, the fe- strates, pieces of cotton were suspended in the male was again held in a vial for at least 5 min be- cage. The pieces of cotton with eggs were collected fore being exposed to the next host. A female was every day and placed with artificial diet (a modi- used to parasitize 3–5 hosts each day. fied Hattori and Atsusawa,1980, Table 1) in a plas- The presence of parasitoid eggs in stung tic container (20 cm 40 cm 5 cm) until the larvae hosts. Immediately after hosts were stung by M. became third-instar. Then, the third-instars were in- croceipes females in the manner as described dividually reared with the artificial diet in a Petri above, some of the hosts were dissected and exam- dish (5.5 cm in diameter) until pupation to prevent ined whether or not they contained a parasitoid cannibalism. The artificial diet was renewed every egg. A total of 20 stung hosts were examined. two days. The pupae were kept in a Petri dish (9 cm Effects of temperature on parasitism. To de- in diameter) until adult emergence. The third in- termine effects of temperature on parasitism by M. stars were used for the following experiments. croceipes, the stung hosts were individually kept in Microplitis croceipes cocoons were shipped a plastic Petri dish (5.5 cm in diameter) with artifi- from Crop Protection and Management Research cial diet at the different temperatures, 13, 15, 20, Unit, USDA, Tifton, GA, USA. The parasitoid co- 23, 25, 28, 30 and 33°C with 16L:8D. The diet was coons were held in a Petri dish (9 cm in diameter) renewed every two days. After parasitoid larvae at 25°C under a 16L:8D photoperiod. Soon after emerged from parasitized hosts and span cocoons, Parasitism of H. armigera by M. croceipes 681 the cocoons were collected and individually placed Behavior of parasitized host and immature par- in a plastic Petri dish (5.5 cm in diameter) until the asitoid adults emerged. Emergence of the parasitoid adults When reared with artificial diet, parasitized H. was checked every day. Developmental time from armigera larvae bored a block of the diet and oviposition to pupation and from pupation to adult formed a chamber with the diet and their own emergence, and percentages of hosts producing frass, as do the unparasitized larvae for their pupa- parasitoid cocoons and adults were recorded. After tion chamber. A parasitoid larva left each host hid- adult emergence, sex and forewing length of the ing in the pupation chamber and then span a silk emerged adults were examined under binocular mi- cocoon for pupation beside the host in the cham- croscope. For each temperature, 100 parasitized ber; 9–10 d after oviposition at 25°C. All the para- hosts were examined. sitized hosts were alive when parasitoid larvae left. Effect of temperature on percentages of the hosts The parasitized hosts continued to stay near the co- that were dead or pupated, and percentage of para- coons and lived even after the parasitoid adults sitoid survival were analyzed by one-way ANOVA emerged from the cocoons; 18–22 d after oviposi- after arc-sine transformation. Tukey-Kramer HSD tion at 25°C. They did not show any aggressive be- test was used to compare the percentages among havior toward the larvae, cocoons or emerging different temperatures. Sex ratio of emerged adults adults of M. croceipes. was analyzed by the chi-square test. Tukey HSD test was conducted to compare forewing lengths of Immature survival emerged adults and developmental times for both Survival of parasitized hosts and parasitoids was sexes at different temperatures after two-way significantly affected by temperature (one-way ANOVA. ANOVA, for percentage of hosts dead, F7,32 15.2, p 0.0001; for percentage survival from oviposi- tion to parasitoid pupation, F 2,148.0, RESULTS 7,32 p 0.0001; for percentage survival from oviposi- Frass contact and oviposition tion to parasitoid adult emergence, F7,32 70.0, When M. croceipes females contacted frass of p 0.0001, Table 2). In the range of 20 to 30°C, H. armigera larvae that had fed on artificial diet, 77–92% of parasitized hosts produced parasitoid they intensively antennated it, as do they frass of pupae, and 57–79% produced parasitoid adults. natural hosts such as H. zea and H. virescens. Percentages of the hosts producing parasitoid When M. croceipes females that had contacted host pupae and adults at 13–15°C and 33°C, however, frass were given H. armigera larvae, they soon at- were significantly lower than 20–30°C (Tukey- tacked the larvae. All of the 20 hosts stung by M. Kramer HSD test, p 0.05, Table 2). At 13°C, 87% croceipes each contained one parasitoid egg. of parasitized hosts neither died without molting
