Agricultural and Forest Entomology (2003) 5, 173–181

Influence of flowering cover crops on parasitoids (: Mymaridae) and Erythroneura (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 1G0, 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’ eggs was higher on vines with buckwheat compared to parasitism on vines with clover or sod in 1996; a similar, non- significant trend, was observed in 1997. 5 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 pro- vided 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, leaf- hoppers, Mymaridae, pro-ovigeny.

Introduction Conservation of natural enemies in agricultural systems has pesticide use), (2) providing supplementary resources been recognized for many years as an important component (e.g. nectar or alternative hosts), and/or (3) providing shel- of biological control (Ehler, 1998). Natural enemies can be ter (e.g. shade or overwintering sites) (Pickett & Bugg, 1998; enhanced by: (1) reducing mortality factors (e.g. modifying Landis et al., 2000). 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) Correspondence: G. English-Loeb. Fax: 315 787 2326; e-mail: for biological control of an important crop pest (grape [email protected] leafhopper Erythroneura elagantula Osborn) (Homoptera:

# 2003 The Royal Entomological Society 174 Greg English-Loeb et al.

Cicadellidae). In this system conservation efforts have Materials and methods concentrated on either: (1) increasing the supply of non-pest leafhopper eggs as necessary overwintering Field experiments evaluating the impact of ground hosts for wasps (Kido et al., 1984; Murphy et al., 1996, cover on incidence of Erythroneura leafhoppers and 1998) or (2) providing nectar to adult wasps by planting Anagrus parasitoids flowering cover crops in row middles (¼ ground between each row of vines) during the field season (Daane & Field experiments were carried out in a commercial vineyard in Costello, 1998; Nicholls et al., 2000). Augmenting over- the Finger Lakes region near Dresden, New York, in 1996 and wintering hosts by planting prune trees Prunus domestica L. 1997. The 1.4-ha experimental site consisted of sixty 80-m-long that support populations of the prune leafhopper rows spaced 3 m apart, with Vitis vinifera L. ‘Chardonnay’ vines Edwardsiana prunicola (Edwards) near vineyards increases planted 2 m apart in each row. Rows ran perpendicularly to a abundance of Anagrus in the vineyard and parasitism rates woodlot located on the south edge of the experimental site. of pest leafhoppers (Murphy et al., 1996, 1998). The use of Experimental units, consisting of five contiguous 80-m-long flowering cover crops in vineyards reduces leafhopper rows, were assigned to one of the following ground cover treat- populations, but whether this is due to enhanced biological ments: (1) sod (primarily orchardgrass, Dactylis glomerata L.), control or reduced vine vigour is under debate (Daane & already established in the experimental site, served as a control, Costello, 1998). and was mowed when it reached 0.5 m; (2) buckwheat Fago- Anagrus spp. are also important natural enemies of grape pyrum esculentum (Moench) was seeded between rows of vines leafhopper pests in vineyards in the eastern U.S.A. in late May of 1996 and 1997; and (3) ladino clover Trifolium (Williams & Martinson, 2000). Several species of Anagrus repens L. was planted between rows of vines in late May of parasitize several species of Eyrthroneura leafhoppers in 1996, and remained established through the 1997 season. New York vineyards (Martinson & Dennehy, 1995; Experiments were replicated four times, using a completely Triapitsyn, 1998). As is true for the western system, wasps randomized block design. In 1997, a prebloom application of overwinter in non-pest leafhopper eggs (several different carbaryl (Sevin1 50W at label rate) was inadvertently sprayed species using several different plant hosts) outside of the in two