Blackwell Publishing AsiaMelbourne, AustraliaAENAustralian Journal of Entomology1326-6756© 2006 The Authors; Journal compilation © 2006 Australian Entomological Society? 2006453244248Original ArticleImpact of aphicide drenches P G Cole and P A Horne

Australian Journal of Entomology (2006) 45, 244–248

The impact of aphicide drenches on tasmaniae (Walker) (: ) and the implications for pest control in lettuce crops

Peter G Cole* and Paul A Horne

IPM Technologies Pty Ltd, PO Box 560, Hurstbridge, Vic. 3099, Australia.

Abstract The recent arrival of lettuce (Nasonovia ribis-nigri (Mosley) ) in Australia has resulted in a pesticide-based protection program based upon seedling drenches of imidacloprid being promoted by many advisory agencies and accepted by growers as the only option available. This has caused concern about potential for incompatibility with existing integrated pest management programs for other pests in lettuce. Two neonicotinoid insecticides, imidacloprid (Confidor 200SC) and thiamethoxam (Actara), were applied to lettuce seedlings by drenching. A model aphid (Macrosiphum euphorbiae (Thomas) ), used because N. ribis-nigri was not present in mainland Australia at that time, was periodically released onto the seedlings over 10 weeks. The effects of imidacloprid and thiamethoxam on larvae of predatory brown lacewings (Micromus tasmaniae (Walker) ) which fed on the were measured over 10 weeks by bioassay. Imidacloprid applied at a rate of 11 mL active ingredient (ai) per 1000 seedlings and thiamethoxam applied at 0.5 g ai per 1000 seedlings were highly toxic to M. tasmaniae that consumed aphids from the seedlings for up to 4 weeks after application. A 1/10 rate of imidaclo- prid (1.1 mL ai per 1000 seedlings) caused moderate toxicity for 3 weeks, and was then harmless to M. tasmaniae. Thiamethoxam and the high rate of imidacloprid caused almost complete mortality of aphids for about 6 weeks after application, and the low rate of imidacloprid displayed similarly high activity for about 3 weeks. Key words imidacloprid, insecticide toxicity, integrated pest management, IPM lettuce, Micromus tasmaniae, thiamethoxam.

