Host Status of Wheat and Corn for suppressalis (: ) Author(s): Maolin Hou, Lixia Hao, Yongqiang Han, and Xiaolan Liao Source: Environmental Entomology, 39(6):1929-1935. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/EN10081 URL: http://www.bioone.org/doi/full/10.1603/EN10081

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. BEHAVIOR Host Status of Wheat and Corn for Chilo suppressalis (Lepidoptera: Crambidae)

1,2 1,3 1 3 MAOLIN HOU, LIXIA HAO, YONGQIANG HAN, AND XIAOLAN LIAO

Environ. Entomol. 39(6): 1929Ð1935 (2010); DOI: 10.1603/EN10081 ABSTRACT Host plant speciÞcity depends on recognition of the host and the ability to discriminate it from nonhost plants. Chilo suppressalis (Walker) (Lepidoptera: Crambidae), an important pest of , is considered to be polyphagous, although few papers have ever reported infestation of C. suppressalis on most of the recorded hosts. The present investigation was designed to test whether two important gramineous crops, wheat and corn, are host plants of C. suppressalis based on the host-plant Þnding process in cage and Y-tube olfactometer tests, oviposition and egg hatching, and larval feeding and survival. In the cage tests, gravid C. suppressalis females did not differentiate rice plants from wheat or corn plants when only visual cues were involved, but were more attracted to rice plants when only olfactory cues or both vision and olfaction were present. The Y-tube olfactometer tests further conÞrmed that the females did not prefer wheat or corn plants, and revealed that they responded equally to clean air and odors from wheat or corn plants. Under no-choice and choice condition alike, the females laid eggs on a lower proportion of wheat and corn plants and egg number and hatching rate were signiÞcantly reduced on wheat and/or corn plants than on rice plants. Larval feeding was not observed in wheat and lower in corn than in rice plants, and no pupae or surviving larvae were collected from wheat and corn plants. The results suggest that wheat and corn are not host plants of C. suppressalis. These Þndings are discussed in context of host-Þnding process in C. suppressalis and management of resistance to transgenic Bt rice.

KEY WORDS Asiatic rice borer, host range, host orientation, olfaction, Lepidoptera

Host range of insect pests is of importance in planning life cycle. Thus, to be a host plant of an insect, the crop production and designing integrated pest man- insect should be able to oviposit in the plant under agement tactics. Phytophagous insect species are Þeld conditions, and the plant should sustain subse- mostly associated with a single or a few host plant quent development of these eggs into larvae, pupae, species (Chapman 1988, Mitter and Farrel 1991). Host and adults (Cowley et al. 1992). speciÞcity involves adaptation of an insect to the food The Asiatic rice borer, Chilo suppressalis (Walker) source, and is mainly dependent on the recognition of (Lepidoptera: Crambidae), is the most abundant stem the host plant and the ability to discriminate it from borer of rice Oryza sativa L. in temperate Asia and also nonhost plants (Van Loon 1996, Hora and Roessingh occurs throughout the tropical rice-growing areas of 1999). Among phytophagous Lepidoptera, correct Asia (Pathak and Khan 1994). The rice borer has one choice of host plants by adult females is critical be- to Þve generations throughout the temperate Asia, and cause the newly hatched larvae are relatively immo- overwinters as mature larva in rice stubble. Newly bile and are not likely to locate an acceptable food hatched larvae feed on the epidermis in the inner side source in the case of oviposition on nonhost plants of leaf sheaths and bore into rice stalks as Þrst instars. (Renwick and Chew 1994). However, because of the Rice plants damaged by the borer show symptoms of different feeding habits between adults and larvae, the dead leaf sheath at tillering stage, dead heart at boot- adult female is unable to assess the nutritional quality ing stage, and white