Abstract. Introduction. Greg English-Loeb*, Marc Rhainds*, Tim Martinson* and Todd Ugine*

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1 Agricultural and Forest Entomology (23) 5, Influence of flowering cover crops on Anagrus parasitoids (Hymenoptera: Mymaridae) and Erythroneura leafhoppers (Homoptera: Cicadellidae) in New York vineyards Greg English-Loeb*, Marc Rhainds*, Tim Martinson* and Todd Ugine* *Department of Entomology, Cornell University, New York State Agricultural Experiment Station, Geneva, New York 14456, U.S.A., ygreenhouse and Processing Crops Research Centre, Harrow, Ontario, NOR 1G, Canada, zcornell Cooperative Extension, Finger Lakes Grape Program, Cornell University, County Office Building, Penn Yan, NY 14427, U.S.A. and Department of Entomology, Cornell University, Ithaca, NY 14853, U.S.A. Abstract 1 We tested the hypothesis that providing nectar-producing cover crops will enhance the biological control of grape leafhoppers (Erythroneura spp.) by Anagrus wasps in commercial vineyards in New York, U.S.A. 2 We established three cover crops between vine rows in a commercial vineyard: buckwheat (Fagopyrum esculentum (Moench)), clover (Trifolium repens L.) and mowed sod (Dactylis glomerata L.). 3 There was no effect of cover crop on adult Anagrus in 1996, whereas in 1997 adults were more abundant within edge vines with buckwheat compared to vines with clover or sod; adults were more abundant at the vineyard edge, especially early in the season. 4 Parasitism of sentinel leafhopper eggs was higher on vines with buckwheat compared to parasitism on vines with clover or sod in 1996; a similar, nonsignificant trend, was observed in Neither the abundance nor the distribution of leafhoppers was influenced by cover crops, although in 1997 there was a trend toward greater numbers of nymphs on edge vines with buckwheat. 6 In a cage experiment, parasitism by Anagrus of leafhopper eggs on grapes was greater when adults had access to flowering buckwheat rather than buckwheat without flowers. 7 In a laboratory study, longevity of female Anagrus was increased when provided with honey or sugar water compared to water only or nothing. 8 Our results suggest that parasitism of grape leafhoppers by Anagrus may be enhanced by providing floral resources within vineyards in New York, although it is unclear whether this will produce meaningful reductions in pest abundance. Keywords Conservation biological control, cover crops, egg parasitoid, leafhoppers, Mymaridae, pro-ovigeny. Introduction Conservation of natural enemies in agricultural systems has been recognized for many years as an important component of biological control (Ehler, 1998). Natural enemies can be enhanced by: (1) reducing mortality factors (e.g. modifying Correspondence: G. English-Loeb. Fax: ; gme1@nysaes.cornell.edu pesticide use), (2) providing supplementary resources (e.g. nectar or alternative hosts), and/or (3) providing shelter (e.g. shade or overwintering sites) (Pickett & Bugg, 1998; Landis et al., 2). The egg parasitoid/leafhopper system in vineyards in the western U.S.A. represents one of the better studied systems for conservation of a natural enemy (Anagrus Haliday spp.) (Hymenoptera: Mymaridae) for biological control of an important crop pest (grape leafhopper Erythroneura elagantula Osborn) (Homoptera: # 23 The Royal Entomological Society

2 174 Greg English-Loeb et al. Cicadellidae). In this system conservation efforts have concentrated on either: (1) increasing the supply of non-pest leafhopper eggs as necessary overwintering hosts for wasps (Kido et al., 1984; Murphy et al., 1996, 1998) or (2) providing nectar to adult wasps by planting flowering cover crops in row middles (¼ ground between each row of vines) during the field season (Daane & Costello, 1998; Nicholls et al., 2). Augmenting overwintering hosts by planting prune trees Prunus domestica L. that support populations of the prune leafhopper Edwardsiana prunicola (Edwards) near vineyards increases abundance of Anagrus in the vineyard and parasitism rates of pest leafhoppers (Murphy et al., 1996, 1998). The use of flowering cover crops in vineyards reduces leafhopper populations, but whether this is due to enhanced biological control or reduced vine vigour is under debate (Daane & Costello, 1998). Anagrus spp. are also important natural enemies of grape leafhopper pests in vineyards in the eastern U.S.A. (Williams & Martinson, 2). Several species of Anagrus parasitize several species of Eyrthroneura leafhoppers in New York vineyards (Martinson & Dennehy, 1995; Triapitsyn, 1998). As is true for the western system, wasps overwinter in non-pest leafhopper eggs (several different species using several different plant hosts) outside of the vineyard and then migrate into the vineyard in the spring and summer to attack pest leafhoppers (Corbett & Rosenheim, 1996; Williams & Martinson, 2). Although parasitism levels in New York