replicates, and data from these two replicates were vineyard and then migrate into the vineyard in the spring excluded from analyses. Experiments were terminated earlier and summer to attack pest leafhoppers (Corbett & Rosenheim, than anticipated in 1997 because the entire vineyard was treated 1996; Williams & Martinson, 2000). Although parasitism levels with carbaryl in early August to control potato leafhoppers in New York vineyards can reach high levels (> 90%), this Empoasca fabae Harris. tends not to occur until late in the season. Moreover, parasitism The following data were collected. (1) Density of adult levels early in the season typically are much greater at the edge leafhoppers and parasitoids was monitored with yellow of a vineyard compared to the interior, suggesting that Anagrus sticky traps suspended on the low canopy wire adjacent to first migrates to vineyard edges and then expands into the the fruit zone of vines, using 10 traps spaced 8 m apart in the vineyard interior over several generations utilizing pest centre row of each experimental unit. Traps were replaced leafhopper eggs (Williams & Martinson, 2000). every 4–7 days (28 May to 14 August 1996, 9 June to 21 July After emerging from grape leafhopper eggs in the labora- 1997), and the number of adults on each trap recorded. (2) tory/insectary, adult Anagrus will readily feed on honey Density of leafhopper nymphs was assessed by sampling before initiating search for hosts (G.E-L., unpublished five leaves of two shoots on vines spaced 8 m apart in the observations). Other Mymarids (Anaphes sp., Gonatocerus centre row of each experimental unit (four times between 1 sp.) have been observed visiting flowers, presumably to July and 13 August in 1996; twice on 7 and 17 July in 1997). obtain nectar (Jervis et al., 1993). Studies with egg parasit- (3) Parasitism by Anagrus females was assessed with ‘senti- oids have shown that availability of carbohydrates in the nel’ leafhopper eggs. Sentinel eggs were established by form of sugar, honey or honeydew will enhance adult wasp confining field-collected leafhoppers (E. bistrata McAtee survival and parasitism (Jervis et al., 1996; Baggen & Gurr, and E. vitifex Fitch complex, referred to as E. bistrata here- 1998). Hence, we hypothesized that providing nectar- after) into clip cages (4 cm in diameter) placed onto one leaf producing cover crops will enhance biological control of of a vine for 2 days (Williams & Martinson, 2000), thereby grape leafhoppers in New York vineyards. Specifically, we providing an even-aged cohort of susceptible hosts of tested the following hypotheses. (1) In comparison with row roughly the same density at all sample sites. One batch of middles planted with non-nectar producing grasses, the sentinel eggs was established every 8 m along the central presence of nectar-producing cover crops in row middles row of each experimental unit. After 3 weeks of field of a commercial vineyard will increase abundance of exposure, sentinel eggs were categorized as parasitized or Anagrus adults, encourage colonization of the vineyard non-parasitized (Wells et al., 1988; Williams & Martinson, interior, elevate parasitism rates of leafhopper eggs on 2000). Parasitism, using the sentinel egg method, was meas- vines and reduce leafhopper densities. (2) The presence of ured twice in 1996 (mid-June and mid-August) and once in nectar-producing flowers of the cover crop, not just the 1997 (early July). To assess the impact of spatial location on vegetative portion of the plant, promotes greater parasitism incidence of leafhoppers and parasitoids, sampling sites rates of leafhopper eggs. (3) Survival of adult Anagrus will along rows were classified as either near the edge or in the be enhanced when fed sugar water or honey mixed with interior of the vineyard (< 40 m or > 40 m from the first vine water relative to water alone or nothing. bordering the woodlot).