head at heading stage. C. suppres- directly and has to rely heavily on her sensory mo- salis is considered to be polyphagous; 41 species of dalities (visual or olfactory) to recognize host plants. plants in six families, primarily wild and cultivated Although some scientists deÞne host plants as plants Poaceae, were recorded to be its host plants (Khan et used as a food resource (Bernays and Chapman 1994), al. 1991), including corn, wheat, sugarcane, , we use the term to indicate a plant species that can and millet. However, Cuong and Cohen (2002) found support the development of an insect throughout its only one review paper (Neupane 1990) reporting C. suppressalis as a pest of any of these cultivated crops. 1 State Key Laboratory for Biology of Plant Diseases and Insect The present investigation was designed to test Pests, Institute of Plant Protection, Chinese Academy of Agricultural whether two important gramineous crops, wheat and Sciences, Beijing 100193, . 2 Corresponding author, e-mail: [email protected]. corn, are host plants of C. suppressalis based on: (1) 3 Hunan Agricultural University, Changsha 410128, China. plant preference of adult females using olfactory and

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Table 1. Plants tested in the cage experiments

Plant ScientiÞc name Family Variety Leaf shape Rice Oryza sativa L. Gramineae Shanyou 63 Blade Corn Zea mays L. Gramineae Jiyuan 1 Blade Wheat Triticum aestivum L. Gramineae Zhongzhi 1 Blade Ryegrass Lolium multiflorum Lam. Gramineae Zhuoyue Blade Leek Allium tuberosum Rottler ex Sprengle Liliaceae Xinludiwang Blade Cucumber Cucumis sativus L. Cucurbitaceae Zhongnong 8 Ovate Cotton Gossypium herbaceum L. Malvaceae Cheng 14 Ovate visual cues in cage and Y-tube olfactometer tests, (2) seven plant species was arranged symmetrically in a oviposition and egg hatching, and (3) larval feeding circle (diameter 85 cm) in a cylindrical cage (diam- and survival. eter 100 cm, height 80 cm) made from iron wire and nylon mesh. The plants were Ϸ38 cm apart from each neighboring plant. All plants were covered with fully Materials and Methods transparent plastic bags that were sealed at the open- . Overwintering larvae of C. suppressalis ing to prevent any volatile compounds escaping. Ten were collected from water-oat, females held for 10 min in a plastic cup were released (Turcz), plants and reared in the insectary with an at the center of the cylindrical cage. The insects left artiÞcial diet developed by us at 28 Ϯ 2ЊC and L14:D10. the cup within 5 min in all observations. Numbers of The main components of the artiÞcial diet include individuals found on each plant was recorded 30 min soybean powder, yeast, sugar, fresh water-oat, agar, after all the climbed out of the cup. The tests vitamin, and water. Before being used in the experi- were performed after 19:00 (moths become most ac- ments, the insects were reared for more than Þve tive around dusk with activity slowly waning through- generations. After pupation, insects were separated out the night) and repeated six times. Between rep- according to sex and placed separately according to etitions, the plants were rotated to balance any effects pupating date and sex. After the day of emergence, from unforeseen asymmetries. The tests were per- females (Ͼ10) were paired with males in a mating formed at ambient temperature (22Ð26ЊC) and rela- cage for 24 h and supplied with 10% honey solution. tive humidity (50Ð75%) in laboratory illuminated with When used in the experiments, the females were 2Ð3 d two ßuorescent lamps at the ceiling. old. Experiment 2. Olfactory Cues (Olfactory Test). Cage Tests for Adult Female’s Preference. As shown This experiment was identical to the Þrst, except that in Table 1, seven plant species were used in the cage the plants were covered with bags made from plant tests. Rice, wheat, and corn are recorded to be host cultivation fabric that was opaque and nonairproof, plants, other plant species are nonhost plants (Khan et thus preventing visual