Effect of Insecticides on Tiphia Vernalis (Hymenoptera: Tiphiidae)

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BIOLOGICAL AND MICROBIAL CONTROL Effect of Insecticides on Tiphia vernalis (Hymenoptera: Tiphiidae) Oviposition and Survival of Progeny to Cocoon Stage When Parasitizing Popillia japonica (Coleoptera: Scarabaeidae) Larvae

JASON B. OLIVER, CATHARINE M. MANNION,1 MICHAEL G. KLEIN,2 JAMES J. MOYSEENKO,2 3 AND BERT BISHOP

Institute of Agricultural and Environmental Research, Tennessee State University, TSU Otis L. Floyd Nursery Research Center, McMinnville, TN 37110

J. Econ. Entomol. 98(3): 694Ð703 (2005) ABSTRACT The effect of insecticides on oviposition of Tiphia vernalis Rohwer and subsequent survival of parasitoid progeny to the cocoon stage was determined in the laboratory by using larval Japanese beetle, Popillia japonica Newman, as the host. Insecticides tested were imidacloprid, thiamethoxam, halofenozide, chlorpyrifos, and carbaryl at labeled rates. Female T. vernalis were allowed 2 d to parasitize P. japonica larvae after the parasitoids had received a 4-d exposure to insecticide- treated soil. Another group of female T. vernalis were allowed2dtoparasitize P. japonica larvae that had been exposed to insecticide-treated soil for 3Ð4 d. Percentage of parasitism of P. japonica larvae in these trials after exposure of adult parasitoids to carbaryl, chlorpyrifos, halofenozide, or imidacloprid-treated soil (23.3Ð50.0%) or adult parasitoids to chlorpyrifos, halofenozide, or imidacloprid- treated grubs (33.0Ð56.7%) was not negatively affected relative to the control treatment (21.7Ð54.2%). A third group of adult T. vernalis and P. japonica larvae were simultaneously exposed to chlorpyrifos or carbaryl treatments. Percentage parasitism in these trials was lower for T. vernalis adults exposed to the chlorpyrifos and carbaryl (15.0Ð25.0%) relative to the control (57.5Ð62.5%) with the exception of one trial with carbaryl (40.0%). However, exposure of the parasitoid and P. japonica to chlorpyrifos 0.5ϫ, carbaryl 0.5ϫ, imidacloprid, halofenozide, or thiamethoxam in several trials resulted in parasitism that was equivalent or greater than (45.0Ð80.0%) the untreated control (57.5Ð62.5%). Japanese beetle larval mortality in these trials was greater in the insecticide and parasitoid combination (97.5Ð100.0%) than with insecticides alone (45.0Ð100.0%). Percentage of survival of T. vernalis progeny to the cocoon stage was not negatively affected by a 4-d adult parasitoid exposure to carbaryl and chlorpyrifos treated soil (11.7Ð16.7% versus 18.3% control) or a 2-d exposure to P. japonica-treated larvae (16.7Ð18.3% versus 28.3% control). However, simultaneous exposure of T. vernalis progeny and P. japonica larvae to chlorpyrifos- and carbaryl-treated soil resulted in no parasitoids surviving to the cocoon stage. Between neonicotinoids, thiamethoxam had more adverse impact on percentage parasitism (52.5%) and survival to the cocoon stage (10.0%) than imidacloprid (80.0 and 32.5%, respectively). Results of this study indicate soil incorporation of imidacloprid and halofenozide had minimal effect on the number of P. japonica larvae parasitized by T. vernalis or survival of T. vernalis progeny to the cocoon stage; therefore, they are more suitable for use with T. vernalis. In contrast, chlorpyrifos, carbaryl, and thiamethoxam lowered the number of T. vernalis progeny surviving to the cocoon stage, and carbaryl and chlorpyrifos reduced the number of P. japonica larvae parasitized. The soil incorporation of insecticides is discussed as one explanation for the minimal effects of some insecticides on T. vernalis.

KEY WORDS Tiphia vernalis, Japanese beetle, Popillia japonica, compatibility, insecticides

JAPANESE BEETLE, Popillia japonica Newman, was intro- The rapid spread of the beetle throughout the eastern duced into the United States Ϸ1916 in New Jersey. United States is attributed to a favorable climate, abundant host plants, and lack of natural enemies 1 University of Florida, TREC, 18905 SW 280th St., Homestead, FL (Fleming 1976). The current distribution of Japanese 33031. beetle includes most states east of the Mississippi River 2 USDAÐARS Application Technology Research Unit, Horticultural and established populations in Nebraska, Minnesota, Insects Group, 1680 Madison Ave., Wooster, OH 44691. and Wisconsin with potential localized sites in Texas 3 Ohio Agricultural Research and Development Center, Computing and Statistical Services, 1680 Madison Ave., The Ohio State University, and Colorado (Vittum et al. 1999, Potter and Held Wooster, OH 44691. 2002).

0022-0493/05/0694Ð0703$04.00/0 ᭧ 2005 Entomological Society of America June 2005 OLIVER ET AL.: EFFECT OF INSECTICIDES ON T. vernalis 695

