Effects of Pesticide Applications on the Euonymus Scale (Homoptera: Diaspididae) and Its Parasitoid, <I>Encarsia citrina</I> (Hymenoptera: Aphelinidae)

HORTICULTURAL ENTOMOLOGY

Effects of Pesticide Applications on the Euonymus Scale (Homoptera: Diaspididae) and Its Parasitoid, Encarsia citrina (Hymenoptera: Aphelinidae) ERIC J. REBEK

AND

CLIFFORD S. SADOF

Department of Entomology, Purdue University, 901 West State Street, West Lafayette, IN 47907

J. Econ. Entomol. 96(2): 446Ð452 (2003)

ABSTRACT Novel biorational insecticides are rapidly replacing more toxic, broad-spectrum compounds to control pests of ornamental plants. These new formulations are widely regarded as safe, effective, and environmentally sound with minimal impact on nontarget organisms. We tested several biorational and traditional insecticides for their ability to control euonymus scale, Unaspis euonymi (Comstock), and their potential impacts on the aphelinid parasitoid, Encarsia citrina (Crawford). Soil-applied acephate and foliar-applied pyriproxyfen exhibited superior control of euonymus scale, but also reduced numbers of surviving E. citrina. Imidacloprid failed to control euonymus scale and decreased parasitism by E. citrina. Thus, the potential impact of a pesticide on biological control is not necessarily predicted by its potential longevity, mode of delivery, or its toxicity to the target pest. Finding the best Þt of a compound into an integrated pest management program requires a consideration of all these factors and direct study of effects on the natural enemies of pests. KEY WORDS scale insects, biological control, biorational pesticide use, systemic insecticides, parasitoids

OUTBREAKS OF ARMORED scales (Homoptera: Diaspididae) are commonly associated with environmental disturbances that disrupt their natural enemy communities. Disturbances that cause armored scale outbreaks include reduced tree species diversity (Hanks and Denno 1993, Tooker and Hanks 2000), the presence of dust from roadsides (Edmunds 1973), or past use of insecticides (reviewed in Raupp et al. 2001). Changes in both the chemistry and modes of delivering pesticides in the past decades have opened new opportunities for developing biorational approaches to pesticide use that reduce pest populations while conserving natural enemies. For example, development of highly reÞned parafÞnic oils with low phytotoxicity has led to their increased use on urban landscape trees as a smothering agent. Compared with organophosphate insecticides, dormant applications of oil had only minor impact on the natural enemy community of armored scales in a pin oak, Quercus palustris Muenchhausen, canopy because of its short residual activity (Raupp et al. 2001). Similarly, application of systemic pesticides (Sclar and Cranshaw 1996, Tattar et al. 1998) to the soil has the potential to reduce nontarget impacts by reducing spray drift in the urban landscape. Euonymus scale, Unaspis euonymi (Comstock) (Homoptera: Diaspididae), provides an excellent opportunity to test this biorational approach. Native to eastern Asia, the euonymus scale feeds principally on plants in the family Celastraceae (Gill et al. 1982). In

urban landscapes throughout the United States, this pest is commonly found in ornamental plantings of shrubs and ground covers in the genera Euonymus and Pachysandra (Raupp et al. 2001, Brewer and Oliver 1984). Euonymus scales damage plants by piercing leaf or stem tissue and sucking the contents of burst plant cells. This disrupts cell-to-cell nutrient transfer, thereby permanently injuring tissues, resulting in leaf abscission, branch dieback, and, in some cases, plant death (CockÞeld and Potter 1990, Sadof and Neal 1993). Although euonymus scale is attacked by hymenopteran parasitoids as well as coccinellid and mite predators (Gill et al. 1982, Bryan et al. 1995), plant mortality is common throughout its range. In southern New England alone, annual losses of Euonymus fortunei L. plantings in urban landscapes exceed $700,000 (Van Driesche et al. 1998). In Indiana, euonymus scale has two generations per year and overwinters on host plants as mated, adult females. Females begin producing eggs in mid- to late-spring and mobile, Þrst-instar crawlers emerge in early May, whereas the second generation emerges in July. Although euonymus scale is attacked by several species (Kosztarab 1996), we have observed only one natural enemy, Encarsia citrina (Crawford) (Hymenoptera: Aphelinidae), parasitizing the scale. This thelytokous endoparasitoid (Taylor 1935, Chumakova 1965) attacks a wide range of coccoid species throughout the world (Malipatil et al. 2000 and references therein). Much of the life history