INTRODUCTION tasmaniae (Walker) (brown lacewing), Nabis kinbergii (Reu- ter) (damsel bug), Coccinella transversalis F. (transverse lady- There are several major lettuce-growing regions in Australia, bird) and Aphidius colemani (Viereck) (aphid parasite). The including the Lockyer Valley in southern Queensland, the use of selective insecticides which only kill the target pest is Riverina of New South Wales, Werribee in southern Victoria, critical in allowing populations of the beneficial species to the Adelaide Hills of South Australia and northern Tasmania establish in the crop. Micromus tasmaniae is the major pred- (Australian Bureau of Statistics 2004). Despite the differences ator of aphids in lettuce and other crops using IPM in southern in climate and growing seasons between these regions, there Australia (Horne et al. 2000). are several common pests which can impact on crop During the growing season of 2003/04 a new aphid pest yields. These include Helicoverpa punctigera (Wallengren) species, Nasonovia ribis-nigri (Mosley) (lettuce aphid) was (native budworm), H. armigera (Hübner) (cotton bollworm), found in lettuce crops in northern Tasmania, which was the Frankliniella occidentalis (Pergande) (Western flower thrips) first recording of this species in Australia (AUSVEG 2004). It and various species of aphids. has subsequently spread to mainland Australia (Van Meurs In recent years, control strategies for these pests have been 2005). This aphid is an established pest of lettuce in New shifting away from routine applications of broad-spectrum Zealand, North America (Forbes & MacKenzie 1982; insecticides. Growers of lettuce, especially in Victoria, are Palumbo 2002) and Europe (Reinink & Dieleman 1993; now more aware of integrated pest management (IPM) and Edward 1999). Its characteristic of reproducing deep inside they incorporate applications of selective or ‘soft’ insecticides the heads of maturing lettuces, where it is difficult for insec- with cultural and biological control methods. Biological con- ticide sprays to reach it, has resulted in high yield losses to trol components usually rely on the build-up of natural popu- growers from rejection of produce by buyers. lations of beneficial species, which include Micromus The Australian vegetable industry is greatly concerned about the impact which this pest may have on lettuce crops. *[email protected] Recent strategic plans (AUSVEG 2005), which are attempting © 2006 The Authors Journal compilation © 2006 Australian Entomological Society doi:10.1111/j.1440-6055.2006.00534.x Impact of aphicide drenches 245 to combat the potential impact of this pest, have included The water volume for all treatments and control was 5.0 L/ support of planting resistant lettuce varieties and increased 1000 seedlings, and the rates of imidacloprid applied were rates of imidacloprid insecticide as a seedling drench. The 11 mL ai per 1000 seedlings and 1.1 mL ai per 1000 seedlings. drenching process involves overhead spraying of seedlings, Thiamethoxam was applied at 0.5 g ai per 1000 seedlings, and just prior to planting, at a volume which saturates the seedling untreated controls were drenched with water. cells but without leaching. Protocols recently put in place by For each treatment, 40 seedlings (four rows of 10 seed- state Plant Protection Agencies (Western Australia, South Aus- lings) in a conventional seedling tray were drenched using a tralia, Queensland and New South Wales) require that lettuce hand-held atomiser fitted with a manual pump. After drench- seedlings are drenched just prior to planting with imidacloprid ing, the seedlings were kept in the trays in a glasshouse for (Confidor 200SC) at a rate of 11 mL active ingredient (ai) per 24 h, and then five randomly selected seedlings from each 1000 seedlings. Based on a water application volume of 2 L treatment were transplanted into 1.5 L pots with standard pot- per seedling tray, this is a much higher rate of imidacloprid ting mix. Osmocote fertiliser was added to the soil surface, per unit area than the current recommended rate of 5.0 mL and the seedlings were watered. These five seedlings from ai/100 L for foliar sprays on other crops. Imidacloprid is toxic each treatment comprised the experimental units for the bio- to some beneficial (Mizell & Sconyers 1992; Sclar assays. They remained in the glasshouse and were maintained et al. 1998), although it can be used safely with some parasi- by overhead watering every second day for the duration of the toid species (Koppert 1998). The increase in the recommended experiment. rate may be detrimental to the establishment of beneficial species in lettuce crops where it is applied. Bioassay procedures In this paper we have assessed the effect of the high rate of imidacloprid as a seedling drench on the predator Commencing 3 days after treatment (DAT), approximately M. tasmaniae, and have compared it with a reduced rate (1/ 12 aphid nymphs were applied to each of the five seedlings 10) of imidacloprid and with another neonicotinoid aphicide, per treatment using a fine paint brush. Seedlings were cov- × thiamethoxam. The effectiveness of these rates on control of ered with a perforated polyethylene bag (400 mm 300 mm) the potato aphid, Macrosiphum euphorbiae Thomas, which is that prevented the escape of aphids. The aphids were main- a pest of lettuce, was measured. Macrosiphum euphorbiae was tained on the seedlings for 48 h, and then mortality due to used as a model aphid species because N. ribis-nigri was not the aphicides was recorded prior to them being transferred to present on mainland Australia at the time of testing. 40-mm-diameter plastic Petri dishes. At this time a second batch of aphids were placed onto the seedlings for another 48 h incubation period. A small section of leaf tissue was cut MATERIALS AND METHODS from each seedling and included in the Petri dishes. Three to five M. tasmaniae second-instar larvae were introduced to Insect colonies the Petri dishes and incubated for 96 h. After 48 h of incuba- tion, the second batch of aphids were removed from the Colonies of M. euphorbiae and M. tasmaniae were maintained seedlings and placed into the Petri dishes to provide another ° + ° at 25 C ( 1.5 C) and 12L:12D photoperiod in our laboratory. supply of prey for the M. tasmaniae larvae. The larvae were The M. euphorbiae colony was derived from individuals therefore provided with two batches of treated aphids over collected from roses in 2004. They were maintained on 96 h. When aphid mortality was less than 100% after feeding excised lettuce leaves in 3.5 L ventilated polypropylene con- on the treated seedlings, the aphids were provided to tainers. Fresh leaves were provided twice weekly, and old M. tasmaniae in approximately the same proportion of live leaves were removed. and dead individuals. We have maintained a colony of M. tasmaniae for several Mortality of M. tasmaniae was recorded after the 96 h years. Field-collected specimens have been regularly intro- incubation period, by which time the majority of aphids had duced to the colony to maintain genetic diversity. Larvae of been consumed. This bioassay procedure was performed eight M. tasmaniae were housed in polypropylene containers, as times over 75 days of the trial to evaluate the persistence of above, and were provided twice weekly with a food source of the effects of the insecticides. Results were statistically anal- green peach aphids (Myzus persicae (Sulzer) ) on excised Chi- ysed using JMP Statistical Software Release 5.0.1.2 (SAS nese cabbage leaves. The containers also had shredded paper Institute 2005). and a water-saturated cotton wool wick to maintain humidity. Larvae pupated in the containers, and when adults emerged, cotton wool squares (40 mm × 30 mm) were provided as an RESULTS egg-laying substrate. Thiamethoxam and the high rate of imidacloprid (11 mL ai Treatment applications per 1000 seedlings) were highly toxic to M. euphorbiae for up Lettuce seedlings (var. Iceberg), which were ready for plant- to 54 days, whereas the low rate of imidacloprid (1.1 mL ai ing, were drenched with Confidor 200SC (200 g L−1 imidaclo- per 1000 seedlings) remained highly toxic for about 26 days prid) or Actara (250 g kg−1 thiamethoxam). (Fig. 1). At the 26 DAT assessment, the low rate of imidaclo- © 2006 The Authors Journal compilation © 2006 Australian Entomological Society 246 P G Cole and P A Horne

Fig. 1. Mortality of Macrosi- phum euphorbiae following exposure to treated lettuce seed- lings for 48 h intervals. Error bars indicate one standard error of the mean.