Japanese beetles are very effective at population dis- 1940, Rogers and Potter 2004b). Females locate Jap- persal with an average range expansion of Ϸ8 km/yr anese beetle larvae in the soil with the aid of grub- (Fleming 1972). Additionally, adult beetle introduc- produced kairomones and probably other unknown tions into new U.S. locations have occurred through factors (King and Parker 1950, Rogers and Potter accidental transport on aircraft (National Agricultural 2002b). After locating the grub, the wasp stings the Pest Information Service 2004). The larval stages of larva causing temporary paralysis and deposits a Japanese beetle are soil inhabiting; therefore, move- single egg (occasionally two eggs) on the grub. The ment of plant materials grown in containers or as T. vernalis larva subsequently feeds as an ectoparasite balled and burlapped also may disperse the beetle. on the host grub, killing the grub and forming a cocoon Current infestations in Louisiana, Kansas, Minnesota, within 4 wk (Gardner 1938, Rogers and Potter 2002b). and Wisconsin have been attributed to movement of A single female T. vernalis can lay 40Ð50 eggs during P. japonica larvae through the nursery trade (Haanstad its life span (King and Parker 1950). The duration of 1997, Schreiber 1997, Mannion et al. 2001). The move- the egg and larval stage is Ϸ1 and 3 wk, respectively ment of plant material that may contain Japanese bee- (Gardner 1938). Larval parasitoids form cocoons tle was regulated by a federal quarantine until 1978 shortly after death of the host grub and complete the (Blosser 1999). The U.S. Japanese Beetle Domestic transformation from pupae to adult by late summer Harmonization Plan now provides guidelines for the (King and Parker 1950). The adult wasp overwinters movement of nursery plants and turfgrass from regions in the cocoon (King and Parker 1950). with Japanese beetle to partially or noninfested areas The compatibility of beneÞcial insects with insec- (Blosser 1999, National Plant Board 2004). ticides can increase the success of pest management Several natural enemies in the United States attack efforts because some insecticides can be used without Japanese beetle. Naturally occurring microorganisms inhibiting the control provided by biological agents include milky spore, Paenibacillus popilliae Dutky; (Bradley 1999, Kunkel et al. 1999, Rogers and Potter fungi such as Metarhizium anisopliae (Metsch) Sorok 2003). Insecticides will continue to be used to manage and Beauveria bassiana (Balsamo) Vuill.; and ento- Japanese beetles in nurseries and turf areas for regu- mopathogenic nematodes, including Heterorhabditis latory purposes and prevention of crop damage. The bacteriophora Poinar and Steinernema glaseri Steiner application timing of several insecticides used to con- (Fleming 1968). Approximately 49 natural enemies of trol or manage Japanese beetles and other nursery Japanese beetle have been imported into the United pests can overlap with the ßight season of T. vernalis States (Fleming 1976, Potter and Held 2002). Among (Bloetscher et al. 2001, Rogers and Potter 2003, Hale the parasitoids, only two imported from China and 2004). There is minimal information in the literature Korea during the 1930s have successfully established regarding the impact of insecticides on tiphiids (Chen in the United States (Fleming 1968, 1976). The ta- et al. 1999, Rogers and Potter 2003). Insecticides that chinid Istocheta aldrichi Mesnil, which became estab- interact negatively with T. vernalis could be detrimen- lished in the northeastern United States, attacks the tal to Japanese beetle and oriental beetle manage- Japanese beetle adult stage. Tiphia vernalis Rohwer, ment, because there are only two parasitoids estab- the other parasitoid, attacks Japanese beetle larvae in lished in the United States that have potential to the spring. T. vernalis occurs in Kentucky, North Caro- control the pests in nurseries and turf settings (Reding lina, Ohio, and Tennessee (Mannion 1998, Klein 2001, and Klein 2001; Rogers and Potter 2002a, 2003). The Rogers and Potter 2003). The U.S. Department of purpose of this study was to determine the effects of Agriculture has used both I. aldrichi and T. vernalis for several soil-incorporated insecticides on the ability of the management of Japanese beetle near areas that T. vernalis to parasitize Japanese beetle larvae in the pose a risk for movement of the pest such as airports laboratory. and nurseries (Tanner et al. 1997). It has been pro- posed that biological control agents such as T. vernalis Materials and Methods may have potential to slow the spread of the Japanese beetle into other regions (McDonald and Taylor Adult female T. vernalis, distinguished from males 1998). by a larger abdomen with rounded posterior tip, were T. vernalis has been shown to be effective in con- collected for 2Ð3 d before conducting experiments. trolling oriental beetle, Anomala (ϭExomala) orien- Female wasps were collected along the perimeter of talis Waterhouse, and Japanese beetle larvae (here- a commercial nursery near Tarlton, TN. Collections after referred to as grubs) (King and Parker 1950, were made in late April and early May for each test Reding and Klein 2001, Rogers and Potter 2002a). The year, because the time interval was near the beginning occurrence of adult T. vernalis (hereafter referred to of Þeld occurrence for female wasps in Tennessee. as wasp) coincides with the presence of third stadia Early Þeld collection of females was an effort to re- Japanese beetle in the spring. Wasps emerge and are duce variability in the age of the cohort (Rogers and active from early to mid-April into June depending on Potter 2003). Wasps were attracted by spraying a 10% geographic location (Rogers and Potter 2004a, b; (wt:vol) sugar water solution with a Spraymaster J.B.O. and M.G.K., unpublished data). Male emer- Sm-87 (Delta Industries, Philadelphia, PA) trigger- gence precedes female appearance. Both sexes feed operated pump sprayer on uncultivated plants (pri- on insect-produced honeydew or plant-associated marily Lonicera japonica Thunberg) growing along a sugar secretions (Gardner 1938, Gardner and Parker fencerow. Daily captures were combined in a 30-cm3 696 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 3

Table 1. Insecticides used in all experiments, including chemical and trade names, formulations, manufacturers, and rates based on labeled amount of product and active ingredient