0022-0493/03/0446Ð0452$04.00/0 䉷 2003 Entomological Society of America

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REBEK AND SADOF: PESTICIDE EFFECTS ON SCALE HOST AND PARASITOID

of this species is unclear, although it overwinters within the scale host as an egg (Chumakova 1965) and begins to feed and mature in the spring. Adult wasps emerge throughout the summer, but peak abundance coincides with euonymus scale crawler emergence (E.J.R., unpublished data). Aside from eggs and crawlers, all stages of scale hosts (Taylor 1935) and both sexes of euonymus scale (E.J.R., unpublished data) serve as adequate hosts. In the current study, we use euonymus scale feeding on Euonymus fortunei to compare the impacts of soilapplied and foliar-applied insecticides on both the euonymus scale and its parasitoid, E. citrina. Materials and Methods Greenhouse and Laboratory. Insecticide trials were conducted in greenhouses on the Purdue University campus in West Lafayette, IN, during the summers of 2000 and 2001. Euonymus plants were obtained from area nurseries and potted in 15-cm (6-inch) diameter plastic pots with standard potting soil. Each year, plants selected for the trial were chosen based on their similarity in vigor and overall appearance. In 2000, eight randomly chosen plants were assigned to each treatment. On 12 May, all plants were infested with euonymus scale by attaching two 6-cm infested euonymus cuttings per plant (see Sadof and Raupp 1991). Because these cuttings also served as sources of E. citrina wasps, cuttings remained on plant stems throughout the trial, allowing emerging wasps to parasitize scales. Pretreatment scale densities were not recorded because visual inspections revealed crawlers were abundant on most plants. All insecticides were applied 17 May (23⬚C outdoor temperature, overcast) to target the crawling and recently settled Þrst-instar scales. Foliar treatments were applied using handpumped spray bottles set to mist at a rate of 10 sprays (⬇12 ml) of liquid per plant. Plants were evenly covered and materials were applied to dripping. The soilapplied acephate treatment was applied by evenly mixing the material into the upper 2 cm of soil and adding 100 ml of water. All plants were watered as needed. Euonymus scale survival was assessed on 26 June by counting the number of adult females present on each plant. All stems containing female scales were cut and taken to the laboratory, where exposed ends were dipped in parafÞn wax to delay desiccation. Stems from each replicate were placed into cylindrical, cardboard-rearing containers (10.5 cm diameter ⫻ 17.5 cm length), capped with plastic disks, and Þtted with a 4-dram glass vial on one side. These containers were used to rear adult parasitoids from euonymus scales at room temperature (25⬚C) under ßuorescent light until all scale and parasitoid activity ceased (approximately 2 mo). Finally, the number of adult female scales with parasitoid emergence holes was recorded and parasitoids were identiÞed to species. In 2001, ten potted euonymus plants were randomly assigned to each treatment. Because scales at our source site failed to produce a distinct ßush of Þrst-

