BIOLOGICAL CONTROL Effects of Systemic Imidacloprid on maculata (Coleoptera: )

S. F. SMITH AND V. A. KRISCHIK

Department of Entomology, University of Minnesota, 219 Hodson Hall, 1980 Folwell Avenue, St. Paul, MN 55108

Environ. Entomol. 28(6): 1189Ð1195 (1999) ABSTRACT The coccinellid predator (DeGeer) is found throughout the central and eastern United States and is a potential biological control agent for interiorscapes. Currently, the systemic insecticide imidacloprid is widely used in interiorscape and landscape integrated pest management. Effects of imidacloprid on the Þtness and behavior of C. maculata were examined by conÞning groups of adults with inßorescences of treated sunßower, Helianthus annus L. ÔBig SmileÕ; chrysanthemum, Chrysanthemum morifolium Ramat. ÔPeleeÕ; and dandelion, Tarax- acum officinale Wiggers. ConÞnement with inßorescences from imidacloprid-treated plants signif- icantly decreased the general mobility of C. maculata in each plant system. The magnitude of the reduction in mobility varied with plant species. In the sunßower bioassay, survivorship was lower for exposed to imidacloprid at the label rate and twice the label rate (38.3 Ϯ 6.60 and 20.0 Ϯ 6.71% survival, respectively) than for beetles conÞned to untreated controls (97.5 Ϯ 2.50% survival). Also, in the sunßower bioassay, beetles exposed to the label rate and twice the label rate of imidacloprid took longer to produce their 1st (9.78 Ϯ 2.01 and 14.00 Ϯ 2.10 d after bioassay respectively) than beetles from untreated controls (2.56 Ϯ 0.50 d after bioassay). The results reported here indicate that the use of imidacloprid may not be compatible with the coccinellid predator C. maculata.

KEY WORDS Coleomegilla maculata, imidacloprid, nontarget effects, landscape integrated pest management, systemic insecticides

CONSERVATION OF NATURAL enemies is an important in the postsynaptic membranes (Boyd and Boethel component of modern integrated pest management 1998). Imidacloprid slowly degrades in the and (IPM) (Hilbeck et al. 1998a). In urban ecosystems, the agonistic nature causes substantial disorder in the many pest populations are maintained at low densities insectÕs nervous system. by indigenous natural enemies (Flanders 1986, Raupp Effects of imidacloprid on several nontarget et al. 1992, Cobb 1997). Pest outbreaks after pesticide have been described. Sclar et al. (1998) showed that applications illustrate the importance of conserving the predator Orius tristicolor (White) suffered higher natural enemies in urban landscapes (Merritt et al. mortality when conÞned with imidacloprid-treated 1983, Raupp et al. 1992, Hanks and Denno 1993, Terry foliage than when conÞned with untreated foliage. et al. 1993). Pesticides that are compatible with natural Mizell and Sconyers (1992) found signiÞcant mortal- enemies can be effective tools for urban IPM (Raupp ity for several insect species, including the predator et al. 1992). Hippodamia convergens (Gue´rin-Me´neville) after ex- Imidacloprid, a chloronicotynol insecticide, was in- posure to imidacloprid residues. Boyd and Boethel troduced to landscape pest management in the early (1998) found that Geocoris punctipes (Say) adults 1990s (Sclar et al. 1998). Its systemic activity, low were as susceptible to the foliar residue of imidaclo- mammalian toxicity, and effectiveness against a wide prid as they were to the residues of methyl parathion range of pests make it an attractive choice for a variety (organophosphate) and permethrin (pyrethroid) 24 h of plant protection programs, including landscape pest after application. management (Mullins 1993). It is effective against Soil application of granular imidacloprid is the most many pests, including , scale insects, whiteßies, common application method in interiorscapes. This some Coleoptera, and some Lepidoptera (Mullins application may be less harmful to nontarget insects 1993). Besides its widespread use in landscapes, imi- than the foliar spray because it is less likely to come in dacloprid is commonly used in interiorscapes because direct