Relative Repellency and Lethality of the Neonicotinoids ...

3 downloads 0 Views 325KB Size Report
bifenthrin was more toxic to R. flavipes termites than either acetamiprid or thiamethoxam alone. The combination acetamiprid bifenthrin termiticide may be ...
HOUSEHOLD AND STRUCTURAL INSECTS

Relative Repellency and Lethality of the Neonicotinoids Thiamethoxam and Acetamiprid and an Acetamiprid/Bifenthrin Combination to Reticulitermes flavipes Termites JOSEPH A. SMITH, ROBERTO M. PEREIRA,1

AND

PHILIP G. KOEHLER

Department of Entomology and Nematology, University of Florida, P.O. Box 110620, Gainesville, FL 32611

J. Econ. Entomol. 101(6): 1881Ð1887 (2008)

ABSTRACT Field-collected Reticulitermes flavipes (Kollar) termites were placed in bioassay tubes containing soil treated with one of three termiticides: thiamethoxam, acetamiprid, or a combination of acetamiprid ⫹ bifenthrin. In the bioassay tubes, treated soil was placed in a layer centered within untreated sand between two 1.5-cm agar plugs. All termiticides were tested at concentrations of 0.1, 1, 10, and 100 ppm with narrow (1 mm), medium (5 mm), and broad (50 mm) thicknesses of treated soil. Soil penetration and termite mortality were measured after 7 d, and repellency was assessed. Thiamethoxam treatments allowed the greatest soil penetration, whereas acetamiprid ⫹ bifenthrin treatments were the most inhibitory to soil penetration. Thiamethoxam treatments also caused consistently greater termite mortality than acetamiprid treatments. These data indicated that acetamiprid prevented soil penetration by termites more than thiamethoxam, although both were less repellent compared with bifenthrin alone, which causes little termite mortality at the tested doses. When there was direct contact of treated soil with the agar plugs in broad treatments, the combination of acetamiprid ⫹ bifenthrin was more toxic to R. flavipes termites than either acetamiprid or thiamethoxam alone. The combination acetamiprid ⫹ bifenthrin termiticide may be effective in keeping termites away from the treated soil, because of the combined effects of acetamiprid and bifenthrin. KEY WORDS termite mortality, soil penetration, treatment depth, neonicotinoids

The neonicotinoids are among the most commonly used new insecticides (Nauen et al. 2003, Tomizawa and Casida 2003), favored for their relatively low mammalian toxicity. Neonicotinoids are based upon the chemistry of the alkaloid nicotine, and they are generally characterized by a 3-pyridylmethylamine moiety within their structure (Tomizawa and Casida 2003, 2005). Neonicotinoids may be broadly classiÞed as nitromethylenes, nitroguanidines, or cyanoamidines depending on their chemical structure. Most neonicotinoid insecticides have been used for the control of crop pests, but imidacloprid, a nitroguanidine, also has been successfully used as an active ingredient in Premise, a nonrepellent termiticide (Gahlhoff and Koehler 1999, Peterson 2007). Two of the newer neonicotinoids are thiamethoxam, a nitroguanidine, and acetamiprid, a cyanoamidine (MaienÞsch et al. 2001). Neonicotinoids exhibit relatively high water solubility. Acetamiprid has a solubility of 4.25 g/liter in distilled water (U.S. EPA 2008), and thiamethoxam has a solubility of 4.1 g/liter in distilled water as described in the product Material Data Safety Sheet. In contrast with the neonicotinoids, pyrethroid insecticides have been used as repellent soil termiticides 1

Corresponding author, e-mail: rpereira@uß.edu.

for many years. The pyrethroid active ingredients currently in use as soil termiticides are bifenthrin, cypermethrin, and permethrin (Potter 2004). Pyrethroid termiticides are known to be highly repellent to termites, protecting structures by forming a barrier of treated soil that termites will not enter (Smith and Rust 1990, Su and Scheffrahn 1990). Pyrethroids are normally highly insoluble in water (Stephenson 1982). Two factors that affect the efÞcacy of a potential termiticide against subterranean termites are repellency and toxicity (Su et al. 1982). A nonrepellent soil termiticide does little to prevent termite entry into treated soil (Thorne and Breisch 2001, Kubota et al. 2007), but with sufÞcient toxicity it kills any termites in contact with treated soil before they can cause structural damage. A repellent soil termiticide prevents termite entry into treated soil and, provided there are no gaps in treatment, can effectively protect a structure (Gahlhoff and Koehler 1999). However, termiticide repellency prevents termites from acquiring lethal doses, reducing termite mortality in spite of any toxicity (Smith and Rust 1990, Su and Scheffrahn 1990). The intersection of percentage of soil penetration and percentage of termite mortality curves on a graph across termiticide concentrations may provide information on the termiticide repellency (Remmen

