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6 Effects on Other Organisms Although neem's effects on pestiferous insects are by far the best known, the tree's various products can influence other pest organisms as well. In the long run, these may well prove the most important of all. At present, however, the effects on noninsect pests are poorly understood. This chapter highlights some of the findings to date. NEMATODES Neem products affect various types of nematodes. This may be significant because certain of these thread worms are among the most devastating agricultural pests and are also among the most difficult to control. In addition, an increasing number of synthetic nematocides have had to be withdrawn from the market for toxicological reasons. Today, there is a small but increasing body of evidence that neem might provide useful replacements. Certain limonoid fractions extracted from neem kernels are proving active against root-knot nematodes, the type most devastating to plants. They inhibit the larvae from emerging and the eggs from hatching, and in at least one test they have done so at concentrations in the parts-per-million range.1 Water extracts of neem cake (the residue remaining after the oil has been pressed out of the seeds) are also nematocidal. In a careful trial in Aligarh, India, amending soil with sawdust and neem cake dropped the root-knot index to zero and, of all the treatments tested, gave the greatest growth of tomatoes, a crop that is very sensitive to these nematodes. In tests in a greenhouse and in the field in Germany, tomato plants were obviously improved by neem products, but there was no significant difference in the numbers of some nematode species in the soil. However, among treated and untreated soils the majority was extracted from the roots of plants in untreated soil.2 1 Devakumar et al., 1985. 2 Rössner and Zebitz, 1987a.
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Cardamom growers in South India are already using neem cake to control nematodes. Of 19 growers interviewed recently, 17 said that nothing works as well. These were sophisticated farmers who monitor world cardamom prices regularly and use synthetic chemicals for controlling other pests in their fields. In other words, they weren't using neem out of ignorance or poverty. They incorporate 100-259 kg per hectare of neem cake in their cardamom fields every year. About 3,000 tons of neem cake are now used annually in India's Cardamom Hills. It is sold by pesticide dealers, who transport it from 250-300 km away. 3 SNAILS Various neem extracts kill snails. This appears to be beneficial in some cases. In laboratory tests, for example, ethanol extracts proved toxic to the aquatic snail (Biomphalaria glabrata), a species that is necessary to the life cycle of the parasite causing schistosomiasis (bilharzia). The extracts killed both the adult snail and its eggs.4 This raises the possibility that neem products may find a role in controlling schistosomiasis, a horrible scourge that infects some 200 million people in the tropics. In another test, an aqueous solution of neem fruit resulted in a 100-percent kill of Melania scabra.5 This snail, common throughout the Orient, is a vector of lung flukes, a parasitic flatworm that encysts in the lungs of livestock, wildlife, and people, causing debilitation and sometimes death. CRUSTACEANS Little is known about neem's effects—beneficial or detrimental—on crustaceans. However, in one intriguing set of experiments in the Philippines, it proved beneficial. In rice paddies, the ostracod Heterocypris luzonensis feeds on the blue-green algae that fix nitrogen from the air. This minute aquatic crustacean thereby reduces a source of fertilizer for the crop. Killing this tiny creature thus would indirectly boost the nitrogen available and probably increase rice yields.6 Aqueous neem-kernel extracts have killed it very effectively under laboratory conditions.7 3 Information from S. Ahmed. 4 Information from D. Heyneman. 5 Muley, 1978. 6 Ketkar and Ketkar, 1984. 7 Grant and Schmutterer, 1986.
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FUNGI Neem has demonstrated antifungal activity. Should this prove widely applicable, the availability of a natural fungicide that can be grown, extracted, and applied by farmers themselves could be of great consequence to worldwide agriculture and food supply. Fungi attack crops in countless numbers and forms. They are constantly evolving enemies of farms and forests. Many can reach epidemic proportions, a few have no cures, and some can make certain crops impossible to grow. And, despite the best of modern science, they still threaten wheat, corn, rice, and other plants that feed the world. Not a lot is known about neem's practical use against rots, smuts, wilts, mildews, die-backs, and other fungal plant diseases. However, several tests have indicated considerable promise. In one test, neem oil protected the seeds of chickpeas against the serious fungal diseases Rhizoctonia solani, Sclerotium rolfsii, and Sclerotinia sclerotiorum. It also slowed the growth of Fusarium oxysporum but did not kill it. In addition, neem cake incorporated into the soil completely blocked the development of the resting forms of R. solani—thereby interfering with the long-term survival of this devastating fungus.8 In another, neem-seed extracts showed beneficial effects against leaf fungi. Spraying crude neem oil on lilac bushes, when done before any sign of outbreak, prevented powdery mildew from breaking out for the rest of the season. This protectant also gave essentially 100 percent control on hydrangeas in greenhouses—better than Benlate ® (benomyl), the standard mildew treatment in much of the world.9 In the case of bean rust, neem extracts have given 90 percent control when applied before the plants were exposed to the fungus. However, they worked poorly once rust was established.10 In addition to affecting root-knot nematodes, treating soil with neem can reduce the populations of pest fungi in the rhizosphere that attack and feed off plant roots.11 Aflatoxin A truly unusual and potentially notable connection between neem and fungi has recently been reported from Louisiana.12 In trials there, neem-leaf extract failed to kill the fungus Aspergillus flavus, but, against all expectations, it completely stopped it from producing aflatoxin (see sidebar). 8 Singh et al., 1980. 9 Information from J. Locke. 10 Locke, 1990. 11 Singh et al., 1985. 12 Information in this section is from D. Bhatnagar. For more, see sidebar.
