5
Effects on Insects

The growing accumulation of experience demonstrates that neem products work by intervening at several stages of an insect's life. The ingredients from this tree approximate the shape and structure of hormones vital to the lives of insects (not to mention some other invertebrates and even some microbes). The bodies of these insects absorb the neem compounds as if they were the real hormones, but this only blocks their endocrine systems. The resulting deep-seated behavioral and physiological aberrations leave the insects so confused in brain and body that they cannot reproduce and their populations plummet.

Increasingly, approaches of this kind are seen as desirable methods of pest control: pests don't have to be killed instantly if their populations can be incapacitated in ways that are harmless to people and the planet as a whole. In the 1990s this is particularly important: many synthetic pesticides are being withdrawn, few replacements are being registered, and rising numbers of insects are developing resistance to the shrinking number of remaining chemical controls.

The precise effects of the various neem-tree extracts on a given insect species are often difficult to pinpoint. Neem's complexity of ingredients and its mixed modes of action vastly complicate clarification. Moreover, the studies to date are hard to compare because they have used differing test insects, dosages, and formulations. Further, the materials used in various tests have often been handled and stored differently, taken from differing parts of the tree, or produced under different environmental conditions.

But, for all the uncertainty over details, various neem extracts are known to act on various insects in the following ways:

  • Disrupting or inhibiting the development of eggs, larvae, or pupae;

  • Blocking the molting of larvae or nymphs;

  • Disrupting mating and sexual communication;

  • Repelling larvae and adults;

  • Deterring females from laying eggs;



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5 Effects on Insects The growing accumulation of experience demonstrates that neem products work by intervening at several stages of an insect's life. The ingredients from this tree approximate the shape and structure of hormones vital to the lives of insects (not to mention some other invertebrates and even some microbes). The bodies of these insects absorb the neem compounds as if they were the real hormones, but this only blocks their endocrine systems. The resulting deep-seated behavioral and physiological aberrations leave the insects so confused in brain and body that they cannot reproduce and their populations plummet. Increasingly, approaches of this kind are seen as desirable methods of pest control: pests don't have to be killed instantly if their populations can be incapacitated in ways that are harmless to people and the planet as a whole. In the 1990s this is particularly important: many synthetic pesticides are being withdrawn, few replacements are being registered, and rising numbers of insects are developing resistance to the shrinking number of remaining chemical controls. The precise effects of the various neem-tree extracts on a given insect species are often difficult to pinpoint. Neem's complexity of ingredients and its mixed modes of action vastly complicate clarification. Moreover, the studies to date are hard to compare because they have used differing test insects, dosages, and formulations. Further, the materials used in various tests have often been handled and stored differently, taken from differing parts of the tree, or produced under different environmental conditions. But, for all the uncertainty over details, various neem extracts are known to act on various insects in the following ways: Disrupting or inhibiting the development of eggs, larvae, or pupae; Blocking the molting of larvae or nymphs; Disrupting mating and sexual communication; Repelling larvae and adults; Deterring females from laying eggs;

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Sterilizing adults; Poisoning larvae and adults; Deterring feeding; Blocking the ability to "swallow" (that is, reducing the motility of the gut); Sending metamorphosis awry at various stages; and Inhibiting the formation of chitin.1 As noted earlier, neem extracts have proved as potent as many commercially available synthetic pesticides. They are effective against dozens of species of insects at concentrations in the parts-per-million range. At present, it can be said that repellency is probably the weakest effect, except in some locust and grasshopper species. Antifeedant activity (although interesting and potentially extremely valuable) is probably of limited significance; its effects are short-lived, and highly variable. Blocking the larvae from molting is likely to be neem's most important quality. Eventually, this larvicidal activity will be used to kill off many pest species. INSECTS AFFECTED By 1990, researchers had shown that neem extracts could influence almost 200 insect species. These included many that are resistant to, or inherently difficult to control with, conventional pesticides: sweet potato whitefly, green peach aphid, western floral thrips, diamondback moth, and several leafminers, for instance. In general, it can be said that neem products are medium- to broad-spectrum pesticides of plant-eating (phytophagous) insects. They affect members of most, if not all, orders of insects, including those discussed below. Orthoptera In Orthoptera (such as grasshoppers, crickets, locusts), the antifeedant effect seems especially important. A number of species refuse to feed on neem-treated plants for several days, sometimes several weeks. Recently, a new effect, which converts the desert locust from the gregarious swarming form into its nonmarauding solitary form, has been discovered. 1   Chitin is the material comprising the insect's exoskeleton. Stopping the formation of a new "skin" for the next stage in its development is one way that azadirachtin acts to regulate the growth of an insect.