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Greenhouse experiment evaluating the impact of sealed using modelling clay. Liquid food was wicked from flowering plants on rate of parasitism by female a holding container into the tube where it flowed to the tip Anagrus by capillary action. Wasps were observed feeding on liquid at the tip of the tube within the enclosure. The no food Ten wood-framed cages (0.8 m 0.5 m 0.5 m) with sleeved treatment also included a tube, which was plugged with entrance holes, glass top and screened sides were assigned to modelling clay to prevent wasps from exiting the chamber. one of two treatments: potted flowering buckwheat with We inspected chambers each day and recorded whether the flowers intact, or with flowers removed. Each cage wasps were alive, dead or missing. A total of 40 female contained a potted Vitis riparia Michaux plant on which wasps were evaluated (10 per food treatment), although adult E. bistrata were confined for 3 days in clip cages four were either missing or dead at the start of the experi- placed onto two leaves, the second leaf timed to be ready ment and were not included in the analysis. 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, Statistical analyses leaves, with many parasitized leafhopper eggs, were Statistical analyses were conducted using SAS statistical enclosed inside a 3.8-litre cylindrical paper carton. A clear package (SAS Institute, 1988). Factorial ANOVA was used glass vial (20 mL) was secured at the top of the carton to to evaluate the impact of sampling date, vineyard location allow light to enter and attract newly emerged wasps. New (edge or interior), and ground cover treatment on number vials were placed on rearing cartons 1 day prior to the of adult leafhoppers and parasitoids per sticky cardboard, Anagrus release date. On the release date, vials were number of leafhopper nymphs per leaf, and proportion of brought to the laboratory where the wasps were sexed leafhopper eggs parasitized; different analyses were con- using a dissecting scope. On the same day, 10 females and ducted in 1996 and 1997 because experiments were not 2–3 males were released into each cage. One day later, the carried out on the same date each year. Factorial ANOVA clip cage containing the first batch of leafhopper eggs was was used to evaluate the impact of buckwheat flowers and removed. Female leafhoppers were then confined in a clip timing of exposure of leafhopper eggs (first or second batch cage placed onto a second leaf of the same V. riparia vine of eggs) on proportion of parasitized eggs. Longevity of for 3 days, after which the clip cage was removed exposing female Anagrus provided with either nothing, water, sugar the second batch of eggs. At the same time, the first batch of solution or honey solution was compared using one-way eggs was covered with a clip cage to prevent further para- ANOVA followed by Student–Newman–Keuls test. Whenever sitism. To provide equal access to water, all cages were necessary, data were subjected to square-root, arcsine or misted once a day and contained vials of water with a rank transformations to reduce heterogeneity of variance. 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 Results emergence of adult Anagrus and leafhoppers after about 21 days. The experiment was replicated twice, approxi- Effects of cover crops on densities of Anagrus mately 2 weeks apart in August 1997, corresponding to parasitoids a total of 10 replicates. Number of adult parasitoids captured in yellow sticky cardboards varied between sampling dates in both 1996 and 1997, although temporal fluctuations of population Tube experiment evaluating the impact of various density exhibited distinct patterns each year (Fig. 1). In food sources on longevity of female Anagrus 1996, captures of parasitoids suggested two generations, In a laboratory study conducted in August 1998, we with a first peak of about four adults per trap in mid June assessed longevity of newly emerged adult female Anagrus and a second peak of about two adults per trap in early July provided with the following food resources: nothing, (Fig. 1). Densities of parasitoids were much higher in 1997 distilled water, honey solution (1 : 1 with water) and sucrose than in 1996, and during that year steadily increased solution (10% by weight). Wasps were obtained from grape between mid June to early July, and decreased thereafter leaves collected from a commercial vineyard (‘Niagara’, (Fig. 1). Adult parasitoids were more abundant near the a cultivar of V. labrusca L.) in the Finger Lakes region of edge rather than in the interior of the vineyard in both upstate New York. Adult Anagrus was collected as 1996 and 1997, but a significant interaction between described for cage experiments, sexed, and transferred, sampling date and vineyard location in 1996 indicated that using a fine brush, into small chambers drilled into a rect- adult parasitoids were more abundant near the edge of the angular block made from acrylic plastic (Plexiglas). CO2 gas vineyard early but not late during the season (Fig. 1). was used prior to transfer to immobilize wasps. After A significant interaction between vineyard location and placing a wasp in a chamber, the hole was covered with ground cover in 1997 indicated higher abundance of adult a glass slide to prevent escape. Food was provided using a parasitoids in plots with buckwheat near the edge but not in small glass tube fashioned from a glass pipette stretched the interior of the vineyard (Fig. 1). thin after heating in a flame. The tube entered the ‘Plexiglas’ Rate of parasitism of sentinel eggs was much lower in chamber from the side through a small hole. Gaps were 1996 than in 1997 (Fig. 2). The significant interaction

