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Journal of Chemical Ecology, Vol. 16, No. 7, 1990

INTERACTION BETWEEN VISUAL AND OLFACTORY STIMULI D U R I N G H O S T - F I N D I N G BY L E A F H O P P E R , Dalbulus maidis (HOMOPTERA: C I C A D E L L I D A E )

J.L. TODD, 1 P.L. PHELAN, and L.R. NAULT Department of Entomology Ohio Agricultural Research & Development Center The Ohio State University Wooster, Ohio 44691 (Received August 23, 1989, accepted December 4, 1989) Abstract--Virtually nothing is known about the role plant volatiles play in host-finding by Homoptera in the Suborder Auchenorrhyncha. In laboratory bioassays, we examined the influence of plant volatiles on orientation and postcontact behaviors of the leafhopper, Dalbulus maidis, and determined the relationship between visual and olfactory stimuli during host-finding. When compared to the number of contacts made with reflected green light in the presence of a hexane control, D. maidis made more contacts when exposed to volatile extracts from its preferred host, maize; a similar number of contacts when exposed to volatiles from a marginal host, gamagrass; and fewer contacts when exposed to volatiles from a nonhost, sorghum. There was no difference between males and females in the number of contacts made with green light when exposed to maize volatiles compared to hexane alone. More contacts were made with green light than with white light of similar intensity, both in the presence and in the absence of olfactory stimuli; however, maize volatiles acted as a synergist by increasing the number of contacts leafhoppers made with green light. After contacting the green light, exposure of maize volatiles significantly increased, relative to hexane, the amount of stationary time, but did not influence the amount of time spent moving, the distance traveled, or the speed while moving when within the boundaries of the green light. This study provides the first evidence for an interaction between visual and olfactory stimuli during host-finding for a leafhopper and also for olfactory mediation of postcontact behaviors not associated with feeding. Key Words--Leafhopper, Dalbulus maidis, Homoptera, Cicadellidae, hostfinding, maize, visual, olfactory, synergism, pest.

Present address: Department of Entomology, University of California, Riverside, California 92521. 2121 0098-0331/90/0700-2121506.00/0

9 1990 Plenum Publishing Corporation

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TODDETAL. INTRODUCTION

Current research suggests differences exist between the two suborders of Homoptera, the Sternorrhyncha and the Auchenorrhyncha, in the importance of volatile chemicals during intraspecific communication and host-finding, with the Sternorrhyncha (aphids, whiteflies, mealybugs, psyllids) being much more responsive to odors than the Auchenorrhyncha (leafhoppers, planthoppers, treehoppers, spittlebugs, cicadas). Olfactory perception of alarm pheromones (Nault and Phelan, 1984, and references therein) and sex pheromones (Card6 and Baker, 1984, and references therein; Eisenbach and Mittler, 1987) has been demonstrated for several Sternorrhyncha. Olfactory receptors responsive to plant volatiles have been identified from aphids (Bromley and Anderson, 1982; Yan and Visser, 1982), and several aphid species are known to alter their behavior when exposed to host and nonhost odors in the laboratory (Pettersson, 1970; Tamaki et al., 1970; Visser and Taanman, 1987) and in the field (Chapman et al., 1981). In contrast, intraspecific communication within the Auchenorrhyncha is mediated primarily by acoustic signals (Claridge, 1985; Heady et al., 1986), although some treehoppers respond to alarm pheromones (Nault et al., 1974). Only a few Auchenorrhyncha have been shown to possess host odor receptors (Klein et al., 1988) and to respond to plant volatiles during hostfinding (Saxena and Saxena, 1974; Khan et al., 1988). The Neotropical leafhopper genus Dalbulus is composed of 11 species that utilize maize, Zea mays L., and its wild relatives, the teosintes (Zea species) and the gamagrasses (Tripsacum species) as hosts (Nault, 1985). One species, Dalbulus maidis (DeLong & Wolcott), is a maize specialist and considered a serious pest in Latin America, primarily by transmitting maize-stunting pathogens (Nault, 1990). Virtually nothing is known about host-finding behaviors of Dalbulus leafhoppers. Todd et al. (1990a) examined the importance of color stimuli in host-finding by three Dalbulus species by comparing pre- and postcontact responses to maize seedlings with those to vertical models differing in hue (dominant wavelengths) or value (total amount of light reflected). Leafhoppers exhibited a strong orientation response to yellow and green models, and maintained contact with these colored models as long or longer than models painted other colors. However, the models provided only color and perhaps structural stimuli and did not elicit contacts by as many leafhoppers as maize. Tenure after contact also was significantly shorter on models than on maize. These data suggested that additional plant stimuli were used by Dalbulus leafhoppers during host-finding and/or accepting behaviors. After contacting a plant, most leafhoppers can detect external plant chemicals during surface exploration, and internal plant chemicals during probing and ingestion (Backus, 1985). However, only two species of Empoasca leafhoppers have been shown to respond to olfactory plant stimuli prior to contact (Saxena et al., 1974). We