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As a test of neem's ability to repel insects, entomologist Thyril Ladd dipped a glass rod into dilute neem extract and wrote the letters "N" and "M" on a soybean leaf. He then exposed the leaf to the Japanese beetle, a pest renowned for a voracious appetite for soybean leaves. As can be seen, the bulk of the leaf was stripped to its woody veins, but the insects succumbed to starvation rather than nibble on the ''N" or "M." (T. Ladd) Homoptera Aphids, leafhoppers, psyllids, whiteflies, scale insects, and other homopterous pests are sensitive to neem products to varying degrees. For instance, nymphs of leafhoppers and planthoppers show considerable antifeedant and growth-regulating effects. However, scale insects (especially soft scale), are little affected. Phloem feeders, such as aphids, are in general not good candidates for neem used systemically (see earlier). In some cases, the host plant may influence the degree of control; this seems to apply to some whiteflies, which are affected on some crops but not on others. Neem derivatives may also influence the ability of homopterous insects to carry and transmit certain viruses. It has been shown, for example, that low doses keep the green rice leafhopper from infecting rice fields with tungro virus. The cause is uncertain but seems to be only partly owing to neem killing the insects or modifying their feeding behavior. Thysanoptera Neem is very effective on thrips larvae, which occur in the soil. However, once the adult thrips and related pests have taken up residence on the plants themselves, they are less sensitive to neem extracts. Oily formulations have shown some success in exploratory trials (perhaps because the oil coated and suffocated these minute creatures).

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Insects Affected by Neem Products Neem is known to affect more than 200 species of insects. Here we present brief information on a sampling of them to show the range of effects and the range of species affected. Insect Effects Mediterranean fruit fly Oriental fruit fly Disrupts growth, toxic Arrests pupae development, retards growth, toxic to larvae Face fly Horn fly Retards growth, toxic Repels, retards growth, disrupts growth Whitefly Repels, retards growth, inhibits feeding Housefly Inhibits feeding, disrupts molting, repels Sorghum shoot fly Yellow-fever mosquito House mosquito Flea Inhibits feeding Kills larvae, disrupts molting Toxic to larvae Retards growth, repels, inhibits feeding, disrupts growth, eggs fail to hatch Head lice Kills, very sensitive to neem oil—traditional use in Asia Spotted cucumber beetle Mexican bean beetle Retards growth, inhibits feeding Retards growth, inhibits feeding, disrupts molting Colorado potato beetle Eggs fail to hatch, larvae fail to molt with azadirachtin levels as low as .3 ppm, inhibits feeding Flea beetle Inhibits feeding Khapra beetle Inhibits feeding, disrupts molting, toxic to larvae Confused flour beetle Japanese beetle  Red flour beetle American cockroach Inhibits feeding, toxic Reduces fecundity and molts, reduces number of fertile eggs Bean aphid Reduces fecundity, disrupts molting Rice gall midge Toxic

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Insect Effects Western thrips Retards growth Diamondback moth Strongly suppresses larvae and pupae, retards growth, inhibits feeding Webbing clothes moth Inhibits feeding, disrupts molting Gypsy moth Retards growth, inhibits feeding, disrupts growth Corn earworm Retards growth, inhibits feeding, disrupts molting Pink bollworm Retards growth, inhibits feeding Fall armyworm Retards growth, repels adults, inhibits feeding, disrupts molting, toxic to larvae Tobacco budworm Inhibits feeding Tobacco hornworm Inhibits feeding, disrupts growth, toxic Cabbage looper Inhibits feeding Leafminer Retards growth, inhibits feeding, disrupts molting, toxic Serpentine leafminer High pupal mortality, retards growth, inhibits feeding, disrupts molting, toxic to larvae Brown planthopper Inhibits feeding, repellent, disrupts growth, mating failures and sterility Green leafhopper Inhibits feeding Migratory locust Stops feeding, converts gregarious nymphs into solitary forms, reduces fitness, adults cannot fly House cricket Disrupts molting Large milkweed bug Toxic, disrupts growth Mealy bugs Repels, inhibits feeding Milkweed bug Difficulty in escaping the "skin" of the last molt, disrupts molting Fire ant Inhibits feeding, disrupts growth Boll weevil Inhibits feeding Cowpea weevil Inhibits feeding, toxic Rice weevil Inhibits feeding, disrupts growth, toxic