contact with the nontarget insect (Mizell and its long-term effectiveness makes frequent applica- Sconyers 1992). However, many natural enemies sup- tions unnecessary, its systemic activity makes its use plement their diet by feeding on plant material, either safe in public areas, and it is effective against the most by feeding directly on the plant as with O. tristicolor common interiorscape pests (West 1998). It has a (Sclar et al. 1998) or by feeding on plant or mode of action similar to that of nicotine, functioning nectar in the case of some predatory beetles and par- as an agonist on the nicotinic acetylcholine receptor asitic wasps (Hagen 1986). If the insecticide is trans-

0046-225X/99/1189Ð1195$02.00/0 ᭧ 1999 Entomological Society of America 1190 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 6 located to ßowers, then these insects may ingest imi- Beetles used in the sunßower bioassay were 28Ð30 d dacloprid. Additionally, systemic pesticides can in old, in the chrysanthemum bioassay 14Ð16 d old, and some cases be translocated to the surface of the plant 17Ð20 d old in the dandelion bioassay. or enter a vapor stage and come in direct contact with Treatments. Four treatments were used. For the 2 insects on the plant (Croft 1990). Any of these modes experimental treatments, potted plants were treated of contact could affect beneÞcial insects associated with Marathon 1% granular (1% [AI] imidacloprid) with imidacloprid-treated plants. (Olympic Horticultural, Mainland, PA) at the maxi- Coleomegilla maculata (DeGeer) was selected as mum labeled rate appropriate for the pot size (1ϫ), the test organism for this study for 2 reasons. First, it and twice that label rate (2ϫ). Individual dandelions is a potential biological control agent for interior- and chrysanthemums were grown in 15.2-cm pots; scapes, which currently release H. convergens for each pot received 20 mg (AI) (1ϫ) or 40 mg (AI) control. C. maculata, unlike H. convergens, is a (2ϫ). Sunßowers, which were larger plants and grown facultative pollen feeder; laboratory studies have in 25.4-cm pots, received 27 mg (AI) (1ϫ)or54mg shown that it is able to complete its life cycle on pollen (AI) (2ϫ). The control treatments in each bioassay alone (Hodek and Honek 1997). During periods of low consisted of untreated plants. A starvation treatment prey density, populations of the biological control was included to determine the effects of 7 d without agent could be maintained on pollen from ßowering access to pollen or nectar. If beetles conÞned to ßower plants in the interiorscape. Second, C. maculata has a heads were not feeding on pollen then no differences broad geographic range in the central and eastern among treatments should be found when compared United States (Gordon 1985) and is commonly found with the starvation treatment. Beetles were conÞned in many urban and agricultural systems. to the experimental arenas (described below) for 7 d. This research examined nontarget effects of the For the beetles conÞned to the ßower heads of the systemic insecticide imidacloprid on C. maculata. The untreated and treated plants, only pollen and nectar effects of imidacloprid on behavior and Þtness produced by the ßower head was available as food. A were measured after conÞning the beetles with inßo- wetted cotton wick was included in each experimental rescences of imidacloprid-treated plants. Behavioral arena and rewetted daily. parameters measured were walk rate and ßip time. Imidacloprid was applied to sunßowers and chry- Several life history parameters including survivorship, santhemums when the ßowers were in their early bud days to 1st oviposition, and daily production were stage. Imidacloprid was therefore present in the soil measured. and available to the plants while they were developing ßowers. We began the sunßower bioassay 25 d after Materials and Methods application, when the sunßower inßorescences were open and producing pollen. For the chrysanthemums, Plant Systems. The effects of imidacloprid on C. maculata were examined in 3 species of