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suggest that the specialization and pest status of D. maidis on maize may be enhanced if leafhoppers can differentiate maize from other plants while airborne or before initiating feeding. Therefore, in a series of laboratory bioassays, we examined the influence of plant volatiles on orientation and postcontact behaviors of male and female D. maidis and ,determined the relationship between visual and olfactory stimuli during host-finding.

METHODS

AND MATERIALS

Leafhoppers. Leafhoppers used in bioassays were between one and four weeks post-adult eclosion and were obtained from colonies kept in a rearing room maintained at 26 _+ 2~ and a 14:10 light-dark photoperiod. Colonies were established from individuals originally collected in Mexico (Nault, 1985), and maintained on six-leaf maize (cv. Aristogold Bantam Evergreen) for 20-60 generations in the laboratory. Leafhoppers were starved for 5-7 hr prior to testing to predispose them to host-finding (Todd et al., 1990) by releasing them into a plywood transfer hood (Heady and Nault, 1985). For bioassays requiring sexed adults, leafhoppers were anesthetized with CO2, and males and females were segregated into 30-cm x 7.2-cm-diam. butyrate tubes. The tubes were placed in the transfer hood until leafhoppers were conditioned for bioassays. Source of Volatiles. Extracts from the whorl leaves of three four-leaf maize seedlings were used as a source of volatiles for most bioassays. Whorl tissue was chosen because adults of D. maidis are found in high numbers in maize whorls in the field (Power, 1987) and in greenhouse studies (Todd et al., 1990b). Seedlings were cut just below the whorl. The whorl leaves were then placed in a glass tissue grinder and macerated in 30 ml of HPLC-grade hexane for 15 min. Extracts also were obtained from gamagrass, Tripsacum dactyloides (L.)L., and seedling sorghum, Sorghum bicolor (L.) Moench. Gamagrass leaves of roughly similar age to maize leaves were obtained by removing the youngest basal leaves that had not completely unfurled, and sorghum leaves were obtained in the same manner as maize leaves. All extracts were stored at - 10~ prior to use in bioassays. Observation Chamber. Bioassays were conducted in a Plexiglas observation chamber (OC) spray-painted black (Dutch Boy Flat Black 3727, The Sherwin-Williams Co.) on all outer surfaces except the top, which was left clear to facilitate observations (Figure 1). The side panels were removable. Two 5-cm x 5-cm windows were cut in the front panel to hold a 550-nm narrow band interference filter (green foliage stimulus) or neutral density filters (Oriel Corp.) of the same dimensions that served as the source of visual stimuli. The windows were centered on the panel and spaced 5 cm apart. The chamber was located in a dark room. A Kodak Ectagraphic III slide projector equipped with a 300-W