0022-0493/08/1881Ð1887$04.00/0 䉷 2008 Entomological Society of America

1882

JOURNAL OF ECONOMIC ENTOMOLOGY

and Su 2005). Gahlhoff and Koehler (1999) reviewed the repellency of available termiticides and determined that all pyrethroids are highly repellent to termites. Imidacloprid, the only neonicotinoid termiticide available for examination by Gahlhoff and Koehler (1999), was determined to be nonrepellent to termites. The most reliable method of determining termiticide repellency is by measuring how far termites will tunnel into soil treated at a range of concentrations. However, termite mortality also must be considered, because a termiticide that is sufÞciently toxic and fast-acting will kill termites before they can tunnel far into treated soil, even if the termiticide itself is not repellent. A new termiticide, Transport (FMC Corporation, Philadelphia, PA) has been formulated and registered using a combination of acetamiprid and bifenthrin, a repellent termiticide, as active ingredients. However, whether this mixture behaves as a repellent or nonrepellent is unknown. Our objective was to test the relative repellency of thiamethoxam, acetamiprid, and a combination of acetamiprid and bifenthrin against Reticulitermes flavipes (Kollar) termites by measuring soil penetration and termite mortality across increasing concentration and varying treatment thickness. Results were compared with previous observations with bifenthrin treatments (Gahlhoff 1999). Also, we were interested in the relative toxicity of thiamethoxam, acetamiprid, and a combination of acetamiprid ⫹ bifenthrin to R. flavipes, as well as the effects of the high water solubility, and potentially low soil absorption coefÞcient, of the active ingredient on pesticidal movement. We tested the hypothesis that repellency of a combination product with repellent and nonrepellent active ingredients can be measured by the relationship between termite mortality and soil penetration, as demonstrated for single active ingredient termiticides. Materials and Methods Termites. R. flavipes termites were Þeld collected in termite traps consisting of a polyvinyl chloride bucket (20 cm in height by 20 cm in diameter; 811192-4, Ventura Packaging Inc., Monroeville, OH), with 11 holes drilled in the sides and base (3 cm in diameter), placed vertically in the ground to a depth of roughly 19 cm, and covered with a polyvinyl chloride lid. Three rolls of single-faced corrugated cardboard (20 cm in length by 10 cm in diameter) were placed into the bucket side by side as a food source. Termites were collected from the trap by removal of cardboard rolls. Termites were removed from the cardboard rolls and maintained at room temperature (⬇23⬚C) in plastic boxes (27 by 19 by 9.5 cm) with moistened cardboard for ⱕ2 wk before placement in the bioassays. Colonies collected at different locations were maintained in the laboratory in different containers and considered to represent different Þeld colonies. Termiticides. The acetamiprid termiticide used in these experiments was F5025 70 WP, 70% active ingredient (AI) (FMC Corporation). The combination

