Natural Resistance of Plants to Pests - American Chemical Society

18 The Neem Tree: Natural Resistance Par Excellence

Downloaded by UNIV OF CALIFORNIA SANTA BARBARA on October 8, 2015 | http://pubs.acs.org Publication Date: January 16, 1986 | doi: 10.1021/bk-1986-0296.ch018

Martin Jacobson Insect Chemical Ecology Laboratory, USDA, Agricultural Reseach Service, Beltsville, M D 20705

Neem (Azadirachta indica A. Juss.), a subtropical tree, is highly resistant to attack by numerous species of insects and nematodes. The tetranortriter-penoids meliantriol, salannin, and azadirachtin, occurring mainly in the seeds, act as antifeedants, disruptants of insect growth and development, or toxicants. Azadirachtin i s effective at dosages as low as 0.1 ppm. Although azadirachtin's complex structure probably precludes i t s ready synthesis, liquid or dust formulations of ethanol extracts of the seeds have been shown to be nontoxic to warm-blooded animals and nonmutagenic, making them suitable for practical use as pesticides. Registration of a neem formulation for use in the United States on nonfood crops by the Environmental Protection Agency is pending. Neem, Azadirachta indica A. Juss. (family Meliaceae), also known commonly as "nim" or "margosa," i s a subtropical tree native to the a r i d areas of India, Pakistan, S r i Lanka, Malaya, Indonesia, Thailand, Burma, and East A f r i c a . It i s under c u l t i v a t i o n i n plantations of West A f r i c a and the Caribbean i s l a n d s , as well as parts of Central and South America. Two neem trees brought from India approximately 40 years ago are t h r i v i n g i n the Miami, Florida area of the United States and a nunber of the young trees c u l t i v a t e d from seed are doing well i n Puerto Rico (_1). When f u l l y grown the tree can reach a height of 60 feet with a trunk diameter of 6 f e e t . It i s estimated that approximately 14 m i l l i o n neem trees are under c u l t i v a t i o n or grow wild i n India alone ( 2 J . The durable wood i s used for b u i l d i n g furniture and sometimes as firewood i n the developing countries, the leaves and twigs are spread among household goods and clothing to repel i n s e c t s , and the bark, which contains 12-14% tannins, i s used for the production of i n d u s t r i a l chemicals (_3, _4). The pulp of the nonedible yellow f r u i t s i s a promising substrate for generating methane gas. P o t e n t i a l l y the most valuable part of the neem tree 1s the seed, which contains up to 40% o i l that i s used i n the developing countries This chapter not subject to U.S. copyright. Published 1986, American Chemical Society

In Natural Resistance of Plants to Pests; Green, M., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1986.


18. JACOBSON

221

The Neem Tree

as fuel for lamps, as a lubricant for machinery, and i n the prepara t i o n of soaps, toothpaste, cosmetics, pharmaceuticals, d i s i n f e c t a n t s , and i n s e c t i c i d e s . Neem cake (the residue remaining a f t e r extraction of the o i l from the seeds) i s an excellent f e r t i l i z e r several times richer i n plant nutrients than manure (5). The tree has long been known to be free of attack by practicalTy a l l species of i n s e c t s , nematodes, and plant diseases, and i t thrives i n areas under c l i m a t i c conditions that are unsuitable for a l l but the most hardy species. A considerable amount of s c i e n t i f i c l i t e r a t u r e e x i s t s on the use of neem as an insect control agent. Of the various tree parts, the seeds are by far the most e f f e c t i v e (for comprehensive reviews of the p e s t i c i d a l properties of neem, see references £ and _7). Chemistry A host of tetranortriterpenoids have been i s o l a t e d from various parts of the neem tree and, although a l l have not been tested for p e s t i c i d a l properties, three compounds obtained from the seed are quite active as insect feeding deterrents, t o x i c a n t s , and(or) disruptants of growth and development against a large variety of insect species and nematodes (6). These s p e c i f i c compounds are m e l i a n t r i o l (I), f i r s t i s o l a t e d i n 1967 by La vie et a l . (_8), salannin (III) (_9), and azadirachtin (III) (10, 11). The highly complicated structure of azadirachtin was io'FntTFied by Zanno (12) and Nakanishi (13). Subsequently, a large series of t e t r a n o r t r i terpenoids and pentanortriterpenoids were i s o l a t e d from the seed o i l by Kraus et a l . (14-18), Lucke et a l . Q £ ) . Garg and Bhakuni (20), and Kubo et al .~~[2TJ~. Other components i s o l a t e d from neem are b e t a - s i t o s t e r o l (2277 f a t t y acids (23), and flavanoids (24). Neem seed o i l possesses an unpleasant, g a r l i c k y - t y p e odor, undoubtedly due to a number of sulfur compounds present. ι