vineyards can reach high levels (> 9%), this tends not to occur until late in the season. Moreover, parasitism levels early in the season typically are much greater at the edge of a vineyard compared to the interior, suggesting that Anagrus first migrates to vineyard edges and then expands into the vineyard interior over several generations utilizing pest leafhopper eggs (Williams & Martinson, 2). After emerging from grape leafhopper eggs in the laboratory/insectary, adult Anagrus will readily feed on honey before initiating search for hosts (G.E-L., unpublished observations). Other Mymarids (Anaphes sp., Gonatocerus sp.) have been observed visiting flowers, presumably to obtain nectar (Jervis et al., 1993). Studies with egg parasitoids have shown that availability of carbohydrates in the form of sugar, honey or honeydew will enhance adult wasp survival and parasitism (Jervis et al., 1996; Baggen & Gurr, 1998). Hence, we hypothesized that providing nectarproducing cover crops will enhance biological control of grape leafhoppers in New York vineyards. Specifically, we tested the following hypotheses. (1) In comparison with row middles planted with non-nectar producing grasses, the presence of nectar-producing cover crops in row middles of a commercial vineyard will increase abundance of Anagrus adults, encourage colonization of the vineyard interior, elevate parasitism rates of leafhopper eggs on vines and reduce leafhopper densities. (2) The presence of nectar-producing flowers of the cover crop, not just the vegetative portion of the plant, promotes greater parasitism rates of leafhopper eggs. (3) Survival of adult Anagrus will be enhanced when fed sugar water or honey mixed with water relative to water alone or nothing. Materials and methods Field experiments evaluating the impact of ground cover on incidence of Erythroneura leafhoppers and Anagrus parasitoids Field experiments were carried out in a commercial vineyard in the Finger Lakes region near Dresden, New York, in 1996 and The 1.4-ha experimental site consisted of sixty 8-m-long rows spaced 3 m apart, with Vitis vinifera L. Chardonnay vines planted 2 m apart in each row. Rows ran perpendicularly to a woodlot located on the south edge of the experimental site. Experimental units, consisting of five contiguous 8-m-long rows, were assigned to one of the following ground cover treatments: (1) sod (primarily orchardgrass, Dactylis glomerata L.), already established in the experimental site, served as a control, and was mowed when it reached.5 m; (2) buckwheat Fagopyrum esculentum (Moench) was seeded between rows of vines in late May of 1996 and 1997; and (3) ladino clover Trifolium repens L. was planted between rows of vines in late May of 1996, and remained established through the 1997 season. Experiments were replicated four times, using a completely randomized block design. In 1997, a prebloom application of carbaryl (Sevin 1 5W at label rate) was inadvertently sprayed in two replicates, and data from these two replicates were excluded from analyses. Experiments were terminated earlier than anticipated in 1997 because the entire vineyard was treated with carbaryl in early August to control potato leafhoppers Empoasca fabae Harris. The following data were collected. (1) Density of adult leafhoppers and parasitoids was monitored with yellow sticky traps suspended on the low canopy wire adjacent to the fruit zone of vines, using 1 traps spaced 8 m apart in the centre row of each experimental unit. Traps were replaced every 4 7 days (28 May to 14 August 1996, 9 June to 21 July 1997), and the number of adults on each trap recorded. (2) Density of leafhopper nymphs was assessed by sampling five leaves of two shoots on vines spaced 8 m apart in the centre row of each experimental unit (four times between 1 July and 13 August in 1996; twice on 7 and 17 July in 1997). (3) Parasitism by Anagrus females was assessed with sentinel leafhopper eggs. Sentinel eggs were established by confining field-collected leafhoppers (E. bistrata McAtee and E. vitifex Fitch complex, referred to as E. bistrata hereafter) into clip cages (4 cm in diameter) placed onto one leaf of a vine for 2 days (Williams & Martinson, 2), thereby providing an even-aged cohort of susceptible hosts of roughly the same density at all sample sites. One batch of sentinel eggs was established every 8 m along the central row of each experimental unit. After 3 weeks of field exposure, sentinel eggs were categorized as parasitized or non-parasitized (Wells et al., 1988; Williams & Martinson, 2). Parasitism, using the sentinel egg method, was measured twice in 1996 (mid-june and mid-august) and once in 1997 (early July). To assess the impact of spatial location on incidence of leafhoppers and parasitoids, sampling sites along rows were classified as either near the edge or in the interior of the vineyard (< 4 m or > 4 m from the first vine bordering the woodlot).

