2 The Progression of Resistance Mechanisms Developed
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against Insecticides A. W. A. B R O W N Department of Entomology, Michigan State University, East Lansing, Mich. 48824
As the f i n a l item i n the symposium on pesticide chemistry i n this century, the need was f e l t for a review of outstanding events i n the insecticide resistance field during t h i s period, along with a projection of expectations during its f i n a l 25 years. This paper, however, will describe progressions rather than events, since resistance has been a steadily developing problem; t h i s pro gression w i l l be described i n d e t a i l , although the Forward Look will be pretty sketchy. Starting i n 1908 i n the orchards of the Pacific northwest, the cases of resistance before World War II and the era of the synthetic organics involved the HCN used against scale insects on c i t r u s , the arsenicals used against orchard c a t e r p i l l a r s and cat tle t i c k s , and tartar emetic applied against the t i n y insect pests called t h r i p s ; as now, many instances originated i n C a l i f o r n i a (Table I ) . The resistance mechanisms were investigated i n two of Table I.
Development of Insecticide-Resistances,
San Jose Scale Black Scale California Red Scale C i t r i c o l a Scale Codling Moth Peach Twig Borer Cattle Tick Blue Tick Citrus Thrips Gladiolus Thrips Two-spotted Mite Walnut Husk Fly
Lime-sulfur HCN HCN HCN Pb Arsenate Pb Arsenate Na Arsenite Na Arsenite Tartar Emetic Tartar Emetic Selenium Cryolite
1908-44.
Wash. State California California California Colorado California Argentina S. Africa California California Eastern US California
08 '12 ! 13 1 25 ! 28 •44 •35 f 38 f 39 f 43 ! 43 f 43
!
the cases: — the arsenic-resistant codling-moth larvae were found to be more resistant to starvation and desiccation, and thus had a longer period of effective locomotion to find an unsprayed spot on the skin of the apple (1); the cyanide-resistant C a l i f o r n i a red 21
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
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22
PESTICIDE CHEMISTRY IN THE 20TH CENTURY
s c a l e had a t i s s u e - r e s p i r a t o r y e l e c t r o n - t r a n s p o r t s y s t e m l e s s de p e n d e n t on c y t o c h r o m e o x i d a s e ( 2 ) , and t h e c h a r a c t e r was f o u n d t o be i n h e r i t e d as i f i t was due t o a s i n g l e s e x - l i n k e d gene. The S w i s s p r o d u c t DDT was i n t r o d u c e d f o r h o u s e f l y c o n t r o l i n n e u t r a l c o u n t r i e s i n 1944, and a l r e a d y by 1946 r e s i s t a n c e had de v e l o p e d i n n o r t h e r n Sweden ( o f a l l u n l i k e l y p l a c e s ) . When h o u s e f l y r e s i s t a n c e a p p e a r e d n e a r Rome, I t a l y i n 1947, P r o f e s s o r M i s s i r o l i c o n s i d e r e d t h a t i t was a d i f f e r e n t s u b s p e c i e s w h i c h he named Musca domestica tiberina a t t h e v e r y same t i m e t h a t W i l s o n and L i n d q u i s t i n t h e USDA O r l a n d o l a b o r a t o r y w e r e p r o d u c i n g a r e s i s t a n t s t r a i n f r o m a s u s c e p t i b l e one by l a b o r a t o r y s e l e c t i o n . By 1952 D D T - r e s i s t a n c e had b e e n d e v e l o p e d i n p o p u l a t i o n s o f i m p o r t a n t p e s t s o f a p p l e , c a b b a g e , p o t a t o e s , t o m a t o e s and g r a p e s , b e s i d e s t h e body l o u s e , t h e b e d b u g , two s p e c i e s o f f l e a s , and s e v e r a l species o f mosquitoes (Table I I ) . Table I I . Cabbage Worm Cabbage L o o p e r C o d l i n g Moth Apple PIant-bug Potato Beetle Potato Fleabeetle Diamondback Moth Tomato Hornworm Grape L e a f h o p p e r
D e v e l o p m e n t o f D D T - R e s i s t a n c e , 1946-52. Wis. N.Y. Ohio Wash. N.Y. Ind. Java Fla. Cal.
House F l y Body L o u s e Bed Bug Human F l e a Dog F l e a House M o s q u i t o Salt-marsh Mosquitoes I r r i g a t i o n - w a t e r Mosquitoes E n c e p h a l i t i s Mosquito
Sweden Korea Hawaii Peru Ga. Italy Fla. Cal. Cal.
The mechanism o f r e s i s t a n c e t o DDT i n t h e h o u s e f l y was a t f i r s t t h o u g h t t o be due t o r e d u c e d p e n e t r a t i o n t h r o u g h t h e c u t i c l e , the Swedish r e s i s t a n t f l i e s having a t h i c k e r t a r s a l integument t h a n n o r m a l l a b o r a t o r y s t r a i n s ( 3 ) . I n t e r s t r a i n d i f f e r e n c e s were f o u n d i n t h e t i t e r s o f c y t o c h r o m e o x i d a s e and c h o l i n e s t e r a s e , b u t t h e y b o r e no c o r r e l a t i o n w i t h t h e r e s i s t a n c e . One c h a r a c t e r i s t i c d i d , and t h a t was t h e d e t o x i c a t i v e d e h y d r o c h l o r i n a t i o n t o t h e noni n s e c t i c i d a l m e t a b o l i t e DDE ( F i g . 1 ) ; and t h e enzyme r e s p o n s i b l e , D D T - d e h y d r o c h l o r i n a s e , w h i c h depended on g l u t a t h i o n e f o r a c t i v a t i o n , was i s o l a t e d f r o m r e s i s t a n t s t r a i n s ( 4 ) . A s e c o n d mechanism due t o n e r v e i n s e n s i t i v i t y t o DDT was d i s c o v e r e d i n s e v e r a l h o u s e f l y s t r a i n s ( 5 ) . An a d d i t i o n a l mechanism o f D D T - r e s i s t a n c e f o u n d i n D a n i s h and C a l i f o r n i a n s t r a i n s s e l e c t e d w i t h OP compounds was due t o o x i d a t i o n , w h i c h c o u l d be p u t i n t o e v i d e n c e by t h e a d d i t i o n o f NADH t o m i c r o s o m a l p r e p a r a t i o n s in vitro, o r by a d d i n g t h e mfoi n h i b i t o r sesamex as a s y n e r g i s t in vivo ( 6 ) . The c y c l o d i e n e g r o u p o f o r g a n o c h l o r i n e s was i n t r o d u c e d i n 1948, s t a r t i n g w i t h c h l o r d a n e , t h e n a l d r i n , d i e l d r i n , e n d r i n and t o x a p h e n e , and t h e n h e p t a c h l o r ; BHC was a l r e a d y a v a i l a b l e a t t h e c l o s e o f t h e war. The e x p e r i e n c e w i t h h o u s e f l y c o n t r o l i n t h e M e d i t e r r a n e a n c o u n t r i e s was t h a t D D T - r e s i s t a n c e came i n 2 y e a r s , and t h e s u b s t i t u t i o n o f BHC was f o l l o w e d by B H C - r e s i s t a n c e a y e a r
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
2.