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Coleoptera The larvae of all kinds of beetles—especially those of phytophagous coccinellids (Mexican bean beetle and cucumber beetle, for example) and chrysomelids (Colorado potato beetle and others)—are also sensitive to neem products. They refuse to feed on neem-treated plants, they grow slowly, and some (such as the soft-skinned larvae of the Colorado potato beetle) are killed on contact Lepidoptera From numerous field trials (notably on various moths), it appears that larvae of most lepidopterous pests are highly sensitive to neem. Indeed, it seems likely that armyworms, fruit borers, corn borers, and related pests will become the main targets of neem products in the near future. Neem blocks them from feeding, although this effect is usually less important than the disruption of growth it causes. Diptera Many species of dipterous insects—fruit fly, face fly, botfly, horn fly, and housefly, for example—are targets for neem products. Mosquitoes, too, are a possibility. Hymenoptera The freely feeding and caterpillar-like larvae of sawflies are target insects as well. In this group, neem's antifeedant and growth regulatory effects are both important. Heteroptera The "true" bugs—including many pests such as the rice bug, the green vegetable bug, and the East African coffee bug that suck juices from crops and trees—are affected by neem products. Neem's systemic qualities affect their feeding behavior and disrupt their growth and development. EXAMPLES As discussed, neem's effects vary with different insects. Some effects on a small selection of major pests are summarized below.

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Desert Locust Recent laboratory research has shown that neem oil causes "solitarization" of gregarious locust nymphs.2 After exposure to doses equal to a mere 2.5 liters per hectare, the juveniles fail to form the massive, moving, marauding plagues that are so destructive of crops and trees. Although alive, they became solitary, lethargic, almost motionless, and thus extremely susceptible to predators such as birds. Neem affects grasshopper nymphs similarly. This discovery differs from earlier ones on locusts. Those first approaches used alcoholic extracts and were aimed at disrupting metamorphosis or at stopping adult locusts from feeding on crops. The new approach uses neem oil enriched with azadirachtin to prevent locusts from developing into their migratory swarms. It apparently blocks the formation of the hormones and the pheromones needed to maintain the yellow-and-black gregarious form, which plagues arid Africa and the Middle East. In an interesting aside, it has been shown that neem oil destroys their antennae, even when applied to the abdomen. Neem trees grow well throughout the locust zones of Africa and the Middle East, and thus, in principle at least, the means to control the plagues could be locally produced. Cockroach Neem kills young cockroaches and inhibits the adults from laying eggs. Baits impregnated with a commercial preparation of neem-seed extract proved to retard the growth of oriental, brown-banded, and German cockroaches.3 First-instar nymphs of all three species failed to develop, and all died within 10 weeks. Last-instar nymphs exhibited retarded growth, and half of them died within 9 weeks. After 24 weeks, only 2 out of the 10 surviving German-cockroach nymphs had reached adulthood. In a "taste test," American cockroach adults preferred neem-treated pellets over untreated ones, but neem-treated milk cartons repelled them.4 Brown Planthopper Neem cake (the residue left after oil has been removed from the kernel) has proved so successful that Philippine farmers are already 2   Schmutterer and Freres, 1990. 3   The baits were lab-chow pellets laced with Margosan-O at 0.5 ml per pellet. 4   Adler and Uebel, 1985.

