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Insect Growth Regulator Effects of Azadirachtin and Neem Oil On H Kraiss, EM Cullen insecticides, to prevent or minimize economic yield by the oil and unique components of complete neem loss.5,7 oil which affect insecticide efficacy. Additionally, a formulation containing complete neem oil was shown 1.2 Arthropod pest management in organic to be more effective than an azadirachtin formulation agriculture in causing adult mortality when treating fruit flies, Arthropod pest management in organic farming Ceratitus capitata (Wiedemann).18 emphasizes a systems approach,8,9 using multiple and Neem-derived insecticides are regarded as varied tactics to prevent damaging pest levels and generally compatible with insect natural enemy minimize the need for curative measures.10 Tactics conservation.10,19 Adult green lacewings, Chrysoperla including, but not limited to, pest-resistant or -tolerant carnea (Stephens), were provided azadirachtin- crop plant selection, crop rotation, soil management treated water with no effect on mortality or and biological control are incorporated into the fertility of the insect.20 Although there was a organic cropping system design.10,11 Only when a significant reduction in C. carnea fecundity, the combination of these tactics has failed to keep pests effect was reversible upon discontinued ingestion below economically damaging levels can National of azadirachtin. When three braconid parasitoids of Organic Program (NOP)-approved insecticides be tephritid fruit flies were monitored for emergence utilized.9,11 Because of reliance on multiple arthropod from azadirachtin-treated fly puparia, no adverse pest management tactics, it is important to ensure that effects were noted.21 Likewise, azadirachtin had insecticide use is compatible with other strategies and little impact on an aphidiid parasitoid, Lysiphlebus minimizes non-target effects on key biological control testaceipes (Cresson), of brown citrus aphid.15 agents. However, among the Coccinellidae, azadirachtin caused delayed pupation, wing deformation and 1.3 Neem-derived insecticides creation of pupa–adult intermediates in Coccinella Seed extracts of the neem tree, Azadirachta indica septempunctata L.22 Conversely, H. axyridis adults were A Juss, have been used for centuries as a botanical unaffected by low concentrations of azadirachtin used insecticide.12 Neem-derived insecticides are approved as a fungicide.23 for use in organic agriculture.13 Depending on target These conflicting reports highlight the importance of insect species and life stage, effects of neem include testing neem-derived insecticides against not only the antifeedant behavior, adult sterility and insect growth target pest insect but also key biological control agents. regulation. Antifeedant effects vary among species, but While neem-derived insecticides are commonly used insect growth disruption and adult sterility are more in organic farming,24 critical information is lacking consistent.14 Neem-derived insecticides have been on their efficacy against soybean aphid and potential shown to be effective against hundreds of pest species non-target effects on coccinellid predators which may including members of Diptera, Lepidoptera and negatively affect biological control. In a previous Hemiptera, which includes aphids.12 Azadirachtin is study, a direct spray application of azadirachtin was considered the main biologically active component of found to be innocuous to multiple life stages of neem-derived insecticides, although there are several A. glycines and H. axyridis when the insects were other limonoids present in complete neem seed oil monitored for mortality for a short term (72 h) post- that show similar insecticidal properties. treatment.25 However, it has previously been shown Both purified azadirachtin and complete neem oil that, when neem extracts were applied topically with have been proven effective in causing aphid mortality. a microsyringe to aphids, it took as many as 9 days Brown citrus aphids, Toxoptera citricida (Kirklady), for insect growth regulating effects to be detected.26 were fed citrus leaves dipped in azadirachtin, resulting Similar contact toxicity may likewise be detected in increased adult and nymph mortality, reduced with a direct spray to the insects. These effects may number of nymphal molts and decreased adult be expressed as immature insects attempt to molt fecundity at all tested concentrations.15 Spraying into later stages of their life cycle. Furthermore, azadirachtin onto T. citricida on potted citrus azadirachtin may be expected to have an effect on plants also significantly reduced aphids, while the fecundity rather than mortality when treating adult water-treated control population increased. Systemic stages of insects.27 applications of azadirachtin to rape plants, Brassica napus subsp. napus L., significantly reduced cabbage aphid, Brevicoryne brassicae (L.), nymphal longevity, 1.4 Objectives increased nymphal mortality and reduced adult The objectives of this study were to assess the fecundity.16 There is some evidence that complete long-term effects of a direct spray application