Rates/AI Chemical name Trade name Formulation Manufacturera Rateb Productc g/kg soil kg/ha lb/acre Carbaryl Sevin XLR Rohm 0.5ϫ 11.1 ␮l 0.004 4.48 4.0 1.0ϫ 22.2 ␮l 0.008 8.97 8.0 Chlorpyrifos Dursban 4E Dow 0.5ϫ 2.75 ␮l 0.001 1.12 1.0 1.0ϫ 5.5 ␮l 0.002 2.24 2.0 Halofenozide Mach2 2SC Dow 1.0ϫ 11.1 ␮l 0.002 2.24 2.0 Imidacloprid Marathon 60WP Olympic 1.0ϫ 8.04 mg 0.0004 0.45 0.4 Thiamethoxam Flagship 25WG Syngenta 1.0ϫ 1.45 mg 0.00027 0.29 0.26

a Rohm, Rohm and Hass, Spring House, PA (company does not currently exist); Dow, Dow AgroSciences LLC, Indianapolis, IN; Olympic, Olympic Horticultural Products, Atlanta, GA; Syngenta, Syngenta Crop Protection, Inc., Greensboro, NC. b 1.0ϫ is labeled rate. c Amount of insecticide added to 165 ml of water and then mixed into 1.34 kg of soil. This amt of insecticide product is equivalent to the estimated active ingredient in the last three columns. aluminum insect cage (BioQuip, Rancho Dominguez, MO) in a plastic bag until the entire soil sample CA) to randomize parasitoids used in the experiments. seemed moist (Ϸ5 min). A 5-liter plastic pan Þlled with moistened sphagnum All experiments were conducted at a temperature moss was placed in the cage. A 2-cm piece of cotton of 20.7 Ϯ 0.2ЊC (measured by hygrothermograph dental wick was placed in a plastic weigh boat (41 mm2 model 5020-A, Weathertronics Division of Qualimet- by 8 mm in height) and saturated with 10% sugar water rics, Inc., Sacramento, CA) and a constant light reg- as a food source for the parasitoids. Third instars of imen of 12.3 Ϯ 0.37 ␮mol/m2/s as measured with a Japanese beetles were collected from a commercial Quantum Light Meter model QMSV (Apogee Instru- sod farm during mechanical harvesting. All grubs were ments, Inc., Logan, UT). Grubs and wasps were held collected 1Ð3 d before conducting experiments. Grubs in Fisherbrand PE short (Fisher, Pittsburgh, PA) were stored in moist Waynesboro loam (WaB) soil 237-ml plastic cups with 45 g of soil per cup. Five holes (U.S. Soil Conservation Service 1967) collected from were perforated in the lid of each cup using a dissect- the Otis L. Floyd Nursery Research Center, McMinn- ing probe. Wasps were provided with a cotton dental ville, TN, and held in 9.5-liter plastic dishpans (100 wick (2 cm in length) saturated in 10% sugar water as grubs per pan) at Ϸ22ЊC. a food source. Grubs were placed on the soil surface To prepare soil for the laboratory experiments, and allowed to enter the soil without assistance 2 h Waynesboro loam (WaB) soil was collected at a before conducting the experiments. Grubs that failed depth of 5Ð10 cm beneath the thatch zone from a to enter the soil within 15 min were replaced with pasture of predominantly tall fescue, Festuca arundi- another one. Japanese beetle larval mortality was as- nacea Schreb. variety Kentucky 31, and orchard grass, sessed using a combination of characteristics, includ- Dactylis glomerata L. maintained by periodic mowing. ing browning of the integument and moribund re- Soil (0.2-m3 volume) was sifted through a screen sponse to gentle probing (absence of C-shape curling (0.063-cm2 openings), steam sterilized in a soil ster- response and movement of maxillary palps). One wasp ilizer (Pro-Grow Supply, BrookÞeld, WI) at the max- was placed per cup with two third instars of Japanese imum setting (93.4ЊC), and oven-dried at 60 Ϯ 5ЊC. beetles for 2Ð3 d because maximum T. vernalis para- The soil was stored in a 121-liter plastic container until sitism occurs within 48 h under laboratory conditions used for the experiments. Soil used in the experiments (Mannion 1998). Grub parasitism was assessed by ex- was remoistened to an equivalent of 123 ml water/kg amining the anterior region of the ventral abdomen for soil, which was Ϸ47% of the satiation point. Satiation the presence of an egg 6Ð8 d after exposure to wasps point was estimated according to recommendations and insecticides. Voucher specimens of T. vernalis and (Jury et al. 1991) by adding water to 100 g of soil Japanese beetle larvae have been deposited in the until shallow ponding occurred on the soil surface. insect collection maintained at the Tennessee State Several insecticides used in turf and nursery settings University Otis L. Floyd Nursery Research Center, were selected, including an organophosphate (chlor- McMinnville, TN. pyrifos), a carbamate (carbaryl), two neonicotinoids Data Collection and Analysis. Data collected in- (imidacloprid and thiamethoxam), and an ecdysone cluded number of Japanese beetle larvae parasitized agonist (halofenozide) (For more information refer to (zero, one, or two) and survival of T. vernalis larvae to Table 1). Pesticide rate per unit of soil was estimated the cocoon stage (based on complete cocoon forma- using methods developed by Tashiro and Neuhauser tion). The deÞnition of parasitism in this study was the (1973). To prepare treated soil, 1.34 kg of dry soil was presence of a T. vernalis egg on the ventral abdomen mixed with an insecticide solution (165-ml volume) of the host grub at the time the grub was examined. and a 15-ml volume of Kwik grass (annual Lolium Occasionally, T. vernalis will lay two eggs on a host multiﬂorum Lam. [88%] and perennial Lolium perenne grub; however, grubs with one or more eggs were all L. [8%] ryegrass) (Pennington Seed Inc., GreenÞeld, counted as parasitized. Average percentage of para- June 2005 OLIVER ET AL.: EFFECT OF INSECTICIDES ON T. vernalis 697

-Table 2. Mean ؎ SE percentage of parasitism of third instars of Japanese beetle by adult female T. vernalis exposed to insecticide treated soil, or insecticide-treated grubs and mean ؎ SE percentage of survival of parasitoid progeny to the cocoon stage

Wasp exposure method Insecticide-treated soil Insecticide-treated grubs Trial Treatment Rate n % survival of % survival of % grubs % grubs parasitoid progeny parasitoid progeny parasitizeda parasitizeda to cocoonb to cocoonb