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/ FIG. 1. Observation chamber for testing the response of D. maidis to plant extracts. OC = observation chamber; MC = mixing chamber; HC = holding chamber; VT = vacuum tubing. The direction of airflow was from the right (upwind) to the left (downwind). Leafhopper contacts with a reflected square of light were recorded by transmitting projector light through filter(s) placed in the downwind window. Chamber dimensions are 25.5 x 21 x 19 cm. quartz projector bulb was placed 60 cm in front of the chamber, and the projector light was transmitted through the filter(s) so a reflected image appeared on the opposite chamber wall. To determine the effects of volatiles on leafhopper host-finding behavior, the chamber was modified by replacing the side panels with nylon mesh screening and by adding a mixing chamber (MC) to stabilize airflow and a holding chamber (HC) for the volatile source at the upwind end of the original chamber (Figure 1). The holding chamber was constructed from 8-cm x 10-cm x 1-cm pieces of wood painted black and placed next to the screening. The top of the holding chamber was removable. The mixing chamber was the same dimensions as the holding chamber and was wrapped tightly with three layers of fine cheesecloth. The two chambers were attached to each other and to the original chamber using black duct tape. An exhaust fan was used to pull volatiles through the chamber at a rate of 2.5 cm/sec and into 10-cm-diam. vacuum tubing (VT) attached to a separate box located at the downwind end of the chamber (Figure 1). The movement of the odor plumes was estimated using titanium tetrachloride and was observed to be nonlaminar, with considerable mixing throughout the chamber. General Bioassay Procedures. Twenty leafhoppers were introduced simultaneously, unless otherwise specified, 1 min prior to volatile presentation at the downwind end of the chamber. Leafhoppers were released by gently tapping them from an aspirator, which was positioned 2-3 cm above the center of the chamber floor. A volatile source was provided by pipetting 1 ml of maize,

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gamagrass, or sorghum extract (0.1 plant equivalents) onto 5.5-cm-diam. filter paper that was attached with an alligator clip to a piece of wire in a rubber cork; the height at the middle of the filter paper was 10 cm. The control consisted of filter paper treated with 1 ml of hexane. The volatile source was placed in the holding chamber (Figure 1), and data were collected on the number of contacts leafhoppers made with a reflected green square of light (bioassays 1-3) produced by transmitting the projector light through the 550-nm narrow band interference filter. Leafhopper response to reflected rather than transmitted light was examined based on previous knowledge of Dalbulus host-finding behavior (Todd et al., 1990a) and on observations indicating that fewer contacts were made with the actual filter than with the reflected image. A contact was recorded if an individual walked or flew directly onto the green light or turned back into the light after leaving momentarily. The number of contacts was recorded every minute for 15 min. Bioassays were conducted between 6 and 12 hr after lights on (14:10 light-dark photoperiod) and replicated 10 times unless otherwise specified, with a replicate consisting of a treatment and control run sequentially. A different group of 20 leafhoppers was used for each treatment and control, and after a bioassay, leafhoppers were returned to colonies. Preliminary observations indicated the window position of the filter did not elicit differential leafhopper contacts; therefore, all bioassays were conducted with the filter placed in the downwind window. The upwind window was covered temporarily with a piece of black construction paper until needed in bioassay 4 to examine the postcontact responses of leafhoppers to green light in the presence and in the absence of olfactory stimuli. All bioassays included a visual stimulus because leafhoppers released into the chamber with only chemical stimuli did not move off the chamber floor and exhibited no upwind orientation. Bioassay 1. Response to Green Light in Presence of Plant Volatiles. Orientation of D. maidis to green light in the presence of volatiles from maize, gamagrass, and sorghum was quantified separately as described in the general bioassay procedures.

Bioassay 2. Response to Green Light by Males and Females in Presence of Maize Volatiles. Differences between the sexes in orientation to green light in the presence of maize volatiles were determined using a randomized complete block design (N = 10) with four treatments presented separately: male + hexane; male + extract; female + hexane; and female + extract. One block was conducted per day, with 20 individuals used for each treatment within a block. Bioassay 3. Relationship between Light Quality and Maize Volatiles. The relationship between visual and olfactory stimuli during the orientation phase of host-finding by D. maidis was determined by quantifying the number of contacts made with two visual stimuli, represented either by green light or by white light, in the presence and in the absence of maize volatiles. The intensity of the white light was made similar to that of the green light (2 #E/m2/sec) by placing

