Movement of the grape berry moth, Endopiza viteana: displacement distance and direction

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1 Physiological Entomology (2004) 29, Movement of the grape berry moth, Endopiza viteana: displacement distance and direction NATALIA BOTERO-GARCE S and RUFUS ISAACS Department of Entomology, Michigan State University, East Lansing, Michigan, U.S.A. Abstract. Mark release recapture is used to quantify displacement by adults of the North American grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae) under field conditions. Moths marked with fluorescent dust are released eight times in the centre of a vineyard over 2 years, and recaptured using pheromone traps and interception traps. In vineyards, male moths are recaptured an average of m from the release site (maximum 58.2 m), whereas female displacement is similar with average flight distances of m (maximum 41.2 m). Increasing wind speed during moth flight activity periods suppresses displacement by both sexes, and females are less likely than males to fly in winds above 0.6 m s 1. The majority of males are recaptured upwind from the release site or at a tangent to the overall mean wind direction when responding to pheromone traps, whereas female moths trapped in interception traps exhibit a large variability in direction from the release point. Releases of marked moths in woods adjacent to a vineyard demonstrates interhabitat movement by E. viteana males and by a single female. The average maximum displacement by males during interhabitat movement is m, significantly greater than the average maximum of m inside the vineyard habitat. Key words. Endopiza viteana, flight, grape, interception trap, pheromone. Introduction The grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae) [Paralobesia viteana (Clemens), J. Brown, personal communication] is a monophagous primary pest of cultivated grapes across Eastern North America (Dennehy et al., 1990; Nagarkatti et al., 2002a, b; Trimble et al., 2003). Its native hosts are Vitis spp. vines (Vitaceae), commonly found in disturbed areas and woods of North America (Morano and Walker, 1995). There are typically two to three generations annually (Biever and Hostetter, 1989; Witzgall et al., 2000; Tobin et al., 2003), with larval infestation in vineyards increasing from generation to generation. Despite the economic importance of this species, little is known about the flight behaviour of adult moths. Pheromone traps have been the main approach used to Correspondence: Dr Rufus Isaacs, Department of Entomology, Michigan State University, 202 Center for Integrated Plant Systems, East Lansing, Michigan 48824, U.S.A. Tel.: þ ; fax: þ ; isaacsr@msu.edu monitor populations, but these have provided only indirect evidence of patterns of male moth distribution within and outside vineyards (Hoffman and Dennehy, 1989; Botero-Garce s and Isaacs, 2003). The distribution of infestation by E. viteana larvae in vineyards has been used to infer that female distribution is consistently greater at the edges of vineyards compared with the interiors, particularly adjacent to wooded borders (Hoffman and Dennehy, 1989; Botero-Garce s and Isaacs, 2004). Because these woods often contain wild Vitis spp. vines (Hoffman and Dennehy, 1989; Morano and Walker, 1995; Botero-Garce s and Isaacs, 2004), movement of female moths from woods to vineyards has been proposed as the cause of the observed larval distributions (Taschenberg and Roelofs, 1977; Dennehy et al., 1990; Trimble, 1993). Direct measurement of movement by this species has not been reported, but mark release recapture methods could provide information concerning displacement, direction of movement and the influence of environmental conditions to help understand distribution of E. viteana. Mark release recapture studies have used marks including tags, body mutilations, paint, genetic markers, # 2004 The Royal Entomological Society 443

2 444 N. Botero-Garce s and Rufus Isaacs radioactive-isotopes, protein or genetically engineered marks (Hagler and Jackson, 2001), or dyes incorporated into meridic diets (Showers et al., 1989; Keil et al., 2001). Marking with fluorescent pigment dusts has been successfully used for marking small insects (García-Salazar and Landis, 1997; Cronin et al., 2001) including moths, without affecting survival or ability to find pheromone traps (Mo et al., 2003). Muirhead-Thomson (1991) has recommended that at least two types of traps with different principles of capture be used when studying insect flight because this may provide comparative data to assist with interpretation of movement patterns, and thus findings are less dependent on trap type. Pheromone traps are highly effective and can provide insight in male moth capacity for flight to potential mates, but they