Asteraceae the bioassay began 36 d after application of imidaclo- (Compositae). Sunßower, Helianthus annus L. ÔBig prid when their inßorescences were open and pro- ducing pollen. Dandelions began continuously pro- smileÕ, and chrysanthemum, Chrysanthemum morifo- Ϸ lium Ramat. ÔPeleeÕ, are common ornamental plants in ducing ßowers 7 mo after planting seeds. At this urban landscapes and interiorscapes. Dandelion, time, all open and developing ßower heads were re- Taraxacum officinale Wiggers, was selected because moved and imidacloprid was applied to the pots. The observations from the Þeld indicate that C. maculata experiment began 10 d after application when new visit the plants early in the season to feed on pollen. ßowers were in full bloom. During the 10-d postap- For turfgrass pest control, granular imidacloprid is plication and prebioassay period, unused ßower heads mixed with fertilizer and applied widely in the urban were removed daily and discarded. landscape. Consequently, imidacloprid may be trans- Bioassay Designs. In the sunßower bioassay, 105 located to the ßowers of dandelions and affect C. plants per treatment and 4 beetles per plant were used. maculata. For the chrysanthemum bioassay, 11 plants per treat- Study Organisms. C. maculata for the sunßower and ment and 4 beetles per plant were used. In these 2 chrysanthemum bioassays were reared by IPM Bio- bioassays, beetles were conÞned using a bag (28 by 33 logicals (Eagan, MN). Beetles used in the dandelion cm) made of no-see-um cloth (Balson Hercules bioassay were reared from a laboratory colony at the Group, New York) that was placed over the ßower University of Minnesota, St. Paul. Before the bioassays, head and secured at the bottom with a rubber band. males and females for each bioassay were kept to- In the dandelion bioassay, mason jars (355 ml) were gether and mating was frequent. Beetles were main- set up in the laboratory, each containing 4 beetles. A tained on diet (described below) and kept under a small section of no-see-um cloth was placed over the photoperiod of 16:8 (L:D) h, 25 Ϯ 1ЊC, and 55Ð75% mouth of each jar and secured with a rubber band. RH. Sunßowers, chrysanthemums, and dandelion Two blocks of 5 jars per treatment were set up on ßowers matured at different rates, which resulted in subsequent days for a total of 10 jars per treatment. the initiation of bioassays at different times. Conse- Dandelion ßower heads were cut from plants in the quently, beetles were of slightly different ages at the greenhouse, placed in glass scintillation vials with wa- onset of the bioassays. Within each plant system, how- ter, and put in the mason jars, 1 per jar. Dandelion ever, beetle age and colony source was consistent. ßower heads stay open for 24Ð48 h. Closed ßower December 1999 SMITH AND KRISCHIK:EFFECTS OF IMIDACLOPRID ON C. maculata 1191 heads were removed from the jars and replaced with open ßower heads every other day. Behavioral Parameters Measured. After7dofcon- Þnement in the experimental arenas, the behavioral parameters walk rate and ßip time were measured. Walk rate was measured by placing each beetle on a piece of multipurpose ofÞce paper (75 g/m2). As the beetle walked, its path was followed and traced with a pencil and the time recorded. The length of the path was measured using a string and converted to a walk- ing rate of cm/s. Time spent following an individual beetle ranged from 1.31 to 30 s. If a beetle did not move in 30 s it was given a score of 0. A 2nd behavioral parameter, ßip time, was included in the study to examine another possible reduction in general mobil- Fig. 1. Mean Ϯ SE walking rates for C. maculata after 7 ity caused by exposure to imidacloprid-treated plants. d of conÞnement to imidacloprid-treated plants, untreated The behavioral parameter ßip time was selected as a plants, or starvation arenas. See Table 1 for ANOVA results. way of testing the ability of a beetle to right itself after dropping from an untreated or imidacloprid-treated range test option, means statement, PROC GLM, SAS, plant. Flip time