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using it on a trial basis against the brown planthopper (and other rice pests).5 Neem oil is being employed as well. Five applications of a 25 percent neem-oil emulsion sprayed with an ultra-low-volume applicator is said to protect rice crops against this increasingly severe scourge. It has been estimated that one neem tree provides enough ingredients to protect a hectare of rice. This use alone exemplifies the economic importance of further developing the neem tree for pest control.6 Stored-Product Insects Neem shows considerable potential for controlling pests of stored products. This is one of the oldest uses in Asia, and the literature contains many references to its benefits. In the traditional practice, neem leaves are mixed with grain kept in storage for 3-6 months. The ingredients responsible for keeping out the stored-grain pests are not yet identified—but they work well. In this connection, repellency seems of primary importance. For instance, treating jute sacks with neem oil or neem extracts prevents pests—in particular, weevils (Sitophilus species) and flour beetles (Tribolium species)—from penetrating for several months. For this use, the degradation problem caused by sunlight is less of a concern because the products are mostly away from the sunlight, inside jars or other containers. Neem oil is an extremely effective and cheap protection for stored beans, cowpeas, and other legumes. It keeps them free of bruchidbeetle infestations for at least 6 months, regardless of whether the beans were infested before treatment or not.7 This process may be unsuited for use in large-scale food stores, but it is potentially valuable for household use and for protecting seeds being held for planting. The treatment in no way inhibits the capacity of the seeds to germinate. Neem has also been used in India to protect stored roots as well as tubers against the potato moth. Small amounts of neem powder are said to extend the storage life of potatoes 3 months. Armyworm Azadirachtin has proved an effective prophylactic against armyworms at extremely low concentrations—a mere 10 mg per hectare.8 5   Saxena et al., 1984; von der Heyde et al., 1984. 6   Information from R.C. Saxena. 7   The amount of oil used was 2-3 ml per kg of beans. Neem oil shows a strong ovicidal effect in bean-seed beetles (bruchids), but its sterilizing and other influences may also be important in controlling these pests, which constitute a major problem when storing beans of many types (Zehrer, 1984). 8   Information from J. Klocke.

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Left row: untreated white cabbage, badly damaged by diamondback moth (and aphids). Right row: cabbage treated with aqueous neem-seed-kernel extract is largely undamaged. On the diamondback moth, neem exerts a combination of effects: it repels, it deters oviposition (eggs that are laid never hatch), and it disrupts molting. This extremely serious pest is found worldwide and in some locations is playing havoc with vital crops of leafy vegetables such as cabbage. (H. Schmutterer)

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For instance, it inhibits the fall armyworm, one of the most devastating pests of food crops in the western hemisphere. It has, however, been found necessary to treat the crop before the insects arrive. If this is done, they "march right on past the fields," but once they have taken up residence, it is harder to get them to move on. Colorado Potato Beetle In advanced trials in the United States, neem extracts have controlled the Colorado potato beetle.9 This is a significant pest in North America and Europe that is becoming increasingly resistant to broad-spectrum insecticides. In experiments in Virginia, for example, neem-seed extracts (at relatively low concentrations of 0.4 percent, 0.8 percent, and 1.2 percent) were tested in potato fields both with and without the synergist piperonyl butoxide (PBO). All treatments significantly lowered the potato beetle populations and raised potato yields; however, the extracts containing PBO were the most effective. The sprayings were most effective when the larvae were young, and were best when conducted as soon as the eggs hatched.10 Leafminers When birch trees were sprayed to control the birch leafminer (Fenusa pusilla), neem extract seemed to perform as well as the registered commercial pesticide Diazinon®. It was, however, slower acting, and the insects continued to damage trees before they died. This leafminer is a serious pest in parts of North America, often browning the crowns of entire forests. The U.S. Environmental Protection Agency has approved a neemseed-extract formulation for use on leafminers. This commercial product, now available almost nationwide, is expected to be especially useful against those leafminers that attack horticultural crops. Added to the soil, neem compounds enter the roots and move up into the crop's leaves so that leafminers munching on the leaves get their molting-hormone jammed, and they end up fatally trapped inside their own juvenile skins. European Corn Borer The European corn borer, a highly adaptable pest of corn and other crops, was introduced to North America in 1917 and subsequently 9   The statements here are based largely on research at Virginia Polytechnic Institute and State University, but generally similar results have been found in various parts of the United States and Canada. 10   Lange and Feuerhake, 1984.