3 Cover crop and parasitism of leafhopper eggs 175 Greenhouse experiment evaluating the impact of flowering plants on rate of parasitism by female Anagrus Ten wood-framed cages (.8 m.5 m.5 m) with sleeved entrance holes, glass top and screened sides were assigned to one of two treatments: potted flowering buckwheat with flowers intact, or with flowers removed. Each cage contained a potted Vitis riparia Michaux plant on which adult E. bistrata were confined for 3 days in clip cages placed onto two leaves, the second leaf timed to be ready for parasitism 3 days after the first one. Grape leaves from a commercial V. vinifera vineyard were used as a source for Anagrus adults in this experiment. To collect adult wasps, leaves, with many parasitized leafhopper eggs, were enclosed inside a 3.8-litre cylindrical paper carton. A clear glass vial (2 ml) was secured at the top of the carton to allow light to enter and attract newly emerged wasps. New vials were placed on rearing cartons 1 day prior to the Anagrus release date. On the release date, vials were brought to the laboratory where the wasps were sexed using a dissecting scope. On the same day, 1 females and 2 3 males were released into each cage. One day later, the clip cage containing the first batch of leafhopper eggs was removed. Female leafhoppers were then confined in a clip cage placed onto a second leaf of the same V. riparia vine for 3 days, after which the clip cage was removed exposing the second batch of eggs. At the same time, the first batch of eggs was covered with a clip cage to prevent further parasitism. To provide equal access to water, all cages were misted once a day and contained vials of water with a cotton wick. After each batch of eggs had been exposed for 3 days, the vines were moved to a different greenhouse and the rate of parasitism was evaluated by recording emergence of adult Anagrus and leafhoppers after about 21 days. The experiment was replicated twice, approximately 2 weeks apart in August 1997, corresponding to a total of 1 replicates. Tube experiment evaluating the impact of various food sources on longevity of female Anagrus In a laboratory study conducted in August 1998, we assessed longevity of newly emerged adult female Anagrus provided with the following food resources: nothing, distilled water, honey solution (1 : 1 with water) and sucrose solution (1% by weight). Wasps were obtained from grape leaves collected from a commercial vineyard ( Niagara, a cultivar of V. labrusca L.) in the Finger Lakes region of upstate New York. Adult Anagrus was collected as described for cage experiments, sexed, and transferred, using a fine brush, into small chambers drilled into a rectangular block made from acrylic plastic (Plexiglas). CO 2 gas was used prior to transfer to immobilize wasps. After placing a wasp in a chamber, the hole was covered with a glass slide to prevent escape. Food was provided using a small glass tube fashioned from a glass pipette stretched thin after heating in a flame. The tube entered the Plexiglas chamber from the side through a small hole. Gaps were sealed using modelling clay. Liquid food was wicked from a holding container into the tube where it flowed to the tip by capillary action. Wasps were observed feeding on liquid at the tip of the tube within the enclosure. The no food treatment also included a tube, which was plugged with modelling clay to prevent wasps from exiting the chamber. We inspected chambers each day and recorded whether the wasps were alive, dead or missing. A total of 4 female wasps were evaluated (1 per food treatment), although four were either missing or dead at the start of the experiment and were not included in the analysis. Statistical analyses Statistical analyses were conducted using SAS statistical package (SAS Institute, 1988). Factorial ANOVA was used to evaluate the impact of sampling date, vineyard location (edge or interior), and ground cover treatment on number of adult leafhoppers and parasitoids per sticky cardboard, number of leafhopper nymphs per leaf, and proportion of leafhopper eggs parasitized; different analyses were conducted in 1996 and 1997 because experiments were not carried out on the same date each year. Factorial ANOVA was used to evaluate the impact of buckwheat flowers and timing of exposure of leafhopper eggs (first or second batch of eggs) on proportion of parasitized eggs. Longevity of female Anagrus provided with