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The Cancer-Causing Fungus While growing up in Rajasthan, India, Deepak Bhatnagar was impressed with neem's qualities. He often saw his parents using the leaves to keep insects out of the wheat they stored in their home. He also saw how well these leaves worked against skin infections when they cured a persistent ulcer on his leg—one that had baffled the best of medical practitioners. Today, Bhatnagar works at the U.S. Department of Agriculture and has taken up the study of neem's effects on certain fungi. In tests in his laboratory in New Orleans, he ground up (or boiled) neem leaves in water (or in potassium phosphate-buffered solution to remove any possible pH effect) and applied the resulting solutions to Aspergillus flavus. This fungus, one of the most deadly on earth, grows on various foods and produces chemicals called aflatoxins that are highly carcinogenic. When Bhatnagar looked at the fungal cultures four days later, they seemed normal. But when he tested them chemically, he could find only 2 percent of the aflatoxin that the fungus normally would have produced. Neem had left the microbe alive, but had switched off its ability to produce aflatoxins. Bhatnagar then moved on to greenhouse studies. He injected neem solutions into cotton bolls, and later infected the bolls with the fungus. Again, aflatoxin production was inhibited (see diagram opposite). Experiments are now under way to determine which components in the neem leaves are responsible for the bioactivity. Once they are identified, cost-effective and efficient delivery systems can probably be developed to control aflatoxin synthesis by the fungus on various crops. Bhatnagar says that the results are ''promising but preliminary." But if his work proves that neem is safe and effective for aflatoxin control, it may open the door to a simple, inexpensive method for protecting stored foods using locally produced materials, even in the remotest rural villages. This is especially significant these days. With the availability of ever more sensitive chemical analyses, health officials are becoming alarmed at aflatoxin's widespread occurrence and potential hazard. Anything that might protect food supplies in tropical regions that can ill afford synthetic fungicides and have difficulty keeping foods fungus-free could be of immense significance.
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Neem-leaf extracts affect the fungus Aspergillus flavus in an unusual way. The fungus appears to grow normally, but it produces far less aflatoxin. This is important because aflatoxin is a powerful carcinogen that is of increasing concern in the world's food supplies. The levels shown here were measured in samples of the fungus grown on developing cottonseed. (D. Bhatnagar) Greenhouse studies have since confirmed these laboratory findings. The extracts appear to halt the formation of substances called polyketides, which the fungi convert into aflatoxin. The enzymes for the conversion remain in place, but key chemicals they need to synthesize the feared toxin are no longer available. It proved easy to take advantage of this in practice: neem leaves were mashed in water, the liquid separated, and it was applied without further refinement. This crude liquid extract turned off aflatoxin production in both laboratory cultures and cotton bolls on living plants. These findings could be of immense significance. Aflatoxin causes liver cancer, and under hot and humid conditions, where fungi thrive, it can form on peanuts, corn, cottonseed, and other widely eaten food crops. It is of great concern these days; it not only threatens health, it also promises economic catastrophe. For example, the United States may soon be banned from exporting cottonseed to feed Europe's cattle. The U.S. aflatoxin limit is 20 parts per billion (ppb), but Europe's goal for the future is a mere 2 ppb in feed and only 0.5 ppb in milk. Also, aflatoxin-contaminated local foods and feeds are causing increased concern in Asia and Africa.