1 (1999) Imidacloprid 1ϫ 60 23.3 Ϯ 5.5a 6.6 Ϯ 3.2a 53.3 Ϯ 6.4a 8.3 Ϯ 3.6a Halofenozide 1ϫ 60 40.0 Ϯ 6.3a 20.0 Ϯ 5.2b 53.3 Ϯ 6.4a 25.0 Ϯ 5.6b Untreated 58 39.7 Ϯ 6.3a 19.0 Ϯ 5.1b 52.5 Ϯ 6.4a 22.0 Ϯ 5.4b 2 (1999) Imidacloprid 1ϫ 60 35.0 Ϯ 6.2ab 5.0 Ϯ 2.8a 49.2 Ϯ 6.5a 27.1 Ϯ 5.7a Halofenozide 1ϫ 60 50.0 Ϯ 6.5b 10.0 Ϯ 3.9a 56.7 Ϯ 6.4a 25.0 Ϯ 5.6a Untreated 60 21.7 Ϯ 5.3a 5.0 Ϯ 2.8a 54.2 Ϯ 6.4a 18.6 Ϯ 5.0a 3 (2000) Carbaryl 1ϫ 60 38.3 Ϯ 6.3a 16.7 Ϯ 4.8a 31.7 Ϯ 6.0a 18.3 Ϯ 4.9a Chlorpyrifos 1ϫ 60 40.0 Ϯ 6.3a 11.7 Ϯ 4.1a 33.0 Ϯ 6.1ab 16.7 Ϯ 4.8a Untreated 60 43.3 Ϯ 6.4a 18.3 Ϯ 4.9a 50.0 Ϯ 6.5b 28.3 Ϯ 5.8a

Means within column by trial followed by a different letter were signiÞcantly different (P Ͻ 0.05) as indicated by binary logistic analysis and ␹2 comparisons (Minitab Inc. 2003). a Number of Japanese beetle grubs with a single T. vernalis egg on the ventral thorax divided by the total number of grubs. For each replicate, the three possible outcomes were no grubs parasitized (0%), one grub parasitized (50%), or two grubs parasitized (100%). b Number of T. vernalis larvae forming cocoons divided by the total number of Japanese beetle grubs. sitism was calculated by converting the number of rameters were the same for both trials. A single adult Japanese beetle larvae parasitized in each replicate to female T. vernalis was exposed to treated soils (de- a percentage (0, 50, or 100%) and averaging within scribed previously) for 4 d and then removed and treatments. For grubs parasitized with a T. vernalis placed into a separate cup containing moistened un- egg, survival of the parasitoid egg and larva to the treated laboratory soil and grass seed (described pre- cocoon stage after a 5Ð6-wk period was used to deÞne viously) and two third instars of Japanese beetles. parasitism success, although the parasitoid was not Each treatment was replicated 30 times. Wasps were followed after this point to determine whether wasp allowed to parasitize grubs for 2 d before being re- emergence from the cocoon occurred. For experi- moved, and Japanese beetle larvae were assessed for ment 3, the number of dead Japanese beetle larvae parasitism after 5 d. Observations were made after (mortality) also was collected for insecticide and wasp 5 wk to determine cocoon development. Data collec- treatments. Comparisons of the insecticide treatment tion and analysis was described previously (see “Data effects on number of grubs parasitized, survival of Collection and Analysis”). wasp progeny to the cocoon stage, and Japanese beetle 2000. The procedures used in both 1999 trials were mortality were analyzed using binary logistic analysis repeated for a laboratory trial (Table 2, trial 3). In- (␣ ϭ 0.05) (Agresti 1996, Minitab Inc. 2003). All ex- secticide treatments included chlorpyrifos and car- periments were arranged in a completely randomized baryl. Wasps were allowed to parasitize grubs for 2 d design. The results of this study are presented as per- before removal, and Japanese beetle larvae were as- centages, but the data were actually binary response sessed for parasitism after 6 d. Observations were data, and therefore, transformations were not neces- made after 6 wk to determine cocoon development. sary. Each Japanese beetle grub provided one datum. Data collection and analysis was previously described. Logistic analyses or analyses of tables of counts using Experiment 2: Parasitoid Exposure to Insecticide- the ␹2 statistics are appropriate for binary response Treated Grubs. 1999. Two laboratory trials were per- data (Agresti 1996). To compare percentages, the test formed to determine percentage of parasitism of arising from the logistic analysis is generally preferred grubs previously exposed to insecticides by T. vernalis to the ␹2 statistics because it is more powerful (Agresti (Table 2, trials 1 and 2). Eighty third instars of Japa- 1996). All statistical results are from logistic analyses. nese beetle were exposed simultaneously to insecti- However, when the cell of a table is 0 (i.e., the sum- cide- or nontreated (control) soil in 9.5-liter dishpans. mary response is all alive [0%] or all dead [100%]) After exposure to soil treatments for 4 d, 60 live grubs there are problems calculating a logistic analysis. For were removed from each dishpan and transferred to a these cases, all comparisons for that treatment used a cup (two grubs per cup) with 45 g of nontreated soil. ␹2 statistics generated from 2 by 2 tables with an A single female wasp was added to the cup after 2 h. associated test or P value to compare that treatment Each treatment was replicated 30 times. Wasps were level with other treatment levels on a pairwise basis. allowed to parasitize grubs for 2 d before being re- For all statistical analyses signiÞcant Þndings are at P Ͻ moved and Japanese beetle larvae were assessed for 0.05 (df ϭ 1). parasitism after 5 d. Observations were made after 5 Experiment 1: Parasitoid Exposure to Insecticide- wk to determine cocoon development. Data collec- Treated Soil. 1999. Two laboratory trials were per- tion and analysis were previously described. formed to test the effect of direct parasitoid exposure 2000. The procedures used in both trials for 1999 to insecticides (Table 2, trials 1 and 2). All test pa- were repeated in a laboratory trial by using only chlor- 698 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 3