Vol. 101, no. 6

termiticide used in these experiments was F4688 50 WP (22.43% acetamiprid, 27.30% bifenthrin, FMC Corporation). This active ingredient composition was similar to the commercial termiticide Transport, which consists of 22.73% acetamiprid and 27.27% bifenthrin. The thiamethoxam termiticide used in these experiments was TH918A 25 WG, 25% active ingredient (Syngenta, Wilmington, DE). Results were compared with experiments by Gahlhoff (1999) who used Talstar F, a termiticide containing bifenthrin as active ingredient. Soil Treatments. Bonneau Þne sand (loamy, siliceous, subactive, thermic Arenic Paleudults; NRCS 2008) was extracted near the Urban Entomology Laboratory on the University of Florida (Gainesville, FL) campus. This soil was sieved through a #35 (0.5-mm) Fisher Company sieve and dried in a drying oven for 48 h at 150⬚C. BuilderÕs sand was purchased locally and likewise sieved and dried. The Bonneau Þne sand was treated with each termiticide type to yield 0.1, 1, 10, and 100 ppm termiticide (AI, wt:wt) as well as a 0 ppm control. The combination termiticide treatment was diluted so the concentrations of acetamiprid in the soil were the same used for the acetamiprid-only termiticide treatments. All treated soils were dried in a fume hood for 1 wk before usage in the bioassays. Bioassay Design. The bioassay was a modiÞcation of the design used previously (Gahlhoff 1999, Gahlhoff and Koehler 2001), to compare our results with GahlhoffÕs bifenthrin data, which was obtained using the same soil type. At the time of testing, dried treated Bonneau Þne sand was removed from the hood, placed into plastic bags, and water was added to the bags to obtain a moisture content of 10% (wt:wt). Fisher brand wood applicators (⬇2.38 mm in diameter) were cut to ⬇47-mm lengths. Three of these wooden applicator sticks were placed in the bottom of each glass test tube (25 by 200 mm) and a 1.5-cm thick plug composed of 5% non-nutrient agar (Bacto-Agar, Difco, Detroit, MI) was inserted into the test tube until it rested on the wooden sticks. Untreated oven-dried and sieved builders sand (1,000 g) was placed into plastic bags and moistened to a concentration of 10% (wt:wt) to serve as untreated soil in the test design. A narrow (1-mm), medium (5-mm), or broad (50-mm) layer of termiticidetreated Bonneau Þne sand was centered between two layers of untreated builders sand for a total sand ⫹ treated soil depth of 50 mm (Fig. 1). Thicknesses of soil treatment were designed to simulate extremes in soil termiticide treatments observed in the Þeld. In preconstruction termiticide treatments, treatment solution will accumulate on some areas of the treated soil (e.g., depressions on horizontal surfaces); therefore, delivering treatment that may penetrate to a greater depth into the soil. In other areas, such as vertical and inclined surfaces that occur when the soil is formed for a monolithic foundation, the treatment solutions run off; therefore the termiticide treatment does not penetrate as deeply. For the broad treatments, the tubes contained only treated soil and no untreated sand, so the treated soil was in direct contact with the agar

December 2008

SMITH ET AL.: REPELLENCY AND LETHALITY OF TERMITICIDES TO R. flavipes

1883

Fig. 1. Bioassay tubes for narrow (A), medium (B), and broad (C) termiticide treatment thicknesses.

plugs. A glass funnel was used to place soil in test tubes and a scintillation vial (10 ml) attached to the shank of a screwdriver was used to lightly tamp and level the layers of soil. Layers of untreated Bonneau Þne sand at various thicknesses served as controls. The sand/soil layer was then capped with a second 1.5-cm agar plug. A white paper towel (5 by 3.75 cm) was folded to ⬇1 cm2 and placed on top of the second agar plug. One hundred workers (undifferentiated larvae of at least the third instar) and one soldier termite were placed in each test tube. Aluminum foil (Reynolds Wrap, Reynolds Metal, Richmond, VA) (3 by 3 cm) was used to cover the top end of each test tube. Ten replicates were tested at three treatment thicknesses and Þve termiticide concentrations (including controls) for a total of 150 tubes for each termiticide type. Depending on availability of termites, replicates were from different Þeld colonies, with a total of 20 colonies used for experiments, and a minimum of seven different colonies for each termiticide. Colonies were used as replicates. Effect of colonies on the variables mortality and penetration were tested and found not to be signiÞcant. Based on these results the factor, colony, was ignored for the statistical comparisons between products. The experiments were designed with termiticide type as the main effect. Test tubes were held vertically in test tube racks with termites at the top of the tube. Bioassay tubes were held at 24 ⫾ 1⬚C for 7 d. At 7 d, the tubes were broken down and the number of live worker termites in each tube was recorded. The maximum vertical distance that the termite galleries penetrated into the treated soil also was recorded at 7 d.