capture only part of the population and may bias male moth movement (Weissling and Knight, 1994). Passive or interception traps give an indication of natural distribution and flight patterns of foraging insects (Muirhead-Thomson, 1991) and can provide information on both male and female moths, which has been difficult to date because no female attractant has been developed for E. viteana. Weissling and Knight (1994) and Knight (2000) used a type of passive interception trap, consisting of transparent plastic panes coated with sticky material and hung in host-plant canopies, to trap both sexes of Cydia pomonella in apple orchards. If appropriately maintained, this trap does not provide visual or olfactory cues (Weissling and Knight, 1994), but functions by moths contacting the sticky surface and being trapped. Quantification of flight parameters by tortricid pests of fruit has been performed for the codling moth, C. pomonella (Schumacher et al., 1997; Dorn et al., 1999; Keil et al., 2001), the oriental fruit moth, Cydia molesta (Hughes and Dorn, 2002) and the European grape berry moth, Lobesia botrana (Hurtrel and Thie ry, 1999). Schumacher et al. (1997) found that C. pomonella has the capacity to engage in long-range flights up to 11 km. Hughes and Dorn (2002) showed that a small proportion of C. molesta, most likely gravid females, ventured into long flights, although these were much shorter than those of C. pomonella. Elucidating the displacement potential of E. viteana will improve knowledge of the ability of the insect to survive in ephemeral environments or the ability to colonize new ones. This may also help to develop effective pest-management strategies because mating disruption of this pest will be less effective if gravid females are capable of immigration from wild areas into vineyards (Trimble, 1993; Trimble et al., 2003). The goals of this study are to determine (i) the displacement capacity of E. viteana adult male and female moths in vineyards; (ii) the effect of environmental parameters on moth displacement; and (iii) whether this species moves between woods and vineyards. Materials and methods The study was conducted in a 4-year-old vineyard (Vitis labrusca, var. Niagara, Vitaceae) (Fig. 1), at the Trevor N woods grasses vineyard 60.0 m orchard Nichols Research Complex, Allegan County, Michigan, during 2001 and The vineyard was 32 rows long by 21 vines wide, planted on a m spacing (672 vines), and was bordered by another vineyard on its eastern side by a 30-year-old deciduous woodland to the west, an apple orchard to the south and a grassy field to the north. The vineyard was managed according to recommendations for disease management (Wise et al., 2003), but received no broad-spectrum insecticides. Traps used for recapture Pheromone traps Pane traps Release point vineyard Fig. 1. Schematic representation (not to scale) of the experimental site where marked moths were released. Pheromone and pane traps were arranged around a central vineyard release point in concentric ovals; a release point inside the woods (20 m from the edge) was also used to determine extent of movement between woods and vineyards. Two types of traps were used to capture E. viteana: (i) pheromone traps for males and (ii) passive interception pane traps for both sexes. The pheromone traps (Large Plastic Delta Trap 1, Suterra LLC, Bend, Oregon) contained rubber septa impregnated with 0.1 mg of synthetic sex pheromone [90 : 10 ratio of (Z)-9-12Ac and (Z)-11-14Ac, respectively] and lined with sticky inserts. New inserts m

3 Displacement of adult Endopiza viteana 445 were used every time that the moths were found in traps, and the pheromone was replenished every month using the same batch of septa. The interception traps were made of mm Plexiglas panes, coated on both sides with tangle trap paste (The Tanglefoot Company, Grand Rapids, Michigan). All traps were hung, longer edge vertical, from a vine trellis with the top approximately 1.5 m high, and the plastic panes were secured to the ground by strings to maintain their position. Twenty-three pheromone traps and 33 interception traps were deployed in the vineyard during 2001 and 25 pheromone plus 31 pane traps in The traps were arranged in a pattern of concentric ovals, radiating from the middle to the periphery to cover the area of the vineyard (Fig. 1). Two pheromone traps were placed in the border of each of the four types of adjacent habitats surrounding the vineyard, separated by 20 m. On the northern grassy edge, the traps were suspended at 1.5 m on steel rods planted into the ground. In the vineyard to the east, they were hung from the trellis wire, before the first vine of the row. In the orchard to the south and woods to the west, the traps were hung from tree branches at 1.5 m. Eight pheromone traps and four pane