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generation crawler activity, euonymus twigs containing second-generation crawlers were used to infest plants. Soil insecticides and two early treatments of pyriproxyfen were applied on 12 July (24⬚C outside temperature, overcast), one day before all plants were infested with scale crawlers, following the protocol established in 2000. Recommended amounts of soil-applied, liquid systemic treatments (imidacloprid, thiamethoxam) were applied to the soil in 100-ml aliquots. The soil-applied granular treatment (acephate) was applied by evenly mixing the material into the upper 2 cm of soil and watering in with an additional 100 ml of water. Plants were treated with the remaining foliar insecticides on 20 July (31⬚C outside temperature, sunny), following previous methods. All plants were watered as needed. On 6 September, all stems containing female scales were cut and placed into rearing containers following the protocol established in 2000. Once all activity ceased, numbers of adult female scales with and without parasitoid emergence holes were counted and parasitoids were identiÞed as described previously. Insecticides. In 2000, we evaluated the foliarapplied insecticides, including pyriproxyfen (Distance IGR; Valent USA, Walnut Creek, CA); hydrophobic extract of neem oil (Triact; Certis USA LLC, Columbia, MD); horticultural oil (Sunspray UltraFine Year-Round Pesticidal Oil; Sunoco, Philadelphia, PA); thiamethoxam (Flagship; Syngenta Crop Protection, Greensboro, NC); abamectin (Avid; Syngenta Crop Protection); and foliar-applied acephate (Orthene 97 Granular [G]; Valent USA). One soil-applied systemic insecticide, acephate (Pinpoint 15 G; Valent USA), was also evaluated. In 2001, we examined the soil-applied systemic insecticide treatments, including acephate, thiamethoxam, and imidacloprid (Marathon 60 Wettable Powder [WP]; Olympic Horticulture Products, Mainland, PA). We also evaluated all of the above foliar-applied insecticide treatments plus the following: capsaicin (Hot Pepper Wax; Bonide Products, Oriskany, NY), an additional neem oil product (Certis USA LLC), and cinnamaldehyde (Cinnamite; Mycotech, Butte, MT). Tap water sprayed in volume equal to the foliar-applied insecticides served as the control treatment in both years. Statistical Analysis. Analysis of variance for a completely randomized design (PROC GLM, SAS Institute, Cary, NC) was used to assess differences among the numbers of intact adult female scales and parasitized female scales. Treatment means were separated using Fisher protected least signiÞcant difference. Pearson correlation coefÞcients (PROC CORR, SAS Institute) were calculated from control treatment data to determine correlations among the number of intact adult female scales, the number of parasitized females, and the total number of female scales available as hosts (intact adult females ⫹ parasitized females). Assuming equal initial scale densities among treatments, the linear relationship between the number of parasitized female scales and the total number of female scales surviving to adulthood or producing parasites on un-

448 Table 1.

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Mean number of female euonymus scales surviving insecticide treatments on stems of Euonymus fortunei, 2000 –2001 Treatment (product)

Application rate (amt. product/500 ml H2O)

Mean no. intact females on stems

% Reduction from control

2000 Water (control) Triact 1% (neem) Triact 2% (neem) Sunspray UFO 0.5% Flagship 25 G (thiamethoxam) Avid (abamectin) ⫹ Sunspray UFO 0.5% Flagship 25 G (thiamethoxam) Orthene 97 G foliar Sunspray UFO 2% Distance IGR (pyriproxyfen) Distance IGR (pyriproxyfen) ⫹ Sunspray UFO 0.5% Distance IGR (pyriproxyfen) ⫹ Sunspray UFO 0.5% Pinpoint 15 G (orthene) Distance IGR (pyriproxyfen) Marathon 60 WP drench (imidacloprid) (1 d pre-crawler placement) Triact 1% (neem) Flagship 25 G foliar (thiamethoxam) Cinnamite (cinnamaldehyde) Water (control) Sunspray UFO 2% Triact 2% (neem) Hot Pepper Wax 2% (capsaicin) Marathon 60 WP foliar (imidacloprid) Neem Oil 1.5% Avid (abamectin) ⫹ Sunspray UFO 0.5% Flagship 25 G drench (thiamethoxam) (1 d pre-crawler placement) Distance IGR (pyriproxyfen) (1 d pre-crawler placement) Distance IGR (pyriproxyfen) Distance IGR (pyriproxyfen) Pinpoint 15 G (orthene) (1 d pre-crawler placement) Distance IGR (pyriproxyfen) (1 d pre-crawler placement)

5 ml 10 ml 2.5 ml 0.15 g 0.156 ml 2.5 ml 0.075 g 0.30 g 10 ml 0.468 ml 0.468 ml 2.5 ml 0.234 ml 2.5 ml 2.10 ga 0.234 ml 2001 0.33 g 5 ml 0.15 g 3.32 ml