# 2003 The Royal Entomological Society, Agricultural and Forest Entomology, 5, 173–181 176 Greg English-Loeb et al.

buckwheat clover control

Edge Interior 6 1996

3 SE)

+/–

Figure 1 Impact of ground cover and vine- yard location on number of adult Anagrus 0 parasitoids captured in yellow sticky traps in 1996 and 1997. Data were analysed using factorial ANOVA, with sampling date, ground 48 1997 cover and vineyard location treated as fixed factors, and replicate as a random factor. Significance levels were as follows: P (date) ¼ 0.0001 in 1996 and 0.0066 in 1997; P (location) ¼ 0.0047 in 1996 and 0.017 in 24 1997; P (cover) ¼ 0.716 in 1996 and 0.271 in 1997; P (date location) 0.0018 in 1996

Number of parasitoids per trap (x ¼ and 0.093 in 1997; P (date cover) ¼ 0.446 in 1996 and 0.502 in 1997; P (cover location) ¼ 0.188 in 1996 and 0.040 in 1997; 0 P (date location cover) ¼ 0.927 in 1996 150 190 230 150 190 230 and 0.464 in 1997. Data were subjected to square-root transformation to reduce hetero- Julian date geneity of variance. between sampling date and ground cover in 1996 indicated Effect of cover crops on densities of Erythroneura a higher rate of parasitism in plots with buckwheat late but leafhoppers not early during the season (Fig. 2). Rate of parasitism was Number of adult leafhoppers captured in yellow sticky also higher in plots with buckwheat in 1997, but the impact cardboards varied significantly between sampling dates in of ground cover was not significant (Fig. 2), possibly both 1996 and 1997, although temporal fluctuations of because the experiment was not repeated through time and population density greatly differed in both years (Fig. 3). used only two replicates. Rate of parasitism was consistently In 1996, captures of leafhoppers suggested two generations, higher near the edge rather than in the interior of the vineyard with a first peak of about 10 adults per trap in early July, in both 1996 and 1997, although neither the impact of vineyard and a second peak of about 20 adults per trap in early location nor the interaction between vineyard location and August (Fig. 3). Densities of leafhoppers were much higher sampling date were significant (Fig. 2).

buckwheat Figure 2 Impact of ground cover and vine- clover control yard location on proportion of leafhopper eggs parasitized by Anagrus adults in 1996 and 1997. Data were analysed using Edge Interior factorial ANOVA, with sampling date, ground SE) 0.70 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 0.874 in 1996; 0.35 P (location) ¼ 0.273 in 1996 and 0.249 in 1997; P (cover) ¼ 0.484 in 1996 and 0.461 in 1997; P (date location) ¼ 0.687 in 1996; P (date cover) ¼ 0.015 in 1996; P (cover location) ¼ 0.279 in 1996 and 0.888 in 1997; 0 P (date location cover) ¼ 0.491 in 1996. 15 June 4 August 4 July 15 June 4 August 4 July

Proportion of parasitized eggs (+ Data were subjected to arcsine transforma- 1996 1997 1996 1997 tion to reduce heterogeneity of variance.

# 2003 The Royal Entomological Society, Agricultural and Forest Entomology, 5, 173–181 Cover crop and parasitism of leafhopper eggs 177 in 1997 than in 1996, and during that year steadily declined the first or second batch of eggs (Fig. 5). Longevity of adult from about 50 to 40 adults per trap between mid June and parasitoids confined in chambers and provided with noth- late July (Fig. 3). A significant interaction between sampling ing or water was extremely low (< 1 day) (Fig. 6). Providing date and vineyard location in 1996 indicated that adult adult parasitoids with a solution of either sugar or honey leafhoppers were more abundant near the edge rather than significantly increased their longevity (Fig. 6). 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 Discussion five leaves) and were not significantly affected by sampling date, vineyard location, ground cover or the interaction Pro-ovigenic Anagrus wasps emerge as adults with a full between these parameters (Fig. 4). In 1997, densities of complement of eggs (Jervis et al., 2001), and do not require nymphs were relatively high and declined from about five protein resources to develop additional eggs, although to two nymphs per five leaves between mid to late July adults may still require food to provide the energy to search (Fig. 4). Densities of nymphs were significantly higher near for and parasitize eggs (Jervis et al., 1996). This food can the edge than in the interior of the vineyard, although the come in several forms, but nectar from flowers or extra- marginally significant interactions between sampling date floral nectaries or honeydew are the most likely sources and vineyard location (P ¼ 0.104) and between sampling (Jervis et al., 1993; Jervis et al., 1996). Although variable, date and ground cover (P ¼ 0.077) suggested that the our results from field, greenhouse and laboratory experi- impact of vineyard location was mostly due to high abun- ments all support the conclusion that nectar from flowers dance of nymphs in plots with buckwheat early during the increases survival and/or effectiveness of Anagrus in the season (Fig. 4). 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 mid- dles, at least at the edge of the vineyard; otherwise, yellow Impact of various food sources on rate of parasitism sticky trap captures of adult wasps did not indicate a strong and longevity of Anagrus cover crop effect (Fig. 1). Parasitism rates of sentinel leaf- The cage experiment conducted in a greenhouse environ- hopper eggs, however, were higher during mid-summer in ment indicated that the presence of buckwheat flowers 1996 on edge vines with buckwheat (Fig. 2). The same trend significantly increased the proportion of parasitized was apparent in 1997 with mean proportion of eggs para- leafhopper eggs; the rate of parasitism did not differ for sitized over 50% for vines associated with buckwheat and