BROWN
Resistance
Mechanisms
against
23
Insecticides
l a t e r ; t h e same t h i n g happened t o t h e c y c l o d i e n e s c h l o r d a n e o r d i e l d r i n , a n d c r o s s - r e s i s t a n c e between BHC a n d t h e c y c l o d i e n e was v i r t u a l l y complete. W i t h i n 10 y e a r s o f t h e i n t r o d u c t i o n o f c y c l o d i e n e s i n t o a g r i c u l t u r e i n 1949, 8 i m p o r t a n t c o t t o n p e s t s h a d gone d e c i s i v e l y r e s i s t a n t t o them, t h e b o l l w e e v i l b e i n g among t h e l a s t t o go ( T a b l e I I I ) . T h i s type o f r e s i s t a n c e developed p a r t i c u l a r l y f a s t i n f l i e s and mosquitoes, w h i l e the A u s t r a l i a n b e e f and wool
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Table
I I I . Development o f C y c l o d i e n e - B H C - R e s i s t a n c e ,
B o l l Weevil C o t t o n Leafworm Cotton Spodoptera Salt-marsh C a t e r p i l l a r Spiny Bollworm Cotton Aphid Cotton Fleahopper Cotton P e r f o r a t o r Sugarcane Froghopper Cabbage L o o p e r
La. Tex. Egypt Cal. Israel SE USA Tex. Cal. Trinidad Ariz.
House F l y Sheep B l o w f l y Body L o u s e Bed Bug German Roach Blue T i c k Cattle Tick Salt-marsh Mosquitoes I-W § Enc. M o s q u i t o e s M a l a r i a Mosquito
1949-58. Sardinia NSW Japan Italy Tex. S. A f r i c a Queensl d Fla. Cal. Nigeria 1
i n d u s t r y n o t a b l y s u f f e r e d from the f a i l u r e o f l i n d a n e and d i e l d r i n t o c o n t r o l t h e sheep b l o w f l y a n d t h e c a t t l e t i c k . The u s e o f a l d r i n a g a i n s t w i r e w o r m s , r o o t w o r m s and r o o t maggots i n t h e s o i l was s o o n r e w a r d e d b y c y c l o d i e n e - r e s i s t a n c e i n 3 w i r e w o r m s p e c i e s , 4 s p e c i e s o f Diabrotica rootworms i n c o r n f i e l d s , and 6 s p e c i e s o f Eylemya r o o t maggots o n o n i o n s , B r a s s i c a s a n d o t h e r v e g e t a b l e c r o p s ( T a b l e I V ) . C y c l o d i e n e - r e s i s t a n c e i s v e r y d e c i s i v e when i t comes, s o t h a t i t s s p r e a d t h r o u g h t h e i n s e c t p o p u l a t i o n c a n be r e a d i l y s e e n , a s f o r example t h a t o f t h e w e s t e r n c o m r o o t w o r m Diabrotica vivgifeva from Nebraska t o the r e s t o f the midwestern s t a t e s b e t w e e n 1961 a n d 1964. Table
IV.
Cyclodiene-Resistance developed
Coleoptera
Conoderus C. Limonius Diabrotica D. D. D.
fallu vespertinus califbimicus virgifera balteata longicomis 11-punctata
Graphognathus leucoloma Hypera postica
in Soil
I n s e c t s , 1955-65
Diptera S.C.
s.c. Wash. Neb. La. S.D. N.C Ala. Utah
Eylemya antiqua brassicae H. liturata H. platura H. floralis H. arambourgi H. Psila rosae Euxesta notata Merodon equestris
Wis. 111. Ont. B.C. Sask. Kenya Ore. Ont. U.K.