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0.1, 0.3, and 0.6 neutral density filters in the downwind window. Light intensity was measured using a portable LI-185B Photometer (Li-Cor, Inc., Lincoln, Nebraska). A randomized complete block design (N = 10) was used with four treatments presented separately: green light + hexane; green light + extract; white light + hexane; and white light + extract. One block was conducted per day, with 20 individuals used for each treatment within a block. Bioassay 4. Postcontact Responses to Green Light in Presence of Maize Volatiles. To examine the chemically modulated, postcontact behaviors of D. maidis to green light, a piece of graph paper with 0.5-cm 2 grids was photocopied onto a transparency, and the transparency was taped to the back wall of the chamber where the green light appeared. To aid in detecting leafhoppers walking towards the light, the grid extended 3 cm in each direction beyond the lighted area. The grid lines outside of the light were illuminated by a 25-W incandescent red bulb positioned 10 cm above the chamber. A sheet of nonglare glass with the same inner dimensions as the chamber was placed in front of the grid to provide a smooth surface similar to that of the chamber walls. Leafhopper behavior was recorded using a RCA videocamera (model TC1005/U9) and a Panasonic videocassette recorder NV-8950. The camera was positioned so it viewed the grid through the upwind window on the front panel of the chamber. Twenty leafhoppers were observed individually for both the treatment and the control. Data were recorded on overall tenure within the green light, which was further subdivided into time spent stationary and time spent moving. The distance traveled was recorded by tracing the paths of individuals on an identical grid sheet photocopied onto a piece of paper. Distance (cm) was determined using an Inch Counter, an instrument that measures the length of a line or curve. Two measures of walking speed were determined by dividing the distance traveled by either the time spent moving or by the overall tenure, which included both stationary and moving time (overall speed). Statistical Analyses. Homogeneity of variances was tested using Bartlett's test (Sokal and Rohlf, 1981). Data from bioassays 1 and 4 were log (x + 1) transformed before being subjected to a t test for paired comparisons ( P _ 0.05), or a two-way analysis of variance (ANOVA) ( P _< 0.05) (bioassays 2, 3).

RESULTS

Bioassay 1. Response to Green Light in Presence of Plant Volatiles. D. maidis made approximately two times as many contacts with green light when exposed to maize volatiles as compared to hexane alone (t = 3.69, df = 9, P < 0.01) (Table 1). In contrast, the presence of gamagrass volatiles did not influence the number of contacts leafhoppers made with green light (t = 0.235,

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df = 9, P > 0.50). Fewer contacts were made with the light when leafhoppers were exposed to sorghum volatiles compared to hexane alone (t = 3.12, df = 9, P < 0.02). When maize volatiles were present, more than half of the leafhoppers were observed moving towards the green light within 2-3 min after release into the chamber compared to 7-8 min in controls. Most leafhoppers oriented towards the light by walking across the chamber floor until they were against the wall-floor juncture and then proceeded to walk up the wall and onto the light. A few individuals flew directly onto the light. Bioassay 2. Response to Green Light by Male and Female Leafl~oppers in Presence of Host Volatiles. Both sexes made more contacts with green light when maize volatiles were present compared to hexane alone ( F = 6.68, df = 1,36, P < 0.025). However, there was no significant difference in the number of contacts with green light made by males as compared to those made by females ( F = 2.72, df = 1,36 P > 0.10) (Table 1), nor was there an interaction between sex and maize volatiles ( F = 0.513, df = 1,36, P > 0.25). The mean number of contacts made with green light by males and females collectively was significantly higher when maize volatiles were present compared to hexane alone (Table 1). Bioassay 3. Relationship between Light Quality and Maize Volatiles. The quality of reflected light (green vs. white) had a highly significant effect on leafhopper contacts (Table 1). In the absence of maize volatiles, leafhoppers consistently made more contacts with green light than with white light ( F =