83.00a 75.50ab 62.13abc 41.63bcd 39.88bcde

0.00 9.04 25.14 49.84 51.95

37.38cde 34.63cdef 32.88cdef 30.13cdef 11.50def

54.96 58.28 60.39 63.70 86.14

9.00def

89.16

6.38def 4.50ef 0.63f

92.31 94.58 99.24

81.00a

⫺134.78

63.50ab 35.50bc 35.40bc 34.50bcd 33.30bcd 26.40cde 26.00cde 24.60cde 24.30cde

⫺84.06 ⫺2.90 ⫺2.61 0.00 3.48 23.48 24.64 28.70 29.57

21.40cde 17.10cde

37.97 50.43

0.234 ml

4.50cde

86.96

0.468 ml 0.234 ml 2.10 ga

4.00cde 3.70de 0.90e

88.41 89.28 97.39

0.468 ml

0.50e

98.55

10 ml 10 ml 10 ml 0.15 g 7.5 ml 0.156 ml 2.5 ml 0.63 g

Means followed by the same letter are not signiÞcantly different (ANOVA, FisherÕs LSD, P ⱕ 0.05). In 2000, all applications were made 5 d after crawlers were placed on plants. In 2001, applications were made 7 d after crawler release, except where noted in table and text. a Application rate per pot.

treated control plants was determined by linear regression (PROC REG, SAS Institute) for data from both years. This relationship was the standard we used to compare the effects of insecticide application on both species. The mean number of parasitized females (⫾SEM) versus the mean number of available hosts was plotted against the regression line to determine how average survival of scales and parasitoids observed per treatment was related to survival in the untreated control. Results Euonymus Scale Control. Table 1 shows the effects of insecticide treatments on the mean abundance of intact adult female euonymus scales in 2000 Ð2001. These data reßect the number of female scales sur-

viving to reproductive maturity. Both soil-applied acephate (Pinpoint) and foliar-applied pyriproxyfen (Distance IGR) resulted in ⬎85% reduction in scale abundance from the control treatment in both years. However, Pinpoint caused leaf scorching in both years, so it is not recommended nor labeled for managing euonymus scale on Euonymus fortunei. Pyriproxyfen retained its high efÞcacy (⬎85%) against euonymus scale regardless of rate, date of application, and delivery with or without horticultural oil. Soil-applied imidacloprid (Marathon) was the least effective treatment overall, resulting in more than twice the number of scales than the control in 2001 (Table 1). The number of scales remaining in another soil-applied compound, thiamethoxam (Flagship), was not signiÞcantly different from the control in 2001. Applied as foliar treatments, imidacloprid, thiame-

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449

Table 2. Mean number of parasitized female euonymus scales following insecticide treatments on stems of Euonymus fortunei, 2000 –2001 Treatment (product)

Sunspray UFO 0.5% Water (control) Triact 1% (neem) Avid (abamectin) Sunspray UFO 0.5% Triact 2% (neem) ⫹ Sunspray UFO 2% Pinpoint 15 G (orthene) Distance IGR (pyriproxyfen) Sunspray UFO 0.5% Distance IGR (pyriproxyfen) Flagship 25 G (thiamethoxam) Distance IGR (pyriproxyfen) ⫹ Sunspray UFO 0.5% Orthene 97 G foliar Distance IGR (pyriproxyfen) Flagship 25 G (thiamethoxam) Flagship 25 G foliar (thiamethoxam) Triact 1% (neem) Cinnamite (cinnamaldehyde) Neem Oil 1.5% Sunspray UFO 2% Water (control) Hot Pepper Wax 2% (capsaicin) Triact 2% (neem) Marathon 60 WP drench (imidacloprid) (1 d pre-crawler placement) Marathon 60 WP foliar (imidacloprid) Avid (abamectin) ⫹ Sunspray UFO 0.5% Flagship 25 G drench (thiamethoxam) (1 d pre-crawler placement) Distance IGR (pyriproxyfen) Distance IGR (pyriproxyfen) (1 d pre-crawler placement) Distance IGR (pyriproxyfen) Pinpoint 15 G (orthene) (1 d pre-crawler placement) Distance IGR (pyriproxyfen) (1 d pre-crawler placement)

Application rate (amt. product/500 ml H2O) 2000 2.5 ml 5 ml 0.156 ml 2.5 ml 10 ml 10 ml 2.10 ga 0.468 ml 2.5 ml 0.468 ml 0.075 g 0.234 ml 2.5 ml 0.30 g 0.234 ml 0.15 g