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Neem Oil Fungicides So far, almost all studies on neem pesticides have employed limonoids extracted from the seed kernel. Neem oil has seldom been considered because its chemical makeup is not very different from that of common seed oils such as soybean or olive oil. However, U.S. Department of Agriculture researchers have recently found that, surprisingly, neem oil has its own valuable pesticidal properties. In particular, it is very successful against fungi that cause certain plant diseases. In both laboratory and field trials, neem oil has controlled the diseases known as rust and powdery mildew—and it did so without harming the plants. In the first of these trials, James Locke, a plant pathologist, emulsified neem oil in water, sprayed it over various types of ornamental plants in pots, and then subjected the plants to rust or powdery mildew. "We had success with emulsions containing as little as 0.25 percent oil," Locke says. "The oil was both insecticidal and fungicidal. We don't really know why, since it contains no azadirachtin, but it does work." In greenhouse trials, plant pathologist J. Rennie Stavely found that neem oil is nearly 100 percent effective against rust on beans. Although its effectiveness was slightly less dramatic on bean plants in the field, neem oil still reduced this serious fungal disease enough to be cost-effective. Hydrangea leaves exposed to powdery mildew. One (left) became badly infected with the fungus. The other, protected by a dilute solution of needseed oil in water, grew to full size and was almost unaffected. (J. Locke, Agricultural Research Service, USDA)
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PLANT VIRUSES Plant viruses pose some of the most severe threats to world agriculture. Because they invade the crop's cells and cloak themselves with the plant's normal life processes, they are far more difficult to control than free-living organisms such as bacteria, protozoa, or fungi. At present, we can only try to halt their spread—something nearly impossible to achieve under even the best of circumstances—because viruses "hitch rides" in insects such as aphids, as well as on dirty tools, blowing dust, or spreading floodwaters. A few virus-inhibiting chemicals are known for treating human and animal diseases (AZT for AIDS, for instance), but at present, none are available for treating plants. Neem might be the first. Crude extracts seem to bind certain plant viruses effectively, and so limit infection.13 However, for the moment at least, neem seems most effective at interfering with the transmission of plant viruses carried by insects. This conclusion is drawn from several successful tests of neem's effects against insect vectors of plant viruses. These tests include the following: A trial in the Philippines where rice fields sprayed with neem oil had significantly lower incidence of the ragged-stunt virus, which affects rice and is transmitted by the brown planthopper;14 A second trial in the Philippines where mixtures of neem oil and custard-apple oil interfered with the transmission of tungro virus, another rice pest;15 Experiments in India where neem-leaf extracts reduced the transmission of tobacco mosaic, a virus that seriously affects several vegetable crops;16 Field trials in the Philippines where fields treated with urea and neem cake were found to be lower in viral diseases than those treated with urea alone;17 and Enzyme-linked immunosorbent assays showing that rice seedlings grown in soil treated with neem cake were significantly freer of rice tungro viruses (transmitted by green rice leafhopper) than those in untreated control plots.18 On the other hand, not all trials have been this successful. In the United States, daily applications of neem leaf extracts over a month's time to turnip plants infected with cauliflower mosaic virus did not reduce viral infection.19 13 Singh, 1971; Tripathi and Tripathi, 1982. 14 Saxena et al.. 1981. 15 Mariappan and Saxena. 1984. For information on custard apples, see the companion report Lost Crops of the Incas. 16 Information from B.G. Joshi. 17 Saxena et al.. 1984. 18 Saxena et al.. 1987. 19 Information from D.W. Unander.
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NONTARGET SPECIES As has been mentioned, neem extracts proved to be "soft" on unintended targets. Further examples follow. Earthworms In greenhouse studies, when neem leaves and seed kernels were incorporated into potting soil containing earthworms (Eiseniafoetida), the number of young worms produced increased 25 percent.20 In field trials there were no differences in the number of worms, but the average weight of each worm was highest in neem-treated plots. Thus, it seems possible that neem products can favor earthworms, at least under certain conditions. Beneficial Insects Neem seems remarkably benign to spiders, butterflies, and insects such as bees that pollinate crops and trees, ladybugs that consume aphids, and wasps that act as parasites on various crop pests.21 In the main, this is because neem products must be ingested to be effective. Thus, insects that feed on plant tissues succumb, while those that feed on nectar or other insects rarely contact significant concentrations of neem products. All this is coming clearer from recent research. For example, only after repeated spraying of highly concentrated neem products onto plants in flower were worker bees at all affected. Under these extreme conditions, the workers carried contaminated pollen or nectar to the hives and fed it to the brood. Small hives then showed insect-growth-regulating effects; however, medium-sized and large bee populations were unaffected. 22 Under laboratory conditions the larvae of ladybugs and lacewings have shown some insect-growth-regulating effects from neem picked up from the bodies of other insects. However, in greenhouse trials in Florida, neem products proved essentially nontoxic to predators and parasitoids of the cotton aphid and the sweet potato whitefly. Neither the amount of predation nor of parasitism was notably reduced. 23 20 Rössner and Zebitz, 1987b. 21 Saxena, 1987. 22 Schmutterer and Holst, 1987. 23 Hoelmer et al., 1990.
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A census of natural aphid enemies collected from seven different field trials indicated that neem has no detrimental effects on either predators (coccinellids, chrysopids, syrphids) or parasitoids (ichneumonids, braconids). The aphids in the neem-treated plots were actually carrying more parasites than were those in either the control plots or the plots treated with the insecticide pyrethrum.24 24 Isman et al., in press.
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