TABLE 1. INFLUENCE OF PLANT EXTRACTS ON CONTACTS MADE BY O. maidis WITH REFLECTED SQUARES OF LIGHT

(•

of contacts with green light

Plant extractb

Extract

Control

mixed

M G S

33.1 ___ 4.1a 12.4 • 1.1a 3.9 __ 0.7a

17.2 + 3.3b 12.9 + 1.9a 8.8 • 1.7b

2

male female mean

M

32.2 • 6.7a 20.8 • 5.3a 26.5 _+ 4.4a

16.3 • 3.4b 1t.8 • 2.5b 14.1 • 2.1b

3

mixed

M

15.7 • 2.0a

8.9 • 1.0b

Bioassay~

Sex

1

(•

of contacts with white light

Extract

Control

3.2 + 0.9c

2.8 + 0.8c

aFor bioassay 1, means within a row followed by the same letter are not significantly different at P _< 0.05 (t test for paired comparisons). For bioassays 2 and 3, means followed by the same letter are not significantly different at P < 0.05 by LSD. t~M = maize, G = gamagrass, S = sorghum.

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37.9, df = 1,36, P < 0.001). The effect of chemical alone was not significant ( F = 3.95, df = 1,36, P > 0.05). However, a significant interaction existed between visual and olfactory stimuli ( F = 5.31, df = 1,36, P < 0.05), with exposure to maize volatiles increasing the number of contacts made with green light but not with white light of similar intensity.

Bioassay 4. Postcontact Responses to Green Light in Presence of Maize Volatiles. Regardless of whether stationary or moving, individuals spent more time inside the boundaries of the green light in the presence of maize volatiles than in their absence (t = 3.47, df = 19, P < 0.01) (Table 2). When overall tenure was subdivided into stationary time and moving time, significantly more time was spent stationary when individuals were exposed to maize volatiles compared to hexane alone (t = 3.70, df = 19, P < 0.01) (Table 2). Maize volatiles did not have an effect on the time spent in movement (t = 0.077, df = 19, P > 0.90), the distance traveled within the green light (t = 0.494, df = 19, P > 0.50), or the rate of locomotion when walking (t = 1.07, df = 19, P > 0.20) (Table 2). However, the overall rate of locomotion was significantly slower within the green light when maize volatiles were present compared to hexane alone, due to increased stationary time (t = 3.09, df = 19, P < 0.01) (Table 2).

DISCUSSION

Host-finding is generally a catenary process during which an insect can be influenced by both noncontact and contact plant stimuli (Miller and Strickler, 1984). Orientation and settling can be mediated by both visual and olfactory stimuli (Prokopy and Owens, 1983; Visser, 1986). Sustained contact may TABLE 2. POSTCONTACT RESPONSES OF D. maidis TO GREEN LIGHT WHEN EXPOSED TO MAIZE VOLATILES

X (• Postcontact response Overall tenure (sec) Tenure stationary (sec) Tenure moving (sec) Distance traveled (cm) Speed moving (cm/sec) Overall speed (cm/sec)

Maize extract 164.5 155.9 8.6 10.2 1.1 0.07

• 25.9a" • 24.8a _+ 1.8a • 2.1a • 0.2a • 0.01a

Control 75.1 66.7 8.4 10.1 1.3 0.15

• 12.1b • l l.6b • 1.4a ___ 1.8a • 0.2a • 0.02b

aMeans within a row followed by the same letter are not significantly different at P _< 0.05 (t test for paired comparisons).