Mean no. parasitized females

% Reduction from control

7.125a 5.750ab 4.000abc

⫺23.91 0.00 30.43

3.875abcd 2.750bcd 0.625cd 0.375cd

32.61 52.17 89.13 93.48

0.286cd 0.250cd 0.125cd

95.03 95.65 97.83

0.000cd 0.000cd 0.000cd 0.000cd

100.00 100.00 100.00 10.00

18.40a 18.40a 14.70ab 12.90abc 12.80abc 11.60abc 11.10abcd 9.90abcd 8.50bcde

⫺58.62 ⫺58.62 ⫺26.72 ⫺11.21 ⫺10.34 0.00 4.31 14.66 26.72

0.15 g 0.156 ml 2.5 ml 0.63 g

8.20bcde

29.31

4.40cde 2.60de

62.07 77.59

0.468 ml 0.234 ml

0.70e 0.50e

93.97 95.69

0.234 ml 2.10 ga

0.40e 0.000e

96.55 100.00

0.468 ml

0.000e

100.00

2001 0.15 g 5 ml 3.32 ml 7.5 ml 10 ml 10 ml 10 ml 0.33 g

Means followed by the same letter are not signiÞcantly different (ANOVA, FisherÕs LSD, P ⱕ 0.05). In 2000, all applications were made 5 d after crawlers were placed on plants. In 2001, applications were made 7 d after crawler release, except where noted in table and text. a Application rate per pot.

thoxam, and abamectin (Avid) plus horticultural oil resulted in scale numbers not signiÞcantly different from the control. The neem oil products did not signiÞcantly reduce scale numbers compared with the control in both years. Horticultural oil (Sunspray 2%) reduced the number of scales by ⬎63% in 2000, but did not signiÞcantly reduce scale abundance compared with the control in 2001. The remaining foliar-applied compounds (e.g., capsaicin, cinnamaldehyde) were not signiÞcantly different from the control. Parasitized Euonymus Scales. The number of parasitized female scales and the total number of available hosts in the control treatment were signiÞcantly correlated in 2001 (r ⫽ 0.9564, n ⫽ 10, P ⬍ 0.0001), but not in 2000 (r ⫽ ⫺0.1857, n ⫽ 8, P ⫽ 0.6598). Table 2 lists the results of insecticide treatments on the mean number of female scales parasitized by

E. citrina. These data represent the effect of insecticide treatments on the number of parasitoids that can emerge from a given number of euonymus scale hosts per plant. The pyriproxyfen and soil-applied acephate treatments resulted in the fewest E. citrina emerging from scales. In both years, the reduction in the number of parasitized females from control was ⬎93% for these insecticides. Foliar acephate (Orthene 97G) also signiÞcantly decreased the number of females parasitized by E. citrina in 2000. The effects of foliarapplied thiamethoxam (applied at 0.15 g/500 ml H2O) and horticultural oil (Sunspray 2%) on parasitoid emergence differed between years. Thiamethoxam was among those chemicals that resulted in the fewest parasitoids emerging in 2000. The following year, however, this insecticide ranked among the most favorable to parasitoid survival (Table 2). Fewer parasitoids

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Fig. 1. Mean parasitized female euonymus scales versus mean female scales surviving to adulthood or producing parasitoids per treatment in 2001. The solid line is the regression line of the control treatment (water). The 95% upper and lower conÞdence limits of the regression line are also plotted. Symbols represent means and bars represent ⫾SEM number of parasitized females. See Tables 1 and 2 for “low” and “high” application rates and see text for “early” and “late” application dates of pyriproxyfen.