The mechanism o f c y c l o d i e n e - r e s i s t a n c e h a s b e e n v e r y d i f f i c u l t to determine. The h y d r o x y l a t i o n o f a l d r i n a n d d i e l d r i n t o a l d r i n g l y c o l a n d d i e l d r i n t r a n s d i o l i s a s l o w p r o c e s s and i s n o t p e c u l i a r t o r e s i s t a n t s t r a i n s , while the increased l i p o i d content
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
PESTICIDE CHEMISTRY IN THE 20TH CENTURY
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24
f r e q u e n t l y noted confers only a s l i g h t l y increased t o l e r a n c e . The most l i k e l y mechanism i s t h e s e q u e s t r a t i o n o f t h e c y c l o d i e n e epox i d e by b i n d i n g w i t h c e l l u l a r p r o t e i n s , t h u s p r o t e c t i n g t h e p r e s y n a p t i c membranes w h i c h a r e t h e i r p r o b a b l e s i t e o f a c t i o n ( 7 ) . L i n d a n e - r e s i s t a n t s t r a i n s a r e c h a r a c t e r i z e d by an i n c r e a s e d d e t o x i c a t i o n , due t o d e h y d r o c h l o r i n a t i o n t o PCCH and t o d i c h l o r o t h i o p h e n o l s , t h e l a t t e r p r o c e s s p u t t i n g SH g r o u p s i n t o t h e m o l e c u l e (8). However, i n c r e a s e d b r e a k d o w n i s p r o b a b l y o n l y o f s e c o n d a r y i m p o r t a n c e , t h e p r i n c i p a l r e s i s t a n c e mechanism b e i n g t h e same as for the cyclodiene i n s e c t i c i d e s . At t h i s t i m e , r e s i s t a n c e t o the organophosphorus insecticides i s o f prime importance. F i r s t a p p e a r i n g i n 1949 i n t h e twos p o t t e d m i t e Tetranyckus urtioae i n greenhouses, w i t h i n the next d e c a d e i t s p r e a d t o 14 s p e c i e s o f t e t r a n y c h i d m i t e s i n f e s t i n g pome and c i t r u s o r c h a r d s , t o 7 s p e c i e s o f a p h i d s , t o f l i e s , m i d g e s and m o s q u i t o e s , and f i n a l l y t o c o c k r o a c h e s ( T a b l e V ) . W a i t i n g i n t h e w i n g s were s t i l l more s e r i o u s O P - r e s i s t a n c e s i n Heliothis c a t e r p i l l a r s on c o t t o n , and i n Tribolium and Sitophilus beetles on s t o r e d g r a i n ( 9 ) . T a b l e V.
Development o f O r g a n o p h o s p h o r u s - R e s i s t a n c e ,
Two-spotted M i t e European S p i d e r - m i t e P a c i f i c ξ McDaniel Mites Citrus Mite Green Peach A p h i d Green A p p l e A p h i d Walnut δ A l f a l f a Aphids
Conn. Ind. Wash. Cal. Wash. Switz l d Cal. f
f
1949-59.
House F l y Coprophagous F l y Lake Midge German Roach House M o s q u i t o I-W Mosquitoes Enc. M o s q u i t o e s
Denmark Congo Fla. Ky. Cameroon Cal. Cal.
The mechanisms o f O P - r e s i s t a n c e i n t h e h o u s e f l y were f o u n d t o d e r i v e not from a decreased o x i d a t i o n o f the t h i o p h o s p h a t e t o the p o w e r f u l p h o s p h a t e a n t i c h o l i n e s t e r a s e , — i n d e e d t h e r e was u s u a l l y a h e i g h t e n e d o x i d a t i o n o f p a r a t h i o n t o paraoxon,for example — , but t o chemical d e g r a d a t i o n o f t h e m o l e c u l a r s t r u c t u r e ( F i g . 2 ) . The mechanism f i r s t t o be d i s c o v e r e d was a p h o s p h a t a s e - t y p e h y d r o l y s i s r e s u l t i n g f r o m t h e g e n e - c o n t r o l l e d c o n v e r s i o n o f an a l i e s t e r a s e f o r w h i c h t h e OP compounds were i n h i b i t o r s , t o an Α-esterase f o r w h i c h t h e s e O P s were s u b s t r a t e s ( 1 0 ) . More i m p o r t a n t , h o w e v e r , was an e n h a n c e d o x i d a t i v e t y p e o f c l e a v a g e o f t h e l e a v i n g g r o u p f r o m t h e p h o s p h o r u s , p r o d u c i n g t h e same m e t a b o l i t e s DPTA o r DPA as t h e e s t e r a s e d i d , b u t b e i n g p u t i n t o e v i d e n c e by t h e a d d i t i o n o f NADH t o m i c r o s o m a l p r e p a r a t i o n s ( 1 1 ) . A t h i r d mechanism was e n h a n c e d d e s a l k y l a t i o n by an a l k y l t r a n s f e r a s e u t i l i z i n g GSH, and f o u n d i n t h e s o l u b l e f r a c t i o n o f homogenates (12). O P - r e s i s t a n t s t r a i n s a l s o u s u a l l y become c h a r a c t e r i z e d by reduced c u t i c u l a r p e n e t r a t i o n , a c h a r a c t e r i s t i c which r e s i s t a n t h o u s e f l i e s u s u a l l y had a l r e a d y g a i n e d a g a i n s t DDT, w h i c h e x t e n d s t o c a r b a m a t e s and p y r e t h r o i d s as w e l l . For r e s i s t a n c e t o malat h i o n , t h e r e i s an a d d i t i o n a l mechanism b a s e d on h y d r o l y s i s o f t h e f
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
2.
BROWN
Resistance
Mechanisms
against
25
Insecticides
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s u c c i n y l e s t e r s i d e - c h a i n (13) b y t h e enzyme l o o s e l y t e r m e d c a r b o x y e s t e r a s e , o r more c o r r e c t l y c a r b o x y l i c - e s t e r h y d r o l a s e . W i t h t h e i n t r o d u c t i o n o f the carbamate i n s e c t i c i d e s i n 1956, r e s i s t a n c e t o c a r b a r y l a p p e a r e d b e t w e e n 1963 a n d 1966 i n a n o r c h a r d l e a f r o l l e r i n New Z e a l a n d , i n t h e c o t t o n l e a f w o r m [Spodoptevd) o f E g y p t , and i n Heliothis viresoens (the s o - c a l l e d tobacco budworm) o n A m e r i c a n c o t t o n ( T a b l e V I ) . R e s i s t a n c e d e v e l o p e d t o OP compounds h a d a l r e a d y g i v e n some c r o s s - t o l e r a n c e t o c a r b a m a t e s Table VI.