either nothing, water, sugar solution or honey solution was compared using one-way ANOVA followed by Student Newman Keuls test. Whenever necessary, data were subjected to square-root, arcsine or rank transformations to reduce heterogeneity of variance. Results Effects of cover crops on densities of Anagrus parasitoids Number of adult parasitoids captured in yellow sticky cardboards varied between sampling dates in both 1996 and 1997, although temporal fluctuations of population density exhibited distinct patterns each year (Fig. 1). In 1996, captures of parasitoids suggested two generations, with a first peak of about four adults per trap in mid June and a second peak of about two adults per trap in early July (Fig. 1). Densities of parasitoids were much higher in 1997 than in 1996, and during that year steadily increased between mid June to early July, and decreased thereafter (Fig. 1). Adult parasitoids were more abundant near the edge rather than in the interior of the vineyard in both 1996 and 1997, but a significant interaction between sampling date and vineyard location in 1996 indicated that adult parasitoids were more abundant near the edge of the vineyard early but not late during the season (Fig. 1). A significant interaction between vineyard location and ground cover in 1997 indicated higher abundance of adult parasitoids in plots with buckwheat near the edge but not in the interior of the vineyard (Fig. 1). Rate of parasitism of sentinel eggs was much lower in 1996 than in 1997 (Fig. 2). The significant interaction

4 176 Greg English-Loeb et al. buckwheat clover control Edge Interior Number of parasitoids per trap (x +/ SE) Julian date Figure 1 Impact of ground cover and vineyard location on number of adult Anagrus parasitoids captured in yellow sticky traps in 1996 and Data were analysed using factorial ANOVA, with sampling date, ground cover and vineyard location treated as fixed factors, and replicate as a random factor. Significance levels were as follows: P (date) ¼.1 in 1996 and.66 in 1997; P (location) ¼.47 in 1996 and.17 in 1997; P (cover) ¼.716 in 1996 and.271 in 1997; P (date location) ¼.18 in 1996 and.93 in 1997; P (date cover) ¼.446 in 1996 and.52 in 1997; P (cover location) ¼.188 in 1996 and.4 in 1997; P (date location cover) ¼.927 in 1996 and.464 in Data were subjected to square-root transformation to reduce heterogeneity of variance. between sampling date and ground cover in 1996 indicated a higher rate of parasitism in plots with buckwheat late but not early during the season (Fig. 2). Rate of parasitism was also higher in plots with buckwheat in 1997, but the impact of ground cover was not significant (Fig. 2), possibly because the experiment was not repeated through time and used only two replicates. Rate of parasitism was consistently higher near the edge rather than in the interior of the vineyard in both 1996 and 1997, although neither the impact of vineyard location nor the interaction between vineyard location and sampling date were significant (Fig. 2). Effect of cover crops on densities of Erythroneura leafhoppers Number of adult leafhoppers captured in yellow sticky cardboards varied significantly between sampling dates in both 1996 and 1997, although temporal fluctuations of population density greatly differed in both years (Fig. 3). In 1996, captures of leafhoppers suggested two generations, with a first peak of about 1 adults per trap in early July, and a second peak of about 2 adults per trap in early August (Fig. 3). Densities of leafhoppers were much higher Proportion of parasitized eggs (+ SE).7.35 Edge 15 June 4 August 4 July buckwheat clover control Interior 15 June 4 August 4 July Figure 2 Impact of ground cover and vineyard location on proportion of leafhopper eggs parasitized by Anagrus adults in 1996 and Data were analysed using factorial ANOVA, with sampling date, ground cover and vineyard location treated as fixed factors, and replicate as a random factor; because the experiment was not repeated through time in 1997, the impact of time could not be evaluated. Significance levels were as follows: P (date) ¼.874 in 1996; P (location) ¼.273 in 1996 and.249 in 1997; P (cover) ¼.484 in 1996 and.461 in 1997; P (date location) ¼.687 in 1996; P (date cover) ¼.15 in 1996; P (cover location) ¼.279 in 1996 and.888 in 1997; P (date location cover) ¼.491 in Data were subjected to arcsine transformation to reduce heterogeneity of variance.