emerged in 2000 than 2001 following applications of Sunspray 2%. However, the number of parasitized females in the control treatment was almost two-fold higher in 2001, which may explain the between-year differences. In 2000, horticultural oil (Sunspray 0.5%), neem, and abamectin plus oil favored greater numbers of parasitized females (Table 2). In 2001, applications of neem, cinnamaldehyde (Cinnamite), and capsaicin (Hot Pepper Wax) resulted in high numbers of parasitized females not signiÞcantly different from control. Abamectin plus oil reduced numbers of parasitized females yet was not signiÞcantly different from control. Imidacloprid applied as both a foliar and soilsystemic treatment resulted in numbers of emerging parasitoids not signiÞcantly different from the control in 2001. However, soil-applied imidacloprid also exhibited poor control over euonymus scale (Table 1), yet yielded fewer parasitoids relative to the number of available scale hosts (Fig. 1). Discussion Superior control of euonymus scale was achieved using the foliar-applied insect growth regulator (IGR), pyriproxyfen (Distance IGR) (Table 1). Foliar-applied imidacloprid (Marathon) and thiamethoxam (Flagship) failed to control scales. Applications of abamectin (Avid) plus oil achieved poor to moderate control of euonymus scale. Biorational foliar insecticides, including neem oil (e.g., Triact), capsaicin (Hot Pepper Wax), and cinnamaldehyde (Cinnamite), did not provide reasonable control of scale populations. Horticultural oil (Sunspray 2%) provided good scale control in 2000, but was not very effective in 2001. The 2000 results are

more consistent with Þeld studies on euonymus scale (Sadof and Sclar 2000). The lack of control in 2001 is difÞcult to explain. Soil-applied acephate (Pinpoint) was highly effective against euonymus scale (Table 1), but it is not recommended for use on Euonymus fortunei to treat euonymus scale because it is phytotoxic to this species. Soil-applied thiamethoxam (Flagship) provided reasonable short-term control in 2001 and performed better than imidacloprid (Marathon). The poor performance of imidacloprid likely relates to euonymus scale feeding strategy and the low solubility of imidacloprid (0.51 g/liter H2O at 20⬚C). Rather than feeding on phloem like other sucking insects, armored scales, such as euonymus scale, feed on subcuticular plant cell contents (Sadof and Neal 1993). Sadof and Sclar (2000) concluded that imidacloprid is not readily translocated beyond vascular plant tissue. Therefore, scale feeding in parenchyma cells does not result in enough contact with imidacloprid to cause signiÞcant scale mortality. In contrast, acephate is much more soluble (790 g/liter H2O at 20⬚C), enabling more insecticide to diffuse into nonvascular plant tissue and providing better control of euonymus scale. Cloyd and Sadof (1998) also found solubility to explain why acephate killed thrips attacking greenhouse ßowers, whereas imidacloprid did not. The relatively higher solubility of thiamethoxam (4.1 g/liter H2O at 25⬚C) compared with imidacloprid may explain the greater control achieved with soil applications of the former (Table 1). Of course, differences in the amount of each product taken up by the roots as well as mode of action of these compounds may also contribute to measured differences in observed levels of control.

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The ability of a compound to kill euonymus scale is only part of the information needed when developing an integrated pest management program. The effect of insecticide treatment on nontarget organisms, particularly natural enemies, also needs to be assessed. Insecticides that destroy these beneÞcials eliminate natural control of pest populations (DeBach and Rose 1977, Raupp et al. 2001) and can exacerbate the problem if pest populations develop resistance. Therefore, it is necessary to seek compounds that provide reasonable scale control with minimal impacts on natural enemies. Although pyriproxyfen was highly effective against euonymus scale, its high efÞcacy left relatively few hosts to sustain a population of its aphelinid parasitoid, E. citrina (Table 2). This situation suggests that the impact of pyriproxyfen on natural enemies could be reduced in Þeld conditions where incomplete spray coverage spares host targets. In contrast, neem, capsaicin and cinnamaldehyde left moderate numbers of hosts available to E. citrina. The effect of pyriproxyfen on long-term biological control of euonymus scale using E. citrina still needs to be assessed because of the unknown effects of this IGR in Þeld conditions. SpeciÞcally, in the heterogeneous landscape environment, differences in microclimate are likely to result in an emergence period of both scales and parasitoids that is far longer than our greenhouse study. Indeed, studies on the effect of neem on the closely related species, Encarsia pergandiella, indicate that this IGR had little or no effect on the parasitoid population when applied to control silverleaf whiteßy, Bemisia argentifolii (Stansly and Liu 1997). Similarly, they found that insecticidal soap and two sugar esters had little or no effect on this parasitoid in the same study plots. In contrast, vegetable Þelds sprayed with imidacloprid showed reduced numbers of Eretmocerus sp., Encarsia nigricephala, E. pergandiella, E. quaintancei, and E. strenua compared with control Þelds (Simmons and Jackson 2000). Parasitoids developing within the body cavity of armored scale hosts are usually protected from foliarapplied insecticides (Rosenheim and Hoy 1988, Schultz 1990, Raupp et al. 2001). But parasitoids that are in ßight are vulnerable to sprays (Schultz 1985, Potter et al. 1989, Schultz 1990) or contact with residual insecticides present on plant surfaces (McClure 1977). Parasitoids of euonymus scale (E.J.R., unpublished data) and other scale species (Schultz 1985, 1990; Potter et al. 1989) show peak activity that coincides with crawler emergence. Unfortunately, maximum parasitoid activity also coincides with pesticide applications to target crawlers of several scale species (Schultz 1985, Potter et al. 1989, Walker et al. 1990, Sadof and Sclar 2000). Thus, applying insecticides with low residual activity when parasitoids are not abundant (e.g., before crawler emergence) could reduce natural enemy mortality (Raupp et al. 2001) and improve the compatibility of biorational insecticides with biological control.