R e s i s t a n c e t o C a r b a m a t e s a n d P y r e t h r o i d s , 1958-66.
Carbaryl
Pyrethrins
T o b a c c o Budworm Cotton Spodoptera L i g h t - b r o w n A p p l e Moth
House F l y T o b a c c o Moth Mushroom F l y
Tex. Egypt N.Z.
Sweden Fla. England
and seemed t o p r e d i s p o s e t h e p e s t f o r a more r a p i d d e v e l o p m e n t o f carbamate-resistance. Resistance t o synergized pyrethrins devel oped i n a S w e d i s h h o u s e f l y p o p u l a t i o n j u s t 1 y e a r a f t e r i t h a d b e e n t a k e n o f f a c o n t r o l r e g i m e o f OP compounds f o l l o w i n g a grounding o f o r g a n o c h l o r i n e - r e s i s t a n c e . The mechanism o f c a r b a m a t e - r e s i s t a n c e , f o r m e r l y c o n s i d e r e d t o be e n h a n c e d h y d r o l y s i s ( e . g . c a r b a r y l t o 1 - n a p h t h o l ) , was f o u n d t o d e r i v e almost e x c l u s i v e l y from h y d r o x y l a t i o n a t v a r i o u s p o i n t s on the m o l e c u l e , n o t o n l y t h e a r o m a t i c l e a v i n g group b u t a l s o t h e N - m e t h y l o n t h e c a r b a m a t e ( F i g . 3 ) , a s w e l l a s some d e s m e t h y l a t i o n f o r good measure ( 1 4 ) . P y r e t h r i n - r e s i s t a n c e , a t f i r s t c o n s i d e r e d t o be due t o h y d r o l y s i s o f t h e a l c o h o l - a c i d l i n k a g e , was a l s o f o u n d t o be due t o a n o x i d a t i o n , o c c u r r i n g a t t h e t r a n s m e t h y l group o f the i s o b u t e n y l s i d e - c h a i n o f the chrysanthemic a c i d (15). By 1975, t h e d e v e l o p m e n t o f some t y p e o f r e s i s t a n c e h a d b e e n p r o v e d and r e p o r t e d i n p o p u l a t i o n s o f 268 s p e c i e s o f p e s t a r t h r o pods ( T a b l e V I I ) . O P - r e s i s t a n c e h a d now s p r e a d t o i n v o l v e 85 T a b l e V I I . Numbers o f S p e c i e s w i t h V a r i o u s T y p e s o f R e s i s t a n c e , 1975
Diptera Lepidoptera Hemiptera Acarina Coleoptera Other Orders Total
DDT
Did
OP
Carb
Other
Total
54 17 10 4 10 18 113
77 20 16 8 27 14 162
23 12 20 19 7 4 85
5 6 3 6 3 0 23
3 3 4 8 2 2 22
103 34 42 30 38 21 268
s p e c i e s , and c a r b a m a t e - r e s i s t a n c e t o 23 s p e c i e s . The o r c h a r d a n d g r e e n h o u s e m i t e s , p a r t i c u l a r l y Tetranychus urtiaae, h a d c h a l k e d up s u c h e x o t i c r e s i s t a n c e a s t h o s e t o a z o b e n z e n e , t o t h e d i n i t r o com pound b i n a p a c r y l , t o t h e s u l f u r - c o n t a i n i n g o r g a n o c h l o r i n e s , t o t h e f o r m a m i d i n e s , and even t o o x y t h i o q u i n o x ( M o r e s t a n ) . When t h e
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
PESTICIDE CHEMISTRY IN THE 20TH CENTURY
0, CI
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Oxidation
Dehydrochlorination
* HC-C-CI CI
Figure 1.
Detoxicative mechanisms imparting DDTresistance
Dealkylation
Oxidation Oxidative Cleavage
Hydrolysis
NO2 Figure 2. Detoxicative mechanisms imparting organophosphorus-resistance (e.g. to methyl parathion)
CH
3
I
NH
Dealkylation
I
0 =C 0
Hydroxyjation — Hydrolysis
Figure 3.
Detoxicative mechanisms imparting carhamate-resistance (e.g. to carbaryl)
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
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2.
BROWN
Resistance
Mechanisms
against
insecticides
27
r e p o r t o f t h e FAO w o r k i n g p a r t y o n r e s i s t a n c e i s p u b l i s h e d some t i m e t h i s y e a r , we w i l l l e a r n t h a t o v e r 300 s p e c i e s o f a r t h r o p o d s h a v e d e v e l o p e d some t y p e o f r e s i s t a n c e i n some p a r t o f t h e w o r l d . The e f f e c t o f t h e s e r e s i s t a n c e s h a s b e e n t o d r i v e c h e m i c a l c o n t r o l f r o m one i n s e c t i c i d e t o t h e n e x t . I n most p a r t s o f t h e N i l e d e l t a t h e c o t t o n l e a f w o r m s c a n s t i l l be c o n t r o l l e d b y some OP compound, s u c h a s c h l o r p y r i f o s , s u p p l e m e n t e d where n e c e s s a r y w i t h the i n s e c t growth r e g u l a t o r D i m i l i n . But i n s o u t h e r n T e x a s , Mexico, N i c a r a g u a a n d P e r u t h e m u l t i p l e r e s i s t a n c e s o f t h e t o b a c c o budworm, and t o a l e s s e x t r e m e d e g r e e o f H. zea a n d Spodoptera sunia, h a v e made e v e n 20 i n s e c t i c i d e a p p l i c a t i o n s a s e a s o n q u i t e w o r t h l e s s , and i n d e e d t h e r e i s l e s s damage t o t h e c o t t o n i f no c h e m i c a l s a r e a p p l i e d a t a l l . The o n l y m a t e r i a l s t h a t c a n be r e l i e d u p o n t o k i l l t h e s e m u l t i r e s i s t a n t H. viresoens arethe dichlorovinyl p y r e t h r o i d NRDC-143 a n d t h e H e l i o t h i s n u c l e a r p o l y h e d r o s i s v i r u s . I t w i l l be n o t e d t h a t t h e p r e s s u r e o f e v e n t s , r e p l a c i n g o r g a n o c h l o r i n e s w i t h 0 P s a n d c a r b a m a t e s , and t h e n r e p l a c i n g them w i t h more b i o l o g i c a l - t y p e a g e n t s , c o n f o r m s t o t h e a s p i r a t i o n s o f t h o s e charged w i t h p r o t e c t i n g t h e environment a g a i n s t p o l l u t i o n . ?