؎ Table 3. Mean ؎ SE percentage of parasitism, mean ؎ SE percentage of survival of parasitoid progeny to the cocoon stage, and mean SE third instar Japanese beetle mortality after exposure to soil incorporated with an insecticide or the combination of soil-incorporated insecticide and T. vernalis for 2000

Wasp ϩ insecticide Insecticide % survival of c c Treatment Rate n % grubs % grub mortality % grub mortality parasitoid progeny parasitizeda to cocoonb 8d42d8d42d Chlorpyrifos 1ϫ 40 15.0 Ϯ 5.7a 0.0 Ϯ 0.0a 77.5 Ϯ 6.6a 100.0 Ϯ 0.0a 65.0 Ϯ 7.5a 100.0 Ϯ 0.0a Carbaryl 1ϫ 40 20.0 Ϯ 6.3a 0.0 Ϯ 0.0a 72.5 Ϯ 7.1a 100.0 Ϯ 0.0a 57.5 Ϯ 7.8a 97.5 Ϯ 2.5ab Halofenozide 1ϫ 40 50.0 Ϯ 7.9b 20.0 Ϯ 6.0b 17.5 Ϯ 6.0b 100.0 Ϯ 0.0a 12.5 Ϯ 5.2b 85.0 Ϯ 5.6b Imidacloprid 1ϫ 40 55.0 Ϯ 7.9b 22.5 Ϯ 6.6b 12.5 Ϯ 5.2b 97.5 Ϯ 2.5a 15.0 Ϯ 5.7b 45.0 Ϯ 7.9c Untreated 40 62.5 Ϯ 7.7b 30.0 Ϯ 7.2b 10.0 Ϯ 4.7b 97.5 Ϯ 2.5a 10.0 Ϯ 4.7b 52.5 Ϯ 7.9c

؎ Table 4. Mean ؎ SE percentage of parasitism, mean ؎ SE percentage of survival of parasitoid progeny to the cocoon stage, and mean SE third instars of Japanese beetle mortality from exposure to soil incorporated with an insecticide or the combination of soil-incorporated insecticide and T. vernalis for 2001

Wasp ϩ insecticide Insecticide % survival c c Treatment Rate n % grubs % grub mortality % grub mortality parasitoid of progeny parasitizeda to cocoonb 7d 35d 7d 35d Chlorpyrifos 1ϫ 40 25.0 Ϯ 6.9a 0.0 Ϯ 0.0a 75.0 Ϯ 6.9a 100.0 Ϯ 0.0a 77.5 Ϯ 6.6a 100.0 Ϯ 0.0a Carbaryl 1ϫ 40 40.0 Ϯ 7.8ab 0.0 Ϯ 0.0a 75.0 Ϯ 6.9a 100.0 Ϯ 0.0a 52.5 Ϯ 7.9b 95.0 Ϯ 3.4ab Chlorpyrifos 0.5ϫ 40 45.0 Ϯ 7.9abc 0.0 Ϯ 0.0a 52.5 Ϯ 7.9b 97.5 Ϯ 2.5ab 22.5 Ϯ 6.6c 87.5 Ϯ 5.2b Carbaryl 0.5ϫ 40 50.0 Ϯ 7.9bc 0.0 Ϯ 0.0a 45.0 Ϯ 7.9b 92.5 Ϯ 4.2abc 47.5 Ϯ 7.9b 67.5 Ϯ 7.4c Thiamethoxam 1ϫ 40 52.5 Ϯ 7.9bc 10.0 Ϯ 4.7b 37.5 Ϯ 7.7b 85.0 Ϯ 5.7bc 15.0 Ϯ 5.6dc 40.0 Ϯ 7.7d Untreated 40 57.5 Ϯ 7.8bc 30.0 Ϯ 7.2c 17.5 Ϯ 6.0c 80.0 Ϯ 6.3c 20.0 Ϯ 6.3c 32.5 Ϯ 7.4d Halofenozide 1ϫ 40 65.0 Ϯ 7.5cd 20.0 Ϯ 6.3bc 15.0 Ϯ 5.7c 82.5 Ϯ 6.0bc 15.0 Ϯ 5.6dc 47.5 Ϯ 7.9cd Imidacloprid 1ϫ 40 80.0 Ϯ 6.3d 32.5 Ϯ 7.4c 10.0 Ϯ 4.7c 90.0 Ϯ 4.7bc 2.5 Ϯ 2.5d 32.5 Ϯ 7.4d