perception from outside and al. 1991). The four gramineous plants species (i.e., rice, allowing plant odors to pass through easily. wheat, corn, and ryegrass) are of the same plant ar- Experiment 3. Visual and Olfactory Cues (Vision- chitecture and leaf shape; one liliaceous species, that and Olfaction-Based Test). This experiment was also is, leek, is not recorded to be host plant of C. suppres- identical to the Þrst, except that the plants were not salis but has the same general leaf shape as the gra- covered with any kind of bag. mineous plants; and cucumber and cotton that are of Y-tube Olfactometer Tests for Adult Female’s Pref- different leaf shape and are known to be nonhost erence. The above experiments showed that C. sup- plants of C. suppressalis. We selected these plants so as pressalis females relied on olfactory cues in host-plant to determine how C. suppressalis females recognize Þnding and that the females did not prefer wheat and host plants, by visual cues, that is, through plantsÕ color corn; a Y-tube olfactometer test was designed to fur- and silhouette, or by olfactory cues. ther determine preference of C. suppressalis females Rice seedlings were transplanted to plastic pots (20 for odors of wheat and corn, two putative host-plants. cm in height and 15 cm in diameter). Other plants Observations were conducted at 26 Ϯ 2ЊC and 50 Ϯ 5% were seeded to plastic pots. All plants were cultured RH under low red light during the Þrst4hofthe in a greenhouse at 27 Ϯ 4ЊC, 80% Ϯ 5% RH and 16L:8D. scotophase. Responses of female C. suppressalis to Cucumber plants were erected by circling the plant different odors were investigated using a glass Y-tube stems around a stake. When the plants were used in olfactometer. The olfactometer consisted of glass tub- the experiments, they were in vegetative growth stage ing of 1.5 cm in internal diameter. The Þrst part, into and 30Ð40 cm high, each with 4Ð6 leaves. which insects were released to walk upwind, was Three cage experiments were performed in the lab- 10-cm long and then divided into two, 10-cm long arms oratory to determine whether C. suppressalis females that were angled at 75Њ to each other. An electric pump are attracted to plants by visual cues or plant odors and pushed air into each arm of the olfactometer, and ßow their orientation preference for the tested plants. meters were used to equalize the two ßow rates at 300 Experiment 1. Visual Cues (Visual Test). The pot- ml/min. Before entering the olfactometer arms, each ted plants were thinned to a single plant before being airstream passed through a glass vial containing acti- used in the observation. A potted plant of each of the vated charcoal and a glass vial containing distilled December 2010 HOU ET AL.: HOST STATUS OF WHEAT AND CORN FOR C. suppressalis 1931 water so as to clean and moisturize the air, and then through a blank glass jar (15.0 cm in diameter and 40.0 cm in height) or a jar containing different plants. The olfactometer was placed horizontally on a table and glass jars with odor sources were placed under the table. One adult was released downwind of the odor sources at the base of the olfactometer, and was ob- served continuously for 5 min as it moved inside the Y-tube. Insects that passed 3 cm into either arm and stayed there for Ͼ1 min or reached the arm open within the Þrst 5 min were judged to have made a Þnal choice, otherwise they were discarded. Fig. 1. Percentages of C. suppressalis females landing on plants in a cage 30 min after release when the plants were The choices offered to female C. suppressalis were: each covered with transparent airproof plastic bags (e.g., (1) wheat versus blank; (2) corn versus blank; (3) rice response to visual cues), or when the plants were each versus blank; (4) wheat versus rice; and (5) corn covered with opaque air-ventilating plant cultivation fabric versus rice. Observations were repeated four times (e.g., response to olfactory cues), or when the plants were and eight females were observed for each