buckwheat clover control

Edge Interior 30 1996

SE) 15

+/–

Figure 3 Impact of ground cover and vineyard location on number of adult Erythroneura 0 leafhoppers captured in yellow sticky traps in 1996 and 1997. Data were analysed using 80 factorial ANOVA, with sampling date, ground cover and vineyard location treated as fixed 1997 factors, and replicate as a random factor. Significance levels were as follows: P (date) ¼ 0.0001 in 1996 and 0.011 in 1997; P (location) ¼ 0.197 in 1996 and 0.592 in 1997; 40 P (cover) ¼ 0.356 in 1996 and 0.420 in 1997; Number of leafhoppers per trap (x P (date location) ¼ 0.0001 in 1996 and 0.842 in 1997; P (date cover) ¼ 0.841 in 1996 and 0.809 in 1997; P (cover location) ¼ 0.071 in 1996 and 0.293 in 1997; P (date location 0 cover) ¼ 0.874 in 1996 and 0.169 in 1997. Data 150 190 230 150 190 230 were subjected to square-root transformation to reduce heterogeneity of variance. Julian date

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buckwheat clover control

Edge Interior 24

1997 1997 SE) 12 +/–

1996 1996 0 Number of nymphs per 5 leaves (x 180 205 230 180 205 230 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 1997. 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 0.220 in 1996 and 0.043 in 1997; P (location) ¼ 0.347 in 1996 and 0.019 in 1997; P (cover) ¼ 0.871 in 1996 and 0.143 in 1997; P (date location) ¼ 0.467 in 1996 and 0.104 in 1997; P (date cover) ¼ 0.196 in 1996 and 0.077 in 1997; P (cover location) ¼ 0.874 in 1996 and 0.473 in 1997; P (date location cover) ¼ 0.573 in 1996 and 0.679 in 1997. Data were subjected to square-root transformation to reduce heterogeneity of variance.

about 30% for vines with sod in the row middles; however, flower shape can have a large effect on accessibility of we had low statistical power in 1997 (two replicates out of nectar. In our field trial, wasps responded to the presence the four were sprayed with insecticide early in the season) of buckwheat in row middles but not of clover (Figs 1 and and these differences were not statistically significant 2). Two factors may have limited the effect of clover on (Fig. 2). In the greenhouse cage experiment, having access Anagrus. First, as a perennial, it takes a full season to to flowers of buckwheat (as compared to only the vegetative become well established. Indeed, there were virtually no part of the plant) resulted in higher parasitism rate of flowers in the clover in 1996 and its not too surprising sentinel leafhopper eggs (Fig. 5). Finally, the laboratory there was no difference between clover and sod. The clover feeding trial showed that access to sugar or honey greatly did become well established by 1997 and flowered, but it did increased survival of adult wasps compared to access to not affect the abundance and activity of Anagrus; because of water alone (Fig. 6). Taken together, these results indicate low statistical power, however, it is difficult to draw any that having access to a sugar source increases the potential definitive conclusions from our results in 1997. Neverthe- impact of Anagrus on grape leafhopper. less, it may be true that buckwheat flowers are particularly As has been observed previously in New York vineyards well suited as a nectar source for small hymenopteran (Williams & Martinson, 2000), abundance and activity of parasitoids. Buckwheat flowers are small and have readily Anagrus were generally greater on the edge of the vineyard accessible nectaries (Lovei et al., 1993). In addition, buck- than in the interior, especially early in the season (Figs 1 and wheat reached the flowering stage rapidly in New York 2). This was especially true for sticky card trap captures State (under 6 weeks after seeds planted) and produced during 1996 and 1997 (Fig. 1). The effect of location was less copious flowers. Other researches have found buckwheat apparent for parasitism of sentinel eggs, although mean to be a good food resource for parasitoid wasps and flies rates were generally greater on the edge than in the interior (Bugg & Dutcher, 1989; Stephens et al., 1998). On the other (Fig. 2). In California, early colonization of vineyards by hand, clover flowers are adapted for bee pollination and, Anagrus increases the probability of successful biological seemingly, wasps have difficulty obtaining nectar rewards. control of leafhoppers in vineyards (Murphy et al., 1998). In the extensive survey of flower-visiting by hymenopteran We had hypothesized that flowering cover crops would parasitoids conducted by Jervis et al. (1993), no parasitoids promote more rapid and earlier colonization of the interior were observed exploiting clover flowers. of New York vineyards, but did not find any strong support As mentioned previously, Anagrus wasps reared from for this hypothesis; on the contrary, the interaction between grape leafhopper eggs readily feed on a sugar solution cover crop and location for sticky trap captures of adult before searching for eggs (G.E.L., unpublished observa- wasps in 1997 was in the opposite direction as predicted tions). Feeding on such a carbohydrate source will not (Fig. 1). increase potential fecundity of the female wasp since she is It is well known that flowering plants are not equal in pro-ovigenic. However, our data show that having access to their suitability as food resources for different species of a carbohydrate source will increase female longevity. In parasitoids (Jervis et al., 1996; Patt et al., 1997). For example, addition, an abundant supply of nectar-producing flowers

