2008 vol. 69, 115-124 DOI: 10.2478/v10032-008-0026-z ______

THE INFLUENCE OF SPINOSAD AND AZADIRACHTIN ON BENEFICIAL FAUNA NATURALLY OCCURRING ON CABBAGE CROPS

Bożenna NAWROCKA Reaserch Institute of Vegetable Crops Konstytucji 3 maja 1/3, 96-100 Skierniewice, Poland Received: August 27, 2008; Accepted: December 3, 2008

Summary The influence of spinosad (SpinTor 480 SC) and azadirachtin (Neem Azal T/S) on beneficial fauna naturally occurring on cabbage crops was evaluated in field experiments conducted in years 2004-2006. The insecticides were applied as a plant spray in field recommended dosages i.e. 96 g of active ingredient (a.i.) per ha for spinosad and 24 ml a.i. per ha for azadirachtin. The effect of direct contact of larva or adult of Coccinellidae ssp., Syrphidae spp. and Chrysopidae ssp. and the percentage of cabbage aphid parasited by Diaeretiella rapae M’Intosh with residues on leaves were observed on the 3rd, 7th, 14th and 21st day after treatment. The results obtained in conducted experiments indicated that there was no influence of two tested insecticides on the reduction of above mentioned groups of predators and parasite. The number of beneficial fauna occurring on treated cabbage plants was similar to those present on control plots. key words: harmfulness, beneficial fauna, cabbage, spinosad, azadirachtin

INTRODUCTION

In Poland, the cabbage aphid Brevicoryne brassicae L. is one of the most important pest damaging cabbage crops. Very important role in keeping cabbage aphid population at low level plays beneficial fauna, in particular: parasitic - Diaeretiella rapae (M'Intosh) and other predatory belonging to Syrphidae, Coccinellidae and Chrysopidae family. Their presence on cabbage plants is a very important part of cabbage aphid integrated control method (Nawrocka 1972). Another very important group of pests causing damage to cabbage crops are caterpillars. Since 2007, spinosad at 96 g of a.i. per ha is registered in Poland in cabbage crops protection against caterpillars of Pieris rapae L., P. brassicae L., Plutella xylostella L. and Mamestra brassicae L.

Corresponding author: e-mail: [email protected] © Copyright by RIVC 116 VEGETABLE CROPS RESEARCH BULLETIN 69 ______

Above mentioned product is naturally derived insecticide classified as environmentally and toxicologically risk reduced material. However, in the same time laboratory experiment indicated their toxic effect on some beneficial insects, especially parasites (Williams et al. 2003). The approach to improve the pest management, especially in the direction of integrated biological and chemical methods is to include the impact of natural enemies and insecticides. Therefore the knowledge of the effects of insecticides on beneficial species for particular crops is very important. According to a document ”A method to measure the environmental impact of pesticides. Table 2” elaborated by Cornell University, spintor and azadirachtin are both situated close to Bacillus thuringieniss, as very selective biological insecticides which can be used in the IPM programme (Kovach et al. 1992). Also “Spinosad Technical Bulletin” classifies spinosad as a safe for beneficial fauna product. In 2003 Wiliams et al., achieved the available information on the impact of spinosad on natural enemies and classified mortality responses to spinosad using the IOBC laboratory and field scales that run from 1 (harmless) to 4 (harmful). They concealed that general parasitoids are very susceptible to spinosad whereas for most predators it is classified as harmless. They pointed that all studies agree that spinosad residues degrade quickly in the field, with little residual toxicity at 3-7 days post-application. The aim of this study was to find out if foliar application of these insecticides under field conditions have any side effect on naturally appearing beneficial fauna.

MATERIAL AND METHODS

The field experiments on foliar spray of white cabbage were conducted to estimate the influence of two reduced risk insecticides on main species of naturally appearing beneficial insects. These experiments were carried out from 2004 till 2006 on the experimental fields at the Research Institute of Vegetable Crops in Skierniewice. The following treatments: spinosad 96 g a.i per ha (as a Spintor 480 SC - 0.2 L·ha-1), azadirachtin 24 ml a.i. per ha (as a NeemAzal T/S – 2.4 L·ha-1) and the control (untreated plants) were investigated. The influence of those insecticides on predatory insects belonging to: Syrphidae, Coccinellidae and Chrysopidae families and on parasite - Diaeretiella rapae (M'Intosh) (Braconidae: Aphidiinae) was observed. Each plot dimension was 3.0 x 3.5 m and the three treatments were replicated five times in a replicated plot design. The cabbage plants were transplanted at the first week of June each year. Thirty five plants were planted on each plot. Treatments were applied when cabbage aphid population was established on cabbage plants (25% of plants were infested). To determine the influence of various treatments on beneficial fauna, each plant on each plot was examined carefully and the number of observed developmental stages of each of beneficial groups was recorded. The B. NAWROCKA – THE INFLUENCE OF SPINOSAD AND ... 117 ______observations were carried out one day before treatment and later on the 3rd, 7th, 14th and 21st day after treatment. Statistical calculations were performed using Newman-Keuls test at P=0.05 level, in accordance with EPPO standards (2004).