was measured by placing each beetle SAS Institute 1998), which controls for type I exper- dorsal side down on a piece of Fisher brand medium- iment wise error. porosity Þlter paper (Fairlawn, NJ). Time until the beetle turned itself upright was recorded. If a beetle Results was unable to right itself in 30 s it was given a score of 31. Beetles that had died during the Þrst7dofthe Exposure to imidacloprid affected beetles in all bioassay were not included in the analysis of behav- plant systems tested. General mobility was signiÞ- ioral parameters. cantly reduced, indicated by a decreased walk rate Fitness Parameters Measured. After the behavioral (Fig. 1; Table 1) and increased ßip time (Fig. 2; Table parameters were measured, the beetles were placed 1), in the imidacloprid treatments in all 3 plant sys- individually in plastic petri dishes (60 by 50 mm) and tems. The magnitude of the differences, however, var- kept in laboratory incubators. They were maintained ied with plant system. In sunßower, behavioral effects under a photoperiod of 16:8 (L:D) h, 25 Ϯ 1ЊC, and were very strong with only 1 of 19 beetles in the 2ϫ 55Ð75% RH. Survivorship, days to 1st oviposition (ovi- treatment scoring a walking rate and 0 of 19 success- positing beetles only), and daily egg production (ovi- fully ßipping (Table 1). Differences were highly sig- positing beetles only) were monitored for 30 d. Each niÞcant in both walking rate (P Ͻ 0.001) and ßip time petri dish contained a 0.5-ml centrifuge tube Þlled (P Ͻ 0.001). Because no beetles moved in the 2ϫ with distilled water and a cotton string for a wick. treatment, the assumption of constant variance was Tubes were reÞlled with water as needed. Each day, violated. When this treatment was removed from the beetles were fed a small cube of “diet 7” as described analysis, a signiÞcant treatment effect was still ob- by Atallah and Newsom (1966). This diet was modiÞed served in both walking rate (F ϭ 250.6; df ϭ 2, 27; P Ͻ by omitting tegosept, aureomycin, and potassium hy- 0.001) and ßip time (F ϭ 111.5; df ϭ 2, 27; P Ͻ 0.001). droxide. For beetles in the chrysanthemum and dandelion bio- Statistical Analysis. All behavioral and Þtness pa- assays, all beetles in the 2ϫ and 1ϫ treatments suc- rameters from the sunßower and chrysanthemum bio- cessfully ßipped and walked, but their general mobil- assays were compared using one-way analyses of vari- ity was reduced. In the chrysanthemum bioassay, both ance (ANOVAs). Data for ßip times from the walking rate (P Ͻ 0.001) and ßip time (P Ͻ 0.001) sunßower bioassay were log transformed, data for days showed signiÞcant treatment effects. In the dandelion to 1st oviposition from the sunßower bioassay were bioassay, walking rate (P Ͻ 0.001) and ßip time (P Ͻ square root transformed, and data for ßip times from 0.001) showed signiÞcant treatment effects. the chrysanthemum bioassay were transformed to in- A signiÞcant treatment effect on C. maculata sur- verse of the square root to equalize variance. Reported vivorship was observed in the sunßower bioassay (P Ͻ means are untransformed. In the dandelion bioassay, 0.001). There was no statistically signiÞcant difference survivorship, days to 1st oviposition, and daily egg between survivorship for beetles from the untreated production for beetles were analyzed using one-way plants (97.5%) and the starvation treatment (85.5%). ANOVAs testing for treatment effects. Flip time and However, survivorship for beetles conÞned to the walk rate for beetles in the dandelion bioassay were ßower heads of the 1ϫ (38.3%) and 2ϫ (20.0%) analyzed using a two-way ANOVA testing for treat- treated sunßowers was signiÞcantly lower than con- ment and day effects. Data for ßip times from the trols (Fig. 3; Table 1). No treatment effect on survi- dandelion bioassay were transformed to the inverse of vorship was found in either the chrysanthemum bio- the square root to equalize variance. Reported means assay (P ϭ 0.20) or the dandelion bioassay (P ϭ 0.40). are untransformed. Means for all variables were sep- A signiÞcant treatment effect was observed in days arated using the RyanÐEinotÐGabrielÐWelsh multiple to 1st oviposition in the sunßower bioassay (P Ͻ 1192 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 6