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10 flowers A no flowers SE)

+ A

0.6 5 SE)

+

B B Longevity (days) (x 0 Air Water Honey Sugar 0.3 solution solution

Figure 6 Longevity of adult Anagrus parasitoids provided with different food sources. One-way ANOVA indicated significant differ- ences between food sources (F ¼ 52.67; d.f. ¼ 3,33; P < 0.0001). Bars superscripted by the same letter are not statistically significant (Student–Newman–Keuls test, P < 0.05). Proportion of parasitized eggs (x 0 reared from leafhopper species that attack a number of First Second different grape species and their hybrids. In this study we did not attempt to distinguish among the different species of Batch of eggs Anagrus and it is probable that our experiments involved Figure 5 Proportion of leafhopper eggs parasitized by Anagrus several different species. This may, in part, explain the adults in the presence or absence of buckwheat flowers. Adult relatively large amount of variation in the results we parasitoids were subjected to two batches of eggs, the first one obtained. It is possible, for example, that some species of when they were 2–4 days old and the second one when they were Anagrus readily feed on nectar or other sugar sources while 5–7 days old. Data were analysed using factorial ANOVA, treating others do not. flower treatment and age of parasitoid as fixed factors, and replicate as a blocking factor. Significance levels were as follows: The ultimate test of the success of a biological control P (flower) ¼ 0.0055; P (age) ¼ 0.265; P (flower age) ¼ 0.282. Data programme is whether it leads to a reduction in pest pres- were subjected to arcsine transformation to reduce heterogeneity of sure. Leafhoppers were relatively rare in 1996 and we did variance. 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 in proximity to leafhopper eggs should reduce the time on leafhopper adults (Figs 3 and 4). Nymphs were similarly needed to obtain energy and proportionally increase the not strongly influenced by cover crop although there was a time available to find and parasitize host eggs. The cage marginally significant interaction between cover and loca- experiment supports this idea since we did find elevated tion in 1997 based on higher numbers of nymphs on grapes parasitism of sentinel leafhopper eggs in cages with buck- at the edge of the vineyard where buckwheat was planted wheat flowers present compared to cages with buckwheat (Fig. 4). There were also significantly more adult Anagrus flowers removed. Interestingly, though, we did not find any captured in the vine canopy in that region of the vineyard in strong evidence that the length of time of oviposition was that year (Fig. 1), possibly indicating a numerical response extended when the wasps had access to nectar (Fig. 5). If of parasitoids to increased density of leafhoppers. However, this were the case, we might expect a greater difference in overall, we did not see any major effects of cover on pest parasitism levels between cages with and without flowers leafhoppers and certainly no reductions in density and, for old rather than young females. Instead, we did not therefore, presumably damage. Hence, for the two years of observe a time effect. It may be true that longevity is our field study, although buckwheat had some measurable increased by having nectar, but the time period for ovipos- positive impact on Anagrus, this did not translate into a ition is not increased to as great an extent (see Baggen & major decline in pest populations. There are several possible Gurr, 1998). More work is required, however, before firm reasons for this. First, an increase in egg mortality due to conclusions can be drawn about Anagrus. Anagrus may have been compensated for by a decrease in In a survey of Anagrus reared from leafhopper eggs col- mortality from other sources. Second, 1996 was when we lected from commercial vineyards in New York, six found the largest significant impact of buckwheat on parasit- different species have been identified. The three most ism rates of sentinel eggs, and this was a year of very low common were: A. daanaei S. Triapitsyn, A. erythroneurae leafhopper densities in the vineyard (Figs 2 and 3). It may S. Triapitsyn and Chiappini, and A. tretiakovae S. Triapitsyn have been that densities were too low overall to detect an effect (Williams & Martinson, 2000). Anagrus erythroneurae on leafhoppers. In 1997, when leafhopper densities were was predominantly reared from leafhoppers attacking higher, we only had two replicates of each cover crop treat- V. vinifera whereas A. daanaei and A. tretiakovae were ment, which makes it difficult to draw strong conclusions.