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slashed Canada's corn yields in half. Today, it infests 40 million acres of corn in the United States each year, and in just an average year American farmers spend an estimated $400 million on chemicals to fight it. Laboratory tests using neem products on this corn borer larvae produced 100 percent mortality at 10 ppm azadirachtin; 90 percent mortality at I ppm. Lower concentrations (0.1 ppm azadirachtin) left the larvae apparently unaffected, but the adults that later emerged had grossly altered sex ratios (there were many more males than females) and the few remaining females laid fewer eggs and laid them too late. This combination of effects suggests that azadirachtin could be effective for controlling this terrible pest.11 Mosquitoes The larvae of a number of mosquito species (including Aedes and Anopheles) are sensitive to neem. They stop feeding and die within 24 hours after treatment. If neem derivatives are used alone, relatively high concentrations are required to obtain high mortality.12 Nonetheless, the use of simple and cheap neem products seems promising for treating pools and ponds in the towns and villages of developing countries. In one test, crushed neem seeds thrown into pools proved nearly as effective at preventing mosquito breeding as methoprene, a rather expensive pesticide that is usually imported in developing countries. Aphids In the Dominican Republic, water extracts of neem seed proved effective against Aphis gossypii on cucumber and okra and against Lipaphis erysimi on cabbage.13 This was in direct-contact sprays. As noted earlier, neem extracts applied in a systemic manner (that is, within plants) usually have little effect on aphids. Apparently, this is because aphids feed only on the phloem tissues, where, for some unknown reason, neem materials accumulate least. Fruit Flies Fruit flies (including the notorious medfly) are among the most serious horticultural pests. They cause millions of dollars in damage to fruits, and their very presence in the tropics is keeping dozens of delicious fruits from becoming major items of international trade. But, at least in experiments, the medfly is proving susceptible to neem. This 11   Arnason et al., 1985. 12   This seems to be particularly true in the case of the yellow-fever mosquito, Aedes aegypti. 13   Information from H. Schmutterer.

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insect pupates underground, and in trials in Hawaii, spraying dilute neem solution under fruit trees resulted in 100 percent control.14 More important, the neem materials were compatible with the biological-control organisms (braconid wasps) used to control fruit flies. When neem was applied to soil at levels that completely inhibited the pest from emerging from pupation, the parasites developing in these pupae emerged and exhibited normal life spans and reproductive rates. Thus, neem is compatible with biological control of fruit flies. Diazinon ®, the current soil treatment for fruit flies, kills not only fruit flies but their internal parasites as well.15 Gypsy Moth The U.S. Environmental Protection Agency has approved a neemseed-extract formulation for use on gypsy moth, a pest that is ravaging forests in parts of North America. In laboratory trials, a commercial neem formulation (Margosan-O®) produced 100 percent kill at very low concentrations (0.2 liters per hectare). After 25 days, the larvae were shrivelled, had stopped eating, and were dying. Field tests are in progress. Horn Flies Ground-up neem seed and stabilized neem extracts can prevent horn flies from breeding in cattle manure. In recent U.S. Department of Agriculture trials in Kerrville, Texas, cattle were fed a diet containing these neem materials in the feed. The animals readily consumed feed containing 0.1-1 percent ground neem seed. The neem compounds passed through the digestive tract and into the manure where they kept the fly larvae from developing.16 Blowflies In Australia neem products have been tested against blowflies on sheep. The larvae of these pests penetrate and burrow under the skin of sheep. They are a major economic burden to Australia's farmers because many of the sheep die. In the tests, azadirachtin kept blowflies from "striking" (that is, laying their eggs on sheep).17 As a result of the excitement this discovery engendered, 1,000 hectares of neem have been planted in Queensland at a cost of more than $4 million. At least one Australian company has been established to produce and distribute neem products to sheep farmers. 14   Information from J.D. Stark. The neem formulation (Margosan-O¬) proved less effective than Diazinon® but at low levels (10 ppm azadirachtin in the soil) provided excellent control for the flies. 15   Information from J.D. Stark. 16   Information from J.A. Miller. 17   Information from M.J. Rice.