Data Analysis. Soil penetration distance was used to calculate percentage of penetration of treated soil. Percentage of termite mortality was calculated from numbers of survivors observed in tubes. An arcsinesquare-root transformation was applied to the percentages. To compare soil penetration and termite mortality on different termiticide types, data for each combination of treatment thickness and termiticide concentration were analyzed with a one-way analysis of variance (ANOVA), with termiticide type as the main effect. Means for each termiticide type within each combination of treatment thickness and termiticide concentration were then separated using the TukeyÐKramer test (␣ ⫽ 0.05; SAS Institute 2003). Results for the thiamethoxam, acetamiprid, and acetamiprid ⫹ bifenthrin treatments were compared graphically with results for bifenthrin treatments reported previously (Gahlhoff 1999). Results and Discussion Soil Penetration. All replicates of the controls (termiticide concentration of 0 ppm) had complete penetration of the soil by termites within 7 d (Fig. 2AÐI). Complete soil penetration also was seen in most treatments with the smallest treatment thickness and lowest termiticide concentration. Thiamethoxam treatments allowed the highest overall soil penetration (Fig. 2A, D, and G), allowing complete soil penetration in narrow and medium treatment thicknesses at concentrations of 0.1Ð10 ppm. Soil penetration in broad thickness thiamethoxam treatments began to sharply decline between concentrations of 1 and 10

1884

JOURNAL OF ECONOMIC ENTOMOLOGY

Vol. 101, no. 6

Fig. 2. Percentage of soil penetration (solid line) and percentage of termite mortality (dotted line) across several concentrations (ppm) of thiamethoxam (A, D, and G), acetamiprid (B, E, and H), and acetamiprid ⫹ bifenthrin (C, F, and I), at narrow (1-mm) (AÐC), medium (5-mm) (DÐF), and broad (50-mm) treated soil thicknesses (GÐI). Solid circles indicate percent soil penetration or percent termite mortality signiÞcantly higher than those on corresponding treatments among the thiamethoxam, acetamiprid, and acetamiprid ⫹ bifenthrin treatments. Open circles indicate values signiÞcantly lower than those on corresponding treatments thiamethoxam, acetamiprid, and acetamiprid ⫹ bifenthrin treatments. Concentration shown in the acetamiprid ⫹ bifenthrin treatments is the concentration of the acetamiprid component only.

ppm. The soil penetration data for thiamethoxam is similar to previous Þndings on R. flavipes penetration of thiamethoxam-treated soil (Remmen and Su 2005), where soil penetration sharply declined between 2 and 4 ppm. The Remmen and Su (2005) study examined soil penetration and termite mortality at more concentrations than our study, but only at a single treatment thickness. The termiticide-treated soil was in direct contact with the agar plugs in their study, similar to the broad thickness treatments in our study. Tests on Premise (AI was neonicotinoid imidacloprid) have shown a pattern of soil penetration similar to that for thiamethoxam (Gahlhoff and Koehler 2001).

Premise had little effect on soil penetration at narrow (1-mm) and medium (5-mm) treatment thicknesses, even at concentrations of 100 ppm. At a treatment thickness of 50 mm, with treated soil in contact with agar plugs, Premise caused soil penetration inhibition similar to that seen with thiamethoxam in our study. Other termiticide active ingredients, such as chlorpyrifos (Gahlhoff and Koehler 2001, Su et al. 1995) and Þpronil (Remmen and Su 2005), caused greater inhibition to soil penetration by R. flavipes termites than imidacloprid or thiamethoxam, although this reduction in penetration was due to termites being killed before signiÞcant penetration occurred.

