The Progression of Resistance Mechanisms Developed against

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.


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


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


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




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


2.

BROWN

Resistance

Mechanisms

against

25

Insecticides


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



0, CI


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)



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



28


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 -



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



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


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


2.

BROWN


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



32


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


2.

BROWN

Resistance

Mechanisms

against Insecticides

33

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34

29. 30. 31.


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The Progression of Resistance Mechanisms Developed against

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