O t h e r p l a n t - f e e d i n g i n s e c t s , s u c h a s t h e c a b b a g e l o o p e r , have p i l e d one r e s i s t a n c e u p o n a n o t h e r , s o t h a t we must l o o k t o p h e r o mones a n d c h e m o s t e r i l a n t s f o r t h e i r c o n t r o l . The w e s t e r n c o r n r o o t w o r m h a s now j o i n e d t h e o n i o n maggot i n g o i n g O P - r e s i s t a n t . R e s i s t a n c e problems on p e s t s o f r i c e i n Japan a r e becoming as severe as t h o s e on c o t t o n i n the Americas. Among i n s e c t s a f f e c t i n g man a n d a n i m a l s , t h e t h r e e m a j o r mosquito v e c t o r s o f d i s e a s e a r e making t h e u s u a l r a k e s progress f r o m one r e s i s t a n c e t o a n o t h e r . The m a l a r i a m o s q u i t o Anopheles albimanus h a s gone t h e w h o l e way, t h e r e s i s t a n c e m a i n l y o w i n g t o t h e p r e s s u r e o f a g r i c u l t u r a l i n s e c t i c i d e s on i t s b r e e d i n g p l a c e s , and t h u s m a l a r i a i s i n c r e a s i n g a g a i n i n C e n t r a l A m e r i c a . The m u l t i p l e r e s i s t a n c e i n some s t r a i n s o f Tribolium i s a s e r i o u s blow to the p r e s e r v a t i o n o f world food s u p p l i e s . S u c c e s s i v e r e s i s t a n c e s have d r i v e n c o n t r o l o f the Boophilus c a t t l e t i c k s a l l t h e way t o OP compounds, a n d f r o m them t o c h l o r phenamidine ( c h l o r d i m e f o r m ) ; a l t h o u g h i t has been r e c e n t l y found that carbaryl i se f f e c t i v e i nc a t t l e dips i f synergized with piperonyl butoxide. The t w o - s p o t t e d m i t e h a s gone t h r o u g h a f a n t a s t i c s e q u e n c e o f a c a r i c i d e s , t h e o n l y ones t o w h i c h r e s i s t a n c e has n o t y e t b e e n r e p o r t e d b e i n g P e n t a c a n d t h e o r g a n o - t i n compound Plictran. The p e s t m o s q u i t o Aedes nigromaoulis o f t h e v a s t San J o a q u i n v a l l e y o f C a l i f o r n i a went r e s i s t a n t t o o r g a n o c h l o r i n e s b y 1951, t o p a r a t h i o n b y 1960, t o f e n t h i o n b y 1965, a n d t o c h l o r p y r i f o s ( D u r s b a n ) b y 1970. A t p r e s e n t r e l i a n c e i s p l a c e d on l a r v i c i d a l o i l s , t h e j u v e n i l e - h o r m o n e mimic methoprene ( A l t o s i d ) and t h e i n s e c t growth r e g u l a t o r d i f l u b e n z u r o n ( D i m i l i n ) , — and on b e t t e r management o f s u r p l u s i r r i g a t i o n w a t e r . R e s i d u a l s p r a y s f o r house f l y c o n t r o l , a t f i r s t so s p e c t a c u l a r w i t h t h e o r g a n o c h l o r i n e s , had t o move i n t o t h e OP compounds, w h i c h were t h e n k n o c k e d o u t i n 1
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
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28
PESTICIDE CHEMISTRY IN THE 20TH CENTURY
s u c c e s s i o n by r e s i s t a n c e . The e x p e r i e n c e i n Denmark b e t w e e n 1951 and 1967 was t h a t e a c h OP compound l a s t e d f o r a b o u t 2 y e a r s , end i n g w i t h d i m e t h o a t e , and t h e o n l y way t h a t i t s u s e c o u l d be e x t e n d ed was by p u t t i n g i t i n h o u s e f l y b a i t s i n s t e a d o f r e s i d u a l s p r a y s . I t s h o u l d be c l e a r t o us t h a t t h e d e v e l o p m e n t o f r e s i s t a n c e i s a l w a y s t o be e x p e c t e d t o any i n s e c t i c i d e we may c h o o s e t o a p p l y , but i t i s not i n e v i t a b l e . DDT s t a y e d e f f e c t i v e a g a i n s t t h e E u r o p e a n c o r n b o r e r f o r a t l e a s t 15 y e a r s ( T a b l e V I I I ) and t h e r e a r e s e v e r a l o t h e r e x a m p l e s , i n c l u d i n g d i a z i n o n and t h e w e s t e r n c o r n rootworm i n Nebraska. Some o f t h e s p e c i e s o f b e n e f i c i a l i n s e c t s w h i c h f o r m e r l y s u f f e r e d f r o m i n s e c t i c i d e damage, s u c h as b r a c o n i d p a r a s i t e s , l a d y b e e t l e s , m a y f l y nymphs and h o n e y b e e s , h a v e now d e v e l o p e d c e r t a i n t o l e r a n c e s , w h i l e s e v e r a l o f t h e P h y t o s e i i d m i t e s w h i c h f e e d on t h e p l a n t - f e e d i n g s p i d e r m i t e s a r e b e c o m i n g as r e s i s t a n t as t h e i r p r e y t o OP's and c a r b a m a t e s . Table V I I I .