Means within column followed by a different letter were signiÞcantly different (P Ͻ 0.05) as indicated by binary logistic analysis and ␹2 comparisons (Minitab Inc. 2003). a Number of Japanese beetle grubs with a single T. vernalis egg on the ventral thorax divided by the total number of grubs. For each replicate, the three possible outcomes were no grubs parasitized (0%), one grub parasitized (50%), or two grubs parasitized (100%). b Number of T. vernalis larvae forming cocoons divided by the total number of Japanese beetle grubs. c Number of dead Japanese beetle grubs due to either parasitoid or insecticide divided by the total number of grubs. June 2005 OLIVER ET AL.: EFFECT OF INSECTICIDES ON T. vernalis 699 centage of survival of parasitoid larvae to the cocoon posure to the 1ϫ rate of chlorpyrifos resulted in lower stage in the imidacloprid treatment was nearly 3 times attack rates on grubs (based on percentage of para- lower than the control. In trial 2, wasp exposure to sitism) than halofenozide, imidacloprid, thiame- imidacloprid again had no signiÞcant effect on per- thoxam, carbaryl at 0.5ϫ, and the control. However, centage of grubs parasitized, but wasps exposed to percentage of parasitism in the chlorpyrifos (1ϫ) halofenozide-treated soil parasitized grubs at greater treatment did not differ signiÞcantly from the carbaryl than twice the rate of the control (Table 2). Unlike at 1ϫ or the chlorpyrifos at 0.5ϫ treatments. Grubs in trial 1, no differences were detected between imida- the imidacloprid treatment had greater percentage cloprid compared with the control treatment for the parasitism than the control and all other treatments, survival of progeny to the cocoon stage. except halofenozide. Percentage parasitism was also 2000. The percentage of grubs parasitized and sur- higher in the halofenozide treatment than the chlor- vival of progeny to the cocoon stage were not signif- pyrifos 1ϫ and carbaryl 1ϫ treatments. icantly affected by chlorpyrifos- or carbaryl-treated After 35 d, no parasitoid progeny survived to the soil relative to the control treatment (Table 2). cocoon stage in all the chlorpyrifos or carbaryl treat- Experiment 2: Parasitoid Exposure to Insecticide- ments (Table 4). Imidacloprid had the highest per- Treated Grubs. 1999. For trial 1, the percentage of centage of survival to the cocoon stage (32.5%) after grubs parasitized was not signiÞcantly affected rela- 35 d; however, survival was not signiÞcantly different tive to the control treatment when wasps were ex- from that of the control or halofenozide treatments. posed to imidacloprid- or halofenozide-treated grubs Parasitoid survival in the thiamethoxam treatment was (Table 2). However, exposure of wasps to imidaclo- signiÞcantly lower (10%) than the control (30%) and prid-treated grubs reduced the survival to the cocoon imidacloprid (32%) treatments, but not the halofeno- stage by greater than twice the control treatment zide (20%) treatment. (Table 2). In trial 2, there were no signiÞcant differ- Japanese beetle larval mortality was similar to the ences between wasps exposed to imidacloprid or results detailed in 2000 (Table 4). In general, the range halofenozide compared with the control treatment for of grub mortality after 7 d was greater for many of the either percentage of grubs parasitized or progeny sur- carbaryl and chlorpyrifos treatments, whether grubs vival to the cocoon stage. were exposed to both T. vernalis and insecticides or 2000. Carbaryl lowered the percentage of grubs insecticides alone. After 7 d, the chlorpyrifos and car- parasitized by nearly half the control percentage; baryl treatments had a percentage grub mortality however, there were no signiÞcant differences among range of 52Ð77% (1ϫ) and 22Ð52% (0.5ϫ), whereas treatments in percentage of survival to the cocoon mortality in the other treatments ranged between 2 stage (Table 2). and 37%. Thiamethoxam along with T. vernalis re- Experiment 3: Simultaneous Exposure of Grubs sulted in higher mortality (Ϸ2ϫ) than the control, and Wasps to Insecticide-Treated Soil. 2000. The ex- halofenozide, and imidacloprid treatments. However, posure of both wasps and grubs to insecticide-treated thiamethoxam did not signiÞcantly differ from the soil resulted in percentage of parasitism that was 3Ð4 latter treatments when T. vernalis was absent. After times lower than the control (Table 3). Likewise, for 35 d, all the chlorpyrifos and carbaryl treatments had the grubs that were parasitized, no T. vernalis progeny higher grub mortality than the other insecticides and survived to the cocoon stage after 5 wk in the chlor- control. For carbaryl and chlorpyrifos, the range of pyrifos- and carbaryl-treated soils, whereas cocoon larval Japanese beetle mortality was only moderately development in the other treatments ranged from higher for treatments with T. vernalis (92Ð100%) than 20Ð30% (Table 3). treatments without (67Ð100%). However, the pres- Percentage of mortality of Japanese beetle larvae ence of T. vernalis with other insecticides resulted in after8dinthecarbaryl and chlorpyrifos treatments higher ranges of Japanese beetle larval mortality (82Ð was Ͼ4 times the mortality of the other treatments, 90%) than without the parasitoid (32Ð47%). regardless of the presence or absence of T. vernalis (Table 3). After 8 d, grub mortality in the soil treated with chlorpyrifos and carbaryl was signiÞcantly Discussion greater (range 57Ð77%) than mortality in the other treatments (range 10 and 17%). After 42 d, all the grubs In this study, chlorpyrifos and carbaryl had a greater exposed to T. vernalis had percentage mortalities that negative impact on parasitism than imidacloprid, ranged from 97 to 100%. However, larvae not exposed thiamethoxam, and halofenozide. The exception was to T. vernalis after 42 d had higher mortality in the trial 3 in 2000 where percentage of parasitism was chlorpyrifos- (100%), carbaryl- (97%), and halofeno- similar among the control, chlorpyrifos, and carbaryl zide (85%)-treated soils compared with imidacloprid treatments. A reduction in parasitism rate may indi- (45%) and the control (52%). For halofenozide and cate less attraction to the host grub by the parasitoid imidacloprid treatments, the presence of adult wasps or insecticidal effects on the parasitoid. Insecticidal increased grub mortality. effects could include greater wasp mortality or dis- 2001. Exposure to carbaryl- and chlorpyrifos- ruption of parasitoid host-Þnding ability (Rogers and treated soils again resulted in the greatest reductions Potter 2002b). However, acute insecticide toxicity to in percentage of parasitism and survival to the cocoon adult wasps in this study was minimal, because nearly stage among the treatments (Table 4). Parasitoid ex- all the wasps survived the 2Ð4-d exposure to insecti- 700 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 3 cide-treated soils or 2-d exposure to insecticide- Krohn and Hellpointner 2002). It is unknown whether treated grubs in the experiments. a relationship exists between insecticide properties