Table 1. Effects of imidacloprid on C. maculata behavior and fitness in 3 plant systems

Mean Ϯ SE Plant system Treatment Walk rate, Flip time, Survivorship, No. days to No. beetles that cm/s s % 1st oviposition laid eggs Sunßower Starved 2.30 Ϯ 0.08a 2.27 Ϯ 0.23a 85.5 Ϯ 5.50a 6.95 Ϯ 0.66b 19 Untreated 2.60 Ϯ 0.08a 3.62 Ϯ 0.85a 97.5 Ϯ 2.50a 2.56 Ϯ 0.50a 16 1X 0.20 Ϯ 0.10b 28.04 Ϯ 1.63b 38.3 Ϯ 6.60b 9.78 Ϯ 2.01b 9 2X 0b 31b 20.0 Ϯ 6.71b 14.00 Ϯ 2.10c 4 FFϭ 362.9 F ϭ 274.2 F ϭ 46.1 F ϭ 15.1 df 3, 36 3, 36 3, 36 3, 44 PPϽ 0.001 P Ͻ 0.001 P Ͻ 0.001 P Ͻ 0.001 Chrysanthemum Starved 3.32 Ϯ 0.12a 1.41 Ϯ 0.14a 97.72 Ϯ 2.27a 10.61 Ϯ 1.66a 23 Untreated 2.95 Ϯ 0.22a 2.44 Ϯ 0.67a 100a 10.64 Ϯ 1.66a 22 1X 1.77 Ϯ 0.33b 9.69 Ϯ 2.52b 90.9 Ϯ 5.08a 11.42 Ϯ 1.75a 19 2X 1.93 Ϯ 0.24b 6.34 Ϯ 1.55b 93.18 Ϯ 3.52a 8.86 Ϯ 1.73a 22 FFϭ 9.8 F ϭ 10.8 F ϭ 1.6 F ϭ 0.4 df 3, 40 3, 40 3, 40 3, 82 PPϽ 0.001 P Ͻ 0.001 P ϭ 0.20 P ϭ 0.76 Dandelion Starved 4.18 Ϯ 0.11ab 0.99 Ϯ 0.07a 100 13.56 Ϯ 1.38a 16 Untreated 4.52 Ϯ 0.10a 1.13 Ϯ 0.13a 100 15.05 Ϯ 1.98a 17 1X 3.85 Ϯ 0.16b 2.02 Ϯ 0.24b 100 15.88 Ϯ 1.42a 16 2X 3.28 Ϯ 0.19c 4.51 Ϯ 1.34b 97.5 Ϯ 2.5 10.85 Ϯ 0.86a 20 FFϭ 16.7 F ϭ 9.9 F ϭ 1.0 F ϭ 2.6 df 3, 35 3, 35 3, 36 3, 65 PPϽ 0.001 P Ͻ 0.001 P ϭ 0.40 P ϭ 0.063

Means within plant system and column followed by the same letter are not signiÞcantly different (P ϭ 0.05); RyanÐEinotÐGabrielÐWelsch multiple F test.

0.001). Beetles from the 2ϫ treatment had the longest of systemic imidacloprid on the aphid, Macro- delay in egg production (14.0 d). Days to 1st egg siphum euphoribae (Thomas), the walking rate of the production in the 1ϫ and the starvation treatments aphid was signiÞcantly reduced at 3 of the 4 concen- were not statistically different from one another (9.8 trations tested (Boiteau and Osborn 1997). A reduc- and 6.9 d, respectively). Beetles from untreated sun- tion in general mobility can affect the prey-Þnding ßower inßorescences had the shortest number of days abilities of natural enemies (Croft 1990), or it can to 1st oviposition (2.6 d) (Fig. 4; Table 1). No treat- expose natural enemies to mortality factors such as ment effect on days to 1st oviposition was found in and desiccation (Ffrench-Constant and either the chrysanthemum bioassay (P ϭ 0.76) or the Vickerman 1985). The decrease in general mobility dandelion bioassay (P ϭ 0.063). observed in the current study indicates that imidaclo- prid-treated plants may diminish searching behavior and prey consumption by C. maculata. Discussion The decrease in beetle mobility after exposure to Exposure to imidacloprid reduced the general mo- imidacloprid was much greater in the sunßower bio- bility of C. maculata in all plant systems. The mode of assay than in either the chrysanthemum or dandelion action of imidacloprid, as an agonist in the insectÕs postsynaptic membrane, makes changes in behavior and general mobility possible. In a study on the effects

Fig. 3. Mean Ϯ SE percent survivorship of C. maculata at the end of the experiments. These beetles were conÞned to imidacloprid-treated plants, untreated plants, or starvation Fig. 2. Mean Ϯ SE ßip times for C. maculata after7dof arenas for 7 d, then kept individually in petri dishes and fed conÞnement to imidacloprid-treated plants, untreated artiÞcial diet daily for the subsequent 30 d. See Table 1 for plants, or starvation arenas. See Table 1 for ANOVA results. ANOVA results. December 1999 SMITH AND KRISCHIK:EFFECTS OF IMIDACLOPRID ON C. maculata 1193