F a i l u r e s of c e r t a i n i n s e c t s to develop r e s i s t a n c e to c e r t a i n i n s e c t i c i d e s . Field
Eur. Corn Borer F l a . Red S c a l e So. House M o s q u i t o Sugarcane Borer B o l l Weevil W. S p r u c e Budworm W. C o r n Rootworm
DDT parathion Flit-MLO azinphosmethyl malathion mexacarbate diazinon
N. Amer. Cal. Tex. La. W. Tex. Idaho Neb.
1950-65 1951-63
Lab. 34 g e n s 60 g e n ί 6 gen 5 1
1
1964-72 1963-72
T
14 gen* s 1963-73
The t h i n g a b o u t r e s i s t a n c e i s t h a t i t i s i n h e r i t e d , t h a t h i g h l y r e s i s t a n t s t r a i n s s t a y r e s i s t a n t e v e n when r e a r e d f o r g e n e r a t i o n s w i t h o u t e x p o s u r e t o t h e i n s e c t i c i d e , and t h a t t h e y were p r o d u c e d i n t h e f i r s t p l a c e by s u b m i t t i n g n o r m a l s t r a i n s t o t h e p r u n i n g power o f s e l e c t i o n . Thus t h e d e t e r m i n a n t s o f r e s i s t a n c e may be s o u g h t i n t h e genes on t h e chromosomes. The a m a z i n g t h i n g was t h a t r e s i s t a n c e , w h i c h was t h o u g h t a priori t o be due t o a l l e l e s o f a number o f m i n o r genes ( i . e . p o l y f a c t o r i a l ) , t i m e and t i m e a g a i n t u r n e d o u t t o be due t o a s i n g l e d e c i s i v e gene ( i . e . monofactorial). T h i s was f i r s t shown i n 1953 f o r D D T - r e s i s t a n c e i n t h e h o u s e f l y and Drosophila, and i n 1956 f o r O P - r e s i s t a n c e i n t h e Tetranyehus m i t e s . S u b s e q u e n t s t u d i e s on t h e g e n e t i c s o f r e s i s t a n c e i n a v a r i e t y o f s p e c i e s showed t h a t t h e gene a l l e l e s r e s p o n s i b l e f o r O P - r e s i s t a n c e and c a r b a m a t e - r e s i s t a n c e were a l w a y s d o m i n a n t , t h o s e f o r c y c l o d i e n e - r e s i s t a n c e were a l w a y s i n t e r m e d i a t e i n e x p r e s s i o n , w h i l e D D T - r e s i s t a n c e genes t u r n e d o u t t o be d o m i n a n t i n some s p e c i e s and r e c e s s i v e i n o t h e r s ( 1 6 ) . By t h e u t i l i z a t i o n o f m a r k e r s t r a i n s b e a r i n g v i s i b l e m u t a n t s , w h i c h a r e a v a i l a b l e f o r t h e h o u s e f l y and t h e i r p o s i t i o n on t h e 6 chromosomes i n t h a t s p e c i e s (17) i t became p o s s i b l e t o l o c a t e t h e genes r e s p o n s i b l e f o r t h e v a r i o u s D D T - r e s i s t a n c e mechanisms already described (Fig. 4). The r e s i s t a n c e due t o d e h y d r o c h l o r -
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
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BROWN
Resistance
Mechanisms
against
Insecticides
OX
a.
Deh
kdr
X o r Y I Figure 4.
Ε
(DR )
(tin)
II
4
(md)
υ
ΠΖ
31
Location of the genes for various resistances on the chromosomes of the housefly
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
PESTICIDE CHEMISTRY IN THE 20TH CENTURY
i n a t i o n was f o u n d t o be l o c a t e d o n chromosome 2 b e t w e e n t h e mark e r s aristapedia a n d carmine. The hétérozygotes f o r t h i s gene a l l e l e , c a l l e d Deh, h a d h a l f a s much D D T - d e h y d r o c h l o r i n a s e a s t h e r e s i s t a n t homozygotes (18). The gene f o r enhanced m i c r o s o m a l o x i d a t i o n md was f o u n d t o be l i n k e d w i t h m a r k e r s o n chromosome 5, b u t i t c a n n o t y e t be l o c a t e d i n a p r e c i s e p o s i t i o n on t h a t chromo some; a n o t h e r gene f o r o x i d a t i o n i s l o c a t e d a t t h e end o f chromo some 2. The gene f o r r e d u c e d n e r v e s e n s i t i v i t y ( e s s e n t i a l l y k n o c k d o w n - r e s i s t a n c e ) was p r e c i s e l y l o c a t e d o n chromosome 3, a l o n g w i t h t h e gene (tin) f o r r e d u c e d c u t i c u l a r p e n e t r a t i o n . (Cyclo d i e n e - r e s i s t a n c e i n t h e h o u s e f l y i s l o c a t e d o n chromosome 4.) E a c h D D T - r e s i s t a n c e gene compounds w i t h t h e o t h e r s t o p r o d u c e r e s i s t a n c e i n t e n s i t i e s w h i c h a r e t h e m u l t i p l e r a t h e r t h a n t h e sum o f each c o n t r i b u t o r . The D D T - r e s i s t a n c e s i n o t h e r s p e c i e s have t u r n e d o u t t o b e due e i t h e r t o o x i d a t i o n , a s i n Drosophila a n d t h e German c o c k r o a c h , o r t o d e h y d r o c h l o r i n a t i o n w i t h reduced p e n e t r a t i o n added, as i n t h e p i n k b o l l w o r m a n d t h e t r o p i c a l h o u s e m o s q u i t o ( T a b l e 9 ) . I n Heliothis virescens one s t r a i n was c h a r a c t e r i z e d b y d e h y d r o c h l o r i n a t i o n , another by reduced p e n e t r a t i o n (19). T a b l e IX.