5 Cover crop and parasitism of leafhopper eggs 177 in 1997 than in 1996, and during that year steadily declined from about 5 to 4 adults per trap between mid June and late July (Fig. 3). A significant interaction between sampling date and vineyard location in 1996 indicated that adult leafhoppers were more abundant near the edge rather than in the interior of the vineyard early but not late during the season (Fig. 3). Densities of nymphs were low in 1996 (fewer than two per five leaves) and were not significantly affected by sampling date, vineyard location, ground cover or the interaction between these parameters (Fig. 4). In 1997, densities of nymphs were relatively high and declined from about five to two nymphs per five leaves between mid to late July (Fig. 4). Densities of nymphs were significantly higher near the edge than in the interior of the vineyard, although the marginally significant interactions between sampling date and vineyard location (P ¼.14) and between sampling date and ground cover (P ¼.77) suggested that the impact of vineyard location was mostly due to high abundance of nymphs in plots with buckwheat early during the season (Fig. 4). Impact of various food sources on rate of parasitism and longevity of Anagrus The cage experiment conducted in a greenhouse environment indicated that the presence of buckwheat flowers significantly increased the proportion of parasitized leafhopper eggs; the rate of parasitism did not differ for the first or second batch of eggs (Fig. 5). Longevity of adult parasitoids confined in chambers and provided with nothing or water was extremely low (< 1 day) (Fig. 6). Providing adult parasitoids with a solution of either sugar or honey significantly increased their longevity (Fig. 6). Discussion Pro-ovigenic Anagrus wasps emerge as adults with a full complement of eggs (Jervis et al., 21), and do not require protein resources to develop additional eggs, although adults may still require food to provide the energy to search for and parasitize eggs (Jervis et al., 1996). This food can come in several forms, but nectar from flowers or extrafloral nectaries or honeydew are the most likely sources (Jervis et al., 1993; Jervis et al., 1996). Although variable, our results from field, greenhouse and laboratory experiments all support the conclusion that nectar from flowers increases survival and/or effectiveness of Anagrus in the New York grape system. In the field during 1997, we observed increased abundance of adult wasps in the canopy of vines with flowering buckwheat planted in the row middles, at least at the edge of the vineyard; otherwise, yellow sticky trap captures of adult wasps did not indicate a strong cover crop effect (Fig. 1). Parasitism rates of sentinel leafhopper eggs, however, were higher during mid-summer in 1996 on edge vines with buckwheat (Fig. 2). The same trend was apparent in 1997 with mean proportion of eggs parasitized over 5% for vines associated with buckwheat and buckwheat clover control 3 Edge 1996 Interior Figure 3 Impact of ground cover and vineyard location on number of adult Erythroneura leafhoppers captured in yellow sticky traps in 1996 and Data were analysed using factorial ANOVA, with sampling date, ground cover and vineyard location treated as fixed factors, and replicate as a random factor. Significance levels were as follows: P (date) ¼.1 in 1996 and.11 in 1997; P (location) ¼.197 in 1996 and.592 in 1997; P (cover) ¼.356 in 1996 and.42 in 1997; P (date location) ¼.1 in 1996 and.842 in 1997; P (date cover) ¼.841 in 1996 and.89 in 1997; P (cover location) ¼.71 in 1996 and.293 in 1997; P (date location cover) ¼.874 in 1996 and.169 in Data were subjected to square-root transformation to reduce heterogeneity of variance. Number of leafhoppers per trap (x +/ SE) Julian date