December 2008

SMITH ET AL.: REPELLENCY AND LETHALITY OF TERMITICIDES TO R. flavipes

The acetamiprid soil treatments in our study allowed complete soil penetration for the narrow treatment thickness at concentrations of 0.1Ð10 ppm (Fig. 2B) and the medium treatment depth at concentrations of 0.1Ð1 ppm (Fig. 2E). Termite penetration into acetamiprid-treated soil was either equal to or significantly less than penetration observed in thiamethoxam treatments, for all concentrations and treatment thicknesses. The highest concentration of acetamiprid at the narrow treatment thickness reduced mean soil penetration to 40% (Fig. 2B), which was signiÞcantly lower than the soil penetration (90%) in the corresponding thiamethoxam treatment (Fig. 2A). A more pronounced reduction of soil penetration was seen in the acetamiprid medium thickness treatments (Fig. 2E), with almost no soil penetration at the highest concentration. Soil penetration in acetamiprid broad thickness treatments declined sharply between concentrations of 0.1 and 1 ppm (Fig. 2H), a 10-fold lower range of concentrations than the range of sharp soil penetration decline for thiamethoxam (Fig. 2F). Acetamiprid ⫹ bifenthrin treatments were the most inhibitory to overall soil penetration (Fig. 2C, F, and I). In all treatment thicknesses, the sharp decline in soil penetration on acetamiprid ⫹ bifenthrin treatments happened within a range of concentrations that was 10-fold lower than the range of decline with acetamiprid-only treatments. In addition, there was no soil penetration in soil with 100 ppm acetamiprid ⫹ bifenthrin in any treatment thickness (Fig. 2C, F, and I) and soil with 10 ppm acetamiprid ⫹ bifenthrin in the broad treatment thickness (Fig. 2I). So, the addition of bifenthrin signiÞcantly decreased termite soil penetration compared with the acetamiprid-only treatment. The termite penetration into soil treated with for bifenthrin only in a previous study (Gahlhoff 1999) was similar to the penetration we observed in the acetamiprid-only treatment in our study, with slightly more penetration in the broad treatment at lower concentrations. These soil penetration data are consistent with previous Þndings (Su and Scheffrahn 1990), where bifenthrin proved to be more inhibitory to soil penetration by R. flavipes termites than imidacloprid (Gahlhoff and Koehler 2001) or thiamethoxam (Remmen and Su 2005) at equivalent concentrations. Several other pyrethroids, including deltamethrin, cypermethrin, permethrin, and ␭-cyhalothrin, also were found to be inhibitory to R. flavipes soil penetration to a degree similar to that seen in bifenthrin (Su and Scheffrahn 1990, Gahlhoff 1999). Mortality. Control mortality was ⬍11% in all cases (dose 0 for all pesticides in Fig. 2AÐI). Many of the lower concentration acetamiprid treatments had similarly low mortality. Thiamethoxam caused relatively little hindrance to soil penetration, and caused consistently higher termite mortality than acetamiprid treatments, except at high doses in the broad treatment (Fig. 2H). In thiamethoxam treatments, mean termite mortality steadily increased with increasing concentration. In two situations (narrow treatment, 100 ppm [Fig. 2A], and broad treatment, 0.1 ppm [Fig.

1885

2G]) thiamethoxam mortality was signiÞcantly higher than the mortality in the acetamiprid treatments. Termite mortality on thiamethoxam treatments was generally greater in broad treatment thickness (Fig. 2G) than on narrow and medium treatment thicknesses (Fig. 2A and D) at all concentrations. For thiamethoxam concentrations of 0.1Ð1 ppm, mortality was signiÞcantly higher on broad thickness treatments than on narrow or medium thickness treatments. However, there were no signiÞcant differences in termite mortality between narrow and medium treatment thicknesses at equivalent concentrations of thiamethoxam. The signiÞcant differences in termite mortality between broad thickness treatments and the other treatment thicknesses may be due to there being no untreated sand in the bioassay tubes in broad thickness treatments, and the treated soil was in direct contact with the agar plugs. This is in contrast to the narrow and medium thickness treatments, where treated soil was separated from the agar plugs by untreated sand. Given the high water solubility and potential mobility of neonicotinoids, the direct contact of treated soil with the agar plugs in the broad thickness treatments may have allowed the termiticide to diffuse into/through the agar, increasing the termitesÕ exposure to thiamethoxam and heightening mortality. Indeed, many termites exposed to high concentration of thiamethoxam in the broad treatment died in or on the agar before penetrating the treated soil. Acetamiprid treatments caused lower termite mortality compared with thiamethoxam treatments, particularly at the narrow and medium treatment thicknesses (Fig. 2B and E). Mean termite mortality with acetamiprid never reached 50% in either the narrow or the medium treatment thickness. In the broad treatment thickness (Fig. 2H), the highest concentration of acetamiprid caused close to 100% termite mortality. However, 1 ppm acetamiprid caused signiÞcantly less mortality than 1 ppm thiamethoxam and the 1 ppm acetamiprid ⫹ bifenthrin at the broad treatment thickness. Although the pattern of soil penetration was similar between our study and that of Remmen and Su (2005), termite mortality on thiamethoxam was far greater on concentrations of 0.1Ð10 ppm in our study, perhaps due to the difference in soil used for termiticide treatment. Our treated soil was Bonneau Þne sand, which has more organic matter than the builders sand used by Remmen and Su (2005). The difference in mortality also could be due to differences in individual termite colonies. Coptotermes formosanus (Shiraki) in the Remmen and Su (2005) study exhibited a pattern of mortality and soil penetration nearly identical to that seen with the R.. flavipes termites in our study. The pattern of termite mortality in the imidaclopridtreated soil (Gahlhoff and Koehler 2001) was similar to that seen for the thiamethoxam treatment in our study. In previous studies, chlorpyrifos (Gahlhoff and Koehler 2001, Su et al. 1995) and Þpronil (Remmen and Su 2005) caused greater termite mortality than

