Control of Helicoverpa zea in Tomatoes with Chlorantraniliprole Applied Through Drip Chemigation

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1 2010 Plant Management Network. Accepted for publication 14 January Published. Control of Helicoverpa zea in Tomatoes with Chlorantraniliprole Applied Through Drip Chemigation Thomas P. Kuhar, Department of Entomology, Eastern Shore AREC, Virginia Polytechnic Institute & State University, Painter, VA 23420; James F. Walgenbach, Department of Entomology, Mountain Horticultural Crops Research Station (MHCRS), North Carolina State University, Mills River, NC 28759; and Hélène B. Doughty, Department of Entomology, Eastern Shore AREC, Virginia Polytechnic Institute & State University, Painter, VA Corresponding author: Thomas P. Kuhar. Kuhar, T. P., Walgenbach, J. F., and Doughty, H. B Control of Helicoverpa zea in tomatoes with chlorantraniliprole applied through drip chemigation. Online. Plant Health Progress doi: /php rs. Abstract Chlorantraniliprole (=Rynaxypyr) is a novel anthranilic diamide insecticide that is of interest to vegetable growers because of its low mammalian toxicity and systemic properties. Field trials were conducted between 2006 and 2008 in North Carolina and Virginia to test the efficacy of chlorantraniliprole as a drip chemigation treatment on tomatoes. Drip chemigation of chlorantraniliprole at various rates and intervals significantly reduced the percentage of tomatoes damaged by tomato fruitworm (Helicoverpa zea) comparable to that typically achieved from multiple foliar applications of insecticides. The best control was achieved with two applications of chlorantraniliprole at kg ai/ha, or a single application at kg ai/ha. Residual ingestion bioassays showed that chlorantraniliprole was effectively taken up by the roots and was active in leaves up to 66 days after treatment (DAT), active in blossoms up to 22 DAT, but was not active in fruit. Drip chemigation of chlorantraniliprole may offer several advantages over foliar applications, including ease of application, reduced pesticide input into the environment, reduced worker exposure to pesticides, and reduced risk to beneficial arthropods. Introduction Tomato fruitworm, Helicoverpa zea (Boddie), is a major pest of tomatoes in the United States (5,7,12,13,20). Commercial growers typically rely on multiple applications of foliar insecticides to protect the developing fruit from feeding injury (Fig. 1) by H. zea and other insect pests (16,7). This preventative spraying approach has several potential drawbacks including suppression of important natural enemies (2), undesirable effects on other non-target species and the environment (16), reduced profits from unwarranted insecticide applications (1,12), and insecticide residues on fruits (18).

2 Fig. 1. Tomato fruitworm larva and damaged tomato fruit. Chlorantraniliprole (= Rynaxypyr) (Coragen, E. I. du Pont de Nemours and Company, Wilmington, DE) is a novel insecticide from a new class of chemistry, the anthranilic diamides, which activate the insect ryanodine receptors affecting calcium release during muscle contraction (10,17). Insects treated with chlorantraniliprole exhibit rapid feeding cessation, lethargy, regurgitation, muscle paralysis, and ultimately death (11). Chlorantraniliprole is effective against numerous Lepidopterous species (3,4,8,9,19), and is xylem-mobile for root uptake providing control of certain leaf-feeding insect pests (8,14,15). Herein, we report field efficacy experiments with chlorantraniliprole applied via drip-chemigation system to manage tomato fruitworm in staked tomatoes. Field Efficacy Experiments in North Carolina Three field experiments were conducted at North Carolina State University s Mountain Horticultural Crops Research Station (MHCRS), Mills River, NC (USA) in 2006, 2007, and 2008, with transplanting dates of 7 June, 23 May, and 2 June, respectively. For all experiments, five-week old Mountain Spring tomato transplants were planted in beds of black plastic mulch. Chapin twinwall drip tape (15.9-mm diameter, 10-ml thickness, emitters spaced 0.3 m apart with a flow rate of 1.89 liters/min/30.4 m) was laid 5 cm below the soil surface under the plastic mulch. Plots consisted of 6-m long single rows in 2006 and 2007 and 7.6-m long single rows in 2008 with plants spaced 0.46 m within rows, and treatment rows spaced 1.5 m apart. Each treatment was replicated four times and 3.6 m of bare ground separated replicates. Insecticides were applied into the drip using an EZ-FLOW fertilizer injector (EZ-FLO Fertilizing Systems, Loomis, CA). To compensate for the low flow rate of water through the drip line (flow rate was 1.89 liters/min/30.4 m and EZ Flow injectors required a minimum flow rate of 3.8 liters/min), a coupler with ball valve was placed in the drip line between inflow and outflow lines of the injector. The drip tubes of treatments between replicates were connected with 1.6-cm polyethylene tubing. Insecticide treatments were applied through drip injection system for 20 min followed by 30 min of flushing the drip system with water. All plots were also irrigated through the drip line as needed during the growing season; plots were irrigated once per week for 2 h before fruit set, and two to three times per week (2 h/day) after fruit set. Mature green fruits were hand-picked from plots and visually evaluated for fruit damage on multiple harvest dates. All efficacy data were analyzed using a two-way ANOVA, and means were separated by Fisher s Protected LSD (P 0.05). Some of the data were arcsine square-root transformed to normalize the variance, but actual data means are presented in the tables. Based on field observations of larvae on plants and the typical diagnostic feeding hole injury (Fig. 2), tomato fruitworm was the primary Lepidopterous pest that caused the majority of insect damage to tomato fruit in all field experiments.

