Crop Protection Products for Organic Agriculture - ACS Publications

Chapter 19

Ecotoxicology of Neem

Downloaded by STANFORD UNIV GREEN LIBR on August 6, 2012 | http://pubs.acs.org Publication Date: December 14, 2006 | doi: 10.1021/bk-2007-0947.ch019

John D. Stark Department of Entomology, Washington State University, Puyallup Research and Extension Center, Puyallup, WA 98371

Because pesticides derived from the neem tree are natural products, there is an automatic assumption that they are environmentally benign. However, pesticides by definition kill living things and because the primary active ingredient of neem, azadirachtin, affects the universal molting hormone of arthropods, neem pesticides should have negative effects on at least some nontarget arthropods. Many researchers have now evaluated the toxicity of neem pesticides on various nontarget organisms in the laboratory and field. In addition, several studies on the persistence of the primary active ingredient, azadirachtin have been published. Here the ecotoxicity of neem pesticides is reviewed focusing particularly on recent studies. The general conclusion is that neem pesticides are less damaging to nontarget organisms than certain synthetic pesticides. However, some nontarget organisms are particularly sensitive to neem pesticides and therefore as with all pesticides, they should be used with caution and continue to be evaluated for nontarget effects.

© 2007 American Chemical Society In Crop Protection Products for Organic Agriculture; Felsot, A., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2006.

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276 Pesticides derived from the neem tree are often considered to be environmentally safe and less damaging to ecosystems than synthetic pesticides. However, recent evidence indicates that neem products can cause damage to some nontarget organisms. There are many biologically active components in neem seed kernels and leaves, but the primary insecticidal component is the highly oxidized limonoid, azadirachtin (1,2). Other limonoids are also present in neem seeds that are toxic or repellent to insects (3,4). Azadirachtin works by inhibiting the release of morphogenetic peptide hormones resulting in the disruption of ecdysteroid and juvenile hormone concentrations in the hemolymph affecting molting, metamorphosis, and reproduction (2). Many studies have been published on the effects of neem on nontarget organisms. It is not my intention to review all of the literature on the toxicity of neem to various organisms as this has been done several times in the past. For a comprehensive review of neem side effects on nontarget organisms see Schmutterer (4). Instead, the focus of this review will be on several more recent papers that deal with the effects of neem on nontarget organisms as well as field studies that involve an examination of the impact of neem on nontarget organisms. Most of the published studies dealing with the effects of neem-derived pesticides on nontarget organisms concern biological control agents because the authors were looking for compatibility of these two control methods for integrated pest management. In general, neem pesticides appear to be less toxic to biocontrol agents compared to pest species (4) and appear to be less toxic than neurotoxic insecticides (5,6). The low toxicity of neem to biological control agents may be due to the requirement of oral ingestion, low toxicity to adult insects, systemic activity, short environmental persistence, and antifeedant and repellent properties (3,7). However, the universal molting hormone of arthropods is ecdysone and because azadirachtin interferes with this hormone, organisms such as crustaceans, spiders and predatory mites may be susceptible. In fact, certain species of biocontrol agents are quite susceptible to neem as discussed below.

Toxicity of the Formulation Versus Toxicity of Neem Ingredients A major problem exists with the interpretation of the neem literature. In many of the published studies dealing with the effects of neem pesticides on pest and beneficial species, very different neem extracts/forumulations, different seed sources, and extraction methods were used. Isman et al. (8) found that active ingredients vary greatly among different seed batches. As such, it is difficult to tell what active ingredients or lack of active ingredients were actually present in these formulations. With the advent of standardized commercial neem formulations and advances in analytical methodology for neem, many of the

In Crop Protection Products for Organic Agriculture; Felsot, A., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2006.