451

There are many factors that can affect rates of parasitism in a host species. These include density of hosts, density of parasitoids, and the presence of insecticide residue in and on a host. In the 2001 control plants, we found a strong density-dependent relationship between the number of scale hosts and the number of those hosts that were parasitized. This strong density-dependent relationship usually held true in 2001 when scale numbers were reduced by insecticide treatments. However, the soil-applied imidacloprid was an exception to that trend. In this case, the number of parasitoids that emerged from scale hosts was well below the number expected from the number of available scale hosts alone (Fig. 1). Although foliar insecticides have the potential to kill natural enemies, Smith and Krischik (1999) state there is a common assumption that systemic insecticides reduce pest populations without harming nontarget species. However, our results suggest that soil-applied imidacloprid actually causes an increase in euonymus scale populations and reduces the number of parasites beyond that which would be expected by merely reducing scale densities (Fig. 1). Sadof and Sclar (2000) also found that applications of imidacloprid on pachysandra increased euonymus scale populations relative to the control. Other potential mechanisms, such as hormoligosis, the increase in development and egg production as a result of sublethal doses of insecticide, or improved plant quality, are not testable with our data. No evidence of hormoligosis has been reported for armored scales (Raupp et al. 2001), but exposure to imidacloprid increased twospotted spider mite fecundity and longevity (James and Price 2002). Despite the variable effectiveness of horticultural oil in controlling euonymus scale (Table 1), this product may still be effective as a summer spray because of its low residual toxicity and often spotty coverage. From the standpoint of biological control, incomplete coverage could help conserve enough scale hosts to maintain populations of natural enemies. The ability of natural enemies to control these fragmented scale populations is likely to be determined by both the foraging capability of the species involved and the extent to which the scale population is patchy (Kareiva 1987). To optimize biological control of euonymus scale, we strongly suggest applying compounds with low residual toxicity at times when natural enemy activity is minimal. Some biorational insecticides, such as pyriproxyfen, were capable of reducing euonymus scale populations (Table 1). Whether this level of reduction could result in local extinctions of parasitoids and subsequent scale resurgence merits further investigation. Imidacloprid and other systemic insecticides must be carefully evaluated for efÞcacy in scale control and impact on natural enemies before implementation into an integrated pest management program. These strategies will enhance biological control of euonymus scale in the urban environment.

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JOURNAL OF ECONOMIC ENTOMOLOGY Acknowledgments

We thank H. Fleck-Funk, W. Brignon, K. Arvin, R. Snyder, J. Marencik, D. Richardson, and L. Knoblock for assistance with greenhouse and laboratory work. We also thank R. Foster, A. York, D. Schuster, and two anonymous reviewers for comments on earlier versions of this manuscript. We thank B. Bunge of LaPorte County Nursery for providing euonymus plants. This research was supported in part by Mycotech Corporation, Olympic Horticultural Products, Syngenta Crop Protection, Valent USA Corporation, and USDA-NRIGP 99-35316-7850. This is paper 16926 of the Indiana Agriculture Research Program.

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