Table2.Effects of rearing temperature on survival of M. croceipes parasitizing H. armigera
% parasitoid survivala Temperature No. insects % % (°C) examined hosts deada hosts pupateda Oviposition to Oviposition to pupation adult emergence
13 100 87.0 a 4.0 a 9.0 c 0 c 15 100 28.0 bc 5.0 a 67.0 ab 31.0 b 20 100 3.0 c 5.0 a 92.0 a 71.0 a 23 100 4.0 c 8.0 a 88.0 a 69.0 a 25 100 7.0 c 7.0 a 86.0 a 72.0 a 28 100 4.0 c 4.0 a 92.0 a 79.0 a 30 100 12.0 bc 11.0 a 77.0 ab 57.0 a 33 100 38.0 b 9.0 a 53.0 b 0 c
a The values with different letters in the same columns were significantly different by Tukey-Kramer HSD test (p 0.05). 682 L. K. HOANG and K. TAKASU
nor produced parasitoid pupae. At 33°C, although F5,367 18.5, p 0.0001). For both sexes, mean over 50% of the hosts produced parasitoid pupae, times from oviposition to pupation and from pupa- none of them emerged as adults from the cocoons. tion to adult emergence increased with decreasing Of the hosts stung by M. croceipes, 4–11% did temperature. Female progeny took longer time not show any indication of parasitism and devel- from oviposition to pupation at 15°C and from pu- oped to moth pupae (one-way ANOVA, F7,32 1.6, pation to adult emergence at 15 and 20°C than p 0.17; Table 2). male progeny at the same temperatures (Tukey HSD test, p 0.05, Tables 3 and 4). Developmental time As a result, total time taken for oviposition to Mean times taken from oviposition to pupation adult emergence was significantly affected by tem- and from pupation to adult emergence were af- perature, sex and the interaction between them fected by temperature and sex (two-way ANOVA, (two-way ANOVA, temperature, F5,367 2,924.2, for time from oviposition to pupation, temperature, p 0.0001; sex, F1,367 87.2, p 0.0001, interaction F5,367 1,406.4, p 0.0001, sex, F1,367 19.9, p between temperature and sex, F5,367 21.1, 0.0001; for time from pupation to adult emergence, p 0.0001, Tables 3 and 4). The mean developmen- temperature, F5,367 1,890.6, p 0.0001, sex, tal times ranged from 15 d at 30°C to 60 d at 15°C. F1,367 117.9, p 0.0001, Tables 3 and 4). For both At 15 and 20°C, mean developmental times for fe- mean time from oviposition to pupation and mean males were longer than for males. For both sexes, time from pupation to adult emergence, the interac- the mean developmental time increased with de- tions between temperature and sex were significant creasing temperature (Tukey HSD test, p 0.05, (for time from oviposition to pupation, F5,367 11.0, Tables 3 and 4). p 0.0001; time from pupation to adult emergence,
Table3.Effect of rearing temperature on developmental time (days) of M. croceipes males
Oviposition to pupationa Pupation to adult emergencea Totala Temperature (°C) N b Mean SEM N b Mean SEM N b Mean SEM
15 16 27.4 1.1 b 16 25.8 0.6 b 16 53.2 1.5 b 20 30 14.2 0.2 c 30 12.6 0.2 d 30 26.8 0.2 d 23 32 9.8 0.2 d 32 9.7 0.1 ef 32 19.5 0.2 ef 25 40 9.5 0.1 d 40 8.9 0.1 f 40 18.4 0.1 f 28 42 7.7 0.1 e 42 7.0 0.1 h 42 14.8 0.1 g 30 25 7.3 0.1 e 25 7.5 0.1 gh 25 14.8 0.2 g
a The values with different letters in the same columns were significantly different by Tukey HSD test (p 0.05). b The number of insects examined.
Table4.Effect of rearing temperature on developmental time (days) of M. croceipes females
Oviposition to pupationa Pupation to adult emergencea Totala Temperature (°C) N b Mean SEM N b Mean SEM N b Mean SEM
15 15 31.2 0.9 a 15 30.1 0.7 a 15 60.7 1.3 a 20 41 14.3 0.1 c 41 14.0 0.2 c 41 28.3 0.2 c 23 37 9.8 0.2 d 37 10.4 0.1 e 37 20.1 0.2 e 25 32 9.3 0.2 d 32 9.4 0.1 f 32 18.7 0.2 ef 28 37 7.8 0.1 e 37 7.4 0.1 gh 37 15.1 0.1 g 30 32 7.6 0.1 e 32 7.9 0.1 g 32 15.5 0.2 g
a The values with different letters in the same columns were significantly different by Tukey HSD test (p 0.05). b The number of insects examined. Parasitism of H. armigera by M. croceipes 683
Table5.Effect of rearing temperature on sex ratio and forewing lengths of emerged adults of M. croceipes adults
Forewing length (mm) Proportion of Temperature females in Male Female (°C) emerged a No. insects No. insects adults Mean SEMb Mean SEMb examined examined
15 0.45 16 4.85 0.07 a 15 4.71 0.04 a 20 0.56 30 4.65 0.06 b 41 4.46 0.04 b 23 0.54 32 4.64 0.06 bc 37 4.33 0.05 bc 25 0.45 40 4.66 0.04 bc 32 4.36 0.05 bc 28 0.47 42 4.50 0.06 c 37 4.27 0.05 c 30 0.54 25 4.43 0.07 c 32 4.26 0.07 c
a The proportions were not significantly different by the chi-square test (p 0.05). b The values with different letters were significantly different by Tukey HSD test (p 0.05).