RESULTS

The results of three years’ experiments do not reveal any toxic effect of tested insecticides on examined beneficial fauna. Spinosad and azadirachtin were applied at the recommended doses and the experiments were carried out under field conditions. During two years of tests the number of Coccinellidae larvae (Fig. 1 & 2) and the number of Coccinellidae beetles (Fig. 3 & 4) was not significantly different on plants treated with tested insecticides and on untreated control plants. Very similar results - no significant differences in the appearance of Syrphidae ssp. larvae in cabbage aphid colonies on cabbage ( Fig. 5 & 6) and on cauliflower plants (Fig. 11 & 12) between treated and untreated plants, were observd in all conducted trials. The number of Chrysoperla sp. eggs laid on cabbage plants treated with spinosad, azadirachtin and on untreated plants was not statistically different (Fig. 7 & 8). Also the percentage of cabbage aphids parasitized by Diaeretiella rapae did not indicate any harmful effect of tested insecticides in field experiments (Fig. 9 & 10).

Note: Newman-Keuls test, the mean numbers betwen treatmens are not significantly different at P=0.05 Fig. 1. The influence of spinosad and azadirachtin on the number of Coccinellidae ssp. larvae on white head cabbage. Field experiment, Skierniewice 2004. 118 VEGETABLE CROPS RESEARCH BULLETIN 69 ______

Note: see Fig. 1 Fig. 2. The influence of spinosad and azadirachtin on the number of Coccinellidae ssp. larvae on white head cabbage. Field experiment, Skierniewice 2005.

Note: see Fig. 1 Fig. 3. The influence of spinosad and azadirachtin on the number of Coccinellidae ssp. beatles on white head cabbage. Field experiment, Skierniewice 2004.

Note: see Fig. 1 Fig. 4. The influence of spinosad and azadirachtin on the number of Coccinellidae spp. beatles on white head cabbage. Field experiment, Skierniewice 2005. B. NAWROCKA – THE INFLUENCE OF SPINOSAD AND ... 119 ______

Note: see Fig. 1 Fig. 5. Influence of spinosad and azadirachtin on the number of Syrphidae ssp. larvae on white head cabbage. Field experiment, Skierniewice 2004.

Note: see Fig. 1 Fig. 6. Influence of spinosad and azadirachtin on the number of Syrphidae ssp. larvae on white head cabbage. Field experiment, Skierniewice 2005.

Note: see Fig. 1 Fig. 7. Influence of spinosad and azadirachtin on the number o eggs laid on white head cabbage by Chrisopidae ssp. Field experiment, Skierniewice 2004. 120 VEGETABLE CROPS RESEARCH BULLETIN 69 ______

Note: see Fig. 1 Fig. 8. Influence of spinosad and azadirachtin on the number of eggs laid on white head cabbage by Chrysopidae ssp. Field experiment, Skierniewice 2006.

Note: see Fig. 1 Fig. 9. Influence of spinosad and azadirachtin on percentage of cabbage aphids parasite by Diaeratella rapae M'Intosh. Field experiment, Skierniewic 2004.

Note: see Fig. 1 Fig. 10. Influence of spinosad and azadirachtin on percentage of cabbage aphids parasited by Diaeratella rapae M'Intosh. Field experiment, Skierniewic 2006 B. NAWROCKA – THE INFLUENCE OF SPINOSAD AND ... 121 ______

Note: see Fig. 1 Fig. 11. Influence of spinosad and azadirachtin on the number of Syrphidae ssp. larvae on cauliflower. Field experiment, Skierniewice 2005.

Note: see Fig. 1 Fig. 12. Influence of spinosad and azadirachtin on the number of Syrphidae ssp. larvae on cauliflower. Field experiment, Skierniewice 2006.