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222

NATURAL RESISTANCE OF PLANTS TO PESTS

Compounds I and II have been obtained i n discrete c r y s t a l l i n e form but azadirachtin has thus f a r been obtained only as a white amorphous powder melting at 154-158°C, despite several attempts to prepare c r y s t a l l i n e derivatives (mainly e s t e r s ) . This i s probably due to the presence of d i f f e r e n t stereoisomers, as Rembold et a l . (25) recently reported the separation of azadirachtin into at least 4 amorphous stereoisomers (azadirachtins A, B, C, and D) with s i m i l a r b i o l o g i c a l a c t i v i t i e s . Of these three compounds, azadiracht i n i s by f a r most active as a feeding deterrent for i n s e c t s ; i t i s e f f e c t i v e against several species at a concentration of 0.1 ppm or less (_1). However, Rembold et a l . (25) have very recently reported the separation of azadirachtin into at least 4 amorphous s t e r e o i somers (azadirachtins A, B, C, and D) with s i m i l a r b i o l o g i c a l a c t i v i t i e s . Morgan (26) has shown that the y i e l d of azadirachtin extracted from 100 grams of neem seed varies markedly according to the o r i g i n of the seed, ranging from 0.2 g using commercial Indian seed (27, 28) t o 3.5 g using seed from Ghana. However, Ermel et a l . , using T ï ï i n T a y e r chromatography on ethanol extracts of seed, found that the best y i e l d s of azadirachtin were obtained from seeds o r i g i n a t i n g i n Togo (6.2 g/100 g) and India (3.5 g/100 g) (29). The procedure used by our Laboratory at the U.S. Department of l i g r i c u l ture to determine the azadirachtin content i n Indian neem extract and formulations showed (Table I) that 95% ethanol i s the preferred solvent f o r crude extraction of the active components (28). However, Feuerhake (30) reported that methanol with or without meThyl-tertbutyl ether was the most e f f i c i e n t extraction solvent i n his hands. Exposure of azadirachtin to sunlight causes a rapid decrease i n antifeeding potency, which i s prevented to some extent (25%) by mixing with neem, a n g e l i c a , c a s t o r , or calamus o i l (31 ). Table I. Azadirachtin determined by high-performance l i q u i d chromatography (HPLC) i n neem kernel extracts prepared with various solvents. Solvent used Ethanol (55%) Methanol-HoO (85:15) Methanol Methylene chloride Ethyl ether Acetone

Azadirachtin found (Ag/lQaL) 0 0 2.60 2.19 1.73 1.28 0.74

Pesticidal Activity Neem extracts are highly e f f e c t i v e not only i n preventing or reducing feeding by a variety of insects but also as a r e p e l l e n t , i n h i b i t o r of growth and development, and s t e r i l a n t . A comprehensive review published by Warthen (6) i n 1979 l i s t s 20 species of the order Coleoptera ( b e e t l e s ) , 4"~species of the order Diptera ( f l i e s ) , 5 species of the order Heteroptera (true bugs), 10 species of the order Homoptera (aphids and scale i n s e c t s ) , 2 species of the order Isoptera (termites), 30 species of the order Lepidoptera (moths and b u t t e r f l i e s ) , and 7 species of the order Orthoptera ( l o c u s t s , grass-



18.