Sex ratio and body size of emerged adults ceipes produced mature larvae. Bryan et al. (1969) The proportions of females in emerged adults at showed that percentage adult emergence of M. cro- different temperatures varied from 0.45 to 0.56, but ceipes from stung H. virescens was 78–91% at the difference was not significant (chi-square 25–30°C. While mean forewing lengths of M. cro- 4.06, df 5, p 0.541, Table 5). ceipes emerged from H. armigera were Mean forewing lengths ranged from 4.43 to 4.4–4.9 mm for males and 4.3–4.7 mm for females 4.85 mm for males and 4.26 to 4.71 mm for fe- in the present study, mean forewing length of M. males (Table 5). Temperature and sex have signifi- croceipes emerged from H. zea was 4.55 mm for cant effects on forewing lengths (temperature, males and 4.34 mm for females (Gupta et al., F5,367 9.9, p 0.0001; sex, F1,367 42.1, p 1996). 0.0001). The interaction between temperature and Here we discuss oviposition behavior, effects of sex was not significant (F5,367 0.63, p 0.67). temperature on parasitism, failure of parasitism in Forewing lengths of males were larger than those stung hosts, behavior of parasitized hosts, and opti- of females at the same temperatures. For both mal temperature for development of M. croceipes. sexes, forewing lengths decreased with increasing temperature (Tukey HSD test, p 0.05). Oviposition in H. armigera Microplitis croceipes females are stimulated to oviposit in hosts by chemicals derived from hosts DISCUSSION (Lewis and Martin, 1990). On contacting frass of The present study has shown that the Japanese the natural hosts H. zea or H. virescens, M. cro- H. armigera strain used for experiments is suitable ceipes females intensively antennated the frass. for parasitism by M. croceipes. Microplitis cro- But, they do not show such intensive antennation ceipes females easily oviposited in H. armigera lar- on frass of the non-host, Spodoptera exigua vae. The parasitoid eggs laid in hosts developed to (Hübner) (Takasu and Lewis, 2003). The chemical adults at 15–30°C. Sex ratio and size of M. cro- in the host frass, 13-methylhentriacontane is re- ceipes adults emerged from the hosts were compa- sponsible for this intensive antennal examination to rable to those emerged from the natural hosts, H. host frass (Jones et al., 1971; Lewis and Jones, zea and H. virescens (Bryan et al., 1969; Lewis, 1971). Hemolymph of host larvae also contains a 1970; Gupta et al., 1996). Of H. armigera para- kairomone that stimulates oviposition behavior of sitized by M. croceipes at 20–30°C, 77–92% pro- M. croceipes (Tilden and Ferkovich, 1988). Our duced parasitoid larvae, and 57–79% produced observation that M. croceipes females intensively parasitoid adults in the present study. Lewis (1970) antennated H. armigera frass and easily oviposited showed that 87–93% of H. zea stung by M. cro- in the larvae, suggests the possibility that H. 684 L. K. HOANG and K. TAKASU armigera frass also contains 13-methylhentriacon- developed to pupae without any symptom of para- tane and its hemolymph does the ovipositional sitism. Although M. croceipes eggs and larvae are stimulus of M. croceipes. encapsulated by atypical hosts including Spodoptera frugiperda (J. E. Smith), S. exigua Effects of temperature on parasitism (Hübner), Trichoplusia ni (Hübner), Galleria mel- While more than 67% of parasitized hosts pro- lonella (L.), Plodia interpunctella (Hübner), and duced parasitoid pupae at 15–30°C, only 9% of Plutella xylostella (L.), encapsulation of M. cro- parasitized hosts produced parasitoid pupae at ceipes eggs or larvae by larvae of Heliothis/Heli- 13°C. At the lower temperature, most of para- coverpa species has not been observed (Lewis, sitized hosts died without producing a parasitoid 1970; Vinson and Lewis, 1973; Blumberg and Fer- larva. Unparasitized H. armigera larvae also die kovich, 1994). In the relative species M. rufiventris, before pupation at 13°C (Takasu and Hoang, un- which is a larval parasitoid of Spodoptera littoralis published data). The lower parasitoid survival up to (Boisd.), some of the hosts stung by this parasitoid pupation at 13°C may be due to failure of develop- developed to adults and appeared to be non-para- ment of not the parasitoid but the host larvae in sitized. In such hosts, parasitoid eggs or young lar- such a low temperature. vae were found dead for encapsulation or unknown Percentage survival up to pupation for M. cro- reasons. ceipes was also significantly lower at 33°C than at 15–30°C. The failure of development up to pupa- Behavior of parasitized hosts tion cannot be explained by the failure of host Caterpillars parasitized by parasitoids