277 recent studies with neem pesticides are conducted with standardized formulations, making interpretation of the data much easier than in the past. Several studies have been conducted that indicate that at least part of the toxicity observed in various species is due to the formulation of commercial neem products and not solely to the active ingredients. Sauke and Schmutterer (9) determined that the formulation of a neem insecticide and not the active ingredients were responsible for the toxicity observed in the water flea, Daphnia magna. Stark and Walter (70) found that neem oil accounted for 60% of the toxicity to pea aphids while Kreutzweiser et al. (77) suggested that the formulation accounts for some of the toxicity to aquatic invertebrates. Additionally, Stark (72) exposed Daphnia pulex to the commercial neem pesticide, Neemix and a formulation blank containing no neem components and found that 47% of the observed toxicity was due to the formulation. These results indicate that the toxicity attributed to neem may be due at least partially to the formulation.

Persistence of Azadirachtin The persistence of azadirachtin, the primary insecticide in neem has been studied in soil, water and on foliage. Azadirachtin is as persistent as the carbamates carbaryl and methomyl and the pyrethroids esfenvalerate and permethrin in water and soil (6). Stark and Walter (75) found that azadirachtin had a disappearance time of approximately 20 days in soil at 25°C. This increased to 31-42 days when the soil was autoclaved indicating that microbes played a major role in degradation of azadiracthin. In water, azadirachtin had a 1-12 day half-life (14). Azadirachtin had a half-life on foliage of less than 1 day similarly to diazinon and malathion (75). Thus, the persistence of azadirachtin is similar to that of some synthetic insecticides (6).

Effects on Biocontrol Agents

Parasitoids Many studies have been conducted on the effects of various neem products to parasitoids. Results of some studies indicate that neem pesticides are not very toxic to parasitoids. For example, injection of azadirachtin into tobacco budworm (Manduca sexta [Linnaeus]) larvae that had been parasitized by the braconid wasp Cotesia congregata (Say) did not negatively affect parasitoid development if the compound was administered after the parasitoids had ecdysed to the second instar (75). However, results of other studies have indicated that



278 neem may indeed have detrimental effects on some parasitoid species. Stark et al. (77) examined the effects of a neem insecticide on three braconid parasitoids of tephritid finit flies. Two of these parasitoids developed normally in flies that had been exposed to concentrations of azadirachtin that completely inhibited host fly eclosion. However, in one species, Psytallia incisi (Silvestri), reproduction was reduced 63-88% after exposure to 20 mg azadirachtin/L. Laboratory experiments were carried out to study the effect of several different neem insecticides on Trichogramma japonicum Ashmead (75). The rate of parasitization and emergence of adults from parasitized eggs was examined. Econeem and Neem Azal were found to be safer compared to the synthetic insecticides quinalphos and chlorpyrifos, which had adverse effects on parasitization. However, the neem formulations Nimbecidine, Neemgold and Rakshak negatively affected parasitization. Villanueva and Hoy (19) assessed the compatibility of several neem insecticides with the citrus leafminer parasitoid, Ageniaspis citricola (Logvinoskaya). They found that Neemix was compatible with this parasitoid, but Align and Neemgard were only semi-compatible for I P M of the leafminer. These differences in effect were probably due to differences in the type and amount of active ingredient and/or components of the formulations. The effects of neem seed oil on the egg parasitoid Trichogramma chilonis (Ishii) was determined by Raguraman and Singh (20). Oviposition deterrence was detected after exposure to neem oil concentrations of 0.3%. Two neem insecticides were found to significantly reduce the food consumption of larvae and emergence of adult Cotesia plutellae (Kurdyumov), a parasitoid of the diamondback moth (27). Thakur and Pawar (22) found that the egg parasitoid T. chilonis was unaffected by two neem insecticides, Achook and Neemactin, while Goudegnon et al. (23) found no effect of neem extract on the parasitoid C. plutellae. Akol et al. (24) investigated the effects of two neem insecticides on a parasitoid of the diamondback moth, Diadegma mollipla (Holmgren). They found that Neemroc and Neemros applied at rates that controlled the diamondback moth did not adversely affect survival and foraging behavior of D. mollipla. Matter et al. (25) studied the effects of neem on the Pieris rapae (Linnaeus) parasitoid, Hyposoter ebeninus (Grav). Treatment with neem at the LC50 level resulted in a large reduction in parasitoid progeny. However, treatment of P. rapae with low concentrations of neem (LC25) could reasonably potentiate parasitism 2-3 times over untreated hosts without drastic losses in parasitoid emergence. Tang et al. (26) evaluated the neem insecticide Neemix 4.5 as a control for the brown citrus aphid and examined the compatibility of this insecticide with a parasitoid of the aphid, Lysiphlebus testaceipes (Cresson). Parasitoid survival and development was virtually unaffected by Neemix. The reproduction and survival of the egg parasitoid Trichogramma minutum Riley after exposure to two neem insecticides, Azatin E C and Neem E C , was