JACOBSON

The Neem Tree

223

hoppers, c r i c k e t s ) affected by neem preparations as feeding i n h i b i tors or growth regulators through the year 1978. Also included were 5 species of nematodes and a species of mite (Acari) whose development i s disrupted by neem. Table II l i s t s those species evaluated for feeding i n h i b i t i o n (FI), growth and development regulation (GR), and t o x i c i t y (T) with neem since 1978. Included are 2 species of mites, 25 species of Coleoptera, 10 species of Diptera, 3 species of Heteroptera, 6 species of Homoptera, 1 species of Hymenoptera, 25 species of Lepidoptera, and 9 species of Orthoptera. The t o t a l number of insect species known to be adversely affected by neem preparations i s presently 123, i n addition to 3 species of mites and 5 species of nematodes. There i s every reason to believe that these nunbers w i l l increase r a p i d l y , judging by the large nunber of s c i e n t i s t s now involved i n neem research. Pharmacological A c t i v i t y Malaria-infected mice fed d a i l y oral doses of an ethanol extract of neem leaves f a i l e d to recover and died from the disease after the f i f t h day (119). The extract caused an appreciable contraction of guinea pig ileum, and intravenous i n j e c t i o n i n the dog resulted i n an i n i t i a l r i s e i n blood pressure followed shortly by a protracted f a l l ; the effect was s i m i l a r to that of histamine (120). A methanol extract of the combined leaves and bark of neem had a pronounced anti -inflammatory effect on rat paw and an a n t i p y r e t i c effect i n rabbits (121). Injection of an aqueous extract of the leaves into guinea pigs and rabbits profoundly reduced blood pressure and reduced the heart rate (122). A n t i - u l c e r studies conducted with laboratory rats using n i n b i d i n , the major b i t t e r p r i n c i p l e of neem seed o i l , showed s i g n i f i c a n t a n t i - u l c e r potential when fed at doses of 20-40 mg/kg. The compound also afforded remarkable protection from duodenal lesions (123). Neem o i l possesses strong i n v i t r o spermicidal action (within 30 sec) against rhesus monkey and human spermatozoa. When used i n t r a v a g i n a l l y at 20 L i n rats and at 1 mL i n monkeys and i n human subjects the o i l was completely e f f e c t i v e i n preventing pregnancy without causing side effects (124). The sodium s a l t of ninbidin also acts as a spermicide (125). Single or multiple i n t r a vaginal a p p l i c a t i o n of neem o i l during the post-implantation period prevented pregnancy i n r a t s , but normal f e r t i l i t y was restored a f t e r 30 days of withdrawal (126). Toxicological A c t i v i t y Birds eat the neem f r u i t i n large quantity with impunity but s p i t out the seed, which has a strongly b i t t e r t a s t e (2). An ethanol extract of the seed i n s t i l l e d into the rabbit eye caused no i r r i t a t i o n and no s i g n i f i c a n t s k i n - s e n s i t i z i n g reaction resulted from i n j e c t i o n into the shaved skin of a guinea p i g . The standard Ames test with azadirachtin showed no mutagenic a c t i v i t y on four s t r a i n s of Salmonella typhimurium (127). The acute oral t o x i c i t y of the extract i n mice was extremely low (13 g/kg) (121). Incorporation of neem seed cake (ethanol-extracted and unextracted) into the ration of lanbs at 10% caused no change i n the growth r a t e ,



Euproctis fraterna Moore Henosepilachna e l a ' t e r i i Rossi Leptinotarsa decemlineata (Say) Nephantis serinopa Meyr."" Phyllotreta s t r i o f a t a (Fabricius) Podagrica~jostedti Jacoby Podagri ca" uni forma "Jacoby P o p i I l i a japonica Newman

COLEOPTERA Acalymma vittatum (Fabricius) Callosobruchus chinensis Li nnaeus Callosobruchus maculatus (Fabricius) Chi rida bipunctata F a b r i c i u s Diabrotica undeci¥punctata howardi Barber Diacrysia obliqua walker Dicladispa armigera 01 i v . E piil a ch na ch ry somel 1 na (Fabricius) Epilachna punctata Mulsant Epilachna" v a r i v e s t i s Mulsant

ACARI Tetranychus cinnabarlnus (Bolsd.) Tetranychus urticae Koch.

S c i e n t i f i c name

s t r i p e-d - f l-e a- beetle flea beetle flea beetle Japanese beetle

spotted cucunber beetle Colorado potato beetle

12-spotted ladybird beetle Mexican bean beetle

striped cucunber beetle pulse beetle cowpea weevil t o r t o i s e beetle spotted cucunber beetle jute hairy c a t e r p i l l a r r i c e hi spa

carmi ne spider mite 2-spotted spider mite

Common name

t

F I , GR FI FI FI FI GR FI

FI T, FI FI FI FI FI FI FI F I , GR Τ F I , GR

F I , GR F I , GR

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growth regulation (GR),

adult adult l a r v a , adult adult adult larva adult larva adult larva adult larva larva l a r v a , adult larva adult adult adult l a r v a , nymph adult

adult adult

Stage

Table II. Arthropods and nematodes evaluated with neem for feeding i n h i b i t i o n ( F I ) and t o x i c i t y (T) (1979-1984).