DISCUSSION

Spinosad and azadirachtin - low risk insecticides are now popular components of IPM and organic plant protection programme of brassica crops in many countries (Hines & Hutchison 2001, Grišakova et al. 2006, Guerena 2006, Burkness & Hutchison 2008). This is an effect of many experiments conducted to prove their efficacy in pest control and also on their environmental side effect. For example, some field observation indicated that spinosad caused no disruption to beneficial species in commercial orchards (Arthurs et al. 2007). However, some laboratory experiments show that spinosad and azadirachtin are toxic to beneficial insects. It was found that Hyposoter didimator (Tunberg) (Ichneumonidae) a parasitoid of early larval instars of lepidopteran pests, is very susceptible to both spinosad and azadirachtin (Schneider et al. 2003). 122 VEGETABLE CROPS RESEARCH BULLETIN 69 ______

According to other investigation, azadirachtin is harmful to the 1st instar nymphs of predatory bug Macrolophus caliginosus Wagner, in the field recommended rate. The persistence of azadirachtin is short so M. caliginosus can be introduced onto crops in the glasshouse after 5 days and therefore azadirachtin may be included in the IPM programme (Tedeschi et al. 2001). Also laboratory experiment with lethal and sublethal effect of spinosad on Orius insidiosus (Say) (Hemiptera: Anthocoridae) and Geocoris punctipes (Say) (Hemiptera: Lygaeidae) showed that spinosad is less toxic to G. punctipes than other tested insecticides. Also the fecundity of O. insidiosus is significantly higher when spinosad is used than when other insecticides are applied and when compared to untreated control (Elzen et al. 2000). The way of spinosad application can influence its side effect i.e.: on beneficial insects. Xu et al. (2004) conducted laboratory experiments to see the effect of selected insecticides on Diadegma insulare (Creson) - a parasitoid of Plutella xylostella L. It was confirmed that spinosad applied on pupal stage had no toxic effect on adult emergence. However, in contact and ingestion spinosad caused 100% adult mortality of D. insulare. Medina et al. (2001) found out that spinosin and azadirachtin are not toxic to eggs and pupae of Chrysoperla carnea (Stephens) - the predator species occuring in our ecosystem. The results of conducted experiments are generally similar to above mentioned ones especially in relation to predators. Spinosad and azadirachtin showed no harmful effect on predators. Observed differences in the number of coccinellid larvae and beetles, as well as syrphid larvae between 2004 and 2005 season suggest that the number of aphid population has the influence on predatory density. It was also noted that the cabbage aphids population was higher in 2004 than in 2005. It is particularly visible in case of coccinellid larvae. Conducted experiments indicated the difference between syrphid larvae appearance on cabbage and cauliflower plants in both years, 2005 and 2006. No toxic effect of spinosad and azadirachtin on the percentage of cabbage aphids parasitized by Diaeretiella rapae is convergent with results showed by Xu et al. (2004). I also agree with the opinion that spinosad and azadirachtin can be included, in many cases to IPM programme. Concluding, this type of observation is needed to create an effective and compatible with a particular environment IPM programme for vegetable crops protection.

CONCLUSION

Spinosad and azadirachtin applied at recommended dosage for cabbage protection against cabbage aphid in field conditions did not show any harmful effect on syrphid larvae, coccinellid adults and larvae, chrysopid eggs as well as on aphid parasite - Diaeretiella rapae. B. NAWROCKA – THE INFLUENCE OF SPINOSAD AND ... 123 ______