the ßower parts, or contact with a vapor layer around the ßower parts. Days to 1st oviposition was shorter for beetles in the 2ϫ treatment than for any other treatment in both the chrysanthemum and the dandelion bioassays (Fig. 4). Although this trend was not statistically signiÞcant, it appeared in 2 plant systems. Several researchers have shown increases in fecundity after pesticide exposure, indicating the complex nature of pesticide effects (Croft 1990). Days to 1st oviposition (Fig. 4) varied widely among the 3 plant systems. Beetles from untreated sunßowers produced eggs 2.6 d after bioassay, whereas beetles in Fig. 4. Mean Ϯ SE days to Þrst oviposition for C. macu- the untreated chrysanthemums (10.6 d after bioassay) lata. These beetles were conÞned to imidacloprid-treated and the untreated dandelions (15.0 d after bioassay) plants, untreated plants, or starvation arenas for 7 d, then kept had a longer delay. Differences in pollen quality could individually in petri dishes and fed artiÞcial diet daily for the have a signiÞcant impact on preoviposition time or egg subsequent 30 d. Day of Þrst oviposition was recorded for production rate (Hodek and Honek 1997). Further- each ovipositing beetle beginning with the Þrst day in petri more, the difference in beetle ages and colony sources dishes. See Table 1 for ANOVA results. could account for the differences in fecundity. Systemic insecticides and plant-expressed toxins that behave like systemics are commonly thought to bioassay. This difference in magnitude of the treat- have minimal impact on nontarget organisms. Genet- ment effect among the plant systems could be the ically engineered crops, containing a gene from Ba- result of a differing amount of imidacloprid present in cillus thuringiensis variety kurstaki (Berliner) that en- the pollen or plant, or it could be the result of pref- codes for the expression of an insecticidal toxin erential feeding by the beetles on sunßower pollen. If, speciÞc to Lepidoptera, are currently available in the through preferential feeding, beetles in the sunßower United States and their use is likely to increase (Ostlie bioassay received a larger dose, we would expect the et al. 1997, Hilbeck et al. 1998a). Several studies dem- magnitude of the effects to be greater. Despite the onstrate the minimal nontarget effects of this plant- differences in magnitude, the effects of imidacloprid expressed toxin on beneÞcial insects. Chrysoperla car- on general mobility are signiÞcant in each plant sys- nea Stephens, Coleomegilla maculata, and Orius tem. insidiosus (Say) had no changes in mortality or de- Survivorship was signiÞcantly reduced by exposure velopment time after eating pollen from corn, Zea to imidacloprid only in the sunßower bioassay (Fig. 3). mays L., expressing the B. thuringiensis variety kurstaki Similarly, oviposition was signiÞcantly delayed by ex- gene (Pilcher et al. 1997). H. convergens larvae and posure to imidacloprid only in the sunßower system adults were unaffected by exposure to Myzus persicae (Fig. 4). These data are based on a small sample; 9 (Sulzer), green peach aphid, reared on potatoes, So- surviving beetles laid eggs in the 1ϫ treatment and lanum tuberosum L., expressing the B. thuringiensis only 4 beetles produced eggs in the 2ϫ treatment variety tenebrionis gene, which is the B. thuringiensis (Table 1). Beetles in the sunßower bioassay could variety speciÞc to beetles (Dogan et al. 1996). have received a higher dose of imidacloprid because Other studies, however, illustrate the potential for of higher levels present in the plant, or because of plant-expressed toxins to affect nontarget organisms. preferential feeding on sunßower pollen or nectar. Hilbeck et al. (1998a) found that C. carnea larvae, Additionally, beetles used in the sunßower bioassay reared on B. thuringiensis variety kurstaki-fed Ostrinia were slightly older. This could inßuence both their nubilalis (Hu¨ bner) larvae, suffered higher mortality survivorship and fecundity. However, the 3 plant sys- and longer developmental time than C. carnea reared tems revealed the same pattern of effects on C. macu- on B. thuringiensis-free larvae (Hilbeck et al. 1998a). lata behavior, which is the critical result for this study. Also, B. thuringiensis variety kurstaki incorporated into There are several possible mechanisms for the ef- artiÞcial diet led to higher mortality and slower de- fects of imidacloprid on the behavior of