6 178 Greg English-Loeb et al. buckwheat clover control Number of nymphs per 5 leaves (x +/ SE) Edge Interior Julian date Figure 4 Impact of ground cover and vineyard location on number of nymph Erythroneura leafhoppers sampled on leaves of vine plants in 1996 and Data were analysed using factorial ANOVA, with sampling date, ground cover and vineyard location treated as fixed factors, and replicate as a random factor. Significance levels were as follows: P (date) ¼.22 in 1996 and.43 in 1997; P (location) ¼.347 in 1996 and.19 in 1997; P (cover) ¼.871 in 1996 and.143 in 1997; P (date location) ¼.467 in 1996 and.14 in 1997; P (date cover) ¼.196 in 1996 and.77 in 1997; P (cover location) ¼.874 in 1996 and.473 in 1997; P (date location cover) ¼.573 in 1996 and.679 in Data were subjected to square-root transformation to reduce heterogeneity of variance. about 3% for vines with sod in the row middles; however, we had low statistical power in 1997 (two replicates out of the four were sprayed with insecticide early in the season) and these differences were not statistically significant (Fig. 2). In the greenhouse cage experiment, having access to flowers of buckwheat (as compared to only the vegetative part of the plant) resulted in higher parasitism rate of sentinel leafhopper eggs (Fig. 5). Finally, the laboratory feeding trial showed that access to sugar or honey greatly increased survival of adult wasps compared to access to water alone (Fig. 6). Taken together, these results indicate that having access to a sugar source increases the potential impact of Anagrus on grape leafhopper. As has been observed previously in New York vineyards (Williams & Martinson, 2), abundance and activity of Anagrus were generally greater on the edge of the vineyard than in the interior, especially early in the season (Figs 1 and 2). This was especially true for sticky card trap captures during 1996 and 1997 (Fig. 1). The effect of location was less apparent for parasitism of sentinel eggs, although mean rates were generally greater on the edge than in the interior (Fig. 2). In California, early colonization of vineyards by Anagrus increases the probability of successful biological control of leafhoppers in vineyards (Murphy et al., 1998). We had hypothesized that flowering cover crops would promote more rapid and earlier colonization of the interior of New York vineyards, but did not find any strong support for this hypothesis; on the contrary, the interaction between cover crop and location for sticky trap captures of adult wasps in 1997 was in the opposite direction as predicted (Fig. 1). It is well known that flowering plants are not equal in their suitability as food resources for different species of parasitoids (Jervis et al., 1996; Patt et al., 1997). For example, flower shape can have a large effect on accessibility of nectar. In our field trial, wasps responded to the presence of buckwheat in row middles but not of clover (Figs 1 and 2). Two factors may have limited the effect of clover on Anagrus. First, as a perennial, it takes a full season to become well established. Indeed, there were virtually no flowers in the clover in 1996 and its not too surprising there was no difference between clover and sod. The clover did become well established by 1997 and flowered, but it did not affect the abundance and activity of Anagrus; because of low statistical power, however, it is difficult to draw any definitive conclusions from our results in Nevertheless, it may be true that buckwheat flowers are particularly well suited as a nectar source for small hymenopteran parasitoids. Buckwheat flowers are small and have readily accessible nectaries (Lovei et al., 1993). In addition, buckwheat reached the flowering stage rapidly in New York State (under 6 weeks after seeds planted) and produced copious flowers. Other researches have found buckwheat to be a good food resource for parasitoid wasps and flies (Bugg & Dutcher, 1989; Stephens et al., 1998). On the other hand, clover flowers are adapted for bee pollination and, seemingly, wasps have difficulty obtaining nectar rewards. In the extensive survey of flower-visiting by hymenopteran parasitoids conducted by Jervis et al. (1993), no parasitoids were observed exploiting clover flowers. As mentioned previously, Anagrus wasps reared from grape leafhopper eggs readily feed on a sugar solution before searching for eggs (G.E.L., unpublished observations). Feeding on such a carbohydrate source will not increase potential fecundity of the female wasp since she is pro-ovigenic. However, our data show that having access to a carbohydrate source will increase female longevity. In addition, an abundant supply of nectar-producing flowers