test. Be- not covered (e.g., response to both visual and olfactory cues) tween alternative repetitions, position of odor sources (*, signiÞcant difference between percentages of females 2 was changed to eliminate possible positional bias in landing on plants, ␹ test, P Ͻ 0.05; ns, no signiÞcant differ- the set-up. ence). Oviposition and Egg Hatching. Oviposition by C. suppressalis females on rice, wheat, and corn plants were investigated under no-choice and choice condi- test. The data were analyzed using SPSS 13.0 for Win- tions. The plants and insects were maintained as dows. above, but the adult females were mated for 48 h. Under no-choice condition, two randomly selected Results gravid females were conÞned with a potted plant in a Cage Tests. When plant odors were masked in the cylindrical mesh cage (diameter 36 cm, height 48 cm) cage tests for visual response, C. suppressalis females for 48 h. After numbers of egg masses and eggs were did not land on wheat and cucumber plants, and ori- checked for each plant, the eggs were left to hatch. ented equally to the other Þve plant species (i.e., rice, Three days later, number of unhatched eggs was corn, ryegrass, leek, and cotton) (␹2 ϭ 1.43; df ϭ 4; P ϭ counted. The experiments were conducted in a green- 0.840; Fig. 1). In the cage tests for olfactory cues, the house at 27 Ϯ 4ЊC, 80% Ϯ 5% RH and 16L:8D. Under females did not respond to leek, cucumber, and cotton choice condition, the set-up was largely the same as plants; higher proportion of C. suppressalis females that under no-choice condition, but Þve gravid fe- was found on rice plants than on the other three plant males were conÞned with one potted plant of rice, species (i.e., corn, wheat, and ryegrass) (␹2 ϭ 54.53; wheat, and corn that were arranged symmetrically in df ϭ 3; P Ͻ 0.001; Fig. 1). And in the cage tests with a cylindrical mesh cage (diameter 80 cm, height 48 both visual and olfactory cues present, the insects did cm). Between repetitions, the plants were rotated to not orient to leek and cucumber plants; more insects balance any effects from unforeseen asymmetries. Ob- landed on rice plants than on the other four plants servations were repeated for 10 and eight times for the (␹2 ϭ 81.10; df ϭ 3; P Ͻ 0.001; Fig. 1). The proportion no-choice and the choice tests, respectively. of C. suppressalis females landing on rice plants in- Larval Feeding and Survival. A blackened egg mass creased signiÞcantly in the olfactory test and in the (with 10 eggs) was clipped to a leaf auricle of rice, vision- and olfaction-based test than in the visual test wheat, or corn plant each in a mesh cage in a green- (␹2 ϭ 12.49; df ϭ 1; P Ͻ 0.001 and ␹2 ϭ 16.41; df ϭ 1; house at 23 Ϯ 5ЊC, 68% Ϯ 5% RH and 16L:8D. Twelve P Ͻ 0.001, respectively), but did not change between plants were used for each plant species. Hatched lar- the olfactory test and the vision- and olfaction-based vae were allowed to feed ad lib. Thirty days after test (␹2 ϭ 0.30; df ϭ 1; P ϭ 0.584). In the three cage inoculation, the plants were checked for boring dam- tests, there were insects not landing on plants (non- age; and after another 15 d, all plants were dissected responsive) (Fig. 2). There were more nonresponsive to check for pupae and surviving larvae. insects in the visual cage test than in the olfactory cage Data Analysis. In the cage tests, numbers of moths test (␹2 ϭ 3.90; df ϭ 1; P ϭ 0.048) and than in the cage from all replicates were pooled for each plant species test with both vision and olfaction present (␹2 ϭ 4.32; before statistical analysis. A ␹2 test was applied to df ϭ 1; P ϭ 0.038). The cage tests indicated that detect the signiÞcance of visual and olfactory cues in olfactory cues dominated host-plant Þnding behavior host-plant Þnding in the cage tests and to determine in C. suppressalis females; also, the females showed no signiÞcant differences between the numbers of insects preference for wheat or corn plants. choosing either odor source in Y-tube olfactometer Y-Tube Olfactometer Tests. The preference for tests. Numbers of egg masses and eggs were subjected rice, wheat, and corn plants were further determined to analysis of variance (ANOVA), and the means were using Y-tube olfactometer tests. When plant odor was separated by TukeyÕs Honest SigniÞcance Difference added to only one of the arms of the olfactometer, 1932 ENVIRONMENTAL ENTOMOLOGY Vol. 39, no. 6