Fig. 2. Mortality of Micromus tasmaniae nymphs after feeding on treated aphids for 4-day inter- vals. Error bars indicate one stan- dard error of the mean. prid caused significantly less mortality to aphids than thia- drenching, and then declined to nil mortality by 37 days methoxam (P = 0.025) and the high rate of imidacloprid (P = (Fig. 2). The mortalities were significantly higher than the 0.008). control mortalities until 23 DAT (P < 0.05), but not higher at Micromus tasmaniae larvae were adversely affected by all 29 DAT (P = 0.480) or at the subsequent assessments. three treatments, but mortality was the highest for the thia- methoxam and the high rate of imidacloprid treatments (Fig. 2). In response to thiamethoxam, mortality was at least DISCUSSION 90% for up to 29 days after drenching, and for the high rate of imidacloprid, mortality was greater than 85% for the first The high rate of imidacloprid for drenching lettuce seedlings 17 days. Mortality of M. tasmaniae in response to thia- has been recommended by the Australian vegetable industry methoxam was significantly higher than control mortality at and is currently (January 2006) required by state Plant Protec- all assessments except the final assessment at 72 DAT (P = tion Agencies in response to the threat of the spread of lettuce 0.141). In comparison, mortality in response to the high rate aphid (N. ribis-nigri Mosley) in mainland Australian lettuce of imidacloprid was significantly higher than control mortality crops (APVMA Permit 2004). We have shown that application for all assessments preceding the 46 DAT assessment, which of imidacloprid to lettuce by drenching the seedlings at the was not significantly different (P = 0.147). high rate caused high mortality of this strain of M. tasmaniae The low rate of imidacloprid caused a steady rate of mor- by eating aphids from the treated plants. Micromus tasmaniae tality (40–50%) of M. tasmaniae for the first 23 days after is one of the most important predatory in Australian © 2006 The Authors Journal compilation © 2006 Australian Entomological Society Impact of aphicide drenches 247 lettuce crops (McDougall 2002). The results suggest that those individuals. Measurements of the amount of imidaclo- establishment of M. tasmaniae in lettuce crops that have been prid in the leaf tissue and in the exposed aphids would be drenched with the recommended rate of imidacloprid may be required to confirm this hypothesis. inhibited for several weeks after planting. Field trials using Chemical control of aphids with the high rate of imidaclo- natural populations of M. tasmaniae would be necessary to prid or thiamethoxam in this trial suggests potential incompat- confirm or refute this assertion. ibility with IPM programs in lettuce crops. This work has The major pests of lettuce crops on mainland Australia are shown that the effect of seedling drenches on populations of H. armigera, H. punctigera, various species of aphids and M. tasmaniae in lettuce crops needs to be determined. potentially F. occidentalis (Western flower thrips) (McDougall 2002). Current integrated pest management practices involve regular crop monitoring, reliance on biological and cultural ACKNOWLEDGEMENTS control, and the supportive use of selective insecticides such as pirimicarb, spinosad, nuclear polyhedrosis virus-based This work was funded by Horticulture Australia Limited and insecticides and Bacillus thuringiensis-based insecticides. AUSVEG (the Australian Vegetable Grower’s Association). These insecticides are relatively specific to targeted pests and We would like to thank Janet Horne and Rhonda McBain for therefore have minimal impact on the establishment of pred- maintaining the insect colonies, and Jessica Page for her work atory beneficial insect species in the crop, although spinosad on IPM dealing with lettuce aphid. is toxic to some adult Hymenoptera (Llewellyn 2002). Bene- ficial species are known to play important roles in the control of H. armigera and H. punctigera (Zalucki et al. 1986; Men- REFERENCES sah & Singleton 1999). In crops where imidacloprid is applied as a seedling drench at 11 mL ai per 1000 seedlings, there may APVMA Permit. 2004. Australian Pesticides and Veterinary Medicines be inhibited establishment of M. tasmaniae or other beneficial Authority Permit Number PER 7416. Australian Pesticides and Vet- species such as damsel bugs (Nabis kinbergii) (P Cole unpubl. erinary Medicines Authority. Australian Bureau of Statistics. 2004. 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