C. maculata. velopment time for C. carnea, indicating B. thuringien- The beetles may have been exposed to the imidaclo- sis has a direct toxic effect on the predator (Hilbeck prid by consuming it through the pollen or nectar, by et al. 1998b). Losey et al. (1999) demonstrated the tarsal contact with the leaf or petal surface, or by direct toxic and sublethal effects of pollen from corn contact with a vapor layer around the plant. In the case expressing the B. thuringiensis toxin. Larvae of Danaus of the dandelion bioassay, no foliage was included in plexippus (L.) reared on milkweed leaves, Asclepias the mason jars and only ßower heads were brought curassavica L., dusted with pollen from corn express- from the greenhouse. Therefore, any observed treat- ing the toxin ate less, grew more slowly, and suffered ment effects in the dandelion bioassay are the result higher mortality than larvae given pollen from B. thu- of contact with the ßower head. This implies that the ringiensis-free corn or larvae given no pollen. imidacloprid was translocated to the ßower head and Imidacloprid, a chloronicotynol, works on a wider affected beetles either through ingestion, contact with range of taxa than the more speciÞc varieties of B. 1194 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 6 thuringiensis. Consequently, nontarget effects of imi- Ffrench-Constant, R. H., and G. P. Vickerman. 1985. Soil dacloprid may occur in a broad range of insect taxa. contact toxicity of insecticides to the European earwig Sclar et al. (1998) showed nontarget effects of imida- Forficula auricularia (Dermaptera). Entomophaga 30: cloprid on the heteropteran O. tristicolor (White). 271Ð278. Wallner et al. (1999) found that Phacelia tanacetifolia Flanders, R. V. 1986. Potential for biological control in ur- Bentham excrete 3Ð10 ppb of imidicloprid in the nec- ban environments, pp. 95Ð127. In G. W. Bennet and J. M. Owens [eds.], Advances in urban pest management. Van tar after seed treatment with Gaucho ([AI] imidaclo- Nostrand Reinhold, New York. prid). This concentration, however, had no effect on Gordon, R. D. 1985. The Cocinellidae (Coleoptera) of behavior or survivorship of the honey bee, Apis mel- America north of Mexico. J. N.Y. Entomol. Soc. 93: 1Ð912. lifera L. When sucrose containing imidacloprid at con- Hagen, K. S. 1986. Ecosystem analysis: plant cultivars centrations Ͼ20 ppb was fed to honey bees, it caused (HPR), entomophagous species and food supplements, a reduction in foraging behavior and induced changes pp. 151Ð197. In D. J. Boethel and R. D. Eikenbary [eds.], in the dancing behavior that discouraged bees that Interactions of plant resistance and parasitoids and pred- were not fed imidacloprid-treated sucrose from for- ators of insects. Wiley, New York. aging (Kirchner 1999). Our study conÞrms the poten- Hanks, L. M., and R. F. Denno. 1993. The white peach scale, tial for systemic imidacloprid to have nontarget effects Pseudaulaspis pentagona (Targioni-Tozzetti) (Homoptera: Diaspididae): life history in Maryland, host plants, and nat- on the behavior and Þtness of a common predator, C. ural enemies. Proc. Entomol. Soc. Wash. 95: 79Ð98. maculata. Widespread use of imidacloprid in many Hilbeck, A., M. Baumgartner, P. M. Fried, and F. Bigler. urban systems may reduce the general mobility and 1998a. Effects of transgenic Bacillus thuringiensis-corn- number of C. maculata present in these systems. These fed prey on mortality and development time of immature effects could in turn increase pest populations by Chrysoperla carnea (Neuroptera: Chrysopidae). Environ. reducing or eliminating predation by the commonly Entomol. 27: 480Ð487. found C. maculata. Hilbeck, A., W. J. Moar, M. Pusztai-Carey, A. Filippini, F. Bigler. 1998b. Toxicity of Bacillus thuringiensis Cry1Ab toxin to the predator Chrysoperla carnea (Neuroptera: Acknowledgments Chrysopidae). Environ. Entomol. 27: 1255Ð1263. Hodek, I., and A. Honek. 