traps were deployed in the woods (Fig. 1). Marking moths Moths for release were taken from the E. viteana colony at the Small Fruit Entomology Laboratory, Michigan State University, East Lansing, Michigan. The colony was established in 2000 from larvae collected in a commercial vineyard in Van Buren County, Michigan. Adult moths (1 : 1 sex ratio) were maintained at 26 C and 70 80% relative humidity (RH) under a LD 16 : 8 h photoperiod. Larvae were reared in the laboratory on commercial table grapes (washed in 1% bleach before use) at C and LD 16 : 8 h, 30% RH, or on a meridic diet (Nagarkatti et al., 2000) inside an environmental chamber at the same conditions as above, except that temperature was 25 C. To help preserve wild traits, moths reared from grapes collected in the same vineyard were added to the colony at the end of Newly emerged adult grape berry moths were collected for 3 days and held in 3.8 L white utility pails covered on the top with fine white mesh. An opening on the side of each pail with a cotton sleeve attached allowed access without the insects being able to escape. Water was provided by damp dental cotton wicks either fixed to the bottom of the cages or on top of the mesh covering it. The insects were not provided with any grapes before release, and the mating status of the moths was not determined. Moths of both sexes were held for up to 4 days until sufficient moths were collected for release. To mark the moths, 0.5 g of dry fluorescent dust dye (Dayglo Color Division, Switzer, Cleveland, Ohio) was dissolved in 75 ml of acetone (99.9%) in a small cosmetic spray bottle. The cotton wick was removed from each bucket and adult moths were sprayed with the solution through the veil. To avoid excess drops of solution forming on the bottom, the pail was inverted then tapped on the bottom so that moths landed on the veil, and then the solution was sprayed through it. Moths on the mesh dried immediately after being sprayed with the acetone and dye solution. After marking, moths were taken to the release point and placed in the shade for 2 4 h until release. Moth releases Releases in the vineyard were made at its central point, at the base of a vine. Moths were released between and hours, when wind speed was low, air temperature was approximately 25 C, and rain was not expected on subsequent days. To release the moths, the bucket was placed on its side and the mesh was removed to enable the moths to fly out. On the next day, the number of moths released was determined by subtracting the number of moths found dead inside the bucket from the original number. Moths were released four times in the vineyard in both 2001 and 2002, and three times in the woods during 2002 (Table 1). Release methods in the woods were similar: marked moths were taken to a point 20 m inside the woods (45 m away from the vineyard), directly across from the vineyard point of release (Fig. 1). The bucket was placed tilted on the ground, and moths were allowed to fly out overnight. The number of released moths was determined by subtracting the number of dead moths found on the next day. Moth recapture All traps were checked at 48-h intervals, starting from 24 h after release to 300 h after release, or until 1 week passed after the last release of the year without recapture of moths. Pheromone trap inserts with moths were taken to the laboratory and examined by illuminating them with a portable 115 V ultraviolet light (Black Ray UVL-22, Ultraviolet Products Inc., San Gabriel, California) under a microscope. The presence of fluorescent dust was used to distinguish released moths from the background population. Moths captured on sticky pane traps were removed with a spatula in the field and taken individually to the laboratory where they were observed in the same way. All moths caught in panes were sexed. Weather data Hourly averages of wind speed, wind direction, precipitation and air temperature were recorded by a CR10X weather station (Campbell Scientific, Logan, Utah) positioned 563 m from the study vineyard. Hourly averages of weather parameters were selected for every day between 1 July and 21 September for each year and, from these values, the values for between and hours were selected