7 Cover crop and parasitism of leafhopper eggs 179 Proportion of parasitized eggs (x + SE).6.3 First flowers no flowers Batch of eggs Second Figure 5 Proportion of leafhopper eggs parasitized by Anagrus adults in the presence or absence of buckwheat flowers. Adult parasitoids were subjected to two batches of eggs, the first one when they were 2 4 days old and the second one when they were 5 7 days old. Data were analysed using factorial ANOVA, treating flower treatment and age of parasitoid as fixed factors, and replicate as a blocking factor. Significance levels were as follows: P (flower) ¼.55; P (age) ¼.265; P (flower age) ¼.282. Data were subjected to arcsine transformation to reduce heterogeneity of variance. in proximity to leafhopper eggs should reduce the time needed to obtain energy and proportionally increase the time available to find and parasitize host eggs. The cage experiment supports this idea since we did find elevated parasitism of sentinel leafhopper eggs in cages with buckwheat flowers present compared to cages with buckwheat flowers removed. Interestingly, though, we did not find any strong evidence that the length of time of oviposition was extended when the wasps had access to nectar (Fig. 5). If this were the case, we might expect a greater difference in parasitism levels between cages with and without flowers for old rather than young females. Instead, we did not observe a time effect. It may be true that longevity is increased by having nectar, but the time period for oviposition is not increased to as great an extent (see Baggen & Gurr, 1998). More work is required, however, before firm conclusions can be drawn about Anagrus. In a survey of Anagrus reared from leafhopper eggs collected from commercial vineyards in New York, six different species have been identified. The three most common were: A. daanaei S. Triapitsyn, A. erythroneurae S. Triapitsyn and Chiappini, and A. tretiakovae S. Triapitsyn (Williams & Martinson, 2). Anagrus erythroneurae was predominantly reared from leafhoppers attacking V. vinifera whereas A. daanaei and A. tretiakovae were Longevity (days) (x + SE) 1 5 B Air reared from leafhopper species that attack a number of different grape species and their hybrids. In this study we did not attempt to distinguish among the different species of Anagrus and it is probable that our experiments involved several different species. This may, in part, explain the relatively large amount of variation in the results we obtained. It is possible, for example, that some species of Anagrus readily feed on nectar or other sugar sources while others do not. The ultimate test of the success of a biological control programme is whether it leads to a reduction in pest pressure. Leafhoppers were relatively rare in 1996 and we did not find any large effects of cover crop (Figs 3 and 4). Leafhoppers were more abundant in 1997 compared to 1996 but we still did not find a significant effect of cover on leafhopper adults (Figs 3 and 4). Nymphs were similarly not strongly influenced by cover crop although there was a marginally significant interaction between cover and location in 1997 based on higher numbers of nymphs on grapes at the edge of the vineyard where buckwheat was planted (Fig. 4). There were also significantly more adult Anagrus captured in the vine canopy in that region of the vineyard in that year (Fig. 1), possibly indicating a numerical response of parasitoids to increased density of leafhoppers. However, overall, we did not see any major effects of cover on pest leafhoppers and certainly no reductions in density and, therefore, presumably damage. Hence, for the two years of our field study, although buckwheat had some measurable positive impact on Anagrus, this did not translate into a major decline in pest populations. There are several possible reasons for this. First, an increase in egg mortality due to Anagrus may have been compensated for by a decrease in mortality from other sources. Second, 1996 was when we found the largest significant impact of buckwheat on parasitism rates of sentinel eggs, and this was a year of very low leafhopper densities in the vineyard (Figs 2 and 3). It may have been that densities were too low overall to detect an effect on leafhoppers. In 1997, when leafhopper densities were higher, we only had two replicates of each cover crop treatment, which makes it difficult to draw strong conclusions. B Water A Honey solution A Sugar solution Figure 6 Longevity of adult Anagrus parasitoids provided with different food sources. One-way ANOVA indicated significant differences between food sources (F ¼ 52.67; d.f. ¼ 3,33; P <.1). Bars superscripted by the same letter are not statistically significant (Student Newman Keuls test, P <.5).