26.51; df ϭ 1; P Ͻ 0.001; Table 2). Under choice con- dition, all rice plants (100%) were deposited with eggs, while only 50% of each of wheat or corn plants re- ceived eggs (␹2 ϭ 16.67; df ϭ 1; P Ͻ 0.001). As in the no-choice test, there were no difference in numbers of egg masses on the three plant species (F ϭ 1.97; df ϭ 15; P ϭ 0.179), but 86.8 and 74.4% more eggs per plant were found on rice than on wheat and corn, respec- tively; difference in egg numbers between rice and wheat was signiÞcant (TukeyÕs HSD test, P ϭ 0.024). Again, egg hatching rates were higher on rice than Fig. 2. Percentages of C. suppressalis females not landing on wheat (␹2 ϭ 17.67; df ϭ 1; P Ͻ 0.001) or on corn on plants (nonresponsive) in a cage 30 min after release (␹2 ϭ 24.71; df ϭ 1; P Ͻ 0.001; Table 2). when only visual cues, only olfactory cues, or both were Larval Feeding and Survival. Thirty days after in- involved. oculation of blackened eggs, all the twelve rice plants were damaged by larval boring, while only two corn more C. suppressalis females were found in the arm plants (16.7%) and no wheat plants were bored. When containing the odor of rice plants (␹2 ϭ 3.90; df ϭ 1; the plants were dissected to check for pupae and P ϭ 0.048), whereas there were no differences in the surviving larvae at the end of the observation, a total number of females choosing between corn odor and of 64 pupae or larvae were located in rice plants, and clean air (␹2 ϭ 0.03; df ϭ 1; P ϭ 0.853) or between no pupae or surviving larvae were found in either wheat odor and clean air (␹2 ϭ 0.33; df ϭ 1; P ϭ 0.564; wheat or corn plants. Fig. 3). When provided with plant odors in both arms, the females preferred rice odor over corn (␹2 ϭ 6.53; Discussion df ϭ 1; P ϭ 0.011) or wheat (␹2 ϭ 9.32; df ϭ 1; P ϭ 0.002) odor (Fig. 3). The Y-tube olfactometer tests In host-Þnding by phytophagous insects, a com- further determined that C. suppressalis females monly accepted view is that plant odors may be the showed no preference for wheat or corn plants. most important cues guiding them to hosts and that the Oviposition and Egg Hatching. Under no-choice strength of odor-mediated attraction is positively cor- condition, more rice plants (90%) caged with two related with the degree of specialization of the her- gravid C. suppressalis females received eggs than bivorous insect (Visser 1986, Bernays and Chapman wheat plants (30%) or corn plants (60%) (␹2 Ͼ 3.90; 1994, Schoonhoven et al. 2005). However, vision may df ϭ 1; P Ͻ 0.014). On the plants with eggs, numbers be equally or even more important in some herbivo- of egg masses per plant were not different on the three rous insects (Finch and Collier 2000, Hirota and Kato plant species (F ϭ 3.51; df ϭ 17; P ϭ 0.056), but there 2001, Bre´vault and Quilici 2007, Stenberg and Ericson were 60.1 and 74.9% more eggs per plant on rice than 2007). Finch and Collier (2000) propose a general on wheat and corn, respectively; difference in egg theory to explain how insect pests locate their hosts. numbers between rice and corn was signiÞcant They argue that, once phytophagous insects have lo- (TukeyÕs honestly signiÞcant difference [HSD] test, cated a suitable habitat by use of plant volatile chem- P ϭ 0.004; Table 2). Egg hatching rates were different ical information, visual stimuli then govern the next on the three plant species, higher on rice than on phase of host-plant location and insects will land in- wheat (␹2 ϭ 5.28; df ϭ 1; P ϭ 0.022) or on corn (␹2 ϭ discriminately on any green object including nonhost plants. They describe this phase as Ôappropriate/inap- propriate landingsÕ. In the present visual test, apart