of an neem seed oil may be more effective than purified azadirachtin commercial insecticide formulation and azadirachtin. Neem seed oil caused 62% more pea complete neem seed oil against multiple life stages aphid, Acyrthosiphon pisum Harris, nymphal mortality of A. glycines and H. axyridis. Mortality, development than purified azadirachtin when aphid nymphs were time and fecundity of survivors were recorded in order placed on treated plants.17 The authors attributed this to address possible differential insect growth regulator result to increased penetration of the insect cuticle effects by insect species and life stage. Pest Manag Sci (2008) DOI: 10.1002/ps Effects of neem insecticides on A. glycines and its predator 2 MATERIALS AND METHODS supply of soybean aphid and frozen Ephestia kuehniella 2.1 Aphis glycines colony and bioassay test Zeller (Lepidoptera: Pyralidae) eggs (Beneficial Insec- units tary, Redding, CA). An A. glycines colony was founded from individ- Petri dishes containing the male and female pairs uals collected in summer 2005 from soybeans at were checked daily for egg masses. Eggs were Arlington Agricultural Research Station, University transferred to a new petri dish (100 × 15 mm) and of Wisconsin-Madison, Arlington, WI. Aphids were kept under the aforementioned conditions. Eggs were maintained on soybean plants (variety ‘Vinton 81’). allowed to hatch, and larvae were reared in fresh petri Soybean plants were grown four plants per 15 cm pot dishes to the desired developmental stage on a diet of in a 1:1 mix of 3M Metro Mix (Conrad Fafard, Inc., frozen E. kuehniella eggs. Agawam, MA) and sphagnum peat moss, with a pinch The experiment was conducted on first and third of Bradyrhizobium japonicum (Nitrogin, Inc., Brook- instars, pupae and adults. Larvae and pupae were field, WI) inoculum added per pot. Plants were grown sprayed 24 ± 4 h after molting. Adults were sprayed in a greenhouse, supplemented with grow lights to 5–7 days after molting. Fifteen individuals of the attain a 16:8 h light:dark photoperiod. Plants were larval stages or ten individuals of pupal or adult fertilized weekly using 20-9-20 water-soluble fertilizer (1:1 sex ratio) stages were considered a replication. (Technigro, Bellevue, WA) and irrigated as needed. Pupae were removed from the substrate on which As aphid-infested plants began to decline, leaves were they had formed by using a razor blade. Replicate excised and placed on healthy plants. Once the aphids groups of larvae, pupae or adults were then placed had migrated to healthy plants, dead plant material into plastic petri dish bottoms (100 × 15 mm) for was removed. treatment application. Test units were kept in a ◦ Aphid adults were randomly collected from the temperature-controlled chamber at 25 ± 1 Cand colony using a fine-tip, No. 1 camel hair brush 16:8 h light:dark photoperiod until time of treatment. and placed on an excised aphid-free soybean leaflet, selected from the upper portion of an uninfested plant, 2.3 Treatments with the underside of the leaf facing upwards, in 2.3.1 Neem-derived insecticides a plastic petri dish (100 × 15 mm). The petiole of Treatments included azadirachtin 45 g L−1 EC the leaflet was wrapped in moistened cotton and (Neemix 4.5 EC; Certis USA, Columbia, MD; 0.511 kept moist until the leaflet was discarded. Petri Lha−1 = 23 g AI ha−1), neem seed oil (Ahimsa Botan- dishes were kept in a temperature-controlled chamber icals, Bloomington, MN; 1% v:v) emulsified with at 22 ± 1 ◦C with a 16:8 h light:dark photoperiod. organic castile soap (Dr Bronner’s Soaps, Menomonee Nymphs produced by these adults were removed Falls, WI; 0.1% v:v) and a deionized water-only con- daily and combined randomly into groups of ten, trol. Neemix was applied at the highest labeled field and each group was placed on a soybean leaflet rate for aphids on a legume crop. A 1% solution of in a petri dish unit, identically to the adults. If neem oil was chosen because this concentration had the desired stage for experimentation was nymph, been found to significantly reduce cotton aphid, Aphis these groups were then used as the test unit for the gossypii Glover, populations under field conditions.28 bioassay. Thus, the bioassay was carried out on first A carrier volume equivalent to 281 L ha−1 (deionized instars. If the desired stage was cohort adults, these water) was used to determine the ratio of insecticide groups were raised to adults, being provided fresh to water needed to prepare treatments for labora- leaflets every 2 days. On the day of the adult aphid tory bioassay. This application volume is similar to bioassay, the groups of F1 adults were transferred to the range recommended to achieve optimal soybean new petri dishes with fresh leaflets. Test units were canopy deposition with insecticides under commercial kept in a temperature-controlled chamber under the field conditions.29 aforementioned conditions until the time of spraying. 2.3.2 Laboratory bioassay 2.2 Harmonia axyridis colony and bioassay test The experiment for each developmental stage of units each insect consisted of the three direct spray The H.
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