1886

JOURNAL OF ECONOMIC ENTOMOLOGY

thiamethoxam and imidacloprid at equivalent concentrations. At narrow and medium treatment thicknesses, termite mortality did not signiÞcantly differ between acetamiprid-only and acetamiprid ⫹ bifenthrin treatments. At a broad treatment thickness, 10 ppm of acetamiprid ⫹ bifenthrin (Fig. 2I) caused signiÞcantly greater mortality than corresponding acetamiprid concentration (Fig. 2H). This heightened mortality may be due to bifenthrin (Koc ⫽ 1.31 ⫻ 105Ð3.02 ⫻ 105 ml/g) being 1,000 times more tightly bound to soil than acetamiprid (Koc ⫽ 132Ð267 ml/g). Acetamiprid ⫹ bifenthrin soil treatments were especially lethal at combinations of high concentration and broad thickness. Combination treatments caused 100% termite mortality in the broad treatment thickness at concentrations of 10 Ð100 ppm (Fig. 2I). At the broad treatment thickness, higher concentrations of acetamipridonly and acetamiprid ⫹ bifenthrin treatments caused 100% termite mortality without termite entry into the agar plugs. This high mortality in the broad thickness treatments was very different from the low mortality seen for bifenthrin only (Su and Scheffrahn 1990, Gahlhoff 1999). In acetamiprid ⫹ bifenthrin treatments at 10 Ð100 ppm (Fig. 2I), there was 0% soil penetration and 100% termite mortality, compared with minimum penetration and minimum mortality for the bifenthrin alone (Gahlhoff 1999). Furthermore, in the acetamiprid ⫹ bifenthrin treatments, the termites were all dead before they even reached the soil. This effect was seen to a lesser degree in the broad acetamiprid treatment at 100 ppm (Fig. 2H), but it was not apparent in the broad thiamethoxam treatment (Fig. 2G). These data suggest that, at the highest concentrations, acetamiprid may have diffused into/ or through the agar and killed the termites before their entry into the soil. Repellency. Remmen and Su (2005) have stated that the level of termiticide repellency may be indicated by the height of the intersection of a percentage of soil penetration curve and a percentage of termite mortality curve. An intersection of the two curves at a low percentage indicates a high level of repellency, whereas an intersection of the two curves at a high percentage indicates a low level of repellency. Based upon the soil penetration and termite mortality data for thiamethoxam treatments across treatment thickness and termiticide concentration, thiamethoxam is clearly the least repellent termiticide, because the mortality and penetration curves either did not intersect for the concentrations tested or intersected above the 50% level (Fig. 2G). In thiamethoxam treatments, there was ⬎50% termite mortality before there was any decrease in termite penetration into treated soil. Clearly, R. flavipes has no aversion to tunneling in soil treated with thiamethoxam. This lack of repellency is consistent with that observed for thiamethoxam previously (Remmen and Su 2005) and imidacloprid (Gahlhoff and Koehler 2001). The intersection of soil penetration and termite mortality curves for acetamiprid lead to a different conclusion. The soil penetration and termite mortality