Mechanisms o f D D T - R e s i s t a n c e i n t h e H o u s e f l y a n d other Insects.
+
+ +
+
+
Culex tarsalis
+
Culex fatigans
Deh ( I I ) md (V) ox ( I I ) hdr ( I I I ) tin ( I I I )
Pomace fly
1
Dehydrochlorin η Oxidation Oxidation I n s e n s i t i v e Nerve Reduced P e n e t r ' n
Pink Bollworm
Resistance Mechanism
Tobacco Budworm
Housefly Gene
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30
+ +
+
F o r O P - r e s i s t a n c e i n t h e h o u s e f l y , t h e gene t h a t d e t e r m i n e s t h e c o n v e r s i o n o f a l i e s t e r a s e i n t o a n Α-esterase, c a l l e d a , i s l o c a t e d o n chromosome 2 v e r y c l o s e t o t h e Deh gene. O f t h e two genes f o r o x i d a t i o n f o u n d i n O P - r e s i s t a n t s t r a i n s , t h e gene ox (diagnosable by the e p o x i d a t i o n o f a l d r i n t o d i e l d r i n ) i s e v i d e n t l y more i m p o r t a n t t h a n md ( f i r s t f o u n d a s d e t e r m i n i n g a sesamexi n h i b i t e d DDT-resistance). D e s a l k y l a t i o n was f o u n d a t t r i b u t a b l e t o a gene ( c a l l e d g) v e r y c l o s e t o a a n d Deh, a n d many O P - r e s i s t a n t s t r a i n s have a l s o a c q u i r e d t h e r e d u c e d p e n e t r a t i o n gene a l l e l e tin. Thus g e n e t i c s c a n h e l p u s s o r t o u t t h e r e s i s t a n c e mechanisms i n a given r e s i s t a n t s t r a i n o r population. The a b i l i t y t o c l e a v e o f f t h e l e a v i n g g r o u p b y a p r o c e s s p r e s u m a b l y h y d r o l y t i c h a s b e e n d e t e c t e d i n a number o f O P - r e s i s t a n t species (Table X). I n t h e t o b a c c o budworm c l e a r e v i d e n c e f o r OPr e s i s t a n c e b e i n g a s s o c i a t e d w i t h o x i d a t i v e c l e a v a g e was o b t a i n e d from the a c t i o n o f microsomes on t h e p h o s p h o r o t h i o n a t e c h l o r p y r i f o s
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
2.
BROWN
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T a b l e X.
Resistance
Mechanisms
against
31
Insecticides
Mechanisms o f O P - R e s i s t a n c e i n t h e H o u s e f l y a n d other Arthropods.
Oxidation Oxidation Hydrolysis Desalkylation Reduced P e n e t r ' n I n s e n s i t i v e ChE
md (V) ox ( I I ) a (II) g (II) tin ( I I I )
+ + +
(+) +
+
+ +
(+)
+ +
+
as a s u b s t r a t e ( 2 0 ) , w h i l e e v i d e n c e f o r i n c r e a s e d h y d r o l y s i s was o b t a i n e d o n t h e p h o s p h a t e GC-6506 a s a s u b s t r a t e ( 2 1 ) . E v i d e n c e ( 2 2 ) f o r d e s a l k y l a t i o n h a s b e e n f o u n d i n t h e p r e d a c e o u s m i t e Amblyseius fallaois a s w e l l a s i n Heliothis. A mutant c h o l i n e s t e r a s e i n s e n s i t i v e t o OP i n h i b i t i o n was o r i g i n a l l y f o u n d n o t t o be a r e s i s t a n c e mechanism i n t h e h o u s e f l y , b u t t o c h a r a c t e r i z e some r e s i s t a n t s t r a i n s o f Tetranyehus urtieae (23) and most O P - r e s i s t a n t s t r a i n s o f t h e A u s t r a l i a n c a t t l e t i c k (24). I t has r e c e n t l y been f o u n d t o be a mechanism i n t h e sheep b l o w f l y ( 2 5 ) , t h e m a l a r i a m o s q u i t o Anopheles albimanus, and a New Y o r k s t r a i n o f t h e h o u s e f l y (27). So we now u n d e r s t a n d how f i e l d p o p u l a t i o n s a n d l a b o r a t o r y s t r a i n s exposed g e n e r a t i o n a f t e r g e n e r a t i o n t o an i n s e c t i c i d e o r i n s e c t i c i d e s a c c u m u l a t e mutant a l l e l e s making f o r r e s i s t a n c e . I f s u s c e p t i b l e genotypes s t i l l remain i n t h e s t r a i n s , they u s u a l l y r e v e r t s i n c e t h e new r e s i s t a n c e genome, b e i n g a b n o r m a l , g e n e r a l l y does n o t do a s w e l l and i s t h u s c o n s t a n t l y d i l u t e d w i t h i n t h e p o p u l a t i o n o r by i m m i g r a t i o n from o u t s i d e . B u t s t r a i n s and popu l a t i o n s t h a t have r e v e r t e d t o s u s c e p t i b i l i t y r e c o v e r t h e i r r e s i s t a n c e a l m o s t i m m e d i a t e l y when t h e o r i g i n a l i n s e c t i c i d e i s r e a p p l i e d ; i n 1956 t h e D a n i s h h o u s e f l y p o p u l a t i o n s w h i c h h a d r e v e r t e d s i n c e o r g a n o c h l o r i n e s were d i s c o n t i n u e d i n 1951 r e c o v e r e d t h e i r r e s i s t a n c e t o DDT a n d c h l o r d a n e a f t e r j u s t one p a r t i a l l y successful reapplication. The m u l t i r e s i s t a n t s t r a i n s now e x t a n t a l s o show a c e r t a i n cross-tolerance, but not resistance, t o the third-generation i n s e c t i c i d e s such as t h e j u v e n i l e - h o r m o n e mimics and o t h e r s o c a l l e d i n s e c t g r o w t h r e g u l a t o r s , a s was f o u n d i n s t r a i n s o f t h e h o u s e f l y , f l o u r b e e t l e a n d t o b a c c o budworm. Resistance t o the JH m i m i c m e t h o p r e n e and Monsanto-585 h a s b e e n i n d u c e d b y l a b o r a t o r y