3 Fig. 2. Tomato fruitworm feeding hole in developing tomato fruit. The 2006 experiment in North Carolina. The experiment included two treatments (0.049 and kg ai/ha) of chlorantraniliprole (Coragen 1.67SC, DuPont, Wilmington, DE) injected into the drip system, a foliar standard application treatment of indoxacarb (Avaunt 30WG, DuPont) (0.073 kg ai/ha), and an untreated control. Foliar applications were made with a Solo (Newport News, VA) backpack sprayer delivering 38 to 115 liters/ha (volume increased as plants grew). All injection treatments and the foliar application of indoxacarb were applied five times (14 and 28 June, 12 and 26 July, and 7 August). Pest pressure was low to moderate with the untreated plots averaging 9.6% and 8.3% fruit damage on 10 and 22 August, respectively (Table 1). Both of the injection treatments of chlorantraniliprole (0.049 and kg ai/ha, each applied 5 times) had significantly less fruit damage than the untreated control (P < 0.05), and were similar to the indoxacarb foliar sprays on the first harvest date. The same numerical trends, statistically not significant, were observed on the second harvest date, 22 August. No visible signs of either phytotoxicity or plant growth effects were detected from the applications of chlorantraniliprole. Moreover, there was no significant treatment effect on the total number of green fruit harvested in the experiment (data not shown; P > 0.05). Table 1. Summary of efficacy of chlorantraniliprole applied through drip irrigation for the control of lepidopterous larvae on tomatoes; Fletcher, NC, * 10 Aug 22 Aug Untreated 9.6 a 8.3 a Chlorantraniliprole (x 5 injections) b 1.2 a Chlorantraniliprole (x 5 injections) b 2.8 a Indoxacarb (x 5 foliar sprays) b 2.2 a * All injection treatments and the foliar application of indoxacarb were applied five times (14 and 28 June, 12 and 26 July, and 7 August). Tomato fruits were evaluated for damage on 10 and 22 August. The 2007 experiment in North Carolina. The experiment included four treatments of chlorantraniliprole injected into the drip system (0.049 and kg ai/ha each applied at either a two-week or a three-week interval beginning on 13 June), a foliar treatment of indoxacarb applied approximately weekly (13, 20, and 27 June, 2, 11, 18, and 23 July, and 1 August), and an untreated control. Tomato fruit damage in the untreated plots averaged 7.6% and 10.8% on 19 July and 2 August, respectively (Table 2). There was a significant treatment effect on both harvest dates. Each of the chlorantraniliprole injection treatments (0.049 and kg ai/ha applied at either a two-week or a three-week interval) and the indoxacarb foliar spray treatment (6 weekly sprays) had less fruit damage than the untreated control (P < 0.05), and no differences were found among the insecticide treatments