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require additional mechanical and/or gustatory stimuli, which presumably provide the insect with more specific information concerning suitability of the plant for feeding or oviposition (Scriber and Slansky, 1981). In the present study, we showed that olfactory plant stimuli influenced both orientation and postcontact behaviors of D. maidis to a foliage stimulus (Tables 1 and 2). Exposure to maize volatiles approximately doubled the number of contacts leafhoppers made with green light compared to contacts made with green light in the presence of hexane alone (Table 1). Discrepancies in the number of contacts made with green light in bioassays 1-3 may be due to differences in the flight activity of leafhoppers that were tested at different times during their photoperiod (R.A.J. Taylor, unpublished data). Volatiles from whorl tissue (Thompson et al., 1974) and other maize structures (Buttery and Ling, 1984) consist mainly of six-carbon green leaf-type compounds and sesquiterpenes, compounds that are attractive to many phytophagous insects during host-finding (Visser, 1986). Similar volatiles were identified from the homogenized-leaf maize extract used in this study and from the headspace over intact leaves using GC-MS (Todd and Phelan, unpublished data). D. maidis also exhibited a neutral response to gamagrass volatiles, and a negative response to sorghum volatiles (Table 1, bioassay 1). Although the constituents of gamagrass odor are not known, the lack of a significant response of D. maidis to odors from this plant compared to maize suggests that gamagrass volatiles are either qualitatively or quantitatively different from those of maize. D. maidis has been collected from gamagrass only when maize in nearby fields has died back (Triplehorn and Nault, 1985). In the laboratory, D. maidis reproduces on gamagrass, but the progeny are few in number, small in size, and take longer to develop than those on maize (Nault and Madden, 1985). Therefore, a weak response to gamagrass odor in the field may limit contacts, and thereby prevent some females from ovipositing in a plant that is not optimal for nymphal development and population growth. A chemical basis for resistance of sorghum to feeding by some homopterans may be due to HCN compounds and various phenolic acids (Dreyer et al., 1981). Although maize and sorghum look the same during seedling stages, if sorghum volatiles act as repellents, they may provide a mechanism by which D. maidis avoids sorghum. The nonhost status of sorghum for D. maidis has been established in the laboratory (L.R. Nault, unpublished data). Perhaps even more interesting than determining responsiveness of D. maidis to olfactory plant stimuli was determining that there was a significant interaction between host volatiles and the quality of reflected light (Table 1, bioassay 3), with maize volatiles acting as a synergist by increasing the number of contacts D. maidis made with green light, but not with quantitatively similar white light (Table 1). Chapman et al. (1981) also provided evidence for an interaction between visual and olfactory stimuli during host-finding by the aphid,

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Cavariella aegopodii (Scopoli), which was trapped in higher numbers in yellow water traps baited with carvone compared to unbaited yellow traps or colorless traps. These two studies provide the only documentation of an interaction between visual and olfactory stimuli within the Homoptera. In the field, the responsiveness of D. maidis to green reflected light may aid in distinguishing foliage from nonfoliage. However, because most plants are green, the use of color stimuli alone during host-finding may result in leafhoppers making contacts with nonhosts. The present data suggest that close-range chemoreception of plant volatiles (_< 20 cm from a source), coupled with an attractive color, may enable D. maidis to distinguish maize from nonhost plants while airborne (Table 1, bioassay 3). Chemoreception over a longer distance may be possible but could not be determined in our bioassays. There were no differences between the sexes in orientation to green light when exposed to maize volatiles, compared to hexane alone (Table 1, bioassay 2). Responsiveness to host odors by both male and female D. maidis may aid in bringing the sexes together for mating and has been shown for several Lepidoptera (Hansson et al., 1989, and references therein). The influence of host odors on the postcontact, nonfeeding behaviors of leafhoppers had not been documented prior to this study, which provides the first evidence that volatiles from a host can increase leafhopper tenure (Table 2). This observed increase in tenure was due to individuals spending more time stationary on the green light in the presence of maize volatiles than in the presence of hexane alone (Table 2), perhaps because the volatiles stimulated D. maidis to initiate probing. That probing is initiated soon after contact with maize seedlings is suggested by electronic monitoring of feeding behavior (A.C. Wayadande, unpublished data) and by observations that D. maidis remains at or near its initial landing position on seedling maize for up to 3 hr (Todd et al., 1990a). By comparison, exposure to maize volatiles resulted in a mean tenure of only 2.75 min for leafhoppers on green light (Table 2), suggesting that gustatory and/or mechanical stimuli perceived during feeding are of primary importance in maintaining leafhopper contact with a host. Although postcontact behaviors of the sexes were not observed separately, observations suggested that males spent more time moving within the boundaries of the green light than females in both the treatment and the control. Greater male mobility was demonstrated for Dalbulus species by Heady and Nault (1985), who showed that males were more likely to fly when mechanically dislodged from maize seedlings than females. Hunt (1988) found that male Graminella nigrifrons (Forbes) leafhoppers engaged in more interplant flights than females when given access to oat seedlings (Avena sativa L.), a strategy for increasing the likelihood of locating a calling virgin female. Similarly, if D. maidis males are very mobile after contacting a host plant, they may increase