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In California vineyard systems, cover crops have been References shown to reduce pest leafhopper populations, although the Baggen, L.R. & Gurr, G.M. (1998) The influence of food on reasons for this are not clear. In an unreplicated vineyard Copidosoma koehleri (Hymenoptera: Encyrtidae), and the use of trial, Nicholls et al. (2000) found lower densities of leafhop- flowering plants as a habitat management tool to enhance pers on leaves within a block of grapes that also included biological control of potato moth, Phthorimaea operculella summer cover crops of buckwheat and sunflower (Lepidoptera: Gelechiidae). Biological Control, 11, 9–17. Helianthus annus L. compared to a matched block of grapes Bugg, R.L. & Dutcher, J.D. (1989) Warm-season cover crops for in which row middles were kept free of vegetation. pecan orchards: horticultural and entomological implications. However, they did not find higher egg parasitism rates Biological Agriculture and Horticulture, 6, 123–148. from Anagrus in the vineyard with flowering cover crops. Bugg, R.L. & Waddington, C. (1994) Using cover crops to manage The authors suggest that increased numbers of generalist pests of orchards: a review. Agricultural Ecosystems and Environment, 50, 11–28. predators such as spiders may be responsible for the differ- Corbett, A. & Rosenheim, J.A. (1996) Impact of a natural enemy ences in leafhopper numbers. Daane & Costello (1998) also overwintering refuge and its interaction with the surrounding compared abundance of leafhoppers, Anagrus, and general- landscape. Ecological Entomology, 21, 155–164. ist predators between California vineyards with and without Daane, K.M. & Costello, M.J. (1998) Can cover crops reduce cover crops in a replicated experiment. They found lower leafhopper abundance in vineyards? California Agriculture, 52, leafhopper densities in vineyards with cover crops. They 27–32. considered three hypotheses to explain the reduced Daane, K.M., Williams, L.E., Yokota, G.Y. & Steffan, S.A. (1995) numbers: increased spider abundance, increased parasitism Leafhoppers prefer vines with greater amounts of irrigation. by Anagrus, or reduced vine vigour due to competition with California Agriculture, 49, 28–32. cover crops. Of the three, they found the best support for Ehler, L. (1998) Conservation biological control: past, present, and Conservation Biology Control the third hypothesis, noting that grape leafhoppers prefer future. In (ed. by P. Barbosa), pp. 1–8. Academic Press, San Diego. et al vigorously growing vines (Daane ., 1995). In some cases Jervis, M.A., Heimpel, G.E., Ferns, N., Harvey, J.A. & Kidd, A.C. they did find higher parasitism rates in vineyards with cover (2001) Life-history strategies in parasitoid wasps: a comparative crops, but this was inconsistent and appeared to be related analysis of ‘ovigeny’. Journal of Ecology, 70, 442–458. to having fewer leafhopper eggs to parasitize due to low Jervis, M.A., Kidd, N.A.C., Fitton, M.G., Huddleston, T. & vine vigour. Dawah, H.A. (1993) Flower-visiting by hymenopteran para- Overall, our results indicate Anagrus species that parasit- sitoids. Journal of Natural History, 27, 67–105. ize leafhopper pests of grapes in New York will feed on Jervis, M.A., Kidd, A.C. & Heimpel, G.E. (1996) Parasitoid adult nectar produced by cover crops, such as buckwheat, which feeding behaviour and biocontrol – a review. Biocontrol News may promote increased adult survival and parasitism of and Information, 17, 1N–26N. leafhopper eggs in the field. However, the response of Kido, H., Flaherty, D.L., Bosch, D.F. & Valero, K.A. (1984) French prune trees as overwintering sites for the grape leafhopper egg Anagrus was variable and, moreover, we did not see any parasite. American Journal of Enology and Viticulture, 35, 156–160. reduction in leafhopper abundance. Hence, although there Landis, D.A., Wratten, S.D. & Gurr, G.M. (2000) Habitat are a number of potential benefits to using flowering cover management to conserve natural enemies of arthropod pests in crops (Bugg & Waddington, 1994), our data do not strongly agriculture. Annual Review of Entomology, 45, 175–201. support enhanced biological control of leafhoppers by Lovei, G.L., Hodgson, D.J., MacLeod, A. & Wratten, S.D. (1993) Anagrus as one benefit for New York vineyards. Larger Attractiveness of some novel crops for flower-visiting hoverflies trials with greater replication may ultimately prove (Diptera: Syrphidae): comparisons from two continents. In Pest otherwise. However, conservation biological control efforts Control and Sustainable Agriculture (ed. by D. J. Dall & for New York vineyards may be better served by exploring W. N. Milne), pp. 368–370. CSIRO Publications, Canberra. ways of creating overwintering refuges for Anagrus near Martinson, T.E. & Dennehy, T.J. (1995) Varietal preferences of Erythroneura leafhoppers (Homoptera: Cicadellidae) feeding on vineyards as has been done in the California system (Kido grapes in New York. Environmental Entomology, 24, 550–558. et al., 1984; Murphy et al., 1996, 1998). Murphy, B.C., Rosenheim, J.A., Dowell, R.V. & Granett, J. (1998) Habitat diversification tactic for improving biological control: parasitism of the western grape leafhopper. Entomologia Acknowledgements Experimentalis et Applicata, 87, 225–235. Murphy, B.C., Rosenheim, J.A. & Granett, J. (1996) Habitat This research was supported by funds from the New York diversification for improving biological control: abundance of Grape Production Fund, USDA Viticultural Consortium, (Hymenoptera: Mymaridae) in grape vineyards. and the New York Wine and Grape Foundation. We Environmental Entomology, 25, 495–504. gratefully acknowledge B. Dick, A. Gillespi, S. Hesler, Nicholls, C.I., Parrella, M.P. & Altieri, M.A. (2000) Reducing the abundance of leafhoppers and thrips in a northern California K. Kunz and C. Marion for assistance with field and organic vineyard through maintenance of full season floral laboratory experiments. A big thank you to D. Miles for diversity with summer cover crops. Agricultural and Forest letting us conduct our field experiment in his vineyard and Entomology, 2, 107–113. helping us establish and maintain cover crops and R. Figel Patt, J.M., Hamilton, G.C. & Lashomb, J.H. (1997) Foraging for allowing us to collect leafhoppers and Anagrus from his success of parasitoid wasps on flowers: interplay of vineyard. K. Daane and M. Jervis provided many useful morphology, floral architecture and searching behavior. suggestions for improving the original manuscript. Entomologia Experimentalis et Applicata, 83, 21–30.