4 446 N. Botero-Garce s and Rufus Isaacs Table 1. Total number of marked Endopiza viteana moths released and recaptured in pheromone and pane traps. Marked E. viteana moths Number recaptured Percentage recaptured Number released Males Females Males Females Releases in vineyard 12 July July July August July August August August Total Releases in woods 1 August August August Total Recapture percentages were calculated for each sex based on a 1 : 1 sex ratio of released moths. because this corresponds to the period of flight activity for grape berry moth (G. English-Loeb, personal communication). For each recaptured moth, weather data were averaged for the period of time between the release and the evening before traps were checked. Data on average wind speeds were also ranked into intervals of 0.2 m s 1, between 0.0 and 2.0 m s 1 for all individual moth flights. Data analysis To determine differences in distance moved between sexes or between moths released in the vineyard vs. those released in the woods, the NPAR1WAY procedure (SAS, Version 8.0; SAS Institute, 1996) was used with a Kruskal Wallis test for nonparametric data (SAS Institute, 1996). To evaluate the direction of moth movement in relation to wind direction, and to compare differences in movement direction between sexes and trap types, the data on individual moths were analysed using Oriana 1 software (Version 1.06; Oriana, 1994). Calculations of Watson s F-test were conducted to compare pairs of circular means because this test is particularly powerful for small samples (Batschelet, 1981). Circular histograms, in which 0 corresponds to the actual North of the spatial location, were produced to show the mean angle direction comprising the mean angle (vector) and 95% confidence intervals for each of the wind and moth direction samples. Data on individual moths recaptured were analysed using the REG procedure (Model 1) (SAS, Version 8.0; SAS Institute, 1996) to determine the relationship between all weather factors and the distance flown by moths. A two sample paired t-test was used to determine whether male and female moth movement was similarly affected by overall wind speed between release and recapture (SAS Institute, 1996). Results A total of 3305 moths was released in the course of 11 releases during the 2 years of the study (Table 1), with 246 moths being recaptured (7.4%). A consistently greater proportion of males was recaptured than females in both habitats, reflecting pheromone trap efficiency (Table 1). Comparison of the weather conditions during the release period, between 1 July and 21 September, showed similar conditions during both years (Fig. 2). The average temperature during hours in this period was 22.3 Cin 2001 and 24.1 C in Mean RH was 68.2% the first year and 63.8% during the second (Fig. 2). Precipitation was low overall (10 periods of moth movement activity with rain events in 2001 and 12 in 2002, over 83 such periods per year) with a mean precipitation of 0.09 mm day 1 in 2001 and 0.04 mm in Mean wind speed was 1.2 m s 1 in 2001 and 1.1 m s 1 in Average wind direction ( h) was (heading ENE) during 2001 and (heading ENE) for 2002 during the days when moths were released in the vineyard, with no significant difference between years (Watson s F ¼ 0.10, d.f. ¼ 1,164, P ¼ 0.75). The eight moth releases in the vineyards across both years were therefore treated as separate replicates in subsequent analyses. Vineyard-released moths Overall, 8.4% of the moths released in vineyards were recaptured, and no moths released in the vineyard were

5 Displacement of adult Endopiza viteana 447 Fig. 2. Weather conditions during the period between 1 July and 21 September of 2001 and 2002 (temperature, relative humidity, wind speed and direction). Vertical arrows represent releases for each year. The circular histograms illustrate wind direction for each year, with mean angular vector and 95% confidence limits. Each ring represents a number of observations. The small arrows next to the histograms represent the average wind direction and 0 represent the North. Data were obtained by averaging values between and hours (moth active time) for each day. recaptured in other habitats. The highest recapture rate was achieved for moths released on 31 July 2001, when almost 32% of the males released were recaptured (Table 1). Only male moths were caught in pheromone traps and, although fewer moths were trapped in the pane traps (13% of total recaptured), 69.1% of moths trapped in this design were female (Table 1). Male E. viteana were recaptured in pheromone traps from 7.11 to 58.2 m from the release point, with the furthest-moving male being caught within 144 h after release. The median of maximum male moth displacement for each release was 43.6 m. Female E. viteana were recaptured in interception traps from 3.2 to 41.2 m from the release point, with the furthest-moving female being caught within 456 h after release. The median maximum female displacement was 78.0 m from the central release point. Mean displacement distances for both sexes were 13.3 m for males and 3.5 m for females. There was no significant difference between sexes in the distance from release point to their recapture on pane traps (Kruskal Wallis w 2 ¼ 0.33, d.f. ¼ 1, P ¼ 0.57). The mean overall direction taken by all recaptured moths during the eight releases was (SSE) for males and (SE) for females (Table 2). Movement