4 (P > 0.05). Again, no visible signs of phytotoxicity or plant growth effects were detected from the applications of chlorantraniliprole, and there was no significant treatment effect on the number of fruit harvested (data not shown; P > 0.05). Table 2. Summary of efficacy of chlorantraniliprole applied through drip chemigation for the control of lepidopterous larvae on tomatoes; Fletcher, NC, * 19 Jul 2 Aug Untreated 7.6 a 10.8 a Chlorantraniliprole (2-week interval) b 1.8 b Chlorantraniliprole (2-week interval) b 0.9 b Chlorantraniliprole (3-week interval) b 0.7 b Chlorantraniliprole (3-week interval) ab 1.7 b Indoxacarb ( 8 foliar sprays) ab 0.5 b * Injection treatments were applied three times each beginning on 13 June and thereafter every two or three weeks as noted. Foliar applications of indoxacarb were made approximately weekly (13, 20, and 27 June, 2, 11, 18, and 23 July, and 1 August). Fruit were evaluated for damage on 19 July and 2 August. The 2008 experiment in North Carolina. The experiment included three treatments of chlorantraniliprole injected into the drip system (0.049 and kg ai/ha each applied twice (17 June and 1 July), and kg ai/ha applied once on 17 June, and an untreated control. Fruits were evaluated for damage on 31 July, 14 and 28 August, and 11 and 25 September. Fruitworm damage was relatively low, with the season average in the control only 4.1% (Table 3). However, there was a significant treatment effect on percentage fruit damage for all harvests except 11 September, when fruit damage averaged less than 2% in the untreated plots. For all other harvests, each of the chlorantraniliprole injection treatments (0.049 and kg ai/ha applied twice each, and kg ai/ha applied once) had less fruit damage than the untreated control (P < 0.05), and no differences were found among the insecticide treatments on any of the harvest dates (P > 0.05). Table 3. Summary of efficacy of chlorantraniliprole applied through drip chemigation for the control of lepidopterous larvae on tomatoes; Fletcher, NC, Jul 14 Aug 28 Aug 11 Sep 25 Sep Untreated 9.7 a 4.8 a 2.1 a 1.9 a 4.1 a Chlorantraniliprole ( 2 injections) Chlorantraniliprole ( 2 injections) Chlorantraniliprole ( 1 injection) b 2.0 b 0.3 b 0.4 a 0.0 b b 0.0 b 0.0 b 0.2 a 1.8 b b 0.9 b 0.6 b 0.8 a 0.3 b * The and kg ai/ha treatments were applied twice each (17 June and 1 July) and the kg ai/ha was applied once on 17 June. Mature green fruits were evaluated for damage on 31 July, 14 and 28 August, and 11 and 25 September.

5 Field Efficacy Experiments in Virginia Two field experiments were conducted at the Virginia Tech Eastern Shore Agricultural Research and Extension Center (ESAREC) near Painter, VA, in 2007 and 2008, with transplanting dates of 13 June and 17 July, respectively. Florida 47 tomatoes were planted in 2007 and Solar Fire tomatoes were planted in All plots were covered with black plastic mulch. Eurodrip drip tape (15.9-mm diameter, emitters spaced 0.3 m apart with a flow rate of 1.89 liters/min/30.4 m) was placed approximately 3 cm below the soil surface. All treatments were replicated 4 times. The drip tubes of treatments between replicates were connected with 1.3-cm diameter Blue-Stripe polyethylene tubing (Toro-Ag, El Cajon, CA). Plots consisted of 1 row by 9.1 m long with a 1.8-m row center. Transplants were spaced 0.46-m apart. All plots were maintained according to standard commercial practices. All drip chemigation treatments were applied just before flowering with the use of HN55 Chemical injectors (Chemilizer Products Inc., Largo, FL). Each insecticide amount was diluted in 150 ml of water, poured into the chemilizer feeding tube and flushed with an additional 300 ml of water. Irrigation events for approximately 1 h always followed chemical application (irrigation was run at least 3 times weekly for a minimum of 1 h for each event). On two harvest dates for each year, a sample of at least 50 mature green fruits were hand-picked from plots and visually evaluated for lepidopteran fruit damage. The 2007 experiment in Virginia. The experiment included five treatments of chlorantraniliprole injected into the drip system (0.074 kg ai/ha applied 1, 2, or 3 times at 10-day intervals beginning 10 August, kg ai/ha applied 1 or 2 at 10 day interval beginning on 10 August, and an untreated control. Lepidopteran fruit damage on the untreated tomatoes averaged 23.1 and 15.5% on 21 September and 2 October, respectively (Table 4). All treatments had significantly less lepidopteran damage than the untreated control except the chlorantraniliprole treatment applied twice at kg ai/ha on the first harvest date and chlorantraniliprole applied once at kg ai/ha on both harvest dates (Table 4). In general, there were no significant differences in efficacy among the insecticide treatments, except on the second harvest date, when chlorantraniliprole applied once at kg ai/ha did not perform as well as the other treatments. Table 4. Summary of efficacy of chlorantraniliprole applied through drip chemigation for the control of lepidopterous larvae on tomatoes; Painter, VA, Sep 2 Oct Untreated 23.1 a 15.5 a Chlorantraniliprole (1 application) ab 18.0 a Chlorantraniliprole (1 application) b 0.5 b Chlorantraniliprole (2 applications) ab 1.0 b Chlorantraniliprole (2 applications) b 1.5 b Chlorantraniliprole (3 applications) b 0.5 b * Injection treatments were applied 1, 2, or 3 times at 10-day intervals beginning 10 August as noted. Fruit were evaluated for damage on 21 September and 2 October. The 2008 experiment in Virginia. The experiment included three treatments of chlorantraniliprole injected into the drip system (0.049 and kg ai/ha each applied twice (12 and 22 August), and kg ai/ha applied once on 12 August, and an untreated control. Lepidopteran pest pressure was the highest of all the experiments with fruit damage on the untreated tomatoes averaging 18.8 and 46.7% on 29 August and 17 September,