from wheat and cucumber plants, C. suppressalis females landed equally on host and nonhost plants (Fig. 1). This indicates that the insects cannot discriminate host from nonhost plants by vision alone. However, the fact that they did not land on wheat and cucumber plants doesnÕt necessarily indicate that the females have made any discrimination in orientation: they might have only chosen a green object and then made no further ÔdecisionÕ. Further, the fact that C. suppressalis females landed equally on host plants (i.e., rice) and nonhost plants (e.g., cotton), which have different plant silhouettes, shows that the insects respond more Fig. 3. Percentages of C. suppressalis females choosing between either arms of Y-tube olfactometer connected to to green color than to plant silhouette. In the olfactory different combinations of odor sources. (n, the number of test, the females landed preferentially on rice than on responsive insects among a total of 32 insects; *, signiÞcant other plants (Fig. 1). When both vision and olfaction difference between arms, ␹2 test, P Ͻ 0.05; ns, no signiÞcant were involved, the females still landed preferentially difference). on rice than on other plants (Fig. 1). Rice and other December 2010 HOU ET AL.: HOST STATUS OF WHEAT AND CORN FOR C. suppressalis 1933

Table 2. Oviposition by C. suppressalis females and egg hatching on rice, wheat, and corn plants under no-choice and choice conditions

No-choice condition Choice condition Plants No. egg % eggs No. egg % eggs No. eggs No. eggs masses hatched masses hatch Rice 1.9 Ϯ 0.2 a 125.3 Ϯ 19.7 a 77.2 2.4 Ϯ 0.5 a 180.9 Ϯ 39.3 a 86.2 Wheat 1.3 Ϯ 0.3 a 50.0 Ϯ 15.7 ab 51.2 1.3 Ϯ 0.3 a 23.8 Ϯ 9.4 b 38.6 Corn 1.2 Ϯ 0.2 a 31.5 Ϯ 9.1 b 25.1 1.5 Ϯ 0.3 a 46.3 Ϯ 20.2 ab 31.9

The data (mean Ϯ SE) in each column followed by the same letter are not signiÞcantly different (TukeyÕs HSD test; P Ͼ 0.05). plants have similar color; so if visual cues were more and egg hatching was obviously hampered on these important at this step of the host-plant Þnding process, plants as compared with on rice plants, which indi- then it might be expected that the proportion of fe- cates that these two plant species are not as suitable for males landing on rice plants in the vision- and olfac- oviposition. After landing on a plant, insect females tion-based test would decrease compared with that in employ chemo- and mechano-receptors probably lo- the olfactory test. However, this does not occur. How- cated on the antennae or tarsi to detect plant olfactory ever, the proportion of females landing on rice plants and tactile cues and to ÔdecideÕ if the plant is suitable in the olfactory and the vision- and olfaction-based for oviposition and how many eggs to oviposit (Van tests increased signiÞcantly compared with that in the Loon 1996, Hora and Roessingh 1999, Ignacimuthu et visual test. In addition, there were more nonrespon- al. 2000, Calatayud et al. 2008). Differences in chem- sive insects in the visual test than in the other two tests ical proÞle and physical texture of the leaf surface (Fig. 2). Further, in the Y-tube olfactometer tests, the between rice and wheat/corn plants may contribute females responded positively to rice odors over clean to the lower rate of egg deposition and reduced egg air (Fig. 3). These results suggest that olfactory cues numbers and hatching rate on wheat and corn plants. play a more important role than visual cues in the Further, there was no larval feeding damage on host-plant Þnding process. Our results conÞrm earlier wheat plants and only two out of 12 corn plants were Þndings on the role of plant volatiles in host-plant bored, while all the tested rice plants were damaged Þnding in C. suppressalis (Chen 2002) and in other 30 d after deposition of blackened eggs. At the end of lepidopteran insects, C. partellus and Busseola fusca the observation, we collected no pupae or surviving (Birkett et al. 2006) and Cydia molesta (Pin˜ ro and larvae on wheat or corn plants. The differences in stem Dorn 