direction data were analysed according to the type of trap used and the sex of moths. For moths captured in pheromone traps (males), there was a significant difference between overall direction of movement and the direction of the wind during the period of flight between release and recapture (F ¼ 47.01, d.f. ¼ 1,390, P < 0.01) (Fig. 3). The mean direction vector for male moths in pheromone traps was , and for wind, indicating that overall moth displacement was at a 64.3 tangent from the direction of the wind (Fig. 3), signifying upwind flight. Male moths caught in pane traps also had a significantly different displacement direction from the wind direction (F ¼ 12.30, d.f. ¼ 1,16, P < 0.01) with a mean vector of for moth displacement and for wind (Fig. 3), indicating a variable and generally downwind displacement by these male moths. The mean direction of female recapture from the point of release was also significantly different from the wind direction (F ¼ 5.43, d.f. ¼ 1,38, P < 0.03), with large variability among individual displacement directions and a mean vector of The wind direction during the flight time of each of these female moths was much less variable, at (Fig. 3). There was no difference in the direction of recapture from the point of release between females

6 448 N. Botero-Garce s and Rufus Isaacs Table 2. Maximum and mean displacement distances of marked Endopiza viteana moths released in two habitats, and mean overall direction from release to recapture. Maximum displacement (m) Mean SE displacement (m) Mean SE direction (degrees) Males Females Males Females Males Females Releases in vineyard 12 July July July August July August August August Average per moth Releases in woods 1 August August August 2002 Average per moth and males caught in pane traps (F ¼ 0.10, d.f. ¼ 1,27, P ¼ 0.76). In general, measured weather factors did not greatly affect moth movement. For males and females, the average wind speed and precipitation did not significantly affect displacement (Table 3). Air temperature (T) affected female, but not male movement (Table 3) because the displacement (D) of individual females tended to be lower at lower air temperatures (D ¼ 2.35T 46.70) than occurred with males (D ¼ 0.44T 3.67). Moths were recaptured when winds were between 0.6 and 2.0 m s 1 and, accordingly, the displacement and captures of moths were compared for males and females across 0.2 m s 1 categories of wind speed across this range. Wind speed averages did not affect displacement by males (F ¼ 1.94, d.f. ¼ 1,203, P ¼ 0.165) or females (F ¼ 2.31, d.f. ¼ 1,18, P ¼ 0.146) (Fig. 4), indicating that similar displacement occurred during each wind speed interval, corroborating results in Table 3. Although lower captures of male moths were found as the wind speed increased (r 2 ¼ 0.57), the regression was not significant (F ¼ 5.30, d.f. ¼ 1,4, P ¼ 0.08) (Fig. 4). The number of female moths recaptured also exhibited no response to wind speed (r 2 ¼ 0.01, F ¼ 0.04, d.f. ¼ 1,4, P ¼ 0.84), although the regression lines for the two sexes were significantly different, indicating a gender-specific response to wind (t ¼ 3.19, d.f. ¼ 1,5, P ¼ 0.02) (Fig. 4). recaptured further from the point of release (64.1 m) than those released in the vineyard (13.8 m) (Table 2) (w 2 ¼ 51.24, d.f. ¼ 1, P < ). Male moth maximum displacement from the release point in the woods ( ) was significantly greater than for those released in the vineyard ( ) (Mann Whitney U-test ¼ 2.08, P ¼ 0.036). Only one female was recaptured from the wood releases, in the adjacent vineyard, and it was not possible to analyse the displacement values of female moths released in the woods. There was a significant difference between the angle of male moth displacement ( ) and wind direction ( ) (F ¼ 348.5, d.f. ¼ 1,46, P < 0.01) (Fig. 5), with moths moving generally in the direction of the wind, toward the adjacent vineyard. Regression analysis of the displacement distances of moths released in the woods and the time between release and recapture was significant (F ¼ 4.46, d.f. ¼ 1,22, P < 0.05) but with a low coefficient of determination (0.17). Of the four weather factors compared, mean wind speed (F ¼ 4.51, d.f. ¼ 1,22, P < 0.05, r 2 ¼ 0.17) was significantly associated with displacement distance by moths released in the woods. Unlike vineyardreleased moths, which were not affected by wind speed, wood-released moths achieved greater displacement under lower wind (W) speeds (D ¼ 49.48W þ ). The distance moths travelled was not significantly correlated with air temperature (F ¼ 1.62, d.f. ¼ 1,22, P ¼ 0.22, r 2 ¼ 0.07). Wood-released moths Twenty-three of the male moths released in the woods were recaptured, 17 of them in the vineyard and the other six in one pheromone trap at the vineyard-facing edge of the woods. On average, male moths released in the woods were Discussion Use of fluorescent dust and two different trap types has enabled the first quantification of displacement by E. viteana under field conditions. Although the exact route taken by moths between release and recapture is not