6 respectively (Table 5). Although tomato fruitworm was the major pest, tomato hornworm, Manduca quinquemaculata (Lepidoptera: Sphingidae) also may have contributed to some fruit damage. The damage was not separated by pest species. There were significant treatment effects on fruit damage on both harvest dates, where the untreated control had more damage than any of the treatments, and there were no differences among the chlorantraniliprole treatments. Table 5. Summary of efficacy of chlorantraniliprole applied through drip chemigation for the control of lepidopterous larvae on tomatoes; Painter, VA, Aug 17 Sep Untreated 18.8 a 46.7 a Chlorantraniliprole (2 applications) b 8.3 b Chlorantraniliprole (2 applications) b 1.7 b Chlorantraniliprole (1 application) b 5.0 b * The and kg ai/ha treatments were applied twice each (12 and 22 August) and the kg ai/ha was applied once on 12 August. Fruit were evaluated for damage on 29 August and 17 September. Laboratory Ingestion Bioassays of Field Treated Plant Parts In addition to the field efficacy experiments, an ingestion bioassay was also conducted in Virginia at the ESAREC in 2007 to evaluate the residual activity of chlorantraniliprole on field-treated plant parts. Tomato plots were established and treated as explained previously for the 2007 Virginia field efficacy experiment, including a single injection treatment of chlorantraniliprole at and kg ai/ha on 10 August. On 14, 17, and 24 August, 1 September, and 3 and 18 October, leaves, blossoms, and fruit (when available) were collected from tomato plants in the field and used for ingestion bioassays with laboratory-reared H. zea larvae. All H. zea used in ingestion bioassays were obtained as neonate larvae (Chesapeake Pearl, Newark, DE) and maintained on artificial diet (F9772, Bio-Serv Inc., Frenchtown, NJ) under controlled environmental conditions (28 ± 1 C, 50% relative humidity, and 16:8 L:D) until needed for bioassays, as 3rd instars. Leaf bioassays. Tomato leaves from the upper and lower canopy, 8 plants per plot, were collected from the back and front of a 50-m length of row plots. Only fully expanded but non-senescing leaves were collected for bioassay studies. Leaflets were removed and each was placed in one individual cell in a 16 cell tray (Clear Pak, Franklin Park, IL). Each cell tray was lined with agar (Bio- Serv) to maintain adequate moisture and turgidity of the leaves. One 3rd instar tomato fruitworm was placed in each cell and the cells were covered with plastic snap-on lids (Brisar Delvco Packaging Services, Philadelphia, PA). Trays with insects were maintained under controlled environmental conditions (28 ± 1 C, 50% relative humidity, and 16:8 L:D) and larval mortality was recorded after 72 h of exposure. Moribund larvae (sluggish, not feeding, and unable to flip over when turned on their backs) were recorded as dead. Blossom bioassays. Tomato blossoms (maximum of 2 per plant for a total of 32) were arbitrarily collected along a 50-meter row from each treatment on 24 August and 1 September. Blossoms were placed in individual cell trays (2 blossoms per cell), and infested with one tomato fruitworm larva per cell. The details of the bioassay were as described above for the leaf bioassay. Fruit bioassays. Small green tomato fruit were arbitrarily collected along a 50-meter row from each treatment (30 fruit per treatment) and placed in 250- ml plastic containers with two tomato fruitworm larvae (Fig. 3) on 24 August and 1 September. Mortality and the presence of scarring and tunneling on the fruit were recorded at 72 h.