2007), although the role of visual cues were not physical structure may explain the observed results. examined in these reports. Plutella xylostella, a lepi- Rice stem is wrapped by succulent leaf sheaths, the dopteran cruciferous specialist, also depends more on newly hatched larvae usually feed in the leaf sheaths olfaction than on vision in host-plant Þnding (Couty and then bore into the stem (Hao et al. 2008, Hou and et al. 2006). Therefore, our results do not conÞrm Han 2010); wheat and corn stems are more rigid and Finch and CollierÕs (2000) theory of host selection by the leaf sheaths are thin, which may prevent the newly insects, that is, Ôindiscriminate landing on any green hatched larvae from boring and result in high mortal- objectÕ, and instead demonstrate that C. suppressalis ity. Although there is no information on the nutrient relies on olfactory cues to discriminate host plants difference between rice and wheat/corn plants, we from nonhost plants. speculate that nutritional conditions of wheat/corn Our results demonstrate that C. suppressalis females stems are not adequate for larval development in C. showed no preference for wheat and corn, two re- suppressalis in that we did not observe any pupae or corded putative host plants of C. suppressalis, whether mature larvae despite of a small proportion of dam- in the olfactory or the vision- and olfaction-based cage aged corn stems. Rothschild (1971) found no Chilo tests (Fig. 1) or in the Y-tube olfactometer tests (Fig. larvae in large samples of grasses and sedges collected 3). It is known that both C. suppressalis adults and near rice Þelds infested with C. suppressalis in Malay- larvae are attracted to oryzanone (pÐmethyl aceto- sia. Cuong and Cohen (2002) demonstrated that C. phenone), a volatile chemical speciÞcally derived suppressalis larvae can barely survive on Þve weedy from rice plants (Munakata et al. 1959, Chen 2002). grasses, and that C. suppressalis generally does not use Given the fact that olfactory cues play a more impor- these plants in the Þeld. A literature analysis by Cuong tant role in the host-plant Þnding process in C. sup- and Cohen (2002) show that there are no quantitative pressalis females and that wheat and corn plants do not data reporting C. suppressalis as a pest of the cultivated possess the volatile chemical attractant, it is reason- corn, wheat, sugarcane, sorghum, and millet, although able that the females do not prefer wheat and corn they were recorded as hosts of C. suppressalis (Khan plants as compared with rice plants, even not over the et al. 1991). blank control. Therefore, we can expect that C. sup- Based on the present results regarding host-Þnding, pressalis females will not orient to wheat and corn oviposition and egg hatching, and larval feeding and plants in the Þeld. survival, it can be concluded that wheat and corn are C. suppressalis females oviposited on a lower pro- not host plants of C. suppressalis. Many of the nonrice portion of wheat and corn plants in both the no-choice host records for C. suppressalis by Khan et al. (1991) and the choice cage tests, and egg numbers were lower might be attributable to misidentiÞcation of other spe- 1934 ENVIRONMENTAL ENTOMOLOGY Vol. 39, no. 6 cies of Chilo, and to cases in which C. suppressalis Bre´vault, T., and S. Quilici. 2007. Visual response of the larvae have dispersed from rice plants of declining tomato fruit ßy, Neoceratitis cyanescens, to colored fruit quality to nearby plants of other species, as suggested models. Entomol. Exp. Appl. 125: 45Ð54. by Cuong and Cohen (2002). Another possibility is Calatayud, P.-A., P. O. Ahuya, A. Wanjoya, B. Le Ru¨ , J.