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evaluated by Lyons et al. (27). They established that exposure to 50 g azadirachtin/ha, resulted in no significant effect on female survival. However, exposure to 500 g azadirachtin/ha, significantly reduced female survival. Exposure to pure azadirachtin did not reduce survival, indicating that other components of the formulations were in part responsible for the toxicity to females. The varying results of the studies listed above indicate that susceptibility of parasitoids to neem is dependent upon the species and the type of neem insecticide. N o generality about the effects of neem pesticides on parasitoids can be drawn.

Predators

Lady beetles Adult seven spot lady beetles, Coccinella septempunctata L., were exposed to 2% neem seed kernel extract or 3% neem oil. Egg production was not affected by either treatment but metamorphosis was negatively affected (28). Kaethner (29) also evaluated the toxicity of two neem insecticides to C. septempunctata. High concentrations (250 and 1000 ppm azadirachtin) were virtually nontoxic to eggs, 2 instars and adults when they were exposed to dried residues on bean leaves. Toxicity to larvae, however, was evident after exposure to direct sprays. Lowery and Isman (30) found that a neem insecticide caused no reduction in survival of C. undecimpunctata L . larvae after topical exposure. However, exposure of larvae to treated foliage and treated food (aphids) resulted in no adult eclosion. Banken and Stark (37) found that the neem insecticide Neemix was relatively non-toxic to 1 and 4 instars of C. septempunctata after direct spray application. LC50's were substantially higher than recommended field application rates. However, in a later study, C. septempunctata was found to be more susceptible than indicated by the earlier study. Banken and Stark (32) exposed C. septempunctata to direct sprays, treated foliage and a pesticidetreated food source, pea aphids. Multiple routes of exposure resulted in greater mortality and effects on egg laying than direct exposure alone. However, the equivalent of 100 ppm azadirachtin, which is a concentration above the recommended field rate, was required to cause a significant effect. Two ladybeetles, Cycloneda sanguinea (L.) and Harmonia axyridis (Pallas), were exposed in the laboratory to neem oil (33). Significant mortality of C. sanguinea larvae occurred after exposure to neem oil as a leaf residue, but not nd

st

th



280 after topical application. However, no negative effect was found in larvae of H. axyridis. Q i et al. (34) fed Harmonia conformis (Boisduval) the larvae of Helicoverpa armigera (Hubner) that had fed on neem. They found that H. armigera larvae exposed to 50- and 200-ppm azadirachtin treatments were not toxic to H. conformis. Elzen and James (35) evaluated the toxicity of neem oil and azadirachtin to the ladybeetle Coleomegilla maculata De Geer. Both of these products exhibited low toxicity to this species. Based on the results of the above-mentioned studies, it appears that the toxicity of neem to ladybeetles depends upon the formulation being evaluated and the susceptibility of individual species, and thus no generality about the toxicity of neem and ladybeetles can be made.