7 Displacement of adult Endopiza viteana 449 Fig. 3. Circular histograms of the frequency and distribution of overall moth displacement vectors and wind direction for the period that moths were flying between release and recapture. The mean angular vector with 95% confidence limits runs beyond the outermost circle; 0 corresponds to the North and the centre of the histogram is the vineyard release point. The arrows represent the average directions from the point of release to where the moths were recaptured and the wind direction. known, maximum displacement is consistently lower for females than males in the vineyard habitat. The shorter displacement of female E. viteana released in the vineyard is unexpected because observations on similar tortricids have indicated that females are more likely than males to engage in longer flights (Schumacher et al., 1997; Hughes and Dorn, 2002). The low female dispersal may have been a response to the abundance of oviposition resources found in the study site. Although female average maximum displacement is further than that for males, it is 10-fold lower than values reported for C. molesta in laboratory studies using flight mills (Hughes and Dorn, 2002). The present data are in agreement with the earlier suggestions by Ingerson (1920) and Nagarkatti et al. (2002a) that E. viteana are poor fliers, although some propensity for longer distance displacement is found; moths recaptured over 50 m from their release point comprised 2.6% in the vineyard and 75.0% in the woods. Environmental conditions determine the extent and occurrence of flight, particularly by small insects (Kisimoto and Sogawa, 1995; Dingle, 1996; Schowalter, 2000). Wind speed is typically one of the most important abiotic factors affecting flight in insects, but this is not a significant factor determining displacement by E. viteana (Table 3). The average wind speed during the flight activity periods was 1.2 m s 1 in 2001 and 1.1 m s 1 in 2002, which is well within the range of m s 1 cited as the range for take off for many insects (Pasek, 1988; Colvin, 1995). However, take-off and directed flight by E. viteana in wind tunnels is reduced in wind of only 0.66 m s 1 (G. English-Loeb, personal communication), further indicating that E. viteana is not a strong flier. Weather data collected during moth flight periods between each moth s release and recapture provide a general estimate of the environmental conditions experienced during moth movement, but the microclimatic conditions experienced during Table 3. Regression analysis of distance between release and recapture of marked Endopiza viteana moths and average weather conditions for periods of flight activity between release and recapture of each moth in the vineyard. Weather factor Moths recaptured in: d.f. Wind speed (m s 1 ) Air temperature ( C) Precipitation (mm) Pheromone traps F 11, P r Pane traps Males F 1, P r Females F 1, P r Significant regressions are indicated in bold.

8 450 N. Botero-Garce s and Rufus Isaacs No. of moths/interval Wind speed intervals (m s 1 ) Males Females Fig. 4. Distribution of male (solid) and female (open) Endopiza viteana adults according to ranked wind speeds that they experienced during flight activity. Data for each 0.2 m s 1 wind speed interval is indicated at the lower end of the interval. flight are expected to vary from that measured at the nearby weather station. Despite the potential differences between measured and experienced climatic conditions, comparisons of moth movement and winds during flight periods indicate that adult E. viteana have some degree of control over their flight. This is demonstrated by some males being caught in pheromone traps upwind from the release point, whereas others are caught by traps located at a tangent to the overall mean wind direction. Support for directed flight by E. viteana is also provided by the recapture of moths released in the woods. In this case, regardless of the presence of pheromone traps located in directions between 135 and 360 around the wood-release point, moths were only recaptured east of the point of release ( ), in directions toward the vineyard. This indicates that male moth movement is not driven solely by a response to pheromone, but rather that moths will fly between habitats. Males recaptured in the woods before crossing the interface towards the vineyard may have encountered the pheromone plume and been diverted from their original direction. Although only one female moth was detected moving from the woods into the vineyard, it