s e l e c t i o n o f Culex tarsalis
(28) and Culex pipiens
( 2 9 ) , and t o
Monsanto-585 i n Culex quinquefaseiatus (30). Whatever i n s e c t o r IGR i s c h o s e n , t h e r e s u l t o f e x p o s u r e t o s e l e c t i v e d o s e s i n s u c c e s s i v e g e n e r a t i o n s i s u s u a l l y t h e development o f r e s i s t a n c e , r e p e a t i n g o u r p r e v i o u s e x p e r i e n c e w i t h c h e m o s t e r i l a n t s , and t h e
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
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32
PESTICIDE CHEMISTRY IN THE 20TH CENTURY
same a p p l i e s t o d i f l u b e n z u r o n ( D i m i l i n ) , t h e new c h i t i n s y n t h e t a s e i n h i b i t o r d e r i v e d from u r e a . Now f o r t h e F o r w a r d L o o k , t h e p r o j e c t i o n o f e x p e c t a t i o n s f o r the remainder o f t h i s century. We c a n e x p e c t t h e c o n t i n u e d s p r e a d and a c c u m u l a t i o n o f r e s i s t a n c e s i n d i r e c t p r o p o r t i o n t o o u r u s e o f c h e m i c a l s , w h i c h i n t h e U n i t e d S t a t e s w i l l be organophosphorous, c a r b a m a t e and f o r m a m i d i n e compounds, p r o b a b l y w i t h e n d o s u l f a n , m e t h o x y c h l o r and l i n d a n e among t h e o r g a n o c h l o r i n e s , some p y r e t h r o i d s , and p e r h a p s w i t h d i f l u b e n z u r o n e and some J H m i m i c s among t h e i n s e c t g r o w t h r e g u l a t o r s . S i n c e new c l e a r a n c e s a r e b a r e l y k e e p i n g up w i t h s u s p e n s i o n s , we must make what we h a v e l a s t as l o n g as p o s s i b l e . S p r a y c a l e n d a r s w h i c h c h o o s e t h e l e a s t p e r s i s t e n t o f t h e OP compounds, s u c h as t r i c h l o r f o n , w i l l n o t e x e r t s e l e c t i o n p r e s s u r e f o r so l o n g a p e r i o d a f t e r a p p l i c a t i o n as t h e more p e r s i s t e n t o n e s , and a r e e a s i e r on t h e p r e d a t o r s and p a r a sites. T h i s i s the i n t e n t i o n o f the i n t e g r a t e d c o n t r o l systems now b e i n g d e v e l o p e d and f o l l o w e d . We may h a v e l e a r n e d f r o m t h e e r r o r s o f t h e p a s t t o be s u f f i c i e n t l y n e r v o u s a b o u t o u r t a r g e t p o p u l a t i o n s , e v e r y t i m e we p u t them u n d e r i n s e c t i c i d e p r e s s u r e , t o go t o t h e t r o u b l e o f m o n i t o r i n g t h e i r s u s c e p t i b i l i t y s t a t u s . S t a n d a r d t e s t methods f o r r e s i s t a n c e h a v e been d e v e l o p e d by FAO (31) and by t h e E n t o m o l o g i c a l S o c i e t y o f A m e r i c a (32) f o r many i m p o r t a n t a r t h r o p o d p e s t g r o u p s , and more a r e b e i n g d e v e l o p e d ( T a b l e X I ) . T h e i r s y s t e m a t i c u s e a t r e g u l a r i n t e r v a l s s h o u l d be an i n t e g r a l p a r t o f p e s t management. F o r i n s e c t s o f p u b l i c - h e a l t h i m p o r t a n c e , t e s t methods h a v e been made a v a i l a b l e f o r a l l s p e c i e s g r o u p s by WHO ( 3 3 ) , and t h e s e a r e s y s t e m a t i c a l l y u s e d , l a r g e l y b e c a u s e t h e y a r e s i m p l e t o p e r f o r m and t e s t k i t s a r e a v a i l a b l e t o c a r r y them o u t . I t i s j u s t p o s s i b l e t h a t i n the l a s t quarterc e n t u r y o f t h i s m i l l e n i u m , a g r i c u l t u r e d e p a r t m e n t s o f s t a t e s and n a t i o n s may be s u f f i c i e n t l y w e l l - i n f o r m e d a b o u t t h e o v e r a l l n a t u r e o f t h e r e s i s t a n c e p r o b l e m , t h a t t r o u b l e may be d e t e c t e d when and where i t i s i m m i n e n t and t h e a p p r o p r i a t e change made i n t h e c o n t r o l method b e f o r e i t becomes a r e a l i t y . Table
X I . T e s t methods f o r s u s c e p t i b i l i t y
FAO
Methods
ESA
Eylemya spp. ξ Psila rosae Chilo suppressalis Myzus persicae Nephotettix cincticeps Tribolium oastaneum Spodoptera littorales Cocoa M i r i d s Tetranychid mites
Laspeyresia
pomonella
Leptinotarsa 10-lineata Adult Locusts Luc-ilia larvae $ adults Beetles i n stored cereals
levels to
insecticides.
Methods
Developed
Anthonomus grandis Heliothis zea & viresoens Hypera postica Diabrotica spp. Developing
Conotrachelus
nenuphar
Lygus bugs A n t h o c o r i d bugs Scarabaeid grubs P h y t o s e i i d mites
Plimmer et al.; Pesticide Chemistry in the 20th Century ACS Symposium Series; American Chemical Society: Washington, DC, 1977.
2.
BROWN
Resistance
Mechanisms
against Insecticides
33
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