7 Fig. 3. Tomato fruit bioassay chamber (250- ml plastic container) for testing residual insecticide efficacy against insects. Ingestion bioassays showed that chlorantraniliprole applied through the drip at and kg ai/ha remained active in tomato leaves for more than 50 days after treatment, killing between 70 to 97% of the laboratory larvae exposed to leaves (Table 6A). At 66 DAT, activity of the treated leaves began to decline. Both chlorantraniliprole treatments protected leaves from feeding injury by the laboratory larvae up to 66 DAT (Table 6A). Both chlorantraniliprole treatments were active in the tomato blossoms up to 22 DAT (Table 6B), killing more than 62% of laboratory larvae. Green fruits collected from the field plots showed no effect of chlorantraniliprole treatment, with larval mortality and fruit injury being similar to that in the untreated control (Table 6B) (Fig. 4). Even though residual activity in the field cannot be directly inferred from these results, they are good indicators of the extended residual of this product applied by drip chemigation. Fig. 4. Healthy tomato fruitworm larva feeding on tomato fruit in the bioassay chamber.

8 Table 6. Summary of tomato fruitworm larval toxicity bioassays conducted on leaves collected at various intervals (A), and blossoms and green fruit collected at 22 DAT (B), from tomato plants treated in the field with drip-chemigation treatments; Painter, VA, (A) Leaves (B) Blossoms and fruit (at 22 DAT) % dead or moribund larvae placed on leaves 4 DAT 7 DAT 14 DAT 22 DAT 53 DAT 66 DAT Untreated 3.1 b 18.8 b 18.8 b 10.1 b 18.8 b 25.0 a Chlorantraniliprole a 70.3 a 92.2 a 70.3 a 96.9 a 72.0 a Chlorantraniliprole a 87.5 a 96.9 a 75.0 a 79.7 a 59.4 a % dead or moribund larvae on Blossoms Fruit % of fruit with feeding scars % of fruit with larval tunnels Untreated 6.3 b 16.7 b 70.0 a 86.7 a Chlorantraniliprole a 20.0 b 93.3 a 86.7 a Chlorantraniliprole a 10.0 b 76.7 a 96.7 a Considerations for Chlorantraniliprole as a Drip-Chemigation Insecticide in Tomatoes The novel mode of action of chlorantraniliprole, combined with its low mammalian toxicity profile and long-lasting activity make it a particularly attractive new insecticide for the control of Lepidopterous pests in fruiting vegetables (4,17). In our experiments, a single chemigation injection of chlorantraniliprole at kg ai/ha or two injections (14 days apart) at kg ai/ha provided effective control of tomato fruitworm (Helicoverpa zea) for the remaining duration of the growing period. In general, the percentage of harvested fruit injured by Lepidopterous larvae in chlorantraniliprole plots was significantly lower than that in the untreated control and comparable in efficacy to multiple foliar applications of standard insecticide treatments (3,6,7). Residual ingestion bioassays using laboratory reared insects showed that chlorantraniliprole had systemic activity through the leaves of the tomato plants for up to 66 DAT and through blossoms up to 22 DAT. No activity of chlorantraniliprole was detected in fruits. Even though residual activity in the field cannot be directly inferred from the results of laboratory bioassays, they are good indicators of the extended residual of this product applied by drip chemigation. Moreover, since growers currently rely on the use of multiple applications of foliar-applied insecticides to manage Lepidopterous pests in commercial tomatoes (1), there is great potential for chlorantraniliprole to reduce the total number of insecticide sprays and total pesticide input on tomatoes, potentially minimizing any negative effect on non-target organisms and reducing overall input costs for the grower. Sound resistance management practices should be incorporated into the overall pest management program for tomatoes to ensure rotation of chlorantraniliprole with other effective insecticides with distinct modes of action. This is particularly relevant given the extended residual control of this product when applied by drip chemigation. Acknowledgments Authors would like to thank E. I. du Pont de Nemours and Company for supporting this research and for reviewing a previous draft of this manuscript.

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