-F. that C. suppressalis larvae may overwinter on these Silvain, and B. Fre´rot. 2008. Importance of plant phys- nonrice plant species near rice Þelds or planted after ical cues in host acceptance for oviposition by Busseola fusca. Entomol. Exp. Appl. 126: 233Ð243. rice harvest; in this case, C. suppressalis larvae may use Chapman, R. F. 1988. Odours and the feeding behavior of these nonrice plants only as overwintering sites. The insects. ISI Altas of Sci. Anim. Plant Sci. 1988: 208Ð212. only plant in addition to O. sativa that is clearly a host Chen, H. C. 2002. Roles of volatiles on the host selection of of C. suppressalis is Zizania latifolia (Griseb.) Turcz. ex Chilo suppressalis Walker, Cnaphalocrocis medinalis Stapf (Konno and Tanaka 1996), on which we re- Guenee and their parasitoids Cotesia chilonis Matsumura, corded severe C. suppressalis damage and collected Cotesia ruficrus Haliday. PhD thesis, Zhejiang University, overwintering larvae (Hou et al. 2009, Han et al. 2009). Hangzhou, China. Rice varieties genetically modiÞed with toxin genes Cohen, M. B., F. Gould, and J. S. Bentur. 2000. Bt rice: from Bacillus thuringiensis Berliner (Bacillaceae) (Bt) practical steps to sustainable use. Intern. Rice Res. Notes are under development in several countries, although 25: 4Ð10. have not yet been commercially released (Cohen et al. Couty, A., H. V. Emden, J. N. Perry, J. Hardie, J. A. Pickett, 2000, Ye et al. 2001). The Bt rice targets against stem and L. J. Wadhams. 2006. The roles of olfaction and vision in host-plant Þnding by the diamondback , borer and rice leaf roller, Cnaphalocrocis medialis Plutella xylostella. Physiol. Entomol. 31: 134Ð145. Guenee. Considering the imminent commercializa- Cowley, J. M., R. T. Baker, and D. S. Harte. 1992. DeÞnition tion of transgenic Bt rice, the problem of host range of and determination of host status for multivoltine fruit ßy C. suppressalis is especially signiÞcant in temperate (Diptera: Tephritidae) species. J. Econ. Entomol. 85: 312Ð Asia where C. suppressalis is the most abundant stem 317. borer. To delay insect resistance to Bt toxins in trans- Cuong, N. L., and M. B. Cohen. 2002. Field survey and genic crops, it is generally accepted to adopt plants greenhouse evaluation of non-rice host plants of the with high dose of toxin in combination with ÔrefugesÕ, striped stem borer, Chilo suppressalis (Lepidoptera: that is, non-Bt plants that serve to maintain Bt-sus- Pyralidae), as refuges for resistance management of rice ceptible target pests in the population (Gould 1998, transformed with Bacillus thuringiensis toxin genes. Bull. Cohen et al. 2000). Refuges may consist of non-Bt Entomol. Res. 92: 265Ð268. Finch, S., and R. H. Collier. 2000. Host-plant selection by cultivars of the same species as the Bt crop as well as, insects: a theory based on Ôappropriate/inappropriate for polyphagous pests, alternative host species. The landingsÕ by pest insects of cruciferous plants. Entomol. narrow host range of C. suppressalis as indicated by our Exp. Appl. 96: 91Ð102. current results and othersÕ (Cuong and Cohen 2002) Gould, F. 1998. Sustainability of transgenic insecticidal cul- suggests Þelds of non-Bt rice need to be maintained as tivars: integrating pest genetics and ecology. Annu. Rev. refuges to sustain sufÞcient Bt-susceptible individuals Entomol. 43: 701Ð726. in C. suppressalis populations. However, this may Han, Y. Q., L. X. Hao, and M. L. Hou. 2009. Comparison of prove to be difÞcult for small-holder, low-income bionomics of overwintering larvae of Chilo suppressalis farmers of most of the Asian rice-growing areas. collected for rice Þelds and water-oat Þelds in northern Therefore, strategies/policies have to be developed China. Chin. J. Eco-Agri. 17: 541Ð544. for Bt resistance management in C. suppressalis in rice Hao, L. X., Y. Q. Han, and M. L. Hou. 2009. Resistance of growing regions (Cohen et al. 2000). japonica rice varieties in Liaohe Valley to Chilo suppres- salis and its underlying mechanisms. Acta Ecol. Sinica 28: 5987Ð5993. Hirota, T., and Y. Kato. 2001. Inßuence of visual stimuli on Acknowledgments host location in the butterßy, Eurema hecabe. Entomol. Exp. Appl. 101: 199Ð206. We are grateful to the two anonymous reviewers and the Hora, K. H., and P. Roessingh. 1999. Oviposition in editors for suggestive comments. 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