was recaptured 79 m from the release site, suggesting a potential for interhabitat movement into vineyard borders, as proposed previously (Taschenberg and Roelofs, 1977; Dennehy et al., 1990; Trimble, 1993; Botero-Garce s and Isaacs, 2004). Laboratory studies of the flight capacity of E. viteana should aim to determine the propensity for long-range flight using flight mills, which would allow determination of whether flight is affected by age, sex or physiological state. Behavioural data can then be added to the information obtained from landscape context studies (e.g. Thies et al., 2003) to improve assessment of the risk of grape berry moth impact on vineyards, and the risk of infestation moving from nearby vineyards and woods. Given that E. viteana is found in cultivated and natural habitats (Trimble, 1993; Nagarkatti et al., 2002a; Botero-Garce s and Isaacs, 2003), the different host density and distribution in these habitats may be an important factor in displacement by this species. It is also important to consider the possibility that different races of E. viteana (proposed by Tobin et al., 2002) may behave differently in different grape agroecosystems, depending on the selection pressure for dispersal ability. Recent studies have demonstrated heritability in the flight activity of C. pomonella populations (Keil et al., 2001), and the variable host availability in woodlands compared with vineyards may be expected to select for greater investment in flight capacity in woodland, compared with vineyard, populations of E. viteana. Acknowledgements We thank Kelly Bahns, Matt Wilson and Zsofia Szendrei for technical assistance with the fieldwork, Elly Maxwell for maintaining the insect colony, John Wise and Matt Daly for maintenance of research sites, and Matthew Collett for statistical advice. Funding was provided by the Michigan Agricultural Experiment Station, National Grape Cooperative, Michigan State Horticultural Society, and by the College of Agriculture and Natural Resources through a Dissertation Completion Fellowship for the primary author. This study was completed in partial fulfilment of the PhD requirements of Natalia Botero- Garce s. Fig. 5. Circular histograms of the frequency and distribution of displacement vectors of moths released from the woods and wind direction for the period that moths were flying between release and recapture in vineyard traps. The mean angular vector with 95% confidence limits runs beyond the outermost circle; 0 corresponds to the North and the centre of the histogram is the wood-release point. The arrows represent the average directions taken by the moths and the wind direction. References Batschelet, E. (1981) Circular Statistics in Biology. Academic Press, U.K. Biever, K.D. & Hostetter, D.L. (1989) Phenology and pheromone trap monitoring of the grape berry moth, Endopiza viteana

9 Displacement of adult Endopiza viteana 451 Clemens (Lepidoptera: Tortricidae) in Missouri. Journal of Entomological Science, 24, Botero-Garce s, N. & Isaacs, R. (2003) Distribution of grape berry moth, Endopiza viteana (Lepidoptera: Tortricidae), in natural and cultivated habitats. Environmental Entomology, 32, Botero-Garce s, N. & Isaacs, R. (2004) Influence of uncultivated habitats and native host plants on cluster infestation by grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae), in Michigan vineyards. Environmental Entomology, 33, Colvin, J. (1995) The regulation of migration in Helicoverpa armigera. Insect Migration. Tracking Resources Through Space and Time (ed. by V. A. Drake and A. G. Gatehouse), pp Cambridge University Press, U.K. Cronin, J.T., Hyland, K. & Abrahamson, W.J. (2001) The pattern, rate, and range of within-patch movement of a stem-galling fly. Ecological Entomology, 26, Dennehy, T.J., Hoffman, C.J., Nyrop, J.P. & Saunders, M.C. (1990) Development of low-spray, biological and pheromone approaches for control of grape berry moth, Endopiza viteana Clemens, in the Eastern United States. Monitoring and Integrated Management of Arthropod Pests of Small Fruit Crops (ed. by N. Bostanian, L. Wilson and T. J. Dennehy), pp Intercept Ltd, U.K. Dingle, H. (1996) Migration: The Biology of Life on the Move. Oxford University Press Inc., U.K. Dorn, S., Schumacher, P., Abivardi, C. & Meyhofer, R. (1999) Global and regional pest insects and their antagonists in orchards: spatial dynamics. Agriculture, Ecosystems and Environment, 73, García-Salazar, C. & Landis, D.A. (1997) Marking Trichogramma brassicae (Hymenoptera: Trichogrammatidae) with fluorescent marker dust and its effect on survival and flight behavior. Journal of Economic Entomology, 90, Hagler, J.R. & Jackson, C.G. (2001) Methods for marking insects: current techniques and future prospects. Annual Review of Entomology, 46, Hoffman, C.J. & Dennehy, T.J. (1989) Phenology, movement