HETEROPTERA DysdercuT cingulatus Fabri ci us Dysdercus" koenigii Tab r i ci us Uncopeltus f a s c i a t u s (Dallas)

Musca autumnal i s de Geer Urseolia oryzae (Wood-Mason)

red cotton bug large milkweed bug

face f l y r i c e g a l l midge

yellowfever mosquito sorghum shoot f l y Mediterranean f r u i t f l y northern house mosquito fruit fly oriental f r u i t fly vegetable leafminer l e a f miner egg, a adult pupa adult

adult

nymph l a r v a , egg adult nymph

larva adult larva, larva larva adult larva, larva, larva, larva, adult

adult l a r v a , adult

confused f lour beetle khapra beetle

Tribolium confusum Jacqueline du Val Trogodermâ granarfum Everts

DIPTERA Aedes aegypti (Linnaeus) Atherigona soccata Rondani C e r a t i t i s capitata (Wiedemann) Culex pTpiens Linnaeus Dacus c T l i a t u s Lw. Da eus dorsal i s Hendel Liriomyza sativae Blanchard Liriomyza t r i f o l i i (Burgess)

adult adult adult adult adult

Stage

lesser grain borer granary weevil r i c e weevil mai ze weevi 1 red f l o u r beetle

Common name

Rhyzopertha dominica (Fabricius) Si top ni 1 us"~gra na r i us (Linnaeus) S i t o p h i l u s oryzae (Linnaeus) Si tophi 1uT zeamais Motschulsky Tribolium castaneum (Herbst)


GR, Τ GR, Τ Τ GR

GR FI GR, Τ Τ (-) FI Τ F I , T, GR F I , GR FI, Τ T, GR Τ

F I , GR, Τ

FI, Τ

FI FI F I , GR, Τ FI

Activity


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honey bee

Mediterranean f l o u r moth almond moth r i c e leaf folder cabbage webworm codli ng moth j u t e hairy c a t e r p i l l a r melonworm spiny b o l l worm cotton bollworm tobacco budworm corn earworm, bollworm gypsy moth cabbage armyworm

LEPIDOPTERA Anagasta kuhniella ( Z e l l e r ) Cadra c a u t e l l a (Walker) Cnaphalocrocis medinalis (Guenee)

Croci dolomia bi notai i s Zel 1 er Cydia pomonella (Linnaeus) D i a c r i s i a obliqua Walker Diaphania hyallnata (Linnaeus) Earias insulana (Boi sduval ) H e l i o t h l s armigera (Hubner) Heliothis" virescens (Fabrlcius) H e l i o t h l s zea (Boddie) Lymantria" dlspar (Linnaeus) Mamestra brassicae Linnaeus

whitebacked planthopper

aphid bean aphid sweetpotato w h i t e f l y green leafhopper brown planthopper

Common name

HYMENOPTERA Apis melfifera Linnaeus

Sogatella f u r c i f e r a (Horvath)

HOMOPTERA Acyrthosiphon pi sum Harr. Aphis fabae Scopoli Bemi silTtaFacI (Gennadi us) Nephotettix yirescens (Distant) Ni la par va"tâ* lu gens ( S t a l . )


Table II—Continued

larva l a r v a , pupa larva adult larva larva larva larva larva l a r v a , adult larva larva larva larva

larva adult

nymph nymph nymph, adult adult l a r v a , nymph, adult adult

Stage

FI, GR, FI GR FI, GR, FI FI, FI FI, FI FI FI FI

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GR, Τ Τ

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NEMATODA

Phaulacridium spp. Schistocerca gregaria Forsk

ΊΓΓΤΤΤ

root-knot nematode

wingless grasshopper desert locust

plague locust walkingstick Carolina grasshopper f i e l d cricket mi gratory locust

(-)

FI

(-) FI FI

adult adult adult

GR FI (-) FI FI FI FI GR GR, Τ

cabbage looper

Trichoplusia ni (Hubner)

GR, Τ

Τ Τ

GR, Τ

F I , GR F I , GR repellent FI

FI, GR FI FI FI FI, FI, FI FI,

Acti v i t y

nymph, adult larva adult adult adult adult larva adult

Egyptian cotton leafworm tobacco c a t e r p i l l a r

Spodoptera l i t t o r a l i s (Boisduval) Spodoptera" l i t u r a (Fâb r i ci u s )

house c r i cket

larva larva adult larva

pink bollworm potato tuberworm diamondback moth Anjoumois grain moth nutgrass armyworm f a l l armyworm