Vol. 101, no. 6

curves either did not intersect (Fig. 2B) or the intersection occurred at low mortality levels (Fig. 2E and H). This would suggest, following Remmen and Su (2005), that acetamiprid is a repellent termiticide. Acetamiprid caused high mortality when higher doses were used in broad thickness treatment (Fig. 2H), with minimum or no soil penetration by the termites. These observations are unlike what is seen with bifenthrin treatments (Gahlhoff 1999), in which the intersection of the mortality and penetration curves occurred at low percentages. The acetamiprid-only data indicate that termite tunneling was signiÞcantly reduced without the termites dying in large numbers. The intersection of the mortality and penetration curves below the 40% level (Fig. 2E) may suggest that acetamiprid inhibited soil penetration, but the lack of penetration may have been due to behavioral changes caused by sublethal effects. Imidacloprid caused R. flavipes termites to become paralyzed at soil concentrations as low as 0.001% (10 ppm) and restricted tunneling behavior at soil concentrations as low as 0.00001% (0.1 ppm) (Boucias et al. 1996). These data suggest that reduced soil penetration is caused by a loss in termite mobility, rather than termiticide repellency. It is possible that acetamiprid acts on R. flavipes termites in a manner similar to imidacloprid, interfering with tunneling activity and indirectly reducing exposure to termiticide-treated soil. This inhibition to tunneling was not seen in our thiamethoxam treatments, but there is evidence that thiamethoxam interacts with the insect nervous system in a way subtly different from that seen with other neonicotinoids. It has been suggested that thiamethoxam may have a different binding interaction with insect acetylcholine receptors than imidacloprid (Weisner and Kayser 2000), one of the most commonly used neonicotinoids. Intersections of the mortality and soil penetration curves occurred at low mortality in the acetamiprid ⫹ bifenthrin treatments (Fig. 2C, F, and I), and they were similar to those in the acetamiprid-only treatments but occurred at a 10-fold lower dose. Although soil penetration patterns were similar between broad thickness acetamiprid ⫹ bifenthrin treatments and previous bifenthrin assays (Su and Scheffrahn 1990, Gahlhoff 1999), termite mortality patterns were very different. The acetamiprid ⫹ bifenthrin treatment (Fig. 2C, F, and I) had a slightly higher level of effective repellency than bifenthrin only (Gahlhoff 1999); however, this combination had a lethality to R. flavipes termites that far exceeded the lethality of bifenthrin only. The combination treatments had a little more than twice the combined AI of the corresponding single termiticide treatments because the combination product was diluted to have the same concentrations of acetamiprid as the acetamiprid-only treatments. This may have contributed to the higher activity levels observed in the assays. Results discussed herein were obtained with speciÞc formulations of the tested active ingredients. Other formulations with unique properties may have

December 2008

SMITH ET AL.: REPELLENCY AND LETHALITY OF TERMITICIDES TO R. flavipes

different effects on termites under similar test conditions. Furthermore, Þeld conditions not adequately replicated in laboratory tube bioassays may affect the termiticide products in manner not observed in our bioassays. Nevertheless, due to its high soil mobility (U.S. EPA 2008), acetamiprid may move away from the initially treated zone and possibly reach termites further from the originally treated soil. Thiamethoxam may potentially be more effective in eliminating termites after they tunnel into and directly contact treated soil. These differences suggest that thiamethoxam may be a better choice if treatment gaps are a concern, a hypothesis that should be further explored in Þeld tests. The acetamiprid ⫹ bifenthrin combination may be useful in keeping termites away from the treated soil, because of combined effects of acetamiprid and bifenthrin. Because acetamiprid has high water solubility, this combination may have the additional short-term beneÞt of the diffusion of acetamiprid into the untreated soil. A variety of termiticides with repellent and nonrepellent properties are available to adequately protect structures. However, understanding the different active ingredients, their effect on termites, mobility in soil, compatibility with other active ingredients, and other properties may be important in designing more efÞcient termiticides, speciÞc for each encountered Þeld condition. Mixtures of active ingredients may represent an important approach for new termiticides to exploit the best qualities of each component. Acknowledgments We thank Gil Marshall for technical assistance during the experiments, FMC Corporation and Syngenta for test materials and support, and anonymous reviewers for help in improving this manuscript.

References Cited Boucias, D. G., C. Stokes, G. Storey, and J. Pendland. 1996. Effect of imidacloprid on both the termite, Reticulitermes flavipes and its interaction with insect pathogens. Pfanzenshutz-Natrichten Bayer 49: 103Ð144. Gahlhoff, J. E. 1999. Penetration and survivorship of the eastern subterranean termite, Reticulitermes flavipes (Kollar), into various thicknesses of termiticide-treated soil. M.S. thesis, University of Florida, Gainesville. Gahlhoff, J. E., and P. G. Koehler. 1999. To kill or not to kill? PCT Magazine, March Issue. Gahlhoff, J. E., and P. G. Koehler. 2001. Penetration of the eastern subterranean termite into soil treated at various thicknesses and concentrations of Dursban TC and Premise 75. J. Econ. Entomol. 94: 486Ð491. Kubota, S., Y. Shono, T. Matsunaga, and K. Tsunoda. 2007. Response of the subterranean termite Coptotermes formosanus (Isoptera: Rhinotermitidae) to soil treated with microencapsulated fenobucarb. Pest Manag. Sci. 63: 1224Ð1229. Maienfisch, P., M. Angst, F. Brandl, W. Fischer, D. Hofer, H. Kayser, W. Kobel, A. Rindlisbacher, R. Senn, A. Steine-