often ex- larval development because unparasitized H. hibit different behavior from unparasitized ones. It armigera larvae normally developed to adults at is suspected that parasitoids manipulate their host’s 33°C (Hoang and Takasu, unpublished). More than physiology and behavior to increase their progeny 30°C may be beyond the optimal temperature for survival (Godfray, 1994). In Apanteles kariyai development of M. croceipes immature themselves. Watanabe, a larval parasitoid of common army- Another significant effect of temperature was the worm, for example, it is speculated that the wasp failure of emergence of M. croceipes pupae at causes the host to move to a favorable position for 15°C. Less than 50% of parasitoid pupae emerged pupation, and prevents the host from dying the at 15°C while more than 80% of the pupae vicinity of the pupae where it might rot or attract emerged at 20–30°C. Bryan et al. (1969) also predators or hyperparasitoids (Sato et al., 1983). In found that M. croceipes never emerged from co- the present study, we did not find any particular be- coons at 15°C. However, they indicated that M. havior of parasitized hosts containing immature M. croceipes reared at 15°C diapaused as prepupae in croceipes. However, behavior of parasitized hosts their cocoons. Since we did not examine the para- after parasitoid larvae left may affect survival of sitoid cocoons reared at 15°C, we do not know parasitoid cocoon and adult emergence. The perfo- whether some of the pupae at 15°C were diapaus- rated caterpillars provided with artificial diet sur- ing or dead in the present study. vived for a few days after the parasitoid larvae emerged from them and stayed next to the para- Failure of parasitism in stung hosts sitoid cocoons in the larval chamber. The host lar- About 4–11% of the hosts stung by M. croceipes vae never showed any aggressive behavior against females pupated without producing a parasitoid. the parasitoid cocoons. When the parasitized larvae The stung host larvae pupated without any symp- from which parasitoid larvae already left were agi- tom of parasitism, and eventually emerged as adult tated with forceps, they became aggressive and at- moths (Hoang and Takasu, unpublished). Since all tempted to bite the forceps (Takasu, unpublished the hosts stung by M. croceipes contained the para- data). If the perforated host larvae become aggres- sitoid egg in the present study, it was likely that sive toward approaching hyperparasitoids or preda- parasitoid eggs were laid in H. armigera larvae, but tors, it might reduce the mortality of parasitoid lar- the parasitoid eggs or the hatched larvae failed to vae or pupae caused by those natural enemies. develop in the hosts. We cannot determine the rea- son why the hosts stung by parasitoids normally Parasitism of H. armigera by M. croceipes 685
Optimal temperature for development of M. cro- armyworm, Mamestra brassicae Linné and the common ceipes armyworm, Mythimna separata Walker (Lepidoptera: Optimal temperature for development of para- Noctuidae) on a simple artificial diet. Jpn. J. Appl. En- tomol. Zool. 24: 36–38 (in Japanese with English sum- sitoids can be evaluated by the factors including mary). parasitoid survival, developmental rate, and sex Herman, T. J. B. and M. M. Davidson (2000) Introduction ratio and size of emerged adults. In the present and establishment of Microplitis croceipes, a larval para- study, sex ratio of emerged M. croceipes adults was sitoid of Heliothis, in North Island pine forests. New not affected by temperature. However, as tempera- Zealand Plant Prot. 53: 328–333. ture increased, development rate of M. croceipes Jones, R. L., W. J. Lewis, M. C. Bowman, M. Beroza and B. A. Bierl (1971) Host-seeking stimulant for parasite of corn was faster while size of emerged adults was earworm: Isolation, identification, and synthesis. Sci- smaller. The faster development at higher tempera- ence 173: 842–843. tures seems to be balanced or compensated for by King, E. G. and R. J. Coleman (1989) Potential for biologi- the smaller size of emerged adults. Percentage sur- cal control of Heliothis species. Annu. Rev. Entomol. vival of this parasitoid from oviposition to adult 34: 53–75. King, E. G., J. E. Powell and R. J. Coleman (1985) A high emergence was highest at the range from 20 to incidence of parasitism of Heliothis spp. (Lepidoptera: 28°C. Based on these results, the range of 20 to Noctuidae) larvae in cotton in southeastern Arkansas. 28°C is optimal for development of M. croceipes in Entomophaga 30: 419–426. H. armigera in the laboratory. Knipling, E. F. and E. A. 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