and within-field distribution of the grape berry moth, Endopiza viteana (Clemens) (Lepidoptera: Tortricidae) in New York vineyards. Canadian Entomologist, 121, Hughes, J. & Dorn, S. (2002) Sexual differences in the flight performance of the oriental fruit moth, Cydia molesta. Entomologia Experimentalis et Applicata, 103, Hurtrel, B. & Thie ry, D. (1999) Modulation of flight activity in Lobesia botrana Den. & Schiff. (Lepidoptera: Tortricidae) females studied in a wind tunnel. Journal of Insect Behavior, 12, Ingerson, H.G. (1920) Life history of the grape-berry moth in northern Ohio. U.S. Department of Agriculture Bulletin 911. USDA, Washington, District of Columbia. Keil, S., Gu, H. & Dorn, S. (2001) Response of Cydia pomonella to selection on mobility: laboratory evaluation and field verification. Ecological Entomology, 26, Kisimoto, R. & Sogawa, K. (1995) Migration of the brown planthopper Nilaparvata lugens and the white-backed planthopper Sogatella furcifera in East Asia: the role of weather and climate. Insect Migration. Tracking Resources Through Space and Time (ed. by V. A. Drake and A. G. Gatehouse), pp Cambridge University Press, U.K. Knight, A.L. (2000) Monitoring codling moth (Lepidoptera: Tortricidae) with passive interception traps in sex pheromonetreated apple orchards. Journal of Economic Entomology, 93, Mo, J., Baker, G., Keller, M. & Roush, R. (2003) Local dispersal of the diamondback moth (Plutella xylostella (L.) (Lepidoptera: Plutellidae). Environmental Entomology, 32, Morano, L.D. & Walker, M.A. (1995) Soils and plant communities associated with three Vitis species. American Midland Naturalist, 134, Muirhead-Thomson, R.C. (1991) Trap Responses of Flying Insects: The Influence of Trap Design on Capture Efficiency. Academic Press, U.K. Nagarkatti, S., Muza, A.J. & Saunders. M.C. (2000) Meridic diet for rearing Endopiza viteana Clemens (Lepidoptera: Tortricidae). Canadian Entomologist, 32, Nagarkatti, S., Muza, A.J., Saunders. M.C. & Tobin, P.C. (2002a) Role of the egg parasitoid Trichogramma minutum in biological control of the grape berry moth, Endopiza viteana. Biocontrol, 47, Nagarkatti, S., Tobin, P.C., Muza, A.J. & Saunders, M.C. (2002b) Carbaryl resistance in populations of grape berry moth (Lepidoptera: Tortricidae) in New York and Pennsylvania. Journal of Economic Entomology, 95, Oriana (1994) Oriana for Windows, Version Kovach Computing Services, U.K. Pasek, J.E. (1988) Influence of wind and windbreaks on local dispersal of insects. Agriculture, Ecosystems and Environment, 22/23, SAS Institute. (1996) PROC User s Manual, Version 8.0, 5th edn. SAS Institute Inc., Cary, North Carolina. Schowalter, T.D. (2000) Insect Ecology: An Ecosystem Approach. Academic Press, San Diego, California. Schumacher, P., Weyeneth, A., Weber, D.C. & Dorn, S. (1997) Long flights in Cydia pomonella L. (Lepidoptera: Tortricidae) measured by a flight mill: influence of sex, mated status and age. Physiological Entomology, 22, Showers, W.B., Smelser, R.B., Keaster, A.J. et al. (1989) Recapture of marked black cutworm (Lepidoptera: Noctuidae) males after long-range transport. Environmental Entomology, 18, Taschenberg, E.F. & Roelofs, W.L. (1977) Mating disruption of the grape berry moth, Paralobesia viteana, with pheromone released from hollow fibers. Environmental Entomology, 6, Thies, C., Steffan-Dewenter, I. & Tscarntke, T. (2003) Effects of landscape context on herbivory and parasitism at different spatial scales. Oikos, 101, Tobin, P.C., Nagarkatti, S. & Saunders, M.C. (2002) Diapause maintenance and termination in the grape berry moth (Lepidoptera: Tortricidae). Environmental Entomology, 31, Tobin, P.C., Nagarkatti, S. & Saunders, M.C. (2003) Phenology of grape berry moth (Lepidoptera: Tortricidae) in cultivated grape at selected geographic locations. Environmental Entomology, 31, Trimble, R.M. (1993) Efficacy of mating disruption for controlling the grape berry moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae), a case study over three consecutive growing seasons. Canadian Entomologist, 125, 1 9. Trimble, R.M., Vickers, P.M., Nielsen, K.E. & Barinshteyn, G. (2003) Sprayable pheromone for controlling the North American grape berry moth by mating disruption. Agricultural and Forest Entomology, 5,

10 452 N. Botero-Garce s and Rufus Isaacs Weissling, T.J. & Knight, A.L. (1994) Passive trap for monitoring codling moth (Lepidoptera: Tortricidae) flight activity. Journal of Economic Entomology, 87, Wise, J.C., Gut, L.J., Isaacs, R. et al. (2003) Michigan Fruit Management Guide. Extension Bulletin E-154. Michigan State University Extension, East Lansing, Michigan. Witzgall, P., Bengtsson, M. & Trimble, R.M. (2000) Sex pheromone of the grape berry moth (Lepidoptera: Tortricidae). Environmental Entomology, 29, Accepted 13 July 2004