1887

mann, et al. 2001. Chemistry and biology of thiamethoxam: a second generation neonicotinoid. Pest Manag. Sci. 57: 906 Ð913. Nauen, R., U. Ebbinghaus-Kintscher, V. L. Salgado, and M. Kaussmann. 2003. Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants, Pestic. Biochem. Physiol. 76: 55Ð 69. [NRCS] Natural Resources Conservation Service. 2008. OfÞcial soil series descriptions. U.S. Dep. Agric.ÐNRCS, Lincoln, NE. (http://soils.usda.gov/technical/classiÞcation/ osd/index.html). Peterson, C. J. 2007. Imidacloprid mobility and longevity in soil columns at a termiticidal application rate. Pest Manag. Sci. 63: 1124 Ð1132. Potter, M. F. 2004. Termites, pp. 217Ð361. In A. Mallis, S. A. Hedges, and D. Moreland [eds.], Handbook of pest control, 9th ed. GIE Media, Inc., RichÞeld, OH. Remmen, L. N., and N.-Y. Su. 2005. Tunneling and mortality of eastern and Formosan subterranean termites (Isoptera: Rhinotermitidae) in sand treated with thiamethoxam or Þpronil. J. Econ. Entomol. 98: 906 Ð910. SAS Institute. 2003. Statistical analysis software computer program, version 8.01. SAS Institute, Cary, NC. Smith, J. L., and M. K. Rust. 1990. Tunneling response and mortality of the western subterranean termite (Isoptera: Rhinotermitidae) to soil treated with termiticides. J. Econ. Entomol. 83: 1395Ð1401. Stephenson, R. R. 1982. Aquatic toxicology of cypermethrin. I. Acute toxicity to some freshwater Þsh and invertebrates in laboratory tests. Aquat. Toxicol. 2: 175Ð 185. Su, N.-Y., and R. H. Scheffrahn. 1990. Comparison of eleven soil termiticides against the Formosan subterranean termite and eastern subterranean termite (Isoptera: Rhinotermitidae). J. Econ. Entomol. 83: 1918 Ð1924. Su, N.-Y., M. Tamashiro, J. R. Yates, and M. I. Haverty. 1982. Effect of behavior on the evaluation of insecticides for prevention of or remedial control of the Formosan subterranean termite. J. Econ. Entomol. 75: 188 Ð193. Su, N.-Y., G. S. Wheeler, and R. H. Scheffrahn. 1995. Subterranean termite (Isoptera: Rhinotermitidae) penetration into sand treated at various thicknesses with termiticides. J. Econ. Entomol. 88: 1690 Ð1694. Thorne, B. L., and N. L. Breisch. 2001. Effect of sublethal exposure to imidacloprid on subsequent behavior of subterranean Reticulitermes virginicus (Isoptera: Rhinotermitidae). J. Econ. Entomol. 94: 492Ð 498. Tomizawa, M., and J. E. Casida. 2003. Selective toxicity of neonicotinoids attributable to speciÞcity of insect and mammalian nicotinic receptors. Annu. Rev. Entomol. 48: 339 Ð364. Tomizawa, M., and J. E. Casida. 2005. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45: 247Ð268. [U.S. EPA] U.S. Environmental Protection Agency. 2008. Acetamiprid fact sheet. U.S. EPA-OfÞce of Pesticide Programs, Washington, DC. (http://www.epa.gov/ opprd001/factsheets/acetamiprid.pdf). Weisner, P., and H. Kayser. 2000. Characterization of nicotinic acetylcholine receptors from the insects Aphis craccivora, Myzus persicae, and Locusta migratoria by radioligand binding assays: relation to thiamethoxam action. J. Biochem. Mol. Toxicol. 14: 221Ð230. Received 13 February 2008; accepted 22 July 2008.