Predaceous mites Stark et al. (36) found that a predaceous mite, Iphisieus degenerans Berlese, and its prey, the two-spotted spider mite, Tetranychus urticae Koch, were equally susceptible to the neem-based insecticide Neemix based on comparisons of the acute LC50. However, when population growth rate was examined, the predator was much more susceptible than its prey. Two spotted spider mite populations were able to maintain a positive growth rate after exposure to the acute L C i of immatures and the L C of adults. Predator mite populations were declining and headed for extinction when exposed to the acute L C for immatures and the L C for adults. Thus, in this study neem was not selective and in fact was much more toxic to the predator than to its prey. The side effects of the neem insecticide Neemark on Phytoseiulus persimilis Athias-Henriot, a predator of the twospotted spider mite T. urticae, were evaluated by Papaioannou et al. (37). Neemmark at 3% and 5% concentrations was highly toxic to immature stages and the adult of P. persimilis. Childers et al. (38) compared the residual toxicity of neem oil to the predaceous mite, Agistemus industani Gonzalez (Acari: Stigmaeidae). Neem oil 90 E C applied at 46.8 L/ha was found to be highly toxic to this predator. The susceptibility of the predaceous mite /. degenerans to neem oil and azadirachtin was evaluated by Ludwig and Oetting (39). Both of these products caused mortality in this species. Similar findings were obtained by Stark et al. (36) with the same species. Cote et al. (40) studied the effects of neem oil on P. persimilis. Neem oil caused no mortality in P. persimilis up to 14 days after initial exposure, indicating that it could be used compatibly with this predator to control T. urticae. 9

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Spiders Several laboratory and field studies on the effects of neem on spiders have been published. Saxena et al. (41) found that topical application of 50 μg of a neem seed kernel extract did not affect the spider Lycosa pseudoannulata (Boesberger & Strand). Mansour et al. (42) determined that 2.5% extracts of neem seed prepared with various solvents were non-toxic to the spider Chiracanthium mildei L . Koch. However, residues from 4% extracts with pentane, acetone, and ethanol resulted in 71, 54, and 33% mortality, respectively. Stark (43) found that applications of Margosan-0 had no significant effect on spiders inhabiting turf grass.

Other predators Macrolophus caliginosus Wagner, a mirid hemipteran, was exposed to three neem pesticides, Neem-Amin E C , Stardoor and B.P. 20/S (44). A l l three products were harmful to first instar nymphs exposed to fresh dry residues on glass plates, resulting in LD50 values much lower than the maximum recommended use rate.

Effects on Other Non-Target Organisms Bees Schmutterer and Hoist (45) conducted field studies to evaluate the impact of neem on honey bees foraging on neem-treated mustard and rape. They found that large honey bee colonies were unaffected by the neem treatments while low numbers of bees were killed in smaller colonies. Bunsen (46) conducted both laboratory and field studies on the effects of neem and honey bees and found that only direct contact of larvae with neem resulted in mortality.

Earthworms and Beneficial Nematodes Neem soil treatments were found to increase Eisenia fetida (Savigny) weight, survival and reproduction (47). Stark (48) investigated the effects of the neem insecticide Margosan-0 on the entomopathogenic nematode species Steinernema carpocapsae (Steiner), S. feltiae (Filipjev) and S. glaseri (Steiner). Margosan-0 was toxic to all three



282 species but only at concentrations higher than the recommended field rate (20 ppm). Infectivity was only affected at concentrations greater than 200 ppm azadirachtin. In an earlier study, Rovesti and Deseô (49) found that a crude neem extract was toxic to five species of entomopathogenic nematodes including the three species evaluated by Stark (48). Hussaini et al. (50) explored the compatibility of neem and two strains each of the entomopathogenic nematodes Steinernema bicomutu Tallosi, Peters & Ehlers and Heterorhabditis indie* Poinar, Kanunakar, and David. Neem was not toxic to S. bicornutum but was toxic to one strain of H. indica. The effects of neem on the entomopathogenic nematode S. feltiae was evaluated by Krishnayya and Grewal (51). Neem oil had no effect on the viability and virulence of S. feltiae.

Aquatic Invertebrates Several laboratory studies have been conducted to examine the toxicity of various neem pesticides on aquatic invertebrates, particularly water fleas (Daphnia). For example, Saucke and Schmutterer (9) estimated the LC50 for Daphnia magna Straus at 0.19 mg/L while Scott and Kaushik (52) estimated an LC50 of 125 mg/L for the same species. Stark (12) evaluated the toxicity of three commercially produced neem insecticides, Neemiz, Azatin and RH-9999 (a wettable powder containing 20% 22, 23-dihydro-azadirachtin) to the water flea D. pulex (Leydig). He found no significant difference between Neemix and Azatin in terms of LC50, but RH-999 was significantly less toxic than the other two products.