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their likelihood o f locating females d u r i n g intraplant m o v e m e n t s and thereby e n h a n c e their m a t i n g success. T h e present data, c o u p l e d with previous k n o w l e d g e on the responses of D. m a i d i s to color stimuli ( T o d d et al., 1990a), provide a m o r e c o m p l e t e u n d e r standing o f host-finding behaviors of this species. The strong orientation response o f D. m a i d i s to y e l l o w a n d green m a y aid this leafhopper in disting u i s h i n g foliage from n o n f o l i a g e w h e n flying above plant canopies. W h e n comb i n e d with an attractive color, the differential responsiveness of D. m a i d i s to plant odor m a y further aid it in orientation and settling. In addition, we have provided further insight into the specialization and pest status of D. m a i d i s on maize by d e m o n s t r a t i n g that maize volatiles not only have an effect on orientation, but also o n postcontact behaviors not associated with feeding. Acknowledgments--We thank W.E. Styer for technical assistance, D.V. Markowitz for help with graphics, and M.O. Harris for stimulating our interest in determining the relationship between visual and chemical stimuli during leafhopper host-finding. Salaries and support were provided by state and federal funds as well as grants from the USDA Competitive Research Grants Office (84CRCR-l-1370 and 88-37153-3528), appropriated to the Ohio Agricultural Research & Development Center, The Ohio State University, Journal Article No. 232-89.

REFERENCES BACKUS,E.A. 1985. Anatomical and sensory mechanisms of leafhopper and planthopper feeding behavior, pp. 163-194, in L.R. Nault and J.G. Rodriguez (eds). The Leafhoppers and Planthoppers. John Wiley & Sons, New York. BROMLEY,A.K., and ANDERSON,M. 1982. An electrophysiological study of olfaction in the aphid Nasonovia ribis-nigri. Entomol. Exp. Appl. 32:101-110. BUTTERY,R.G., and L~NG,L.C. 1984. Corn leaf volatiles: Identification using Tenax trapping for possible insect attractants. J. Agric. Food Chem. 32:1104-1 t06. CARD~, R.T. and BAKER,T.C. 1984. Sexual communication with pheromones, pp. 355-383, in W.J. Bell and R.T. Card6 (eds.). Chemical Ecology of Insects. Sinauer Assoc., Sunderland, Massachusetts. CHAPMAN,R.F., BERNAYS,E.A., and SIMPSON,S.J. 1981. Attraction and repulsion of the aphid, Cavariella aegopodii, by plant odors. J. Chem. Ecol. 7:881-888. CLAR1DGE,M.F. 1985. Acoustic signals in the Homoptera: behavior, taxonomy, and evolution. Annu. Rev. Entomol. 30:297-317. DREYER, D.L., REESE,J.C., and JONES, K.C. 1981. Aphid feeding deterrents in sorghum: Bioassay, isolation, and characterization. J. Chem. Ecol. 7:273-284. EISENBACH,J., and M1TTLER,T.E. 1987. Sex pheromone discrimination by male aphids of a biotype of Schizaphis graminum. EntomoI. Exp. Appl. 43:181-182. HANSSON,B.S., VAN DER PERS, S.N.C., and LOFQUmT,J. 1989. Comparison of male and female olfactory cell response to pheromone compounds and plant volatiles in the turnip moth, Agrotis s eg etum. Physiol. Entomol. 14:147-155. HEADY, S.E., and NAULT, L.R. 1985. Escape behavior in Dalbulus and Baldulus leafhoppers. Environ. Entomo l. 14:155-158.

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