REFERENCES

Anonymous 2001. Spinosad Technical Bulletin. DOW AgroSciences. Anonymous 2004. EPPO standards, efficacy evaluation of plant protection products, vol. 3, Insecticides & Acaricides, European and Mediterranean Plant Protection Organization, Paris, France 2004, pp. 250. Arthurs S.P., Lacey L.A., Miliczky E.R. 2007. Evaluation of the codling moth granulovirus and spinosad for codling moth control and impact on non-target species in pear orchards. Biological Control 41 (1): 99-109. [DOI: 10.1016/j.biocontrol.2007.01.001] Burkness E.C., Hutchison W.D. 2008. Implementing reduced-risk integrated pest management in fresh-market cabbage: improved net returns via scouting and timing of effective control. J.Econ.Ent. 101.(2): 461- 471. [DOI: 10.1603/0022-0493(2008)101[461:IRIPMI]2.0.CO;2] Grišakova M., Metspalu L., Jõgar K., Hiiesaar K., Kuusik A., Põldma P. 2006. Effects of biopesticide Neem EC on the large white butterfly, Pieris brassicae L. (Lepidoptera, Pieridae). Agronomy Research 4 (Special issue): 181-186. available at: http:// www.eau.ee/~agronomy/vol04Spec/p4514 Guerena M. 2006. Cole crops and other brassicas: organic production. A publication of ATTRA-National Sustainable Agriculture Information Service.1-20. available at: http:// www.attra.ncat.org/attra-pub/PDF/cole.pdf Hines R.L., Hutchison W.D. 2001. Evaluation of Action Thresholds and Spinosad for Lepidopteran Pest Management in Minnesota Cabbage. J.Econ. Ent. 94.(1): 190- 196. [DOI: 10.1603/0022-0493(2001)094[0190:EOATAS]2.0.CO;2] Kovach J., Petzoldt C., Degni J.C., Tette J. 1992. New York State Integrated Pest management Program. A method to measure the environmental impact of pesticides, Table 2, list of pesticides. NY Agricultural Experiment Station Bulletin no 139. Cornell University, Ithaca, NY: 7 pp. Update version (2007) available at: http://www.nysipm.cornell.edu/publications/EIQ.html Elzen G.W., Maldonado S.N., Rojas M.G. 2000. Lethal and sublethal effects of selected insecticides and an insect growth regulator on the boll weevil (Coleoptera: Curculionidae) ectoparasitoid (Hymenoptera: ). J. Econ. Ent. 93(2): 300-303. [DOI: 10.1603/0022-0493(2000)093[0300:LASEOS]2.0.CO;2] Medina P., Budia F., Tirry L., Smagghe G., Vi E. 2001. Compatibility of Spinosad, Tebufenozide and Azadirachtin with eggs and pupae of the predator Chrysoperla carnea (Stephens) under laboratory conditions. Biocontrol Science and Technology 11(5): 597-610. Nawrocka B. 1972. [Metoda integracji walki biologicznej z chemiczną przeciwko mszycy kapuścianej (Brevicoryne brassicae L) na kapuście głowiastej białej.] Biul. Inst. Ochrony Roślin. 52: 379-387. [in Polish with English summary] Schneider M.I., Smagghe G., Gobbi A., Viñuela E. 2003. Toxicity and pharmacokinetics of insect growth regulators and other novel insecticides on pupae of Hyposoter didymator (Hymenoptera: Ichneumonidae), a parasitoid of early larval instars of lepidopteran pests. J. Econ. Entomol. 96(4): 1054-1065. [DOI: 10.1603/0022-0493(2003)096[1054:TAPOIG]2.0.CO;2] Tedeschi R., Alma A., Tavella L. 2001. Side-effects of three neem (Azadirachta indica A. Juss) products on the predator Macrolophus caliginosus Wagner (Het., Miridae). J. App. Entomol. 125 (7): 397-402. [DOI: 10.1046/j.1439-0418.2001.00563] 124 VEGETABLE CROPS RESEARCH BULLETIN 69 ______

Williams T., Vale J., Vi E. 2003. Is the naturally derived insecticide Spinosad® compatibile with insect natural enemies? Biocontrol Sci. Technol. 13(5): 459-475. [DOI: 10.1603/0022-0493(2001)094[0055:LASEOI]2.0.CO;2] Xu Y., Liu T., Gary L., Leibee G.L., Jones W.A., 2004. Effects of selected insecticides on Diadegma insulare (Hymenoptera: Ichneumonidae), a parasitoid of Plutella xylostella (Lepidoptera: Plutellidae). Biocontrol Sci. Technol. 14 (7): 713-723. [DOI: 10.1080/09583150410001682395]

WPŁYW SPINOSADU I AZADIRACHTYNY NA NATURALNIE WYSTĘPUJĄCĄ FAUNĘ POŻYTECZNĄ NA WARZYWACH KAPUSTNYCH

Streszczenie W latach 2004-2006 przeprowadzono doświadczenia nad wpływem spinosadu (SpinTor 480 SC) oraz azadirachtyny (NeemAzal T/S) na naturalnie występującą faunę pożyteczna na warzywach kapustnych. Wymienione środki w dawkach 96 g s.a./ha dla spinosadu i 24 ml s.a.·ha-1 dla azadirachtyny nanoszono na rośliny w formie opryskiwania. Wpływ bezpośredniego kontaktu pozostałości badanych środków, na liściach roślin, na obecność drapieżnych biedronek, bzygów i złotooków oraz procent spasożytowanych mszyc przez pasożytniczą błonkówkę Diaeretiella rapae M’Intosh oceniano w 3,7,14 i 21 dni po wykonaniu zabiegu. Uzyskane wyniki wskazują, że żaden z trzech badanych insektycydów nie wykazał ujemnego wpływu na występowanie wymienionych grup owadów pożytecznych. Nie stwierdzono istotnych różnic w liczebności owadów dorosłych, larw i jaj drapieżców oraz procentu spasożytowania mszyc w porównaniu z kombinacjami traktowanymi i kombinacją kontrolną nie traktowaną.