Fish Several studies involving estimates of toxicity of neem to various fish species have been published. Attri and Prasad (53) studied the toxicity of neem oil extract to Gambusia sp. in the laboratory. The extract was nontoxic at 0.005% but caused 100 % mortality at 0.4%. Margraf (54) applied neem oil (ΙΟ Ι 00 mg/L) to rice paddy fields in the Philippines and found no negative effect on the fish Misgurnus anguillicaudatus (Cantor). Wan et al. (55) estimated the 96 h LC50 of pure azadirachtin to juvenile coho and Chinook salmon to be approximately 4 mg/1. The acute toxicity of water extracts of bark of the Neem tree was evaluated in the cichlid Tilapia zilli Gerv by Omoregie and Okpanachi (56). The 96 h LC50 was estimated to be 6.03 mg/1. Exposure to the neem extract also increased opercular ventilation rates. Prior to death, darkening of the exposed fish, erratic swimming, and respiratory distress occurred. The acute toxicity of neem to Indian carp was evaluated by Das et al. (57). Fingerlings of Rohu (Labeo rohita [Hamilton]), Catla (Catla catla [Hamilton]),


283 and Mrigal (Cirrhinus mrigala [Hamilton]) carp were exposed to limnoids of neem, and the 96 h LC50's were estimated to be 2.36, 2.04, and 2.78 ppm, respectively. In summary, toxicity studies with fish indicate that some species may be susceptible to neem while others are not.


Field Studies

Aquatic Field Studies Several field studies on the effects of neem insecticides on aquatic organisms have been conducted. See Thompson and Kreutzweiser (Chapter 18 of this publication) for a more detailed discussion of field experiments with neem. Dunkel and Richards (58) studied the effects of a neem insecticide on nontarget stream insects and found that these species may be vulnerable to neem insecticides at the expected environmental concentration (EEC) of 0.035 mg/1. However, a field study conducted by Kreutweizer et al. (59) indicated that the neem-based insecticide Neemix caused significant changes to an aquatic community, but only at concentrations much higher than the E E C (0.035 mg/1). These conflicting results indicate a need for further research on the aquatic ecotoxicological effects of neem.

Terrestrial Field Studies A comparison of the impact of the neem insecticide, Margosan-0 and the synthetic organophosphorous insecticide, chlorpyrifos on invertebrates inhabiting a turf grass ecosystem was conducted by Stark (5). Margosan-0 had much less effect on most of the invertebrates studied compared to chlorpyrifos. However, certain groups of invertebrates, particularly the Oribatid mites were more susceptible to neem than to chlorpyrifos. The sminthurid and nonsminthurid Collembola were less susceptible to Margosan-0 than to chlorpyrifos but their populations were significantly reduced compared to the control. Chorpyrifos, but not Margosan-O, significantly reduced populations of nonoribatid mites and spiders. In general, Margosan-0 was less detrimental than chlorpyrifos to most of the organisms studied. M a et al. (60) conducted a field study to control Helicoverpa spp. in cotton. Moderate rate-dependent control was obtained in plots treated with neem seed extracts containing azadirachtin at rates of 30, 60 and 90 g/ha. Several predators, including lady beetles, lacewings, spiders and predatory bugs, were not affected by neem.


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Conclusions Based on the studies reviewed here it appears that some nontarget organisms are susceptible to neem pesticides while other species are not very susceptible. However, much of the data suggest that insecticides derived from the neem tree are less likely to cause substantial environmental damage than synthetic insecticides. Because the active ingredients in neem are poisons and some species are very susceptible to these products, they should be used cautiously. Future studies designed to investigate the contribution of various neem liminoids and neem oil to toxicity of nontarget organisms should be conducted so that specialized neem products can be developed to target certain pests while sparing their natural enemies. Additionally, the contribution to toxicity of individual adjuvants that are components of various neem formulations should be determined so that they may be avoided when designing new neem pesticides.

References 1. 2. 3. 4.

5. 6.

7. 8. 9. 10. 11. 12. 13. 14.

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