0RTH0PTERA Acheta domesticus (Linnaeus) Amsacta moorei "Butler Choriocetes termi ni fera (Walker) Diapheroméra"Témorata (Sav) Dissosteira Carolina ( Li n na eu s ) Gryllus pennsyl vani eus Burmeister Locusta rmgratona mi gratori oides

larva larva larva larva larva larva adult larva larva

Stage

tobacco hornworm r i c e earcutting c a t e r p i l l a r

Common name

Manduca sexta (Linnaeus) Mythimna separata (Walker) P a p i l i o demodocus Esper Pectinophora gossypiella (Saunders) Phthorimaea o p e r c u l e l l a (Zel 1 er) P|uteTla~xy1ostella (Linnaeus) Sitôt r o g a c e r e a l e l l a ( O l i v i e r ) Spodoptera exemptaTWa l ker ) Spodoptera" frugiperda ( J . E. Smith)



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228


20% increased the growth r a t e , and 30% s i g n i f i c a n t l y reduced the growth r a t e . Blood glucose, hemoglobin content, and urea nitrogen remained normal at a l l dosages (128). Neemrich 100, a formulation containing 30% neem o i l , applied dermally to albino rats at d a i l y dose l e v e l s of 200, 400, and 600 mg/kg for 3 weeks, caused no overt signs of t o x i c i t y or abnormal behavior. Treated rats exhibited higher food consumption, gained weight, and showed no abnormal blood l e v e l s (129). Albino rats and mice showed no t o x i c i t y when fed ninbidin up to 2000 mg/kg or when administered i n t r a p e r i t o n e a l ^ at 1000 mg/kg. Dogs fed ninbidin d a i l y at 10 and 20 mg/kg for 4 weeks showed no systemic t o x i c i t y (130). Malaysian infants given large (up to 5 mL) oral doses of neem o i l for minor ailments showed vomiting, drowsiness, metabolic a c i d o s i s , polymorpho-nuclear l e u c o c y t o s i s , and encephalopathy within hours of ingestion (131). Potential for Practical Use as a Pesticide Homemade formulations of neem seeds have been used e f f e c t i v e l y by farmers i n the developing countries for many years for con t r o l l i n g a g r i c u l t u r a l pests of tobacco and cotton (3,7). Although the compexity of the azadirachtin molecule probably precludes i t s ready synthesis, both crude and p a r t i a l l y p u r i f i e d extracts of the seeds can be used for pest c o n t r o l . Improved methods for I s o l a t i n g highly active fractions have been developed, a neem p i l o t plant i s presently i n operation i n Burma (132), and the c u l t i v a t i o n and processing of neem on a large scale are being sponsored 1n various parts of the world by the German Agency for Technical Cooperation, the U.S. Agency for International Development, and several a g r i c u l tural agencies (JU £ , 5, 133, 134). The f i r s t hurdle toward the commercial development and marketing of neem formulations for c o n t r o l l i n g a g r i c u l t u r a l pests i n the United States i s being overcome by a private concern which i s to be granted r e g i s t r a t i o n by the Environmental Protection Agency (EPA) for use on nonfood crops (135). Since a large volume of t o x i c o l o g i c a l test data has been supplied to EPA showing that the formulations are nontoxic to man and animals, r e g i s t r a t i o n may be granted for use on food crops as w e l l .

Literature Cited 1. Jacobson, M. Proc. 1st Intern. Neem Conf., 1981, pp. 33-42. 2. Saxena, R. C., personal communication. 3. Radwanski, S. World Crops Livestock 1977, 29, 111-113. 4. "Firewood Crops. Shrub and Tree Species for Energy Production," National Academy of Sciences, 1980, p. 114. 5. Michel-Kim, H.; Brandt, A. Proc. 1st Intern. Neem Conf. 1981, pp. 279-290. 6. Warthen, J. D., Jr. USDA Sci. Educ. Admin., Agric. Revs. Manuals ARM-NE-4, 1979, 22 pp. 7. Jain, H. K. Indian Agric. Res. Inst. Bull. No. 40, 1983, 63 pp. 8. Lavie, D.; Jain, M. K.; Shpan-Gabrielith, S. R. Chem. Commun. 1967, 910. 9. Henderson, R.; McCrindle, R.; Overton, Κ. H. Tetrahedron Lett. 1964, 3969-3974. 10. Butterworth, J . H.; Morgan, E. D. Chem. Commun. 1968, 23-24. In Natural Resistance of Plants to Pests; Green, M., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1986.


18. JACOBSON

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Natural Resistance of Plants to Pests - American Chemical Society

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