8 18 Greg English-Loeb et al. In California vineyard systems, cover crops have been shown to reduce pest leafhopper populations, although the reasons for this are not clear. In an unreplicated vineyard trial, Nicholls et al. (2) found lower densities of leafhoppers on leaves within a block of grapes that also included summer cover crops of buckwheat and sunflower Helianthus annus L. compared to a matched block of grapes in which row middles were kept free of vegetation. However, they did not find higher egg parasitism rates from Anagrus in the vineyard with flowering cover crops. The authors suggest that increased numbers of generalist predators such as spiders may be responsible for the differences in leafhopper numbers. Daane & Costello (1998) also compared abundance of leafhoppers, Anagrus, and generalist predators between California vineyards with and without cover crops in a replicated experiment. They found lower leafhopper densities in vineyards with cover crops. They considered three hypotheses to explain the reduced numbers: increased spider abundance, increased parasitism by Anagrus, or reduced vine vigour due to competition with cover crops. Of the three, they found the best support for the third hypothesis, noting that grape leafhoppers prefer vigorously growing vines (Daane et al., 1995). In some cases they did find higher parasitism rates in vineyards with cover crops, but this was inconsistent and appeared to be related to having fewer leafhopper eggs to parasitize due to low vine vigour. Overall, our results indicate Anagrus species that parasitize leafhopper pests of grapes in New York will feed on nectar produced by cover crops, such as buckwheat, which may promote increased adult survival and parasitism of leafhopper eggs in the field. However, the response of Anagrus was variable and, moreover, we did not see any reduction in leafhopper abundance. Hence, although there are a number of potential benefits to using flowering cover crops (Bugg & Waddington, 1994), our data do not strongly support enhanced biological control of leafhoppers by Anagrus as one benefit for New York vineyards. Larger trials with greater replication may ultimately prove otherwise. However, conservation biological control efforts for New York vineyards may be better served by exploring ways of creating overwintering refuges for Anagrus near vineyards as has been done in the California system (Kido et al., 1984; Murphy et al., 1996, 1998). Acknowledgements This research was supported by funds from the New York Grape Production Fund, USDA Viticultural Consortium, and the New York Wine and Grape Foundation. We gratefully acknowledge B. Dick, A. Gillespi, S. Hesler, K. Kunz and C. Marion for assistance with field and laboratory experiments. A big thank you to D. Miles for letting us conduct our field experiment in his vineyard and helping us establish and maintain cover crops and R. Figel for allowing us to collect leafhoppers and Anagrus from his vineyard. K. Daane and M. Jervis provided many useful suggestions for improving the original manuscript. References Baggen, L.R. & Gurr, G.M. (1998) The influence of food on Copidosoma koehleri (Hymenoptera: Encyrtidae), and the use of flowering plants as a habitat management tool to enhance biological control of potato moth, Phthorimaea operculella (Lepidoptera: Gelechiidae). Biological Control, 11, Bugg, R.L. & Dutcher, J.D. (1989) Warm-season cover crops for pecan orchards: horticultural and entomological implications. Biological Agriculture and Horticulture, 6, Bugg, R.L. & Waddington, C. (1994) Using cover crops to manage arthropod pests of orchards: a review. Agricultural Ecosystems and Environment, 5, Corbett, A. & Rosenheim, J.A. 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9 Cover crop and parasitism of leafhopper eggs 181 Pickett, C.H. & Bugg, R.L. (1998) Enhancing Biology Control: Habitat Management to Promote Natural Enemies of Agricultural Pests. University of California Press, Berkeley. SAS Institute. (1988) SAS/STAT User s Guide, Release 6.3. SAS Institute, Cary, NC. Stephens, M.J., France, C.M., Wratten, S.D. & Frampton, C. (1998) Enhancing biological control of leafrollers (Lepidoptera: Torticidae) by sowing buckwheat (Fagopyrum esculentum) in an orchard. Biocontrol Science and Technology, 8, Triapitsyn, S.V. (1998) Anagrus (Hymenoptera: Mymaridae) egg parasitoids of Erythroneura spp. & other leafhoppers (Homoptera: Cicadellidae) in north america vineyards and orchards: a taxonomic review. Transactions of the American Entomological Society, 124, Wells, J.D., Cone, W.W. & Conant, M.M. (1988) Chemical and biological control of Erythroneura leafhoppers on Vitis vinifera in southcentral Washington. Journal of the Entomological Society of British Columbia, 85, Williams, L. III & Martinson, T.E. (2) Colonization of new york vineyards by Anagrus spp. (Hymenoptera: Mymaridae): overwintering biology, within-vineyard distribution of wasps, and parasitism of grape leafhopper, Erythroneura spp. (Homoptera: Cicadellidae), eggs. Biological Control, 18, Accepted 3 November 22

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