The parasitoid and insecticide combinations re- such as Koc and water solubility and the toxicity of sulted in greater grub mortality than treatments with the insecticide to T. vernalis. The soil incorporation only insecticides. However, thiamethoxam, chlorpyr- method was used in this study, because it provided a ifos, and carbaryl also reduced the ability of the larval consistent exposure to both wasps and grubs and is an parasitoid to develop to the cocoon stage relative to accepted method for insecticide bioassays against soil- the control treatment. The exception was trial 3 where feeding insects such as grubs (Tashiro and Neuhauser survival to the cocoon stage was similar among the 1973, Villani et al. 1988). Soil incorporation also re- control, carbaryl, and chlorpyrifos treatments. In most duces the impact of factors such as insecticide accu- trials, the exposure of parasitoids to halofenozide- or mulation in thatch. imidacloprid-treated soils did not reduce parasitism The soil incorporation of halofenozide, imidaclo- rates or survival of parasitoid larvae to the cocoon prid, and thiamethoxam did not prevent wasps from stage relative to the control. Likewise, thiamethoxam locating and parasitizing grubs compared with the did not affect parasitism rates relative to the control, control, but thiamethoxam exposure lowered parasi- but it did reduce parasitoid development to the co- toid development to the cocoon stage. In contrast, coon stage compared with the control. The lower imidacloprid residues on turf cores that had been cocoon formation rates associated with chlorpyrifos surface sprayed affected the ability of T. vernalis to and carbaryl were probably due to the toxicity of these locate and parasitize Japanese beetle larvae (Rogers insecticides to the parasitoid larva or the grub. Wasp and Potter 2003). Likewise, surface sprays of chlor- progeny that survived exposure to insecticide treat- pyrifos, carbaryl, and imidacloprid on grass blades ments were not evaluated past the cocoon stage to and maple leaves increased T. vernalis mortality rel- assess other potential negative effects. For example, a ative to the control, but halofenozide had minimal detrimental effect that is known to occur when imi- effect (J.B.O. and M.G.K., unpublished data). The dacloprid is applied to the soil surface is interference negligible effects on T. vernalis from halofenozide with the parasitoidÕs ability to locate and parasitize exposure, either as a surface spray or soil incorpora- larvae by using grub-produced kairomones (Rogers tion application, likely relates to the selectivity of and Potter 2002b, 2003). this insecticide toward scarab, cutworm, and web- The insecticides tested are labeled for use against worm larvae (Dhadialla et al. 1998, Cowles et al. Japanese beetle larvae and are commonly applied as 1999). Halofenozide and imidacloprid had minimal surface sprays over turf and nursery rows or as foliar impact on beneÞcial arthropods when applied to turf- sprays to control leaf-feeding insects (Turf and grass, and posttreatment irrigation further reduced Ornamental Reference 2004). However, in our study the toxicity of imidacloprid (Kunkel et al. 1999). Based insecticides were soil incorporated. Although soil in- on number of grubs parasitized, thiamethoxam ap- corporation is not widely practiced in turf and nursery parently had properties that did not interfere with settings, subsurface application technology can be T. vernalis hunting ability, but unlike imidacloprid very effective at managing soil pests such as grubs and halofenozide, were toxic to developing para- (Vittum 1994, Reding et al. 2004). Insecticides surface sitoid larvae. Thiamethoxam has the same mode of applied to turf often concentrate in the thatch zone insecticidal action as imidacloprid, but differs in some due to adsorption. For example, several studies have chemical properties such as a water solubility that is reported residue recoveries in the thatch zone ranging 8 times greater than imidacloprid. In this study, the from 90Ð99% for weeks to months after treatment effects of insecticides on T. vernalis progeny were not (Niemczyk and Krueger 1987, Niemczyk et al. 1988, studied past the cocoon stage; therefore, imidacloprid, Stone et al. 1994, Lickfeldt and Branham 1995). In- halofenozide, and thiamethoxam may have had sub- secticides with low water solubility and chemical sequent effects that were not measured. properties that favor strong adsorption to substrates The differences in observed T. vernalis mortality may not enter the upper root zone of the soil where after exposure to soil incorporated imidacloprid ver- grubs feed due to accumulation in the thatch (Vittum sus studies that surface applied imidacloprid, must et al. 1999). Among the insecticides tested, the water be due to factors other than insecticide selectivity, solubility for chlorpyrifos, carbaryl, imidacloprid, because surface-sprayed imidacloprid is known to and thiamethoxam is reported at Ϸ4, 26, 510, and cause behavioral changes or increase mortality in