# 2003 The Royal Entomological Society, Agricultural and Forest Entomology, 5, 173–181 Cover crop and parasitism of leafhopper eggs 181

Pickett, C.H. & Bugg, R.L. (1998) Enhancing Biology Control: Wells, J.D., Cone, W.W. & Conant, M.M. (1988) Chemical and Habitat Management to Promote Natural Enemies of Agricultural biological control of Erythroneura leafhoppers on Vitis vinifera Pests. University of California Press, Berkeley. in southcentral Washington. Journal of the Entomological SAS Institute. (1988) SAS/STAT User’s Guide, Release 6.03. SAS Society of British Columbia, 85, 45–52. Institute, Cary, NC. Williams, L. III & Martinson, T.E. (2000) Colonization of new Stephens, M.J., France, C.M., Wratten, S.D. & Frampton, york vineyards by Anagrus spp. (Hymenoptera: Mymaridae): C. (1998) Enhancing biological control of leafrollers (Lepidoptera: overwintering biology, within-vineyard distribution of wasps, Torticidae) by sowing buckwheat (Fagopyrum esculentum)inan and parasitism of grape leafhopper, Erythroneura spp. (Homo- orchard. Biocontrol Science and Technology, 8, 547–558. ptera: Cicadellidae), eggs. Biological Control, 18, 136–146. Triapitsyn, S.V. (1998) Anagrus (Hymenoptera: Mymaridae) egg parasitoids of Erythroneura spp. & other leafhoppers (Homo- ptera: Cicadellidae) in north america vineyards and orchards: a taxonomic review. Transactions of the American Entomological Society, 124, 77–112. Accepted 30 November 2002

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