1997. Ecology of Coccinelidae. We thank J. Dreis (Department of Entomology, University Kluwer, Dordrechedt. of Minnesota) for his help in carrying out the bioassays and Kirchner, W. H. 1999. Mad-bee-disease? Sublethal effects maintaining the beetles. We also thank the staff at the Como of Imidacloprid (“Gaucho”) on the behavior of honey- Park Conservatory (St. Paul, MN) for providing greenhouse bees. Apidologie 30: 422. space and growing the plants used in the bioassays. We thank Losey, J. E., L. S. Rayor, and M. E. Carter. 1999. Transgenic G. E. Heimpel (Department of Entomology, University of pollen harms monarch larvae. Nature (Lond.) 399: 214. Minnesota) for providing beetle diet. We thank G. E. He- Merritt, R. W., M. K. Kennedy, and E. F. Gersabek. 1983. impel, W. D. Hutchison (Department of Entomology, Uni- Integrated pest management of nuisance and biting ßies versity of Minnesota), and H. M. Pellett (Department of in a Michigan resort: dealing with secondary pest out- Horticultural Science, University of Minnesota) for review- breaks, pp. 277Ð299. In G. W. Frankie and C. S. Koehler ing the manuscript and giving many helpful suggestions. This [eds.], Urban entomology: interdisciplinary perspectives. research was supported by a 1997 Minnesota Department of Praeger, New York. Agriculture Biological Control grant paper 99117-0225- Mizell, R. F., and M. C. Sconyers. 1992. Toxicity of imida- Project MIN-17027. cloprid to selected predators in the laboratory. Fla. Entomol. 75: 277Ð280. Mullins, J. W. 1993. Imidacloprid: a new nitroguanidine in- References Cited secticide, pp. 183Ð189. In S. O. Duke, J. J. Menn, and J. R. Atallah, Y. H., and L. D. Newsom. 1966. Ecological and Plimmer [eds.], Pest control with enhanced environmen- nutritional studies on Coleomegilla maculata De Geer tal safety. American Chemical Society Symposium, ACS, (Coleoptera: Coccinellidae). I. The Development of an Washington DC. artiÞcial diet and laboratory rearing technique. J. Econ. Ostlie, K. R., W. D. Hutchison, and R. L. Hellmich. 1997. Bt Entomol. 59: 1173Ð1179. corn and . NCR publication 602. Boiteau, G., and W.P.L. Osborn. 1997. Behavioural effects University of Minnesota, St. Paul. of imidacloprid, a new nicotynal insecticide, on the po- Pilcher, C. D., J. J. Obrycki, M. E. Rice, and L. C. Lewis. 1997. tato aphid, Macrosiphum euphorbiae (Thomas) (Ho- Preimaginal development, survival, and Þeld abundance moptera: Aphididae). Can. Entomol. 129: 241Ð249. of insect predators on transgenic Bacillus thuringiensis Boyd, M. L., and D. J. Boethel. 1998. Residual toxicity of corn. Environ. Entomol. 26: 446Ð454. selected insecticides to Heteropteran predaceous species Raupp, M. J., C. S. Koehler, and J. A. Davidson. 1992. Ad- (Heteropotera: Lygaeidae, Nabidae, Pentatomidae) on vances in implementing integrated pest management for . Environ. Entomol. 27: 154Ð160. woody landscape plants. Annu. Rev. Entomol. 37:561:585. Cobb, P. P. 1997. Biorational suppression of pests in land- SAS Institute. 1998. UserÕs manual, version 7.0. SAS Insti- scapes. J. Agric. Entomol. 14: 333Ð337. tute, Cary, NC. Croft, B. A. 1990. Arthropod biological control agents and Sclar, D. C., D. Gerace, and W. S. Cranshaw. 1998. Obser- pesticides. Wiley, New York. vations of population increases and injury by spider Dogan, E. B., R. E. Berry, G. L. Reed, and P. A. Rossignol. (Acari: Tetranychidae) on ornamental plants. J. Econ. 1996. Biological parameters of convergent lady beetle Entomol. 91: 250Ð255. (Coleoptera: Coccinellidae) feeding on aphids (Ho- Terry, L. A., D. A. Potter, and P. G. Spicer. 1993. Insecti- moptera: Aphididae) on transgenic potato. J. Econ. En- cides affect predatory and predation on Jap- tomol. 89: 1105Ð1108. anese beetle (Coleoptera: Scarabaeidae) eggs and fall December 1999 SMITH AND KRISCHIK:EFFECTS OF IMIDACLOPRID ON C. maculata 1195

armyworm (Lepidoptera: Noctuidae) pupae in turfgrass. West, B. 1998. An interior perspective. Lawn Landsc. 19: J. Econ. Entomol. 86: 871Ð878. 90Ð114. Wallner, K., A. Schur, and B. Sturz. 1999. Tests regarding the danger of the seed disinfectant, Gaucho, for bees. Received for publication 26 May 1999; accepted 18 August Apidologie 30: 423. 1999.