4,100 ppm and adsorption coefÞcients (Koc) at 7,500, adult T. vernalis shortly after exposure (Rogers and 300, 350, and unknown milligrams per milliliter, re- Potter 2003, J.B.O. and M.G.K., unpublished data). A spectively (Vittum et al. 1999, Technical Bulletin likely explanation is imidacloprid has less soil activity 2000). Halofenozide is listed as dispersible, but spe- against T. vernalis. There was minimal surface vege- ciÞc water solubility and Koc coefÞcients are un- tation and thatch in the soils used in this study, be- available (Turf and Ornamental Reference 2004). The cause test soils were Þeld-collected beneath the thatch water solubility and adsorption coefÞcient for chlor- zone. Differences in behavioral patterns of T. vernalis pyrifos indicate a chemical that will strongly adsorb to adults between surface and soil environments may soil or thatch and therefore be less susceptible to further reduce ingestion or contact exposure between leaching, whereas the other insecticides are in the insecticides that are surface sprayed versus soil incor- range of moderately mobility (Wright et al. 1993, porated. Unlike grubs, which commonly consume soil June 2005 OLIVER ET AL.: EFFECT OF INSECTICIDES ON T. vernalis 701 particles during root feeding, wasps feed almost ex- cides, herbicides, and fungicides that are applied dur- clusively on honeydew produced by Homoptera or ing the adult ßight period by both foliar- and soil- plant secretions (Gardner 1938). However, T. vernalis incorporated methods. This study has shown that soil- regularly groom their legs and antennae like other incorporated halofenozide and imidacloprid had solitary hymenopteron parasitoids (Evans 1966, Rog- minimal impact on the ability of adult T. vernalis to ers and Potter 2003), which would afford an oppor- locate and parasitize Japanese beetle grubs. Likewise, tunity to ingest any insecticide residues on the in- imidacloprid and halofenozide also did not prevent tegument. If imidacloprid residues in thatch are the T. vernalis progeny from developing to the cocoon displaced to the wasp integument more easily than stage. In contrast, thiamethoxam reduced survival of residues in the soil, then studies that surface spray T. vernalis progeny to the cocoon stage, but did not imidacloprid would be likely to cause greater T. ver- prevent adult wasps from locating and parasitizing nalis toxicity. Other studies using multiple insecti- the grubs. Chlorpyrifos and carbaryl both reduced cides, which included carbaryl and chlorpyrifos, parasitism and subsequent progeny survival to the have shown a direct correlation between mortality cocoon stage. Therefore, imidacloprid and halofeno- levels of different parasitic Hymenoptera species and zide, and thiamethoxam to a lesser extent, are gener- the amount of insecticide residue dislodged from fo- ally more compatible with T. vernalis for managing liage (Bellows et al. 1993, Chukwudebe et al. 1997). Japanese beetle grubs. If imidacloprid is applied at a The degree of insecticide volatilization is another fac- time when adult T. vernalis are active, the results of tor that may explain differences in imidacloprid tox- this study indicate soil incorporation or subsurface icity between studies that soil-incorporate versus sur- placement is better than surface application for con- face apply. The type of substrate insecticide residues serving T. vernalis. are deposited on can alter the degree of insecticide volatilization (Antonious and Snyder 1995). Imidaclo- prid may have lower volatility in soil than when sur- Acknowledgments face applied. The toxicity of some insecticides such as We thank Mike Reding, Crystal Lemings, Jimmy Clark, chlorpyrifos is closely related to insecticide volatility Ricky Alexander, and Caleb Graves for assistance with the (Elliott 1988). The vapor pressure of imidacloprid is experiments; a private nursery and turf farm for allowing us lower than that of carbaryl or chlorpyrifos (Vittum et to collect tiphiid wasps and Japanese beetle larvae; and chem- al. 1999), which may explain the lower impact of imi- ical companies Dow AgroSciences LLC, Syngenta Crop Pro- dacloprid on T. vernalis parasitism and progeny sur- tection, Inc., Olympic Horticultural Products, and Rohm and vival observed in this study. A number of additional Haas for providing product for testing. We thank Daniel soil parameters are known to inßuence insecticide Potter, Michael Rogers, and William Klingeman for providing efÞcacy in soil such as organic matter, soil pH, cation outside reviews of this manuscript. We also thank Sam Den- nis and Sam Ochieng for reviewing portions of the manu- exchange capacity, soil moisture, microbial degrada- script dealing with the interaction of insecticides with soils. tion, and temperature (Brady 1984, Cowles and Villani 1994, Callcott et al. 1995). The impact of the other factors on the outcome of this study is unknown. References Cited Turf and nursery management practices might lessen T. vernalis exposure to foliar- or soil-applied Agresti, A. 1996. Categorical data analysis by Alan Agresti. John Wiley and Sons, Inc., New York. insecticides. For example, posttreatment irrigation Antonious, G. F., and J. C. Snyder. 1995. Pirimiphos-methyl may move residues from surface vegetation into the residues and control of greenhouse whiteßy (Homoptera: soil (and thatch) where effects on T. vernalis may be Aleyrodidae) on seven vegetables. J. Entomol. Sci. 30: minimized (Niemczyk and Krueger 1987, Starrett et al. 191Ð201. 1996). Timing of insecticide application also may Bellows, T. S., Jr., J. G. Morse, and L. K. Gaston. 1993. Re- limit T. vernalis exposure. In the central United States, sidual toxicity of pesticides used for lepidopteran insect T. vernalis adults are active from early April to mid- control of citrus to Aphytis melinus DeBach (Hymenop- June (Rogers and Potter 2003). For Japanese beetle tera: Aphelinidae). Can. Entomol. 125: 995Ð1001. control, imidacloprid, halofenozide, and thiameth- Bloetscher, B., W. Pound, J. Rimelspach, D. Shetler, and J. Street. 2001. Management of turfgrass pests: weeds, oxam are most effective when applied from May to diseases, and insects. Ohio State Univ. Ext. Bull. L-187-01. early August, whereas carbaryl and chlorpyrifos rec- Blosser, W. 1999. Japanese beetle quarantines Ðwhere are ommendations specify treatments during a broader we now? Regul. Hortic. 25: 4Ð6. time span (Mannion et al. 2001, Turf and Ornamental Bradley, J. R., Jr. 1999. Integrating new insecticide tech- Reference 2004). Nursery quarantine treatments for nologies in IPM, pp. 384Ð399. In G. G. Kennedy and Japanese beetle by using imidacloprid and halofeno- T. B. Sutton [eds.], Proceedings of the Conference on zide mandate a May to July treatment (National Plant Emerging Technologies for Integrated Pest Management, Board 2004). The application of insecticides after mid- 8Ð10 March 1999, Raleigh, NC. American Phytopatho- June would still meet nursery quarantine require- logical Society Press, St. Paul, MN. Brady, N. C. 1984. Organic matter of mineral soils, pp. 253Ð ments, but it would greatly reduce exposure of adult 282. In N. C. Brady [ed.], The nature and properties of parasitoids to insecticides and allow time for larvae to soils, 9th ed. MacMillan Publishing Company, New York. complete development to the more protected cocoon Callcott, A., H. L. Collins, and T. C. Lockley. 1995. Factors stage. Future research is needed to compare T. vernalis inßuencing residual activity of chlorpyrifos against im- compatibility with other common nursery insecti- ported Þre ants (Hymenoptera: Formicidae) in nursery 702 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 3

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